Assessing the ability of zebrafish scales to contribute to the short-term homeostatic regulation of [Ca2+] in the extracellular fluid during calcemic challenges

Ablain J, Zon LI (2013) Of fish and men: using zebrafish to fight human diseases. Trends Cell Biol 23:584–586 Andreasan P (1985) Free and total calcium concentrations in the blood of rainbow trout, Salmo gairdneri, during ‘stress’ conditions. J Exp Biol 118:111–120 Bakkers J (2011) Zebrafish as a model to study cardiac development and human cardiac disease. Cardiovasc Res 91:279–288 Berridge MJ, Bootman MD, Roderick HL (2003) Calcium signalling: dynamics, homeostasis and remodelling. Nat Rev Mol Cell Biol 4:517–529 Blaine J, Chonchol M, Levi M (2014) Renal control of calcium, phosphate, and magnesium homeostasis. Clin J Am Soc Nephrol 10:1257–1272 Breitwieser GE (2008) Extracellular calcium as an integrator of tissue function. Int J Biochem Cell Biol 40:1467–1480 Bronner F (1992) Bone and calcium homeostasis. Neurotoxicology 13:775–782 Burns CG, MacRae CA (2006) Purification of hearts from zebrafish embryos. Biotechniques 40:274 (276, 278) Catté M, Dussap C-G, Gros J-B (1995) A physical chemical UNIFAC model for aqueous solutions of sugars. Fluid Phase Equilib 105:1–25 Craig TA, Sommer S, Sussman CR, Grande JP, Kumar R (2008) Expression and regulation of the vitamin D receptor in the zebrafish, Danio rerio. J Bone Mineral Res 23:1486–1496 De Luisa A, Hofer AM (2003) Evidence that Ca2+ cycling by the plasma membrane Ca2+-ATPase increases the ‘excitability’ of the extracellular Ca2+-sensing receptor. J Cell Sci 116:1527–1538 De Vrieze E, Metz JR, Von den Hoff JW, Flik G (2010) ALP, TRAcP, and cathepsin K in elasmoid scales; a role in mineral metabolism? J Appl Ichthyol 26:210–213 De Vrieze E, Sharif F, Metz JR, Flik G, Richardson MK (2011) Matrix metalloproteinases in osteoclast of ontogenetic and regenerating zebrafish scales. Bone 48:704–722 Dedic C, Hung JT, Shipley AM, Maeda A, Gardella T, Miller AL, Divieti Pajevic P, Kunkel J, Rubinacci A (2018) Calcium fluxes at the bone-plasma interface: acute effects of parathyroid hormone (PTH) and targeted deletion of PTH/PTH-related peptide (PTHrP) receptor in the osteocyte. Bone 116:135–143 Dehal P, Boore JL (2005) Two rounds of whole genome duplication in the ancestral vertebrate. PLoS Biol 3(10):e314. https://doi.org/10.1371/journal.pbio.0030314 Donoghue PC, Sansom IJ (2002) Origin and early evolution of vertebrate skeletonization. Microsc Res Tech 59:352–372 Dooley K, Zon LI (2000) Zebrafish: a model system for the study of human disease. Curr Opin Gen Devel 10:252–256 Elliott DG (2000) Integumenatry system. In: Ostrander GK (ed) Handbook of experimental animals: the laboratory fish. Academic Press, Cambridge, pp 271–306 Flik G, Verbost PM (1993) Calcium transport in fish gills and intestine. J Exp Biol 184:17–29 Flik G, Fenwick JC, Kolar Z, Mayer-Gostan N, Wendelaar Bonga SE (1986) Effects of low ambient calcium levels on wholebody Ca2+ flux rates and internal calcium pools in the freshwater teleost, Oreochromis mossambicus. J Exp Biol 120:249–264 Flik G, Verbost PM, Wendelaar Bonga SE (1995) Calcium transport processes in fishes. Fish Physiol 14:317–342 Gilabert JA (2012) Cytoplasmic calcium buffering. In: Islam M (ed) Calcium signaling. Advances in experimental medicine and biology. Springer, Dordrecht, pp 483–498 Goldberg RN (1981) Evaluated activity and osmotic coefficients for aqueous solutions: thirty-six uni-bivalent electrolytes. J Phys Chem Ref Data 10:671–764 Goldberg RN, Nuttall RL (1978) Evaluated activity and osmotic coefficients for aqueous solutions: the alkaline earth metal halides. J Phys Chem Ref Data 7:263–310 Goldsmith JR, Jobin C (2012) Think small: zebrafish as a model system of human pathology. J Biomed Biotech 2012:817341. https://doi.org/10.1155/2012/817341 Golpour A, Pšenička M, Niksirat H (2016) Subcellular localizations of calcium deposits during zebrafish (Danio rerio) oogenesis. Micron 80:6–13 Greenwood MP, Flik G, Wagner GF, Balment RJ (2009) The corpuscles of Stannius, calcium-sensing receptor, and stanniocalcin: responses to calcimimetics and physiological challenges. Endocrinology 150:3002–3010 Guerrerio PM, Fuentes J, Canário AVM, Power DM (2002) Calcium balance in sea bream (Sparus aurata): the effect of oestradiol-17β. J Endocrinol 173:377–385 Guh YJ, Lin CH, Hwang PP (2015) Osmoregulation in zebrafish: ion transport mechanisms and functional regulation. Exp Clin Sci J 14:627–659 Hamer WJ, Wu Y-C (1972) Osmotic coefficients and mean activity coefficients of uni-univalent electrolytes in water at 25 °C. J Phys Chem Ref Data 1:1047–1100 Herbert ER, Boon P, Burgin AJ, Neubauer SC, Franklin RB, Ardón M, Hopfensperger KN, Lamers LPM, Gell P (2015) A global perspective on wetland salinization: ecological consequences of a growing threat to freshwater wetlands. Ecosphere 6(10):1–43. https://doi.org/10.1890/ES14-00534.1 Hirasawa T, Karatani S (2015) Evolution of the vertebrate skeleton: morphology, embryology, and development. Zool Lett 1:2. https://doi.org/10.1186/s40851-014-0007-7 Hofer AM (2005) Another dimension to calcium signaling: a look at extracellular calcium. J Cell Sci 118:855–862 Hohman EE, Hodges JK, Wastney ME, Lacheik PJ, Han CY, Dwyer D, Peacock M, Kostenuik PJ, Weaver CM (2018) Serum calcium concentration is maintained when bone resorption is suppressed by osteoprotegerin in young growing male rats. Bone 116:162–170 Hwang PP, Chou MY (2013) Zebrafish as an animal model to study ion homeostasis. Pflugers Arch Eur J Physiol 465:1233–1247 Hwang PP, Lee TH, Lin LY (2011) Ion regulation in fish gills: recent progress in the cellular and molecular mechanisms. Am J Physiol Regul Integr Comp Physiol 301:R28–R47 Ingham PW (2009) The power of zebrafish for disease analysis. Human Mol Genet 18:R107–R112 Iwasaki M, Kuroda J, Kawakami K, Wada H (2018) Epidermal regulation of bone morphogenesis through the development and regeneration of osteoblasts in the zebrafish scale. Dev Biol 437:105–119 Kacem A, Baglinière JL, Meunier FJ (2013) Resorption of scales in Atlantic salmon (Salmo salar) during its anadromous migration: a quantitative study. Cybium: Revue Internationale d’Ichtyologie 37:199–206 Kalueff AV, Stewart AM, Gerlai R (2014) Zebrafish as an emerging model for studying complex brain disorders. Trends Pharmacol Sci 35:63–75 Kinkel MD, Eames SC, Philipson LH, Prince VE (2010) Intraperitoneal injection into adult zebrafish. J Vis Exp. https://doi.org/10.3791/2126 Kitamura K, Takahira K, Inari M, Satoh Y, Hayakawa K, Tabuchi Y, Ogai K, Nishiuchi T, Kondo T, Mikuni-Takagaki Y, Chan W, Hattori A, Suzuki N (2013) Zebrafish scales respond differently to in vitro dynamic and static acceleration: analysis of interaction between osteoblasts and osteoclasts. Comp Biochem Physiol Part A Mol Integr Physiol 166:74–80 Kühtreiber WM, Jaffe LF (1990) Detection of extracellular calcium gradients with a calcium-specific vibrating electrode. J Cell Biol 110:1565–1573 Kunkel JG, Cordeiro S, Xu Y, Shipley AM, Feijó JA (2006) Use of non-invasive ion-selective microelectrode for the study of plant development. In: Volkov AG (ed) Plant electrophysiology. Springer, Berlin, pp 109–137 Kwong RW, Kumai Y, Perry SF (2016) Neuroendocrine control of ionic balance in zebrafish. Gen Comp Endocrinol 234:40–46 Laizé V, Gavaia PJ, Cancela ML (2014) Fish: a suitable system to model human bone disorders and discover drugs with osteogenic or osteotoxic activities. Drug Discov Today Dis Mod 13:29–37 Lee RTH, Thiery JP, Carney TJ (2013) Dermal fin rays and scales derive from mesoderm, not neural crest. Curr Biol 23:R336–R337 Lin CH, Hwang PP (2016) The control of calcium metabolism in zebrafish (Danio rerio). Int J Mol Sci. https://doi.org/10.3390/ijms17111738 Lin C-Y, Chiang C-Y, Tsai HJ (2016) Zebrafish and medaka: New model organisms for modern biomedical research. J Biomed Sci 23:19. https://doi.org/10.1186/s12929-016-0236-5 Lu W, Jin Y, Xu J, Greenwood MP, Balment RJ (2017) Molecular characterisation and expression of parathyroid hormone-related protein in the caudal neurosecretory system of the euryhaline flounder, Platichthys flesus. Gen Comp Endocrinol 249:24–31 Majore I, Jager V, Rohde M (2007) Influence of extracellular calcium concentration on the bone matrix synthesis and mineralization in cultures of human primary osteoprogenitor cells. J Stem Cell Regen Med 2:125–126 Marenzana M, Shipley AM, Squitiero P, Kunkel JG, Rubinacci A (2005) Bone as an ion exchange organ: evidence for instantaneous cell-dependent calcium efflux from bone not due to resorption. Bone 37:545–554 Mariotti M, Carnovali M, Banfi G (2015) Danio rerio: the Janus of the bone from embryo to scale. Clin Cases Min Bone Metab 12:188–194 Metz JR, De Vrieze E, Lock EJ, Schulten IE, Flik G (2012) Elasmoid scales of fishes as a model in biomedical bone research. J Appl Ichthyol 28:382–387 Metz JR, Leeuwis RHJ, Zethof J, Flik G (2014) Zebrafish (Danio rerio) in calcium-poor water mobilize calcium and phosphorus from scales. J Appl Ichthyol 30:671–677 Meunier FJ (1984) Spatial organization and mineralization of the basal plate of the elasmoid scales in osteichthyans. Am Zool 24:953–964 Mongera A, Nüsslein-Volhard C (2013) Scales of fish arise from mesoderm. Curr Biol 23:338–339 Moysés-Neto M, Guimarães FM, Ayoub FH, Vieira-Neto OM, Costa JAC, Dantas M (2006) Acute renal failure and hypercalcemia. Ren Fail 28:153–159 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 Biochem Physiol A Physiol 57:197–202 Mundy GR, Guise TA (1999) Hormonal control of calcium homeostasis. Clin Chem 45:1347–1352 Nakamura T, Gehrke AR, Lemberg J, Szymaszek J, Shubin NH (2016) Digits and fin rays share common developmental histories. Nature 537:225–228 Nakari T, Erkomaa K (2003) Effects of phytosterols on zebrafish reproduction in multigeneration test. Environ Pollut 123:267–273 Ogawa N, Ura K, Takagi Y (2010) Scale calcification in the goldfish in vitro: histological and quantitative analysis. Fish Sci 76:189–198 Okuda M, Ogawa N, Takeguchi M, Hashimoto A, Tagaya M, Chen S, Hanagata N, Ikoma T (2011) Minerals and aligned collagen fibrils in tilapia fish scales: structural analysis using dark-field and energy-filtered transmission electron microscopy and electron tomography. Microsc Microanal 17:788–798 Pan C (1977) Activity and osmotic coefficients in dilute aqueous solutions of bi-univalent electrolytes at 25 °C. J Chem Eng Data 22:234–237 Pasqualetti S, Banfi G, Mariotti M (2012a) Osteoblast and osteoclast behavior in zebrafish cultured scales. Cell Tissue Res 350:69–75 Pasqualetti S, Banfi G, Mariotti M (2012b) The zebrafish scale as a model to study the bone mineralization process. J Mol Histol 43:589–595 Persson P, Sundell K, Björnsson BT, Lundqvist H (1998) Calcium metabolism and osmoregulation during sexual maturation of river running Atlantic salmon. J Fish Biol 52:334–349 Persson P, Björnsson BT, Takagi Y (1999) Characterisation of morphology and physiological actions of scale osteoclasts in the rainbow trout. J Fish Biol 54:669–684 Persson P, Shrimpton JM, McCormick SD, Björnsson BT (2000) The presence of high-affinity, low capacity estradiol-17β binding in rainbow trout scale indicates a possible endocrine route for the regulation of scale resorption. Gen Comp Endocrinol 120:35–43 Pitzer KS, Peiper JC (1979) Activity coefficient of aqueous NaHCO3. J Phys Chem 84:2396–2398 Rard JA, Miller DG (1981) Isopiestic determination of the osmotic coefficients of aqueous Na2SO4, MgSO4, and Na2SO4–MgSO4 at 25 °C. J Chem Eng Data 26:33–38 Reid B, Zhao M (2011) Ion-selective self-referencing probes for measuring specific ion flux. Commun Integr Biol 4:524–527 Reuter M (2012) DotCount software. Cambridge https://reuter.mit.edu/software/dotcount/ Rotllant J, Redrullo B, Guerreiro PM, Fernandes H, Canario AMV, Power DM (2005) Calcium mobilization from fish scales in mediated by parathyroid hormone related protein via the parathyroid hormone receptor type 1 receptor. Regul Peptides 132:33–40 Rubin DA, Jüppner H (1999) Zebrafish express the common parathyroid hormone/parathyroid hormone-related peptide receptor (PTH1R) and a novel receptor (PTH3R) that is preferentially activated by mammalian and fugufish parathyroid hormone-related peptide. J Biol Chem 274:28185–28190 Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675 Schönbörner AA, Boivin G, Baud CV (1979) The mineralization process in teleost fish scales. Cell Tissue Res 202:203–212 Sharif F, de Bakker MAG, Richardson MK (2014) Osteoclast-like cells in early zebrafish embryos. Cell J 16:211–224 Shi WC, Fang ZB, Li L, Luo LF (2015) Using zebrafish as the model organism to understand organ regeneration. Sci China Life Sci 58:343–351 Shimada A, Kawanishi T, Kaneko T, Yoshihara H, Yano T, Inohaya K, Kinoshita M, Kamei Y, Yamura K, Takeda H (2013) Trunk exoskeleton in teleosts is mesodermal in origin. Nat Commun. https://doi.org/10.1038/ncomms2643 Shipley AM (2009) Scanning microelectrode techniques (SIET/SPET) system manual. Applicable Electronics Inc, Forestdale Sionkowska A, Kozlowska J (2013) Fish scales as a biocomposite of collagen and calcium salts. Key Eng Mater 587:185–190 Sire JY, Akimenko MA (2004) Scale development in fish: A review, with description of sonic hedgehog (shh) expression in the zebrafish (Danio rerio). Int J Dev Biol 48:233–247 Sire JY, Huysseune A (2003) Formation of dermal skeleton and dental tissues in fish: a comparative and evolutionary approach. Biol Rev Camb Philos Soc 78:219–249 Sire JY, Allizard F, Babiar O, Bourguignon J, Quilhac S (1997) Scale development in zebrafish (Danio rerio). J Anat 190:545–561 Sire JY, Girondot M, Babiar O (2000) Marking zebrafish, Danio rerio (cyprinidae), using scale regeneration. J Exp Zool 286:297–304 Smith PJ, Hammar K, Porterfield DM, Sanger RH, Trimarchi JR (1999) Self-referencing, non-invasive, ion selective electrode for single cell detection of trans-plasma membrane calcium flux. Micro Res Tech 46:398–417 Sugimoto T, Kanatani M, Kano J, Kaji H, Tsukamoto T, Yamaguchi T, Fukase M, Chihara K (1993) Effects of high calcium concentration on the functions and interactions of osteoblastic cells and monocytes and on the formation of osteoclast-like cells. J Bone Miner Res 8:1445–1452 Suzuki N, Danks JA, Maruyama Y, Ikegame M, Sasayama Y, Hattori A, Nakamura M, Tabata MJ, Yamamoto T, Furuya R, Saijoh K, Mishima H, Srivastav AK, Furusawa Y, Kondo T, Tabuchi Y, Takasaki I, Chowdhury VS, Hayakawa K, Martin TJ (2011) Parathyroid hormone 1(1–34) acts on the scales and involves calcium metabolism in goldfish. Bone 48:1186–1193 Suzuki N, Hanmoto T, Yano S, Furusawa Y, Ikegame M, Tabuchi Y, Kondo T, Kitamura K, Endo M, Yamamoto T, Sekiguchi T, Urata M, Mikuni-Takagaki Y, Hattori A (2016a) Low-intensity pulsated ultrasound induces apoptosis is osteoclasts: Fish scales are suitable model for the analysis of bone metabolism. Comp Biochem Physiol A Mol Integr Physiol 195:26–31 Suzuki N, Kitamura K, Hattori A (2016b) Fish scale is a suitable model for analyzing determinants of skeletal fragility in type-2 diabetes. Endocrine 54:575–577 Takagi Y, Hirano T, Yamada J (1989) Scale regeneration of tilapia (Oreochromis niloticus) under various ambient and dietary calcium concentrations. Comp Biochem Physiol A Physiol 92:605–608 Tas CA (2014) The use of physiological solutions or media in calcium phosphate synthesis and processing. Acta Biomater 10:1771–1792 Unal M, Creecy A, Nyman JS (2018) The role of matrix composition in the mechanical behavior of bone. Curr Osterporos Rep 16:205–215 Viera FA, Gregorio SF, Ferraresso S, Thorne MAS, Costa R, Milan M, Bargelloni L, Clark MS, Canario AVM, Power DM (2011) Skin healing and scale regeneration in fed and unfed sea bream, Sparus auratus. BMC Genomics 12:490. https://doi.org/10.1186/1471-2164-12-490 Wang X, Chen H, Ouyang Y, Liu J, Zhao G, Bao W, Yan M (2014) Dietary calcium intake and mortality risk from cardiovascular disease and all causes: a meta-analysis of prospective cohort studies. BMC Med 12:158. https://doi.org/10.1186/s12916-014-0158-6 Waterman RE (1970) Fine structure of scale development in the teleost, Brachydanio rerio. Anat Rec 168:361–379 Weiner S, Wagner HD (1998) The material bone: structure–mechanical function relations. Ann Rev Mat Sci 28:271–298 Welldon KJ, Findlay DM, Evdokiou A, Ormsby RT, Atkins GJ (2013) Calcium induces pro-anabolic effects on human primary osteoblasts associated with acquisition of mature osteocyte markers. Mol Cell Endocrinol 376:85–92 Wendelaar Bonga SE, Flik G (1993) Calcium regulation in fish. In: Lahlou B, Vitiello P (eds) Aquaculture: fundamental and applied research. American Geophysical Union, New York, pp 47–59 Westerfield M (2000) The Zebrafish book: a guide for the laboratory use of zebrafish (Danio rerio). University of Oregon Press, Corvallis Yoshikubo H, Suzuki N, Takemura K, Hoso M, Yashima S, Iwamuro S, Takagi Y, Tabata MJ, Hattori A (2005) Osteoblastic activity and estrogenic response in the regenerating scale of goldfish, a good model for osteogenesis. Life Sci 76:2699–2709