Cellular morphology and markers of cartilage and bone in the marine teleost Sparus auratus

Cell and Tissue Research

Volumn 343, Issue 3, 2011, Pages 619-635

  Estêvão, M Dulce ^a   Silva, Nadia ^b   Redruello, Begona ^c   Costa, Rita ^a   Gregório, Silvia ^a   Canário, Adelino V M ^a   Power, Deborah M ^a  

^a UNIVERSITY OF ALGARVE   (Portugal)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c DEPARTMENT OF MICROBIOLOGY AND BIOCHEMISTRY OF DAIRY PRODUCTS   (Spain)

Author keywords

Extracellular matrix; Molecular markers; Ontogeny; Sea bream, Sparus auratus (Teleostei); Skeletogenesis

Indexed keywords

COLLAGEN TYPE 1; CYCLINE; OSTEOPONTIN;

ARTICLE; CARTILAGE CELL; CELL STRUCTURE; CONTROLLED STUDY; EXTRACELLULAR MATRIX; GENETIC TRANSCRIPTION; MESENCHYME CELL; MINERALIZATION; NONHUMAN; ONTOGENY; PERIOSTEUM; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN MODIFICATION; SPARUS AURATUS; TELEOST;

ANIMALS; BIOLOGICAL MARKERS; BONE AND BONES; CALCIFICATION, PHYSIOLOGIC; CARTILAGE; CELL SHAPE; EXTRACELLULAR MATRIX; HUMANS; IN SITU HYBRIDIZATION; LARVA; RNA, MESSENGER; SEA BREAM;

ARCHOSARGUS RHOMBOIDALIS; MAMMALIA; SPARUS AURATA; TELEOSTEI; VERTEBRATA;

EID: 79953832420     PISSN: 0302766X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00441-010-1109-y     Document Type: Article

References (76)

1. Adams JC, Watt FM (1993) Regulation of development and differentiation by the extracellular matrix. Development 117:1183-1198 (Pubitemid 23154486)
2. Avaron F, Hoffman L, Guay D, Akimenko MA (2006) Characterization of two new zebrafish members of the hedgehog family: atypical expression of a zebrafish Indian hedgehog gene in skeletal elements of both endochondral and dermal origins. Dev Dyn 235:478-489 (Pubitemid 43100953)
3. Bayliss PE, Bellavance KL, Whitehead GG, Abrams JM, Aegerter S, Robbins HS, Cowan DB, Keating MT, O'Reilly T, Wood JM, Roberts TM, Chan J (2006) Chemical modulation of receptor signaling inhibits regenerative angiogenesis in adult zebrafish. Nat Chem Biol 2:265-273
4. Behonick DJ, Werb Z (2003) A bit of give and take: the relationship between the extracellular matrix and the developing chondrocyte. Mech Dev 120:1327-1336 (Pubitemid 37421166)
5. Benjamin M, Ralphs JR, Eberewariye OS (1992) Cartilage and related tissues in the trunk and fins of teleosts. J Anat 181:113-118
6. Bird NC, Mabee PM (2003) Development morphology of the axial skeleton of the zebra fish, Danio rerio (Ostariophysi:Cyprinidae). Dev Dyn 228:337-357
7. Brittijn SA, Duivesteijn SJ, Belmamoune M, Bertens LFM, Bitter W, De Bruijn JD, Champagne DL, Cuppen E, Flik G, Vanderbroucke-Grauls CM, Janssen RAJ, De Jong IML, De Kloet ER, Kros A, Meijer AH, Metz JR, Van Der Sar AM, Schaaf JM, Schulte-Merker S, Spaink HP, Tak PP, Verbeek FJ, Vervoordeldonk MJ, Vomk FJ, Witte F, Yuan H, Richardson MK (2009) Zebrafish development and regeneration: new tools for biomedical research. Int J Dev Biol 53:835-850
8. Bruneau S, Mourrain P, Rosa FM (1997) Expression of contact, a new zebrafish DVR member, marks mesenchymal cell lineages in the developing pectoral fins and head and is regulated by retinoic acid. Mech Dev 65:163-173 (Pubitemid 27314598)
9. Campinho MA, Moutou KA, Power DM (2004) Temperature sensitivity of skeletal ontogeny in Oreochromis mossambicus. J Fish Biol 65:1003-1025 (Pubitemid 39342666)
10. Compston JE (2001) Sex steroids and bone. Physiol Rev 81:419-447
11. Downey PA, Siegel MI (2006) Bone biology and the clinical implications for osteoporosis. Phys Ther 86:177-191
12. Du SJ, Frenkel V, Kindschi G, Zohar Y (2001) Visualizing normal and defective bone development in zebrafish embryos using the fluorescent chromophore calcein. Dev Biol 238:239-246 (Pubitemid 32977293)
13. 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
14. Ekanayake S, Hall BK (1988) Ultrastructure of the osteogenesis of acellular vertebral bone in the Japanese medaka, Oryzias latipes (Teleostei, Cyprinidontidae). Am J Anat 182:241-249
15. Estêvão MD, Redruello B, Canario AVM, Power DM (2005) Ontogeny of osteonectin expression in embryos and larvae of sea bream (Sparus auratus). Gen Comp Endocrinol 142:155-162 (Pubitemid 40614704)
16. Faustino M, Power DM (1998) Developmental of osteological structures in the sea bream: vertebral column and caudal fin complex. J Fish Biol 52:11-22 (Pubitemid 28110956)
17. Fiujita K (1992) Skeleton of the caudal skeleton in the tetraodontid fish, Takifugu niphobles. Jpn J Ichthyol 38:438-440
18. Gavaia PJ, Simes DC, Ortiz-Delgado JB, Viegas CSB, Pinto JP, Kelsh RN, Sarasquete MC, Cancela ML (2006) Osteocalcin and matrix Gla protein in zebrafish (Danio rerio) and Senegal sole (Solea senegalensis): comparative gene and protein expression during larval development through adulthood. Gene Expr Patterns 6:637-652 (Pubitemid 43785857)
19. Gustafsson E, Fassler R (2000) Insights into extracellular matrix functions from mutant mouse models. Exp Cell Res 261:52-68
20. Hall BK (2005) Bones and cartilage: development and evolutionary skeletal biology. Elsevier Academic, London
21. Hall BK, Witten PE (2007) Plasticity of and transitions between skeletal tissues in vertebrate evolution and development. In: Anderson JS, Sues H-D (eds) Major transitions in vertebrate evolution. Indiana University Press, Bloomington, pp 13-56
22. Hammond CL, Schulte-Merker S (2009) Two populations of endochondral osteoblasts with differential sensitivity to Hedgehog signalling. Development 136:3991-4000
23. Hemre G-I, Dengb D-F, Wilsonb RP, Berntssena MHG (2004) Vitamin A metabolism and early biological responses in juvenile sunshine bass (Morone chrysops x M. saxatilis) fed graded levels of vitamin A. Aquaculture 235:645-658 (Pubitemid 38617271)
24. Hillier ML, Bell LS (2007) Differentiating human bone from animal bone: a review of histological methods. J Forensic Sci 52:249-263 (Pubitemid 46280532)
25. Huysseune A, Sire JY (1990) Ultrastructural observations on chondroid bone in the teleost fish Hemichromis bimaculatus. Tissue Cell 22:371-383 (Pubitemid 20232222)
26. Inohaya K, Takano Y, Kudo A (2007) The teleost intervertebral region acts as a growth center of the centrum: in vivo visualization of osteoblasts and their progenitors in transgenic fish. Dev Dyn 236:3031-3046 (Pubitemid 350175001)
27. Kang JS, Oohashi T, Kawakami Y, Bekku Y, Belmonte JCI, Ninomiya Y (2004) Characterization of dermacan, a novel zebrafish lectican gene, expressed in dermal bones. Mech Dev 121:301-312 (Pubitemid 38293466)
28. Kang Y-J, Stevenon AM, Yau PM, Kollmar R (2008) Sparc protein is required for normal growth of zebrafish otoliths. J Assoc Res Otolaryngol 9:436-451
29. Kardong KV (1998) Vertebrates - comparative anatomy, function, evolution. McGraw-Hill, Boston
30. Kestin SC, Warriss PD (2001) Farmed fish quality. Fishing News Books, Oxford
31. Kleinman HK, Philp D, Hoffman MP (2003) Role of the extracellular matrix in morphogenesis. Curr Opin Biotechnol 14:526-532 (Pubitemid 37298039)
32. Koumoundouros G, Divanach P, Kentouri M (2001a) Osteological development of Dentex dentex (Osteichthyes: Sparidae): dorsal, anal, paired fins and squamation. Mar Biol 138:399-406 (Pubitemid 32180311)
33. Koumoundouros G, Sfakianakis DG, Maingot E, Divanach P, Kentouri M (2001b) Osteological development of the vertebral column and of the fins in Diplodus sargus (Teleostei: Perciformes: Sparidae). Mar Biol 139:853-862 (Pubitemid 34002011)
34. Kranenbarg S, van Cleynenbreugel T, Schipper H, Leeuwen J van (2005) Adaptive bone formation in acellular vertebrae of sea mass (Dicentrarchus labrax, L.). J Exp Biol 208:3493-3502 (Pubitemid 41463271)
35. Lehane DB, McKie N, Russell RG, Henderson IW (1999) Cloning of a fragment of the osteonectin gene from goldfish, Carassius auratus: its expression and potential regulation by estrogen. Gen Comp Endocrinol 114:80-87
36. Marí-Beffa M, Santamaría JA, Murciano C, Santos-Ruiz L, Andrades JA, Guerado E, Becerra J (2007) Zebrafish fins as a model system for skeletal human studies. Sci World J 7:1114-1127 (Pubitemid 47036151)
37. Marks SC, Odgren PR (2002) Structure and development of the skeleton. In: Bilezikian JP, Raisz LG, Rodan GA (eds) Principles of bone biology, vol 1. Academic Press, New York, pp 3-15
38. Meunier FJ, Huysseune A (1992) Tne concept of bone tissue in osteichthyes. Neth J Zool 42:445-458
39. Moss ML (1963) The biology of acellular teleost bone. Ann N Y Acad Sci 109:337-350
40. Mugiya Y, Watabe N (1977) Studies on fish scale formation and resorption. II. Effect of estradiol on calcium homeostasis and skeletal tissue resorption in the goldfish, Carassius auratus, and the killifish, Fundulus heteroclitus. Comp Physiol Biochem 57A:197-202
41. Nakashima K, Crombrugghe B de (2003) Transcriptional mechanisms in osteoblast differentiation and bone formation. Trends Genet 19:458-466 (Pubitemid 36930029)
42. Nishimoto SK, Araki N, Robinson FD, Waitell JH (1992) Discovery of bone γ-carboxyglutamic acid protein in mineralized scales. J Biol Chem 267:11600-11605
43. Nordvik K, Kryvi H, Totland GK, Grotmol S (2005) The salmon vertebral body develops through mineralization of two preformed tissues that are encompassed by two layers of bone. J Anat 206:103-114 (Pubitemid 40372804)
44. Omori M, Sugawara Y, Honda H (1996) Morphogenesis in hatchery-reared larvae of the black rockfish, Sebastes schleeli, and its relationship to the development of swimming and feeding functions. Ichthyol Res 43:267-282
45. Ortego LS, Hawkins WE, Walker WW, Krol RM, Benson WH (1994) Detection of proliferating cell nuclear antigen in tissues of three small fish species. Biotech Histochem 69:317-323
46. Paperna I (1978) Swimbladder and skeletal deformations in hatchery bred Sparus aurata. J Fish Biol 12:109-114
47. Persson P, Takagi Y, Bjornsson BT (1995) Tartrate resistant acid phosphatase as a marker for scale resorption in rainbow trout, Oncorhynchus mykiss: effects of estradiol-17β treatment and refeeding. Fish Physiol Biochem 14:329-339
48. Persson P, Bjornsson BT, Takagi Y (1999) Characterization of morphology and physiological actions of scale osteoclasts in the rainbow trout. J Fish Biol 54:669-684 (Pubitemid 29120498)
49. Pinto JP, Conceicao N, Gavaia PJ, Cancela ML (2003) Matrix Gla protein gene expression and protein accumulation colocalize with cartilage distribution during development of the teleost fish Sparus aurata. Bone 32:201-210 (Pubitemid 36349523)
50. Potthoff T, Kelly S, Javech JC (1986) Cartilage and bone development in scombroid fishes. Fish Bull 84:647-678
51. Rafael MS, Laizé V, Cancela ML (2006) Identification of Sparus aurata bone morphogenetic protein 2: molecular cloning, gene expression and in silico analysis of protein conserved features in vertebrates. Bone 39:1373-1381 (Pubitemid 44827919)
52. Redruello B, Estêvão MD, Rotllant J, Guerreiro PM, Anjos LI, Canario AVM, Power DM (2005) Isolation and characterization of piscine osteonectin and downregulation of its expression by parathyroid hormone-related protein. J Bone Miner Res 20:682-692 (Pubitemid 40393077)
53. Renn J, Winkler C (2009) Osterix-mCherry trangenic medaka for in vivo imaging of bone formation. Dev Dyn 238:241-248
54. Renn J, Winkler C (2010) Characterization of collagen type 10a1 and osteocalcin in early and mature osteoblasts during skeleton formation in medaka. J Appl Ichthyol 26:196-201
55. Renn J, Schaedel M, Volff J-N, Goerlich R, Schartl M, Winkler C (2006a) Dynamic expression of sparc precedes formation of skeletal elements in the medaka (Oryzias latipes). Gene 372:208-218
56. Renn J, Winkler C, Schartl M, Fisher R, Goerlich R (2006b) Zebrafish and medaka as models for bone reserach including implications regarding space-related issues. Protoplasma 229:209-214 (Pubitemid 46016004)
57. Ristovska M, Karaman B, Varraes W, Adriaens D (2006) Early development of the postcranial axial skeleton in Salmo letnica (Karaman, 1924) (Teleostei: Salmonidae). J Fish Biol 68:458-480
58. Rotllant J, Liu D, Yan Y-L, Postlethwait JH, Westerfield M, Du S-J (2008) Sparc (osteonectin) functions in morphogenesis of the pharyngeal skeleton and inner ear. Matrix Biol 27:561-572
59. Sfakianakis DG, Koumoundouros G, Divanach P, Kentori M (2004) Osteological development of the vertebral column and the fins in Pagellus erythrinus (L. 1785). Temperature effect on the developmental plasticity and morpho-anatomical abnormalities. Aquaculture 232:407-424
60. Simmons DJ, Simmons NB, Marshall JH (1970) The uptake of calcium-45 in the acellular-boned toadfish. Calcif Tissue Int 5:206-221
61. Sire J-Y, Huysseune A (1993) Fine structure of the developing frontal bones and scales of the cranial vault in the cichlid fish Hemichromis bimaculatus (Teleostei, Perciformes). Cell Tissue Res 273:511-524 (Pubitemid 23258498)
62. Sommerfeldt DW, Rubin CT (2001) Biology of bone and how it orchestrates the form and function of the skeleton. Eur Spine J 10 (Suppl 2):S86-S95
63. Suzuki N, Suzuki T, Kutokawa T (2000) Suppression of osteoclastic activities by calcitonin in the scales of goldfish (freshwater teleost) and nibbler fish (seawater fish). Peptides 21:115-124 (Pubitemid 30126050)
64. Velleman SG (2000) The role of the extracellular matrix in skeletal development. Poult Sci 79:985-989
65. Wagner EF, Karsenty G (2001) Genetic control of skeletal development. Curr Opin Genet Dev 11:527-532 (Pubitemid 32800726)
66. Wagner TU, Renn J, Riemensperger T, Volff J-N, Koster RW, Goerlich R, Schartl M, Winkler C (2003) The teleost fish medaka (Oryzias latipes) as genetic model to study gravity dependent bone homeostasis in vivo. Adv Space Res 32:1459-1465 (Pubitemid 38034093)
67. Weiss RE, Watabe N (1979) Studies on the biology of fish bon. III. Ultrastructure of osteogenesis and resorption in osteocytic (cellular) and anosteocytic (acellular) bones. Calcif Tissue Int 28:43-56
68. Witten PE (1997) Enzyme histochemical characteristics of osteoblasts and mononucleated osteoclasts in a teleost fish with acellular bone (Oreochromis niloticus, Cichlidae). Cell Tissue Res 287:591-599
69. Witten PE, Hall BK (2002) Differentiation and growth of kype skeletal tissues in anadromous male Atlantic salmon (Salmo salar). Int J Dev Biol 46:719-730
70. Witten PE, Hall BK (2003) Seasonal changes in the lower jaw skeleton in male Atlantic salmon (Salmo salar L.): remodelling and regression of the kype after spawning. J Anat 203:435-450 (Pubitemid 37441575)
71. Witten PE, Huysseune A (2007) Mechanisms of chondrogenesis and osteogenesis in fins. In: Hall BK (ed) Fins into limbs: evolution, development, and transformation. University of Chicago Press, Chicago, pp 79-92
72. Witten PE, Huysseune A (2009) A comparative view on mechanisms and functions of skeletal remodelling in teleost fish, with special emphasis on osteoclasts and their function. Biol Rev 84:315-346
73. Witten PE, Hansen A, Hall BK (2001) Features of mono- and multinucleated bone resorbing cells of the zebrafish Danio rerio and their contribution to skeletal development, remodeling, and growth. J Morphol 250:197-207 (Pubitemid 33087222)
74. Yang X, Karsenty G (2002) Transcription factors in bone: developmental and pathological aspects. Trends Mol Med 8:340-345 (Pubitemid 34733388)
75. Yokoi H, Kobayashi T, Tanaka M, Nagahama Y, Wakamatsu Y, Takeda H, Araki K, Morohashi K, Ozato K (2002) Sox9 in a teleost fish, medaka (Oryzias latipes): evidence for diversified function of Sox9 in gonad differentiation. Mol Reprod Dev 63:5-16 (Pubitemid 34831308)
76. Young B, Lowe JS, Stevens A, Heath JW (2006) Wheater's functional histology: a text and colour atlas. Churchill Livingstone, London