Effects of Fusarium mycotoxins on steroid production by porcine granulosa cells

Animal Reproduction Science

Volumn 107, Issue 1-2, 2008, Pages 115-130

  Ranzenigo, Giovanni ^a   Caloni, Francesca ^a   Cremonesi, Fausto ^a   Aad, Pauline Y ^b   Spicer, Leon J ^b  

^a UNIVERSITY OF MILAN   (Italy)

^b OKLAHOMA STATE UNIVERSITY   (United States)

Author keywords

Gene expression; Granulosa cells; Mycotoxins; Steroid production; Swine

Indexed keywords

CHOLESTEROL MONOOXYGENASE (SIDE CHAIN CLEAVING); CYTOCHROME P450 1A1; DRUG DERIVATIVE; FOLLITROPIN; MESSENGER RNA; SOMATOMEDIN C; STEROID; TRICHOTHECENE DERIVATIVE; VOMITOXIN; ZEARALENOL; ZERANOL;

ANIMAL; ARTICLE; BIOSYNTHESIS; CELL CULTURE; CELL PROLIFERATION; DRUG EFFECT; FEMALE; FUSARIUM; GENE EXPRESSION REGULATION; GENETICS; GRANULOSA CELL; METABOLISM; SWINE;

ANIMALS; CELL PROLIFERATION; CELLS, CULTURED; CHOLESTEROL SIDE-CHAIN CLEAVAGE ENZYME; CYTOCHROME P-450 CYP1A1; FEMALE; FOLLICLE STIMULATING HORMONE; FUSARIUM; GENE EXPRESSION REGULATION; GRANULOSA CELLS; INSULIN-LIKE GROWTH FACTOR I; RNA, MESSENGER; STEROIDS; SWINE; TRICHOTHECENES; ZERANOL;

BOVINAE; FUSARIUM; SUIDAE; SUS;

EID: 43849112466     PISSN: 03784320     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.anireprosci.2007.06.023     Document Type: Article

References (58)

1. Aad P.Y., Voge J.L., Santiago C.A., Malayer J.R., and Spicer L.J. Real-Time RT-PCR Quantification of pregnancy-associated plasma protein-A mRNA abundance in bovine granulosa and theca cells: effects of hormones in vitro. Domest. Anim. Endocrinol. 31 (2006) 357-372
2. Adashi E.Y., and Hsueh A.J. Estrogens augment the stimulation of ovarian aromatase activity by follicle-stimulating hormone in cultured rat granulosa ccells. J. Biol. Chem. 257 (1982) 6077-6083
3. Alm H., Brussow K.P., Torner H., Vanselow J., Tomek W., Danicke S., and Tiemann U. Influence of Fusarium-toxin contaminated feed on initial quality and meiotic competence of gilt oocytes. Reprod. Toxicol. 22 (2006) 44-50
4. Alm H., Greising T., Brüssow K.-P., Torner H., and Tiemann U. The influence of the mycotoxins deoxynivalenol and zearalenol on in vitro maturation of pig oocytes and in vitro culture of pig zygotes. Toxicol. In Vitro 16 (2002) 643-648
5. Baranao J.L., and Hammond J.M. Comparative effects of insulin and insulin-like growth factors on DNA synthesis and differentiation of porcine granulosa cells. Biochem. Biophys. Res. Commun. 124 (1984) 484-490
6. Chan W.K., and Tan C.H. Aminoglutethimide augments follicle-stimulating hormone-induced aromatase activity in cultured porcine granulosa cells. Endocrinology 122 (1988) 2290-2298
7. Charoenpornsook K., Fitzpatrick J.L., and Smith J.E. The effects of four mycotoxins on the mitogen stimulated proliferation of bovine peripheral blood mononuclear cells in vitro. Mycopathologia 143 (1998) 105-111
8. Collins B.M., McLachlan J.A., and Arnold S.F. The estrogenic and antiestrogenic activities of phytochemicals with the human estrogen receptor expressed in yeast. Steroids 62 (1997) 365-372
9. Coulombe R.A. Biological action of mycotoxins. J. Dairy Sci. 76 (1993) 880-891
10. Danicke S., Valenta H., and Doll S. On the toxicokinetics and the metabolism of deoxynivalenol (DON) in the pig. Arch. Anim. Nutr. 58 (2004) 169-180
11. Diekman M.A., and Green M.L. Mycotoxins and reproduction in domestic livestock. J. Anim. Sci. 70 (1992) 1615-1627
12. D'Mello J.P.F., Placinta C.M., and Macdonald A.M.C. Fusarium mycotoxins, a review of global implications for animal health, welfare and productivity. Anim. Feed Sci. Technol. 80 (1999) 183-205
13. Drochner W., Schollenberger M., Gotz S., Lauber U., Tafaj M., and Piepho H.P. Subacute effects of moderate feed loads of isolated Fusarium toxin deoxynivalenol on selected parameters of metabolism in weaned growing piglets. J. Anim. Physiol. Anim. Nutr. (Berl.) 90 (2006) 421-428
14. Fanjul L.F., Ruiz de Galarreta C.M., and Hsueh A.J. Estrogen regulation of progestin biosynthetic enzymes in cultured rat granulosa cells. Biol. Reprod. 30 (1984) 903-912
15. Fitzpatrick D.W., Picken C.A., Murphy L.C., and Buhr M.M. Measurement of the relative binding affinity of zearalenone, α-zearalenol and β-zearalenol for uterine and oviduct estrogen receptors in swine, rats and chickens: an indicator of estrogenic potencies. Comp. Biochem. Physiol. C 94 (1989) 691-694
16. Glávits R., Sandor G., Vanyi A., and Gajdacs G. Reproductive disorders caused by trichotechene myctoxins in a large scale pig herd. Acta Vet. Hung. 31 (1983) 173-181
17. Goyarts T., and Danicke S. Bioavailability of the Fusarium toxin deoxynivalenol (DON) from naturally contaminated wheat for the pig. Toxicol. Lett. 163 (2006) 171-182
18. Hammond J.M., and English H.F. Regulation of deoxyribonucleic acid synthesis in cultured porcine granulosa cells by growth factors and hormones. Endocrinology 120 (1987) 1039-1046
19. Keel B.A., Eddy K.B., He Y., Gangrade B.K., and May J.V. Purified human α-fetoprotein inhibits follicle-stimulating hormone-stimulated estradiol production by porcine granulosa cells in culture. Mol. Cell. Endocrinol. 94 (1993) 21-25
20. Krazeisen A., Breitling R., Moller G., and Adamski J. Phytoestrogens inhibit human 17β-hydroxysteroid dehydrogenase type 5. Mol. Cell. Endocrinol. 171 (2001) 151-162
21. Kumagai S., and Shimizu T. Neonatal exposure to zearalenone causes persistent anovulatory estrus in the rat. Arch. Toxicol. 50 (1982) 279-286
22. Langhout D.J., Spicer L.J., and Geisert R.D. Development of a culture system for bovine granulosa cells: effects of growth hormone, estradiol, and gonadotropins on cell proliferation, steroidogenesis, and protein synthesis. J. Anim. Sci. 69 (1991) 3321-3334
23. Larsen J.C., Hunt J., Perrin I., and Ruckenbauer P. Workshop on trichothecenes with a focus on DON: summary report. Toxicol. Lett. 153 (2004) 1-22
24. LaVoie H.A., Garmey J.C., Day R.N., and Veldhuis J.D. Concerted regulation of low density lipoprotein receptor gene expression by follicle-stimulating hormone and insulin-like growth factor I in porcine granulosa cells: promoter activation, messenger ribonucleic acid stability, and sterol feedback. Endocrinology 140 (1999) 178-186
25. Long G.G., Diekman M., Tuite J.F., Shannon G.M., and Vesonder R.F. Effect of Fusarium roseum corn culture containing zearalenone on early pregnancy in swine. Am. J. Vet. Res. 43 (1982) 1599-1603
26. Maitra A., LaVoie H.A., Day R.N., Garmey J.C., and Veldhuis J.D. Regulation of porcine granulosa cell 3-hydroxy-3-methylglutaryl coenzyme A reductase by insulin and insulin-like growth factor I: synergism with follicle-stimulating hormone or protein kinase A agonist. Endocrinology 136 (1995) 5111-5117
27. Makela S., Poutanen M., Lehtimaki J., Kostian M.L., Santti R., and Vihko R. Estrogen-specific 17β-hydroxysteroid oxidoreductase type 1 (E.C. 1.1.1.62) as a possible target for the action of phytoestrogens. Proc. Soc. Exp. Biol. Med. 208 (1995) 51-59
28. Malekinejad H., Van Tol H.T., Colenbrander B., and Fink-Gremmels J. Expression of 3α- and 3β-hydroxy steroid dehydrogenase mRNA in COCs and granulosa cells determines zearalenone biotransformation. Toxicol. In Vitro 20 (2006) 458-463
29. Miksicek R.J. Interaction of naturally occurring nonsteroidal estrogens with expressed recombinant human estrogen receptor. J. Steroid. Biochem. Mol. Biol. 49 (1994) 153-160
30. Minervini F., Del'Aquila M.E., Maritano P., Minoia P., and Visconti A. Toxic effects of the mycotoxin zearalenone and its derivatives on in vitro maturation of bovine oocytes and 17β-estradiol levels in mural granulosa cell cultures. Toxicol. In Vitro 15 (2001) 489-495
31. Minervini F., Fornelli F., and Flynn K.M. Toxicity and apoptosis induced by the mycotoxins nivalenol, deoxynivalenol and fumonisin B1 in a human erythroleukemia cell line. Toxicol. In Vitro 18 (2004) 21-28
32. Minervini F., Giannoccaro A., Cavallini A., and Visconti A. Investigations on cellular proliferation induced by zearalenone and its derivatives in relation to the estrogenic parameters. Toxicol. Lett. 159 (2005) 272-283
33. Minegishi T., Hirakawa T., Kishi H., Abe K., Abe Y., Mizutani T., and Miyamoto K. A role of insulin-like growth factor I for follicle-stimulating hormone receptor expression in rat granulosa cells. Biol. Reprod. 62 (2000) 325-333
34. Olsen M., Malmlof K., Pettersson H., Sandholm K., and Kiessling K.H. Plasma and urinary levels of zearalenone and α-zearalenol in a prepubertal gilt fed zearalenone. Acta Pharmacol. Toxicol. 56 (1985) 239-243
35. Ott L. Multiple comparisons. An Introduction to Statistical Methods and Data Analysis (1977), Duxbury Press, North Scituate, MA pp. 384-388
36. Park J.J., Smalley E.B., and Chu F.S. Natural occurrence of Fusarium mycotoxins in field samples from the 1992 Wisconsin corn crop. Appl. Envir. Microbiol. 62 (1996) 1642-1648
37. Picton H.M., Campbell B.K., and Hunter M.G. Maintenance of oestradiol production and expression of cytochrome P450 aromatase enzyme mRNA in long-term serum-free cultures of pig granulosa cells. J. Reprod. Fertil. 115 (1999) 67-77
38. SAS. The SAS System for Windows: Version 8 (1999), SAS Institute Inc., Cary, NC
39. Schollenberger M., Muller H.M., Rufle M., Terry-Jara H., Suchy S., Plank S., and Drochner W. Natural occurrence of Fusarium toxins in soy food marketed in Germany. Int. J. Food Microbiol. 113 (2007) 142-146
40. Skorska-Wyszynska E., Jakimiuk E., Gajecka M., Mlynarczuk J., Obremski K., and Gajecki M. Preliminary evaluation of influence of zearalenone on cocultures of granulosa and internal theca cells of ovarian follicles in bitches in in vitro culture. Pol. J. Vet. Sci. 7 (2004) 305-309
41. Spicer L.J., and Aad P.Y. Insulin-like growth gactor (IGF) 2 stimulates steroidogenesis and mitosis of bovine granulosa cells through the IGF1 receptor: role of follicle-stimulating hormone and IGF2 receptor. Biol. Reprod. 77 (2007) 18-27
42. Spicer L.J., Alpizar E., and Echternkamp S.E. Effects of insulin, insulin-like growth factor I, and gonadotropins on bovine granulosa cell proliferation, progesterone production, Estradiol production, and (or) insulin-like growth factor I production in vitro. J. Anim. Sci. 71 (1993) 1232-1241
43. Spicer L.J., and Chamberlain C.S. Influence of cortisol on insulin- and insulin-like growth factor 1 (IGF-I)-induced steroid production and on IGF-I receptors in cultured bovine granulosa cells and thecal cells. Endocrine 9 (1998) 153-161
44. Spicer L.J., Chamberlain C.S., and Maciel S.M. Influence of gonadotropins on insulin- and insulin-like growth factor-I (IGF-I)-induced steroid production by bovine granulosa cells. Domest. Anim. Endocrinol. 22 (2002) 237-254
45. Spicer L.J., and Hammond J.M. 2-Hydroxyestradiol modulates a facilitative action of catecholamines on porcine granulosa cells. Endocrinology 120 (1987) 2375-2382
46. Spicer L.J., and Hammond J.M. Catecholestrogens inhibit proliferation and DNA synthesis of porcine granulosa cells in vitro: comparison with estradiol, 5 α-dihydrotestosterone, gonadotropins and catecholamines. Mol. Cell. Endocrinol. 64 (1989) 119-126
47. Spicer L.J., Kao L.C., Strauss III J.F., and Hammond J.M. 2-Hydroxyestradiol enhanced progesterone production by porcine granulosa cells: dependence on de novo cholesterol synthesis and stimulation of cholesterol side-chain cleavage activity and cytochrome P450scc messenger ribonucleic acid levels. Endocrinology 127 (1990) 2763-2770
48. Sundstol Eriksen G., Pettersson H., and Lundh T. Comparative cytotoxicity of deoxynivalenol, nivalenol, their acetylated dervatives and de-epoxy metabolites. Food Chem. Toxicol. 42 (2004) 69-624
49. Tiemann U., Tomek W., Schneider F., and Vanselow J. Effects of the mycotoxins α- and β-zearalenol on regulation of progesterone synthesis in cultured granulosa cells from porcine ovaries. Reprod. Toxicol. 17 (2003) 673-681
50. Veldhuis J.D., and Demers L.M. A role for somatomedin C as a differentiating hormone and amplifier of hormone action on ovarian cells: studies with synthetically pure human somatomedin C and swine granulosa cells. Biochem. Biophys. Res. Commun. 130 (1985) 234-240
51. Veldhuis J.D., and Rodgers R.J. Mechanisms subserving the steroidogenic synergism between follicle-stimulating hormone and insulin-like growth factor I (somatomedin C). Alterations in cellular sterol metabolism in swine granulosa cells. J. Biol. Chem. 262 (1987) 7658-7664
52. Voge J.L., Santiago C.A., Aad P.Y., Goad D.W., Malayer J.R., and Spicer L.J. Effect of insulin like growth factors (IGF), FSH, and leptin on IGF-binding-protein mRNA expression in bovine granulosa and theca cells: quantitative detection by real-time PCR. Peptides 25 (2004) 2195-2203
53. Whitehead S.A., and Lacey M. Phytoestrogens inhibit aromatase but not 17β-hydroxysteroid dehydrogenase (HSD) type 1 in human granulosa-luteal cells: evidence for FSH induction of 17β-HSD. Hum. Reprod. 18 (2003) 487-494
54. Yasuda K., Fukuoka M., Taii S., Takakura K., and Mori T. Inhibitory effects of interleukin-1 on follicle-stimulating hormone induction of aromatase activity, progesterone secretion, and functional luteinizing hormone receptors in cultures of porcine granulosa cells. Biol. Reprod. 43 (1990) 905-912
55. Young L.G., Ping H., and King G.J. Effects of feeding zearalenone to sows on rebreeding and pregnancy. J. Anim. Sci. 68 (1990) 15-20
56. Zhou J., Kumar T.R., Matzuk M.M., and Bondy C. Insulin-like growth factor I regulates gonadotropin responsiveness in the murine ovary. Mol. Endocrinol. 11 (1997) 1924-1933
57. Zwierzchowski W., Obremski K., Zielonka L., Skorska-Wyszynska E., Gajecka M., Jakimiuk E., Polak M., Jana B., Rybarczyk L., and Gajecki M. The impact of zearalenone on the level of the selected estrogens in blood serum of sexually immature gilts. Pol. J. Vet. Sci. 9 (2006) 247-252
58. Zwierzchowski W., Przybylowicz M., Obremski K., Zielonka L., Skorska-Wyszynska E., Gajecka M., Polak M., Jakimiuk E., Jana B., Rybarczyk L., and Gajecki M. Level of zearalenone in blood serum and lesions in ovarian follicles of sexually immature gilts in the course of zearalenone micotoxicosis. Pol. J. Vet. Sci. 8 (2005) 209-218