[en] AIM: To investigate the formation of Mycobacterium avium membrane vesicles (MVs) within macrophage phagosomes.
MATERIALS & METHODS: A phagosome model was utilized to characterize proteomics and lipidomics of MVs. A click chemistry-based enrichment assay was employed to examine the presence of MV proteins in the cytosol of host cells.
RESULTS: Exposure to metals at concentrations present in phagosomes triggers formation of bacterial MVs. Proteomics identified several virulence factors, including enzymes involved in the cell wall synthesis, lipid and fatty acid metabolism. Some of MV proteins were also identified in the cytosol of infected macrophages. MVs harbor dsDNA.
CONCLUSION: M. avium produces MVs within phagosomes. MVs carry products with potential roles in modulation of host immune defenses and intracellular survival.
Disciplines :
Microbiology
Author, co-author :
Chiplunkar, Sanket Sanjeev ; Université de Liège - ULiège > GIGA > GIGA Cancer ; Université de Liège - ULiège > GIGA ; Université de Liège - ULiège > Faculté de Médecine > Doct. sc. méd. (paysage)
Silva, Carlos A; Department of Biomedical Sciences, College of Veterinary Medicine, Oregon State University, Corvallis, OR 97331, USA
Bermudez, Luiz E; Department of Biomedical Sciences, College of Veterinary Medicine, Oregon State University, Corvallis, OR 97331, USA ; Department of Microbiology, College of Science, Oregon State University, Corvallis, OR 97331, USA
Danelishvili, Lia; Department of Biomedical Sciences, College of Veterinary Medicine, Oregon State University, Corvallis, OR 97331, USA
Language :
English
Title :
Characterization of membrane vesicles released by Mycobacterium avium in response to environment mimicking the macrophage phagosome.
chaperones, upon MV-mediated secretion, may trigger host proinflammatory immune responses, which actually benefit the colonization and spread of MAH104. This possibility is supported by the finding that M. tuberculosis chaperonins are highly immunogenic and potent proinflammatory cytokine stimulators [53].
Nishiuchi Y, Iwamoto T, Maruyama F. Infection sources of a common non-tuberculous mycobacterial pathogen, Mycobacterium avium complex. Front. Med. (Lausanne) 4, 27 (2017).
Armstrong D, Gold JW, Dryjanski J et al. Treatment of infections in patients with the acquired immunodeficiency syndrome. Ann. Intern. Med. 103(5), 738-743 (1985).
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. 175(4), 367-416 (2007).
Field SK, Fisher D, Cowie RL. Mycobacterium avium complex pulmonary disease in patients without HIV infection. Chest 126(2), 566-581 (2004).
Mcnamara M, Danelishvili L, Bermudez LE. The Mycobacterium avium ESX-5 PPE protein, PPE25-MAV, interacts with an ESAT-6 family protein, MAV 2921, and localizes to the bacterial surface. Microb. Pathog. 52(4), 227-238 (2012).
Li Y,Miltner E, Wu M, PetrofskyM, Bermudez LE. A Mycobacterium avium PPE gene is associated with the ability of the bacterium to grow in macrophages and virulence in mice. Cell Microbiol. 7(4), 539-548 (2005).
Danelishvili L, Bermudez LE. Mycobacterium avium MAV 2941 mimics phosphoinositol-3-kinase to interfere with macrophage phagosome maturation. Microbes Infect. 17(9), 628-637 (2015).
Danelishvili L, Wu M, Stang B et al. Identification of Mycobacterium avium pathogenicity island important for macrophage and amoeba infection. Proc. Natl Acad. Sci. USA 104(26), 11038-11043 (2007).
Danelishvili L, Bermudez LE. Mycobacterium avium MAV 2941 mimics phosphoinositol-3-kinase to interfere with macrophage phagosome maturation. Microbes Infect. 17(9), 628-637 (2015).
Abdallah AM, Gey Van Pittius NC, Champion PA et al. Type VII secretion-mycobacteria show the way. Nat. Rev. Microbiol. 5(11), 883-891 (2007).
Cambier CJ, Falkow S, Ramakrishnan L. Host evasion and exploitation schemes of Mycobacterium tuberculosis. Cell 159(7), 1497-1509 (2014).
Kulp A, Kuehn MJ. Biological functions and biogenesis of secreted bacterial outer membrane vesicles. Annu. Rev. Microbiol. 64, 163-184 (2010).
Ellis TN, Kuehn MJ. Virulence and immunomodulatory roles of bacterial outer membrane vesicles. Microbiol. Mol. Biol. Rev. 74(1), 81-94 (2010).
Brown L, Wolf JM, Prados-Rosales R, Casadevall A. Through the wall: extracellular vesicles in Gram-positive bacteria, mycobacteria and fungi. Nat. Rev. Microbiol. 13(10), 620-630 (2015).
Kuehn MJ, Kesty NC. Bacterial outer membrane vesicles and the host-pathogen interaction. Genes Dev. 19(22), 2645-2655 (2005).
Schertzer JW, Whiteley M. Bacterial outer membrane vesicles in trafficking, communication and the host-pathogen interaction. J. Mol. Microbiol. Biotechnol. 23(1-2), 118-130 (2013).
Ellis TN, Kuehn MJ. Virulence and immunomodulatory roles of bacterial outer membrane vesicles. Microbiol. Mol. Biol. Rev. 74(1), 81-94 (2010).
Deatherage BL, Cookson BT. Membrane vesicle release in bacteria, eukaryotes, and archaea: a conserved yet underappreciated aspect of microbial life. Infect. Immun. 80(6), 1948-1957 (2012).
Kaparakis-Liaskos M, Ferrero RL. Immune modulation by bacterial outer membrane vesicles. Nat. Rev. Immunol. 15(6), 375-387 (2015).
Prados-Rosales R, Weinrick BC, Pique DG, Jacobs WR Jr., Casadevall A, Rodriguez GM. Role for Mycobacterium tuberculosis membrane vesicles in iron acquisition. J. Bacteriol. 196(6), 1250-1256 (2014).
Prados-Rosales R, Baena A, Martinez LR et al. Mycobacteria release active membrane vesicles that modulate immune responses in a TLR2-dependent manner in mice. J. Clin. Invest. 121(4), 1471-1483 (2011).
Athman JJ, Sande OJ, Groft SG et al. Mycobacterium tuberculosis membrane vesicles inhibit T cell activation. J. Immunol. 198(5), 2028-2037 (2017).
Wagner D, Maser J, Lai B et al. Elemental analysis of Mycobacterium avium-, Mycobacterium tuberculosis-, and Mycobacterium smegmatis-containing phagosomes indicates pathogen-induced microenvironments within the host cell's endosomal system. J. Immunol. 174(3), 1491-1500 (2005).
Early J, Bermudez LE. Mimicry of the pathogenic mycobacterium vacuole in vitro elicits the bacterial intracellular phenotype, including early-onset macrophage death. Infect. Immun. 79(6), 2412-2422 (2011).
Chinison JJ, Danelishvili L, Gupta R, Rose SJ, Babrak LM, Bermudez LE. Identification of Mycobacterium avium subsp. hominissuis secreted proteins using an in vitro system mimicking the phagosomal environment. BMC Microbiol. 16(1), 270 (2016).
Prados-Rosales R, Brown L, Casadevall A, Montalvo-Quiros S, Luque-Garcia JL. Isolation and identification of membrane vesicle-associated proteins in Gram-positive bacteria and mycobacteria. MethodsX 1, 124-129 (2014).
Bitto NJ, Chapman R, Pidot S et al. Bacterial membrane vesicles transport their DNA cargo into host cells. Sci. Rep. 7(1), 7072 (2017).
Van Soolingen D, De Haas PE, Hermans PW, Van Embden JD. DNA fingerprinting of Mycobacterium tuberculosis. Methods Enzymol. 235, 196-205 (1994).
Schnappinger D, Ehrt S, Voskuil MI et al. Transcriptional adaptation of Mycobacterium tuberculosis within macrophages: insights into the phagosomal environment. J. Exp. Med. 198(5), 693-704 (2003).
Jeffrey B, Rose SJ, Gilbert K, Lewis M, Bermudez LE. Comparative analysis of the genomes of clinical isolates of Mycobacterium avium subsp. hominissuis regarding virulence-related genes. J. Med. Microbiol. 66(7), 1063-1075 (2017).
Mckinney JD, Honer Zu Bentrup K, Munoz-Elias EJ et al. Persistence of Mycobacterium tuberculosis in macrophages and mice requires the glyoxylate shunt enzyme isocitrate lyase. Nature 406(6797), 735-738 (2000).
Munoz-Elias EJ, Mckinney JD. Mycobacterium tuberculosis isocitrate lyases 1 and 2 are jointly required for in vivo growth and virulence. Nat. Med. 11(6), 638-644 (2005).
Nguyen MT, Gotz F. Lipoproteins of Gram-positive bacteria: key players in the immune response and virulence. Microbiol. Mol. Biol. Rev. 80(3), 891-903 (2016).
Gaur RL, Ren K, Blumenthal A et al. LprG-mediated surface expression of lipoarabinomannan is essential for virulence of Mycobacterium tuberculosis. PLoS Pathog. 10(9), e1004376 (2014).
Mahdavi A, Szychowski J, Ngo JT et al. Identification of secreted bacterial proteins by noncanonical amino acid tagging. Proc. Natl Acad. Sci. USA 111(1), 433-438 (2014).
Grammel M, Zhang MM, Hang HC. Orthogonal alkynyl amino acid reporter for selective labeling of bacterial proteomes during infection. Angew. Chem. Int. Ed. Engl. 49(34), 5970-5974 (2010).
Wier GM, Mcgreevy EM, Brown MJ, Boyle JP. New method for the orthogonal labeling and purification of Toxoplasma gondii proteins while inside the host cell. MBio 6(2), e01628 (2015).
Barry CE 3rd. Interpreting cell wall 'virulence factors' of Mycobacterium tuberculosis. Trends Microbiol. 9(5), 237-241 (2001).
Kaparakis M, Turnbull L, Carneiro L et al. Bacterial membrane vesicles deliver peptidoglycan to NOD1 in epithelial cells. Cell Microbiol. 12(3), 372-385 (2010).
Renelli M, Matias V, Lo RY, Beveridge TJ. DNA-containing membrane vesicles of Pseudomonas aeruginosa PAO1 and their genetic transformation potential. Microbiology 150(Pt 7), 2161-2169 (2004).
Dorward DW, Garon CF. DNA is packaged within membrane-derived vesicles of Gram-negative but not Gram-positive bacteria. Appl. Environ. Microbiol. 56(6), 1960-1962 (1990).
Dorward DW, Garon CF, Judd RC. Export and intercellular transfer of DNA via membrane blebs of Neisseria gonorrhoeae. J. Bacteriol. 171(5), 2499-2505 (1989).
Zuber B, Chami M, Houssin C, Dubochet J, Griffiths G, Daffe M. Direct visualization of the outer membrane of mycobacteria and corynebacteria in their native state. J. Bacteriol. 190(16), 5672-5680 (2008).
Kim JH, Lee J, Park J, Gho YS. Gram-negative and Gram-positive bacterial extracellular vesicles. Semin. Cell Dev. Biol. 40, 97-104 (2015).
Wei J, Dahl JL, Moulder JW et al. Identification of a Mycobacterium tuberculosis gene that enhances mycobacterial survival in macrophages. J. Bacteriol. 182(2), 377-384 (2000).
Shin DM, Jeon BY, Lee HM et al. Mycobacterium tuberculosis Eis regulates autophagy, inflammation, and cell death through redox-dependent signaling. PLoS Pathog. 6(12), e1001230 (2010).
Dahl JL, Wei J, Moulder JW, Laal S, Friedman RL. Subcellular localization of the Iitracellular survival-enhancing Eis protein of Mycobacterium tuberculosis. Infect. Immun. 69(7), 4295-4302 (2001).
Kalscheuer R, Weinrick B, Veeraraghavan U, Besra GS, Jacobs WR Jr. Trehalose-recycling ABC transporter LpqY-SugA-SugB-SugC is essential for virulence of Mycobacterium tuberculosis. Proc. Natl Acad. Sci. USA 107(50), 21761-21766 (2010).
Ishikawa E, Ishikawa T, Morita YS et al. Direct recognition of the mycobacterial glycolipid, trehalose dimycolate, by C-type lectin Mincle. J. Exp. Med. 206(13), 2879-2888 (2009).
Ehlers S, Kutsch S, Benini J et al. NOS2-derived nitric oxide regulates the size, quantity and quality of granuloma formation in Mycobacterium avium-infected mice without affecting bacterial loads. Immunology 98(3), 313-323 (1999).
Stewart GR, Wernisch L, Stabler R et al. Dissection of the heat-shock response in Mycobacterium tuberculosis using mutants and microarrays. Microbiology 148(Pt 10), 3129-3138 (2002).
Lewthwaite JC, Coates AR, Tormay P et al. Mycobacterium tuberculosis chaperonin 60.1 is a more potent cytokine stimulator than chaperonin 60.2 (Hsp 65) and contains a CD14-binding domain. Infect. Immun. 69(12), 7349-7355 (2001).
Fang FC. Antimicrobial reactive oxygen and nitrogen species: concepts and controversies. Nat. Rev. Microbiol. 2(10), 820-832 (2004).
Sampson SL. Mycobacterial PE/PPE proteins at the host-pathogen interface. Clin. Dev. Immunol. 2011, 497203 (2011).
Bermudez LE, Danelishvili L, Babrack L, Pham T. Evidence for genes associated with the ability of Mycobacterium avium subsp. hominissuis to escape apoptotic macrophages. Front. Cell Infect. Microbiol. 5, 63 (2015).
Singh P, Rao RN, Reddy JR et al. PE11, a PE/PPE family protein of Mycobacterium tuberculosis is involved in cell wall remodeling and virulence. Sci. Rep. 6, 21624 (2016).
Pathirana RD, Kaparakis-Liaskos M. Bacterial membrane vesicles: biogenesis, immune regulation and pathogenesis. Cell Microbiol. 18(11), 1518-1524 (2016).
Tullius MV, Harth G, Horwitz MA. Glutamine synthetase GlnA1 is essential for growth of Mycobacterium tuberculosis in human THP-1 macrophages and guinea pigs. Infect. Immun. 71(7), 3927-3936 (2003).
Harth G, Clemens DL, Horwitz MA. Glutamine synthetase of Mycobacterium tuberculosis: extracellular release and characterization of its enzymatic activity. Proc. Natl Acad. Sci. USA 91(20), 9342-9346 (1994).
Alvarez ME, Mccarthy CM. Glutamine synthetase from Mycobacterium avium. Can. J. Microbiol. 30(3), 353-359 (1984).
Bomberger JM, Maceachran DP, Coutermarsh BA, Ye S, O'toole GA, Stanton BA. Long-distance delivery of bacterial virulence factors by Pseudomonas aeruginosa outer membrane vesicles. PLoS Pathog. 5(4), e1000382 (2009).
Kesty NC, Mason KM, Reedy M, Miller SE, Kuehn MJ. Enterotoxigenic Escherichia coli vesicles target toxin delivery into mammalian cells. EMBO J. 23(23), 4538-4549 (2004).
Vanaja SK, Russo AJ, Behl B et al. Bacterial outer membrane vesicles mediate cytosolic localization of LPS and caspase-11 activation. Cell 165(5), 1106-1119 (2016).
Catherinot E, Roux AL, Vibet MA et al. Mycobacterium avium and Mycobacterium abscessus complex target distinct cystic fibrosis patient subpopulations. J. Cyst. Fibros. 12(1), 74-80 (2013).
Parsek MR, Greenberg EP. Sociomicrobiology: the connections between quorum sensing and biofilms. Trends Microbiol. 13(1), 27-33 (2005).
Turnbull L, Toyofuku M, Hynen AL et al. Explosive cell lysis as a mechanism for the biogenesis of bacterial membrane vesicles and biofilms. Nat. Commun. 7, 11220 (2016).
Polkade AV, Mantri SS, Patwekar UJ, Jangid K. Quorum sensing: an under-explored phenomenon in the phylum actinobacteria. Front. Microbiol. 7, 131 (2016).
Watson RO, Bell SL, Macduff DA et al. The cytosolic sensor cGAS detects Mycobacterium tuberculosis DNA to induce type I interferons and activate autophagy. Cell Host Microbe 17(6), 811-819 (2015).
Manzanillo PS, Shiloh MU, Portnoy DA, Cox JS. Mycobacterium tuberculosis activates the DNA-dependent cytosolic surveillance pathway within macrophages. Cell Host Microbe 11(5), 469-480 (2012).
