Analysis of type IX collagen in zebrafish axial development

ANALYSIS OF TYPE IX COLLAGEN IN ZEBRAFISH AXIAL DEVELOPMENT SUDHA PUTTUR MUDUMANA NATIONAL UNIVERSITY OF SINGAPORE 2003 ANALYSIS OF TYPE IX COLLAGEN IN ZEBRAFISH AXIAL DEVELOPMENT SUDHA PUTTUR MUDUMANA (B.F.Sc, M.F.Sc, College of Fisheries, University of Agricultural Sciences, Bangalore, India) A THESIS SUBMITTED FOR THE DOCTOR OF PHILOSOPHY DEPARTMENT OF BIOLOGICAL SCIENCES NATIONAL UNIVERSITY OF SINGAPORE 2003 If we knew what it was we were doing, it would not be called research, would it? --Albert Einstein Acknowledgements ACKNOWLEDGEMENTS In the course of past few years, I am honored that I have had the opportunity to work with so many brilliant people, who have achieved much in their field of work. First and foremost, I would like to thank my supervisors, A/P Zhiyuan Gong and A/P Vladimir Korzh for their guidance, innovative insight and constant support throughout my study. If not for their foresight and unsurpassed knowledge of zebrafish development, this work would have never achieved this stage. I also wish to thank my thesis advisory committee members, A/P Sin Yoke Min and A/P Leung Ka Yin for their valuable inputs during the course of this work. It was my luck that I got into one of the most vibrant and friendly labs on campus. I will always be thankful that I met and had the pleasure of being around a cheerful, friendly and helpful gang of people. A big thanks to Jiangyan, Yan Tie, Bensheng, Yan Fei, Wang Hai, Xukun, Zeng Sheng, Hai Yan, Jacqueline, Jennifer, Yilian, Shan Tao, Safia, Simon, Li Zhen, Tong Yan, Dilhan, Tuan Leng, Ke, Xingjun, Siew Hong, Pan, Zeng, Shalin, Prakash, Jane, Hui Qing, Hu Jing and Xiao Ming for everything. I wish to thank all the help and technical assistance given by the great bunch of people at the office and other facilities in the department including Joan, Cynthia, Jessie, Ms. Chan, Reena, Sally, Ms. Tan, Ann Nee, Mr. Loh, Salim, Wai Peng, Chong Mun, Allan, Subha, Chye Fong, Mr. Cheong, Veronica and Ms. Chew. Special thanks goes to Dr. Korzh and his intelligent and humble group of researchers. I learnt a great deal from them not just in doing good research and reasoning but also in becoming a better person and developing confidence to face the challenges of life. The long hours spend in discussing various strategies and hypothesis to tackle the mysterious ways of vertebrate development are the memories I would always cherish for many years to come. In particular, for the guidance, help and for making me feel at home, I will always be thankful to Inna, Sasha, Michael, Lee Thean, Steven, Shang Wei, Cathleen, Eric, Lana, Kar Lai, Chai Chou, Sergei, Dmitri, Igor, Mike and Gao Rong. Thanks for critically evaluating my work and Michael, special thanks to you for going through my thesis. Thank you guys! The help rendered by the ever-smiling and helpful aunties and Chin Heng at the IMA/IMCB/TLL fish facility and other people at the institute are greatly appreciated. My stay in Singapore was one of the most memorable of my life. I made great friends who always provided the fun environment that’s a must in a researcher’s life. Thanks goes to Kiran, Vineet, Gagan, Deepak, Ashu, Pattabi, Sharmila, Nidhi, Shalini, Bindya, Sowmya, Naslin, Neeyor, Iti, Bala, Sidd, Surya, Sudhir, King, Akshay, Lovelin, Mona, Amrit, Rajat, May, Mariam, Madhavi, Shibu, Senthil, Dhruba, Srinivas, Ashok, Joseph, Sasi for being there always for me. Thanks EC! No word could sufficiently describe the happiness I feel in having Tushar as my best friend. His cheerful and happy demeanor always brought back smile to my face in every trying circumstance. Thanks are due to Aunty, Uncle and Tarun for their love. I am lucky that I have the greatest parents and sisters in the world. They always had total confidence in me that I could achieve what I set out to do. Thanks a lot my dearest Dad and Mom. Thanks Sandhya and Sindhu for being the greatest friends and loving sisters. Thanks Arvind, Parameswaran, Anshu and Sreenath for bringing happiness to our lives. Finally, I wish to extend my greatest appreciation to National University of Singapore for providing me the graduate research scholarship during the course of my study. God Bless Everyone! i Table of Contents CONTENTS ACKNOWLEDGEMENTS………………………………………………………… i TABLE OF CONTENTS…………………………………………………………… ii LIST OF FIGURES………………………………………………………………… viii LIST OF TABLES…………………………………………………………………… xi LIST OF ABBREVIATIONS…………………………………………………………. xii LIST OF PUBLICATIONS…………………………………………………………… xv SUMMARY……………………………………………………………………………. xvii I. INTRODUCTION………………………………………………………… 1.1 Zebrafish as a model organism in developmental biology………………. 1.2 Zebrafish development……………………………………………………. 1.2.1 Anatomical staging of development…………………………………… . 1.2.1.1 Cleavage and Blastula (¾ - hpf)………………………………………. 1.2.1.2 Gastrulation (4 – 10 hpf)…………………………………………………. 1.2.1.3 Segmentation (101/3 – 36 hpf) …………………………………………… 1.2.1.4 Pharyngula (36 – 48 hpf)…………………………………………………. 12 1.2.1.5 Hatching (>48 hpf)………………………………………………………… 12 1.2.2 Zebrafish Axis development………………………………………………. 12 1.2.3 Induction and function of the axial structures……………………… …. 13 1.2.3.1 Notochord.…………………………………………………………………. 15 1.2.3.2 Floor plate………………………………………………………………… . 17 1.2.3.3 Hypochord………………………………………………………………… 20 1.3 Extracellular matrix (ECM) proteins ……………………………………. 20 1.3.1 ECM in axial structures…………………………………………………… 20 1.3.2 ECM in development……………………………………………………… 22 1.4 Collagen gene family………………… ………………………………… . 25 ii Table of Contents 1.4.1 Structural organization of collagen gene……………………………….… 26 1.4.2 Classification of collagen genes………………………………………….… 27 1.4.2.1 Fibrillar collagens………………………………………………………… 28 1.4.2.2 Basement membrane collagens…………………………………………… 30 1.4.2.3 Network collagens…………………………………………………………. 32 1.4.2.4 Microfibril collagens……………………………………………………… 32 1.4.2.5 Anchoring fibrils with interrupted triple helix (long-chain collagen)… . 32 1.4.2.6 Transmembrane collagens…………………………………………….… . 32 1.4.2.7 Endostatin forming collagens……………………………………………… 33 1.4.2.8 Fibril associated collagens with interrupted helices (FACIT)…………… 33 1.4.3 Mutations of collagen genes and diseases .……………………………… 36 1.5 Morphogenetic role of extracellular matrix proteins…………………… 39 1.6 Rationale of the proposed study………………………………………… 44 1.6.1 Role of collagens in development………………………………………… . 44 1.6.2 Objectives………………………………………………………………… . 45 II. MATERIALS AND METHODS…………………………………………. 48 2.1 Cloning and mapping………………………………………….………… 49 2.1.1 DNA isolation……………………………………………………………… 49 2.1.1.1 Isolation and purification of plasmid DNA………………………………. 49 2.1.1.2 Isolation of genomic DNA…………………………………………………. 50 2.1.1.3 Isolation of DNA from agarose gel………………………………………… 50 2.1.2 Restriction endonuclease digestion of plasmid DNA……………………. 51 2.1.2.1 Incubation with restriction endonuclease………………………………… 51 2.1.2.2 Precipitation of digested fragment……………………………………… . 51 2.1.2.3 Quantification of DNA by gel electrophoresis……………………………. 52 2.1.2.4 Quantification of DNA by spectrophotometry…………………………… 52 2.1.3 Purification of PCR products…………………………………………… 52 2.1.4 DNA ligation………………………………………………………………. 53 2.1.5 Transformation…………………………………………………………… 53 2.1.5.1 Preparation of competent cells……………………………………………. 53 2.1.5.2 Transformation……………………………………………………………. 54 iii Table of Contents 2.1.6 Subdividing cDNA library………………………………………………… 55 2.1.7 Isolation of RNA…………………………………………………………… 55 2.1.7.1 Isolation of total RNA from tissue or embryos…………………………… 55 2.1.7.2 Measurement of RNA concentration……………………………………… 56 2.1.7.3 RNA gel electrophoresis…………………………………………………… 56 2.1.7.4 Synthesis of 5’ capped mRNA…………………………………………… . 56 2.1.8 Polymerase chain reaction (PCR)…………………………………………. 57 2.1.8.1 Standard PCR…………………………………………………………….… 57 2.1.8.2 Reverse-transcriptase PCR (RT-PCR)……………………………………. 58 2.1.8.3 5’ Rapid amplification of cDNA ends (5’ RACE)………………………… 58 2.1.8.4 Colony screening PCR……………………………………………………… 59 2.1.8.5 Cloning of PCR products………………………………………………… 60 2.1.9 Sequencing of double-stranded DNA……………………………………… 60 2.1.9.1 Manual sequencing…………………………………………………………. 60 2.1.9.2 Automatic sequencing……………………………………………………… 61 2.1.10 Radiation hybrid mapping…………………………………………………. 62 2.1.11 Phylogenetic analyses………………………………………………………. 62 2.1.12 Vectors used………………………………………………………………… 63 2.1.12.1 pBluescript SK(+/-)…………………………………………………………. 63 2.1.12.2 pT7Blue……………………………………………………………………… 64 2.1.12.3 pGEMT…………………………………………………………………… . 65 2.1.12.4 pBK-CMV………………………………………………………………… 66 2.2 Expression analyses………………………………………………………… 67 2.2.1 Zebrafish……………………………………………………………………. 67 2.2.1.1 Wild type zebrafish.……………………………………………………… . 67 2.2.1.2 Mutant lines of zebrafish………………………………………………… . 68 2.2.1.3 Stages of embryonic development…………………………………………. 68 2.2.2 In situ hybridization……………………………………………………… . 69 2.2.2.1 Synthesis of labeled RNA probe…………………………………………… 69 2.2.2.1.1 Linearization of plasmid DNA…………………………………………… . 69 2.2.2.1.2 Probe incubation and precipitation……………………………………… 70 iv Table of Contents 2.2.2.1.3 Quantification of labeled probe……………….….…………………… 70 2.2.2.2 Whole-mount in situ hybridization……………….………………… . 70 2.2.2.2.1 Preparation of zebrafish embryos……………………………………. 70 2.2.2.2.2 Proteinase K treatment……………………………………………… 71 2.2.2.2.3 Prehybridization………………………………………………………. 72 2.2.2.2.4 Hybridization………………………………………………………… 72 2.2.2.2.5 Post-Hybridization washes…………………………………………… 72 2.2.2.2.6 Antibody Incubation………………………………………………… 73 2.2.2.2.6.1 Preparation of preabsorbed DIG antibody…………………………… 73 2.2.2.2.6.2 Incubation with preabsorbed antibodies……………………………… 73 2.2.2.2.7 Color Development…………………………………………………… . 73 2.2.2.2.8 Mounting and photography……………………………………………. 74 2.2.2.3 Cryosectioning embryos……………………………………………… 74 2.2.2.3.1 Preparation of slides and blocks………………………………………. 75 2.2.2.3.2 Sectioning, mounting and photography………………………………. 75 2.2.2.4 Alcian blue staining of cartilage tissues………………………………. 76 2.3 Protein applications……………………………………………………. 76 2.3.1 Extraction of protein…………………………………………………… 76 2.3.2 Western blotting of protein samples…………………………………… 77 2.3.2.1 Estimation of protein concentration…………………………………… 77 2.3.2.2 Preparation and running the gel………………………………………. 78 2.3.2.3 Western blotting……………………………………………………… . 79 2.3.3 Immunoblotting with antibodies……………………………………… 79 2.4 Functional analyses…………………………………………………… 80 2.4.1 Microinjection into embryos………………………………………… . 80 2.4.2 Design of anti-sense morpholinos……………………………………… 81 2.4.3 Animal cap assay and re-integration experiments…………………… 81 III. RESULTS………………………………………………………………. 82 3.1 Characterization of zebrafish colIXα2 gene………………………… 3.1.1 Isolation of full length sequence of colIXα2…………………………… 83 3.1.2 Sequence features of zebrafish colIXα2……………………………… 84 83 v Table of Contents 3.1.3 Phylogenetic analyses of FACIT collagens…………………………… 89 3.1.4 Genomic mapping and synteny analyses……………………………… 90 3.2 Expression analyses of colIXα2 in zebrafish by RT-PCR……………. 94 3.3 Expression analyses of colIXα2 in embryonic zebrafish by WISH……………………………………………………………… 95 3.3.1 Expression of colIXα2 during segmentation period (10.3 – 36 hpf) …………………………………………………………. 95 3.3.2 Expression of colIXα2 during post-segmentation period (>36 hpf) ………………………………………………………………. 98 3.4 Expression analyses of colIXα1 and colIXα3 in embryonic zebrafish…………………………………………………… 101 3.5 Functional analysis of colIXα2 using anti-sense morpholino oligonucleotides…………………………………………………………107 3.5.1 Classification of phenotypical abnormalities in embryos caused by inhibition of translation of colIXα2………………………. 107 3.5.2 Inhibition of colIXα2 caused defects in various cell populations…… 112 3.5.2.1 colIXα2 plays a role in establishing integrity of axial mesoderm… . 112 3.5.2.2 Inhibition of ColIXα2 resulted in loss of reintegration of cells in vitro…………………………………………………………… 116 3.5.2.3 ColIXα2 is required for maintenance of the floor plate identity…… 119 3.5.2.4 Inhibition of colIXα2 affects somite organization………………… . 122 3.5.2.5 colIXα2 affects integrity of sclerotome, cartilage and neural crest…. 125 3.5.2.6 colIXα2 affects integrity of epithelium………………………………. 128 3.5.2.6.1 Expression of cadherins was affected in anti-colIXα2MO injected embryos…………………………………………………… . 128 3.5.2.6.2 Reduction of expression of integrin-α6 in anti-colIXα2MO injected embryos……………………………………………………………… 131 3.6 Regulation of colIXα2 expression in zebrafish development……… 135 3.6.1 colIXα2 expression in axial structures is independent of the notochord…………………………………………………………. 135 3.6.2 colIXα2 transcription is regulated by TGFβ signalling…………… . 139 3.6.3 colIXα2 expression in floor plate depends on Nodal signaling……… 141 vi Table of Contents IV. DISCUSSION……………………………………………………… 147 4.1 Zebrafish colIXα2 belongs to the unique family of FACIT collagens 148 4.2 Genome mapping of colIXα2 reveals a conserved synteny………… 150 4.3 Zebrafish Collagen IX chains are expressed in the axial structures… 150 4.4 colIXα2 express in a unique temporal order in zebrafish axis…… 156 4.5 colIXα2 might play a role in craniofacial development…………… . 157 4.6 ColIXα2 and the integrity of tissues………….………………………. 160 4.7 ColIXα2 and somite patterning………………………………………. 166 4.8 colIXα2 expression in floor plate is independent of notochord…… . 168 4.9 colIXα2 is regulated by TGF-β pathway molecules………………… 168 4.10 colIXα2 and determination of non-notochordal axial precursors…. 171 4.11 Concluding remarks………………………………………………… 175 V. CONCLUSION ………………………………………………………. 177 VI. REFERENCES……………………………………………………… 181 vii References Miyagoe,Y., Hanaoka,K., Nonaka,I., Hayasaka,M., Nabeshima,Y., Arahata,K., Nabeshima,Y., and Takeda,S. (1997). Laminin alpha2 chain-null mutant mice by targeted disruption of the Lama2 gene: a new model of merosin (laminin 2)-deficient congenital muscular dystrophy. FEBS Lett. 415:33-39. Montesano,R. (1986). Cell-extracellular matrix interactions in morphogenesis: an in vitro approach. Experientia 42:977-985. Moon,R.T. (1993). In pursuit of the functions of the Wnt family of developmental regulators: insights from Xenopus laevis. Bioessays 15:91-97. Morin-Kensicki,E.M. and Eisen,J.S. (1997). Sclerotome development and peripheral nervous system segmentation in embryonic zebrafish. Development 124:159167. Mudumana,S.P., Wan,H., Korzh,V., and Gong,Z. (2004). Expression analyses of zebrafish transferrin, ifabp, and elastaseB mRNAs as differentiation markers for the three major endodermal organs: Liver, intestine, and exocrine pancreas. Dev. Dyn. 230:165-173. Muragaki,Y., Mariman,E.C., van Beersum,S.E., Perala,M., van Mourik,J.B., Warman,M.L., Hamel,B.C., and Olsen,B.R. (1996). A mutation in COL9A2 causes multiple epiphyseal dysplasia (EDM2). Ann.N.Y.Acad.Sci. 785:303306. Murata,H., Zhou,L., Ochoa,S., Hasan,A., Badiavas,E., and Falanga,V. (1997). TGFbeta3 stimulates and regulates collagen synthesis through TGF-beta1dependent and independent mechanisms. J.Invest Dermatol. 108:258-262. Murcia,C.L. and Woychik,R.P. (2001). Expression of Pcdh15 in the inner ear, nervous system and various epithelia of the developing embryo. Mech.Dev. 105:163166. Myllyharju,J. and Kivirikko,K.I. (2001). Collagens and collagen-related diseases. Ann.Med. 33:7-21. Nah,H.D., Barembaum,M., and Upholt,W.B. (1992). The chicken alpha (XI) collagen gene is widely expressed in embryonic tissues. J.Biol.Chem. 267:22581-22586. Nasevicius,A. and Ekker,S.C. (2000). Effective targeted gene 'knockdown' in zebrafish. Nat.Genet. 26:216-220. Ninomiya,Y., van der,R.M., Mayne,R., Lozano,G., and Olsen,B.R. (1985). Construction and characterization of cDNA encoding the alpha chain of chicken type IX collagen. Biochemistry 24:4223-4229. Nishimura,I., Muragaki,Y., and Olsen,B.R. (1989). Tissue-specific forms of type IX collagen-proteoglycan arise from the use of two widely separated promoters. J.Biol.Chem. 264:20033-20041. 200 References Noakes,P.G., Gautam,M., Mudd,J., Sanes,J.R., and Merlie,J.P. (1995). Aberrant differentiation of neuromuscular junctions in mice lacking s-laminin/laminin beta 2. Nature 374:258-262. Nornes,S., Mikkola,I., Krauss,S., Delghandi,M., Perander,M., and Johansen,T. (1996). Zebrafish Pax9 encodes two proteins with distinct C-terminal transactivating domains of different potency negatively regulated by adjacent N-terminal sequences. J.Biol.Chem. 271:26914-26923. Odenthal,J., Haffter,P., Vogelsang,E., Brand,M., van Eeden,F.J., Furutani-Seiki,M., Granato,M., Hammerschmidt,M., Heisenberg,C.P., Jiang,Y.J., Kane,D.A., Kelsh,R.N., Mullins,M.C., Warga,R.M., Allende,M.L., Weinberg,E.S., and Nusslein-Volhard,C. (1996). Mutations affecting the formation of the notochord in the zebrafish, Danio rerio. Development 123:103-115. Odenthal,J. and Nusslein-Volhard,C. (1998). fork head domain genes in zebrafish. Dev.Genes Evol. 208:245-258. Odenthal,J., van Eeden,F.J., Haffter,P., Ingham,P.W., and Nusslein-Volhard,C. (2000). Two distinct cell populations in the floor plate of the zebrafish are induced by different pathways. Dev.Biol. 219:350-363. Olsen,B.R. (1995). New insights into the function of collagens from genetic analysis. Curr.Opin.Cell Biol. 7:720-727. Olsen,B.R. (1997). Collagen IX. Int.J.Biochem.Cell Biol. 29:555-558. Onda,H., Poulin,M.L., Tassava,R.A., and Chiu,I.M. (1991). Characterization of a newt tenascin cDNA and localization of tenascin mRNA during newt limb regeneration by in situ hybridization. Dev.Biol. 148:219-232. Oppenheimer, J.M. (1936). Structures developed in amphibians by implantation of living fish organizer. Proc. Soc. exp. Biol. Med. 34:461-463. Orentas,D.M., Hayes,J.E., Dyer,K.L., and Miller,R.H. (1999). Sonic hedgehog signaling is required during the appearance of spinal cord oligodendrocyte precursors. Development 126:2419-2429. Osaki,M., Tan,L., Choy,B.K., Yoshida,Y., Cheah,K.S., Auron,P.E., and Goldring,M.B. (2003). The TATA-containing core promoter of the type II collagen gene (COL2A1) is the target of interferon-gamma-mediated inhibition in human chondrocytes: requirement for Stat1 alpha, Jak1 and Jak2. Biochem.J. 369:103-115. Ozawa,M., Baribault,H., and Kemler,R. (1989). The cytoplasmic domain of the cell adhesion molecule uvomorulin associates with three independent proteins structurally related in different species. EMBO J. 8:1711-1717. Paassilta,P., Pihlajamaa,T., Annunen,S., Brewton,R.G., Wood,B.M., Johnson,C.C., Liu,J., Gong,Y., Warman,M.L., Prockop,D.J., Mayne,R., and Ala-Kokko,L. 201 References (1999a). Complete sequence of the 23-kilobase human COL9A3 gene. Detection of Gly-X-Y triplet deletions that represent neutral variants. J.Biol.Chem. 274:22469-22475. Paassilta,P., Lohiniva,J., Annunen,S., Bonaventure,J., Le Merrer,M., Pai,L., and AlaKokko,L. (1999b). COL9A3: A third locus for multiple epiphyseal dysplasia. Am.J.Hum.Genet. 64:1036-1044. Panayotou,G., End,P., Aumailley,M., Timpl,R., and Engel,J. (1989). Domains of laminin with growth-factor activity. Cell 56:93-101. Parsons,M.J., Pollard,S.M., Saude,L., Feldman,B., Coutinho,P., Hirst,E.M., and Stemple,D.L. (2002). Zebrafish mutants identify an essential role for laminins in notochord formation. Development 129:3137-3146. Patton,B.L., Miner,J.H., Chiu,A.Y., and Sanes,J.R. (1997). Distribution and function of laminins in the neuromuscular system of developing, adult, and mutant mice. J.Cell Biol. 139:1507-1521. Peifer,M. (1997). Beta-catenin as oncogene: the smoking gun. Science 275:17521753. Pelegri,F. and Maischein,H.M. (1998). Function of zebrafish beta-catenin and TCF-3 in dorsoventral patterning. Mech.Dev. 77:63-74. Perälä,M., Hanninen,M., Hastbacka,J., Elima,K., and Vuorio,E. (1993). Molecular cloning of the human alpha 2(IX) collagen cDNA and assignment of the human COL9A2 gene to chromosome 1. FEBS Lett. 319:177-180. Perälä,M., Elima,K., Metsaranta,M., Rosati,R., de Crombrugghe,B., and Vuorio,E. (1994). The exon structure of the mouse alpha 2(IX) collagen gene shows unexpected divergence from the chick gene. J.Biol.Chem. 269:5064-5071. Perälä,M., Savontaus,M., Metsaranta,M., and Vuorio,E. (1997). Developmental regulation of mRNA species for types II, IX and XI collagens during mouse embryogenesis. Biochem.J. 324 ( Pt 1):209-216. Perrimon,N. and Bernfield,M. (2000). Specificities of heparan sulphate proteoglycans in developmental processes. Nature 404:725-728. Perris,R. and Perissinotto,D. (2000). Role of the extracellular matrix during neural crest cell migration. Mech.Dev. 95:3-21. Pihlajamaa,T., Vuoristo,M.M., Annunen,S., Perala,M., Prockop,D.J., and AlaKokko,L. (1998). Human COL9A1 and COL9A2 genes. Two genes of 90 and 15 kb code for similar polypeptides of the same collagen molecule. Matrix Biol. 17:237-241. Piotrowski,T., Schilling,T.F., Brand,M., Jiang,Y.J., Heisenberg,C.P., Beuchle,D., Grandel,H., van Eeden,F.J., Furutani-Seiki,M., Granato,M., Haffter,P., 202 References Hammerschmidt,M., Kane,D.A., Kelsh,R.N., Mullins,M.C., Odenthal,J., Warga,R.M., and Nusslein-Volhard,C. (1996). Jaw and branchial arch mutants in zebrafish II: anterior arches and cartilage differentiation. Development 123:345-356. Placzek,M., Tessier-Lavigne,M., Yamada,T., Jessell,T., and Dodd,J. (1990). Mesodermal control of neural cell identity: floor plate induction by the notochord. Science 250:985-988. Placzek,M., Jessell,T.M., and Dodd,J. (1993). Induction of floor plate differentiation by contact-dependent, homeogenetic signals. Development 117:205-218. Placzek,M., Dodd,J., and Jessell,T.M. (2000). Discussion point. The case for floor plate induction by the notochord. Curr.Opin.Neurobiol. 10:15-22. Pons,S. and Marti,E. (2000). Sonic hedgehog synergizes with the extracellular matrix protein vitronectin to induce spinal motor neuron differentiation. Development 127:333-342. Postlethwait,J.H., Yan,Y.L., Gates,M.A., Horne,S., Amores,A., Brownlie,A., Donovan,A., Egan,E.S., Force,A., Gong,Z., Goutel,C., Fritz,A., Kelsh,R., Knapik,E., Liao,E., Paw,B., Ransom,D., Singer,A., Thomson,M., Abduljabbar,T.S., Yelick,P., Beier,D., Joly,J.S., Larhammar,D., Rosa,F., and . (1998). Vertebrate genome evolution and the zebrafish gene map. Nat.Genet. 18:345-349. Postlethwait,J.H., Woods,I.G., Ngo-Hazelett,P., Yan,Y.L., Kelly,P.D., Chu,F., Huang,H., Hill-Force,A., and Talbot,W.S. (2000). Zebrafish comparative genomics and the origins of vertebrate chromosomes. Genome Res. 10:18901902. Pourquie,O. (2001). Vertebrate somitogenesis. Annu.Rev.Cell Dev.Biol. 17:311-350. Pourquie,O., Coltey,M., Teillet,M.A., Ordahl,C., and Le Douarin,N.M. (1993). Control of dorsoventral patterning of somitic derivatives by notochord and floor plate. Proc.Natl.Acad.Sci.U.S.A 90:5242-5246. Prater,C.A., Plotkin,J., Jaye,D., and Frazier,W.A. (1991). The properdin-like type I repeats of human thrombospondin contain a cell attachment site. J. Cell Biol. 112:1031-1040. Preissner,K.T. (1991). Structure and biological role of vitronectin. Annu.Rev.Cell Biol. 7:275-310. Pringle,N.P., Yu,W.P., Guthrie,S., Roelink,H., Lumsden,A., Peterson,A.C., and Richardson,W.D. (1996). Determination of neuroepithelial cell fate: induction of the oligodendrocyte lineage by ventral midline cells and sonic hedgehog. Dev.Biol. 177:30-42. 203 References Prockop,D.J. and Kivirikko,K.I. (1995). Collagens: molecular biology, diseases, and potentials for therapy. Annu.Rev.Biochem. 64:403-434. Ramirez,F. and Di Liberto,M. (1990). Complex and diversified regulatory programs control the expression of vertebrate collagen genes. FASEB J. 4:1616-1623. Ramirez,F., Boast,S., D'Alessio,M., Prince,J., Su,M.W., and Vissing,H. (1989). Molecular pathobiology of human collagens. Connect.Tissue Res. 21:79-88. Rastegar,S., Albert,S., Le,R., I, Fischer,N., Blader,P., Muller,F., and Strahle,U. (2002). A floor plate enhancer of the zebrafish netrin1 gene requires Cyclops (Nodal) signalling and the winged helix transcription factor FoxA2. Dev.Biol. 252:1-14. Rebagliati,M.R., Weeks,D.L., Harvey,R.P., and Melton,D.A. (1985). Identification and cloning of localized maternal RNAs from Xenopus eggs. Cell 42:769-777. Rebagliati,M.R., Toyama,R., Fricke,C., Haffter,P., and Dawid,I.B. (1998a). Zebrafish nodal-related genes are implicated in axial patterning and establishing leftright asymmetry. Dev.Biol. 199:261-272. Rebagliati,M.R., Toyama,R., Haffter,P., and Dawid,I.B. (1998b). cyclops encodes a nodal-related factor involved in midline signaling. Proc.Natl.Acad.Sci.U.S.A 95:9932-9937. Reichenberger,E., and Olsen,B.R. (1996). Collagens as organizers of extracellular matrix during morphogenesis. Sem. Cell Dev. Biol.7:631-638. Reilly,K.M. and Melton,D.A. (1996). Short-range signaling by candidate morphogens of the TGF beta family and evidence for a relay mechanism of induction. Cell 86:743-754. Renucci,A., Lemarchandel,V., and Rosa,F. (1996). An activated form of type I serine/threonine kinase receptor TARAM-A reveals a specific signalling pathway involved in fish head organiser formation. Development 122:37353743. Ridley, A.J., Paterson, H.F., Johnston, C.L., Diekman, D. and Hall, A. (1992). The small GTP-binding protein rac regulates growth factor-induced membrane ruffling. Cell 70:401-410. Rimoin, D.L. (1996). Molecular defects in the chondrodysplasias. Am J Med Genet. 63:106-10. Ring,C., Hassell,J., and Halfter,W. (1996). Expression pattern of collagen IX and potential role in the segmentation of the peripheral nervous system. Dev.Biol. 180:41-53. 204 References Riou, J.F., Umbhauer, M., Shi, D.L., and Boucaut, J.C. (1992) Tenascin: a potential modulator of cell-extracellular matrix interactions during vertebrate embryogenesis. Biol Cell. 75:1-9. Roelink,H., Augsburger,A., Heemskerk,J., Korzh,V., Norlin,S., Altaba,A., Tanabe,Y., Placzek,M., Edlund,T., Jessell,T.M., and . (1994). Floor plate and motor neuron induction by vhh-1, a vertebrate homolog of hedgehog expressed by the notochord. Cell 76:761-775. Roelink,H., Porter,J.A., Chiang,C., Tanabe,Y., Chang,D.T., Beachy,P.A., and Jessell,T.M. (1995). Floor plate and motor neuron induction by different concentrations of the amino-terminal cleavage product of sonic hedgehog autoproteolysis. Cell 81:445-455. Rose,C.S. and Malcolm,S. (1997). A TWIST in development. Trends Genet. 13:384387. Roskelly,C.D., Srebrow,A., and Bissell,M.J. (1995). A hierarchy of ECM-mediated signalling regulates tissue-specific gene expression. Curr. Opin. Cell Biol.7:736-747. Ruiz I Altaba, A. (1996). Coexpression of HNF-3 beta and Isl-1/2 and mixed distribution of ventral cell types in the early neural tube. Int.J.Dev.Biol. 40:1081-1088. Ruiz I Altaba,A. and Jessell,T.M. (1993). Midline cells and the organization of the vertebrate neuraxis. Curr.Opin.Genet.Dev. 3:633-640. Runyan,R.B., Potts,J.D., Sharma,R.V., Loeber,C.P., Chiang,J.J., and Bhalla,R.C. (1990). Signal transduction of a tissue interaction during embryonic heart development. Cell Regul. 1:301-313. Ruoslahti,E. (1999). Fibronectin and its integrin receptors in cancer. Adv.Cancer Res. 76:1-20. Ryan,M.C. and Sandell,L.J. (1990). Differential expression of a cysteine-rich domain in the amino-terminal propeptide of type II (cartilage) procollagen by alternative splicing of mRNA. J.Biol.Chem. 265:10334-10339. Ryan,M.C., Christiano,A.M., Engvall,E., Wewer,U.M., Miner,J.H., Sanes,J.R., and Burgeson,R.E. (1996). The functions of laminins: lessons from in vivo studies. Matrix Biol.15:369-381. Ryan,M.C., Lee,K., Miyashita,Y., and Carter,W.G. (1999). Targeted disruption of the LAMA3 gene in mice reveals abnormalities in survival and late stage differentiation of epithelial cells. J.Cell Biol. 145:1309-1323. Saarela,J., Ylikarppa,R., Rehn,M., Purmonen,S., and Pihlajaniemi,T. (1998). Complete primary structure of two variant forms of human type XVIII 205 References collagen and tissue-specific differences in the expression of the corresponding transcripts. Matrix Biol. 16:319-328. Sado,Y., Kagawa,M., Naito,I., Ueki,Y., Seki,T., Momota,R., Oohashi,T., and Ninomiya,Y. (1998). Organization and expression of basement membrane collagen IV genes and their roles in human disorders. J.Biochem.(Tokyo) 123:767-776. Saga,Y., Yagi,T., Ikawa,Y., Sakakura,T., and Aizawa,S. (1992). Mice develop normally without tenascin. Genes Dev. 6:1821-1831. Sage,E.H. and Bornstein,P. (1991). Extracellular proteins that modulate cell-matrix interactions. SPARC, tenascin, and thrombospondin. J.Biol.Chem. 266:1483114834. Sagerström,C.G., Grinbalt,Y., and Sive,H. (1996). Anteroposterior patterning in the zebrafish, Danio rerio: an explant assay reveals inductive and suppressive cell interactions. Development 122:1873-1883. Sampath,K., Rubinstein,A.L., Cheng,A.M., Liang,J.O., Fekany,K., Solnica-Krezel,L., Korzh,V., Halpern,M.E., and Wright,C.V. (1998). Induction of the zebrafish ventral brain and floorplate requires cyclops/nodal signalling. Nature 395:185189. Sandell,L.J. (1994). In situ expression of collagen and proteoglycan genes in notochord and during skeletal development and growth. Microsc.Res.Tech. 28:470-482. Sandell,L.J., Morris,N., Robbins,J.R., and Goldring,M.B. (1991). Alternatively spliced type II procollagen mRNAs define distinct populations of cells during vertebral development: differential expression of the amino-propeptide. J.Cell Biol. 114:1307-1319. Sandell,L.J., Nalin,A.M., and Reife,R.A. (1994). Alternative splice form of type II procollagen mRNA (IIA) is predominant in skeletal precursors and noncartilaginous tissues during early mouse development. Dev.Dyn. 199:129-140. Sanger,F., Nicklen,S., and Coulson,A.R. (1977). DNA sequencing with chainterminating inhibitors. Proc.Natl.Acad.Sci.U.S.A 74:5463-5467. Sasai,Y., Lu,B., Steinbeisser,H., Geissert,D., Gont,L.K., and De Robertis,E.M. (1994). Xenopus chordin: a novel dorsalizing factor activated by organizerspecific homeobox genes. Cell 79:779-790. Sasaki,H. and Hogan,B.L. (1996). Enhancer analysis of the mouse HNF-3 beta gene: regulatory elements for node/notochord and floor plate are independent and consist of multiple sub-elements. Genes Cells 1:59-72. Sasaki,T., Fukai,N., Mann,K., Gohring,W., Olsen,B.R., and Timpl,R. (1998). Structure, function and tissue forms of the C-terminal globular domain of 206 References collagen XVIII containing the angiogenesis inhibitor endostatin. EMBO J. 17:4249-4256. Savontaus,M., Metsaranta,M., and Vuorio,E. (1997). Mutation in type II collagen gene disturbs spinal development and gene expression patterns in transgenic Del1 mice. Lab Invest 77:591-600. Savontaus,M., Ihanamaki,T., Perala,M., Metsaranta,M., Sandberg-Lall,M., and Vuorio,E. (1998). Expression of type II and IX collagen isoforms during normal and pathological cartilage and eye development. Histochem.Cell Biol. 110:149-159. Schaller,M.D. and Parsons,J.T. (1994). Focal adhesion kinase and associated proteins. Curr.Opin.Cell Biol. 6:705-710. Schauerte,H.E., van Eeden,F.J., Fricke,C., Odenthal,J., Strahle,U., and Haffter,P. (1998). Sonic hedgehog is not required for the induction of medial floor plate cells in the zebrafish. Development 125:2983-2993. Scheer, N., and Campos-Ortega, J.A. (1999). Use of the GAL4-UAS technique for targeted gene expression in the zebrafish. Mech Dev 80:153-158. Scheer, N., Groth, A., Hans, S., and Campos-Ortega, J.A. (2001). An instructive function for Notch in promoting gliogenesis in the zebrafish retina. Development. 128: 1099-1107. Schier,A.F. and Shen,M.M. (2000). Nodal signalling in vertebrate development. Nature 403:385-389. Schier,A.F., Neuhauss,S.C., Helde,K.A., Talbot,W.S., and Driever,W. (1997). The one-eyed pinhead gene functions in mesoderm and endoderm formation in zebrafish and interacts with no tail. Development 124:327-342. Schilling,T.F., Piotrowski,T., Grandel,H., Brand,M., Heisenberg,C.P., Jiang,Y.J., Beuchle,D., Hammerschmidt,M., Kane,D.A., Mullins,M.C., van Eeden,F.J., Kelsh,R.N., Furutani-Seiki,M., Granato,M., Haffter,P., Odenthal,J., Warga,R.M., Trowe,T., and Nusslein-Volhard C. (1996). Jaw and branchial arch mutants in zebrafish I: branchial arches. Development 123:329-344. Schmid,B., Furthauer,M., Connors,S.A., Trout,J., Thisse,B., Thisse,C., and Mullins,M.C. (2000). Equivalent genetic roles for bmp7/snailhouse and bmp2b/swirl in dorsoventral pattern formation. Development 127:957-967. Schulte-Merker,S. (2000). Zebrafish functional genomics. Interview by Joanne Wixon. Yeast 17:232-234. Schulte-Merker,S. and Smith,J.C. (1995). Mesoderm formation in response to Brachyury requires FGF signalling. Curr.Biol. 5:62-67. 207 References Schulte-Merker,S., Ho,R.K., Herrmann,B.G., and Nusslein-Volhard,C. (1992). The protein product of the zebrafish homologue of the mouse T gene is expressed in nuclei of the germ ring and the notochord of the early embryo. Development 116:1021-1032. Schulte-Merker,S., Hammerschmidt,M., Beuchle,D., Cho,K.W., De Robertis,E.M., and Nusslein-Volhard,C. (1994a). Expression of zebrafish goosecoid and no tail gene products in wild-type and mutant no tail embryos. Development 120:843-852. Schulte-Merker,S., van Eeden,F.J., Halpern,M.E., Kimmel,C.B., and NussleinVolhard,C. (1994b). no tail (ntl) is the zebrafish homologue of the mouse T (Brachyury) gene. Development 120:1009-1015. Schwartz,M.A. and Baron,V. (1999). Interactions between mitogenic stimuli, or, a thousand and one connections. Curr.Opin.Cell Biol. 11:197-202. Selleck,S.B. (2000). Proteoglycans and pattern formation: sugar biochemistry meets developmental genetics. Trends Genet. 16:206-212. Selleck,M.A. and Stern,C.D. (1991). Fate mapping and cell lineage analysis of Hensen's node in the chick embryo. Development 112:615-626. Serafini,T., Kennedy,T.E., Galko,M.J., Mirzayan,C., Jessell,T.M., and TessierLavigne,M. (1994). The netrins define a family of axon outgrowth-promoting proteins homologous to C. elegans UNC-6. Cell 78:409-424. Serafini,T., Colamarino,S.A., Leonardo,E.D., Wang,H., Beddington,R., Skarnes,W.C., and Tessier-Lavigne,M. (1996). Netrin-1 is required for commissural axon guidance in the developing vertebrate nervous system. Cell 87:1001-1014. Seufert,D.W., Hanken,J., and Klymkowsky,M.W. (1994). Type II collagen distribution during cranial development in Xenopus laevis. Anat.Embryol.(Berl) 189:81-89. Shaw,L.M. and Olsen,B.R. (1991). FACIT collagens: diverse molecular bridges in extracellular matrices. Trends Biochem.Sci. 16:191-194. Shih,J. and Fraser,S.E. (1995). Distribution of tissue progenitors within the shield region of the zebrafish gastrula. Development 121:2755-2765. Shih,J. and Fraser,S.E. (1996). Characterizing the zebrafish organizer: microsurgical analysis at the early-shield stage. Development 122:1313-1322. Sirotkin,H.I., Dougan,S.T., Schier,A.F., and Talbot,W.S. (2000). bozozok and squint act in parallel to specify dorsal mesoderm and anterior neuroectoderm in zebrafish. Development 127:2583-2592. 208 References Slack,J.M., Isaacs,H.V., and Darlington,B.G. (1988). Inductive effects of fibroblast growth factor and lithium ion on Xenopus blastula ectoderm. Development 103:581-590. Smith,R. (1986). The molecular genetics of collagen disorders. Clin.Sci.(Lond) 71:129-135. Smith,J. (1997). Brachyury and the T-box genes. Curr.Opin.Genet.Dev. 7:474-480. Smith,J.C. and Slack,J.M. (1983). Dorsalization and neural induction: properties of the organizer in Xenopus laevis. J.Embryol.Exp.Morphol. 78:299-317. Smyth,N., Vatansever,H.S., Murray,P., Meyer,M., Frie,C., Paulsson,M., and Edgar,D. (1999). Absence of basement membranes after targeting the LAMC1 gene results in embryonic lethality due to failure of endoderm differentiation. J.Cell Biol. 144:151-160. Solursh,M., Jensen,K.L., Zanetti,N.C., Linsenmayer,T.F., and Reiter,R.S. (1984). Extracellular matrix mediates epithelial effects on chondrogenesis in vitro. Dev.Biol. 105:451-457. Spemann, H. (1938). Experimentelle Beiträge zu einer Theorie der Entwicklung (Embryonic Development and Induction). Freiburg, Germany. Spemann, H., and Mangold, H. (1924). Uber die Induktion von Embryoanlagen durch Implantation artfremder Organisatoren. Roux’ Arch. Mikrosk. Anat. Enwicklungsmech. 100:599-638. Stachel,S.E., Grunwald,D.J., and Myers,P.Z. (1993). Lithium perturbation and goosecoid expression identify a dorsal specification pathway in the pregastrula zebrafish. Development 117:1261-1274. Steindler,D.A., Settles,D., Erickson,H.P., Laywell,E.D., Yoshiki,A., Faissner,A., and Kusakabe,M. (1995). Tenascin knockout mice: barrels, boundary molecules, and glial scars. J.Neurosci. 15:1971-1983. Stemple,D.L., Solnica-Krezel,L., Zwartkruis,F., Neuhauss,S.C., Schier,A.F., Malicki,J., Stainier,D.Y., Abdelilah,S., Rangini,Z., Mountcastle-Shah,E., and Driever,W. (1996). Mutations affecting development of the notochord in zebrafish. Development 123:117-128. Stern,C.D. and Keynes,R.J. (1987). Interactions between somite cells: the formation and maintenance of segment boundaries in the chick embryo. Development 99:261-272. Stickney,H.L., Barresi,M.J., and Devoto,S.H. (2000). Somite development in zebrafish. Dev.Dyn. 219:287-303. 209 References Strähle,U., Blader,P., Henrique,D., and Ingham,P.W. (1993). Axial, a zebrafish gene expressed along the developing body axis, shows altered expression in cyclops mutant embryos. Genes Dev. 7:1436-1446. Strähle,U., Blader,P., and Ingham,P.W. (1996). Expression of axial and sonic hedgehog in wildtype and midline defective zebrafish embryos. Int.J.Dev.Biol. 40:929-940. Strähle,U., Fischer,N., and Blader,P. (1997a). Expression and regulation of a netrin homologue in the zebrafish embryo. Mech.Dev. 62:147-160. Strähle,U., Jesuthasan,S., Blader,P., Garcia-Villalba,P., Hatta,K., and Ingham,P.W. (1997b). one-eyed pinhead is required for development of the ventral midline of the zebrafish (Danio rerio) neural tube. Genes Funct. 1:131-148. Streuli,C. (1999). Extracellular matrix remodelling and cellular differentiation. Curr.Opin.Cell Biol. 11:634-640. Summerton,J. and Weller,D. (1997). Morpholino antisense oligomers: design, preparation, and properties. Antisense Nucleic Acid Drug Dev. 7:187-195. Svoboda,K.K., Nishimura,I., Sugrue,S.P., Ninomiya,Y., and Olsen,B.R. (1988). Embryonic chicken cornea and cartilage synthesize type IX collagen molecules with different amino-terminal domains. Proc.Natl.Acad.Sci.U.S.A 85:7496-7500. Swiderski,R.E. and Solursh,M. (1992a). Differential co-expression of long and short form type IX collagen transcripts during avian limb chondrogenesis in ovo. Development 115:169-179. Swiderski,R.E. and Solursh,M. (1992b). Localization of type II collagen, long form alpha 1(IX) collagen, and short form alpha 1(IX) collagen transcripts in the developing chick notochord and axial skeleton. Dev.Dyn. 194:118-127. Talbot,W.S. and Hopkins,N. (2000). Zebrafish mutations and functional analysis of the vertebrate genome. Genes Dev. 14:755-762. Talbot,W.S., Trevarrow,B., Halpern,M.E., Melby,A.E., Farr,G., Postlethwait,J.H., Jowett,T., Kimmel,C.B., and Kimelman,D. (1995). A homeobox gene essential for zebrafish notochord development. Nature 378:150-157. Tan,J.T., Korzh,V., and Gong,Z. (1999). Expression of a zebrafish iroquois homeobox gene, Ziro3, in the midline axial structures and central nervous system. Mech.Dev. 87:165-168. Tanabe,Y. and Jessell,T.M. (1996). Diversity and pattern in the developing spinal cord. Science 274:1115-1123. Taub,M., Wang,Y., Szczesny,T.M., and Kleinman,H.K. (1990). Epidermal growth factor or transforming growth factor alpha is required for kidney tubulogenesis 210 References in matrigel cultures in serum-free medium. Proc.Natl.Acad.Sci.U.S.A 87:40024006. Taylor,J., Pesheva,P., and Schachner,M. (1993). Influence of janusin and tenascin on growth cone behavior in vitro. J.Neurosci.Res. 35:347-362. Te,K.G. and Reggiani,C. (2002). Skeletal muscle fibre type specification during embryonic development. J.Muscle Res.Cell Motil. 23:65-69. Teillet,M.A., Lapointe,F., and Le Douarin,N.M. (1998). The relationships between notochord and floor plate in vertebrate development revisited. Proc.Natl.Acad.Sci.U.S.A 95:11733-11738. Thisse,C., Thisse,B., Schilling,T.F., and Postlethwait,J.H. (1993). Structure of the zebrafish snail1 gene and its expression in wild-type, spadetail and no tail mutant embryos. Development 119:1203-1215. Thorogood,P. (1988). The developmental specification of the vertebrate skull. Development 103 Suppl:141-153. Thorogood,P., Bee,J., and von der,M.K. (1986). Transient expression of collagen type II at epitheliomesenchymal interfaces during morphogenesis of the cartilaginous neurocranium. Dev.Biol. 116:497-509. Tian,J., Yam,C., Balasundaram,G., Wang,H., Gore,A., and Sampath,K. (2003). A temperature-sensitive mutation in the nodal-related gene cyclops reveals that the floor plate is induced during gastrulation in zebrafish. Development 130:3331-3342. Tongiorgi,E. (1999). Tenascin-C expression in the trunk of wild-type, cyclops and floating head zebrafish embryos. Brain Res.Bull. 48:79-88. Topczewski,J., Sepich,D.S., Myers,D.C., Walker,C., Amores,A., Lele,Z., Hammerschmidt,M., Postlethwait,J., and Solnica-Krezel,L. (2001). The zebrafish glypican knypek controls cell polarity during gastrulation movements of convergent extension. Dev.Cell 1:251-264. Townes, P.L., and Holtfreter, J. (1955). Directed movements and selective adhesion of embryonic amphibian cells. J. Exp. Zool. 128:53-120. Tucker,J.E., Lemon,R., Mackie,E.J., and Tucker,R.P. (1991). Immunohistochemical localization of tenascin and fibronectin in the dentine and gingiva of Canis familiaris. Arch.Oral Biol. 36:165-170. Tucker,R.P., Brunso-Bechtold,J.K., Jenrath,D.A., Khan,N.A., Poss,P.M., Sweatt,A.J., and Xu,Y. (1994). Cellular origins of tenascin in the developing nervous system. Perspect.Dev.Neurobiol. 2:89-99. Uchida, N., Shimamura, K., Miyatani, S., Copeland, N., Gilbert, D., Jenkins, N., and Takeichi, M. (1994). Mouse alpha N-catenin, two isoforms, specific 211 References expression in the nervous system, and chromosomal localization of the gene. Dev. Biol. 163, 75-85. van der Rest, M. and Mayne,R. (1988). Type IX collagen proteoglycan from cartilage is covalently cross-linked to type II collagen. J.Biol.Chem. 263:1615-1618. van der Rest, M., Mayne,R., Ninomiya,Y., Seidah,N.G., Chretien,M., and Olsen,B.R. (1985). The structure of type IX collagen. J.Biol.Chem. 260:220-225. van Straaten,H.W. and Hekking,J.W. (1991). Development of floor plate, neurons and axonal outgrowth pattern in the early spinal cord of the notochord-deficient chick embryo. Anat.Embryol.(Berl) 184:55-63. van Straaten,H.W., Hekking,J.W., Wiertz-Hoessels,E.J., Thors,F., and Drukker,J. (1988). Effect of the notochord on the differentiation of a floor plate area in the neural tube of the chick embryo. Anat.Embryol.(Berl) 177:317-324. Vaughan, L., Weber, P., D'Alessandri, L., Zisch, A.H., and Winterhalter, K.H. (1994) Tenascin-contactin/F11 interactions: a clue for a developmental role? Perspect Dev Neurobiol. 2:43-52. Vogel,W. (1999). Discoidin domain receptors: structural relations and functional implications. FASEB J. 13 Suppl:S77-S82. Vogel, W.F. (2001). Collagen-receptor Eur.J.Dermatol. 11:506-514. signaling in health and disease. Vukicevic, S., Kleinman,H.K., Luyten,F.P., Roberts,A.B., Roche,N.S., and Reddi,A.H. (1992). Identification of multiple active growth factors in basement membrane Matrigel suggests caution in interpretation of cellular activity related to extracellular matrix components. Exp.Cell Res. 202:1-8. Wang, H. and Gong,Z. (1999). Characterization of two zebrafish cDNA clones encoding egg envelope proteins ZP2 and ZP3. Biochim.Biophys.Acta 1446:156-160. Wang, H., Yan,T., Tan,J.T., and Gong,Z. (2000). A zebrafish vitellogenin gene (vg3) encodes a novel vitellogenin without a phosvitin domain and may represent a primitive vertebrate vitellogenin gene. Gene 256:303-310. Wang,X., Chu,L.T., He,J., Emelyanov,A., Korzh,V., and Gong,Z. (2001). A novel zebrafish bHLH gene, neurogenin3, is expressed in the hypothalamus. Gene 275:47-55. Wang,X., Emelyanov,A., Sleptsova-Friedrich,I., Korzh,V., and Gong,Z. (2001). Expression of two novel zebrafish iroquois homologues (ziro1 and ziro5) during early development of axial structures and central nervous system. Mech.Dev. 105:191-195. 212 References Wang,X., Emelyanov,A., Korzh,V., and Gong,Z. (2003). Zebrafish atonal homologue zath3 is expressed during neurogenesis in embryonic development. Dev.Dyn. 227:587-592. Ward,A.C. and Lieschke,G.J. (2002). The zebrafish as a model system for human disease. Front Biosci. 7:d827-d833. Warga,R.M. and Kimmel,C.B. (1990). Cell movements during epiboly and gastrulation in zebrafish. Development 108:569-580. Warman,M.L., McCarthy,M.T., Perala,M., Vuorio,E., Knoll,J.H., McDaniels,C.N., Mayne,R., Beier,D.R., and Olsen,B.R. (1994). The genes encoding alpha 2(IX) collagen (COL9A2) map to human chromosome 1p32.3-p33 and mouse chromosome 4. Genomics 23:158-162. Wehrle,B. and Chiquet,M. (1990). Tenascin is accumulated along developing peripheral nerves and allows neurite outgrowth in vitro. Development 110:401-415. Wehrle-Haller,B. and Chiquet,M. (1993). Dual function of tenascin: simultaneous promotion of neurite growth and inhibition of glial migration. J.Cell Sci. 106 ( Pt 2):597-610. Wehrle-Haller,B., Koch,M., Baumgartner,S., Spring,J., and Chiquet,M. (1991). Nerve-dependent and -independent tenascin expression in the developing chick limb bud. Development 112:627-637. Weinberg,E.S., Allende,M.L., Kelly,C.S., Abdelhamid,A., Murakami,T., Andermann,P., Doerre,O.G., Grunwald,D.J., and Riggleman,B. (1996). Developmental regulation of zebrafish MyoD in wild-type, no tail and spadetail embryos. Development 122:271-280. Weinstein,D.C., Altaba,A., Chen,W.S., Hoodless,P., Prezioso,V.R., Jessell,T.M., and Darnell,J.E., Jr. (1994). The winged-helix transcription factor HNF-3 beta is required for notochord development in the mouse embryo. Cell 78:575-588. Westerfield, M. (1989). The Zebrafish Book: A guide for the laboratory use of zebrafish (Brachydanio rerio). University of oregon press, Eugene. Westerfield, M., Doerry, E., and Douglas, S. Zebrafish in the Net.(1999a). Trends Genet. 15:248-249. Westerfield, M., Doerry, E., Kirkpatrick, A.E., and Douglas, S.A. (1999b). Zebrafish informatics and the ZFIN database In: The Zebrafish: Genetics and Genomics, eds. H.W. Detrich, III, M. Westerfield, and L.I. Zon, San Diego, CA: Academic Press. Whitman,M. (2001). Nodal signaling in early vertebrate embryos: themes and variations. Dev.Cell 1:605-617. 213 References Wilson, H.V. (1907). On some phenomena of coalescence and regeneration in sponges. J. Exp. Zool. 5: 245-258. Wood,A., Ashhurst,D.E., Corbett,A., and Thorogood,P. (1991). The transient expression of type II collagen at tissue interfaces during mammalian craniofacial development. Development 111:955-968. Woods,I.G., Kelly,P.D., Chu,F., Ngo-Hazelett,P., Yan,Y.L., Huang,H., Postlethwait,J.H., and Talbot,W.S. (2000). A comparative map of the zebrafish genome. Genome Res. 10:1903-1914. Wu,J.J., Woods,P.E., and Eyre,D.R. (1992). Identification of cross-linking sites in bovine cartilage type IX collagen reveals an antiparallel type II-type IX molecular relationship and type IX to type IX bonding. J.Biol.Chem. 267:23007-23014. Xu,H., Wu,X.R., Wewer,U.M., and Engvall,E. (1994). Murine muscular dystrophy caused by a mutation in the laminin alpha (Lama2) gene. Nat.Genet. 8:297302. Xu,Y., He,J., Tian,H.L., Chan,C.H., Liao,J., Yan,T., Lam,T.J., and Gong,Z. (1999). Fast skeletal muscle-specific expression of a zebrafish myosin light chain gene and characterization of its promoter by direct injection into skeletal muscle. DNA Cell Biol. 18:85-95. Xu,Y., He,J., Wang,X., Lim,T.M., and Gong,Z. (2000). Asynchronous activation of 10 muscle-specific protein (MSP) genes during zebrafish somitogenesis. Dev.Dyn. 219:201-215. Yamada,T., Placzek,M., Tanaka,H., Dodd,J., and Jessell,T.M. (1991). Control of cell pattern in the developing nervous system: polarizing activity of the floor plate and notochord. Cell 64:635-647. Yamada,T., Pfaff,S.L., Edlund,T., and Jessell,T.M. (1993). Control of cell pattern in the neural tube: motor neuron induction by diffusible factors from notochord and floor plate. Cell 73:673-686. Yan,Y.L., Hatta,K., Riggleman,B., and Postlethwait,J.H. (1995). Expression of a type II collagen gene in the zebrafish embryonic axis. Dev.Dyn. 203:363-376. Yan,Y.T., Gritsman,K., Ding,J., Burdine,R.D., Corrales,J.D., Price,S.M., Talbot,W.S., Schier,A.F., and Shen,M.M. (1999). Conserved requirement for EGF-CFC genes in vertebrate left-right axis formation. Genes Dev. 13:2527-2537. Young,D.L., Schneider,R.A., Hu,D., and Helms,J.A. (2000). Genetic and teratogenic approaches to craniofacial development. Crit Rev.Oral Biol.Med. 11:304-317. Zatterstrom, U.K., Felbor, U., Fukai, N., and Olsen, B.R. (2000). Collagen XVIII/endostatin structure and functional role in angiogenesis. Cell Struct Funct.25:97-101. 214 References Zhang,J., Talbot,W.S., and Schier,A.F. (1998). Positional cloning identifies zebrafish one-eyed pinhead as a permissive EGF-related ligand required during gastrulation. Cell 92:241-251. Zheng,X., Saunders,T.L., Camper,S.A., Samuelson,L.C., and Ginsburg,D. (1995). Vitronectin is not essential for normal mammalian development and fertility. Proc.Natl.Acad.Sci.U.S.A 92:12426-12430. Zhong,T.P., Kaphingst,K., Akella,U., Haldi,M., Lander,E.S., and Fishman,M.C. (1998). Zebrafish Genomic Library in Yeast Artificial Chromosomes. Genomics 48:136-138. Zhou,X., Sasaki,H., Lowe,L., Hogan,B.L., and Kuehn,M.R. (1993). Nodal is a novel TGF-beta-like gene expressed in the mouse node during gastrulation. Nature 361:543-547. Zhu,Y., McAlinden,A., and Sandell,L.J. (2001). Type IIA procollagen in development of the human intervertebral disc: regulated expression of the NH(2)-propeptide by enzymic processing reveals a unique developmental pathway. Dev.Dyn. 220:350-362. Zhurinsky,J., Shtutman,M., and Ben Ze'ev,A. (2000). Plakoglobin and beta-catenin: protein interactions, regulation and biological roles. J.Cell Sci. 113 ( Pt 18):3127-3139. 215 [...]... colIXa2 expression in later development of zebrafish 99 Fig 3.9 colIXa2 expresses strongly in the anterior regions of late stage zebrafish 100 Fig 3.10 colIXa1 expression during early development of zebrafish 104 Fig 3.11 colIXa3 expression during early development of zebrafish 105 Fig 3.12 Schematic representation of expression profile exhibited by three chains of zebrafish type IX collagen and type. .. and cloning of full length zebrafish colIXα2 cDNA clone by 5’-RACE-PCR 85 The complete nucleotide sequence of the zebrafish colIXα2 cDNA and deduced amino acid sequence 86-87 Amino acid sequence alignment of Zebrafish, Human, Mouse and Chick ColIXα2 88 Phylogenetic tree of FACIT family comprising of chains of collagen IX, collagen XII, collagen XIV and collagen XIX 89 Mapping of colIXα2 colIXα2 was... collagen and type II collagen alpha 1 in the tail bud during segmentation and post-segmentation period 106 Translation inhibition of colIXa2 affects early development of zebrafish 111 Fig 3.14 colIXα2 plays a role in establishing integrity of axial mesoderm 115 Fig 3.15 Inhibition of ColIXa2 resulted in loss of reintegration of cells in vitro 118 Fig 3.16 ColIXa2 is required for maintenance of the floor plate... role of colIXα2 in precursors of axial structures, translation of colIXα2 was inhibited by morpholino oligonucleotides This resulted in loss of identity of the floor plate Thus, ColIXα2 plays a role in early events of specification of the floor plate Further, in absence of ColIXα2 the ability of cells to reassemble has been compromised Additionally, inhibition of ColIXα2 also caused defects in the integrity... Inhibition of colIXa2 translation causes somitic defects in the zebrafish 124 Inhibition of colIXa2 translation affects sclerotome, neural crest and pharyngeal arches in zebrafish 127 Cadherins and β-Catenin are affected by inhibition of colIXa2 translation 133 n-cadherin and integrin-a6 are severely reduced in midbrain of colIXa2MO injected embryos 134 Fig 3-6 Fig 3.13 Fig 3.18 Fig 3.19 Fig 3.20 ix. .. than other axial structures The lineages of axial structures are initially established during late gastrula and this process is maintained in the organizer of teleosts, the embryonic shield and later on in chordo-neural hinge of the tail bud The extracellular matrix (ECM) plays an important role in providing integrity of emerging organs, but the role of individual components of the ECM in these events... six categories of collagen genes 28 Table 1.2 Collagen types and their tissue distribution 31 Table 1.3 Mutations in Collagen genes and resulting disorders 38 Table 3.1 Phenotypes obtained after injection of antisense morpholino oligonucleotides against colIXα2 in embryonic zebrafish 110 Table showing the mean number of cell clusters obtained after reintegration 117 Table 3-2 Table 3-3 Table showing... (44.1-50.0 cM) using T51 radiation hybrid panel 92 Fig 1.2 Fig 1.5 Fig 3.2 Fig 3.3 Fig 3-4 Fig.3-5 (A) viii List of Figures Fig.3-5 (B, C) Mapping of colIXα2 Conserved synteny of zebrafish, mouse and human chromosomes containing colIXα2genes and syntenic relationshop 93 RT-PCR analysis of colIXa2 mRNAs in different stages of zebrafish development 94 Fig 3.7 colIXa2 expression in early development of zebrafish. .. of Figures Fig 3.21 Fig 3.22 Fig 3.23 Fig 3.24 The expression of colIXa2 in axial structures is independent of notochord 138 colIXa2 expression was induced by mesodermal inducers like activin 140 Expression of colIXa2 is dependent on nodal signaling in the floor plate 145 Differential requirement of components of Nodal signaling in floor plate 146 x List of Tables LIST OF TABLES Table 1.1 Summary of. .. and Gong Zhiyuan 2000 Expression analysis of type IX collagen in embryonic zebrafish Poster presented at Zebrafish development and Genetics Meeting at Cold Spring Harbor Laboratory, Cold Spring Harbor, New York USA April 26-30, 2000 5 Sudha Puttur Mudumana, Inna Sleptsova Friedrich, Vladimir Korzh and Gong Zhiyuan 2000 Expression analysis of type IX collagen in embryonic zebrafish Poster presented at . ANALYSIS OF TYPE IX COLLAGEN IN ZEBRAFISH AXIAL DEVELOPMENT SUDHA PUTTUR MUDUMANA NATIONAL UNIVERSITY OF SINGAPORE 2003 ANALYSIS OF TYPE IX COLLAGEN IN. analysis of colIXa2 mRNAs in different stages of zebrafish development 94 Fig. 3.7 colIXa2 expression in early development of zebrafish 97 Fig. 3.8 colIXa2 expression in later development. colIXa3 expression during early development of zebrafish 105 Fig. 3.12 Schematic representation of expression profile exhibited by three chains of zebrafish type IX collagen and type II collagen