PMC:4429232 / 9186-14630 JSONTXT

{"project":"0_colil","denotations":[{"id":"26029038-18927580-565800","span":{"begin":314,"end":318},"obj":"18927580"},{"id":"26029038-24998387-565801","span":{"begin":338,"end":342},"obj":"24998387"},{"id":"26029038-18927580-565802","span":{"begin":1041,"end":1045},"obj":"18927580"},{"id":"26029038-24998387-565803","span":{"begin":1065,"end":1069},"obj":"24998387"},{"id":"26029038-12142278-565804","span":{"begin":1205,"end":1209},"obj":"12142278"},{"id":"26029038-21183788-565805","span":{"begin":1861,"end":1865},"obj":"21183788"},{"id":"26029038-24948391-565806","span":{"begin":1884,"end":1888},"obj":"24948391"},{"id":"26029038-17726517-565807","span":{"begin":1991,"end":1995},"obj":"17726517"},{"id":"26029038-22414251-565808","span":{"begin":2014,"end":2018},"obj":"22414251"},{"id":"26029038-21701143-565809","span":{"begin":2165,"end":2169},"obj":"21701143"},{"id":"26029038-17533671-565810","span":{"begin":2323,"end":2327},"obj":"17533671"},{"id":"26029038-24105342-565811","span":{"begin":2343,"end":2347},"obj":"24105342"},{"id":"26029038-25417155-565812","span":{"begin":2361,"end":2365},"obj":"25417155"},{"id":"26029038-2760266-565813","span":{"begin":4121,"end":4125},"obj":"2760266"},{"id":"26029038-1683805-565814","span":{"begin":4358,"end":4362},"obj":"1683805"},{"id":"26029038-8097979-565815","span":{"begin":4364,"end":4368},"obj":"8097979"},{"id":"26029038-11784017-565816","span":{"begin":4467,"end":4471},"obj":"11784017"},{"id":"26029038-11585802-565817","span":{"begin":4491,"end":4495},"obj":"11585802"},{"id":"26029038-18832334-565818","span":{"begin":4997,"end":5001},"obj":"18832334"}],"text":"Models of transition from a three to a six layered cortex\nThe study of the organization of genes underlying cell identity suggests that genes sub-serving specific functions can be grouped into modules whose expression is regulated by a limited number of transcription factors also called “selector genes” (Arendt, 2008; Achim and Arendt, 2014). In this model, during development morphogens regulate patterning by inducing the expression of the selector genes at specific times and place. Starting from these considerations, three major mechanisms have been recently proposed to underlie the evolution of new cell types from a precursor cell in a given lineage: (1) Divergence of functions, in which two sister cell types inherit the same gene modules and gradually modify them with time, (2) Segregation of functions, in which two sister cell types lose complementary parts of the gene modules of the former precursor cells. (3) Co-option of functions, in which the precursor cell co-opts the gene modules of an unrelated cell type (Arendt, 2008; Achim and Arendt, 2014). It is to note that the term co-option generally refers to the acquisition of new roles by pre-existing characters (True and Carroll, 2002). In the specific case of the gene regulatory networks controlling cell type specification, co-option may occur for cis- and trans- acting transcriptional regulators at multiple levels and can thus be involved in all the presented modes of cell type evolution. Nonetheless, for the co-option of functions hypothesis these mechanisms should act at the level of selector genes, thus leading to the ectopic expression of the pre-existent gene regulatory networks of complex developmental programs. This latter possibility has been proposed to explain multiple evolutionary innovations such as the evolution of novel sex determining genes (Sutton et al., 2011; Takehana et al., 2014) or the acquisition of a chondrogenic fate in the neural crest lineage (Meulemans and Bronner-Fraser, 2007; Hall and Gillis, 2013).\nThe specification of neocortical neurons depends on spatial patterning events delimiting the DP progenitors (Figure 1A; see for review Puelles, 2011), followed by temporal patterning mechanisms that lead these cells to sequentially produce the DL (first) and UL (last) (Figure 1C; Angevine and Sidman, 1961; Greig et al., 2013; Gao et al., 2014). When applying the above mentioned concepts to the evolution of the neocortical neurons, three main hypotheses can be drawn (Figure 1D): (1) Simple Expansion: DP progenitors of the reptilian ancestors produced homologous of both UL and DL neocortical neurons following the same temporal patterning mechanisms as in the modern neocortex. In this model the emergence of the neocortex was driven by changes only in the proliferation of DP progenitors and migration of their daughter cells. (2) Expansion and Segregation: gene modules underlying specific functions of UL and DL were present in a single precursor cell in the ancestral DP derivatives and became segregated and subsequently refined in distinct sister cell types. In this case the temporal patterning of DP progenitors will be a mammalian innovation. (3) Spatial to Temporal patterning switch: DP progenitors co-opted the expression of gene modules specifying the neuronal types of other pallial regions (i.e., MP, VP or LP), thus leading to the appearance of new cell types in the DP derivatives. The temporal patterning of neocortical progenitors may thus represent a patchwork of formerly spatially segregated developmental programs. In this case part of the neocortical cells may have a sister cell type in a different pallial domain.\nSome evidences against the first two hypotheses were first presented by Ebner based on hodological considerations (Ebner, 1976). Indeed, reptilian dorsal cortex neurons have projections to subcortical targets that resemble those of neocortical DL neurons but lack the extensive network of intracortical connections, including homotopic contralateral projections, that are typical of UL neurons (Ebner, 1976; Desan, 1984; Hoogland and Vermeulen-Vanderzee, 1989). Thus, Ebner proposed that the UL neurons may represent an evolutionary novelty. In the early'90 Anton Reiner extended Ebner hypotheses by showing that UL specific interneurons are lacking from the reptilian dorsal cortex (Reiner, 1991, 1993). However, later studies showed that interneurons are generated in the sub-pallium (Cobos et al., 2001; Wichterle et al., 2001) and this makes the Reneir's observations only indirectly related to the DP progenitors developmental program. In 2009 we described a specific population of neurons of the layer II of the neocortex that according with Ebner and Reiner ideas was absent from the dorsal cortex of Lacerta Muralis, a lizard. However, virtually identical cell types were observed in the LP and VP derivatives of both lizard and mammals thus supporting the spatial to temporal patterning switch hypothesis (Luzzati et al., 2009). The interest about these cells comes from the fact that (1) they express Tbr1, suggesting a pallial origin, and (2) morphological and distributive features support that they represent a specific neuronal population that is shared by different pallial derivatives and tetrapod species. In the following sections we will describe and discuss in detail our observations in the context of more recent data that further support these hypotheses."}

{"project":"2_test","denotations":[{"id":"26029038-18927580-38462706","span":{"begin":314,"end":318},"obj":"18927580"},{"id":"26029038-24998387-38462707","span":{"begin":338,"end":342},"obj":"24998387"},{"id":"26029038-18927580-38462708","span":{"begin":1041,"end":1045},"obj":"18927580"},{"id":"26029038-24998387-38462709","span":{"begin":1065,"end":1069},"obj":"24998387"},{"id":"26029038-12142278-38462710","span":{"begin":1205,"end":1209},"obj":"12142278"},{"id":"26029038-21183788-38462711","span":{"begin":1861,"end":1865},"obj":"21183788"},{"id":"26029038-24948391-38462712","span":{"begin":1884,"end":1888},"obj":"24948391"},{"id":"26029038-17726517-38462713","span":{"begin":1991,"end":1995},"obj":"17726517"},{"id":"26029038-22414251-38462714","span":{"begin":2014,"end":2018},"obj":"22414251"},{"id":"26029038-21701143-38462715","span":{"begin":2165,"end":2169},"obj":"21701143"},{"id":"26029038-17533671-38462716","span":{"begin":2323,"end":2327},"obj":"17533671"},{"id":"26029038-24105342-38462717","span":{"begin":2343,"end":2347},"obj":"24105342"},{"id":"26029038-25417155-38462718","span":{"begin":2361,"end":2365},"obj":"25417155"},{"id":"26029038-2760266-38462719","span":{"begin":4121,"end":4125},"obj":"2760266"},{"id":"26029038-1683805-38462720","span":{"begin":4358,"end":4362},"obj":"1683805"},{"id":"26029038-8097979-38462721","span":{"begin":4364,"end":4368},"obj":"8097979"},{"id":"26029038-11784017-38462722","span":{"begin":4467,"end":4471},"obj":"11784017"},{"id":"26029038-11585802-38462723","span":{"begin":4491,"end":4495},"obj":"11585802"},{"id":"26029038-18832334-38462724","span":{"begin":4997,"end":5001},"obj":"18832334"}],"text":"Models of transition from a three to a six layered cortex\nThe study of the organization of genes underlying cell identity suggests that genes sub-serving specific functions can be grouped into modules whose expression is regulated by a limited number of transcription factors also called “selector genes” (Arendt, 2008; Achim and Arendt, 2014). In this model, during development morphogens regulate patterning by inducing the expression of the selector genes at specific times and place. Starting from these considerations, three major mechanisms have been recently proposed to underlie the evolution of new cell types from a precursor cell in a given lineage: (1) Divergence of functions, in which two sister cell types inherit the same gene modules and gradually modify them with time, (2) Segregation of functions, in which two sister cell types lose complementary parts of the gene modules of the former precursor cells. (3) Co-option of functions, in which the precursor cell co-opts the gene modules of an unrelated cell type (Arendt, 2008; Achim and Arendt, 2014). It is to note that the term co-option generally refers to the acquisition of new roles by pre-existing characters (True and Carroll, 2002). In the specific case of the gene regulatory networks controlling cell type specification, co-option may occur for cis- and trans- acting transcriptional regulators at multiple levels and can thus be involved in all the presented modes of cell type evolution. Nonetheless, for the co-option of functions hypothesis these mechanisms should act at the level of selector genes, thus leading to the ectopic expression of the pre-existent gene regulatory networks of complex developmental programs. This latter possibility has been proposed to explain multiple evolutionary innovations such as the evolution of novel sex determining genes (Sutton et al., 2011; Takehana et al., 2014) or the acquisition of a chondrogenic fate in the neural crest lineage (Meulemans and Bronner-Fraser, 2007; Hall and Gillis, 2013).\nThe specification of neocortical neurons depends on spatial patterning events delimiting the DP progenitors (Figure 1A; see for review Puelles, 2011), followed by temporal patterning mechanisms that lead these cells to sequentially produce the DL (first) and UL (last) (Figure 1C; Angevine and Sidman, 1961; Greig et al., 2013; Gao et al., 2014). When applying the above mentioned concepts to the evolution of the neocortical neurons, three main hypotheses can be drawn (Figure 1D): (1) Simple Expansion: DP progenitors of the reptilian ancestors produced homologous of both UL and DL neocortical neurons following the same temporal patterning mechanisms as in the modern neocortex. In this model the emergence of the neocortex was driven by changes only in the proliferation of DP progenitors and migration of their daughter cells. (2) Expansion and Segregation: gene modules underlying specific functions of UL and DL were present in a single precursor cell in the ancestral DP derivatives and became segregated and subsequently refined in distinct sister cell types. In this case the temporal patterning of DP progenitors will be a mammalian innovation. (3) Spatial to Temporal patterning switch: DP progenitors co-opted the expression of gene modules specifying the neuronal types of other pallial regions (i.e., MP, VP or LP), thus leading to the appearance of new cell types in the DP derivatives. The temporal patterning of neocortical progenitors may thus represent a patchwork of formerly spatially segregated developmental programs. In this case part of the neocortical cells may have a sister cell type in a different pallial domain.\nSome evidences against the first two hypotheses were first presented by Ebner based on hodological considerations (Ebner, 1976). Indeed, reptilian dorsal cortex neurons have projections to subcortical targets that resemble those of neocortical DL neurons but lack the extensive network of intracortical connections, including homotopic contralateral projections, that are typical of UL neurons (Ebner, 1976; Desan, 1984; Hoogland and Vermeulen-Vanderzee, 1989). Thus, Ebner proposed that the UL neurons may represent an evolutionary novelty. In the early'90 Anton Reiner extended Ebner hypotheses by showing that UL specific interneurons are lacking from the reptilian dorsal cortex (Reiner, 1991, 1993). However, later studies showed that interneurons are generated in the sub-pallium (Cobos et al., 2001; Wichterle et al., 2001) and this makes the Reneir's observations only indirectly related to the DP progenitors developmental program. In 2009 we described a specific population of neurons of the layer II of the neocortex that according with Ebner and Reiner ideas was absent from the dorsal cortex of Lacerta Muralis, a lizard. However, virtually identical cell types were observed in the LP and VP derivatives of both lizard and mammals thus supporting the spatial to temporal patterning switch hypothesis (Luzzati et al., 2009). The interest about these cells comes from the fact that (1) they express Tbr1, suggesting a pallial origin, and (2) morphological and distributive features support that they represent a specific neuronal population that is shared by different pallial derivatives and tetrapod species. In the following sections we will describe and discuss in detail our observations in the context of more recent data that further support these hypotheses."}