#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Immunization with a murine cytomegalovirus based vector encoding retrovirus envelope confers strong protection from Friend retrovirus challenge infection


Autoři: Nadine Bongard aff001;  Vu Thuy Khanh Le-Trilling aff001;  Anna Malyshkina aff001;  Meike Rückborn aff001;  Kerstin Wohlgemuth aff001;  Ina Wensing aff001;  Sonja Windmann aff001;  Ulf Dittmer aff001;  Mirko Trilling aff001;  Wibke Bayer aff001
Působiště autorů: Institute for Virology, University Hospital Essen, University Duisburg-Essen, Essen, Germany aff001
Vyšlo v časopise: Immunization with a murine cytomegalovirus based vector encoding retrovirus envelope confers strong protection from Friend retrovirus challenge infection. PLoS Pathog 15(9): e32767. doi:10.1371/journal.ppat.1008043
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.ppat.1008043

Souhrn

Immunization vectors based on cytomegalovirus (CMV) have attracted a lot of interest in recent years because of their high efficacy in the simian immunodeficiency virus (SIV) macaque model, which has been attributed to their ability to induce strong, unusually broad, and unconventionally restricted CD8+ T cell responses. To evaluate the ability of CMV-based vectors to mediate protection by other immune mechanisms, we evaluated a mouse CMV (MCMV)-based vector encoding Friend virus (FV) envelope (Env), which lacks any known CD8+ T cell epitopes, for its protective efficacy in the FV mouse model. When we immunized highly FV-susceptible mice with the Env-encoding MCMV vector (MCMV.env), we could detect high frequencies of Env-specific CD4+ T cells after a single immunization. While the control of an early FV challenge infection was highly variable, an FV infection applied later after immunization was tightly controlled by almost all immunized mice. Protection of mice correlated with their ability to mount a robust anamnestic neutralizing antibody response upon FV infection, but Env-specific CD4+ T cells also produced appreciable levels of interferon γ. Depletion and transfer experiments underlined the important role of antibodies for control of FV infection but also showed that while no Env-specific CD8+ T cells were induced by the MCMV.env vaccine, the presence of CD8+ T cells at the time of FV challenge was required. The immunity induced by MCMV.env immunization was long-lasting, but was restricted to MCMV naïve animals. Taken together, our results demonstrate a novel mode of action of a CMV-based vaccine for anti-retrovirus immunization that confers strong protection from retrovirus challenge, which is conferred by CD4+ T cells and antibodies.

Klíčová slova:

Antibodies – Antibody response – Cytotoxic T cells – Immune response – Mouse models – Spleen – T cells – Viral load


Zdroje

1. Stern-Ginossar N, Weisburd B, Michalski A, Le VT, Hein MY, Huang SX, et al. Decoding human cytomegalovirus. Science. 2012;338(6110):1088–93. Epub 2012/11/28. doi: 10.1126/science.1227919 23180859.

2. Jackson SE, Mason GM, Wills MR. Human cytomegalovirus immunity and immune evasion. Virus Res. 2011;157(2):151–60. Epub 2010/11/09. doi: 10.1016/j.virusres.2010.10.031 21056604.

3. Emery VC. Investigation of CMV disease in immunocompromised patients. J Clin Pathol. 2001;54(2):84–8. Epub 2001/02/24. doi: 10.1136/jcp.54.2.84 11215290.

4. O'Hara GA, Welten SP, Klenerman P, Arens R. Memory T cell inflation: understanding cause and effect. Trends Immunol. 2012;33(2):84–90. Epub 2012/01/10. doi: 10.1016/j.it.2011.11.005 22222196.

5. Seckert CK, Griessl M, Buttner JK, Scheller S, Simon CO, Kropp KA, et al. Viral latency drives 'memory inflation': a unifying hypothesis linking two hallmarks of cytomegalovirus infection. Med Microbiol Immunol. 2012;201(4):551–66. Epub 2012/09/20. doi: 10.1007/s00430-012-0273-y 22991040.

6. Karrer U, Wagner M, Sierro S, Oxenius A, Hengel H, Dumrese T, et al. Expansion of protective CD8+ T-cell responses driven by recombinant cytomegaloviruses. J Virol. 2004;78(5):2255–64. Epub 2004/02/14. doi: 10.1128/JVI.78.5.2255-2264.2004 14963122.

7. Tsuda Y, Caposio P, Parkins CJ, Botto S, Messaoudi I, Cicin-Sain L, et al. A replicating cytomegalovirus-based vaccine encoding a single Ebola virus nucleoprotein CTL epitope confers protection against Ebola virus. PLoS Negl Trop Dis. 2011;5(8):e1275. Epub 2011/08/23. doi: 10.1371/journal.pntd.0001275 21858240.

8. Tierney R, Nakai T, Parkins CJ, Caposio P, Fairweather NF, Sesardic D, et al. A single-dose cytomegalovirus-based vaccine encoding tetanus toxin fragment C induces sustained levels of protective tetanus toxin antibodies in mice. Vaccine. 2012;30(20):3047–52. Epub 2012/03/15. doi: 10.1016/j.vaccine.2012.02.043 22414558.

9. Marzi A, Murphy AA, Feldmann F, Parkins CJ, Haddock E, Hanley PW, et al. Cytomegalovirus-based vaccine expressing Ebola virus glycoprotein protects nonhuman primates from Ebola virus infection. Sci Rep. 2016;6:21674. Epub 2016/02/16. doi: 10.1038/srep21674 26876974.

10. Hansen SG, Ford JC, Lewis MS, Ventura AB, Hughes CM, Coyne-Johnson L, et al. Profound early control of highly pathogenic SIV by an effector memory T-cell vaccine. Nature. 2011;473:523–9. doi: 10.1038/nature10003 21562493

11. Hansen SG, Sacha JB, Hughes CM, Ford JC, Burwitz BJ, Scholz I, et al. Cytomegalovirus Vectors Violate CD8+ T Cell Epitope Recognition Paradigms. Science. 2016;340(6135):1237874.

12. Hansen SG, Wu HL, Burwitz BJ, Hughes CM, Hammond KB, Ventura AB, et al. Broadly targeted CD8+ T cell responses restricted by major histocompatibility complex E. Science. 2016;351(6274):714–20. doi: 10.1126/science.aac9475 26797147

13. Fruh K, Picker L. CD8+ T cell programming by cytomegalovirus vectors: applications in prophylactic and therapeutic vaccination. Curr Opin Immunol. 2017;47:52–6. Epub 2017/07/25. doi: 10.1016/j.coi.2017.06.010 28734175.

14. Friend C. Cell-free transmission in adult Swiss mice of a disease having the character of a leukemia. J Exp Med. 1957;105(4):307–18. doi: 10.1084/jem.105.4.307 13416470

15. Miyazawa M, Tsuji-Kawahara S, Kanari Y. Host genetic factors that control immune responses to retrovirus infections. Vaccine. 2008;26(24):2981–96. Epub 2008/02/08. doi: 10.1016/j.vaccine.2008.01.004 18255203.

16. Windmann S, Otto L, Hrycak CP, Malyshkina A, Bongard N, David P, et al. Infection of B Cell-Follicle-Resident Cells by Friend Retrovirus Occurs during Acute Infection and Is Maintained during Viral Persistence. mBio. 2019. doi: 10.1128/mBio.00004-19 30782653

17. Zelinskyy G, Robertson SJ, Schimmer S, Messer RJ, Hasenkrug KJ, Dittmer U. CD8+ T-cell dysfunction due to cytolytic granule deficiency in persistent Friend retrovirus infection. J Virol. 2005;79(16):10619–26. Epub 2005/07/30. doi: 10.1128/JVI.79.16.10619-10626.2005 16051854.

18. Zelinskyy G, Werner T, Dittmer U. Natural regulatory T cells inhibit production of cytotoxic molecules in CD8(+) T cells during low-level Friend retrovirus infection. Retrovirology. 2013;10:109. Epub 2013/10/26. doi: 10.1186/1742-4690-10-109 24156479.

19. Dittmer U, Brooks DM, Hasenkrug KJ. Characterization of a live-attenuated retroviral vaccine demonstrates protection via immune mechanisms. J Virol. 1998;72(8):6554–8. 9658099

20. Dittmer U, Brooks DM, Hasenkrug KJ. Requirement for multiple lymphocyte subsets in protection by a live attenuated vaccine against retroviral infection. Nat Med. 1999;5(2):189–93. doi: 10.1038/5550 9930867

21. Dittmer U, Brooks DM, Hasenkrug KJ. Protection against establishment of retroviral persistence by vaccination with a live attenuated virus. J Virol. 1999;73(5):3753–7. 10196269

22. Messer RJ, Dittmer U, Peterson KE, Hasenkrug KJ. Essential role for virus-neutralizing antibodies in sterilizing immunity against Friend retrovirus infection. Proc Natl Acad Sci U S A. 2004;101(33):12260–5. doi: 10.1073/pnas.0404769101 15297622

23. Halemano K, Barrett BS, Li SX, Harper MS, Smith DS, Heilman KJ, et al. Fv1 restriction and retrovirus vaccine immunity in Apobec3-deficient 129P2 mice. PLoS One. 2013;8(3):e60500. doi: 10.1371/journal.pone.0060500 23533681

24. Ishihara C, Miyazawa M, Nishio J, Azuma I, Chesebro B. Use of low toxicity adjuvants and killed virus to induce protective immunity against the Friend murine leukaemia retrovirus-induced disease. Vaccine. 1992;10(5):353–6. doi: 10.1016/0264-410x(92)90378-w 1574922

25. Ishihara C, Miyazawa M, Nishio J, Chesebro B. Induction of protective immunity to Friend murine leukemia virus in genetic nonresponders to virus envelope protein. J Immunol. 1991;146(11):3958–63. 2033265

26. Iwanami N, Niwa A, Yasutomi Y, Tabata N, Miyazawa M. Role of natural killer cells in resistance against friend retrovirus-induced leukemia. J Virol. 2001;75(7):3152–63. doi: 10.1128/JVI.75.7.3152-3163.2001 11238842

27. Kleiser C, Schneider J, Bayer H, Hunsmann G. Immunoprevention of Friend leukaemia virus-induced erythroleukaemia by vaccination with aggregated gp70. J Gen Virol. 1986;67 (Pt 9):1901–7.

28. Miyazawa M, Fujisawa R, Ishihara C, Takei YA, Shimizu T, Uenishi H, et al. Immunization with a single T helper cell epitope abrogates Friend virus-induced early erythroid proliferation and prevents late leukemia development. J Immunol. 1995;155(2):748–58. 7541823

29. Knuschke T, Bayer W, Rotan O, Sokolova V, Wadwa M, Kirschning CJ, et al. Prophylactic and therapeutic vaccination with a nanoparticle-based peptide vaccine induces efficient protective immunity during acute and chronic retroviral infection. Nanomedicine. 2014;10(8):1787–98. doi: 10.1016/j.nano.2014.06.014 25014891

30. Bayer W, Lietz R, Ontikatze T, Johrden L, Tenbusch M, Nabi G, et al. Improved vaccine protection against retrovirus infection after co-administration of adenoviral vectors encoding viral antigens and type I interferon subtypes. Retrovirology. 2011;8:75. doi: 10.1186/1742-4690-8-75 21943056

31. Bayer W, Schimmer S, Hoffmann D, Dittmer U, Wildner O. Evaluation of the Friend Virus model for the development of improved adenovirus-vectored anti-retroviral vaccination strategies. Vaccine. 2008;26(5):716–26. doi: 10.1016/j.vaccine.2007.11.050 18160188

32. Bayer W, Tenbusch M, Lietz R, Johrden L, Schimmer S, Uberla K, et al. Vaccination with an adenoviral vector that encodes and displays a retroviral antigen induces improved neutralizing antibody and CD4+ T-cell responses and confers enhanced protection. J Virol. 2010;84(4):1967–76. doi: 10.1128/JVI.01840-09 20007267

33. Dittmer U, Werner T, Kraft AR. Co-immunization of mice with a retroviral DNA vaccine and GITRL-encoding plasmid augments vaccine-induced protection against retrovirus infection. Viral Immunol. 2008;21(4):459–67. doi: 10.1089/vim.2008.0046 19115935

34. Earl PL, Moss B, Morrison RP, Wehrly K, Nishio J, Chesebro B. T-lymphocyte priming and protection against Friend leukemia by vaccinia-retrovirus env gene recombinant. Science. 1986;234(4777):728–31. doi: 10.1126/science.3490689 3490689

35. Godel P, Windmann S, Dietze KK, Dittmer U, Bayer W. Modification of one epitope-flanking amino acid allows for the induction of friend retrovirus-specific CD8+ T cells by Adenovirus-based immunization. J Virol. 2012;86(22):12422–5. doi: 10.1128/JVI.01607-12 22933287

36. Hasenkrug KJ, Brooks DM, Nishio J, Chesebro B. Differing T-cell requirements for recombinant retrovirus vaccines. J Virol. 1996;70(1):368–72. 8523549

37. Lietz R, Bayer W, Ontikatze T, Johrden L, Tenbusch M, Storcksdieck Genannt BM, et al. Codelivery of the chemokine CCL3 by an adenovirus-based vaccine improves protection from retrovirus infection. J Virol. 2012;86(3):1706–16. doi: 10.1128/JVI.06244-11 22090142

38. Miyazawa M, Nishio J, Chesebro B. Protection against Friend retrovirus-induced leukemia by recombinant vaccinia viruses expressing the gag gene. J Virol. 1992;66(7):4497–507. 1534853

39. Ohs I, Windmann S, Wildner O, Dittmer U, Bayer W. Interleukin-encoding adenoviral vectors as genetic adjuvant for vaccination against retroviral infection. PLoS One. 2013;8(12):e82528. doi: 10.1371/journal.pone.0082528 24349306

40. Kaulfuss M, Wensing I, Windmann S, Hrycak CP, Bayer W. Induction of complex immune responses and strong protection against retrovirus challenge by adenovirus-based immunization depends on the order of vaccine delivery. Retrovirology. 2017;14(1):8. Epub 2017/02/09. doi: 10.1186/s12977-017-0336-7 28166802.

41. Lodoen MB, Lanier LL. Viral modulation of NK cell immunity. Nat Rev Microbiol. 2005;3(1):59–69. Epub 2004/12/21. doi: 10.1038/nrmicro1066 15608700.

42. Ruan KS, Lilly F. Identification of an epitope encoded in the env gene of Friend murine leukemia virus recognized by anti-Friend virus cytotoxic T lymphocytes. Virology. 1991;181(1):91–100. Epub 1991/03/01. doi: 10.1016/0042-6822(91)90473-o 1704662.

43. Chen W, Qin H, Chesebro B, Cheever MA. Identification of a gag-encoded cytotoxic T-lymphocyte epitope from FBL-3 leukemia shared by Friend, Moloney, and Rauscher murine leukemia virus-induced tumors. J Virol. 1996;70(11):7773–82. 8892898

44. Messer RJ, Lavender KJ, Hasenkrug KJ. Mice of the resistant H-2(b) haplotype mount broad CD4(+) T cell responses against 9 distinct Friend virus epitopes. Virology. 2014;456–457:139–44. doi: 10.1016/j.virol.2014.03.012 24889233

45. Schone D, Hrycak CP, Windmann S, Lapuente D, Dittmer U, Tenbusch M, et al. Immunodominance of Adenovirus-Derived CD8(+) T Cell Epitopes Interferes with the Induction of Transgene-Specific Immunity in Adenovirus-Based Immunization. J Virol. 2017;91(20). Epub 2017/08/05. doi: 10.1128/JVI.01184-17 28768877.

46. Bongard N, Lapuente D, Windmann S, Dittmer U, Tenbusch M, Bayer W. Interference of retroviral envelope with vaccine-induced CD8(+) T cell responses is relieved by co-administration of cytokine-encoding vectors. Retrovirology. 2017;14(1):28. Epub 2017/04/30. doi: 10.1186/s12977-017-0352-7 28449719.

47. Francois S, Peng J, Schwarz T, Duppach J, Gibbert K, Dittmer U, et al. NK cells improve control of friend virus infection in mice persistently infected with murine cytomegalovirus. Retrovirology. 2013;10:58. Epub 2013/06/07. doi: 10.1186/1742-4690-10-58 23738889.

48. Lander MR, Chattopadhyay SK. A Mus dunni cell line that lacks sequences closely related to endogenous murine leukemia viruses and can be infected by ectropic, amphotropic, xenotropic, and mink cell focus-forming viruses. J Virol. 1984;52(2):695–8. 6092693

49. Robertson MN, Miyazawa M, Mori S, Caughey B, Evans LH, Hayes SF, et al. Production of monoclonal antibodies reactive with a denatured form of the Friend murine leukemia virus gp70 envelope protein: use in a focal infectivity assay, immunohistochemical studies, electron microscopy and western blotting. J Virol Methods. 1991;34(3):255–71. doi: 10.1016/0166-0934(91)90105-9 1744218

50. Le-Trilling VT, Trilling M. Mouse newborn cells allow highly productive mouse cytomegalovirus replication, constituting a novel convenient primary cell culture system. PLoS One. 2017;12(3):e0174695. Epub 2017/03/25. doi: 10.1371/journal.pone.0174695 28339479.

51. Donnarumma T, Young GR, Merkenschlager J, Eksmond U, Bongard N, Nutt SL, et al. Opposing Development of Cytotoxic and Follicular Helper CD4 T Cells Controlled by the TCF-1-Bcl6 Nexus. Cell Rep. 2016;17(6):1571–83. Epub 2016/11/03. doi: 10.1016/j.celrep.2016.10.013 27806296.

52. Jordan S, Krause J, Prager A, Mitrovic M, Jonjic S, Koszinowski UH, et al. Virus progeny of murine cytomegalovirus bacterial artificial chromosome pSM3fr show reduced growth in salivary Glands due to a fixed mutation of MCK-2. J Virol. 2011;85(19):10346–53. Epub 2011/08/05. doi: 10.1128/JVI.00545-11 21813614.

53. Chesebro B, Wehrly K, Stimpfling J. Host genetic control of recovery from Friend leukemia virus-induced splenomegaly: mapping of a gene within the major histocompatability complex. J Exp Med. 1974;140(6):1457–67. doi: 10.1084/jem.140.6.1457 4430891

54. Robertson MN, Miyazawa M, Mori S, Caughey B, Evans LH, Hayes SF, et al. Production of monoclonal antibodies reactive with a denatured form of the Friend murine leukemia virus gp70 envelope protein: use in a focal infectivity assay, immunohistochemical studies, electron microscopy and western blotting. JVirolMethods. 1991;34(3):255–71.

55. Hasenkrug KJ, Brooks DM, Robertson MN, Srinivas RV, Chesebro B. Immunoprotective determinants in friend murine leukemia virus envelope protein. Virology. 1998;248(1):66–73. Epub 1998/08/15. doi: 10.1006/viro.1998.9264 9705256.

56. Sitbon M, Nishio J, Wehrly K, Lodmell D, Chesebro B. Use of a focal immunofluorescence assay on live cells for quantitation of retroviruses: distinction of host range classes in virus mixtures and biological cloning of dual-tropic murine leukemia viruses. Virology. 1985;141(1):110–8. doi: 10.1016/0042-6822(85)90187-4 2983493

57. Iwashiro M, Kondo T, Shimizu T, Yamagishi H, Takahashi K, Matsubayashi Y, et al. Multiplicity of virus-encoded helper T-cell epitopes expressed on FBL-3 tumor cells. J Virol. 1993;67(8):4533–42. 7687300

58. Munks MW, Gold MC, Zajac AL, Doom CM, Morello CS, Spector DH, et al. Genome-wide analysis reveals a highly diverse CD8 T cell response to murine cytomegalovirus. J Immunol. 2006;176(6):3760–6. Epub 2006/03/07. doi: 10.4049/jimmunol.176.6.3760 16517745.

59. Cobbold SP, Jayasuriya A, Nash A, Prospero TD, Waldmann H. Therapy with monoclonal antibodies by elimination of T-cell subsets in vivo. Nature. 1984;312(5994):548–51. Epub 1984/12/06. doi: 10.1038/312548a0 6150440.

Štítky
Hygiena a epidemiologie Infekční lékařství Laboratoř

Článek vyšel v časopise

PLOS Pathogens


2019 Číslo 9
Nejčtenější tento týden
Nejčtenější v tomto čísle
Kurzy

Zvyšte si kvalifikaci online z pohodlí domova

plice
INSIGHTS from European Respiratory Congress
nový kurz

Současné pohledy na riziko v parodontologii
Autoři: MUDr. Ladislav Korábek, CSc., MBA

Svět praktické medicíny 3/2024 (znalostní test z časopisu)

Kardiologické projevy hypereozinofilií
Autoři: prof. MUDr. Petr Němec, Ph.D.

Střevní příprava před kolonoskopií
Autoři: MUDr. Klára Kmochová, Ph.D.

Všechny kurzy
Kurzy Podcasty Doporučená témata Časopisy
Přihlášení
Zapomenuté heslo

Zadejte e-mailovou adresu, se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.

Přihlášení

Nemáte účet?  Registrujte se

#ADS_BOTTOM_SCRIPTS#