Human alveolar macrophage gene responses to mycobacterium tuberculosis strains H37Ra and H37Rv

American Journal of Respiratory Cell and Molecular Biology

Volumn 40, Issue 4, 2009, Pages 491-504

  Silver, Richard F ^a,b,c   Walrath, Jessica ^a,c   Lee, Hung ^a,c   Jacobson, Bruce A ^d   Horton, Heidi ^d   Bowman, Michael R ^d   Nocka, Karl ^d   Sypek, Joseph P ^d  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY HOSPITALS OF CLEVELAND   (United States)

^c LOUIS STOKES CLEVELAND VA MEDICAL CENTER   (United States)

^d PFIZER INC   (United States)

Author keywords

Alveolar macrophage; IL 23; Microarray; Tuberculosis; Virulence

Indexed keywords

GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 12P35; INTERLEUKIN 23; INTERLEUKIN 23P19;

ARTICLE; BACTERIAL IMMUNITY; BACTERIAL STRAIN; BACTERIAL VIRULENCE; CELL TYPE; CONTROLLED STUDY; CYTOKINE PRODUCTION; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; LUNG ALVEOLUS MACROPHAGE; LUNG TUBERCULOSIS; MICROARRAY ANALYSIS; MONOCYTE; MYCOBACTERIUM TUBERCULOSIS; MYCOBACTERIUM TUBERCULOSIS H37RA; MYCOBACTERIUM TUBERCULOSIS H37RV; UPREGULATION; BIOSYNTHESIS; CLASSIFICATION; CYTOLOGY; DNA MICROARRAY; DOWN REGULATION; GENETICS; INTRACELLULAR SPACE; LUNG LAVAGE; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; POLYMERASE CHAIN REACTION; TUBERCULOSIS;

MYCOBACTERIUM TUBERCULOSIS;

BRONCHOALVEOLAR LAVAGE FLUID; DOWN-REGULATION; GENE EXPRESSION REGULATION; GRANULOCYTE-MACROPHAGE COLONY-STIMULATING FACTOR; HUMANS; INTERLEUKIN-23; INTRACELLULAR SPACE; MACROPHAGES, ALVEOLAR; MONOCYTES; MYCOBACTERIUM TUBERCULOSIS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; POLYMERASE CHAIN REACTION; TUBERCULOSIS; UP-REGULATION;

EID: 63349104087     PISSN: 10441549     EISSN: None     Source Type: Journal    
DOI: 10.1165/rcmb.2008-0219OC     Document Type: Article

References (45)

1. Steenken JWJ, Gardner LU. History of H37 strain of tubercle bacillus. Am Rev Tuberc 1946;54:62-66.
2. Pierce CH, Dubos RJ, Schaefer WB. Multiplication and survival of tubercle bacilli in the organs of mice. J Exp Med 1953;92:189-206.
3. Collins FM, Smith MJ. A comparative study of the virulence of Mycobacterium tuberculosis measured in mice and guinea pigs. Am Rev Respir Dis1969;100:631-639.
4. Cole ST, Brosch R, Parkhill J, Gamier T, Churcher C, Harris D, Gordon SV, Eiglmeier K, Gas S, Barry CE, et al. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature1998;393:537-544.
5. Brosch R, Phillip WJ, Stravropoulos E, Colston MJ, Cole ST, Gordon SV. Genomic analysis reveals variation between Mycobacterium H37Rv and the attenuated M. tuberculosis H37Ra strain. Infect Immun 1999;67:5768-5774.
6. Betts JC, Lukey PT, Robb LC, McAdam RA, Duncan K. Evaluation of a nutrient starvation model of M. tuberculosis persistence by gene and protein expression profiling. Mol Microbiol 2002;43:717-731.
7. Fisher MA, Plikaytis BB, Shinnick TM. Microarray analysis of the Mycobacterium tuberculosis transcriptional response to the acidic conditions found in phagosomes. J Bacteriol 2002;184:4025-432.
8. Gao Q, Kripke KE, Saldanha AJ, Holmes S, Small PM. Gene expression diversity among Mycobacterium tuberculosis clinical isolates. Microbiology 2005;151:5-14.
9. Zhang M, Gong J, Lin Y, Barnes PF. Growth of virulent and avirulent Mycobacterium tuberculosis strains in human macrophages. Infect Immun 1998;66:794-799.
10. Silver RF, Li Q, Ellner JJ. Expression of virulence of Mycobacterium tuberculosis within human monocytes: virulence correlates with intracellular growth and induction of tumor necrosis factor alpha, but not with evasion of lymphocyte-dependent monocyte effector functions. Infect Immun 1998;66:1190-1199.
11. Zhang M, Gong J, Yang Z, Samten B, Cave MD, Barnes PF. Enhanced capacity of a widespread strain of Mycobacterium tuberculosis to grow in human macrophages. J Infect Dis 1999;179:1213-1217.
12. Theus SA, Cave MD, Eisenach KD. Intracellular macrophage growth rates and cytokine profiles of Mycobacterium tuberculosis strains with different transmission dynamics. J Infect Dis 2005;191:453-460.
13. Spira A, Carroll JD, Liu G, Aziz Z, Shah V, Kornfeld H, Keane J. Apoptosis genes in human alveolar macrophages infected with virulent or attenuated Mycobacterium tuberculosis: a pivotal role for tumor necrosis factor. Am J Respir Cell Mol Biol 2003;29:545-551.
14. Manca C, Reed MB, Freeman S, Mathema B, Kreiswirth B, Barry CE III, Kaplan G. Differential monocyte activation underlies strainspecific Mycobacterium tuberculosis pathogenesis. Infect Immun 2004;72:5511-5514.
15. Silver RF, Li Q, Boom WH, Ellner JJ. Lymphocyte-dependent inhibition of growth of virulent Mycobacterium tuberculosis H37Rv within human monocytes: requirement for CD4+ T cells in purified protein derivative-positive, but not in purified protein derivativenegative subjects.J Immunol 1998;160:2408-2417.
16. Byrne MC, Whiteley MZ, Follettie MT. Preparation of mRNA for expression monitoring. In: Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA, Struhl K, editors. Current protocols in molecular biology. Hoboken, NJ: John Wiley and Sons; 2000.
17. Hill AA, Brown EL, Whitely MZ, Tucker-Kellogg G, Hunter CP, Slonim DK. Evaluation of normalization procedures for oligonucleotide array data based on spiked cRNA controls. Genome Biology 2001;2:0055.1-0055.13.
18. Affymetrix. Statistical algorithms description document. [Accessed 2002.] Available from: http://www.affymetrix.com/support/technical/ whitepapers/sadd-whitepaper.pdf
19. Aggarwal S, Ghilardi N, Xie M-H, de Sauvage FJ, Gurney AL. Interleukin-23 promotes a distinct CD4 T cell activation state characterized by the production of Interleukin-17.J Biol Chem 2003;278:1910-1914.
20. Oppmann B, Lesley R, Blom B, Timans JC, Xu Y, Hunte B, Vega F, Yu N, Wang J, Singh K., et al. Novel pl9 protein engages IL-12p40 to form a new cytokine, IL-23, with biological activities similar as well as distinct from IL-12. Immunity 2000;13:715-725.
21. Nau GJ, Richmond JFL, Schlesinger A, Jennings EG, Lander ES, Young RA. Human macrophage activation programs induced by bacterial pathogens. Proc Natl Acad Sci USA 2002;99:1503-1508.
22. Sadek MI, Sada E, Toossi Z, Schwander SK, Rich EA. Chemokines induced by infection of mononuclear phagocytes with mycobacteria and present in lung alveoli during active pulmonary tuberculosis. Am J Respir Cell Mol Biol 1998;19:513-521.
23. Keane J, Remold HG, Kornfeld H. Virulent mycobacterium tuberculosis strains evade apoptosis of infected alveolar macrophages. J Immunol 2000;164:2016-2020.
24. Li Q, Whalen CC, Larkin R, Zukowski L, Albert J, Cave MD, Silver RF. Differences in rate and variability of intracellular growth of a panel of clinical isolates of Mycobacterium tuberculosis within a human monocyte model. Infect Immun 2002;70:6489-6493.
25. Fulton SA, Johnsen JM, Wolf SF, Sieburth DS, Boom WH. Interleukin- 12 production by human monocytes infected with Mycobacterium tuberculosis: role of phagocytosis. Infect Immun 1996;64:2523-2531.
26. Cooper AM, Magram J, Ferrante J, Orme IM. Interleukin 12 (IL-12) is crucial to the development of protective immunity in mice intravenously infected with Mycobacterium tuberculosis. J Exp Med 1997;186:39-45.
27. Altare F, Durandy A, Lammas D, Emile JF, Lamhamedi S, Le Deist F, Drysdale P, Jouanguy E, Doffinger R, Bernaudin F, et al. Impairment of mycobacterial immunity in human interleukin-12 receptor deficiency. Science1998;280:1432-1435.
28. de Jong R, Altare F, Haagen IA, Elferink DG, Boer T, van Breda Vriesman PJ, Kabel PJ, Draaisma JM, van Dissel JT, Kroon FP, et al. Severe mycobacterial and Salmonella infections in interleukin-12 receptor-deficient patients. Science 1998;280:1435-1438.
29. Cooper AM, Kipnis A, Turner J, Magram J, Ferrante J, Orme IM. Mice lacking bioactive IL-12 can generate protective, antigen-specific cellular responses to mycobacterial infection only if the IL-12 p40 subunit is present. J Immunol 2002;168:1322-1327.
30. Khader SA, Pearl JE, Sakamoto K, Gilmartin L, Bell GK, Jelley-Gibbs DM, Ghilardi N, deSauvage F, Cooper AM. IL-23 compensates for the absence of IL-12 p70 and is essential for the IL-17 response during tuberculosis but is dispensable for protection and antigenspecific IFN-γ responses if IL-12 p70 is available. J Immunol 2005; 175:788-795.
31. Khader S, Bell G, Pearl J, Fountain J, Rangel-Moreno J, Cilley G, Shen F, Eaton S, Gaffen S, Swain S, et al. IL-23 and IL-17 in the establishment of preective pulmonary CD4+ T-cell responses after vaccination and during Mycobacterium tuberculosis challenge. Nat Immunol 2007;8:369-377.
32. Robinson DS, Bentley AM, Hartnell A, Kay AB, Durham SR. Activated memory T helper cells in bronchoalveolar lavage fluid from patients with atopic asthma: relation to asthma symptoms, lung function, and bronchial responsiveness. Thorax 1993;48:26-32.
33. Walrath J, Zukowski L, Krywiak A, Silver RF. Resident Thl-like effector memory cells in pulmonary recall responses to Mycobacterium tuberculosis. Am J Respir Cell Mol Biol 2005;33:48-55.
34. Gonzalez-Juarrero M, Hattle JM, Izzo A, Junqueira-Kipnis AP, Shim TS, Trapnell BC, Cooper AM, Orme IM. Disruption of granulocyte macrophage-colony stimulating factor production in the lungs severely affects the ability of mice to control Mycobacterium tuberculosis infection. J Leukoc Biol 2005;77:914-922.
35. Verreck FAW, de Boer T, Langenberg DML, Hoeve MA, Kramer M, Vaisberg E, Kastelein R, Kolk A, de Waal-Malefyt R, Ottenhoff THM. Human IL-23-producing type 1 macrophages promote but IL- 10-producing type 2 macrophages subvert immunity to (myco)bacteria. Proc Natl Acad Sci USA 2004;101:4560-4565.
36. Sreevatsan S, Pan X, Stockbauer KE, Connell ND, Kresiwirth BN, Whittam TS, Musser JM. Restricted structural gene polymorphism in the Mycobacterium tuberculosis complex indicates evolutionarily recent global dissemination. Proc Natl Acad Sci USA 1997;94:9869- 9874.
37. Agerton TB, Valway SE, Blinkhorn RJ, Shilkret KL, Reves R, Schluter WW, Gore B, Pozsik CJ, Plikaytis BB, Woodley C, et al. Spread of strain W, a highly drug-resistant strain of Mycobacterium tuberculosis, across the United States. Clin Infect Dis1999;29:85-92.
38. Milan SJ, Haugue KA, Kurepina NE, Lofy KH, Goldberg SV, Narita M, Nolan CM, McElroy PD, Kresiwirth BN, Cangelosi GA. Expanded geographical distribution of the N family of Mycobacterium tuberculosis strains within the United States. J Clin Microbiol 2004;42:1064- 1068.
39. Glynn J, Witely J, Bifani P, Kremer K, van Soolingen D. Worldwide occurrence of Beijing/W strans of Mycobacterium tuberculosis: a systemic review. Emerg Infect Dis 2002;8:843-849.
40. Bifani P, Moghazeh S, Shopsin B, Driscoll J, Ravikovitch A, Kreiswirth B. Molecular characterization of Mycobacterium tuberculosis H37Rv/ Ra variants: sintinguishing the mycobacterial laboratory strain. J Clin Microbiol 2000;38:3200-3204.
41. Valway S, Sanchez M, Shinnick T, Orme I, Argerton T, Hoy D, Jones J, Westermoreland H, Onorato I. An outbreak involving extensive transmission of a virulent strain of Mycobacterium tuberculosis. N Engl J Med1998;10:633- 639.
42. Reed M, Domenech P, Manca C, Su H, Barczak A, Kreiswirth B, Kaplan G, Barry CEI. A glycolipid of hypervirulent tuberculosis strains that inhibits the innate immune response. Nature 2004;431:84-87.
43. McDonough KA, Kress Y, Bloom BR. Pathogenesis of tuberculosis: interaction of Mycobacterium tuberculosis with macrophages. Infect Immun 1993;61:2763-2773.
44. North RJ, Izzo AA. Mycobacterial virulence: virulent strains of Mycobacteria tuberculosis have faster in vivo doubling times and are better equipped to resist growth-inhibiting functions of macrophages in the presence and absence of specific immunity. J Exp Med 1993;177:1723-1733.
45. McMurray D, Carlomango M, Cumberland P. Respiratory infection with attenuated Mycobacterium tuberculosis H37Ra in malnourished guinea pigs. Infect Immun1982;39:793-799.