Development and evolution of chordate cartilage

Journal of Experimental Zoology Part B: Molecular and Developmental Evolution

Volumn 308, Issue 3, 2007, Pages 325-335

  Rychel, Amanda L ^a,b   Swalla, Billie J ^a,b  

^a UNIVERSITY OF WASHINGTON   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FIBRILLAR COLLAGEN; PAIRED BOX TRANSCRIPTION FACTOR; PAX1 TRANSCRIPTION FACTOR; PRIMER DNA; UNCLASSIFIED DRUG;

ANIMAL; ARTICLE; BRANCHIAL ARCH; CARTILAGE; CHORDATA; COMPARATIVE STUDY; DNA SEQUENCE; ENDODERM; EVOLUTION; GENETICS; HISTOLOGY; IN SITU HYBRIDIZATION; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYLOGENY; PRENATAL DEVELOPMENT; SPECIES DIFFERENCE;

ANIMALS; BASE SEQUENCE; BRANCHIAL REGION; CARTILAGE; CHORDATA; DNA PRIMERS; ENDODERM; EVOLUTION; FIBRILLAR COLLAGENS; IN SITU HYBRIDIZATION; MOLECULAR SEQUENCE DATA; PAIRED BOX TRANSCRIPTION FACTORS; PHYLOGENY; SEQUENCE ANALYSIS, DNA; SPECIES SPECIFICITY;

ANIMALIA; BRANCHIOSTOMIDAE; DEUTEROSTOMIA; ECHINODERMATA; HEMICHORDATA; INVERTEBRATA; UROCHORDATA; VERTEBRATA; XENOTURBELLIDA;

EID: 34249782269     PISSN: 15525007     EISSN: 15525015     Source Type: Journal    
DOI: 10.1002/jez.b.21157     Document Type: Article

References (68)

1. Aouacheria A, Cluzel C, Lethias C, Gouy M, Garrone R, Exposito JY. 2004. Invertebrate data predict an early emergence of vertebrate fibrillar collagen clades and an anti-incest model. J Biol Chem 279:47711-47719.
2. Bell DM, Leung KK, Wheatley SC, Ng LJ, Zhou S, Ling KW, Sham MH, Koopman P, Tam PP, Cheah KS. 1997. SOX9 directly regulates the type-II collagen gene. Nat Genet 16:174-178.
3. Benson S, Sucov H, Stephens L, Davidson E, Wilt F. 1987. A lineage-specific gene encoding a major matrix protein of the sea urchin embryo spicule. I. Authentication of the cloned gene and its developmental expression. Dev Biol 120:499-506.
4. Bi W, Deng JM, Zhang Z, Behringer RR, de Crombrugghe B. 1999. Sox9 is required for cartilage formation. Nat Genet 22:85-89.
5. Blair JE, Hedges SB. 2005. Molecular phylogeny and divergence times of deuterostome animals. Mol Biol Evol 22:2275-2284.
6. Bourlat SJ, Juliusdottir T, Lowe CJ, Freeman R, Aronowicz J, Kirschner M, Lander ES, Thorndyke M, Nakano H, Kohn AB, Heyland A, Moroz LL, Copley RR, Telford MJ. 2006. Deuterostome phylogeny reveals monophyletic chordates and the new phylum Xenoturbellida. Nature 444:85-88.
7. Bowles J, Schepers G, Koopman P. 2000. Phylogeny of the SOX family of developmental transcription factors based on sequence and structural Indicators. Dev Biol 227:239-255.
8. Cameron CB. 2002. Particle retention and flow in the pharynx of the enteropneust worm Harrimania planktophilus: The filter-feeding pharynx may have evolved before the chordates. Biol Bull 202:192-200.
9. Cameron CB, Garey JR, Swalla BJ. 2000. Evolution of the chordate body plan: new insights from phylogenetic analyses of deuterostome phyla. Proc Natl Acad Sci USA 97:4469-4474.
10. Cheah KS, Lau ET, Au PK, Tam PP. 1991. Expression of the mouse alpha 1(II) collagen gene is not restricted to cartilage during development. Development 111:945-953.
11. Chen JY, Dzik J, Edgecombe GD, Ramskold L, Zhou GQ. 1995. A possible Early Cambrian chordate. Nature 377:720-722.
12. Cole AG, Hall BK. 2004a. Cartilage is a metazoan tissue; integrating data from nonvertebrate sources. Acta Zoologica 85:69-80.
13. Cole AG, Hall BK. 2004b. The nature and significance of invertebrate cartilages revisited: distribution and histology of cartilage and cartilage-like tissues within the Metazoa. Zoology 107:261-273.
14. David NB, Saint-Etienne L, Tsang M, Schilling TF, Rosa FM. 2002. Requirement for endoderm and FGF3 in ventral head skeleton formation. Development 129:4457-4468.
15. De Beer GR. 1937. The development of the vertebrate skull. Oxford: Oxford University Press. 408p.
16. de Crombrugghe B, Lefebvre V, Behringer RR, Bi W, Murakami S, Huang W. 2000. Transcriptional mechanisms of chondrocyte differentiation. Matrix Biol 19:389-394.
17. Delsuc F, Brinkmann H, Chourrout D, Philippe H. 2006. Tunicates and not cephalochordates are the closest living relatives of vertebrates. Nature 439:965-968.
18. Donoghue PCJ, Sansom IJ, Downs JP. 2006. Early evolution of vertebrate skeletal tissues and cellular interactions, and the canalization of skeletal development. J Exp Zool B: Mol Dev Evol 306B:278-294.
19. Dziadek M. 1995. Role of laminin-nidogen complexes in basement membrane formation during embryonic development. Experientia 51:901-913.
20. Ekanayake S, Hall BK. 1987. The development of acellularity of the vertebral bone of the Japanese medaka, Oryzias latipes (Teleostei; Cyprinidontidae). J Morphol 193:253-261.
21. Ekanayake S, Hall BK. 1988. Ultrastructure of the osteogenesis of acellular vertebral bone in the Japanese medaka, Oryzias latipes (teleostei, cyprinidontidae). Am J Anatomy 182:241-249.
22. Fleming A, Keynes R, Tannahill D. 2004. A central role for the notochord in vertebral patterning. Development 131:873-880.
23. Garcia-Fernandez J, Holland PWH. 1994. Archetypal organization of the amphioxus Hox gene cluster. Nature 370:563-566.
24. George NC, Killian CE, Wilt FH. 1991. Characterization and expression of a gene encoding a 30.6-kDa Strongylocentrotus purpuratus spicule matrix protein. Dev Biol 147:334-342.
25. Goldring MB, Tsuchimochi K, Ijiri K. 2006. The control of chondrogenesis. J Cellular Biochem 97:33-44.
26. Graham A, Okabe M, Quinlan R. 2005. The role of the endoderm in the development and evolution of the pharyngeal arches. J Anatomy 207:479-487.
27. Hall BK. 2005. Cartilage. Bones and cartilage: developmental and evolutionary skeletal biology. San Diego: Elsevier Academic Press. p 33-47.
28. Harkey MA, Klueg K, Sheppard P, Raff RA. 1995. Structure, expression, and extracellular targeting of PM27, a skeletal protein associated specifically with growth of the sea urchin larval spicule. Dev Biol 168:549-566.
29. Hyman LH. 1959. The enterocoelous coelomates - phylum Hemichordata. The invertebrates: smaller coelomate groups. New York: McGraw-Hill. p 72-207.
30. Ikuta T, Yoshida N, Satoh N, Saiga H. 2004. Ciona intestinalis Hox gene cluster: its dispersed structure and residual colinear expression in development. Proc Natl Acad Sci 101:15118-15123.
31. Illies MR, Peeler MT, Dechtiaruk AM, Ettensohn CA. 2002. Identification and developmental expression of new biomineralization proteins in the sea urchin Strongylocentrotus purpuratus. Dev Genes Evol 212:419-431.
32. Jeanmougin F, Thompson JD, Gouy M, Higgins DG, Gibson TJ. 1998. Multiple sequence alignment with Clustal X. Trends in Biochem Sci 23:403-405.
33. Kardong KV. 2006. Vertebrates: comparative anatomy, function, evolution. New York: McGraw-Hill. p 47-83.
34. Katoh-Fukui Y, Noce T, Ueda T, Fujiwara Y, Hashimoto N, Higashinakagawa T, Killian CE, Livingston BT, Wilt FH, Benson SC, Sucor HM, Davidson EH. 1991. The corrected structure of the SM50 spicule matrix protein of Strongylocentrotus purpuratus. Dev Biol 145:201-202.
35. Kellerer S, Schreiner S, Stolt CC, Scholz S, Bosl MR, Wegner M. 2006. Replacement of the Sox10 transcription factor by Sox8 reveals incomplete functional equivalence. Development 133:2875-2886.
36. Killian CE, Wilt FH. 1996. Characterization of the proteins comprising the integral matrix of Strongylocentrotus purpuratus embryonic spicules. J Biol Chem 271:9150-9159.
37. Kimmel CB, Miller CT, Moens CB. 2001. Specification and morphogenesis of the zebrafish larval head skeleton. Dev Biol 233:239-257.
38. Kosher RA, Solursh M. 1989. Widespread distribution of type II collagen during embryonic chick development. Dev Biol 131:558-566.
39. Lee YH, Britten RJ, Davidson EH. 1999. SM37, a skeletogenic gene of the sea urchin embryo linked to the SM50 gene. Dev, Growth Differ 41:303-312.
40. Livingston BT, Killian CE, Wilt F, Cameron A, Landrum MJ, Ermolaeva O, Sapojnikov V, Maglott DR, Buchanan AM, Ettensohn CA. 2006. A genome-wide analysis of biomineralization-related proteins in the sea urchin Strongylocentrotus purpuratus. Dev Biol 300:335-348.
41. Mayor R, Young R, Vargas A. 1999. Development of neural crest in Xenopus. Curr Top Dev Biol 43:85-113.
42. McCauley DW, Bronner-Fraser M. 2006. Importance of SoxE in neural crest development and the evolution of the pharynx. Nature 441:750-752.
43. Ng LJ, Wheatley S, Muscat GE, Conway-Campbell J, Bowles J, Wright E, Bell DM, Tam PP, Cheah KS, Koopman P. 1997. SOX9 binds DNA, activates transcription, and coexpresses with type II collagen during chondrogenesis in the mouse. Dev Biol 183:108-121.
44. Noden DM. 1978. The control of avian cephalic neural crest cytodifferentiation: I. Skeletal and connective tissues. Dev Biol 67:296-312.
45. O'Donnell M, Hong C-S, Huang X, Delnicki RJ, Saint-Jeannet J-P. 2006. Functional analysis of Sox8 during neural crest development in Xenopus. Development 133:3817-3826.
46. Ogasawara M, Wada H, Peters H, Satoh N. 1999. Developmental expression of Pax1/9 genes in urochordate and hemichordate gills: insight into function and evolution of the pharyngeal epithelium. Development 126:2539-2550.
47. Panopoulou G, Hennig S, Groth D, Krause A, Poustka AJ, Herwig R, Vingron M, Lehrach H. 2003. New evidence for genome-wide duplications at the origin of vertebrates using an amphioxus gene set and completed animal genomes. Genome Res 13:1056-1066.
48. Pardos F, Benito J. 1988. Blood vessels and related structures in the gill bars of Glossobalanus minutus (Enteropneusta). Acta Zoologica 69:87-94.
49. Passamaneck YJ, Di Gregorio A. 2005. Ciona intestinalis: Chordate development made simple. Dev Dyn 233:1-19.
50. Pennachetti CA. 1984. Functional morphology of the branchial basket of Ascidia paratropa (Tunicata, Ascidiacea). Zoomorphology 104:216-222.
51. Rahr H. 1982. Ultrastructure of gill bars of Branchiostoma lanceolatum with special reference to gill skeleton and blood vessels (Cephalochordata). Zoomorphology 99:167-180.
52. Robson P, Wright GM, Sitarz E, Maiti A, Rawat M, Youson JH, Keeley FW. 1993. Characterization of lamprin, an unusual matrix protein from lamprey cartilage. Implications for evolution, structure, and assembly of elastin and other fibrillar proteins. J Biol Chem 268:1440-1447.
53. Rychel AL, Smith SE, Shimamoto HT, Swalla BJ. 2006. Evolution and development of the chordates: collagen and pharyngeal cartilage. Mol Biol Evol 23:541-549.
54. Schaeffer B. 1987. Deuterostome monophyly and phylogeny. Evol Biol 21:179-235.
55. Sea Urchin Genome Sequencing Consortium: Sodergren E, Weinstock GM, Davidson EH, Cameron RA, Gibbs RA, Angerer RC, Angerer LM, Arnone MI, Burgess DR, Burke RD, Coffman JA, Dean M, Elphick MR, Ettensohn CA, Foltz KR, Hamdoun A, Hynes RO, Klein WH, Marzluff W, McClay DR, Morris RL, Mushegian A, Rast JP, Smith LC, Thorndyke MC, Vacquier VD, Wessel GM, Wray G, Zhang L, Elsik CG, Ermolaeva O, Hlavina W, Hofmann G, Kitts P, Landram MJ, Mackey AJ, Maglott D, Panopoulou G, Poustka AJ, Praitt K, Sapojnikov V, Song X, Souvorov A, Solovyev V, Wei Z, Whittaker CA, Worley K, Durbin KJ, Shen Y, Fedrigo O, Garfield D, Haygood R, Primus A, Satija R, Severson T, Gonzalez-Garay ML, Jackson AR, Milosavljevic A, Tong M, Killian CE, Livingston BT, Wilt FH, Adams N, Belle R, Carbonneau S, Cheung R, Cormier P, Cosson B, Croce J, Fernandez-Guerra A, Geneviere A-M, Goel M, Kelkar H, Morales J, Mulner-Lorillon O, Robertson AJ, Goldstone JV, Cole B, Epel D, Gold B, Hahn ME, Howard-Ashby M, Scally M, Stegeman JJ, Allgood EL, Cool J, Judkins KM, McCafferty SS, Musante AM, Obar RA, Rawson AP, Rossetti BJ, Gibbons IR, Hoffman MP, Leone A, Istrail S, Materna SC, Samanta MP, Stolc V, Tongprasit W, Tu Q, Bergeron K-F, Brandhorst BP, Whittle J, Berney K, Bottjer DJ, Calestani C, Peterson K, Chow E, Yuan QA, Elhaik E, Graur D, Reese JT, Bosdet I, Heesun S, Marra MA, Schein J, Anderson MK, Brockton V, Buckley KM, Cohen AH, Fugmann SD, Hibino T, Loza-Coll M, Majeske AJ, Messier C, Nair SV, Pancer Z, Terwilliger DP, Agca C, Arboleda E, Chen N, Churcher AM, Hallbook F, Humphrey GW, Idris MM, Kiyama T, Liang S, Mellott D, Mu X, Murray G, Olinski RP, Raible F, Rowe M, Taylor JS, Tessmar-Raible K, Wang D, Wilson KH, Yaguchi S, Gaasterland T, Galindo BE, Gunaratne HJ, Juliano C, Kinukawa M, Moy GW, Neill AT, Nomura M, Raisch M, Reade A, Roux MM, Song JL, Su Y-H, Townley IK, Voronina E, Wong JL, Amore G, Branno M, Brown ER, Cavalieri V, Duboc V, Duloquin L, Flytzanis C, Gache C, Lapraz F, Lepage T, Locaselo A, Martinez P, Matassi G, Matranga V, Range R, Rizzo F, Rottinger E, Beane W, Bradham C, Byram C, Glenn T, Hussain S, Manning FG, Miranda E, Thomason R, Walton K, Wikramanayke A, Wu S-Y, Xu R, Brown CT, Chen L, Gray RF, Lee PY, Nam J, Oliveri P, Smith J, Muzny D, Bell S, Chacko J, Cree A, Curry S, Davis C, Dinh H, Dugan-Rocha S, Fowler J, Gill R, Hamilton C, Hernandez J, Hines S, Hume J, Jackson L, Jolivet A, Kovar C, Lee S, Lewis L, Miner G, Morgan M, Nazareth LV, Okwuonu G, Parker D, Pu L-L, Thorn R, Wright R. 2006. The genome of the sea urchin Strongylocentrotus purpuratus. Science 314:941-952.
56. Sekiya I, Tsuji K, Koopman P, Watanabe H, Yamada Y, Shinomiya K, Nifuji A, Noda M. 2000. SOX9 enhances aggrecan gene promoter/enhancer activity and is up-regulated by retinoic acid in a cartilage-derived cell line, TC6. J Biol Chem 275:10738-10744.
57. Smith SE, Douglas R, da Silva KB, Swalla BJ. 2003. Morphological and molecular identification of Saccoglossus species (Hemichordata: Harrimaniidae) in the Pacific Northwest. Can J Zool 81:133-141.
58. Suzuki T, Sakai D, Osumi N, Wada H, Wakamatsu Y. 2006. Sox genes regulate type 2 collagen expression in avian neural crest cells. Dev Growth Differ 48:477-486.
59. Swalla BJ. 2006. Building divergent body plans with similar genetic pathways. Heredity 97:235-243.
60. Swalla BJ. 2007. New insights into vertebrate origins. In: Moody S, editor. Principles of developmental genetics. San Diego: Elsevier Science/Academic Press.
61. Swofford DL. 1999. PAUP*: phylogenetic analysis using parsimony (*and other methods). Version 4. Sunderland, Mass: Sinaeur Associates.
62. Wada H, Okuyama M, Satoh N, Zhang S. 2006. Molecular evolution of fibrillar collagen in chordates, with implications for the evolution of vertebrate skeletons and chordate phylogeny. Evol Dev 8:370-377.
63. Wright GM, Keeley FW, Robson P. 2001. The unusual cartilaginous tissues of jawless craniates, cephalochordates and invertebrates. Cell Tissue Res 304:165-174.
64. Yan YL, Hatta K, Riggleman B, Postlethwait JH. 1995. Expression of a type II collagen gene in the zebrafish embryonic axis. Dev Dyn 203:363-376.
65. Yan YL, Miller CT, Nissen RM, Singer A, Liu D, Kirn A, Draper B, Willoughby J, Morcos PA, Amsterdam A, Chung BC, Westerfield M, Haffter P, Hopkins N, Kimmel C, Postlethwait JH. 2002. A zebrafish sox9 gene required for cartilage morphogenesis. Development 129:5065-5079.
66. Zeng LY, Swalla BJ. 2005. Molecular phylogeny of the protochordates: chordate evolution. Can J Zool - Revue Canadienne De Zoologie 83:24-33.
67. Zhang G, Miyamoto MM, Cohn MJ. 2006. Lamprey type II collagen and Sox9 reveal an ancient origin of the vertebrate collagenous skeleton. Proc Natl Acad Sci 103:3180-3185.
68. Zhao Q, Eberspaecher H, Lefebvre V, De Crombrugghe B. 1997. Parallel expression of Sox9 and Col2α1 in cells undergoing chondrogenesis. Dev Dyn 209:377-386.