Inflammasome activation during spontaneous preterm labor with intra-amniotic infection or sterile intra-amniotic inflammation

American Journal of Reproductive Immunology

Volumn 80, Issue 5, 2018, Pages

  Gomez Lopez, Nardhy ^a,b,e   Romero, Roberto ^a,b,c,d,e   Panaitescu, Bogdan ^a,b,e   Leng, Yaozhu ^a,b,e   Xu, Yi ^a,b,e   Tarca, Adi L ^a,b,e   Faro, Jonathan ^a,b,e   Pacora, Percy ^a,b,e   Hassan, Sonia S ^a,b,e   Hsu, Chaur Dong ^b  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

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

^c UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^d MICHIGAN STATE UNIVERSITY   (United States)

^e Wayne State University ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APOPTOSIS ASSOCIATED SPECK LIKE PROTEIN CONTAINING A CARD; CELL PROTEIN; INFLAMMASOME; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; INTERLEUKIN 6; UNCLASSIFIED DRUG; CASPASE RECRUITMENT DOMAIN SIGNALING PROTEIN; PYCARD PROTEIN, HUMAN;

ADULT; AMNION FLUID; AMNION FLUID LEVEL; AMNIONITIS; ARTICLE; CHORIOAMNIONITIS; CLINICAL ARTICLE; COMPARATIVE STUDY; CONTROLLED STUDY; CROSS-SECTIONAL STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; EXTRACELLULAR SPACE; FEMALE; FETUS MEMBRANE; GESTATIONAL AGE; HUMAN; HUMAN TISSUE; IMMUNOFLUORESCENCE; INFLAMMATION; INTRA AMNIOTIC INFECTION; LEUKOCYTE COUNT; PLACENTA; PREMATURE LABOR; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETROSPECTIVE STUDY; STERILE INTRA AMNIOTIC INFLAMMATION; TERM BIRTH; YOUNG ADULT; AMNION; IMMUNOLOGY; INFECTION; METABOLISM; PREGNANCY; SPONTANEOUS ABORTION;

ABORTION, SPONTANEOUS; ADULT; AMNION; AMNIOTIC FLUID; CARD SIGNALING ADAPTOR PROTEINS; CASPASE 1; CROSS-SECTIONAL STUDIES; FEMALE; HUMANS; INFECTION; INFLAMMASOMES; INFLAMMATION; INTERLEUKIN-1BETA; INTERLEUKIN-6; PLACENTA; PREGNANCY; RETROSPECTIVE STUDIES; YOUNG ADULT;

EID: 85053459491     PISSN: 10467408     EISSN: 16000897     Source Type: Journal    
DOI: 10.1111/aji.13049     Document Type: Article

References (162)

1. Blencowe H, Cousens S, Oestergaard MZ, et al. National, regional, and worldwide estimates of preterm birth rates in the year 2010 with time trends since 1990 for selected countries: a systematic analysis and implications. Lancet. 2012;379:2162-2172.
2. Liu L, Oza S, Hogan D, et al. Global, regional, and national causes of child mortality in 2000-13, with projections to inform post-2015 priorities: An updated systematic analysis. Lancet. 2015;385:430-440.
3. Manuck TA, Rice MM, Bailit JL, et al. Eunice Kennedy Shriver National Institute of Child H, Human Development Maternal-Fetal Medicine Units N: Preterm neonatal morbidity and mortality by gestational age: A contemporary cohort. Am J Obstet Gynecol. 2016;215:103 e101-103 e114.
4. Romero R, Mazor M, Munoz H, Gomez R, Galasso M, Sherer DM. The preterm labor syndrome. Ann N Y Acad Sci. 1994;734:414-429.
5. Berkowitz GS, Blackmore-Prince C, Lapinski RH, Savitz DA. Risk factors for preterm birth subtypes. Epidemiology. 1998;9:279-285.
6. Moutquin JM. Classification and heterogeneity of preterm birth. BJOG. 2003;110(Suppl 20):30-33.
7. Goldenberg RL, Culhane JF, Iams JD, Romero R. Epidemiology and causes of preterm birth. Lancet. 2008;371:75-84.
8. Muglia LJ, Katz M. The enigma of spontaneous preterm birth. N Engl J Med. 2010;362:529-535.
9. Romero R, Mazor M, Wu YK, et al. Infection in the pathogenesis of preterm labor. Semin Perinatol. 1988;12:262-279.
10. Gomez R, Romero R, Edwin SS, David C. Pathogenesis of preterm labor and preterm premature rupture of membranes associated with intraamniotic infection. Infect Dis Clin North Am. 1997;11:135-176.
11. 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.
12. Romero R, Miranda J, Chaiworapongsa T, et al. A novel molecular microbiologic technique for the rapid diagnosis of microbial invasion of the amniotic cavity and intra-amniotic infection in preterm labor with intact membranes. Am J Reprod Immunol. 2014;71:330-358.
13. Romero R, Miranda J, Chaiworapongsa T, et al. Prevalence and clinical significance of sterile intra-amniotic inflammation in patients with preterm labor and intact membranes. Am J Reprod Immunol. 2014;72:458-474.
14. Romero R, Miranda J, Chaiworapongsa T, et al. Sterile intra-amniotic inflammation in asymptomatic patients with a sonographic short cervix: prevalence and clinical significance. J Matern Fetal Neonatal Med. 2014;24:1-17.
15. Romero R, Miranda J, Chaemsaithong P, et al. Sterile and microbial-associated intra-amniotic inflammation in preterm prelabor rupture of membranes. J Matern Fetal Neonatal Med. 2015;28:1394-1409.
16. Romero R, Miranda J, Kusanovic JP, et al. Clinical chorioamnionitis at term I: microbiology of the amniotic cavity using cultivation and molecular techniques. J Perinat Med. 2015;43:19-36.
17. Romero R, Chaemsaithong P, Korzeniewski SJ, et al. Clinical chorioamnionitis at term II: the intra-amniotic inflammatory response. J Perinat Med. 2016;44:5-22.
18. Romero R, Chaemsaithong P, Korzeniewski SJ, et al. Clinical chorioamnionitis at term III: how well do clinical criteria perform in the identification of proven intra-amniotic infection? J Perinat Med. 2016;44:23-32.
19. Romero R, Chaemsaithong P, Docheva N, et al. Clinical chorioamnionitis at term IV: the maternal plasma cytokine profile. J Perinat Med. 2016;44:77-98.
20. Romero R, Chaemsaithong P, Docheva N, et al. Clinical chorioamnionitis at term V: umbilical cord plasma cytokine profile in the context of a systemic maternal inflammatory response. J Perinat Med. 2016;44:53-76.
21. Romero R, Chaemsaithong P, Docheva N, et al. Clinical chorioamnionitis at term VI: acute chorioamnionitis and funisitis according to the presence or absence of microorganisms and inflammation in the amniotic cavity. J Perinat Med. 2016;44:33-51.
22. Rubartelli A, Lotze MT. Inside, outside, upside down: damage-associated molecular-pattern molecules (DAMPs) and redox. Trends Immunol. 2007;28:429-436.
23. Lotze MT, Zeh HJ, Rubartelli A, et al. The grateful dead: damage-associated molecular pattern molecules and reduction/oxidation regulate immunity. Immunol Rev. 2007;220:60-81.
24. Oppenheim JJ, Yang D. Alarmins: chemotactic activators of immune responses. Curr Opin Immunol. 2005;17:359-365.
25. Romero R, Brody DT, Oyarzun E, et al. Infection and labor. III. Interleukin-1: a signal for the onset of parturition. Am J Obstet Gynecol. 1989;160:1117-1123.
26. Romero R, Mazor M, Brandt F, et al. Interleukin-1 alpha and interleukin-1 beta in preterm and term human parturition. Am J Reprod Immunol. 1992;27:117-123.
27. Friel LA, Romero R, Edwin S, et al. The calcium binding protein, S100B, is increased in the amniotic fluid of women with intra-amniotic infection/inflammation and preterm labor with intact or ruptured membranes. J Perinat Med. 2007;35:385-393.
28. Chaiworapongsa T, Erez O, Kusanovic JP, et al. Amniotic fluid heat shock protein 70 concentration in histologic chorioamnionitis, term and preterm parturition. J Matern Fetal Neonatal Med. 2008;21:449-461.
29. Romero R, Chaiworapongsa T, Alpay Savasan Z, 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.
30. Romero R, Chaiworapongsa T, Savasan ZA, et al. 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.
31. Gomez-Lopez N, Romero R, Plazyo O, et al. Intra-amniotic administration of HMGB1 induces spontaneous preterm labor and birth. Am J Reprod Immunol. 2016;75:3-7.
32. Plazyo O, Romero R, Unkel R, et al. HMGB1 induces an inflammatory response in the chorioamniotic membranes that is partially mediated by the inflammasome. Biol Reprod. 2016;95:130.
33. Gotsch F, Romero R, Chaiworapongsa T, 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.
34. Jaiswal MK, Agrawal V, Mallers T, Gilman-Sachs A, Hirsch E, Beaman KD. Regulation of apoptosis and innate immune stimuli in inflammation-induced preterm labor. J Immunol. 2013;191:5702-5713.
35. Brickle A, Tran HT, Lim R, Liong S, Lappas M. Autophagy, which is decreased in labouring fetal membranes, regulates IL-1beta production via the inflammasome. Placenta. 2015;36:1393-1404.
36. Modi BP, Teves ME, Pearson LN, et al. Mutations in fetal genes involved in innate immunity and host defense against microbes increase risk of preterm premature rupture of membranes (PPROM). Mol Genet Genomic Med. 2017;5:720-729.
37. Cross SN, Potter JA, Aldo P, et al. Viral infection sensitizes human fetal membranes to bacterial lipopolysaccharide by MERTK inhibition and inflammasome activation. J Immunol. 2017;199:2885-2895.
38. Strauss JF 3rd, Romero R, Gomez-Lopez N, et al. Spontaneous preterm birth: advances toward the discovery of genetic predisposition. Am J Obstet Gynecol. 2018;218(294–314):e292.
39. Lim R, Lappas M. NOD-like receptor pyrin domain-containing-3 (NLRP3) regulates inflammation-induced pro-labor mediators in human myometrial cells. Am J Reprod Immunol. 2018;79:e12825.
40. Martinon F, Burns K, Tschopp J. The inflammasome: a molecular platform triggering activation of inflammatory caspases and processing of proIL-beta. Mol Cell. 2002;10:417-426.
41. Petrilli V, Papin S, Tschopp J. The inflammasome. Curr Biol. 2005;15:R581.
42. Ogura Y, Sutterwala FS, Flavell RA. The inflammasome: first line of the immune response to cell stress. Cell. 2006;126:659-662.
43. Sharma D, Kanneganti TD. The cell biology of inflammasomes: Mechanisms of inflammasome activation and regulation. J Cell Biol. 2016;213:617-629.
44. Sutterwala FS, Ogura Y, Flavell RA. The inflammasome in pathogen recognition and inflammation. J Leukoc Biol. 2007;82:259-264.
45. Mariathasan S, Monack DM. Inflammasome adaptors and sensors: intracellular regulators of infection and inflammation. Nat Rev Immunol. 2007;7:31-40.
46. Franchi L, Eigenbrod T, Munoz-Planillo R, Nunez G. The inflammasome: a caspase-1-activation platform that regulates immune responses and disease pathogenesis. Nat Immunol. 2009;10:241-247.
47. Jha S, Ting JP. Inflammasome-associated nucleotide-binding domain, leucine-rich repeat proteins and inflammatory diseases. J Immunol. 2009;183:7623-7629.
48. Latz E. The inflammasomes: mechanisms of activation and function. Curr Opin Immunol. 2010;22:28-33.
49. Schroder K, Tschopp J. The inflammasomes. Cell. 2010;140:821-832.
50. Franchi L, Munoz-Planillo R, Reimer T, Eigenbrod T, Nunez G. Inflammasomes as microbial sensors. Eur J Immunol. 2010;40:611-615.
51. Lamkanfi M, Dixit VM. Modulation of inflammasome pathways by bacterial and viral pathogens. J Immunol. 2011;187:597-602.
52. Horvath GL, Schrum JE, De Nardo CM, Latz E. Intracellular sensing of microbes and danger signals by the inflammasomes. Immunol Rev. 2011;243:119-135.
53. Franchi L, Munoz-Planillo R, Nunez G. Sensing and reacting to microbes through the inflammasomes. Nat Immunol. 2012;13:325-332.
54. Rathinam VA, Vanaja SK, Fitzgerald KA. Regulation of inflammasome signaling. Nat Immunol. 2012;13:333-342.
55. Franchi L, Nunez G. Immunology. Orchestrating inflammasomes. Science. 2012;337:1299-1300.
56. Latz E, Xiao TS, Stutz A. Activation and regulation of the inflammasomes. Nat Rev Immunol. 2013;13:397-411.
57. Vanaja SK, Rathinam VA, Fitzgerald KA. Mechanisms of inflammasome activation: recent advances and novel insights. Trends Cell Biol. 2015;25:308-315.
58. Guo H, Callaway JB, Ting JP. Inflammasomes: mechanism of action, role in disease, and therapeutics. Nat Med. 2015;21:677-687.
59. Black RA, Kronheim SR, Merriam JE, March CJ, Hopp TP. A pre-aspartate-specific protease from human leukocytes that cleaves pro-interleukin-1 beta. J Biol Chem. 1989;264:5323-5326.
60. Kostura MJ, Tocci MJ, Limjuco G, et al. Identification of a monocyte specific pre-interleukin 1 beta convertase activity. Proc Natl Acad Sci U S A. 1989;86:5227-5231.
61. Thornberry NA, Bull HG, Calaycay JR, et al., et al. A novel heterodimeric cysteine protease is required for interleukin-1 beta processing in monocytes. Nature. 1992;356:768-774.
62. Cerretti DP, Kozlosky CJ, Mosley B, et al., et al. Molecular cloning of the interleukin-1 beta converting enzyme. Science. 1992;256:97-100.
63. Gu Y, Kuida K, Tsutsui H, et al. Activation of interferon-gamma inducing factor mediated by interleukin-1beta converting enzyme. Science. 1997;275:206-209.
64. Ghayur T, Banerjee S, Hugunin M, et al. Caspase-1 processes IFN-gamma-inducing factor and regulates LPS-induced IFN-gamma production. Nature. 1997;386:619-623.
65. Dinarello CA. Interleukin-1 beta, interleukin-18, and the interleukin-1 beta converting enzyme. Ann N Y Acad Sci. 1998;856:1-11.
66. Fantuzzi G, Dinarello CA. Interleukin-18 and interleukin-1 beta: two cytokine substrates for ICE (caspase-1). J Clin Immunol. 1999;19:1-11.
67. Sansonetti PJ, Phalipon A, Arondel J, et al. Caspase-1 activation of IL-1beta and IL-18 are essential for Shigella flexneri-induced inflammation. Immunity. 2000;12:581-590.
68. Kahlenberg JM, Lundberg KC, Kertesy SB, Qu Y, Dubyak GR. Potentiation of caspase-1 activation by the P2X7 receptor is dependent on TLR signals and requires NF-kappaB-driven protein synthesis. J Immunol. 2005;175:7611-7622.
69. Netea MG, van de Veerdonk FL, van der Meer JW, Dinarello CA, Joosten LA. Inflammasome-independent regulation of IL-1-family cytokines. Annu Rev Immunol. 2015;33:49-77.
70. Cookson BT, Brennan MA. Pro-inflammatory programmed cell death. Trends Microbiol. 2001;9:113-114.
71. Miao EA, Rajan JV, Aderem A. Caspase-1-induced pyroptotic cell death. Immunol Rev. 2011;243:206-214.
72. Shalini S, Dorstyn L, Dawar S, Kumar S. Old, new and emerging functions of caspases. Cell Death Differ. 2015;22:526-539.
73. Fernandes-Alnemri T, Wu J, Yu JW, et al. The pyroptosome: a supramolecular assembly of ASC dimers mediating inflammatory cell death via caspase-1 activation. Cell Death Differ. 2007;14:1590-1604.
74. Vajjhala PR, Mirams RE, Hill JM. Multiple binding sites on the pyrin domain of ASC protein allow self-association and interaction with NLRP3 protein. J Biol Chem. 2012;287:41732-41743.
75. Baroja-Mazo A, Martin-Sanchez F, Gomez AI, et al. The NLRP3 inflammasome is released as a particulate danger signal that amplifies the inflammatory response. Nat Immunol. 2014;15:738-748.
76. Franklin BS, Bossaller L, De Nardo D, et al. The adaptor ASC has extracellular and ‘prionoid’ activities that propagate inflammation. Nat Immunol. 2014;15:727-737.
77. Stutz A, Horvath GL, Monks BG, Latz E. ASC speck formation as a readout for inflammasome activation. Methods Mol Biol. 2013;1040:91-101.
78. Romero R, Xu Y, Plazyo O, et al. A role for the inflammasome in spontaneous labor at term. Am J Reprod Immunol. 2018;79:e12440.
79. Gomez-Lopez N, Romero R, Xu Y, et al. Inflammasome assembly in the chorioamniotic membranes during spontaneous labor at term. Am J Reprod Immunol. 2017;77.
80. Gomez-Lopez N, Romero R, Xu Y, et al. A role for the inflammasome in spontaneous labor at term with acute histologic chorioamnionitis. Reprod Sci. 2017;24:934-953.
81. Gomez-Lopez N, Romero R, Xu Y, et al. A role for the inflammasome in spontaneous preterm labor with acute histologic chorioamnionitis. Reprod Sci. 2017;24:1382-1401.
82. Panaitescu B, Romero R, Gomez-Lopez N, et al. In vivo evidence of inflammasome activation during spontaneous labor at term. J Matern Fetal Neonatal Med. 2018;17:1-14.
83. Combs CA, Gravett M, Garite TJ, et al. ProteoGenix/Obstetrix Collaborative Research N: Amniotic fluid infection, inflammation, and colonization in preterm labor with intact membranes. Am J Obstet Gynecol. 2014;210:125 e121-125 e115.
84. Romero R, Grivel JC, Tarca AL, et al. Evidence of perturbations of the cytokine network in preterm labor. Am J Obstet Gynecol. 2015;213:836 e831-836 e818.
85. DiGiulio DB, Romero R, Amogan HP, et al. Microbial prevalence, diversity and abundance in amniotic fluid during preterm labor: a molecular and culture-based investigation. PLoS ONE. 2008;3:e3056.
86. DiGiulio DB, Romero R, Kusanovic JP, 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.
87. DiGiulio DB, Gervasi M, Romero R, et al. Microbial invasion of the amniotic cavity in preeclampsia as assessed by cultivation and sequence-based methods. J Perinat Med. 2010;38:503-513.
88. DiGiulio DB, Gervasi MT, Romero R, et al. Microbial invasion of the amniotic cavity in pregnancies with small-for-gestational-age fetuses. J Perinat Med. 2010;38:495-502.
89. Yoon BH, Romero R, Moon JB, et al. Clinical significance of intra-amniotic inflammation in patients with preterm labor and intact membranes. Am J Obstet Gynecol. 2001;185:1130-1136.
90. Chaemsaithong P, Romero R, Korzeniewski SJ, et al. A rapid interleukin-6 bedside test for the identification of intra-amniotic inflammation in preterm labor with intact membranes. J Matern Fetal Neonatal Med. 2016;29:349-359.
91. Chaemsaithong P, Romero R, Korzeniewski SJ, et al. A point of care test for interleukin-6 in amniotic fluid in preterm prelabor rupture of membranes: a step toward the early treatment of acute intra-amniotic inflammation/infection. J Matern Fetal Neonatal Med. 2016;29:360-367.
92. Gomez-Lopez N, Romero R, Xu Y, et al. Are amniotic fluid neutrophils in women with intraamniotic infection and/or inflammation of fetal or maternal origin? Am J Obstet Gynecol. 2017;217:693. e1-693.e16.
93. Pacora P, Romero R, Erez O, et al. The diagnostic performance of the beta-glucan assay in the detection of intra-amniotic infection with Candida species. J Matern Fetal Neonatal Med. 2017;27:1-18.
94. Musilova I, Bestvina T, Hudeckova M, et al. Vaginal fluid IL-6 concentrations as a point-of-care test is of value in women with preterm PROM. Am J Obstet Gynecol. 2016. [Epub ahead of print].
95. Musilova I, Bestvina T, Hudeckova M, et al. Vaginal fluid interleukin-6 concentrations as a point-of-care test is of value in women with preterm prelabor rupture of membranes. Am J Obstet Gynecol. 2016;215:619. e1-619.e12.
96. Romero R, Quintero R, Nores J, et al. Amniotic fluid white blood cell count: a rapid and simple test to diagnose microbial invasion of the amniotic cavity and predict preterm delivery. Am J Obstet Gynecol. 1991;165:821-830.
97. Romero R, Jimenez C, Lohda AK, et al. Amniotic fluid glucose concentration: a rapid and simple method for the detection of intraamniotic infection in preterm labor. Am J Obstet Gynecol. 1990;163:968-974.
98. Romero R, Emamian M, Quintero R, et al. The value and limitations of the Gram stain examination in the diagnosis of intraamniotic infection. Am J Obstet Gynecol. 1988;159:114-119.
99. Kim CJ, Romero R, Chaemsaithong P, Chaiyasit N, Yoon BH, Kim YM. Acute chorioamnionitis and funisitis: definition, pathologic features, and clinical significance. Am J Obstet Gynecol. 2015;213:S29-S52.
100. Redline RW, Faye-Petersen O, Heller D, Qureshi F, Savell V, Vogler C. Society for pediatric pathology PSAFINC: amniotic infection syndrome: nosology and reproducibility of placental reaction patterns. Pediatr Dev Pathol. 2003;6:435-448.
101. Redline RW. Inflammatory responses in the placenta and umbilical cord. Semin Fetal Neonatal Med. 2006;11:296-301.
102. Redline RW. Classification of placental lesions. Am J Obstet Gynecol. 2015;213:S21-S28.
103. Khong TY, Mooney EE, Ariel I, et al. Sampling and definitions of placental lesions: Amsterdam placental workshop group consensus statement. Arch Pathol Lab Med. 2016;140:698-713.
104. Romero R, Kim YM, Pacora P, et al. The frequency and type of placental histologic lesions in term pregnancies with normal outcome. J Perinat Med. 2018;46:613-630.
105. Romero R, Chaemsaithong P, Chaiyasit N, et al. CXCL10 and IL-6: Markers of two different forms of intra-amniotic inflammation in preterm labor. Am J Reprod Immunol. 2017;78:1-17.
106. Pacora P, Romero R, Maymon E, et al. Participation of the novel cytokine interleukin 18 in the host response to intra-amniotic infection. Am J Obstet Gynecol. 2000;183:1138-1143.
107. Blanc WA. Amniotic infection syndrome; pathogenesis, morphology, and significance in circumnatal mortality. Clin Obstet Gynecol. 1959;2:705-734.
108. Russell P. Inflammatory lesions of the human placenta: Clinical significance of acute chorioamnionitis. Am J Diagn Gynecol Obstet. 1979;2:127-137.
109. Blanc WA. Pathology of the placenta and cord in ascending and in haematogenous infection. Ciba Found Symp. 1979;77:17-38.
110. Hillier SL, Martius J, Krohn M, Kiviat N, Holmes KK, Eschenbach DA. A case-control study of chorioamnionic infection and histologic chorioamnionitis in prematurity. N Engl J Med. 1988;319:972-978.
111. Hillier SL, Krohn MA, Kiviat NB, Watts DH, Eschenbach DA. Microbiologic causes and neonatal outcomes associated with chorioamnion infection. Am J Obstet Gynecol. 1991;165:955-961.
112. Romero R, Salafia CM, Athanassiadis AP, et al. The relationship between acute inflammatory lesions of the preterm placenta and amniotic fluid microbiology. Am J Obstet Gynecol. 1992;166:1382-1388.
113. Redline RW. Placental inflammation. Semin Neonatol. 2004;9:265-274.
114. Fox H, Sebire NJ. Infections and Inflammatory Lesions of the Placenta, In Pathology of the Placenta. 3rd edn. Edinburgh, UK: Elsevier Saunders; 2007:303-354.
115. Benirschke K, Burton G, Baergen R. Infectious Diseases. In Pathology of the Human Placenta. Berlin Heidelberg: Springer; 2012:557-655.
116. Anders AP, Gaddy JA, Doster RS, Aronoff DM. Current concepts in maternal-fetal immunology: Recognition and response to microbial pathogens by decidual stromal cells. Am J Reprod Immunol. 2017;77.
117. Lappas M. Caspase-1 activation is increased with human labour in foetal membranes and myometrium and mediates infection-induced interleukin-1beta secretion. Am J Reprod Immunol. 2014;71:189-201.
118. Gibbs RS, Blanco JD, St Clair PJ, Castaneda YS. Quantitative bacteriology of amniotic fluid from women with clinical intraamniotic infection at term. J Infect Dis. 1982;145:1-8.
119. Romero R, Sirtori M, Oyarzun E, et al. Infection and labor. V. Prevalence, microbiology, and clinical significance of intraamniotic infection in women with preterm labor and intact membranes. Am J Obstet Gynecol. 1989;161:817-824.
120. Yoneda N, Yoneda S, Niimi H, et al. Polymicrobial amniotic fluid infection with mycoplasma/ureaplasma and other bacteria induces severe intra-amniotic inflammation associated with poor perinatal prognosis in preterm labor. Am J Reprod Immunol. 2016;75:112-125.
121. Cox C, Saxena N, Watt AP, et al. The common vaginal commensal bacterium Ureaplasma parvum is associated with chorioamnionitis in extreme preterm labor. J Matern Fetal Neonatal Med. 2016;29:3646-3651.
122. Oh KJ, Kim SM, Hong JS, et al. Twenty-four percent of patients with clinical chorioamnionitis in preterm gestations have no evidence of either culture-proven intraamniotic infection or intraamniotic inflammation. Am J Obstet Gynecol. 2017;216:604.e601-604.e611.
123. Oh KJ, Hong JS, Romero R, Yoon BH. The frequency and clinical significance of intra-amniotic inflammation in twin pregnancies with preterm labor and intact membranes. J Matern Fetal Neonatal Med. 2017;1-15. [Epub ahead of print].
124. Marques LM, Rezende IS, Barbosa MS, et al. Ureaplasma diversum genome provides new insights about the interaction of the surface molecules of this bacterium with the host. PLoS ONE. 2016;11:e0161926.
125. Martinez-Varea A, Romero R, Xu Y, et al. Clinical chorioamnionitis at term VII: the amniotic fluid cellular immune response. J Perinat Med. 2017;45:523-538.
126. Gomez-Lopez N, Romero R, Garcia-Flores V, et al. Amniotic fluid neutrophils can phagocytize bacteria: A mechanism for microbial killing in the amniotic cavity. Am J Reprod Immunol. 2017;78.
127. Gomez-Lopez N, Romero R, Xu Y, et al. Neutrophil extracellular traps in the amniotic cavity of women with intra-amniotic infection: a new mechanism of host defense. Reprod Sci. 2017;24:1139-1153.
128. Gomez-Lopez N, Romero R, Xu Y, et al. The immunophenotype of amniotic fluid leukocytes in normal and complicated pregnancies. Am J Reprod Immunol. 2018;79:e12827.
129. Gomez-Lopez N, Romero R, Leng Y, et al. Neutrophil extracellular traps in acute chorioamnionitis: a mechanism of host defense. Am J Reprod Immunol. 2017;77.
130. Di Paolo NC, Shayakhmetov DM. Interleukin 1alpha and the inflammatory process. Nat Immunol. 2016;17:906-913.
131. Romero R, Mazor M, Tartakovsky B. Systemic administration of interleukin-1 induces preterm parturition in mice. Am J Obstet Gynecol. 1991;165:969-971.
132. 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.
133. Harris HE, Raucci A. Alarmin(g) news about danger: workshop on innate danger signals and HMGB1. EMBO Rep. 2006;7:774-778.
134. Wang H, Bloom O, Zhang M, et al. HMG-1 as a late mediator of endotoxin lethality in mice. Science. 1999;285:248-251.
135. Kanneganti TD, Body-Malapel M, Amer A, et al. Critical role for Cryopyrin/Nalp3 in activation of caspase-1 in response to viral infection and double-stranded RNA. J Biol Chem. 2006;281:36560-36568.
136. Koo IC, Wang C, Raghavan S, Morisaki JH, Cox JS, Brown EJ. ESX-1-dependent cytolysis in lysosome secretion and inflammasome activation during mycobacterial infection. Cell Microbiol. 2008;10:1866-1878.
137. Muruve DA, Petrilli V, Zaiss AK, et al. The inflammasome recognizes cytosolic microbial and host DNA and triggers an innate immune response. Nature. 2008;452:103-107.
138. Thomas PG, Dash P, Aldridge JR Jr, et al. The intracellular sensor NLRP3 mediates key innate and healing responses to influenza A virus via the regulation of caspase-1. Immunity. 2009;30:566-575.
139. Allen IC, Scull MA, Moore CB, et al. The NLRP3 inflammasome mediates in vivo innate immunity to influenza A virus through recognition of viral RNA. Immunity. 2009;30:556-565.
140. Duncan JA, Gao X, Huang MT, et al. Neisseria gonorrhoeae activates the proteinase cathepsin B to mediate the signaling activities of the NLRP3 and ASC-containing inflammasome. J Immunol. 2009;182:6460-6469.
141. Joly S, Ma N, Sadler JJ, Soll DR, Cassel SL, Sutterwala FS. Cutting edge: Candida albicans hyphae formation triggers activation of the Nlrp3 inflammasome. J Immunol. 2009;183:3578-3581.
142. Ichinohe T, Lee HK, Ogura Y, Flavell R, Iwasaki A. Inflammasome recognition of influenza virus is essential for adaptive immune responses. J Exp Med. 2009;206:79-87.
143. Menu P, Vince JE. The NLRP3 inflammasome in health and disease: the good, the bad and the ugly. Clin Exp Immunol. 2011;166:1-15.
144. Rathinam VA, Vanaja SK, Waggoner L, et al. TRIF licenses caspase-11-dependent NLRP3 inflammasome activation by gram-negative bacteria. Cell. 2012;150:606-619.
145. Clay GM, Sutterwala FS, Wilson ME. NLR proteins and parasitic disease. Immunol Res. 2014;59:142-152.
146. Martinon F, Petrilli V, Mayor A, Tardivel A, Tschopp J. Gout-associated uric acid crystals activate the NALP3 inflammasome. Nature. 2006;440:237-241.
147. Mariathasan S, Weiss DS, Newton K, et al. Cryopyrin activates the inflammasome in response to toxins and ATP. Nature. 2006;440:228-232.
148. Hornung V, Bauernfeind F, Halle A, et al. Silica crystals and aluminum salts activate the NALP3 inflammasome through phagosomal destabilization. Nat Immunol. 2008;9:847-856.
149. Dostert C, Petrilli V, Van Bruggen R, Steele C, Mossman BT, Tschopp J. Innate immune activation through Nalp3 inflammasome sensing of asbestos and silica. Science. 2008;320:674-677.
150. Cassel SL, Eisenbarth SC, Iyer SS, et al. The Nalp3 inflammasome is essential for the development of silicosis. Proc Natl Acad Sci U S A. 2008;105:9035-9040.
151. Yamasaki K, Muto J, Taylor KR, et al. NLRP3/cryopyrin is necessary for interleukin-1beta (IL-1beta) release in response to hyaluronan, an endogenous trigger of inflammation in response to injury. J Biol Chem. 2009;284:12762-12771.
152. Cassel SL, Joly S, Sutterwala FS. The NLRP3 inflammasome: a sensor of immune danger signals. Semin Immunol. 2009;21:194-198.
153. Cassel SL, Sutterwala FS. Sterile inflammatory responses mediated by the NLRP3 inflammasome. Eur J Immunol. 2010;40:607-611.
154. Leemans JC, Cassel SL, Sutterwala FS. Sensing damage by the NLRP3 inflammasome. Immunol Rev. 2011;243:152-162.
155. Bezbradica JS, Coll RC, Schroder K. Sterile signals generate weaker and delayed macrophage NLRP3 inflammasome responses relative to microbial signals. Cell Mol Immunol. 2017;14:118-126.
156. Gomez-Lopez N, Romero R, Plazyo O, et al. Preterm labor in the absence of acute histologic chorioamnionitis is characterized by cellular senescence of the chorioamniotic membranes. Am J Obstet Gynecol. 2017;217:592. e591-592 e517.
157. Yao Y, Chen S, Cao M, et al. Antigen-specific CD8(+) T cell feedback activates NLRP3 inflammasome in antigen-presenting cells through perforin. Nat Commun. 2017;8:15402.
158. Gomez-Lopez N, Vega-Sanchez R, Castillo-Castrejon M, Romero R, Cubeiro-Arreola K, Vadillo-Ortega F. Evidence for a role for the adaptive immune response in human term parturition. Am J Reprod Immunol. 2013;69:212-230.
159. Kim CJ, Romero R, Chaemsaithong P, Kim JS. Chronic inflammation of the placenta: definition, classification, pathogenesis, and clinical significance. Am J Obstet Gynecol. 2015;213:S53-S69.
160. Gomez-Lopez N, Romero R, Arenas-Hernandez M, et al. In vivo T-cell activation by a monoclonal alphaCD3epsilon antibody induces preterm labor and birth. Am J Reprod Immunol. 2016;76:386-390.
161. Gomez-Lopez N, Romero R, Arenas-Hernandez M, et al. In vivo activation of invariant natural killer T cells induces systemic and local alterations in T-cell subsets prior to preterm birth. Clin Exp Immunol. 2017;189:211-225.
162. Frascoli M, Coniglio L, Witt R, et al. Alloreactive fetal T cells promote uterine contractility in preterm labor via IFN-gamma and TNF-alpha. Sci Transl Med. 2018;10.