Organisation of the lamprey (Lampetra fluviatilis) embryonic brain: Insights from LIM-homeodomain, Pax and hedgehog genes

Abstract

To investigate the embryonic development of the central nervous system of the lamprey Lampetra fluviatilis, we have isolated and analysed the expression patterns of members of the LIM-homeodomain, Pax, Hedgehog and Nkx2.1 families. Using degenerate RT-PCR, single representatives of Lhx1/Lhx5, Lhx2/Lhx9, Pax3/Pax7 and Hedgehog families could be isolated in L. fluviatilis. Expression analysis revealed that the lamprey forebrain presents a clear neuromeric pattern. We describe the existence of 4 embryonic diencephalic prosomeres whose boundaries can be identified by the combined and relative expressions of LfPax37, LfLhx15 and LfLhx29. This suggests that the embryonic lamprey and gnathostome forebrain are patterned in a highly similar manner. Moreover, analysis of the LfHh gene, which is expressed in the hypothalamus, zona limitans intrathalamica and floor plate, reveals the possible molecular origin of this neuromeric brain pattern. By contrast, LfHh and LfNkx2.1 expressions suggest major differences in patterning mechanisms of the ventral telencephalon when compared to gnathostomes. In summary, our findings highlight a neuromeric organisation of the embryonic agnathan forebrain and point to the possible origin of this organisation, which is thus a truly vertebrate character. They also suggest that Hh/Shh midline signalling might act as a driving force for forebrain evolution.

Involvement of Hedgehog and FGF signalling in the lamprey telencephalon: evolution of regionalization and dorsoventral patterning of the vertebrate forebrain

“…By stage 24, LjHhA transcripts had not been detected in the neural tube rostral to the zona limitans intrathalamica (zli), but they began to be detected in the hypothalamus from stage 26, which was discontinuous from the more caudal expression domain (Fig. 1D,E) (Osorio et al, 2005). Otherwise, transcripts were also distributed in the endostyle (Fig.…”

“…Furthermore, based on the expression pattern of the Emx homologue, the pallium can be further divided into at least two domains that are specified dorsolaterally (Murakami et al, 2001). In addition, because the Nkx2.1 (also known as TTF-1) expression domain is absent in the subpallium and no Hh cognates are expressed in the telencephalon (Uchida et al, 2003;Osorio et al, 2005), the lampreys were assumed to lack a domain equivalent to the gnathostome MGE (Murakami et al, 2005). These traits pose a few questions regarding forebrain patterning in the lamprey.…”

Molecular Pathways Controlling Development of Thalamus and Hypothalamus: From Neural Specification to Circuit Formation

“…Selective expression of hedgehog family genes in the MDO of vertebrate model organisms is observed in lamprey (Osorio et al, 2005), zebrafish (Macdonald et al, 1995), frog (Ruiz i Altaba, 1998), chick (Kitamura et al, 1997), and mouse (Kitamura et al, 1997). Experimental abrogation of Shh signaling in zebrafish, chick, and mouse results in loss of genetic fate determinants and cell identity in prethalamus and thalamus (Kiecker and Lumsden, 2004;Scholpp et al, 2006;Vue et al, 2009).…”

Expanded expression of Sonic Hedgehog inAstyanaxcavefish:multiple consequences on forebrain development and evolution

“…Strikingly, lampreys do not express Shh and Nkx2.1 in their embryonic ventral forebrain (Murakami et al, 2001;Osorio et al, 2005), they do not have a pallidal division in their adult subpallium (Weigle and Northcutt, 1999), and they do not possess GABAergic interneurons in their pallium (Melendez-Ferro et al, 2002). Thus, the presence of regulatory cascades controlling cell migrations and generating diversity in neuronal patterning in the forebrain seems to be a novelty that emerged at the transition from agnathans to fish, and for which the impact of Shh midline signalling is crucial.…”

“…For example, although the global developmental organisation of the forebrain is highly conserved in lampreys (jawless vertebrates) compared with gnathostomes (Murakami et al, 2001;Murakami et al, 2005), their ventral telencephalon 'lacks' a pallidum (Weigle and Northcutt, 1999). Strikingly, there is no Shh signalling at the lamprey telencephalic ventral midline (Osorio et al, 2005), suggesting that Shh expression in the anterior ventral midline was responsible for the appearance of a novel forebrain subdivision, and further that midline signalling may be a powerful motor for forebrain evolution in jawed vertebrates.…”