Multiple M. tuberculosis phenotypes in mouse and guinea pig lung tissue revealed by a dual-staining approach

PLoS ONE

Volumn 5, Issue 6, 2010, Pages

  Ryan, Gavin J ^a   Hoff, Donald R ^a   Driver, Emily R ^a   Voskuil, Martin I ^b   Gonzalez Juarrero, Mercedes ^a   Basaraba, Randall J ^a   Crick, Dean C ^a   Spencer, John S ^a   Lenaerts, Anne J ^a  

^a Department of Environmental and Radiological Health Sciences   (United States)

^b UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AURAMINE; BACTERIAL PROTEIN; MYCOLIC ACID; POLYCLONAL ANTIBODY; RHODAMINE;

ADAPTATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL CELL WALL; BACTERIUM CULTURE; CELL LYSATE; CONTROLLED STUDY; DRUG DESIGN; FEMALE; GUINEA PIG; IMMUNOFLUORESCENCE; IN VITRO STUDY; LIPIDOMICS; LUNG PARENCHYMA; MICROENVIRONMENT; MOUSE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PHENOTYPE; PROTEOMICS; STAINING; TISSUE SECTION; TUBERCULOSIS; WHOLE CELL; ANIMAL; CLASSIFICATION; DISEASE MODEL; DNA PROBE; FLUORESCENCE IN SITU HYBRIDIZATION; FLUORESCENCE MICROSCOPY; METABOLISM; NUCLEOTIDE SEQUENCE;

BACILLI (CLASS); BACTERIA (MICROORGANISMS); CAVIA; MUS; MYCOBACTERIUM TUBERCULOSIS;

ANIMALS; BASE SEQUENCE; DISEASE MODELS, ANIMAL; DNA PROBES; FEMALE; GUINEA PIGS; IN SITU HYBRIDIZATION, FLUORESCENCE; MICE; MICROSCOPY, FLUORESCENCE; MYCOBACTERIUM TUBERCULOSIS; PHENOTYPE;

EID: 77956213734     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0011108     Document Type: Article

References (58)

1. WHO (2009) WHO report 2009; Global tuberculosis control: epidemiology, strategy, financing.
2. Zhang Y (2004) Persistent and dormant tubercle bacilli and latent tuberculosis. Front Biosci 9: 1136-1156.
3. Dhar N, McKinney JD (2007) Microbial phenotypic heterogeneity and antibiotic tolerance. Curr Opin Microbiol 10: 30-38.
4. Saunders BM, Cooper AM (2000) Restraining mycobacteria: role of granulomas in mycobacterial infections. Immunol Cell Biol 78: 334-341.
5. Smith DW, Balasubramanian V, Wiegeshaus E (1991) A guinea pig model of experimental airborne tuberculosis for evaluation of the response to chemotherapy: the effect on bacilli in the initial phase of treatment. Tubercle 72: 223-231.
6. McMurray DN (2003) Hematogenous reseeding of the lung in low-dose, aerosolinfected guinea pigs: unique features of the host-pathogen interface in secondary tubercles. Tuberculosis (Edinb) 83: 131-134.
7. Lenaerts AJ, Hoff D, Aly S, Ehlers S, Andries K, et al. (2007) Location of persisting mycobacteria in a Guinea pig model of tuberculosis revealed by r207910. Antimicrob Agents Chemother 51: 3338-3345.
8. Via LE, Lin PL, Ray SM, Carrillo J, Allen SS, et al. (2008) Tuberculous granulomas are hypoxic in guinea pigs, rabbits, and nonhuman primates. Infect Immun 76: 2333-2340.
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. Dick T (2001) Dormant tubercle bacilli: the key to more effective TB chemotherapy? J Antimicrob Chemother 47: 117-118.
11. Schnappinger D, Ehrt S, Voskuil MI, Liu Y, Mangan JA, et al. (2003) Transcriptional Adaptation of Mycobacterium tuberculosis within Macrophages: Insights into the Phagosomal Environment. J Exp Med 198: 693-704.
12. Voskuil MI (2004) Mycobacterium tuberculosis gene expression during environmental conditions associated with latency. Tuberculosis (Edinb) 84: 138-143.
13. Voskuil MI, Visconti KC, Schoolnik GK (2004) Mycobacterium tuberculosis gene expression during adaptation to stationary phase and low-oxygen dormancy. Tuberculosis (Edinb) 84: 218-227.
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.
15. Parrish NM, Dick JD, Bishai WR (1998) Mechanisms of latency in Mycobacterium tuberculosis. Trends Microbiol 6: 107-112.
16. Gomez JE, McKinney JD (2004) M. tuberculosis persistence, latency, and drug tolerance. Tuberculosis (Edinb) 84: 29-44.
17. Steingart KR, Henry M, Ng V, Hopewell PC, Ramsay A, et al. (2006) Fluorescence versus conventional sputum smear microscopy for tuberculosis: a systematic review. Lancet Infect Dis 6: 570-581.
18. Purohit MR, Mustafa T, Wiker HG, Morkve O, Sviland L (2007) Immunohistochemical diagnosis of abdominal and lymph node tuberculosis by detecting Mycobacterium tuberculosis complex specific antigen MPT64. Diagn Pathol 2: 36.
19. Seiler P, Ulrichs T, Bandermann S, Pradl L, Jorg S, et al. (2003) Cell-wall alterations as an attribute of Mycobacterium tuberculosis in latent infection. J Infect Dis 188: 1326-1331.
20. Ulrichs T, Lefmann M, Reich M, Morawietz L, Roth A, et al. (2005) Modified immunohistological staining allows detection of Ziehl-Neelsen-negative Mycobacterium tuberculosis organisms and their precise localization in human tissue. J Pathol 205: 633-640.
21. St Amand AL, Frank DN, De Groote MA, Basaraba RJ, Orme IM, et al. (2005) Use of specific rRNA oligonucleotide probes for microscopic detection of Mycobacterium tuberculosis in culture and tissue specimens. J Clin Microbiol 43: 5369-5371.
22. Fenhalls G, Stevens L, Moses L, Bezuidenhout J, Betts JC, et al. (2002) In situ detection of Mycobacterium tuberculosis transcripts in human lung granulomas reveals differential gene expression in necrotic lesions. Infect Immun 70: 6330-6338.
23. Deb C, Lee CM, Dubey VS, Daniel J, Abomoelak B, et al. (2009) A novel in vitro multiple-stress dormancy model for Mycobacterium tuberculosis generates a lipid-loaded, drug-tolerant, dormant pathogen. PLoS One 4: e6077.
24. Bhatt A, Fujiwara N, Bhatt K, Gurcha SS, Kremer L, et al. (2007) 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.
25. Yuan Y, Zhu Y, Crane DD, Barry CE, 3rd (1998) The effect of oxygenated mycolic acid composition on cell wall function and macrophage growth in Mycobacterium tuberculosis. Mol Microbiol 29: 1449-1458.
26. Cunningham AF, Spreadbury CL (1998) Mycobacterial stationary phase induced by low oxygen tension: cell wall thickening and localization of the 16- kilodalton alpha-crystallin homolog. J Bacteriol 180: 801-808.
27. Voskuil MI, Schnappinger D, Visconti KC, Harrell MI, Dolganov GM, et al. (2003) Inhibition of respiration by nitric oxide induces a Mycobacterium tuberculosis dormancy program. J Exp Med 198: 705-713.
28. Shiloh MU, Manzanillo P, Cox JS (2008) Mycobacterium tuberculosis senses host-derived carbon monoxide during macrophage infection. Cell Host Microbe 3: 323-330.
29. Sherman DR, Voskuil M, Schnappinger D, Liao R, Harrell MI, et al. (2001) Regulation of the Mycobacterium tuberculosis hypoxic response gene encoding alpha -crystallin. Proc Natl Acad Sci USA 98: 7534-7539.
30. Wayne LG, Sohaskey CD (2001) Nonreplicating persistence of mycobacterium tuberculosis. Annu Rev Microbiol 55: 139-163.
31. Richards OW (1941) The Staining of Acid-Fast Tubercle Bacteria. Science 93: 190.
32. Harada K (1976) The nature of mycobacterial acid-fastness. Stain Technol 51: 255-260.
33. Goren MB, Cernich M, Brokl O (1978) Some observations of mycobacterial acid-fastness. Am Rev Respir Dis 118: 151-154.
34. Shapiro HM, Hanscheid T (2008) Fuchsin fluorescence in Mycobacterium tuberculosis: the Ziehl-Neelsen stain in a new light. J Microbiol Methods 74: 119-120.
35. Oster G (1951) [Fluorescence of auramine O in the presence of nucleic acid.]. C R Hebd Seances Acad Sci 232: 1708-1710.
36. Kojima K, Niri M, Setoguchi K, Tsuda I, Tatsumi N (1989) An automated optoelectronic reticulocyte counter. Am J Clin Pathol 92: 57-61.
37. Hanscheid T, Ribeiro CM, Shapiro HM, Perlmutter NG (2007) Fluorescence microscopy for tuberculosis diagnosis. Lancet Infect Dis 7: 236-237.
38. Kelly BP, Furney SK, Jessen MT, Orme IM (1996) Low-dose aerosol infection model for testing drugs for efficacy against Mycobacterium tuberculosis. Antimicrob Agents Chemother 40: 2809-2812.
39. Hoff DR, Caraway ML, Brooks EJ, Driver ER, Ryan GJ, et al. (2008) Metronidazole lacks antibacterial activity in guinea pigs infected with Mycobacterium tuberculosis. Antimicrob Agents Chemother 52: 4137-4140.
40. Brandt L, Skeiky YA, Alderson MR, Lobet Y, Dalemans W, et al. (2004) The protective effect of the Mycobacterium bovis BCG vaccine is increased by coadministration with the Mycobacterium tuberculosis 72-kilodalton fusion polyprotein Mtb72F in M. tuberculosis-infected guinea pigs. Infect Immun 72: 6622-6632.
41. Lenaerts AJ, Gruppo V, Marietta KS, Johnson CM, Driscoll DK, et al. (2005) Preclinical testing of the nitroimidazopyran PA-824 for activity against Mycobacterium tuberculosis in a series of in vitro and in vivo models. Antimicrob Agents Chemother 49: 2294-2301.
42. Murugasu-Oei B, Dick T (2000) Bactericidal activity of nitrofurans against growing and dormant Mycobacterium bovis BCG. J Antimicrob Chemother 46: 917-919.
43. Kraft SL, Dailey D, Kovach M, Stasiak KL, Bennett J, et al. (2004) Magnetic resonance imaging of pulmonary lesions in guinea pigs infected with Mycobacterium tuberculosis. Infect Immun 72: 5963-5971.
44. Johnson CM, Pandey R, Sharma S, Khuller GK, Basaraba RJ, et al. (2005) Oral therapy using nanoparticle-encapsulated antituberculosis drugs in guinea pigs infected with Mycobacterium tuberculosis. Antimicrob Agents Chemother 49: 4335-4338.
45. Ludwig W, Strunk O, Westram R, Richter L, Meier H, et al. (2004) ARB: a software environment for sequence data. Nucleic Acids Res 32: 1363-1371.
46. DeLong EF, Wickham GS, Pace NR (1989) Phylogenetic stains: ribosomal RNA-based probes for the identification of single cells. Science 243: 1360-1363.
47. Wallner G, Amann R, Beisker W (1993) Optimizing fluorescent in situ hybridization with rRNA-targeted oligonucleotide probes for flow cytometric identification of microorganisms. Cytometry 14: 136-143.
48. Turner OC, Basaraba RJ, Frank AA, Orme IM (2003) Granulomatous Infections and Inflammations: Cellular and Molecular Mechanisms; Boros DL, ed. Washington, D.C.: ASM Press. pp 65-84.
49. Basaraba RJ (2008) Experimental tuberculosis: the role of comparative pathology in the discovery of improved tuberculosis treatment strategies. Tuberculosis (Edinb) 88 Suppl 1: S35-47.
50. Lenaerts AJ, Degroote MA, Orme IM (2008) Preclinical testing of new drugs for tuberculosis: current challenges. Trends Microbiol 16: 48-54.
51. Rhoades ER, Frank AA, Orme IM (1997) Progression of chronic pulmonary tuberculosis in mice aerogenically infected with virulent Mycobacterium tuberculosis. Tuber Lung Dis 78: 57-66.
52. Cooper AM, Dalton DK, Stewart TA, Griffin JP, Russell DG, et al. (1993) Disseminated tuberculosis in interferon gamma gene-disrupted mice. J Exp Med 178: 2243-2247.
53. Pearl JE, Saunders B, Ehlers S, Orme IM, Cooper AM (2001) Inflammation and lymphocyte activation during mycobacterial infection in the interferon-gammadeficient mouse. Cell Immunol 211: 43-50.
54. Flynn JL, Chan J, Triebold KJ, Dalton DK, Stewart TA, et al. (1993) An essential role for interferon gamma in resistance to Mycobacterium tuberculosis infection. J Exp Med 178: 2249-2254.
55. Kussell E, Leibler S (2005) Phenotypic diversity, population growth, and information in fluctuating environments. Science 309: 2075-2078.
56. Kussell E, Kishony R, Balaban NQ, Leibler S (2005) Bacterial persistence: a model of survival in changing environments. Genetics 169: 1807-1814.
57. Ortalo-Magne A, Dupont MA, Lemassu A, Andersen AB, Gounon P, et al. (1995) Molecular composition of the outermost capsular material of the tubercle bacillus. Microbiology 141 (Pt 7): 1609-1620.
58. Desjardin LE, Hayes LG, Sohaskey CD, Wayne LG, Eisenach KD (2001) Microaerophilic induction of the alpha-crystallin chaperone protein homologue (hspX) mRNA of Mycobacterium tuberculosis. J Bacteriol 183: 5311-5316.