Differential influence of nutrient-starved Mycobacterium tuberculosis on adaptive immunity results in progressive tuberculosis disease and pathology

Infection and Immunity

Volumn 83, Issue 12, 2015, Pages 4731-4739

  Dietrich, Jes ^a   Roy, Sugata ^a,c   Rosenkrands, Ida ^a   Lindenstrøm, Thomas ^a   Filskov, Jonathan ^a   Rasmussen, Erik Michael ^a   Cassidy, Joseph ^b   Andersen, Peter ^a  

^a STATENS SERUM INSTITUT   (Denmark)

^b UNIVERSITY COLLEGE DUBLIN   (Ireland)

^c RIKEN   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 2; TUMOR NECROSIS FACTOR ALPHA; BACTERIAL ANTIGEN; CULTURE MEDIUM; PEPTIDE; TUMOR NECROSIS FACTOR;

ADAPTIVE IMMUNITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD4+ T LYMPHOCYTE; COLONY FORMING UNIT; DISEASE COURSE; FEMALE; IMMUNOPATHOLOGY; IN VITRO STUDY; IN VIVO STUDY; MOUSE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; NUTRIENT LIMITATION; PRIORITY JOURNAL; TUBERCULOSIS; ANIMAL; BACTERIAL COUNT; BAGG ALBINO MOUSE; BIOSYNTHESIS; C57BL MOUSE; CHEMISTRY; CHIMERA; CULTURE MEDIUM; DISEASE MODEL; DRUG EFFECTS; GENE EXPRESSION; GROWTH, DEVELOPMENT AND AGING; HOST PATHOGEN INTERACTION; HUMAN; IMMUNOLOGY; IMMUNOPHENOTYPING; MICROBIOLOGY; PATHOLOGY; PHARMACOLOGY; STARVATION; SYNTHESIS; T LYMPHOCYTE; TUBERCULOSIS, PULMONARY; VACCINATION;

ADAPTIVE IMMUNITY; ANIMALS; ANTIGENS, BACTERIAL; CHIMERA; COLONY COUNT, MICROBIAL; CULTURE MEDIA; DISEASE MODELS, ANIMAL; GENE EXPRESSION; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNOPHENOTYPING; INTERFERON-GAMMA; INTERLEUKIN-2; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MYCOBACTERIUM TUBERCULOSIS; PEPTIDES; STARVATION; T-LYMPHOCYTES; TUBERCULOSIS, PULMONARY; TUMOR NECROSIS FACTOR-ALPHA; VACCINATION;

EID: 84949637879     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01055-15     Document Type: Article

References (54)

1. Smeulders MJ, Keer J, Speight RA, Williams HD. 1999. Adaptation of Mycobacterium smegmatis to stationary phase. J Bacteriol 181:270-283.
2. Gengenbacher M, Kaufmann SHE. 2012. Mycobacterium tuberculosis: success through dormancy. FEMS Microbiol Rev 36:514-532. http://dx.doi.org/10.1111/j.1574-6976.2012.00331.x.
3. Kochi A. 1994. Tuberculosis: distribution, risk factors, mortality. Immunobiology 191:325-336. http://dx.doi.org/10.1016/S0171-2985(11)80437-7.
4. Tsai MC, Chakravarty S, Zhu G, Xu J, Tanaka K, Koch C, Tufariello J, Flynn J, Chan J. 2006. Characterization of the tuberculous granuloma in murine and human lungs: cellular composition and relative tissue oxygen tension. Cell Microbiol 8:218-232. http://dx.doi.org/10.1111/j.1462-5822.2005.00612.x.
5. Nathan C, Shiloh MU. 2000. Reactive oxygen and nitrogen intermediates in the relationship between mammalian hosts and microbial pathogens. Proc Natl Acad Sci U S A 97:8841-8848. http://dx.doi.org/10.1073/pnas.97.16.8841.
6. Ryter SW, Alam J, Choi AM. 2006. Heme oxygenase-1/carbon monoxide: from basic science to therapeutic applications. Physiol Rev 86:583-650. http://dx.doi.org/10.1152/physrev.00011.2005.
7. Rifat D, Bishai WR, Karakousis PC. 2009. Phosphate depletion: a novel trigger for Mycobacterium tuberculosis persistence. J Infect Dis 200: 1126-1135. http://dx.doi.org/10.1086/605700.
8. Wayne LG. 1976. Dynamics of submerged growth of Mycobacterium tuberculosis under aerobic and microaerophilic conditions. Am Rev Respir Dis 114:807-811.
9. Wayne LG, Hayes LG. 1996. An in vitro model for sequential study of shiftdown of Mycobacterium tuberculosis through two stages of nonreplicating persistence. Infect Immun 64:2062-2069.
10. Wayne LG, Sohaskey CD. 2001. Nonreplicating persistence of mycobacterium tuberculosis. Annu Rev Microbiol 55:139-163. http://dx.doi.org/10.1146/annurev.micro.55.1.139.
11. Leistikow RL, Morton RA, Bartek IL, Frimpong I, Wagner K, Voskuil MI. 2010. The Mycobacterium tuberculosis DosR regulon assists in metabolic homeostasis and enables rapid recovery from nonrespiring dormancy. J Bacteriol 192:1662-1670. http://dx.doi.org/10.1128/JB.00926-09.
12. Loebel RO, Shorr E, Richardson HB. 1933. The influence of foodstuffs upon the respiratory metabolism and growth of human tubercle bacilli. J Bacteriol 26:139-166.
13. Loebel RO, Shorr E, Richardson HB. 1933. The influence of adverse conditions upon the respiratory metabolism and growth of human tubercle bacilli. J Bacteriol 26:167-200.
14. Betts JC, Lukey PT, Robb LC, McAdam RA, Duncan K. 2002. Evaluation of a nutrient starvation model of Mycobacterium tuberculosis persistence by gene and protein expression profiling. Mol Microbiol 43:717-731. http://dx.doi.org/10.1046/j.1365-2958.2002.02779.x.
15. Betts JC, Dodson P, Quan S, Lewis AP, Thomas PJ, Duncan K, Mc-Adam RA. 2000. Comparison of the proteome of Mycobacterium tuberculosis strain H37Rv with clinical isolate CDC 1551. Microbiology 146: 3205-3216. http://dx.doi.org/10.1099/00221287-146-12-3205.
16. Aagaard C, Hoang T, Dietrich J, Cardona PJ, Izzo A, Dolganov G, Schoolnik GK, Cassidy JP, Billeskov R, Andersen P. 2011. A multistage tuberculosis vaccine that confers efficient protection before and after exposure. Nat Med 17:189-194. http://dx.doi.org/10.1038/nm.2285.
17. Kaufmann SH, Lange C, Rao M, Balaji KN, Lotze M, Schito M, Zumla AI, Maeurer M. 2014. Progress in tuberculosis vaccine development and host-directed therapies-a state of the art review. Lancet Respir Med 2:301-320. http://dx.doi.org/10.1016/S2213-2600(14)70033-5.
18. Samuel JE, Kiss K, Varghees S. 2003. Molecular pathogenesis of Coxiella burnetii in a genomics era. Ann N Y Acad Sci 990:653-663. http://dx.doi.org/10.1111/j.1749-6632.2003.tb07440.x.
19. Swanson MS, Fernandez-Moreira E. 2002. A microbial strategy to multiply in macrophages: the pregnant pause. Traffic 3:170-177. http://dx.doi.org/10.1034/j.1600-0854.2002.030302.x.
20. Hammerschlag MR. 2002. The intracellular life of chlamydiae. Semin Pediatr Infect Dis 13:239-248. http://dx.doi.org/10.1053/spid.2002.127201.
21. Molofsky AB, Swanson MS. 2004. Differentiate to thrive: lessons from the Legionella pneumophila life cycle. Mol Microbiol 53:29-40. http://dx.doi.org/10.1111/j.1365-2958.2004.04129.x.
22. Albrethsen J, Agner J, Piersma SR, Hojrup P, Pham TV, Weldingh K, Jimenez CR, Andersen P, Rosenkrands I. 2013. Proteomic profiling of Mycobacterium tuberculosis identifies nutrient-starvation-responsive toxin-antitoxin systems. Mol Cell Proteomics 12:1180-1191. http://dx.doi.org/10.1074/mcp.M112.018846.
23. Shleeva MO, Bagramyan K, Telkov MV, Mukamolova GV, Young M, Kell DB, Kaprelyants AS. 2002. Formation and resuscitation of "nonculturable" cells of Rhodococcus rhodochrous and Mycobacterium tuberculosis in prolonged stationary phase. Microbiology 148:1581-1591. http://dx.doi.org/10.1099/00221287-148-5-1581.
24. De Man JC. 1975. The probability of most probable numbers. Eur J Appl Microbiol 1:2.
25. Li H, Durbin R. 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25:1754-1760. http://dx.doi.org/10.1093/bioinformatics/btp324.
26. Billeskov R, Vingsbo-Lundberg C, Andersen P, Dietrich J. 2007. Induction of CD8 T cells against a novel epitope in TB10.4: correlation with mycobacterial virulence and the presence of a functional region of difference-1. J Immunol 179:3973-3981. http://dx.doi.org/10.4049/jimmunol.179.6.3973.
27. Biketov S, Mukamolova GV, Potapov V, Gilenkov E, Vostroknutova G, Kell DB, Young M, Kaprelyants AS. 2000. Culturability of Mycobacterium tuberculosis cells isolated from murine macrophages: a bacterial growth factor promotes recovery. FEMS Immunol Med Microbiol 29: 233-240. http://dx.doi.org/10.1111/j.1574-695X.2000.tb01528.x.
28. Zhang Y, Yang Y, Woods A, Cotter RJ, Sun Z. 2001. Resuscitation of dormant Mycobacterium tuberculosis by phospholipids or specific peptides. Biochem Biophys Res Commun 284:542-547. http://dx.doi.org/10.1006/bbrc.2001.4993.
29. Sun Z, Zhang Y. 1999. Spent culture supernatant of Mycobacterium tuberculosis H37Ra improves viability of aged cultures of this strain and allows small inocula to initiate growth. J Bacteriol 181:7626-7628.
30. Kell DB, Kaprelyants AS, Weichart DH, Harwood CR, Barer MR. 1998. Viability and activity in readily culturable bacteria: a review and discussion of the practical issues. Antonie Van Leeuwenhoek 73:169-187. http://dx.doi.org/10.1023/A:1000664013047.
31. Nyka W. 1974. Studies on the effect of starvation on mycobacteria. Infect Immun 9:843-850.
32. Deb C, Lee CM, Dubey VS, Daniel J, Abomoelak B, Sirakova TD, Pawar S, Rogers L, Kolattukudy PE. 2009. A novel in vitro multiple-stress dormancy model for Mycobacterium tuberculosis generates a lipidloaded, drug-tolerant, dormant pathogen. PLoS One 4:e6077. http://dx.doi.org/10.1371/journal.pone.0006077.
33. Andersen P, Doherty TM. 2005. TB subunit vaccines-putting the pieces together. Microbes Infect 7:911-921. http://dx.doi.org/10.1016/j.micinf.2005.03.013.
34. +-T-cell responses of Mycobacterium-infected mice to a newly identified major histocompatibility complex class I-restricted epitope shared by proteins of the ESAT-6 family. Infect Immun 71:7173-7177. http://dx.doi.org/10.1128/IAI.71.12.7173-7177.2003.
35. Radosevic K, Wieland CW, Rodriguez A, Weverling GJ, Mintardjo R, Gillissen G, Vogels R, Skeiky YA, Hone DM, Sadoff JC, van der Poll T, Havenga M, Goudsmit J. 2007. Protective immune responses to a recombinant adenovirus type 35 tuberculosis vaccine in two mouse strains: CD4 and CD8 T-cell epitope mapping and role of gamma interferon. Infect Immun 75:4105-4115. http://dx.doi.org/10.1128/IAI.00004-07.
36. Agger EM, Rosenkrands I, Olsen AW, Hatch G, Williams A, Kritsch C, Lingnau K, von Gabain A, Andersen CS, Korsholm KS, Andersen P. 2006. Protective immunity to tuberculosis with Ag85B-ESAT-6 in a synthetic cationic adjuvant system IC31. Vaccine 24:5452-5460. http://dx.doi.org/10.1016/j.vaccine.2006.03.072.
37. Lindenstrom T, Knudsen NP, Agger EM, Andersen P. 2013. Control of chronic mycobacterium tuberculosis infection by CD4 KLRG1-IL-2-secreting central memory cells. J Immunol 190:6311-6319. http://dx.doi.org/10.4049/jimmunol.1300248.
38. Woolhiser L, Tamayo MH, Wang B, Gruppo V, Belisle JT, Lenaerts AJ, Basaraba RJ, Orme IM. 2007. In vivo adaptation of the Wayne model of latent tuberculosis. Infect Immun 75:2621-2625. http://dx.doi.org/10.1128/IAI.00918-06.
39. Bacon J, Alderwick LJ, Allnutt JA, Gabasova E, Watson R, Hatch KA, Clark SO, Jeeves RE, Marriott A, Rayner E, Tolley H, Pearson G, Hall G, Besra GS, Wernisch L, Williams A, Marsh PD. 2014. Non-replicating Mycobacterium tuberculosis elicits a reduced infectivity profile with corresponding modifications to the cell wall and extracellular matrix. PLoS One 9:e87329. http://dx.doi.org/10.1371/journal.pone.0087329.
40. Redford PS, Murray PJ, O'Garra A. 2011. The role of IL-10 in immune regulation during M. tuberculosis infection. Mucosal Immunol 4:261-270. http://dx.doi.org/10.1038/mi.2011.7.
41. Feng CG, Kullberg MC, Jankovic D, Cheever AW, Caspar P, Coffman RL, Sher A. 2002. Transgenic mice expressing human interleukin-10 in the antigen-presenting cell compartment show increased susceptibility to infection with Mycobacterium avium associated with decreased macrophage effector function and apoptosis. Infect Immun 70:6672-6679. http://dx.doi.org/10.1128/IAI.70.12.6672-6679.2002.
42. Darrah PA, Patel DT, De Luca PM, Lindsay RW, Davey DF, Flynn BJ, Hoff ST, Andersen P, Reed SG, Morris SL, Roederer M, Seder RA. 2007. Multifunctional TH1 cells define a correlate of vaccine-mediated protection against Leishmania major. Nat Med 13:843-850. http://dx.doi.org/10.1038/nm1592.
43. Imai N, Ikeda H, Tawara I, Shiku H. 2009. Tumor progression inhibits the induction of multifunctionality in adoptively transferred tumorspecific CD8+ T cells. Eur J Immunol 39:241-253. http://dx.doi.org/10.1002/eji.200838824.
44. Forbes EK, Sander C, Ronan EO, McShane H, Hill AV, Beverley PC, Tchilian EZ. 2008. Multifunctional, high-level cytokine-producing Th1 cells in the lung, but not spleen, correlate with protection against Mycobacterium tuberculosis aerosol challenge in mice. J Immunol 181:4955-4964. http://dx.doi.org/10.4049/jimmunol.181.7.4955.
45. Kannanganat S, Ibegbu C, Chennareddi L, Robinson HL, Amara RR. 2007. Multiple-cytokine-producing antiviral CD4 T cells are functionally superior to single-cytokine-producing cells. J Virol 81:8468-8476. http://dx.doi.org/10.1128/JVI.00228-07.
46. Huet G, Constant P, Malaga W, Laneelle MA, Kremer K, van Soolingen D, Daffe M, Guilhot C. 2009. A lipid profile typifies the Beijing strains of Mycobacterium tuberculosis: identification of a mutation responsible for a modification of the structures of phthiocerol dimycocerosates and phenolic glycolipids. J Biol Chem 284:27101-27113. http://dx.doi.org/10.1074/jbc.M109.041939.
47. Dormans J, Burger M, Aguilar D, Hernandez-Pando R, Kremer K, Roholl P, Arend SM, van Soolingen D. 2004. Correlation of virulence, lung pathology, bacterial load and delayed type hypersensitivity responses after infection with different Mycobacterium tuberculosis genotypes in a BALB/c mouse model. Clin Exp Immunol 137:460-468. http://dx.doi.org/10.1111/j.1365-2249.2004.02551.x.
48. Barczak AK, Domenech P, Boshoff HI, Reed MB, Manca C, Kaplan G, Barry CE, III. 2005. In vivo phenotypic dominance in mouse mixed infections with Mycobacterium tuberculosis clinical isolates. J Infect Dis 192:600-606. http://dx.doi.org/10.1086/432006.
49. Wymann MP, Schneiter R. 2008. Lipid signalling in disease. Nat Rev Mol Cell Biol 9:162-176. http://dx.doi.org/10.1038/nrm2335.
50. Brennan PJ. 2003. Structure, function, and biogenesis of the cell wall of Mycobacterium tuberculosis. Tuberculosis (Edinb) 83:91-97. http://dx.doi.org/10.1016/S1472-9792(02)00089-6.
51. Asselineau J. 1966. The bacterial lipids. Hermann, Paris, France.
52. Minnikin DE. 1982. Lipids: complex lipids, their chemistry, biosynthesis and roles, p 95-184. InCRatledge and J L Stanford (ed), The biology of the mycobacteria. Academic Press, London, United Kingdom.
53. Daniel J, Maamar H, Deb C, Sirakova TD, Kolattukudy PE. 2011. Mycobacterium tuberculosis uses host triacylglycerol to accumulate lipid droplets and acquires a dormancy-like phenotype in lipid-loaded macrophages. PLoS Pathog 7:e1002093. http://dx.doi.org/10.1371/journal.ppat.1002093.
54. Sirakova TD, Dubey VS, Deb C, Daniel J, Korotkova TA, Abomoelak B, Kolattukudy PE. 2006. Identification of a diacylglycerol acyltransferase gene involved in accumulation of triacylglycerol in Mycobacterium tuberculosis under stress. Microbiology 152:2717-2725. http://dx.doi.org/10.1099/mic.0.28993-0.