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ISSN (Online): 1875-5607

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Mini-Review Article

Tuberculosis, BCG Vaccination, and COVID-19: Are They Connected?

Author(s): Kellen Christina Malheiros Borges, Adeliane Castro da Costa, Lília Cristina de Souza Barbosa, Kaio Mota Ribeiro, Laura Raniere Borges dos Anjos, André Kipnis and Ana Paula Junqueira-Kipnis*

Volume 22, Issue 12, 2022

Published on: 27 January, 2022

Page: [1631 - 1647] Pages: 17

DOI: 10.2174/1389557522666220104152634

Price: $65

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Abstract

Evidence from multiple scientific studies suggests that the Bacillus Calmette–Guérin (BCG) vaccine, widely used worldwide as a preventive measure against tuberculosis, also offers crossprotection against other pathogens. This review aimed to gather data from research that studied the mechanisms involved in the immunological protection induced by the BCG vaccine, which may be important in the control of viral infections, such as COVID-19. Through a literature review, we compiled information about the different BCG strains used worldwide, as well as the responses and protection elicited by them. We commented on the mechanisms of immune response to Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2), and we discussed the possibility of cross-protection of different BCG strains on the control of COVID-19. Due to the immunomodulatory properties of BCG, some BCG strains were able to induce an effective cellular immune response and, through epigenetic modifications, activate cells of the innate immune system, such as monocytes, macrophages and natural killer cells, which are crucial for the control of viral infections. Although several vaccines have already been developed and used in an attempt to control the COVID-19 pandemic, some BCG vaccine strains may help stimulate the basal defences against these pathogens and can be used as additional defences in this and future pandemics.

Keywords: BCG, SARS-CoV-2, innate immunity, heterologous vaccine effects, natural killer cells, macrophages, tuberculosis.

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[1]
Zhu, N.; Zhang, D.; Wang, W.; Li, X.; Yang, B.; Song, J.; Zhao, X.; Huang, B.; Shi, W.; Lu, R.; Niu, P.; Zhan, F.; Ma, X.; Wang, D.; Xu, W.; Wu, G.; Gao, G.F.; Tan, W. A novel coronavirus from patients with pneumonia in China, 2019. N. Engl. J. Med., 2020, 382(8), 727-733.
[http://dx.doi.org/10.1056/NEJMoa2001017] [PMID: 31978945]
[2]
Li, T.; Liu, D.; Yang, Y.; Guo, J.; Feng, Y.; Zhang, X.; Cheng, S.; Feng, J. Phylogenetic supertree reveals detailed evolution of SARS-CoV-2. Sci. Rep., 2020, 10(1), 22366.
[http://dx.doi.org/10.1038/s41598-020-79484-8] [PMID: 33353955]
[3]
Huang, C.; Wang, Y.; Li, X.; Ren, L.; Zhao, J.; Hu, Y.; Zhang, L.; Fan, G.; Xu, J.; Gu, X.; Cheng, Z.; Yu, T.; Xia, J.; Wei, Y.; Wu, W.; Xie, X.; Yin, W.; Li, H.; Liu, M.; Xiao, Y.; Gao, H.; Guo, L.; Xie, J.; Wang, G.; Jiang, R.; Gao, Z.; Jin, Q.; Wang, J.; Cao, B. Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. Lancet, 2020, 395(10223), 497-506.
[http://dx.doi.org/10.1016/S0140-6736(20)30183-5] [PMID: 31986264]
[4]
La Rosa, G.; Mancini, P.; Bonanno Ferraro, G.; Veneri, C.; Iaconelli, M.; Lucentini, L.; Bonadonna, L.; Brusaferro, S.; Brandtner, D.; Fa-sanella, A.; Pace, L.; Parisi, A.; Galante, D.; Suffredini, E. Rapid screening for SARS-CoV-2 variants of concern in clinical and environ-mental samples using nested RT-PCR assays targeting key mutations of the spike protein. Water Res., 2021, 197, 117104.
[http://dx.doi.org/10.1016/j.watres.2021.117104] [PMID: 33857895]
[5]
Lotfi, M.; Hamblin, M.R.; Rezaei, N. COVID-19: Transmission, prevention and potential therapeutic opportunities. Clin. Chim. Acta, 2020, 508, 254-266.
[http://dx.doi.org/10.1016/j.cca.2020.05.044] [PMID: 32474009]
[6]
World Health Organization. BCG vaccine. 2021. Available from: https://www.who.int/teams/health-product-policy-and-standards/standards-and-specifications/vaccines-quality/bcg [cited 2021 Aug 3].
[7]
Netea, M.G.; Domínguez-Andrés, J.; Barreiro, L.B.; Chavakis, T.; Divangahi, M.; Fuchs, E.; Joosten, L.A.B.; van der Meer, J.W.M.; Mhlanga, M.M.; Mulder, W.J.M.; Riksen, N.P.; Schlitzer, A.; Schultze, J.L.; Stabell Benn, C.; Sun, J.C.; Xavier, R.J.; Latz, E. Defining trai-ned immunity and its role in health and disease. Nat. Rev. Immunol., 2020, 20(6), 375-388.
[http://dx.doi.org/10.1038/s41577-020-0285-6] [PMID: 32132681]
[8]
Netea, M.G.; Giamarellos-Bourboulis, E.J.; Domínguez-Andrés, J.; Curtis, N.; van Crevel, R.; van de Veerdonk, F.L.; Bonten, M. Trained immunity: A tool for reducing susceptibility to and the severity of SARS-CoV-2 infection. Cell, 2020, 181(5), 969-977.
[http://dx.doi.org/10.1016/j.cell.2020.04.042] [PMID: 32437659]
[9]
Kleinnijenhuis, J.; Quintin, J.; Preijers, F.; Joosten, L.A.B.; Ifrim, D.C.; Saeed, S.; Jacobs, C.; van Loenhout, J.; de Jong, D.; Stunnenberg, H.G.; Xavier, R.J.; van der Meer, J.W.; van Crevel, R.; Netea, M.G. Bacille Calmette-Guerin induces NOD2-dependent nonspecific protec-tion from reinfection via epigenetic reprogramming of monocytes. Proc. Natl. Acad. Sci. USA, 2012, 109(43), 17537-17542.
[http://dx.doi.org/10.1073/pnas.1202870109] [PMID: 22988082]
[10]
Kleinnijenhuis, J.; Quintin, J.; Preijers, F.; Benn, C.S.; Joosten, L.A.B.; Jacobs, C.; van Loenhout, J.; Xavier, R.J.; Aaby, P.; van der Meer, J.W.; van Crevel, R.; Netea, M.G. Long-lasting effects of BCG vaccination on both heterologous Th1/Th17 responses and innate trained immunity. J. Innate Immun., 2014, 6(2), 152-158.
[http://dx.doi.org/10.1159/000355628] [PMID: 24192057]
[11]
Kleinnijenhuis, J.; Quintin, J.; Preijers, F.; Joosten, L.A.B.; Jacobs, C.; Xavier, R.J.; van der Meer, J.W.; van Crevel, R.; Netea, M.G. BCG-induced trained immunity in NK cells: Role for non-specific protection to infection. Clin. Immunol., 2014, 155(2), 213-219.
[http://dx.doi.org/10.1016/j.clim.2014.10.005] [PMID: 25451159]
[12]
Covián, C.; Fernández-Fierro, A.; Retamal-Díaz, A.; Díaz, F.E.; Vasquez, A.E.; Lay, M.K.; Riedel, C.A.; González, P.A.; Bueno, S.M.; Kalergis, A.M. BCG-induced cross-protection and development of trained immunity: Implication for vaccine design. Front. Immunol., 2019, 10, 2806.
[http://dx.doi.org/10.3389/fimmu.2019.02806] [PMID: 31849980]
[13]
World Health Organization. Global tuberculosis report 2020. 2020. Available from: https://apps.who.int/iris/bitstream/handle/10665/336069/9789240013131-eng.pdf
[14]
Ministério Da Saúde. Secretaria de Vigilância em Saúde. Boletim Epidemiológico - Tuberculose 2021. 2021. Available from: https://www.gov.br/saude/pt-br/media/pdf/2021/marco/24/boletim-tuberculose-2021_24.03 [cited 2021 Sep 2].
[15]
Brasil. Brasil Livre da Tuberculose Plano Nacional pelo Fim da Tuberculose como Problema de Saúde Pública. 2017. Available from: http://bvsms.saude.gov.br/bvs/publicacoes/brasil_livre_tuberculose_plano_nacional.pdf
[16]
Abdallah, A.M.; Hill-Cawthorne, G.A.; Otto, T.D.; Coll, F.; Guerra-Assunção, J.A.; Gao, G.; Naeem, R.; Ansari, H.; Malas, T.B.; Adroub, S.A.; Verboom, T.; Ummels, R.; Zhang, H.; Panigrahi, A.K.; McNerney, R.; Brosch, R.; Clark, T.G.; Behr, M.A.; Bitter, W.; Pain, A. Ge-nomic expression catalogue of a global collection of BCG vaccine strains show evidence for highly diverged metabolic and cell-wall adap-tations. Sci. Rep., 2015, 5(1), 15443.
[http://dx.doi.org/10.1038/srep15443] [PMID: 26487098]
[17]
Abdallah, A.M.; Behr, M.A. Evolution and strain variation in BCG., 2017, 155-169. Available from: http://link.springer.com/10.1007/978-3-319-64371-78
[http://dx.doi.org/10.1007/978-3-319-64371-7_8]
[18]
Ritz, N.; Curtis, N. Mapping the global use of different BCG vaccine strains. Tuberculosis (Edinb.), 2009, 89(4), 248-251.
[http://dx.doi.org/10.1016/j.tube.2009.03.002] [PMID: 19540166]
[19]
Zhang, W.; Zhang, Y.; Zheng, H.; Pan, Y.; Liu, H.; Du, P.; Wan, L.; Liu, J.; Zhu, B.; Zhao, G.; Chen, C.; Wan, K. Genome sequencing and analysis of BCG vaccine strains. PLoS One, 2013, 8(8), e71243.
[http://dx.doi.org/10.1371/journal.pone.0071243] [PMID: 23977002]
[20]
Joung, S.M.; Ryoo, S. BCG vaccine in Korea. Clin. Exp. Vaccine Res., 2013, 2(2), 83-91.
[http://dx.doi.org/10.7774/cevr.2013.2.2.83] [PMID: 23858398]
[21]
Orduña, P.; Cevallos, M.A.; de León, S.P.; Arvizu, A.; Hernández-González, I.L.; Mendoza-Hernández, G.; López-Vidal, Y. Genomic and proteomic analyses of Mycobacterium bovis BCG Mexico 1931 reveal a diverse immunogenic repertoire against tuberculosis infection. BMC Genomics, 2011, 12(1), 493.
[http://dx.doi.org/10.1186/1471-2164-12-493] [PMID: 21981907]
[22]
Brosch, R.; Gordon, S.V.; Garnier, T.; Eiglmeier, K.; Frigui, W.; Valenti, P.; Dos Santos, S.; Duthoy, S.; Lacroix, C.; Garcia-Pelayo, C.; Inwald, J.K.; Golby, P.; Garcia, J.N.; Hewinson, R.G.; Behr, M.A.; Quail, M.A.; Churcher, C.; Barrell, B.G.; Parkhill, J.; Cole, S.T. Genome plasticity of BCG and impact on vaccine efficacy. Proc. Natl. Acad. Sci. USA, 2007, 104(13), 5596-5601.
[http://dx.doi.org/10.1073/pnas.0700869104] [PMID: 17372194]
[23]
Luca, S.; Mihaescu, T. History of BCG vaccine. Maedica (Buchar.), 2013, 8(1), 53-58. Available from: http://www.ncbi.nlm.nih.gov/pubmed/24023600
[PMID: 24023600]
[24]
World Health Organization. Issues relating to the use of BCG in immunization programmes: A discussion document., 1999. Available from: https://apps.who.int/iris/handle/10665/66120
[25]
Ministério Da Saúde. NOTA INFORMATIVA No 18/2018- CGPNI/DEVIT/SVS/MS. 2021. Available from: http://nhe.fmrp.usp.br/wp-content/uploads/2018/04/NOTA-INFORMATIVA-N
[26]
Aronson, N.E.; Santosham, M.; Comstock, G.W.; Howard, R.S.; Moulton, L.H.; Rhoades, E.R.; Harrison, L.H. Long-term efficacy of BCG vaccine in American Indians and Alaska Natives: A 60-year follow-up study. JAMA, 2004, 291(17), 2086-2091.
[http://dx.doi.org/10.1001/jama.291.17.2086] [PMID: 15126436]
[27]
ICMR TRC Fifteen year follow up of trial of BCG vaccines in south India for tuberculosis prevention. Tuberculosis Research Centre (ICMR), Chennai. Indian J. Med. Res., 1999, 110, 56-69.
[PMID: 10573656]
[28]
Barreto, M.L.; Pereira, S.M.; Pilger, D.; Cruz, A.A.; Cunha, S.S.; Sant’Anna, C.; Ichihara, M.Y.; Genser, B.; Rodrigues, L.C. Evidence of an effect of BCG revaccination on incidence of tuberculosis in school-aged children in Brazil: Second report of the BCG-REVAC cluster-randomised trial. Vaccine, 2011, 29(31), 4875-4877.
[http://dx.doi.org/10.1016/j.vaccine.2011.05.023] [PMID: 21616115]
[29]
Favorov, M.; Ali, M.; Tursunbayeva, A.; Aitmagambetova, I.; Kilgore, P.; Ismailov, S.; Chorba, T. Comparative tuberculosis (TB) preven-tion effectiveness in children of Bacillus Calmette-Guérin (BCG) vaccines from different sources, Kazakhstan. PLoS One, 2012, 7(3), e32567.
[http://dx.doi.org/10.1371/journal.pone.0032567] [PMID: 22427854]
[30]
Velmurugan, K.; Grode, L.; Chang, R.; Fitzpatrick, M.; Laddy, D.; Hokey, D.; Derrick, S.; Morris, S.; McCown, D.; Kidd, R.; Gengenba-cher, M.; Eisele, B.; Kaufmann, S.H.; Fulkerson, J.; Brennan, M.J. Nonclinical development of BCG replacement vaccine candidates. Vaccines (Basel), 2013, 1(2), 120-138.
[http://dx.doi.org/10.3390/vaccines1020120] [PMID: 26343962]
[31]
Hoft, D.F.; Blazevic, A.; Selimovic, A.; Turan, A.; Tennant, J.; Abate, G.; Fulkerson, J.; Zak, D.E.; Walker, R.; McClain, B.; Sadoff, J.; Scott, J.; Shepherd, B.; Ishmukhamedov, J.; Hokey, D.A.; Dheenadhayalan, V.; Shankar, S.; Amon, L.; Navarro, G.; Podyminogin, R.; Aderem, A.; Barker, L.; Brennan, M.; Wallis, R.S.; Gershon, A.A.; Gershon, M.D.; Steinberg, S. Safety and immunogenicity of the recom-binant BCG vaccine AERAS-422 in healthy BCG-naïve adults: A randomized, active-controlled, first-in-human phase 1 trial. Exp. Biol. Med., 2016, 7(May), 278-286.
[http://dx.doi.org/10.1016/j.ebiom.2016.04.010] [PMID: 27322481]
[32]
Marinova, D.; Gonzalo-Asensio, J.; Aguilo, N.; Martin, C. Recent developments in tuberculosis vaccines. Expert Rev. Vaccines, 2013, 12(12), 1431-1448.
[http://dx.doi.org/10.1586/14760584.2013.856765] [PMID: 24195481]
[33]
Grode, L.; Seiler, P.; Baumann, S.; Hess, J.; Brinkmann, V.; Nasser Eddine, A.; Mann, P.; Goosmann, C.; Bandermann, S.; Smith, D.; Ban-croft, G.J.; Reyrat, J.M.; van Soolingen, D.; Raupach, B.; Kaufmann, S.H. Increased vaccine efficacy against tuberculosis of recombinant Mycobacterium bovis Bacille Calmette-Guérin mutants that secrete listeriolysin. J. Clin. Invest., 2005, 115(9), 2472-2479.
[http://dx.doi.org/10.1172/JCI24617] [PMID: 16110326]
[34]
Grode, L.; Ganoza, C.A.; Brohm, C.; Weiner, J., III; Eisele, B.; Kaufmann, S.H.E. Safety and immunogenicity of the recombinant BCG vaccine VPM1002 in a phase 1 open-label randomized clinical trial. Vaccine, 2013, 31(9), 1340-1348.
[http://dx.doi.org/10.1016/j.vaccine.2012.12.053] [PMID: 23290835]
[35]
Farinacci, M.; Weber, S.; Kaufmann, S.H.E. The recombinant tuberculosis vaccine rBCG ΔureC: hly(+) induces apoptotic vesicles for improved priming of CD4(+) and CD8(+) T cells. Vaccine, 2012, 30(52), 7608-7614.
[http://dx.doi.org/10.1016/j.vaccine.2012.10.031] [PMID: 23088886]
[36]
Nieuwenhuizen, N.E.; Kaufmann, S.H.E. Next-Generation vaccines based on bacille Calmette-Guérin. Front. Immunol., 2018, 9, 121.
[http://dx.doi.org/10.3389/fimmu.2018.00121] [PMID: 29459859]
[37]
Kaufmann, S.H.E. EFIS lecture. Immune response to tuberculosis: How to control the most successful pathogen on earth. Immunol. Lett., 2016, 175, 50-57.
[http://dx.doi.org/10.1016/j.imlet.2016.05.006] [PMID: 27181094]
[38]
Loxton, A.G.; Knaul, J.K.; Grode, L.; Gutschmidt, A.; Meller, C.; Eisele, B.; Johnstone, H.; van der Spuy, G.; Maertzdorf, J.; Kaufmann, S.H.E.; Hesseling, A.C.; Walzl, G.; Cotton, M.F. Safety and immunogenicity of the recombinant Mycobacterium bovis BCG vaccine VPM1002 in HIV-unexposed newborn infants in South Africa. Clin. Vaccine Immunol., 2017, 24(2), e00439-e16.
[http://dx.doi.org/10.1128/CVI.00439-16] [PMID: 27974398]
[39]
Nieuwenhuizen, N.E.; Kulkarni, P.S.; Shaligram, U.; Cotton, M.F.; Rentsch, C.A.; Eisele, B.; Grode, L.; Kaufmann, S.H.E. The recombi-nant Bacille Calmette-Guérin vaccine VPM1002: Ready for clinical efficacy testing. Front. Immunol., 2017, 8, 1147.
[http://dx.doi.org/10.3389/fimmu.2017.01147] [PMID: 28974949]
[40]
Brazier, B.; McShane, H. Towards new TB vaccines. Semin. Immunopathol., 2020, 42(3), 315-331.
[http://dx.doi.org/10.1007/s00281-020-00794-0] [PMID: 32189035]
[41]
Lucas, C.; Wong, P.; Klein, J.; Castro, T.B.R.; Silva, J.; Sundaram, M.; Ellingson, M.K.; Mao, T.; Oh, J.E.; Israelow, B.; Takahashi, T.; Tokuyama, M.; Lu, P.; Venkataraman, A.; Park, A.; Mohanty, S.; Wang, H.; Wyllie, A.L.; Vogels, C.B.F.; Earnest, R.; Lapidus, S.; Ott, I.M.; Moore, A.J.; Muenker, M.C.; Fournier, J.B.; Campbell, M.; Odio, C.D.; Casanovas-Massana, A.; Herbst, R.; Shaw, A.C.; Medzhitov, R.; Schulz, W.L.; Grubaugh, N.D.; Dela Cruz, C.; Farhadian, S.; Ko, A.I.; Omer, S.B.; Iwasaki, A. Longitudinal analyses reveal immunolo-gical misfiring in severe COVID-19. Nature, 2020, 584(7821), 463-469.
[http://dx.doi.org/10.1038/s41586-020-2588-y] [PMID: 32717743]
[42]
Giamarellos-Bourboulis, E.J.; Netea, M.G.; Rovina, N.; Akinosoglou, K.; Antoniadou, A.; Antonakos, N.; Damoraki, G.; Gkavogianni, T.; Adami, M.E.; Katsaounou, P.; Ntaganou, M.; Kyriakopoulou, M.; Dimopoulos, G.; Koutsodimitropoulos, I.; Velissaris, D.; Koufargyris, P.; Karageorgos, A.; Katrini, K.; Lekakis, V.; Lupse, M.; Kotsaki, A.; Renieris, G.; Theodoulou, D.; Panou, V.; Koukaki, E.; Koulouris, N.; Gogos, C.; Koutsoukou, A. Complex immune dysregulation in COVID-19 patients with severe respiratory failure. Cell Host Microbe, 2020, 27(6), 992-1000.
[http://dx.doi.org/10.1016/j.chom.2020.04.009] [PMID: 32320677]
[43]
Gupta, S.; Hayek, S.S.; Wang, W.; Chan, L.; Mathews, K.S.; Melamed, M.L.; Brenner, S.K.; Leonberg-Yoo, A.; Schenck, E.J.; Radbel, J.; Reiser, J.; Bansal, A.; Srivastava, A.; Zhou, Y.; Sutherland, A.; Green, A.; Shehata, A.M.; Goyal, N.; Vijayan, A.; Velez, J.C.Q.; Shaefi, S.; Parikh, C.R.; Arunthamakun, J.; Athavale, A.M.; Friedman, A.N.; Short, S.A.P.; Kibbelaar, Z.A.; Abu Omar, S.; Admon, A.J.; Donnelly, J.P.; Gershengorn, H.B.; Hernán, M.A.; Semler, M.W.; Leaf, D.E. Factors associated with death in critically ill patients with coronavirus disease 2019 in the uS. JAMA Intern. Med., 2020, 180(11), 1436-1447.
[http://dx.doi.org/10.1001/jamainternmed.2020.3596] [PMID: 32667668]
[44]
Qin, C.; Zhou, L.; Hu, Z.; Zhang, S.; Yang, S.; Tao, Y.; Xie, C.; Ma, K.; Shang, K.; Wang, W.; Tian, D.S. Dysregulation of immune respon-se in patients with coronavirus 2019 (COVID-19) in Wuhan, China. Clin. Infect. Dis., 2020, 71(15), 762-768.
[http://dx.doi.org/10.1093/cid/ciaa248] [PMID: 32161940]
[45]
Quan, C.; Li, C.; Ma, H.; Li, Y.; Zhang, H. Immunopathogenesis of coronavirus-induced Acute Respiratory Distress Syndrome (ARDS): Potential infection-associated hemophagocytic lymphohistiocytosis. Clin. Microbiol. Rev., 2020, 34(1), e00074-e20.
[http://dx.doi.org/10.1128/CMR.00074-20] [PMID: 33055229]
[46]
Wang, J.; Jiang, M.; Chen, X.; Montaner, L.J. Cytokine storm and leukocyte changes in mild versus severe SARS-CoV-2 infection: Review of 3939 COVID-19 patients in China and emerging pathogenesis and therapy concepts. J. Leukoc. Biol., 2020, 108(1), 17-41.
[http://dx.doi.org/10.1002/JLB.3COVR0520-272R] [PMID: 32534467]
[47]
Zhang, L.; Jackson, C.B.; Mou, H.; Ojha, A.; Peng, H.; Quinlan, B.D.; Rangarajan, E.S.; Pan, A.; Vanderheiden, A.; Suthar, M.S.; Li, W.; Izard, T.; Rader, C.; Farzan, M.; Choe, H. SARS-CoV-2 spike-protein D614G mutation increases virion spike density and infectivity. Nat. Commun., 2020, 11(1), 6013.
[http://dx.doi.org/10.1038/s41467-020-19808-4] [PMID: 33243994]
[48]
Arya, R.; Kumari, S.; Pandey, B.; Mistry, H.; Bihani, S.C.; Das, A.; Prashar, V.; Gupta, G.D.; Panicker, L.; Kumar, M. Structural insights into SARS-CoV-2 proteins. J. Mol. Biol., 2021, 433(2), 166725.
[http://dx.doi.org/10.1016/j.jmb.2020.11.024] [PMID: 33245961]
[49]
Thoms, M.; Buschauer, R.; Ameismeier, M.; Koepke, L.; Denk, T.; Hirschenberger, M. Structural basis for translational shutdown and immune evasion by the Nsp1 protein of SARS-CoV-2. Science, 2020, 369(6508), 1249-1255.
[50]
Osman, M.; Faridi, R.M.; Sligl, W.; Shabani-Rad, M-T.; Dharmani-Khan, P.; Parker, A.; Kalra, A.; Tripathi, M.B.; Storek, J. Cohen Ter-vaert, J.W.; Khan, F.M. Impaired natural killer cell counts and cytolytic activity in patients with severe COVID-19. Blood Adv., 2020, 4(20), 5035-5039.
[http://dx.doi.org/10.1182/bloodadvances.2020002650] [PMID: 33075136]
[51]
Shah, V.K.; Firmal, P.; Alam, A.; Ganguly, D.; Chattopadhyay, S. Overview of immune response during SARS-CoV-2 infection: Lessons from the past. Front. Immunol., 2020, 11, 1949.
[http://dx.doi.org/10.3389/fimmu.2020.01949] [PMID: 32849654]
[52]
He, R.; Lu, Z.; Zhang, L.; Fan, T.; Xiong, R.; Shen, X.; Feng, H.; Meng, H.; Lin, W.; Jiang, W.; Geng, Q. The clinical course and its correla-ted immune status in COVID-19 pneumonia. J. Clin. Virol., 2020, 127, 104361.
[http://dx.doi.org/10.1016/j.jcv.2020.104361] [PMID: 32344320]
[53]
Jiang, Y.; Wei, X.; Guan, J.; Qin, S.; Wang, Z.; Lu, H.; Qian, J.; Wu, L.; Chen, Y.; Chen, Y.; Lin, X. COVID-19 pneumonia: CD8+ T and NK cells are decreased in number but compensatory increased in cytotoxic potential. Clin. Immunol., 2020, 218(Sep), 108516.
[http://dx.doi.org/10.1016/j.clim.2020.108516] [PMID: 32574709]
[54]
Wang, M-Y.; Zhao, R.; Gao, L-J.; Gao, X-F.; Wang, D-P.; Cao, J-M. SARS-CoV-2: Structure, biology, and structure-based therapeutics development. Front. Cell. Infect. Microbiol., 2020, 10, 587269.
[http://dx.doi.org/10.3389/fcimb.2020.587269] [PMID: 33324574]
[55]
Xu, Z.; Shi, L.; Wang, Y.; Zhang, J.; Huang, L.; Zhang, C.; Liu, S.; Zhao, P.; Liu, H.; Zhu, L.; Tai, Y.; Bai, C.; Gao, T.; Song, J.; Xia, P.; Dong, J.; Zhao, J.; Wang, F.S. Pathological findings of COVID-19 associated with acute respiratory distress syndrome. Lancet Respir. Med., 2020, 8(4), 420-422.
[http://dx.doi.org/10.1016/S2213-2600(20)30076-X] [PMID: 32085846]
[56]
Bordoni, V.; Sacchi, A.; Cimini, E.; Notari, S.; Grassi, G.; Tartaglia, E.; Casetti, R.; Giancola, M.L.; Bevilacqua, N.; Maeurer, M.; Zumla, A.; Locatelli, F.; De Benedetti, F.; Palmieri, F.; Marchioni, L.; Capobianchi, M.R.; D’Offizi, G.; Petrosillo, N.; Antinori, A.; Nicastri, E.; Ip-polito, G.; Agrati, C. An inflammatory profile correlates with decreased frequency of cytotoxic cells in coronavirus disease 2019. Clin. Infect. Dis., 2020, 71(16), 2272-2275.
[http://dx.doi.org/10.1093/cid/ciaa577] [PMID: 32407466]
[57]
Bao, C.; Tao, X.; Cui, W.; Hao, Y.; Zheng, S.; Yi, B.; Pan, T.; Young, K.H.; Qian, W. Natural killer cells associated with SARS-CoV-2 viral RNA shedding, antibody response and mortality in COVID-19 patients. Exp. Hematol. Oncol., 2021, 10(1), 5.
[http://dx.doi.org/10.1186/s40164-021-00199-1] [PMID: 33504359]
[58]
Ritz, N.; Hanekom, W.A.; Robins-Browne, R.; Britton, W.J.; Curtis, N. Influence of BCG vaccine strain on the immune response and pro-tection against tuberculosis. FEMS Microbiol. Rev., 2008, 32(5), 821-841.
[http://dx.doi.org/10.1111/j.1574-6976.2008.00118.x] [PMID: 18616602]
[59]
Davids, V.; Hanekom, W.A.; Mansoor, N.; Gamieldien, H.; Gelderbloem, S.J.; Hawkridge, A.; Hussey, G.D.; Hughes, E.J.; Soler, J.; Mu-rray, R.A.; Ress, S.R.; Kaplan, G. The effect of bacille Calmette-Guérin vaccine strain and route of administration on induced immune res-ponses in vaccinated infants. J. Infect. Dis., 2006, 193(4), 531-536.
[http://dx.doi.org/10.1086/499825] [PMID: 16425132]
[60]
Castro-Rodriguez, J.A.; Mallol, J.; Andrade, R.; Muñoz, M.; Azzini, I. Comparison of tuberculin skin test response after three modalities of neonatal BCG vaccination. Trans. R. Soc. Trop. Med. Hyg., 2007, 101(5), 493-496.
[http://dx.doi.org/10.1016/j.trstmh.2006.08.003] [PMID: 16997338]
[61]
Roth, A.; Sodemann, M.; Jensen, H.; Poulsen, A.; Gustafson, P.; Gomes, J.; Djana, Q.; Jakobsen, M.; Garly, M.L.; Rodrigues, A.; Aaby, P. Vaccination technique, PPD reaction and BCG scarring in a cohort of children born in Guinea-Bissau 2000-2002. Vaccine, 2005, 23(30), 3991-3998.
[http://dx.doi.org/10.1016/j.vaccine.2004.10.022] [PMID: 15899539]
[62]
Guérin, N.; Teulières, L.; Noba, A.; Schlumberger, M.; Bregère, P.; Chauvin, P. Comparison of the safety and immunogenicity of the lyop-hilized Mérieux seed and the World Health Organization working reference BCG vaccines in school-aged children in Senegal. Vaccine, 1999, 17(2), 105-109.
[http://dx.doi.org/10.1016/S0264-410X(98)00186-8] [PMID: 9987142]
[63]
Suciliene, E.; Rønne, T.; Plesner, A.M.; Semenaite, B.; Slapkauskaite, D.; Larsen, S.O.; Hasløv, K. Infant BCG vaccination study in Lithuania. Int. J. Tuberc. Lung Dis., 1999, 3(11), 956-961.
[PMID: 10587317]
[64]
Prezzemolo, T.; Guggino, G.; La Manna, M.P.; Di Liberto, D.; Dieli, F.; Caccamo, N. Functional signatures of human CD4 and CD8 T cell responses to Mycobacterium tuberculosis. Front. Immunol., 2014, 5, 180.
[http://dx.doi.org/10.3389/fimmu.2014.00180] [PMID: 24795723]
[65]
Soares, A.P.; Scriba, T.J.; Joseph, S.; Harbacheuski, R.; Murray, R.A.; Gelderbloem, S.J.; Hawkridge, A.; Hussey, G.D.; Maecker, H.; Kaplan, G.; Hanekom, W.A. Bacillus Calmette-Guérin vaccination of human newborns induces T cells with complex cytokine and pheno-typic profiles. J. Immunol., 2008, 180(5), 3569-3577.
[http://dx.doi.org/10.4049/jimmunol.180.5.3569] [PMID: 18292584]
[66]
Soares, A.P.; Kwong Chung, C.K.C.; Choice, T.; Hughes, E.J.; Jacobs, G.; van Rensburg, E.J.; Khomba, G.; de Kock, M.; Lerumo, L.; Makhethe, L.; Maneli, M.H.; Pienaar, B.; Smit, E.; Tena-Coki, N.G.; van Wyk, L.; Boom, W.H.; Kaplan, G.; Scriba, T.J.; Hanekom, W.A. Longitudinal changes in CD4(+) T-cell memory responses induced by BCG vaccination of newborns. J. Infect. Dis., 2013, 207(7), 1084-1094.
[http://dx.doi.org/10.1093/infdis/jis941] [PMID: 23293360]
[67]
Kiravu, A.; Osawe, S.; Happel, A-U.; Nundalall, T.; Wendoh, J.; Beer, S.; Dontsa, N.; Alinde, O.B.; Mohammed, S.; Datong, P.; Cameron, D.W.; Rosenthal, K.; Abimiku, A.; Jaspan, H.B.; Gray, C.M. Bacille Calmette-Guérin vaccine strain modulates the ontogeny of both myco-bacterial-specific and heterologous t cell immunity to vaccination in infants. Front. Immunol., 2019, 10, 2307.
[http://dx.doi.org/10.3389/fimmu.2019.02307] [PMID: 31649662]
[68]
Kagina, B.M.N.; Abel, B.; Scriba, T.J.; Hughes, E.J.; Keyser, A.; Soares, A.; Gamieldien, H.; Sidibana, M.; Hatherill, M.; Gelderbloem, S.; Mahomed, H.; Hawkridge, A.; Hussey, G.; Kaplan, G.; Hanekom, W.A. Specific T cell frequency and cytokine expression profile do not correlate with protection against tuberculosis after bacillus Calmette-Guérin vaccination of newborns. Am. J. Respir. Crit. Care Med., 2010, 182(8), 1073-1079.
[http://dx.doi.org/10.1164/rccm.201003-0334OC] [PMID: 20558627]
[69]
Darboe, F.; Adetifa, J.U.; Reynolds, J.; Hossin, S.; Plebanski, M.; Netea, M.G.; Rowland-Jones, S.L.; Sutherland, J.S.; Flanagan, K.L. Mi-nimal sex-differential modulation of reactivity to pathogens and toll-like receptor ligands following infant Bacillus Calmette-Guérin Russia vaccination. Front. Immunol., 2017, 8, 1092.
[http://dx.doi.org/10.3389/fimmu.2017.01092] [PMID: 28951731]
[70]
Djuardi, Y.; Sartono, E.; Wibowo, H.; Supali, T.; Yazdanbakhsh, M. Correction: A Longitudinal Study of BCG Vaccination in Early Childhood: The Development of Innate and Adaptive Immune Responses. PLoS One, 2013, 8(12), 10.
[http://dx.doi.org/10.1371/annotation/81a1f333-7fb3-4afd-b158-94774d5522fa]
[71]
Jensen, K.J.; Larsen, N.; Biering-Sørensen, S.; Andersen, A.; Eriksen, H.B.; Monteiro, I.; Hougaard, D.; Aaby, P.; Netea, M.G.; Flanagan, K.L.; Benn, C.S. Heterologous immunological effects of early BCG vaccination in low-birth-weight infants in Guinea-Bissau: A randomi-zed-controlled trial. J. Infect. Dis., 2015, 211(6), 956-967.
[http://dx.doi.org/10.1093/infdis/jiu508] [PMID: 25210141]
[72]
Ritz, N.; Dutta, B.; Donath, S.; Casalaz, D.; Connell, T.G.; Tebruegge, M.; Robins-Browne, R.; Hanekom, W.A.; Britton, W.J.; Curtis, N. The influence of bacille Calmette-Guerin vaccine strain on the immune response against tuberculosis: A randomized trial. Am. J. Respir. Crit. Care Med., 2012, 185(2), 213-222.
[http://dx.doi.org/10.1164/rccm.201104-0714OC] [PMID: 22071384]
[73]
Anderson, E.J.; Webb, E.L.; Mawa, P.A.; Kizza, M.; Lyadda, N.; Nampijja, M.; Elliott, A.M. The influence of BCG vaccine strain on my-cobacteria-specific and non-specific immune responses in a prospective cohort of infants in Uganda. Vaccine, 2012, 30(12), 2083-2089.
[http://dx.doi.org/10.1016/j.vaccine.2012.01.053] [PMID: 22300718]
[74]
Wu, B.; Huang, C.; Garcia, L.; Ponce de Leon, A.; Osornio, J.S.; Bobadilla-del-Valle, M.; Ferreira, L.; Canizales, S.; Small, P.; Kato-Maeda, M.; Krensky, A.M.; Clayberger, C. Unique gene expression profiles in infants vaccinated with different strains of Mycobacterium bovis bacille Calmette-Guerin. Infect. Immun., 2007, 75(7), 3658-3664.
[http://dx.doi.org/10.1128/IAI.00244-07] [PMID: 17502394]
[75]
Gorak-Stolinska, P.; Weir, R.E.; Floyd, S.; Lalor, M.K.; Stenson, S.; Branson, K.; Blitz, R.; Luke, S.; Nazareth, B.; Ben-Smith, A.; Fine, P.E.; Dockrell, H.M. Immunogenicity of Danish-SSI 1331 BCG vaccine in the UK: Comparison with Glaxo-Evans 1077 BCG vaccine. Vaccine, 2006, 24(29-30), 5726-5733.
[http://dx.doi.org/10.1016/j.vaccine.2006.04.037] [PMID: 16723176]
[76]
Di Vito, C.; Mikulak, J.; Mavilio, D. On the way to become a natural killer cell. Front. Immunol., 2019, 10, 1812.
[http://dx.doi.org/10.3389/fimmu.2019.01812] [PMID: 31428098]
[77]
Madera, S.; Rapp, M.; Firth, M.A.; Beilke, J.N.; Lanier, L.L.; Sun, J.C. Type I IFN promotes NK cell expansion during viral infection by protecting NK cells against fratricide. J. Exp. Med., 2016, 213(2), 225-233.
[http://dx.doi.org/10.1084/jem.20150712] [PMID: 26755706]
[78]
Li, Y.; Wang, J.; Yin, J.; Liu, X.; Yu, M.; Li, T.; Yan, H.; Wang, X. Chromatin state dynamics during NK cell activation. Oncotarget, 2017, 8(26), 41854-41865.
[http://dx.doi.org/10.18632/oncotarget.16688] [PMID: 28402957]
[79]
Sun, J.C.; Madera, S.; Bezman, N.A.; Beilke, J.N.; Kaplan, M.H.; Lanier, L.L. Proinflammatory cytokine signaling required for the genera-tion of natural killer cell memory. J. Exp. Med., 2012, 209(5), 947-954.
[http://dx.doi.org/10.1084/jem.20111760] [PMID: 22493516]
[80]
Dokun, A.O.; Kim, S.; Smith, H.R.; Kang, H.S.; Chu, D.T.; Yokoyama, W.M. Specific and nonspecific NK cell activation during virus infection. Nat. Immunol., 2001, 2(10), 951-956.
[http://dx.doi.org/10.1038/ni714] [PMID: 11550009]
[81]
Sun, J.C.; Beilke, J.N.; Lanier, L.L. Adaptive immune features of natural killer cells. Nature, 2009, 457(7229), 557-561.
[http://dx.doi.org/10.1038/nature07665] [PMID: 19136945]
[82]
Lau, C.M.; Adams, N.M.; Geary, C.D.; Weizman, O-E.; Rapp, M.; Pritykin, Y.; Leslie, C.S.; Sun, J.C. Epigenetic control of innate and adaptive immune memory. Nat. Immunol., 2018, 19(9), 963-972.
[http://dx.doi.org/10.1038/s41590-018-0176-1] [PMID: 30082830]
[83]
Gumá, M.; Angulo, A.; Vilches, C.; Gómez-Lozano, N.; Malats, N.; López-Botet, M. Imprint of human cytomegalovirus infection on the NK cell receptor repertoire. Blood, 2004, 104(12), 3664-3671.
[http://dx.doi.org/10.1182/blood-2004-05-2058] [PMID: 15304389]
[84]
Misale, M.S.; Witek Janusek, L.; Tell, D.; Mathews, H.L. Chromatin organization as an indicator of glucocorticoid induced natural killer cell dysfunction. Brain Behav. Immun., 2018, 67, 279-289.
[http://dx.doi.org/10.1016/j.bbi.2017.09.004] [PMID: 28911980]
[85]
Schlums, H.; Cichocki, F.; Tesi, B.; Theorell, J.; Beziat, V.; Holmes, T.D.; Han, H.; Chiang, S.C.; Foley, B.; Mattsson, K.; Larsson, S.; Schaffer, M.; Malmberg, K.J.; Ljunggren, H.G.; Miller, J.S.; Bryceson, Y.T. Cytomegalovirus infection drives adaptive epigenetic diversifi-cation of NK cells with altered signaling and effector function. Immunity, 2015, 42(3), 443-456.
[http://dx.doi.org/10.1016/j.immuni.2015.02.008] [PMID: 25786176]
[86]
Luetke-Eversloh, M.; Cicek, B.B.; Siracusa, F.; Thom, J.T.; Hamann, A.; Frischbutter, S.; Baumgrass, R.; Chang, H.D.; Thiel, A.; Dong, J.; Romagnani, C. NK cells gain higher IFN-γ competence during terminal differentiation. Eur. J. Immunol., 2014, 44(7), 2074-2084.
[http://dx.doi.org/10.1002/eji.201344072] [PMID: 24752800]
[87]
García-Cuesta, E.M.; Esteso, G.; Ashiru, O.; López-Cobo, S.; Álvarez-Maestro, M.; Linares, A.; Ho, M.M.; Martínez-Piñeiro, L.; T. Rey-burn, H.; Valés-Gómez, M. Characterization of a human anti-tumoral NK cell population expanded after BCG treatment of leukocytes. OncoImmunology, 2017, 6(4), e1293212.
[http://dx.doi.org/10.1080/2162402X.2017.1293212] [PMID: 28507799]
[88]
Arts, R.J.W.; Moorlag, S.J.C.F.M.; Novakovic, B.; Li, Y.; Wang, S-Y.; Oosting, M.; Kumar, V.; Xavier, R.J.; Wijmenga, C.; Joosten, L.A.B.; Reusken, C.B.E.M.; Benn, C.S.; Aaby, P.; Koopmans, M.P.; Stunnenberg, H.G.; van Crevel, R.; Netea, M.G. BCG vaccination protects against experimental viral infection in humans through the induction of cytokines associated with trained immunity. Cell Host Microbe, 2018, 23(1), 89-100.
[http://dx.doi.org/10.1016/j.chom.2017.12.010] [PMID: 29324233]
[89]
Suliman, S.; Geldenhuys, H.; Johnson, J.L.; Hughes, J.E.; Smit, E.; Murphy, M.; Toefy, A.; Lerumo, L.; Hopley, C.; Pienaar, B.; Chheng, P.; Nemes, E.; Hoft, D.F.; Hanekom, W.A.; Boom, W.H.; Hatherill, M.; Scriba, T.J. Bacillus Calmette-Guérin (BCG) revaccination of adults with latent Mycobacterium tuberculosis infection induces long-lived BCG-Reactive NK cell responses. J. Immunol., 2016, 197(4), 1100-1110.
[http://dx.doi.org/10.4049/jimmunol.1501996] [PMID: 27412415]
[90]
Hammer, Q.; Romagnani, C. About Training and Memory: NK-Cell Adaptation to Viral Infections. Adv. Immunol., 2017, 133, 171-207.
[http://dx.doi.org/10.1016/bs.ai.2016.10.001] [PMID: 28215279]
[91]
Bernatowska, E.; Skomska-Pawliszak, M. Wolska-Kuśnierz, B.; Pac, M.; Heropolitanska-Pliszka, E.; Pietrucha, B.; Bernat-Sitarz, K.; Dąbrowska-Leonik, N.; Bohynikova, N.; Piątosa, B.; Lutyńska, A.; Augustynowicz, E.; Augustynowicz-Kopeć, E.; Korzeniewska- Koseła, M.; Krasińska, M.; Krzysztopa-Grzybowska, K.; Wieteska- Klimczak, A.; Książyk, J.; Jackowska, T.; van den Burg, M.; van Dongen, J.J.M.; Casanova, J.L.; Picard, C.; Mikołuć, B. BCG Moreau vaccine safety profile and NK cells-double protection against disseminated BCG Infection in retrospective study of BCG vaccination in 52 polish children with severe combined immunodeficiency. J. Clin. Immunol., 2020, 40(1), 138-146.
[http://dx.doi.org/10.1007/s10875-019-00709-1] [PMID: 31749033]
[92]
Cooper, M.A.; Elliott, J.M.; Keyel, P.A.; Yang, L.; Carrero, J.A.; Yokoyama, W.M. Cytokine-induced memory-like natural killer cells. Proc. Natl. Acad. Sci. USA, 2009, 106(6), 1915-1919.
[http://dx.doi.org/10.1073/pnas.0813192106] [PMID: 19181844]
[93]
Romee, R.; Schneider, S.E.; Leong, J.W.; Chase, J.M.; Keppel, C.R.; Sullivan, R.P.; Cooper, M.A.; Fehniger, T.A. Cytokine activation indu-ces human memory-like NK cells. Blood, 2012, 120(24), 4751-4760.
[http://dx.doi.org/10.1182/blood-2012-04-419283] [PMID: 22983442]
[94]
Allen, M.; Bailey, C.; Cahatol, I.; Dodge, L.; Yim, J.; Kassissa, C.; Luong, J.; Kasko, S.; Pandya, S.; Venketaraman, V. Mechanisms of control of Mycobacterium tuberculosis by NK cells: Role of glutathione. Front. Immunol., 2015, 6, 508.
[http://dx.doi.org/10.3389/fimmu.2015.00508] [PMID: 26500648]
[95]
Garand, M.; Goodier, M.; Owolabi, O.; Donkor, S.; Kampmann, B.; Sutherland, J.S. Functional and phenotypic changes of natural killer cells in whole blood during Mycobacterium tuberculosis infection and disease. Front. Immunol., 2018, 9, 257.
[http://dx.doi.org/10.3389/fimmu.2018.00257] [PMID: 29520269]
[96]
Harris, L.D.; Khayumbi, J.; Ongalo, J.; Sasser, L.E.; Tonui, J.; Campbell, A.; Odhiambo, F.H.; Ouma, S.G.; Alter, G.; Gandhi, N.R.; Day, C.L. Distinct human NK cell phenotypes and functional responses to Mycobacterium tuberculosis in adults from TB endemic and non-endemic regions. Front. Cell. Infect. Microbiol., 2020, 10, 120.
[http://dx.doi.org/10.3389/fcimb.2020.00120] [PMID: 32266170]
[97]
Yoneda, T.; Ellner, J.J. CD4(+) T cell and natural killer cell-dependent killing of Mycobacterium tuberculosis by human monocytes. Am. J. Respir. Crit. Care Med., 1998, 158(2), 395-403.
[http://dx.doi.org/10.1164/ajrccm.158.2.9707102] [PMID: 9700112]
[98]
Gabrielli, S.; Ortolani, C.; del Zotto, G.; Luchetti, F.; Canonico, B.; Buccella, F. The memories of NK cells: Innate-adaptive immune intrin-sic crosstalk. J. Immunol. Res., 2016, 2016, 1376595.
[99]
Murray, P.J. Macrophage polarization. Annu. Rev. Physiol., 2017, 79(1), 541-566.
[http://dx.doi.org/10.1146/annurev-physiol-022516-034339] [PMID: 27813830]
[100]
Ying, W.; Lee, Y.S.; Dong, Y.; Seidman, J.S.; Yang, M.; Isaac, R.; Seo, J.B.; Yang, B.H.; Wollam, J.; Riopel, M.; McNelis, J.; Glass, C.K.; Olefsky, J.M.; Fu, W. Expansion of islet-resident macrophages leads to inflammation affecting β cell proliferation and function in obesity. Cell Metab., 2019, 29(2), 457-474.e5.
[http://dx.doi.org/10.1016/j.cmet.2018.12.003] [PMID: 30595478]
[101]
Colegio, O.R.; Chu, N-Q.; Szabo, A.L.; Chu, T.; Rhebergen, A.M.; Jairam, V.; Cyrus, N.; Brokowski, C.E.; Eisenbarth, S.C.; Phillips, G.M.; Cline, G.W.; Phillips, A.J.; Medzhitov, R. Functional polarization of tumour-associated macrophages by tumour-derived lactic acid. Nature, 2014, 513(7519), 559-563.
[http://dx.doi.org/10.1038/nature13490] [PMID: 25043024]
[102]
Kumar, A.; Das, S.; Mandal, A.; Verma, S.; Abhishek, K.; Kumar, A.; Kumar, V.; Ghosh, A.K.; Das, P. Leishmania infection activates host mTOR for its survival by M2 macrophage polarization. Parasite Immunol., 2018, 40(11), e12586.
[http://dx.doi.org/10.1111/pim.12586] [PMID: 30187512]
[103]
Lee, Y.G.; Jeong, J.J.; Nyenhuis, S.; Berdyshev, E.; Chung, S.; Ranjan, R.; Karpurapu, M.; Deng, J.; Qian, F.; Kelly, E.A.; Jarjour, N.N.; Ackerman, S.J.; Natarajan, V.; Christman, J.W.; Park, G.Y. Recruited alveolar macrophages, in response to airway epithelial-derived mo-nocyte chemoattractant protein 1/CCl2, regulate airway inflammation and remodeling in allergic asthma. Am. J. Respir. Cell Mol. Biol., 2015, 52(6), 772-784.
[http://dx.doi.org/10.1165/rcmb.2014-0255OC] [PMID: 25360868]
[104]
Cai, Y.; Sugimoto, C.; Arainga, M.; Alvarez, X.; Didier, E.S.; Kuroda, M.J. In vivo characterization of alveolar and interstitial lung macrop-hages in rhesus macaques: Implications for understanding lung disease in humans. J. Immunol., 2014, 192(6), 2821-2829.
[http://dx.doi.org/10.4049/jimmunol.1302269] [PMID: 24534529]
[105]
Boyette, L.B.; Macedo, C.; Hadi, K.; Elinoff, B.D.; Walters, J.T.; Ramaswami, B.; Chalasani, G.; Taboas, J.M.; Lakkis, F.G.; Metes, D.M. Phenotype, function, and differentiation potential of human monocyte subsets. PLoS One, 2017, 12(4), e0176460.
[http://dx.doi.org/10.1371/journal.pone.0176460] [PMID: 28445506]
[106]
Kapellos, T.S.; Bonaguro, L.; Gemünd, I.; Reusch, N.; Saglam, A.; Hinkley, E.R.; Schultze, J.L. Human monocyte subsets and phenotypes in major chronic inflammatory diseases. Front. Immunol., 2019, 10, 2035.
[http://dx.doi.org/10.3389/fimmu.2019.02035] [PMID: 31543877]
[107]
Castaño, D.; García, L.F.; Rojas, M. Increased frequency and cell death of CD16+ monocytes with Mycobacterium tuberculosis infection. Tuberculosis (Edinb.), 2011, 91(5), 348-360.
[http://dx.doi.org/10.1016/j.tube.2011.04.002] [PMID: 21621464]
[108]
Cirovic, B.; de Bree, L.C.J.; Groh, L.; Blok, B.A.; Chan, J.; van der Velden, W.J.F.M.; Bremmers, M.E.J.; van Crevel, R.; Händler, K.; Pice-lli, S.; Schulte-Schrepping, J.; Klee, K.; Oosting, M.; Koeken, V.A.C.M.; van Ingen, J.; Li, Y.; Benn, C.S.; Schultze, J.L.; Joosten, L.A.B.; Curtis, N.; Netea, M.G.; Schlitzer, A. BCG vaccination in humans elicits trained immunity via the hematopoietic progenitor compartment. Cell Host Microbe, 2020, 28(2), 322-334.e5.
[http://dx.doi.org/10.1016/j.chom.2020.05.014] [PMID: 32544459]
[109]
Arts, R.J.W.; Carvalho, A.; La Rocca, C.; Palma, C.; Rodrigues, F.; Silvestre, R.; Kleinnijenhuis, J.; Lachmandas, E.; Gonçalves, L.G.; Be-linha, A.; Cunha, C.; Oosting, M.; Joosten, L.A.B.; Matarese, G.; van Crevel, R.; Netea, M.G. Immunometabolic pathways in BCG-induced trained immunity. Cell Rep., 2016, 17(10), 2562-2571.
[http://dx.doi.org/10.1016/j.celrep.2016.11.011] [PMID: 27926861]
[110]
Bekkering, S.; Arts, R.J.W.; Novakovic, B.; Kourtzelis, I.; van der Heijden, C.D.C.C.; Li, Y.; Popa, C.D.; Ter Horst, R.; van Tuijl, J.; Netea-Maier, R.T.; van de Veerdonk, F.L.; Chavakis, T.; Joosten, L.A.B.; van der Meer, J.W.M.; Stunnenberg, H.; Riksen, N.P.; Netea, M.G. Me-tabolic induction of trained immunity through the mevalonate pathway. Cell, 2018, 172(1-2), 135-146.
[http://dx.doi.org/10.1016/j.cell.2017.11.025] [PMID: 29328908]
[111]
Saeed, S.; Quintin, J.; Kerstens, H.H.D.; Rao, N.A.; Aghajanirefah, A.; Matarese, F. Epigenetic programming of monocyte-to-macrophage diffe-rentiation and trained innate immunity. Science, 2014, 345(6204), 1251086.
[http://dx.doi.org/10.1126/science.1251086]
[112]
Michlmayr, D.; Andrade, P.; Gonzalez, K.; Balmaseda, A.; Harris, E. CD14+CD16+ monocytes are the main target of Zika virus infection in peripheral blood mononuclear cells in a paediatric study in Nicaragua. Nat. Microbiol., 2017, 2(11), 1462-1470.
[http://dx.doi.org/10.1038/s41564-017-0035-0] [PMID: 28970482]
[113]
Yoshida, K.; Maekawa, T.; Zhu, Y.; Renard-Guillet, C.; Chatton, B.; Inoue, K.; Uchiyama, T.; Ishibashi, K.; Yamada, T.; Ohno, N.; Shi-rahige, K.; Okada-Hatakeyama, M.; Ishii, S. The transcription factor ATF7 mediates lipopolysaccharide-induced epigenetic changes in ma-crophages involved in innate immunological memory. Nat. Immunol., 2015, 16(10), 1034-1043.
[http://dx.doi.org/10.1038/ni.3257] [PMID: 26322480]
[114]
Quintin, J.; Saeed, S.; Martens, J.H.A.; Giamarellos-Bourboulis, E.J.; Ifrim, D.C.; Logie, C.; Jacobs, L.; Jansen, T.; Kullberg, B.J.; Wijmen-ga, C.; Joosten, L.A.B.; Xavier, R.J.; van der Meer, J.W.M.; Stunnenberg, H.G.; Netea, M.G. Candida albicans infection affords protection against reinfection via functional reprogramming of monocytes. Cell Host Microbe, 2012, 12(2), 223-232.
[http://dx.doi.org/10.1016/j.chom.2012.06.006] [PMID: 22901542]
[115]
Angelidou, A.; Diray-Arce, J.; Conti, M-G.; Netea, M.G.; Blok, B.A.; Liu, M.; Sanchez-Schmitz, G.; Ozonoff, A.; van Haren, S.D.; Levy, O. Human newborn monocytes demonstrate distinct BCG-induced primary and trained innate cytokine production and metabolic activa-tion in vitro. Front. Immunol., 2021, 12, 674334.
[http://dx.doi.org/10.3389/fimmu.2021.674334] [PMID: 34326836]
[116]
Namakula, R.; de Bree, L.C.J. Monocytes from neonates and adults have a similar capacity to adapt their cytokine production after pre-vious exposure to BCG and β-glucan. PLoS One, 2020, 15(2), e0229287.
[117]
Burgos, R.M.; Badowski, M.E.; Drwiega, E.; Ghassemi, S.; Griffith, N.; Herald, F.; Johnson, M.; Smith, R.O.; Michienzi, S.M. The race to a COVID-19 vaccine: Opportunities and challenges in development and distribution. Drugs Context, 2021, 10, 10.
[http://dx.doi.org/10.7573/dic.2020-12-2] [PMID: 33643421]
[118]
World Health Organization. Covid-19 Vaccines. 2021. Available from: 2021.https://www.who.int/emergencies/diseases/novel-coronavirus-2019/covid-19-vaccines
[119]
Aleem, A.; Akbar Samad, A.B.; Slenker, A.K. Emerging Variants of SARS-CoV-2 And Novel Therapeutics Against Coronavirus (COVID-19). StatPearls; StatPearls Publishing: Treasure Island, FL, 2021. Available from: http://www.ncbi.nlm.nih.gov/pubmed/34033342
[120]
Arrais, C.A.; Corcioli, G.; Medina, G da S. The role played by public universities in mitigating the coronavirus catastrophe in Brazil: Soli-darity, research and support to local governments facing the health crisis. Front. Sociol., 2021, 6, 610297.
[121]
de Castro, M.J.; Pardo-Seco, J.; Martinón-Torres, F. Nonspecific (heterologous) protection of neonatal BCG vaccination against hospitali-zation due to respiratory infection and sepsis. Clin. Infect. Dis., 2015, 60(11), 1611-1619.
[http://dx.doi.org/10.1093/cid/civ144] [PMID: 25725054]
[122]
O’Neill, L.A.J.; Netea, M.G. BCG-induced trained immunity: Can it offer protection against COVID-19? Nat. Rev. Immunol., 2020, 20(6), 335-337.
[http://dx.doi.org/10.1038/s41577-020-0337-y] [PMID: 32393823]
[123]
Miller, A.; Reandelar, M.J.; Fasciglione, K.; Roumenova, V.; Li, Y.; Otazu, G.H. Correlation between universal BCG vaccination policy and reduced mortality for COVID-19. medRxiv, 2021.
[http://dx.doi.org/10.1101/2020.03.24.20042937]
[124]
Escobar, L.E.; Molina-Cruz, A.; Barillas-Mury, C. BCG vaccine protection from severe coronavirus disease 2019 (COVID-19). Proc. Natl. Acad. Sci. USA, 2020, 117(30), 17720-17726.
[http://dx.doi.org/10.1073/pnas.2008410117] [PMID: 32647056]
[125]
Ozdemir, C.; Kucuksezer, U.C.; Tamay, Z.U. Is BCG vaccination affecting the spread and severity of COVID-19? Allergy, 2020, 75(7), 1824-1827.
[http://dx.doi.org/10.1111/all.14344] [PMID: 32330314]
[126]
Giamarellos-Bourboulis, E.J.; Tsilika, M.; Moorlag, S.; Antonakos, N.; Kotsaki, A.; Domínguez-Andrés, J.; Kyriazopoulou, E.; Gkavogianni, T.; Adami, M.E.; Damoraki, G.; Koufargyris, P.; Karageorgos, A.; Bolanou, A.; Koenen, H.; van Crevel, R.; Droggiti, D.I.; Renieris, G.; Papadopoulos, A.; Netea, M.G. Activate: Randomized clinical trial of BCG vaccination against infection in the elderly. Cell, 2020, 183(2), 315-323.
[http://dx.doi.org/10.1016/j.cell.2020.08.051] [PMID: 32941801]
[127]
Gonzalez-Perez, M.; Sanchez-Tarjuelo, R.; Shor, B.; Nistal-Villan, E.; Ochando, J. The BCG vaccine for COVID-19: First verdict and futu-re directions. Front. Immunol., 2021, 12, 632478.
[http://dx.doi.org/10.3389/fimmu.2021.632478] [PMID: 33763077]
[128]
Junqueira-Kipnis, A.P.; Dos Anjos, L.R.B.; Barbosa, L.C.S.; da Costa, A.C.; Borges, K.C.M.; Cardoso, A.D.R.O.; Ribeiro, K.M.; Rosa, S.B.A.; Souza, C.C. das Neves, R.C.; Saraiva, G.; da Silva, S.M.; Silveira, E.A.; Rabahi, M.F.; Conte, M.B.; Kipnis, A. BCG revaccination of health workers in Brazil to improve innate immune responses against COVID-19: A structured summary of a study protocol for a ran-domised controlled trial. Trials, 2020, 21(1), 881.
[http://dx.doi.org/10.1186/s13063-020-04822-0] [PMID: 33106170]
[129]
Hamiel, U.; Kozer, E.; Youngster, I. SARS-CoV-2 rates in BCG-vaccinated and unvaccinated young adults. JAMA, 2020, 323(22), 2340-2341.
[http://dx.doi.org/10.1001/jama.2020.8189] [PMID: 32401274]
[130]
Rivas, M.N.; Ebinger, J.E.; Wu, M.; Sun, N.; Braun, J.; Sobhani, K.; Van Eyk, J.E.; Cheng, S.; Arditi, M. BCG vaccination history associa-tes with decreased SARS-CoV-2 seroprevalence across a diverse cohort of health care workers. J. Clin. Invest., 2021, 131(2), 145157.
[http://dx.doi.org/10.1172/JCI145157] [PMID: 33211672]
[131]
Moorlag, S.J.C.F.M.; van Deuren, R.C.; van Werkhoven, C.H.; Jaeger, M.; Debisarun, P.; Taks, E. Safety and COVID-19 symptoms in individuals recently vaccinated with BCG: A retrospective cohort study. Cell Reports Med., 2020, 1(5), 100073.
[132]
Koeken, V.A.C.M.; de Bree, L.C.J.; Mourits, V.P.; Moorlag, S.J.C.F.M.; Walk, J.; Cirovic, B.; Arts, R.J.; Jaeger, M.; Dijkstra, H.; Lemmers, H.; Joosten, L.A.; Benn, C.S.; van Crevel, R.; Netea, M.G. BCG vaccination in humans inhibits systemic inflammation in a sex-dependent manner. J. Clin. Invest., 2020, 130(10), 5591-5602.
[http://dx.doi.org/10.1172/JCI133935] [PMID: 32692728]
[133]
Pavan Kumar, N.; Padmapriyadarsini, C.; Rajamanickam, A.; Marinaik, S.B.; Nancy, A.; Padmanaban, S.; Akbar, N.; Murhekar, M.; Babu, S. Effect of BCG vaccination on proinflammatory responses in elderly individuals. Sci. Adv., 2021, 7(32), abg7181.
[http://dx.doi.org/10.1126/sciadv.abg7181] [PMID: 34348897]

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