Skip to main content

Advertisement

SpringerLink
Log in

Sodium fluoride influences calcium metabolism resulting from the suppression of osteoclasts in the scales of nibbler fish Girella punctata

  • Original Article
  • Biology
  • Published:
Fisheries Science Aims and scope Submit manuscript

An Erratum to this article was published on 23 May 2017

Abstract

The influence of sodium fluoride (NaF) on calcium metabolism was examined in nibbler fish (marine teleosts). Two days after the administration of NaF (5 μg/g of body weight) (around 10−4 M in fish), we showed that plasma calcium levels significantly decreased in NaF-treated nibbler fish. In addition, we detected fluoride in the treated scales by use of a scanning electron microscope with an energy-dispersive X-ray microanalysis, indicating that NaF directly affects their scales. Therefore, the influence of NaF on osteoblasts and osteoclasts in the scales was examined. In the scales of NaF-injected nibbler fish, tartrate-resistant acid phosphatase (TRAP) (osteoclastic marker enzyme) decreased, although alkaline phosphatase (osteoblastic marker enzyme) was activated. To confirm the effect of NaF on osteoclasts, furthermore, the mRNA expressions of osteoclastic markers (matrix metalloproteinase-9 and TRAP) were decreased significantly 2 days after incubation. In barred knifejaws, plasma calcium levels decreased as they did in nibbler fish. Therefore, NaF functions in both osteoblasts and osteoclasts and then influences calcium metabolism in marine fish. In the marine environment, high levels of fluoride (1.2–1.5 mg F−/l) (around 10−5–10−4 M) are present in seawater. It is probable that teleosts living in seawater efficiently use fluoride to regulate their blood calcium levels.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Mandinic Z, Curcic M, Antonijevic B, Carevic M, Mandic J, Djukic-Cosic D, Lekic CP (2010) Fluoride in drinking water and dental fluorosis. Sci Total Environ 408:3507–3512

    Article  CAS  PubMed  Google Scholar 

  2. Gbadebo AM (2012) Groundwater fluoride and dental fluorosis in southwestern Nigeria. Environ Geochem Health 34:597–604

    Article  CAS  PubMed  Google Scholar 

  3. Camargo JA (2003) Fluoride toxicity to aquatic organisms: a review. Chemosphere 50:251–264

    Article  PubMed  Google Scholar 

  4. Adelung D, Buchholz F, Culik B, Keck A (1987) Fluoride in tissues of krill Euphausia superba Dana and Meganyctiphanes norvegica M. Sars in relation to the moult cycle. Polar Biol 7:43–50

    Article  CAS  Google Scholar 

  5. Yoshitomi B, Nagano I (2012) Effect of dietary fluoride derived from Antarctic krill (Euphausia superba) meal on growth of yellowtail (Seriola quinqueradiata). Chemosphere 86:891–897

    Article  CAS  PubMed  Google Scholar 

  6. Bereiter-Hahn J, Zylberberg L (1993) Regeneration of teleost fish scale. Comp Biochem Physiol Part A 105:625–641

    Article  Google Scholar 

  7. Suzuki N, Suzuki T, Kurokawa T (2000) Suppression of osteoclastic activities by calcitonin in the scales of goldfish (freshwater teleost) and nibbler fish (seawater teleost). Peptides 21:115–124

    Article  CAS  PubMed  Google Scholar 

  8. 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 of osteogenesis. Life Sci 76:2699–2709

    Article  CAS  PubMed  Google Scholar 

  9. Suzuki N, Kitamura K, Nemoto T, Shimizu N, Wada S, Kondo T, Tabata MJ, Sodeyama F, Ijiri K, Hattori A (2007) Effect of vibration on osteoblastic and osteoclastic activities: analysis of bone metabolism using goldfish scale as a model for bone. Adv Space Res 40:1711–1721

    Article  CAS  Google Scholar 

  10. Ohira Y, Shimizu M, Ura K, Takagi Y (2007) Scale regeneration and calcification in goldfish Carassius auratus: quantitative and morphological processes. Fish Sci 73:46–54

    Article  CAS  Google Scholar 

  11. Suzuki N, Somei M, Seki A, Reiter RJ, Hattori A (2008) Novel bromomelatonin derivatives as potentially effective drugs to treat bone diseases. J Pineal Res 45:229–234

    Article  CAS  PubMed  Google Scholar 

  12. Yamada J (1961) Studies on the structure and growth of the scales in the goldfish. Mem Fac Fish Hokkaido Univ 9:181–226

    Google Scholar 

  13. Berg A (1968) Studies on the metabolism of calcium and strontium in freshwater fish I: relative contribution of direct and intestinal absorption. Mem Ist Ital Idrobiol 23:161–196

    Google Scholar 

  14. 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 Part A 57:197–202

    Article  CAS  Google Scholar 

  15. Suzuki N, Hattori A (2002) Melatonin suppresses osteoclastic and osteoblastic activities in the scales of goldfish. J Pineal Res 33:253–258

    Article  CAS  PubMed  Google Scholar 

  16. 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

    Article  CAS  PubMed  Google Scholar 

  17. Sato M, Hanmoto T, Yachiguchi K, Tabuchi Y, Kondo T, Endo M, Kitani Y, Sekiguchi T, Urata M, Hai TN, Srivastav AK, Mishima H, Hattori A, Suzuki N (2016) Sodium fluoride induces hypercalcemia resulting from the upregulation of both osteoblastic and osteoclastic activities in goldfish, Carassius auratus. Comp Biochem Physiol Part C 189:54–60

    CAS  Google Scholar 

  18. Suzuki N, Yamamoto M, Watanabe K, Kambegawa A, Hattori A (2004) Both mercury and cadmium directly influence calcium homeostasis resulting from the suppression of scale bone cells: the scale is a good model for the evaluation of heavy metals in bone metabolism. J Bone Miner Metab 22:439–446

    CAS  PubMed  Google Scholar 

  19. Suzuki N, Yamamoto K, Sasayama Y, Suzuki T, Kurokawa T, Kambegawa A, Srivastav AK, Hayashi S, Kikuyama S (2004) Possible direct induction by estrogen of calcitonin secretion from ultimobranchial cells in the goldfish. Gen Comp Endocrinol 138:121–127

    Article  CAS  PubMed  Google Scholar 

  20. Omori K, Wada S, Maruyama Y, Hattori A, Kitamura K, Sato Y, Nara M, Funahashi H, Yachiguchi K, Hayakawa K, Endo M, Kusakari R, Yano S, Srivastav AK, Kusui T, Ejiri S, Chen W, Tabuchi Y, Furusawa Y, Kondo T, Sasayama Y, Nishiuchi T, Nakano M, Sakamoto T, Suzuki N (2012) Prostaglandin E2 increases both osteoblastic and osteoclastic activities in the scales of goldfish and participates in the calcium metabolism in goldfish. Zool Sci 29:499–504

    Article  CAS  PubMed  Google Scholar 

  21. Yachiguchi K, Matsumoto N, Haga Y, Suzuki M, Matsumura C, Tsurukawa M, Okuno T, Nakano T, Kawabe K, Kitamura K, Toriba A, Hayakawa K, Chowdhury VS, Endo M, Chiba A, Sekiguchi T, Nakano M, Tabuchi Y, Kondo T, Wada S, Mishima H, Hattori A, Suzuki N (2014) Polychlorinated biphenyl (118) activates osteoclasts and induces bone resorption in goldfish. Env Sci Poll Res 21:6365–6372

    Article  CAS  Google Scholar 

  22. Mishima H, Sakae T, Kozawa Y (1995) Scanning electron microscopy and energy dispersive spectroscopy analysis of calciotraumatic lines in rat labial dentin after acute exposure to strontium chloride. Scanning Microsc 9:797–803

    CAS  PubMed  Google Scholar 

  23. Vaes G (1988) Cellular biology and biochemical mechanism of bone resorption. Clin Orthop 231:239–271

    CAS  Google Scholar 

  24. Dimai HP, Linkhart TA, Linkhart SG, Donahue LR, Beamer WG, Rosen CJ, Farley JR, Baylink DJ (1998) Alkaline phosphatase levels and osteoprogenitor cell numbers suggest bone formation may contribute to peak bone density differences between two inbred strains of mice. Bone 22:211–216

    Article  CAS  PubMed  Google Scholar 

  25. Suda T, Takahashi N, Udagawa N, Jimi E, Gillespie MT, Martin TJ (1999) Modulation of osteoclast differentiation and function by the new members of the tumor necrosis factor receptor and ligand families. Endocr Rev 20:345–357

    Article  CAS  PubMed  Google Scholar 

  26. Suzuki N, Kitamura K, Omori K, Nemoto T, Satoh Y, Tabata MJ, Ikegame M, Yamamoto T, Ijiri K, Furusawa Y, Kondo T, Takasaki I, Tabuchi Y, Wada S, Shimizu N, Sasayama Y, Endo M, Takeuchi T, Nara M, Somei M, Maruyama Y, Hayakawa K, Shimazu T, Shigeto Y, Yano S, Hattori A (2009) Response of osteoblasts and osteoclasts in regenerating scales to gravity loading. Biol Sci Space 23:211–217

    Article  Google Scholar 

  27. Pan L, Shi X, Liu S, Guo X, Zhao M, Cai R, Sun G (2014) Fluoride promotes osteoblastic differentiation through canonical Wnt/β-catenin signaling pathway. Toxicol Lett 225:34–42

    Article  CAS  PubMed  Google Scholar 

  28. Yachiguchi K, Sekiguchi T, Nakano M, Hattori A, Yamamoto M, Kitamura K, Maeda M, Tabuchi Y, Kondo T, Kamauchi H, Nakabayashi H, Srivastav AK, Hayakawa K, Sakamoto T, Suzuki N (2014) Effect of inorganic mercury and methylmercury on osteoclasts and osteoblasts in the scales of the marine teleost as a model system of bone. Zool Sci 31:330–337

    Article  CAS  PubMed  Google Scholar 

  29. Thamamongood TA, Furuya R, Fukuba S, Nakamura M, Suzuki N, Hattori A (2012) Expression of osteoblastic and osteoclastic genes during spontaneous regeneration and autotransplantation of goldfish scale: a new tool to study intramembranous bone regeneration. Bone 50:1240–1249

    Article  CAS  PubMed  Google Scholar 

  30. Lacey DL, Boyle WJ, Simonet WS, Kostenuik PJ, Dougall WC, Sullivan JK, Martin JS, Dansey R (2012) Bench to bedside: elucidation of the OPG-RANK-RANKL pathway and the development of denosumab. Nat Rev Drug Discov 11:401–419

    Article  CAS  PubMed  Google Scholar 

  31. Kearns AE, Khosla S, Kostenuik PJ (2008) Receptor activator of nuclear factor κB ligand and osteoprotegerin regulation of bone remodeling in health and disease. Endocr Rev 29:155–192

    Article  CAS  PubMed  Google Scholar 

  32. Silva I, Branco JC (2011) RANK/RANKL/OPG: literature review. Acta Reumatol Port 36:209–218

    CAS  PubMed  Google Scholar 

  33. Everett ET (2011) Fluoride’s effects on the formation of teeth and bones, and the influence of genetics. J Dent Res 90:552–560

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This study was supported in part by grants to N.S. (Grant-in-Aid for Scientific Research [C] No. 16K07871 by JSPS), to A.H. (Grant-in-Aid for Scientific Research [C] No. 24570068 by JSPS), to T.S. (Scientific Research [C] No. 15K07126 by JSPS), and to H.M. (Scientific Research [C] No. 15K11034 by JSPS). This work was performed under the cooperative research program of the Institute of Nature and Environmental Technology, Kanazawa University, Acceptance No. 17022, in 2017. We greatly appreciate Notojima and Uozu aquariums for providing us with barred knifejaw.

Author information

Authors and Affiliations

  1. Noto Marine Laboratory, Institute of Nature and Environmental Technology, Kanazawa University, Ogi, Noto-cho, Ishikawa, 927-0553, Japan

    Masayuki Sato, Koji Yachiguchi, Yoichiro Kitani, Takahiro Ikari, Shouzo Ogiso, Toshio Sekiguchi, Makoto Urata & Nobuo Suzuki

  2. Electron Microscope Center, Tokyo University of Agriculture, Tokyo, 156-8502, Japan

    Keiichi Motohashi & Yukio Yaguchi

  3. Division of Molecular Genetics Research, Life Science Research Center, University of Toyama, Sugitani, Toyama, 930-0194, Japan

    Yoshiaki Tabuchi

  4. College of Aquaculture and Fisheries, Can Tho University, Can Tho, Vietnam

    Tran Ngoc Hai & Do Thi Thanh Huong

  5. Department of Science and Technology, Center of Application and Information, Camau, Vietnam

    Nguyen Viet Hoang

  6. Institute of Noto SATOUMI Education Research, Noto-cho, Ishikawa, 927-0553, Japan

    Makoto Urata

  7. Department of Dental Engineering, Tsurumi University School of Dental Medicine, Yokohama, 230-8501, Japan

    Hiroyuki Mishima

  8. Department of Biology, College of Liberal Arts and Sciences, Tokyo Medical and Dental University, Ichikawa, Chiba, 272-0827, Japan

    Atsuhiko Hattori

Authors
  1. Masayuki Sato
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Koji Yachiguchi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Keiichi Motohashi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yukio Yaguchi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yoshiaki Tabuchi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yoichiro Kitani
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Takahiro Ikari
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Shouzo Ogiso
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Toshio Sekiguchi
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Tran Ngoc Hai
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Do Thi Thanh Huong
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Nguyen Viet Hoang
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Makoto Urata
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Hiroyuki Mishima
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Atsuhiko Hattori
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. Nobuo Suzuki
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Nobuo Suzuki.

Additional information

An erratum to this article is available at http://dx.doi.org/10.1007/s12562-017-1092-2.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sato, M., Yachiguchi, K., Motohashi, K. et al. Sodium fluoride influences calcium metabolism resulting from the suppression of osteoclasts in the scales of nibbler fish Girella punctata . Fish Sci 83, 543–550 (2017). https://doi.org/10.1007/s12562-017-1086-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12562-017-1086-0

Keywords

Search

Navigation