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Research Article

Mutation on lysX from Mycobacterium avium hominissuis impacts the host–pathogen interaction and virulence phenotype

, , ORCID Icon, ORCID Icon &
Pages 132-144 | Received 03 Jul 2019, Accepted 26 Nov 2019, Published online: 29 Jan 2020

References

  • Franco-Paredes C, Marcos L, Henao-Martínez A, et al. Cutaneous mycobacterial infections. Clin Microbiol Rev. 2019;32:e00069–18.
  • Falkinham Iii JO. Surrounded by mycobacteria: nontuberculous mycobacteria in the human environment. J Appl Microbiol. 2009;107(2):356–367.
  • Falkinham JO. Environmental sources of nontuberculous mycobacteria. Clin Chest Med. 2015;36(1):35–41.
  • O’Brien C. Update on mycobacterial infections: diagnosis, management, and zoonotic considerations, in August’s consultations in feline internal medicine. St. Louis: Elsevier; 2015. p. 35–56.
  • Griffith DE, Aksamit T, Brown-Elliott BA, et al. An official ATS/IDSA statement: diagnosis, treatment, and prevention of nontuberculous mycobacterial diseases. Am J Respir Crit Care Med. 2007;175(4):367–416.
  • Brown-Elliott BA, Nash KA, Wallace RJ Jr. Antimicrobial susceptibility testing, drug resistance mechanisms, and therapy of infections with nontuberculous mycobacteria. Clin Microbiol Rev. 2012;25(3):545–582.
  • Inderlied CB, Kemper CA, Bermudez LEM. The Mycobacterium avium complex. Clin Microbiol Rev. 1993;6(3):266–310.
  • Cassidy PM, Hedberg K, Saulson A, et al. Nontuberculous mycobacterial disease prevalence and risk factors: A changing epidemiology. Clin Infect Dis. 2009;49(12):e124–e129.
  • Epson E, Winthrop K. Nontuberculous mycobacterial lung disease: an emerging disease in the elderly. Open Longev Sci. 2012;6:92–100.
  • Gopinath K, Singh S. Non-Tuberculous mycobacteria in TB-endemic countries: are we neglecting the danger? PLoS Negl Trop Dis. 2010;4(4):e615.
  • Tabarsi P, Baghaei P, Farnia P, et al. Nontuberculous mycobacteria among patients who are suspected for multidrug-resistant tuberculosis - need for earlier identification of nontuberculosis mycobacteria. Am J Med Sci. 2009;337(3):182–184.
  • Nishiuchi Y, Iwamoto T, Maruyama F. Infection sources of a common non-tuberculous mycobacterial pathogen, Mycobacterium avium complex. Front Med (Lausanne). 2017;4:27.
  • Prevots DR, Marras TK. Epidemiology of human pulmonary infection with nontuberculous mycobacteria a review. Clin Chest Med. 2015;36(1):13–34.
  • Thomson RM. Changing epidemiology of pulmonary nontuberculous mycobacteria infections. Emerg Infect Dis. 2010;16(10):1576–1583.
  • Adjemian J, Olivier KN, Seitz AE, et al. Spatial clusters of nontuberculous mycobacterial lung disease in the United States. Am J Respir Crit Care Med. 2012;186(6):553–558.
  • Koh WJ, Chang B, Jeong BH, et al. Increasing recovery of nontuberculous mycobacteria from respiratory specimens over a 10-year period in a tertiary referral hospital in South Korea. Tuberc Respir Dis (Seoul). 2013;75(5):199–204.
  • Namkoong H, Kurashima A, Morimoto K, et al. Epidemiology of pulmonary nontuberculous mycobacterial disease, Japan. Emerg Infect Dis. 2016;22(6):1116–1117.
  • Shah NM, Davidson JA, Anderson LF, et al. Pulmonary Mycobacterium avium-intracellulare is the main driver of the rise in non-tuberculous mycobacteria incidence in England, Wales and Northern Ireland, 2007-2012. BMC Infect Dis. 2016;16(1):195.
  • Danelishvili L, Stang B, Bermudez LE. Identification of Mycobacterium avium genes expressed during invivo infection and the role of the oligopeptide transporter OppA in virulence. Microb Pathog. 2014;76:67–76.
  • Laurent JP, Hauge K, Burnside K, et al. Mutational analysis of cell wall biosynthesis in Mycobacterium avium. J Bacteriol. 2003;185(16):5003–5006.
  • Freeman R, Geier H, Weigle KM, et al. Roles for cell wall glycopeptidolipid in surface adherence and planktonic dispersal of Mycobacterium avium. Appl Environ Microbiol. 2006;72(12):7554–7558.
  • Krzywinska E, Schorey JS. Characterization of genetic differences between Mycobacterium avium subsp. avium strains of diverse virulence with a focus on the glycopeptidolipid biosynthesis cluster. Vet Microbiol. 2003;91(2–3):249–264.
  • Shimada KI, Takimoto H, Yano I, et al. Involvement of mannose receptor in glycopeptidolipid-mediated inhibition of phagosome-lysosome fusion. Microbiol Immunol. 2006;50(3):243–251.
  • Schorey JS, Sweet L. The mycobacterial glycopeptidolipids: structure, function, and their role in pathogenesis. Glycobiology. 2008;18(11):832–841.
  • Horgen L, Barrow ELW, Barrow WW, et al. Exposure of human peripheral blood mononuclear cells to total lipids and serovar-specific glycopeptidolipids from Mycobacterium avium serovars 4 and 8 results in inhibition of TH1-type responses. Microb Pathog. 2000;29(1):9–16.
  • Maloney E, Stankowska D, Zhang J, et al. The two-domain lysX protein of Mycobacterium tuberculosis is required for production of lysinylated phosphatidylglycerol and resistance to cationic antimicrobial peptides. PLoS Pathog. 2009;5(7):e1000534.
  • Motamedi N, Danelishvili L, Bermudez LE. Identification of Mycobacterium avium genes associated with resistance to host antimicrobial peptides. J Med Microbiol. 2014;63(PART 7):923–930.
  • Kirubakar G, Murugaiyan J, Schaudinn C, et al. Proteome analysis of a M. avium mutant exposes a novel role of the bifunctional protein LysX in the regulation of metabolic activity. J Infect Dis. 2018;218(2):291–299.
  • Horan KL, Freeman R, Weigel K, et al. Isolation of the genome sequence strain Mycobacterium avium 104 from multiple patients over a 17-year period. J Clin Microbiol. 2006;44:783–789.
  • Khattak FA, Kumar A, Kamal E, et al. Illegitimate recombination: an efficient method for random mutagenesis in Mycobacterium avium subsp. hominissuis. BMC Microbiol. 2012;12(1):204.
  • Sharbati J, Lewin A, Kutz-Lohroff B, et al. Integrated microRNA-mRNA-analysis of human monocyte derived macrophages upon Mycobacterium avium subsp. hominissuis infection. PLoS One. 2011;6(5):e20258.
  • Kitada S, Maekura R, Toyoshima N, et al. Serodiagnosis of pulmonary disease due to Mycobacterium avium complex with an enzyme immunoassay that uses a mixture of glycopeptidolipid antigens. Clinl Infect Dis. 2002;35(11):1328–1335.
  • Mukherjee R, Gomez M, Jayaraman N, et al. Hyperglycosylation of glycopeptidolipid of Mycobacterium smegmatis under nutrient starvation: structural studies. Microbiology. 2005;151(7):2385–2392.
  • Kunisch R, Kamal E, Lewin A. The role of the mycobacterial DNA-binding protein 1 (MDP1) from Mycobacterium bovis BCG in host cell interaction. BMC Microbiol. 2012;12: 165.
  • Sweet L, Schorey JS. Glycopeptidolipids from Mycobacterium avium promote macrophage activation in a TLR2‐and MyD88‐dependent manner. J Leukoc Biol. 2006;80(2):415–423.
  • Fujiwara N, Kobayashi K. Mycobacterial glycolipids and host responses, in Glycolipids: new research. New York: Nova Science Publishers Inc; 2008. p. 99–116.
  • Guirado E, Arcos J, Knaup R, et al. Characterization of clinical and environmental Mycobacterium avium spp. isolates and their interaction with human macrophages. PloS One. 2012;7(9):e45411.
  • Kitada S, Maekura R, Toyoshima N, et al. Use of glycopeptidolipid core antigen for serodiagnosis of Mycobacterium avium complex pulmonary disease in immunocompetent patients. Clin Diagn Lab Immunol. 2005;12(1):44–51.
  • Palmer MV, Thacker TC, Waters WR. Multinucleated giant cell cytokine expression in pulmonary granulomas of cattle experimentally infected with Mycobacterium bovis. Vet Immunol Immunopathol. 2016;180:34–39.
  • Montoya-Rosales A, Provvedi R, Torres-Juarez F, et al. lysX gene is differentially expressed among Mycobacterium tuberculosis strains with different levels of virulence. Tuberculosis. 2017;106:106–117.
  • Lamichhane G. Mycobacterium tuberculosis response to stress from reactive oxygen and nitrogen species. Front Microbiol. 2011;2:176.
  • Voskuil MI, Bartek IL, Visconti K, et al. The response of Mycobacterium tuberculosis to reactive oxygen and nitrogen species. Front Microbiol. 2011;2:105.
  • Shastri MD, Shukla SD, Chong WC, et al. Role of oxidative stress in the pathology and management of human tuberculosis. Oxid Med Cell Longev. 2018;2018:1–10.
  • Tomioka H, Sato K, Sano C, et al. Effector molecules of the host defence mechanism against Mycobacterium avium complex: the evidence showing that reactive oxygen intermediates, reactive nitrogen intermediates, and free fatty acids each alone are not decisive in expression of macrophage antimicrobial activity against the parasites. Clin Exp Immunol. 1997;109(2):248–254.
  • Johansson MEV, Holmén Larsson JM, Hansson GC. The two mucus layers of colon are organized by the MUC2 mucin, whereas the outer layer is a legislator of host-microbial interactions. Proc Natl Acad Sci U S A. 2011;108(SUPPL. 1):4659–4665.
  • Dong H, Lv Y, Zhao D, et al. Defensins: the case for their use against mycobacterial infections. J Immunol Res. 2016;2016:1–9.
  • Ashitani JI, Mukae H, Hiratsuka T, et al. Plasma and BAL fluid concentrations of antimicrobial peptides in patients with Mycobacterium avium-intracellulare infection. Chest. 2001;119(4):1131–1137.
  • Peschel A, Jack RW, Otto M, et al. Staphylococcus aureus resistance to human defensins and evasion of neutrophil killing via the novel virulence factor MprF is based on modification of membrane lipids with L-lysine. The Journal of Experimental Medicine. 2001;193(9):1067–1076.
  • Cooper AM, Mayer-Barber KD, Sher A. Role of innate cytokines in mycobacterial infection. Mucosal Immunol. 2011;4(3):252.
  • González-Pérez M, Mariño-Ramírez L, Parra-López CA, et al. Virulence and immune response induced by Mycobacterium avium complex strains in a model of progressive pulmonary tuberculosis and subcutaneous infection in BALB/c mice. Infect Immun. 2013;81(11):4001–4012.
  • Ghazaei C. Mycobacterium tuberculosis and lipids: insights into molecular mechanisms from persistence to virulence. J Res Med Sci. 2018;23:63.
  • Hernandez-Pando R, Bornstein QL, Aguilar Leon D, et al. Inflammatory cytokine production by immunological and foreign body multinucleated giant cells. Immunology. 2000;100(3):352–358.
  • Ramakrishnan L. Revisiting the role of the granuloma in tuberculosis. Nat Rev Immunol. 2012;12(5):352–366.
  • Puissegur M-P, Lay G, Gilleron M, et al. Mycobacterial lipomannan induces granuloma macrophage fusion via a TLR2-dependent, ADAM9-and β1 integrin-mediated pathway. J Immunol. 2007;178(5):3161–3169.
  • Kolly GS, Boldrin F, Sala C, et al. Assessing the essentiality of the decaprenyl‐phospho‐d‐arabinofuranose pathway in Mycobacterium tuberculosis using conditional mutants. Mol Microbiol. 2014;92(1):194–211.
  • Wojda I. Immunity of the greater wax moth Galleria mellonella. Insect Sci. 2017;24(3):342–357.
  • Li Y, Spiropoulos J, Cooley W, et al. Galleria mellonella-a novel infection model for the Mycobacterium tuberculosis complex. Virulence. 2018;9(1):1126–1137.
  • Meir M, Grosfeld T, Barkan D. Establishment and validation of Galleria mellonella as a novel model organism to study Mycobacterium abscessus infection, pathogenesis, and treatment. Antimicrob Agents Chemother. 2018;62(4):e02539–17.
  • Entwistle F, Coote PJ. Evaluation of greater wax moth larvae, Galleria mellonella, as a novel in vivo model for non-tuberculosis Mycobacteria infections and antibiotic treatments. J Med Microbiol. 2018;67:585–597.
  • Fedrizzi T, Meehan CJ, Grottola A, et al. Genomic characterization of nontuberculous mycobacteria. Sci Rep. 2017;7:45258.
  • Lee K-I, Choi H-G, Son Y-J, et al. Mycobacterium avium MAV2052 protein induces apoptosis in murine macrophage cells through Toll-like receptor 4. Apoptosis. 2016;21(4):459–472.
  • Forrellad MA, Bianco M, Blanco F, et al. Study of the in vivo role of Mce2R, the transcriptional regulator of mce2 operon in Mycobacterium tuberculosis. BMC Microbiol. 2013;13(1):200.
  • Velmurugan K, Chen B, Miller JL, et al. Mycobacterium tuberculosis nuoG is a virulence gene that inhibits apoptosis of infected host cells. PLoS Pathog. 2007;3(7):e110.
  • Sweet L, Zhang W, Torres-Fewell H, et al. Mycobacterium avium glycopeptidolipids require specific acetylation and methylation patterns for signaling through toll-like receptor 2. J Biol Chem. 2008;283(48):33221–33231.
  • Pang L, Tian X, Pan W, et al. Structure and function of mycobacterium glycopeptidolipids from comparative genomics perspective. J Cell Biochem. 2013;114(8):1705–1713.
  • Thegerström J, Jönsson B, Brudin L, et al. Mycobacterium avium subsp. avium and subsp. hominissuis give different cytokine responses after in vitro stimulation of human blood mononuclear cells. PloS One. 2012;7(4):e34391.
  • Barrow WW. Processing of mycobacterial lipids and effects on host responsiveness. Front Biosci. 1997;2:d387–400.