Viral persistence induces antibody inflation without altering antibody avidity

Journal of Virology

Volumn 90, Issue 9, 2016, Pages 4402-4411

  Welten, Suzanne P M ^a   Redeker, Anke ^a   Toes, René E M ^a   Arens, Ramon ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

B7 ANTIGEN; CD27 ANTIGEN; CD28 ANTIGEN; CD70 ANTIGEN; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; NEUTRALIZING ANTIBODY; VIRUS ANTIBODY;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY AVIDITY; ANTIBODY INFLATION; ANTIBODY RESPONSE; ARTICLE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOMEGALOVIRUS INFECTION; GERMINAL CENTER; IN VITRO STUDY; IN VIVO STUDY; INOCULATION; MEMORY CELL; MOUSE; NONHUMAN; PLASMA CELL; PRIORITY JOURNAL; VIRUS NEUTRALIZATION; VIRUS PARTICLE; ANIMAL; ANTIBODY AFFINITY; BLOOD; ENZYME LINKED IMMUNOSORBENT ASSAY; HERPES VIRUS INFECTION; HOST PATHOGEN INTERACTION; IMMUNOLOGY; KNOCKOUT MOUSE; METABOLISM; MUROMEGALOVIRUS; SERODIAGNOSIS; T LYMPHOCYTE SUBPOPULATION; VIROLOGY; VIRUS LOAD;

ANIMALS; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; ANTIBODY AFFINITY; ANTIGENS, CD28; B7 ANTIGENS; CD4-POSITIVE T-LYMPHOCYTES; ENZYME-LINKED IMMUNOSORBENT ASSAY; HERPESVIRIDAE INFECTIONS; HOST-PATHOGEN INTERACTIONS; IMMUNOGLOBULIN G; MICE; MICE, KNOCKOUT; MUROMEGALOVIRUS; NEUTRALIZATION TESTS; T-LYMPHOCYTE SUBSETS; VIRAL LOAD;

EID: 84964963323     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.03177-15     Document Type: Article

References (56)

1. Amanna IJ, Slifka MK. 2010. Mechanisms that determine plasma cell lifespan and the duration of humoral immunity. Immunol Rev 236:125-138. http://dx.doi.org/10.1111/j.1600-065X.2010.00912.x.
2. Tarlinton D, Good-Jacobson K. 2013. Diversity among memory B cells: origin, consequences, and utility. Science 341:1205-1211. http://dx.doi.org/10.1126/science.1241146.
3. Amanna IJ, Slifka MK, Crotty S. 2006. Immunity and immunological memory following smallpox vaccination. Immunol Rev 211:320-337. http://dx.doi.org/10.1111/j.0105-2896.2006.00392.x.
4. Nutt SL, Hodgkin PD, Tarlinton DM, Corcoran LM. 2015. The generation of antibody-secreting plasma cells. Nat Rev Immunol 15:160-171. http://dx.doi.org/10.1038/nri3795.
5. Hansen SG, Ford JC, Lewis MS, Ventura AB, Hughes CM, Coyne-Johnson L, Whizin N, Oswald K, Shoemaker R, Swanson T, Legasse AW, Chiuchiolo MJ, Parks CL, Axthelm MK, Nelson JA, Jarvis MA, Piatak M, Jr, Lifson JD, Picker LJ. 2011. Profound early control of highly pathogenic SIV by an effector memory T-cell vaccine. Nature 473:523-527. http://dx.doi.org/10.1038/nature10003.
6. Tsuda Y, Caposio P, Parkins CJ, Botto S, Messaoudi I, Cicin-Sain L, Feldmann H, Jarvis MA. 2011. A replicating cytomegalovirus-based vaccine encoding a single Ebola virus nucleoprotein CTL epitope confers protection against Ebola virus. PLoS Negl Trop Dis 5:e1275. http://dx.doi.org/10.1371/journal.pntd.0001275.
7. Karrer U, Wagner M, Sierro S, Oxenius A, Hengel H, Dumrese T, Freigang S, Koszinowski UH, Phillips RE, Klenerman P. 2004. Expansion of protective CD8+ T-cell responses driven by recombinant cytomegaloviruses. J Virol 78:2255-2264. http://dx.doi.org/10.1128/JVI.78.5.2255-2264.2004.
8. Tierney R, Nakai T, Parkins CJ, Caposio P, Fairweather NF, Sesardic D, Jarvis MA. 2012. A single-dose cytomegalovirus-based vaccine encoding tetanus toxin fragment C induces sustained levels of protective tetanus toxin antibodies in mice. Vaccine 30:3047-3052. http://dx.doi.org/10.1016/j.vaccine.2012.02.043.
9. Xu G, Smith T, Grey F, Hill AB. 2013. Cytomegalovirus-based cancer vaccines expressing TRP2 induce rejection of melanoma in mice. Biochem Biophys Res Commun 437:287-291. http://dx.doi.org/10.1016/j.bbrc.2013.06.068.
10. O'Hara GA, Welten SP, Klenerman P, Arens R. 2012. Memory T cell inflation: understanding cause and effect. Trends Immunol 33:84-90. http://dx.doi.org/10.1016/j.it.2011.11.005.
11. Coquet JM, Middendorp S, van der Horst G, Kind J, Veraar EA, Xiao Y, Jacobs H, Borst J. 2013. The CD27 and CD70 costimulatory pathway inhibits effector function of T helper 17 cells and attenuates associated autoimmunity. Immunity 38:53-65. http://dx.doi.org/10.1016/j.immuni.2012.09.009.
12. Borriello F, Sethna MP, Boyd SD, Schweitzer AN, Tivol EA, Jacoby D, Strom TB, Simpson EM, Freeman GJ, Sharpe AH. 1997. B7-1 and B7-2 have overlapping, critical roles in immunoglobulin class switching and germinal center formation. Immunity 6:303-313. http://dx.doi.org/10.1016/S1074-7613(00)80333-7.
13. Welten SP, Redeker A, Franken KL, Oduro JD, Ossendorp F, Cicin-Sain L, Melief CJ, Aichele P, Arens R. 2015. The viral context instructs the redundancy of costimulatory pathways in driving CD8(+) T cell expansion. eLife 4:e07486. http://dx.doi.org/10.7554/eLife.07486.
14. Schneider K, Loewendorf A, De TC, Fulton J, Rhode A, Shumway H, Ha S, Patterson G, Pfeffer K, Nedospasov SA, Ware CF, Benedict CA. 2008. Lymphotoxin-mediated crosstalk between B cells and splenic stroma promotes the initial type I interferon response to cytomegalovirus. Cell Host Microbe 3:67-76. http://dx.doi.org/10.1016/j.chom.2007.12.008.
15. Redeker A, Welten SP, Arens R. 2014. Viral inoculum dose impacts memory T-cell inflation. Eur J Immunol 44:1046-1057. http://dx.doi.org/10.1002/eji.201343946.
16. Suwannalai P, Scherer HU, van der Woude D, Ioan-Facsinay A, Jol-van der Zijde CM, van Tol MJ, Drijfhout JW, Huizinga TW, Toes RE, Trouw LA. 2011. Anti-citrullinated protein antibodies have a low avidity compared with antibodies against recall antigens. Ann Rheum Dis 70:373-379. http://dx.doi.org/10.1136/ard.2010.135509.
17. Crotty S, Kersh EN, Cannons J, Schwartzberg PL, Ahmed R. 2003. SAP is required for generating long-term humoral immunity. Nature 421:282-287. http://dx.doi.org/10.1038/nature01318.
18. Welten SP, Redeker A, Franken KL, Benedict CA, Yagita H, Wensveen FM, Borst J, Melief CJ, van Lier RA, van Gisbergen KP, Arens R. 2013. CD27-CD70 costimulation controls T cell immunity during acute and persistent cytomegalovirus infection. J Virol 87:6851-6865. http://dx.doi.org/10.1128/JVI.03305-12.
19. Munks MW, Gold MC, Zajac AL, Doom CM, Morello CS, Spector DH, Hill AB. 2006. Genome-wide analysis reveals a highly diverse CD8 T cell response to murine cytomegalovirus. J Immunol 176:3760-3766. http://dx.doi.org/10.4049/jimmunol.176.6.3760.
20. Arens R, Wang P, Sidney J, Loewendorf A, Sette A, Schoenberger SP, Peters B, Benedict CA. 2008. Cutting edge: murine cytomegalovirus induces a polyfunctional CD4 T cell response. J Immunol 180:6472-6476. http://dx.doi.org/10.4049/jimmunol.180.10.6472.
21. Coutelier JP, van der Logt JT, Heessen FW, Vink A, Van SJ. 1988. Virally induced modulation of murine IgG antibody subclasses. J Exp Med 168:2373-2378. http://dx.doi.org/10.1084/jem.168.6.2373.
22. Coutelier JP, van der Logt JT, Heessen FW, Warnier G, Van SJ. 1987. IgG2a restriction of murine antibodies elicited by viral infections. J Exp Med 165:64-69. http://dx.doi.org/10.1084/jem.165.1.64.
23. Miao H, Hollenbaugh JA, Zand MS, Holden-Wiltse J, Mosmann TR, Perelson AS, Wu H, Topham DJ. 2010. Quantifying the early immune response and adaptive immune response kinetics in mice infected with influenza A virus. J Virol 84:6687-6698. http://dx.doi.org/10.1128/JVI.00266-10.
24. Arens R, Loewendorf A, Her MJ, Schneider-Ohrum K, Shellam GR, Janssen E, Ware CF, Schoenberger SP, Benedict CA. 2011. B7-mediated costimulation of CD4 T cells constrains cytomegalovirus persistence. J Virol 85:390-396. http://dx.doi.org/10.1128/JVI.01839-10.
25. Boettler T, Moeckel F, Cheng Y, Heeg M, Salek-Ardakani S, Crotty S, Croft M, von Herrath MG. 2012. OX40 facilitates control of a persistent virus infection. PLoS Pathog 8:e1002913. http://dx.doi.org/10.1371/journal.ppat.1002913.
26. Clouthier DL, Zhou AC, Wortzman ME, Luft O, Levy GA, Watts TH. 2015. GITR intrinsically sustains early type 1 and late follicular helper CD4 T cell accumulation to control a chronic viral infection. PLoS Pathog 11:e1004517. http://dx.doi.org/10.1371/journal.ppat.1004517.
27. Raftery MJ, Wolter E, Fillatreau S, Meisel H, Kaufmann SH, Schonrich G. 2014. NKT cells determine titer and subtype profile of virus-specific IgG antibodies during herpes simplex virus infection. J Immunol 192: 4294-4302. http://dx.doi.org/10.4049/jimmunol.1300148.
28. Fornara C, Furione M, Lilleri D, Cane I, Revello MG, Zavattoni M, Gerna G. 2015. Primary human cytomegalovirus infections: kinetics of ELISA-IgG and neutralizing antibody in pauci/asymptomatic pregnant women vs symptomatic non-pregnant subjects. J Clin Virol 64:45-51. http://dx.doi.org/10.1016/j.jcv.2015.01.004.
29. Gerna G, Lilleri D, Fornara C, Bruno F, Gabanti E, Cane I, Furione M, Revello MG. 2015. Differential kinetics of human cytomegalovirus load and antibody responses in primary infection of the immunocompetent and immunocompromised host. J Gen Virol 96:360-369. http://dx.doi.org/10.1099/vir.0.070441-0.
30. Xiao Y, Hendriks J, Langerak P, Jacobs H, Borst J. 2004. CD27 is acquired by primed B cells at the centroblast stage and promotes germinal center formation. J Immunol 172:7432-7441. http://dx.doi.org/10.4049/jimmunol.172.12.7432.
31. Bertram EM, Tafuri A, Shahinian A, Chan VS, Hunziker L, Recher M, Ohashi PS, Mak TW, Watts TH. 2002. Role of ICOS versus CD28 in antiviral immunity. Eur J Immunol 32:3376-3385. http://dx.doi.org/10.1002/1521-4141(200212)32:12<3376::AID-IMMU3376>3.0.CO;2-Y.
32. Slifka MK, Matloubian M, Ahmed R. 1995. Bone marrow is a major site of long-term antibody production after acute viral infection. J Virol 69: 1895-1902.
33. Lawson CM, Grundy JE, Shellam GR. 1988. Antibody responses to murine cytomegalovirus in genetically resistant and susceptible strains of mice. J Gen Virol 69(Part 8):1987-1998. http://dx.doi.org/10.1099/0022-1317-69-8-1987.
34. Cekinovic D, Golemac M, Pugel EP, Tomac J, Cicin-Sain L, Slavuljica I, Bradford R, Misch S, Winkler TH, Mach M, Britt WJ, Jonjic S. 2008. Passive immunization reduces murine cytomegalovirus-induced brain pathology in newborn mice. J Virol 82:12172-12180. http://dx.doi.org/10.1128/JVI.01214-08.
35. Jonjic S, Pavic I, Polic B, Crnkovic I, Lucin P, Koszinowski UH. 1994. Antibodies are not essential for the resolution of primary cytomegalovirus infection but limit dissemination of recurrent virus. J Exp Med 179:1713-1717. http://dx.doi.org/10.1084/jem.179.5.1713.
36. Klenovsek K, Weisel F, Schneider A, Appelt U, Jonjic S, Messerle M, Bradel-Tretheway B, Winkler TH, Mach M. 2007. Protection from CMV infection in immunodeficient hosts by adoptive transfer of memory B cells. Blood 110:3472-3479. http://dx.doi.org/10.1182/blood-2007-06-095414.
37. Nigro G, Adler SP, La TR, Best AM. 2005. Passive immunization during pregnancy for congenital cytomegalovirus infection. N Engl J Med 353: 1350-1362. http://dx.doi.org/10.1056/NEJMoa043337.
38. Shanley JD, Jordan MC, Stevens JG. 1981. Modification by adoptive humoral immunity of murine cytomegalovirus infection. J Infect Dis 143: 231-237. http://dx.doi.org/10.1093/infdis/143.2.231.
39. Wirtz N, Schader SI, Holtappels R, Simon CO, Lemmermann NA, Reddehase MJ, Podlech J. 2008. Polyclonal cytomegalovirus-specific antibodies not only prevent virus dissemination from the portal of entry but also inhibit focal virus spread within target tissues. Med Microbiol Immunol 197:151-158. http://dx.doi.org/10.1007/s00430-008-0095-0.
40. Hangartner L, Zinkernagel RM, Hengartner H. 2006. Antiviral antibody responses: the two extremes of a wide spectrum. Nat Rev Immunol 6:231-243. http://dx.doi.org/10.1038/nri1783.
41. Racine R, McLaughlin M, Jones DD, Wittmer ST, MacNamara KC, Woodland DL, Winslow GM. 2011. IgM production by bone marrow plasmablasts contributes to long-term protection against intracellular bacterial infection. J Immunol 186:1011-1021. http://dx.doi.org/10.4049/jimmunol.1002836.
42. Taillardet M, Haffar G, Mondiere P, Asensio MJ, Gheit H, Burdin N, Defrance T, Genestier L. 2009. The thymus-independent immunity conferred by a pneumococcal polysaccharide is mediated by long-lived plasma cells. Blood 114:4432-4440. http://dx.doi.org/10.1182/blood-2009-01-200014.
43. Foote JB, Mahmoud TI, Vale AM, Kearney JF. 2012. Long-term maintenance of polysaccharide-specific antibodies by IgM-secreting cells. J Immunol 188:57-67. http://dx.doi.org/10.4049/jimmunol.1100783.
44. Prince HE, Lape-Nixon M. 2014. Role of cytomegalovirus (CMV) IgG avidity testing in diagnosing primary CMV infection during pregnancy. Clin Vaccine Immunol 21:1377-1384. http://dx.doi.org/10.1128/CVI.00487-14.
45. Pedersen GK, Hoschler K, Oie Solbak SM, Bredholt G, Pathirana RD, Afsar A, Breakwell L, Nostbakken JK, Raae AJ, Brokstad KA, Sjursen H, Zambon M, Cox RJ. 2014. Serum IgG titres, but not avidity, correlates with neutralizing antibody response after H5N1 vaccination. Vaccine 32: 4550-4557. http://dx.doi.org/10.1016/j.vaccine.2014.06.009.
46. Grewal JS, Pilgrim MJ, Grewal S, Kasman L, Werner P, Bruorton ME, London SD, London L. 2011. Salivary glands act as mucosal inductive sites via the formation of ectopic germinal centers after site-restricted MCMVinfection. FASEB J 25:1680-1696. http://dx.doi.org/10.1096/fj.10-174656.
47. Simon CO, Kuhnapfel B, Reddehase MJ, Grzimek NK. 2007. Murine cytomegalovirus major immediate-early enhancer region operating as a genetic switch in bidirectional gene pair transcription. J Virol 81:7805-7810. http://dx.doi.org/10.1128/JVI.02388-06.
48. Penaloza-Macmaster P, Rasheed AU, Iyer SS, Yagita H, Blazar BR, Ahmed R. 2011. Opposing effects of CD70 costimulation during acute and chronic lymphocytic choriomeningitis virus infection of mice. J Virol 85:6168-6174. http://dx.doi.org/10.1128/JVI.02205-10.
49. Matter M, Odermatt B, Yagita H, Nuoffer JM, Ochsenbein AF. 2006. Elimination of chronic viral infection by blocking CD27 signaling. J Exp Med 203:2145-2155. http://dx.doi.org/10.1084/jem.20060651.
50. Arens R, Tesselaar K, Baars PA, van Schijndel GM, Hendriks J, Pals ST, Krimpenfort P, Borst J, van Oers MH, van Lier RA. 2001. Constitutive CD27/CD70 interaction induces expansion of effector-type T cells and results in IFNgamma-mediated B cell depletion. Immunity 15:801-812. http://dx.doi.org/10.1016/S1074-7613(01)00236-9.
51. Bertram EM, Lau P, Watts TH. 2002. Temporal segregation of 4-1BB versus CD28-mediated costimulation: 4-1BB ligand influences T cell numbers late in the primary response and regulates the size of the T cell memory response following influenza infection. J Immunol 168:3777-3785. http://dx.doi.org/10.4049/jimmunol.168.8.3777.
52. Edelmann KH, Wilson CB. 2001. Role of CD28/CD80-86 and CD40/CD154 costimulatory interactions in host defense to primary herpes simplex virus infection. J Virol 75:612-621. http://dx.doi.org/10.1128/JVI.75.2.612-621.2001.
53. Salek-Ardakani S, Arens R, Flynn R, Sette A, Schoenberger SP, Croft M. 2009. Preferential use of B7.2 and not B7.1 in priming of vaccinia virusspecific CD8 T cells. J Immunol 182:2909-2918. http://dx.doi.org/10.4049/jimmunol.0803545.
54. Rozanski CH, Arens R, Carlson LM, Nair J, Boise LH, Chanan-Khan AA, Schoenberger SP, Lee KP. 2011. Sustained antibody responses depend on CD28 function in bone marrow-resident plasma cells. J Exp Med 208:1435-1446. http://dx.doi.org/10.1084/jem.20110040.
55. Klyushnenkova EN, Kouiavskaia DV, Parkins CJ, Caposio P, Botto S, Alexander RB, Jarvis MA. 2012. A cytomegalovirus-based vaccine expressing a single tumor-specific CD8+ T-cell epitope delays tumor growth in a murine model of prostate cancer. J Immunother 35:390-399. http://dx.doi.org/10.1097/CJI.0b013e3182585d50.
56. Qiu Z, Huang H, Grenier JM, Perez OA, Smilowitz HM, Adler B, Khanna KM. 2015. Cytomegalovirus based vaccine expressing a modified tumor antigen induces potent tumor-specific CD8+ T cell response and protects mice from melanoma. Cancer Immunol Res 3:536-546. http://dx.doi.org/10.1158/2326-6066.CIR-14-0044.