Uric Acid Induces Trophoblast IL-1β Production Via the Inflammasome: Implications for the Pathogenesis of Preeclampsia

American Journal of Reproductive Immunology

Volumn 65, Issue 6, 2011, Pages 542-548

  Mulla, Melissa J ^a   Myrtolli, Kledia ^a   Potter, Julie ^a   Boeras, Crina ^a   Kavathas, Paula B ^a   Sfakianaki, Anna K ^a   Tadesse, Serkelem ^a,b   Norwitz, Errol R ^a,b   Guller, Seth ^a   Abrahams, Vikki M ^a  

^a YALE UNIVERSITY   (United States)

^b TUFTS MEDICAL CENTER   (United States)

Author keywords

Inflammasome; Nod like receptor; Placenta; Preeclampsia; Trophoblast; Uric acid

Indexed keywords

APOPTOSIS ASSOCIATED SPECK LIKE PROTEIN CONTAINING A CARD; INFLAMMASOME; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; NALP1 INFLAMMASOME; NALP3 INFLAMMASOME; UNCLASSIFIED DRUG; URATE; URIC ACID;

ARTICLE; CELL ISOLATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DISEASE ASSOCIATION; FEMALE; FIRST TRIMESTER PREGNANCY; HUMAN; HUMAN CELL; HUMAN TISSUE; NUCLEOTIDE SEQUENCE; PATHOGENESIS; PLACENTA; PREECLAMPSIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; THIRD TRIMESTER PREGNANCY; TROPHOBLAST; UPREGULATION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; APOPTOSIS REGULATORY PROTEINS; CARRIER PROTEINS; CASPASE 1; CELL LINE; CYTOSKELETAL PROTEINS; DISEASE PROGRESSION; ENZYME ACTIVATION; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; HYPERURICEMIA; INFLAMMASOMES; INTERLEUKIN-1BETA; MATERNAL-FETAL RELATIONS; PRE-ECLAMPSIA; PREGNANCY; TROPHOBLASTS; URIC ACID;

EID: 79955126578     PISSN: 10467408     EISSN: 16000897     Source Type: Journal    
DOI: 10.1111/j.1600-0897.2010.00960.x     Document Type: Article

References (39)

1. Brown MA: The physiology of pre-eclampsia. Clin Exp Pharmacol Physiol 1995; 22:781-791.
2. Funai EF, Friedlander Y, Paltiel O, Tiram E, Xue X, Deutsch L, Harlap S: Long-term mortality after preeclampsia. Epidemiology 2005; 16:206-215.
3. Pijnenborg R, Bland JM, Robertson WB, Brosens I: Uteroplacental arterial changes related to interstitial trophoblast migration in early human pregnancy. Placenta 1983; 4:397-413.
4. Roberts JM, Taylor RN, Musci TJ, Rodgers GM, Hubel CA, McLaughlin MK: Preeclampsia: an endothelial cell disorder. Am J Obstet Gynecol 1989; 161:1200-1204.
5. Redman CW, Sargent IL: Immunology of pre-eclampsia. Am J Reprod Immunol 2010; 63:534-543.
6. Young BC, Levine RJ, Karumanchi SA: Pathogenesis of preeclampsia. Annu Rev Pathol 2010; 5:173-192.
7. Myatt L: Role of placenta in preeclampsia. Endocrine 2002; 19:103-111.
8. Kim YM, Romero R, Oh SY, Kim CJ, Kilburn BA, Armant DR, Nien JK, Gomez R, Mazor M, Saito S, Abrahams VM, Mor G: Toll-like receptor 4: a potential link between "danger signals, "the innate immune system, and preeclampsia? Am J Obstet Gynecol 2005; 193:921-927.
9. Saito S, Shiozaki A, Nakashima A, Sakai M, Sasaki Y: The role of the immune system in preeclampsia. Mol Aspects Med 2007; 28:192-209.
10. Founds SA, Conley YP, Lyons-Weiler JF, Jeyabalan A, Hogge WA, Conrad KP: Altered global gene expression in first trimester placentas of women destined to develop preeclampsia. Placenta 2009; 30:15-24.
11. Huang SJ, Chen CP, Schatz F, Rahman M, Abrahams VM, Lockwood CJ: Pre-eclampsia is associated with dendritic cell recruitment into the uterine decidua. J Pathol 2008; 214:328-336.
12. Rieger L, Segerer S, Bernar T, Kapp M, Majic M, Morr AK, Dietl J, Kammerer U: Specific subsets of immune cells in human decidua differ between normal pregnancy and preeclampsia - a prospective observational study. Reprod Biol Endocrinol 2009; 7:132.
13. Williams PJ, Bulmer JN, Searle RF, Innes BA, Robson SC: Altered decidual leucocyte populations in the placental bed in pre-eclampsia and foetal growth restriction: a comparison with late normal pregnancy. Reproduction 2009; 138:177-184.
14. Bainbridge SA, Roberts JM: Uric acid as a pathogenic factor in preeclampsia. Placenta 2008; 29(Suppl A):S67-S72.
15. Bainbridge SA, Roberts JM, von Versen-Hoynck F, Koch J, Edmunds L, Hubel CA: Uric acid attenuates trophoblast invasion and integration into endothelial cell monolayers. Am J Physiol Cell Physiol 2009; 297:C440-C450.
16. Jin C, Flavell RA: Molecular mechanism of NLRP3 inflammasome activation. J Clin Immunol 2010; 30:628-631.
17. 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.
18. Martinon F, Tschopp J: Inflammatory caspases: linking an intracellular innate immune system to autoinflammatory diseases. Cell 2004; 117:561-574.
19. Becker CE, O'Neill LA: Inflammasomes in inflammatory disorders: the role of TLRs and their interactions with NLRs. Semin Immunopathol 2007; 29:239-248.
20. 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.
21. Costello MJ, Joyce SK, Abrahams VM: NOD protein expression and function in first trimester trophoblast cells. Am J Reprod Immunol 2007; 57:67-80.
22. 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.
23. Straszewski-Chavez SL, Abrahams VM, Alvero AB, Aldo PB, Ma Y, Guller S, Romero R, Mor G: Isolation and characterization of a novel telomerase immortalized first trimester trophoblast cell line, Swan 71. Placenta 2009; 30:939-948.
24. Graham CH, Hawley TS, Hawley RG, MacDougall JR, Kerbel RS, Khoo N, Lala PK: Establishment and characterization of first trimester human trophoblast cells with extended lifespan. Exp Cell Res 1993; 206:204-211.
25. Kliman HJ, Nestler JE, Sermasi E, Sanger JM, Strauss JF III: Purification, characterization, and in vitro differentiation of cytotrophoblasts from human term placentae. Endocrinology 1986; 118:1567-1582.
26. Guller S, LaCroix NC, Kirkun G, Wozniak R, Markiewicz L, Wang EY, Kaplan P, Lockwood CJ: Steroid regulation of oncofetal fibronectin expression in human cytotrophoblasts. J Steroid Biochem Mol Biol 1993; 46:1-10.
27. Feldmann J, Prieur AM, Quartier P, Berquin P, Certain S, Cortis E, Teillac-Hamel D, Fischer A, de Saint Basile G: Chronic infantile neurological cutaneous and articular syndrome is caused by mutations in CIAS1, a gene highly expressed in polymorphonuclear cells and chondrocytes. Am J Hum Genet 2002; 71:198-203.
28. Sanz C, Calasanz MJ, Andreu E, Richard C, Prosper F, Fernandez-Luna JL: NALP1 is a transcriptional target for cAMP-response-element-binding protein (CREB) in myeloid leukaemia cells. Biochem J 2004; 384:281-286.
29. Abrahams VM: Pattern recognition at the maternal-fetal interface. Immunol Invest 2008; 37:427-447.
30. Martinon F, Petrilli V, Mayor A, Tardivel A, Tschopp J: Gout-associated uric acid crystals activate the NALP3 inflammasome. Nature 2006; 440:237-241.
31. Gowri V, Al-Zakwani I: Prevalence of cesarean delivery in preeclamptic patients with elevated uric acid. Hypertens Pregnancy 2010; 29:231-235.
32. Koopmans CM, van Pampus MG, Groen H, Aarnoudse JG, van den Berg PP, Mol BW: Accuracy of serum uric acid as a predictive test for maternal complications in pre-eclampsia: bivariate meta-analysis and decision analysis. Eur J Obstet Gynecol Reprod Biol 2009; 146:8-14.
33. Redman CW, Bonnar J: Plasma urate changes in pre-eclampsia. Br Med J 1978; 1:1484-1485.
34. Roberts JM, Bodnar LM, Lain KY, Hubel CA, Markovic N, Ness RB, Powers RW: Uric acid is as important as proteinuria in identifying fetal risk in women with gestational hypertension. Hypertension 2005; 46:1263-1269.
35. Wolak T, Sergienko R, Wiznitzer A, Paran E, Sheiner E: High uric acid level during the first 20 weeks of pregnancy is associated with higher risk for gestational diabetes mellitus and mild preeclampsia. Hypertens Pregnancy 2010. [Epub ahead of print].
36. Canakci V, Canakci CF, Yildirim A, Ingec M, Eltas A, Erturk A: Periodontal disease increases the risk of severe pre-eclampsia among pregnant women. J Clin Periodontol 2007; 34:639-645.
37. Rinehart BK, Terrone DA, Lagoo-Deenadayalan S, Barber WH, Hale EA, Martin JN Jr, Bennett WA: Expression of the placental cytokines tumor necrosis factor alpha, interleukin 1beta, and interleukin 10 is increased in preeclampsia. Am J Obstet Gynecol 1999; 181:915-920.
38. Munno I, Chiechi LM, Lacedra G, Putignano G, Patimo C, Lobascio A, Loizzi P: Spontaneous and induced release of prostaglandins, interleukin (IL)-1beta, IL-6, and tumor necrosis factor-alpha by placental tissue from normal and preeclamptic pregnancies. Am J Reprod Immunol 1999; 42:369-374.
39. Xie F, Hu Y, Turvey SE, Magee LA, Brunham RM, Choi KC, Krajden M, Leung PC, Money DM, Patrick DM, Thomas E, von Dadelszen P: Toll-like receptors 2 and 4 and the cryopyrin inflammasome in normal pregnancy and pre-eclampsia. BJOG 2010; 117:99-108.