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Bardet, PL, Schubert M, Horard B, Holland LZ, Laudet V, Holland ND, Vanacker JM.  2005.  Expression of estrogen-receptor related receptors in amphioxus and zebrafish: implications for the evolution of posterior brain segmentation at the invertebrate-to-vertebrate transition. Evolution & Development. 7:223-233.   10.1111/j.1525-142X.2005.05025.x   AbstractWebsite

The evolutionary origin of vertebrate hindbrain segmentation is unclear since the amphioxus, the closest living invertebrate relative to the vertebrates, possesses a hindbrain homolog that displays no gross morphological segmentation. Three of the estrogen-receptor related (ERR) receptors are segmentally expressed in the zebrafish hindbrain, suggesting that their common ancestor was expressed in a similar, reiterated manner. We have also cloned and determined the developmental expression of the single homolog of the vertebrate ERR genes in the amphioxus (AmphiERR). This gene is also expressed in a segmented manner in a region considered homologous to the vertebrate hindbrain. In contrast to the expression of amphioxus islet (a LIM-homeobox gene that also labels motoneurons), AmphiERR expression persists longer in the hindbrain homolog and does not later extend to additional posterior cells. In addition, AmphiERR and one of its vertebrate homologs (ERR alpha) are expressed in the developing somitic musculature of amphioxus and zebrafish, respectively. Altogether, our results are consistent with fine structural evidence suggesting that the amphioxus hindbrain is segmented, and indicate that chordate ERR gene expression is a marker for both hindbrain and muscle segmentation. Furthermore, our data support an evolution model of chordate brain segmentation: originally, the program for anterior segmentation in the protochordate ancestors of the vertebrates resided in the developing axial mesoderm which imposed reiterated patterning on the adjacent neural tube; during early vertebrate evolution, this segmentation program was transferred to and controlled by the neural tube.

Beaster-Jones, L, Kaltenbach S, Koop D, Yuan SC, Chastain R, Holland LZ.  2008.  Expression of somite segmentation genes in amphioxus: a clock without a wavefront? Development Genes and Evolution. 218:599-611.   10.1007/s00427-008-0257-5   AbstractWebsite

In the basal chordate amphioxus (Branchiostoma), somites extend the full length of the body. The anteriormost somites segment during the gastrula and neurula stages from dorsolateral grooves of the archenteron. The remaining ones pinch off, one at a time, from the tail bud. These posterior somites appear to be homologous to those of vertebrates, even though the latter pinch off from the anterior end of bands of presomitic mesoderm rather than directly from the tail bud. To gain insights into the evolution of mesodermal segmentation in chordates, we determined the expression of ten genes in nascent amphioxus somites. Five (Uncx4.1, NeuroD/atonal-related, IrxA, Pcdh delta 2-17/18, and Hey1) are expressed in stripes in the dorsolateral mesoderm at the gastrula stage and in the tail bud while three (Paraxis, Lcx, and Axin) are expressed in the posterior mesendoderm at the gastrula and neurula stages and in the tail bud at later stages. Expression of two genes (Pbx and OligA) suggests roles in the anterior somites that may be unrelated to initial segmentation. Together with previous data, our results indicate that, with the exception that Engrailed is only segmentally expressed in the anterior somites, the genetic mechanisms controlling formation of both the anterior and posterior somites are probably largely identical. Thus, the fundamental pathways for mesodermal segmentation involving Notch-Delta, Wnt/beta-catenin, and Fgf signaling were already in place in the common ancestor of amphioxus and vertebrates although budding of somites from bands of presomitic mesoderm exhibiting waves of expression of Notch, Wnt, and Fgf target genes was likely a vertebrate novelty. Given the conservation of segmentation gene expression between amphioxus and vertebrate somites, we propose that the clock mechanism may have been established in the basal chordate, while the wavefront evolved later in the vertebrate lineage.

Beaster-Jones, L, Schubert M, Holland LZ.  2007.  Cis-regulation of the amphioxus engrailed gene: Insights into evolution of a muscle-specific enhancer. Mechanisms of Development. 124:532-542.   10.1016/j.mod.2007.06.002   AbstractWebsite

To gain insights into the relation between evolution of cis-regulatory DNA and evolution of gene function, we identified tissue-specific enhancers of the engrailed gene of the basal chordate amphioxus (Branch iostoma floridae) and compared their ability to direct expression in both amphioxus and its nearest chordate relative, the tunicate Ciona intestinalis. In amphioxus embryos, the native engrailed gene is expressed in three domains - the eight most anterior somites, a few cells in the central nervous system (CNS) and a few ectodermal cells. In contrast, in C. intestinalis, in which muscle development is highly divergent, engrailed expression is limited to the CNS. To characterize the tissue-specific enhancers of amphioxus engrailed, we first showed that 7.8 kb of upstream DNA of amphioxus engrailed directs expression to all three domains in amphioxus that express the native gene. We then identified the amphioxus engrailed muscle-specific enhancer as the 1.2 kb region of upstream DNA with the highest sequence identity to the mouse en-2 jaw muscle enhancer. This amphioxus enhancer directed expression to both the somites in amphioxus and to the larval muscles in C intestinalis. These results show that even though expression of the native engrailed has apparently been lost in developing C intestinalis muscles, they express the transcription factors necessary to activate transcription from the amphioxus engrailed enhancer, suggesting that gene networks may not be completely disrupted if an individual component is lost. (c) 2007 Elsevier Ireland Ltd. All rights reserved.

Beaster-Jones, L, Horton AC, Gibson-Brown JJ, Holland ND, Holland LZ.  2006.  The amphioxus T-box gene, AmphiTbx15/18/22, illuminates the origins of chordate segmentation. Evolution & Development. 8:119-129.   10.1111/j.1525-142X.2006.00083.x   AbstractWebsite

Amphioxus and vertebrates are the only deuterostomes to exhibit unequivocal somitic segmentation. The relative simplicity of the amphioxus genome makes it a favorable organism for elucidating the basic genetic network required for chordate somite development. Here we describe the developmental expression of the somite marker, AmphiTbx15/18/22, which is first expressed at the mid-gastrula stage in dorsolateral mesendoderm. At the early neurula stage, expression is detected in the first three pairs of developing somites. By the mid-neurula stage, expression is downregulated in anterior somites, and only detected in the penultimate somite primordia. In early larvae, the gene is expressed in nascent somites before they pinch off from the posterior archenteron (tail bud). Integrating functional, phylogenetic and expression data from a variety of triploblast organisms, we have reconstructed the evolutionary history of the Tbx15/18/22 subfamily. This analysis suggests that the Tbx15/18/22 gene may have played a role in patterning somites in the last common ancestor of all chordates, a role that was later conserved by its descendents following gene duplications within the vertebrate lineage. Furthermore, the comparison of expression domains within this gene subfamily reveals similarities in the genetic bases of trunk and cranial mesoderm segmentation. This lends support to the hypothesis that the vertebrate head evolved from an ancestor possessing segmented cranial mesoderm.

Boldrin, F, Martinucci G, Holland LZ, Miller RL, Burighel P.  2009.  Internal fertilization in the salp Thalia democratica. Canadian Journal of Zoology-Revue Canadienne De Zoologie. 87:928-940.   10.1139/z09-083   AbstractWebsite

Among tunicates, gamete morphology and sperm-egg interactions have been extensively investigated in ascidians, and to a lesser extent in appendicularians and thaliaceans. Sperm-egg interaction has been studied in only one salp, Pegea socia (Bosc, 1802). To determine if the pattern of internal fertilization of P. socia is generally applicable to salps, we performed an ultrastructural study on blastozooids of Thalia democratica (Forsskal, 1775). The ovary, located in the mantle near the gut, consists of a single oocyte connected to the atrial chamber wall by a "fertilization duct", resembling a stack of single cells without a lumen. The flagellate sperm has a long corkscrew-like head with the single mitochondrion twisted around the nucleus. Fertilization is internal, and sperm actively penetrate the atrial wall and bore through the cells of the fertilization duct. During this process, the fertilization duct shortens as the cells move apart, one to one side and the next to the other, and rejoin to form a central lumen, which contains many sperm. At the same time a few sperm reach the periovular space for fertilizing the oocyte. Comparisons with P. socia indicate that this singular mode of internal fertilization with a complex corkscrew sperm actively penetrating the fertilization duct cells, probably evolved in the salp ancestor and has been modified to some extent in various genera.

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Castro, LFC, Rasmussen SLK, Holland PWH, Holland ND, Holland LZ.  2006.  A Gbx homeobox gene in amphioxus: Insights into ancestry of the ANTP class and evolution of the midbrain/hindbrain boundary. Developmental Biology. 295:40-51.   10.1016/j.ydbio.2006.03.003   AbstractWebsite

In the vertebrate central nervous system (CNS), mutual antagonism between posteriorly expressed Gbx2 and anteriorly expressed OtX2 positions the midbrain/hindbrain boundary (MHB), but does not induce MHB organizer genes such as En, Pax2/5/8 and Wnt1. In the CNS of the cephalochordate amphioxus, Otx is also expressed anteriorly, but En, Pax2/5/8 and Wnt1 are not expressed near the caudal limit of Otx, raising questions about the existence of an MHB organizer in amphioxus. To investigate the evolutionary origins of the MHB, we cloned the single amphioxus Gbx gene. Fluorescence in situ hybridization showed that, as in vertebrates, amphioxus Gbx and the Hox cluster are on the same chromosome. From analysis of linked genes, we argue that during evolution a single ancestral Gbx gene duplicated fourfold in vertebrates, with subsequent loss of two duplicates. Amphioxus Gbx is expressed in all germ layers in the posterior 75% of the embryo, and in the CNS, the Gbx and Otx domains abut at the boundary between the cerebral vesicle (forebrain/midbrain) and the hindbrain. Thus, the genetic machinery to position the MHB was present in the protochordate ancestors of the vertebrates, but is insufficient for induction of organizer genes. Comparison with hemichordates suggests that anterior Otx and posterior Gbx domains were probably overlapping in the ancestral deuterostome and came to abut at the MHB early in the chordate lineage before MHB organizer properties evolved. (c) 2006 Elsevier Inc. All rights reserved.

Cross, NL, Slezynger TC, Holland LZ.  1985.  Isolation and Partial Characterization of Urechis-Caupo Egg Envelopes. Journal of Cell Science. 74:193-205.Website
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Escriva, H, Holland ND, Gronemeyer H, Laudet C, Holland LZ.  2002.  The retinoic acid signaling pathway regulates anterior/posterior patterning in the nerve cord and pharynx of amphioxus, a chordate lacking neural crest. Development. 129:2905-2916. AbstractWebsite

Amphioxus, the closest living invertebrate relative of the vertebrates, has a notochord, segmental axial musculature, pharyngeal gill slits and dorsal hollow nerve cord, but lacks neural crest. In amphioxus, as in vertebrates, exogenous retinoic acid (RA) posteriorizes the embryo. The mouth and gill slits never form, AmphiPax1, which is normally downregulated where gill slits form, remains upregulated and AmphiHox1 expression shifts anteriorly in the nerve cord. To dissect the role of RA signaling in patterning chordate embryos, we have cloned the single retinoic acid receptor (AmphiRAR), retinoid X receptor (AmphiRXR) and an orphan receptor (AmphiTR2/4) from amphioxus. AmphiTR2/4 inhibits AmphiRAR-AmphiRXR-mediated transactivation in the presence of RA by competing for DR5 or IR7 retinoic acid response elements (RAREs). The 5' untranslated region of AmphiTR2/4 contains an IR7 element, suggesting possible auto- and RA-regulation. The patterns of AmphiTR2/4 and AmphiRAR expression during embryogenesis are largely complementary: AmphiTR2/4 is strongly expressed in the cerebral vesicle (homologous to the diencephalon plus anterior midbrain), while AmphiRAR expression is high in the equivalent of the hindbrain and spinal cord. Similarly, while AmphiTR2/4 is expressed most strongly in the anterior and posterior thirds of the endoderm, the highest AmphiRAR expression is in the middle third. Expression of AmphiRAR is upregulated by exogenous RA and completely downregulated by the RA antagonist BMS009. Moreover, BMS009 expands the pharynx posteriorly; the first three gill slit primordia are elongated and shifted posteriorly, but do not penetrate, and additional, non-penetrating gill slit primordia are induced. Thus, in an organism without neural crest, initiation and penetration of gill slits appear to be separate events mediated by distinct levels of RA signaling in the pharyngeal endoderm. Although these compounds have little effect on levels of AmphiTR2/4 expression, RA shifts pharyngeal expression of AmphiTR2/4 anteriorly, while BMS009 extends it posteriorly. Collectively, our results suggest a model for anteroposterior patterning of the amphioxus nerve cord and pharynx, which is probably applicable to vertebrates as well, in which a low anterior level of AmphiRAR (caused, at least in part, by competitive inhibition by AmphiTR2/4) is necessary for patterning the forebrain and formation of gill slits, the posterior extent of both being set by a sharp increase in the level of AmphiRAR.

Escriva, H, Bertrand S, Germain P, Robinson-Rechavi M, Umbhauer M, Cartry J, Duffraisse M, Holland L, Gronemeyer H, Laudet V.  2006.  Neofunctionalization in vertebrates: The example of retinoic acid receptors. Plos Genetics. 2:955-965.   10.1371/journal.pgen.0020102   AbstractWebsite

Understanding the role of gene duplications in establishing vertebrate innovations is one of the main challenges of Evo-Devo (evolution of development) studies. Data on evolutionary changes in gene expression (i.e., evolution of transcription factor-cis-regulatory elements relationships) tell only part of the story; protein function, best studied by biochemical and functional assays, can also change. In this study, we have investigated how gene duplication has affected both the expression and the ligand-binding specificity of retinoic acid receptors (RARs), which play a major role in chordate embryonic development. Mammals have three paralogous RAR genes-RAR alpha, beta, and gamma-which resulted from genome duplications at the origin of vertebrates. By using pharmacological ligands selective for specific paralogues, we have studied the ligand-binding capacities of RARs from diverse chordates species. We have found that RAR beta-like binding selectivity is a synapomorphy of all chordate RARs, including a reconstructed synthetic RAR representing the receptor present in the ancestor of chordates. Moreover, comparison of expression patterns of the cephalochordate amphioxus and the vertebrates suggests that, of all the RARs, RAR beta expression has remained most similar to that of the ancestral RAR. On the basis of these results together, we suggest that while RAR beta kept the ancestral RAR role, RAR alpha and RAR gamma diverged both in ligand-binding capacity and in expression patterns. We thus suggest that neofunctionalization occurred at both the expression and the functional levels to shape RAR roles during development in vertebrates.

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Fujimura, Y, Titani K, Holland LZ, Roberts JR, Kostel P, Ruggeri ZM, Zimmerman TS.  1987.  A Heparin-Binding Domain of Human Vonwillebrand-Factor - Characterization and Localization to a Tryptic Fragment Extending from Amino-Acid Residue Val-449 to Lys-728. Journal of Biological Chemistry. 262:1734-1739.Website
Fujimura, Y, Titani K, Holland LZ, Russell SR, Roberts JR, Elder JH, Ruggeri ZM, Zimmerman TS.  1986.  Vonwillebrand-Factor - a Reduced and Alkylated 52/48-Kda Fragment Beginning at Amino-Acid Residue-449 Contains the Domain Interacting with Platelet Glycoprotein Ib. Journal of Biological Chemistry. 261:381-385.Website
Fulcher, CA, Roberts JR, Holland LZ, Zimmerman TS.  1985.  Human Factor-Viii Procoagulant Protein - Monoclonal-Antibodies Define Precursor-Product Relationships and Functional Epitopes. Journal of Clinical Investigation. 76:117-124.   10.1172/jci111933   Website
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Gibson-Brown, JJ, Osoegawa K, McPherson JD, Waterston RH, de Jong PJ, Rokhsar DS, Holland LZ.  2003.  A proposal to sequence the amphioxus genome submitted to the joint genome institute of the US department of energy. Journal of Experimental Zoology Part B-Molecular and Developmental Evolution. 300B:5-22.   10.1002/jez.b.00042   Website
Glardon, S, Holland LZ, Gehring WJ, Holland ND.  1998.  Isolation and developmental expression of the amphioxus Pax-6 gene (AmphiPax-6): insights into eye and photoreceptor evolution. Development. 125:2701-2710. AbstractWebsite

Pax-6 genes have been identified from a broad range of invertebrate and vertebrate animals and shown to be always involved in early eye development. Therefore, it has been proposed that the various types of eyes evolved from a single eye prototype, by a Pax-6-dependent mechanism. Here we describe the characterization of a cephalochordate Pax-6 gene. The single amphioxus Pax-6 gene (AmphiPax-6) can produce several alternatively spliced transcripts, resulting in proteins with markedly different amino and carboxy termini, The amphioxus Pax-6 proteins are 92% identical to mammalian Pax-6 proteins in the paired domain and 100% identical in the homeodomain. Expression of AmphiPax-6 in the anterior epidermis of embryos may be related to development of an olfactory epithelium. Expression is also detectable in Hatschek's left diverticulum as it forms the preoral ciliated pit, part of which gives rise to the homolog of the vertebrate anterior pituitary, A zone of expression in the anterior neural plate of early embryos is carried into the cerebral vesicle (a probable diencephalic homolog) during neurulation, This zone includes cells that will differentiate into the lamellar body, a presumed homolog of the vertebrate pineal eye, In neurulae, AmphiPax-6 is also expressed in ventral cells at the anterior tip of the nerve cord; these cells are precursors of the photoreceptive neurons of the frontal eye, the presumed homolog of the vertebrate paired eyes. However, AmphiPax-6 expression was not detected in two additional types of photoreceptors, the Joseph cells or the organs of Hesse, which are evidently relatively recent adaptations (ganglionic photoreceptors) and appear to be rare exceptions to the general rule that animal photoreceptors develop from a genetic program triggered by Pax-6.

Gould-Somero, M, Holland LZ.  1974.  Timing of RNA-synthesis for Spermiogenesis in Organ-cultures of Drosophila melanogaster testes. TIWilhelm Roux Archiv fur Entwicklungsmechanik der Organismen . 174(2):133-148.
Gould-Somero, M, Holland LZ.  1975.  Fine-structural Investigation of Insemination Response in Urechis caupo . Developmental Biology . 46(2):358-369.   10.1016/0012-1606(75)90112-8  
Gould-Somero, M, Jaffe LA, Holland LZ.  1979.  Electrically Mediated Fast Polyspermy Block in Eggs of the Marine Worm, Urechis-Caupo. Journal of Cell Biology. 82:426-440.   10.1083/jcb.82.2.426   Website
Gould-Somero, M, Holland LZ.  1975.  Oocyte differentiation in Urechis caupo (Echiura)-- A Fine-structural Study. Journal of Morphology . 147(4):475-505.   10.1002/jmor.1051470407  
Gould-Somero, M, Hardy R, Holland LZ.  1974.  Y-chromosome and Sperm Length in D. melanogaster. Experimental Cell Research . 87(2):397-398.   10.1016/0014-4827(74)90500-X  
Gould-Somero, M, Holland LZ, Paul M.  1977.  Cytochalasin-B Inhibits Sperm Penetration into eggs of Urechis caupo (Echiura). Developmental Biology. 58(1):11-22.   10.1016/0012-1606(77)90071-9  
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Holland, LZ.  2015.  The origin and evolution of chordate nervous systems. Philosophical Transactions of the Royal Society B-Biological Sciences. 370   10.1098/rstb.2015.0048   AbstractWebsite

In the past 40 years, comparisons of developmental gene expression and mechanisms of development (evodevo) joined comparative morphology as tools for reconstructing long-extinct ancestral forms. Unfortunately, both approaches typically give congruent answers only with closely related organisms. Chordate nervous systems are good examples. Classical studies alone left open whether the vertebrate brain was a new structure or evolved from the anterior end of an ancestral nerve cord like that of modern amphioxus. Evodevo plus electron microscopy showed that the amphioxus brain has a diencephalic forebrain, small midbrain, hindbrain and spinal cord with parts of the genetic mechanisms for the midbrain/hindbrain boundary, zona limitans intrathalamica and neural crest. Evodevo also showed how extra genes resulting from whole-genome duplications in vertebrates facilitated evolution of new structures like neural crest. Understanding how the chordate central nervous system (CNS) evolved from that of the ancestral deuterostome has been truly challenging. The majority view is that this ancestor had a CNS with a brain that gave rise to the chordate CNS and, with loss of a discrete brain, to one of the two hemichordate nerve cords. The minority view is that this ancestor had no nerve cord; those in chordates and hemichordates evolved independently. New techniques such as phylostratigraphy may help resolve this conundrum.