876
Views
3
CrossRef citations to date
0
Altmetric
Original Research

Activation of the FcgammaReceptorIIIa on human natural killer cells leads to increased expression of functional interleukin-21 receptor

, , , , , , , , , , , , & , MD show all
Article: e1312045 | Received 21 Feb 2017, Accepted 23 Mar 2017, Published online: 08 May 2017

References

  • Carson WE, Giri JG, Lindemann MJ, Linett ML, Ahdieh M, Paxton R, Anderson D, Eisenmann J, Grabstein K, Caligiuri MA. Interleukin (IL) 15 is a novel cytokine that activates human natural killer cells via components of the IL-2 receptor. J Exp Med 1994; 180(4):1395-403; PMID:7523571; https://doi.org/10.1084/jem.180.4.1395
  • Carson WE, Lindemann MJ, Baiocchi R, Linett M, Tan JC, Chou CC, Narula S, Caligiuri MA. The functional characterization of interleukin-10 receptor expression on human natural killer cells. Blood 1995; 85(12):3577-85; PMID:7540068.
  • Fehniger TA, Shah MH, Turner MJ, VanDeusen JB, Whitman SP, Cooper MA, Suzuki K, Wechser M, Goodsaid F, Caligiuri MA. Differential cytokine and chemokine gene expression by human NK cells following activation with IL-18 or IL-15 in combination with IL-12: implications for the innate immune response. J Immunol 1999; 162(8):4511-20; PMID:10201989
  • Bluman EM, Bartynski KJ, Avalos BR, Caligiuri MA. Human natural killer cells produce abundant macrophage inflammatory protein-1 alpha in response to monocyte-derived cytokines. J Clin Invest 1996; 97(12):2722-7; PMID:8675682; https://doi.org/10.1172/JCI118726
  • Somersalo K, Carpén O, Saksela E. Stimulated natural killer cells secrete factors with chemotactic activity, including NAP-1/IL-8, which supports VLA-4- and VLA-5-mediated migration of T lymphocytes. Eur J Immunol 1994; 24(12):2957-65; PMID:7805722; https://doi.org/10.1002/eji.1830241206
  • Ozaki K, Spolski R, Ettinger R, Kim HP, Wang G, Qi CF, Hwu P, Shaffer DJ, Akilesh S, Roopenian DC 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(9):5361-71; PMID:15494482; https://doi.org/10.4049/jimmunol.173.9.5361
  • Ettinger R, Sims GP, Fairhurst AM, Robbins R, da Silva YS, Spolski R, Leonard WJ, Lipsky PE. IL-21 induces differentiation of human naive and memory B cells into antibody-secreting plasma cells. J Immunol 2005; 175(12):7867-79; PMID:16339522; https://doi.org/10.4049/jimmunol.175.12.7867
  • Ozaki K, Spolski R, Feng CG, Qi CF, Cheng J, Sher A, Morse HC 3rd, Liu C, Schwartzberg PL, Leonard WJ. A critical role for IL-21 in regulating immunoglobulin production. Science 2002; 298(5598):1630-4; PMID:12446913; https://doi.org/10.1126/science.1077002
  • Suto A, Nakajima H, Hirose K, Suzuki K, Kagami S, Seto Y, Hoshimoto A, Saito Y, Foster DC, Iwamoto I. Interleukin 21 prevents antigen-induced IgE production by inhibiting germ line Cϵ transcription of IL-4-stimulated B cells. Blood 2002; 100(13):4565-73; PMID:12393685; https://doi.org/10.1182/blood-2002-04-1115
  • Davis ID, Skrumsager BK, Cebon J, Nicholaou T, Barlow JW, Moller NP, Skak K, Lundsgaard D, Frederiksen KS, Thygesen P et al. An open-label, two-arm, phase I trial of recombinant human interleukin-21 in patients with metastatic melanoma. Clin Cancer Res 2007; 13(12):3630-6; PMID:17575227; https://doi.org/10.1158/1078-0432.CCR-07-0410
  • Elsaesser H, Sauer K, Brooks DG. IL-21 is required to control chronic viral infection. Science 2009; 324(5934):1569-72; PMID:19423777; https://doi.org/10.1126/science.1174182
  • Habib T, Senadheera S, Weinberg K, Kaushansky K. The common γ chain (γc) is a required signaling component of the IL-21 receptor and supports IL-21-induced cell proliferation via JAK3. Biochemistry 2002; 41(27):8725-31; PMID:12093291; https://doi.org/10.1021/bi0202023
  • Parrish-Novak J, Dillon SR, Nelson A, Hammond A, Sprecher C, Gross JA, Johnston J, Madden K, Xu W, West J. Interleukin 21 and its receptor are involved in NK cell expansion and regulation of lymphocyte function. Nature 2000; 408(6808):57-63; PMID:11081504; https://doi.org/10.1038/35040504
  • Zeng R, Spolski R, Casas E, Zhu W, Levy DE, Leonard WJ. The molecular basis of IL-21-mediated proliferation. Blood 2007; 109(10):4135-42; PMID:17234735; https://doi.org/10.1182/blood-2006-10-054973
  • Hinrichs CS, Spolski R, Paulos CM, Gattinoni L, Kerstann KW, Palmer DC, Klebanoff CA, Rosenberg SA, Leonard WJ, Restifo NP. IL-2 and IL-21 confer opposing differentiation programs to CD8+ T cells for adoptive immunotherapy. Blood 2008; 111(11):5326-33; PMID:18276844; https://doi.org/10.1182/blood-2007-09-113050
  • di Carlo E, de Totero D, Piazza T, Fabbi M, Ferrini S. Role of IL-21 in immune-regulation and tumor immunotherapy. Cancer Immunol Immunother 2007; 56(9):1323-34; PMID:17447063; https://doi.org/10.1007/s00262-007-0326-z
  • Davis ID, Skak K, Smyth MJ, Kristjansen PE, Miller DM, Sivakumar PV. Interleukin-21 signaling: functions in cancer and autoimmunity. Clin Cancer Res 2007; 13(23):6926-32; PMID:18056166; https://doi.org/10.1158/1078-0432.CCR-07-1238
  • Spolski R, Leonard WJ. Interleukin-21: basic biology and implications for cancer and autoimmunity. Annu Rev Immunol 2008; 26:57-79; PMID:17953510; https://doi.org/10.1146/annurev.immunol.26.021607.090316
  • Brady J, Hayakawa Y, Smyth MJ, Nutt SL. IL-21 induces the functional maturation of murine NK cells. J Immunol 2004; 172(4):2048-58; PMID:14764669; https://doi.org/10.4049/jimmunol.172.4.2048
  • Burgess SJ, Marusina AI, Pathmanathan I, Borrego F, Coligan JE. IL-21 down-regulates NKG2D/DAP10 expression on human NK and CD8+ T cells. J Immunol 2006; 176(3):1490-7; PMID:16424177; https://doi.org/10.4049/jimmunol.176.3.1490
  • Wang G, Tschoi M, Spolski R, Lou Y, Ozaki K, Feng C, Kim G, Leonard WJ, Hwu P. In vivo antitumor activity of interleukin 21 mediated by natural killer cells. Cancer Res 2003; 63(24):9016-22; PMID:14695220
  • Ma HL, Whitters MJ, Konz RF, Senices M, Young DA, Grusby MJ, Collins M, Dunussi-Joannopoulos K. IL-21 activates both innate and adaptive immunity to generate potent antitumor responses that require perforin but are independent of IFN-gamma. J Immunol 2003; 171(2):608-15; PMID:12847225; https://doi.org/10.4049/jimmunol.171.2.608
  • Di Carlo E, Comes A, Orengo AM, Rosso O, Meazza R, Musiani P, Colombo MP, Ferrini S. IL-21 induces tumor rejection by specific CTL and IFN-gamma-dependent CXC chemokines in syngeneic mice. J Immunol 2004; 172(3):1540-7; PMID:14734732; https://doi.org/10.4049/jimmunol.172.3.1540
  • Smyth MJ, Wallace ME, Nutt SL, Yagita H, Godfrey DI, Hayakawa Y. Sequential activation of NKT cells and NK cells provides effective innate immunotherapy of cancer. J Exp Med 2005; 201(12):1973-85; PMID:15967825; https://doi.org/10.1084/jem.20042280
  • Takaki R, Hayakawa Y, Nelson A, Sivakumar PV, Hughes S, Smyth MJ, Lanier LL. IL-21 enhances tumor rejection through a NKG2D-dependent mechanism. J Immunol 2005; 175(4):2167-73; PMID:16081783; https://doi.org/10.4049/jimmunol.175.4.2167
  • Comes A, Rosso O, Orengo AM, Di Carlo E, Sorrentino C, Meazza R, Piazza T, Valzasina B, Nanni P, Colombo MP et al. CD25+ regulatory T cell depletion augments immunotherapy of micrometastases by an IL-21-secreting cellular vaccine. J Immunol 2006; 176(3):1750-8; PMID:16424205; https://doi.org/10.4049/jimmunol.176.3.1750
  • McMichael EL, Jaime-Ramirez AC, Guenterberg KD, Luedke E, Atwal LS, Campbell AR, Hu Z, Tatum AS, Kondadasula SV, Mo X et al. IL-21 enhances natural killer cell response to cetuximab-coated pancreatic tumor cells. Clin Cancer Res 2017; 23(2):489-502; PMID:27435400; https://doi.org/10.1158/1078-0432.CCR-16-0004
  • Kondadasula SV, Roda JM, Parihar R, Yu J, Lehman A, Caligiuri MA, Tridandapani S, Burry RW, Carson WE 3rd. Colocalization of the IL-12 receptor and FcgammaRIIIa to natural killer cell lipid rafts leads to activation of ERK and enhanced production of interferon-gamma. Blood 2008; 111(8):4173-83; PMID:18174382; https://doi.org/10.1182/blood-2007-01-068908
  • Parihar R, Dierksheide J, Hu Y, Carson WE. IL-12 enhances the natural killer cell cytokine response to Ab-coated tumor cells. J Clin Invest 2002; 110(7):983-92; PMID:12370276; https://doi.org/10.1172/JCI0215950
  • Campbell AR, Regan K, Bhave N, Pattanayak A, Parihar R, Stiff AR, Trikha P, Scoville SD, Liyanarachchi S, Kondadasula SV et al. Gene expression profiling of the human natural killer cell response to Fc receptor activation: unique enhancement in the presence of interleukin-12. BMC Med Genom 2015; 8:66; PMID:26470881; https://doi.org/10.1186/s12920-015-0142-9
  • Lesinski GB, Badgwell B, Zimmerer J, Crespin T, Hu Y, Abood G, Carson WE 3rd. IL-12 pretreatments enhance IFN-alpha-induced Janus kinase-STAT signaling and potentiate the antitumor effects of IFN-alpha in a murine model of malignant melanoma. J Immunol 2004; 172(12):7368-76; PMID:15187113; https://doi.org/10.4049/jimmunol.172.12.7368
  • Lesinski GB, Kondadasula SV, Crespin T, Shen L, Kendra K, Walker M, Carson WE 3rd. Multiparametric flow cytometric analysis of inter-patient variation in STAT1 phosphorylation following interferon Alfa immunotherapy. J Natl Cancer Inst 2004; 96(17):1331-42; PMID:15339971; https://doi.org/10.1093/jnci/djh252
  • Carson WE, Parihar R, Lindemann MJ, Personeni N, Dierksheide J, Meropol NJ, Baselga J, Caligiuri MA. Interleukin-2 enhances the natural killer cell response to herceptin-coated Her2/neu-positive breast cancer cells. Eur J Immunol 2001; 31(10):3016-25; PMID:11592078; https://doi.org/10.1002/1521-4141(2001010)31:10%3c3016::AID-IMMU3016%3e3.0.CO;2-J
  • Roda JM, Parihar R, Lehman A, Mani A, Tridandapani S, Carson WE 3rd. Interleukin-21 enhances NK cell activation in response to antibody-coated targets. J Immunol 2006; 177(1):120-9; PMID:16785506; https://doi.org/10.4049/jimmunol.177.1.120
  • Vermes I, Haanen C, Steffens-Nakken H, Reutelingsperger C. A novel assay for apoptosis. Flow cytometric detection of phosphatidylserine expression on early apoptotic cells using fluorescein labelled Annexin V. J Immunol Methods 1995; 184(1):39-51; PMID:7622868; https://doi.org/10.1016/0022-1759(95)00072-I
  • Raulet DH. Interplay of natural killer cells and their receptors with the adaptive immune response. Nat Immunol 2004; 5(10):996-1002; PMID:15454923; https://doi.org/10.1038/ni1114
  • Carson WE, Dierksheide JE, Jabbour S, Anghelina M, Bouchard P, Ku G, Yu H, Baumann H, Shah MH, Cooper MA et al. Coadministration of interleukin-18 and interleukin-12 induces a fatal inflammatory response in mice: critical role of natural killer cell interferon-gamma production and STAT-mediated signal transduction. Blood 2000; 96(4):1465-73; PMID:10942393
  • Jaime-Ramirez AC, Mundy-Bosse BL, Kondadasula S, Jones NB, Roda JM, Mani A, Parihar R, Karpa V, Papenfuss TL, LaPerle KM et al. IL-12 enhances the antitumor actions of trastuzumab via NK cell IFN-γ production. J Immunol 2011; 186(6):3401-9; PMID:21321106; https://doi.org/10.4049/jimmunol.1000328
  • Deaglio S, Zubiaur M, Gregorini A, Bottarel F, Ausiello CM, Dianzani U, Sancho J, Malavasi F. Human CD38 and CD16 are functionally dependent and physically associated in natural killer cells. Blood 2002; 99(7):2490-8; PMID:11895784; https://doi.org/10.1182/blood.V99.7.2490
  • Spolski R, Leonard WJ. Interleukin-21: a double-edged sword with therapeutic potential. Nat Rev Drug Discov 2014; 13(5):379-95; PMID:24751819; https://doi.org/10.1038/nrd4296
  • Kasaian MT, Whitters MJ, Carter LL, Lowe LD, Jussif JM, Deng B, Johnson KA, Witek JS, Senices M, Konz RF et al. IL-21 limits NK cell responses and promotes antigen-specific T cell activation: a mediator of the transition from innate to adaptive immunity. Immunity 2002; 16(4):559-69; PMID:11970879; https://doi.org/10.1016/S1074-7613(02)00295-9
  • Søndergaard H, Galsgaard ED, Bartholomaeussen M, Straten PT, Odum N, Skak K. Intratumoral interleukin-21 increases antitumor immunity, tumor-infiltrating CD8+ T-cell density and activity, and enlarges draining lymph nodes. J Immunother 2010; 33(3):236-49; PMID:20445344; https://doi.org/10.1097/CJI.0b013e3181c0c1cb
  • Sivakumar PV, Garcia R, Waggie KS, Anderson-Haley M, Nelson A, Hughes SD. Comparison of vascular leak syndrome in mice treated with IL21 or IL2. Comp Med 2013; 63(1):13-21; PMID:23561933
  • Skak K, Frederiksen KS, Lundsgaard D. Interleukin-21 activates human natural killer cells and modulates their surface receptor expression. Immunology 2008; 123(4):575-83; PMID:18005035; https://doi.org/10.1111/j.1365-2567.2007.02730.x
  • Krejsa CM, Holly RD, Heipel M, Bannink KM, Johnson R, Roque R, Heffernan J, Hill J, Chin L, Wagener F et al. Interleukin-21 enhances rituximab activity in a cynomolgus monkey model of B cell depletion and in mouse B cell lymphoma models. PLoS One 2013; 8(6):e67256; PMID:23825648; https://doi.org/10.1371/journal.pone.0067256
  • Taylor RP, Lindorfer MA. Immunotherapeutic mechanisms of anti-CD20 monoclonal antibodies. Curr Opin Immunol 2008; 20(4):444-9; PMID:18585457; https://doi.org/10.1016/j.coi.2008.05.011
  • Seidel UJ, Schlegel P, Lang P. Natural killer cell mediated antibody-dependent cellular cytotoxicity in tumor immunotherapy with therapeutic antibodies. Front Immunol 2013; 4:76; PMID:23543707; https://doi.org/10.3389/fimmu.2013.00076
  • Vivier E, Raulet DH, Moretta A, Caligiuri MA, Zitvogel L, Lanier LL, Yokoyama WM, Ugolini S. Innate or adaptive immunity? The example of natural killer cells. Science 2011; 331(6013):44-9; PMID:21212348; https://doi.org/10.1126/science.1198687
  • Banks ND, Kinsey N, Clements J, Hildreth JE. Sustained antibody-dependent cell-mediated cytotoxicity (ADCC) in SIV-infected macaques correlates with delayed progression to AIDS. AIDS Res Hum Retrovir 2002; 18(16):1197-205; PMID:12487826; https://doi.org/10.1089/08892220260387940
  • Nimmerjahn F, Ravetch JV. FcγRs in health and disease. Curr Top Microbiol Immunol 2011; 350:105-25; PMID:20680807
  • Leong JW, Chase JM, Romee R, Schneider SE, Sullivan RP, Cooper MA, Fehniger TA. Preactivation with IL-12, IL-15, and IL-18 induces CD25 and a functional high-affinity IL-2 receptor on human cytokine-induced memory-like natural killer cells. Biol Blood Marrow Transpl 2014; 20(4):463-73; PMID:24434782; https://doi.org/10.1016/j.bbmt.2014.01.006

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.