Publications

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2002
Yu, JK, Holland LZ, Holland ND.  2002.  An amphioxus nodal gene (AmphiNodal) with early symmetrical expression in the organizer and mesoderm and later asymmetrical expression associated with left-right axis formation. Evolution & Development. 4:418-425.   10.1046/j.1525-142X.2002.02030.x   AbstractWebsite

The full- length sequence and zygotic expression of an amphioxus nodal gene are described. Expression is first detected in the early gastrula just within the dorsal lip of the blastopore in a region of hypoblast that is probably comparable with the vertebrate Spemann's organizer. In the late gastrula and early neurula, expression remains bilaterally symmetrical, limited to paraxial mesoderm and immediately overlying regions of the neural plate. Later in the neurula stage, all neural expression disappears, and mesodermal expression disappears from the right side. All along the left side of the neurula, mesodermal expression spreads into the left side of the gut endoderm. Soon thereafter, all expression is down- regulated except near the anterior and posterior ends of the animal, where transcripts are still found in the mesoderm and endoderm on the left side. At this time, expression also begins in the ectoderm on the left side of the head, in the region where the mouth later forms. These results suggest that amphioxus and vertebrate nodal genes play evolutionarily conserved roles in establishing Spemann's organizer, patterning the mesoderm rostrocaudally and setting up the asymmetrical left - right axis of the body.

Yu, JK, Holland ND, Holland LZ.  2002.  An amphioxus winged helix/forkhead gene, AmphiFoxD: Insights into vertebrate neural crest evolution. Developmental Dynamics. 225:289-297.   10.1002/dvdy.10173   AbstractWebsite

During amphioxus development, the neural plate is bordered by cells expressing many genes with homologs involved in vertebrate neural crest induction. However, these amphioxus cells evidently lack additional genetic programs for the cell delaminations, migrations, and differentiations characterizing definitive vertebrate neural crest. We characterize an amphioxus winged helix/forkhead gene (AmphiFoxD) closely related to vertebrate FoxD genes. Phylogenetic analysis indicates that the AmphiFoxD is basal to vertebrate FoxD1, FoxD2, FoxD3, FoxD4, and FoxD5. One of these vertebrate genes (FoxD3) consistently marks neural crest during development. Early in amphioxus development, AmphiFoxD is expressed medially in the anterior neural plate as well as in axial (notochordal) and paraxial mesoderm; later, the gene is expressed in the somites, notochord, cerebral vesicle (diencephalon), and hindgut endoderm. However, there is never any expression in cells bordering the neural plate. We speculate that an AmphiFoxD homolog in the common ancestor of amphioxus and vertebrates was involved in histogenic processes in the mesoderm (evagination and delamination of the somites and notochord); then, in the early vertebrates, descendant paralogs of this gene began functioning in the presumptive neural crest bordering the neural plate to help make possible the delaminations and cell migrations that characterize definitive vertebrate neural crest. (C) 2002 Wiley-Liss, Inc.

2001
Schubert, M, Holland LZ, Stokes MD, Holland ND.  2001.  Three amphioxus Wnt genes (AmphiWnt3, AmphiWnt5, and AmphiWnt6) associated with the tail bud: The evolution of somitogenesis in chordates. Developmental Biology. 240:262-273.   10.1006/dbio.2001.0460   AbstractWebsite

The amphioxus tail bud is similar to the amphibian tail bud in having an epithelial organization without a mesenchymal component. We characterize three amphioxus Wnt genes (AmphiWnt3, AmphiWnt5, and AmphiWnt6) and show that their early expression around the blastopore can subsequently be traced into the tail bud; in vertebrate embryos, there is a similar progression of expression domains for Wnt3, Wnt5, and Wnt6 genes from the blastopore lip (or its equivalent) to the tail bud. In amphioxus, AmphiWnt3, AmphiWnt5, and AmphiWnt6 are each expressed in a specific subregion of the tail bud, tentatively suggesting that a combinatorial code of developmental gene expression may help generate specific tissues during posterior elongation and somitogenesis. In spite of similarities within their tail buds, vertebrate and amphioxus embryos differ markedly in the relation between the tail bud and the nascent somites: vertebrates have a relatively extensive zone of unsegmented mesenchyme (i.e., presomitic mesoderm) intervening between the tail bud and the forming somites, whereas the amphioxus tail bud gives rise to new somites directly. It is likely that presomitic mesoderm is a vertebrate innovation made possible by developmental interconversions between epithelium and mesenchyme that first became prominent at the dawn of vertebrate evolution. (C) 2001 Academic Press.

2000
Schubert, M, Holland LZ, Holland ND.  2000.  Characterization of two amphioxus Wnt genes (AmphiWnt4 and AmphiWnt7b) with early expression in the developing central nervous system. Developmental Dynamics. 217:205-215.   10.1002/(sici)1097-0177(200002)217:2<205::aid-dvdy7>3.0.co;2-f   AbstractWebsite

Full-length sequences and developmental expression patterns of two amphioxus Wnt genes (AmphiWnt4 and AmphiWnt7b) are described for the first time. The dynamic expression pattern of AmphiWnt4 suggests roles in the development of the posterior mesoderm, central nervous system, muscular somites, heart, and endostyle (a homolog of the vertebrate thyroid). The less diverse expression domains of AmphiWnt7b indicate that this gene may be involved only in the development of the central nervous system and the endostyle, In contrast to amphioxus, vertebrate embryos do not express Wnt4 homologues in the posterior mesoderm, somites, or heart; instead, Wnt genes of other subfamilies are expressed in these developing vertebrate organs, Because the developmental genetic programs of amphioxus may approximate those in the invertebrate chordate ancestor of the vertebrates, it is possible that some developmental functions of an ancestral Wnt4 gene may have been assumed by genes of other Wnt subfamilies during vertebrate evolution, possibly as a result of functional redundancy among Wnt subfamilies. (C) 2000 Wiley-Liss, Inc.

1999
Kozmik, Z, Holland ND, Kalousova A, Paces J, Schubert M, Holland LZ.  1999.  Characterization of an amphioxus paired box gene, AmphiPax2/5/8: developmental expression patterns in optic support cells, nephridium, thyroid-like structures and pharyngeal gill slits, but not in the midbrain-hindbrain boundary region. Development. 126:1295-1304. AbstractWebsite

On the basis of developmental gene expression, the vertebrate central nervous system comprises: a forebrain plus anterior midbrain, a midbrain-hindbrain boundary region (MHB) having organizer properties, and rhombospinal domain. The vertebrate MHB is characterized by position, by organizer properties and by being the early site of action of Wnt1 and engrailed genes, and of genes of the Pax2/5/8 subfamily. Wada and others (Wada, H., Saiga, H., Satoh, N. and Holland, P.W.H. (1998) Development 125, 1113-1122) suggested that ascidian tunicates have a vertebrate-like MHB on the basis of ascidian Pax258 expression there. In another invertebrate chordate, amphioxus, comparable gene expression evidence for a vertebrate-like MHB is lacking, We, therefore, isolated and characterized AmphiPax2/5/8, the sole member of this subfamily in amphioxus, AmphiPax2/5/8 is initially expressed well back in the rhombospinal domain and not where a MHB would be expected. In contrast, most of the other expression domains of AmphiPax2/5/8 correspond to expression domains of vertebrate Pax2, Pax5 and Pax8 in structures that are probably homologous - support cells of the eye, nephridium, thyroid-like structures and pharyngeal gill slits; although AmphiPax2/5/8 is not transcribed in any structures that could be interpreted as homologues of vertebrate otic placodes or otic vesicles. In sum, the developmental expression of AmphiPax2/5/8 indicates that the amphioxus central nervous system lacks a MHB resembling the vertebrate isthmic region, Additional gene expression data for the developing ascidian and amphioxus nervous systems would help determine whether a MHB is a basal chordate character secondarily lost in amphioxus, The alternative is that the MHB is a vertebrate innovation.

1998
Panopoulou, GD, Clark MD, Holland LZ, Lehrach H, Holland ND.  1998.  AmphiBMP2/4, an amphioxus bone morphogenetic protein closely related to Drosophila decapentaplegic and vertebrate BMP2 and BMP4: Insights into evolution of dorsoventral axis specification. Developmental Dynamics. 213:130-139.   10.1002/(sici)1097-0177(199809)213:1<130::aid-aja13>3.3.co;2-z   AbstractWebsite

Amphioxus AmphiBMP2/4 appears to be a single gene closely related to vertebrate BMP2 and BMP4. In amphioxus embryos, the expression patterns of AmphiBMP2/4 suggest patterning roles in the ectodermal dorsoventral axis (comparable to dorsoventral axis establishment in the ectoderm by Drosophila decapentaplegic and vertebrate BMP4). In addition AmphiBMP2/4 may be involved in somite evagination, tail bud growth, pharyngeal differentiation (resulting in club-shaped gland morphogenesis), hindgut regionalization, differentiation of olfactory epithelium, patterning of the anterior central nervous system, and establishment of the heart primordium, One difference between the developmental role of amphioxus AmphiBMP2/4 and vertebrate BMP4 is that the former does not appear to be involved in the initial establishment of the dorsoventral polarity of the mesoderm, Dev. Dyn. 1998;213:130-139. (C) 1998 Wiley-Liss, Inc.

1993