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Review

Drugs for Multiple Sclerosis Activate Natural Killer Cells: Do They Protect Against COVID-19 Infection?

, ORCID Icon, & ORCID Icon
Pages 3243-3254 | Published online: 22 Sep 2020

References

  • Rota PA, Oberste MS, Monroe SS, et al. Characterization of a novel coronavirus associated with severe acute respiratory syndrome. Science. 2003;300(5264):1394–1399. doi:10.1126/science.108595212730500
  • Velavan TP, Meyer CG. The COVID-19 epidemic. Trop Med Int Health. 2020;25(3):278–280. doi:10.1111/tmi.1338332052514
  • Zhou P, Yang XL, Wang XG, et al. A pneumonia outbreak associated with a new coronavirus of probable bat origin. Nature. 2020;579(7798):270–273. doi:10.1038/s41586-020-2012-732015507
  • GISAID Global Initiative on Sharing All Influenza Data. Phylogeny of SARS-like betacoronaviruses including novelcoronavirus (nCoV). Available from: https://nextstrain.org/groups/blab/sars-like-cov.
  • Wang C, Horby PW, Hayden FG, Gao GF. A novel coronavirus outbreak of global health concern. Lancet. 2020;395(10223):470–473. doi:10.1016/S0140-6736(20)30185-931986257
  • Manocha S, Walley KR, Russell JA. Severe acute respiratory distress syndrome (SARS): a critical care perspective. Crit Care Med. 2003;31(11):2684–2692. doi:10.1097/01.CCM.0000091929.51288.5F14605542
  • Rothe C, Schunk M, Sothmann P, et al. Transmission of 2019-nCoV infection from an asymptomatic contact in Germany. N Engl J Med. 2020;382(10):970–971. doi:10.1056/NEJMc200146832003551
  • Cheng ZJ, Shan J. Novel coronavirus: where we are and what we know. Infection. 2019;2020(48):155–163. doi:10.1007/s15010-020-01401-y
  • Prabakaran P, Xiao X, Dimitrov DS. A model of the ACE2 structure and function as a SARS-CoV receptor. Biochem Biophys Res Commun. 2004;314(1):235–241. doi:10.1016/j.bbrc.2003.12.08114715271
  • Li W, Moore MJ, Vasilieva N, et al. Angiotensin-converting enzyme 2 is a functional receptor for the SARS coronavirus. Nature. 2003;426:450–454. doi:10.1038/nature0214514647384
  • Yan R, Zhang Y, Li Y, Xia L, Guo Y, Zhou Q. Structural basis for the recognition of SARS-CoV-2 by full-length human ACE2. Science. 2020;367:1444–1448. doi:10.1126/science.abb276232132184
  • Buscarini E, Manfredi G, Brambilla G, et al. GI symptoms as early signs of COVID-19 in hospitalised Italian patients. Gut. 2020;69:1547–1548. doi:10.1136/gutjnl-2020-32143432409587
  • Guan W, Ni Z, Hu Y, et al. Clinical characteristics of coronavirus disease 2019 in China. N Engl J Med. 2020;382:1708–1720. doi:10.1056/NEJMoa200203232109013
  • Chen F, Liu ZS, Zhang FR, et al. [First case of severe childhood novel coronavirus pneumonia in China]. Zhonghua Er Ke Za Zhi. 2020;58:E005. doi:10.3760/cma.j.issn.0578-1310.2020.0005. [in Chinese.].32045966
  • Chen N, Zhou M, Dong X, et al. Epidemiological and clinical characteristics of 99 cases of 2019 novel coronavirus pneumonia in Wuhan, China: a descriptive study. Lancet. 2020;395(10223):507–513. doi:10.1016/S0140-6736(20)30211-732007143
  • Huang C, Wang Y, Li X, et al. Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. Lancet. 2020;395(10223):497–506. doi:10.1016/S0140-6736(20)30183-531986264
  • Mehta P, McAuley DF, Brown M, Sanchez E, Tattersall RS, Manson JJ. COVID-19: consider cytokine storm syndromes and immunosuppression. Lancet. 2020;395(10229):1033–1034. doi:10.1016/S0140-6736(20)30628-032192578
  • Cao W, Liu X, Bai T, et al. High-dose intravenous immunoglobulin as a therapeutic option for deteriorating patients with coronavirus disease 2019. Open Forum Infect Dis. 2020;7(3):ofaa102. doi:10.1093/ofid/ofaa10232258207
  • Wang M, Cao R, Zhang L, et al. Remdesivir and chloroquine effectively inhibit the recently emerged novel coronavirus (2019-nCoV) in vitro. Cell Res. 2020;30(3):269–271. doi:10.1038/s41422-020-0282-032020029
  • Chu CM, Cheng VCC, Hung IFN, et al. Role of lopinavir/ritonavir in the treatment of SARS: initial virological and clinical findings. Thorax. 2004;59(3):252. doi:10.1136/thorax.2003.01265814985565
  • Stower H. Lopinavir–ritonavir in severe COVID-19. Nat Med. 2020;26(4):465. doi:10.1038/s41591-020-0849-9
  • Richardson P, Griffin I, Tucker C, et al. Baricitinib as potential treatment for 2019-nCoV acute respiratory disease. Lancet. 2020;395(10223):e30e31. doi:10.1016/S0140-6736(20)30304-432032529
  • Cantini F, Niccoli L, Matarrese D, Nicastri E, Stobbione P, Goletti D. Baricitinib therapy in COVID-19: a pilot study on safety and clinical impact. J Infect. 2020;81:318–356. doi:10.1016/j.jinf.2020.04.017
  • Lanier LL. Evolutionary struggles between NK cells and viruses. Nat Rev Immunol. 2008;8(4):259–268. doi:10.1038/nri227618340344
  • Maghazachi AA, Al-Aoukaty A. Chemokines activate natural killer cells through heterotrimeric G-proteins: implications for the treatment of AIDS and cancer. FASEB J. 1998;12(11):913–924. doi:10.1096/fasebj.12.11.9139707163
  • Jost S, Altfeld M. Control of human viral infections by natural killer cells. Annu Rev Immunol. 2013;31:163–194. doi:10.1146/annurev-immunol-032712-10000123298212
  • Long EO, Sik Kim H, Liu D, Peterson ME, Rajagopalan S. Controlling natural killer cell responses: integration of signals for activation and inhibition. Annu Rev Immunol. 2013;31:227–258. doi:10.1146/annurev-immunol-020711-07500523516982
  • Cooper MA, Fehniger TA, Turner SC, et al. Human natural killer cells: a unique innate immunoregulatory role for the CD56bright subset. Blood. 2001;97(10):3146–3151. doi:10.1182/blood.v97.10.314611342442
  • Guidotti LG, Chisari FV. Cytokine-mediated control of viral infections. Virology. 2000;273(2):221–227. doi:10.1006/viro.2000.044210915592
  • Biron CA, Nguyen KB, Pien GC, Cousens LP, Salazar-Mather TP. Natural killer cells in antiviral defense: function and regulation by innate cytokines. Annu Rev Immunol. 1999;17:189–220. doi:10.1146/annurev.immunol.17.1.18910358757
  • Vivier E, Tomasello E, Baratin M, Walzer T, Ugolini S. Functions of natural killer cells. Nat Immunol. 2008;9(5):503–510. doi:10.1038/ni158218425107
  • Degli-Esposti MA, Smyth MJ. Close encounters of different kinds: dendritic cells and NK cells take centre stage. Nat Rev Immunol. 2005;5(2):112–124. doi:10.1038/nri154915688039
  • Cooper MA, Fehniger TA, Caligiuri MA. The biology of human natural killer-cell subsets. Trends Immunol. 2001;22(11):633–640. doi:10.1016/s1471-4906(01)02060-911698225
  • Maghazachi AA. Compartmentalization of human natural killer cells. Mol Immunol. 2005;42(4):523–529. doi:10.1016/j.molimm.2004.07.03615607808
  • Maghazachi AA. Insights into seven and single transmembrane-spanning domain receptors and their signaling pathways in human natural killer cells. Pharmacol Rev. 2005;57(3):339–357. doi:10.1124/pr.57.3.516109839
  • Cantoni C, Bottino C, Vitale M, et al. NKp44, a triggering receptor involved in tumor cell lysis by activated human natural killer cells, is a novel member of the immunoglobulin superfamily. J Exp Med. 1999;189(5):787–796. doi:10.1084/jem.189.5.78710049942
  • Koch J, Steinle A, Watzl C, Mandelboim O. Activating natural cytotoxicity receptors of natural killer cells in cancer and infection. Trends Immunol. 2013;34(4):182–191. doi:10.1016/j.it.2013.01.00323414611
  • Pende D, Parolini S, Pessino A, et al. Identification and molecular characterization of NKp30, a novel triggering receptor involved in natural cytotoxicity mediated by human natural killer cells. J Exp Med. 1999;190(10):1505–1516. doi:10.1084/jem.190.10.150510562324
  • Pessino A, Sivori S, Bottino C, et al. Molecular cloning of NKp46: a novel member of the immunoglobulin superfamily involved in triggering of natural cytotoxicity. J Exp Med. 1998;188(5):953–960. doi:10.1084/jem.188.5.9539730896
  • Wu J, Song Y, Bakker ABH, et al. An activating immunoreceptor complex formed by NKG2D and DAP10. Science. 1999;285(5428):730–732. doi:10.1126/science.285.5428.73010426994
  • Hayakawa Y, Huntington ND, Nutt SL, Smyth MJ. Functional subsets of mouse natural killer cells. Immunol Rev. 2006;214:47–55. doi:10.1111/j.1600-065X.2006.00454.x17100875
  • Lanier LL. NK cell receptors. Annu Rev Immunol. 1998;16:359–393. doi:10.1146/annurev.immunol.16.1.3599597134
  • Abel AM, Yang C, Thakar MS, Malarkannan S. Natural killer cells: development, maturation, and clinical utilization. Front Immunol. 2018;9:1869. doi:10.3389/fimmu.2018.0186930150991
  • Sun JC, Lanier LL. NK cell development, homeostasis and function: parallels with CD8+ T cells. Nat Rev Immunol. 2011;11(10):645–657. doi:10.1038/nri304421869816
  • Lee S-H, Biron CA. Here today-not gone tomorrow: roles for activating receptors in sustaining NK cells during viral infections. Eur J Immunol. 2010;40(4):923–932. doi:10.1002/eji.20104030420209503
  • Biron CA, Byron KS, Sullivan JL. Severe herpesvirus infections in an adolescent without natural killer cells. N Engl J Med. 1989;320(26):1731–1735. doi:10.1056/NEJM1989062932026052543925
  • Brandstadter JD, Yang Y. Natural killer cell responses to viral infection. J Innate Immun. 2011;3(3):274–279. doi:10.1159/00032417621411975
  • Elemam NM, Mekky RY, El-Ekiaby NM, et al. Repressing PU.1 by miR-29a in NK cells of HCV patients, diminishes its cytolytic effect on HCV infected cell models. Hum Immunol. 2015;76(9):687–694. doi:10.1016/j.humimm.2015.09.02126429314
  • Orange Jordan S. Human natural killer cell deficiencies and susceptibility to infection. Microbes Infect. 2002;4(15):1545–1558. doi:10.1016/s1286-4579(02)00038-212505527
  • Yoon JC, Yang CM, Song Y, Lee JM. Natural killer cells in hepatitis C: current progress. World J Gastroenterol. 2016;22(4):1449–1460. doi:10.3748/wjg.v22.i4.144926819513
  • Arase H, Lanier LL. Specific recognition of virus-infected cells by paired NK receptors. Rev Med Virol. 2004;14(2):83–93. doi:10.1002/rmv.42215027001
  • Scalzo AA, Yokoyama WM. Cmv1 and natural killer cell responses to murine cytomegalovirus infection. Curr Top Microbiol Immunol. 2008;321:101–122. doi:10.1007/978-3-540-75203-5_518727489
  • Hammer Q, Rückert T, Romagnani C. Natural killer cell specificity for viral infections. Nat Immunol. 2018;19(8):800–808. doi:10.1038/s41590-018-0163-630026479
  • Lam VC, Lanier LL. NK cells in host responses to viral infections. Curr Opin Immunol. 2017;44:43–51. doi:10.1016/j.coi.2016.11.00327984782
  • van Erp EA, van Kampen MR, van Kasteren PB, de Wit J. Viral infection of human natural killer cells. Viruses. 2019;11(3):243. doi:10.3390/v11030243
  • Guimei MM, Barqawi HJ, Dash NR, Maghazachi AA. Sepsis-the dilemma continues. MOJ Immunol. 2016;4(3):00125. doi:10.15406/moji.2016.04.00125
  • Liu WJ, Zhao M, Liu K, et al. T-cell immunity of SARS-CoV: implications for vaccine development against MERS-CoV. Antivir Res. 2017;137:82–92. doi:10.1016/j.antiviral.2016.11.00627840203
  • Zhang C, Wang XM, Li SR, et al. NKG2A is a NK cell exhaustion checkpoint for HCV persistence. Nat Commun. 2019;10(1):1507. doi:10.1038/s41467-019-09212-y30944315
  • Zheng M, Gao Y, Wang G, et al. Functional exhaustion of antiviral lymphocytes in COVID-19 patients. Cell Mol Immunol. 2020;17(5):533–535. doi:10.1038/s41423-020-0402-232203188
  • Hadjadj J, Yatim N, Barnabei L, et al. Impaired type I interferon activity and inflammatory responses in severe COVID-19 patients. Science. 2020;369(6504):718. doi:10.1126/science.abc602732661059
  • Cinatl J, Morgenstern B, Bauer G, Chandra P, Rabenau H, Doerr HW. Treatment of SARS with human interferons. Lancet. 2003;362(9380):293–294. doi:10.1016/s0140-6736(03)13973-612892961
  • Rothan HA, Byrareddy SN. The epidemiology and pathogenesis of coronavirus disease (COVID-19) outbreak. J Autoimmun. 2020;109:102433. doi:10.1016/j.jaut.2020.10243332113704
  • Wang F, Nie J, Wang H, et al. Characteristics of peripheral lymphocyte subset alteration in COVID-19 pneumonia. J Infect Dis. 2020;221(11):1762–1769. doi:10.1093/infdis/jiaa15032227123
  • Cui W, Fan Y, Wu W, Zhang F, Wang JY, Ni AP. Expression of lymphocytes and lymphocyte subsets in patients with severe acute respiratory syndrome. Clin Infect Dis. 2003;37(6):857–859. doi:10.1086/37858712955652
  • He Z, Zhao C, Dong Q, et al. Effects of severe acute respiratory syndrome (SARS) coronavirus infection on peripheral blood lymphocytes and their subsets. Int J Infect Dis. 2005;9(6):323–330. doi:10.1016/j.ijid.2004.07.01416095942
  • National Research Project for Sars BG. The involvement of natural killer cells in the pathogenesis of severe acute respiratory syndrome. Am J Clin Pathol. 2004;121(4):507–511. doi:10.1309/WPK7-Y2XK-NF4C-BF3R.15080302
  • Osman MS, van Eeden C, Cohen Tervaert JW. Fatal COVID-19 infections: is NK cell dysfunction a link with autoimmune HLH? Autoimmun Rev. 2020;19(7):102561. doi:10.1016/j.autrev.2020.10256132376401
  • Celularity and Infectious Disease Research Institute will try out COVID-19 cell therapy. Available from: https://www.geekwire.com/2020/celularity-infectious-disease-research-institute-win-fdas-ok-try-covid-19-cell-therapy. Accessed 2020.
  • Giuliani-promoted COVID-19 therapy from Celularity nabs FDA speedy trial start. Available from: https://www.fiercebiotech.com/biotech/rudy-giuliani-backed-covid-19-therapy-from-celularity-nabs-fda-speedy-trial-start. Accessed 2020.
  • Han J, Chu J, Keung Chan W, et al. CAR-engineered NK cells targeting wild-type EGFR and EGFRvIII enhance killing of glioblastoma and patient-derived glioblastoma stem cells. Sci Rep. 2015;5:11483. doi:10.1038/srep1148326155832
  • Liu E, Marin D, Banerjee P, et al. Use of CAR-transduced natural killer cells in CD19-positive lymphoid tumors. N Engl J Med. 2020;382(6):545–553. doi:10.1056/NEJMoa191060732023374
  • Wang W, Jiang J, Wu C. CAR-NK for tumor immunotherapy: clinical transformation and future prospects. Cancer Lett. 2020;472:175–180. doi:10.1016/j.canlet.2019.11.03331790761
  • Market M, Angka L, Martel AB, et al. Flattening the COVID-19 curve with natural killer cell based immunotherapies. Front Immunol. 2020;11:1512. doi:10.3389/fimmu.2020.0151232655581
  • Hachim MY, Elemam NM, Maghazachi AA. The beneficial and debilitating effects of environmental and microbial toxins, drugs, organic solvents and heavy metals on the onset and progression of multiple sclerosis. Toxins. 2019;11(3):147. doi:10.3390/toxins11030147
  • Caprariello AV, Rogers JA, Morgan ML, et al. Biochemically altered myelin triggers autoimmune demyelination. Proc Natl Acad Sci USA. 2018;115(21):5528–5533. doi:10.1073/pnas.172111511529728463
  • Steinman L. Multiple sclerosis: a coordinated immunological attack against myelin in the central nervous system. Cell. 1996;85(3):299–302. doi:10.1016/s0092-8674(00)81107-18616884
  • Maghazachi AA. Role of natural killer cells in multiple sclerosis. ISRN Immunol. 2012;2012:1–14. doi:10.5402/2012/795075
  • Maghazachi AA. On the role of natural killer cells in neurodegenerative diseases. Toxins. 2013;5(2):363–375. doi:10.3390/toxins502036323430541
  • Hestvik AL. The double-edged sword of autoimmunity: lessons from multiple sclerosis. Toxins. 2010;2(4):856–877. doi:10.3390/toxins204085622069614
  • Ghasemi N, Razavi S, Nikzad E. Multiple sclerosis: pathogenesis, symptoms, diagnoses and cell-based therapy. Cell J. 2017;19(1):1–10. doi:10.22074/cellj.2016.4867
  • Lublin FD, Reingold SC. Defining the clinical course of multiple sclerosis: results of an international survey. National multiple sclerosis society (USA) advisory committee on clinical trials of new agents in multiple sclerosis. Neurology. 1996;46(4):907–911. doi:10.1212/wnl.46.4.9078780061
  • Boiko A, Vorobeychik G, Paty D, Devonshire V, Sadovnick D. Early onset multiple sclerosis: a longitudinal study. Neurology. 2002;59(7):1006–1010. doi:10.1212/wnl.59.7.100612370453
  • Gadoth N. Multiple sclerosis in children. Brain Dev. 2003;25(4):229–232. doi:10.1016/s0387-7604(03)00035-412767451
  • Förster M, Küry P, Aktas O, et al. Managing risks with immune therapies in multiple sclerosis. Drug Saf. 2019;42(5):633–647. doi:10.1007/s40264-018-0782-830607830
  • Al-Jaderi Z, Maghazachi AA. Utilization of dimethyl fumarate and related molecules for treatment of multiple sclerosis, cancer, and other diseases. Front Immunol. 2016;7:278. doi:10.3389/fimmu.2016.0027827499754
  • Gandhi R, Laroni A, Weiner HL. Role of the innate immune system in the pathogenesis of multiple sclerosis. J Neuroimmunol. 2010;221(12):7–14. doi:10.1016/j.jneuroim.2009.10.01519931190
  • Lünemann JD, Münz C. Do natural killer cells accelerate or prevent autoimmunity in multiple sclerosis? Brain. 2008;131(Pt 7)):1681–1683. doi:10.1093/brain/awn13218586760
  • Mimpen M, Smolders J, Hupperts R, Damoiseaux J. Natural killer cells in multiple sclerosis: a review. Immunol Lett. 2020;222:1–11. doi:10.1016/j.imlet.2020.02.01232113900
  • Morandi B, Bramanti P, Bonaccorsi I, et al. Role of natural killer cells in the pathogenesis and progression of multiple sclerosis. Pharmacol Res. 2008;57(1):1–5. doi:10.1016/j.phrs.2007.11.00318182304
  • Leavenworth JW, Schellack C, Kim HJ, Lu L, Spee P, Cantor H. Analysis of the cellular mechanism underlying inhibition of EAE after treatment with anti-NKG2A F(ab’)2. Proc Natl Acad Sci USA. 2010;107(6):2562–2567. doi:10.1073/pnas.091473210720133787
  • Hao J, Liu R, Piao W, et al. Central nervous system (CNS)–resident natural killer cells suppress Th17 responses and CNS autoimmune pathology. J Exp Med. 2010;207(9):1907–1921. doi:10.1084/jem.2009274920696699
  • Matsumoto Y, Kohyama K, Aikawa Y, et al. Role of natural killer cells and TCRγ δ T cells in acute autoimmune encephalomyelitis. Eur J Immunol. 1998;28(5):1681–1688. doi:10.1002/(SICI)1521-4141(199805)28:05<1681::AID-IMMU1681>3.0.CO;2-T9603475
  • Segal BM. The role of natural killer cells in curbing neuroinflammation. J Neuroimmunol. 2007;191(12):2–7. doi:10.1016/j.jneuroim.2007.09.00617904646
  • Takahashi K, Aranami T, Endoh M, Miyake S, Yamamura T. The regulatory role of natural killer cells in multiple sclerosis. Brain. 2004;127(Pt 9):1917–1927. doi:10.1093/brain/awh21915229129
  • Liu Q, Sanai N, Jin WN, La-Cava A, Van-Kaer L, Shi FD. Neural stem cells sustain natural killer cells that dictate recovery from brain inflammation. Nat Neurosci. 2016;19(2):243–252. doi:10.1038/nn.421126752157
  • Lepennetier G, Hracsko Z, Unger M, et al. Cytokine and immune cell profiling in the cerebrospinal fluid of patients with neuro-inflammatory diseases. J Neuroinflammation. 2019;16(1):219. doi:10.1186/s12974-019-1601-631727097
  • Gross CC, Schulte-Mecklenbeck A, Rünzi A, et al. Impaired NK-mediated regulation of T-cell activity in multiple sclerosis is reconstituted by IL-2 receptor modulation. Proc Natl Acad Sci USA. 2016;113(21):E2973E2982. doi:10.1073/pnas.152492411327162345
  • Rodríguez-Martín E, Picón C, Costa-Frossard L, et al. Natural killer cell subsets in cerebrospinal fluid of patients with multiple sclerosis. Clin Exp Immunol. 2015;180(2):243–249. doi:10.1111/cei.1258025565222
  • Pandya AD, Al-Jaderi Z, Høglund RA, et al. Identification of human NK17/NK1 cells. PLoS One. 2011;6(10):e26780. doi:10.1371/journal.pone.002678022039549
  • Elemam NM, Hannawi S, Maghazachi AA. Innate lymphoid cells (ILCs) as mediators of inflammation, release of cytokines and lytic molecules. Toxins. 2017;9(12):E398. doi:10.3390/toxins912039829232860
  • Gross CC, Schulte-Mecklenbeck A, Wiendl H, et al. Regulatory functions of natural killer cells in multiple sclerosis. Front Immunol. 2016;7:606. doi:10.3389/fimmu.2016.0060628066417
  • Durrenberger PF, Webb LV, Sim MJ, et al. Expression in white matter lesions in multiple sclerosis. Immunology. 2012;137(4):317–325. doi:10.1111/imm.1201223039207
  • Laroni A, Uccelli A. CD56bright natural killer cells: a possible biomarker of different treatments in multiple sclerosis. J Clin Med. 2020;9:5. doi:10.3390/jcm9051450
  • Arnon R, Aharoni R. Mechanism of action of glatiramer acetate in multiple sclerosis and its potential for the development of new applications. Proc Natl Acad Sci USA. 2004;101:14593–14598. doi:10.1073/pnas.040488710115371592
  • Kala M, Miravalle A, Vollmer T. Recent insights into the mechanism of action of glatiramer acetate. J Neuroimmunol. 2011;235(12):9–17. doi:10.1016/j.jneuroim.2011.01.00921402415
  • Weber MS, Starck M, Wagenpfeil S, Meinl E, Hohlfeld R, Farina C. Multiple sclerosis: glatiramer acetate inhibits monocyte reactivity in vitro and in vivo. Brain. 2004;127(Pt 6):1370–1378. doi:10.1093/brain/awh16315090474
  • Sand KL, Knudsen E, Rolin J, Al-Falahi Y, Maghazachi AA. Modulation of natural killer cell cytotoxicity and cytokine release by the drug glatiramer acetate. Cell Mol Life Sci. 2009;66(8):1446–1456. doi:10.1007/s00018-009-8726-119277466
  • Høglund RA, Holmøy T, Harbo HF, Maghazachi AA. A one year follow-up study of natural killer and dendritic cells activities in multiple sclerosis patients receiving glatiramer acetate (GA). PLoS One. 2013;8(4):e62237. doi:10.1371/journal.pone.006223723614042
  • Duda PW, Schmied MC, Cook SL, Krieger JI, Hafler DA. Glatiramer acetate (Copaxone®) induces degenerate, Th2-polarized immune responses in patients with multiple sclerosis. J Clin Invest. 2000;105(7):967–976. doi:10.1172/JCI897010749576
  • Kim HJ, Ifergan I, Antel JP, et al. Type 2 monocyte and microglia differentiation mediated by glatiramer acetate therapy in patients with multiple sclerosis. J Immunol. 2004;172(11):7144–7153. doi:10.4049/jimmunol.172.11.714415153538
  • Moharregh-Khiabani D, Linker RA, Gold R, Stangel M. Fumaric acid and its esters: an emerging treatment for multiple sclerosis. Curr Neuropharmacol. 2009;7(1):60–64. doi:10.2174/15701590978760278819721818
  • Bomprezzi R. Dimethyl fumarate in the treatment of relapsing-remitting multiple sclerosis: an overview. Ther Adv Neurol Disord. 2015;8(1):20–30. doi:10.1177/175628561456415225584071
  • Linker RA, Lee DH, Ryan S, et al. Fumaric acid esters exert neuroprotective effects in neuroinflammation via activation of the Nrf2 antioxidant pathway. Brain. 2011;134(Pt 3)):678–692. doi:10.1093/brain/awq38621354971
  • Marastoni D, Buriani A, Pisani AI, et al. Increased NK cell count in multiple sclerosis patients treated with dimethyl fumarate: a 2-year longitudinal study. Front Immunol. 2019;10:1666. doi:10.3389/fimmu.2019.0166631379857
  • de Jong R, Bezemer AC, Zomerdijk TP, van de Pouw-kraan T, Ottenhoff TH, Nibbering PH. Selective stimulation of T helper 2 cytokine responses by the anti-psoriasis agent monomethylfumarate. Eur J Immunol. 1996;26(9):2067–2074. doi:10.1002/eji.18302609168814248
  • Al-Jaderi Z, Maghazachi AA. Vitamin D3 and monomethyl fumarate enhance natural killer cell lysis of dendritic cells and ameliorate the clinical score in mice suffering from experimental autoimmune encephalomyelitis. Toxins. 2015;7(11):4730–4744. doi:10.3390/toxins711473026580651
  • Elemam NM, Al-Jaderi Z, Hachim MY, Maghazachi AA. HCT-116 colorectal cancer cells secrete chemokines which induce chemoattraction and intracellular calcium mobilization in NK92 cells. Cancer Immunol Immunother. 2019;68(6):883–895. doi:10.1007/s00262-019-02319-730847498
  • Vego H, Sand KL, Høglund RA, et al. Monomethyl fumarate augments NK cell lysis of tumor cells through degranulation and the upregulation of NKp46 and CD107a. Cell Mol Immunol. 2016;13(1):57–64. doi:10.1038/cmi.2014.11425435072
  • Maghazachi AA, Sand KL, Al-Jaderi Z. Glatiramer acetate, dimethyl fumarate, and monomethyl fumarate upregulate the expression of CCR10 on the surface of natural killer cells and enhance their chemotaxis and cytotoxicity. Front Immunol. 2016;7:437. doi:10.3389/fimmu.2016.0043727807435
  • Mohan T, Deng L, Wang BZ. CCL28 chemokine: an anchoring point bridging innate and adaptive immunity. Int Immunopharmacol. 2017;51:165–170. doi:10.1016/j.intimp.2017.08.01228843907
  • Muhammad JS, Jayakumar MN, Elemam NM, et al. Gasdermin D hypermethylation inhibits pyroptosis and LPS-induced IL-1β release from NK92 cells. Immunotargets Ther. 2019;8:29–41. doi:10.2147/ITT.S21986731687364
  • Smith MD, Calabresi PA, Bhargava P. Dimethyl fumarate treatment alters NK cell function in multiple sclerosis. Eur J Immunol. 2018;48(2):380–383. doi:10.1002/eji.20174727729108094
  • Medina S, Villarrubia N, Sainz de la Maza S, et al. Optimal response to dimethyl fumarate associates in MS with a shift from an inflammatory to a tolerogenic blood cell profile. Mult Scler. 2018;24(10):1317–1327. doi:10.1177/135245851771708828653862
  • Ascherio A, Munger KL. Environmental risk factors for multiple sclerosis. Part II: noninfectious factors. Ann Neurol. 2007;61(6):504–513. doi:10.1002/ana.2114117492755
  • Lemire JM, Archer DC. 1,25-dihydroxyvitamin D3 prevents the in vivo induction of murine experimental autoimmune encephalomyelitis. J Clin Invest. 1991;87(3):1103–1107. doi:10.1172/JCI1150721705564
  • Cantorna MT, Hayes CE, DeLuca HF. 1,25-Dihydroxyvitamin D3 reversibly blocks the progression of relapsing encephalomyelitis, a model of multiple sclerosis. Proc Natl Acad Sci USA. 1996;93(15):7861–7864. doi:10.1073/pnas.93.15.78618755567
  • Burton JM, Kimball S, Vieth R, et al. A Phase I/II dose-escalation trial of vitamin D3 and calcium in multiple sclerosis. Neurology. 2010;74(23):1852–1859. doi:10.1212/WNL.0b013e3181e1cec220427749
  • Hupperts R, Smolders J, Vieth R, et al. Randomized trial of daily high-dose vitamin D(3) in patients with RRMS receiving subcutaneous interferon β-1a. Neurology. 2019;93(20):e1906e1916. doi:10.1212/wnl.000000000000844531594857
  • Rinaldi AO, Sanseverino I, Purificato C, et al. Increased circulating levels of vitamin D binding protein in MS patients. Toxins. 2015;7(1):129–137. doi:10.3390/toxins701012925590278
  • Al-Jaderi Z, Maghazachi AA. Effects of vitamin D3, calcipotriol and FTY720 on the expression of surface molecules and cytolytic activities of human natural killer cells and dendritic cells. Toxins. 2013;5(11):1932–1947. doi:10.3390/toxins511193224169587
  • Smolders J, Peelen E, Thewissen M, et al. Safety and T cell modulating effects of high dose vitamin d3 supplementation in multiple sclerosis. PLoS One. 2010;5(12):e15235. doi:10.1371/journal.pone.001523521179201
  • Smolders J, Thewissen M, Peelen E, et al. Vitamin D status is positively correlated with regulatory T cell function in patients with multiple sclerosis. PLoS One. 2009;4(8):e6635. doi:10.1371/journal.pone.000663519675671
  • Connor P, Comi G, Montalban X, et al. Oral fingolimod (FTY720) in multiple sclerosis: two-year results of a Phase II extension study. Neurology. 2009;72(1):73–79. doi:10.1212/01.wnl.0000338569.32367.3d19122034
  • Kappos L, Antel J, Comi G, et al. Oral fingolimod (FTY720) for relapsing multiple sclerosis. N Engl J Med. 2006;355(11):1124–1140. doi:10.1056/NEJMoa05264316971719
  • Rolin J, Sand KL, Knudsen E, Maghazachi AA. FTY720 and SEW2871 reverse the inhibitory effect of S1P on natural killer cell mediated lysis of K562 tumor cells and dendritic cells but not on cytokine release. Cancer Immunol Immunother. 2010;59(4):575–586. doi:10.1007/s00262-009-0775-719823820
  • Saraste M, Irjala H, Airas L. Expansion of CD56bright natural killer cells in the peripheral blood of multiple sclerosis patients treated with interferon-beta. Neurol Sci. 2007;28(3):121–126. doi:10.1007/s10072-007-0803-317603762
  • Martínez-Rodríguez JE, López-Botet M, Munteis E, et al. Natural killer cell phenotype and clinical response to interferon-beta therapy in multiple sclerosis. Clin Immunol. 2011;141(3):348–356. doi:10.1016/j.clim.2011.09.00621992960
  • Kaufmann M, Haase R, Proschmann U, Ziemssen T, Akgün K. Real-world lab data in natalizumab treated multiple sclerosis patients up to 6 years long-term follow up. Front Neurol. 2018;9:1071. doi:10.3389/fneur.2018.0107130581413
  • Greenfield AL, Hauser SL. B-cell therapy for multiple sclerosis: entering an era. Ann Neurol. 2018;83(1):13–26. doi:10.1002/ana.2511929244240