HMGB1 induces an inflammatory response in the chorioamniotic membranes that is partially mediated by the inflammasome

Biology of Reproduction

Volumn 95, Issue 6, 2016, Pages 1-14

  Plazyo, Olesya ^a,b,c   Romero, Roberto ^a,c,d,e   Unkel, Ronald ^a,b,c   Balancio, Amapola ^a,b,c   Mial, Tara N ^a,b,c   Xu, Yi ^a,b,c   Dong, Zhong ^a,b,c   Hassan, Sonia S ^a,b,c   Gomez Lopez, Nardhy ^a,b,c  

^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 SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^e MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

AIM2; Alarmins; Caspase 1; DAMPs; Interleukin 1b; Interleukin 6; MMP 9; NLRP3; NOD2; Parturition; Pregnancy; Preterm birth; Preterm labor; RAGE; Sterile inflammation; Sterile intra amniotic inflammation; TLR 2

Indexed keywords

ALARMIN; ALARMIN 2; CASPASE RECRUITMENT DOMAIN PROTEIN 15; CASPASE RECRUITMENT DOMAIN PROTEIN 4; CRYOPYRIN; GAMMA INTERFERON RECEPTOR 1; HIGH MOBILITY GROUP B1 PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INFLAMMASOME; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; INTERLEUKIN 6; MESSENGER RNA; TOLL LIKE RECEPTOR 2; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; AUTACOID;

ADULT; ARTICLE; CLINICAL ARTICLE; CYTOKINE RELEASE; FEMALE; FETUS MEMBRANE; GENE EXPRESSION REGULATION; HUMAN; INFLAMMATION; PREMATURE LABOR; PRIORITY JOURNAL; UPREGULATION; AMNION; CHEMICALLY INDUCED; CHORION; DRUG EFFECTS; METABOLISM; PHOSPHORYLATION; PREMATURITY; YOUNG ADULT;

ADULT; AMNION; CASPASE 1; CHORION; FEMALE; HMGB1 PROTEIN; HUMANS; INFLAMMASOMES; INFLAMMATION; INFLAMMATION MEDIATORS; PHOSPHORYLATION; PREMATURE BIRTH; UP-REGULATION; YOUNG ADULT;

EID: 85015407320     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.116.144139     Document Type: Article

References (154)

1. Liu L, Oza S, Hogan D, Perin J, Rudan I, Lawn JE, Cousens S, Mathers C, Black RE. 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.
2. Martin JA, Martin MPH, Hamilton BE, Osterman MJK. Births in the United States, 2015. NCHS Data Brief No. 258, 2016. http://www.cdc. gov/nchs/data/databriefs/db258.pdf. Accessed September 2016.
3. Societal costs of preterm birth. In: Behrman RE, Butler AS (eds.), Preterm Birth: Causes, Consequences, and Prevention. Washington DC: National Academic Press; 2007.
4. Lubow JM, How HY, Habli M, Maxwell R, Sibai BM. Indications for delivery and short-term neonatal outcomes in late preterm as compared with term births. Am J Obstet Gynecol 2009; 200:e30-e33.
5. Mwaniki MK, Atieno M, Lawn JE, Newton CR. Long-term neurodevelopmental outcomes after intrauterine and neonatal insults: a systematic review. Lancet 2012; 379:445-452.
6. Manuck TA, Sheng X, Yoder BA, Varner MW. Correlation between initial neonatal and early childhood outcomes following preterm birth. Am J Obstet Gynecol 2014; 210:426.
7. Goldenberg RL, Culhane JF, Iams JD, Romero R. Epidemiology and causes of preterm birth. Lancet 2008; 371:75-84.
8. Romero R, Dey SK, Fisher SJ. Preterm labor: one syndrome, many causes. Science 2014; 345:760-765.
9. Gravett MG, Witkin SS, Haluska GJ, Edwards JL, Cook MJ, Novy MJ. An experimental model for intraamniotic infection and preterm labor in rhesus monkeys. Am J Obstet Gynecol 1994; 171:1660-1667.
10. Baggia S, Gravett MG, Witkin SS, Haluska GJ, Novy MJ. Interleukin-1 beta intra-amniotic infusion induces tumor necrosis factor-alpha, prostaglandin production, and preterm contractions in pregnant rhesus monkeys. J Soc Gynecol Investig 1996; 3:121-126.
11. 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.
12. Presicce P, Senthamaraikannan P, Alvarez M, Rueda CM, Cappelletti M, Miller LA, Job AH, Chougnet CA, Kallapur SG. Neutrophil recruitment and activation in decidua with intra-amniotic IL-1beta in the preterm rhesus macaque. Biol Reprod 2015; 92:56.
13. Jacobsson B. Intra-amniotic infection and inflammation in preterm birth-is bacteria always the connection? Commentary on the article by Miralles et al. on page 570.Pediatr Res 2005; 57:473-474.
14. Romero R, Espinoza J, Goncalves LF, Kusanovic JP, Friel L, Hassan S. The role of inflammation and infection in preterm birth. Semin Reprod Med 2007; 25:21-39.
15. Matzinger P. An innate sense of danger. Semin Immunol 1998; 10: 399-415.
16. Lotze MT, Deisseroth A, Rubartelli A. Damage associated molecular pattern molecules. Clin Immunol 2007; 124:1-4.
17. Oppenheim JJ, Yang D. Alarmins: chemotactic activators of immune responses. Curr Opin Immunol 2005; 17:359-365.
18. Chen GY, Nunez G. Sterile inflammation: sensing and reacting to damage. Nat Rev Immunol 2010; 10:826-837.
19. Romero R, Miranda J, Chaiworapongsa T, Chaemsaithong P, Gotsch F, Dong Z, Ahmed AI, Yoon BH, Hassan SS, Kim CJ, Korzeniewski SJ, Yeo L. 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.
20. Romero R, Miranda J, Chaiworapongsa T, Korzeniewski SJ, Chaemsaithong P, Gotsch F, Dong Z, Ahmed AI, Yoon BH, Hassan SS, Kim CJ, Yeo L. 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.
21. Romero R, Miranda J, Chaiworapongsa T, Chaemsaithong P, Gotsch F, Dong Z, Ahmed AI, Yoon BH, Hassan SS, Kim CJ, Korzeniewski SJ, Yeo L, et al. Sterile intra-amniotic inflammation in asymptomatic patients with a sonographic short cervix: prevalence and clinical significance. J Matern Fetal Neonatal Med 2014; 28:1-17.
22. Romero R, Miranda J, Chaemsaithong P, Chaiworapongsa T, Kusanovic JP, Dong Z, Ahmed AI, Shaman M, Lannaman K, Yoon BH, Hassan SS, Kim CJ, et al. Sterile and microbial-associated intra-amniotic inflammation in preterm prelabor rupture of membranes. J Matern Fetal Neonatal Med 2015; 28:1394-1409.
23. Romero R, Grivel JC, Tarca AL, Chaemsaithong P, Xu Z, Fitzgerald W, Hassan SS, Chaiworapongsa T, Margolis L. Evidence of perturbations of the cytokine network in preterm labor. Am J Obstet Gynecol 2015. 213: 836.
24. Romero R, Miranda J, Kusanovic JP, Chaiworapongsa T, Chaemsaithong P, Martinez A, Gotsch F, Dong Z, Ahmed AI, Shaman M, Lannaman K, Yoon BH, et al. Clinical chorioamnionitis at term I: microbiology of the amniotic cavity using cultivation and molecular techniques. J Perinat Med 2015; 43:19-36.
25. Romero R, Chaemsaithong P, Korzeniewski SJ, Tarca AL, Bhatti G, Xu Z, Kusanovic JP, Dong Z, Docheva N, Martinez-Varea A, Yoon BH, Hassan SS, et al. Clinical chorioamnionitis at term II: the intra-amniotic inflammatory response. J Perinat Med 2016; 44:5-22.
26. Romero R, Chaemsaithong P, Korzeniewski SJ, Kusanovic JP, Docheva N, Martinez-Varea A, Ahmed AI, Yoon BH, Hassan SS, Chaiworapongsa T, Yeo L. 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.
27. Romero R, Chaemsaithong P, Docheva N, Korzeniewski SJ, Tarca AL, Bhatti G, Xu Z, Kusanovic JP, Dong Z, Chaiyasit N, Ahmed AI, Yoon BH, et al. Clinical chorioamnionitis at term IV: the maternal plasma cytokine profile. J Perinat Med 2016; 44:77-98.
28. Romero R, Chaemsaithong P, Docheva N, Korzeniewski SJ, Tarca AL, Bhatti G, Xu Z, Kusanovic JP, Chaiyasit N, Dong Z, Yoon BH, Hassan SS, 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.
29. Romero R, Chaemsaithong P, Docheva N, Korzeniewski SJ, Kusanovic JP, Yoon BH, Kim JS, Chaiyasit N, Ahmed AI, Qureshi F, Jacques SM, Kim CJ, 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.
30. 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.
31. Friel LA, Romero R, Edwin S, Nien JK, Gomez R, Chaiworapongsa T, Kusanovic JP, Tolosa JE, Hassan SS, Espinoza J. The calcium binding protein, S100B, is increased in the amniotic fluid of women with intraamniotic infection/inflammation and preterm labor with intact or ruptured membranes. J Perinat Med 2007; 35:385-393.
32. Chaiworapongsa T, Erez O, Kusanovic JP, Vaisbuch E, Mazaki-Tovi S, Gotsch F, Than NG, Mittal P, Kim YM, Camacho N, Edwin S, Gomez R, 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.
33. Romero R, Chaiworapongsa T, Alpay Savasan Z, Xu Y, Hussein Y, Dong Z, Kusanovic JP, Kim CJ, Hassan SS. 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.
34. 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.
35. Gomez-Lopez N, Romero R, Plazyo O, Panaitescu B, Furcron AE, Miller D, Roumayah T, Flom E, Hassan SS. Intra-amniotic administration of HMGB1 induces spontaneous preterm labor and birth. Am J Reprod Immunol 2016; 75:3-7.
36. Wang H, Bloom O, Zhang M, Vishnubhakat JM, Ombrellino M, Che J, Frazier A, Yang H, Ivanova S, Borovikova L, Manogue KR, Faist E, et al. HMG-1 as a late mediator of endotoxin lethality in mice. Science 1999; 285:248-251.
37. Lotze MT, Tracey KJ. High-mobility group box 1 protein (HMGB1): nuclear weapon in the immune arsenal. Nat Rev Immunol 2005; 5: 331-342.
38. Hori O, Brett J, Slattery T, Cao R, Zhang J, Chen JX, Nagashima M, Lundh ER, Vijay S, Nitecki D, Morser J, Stern D, Schmidt AM. The receptor for advanced glycation end products (RAGE) is a cellular binding site for amphoterin. Mediation of neurite outgrowth and coexpression of rage and amphoterin in the developing nervous system. J Biol Chem 1995; 270:25752-25761.
39. Park JS, Gamboni-Robertson F, He Q, Svetkauskaite D, Kim JY, Strassheim D, Sohn JW, Yamada S, Maruyama I, Banerjee A, Ishizaka A, Abraham E. High mobility group box 1 protein interacts with multiple Toll-like receptors. Am J Physiol Cell Physiol 2006; 290:C917-C924.
40. Andersson U, Wang H, Palmblad K, Aveberger AC, Bloom O, Erlandsson-Harris H, Janson A, Kokkola R, Zhang M, Yang H, Tracey KJ. High mobility group 1 protein (HMG-1) stimulates proinflammatory cytokine synthesis in human monocytes. J Exp Med 2000; 192:565-570.
41. Park JS, Arcaroli J, Yum HK, Yang H, Wang H, Yang KY, Choe KH, Strassheim D, Pitts TM, Tracey KJ, Abraham E. Activation of gene expression in human neutrophils by high mobility group box 1 protein. Am J Physiol Cell Physiol 2003; 284:C870-C879.
42. Orlova VV, Choi EY, Xie C, Chavakis E, Bierhaus A, Ihanus E, Ballantyne CM, Gahmberg CG, Bianchi ME, Nawroth PP, Chavakis T. A novel pathway of HMGB1-mediated inflammatory cell recruitment that requires Mac-1-integrin. EMBO J 2007; 26:1129-1139.
43. Messmer D, Yang H, Telusma G, Knoll F, Li J, Messmer B, Tracey KJ, Chiorazzi N. High mobility group box protein 1: an endogenous signal for dendritic cell maturation and Th1 polarization. J Immunol 2004; 173: 307-313.
44. Fiuza C, Bustin M, Talwar S, Tropea M, Gerstenberger E, Shelhamer JH, Suffredini AF. Inflammation-promoting activity of HMGB1 on human microvascular endothelial cells. Blood 2003; 101:2652-2660.
45. Pineles BL, Romero R, Montenegro D, Tarca AL, Than NG, Hassan S, Gotsch F, Draghici S, Espinoza J, Kim CJ. ''The inflammasome'' in human parturition. Reprod Sci 2007; 14:59A.
46. Gotsch F, Romero R, Chaiworapongsa T, Erez O, Vaisbuch E, Espinoza J, Kusanovic JP, Mittal P, Mazaki-Tovi S, Kim CJ, Kim JS, Edwin S, 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.
47. Romero R, Xu Y, Plazyo O, Chaemsaithong P, Chaiworapongsa T, Unkel R, Than NG, Chiang PJ, Dong Z, Xu Z, Tarca AL, Abrahams VM, et al. A role for the inflammasome in spontaneous labor at term. Am J Reprod Immunol (in press). Published online ahead of print 8 March 2016 as DOI: 10.1111/aji.12440.
48. 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.
49. Petrilli V, Papin S, Tschopp J. The inflammasome. Curr Biol 2005; 15: R581.
50. Ogura Y, Sutterwala FS, Flavell RA. The inflammasome: first line of the immune response to cell stress. Cell 2006; 126:659-662.
51. Mariathasan S, Monack DM. Inflammasome adaptors and sensors: intracellular regulators of infection and inflammation. Nat Rev Immunol 2007; 7:31-40.
52. Stutz A, Golenbock DT, Latz E. Inflammasomes: too big to miss. J Clin Invest 2009; 119:3502-3511.
53. 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.
54. Jha S, Ting JP. Inflammasome-associated nucleotide-binding domain, leucine-rich repeat proteins and inflammatory diseases. J Immunol 2009; 183:7623-7629.
55. Schroder K, Tschopp J. The inflammasomes. Cell 2010; 140:821-832.
56. Franchi L, Munoz-Planillo R, Reimer T, Eigenbrod T, Nunez G. Inflammasomes as microbial sensors. Eur J Immunol 2010; 40:611-615.
57. Gross O, Thomas CJ, Guarda G, Tschopp J. The inflammasome: an integrated view. Immunol Rev 2011; 243:136-151.
58. Lamkanfi M, Dixit VM. Modulation of inflammasome pathways by bacterial and viral pathogens. J Immunol 2011; 187:597-602.
59. 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.
60. van de Veerdonk FL, Netea MG, Dinarello CA, Joosten LA. Inflammasome activation and IL-1beta and IL-18 processing during infection. Trends Immunol 2011; 32:110-116.
61. Franchi L, Munoz-Planillo R, Nunez G. Sensing and reacting to microbes through the inflammasomes. Nat Immunol 2012; 13:325-332.
62. Franchi L, Nunez G. Immunology. Orchestrating inflammasomes. Science 2012; 337:1299-1300.
63. Henao-Mejia J, Elinav E, Strowig T, Flavell RA. Inflammasomes: far beyond inflammation. Nat Immunol 2012; 13:321-324.
64. Latz E, Xiao TS, Stutz A. Activation and regulation of the inflammasomes. Nat Rev Immunol 2013; 13:397-411.
65. Lamkanfi M, Dixit VM. Mechanisms and functions of inflammasomes. Cell 2014; 157:1013-1022.
66. Guo H, Callaway JB, Ting JP. Inflammasomes: mechanism of action, role in disease, and therapeutics. Nat Med 2015; 21:677-687.
67. Black RA, Kronheim SR, Merriam JE, March CJ, Hopp TP. A preaspartate-specific protease from human leukocytes that cleaves prointerleukin-1 beta. J Biol Chem 1989; 264:5323-5326.
68. Kostura MJ, Tocci MJ, Limjuco G, Chin J, Cameron P, Hillman AG, Chartrain NA, Schmidt JA. Identification of a monocyte specific preinterleukin 1 beta convertase activity. Proc Natl Acad Sci U S A 1989; 86:5227-5231.
69. Thornberry NA, Bull HG, Calaycay JR, Chapman KT, Howard AD, Kostura MJ, Miller DK, Molineaux SM, Weidner JR, Aunins J, Elliston KO, Ayala JM, et al. A novel heterodimeric cysteine protease is required for interleukin-1 beta processing in monocytes. Nature 1992; 356: 768-774.
70. Cerretti DP, Kozlosky CJ, Mosley B, Nelson N, Van Ness K, Greenstreet TA, March CJ, Kronheim SR, Druck T, Cannizzaro LA, Huebner K, Black RA. Molecular cloning of the interleukin-1 beta converting enzyme. Science 1992; 256:97-100.
71. Gu Y, Kuida K, Tsutsui H, Ku G, Hsiao K, Fleming MA, Hayashi N, Higashino K, Okamura H, Nakanishi K, Kurimoto M, Tanimoto T, et al. Activation of interferon-gamma inducing factor mediated by interleukin-1beta converting enzyme. Science 1997; 275:206-209.
72. Ghayur T, Banerjee S, Hugunin M, Butler D, Herzog L, Carter A, Quintal L, Sekut L, Talanian R, Paskind M, Wong W, Kamen R, et al. Caspase-1 processes IFN-gamma-inducing factor and regulates LPSinduced IFN-gamma production. Nature 1997; 386:619-623.
73. Dinarello CA. Interleukin-1 beta, interleukin-18, and the interleukin-1 beta converting enzyme. Ann N Y Acad Sci 1998; 856:1-11.
74. Fantuzzi G, Dinarello CA. Interleukin-18 and interleukin-1 beta: two cytokine substrates for ICE (caspase-1). J Clin Immunol 1999; 19:1-11.
75. 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.
76. American College of Obstetrics, Gynecology Committee on Practice Bulletins-Obstetrics. ACOG Practice Bulletin Number 49, December 2003: dystocia and augmentation of labor. Obstet Gynecol 2003; 102: 1445-1454.
77. Redline RW. Placental pathology: a systematic approach with clinical correlations. Placenta 2008; 29(Suppl A):S86-S91.
78. 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.
79. Menon R, Behnia F, Polettini J, Saade GR, Campisi J, Velarde M. Placental membrane aging and HMGB1 signaling associated with human parturition. Aging 2016; 8:216-230.
80. van Beijnum JR, Buurman WA, Griffioen AW. Convergence and amplification of toll-like receptor (TLR) and receptor for advanced glycation end products (RAGE) signaling pathways via high mobility group B1 (HMGB1). Angiogenesis 2008; 11:91-99.
81. Guey B, Bodnar M, Manie SN, Tardivel A, Petrilli V. Caspase-1 autoproteolysis is differentially required for NLRP1b and NLRP3 inflammasome function. Proc Natl Acad Sci U S A 2014; 111: 17254-17259.
82. He Y, Zeng MY, Yang D, Motro B, Nunez G. NEK7 is an essential mediator of NLRP3 activation downstream of potassium efflux. Nature 2016; 530:354-357.
83. Romero R, Chaiworapongsa T, Espinoza J, Gomez R, Yoon BH, Edwin S, Mazor M, Maymon E, Berry S. Fetal plasma MMP-9 concentrations are elevated in preterm premature rupture of the membranes. Am J Obstet Gynecol 2002; 187:1125-1130.
84. Ferrand PE, Parry S, Sammel M, Macones GA, Kuivaniemi H, Romero R, Strauss JF III. A polymorphism in the matrix metalloproteinase-9 promoter is associated with increased risk of preterm premature rupture of membranes in African Americans. Mol Hum Reprod 2002; 8: 494-501.
85. Romero R, Mazor M, Tartakovsky B. Systemic administration of interleukin-1 induces preterm parturition in mice. Am J Obstet Gynecol 1991; 165:969-971.
86. 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.
87. 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.
88. Martinon F, Tschopp J. Inflammatory caspases and inflammasomes: master switches of inflammation. Cell Death Differ 2007; 14:10-22.
89. Dinarello CA. Biologic basis for interleukin-1 in disease. Blood 1996; 87:2095-2147.
90. Coeshott C, Ohnemus C, Pilyavskaya A, Ross S, Wieczorek M, Kroona H, Leimer AH, Cheronis J. Converting enzyme-independent release of tumor necrosis factor alpha and IL-1beta from a stimulated human monocytic cell line in the presence of activated neutrophils or purified proteinase 3. Proc Natl Acad Sci U S A 1999; 96:6261-6266.
91. Sugawara S, Uehara A, Nochi T, Yamaguchi T, Ueda H, Sugiyama A, Hanzawa K, Kumagai K, Okamura H, Takada H. Neutrophil proteinase 3-mediated induction of bioactive IL-18 secretion by human oral epithelial cells. J Immunol 2001; 167:6568-6575.
92. Herzog C, Haun RS, Kaushal V, Mayeux PR, Shah SV, Kaushal GP. Meprin A and meprin alpha generate biologically functional IL-1beta from pro-IL-1beta. Biochem Biophys Res Commun 2009; 379:904-908.
93. Gomez-Lopez N, Romero R, Xu Y, Plazyo O, Unkel R, Than NG, Chaemsaithong P, Chaiworapongsa T, Dong Z, Tarca AL, Abrahams VM, Yeo L, et al. A role for the inflammasome in spontaneous labor at term with acute histologic chorioamnionitis. Reprod Sci (in press). Published online ahead of print 16 November 2016 as DOI: 10.1177/1933719116675058.
94. Gomez-Lopez N, Romero R, Xu Y, Plazyo O, Unkel R, Leng Y, Than NG, Chaiworapongsa T, Panaitescu B, Dong Z, Tarca AL, Abrahams VM, et al. A role for the inflammasome in spontaneous preterm labor with acute histologic chorioamnionitis. Reprod Sci (in press). DOI: 10. 1177/1933719116687656.
95. 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.
96. 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.
97. Hertelendy F, Romero R, Molnar M, Todd H, Baldassare JJ. Cytokineinitiated signal transduction in human myometrial cells. Am J Reprod Immunol 1993; 30:49-57.
98. Hertelendy F, Rastogi P, Molnar M, Romero R. Interleukin-1betainduced prostaglandin E2 production in human myometrial cells: role of a pertussis toxin-sensitive component. Am J Reprod Immunol 2001; 45: 142-147.
99. Belt AR, Baldassare JJ, Molnar 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.
100. Watari M, Watari H, DiSanto ME, Chacko S, Shi GP, Strauss JF III. Proinflammatory cytokines induce expression of matrix-metabolizing enzymes in human cervical smooth muscle cells. Am J Pathol 1999; 154:1755-1762.
101. Agostini L, Martinon F, Burns K, McDermott MF, Hawkins PN, Tschopp J. NALP3 forms an IL-1beta-processing inflammasome with increased activity in Muckle-Wells autoinflammatory disorder. Immunity 2004; 20:319-325.
102. Sutterwala FS, Ogura Y, Zamboni DS, Roy CR, Flavell RA. NALP3: a key player in caspase-1 activation. J Endotoxin Res 2006; 12:251-256.
103. Chae JJ, Cho YH, Lee GS, Cheng J, Liu PP, Feigenbaum L, Katz SI, Kastner DL. Gain-of-function pyrin mutations induce NLRP3 proteinindependent interleukin-1beta activation and severe autoinflammation in mice. Immunity 2011; 34:755-768.
104. Martinon F, Petrilli V, Mayor A, Tardivel A, Tschopp J. Gout-associated uric acid crystals activate the NALP3 inflammasome. Nature 2006; 440: 237-241.
105. Hornung V, Bauernfeind F, Halle A, Samstad EO, Kono H, Rock KL, Fitzgerald KA, Latz E. Silica crystals and aluminum salts activate the NALP3 inflammasome through phagosomal destabilization. Nat Immunol 2008; 9:847-856.
106. Mariathasan S, Weiss DS, Newton K, McBride J, O'Rourke K, Roose-Girma M, Lee WP, Weinrauch Y, Monack DM, Dixit VM. Cryopyrin activates the inflammasome in response to toxins and ATP. Nature 2006; 440:228-232.
107. Kool M, Petrilli V, De Smedt T, Rolaz A, Hammad H, van Nimwegen M, Bergen IM, Castillo R, Lambrecht BN, Tschopp J. Cutting edge: alum adjuvant stimulates inflammatory dendritic cells through activation of the NALP3 inflammasome. J Immunol 2008; 181:3755-3759.
108. Li H, Willingham SB, Ting JP, Re F. Cutting edge: inflammasome activation by alum and alum's adjuvant effect are mediated by NLRP3. J Immunol 2008; 181:17-21.
109. Eisenbarth SC, Colegio OR, O'Connor W, Sutterwala FS, Flavell RA. Crucial role for the Nalp3 inflammasome in the immunostimulatory properties of aluminium adjuvants. Nature 2008; 453:1122-1126.
110. Franchi L, Nunez G. The Nlrp3 inflammasome is critical for aluminium hydroxide-mediated IL-1beta secretion but dispensable for adjuvant activity. Eur J Immunol 2008; 38:2085-2089.
111. Demento SL, Eisenbarth SC, Foellmer HG, Platt C, Caplan MJ, Mark Saltzman W, Mellman I, Ledizet M, Fikrig E, Flavell RA, Fahmy TM. Inflammasome-activating nanoparticles as modular systems for optimizing vaccine efficacy. Vaccine 2009; 27:3013-3021.
112. Nakahira K, Haspel JA, Rathinam VA, Lee SJ, Dolinay T, Lam HC, Englert JA, Rabinovitch M, Cernadas M, Kim HP, Fitzgerald KA, Ryter SW, et al. Autophagy proteins regulate innate immune responses by inhibiting the release of mitochondrial DNA mediated by the NALP3 inflammasome. Nat Immunol 2011; 12:222-230.
113. Iyer SS, He Q, Janczy JR, Elliott EI, Zhong Z, Olivier AK, Sadler JJ, Knepper-Adrian V, Han R, Qiao L, Eisenbarth SC, Nauseef WM, et al. Mitochondrial cardiolipin is required for Nlrp3 inflammasome activation. Immunity 2013; 39:311-323.
114. O'Neill LA. Cardiolipin and the Nlrp3 inflammasome. Cell Metab 2013; 18:610-612.
115. Gurcel L, Abrami L, Girardin S, Tschopp J, van der Goot FG. Caspase-1 activation of lipid metabolic pathways in response to bacterial poreforming toxins promotes cell survival. Cell 2006; 126:1135-1145.
116. Munoz-Planillo R, Franchi L, Miller LS, Nunez G. A critical role for hemolysins and bacterial lipoproteins in Staphylococcus aureus-induced activation of the Nlrp3 inflammasome. J Immunol 2009; 183:3942-3948.
117. Bauernfeind FG, Horvath G, Stutz A, Alnemri ES, MacDonald K, Speert D, Fernandes-Alnemri T, Wu J, Monks BG, Fitzgerald KA, Hornung V, Latz E. Cutting edge: NF-kappaB activating pattern recognition and cytokine receptors license NLRP3 inflammasome activation by regulating NLRP3 expression. J Immunol 2009; 183:787-791.
118. Sutterwala FS, Haasken S, Cassel SL. Mechanism of NLRP3 inflammasome activation. Ann N Y Acad Sci 2014; 1319:82-95.
119. Franchi L, Eigenbrod T, Nunez G. Cutting edge: TNF-alpha mediates sensitization to ATP and silica via the NLRP3 inflammasome in the absence of microbial stimulation. J Immunol 2009; 183:792-796.
120. Kanneganti TD, Lamkanfi M, Nunez G. Intracellular NOD-like receptors in host defense and disease. Immunity 2007; 27:549-559.
121. Costello MJ, Joyce SK, Abrahams VM. NOD protein expression and function in first trimester trophoblast cells. Am J Reprod Immunol 2007; 57:67-80.
122. Kim YG, Park JH, Shaw MH, Franchi L, Inohara N, Nunez G. The cytosolic sensors Nod1 and Nod2 are critical for bacterial recognition and host defense after exposure to Toll-like receptor ligands. Immunity 2008; 28:246-257.
123. King AE, Horne AW, Hombach-Klonisch S, Mason JI, Critchley HO. Differential expression and regulation of nuclear oligomerization domain proteins NOD1 and NOD2 in human endometrium: a potential role in innate immune protection and menstruation. Mol Hum Reprod 2009; 15: 311-319.
124. Mulla MJ, Yu AG, Cardenas I, Guller S, Panda B, Abrahams VM. Regulation of Nod1 and Nod2 in first trimester trophoblast cells. Am J Reprod Immunol 2009; 61:294-302.
125. Franchi L, Warner N, Viani K, Nunez G. Function of Nod-like receptors in microbial recognition and host defense. Immunol Rev 2009; 227: 106-128.
126. Cardenas I, Mulla MJ, Myrtolli K, Sfakianaki AK, Norwitz ER, Tadesse S, Guller S, Abrahams VM. Nod1 activation by bacterial iE-DAP induces maternal-fetal inflammation and preterm labor. J Immunol 2011; 187: 980-986.
127. Kersse K, Bertrand MJ, Lamkanfi M, Vandenabeele P. NOD-like receptors and the innate immune system: coping with danger, damage and death. Cytokine Growth Factor Rev 2011; 22:257-276.
128. Shah A, Hirsch E. TRIF is an essential adaptor protein of TLR3 and NOD2 synergy in macrophages-a role for viral priming in inflammationinduced parturition. Am J Obstet Gynecol 2014; 210:S231-S232.
129. Hoang M, Potter JA, Gysler SM, Han CS, Guller S, Norwitz ER, Abrahams VM. Human fetal membranes generate distinct cytokine profiles in response to bacterial Toll-like receptor and nod-like receptor agonists. Biol Reprod 2014; 90:39.
130. Keestra-Gounder AM, Byndloss MX, Seyffert N, Young BM, Chavez-Arroyo A, Tsai AY, Cevallos SA, Winter MG, Pham OH, Tiffany CR, de Jong MF, Kerrinnes T, et al. NOD1 and NOD2 signalling links ER stress with inflammation. Nature 2016; 532:394-397.
131. Conforti-Andreoni C, Beretta O, Licandro G, Qian HL, Urbano M, Vitulli F, Ricciardi-Castagnoli P, Mortellaro A. Synergism of NOD2 and NLRP3 activators promotes a unique transcriptional profile in murine dendritic cells. J Leukoc Biol 2010; 88:1207-1216.
132. Lappas M. NOD1 and NOD2 regulate proinflammatory and prolabor mediators in human fetal membranes and myometrium via nuclear factorkappa B. Biol Reprod 2013; 89:14.
133. Fernandes-Alnemri T, Wu J, Yu JW, Datta P, Miller B, Jankowski W, Rosenberg S, Zhang J, Alnemri ES. The pyroptosome: a supramolecular assembly of ASC dimers mediating inflammatory cell death via caspase-1 activation. Cell Death Differ 2007; 14:1590-1604.
134. Martinon F, Tschopp J. Inflammatory caspases: linking an intracellular innate immune system to autoinflammatory diseases. Cell 2004; 117: 561-574.
135. 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.
136. Wu D, Choi JC, Coselli J, Shen YH, LeMaire SA. NLRP3 inflammasome activates matrix metalloproteinase-9: potential role in smooth muscle cell dysfunction in thoracic aortic disease. J Surg Res 2013; 179:204.
137. Gross J, Lapiere CM. Collagenolytic activity in amphibian tissues: a tissue culture assay. Proc Natl Acad Sci U S A 1962; 48:1014-1022.
138. Woessner JF Jr. Matrix metalloproteinases and their inhibitors in connective tissue remodeling. FASEB J 1991; 5:2145-2154.
139. Vu TH, Werb Z. Matrix metalloproteinases: effectors of development and normal physiology. Genes Dev 2000; 14:2123-2133.
140. Light A, Hammes SR. LH-Induced steroidogenesis in the mouse ovary, but not testis, requires matrix metalloproteinase 2-and 9-mediated cleavage of upregulated EGF receptor ligands. Biol Reprod 2015; 93:65.
141. Nguyen TT, Shynlova O, Lye SJ. Matrix metalloproteinase expression in the rat myometrium during pregnancy, term labor, and postpartum. Biol Reprod 2016; 95:24.
142. Sopata I, Wize J. A latent gelatin specific proteinase of human leucocytes and its activation. Biochim Biophys Acta 1979; 571:305-312.
143. Athayde N, Edwin SS, Romero R, Gomez R, Maymon E, Pacora P, Menon R. A role for matrix metalloproteinase-9 in spontaneous rupture of the fetal membranes. Am J Obstet Gynecol 1998; 179:1248-1253.
144. Athayde N, Edwin SS, Pacora P, Romero R. Human decidual cells respond to lipopolysaccharide, proinflammatory cytokines (interleukin 1-beta and tumor necrosis factor-alpha) and interleukin-8 with release of matrix metalloproteinase-9. In: The 45th Annual Meeting of the Society of Gynecologic Investigation, Atlanta, GA. 1998; 5:62A-63A.
145. Athayde N, Romero R, Gomez R, Maymon E, Pacora P, Mazor M, Yoon BH, Fortunato S, Menon R, Ghezzi F, Edwin SS. Matrix metalloproteinases-9 in preterm and term human parturition. J Matern Fetal Med 1999; 8:213-219.
146. Maymon E, Romero R, Pacora P, Gervasi MT, Gomez R, Edwin SS, Yoon BH. Evidence of in vivo differential bioavailability of the active forms of matrix metalloproteinases 9 and 2 in parturition, spontaneous rupture of membranes, and intra-amniotic infection. Am J Obstet Gynecol 2000; 183:887-894.
147. Sorokin Y, Romero R, Mele L, Wapner RJ, Iams JD, Dudley DJ, Spong CY, Peaceman AM, Leveno KJ, Harper M, Caritis SN, Miodovnik M, et al. Maternal serum interleukin-6, C-reactive protein, and matrix metalloproteinase-9 concentrations as risk factors for preterm birth ≤32 weeks and adverse neonatal outcomes. Am J Perinatol 2010; 27:631-640.
148. Osmers RG, Blaser J, Kuhn W, Tschesche H. Interleukin-8 synthesis and the onset of labor. Obstet Gynecol 1995; 86:223-229.
149. Vadillo-Ortega F, Gonzalez-Avila G, Furth EE, Lei H, Muschel RJ, Stetler-Stevenson WG, Strauss JF III. 92-kd type IV collagenase (matrix metalloproteinase-9) activity in human amniochorion increases with labor. Am J Pathol 1995; 146:148-156.
150. Vadillo-Ortega F, Hernandez A, Gonzalez-Avila G, Bermejo L, Iwata K, Strauss JF III. Increased matrix metalloproteinase activity and reduced tissue inhibitor of metalloproteinases-1 levels in amniotic fluids from pregnancies complicated by premature rupture of membranes. Am J Obstet Gynecol 1996; 174:1371-1376.
151. Xu P, Alfaidy N, Challis JR. Expression of matrix metalloproteinase (MMP)-2 and MMP-9 in human placenta and fetal membranes in relation to preterm and term labor. J Clin Endocrinol Metab 2002; 87:1353-1361.
152. Gomez-Lopez N, Vadillo-Perez L, Hernandez-Carbajal A, Godines-Enriquez M, Olson DM, Vadillo-Ortega F. Specific inflammatory microenvironments in the zones of the fetal membranes at term delivery. Am J Obstet Gynecol 2011; 205:235.
153. 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.
154. Castillo-Castrejon M, Meraz-Cruz N, Gomez-Lopez N, Flores-Pliego A, Beltran-Montoya J, Viveros-Alcaraz M, Vadillo-Ortega F. Choriodecidual cells from term human pregnancies show distinctive functional properties related to the induction of labor. Am J Reprod Immunol 2014; 71:86-93.