Caspase-1 Activation is Increased with Human Labour in Foetal Membranes and Myometrium and Mediates Infection-Induced Interleukin-1β Secretion

American Journal of Reproductive Immunology

Volumn 71, Issue 2, 2014, Pages 189-201

  Lappas, Martha ^a,b  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b MERCY HOSPITAL FOR WOMEN   (Australia)

Author keywords

Caspase 1; Foetal membranes; Human labour; IL 1 ; Inflammasome; Myometrium

Indexed keywords

HYDROGEN POTASSIUM ADENOSINE TRIPHOSPHATASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INFLAMMASOME; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; LIPOPOLYSACCHARIDE; NIGERICIN; PURINERGIC P2X7 RECEPTOR; ADENOSINE TRIPHOSPHATE; GAP JUNCTION PROTEIN; NERVE PROTEIN; PANX1 PROTEIN, HUMAN;

ARTICLE; BREECH PRESENTATION; CESAREAN SECTION; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE RELEASE; ENZYME ACTIVATION; EXPLANT; FEMALE; FETUS MEMBRANE; GENE EXPRESSION; HUMAN; HUMAN TISSUE; INTRAUTERINE INFECTION; LABOR; MYOMETRIUM; PRIORITY JOURNAL; PROTEIN EXPRESSION; CELL CULTURE; DRUG EFFECTS; EMBRYO MEMBRANE; GENETICS; IMMUNOLOGY; METABOLISM; PREGNANCY;

ADENOSINE TRIPHOSPHATE; CASPASE 1; CELLS, CULTURED; CONNEXINS; ENZYME ACTIVATION; EXTRAEMBRYONIC MEMBRANES; FEMALE; HUMANS; INFLAMMASOMES; INTERLEUKIN-1BETA; LABOR, OBSTETRIC; LIPOPOLYSACCHARIDES; MYOMETRIUM; NERVE TISSUE PROTEINS; NF-KAPPA B; NIGERICIN; PREGNANCY; RECEPTORS, PURINERGIC P2X7;

EID: 84892445160     PISSN: 10467408     EISSN: 16000897     Source Type: Journal    
DOI: 10.1111/aji.12174     Document Type: Article

References (74)

1. Callaghan WM, MacDorman MF, Rasmussen SA, Qin C, Lackritz EM: The contribution of preterm birth to infant mortality rates in the United States. Pediatrics 2006; 118:1566-1573.
2. Saigal S, Doyle LW: An overview of mortality and sequelae of preterm birth from infancy to adulthood. Lancet 2008; 371:261-269.
3. Goldenberg RL, Culhane JF, Iams JD, Romero R: Epidemiology and causes of preterm birth. Lancet 2008; 371:75-84.
4. Goldenberg RL, Hauth JC, Andrews WW: Mechanisms of disease-intrauterine infection and preterm delivery. N Engl J Med 2000; 342:1500-1507.
5. Muglia LJ, Katz M: The enigma of spontaneous preterm birth. N Engl J Med 2010; 362:529-535.
6. Gibbs RS, Romero R, Hillier SL, Eschenbach DA, Sweet RL: A review of premature birth and subclinical infection. Am J Obstet Gynecol 1992; 166:1515-1528.
7. Romero R, Sirtori M, Oyarzun E, Avila C, Mazor M, Callahan R, Sabo V, Athanassiadis AP, Hobbins JC: 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.
8. Menon R, Fortunato SJ: Infection and the role of inflammation in preterm premature rupture of the membranes. Best Pract Res Clin Obstet Gynaecol 2007; 21:467-478.
9. Goldenberg RL, Hauth JC, Andrews WW: Intrauterine infection and preterm delivery. N Engl J Med 2000; 342:1500-1507.
10. Bokstrom H, Brannstrom M, Alexandersson M, Norstrom A: Leukocyte subpopulations in the human uterine cervical stroma at early and term pregnancy. Hum Reprod 1997; 12:586-590.
11. Osman I, Young A, Ledingham MA, Thomson AJ, Jordan F, Greer IA, Norman JE: Leukocyte density and pro-inflammatory cytokine expression in human fetal membranes, decidua, cervix and myometrium before and during labour at term. Mol Hum Reprod 2003; 9:41-45.
12. Thomson AJ, Telfer JF, Young A, Campbell S, Stewart CJR, Cameron IT, Greer IA, Norman JE: Leukocytes infiltrate the myometrium during human parturition: further evidence that labour is an inflammatory process. Hum Reprod 1999; 14:229-236.
13. Bollopragada S, Youssef R, Jordan F, Greer I, Norman J, Nelson S: Term labor is associated with a core inflammatory response in human fetal membranes, myometrium, and cervix. Am J Obstet Gynecol 2009; 200:104.e1-11.
14. Elliott CL, Loudon JAZ, Brown N, Slater DM, Bennett PR, Sullivan MHF: IL-1β and IL-8 in human fetal membranes: changes with gestational age, labor, and culture conditions. Am J Reprod Immunol 2001; 46:260-267.
15. Bowen JM, Chamley L, Keelan JA, Mitchell MD: Cytokines of the placenta and extra-placental membranes: roles and regulation during human pregnancy and parturition. Placenta 2002; 23:257-273.
16. Romero R, Mazor M, Tartakovsky B: Systemic administration of interleukin-1 induces preterm parturition in mice. Am J Obstet Gynecol 1991; 165:969-971.
17. 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.
18. 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.
19. Schroder K, Tschopp J: The inflammasomes. Cell 2010; 140:821-832.
20. Yu HB, Finlay BB: The caspase-1 inflammasome: a pilot of innate immune responses. Cell Host Microbe 2008; 4:198-208.
21. Stutz A, Golenbock DT, Latz E: Inflammasomes: too big to miss. J Clin Invest 2009; 119:3502-3511.
22. Kuida K, Lippke JA, Ku G, Harding MW, Livingston DJ, Su MS, Flavell RA: Altered cytokine export and apoptosis in mice deficient in interleukin-1 beta converting enzyme. Science 1995;267:2000-2003.
23. Li P, Allen H, Banerjee S, Franklin S, Herzog L, Johnston C, McDowell J, Paskind M, Rodman L, Salfeld J, Towne E, Tracey D, Wardwell S, Wei F-Y, Wong W, Kamen R, Seshadri T: Mice deficient in IL-1 beta-converting enzyme are defective in production of mature IL-1 beta and resistant to endotoxic shock. Cell 1995; 80:401-411.
24. Ghayur T, Banerjee S, Hugunin M, Butler D, Herzog L, Carter A, Quintal L, Sekut L, Talanian R, Paskind M, Wong W, Kamen R, Tracey D, Allen H: Caspase-1 processes IFN-gamma-inducing factor and regulates LPS-induced IFN-gamma production. Nature 1997; 386:619-623.
25. Mulla MJ, Myrtolli K, Potter J, Boeras C, Kavathas PB, Sfakianaki AK, Tadesse S, Norwitz ER, Guller S, Abrahams VM: Uric acid induces trophoblast IL-1beta production via the inflammasome: implications for the pathogenesis of preeclampsia. Am J Reprod Immunol 2011; 65:542-548.
26. Kavathas PB, Boeras CM, Mulla MJ, Abrahams VM: Nod1, but not the ASC inflammasome, contributes to induction of IL-1beta secretion in human trophoblasts after sensing of Chlamydia trachomatis. Mucosal Immunol 2013; 6:235-243.
27. Abrahams VM: The role of the Nod-like receptor family in trophoblast innate immune responses. J Reprod Immunol 2011; 88:112-117.
28. Lappas M, Riley C, Rice GE, Permezel M: Increased expression of ac-FoxO1 protein in prelabor fetal membranes overlying the cervix: possible role in human fetal membrane rupture. Reprod Sci 2009; 16:635-641.
29. Lappas M, Mitton A, Lim R, Barker G, Riley C, Permezel M: SIRT1 is a novel regulator of key pathways of human labor. Biol Reprod 2011; 84:167-178.
30. Lim R, Barker G, Lappas M: SIRT6 is decreased with preterm labour and regulates key terminal effector pathways of human labour in fetal membranes. Biol Reprod 2012; 17:1-10.
31. Lappas M, Odumetse TL, Riley C, Reti NG, Holdsworth-Carson SJ, Rice GE, Permezel M: Pre-labour fetal membranes overlying the cervix display alterations in inflammation and NF-kappaB signalling pathways. Placenta 2008; 29:995-1002.
32. Lappas M, Permezel M, Georgiou HM, Rice GE: Nuclear factor kappa B regulation of proinflammatory cytokines in human gestational tissues in vitro. Biol Reprod 2002; 67:668-673.
33. Lappas M, Permezel M, Rice GE: N-Acetyl-cysteine inhibits phospholipid metabolism, proinflammatory cytokine release, protease activity, and nuclear factor-kappaB deoxyribonucleic acid-binding activity in human fetal membranes in vitro. J Clin Endocrinol Metab 2003; 88:1723-1729.
34. Perregaux D, Gabel CA: Interleukin-1 beta maturation and release in response to ATP and nigericin. Evidence that potassium depletion mediated by these agents is a necessary and common feature of their activity. J Biol Chem 1994; 269:15195-15203.
35. Cheneval D, Ramage P, Kastelic T, Szelestenyi T, Niggli H, Hemmig R, Bachmann M, MacKenzie A: Increased mature interleukin-1β (IL-1β) secretion from THP-1 cells induced by nigericin is a result of activation of p45 IL-1β-converting enzyme processing. J Biol Chem 1998; 273:17846-17851.
36. Hentze H, Lin XY, Choi MS, Porter AG: Critical role for cathepsin B in mediating caspase-1-dependent interleukin-18 maturation and caspase-1-independent necrosis triggered by the microbial toxin nigericin. Cell Death Differ 2003; 10:956-968.
37. Strowig T, Henao-Mejia J, Elinav E, Flavell R: Inflammasomes in health and disease. Nature 2012; 481:278-286.
38. Lamkanfi M, Dixit VM: Inflammasomes and their roles in health and disease. Annu Rev Cell Dev Biol 2012; 28:137-161.
39. 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.
40. 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-kappa B-driven protein synthesis. J Immunol 2005; 175:7611-7622.
41. Franchi L, Kanneganti TD, Dubyak GR, Nunez G: Differential requirement of P2X7 receptor and intracellular K+ for caspase-1 activation induced by intracellular and extracellular bacteria. J Biol Chem 2007; 282:18810-18818.
42. Mehta VB, Hart J, Wewers MD: ATP-stimulated release of interleukin (IL)-1 beta and IL-18 requires priming by lipopolysaccharide and is independent of caspase-1 cleavage. J Biol Chem 2001; 276:3820-3826.
43. Pelegrin P, Barroso-Gutierrez C, Surprenant A: P2X(7) receptor differentially couples to distinct release pathways for IL-1 beta in mouse macrophage. J Immunol 2008; 180:7147-7157.
44. Pelegrin P, Surprenant A: Pannexin-1 couples to maitotoxin- and nigericin-induced interleukin-1 beta release through a dye uptake-independent pathway. J Biol Chem 2007; 282:2386-2394.
45. Pelegrin P, Surprenant A: Pannexin-1 mediates large pore formation and interleukin-1 beta release by the ATP-gated P2X(7) receptor. EMBO J 2006; 25:5071-5082.
46. 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.
47. 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.
48. Netea MG, Nold-Petry CA, Nold MF, Joosten LA, Opitz B, van dMJ, van de Veerdonk FL, Ferwerda G, Heinhuis B, Devesa I, Funk CJ, Mason RJ, Kullberg BJ, Rubartelli A, van dMJ, Dinarello CA: Differential requirement for the activation of the inflammasome for processing and release of IL-1beta in monocytes and macrophages. Blood 2009; 113:2324-2335.
49. 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.
50. Cruz CM, Rinna A, Forman HJ, Ventura AL, Persechini PM, Ojcius DM: ATP activates a reactive oxygen species-dependent oxidative stress response and secretion of proinflammatory cytokines in macrophages. J Biol Chem 2007; 282:2871-2879.
51. 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.
52. Duan S, Neary JT: P2X(7) receptors: properties and relevance to CNS function. Glia 2006; 54:738-746.
53. Solle M, Labasi J, Perregaux DG, Stam E, Petrushova N, Koller BH, Griffiths RJ, Gabel CA: Altered cytokine production in mice lacking P2X(7) receptors. J Biol Chem 2001; 276:125-132.
54. Urabe S, Miyoshi H, Fujiwara H, Yamaoka K, Kudo Y: Enhanced expression of P2X4 and P2X7 purinergic receptors in the myometrium of pregnant rats in preterm delivery models. Reprod sci 2009; 16:1186-1192.
55. Miyoshi H, Yamaoka K, Urabe S, Kudo Y: ATP-induced currents carried through P2X7 receptor in rat myometrial cells. Reprod sci 2012; 19:1285-1291.
56. Miyoshi H, Yamaoka K, Urabe S, Kodama M, Kudo Y: Functional expression of purinergic P2X7 receptors in pregnant rat myometrium. Am J Physiol Regul Integr Comp Physiol 2010; 298:R1117-R1124.
57. Davis BK, Wen H, Ting JP: The inflammasome NLRs in immunity, inflammation, and associated diseases. Annu Rev Immunol 2011; 29:707-735.
58. 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.
59. 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.
60. Romero R, Espinoza J, Kusanovic JP, Gotsch F, Hassan S, Erez O, Chaiworapongsa T, Mazor M: The preterm parturition syndrome. BJOG 2006; 113(Suppl 3):17-42.
61. Mitchell K, Brou L, Bhat G, Drobek CO, Kramer M, Hill A, Fortunato SJ, Menon R: Group B Streptococcus colonization and higher maternal IL-1 beta concentrations are associated with early term births. J Matern Fetal Neonatal Med 2013; 26:56-61.
62. Costa A, Gupta R, Signorino G, Malara A, Cardile F, Biondo C, Midiri A, Galbo R, Trieu-Cuot P, Papasergi S, Teti G, Henneke P, Mancuso G, Golenbock DT, Beninati C: Activation of the NLRP3 inflammasome by group B streptococci. J Immunol 2012;188:1953-1960.
63. Menon R, Peltier MR, Eckardt J, Fortunato SJ: Diversity in cytokine response to bacteria associated with preterm birth by fetal membranes. Am J Obstet Gynecol 2009; 201:306.e301-306.e306.
64. Dinarello CA: Interleukin-18 and the pathogenesis of inflammatory diseases. Semin Nephrol 2007; 27:98-114.
65. 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.
66. Jacobsson B, Holst RM, Mattsby-Baltzer I, Nikolaitchouk N, Wennerholm UB, Hagberg H: Interleukin-18 in cervical mucus and amniotic fluid: relationship to microbial invasion of the amniotic fluid, intra-amniotic inflammation and preterm delivery. BJOG 2003; 110:598-603.
67. Menon R, Lombardi SJ, Fortunato SJ: IL-18, a product of choriodecidual cells, increases during premature rupture of membranes but fails to turn on the Fas-FasL-mediated apoptosis pathway. J Assist Reprod Genet 2001; 18:276-284.
68. Topping V, Romero R, Than NG, Tarca AL, Xu ZH, Kim SY, Wang B, Yeo L, Kim CJ, Hassan SS, Kim JS: Interleukin-33 in the human placenta. J Matern Fetal Neonatal Med 2013; 26:327-338.
69. Chatterjee PK, Todorovic Z, Sivarajah A, Mota-Filipe H, Brown PA, Stewart KN, Cuzzocrea S, Thiemermann C: Differential effects of caspase inhibitors on the renal dysfunction and injury caused by ischemia-reperfusion of the rat kidney. Eur J Pharmacol 2004; 503:173-183.
70. Paszkowski AS, Rau B, Mayer JM, Moller P, Beger HG: Therapeutic application of caspase 1/interleukin-1beta-converting enzyme inhibitor decreases the death rate in severe acute experimental pancreatitis. Ann Surg 2002; 235:68-76.
71. Rowe SJ, Allen L, Ridger VC, Hellewell PG, Whyte MKB: Caspase-1-deficient mice have delayed neutrophil apoptosis and a prolonged inflammatory response to lipopolysaccharide-induced acute lung injury. J Immunol 2002; 169:6401-6407.
72. Frantz S, Ducharme A, Sawyer D, Rohde LE, Kobzik L, Fukazawa R, Tracey D, Allen H, Lee RT, Kelly RA: Targeted deletion of caspase-1 reduces early mortality and left ventricular dilatation following myocardial infarction. J Mol Cell Cardiol 2003; 35:685-694.
73. Taylor SRJ, Turner CM, Elliott JI, McDaid J, Hewitt R, Smith J, Pickering MC, Whitehouse DL, Cook HT, Burnstock G, Pusey CD, Unwin RJ, Tam FWK: P2X7 deficiency attenuates renal injury in experimental glomerulonephritis. J Am Soc Nephrol 2009; 20:1275-1281.
74. Lucattelli M, Cicko S, Müller T, Lommatzsch M, Cunto GD, Cardini S, Sundas W, Grimm M, Zeiser R, Dürk T, Zissel G, Sorichter S, Ferrari D, Virgilio FD, Virchow JC, Lungarella G, Idzko M: P2X7 receptor signaling in the pathogenesis of smoke-induced lung inflammation and emphysema. Am J Respir Cell Mol Biol 2011; 44:423-429.