Species of environmental mycobacteria differ in their abilities to grow in human, mouse, and carp macrophages and with regard to the presence of mycobacterial virulence genes, as observed by DNA microarray hybridization

Applied and Environmental Microbiology

Volumn 74, Issue 1, 2008, Pages 275-285

  Harriff, Melanie J ^a   Wu, Martin ^a   Kent, Michael L ^a   Bermudez, Luiz E ^a  

^a OREGON STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIODIVERSITY; DNA; GENE EXPRESSION; MACROPHAGES; MICROARRAYS; PATHOGENS; VIRUSES;

ENVIRONMENTAL MYCOBACTERIA (EM); METABOLIC PATHWAYS; MICROARRAY HYBRIDIZATION; MOLECULAR MECHANISMS; VIRULENCE GENES;

BACTERIA;

BACTERIAL DNA; GENOMIC DNA;

BACTERIUM; CYPRINID; DNA; FATTY ACID; GENOME; GROWTH RATE; HOMINID; HOST SPECIFICITY; PATHOGENICITY; RODENT; VIRULENCE;

ANIMAL CELL; ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL VIRULENCE; BACTERIUM ISOLATE; CARP; CELL TYPE; DNA HYBRIDIZATION; DNA MICROARRAY; ENVIRONMENTAL MYCOBACTERIUM; HUMAN; HUMAN CELL; MACROPHAGE; MOUSE; MYCOBACTERIUM; NONHUMAN; SPECIES DIFFERENCE; ZOONOSIS;

ANIMALS; CARPS; CELL LINE; DNA, BACTERIAL; ENVIRONMENTAL MICROBIOLOGY; GENOME, BACTERIAL; HUMANS; MACROPHAGES; MICE; MICROARRAY ANALYSIS; MYCOBACTERIUM; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; VIRULENCE FACTORS;

ANIMALIA; BACTERIA (MICROORGANISMS); CORYNEBACTERINEAE; CYPRINIDAE; MUS; MYCOBACTERIUM; MYCOBACTERIUM AVIUM; MYCOBACTERIUM CHELONAE; MYCOBACTERIUM PEREGRINUM;

EID: 37849050224     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.01480-07     Document Type: Article

References (55)

1. Arakawa, C. K., and J. L. Fryer. 1984. Isolation and characterization of a new subspecies of Mycobacterium chelonei infectious for salmonid fish. Helgolander Meeresun 37:329-342.
2. Astrofsky, K. M., M. D. Schrenzel, R. A. Bullis, R. M. Smolowitz, and J. G. Fox. 2000. Diagnosis and management of atypical Mycobacterium spp. infections in established laboratory zebrafish (Brachydanio rerio) facilities. Comp. Med. 50:666-672.
3. Banks, J. 1994. Environmental mycobacteria, p. 265-276. In P. D. O. Davies (ed.), Clinical tuberculosis. Chapman and Hall, London, United Kingdom.
4. Bannantine, J. P., Q. Zhang, L. L. Li, and V. Kapur. 2003. Genomic homogeneity between Mycobacterium avium subsp. avium and Mycobacterium avium subsp. paratuberculosis belies their divergent growth rates. BMC Microbiol. 3:10.
5. Behr, M. A., M. A. Wilson, W. P. Gill, H. Salamon, G. K. Schoolnik, S. Rane, and P. M. Small. 1999. Comparative genomics of BCG vaccines by whole-genome DNA microarray. Science 284:1520-1523.
6. Bermudez, L. E., and M. Petrofsky. 1997. Regulation of the expression of Mycobacterium avium complex proteins differs according to the environment within host cells. Immunol. Cell Biol. 75:35-40.
7. Braunstein, M., T. I. Griffin, J. I. Kriakov, S. T. Friedman, N. D. Grindley, and W. R. Jacobs, Jr. 2000. Identification of genes encoding exported Mycobacterium tuberculosis proteins using a Tn552′ phoA in vitro transposition system. J. Bacteriol. 182:2732-2740.
8. Brocklebank, J., S. Raverty, and J. Robinson. 2003. Mycobacteriosis in Atlantic salmon farmed in British Columbia. Can. Vet. J. 44:486-489.
9. Brown-Elliott, B. A., and R. J. Wallace, Jr. 2002. Clinical and taxonomic status of pathogenic nonpigmented or late-pigmenting rapidly growing mycobacteria. Clin. Microbiol. Rev. 15:716-746.
10. Bruno, D. W., J. Griffiths, C. G. Mitchell, B. P. Wood, Z. J. Fletcher, F. A. Drobniewski, and T. S. Hastings. 1998. Pathology attributed to Mycobacterium chelonae infection among farmed and laboratory-infected Atlantic salmon Salmo salar. Dis. Aquat. Organ. 33:101-109.
11. Chang, C. T., L. Y. Wang, C. Y. Liao, and S. P. Huang. 2002. Identification of nontuberculous mycobacteria existing in tap water by PCR-restriction fragment length polymorphism. Appl. Environ. Microbiol. 68:3159-3161.
12. Chinabut, S. 1999. Mycobacteriosis and nocardiosis, p. 319-340. In W. B. Woo and P. T. K. (ed.), Fish diseases and disorders: viral bacterial and fungal infections, vol. 3. CAB International, New York, NY.
13. Danelishvili, L., M. J. Poort, and L. E. Bermudez. 2004. Identification of Mycobacterium avium genes up-regulated in cultured macrophages and in mice. FEMS Microbiol. Lett. 239:41-49.
14. Danelishvili, L., M. Wu, B. Stang, M. Harriff, S. Cirillo, J. Cirillo, R. Bildfell, B. Arbogast, and L. E. Bermudez. 2007. Identification of Mycobacterium avium pathogenicity island important for macrophage and amoeba infection. Proc. Natl. Acad. Sci. USA 104:11038-11043.
15. Decostere, A., K. Hermans, and F. Haesebrouck. 2004. Piscine mycobacteriosis: a literature review covering the agent and the disease it causes in fish and humans. Vet. Microbiol. 99:159-166.
16. Dubnau, E., P. Fontan, R. Manganelli, S. Soares-Appel, and I. Smith. 2002. Mycobacterium tuberculosis genes induced during infection of human macrophages. Infect. Immun. 70:2787-2795.
17. Ebert, D. L., and K. N. Olivier. 2002. Nontuberculosis mycobacteria in the setting of cystic fibrosis. Clin. Chest Med. 23:655-663.
18. Falkinham, J. O., III, C. D. Norton, and M. W. LeChevallier. 2001. Factors influencing numbers of Mycobacterium avium, Mycobacterium intracellular, and other Mycobacteria in drinking water distribution systems. Appl. Environ. Microbiol. 67:1225-1231.
19. Fol, M., A. Chauhan, N. K. Nair, E. Maloney, M. Moomey, C. Jagannath, M. V. Madiraju, and M. Rajagopalan. 2006. Modulation of Mycobacterium tuberculosis proliferation by MtrA, an essential two-component response regulator. Mol. Microbiol. 60:643-657.
20. Frota, C. C., D. M. Hunt, R. S. Buxton, L. Rickman, J. Hinds, K. Kremer, D. van Soolingen, and M. J. Colston. 2004. Genome structure in the vole bacillus, Mycobacterium microti, a member of the Mycobacterium tuberculosis complex with a low virulence for humans. Microbiology 150:1519-1527.
21. Gonzalo Asensio, J., C. Maia, N. L. Ferrer, N. Barilone, F. Laval, C. Y. Soto, N. Winter, M. Daffe, B. Gicquel, C. Martin, and M. Jackson. 2006. The virulence-associated two-component PhoP-PhoR system controls the biosynthesis of polyketide-derived lipids in Mycobacterium tuberculosis. J. Biol. Chem. 281:1313-1316.
22. Hamelin, K., G. Bruant, A. El-Shaarawi, S. Hill, T. A. Edge, S. Bekal, J. M. Fairbrother, J. Harel, C. Maynard, L. Massen, and R. Brousseau. 2006. A virulence and antimicrobial resistance DNA microarray detects a high frequency of virulence genes in Escherichia coli isolates from Great Lakes recreational waters. Appl. Environ. Microbiol. 72:4200-4206.
23. Hamelin, K., G. Bruant, A. El-Shaarawi, S. Hill, T. A. Edge, J. Fairbrother, J. Harel, C. Maynard, L. Massen, and R. Brousseau. 2007. Occurrence of virulence and antimicrobial resistance genes in Escherichia coli isolates from different aquatic ecosystems within the St. Clair River and Detroit River areas. Appl. Environ. Microbiol. 73:477-484.
24. Harriff, M., L. Bermudez, and M. L. Kent. 2007. Experimental exposure of zebrafish (Danio rerio Hamilton) to Mycobacterium marinum and Mycobacterium peregrinum reveals the gastrointestinal tract as the primary route of infection: A potential model for environmental mycobacterial infection. J. Fish Dis. 30:587-600.
25. Hou, J. Y., J. E. Graham, and J. E. Clark-Curtiss. 2002. Mycobacterium avium genes expressed during growth in human macrophages detected by selective capture of transcribed sequences (SCOTS). Infect. Immun. 70:3714-3726.
26. Inderlied, C. B., L. S. Young, and J. K. Yamada. 1987. Determination of in vitro susceptibility of Mycobacterium avium complex isolates to antimycobacterial agents by various methods. Antimicrob. Agents Chemother. 31:1697-1702.
27. Kent, M. L., V. Watral, M. Wu, and L. E. Bermudez. 2006. In vivo and in vitro growth of Mycobacterium marinum at homoeothermic temperatures. FEMS Microbiol. Lett. 257:69-75.
28. Kent, M. L., C. M. Whipps, J. L. Matthews, D. Florio, V. Watral, J. K. Bishop-Stewart, M. Poort, and L. Bermudez. 2004. Mycobacteriosis in zebrafish (Danio rerio) research facilities. Comp. Biochem. Physiol. C 138: 383-390.
29. Lai, K. K., K. D. Stottmeier, I. H. Sherman, and W. R. McCabe. 1984. Mycobacterial cervical lymphadenopathy. Relation of etiologic agents to age. JAMA 251:1286-1288.
30. Li, F., and G. D. Stormo. 2001. Selection of optimal DNA oligos for gene expression arrays. Bioinformatics 17:1067-1076.
31. Marsh, I. B., J. P. Bannantine, M. L. Paustian, M. L. Tizard, V. Kapur, and R. J. Whittington. 2006. Genomic comparison of Mycobacterium avium subsp. paratuberculosis sheep and cattle strains by microarray hybridization. J. Bacteriol. 188:2290-2293.
32. Parish, T., D. A. Smith, S. Kendall, N. Casali, G. J. Bancroft, and N. G. Stoker. 2003. Deletion of two-component regulatory systems increases the virulence of Mycobacterium tuberculosis. Infect. Immun. 71:1134-1140.
33. Parish, T., D. A. Smith, G. Roberts, J. Betts, and N. G. Stoker. 2003. The senX3-regX3 two-component regulatory system of Mycobacterium tuberculosis is required for virulence. Microbiology 149:1423-1435.
34. Pattyn, S. R., and G. Verdoolaeche-Van Loo. 1974. The result of inoculation of Mycobacterium leprae in the goldfish (Carassius auratus). Acta Zool. Pathol. Antverp. 58:109-116.
35. Paustian, M. L., V. Kapur, and J. P. Bannantine. 2005. Comparative genomic hybridizations reveal genetic regions within the Mycobacterium avium complex that are divergent from Mycobacterium avium subsp. paratuberculosis isolates. J. Bacteriol. 187:2406-2415.
36. Perez, E., S. Samper, Y. Bordas, C. Guilhot, B. Gicquel, and C. Martin. 2001. An essential role for phoP in Mycobacterium tuberculosis virulence. Mol. Microbiol. 41:179-187.
37. Poort, M. J., C. M. Whipps, V. G. Watral, W. F. Font, and M. L. Kent. 2006. Molecular characterization of a Mycobacterium species in non-native poeciliids in Hawaii using DNA sequences. J. Fish Dis. 29:181-185.
38. Porwollik, S., E. F. Boyd, C. Choy, P. Cheng, L. Florea, E. Proctor, and M. McClelland. 2004. Characterization of Salmonella enterica subspecies I genovars by use of microarrays. J. Bacteriol. 186:5883-5898.
39. Porwollik, S., C. A. Santiviago, P. Cheng, L. Florea, and M. McClelland. 2005. Differences in gene content between Salmonella enterica serovar Enteritidis isolates and comparison to closely related serovars Gallinarum and Dublin. J. Bacteriol. 187:6545-6555.
40. Porwollik, S., R. M. Wong, and M. McClelland. 2002. Evolutionary genomics of Salmonella: gene acquisitions revealed by microarray analysis. Proc. Natl. Acad. Sci. USA 99:8956-8961.
41. Pozos, T. C., and L. Ramakrishnan. 2004. New models for the study of Mycobacterium-host interactions. Curr. Opin. Immunol. 16:499-505.
42. Prouty, M. G., N. E. Correa, L. P. Barker, P. Jagadeeswaran, and K. E. Klose. 2003. Zebrafish-Mycobacterium marinum model for mycobacterial pathogenesis. FEMS Microbiol. Lett. 225:177-182.
43. Ramakrishnan, L. 2004. Using Mycobacterium marinum and its hosts to study tuberculosis. Curr. Sci. 86:82-92.
44. Ross, A. J. 1960. Mycobacterium salmoniphilum sp. nov. from salmonid fishes. Am. Rev. Respir. Dis. 81:241-250.
45. Ruley, K. M., R. Reimschuessel, and M. Trucksis. 2002. Goldfish as an animal model system for mycobacterial infection. Methods Enzymol. 358:29-39.
46. Sanders, G. E., and L. E. Swaim. 2001. Atypical piscine mycobacteriosis in Japanese medaka (Oryzias latipes). Comp. Med. 51:171-175.
47. Sassetti, C. M., and E. J. Rubin. 2003. Genetic requirements for mycobacterial survival during infection. Proc. Natl. Acad. Sci. USA 100:12989-12994.
48. Semret, M., G. Zhai, S. Mostowy, C. Cleto, D. Alexander, G. Cangelosi, D. Cousins, D. M. Collins, D. van Soolingen, and M. A. Behr. 2004. Extensive genomic polymorphism within Mycobacterium avium. J. Bacteriol. 186:6332-6334.
49. Talaat, A. M., R. Reimschuessel, S. S. Wasserman, and M. Trucksis. 1998. Goldfish, Carassius auratus, a novel animal model for the study of Mycobacterium marinum pathogenesis. Infect. Immun. 66:2938-2942.
50. van der Sar, A. M., B. J. Appelmelk, C. M. Vandenbroucke-Grauls, and W. Bitter. 2004. A star with stripes: zebrafish as an infection model. Trends Microbiol. 12:451-457.
51. Watral, V., and M. L. Kent. 2007. Pathogenesis of Mycobacterium spp. in zebrafish (Danio rerio) from research facilities. Comp. Biochem. Physiol. C 145:55-60.
52. Whipps, C. M., W. R. Butler, F. Pourahmad, V. Watral, and M. L. Kent. 2007. Molecular systematics support the revival of Mycobacterium salmoniphilum (ex Ross, 1960) sp. nov., nom. rev., a species closely related to Mycobacterium chelonae. Int. J. Syst. Evol. Microbiol. 57:2525-2531.
53. Whipps, C. M., S. T. Dougan, and M. L. Kent. 2007. Mycobacterium haemophilum infections of zebrafish (Danio rerio) in research facilities. FEMS Microbiol. Lett. 270:21-26.
54. Whipps, C. M., V. G. Watral, and M. L. Kent. 2003. Characterization of a Mycobacterium sp. in rockfish, Sebastes alutus (Gilbert) and Sebastes reedi (Westrheim and Tsuyuki), using rDNA sequences. J. Fish Dis. 26:241-245.
55. Zahrt, T. C., and V. Deretic. 2000. An essential two-component signal transduction system in Mycobacterium tuberculosis. J. Bacteriol. 182:3832-3838.