Mycobacterium tuberculosis nuoG Is a virulence gene that inhibits apoptosis of infected host cells

PLoS Pathogens

Volumn 3, Issue 7, 2007, Pages 0972-0980

  Velmurugan, Kamalakannan ^a   Chen, Bing ^b   Miller, Jessica L ^a   Azogue, Sharon ^a   Gurses, Serdar ^a   Hsu, Tsungda ^b   Glickman, Michael ^c   Jacobs Jr , William R ^b   Porcelli, Steven A ^b   Briken, Volker ^a  

^a Bldg 142   (United States)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^c MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BACTERIAL GENE; BACTERIAL VIRULENCE; CELL DEATH; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME SUBUNIT; FEMALE; GENE DELETION; GENE LOCUS; GENETIC SCREENING; GENETIC TRAIT; HOST RESISTANCE; HUMAN; HUMAN CELL; LUNG TUBERCULOSIS; MOUSE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; SCID MOUSE; ANIMAL; BAGG ALBINO MOUSE; CELL LINE; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENE SILENCING; GENETICS; HOST PATHOGEN INTERACTION; MACROPHAGE; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; MONOCYTE; MOUSE MUTANT; PATHOGENICITY; PATHOLOGY; VIRULENCE;

CORYNEBACTERINEAE; MUS; MYCOBACTERIUM TUBERCULOSIS;

REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE DEHYDROGENASE;

ANIMALS; APOPTOSIS; BASE SEQUENCE; CELL LINE; FEMALE; GENE EXPRESSION REGULATION, BACTERIAL; GENE SILENCING; GENES, BACTERIAL; HOST-PATHOGEN INTERACTIONS; HUMANS; MACROPHAGES; MICE; MICE, INBRED BALB C; MICE, SCID; MOLECULAR SEQUENCE DATA; MONOCYTES; MYCOBACTERIUM TUBERCULOSIS; NADH DEHYDROGENASE; NADPH DEHYDROGENASE; VIRULENCE;

EID: 34547642553     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.0030110     Document Type: Article

References (47)

1. Dye C, Watt CJ, Bleed DM, Hosseini SM, Raviglione MC (2005) Evolution of tuberculosis control and prospects for reducing tuberculosis incidence, prevalence, and deaths globally. JAMA 293: 2767-2775.
2. Manabe YC, Bishai WR (2000) Latent Mycobacterium tuberculosis - Persistence, patience, and winning by waiting. Nat Med 6: 1327-1329.
3. Honer zu Bentrup K, Russell DG (2001) Mycobacterial persistence: Adaptation to a changing environment. Trends Microbiol 9: 597-605.
4. Hingley-Wilson SM, Sambandamurthy VK, Jacobs WR Jr (2003) Survival perspectives from the world's most successful pathogen, Mycobacterium tuberculosis. Nat Immunol 4: 949-955.
5. Smith CV, Sharma V, Sacchettini JC (2004) TB drug discovery: Addressing issues of persistence and resistance. Tuberculosis (Edinb) 84: 45-55.
6. Abramovitch RB, Martin GB (2004) Strategies used by bacterial pathogens to suppress plant defenses. Curr Opin Plant Biol 7: 356-364.
7. Stuart LM, Ezekowitz RA (2005) Phagocytosis: Elegant complexity. Immunity 22: 539-550.
8. Boya P, Roques B, Kroemer G (2001) New EMBO members' review: Viral and bacterial proteins regulating apoptosis at the mitochondrial level. EMBO J 20: 4325-4331.
9. Dockrell DH (2003) The multiple roles of Fas ligand in the pathogenesis of infectious diseases. Clin Microbiol Infect 9: 766-779.
10. Hilleman MR (2004) Strategies and mechanisms for host and pathogen survival in acute and persistent viral infections. Proc Natl Acad Sci U S A 101 (Suppl 2): 14560-14566.
11. Monack DM, Mueller A, Falkow S (2004) Persistent bacterial infections: the interface of the pathogen and the host immune system. Nat Rev Microbiol 2: 747-765.
12. Hacker G, Kirschnek S, Fischer SF (2006) Apoptosis in infectious disease: How bacteria interfere with the apoptotic apparatus. Med Microbiol Immunol 195: 11-19.
13. Rojas M, Barrera LF, Puzo G, Garcia LF (1997) Differential induction of apoptosis by virulent Mycobacterium tuberculosis in resistant and susceptible murine macrophages: Role of nitric oxide and mycobacterial products. J Immunol 159: 1352-1361.
14. Danelishvili L, McGarvey J, Li YJ, Bermudez LE (2003) Mycobacterium tuberculosis infection causes different levels of apoptosis and necrosis in human macrophages and alveolar epithelial cells. Cell Microbiol 5: 649-660.
15. Schaible UE, Winau F, Sieling PA, Fischer K, Collins HL, et al. (2003) Apoptosis facilitates antigen presentation to T lymphocytes through MHC-I and CD1 in tuberculosis. Nat Med 9: 1039-1046.
16. Derrick SC, Morris SL (2007) The ESAT6 protein of Mycobacterium tuberculosis induces apoptosis of macrophages by activating caspase expression. Cell Microbiol 9: 1547-1555.
17. Keane J, Remold HG, Kornfeld H (2000) Virulent Mycobacterium tuberculosis strains evade apoptosis of infected alveolar macrophages. J Immunol 164: 2016-2020.
18. Oddo M, Renno T, Attinger A, Bakker T, MacDonald HR, et al. (1998) Fas ligand-induced apoptosis of infected human macrophages reduces the viability of intracellular Mycobacterium tuberculosis. J Immunol 160: 5448-5454.
19. Sly LM, Hingley-Wilson SM, Reiner NE, McMaster WR (2003) Survival of Mycobacterium tuberculosis in host macrophages involves resistance to apoptosis dependent upon induction of antiapoptotic Bcl-2 family member Mcl-1. J Immunol 170: 430-437.
20. Pan H, Yan BS, Rojas M, Shebzukhov YV, Zhou H, et al. (2005) Ipr1 gene mediates innate immunity to tuberculosis. Nature 434: 767-772.
21. Kausalya S, Somogyi R, Orlofsky A, Prystowsky MB (2001) Requirement of A1-a for bacillus Calmette-Guerin-mediated protection of macrophages against nitric oxide-induced apoptosis. J Immunol 166: 4721-4727.
22. Kremer L, Estaquier J, Brandt E, Ameisen JC, Locht C (1997) Mycobacterium bovis Bacillus Calmette Guerin infection prevents apoptosis of resting human monocytes. Eur J Immunol 27: 2450-2456.
23. Riendeau CJ, Kornfeld H (2003) THP-1 cell apoptosis in response to Mycobacterial infection. Infect Immun 71: 254-259.
24. Loeuillet C, Martinon F, Perez C, Munoz M, Thome M, et al. (2006) Mycobacterium tuberculosis subverts innate immunity to evade specific effectors. J Immunol 177: 6245-6255.
25. Balcewicz-Sablinska MK, Keane J, Kornfeld H, Remold HG (1998) Pathogenic Mycobacterium tuberculosis evades apoptosis of host macrophages by release of TNF-R2, resulting in inactivation of TNF-alpha. J Immunol 161: 2636-2641.
26. McKinney JD, Honer zu Bentrup K, Munoz-Elias EJ, Miczak A, Chen B, et al. (2000) Persistence of Mycobacterium tuberculosis in macrophages and mice requires the glyoxylate shunt enzyme isocitrate lyase. Nature 406: 735-738.
27. Stewart GR, Robertson BD, Young DB (2003) Tuberculosis: A problem with persistence. Nat Rev Microbiol 1: 97-105.
28. Fratazzi C, Arbeit RD, Carini C, Remold HG (1997) Programmed cell death of Mycobacterium avium serovar 4-infected human macrophages prevents the mycobacteria from spreading and induces mycobacterial growth inhibition by freshly added, uninfected macrophages. J Immunol 158: 4320-4327.
29. Molloy A, Laochumroonvorapong P, Kaplan G (1994) Apoptosis, but not necrosis, of infected monocytes is coupled with killing of intracellular bacillus Calmette-Guerin. J Exp Med 180: 1499-1509.
30. Winau F, Kaufmann SH, Schaible UE (2004) Apoptosis paves the detour path for CD8 T cell activation against intracellular bacteria. Cell Microbiol 6: 599-607.
31. Winau F, Hegasy G, Kaufmann SH, Schaible UE (2005) No life without death-apoptosis as prerequisite for T cell activation. Apoptosis 10: 707-715.
32. Kaufmann SH (2006) Tuberculosis: Back on the immunologists' agenda. Immunity 24: 351-357.
33. Grode L, Seiler P, Baumann S, Hess J, Brinkmann V, et al. (2005) Increased vaccine efficacy against tuberculosis of recombinant Mycobacterium bovis bacille Calmette-Guerin mutants that secrete listeriolysin. J Clin Invest 115: 2472-2479.
34. Kaufmann SH (2006) Envisioning future strategies for vaccination against tuberculosis. Nat Rev Immunol 6: 699-704.
35. Snapper SB, Melton RE, Mustafa S, Kieser T, Jacobs WR Jr (1990) Isolation and characterization of efficient plasmid transformation mutants of Mycobacterium smegmatis. Mol Microbiol 4: 1911-1919.
36. Cole ST, Brosch R, Parkhill J, Garnier T, Churcher C, et al. (1998) Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393: 537-544.
37. Bardarov S, Bardarov Jr S, Pavelka Jr MS, Sambandamurthy V, Larsen M, et al. (2002) Specialized transduction: An efficient method for generating marked and unmarked targeted gene disruptions in Mycobacterium tuberculosis, M. bovis BCG and M. smegmatis. Microbiology 148: 3007-3017.
38. Stover CK, de la Cruz VF, Fuerst TR, Burlein JE, Benson LA, et al. (1991) New use of BCG for recombinant vaccines. Nature 351: 456-460.
39. Sassetti CM, Boyd DH, Rubin EJ (2003) Genes required for mycobacterial growth defined by high density mutagenesis. Mol Microbiol 48: 77-84.
40. Shi L, Sohaskey CD, Kana BD, Dawes S, North RJ, et al. (2005) Changes in energy metabolism of Mycobacterium tuberculosis in mouse lung and under in vitro conditions affecting aerobic respiration. Proc Natl Acad Sci U S A 102: 15629-15634.
41. Weinstein EA, Yano T, Li LS, Avarbock D, Avarbock A, et al. (2005) Inhibitors of type II NADH:menaquinone oxidoreductase represent a class of antitubercular drugs. Proc Natl Acad Sci U S A 102: 4548-4553.
42. Friedrich T, Bottcher B (2004) The gross structure of the respiratory complex I: A Lego system. Biochim Biophys Acta 1608: 1-9.
43. Braunstein M, Brown AM, Kurtz S, Jacobs WR Jr. (2001) Two nonredundant SecA homologues function in mycobacteria. J Bacteriol 183: 6979-6990.
44. Hinchey J, Lee S, Jeon BY, Basaraba RJ, Venkataswamy MM, et al. (2007) Enhanced priming of adaptive immunity by a proapoptotic mutant of Mycobacterium tuberculosis. J Clin Invest. In press.
45. Edwards KM, Cynamon MH, Voladri RK, Hager CC, DeStefano MS, et al. (2001) Iron-cofactored superoxide dismutase inhibits host responses to Mycobacterium tuberculosis. Am J Respir Crit Care Med 164: 2213-2219.
46. Dao DN, Kremer L, Guerardel Y, Molano A, Jacobs WR Jr, et al. (2004) Mycobacterium tuberculosis lipomannan induces apoptosis and interleukin-12 production in macrophages. Infect Immun 72: 2067-2074.
47. Bange FC, Collins FM, Jacobs WR Jr (1999) Survival of mice infected with Mycobacterium smegmatis containing large DNA fragments from Mycobacterium tuberculosis. Tuber Lung Dis 79: 171-180.