Mineral homeostasis and regulation of mineralization processes in the skeletons of sharks, rays and relatives (Elasmobranchii)

Seminars in Cell and Developmental Biology

Volumn 46, Issue , 2015, Pages 51-67

  Dean, Mason N ^a   Ekstrom, Laura ^b   Monsonego Ornan, Efrat ^c   Ballantyne, Jim ^d   Witten, P Eckhard ^e   Riley, Cyrena ^f   Habraken, Wouter ^a   Omelon, Sidney ^g  

^a MAX PLANCK INSTITUTE OF COLLOIDS AND INTERFACES   (Germany)

^b WHEATON COLLEGE   (United States)

^c HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^d UNIVERSITY OF GUELPH   (Canada)

^e GHENT UNIVERSITY   (Belgium)

^f UNIVERSITÉ DU QUÉBEC À RIMOUSKI   (Canada)

^g UNIVERSITY OF OTTAWA   (Canada)

Author keywords

Apatite; Biomineralization; Elasmobranch; Skeleton; Tessellated cartilage; Tesserae

Indexed keywords

CALCIUM; HORMONE; MINERAL; PHOSPHATE; BICARBONATE;

BIOMINERALIZATION; BONE DEVELOPMENT; BONE MINERALIZATION; CALCIFICATION; CALCIUM BLOOD LEVEL; CARTILAGE; CRYSTALLIZATION; ELASMOBRANCH; FISH; GENETIC REGULATION; HOMEOSTASIS AND REGULATION; HORMONAL REGULATION; MAMMAL; MINERAL METABOLISM; NONHUMAN; ONTOGENY; PHOSPHATE BLOOD LEVEL; RAY; REVIEW; SHARK; SKELETON; VERTEBRATE; ANIMAL; CLASSIFICATION; HOMEOSTASIS; METABOLISM; SKATES (FISH);

ANIMALS; BICARBONATES; CALCIUM; CARTILAGE; ELASMOBRANCHII; HOMEOSTASIS; MINERALS; PHOSPHATES; SHARKS; SKATES (FISH);

EID: 84952637818     PISSN: 10849521     EISSN: 10963634     Source Type: Journal    
DOI: 10.1016/j.semcdb.2015.10.022     Document Type: Review

References (228)

1. Currey J.D. Bones 2002, Princeton University Press, Princeton.
2. Lowenstam H.A., Weiner S. On Biomineralization 1989, Oxford University Press.
3. Knoll A.H. Biomineralization and evolutionary history. Rev. Mineral. Geochem. 2003, 54:329-356.
4. Urist M.R. Calcium and phosphorus in the blood and skeleton of the Elasmobranchii. Endocrinology 1961, 69:778-801.
5. Applegate S.P. A survey of shark hard parts. Sharks, Skates, Rays 1967, 37-66. Johns Hopkins Press, Maryland. P.W. Gilbert, R.F. Mathewson, D.P. Rall (Eds.).
6. Moss S.A. Skeletal tissues in sharks. Am. Zool. 1977, 17:335-342.
7. Omelon S., Georgiou J., Variola F., Dean M.N. Colocation and role of polyphosphates and alkaline phosphatase in apatite biomineralization of elasmobranch tesserae. Acta Biomater. 2014, 10:3899-3910.
8. Kemp N.E., Westrin S.K. Ultrastructure of calcified cartilage in the endoskeletal tesserae of sharks. J. Morphol. 1979, 160:75-101.
9. Clement J.G. Re-examination of the fine structure of endoskeletal mineralization in Chondrichthyes: implications for growth, ageing and calcium homeostasis. Aust. J. Mar. Freshw. Res. 1992, 43:157-181.
10. Dean M.N., Mull C.G., Gorb S.N., Summers A.P. Ontogeny of the tessellated skeleton: insight from the skeletal growth of the round stingray Urobatis halleri. J. Anat. 2009, 215:227-239.
11. Bordat C. Les cartilages calcifiés de la petite roussette (Scyliorhinus canicula L., Chondrichthyens): histologie et ultrastructure. Can. J. Zool. 1988, 66:1432-1445.
12. Egerbacher M., Helmreich M., Mayrhofer E., Böck P. Mineralisation of the hyaline cartilage in the small-spotted dogfish Scyliorhinus canicula L. Scr. Med. (BRNO) 2006, 79:199-212.
13. Enault S., Muñoz D.N., Silva W.T., Borday-Birraux V., Bonade M., Oulion S., et al. Molecular footprinting of skeletal tissues in the catshark Scyliorhinus canicula and the clawed frog Xenopus tropicalis identifies conserved and derived features of vertebrate calcification. Front. Genet. 2015, 6:283.
14. Benzer P. Morphology of calcification in Squalus acanthias. Copeia 1944, 1944:217.
15. Schmidt W.J. Über Die Verkalkung Des Knorpelgewebes Der Haie. Z. Zellforsch. Mikrosk. Anat. 1952, 37:377-388.
16. Doyle J. Ageing changes in cartilage from Squalus acanthias L. Comp. Biochem. Physiol. 1968, 25:201.
17. Ashhurst D.E. The cartilaginous skeleton of an elasmobranch fish does not heal. Matrix Biol. 2004, 23:15-22.
18. Maisey J.G. The diversity of tessellated calcification in modern and extinct chondrichthyans. Rev. Paléobiol. Genève 2013, 32:355-371.
19. Lund R., Grogan E.D. Relationships of the Chimaeriformes and the basal radiation of the Chondrichthyes. Rev. Fish Biol. Fish. 1997, 7:65-123.
20. Ørvig T. Histologic studies of placoderms and fossil elasmobranchs. I: The endoskeleton, with remarks on the hard tissues of lower vertebrates in general. Ark. Zool. 1951, 2:321-454.
21. Ridewood W.G. On the calcification of the vertebral centra in sharks and rays. Philos. Trans. R. Soc. B: Biol. Sci. 1921, 210:311-407.
22. Dean M.N., Summers A.P. Cartilage in the skeleton of cartilaginous fishes. Zoology 2006, 109:164-168.
23. Hasse J.C.F. Über den Bau und über die Entwickelung des Knorpels bei den Elasmobranchiern. Zool. Anz. 1879, 2:325-374.
24. Cailliet G.M., Smith W.D., Mollet H.F., Goldman K.J. Age and Growth Studies of Chondrichthyan Fishes: The Need for Consistency in Terminology, Verification, Validation, and Growth Function Fitting. Special Issue: Age and Growth of Chondrichthyan Fishes: New Methods, Techniques and Analysis 2006, 211-228. Springer Science+Business Media.
25. Caillet G.M., Goldman K.J. Age determination and validation in chondrichthyan fishes. Biology of Sharks and Their Relatives 2004, 399-447. CRC Press, Chicago. J.C. Carrier, J.A. Musick, M.R. Heithaus (Eds.).
26. Devillers C.H. Structure et évolution de la colonne vertébrale. Traité de Zoologie 1954, vol. 12:605-672. Masson et Cie, Paris.
27. Compagno L.J.V. Endoskeleton. Sharks, Skates, and Rays: The Biology of Elasmobranch Fishes 1999, 69-92. Johns Hopkins Press, Baltimore. W.C. Hamlett (Ed.).
28. Smith W.D., Miller J.A., Heppell S.S. Elemental markers in elasmobranchs: effects of environmental history and growth on vertebral chemistry. PLOS ONE 2013, 8:e62423.
29. Urist M.R. Further observations bearing on the bone-body fluid continuum: composition of the skeleton and serums of cyclostomes, elasmobranchs, and bony vertebrates. Bone Biodyn. 1964, 151-179.
30. Urist M.R. Biogenesis of bone: calcium and phosphorus in the skeleton and blood in vertebrate evolution. Handbook of Physiology, Endocrinology 1976, 183-213. American Physiological Society, Washington, DC, USA.
31. Ballantyne J.S., Fraser D.I. Euryhaline elasmobranchs. Euryhaline Fishes: Fish Physiology 2013, vol. 32:125-198. Academic Press, Amsterdam.
32. Rao D.S., Raghuramulu N. Vitamin D3 and its metabolites have no role in calcium and phosphorus metabolism in Tilapia mossambica. J. Nutr. Sci. Vitaminol. 1999, 45:9-19.
33. Flik G., Verbost P.M. Calcium homeostasis in fish. The Comparative Endocrinology of Calcium Regulation 1996, 43-53. The Journal of Endocrinology Ltd, Bristol. C. Dacke, J. Danks, I. Caple, G. Flik (Eds.).
34. Anderson W.G., Dasiewicz P.J., Liban S., Ryan C., Taylor J.R., Grosell M., et al. Gastro-intestinal handling of water and solutes in three species of elasmobranch fish, the white-spotted bamboo shark, Chiloscyllium plagiosum, little skate, Leucoraja erinacea and the clear nose skate Raja eglanteria. Comp. Biochem. Physiol. A: Mol. Integr. Physiol. 2010, 155:493-502.
35. Wood C.M., Matsuo A.Y.O., Gonzalez R.J., Wilson R.W., Patrick M.L., Val A.L. Mechanisms of ion transport in Potamotrygon, a stenohaline freshwater elasmobranch native to the ion-poor blackwaters of the Rio Negro. J. Exp. Biol. 2002, 205:3039-3054.
36. Flik G., Klaren P.H.M., Schoenmakers T.J.M., Bijvelds M.J.C., Verbost P.M., Wendelaar Bonga S.E. Cellular calcium transport in fish: unique and universal mechanisms. Physiol. Zool. 1996, 69:403-417.
37. Witten P.E., Huysseune A. A comparative view on mechanisms and functions of skeletal remodelling in teleost fish, with special emphasis on osteoclasts and their function. Biol. Rev. 2009, 84:315-346.
38. Schoenmakers T.J.M., Verbost P.M., Wendelaar Bonga S.E. Transcellular intestinal calcium transport in freshwater and seawater fish and its dependence on sodium calcium exchange. J. Exp. Biol. 1993, 176:195-206.
39. Moss M.L. Studies of the acellular bone of teleost fish. II. Response to fracture under normal and acalcemic conditions. Cells Tissues Organs 1962, 48:46-60.
40. Takagi Y., Yamada J. Effects of Calcium and Phosphate Deficiencies on Bone Metabolism in a Teleost, Tilapia (Oreochromis niloticus): A Histomorphometric Study. Mechanisms and Phylogeny of Mineralization in Biological Systems 1991, 187-191. Springer-Verlag, Tokyo.
41. Takagi Y., Yamada J. Effects of calcium deprivation on the metabolism of acellular bone in tilapia, Oreochromis niloticus. Comp. Biochem. Physiol. A: Physiol. 1992, 102:481-485.
42. Rona P., Takahashi D. Beitrag zur Frage nach dem Verhalten des Calciums im Serum. Biochem. Z. 1913, 49:370.
43. Barrett K., Brooks H., Boitano S., Barman S. Ganong's Review of Medical Physiology 2010, Appleton and Lange, Norwalk, Connecticut.
44. Greenwald I., Gross J. The effect of long continued administration of parathyroid extract upon the excretion of phosphorous and calcium. J. Biol. Chem. 1926, 68:325-333.
45. Kanis J.A., Yates A. Measuring serum calcium. Br. Med. J. 1985, 290:728-729.
46. Gosling P. Analytical reviews in clinical biochemistry: calcium measurement. Ann. Clin. Biochem. 1986, 23:146-156.
47. Roberston W., Marshall R. Calcium measurements in serum and plasma - total and ionized. Crit. Rev. Clin. Lab. Sci. 1979, 11:271-304.
48. Bushinsky D.A., Monk R.D. Calcium. Lancet 1998, 352:306-311.
49. Slomp J., van der Voort P.H.J., Gerritsen R.T., Berk J.A.M., Bakker A.J. Albumin-adjusted calcium is not suitable for diagnosis of hyper- and hypocalcemia in the critically ill. Crit. Care Med. 2003, 31:1389-1393.
50. Willis J. The determination of metals in blood serum by atomic absorption spectroscopy. I: Calcium. Spectrochim. Acta 1960, 16:259-272.
51. Schwarzenbach G. The complexones and their analytical application. Analyst 1955, 80:713-729.
52. Kessler G., Wolfman M. An automated procedure for the simultaneous determination of calcium and phosphorus. Clin. Chem. 1964, 10:686-703.
53. Bauer P.J. Affinity and stoichiometry of calcium binding by arsenazo III. Anal. Biochem. 1981, 110:61-72.
54. Michaylova V., Ilkova P. Photometric determination of micro amounts of calcium with arsenazo III. Anal. Chim. Acta 1971, 53:194-198.
55. Yofe J., Finkelstein R. Elimination of anionic interference in flame photometric determination of calcium in the presence of phosphate and sulphate. Anal. Chim. Acta 1958, 19:166-173.
56. Rhys J., David O., Basil I., F S.M., P W.C., B H.C., et al. Pseudohypercalcaemia in two patients with IgM paraproteinaemia. Ann. Clin. Biochem. 1997, 34:694-696.
57. Thode J., Juul-Jørgensen B., Bhatia H.M., Kærulf-Nielsen M., Bartels P.D., Fogh-Andersen N., et al. Comparison of serum total calcium, albumin-corrected total calcium, and ionized calcium in 1213 patients with suspected calcium disorders. Scand. J. Clin. Lab. Invest. 1989, 49:217-223.
58. Berth M., Delanghe J. Protein precipitation as a possible important pitfall in the clinical chemistry analysis of blood samples containing monoclonal immunoglobulins: 2. Case reports and a review of the literature. Acta Clin. Belg. 2004, 59:263-273.
59. Payne R.B., Little A.J., Williams R.B., Milner J.R. Interpretation of serum calcium in patients with abnormal serum proteins. Br. Med. J. 1973, 4:643-646.
60. Ballantyne J.S., Robinson J.W. Physiology of sharks, skates and rays. Encyclopedia of Fish Physiology: From Genome to Environment 2011, vol. 3:1807-1818. Academic Press, San Diego.
61. Rose G.A. Determination of the ionised and ultrafilterable calcium of normal human plasma. Clin. Chim. Acta 1957, 2:227-236.
62. Toribara T., Terepka A.R., Dewey P.A. The ultrafiltrable calcium of human serum. I. Ultrafiltration methods and normal values. J. Clin. Invest. 1957, 36:738.
63. Withers P.C. An exploration of salt and water balance in invertebrate and vertebrate animals. The Comparative Endocrinology of Calcium Regulation 1996, 17-42. The Journal of Endocrinology, Bristol. C. Dacke, J.A. Danks, I. Caple, G. Flik (Eds.).
64. Urist M.R. Calcium and other ions in blood and skeleton of Nicaraguan fresh-water shark. Science 1962, 137:984-986.
65. Ketola H.G. Requirement of atlantic salmon for dietary phosphorus. Trans. Am. Fish. Soc. 1975, 104:548-551.
66. Vielma J., Lall S.P. Phosphorus utilization by Atlantic salmon (Salmo salar) reared in freshwater is not influenced by higher dietary calcium intake. Aquaculture 1998, 160:117-128.
67. Guerreiro P. Calcium balance in sea bream (Sparus aurata): the effect of oestradiol-17beta. J. Endocrinol. 2002, 173:377-385.
68. Perry S.F., Shahsavarani A., Georgalis T., Bayaa M., Furimsky M., Thomas S.L.Y. Channels, pumps, and exchangers in the gill and kidney of freshwater fishes: their role in ionic and acid-base regulation. J. Exp. Zool. 2003, 300A:53-62.
69. Halstead Tarlo B.H. The origin of bone. Bone and Tooth Proceedings of the First European Bone and Tooth Symposium 1964, 3-15. Pergamon Press, Oxford. H.J.J. Blackwood (Ed.).
70. Simmons D.J. Calcium and skeletal tissue physiology in teleost fishes. Clin. Orthop. Relat. Res. 1971, 76:244-280.
71. Lall S.P., Bishop F.J. Studies on mineral and protein utilization by Atlantic salmon growth in sea water. Fisheries and Marine Service Technical Report No. 688 1977, 1-17. Department of Fisheries and Environment, Halifax.
72. Roy P.K., Witten P.E., Hall B.K., Lall S.P. Effects of dietary phosphorus on bone growth and mineralisation of vertebrae in haddock (Melanogrammus aeglefinus L.). Fish Physiol. Biochem. 2002, 27:35-48.
73. Witten P.E., Hall B.K. Seasonal changes in the lower jaw skeleton in male Atlantic salmon (Salmo salar L.): remodelling and regression of the kype after spawning. J. Anat. 2003, 203:435-450.
74. Lall S.P., Lewis-McCrea L.M. Role of nutrients in skeletal metabolism and pathology in fish - an overview. Aquaculture 2007, 267:3-19.
75. Carroll R.L. Vertebrate Paleontology and Evolution 1988, WH Freeman and Company, New York, 698 pp.
76. Hall B.K., Witten P.E. The origin and plasticity of skeletal tissues in vertebrate evolution and development. Major Transitions in Vertebrate Evolution 2007, Indiana University Press, Bloomington. J.S. Anderson, H.-D. Sues (Eds.).
77. Bakke A.M., Glover C., Koghdahl A. Feeding, digestion and absorption of nutrients. Fish Physiology. Volume 30. The multifinctional gut of fish 2011, 57-110. Academic Press, New York. M. Grosell, A.P. Farrell, C.J. Brauner (Eds.).
78. Stolte H., Galaske R.G., Eisenbach G.M., Lechene C., Schmidt-Nielsen B., Boylan J.W. Renal tubule ion transport and collecting duct function in the elasmobranch little skate, Raja erinacea. J. Exp. Zool. 1977, 199:403-410.
79. Bansal V. Serum inorganic phosphorus. Clinical Methods: The History, Physical, and Laboratory Examinations 1990, Butterworths, Boston, MA. H. Walker, W. Hall, J. Hurst (Eds.).
80. Kulaev I.S., Vagabov V., Kulakovskaya T. The Biochemistry of Inorganic Polyphosphates 2005, John Wiley & Sons.
81. Bjerrum N. Calciumorthophosphate I. Die Festen Calciumorthophosphate II. Komplexbildung in Lösung von Calcium- und Phosphate-Ionen. Mat. fys. Medd. K. Dan. Vidensk. Selsk. 1958, 31:79.
82. Chughtai A.R., Marshall R., Nancollas G.H. Complexes in calcium phosphate solutions. J. Phys. Chem. 1968, 72:208-211.
83. Habraken W.J.E.M., Tao J., Brylka L.J., Friedrich H., Bertinetti L., Schenk A.S., et al. Ion-association complexes unite classical and non-classical theories for the biomimetic nucleation of calcium phosphate. Nat. Commun. 2013, 4:1507.
84. Fiske C.H., Subbarow Y. The colorimetric determination of phosphorous. J. Biol. Chem. 1925, 66:375-400.
85. Berenblum I., Chain E. An improved method for the colorimetric determination of phosphate. Biochem. J. 1938, 32:295.
86. Robinson R., Roughan M.E., Wagstaff D. Measuring inorganic phosphate without using a reducing agent. Ann. Clin. Biochem. 1971, 8:168-170.
87. Chifflet S., Torriglia A., Chiesa R., Tolosa S. A method for the determination of inorganic phosphate in the presence of labile organic phosphate and high concentrations of protein: application to lens ATPases. Anal. Biochem. 1988, 168:1-4.
88. Ames B. Assay of Inorganic Phosphate, Total Phosphate and Phosphatase 1966, Academic Press, New York, NY.
89. Baginski E., Foa P., Zak B. Determination of phosphate: study of labile organic phosphate interference. Clin. Chim. Acta 1967, 15:155-158.
90. Drueckes P., Schinzel R., Palm D. Photometric microtiter assay of inorganic phosphate in the presence of acid-labile organic phosphates. Anal. Biochem. 1995, 230:173-177.
91. Lowry O.H., Lopez J.A. The determination of inorganic phosphate in the presence of labile phosphate esters. J. Biol. Chem. 1946, 162:421-428.
92. He Z., Honeycutt C.W. A modified molybdenum blue method for orthophosphate determination suitable for investigating enzymatic hydrolysis of organic phosphates. Commun. Soil Sci. Plant Anal. 2005, 36:1373-1383.
93. Røtset O. Determination of phosphate species in nutrient solutions and phosphorus in plant material as phosphovanadomolybdic acid by flow injection analysis. Anal. Chim. Acta 1985, 178:217-221.
94. Dalal B.I., Brigden M.L. Factitious biochemical measurements resulting from hematologic conditions. Am. J. Clin. Pathol. 2009, 131:195-204.
95. Larner A.J. Pseudohyperphosphatemia. Clin. Biochem. 1995, 28:391-393.
96. ® and associated equipment. Deep Sea Res. Oceanogr. Abstr. 1967, 381-389. (Elsevier).
97. Bowles S.A., Tait R.C., Jefferson S.G., Gilleece M.H., Haeney M.R. Characteristics of monoclonal immunoglobulins that interfere with serum inorganic phosphate measurement. Ann. Clin. Biochem. 1994, 31:249-254.
98. Smogorzewska A., Flood J.G., Long W.H., Dighe A.S. Paraprotein interference in automated chemistry analyzers. Clin. Chem. 2004, 50:1691-1693.
99. Sonnenblick M., Eylath U., Brisk R., Eldad C., Hershko C. Paraprotein interference with colorimetry of phosphate in serum of some patients with multiple myeloma. Clin. Chem. 1986, 32:1537-1539.
100. Anderson R.L., Davis S. An organic phosphorus assay which avoids the use of hazardous perchloric acid. Clin. Chim. Acta 1982, 121:111-116.
101. Mueller C.B., Hastings A.B. Glycolysis and phosphate fractions of red blood cells. J. Biol. Chem. 1951, 189:881-888.
102. Hunter R.J. Introduction to Modern Colloid Science 1993, Oxford University Press, Oxford, 360 pp.
103. Fleisch H. Role of nucleation and inhibition in calcification. Clin. Orthop. Relat. Res. 1964, 32:170-182.
104. Shelling D.H., Kramer B., Orent E.R. Studies upon calcification in vitro: III. Inorganic factors determining calcification. J. Biol. Chem. 1928, 77:157-170.
105. Walser M. Ion association. VI. Interactions between calcium magnesium, inorganic phosphate, citrate and protein in normal human plasma. J. Clin. Invest. 1961, 40:723-730.
106. Fleisch H., Neuman W.F. Mechanisms of calcification: role of collagen, polyphosphates, and phosphatase. Am. J. Physiol. 1961, 200:1296-1300.
107. Bedford J.J. The composition of the fluid compartments of two chondrichthyans, Callorhyncus millii and Squalus acanthias. Comp. Biochem. Physiol. A: Physiol. 1983, 76:75-80.
108. McLean F.C., Hastings A.B. The state of calcium in the fluids of the body I. The conditions affecting the ionization of calcium. J. Biol. Chem. 1935, 108:285-321.
109. Flik G., Verbost P.M., Wendelaar Bonga S.E. Calcium transport processes in fishes. Fish Physiology Volume 14 Cellular and Molecular Approaches to Fish Ionic Regulation 1995, 317-342. Academic Press Inc., New York. C.M. Wood, T.J. Shuttleworth (Eds.).
110. Quarles L.D. Endocrine functions of bone in mineral metabolism regulation. J. Clin. Invest. 2008, 118:3820-3828.
111. St-Arnaud R. The direct role of vitamin D on bone homeostasis. Arch. Biochem. Biophys. 2008, 473:225-230.
112. Bouillon R., Carmeliet G., Verlinden L., van Etten E., Verstuyf A., Luderer H.F., Vitamin D., et al. Vitamin D and human health: lessons from vitamin D receptor null mice. Endocr. Rev. 2008, 29:726-776.
113. Dusso A.S., Brown A.J., Slatopolsky E. Vitamin D. Am. J. Physiol. Renal Physiol. 2005, 289:F8-F28.
114. Rizzoli R., Fleisch H., Bonjour J.-P. Role of 1,25-dihydroxyvitamin D3 on intestinal phosphate absorption in rats with a normal vitamin D supply. J. Clin. Invest. 1977, 60:639-647.
115. Danks J.A., D'Souza D.G., Gunn H.J., Milley K.M., Richardson S.J. Evolution of the parathyroid hormone family and skeletal formation pathways. Gen. Comp. Endocrinol. 2011, 170:79-91.
116. Silva B.C., Bilezikian J.P. Parathyroid hormone: anabolic and catabolic actions on the skeleton. Curr. Opin. Pharmacol. 2015, 22:41-50.
117. Chambers T.J., Moore A. The sensitivity of isolated osteoclasts to morphological transformation by calcitonin. J. Clin. Endocr. Metab. 1983, 57:819-824.
118. Hoff A.O., Catala-Lehnen P., Thomas P.M., Priemel M., Rueger J.M., Nasonkin I., et al. Increased bone mass is an unexpected phenotype associated with deletion of the calcitonin gene. J. Clin. Invest. 2002, 110:1849-1857.
119. Liu S. Fibroblast Growth Factor 23 is a counter-regulatory phosphaturic hormone for vitamin D. J. Am. Soc. Nephrol. 2006, 17:1305-1315.
120. Bonewald L.F., Wacker M.J. FGF23 production by osteocytes. Pediatr. Nephrol. 2013, 28:563-568.
121. Nakatani T., Sarraj B., Ohnishi M., Densmore M.J., Taguchi T., Goetz R., et al. In vivo genetic evidence for klotho-dependent, fibroblast growth factor 23 (Fgf23)-mediated regulation of systemic phosphate homeostasis. FASEB J. 2008, 23:433-441.
122. Rowe P.S.N. Regulation of bone-renal mineral and energy metabolism: the PHEX, FGF23, DMP1, MEPE ASARM pathway. Crit. Rev. Eukaryot. Gene Expr. 2012, 22:61-86.
123. Imura A., Tsuji Y., Murata M., Maeda R., Kubota K., Iwano A., et al. Alpha-Klotho as a regulator of calcium homeostasis. Science 2007, 316:1615-1618.
124. Ben-Dov I.Z., Galitzer H., Lavi-Moshayoff V., Goetz R., Kuro-o M., Mohammadi M., et al. The parathyroid is a target organ for FGF23 in rats. J. Clin. Invest. 2007, 117:4003-4008.
125. Shimada T., Kakitani M., Yamazaki Y., Hasegawa H., Takeuchi Y., Fujita T., et al. Targeted ablation of Fgf23 demonstrates an essential physiological role of FGF23 in phosphate and vitamin D metabolism. J. Clin. Invest. 2004, 113:561-568.
126. Ichikawa S., Imel E.A., Kreiter M.L., Yu X., Mackenzie D.S., Sorenson A.H., et al. A homozygous missense mutation in human KLOTHO causes severe tumoral calcinosis. J. Clin. Invest. 2007, 117:2684-2691.
127. Pi M., Quarles L.D. Novel bone endocrine networks integrating mineral and energy metabolism. Curr. Osteoporos. Rep. 2013, 11:391-399.
128. Karsenty G., Ferron M. The contribution of bone to whole-organism physiology. Nature 2012, 481:314-320.
129. Guerreiro P.M., Renfro J.L., Power D.M., Canario A.V.M. The parathyroid hormone family of peptides: structure, tissue distribution, regulation, and potential functional roles in calcium and phosphate balance in fish. AJP: Regul. Integr. Comp. Physiol. 2007, 292:R679-R696.
130. Bouillon R., Suda T. Vitamin D: calcium and bone homeostasis during evolution. BoneKEy Rep. 2014, 3.
131. Pang P.K. Calcitonin and ultimobranchial glands in fishes. J. Exp. Zool. 1971, 178:89-99.
132. Abbink W., Flik G. Parathyroid hormone-related protein in teleost fish. Gen. Comp. Endocrinol. 2007, 152:243-251.
133. Danks J.A., Ho P.M.W., Notini A.J., Katsis F., Hoffmann P., Kemp B.E., et al. Identification of a parathyroid hormone in the fish Fugu rubripes. J. Bone Miner. Res. 2003, 18:1326-1331.
134. Gensure R.C., Ponugoti B., Gunes Y., Papasani M.R., Lanske B., Bastepe M., et al. Identification and characterization of two parathyroid hormone-like molecules in zebrafish. Endocrinology 2004, 145:1634-1639.
135. Liu Y., Ibrahim A.S., Tay B.-H., Richardson S.J., Bell J., Walker T.I., et al. Parathyroid hormone gene family in a cartilaginous fish, the elephant shark (Callorhinchus milii). J. Bone Miner. Res. 2010, 25:2613-2623.
136. Stahl B.J. Morphology and relationships of the Holocephali, with special reference to the venous system. Bull. Mus. Comp. Zool. 1966, 135:141-213.
137. Hurwitz S. Homeostatic control of plasma calcium concentration. Crit. Rev. Biochem. Mol. Biol. 1996, 31:41-100.
138. Glowacki J., Deftos L.J. Skeletal and mineral metabolism in sharks, rays, and fish. Endocrine Control of Bone and Calcium Metabolism 1984, 194-196. Elsevier, New York. D.V. Cohn, J.T. Potts, T. Fujita (Eds.).
139. Fleming A. High-throughput in vivo screening for bone anabolic compounds with zebrafish. J. Biomol. Screen. 2005, 10:823-831.
140. Aceto J., Nourizadeh-Lillabadi R., Marée R., Dardenne N., Jeanray N., Wehenkel L., et al. Zebrafish bone and general physiology are differently affected by hormones or changes in gravity. PLOS ONE 2015, 10(6):e0126928.
141. Suzuki N., Danks J.A., Maruyama Y., Ikegame M., Sasayama Y., Hattori A., et al. Parathyroid hormone 1 (1-34) acts on the scales and involves calcium metabolism in goldfish. Bone 2011, 48:1186-1193.
142. Ingleton P.M., Danks J.A. Distribution and functions of parathyroid hormone-related protein in vertebrate cells. Int. Rev. Cytol. 1996, 166:231.
143. Venkatesh B., Lee A.P., Ravi V., Maurya A.K., Lian M.M., Swann J.B., et al. Elephant shark genome provides unique insights into gnathostome evolution. Nature 2014, 505:174-179.
144. Ingleton P.M., Hazon N., Ho P.M.W., Martin T.J., Danks J.A. Immunodetection of parathyroid hormone-related protein in plasma and tissues of an elasmobranch (Scyliorhinus canicula). Gen. Comp. Endocrinol. 1995, 98:211-218.
145. Trivett M.K., Walker T.I., Macmillan D.L., Clement J.G., Martin T.J., Danks J.A. Parathyroid hormone-related protein (PTHrP) production sites in elasmobranchs. J. Anat. 2002, 201:41-52.
146. Philbrick W.M., Wysolmerski J.J., Galbraith S., Holt E., Orloff J.J., Yang K.H., et al. Defining the roles of parathyroid hormone-related protein in normal physiology. Physiol. Rev. 1996, 76:127-173.
147. Loveys L.S., Gelb D., Hurwitz S.R., Puzas J.E., Rosier R.N. Effects of parathyroid hormone-related peptide on chick growth-plate chondrocytes. J. Orthop. Res. 1993, 11:884-891.
148. Panda D., Goltzman D., Juppner H., Karaplis A.C. TIP39/parathyroid hormone type 2 receptor signaling is a potent inhibitor of chondrocyte proliferation and differentiation. Am. J. Physiol. Endocrinol. Metab. 2009, 297:E1125-E1136.
149. Martin T.J., Moseley J.M., Williams E.D. Parathyroid hormone-related protein: hormone and cytokine. J. Endocrinol. 1997, 154:S23-S37.
150. Rizzoli R., Caverzasio J., Chapuy M.C., Martin T.J., Bonjour J.P. Role of bone and kidney in parathyroid hormone-related peptide-induced hypercalcemia in rats. J. Bone Miner. Res. 1989, 4:759-765.
151. Zhou H., Leaver D.D., Moseley J.M., Kemp B., Ebeling P.R., Martin T.J. Actions of parathyroid hormone-related protein on the rat-kidney in vivo. J. Endocrinol. 1989, 122:229-235.
152. Fuentes J., Figueiredo J., Power D.M., Canario A.V.M. Parathyroid hormone-related protein regulates intestinal calcium transport in sea bream (Sparus auratus). AJP: Regul. Integr. Comp. Physiol. 2006, 291:R1499-R1506.
153. Trivett M.K., Walker T.I., Clement J.G., Ho P.M.W., Martin T.J., Danks J.A. Effects of water temperature and salinity on parathyroid hormone-related protein in the circulation and tissues of elasmobranchs. Comp. Biochem. Physiol. B: Biochem. Mol. Biol. 2001, 129:327-336.
154. Akino K., Ohtsuru A., Nakashima M., Ito M., Ting-Ting Y., Braiden V., et al. Distribution of the parathyroid hormone-related peptide and its receptor in the saccus vasculosus and choroid plexus in the red stingray (Dasyatis akajei: Elasmobranch). Cell. Mol. Neurobiol. 1998, 18:361-368.
155. Trivett M.K., Officer R.A., Clement J.G., Walker T.I., Joss J.M., Ingleton P.M., et al. Parathyroid hormone-related protein (PTHrP) in cartilaginous and bony fish tissues. J. Exp. Zool. 1999, 284:541-548.
156. Horst R.L., Reinhardt T.A. Vitamin D Metabolism 2005, 13-31. Elsevier Academic Press, London, UK. 2nd ed. D. Feldman, J.W. Pike, F.H. Glorieux (Eds.).
157. Glowacki J., Deftos L.J., Mayer E., Norman A.W. Chondrichthyes cannot resorb implanted bone and have calcium-regulationg hormones. Vitamin D, Chemical, Biochemical and Clinical Endocrinology of Calcium Metabolism 1982, 613-615. Walter de Gruyter & Co., Berlin; New York.
158. Kobayashi T., Takeuchi A., Okano T. An evolutionary aspect in vertebrates from the viewpoint of vitamin D3 metabolism. Vitamin D: Gene Regulation, Structure-Function Analysis and Clinical Application 1991, Walter de Gruyter & Co., Berlin. A.W. Norman, R. Bouillon, M. Thomasset (Eds.).
159. Lopez E., Mac Intyre I., Martelly E., Lallier F., Vidal B. Paradoxical effect of 1.25 dihydroxycholecalciferol on osteoblastic and osteoclastic activity in the skeleton of the eel Anguilla anguilla L. Calcif. Tissue Int. 1980, 32:83-87.
160. Mangos S., Amaral A.P., Faul C., Juppner H., Reiser J., Wolf M. Expression of fgf23 and klotho in developing embryonic tissues and adult kidney of the zebrafish, Danio rerio. Nephrol. Dial. Transplant. 2012, 27:4314-4322.
161. Yeung B.H.Y., Law A.Y.S., Wong C.K.C. Evolution and roles of stanniocalcin. Mol. Cell. Endocrinol. 2012, 349:272-280.
162. Wendelaar Bonga S.E., Pang P.K.T. Control of calcium regulating hormones in the vertebrates: parathyroid hormone, calcitonin, prolactin, and stanniocalcin. Int. Rev. Cytol. 1991, 128:139-213.
163. Wagner G.F., Guiraudon C.C., Milliken C., Copp D.H. Immunological and biological evidence for a stanniocalcin-like hormone in human kidney. Proc. Natl. Acad. Sci. U. S. A. 1995, 92:1871-1875.
164. Srivastav A.K., Srivastav S.K., Sasayama Y., Suzuki N. Corpuscles of Stannius-extract-induced rapid but transient hypocalcemia and hyperphosphatemia in stingray, Dasyatis akajei. Gen. Comp. Endocrinol. 1996, 104:37-40.
165. Srivastav A.K., Srivastav S.K., Sasayama Y., Suzuki N. Salmon calcitonin induced hypocalcemia and hyperphosphatemia in an elasmobranch, Dasyatis akajei. Gen. Comp. Endocrinol. 1998, 109:8-12.
166. Copp D.H., Cockcroft D.W., Kueh Y. Calcitonin from ultimobranchial glands of dogfish and chickens. Science 1967, 158:924-925.
167. Suzuki N., Takagi T., Sasayama Y., Kambegawa A. Effects of ultimobranchialectomy on the mineral balances of the plasma and bile in the stingray (Elasmobranchii). Zool. Sci. 1995, 12:239-242.
168. Louw G.N., Stahl P.D., Kenny A.D. Thyrocalcitonin studies on elasmobranch fish. Zool. Afr. 1969, 4.
169. Alluchon-Gerard M.J. Influence de la thyroïdectomie et du traitement par le propylthiouracile sur l'ultrastructure du cartilage de l'embryon et de la très jeune roussette (Scyllium canicula, Chondrichthyens). Arch. Anat. Microsc. Morph. Exp. 1982, 71:51-70.
170. Woodhead P.M.J. Effects of oestradiol and thryoxine upon the plasma calcium content of a shark, Scyliorhinus canicula. Gen. Comp. Endocrinol. 1969, 13:310-312.
171. Copp D.H. Calcitonin and parathyroid hormone. Annu. Rev. Pharmacol. 1969, 9:327-344.
172. Glowacki J., O'Sullivan J., Miller M., Wilkie D.W., Deftos L.J. Calcitonin produces a hypercalcemia in leopard sharks. Endocrinology 1985, 116:827-829.
173. Urist M.R. Avian parathyroid physiology: including a special comment on calcitonin. Am. Zool. 1967, 7:883-895.
174. Sasayama Y., Suzuki N., Oguro C., Takei Y., Takahashi A., Watanabe T.X., et al. Calcitonin of the stingray: comparison of the hypocalcemic activity with other calcitonins. Gen. Comp. Endocrinol. 1992, 86:269-274.
175. Hayslett J.P., Epstein M., Spector D., Myers J.D., Murdaugh H.V. Lack of effect of calcitonin on renal function in the elasmobranch, Squalus acanthias. Comp. Biochem. Physiol. 1972, 43A:223-226.
176. Chesnut C.H., Azria M., Silverman S., Engelhardt M., Olson M., Mindeholm L. Salmon calcitonin: a review of current and future therapeutic indications. Osteoporos. Int. 2007, 19:479-491.
177. Suzuki N., Sekiguchi T., Satake H., Kato K., Nishiyama Y., Takahashi H., et al. Cloning of two members of the calcitonin-family receptors from stingray, Dasyatis akajei: possible physiological roles of the calcitonin family in osmoregulation. Gene 2012, 499:326-331.
178. Summers A.P. Stiffening the stingray skeleton - an investigation of durophagy in myliobatid stingrays (Chondrichthyes, Batoidea, Myliobatidae). J. Morphol. 2000, 243:113-126.
179. Hoenig J.M., Walsh A.H. The occurrence of cartilage canals in shark vertebrae. Can. J. Zool. 1982, 60:483-485.
180. Dean M.N. Cartilaginous fish skeletal tissues. Encyclopedia of Fish Physiology: From Genome to Environment 2011, 428-433. Academic Press, San Diego. A.P. Farrell (Ed.).
181. Peignoux-Deville J., Lallier F., Vidal B. Evidence for the presence of osseous tissue in dogfish vertebrae. Cell Tissue Res. 1982, 222:605-614.
182. Bormuth H. Die trajektoriellen Strukturen im Knorpel der Haifische auf Grund von Untersuchungen im polarisierten Lichte. Cell Tissue Res. 1933, 17:767-797.
183. Bargmann W. Zur Kenntnis des Knorpelarchitekturen: Untersuchungen am Skeletsystem von Selachiern. Z. Zellforsch. Mikrosk. Anat. 1939, 29:405-424.
184. Mizuta S., Hwang J.-H., Yoshinaka R. Molecular species of collagen in pectoral fin cartilage of skate (Raja kenojei). Food Chem. 2003, 80:1-7.
185. Rama S., Chandrakasan G. Distribution of different molecular species of collagen in the vertebral cartilage of shark (Carcharius acutus). Connect. Tissue Res. 1984, 12:111-118.
186. Sivakumar P., Chandrakasan G. Occurrence of a novel collagen with three distinct chains in the cranial cartilage of the squid Sepia officinalis: comparison with shark cartilage collagen. Biochim. Biophys. Acta: Gen. Subj. 1998, 1381:161-169.
187. Eames B.F., Allen N., Young J., Kaplan A., Helms J.A., Schneider R.A. Skeletogenesis in the swell shark Cephaloscyllium ventriosum. J. Anat. 2007, 210:542-554.
188. Conrad G.W., Kelly P.T., von der Mark K., Edelhauser H.F. A comparative study of elasmobranch corneal and scleral collagens. Exp. Eye Res. 1981, 32:659-672.
189. Nudelman F., Pieterse K., George A., Bomans P.H.H., Friedrich H., Brylka L.J., et al. The role of collagen in bone apatite formation in the presence of hydroxyapatite nucleation inhibitors. Nat. Mater. 2010, 9:1004-1009.
190. Gower L.B. Biomimetic model systems for investigating the amorphous precursor pathway and its role in biomineralization. Chem. Rev. 2008, 108:4551-4627.
191. Schäfer C., Heiss A., Schwarz A., Westenfeld R., Ketteler M., Floege J., et al. The serum protein α(2)-Heremans-Schmid glycoprotein/fetuin-A is a systemically acting inhibitor of ectopic calcification. J. Clin. Invest. 2003, 112:357-366.
192. Price P.A., Toroian D., Chan W.S. Tissue-nonspecific alkaline phosphatase is required for the calcification of collagen in serum: a possible mechanism for biomineralization. J. Biol. Chem. 2009, 284:4594-4604.
193. Price P.A., Toroian D., Lim J.E. Mineralization by inhibitor exclusion: the calcification of collagen with fetuin. J. Biol. Chem. 2009, 284:17092-17101.
194. Hamlin N.J., Ong K.G., Price P.A. A serum factor that recalcifies demineralized bone is conserved in bony fish and sharks but is not found in invertebrates. Calcif. Tissue Int. 2006, 78:326-334.
195. Takagi M., Parmley R.T., Denys F.R., Yagasaki H., Toda Y. Ultrastructural cytochemistry of proteoglycans associated with calcification of shark cartilage. Anat. Rec. 1984, 208:149-158.
196. Michelacci Y.M., Horton D.S.P.Q. Proteoglycans from the cartilage of young hammerhead shark Sphyrna lewini. Comp. Biochem. Physiol. B: Biochem. Mol. Biol. 1989, 92:651-658.
197. Gelsleichter J.J., Musick J.A., van Veld P. Proteoglycans from the vertebral cartilage of the clearnose skate, Raja eglanteria - inhibition of hydroxyapatite formation. Fish Physiol. Biochem. 1995, 14:247-251.
198. Ortiz-Delgado J.B., Simes D.C., Viegas C.S.B., Schaff B.J., Sarasquete C., Cancela M.L. Cloning of matrix Gla protein in a marine cartilaginous fish, Prionace glauca: preferential protein accumulation in skeletal and vascular systems. Histochem. Cell Biol. 2005, 126:89-101.
199. Vortkamp A., Lee K., Lanske B., Segre G.V., Kronenberg H.M., Tabin C.J. Regulation of rate of cartilage differentiation by Indian hedgehog and PTH-related protein. Science 1996, 273:613-622.
200. Kawasaki K., Suzuki T., Weiss K.M. Genetic basis for the evolution of vertebrate mineralized tissue. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:11356-11361.
201. Kawasaki K., Buchanan A.V., Weiss K.M. Gene duplication and the evolution of vertebrate skeletal mineralization. Cells Tissues Organs 2007, 186:7-24.
202. Kawasaki K., Weiss K.M. Evolutionary genetics of vertebrate tissue mineralization: the origin and evolution of the secretory calcium-binding phosphoprotein family. J. Exp. Zool. B: Mol. Dev. Evol. 2006, 306B:295-316.
203. Kawasaki K., Amemiya C.T. SCPP genes in the coelacanth: tissue mineralization genes shared by sarcopterygians. J. Exp. Zool. B: Mol. Dev. Evol. 2013, 322:390-402.
204. Dean M.N., Socha J.J., Hall B.K., Summers A.P. Canaliculi in the tessellated skeleton of cartilaginous fishes. J. Appl. Ichthyol. 2010, 26:263-267.
205. Johanson Z., Kearsley A., den Blaauwen J., Newman M., Smith M.M. No bones about it: an enigmatic Devonian fossil reveals a new skeletal framework - a potential role of loss of gene regulation. Sem. Cell Dev. Biol. 2010, 21:414-423.
206. Quekett J. On the intimate structure of bone, as composing the skeleton, in the four great classes of animals, viz., mammals, birds, reptiles, and fishes, with some remarks on the great value of the knowledge of such structure in determining the affinities of minute fragments of organic remains. Trans. Microsc. Soc. Lond. 1849, 2:46-58.
207. Mahamid J., Sharir A., Addadi L., Weiner S. Amorphous calcium phosphate is a major component of the forming fin bones of zebrafish: indications for an amorphous precursor phase. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:12748-12753.
208. Mahamid J., Aichmayer B., Shimoni E., Ziblat R., Li C., Siegel S., et al. Mapping amorphous calcium phosphate transformation into crystalline mineral from the cell to the bone in zebrafish fin rays. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:6316-6321.
209. Mahamid J., Sharir A., Gur D., Zelzer E., Addadi L., Weiner S. Bone mineralization proceeds through intracellular calcium phosphate loaded vesicles: a cryo-electron microscopy study. J. Struct. Biol. 2011, 174:527-535.
210. Bennet M., Akiva A., Faivre D., Malkinson G., Yaniv K., Abdelilah-Seyfried S., et al. Simultaneous Raman microspectroscopy and fluorescence imaging of bone mineralization in living zebrafish larvae. Biophys. J. 2014, 106:L17-L19.
211. Bonewald L.F. The amazing osteocyte. J. Bone Miner. Res. 2011, 26:229-238.
212. Boyne P.J. Study of the chronologic development and eruption of teeth in elasmobranchs. J. Dent. Res. 1970, 49:556-560.
213. Peignoux-Deville J., Bordat C., Vidal B. Demonstration of bone resorbing cells in elasmobranchs: comparison with osteoclasts. Tissue Cell 1989, 21:925-933.
214. Officer R.A., Clement J.G., Rowler D.K. Vertebral deformities in a school shark, Galeorhinus galeus: circumstantial evidence for endoskeletal resorption. J. Fish Biol. 1995, 46:85-98.
215. Glowacki J., Cox K.A., O'Sullivan J., Wilkie D., Deftos L.J. Osteoclasts can be induced in fish having an acellular bony skeleton. Proc. Natl. Acad. Sci. U. S. A. 1986, 83:4104-4107.
216. Clement J.G. The Development, Structure and Chemistry of Elasmobranch Skeletal Tissues 1986, (Dissertation), University of London.
217. Hoenig J.M., Walsh A.H. Skeletal lesions and deformities in large sharks. J. Wildl. Dis. 1983, 19:27-33.
218. Porter M.E., Beltran J.L., Koob T.J., Summers A.P. Material properties and biochemical composition of mineralized vertebral cartilage in seven elasmobranch species (Chondrichthyes). J. Exp. Biol. 2006, 209:2920-2928.
219. Huber D., Neveu D.E., Stinson C.M., Anderson P.A., Berzins I.K. Mechanical properties of sand tiger shark Carcharias taurus vertebrae in relation to spinal deformity. J. Exp. Biol. 2013, 216:4256-4263.
220. Dean M.N., Huber D.R., Nance H.A. Functional morphology of jaw trabeculation in the lesser electric ray Narcine brasiliensis, with comments on the evolution of structural support in the Batoidea. J. Morphol. 2006, 267:1137-1146.
221. Dingerkus G., Séret B., Guilbert E. Multiple prismatic calcium phosphate layers in the jaws of present-day sharks (Chondrichthyes; Selachii). Experientia 1991, 47:38-40.
222. Claeson K.M. The synarcual cartilage of batoids with emphasis on the synarcual of Rajidae. J. Morphol. 2011, 272:1444-1463.
223. Johanson Z., Trinajstic K., Carr R., Ritchie A. Evolution and development of the synarcual in early vertebrates. Zoomorphology 2012, 132:95-110.
224. Jollie M. Some developmental aspects of the head skeleton of the 35-37mm Squalus acanthias foetus. J. Morphol. 1971, 133:17-40.
225. Summers A.P., Ketcham R.A., Rowe T. Structure and function of the horn shark (Heterodontus francisci) cranium through ontogeny: development of a hard prey specialist. J. Morphol. 2004, 260:1-12.
226. Schaefer J.T., Summers A.P. Batoid wing skeletal structure: novel morphologies, mechanical implications, and phylogenetic patterns. J. Morphol. 2005, 264:298-313.
227. Fiaz A.W., Léon-Kloosterziel K.M., Gort G., Schulte-Merker S., van Leeuwen J.L., Kranenbarg S. Swim-training changes the spatio-temporal dynamics of skeletogenesis in zebrafish larvae (Danio rerio). PLoS ONE 2012, 7:e34072-e34113.
228. de Beer G.R. The development of the vertebrate skull 1937, Oxford University Press, New York, 760 pp.