Evidence for the cytotoxic effects of Mycobacterium tuberculosis phospholipase C towards macrophages

Biochimica et Biophysica Acta - Molecular and Cell Biology of Lipids

Volumn 1801, Issue 12, 2010, Pages 1305-1313

  Bakala N'Goma, J C ^a   Schue M ^a   Carriere F ^a   Geerlof, A ^b,c   Canaan, S ^a  

^a Centre National de la Recherche Scientifique   (France)

^b DESY   (Germany)

^c INSTITUTE OF EPIDEMIOLOGY   (Germany)

Author keywords

Cytotoxicity; M. smegmatis; Macrophage; Mycobacterium tuberculosis; Phospholipase C

Indexed keywords

CALCIUM; MEMBRANE PHOSPHOLIPID; PHOSPHOLIPASE C;

ANIMAL CELL; ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; CYTOTOXICITY; ENZYME ACTIVITY; ENZYME PURIFICATION; HEMOLYSIS; HYDROLYSIS; IN VITRO STUDY; MACROPHAGE; MOLECULAR CLONING; MOUSE; MYCOBACTERIUM SMEGMATIS; NONHUMAN; PH MEASUREMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; TEMPERATURE SENSITIVITY; THIN LAYER CHROMATOGRAPHY;

MUS; MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS;

EID: 77958021388     PISSN: 13881981     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbalip.2010.08.007     Document Type: Article

References (45)

1. Minnikin D.E., Kremer L., Dover L.G., Besra G.S. The methyl-branched fortifications of Mycobacterium tuberculosis. Chem. Biol. 2002, 9:545-553.
2. Daffe M., Draper P. The envelope layers of mycobacteria with reference to their pathogenicity. Adv. Microb. Physiol. 1998, 39:131-203.
3. Wayne L.G., Sohaskey C.D. Nonreplicating persistence of Mycobacterium tuberculosis. Annu. Rev. Microbiol. 2001, 55:139-163.
4. Côtes K., Bakala N'goma C., Dhouib J.R., Douchet I., Maurin D., Carriere F., Canaan S. Lipolytic enzymes in Mycobacterium tuberculosis. Appl. Microbiol. Biotechnol. 2008, 78:741-749.
5. Schmiel D.H., Miller V.L. Bacterial phospholipases and pathogenesis. Microbes Infect. 1999, 1:1103-1112.
6. Songer J.G. Bacterial phospholipases and their role in virulence. Trends Microbiol. 1997, 5:156-161.
7. Titball R.W. Bacterial phospholipases. Symp. Ser. Soc. Appl. Microbiol. 1998, 27:127S-137S.
8. Flores-Diaz M., Alape-Giron A. Role of Clostridium perfringens phospholipase C in the pathogenesis of gas gangrene. Toxicon 2003, 42:979-986.
9. Poussin M.A., Leitges M., Goldfine H. The ability of Listeria monocytogenes PI-PLC to facilitate escape from the macrophage phagosome is dependent on host PKCbeta. Microb. Pathog. 2009, 46:1-5.
10. Bomberger J.M., Maceachran D.P., Coutermarsh B.A., Ye S., O'Toole G.A., Stanton B.A. Long-distance delivery of bacterial virulence factors by Pseudomonas aeruginosa outer membrane vesicles. PLoS Pathog. 2009, 5:e1000382.
11. Côtes K., Dhouib R., Douchet I., Chahinian H., de Caro A., Carriere F., Canaan S. Characterization of an exported monoglyceride lipase from Mycobacterium tuberculosis possibly involved in the metabolism of host cell membrane lipids. Biochem. J. 2007, 408:417-427.
12. Schué M., Maurin D., Dhouib R., Bakala N'Goma J.-C., Delorme V., Lambeau G., Carrière F., Canaan S. Two cutinase-like proteins secreted by Mycobacterium tuberculosis show very different lipolytic activities reflecting their physiological function. Faseb J. 2010, 24(6):1893-1903.
13. Cole S.T., Brosch R., Parkhill J., Garnier T., Churcher C., Harris D., Gordon S.V., Eiglmeier K., Gas S., Barry C.E., Tekaia F., Badcock K., Basham D., Brown D., Chillingworth T., Connor R., Davies R., Devlin K., Feltwell T., Gentles S., Hamlin N., Holroyd S., Hornsby T., Jagels K., Barrell B.G., et al. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 1998, 393:537-544.
14. Camus J., Pryor M., Medigue C., Cole S. Re-annotation of the genome sequence of Mycobacterium tuberculosis H37Rv. Microbiology 2002, 148:2967-2973.
15. Raynaud C., Guilhot C., Rauzier J., Bordat Y., P.V., Manganelli R., Smith I., Gicquel B., Jackson M. Phospholipases C are involved in the virulence of Mycobacterium tuberculosis. Mol. Microbiol. 2002, 45:203-217.
16. Matsui T., Carneiro C.R., Leao S.C. Evidence for the expression of native Mycobacterium tuberculosis phospholipase C: recognition by immune sera and detection of promoter activity. Braz. J. Med. Biol. Res. 2000, 33:1275-1282.
17. Leao S.C., Rocha C.L., Murillo L.A., Parra C.A., Patarroyo M.E. A species-specific nucleotide sequence of Mycobacterium tuberculosis encodes a protein that exhibits hemolytic activity when expressed in Escherichia coli. Infect. Immun. 1995, 63:4301-4306.
18. Ostroff R.M., Vasil A.I., Vasil M.L. Molecular comparison of a nonhemolytic and a hemolytic phospholipase C from Pseudomonas aeruginosa. J. Bacteriol. 1990, 172:5915-5923.
19. Gomez A., Mve-Obiang A., Vray B., Rudnicka W., Shamputa I.C., Portaels F., Meyers W.M., Fonteyne P.A., Realini L. Detection of phospholipase C in nontuberculous mycobacteria and its possible role in hemolytic activity. J. Clin. Microbiol. 2001, 39:1396-1401.
20. Johansen K., Gill R., Vasil M. Biochemical and molecular analysis of phospholipase C and phospholipase D activity in mycobacteria. Infect. Immun. 1996, 64:3259-3266.
21. Bendtsen J.D., Nielsen H., Widdick D., Palmer T., Brunak S. Prediction of twin-arginine signal peptides. BMC Bioinform. 2005, 6:167.
22. McDonough J.A., McCann J.R., Tekippe E.M., Silverman J.S., Rigel N.W., Braunstein M. Identification of functional Tat signal sequences in Mycobacterium tuberculosis proteins. J. Bacteriol. 2008, 190:6428-6438.
23. McDonough J.A., Hacker K.E., Flores A.R., Pavelka M.S., Braunstein M. The twin-arginine translocation pathway of Mycobacterium smegmatis is functional and required for the export of mycobacterial beta-lactamases. J. Bacteriol. 2005, 187:7667-7679.
24. Ferrandez Y., Condemine G. Novel mechanism of outer membrane targeting of proteins in Gram-negative bacteria. Mol. Microbiol. 2008, 69:1349-1357.
25. Palmer T., Sargent F., Berks B.C. Export of complex cofactor-containing proteins by the bacterial Tat pathway. Trends Microbiol. 2005, 13:175-180.
26. Oresnik I.J., Ladner C.L., Turner R.J. Identification of a twin-arginine leader-binding protein. Mol. Microbiol. 2001, 40:323-331.
27. Demchick P., Koch A.L. The permeability of the wall fabric of Escherichia coli and Bacillus subtilis. J. Bacteriol. 1996, 178:768-773.
28. Stonehouse M.J., Cota-Gomez A., Parker S.K., Martin W.E., Hankin J.A., Murphy R.C., Chen W., Lim K.B., Hackett M., Vasil A.I., Vasil M.L. A novel class of microbial phosphocholine-specific phospholipases C. Mol. Microbiol. 2002, 46:661-676.
29. Titball R.W. Bacterial phospholipase C. Microb. Rev. 1993, 57:347-366.
30. Russell D.G., Vanderven B.C., Glennie S., Mwandumba H., Heyderman R.S. The macrophage marches on its phagosome: dynamic assays of phagosome function. Nat. Rev. Immunol. 2009, 9:594-600.
31. Ninomiya M., Matsushita O., Minami J., Sakamoto H., Nakano M., Okabe A. Role of alpha-toxin in Clostridium perfringens infection determined by using recombinants of C. perfringens and Bacillus subtilis. Infect. Immun. 1994, 62:5032-5039.
32. Stevens D.L., Bryant A.E. The role of clostridial toxins in the pathogenesis of gas gangrene. Clin. Infect. Dis. 2002, 35:S93-S100.
33. Goldfine H., Bannam T., Johnston N.C., Zuckert W.R. Bacterial phospholipases and intracellular growth: the two distinct phospholipases C of Listeria monocytogenes. Symp. Ser. Soc. Appl. Microbiol. 1998, 27:7S-14S.
34. Wheeler P.R., Bulmer K., Ratledge C. Enzymes for biosynthesis de novo and elongation of fatty acids in mycobacteria grown in host cells: is Mycobacterium leprae competent in fatty acid biosynthesis?. J. Gen. Microbiol. 1990, 136:211-217.
35. Schiess K., Kaszkin M., Jordan P., Seidler L., Kinzel V. Mobilization of diacylglycerol in intact HeLa cells by exogenous phospholipase C from Cl. perfringens is accompanied by release of fatty acids including arachidonic acid. Biochim. Biophys. Acta 1992, 1137:82-94.
36. Gustafson C., Tagesson C. Phospholipase C from Clostridium perfringens stimulates phospholipase A2-mediated arachidonic acid release in cultured intestinal epithelial cells (INT 407). Scand. J. Gastroenterol. 1990, 25:363-371.
37. Philipp W.J., Poulet S., Eiglmeier K., Pascopella L., Balasubramanian V., Heym B., Bergh S., Bloom B.R., Jacobs W.R., Cole S.T. Balasubramanian, B. Heym, S. Bergh, B.R. Bloom, W.R. Jacobs, Jr., S.T. Cole, An integrated map of the genome of the tubercle bacillus, Mycobacterium tuberculosis H37Rv, and comparison with Mycobacterium leprae. Proc. Natl. Acad. Sci. USA 1996, 93:3132-3137.
38. Daugelat S., Kowall J., Mattow J., Bumann D., Winter R., Hurwitz R., Kaufmann S.H. The RD1 proteins of Mycobacterium tuberculosis: expression in Mycobacterium smegmatis and biochemical characterization. Microbes Infect. 2003, 5:1082-1095.
39. Jacobs W.R., Kalpana G.V., Cirillo J.D., Pascopella L., Snapper S.B., Udani R.A., Jones W., Barletta R.G., Bloom B.R. Genetic systems for mycobacteria. Methods Enzymol. 1991, 204:537-555.
40. McNally E., Sohn R., Frankel S., Leinwand L. Expression of myosin and actin in Escherichia coli. Methods Enzymol. 1991, 196:368-389.
41. Frankel S., Sohn R., Leinwand L. The use of sarkosyl in generating soluble protein after bacterial expression. Proc. Natl. Acad. Sci. USA 1991, 88:1192-1196.
42. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227:680-685.
43. Fliegera A., Gong S., Faigle M., Neumeister B. Critical evaluation of p-nitrophenylphosphorylcholine (p-NPPC) as artificial substrate for the detection of phospholipase C. Enzyme Microb. Technol. 2000, 26:451-458.
44. Folch J., Lees M., Sloane Stanley G.H. A simple method for the isolation and purification of total lipides from animal tissues. J. Biol. Chem. 1957, 226:497-509.
45. Garcia J.J., Curi R., Martins E., Carpinelli A. Macrophages transfer [14C]-labelled fatty acids to pancreatic islets in culture. Cell Biochem. Funct. 2001, 19:11-17.