Maternal CD4+ T cells protect against severe congenital cytomegalovirus disease in a novel nonhuman primate model of placental cytomegalovirus transmission

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 44, 2015, Pages 13645-13650

  Bialas, Kristy M ^a   Tanaka, Takayuki ^b   Tran, Dollnovan ^b,c   Varner, Valerie ^b   De La Rosa, Eduardo Cisneros ^a   Chiuppesi, Flavia ^d   Wussow, Felix ^d   Kattenhorn, Lisa ^b   Macri, Sheila ^b   Kunz, Erika L ^a   Estroff, Judy A ^e   Kirchherr, Jennifer ^a   Yue, Yujuan ^f   Fan, Qihua ^a   Lauck, Michael ^g   O'Connor, David H ^g,h   Hall, Allison H S ^a   Xavier, Alvarez ^c   Diamond, Don J ^d   Barry, Peter A ^f   Kaur, Amitinder ^b,c   Permar, Sallie R ^a   more..

^a DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c TULANE NATIONAL PRIMATE RESEARCH CENTER   (United States)

^d CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

^e BOSTON CHILDREN S HOSPITAL   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

^g UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^h UNIVERSITY OF WISCONSIN   (United States)

Author keywords

Congenital cytomegalovirus; Neutralizing antibody; Rhesus CMV; Rhesus model; T cell immunity

Indexed keywords

GAMMA INTERFERON; IMMEDIATE EARLY PROTEIN; INTERLEUKIN 2; TUMOR NECROSIS FACTOR ALPHA; V SET DOMAIN CONTAINING T CELL ACTIVATION INHIBITOR 1; VIRUS ANTIBODY;

AMNION FLUID; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY PRODUCTION; ARTICLE; ASYMPTOMATIC INFECTION; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONGENITAL INFECTION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTION; FEMALE; FETUS; FETUS WASTAGE; GENETIC VARIABILITY; HUMORAL IMMUNITY; INFANT; INTRAUTERINE INFECTION; MATERNAL PLASMA; NONHUMAN; PLACENTAL TRANSFER; PRIORITY JOURNAL; RHESUS MONKEY; SECOND TRIMESTER PREGNANCY; T CELL DEPLETION; VIRUS LOAD; VIRUS REPLICATION; VIRUS TRANSMISSION; ANIMAL; CYTOMEGALOVIRUS INFECTIONS; DISEASE MODEL; FETOMATERNAL TRANSFUSION; IMMUNOLOGY; PREGNANCY; TRANSMISSION; VERTICAL TRANSMISSION;

ANIMALS; ANTIBODIES, VIRAL; CD4-POSITIVE T-LYMPHOCYTES; CYTOMEGALOVIRUS INFECTIONS; DISEASE MODELS, ANIMAL; FEMALE; INFECTIOUS DISEASE TRANSMISSION, VERTICAL; MACACA MULATTA; MATERNAL-FETAL EXCHANGE; PREGNANCY;

EID: 84946601394     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1511526112     Document Type: Article

References (50)

1. Dollard SC, Grosse SD, Ross DS (2007) New estimates of the prevalence of neurological and sensory sequelae and mortality associated with congenital cytomegalovirus infection. Rev Med Virol 17(5):355-363.
2. Kenneson A, Cannon MJ (2007) Review and meta-analysis of the epidemiology of congenital cytomegalovirus (CMV) infection. Rev Med Virol 17(4):253-276.
3. Cheeran MCJ, Lokensgard JR, Schleiss MR (2009) Neuropathogenesis of congenital cytomegalovirus infection: Disease mechanisms and prospects for intervention. Clin Microbiol Rev 22(1):99-126.
4. Choi YC, Hsiung GD (1978) Cytomegalovirus infection in guinea pigs. II. Transplacental and horizontal transmission. J Infect Dis 138(2):197-202.
5. Kanai K, et al. (2011) Re-evaluation of the genome sequence of guinea pig cytomegalovirus. J Gen Virol 92(Pt 5):1005-1020.
6. Griffith BP, Lucia HL, Hsiung GD (1982) Brain and visceral involvement during congenital cytomegalovirus infection of guinea pigs. Pediatr Res 16(6):455-459.
7. Bia FJ, et al. (1984) Vaccination against transplacental cytomegalovirus transmission: Vaccine reactivation and efficacy in guinea pigs. J Infect Dis 149(3):355-362.
8. Leviton MP, et al. (2013) An attenuated cytomegalovirus vaccine with a deletion of a viral chemokine gene is protective against congenital CMV transmission in a guinea pig model. Clin Dev Immunol 2013:906948.
9. Chatterjee A, Harrison CJ, Britt WJ, Bewtra C (2001) Modification of maternal and congenital cytomegalovirus infection by anti-glycoprotein b antibody transfer in guinea pigs. J Infect Dis 183(11):1547-1553.
10. Auerbach MR, et al. (2014) A neutralizing anti-gH/gL monoclonal antibody is protective in the guinea pig model of congenital CMV infection. PLoS Pathog 10(4):e1004060.
11. Schleiss MR, et al. (2014) Glycoprotein B (gB) vaccines adjuvanted with AS01 or AS02 protect female guinea pigs against cytomegalovirus (CMV) viremia and offspring mortality in a CMV-challenge model. Vaccine 32(23):2756-2762.
12. Pass RF, et al. (2009) Vaccine prevention of maternal cytomegalovirus infection. N Engl J Med 360(12):1191-1199.
13. Revello MG, et al.; CHIP Study Group (2014) A randomized trial of hyperimmune globulin to prevent congenital cytomegalovirus. N Engl J Med 370(14):1316-1326.
14. Lockridge KM, et al. (1999) Pathogenesis of experimental rhesus cytomegalovirus infection. J Virol 73(11):9576-9583.
15. Antoine P, et al. (2012) Functional exhaustion of CD4+ T lymphocytes during primary cytomegalovirus infection. J Immunol 189(5):2665-2672.
16. Yue Y, Zhou SS, Barry PA (2003) Antibody responses to rhesus cytomegalovirus glycoprotein B in naturally infected rhesus macaques. J Gen Virol 84(Pt 12):3371-3379.
17. Hansen SG, Strelow LI, Franchi DC, Anders DG, Wong SW (2003) Complete sequence and genomic analysis of rhesus cytomegalovirus. J Virol 77(12):6620-6636.
18. Rivailler P, Kaur A, Johnson RP, Wang F (2006) Genomic sequence of rhesus cytomegalovirus 180.92: Insights into the coding potential of rhesus cytomegalovirus. J Virol 80(8):4179-4182.
19. Yue Y, Barry PA (2008) Rhesus cytomegalovirus a nonhuman primate model for the study of human cytomegalovirus. Adv Virus Res 72:207-226.
20. London WT, et al. (1986) Experimental congenital disease with simian cytomegalovirus in rhesus monkeys. Teratology 33(3):323-331.
21. Tarantal AF, et al. (1998) Neuropathogenesis induced by rhesus cytomegalovirus in fetal rhesus monkeys (Macaca mulatta). J Infect Dis 177(2):446-450.
22. Vogel P, Weigler BJ, Kerr H, Hendrickx AG, Barry PA (1994) Seroepidemiologic studies of cytomegalovirus infection in a breeding population of rhesus macaques. Lab Anim Sci 44(1):25-30.
23. Asher DM, Gibbs CJ Jr, Lang DJ, Gajdusek DC, Chanock RM (1974) Persistent shedding of cytomegalovirus in the urine of healthy Rhesus monkeys. Proc Soc Exp Biol Med 145(3):794-801.
24. Kaur A, et al. (1996) Cytotoxic T-lymphocyte responses to cytomegalovirus in normal and simian immunodeficiency virus-infected rhesus macaques. J Virol 70(11):7725-7733.
25. Oxford KL, et al. (2011) Open reading frames carried on UL/b′ are implicated in shedding and horizontal transmission of rhesus cytomegalovirus in rhesusmonkeys. J Virol 85(10):5105-5114.
26. Kaur A, et al. (2002) Decreased frequency of cytomegalovirus (CMV)-specific CD4+ T lymphocytes in simian immunodeficiency virus-infected rhesus macaques: Inverse relationship with CMV viremia. J Virol 76(8):3646-3658.
27. Widmann T, et al. (2008) Levels of CMV specific CD4 T cells are dynamic and correlate with CMV viremia after allogeneic stem cell transplantation. PLoS One 3(11):e3634.
28. Bronke C, et al. (2005) Dynamics of cytomegalovirus (CMV)-specific T cells in HIV-1-infected individuals progressing to AIDS with CMV end-organ disease. J Infect Dis 191(6):873-880.
29. Assaf BT, et al. (2014) Limited dissemination and shedding of the UL128 complexintact, UL/b′-defective rhesus cytomegalovirus strain 180.92. J Virol 88(16):9310-9320.
30. Yue Y, et al. (2008) Evaluation of recombinant modified vaccinia Ankara virus-based rhesus cytomegalovirus vaccines in rhesus macaques. Med Microbiol Immunol (Berl) 197(2):117-123.
31. Boppana SB, et al.; National Institute on Deafness and Other Communication Disorders CHIMES Study (2011) Saliva polymerase-chain-reaction assay for cytomegalovirus screening in newborns. N Engl J Med 364(22):2111-2118.
32. Boppana SB, Ross SA, Fowler KB (2013) Congenital cytomegalovirus infection: Clinical outcome. Clin Infect Dis 57(Suppl 4):S178-S181.
33. Renzette N, Bhattacharjee B, Jensen JD, Gibson L, Kowalik TF (2011) Extensive genome- wide variability of human cytomegalovirus in congenitally infected infants. PLoS Pathog 7(5):e1001344.
34. Boppana SB, Britt WJ (1995) Antiviral antibody responses and intrauterine transmission after primary maternal cytomegalovirus infection. J Infect Dis 171(5):1115-1121.
35. Lilleri D, et al. (2013) Fetal human cytomegalovirus transmission correlates with delayed maternal antibodies to gH/gL/pUL128-130-131 complex during primary infection. PLoS One 8(3):e59863.
36. Boppana SB, Pass RF, Britt WJ, Stagno S, Alford CA (1992) Symptomatic congenital cytomegalovirus infection: Neonatal morbidity and mortality. Pediatr Infect Dis J 11(2):93-99.
37. Iwasenko JM, et al. (2011) Human cytomegalovirus infection is detected frequently in stillbirths and is associated with fetal thrombotic vasculopathy. J Infect Dis 203(11):1526-1533.
38. Antoine P, et al. (2014) Postnatal acquisition of primary rhesus cytomegalovirus infection is associated with prolonged virus shedding and impaired CD4+ T lymphocyte function. J Infect Dis 210(7):1090-1099.
39. Tu W, et al. (2004) Persistent and selective deficiency of CD4+ T cell immunity to cytomegalovirus in immunocompetent young children. J Immunol 172(5):3260-3267.
40. Calleja-Aguius J, Muttukrishna S, Jauniaux E (2012) The role of tumor necrosis factorreceptors in pregnancy with normal and adverse outcome. IJICMR 2012(4):1-15.
41. Toder V, Fein A, Carp H, Torchinsky A (2003) TNF-α in pregnancy loss and embryo maldevelopment: A mediator of detrimental stimuli or a protector of the fetoplacental unit? J Assist Reprod Genet 20(2):73-81.
42. Maidji E, McDonagh S, Genbacev O, Tabata T, Pereira L (2006) Maternal antibodies enhance or prevent cytomegalovirus infection in the placenta by neonatal Fc receptor- mediated transcytosis. Am J Pathol 168(4):1210-1226.
43. Schleiss MR, McVoy MA (2010) Guinea pig cytomegalovirus (GPCMV): Amodel for the study of the prevention and treatment of maternal-fetal transmission. Future Virol 5(2):207-217.
44. De Ruick EPCT, Van Esch E (2008) The macaque placenta: A mini-review. Toxicol Pathol 36(7):1085-1185.
45. National Research Council (2011) Guide for the Care and Use of Laboratory Animals (National Academies Press, Washington, DC), 8th Ed.
46. Keele BF, et al. (2008) Identification and characterization of transmitted and early founder virus envelopes in primary HIV-1 infection. Proc Natl Acad Sci USA 105(21):7552-7557.
47. Wussow F, et al. (2013) A vaccine based on the rhesus cytomegalovirus UL128 complex induces broadly neutralizing antibodies in rhesus macaques. J Virol 87(3):1322-1332.
48. Abel K, et al. (2011) Vaccine-induced control of viral shedding following rhesus cytomegalovirus challenge in rhesus macaques. J Virol 85(6):2878-2890.
49. Tarantal AF (2005) Ultrasound imaging in rhesus (Macaca mulatta) and long-tailed (Macaca fascicularis) macaques: Reproductive and research applications. The Laboratory Primate, ed Wolfe-Coote S (Elsevier Academic, San Diego), pp 331-334.
50. Tarantal AF, Hendrickx AG (1988) Use of ultrasound for early pregnancy detection in the rhesus and cynomolgus macaque (Macaca mulatta and Macaca fascicularis). J Med Primatol 17(2):105-112.