[KSCI] Korea Science Citation Index Service

http://dx.doi.org/10.4110/in.2009.9.2.46

The Role of Nitric Oxide in Mycobacterial Infections

Yang, Chul-Su (Department of Microbiology and Infection Signaling Network Research Center, College of Medicine, Chungnam National University)
Yuk, Jae-Min (Department of Microbiology and Infection Signaling Network Research Center, College of Medicine, Chungnam National University)
Jo, Eun-Kyeong (Department of Microbiology and Infection Signaling Network Research Center, College of Medicine, Chungnam National University)

Publication Information

IMMUNE NETWORK / v.9, no.2, 2009 , pp. 46-52 More about this Journal

Abstract

Although tuberculosis poses a significant health threat to the global population, it is a challenge to develop new and effective therapeutic strategies. Nitric oxide (NO) and inducible NO synthase (iNOS) are important in innate immune responses to various intracellular bacterial infections, including mycobacterial infections. It is generally recognized that reactive nitrogen intermediates play an effective role in host defense mechanisms against tuberculosis. In a murine model of tuberculosis, NO plays a crucial role in antimycobacterial activity; however, it is controversial whether NO is critically involved in host defense against Mycobacterium tuberculosis in humans. Here, we review the roles of NO in host defense against murine and human tuberculosis. We also discuss the specific roles of NO in the central nervous system and lung epithelial cells during mycobacterial infection. A greater understanding of these defense mechanisms in human tuberculosis will aid in the development of new strategies for the treatment of disease.

Keywords

nitric oxide; mycobacteria; macrophages; host defense;

Citations & Related Records

Reference

1	Adams LB, Dinauer MC, Morgenstern DE, Krahenbuhl JL:Comparison of the roles of reactive oxygen and nitrogen intermediates in the host response to Mycobacterium tuberculosis using transgenic mice. Tuber Lung Dis 78;237-246, 1997 DOI ScienceOn
2	Chan J, Tanaka K, Carroll D, Flynn J, Bloom BR: Effects of nitric oxide synthase inhibitors on murine infection with Mycobacterium tuberculosis. Infect Immun 63;736-740, 1995 PUBMED
3	Mayer B, Hemmens B: Biosynthesis and action of nitric oxide in mammalian cells. Trends Biochem Sci 22;477-481, 1997 DOI PUBMED ScienceOn
4	Choi HS, Rai PR, Chu HW, Cool C, Chan ED: Analysis of nitric oxide synthase and nitrotyrosine expression in human pulmonary tuberculosis. Am J Respir Crit Care Med 166; 178-186, 2002 DOI ScienceOn
5	Nicholson S, Bonecini-Almeida Mda G, Lapa e Silva JR, Nathan C, Xie QW, Mumford R, Weidner JR, Calaycay J, Geng J, Boechat N, Linhares C, Rom W, Ho JL: Inducible nitric oxide synthase in pulmonary alveolar macrophages from patients with tuberculosis. J Exp Med 183;2293-2302, 1996 DOI ScienceOn
6	Paton NI, Chua YK, Earnest A, Chee CB: Randomized controlled trial of nutritional supplementation in patients with newly diagnosed tuberculosis and wasting. Am J Clin Nutr 80;460-465, 2004 PUBMED
7	Zaki MH, Akuta T, Akaike T: Nitric oxide-induced nitrative stress involved in microbial pathogenesis. J Pharmacol Sci 98;117-129, 2005 DOI ScienceOn
8	Zaragoza C, Ocampo CJ, Saura M, Bao C, Leppo M, Lafond-Walker A, Thiemann DR, Hruban R, Lowenstein CJ: Inducible nitric oxide synthase protection against coxsackievirus pancreatitis. J Immunol 163;5497-5504, 1999 PUBMED
9	MacLean A, Wei XQ, Huang FP, Al-Alem UA, Chan WL, Liew FY: Mice lacking inducible nitric-oxide synthase are more susceptible to herpes simplex virus infection despite enhanced Th1 cell responses. J Gen Virol 79;825-830, 1998 DOI PUBMED
10	Adler H, Beland JL, Del-Pan NC, Kobzik L, Brewer JP, Martin TR, Rimm IJ: Suppression of herpes simplex virus type 1 (HSV-1)-induced pneumonia in mice by inhibition of inducible nitric oxide synthase (iNOS, NOS2). J Exp Med 185;1533-1540, 1997 DOI ScienceOn
11	Flesch IE, Hess JH, Kaufmann SH: NADPH diaphorase staining suggests a transient and localized contribution of nitric oxide to host defence against an intracellular pathogen in situ. Int Immunol 6;1751-1757, 1994 DOI ScienceOn
12	Scanga CA, Mohan VP, Yu K, Joseph H, Tanaka K, Chan J, Flynn JL: Depletion of CD4(+) T cells causes reactivation of murine persistent tuberculosis despite continued expression of interferon gamma and nitric oxide synthase 2. J Exp Med 192;347-358, 2000 DOI ScienceOn
13	Rich EA, Torres M, Sada E, Finegan CK, Hamilton BD, Toossi Z: Mycobacterium tuberculosis (MTB)-stimulated production of nitric oxide by human alveolar macrophages and relationship of nitric oxide production to growth inhibition of MTB. Tuber Lung Dis 78;247-255, 1997 DOI ScienceOn
14	Facchetti F, Vermi W, Fiorentini S, Chilosi M, Caruso A, Duse M, Notarangelo LD, Badolato R: Expression of inducible nitric oxide synthase in human granulomas and histiocytic reactions. Am J Pathol 154;145-152, 1999 DOI PUBMED ScienceOn
15	Peterson PK, Hu S, Anderson WR, Chao CC: Nitric oxide production and neurotoxicity mediated by activated microglia from human versus mouse brain. J Infect Dis 170;457-460, 1994 DOI PUBMED ScienceOn
16	Kwon OJ, Kim JH, Kim HC, Suh GY, Park JW, Chung MP, Kim H, Rhee CH: Nitric oxide expression in airway epithelial cells in response to tubercle bacilli stimulation. Respirology 3;119-124, 1998 DOI ScienceOn
17	Rodriguez PC, Zea AH, DeSalvo J, Culotta KS, Zabaleta J, Quiceno DG, Ochoa JB, Ochoa AC: L-arginine consumption by macrophages modulates the expression of CD3zeta chain in T lymphocytes. J Immunol 171;1232-1239, 2003 DOI PUBMED
18	Roy S, Sharma S, Sharma M, Aggarwal R, Bose M: Induction of nitric oxide release from the human alveolar epithelial cell line A549: an in vitro correlate of innate immune response to Mycobacterium tuberculosis. Immunology 112;471-480, 2004 DOI ScienceOn
19	Adams LB, Franzblau SG, Vavrin Z, Hibbs JB Jr, Krahenbuhl JL: L-arginine-dependent macrophage effector functions inhibit metabolic activity of Mycobacterium leprae. J Immunol 147;1642-1646, 1991 PUBMED
20	Kuo HP, Wang CH, Huang KS, Lin HC, Yu CT, Liu CY, Lu LC: Nitric oxide modulates interleukin-1beta and tumor necrosis factor-alpha synthesis by alveolar macrophages in pulmonary tuberculosis. Am J Respir Crit Care Med 161;192-199, 2000 DOI PUBMED ScienceOn
21	Arias M, Rojas M, Zabaleta J, Rodríguez JI, París SC, Barrera LF, Garc $\acute{i}$ a LF: Inhibition of virulent Mycobacterium tuberculosis by Bcg(r) and Bcg(s) macrophages correlates with nitric oxide production. J Infect Dis 176;1552-1558, 1997 DOI ScienceOn
22	Kwon OJ: The role of nitric oxide in the immune response of tuberculosis. J Korean Med Sci 12;481-487, 1997 DOI PUBMED
23	Bermudez LE: Differential mechanisms of intracellular killing of Mycobacterium avium and Listeria monocytogenes by activated human and murine macrophages. The role of nitric oxide. Clin Exp Immunol 91;277-281, 1993 DOI ScienceOn
24	MacMicking J, Xie QW, Nathan C: Nitric oxide and macrophage function. Annu Rev Immunol 15;323-350, 1997 DOI ScienceOn
25	Nathan C, Xie QW: Regulation of biosynthesis of nitric oxide. J Biol Chem 269;13725-13728, 1994 PUBMED
26	Rock RB, Gekker G, Hu S, Sheng WS, Cheeran M, Lokensgard JR, Peterson PK: Role of microglia in central nervous system infections. Clin Microbiol Rev 17;942-964, 2004 DOI ScienceOn
27	van Well GT, Wieland CW, Florquin S, Roord JJ, van der Poll T, van Furth AM: A new murine model to study the pathogenesis of tuberculous meningitis. J Infect Dis 195;694-697, 2007 DOI ScienceOn
28	Chan J, Xing Y, Magliozzo RS, Bloom BR: Killing of virulent Mycobacterium tuberculosis by reactive nitrogen intermediates produced by activated murine macrophages. J Exp Med 175;1111-1122, 1992 DOI ScienceOn
29	Wang CH, Liu CY, Lin HC, Yu CT, Chung KF, Kuo HP: Increased exhaled nitric oxide in active pulmonary tuberculosis due to inducible NO synthase upregulation in alveolar macrophages. Eur Respir J 11;809-815, 1998 DOI ScienceOn
30	Kropf P, Baud D, Marshall SE, Munder M, Mosley A, Fuentes JM, Bangham CR, Taylor GP, Herath S, Choi BS, Soler G, Teoh T, Modolell M, M $\ddot{u}$ ller I: Arginase activity mediates reversible T cell hyporesponsiveness in human pregnancy. Eur J Immunol 37;935-945, 2007 DOI ScienceOn
31	Rockett KA, Brookes R, Udalova I, Vidal V, Hill AV, Kwiatkowski D: 1,25-Dihydroxyvitamin D3 induces nitric oxide synthase and suppresses growth of Mycobacterium tuberculosis in a human macrophage-like cell line. Infect Immun 66;5314-5321, 1998 PUBMED
32	Lee SC, Dickson DW, Liu W, Brosnan CF: Induction of nitric oxide synthase activity in human astrocytes by interleukin-1beta and interferon-gamma. J Neuroimmunol 46;19-24, 1993 DOI ScienceOn
33	Olin MR, Armien AG, Cheeran MC, Rock RB, Molitor TW, Peterson PK: Role of nitric oxide in defense of the central nervous system against Mycobacterium tuberculosis. J Infect Dis 198;886-889, 2008 DOI ScienceOn
34	Umezawa K, Akaike T, Fujii S, Suga M, Setoguchi K, Ozawa A, Maeda H: Induction of nitric oxide synthesis and xanthine oxidase and their roles in the antimicrobial mechanism against Salmonella typhimurium infection in mice. Infect Immun 65;2932-2940, 1997 PUBMED
35	Alam MS, Akaike T, Okamoto S, Kubota T, Yoshitake J, Sawa T, Miyamoto Y, Tamura F, Maeda H: Role of nitric oxide in host defense in murine salmonellosis as a function of its antibacterial and antiapoptotic activities. Infect Immun 70;3130-3142, 2002 DOI ScienceOn
36	Robbins RA, Barnes PJ, Springall DR, Warren JB, Kwon OJ, Buttery LD, Wilson AJ, Geller DA, Polak JM: Expression of inducible nitric oxide in human lung epithelial cells. Biochem Biophys Res Commun 203;209-218, 1994 DOI ScienceOn
37	Canthaboo C, Xing D, Wei XQ, Corbel MJ: Investigation of role of nitric oxide in protection from Bordetella pertussis respiratory challenge. Infect Immun 70;679-684, 2002 DOI ScienceOn
38	Wang CH, Lin HC, Liu CY, Huang KH, Huang TT, Yu CT, Kuo HP: Upregulation of inducible nitric oxide synthase and cytokine secretion in peripheral blood monocytes from pulmonary tuberculosis patients. Int J Tuberc Lung Dis 5;283-291, 2001 PUBMED
39	Flynn JL, Scanga CA, Tanaka KE, Chan J: Effects of aminoguanidine on latent murine tuberculosis. J Immunol 160; 1796-1803, 1998 PUBMED
40	Gazzinelli RT, Eltoum I, Wynn TA, Sher A: Acute cerebral toxoplasmosis is induced by in vivo neutralization of TNF-alpha and correlates with the down-regulated expression of inducible nitric oxide synthase and other markers of macrophage activation. J Immunol 151;3672-3681, 1993 PUBMED
41	Bolovan-Fritts CA, Spector SA: Endothelial damage from cytomegalovirus-specific host immune response can be prevented by targeted disruption of fractalkine-CX3CR1 interaction. Blood 111;175-182, 2008 DOI ScienceOn
42	Wu G, Morris SM Jr: Arginine metabolism: nitric oxide and beyond. Biochem J 336;1-17, 1998 DOI PUBMED
43	Rock RB, Hu S, Deshpande A, Munir S, May BJ, Baker CA, Peterson PK, Kapur V: Transcriptional response of human microglial cells to interferon- $\gamma$ . Genes Immun 6;712-719, 2005 DOI PUBMED
44	Rojas M, Barrera LF, Puzo G, Garcia LF: Differential induction of apoptosis by virulent Mycobacterium tuberculosis in resistant and susceptible murine macrophages:role of nitric oxide and mycobacterial products. J Immunol 159;1352-1361, 1997 PUBMED
45	Nathan C, Shiloh MU: Reactive oxygen and nitrogen intermediates in the relationship between mammalian hosts and microbial pathogens. Proc Natl Acad Sci U S A 97;8841-8848, 2000 DOI ScienceOn
46	Croen KD: Evidence for antiviral effect of nitric oxide. Inhibition of herpes simplex virus type 1 replication. J Clin Invest 91;2446-2452, 1993 DOI ScienceOn
47	Denis M: In vivo modulation of atypical mycobacterial infection: adjuvant therapy increases resistance to Mycobacterium avium by enhancing macrophage effector functions. Cell Immunol 134;42-53, 1991 DOI PUBMED ScienceOn
48	Zaragoza C, Ocampo CJ, Saura M, McMillan A, Lowenstein CJ: Nitric oxide inhibition of coxsackievirus replication in vitro. J Clin Invest 100;1760-1767, 1997 DOI ScienceOn
49	Akaike T, Okamoto S, Sawa T, Yoshitake J, Tamura F, Ichimori K, Miyazaki K, Sasamoto K, Maeda H: 8-nitroguanosine formation in viral pneumonia and its implication for pathogenesis. Proc Natl Acad Sci U S A 100;685-690, 2003 DOI ScienceOn
50	Nozaki Y, Hasegawa Y, Ichiyama S, Nakashima I, Shimokata K: Mechanism of nitric oxide-dependent killing of Mycobacterium bovis BCG in human alveolar macrophages. Infect Immun 65;3644-3647, 1997 PUBMED
51	Gamba G, Cavalieri H, Courreges MC, Massouh EJ, Benencia F: Early inhibition of nitric oxide production increases HSV-1 intranasal infection. J Med Virol 73;313-322, 2004 DOI ScienceOn
52	Fujii S, Akaike T, Maeda H: Role of nitric oxide in pathogenesis of herpes simplex virus encephalitis in rats. Virology 256;203-212, 1999 DOI ScienceOn
53	Mannick JB, Asano K, Izumi K, Kieff E, Stamler JS: Nitric oxide produced by human B lymphocytes inhibits apoptosis and Epstein-Barr virus reactivation. Cell 79;1137-1146, 1994 DOI ScienceOn
54	Jagannath C, Actor JK, Hunter RL Jr: Induction of nitric oxide in human monocytes and monocyte cell lines by Mycobacterium tuberculosis. Nitric Oxide 2;174-186, 1998 DOI ScienceOn
55	Sharma M, Sharma S, Roy S, Varma S, Bose M: Pulmonary epithelial cells are a source of interferon-gamma in response to Mycobacterium tuberculosis infection. Immunol Cell Biol 85;229-237, 2007 DOI PUBMED
56	Tucker PC, Griffin DE, Choi S, Bui N, Wesselingh S: Inhibition of nitric oxide synthesis increases mortality in Sindbis virus encephalitis. J Virol 70;3972-3977, 1996 PUBMED
57	Kreil TR, Eibl MM: Nitric oxide and viral infection: NO antiviral activity against a flavivirus in vitro, and evidence for contribution to pathogenesis in experimental infection in vivo. Virology 219;304-306, 1996 DOI ScienceOn
58	Doi T, Ando M, Akaike T, Suga M, Sato K, Maeda H: Resistance to nitric oxide in Mycobacterium avium complex and its implication in pathogenesis. Infect Immun 61; 1980-1989, 1993 PUBMED
59	Moncada S, Palmer RM, Higgs EA: Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacol Rev 43;109-142, 1991 PUBMED
60	Zaragoza C, Ocampo C, Saura M, Leppo M, Wei XQ, Quick R, Moncada S, Liew FY, Lowenstein CJ: The role of inducible nitric oxide synthase in the host response to coxsackievirus myocarditis. Proc Natl Acad Sci U S A 95;2469-2474, 1998 DOI ScienceOn
61	Aston C, Rom WN, Talbot AT, Reibman J: Early inhibition of mycobacterial growth by human alveolar macrophages is not due to nitric oxide. Am J Respir Crit Care Med 157;1943-1950, 1998 DOI PUBMED ScienceOn
62	Gow AJ, Thom SR, Ischiropoulos H: Nitric oxide and peroxynitrite-mediated pulmonary cell death. Am J Physiol 274;L112-L118, 1998 DOI PUBMED
63	Zhang M, Xin H, Atherton SS: Murine cytomegalovirus (MCMV) spreads to and replicates in the retina after endotoxin-induced disruption of the blood-retinal barrier of immunosuppressed BALB/c mice. J Neurovirol 11;365-375, 2005 DOI ScienceOn
64	MacMicking JD, North RJ, LaCourse R, Mudgett JS, Shah SK, Nathan CF: Identification of nitric oxide synthase as a protective locus against tuberculosis. Proc Natl Acad Sci U S A 94;5243-5248, 1997 DOI ScienceOn
65	Yoshitake J, Akaike T, Akuta T, Tamura F, Ogura T, Esumi H, Maeda H: Nitric oxide as an endogenous mutagen for Sendai virus without antiviral activity. J Virol 78;8709-8719, 2004 DOI ScienceOn
66	Mazzolla R, Puliti M, Barluzzi R, Neglia R, Bistoni F, Barbolini G, Blasi E: Differential microbial clearance and immunoresponse of Balb/c (Nramp1 susceptible) and DBA2 (Nramp1 resistant) mice intracerebrally infected with Mycobacterium bovis BCG (BCG). FEMS Immunol Med Microbiol 32;149-158, 2002 DOI ScienceOn
67	Ralph AP, Kelly PM, Anstey NM: L-arginine and vitamin D:novel adjunctive immunotherapies in tuberculosis. Trends Microbiol 16;336-344, 2008 DOI ScienceOn

Reference

8	(2010) Pharmaceutical biology Antimycobacterial activity of<I>Indigofera suffruticosa</I>with activation potential of the innate immune system / 48 (8) , 878
None	(2009) Frontiers in microbiology The Response of <I>Mycobacterium Tuberculosis</I> to Reactive Oxygen and Nitrogen Species / 2 (None) , 105
6	(2009) Microbial pathogenesis <I>Mycobacterium tuberculosis</I> lipoarabinomannan enhances LPS-induced TNF-α production and inhibits NO secretion by engaging scavenger receptors / 50 (6) , 350
None	(2009) BMC immunology Distinct roles for nitric oxide in resistant C57BL/6 and susceptible BALB/c mice to control <I>Burkholderia pseudomallei </I> infection / 12 (None) , 20
None	(2013) BMC microbiology The role of 3-ketosteroid 1(2)-dehydrogenase in the pathogenicity of <I>Mycobacterium tuberculosis</I> / 13 (None) , 43
11	(2013) PLoS ONE The Scavenger Protein Apoptosis Inhibitor of Macrophages (AIM) Potentiates the Antimicrobial Response against <I>Mycobacterium tuberculosis</I> by Enhancing Autophagy / 8 (11) , e79670
12	(2009) Infection and immunity The Endothelin System Has a Significant Role in the Pathogenesis and Progression of <I>Mycobacterium tuberculosis</I> Infection / 82 (12) , 5154
6	SU HYUN HONG. (2009) Molecular medicine reports Esculetin suppresses lipopolysaccharide-induced inflammatory mediators and cytokines by inhibiting nuclear factor-κB translocation in RAW 264.7 macrophages / 10 (6) , 3241
38	(2009) Proceedings of the National Academy of Sciences of the United States of America Macrophage arginase-1 controls bacterial growth and pathology in hypoxic tuberculosis granulomas / 111 (38) , E4024
4	(2009) Clinical and experimental medicine CD3+ICOS+ T cells show differences in the synthesis of nitric oxide, IFN-γ, and IL-10 in patients with pulmonary tuberculosis or in healthy household contacts / 16 (4) , 481
3	(2016) Neuromolecular medicine Does Concurrent Use of Some Botanicals Interfere with Treatment of Tuberculosis? / 18 (3) , 483
4	(2009) Biology bulletin reviews Macrophage and Mycobacterium: The war without beginning or end / 6 (4) , 289
1	(2009) PLoS ONE Glutamate Dehydrogenase Is Required by <I>Mycobacterium bovis</I> BCG for Resistance to Cellular Stress / 11 (1) , e0147706
None	(2009) Scientific reports STAT3 Represses Nitric Oxide Synthesis in Human Macrophages upon <I>Mycobacterium tuberculosis</I> Infection / 6 (None) , 29297
1	(2009) Indonesian journal of tropical and infectious disease CELLULAR IMMUNITY ACTIVATION METHOD BY STIMULATING RD1 COMPLEX PROTEINS AS VIRULENCE MARKER ON Mycobacterium tuberculum TO ESTABLISH DIAGNOSIS ON TUBERCULOSIS AND LATENT TUBERCULOSIS INFECTION / 6 (1) , 12
10	(2016) The journal of immunology : official journal of the American Association of Immunologists Aberrant Inflammasome Activation Characterizes Tuberculosis-Associated Immune Reconstitution Inflammatory Syndrome / 196 (10) , 4052
None	(2009) Frontiers in immunology Mycobacterial Dormancy Systems and Host Responses in Tuberculosis / 8 (None) , 84
None	(2009) Frontiers in immunology Nucleotide-Binding Oligomerization Domain 2 Contributes to Limiting Growth of <I>Mycobacterium abscessus</I> in the Lung of Mice by Regulating Cytokines and Nitric Oxide Production / 8 (None) , 1477
None	(2017) Frontiers in microbiology Nitric Oxide in the Pathogenesis and Treatment of Tuberculosis / 8 (None) , 2008
17	(2009) The Journal of biological chemistry <I>Mycobacterium tuberculosis</I> EsxL inhibits MHC-II expression by promoting hypermethylation in class-II transactivator loci in macrophages / 292 (17) , 6855
5	(2009) The journal of immunology : official journal of the American Association of Immunologists Nitric Oxide Modulates Macrophage Responses to <I>Mycobacterium tuberculosis</I> Infection through Activation of HIF-1α and Repression of NF-κB / 199 (5) , 1805
None	(2009) Scientific reports The influence of haemoglobin and iron on <I>in vitro</I> mycobacterial growth inhibition assays / 7 (None) , 43478
12	(2009) EMBO reports Mycobacteria exploit nitric oxide‐induced transformation of macrophages into permissive giant cells / 18 (12) , 2144
4	(2009) Natural product research Immune modulation properties of herbal plant leaves: <I>Phyllanthus niruri</I> aqueous extract on immune cells of tuberculosis patient - <I>in vitro</I> study / 32 (4) , 463
None	(2009) Frontiers in immunology Reinforcing the Functionality of Mononuclear Phagocyte System to Control Tuberculosis / 9 (None) , 193
2	(2009) Experimental lung research Tuberculosis and cigarette smoke exposure: An update of<I>in vitro</I>and<I>in vivo</I>studies / 44 (2) , 113
4	(2019) Journal of cellular biochemistry Phospholipase C‐γ2 promotes intracellular survival of mycobacteria / 120 (4) , 5062
None	(2009) Gene reports Host and Mycobacterium tuberculosis interaction; expression of iNOS and Tbet genes from the host and virulence factors of the bacteria / 17 (None) , 100503
7	(2009) Applied sciences Oxidative Phosphorylation-an Update on a New, Essential Target Space for Drug Discovery in Mycobacterium tuberculosis / 10 (7) , 2339
4	(2009) ERJ open research European Respiratory Society International Congress, Madrid, 2019: nontuberculous mycobacterial pulmonary disease highlights / 6 (4) , 00317-2020
None	(2009) Immunology letters Determination of <I>in vitro</I> and <I>in vivo</I> immune response to recombinant cholesterol oxidase from <I>Mycobacterium tuberculosis</I> / 228 (None) , 103
12	(2020) Molecules and cells Lysophosphatidylcholine Enhances Bactericidal Activity by Promoting Phagosome Maturation via the Activation of the NF-κB Pathway during Salmonella Infection in Mouse Macrophages / 43 (12) , 989
None	(2021) Frontiers in immunology A Dual Marker for Monitoring MDR-TB Treatment: Host-Derived miRNAs and M. tuberculosis-Derived RNA Sequences in Serum / 12 (None) , 760468
1	(2021) Immunological reviews Host‐directed therapy to combat mycobacterial infections* / 301 (1) , 62