Neurodevelopment Genes in Lampreys Reveal Trends for Forebrain Evolution in Craniates

Abstract

The forebrain is the brain region which has undergone the most dramatic changes through vertebrate evolution. Analyses conducted in lampreys are essential to gain insight into the broad ancestral characteristics of the forebrain at the dawn of vertebrates, and to understand the molecular basis for the diversifications that have taken place in cyclostomes and gnathostomes following their splitting. Here, we report the embryonic expression patterns of 43 lamprey genes, coding for transcription factors or signaling molecules known to be involved in cell proliferation, stemcellness, neurogenesis, patterning and regionalization in the developing forebrain. Systematic expression patterns comparisons with model organisms highlight conservations likely to reflect shared features present in the vertebrate ancestors. They also point to changes in signaling systems –pathways which control the growth and patterning of the neuroepithelium-, which may have been crucial in the evolution of forebrain anatomy at the origin of vertebrates.

Molecular characterization of prosomeric and intraprosomeric subdivisions of the embryonic zebrafish diencephalon

“…Basal forebrain expression of the Shh ortholog, lamprey Hha, shows a dorsal deflection in the mid-diencephalon consistent with the existence of a zli or p2/ p3 boundary (Os orio et al, 2005). This is supported by expression of the proliferation marker PCNA, which displays a discontinuity at this position (Guerin et al, 2009). A region with halted mitosis is a characteristic trait for signaling centers like the Shh-positive zli.…”

“…In recent years a growing body of neuroanatomical and comparative gene expression data have become available for lamprey consistent with a prosomeric diencephalic organization (Pombal and Puelles, 1999;Murakami et al, 2002Murakami et al, , 2005Pombal et al, 2009;Guerin et al, 2009). As in gnathostomes, combined Pax6 and Pax3/7 expression defines a pretectal territory in lampreys (Murakami et al, 2001;Os orio et al, 2005;Guerin et al, 2009). Basal forebrain expression of the Shh ortholog, lamprey Hha, shows a dorsal deflection in the mid-diencephalon consistent with the existence of a zli or p2/ p3 boundary (Os orio et al, 2005).…”

High Mobility Group Box-1 (HMGB1; Amphoterin) Is Required for Zebrafish Brain Development

“…Previous in situ hybridization studies have shown that during organogenesis,HMGB1 mRNA accumulates in early brain structures in many nonvertebrate species, such as amphioxus (12) and Xenopus (13) and the basal vertebrate lamprey (11). In vertebrates, a high expression level of HMGB1 (amphoterin) has been demonstrated in embryonic rat brain compared with the adult brain (6), and mapping studies using in situ hybridization have shown that during organogenesis in zebrafish HMGB1 is essentially a nervous system protein that is abundantly expressed in brain (see The Zebrafish Model Organism Database).…”

The ancestral role of nodal signalling in breaking L/R symmetry in the vertebrate forebrain

“…The P. marinus PmOtxB probe was obtained by degenerate RT-PCR starting from stage 24 to 28 prolarval cDNAs, cloned into the pTZ19U vector and characterized by sequencing using the universal primers M13_pUC_rev and M13_pUC_fwd. ScPitx2, ScKctd12a, ScKctd12b, ScLeftyB and PmLefty probes were obtained from collections of embryonic S. canicula or prolarval P. marinus cDNA recombinants, characterized by Sanger sequencing and described in refs 43,46. Cloning of the ScGfi1, ScKctd8 and PmKctd12 gene fragment and riboprobe synthesis are described in Supplementary Table 4.…”