Estrous cycle-dependent changes of Fas expression in the bovine corpus luteum: influence of keratin 8/18 intermediate filaments and cytokines

Reproductive Biology and Endocrinology

David Townson¹  Alyssa Birt²  Jennifer Forcina¹  Alice Duncan¹ 

[1] Department of Molecular, Cellular and Biomedical Sciences, University of New Hampshire, Durham, NH, USA;Department of Dairy and Animal Science, The Pennsylvania State University, University Park, PA, USA

关键词: Ovary;    Fas;    Cytoskeleton;    Cytokines;    Corpus Luteum;    Apoptosis;   

Others  :  1149873
DOI  :  10.1186/1477-7827-10-90

 received in 2012-08-29, accepted in 2012-10-26,  发布年份 2012

【 摘 要 】

Background

Fas expression and Fas-induced apoptosis are mechanisms attributed to the selective destruction of cells of the corpus luteum (CL) during luteal regression. In certain cell-types, sensitivity to these death-inducing mechanisms is due to the loss or cleavage of keratin-containing intermediate filaments. Specifically, keratin 8/18 (K8/K18) filaments are hypothesized to influence cell death in part by regulating Fas expression at the cell surface.

Methods

Here, Fas expression on bovine luteal cells was quantified by flow cytometry during the early (Day 5, postovulation) and late stages (Days 16–18, postovulation) of CL function, and the relationship between Fas expression, K8/K18 filament expression and cytokine-induced cell death in vitro was evaluated.

Results

Both total and cell surface expression of Fas on luteal cells was greater for early versus late stage bovine CL (89% vs. 44% of cells for total Fas; 65% vs.18% of cells for cell surface Fas; respectively, P<0.05, n=6-9 CL/stage). A similar increase in the steady-state concentration of mRNA for Fas, as detected by quantitative real-time polymerase chain reaction, however, was not observed. Transient disruption of K8/K18 filaments in the luteal cells with acrylamide (5 mM), however, had no effect on the surface expression of Fas (P>0.05, n=4 CL/stage), despite evidence these conditions increased Fas expression on HepG2 cells (P<0.05, n= 3 expts). Exposure of the luteal cells to cytokines induced cell death (P<0.05) as expected, but there was no effect of K8/K18 filament disruption by acrylamide (P>0.05) or stage of CL (P>0.05, n= 4 CL/stage) on this outcome.

Conclusion

In conclusion, we rejected our null hypothesis that the cell surface expression of Fas does not differ between luteal cells of early and late stage CL. The results also did not support the idea that K8/K18 filaments influence the expression of Fas on the surface of bovine luteal cells. Potential downstream effects of these filaments on death signaling, however, remain a possibility. Importantly, the elevated expression of Fas observed on cells of early stage bovine CL compared to late stage bovine CL raises a provocative question concerning the physiological role(s) of Fas in the corpus luteum, particularly during early luteal development.

【 授权许可】

   
2012 Duncan et al.; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]Ashkenazi A, Dixit VM: Death receptors: signaling and modulation. Science 1998, 281(5381):1305-1308.
• [2]Wajant H: The Fas signaling pathway: more than a paradigm. Science 2002, 296(5573):1635-1636.
• [3]Nagata S: Fas ligand-induced apoptosis. Annu Rev Genet 1999, 33:29-55.
• [4]Scaffidi C, Fulda S, Srinivasan A, Friesen C, Li F, Tomaselli KJ, Debatin KM, Krammer PH, Peter ME: Two CD95 (APO-1/Fas) signaling pathways. EMBO J 1998, 17(6):1675-1687.
• [5]Taniguchi H, Yokomizo Y, Okuda K: Fas-Fas ligand system mediates luteal cell death in bovine corpus luteum. Biol Reprod 2002, 66(3):754-759.
• [6]Pru JK, Hendry IR, Davis JS, Rueda BR: Soluble Fas ligand activates the sphingomyelin pathway and induces apoptosis in luteal steroidogenic cells independently of stress-activated p38(MAPK). Endocrinology 2002, 143(11):4350-4357.
• [7]Kliem H, Berisha B, Meyer HH, Schams D: Regulatory changes of apoptotic factors in the bovine corpus luteum after induced luteolysis. Mol Reprod Dev 2009, 76(3):220-230.
• [8]Carambula SF, Pru JK, Lynch MP, Matikainen T, Goncalves PB, Flavell RA, Tilly JL, Rueda BR: Prostaglandin F2alpha- and FAS-activating antibody-induced regression of the corpus luteum involves caspase-8 and is defective in caspase-3 deficient mice. Reprod Biol Endocrinol 2003, 1:15. BioMed Central Full Text
• [9]Moll R, Franke WW, Schiller DL, Geiger B, Krepler R: The catalog of human cytokeratins: patterns of expression in normal epithelia, tumors and cultured cells. Cell 1982, 31(1):11-24.
• [10]Czernobilsky B, Moll R, Levy R, Franke WW: Co-expression of cytokeratin and vimentin filaments in mesothelial, granulosa and rete ovarii cells of the human ovary. Eur J Cell Biol 1985, 37:175-190.
• [11]Gall L, De Smedt V, Ruffini S: Co-expression of cytokeratins and vimentin in sheep cumulus-oocyte complexes. Alteration of intermediate filament distribution by acrylamide. Dev Growth Differ 1992, 34(5):579-587.
• [12]Gallicano GI, Larabell CA, McGaughey RW, Capco DG: Novel cytoskeletal elements in mammalian eggs are composed of a unique arrangement of intermediate filaments. Mech Dev 1994, 45(3):211-226.
• [13]Nilsson I, Mattsson MO, Selstam G: Presence of the intermediate filaments cytokeratins and vimentin in the rat corpus luteum during luteal life-span. Histochem Cell Biol 1995, 103(3):237-242.
• [14]Santini D, Ceccarelli C, Mazzoleni G, Pasquinelli G, Jasonni VM, Martinelli GN: Demonstration of cytokeratin intermediate filaments in oocytes of the developing and adult human ovary. Histochemistry 1993, 99(4):311-319.
• [15]van den Hurk R, Dijkstra G, van Mil FN, Hulshof SC, van den Ingh TS: Distribution of the intermediate filament proteins vimentin, keratin, and desmin in the bovine ovary. Mol Reprod Dev 1995, 41(4):459-467.
• [16]Townson DH, Putnam AN, Sullivan BT, Guo L, Irving-Rodgers HF: Expression and distribution of cytokeratin 8/18 intermediate filaments in bovine antral follicles and corpus luteum: an intrinsic mechanism of resistance to apoptosis? Histol Histopathol 2010, 25(7):889-900.
• [17]Fuchs E, Weber K: Intermediate filaments: structure, dynamics, function, and disease. Annu Rev Biochem 1994, 63:345-382.
• [18]Singh S, Koke JR, Gupta PD, Malhotra SK: Multiple roles of intermediate filaments. Cytobios 1994, 77(308):41-57.
• [19]Eriksson JE, Dechat T, Grin B, Helfand B, Mendez M, Pallari HM, Goldman RD: Introducing intermediate filaments: from discovery to disease. J Clin Invest 2009, 119(7):1763-1771.
• [20]Gilbert S, Loranger A, Daigle N, Marceau N: Simple epithelium keratins 8 and 18 provide resistance to Fas-mediated apoptosis. The protection occurs through a receptor-targeting modulation. J Cell Biol 2001, 154(4):763-773.
• [21]Ku NO, Soetikno RM, Omary MB: Keratin mutation in transgenic mice predisposes to Fas but not TNF-induced apoptosis and massive liver injury. Hepatology 2003, 37(5):1006-1014.
• [22]Marceau N, Loranger A, Gilbert S, Daigle N, Champetier S: Keratin-mediated resistance to stress and apoptosis in simple epithelial cells in relation to health and disease. Biochem Cell Biol 2001, 79(5):543-555.
• [23]Ricken AM, Spanel-Borowski K, Saxer M, Huber PR: Cytokeratin expression in bovine corpora lutea. Histochem Cell Biol 1995, 103(5):345-354.
• [24]Pate JL, Condon WA: Effects of serum and lipoproteins on steroidogenesis in cultured bovine luteal cells. Mol Cell Endocrinol 1982, 28(3):551-562.
• [25]Goldberg MJ, Moses MA, Tsang PC: Identification of matrix metalloproteinases and metalloproteinase inhibitors in bovine corpora lutea and their variation during the estrous cycle. J Anim Sci 1996, 74(4):849-857.
• [26]Vickers SL, Cowan RG, Harman RM, Porter DA, Quirk SM: Expression and activity of the Fas antigen in bovine ovarian follicle cells. Biol Reprod 2000, 62(1):54-61.
• [27]Eckert BS, Yeagle PL: Acrylamide treatment of PtK1 cells causes dephosphorylation of keratin polypeptides. Cell Motil Cytoskeleton 1988, 11(1):24-30.
• [28]Durham HD, Pena SD, Carpenter S: The neurotoxins 2,5-hexanedione and acrylamide promote aggregation of intermediate filaments in cultured fibroblasts. Muscle Nerve 1983, 6(9):631-637.
• [29]Eckert BS: Alteration of intermediate filament distribution in PtK1 cells by acrylamide. Eur J Cell Biol 1985, 37:169-174.
• [30]Eckert BS: Alteration of the distribution of intermediate filaments in PtK1 cells by acrylamide. II: effect on the organization of cytoplasmic organelles. Cell Motil Cytoskeleton 1986, 6(1):15-24.
• [31]Shiver TM, Sackett DL, Knipling L, Wolff J: Intermediate filaments and steroidogenesis in adrenal Y-1 cells: acrylamide stimulation of steroid production. Endocrinology 1992, 131(1):201-207.
• [32]Quirk SM, Harman RM, Cowan RG: Regulation of Fas antigen (Fas, CD95)-mediated apoptosis of bovine granulosa cells by serum and growth factors. Biol Reprod 2000, 63(5):1278-1284.
• [33]Bowolaksono A, Nishimura R, Hojo T, Sakumoto R, Acosta TJ, Okuda K: Anti-apoptotic roles of prostaglandin E2 and F2alpha in bovine luteal steroidogenic cells. Biol Reprod 2008, 79(2):310-317.
• [34]Sakamaki K, Yoshida H, Nishimura Y, Nishikawa S, Manabe N, Yonehara S: Involvement of Fas antigen in ovarian follicular atresia and luteolysis. Mol Reprod Dev 1997, 47(1):11-18.
• [35]Roughton SA, Lareu RR, Bittles AH, Dharmarajan AM: Fas and Fas ligand messenger ribonucleic acid and protein expression in the rat corpus luteum during apoptosis-mediated luteolysis. Biol Reprod 1999, 60(4):797-804.
• [36]Komatsu K, Manabe N, Kiso M, Shimabe M, Miyamoto H: Soluble Fas (FasB) regulates luteal cell apoptosis during luteolysis in murine ovaries. Mol Reprod Dev 2003, 65(4):345-352.
• [37]Hughes DP, Crispe IN: A naturally occurring soluble isoform of murine Fas generated by alternative splicing. J Exp Med 1995, 182(5):1395-1401.
• [38]Cheng J, Zhou T, Liu C, Shapiro JP, Brauer MJ, Kiefer MC, Barr PJ, Mountz JD: Protection from Fas-mediated apoptosis by a soluble form of the Fas molecule. Science 1994, 263(5154):1759-1762.
• [39]Pan G, Ni J, Wei YF, Yu G, Gentz R, Dixit VM: An antagonist decoy receptor and a death domain-containing receptor for TRAIL. Science 1997, 277(5327):815-818.
• [40]Marsters SA, Sheridan JP, Pitti RM, Huang A, Skubatch M, Baldwin D, Yuan J, Gurney A, Goddard AD, Godowski P, et al.: A novel receptor for Apo2L/TRAIL contains a truncated death domain. Curr Biol 1997, 7(12):1003-1006.
• [41]Sheridan JP, Marsters SA, Pitti RM, Gurney A, Skubatch M, Baldwin D, Ramakrishnan L, Gray CL, Baker K, Wood WI, et al.: Control of TRAIL-induced apoptosis by a family of signaling and decoy receptors. Science 1997, 277(5327):818-821.
• [42]Sugimoto M, Kagawa N, Morita M, Kume S, Wongpanit K, Jin H, Manabe N: Changes in the expression of decoy receptor 3 in granulosa cells during follicular atresia in porcine ovaries. J Reprod Dev 2010, 56(4):467-474.
• [43]Jenkins M, Keir M, McCune JM: A membrane-bound Fas decoy receptor expressed by human thymocytes. J Biol Chem 2000, 275(11):7988-7993.
• [44]Peter ME, Budd RC, Desbarats J, Hedrick SM, Hueber AO, Newell MK, Owen LB, Pope RM, Tschopp J, Wajant H, et al.: The CD95 receptor: apoptosis revisited. Cell 2007, 129(3):447-450.
• [45]Desbarats J, Newell MK: Fas engagement accelerates liver regeneration after partial hepatectomy. Nat Med 2000, 6(8):920-923.
• [46]Barnhart BC, Legembre P, Pietras E, Bubici C, Franzoso G, Peter ME: CD95 ligand induces motility and invasiveness of apoptosis-resistant tumor cells. EMBO J 2004, 23(15):3175-3185.
• [47]Badorff C, Ruetten H, Mueller S, Stahmer M, Gehring D, Jung F, Ihling C, Zeiher AM, Dimmeler S: Fas receptor signaling inhibits glycogen synthase kinase 3β and induces cardiac hypertrophy following pressure overload. J Clin Invest 2002, 109(3):373-381.
• [48]Rueda BR, Hendry IR, Ndjountche L, Suter J, Davis JS: Stress-induced mitogen-activated protein kinase signaling in the corpus luteum. Mol Cell Endocrinol 2000, 164(1–2):59-67.
• [49]Chen D, Fong HW, Davis JS: Induction of c-fos and c-junMessenger ribonucleic acid expression by prostaglandin F2α is mediated by a protein kinase C-dependent extracellular signal-regulated kinase mitogen-activated protein kinase pathway in bovine luteal cells. Endocrinology 2001, 142(2):887-895.
• [50]Arvisais E, Hou X, Wyatt TA, Shirasuna K, Bollwein H, Miyamoto A, Hansen TR, Rueda BR, Davis JS: Prostaglandin F2α represses IGF-I-stimulated IRS1/Phosphatidylinositol-3-Kinase/AKT signaling in the corpus luteum: role of ERK and P70 ribosomal S6 kinase. Mol Endocrinol 2010, 24(3):632-643.
• [51]Pate JL, Landis Keyes P: Immune cells in the corpus luteum: friends or foes? Reproduction 2001, 122(5):665-676.