Skip to main content
SpringerLink
Log in

Mapping Fifteen Trace Elements in Human Seminal Plasma and Sperm DNA

  • Published:
Biological Trace Element Research Aims and scope Submit manuscript

Abstract

Studies suggest a relationship between semen quality and the concentration of trace elements in serum or seminal plasma. However, trace elements may be linked to DNA and capable of altering the gene expression patterns. Thus, trace element interactions with DNA may contribute to the mechanisms for a trans-generational reproductive effect. We developed an analytical method to determine the amount of trace elements bound to the sperm DNA, and to estimate their affinity for the sperm DNA by the ratio: R = Log [metal concentration in the sperm DNA/metal concentration in seminal plasma]. We then analyzed the concentrations of 15 trace elements (Al, Cd, Cr, Cu, Hg, Mn, Mo, Ni, Pb, Ti, V, Zn, As, Sb, and Se) in the seminal plasma and the sperm DNA in 64 normal and 30 abnormal semen specimens with Inductively Coupled Plasma/Mass Spectrometry (ICP-MS). This study showed all trace elements were detected in the seminal plasma and only metals were detected in the sperm DNA. There was no correlation between the metals’ concentrations in the seminal plasma and the sperm DNA. Al had the highest affinity for DNA followed by Pb and Cd. This strong affinity is consistent with the known mutagenic effects of these metals. The lowest affinity was observed for Zn and Ti. We observed a significant increase of Al linked to the sperm DNA of patients with oligozoospermia and teratozoospermia. Al’s reproductive toxicity might be due to Al linked to DNA, by altering spermatogenesis and expression patterns of genes involved in the function of reproduction.

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

Similar content being viewed by others

References

  1. Geoffroy-Siraudin C, Loundou AD, Romain F, Achard V, Courbiere B, Perrard MH, et al. (2012) Decline of semen quality among 10 932 males consulting for couple infertility over a 20-year period in Marseille, France. Asian J Androl 14:584–590

    Article  PubMed  PubMed Central  Google Scholar 

  2. Al Bakheet SA, Attafi IM, Maayah ZH, Abd-Allah AR, Asiri YA, Korashy HM (2013) Effect of long-term human exposure to environmental heavy metals on the expression of detoxification and DNA repair genes. Environ Pollut 181:226–232

    Article  PubMed  Google Scholar 

  3. Godschalk R, Hogervorst J, Albering H, Mercelina-Roumans P, van Schooten FJ, de Haan J, et al. (2005) Interaction between cadmium and aromatic DNA adducts in hprt mutagenesis during foetal development. Mutagenesis 20:181–185

    Article  CAS  PubMed  Google Scholar 

  4. Xu DX, Shen HM, Zhu QX, Chua L, Wang QN, Chia SE, et al. (2003) The associations among semen quality, oxidative DNA damage in human spermatozoa and concentrations of cadmium, lead and selenium in seminal plasma. Mutat Res 534:155–163

    Article  CAS  PubMed  Google Scholar 

  5. Venkatramreddy V, Tchounwou PB (2013) Oxidative stress and DNA damage induced by chromium in liver and kidney of goldfish, Carassius auratus. Biomark Insights 8:43–51

    Google Scholar 

  6. Caicedo M, Jacobs JJ, Reddy A, Hallab NJ (2007) Analysis of metal ion-induced DNA damage, apoptosis, and necrosis in human (Jukart) T-cells demonstrates Ni2+ and V3+ are more toxic than other metals: Al3+, Be2+, Co2+, Cr3+, Cu2+, Fe3+, Mo5+, Nb5+, Zr2+. J Biomed Mater Res Part A:905–913

    Google Scholar 

  7. Kawata K, Shimazaki R, Okabe S (2009) Comparison of gene expression profiles in HepG2 cells exposed to arsenic, cadmium, nickel, and three model carcinogens for investigating the mechanisms of metal carcinogenesis. Environ Mol Mutagen 50:46–59

    Article  CAS  PubMed  Google Scholar 

  8. Sorokin VA, Valeev VA, Gladchenko GO, Sysa IV, Blagoi YP, Volchok IV (1996) Interaction of bivalent copper, nickel, manganese ions with native DNA and its monomers. J Inorg Biochem 63:79–98

    Article  CAS  PubMed  Google Scholar 

  9. Mazzuca D, Russo N, Toscano M, Grand A (2006) On the interaction of bare and hydrated aluminum ion with nucleic acid bases (U, T, C, a, G) and monophosphate nucleotides (UMP, dTMP, dCMP, dAMP, dGMP). J Phys Chem B 110:8815–8824

    Article  CAS  PubMed  Google Scholar 

  10. Zhang X, Wang F, Liu B, Kelly EY, Servos MR, Liu J (2014) Adsorption of DNA oligonucleotides by titanium dioxide nanoparticles. Langmuir 30:839–845

    Article  CAS  PubMed  Google Scholar 

  11. Millonig H, Pous J, Gouyette C, Subirana JA, Campos JL (2009) The interaction of manganese ions with DNA. J Inorg Biochem 103:876–880

    Article  CAS  PubMed  Google Scholar 

  12. Smith NM, Amrane S, Rosu F, Gabelica V, Mergny JL (2012) Mercury-thymine interaction with a chair type G-quadruplex architecture. Chem Commun (Cambridge, England) 48:11464–11466

    Article  CAS  Google Scholar 

  13. Koc H, Swenberg JA (2002) Applications of mass spectrometry for quantification of DNA adducts. J Chromatogr 778:323–343

    CAS  Google Scholar 

  14. Carette D, Perrard MH, Prisant N, Gilleron J , Pointis G, Segretain D, Durand D. Hexavalent chromium at low concentration alters Sertoli cell barrier and connexin-43 gap junction but not claudin-11 and N-cadherin in the rat seminiferous tubule culture model. Toxicol Appl Pharmacol 2013;268:27–36.

    Article  CAS  PubMed  Google Scholar 

  15. Chung NP, Cheng CY (2001) Is cadmium chloride-induced inter-Sertoli tight junction permeability barrier disruption a suitable in vitro model to study the events of junction disassembly during spermatogenesis in the rat testis? Endocrinology 142:1878–1888

    CAS  PubMed  Google Scholar 

  16. Oldereid NB, Thomassen Y, Purvis K (1998) Selenium in human male reproductive organs. Hum Reprod 13:2172–2176

    Article  CAS  PubMed  Google Scholar 

  17. Bjorndahl L, Kvist U (2010) Human sperm chromatin stabilization: a proposed model including zinc bridges. Mol Hum Reprod 16:23–29

    Article  PubMed  Google Scholar 

  18. Lai JC, Lai MB, Jandhyam S, Dukhande VV, Bhushan A, Daniels CK, et al. (2008) Exposure to titanium dioxide and other metallic oxide nanoparticles induces cytotoxicity on human neural cells and fibroblasts. Int J Nanomedicine 3:533–545

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Ema M, Kobayashi N, Naya M, Hanai S, Nakanishi J (2010) Reproductive and developmental toxicity studies of manufactured nanomaterials. Reprod Toxicol (Elmsford, NY) 30:343–352

    Article  CAS  Google Scholar 

  20. Peto MV (2010) Aluminium and iron in humans: bioaccumulation, pathology, and removal. Rejuvenation Res 13:589–598

    Article  CAS  PubMed  Google Scholar 

  21. Kim H, Lee HJ, Hwang JY, Ha EH, Park H, Ha M, et al. (2010) Blood cadmium concentrations of male cigarette smokers are inversely associated with fruit consumption. J Nutr 140:1133–1138

    Article  CAS  PubMed  Google Scholar 

  22. Barceloux DG (1999) Chromium. J Toxicol Clin Toxicol 37:173–194

    Article  CAS  PubMed  Google Scholar 

  23. Von Burg R, Liu D (1993) Chromium and hexavalent chromium. J Appl Toxicol 13:225–230

    Article  Google Scholar 

  24. World Health Organisation (2010) WHO Laboratory manual for the examination and processing of human semen. WHO Press, Geneva

    Google Scholar 

  25. Auger J, Eustache F, David G (2000) Standardisation de la classification morphologique des spermatozoïdes humains selon la méthode de David modifiée. Andrologie 10:358–373

    Article  Google Scholar 

  26. Queiroz EK, Waissmann W (2006) Occupational exposure and effects on the male reproductive system. Cad Saude Publica 22:485–493

    Article  PubMed  Google Scholar 

  27. Minguez-Alarcon L, Mendiola J, Roca M, Lopez-Espin JJ, Guillen JJ, Moreno JM, et al. (2012) Correlations between different heavy metals in diverse body fluids: studies of human semen quality. Adv Urol 2012:420893

    Article  PubMed  PubMed Central  Google Scholar 

  28. Giaccio L, Cicchella D, De Vivo B, Lombardi G, De Rosa M (2012) Does heavy metals pollution affects semen quality in men? A case of study in the metropolitan area of Naples (Italy). J Geochem Explor 112:218–225

    Article  CAS  Google Scholar 

  29. Benoff S, Centola GM, Millan C, Napolitano B, Marmar JL, Hurley IR (2003) Increased seminal plasma lead levels adversely affect the fertility potential of sperm in IVF. Hum Reprod 18:374–383

    Article  CAS  PubMed  Google Scholar 

  30. Mendiola J, Moreno JM, Roca M, Vergara-Juarez N, Martinez-Garcia MJ, Garcia-Sanchez A, et al. (2011) Relationships between heavy metal concentrations in three different body fluids and male reproductive parameters: a pilot study. Environ Health 10:6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Telisman S, Cvitkovic P, Jurasovic J, Pizent A, Gavella M, Rocic B (2000) Semen quality and reproductive endocrine function in relation to biomarkers of lead, cadmium, zinc, and copper in men. Environ Health Perspect 108:45–53

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Telisman S, Colak B, Pizent A, Jurasovic J, Cvitkovic P (2007) Reproductive toxicity of low-level lead exposure in men. Environ Res 105:256–266

    Article  CAS  PubMed  Google Scholar 

  33. Li P, Zhong Y, Jiang X, Wang C, Zuo Z, Sha A (2012) Seminal plasma metals concentration with respect to semen quality. Biol Trace Elem Res 148:1–6

    Article  CAS  PubMed  Google Scholar 

  34. Rossman TG, Klein CB (2011) Genetic and epigenetic effects of environmental arsenicals. Metallomics 3:1135–1141

    Article  CAS  PubMed  Google Scholar 

  35. ViIlaverde AISB, Fioratti EG, Ramos RS, Neves RCF, Ferreira JCP, Cardoso GS, Padilha PM, Lopes MD (2014) Blood and seminal plasma concentrations of selenium, zinc and testosterone and their relationship to sperm quality and testicular biometry in domestic cats. Anim Reprod Sci 150:50–55

    Article  Google Scholar 

  36. Atig F, Raffa M, Habib BA, Kerkeni A, Saad A, Ajina M (2012) Impact of seminal trace element and glutathione levels on semen quality of Tunisian infertile men. BMC Urol 12:6–13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Figa-Talamenca I, Traina ME, Urbani E (2001) Occupational exposure to metals, solvents and pesticides: recent evidence on male reproductive effects and biological markers. Occup Med 51:174–188

    Article  Google Scholar 

  38. Hovatta O, Venalainen ER, Kuusimaki L, Heikkila J, Hirvi T, Reima I (1998) Aluminium, lead and cadmium concentrations in seminal plasma and spermatozoa, and semen quality in Finnish men. Hum Reprod 13:115–119

    Article  CAS  PubMed  Google Scholar 

  39. Klein JP, Mold M, Mery L, Cottier M, Exley C (2014) Aluminum content of human semen: implications for semen quality. Reprod Toxicol (Elmsford, NY) 50:43–48

    Article  CAS  Google Scholar 

  40. Alexander BH, Checkoway H, Faustman EM, van Netten C, Muller CH, Ewers TG (1998) Contrasting associations of blood and semen lead concentrations with semen quality among lead smelter workers. Am J Ind Med 34:464–469

    Article  CAS  PubMed  Google Scholar 

  41. Exley C (2013) Human exposure to aluminium. Environ Sci Process Impacts 15:1807–1816

    Article  CAS  PubMed  Google Scholar 

  42. Bagchi D, Stohs SJ, Downs BW, Bagchi M, Preuss HG (2002) Cytotoxicity and oxidative mechanisms of different forms of chromium. Toxicology 180:5–22

    Article  CAS  PubMed  Google Scholar 

  43. Aduayom I, Campbell PG, Denizeau F, Jumarie C (2003) Different transport mechanisms for cadmium and mercury in Caco-2 cells: inhibition of Cd uptake by Hg without evidence for reciprocal effects. Toxicol Appl Pharmacol 189:56–67

    Article  CAS  PubMed  Google Scholar 

  44. Zhang RY, Liu Y, Pang DW, Cai RX, Qi YP (2002) Spectroscopic and voltammetric study on the binding of aluminium (III) to DNA. Anal Sci 18:761–766

    Article  CAS  PubMed  Google Scholar 

  45. Rani A, Kumar A, Lal A, Pant M (2014) Cellular mechanisms of cadmium-induced toxicity: a review. Int J Environ Health Res 24:378–399

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank C. Metton, M.J. Fays-Bernardin, and D. Daioglou for their technical assistance as well as Germetheque for their support.

Author information

Authors and Affiliations

  1. Department of Biology, Faculty of Science and Education Sciences, School of Science, University of Sulaimani, Sulaimani, Kurdistan Region, Iraq

    Sazan Ali

  2. IMBE, UMR CNRS, IRD, Faculté de Médecine, Aix Marseille Université, Avignon Université, Marseille, France

    Sazan Ali, Florence Chaspoul, David Bergé-Lefranc, Vincent Achard, Jeanne Perrin, Philippe Gallice & Marie Guichaoua

  3. Laboratoire de Chimie Physique et Prévention des risques et Nuisances Technologiques, Faculté de Pharmacie, Marseille, France

    Florence Chaspoul, David Bergé-Lefranc & Philippe Gallice

  4. Methodological Assistance Unity for Clinical Research, Department of Public Health, Faculty of Medicine, Marseille, France

    Loundou Anderson

  5. Department of Gynecology Obstetrics and Reproduction (Gynepole), CECOS Laboratory of Biology of Reproduction, AP-HM La Conception University Hospital, Marseille, France

    Vincent Achard & Jeanne Perrin

Authors
  1. Sazan Ali
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Florence Chaspoul
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Loundou Anderson
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. David Bergé-Lefranc
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Vincent Achard
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jeanne Perrin
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Philippe Gallice
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Marie Guichaoua
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Florence Chaspoul.

Ethics declarations

Funding Source and Approval Committee

GERMETHEQUE biobank (France, Marseille University Hospital la Conception) provided all samples and exposure data. In accordance with the 1975 Helsinki Declaration on human experimentation, GERMETHEQUE obtained consent to use each participant’s samples in the human fertility studies. The Germetheque scientific committee approved the study design, and, as a consequence, GERMETHEQUE was validated by the Institutional Review Board (CPP Sud-Ouest and Outremer, n°2-15-27).

The Germetheque sample collection was supported by grants from the ANR (Agence Nationale pour la Recherche), the ABM (Agence de la Biomédecine), the Centre Hospitalier Universitaire de Toulouse, and APHM (Assistance Publique Hôpitaux de Marseille).

Additional information

Sazan Ali and Florence Chaspoul participated equally in this work.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ali, S., Chaspoul, F., Anderson, L. et al. Mapping Fifteen Trace Elements in Human Seminal Plasma and Sperm DNA. Biol Trace Elem Res 175, 244–253 (2017). https://doi.org/10.1007/s12011-016-0772-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12011-016-0772-6

Keywords

Search

Navigation