Mycobacterium abscessus cording prevents phagocytosis and promotes abscess formation

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 10, 2014, Pages

  Bernut, Audrey ^a   Herrmann, Jean Louis ^b   Kissa, Karima ^a,c   Dubremetz, Jean François ^a   Gaillard, Jean Louis ^b   Lutfalla, Georges ^a   Kremer, Laurent ^a,c  

^a UNIVERSITÉ DE MONTPELLIER   (France)

^b Laboratoire de Microbiologie   (France)

^c INSERM   (France)

Author keywords

Granuloma; Innate immunity; Morphotype; Pathogenesis

Indexed keywords

ABSCESS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; CONTROLLED STUDY; EMBRYO; IMMUNE EVASION; IN VIVO STUDY; MACROPHAGE; MYCOBACTERIOSIS; MYCOBACTERIUM ABSCESSUS; MYCOBACTERIUM ABSCESSUS INFECTION; NONHUMAN; PATHOGENICITY; PATHOPHYSIOLOGY; PHAGOCYTOSIS; PRIORITY JOURNAL; ZEBRA FISH;

GRANULOMA; INNATE IMMUNITY; MORPHOTYPE; PATHOGENESIS;

ABSCESS; ANIMALS; CLODRONIC ACID; CORD FACTORS; DNA PRIMERS; EMBRYO, NONMAMMALIAN; GLYCOLIPIDS; GLYCOPEPTIDES; HISTOCYTOCHEMISTRY; IMAGE PROCESSING, COMPUTER-ASSISTED; IMMUNOLOGIC FACTORS; MACROPHAGES; MICROSCOPY, FLUORESCENCE; MORPHOLINOS; MYCOBACTERIUM; MYCOBACTERIUM INFECTIONS; PHAGOCYTOSIS; VIRULENCE; ZEBRAFISH;

EID: 84896286449     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1321390111     Document Type: Article

References (62)

1. Brown-Elliott BA, Wallace RJ, Jr. (2002) Clinical and taxonomic status of pathogenic non-pigmented or late-pigmenting rapidly growing mycobacteria. Clin Microbiol Rev 15(4): 716-746.
2. Wallace RG, Jr., Silcox V, Brown BA (1994) Taxonomy of rapidly growing mycobacteria. Clin Infect Dis 18(1):121-122.
3. Olivier KN, et al.; Nontuberculous Mycobacteria in Cystic Fibrosis Study Group (2003) Nontuberculous mycobacteria. I: Multicenter prevalence study in cystic fibrosis. Am J Respir Crit Care Med 167(6):828-834.
4. Jönsson BE, et al. (2007) Molecular epidemiology of Mycobacterium abscessus, with focus on cystic fibrosis. J Clin Microbiol 45(5):1497-1504.
5. Roux AL, et al.; Jean-Louis Herrmann for the OMA Group (2009) Multicenter study of prevalence of nontuberculous mycobacteria in patients with cystic fibrosis in france. J Clin Microbiol 47(12):4124-4128.
6. Sermet-Gaudelus I, et al. (2003) Mycobacterium abscessus and children with cystic fibrosis. Emerg Infect Dis 9(12):1587-1591.
7. Medjahed H, Gaillard JL, Reyrat JM (2010) Mycobacterium abscessus: A new player in the mycobacterial field. Trends Microbiol 18(3): 117-123.
8. Byrd TF, Lyons CR (1999) Preliminary characterization of a Mycobacterium ab scessus mutant in human and murine models of infection. Infect Immun 67(9): 4700-4707.
9. Catherinot E, et al. (2007) Hypervirulence of a rough variant of the Mycobacterium abscessus type strain. Infect Immun 75(2):1055-1058.
10. Cullen AR, Cannon CL, Mark EJ, Colin AA (2000) Mycobacterium abscessus infection in cystic fibrosis. Colonization or infection? Am J Respir Crit Care Med 161(2 Pt 1): 641-645.
11. Catherinot E, et al. (2009) Acute respiratory failure involving an R variant of Myco bacterium abscessus. J Clin Microbiol 47(1):271-274.
12. Howard ST, et al. (2006) Spontaneous reversion of Mycobacterium abscessus from a smooth to a rough morphotype is associated with reduced expression of glyco-peptidolipid and reacquisition of an invasive phenotype. Microbiology 152(Pt 6): 1581-1590.
13. Cortes M, et al. (2011) Conditional gene expression in Mycobacterium abscessus. PLoS ONE 6(b):e29306.
14. Medjahed H, Reyrat JM (2009) Construction of Mycobacterium abscessus defined glycopeptidolipid mutants: Comparison of genetic tools. Appl Environ Microbiol 75(5):1331-1338.
15. Ripoll F, et al. (2009) Non mycobacterial virulence genes in the genome of the emerging pathogen Mycobacterium abscessus. PLoS ONE 4(6):e5660.
16. Zerihun MA, Hjortaas MJ, Falk K, Colquhoun DJ (2011) Immunohistochemical and Taqman real-time PCR detection of mycobacterial infections in fish. J Fish Dis 34(3): 235-246.
17. Jacobs JM, Stine CB, Baya AM, Kent ML (2009) A review of mycobacteriosis in marine fish. J Fish Dis 32(2):119-130.
18. Kang GC, Gan AW, Yam A, Tan AB, Tay SC (2010) Mycobacterium abscessus Hand infections in immunocompetent fish handlers: Case Report. J Hand Surg Am 35(7): 1142-1145.
19. Davis JM, et al. (2002) Real-time visualization of mycobacterium- macrophage inter actions leading to initiation of granuloma formation in zebrafish embryos. Immunity 17(6):693-702.
20. van der Sar AM, Appelmelk BJ, Vandenbroucke-Grauls CM, Bitter W (2004) A star with stripes: Zebrafish as an infection model. Trends Microbiol 12(10):451-457.
21. Clay H, Volkman HE, Ramakrishnan L (2008) Tumor necrosis factor signaling mediates resistance to mycobacteria by inhibiting bacterial growth and macrophage death. Immunity 29(2):283-294.
22. Prajsnar TK, Cunliffe VT, Foster SJ, Renshaw SA (2008) A novel vertebrate model of Staphylococcus aureus infection reveals phagocyte-dependent resistance of zebrafish to non-host specialized pathogens. Cell Microbiol 10(11):2312-2325.
23. Levraud JP, et al. (2009) Real-time observation of listeria monocytogenes-phagocyte interactions in living zebrafish larvae. Infect Immun 77(9):3651-3660.
24. Alibaud L, et al. (2011) A Mycobacterium marinum TesA mutant defective for major cell wall-associated lipids is highly attenuated in Dictyostelium discoideum and ze brafish embryos. Mol Microbiol 80(4):919-934.
25. Vergunst AC, Meijer AH, Renshaw SA O'Callaghan D (2010) Burkholderia cenocepacia creates an intramacrophage replication niche in zebrafish embryos, followed by bacterial dissemination and establishment of systemic infection. Infect Immun 78(4):1495-1508.
26. Berg RD, Ramakrishnan L (2012) Insights into tuberculosis from the zebrafish model. Trends Mol Med 18(12):689-690.
27. Tobin DM, et al. (2010) The lta4h locus modulates susceptibility to mycobacterial in fection in zebrafish and humans. Cell 140(5):717-730.
28. Davis JM, Ramakrishnan L (2009) The role of the granuloma in expansion and dis semination of early tuberculous infection. Cell 136(1):37-49.
29. Adams KN, et al. (2011) Drug tolerance in replicating mycobacteria mediated by a macrophage-induced efflux mechanism. Cell 145(1):39-53.
30. Volkman HE, et al. (2004) Tuberculous granuloma formation is enhanced by a myco bacterium virulence determinant. PLoS Biol 2(11):e367.
31. Adékambi T, et al. (2004) Amoebal coculture of "Mycobacterium massiliense" sp. Nov. from the sputum of a patient with hemoptoic pneumonia. J Clin Microbiol 42(12):5493-5501.
32. Adékambi T, Berger P, Raoult D, Drancourt M (2006) rpoB gene sequence-based characterization of emerging non-tuberculous mycobacteria with descriptions of Mycobacterium bolletii sp. nov., Mycobacterium phocaicum sp. Nov. and Mycobacterium aubagnense sp. Nov. IntJ Syst Evol Microbiol 56(Pt 1):133-143.
33. Sánchez-Chardi A, et al. (2011) Demonstration of cord formation by rough Myco bacterium abscessus variants: Implications for the clinical microbiology laboratory. J Clin Microbiol 49(6):2293-2295.
34. Pawlik A, et al. (2013) Identification and characterization of the genetic changes responsible for the characteristic smooth-to-rough morphotype alterations of clini cally persistent Mycobacterium abscessus. Mol Microbiol 90(3):612-629.
35. Roux AL, et al. (2011) Overexpression of proinflammatory TLR-2-signalling lip-oproteins in hypervirulent mycobacterial variants. Cell Microbiol 13(5):692-704.
36. Van Rooijen N, Sanders A (1994) Liposome mediated depletion of macrophages: Mechanism of action, preparation of liposomes and applications. J Immunol Methods 174(1-2):83-93.
37. Clay H, et al. (2007) Dichotomous role of the macrophage in early Mycobacterium marinum infection of the zebrafish. Cell Host Microbe 2(1):29-39.
38. Cosma CL, Klein K, Kim R, Beery D, Ramakrishnan L (2006) Mycobacterium marinum Erp is a virulence determinant required for cell wall integrity and intracellular sur vival. Infect Immun 74(6):3125-3133.
39. Talati NJ, Rouphael N, Kuppalli K, Franco-Paredes C (2008) Spectrum of CNS disease caused by rapidly growing mycobacteria. Lancet Infect Dis 8(6):390-398.
40. Lee MR, et al. (2012) CNS infections caused by Mycobacterium abscessus complex: Clinical features and antimicrobial susceptibilities of isolates. J Antimicrob Chemother 67(1):222-225.
41. Herbomel P, Thisse B, Thisse C (1999) Ontogeny and behaviour of early macrophages in the zebrafish embryo. Development 126(17):3735-3745.
42. Runyon EH (1959) Anonymous mycobacteria in pulmonary disease. Med Clin North Am43(1):273-290.
43. Recht J, Martínez A, Torello S, Kolter R (2000) Genetic analysis of sliding motility in Mycobacterium smegmatis. J Bacteriol 182(15):4348-4351.
44. Recht J, Kolter R (2001) Glycopeptidolipid acetylation affects sliding motility and bi-ofilm formation in Mycobacterium smegmatis. J Bacteriol 183(19):5718-5724.
45. Rhoades ER, et al. (2009) Mycobacterium abscessus Glycopeptidolipids mask un derlying cell wall phosphatidyl-myo-inositol mannosides blocking induction of human macrophage TNF-alpha by preventing interaction with TLR2. J Immunol 183(3): 1997-2007.
46. Glickman MS, Cox JS, Jacobs WR, Jr. (2000) A novel mycolic acid cyclopropane syn-thetase is required for cording, persistence, and virulence of Mycobacterium tuber culosis. Mol Cell 5(4):717-727.
47. Grosset J (2003) Mycobacterium tuberculosis in the extracellular compartment: An underestimated adversary. Antimicrob Agents Chemother 47(3):833-836.
48. Weiser JN (2013) The battle with the host over microbial size. Curr Opin Microbiol 16(1):59-62.
49. Justice SS, Hunstad DA, Cegelski L, Hultgren SJ (2008) Morphological plasticity as a bacterial survival strategy. Nat Rev Microbiol 6(2):162-168.
50. Horvath DJ, Jr., et al. (2011) Morphological plasticity promotes resistance to phago cyte killing of uropathogenic Escherichia coli. Microbes Infect 13(5):426-437.
51. Corrales RM, et al. (2012) Phosphorylation of mycobacterial PcaA inhibits mycolic acid cyclopropanation: Consequences for intracellular survival and for phagosome matu ration block. JBiolChem 287(31):26187-26199.
52. Griffith DE, Girard WM, Wallace RJ, Jr. (1993) Clinical features of pulmonary disease caused by rapidly growing mycobacteria. An analysis of 154 patients. Am Rev Respir Dis 147(5):1271-1278.
53. Pierre-Audigier C, et al. (2005) Age-related prevalence and distribution of non-tuberculous mycobacterial species among patients with cystic fibrosis. J Clin Microbiol 43(7):3467-3470.
54. Govan JR, Deretic V (1996) Microbial pathogenesis in cystic fibrosis: Mucoid Pseudo-monas aeruginosa and Burkholderia cepacia. Microbiol Rev 60(3):539-574.
55. Govan JR, Fyfe JA (1978) Mucoid Pseudomonas aeruginosa and cystic fibrosis: Re sistance of the mucoid from to carbenicillin, flucloxacillin and tobramycin and the isolation of mucoid variants in vitro. J Antimicrob Chemother 4(3):233-240.
56. Phennicie RT, Sullivan MJ, Singer JT, Yoder JA, Kim CH (2010) Specific resistance to Pseudomonas aeruginosa infection in zebrafish is mediated by the cystic fibrosis transmembrane conductance regulator. Infect Immun 78(11):4542-4550.
57. Takaki K, Cosma CL, Troll MA, Ramakrishnan L (2012) An in vivo platform for rapid high-throughput antitubercular drug discovery. Cell Rep 2(1):175-184.
58. Stover CK, et al. (1991) New use of BCG for recombinant vaccines. Nature 351(6326): 456-460.
59. Lamason RL, et al. (2005) SLC24A5, a putative cation exchanger, affects pigmentation in zebrafish and humans. Science 310(5755):1782-1786.
60. Renshaw SA, et al. (2006) A transgenic zebrafish model of neutrophilic inflammation. Blood 108(13):3976-3978.
61. Jin SW, Beis D, Mitchell T, Chen JN, Stainier DY (2005) Cellular and molecular analyses of vascular tube and lumen formation in zebrafish. Development 132(23):5199-5209.
62. Giffard-Mena I, Charmantier G, Grousset E, Aujoulat F, Castille R (2006) Digestive tract ontogeny of Dicentrarchus labrax: Implication in osmoregulation. Dev Growth Differ 48(3):139-151.