Retinoic acid signaling and neurogenic niche regulation in the developing peripheral nervous system of the cephalochordate amphioxus

Zieger, Elisabeth; Garbarino, Greta; Naeije, Robert; Yu, Jr-Kai; Croce, Jenifer C.; Candiani, Simona; Schubert, Michael

doi:10.1007/s00018-017-2734-3

Cited by 18 publications

(28 citation statements)

References 109 publications

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“…Given the role of RA signaling in patterning the amphioxus general ectoderm (Schubert et al, 2004) and the scattered expression of CYP26-2 in this tissue (Carvalho et al, 2017), we next assessed the effects of CYP26 inhibition in the general ectoderm by assessing expression of Pax6, Tlx as well as Prdm12. The expression profiles of Pax6 and Tlx have previously been described during B. floridae development (Glardon et al, 1998;Kaltenbach et al, 2009;Lu et al, 2012) and those of Tlx have been reported in developing B. lanceolatum (Zieger, 2016). Furthermore, the effects of RA and BMS493 on Tlx expression have been assessed in B. lanceolatum (Zieger, 2016).…”

Section: Cyp26 Plays a Major Role In Patterning Specific Ectodermal Smentioning

confidence: 89%

“…The expression profiles of Pax6 and Tlx have previously been described during B. floridae development (Glardon et al, 1998;Kaltenbach et al, 2009;Lu et al, 2012) and those of Tlx have been reported in developing B. lanceolatum (Zieger, 2016). Furthermore, the effects of RA and BMS493 on Tlx expression have been assessed in B. lanceolatum (Zieger, 2016).…”

Section: Cyp26 Plays a Major Role In Patterning Specific Ectodermal Smentioning

confidence: 89%

“…Furthermore, we compared and contrasted the effects of CYP26 inhibition with those obtained by treatments with RA or a RAR antagonist, hence allowing an estimate of the importance of RA degradation in the global regulation of the developmental RA signaling system. Tissuespecific phenotypes in endoderm, mesoderm, ectoderm, and CNS were analyzed by assaying expression of six tissue-specific marker genes, En (Engrailed), Pax2/5/8 (Paired box 2/5/8), Pitx (Pairedlike homeodomain), Pax6 (Paired box 6), Tlx (T-cell leukemia homeobox), and Prdm12 (PR/SET domain 12) (Beaster-Jones et al, 2008;Boorman and Shimeld, 2002;Glardon et al, 1998;Holland et al, 1997;Holland and Holland, 1998;Kaltenbach et al, 2009;Kozmik et al, 1999;Lu et al, 2012;Schubert et al, 2005;Schubert et al, 2006;Somorjai et al, 2008;Soukup et al, 2015;Thélie et al, 2015;Yasui et al, 2000;Zieger et al, 2016). Altogether, this work establishes that CYP26 function is a crucial component of the overall developmental RA signaling system, modulating RA activity in very specific domains of the embryo: the anterior endoderm, the anterior-and posterior-most ectoderm, and along the A-P axis of the CNS, but not in the mesoderm.…”

Section: Introductionmentioning

confidence: 99%

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CYP26 function is required for the tissue-specific modulation of retinoic acid signaling during amphioxus development

Carvalho¹,

Lahaye²,

Croce³

et al. 2017

Int. J. Dev. Biol.

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During development, morphogens, such as retinoic acid (RA), act as mediators of intercellular communication systems to control patterning and cell fate specification processes. In vertebrates, the tightly regulated production and degradation of RA creates an anterior-posterior (A-P) morphogen gradient that is required for regional patterning of the embryo. RA catabolism in particular, mediated by members of the cytochrome P450 subfamily 26 (CYP26), has been highlighted as a key regulatory component for the formation of this gradient. RA-dependent developmental patterning is now widely recognized as a shared feature of all chordate groups (i.e. of vertebrates, tunicates, and cephalochordates). However, the evolutionary origin of the RA morphogen gradient still remains elusive. Thus, in the present study, we used pharmacological approaches to assess the roles of CYP26 enzymes in tissue-specific patterning processes in embryos and larvae of the cephalochordate amphioxus (Branchiostoma lanceolatum). Marker gene analyses revealed selective requirements for CYP26 activity in anterior endoderm, general ectoderm as well as central nervous system (CNS), but not in mesoderm. Furthermore, comparisons of the effects induced by CYP26 inhibition with those obtained by the pharmacological upregulation or downregulation of global RA signaling levels yielded evidence for a role of CYP26 in establishing an A-P RA gradient in the amphioxus embryo, important at least for patterning the CNS. Altogether, this work hence highlights the involvement of CYP26 in tissue-specific modulations of RA signaling activity in the amphioxus embryo and suggests that a RA morphogen gradient already functioned in the last common ancestor of all chordates.

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Section: Cyp26 Plays a Major Role In Patterning Specific Ectodermal Smentioning

confidence: 89%

Section: Cyp26 Plays a Major Role In Patterning Specific Ectodermal Smentioning

confidence: 89%

Section: Introductionmentioning

confidence: 99%

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CYP26 function is required for the tissue-specific modulation of retinoic acid signaling during amphioxus development

Carvalho¹,

Lahaye²,

Croce³

et al. 2017

Int. J. Dev. Biol.

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“…(c) The early neurula (cross‐section view) and very early larva (lateral view) of amphioxus are shown. ESN s are (light blue) originated from the ventral ectoderm (Zieger et al., ). The arrows show the delamination and dorsal migration of ESN precursors (Kaltenbach et al., ).…”

Section: Pns Neurons Derived From Primitive Neural Crest and Placode mentioning

confidence: 99%

Lateral neural borders as precursors of peripheral nervous systems: A comparative view across bilaterians

2018

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The nervous systems in most bilaterians are centralized, composed of central nervous systems (CNS) and peripheral nervous systems (PNS). Common molecular and cellular patterns of medial nerve cords have been observed in various distantly related bilaterians, suggesting deep homology of CNS. The development patterns of PNS, however, are more diverse than CNS across different phylogenetic lineages and the evolution of PNS so far has been thought to be polygenic. The molecular and cellular programs during the development of PNS among different bilaterian branches are drastically different. For example, vertebrate PNS is essentially derived from neural crest cells and placodes, which are largely vertebrate innovations and do not exist in invertebrates. On the other hand, the lack of common precursor cell types does not necessarily lead to the conclusion of different evolutionary origins. Homology needs to be examined with a deeper and broader scope. In this review, we examined the molecular, cellular and developmental characteristics of PNS in a broad range of bilaterians to summarize our current understanding of variation and potentially conserved themes. These comparisons demonstrate that there exist both migratory and non‐migratory neuroblasts in the lateral border of CNS precursors in most model bilaterian animals. These lateral border neuroblasts are specified by conserved gene regulatory network and give rise to sensory neurons, suggesting that lateral border neuroblasts represent the progenitor of PNS and share deep homology among different branches of Bilateria. Future studies are needed to elucidate the evo‐devo mechanisms of the lateral neural borders as PNS progenitors.

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“…Nuclear DNA staining was performed for 10 minutes at room temperature using lanceolatum embryos and larvae were fixed overnight at 4ºC in freshly prepared ice-cold 4% paraformaldehyde in MOPS buffer [69]. Immunohistochemistry was performed as previously described [70], using a primary antibody against aPKC subsequently carried out with a mrf1-specific antisense riboprobe as previously described [69,71].…”

Section: Fluorescent Staining Immunohistochemistry and In Situ Hybrimentioning

confidence: 99%

An updated staging system for cephalochordate development: one table suits them all

Carvalho

Lahaye

Yong

et al. 2020

Preprint

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Background:The chordates are divided into three subphyla: Vertebrata, Tunicata and Cephalochordata. Phylogenetically, the Cephalochordata, more commonly known as lancelets or amphioxus, constitute the sister group of Vertebrata plus Tunicata. Due to their phylogenetic position and their conserved morphology and genome architecture, lancelets are important models for understanding the evolutionary history of chordates. Lancelets are small, marine filter-feeders, and the few dozen species that have so far been described have been grouped into three genera: Branchiostoma, Epigonichthys and Asymmetron.Given their relevance for addressing questions about the evolutionary diversification of chordates, lancelets have been the subjects of study by generations of scientists, with the first descriptions of adult anatomy and developmental morphology dating back to the 19 th century. Today, several different lancelet species are used as laboratory models, predominantly for developmental, molecular and genomic studies. It is thus very surprising that there is currently no universal staging system and no unambiguous nomenclature for developing lancelets. Results:We illustrated the development of the European amphioxus (Branchiostoma lanceolatum) using confocal microscopy and compiled a streamlined developmental staging system, from fertilization through larval life, with an unambiguous stage nomenclature. By tracing growth curves of the European amphioxus reared at different temperatures, we were able to show that our staging system permits the easy conversion of any developmental time into a defined 3 stage name. Furthermore, comparisons of embryos and larvae from the European amphioxus (B. lanceolatum), the Florida amphioxus (B. floridae), the Chinese amphioxus (B. belcheri), the Japanese amphioxus (B. japonicum) and the Bahamas lancelet (Asymmetron lucayanum) demonstrated that our staging system can readily be applied to other lancelet species.Conclusions: Here, we propose an updated staging and nomenclature system for lancelets. Although the detailed staging description was carried out on developing B. lanceolatum, comparisons with other lancelet species strongly suggest that both staging and nomenclature are applicable to all extant lancelets.We thus believe that this description of embryonic and larval development can be of great use for the scientific community and hope that it will become the new standard for defining and naming developing lancelets. KeywordsAmphioxus, Asymmetron lucayanum, Branchiostoma belcheri, Branchiostoma floridae, Branchiostoma japonicum, Branchiostoma lanceolatum, Confocal Microscopy, Embryonic and Larval Development, Evolution and Development, Lancelet 4

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Retinoic acid signaling and neurogenic niche regulation in the developing peripheral nervous system of the cephalochordate amphioxus

Cited by 18 publications

References 109 publications

CYP26 function is required for the tissue-specific modulation of retinoic acid signaling during amphioxus development

CYP26 function is required for the tissue-specific modulation of retinoic acid signaling during amphioxus development

Lateral neural borders as precursors of peripheral nervous systems: A comparative view across bilaterians

An updated staging system for cephalochordate development: one table suits them all

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