Portal de Periódicos da CAPES

A Nomenclature for Prospective Somites and Phases of Cyclic Gene Expression in the Presomitic Mesoderm

2001; Elsevier BV; Volume: 1; Issue: 5 Linguagem: Inglês

10.1016/s1534-5807(01)00082-x

1878-1551

Olivier Pourquié, Patrick Tam,

Genetic and Clinical Aspects of Sex Determination and Chromosomal Abnormalities

In July 2001, a meeting dedicated to embryonic segmentation was held in Nara, Japan. Discussions at this meeting emphasized that many aspects of the basic segmentation machinery are conserved among vertebrates and that it seems important to adopt a unified nomenclature among species. This letter outlines a new numeration system for segmental domains that provides consistency between different vertebrate model systems. In vertebrates, the paraxial mesoderm is composed of serially repeated segments (somites) that are aligned along the anteroposterior (AP) axis. Somites are formed by successive segmentation of the presomitic mesoderm (PSM; Figure 1A) in a cranial to caudal manner, resulting in the formation of a finite and species-specific number of segmental units. Once formed, each somite follows a consistent timetable of differentiation. For example, myogenic determinants such as myf5 are expressed immediately after somite formation, and initiation of sclerotome dispersal in a given somite occurs after three to four more somites have formed from the PSM. This means that during somitogenesis the somites forming along the body axis are at a succession of developmental stages from segmentation to tissue differentiation, with the rostral somites being the most advanced and the caudal ones displaying earlier events. This observation forms the basis for the currently existing system for staging and comparing somite differentiation. Individual somites are numbered (in roman numerals: I, II, III, etc.) according to their craniocaudal position beginning with the most recently segmented somite (Ordahl 1993Ordahl C.P. Myogenic lineages within the developing somite.in: Bernfield M. Molecular Basis of Morphogenesis. John Wiley and Sons, New York1993Google Scholar). Somites of the same number are similar in their cellular and molecular properties independent of the actual age of the embryo such that somite V of an embryo with 15 somites is equivalent to somite V of another embryo with 20 somites in terms of myogenic gene expression and other aspects of somite maturation. Recent embryological and molecular analyses have focused on the cellular and molecular organization of a presegmental pattern of prospective somites in the presomitic mesoderm (Tam et al. 2000Tam P.P.L. Goldman D. Camus A. Schoenwolf G.C. Early events of somitogenesis in higher vertebrates allocation of precursor cells during gastrulation and the organization of a meristic pattern in the paraxial mesoderm.Curr. Top. Dev. Biol.. 2000; 47: 1-32Crossref PubMed Scopus (39) Google Scholar). Analysis of expression patterns has shown that some genes are expressed in a dynamic mode encompassing different domains of the presomitic mesoderm or in restricted domains that may correspond to prospective somites. As more data become available, it will be important to describe patterns of gene expression in a consistent manner so that results obtained in studies of different genes at different developmental stages and in different species can be compared. Discussions during and following the Nara meeting on segmentation have led to a consensus agreement to extend the existing nomenclature to include the prospective somites in the presomitic mesoderm. As in the Ordahl system, the last completely segmented somite is somite SI. The intersomitic fissure between somite SI and the presomitic mesoderm is border 0 (B0). The presomitic mesoderm is then subdivided into prospective somites beginning with somite S0, S-I, S-II, S-III, and so on. Prospective boundaries are labeled beginning with -1 for the caudal boundary of somite S0 and border -2 for the caudal boundary of Somite S-I, and so on (Figure 1A). As was originally proposed in theoretical models, recent evidence from work performed in fish, chick, and mouse embryos has led to the conclusion that segmentation of the vertebrate embryonic body relies on a molecular oscillator called the segmentation clock. The existence of this clock is suggested by the rhythmic expression in the PSM of a particular set of genes linked to the Notch pathway, called the cyclic genes. These genes include those encoding transcription factors related to the Hairy and Enhancer-of-split Drosophila genes, such as c-Hairy1, c-Hairy2, c-Hey2, HES1, HES7, and Her1 in chick, mouse, and fish, the glycosyl-transferase Lunatic Fringe in chick and mouse, and the Notch ligand DeltaC in zebrafish (Aulehla and Johnson 1999Aulehla A. Johnson R.L. Dynamic expression of lunatic fringe suggests a link between notch signaling and an autonomous cellular oscillator driving somite segmentation.Dev. Biol. 1999; 207: 49-61Crossref PubMed Scopus (170) Google Scholar, Bessho et al. 2001Bessho Y. Miyoshi G. Sakata R. Kageyama R. Hes7 a bHLH-type repressor gene regulated by Notch and expressed in the presomitic mesoderm.Genes Cells. 2001; 6: 175-185Crossref PubMed Scopus (141) Google Scholar, Forsberg et al. 1998Forsberg H. Crozet F. Brown N.A. Waves of mouse Lunatic fringe expression, in four-hour cycles at two-hour intervals, precede somite boundary formation.Curr. Biol. 1998; 8: 1027-1030Abstract Full Text Full Text PDF PubMed Scopus (208) Google Scholar, Holley et al. 2000Holley S.A. Geisler R. Nusslein-Volhard C. Control of her1 expression during zebrafish somitogenesis by a delta-dependent oscillator and an independent wave-front activity.Genes Dev. 2000; 14: 1678-1690PubMed Google Scholar, Jiang et al. 2000Jiang Y.J. Aerne B.L. Smithers L. Haddon C. Ish-Horowicz D. Lewis J. Notch signalling and the synchronization of the somite segmentation clock.Nature. 2000; 408: 475-479Crossref PubMed Scopus (402) Google Scholar, Jouve et al. 2000Jouve C. Palmeirim I. Henrique D. Beckers J. Gossler A. Ish-Horowicz D. Pourquie O. Notch signalling is required for cyclic expression of the hairy-like gene HES1 in the presomitic mesoderm.Development. 2000; 127: 1421-1429PubMed Google Scholar, Leimeister et al. 2000Leimeister C. Dale K. Fischer A. Klamt B. Hrabe de Angelis M. Radtke F. McGrew M.J. Pourquie O. Gessler M. Oscillating expression of c-hey2 in the presomitic mesoderm suggests that the segmentation clock may use combinatorial signaling through multiple interacting bHLH factors.Dev. Biol.. 2000; 227: 91-103Crossref PubMed Scopus (134) Google Scholar, McGrew et al. 1998McGrew M.J. Dale J.K. Fraboulet S. Pourquie O. The lunatic fringe gene is a target of the molecular clock linked to somite segmentation in avian embryos.Curr. Biol.. 1998; 8: 979-982Abstract Full Text Full Text PDF PubMed Scopus (217) Google Scholar, Palmeirim et al. 1997Palmeirim I. Henrique D. Ish-Horowicz D. Pourquié O. Avian hairy gene expression identifies a molecular clock linked to vertebrate segmentation and somitogenesiss.Cell. 1997; 91: 639-648Abstract Full Text Full Text PDF PubMed Scopus (689) Google Scholar, Sawada et al. 2000Sawada A. Fritz A. Jiang Y. Yamamoto A. Yamasu K. Kuroiwa A. Saga Y. Takeda H. Zebrafish Mesp family genes, mesp-a and mesp-b are segmentally expressed in the presomitic mesoderm, and Mesp-b confers the anterior identity to the developing somites.Development. 2000; 127: 1691-1702PubMed Google Scholar). These genes are expressed in a dynamic temporal and spatial sequence in the PSM. Initially, they are expressed in a broad caudal domain extending from the primitive streak and/or tail bud across the caudal half of the PSM (see Figure 1B). Expression then becomes progressively more restricted to domains (or prospective somites) in the anterior region of the PSM. This whole sequence is reiterated once during the formation of each somite. In the proposed nomenclature system, the dynamic sequences of gene expression are described as three phases: phase I, when the genes are expressed by the cells of the caudal PSM; phase II, when expression is found in a broad domain in the middle region of the PSM; and phase III, when genes are expressed in a discrete domain in PSM tissues that are about to undergo segmentation (Figure 1B). This expanded nomenclature provides a framework for discussion of newly emerging data on somitogenesis. It represents a consensus opinion across a broad spectrum of the field, and we hope that it will be adopted by the entire community to facilitate comparison and discussion of results and models. We are grateful to many individuals for contributions to the discussions that led to this consensus, particularly Denis Duboule, Achim Gossler, Scott Holley, David Ish-Horowicz, Yun-Jin Jiang, Randy Johnson, Chris Kintner, Marc Kirschner, Robb Krumlauf, Julian Lewis, Charles Ordahl, Yumiko Saga, Claudio Stern, Cliff Tabin, Yoshiko Takahashi, and Hiroyuki Takeda.