The Role of Lipid Raft Aggregation in the Infection of Type II Pneumocytes by Mycobacterium tuberculosis

PLoS ONE

Volumn 7, Issue 9, 2012, Pages

  Fine Coulson, Kari ^a   Reaves, Barbara J ^a   Karls, Russell K ^a   Quinn, Frederick D ^a  

^a UNIVERSITY OF GEORGIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; FILIPIN; LIPID;

ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BIOACCUMULATION; BIOSYNTHESIS; CELL MEMBRANE; CELL SURVIVAL; CONTROLLED STUDY; DISEASE COURSE; GAMMA IRRADIATION; HOST CELL; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; INTERNALIZATION; LIPID RAFT; LUNG ALVEOLUS CELL TYPE 2; LUNG TUBERCULOSIS; MICROBIAL ACTIVITY; MTB GENE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN;

ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; CELL LINE; FILIPIN; GAMMA RAYS; HUMANS; MEMBRANE MICRODOMAINS; MYCOBACTERIUM TUBERCULOSIS; PHAGOCYTOSIS; PNEUMOCYTES; PROTEIN TRANSPORT; TOLL-LIKE RECEPTORS;

BACILLI (CLASS); MYCOBACTERIUM TUBERCULOSIS;

EID: 84866411764     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0045028     Document Type: Article

References (76)

1. Hauck FR, Neese BH, Panchal AS, El-Amin W, (2009) Identification and management of latent tuberculosis infection. Am Fam Physician 79: 879-886.
2. Sato K, Tomioka H, Shimizu T, Gonda T, Ota F, et al. (2002) Type II alveolar cells play roles in macrophage-mediated host innate resistance to pulmonary mycobacterial infections by producing proinflammatory cytokines. J Infect Dis 185: 1139-1147.
3. Bermudez LE, Goodman J, (1996) Mycobacterium tuberculosis invades and replicates within type II alveolar cells. Infect Immun 64: 1400-1406.
4. Kumari M, Saxena RK, (2011) Relative efficacy of uptake and presentation of Mycobacterium bovis BCG antigens by type I mouse lung epithelial cells and peritoneal macrophages. Infect Immun 79: 3159-3167.
5. Mehta PK, King CH, White EH, Murtagh JJ Jr, Quinn FD, (1996) Comparison of in vitro models for the study of Mycobacterium tuberculosis invasion and intracellular replication. Infect Immun 64: 2673-2679.
6. Fine KL, Metcalfe MG, White E, Virji M, Karls RK, et al. (2012) Involvement of the autophagy pathway in trafficking of Mycobacterium tuberculosis bacilli through cultured human type II epithelial cells. Cell Microbiol. doi:10.1111/j.1462-5822.2012.01804.
7. Ramakrishnan L, (2012) Revisiting the role of the granuloma in tuberculosis. Nat Rev Immunol 12: 352-366.
8. Wickremasinghe MI, Thomas LH, Friedland JS, (1999) Pulmonary epithelial cells are a source of IL-8 in the response to Mycobacterium tuberculosis: essential role of IL-1 from infected monocytes in a NF-kappa B-dependent network. J Immunol 163: 3936-3947.
9. Roy S, Sharma S, Sharma M, Aggarwal R, Bose M, (2004) 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.
10. Nichols B, (2003) Caveosomes and endocytosis of lipid rafts. J Cell Sci 116: 4707-4714.
11. Triantafilou M, Morath S, Mackie A, Hartung T, Triantafilou K, (2004) Lateral diffusion of Toll-like receptors reveals that they are transiently confined within lipid rafts on the plasma membrane. J Cell Sci 117: 4007-4014.
12. Lingwood D, Simons K, (2010) Lipid rafts as a membrane-organizing principle. Science 327: 46-50.
13. Pralle A, Keller P, Florin EL, Simons K, Horber JK, (2000) Sphingolipid-cholesterol rafts diffuse as small entities in the plasma membrane of mammalian cells. J Cell Biol 148: 997-1008.
14. Sharma P, Varma R, Sarasij RC, Ira, Gousset K, et al. (2004) Nanoscale organization of multiple GPI-anchored proteins in living cell membranes. Cell 116: 577-589.
15. Gekara NO, Jacobs T, Chakraborty T, Weiss S, (2005) The cholesterol-dependent cytolysin listeriolysin O aggregates rafts via oligomerization. Cell Microbiol 7: 1345-1356.
16. Popik W, Alce TM, Au WC, (2002) Human immunodeficiency virus type 1 uses lipid raft-colocalized CD4 and chemokine receptors for productive entry into CD4(+) T cells. J Virol 76: 4709-4722.
17. Kowalski MP, Pier GB, (2004) Localization of cystic fibrosis transmembrane conductance regulator to lipid rafts of epithelial cells is required for Pseudomonas aeruginosa-induced cellular activation. J Immunol 172: 418-425.
18. Rogee S, Grellier E, Bernard C, Loyens A, Beauvillain JC, et al. (2007) Intracellular trafficking of a fiber-modified adenovirus using lipid raft/caveolae endocytosis. Mol Ther 15: 1963-1972.
19. Gajate C, Gonzalez-Camacho F, Mollinedo F, (2009) Involvement of raft aggregates enriched in Fas/CD95 death-inducing signaling complex in the antileukemic action of edelfosine in Jurkat cells. PLoS One 4: e5044.
20. Xu ZX, Ding T, Haridas V, Connolly F, Gutterman JU, (2009) Avicin D, a plant triterpenoid, induces cell apoptosis by recruitment of Fas and downstream signaling molecules into lipid rafts. PLoS One 4: e8532.
21. Barman S, Adhikary L, Chakrabarti AK, Bernas C, Kawaoka Y, et al. (2004) Role of transmembrane domain and cytoplasmic tail amino acid sequences of influenza a virus neuraminidase in raft association and virus budding. J Virol 78: 5258-5269.
22. Hurley JH, Boura E, Carlson LA, Rozycki B, (2010) Membrane budding. Cell 143: 875-887.
23. Lencer WI, Hirst TR, Holmes RK, (1999) Membrane traffic and the cellular uptake of cholera toxin. Biochim Biophys Acta 1450: 177-190.
24. Hansen CG, Nichols BJ, (2010) Exploring the caves: cavins, caveolins and caveolae. Trends Cell Biol 20: 177-186.
25. Lim JS, Choy HE, Park SC, Han JM, Jang IS, et al. (2010) Caveolae-mediated entry of Salmonella typhimurium into senescent nonphagocytotic host cells. Aging Cell 9: 243-251.
26. Duncan MJ, Li G, Shin JS, Carson JL, Abraham SN, (2004) Bacterial penetration of bladder epithelium through lipid rafts. J Biol Chem 279: 18944-18951.
27. Zaas DW, Duncan MJ, Li G, Wright JR, Abraham SN, (2005) Pseudomonas invasion of type I pneumocytes is dependent on the expression and phosphorylation of caveolin-2. J Biol Chem 280: 4864-4872.
28. Zaas DW, Swan ZD, Brown BJ, Li G, Randell SH, et al. (2009) Counteracting signaling activities in lipid rafts associated with the invasion of lung epithelial cells by Pseudomonas aeruginosa. J Biol Chem 284: 9955-9964.
29. Zaas DW, Duncan M, Rae Wright J, Abraham SN, (2005) The role of lipid rafts in the pathogenesis of bacterial infections. Biochim Biophys Acta 1746: 305-313.
30. Shin DM, Yang CS, Lee JY, Lee SJ, Choi HH, et al. (2008) Mycobacterium tuberculosis lipoprotein-induced association of TLR2 with protein kinase C zeta in lipid rafts contributes to reactive oxygen species-dependent inflammatory signalling in macrophages. Cell Microbiol 10: 1893-1905.
31. Gatfield J, Pieters J, (2000) Essential role for cholesterol in entry of mycobacteria into macrophages. Science 288: 1647-1650.
32. Munoz S, Rivas-Santiago B, Enciso JA, (2009) Mycobacterium tuberculosis entry into mast cells through cholesterol-rich membrane microdomains. Scand J Immunol 70: 256-263.
33. Welin A, Winberg ME, Abdalla H, Sarndahl E, Rasmusson B, et al. (2008) Incorporation of Mycobacterium tuberculosis lipoarabinomannan into macrophage membrane rafts is a prerequisite for the phagosomal maturation block. Infect Immun 76: 2882-2887.
34. Hayakawa E, Tokumasu F, Nardone GA, Jin AJ, Hackley VA, et al. (2007) A Mycobacterium tuberculosis-derived lipid inhibits membrane fusion by modulating lipid membrane domains. Biophys J 93: 4018-4030.
35. Manca C, Tsenova L, Barry CE, 3rd, Bergtold A, Freeman S, et al (1999) Mycobacterium tuberculosis CDC1551 induces a more vigorous host response in vivo and in vitro, but is not more virulent than other clinical isolates. J Immunol 162: 6740-6746.
36. Barczak AK, Domenech P, Boshoff HI, Reed MB, Manca C, et al. (2005) In vivo phenotypic dominance in mouse mixed infections with Mycobacterium tuberculosis clinical isolates. J Infect Dis 192: 600-606.
37. Tsenova L, Ellison E, Harbacheuski R, Moreira AL, Kurepina N, et al. (2005) Virulence of selected Mycobacterium tuberculosis clinical isolates in the rabbit model of meningitis is dependent on phenolic glycolipid produced by the bacilli. J Infect Dis 192: 98-106.
38. Kremer L, Guerardel Y, Gurcha SS, Locht C, Besra GS, (2002) Temperature-induced changes in the cell-wall components of Mycobacterium thermoresistibile. Microbiology 148: 3145-3154.
39. Kalia A, Rattan A, Chopra P, (1999) A method for extraction of high-quality and high-quantity genomic DNA generally applicable to pathogenic bacteria. Anal Biochem 275: 1-5.
40. Constant P, Perez E, Malaga W, Laneelle MA, Saurel O, et al. (2002) Role of the pks15/1 gene in the biosynthesis of phenolglycolipids in the Mycobacterium tuberculosis complex. Evidence that all strains synthesize glycosylated p-hydroxybenzoic methyl esters and that strains devoid of phenolglycolipids harbor a frameshift mutation in the pks15/1 gene. J Biol Chem 277: 38148-38158.
41. Simons K, Ehehalt R, (2002) Cholesterol, lipid rafts, and disease. J Clin Invest 110: 597-603.
42. Drennan MB, Nicolle D, Quesniaux VJ, Jacobs M, Allie N, et al. (2004) Toll-like receptor 2-deficient mice succumb to Mycobacterium tuberculosis infection. Am J Pathol 164: 49-57.
43. Henning LN, Azad AK, Parsa KV, Crowther JE, Tridandapani S, et al. (2008) Pulmonary surfactant protein A regulates TLR expression and activity in human macrophages. J Immunol 180: 7847-7858.
44. Orlandi PA, Fishman PH, (1998) Filipin-dependent inhibition of cholera toxin: evidence for toxin internalization and activation through caveolae-like domains. J Cell Biol 141: 905-915.
45. Pike LJ, (2009) The challenge of lipid rafts. J Lipid Res 50Suppl: S323-328.
46. Amer AO, Byrne BG, Swanson MS, (2005) Macrophages rapidly transfer pathogens from lipid raft vacuoles to autophagosomes. Autophagy 1: 53-58.
47. Togayachi A, Kozono Y, Ikehara Y, Ito H, Suzuki N, et al. (2010) Lack of lacto/neolacto-glycolipids enhances the formation of glycolipid-enriched microdomains, facilitating B cell activation. Proc Natl Acad Sci U S A 107: 11900-11905.
48. French CT, Panina EM, Yeh SH, Griffith N, Arambula DG, et al. (2009) The Bordetella type III secretion system effector BteA contains a conserved N-terminal motif that guides bacterial virulence factors to lipid rafts. Cell Microbiol 11: 1735-1749.
49. Yu C, Alterman M, Dobrowsky RT, (2005) Ceramide displaces cholesterol from lipid rafts and decreases the association of the cholesterol binding protein caveolin-1. J Lipid Res 46: 1678-1691.
50. Rothberg KG, Heuser JE, Donzell WC, Ying YS, Glenney JR, et al. (1992) Caveolin, a protein component of caveolae membrane coats. Cell 68: 673-682.
51. Cohen AW, Hnasko R, Schubert W, Lisanti MP, (2004) Role of caveolae and caveolins in health and disease. Physiol Rev 84: 1341-1379.
52. Le Lay S, Li Q, Proschogo N, Rodriguez M, Gunaratnam K, et al. (2009) Caveolin-1-dependent and-independent membrane domains. J Lipid Res 50: 1609-1620.
53. Patel HH, Insel PA, (2009) Lipid rafts and caveolae and their role in compartmentation of redox signaling. Antioxid Redox Signal 11: 1357-1372.
54. Radeva G, Perabo J, Sharom FJ, (2005) P-Glycoprotein is localized in intermediate-density membrane microdomains distinct from classical lipid rafts and caveolar domains. FEBS J 272: 4924-4937.
55. Querbes W, O'Hara BA, Williams G, Atwood WJ, (2006) Invasion of host cells by JC virus identifies a novel role for caveolae in endosomal sorting of noncaveolar ligands. J Virol 80: 9402-9413.
56. Tahir SA, Yang G, Goltsov AA, Watanabe M, Tabata K, et al. (2008) Tumor cell-secreted caveolin-1 has proangiogenic activities in prostate cancer. Cancer Res 68: 731-739.
57. Parton RG, Richards AA, (2003) Lipid rafts and caveolae as portals for endocytosis: new insights and common mechanisms. Traffic 4: 724-738.
58. Zheng YZ, Boscher C, Inder KL, Fairbank M, Loo D, et al. (2011) Differential impact of caveolae and caveolin-1 scaffolds on the membrane raft proteome. Mol Cell Proteomics 10: M110 007146.
59. Janes PW, Ley SC, Magee AI, Kabouridis PS, (2000) The role of lipid rafts in T cell antigen receptor (TCR) signalling. Semin Immunol 12: 23-34.
60. Young RM, Holowka D, Baird B, (2003) A lipid raft environment enhances Lyn kinase activity by protecting the active site tyrosine from dephosphorylation. J Biol Chem 278: 20746-20752.
61. Mitchell JS, Brown WS, Woodside DG, Vanderslice P, McIntyre BW, (2009) Clustering T-cell GM1 lipid rafts increases cellular resistance to shear on fibronectin through changes in integrin affinity and cytoskeletal dynamics. Immunol Cell Biol 87: 324-336.
62. Ordway D, Henao-Tamayo M, Harton M, Palanisamy G, Troudt J, et al. (2007) The hypervirulent Mycobacterium tuberculosis strain HN878 induces a potent TH1 response followed by rapid down-regulation. J Immunol 179: 522-531.
63. Reed MB, Domenech P, Manca C, Su H, Barczak AK, et al. (2004) A glycolipid of hypervirulent tuberculosis strains that inhibits the innate immune response. Nature 431: 84-87.
64. Sinsimer D, Huet G, Manca C, Tsenova L, Koo MS, et al. (2008) The phenolic glycolipid of Mycobacterium tuberculosis differentially modulates the early host cytokine response but does not in itself confer hypervirulence. Infect Immun 76: 3027-3036.
65. Regueiro V, Moranta D, Campos MA, Margareto J, Garmendia J, et al. (2009) Klebsiella pneumoniae increases the levels of Toll-like receptors 2 and 4 in human airway epithelial cells. Infect Immun 77: 714-724.
66. Goluszko P, Nowicki B, (2005) Membrane cholesterol: a crucial molecule affecting interactions of microbial pathogens with mammalian cells. Infect Immun 73: 7791-7796.
67. Lafont F, van der Goot FG, (2005) Bacterial invasion via lipid rafts. Cell Microbiol 7: 613-620.
68. Kaksonen M, Toret CP, Drubin DG, (2006) Harnessing actin dynamics for clathrin-mediated endocytosis. Nat Rev Mol Cell Biol 7: 404-414.
69. de Chastellier C, Thilo L, (2006) Cholesterol depletion in Mycobacterium avium-infected macrophages overcomes the block in phagosome maturation and leads to the reversible sequestration of viable mycobacteria in phagolysosome-derived autophagic vacuoles. Cell Microbiol 8: 242-256.
70. Ros-Baro A, Lopez-Iglesias C, Peiro S, Bellido D, Palacin M, et al. (2001) Lipid rafts are required for GLUT4 internalization in adipose cells. Proc Natl Acad Sci U S A 98: 12050-12055.
71. Auriac A, Willemetz A, Canonne-Hergaux F, (2010) Lipid raft-dependent endocytosis: a new route for hepcidin-mediated regulation of ferroportin in macrophages. Haematologica 95: 1269-1277.
72. Drake DR, 3rd, Braciale TJ (2001) Cutting edge: lipid raft integrity affects the efficiency of MHC class I tetramer binding and cell surface TCR arrangement on CD8+ T cells. J Immunol 166: 7009-7013.
73. Dobos KM, Spotts EA, Quinn FD, King CH, (2000) Necrosis of lung epithelial cells during infection with Mycobacterium tuberculosis is preceded by cell permeation. Infect Immun 68: 6300-6310.
74. Dao DN, Sweeney K, Hsu T, Gurcha SS, Nascimento IP, et al. (2008) Mycolic acid modification by the mmaA4 gene of M. tuberculosis modulates IL-12 production. PLoS Pathog 4: e1000081.
75. Rocha-Ramirez LM, Estrada-Garcia I, Lopez-Marin LM, Segura-Salinas E, Mendez-Aragon P, et al. (2008) Mycobacterium tuberculosis lipids regulate cytokines, TLR-2/4 and MHC class II expression in human macrophages. Tuberculosis (Edinb) 88: 212-220.
76. Abramoff MD, Magelhaes PJ, Ram SJ, (2004) Image Processing with ImageJ. Biophotonics International 11: 36-42.