Interleukin-33 in the human placenta

Journal of Maternal-Fetal and Neonatal Medicine

Volumn 26, Issue 4, 2013, Pages 327-338

  Topping, Vanessa ^a,f   Romero, Roberto ^a,f   Than, Nandor Gabor ^a,b,f   Tarca, Adi L ^a,c,f   Xu, Zhonghui ^a,f   Kim, Sun Young ^a,f   Wang, Bing ^a,f   Yeo, Lami ^a,b,f   Kim, Chong Jai ^a,b,d,f   Hassan, Sonia S ^a,b,f   Kim, Jung Sun ^a,e,f  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^b WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c Wayne State University   (United States)

^d University of Ulsan College of Medicine   (South Korea)

^e Sungkyunkwan University School of Medicine   (South Korea)

^f HUTZEL HOSPITAL   (United States)

Author keywords

Alarmin; Chorioamnionitis; Interleukin 1 family; Pregnancy; Preterm birth; Preterm labor

Indexed keywords

CD14 ANTIGEN; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INTERLEUKIN 1 RECEPTOR; INTERLEUKIN 1BETA; INTERLEUKIN 33; PROTEIN IL1RL1; UNCLASSIFIED DRUG;

ADULT; ARTICLE; CELL NUCLEUS; CELLULAR DISTRIBUTION; CHORIOAMNIONITIS; CLINICAL ARTICLE; CONTROLLED STUDY; ENDOTHELIUM CELL; FEMALE; FETUS MEMBRANE; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; MACROPHAGE; MYOFIBROBLAST; PLACENTA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; UMBILICAL CORD; WHARTON JELLY;

ACUTE DISEASE; AMNION; ANTIGENS, CD14; CELL NUCLEUS; CHORIOAMNIONITIS; CHORION; CHRONIC DISEASE; CROSS-SECTIONAL STUDIES; ENDOTHELIAL CELLS; FEMALE; HUMANS; INTERLEUKINS; LABOR, OBSTETRIC; MACROPHAGES; MESENCHYMAL STROMAL CELLS; OBSTETRIC LABOR, PREMATURE; PLACENTA; PREGNANCY; RECEPTORS, CELL SURFACE; RNA, MESSENGER; UMBILICAL VEINS;

EID: 84873442131     PISSN: 14767058     EISSN: 14764954     Source Type: Journal    
DOI: 10.3109/14767058.2012.735724     Document Type: Article

References (159)

1. Romero R. Prenatal medicine: The child is the father of the man. 1996. J Matern Fetal Neonatal Med 2009;22:636-639
2. Di Renzo GC. The great obstetrical syndromes. J Matern Fetal Neonatal Med 2009;22:633-635
3. Gervasi MT, Chaiworapongsa T, Pacora P, Naccasha N, Yoon BH, Maymon E, Romero R. Phenotypic and metabolic characteristics of monocytes and granulocytes in preeclampsia. Am J Obstet Gynecol 2001;185:792-797
4. Sacks GP, Studena K, Sargent K, Redman CW. Normal pregnancy and preeclampsia both produce inflammatory changes in peripheral blood leukocytes akin to those of sepsis. Am J Obstet Gynecol 1998;179:80-86
5. Romero R, Espinoza J, Kusanovic JP, Gotsch F, Hassan S, Erez O, Chaiworapongsa T, Mazor M. The preterm parturition syndrome. BJOG 2006;113 SUPPL3:17-42
6. Gervasi MT, Chaiworapongsa T, Naccasha N, Blackwell S, Yoon BH, Maymon E, Romero R. Phenotypic and metabolic characteristics of maternal monocytes and granulocytes in preterm labor with intact membranes. Am J Obstet Gynecol 2001;185:1124-1129
7. Gervasi MT, Chaiworapongsa T, Naccasha N, Pacora P, Berman S, Maymon E, Kim JC, et al. Maternal intravascular inflammation in preterm premature rupture of membranes. J Matern Fetal Neonatal Med 2002;11:171-175
8. Erez O, Gotsch F, Mazaki-Tovi S, Vaisbuch E, Kusanovic JP, Kim CJ, Chaiworapongsa T, et al. Evidence of maternal platelet activation, excessive thrombin generation, and high amniotic fluid tissue factor immunoreactivity and functional activity in patients with fetal death. J Matern Fetal Neonatal Med 2009;22:672-687
9. Richani K, Romero R, Soto E, Espinoza J, Nien JK, Chaiworapongsa T, Refuerzo J, et al. Unexplained intrauterine fetal death is accompanied by activation of complement. J Perinat Med 2005;33:296-305
10. Blackwell S, Romero R, Chaiworapongsa T, Refuerzo J, Gervasi MT, Yoshimatsu J, Espinoza J, et al. Unexplained fetal death is associated with changes in the adaptive limb of the maternal immune response consistent with prior antigenic exposure. J Matern Fetal Neonatal Med 2003;14:241-246
11. Naccasha N, Gervasi MT, Chaiworapongsa T, Berman S, Yoon BH, Maymon E, Romero R. Phenotypic and metabolic characteristics of monocytes and granulocytes in normal pregnancy and maternal infection. Am J Obstet Gynecol 2001;185:1118-1123
12. OggG, Romero R, Chaiworapongsa T, Gervasi MT, Pacora P, Erez O, Kusanovic JP, et al. Leukocytes of pregnant women with small-forgestational age neonates have a different phenotypic and metabolic activity from those of women with preeclampsia. J Matern Fetal Neonatal Med 2010;23:476-487
13. Gotsch F, Romero R, Kusanovic JP, Mazaki-Tovi S, Pineles BL, Erez O, Espinoza J, Hassan SS. The fetal inflammatory response syndrome. Clin Obstet Gynecol 2007;50:652-683
14. Kim YM, Romero R, Chaiworapongsa T, Espinoza J, Mor G, Kim CJ. Dermatitis as a component of the fetal inflammatory response syndrome is associated with activation of Toll-like receptors in epidermal keratinocytes. Histopathology 2006;49:506-514
15. Madsen-Bouterse SA, Romero R, Tarca AL, Kusanovic JP, Espinoza J, Kim CJ, Kim JS, et al. The transcriptome of the fetal inflammatory response syndrome. Am J Reprod Immunol 2010;63:73-92
16. Kim SK, Romero R, Chaiworapongsa T, Kusanovic JP, Mazaki-Tovi S, Mittal P, Erez O, et al. Evidence of changes in the immunophenotype and metabolic characteristics (intracellular reactive oxygen radicals) of fetal, but not maternal, monocytes and granulocytes in the fetal inflammatory response syndrome. J Perinat Med 2009;37:543-552
17. Kim YM, Romero R, Oh SY, Kim CJ, Kilburn BA, Armant DR, Nien JK, et al. Toll-like receptor 4: A potential link between "danger signals," the innate immune system, and preeclampsia? Am J Obstet Gynecol 2005;193:921-927
18. Faupel-Badger JM, Fichorova RN, Allred EN, Hecht JL, Dammann O, Leviton A, McElrath TF. Cluster analysis of placental inflammatory proteins can distinguish preeclampsia from preterm labor and premature membrane rupture in singleton deliveries less than 28 weeks of gestation. Am J Reprod Immunol 2011;66:488-494
19. Centlow M, Wingren C, Borrebaeck C, Brownstein MJ, Hansson SR. Differential gene expression analysis of placentas with increased vascular resistance and pre-eclampsia using whole-genome microarrays. J Pregnancy 2011;2011:472354
20. Sitras V, Paulssen RH, Graas H, Leirvik J, Hanssen TA, Vtun A, Acharya G. Differential placental gene expression in severe preeclampsia. Placenta 2009;30:424-433
21. Redman CW, Sargent IL. Placental stress and pre-eclampsia: A revised view. Placenta 2009;30 SUPPLA:S38-S42
22. Cindrova-Davies T. Gabor Than Award Lecture 2008: Pre-eclampsia - from placental oxidative stress to maternal endothelial dysfunction. Placenta 2009;30 SUPPLA:S55-S65
23. Vkonyi T, Nagy B, Fe T, Tarca AL, Karzi K, Schler J, Hupuczi P, et al. Microarray profiling reveals that placental transcriptomes of early-onset HELLP syndrome and preeclampsia are similar. Placenta 2011;32 Suppl:S21-S29
24. Gersell DJ, Phillips NJ, Beckerman K. Chronic chorioamnionitis: A clinicopathologic study of 17 cases. Int J Gynecol Pathol 1991;10:217-229
25. Jacques SM, Qureshi F. Chronic chorioamnionitis: A clinicopathologic and immunohistochemical study. Hum Pathol 1998;29:1457-1461
26. Kim CJ, Romero R, Kusanovic JP, Yoo W, Dong Z, Topping V, Gotsch F, et al. The frequency, clinical significance, and pathological features of chronic chorioamnionitis: A lesion associated with spontaneous preterm birth. Mod Pathol 2010;23:1000-1011
27. Romero R, Espinoza J, Gonlves LF, Kusanovic JP, Friel L, Hassan S. The role of inflammation and infection in preterm birth. Semin Reprod Med 2007;25:21-39
28. Romero R, Espinoza J, Gonlves LF, Kusanovic JP, Friel LA, Nien JK. Inflammation in preterm and term labour and delivery. Semin Fetal Neonatal Med 2006;11:317-326
29. Romero R, Gotsch F, Pineles B, Kusanovic JP. Inflammation in pregnancy: Its roles in reproductive physiology, obstetrical complications, and fetal injury. Nutr Rev 2007;65:S194-S202
30. Romero R, Wu YK, Brody DT, Oyarzun E, Duff GW, Durum SK. Human decidua: A source of interleukin-1. Obstet Gynecol 1989;73:31-34
31. Romero R, Chaiworapongsa T, Savasan ZA, Hussein Y, Dong Z, Kusanovic JP, Kim CJ, Hassan SS. Clinical chorioamnionitis is characterized by changes in the expression of the alarmin HMGB1 and one of its receptors, sRAGE. J Matern Fetal Neonatal Med 2012;25:558-567
32. Lee J, Romero R, Xu Y, Kim JS, Park JY, Kusanovic JP, Chaiworapongsa T, et al. Maternal HLA panel-reactive antibodies in early gestation positively correlate with chronic chorioamnionitis: Evidence in support of the chronic nature of maternal anti-fetal rejection. Am J Reprod Immunol 2011;66:510-526
33. Lee J, Romero R, Xu Y, Kim JS, Topping V, Yoo W, Kusanovic JP, et al. A signature of maternal anti-fetal rejection in spontaneous preterm birth: Chronic chorioamnionitis, anti-human leukocyte antigen antibodies, and C4d. PLoS ONE 2011;6:e16806
34. Lee J, Romero R, Dong Z, Xu Y, Qureshi F, Jacques S, Yoo W, et al. Unexplained fetal death has a biological signature of maternal antifetal rejection: Chronic chorioamnionitis and alloimmune anti-human leucocyte antigen antibodies. Histopathology 2011;59:928-938
35. Goldenberg RL, Hauth JC, Andrews WW. Intrauterine infection and preterm delivery. N Engl J Med 2000;342:1500-1507
36. DiGiulio DB, Romero R, Amogan HP, Kusanovic JP, Bik EM, Gotsch F, Kim CJ, et al. Microbial prevalence, diversity and abundance in amniotic fluid during preterm labor: A molecular and culture-based investigation. PLoS ONE 2008;3:e3056
37. DiGiulio DB, Romero R, Kusanovic JP, Gez R, Kim CJ, Seok KS, Gotsch F, et al. Prevalence and diversity of microbes in the amniotic fluid, the fetal inflammatory response, and pregnancy outcome in women with preterm pre-labor rupture of membranes. Am J Reprod Immunol 2010;64:38-57
38. Kim SK, Romero R, Kusanovic JP, Erez O, Vaisbuch E, Mazaki-Tovi S, Gotsch F, et al. The prognosis of pregnancy conceived despite the presence of an intrauterine device (IUD). J Perinat Med 2010;38:45-53
39. Kim MJ, Romero R, Gervasi MT, Kim JS, Yoo W, Lee DC, Mittal P, et al. Widespread microbial invasion of the chorioamniotic membranes is a consequence and not a cause of intra-Amniotic infection. Lab Invest 2009;89:924-936
40. Seong HS, Lee SE, Kang JH, Romero R, Yoon BH. The frequency of microbial invasion of the amniotic cavity and histologic chorioamnionitis in women at term with intact membranes in the presence or absence of labor. Am J Obstet Gynecol 2008;199:375.e1-375.e5
41. Kusanovic JP, Espinoza J, Romero R, Gonlves LF, Nien JK, Soto E, Khalek N, et al. Clinical significance of the presence of amniotic fluid 'sludge' in asymptomatic patients at high risk for spontaneous preterm delivery. Ultrasound Obstet Gynecol 2007;30:706-714
42. Lee SE, Romero R, Kim CJ, Shim SS, Yoon BH. Funisitis in term pregnancy is associated with microbial invasion of the amniotic cavity and intra-Amniotic inflammation. J Matern Fetal Neonatal Med 2006;19:693-697
43. Hassan S, Romero R, Hendler I, Gomez R, Khalek N, Espinoza J, Nien JK, et al. A sonographic short cervix as the only clinical manifestation of intra-Amniotic infection. J Perinat Med 2006;34:13-19
44. Gez R, Romero R, Nien JK, Medina L, Carstens M, Kim YM, Chaiworapongsa T, et al. Idiopathic vaginal bleeding during pregnancy as the only clinical manifestation of intrauterine infection. J Matern Fetal Neonatal Med 2005;18:31-37
45. Espinoza J, Gonlves LF, Romero R, Nien JK, Stites S, Kim YM, Hassan S, et al. The prevalence and clinical significance of amniotic fluid 'sludge' in patients with preterm labor and intact membranes. Ultrasound Obstet Gynecol 2005;25:346-352
46. Blackwell S, Romero R, Chaiworapongsa T, Kim YM, Bujold E, Espinoza J, Camacho N, et al. Maternal and fetal inflammatory responses in unexplained fetal death. J Matern Fetal Neonatal Med 2003;14:151-157
47. Yoon BH, Romero R, Moon J, Chaiworapongsa T, Espinoza J, Kim YM, Edwin S, et al. Differences in the fetal interleukin-6 response to microbial invasion of the amniotic cavity between term and preterm gestation. J Matern Fetal Neonatal Med 2003;13:32-38
48. Romero R, Gomez R, Galasso M, Munoz H, Acosta L, Yoon BH, Svinarich D, Cotton DB. Macrophage inflammatory protein-1 alpha in term and preterm parturition: Effect of microbial invasion of the amniotic cavity. Am J Reprod Immunol 1994;32:108-113
49. Salafia CM, Weigl C, Silberman L. The prevalence and distribution of acute placental inflammation in uncomplicated term pregnancies. Obstet Gynecol 1989;73:383-389
50. Redline RW, Faye-Petersen O, Heller D, Qureshi F, Savell V, Vogler C; Society for Pediatric Pathology, Perinatal Section, Amniotic Fluid Infection Nosology Committee. Amniotic infection syndrome: Nosology and reproducibility of placental reaction patterns. Pediatr Dev Pathol 2003;6:435-448
51. Baumann P, Romero R. [Intra-Amniotic infection, cytokines and premature labor]. Wien Klin Wochenschr 1995;107:598-607
52. Bry K, Hallman M. Transforming growth factor-beta opposes the stimulatory effects of interleukin-1 and tumor necrosis factor on amnion cell prostaglandin E2 production: Implication for preterm labor. Am J Obstet Gynecol 1992;167:222-226
53. Chen FC, Sarioglu N, Bcher U, Dudenhausen JW. Lipopolysaccharide binding protein in the early diagnosis of intraamniotic infection of pregnant women with premature rupture of the membranes. J Perinat Med 2009;37:135-139
54. Fidel PL Jr, Romero R, Wolf N, Cutright J, Ramirez M, Araneda H, Cotton DB. Systemic and local cytokine profiles in endotoxin-induced preterm parturition in mice. Am J Obstet Gynecol 1994;170:1467-1475
55. Hillier SL, Witkin SS, Krohn MA, Watts DH, Kiviat NB, Eschenbach DA. The relationship of amniotic fluid cytokines and preterm delivery, amniotic fluid infection, histologic chorioamnionitis, and chorioamnion infection. Obstet Gynecol 1993;81:941-948
56. Keelan JA, Blumenstein M, Helliwell RJ, Sato TA, Marvin KW, Mitchell MD. Cytokines, prostaglandins and parturition-A review. Placenta 2003;24 SUPPLA:S33-S46
57. Maymon E, Romero R, Pacora P, Gomez R, Mazor M, Edwin S, Chaiworapongsa T, et al. A role for the 72 kDa gelatinase (MMP-2) and its inhibitor (TIMP-2) in human parturition, premature rupture of membranes and intraamniotic infection. J Perinat Med 2001;29:308-316
58. Moln M, Romero R, Hertelendy F. Interleukin-1 and tumor necrosis factor stimulate arachidonic acid release and phospholipid metabolism in human myometrial cells. Am J Obstet Gynecol 1993;169:825-829
59. Romero R, Brody DT, Oyarzun E, Mazor M, Wu YK, Hobbins JC, Durum SK. Infection and labor. III. Interleukin-1: A signal for the onset of parturition. Am J Obstet Gynecol 1989;160:1117-1123
60. Romero R, Durum S, Dinarello CA, Oyarzun E, Hobbins JC, Mitchell MD. Interleukin-1 stimulates prostaglandin biosynthesis by human amnion. Prostaglandins 1989;37:13-22
61. Romero R, Mazor M, Tartakovsky B. Systemic administration of interleukin-1 induces preterm parturition in mice. Am J Obstet Gynecol 1991;165:969-971
62. Romero R, Mazor M, Brandt F, Sepulveda W, Avila C, Cotton DB, Dinarello CA. Interleukin-1 alpha and interleukin-1 beta in preterm and term human parturition. Am J Reprod Immunol 1992;27:117-123
63. Sadowsky DW, Adams KM, Gravett MG, Witkin SS, Novy MJ. Preterm labor is induced by intraamniotic infusions of interleukin-1beta and tumor necrosis factor-Alpha but not by interleukin-6 or interleukin-8 in a nonhuman primate model. Am J Obstet Gynecol 2006;195:1578-1589
64. Bashiri A, Burstein E, Mazor M. Cerebral palsy and fetal inflammatory response syndrome: A review. J Perinat Med 2006;34:5-12
65. Hagberg H, Mallard C, Jacobsson B. Role of cytokines in preterm labour and brain injury. BJOG 2005;112 SUPPL1:16-18
66. Kannan S, Saadani-Makki F, Muzik O, Chakraborty P, Mangner TJ, Janisse J, Romero R, Chugani DC. Microglial activation in perinatal rabbit brain induced by intrauterine inflammation: Detection with 11C-®-PK11195 and small-Animal PET. J Nucl Med 2007;48:946-954
67. Kannan S, Saadani-Makki F, Balakrishnan B, Chakraborty P, Janisse J, Lu X, Muzik O, et al. Magnitude of [(11)C]PK11195 binding is related to severity of motor deficits in a rabbit model of cerebral palsy induced by intrauterine endotoxin exposure. Dev Neurosci 2011;33:231-240
68. Kannan S, Dai H, Navath RS, Balakrishnan B, Jyoti A, Janisse J, Romero R, Kannan RM. Dendrimer-based postnatal therapy for neuroinflammation and cerebral palsy in a rabbit model. Sci Transl Med 2012;4:130ra46
69. O'Shea TM, Klinepeter KL, Meis PJ, Dillard RG. Intrauterine infection and the risk of cerebral palsy in very low-birthweight infants. Paediatr Perinat Epidemiol 1998;12:72-83
70. Saadani-Makki F, Kannan S, Lu X, Janisse J, Dawe E, Edwin S, Romero R, Chugani D. Intrauterine administration of endotoxin leads to motor deficits in a rabbit model: A link between prenatal infection and cerebral palsy. Am J Obstet Gynecol 2008;199:651.e1-651.e7
71. Yoon BH, Kim CJ, Romero R, Jun JK, Park KH, Choi ST, Chi JG. Experimentally induced intrauterine infection causes fetal brain white matter lesions in rabbits. Am J Obstet Gynecol 1997;177:797-802
72. Yoon BH, Romero R, Park JS, Kim CJ, Kim SH, Choi JH, Han TR. Fetal exposure to an intra-Amniotic inflammation and the development of cerebral palsy at the age of three years. Am J Obstet Gynecol 2000;182:675-681
73. Jobe AH, Ikegami M. Antenatal infection/inflammation and postnatal lung maturation and injury. Respir Res 2001;2:27-32
74. Jobe AH. Antenatal associations with lung maturation and infection. J Perinatol 2005;25 SUPPL2:S31-S35
75. Kramer BW, Kallapur S, Newnham J, Jobe AH. Prenatal inflammation and lung development. Semin Fetal Neonatal Med 2009;14:2-7
76. Novy MJ, Duffy L, Axthelm MK, Sadowsky DW, Witkin SS, Gravett MG, Cassell GH, Waites KB. Ureaplasma parvum or Mycoplasma hominis as sole pathogens cause chorioamnionitis, preterm delivery, and fetal pneumonia in rhesus macaques. Reprod Sci 2009;16:56-70
77. Polglase GR, Dalton RG, Nitsos I, Knox CL, Pillow JJ, Jobe AH, Moss TJ, et al. Pulmonary vascular and alveolar development in preterm lambs chronically colonized with Ureaplasma parvum. Am J Physiol Lung Cell Mol Physiol 2010;299:L232-L241
78. Panzer U, Reinking RR, Steinmetz OM, Zahner G, Sudbeck U, Fehr S, Pfalzer B, et al. CXCR3 and CCR5 positive T-cell recruitment in acute human renal allograft rejection. Transplantation 2004;78:1341-1350
79. Tan J, Zhou G. Chemokine receptors and transplantation. Cell Mol Immunol 2005;2:343-349
80. Wysocki CA, Panoskaltsis-Mortari A, Blazar BR, Serody JS. Leukocyte migration and graft-Versus-host disease. Blood 2005;105:4191-4199
81. Piper KP, Horlock C, Curnow SJ, Arrazi J, Nicholls S, Mahendra P, Craddock C, Moss PA. CXCL10-CXCR3 interactions play an important role in the pathogenesis of acute graft-Versus-host disease in the skin following allogeneic stem-cell transplantation. Blood 2007;110:3827-3832
82. Loetscher M, Loetscher P, Brass N, Meese E, Moser B. Lymphocytespecific chemokine receptor CXCR3: Regulation, chemokine binding and gene localization. Eur J Immunol 1998;28:3696-3705
83. Garc-Lez MA, Schez-Madrid F, Rodruez-Frade JM, Mellado M, Acevedo A, Garc MI, Albar JP, et al. CXCR3 chemokine receptor distribution in normal and inflamed tissues: Expression on activated lymphocytes, endothelial cells, and dendritic cells. Lab Invest 2001;81:409-418
84. Kim MJ, Romero R, Kim CJ, Tarca AL, Chhauy S, LaJeunesse C, Lee DC, et al. Villitis of unknown etiology is associated with a distinct pattern of chemokine up-regulation in the feto-Maternal and placental compartments: Implications for conjoint maternal allograft rejection and maternal anti-fetal graft-Versus-host disease. J Immunol 2009;182:3919-3927
85. Xu Y, Tarquini F, Romero R, Kim CJ, Tarca AL, Bhatti G, Lee J, et al. Peripheral CD300a+CD8+ T lymphocytes with a distinct cytotoxic molecular signature increase in pregnant women with chronic chorioamnionitis. Am J Reprod Immunol 2012;67:184-197
86. Dinarello CA. The biological properties of interleukin-1. Eur Cytokine Netw 1994;5:517-531
87. Dinarello CA. Biologic basis for interleukin-1 in disease. Blood 1996;87:2095-2147
88. Dinarello CA. Interleukin-18, a proinflammatory cytokine. Eur Cytokine Netw 2000;11:483-486
89. Dunne A, O'Neill LA. The interleukin-1 receptor/Toll-like receptor superfamily: Signal transduction during inflammation and host defense. Sci STKE 2003;2003:re3
90. Dinarello CA. Interleukin-1. Cytokine Growth Factor Rev 1997;8:253-265
91. Schmitz J, Owyang A, Oldham E, Song Y, Murphy E, McClanahan TK, Zurawski G, et al. IL-33, an interleukin-1-like cytokine that signals via the IL-1 receptor-related protein ST2 and induces T helper type 2-Associated cytokines. Immunity 2005;23:479-490
92. Romero R, Parvizi ST, Oyarzun E, Mazor M, Wu YK, Avila C, Athanassiadis AP, Mitchell MD. Amniotic fluid interleukin-1 in spontaneous labor at term. J Reprod Med 1990;35:235-238
93. Kim MJ, Romero R, Gervasi MT, Kim JS, Yoo W, Lee DC, Mittal P, Erez O, Kusanovic JP, Hassan SS, Kim CJ. Widespread microbial invasion of the chorioamniotic membranes is a consequence and not a cause of intra-Amniotic infection. Lab Invest 2009;89:924-936
94. Mitchell MD, Romero RJ, Edwin SS, Trautman MS. Prostaglandins and parturition. Reprod Fertil Dev 1995;7:623-632
95. Belt AR, Baldassare JJ, Moln M, Romero R, Hertelendy F. The nuclear transcription factor NF-kappaB mediates interleukin-1beta-induced expression of cyclooxygenase-2 in human myometrial cells. Am J Obstet Gynecol 1999;181:359-366
96. Mitchell MD, Chang MC, Chaiworapongsa T, Lan HY, Helliwell RJ, Romero R, Sato TA. Identification of 9alpha,11beta-prostaglandin F2 in human amniotic fluid and characterization of its production by human gestational tissues. J Clin Endocrinol Metab 2005;90:4244-4248
97. Han YM, Romero R, Kim JS, Tarca AL, Kim SK, Draghici S, Kusanovic JP, et al. Region-Specific gene expression profiling: Novel evidence for biological heterogeneity of the human amnion. Biol Reprod 2008;79:954-961
98. Romero R, Sepulveda W, Mazor M, Brandt F, Cotton DB, Dinarello CA, Mitchell MD. The natural interleukin-1 receptor antagonist in term and preterm parturition. Am J Obstet Gynecol 1992;167:863-872
99. Fidel PL Jr, Romero R, Ramirez M, Cutright J, Edwin SS, LaMarche S, Cotton DB, Mitchell MD. Interleukin-1 receptor antagonist (IL-1ra) production by human amnion, chorion, and decidua. Am J Reprod Immunol 1994;32:1-7
100. Romero R, Gomez R, Galasso M, Mazor M, Berry SM, Quintero RA, Cotton DB. The natural interleukin-1 receptor antagonist in the fetal, maternal, and amniotic fluid compartments: The effect of gestational age, fetal gender, and intrauterine infection. Am J Obstet Gynecol 1994;171:912-921
101. Romero R, Tartakovsky B. The natural interleukin-1 receptor antagonist prevents interleukin-1-induced preterm delivery in mice. Am J Obstet Gynecol 1992;167:1041-1045
102. Fidel PL Jr, Romero R, Cutright J, Wolf N, Gomez R, Araneda H, Ramirez M, Yoon BH. Treatment with the interleukin-I receptor antagonist and soluble tumor necrosis factor receptor Fc fusion protein does not prevent endotoxin-induced preterm parturition in mice. J Soc Gynecol Investig 1997;4:22-26
103. Pacora P, Romero R, Maymon E, Gervasi MT, Gomez R, Edwin SS, Yoon BH. Participation of the novel cytokine interleukin 18 in the host response to intra-Amniotic infection. Am J Obstet Gynecol 2000;183:1138-1143
104. Wang X, Hagberg H, Mallard C, Zhu C, Hedtjn M, Tiger CF, Eriksson K, et al. Disruption of interleukin-18, but not interleukin-1, increases vulnerability to preterm delivery and fetal mortality after intrauterine inflammation. Am J Pathol 2006;169:967-976
105. Carriere V, Roussel L, Ortega N, Lacorre DA, Americh L, Aguilar L, Bouche G, Girard JP. IL-33, the IL-1-like cytokine ligand for ST2 receptor, is a chromatin-Associated nuclear factor in vivo. Proc Natl Acad Sci USA 2007;104:282-287
106. Palmer G, Gabay C. Interleukin-33 biology with potential insights into human diseases. Nat Rev Rheumatol 2011;7:321-329
107. Liew FY, Pitman NI, McInnes IB. Disease-Associated functions of IL-33: The new kid in the IL-1 family. Nat Rev Immunol 2010;10:103-110
108. Kurowska-Stolarska M, Hueber A, Stolarski B, McInnes IB. Interleukin-33: A novel mediator with a role in distinct disease pathologies. J Intern Med 2011;269:29-35
109. Pineles B, Romero R, Montenegro D, Tarca AL, Than NG, Hassan S, Gotsch F, Draghici S, Espinoza J. "The Inflammasome" in Human Parturition. Reprod Sci 2007;14:59A-60A.
110. Montenegro D, Romero R, Pineles B, Tarca AL, Madsen-Bouterse SA, Hassan S, Kusanovic JP, Draghici S, Espinoza J, Kim CJ. Differential expression of the inflammasome components in the fetal inflammatory response syndrome. Reprod. Sci 2007; 14:59A-60A.
111. Gotsch F, Romero R, Chaiworapongsa T, Erez O, Vaisbuch E, Espinoza J, Kusanovic JP, et al. Evidence of the involvement of caspase-1 under physiologic and pathologic cellular stress during human pregnancy: A link between the inflammasome and parturition. J Matern Fetal Neonatal Med 2008;21:605-616
112. Talabot-Ayer D, Lamacchia C, Gabay C, Palmer G. Interleukin-33 is biologically active independently of caspase-1 cleavage. J Biol Chem 2009;284:19420-19426
113. Lamkanfi M, Kanneganti TD, Van Damme P, Vanden Berghe T, Vanoverberghe I, Vandekerckhove J, Vandenabeele P, et al. Targeted peptidecentric proteomics reveals caspase-7 as a substrate of the caspase-1 inflammasomes. Mol Cell Proteomics 2008;7:2350-2363
114. Cayrol C, Girard JP. The IL-1-like cytokine IL-33 is inactivated after maturation by caspase-1. Proc Natl Acad Sci USA 2009;106:9021-9026
115. Lhi AU, Cullen SP, McNeela EA, Duriez PJ, Afonina IS, Sheridan C, Brumatti G, et al. Suppression of interleukin-33 bioactivity through proteolysis by apoptotic caspases. Immunity 2009;31:84-98
116. Hayakawa M, Hayakawa H, Matsuyama Y, Tamemoto H, Okazaki H, Tominaga S. Mature interleukin-33 is produced by calpain-Mediated cleavage in vivo. Biochem Biophys Res Commun 2009;387:218-222
117. Eigenbrod T, Park JH, Harder J, Iwakura Y, Nez G. Cutting edge: Critical role for mesothelial cells in necrosis-induced inflammation through the recognition of IL-1 alpha released from dying cells. J Immunol 2008;181:8194-8198
118. Sakurai T, He G, Matsuzawa A, Yu GY, Maeda S, Hardiman G, Karin M. Hepatocyte necrosis induced by oxidative stress and IL-1 alpha release mediate carcinogen-induced compensatory proliferation and liver tumorigenesis. Cancer Cell 2008;14:156-165
119. Mler S, Scaffidi P, Degryse B, Bonaldi T, Ronfani L, Agresti A, Beltrame M, Bianchi ME. New EMBO members' review: The double life of HMGB1 chromatin protein: Architectural factor and extracellular signal. EMBO J 2001;20:4337-4340
120. Klune JR, Dhupar R, Cardinal J, Billiar TR, Tsung A. HMGB1: Endogenous danger signaling. Mol Med 2008;14:476-484
121. Scaffidi P, Misteli T, Bianchi ME. Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature 2002;418:191-195
122. Kazama H, Ricci JE, Herndon JM, Hoppe G, Green DR, Ferguson TA. Induction of immunological tolerance by apoptotic cells requires caspase-Dependent oxidation of high-Mobility group box-1 protein. Immunity 2008;29:21-32
123. Oppenheim JJ, Yang D. Alarmins: Chemotactic activators of immune responses. Curr Opin Immunol 2005;17:359-365
124. Bianchi ME. DAMPs, PAMPs and alarmins: All we need to know about danger. J Leukoc Biol 2007;81:1-5
125. Moussion C, Ortega N, Girard JP. The IL-1-like cytokine IL-33 is constitutively expressed in the nucleus of endothelial cells and epithelial cells in vivo: A novel 'alarmin'? PLoS ONE 2008;3:e3331
126. Haraldsen G, Balogh J, Pollheimer J, Sponheim J, Khler AM. Interleukin-33 - Cytokine of dual function or novel alarmin? Trends Immunol 2009;30:227-233
127. Lamkanfi M, Dixit VM. IL-33 raises alarm. Immunity 2009;31:5-7
128. Romero R, Chaiworapongsa T, Alpay Savasan Z, Xu Y, Hussein Y, Dong Z, Kusanovic JP, et al. Damage-Associated molecular patterns (DAMPs) in preterm labor with intact membranes and preterm PROM: A study of the alarmin HMGB1. J Matern Fetal Neonatal Med 2011;24:1444-1455
129. Than NG, Kim SS, Abbas A, Han YM, Hotra J, Tarca AL, Erez O, et al. Chorioamnionitis and increased galectin-1 expression in PPROM -An anti-inflammatory response in the fetal membranes? Am J Reprod Immunol 2008;60:298-311
130. Redline RW, Heller D, Keating S, Kingdom J. Placental diagnostic criteria and clinical correlation-A workshop report. Placenta 2005;26 SUPPLA:S114-S117
131. Kim SY, Romero R, Tarca AL, Bhatti G, Lee J, Chaiworapongsa T, Hassan SS, Kim CJ. miR-143 regulation of prostaglandin-endoperoxidase synthase 2 in the amnion: Implications for human parturition at term. PLoS ONE 2011;6:e24131
132. Marin V, Kaplanski G, Gr S, Farnarier C, Bongrand P. Endothelial cell culture: Protocol to obtain and cultivate human umbilical endothelial cells. J Immunol Methods 2001;254:183-190
133. Baudin B, Bruneel A, Bosselut N, Vaubourdolle M. A protocol for isolation and culture of human umbilical vein endothelial cells. Nat Protoc 2007;2:481-485
134. Pinheiro J, Bornkamp B, Bretz F. Design and analysis of dose-finding studies combining multiple comparisons and modeling procedures. J Biopharm Stat 2006;16:639-656
135. Granne I, Southcombe JH, Snider JV, Tannetta DS, Child T, Redman CW, Sargent IL. ST2 and IL-33 in pregnancy and pre-eclampsia. PLoS ONE 2011;6:e24463
136. Khler AM, Pollheimer J, Balogh J, Sponheim J, Manley L, Sorensen DR, De Angelis PM, et al. Nuclear interleukin-33 is generally expressed in resting endothelium but rapidly lost upon angiogenic or proinflammatory activation. Am J Pathol 2008;173:1229-1242
137. Miller AM, Xu D, Asquith DL, Denby L, Li Y, Sattar N, Baker AH, et al. IL-33 reduces the development of atherosclerosis. J Exp Med 2008;205:339-346
138. Prontaine D, Lajoie-Kadoch S, Foley S, Audusseau S, Olivenstein R, Halayko AJ, Lemie C, et al. Increased expression of IL-33 in severe asthma: Evidence of expression by airway smooth muscle cells. J Immunol 2009;183:5094-5103
139. Mor G, Koga K. Macrophages and pregnancy. Reprod Sci 2008;15:435-436
140. Nagamatsu T, Schust DJ. The contribution of macrophages to normal and pathological pregnancies. Am J Reprod Immunol 2010;63:460-471
141. Nagamatsu T, Schust DJ. The immunomodulatory roles of macrophages at the maternal-fetal interface. Reprod Sci 2010;17:209-218
142. Svensson J, Jenmalm MC, Matussek A, Geffers R, Berg G, Ernerudh J. Macrophages at the fetal-Maternal interface express markers of alternative activation and are induced by M-CSF and IL-10. J Immunol 2011;187:3671-3682
143. McIntire RH, Petroff MG, Phillips TA, Hunt JS. In vitro models for studying human uterine and placental macrophages. Methods Mol Med 2006;122:123-148
144. Renaud SJ, Graham CH. The role of macrophages in utero-placental interactions during normal and pathological pregnancy. Immunol Invest 2008;37:535-564
145. Nile CJ, Barksby E, Jitprasertwong P, Preshaw PM, Taylor JJ. Expression and regulation of interleukin-33 in human monocytes. Immunology 2010;130:172-180
146. Baekkevold ES, Roussign M, Yamanaka T, Johansen FE, Jahnsen FL, Amalric F, Brandtzaeg P, et al. Molecular characterization of NF-HEV, a nuclear factor preferentially expressed in human high endothelial venules. Am J Pathol 2003;163:69-79
147. Sakashita M, Yoshimoto T, Hirota T, Harada M, Okubo K, Osawa Y, Fujieda S, et al. Association of serum interleukin-33 level and the interleukin-33 genetic variant with Japanese cedar pollinosis. Clin Exp Allergy 2008;38:1875-1881
148. Pushparaj PN, Tay HK, H'ng SC, Pitman N, Xu D, McKenzie A, Liew FY, Melendez AJ. The cytokine interleukin-33 mediates anaphylactic shock. Proc Natl Acad Sci USA 2009;106:9773-9778
149. Seidelin JB, Bjerrum JT, Coskun M, Widjaya B, Vainer B, Nielsen OH. IL-33 is upregulated in colonocytes of ulcerative colitis. Immunol Lett 2010;128:80-85
150. Palmer G, Talabot-Ayer D, Lamacchia C, Toy D, Seemayer CA, Viatte S, Finckh A, et al. Inhibition of interleukin-33 signaling attenuates the severity of experimental arthritis. Arthritis Rheum 2009;60:738-749
151. Kono H, Rock KL. How dying cells alert the immune system to danger. Nat Rev Immunol 2008;8:279-289
152. Matzinger P. Tolerance, danger, and the extended family. Annu Rev Immunol 1994;12:991-1045
153. Matzinger P. Friendly and dangerous signals: Is the tissue in control? Nat Immunol 2007;8:11-13
154. Sato S, St-Pierre C, Bhaumik P, Nieminen J. Galectins in innate immunity: Dual functions of host soluble beta-galactoside-binding lectins as damageassociated molecular patterns (DAMPs) and as receptors for pathogenassociated molecular patterns (PAMPs). Immunol Rev 2009;230:172-187
155. Balogh A, Pozsgay J, Matk J, Dong Z, Kim CJ, Vkonyi T, Sammar M, et al. Placental protein 13 (PP13/galectin-13) undergoes lipid raftassociated subcellular redistribution in the syncytiotrophoblast in preterm preeclampsia and HELLP syndrome. Am J Obstet Gynecol 2011;205:156.e1-156.14
156. Than NG, Romero R, Kim CJ, McGowen MR, Papp Z, Wildman DE. Galectins: Guardians of eutherian pregnancy at the maternal-fetal interface. Trends
157. Than NG, Erez O, Wildman DE, Tarca AL, Edwin SS, Abbas A, Hotra J, et al. Severe preeclampsia is characterized by increased placental expression of galectin-1. J Matern Fetal Neonatal Med 2008;21:429-442
158. Abrahams VM, Bole-Aldo P, Kim YM, Straszewski-Chavez SL, Chaiworapongsa T, Romero R, Mor G. Divergent trophoblast responses to bacterial products mediated by TLRs. J Immunol 2004;173:4286-4296
159. Koga K, Mor G. Toll-like receptors at the maternal-fetal interface in normal pregnancy and pregnancy disorders. Am J Reprod Immunol 2010;63:587-600