Ectoplacental cone induces resistance to apoptosis in high doses of interferon (IFN)-γ-treated decidual cells

American Journal of Reproductive Immunology

Volumn 67, Issue 1, 2012, Pages 73-83

  Borbely, Alexandre U ^a   Fontenele Neto, José D ^b   Vidsiunas, Alex K ^c   Gomes, Sara Z ^a   Hoshida, Mara S ^a   de Oliveira, Sérgio F ^a   Bevilacqua, Estela ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b Federal University of the Semi arid   (Brazil)

^c Nove de Julho University   (Brazil)

Author keywords

Cell death; Coculture assay; Interferon ; Mesometrial decidual cells; Trophoblast; TUNEL reaction

Indexed keywords

GAMMA INTERFERON;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL; CELL CULTURE; CELL DEATH; CELL PROLIFERATION; CELL SURVIVAL; COCULTURE; CONTROLLED STUDY; DECIDUAL CELL; ECTOPLACENTAL CONE; EMBRYO; FEMALE; MORTALITY; MOUSE; NONHUMAN; PLACENTA; PREGNANCY; PRIORITY JOURNAL;

ANIMALS; APOPTOSIS; CELL COMMUNICATION; CELL SURVIVAL; COCULTURE TECHNIQUES; DECIDUA; DIFFUSION CHAMBERS, CULTURE; FEMALE; HUMANS; IN SITU NICK-END LABELING; INTERFERON-GAMMA; MICE; MICROSCOPY, FLUORESCENCE; ORGAN SPECIFICITY; PLACENTA; PREGNANCY; PRIMARY CELL CULTURE;

EID: 83555176232     PISSN: 10467408     EISSN: 16000897     Source Type: Journal    
DOI: 10.1111/j.1600-0897.2011.01060.x     Document Type: Article

References (62)

1. Abrahamsohn PA, Zorn TMT, Oliveira S: Decidua in rodents. In The Endometrium, SR Glasser, JD Aplin, LC Giudice, S Tabibzadeh (eds). London, Taylor and Francis, 2002, pp 279-293.
2. Dimitriadis E, White CA, Jones RL, Salamonsen LA: Cytokines, chemokines and growth factors in endometrium related to implantation. Hum Reprod Update 2005; 11:613-630.
3. Chaouat G, Dubanchet S, Ledée N: Cytokines: important for implantation? J Assist Reprod Genet 2007; 24:491-505. Review.
4. Audus KL, Soares MJ, Hunt JS: Characteristics of the fetal/maternal interface with potential usefulness in the development of future immunological and pharmacological strategies. J Pharmacol Exp Therap 2002; 301:402-409.
5. Hess AP, Hamilton AE, Talbi S, Dosiou C, Nyegaard M, Nayak N, Genbecev-Krtolica O, Mavrogianis P, Ferrer K, Kruessel J, Fazleabas AT, Fisher SJ, Giudice LC: Decidual stromal cell response to paracrine signals from the trophoblast: amplification of immune and angiogenic modulators. Biol Reprod 2007; 76:102-117.
6. Platt JS, Hunt JS: Interferon-γ gene expression in cycling and pregnant mouse uterus: temporal aspects and cellular localization. J Leukoc Biol 1998; 64:393-400.
7. Ashkar AA, Croy BA: Functions of uterine natural killer cells are mediated by interferon gamma production during murine pregnancy. Semin Immunol 2001; 13:235-241.
8. Zourbas S, Dubanchet S, Martal J, Chaouat G: Localization of pro-inflammatory (IL-12, IL-15) and anti-inflammatory (IL-11, IL-13) cytokines at the foetomaternal interface during murine pregnancy. Clin Exp Immunol 2001; 126:519-528.
9. Chaouat G, Zourbas S, Ostojic S, Lappree-Delage G, Dubanchet S, Ledee N, Martal J: A brief review of recent data on some cytokine expressions at the materno-foetal interface which might challenge the classical Th1/Th2 dichotomy. J Reprod Immunol 2002; 53:241-256.
10. Croy BA, Chantakru S, Esadeg S, Ashkar AA, Wei Q: Decidual natural killer cells: key regulators of placental development (a review). J Reprod Immunol 2002; 57:151-168.
11. Esadeg S, He H, Pijnenborg R, Van Leuven F, Croy BA: Alpha-2 macroglobulin controls trophoblast positioning in mouse implantation sites. Placenta 2003; 24:912-921.
12. Mincheva-Nilsson L: Pregnancy and gamma/delta T cells: taking on the hard questions. Reprod Biol Endocrinol 2003; 1:120.
13. Ashkar AA, Di Santo JP, Croy BA: Interferon gamma contributes to initiation of uterine vascular modification, decidual integrity, and uterine natural killer cell maturation during normal murine pregnancy. J Exp Med 2000; 192:259-270.
14. Joswig A, Gabriel HD, Kibschull M, Winterhager E: Apoptosis in uterine epithelium and decidua in response to implantation: evidence for two different pathways. Reprod Biol Endocrinol 2003; 26:1-44.
15. Wu X, Wei H, Zhang J, Tian Z: Increased uterine NK-derived IFN-gamma and TNF-alpha in C57BL/6J mice during early gestation. Cell Mol Immunol 2006; 3:131-137.
16. Guimond MJ, Luross JA, Wang B, Terhorst C, Danial S, Croy BA: Absence of natural killer cells during murine pregnancy is associated with reproductive compromise in TgE26 mice. Biol Reprod 1997; 56:169-179.
17. Redline RW: Role of uterine natural killer cells and interferon gamma in placental development. J Exp Med 2000; 192:F1-F4.
18. Ashkar AA, Croy BA: Interferon-gamma contributes to the normalcy of murine pregnancy. Biol Reprod 1999; 61:493-502.
19. Hoshida MS, Gorjão R, Lima C, Daher S, Curi R, Bevilacqua E: Regulation of gene expression in mouse trophoblast cells by interferon-gamma. Placenta 2007; 28:1059-1072.
20. Liu Y, Janeway Jr CA: Interferon γ plays a critical role in induced cell death of effector T cell: a possible third mechanism of self-tolerance. J Exp Med 1990; 172:1735-1739.
21. Deiss LP, Feinstein E, Berissi H, Cohen O, Kimchi A: Identification of a novel serine/threonine kinase and a novel 15-kD protein as potential mediators of the gamma interferon-induced cell death. Genes Dev 1995; 9:15-30.
22. Wu AJ, Chen ZJ, Tsokos M, O'Connell BC, Ambudkar IS, Baum BJ: Interferon-gamma induced cell death in a cultured human salivary gland cell line. J Cell Physiol 1996; 167:297-304.
23. Refaeli Y, Van Parijs L, Alexander SI, Abbas AK: Interferon-γ is required for activation-induced death of T lymphocytes. J Exp Med 2002; 196:999-1005.
24. Augstein P, Heinke P, Schober C, Salzsieder E: Impact of cytokine- and FasL-induced apoptosis in the beta-cell Line NIT-1. Horm Metab Res 2009; 41:207-212.
25. Foulds KE, Rotte MJ, Paley MA, Singh B, Douek DC, Hill BJ, O'Shea JJ, Watford WT, Seder RA, Wu CY: IFN-gamma mediates the death of Th1 cells in a paracrine manner. J Immunol 2008; 180:842-849.
26. Melloul D: Role of NF-kappaB in beta-cell death. Biochem Soc Trans 2008; 36:334-339. Review.
27. Almeida A, Correia-da-Silva G, Cepa M, Bell SC, Teixeira NA: Synergistic induction of apoptosis in primary rat decidual cells by INF-gamma and TNF. Mol Reprod Dev 2007; 74:371-377.
28. Liu Z, Sun QH, Yang Y, Liu JM, Peng JP: Effect of IFN-gamma on caspase-3, Bcl-2 and Bax expression, and apoptosis in rabbit placenta. Cytokine 2003; 24:201-209.
29. Jacobs AL, Carson DD: Proteoglycan synthesis and metabolism by mouse uterine stroma cultured in vitro. J Biol Chem 1991; 266:15464-15473.
30. Vladimirsky F, Chen L, Amsterdam A, Zor U, Lindner HR: Differentiation of decidual cells in cultures of rat endometrium. J Reprod Fertil 1977; 49:61-68.
31. Bell SC, Searle RF: Differentiation of decidual cells in mouse endometrial cell cultures. Reprod Fertil 1981; 61:425-433.
32. Sananès N, Weiller S, Baulieu EE, Le Goascogne C: In vitro decidualization of rat endometrial cells. Endocrinology 1978; 103:86-95.
33. Babiarz BS, Romagnano LC, Kurilla GM: Interaction of mouse ectoplacental cone trophoblast and uterine decidua in vitro. In Vitro Cell Dev Biol 1992; 28A:500-508.
34. Piva M, Flieger O, Rider V: Growth factor control of cultured rat uterine stromal cell proliferation is progesterone dependent. Biol Reprod 1996; 55:1333-1342.
35. Srivastava RK, Gu Y, Zilberstein M, Ou JS, Mayo KE, Chou JY, Gibori G: Development and characterization of a simian virus 40-transformed, temperature-sensitive rat antimesometrial decidual cell line. Endocrinology 1995; 136:1913-1919.
36. Afonso S, Tovar C, Romagnano L, Babiarz B: Control and expression of cystatin C by mouse decidual cultures. Mol Reprod Dev 2002; 61:155-163.
37. Müntener M, Hsu YC: Development of trophoblast and placenta of the mouse. A reinvestigation with regard to the in vitro culture of mouse trophoblast and placenta. Acta Anat 1977; 98:241-252.
38. Rossant J, Tamura-Lis W: Effect of culture conditions on diploid to giant-cell transformation in postimplantation mouse trophoblast. J Embryol Exp Morphol 1981; 62:217-227.
39. Gagioti S, Scavone C, Bevilacqua E: Participation of the mouse implanting trophoblast in nitric oxide production during pregnancy. Biol Reprod 2000; 62:260-268.
40. El-Hashash AH, Kimber SJ: Trophoblast differentiation in vitro: establishment and characterisation of a serum-free culture model for murine secondary trophoblast giant cells. Reproduction 2004; 128:53-71.
41. Albieri A, Hoshida MS, Gagioti SM, Leanza EC, Abrahamsohn I, Croy A, Ashkar AA, Bevilacqua E: Interferon-gamma alters the phagocytic activity of the mouse trophoblast. Reprod Biol Endocrinol 2005; 10:3-34.
42. Shiokawa S, Yoshimura Y, Nagamatsu S, Sawa H, Hanashi H, Koyama N, Katsumata Y, Nagai A, Nakamura Y: Function of P, integrins on human decidual cells during implantation. Biol Reprod 1996; 54:745-752.
43. Dai B, Cao K, Liu W, Li S, Yang Y, Chen D, Duan E: Dual roles of progesterone in embryo implantation in mouse. Endocrine 2003; 21:123-132.
44. Enders AC, Schlafke S: A morphological analysis of the early implantation stages in the rat. Am J Anat 1967; 120:185-226.
45. Tachi S, Tachi C, Lindner HR: Ultrastructural features of blastocysts attachment and trophoblast invasion in the rat. J Reprod Fertil 1970; 21:37-56.
46. Bevilacqua E, Abrahamsohn PA: Trophoblast invasion during implantation of the mouse embryo. Arch Biol Med Exp 1989; 22:107-118.
47. Peng S, Li J, Miao C, Jia L, Hu Z, Zhao P, Li J, Zhang Y, Chen Q, Duan E: Dickkopf-1 secreted by decidual cells promotes trophoblast cell invasion during murine placentation. Reproduction 2008; 135:367-375.
48. Yui J, Garcia-Lloret M, Wegmann TG, Guilbert LJ: Cytotoxicity of tumour necrosis factor-alpha and gamma-interferon against primary human placental trophoblasts. Placenta 1994; 15:819-835.
49. Tomita Y, Bilim V, Takeda M, Takahashi K: Upregulation of Fas-induced apoptosis by interferon-y accompanied by increased ICE expression in renal cell cancer cells. Apoptosa 1996; 1:209-212.
50. Kim EJ, Lee JM, Namkoong SE, Um SJ, Park JS: Interferon regulatory factor-1 mediates interferon-gamma-induced apoptosis in ovarian carcinoma cells. J Cell Biochem 2002; 85:369-380.
51. Zou GM, Reznikoff-Etievant MF, Hirsch F, Milliez J: IFN-gamma induces apoptosis in mouse embryonic stem cells, a putative mechanism of its embryotoxicity. Dev Growth Differ 2000; 42:257-264.
52. Schroder K, Hertzog PH, Ravasi T, Hume DA: Interferon-γ: an overview of signals, mechanisms and functions. J Leukoc Biol 2004; 75:163-189.
53. Hollenbaugh JA, Dutton RW: IFN-gamma regulates donor CD8 T cell expansion, migration, and leads to apoptosis of cells of a solid tumor. J Immunol 2006; 177:3004-3011.
54. Ekmekcioglu S, Mumm JB, Udtha M, Chada S, Grimm EA: Killing of human melanoma cells induced by activation of class I interferon-regulated signaling pathways via MDA-7/IL-24. Cytokine 2008; 43:34-44.
55. Correia-da-Silva G, Bell SC, Pringle JH, Teixeira NA: Patterns of expression of Bax, Bcl-2 and Bcl-x(L) in the implantation site in rat during pregnancy. Placenta 2005; 26:796-806.
56. Arya R, Mallik M, Lakhotia SC: Heat shock genes - integrating cell survival and death. J Biosci 2007; 32:595-610.
57. Rong Y, Distelhorst CW: Bcl-2 protein family members: versatile regulators of calcium signaling in cell survival and apoptosis. Annu Rev Physiol 2008; 70:73-91.
58. Fan Y, Dutta J, Gupta N, Fan G, Gélinas C: Regulation of programmed cell death by NF-kappaB and its role in tumorigenesis and therapy. Adv Exp Med Biol 2008; 615:223-250.
59. Srinivasula SM, Ashwell JD: IAPs: what's in a name? Mol Cell 2008; 30:123-135.
60. Garcia-Lloret MI, Yui J, Winkler-Lowen B, Guilbert LJ: Epidermal growth factor inhibits cytokine-induced apoptosis of primary human trophoblasts. J Cell Physiol 1996; 167:324-332.
61. Idziorek T, Khalife J, Billaut-Mulot O, Aumercier M, Mouton Y, Capron A, Bahr GM: Recombinant IL-16 inhibits HIV-1 replication and protects against activation-induced cell death (AICD). Clin Exp Immunol 1998; 112:84-91.
62. Spinetti G, Bernardini G, Camarda G, Mangoni A, Santoni A, Capogrossi MC, Napolitano M: The chemokine receptor CCR8 mediates rescue from dexamethasone-induced apoptosis via an ERK-dependent pathway. J Leukoc Biol 2003; 73:201-207.