Surface hydrolysis of sphingomyelin by the outer membrane protein Rv0888 supports replication of Mycobacterium tuberculosis in macrophages

Molecular Microbiology

Volumn 97, Issue 5, 2015, Pages 881-897

  Speer, Alexander ^a   Sun, Jim ^a   Danilchanka, Olga ^a,f   Meikle, Virginia ^a   Rowland, Jennifer L ^a,g   Walter, Kerstin ^b,c   Buck, Bradford R ^a   Pavlenok, Mikhail ^a   Hölscher, Christoph ^b,c,d   Ehrt, Sabine ^e   Niederweis, Michael ^a  

^a University of Alabama at Birmingham   (United States)

^b RESEARCH CENTER BORSTEL   (Germany)

^c German Center for Infection Research   (Germany)

^d UNIVERSITY OF KIEL   (Germany)

^e WEILL CORNELL MEDICAL COLLEGE   (United States)

^f HARVARD MEDICAL SCHOOL   (United States)

^g UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON; CERAMIDE; GLUCOSE; NITROGEN; OUTER MEMBRANE PROTEIN; PHOSPHORUS; PHOSPHORYLCHOLINE; PORIN; PROTEIN RV0888; SPHINGOMYELIN; SPHINGOMYELIN PHOSPHODIESTERASE; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL GROWTH; CARBON SOURCE; CARBOXY TERMINAL SEQUENCE; DELETION MUTANT; ENZYME ACTIVITY; ERYTHROCYTE; ERYTHROCYTE MEMBRANE; EUKARYOTIC CELL; GLUCOSE TRANSPORT; HEMOLYSIS; LIPID HYDROLYSIS; MACROPHAGE; MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FOLDING; CELL CULTURE; CHEMISTRY; GENE DELETION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HOST PATHOGEN INTERACTION; HUMAN; HYDROLYSIS; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PHAGOCYTOSIS;

EUKARYOTA; MYCOBACTERIUM TUBERCULOSIS;

BACTERIAL OUTER MEMBRANE PROTEINS; CELLS, CULTURED; CERAMIDES; ERYTHROCYTE MEMBRANE; HEMOLYSIS; HOST-PATHOGEN INTERACTIONS; HUMANS; HYDROLYSIS; MACROPHAGES; MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS; PHAGOCYTOSIS; PHOSPHORYLCHOLINE; PORINS; SEQUENCE DELETION; SPHINGOMYELINS;

EID: 84939832530     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.13073     Document Type: Article

References (89)

1. Barry, C.E., 3rd, Boshoff, H.I., Dartois, V., Dick, T., Ehrt, S., Flynn, J., etal. (2009) The spectrum of latent tuberculosis: rethinking the biology and intervention strategies. Nat Rev Microbiol 7: 845-855.
2. Bernheimer, A.W., Avigad, L.S., and Kim, K.S. (1974) Staphylococcal sphingomyelinase (beta-hemolysin). Ann N Y Acad Sci 236: 292-306.
3. Blasband, A.J., Marcotte, W.R., Jr, and Schnaitman, C.A. (1986) Structure of the lc and nmpC outer membrane porin protein genes of lambdoid bacteriophage. J Biol Chem 261: 12723-12732.
4. Boritsch, E.C., Supply, P., Honore, N., Seeman, T., Stinear, T.P., and Brosch, R. (2014) A glimpse into the past and predictions for the future: the molecular evolution of the tuberculosis agent. Mol Microbiol 93: 835-852.
5. Boshoff, H.I., Myers, T.G., Copp, B.R., McNeil, M.R., Wilson, M.A., and Barry, C.E., 3rd (2004) The transcriptional responses of Mycobacterium tuberculosis to inhibitors of metabolism: novel insights into drug mechanisms of action. J Biol Chem 279: 40174-40184.
6. Brennan, P.J., and Nikaido, H. (1995) The envelope of mycobacteria. Annu Rev Biochem 64: 29-63.
7. Cao, Y., and Bazemore-Walker, C.R. (2014) Proteomic profiling of the surface-exposed cell envelope proteins of Caulobacter crescentus. J Proteomics 97: 187-194.
8. Clarke, C.J., Snook, C.F., Tani, M., Matmati, N., Marchesini, N., and Hannun, Y.A. (2006) The extended family of neutral sphingomyelinases. Biochemistry 45: 11247-11256.
9. Cole, C., Barber, J.D., and Barton, G.J. (2008) The Jpred 3 secondary structure prediction server. Nucleic Acids Res 36: W197-W201.
10. Danilchanka, O., Mailaender, C., and Niederweis, M. (2008a) Identification of a novel multidrug efflux pump of Mycobacterium tuberculosis. Antimicrob Agents Chemother 52: 2503-2511.
11. Danilchanka, O., Pavlenok, M., and Niederweis, M. (2008b) Role of porins for uptake of antibiotics by Mycobacterium smegmatis. Antimicrob Agents Chemother 52: 3127-3134.
12. Danilchanka, O., Sun, J., Pavlenok, M., Maueroder, C., Speer, A., Siroy, A., etal. (2014) An outer membrane channel protein of Mycobacterium tuberculosis with exotoxin activity. Proc Natl Acad Sci USA 111: 6750-6755.
13. Danilchanka, O., Pires, D., Anes, E., and Niederweis, M. (2015) The Mycobacterium tuberculosis outer membrane channel protein CpnT confers susceptibility to toxic molecules. Antimicrob Agents Chemother 59: 2328-2336.
14. Doll, V.M., Ehling-Schulz, M., and Vogelmann, R. (2013) Concerted action of sphingomyelinase and non-hemolytic enterotoxin in pathogenic Bacillus cereus. PLoS ONE 8: e61404.
15. Domenech, P., and Reed, M.B. (2009) Rapid and spontaneous loss of phthiocerol dimycocerosate (PDIM) from Mycobacterium tuberculosis grown in vitro: implications for virulence studies. Microbiology 155: 3532-3543.
16. Dubos, R.J. (1948) The effect of sphingomyelin on the growth of tubercle bacilli. J Exp Med 88: 73-79.
17. Ehrt, S., and Rhee, K. (2013) Mycobacterium tuberculosis metabolism and host interaction: mysteries and paradoxes. Curr Top Microbiol Immunol 374: 163-188.
18. Fabrino, D.L., Bleck, C.K., Anes, E., Hasilik, A., Melo, R.C., Niederweis, M., etal. (2009) Porins facilitate nitric oxide-mediated killing of mycobacteria. Microbes Infect 11: 868-875.
19. Fajardo, D.A., Cheung, J., Ito, C., Sugawara, E., Nikaido, H., and Misra, R. (1998) Biochemistry and regulation of a novel Escherichia coli K-12 porin protein, OmpG, which produces unusually large channels. J Bacteriol 180: 4452-4459.
20. Finn, R.D., Bateman, A., Clements, J., Coggill, P., Eberhardt, R.Y., Eddy, S.R., etal. (2014) Pfam: the protein families database. Nucleic Acids Res 42: D222-D230.
21. Galagan, J.E., Sisk, P., Stolte, C., Weiner, B., Koehrsen, M., Wymore, F., etal. (2010) TB database 2010: overview and update. Tuberculosis (Edinb) 90: 225-235.
22. Gaus, K., Rodriguez, M., Ruberu, K.R., Gelissen, I., Sloane, T.M., Kritharides, L., and Jessup, W. (2005) Domain-specific lipid distribution in macrophage plasma membranes. J Lipid Res 46: 1526-1538.
23. Gonzalez-Zorn, B., Dominguez-Bernal, G., Suarez, M., Ripio, M.T., Vega, Y., Novella, S., and Vazquez-Boland, J.A. (1999) The smcL gene of Listeria ivanovii encodes a sphingomyelinase C that mediates bacterial escape from the phagocytic vacuole. Mol Microbiol 33: 510-523.
24. Griffin, J.E., Gawronski, J.D., Dejesus, M.A., Ioerger, T.R., Akerley, B.J., and Sassetti, C.M. (2011) High-resolution phenotypic profiling defines genes essential for mycobacterial growth and cholesterol catabolism. PLoS Pathog 7: e1002251.
25. He, X., Chen, F., McGovern, M.M., and Schuchman, E.H. (2002) A fluorescence-based, high-throughput sphingomyelin assay for the analysis of Niemann-Pick disease and other disorders of sphingomyelin metabolism. Anal Biochem 306: 115-123.
26. Hoffmann, C., Leis, A., Niederweis, M., Plitzko, J.M., and Engelhardt, H. (2008) Disclosure of the mycobacterial outer membrane: cryo-electron tomography and vitreous sections reveal the lipid bilayer structure. Proc Natl Acad Sci USA 105: 3963-3967.
27. Huseby, M., Shi, K., Brown, C.K., Digre, J., Mengistu, F., Seo, K.S., etal. (2007) Structure and biological activities of beta toxin from Staphylococcus aureus. J Bacteriol 189: 8719-8726.
28. Ingraham, L.M., Burns, C.P., Boxer, L.A., Baehner, R.L., and Haak, R.A. (1981) Fluidity properties and liquid composition of erythrocyte membranes in Chediak-Higashi syndrome. J Cell Biol 89: 510-516.
29. Johansen, K.A., Gill, R.E., and Vasil, M.L. (1996) Biochemical and molecular analysis of phospholipase C and phospholipase D activity in mycobacteria. Infect Immun 64: 3259-3266.
30. Jones, C.M., and Niederweis, M. (2011) Mycobacterium tuberculosis can utilize heme as an iron source. J Bacteriol 193: 1767-1770.
31. Kartmann, B., Stenger, S., and Niederweis, M. (1999) Porins in the cell wall of Mycobacterium tuberculosis. J Bacteriol 181: 6543-6546. Authors' correction appeared in J. Bacteriol. 6181, 7650.
32. Keating, L.A., Wheeler, P.R., Mansoor, H., Inwald, J.K., Dale, J., Hewinson, R.G., and Gordon, S.V. (2005) The pyruvate requirement of some members of the Mycobacterium tuberculosis complex is due to an inactive pyruvate kinase: implications for in vivo growth. Mol Microbiol 56: 163-174.
33. Kennedy, G.M., Hooley, G.C., Champion, M.M., Mba Medie, F., and Champion, P.A. (2014) A novel ESX-1 locus reveals that surface-associated ESX-1 substrates mediate virulence in Mycobacterium marinum. J Bacteriol 196: 1877-1888.
34. Kiefer, F., Arnold, K., Kunzli, M., Bordoli, L., and Schwede, T. (2009) The SWISS-MODEL Repository and associated resources. Nucleic Acids Res 37: D387-D392.
35. King, C.H., Mundayoor, S., Crawford, J.T., and Shinnick, T.M. (1993) Expression of contact-dependent cytolytic activity by Mycobacterium tuberculosis and isolation of the genomic locus that encodes the activity. Infect Immun 61: 2708-2712.
36. Lambert, P.A. (2002) Cellular impermeability and uptake of biocides and antibiotics in Gram-positive bacteria and mycobacteria. J Appl Microbiol 92 (Suppl.): 46S-54S.
37. Leyton, D.L., Rossiter, A.E., and Henderson, I.R. (2012) From self sufficiency to dependence: mechanisms and factors important for autotransporter biogenesis. Nat Rev Microbiol 10: 213-225.
38. Lichtinger, T., Heym, B., Maier, E., Eichner, H., Cole, S.T., and Benz, R. (1999) Evidence for a small anion-selective channel in the cell wall of Mycobacterium bovis BCG besides a wide cation-selective pore. FEBS Lett 454: 349-355.
39. Lin, P.L., Rodgers, M., Smith, L., Bigbee, M., Myers, A., Bigbee, C., etal. (2009) Quantitative comparison of active and latent tuberculosis in the cynomolgus macaque model. Infect Immun 77: 4631-4642.
40. Lofthouse, E.K., Wheeler, P.R., Beste, D.J., Khatri, B.L., Wu, H., Mendum, T.A., etal. (2013) Systems-based approaches to probing metabolic variation within the Mycobacterium tuberculosis complex. PLoS ONE 8: e75913.
41. McDonel, J.L. (1980) Clostridium perfringens toxins (type A, B, C, D, E). Pharmacol Ther 10: 617-655.
42. Mailaender, C., Reiling, N., Engelhardt, H., Bossmann, S., Ehlers, S., and Niederweis, M. (2004) The MspA porin promotes growth and increases antibiotic susceptibility of both Mycobacterium bovis BCG and Mycobacterium tuberculosis. Microbiology 150: 853-864.
43. Marrero, J., Trujillo, C., Rhee, K.Y., and Ehrt, S. (2013) Glucose phosphorylation is required for Mycobacterium tuberculosis persistence in mice. PLoS Pathog 9: e1003116.
44. Neyrolles, O., Hernandez-Pando, R., Pietri-Rouxel, F., Fornes, P., Tailleux, L., Payan, J.A., etal. (2006) Is adipose tissue a place for Mycobacterium tuberculosis persistence? PLoS ONE 1: e43.
45. Neyrolles, O., Wolschendorf, F., Mitra, A., and Niederweis, M. (2014) Mycobacteria, metals and the macrophage. Immunol Rev 264: 249-263.
46. Neyrolles, O., Wolschendorf, F., Mitra, A., and Niederweis, M. (2015) Mycobacteria, metals, and the macrophage. Immunol Rev 264: 249-263.
47. Niederweis, M. (2008) Nutrient acquisition by mycobacteria. Microbiology 154: 679-692.
48. Niederweis, M., Danilchanka, O., Huff, J., Hoffmann, C., and Engelhardt, H. (2010) Mycobacterial outer membranes: in search of proteins. Trends Microbiol 18: 109-116.
49. Nikaido, H. (2003) Molecular basis of bacterial outer membrane permeability revisited. Microbiol Mol Biol Rev 67: 593-656.
50. Nikaido, H., and Jarlier, V. (1991) Permeability of the mycobacterial cell wall. Res Microbiol 142: 437-443.
51. Oda, M., Takahashi, M., Matsuno, T., Uoo, K., Nagahama, M., and Sakurai, J. (2010) Hemolysis induced by Bacillus cereus sphingomyelinase. Biochim Biophys Acta 1798: 1073-1080.
52. Oda, M., Hashimoto, M., Takahashi, M., Ohmae, Y., Seike, S., Kato, R., etal. (2012) Role of sphingomyelinase in infectious diseases caused by Bacillus cereus. PLoS ONE 7: e38054.
53. Pandey, A.K., and Sassetti, C.M. (2008) Mycobacterial persistence requires the utilization of host cholesterol. Proc Natl Acad Sci USA 105: 4376-4380.
54. Pandey, A.K., Raman, S., Proff, R., Joshi, S., Kang, C.M., Rubin, E.J., etal. (2009) Nitrile-inducible gene expression in mycobacteria. Tuberculosis (Edinb) 89: 12-16.
55. Parker, S.K., Barkley, R.M., Rino, J.G., and Vasil, M.L. (2009) Mycobacterium tuberculosis Rv3802c encodes a phospholipase/thioesterase and is inhibited by the antimycobacterial agent tetrahydrolipstatin. PLoS ONE 4: e4281.
56. Portevin, D., De Sousa-D'Auria, C., Houssin, C., Grimaldi, C., Chami, M., Daffe, M., and Guilhot, C. (2004) A polyketide synthase catalyzes the last condensation step of mycolic acid biosynthesis in mycobacteria and related organisms. Proc Natl Acad Sci USA 101: 314-319.
57. Prados-Rosales, R., Baena, A., Martinez, L.R., Luque-Garcia, J., Kalscheuer, R., Veeraraghavan, U., etal. (2011) Mycobacteria release active membrane vesicles that modulate immune responses in a TLR2-dependent manner in mice. J Clin Invest 121: 1471-1483.
58. Puckett, S., Trujillo, C., Eoh, H., Marrero, J., Spencer, J., Jackson, M., etal. (2014) Inactivation of fructose-1, 6-bisphosphate aldolase prevents optimal co-catabolism of glycolytic and gluconeogenic carbon substrates in Mycobacterium tuberculosis. PLoS Pathog 10: e1004144.
59. Ratledge, C. (2004) Iron, mycobacteria and tuberculosis. Tuberculosis 84: 110-130.
60. Raynaud, C., Guilhot, C., Rauzier, J., Bordat, Y., Pelicic, V., Manganelli, R., etal. (2002) Phospholipases C are involved in the virulence of Mycobacterium tuberculosis. Mol Microbiol 45: 203-217.
61. Rohde, K., Yates, R.M., Purdy, G.E., and Russell, D.G. (2007) Mycobacterium tuberculosis and the environment within the phagosome. Immunol Rev 219: 37-54.
62. Russell, D.G. (2011) Mycobacterium tuberculosis and the intimate discourse of a chronic infection. Immunol Rev 240: 252-268.
63. Russell, D.G., Cardona, P.J., Kim, M.J., Allain, S., and Altare, F. (2009) Foamy macrophages and the progression of the human tuberculosis granuloma. Nat Immunol 10: 943-948.
64. Russell, D.G., VanderVen, B.C., Lee, W., Abramovitch, R.B., Kim, M.J., Homolka, S., etal. (2010) Mycobacterium tuberculosis wears what it eats. Cell Host Microbe 8: 68-76.
65. Sassetti, C.M., and Rubin, E.J. (2003) Genetic requirements for mycobacterial survival during infection. Proc Natl Acad Sci USA 100: 12989-12994.
66. Schnappinger, D., Ehrt, S., Voskuil, M.I., Liu, Y., Mangan, J.A., Monahan, I.M., etal. (2003) Transcriptional adaptation of Mycobacterium tuberculosis within macrophages: insights into the phagosomal environment. J Exp Med 198: 693-704.
67. Simeone, R., Bobard, A., Lippmann, J., Bitter, W., Majlessi, L., Brosch, R., and Enninga, J. (2012) Phagosomal rupture by Mycobacterium tuberculosis results in toxicity and host cell death. PLoS Pathog 8: e1002507.
68. Skaar, E.P. (2010) The battle for iron between bacterial pathogens and their vertebrate hosts. PLoS Pathog 6: e1000949.
69. Smith, J., Manoranjan, J., Pan, M., Bohsali, A., Xu, J., Liu, J., etal. (2008) Evidence for pore formation in host cell membranes by ESX-1-secreted ESAT-6 and its role in Mycobacterium marinum escape from the vacuole. Infect Immun 76: 5478-5487.
70. Song, H., and Niederweis, M. (2012) Uptake of sulfate but not phosphate by Mycobacterium tuberculosis is slower than that for Mycobacterium smegmatis. J Bacteriol 194: 956-964.
71. Song, H., Sandie, R., Wang, Y., Andrade-Navarro, M.A., and Niederweis, M. (2008) Identification of outer membrane proteins of Mycobacterium tuberculosis. Tuberculosis 88: 526-544.
72. Speer, A., Rowland, J.L., Haeili, M., Niederweis, M., and Wolschendorf, F. (2013a) Porins increase copper susceptibility of Mycobacterium tuberculosis. J Bacteriol 195: 5133-5140.
73. Speer, A., Rowland, J.L., and Niederweis, M. (2013b) Mycobacterium tuberculosis is resistant to streptolydigin. Tuberculosis (Edinb) 93: 401-404.
74. Stahl, C., Kubetzko, S., Kaps, I., Seeber, S., Engelhardt, H., and Niederweis, M. (2001) MspA provides the main hydrophilic pathway through the cell wall of Mycobacterium smegmatis. Mol Microbiol 40: 451-464. Authors' correction appeared in Mol. Microbiol. 457, 1509.
75. Steinbrecher, U.P., Gomez-Munoz, A., and Duronio, V. (2004) Acid sphingomyelinase in macrophage apoptosis. Curr Opin Lipidol 15: 531-537.
76. Stephan, J., Mailaender, C., Etienne, G., Daffe, M., and Niederweis, M. (2004) Multidrug resistance of a porin deletion mutant of Mycobacterium smegmatis. Antimicrob Agents Chemother 48: 4163-4170.
77. Stephan, J., Bender, J., Wolschendorf, F., Hoffmann, C., Roth, E., Mailänder, C., etal. (2005) The growth rate of Mycobacterium smegmatis depends on sufficient porin-mediated influx of nutrients. Mol Microbiol 58: 714-730.
78. Van der Geize, R., Yam, K., Heuser, T., Wilbrink, M.H., Hara, H., Anderton, M.C., etal. (2007) A gene cluster encoding cholesterol catabolism in a soil actinomycete provides insight into Mycobacterium tuberculosis survival in macrophages. Proc Natl Acad Sci USA 104: 1947-1952.
79. Vargas-Villarreal, J., Mata-Cardenas, B.D., Deslauriers, M., Quinn, F.D., Castro-Garza, J., Martinez-Rodrlguez, H.G., and Said-Fernandez, S. (2003) Identification of acidic, alkaline, and neutral sphingomyelinase activities in Mycobacterium tuberculosis. Med Sci Monit 9: BR225-BR230.
80. Voskuil, M.I., Visconti, K.C., and Schoolnik, G.K. (2004) Mycobacterium tuberculosis gene expression during adaptation to stationary phase and low-oxygen dormancy. Tuberculosis 84: 218-227.
81. Voss, B.J., Gaddy, J.A., McDonald, W.H., and Cover, T.L. (2014) Analysis of surface-exposed outer membrane proteins in Helicobacter pylori. J Bacteriol 196: 2455-2471.
82. Wang, L., Slayden, R.A., Barry, C.E., 3rd, and Liu, J. (2000) Cell wall structure of a mutant of Mycobacterium smegmatis defective in the biosynthesis of mycolic acids. J Biol Chem 275: 7224-7229.
83. Watanabe, S., Zimmermann, M., Goodwin, M.B., Sauer, U., Barry, C.E., 3rd, and Boshoff, H.I. (2011) Fumarate reductase activity maintains an energized membrane in anaerobic Mycobacterium tuberculosis. PLoS Pathog 7: e1002287.
84. van der Wel, N., Hava, D., Houben, D., Fluitsma, D., van Zon, M., Pierson, J., etal. (2007) M.tuberculosis and M.leprae translocate from the phagolysosome to the cytosol in myeloid cells. Cell 129: 1287-1298.
85. Wolf, A.J., Linas, B., Trevejo-Nunez, G.J., Kincaid, E., Tamura, T., Takatsu, K., and Ernst, J.D. (2007) Mycobacterium tuberculosis infects dendritic cells with high frequency and impairs their function in vivo. J Immunol 179: 2509-2519.
86. Wolschendorf, F., Mahfoud, M., and Niederweis, M. (2007) Porins are required for uptake of phosphates by Mycobacterium smegmatis. J Bacteriol 189: 2435-2442.
87. Wong, D., Bach, H., Sun, J., Hmama, Z., and Av-Gay, Y. (2011) Mycobacterium tuberculosis protein tyrosine phosphatase (PtpA) excludes host vacuolar-H+-ATPase to inhibit phagosome acidification. Proc Natl Acad Sci USA 108: 19371-19376.
88. Xu, G., Jia, H., Li, Y., Liu, X., Li, M., and Wang, Y. (2010) Hemolytic phospholipase Rv0183 of Mycobacterium tuberculosis induces inflammatory response and apoptosis in alveolar macrophage RAW264.7 cells. Can J Microbiol 56: 916-924.
89. Zhang, Y.J., Ioerger, T.R., Huttenhower, C., Long, J.E., Sassetti, C.M., Sacchettini, J.C., and Rubin, E.J. (2012) Global assessment of genomic regions required for growth in Mycobacterium tuberculosis. PLoS Pathog 8: e1002946.