The effect of PCB126, 77, and 153 on the intracellular mobilization of Caplus 2 in bovine granulosa and luteal cells after FSH and LH surge in vitro

• Autorzy: Mlynarczuk J. , Kowalik M.
• Języki publikacji: EN

Abstrakty

EN

Polychlorinated biphenyls (PCBs) are a group of persistent environmental pollutants that impair cattle reproduction. Among other effects, PCBs can disturb the intracellular mobilization of Ca²⁺ in several cell types. Hence, it is possible that they disrupt the transduction of intracellular signals generated from gonadotropin (FSH/LH) receptors. In steroidogenic ovarian cells, a defect in Ca²⁺ mobilization may have a detrimental influence on two important processes: the secretion of steroids (E2 or/and P4) and their morphological and functional differentiation. The aim of this study was to determine the influence of PCBs: 126 (dioxin-like) 77 (ambivalent) and 153 (estrogen-like) and a mixture of PCBs (Aroclor 1248) on these processes. Bovine granulosa and luteal cells were incubated for 72 hrs with PCBs (100 ng/ml), followed by Fura 2AM dye, and the fluctuations in intracellular Ca²⁺ mobilization after FSH/LH treatment were determined using an inverted microscope coupled with a CCD camera. The intensity and area of fluorescence excited by UV light were detected in the green spectrum of visible light. Aroclor 1248 and PCBs 153 and 77 significantly decreased (P < 0.01-0.001) the effect of FSH on intracellular Ca²⁺ mobilization in granulosa cells. In luteal cells, the most effective PCB on this process was PCB 77. The results revealed adverse effects of PCBs on the mobilization of intracellular Ca²⁺. Moreover, the estrogen-like congeners were found to more effectively disturb this process than the dioxin-like PCB 126. Hence, it is possible for PCBs to have a negative influence on reproductive processes by affecting calcium mobilization.

• Wydawca: -
• Czasopismo: Polish Journal of Veterinary Sciences
• Rocznik: 2013
• Tom: 16
• Numer: 3
• Opis fizyczny: p.417-424,fig.,ref.

Twórcy

autor

Mlynarczuk J.

• Institute of Animal Reproduction and Food Research, Polish Academy of Sciences, Tuwima 10, 10-747 Olsztyn, Poland

autor

Kowalik M.

• Institute of Animal Reproduction and Food Research, Polish Academy of Sciences, Tuwima 10, 10-747 Olsztyn, Poland

Bibliografia

• Adriaens I, Cortvrindt R, Smitz J (2004) Differential FSH exposure in preantral follicle culture has marked effects on folliculogenesis and oocyte developmental competence. Hum Reprod 19: 398-408.
• Archbald LF, Thatcher WW (1992) Ovarian follicular dynamics and management of ovarian cysts. In: van Horn HH, Wilcox CJ (eds), Large Dairy Herd Management. I ed., American Dairy Science Association, Champaign, pp 199-208.
• Armstrong DT, Irvine BJ, Earl CR, McLean D, Seamark RF (1994) Gonadotropin stimulation regimens for follicular aspiration and in vitro embryo production from calf oocytes. Theriogenology 42: 1227-1236.
• Bae J, Stuenkel EL, Loch-Caruso R (1999) Stimulation of oscillatory uterine contraction by the PCB mixture Aroclor 1242 may involve increased [Ca²⁺]i through voltage-operated calcium channels. Toxicol Appl Pharmacol 155: 261-272.
• Baird DT (1992) Luteotrohpic control of the corpus luteum. Anim Reprod Sci 28: 95-102.
• Bartlett PC, Ngategize PK, Kaneene JB, Kirk JH, Anderson SM, Mather EC (1986) Cystic follicular disease in Michigan Holstein-Friesian cattle: incidence, descriptive epidemiology and economic impact. Prev Vet Med 4: 15-33.
• Brendtson AK, Vincent SE, Fortune JE (1995) Low and high concentrations of gonadotropins differentially regulate hormone production by theca interna and granulosa cells from bovine preovulatory follicles. Biol Reprod 52: 1334-1342.
• Campbell BK, Dobson H, Baird DT, Scaramuzzi RJ (1999) Examination of the relative role of FSH and LH in the mechanism of ovulatory follicle selection in sheep. J Reprod Fertil 117: 355-367.
• Fields MJ, Fields PA (1996) Morphological characteristics of the bovine corpus luteum during the estrous cycle and pregnancy. Theriogenology 45: 1295-1325.
• Fortune JE (1993) Follicular dynamics during the bovine estrous cycle: a limiting factor in improvement of fertility? Anim Reprod Sci 33: 111-125.
• Fortune JE, Rivera GM, Evans AC, Turzillo AM (2001) Differentiation of dominant versus subordinate follicles in cattle. Biol Reprod 65: 648-654.
• Frame GM, Cochran JW, Bowadt SS (1996) Complete PCB congener distributions for 17 Aroclor mixtures determined by 3 HRCG systems optimized for comprehensive, quantitative, congener-specific analysis. J High Res Chromatog 19: 657-668.
• Glynn AW, Wernroth L, Atuma S, Linder C-E, Aune M, Nilsson I, Darnerud PO (2000) PCB and chlorinated pesticide concentrations in swine and bovine adipose tissue in Sweden 1991 – 1997: spatial and temporal trends. Sci Total Environ 246: 195-206.
• Götz F, Thieme S, Dörner G (2001) Female infertility – effect of perinatal xenoestrogen exposure on reproductive functions in animals and humans. Folia Histochem Cytobiol 39; (Suppl 2): 40-43.
• Grynkiewicz G, Poenie M, Tsien RY (1985) A new generation of Ca²⁺ indicators with greatly improved fluorescence properties. J Biol Chem 260: 3440-3450.
• Henderson KM, McNatty KP, Smith P, Gibb M, O’Keeffe LE, Lun S, Heath DA, Prisk MD (1987) Influence of follicular health on the steroidogenic and morphological characteristics of bovine granulosa cells in vitro. J Reprod Fertil 79: 185-193.
• Heirichs WL, Gellert RJ, Bakke JL, Lawrence NL (1971) DDT administered to neonatal rats induces persistent estrus syndrome. Science 173: 642-643.
• Hunter MG, Robinson RS, Mann GE, Webb R (2004) Endocrine and paracrine control of follicular development and ovulation rate in farm species. Anim Reprod Sci 82-83: 461-477.
• Inglefield JR, Mundy WR, Shafer TJ (2001) Inositol 1,4,5-triphosphate receptor- sensitive Ca²⁺ release, store-operated Ca²⁺ entry, and cAMP responsive element binding protein phosphorylation in developing cortical cells following exposure to polychlorinated biphenyls. J Pharmacol Exp Ther 297: 762-773.
• Ireland JJ, Murphee RL, Coulson PB (1980) Accuracy of predicting stages of bovine estrous cycle by gross appearance of the corpus luteum. J Dairy Sci 63: 155-160.
• Ji TH, Grossmann M, Ji I (1998) G protein-coupled receptors. I. Diversity of receptor- ligand interactions. J Biol Chem 273: 17299-17302.
• Jonsson HT Jr, Keil JE, Gaddy RG, Loadholt CB, Hennigar GR, Walker EM Jr (1975-1976) Prolonged ingestion of commercial DDT and PCB; effects on progesterone levels and reproduction in the mature female rat. Arch Environ Contam Toxicol 3: 479-490.
• Kawate N (2004) Studies on the regulation of expression of luteinizing hormone receptor in the ovary and the mechanism of follicular cyst formation in ruminants. J Reprod Dev 50: 1-8.
• Kamarianos A, Karamanlis X, Goulas P, Theodosiadou E, Smokovitis A (2003) The presence of environmental pollutants in the follicular fluid of farm animals (cattle, sheep, goats and pigs). Reprod Toxicol 17: 185-195.
• Katzenellenbogen BS, Bhardwaj B, Fang H, Ince BA, Pakdel F, Reese JC, Schodin D, Wrenn CK (1993) Hormone binding and transcription activation by estrogen receptors: analyses using mammalian and yeast systems. J Steroid Biochem Mol Biol 47: 39-48.
• Kotwica J, Wróbel M, Młynarczuk J (2006) The influence of polychlorinated biphenyls (PCBs) and phytoestrogens in vitro on functioning of reproductive tract in cow. Reprod Biol 6 (Suppl 1): 189-194.
• Lind PM, Eriksen EF, Sahlin L, Edlund M, Orberg J (1999) Effects of the antiestrogenic environmental pollutant 3,3’,4,4’,5-pentachlorobiphenyl (PCB-126) in rat bone and uterus: diverging effects in ovariectomized and intact animals. Toxicol Appl Pharmacol 154: 236-244.
• Llansola M, Piedrafita B, Rodrigo R, Montoliu C, Felipo V (2009) Polychlorinated biphenyls PCB 153 and PCB 126 impair the glutamate-nitric oxide-cGMP pathway in cerebellar neurons in culture by different mechanisms. Neurotox Res 16: 97-105.
• Meeker JD, Hauser R (2010) Exposure to polychlorinated biphenyls (PCBs) and male reproduction. Syst Biol Reprod Med 56: 122-131.
• Menon KM, Menon B (2012) Structure, function and regulation of gonadotropin receptors – a perspective. Mol Cell Endocrinol 356: 88-97.
• Mlynarczuk J, Kotwica J (2005) Influence of polychlorinated biphenyls on the secretion of oxytocin from bovine luteal cells anf from granulosa cells obtained from the follicles of different size. Pol J Vet Sci 8: 261-267.
• Mlynarczuk JJ, Niewiadowska A, Kotwica J (2005) Polychlorinated biphenyls impair FSH-stimulated effect on the secretion of steroids and oxytocin from cultured bovine granulosa cells. Bull Vet I Pulawy 49: 411-417.
• Mlynarczuk J, Kotwica J (2006) Influence of polychlorinated biphenyls on LH-stimulated secretion of progestereone and oxytocin from bovine luteal cells. Pol J Vet Sci 9: 101-108.
• Nesaretnam K, Corcoran D, Dils RR, Darbre P (1996) 3,4,3’,4’-Tetrachlorobiphenyl acts as an estrogen in vitro and in vivo model. Mol Endocrinol 10: 923-936.
• Nikula H, Talonpoika T, Kaleva M, Toppari J (1999) Inhibition of hCG-stimulated steroidogenesis in cultured mouse Leydig tumor cells by bisphenol A and octylphenols. Toxicol Appl Pharmacol 157: 166-173.
• Okuda K, Miyamoto A, Sauerwein H, Schweigert FJ, Schams D (1992) Evidence for oxytocin receptors in cultured bovine luteal cells. Biol Reprod 46: 1001-1006.
• Pang S, Cao JQ, Katz BH, Hayes CL, Sutter TR, Spink DC (1999) Inductive and inhibitory effects of non-ortho-substituted polychlorinated biphenyls on estrogen metabolism and human cytochromes P450 1A1 and 1B1. Biochem Pharmacol 58: 29-38.
• Pöhland R, Tiemann U (2003) Forskolin-induced cyclic AMP signaling in single adherent bovine oviductal cells: effect of dichlorodiphenyltrichloroethane (DDT) and tris(4-chlorophenyl)methanol (TCPM). Toxicol In Vitro 17: 375-383.
• Roselli M, Reinhart K, Imthurn B, Keller PJ, Dubey RK (2000) Cellular and biochemical mechanisms by which environmental oestrogens influence reproductive function. Hum Reprod Update 6: 332-350.
• Ryu KS, Gilchrist RL, Koo YB, Ji I, Ji TH (1998) Gene, interaction, signal generation, signal divergence and signal transduction of the LH/GC receptor. Int J Gynecol Obstet 60: S9-S20.
• Shemesh M, Hansel W (1976) Steroid synthesis by ovarian follicles in response to LH and PGF2alpha. Proc Soc Exp Biol Med 152: 86-89.
• Suh J, Kang JS, Yang KH, Kaminski NE (2003) Antagonism of aryl hydrocarbon receptor-dependent induction of CYP1A1 and inhibition of IgM expression by di-ortho-substituted polychlorinated biphenyls. Toxicol Appl Pharmacol 187: 11-21.
• Thomas GO, Sweetman AJ, Jones KC (1999) Metabolism and body-burden of PCBs in lactating dairy cows. Chemosphere 39: 1533-1544.
• Ulbrich B, Stahlmann R (2004) Developmental toxicity of polychlorinated biphenyls (PCBs): a systematic review of experimental data. Arch Toxicol 78: 252-268.
• Vanholder T, Opsomer G, de Kruif, A (1997) Aetiology and pathogenesis of cystic ovarian follicles in dairy cattle: a review. Reprod Nutr Dev 46: 105-119.
• Voie OA, Fonnum F (1998) Ortho substituted polychlorinated biphenyls elevate intracellular [Ca(2+)] in human granulocytes. Environ Toxicol Pharmacol 5: 105-112.
• Voss AK, Fortune JE (1991) Oxytocin stimulates progesterone production by bovine granulosa cells isolated before, but not after, the luteinizing hormone surge. Mol Cell Endocrinol 78: 17-24.
• Wójtowicz AK, Kajta M, Gregoraszczuk EŁ (2007) DDT- and DDE-induced disruption of ovarian steroidogenesis in prepubertal porcine ovarian follicles: a possible interaction with the main steroidogenic enzymes and estrogen receptor beta. J Physiol Pharmacol 58: 873-885.
• Wrobel M, Kotwica J (2005) Effect of polychlorinated biphenyls (PCBs) on basal and OT-stimulated calcium concentrations in myometrial cells in cow. Reprod Biol 5: 321-330.
• Wrobel MH, Rekawiecki R, Kotwica J (2009) Involvement of prostaglandin F2α in the adverse effect of PCB 77 on the force of contractions of bovine myometrium. Toxicology 262: 224-229.
• Wrobel MH, Mlynarczuk J, Kotwica J (2010) Influence of polychlorinated biphenyls and their hydroxylated metabolites on prostaglandins secretion from epithelial cells of bovine oviduct, in vitro. Toxicology 270: 85-91.
• Yilmaz B, Sandal S, Chen CH, Carpenter DO (2006) Effects of PCB 52 and PCB 77 on cell viability, [Ca(2+)](i) levels and membrane fluidity in mouse thymocytes. Toxicology 217: 184-193.
• Zhu X, Gilbert S, Birnbaumer R, Birnbaumer L (1994) Dual signaling potential is common among Gs-coupled receptors and dependent on receptor density. Mol Pharmacol 46: 460-469.