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Immunotherapeutics – Research Paper

Human placental hematopoietic stem cell derived natural killer cells (CYNK-001) mediate protection against influenza a viral infection

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Article: 2055945 | Received 27 Dec 2021, Accepted 17 Mar 2022, Published online: 11 Apr 2022

References

  • Ferkol T, Schraufnagel D. The global burden of respiratory disease. Ann Am Thorac Soc. 2014;11(3):404–9. doi:10.1513/AnnalsATS.201311-405PS.
  • Peteranderl C, Herold S, Schmoldt C. Human influenza virus infections. Semin Respir Crit Care Med. 2016;37(04):487–500. doi:10.1055/s-0036-1584801.
  • Doyle JD, Chung JR, Kim SS, Gaglani M, Raiyani C, Zimmerman RK, Nowalk MP, Jackson ML, Jackson LA, Monto AS, et al. Interim estimates of 2018–19 seasonal influenza vaccine effectiveness — United States, February 2019. MMWR Morb Mortal Wkly Rep. 2019;68(6):135–39. doi:10.15585/mmwr.mm6806a2.
  • Lanier LL. Evolutionary struggles between NK cells and viruses. Nat Rev Immunol. 2008;8(4):259–68. doi:10.1038/nri2276.
  • Marofi F, Al-Awad AS, Sulaiman Rahman H, Markov A, Abdelbasset WK, Ivanovna Enina Y, Mahmoodi M, Hassanzadeh A, Yazdanifar M, Stanley Chartrand M, et al. CAR-NK cell: a new paradigm in tumor immunotherapy. Front Oncol. 2021;11:673276. doi:10.3389/fonc.2021.673276.
  • Arnon TI, Lev M, Katz G, Chernobrov Y, Porgador A, Mandelboim O. Recognition of viral hemagglutinins by NKp44 but not by NKp30. Eur J Immunol. 2001;31(9):2680–89. doi:10.1002/1521-4141(200109)31:9<2680:AID-IMMU2680>3.0.CO;2-A.
  • Luczo JM, Ronzulli SL, Tompkins SM. Influenza a virus hemagglutinin and other pathogen glycoprotein interactions with NK cell natural cytotoxicity receptors NKp46, NKp44, and NKp30. Viruses. 2021;13(2):156. doi:10.3390/v13020156.
  • Vivier E, Tomasello E, Baratin M, Walzer T, Ugolini S. Functions of natural killer cells. Nat Immunol. 2008;9(5):503–10. doi:10.1038/ni1582.
  • Ivanova D, Krempels R, Ryfe J, Weitzman K, Stephenson D, Gigley JP. NK cells in mucosal defense against infection. Biomed Res Int. 2014;2014:413982. doi:10.1155/2014/413982.
  • Littwitz E, Francois S, Dittmer U, Gibbert K. Distinct roles of NK cells in viral immunity during different phases of acute Friend retrovirus infection. Retrovirology. 2013;10:127. doi:10.1186/1742-4690-10-127.
  • Gazit R, Gruda R, Elboim M, Arnon TI, Katz G, Achdout H, Hanna J, Qimron U, Landau G, Greenbaum E, et al. Lethal influenza infection in the absence of the natural killer cell receptor gene Ncr1. Nat Immunol. 2006;7(5):517–23. doi:10.1038/ni1322.
  • Nogusa S, Ritz BW, Kassim SH, Jennings SR, Gardner EM. Characterization of age-related changes in natural killer cells during primary influenza infection in mice. Mech Ageing Dev. 2008;129(4):223–30. doi:10.1016/j.mad.2008.01.003.
  • Stein-Streilein J, Guffee J. In vivo treatment of mice and hamsters with antibodies to asialo GM1 increases morbidity and mortality to pulmonary influenza infection. J Immunol. 1986;136:1435–41. [accessed 2021 July 15].
  • Kumar P, Thakar MS, Ouyang W, Malarkannan S. IL-22 from conventional NK cells is epithelial regenerative and inflammation protective during influenza infection. Mucosal Immunol. 2013;6(1):69–82. doi:10.1038/mi.2012.49.
  • Zhou K, Wang J, Li A, Zhao W, Wang D, Zhang W, Yan J, Gao GF, Liu W, Fang M, et al. Swift and strong NK cell responses protect 129 mice against high-dose Iinfluenza virus infection. J Immunol. 2016;196(4):1842–54. doi:10.4049/jimmunol.1501486.
  • Abdul-Careem MF, Mian MF, Yue G, Gillgrass A, Chenoweth MJ, Barra NG, Chew MV, Chan T, Al-Garawi AA, Jordana M, et al. Critical role of natural killer cells in lung immunopathology during influenza infection in mice. J Infect Dis. 2012;206(2):167–77. doi:10.1093/infdis/jis340.
  • Zhou G, Juang SW, Kane KP. NK cells exacerbate the pathology of influenza virus infection in mice. Eur J Immunol. 2013;43(4):929–38. doi:10.1002/eji.201242620.
  • Jost S, Quillay H, Reardon J, Peterson E, Simmons RP, Parry BA, Bryant NNP, Binder WD, Altfeld M, et al. Changes in cytokine levels and NK cell activation associated with influenza. PLoS One. 2011;6(9):e25060. doi:10.1371/journal.pone.0025060.
  • Denney L, Aitken C, Li CK, Wilson-Davies E, Kok WL, Clelland C, Rooney K, Young D, Dong T, McMichael AJ, et al. Reduction of natural killer but not effector CD8 T lymphocytes in three consecutive cases of severe/lethal H1N1/09 influenza a virus infection. PLoS One. 2010;5(5):e10675. doi:10.1371/journal.pone.0010675.
  • Fox A, Le NM, Horby P, van Doorn HR, Nguyen VT, Nguyen HH, Cap NT, Phu VD, Ha NM, Ngoc DNT, et al. Severe pandemic H1N1 2009 infection is associated with transient NK and T deficiency and aberrant CD8 responses. PLoS One. 2012;7(2):e31535. doi:10.1371/journal.pone.0031535.
  • Spanholtz J, Tordoir M, Eissens D, Preijers F, van der Meer A, Joosten I, Schaap N, de Witte TM, Dolstra H, et al. High log-scale expansion of functional human natural killer cells from umbilical cord blood CD34-positive cells for adoptive cancer immunotherapy. PLoS One. 2010;5(2):e9221. doi:10.1371/journal.pone.0009221.
  • Szretter KJ, Balish AL, Katz JM. Influenza: propagation, quantification, and storage. Curr Protoc Microbiol. 2006;3(1). Chapter 15:Unit 15G 1. doi:10.1002/0471729256.mc15g01s3.
  • Yu YR, O’-Koren EG, Hotten DF, Kan MJ, Kopin D, Nelson ER, Que L, Gunn MD. A protocol for the comprehensive flow cytometric analysis of immune cells in normal and inflamed murine non-lymphoid tissues. PLoS One. 2016;11(3):e0150606. doi:10.1371/journal.pone.0150606.
  • Kang L, Voskinarian-Berse V, Law E, Reddin T, Bhatia M, Hariri A, Ning Y, Dong D, Maguire T, Yarmush M, et al. Characterization and ex vivo expansion of human placenta-derived natural killer cells for cancer immunotherapy. Front Immunol. 2013;4:101. doi:10.3389/fimmu.2013.00101.
  • Gao R, Bhatnagar J, Blau DM, Greer P, Rollin DC, Denison AM, Deleon-Carnes M, Shieh W-J, Sambhara S, Tumpey TM, et al. Cytokine and chemokine profiles in lung tissues from fatal cases of 2009 pandemic influenza a (H1N1): role of the host immune response in pathogenesis. Am J Pathol. 2013;183(4):1258–68. doi:10.1016/j.ajpath.2013.06.023.
  • Koutsakos M, Kedzierska K, Subbarao K. Immune responses to Avian influenza viruses. J Immunol. 2019;202(2):382–91. doi:10.4049/jimmunol.1801070.
  • Wang Z, Loh L, Kedzierski L, Kedzierska K. Avian influenza viruses, inflammation, and CD8(+) T cell immunity. Front Immunol. 2016;7:60. doi:10.3389/fimmu.2016.00060.
  • Liu Y, Du X, Chen J, Jin Y, Peng L, Wang HHX, Luo M, Chen L, Zhao Y. Neutrophil-To-Lymphocyte ratio as an independent risk factor for mortality in hospitalized patients with COVID-19. J Infect. 2020;81(1):e6–e12. doi:10.1016/j.jinf.2020.04.002.
  • Lagunas-Rangel FA. Neutrophil-To-Lymphocyte ratio and lymphocyte-to-C-reactive protein ratio in patients with severe coronavirus disease 2019 (COVID-19): a meta-analysis. J Med Virol. 2020;92(10):1733–34. doi:10.1002/jmv.25819.
  • Carissimo G, Xu W, Kwok I, Abdad MY, Chan YH, Fong SW, Puan KJ, Lee CYP, Yeo NKW, Amrun SN, et al. Whole blood immunophenotyping uncovers immature neutrophil-to-VD2 T-cell ratio as an early marker for severe COVID-19. Nat Commun. 2020;11(1):5243. doi:10.1038/s41467-020-19080-6.
  • Mandelboim O, Lieberman N, Lev M, Paul L, Arnon TI, Bushkin Y, Davis DM, Strominger JL, Yewdell JW, Porgador A, et al. Recognition of haemagglutinins on virus-infected cells by NKp46 activates lysis by human NK cells. Nature. 2001;409(6823):1055–60. doi:10.1038/35059110.
  • Waggoner SN, Cornberg M, Selin LK, Welsh RM. Natural killer cells act as rheostats modulating antiviral T cells. Nature. 2011;481(7381):394–98. doi:10.1038/nature10624.
  • Kronstad LM, Seiler C, Vergara R, Holmes SP, Blish CA. Differential induction of IFN-α and modulation of CD112 and CD54 expression hovern the magnitude of NK cell IFN-γ response to Influenza A viruses. J Immunol. 2018;201(7):2117–31. doi:10.4049/jimmunol.1800161.
  • Juarez-Reyes A, Noyola DE, Monsivais-Urenda A, Alvarez-Quiroga C, Gonzalez-Amaro R. Influenza virus infection but not H1N1 influenza virus immunization is associated with changes in peripheral blood NK cell subset levels. Clin Vaccine Immunol. 2013;20(8):1291–97. doi:10.1128/CVI.00194-13.
  • Cooper GE, Ostridge K, Khakoo SI, Wilkinson TMA, Staples KJ. Human CD49a(+) lung natural killer cell cytotoxicity in response to Influenza A virus. Front Immunol. 2018;9:1671. doi:10.3389/fimmu.2018.01671.
  • Arnon TI, Achdout H, Lieberman N, Gazit R, Gonen-Gross T, Katz G, Bar-Ilan A, Bloushtain N, Lev M, Joseph A, et al. The mechanisms controlling the recognition of tumor- and virus-infected cells by NKp46. Blood. 2004;103(2):664–72. doi:10.1182/blood-2003-05-1716.
  • Ferlazzo G, Thomas D, Lin SL, Goodman K, Morandi B, Muller WA, Moretta A, Münz C. The abundant NK cells in human secondary lymphoid tissues require activation to express killer cell Ig-like receptors and become cytolytic. J Immunol. 2004;172(3):1455–62. doi:10.4049/jimmunol.172.3.1455.
  • Vitale M, Bottino C, Sivori S, Sanseverino L, Castriconi R, Marcenaro E, Augugliaro R, Moretta L, Moretta A. Nkp44, a novel triggering surface molecule specifically expressed by activated natural killer cells, is involved in non–major histocompatibility complex–restricted tumor cell Lysis. J Exp Med. 1998;187(12):2065–72. doi:10.1084/jem.187.12.2065.
  • Guo X, Mahlakoiv T, Ye Q, Somanchi S, He S, Rana H, DiFiglia A, Gleason J, van der Touw W, Hariri R, et al. CBLB ablation with CRISPR/Cas9 enhances cytotoxicity of human placental stem cell-derived NK cells for cancer immunotherapy. J Immunother Cancer. 2021;9(3):e001975. doi:10.1136/jitc-2020-001975.
  • Alon R, Sportiello M, Kozlovski S, Kumar A, Reilly EC, Zarbock A, Garbi N, Topham DJ. Leukocyte trafficking to the lungs and beyond: lessons from influenza for COVID-19. Nat Rev Immunol. 2021;21(1):49–64. doi:10.1038/s41577-020-00470-2.
  • Myers MA, Smith AP, Lane LC, Moquin DJ, Aogo R, Woolard S, Thomas P, Vogel P, Smith AM. Dynamically linking influenza virus infection kinetics, lung injury, inflammation, and disease severity. Elife. 2021;10:10. doi:10.7554/eLife.68864.
  • Califano D, Furuya Y, Roberts S, Avram D, McKenzie ANJ, Metzger DW. IFN-γ increases susceptibility to influenza a infection through suppression of group II innate lymphoid cells. Mucosal Immunol. 2018;11(1):209–19. doi:10.1038/mi.2017.41.
  • Nicol MQ, Campbell GM, Shaw DJ, Dransfield I, Ligertwood Y, Beard PM, Nash AA, Dutia BM. Lack of IFNγ signaling attenuates spread of influenza a virus in vivo and leads to reduced pathogenesis. Virology. 2019;526:155–64. doi:10.1016/j.virol.2018.10.017.
  • Hui KP, Lee SM, Cheung CY, Ng IH, Poon LL, Guan Y, Ip NYY, Lau ASY, Peiris JSM. Induction of proinflammatory cytokines in primary human macrophages by influenza a virus (H5N1) is selectively regulated by IFN regulatory factor 3 and p38 MAPK. J Immunol. 2009;182(2):1088–98. doi:10.4049/jimmunol.182.2.1088.
  • Liu B, Bao L, Wang L, Li F, Wen M, Li H, Deng W, Zhang X, Cao B. Anti-IFN-γ therapy alleviates acute lung injury induced by severe influenza a (H1N1) pdm09 infection in mice. J Microbiol Immunol Infect. 2021;54(3):396–403. doi:10.1016/j.jmii.2019.07.009.
  • Weiss ID, Wald O, Wald H, Beider K, Abraham M, Galun E, Nagler A, Peled A. IFN-γ treatment at early stages of influenza virus infection protects mice from death in a NK cell-dependent manner. J Interferon Cytokine Res. 2010;30(6):439–49. doi:10.1089/jir.2009.0084.
  • Karupiah G, Chen JH, Mahalingam S, Nathan CF, MacMicking JD. Rapid interferon γ–dependent clearance of Influenza A virus and protection from consolidating pneumonitis in nitric oxide Synthase 2–deficient mice. J Exp Med. 1998;188(8):1541–46. doi:10.1084/jem.188.8.1541.
  • Deshmane SL, Kremlev S, Amini S, Sawaya BE. Monocyte chemoattractant protein-1 (MCP-1): an overview. J Interferon Cytokine Res. 2009;29(6):313–26. doi:10.1089/jir.2008.0027.
  • Indavarapu A, Akinapelli A. Neutrophils to lymphocyte ratio as a screening tool for swine influenza. Indian J Med Res. 2011;134:389–91. [accessed 2021 Jul 15].
  • Zhang Y, Zou P, Gao H, Yang M, Yi P, Gan J, Shen Y, Wang W, Zhang W, Li J, et al. Neutrophil–lymphocyte ratio as an early new marker in AIV-H7N9-infected patients: a retrospective study. Ther Clin Risk Manag. 2019;15:911–19. doi:10.2147/TCRM.S206930.
  • Hosseini S, Wilk E, Michaelsen-Preusse K, Gerhauser I, Baumgartner W, Geffers R, Schughart K, Korte M. Long-Term neuroinflammation induced by Influenza A virus infection and the impact on Hippocampal neuron morphology and function. J Neurosci. 2018;38(12):3060–80. doi:10.1523/JNEUROSCI.1740-17.2018.
  • Wunderlich M, Chou FS, Sexton C, Presicce P, Chougnet CA, Aliberti J, Mulloy JC. Improved multilineage human hematopoietic reconstitution and function in NSGS mice. PLoS One. 2018;13(12):e0209034. doi:10.1371/journal.pone.0209034.