Mineralization of the vertebral bodies in Atlantic salmon (Salmo salar L.) is initiated segmentally in the form of hydroxyapatite crystal accretions in the notochord sheath

Journal of Anatomy

Volumn 223, Issue 2, 2013, Pages 159-170

  Wang, Shou ^a   Kryvi, Harald ^a   Grotmol, Sindre ^a   Wargelius, Anna ^b   Krossøy, Christel ^a   Epple, Mattias ^c   Neues, Frank ^c   Furmanek, Tomasz ^b   Totland, Geir K ^a  

^a UNIVERSITY OF BERGEN   (Norway)

^b INSTITUTE OF MARINE RESEARCH   (Norway)

^c UNIVERSITY OF DUISBURG ESSEN   (Germany)

Author keywords

Collagen; Hydroxyapatite; Mineralization; Notochord; Salmon

Indexed keywords

COLLAGEN FIBRIL; COLLAGEN TYPE 1; COLLAGEN TYPE 2; HYDROXYAPATITE; PARATHYROID HORMONE RECEPTOR 1; SONIC HEDGEHOG PROTEIN; TRANSFORMING GROWTH FACTOR BETA1;

AMPLICON; ARTICLE; ATLANTIC SALMON; BONE DEVELOPMENT; BONE MINERALIZATION; CRYSTALLIZATION; MOLECULAR BIOLOGY; MORPHOLOGY; NONHUMAN; NOTOCHORD; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; SCLEROTOME; SYNCHROTRON; VERTEBRA BODY; X RAY DIFFRACTION;

COLLAGEN; HYDROXYAPATITE; MINERALIZATION; NOTOCHORD; SALMON;

ANIMALS; ANIMALS, NEWBORN; BIOLOGICAL MARKERS; CALCIFICATION, PHYSIOLOGIC; COLLAGEN; DURAPATITE; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MICROSCOPY, ELECTRON, TRANSMISSION; NOTOCHORD; SALMO SALAR; SPINE; X-RAY DIFFRACTION;

ERINACEIDAE; SALMO SALAR; TELEOSTEI;

EID: 84880144911     PISSN: 00218782     EISSN: 14697580     Source Type: Journal    
DOI: 10.1111/joa.12067     Document Type: Article

References (53)

1. Abbink W, Glik G (2007) Parathyroid hormone-related protein in teleost fish. Gen Comp Endocrinol 152, 243-251.
2. Adams DS, Keller R, Koehl MAR (1990) The mechanics of notochord elongation, straightening and stiffening in the embryo of Xenopus laevis. Development 110, 115-130.
3. Alvarez J, Sohn P, Zeng X, et al. (2002) TGFbeta2 mediates the effects of hedgehog on hypertrophic differentiation and PTHrP expression. Development 129, 1913-1924.
4. Anderson H, Garimella R, Tague SE (2005) The role of matrix vesicles in growth plate development and biomineralization. Front Biosci 10, 822-837.
5. Becker A, Epple M, Müller KM, et al. (2004) A comparative study of clinically well-characterized human atherosclerotic plaques with histological, chemical, and ultrastructural methods. J Inorg Biochem 98, 2032-2038.
6. Bensimon-Brito A, Cardeira J, Cancela ML, et al. (2012) Distinct patterns of notochord mineralization in zebrafish coincide with the localization of Osteocalcin isoform 1 during early vertebral centra formation. BMC Dev Biol 12, 28.
7. Bhattacharya P, Yan YL, Postlethwait J, et al. (2011) Evolution of the vertebrate pth2 (tip39) gene family and the regulation of PTH type 2 receptor (pth2r) and its endogenous ligand pth2 by hedgehog signalling in zebrafish development. J Endocrinol 211, 187-200.
8. Blaschke UK, Eikenberry EF, Hulmes DJ, et al. (2000) Collagen XI nucleates self-assembly and limits lateral growth of cartilage fibrils. J Biol Chem 275, 10370-10378.
9. Bonucci E (2012) Bone mineralization. Front Biosci 17, 100-128.
10. Boskey AL (2007) Mineralization of bones and teeth. Elements 3, 387-393.
11. Choi K-S, Cohn MJ, Harfe BD (2008) Identification of nucleus pulposus precursor cells and notochordal remnants in the mouse: implications for disk degeneration and chordoma formation. Dev Dyn 237, 3953-3958.
12. Chung UI, Schipani E, McMahon AP, et al. (2001) Indian hedgehog couples chondrogenesis to osteogenesis in endochondral bone development. J Clin Invest 107, 295-304.
13. Coutinho P, Parsons MJ, Thomas KA, et al. (2004) Differential requirements for COPI transport during vertebrate early development. Dev Cell 7, 547-558.
14. Currie PD, Ingham PW (1996) Induction of a specific muscle cell type by a hedgehog-like protein in zebrafish. Nature 382, 452-455.
15. Dahia CL, Mahoney E, Wylie C (2012) Shh signaling from the nucleus pulposus is required for the postnatal growth and differentiation of the mouse intervertebral disc. PLoS ONE 7, e35944.
16. Dorozhkin SV, Epple M (2002) Biological and medical significance of calcium phosphates. Angew Chem Int Ed Engl 41, 3130-3146.
17. Eikenberry EF, Childs B, Sheren SB, et al. (1984) Crystalline fibril structure of type II collagen in lamprey notochord sheath. J Mol Biol 176, 261-277.
18. Fleming A, Keynes R, Tannahill D (2004) A central role for the notochord in vertebral patterning. Development 131, 873-880.
19. Glimcher MJ (2006) Bone: nature of the calcium phosphate crystals and cellular, structural, and physical chemical mechanisms in their formation. Rev Mineral Geochem 64, 223-282.
20. Gorski JP (2011) Biomineralization of bone: a fresh view of the roles of non-collagenous proteins. Front Biosci 16, 2598-2621.
21. Grotmol S, Kryvi H, Nordvik K, et al. (2003) Notochord segmentation may lay down the pathway for the development of the vertebral bodies in the Atlantic salmon. Anat Embryol (Berl) 207, 263-272.
22. Grotmol S, Nordvik K, Kryvi H, et al. (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.
23. Grotmol S, Kryvi H, Keynes R, et al. (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.
24. Hall BK (2005) The Search for the Magic Bullet. In: Bones and Cartilage: Developmental and Evolutionary Skeletal Biology. (ed. Hall BK), pp. 525-526, London: Elsevier Academic Press.
25. Huq NL, Cross KJ, Ung M, et al. (2005) A review of protein structure and gene organisation for proteins associated with mineralised tissue and calcium phosphate stabilisation encoded on human chromosome 4. Arch Oral Biol 50, 599-609.
26. Janvier P (1996) Early Vertebrates. Oxford: Clarendon Press.
27. Karp SJ, Schipani E, St-Jacques B, et al. (2000) Indian hedgehog coordinates endochondral bone growth and morphogenesis via parathyroid hormone related-protein-dependent and -independent pathways. Development 127, 543-548.
28. Karsenty G (2003) The complexities of skeletal biology. Nature 423, 316-318.
29. Knapp M, Baehtz C, Ehrenberg H, et al. (2004a) The synchrotron powder diffractometer at beamline B2 at HASYLAB/DESY: status and capabilities. J Synchrotron Radiat 11, 328-334.
30. Knapp M, Joco V, Baehtz C, et al. (2004b) Position-sensitive detector system OBI for high resolution X-ray powder diffraction using on-site readable image plates. Nucl Instr Methods Phys Res 521, 565-570.
31. Koehl MAR, Quillin K, Pell C (2000) Mechanical design of fiber-wound hydraulic skeletons: the stiffening and straightening of embryonic notochords. Am Zool 40, 28-41.
32. Krauss S, Concordet JP, Ingham PW (1993) A functionally conserved homolog of the Drosophila segment polarity gene hh is expressed in tissues with polarizing activity in zebrafish embryos. Cell 75, 1431-1444.
33. Kronenberg HM (2003) Developmental regulation of the growth plate. Nature 423, 332-336.
34. Landis WJ, Silver FH (2009) Mineral deposition in the extracellular matrices of vertebrate tissues: identification of possible apatite nucleation sites on type I collagen. Cells Tissues Organs 189, 20-24.
35. Lanske B, Karaplis AC, Lee K, et al. (1996) PTH/PTHrP receptor in early development and Indian hedgehog-regulated bone growth. Science 273, 663-666.
36. Lefebvre V, Bhattaram P (2010) Vertebrate skeletogenesis. Cur Top Dev Biol 90, 291-317.
37. Nordvik K, Kryvi H, Totland GK, et al. (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.
38. Olsvik PA, Lie KK, Jordal A-EO, et al. (2005) Evaluation of potential reference genes in real-time RT-PCR studies of Atlantic salmon. BMC Mol Biol 17, 6-21.
39. Peters F, Schwarz K, Epple M (2000) The structure of bone studied with synchrotron X-ray diffraction, X-ray absorption spectroscopy and thermal analysis. Thermochim Acta 361, 131-138.
40. Qin C, Baba O, Butler WT (2004) Post-translational modifications of sibling proteins and their roles in osteogenesis and dentinogenesis. Crit Rev Oral Biol Med 15, 126-136.
41. Sagstad A, Grotmol S, Kryvi H, et al. (2011) Identification of vimentin- and elastin-like transcripts specifically expressed in developing notochord of Atlantic salmon (Salmo salar L.). Cell Tissue Res 346, 191-202.
42. Sasaki N, Tagami A, Goto T, et al. (2002) Atomic force microscopic studies on the structure of bovine femoral cortical bone at the collagen fibril-mineral level. J Mater Sci Mater Med 13, 333-337.
43. Schmitt F (1956) Macromolecular interaction patterns in biological systems. Proc Am Philos Soc 100, 476-486.
44. Senthinathan B, Sousa C, Tannahill D, et al. (2012) The generation of vertebral segmental patterning in the chick embryo. J Anat 220, 591-602.
45. Stemple DL (2005) Structure and function of the notochord: an essential organ for chordate development. Development 132, 2503-2512.
46. Stern CD (1990) Two distinct mechanisms for segmentation? Semin Dev Biol 1, 109-116.
47. St-Jacques B, Hammerschmidt M, McMahon AP (1999) Indian hedgehog signaling regulates proliferation and differentiation of chondrocytes and is essential for bone formation. Genes Dev 13, 2072-2086. Erratum in: Genes Dev 13, 2617.
48. Veis A (2003) Mineralization in organic matrix frameworks. Rev Mineral Geochem 54, 249-289.
49. Wang Y, Azaïs T, Robin M, et al. (2012) The predominant role of collagen in the nucleation, growth, structure and orientation of bone apatite. Nat Mater 11, 724-733.
50. Wargelius A, Fjelldal PG, Nordgarden U, et al. (2010) Collagen type XI (α1) may be involved in the structural plasticity of the vertebral column in Atlantic salmon (Salmo salar L.). J Exp Biol 213, 1207-1216.
51. Wenstrup RJ, Smith SM, Florer JB, et al. (2004) Regulation of collagen fibril nucleation and initial fibril assembly involves coordinate interactions with collagens V and XI in developing tendon. J Biol Chem 279, 53331-53337.
52. Yu B, Zhao X, Yang C, et al. (2012) Parathyroid hormone induces differentiation of mesenchymal stromal/stem cells by enhancing bone morphogenetic protein signalling. J Bone Miner Res 27, 2001-2014.
53. Zhu W, Robey PG, Boskey AL (2008) The regulatory role of matrix proteins in mineralization of bone. In: Osteoporosis. (eds Marcus R, Feldman D, Nelson D, Rosen C), 3rd edn, pp. 191-240, New York: Elsevier.