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in Trichothiodystrophy by Homozygous Lethal Xpd Alleles\nCompound Heterozygosity at theXpd Locus\n\nAbstract\nAlthough compound heterozygosity, or the presence of two different mutant alleles of the same gene, is common in human recessive disease, its potential to impact disease outcome has not been well documented. This is most likely because of the inherent difficulty in distinguishing specific biallelic effects from differences in environment or genetic background. We addressed the potential of different recessive alleles to contribute to the enigmatic pleiotropy associated with XPD recessive disorders in compound heterozygous mouse models. Alterations in this essential helicase, with functions in both DNA repair and basal transcription, result in diverse pathologies ranging from elevated UV sensitivity and cancer predisposition to accelerated segmental progeria. We report a variety of biallelic effects on organismal phenotype attributable to combinations of recessive Xpd alleles, including the following: (i) the ability of homozygous lethal Xpd alleles to ameliorate a variety of disease symptoms when their essential basal transcription function is supplied by a different disease-causing allele, (ii) differential developmental and tissue-specific functions of distinct Xpd allele products, and (iii) interallelic complementation, a phenomenon rarely reported at clinically relevant loci in mammals. Our data suggest a re-evaluation of the contribution of “null” alleles to XPD disorders and highlight the potential of combinations of recessive alleles to affect both normal and pathological phenotypic plasticity in mammals.\n\nEffects of mutations in Xpd were investigated in mice. Compound heterozygotes of otherwise homozygous lethal alleles demonstrated interallelic complementation and partial phenotypic rescue of XPD-related disease symptoms.\n\nIntroduction\nInterallelic complementation is defined as the ability of two differentially mutated alleles to function better together than either can on its own. Despite its near universality in lower organisms [1], its potential to contribute to clinical heterogeneity in human disease is seldom considered. Evidence of interallelic complementation at clinically relevant loci is limited to biochemical and cell-based studies of a handful of metabolic disorders with defects in enzymes including propinyl-CoA carboxylase [2], argininosuccinate lyase [3], galactose-1-phosphate uridylyltransferase [4], and methylmalonyl CoA mutase [5].\nCompound heterozygotes are individuals carrying two different mutant alleles of the same gene. In the absence of a dominant (wild-type [wt]) allele, genetic interactions between recessive alleles (referred to here as “biallelic” effects) could result in different phenotypic outcomes including interallelic complementation. Although amelioration of disease symptoms by interallelic complementation would create an ascertainment bias in the clinic, the lack of evidence concerning interallelic complementation or other biallelic effects in human disease is likely caused by the difficulty in distinguishing such effects from environment and genetic background.\nXPD encodes one of the two helicase components of basal transcription/DNA repair factor IIH (TFIIH), a ten-subunit, multifunctional complex that is essential for multiple processes, including basal transcription initiation and DNA damage repair via the nucleotide excision repair (NER) pathway [6,7]. Alterations in XPD resulting in defective TFIIH function are associated with UV-sensitive, multisystem disorders including xeroderma pigmentosum (XP), XP combined with Cockayne syndrome (CS), and trichothiodystrophy (TTD) [8–10]. XP is marked by sun-induced pigmentation anomalies and a greater than 1,000-fold elevation in skin cancer risk. Severe cases can also present with growth retardation and primary neurodegeneration [11]. CS and TTD, on the other hand, are segmental progeroid disorders characterised by progressive post-natal growth failure and primary demyelination resulting in severe neurodysfunction, but without a clear cancer predisposition [12–15]. Patients with TTD additionally display hallmark sulphur-deficient brittle hair and nails and scaling skin [13], resulting from a basal transcription defect in specific cell types [16,17]. A related disorder with the cancer predisposition of XP combined with the neurodevelopmental complications of CS (XPCS), although rare, has also been described [18].\nMany XPD mutations are associated with an exclusive disease phenotype (e.g., XPDR722W with TTD and XPDR683W with XP) and are thus viewed as causative of the corresponding syndromes. Alleles not associated exclusively with one disorder are considered “likely null” alleles [19,20]. Some of these alleles fail to support viability in a haploid Schizosaccharomyces pombe yeast strain with a null mutation in the XPD homologue rad15 and are thus considered devoid of significant biological activity [19]. This classification of alleles as either causative or null currently defines what we refer to as a “monoallelic” paradigm of XPD disease. However, the identification in recent years of XP complementation group D patients with atypical disease presentation, including symptoms of both XP and TTD [8], casts doubt on the ability of such a monoallelic paradigm to explain clinical heterogeneity in compound heterozygotes.\nPreviously, we generated a TTD mouse model (XPDR722W) that phenocopies the human syndrome [15,21]. Here we report the generation of additional mutant Xpd alleles that fail to support viability on their own but nevertheless ameliorate TTD-associated premature segmental ageing, cutaneous features, cellular DNA repair capacity, and UV survival when present in a compound heterozygote state.\n\nResults\n\nGeneration of Xpd Compound Heterozygotes\nWe generated an Xpd knock-in allele with a point mutation encoding a single amino acid change (XPDG602D) found in the XPCS patient XPCS2 (Figure 1A–1C). mRNA expression from the targeted allele could be detected in embryonic stem cells by RT-PCR (Figure 1D), although expression was reduced approximately 5-fold relative to wt mRNA transcript levels as determined by Northern blotting of RNA from the testis of heterozygous animals (Figure 1E). Because patient XPCS2 was a hemizygote with mutant XPD protein (XPDG602D) expressed from a single allele, the corresponding mutation was expected to be viable in the homozygous state. However, homozygous mutant mice were not observed, neither amongst live births nor embryonic day 13.5 (E13.5) or E3.5 embryos (Table 1). The corresponding hypomorphic, mutant allele was thus designated as homozygous lethal (†XPCS). Homozygous lethality of the XPCS allele is likely due to reduced levels of expression of this essential protein as a result of gene targeting (Figure 1A) rather than to the mutation itself. Xpd ablation (XpdKO /KO ) is similarly incompatible with life beyond the earliest stages of embryogenesis [22]. Consistent with this interpretation, a different targeted Xpd mutation encoding XPDR683W, which is associated with XP in the homozygous state in humans, was similarly underexpressed and lethal in the homozygous state (designated as †XP allele) (Figure 1A–1C; Table 1; unpublished data). Also, a different targeting approach leading to the use of the native 3′UTR and removal of the neo gene resulted in normalisation of XpdXPCS mRNA levels and viable homozygous XpdXPCS/XPCS (XPDG602D/G602D) animals [23].\nFigure 1 Targeting of the Mouse Xpd Gene\n(A) Schematic representation of the genomic structure and partial restriction map of the wt and targeted mouse Xpd loci. For the wt Xpd allele, shaded boxes represent coding regions of exons 12 and 19–23; the 3′UTR is represented by an open box. TGA indicates the translational stop codon; PolyA indicates the polyadenylation signal. For the XpdTTD targeted allele, the 194–base pair (bp) human XPD cDNA fragment fused to exon 22 is indicated as a striped box including the TTD (R722W) mutation indicated by a vertical arrow. Chicken β-globin exons 2 and 3 including the 3′UTR are indicated as black boxes with corresponding Roman numerals followed by the β-globin polyadenylation signal (PolyA*). For the Xpd†XP and Xpd†XPCS targeted alleles, vertical arrows indicate XPCS (G602D-encoding) and XP (R683W-encoding) mutations in exons 19 and 22, respectively. The unique 3′ probe located outside the targeting construct is marked by a thick black line. Restriction sites: B, BamHI; C, ClaI; E, EcoRI; H, HindIII; Hp, HpaI; Sf, SfiI.\n(B) Southern blot analysis of EcoRI-digested genomic DNA from wt, Xpd†XPCS/wt, and Xpd†XP/wt recombinant embryonic stem cell clones hybridised with the 3′ probe depicted in (A). The wt allele yields a 6.5-kilobase (kb) fragment, whereas both targeted Xpd†XP and Xpd†XPCS alleles yield a 5.1-kb fragment.\n(C) Genotyping of wt and targeted alleles by PCR using primers F2, R1, and mR as indicated in (A) yields fragments of 399 bp and 468 bp, respectively.\n(D) RT-PCR detection of mRNA expression originating from the targeted †XP and †XPCS alleles in embryonic stem cell clones using primers F1 (hybridising outside the targeting construct) and mR as indicated in (A) results in a 1,416-bp fragment.\n(E) Northern blot analysis of total RNA isolated from testis of homozygous wt and XpdTTD/TTD, heterozygous Xpd†XPCS/wt and XpdTTD/wt, and compound heterozygous Xpd†XPCS/TTD mice as indicated. Hybridisation with a 1.4-kb mouse Xpd cDNA probe detects mRNAs of 4, 3.3, and 2.7 kb from wt, Xpd†XPCS, and XpdTTD alleles, respectively. An ethidium bromide (EtBr)–stained gel showing the amount of total RNA loaded is shown below.\nTable 1 Frequency of Xpd†XP/†XP, Xpd†XPCS/†XPCS, and Compound Heterozygous Xpd†XP/†XPCS Embryos and Offspring\n\n“Null” Allele Can Alleviate Developmental Delay, Skin, and Hair Features of TTD\nTo test the potential of a homozygous lethal “null” allele to nevertheless contribute to organismal phenotype, we combined an Xpd†XPCS allele with a viable XpdTTD allele by crossing the corresponding heterozygous animals. Similar to hemizygous TTD mice carrying one true Xpd knockout allele (XpdTTD/KO), compound heterozygous XpdTTD/†XPCS mice were born at the expected Mendelian frequencies. Expression from the Xpd†XPCS allele was also reduced in the testis of compound heterozygous animals, whereas expression from the XpdTTD allele was increased relative to wt by ~5-fold (Figure 1E). Because of a lack of available antibodies and the inability to distinguish amongst various mutant forms of XPD differing only by single amino acid substitutions, we were unable to ascertain the relative amount of XPD protein from the different alleles.\nDespite reduced levels of mRNA expression, the homozygous lethal Xpd†XPCS allele ameliorated multiple XpdTTD-associated disease symptoms in compound heterozygous XpdTTD/†XPCS animals including the hallmark brittle hair and cutaneous features fully penetrant in homo- and hemizygous TTD mice (Figure 2A–2C). In marked contrast to XpdTTD/TTD (and XpdTTD/KO) mice, which display complete hair loss in the first hair cycle and partial hair loss in subsequent cycles throughout their lives [21], compound heterozygous XpdTTD/†XPCS mice displayed some hair loss only during the first hair cycle and only locally at the back (Figure 2A). Scanning electron microscope analysis of XpdTTD/†XPCS hair revealed an almost normal appearance, with TTD-like features such as broken hairs found only at very low frequency (unpublished data). Amino acid analysis confirmed that cysteine levels in the hair of the XpdTTD/†XPCS mice were significantly higher than in XpdTTD/TTD animals, but remained below the wt level (Figure 2C). TTD hemizygotes (XpdTTD/KO) do not display significant differences in cutaneous features and longevity relative to homozygous XpdTTD/TTD mice [21].\nFigure 2 Partial Rescue of TTD Cutaneous, Blood, and Developmental Phenotypes in Compound Heterozygous XpdTTD/†XPCS Mice\n(A) Photographs of 5-mo-old homozygous XpdTTD/TTD, compound heterozygous XpdTTD/†XPCS, and wt mice. Insets: images of first-round hair loss.\n(B) Histological analysis of the skin of XpdTTD/TTD, XpdTTD/†XPCS, and wt mice. TTD-associated acanthosis (thicker epidermis, indicated by solid vertical line), pronounced granular layer (indicated by arrows), and sebacious gland hyperplasia (indicated by dotted vertical line) were absent in the epidermis of XpdTTD/†XPCS and wt mice. Magnification 400×.\n(C) Cysteine content of hair from wt, XpdTTD/TTD, and XpdTTD/†XPCS mice. The p-value indicates significant differences between mutants and wt, as well as between XpdTTD/TTD and XpdTTD/†XPCS mice. Error bars indicate standard error of the mean (SEM).\n(D) Hematocrit values from blood of XpdTTD/TTD and XpdTTD/†XPCS mice. The p-values indicate the significance of the difference relative to wt. Error bars indicate SEM.\n(E) Body weights of developing XpdTTD/TTD and XpdTTD/†XPCS mice after weaning plotted as a percentage of the weight of age-matched control wt and heterozygote (hz) littermates (set at 100%). Error bars indicate SEM. Other prominent TTD features in the epidermis, including acanthosis (thickening of the layer of the nucleated cells), hyperkeratosis (prominent thickening of the cornified layer), and pronounced granular layer and sebacious gland hyperplasia (causing greasy appearance of the hair), were absent in the skin of XpdTTD/†XPCS mice, as established by blind microscopic examination of skin sections (Figure 2B). Furthermore, anaemia and developmental delay present in patients with TTD [24] and in XpdTTD/TTD mice [15] were both partially rescued in compound heterozygous XpdTTD/†XPCS mice (Figure 2D and 2E).\n\nRescue of Progeroid"}

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in Trichothiodystrophy by Homozygous Lethal Xpd Alleles\nCompound Heterozygosity at theXpd Locus\n\nAbstract\nAlthough compound heterozygosity, or the presence of two different mutant alleles of the same gene, is common in human recessive disease, its potential to impact disease outcome has not been well documented. This is most likely because of the inherent difficulty in distinguishing specific biallelic effects from differences in environment or genetic background. We addressed the potential of different recessive alleles to contribute to the enigmatic pleiotropy associated with XPD recessive disorders in compound heterozygous mouse models. Alterations in this essential helicase, with functions in both DNA repair and basal transcription, result in diverse pathologies ranging from elevated UV sensitivity and cancer predisposition to accelerated segmental progeria. We report a variety of biallelic effects on organismal phenotype attributable to combinations of recessive Xpd alleles, including the following: (i) the ability of homozygous lethal Xpd alleles to ameliorate a variety of disease symptoms when their essential basal transcription function is supplied by a different disease-causing allele, (ii) differential developmental and tissue-specific functions of distinct Xpd allele products, and (iii) interallelic complementation, a phenomenon rarely reported at clinically relevant loci in mammals. Our data suggest a re-evaluation of the contribution of “null” alleles to XPD disorders and highlight the potential of combinations of recessive alleles to affect both normal and pathological phenotypic plasticity in mammals.\n\nEffects of mutations in Xpd were investigated in mice. Compound heterozygotes of otherwise homozygous lethal alleles demonstrated interallelic complementation and partial phenotypic rescue of XPD-related disease symptoms.\n\nIntroduction\nInterallelic complementation is defined as the ability of two differentially mutated alleles to function better together than either can on its own. Despite its near universality in lower organisms [1], its potential to contribute to clinical heterogeneity in human disease is seldom considered. Evidence of interallelic complementation at clinically relevant loci is limited to biochemical and cell-based studies of a handful of metabolic disorders with defects in enzymes including propinyl-CoA carboxylase [2], argininosuccinate lyase [3], galactose-1-phosphate uridylyltransferase [4], and methylmalonyl CoA mutase [5].\nCompound heterozygotes are individuals carrying two different mutant alleles of the same gene. In the absence of a dominant (wild-type [wt]) allele, genetic interactions between recessive alleles (referred to here as “biallelic” effects) could result in different phenotypic outcomes including interallelic complementation. Although amelioration of disease symptoms by interallelic complementation would create an ascertainment bias in the clinic, the lack of evidence concerning interallelic complementation or other biallelic effects in human disease is likely caused by the difficulty in distinguishing such effects from environment and genetic background.\nXPD encodes one of the two helicase components of basal transcription/DNA repair factor IIH (TFIIH), a ten-subunit, multifunctional complex that is essential for multiple processes, including basal transcription initiation and DNA damage repair via the nucleotide excision repair (NER) pathway [6,7]. Alterations in XPD resulting in defective TFIIH function are associated with UV-sensitive, multisystem disorders including xeroderma pigmentosum (XP), XP combined with Cockayne syndrome (CS), and trichothiodystrophy (TTD) [8–10]. XP is marked by sun-induced pigmentation anomalies and a greater than 1,000-fold elevation in skin cancer risk. Severe cases can also present with growth retardation and primary neurodegeneration [11]. CS and TTD, on the other hand, are segmental progeroid disorders characterised by progressive post-natal growth failure and primary demyelination resulting in severe neurodysfunction, but without a clear cancer predisposition [12–15]. Patients with TTD additionally display hallmark sulphur-deficient brittle hair and nails and scaling skin [13], resulting from a basal transcription defect in specific cell types [16,17]. A related disorder with the cancer predisposition of XP combined with the neurodevelopmental complications of CS (XPCS), although rare, has also been described [18].\nMany XPD mutations are associated with an exclusive disease phenotype (e.g., XPDR722W with TTD and XPDR683W with XP) and are thus viewed as causative of the corresponding syndromes. Alleles not associated exclusively with one disorder are considered “likely null” alleles [19,20]. Some of these alleles fail to support viability in a haploid Schizosaccharomyces pombe yeast strain with a null mutation in the XPD homologue rad15 and are thus considered devoid of significant biological activity [19]. This classification of alleles as either causative or null currently defines what we refer to as a “monoallelic” paradigm of XPD disease. However, the identification in recent years of XP complementation group D patients with atypical disease presentation, including symptoms of both XP and TTD [8], casts doubt on the ability of such a monoallelic paradigm to explain clinical heterogeneity in compound heterozygotes.\nPreviously, we generated a TTD mouse model (XPDR722W) that phenocopies the human syndrome [15,21]. Here we report the generation of additional mutant Xpd alleles that fail to support viability on their own but nevertheless ameliorate TTD-associated premature segmental ageing, cutaneous features, cellular DNA repair capacity, and UV survival when present in a compound heterozygote state.\n\nResults\n\nGeneration of Xpd Compound Heterozygotes\nWe generated an Xpd knock-in allele with a point mutation encoding a single amino acid change (XPDG602D) found in the XPCS patient XPCS2 (Figure 1A–1C). mRNA expression from the targeted allele could be detected in embryonic stem cells by RT-PCR (Figure 1D), although expression was reduced approximately 5-fold relative to wt mRNA transcript levels as determined by Northern blotting of RNA from the testis of heterozygous animals (Figure 1E). Because patient XPCS2 was a hemizygote with mutant XPD protein (XPDG602D) expressed from a single allele, the corresponding mutation was expected to be viable in the homozygous state. However, homozygous mutant mice were not observed, neither amongst live births nor embryonic day 13.5 (E13.5) or E3.5 embryos (Table 1). The corresponding hypomorphic, mutant allele was thus designated as homozygous lethal (†XPCS). Homozygous lethality of the XPCS allele is likely due to reduced levels of expression of this essential protein as a result of gene targeting (Figure 1A) rather than to the mutation itself. Xpd ablation (XpdKO /KO ) is similarly incompatible with life beyond the earliest stages of embryogenesis [22]. Consistent with this interpretation, a different targeted Xpd mutation encoding XPDR683W, which is associated with XP in the homozygous state in humans, was similarly underexpressed and lethal in the homozygous state (designated as †XP allele) (Figure 1A–1C; Table 1; unpublished data). Also, a different targeting approach leading to the use of the native 3′UTR and removal of the neo gene resulted in normalisation of XpdXPCS mRNA levels and viable homozygous XpdXPCS/XPCS (XPDG602D/G602D) animals [23].\nFigure 1 Targeting of the Mouse Xpd Gene\n(A) Schematic representation of the genomic structure and partial restriction map of the wt and targeted mouse Xpd loci. For the wt Xpd allele, shaded boxes represent coding regions of exons 12 and 19–23; the 3′UTR is represented by an open box. TGA indicates the translational stop codon; PolyA indicates the polyadenylation signal. For the XpdTTD targeted allele, the 194–base pair (bp) human XPD cDNA fragment fused to exon 22 is indicated as a striped box including the TTD (R722W) mutation indicated by a vertical arrow. Chicken β-globin exons 2 and 3 including the 3′UTR are indicated as black boxes with corresponding Roman numerals followed by the β-globin polyadenylation signal (PolyA*). For the Xpd†XP and Xpd†XPCS targeted alleles, vertical arrows indicate XPCS (G602D-encoding) and XP (R683W-encoding) mutations in exons 19 and 22, respectively. The unique 3′ probe located outside the targeting construct is marked by a thick black line. Restriction sites: B, BamHI; C, ClaI; E, EcoRI; H, HindIII; Hp, HpaI; Sf, SfiI.\n(B) Southern blot analysis of EcoRI-digested genomic DNA from wt, Xpd†XPCS/wt, and Xpd†XP/wt recombinant embryonic stem cell clones hybridised with the 3′ probe depicted in (A). The wt allele yields a 6.5-kilobase (kb) fragment, whereas both targeted Xpd†XP and Xpd†XPCS alleles yield a 5.1-kb fragment.\n(C) Genotyping of wt and targeted alleles by PCR using primers F2, R1, and mR as indicated in (A) yields fragments of 399 bp and 468 bp, respectively.\n(D) RT-PCR detection of mRNA expression originating from the targeted †XP and †XPCS alleles in embryonic stem cell clones using primers F1 (hybridising outside the targeting construct) and mR as indicated in (A) results in a 1,416-bp fragment.\n(E) Northern blot analysis of total RNA isolated from testis of homozygous wt and XpdTTD/TTD, heterozygous Xpd†XPCS/wt and XpdTTD/wt, and compound heterozygous Xpd†XPCS/TTD mice as indicated. Hybridisation with a 1.4-kb mouse Xpd cDNA probe detects mRNAs of 4, 3.3, and 2.7 kb from wt, Xpd†XPCS, and XpdTTD alleles, respectively. An ethidium bromide (EtBr)–stained gel showing the amount of total RNA loaded is shown below.\nTable 1 Frequency of Xpd†XP/†XP, Xpd†XPCS/†XPCS, and Compound Heterozygous Xpd†XP/†XPCS Embryos and Offspring\n\n“Null” Allele Can Alleviate Developmental Delay, Skin, and Hair Features of TTD\nTo test the potential of a homozygous lethal “null” allele to nevertheless contribute to organismal phenotype, we combined an Xpd†XPCS allele with a viable XpdTTD allele by crossing the corresponding heterozygous animals. Similar to hemizygous TTD mice carrying one true Xpd knockout allele (XpdTTD/KO), compound heterozygous XpdTTD/†XPCS mice were born at the expected Mendelian frequencies. Expression from the Xpd†XPCS allele was also reduced in the testis of compound heterozygous animals, whereas expression from the XpdTTD allele was increased relative to wt by ~5-fold (Figure 1E). Because of a lack of available antibodies and the inability to distinguish amongst various mutant forms of XPD differing only by single amino acid substitutions, we were unable to ascertain the relative amount of XPD protein from the different alleles.\nDespite reduced levels of mRNA expression, the homozygous lethal Xpd†XPCS allele ameliorated multiple XpdTTD-associated disease symptoms in compound heterozygous XpdTTD/†XPCS animals including the hallmark brittle hair and cutaneous features fully penetrant in homo- and hemizygous TTD mice (Figure 2A–2C). In marked contrast to XpdTTD/TTD (and XpdTTD/KO) mice, which display complete hair loss in the first hair cycle and partial hair loss in subsequent cycles throughout their lives [21], compound heterozygous XpdTTD/†XPCS mice displayed some hair loss only during the first hair cycle and only locally at the back (Figure 2A). Scanning electron microscope analysis of XpdTTD/†XPCS hair revealed an almost normal appearance, with TTD-like features such as broken hairs found only at very low frequency (unpublished data). Amino acid analysis confirmed that cysteine levels in the hair of the XpdTTD/†XPCS mice were significantly higher than in XpdTTD/TTD animals, but remained below the wt level (Figure 2C). TTD hemizygotes (XpdTTD/KO) do not display significant differences in cutaneous features and longevity relative to homozygous XpdTTD/TTD mice [21].\nFigure 2 Partial Rescue of TTD Cutaneous, Blood, and Developmental Phenotypes in Compound Heterozygous XpdTTD/†XPCS Mice\n(A) Photographs of 5-mo-old homozygous XpdTTD/TTD, compound heterozygous XpdTTD/†XPCS, and wt mice. Insets: images of first-round hair loss.\n(B) Histological analysis of the skin of XpdTTD/TTD, XpdTTD/†XPCS, and wt mice. TTD-associated acanthosis (thicker epidermis, indicated by solid vertical line), pronounced granular layer (indicated by arrows), and sebacious gland hyperplasia (indicated by dotted vertical line) were absent in the epidermis of XpdTTD/†XPCS and wt mice. Magnification 400×.\n(C) Cysteine content of hair from wt, XpdTTD/TTD, and XpdTTD/†XPCS mice. The p-value indicates significant differences between mutants and wt, as well as between XpdTTD/TTD and XpdTTD/†XPCS mice. Error bars indicate standard error of the mean (SEM).\n(D) Hematocrit values from blood of XpdTTD/TTD and XpdTTD/†XPCS mice. The p-values indicate the significance of the difference relative to wt. Error bars indicate SEM.\n(E) Body weights of developing XpdTTD/TTD and XpdTTD/†XPCS mice after weaning plotted as a percentage of the weight of age-matched control wt and heterozygote (hz) littermates (set at 100%). Error bars indicate SEM. Other prominent TTD features in the epidermis, including acanthosis (thickening of the layer of the nucleated cells), hyperkeratosis (prominent thickening of the cornified layer), and pronounced granular layer and sebacious gland hyperplasia (causing greasy appearance of the hair), were absent in the skin of XpdTTD/†XPCS mice, as established by blind microscopic examination of skin sections (Figure 2B). Furthermore, anaemia and developmental delay present in patients with TTD [24] and in XpdTTD/TTD mice [15] were both partially rescued in compound heterozygous XpdTTD/†XPCS mice (Figure 2D and 2E).\n\nRescue of Progeroid"}

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in Trichothiodystrophy by Homozygous Lethal Xpd Alleles\nCompound Heterozygosity at theXpd Locus\n\nAbstract\nAlthough compound heterozygosity, or the presence of two different mutant alleles of the same gene, is common in human recessive disease, its potential to impact disease outcome has not been well documented. This is most likely because of the inherent difficulty in distinguishing specific biallelic effects from differences in environment or genetic background. We addressed the potential of different recessive alleles to contribute to the enigmatic pleiotropy associated with XPD recessive disorders in compound heterozygous mouse models. Alterations in this essential helicase, with functions in both DNA repair and basal transcription, result in diverse pathologies ranging from elevated UV sensitivity and cancer predisposition to accelerated segmental progeria. We report a variety of biallelic effects on organismal phenotype attributable to combinations of recessive Xpd alleles, including the following: (i) the ability of homozygous lethal Xpd alleles to ameliorate a variety of disease symptoms when their essential basal transcription function is supplied by a different disease-causing allele, (ii) differential developmental and tissue-specific functions of distinct Xpd allele products, and (iii) interallelic complementation, a phenomenon rarely reported at clinically relevant loci in mammals. Our data suggest a re-evaluation of the contribution of “null” alleles to XPD disorders and highlight the potential of combinations of recessive alleles to affect both normal and pathological phenotypic plasticity in mammals.\n\nEffects of mutations in Xpd were investigated in mice. Compound heterozygotes of otherwise homozygous lethal alleles demonstrated interallelic complementation and partial phenotypic rescue of XPD-related disease symptoms.\n\nIntroduction\nInterallelic complementation is defined as the ability of two differentially mutated alleles to function better together than either can on its own. Despite its near universality in lower organisms [1], its potential to contribute to clinical heterogeneity in human disease is seldom considered. Evidence of interallelic complementation at clinically relevant loci is limited to biochemical and cell-based studies of a handful of metabolic disorders with defects in enzymes including propinyl-CoA carboxylase [2], argininosuccinate lyase [3], galactose-1-phosphate uridylyltransferase [4], and methylmalonyl CoA mutase [5].\nCompound heterozygotes are individuals carrying two different mutant alleles of the same gene. In the absence of a dominant (wild-type [wt]) allele, genetic interactions between recessive alleles (referred to here as “biallelic” effects) could result in different phenotypic outcomes including interallelic complementation. Although amelioration of disease symptoms by interallelic complementation would create an ascertainment bias in the clinic, the lack of evidence concerning interallelic complementation or other biallelic effects in human disease is likely caused by the difficulty in distinguishing such effects from environment and genetic background.\nXPD encodes one of the two helicase components of basal transcription/DNA repair factor IIH (TFIIH), a ten-subunit, multifunctional complex that is essential for multiple processes, including basal transcription initiation and DNA damage repair via the nucleotide excision repair (NER) pathway [6,7]. Alterations in XPD resulting in defective TFIIH function are associated with UV-sensitive, multisystem disorders including xeroderma pigmentosum (XP), XP combined with Cockayne syndrome (CS), and trichothiodystrophy (TTD) [8–10]. XP is marked by sun-induced pigmentation anomalies and a greater than 1,000-fold elevation in skin cancer risk. Severe cases can also present with growth retardation and primary neurodegeneration [11]. CS and TTD, on the other hand, are segmental progeroid disorders characterised by progressive post-natal growth failure and primary demyelination resulting in severe neurodysfunction, but without a clear cancer predisposition [12–15]. Patients with TTD additionally display hallmark sulphur-deficient brittle hair and nails and scaling skin [13], resulting from a basal transcription defect in specific cell types [16,17]. A related disorder with the cancer predisposition of XP combined with the neurodevelopmental complications of CS (XPCS), although rare, has also been described [18].\nMany XPD mutations are associated with an exclusive disease phenotype (e.g., XPDR722W with TTD and XPDR683W with XP) and are thus viewed as causative of the corresponding syndromes. Alleles not associated exclusively with one disorder are considered “likely null” alleles [19,20]. Some of these alleles fail to support viability in a haploid Schizosaccharomyces pombe yeast strain with a null mutation in the XPD homologue rad15 and are thus considered devoid of significant biological activity [19]. This classification of alleles as either causative or null currently defines what we refer to as a “monoallelic” paradigm of XPD disease. However, the identification in recent years of XP complementation group D patients with atypical disease presentation, including symptoms of both XP and TTD [8], casts doubt on the ability of such a monoallelic paradigm to explain clinical heterogeneity in compound heterozygotes.\nPreviously, we generated a TTD mouse model (XPDR722W) that phenocopies the human syndrome [15,21]. Here we report the generation of additional mutant Xpd alleles that fail to support viability on their own but nevertheless ameliorate TTD-associated premature segmental ageing, cutaneous features, cellular DNA repair capacity, and UV survival when present in a compound heterozygote state.\n\nResults\n\nGeneration of Xpd Compound Heterozygotes\nWe generated an Xpd knock-in allele with a point mutation encoding a single amino acid change (XPDG602D) found in the XPCS patient XPCS2 (Figure 1A–1C). mRNA expression from the targeted allele could be detected in embryonic stem cells by RT-PCR (Figure 1D), although expression was reduced approximately 5-fold relative to wt mRNA transcript levels as determined by Northern blotting of RNA from the testis of heterozygous animals (Figure 1E). Because patient XPCS2 was a hemizygote with mutant XPD protein (XPDG602D) expressed from a single allele, the corresponding mutation was expected to be viable in the homozygous state. However, homozygous mutant mice were not observed, neither amongst live births nor embryonic day 13.5 (E13.5) or E3.5 embryos (Table 1). The corresponding hypomorphic, mutant allele was thus designated as homozygous lethal (†XPCS). Homozygous lethality of the XPCS allele is likely due to reduced levels of expression of this essential protein as a result of gene targeting (Figure 1A) rather than to the mutation itself. Xpd ablation (XpdKO /KO ) is similarly incompatible with life beyond the earliest stages of embryogenesis [22]. Consistent with this interpretation, a different targeted Xpd mutation encoding XPDR683W, which is associated with XP in the homozygous state in humans, was similarly underexpressed and lethal in the homozygous state (designated as †XP allele) (Figure 1A–1C; Table 1; unpublished data). Also, a different targeting approach leading to the use of the native 3′UTR and removal of the neo gene resulted in normalisation of XpdXPCS mRNA levels and viable homozygous XpdXPCS/XPCS (XPDG602D/G602D) animals [23].\nFigure 1 Targeting of the Mouse Xpd Gene\n(A) Schematic representation of the genomic structure and partial restriction map of the wt and targeted mouse Xpd loci. For the wt Xpd allele, shaded boxes represent coding regions of exons 12 and 19–23; the 3′UTR is represented by an open box. TGA indicates the translational stop codon; PolyA indicates the polyadenylation signal. For the XpdTTD targeted allele, the 194–base pair (bp) human XPD cDNA fragment fused to exon 22 is indicated as a striped box including the TTD (R722W) mutation indicated by a vertical arrow. Chicken β-globin exons 2 and 3 including the 3′UTR are indicated as black boxes with corresponding Roman numerals followed by the β-globin polyadenylation signal (PolyA*). For the Xpd†XP and Xpd†XPCS targeted alleles, vertical arrows indicate XPCS (G602D-encoding) and XP (R683W-encoding) mutations in exons 19 and 22, respectively. The unique 3′ probe located outside the targeting construct is marked by a thick black line. Restriction sites: B, BamHI; C, ClaI; E, EcoRI; H, HindIII; Hp, HpaI; Sf, SfiI.\n(B) Southern blot analysis of EcoRI-digested genomic DNA from wt, Xpd†XPCS/wt, and Xpd†XP/wt recombinant embryonic stem cell clones hybridised with the 3′ probe depicted in (A). The wt allele yields a 6.5-kilobase (kb) fragment, whereas both targeted Xpd†XP and Xpd†XPCS alleles yield a 5.1-kb fragment.\n(C) Genotyping of wt and targeted alleles by PCR using primers F2, R1, and mR as indicated in (A) yields fragments of 399 bp and 468 bp, respectively.\n(D) RT-PCR detection of mRNA expression originating from the targeted †XP and †XPCS alleles in embryonic stem cell clones using primers F1 (hybridising outside the targeting construct) and mR as indicated in (A) results in a 1,416-bp fragment.\n(E) Northern blot analysis of total RNA isolated from testis of homozygous wt and XpdTTD/TTD, heterozygous Xpd†XPCS/wt and XpdTTD/wt, and compound heterozygous Xpd†XPCS/TTD mice as indicated. Hybridisation with a 1.4-kb mouse Xpd cDNA probe detects mRNAs of 4, 3.3, and 2.7 kb from wt, Xpd†XPCS, and XpdTTD alleles, respectively. An ethidium bromide (EtBr)–stained gel showing the amount of total RNA loaded is shown below.\nTable 1 Frequency of Xpd†XP/†XP, Xpd†XPCS/†XPCS, and Compound Heterozygous Xpd†XP/†XPCS Embryos and Offspring\n\n“Null” Allele Can Alleviate Developmental Delay, Skin, and Hair Features of TTD\nTo test the potential of a homozygous lethal “null” allele to nevertheless contribute to organismal phenotype, we combined an Xpd†XPCS allele with a viable XpdTTD allele by crossing the corresponding heterozygous animals. Similar to hemizygous TTD mice carrying one true Xpd knockout allele (XpdTTD/KO), compound heterozygous XpdTTD/†XPCS mice were born at the expected Mendelian frequencies. Expression from the Xpd†XPCS allele was also reduced in the testis of compound heterozygous animals, whereas expression from the XpdTTD allele was increased relative to wt by ~5-fold (Figure 1E). Because of a lack of available antibodies and the inability to distinguish amongst various mutant forms of XPD differing only by single amino acid substitutions, we were unable to ascertain the relative amount of XPD protein from the different alleles.\nDespite reduced levels of mRNA expression, the homozygous lethal Xpd†XPCS allele ameliorated multiple XpdTTD-associated disease symptoms in compound heterozygous XpdTTD/†XPCS animals including the hallmark brittle hair and cutaneous features fully penetrant in homo- and hemizygous TTD mice (Figure 2A–2C). In marked contrast to XpdTTD/TTD (and XpdTTD/KO) mice, which display complete hair loss in the first hair cycle and partial hair loss in subsequent cycles throughout their lives [21], compound heterozygous XpdTTD/†XPCS mice displayed some hair loss only during the first hair cycle and only locally at the back (Figure 2A). Scanning electron microscope analysis of XpdTTD/†XPCS hair revealed an almost normal appearance, with TTD-like features such as broken hairs found only at very low frequency (unpublished data). Amino acid analysis confirmed that cysteine levels in the hair of the XpdTTD/†XPCS mice were significantly higher than in XpdTTD/TTD animals, but remained below the wt level (Figure 2C). TTD hemizygotes (XpdTTD/KO) do not display significant differences in cutaneous features and longevity relative to homozygous XpdTTD/TTD mice [21].\nFigure 2 Partial Rescue of TTD Cutaneous, Blood, and Developmental Phenotypes in Compound Heterozygous XpdTTD/†XPCS Mice\n(A) Photographs of 5-mo-old homozygous XpdTTD/TTD, compound heterozygous XpdTTD/†XPCS, and wt mice. Insets: images of first-round hair loss.\n(B) Histological analysis of the skin of XpdTTD/TTD, XpdTTD/†XPCS, and wt mice. TTD-associated acanthosis (thicker epidermis, indicated by solid vertical line), pronounced granular layer (indicated by arrows), and sebacious gland hyperplasia (indicated by dotted vertical line) were absent in the epidermis of XpdTTD/†XPCS and wt mice. Magnification 400×.\n(C) Cysteine content of hair from wt, XpdTTD/TTD, and XpdTTD/†XPCS mice. The p-value indicates significant differences between mutants and wt, as well as between XpdTTD/TTD and XpdTTD/†XPCS mice. Error bars indicate standard error of the mean (SEM).\n(D) Hematocrit values from blood of XpdTTD/TTD and XpdTTD/†XPCS mice. The p-values indicate the significance of the difference relative to wt. Error bars indicate SEM.\n(E) Body weights of developing XpdTTD/TTD and XpdTTD/†XPCS mice after weaning plotted as a percentage of the weight of age-matched control wt and heterozygote (hz) littermates (set at 100%). Error bars indicate SEM. Other prominent TTD features in the epidermis, including acanthosis (thickening of the layer of the nucleated cells), hyperkeratosis (prominent thickening of the cornified layer), and pronounced granular layer and sebacious gland hyperplasia (causing greasy appearance of the hair), were absent in the skin of XpdTTD/†XPCS mice, as established by blind microscopic examination of skin sections (Figure 2B). Furthermore, anaemia and developmental delay present in patients with TTD [24] and in XpdTTD/TTD mice [15] were both partially rescued in compound heterozygous XpdTTD/†XPCS mice (Figure 2D and 2E).\n\nRescue of Progeroid"}

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This is most likely because of the inherent difficulty in distinguishing specific biallelic effects from differences in environment or genetic background. We addressed the potential of different recessive alleles to contribute to the enigmatic pleiotropy associated with XPD recessive disorders in compound heterozygous mouse models. Alterations in this essential helicase, with functions in both DNA repair and basal transcription, result in diverse pathologies ranging from elevated UV sensitivity and cancer predisposition to accelerated segmental progeria. We report a variety of biallelic effects on organismal phenotype attributable to combinations of recessive Xpd alleles, including the following: (i) the ability of homozygous lethal Xpd alleles to ameliorate a variety of disease symptoms when their essential basal transcription function is supplied by a different disease-causing allele, (ii) differential developmental and tissue-specific functions of distinct Xpd allele products, and (iii) interallelic complementation, a phenomenon rarely reported at clinically relevant loci in mammals. Our data suggest a re-evaluation of the contribution of “null” alleles to XPD disorders and highlight the potential of combinations of recessive alleles to affect both normal and pathological phenotypic plasticity in mammals.\n\nEffects of mutations in Xpd were investigated in mice. Compound heterozygotes of otherwise homozygous lethal alleles demonstrated interallelic complementation and partial phenotypic rescue of XPD-related disease symptoms.\n\nIntroduction\nInterallelic complementation is defined as the ability of two differentially mutated alleles to function better together than either can on its own. Despite its near universality in lower organisms [1], its potential to contribute to clinical heterogeneity in human disease is seldom considered. Evidence of interallelic complementation at clinically relevant loci is limited to biochemical and cell-based studies of a handful of metabolic disorders with defects in enzymes including propinyl-CoA carboxylase [2], argininosuccinate lyase [3], galactose-1-phosphate uridylyltransferase [4], and methylmalonyl CoA mutase [5].\nCompound heterozygotes are individuals carrying two different mutant alleles of the same gene. In the absence of a dominant (wild-type [wt]) allele, genetic interactions between recessive alleles (referred to here as “biallelic” effects) could result in different phenotypic outcomes including interallelic complementation. Although amelioration of disease symptoms by interallelic complementation would create an ascertainment bias in the clinic, the lack of evidence concerning interallelic complementation or other biallelic effects in human disease is likely caused by the difficulty in distinguishing such effects from environment and genetic background.\nXPD encodes one of the two helicase components of basal transcription/DNA repair factor IIH (TFIIH), a ten-subunit, multifunctional complex that is essential for multiple processes, including basal transcription initiation and DNA damage repair via the nucleotide excision repair (NER) pathway [6,7]. Alterations in XPD resulting in defective TFIIH function are associated with UV-sensitive, multisystem disorders including xeroderma pigmentosum (XP), XP combined with Cockayne syndrome (CS), and trichothiodystrophy (TTD) [8–10]. XP is marked by sun-induced pigmentation anomalies and a greater than 1,000-fold elevation in skin cancer risk. Severe cases can also present with growth retardation and primary neurodegeneration [11]. CS and TTD, on the other hand, are segmental progeroid disorders characterised by progressive post-natal growth failure and primary demyelination resulting in severe neurodysfunction, but without a clear cancer predisposition [12–15]. Patients with TTD additionally display hallmark sulphur-deficient brittle hair and nails and scaling skin [13], resulting from a basal transcription defect in specific cell types [16,17]. A related disorder with the cancer predisposition of XP combined with the neurodevelopmental complications of CS (XPCS), although rare, has also been described [18].\nMany XPD mutations are associated with an exclusive disease phenotype (e.g., XPDR722W with TTD and XPDR683W with XP) and are thus viewed as causative of the corresponding syndromes. Alleles not associated exclusively with one disorder are considered “likely null” alleles [19,20]. Some of these alleles fail to support viability in a haploid Schizosaccharomyces pombe yeast strain with a null mutation in the XPD homologue rad15 and are thus considered devoid of significant biological activity [19]. This classification of alleles as either causative or null currently defines what we refer to as a “monoallelic” paradigm of XPD disease. However, the identification in recent years of XP complementation group D patients with atypical disease presentation, including symptoms of both XP and TTD [8], casts doubt on the ability of such a monoallelic paradigm to explain clinical heterogeneity in compound heterozygotes.\nPreviously, we generated a TTD mouse model (XPDR722W) that phenocopies the human syndrome [15,21]. Here we report the generation of additional mutant Xpd alleles that fail to support viability on their own but nevertheless ameliorate TTD-associated premature segmental ageing, cutaneous features, cellular DNA repair capacity, and UV survival when present in a compound heterozygote state.\n\nResults\n\nGeneration of Xpd Compound Heterozygotes\nWe generated an Xpd knock-in allele with a point mutation encoding a single amino acid change (XPDG602D) found in the XPCS patient XPCS2 (Figure 1A–1C). mRNA expression from the targeted allele could be detected in embryonic stem cells by RT-PCR (Figure 1D), although expression was reduced approximately 5-fold relative to wt mRNA transcript levels as determined by Northern blotting of RNA from the testis of heterozygous animals (Figure 1E). Because patient XPCS2 was a hemizygote with mutant XPD protein (XPDG602D) expressed from a single allele, the corresponding mutation was expected to be viable in the homozygous state. However, homozygous mutant mice were not observed, neither amongst live births nor embryonic day 13.5 (E13.5) or E3.5 embryos (Table 1). The corresponding hypomorphic, mutant allele was thus designated as homozygous lethal (†XPCS). Homozygous lethality of the XPCS allele is likely due to reduced levels of expression of this essential protein as a result of gene targeting (Figure 1A) rather than to the mutation itself. Xpd ablation (XpdKO /KO ) is similarly incompatible with life beyond the earliest stages of embryogenesis [22]. Consistent with this interpretation, a different targeted Xpd mutation encoding XPDR683W, which is associated with XP in the homozygous state in humans, was similarly underexpressed and lethal in the homozygous state (designated as †XP allele) (Figure 1A–1C; Table 1; unpublished data). Also, a different targeting approach leading to the use of the native 3′UTR and removal of the neo gene resulted in normalisation of XpdXPCS mRNA levels and viable homozygous XpdXPCS/XPCS (XPDG602D/G602D) animals [23].\nFigure 1 Targeting of the Mouse Xpd Gene\n(A) Schematic representation of the genomic structure and partial restriction map of the wt and targeted mouse Xpd loci. For the wt Xpd allele, shaded boxes represent coding regions of exons 12 and 19–23; the 3′UTR is represented by an open box. TGA indicates the translational stop codon; PolyA indicates the polyadenylation signal. For the XpdTTD targeted allele, the 194–base pair (bp) human XPD cDNA fragment fused to exon 22 is indicated as a striped box including the TTD (R722W) mutation indicated by a vertical arrow. Chicken β-globin exons 2 and 3 including the 3′UTR are indicated as black boxes with corresponding Roman numerals followed by the β-globin polyadenylation signal (PolyA*). For the Xpd†XP and Xpd†XPCS targeted alleles, vertical arrows indicate XPCS (G602D-encoding) and XP (R683W-encoding) mutations in exons 19 and 22, respectively. The unique 3′ probe located outside the targeting construct is marked by a thick black line. Restriction sites: B, BamHI; C, ClaI; E, EcoRI; H, HindIII; Hp, HpaI; Sf, SfiI.\n(B) Southern blot analysis of EcoRI-digested genomic DNA from wt, Xpd†XPCS/wt, and Xpd†XP/wt recombinant embryonic stem cell clones hybridised with the 3′ probe depicted in (A). The wt allele yields a 6.5-kilobase (kb) fragment, whereas both targeted Xpd†XP and Xpd†XPCS alleles yield a 5.1-kb fragment.\n(C) Genotyping of wt and targeted alleles by PCR using primers F2, R1, and mR as indicated in (A) yields fragments of 399 bp and 468 bp, respectively.\n(D) RT-PCR detection of mRNA expression originating from the targeted †XP and †XPCS alleles in embryonic stem cell clones using primers F1 (hybridising outside the targeting construct) and mR as indicated in (A) results in a 1,416-bp fragment.\n(E) Northern blot analysis of total RNA isolated from testis of homozygous wt and XpdTTD/TTD, heterozygous Xpd†XPCS/wt and XpdTTD/wt, and compound heterozygous Xpd†XPCS/TTD mice as indicated. Hybridisation with a 1.4-kb mouse Xpd cDNA probe detects mRNAs of 4, 3.3, and 2.7 kb from wt, Xpd†XPCS, and XpdTTD alleles, respectively. An ethidium bromide (EtBr)–stained gel showing the amount of total RNA loaded is shown below.\nTable 1 Frequency of Xpd†XP/†XP, Xpd†XPCS/†XPCS, and Compound Heterozygous Xpd†XP/†XPCS Embryos and Offspring\n\n“Null” Allele Can Alleviate Developmental Delay, Skin, and Hair Features of TTD\nTo test the potential of a homozygous lethal “null” allele to nevertheless contribute to organismal phenotype, we combined an Xpd†XPCS allele with a viable XpdTTD allele by crossing the corresponding heterozygous animals. Similar to hemizygous TTD mice carrying one true Xpd knockout allele (XpdTTD/KO), compound heterozygous XpdTTD/†XPCS mice were born at the expected Mendelian frequencies. Expression from the Xpd†XPCS allele was also reduced in the testis of compound heterozygous animals, whereas expression from the XpdTTD allele was increased relative to wt by ~5-fold (Figure 1E). Because of a lack of available antibodies and the inability to distinguish amongst various mutant forms of XPD differing only by single amino acid substitutions, we were unable to ascertain the relative amount of XPD protein from the different alleles.\nDespite reduced levels of mRNA expression, the homozygous lethal Xpd†XPCS allele ameliorated multiple XpdTTD-associated disease symptoms in compound heterozygous XpdTTD/†XPCS animals including the hallmark brittle hair and cutaneous features fully penetrant in homo- and hemizygous TTD mice (Figure 2A–2C). In marked contrast to XpdTTD/TTD (and XpdTTD/KO) mice, which display complete hair loss in the first hair cycle and partial hair loss in subsequent cycles throughout their lives [21], compound heterozygous XpdTTD/†XPCS mice displayed some hair loss only during the first hair cycle and only locally at the back (Figure 2A). Scanning electron microscope analysis of XpdTTD/†XPCS hair revealed an almost normal appearance, with TTD-like features such as broken hairs found only at very low frequency (unpublished data). Amino acid analysis confirmed that cysteine levels in the hair of the XpdTTD/†XPCS mice were significantly higher than in XpdTTD/TTD animals, but remained below the wt level (Figure 2C). TTD hemizygotes (XpdTTD/KO) do not display significant differences in cutaneous features and longevity relative to homozygous XpdTTD/TTD mice [21].\nFigure 2 Partial Rescue of TTD Cutaneous, Blood, and Developmental Phenotypes in Compound Heterozygous XpdTTD/†XPCS Mice\n(A) Photographs of 5-mo-old homozygous XpdTTD/TTD, compound heterozygous XpdTTD/†XPCS, and wt mice. Insets: images of first-round hair loss.\n(B) Histological analysis of the skin of XpdTTD/TTD, XpdTTD/†XPCS, and wt mice. TTD-associated acanthosis (thicker epidermis, indicated by solid vertical line), pronounced granular layer (indicated by arrows), and sebacious gland hyperplasia (indicated by dotted vertical line) were absent in the epidermis of XpdTTD/†XPCS and wt mice. Magnification 400×.\n(C) Cysteine content of hair from wt, XpdTTD/TTD, and XpdTTD/†XPCS mice. The p-value indicates significant differences between mutants and wt, as well as between XpdTTD/TTD and XpdTTD/†XPCS mice. Error bars indicate standard error of the mean (SEM).\n(D) Hematocrit values from blood of XpdTTD/TTD and XpdTTD/†XPCS mice. The p-values indicate the significance of the difference relative to wt. Error bars indicate SEM.\n(E) Body weights of developing XpdTTD/TTD and XpdTTD/†XPCS mice after weaning plotted as a percentage of the weight of age-matched control wt and heterozygote (hz) littermates (set at 100%). Error bars indicate SEM. Other prominent TTD features in the epidermis, including acanthosis (thickening of the layer of the nucleated cells), hyperkeratosis (prominent thickening of the cornified layer), and pronounced granular layer and sebacious gland hyperplasia (causing greasy appearance of the hair), were absent in the skin of XpdTTD/†XPCS mice, as established by blind microscopic examination of skin sections (Figure 2B). Furthermore, anaemia and developmental delay present in patients with TTD [24] and in XpdTTD/TTD mice [15] were both partially rescued in compound heterozygous XpdTTD/†XPCS mice (Figure 2D and 2E).\n\nRescue of Progeroid"}