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In vivo influence of sodium fluoride on sperm chemotaxis in male mice

  • Reproductive Toxicology
  • Published:
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Abstract

Reproductive process covers lots of procedures, including capacitation, hyperactivation, chemotaxis and the acrosome reaction. Each plays an important role in the success of fertilization. Although multiple studies have reported the toxic effects of fluoride on the male reproduction, the effect of fluoride on sperm chemotaxis is little known. This study is to examine the effect of fluoride on the sperm chemotaxis and then to reveal the underling mechanisms of fluoride toxicity in sperm chemotaxis. 260 healthy Kunming male mice (8 weeks old) were randomly divided into four groups and exposed to 50, 100, 150 mg NaF/L in the drinking water for 8 weeks. At the end of the exposure, sperm chemotaxis was examined using a microchannel-based device. Ca2+ concentration, adenylate cyclase (AC) content and mRNA expression of mACIII, mACVIII, Golf alpha, CatSper1, CatSper2 were measured to elucidate the possible molecular mechanisms. The results showed that the percentage of chemotactic sperm was decreased by NaF in a dose-dependent manner. In the 100 and 150 mg/L groups, Ca2+ concentration and AC content were notably lower than the control group. Compared with the control group, mRNA expression of CatSper1 in the 100 and 150 mg/L treatment groups was decreased significantly, and other genes showed no statistical difference. These data suggested that excessive fluoride did adversely affect sperm chemotaxis. The alteration of Ca2+ concentration, AC content and CatSper1 mRNA expression level may play a key role in the mechanism underlying the affection.

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References

  • Alvarez L, Dai L, Friedrich BM, Kashikar ND, Gregor I, Pascal R, Kaupp UB (2012) The rate of change in Ca2+ concentration controls sperm chemotaxis. J Cell Biol 196(5):653–663

    Article  CAS  PubMed  Google Scholar 

  • Bataineh HN, Nusier MK (2006) Impact of 12-week ingestion of sodium fluoride on aggression, sexual behavior, and fertility in adult male rats. Fluoride 39(4):293–301

    CAS  Google Scholar 

  • Blengini CS, Teves ME, Uñates DR, Guidobaldi HA, Gatica LV, Giojalas LC (2011) Human sperm pattern of movement during chemotactic re-orientation towards a progesterone source. J Asian Androl 13(5):769–773

    Article  Google Scholar 

  • Branscomb A, Seger J, White RL (2000) Evolution of odorant receptors expressed in mammalian testes. Genetics 156(2):785–997

    CAS  PubMed  Google Scholar 

  • Chlubek D (2003) Fluoride and oxidative stress. Fluoride 36(4):217–228

    CAS  Google Scholar 

  • Dvoráková-Hortová K, Sandera M, Jursová M, Vasinová J, Peknicová J (2008) The influence of fluorides on mouse sperm capacitation. Anim Reprod Sci 108(1–2):157–170

    Article  PubMed  Google Scholar 

  • Eisenbach M (1999) Sperm chemotaxis. Rev Reprod 4(1):56–66

    Article  CAS  PubMed  Google Scholar 

  • Eisenbach M, Giojalas LC (2006) Sperm guidance in mammals: an unpaved road to the egg. Nat Rev Mol Cell Biol 7(4):276–285

    Article  CAS  PubMed  Google Scholar 

  • Fawell J, Bailey K, Chilton J, Dahi E, Fewtrell L, Magara Y (2006) Fluoride in drinking-water. IWA Publishing and World Health Publishing, London, p 100

    Google Scholar 

  • Freni SC (1994) Exposure to high fluoride concentrations in drinking water is associated with decreased birth rates. J Toxicol Environ Health 42(1):109–121

    Article  CAS  PubMed  Google Scholar 

  • Friedrich BM, Jülicher F (2007) Chemotaxis of sperm cells. PNAS 104(33):13256–13261

    Article  CAS  PubMed  Google Scholar 

  • Ghosh D, Das Sarkar S, Maiti R, Jana D, Das UB (2002) Testicular toxicity in sodium fluoride treated rats: association with oxidative stress. Reprod Toxicol 16(4):385–390

    Article  CAS  PubMed  Google Scholar 

  • Guo XY, Sun GF, Sun YC (2003) Oxidative stress from fluoride-induced hepatotoxicity in rats. Fluoride 36(1):25–29

    CAS  Google Scholar 

  • Huang C, Niu RY, Wang JD (2007) Toxic effects of sodium fluoride on reproductive function in male mice. Fluoride 40(3):162–168

    CAS  Google Scholar 

  • Huang C, Yang HB, Niu RY, Sun ZL, Wang JD (2008) Effects of sodium fluoride on androgen receptor expression in male mice. Fluoride 41(1):10–17

    CAS  Google Scholar 

  • Izquierdo-Vega JA, Sánchez-Gutiérrez M, Del Razo LM (2008) Decreased in vitro fertility in male rats exposed to fluoride-induced oxidative stress damage and mitochondrial transmembrane potential loss. Toxicol Appl Pharmacol 230(3):352–357

    Article  CAS  PubMed  Google Scholar 

  • Kaupp UB, Hildebrand E, Weyand I (2006) Sperm chemotaxis in marine invertebrates: molecules and mechanisms. J Cell Physiol 208(3):487–494

    Article  CAS  PubMed  Google Scholar 

  • Kirichok Y, Lishko PV (2011) Rediscovering sperm ion channels with the patch-clamp technique. Mol Hum Reprod 17(8):478–499

    Article  CAS  PubMed  Google Scholar 

  • Ko YJ, Maeng JH, Lee BC, Lee S, Hwang SY, Ahn Y (2012) Separation of progressive motile sperm from mouse semen using on-chip chemotaxis. Anal Sci 28(1):27–32

    Article  CAS  PubMed  Google Scholar 

  • Koyama S, Amarie D, Soini HA, Novotny MV, Jacobson SC (2006) Chemotaxis assays of mouse sperm on microfluidic devices. Anal Chem 78(10):3354–3359

    Article  CAS  PubMed  Google Scholar 

  • Krechniak J, Inkielewicz I (2005) Correlations between fluoride concentration and free radical parameters in soft tissues of rats. Fluoride 38(4):293–296

    CAS  Google Scholar 

  • Lawson PB, Yu MH (2003) Fluoride inhibition of superoxide dismutase (SOD) from the earthworm Eisenia fetida. Fluoride 36(3):143–151

    CAS  Google Scholar 

  • Lishko PV, Kirichok Y, Ren D, Navarro B, Chung JJ, Clapham DE (2012) The control of male fertility by spermatozoan ion channels. Annu Rev Physiol 74:453–475

    Article  CAS  PubMed  Google Scholar 

  • Lou DD, Guan ZZ, Liu YJ, Liu YF, Zhang KL, Pan JG, Pei JJ (2013) The influence of chronic fluorosis on mitochondrial dynamics morphology and distribution in cortical neurons of the rat brain. Arch Toxicol 87(3):449–457

    Article  CAS  PubMed  Google Scholar 

  • Mittal M, Flora SJ (2007) Vitamin E supplementation protects oxidative stress during arsenic and fluoride antagonism in male mice. Drug Chem Toxicol 30(3):263–281

    Article  CAS  PubMed  Google Scholar 

  • Nabavi SF, Nabavi SM, Latifi AM, Mirzaei M, Habtemariam S, Moghaddam AH (2012) Mitigating role of quercetin against sodium fluoride-induced oxidative stress in the rat brain. Pharm Biol 50(11):1380–1383

    Article  CAS  PubMed  Google Scholar 

  • Narayana MV, Chinoy NJ (1994) Effect of fluoride on rat testicular steroidogenesis. Fluoride 27(1):7–12

    CAS  Google Scholar 

  • Oliveira RG, Tomasi L, Rovasio RA, Giojalas LC (1999) Increased velocity and induction of chemotactic response in mouse spermatozoa by follicular and oviductal fluids. J Reprod Fertil 115(1):23–27

    Article  CAS  PubMed  Google Scholar 

  • Ortiz-Pérez D, Rodríguez-Martínez M, Martínez F, Borja-Aburto VH, Castelo J, Grimaldo JI, de la Cruz E, Carrizales L, Díaz-Barriga F (2003) Fluoride-induced disruption of reproductive hormones in men. Environ Res 93(1):20–30

    Article  PubMed  Google Scholar 

  • Ostermeier GC, Dix DJ, Miller D, Khatri P, Krawetz SA (2002) Spermatozoal RNA profiles of normal fertile men. Lancet 360(9335):772–777

    Article  CAS  PubMed  Google Scholar 

  • Parmentier M, Libert F, Schurmans S, Schiffmann S, Lefort A, Eggerickx D, Ledent C, Mollereau C, Gérard C, Perret J et al (1992) Expression of members of the putative olfactory receptor gene family in mammalian germ cells. Nature 355(6359):453–455

    Article  CAS  PubMed  Google Scholar 

  • Pushpalatha T, Srinivas M, Sreenivasula Reddy P (2005) Exposure to high fluoride concentration in drinking water will affect spermatogenesis and steroidogenesis in male albino rats. Biometals 18(3):207–212

    Article  CAS  PubMed  Google Scholar 

  • Shanthakumari D, Srinivasalu S, Subramanian S (2004) Effect of fluoride intoxication on lipidperoxidation and antioxidant status in experimental rats. Toxicology 204(2–3):219–228

    Article  CAS  PubMed  Google Scholar 

  • Spehr M, Schwane K, Riffell JA, Barbour J, Zimmer RK, Neuhaus EM, Hatt H (2004) Particulate adenylate cyclase plays a key role in human sperm olfactory receptor-mediated chemotaxis. J Biol Chem 279(38):40194–40203

    Article  CAS  PubMed  Google Scholar 

  • Spittle B (2008) Fluoride and fertility [editorial]. Fluoride 41(2):98–100

    Google Scholar 

  • Strünker T, Goodwin N, Brenker C, Kashikar ND, Weyand I, Seifert R, Kaupp UB (2011) The CatSper channel mediates progesterone-induced Ca2+ influx in human sperm. Nature 471(7338):382–386

    Article  PubMed  Google Scholar 

  • Sun F, Giojalas LC, Rovasio RA, Tur-Kaspa I, Sanchez R, Eisenbach M (2003) Lack of species-specificity in mammalian sperm chemotaxis. Dev Biol 255(2):423–427

    Article  CAS  PubMed  Google Scholar 

  • Sun F, Bahat A, Gakamsky A, Girsh E, Katz N, Giojalas LC, Tur-Kaspa I, Eisenbach M (2005) Human sperm chemotaxis: both the oocyte and its surrounding cumulus cells secrete sperm chemoattractants. Hum Reprod 20(3):761–767

    Article  CAS  PubMed  Google Scholar 

  • Sun Z, Niu R, Su K, Wang B, Wang J, Zhang J, Wang J (2010) Effects of sodium fluoride on hyperactivation and Ca2+ signaling pathway in sperm from mice: an in vivo study. Arch Toxicol 84(5):353–361

    Article  CAS  PubMed  Google Scholar 

  • Sun Z, Niu R, Wang B, Jiao Z, Wang J, Zhang J, Wang S, Wang J (2011) Fluoride-induced apoptosis and gene expression profiling in mice sperm in vivo. Arch Toxicol 85(11):1441–1452

    Article  CAS  PubMed  Google Scholar 

  • Susheela AK, Kumar A (1991) A study of the effect of high concentrations of fluoride on the reproductive organs of male rabbits, using light and scanning electron microscopy. J Reprod Fertil 92(2):353–360

    Article  CAS  PubMed  Google Scholar 

  • Teves ME, Guidobaldi HA, Uñates DR, Sanchez R, Miska W, Publicover SJ, Morales Garcia AA, Giojalas LC (2009) Molecular mechanism for human sperm chemotaxis mediated by progesterone. PLoS One 4(12):e8211

    Article  PubMed Central  PubMed  Google Scholar 

  • Varol E, Varol S (2012) Effect of fluoride toxicity on cardiovascular systems: role of oxidative stress. Arch Toxicol 86(10):1627

    Article  CAS  PubMed  Google Scholar 

  • Wolfner MF (2011) Precious essences: female secretions promote sperm storage in Drosophila. PLoS Biol 9(11):e1001191

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Xie L, Ma R, Han C, Su K, Zhang Q, Qiu T, Wang L, Huang G, Qiao J, Wang J, Cheng J (2010) Integration of sperm motility and chemotaxis screening with a microchannel-based device. Clin Chem 56(8):1270–1278

    Article  CAS  PubMed  Google Scholar 

  • Zhang JH, Liang C, Ma JJ, Niu RY, Wang JD (2006) Effects of sodium fluoride and sulfur dioxide on sperm motility and serum testosterone in male rats. Fluoride 39(2):126–131

    CAS  Google Scholar 

  • Zimmer RK, Riffrey JA (2011) Sperm chemotaxis, fluid shear, and the evolution of sexual reproduction. PNAS 108(32):13200–13205

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This research was supported by China National Natural Science Foundation (31072180, 31201965 and 31172376).

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The authors declare that there are no conflicts of interest.

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Authors and Affiliations

  1. Shanxi Key Laboratory of Ecological Animal Science and Environmental Veterinary Medicine, Shanxi Agricultural University, Taigu, 030801, Shanxi, People’s Republic of China

    Zhaojing Lu, Zilong Sun, Ruiyan Niu & Jundong Wang

  2. Department of Psychiatry and Neurobehavioral Sciences, University of Virginia, Charlottesville, VA, 22911, USA

    Shaolin Wang

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  1. Zhaojing Lu
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  2. Shaolin Wang
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  3. Zilong Sun
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  4. Ruiyan Niu
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  5. Jundong Wang
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Correspondence to Jundong Wang.

Additional information

Zhaojing Lu, Shaolin Wang and Zilong Sun have contributed equally to this work and should be considered co-first authors.

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Lu, Z., Wang, S., Sun, Z. et al. In vivo influence of sodium fluoride on sperm chemotaxis in male mice. Arch Toxicol 88, 533–539 (2014). https://doi.org/10.1007/s00204-013-1099-0

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  • DOI: https://doi.org/10.1007/s00204-013-1099-0

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