Interleukin-10: A pleiotropic regulator in pregnancy

American Journal of Reproductive Immunology

Volumn 73, Issue 6, 2015, Pages 487-500

  Cheng, Shi Bin ^a   Sharma, Surendra ^a  

^a BROWN UNIVERSITY   (United States)

Author keywords

Adverse pregnancy outcomes; Angiogenesis; Autophagy; Endoplasmic reticulum stress; Immune tolerance; Preeclampsia

Indexed keywords

HEME OXYGENASE 1; INTERLEUKIN 1; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 6; TUMOR NECROSIS FACTOR ALPHA; HLA ANTIGEN CLASS 2; IL10 PROTEIN, HUMAN; JANUS KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; STAT PROTEIN;

ANTIGEN PRESENTATION; ANTIINFLAMMATORY ACTIVITY; ARTICLE; AUTOPHAGY; BARE LYMPHOCYTE SYNDROME; BIOLOGICAL FUNCTIONS; CELLS BY BODY ANATOMY; ENDOPLASMIC RETICULUM; FEMALE; GENE EXPRESSION; HUMAN; IMMUNOLOGICAL TOLERANCE; PHYSIOLOGICAL PROCESS; PLEIOTROPY; PREECLAMPSIA; PREGNANCY OUTCOME; PREGNANT WOMAN; PREMATURE LABOR; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SPONTANEOUS ABORTION; ANIMAL; ENDOPLASMIC RETICULUM STRESS; IMMUNOLOGY; PATHOLOGY; PREGNANCY; PREGNANCY COMPLICATIONS;

ANIMALS; ENDOPLASMIC RETICULUM STRESS; FEMALE; HISTOCOMPATIBILITY ANTIGENS CLASS II; HUMANS; IMMUNE TOLERANCE; INTERLEUKIN-10; JANUS KINASES; PHOSPHATIDYLINOSITOL 3-KINASES; PREGNANCY; PREGNANCY COMPLICATIONS; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; STAT TRANSCRIPTION FACTORS;

EID: 84929267733     PISSN: 10467408     EISSN: 16000897     Source Type: Journal    
DOI: 10.1111/aji.12329     Document Type: Article

References (140)

1. Murphy SP, Sharma S. IL-10 and pregnancy. In Immunology of Pregnancy. G Mor (ed.), New york, Springer Science, 2004, pp 26-36.
2. Kalkunte S, Nevers T, Norris WE, Sharma S: Vascular IL-10: a protective role in preeclampsia. J Reprod Immunol 2011; 88:165-169.
3. Thaxton JE, Sharma S: Interleukin-10: a multi-faceted agent of pregnancy. Am J Reprod Immunol 2010; 63:482-9110.
4. Sharma S: Natural killer cells and regulatory T cells in early pregnancy loss. Int J Dev Biol 2014; 58:219-229.
5. Dealtry GB, O'Farrell MK, Fernandez N: The Th2 cytokine environment of the placenta. Int Arch Allergy Immunol 2000; 123:107-119.
6. Hanna N, Hanna I, Hleb M, Wagner E, Dougherty J, Balkundi D, Padbury J, Sharma S: Gestational age-dependent expression of IL-10 and its receptor in human placental tissues and isolated cytotrophoblasts. J Immunol 2000; 164:5721-5728.
7. Ouyang W, Rutz S, Crellin NK, Valdez PA, Hymowitz SG: Regulation and functions of the IL-10 family of cytokines in inflammation and disease. Annu Rev Immunol 2011; 29:71-109.
8. Fiorentino DF, Bond MW, Mosmann TR: Two types of mouse T helper cell. IV. Th2 clones secrete a factor that inhibits cytokine production by Th1 clones. J Exp Med 1989; 170:2081-2095.
9. Saraiva M, O'Garra A: The regulation of IL-10 production by immune cells. Nat Rev Immunol 2010; 10:170-181.
10. Chatterjee P, Chiasson VL, Bounds KR, Mitchell BM: Regulation of the Anti-Inflammatory cytokines Interleukin-4 and Interleukin-10 during Pregnancy. Front Immunol 2014; 5:253.
11. Moore KW, de Waal Malefyt R, Coffman RL, O'Garra A: Interleukin-10 and the interleukin-10 receptor. Annu Rev Immunol 2001; 19:683-765.
12. Asadullah K, Sterry W, Volk HD: Interleukin-10 therapy-review of a new approach. Pharmacol Rev 2003; 55:241-269.
13. Tewari N, Kalkunte S, Murray DW, Sharma S: The water channel aquaporin 1 is a novel molecular target of polychlorinated biphenyls for in utero anomalies. J Biol Chem 2009; 284:15224-15232.
14. Kalkunte S, Lai Z, Tewari N, Chichester C, Romero R, Padbury J, Sharma S: In vitro and in vivo evidence for lack of endovascular remodeling by third trimester trophoblasts. Placenta 2008; 29:871-878.
15. Gunnett CA, Berg DJ, Faraci FM, Feuerstein G: Vascular effects of lipopolysaccharide are enhanced in interleukin-10-deficient mice. Stroke 1999; 30:2191-2195.
16. Gunnett CA, Heistad DD, Berg DJ, Faraci FM: IL-10 deficiency increases superoxide and endothelial dysfunction during inflammation. Am J Physiol Heart Circ Physiol 2000; 279:H1555-H1562.
17. Gunnett CA, Heistad DD, Faraci FM: Interleukin-10 protects nitric oxide-dependent relaxation during diabetes: role of superoxide. Diabetes 2002; 51:1931-1937.
18. Gunnett CA, Lund DD, Faraci FM, Heistad DD: Vascular interleukin-10 protects against LPS-induced vasomotor dysfunction. Am J Physiol Heart Circ Physiol 2005; 289:H624-H630.
19. Didion SP, Kinzenbaw DA, Schrader LI, Chu Y, Faraci FM: Endogenous interleukin-10 inhibits angiotensin II-induced vascular dysfunction. Hypertension 2009; 54:619-624.
20. Lai Z, Kalkunte S, Sharma S: A critical role of interleukin-10 in modulating hypoxia-induced preeclampsia-like disease in mice. Hypertension 2011; 57:505-514.
21. Kalkunte S, Boij R, Norris W, Friedman J, Lai Z, Kurtis J, Lim KH, Padbury JF, Matthiesen L, Sharma S: Sera from preeclampsia patients elicit symptoms of human disease in mice and provide a basis for an in vitro predictive assay. Am J Pathol 2010; 177:2387-2398.
22. Murphy SP, Fast LD, Hanna NN, Sharma S: Uterine NK cells mediate inflammation-induced fetal demise in IL-10-null mice. J Immunol 2005; 175:4084-9010.
23. Murphy SP, Hanna NN, Fast LD, Shaw SK, Berg G, Padbury JF, Romero R, Sharma S: Evidence for participation of uterine natural killer cells in the mechanisms responsible for spontaneous preterm labor and delivery. Am J Obstet Gynecol 2009; 200:308.e1-9.
24. Robertson SA, Care AS, Skinner RJ: Interleukin 10 regulates inflammatory cytokine synthesis to protect against lipopolysaccharide-induced abortion and fetal growth restriction in mice. Biol Reprod 2007; 76:738-4810.
25. Tinsley JH, South S, Chiasson VL, Mitchell BM: Interleukin-10 reduces inflammation, endothelial dysfunction, and blood pressure in hypertensive pregnant rats. Am J Physiol Regul Integr Comp Physiol 2010; 298:R713-R719.
26. Lin Y, Liu X, Shan B, Wu J, Sharma S, Sun Y: Prevention of CpG-induced pregnancy disruption by adoptive transfer of in vitro-induced regulatory T cells. PLoS One 2014; 9:e94702.
27. Chatterjee P, Chiasson VL, Kopriva SE, Young KJ, Chatterjee V, Jones KA, Mitchell BM: Interleukin 10 deficiency exacerbates toll-like receptor 3-induced preeclampsia-like symptoms in mice. Hypertension 2011; 58:489-496.
28. Chatterjee P, Chiasson VL, Seerangan G, Tobin RP, Kopriva SE, Newell-Rogers MK, Mitchell BM: Cotreatment With Interleukin 4 and Interleukin 10 Modulates Immune Cells and Prevents Hypertension in Pregnant Mice. Am J Hypertens 2014; Jun 6. pii: hpu100. [Epub ahead of print].
29. Rivera DL, Olister SM, Liu X, Thompson JH, Zhang XJ, Pennline K, Azuero R, Clark DA, Miller MJ: Interleukin-10 attenuates experimental fetal growth restriction and demise. FASEB J 1998; 12:189-197.
30. Terrone DA, Rinehart BK, Granger JP, Barrilleaux PS, Martin JN Jr, Bennett WA: Interleukin-10 administration and bacterial endotoxin-induced preterm birth in a rat model. Obstet Gynecol 2001; 98:476-480.
31. Sharma S, Stabila J, Pietras L, Singh AR, McGonnigal B, Ernerudh J, Matthiesen L, Padbury JF: Haplotype-dependent differential activation of the human IL-10 gene promoter in macrophages and trophoblasts: implications for placental IL-10 deficiency and pregnancy complications. Am J Reprod Immunol 2010; 64:179-187.
32. Sicinschi LA, Lopez-Carrillo L, Camargo MC, Correa P, Sierra RA, Henry RR, Chen J, Zabaleta J, Piazuelo MB, Schneider BG: Gastric cancer risk in a Mexican population: role of Helicobacter pylori CagA positive infection and polymorphisms in interleukin-1 and -10 genes. Int J Cancer 2006; 118:649-657.
33. Lim S, Crawley E, Woo P, Barnes PJ: Haplotype associated with low interleukin-10 production in patients with severe asthma. Lancet 1998; 352:113.
34. Shin HD, Winkler C, Stephens JL, Bream J, Young H, Goedert JJ, O'Brien T, Vlahov D, Buchbinder S, Giorgi J, Rinaldo C, Donfield S, Willoughby A, O'Brien SJ, Smith MW: Genetic restriction of HIV-1 pathogenesis to AIDS by promoter alleles of IL-10. Proc Natl Acad Sci USA 2000; 97:14467-14472.
35. Lin MT, Storer B, Martin PJ, Tseng LH, Gooley T, Chen PJ, Hansen JA: Relation of an interleukin-10 promoter polymorphism to graft-versus-host disease and survival after hematopoietic cell transplantation. N Engl J Med 2003; 349:2201-2210.
36. Steinke JW, BarekZi E, Hagman J, Borish L: Functional analysis of -571 IL-10 promoter polymorphism reveals a repressor element controlled by Sp1. J Immunol 2004; 173:3215-3222.
37. Costa GC, da Costa Rocha MO, Moreira PR, Menezes CA, Silva MR, Gollob KJ, Dutra WO: Functional IL-10 gene polymorphism is associated with Chagas disease cardiomyopathy. J Infect Dis 2009; 199:451-454.
38. Villagra A, Cheng F, Wang HW, Suarez I, Glozak M, Maurin M, Nguyen D, Wright KL, Atadja PW, Bhalla K, Pinilla-Ibarz J, Seto E, Sotomayor EM: The histone deacetylase HDAC11 regulates the expression of interleukin 10 and immune tolerance. Nat Immunol 2009; 10:92-100.
39. Gezen-Ak D, Dursun E, Hanağasi H, Bilgiç B, Lohman E, Araz ÖS, Atasoy IL, Alaylioğlu M, Önal B, Gürvit H, Yilmazer S: BDNF, TNFα, HSP90, CFH, and IL-10 serum levels in patients with early or late onset Alzheimer's disease or mild cognitive impairment. J Alzheimers Dis 2013; 37:185-195.
40. Di Bona D, Rizzo C, Bonaventura G, Candore G, Caruso C: Association between interleukin-10 polymorphisms and Alzheimer's disease: a systematic review and meta-analysis. J Alzheimers Dis 2012; 29:751-759.
41. Sowmya S, Ramaiah A, Sunitha T, Nallari P, Jyothy A, Venkateshwari A: Role of IL-10 -819(t/c) promoter polymorphism in preeclampsia. Inflammation 2014; 37:1022-1027.
42. Cao S, Liu J, Song L, Ma X: The protooncogene c-Maf is an essential transcription factor for IL-10 gene expression in macrophages. J Immunol 2005; 174:3484-3492.
43. Sharabi AB, Aldrich M, Sosic D, Olson EN, Friedman AD, Lee SH, Chen SY: Twist-2 controls myeloid lineage development and function. PLoS Biol 2008; 6:e316.
44. van den Bosch MW, Palsson-Mcdermott E, Johnson DS, O'Neill LA: LPS induces the degradation of PDCD4 to release Twist2, activating c-Maf transcription to promote IL-10 production. J Biol Chem 2014; 289:22980-22990.
45. Neumann C, Heinrich F, Neumann K, Junghans V, Mashreghi MF, Ahlers J, Janke M, Rudolph C, Mockel-Tenbrinck N, Kühl AA, Heimesaat M M, Esser C, Im SH, Radbruch A, Rutz S, Scheffold A: Role of Blimp-1 in programing Th effector cells into IL-10 producers. J Exp Med 2014; 211:1807-1819.
46. Roth I, Corry DB, Locksley RM, Abrams JS, Litton MJ, Fisher SJ: Human placental cytotrophoblasts produce the immunosuppressive cytokine interleukin 10. J Exp Med 1996; 184:539-4810.
47. Ozörnek MH, Bielfeld P, Krüssel JS, Moustafa M, Mikat-Drozdzynski B, Koldovsky U, Kuhn U: Interferon gamma and interleukin 10 levels in preimplantation embryo culture media. J Assist Reprod Genet 1995; 12:590-593.
48. Thaxton JE, Romero R, Sharma S: TLR9 activation coupled to IL-10 deficiency induces adverse pregnancy outcomes. J Immunol 2009; 183:1144-1154.
49. Lin H, Mosmann TR, Guilbert L, Tuntipopipat S, Wegmann TG: Synthesis of T helper 2-type cytokines at the maternal-fetal interface. J Immunol 1993; 151:4562-4573.
50. Simpson KL, Keelan JA, Mitchell MD: Labor-associated changes in interleukin-10 production and its regulation by immunomodulators in human choriodecidua. J Clin Endocrinol Metab 1998; 83:4332-4337.
51. Roth I, Fisher SJ: IL-10 is an autocrine inhibitor of human placental cytotrophoblast MMP-9 production and invasion. Dev Biol 1999; 205:194-204.
52. Plevyak M, Hanna N, Mayer S, Murphy S, Pinar H, Fast L, Ekerfelt C, Ernerudh J, Berg G, Matthiesen L, Sharma S: Deficiency of decidual IL-10 in first trimester missed abortion: a lack of correlation with the decidual immune cell profile. Am J Reprod Immunol 2002; 47:242-250.
53. Hanna N, Bonifacio L, Weinberger B, Reddy P, Murphy S, Romero R, Sharma S: Evidence for interleukin-10-mediated inhibition of cyclo- oxygenase-2 expression and prostaglandin production in preterm human placenta. Am J Reprod Immunol 2006; 55:19-27.
54. Makris A, Xu B, Yu B, Thornton C, Hennessy A: Placental deficiency of interleukin-10 (IL-10) in preeclampsia and its relationship to an IL10 promoter polymorphism. Placenta 2006; 27:445-451.
55. Szony BJ, Bata-Csörgo Z, Bártfai G, Kemény L, Dobozy A, Kovács L: Interleukin-10 receptors are expressed by basement membrane anchored, alpha(6) integrin(+) cytotrophoblast cells in early human placenta. Mol Hum Reprod 1999; 5:1059-1065.
56. Donnelly RP, Dickensheets H, Finbloom DS: The interleukin-10 signal transduction pathway and regulation of gene expression in mononuclear phagocytes. J Interferon Cytokine Res 1999; 19:563-573.
57. Lee TS, Chau LY: Heme oxygenase-1 mediates the anti-inflammatory effect of interleukin-10 in mice. Nat Med 2002; 8:240-246.
58. Otterbein LE, Bach FH, Alam J, Soares M, Tao Lu H, Wysk M, Davis RJ, Flavell RA, Choi AM: Carbon monoxide has anti-inflammatory effects involving the mitogen-activated protein kinase pathway. Nat Med 2000; 6:422-428.
59. Strle K, Zhou JH, Broussard SR, Venters HD, Johnson RW, Freund GG, Dantzer R, Kelley KW: IL-10 promotes survival of microglia without activating Akt. J Neuroimmunol 2002; 122:9-19.
60. Roberts CT, White CA, Wiemer NG, Ramsay A, Roberston SA: Altered placental development in interleukin-10 null mutant mice. Placenta 2003; 17:S94-S99.
61. Thaxton JE, Nevers T, Lippe EO, Blois SM, Saito S, Sharma S: NKG2D blockade inhibits poly(I:C)-triggered fetal loss in wild type but not in IL-10-/- mice. J Immunol 2013; 190:3639-4710.
62. Hill JA, Polgar K, Anderson DJ: T-helper 1-type immunity to trophoblast in women with recurrent spontaneous abortion. JAMA 1995; 273:1933-1936.
63. Hennessy A, Pilmore HL, Simmons LA, Painter DM: A Deficiency of Placental IL-10 in Preeclampsia. J Immunol 1999; 163:3491-3495.
64. Raghupathy R, Makhseed M, Azizieh F, Hassan N, Al-Azemi M, Al-Shamali E: Maternal Th1- and Th2-type reactivity to placental antigens in normal human pregnancy and unexplained recurrent spontaneous abortions. Cell Immunol 1999; 196:122-130.
65. Rezaei A, Dabbagh A: T-helper (1) cytokines increase during early pregnancy in women with a history of recurrent spontaneous abortion. Med Sci Monit 2002; 8:CR607-CR610.
66. Makhseed M, Raghupathy R, El-Shazly S, Azizieh F, Al-Harmi JA, Al-Azemi MM: Pro-inflammatory maternal cytokine profile in preterm delivery. Am J Reprod Immunol 2003; 49:308-318.
67. Chaouat G, Tranchot Diallo J, Volumenie JL, Menu E, Gras G, Delage G, Mognetti B: Immune suppression and Th1/Th2 balance in pregnancy revisited: a (very) personal tribute to Tom Wegmann. Am J Reprod Immunol 1997; 37:427-434.
68. Lidstrom C, Matthiesen L, Berg G, Sharma S, Ernerudh J, Ekerfelt C: Cytokine secretion patterns of NK cells and macrophages in early human pregnancy decidua and blood: implications for suppressor macrophages in decidua. Am J Reprod Immunol 2003; 50:444-452.
69. Kalkunte S, Chichester CO, Gotsch F, Sentman CL, Romero R, Sharma S: Evolution of non-cytotoxic uterine natural killer cells. Am J Reprod Immunol 2008; 59:425-432.
70. Kalkunte SS, Mselle TF, Norris WE, Wira CR, Sentman CL, Sharma S: Vascular endothelial growth factor C facilitates immune tolerance and endovascular activity of human uterine NK cells at the maternal-fetal interface. J Immunol 2009; 182:4085-4092.
71. Fu B, Li X, Sun R, Tong X, Ling B, Tian Z, Wei H: Natural killer cells promote immune tolerance by regulating inflammatory TH17 cells at the human maternal-fetal interface. Proc Natl Acad Sci USA 2013; 110:E231-E240.
72. Peters A, Lee Y, Kuchroo VK: The many faces of Th17 cells. Curr Opin Immunol 2011; 23:702-706.
73. Korn T, Bettelli E, Oukka M, Kuchroo VK: IL-17 and Th17 Cells. Annu Rev Immunol 2009; 27:485-517.
74. Park H, Li Z, Yang XO, Chang SH, Nurieva R, Wang YH, Wang Y, Hood L, Zhu Z, Tian Q, Dong C: A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat Immunol 2005; 6:1133-1141.
75. Wang WJ, Hao CF, Qu QL, Wang X, Qiu LH, Lin QD: The deregulation of regulatory T cells on interleukin-17-producing T helper cells in patients with unexplained early recurrent miscarriage. Hum Reprod 2010; 25:2591-2596.
76. Saito S, Nakashima A, Shima T, Ito M: Th1/Th2/Th17 and regulatory T-cell paradigm in pregnancy. Am J Reprod Immunol 2010; 63:601-610.
77. D'Addio F, Riella LV, Mfarrej BG, Chabtini L, Adams LT, Yeung M, Yagita H, Azuma M, Sayegh MH, Guleria I: The link between the PDL1 costimulatory pathway and Th17 in fetomaternal tolerance. J Immunol 2011; 187:4530-4541.
78. Yuan X, Paez-Cortez J, Schmitt-Knosalla I, D'Addio F, Mfarrej B, Donnarumma M, Habicht A, Clarkson MR, Iacomini J, Glimcher LH, Sayegh MH, Ansari MJ: A novel role of CD4 Th17 cells in mediating cardiac allograft rejection and vasculopathy. J Exp Med 2008; 205:3133-3144.
79. Huber S, Gagliani N, Esplugues E, O'Connor W Jr, Huber FJ, Chaudhry A, Kamanaka M, Kobayashi Y, Booth CJ, Rudensky AY, Roncarolo MG, Battaglia M, Flavell RA: Th17 cells express interleukin-10 receptor and are controlled by Foxp3 and Foxp3 + regulatory CD4 + T cells in an interleukin-10-dependent manner. Immunity 2011; 34:554-565.
80. Aluvihare VR, Kallikourdis M, Betz AG: Regulatory T cells mediate maternal tolerance to the fetus. Nat Immunol 2004; 5:266-271.
81. Blois SM, Kammerer U, Alba Soto C, Tometten MC, Shaikly V, Barrientos G, Jurd R, Rukavina D, Thomson AW, Klapp BF, Fernández N, Arck PC: Dendritic cells: key to fetal tolerance? Biol Reprod 2007; 77:590-598.
82. Nagamatsu T, Schust DJ: The immunomodulatory roles of macrophages at the maternal-fetal interface. Reprod Sci 2010; 17:209-218.
83. Hsu P, Nanan RK: Innate and adaptive immune interactions at the fetal-maternal interface in healthy human pregnancy and pre-eclampsia. Front Immunol 2014; 5:125.
84. Hsu P, Santner-Nanan B, Joung S, Peek MJ, Nanan R: Expansion of CD4(+) HLA-G(+) T Cell in human pregnancy is impaired in pre-eclampsia. Am J Reprod Immunol 2014; 71:217-228.
85. Kassan M, Galan M, Partyka M, Trebak M, Matrougui K: Interleukin-10 released by CD4(+)CD25(+) natural regulatory T cells improves microvascular endothelial function through inhibition of NADPH oxidase activity in hypertensive mice. Arterioscler Thromb Vasc Biol 2011; 31:2534-2542.
86. Kinzenbaw DA, Chu Y, Peña Silva RA, Didion SP, Faraci FM: Interleukin-10 protects against aging-induced endothelial dysfunction. Physiol Rep 2013; 1:e00149.
87. Parikh SM, Karumanchi SA: Putting pressure on pre-eclampsia. Nat Med 2008; 14:855-862.
88. Brosens I, Dixon HG, Robertson WB: Fetal growth retardation and the arteries of the placental bed. Br J Obstet Gynaecol 1977; 84:656-663.
89. Meekins JW, Pijnenborg R, Hanssens M, McFadyen IR, van Asshe A: A study of placental bed spiral arteries and trophoblast invasion in normal and severe pre-eclamptic pregnancies. Br J Obstet Gynaecol 1994; 101:669-674.
90. Redman CW, Sargent IL: Placental stress and pre-eclampsia: a revised view. Placenta 2009; 30:S38-S42.
91. Kalkunte S, Lai Z, Norris WE, Pietras LA, Tewari N, Boij R, Neubeck S, Markert UR, Sharma S: Novel approaches for mechanistic understanding and predicting preeclampsia. J Reprod Immunol 2009; 83:134-138.
92. Kalkunte SS, Neubeck S, Norris WE, Cheng SB, Kostadinov S, Vu Hoang D, Ahmed A, von Eggeling F, Shaikh Z, Padbury J, Berg G, Olofsson A, Markert UR, Sharma S: Transthyretin is dysregulated in preeclampsia, and its native form prevents the onset of disease in a preclinical mouse model. Am J Pathol 2013; 183:1425-1436.
93. Levine RJ, Maynard SE, Qian C, Lim KH, England LJ, Yu KF, Schisterman EF, Thadhani R, Sachs BP, Epstein FH, Sibai BM, Sukhatme VP, Karumanchi SA: Circulating angiogenic factors and the risk of preeclampsia. N Engl J Med 2004; 350:672-683.
94. Wilczynski JR, Tchorzewski H, Glowacka E, Banasik M, Lewkowicz P, Szpakowski M, Zeman K, Wilczynski J: Cytokine secretion by decidual lymphocytes in transient hypertension of pregnancy and pre-eclampsia. Mediators Inflamm. 2002; 11: 105-111.
95. Kalantar F, Rajaei S, Heidari AB, Mansouri R, Rashidi N, Izad MH, Mirahmadian M: Serum levels of tumor necrosis factor-α, interleukin-15 and interleukin-10 in patients with pre-eclampsia in comparison with normotensive pregnant women. Iran J Nurs Midwifery Res 2013; 18:463-466.
96. Peraçoli JC, Bannwart-Castro CF, Romao M, Weel IC, Ribeiro VR, Borges VT, Rudge MV, Witkin SS, Peraçoli MT: High levels of heat shock protein 70 are associated with pro-inflammatory cytokines and may differentiate early- from late-onset preeclampsia. J Reprod Immunol 2013; 100:129-134.
97. Kumar A, Begum N, Prasad S, Agarwal S, Sharma S: IL-10, TNF-α & IFN-γ: potential early biomarkers for preeclampsia. Cell Immunol 2013; 283:70-74.
98. Pinheiro MB, Martins-Filho OA, Mota AP, Alpoim PN, Godoi LC, Silveira AC, Teixeira-Carvalho A, Gomes KB, Dusse LM: Severe preeclampsia goes along with a cytokine network disturbance towards a systemic inflammatory state. Cytokine 2013; 62:165-173.
99. Peltier MR: Immunology of term and preterm labor. Reprod Biol Endocrinol 2003; 1:122.
100. Marzi M, Vigano A, Trabattoni D, Villa ML, Salvaggio A, Clerici E: Characterization of type 1 and type 2 cytokine production profile in physiologic and pathologic human pregnancy. Clin Exp Immunol 1996; 106:127-3310.
101. Jin LP, Fan DX, Zhang T, Guo PF, Li DJ: The costimulatory signal upregulation is associated with Th1 bias at the maternal-fetal interface in human miscarriage. Am J Reprod Immunol 2011; 66:270-810.
102. Hanzlikova J, Ulcova-Gallova Z, Malkusova I, Sefrna F, Panzner P: TH1-TH2 response and the atopy risk in patients with reproduction failure. Am J Reprod Immunol 2009; 61:213-2010.
103. Piccinni MP, Beloni L, Livi C, Maggi E, Scarselli G, Romagnani S: Defective production of both leukemia inhibitory factor and type 2 T-helper cytokines by decidual T cells in unexplained recurrent abortions. Nat Med 1998; 4:1020-1410.
104. Fukui A, Kwak-Kim J, Ntrivalas E, Gilman-Sachs A, Lee SK, Beaman K: Intracellular cytokine expression of peripheral blood natural killer cell subsets in women with recurrent spontaneous abortions and implantation failures. Fertil Steril 2008; 89:157-6510.
105. Rolle L, Memarzadeh Tehran M, Morell-Garcia A, Raeva Y, Schumacher A, Hartig R, et al.: Cutting edge: IL-10-producing regulatory B cells in early human pregnancy. Am J Reprod Immunol 2013; 70:448-5310.
106. Wang WJ, Hao CF, Lin QD: Dysregulation of macrophage activation by decidual regulatory T cells in unexplained recurrent miscarriage patients. J Reprod Immunol 2011; 92:97-10210.
107. Banerjee P, Ghosh S, Dutta M, Subramani E, Khalpada J, Roychoudhury S, Chakravarty B, Chaudhury K: Identification of key contributory factors responsible for vascular dysfunction in idiopathic recurrent spontaneous miscarriage. PLoS One 2013; 8:e80940.
108. Sun X, Cappelletti M, Li Y, Karp CL, Divanovic S, Dey SK: Cnr2 deficiency confers resistance to inflammation-induced preterm birth in mice. Endocrinology 2014; 155:4006-4014.
109. Sun Y, Qin X, Shan B, Wang W, Zhu Q, Sharma S, Wu J, Lin Y: Differential effects of the CpG-Toll-like receptor 9 axis on pregnancy outcome in nonobese diabetic mice and wild-type controls. Fertil Steril 2013; 99:1759-1767.
110. Wang W, Lin Y, Zeng S, Li DJ: Improvement of fertility with adoptive CD25 + natural killer cell transfer in subfertile non-obese diabetic mice. Reprod Biomed Online 2009; 18:95-103.
111. Gardner BM, Pincus D, Gotthardt K, Gallagher CM, Walter P: Endoplasmic reticulum stress sensing in the unfolded protein response. Cold Spring Harb Perspect Biol 2013; 5:a013169.
112. Cuanalo-Contreras K, Mukherjee A, Soto C: Role of Protein Misfolding and Proteostasis Deficiency in Protein Misfolding Diseases and Aging. Int J Cell Biol 2013; 2013:638083.
113. Jovaisaite V, Mouchiroud L, Auwerx J: The mitochondrial unfolded protein response, a conserved stress response pathway with implications in health and disease. J Exp Biol 2014; 217(Pt 1):137-143.
114. Scheper W, Hoozemans JJ: Endoplasmic reticulum protein quality control in neurodegenerative disease: the good, the bad and the therapy. Curr Med Chem 2009; 16:615-626.
115. Travers KJ, Patil CK, Wodicka L, Lockhart DJ, Weissman JS, Walter P: Functional and genomic analyses reveal an essential coordination between the unfolded protein response and ER-associated degradation. Cell 2000; 101:249-258.
116. Schröder M, Kaufman RJ: The mammalian unfolded protein response. Annu Rev Biochem 2005; 74:739-789.
117. Hasnain SZ, Tauro S, Das I, Tong H, Chen AC, Jeffery PL, McDonald V, Florin TH, McGuckin MA: IL-10 promotes production of intestinal mucus by suppressing protein misfolding and endoplasmic reticulum stress in goblet cells. Gastroenterology 2013; 144:357-368.
118. Burton GJ, Yung HW: Endoplasmic reticulum stress in the pathogenesis of early-onset pre-eclampsia. Pregnancy Hypertens 2011; 1:72-78.
119. Burton GJ, Yung HW, Cindrova-Davies T, Charnock-Jones DS: Placental endoplasmic reticulum stress and oxidative stress in the pathophysiology of unexplained intrauterine growth restriction and early onset preeclampsia. Placenta 2009; 30(Suppl A):S43-S48.
120. Gao HJ, Zhu YM, He WH, Liu AX, Dong MY, Jin M, Sheng JZ, Huang HF: Endoplasmic reticulum stress induced by oxidative stress in decidual cells: a possible mechanism of early pregnancy loss. Mol Biol Rep 2012; 39:9179-9186.
121. Jones CJ, Fox H: An ultrastructural and ultrahistochemical study of the human placenta in maternal pre-eclampsia. Placenta 1980; 1:61-76.
122. Kawakami T, Yoshimi M, Kadota Y, Inoue M, Sato M, Suzuki S: Prolonged endoplasmic reticulum stress alters placental morphology and causes low birth weight. Toxicol Appl Pharmacol 2014; 275:134-144.
123. Lian IA, Løset M, Mundal SB, Fenstad MH, Johnson MP, Eide IP, Bjørge L, Freed KA, Moses EK, Austgulen R: Increased endoplasmic reticulum stress in decidual tissue from pregnancies complicated by fetal growth restriction with and without pre-eclampsia. Placenta 2011; 32:823-829.
124. Yung HW, Calabrese S, Hynx D, Hemmings BA, Cetin I, Charnock-Jones DS, Burton GJ: Evidence of placental translation inhibition and endoplasmic reticulum stress in the etiology of human intrauterine growth restriction. Am J Pathol 2008; 173:451-462.
125. Yung HW, Atkinson D, Campion-Smith T, Olovsson M, Charnock-Jones DS, Burton GJ: Differential activation of placental unfolded protein response pathways implies heterogeneity in causation of early- and late-onset pre-eclampsia. J Pathol 2014; 234:262-276.
126. Wang Z, Wang H, Xu ZM, Ji YL, Chen YH, Zhang ZH, Zhang C, Meng XH, Zhao M, Xu DX: Cadmium-induced teratogenicity: association with ROS-mediated endoplasmic reticulum stress in placenta. Toxicol Appl Pharmacol 2012; 259:236-247.
127. Shkoda A, Ruiz PA, Daniel H, Kim SC, Rogler G, Sartor RB, Haller D: Interleukin-10 blocked endoplasmic reticulum stress in intestinal epithelial cells: impact on chronic inflammation. Gastroenterology 2007; 132:190-207.
128. Levine B, Deretic V: Unveiling the roles of autophagy in innate and adaptive immunity. Nat Rev Immunol 2007; 7:767-777.
129. Hung TH, Hsieh TT, Chen SF, Li MJ, Yeh YL: Autophagy in the Human Placenta throughout Gestation. PLoS One 2013; 8:e83475.
130. Harris J: Autophagy and cytokines. Cytokine 2011; 56:140-144.
131. Park HJ, Lee SJ, Kim SH, Han J, Bae J, Kim SJ, Park CG, Chun T: IL-10 inhibits the starvation induced autophagy in macrophages via class I phosphatidylinositol 3-kinase (PI3K) pathway. Mol Immunol 2011; 48:720-727.
132. Van Grol J, Subauste C, Andrade RM, Fujinaga K, Nelson J, Subauste CS: HIV-1 inhibits autophagy in bystander macrophage/monocytic cells through Src-Akt and STAT3. PLoS One 2010; 5:e11733.
133. Wang L, Zhang H, Qian J, Wang K, Zhu J: Interleukin-10 blocks in vitro replication of human cytomegalovirus by inhibiting the virus-induced autophagy in MRC5 cells. Biochem Biophys Res Commun 2014; 448:448-453.
134. Liu C, Gao Y, Barrett J, Hu B: Autophagy and protein aggregation after brain ischemia. J Neurochem 2010; 115:68-78.
135. Luo T, Park Y, Sun X, Liu C, Hu B: Protein misfolding, aggregation, and autophagy after brain ischemia. Transl Stroke Res 2013; 4:581-588.
136. Hung TH, Chen SF, Lo LM, Li MJ, Yeh YL, Hsieh TT: Increased autophagy in placentas of intrauterine growth-restricted pregnancies. PLoS One 2012; 7:e40957.
137. Oh SY, Choi SJ, Kim KH, Cho EY, Kim JH, Roh CR: Autophagy-related proteins, LC3 and Beclin-1, in placentas from pregnancies complicated by preeclampsia. Reprod Sci 2008; 15:912-920.
138. Saito S, Nakashima A: A review of the mechanism for poor placentation in early-onset preeclampsia: the role of autophagy in trophoblast invasion and vascular remodeling. J Reprod Immunol 2014; 101-102:80-88.
139. Nakashima A, Yamanaka-Tatematsu M, Fujita N, Koizumi K, Shima T, Yoshida T, Nikaido T, Okamoto A, Yoshimori T, Saito S: Impaired autophagy by soluble endoglin, under physiological hypoxia in early pregnant period, is involved in poor placentation in preeclampsia. Autophagy 2013; 9:303-316.
140. Kanninen T, Jayaram A, Jaffe Lifshitz S, Witkin S: Altered autophagy induction by sera from pregnant women with pre-eclampsia: a case-control study. BJOG 2014; 121:958-964.