Placental Viral Infection Sensitizes to Endotoxin-Induced Pre-Term Labor: A Double Hit Hypothesis

American Journal of Reproductive Immunology

Volumn 65, Issue 2, 2011, Pages 110-117

  Cardenas, Ingrid ^a   Mor, Gil ^a   Aldo, Paulomi ^a   Lang, Sabine M ^a   Stabach, Paul ^a   Sharp, Andrew ^a   Romero, Roberto ^b   Mazaki Tovi, Shali ^b   Gervasi, MariaTeresa ^c   Means, Robert E ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b WAYNE STATE UNIVERSITY   (United States)

^c UNIVERSITY HOSPITAL OF PADOVA   (Italy)

Author keywords

Double hit hypothesis; Lipopolysaccharide; Placenta; Toll like receptors; Trophoblast; Viral infection

Indexed keywords

CHEMOKINE; CYTOKINE; ENDOTOXIN; LIPOPOLYSACCHARIDE;

ADOLESCENT; ANIMAL EXPERIMENT; ARTICLE; BACTERIAL INFECTION; C57BL 6 MOUSE; CONTROLLED STUDY; DECIDUA; GAMMAHERPESVIRINAE; HYPOTHESIS; IMMUNE RESPONSE; MOUSE; NIDATION; NONHUMAN; PLACENTA; PLACENTA DISORDER; PREGNANCY OUTCOME; PREGNANT WOMAN; PREMATURE LABOR; PRIORITY JOURNAL; PROGNOSIS; SENSITIZATION; TROPHOBLAST; VIRUS INFECTION;

ANIMALS; BACTERIAL INFECTIONS; ENDOTOXINS; FEMALE; FETAL DEATH; HERPESVIRIDAE INFECTIONS; HUMANS; LABOR, INDUCED; LIPOPOLYSACCHARIDES; MICE; MICE, INBRED C57BL; NIH 3T3 CELLS; OBSTETRIC LABOR, PREMATURE; PLACENTA; PLACENTA DISEASES; PREGNANCY; RHADINOVIRUS; TUMOR VIRUS INFECTIONS;

EID: 78650989958     PISSN: 10467408     EISSN: 16000897     Source Type: Journal    
DOI: 10.1111/j.1600-0897.2010.00908.x     Document Type: Article

References (30)

1. Digiulio DB, Romero R, Kusanovic JP, Gomez R, Kim CJ, Seok KS, Gotsch F, Mazaki-Tovi S, Vaisbuch E, Sanders K, Bik EM, Chaiworapongsa T, Oyarzun E, Relman DA: 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.
2. Romero R, Espinoza J, Goncalves LF, Kusanovic JP, Friel LA, Nien JK: Inflammation in preterm and term labour and delivery. Semin Fetal Neonatal Med 2006; 11:317-326.
3. Jacobsson B, Hagberg G: Antenatal risk factors for cerebral palsy. Best Pract Res Clin Obstet Gynaecol 2004; 18:425-436.
4. Haun L, Kwan N, Hollier LM: Viral infections in pregnancy. Minerva Ginecol 2007; 59:159-174.
5. Romero R, Espinoza J, Chaiworapongsa T, Kalache K: Infection and prematurity and the role of preventive strategies. Semin Neonatol 2002; 7:259-274.
6. Al-Adnani M, Sebire NJ: The role of perinatal pathological examination in subclinical infection in obstetrics. Best Pract Res Clin Obstet Gynaecol 2007; 21:505-521.
7. Digiulio DB, Gervasi M, Romero R, Vaisbuch E, Mazaki-Tovi S, Kusanovic JP, Seok KS, Gomez R, Mittal P, Gotsch F, Chaiworapongsa T, Oyarzun E, Kim CJ, Relman DA: Microbial invasion of the amniotic cavity in pregnancies with small-for-gestational-age fetuses. J Perinat Med 2010; DOI: [Epub ahead of print].
8. Xu F, Sternberg MR, Kottiri BJ, McQuillan GM, Lee FK, Nahmias AJ, Berman SM, Markowitz LE: Trends in herpes simplex virus type 1 and type 2 seroprevalence in the United States. JAMA 2006; 296:964-973.
9. Avgil M, Ornoy A: Herpes simplex virus and Epstein-Barr virus infections in pregnancy: consequences of neonatal or intrauterine infection. Reprod Toxicol 2006; 21:436-445.
10. Romero R, Kadar N, Vaisbuch E, Hassan SS: Maternal death following cardiopulmonary collapse after delivery: amniotic fluid embolism or septic shock due to intrauterine infection? Am J Reprod Immunol 2010; 64:113-125.
11. Goldenberg RL, Culhane JF, Iams JD, Romero R: Epidemiology and causes of preterm birth. Lancet 2008; 371:75-84.
12. Mor G: Inflammation and pregnancy: the role of toll-like receptors in trophoblast-immune interaction. Ann N Y Acad Sci 2008; 1127:121-128.
13. Madan I, Romero R, Kusanovic JP, Mittal P, Chaiworapongsa T, Dong Z, Mazaki-Tovi S, Vaisbuch E, Alpay Savasan Z, Yeo L, Kim CJ, Hassan SS: The frequency and clinical significance of intra-amniotic infection and/or inflammation in women with placenta previa and vaginal bleeding: an unexpected observation. J Perinat Med 2010; 38:275-279.
14. Soto E, Romero R, Vaisbuch E, Erez O, Mazaki-Tovi S, Kusanovic JP, Dong Z, Chaiworapongsa T, Yeo L, Mittal P, Hassan SS: Fragment Bb: evidence for activation of the alternative pathway of the complement system in pregnant women with acute pyelonephritis. J Matern Fetal Neonatal Med 2010; DOI: [Epub ahead of print].
15. Robertson SA, Skinner RJ, Care AS: Essential role for IL-10 in resistance to lipopolysaccharide-induced preterm labor in mice. J Immunol 2006; 177:4888-4896.
16. Nansen A, Randrup Thomsen A: Viral infection causes rapid sensitization to lipopolysaccharide: central role of IFN-alpha beta. J Immunol 2001; 166:982-988.
17. Oluyomi-Obi T, Avery L, Schneider C, Kumar A, Lapinsky S, Menticoglou S, Zarychanski R: Perinatal and maternal outcomes in critically ill obstetrics patients with pandemic H1N1 Influenza A. J Obstet Gynaecol Can 2000; 32:443-447. 448-452.
18. Olivadoti M, Toth LA, Weinberg J, Opp MR: Murine gammaherpesvirus 68: a model for the study of Epstein-Barr virus infections and related diseases. Comp Med 2007; 57:44-50.
19. 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. 651-657.
20. Murphy SP, Hanna NN, Fast LD, Shaw SK, Berg G, Padbury JF, Romero R, Sharma S: Evidence for participation of uterine natural killer cells in the mechanisms responsible for spontaneous preterm labor and delivery. Am J Obstet Gynecol 2009; 200:308. 301-309.
21. Cardenas I, Means RE, Aldo P, Koga K, Lang SM, Booth C, Manzur A, Oyarzun E, Romero R, Mor G: Viral infection of the placenta leads to fetal inflammation and sensitization to bacterial products predisposing to preterm labor. J Immunol 2010; 185:1248-1257.
22. Straszewski-Chavez SL, Abrahams VM, Aldo PB, Mor G: Isolation and characterization of a novel telomerase-immortalized human first trimester trophoblast cell line. Placenta 2005; 26:A.62.
23. Koga K, Cardenas I, Aldo P, Abrahams VM, Peng B, Fill S, Romero R, Mor G: Activation of TLR3 in the trophoblast is associated with preterm delivery. Am J Reprod Immunol 2009; 61:196-212.
24. Romero R, Mazaki-Tovi S, Vaisbuch E, Kusanovic JP, Chaiworapongsa T, Gomez R, Nien JK, Yoon BH, Mazor M, Luo J, Banks D, Ryals J, Beecher C: Metabolomics in premature labor: a novel approach to identify patients at risk for preterm delivery. J Matern Fetal Neonatal Med 2010; DOI: [Epub ahead of print].
25. Kim CJ, Romero R, Kusanovic JP, Yoo W, Dong Z, Topping V, Gotsch F, Yoon BH, Chi JG, Kim JS: The frequency, clinical significance, and pathological features of chronic chorioamnionitis: a lesion associated with spontaneous preterm birth. Mod Pathol 2010; 23:1000-1011.
26. 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.
27. Mor G, Cardenas I: The immune system in pregnancy: a unique complexity. Am J Reprod Immunol 2010; 63:425-433.
28. 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.
29. Fest S, Aldo PB, Abrahams VM, Visintin I, Alvero A, Chen R, Chavez SL, Romero R, Mor G: Trophoblast-macrophage interactions: a regulatory network for the protection of pregnancy. Am J Reprod Immunol 2007; 57:55-66.
30. Ogge G, Romero R, Chaiworapongsa T, Gervasi MT, Pacora P, Erez O, Kusanovic JP, Vaisbuch E, Mazaki-Tovi S, Gotsch F, Mittal P, Kim YM, Hassan SS: Leukocytes of pregnant women with small-for-gestational age neonates have a different phenotypic and metabolic activity from those of women with preeclampsia. J Matern Fetal Neonatal Med 2010; 23:476-487.