Vitamin A effects on vertebral bone tissue homeostasis in gilthead sea bream (Sparus aurata) juveniles

Journal of Applied Ichthyology

Volumn 28, Issue 3, 2012, Pages 419-426

  Fernandez I ^a   Ortiz Delgado, J B ^b   Sarasquete, C ^b   Gisbert, E ^a  

^a IRTA   (Spain)

^b INSTITUTO DE CIENCIAS MARINAS DE ANDALUCÍA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ARCHOSARGUS RHOMBOIDALIS; SPARUS AURATA; TELEOSTEI;

EID: 84861303323     PISSN: 01758659     EISSN: 14390426     Source Type: Journal    
DOI: 10.1111/j.1439-0426.2012.01997.x     Document Type: Article

References (65)

1. Aguiar, D. J.; Johnson, S. L.; Oegema, T. R., 1999: Notochordal cells interact with nucleus pulposus cells: regulation of proteoglycan synthesis. Exp. Cell Res. 246, 129-137.
2. Arratia, G.; Schultze, H. P.; Casciotta, J., 2001: Vertebral column and associated elements in dipnoans and comparison with other fishes: development and homology. J. Morphol. 250, 101-172.
3. Bancroft, J. D.; Stevens, A., 1990: Theory and practice of histological techniques, 3rd edn. Churchill Livingstone, Edinburgh, London, Melbourne and New York, pp. 726.
4. Boglione, C.; Costa, C., 2011: Skeletal deformities and juvenile quality. In: Sparidae: biology and aquaculture of Gilthead Sea Bream and other species, biology and aquaculture of Gilthead Sea Bream and other species. M. A. Pavlidis, C. C. Mylonas (Eds). Wiley-Blackwell, Oxford, UK., 233-294.
5. Chatain, B., 1994: Abnormal swimbladder development and lordosis in sea bass (Dicentrarchus labrax) and sea bream (Sparus auratus). Aquaculture 119, 371-379.
6. Cleaver, O.; Krieg, P. A., 2001: Notochord patterning of the endoderm. Dev. Biol. 234, 1-12.
7. Coleman, R., 2011: Picrosirius red staining revisited. Acta Histochem. 113, 231-233.
8. Compston, J. E., 2001: Sex steroids and bone. Physiol. Rev. 81, 419-447.
9. Debessa, C. R. G.; Maifrino, L. B. M.; de Souza, R. R., 2001: Age related changes of the collagen network of the human heart. Mech. Age. Dev. 122, 1049-1058.
10. Faustino, M.; Power, D. M., 1998: Development of osteological structures in the sea bream: vertebral column and caudal fin complex. J. Fish Biol. 52, 11-22.
11. Faustino, M.; Power, D. M., 1999: Development of the pectoral, pelvic, dorsal and anal fins in cultured sea bream. J. Fish Biol. 54, 1094-1110.
12. Faustino, M.; Power, M. D., 2001: Osteologic development of the viscerocranial skeleton in sea bream: alternative ossification strategies in teleost fish. J. Fish Biol. 58, 537-572.
13. Fernández, I.; Gisbert, E., 2010: Senegalese sole bone tissue originated from chondral ossification is more sensitive than dermal bone to high vitamin A content in enriched Artemia. J. Appl. Ichthyol. 26, 344-349.
14. Fernández, I.; Gisbert, E., 2011: The effect of vitamin A on flatfish development and skeletogenesis: a review. Aquaculture 315, 34-48.
15. Fernández, I.; Hontoria, F.; Ortiz-Delgado, J. B.; Kotzamanis, Y.; Estévez, A.; Zambonino-Infante, J. L.; Gisbert, E., 2008: Larval performance and skeletal deformities in farmed gilthead sea bream (Sparus aurata) fed with graded levels of Vitamin A enriched rotifers (Brachionus plicatilis). Aquaculture 283, 102-115.
16. Fernández, I.; Pimentel, M. S.; Ortiz-Delgado, J. B.; Hontoria, F.; Sarasquete, C.; Estévez, A.; Zambonino-Infante, J. L.; Gisbert, E., 2009: Effect of dietary vitamin A on Senegalese sole, Solea senegalensis skeletogenesis and larval quality. Aquaculture 295, 250-265.
17. Fernández, I.; Darias, M.; Andree, K. B.; Mazurais, D.; Zambonino-Infante, J. L.; Gisbert, E., 2011: Coordinated gene expression during gilthead sea bream skeletogenesis and its disruption by nutritional hypervitaminosis A. BMC Dev. Biol. 11, 7.
18. Fleming, A.; Keynes, R.; Tannahill, D., 2004: A central role for the notochord in vertebral patterning. Development 131, 873-880.
19. Gavaia, P. J.; Simes, D. C.; Ortiz-Delgado, J. B.; Viegas, C. S. B.; Pinto, J. P.; Kelsh, R. N.; Sarasquete, M. C.; Cancela, M. L., 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.
20. Glickman, N. S.; Kimmel, C. B.; Jones, M. A.; Adams, R. J., 2003: Shaping the zebrafish notochord. Development 130, 873-887.
21. Gorman, K. F.; Breden, F., 2007: Teleosts as models for human vertebral stability and deformity. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 145, 28-38.
22. Gorman, K. F.; Handrigan, G. R.; Jin, G.; Wallis, R.; Breden, F., 2010: Structural and micro-anatomical changes in vertebrae associated with idiopathic-type spinal curvature in the curveback guppy model. Scoliosis 5, 10.
23. Grotmol, S.; Kryvi, H.; Nordvik, K.; Totland, G. K., 2003: Notochord segmentation may lay down the pathway for the development of the vertebral bodies in the Atlantic salmon. Anat. Embryol. 207, 263-272.
24. Grotmol, S.; Nordvik, K.; Kryvi, H.; Totland, G. K., 2005: A segmental pattern of alkaline phosphatase activity within the notochord coincides with the initial formation of the vertebral bodies. J. Anat. 206, 427-436.
25. Grotmol, S.; Kryvi, H.; Keynes, R.; Krossoy, C.; Nordvik, K.; Totland, G. K., 2006: Stepwise enforcement of the notochord and its intersection with the myoseptum: an evolutionary path leading to development of the vertebra? J. Anat. 209, 339-357.
26. Gustafsson, E.; Fassler, R., 2000: Insights into extracellular matrix functions from mutant mouse models. Exp. Cell Res. 261, 52-68.
27. Haga, Y.; Dominique, V. J.; Du, S. J., 2009: Analyzing notochord segmentation and intervertebral disc formation using the twhh: gfp transgenic zebrafish model. Transgenic Res. 18, 669-683.
28. Hall, B. K., 2005: Bones and cartilage: developmental skeletal biology. Academic Press, London.
29. Hernández, L. H. H.; Teshima, S. I.; Ishikawa, M.; Alam, S.; Koshio, S.; Tanaka, Y., 2005: Dietary vitamin A requirements of juvenile Japanese flounder Paralichthys olivaceus. Aquacult. Nutr. 11, 3-9.
30. Huysseune, A., 2000: Skeletal system. In: The laboratory fish. G. Ostrander (Ed.). Academic Press, London, pp. 307-317.
31. Iwasaki, M.; Jikko, A.; Le, A. X., 1999: Age-dependent effects of hedgehog protein on chondrocytes. J. Bone Joint Surg. Br. 81, 1076-1082.
32. Kanemoto, M.; Hukuda, S.; Komiya, Y.; Katsuura, A.; Nishioka, J.;, 1996: Immunohistochemical study of matrix metalloproteinase-3 and tissue inhibitor of metalloproteinase-1 in human intervertebral discs. Spine 21, 1-8.
33. Kiernan, J. A., 2008: Histological and histochemical methods: theory and practice, 4th edn. Scion, Bloxham, UK.
34. Koumoundouros, G., 2010: Morpho-anatomical abnormalities in Mediterranean marine aquaculture. In: Recent advances in aquaculture research. G. Koumoundouros (ed.). Transworld Research Network, Kerala, India, pp. 125-148.
35. Kranenbarg, S.; Waarsing, J. H.; Muller, M.; Weinans, H.; van Leeuwen, J. L., 2005a: Lordotic vertebrae in sea bass (Dicentrarchus labrax L.) are adapted to increased loads. J. Biomech. 38, 1239-1246.
36. Kranenbarg, S.; van Cleynenbreugel, T.; Schipper, H.; van Leeuwen, J., 2005b: Adaptive bone formation in acellular vertebrae of sea bass (Dicentrarchus labrax L.). J. Exp. Biol. 208, 3493-3502.
37. Lall, S. P.; Lewis-McCrea, L., 2007: Role of nutrients in skeletal metabolism and pathology in fish, an overview. Aquaculture 267, 3-19.
38. Laue, K.; Jänicke, M.; Plaster, N.; Sonntag, C.; Hammerschmidt, M., 2008: Restriction of retinoic acid activity by Cyp26b1 is required for proper timing and patterning of osteogenesis during zebrafish development. Development 135, 3775-3787.
39. Lewis-McCrea, L. M.; Lall, S. P., 2010: Effects of phosphorus and vitamin C deficiency, vitamin A toxicity, and lipid peroxidation on skeletal abnormalities in Atlantic halibut (Hippoglossus hippoglossus). J. Appl. Ichthyol. 26, 334-343.
40. Marin, F.; Luquet, G.; Marie, B.; Medakovic, D., 2007: Molluscan shell proteins: primary structure, origin, and evolution. Curr. Top. Dev. Biol. 80, 209-276.
41. Martoja, R.; Martoja-Pierson, M., 1970: Técnicas de histología animal, Toray Masson S. A., Barcelona.
42. Mazurais, D.; Glynatsi, N.; Darias, M. J.; Christodoulopoulou, S.; Cahu, C. L.; Zambonino-Infante, J. L.; Koumoundouros, G., 2009: Optimal levels of dietary vitamin A for reduced deformity incidence during development of European sea bass larvae (Dicentrarchus labrax) depend on malformation type. Aquaculture 294, 262-270.
43. Midura, R. J.; Hascall, V. C., 1996: Bone sialoprotein-a mucin in disguise? Glycobiology 6, 677-681.
44. Nordvik, K.; Kryvi, H.; Totland, G. K.; 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.
45. Ortiz-Delgado, J. B.; Simes, D. C.; Gavaia, P.; Sarasquete, C.; Cancela, M. L., 2005: Osteocalcin and matrix GLA protein in developing teleost teeth: identification of sites of mRNA and protein accumulation at single cell resolution. Histochem. Cell Biol. 124, 123-130.
46. Palazón-Fernández, J. L. 2008. Biología y atlas histológico del pez sapo, Halobatrachus didactylus (Schneider, 1801) (Pisces: Batrachoididae) de la Bahía de Cádiz. PhD Thesis. Universidad de Cadiz, Spain.
47. Pearse, A. G. E., 1985: Histochemistry. Theoretical and applied. Vol. 2 Analytical Technology, 4th edn. Churchill Livingstone. New York. NY.
48. Pinto, J. P.; Ohresser, M. C. P.; Cancela, M. L., 2001: Cloning of the bone Gla protein gene from the teleost fish Sparus aurata. Evidence for overall conservation in gene organization and bone-specific expression from fish to man. Gene 270, 77-91.
49. Rich, L.; Whittaker, L., 2005: Collagen and picrosirius red staining: a polarized light assessment of fibrillar hue and spatial distribution. Braz. J. morphol. Sci. 22, 97-104.
50. Roberto, V. P.; Cavaco, S.; Viegas, C. S. B.; Simes, D. C.; Ortiz-Delgado, J. B.; Sarasquete, M. C.; Gavaia, P. J.; Cancela, M. L., 2009: Matrix Gla protein in turbot (Scophthalmus maximus): gene expression analysis and identification of sites of protein accumulation. Aquaculture 294, 202-211.
51. Ross, S. A.; Caffery, P. J.; Draguer, U. C.; De Luca, L. M., 2000: Retinoids in embryonal development. Physiol. Rev. 80, 1021-1054.
52. Sæle, Ø.; Solvakken, J. S.; Watanabe, K.; Hamre, K.; Pittman, K., 2003: The effect of diet on ossification and eye migration in Atlantic halibut larvae (Hippoglossus hippoglossus L.). Aquaculture 220, 683-696.
53. Sarasquete, C.; Gutiérrez, M., 2005: New tetrachromic VOF stain (Type III-G.S) for normal and pathological fish tissues. Eur. J. Histochem. 49, 105-114.
54. Simes, D. C.; Williamson, M. K.; Schaff, B. J.; Gavaia, P. J.; Ingleton, P. M.; Price, P. A.; Cancela, M. L., 2003: Characterization of osteocalcin (BGP) and matrix Gla protein (MGP) fish specific antibodies: validation for immunodetection studies in lower vertebrates. Calcif. Tissue Int. 74, 170-180.
55. Sire, J. Y.; Donoghue, P. C. J.; Vickaryous, M. K., 2009: Origin and evolution of the integumentary skeleton in non-tetrapod vertebrates. J. Anat. 214, 409-440.
56. Sivan, S. S.; Tsitron, E.; Wachtel, E.; Roughley, P. J.; Sakkee, N.; Van Der Ham, F.; DeGroot, J.; Roberts, S.; Maroudas, A., 2006: Aggrecan turnover in human intervertebral disc as determined by the racemization of aspartic acid. J. Biol. Chem. 281, 13009-13014.
57. Spoorendonk, K. M.; Peterson-Maduro, J.; Renn, J.; Trowe, T.; Kranenbarg, S.; Winkler, C.; Schulte-Merker, S., 2008: Retinoic acid and Cyp26b1 are critical regulators of osteogenesis in the axial skeleton. Development 135, 3765-3774.
58. Varghese, S.; Rydziel, S.; Jeffrey, J. J.; Canalis, E., 1994: Regulation of interstitial collagenase expression and collagen degradation by retinoic acid in bone cells. Endocrinology 134, 2438-2444.
59. Watanabe, N.; Kawashima, H.; Li, Y. F.; Miyasaka, M., 1999: Identification and characterization of ligands for L-selectin in the kidney. III. Characterization of L-selectin reactive heparan sulfate proteoglycans. J. Biochem. 125, 826-831.
60. Witten, P. E.; Hall, B. K., 2002: Differentiation and growth of kype skeletal tissues in anadromous male Atlantic salmon (Salmo salar). Int. J. Dev. Biol. 46, 719-730.
61. Witten, P.E.; Huysseune, A., 2007: Mechanisms of chondrogenesis and osteogenesis in fins. In: Fins and limbs; development, evolution and transformation. B.K. Hall (Ed.). Chicago University Press, Chicago, pp. 79-92.
62. Witten, P. E.; Gil-Martens, L.; Huysseune, A.; Takle, H.; Hjelde, K., 2009: Towards a classification and an understanding of developmental relationships of vertebral body malformations in Atlantic salmon (Salmo salar L.). Aquaculture 295, 6-14.
63. Witten, P. E.; Gil-Martens, L.; Hall, B. K.; Huysseune, A.; Obach, A., 2005: Compressed vertebrae in Atlantic salmon Salmo salar: evidence for metaplastic chondrogenesis as a skeletogenic response late in ontogeny. Dis. Aquat. Org. 64, 237-246.
64. Ytteborg, E.; Torgersen, J. S.; Pedersen, M. E.; Baeverfjord, G.; Hannesson, K. O.; Takle, H., 2010a: Remodeling of the notochord during development of vertebral fusions in Atlantic salmon (Salmo salar). Cell Tissue Res. 342, 363-376.
65. Ytteborg, E.; Torgersen, J.; Baeverfjord, G.; Hjelde, K.; Takle, H., 2010b: Morphological and molecular characterization of developing vertebral fusions using a teleost model. BMC Physiol. 10, 13.