Transcriptional responses of Mycobacterium tuberculosis to lung surfactant

Microbial Pathogenesis

Volumn 46, Issue 4, 2009, Pages 185-193

  Schwab, Ute ^a   Rohde, Kyle H ^a   Wang, Zhengdong ^b   Chess, Patricia R ^b   Notter, Robert H ^b   Russell, David G ^a  

^a Animal Health Diagnostic Center   (United States)

^b UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

Author keywords

Microarray; Mycobacterium tuberculosis; Surfactant; Surfactant proteins; Transcriptional responses

Indexed keywords

APOPROTEIN; LUNG SURFACTANT; LUNG SURFACTANT EXTRACT; PENICILLOYL POLYLYSINE; SURFACTANT PROTEIN A; SURFACTANT PROTEIN B; SURFACTANT PROTEIN C; SURFACTANT PROTEIN D; TRIACYLGLYCEROL LIPASE;

ARTICLE; CONTROLLED STUDY; DOWN REGULATION; GENE EXPRESSION; GENETIC TRANSCRIPTION; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; UPREGULATION;

ANIMALS; CATTLE; GENE EXPRESSION PROFILING; HUMANS; MYCOBACTERIUM TUBERCULOSIS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PULMONARY SURFACTANTS; STRESS, PHYSIOLOGICAL;

BOVINAE; MYCOBACTERIUM TUBERCULOSIS;

EID: 62749162214     PISSN: 08824010     EISSN: 10961208     Source Type: Journal    
DOI: 10.1016/j.micpath.2008.12.006     Document Type: Article

References (68)

1. World Health Organization (WHO). Global tuberculosis: control, surveillance, planning, financing. WHO report 2006 (Document WHO/HTM/TB/2006.362). Geneva, Switzerland; 2006. p. 1-242.
2. Russell D.G. Mycobacterium tuberculosis: here today, and here tomorrow. Nat Rev Mol Cell Biol 2 (2001) 569-577
3. Creuwels L.A., van Golde L.M., and Haagsman H.P. The pulmonary surfactant system: biochemical and clinical aspects. Lung 175 (1997) 1-39
4. Notter R.H. Lung surfactants: basic science and clinical applications (2000), Marcel Dekker, Inc., New York
5. Notter R.H., and Wang Z. Pulmonary surfactant: physical chemistry, physiology and replacement. Rev Chem Eng 13 (1997) 1-118
6. Gaynor C.D., McCormack F.X., Voelker D.R., McGowan S.E., and Schlesinger L.S. Pulmonary surfactant protein A mediates enhanced phagocytosis of Mycobacterium tuberculosis by a direct interaction with human macrophages. J Immunol 155 (1995) 5343-5351
7. Ferguson J.S., Martin J.L., Azad A.K., McCarthy T.R., Kang P.B., Voelker D.R., et al. Surfactant protein D increases fusion of Mycobacterium tuberculosis-containing phagosomes with lysosomes in human macrophages. Infect Immun 74 (2006) 7005-7009
8. Ferguson J.S., Voelker D.R., McCormack F.X., and Schlesinger L.S. Surfactant protein D binds to Mycobacterium tuberculosis bacilli and lipoarabinomannan via carbohydrate-lectin interactions resulting in reduced phagocytosis of the bacteria by macrophages. J Immunol 163 (1999) 312-321
9. Ferguson J.S., Voelker D.R., Ufnar J.A., Dawson A.J., and Schlesinger L.S. Surfactant protein D inhibition of human macrophage uptake of Mycobacterium tuberculosis is independent of bacterial agglutination. J Immunol 168 (2002) 1309-1314
10. McCormack F.X. New concepts in collectin-mediated host defense at the air-liquid interface of the lung. Respirology Suppl. 11 (2006) S7-10
11. McCormack F.X., and Whitsett J.A. The pulmonary collectins, SP-A and SP-D, orchestrate innate immunity in the lung. J Clin Invest 109 (2002) 707-712
12. Wright J.R. Immunomodulatory functions of surfactant. Physiol Rev 77 (1997) 931-962
13. Crouch E., and Wright J.R. Surfactant proteins A and D and pulmonary host defense. Annu Rev Physiol 63 (2001) 521-554
14. Chimote G., and Banerjee R. Lung surfactant dysfunction in tuberculosis: effect of mycobacterial tubercular lipids on dipalmitoylphosphatidylcholine surface activity. Colloids Surf B Biointerfaces 45 (2005) 215-223
15. Wang Z., Schwab U., Rhoades E., Chess P.R., Russell D.G., and Notter R.H. Peripheral cell wall lipids of Mycobacterium tuberculosis are inhibitory to surfactant function. Tuberculosis (Edinb) 88 (2008) 178-186
16. Rohde K.H., Abramovitch R.B., and Russell D.G. Mycobacterium tuberculosis invasion of macrophages: linking bacterial gene expression to environmental cues. Cell Host Microbe 2 (2007) 352-364
17. Manganelli R., Voskuil M.I., Schoolnik G.K., and Smith I. The Mycobacterium tuberculosis ECF sigma factor sigmaE: role in global gene expression and survival in macrophages. Mol Microbiol 41 (2001) 423-437
18. Sherman D.R., Voskuil M., Schnappinger D., Liao R., Harrell M.I., and Schoolnik G.K. Regulation of the Mycobacterium tuberculosis hypoxic response gene encoding alpha-crystallin. Proc Natl Acad Sci U S A 98 (2001) 7534-7539
19. Waddell S.J., and Butcher P.D. Microarray analysis of whole genome expression of intracellular Mycobacterium tuberculosis. Curr Mol Med 7 (2007) 287-296
20. Butcher P.D., Mangan J.A., and Monahan I.M. Intracellular gene expression. Analysis of RNA from mycobacteria in macrophages using RT-PCR. Methods Mol Biol 101 (1998) 285-306
21. Fisher M.A., Plikaytis B.B., and Shinnick T.M. Microarray analysis of the Mycobacterium tuberculosis transcriptional response to the acidic conditions found in phagosomes. J Bacteriol 184 (2002) 4025-4032
22. Deb C., Daniel J., Sirakova T.D., Abomoelak B., Dubey V.S., and Kolattukudy P.E. A novel lipase belonging to the hormone-sensitive lipase family induced under starvation to utilize stored triacylglycerol in Mycobacterium tuberculosis. J Biol Chem 281 (2006) 3866-3875
23. Cascioferro A., Delogu G., Colone M., Sali M., Stringaro A., Arancia G., et al. PE is a functional domain responsible for protein translocation and localization on mycobacterial cell wall. Mol Microbiol 66 (2007) 1536-1547
24. Perez E., Constant P., Laval F., Lemassu A., Laneelle M.A., Daffe M., et al. Molecular dissection of the role of two methyltransferases in the biosynthesis of phenolglycolipids and phthiocerol dimycoserosate in the Mycobacterium tuberculosis complex. J Biol Chem 279 (2004) 42584-42592
25. Rao A., and Ranganathan A. Interaction studies on proteins encoded by the phthiocerol dimycocerosate locus of Mycobacterium tuberculosis. Mol Genet Genomics 272 (2004) 571-579
26. Kana B.D., Gordhan B.G., Downing K.J., Sung N., Vostroktunova G., Machowski E.E., et al. The resuscitation-promoting factors of Mycobacterium tuberculosis are required for virulence and resuscitation from dormancy but are collectively dispensable for growth in vitro. Mol Microbiol 67 (2008) 672-684
27. MacGurn J.A., Raghavan S., Stanley S.A., and Cox J.S. A non-RD1 gene cluster is required for Snm secretion in Mycobacterium tuberculosis. Mol Microbiol 57 (2005) 1653-1663
28. Notter R.H., and Finkelstein J.N. Pulmonary surfactant: an interdisciplinary approach. J Appl Physiol 57 (1984) 1613-1624
29. Onwueme K.C., Vos C.J., Zurita J., Ferreras J.A., and Quadri L.E. The dimycocerosate ester polyketide virulence factors of mycobacteria. Prog Lipid Res 44 (2005) 259-302
30. Cole S.T., Brosch R., Parkhill J., Garnier T., Churcher C., Harris D., et al. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393 (1998) 537-544
31. Russell D.G. Phagosomes, fatty acids and tuberculosis. Nat Cell Biol 5 (2003) 776-778
32. Grabner R., and Meerbach W. Phagocytosis of surfactant by alveolar macrophages in vitro. Am J Physiol 261 (1991) L472-L477
33. Wright J.R., and Youmans D.C. Degradation of surfactant lipids and surfactant protein A by alveolar macrophages in vitro. Am J Physiol 268 (1995) L772-L780
34. Poelma D.L., Zimmermann L.J., Scholten H.H., Lachmann B., and van Iwaarden J.F. In vivo and in vitro uptake of surfactant lipids by alveolar type II cells and macrophages. Am J Physiol Lung Cell Mol Physiol 283 (2002) L648-L654
35. Bouhafs R.K., and Jarstrand C. Lipid peroxidation of lung surfactant by bacteria. Lung 177 (1999) 101-110
36. Beatty A.L., Malloy J.L., and Wright J.R. Pseudomonas aeruginosa degrades pulmonary surfactant and increases conversion in vitro. Am J Respir Cell Mol Biol 32 (2005) 128-134
37. Crystal R.J. Alveolar macrophages (1991), Raven Press, New York, NY
38. Cox J.S., Chen B., McNeil M., and Jacobs Jr. W.R. Complex lipid determines tissue-specific replication of Mycobacterium tuberculosis in mice. Nature 402 (1999) 79-83
39. Camacho L.R., Constant P., Raynaud C., Laneelle M.A., Triccas J.A., Gicquel B., et al. Analysis of the phthiocerol dimycocerosate locus of Mycobacterium tuberculosis. Evidence that this lipid is involved in the cell wall permeability barrier. J Biol Chem 276 (2001) 19845-19854
40. Rousseau C., Winter N., Pivert E., Bordat Y., Neyrolles O., Ave P., et al. Production of phthiocerol dimycocerosates protects Mycobacterium tuberculosis from the cidal activity of reactive nitrogen intermediates produced by macrophages and modulates the early immune response to infection. Cell Microbiol 6 (2004) 277-287
41. Soliveri J.A., Gomez J., Bishai W.R., and Chater K.F. Multiple paralogous genes related to the Streptomyces coelicolor developmental regulatory gene whiB are present in Streptomyces and other actinomycetes. Microbiology 146 (2000) 333-343
42. Geiman D.E., Raghunand T.R., Agarwal N., and Bishai W.R. Differential gene expression in response to exposure to antimycobacterial agents and other stress conditions among seven Mycobacterium tuberculosis whiB-like genes. Antimicrob Agents Chemother 50 (2006) 2836-2841
43. Morris R.P., Nguyen L., Gatfield J., Visconti K., Nguyen K., Schnappinger D., et al. Ancestral antibiotic resistance in Mycobacterium tuberculosis. Proc Natl Acad Sci U S A 102 (2005) 12200-12205
44. Mason R.J., Greene K., and Voelker D.R. Surfactant protein A and surfactant protein D in health and disease. Am J Physiol 275 (1998) L1-L13
45. Kuroki Y., and Voelker D.R. Pulmonary surfactant proteins. J Biol Chem 269 (1994) 25943-25946
46. Williams M.C., Hawgood S., and Hamilton R.L. Changes in lipid structure produced by surfactant proteins SP-A, SP-B, and SP-C. Am J Respir Cell Mol Biol 5 (1991) 41-50
47. Persson A., Chang D., Rust K., Moxley M., Longmore W., and Crouch E. Purification and biochemical characterization of CP4 (SP-D), a collagenous surfactant-associated protein. Biochemistry 28 (1989) 6361-6367
48. Sidobre S., Nigou J., Puzo G., and Riviere M. Lipoglycans are putative ligands for the human pulmonary surfactant protein A attachment to mycobacteria. Critical role of the lipids for lectin-carbohydrate recognition. J Biol Chem 275 (2000) 2415-2422
49. Beharka A.A., Gaynor C.D., Kang B.K., Voelker D.R., McCormack F.X., and Schlesinger L.S. Pulmonary surfactant protein A up-regulates activity of the mannose receptor, a pattern recognition receptor expressed on human macrophages. J Immunol 169 (2002) 3565-3573
50. Ragas A., Roussel L., Puzo G., and Riviere M. The Mycobacterium tuberculosis cell-surface glycoprotein apa as a potential adhesin to colonize target cells via the innate immune system pulmonary C-type lectin surfactant protein A. J Biol Chem 282 (2007) 5133-5142
51. Henning L.N., Azad A.K., Parsa K.V., Crowther J.E., Tridandapani S., and Schlesinger L.S. Pulmonary surfactant protein A regulates TLR expression and activity in human aacrophages. J Immunol 180 (2008) 7847-7858
52. Pasula R., Wright J.R., Kachel D.L., and Martin II W.J. Surfactant protein A suppresses reactive nitrogen intermediates by alveolar macrophages in response to Mycobacterium tuberculosis. J Clin Invest 103 (1999) 483-490
53. Wu H., Kuzmenko A., Wan S., Schaffer L., Weiss A., Fisher J.H., et al. Surfactant proteins A and D inhibit the growth of Gram-negative bacteria by increasing membrane permeability. J Clin Invest 111 (2003) 1589-1602
54. Childs R.A., Wright J.R., Ross G.F., Yuen C.T., Lawson A.M., Chai W., et al. Specificity of lung surfactant protein SP-A for both the carbohydrate and the lipid moieties of certain neutral glycolipids. J Biol Chem 267 (1992) 9972-9979
55. Gao E., Wang Y., McCormick S.M., Li J., Seidner S.R., and Mendelson C.R. Characterization of two baboon surfactant protein A genes. Am J Physiol 271 (1996) L617-L630
56. Johansson J., and Curstedt T. Molecular structures and interactions of pulmonary surfactant components. Eur J Biochem 244 (1997) 675-693
57. McCormack F.X. The structure and function of surfactant protein-A. Chest 111 (1997) 114S-119S
58. Voss T., Melchers K., Scheirle G., and Schafer K.P. Structural comparison of recombinant pulmonary surfactant protein SP-A derived from two human coding sequences: implications for the chain composition of natural human SP-A. Am J Respir Cell Mol Biol 4 (1991) 88-94
59. Hall S.B., Wang Z., and Notter R.H. Separation of subfractions of the hydrophobic components of calf lung surfactant. J Lipid Res 35 (1994) 1386-1394
60. Notter R.H., Wang Z., Egan E.A., and Holm B.A. Component-specific surface and physiological activity in bovine-derived lung surfactants. Chem Phys Lipids 114 (2002) 21-34
61. Bligh E.G., and Dyer W.J. A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37 (1959) 911-917
62. Willson D.F., Thomas N.J., Markovitz B.P., DiCarlo J.V., Pon S., Jacobs B.R., et al. Effect of exogenous surfactant (calfactant) in pediatric acute lung injury: a randomized controlled trial. JAMA 293 (2005) 470-476
63. Hudak M.L., Farrell E.E., Rosenberg A.A., Jung A.L., Auten R.L., Durand D.J., et al. A multicenter randomized masked comparison of natural vs synthetic surfactant for the treatment of respiratory distress syndrome. J Pediatr 128 (1996) 396-406
64. Hudak M.L., Martin D.J., Egan E.A., Matteson E.J., Cummings J., Jung A.L., et al. A multicenter randomized masked comparison trial of synthetic surfactant versus calf lung surfactant extract in the prevention of neonatal respiratory distress syndrome. Pediatrics 100 (1997) 39-50
65. Lowry O.H., Rosebrough N.J., Farr A.L., and Randall R.J. Protein measurement with the Folin phenol reagent. J Biol Chem 193 (1951) 265-275
66. Kaplin R.S., and Pedersen P.L. Sensitive protein assay in the presence of high levels of lipid. Anal Biochem 150 (1989) 97-104
67. Wright J.R., Wager R.E., Hawgood S., Dobbs L., and Clements J.A. Surfactant apoprotein Mr = 26,000-36,000 enhances uptake of liposomes by type II cells. J Biol Chem 262 (1987) 2888-2894
68. Schmittgen T.D. Real-time quantitative PCR. Methods 25 (2001) 383-385