A screen to identify small molecule inhibitors of protein-protein interactions in mycobacteria

Assay and Drug Development Technologies

Volumn 9, Issue 3, 2011, Pages 299-310

  Mai, Deborah ^a   Jones, Jennifer ^b   Rodgers, John W ^c   Hartman, John L ^c   Kutsch, Olaf ^b   Steyn, Adrie J C ^a  

^a University of Alabama at Birmingham   (United States)

^b University of Alabama at Birmingham   (United States)

^c UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RAPAMYCIN; TUBERCULOSTATIC AGENT;

ARTICLE; COMPLEX FORMATION; DRUG SCREENING; DRUG TARGETING; MYCOBACTERIAL PROTEIN FRAGMENT COMPLEMENTATION; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PROTEIN ANALYSIS; PROTEIN PROTEIN INTERACTION; TUBERCULOSIS;

ANTITUBERCULAR AGENTS; BACTERIAL PROTEINS; DRUG EVALUATION, PRECLINICAL; MYCOBACTERIUM TUBERCULOSIS; PROTEIN BINDING; PROTEIN INTERACTION MAPPING;

EID: 79957636068     PISSN: 1540658X     EISSN: 15578127     Source Type: Journal    
DOI: 10.1089/adt.2010.0326     Document Type: Article

References (88)

1. TB Fact Sheet: WHO; 2009. www.who.int/tb/publications/2009/tbfactsheet- 2009update-one-page.pdf
2. TB/HIV Fact Sheet: WHO; 2009. www.who.int/tb/challenges/hiv/factsheet- hivtv- 2009update.pdf
3. Franco-Paredes C, Rouphael N, del Rio C, Santos-Preciado JI: Vaccination strategies to prevent tuberculosis in the new millennium: from BCG to new vaccine candidates. Int J Infect Dis 2006;10:93-102. (Pubitemid 43255595)
4. Duncan K: Progress in TB drug development and what is still needed. Tuberculosis (Edinb) 2003;83:201-207. (Pubitemid 36683572)
5. Brewer TF: Preventing tuberculosis with Bacillus Calmette-Guerin vaccine: a meta-analysis of the literature. Clin Infect Dis 2000;31 Suppl 3:S64-S67. (Pubitemid 32269590)
6. Casenghi M, Schoen-Angerer T: Development of new drugs for TB chemotherapy: analysis of the current drug pipeline. MSF 2006:1-48.
7. Rubin EJ: Toward a new therapy for tuberculosis. N Engl J Med 2005;352: 933-934. (Pubitemid 40300305)
8. Payne DJ, Gwynn MN, Holmes DJ, Pompliano DL: Drugs for bad bugs: confronting the challenges of antibacterial discovery. Nat Rev Drug Discov 2007;6:29-40. (Pubitemid 46020284)
9. Alksne LE, Dunman PM: Target-based antimicrobial drug discovery. Methods Mol Biol 2008;431:271-283. (Pubitemid 351366066)
10. Projan SJ: New (and not so new) antibacterial targets-from where and when will the novel drugs come? Curr Opin Pharmacol 2002;2:513-522.
11. Wells JA, McClendon CL: Reaching for high-hanging fruit in drug discovery at protein-protein interfaces. Nature 2007;450:1001-1009. (Pubitemid 350273630)
12. Bogan AA, Thorn KS: Anatomy of hot spots in protein interfaces. J Mol Biol 1998;280:1-9. (Pubitemid 28312802)
13. Jones S, Thornton JM: Principles of protein-protein interactions. Proc Natl Acad Sci U S A 1996;93:13-20. (Pubitemid 26038096)
14. Clackson T, Wells JA: A hot spot of binding energy in a hormone-receptor interface. Science 1995;267:383-386.
15. Lo Conte L, Chothia C, Janin J: The atomic structure of protein-protein recognition sites. J Mol Biol 1999;285:2177-2198. (Pubitemid 29078179)
16. Ma B, Elkayam T, Wolfson H, Nussinov R: Protein-protein interactions: structurally conserved residues distinguish between binding sites and exposed protein surfaces. Proc Natl Acad Sci U S A 2003;100:5772-5777. (Pubitemid 36576883)
17. Ma B, Nussinov R: Trp/Met/Phe hot spots in protein-protein interactions: potential targets in drug design. Curr Top Med Chem 2007;7:999-1005. (Pubitemid 47040527)
18. Keskin O, Ma B, Nussinov R: Hot regions in protein-protein interactions: the organization and contribution of structurally conserved hot spot residues. J Mol Biol 2005;345:1281-1294. (Pubitemid 40092239)
19. Arkin MR, Wells JA: Small-molecule inhibitors of protein-protein interactions: progressing towards the dream. Nat Rev Drug Discov 2004;3:301-317. (Pubitemid 38499758)
20. Loregian A, Palu G: Disruption of protein-protein interactions: towards new targets for chemotherapy. J Cell Physiol 2005;204:750-762. (Pubitemid 41099260)
21. Andre E, Bastide L, Villain-Guillot P, Latouche J, Rouby J, Leonetti JP: A multiwell assay to isolate compounds inhibiting the assembly of the prokaryotic RNA polymerase. Assay Drug Dev Technol 2004;2:629-635. (Pubitemid 40309422)
22. Andre E, Bastide L, Michaux-Charachon S, Gouby A, Villain-Guillot P, Latouche J, Bouchet A, Gualtieri M, Leonetti JP: Novel synthetic molecules targeting the bacterial RNA polymerase assembly. J Antimicrob Chemother 2006;57:245-251. (Pubitemid 43160165)
23. Tsao DH, Sutherland AG, Jennings LD, Li Y, Rush TS, 3rd, Alvarez JC, Ding W, Dushin EG, Dushin RG, Haney SA: Discovery of novel inhibitors of the ZipA/FtsZ complex by NMR fragment screening coupled with structure-based design. Bioorg Med Chem 2006;14:7953-7961. (Pubitemid 44584704)
24. Hung DT, Shakhnovich EA, Pierson E, Mekalanos JJ: Small-molecule inhibitor of Vibrio cholerae virulence and intestinal colonization. Science 2005;310: 670-674. (Pubitemid 41528158)
25. Shakhnovich EA, Hung DT, Pierson E, Lee K, Mekalanos JJ: Virstatin inhibits dimerization of the transcriptional activator ToxT. Proc Natl Acad Sci U S A 2007;104:2372-2377. (Pubitemid 46391404)
26. Michnick SW: Exploring protein interactions by interaction-induced folding of proteins from complementary peptide fragments. Curr Opin Struct Biol 2001; 11:472-477. (Pubitemid 32728500)
27. Michnick SW, Ear PH, Manderson EN, Remy I, Stefan E: Universal strategies in research and drug discovery based on protein-fragment complementation assays. Nat Rev Drug Discov 2007;6:569-582. (Pubitemid 47019445)
28. Remy I, Ghaddar G, Michnick SW: Using the beta-lactamase protein-fragment complementation assay to probe dynamic protein-protein interactions. Nat Protoc 2007;2:2302-2306. (Pubitemid 351565868)
29. Pelletier JN, Campbell-Valois FX, Michnick SW: Oligomerization domain-directed reassembly of active dihydrofolate reductase from rationally designed fragments. Proc Natl Acad Sci U S A 1998;95:12141-12146. (Pubitemid 28483732)
30. Singh A, Mai D, Kumar A, Steyn AJ: Dissecting virulence pathways of Mycobacterium tuberculosis through protein-protein association. Proc Natl Acad Sci U S A 2006;103:11346-11351. (Pubitemid 44156520)
31. Pearce MJ, Mintseris J, Ferreyra J, Gygi SP, Darwin KH: Ubiquitin-like protein involved in the proteasome pathway of Mycobacterium tuberculosis. Science 2008;322:1104-1107.
32. Jacobs WRJ: Mycobacterium tuberculosis: a once genetically intractable organism. In: Molecular Genetics of Mycobacteria. Hatfull GF, Jacobs WRJ (eds.), pp. 1-18. ASM Press, Washington, DC, 2000.
33. Lee JM, Cho HY, Cho HJ, Ko IJ, Park SW, Baik HS, Oh JH, Eom CY, Kim YM, Kang BS: O2- and NO-sensing mechanism through the DevSR two-component system in Mycobacterium smegmatis. J Bacteriol 2008;190:6795-6804.
34. Garbe T, Harris D, Vordermeier M, Lathigra R, Ivanyi J, Young D: Expression of the Mycobacterium tuberculosis 19-kilodalton antigen in Mycobacterium smegmatis: immunological analysis and evidence of glycosylation. Infect Immun 1993;61:260-267. (Pubitemid 23015425)
35. Bagchi G, Mayuri, Tyagi JS: Hypoxia-responsive expression of Mycobacterium tuberculosis Rv3134c and devR promoters in Mycobacterium smegmatis. Microbiology 2003;149:2303-2305. (Pubitemid 37160707)
36. Harth G, Lee BY, Horwitz MA: High-level heterologous expression and secretion in rapidly growing nonpathogenic mycobacteria of four major Mycobacterium tuberculosis extracellular proteins considered to be leading vaccine candidates and drug targets. Infect Immun 1997;65:2321-2328. (Pubitemid 27237316)
37. Chaturvedi V, Dwivedi N, Tripathi RP, Sinha S: Evaluation of Mycobacterium smegmatis as a possible surrogate screen for selecting molecules active against multi-drug resistant Mycobacterium tuberculosis. J Gen Appl Microbiol 2007; 53:333-337. (Pubitemid 351266157)
38. Taneja NK, Tyagi JS: Resazurin reduction assays for screening of anti-tubercular compounds against dormant and actively growing Mycobacterium tuberculosis, Mycobacterium bovis BCG and Mycobacterium smegmatis. J Antimicrob Chemother 2007;60:288-293. (Pubitemid 47243876)
39. Zhang Y: The magic bullets and tuberculosis drug targets. Annu Rev Pharmacol Toxicol 2005;45:529-564. (Pubitemid 40261816)
40. Wayne LG, Hayes LG: An in vitro model for sequential study of shiftdown of Mycobacterium tuberculosis through two stages of nonreplicating persistence. Infect Immun 1996;64:2062-2069. (Pubitemid 26165667)
41. Park HD, Guinn KM, Harrell MI, Liao R, Voskuil MI, Tompa M, Schoolnik GK, Sherman DR: Rv3133c/dosR is a transcription factor that mediates the hypoxic response of Mycobacterium tuberculosis. Mol Microbiol 2003;48: 833-843. (Pubitemid 36819066)
42. Dasgupta N, Kapur V, Singh KK, Das TK, Sachdeva S, Jyothisri K, Tyagi JS: Characterization of a two-component system, devR-devS, of Mycobacterium tuberculosis. Tuber Lung Dis 2000;80:141-159.
43. Roberts DM, Liao RP, Wisedchaisri G, Hol WG, Sherman DR: Two sensor kinases contribute to the hypoxic response of Mycobacterium tuberculosis. J Biol Chem 2004;279:23082-23087. (Pubitemid 38685612)
44. Sousa EH, Tuckerman JR, Gonzalez G, Gilles-Gonzalez MA: DosT and DevS are oxygen-switched kinases in Mycobacterium tuberculosis. Protein Sci 2007;16: 1708-1719. (Pubitemid 47195697)
45. Kumar A, Toledo JC, Patel RP, Lancaster JR, Jr., Steyn AJ: Mycobacterium tuberculosis DosS is a redox sensor and DosT is a hypoxia sensor. Proc Natl Acad Sci U S A 2007;104:11568-11573. (Pubitemid 47175053)
46. Kumar A, Deshane JS, Crossman DK, Bolisetty S, Yan BS, Kramnik I, Agarwal A, Steyn AJ: Heme oxygenase-1-derived carbon monoxide induces the Mycobacterium tuberculosis dormancy regulon. J Biol Chem 2008;283:18032-18039.
47. Honer zu Bentrup K, Russell DG: Mycobacterial persistence: adaptation to a changing environment. Trends Microbiol 2001, 9:597-605 (Pubitemid 33135416)
48. Malhotra V, Sharma D, Ramanathan VD, Shakila H, Saini DK, Chakravorty S, Das TK, Li Q, Silver RF, Narayanan PR: Disruption of response regulator gene, devR, leads to attenuation in virulence of Mycobacterium tuberculosis. FEMS Microbiol Lett 2004;231:237-245. (Pubitemid 38251605)
49. Zhang JH, Chung TD, Oldenburg KR: A simple statistical parameter for use in evaluation and validation of high throughput screening assays. J Biomol Screen 1999;4:67-73. (Pubitemid 29278954)
50. Hu CD, Chinenov Y, Kerppola TK: Visualization of interactions among bZIP and Rel family proteins in living cells using bimolecular fluorescence complementation. Mol Cell 2002;9:789-798. (Pubitemid 34454889)
51. Magliery TJ, Wilson CG, Pan W, Mishler D, Ghosh I, Hamilton AD, Regan L: Detecting protein-protein interactions with a green fluorescent protein fragment reassembly trap: scope and mechanism. J Am Chem Soc 2005;127: 146-157. (Pubitemid 40094379)
52. Chen J, Zheng XF, Brown EJ, Schreiber SL: Identification of an 11-kDa FKBP12- rapamycin-binding domain within the 289-kDa FKBP12-rapamycin-associated protein and characterization of a critical serine residue. Proc Natl Acad Sci U S A 1995;92:4947-4951.
53. Liang J, Choi J, Clardy J: Refined structure of the FKBP12-rapamycin-FRB ternary complex at 2.2 A resolution. Acta Crystallogr D Biol Crystallogr 1999; 55:736-744. (Pubitemid 29194519)
54. Van Duyne GD, Standaert RF, Karplus PA, Schreiber SL, Clardy J: Atomic structure of FKBP-FK506, an immunophilin-immunosuppressant complex. Science 1991;252:839-842. (Pubitemid 121000524)
55. Choi J, Chen J, Schreiber SL, Clardy J: Structure of the FKBP12-rapamycin complex interacting with the binding domain of human FRAP. Science 1996;273:239-242. (Pubitemid 26285890)
56. Remy I, Michnick SW: A highly sensitive protein-protein interaction assay based on Gaussia luciferase. Nat Methods 2006;3:977-979. (Pubitemid 44782695)
57. Rodriguez GM, Voskuil MI, Gold B, Schoolnik GK, Smith I: ideR, An essential gene in Mycobacterium tuberculosis: role of IdeR in iron-dependent gene expression, iron metabolism, and oxidative stress response. Infect Immun 2002;70:3371-3381. (Pubitemid 34665972)
58. Bange FC, Brown AM, Jacobs WR, Jr.: Leucine auxotrophy restricts growth of Mycobacterium bovis BCG in macrophages. Infect Immun 1996;64:1794-1799. (Pubitemid 26129841)
59. McAdam RA, Weisbrod TR, Martin J, Scuderi JD, Brown AM, Cirillo JD, Bloom BR, Jacobs WR, Jr.: In vivo growth characteristics of leucine and methionine auxotrophic mutants of Mycobacterium bovis BCG generated by transposon mutagenesis. Infect Immun 1995;63:1004-1012.
60. DiGiuseppe Champion PA, Cox JS: Protein secretion systems in Mycobacteria. Cell Microbiol 2007;9:1376-1384. (Pubitemid 46774011)
61. Callahan B, Nguyen K, Collins A, Valdes K, Caplow M, Crossman DK, Steyn AJ, Eisele L, Derbyshire KM: Conservation of structure and protein-protein interactions mediated by the secreted mycobacterial proteins EsxA, EsxB, and EspA. J Bacteriol 2009;192:326-335.
62. Inglese J, Auld DS, Jadhav A, Johnson RL, Simeonov A, Yasgar A, Zheng W, Austin CP: Quantitative high-throughput screening: a titration-based approach that efficiently identifies biological activities in large chemical libraries. Proc Natl Acad Sci U S A 2006;103:11473-11478. (Pubitemid 44182476)
63. Danilchanka O, Pavlenok M, Niederweis M: Role of porins for uptake of antibiotics by Mycobacterium smegmatis. Antimicrob Agents Chemother 2008; 52:3127-3134.
64. Nguyen L, Thompson CJ: Foundations of antibiotic resistance in bacterial physiology: the mycobacterial paradigm. Trends Microbiol 2006;14:304-312. (Pubitemid 43963364)
65. Brennan PJ, Nikaido H: The envelope of mycobacteria. Annu Rev Biochem 1995;64:29-63.
66. Joshi PB, Hirst M, Malcolm T, Parent J, Mitchell D, Lund K, Sadowski I: Identification of protein interaction antagonists using the repressed transactivator two-hybrid system. Biotechniques 2007;42:635-644. (Pubitemid 46932738)
67. Hondalus MK, Bardarov S, Russell R, Chan J, Jacobs WR, Jr., Bloom BR: Attenuation of and protection induced by a leucine auxotroph of Mycobacterium tuberculosis. Infect Immun 2000;68:2888-2898. (Pubitemid 30253869)
68. Dussurget O, Rodriguez M, Smith I: An ideR mutant of Mycobacterium smegmatis has derepressed siderophore production and an altered oxidativestress response. Mol Microbiol 1996;22:535-544. (Pubitemid 26373837)
69. Wisedchaisri G, Wu M, Sherman DR, Hol WG: Crystal structures of the response regulator DosR from Mycobacterium tuberculosis suggest a helix rearrangement mechanism for phosphorylation activation. J Mol Biol 2008;378: 227-242.
70. Gao R, Mack TR, Stock AM: Bacterial response regulators: versatile regulatory strategies from common domains. Trends Biochem Sci 2007;32:225-234. (Pubitemid 46711171)
71. Gao R, Stock AM: Biological insights from structures of two-component proteins. Annu Rev Microbiol 2009;63:133-154.
72. Maris AE, Sawaya MR, Kaczor-Grzeskowiak M, Jarvis MR, Bearson SM, Kopka ML, Schroder I, Gunsalus RP, Dickerson RE: Dimerization allows DNA target site recognition by the NarL response regulator. Nat Struct Biol 2002;9: 771-778.
73. Gupta RK, Thakur TS, Desiraju GR, Tyagi JS: Structure-based design of DevR inhibitor active against nonreplicating Mycobacterium tuberculosis. J Med Chem 2009;52:6324-6334.
74. Vilcheze C, Jacobs WR, Jr.: The mechanism of isoniazid killing: clarity through the scope of genetics. Annu Rev Microbiol 2007;61:35-50. (Pubitemid 350058198)
75. Beggs WH: Influence of growth phase on the susceptibility of Candida albicans to butoconazole, oxiconazole, and sulconazole. J Antimicrob Chemother 1985; 16:397.
76. Maddry JA, Ananthan S, Goldman RC, Hobrath JV, Kwong CD, Maddox C, Rasmussen L, Reynolds RC, Secrist JA, 3rd, Sosa MI: Antituberculosis activity of the molecular libraries screening center network library. Tuberculosis (Edinb) 2009;89:354-363.
77. Ananthan S, Faaleolea ER, Goldman RC, Hobrath JV, Kwong CD, Laughon BE, Maddry JA, Mehta A, Rasmussen L, Reynolds RC: High-throughput screening for inhibitors of Mycobacterium tuberculosis H37Rv. Tuberculosis (Edinb) 2009; 89:334-353.
78. Kalkut G: Sulfonamides and trimethoprim. Cancer Invest 1998;16:612-615. (Pubitemid 28541782)
79. Weidner Wells MA, Macielag MJ: Antibacterial Agents, Sulfonamides. Wiley Online Library, 2003. onlinelibrary.wiley.com/doi/10.1002/0471238961 .1921120606152505.a01.pub2/full
80. Bush K, Freudenberger JS, Slusarchyk DS, Sykes RB, Meyers E: Activity of sulfa drugs and dihydrofolate reductase inhibitors against Candida albicans. Cell Mol Life Sci 1982;38:436-437. (Pubitemid 12116609)
81. Suling WJ, Seitz LE, Reynolds RC, Barrow WW: New Mycobacterium avium antifolate shows synergistic effect when used in combination with dihydropteroate synthase inhibitors. Antimicrob Agents Chemother 2005;49:4801-4803. (Pubitemid 41552625)
82. Smith CL, Powell KR: Review of the sulfonamides and trimethoprim. Pediatr Rev 2000;21:368.
83. Porras MC, Lecumberri JN, Castrillon JL: Trimethoprim/sulfamethoxazole and metabolic acidosis in HIV-infected patients. Ann Pharmacother 1998;32:185-189. (Pubitemid 28082329)
84. Wallace RJ, Jr., Wiss K, Bushby MB, Hollowell DC: In vitro activity of trimethoprim and sulfamethoxazole against the nontuberculous mycobacteria. Rev Infect Dis 1982;4:326-331.
85. Wormser GP, Keusch GT, Heel RC: Co-trimoxazole (trimethoprim- sulfamethoxazole). Drugs 1982;24:459-518.
86. Suling WJ, Reynolds RC, Barrow EW, Wilson LN, Piper JR, Barrow WW: Susceptibilities of Mycobacterium tuberculosis and Mycobacterium avium complex to lipophilic deazapteridine derivatives, inhibitors of dihydrofolate reductase. J Antimicrob Chemother 1998;42:811-815. (Pubitemid 29008085)
87. Suling WJ, Seitz LE, Pathak V, Westbrook L, Barrow EW, Zywno-Van-Ginkel S, Reynolds RC, Piper JR, Barrow WW: Antimycobacterial activities of 2,4-diamino-5-deazapteridine derivatives and effects on mycobacterial dihydrofolate reductase. Antimicrob Agents Chemother 2000;44:2784-2793.
88. McGovern SL, Caselli E, Grigorieff N, Shoichet BK: A common mechanism underlying promiscuous inhibitors from virtual and high-throughput screening. J Med Chem 2002;45:1712-1722. (Pubitemid 34293537)