Conserved genetic programs in insect and mammalian brain development

Hirth, Frank; Reichert, Heinrich

doi:10.1002/(sici)1521-1878(199908)21:8<677::aid-bies7>3.0.co;2-8

Cited by 134 publications

(32 citation statements)

References 58 publications

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“…The problem is that although they do mediate A/P patterning of the CNS in bilaterians [45,46], they mediate A/P patterning of other tissues as well [47-54]. Thus, while their expression patterns have been used to infer homologies between the CNS in insects and vertebrates, it remains possible that they patterned the entire body axis of the Urbilaterian and were independently coopted into the CNSs of protostomes and deuterostomes.…”

Section: Reviewmentioning

confidence: 99%

“…Thus, Reichert and colleagues used gene expression patterns to support the perhaps surprising idea that the three parts of the Drosophila brain – protocerebrum, deutocerebrum and tritocerebrum [5,45] – are homologous to the forebrain, midbrain and hindbrain of vertebrates (Figure 2) [60]. For example, in D. melanogaster , the Otx homolog Otd is expressed throughout the protocerebrum and deutocerebrum, while unpg (homologous to Gbx ) is expressed in the tritocerebrum, the subesophageal ganglion and the ventral nerve cord [5].…”

Section: Reviewmentioning

confidence: 99%

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Evolution of bilaterian central nervous systems: a single origin?

Holland

Carvalho

Escrivà

et al. 2013

EvoDevo

156

214

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The question of whether the ancestral bilaterian had a central nervous system (CNS) or a diffuse ectodermal nervous system has been hotly debated. Considerable evidence supports the theory that a CNS evolved just once. However, an alternative view proposes that the chordate CNS evolved from the ectodermal nerve net of a hemichordate-like ancestral deuterostome, implying independent evolution of the CNS in chordates and protostomes. To specify morphological divisions along the anterior/posterior axis, this ancestor used gene networks homologous to those patterning three organizing centers in the vertebrate brain: the anterior neural ridge, the zona limitans intrathalamica and the isthmic organizer, and subsequent evolution of the vertebrate brain involved elaboration of these ancestral signaling centers; however, all or part of these signaling centers were lost from the CNS of invertebrate chordates. The present review analyzes the evidence for and against these theories. The bulk of the evidence indicates that a CNS evolved just once – in the ancestral bilaterian. Importantly, in both protostomes and deuterostomes, the CNS represents a portion of a generally neurogenic ectoderm that is internalized and receives and integrates inputs from sensory cells in the remainder of the ectoderm. The expression patterns of genes involved in medio/lateral (dorso/ventral) patterning of the CNS are similar in protostomes and chordates; however, these genes are not similarly expressed in the ectoderm outside the CNS. Thus, their expression is a better criterion for CNS homologs than the expression of anterior/posterior patterning genes, many of which (for example, Hox genes) are similarly expressed both in the CNS and in the remainder of the ectoderm in many bilaterians. The evidence leaves hemichordates in an ambiguous position – either CNS centralization was lost to some extent at the base of the hemichordates, or even earlier, at the base of the hemichordates + echinoderms, or one of the two hemichordate nerve cords is homologous to the CNS of protostomes and chordates. In any event, the presence of part of the genetic machinery for the anterior neural ridge, the zona limitans intrathalamica and the isthmic organizer in invertebrate chordates together with similar morphology indicates that these organizers were present, at least in part, at the base of the chordates and were probably elaborated upon in the vertebrate lineage.

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Section: Reviewmentioning

confidence: 99%

Section: Reviewmentioning

confidence: 99%

Evolution of bilaterian central nervous systems: a single origin?

Holland

Carvalho

Escrivà

et al. 2013

EvoDevo

156

214

View full text Add to dashboard Cite

show abstract

“…al. These data indicate that aspects of the genetic mechanisms underlying anterior development are evolutionarily conserved, and have led to Otx being considered an essential participant in A/P axis formation in all metazoan phyla, except possibly echinoderms (Hirth and Reichert 1999;Issacs et al 1999;Kammermeier and Reichert 2001;Adachi et al 2001). All but echinoderms share anterior ectodermal expression domains, and studies in Drosophila, ascidians, and mouse demonstrate Otx functions in patterning the insect and chordate brain Acampora et al 1998;Nagao et al 1998;Acampora and Simone 1999;Adachi et al 2001).…”

Section: Introductionmentioning

confidence: 99%

Evolutionary convergence in Otx expression in the pentameral adult rudiment in direct-developing sea urchins

et al. 2003

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Convergence is a significant evolutionary phenomenon. Arrival at similar morphologies from different starting points indicates a strong role for natural selection in shaping morphological phenotypes. There is no evidence yet of convergence in the developmental mechanisms that underlie the evolution of convergent developmental phenotypes. Here we report the expression domains in sea urchins of two important developmental regulatory genes (Orthodenticle and Runt), and show evidence of molecular convergence in the evolution of direct-developing sea urchins. Indirect development is ancestral in sea urchins. Evolutionary loss of the feeding pluteus stage and precocious formation of the radially symmetric juvenile has evolved independently in numerous sea urchin lineages, thus direct development is an evolutionary convergence. Indirect-developing species do not express Otx during the formation of their five primordial tube feet, the ancestral condition. However, each direct-developing urchin examined does express Otx in the tube feet. Otx expression in the radial arms of direct-developing sea urchins is thus convergent, and may indicate a specific need for Otx use in direct development, a constraint that would make direct development less able to evolve than if there were multiple molecular means for it to evolve. In contrast, Runt is expressed in tube feet in both direct-and indirect-developing species. Because echinoderms are closely related to chordates and postdate the protostome/deuterostome divergence, they must have evolved from bilaterally symmetrical ancestors. Arthropods and chordates use Otx in patterning their anterior axis, and Runt has multiple roles including embryonic patterning in arthropods, and blood and bone cell differentiation in vertebrates. Runt has apparently been co-opted in echinoderms for patterning of pentamery, and Otx in pentameral patterning among direct-developing echinoids. The surprisingly dynamic nature of Otx evolution reinvigorates debate on the role of natural selection vs shared ancestry in the evolution of novel features.

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“…Drawings after Arendt and Nübler-Jung (1996) and used with permission of John Wiley & Sons. B: schematic block-diagram representation of lateral views of the brains of fly and mouse to compare gene expression patters regionally, based on Hirth and Reichert (1999) [see also Hirth et al (1998)]. As in A, otd/Otx gene expression is limited to the forebrain regions in both, and Hox/Hoxb family genes are expressed in the hindbrain, in the same sequence and pattern regarding the rostral-most limit of the domain for each gene.…”

Section: Insect Brain Organizationmentioning

confidence: 99%