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Nickel deficiency diminishes sperm quantity and movement in rats

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Abstract

Early studies on nickel essentiality with rats and goats indicated that nickel deprivation impaired reproductive performance. Nickel also has been found to influence cyclic nucleotide gated channels (CNG); these types of channels are important in sperm physiology. Thus, two experiments were conducted to test the hypothesis that nickel deficiency affects sperm physiology in a manner consistent with nickel having an essential function related to CNG channel functions. The experiments were factorially arranged with four treatment groups of eight weanling rats in each. In experiment 1, the treatments were supplemental dietary nickel of 0 and 1 mg/kg and N ω-nitro-l-arginine methyl ester (l-NAME, a nitric oxide synthase inhibitor) added to the drinking water (50 mg/100 mL) the last 3 wk of an 8-wk experiment. In experment 2, the treatments were supplemental dietary nickel at 0 and 1 mg/kg and supplemental dietary sodium chloride (NaCl) at 0 and 80 g/kg. The NaCl and l-NAME variables were included to act as stressors affecting CNG channel activity. The basal diet contained per kilogram about 27 µg of nickel and 1 g of sodium. After 8 wk in experiment 1 and 16 wk in experiment 2, urine while fasting and testes and epididymis in both experiments, and seminal vesicles and prostates in experiment 2 were harvested for analysis. Nickel deprivation significantly decreased spermatozoa motility and density in the epididymides, epididymal transit time of spermatozoa, and testes sperm production rate. Nickel deficiency also significantly decreased the weights of the seminal vesicles and prostate glands. Excessive NaCl had no effect on sperm physiology; however, it decreased prostate gland weights. The findings support the hypothesis that nickel has an essential function that possibly could affect reproductive performance in higher animals, perhaps through affecting a CNG channel function.

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References

  1. F. H. Nielsen, D. R. Myron, S. H. Givand, et al., Nickel deficiency in rats, J. Nutr. 105, 1620–1630 (1975).

    PubMed  CAS  Google Scholar 

  2. M. Anke, B. Groppel, U. Krause, et al., Further data on the biological essentiality of nickel, in Trace Elements in Man and Animals 6, L. S. Hurley, C. L. Keen, B. Lonnerdal, et al., eds., Plenum, New York, pp. 467–469 (1988).

    Google Scholar 

  3. M. Ildefonse and N. Bennett, Single-channel study of the cGMP-dependent conductance of retinal rods from incorporation of native vesicles into planar bilayers, J. Membr. Biol. 123, 133–147 (1991).

    Article  PubMed  CAS  Google Scholar 

  4. M. Ildefonse, S. Crouzy, and N. Bennett, Gating of retinal rod cation channel by different nucleotides: comparative study of unitary currents, J. Membr. Biol. 130, 91–104 (1992).

    PubMed  CAS  Google Scholar 

  5. J. W. Karpen, R. L. Brown, L. Stryer, et al., Interaction between divalent cations and the gating machinery of cyclic GMP-activated channels in salamander retinal rods, J. Gen. Physiol. 101, 1–25 (1993).

    Article  PubMed  CAS  Google Scholar 

  6. P. A. Kingston, F. Zufall, and C. J. Barnstable, Rat hippocampal neurons express genes for both rod retinal and olfactory cyclic nucleotide-gated channels: novel targets for cAMP/cGMP function, Proc. Natl. Acad. Sci. USA 93, 10,440–10,445 (1996).

    Article  CAS  Google Scholar 

  7. J. Bradley, Y. Zhang, R. Bakin, et al., Functional expression of the heteomeric “olfactory” cyclic nucleotide-gated channel in the hippocampus: a potential effector of synaptic plasticity in brain neurons, J. Neurosci. 17, 1993–2005 (1997).

    PubMed  CAS  Google Scholar 

  8. I. Ahmad, C. Korbmacher, A. S. Segal, et al., Mouse cortical collecting duct cells show nonselective cation channel activity and express a gene related to the cGMP-gated rod photoreceptor channel, Proc. Natl. Acad. Sci. USA 89, 10,262–10,266 (1999).

    Google Scholar 

  9. M. Biel, X. Zong, M. Distler, et al., Another member of the cyclic nucleotide-gated channel family, expressed in testis, kidney, and heart, Proc. Natl. Acad. Sci. USA 91, 3505–3509 (1994).

    Article  PubMed  CAS  Google Scholar 

  10. M. Biel, W. Altenhofen, R. Hullin, et al., Primary structure and functional expression of a cyclic nucleotide-gated channel from rabbit aorta, FEBS Lett. 329, 134–138 (1993).

    Article  PubMed  CAS  Google Scholar 

  11. I. Weyand, M. Godde, S. Frings, et al., Cloning and functional expression of a cyclicnucleotide-gated channel from mammalian sperm, Nature 368, 859–863 (1994).

    Article  PubMed  CAS  Google Scholar 

  12. B. Wiesner, J. Weiner, R. Middendorff, et al., Cyclic nucleotide-gated channels on the flagellum control Ca2+ entry into sperm, J. Cell Biol. 142, 473–484 (1998).

    Article  PubMed  CAS  Google Scholar 

  13. D. Ritter, A. D. Dean, S. L. Gluck, et al., Natriuretic peptide receptors A and B have different cellular distribution in rat kidney, Kidney Int. 48, 5758–5766 (1995).

    Article  PubMed  CAS  Google Scholar 

  14. Y. Terada, K. Tomita, H. Nonoguchi, et al., PCR localization of C-type natriuretic peptide and B-type receptor mRNAs in rat nephron segments, Am. J. Physiol. 267, F215–F222 (1994).

    PubMed  CAS  Google Scholar 

  15. J. Navarro, A. Sanchez, J. Saiz, et al., Hormonal, renal, and metabolic alterations during hypertension induced by chronic inhibition of NO in rats, Am. J. Physiol. 267, R1516–R1521 (1994).

    PubMed  CAS  Google Scholar 

  16. P. Burguera, A. Sanchez de Briceno, C. E. Rondon, et al., Determination of nickel in saliva by electrothermal atomic absorption spectrometry using various chemical modifiers with Zeeman effect background correction, J. Trace Elements Med. Biol. 12, 115–120 (1998).

    CAS  Google Scholar 

  17. R. L. Dahlquist and J. W. Knoll, Inductively coupled plasma-atomic emission spectrometry: analysis of biological materials and soils in major, trace and ultra-trace elements, Appl. Spectrosc. 32, 1–29 (1978).

    Article  CAS  Google Scholar 

  18. P. G. Reeves and K. L. Rossow, Zinc deficiency affects the activity and protein concentration of angiotensin-converting enzyme in rat testes, Proc. Soc. Exp. Biol. Med. 203, 336–342 (1993).

    PubMed  CAS  Google Scholar 

  19. G. W. Robb, R. P. Amann, and G. J. Killian, Daily sperm production and epididymal sperm reserves of pubertal and adult rats, J. Reprod. Fertil. 54, 103–107 (1978).

    Article  PubMed  CAS  Google Scholar 

  20. A. Fernandez-Rivas, J. Garcia-Estan, and F. Vargas, Effects of chronic increased salt intake on nitric oxide synthesis inhibition-induced hypertension, J. Hypertens. 13, 123–128 (1995).

    Article  PubMed  CAS  Google Scholar 

  21. A. Swislocki, T. Eason, and C. A. Kaysen, Oral administration of the nitric oxide biosynthesis inhititor, N-nitro-l-arginine methyl ester (l-NAME), causes hypertension, but not glucose intolerance or insulin resistance, in rats, Am. J. Hypertens. 8, 1009–1014 (1995).

    Article  PubMed  CAS  Google Scholar 

  22. H. Tsukahara, T. Imura, S. Tsuchida, et al., Renal functional measurements in young rats with chronic inhibition of nitric oxide synthase, Acta Paediatr. Jpn. 38, 614–618 (1996).

    PubMed  CAS  Google Scholar 

  23. S. L. Lubarsky, R. A. Ahokas, S. A. Friedman, et al., The effect of chronic nitric oxide synthesis inhibition on blood pressure and angiotension II responsiveness in the pregnant rat, Am. J. Obstet. Gynecol. 176, 1069–1076 (1997).

    Article  PubMed  CAS  Google Scholar 

  24. N. Akuzawa, T. Nakamura, T. Kurashina, et al., Antihypertensive agents prevent nephrosclerosis and left ventricular hypertrophy induced in rats by prolonged inhibition of nitric oxide synthesis, Am. J. Hypertens. 11, 697–707 (1998).

    Article  PubMed  CAS  Google Scholar 

  25. R. Kakela, A. Kakela, and H. Hyvarinen, Effects of nickel chloride on reproduction of the rat and possible antagonistic role of selenium, Comp. Biochem. Physiol. C. 123, 27–37 (1999).

    PubMed  CAS  Google Scholar 

  26. E. Obone, S. K. Chakrabarti, C. Bai, et al., Toxicity and bioaccumulation of nickel sulfate in Sprague-Dawley rats following 13 weeks of subchronic exposure, J. Toxicol. Environ. Health 57A, 379–401 (1999).

    Article  Google Scholar 

  27. L. M. King, W. A. Banks, and W. J. George, Differential zinc transport into testis and brain of cadmium-sensitive and -resistant murine strains, J. Androl. 21, 656–663 (2000).

    PubMed  CAS  Google Scholar 

  28. S. E. Gordon and W. N. Zagotta, Subunit interactions in coordination of Ni2+ in cyclic nucleotide-gated channels, Proc. Natl. Acad. Sci. USA 92, 10,222–10,226 (1995).

    Article  CAS  Google Scholar 

  29. B. Morton, J. Harrigan-Lum, L. Albagli, et al., The activation of motility in quiescent hamster sperm from the epididymis by calcium and cyclic nucleotides, Biochem. Biophys. Res. Commun. 56, 372–379 (1974).

    Article  PubMed  CAS  Google Scholar 

  30. R. A. Anderson, Jr., K. A. Feathergill, R. G. Rawlins, et al., Atrial natriuretic peptide: a chemoattractant of human spermatozoa by a guanylate cyclase-dependent pathway, Mol. Reprod. Dev. 40, 371–378 (1995).

    Article  PubMed  CAS  Google Scholar 

  31. D. E. McCoy, S. E. Guggino, and B. A. Stanton, The renal cGMP-gated cation channel: its molecular structure and physiological role, Kidney Int. 48, 1125–1133 (1995).

    Article  PubMed  CAS  Google Scholar 

  32. D. H. Vandorpe, F. Ciampolillo, R. B. Green, et al., Cyclic nucleotide-gated cation channels mediate sodium absorption by IMCD (mIMCD-K2) cells, Am. J. Physiol. 272, C901–C910 (1997).

    PubMed  CAS  Google Scholar 

  33. J. C. Hansen and R. C. Jones, In vivo microperfusion of the ductuli efferentes testis of the rat: flow dependence of fluid reabsorption, Exp. Physiol. 81, 633–644 (1996).

    PubMed  Google Scholar 

  34. R. Middendorff, M. S. Davidoff, S. Behrends, et al., Multiple roles of the messenger molecule cGMP in testicular function, Andrologia 32, 55–59 (2000).

    PubMed  CAS  Google Scholar 

  35. R. Middendorff, D. Muller, H. J. Paust, et al., New aspects of Leydig cell function, Adv. Exp. Med. Biol. 424, 125–138 (1997).

    PubMed  CAS  Google Scholar 

  36. P. Rossi, R. Pezzotti, M. Conti, et al., Cyclic nucleotide phosphodiesterases in somatic and germ cells of mouse seminiferous tubules, J. Reprod. Fertil. 74, 317–322 (1985).

    Article  PubMed  CAS  Google Scholar 

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Author notes

  1. Katsuhiko Yokoi

    Present address: Department of Human Life and Culture, Seitoku University Faculty of Humanities, 550 Iwase, Matsudo, 271-8555, Chiba, Japan

Authors and Affiliations

  1. United States Department of Agriculture, Agricultural Research Service, Grand Forks Human Nutrition Research Center, 58202-9034, Grand Forks, ND

    Katsuhiko Yokoi, Eric O. Uthus & Forrest H. Nielsen

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  1. Katsuhiko Yokoi
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  2. Eric O. Uthus
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  3. Forrest H. Nielsen
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Additional information

Part of the data was presented at the Experimental Biology 2001 Meeting, Orlando, FL, March 31–April 4, 2001. (F. H. Nielsen, E. O. Uthus and K. Yokoi, Dietary nickel deprivation decreases sperm motility and evokes hypertension in rats, FASEB J. 15, A972 (2001), and K. Yokoi, E. O. Uthus and F. H. Nielsen, Nickel deficiency induces renal damages and hypertension in rats which is augmented by sodium chloride, FASEB J. 15, A973 (2001).

The US Department of Agriculture, Agricultural Research Service, Northern Plains Area, is an equal opportunity/affirmative action employer and all agency services are available without discrimination.

Mention of a trademark or proprietary product does not constitute a guarantee or warranty of the product by the US Department of Agriculture and does not imply its approval to the exclusion of the products that may also be suitable.

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Yokoi, K., Uthus, E.O. & Nielsen, F.H. Nickel deficiency diminishes sperm quantity and movement in rats. Biol Trace Elem Res 93, 141–153 (2003). https://doi.org/10.1385/BTER:93:1-3:141

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  • DOI: https://doi.org/10.1385/BTER:93:1-3:141

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