Ex-vivo assessment of chronic toxicity of low levels of cadmium on testicular meiotic cells

Toxicology and Applied Pharmacology

Volumn 262, Issue 3, 2012, Pages 238-246

  Geoffroy Siraudin, Cendrine ^a,b   Perrard, Marie Hélène ^d   Ghalamoun Slaimi, Rahma ^a,b   Ali, Sazan ^a   Chaspoul, Florence ^a,c   Lanteaume, André ^a   Achard, Vincent ^b   Gallice, Philippe ^a,c   Durand, Philippe ^d   Guichaoua, Marie Roberte ^a,b  

^a FR 3098 Aix Marseille University CNRS   (France)

^b HÔPITAL DE LA CONCEPTION   (France)

^c AIX MARSEILLE UNIVERSITY   (France)

^d UNIVERSITÉ DE LYON   (France)

Author keywords

Cadmium; Culture; Meiosis; Rat; Spermatogenesis; Synaptonemal complex

Indexed keywords

CADMIUM;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL CULTURE; CHRONIC TOXICITY; CLINICAL ASSESSMENT; CONTROLLED STUDY; CULTURE MEDIUM; DOSE RESPONSE; EX VIVO STUDY; FLOW CYTOMETRY; GERM CELL; IMMUNOCYTOCHEMISTRY; MALE; MASS SPECTROMETRY; MEIOTIC PROPHASE I; NONHUMAN; PACHYTENE; PROTEIN FUNCTION; PROTEIN STRUCTURE; QUALITATIVE RESEARCH; RAT; SEMINIFEROUS TUBULE; SERTOLI CELL; SPERMATOCYTE; SPERMATOGENESIS; SPERMATOGONIUM; SYNAPTONEMAL COMPLEX; TESTIS CELL; VALIDATION PROCESS;

ANIMALS; CADMIUM; DOSE-RESPONSE RELATIONSHIP, DRUG; FLOW CYTOMETRY; MALE; MEIOSIS; RATS; RATS, SPRAGUE-DAWLEY; SERTOLI CELLS; SPERMATOGENESIS; TESTIS;

RATTUS;

EID: 84863849829     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2012.04.033     Document Type: Article

References (42)

1. Allen J.W., Gibson J.B., Poorman P.A., Backer L.C., Moses M.J. Synaptonemal complex damage induced by clastogenic and anti-mitotic chemicals, implications for non-disjunction and aneuploidy. Mutat. Res. 1988, 201:313-324.
2. Allen J.W., Poorman P.A., Backer L.C., Gibson J.B., Westbrook-Collins B., Moses M.J. Synaptonemal complex damage as a measure of genotoxicity at meiosis. Cell Biol. Toxicol. 1988, 4:487-494.
3. Angenard G., Muczynski V., Coffigny H., Pairault C., Duquenne C., Frydman R., Habert Rouiier-Fabre V., Livera G. Cadmium increase human fetal germ cell apoptosis. Environ. Health Perspect. 2010, 118:331-337.
4. Backer L.C., Gibson J.B., Allen J.W., Moses M.J. Synaptonemal complex damage in relation to meiotic chromosomes aberrations after exposure of male mice to cyclophosphamide. Mutat. Res. 1988, 203:317-330.
5. Benoff S., Auborn K., Marmar J.L., Hurley I.R. Link between low-dose environmentally relevant cadmium exposures and asthenozoospermia in a rat model. Fertil. Steril. 2008, 89(Suppl. 1):e73-e79.
6. Benoff S., Hauser R., Marmar J.L., Hurley I.R., Napolitano B., Centola G.M. Cadmium concentration in blood and seminal plasma: correlations with sperm number and motility in three male populations (infertility patients, artificial insemination donors, and unselected volunteers). Mol. Med. 2009, 15:248-262.
7. Buck Louis G.M., Sundaram R., Schisterman E.F., Sweeney A.M., Lynch C.D., Gore-Langton R.E., Chen Z., Kim S., Caldwell K.L., Barr D.B. Heavy metals and couple fecundity, the LIFE study. Chemosphere 2012, 87:1201-1207.
8. Chardin B., Dolla A., Chaspoul F., Fardeau M.L., Gallice P., Bruschi M. Bioremediation of chromate: thermodynamic analysis of the effects of Cr(VI) on sulphate reducing bacteria. Appl. Microbiol. Biotechnol. 2002, 60:352-360.
9. Chia S.E., Xu B., Ong C.N., Tsakok F.M., Lee S.T. Effect of cadmium and cigarette smoking on human semen quality. Int. J. Fertil. Menopausal Stud. 1994, 39:292-298.
10. Chung N.P.Y., Cheng C.Y. 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 2001, 142:1878-1888.
11. Fouchécourt S., Godet M., Sabido O., Durand P. Glial cell line-derived-neurotropic factor and its receptors are expressed by germinal and somatic cells of the rat testis. J. Endocrinol. 2006, 190:59-71.
12. Geoffroy-Siraudin C., Perrard M.H., Chaspoul F., Lanteaume A., Gallice P., Durand P., Guichaoua M.R. Validation of a rat seminiferous tubule culture system for studying toxicant impact on meiosis effect of the hexavalent chromium exposure. Toxicol. Sci. 2010, 1:286-296.
13. Geoffroy-Siraudin C., Loundou A.D., Romain F., Achard V., Courbière B., Perrard M.H., Durand P., Guichaoua M.R. Decline of semen quality among 10932 males consulting for couple infertility over a 20years period in Marseille, France. Asian J. Androl. 2012.
14. Godet M., Thomas A., Rudkin B., Durand P. Developmental changes in cyclin B1 and cyclin-dependant kinase (CDK) levels in the different populations of spermatogenic cells of the post-natal rat testis. Eur. J. Cell Biol. 2000, 79:816-823.
15. Godet M., Damestoy A., Mouradian S., Rudkin B., Durand P. Key role for cyclin dependant kinases in the first and second meiotic divisions of rat spermatocytes. Biol. Reprod. 2004, 70:1147-1152.
16. Godet M., Sabido O., Gilleron J., Durand P. Meiotic progression of rat spermatocytes require mitogen-activated kinases of Sertoli cells and close contact between the germ cells and the Sertoli cells. Dev. Biol. 2008, 315:173-188.
17. Gonzalez-Estecha M., Trasobares E., Fuentes M., Martinez M.J., Cano S., Vergera N., Gaspar M.J., Gonzalez-Revalferia J., Barciela M.C., Bugarin Z., Fernandez M.D., Badia P., Pintos C., Gonzalez M., Guillen J.J., Bermejo P., Fernandez C., Aroyo M. Blood lead and cadmium levels in a six hospital employee population. PESA study, 2009. J. Trace Elem. Med. Biol. 2011, 25(Suppl. 1):S22-S29. PESA Group.
18. Goyer R.A., Liu J., Waalkes M.P. Cadmium and cancer of prostate and testis. BioMetals 2004, 17:555-558.
19. Guichaoua M.R., Perrin J., Metzler-Guillemain C., Saias-Magnan J., Giorgi R., Grillo J.M. Meiotic anomalies in infertile men with a severe defect in spermatogenesis. Hum. Reprod. 2005, 20:1897-1902.
20. Hassler E., Lind B., Piscator M. Cadmium in blood and urine related to present and past exposure. A study of workers in an alkaline battery factory. Br. J. Ind. Med. 1983, 13:420-425.
21. Hue D., Staub C., Perrard-Sapori M.H., Weiss M., Nicolle J.C., Vigier M., Durand P. Meiotic differentiation of meiotic cells in three-week cultures of whole cell population from rat seminiferous tubules. Biol. Reprod. 1998, 59:379-387.
22. Järup l, Åkesson A. Current status of cadmium as an environmental health problem. Toxicol. Appl. Pharmacol. 2009, 238:201-208.
23. Keeney S., Giroux C.N., Kleckner N. Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family. Cell 1997, 88:375-384.
24. Kim N.S., Lee B.K. National estimates of blood lead, cadmium, and mercury levels in the Korean general adult population. Int. Arch. Occup. Environ. Health 2011, 84:53-63.
25. Kim H., Lee H.J., Hwang J.Y., Ha E.H., Park H., Ha M., Kim J.H., Hong Y.C., Chang N. Blood cadmium concentrations of male cigarette smokers are inversely associated with fruit consumption. J. Nutr. 2010, 140:1133-1138.
26. Kriegel A.M., Soliman A.S., Zhang Q., El-Ghawalby N., Ezzat F., Soultan A., Abdel-Wahab M., Fathy O., Ebidi G., Bassiouni N., Hamilton S.R., Abbruzzese J.L., Lacey M.R., Blake D.A. Serum cadmium levels in pancreatic cancer patients from the east Nile Delta region of Egypt. Environ. Health Perspect. 2006, 114:113-119.
27. Martin M.B., Voeller H.J., Gelmann E.P., Lu J., Stoica E.G., Hebert E.J., Reiter R., Singh B., Danielsen M., Pentecost E., Stoica A. Role of cadmium in the regulation of AR gene expression and activity. Endocrinology 2002, 143:263-275.
28. Mendiola J., Moreno J.M., Roca M., Vegara-Juarez N., Martinez-Garcia M.J., Garcia-Sanchez A., Elvira-Rendueles B., Moreno-Grao S., Lopez-Espin J., Ten J., Bernabeu R., Torres-Cantero A.M. Relationships between heavy metals concentrations in three different body fluids and male reroductive parameters: a pilot study. Environ. Health 2011, 10:6-12.
29. Metzler-Guillemain C., Guichaoua M.R. A simple and reliable method for meiotic studies on testicular samples used for intracytoplasmic sperm injection. Fertil. Steril. 2000, 74:916-919.
30. Nunes J.A., Batista B.L., Rodrigues J.L., Caldas N.M., Barbosa J.R. A simple method based on ICP-MS for estimation of background levels of arsenic, cadmium, copper, manganese, nickel, lead, and selenium in blood of the Brazilian population. J. Toxicol. Environ. Health 2010, 73:878-887.
31. Page S.L., Hawley S. The genetics and molecular biology of the synaptonemal complex. Annu. Rev. Cell Dev. Biol. 2004, 20:525-558.
32. Perrard M.H., Hue D., Staub C., Le Vern Y., Kerboeuf D., Durand P. Development of the meiotic step in testes of pubertal rats/comparison between the in vivo situation and under in vitro conditions. Mol. Reprod. Dev. 2003, 65:86-95.
33. Perrard M.H., Prisant N., Geoffroy-Siraudin C., Segretain D., Pointis G., Guichaoua M.R., Durand P. Analysis of the intratesticular control of spermatogenesis by ex-vivo approaching. Folia Histochem. Cytobiol. 2009, 47:S89-S94.
34. Perrard M.H., Grenet C., Prisant N., Geoffroy-Siraudin C., Segretain D., Pointis G., Guichaoua M.R., Durand P. European regulation REACH and the assessment of testicular toxicity. Med. Sci. 2010, 26:305-310.
35. Siu E.R., Mruk D.D., Porto C., Cheng C.Y. Cadmium-induced testicular injury. Toxicol. Appl. Pharmacol. 2009, 238:240-249.
36. Staub C., Hue D., Nicolle J.C., Perrard-Sapori M.H., Segretain Durand P. The whole meiotic process can occur ex vivo in untransformed rat spermatogenic cells. Exp. Cell Res. 2000, 260:85-95.
37. Stoica A., Katzellenbogen B.S., Martin M.B. Activation of estrogen receptor-α by heavy metal cadmium. Mol. Endocrinol. 2000, 14:545-553.
38. Tassistro V., Ghalamoun R., Saias-Magnan J., Guichaoua M.R. Meiosis in normal and abnormal spermatogenesis, a new index to evaluate spermatogenesis. Indian J. Med. Res. 2009, 129:268-278.
39. Thompson J., Bannigan J. Cadmium: toxic effects on the reproductive system and the embryo. Reprod. Toxicol. 2008, 25:304-315.
40. World Health Organization (WHO) Exposure to cadmium: a major public health concern. Provisional tolerable monthly intake (PTMI) 2010.
41. Yu X., Sidhu J.S., hong S., Fautsman E.M. Essential role of extracellular matrix (ECM) overlay in establishing the functional integrity of primary neonatal rat Sertoli cell/gonocyte co-culture: an improved in vitro model for assessment of male reproductive toxicity. Toxicol. Sci. 2005, 84:378-393.
42. Yu X., Hong S., Faustman M. Cadmium-induced activation of stress signaling pathways, disruption of Ubiquitin-dependent protein degradation and apoptosis in primary rat Sertoli cell-gonocytes coculture. Toxicol. Sci. 2008, 104:385-396.