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major hurdle in developing new treatments for MSUD has been the lack of a practical, accurate animal model of the disease. This hurdle has now been overcome. In this report, we describe the development and characterization of two genetically engineered mouse models that are phenotypically very similar to MSUD patients with the classic and intermediate forms of the disease.\nOur model of classic MSUD was created by gene knockout of the E2 subunit of BCKDH. The phenotype of these knockout animals is strikingly similar to humans with classic MSUD. Knockout mice were born at the expected frequency and appeared normal at birth. Within a day of birth and following suckling, blood levels of BCAA were markedly elevated. Concomitantly, levels of the amino acids alanine, glutamate, and glutamine, whose synthesis is linked with normal metabolism of BCAA, were decreased (Table 1). The activity of BCKDH in livers of homozygous knockout mouse pups was undetectable, accounting for the accumulation of unmetabolized BCAA. Immunoreactive E2 protein was absent in liver and fibroblasts of homozygous pups. The phenotypic behavior of homozygous mouse pups resembles symptoms seen in newborn classic MSUD patients. These include signs of neurologic dysfunction such as seizures, stupor, lethargy, loss of motor activity, and respiratory difficulties [1]. These neurologic symptoms may result from reduced levels of glutamate, glutamine, alanine, and other similar neuroactive amino acids, which are considered the culprit for MSUD encephalopathies in patients [1,37]. Finally, nearly all of the homozygous pups died within 72 hours of birth. This neonatal lethality is likely due to the accumulation of BCAA to neurotoxic levels, ketoacidosis, brain edema, dehydration, and malnutrition as observed in the MSUD calf [17] and in classic MSUD patients [1]. Heterozygous knockouts were normal and had normal levels of BCAA despite having approximately half of BCKDH enzymatic activity. From the characterization studies completed thus far, the null mutation mouse accurately represents a model of classic MSUD and appears to be a faithful model of the human disease with respect to several biochemical phenotypes [1].\nTo create a model of intermediate MSUD, we used a transgenic strategy to express human E2 in the liver of E2 knockout mice. As mentioned above, E2 knockouts without transgene derived E2 die during the early neonatal period. We show that expression of a human E2 transgene in the liver of these knockout mice is able to rescue the neonatal lethality. Many of the rescue mice survived to adulthood. It is interesting to note that in these mouse lines only ~5–6% of normal BCKDH activity in the liver was sufficient to allow survival. We also demonstrated that BCAA levels in blood of these rescue mice were intermediate between controls and knockouts. The hallmarks of intermediate MSUD human patients are persistently increased levels of BCAA and BCKDH activity in the range of 3–30% of normal [1]. Because of the phenotypic similarities of the rescue mice to the human patients, these genetically engineered mice represent a useful small animal model of the intermediate form of MSUD.\nThe transgenic approach that was used to create the intermediate MSUD model was based on the tetracycline regulated gene switch system that has been used with great success in other studies, for example [34]. The strategy behind our approach was to create mice with an intermediate MSUD phenotype that could be converted to the classic phenotype at the investigator's discretion by turning off the rescuing transgene. However, we were unable to consistently turn off the human E2 expression cassette by the potent tetracycline analogue, doxycycline in either of the two transgenic lines tested (data not shown). The reason these two lines were unresponsive to doxycycline is unknown. It is conceivable that the integration site of the transgenes was not permissive for regulated expression. Screening of additional lines may be needed to find lines that allow for survival and can also be regulated.\nThe models described in this communication are important advances over the previously described models. An ENU mouse resembling human MSUD was previously created by disrupting the mitochondrial BCAT gene [20]. The BCKDH activity in the liver and muscle of this mouse was normal even though the blood BCAA levels were markedly elevated. While this is an interesting model, it is not a true model of MSUD because the mutation is not in BCKDH and the levels of BCKDH are normal. Furthermore, no case of MSUD has been described attributing this disease to BCAT deficiency. In addition to this mouse model, a cow model of MSUD has also been previously described [17-19]. However, due to practical constraints imposed by such a large animal model and due to the observation of differences between the MSUD cow model and MSUD humans [1], this model is also of limited utility. In contrast, the murine models described in this report are more valid and appropriate for modeling human MSUD.\nThe most significant opportunity presented by the MSUD mouse models is to test novel treatments such as gene [38-41] and cell based therapies (e.g., hepatocytes [42,43] or embryonic stem cells [44]). Relevant to gene therapy, recent problems with gene therapy in humans highlight the importance and critical need of animal models of genetic diseases for preclinical studies. The testing of gene and cell based therapies on appropriate animal model systems provides a preliminary method of establishing not only the efficacy, but also short- and long-term safety. Success with animal studies is expected to advance such therapeutic approaches and could pave the way for studies in humans. In addition to testing various treatments, these models should also be very useful for investigating the underlying pathophysiologic consequences of the disease. Such studies are very difficult/impossible to do in human patients for obvious ethical reasons, and often must rely on autopsy tissue. Additionally, the intermediate MSUD model may also be useful for studies to test the effect of thiamin. A thiamin-responsive form of MSUD has been described [1]. The phenotype of these patients is heterogeneous and treatment with a wide range of thiamin doses has produced limited success [1]. Recent cell culture studies with MSUD cells have suggested that the thiamin-responsive phenotype is dependent upon the presence of at least one E2 expressing allele [45,46]. In light of these newer findings, our intermediate MSUD mouse provides a model to test the effect of thiamin with respect to BCKDH activity and blood amino acid levels at the level of the whole animal. Because of recent interest in structural analysis of multienzyme complexes [35,36,45,46], the intermediate MSUD model may provide a valuable resource for studies of structural biology. Lastly, the information and knowledge gained from studies with the MSUD models described here will also be applicable and transferable to other mitochondrial disorders due to defects in multisubunit enzymes."}

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"obj":"NCBITaxon_UBERON_EXT:pup"},{"id":"T19692","span":{"begin":1483,"end":1494},"obj":"CHEBI_SO_EXT:amino_acid"},{"id":"T19691","span":{"begin":1444,"end":1451},"obj":"CHEBI_SO_EXT:alanine"},{"id":"T19690","span":{"begin":1433,"end":1442},"obj":"CHEBI_SO_EXT:glutamine"},{"id":"T19689","span":{"begin":1422,"end":1431},"obj":"CHEBI_EXT:glutamate"},{"id":"T19688","span":{"begin":1368,"end":1378},"obj":"UBERON:0001016"},{"id":"T19687","span":{"begin":1332,"end":1343},"obj":"UBERON:0001004"},{"id":"T19686","span":{"begin":1312,"end":1317},"obj":"GO_EXT:biological_movement_or_translocation_process"},{"id":"T19685","span":{"begin":1245,"end":1255},"obj":"UBERON:0001016"},{"id":"T19684","span":{"begin":1191,"end":1198},"obj":"PATO_UBERON_EXT:neonate_or_newborn"},{"id":"T19683","span":{"begin":1159,"end":1163},"obj":"NCBITaxon_UBERON_EXT:pup"},{"id":"T19682","span":{"begin":1153,"end":1158},"obj":"NCBITaxon:10088"},{"id":"T19681","span":{"begin":1130,"end":1138},"obj":"GO_PATO_EXT:biological_behavior"},{"id":"T19680","span":{"begin":1109,"end":1113},"obj":"NCBITaxon_UBERON_EXT:pup"},{"id":"T19679","span":{"begin":1083,"end":1094},"obj":"CL:0000057"},{"id":"T19678","span":{"begin":1073,"end":1078},"obj":"UBERON:0002107"},{"id":"T19677","span":{"begin":1051,"end":1058},"obj":"CHEBI_PR_EXT:protein"},{"id":"T19676","span":{"begin":1048,"end":1050},"obj":"PR_EXT:000006300"},{"id":"T19675","span":{"begin":1027,"end":1031},"obj":"CHEBI:22918"},{"id":"T19674","span":{"begin":1015,"end":1026},"obj":"GO:0008152"},{"id":"T19673","span":{"begin":955,"end":959},"obj":"NCBITaxon_UBERON_EXT:pup"},{"id":"T19672","span":{"begin":949,"end":954},"obj":"NCBITaxon:10088"},{"id":"T19671","span":{"begin":919,"end":925},"obj":"UBERON:0002107"},{"id":"T19670","span":{"begin":862,"end":866},"obj":"CHEBI:22918"},{"id":"T19669","span":{"begin":848,"end":866},"obj":"GO:0009081"},{"id":"T19668","span":{"begin":799,"end":808},"obj":"CHEBI_SO_EXT:glutamine"},{"id":"T19667","span":{"begin":784,"end":793},"obj":"CHEBI_EXT:glutamate"},{"id":"T19666","span":{"begin":775,"end":782},"obj":"CHEBI_SO_EXT:alanine"},{"id":"T19665","span":{"begin":763,"end":774},"obj":"CHEBI_SO_EXT:amino_acid"},{"id":"T19664","span":{"begin":705,"end":709},"obj":"CHEBI:22918"},{"id":"T19663","span":{"begin":689,"end":694},"obj":"UBERON:0000178"},{"id":"T19662","span":{"begin":679,"end":687},"obj":"GO:0001967"},{"id":"T19661","span":{"begin":659,"end":664},"obj":"GO:0007567"},{"id":"T19660","span":{"begin":636,"end":641},"obj":"GO:0007567"},{"id":"T19659","span":{"begin":582,"end":586},"obj":"GO:0007567"},{"id":"T19658","span":{"begin":572,"end":576},"obj":"NCBITaxon:10088"},{"id":"T19657","span":{"begin":537,"end":543},"obj":"NCBITaxon:9606"},{"id":"T19656","span":{"begin":504,"end":511},"obj":"NCBITaxon:33208"},{"id":"T19655","span":{"begin":451,"end":470},"obj":"PR_EXT:000006300"},{"id":"T19654","span":{"begin":430,"end":434},"obj":"SO_EXT:0000704"},{"id":"T19653","span":{"begin":266,"end":271},"obj":"NCBITaxon:10088"},{"id":"T19652","span":{"begin":243,"end":254},"obj":"SO_EXT:0000704"},{"id":"T19651","span":{"begin":107,"end":113},"obj":"NCBITaxon:33208"}],"text":"Discussion\nA major hurdle in developing new treatments for MSUD has been the lack of a practical, accurate animal model of the disease. This hurdle has now been overcome. In this report, we describe the development and characterization of two genetically engineered mouse models that are phenotypically very similar to MSUD patients with the classic and intermediate forms of the disease.\nOur model of classic MSUD was created by gene knockout of the E2 subunit of BCKDH. The phenotype of these knockout animals is strikingly similar to humans with classic MSUD. Knockout mice were born at the expected frequency and appeared normal at birth. Within a day of birth and following suckling, blood levels of BCAA were markedly elevated. Concomitantly, levels of the amino acids alanine, glutamate, and glutamine, whose synthesis is linked with normal metabolism of BCAA, were decreased (Table 1). The activity of BCKDH in livers of homozygous knockout mouse pups was undetectable, accounting for the accumulation of unmetabolized BCAA. Immunoreactive E2 protein was absent in liver and fibroblasts of homozygous pups. The phenotypic behavior of homozygous mouse pups resembles symptoms seen in newborn classic MSUD patients. These include signs of neurologic dysfunction such as seizures, stupor, lethargy, loss of motor activity, and respiratory difficulties [1]. These neurologic symptoms may result from reduced levels of glutamate, glutamine, alanine, and other similar neuroactive amino acids, which are considered the culprit for MSUD encephalopathies in patients [1,37]. Finally, nearly all of the homozygous pups died within 72 hours of birth. This neonatal lethality is likely due to the accumulation of BCAA to neurotoxic levels, ketoacidosis, brain edema, dehydration, and malnutrition as observed in the MSUD calf [17] and in classic MSUD patients [1]. Heterozygous knockouts were normal and had normal levels of BCAA despite having approximately half of BCKDH enzymatic activity. From the characterization studies completed thus far, the null mutation mouse accurately represents a model of classic MSUD and appears to be a faithful model of the human disease with respect to several biochemical phenotypes [1].\nTo create a model of intermediate MSUD, we used a transgenic strategy to express human E2 in the liver of E2 knockout mice. As mentioned above, E2 knockouts without transgene derived E2 die during the early neonatal period. We show that expression of a human E2 transgene in the liver of these knockout mice is able to rescue the neonatal lethality. Many of the rescue mice survived to adulthood. It is interesting to note that in these mouse lines only ~5–6% of normal BCKDH activity in the liver was sufficient to allow survival. We also demonstrated that BCAA levels in blood of these rescue mice were intermediate between controls and knockouts. The hallmarks of intermediate MSUD human patients are persistently increased levels of BCAA and BCKDH activity in the range of 3–30% of normal [1]. Because of the phenotypic similarities of the rescue mice to the human patients, these genetically engineered mice represent a useful small animal model of the intermediate form of MSUD.\nThe transgenic approach that was used to create the intermediate MSUD model was based on the tetracycline regulated gene switch system that has been used with great success in other studies, for example [34]. The strategy behind our approach was to create mice with an intermediate MSUD phenotype that could be converted to the classic phenotype at the investigator's discretion by turning off the rescuing transgene. However, we were unable to consistently turn off the human E2 expression cassette by the potent tetracycline analogue, doxycycline in either of the two transgenic lines tested (data not shown). The reason these two lines were unresponsive to doxycycline is unknown. It is conceivable that the integration site of the transgenes was not permissive for regulated expression. Screening of additional lines may be needed to find lines that allow for survival and can also be regulated.\nThe models described in this communication are important advances over the previously described models. An ENU mouse resembling human MSUD was previously created by disrupting the mitochondrial BCAT gene [20]. The BCKDH activity in the liver and muscle of this mouse was normal even though the blood BCAA levels were markedly elevated. While this is an interesting model, it is not a true model of MSUD because the mutation is not in BCKDH and the levels of BCKDH are normal. Furthermore, no case of MSUD has been described attributing this disease to BCAT deficiency. In addition to this mouse model, a cow model of MSUD has also been previously described [17-19]. However, due to practical constraints imposed by such a large animal model and due to the observation of differences between the MSUD cow model and MSUD humans [1], this model is also of limited utility. In contrast, the murine models described in this report are more valid and appropriate for modeling human MSUD.\nThe most significant opportunity presented by the MSUD mouse models is to test novel treatments such as gene [38-41] and cell based therapies (e.g., hepatocytes [42,43] or embryonic stem cells [44]). Relevant to gene therapy, recent problems with gene therapy in humans highlight the importance and critical need of animal models of genetic diseases for preclinical studies. The testing of gene and cell based therapies on appropriate animal model systems provides a preliminary method of establishing not only the efficacy, but also short- and long-term safety. Success with animal studies is expected to advance such therapeutic approaches and could pave the way for studies in humans. In addition to testing various treatments, these models should also be very useful for investigating the underlying pathophysiologic consequences of the disease. Such studies are very difficult/impossible to do in human patients for obvious ethical reasons, and often must rely on autopsy tissue. Additionally, the intermediate MSUD model may also be useful for studies to test the effect of thiamin. A thiamin-responsive form of MSUD has been described [1]. The phenotype of these patients is heterogeneous and treatment with a wide range of thiamin doses has produced limited success [1]. Recent cell culture studies with MSUD cells have suggested that the thiamin-responsive phenotype is dependent upon the presence of at least one E2 expressing allele [45,46]. In light of these newer findings, our intermediate MSUD mouse provides a model to test the effect of thiamin with respect to BCKDH activity and blood amino acid levels at the level of the whole animal. Because of recent interest in structural analysis of multienzyme complexes [35,36,45,46], the intermediate MSUD model may provide a valuable resource for studies of structural biology. Lastly, the information and knowledge gained from studies with the MSUD models described here will also be applicable and transferable to other mitochondrial disorders due to defects in multisubunit enzymes."}

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major hurdle in developing new treatments for MSUD has been the lack of a practical, accurate animal model of the disease. This hurdle has now been overcome. In this report, we describe the development and characterization of two genetically engineered mouse models that are phenotypically very similar to MSUD patients with the classic and intermediate forms of the disease.\nOur model of classic MSUD was created by gene knockout of the E2 subunit of BCKDH. The phenotype of these knockout animals is strikingly similar to humans with classic MSUD. Knockout mice were born at the expected frequency and appeared normal at birth. Within a day of birth and following suckling, blood levels of BCAA were markedly elevated. Concomitantly, levels of the amino acids alanine, glutamate, and glutamine, whose synthesis is linked with normal metabolism of BCAA, were decreased (Table 1). The activity of BCKDH in livers of homozygous knockout mouse pups was undetectable, accounting for the accumulation of unmetabolized BCAA. Immunoreactive E2 protein was absent in liver and fibroblasts of homozygous pups. The phenotypic behavior of homozygous mouse pups resembles symptoms seen in newborn classic MSUD patients. These include signs of neurologic dysfunction such as seizures, stupor, lethargy, loss of motor activity, and respiratory difficulties [1]. These neurologic symptoms may result from reduced levels of glutamate, glutamine, alanine, and other similar neuroactive amino acids, which are considered the culprit for MSUD encephalopathies in patients [1,37]. Finally, nearly all of the homozygous pups died within 72 hours of birth. This neonatal lethality is likely due to the accumulation of BCAA to neurotoxic levels, ketoacidosis, brain edema, dehydration, and malnutrition as observed in the MSUD calf [17] and in classic MSUD patients [1]. Heterozygous knockouts were normal and had normal levels of BCAA despite having approximately half of BCKDH enzymatic activity. From the characterization studies completed thus far, the null mutation mouse accurately represents a model of classic MSUD and appears to be a faithful model of the human disease with respect to several biochemical phenotypes [1].\nTo create a model of intermediate MSUD, we used a transgenic strategy to express human E2 in the liver of E2 knockout mice. As mentioned above, E2 knockouts without transgene derived E2 die during the early neonatal period. We show that expression of a human E2 transgene in the liver of these knockout mice is able to rescue the neonatal lethality. Many of the rescue mice survived to adulthood. It is interesting to note that in these mouse lines only ~5–6% of normal BCKDH activity in the liver was sufficient to allow survival. We also demonstrated that BCAA levels in blood of these rescue mice were intermediate between controls and knockouts. The hallmarks of intermediate MSUD human patients are persistently increased levels of BCAA and BCKDH activity in the range of 3–30% of normal [1]. Because of the phenotypic similarities of the rescue mice to the human patients, these genetically engineered mice represent a useful small animal model of the intermediate form of MSUD.\nThe transgenic approach that was used to create the intermediate MSUD model was based on the tetracycline regulated gene switch system that has been used with great success in other studies, for example [34]. The strategy behind our approach was to create mice with an intermediate MSUD phenotype that could be converted to the classic phenotype at the investigator's discretion by turning off the rescuing transgene. However, we were unable to consistently turn off the human E2 expression cassette by the potent tetracycline analogue, doxycycline in either of the two transgenic lines tested (data not shown). The reason these two lines were unresponsive to doxycycline is unknown. It is conceivable that the integration site of the transgenes was not permissive for regulated expression. Screening of additional lines may be needed to find lines that allow for survival and can also be regulated.\nThe models described in this communication are important advances over the previously described models. An ENU mouse resembling human MSUD was previously created by disrupting the mitochondrial BCAT gene [20]. The BCKDH activity in the liver and muscle of this mouse was normal even though the blood BCAA levels were markedly elevated. While this is an interesting model, it is not a true model of MSUD because the mutation is not in BCKDH and the levels of BCKDH are normal. Furthermore, no case of MSUD has been described attributing this disease to BCAT deficiency. In addition to this mouse model, a cow model of MSUD has also been previously described [17-19]. However, due to practical constraints imposed by such a large animal model and due to the observation of differences between the MSUD cow model and MSUD humans [1], this model is also of limited utility. In contrast, the murine models described in this report are more valid and appropriate for modeling human MSUD.\nThe most significant opportunity presented by the MSUD mouse models is to test novel treatments such as gene [38-41] and cell based therapies (e.g., hepatocytes [42,43] or embryonic stem cells [44]). Relevant to gene therapy, recent problems with gene therapy in humans highlight the importance and critical need of animal models of genetic diseases for preclinical studies. The testing of gene and cell based therapies on appropriate animal model systems provides a preliminary method of establishing not only the efficacy, but also short- and long-term safety. Success with animal studies is expected to advance such therapeutic approaches and could pave the way for studies in humans. In addition to testing various treatments, these models should also be very useful for investigating the underlying pathophysiologic consequences of the disease. Such studies are very difficult/impossible to do in human patients for obvious ethical reasons, and often must rely on autopsy tissue. Additionally, the intermediate MSUD model may also be useful for studies to test the effect of thiamin. A thiamin-responsive form of MSUD has been described [1]. The phenotype of these patients is heterogeneous and treatment with a wide range of thiamin doses has produced limited success [1]. Recent cell culture studies with MSUD cells have suggested that the thiamin-responsive phenotype is dependent upon the presence of at least one E2 expressing allele [45,46]. In light of these newer findings, our intermediate MSUD mouse provides a model to test the effect of thiamin with respect to BCKDH activity and blood amino acid levels at the level of the whole animal. Because of recent interest in structural analysis of multienzyme complexes [35,36,45,46], the intermediate MSUD model may provide a valuable resource for studies of structural biology. Lastly, the information and knowledge gained from studies with the MSUD models described here will also be applicable and transferable to other mitochondrial disorders due to defects in multisubunit enzymes."}