Interleukin-21 administration to rhesus macaques chronically infected with simian immunodeficiency virus increases cytotoxic effector molecules in T cells and NK cells and enhances B cell function without increasing immune activation or viral replication

Vaccine

Volumn 29, Issue 49, 2011, Pages 9229-9238

  Pallikkuth, Suresh ^a   Rogers, Kenneth ^b   Villinger, Francois ^b   Dosterii, Melvin ^c   Vaccari, Monica ^c   Franchini, Genoveffa ^c   Pahwa, Rajendra ^d   Pahwa, Savita ^a  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^b EMORY UNIVERSITY   (United States)

^c NATIONAL CANCER INSTITUTE   (United States)

^d Max Healthcare   (India)

Author keywords

B cells; Interleukin 21; Natural killer cells; Rhesus macaques; SIV; T cells

Indexed keywords

B LYMPHOCYTE DIFFERENTIATION FACTOR; CD27 ANTIGEN; GAMMA INTERFERON; GRANZYME B; HLA DR ANTIGEN; INTERLEUKIN 2; INTERLEUKIN 21; KI 67 ANTIGEN; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; PERFORIN; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY TITER; ARTICLE; B LYMPHOCYTE; BLOOD; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL ACTIVATION; CELL FUNCTION; CELL PROLIFERATION; CONTROLLED STUDY; CYTOTOXICITY; DRUG ACTIVITY; DRUG DOSE ESCALATION; DRUG SAFETY; IMMUNITY; LYMPH NODE; MEMORY CELL; MESENTERY LYMPH NODE; NATURAL KILLER CELL; NONHUMAN; PILOT STUDY; PRIORITY JOURNAL; RHESUS MONKEY; SIMIAN IMMUNODEFICIENCY VIRUS; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; VIRUS LOAD; VIRUS REPLICATION;

ANIMALS; ANTIBODIES, VIRAL; ANTIGENS, CD27; B-LYMPHOCYTES; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELL PROLIFERATION; GRANZYMES; IMMUNOLOGIC MEMORY; INTERFERON-GAMMA; INTERLEUKINS; KILLER CELLS, NATURAL; LYMPHOCYTE ACTIVATION; LYSOSOMAL-ASSOCIATED MEMBRANE PROTEIN 1; MACACA MULATTA; PERFORIN; PILOT PROJECTS; RNA, VIRAL; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; VIRAL LOAD;

EID: 82555187124     PISSN: 0264410X     EISSN: 18732518     Source Type: Journal    
DOI: 10.1016/j.vaccine.2011.09.118     Document Type: Article

References (68)

1. Parrish-Novak J., Dillon S.R., Nelson A., Hammond A., Sprecher C., Gross J.A., et al. Interleukin 21 and its receptor are involved in NK cell expansion and regulation of lymphocyte function. Nature 2000, 408(November (6808)):57-63.
2. Spolski R., Leonard W.J. Interleukin-21: basic biology and implications for cancer and autoimmunity. Annu Rev Immunol 2008, 26:57-79.
3. Elsaesser H., Sauer K., Brooks D.G. IL-21 is required to control chronic viral infection. Science 2009, 324(June (5934)):1569-1572.
4. Frohlich A., Kisielow J., Schmitz I., Freigang S., Shamshiev A.T., Weber J., et al. IL-21R on T cells is critical for sustained functionality and control of chronic viral infection. Science 2009, 324(June (5934)):1576-1580.
5. Yi J.S., Du M., Zajac A.J. A vital role for interleukin-21 in the control of a chronic viral infection. Science 2009, 324(June (5934)):1572-1576.
6. + T cell function. J Virol 2011, 85(January (2)):733-741.
7. + T cells are induced in acute and chronic progressive HIV infection and are associated with relative viral control. J Immunol 2010, 185(July (1)):498-506.
8. Hersperger A.R., Pereyra F., Nason M., Demers K., Sheth P., Shin L.Y., et al. Perforin expression directly ex vivo by HIV-specific CD8 T-cells is a correlate of HIV elite control. PLoS Pathog 2010, 6(5):e1000917.
9. + T cells is required for HIV-infected cell elimination associated with immune control. Immunity 2008, 29(December (6)):1009-1021.
10. + lymphocytes. Science 1999, 283(February (5403)):857-860.
11. Alter G., Altfeld M. NK cells in HIV-1 infection: evidence for their role in the control of HIV-1 infection. J Intern Med 2009, 265(January (1)):29-42.
12. Tiemessen C.T., Shalekoff S., Meddows-Taylor S., Schramm D.B., Papathanasopoulos M.A., Gray G.E., et al. Natural killer cells that respond to human immunodeficiency virus type 1 (HIV-1) peptides are associated with control of HIV-1 infection. J Infect Dis 2010, 202(November (9)):1444-1453.
13. Jenne D.E., Tschopp J. Granzymes, a family of serine proteases released from granules of cytolytic T lymphocytes upon T cell receptor stimulation. Immunol Rev 1988, 103(March):53-71.
14. Young J.D., Hengartner H., Podack E.R., Cohn Z.A. Purification and characterization of a cytolytic pore-forming protein from granules of cloned lymphocytes with natural killer activity. Cell 1986, 44(March (6)):849-859.
15. Harari A., Enders F.B., Cellerai C., Bart P.A., Pantaleo G. Distinct profiles of cytotoxic granules in memory CD8 T cells correlate with function, differentiation stage, and antigen exposure. J Virol 2009, 83(April (7)):2862-2871.
16. Champagne P., Ogg G.S., King A.S., Knabenhans C., Ellefsen K., Nobile M., et al. Skewed maturation of memory HIV-specific CD8 T lymphocytes. Nature 2001, 410(March (6824)):106-111.
17. + T-cell defects. J Virol 2007, 81(October (20)):10861-10868.
18. White L., Krishnan S., Strbo N., Liu H., Kolber M.A., Lichtenheld M.G., et al. Differential effects of IL-21 and IL-15 on perforin expression, lysosomal degranulation, and proliferation in CD8 T cells of patients with human immunodeficiency virus-1 (HIV). Blood 2007, 109(May (9)):3873-3880.
19. Strbo N., de Armas L., Liu H., Kolber M.A., Lichtenheld M., Pahwa S. IL-21 augments natural killer effector functions in chronically HIV-infected individuals. AIDS 2008, 22(August (13)):1551-1560.
20. Hel Z., Venzon D., Poudyal M., Tsai W.P., Giuliani L., Woodward R., et al. Viremia control following antiretroviral treatment and therapeutic immunization during primary SIV251 infection of macaques. Nat Med 2000, 6(October (10)):1140-1146.
21. + T cells in macaques chronically infected with SIVmac251. J Immunol 2005, 174(February (4)):1913-1921.
22. + t cells and NK Cells in simian immunodeficiency virus-infected macaques. J Virol 2005, 79(April (8)):4877-4885.
23. Villinger F., Miller R., Mori K., Mayne A.E., Bostik P., Sundstrom J.B., et al. IL-15 is superior to IL-2 in the generation of long-lived antigen specific memory CD4 and CD8 T cells in rhesus macaques. Vaccine 2004, 22(September (25-26)):3510-3521.
24. + T cell levels during IL-7 administration of antiretroviral therapy-treated simian immunodeficiency virus-positive macaques are not dependent on strong proliferative responses. J Immunol 2010, 185(August (3)):1650-1659.
25. Picker L.J., Reed-Inderbitzin E.F., Hagen S.I., Edgar J.B., Hansen S.G., Legasse A., et al. IL-15 induces CD4 effector memory T cell production and tissue emigration in nonhuman primates. J Clin Invest 2006, 116(June (6)):1514-1524.
26. Romano J.W., Williams K.G., Shurtliff R.N., Ginocchio C., Kaplan M. NASBA technology: isothermal RNA amplification in qualitative and quantitative diagnostics. Immunol Invest 1997, 26(January-February (1-2)):15-28.
27. Hryniewicz A., Price D.A., Moniuszko M., Boasso A., Edghill-Spano Y., West S.M., et al. Interleukin-15 but not interleukin-7 abrogates vaccine-induced decrease in virus level in simian immunodeficiency virus mac251-infected macaques. J Immunol 2007, 178(March (6)):3492-3504.
28. Maecker H.T., Trotter J. Flow cytometry controls, instrument setup, and the determination of positivity. Cytometry A 2006, 69(September (9)):1037-1042.
29. Perfetto S.P., Ambrozak D., Nguyen R., Chattopadhyay P., Roederer M. Quality assurance for polychromatic flow cytometry. Nat Protoc 2006, 1(3):1522-1530.
30. + T-cell responses in vervet African green monkeys chronically infected with SIVagm. J Virol 2008, 82(December (23)):11577-11588.
31. Zuber B., Quigley M.F., Critchfield J.W., Shacklett B.L., Abel K., Miller C.J., et al. Detection of macaque perforin expression and release by flow cytometry, immunohistochemistry, ELISA, and ELISpot. J Immunol Methods 2006, 312(May (1-2)):45-53.
32. Kuhrt D., Faith S.A., Leone A., Rohankedkar M., Sodora D.L., Picker L.J., et al. Evidence of early B-cell dysregulation in simian immunodeficiency virus infection: rapid depletion of naive and memory B-cell subsets with delayed reconstitution of the naive B-cell population. J Virol 2010, 84(March (5)):2466-2476.
33. Robinson J.E., Holton D., Liu J., McMurdo H., Murciano A., Gohd R. A novel enzyme-linked immunosorbent assay (ELISA) for the detection of antibodies to HIV-1 envelope glycoproteins based on immobilization of viral glycoproteins in microtiter wells coated with concanavalin A. J Immunol Methods 1990, 132(August (1)):63-71.
34. Ettinger R., Sims G.P., Fairhurst A.M., Robbins R., da Silva Y.S., Spolski R., et al. IL-21 induces differentiation of human naive and memory B cells into antibody-secreting plasma cells. J Immunol 2005, 175(December (12)):7867-7879.
35. Beq S., Nugeyre M.T., Ho Tsong Fang R., Gautier D., Legrand R., Schmitt N., et al. IL-7 induces immunological improvement in SIV-infected rhesus macaques under antiviral therapy. J Immunol 2006, 176(January (2)):914-922.
36. + T lymphocytes in naive and simian immunodeficiency virus-infected rhesus monkeys. AIDS Res Hum Retroviruses 2001, 17(July (10)):873-886.
37. Fry T.J., Moniuszko M., Creekmore S., Donohue S.J., Douek D.C., Giardina S., et al. IL-7 therapy dramatically alters peripheral T-cell homeostasis in normal and SIV-infected nonhuman primates. Blood 2003, 101(March (6)):2294-2299.
38. Levy Y., Lacabaratz C., Weiss L., Viard J.P., Goujard C., Lelievre J.D., et al. Enhanced T cell recovery in HIV-1-infected adults through IL-7 treatment. J Clin Invest 2009, 119(April (4)):997-1007.
39. + T cells that express the interleukin-7 receptor in blood and tissues of SIV-infected macaques. Virology 2006, 356(December (1-2)):188-197.
40. Sereti I., Dunham R.M., Spritzler J., Aga E., Proschan M.A., Medvik K., et al. IL-7 administration drives T cell-cycle entry and expansion in HIV-1 infection. Blood 2009, 113(June (25)):6304-6314.
41. Williams L.D., Bansal A., Sabbaj S., Heath S.L., Song W., Tang J., et al. Interleukin-21-Producing HIV-1-Specific CD8 T Cells Are Preferentially Seen in Elite Controllers. J Virol 2011, 85(March (5)):2316-2324.
42. + T lymphocyte granules in lymphoid tissue during acute human immunodeficiency virus type 1 infection. J Infect Dis 2002, 185(May (9)):1355-1358.
43. Jansen C.A., Piriou E., Bronke C., Vingerhoed J., Kostense S., van Baarle D., et al. Characterization of virus-specific CD8(+) effector T cells in the course of HIV-1 infection: longitudinal analyses in slow and rapid progressors. Clin Immunol 2004, 113(December (3)):299-309.
44. + T cells in GALT: implications for immune control of HIV-1 infection. J Immunol 2004, 173(July (1)):641-648.
45. Parmigiani A., Pallin M.F., Schmidtmayerova H., Lichtenheld M.G., Pahwa S. Interleukin-21 and cellular activation concurrently induce potent cytotoxic function and promote antiviral activity in human CD8 T cells. Hum Immunol 2011, 72(October):115-123.
46. Iannello A., Boulassel M.R., Samarani S., Debbeche O., Tremblay C., Toma E., et al. Dynamics and consequences of IL-21 production in HIV-infected individuals: a longitudinal and cross-sectional study. J Immunol 2010, 184(January (1)):114-126.
47. Iannello A., Boulassel M.R., Samarani S., Tremblay C., Toma E., Routy J.P., et al. IL-21 enhances NK cell functions and survival in healthy and HIV-infected patients with minimal stimulation of viral replication. J Leukoc Biol 2010, 87(May (5)):857-867.
48. Goulder P.J., Watkins D.I. HIV and SIV CTL escape: implications for vaccine design. Nat Rev Immunol 2004, 4(August (8)):630-640.
49. + T cells from the dynamics of viral immune escape. J Virol 2007, 81(November (21)):11982-11991.
50. Villinger F., Bucur S., Chikkala N.F., Brar S.S., Bostik P., Mayne A.E., et al. In vitro and in vivo responses to interleukin 12 are maintained until the late SIV infection stage but lost during AIDS. AIDS Res Hum Retroviruses 2000, 16(May (8)):751-763.
51. Ansari A.A., Mayne A.E., Sundstrom J.B., Bostik P., Grimm B., Altman J.D., et al. Administration of recombinant rhesus interleukin-12 during acute simian immunodeficiency virus (SIV) infection leads to decreased viral loads associated with prolonged survival in SIVmac251-infected rhesus macaques. J Virol 2002, 76(February (4)):1731-1743.
52. + T cell count in HIV-seropositive individuals with undetectable plasma HIV RNA levels in the absence of therapy. J Infect Dis 2008, 197(January (1)):126-133.
53. Madec Y., Boufassa F., Porter K., Meyer L. Spontaneous control of viral load and CD4 cell count progression among HIV-1 seroconverters. AIDS 2005, 19(November (17)):2001-2007.
54. Avery D.T., Bryant V.L., Ma C.S., de Waal Malefyt R., Tangye S.G. IL-21-induced isotype switching to IgG and IgA by human naive B cells is differentially regulated by IL-4. J Immunol 2008, 181(August (3)):1767-1779.
55. Ozaki K., Spolski R., Ettinger R., Kim H.P., Wang G., Qi C.F., et al. Regulation of B cell differentiation and plasma cell generation by IL-21, a novel inducer of Blimp-1 and Bcl-6. J Immunol 2004, 173(November (9)):5361-5371.
56. Pene J., Gauchat J.F., Lecart S., Drouet E., Guglielmi P., Boulay V., et al. Cutting edge: IL-21 is a switch factor for the production of IgG1 and IgG3 by human B cells. J Immunol 2004, 172(May (9)):5154-5157.
57. Avery D.T., Deenick E.K., Ma C.S., Suryani S., Simpson N., Chew G.Y., et al. B cell-intrinsic signaling through IL-21 receptor and STAT3 is required for establishing long-lived antibody responses in humans. J Exp Med 2010, 207(January (1)):155-171.
58. Ettinger R., Sims G.P., Robbins R., Withers D., Fischer R.T., Grammer A.C., et al. IL-21 and BAFF/BLyS synergize in stimulating plasma cell differentiation from a unique population of human splenic memory B cells. J Immunol 2007, 178(March (5)):2872-2882.
59. Borte S., Pan-Hammarstrom Q., Liu C., Sack U., Borte M., Wagner U., et al. Interleukin-21 restores immunoglobulin production ex vivo in patients with common variable immunodeficiency and selective IgA deficiency. Blood 2009, 114(November (19)):4089-4098.
60. Konforte D., Simard N., Paige C.J. IL-21: an executor of B cell fate. J Immunol 2009, 182(February (4)):1781-1787.
61. Moir S., Fauci A.S. B cells in HIV infection and disease. Nat Rev Immunol 2009, 9(April (4)):235-245.
62. Moir S., Ho J., Malaspina A., Wang W., DiPoto A.C., O'Shea M.A., et al. Evidence for HIV-associated B cell exhaustion in a dysfunctional memory B cell compartment in HIV-infected viremic individuals. J Exp Med 2008, 205(August (8)):1797-1805.
63. Bolesta E., Kowalczyk A., Wierzbicki A., Eppolito C., Kaneko Y., Takiguchi M., et al. Increased level and longevity of protective immune responses induced by DNA vaccine expressing the HIV-1 Env glycoprotein when combined with IL-21 and IL-15 gene delivery. J Immunol 2006, 177(July (1)):177-191.
64. Cui F.D., Asada H., Jin M.L., Kishida T., Shin-Ya M., Nakaya T., et al. Cytokine genetic adjuvant facilitates prophylactic intravascular DNA vaccine against acute and latent herpes simplex virus infection in mice. Gene Ther 2005, 12(January (2)):160-168.
65. Dou J., Tang Q., Zhao F., Chu L., Chen J., Cao M., et al. Comparison of immune responses induced in mice by vaccination with DNA vaccine constructs expressing mycobacterial antigen 85A and interleukin-21 and Bacillus Galmette-Guerin. Immunol Invest 2008, 37(2):113-127.
66. Davis I.D., Brady B., Kefford R.F., Millward M., Cebon J., Skrumsager B.K., et al. Clinical and biological efficacy of recombinant human interleukin-21 in patients with stage IV malignant melanoma without prior treatment: a phase IIa trial. Clin Cancer Res 2009, 15(March (6)):2123-2129.
67. Frederiksen K.S., Lundsgaard D., Freeman J.A., Hughes S.D., Holm T.L., Skrumsager B.K., et al. IL-21 induces in vivo immune activation of NK cells and CD8(+) T cells in patients with metastatic melanoma and renal cell carcinoma. Cancer Immunol Immunother 2008, 57(October (10)):1439-1449.
68. Thompson J.A., Curti B.D., Redman B.G., Bhatia S., Weber J.S., Agarwala S.S., et al. Phase I study of recombinant interleukin-21 in patients with metastatic melanoma and renal cell carcinoma. J Clin Oncol 2008, 26(April (12)):2034-2039.