Diversion of phagosome trafficking by pathogenic Rhodococcus equi depends on mycolic acid chain length

Cellular Microbiology

Volumn 15, Issue 3, 2013, Pages 458-473

  Sydor, Tobias ^a   von Bargen, Kristine ^a   Hsu, Fong Fu ^b   Huth, Gitta ^a   Holst, Otto ^c   Wohlmann, Jens ^a   Becken, Ulrike ^a   Dykstra, Tobias ^a   Söhl, Kristina ^a   Lindner, Buko ^c   Prescott, John F ^d   Schaible, Ulrich E ^c   Utermöhlen, Olaf ^e   Haas, Albert ^a  

^a UNIVERSITY OF BONN   (Germany)

^b WASHINGTON UNIVERSITY   (United States)

^c RESEARCH CENTER BORSTEL   (Germany)

^d UNIVERSITY OF GUELPH   (Canada)

^e UNIVERSITY OF COLOGNE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

3 HYDROXYACYL COENZYME A DEHYDROGENASE; CORD FACTOR; MYCOLIC ACID;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL COUNT; BACTERIAL GROWTH; BACTERIAL LOAD; BACTERIUM MUTANT; CARBON SOURCE; CELL MIGRATION; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; ENTAMOEBA COLI; MACROPHAGE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PHAGOLYSOSOME; PRIORITY JOURNAL; RHODOCOCCUS EQUI; TRANSPOSON;

3-OXOACYL-(ACYL-CARRIER-PROTEIN) SYNTHASE; ACTINOMYCETALES INFECTIONS; ANIMALS; CELL LINE; DISEASE MODELS, ANIMAL; DNA TRANSPOSABLE ELEMENTS; DNA, BACTERIAL; GENE KNOCKOUT TECHNIQUES; HOST-PATHOGEN INTERACTIONS; MACROPHAGES; MICE; MOLECULAR SEQUENCE DATA; MUTAGENESIS, INSERTIONAL; MYCOLIC ACIDS; PHAGOSOMES; RHODOCOCCUS EQUI; SEQUENCE ANALYSIS, DNA; VIRULENCE;

CORYNEBACTERINEAE; MYCOBACTERIUM; RHODOCOCCUS EQUI;

EID: 84873743701     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/cmi.12050     Document Type: Article

References (76)

1. Almog, R., and Mannella, C.A. (1996) Molecular packing of cord factor and its interaction with phosphatidylinositol in mixed monolayers. Biophys J 71: 3311-3319.
2. Ashour, J., and Hondalus, M.K. (2003) Phenotypic mutants of the intracellular actinomycete Rhodococcus equi created by in vivo Himar1 transposon mutagenesis. J Bacteriol 185: 2644-2652.
3. Astarie-Dequeker, C., Guyader, L.L., Malaga, W., Seaphanh, F.K., Chalut, C., Lopez, A., etal. (2009) Phthiocerol dimycocerosates of M.tuberculosis participate in macrophage invasion by inducing changes in the organization of plasma membrane lipids. PLoS Pathog 5: e1000289.
4. Axelrod, S., Oschkinat, H., Enders, J., Schlegel, B., Brinkmann, V., Kaufmann, S.H.E., etal. (2008) Delay of phagosome maturation by a mycobacterial lipid is reversed by nitric oxide. Cell Microbiol 10: 1530-1545.
5. von Bargen, K., and Haas, A. (2009) Molecular and infection biology of the horse pathogen Rhodococcus equi. FEMS Microbiol Rev 33: 870-891.
6. von Bargen, K., Polidori, M., Becken, U., Huth, G., Prescott, J.F., and Haas, A. (2009) Rhodococcus equi virulence-associated protein A is required for diversion of phagosome biogenesis but not for cytotoxicity. Infect Immun 77: 5676-5681.
7. von Bargen, K., Wohlmann, J., Taylor, G.A., Utermöhlen, O., and Haas, A. (2011) Nitric oxide-mediated intracellular growth restriction of pathogenic Rhodococcus equi can be prevented by iron. Infect Immun 79: 2098-2111.
8. Barkan, D., Liu, Z., Sacchettini, J.C., and Glickman, M.S. (2009) Mycolic acid cyclopropanation is essential for viability, drug resistance, and cell wall integrity of Mycobacterium tuberculosis. Chem Biol 16: 499-509.
9. Barry, C.E., Lee, R.E., Mdluli, K., Sampson, A.E., Schroeder, B.G., Slayden, R.A., etal. (1998) Mycolic acids: structure, biosynthesis and physiological functions. Prog Lipid Res 37: 143-179.
10. Becken, U., Jeschke, A., Veltman, K., and Haas, A. (2010) Cell-free fusion of bacteria-containing phagosomes with endocytic compartments. Proc Natl Acad Sci USA 107: 20726-20731.
11. Bhatt, A., Kremer, L., Dai, A.Z., Sacchettini, J.C., and Jacobs, W.R. (2005) Conditional depletion of KasA, a key enzyme of mycolic acid biosynthesis, leads to mycobacterial cell lysis. J Bacteriol 187: 7596-7606.
12. Bhatt, A., Fujiwara, N., Bhatt, K., Gurcha, S.S., Kremer, L., Chen, B., etal. (2007a) Deletion of kasB in Mycobacterium tuberculosis causes loss of acid-fastness and subclinical latent tuberculosis in immunocompetent mice. Proc Natl Acad Sci USA 104: 5157-5162.
13. Bhatt, A., Molle, V., Besra, G.S., Jacobs, W.R., and Kremer, L. (2007b) The Mycobacterium tuberculosis FAS-II condensing enzymes: their role in mycolic acid biosynthesis, acid-fastness, pathogenesis and in future drug development. Mol Microbiol 64: 1442-1454.
14. Brennan, P.J., and Nikaido, H. (1995) The envelope of mycobacteria. Annu Rev Biochem 64: 29-63.
15. Brodin, P., Poquet, Y., Levillain, F., Peguillet, I., Larrouy-Maumus, G., Gilleron, M., etal. (2010) High content phenotypic cell-based visual screen identifies Mycobacterium tuberculosis acyltrehalose-containing glycolipids involved in phagosome remodeling. PLoS Pathog 6: e1001100.
16. Brown, A.K., Sridharan, S., Kremer, L., Lindenberg, S., Dover, L.G., Sacchettini, J.C., etal. (2005) Probing the mechanism of the Mycobacterium tuberculosis beta-ketoacyl-acyl carrier protein synthase III mtFabH: factors influencing catalysis and substrate specificity. J Biol Chem 280: 32539-32547.
17. Crowe, L.M., Spargo, B.J., Ioneda, T., Beaman, B.L., and Crowe, J.H. (1994) Interaction of cord factor (alpha, alpha′-trehalose-6, 6′-dimycolate) with phospholipids. Biochim Biophys Acta 1194: 53-60.
18. Dermine, J.F., Goyette, G., Houde, M., Turco, S.J., and Desjardins, M. (2005) Leishmania donovani lipophosphoglycan disrupts phagosome microdomains in J774 macrophages. Cell Microbiol 7: 1263-1270.
19. Dykstra, T., Utermoehlen, O., and Haas, A. (2011) Defined particle ligands trigger specific defense mechanisms of macrophages. Innate Immun 17: 388-402.
20. Fernandez-Mora, E., Polidori, M., Lührmann, A., Schaible, U.E., and Haas, A. (2005) Maturation of Rhodococcus equi-containing vacuoles is arrested after completion of the early endosome stage. Traffic 6: 635-653.
21. Fratti, R.A., Chua, J., Vergne, I., and Deretic, V. (2003) Mycobacterium tuberculosis glycosylated phosphatidylinositol causes phagosome maturation arrest. Proc Natl Acad Sci USA 100: 5437-5442.
22. Gao, L.Y., Laval, F., Lawson, E.H., Groger, R.K., Woodruff, A., Morisaki, J.H., etal. (2003) Requirement for kasB in Mycobacterium mycolic acid biosynthesis, cell wall impermeability and intracellular survival: implications for therapy. Mol Microbiol 49: 1547-1563.
23. Garton, N.J., Gilleron, M., Brando, T., Dan, H.H., Giguére, S., Puzo, G., etal. (2002) A novel lipoarabinomannan from the equine pathogen Rhodococcus equi. Structure and effect on macrophage cytokine production. J Biol Chem 277: 31722-31733.
24. Ge, M., and Freed, J.H. (2011) Two conserved residues are important for inducing highly ordered membrane domains by the transmembrane domain of influenza hemagglutinin. Biophys J 100: 90-97.
25. Geisel, R.E., Sakamoto, K., Russell, D.G., and Rhoades, E.R. (2005) In vivo activity of released cell wall lipids of Mycobacterium bovis bacillus Calmette-Guérin is due principally to trehalose mycolates. J Immunol 174: 5007-5015.
26. Gotoh, K., Mitsuyama, M., Imaizumi, S., Kawamura, I., and Yano, I. (1991) Mycolic acid-containing glycolipid as a possible virulence factor of Rhodococcus equi for mice. Microbiol Immunol 35: 175-185.
27. Haas, A. (2007) The phagosome: compartment with a license to kill. Traffic 8: 311-330.
28. Harland, C.W., Botyanszki, Z., Rabuka, D., Bertozzi, C.R., and Parthasarathy, R. (2009) Synthetic trehalose glycolipids confer desiccation resistance to supported lipid monolayers. Langmuir 25: 5193-5198.
29. Harris, S.P., Fujiwara, N., Mealey, R.H., Alperin, D.C., Naka, T., Goda, R., etal. (2010) Identification of Rhodococcus equi lipids recognized by host cytotoxic T lymphocytes. Microbiology 156: 1836-1847.
30. Hayakawa, E., Tokumasu, F., Nardone, G.A., Jin, A.J., Hackley, V.A., and Dvorak, J.A. (2007) A Mycobacterium tuberculosis-derived lipid inhibits membrane fusion by modulating lipid membrane domains. Biophys J 93: 4018-4030.
31. Hayashi, T., Yamamoto, O., Sasaki, H., Kawaguchi, A., and Okazaki, H. (1983) Mechanism of action of the antibiotic thiolactyomcin inhibition of fatty acid synthesis of Escherichia coli. Biochem Biophys Res Commun 115: 1108-1113.
32. Herrmann, J.L., O'Gaora, P., Gallagher, A., Thole, J.E., and Young, D.B. (1996) Bacterial glycoproteins: a link between glycosylation and proteolytic cleavage of a 19kDa antigen from Mycobacterium tuberculosis. EMBO J 15: 3547-3554.
33. Hietala, S.K., and Ardans, A.A. (1987) Interaction of Rhodococcus equi with phagocytic cells from R.equi-exposed and non-exposed foals. Vet Microbiol 14: 307-320.
34. 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.
35. Hondalus, M.K., and Mosser, D.M. (1994) Survival and replication of Rhodococcus equi in macrophages. Infect Immun 62: 4167-4175.
36. Hsu, F.F., Wohlmann, J., Turk, J., and Haas, A. (2011a) Structural definition of trehalose 6-monomycolates and trehalose 6, 6′-dimycolates from the pathogen Rhodococcus equi by multiple-stage linear ion-trap mass spectrometry with electrospray ionization. J Am Soc Mass Spectrom 22: 2160-2170.
37. Hsu, F.F., Soehl, K., Turk, J., and Haas, A. (2011b) Characterization of mycolic acids from the pathogen Rhodococcus equi by tandem mass spectrometry with electrospray ionization. Anal Biochem 409: 112-122.
38. Hunter, R.L., Olsen, M.R., Jagannath, C., and Actor, J.K. (2006) Multiple roles of cord factor in the pathogenesis of primary, secondary, and cavitary tuberculosis, including a revised description of the pathology of secondary disease. Ann Clin Lab Sci 36: 371-386.
39. Indrigo, J., Hunter, R.L., and Actor, J.K. (2003) Cord factor trehalose 6, 6′-dimycolate (TDM) mediates trafficking events during mycobacterial infection of murine macrophages. Microbiology 149: 2049-2059.
40. Ishikawa, E., Ishikawa, T., Morita, Y.S., Toyonaga, K., Yamada, H., Takeuchi, O., etal. (2009) Direct recognition of the mycobacterial glycolipid, trehalose dimycolate, by C-type lectin Mincle. J Exp Med 206: 2879-2888.
41. Ishikawa, J., Yamashita, A., Mikami, Y., Hoshino, Y., Kurita, H., Hotta, K., etal. (2004) The complete genomic sequence of Nocardia farcinica IFM 10152. Proc Natl Acad Sci USA 101: 14925-14930.
42. Jain, S., Bloom, B.R., and Hondalus, M.K. (2003) Deletion of vapA encoding virulence associated protein A attenuates the intracellular actinomycete Rhodococcus equi. Mol Microbiol 50: 115-128.
43. Kremer, L., Douglas, J.D., Baulard, A.R., Morehouse, C., Guy, M.R., Alland, D., etal. (2000) Thiolactomycin and related analogues as novel anti-mycobacterial agents targeting KasA and KasB condensing enzymes in Mycobacterium tuberculosis. J Biol Chem 275: 16857-16864.
44. Letek, M., González, P., Macarthur, I., Rodríguez, H., Freeman, T.C., Valero-Rello, A., etal. (2010) The genome of a pathogenic rhodococcus: cooptive virulence underpinned by key gene acquisitions. PLoS Genet 6: e1001145.
45. Liu, B., Wang, Y., Fillgrove, K.L., and Anderson, V.E. (2002) Triclosan inhibits enoyl-reductase of type I fatty acid synthase in vitro and is cytotoxic to MCF-7 and SKBr-3 breast cancer cells. Cancer Chemother Pharmacol 49: 187-193.
46. Liu, J., and Nikaido, H. (1999) A mutant of Mycobacterium smegmatis defective in the biosynthesis of mycolic acids accumulates meromycolates. Proc Natl Acad Sci USA 96: 4011-4016.
47. Liu, J., Rosenberg, E.Y., and Nikaido, H. (1995) Fluidity of the lipid domain of cell wall from Mycobacterium chelonae. Proc Natl Acad Sci USA 92: 11254-11258.
48. Lührmann, A., Mauder, N., Sydor, T., Fernandez-Mora, E., Schulze-Luehrmann, J., Takai, S., etal. (2004) Necrotic death of Rhodococcus equi-infected macrophages is regulated by virulence-associated plasmids. Infect Immun 72: 853-862.
49. McLeod, M.P., Warren, R.L., Hsiao, W.W.L., Araki, N., Myhre, M., Fernandes, C., etal. (2006) The complete genome of Rhodococcus sp. RHA1 provides insights into a catabolic powerhouse. Proc Natl Acad Sci USA 103: 15582-15587.
50. Matsunaga, I., and Moody, D.B. (2009) Mincle is a long sought receptor for mycobacterial cord factor. J Exp Med 206: 2865-2868.
51. Mitani, Y., Suzuki, K., Kondo, K., Okumura, K., and Tamura, T. (2006) Gene expression analysis using a modified HiCEP method applicable to prokaryotes: a study of the response of Rhodococcus to isoniazid and ethambutol. J Biotechnol 123: 259-272.
52. Neyrolles, O., and Guilhot, C. (2011) Recent advances in deciphering the contribution of Mycobacterium tuberculosis lipids to pathogenesis. Tuberculosis (Edinb) 91: 187-195.
53. Niescher, S., Wray, V., Lang, S., Kaschabek, S.R., and Schlömann, M. (2006) Identification and structural characterisation of novel trehalose dinocardiomycolates from n-alkane-grown Rhodococcus opacus 1CP. Appl Microbiol Biotechnol 70: 605-611.
54. Ojha, A., Anand, M., Bhatt, A., Kremer, L., Jacobs, W.R., and Hatfull, G.F. (2005) GroEL1: a dedicated chaperone involved in mycolic acid biosynthesis during biofilm formation in mycobacteria. Cell 123: 861-873.
55. Pei, Y., Dupont, C., Sydor, T., Haas, A., and Prescott, J.F. (2006) Cholesterol oxidase (ChoE) is not important in the virulence of Rhodococcus equi. Vet Microbiol 118: 240-246.
56. Pethe, K., Swenson, D.L., Alonso, S., Anderson, J., Wang, C., and Russell, D.G. (2004) Isolation of Mycobacterium tuberculosis mutants defective in the arrest of phagosome maturation. Proc Natl Acad Sci USA 101: 13642-13647.
57. Portevin, D., Sousa-D'Auria, C.D., Houssin, C., Grimaldi, C., Chami, M., Daffé, M., etal. (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.
58. Rhoades, E., Hsu, F.F., Torrelles, J.B., Turk, J., Chatterjee, D., and Russell, D.G. (2003) Identification and macrophage-activating activity of glycolipids released from intracellular Mycobacterium bovis BCG. Mol Microbiol 48: 875-888.
59. Rhoades, E.R., and Ullrich, H.J. (2000) How to establish a lasting relationship with your host: lessons learned from Mycobacterium spp. Immunol Cell Biol 78: 301-310.
60. Robinson, N., Wolke, M., Ernestus, K., and Plum, G. (2007) A mycobacterial gene involved in synthesis of an outer cell envelope lipid is a key factor in prevention of phagosome maturation. Infect Immun 75: 581-591.
61. Sacco, E., Covarrubias, A.S., O'Hare, H.M., Carroll, P., Eynard, N., Jones, T.A., etal. (2007) The missing piece of the type II fatty acid synthase system from Mycobacterium tuberculosis. Proc Natl Acad Sci USA 104: 14628-14633.
62. Schoenen, H., Bodendorfer, B., Hitchens, K., Manzanero, S., Werninghaus, K., Nimmerjahn, F., etal. (2010) Cutting edge: Mincle is essential for recognition and adjuvanticity of the mycobacterial cord factor and its synthetic analog trehalose-dibehenate. J Immunol 184: 2756-2760.
63. Schramm, M., Herz, J., Haas, A., Krönke, M., and Utermöhlen, O. (2008) Acid sphingomyelinase is required for efficient phago-lysosomal fusion. Cell Microbiol 10: 1839-1853.
64. Sekizaki, T., Tanoue, T., Osaki, M., Shimoji, Y., Tsubaki, S., and Takai, S. (1998) Improved electroporation of Rhodococcus equi. J Vet Med Sci 60: 277-279.
65. Slayden, R.A., and Barry, C.E. (2002) The role of KasA and KasB in the biosynthesis of meromycolic acids and isoniazid resistance in Mycobacterium tuberculosis. Tuberculosis (Edinb) 82: 149-160.
66. Slayden, R.A., Lee, R.E., Armour, J.W., Cooper, A.M., Orme, I.M., Brennan, P.J., etal. (1996) Antimycobacterial action of thiolactomycin: an inhibitor of fatty acid and mycolic acid synthesis. Antimicrob Agents Chemother 40: 2813-2819.
67. Spargo, B.J., Crowe, L.M., Ioneda, T., Beaman, B.L., and Crowe, J.H. (1991) Cord factor (alpha, alpha-trehalose 6, 6′-dimycolate) inhibits fusion between phospholipid vesicles. Proc Natl Acad Sci USA 88: 737-740.
68. Sutcliffe, I.C. (1998) Cell envelope composition and organisation in the genus Rhodococcus. Antonie Van Leeuwenhoek 74: 49-58.
69. Sydor, T., von Bargen, K., Becken, U., Spuerck, S., Nicholson, V.M., Prescott, J.F., etal. (2008) A mycolyl transferase mutant of Rhodococcus equi lacking capsule integrity is fully virulent. Vet Microbiol 128: 327-341.
70. Takai, S., Koike, K., Ohbushi, S., Izumi, C., and Tsubaki, S. (1991) Identification of 15- to 17-kilodalton antigens associated with virulent Rhodococcus equi. J Clin Microbiol 29: 439-443.
71. Takai, S., Iie, M., Kobayashi, C., Morishita, T., Nishio, T., Ishida, T., etal. (1993) Monoclonal antibody specific to virulence-associated 15- to 17-kilodalton antigens of Rhodococcus equi. J Clin Microbiol 31: 2780-2782.
72. Takai, S., Hines, S.A., Sekizaki, T., Nicholson, V.M., Alperin, D.A., Osaki, M., etal. (2000) DNA sequence and comparison of virulence plasmids from Rhodococcus equi ATCC 33701 and 103. Infect Immun 68: 6840-6847.
73. Takayama, K., Wang, C., and Besra, G.S. (2005) Pathway to synthesis and processing of mycolic acids in Mycobacterium tuberculosis. Clin Microbiol Rev 18: 81-101.
74. Vergne, I., Fratti, R.A., Hill, P.J., Chua, J., Belisle, J., and Deretic, V. (2004) Mycobacterium tuberculosis phagosome maturation arrest: mycobacterial phosphatidylinositol analog phosphatidylinositol mannoside stimulates early endosomal fusion. Mol Biol Cell 15: 751-760.
75. Vishniac, W., and Santer, M. (1957) The thiobacilli. Bacteriol Rev 21: 195-213.
76. Zink, M.C., Yager, J.A., Prescott, J.F., and Fernando, M.A. (1987) Electron microscopic investigation of intracellular events after ingestion of Rhodococcus equi by foal alveolar macrophages. Vet Microbiol 14: 295-305.