Sub-acute intravenous administration of silver nanoparticles in male mice alters Leydig cell function and testosterone levels

Reproductive Toxicology

Volumn 45, Issue , 2014, Pages 59-70

  Garcia, Thomas X ^a,b   Costa, Guilherme M J ^c   França, Luiz R ^c   Hofmann, Marie Claude ^a,b  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^c FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

Author keywords

Fertility; Reproductive toxicity; Spermatogenesis; Testis

Indexed keywords

3 BETA-HYDROXYSTEROID OXIDOREDUCTASE-DELTA(5) 3-KETOSTEROID ISOMERASE; 3BETA HYDROXY DELTA5 STEROID DEHYDROGENASE; CHOLESTEROL MONOOXYGENASE (SIDE CHAIN CLEAVING); MESSENGER RNA; METAL NANOPARTICLE; MULTIENZYME COMPLEX; SILVER; STEROID DELTA ISOMERASE; TESTOSTERONE;

ANIMAL; BLOOD; DRUG EFFECTS; FEMALE; GENE EXPRESSION; GENETICS; INTRAVENOUS DRUG ADMINISTRATION; MALE; METABOLISM; MOUSE; PATHOLOGY; TESTIS; TOXICITY; TOXICITY TESTING;

ADMINISTRATION, INTRAVENOUS; ANIMALS; CHOLESTEROL SIDE-CHAIN CLEAVAGE ENZYME; FEMALE; GENE EXPRESSION; MALE; METAL NANOPARTICLES; MICE; MULTIENZYME COMPLEXES; PROGESTERONE REDUCTASE; RNA, MESSENGER; SILVER; STEROID ISOMERASES; TESTIS; TESTOSTERONE; TOXICITY TESTS, SUBACUTE;

EID: 84893506553     PISSN: 08906238     EISSN: 18731708     Source Type: Journal    
DOI: 10.1016/j.reprotox.2014.01.006     Document Type: Article

References (57)

1. Pryor J.L., Hughes C., Foster W., Hales B.F., Robaire B. Critical windows of exposure for children's health: the reproductive system in animals and humans. Environ Health Perspect 2000, 108(Suppl. 3):491-503.
2. Lucas B., Fields C., Hofmann M.C. Signaling pathways in spermatogonial stem cells and their disruption by toxicants. Birth Defects Res C Embryo Today 2009, 87:35-42.
3. Lucas B.E., Fields C., Joshi N., Hofmann M.C. Mono-(2-ethylhexyl)-phthalate (MEHP) affects ERK-dependent GDNF signalling in mouse stem-progenitor spermatogonia. Toxicology 2012, 299:10-19.
4. Kashiwada S. Distribution of nanoparticles in the see-through medaka (Oryzias latipes). Environ Health Perspect 2006, 114:1697-1702.
5. Kim J.S., Yoon T.J., Yu K.N., Kim B.G., Park S.J., Kim H.W., et al. Toxicity and tissue distribution of magnetic nanoparticles in mice. Toxicol Sci 2006, 89:338-347.
6. Oberdorster G. Safety assessment for nanotechnology and nanomedicine: concepts of nanotoxicology. J Intern Med 2010, 267:89-105.
7. De Jong W.H., Borm P.J. Drug delivery and nanoparticles: applications and hazards. Int J Nanomed 2008, 3:133-149.
8. Kwon J.T., Hwang S.K., Jin H., Kim D.S., Minai-Tehrani A., Yoon H.J., et al. Body distribution of inhaled fluorescent magnetic nanoparticles in the mice. J Occup Health 2008, 50:1-6.
9. Sharma H.S., Hussain S., Schlager J., Ali S.F., Sharma A. Influence of nanoparticles on blood-brain barrier permeability and brain edema formation in rats. Acta Neurochir Suppl 2010, 106:359-364.
10. Jain J., Arora S., Rajwade J.M., Omray P., Khandelwal S., Paknikar K.M. Silver nanoparticles in therapeutics: development of an antimicrobial gel formulation for topical use. Mol Pharm 2009, 6:1388-1401.
11. Park E.J., Yi J., Kim Y., Choi K., Park K. Silver nanoparticles induce cytotoxicity by a Trojan-horse type mechanism. Toxicol In Vitro 2010, 24:872-878.
12. Ahamed M., Karns M., Goodson M., Rowe J., Hussain S.M., Schlager J.J., et al. DNA damage response to different surface chemistry of silver nanoparticles in mammalian cells. Toxicol Appl Pharmacol 2008, 233:404-410.
13. Carlson C., Hussain S.M., Schrand A.M., Braydich-Stolle L.K., Hess K.L., Jones R.L., et al. Unique cellular interaction of silver nanoparticles: size-dependent generation of reactive oxygen species. J Phys Chem B 2008, 112:13608-13619.
14. Ahamed M., Posgai R., Gorey T.J., Nielsen M., Hussain S.M., Rowe J.J. Silver nanoparticles induced heat shock protein 70, oxidative stress and apoptosis in Drosophila melanogaster. Toxicol Appl Pharmacol 2010, 242:263-269.
15. Asharani P.V., Hande M.P., Valiyaveettil S. Anti-proliferative activity of silver nanoparticles. BMC Cell Biol 2009, 10:65.
16. Asharani P.V., Low Kah Mun G., Hande M.P., Valiyaveettil S. Cytotoxicity and genotoxicity of silver nanoparticles in human cells. ACS Nano 2009, 3:279-290.
17. Cha K., Hong H.W., Choi Y.G., Lee M.J., Park J.H., Chae H.K., et al. Comparison of acute responses of mice livers to short-term exposure to nano-sized or micro-sized silver particles. Biotechnol Lett 2008, 30:1893-1899.
18. Sung J.H., Ji J.H., Yoon J.U., Kim D.S., Song M.Y., Jeong J., et al. Lung function changes in Sprague-Dawley rats after prolonged inhalation exposure to silver nanoparticles. Inhal Toxicol 2008, 20:567-574.
19. Kim Y.S., Song M.Y., Park J.D., Song K.S., Ryu H.R., Chung Y.H., et al. Subchronic oral toxicity of silver nanoparticles. Part Fibre Toxicol 2010, 7:20.
20. Park E.J., Bae E., Yi J., Kim Y., Choi K., Lee S.H., et al. Repeated-dose toxicity and inflammatory responses in mice by oral administration of silver nanoparticles. Environ Toxicol Pharmacol 2010, 30:162-168.
21. Lee Y., Kim P., Yoon J., Lee B., Choi K., Kil K.H., et al. Serum kinetics, distribution and excretion of silver in rabbits following 28 days after a single intravenous injection of silver nanoparticles. Nanotoxicology 2013, 7:1120-1130.
22. Braydich-Stolle L., Hussain S., Schlager J.J., Hofmann M.C. In vitro cytotoxicity of nanoparticles in mammalian germline stem cells. Toxicol Sci 2005, 88:412-419.
23. Braydich-Stolle L.K., Lucas B., Schrand A., Murdock R.C., Lee T., Schlager J.J., et al. Silver nanoparticles disrupt GDNF/Fyn kinase signaling in spermatogonial stem cells. Toxicol Sci 2010, 116:577-589.
24. Hofmann M.C., Braydich-Stolle L., Dettin L., Johnson E., Dym M. Immortalization of mouse germ line stem cells. Stem Cells 2005, 23:200-210.
25. Bai Y., Zhang Y., Zhang J., Mu Q., Zhang W., Butch E.R., et al. Repeated administrations of carbon nanotubes in male mice cause reversible testis damage without affecting fertility. Nat Nanotechnol 2010, 5:683-689.
26. De Jong W.H., Hagens W.I., Krystek P., Burger M.C., Sips A.J., Geertsma R.E. Particle size-dependent organ distribution of gold nanoparticles after intravenous administration. Biomaterials 2008, 29:1912-1919.
27. Li C., Taneda S., Taya K., Watanabe G., Li X., Fujitani Y., et al. Effects of inhaled nanoparticle-rich diesel exhaust on regulation of testicular function in adult male rats. Inhal Toxicol 2009, 21:803-811.
28. Yoshida S., Hiyoshi K., Ichinose T., Takano H., Oshio S., Sugawara I., et al. Effect of nanoparticles on the male reproductive system of mice. Int J Androl 2009, 32:337-342.
29. Costa G.M., Leal M.C., Ferreira C.S., Guimaraes D.A., Franca L.R. Duration of spermatogenesis and spermatogenic efficiency in 2 large neotropical rodent species: the agouti (Dasyprocta leporina) and paca (Agouti paca). J Androl 2010, 31:489-499.
30. Rodriguez-Sosa J.R., Costa G.M., Rathi R., Franca L.R., Dobrinski I. Endocrine modulation of the recipient environment affects development of bovine testis tissue ectopically grafted in mice. Reproduction 2012, 144:37-51.
31. Burnett L.A., Blais E.M., Unadkat J.D., Hille B., Tilley S.L., Babcock D.F. Testicular expression of Adora3i2 in Adora3 knockout mice reveals a role of mouse A3Ri2 and human A3Ri3 adenosine receptors in sperm. J Biol Chem 2010, 285:33662-33670.
32. Haavisto A.M., Pettersson K., Bergendahl M., Perheentupa A., Roser J.F., Huhtaniemi I. A supersensitive immunofluorometric assay for rat luteinizing hormone. Endocrinology 1993, 132:1687-1691.
33. Gay V.L., Midgley A.R., Niswender G.D. Patterns of gonadotrophin secretion associated with ovulation. Fed Proc 1970, 29:1880-1887.
34. Xu Y.P., Chedrese P.J., Thacker P.A. Growth hormone amplifies insulin-like growth factor I induced progesterone accumulation and P450scc mRNA expression. Mol Cell Endocrinol 1995, 111:199-206.
35. Wang G.M., O'Shaughnessy P.J., Chubb C., Robaire B., Hardy M.P. Effects of insulin-like growth factor I on steroidogenic enzyme expression levels in mouse leydig cells. Endocrinology 2003, 144:5058-5064.
36. Eacker S.M., Agrawal N., Qian K., Dichek H.L., Gong E.Y., Lee K., et al. Hormonal regulation of testicular steroid and cholesterol homeostasis. Mol Endocrinol 2008, 22:623-635.
37. Stocco D.M., Clark B.J. Role of the steroidogenic acute regulatory protein (StAR) in steroidogenesis. Biochem Pharmacol 1996, 51:197-205.
38. Papadopoulos V., Baraldi M., Guilarte T.R., Knudsen T.B., Lacapere J.J., Lindemann P., et al. Translocator protein (18kDa): new nomenclature for the peripheral-type benzodiazepine receptor based on its structure and molecular function. Trends Pharmacol Sci 2006, 27:402-409.
39. Payne A.H., Hales D.B. Overview of steroidogenic enzymes in the pathway from cholesterol to active steroid hormones. Endocr Rev 2004, 25:947-970.
40. Bucci L.R., Meistrich M.L. Effects of busulfan on murine spermatogenesis: cytotoxicity, sterility, sperm abnormalities, and dominant lethal mutations. Mutat Res 1987, 176:259-268.
41. Zohni K., Zhang X., Tan S.L., Chan P., Nagano M.C. The efficiency of male fertility restoration is dependent on the recovery kinetics of spermatogonial stem cells after cytotoxic treatment with busulfan in mice. Hum Reprod 2012, 27:44-53.
42. Sung J.H., Ji J.H., Park J.D., Yoon J.U., Kim D.S., Jeon K.S., et al. Subchronic inhalation toxicity of silver nanoparticles. Toxicol Sci 2009, 108:452-461.
43. Gromadzka-Ostrowska J., Dziendzikowska K., Lankoff A., Dobrzynska M., Instanes C., Brunborg G., et al. Silver nanoparticles effects on epididymal sperm in rats. Toxicol Lett 2012.
44. Yeung B.H., Wan H.T., Law A.Y., Wong C.K. Endocrine disrupting chemicals: multiple effects on testicular signaling and spermatogenesis. Spermatogenesis 2011, 1:231-239.
45. Lehmann K.P., Phillips S., Sar M., Foster P.M., Gaido K.W. Dose-dependent alterations in gene expression and testosterone synthesis in the fetal testes of male rats exposed to di (n-butyl) phthalate. Toxicol Sci 2004, 81:60-68.
46. Naciff J.M., Hess K.A., Overmann G.J., Torontali S.M., Carr G.J., Tiesman J.P., et al. Gene expression changes induced in the testis by transplacental exposure to high and low doses of 17{alpha}-ethynyl estradiol, genistein, or bisphenol A. Toxicol Sci 2005, 86:396-416.
47. Ferrara D., Hallmark N., Scott H., Brown R., McKinnell C., Mahood I.K., et al. Acute and long-term effects of in utero exposure of rats to di(n-butyl) phthalate on testicular germ cell development and proliferation. Endocrinology 2006, 147:5352-5362.
48. Ryu J.Y., Lee B.M., Kacew S., Kim H.S. Identification of differentially expressed genes in the testis of Sprague-Dawley rats treated with di(n-butyl) phthalate. Toxicology 2007, 234:103-112.
49. Heller C.G., Leach D.R. Quantification of Leydig cells and measurement of Leydig-cell size following administration of human chorionic gonadotrophin to normal men. J Reprod Fert 1971, 25:185-192.
50. Ramdhan D.H., Ito Y., Yanagiba Y., Yamagishi N., Hayashi Y., Li C., et al. Nanoparticle-rich diesel exhaust may disrupt testosterone biosynthesis and metabolism via growth hormone. Toxicol Lett 2009, 191:103-108.
51. Midzak A., Rone M., Aghazadeh Y., Culty M., Papadopoulos V. Mitochondrial protein import and the genesis of steroidogenic mitochondria. Mol Cell Endocrinol 2011, 336:70-79.
52. Manna P.R., Dyson M.T., Stocco D.M. Regulation of the steroidogenic acute regulatory protein gene expression: present and future perspectives. Mol Hum Reprod 2009, 15:321-333.
53. Arakane F., King S.R., Du Y., Kallen C.B., Walsh L.P., Watari H., et al. Phosphorylation of steroidogenic acute regulatory protein (StAR) modulates its steroidogenic activity. J Biol Chem 1997, 272:32656-32662.
54. Shaw N.D., Butler J.P., McKinney S.M., Nelson S.A., Ellenbogen J.M., Hall J.E. Insights into puberty: the relationship between sleep stages and pulsatile LH secretion. J Clin Endocrinol Metab 2012, 97:E2055-E2062.
55. Loeschner K., Hadrup N., Qvortrup K., Larsen A., Gao X., Vogel U., et al. Distribution of silver in rats following 28 days of repeated oral exposure to silver nanoparticles or silver acetate. Part Fibre Toxicol 2011, 8:18.
56. Xiu Z.M., Zhang Q.B., Puppala H.L., Colvin V.L., Alvarez P.J. Negligible particle-specific antibacterial activity of silver nanoparticles. Nano Lett 2012, 12:4271-4275.
57. Shetty G., Weng C.C., Meachem S.J., Bolden-Tiller O.U., Zhang Z., Pakarinen P., et al. Both testosterone and follicle-stimulating hormone independently inhibit spermatogonial differentiation in irradiated rats. Endocrinology 2006, 147:472-482.