HSV-2 enhances ZIKV infection of the placenta and induces apoptosis in first-trimester trophoblast cells

American Journal of Reproductive Immunology

Volumn 76, Issue 5, 2016, Pages 348-357

  Aldo, Paulomi ^a   You, Yuan ^a   Szigeti, Klara ^a   Horvath, Tamas L ^a   Lindenbach, Brett ^a   Mor, Gil ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

co infection; fetal viral infection; HSV 1 2; pika virus; placenta; pregnancy

Indexed keywords

BETA INTERFERON; CASPASE 3; INTERFERON; INTERFERON REGULATORY FACTOR 3; MESSENGER RNA; PROTEIN; RECEPTOR; TAM RECEPTOR; TBK 1 PROTEIN; UNCLASSIFIED DRUG; VIRUS RNA;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BLOOD PLACENTA BARRIER; CELL DIFFERENTIATION; CONTROLLED STUDY; FEMALE; FIRST TRIMESTER PREGNANCY; GENE EXPRESSION; HERPES SIMPLEX; HERPES SIMPLEX VIRUS 2; HUMAN; HUMAN CELL; INFECTION RISK; META ANALYSIS; MIXED INFECTION; MOUSE; NONHUMAN; PLACENTA; PLACENTA TISSUE; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TROPHOBLAST; VERO CELL LINE; VIRUS ENTRY; VIRUS STRAIN; YELLOW FEVER; YOUNG ADULT; ZIKA FEVER;

EID: 84990188388     PISSN: 10467408     EISSN: 16000897     Source Type: Journal    
DOI: 10.1111/aji.12578     Document Type: Article

References (48)

1. Weaver SC, Costa F, Garcia-Blanco MA, et al. Zika virus: history, emergence, biology, and prospects for control. Antiviral Res. 2016;130:69–80.
2. Baptista T, Quaghebeur G, Alarcon A. Neuroimaging findings of babies with microcephaly and presumed congenital Zika virus infection. BMJ. 2016;353:i2194.
3. Brett-Major DM, Roth CE. Zika virus, emergencies, uncertainty and vulnerable populations. J R Coll Physicians Edinb. 2016;46:3–6.
4. Cavalheiro S, Lopez A, Serra S, et al. Microcephaly and Zika virus: neonatal neuroradiological aspects. Childs Nerv Syst. 2016;32:1057–1060.
5. Mlakar J, Korva M, Tul N, et al. Zika virus associated with microcephaly. N Engl J Med. 2016;374:951–958.
6. Garcez PP, Loiola EC, Madeiro da Costa R, et al. Zika virus impairs growth in human neurospheres and brain organoids. Science. 2016;352:816–818.
7. Miner JJ, Diamond MS. Understanding how zika virus enters and infects neural target cells. Cell Stem Cell. 2016;18:559–560.
8. Miner JJ, Cao B, Govero J, et al. Zika virus infection during pregnancy in mice causes placental damage and fetal demise. Cell. 2016;165:1081–1091.
9. Bayer A, Lennemann NJ, Ouyang Y, et al. Type III interferons produced by human placental trophoblasts confer protection against zika virus infection. Cell Host Microbe. 2016;9:705–712.
10. Mor G, Cardenas I. The immune system in pregnancy: a unique complexity. Am J Reprod Immunol. 2010;63:425–433.
11. Hajishengallis G, Lambris JD. Microbial manipulation of receptor crosstalk in innate immunity. Nat Rev Immunol. 2011;11:187–200.
12. Bakaletz LO. Developing animal models for polymicrobial diseases. Nat Rev Microbiol. 2004;2:552–568.
13. Smith H. The role of microbial interactions in infectious disease. Philos Trans R Soc Lond B Biol Sci. 1982;297:551–561.
14. Anzivino E, Fioriti D, Mischitelli M, et al. Herpes simplex virus infection in pregnancy and in neonate: status of art of epidemiology, diagnosis, therapy and prevention. Virol J. 2009;6:40–1743-422X.
15. Smith PD, Roberts CM. American College Health Association annual Pap test and sexually transmitted infection survey: 2006. J ACH. 2009;57:389–394.
16. Desselberger U. Herpes simplex virus infection in pregnancy: diagnosis and significance. Intervirology. 1998;41:185–190.
17. Harding-Esch EM, Edwards T, Sillah A, et al. Active trachoma and ocular Chlamydia trachomatis infection in two Gambian regions: on course for elimination by 2020? PLoS Negl Trop Dis. 2009;3:e573.
18. Henriquez SA, Brett R, Alexander J, Pratt J, Roberts CW. Neuropsychiatric disease and Toxoplasma gondii infection. NeuroImmunoModulation. 2009;16:122–133.
19. Kawana K, Yoshikawa H, Sata T. Post-partum detection of varicella-zoster virus DNA in the placenta. Int J Gynaecol Obstet. 1996;55:165–166.
20. Pereira VS, Moizeis RN, Fernandes TA, Araujo JM, Meissner RV, Fernandes JV. Herpes simplex virus type 1 is the main cause of genital herpes in women of Natal, Brazil. Eur J Obstet Gynecol Reprod Biol. 2012;161:190–193.
21. Clemens SA, Farhat CK. Seroprevalence of herpes simplex 1-2 antibodies in Brazil. Rev Saude Publica. 2010;44:726–734.
22. Racicot K, Cardenas I, Wunsche V, et al. Viral infection of the pregnant cervix predisposes to ascending bacterial infection. J Immunol. 2013;191:934–941.
23. Bredenbeek PJ, Kooi EA, Lindenbach B, Huijkman N, Rice CM, Spaan WJ. A stable full-length yellow fever virus cDNA clone and the role of conserved RNA elements in flavivirus replication. J Gen Virol. 2003;84:1261–1268.
24. Lindenbach BD, Rice CM. trans-Complementation of yellow fever virus NS1 reveals a role in early RNA replication. J Virol. 1997;71:9608–9617.
25. Foy BD, Kobylinski KC, Chilson Foy JL, et al. Probable non-vector-borne transmission of Zika virus, Colorado, USA. Emerg Infect Dis. 2011;17:880–882.
26. Lanciotti RS, Kosoy OL, Laven JJ, et al. Genetic and serologic properties of Zika virus associated with an epidemic, Yap State, Micronesia, 2007. Emerg Infect Dis. 2008;14:1232–1239.
27. Aldo PB, Racicot K, Craviero V, Guller S, Romero R, Mor G. Trophoblast induces monocyte differentiation into CD14+/CD16+ macrophages. Am J Reprod Immunol. 2014;72:270–284.
28. Holmberg JC, Haddad S, Wunsche V, et al. An in vitro model for the study of human implantation. Am J Reprod Immunol. 2012;67:169–178.
29. Straszewski-Chavez SL, Abrahams VM, Aldo PB, Mor G. Isolation and characterization of a novel telomerase-immortalized human first trimester trophoblast cell line. Placenta. 2009;30:939–948.
30. Aldo PB, Mulla MJ, Romero R, Mor G, Abrahams VM. Viral ssRNA induces first trimester trophoblast apoptosis through an inflammatory mechanism. Am J Reprod Immunol. 2010;64:27–37.
31. Welsch S, Miller S, Romero-Brey I, et al. Composition and three-dimensional architecture of the dengue virus replication and assembly sites. Cell Host Microbe. 2009;5:365–375.
32. Ishihara N, Matsuo H, Murakoshi H, Laoag-Fernandez J, Samoto T, Maruo T. Changes in proliferative potential, apoptosis and Bcl-2 protein expression in cytotrophoblasts and syncytiotrophoblast in human placenta over the course of pregnancy. Endoc J. 2000;47:317–327.
33. Racicot K, Kwon JY, Aldo P, et al. Type I interferon regulates the placental inflammatory response to bacteria and is targeted by virus: mechanism of polymicrobial infection-induced preterm birth. Am J Reprod Immunol. 2016;75:451–460.
34. Miner JJ, Cao B, Govero J, et al. Zika virus infection during pregnancy in mice causes placental damage and fetal demise. Cell. 2016;165:1081–1091.
35. Tabata T, Petitt M, Fang-Hoover J, et al. Cytomegalovirus impairs cytotrophoblast-induced lymphangiogenesis and vascular remodeling in an in vivo human placentation model. Am J Pathol. 2012;181:1540–1559.
36. Genbacev O, Donne M, Kapidzic M, et al. Establishment of human trophoblast progenitor cell lines from the chorion. Stem Cells. 2011;29:1427–1436.
37. Geyer AI, Kraus T, Roberts M, et al. Plasma level of interferon gamma induced protein 10 is a marker of sarcoidosis disease activity. Cytokine. 2013;64:152–157.
38. Li W, Moltedo B, Moran TM. Type I interferon induction during influenza virus infection increases susceptibility to secondary Streptococcus pneumoniae infection by negative regulation of gammadelta T cells. J Virol. 2012;86:12304–12312.
39. Pazos M, Sperling RS, Moran TM, Kraus TA. The influence of pregnancy on systemic immunity. Immunol Res. 2012;54:254–261.
40. Xu F, Sternberg MR, Kottiri BJ, et al. Trends in herpes simplex virus type 1 and type 2 seroprevalence in the United States. JAMA. 2006;296:964–973.
41. Hunt CL, Kolokoltsov AA, Davey RA, Maury W. The Tyro3 receptor kinase Axl enhances macropinocytosis of Zaire ebolavirus. J Virol. 2011;85:334–347.
42. Perera-Lecoin M, Meertens L, Carnec X, Amara A. Flavivirus entry receptors: an update. Viruses. 2014;6:69–88.
43. Anderson HA, Maylock CA, Williams JA, Paweletz CP, Shu H, Shacter E. Serum-derived protein S binds to phosphatidylserine and stimulates the phagocytosis of apoptotic cells. Nat Immunol. 2003;4:87–91.
44. Rothlin CV, Lemke G. TAM receptor signaling and autoimmune disease. Curr Opin Immunol. 2010;22:740–746.
45. Chan PY, Carrera Silva EA, De Kouchkovsky D, et al. The TAM family receptor tyrosine kinase TYRO3 is a negative regulator of type 2 immunity. Science. 2016;352:99–103.
46. Lemke G, Rothlin CV. Immunobiology of the TAM receptors. Nat Rev Immunol. 2008;8:327–336.
47. Rothlin CV, Carrera-Silva EA, Bosurgi L, Ghosh S. TAM receptor signaling in immune homeostasis. Annu Rev Immunol. 2015;33:355–391.
48. Rothlin CV, Leighton JA, Ghosh S. Tyro3, Axl, and Mertk receptor signaling in inflammatory bowel disease and colitis-associated cancer. Inflamm Bowel Dis. 2014;20:1472–1480.