Mycobacterium tuberculosis proteases and implications for new antibiotics against tuberculosis

Critical Reviews in Eukaryotic Gene Expression

Volumn 21, Issue 4, 2011, Pages 347-361

  Zhao, Quan Ju ^a   Xie, Jian Ping ^a  

^a SOUTHWEST UNIVERSITY   (China)

Author keywords

Drug target; Molecular mechanisms; Protease; Virulence factor

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ANTIBIOTIC AGENT; BACTERIAL PROTEIN; ES 31 PROTEIN; ESX 1 PROTEIN; FTSH PROTEIN; GLYCOPROTEIN; METALLOPROTEINASE; MYC PROTEIN; MYCP1 PROTEIN; PEPD PROTEIN; PROTEASOME; RV 0198C; RV 2869C; RV 3671C; SERINE PROTEINASE; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

ARTICLE; BACTERIAL VIRULENCE; DRUG TARGETING; GENE EXPRESSION REGULATION; GENETIC ANALYSIS; HOMEOSTASIS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN SECRETION; SIGNAL TRANSDUCTION; STRESS; TUBERCULOSIS;

EID: 83655211590     PISSN: 10454403     EISSN: None     Source Type: Journal    
DOI: 10.1615/CritRevEukarGeneExpr.v21.i4.50     Document Type: Article

References (76)

1. Sachdeva P, Misra R, Tyagi AK, Singh Y. The sigma factors of Mycobacterium tuberculosis: regulation of the regulators. FEBS J. 2010;277(3):605-26.
2. Butler SM, Festa RA, Pearce MJ, Darwin KH. Self-compartmentalized bacterial proteases and pathogenesis. Mol Microbiol. 2006;60(3):553-62.
3. Kristjansson MM, Asgeirsson B, Bjarnason JB. Serine proteinases from cold-adapted organisms. Adv Exp Med Biol. 1997;415:27-46.
4. Armstrong PB. Proteases and protease inhibitors: a balance of activities in host-pathogen interaction. Immunobiology. 2006;211(4):263-81.
5. Hu Q, Liu P, Yu Z, Zhao G, Li J, Teng L, Zhou M, Bei W, Chen H, Jin M. Identification of a cell wall-associated subtilisin-like serine protease involved in the pathogenesis of Streptococcus suis serotype 2. Microb Pathog. 2010;48(3-4):103-9.
6. Fernaays MM, Lesse AJ, Cai X, Murphy TF. Characterization of igaB, a second immunoglobulin A1 protease gene in nontypeable Haemophilus influenzae. Infect Immun. 2006;74(10):5860-70.
7. Elkind E, Rechnitzer H, Vaisid T, Kornspan JD, Barnoy S, Rottem S, Kosower NS. Mycoplasma hyorhinis upregulates calpastatin and inhibits calpain-dependent proteolysis in SH-SY5Y neuroblastoma cells. FEMS Microbiol Lett. 2010;304(1):62-8.
8. Iwase T, Uehara Y, Shinji H, Tajima A, Seo H, Takada K, Agata T, Mizunoe Y. Staphylococcus epidermidis Esp inhibits Staphylococcus aureus biofilm formation and nasal colonization. Nature. 2010;465(7296):346-9.
9. Sassetti CM, Boyd DH, Rubin EJ. Genes required for mycobacterial growth defined by high density mutagenesis. Mol Microbiol. 2003;48(1):77-84.
10. Lopes Ribeiro-Guimaraes M, Pessolania MCV. Comparative genomics of mycobacterial proteases. Microbial Pathogenesis. [Mini review]. 2007;173-78.
11. Zhong G. Chlamydia trachomatis secretion of proteases for manipulating host signaling pathways. Front Microbiol. 2011;2:14.
12. Brown GD, Dave JA, Gey van Pittius NC, Stevens L, Ehlers MR, Beyers AD. The mycosins of Mycobacterium tuberculosis H37Rv a family of subtilisin-like serine proteases. Gene. 2000;254(1-2):147-55.
13. Dave JA, Gey van Pittius NC, Beyers AD, Ehlers MR, Brown GD. Mycosin-1, a subtilisin-like serine protease of Mycobacterium tuberculosis, is cell wall-associated and expressed during infection of macrophages. BMC Microbiol. 2002; 2(30).
14. Ohol YM, Goetz DH, Chan K, Shiloh MU, Craik CS, Cox JS. Mycobacterium tuberculosis MycP1 protease plays a dual role in regulation of ESX-1 secretion and virulence. Cell Host Microbe. 2010; 7(3):210-20.
15. Sun R, Converse PJ, Ko C, Tyagi S, Morrison NE, Bishai WR Mycobacterium tuberculosis ECF sigma factor sigC is required for lethality in mice and for the conditional expression of a defined gene set. Mol Microbiol. 2004;52:25-38.
16. Biswas T, Small J, Vanda O, Odaira T, Deng H, Ehrt S, Tsodikov OV. Structural insight into serine protease Rv3671c that Protects M. Tuberculosis. Structure. 2010;18:1353-63.
17. Vandal OH, Pierini LM, Schnappinger D, Nathan CF, Ehrt S. A membrane protein preserves intrabacterial pH in intraphagosomal Mycobacterium tuberculosis. Nat Med. 2008;14(8):849-54.
18. Mohamedmohaideen NN, Palaninathan SK, Morin PM, Williams BJ, Braunstein M, Tichy SE, Locker J, Russell DH, Jacobs WR Jr, Sacchettini JC. Structure and function of the virulence-associated high-temperature requirement A of Mycobacterium tuberculosis. Biochemistry. 2008;47(23):6092-102.
19. White MJ, Savaryn JP, Bretl DJ, He H, Penoske RM, Terhune SS, Zahrt TC. The HtrA-Like Serine Protease PepD Interacts with and Modulates the Mycobacterium tuberculosis 35-kDa Antigen Outer Envelope Protein. PLoS One. 2011;6(3):e18175.
20. Upadhye V, Majumdar A, Gomashe A, Joshi D, Gangane N, Thamke D, Mendiratta D, Harinath BC. Inhibition of Mycobacterium tuberculosis secretory serine protease blocks bacterial multiplication both in axenic culture and in human macrophages. Scand J Infect Dis. 2009;41(8):569-76.
21. Cole ST, Brosch R, Parkhill J, Garnier T, Churcher C, Harris D, Gordon SV, Eiglmeier K, Gas S, Barry CE 3rd, Tekaia F, Badcock K, Basham D, Brown D, Chillingworth T, Connor R, Davies R, Devlin K, Feltwell T, Gentles S, Hamlin N, Holroyd S, Hornsby T, Jagels K, Krogh A, McLean J, Moule S, Murphy L, Oliver K, Osborne J, Quail MA, Rajandream MA, Rogers J, Rutter S, Seeger K, Skelton J, Squares R, Squares S, Sulston JE, Taylor K, Whitehead S, Barrell BG. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature. 1998;393(6685):537-44.
22. Dziedzic R, Kiran M, Plocinski P, Ziolkiewicz M, Brzostek A, Moomey M, Vadrevu IS, Dziadek J, Madiraju M, Rajagopalan M. Mycobacterium tuberculosis ClpX interacts with FtsZ and interferes with FtsZ assembly. PLoS One. 2010;5(7):e11058.
23. Maurizi MR, Clark WP, Kim SH, Gottesman S. ClpP Represents a unique family of serine proteases. Biological Chemistry. 1990;265(21):12546-52.
24. Tiwari A, Gupta S, Srivastava S, Srivastava R, Kumar Rawat A. A ClpP protein model as tuberculosis target for screening marine compounds. Biomedical Informatics. 2010:405-08.
25. Flynn JM, Neher SB, Kim YI, Sauer RT, Baker TA. Proteomic discovery of cellular substrates of the ClpXP protease reveals five classes of ClpX-recognition signals. Mol Cell. 2003;11(3):671-83.
26. Darwin KH. Prokaryotic ubiquitin-like protein (Pup), proteasomes and pathogenesis. Nat Rev Microbiol. 2009;7(7):485-91.
27. Pearce MJ, Mintseris J, Ferreyra J, Gygi SP, Darwin KH. Ubiquitin-like protein involved in the proteasome pathway of Mycobacterium tuberculosis. Science. 2008;322(5904):1104-7.
28. Xing Y, Johnson CV, Dobner PR, Lawrence JB. Higher level organization of individual gene transcription and RNA splicing. Science. 1993;259(5099):1326-30.
29. Botella H, Peyron P, Levillain F, Poincloux R, Poquet Y, Brandli I, Wang C, Tailleux L, Tilleul S, Charrière GM, Waddell SJ, Foti M, Lugo-Villarino G, Gao Q, Maridonneau-Parini I, Butcher PD, Castagnoli PR, Gicquel B, de Chastellier C, Neyrolles O. Mycobacterial p(1)-type ATPases mediate resistance to zinc poisoning in human macrophages. Cell Host Microbe. 2011;10(3):248-59.
30. Muttucumaru DG, Smith DA, McMinn EJ, Reese V, Coler RN, Parish T. Mycobacterium tuberculosis Rv0198c, a putative matrix metalloprotease is involved in pathogenicity. Tuberculosis (Edinb). 2011.
31. Sklar JG, Makinoshima H, Schneider JS, Glickman MS. M. tuberculosis intramembrane protease Rip1 controls transcription through three anti-sigma factor substrates. Mol Microbiol. 2010;77(3):605-17.
32. Makinoshima H, Glickman MS. Regulation of Mycobacterium tuberculosis cell envelope composition and virulence by intramembrane proteolysis. Nature. 2005;436(7049):406-9.
33. Akiyama Y, Ito K. Reconstitution of membrane proteolysis by FtsH. J Biol Chem. 2003;278(20):18146-53.
34. Srinivasan R, Anilkumar G, Rajeswari H, Ajitkumar P. Functional characterization of AAA family FtsH protease of Mycobacterium tuberculosis. FEMS Microbiol Lett. 2006;259(1):97-105.
35. Kiran M, Chauhan A, Dziedzic R, Maloney E, Mukherji SK, Madiraju M, Rajagopalan M. Mycobacterium tuberculosis ftsH expression in response to stress and viability. Tuberculosis (Edinb). 2009;89 Suppl 1:S70-3.
36. Zhang X, Chaney M, Wigneshweraraj SR, Schumacher J, Bordes P, Cannon W, Buck M. Mechanochemical ATPases and transcriptional activation. Mol Microbiol. 2002;45(4):895-903.
37. Urban S. Making the cut: central roles of intramembrane proteolysis in pathogenic microorganisms. Nat Rev Microbiol. 2009;7(6):411-23.
38. Zellmeier S, Zuber U, Schumann W, Wiegert T. The absence of FtsH metalloprotease activity causes overexpression of the sigmaW-controlled pbpE gene, resulting in filamentous growth of Bacillus subtilis. J Bacteriol 2003;185(3):973-82.
39. Liu J, Zuber P. The ClpX protein of Bacillus subtilis indirectly influences RNA polymerase holoenzyme composition and directly stimulates sigma-dependent transcription. Mol Microbiol. 2000;37(4):885-97.
40. Heinrich J, Hein K, Wiegert T. Two proteolytic modules are involved in regulated intramembrane proteolysis of Bacillus subtilis RsiW. Mol Microbiol. 2009;74(6):1412-26.
41. Estorninho M, Smith H, Thole J, Harders-Westerveen J, Kierzek A, Butler RE, Neyrolles O, Stewart GR. ClgR regulation of chaperone and protease systems is essential for Mycobacterium tuberculosis parasitism of the macrophage. Microbiology. 2010;156(Pt 11):3445-55.
42. Donà V, Rodrigue S, Dainese E, Palù G, Gaudreau L, Manganelli R, Provvedi R. Evidence of complex transcriptional, translational, and posttranslational regulation of the extracytoplasmic function sigma factor sigmaE in Mycobacterium tuberculosis. J Bacteriol. 2008;190(17):5963-71.
43. Ohol YM, Goetz DH, Chan K, Shiloh MU, Craik CS, Cox JS. Mycobacterium tuberculosis MycP1 protease plays a dual role in regulation of ESX-1 secretion and virulence. Cell Host Microbe. 2010;7(3):210-20.
44. Pathak SK, Basu S, Basu KK, Banerjee A, Pathak S, Bhattacharyya A, Kaisho T, Kundu M, Basu J. Direct extracellular interaction between the early secreted antigen ESAT-6 of Mycobacterium tuberculosis and TLR2 inhibits TLR signaling in macrophages. Nat Immunol. 2007;8(6):610-8.
45. Pathak SK, Basu S, Basu KK, Banerjee A, Pathak S, Bhattacharyya A, Kaisho T, Kundu M, Basu J. Direct extracellular interaction between the early secreted antigen ESAT-6 of Mycobacterium tuberculosis and TLR2 inhibits TLR signaling in macrophages. Nat Immunol. 2007 8(6):610-8.
46. Dave JA, Gey van Pittius NC, Beyers AD, Ehlers MR, Brown GD. Mycosin-1, a subtilisin-like serine protease of Mycobacterium. BMC Microbiol. 2002;2:30.
47. Shah F, Mukherjee P, Gut J, Legac J, Rosenthal PJ, Tekwani BL, Avery MA. Identification of novel malarial cysteine protease inhibitors using structure-based virtual screening of a focused cysteine protease inhibitor library. J Chem Inf Model. 2011;51(4):852-64.
48. de Farias Silva N, Lameira J, Alves CN. Computational analysis of aspartic protease plasmepsin II complexed with EH58 inhibitor: a QM/MM MD study. J Mol Model. 2011.
49. Schmitt EK, Riwanto M, Sambandamurthy V, Roggo S, Miault C, Zwingelstein C, Krastel P, Noble C, Beer D, Rao SP, Au M, Niyomrattanakit P, Lim V, Zheng J, Jeffery D, Pethe K, Camacho LR. The natural product cyclomarin kills mycobacterium tuberculosis by targeting the ClpC1 subunit of the caseinolytic protease. Angew Chem Int Ed Engl. 2011;50(26):5889-91.
50. Casari G, De Fusco M, Ciarmatori S, Zeviani M, Mora M, Fernandez P, De Michele G, Filla A, Cocozza S, Marconi R, Dürr A, Fontaine B, Ballabio A. Spastic paraplegia and OXPHOS impairment caused by mutations in paraplegin, a nuclear-encoded mitochondrial metalloprotease. Cell. 1998;93(6):973-83.
51. Lin G, Li D, de Carvalho LP, Deng H, Tao H, Vogt G, Wu K, Schneider J, Chidawanyika T, Warren JD, Li H, Nathan C. Inhibitors selective for mycobacterial versus human proteasomes. Nature. 2009;461(7264):621-6.
52. Majumdar A, Wankhade G, Kamble PD, Harinath BC. Effect of HIV protease inhibitors and Orlistat on mycobacterial ES-31 serine protease, a potential drug target in Mycobacterium tuberculosis. Indian J Tuberc. 2011;58(1):4-10.
53. Davide M. Ferraris DS, Petrera A, Marini S, Amstutz B, Coletta M, Sander P, Rizzi M. Crystal structure of Mycobacterium tuberculosis ZMP1, a metalloprotease involved in pathogenicity jbc. 2011.
54. Staroscik AM, Denkin SM, Nelson DR. 89 Regulation of the Vibrio anguillarum metalloprotease EmpA by posttranslational modification. J Bacteriol. 2005;187(7):2257-60.
55. Takaya A, Suzuki A, Kikuchi Y, Eguchi M, Isogai E, Tomoyasu T, Yamamoto T. Derepression of Salmonella pathogenicity island 1 genes within macrophages leads to rapid apoptosis via caspase-1- and caspase-3-dependent pathways. Cell Microbiol. 2005;7(1):79-90.
56. Yeoh S, O'Donnell RA, Koussis K, Dluzewski AR, Ansell KH, Osborne SA, Hackett F, Withers-Martinez C, Mitchell GH, Bannister LH, Bryans JS, Kettleborough CA, Blackman MJ. Subcellular discharge of a serine protease mediates release of invasive malaria parasites from host erythrocytes. Cell. 2007;131(6):1072-83.
57. Gregory DJ, Godbout M, Contreras I, Forget G, Olivier M. A novel form of NF-kappaB is induced by Leishmania infection: involvement in macrophage gene expression. Eur J Immunol. 2008;38(4):1071-81.
58. Le Negrate G, Krieg A, Faustin B, Loeffler M, Godzik A, Krajewski S, Reed JC. ChlaDub1 of Chlamydia trachomatis suppresses NF-kappaB activation and inhibitsIkappaBalpha ubiquitination and degradation. Cell Microbiol. 2008;10(9):1879-92.
59. Engel LS, Hill JM, Caballero AR, Green LC, O'Callaghan RJ. Protease IV, a unique extracellular protease and virulence factor from Pseudomonas aeruginosa. J Biol Chem. 1998;273(27):16792-7.
60. Kuramitsu HK. Proteases of Porphyromonas gingivalis: what don't they do? Oral Microbiol Immunol. 1998;13(5):263-70.
61. Nakayama K. Molecular genetics of Porphyromonas gingivalis: gingipains and other virulence factors. Curr Protein Pept Sci. 2003;4(6):389-95.
62. Maeda H, Molla A, Oda T, Katsuki T. Internalization of serratial protease into cells as an enzyme-inhibitor complex with alpha 2-macroglobulin and regeneration of protease activity and cytotoxicity. J Biol Chem. 1987;262(23):10946-50.
63. Reed S, Bouvier J, Pollack AS, Engel JC, Brown M, Hirata K, Que X, Eakin A, Hagblom P, Gillin F. Cloning of a virulence factor of Entamoeba histolytica. Pathogenic strains possess a unique cysteine proteinase gene. J Clin Invest. 1993;91(4):1532-40.
64. Breton CB, Blisnick T, Jouin H, Barale JC, Rabilloud T, Langsley G, Pereira da Silva LH. Plasmodium chabaudi p68 serine protease activity required for merozoite entry into mouse erythrocytes. Proc Natl Acad Sci U S A. 1992;89(20):9647-51.
65. Fuchs H, Wallich R, Simon MM, Kramer MD. The outer surface protein A of the spirochete Borrelia burgdorferi is a plasmin(ogen) receptor. Proc Natl Acad Sci U S A. 1994;91(26):12594-8.
66. Francis SE, Sullivan DJ, Jr., Goldberg DE. Hemoglobin metabolism in the malaria parasite Plasmodium falciparum. Annu Rev Microbiol. 1997;51 97-123.
67. Rasmussen M, Muller HP, Bjorck L. Protein GRAB of Streptococcus pyogenes regulates proteolysis at the bacterial surface by binding alpha2-macroglobulin. J Biol Chem. 1999;274(22):15336-44.
68. Schenkein HA, Fletcher HM, Bodnar M, Macrina FL. Increased opsonization of a prtH-defective mutant of Porphyromonas gingivalis W83 is caused by reduced degradation of complement-derived opsonins. J Immunol. 1995;154(10):5331-7.
69. Zhong G, Fan P, Ji H, Dong F, Huang Y. Identification of a chlamydial protease-like activity factor responsible for the degradation of host transcription factors J Exp Med. 2001;193(8):935-42.
70. Espinosa A, Alfano JR. Disabling surveillance: bacterial type III secretion system effectors that suppress innate immunity. Cell Microbiol. 2004;6(11):1027-40.
71. Li K, Foy E, Ferreon JC, Nakamura M, Ferreon AC, Ikeda M, Ray SC, Gale M Jr, Lemon SM. Immune evasion by hepatitis C virus NS3/4A protease-mediated cleavage of the Toll-like receptor 3 adaptor protein TRIF. Proc Natl Acad Sci U S A. 2005;102(8):2992-7.
72. Lad SP, Li J, da Silva Correia J, Pan Q, Gadwal S, Ulevitch RJ, Li E. Cleavage of p65/RelA of the NF-kappaB pathway by Chlamydia. Proc Natl Acad Sci U S A. 2007;104(8):2933-8.
73. Kai M, Piechulla B. Impact of volatiles of the rhizobacteria Serratia odorifera on the moss Physcomitrella patens. Plant Signal Behav. 2010;5(4):444-6.
74. DeCarlo AA, Grenett HE, Harber GJ, Windsor LJ, Bodden MK, Birkedal-Hansen B, Birkedal-Hansen H. Induction of matrix metalloproteinases and a collagen-degrading phenotype in fibroblasts and epithelial cells by secreted Porphyromonas gingivalis proteinase. J Periodontal Res. 1998;33(7):408-20.
75. Dave JA, Gey van Pittius NC, Beyers AD, Ehlers MR, Brown GD. Mycosin-1, a subtilisin-like serine protease of Mycobacterium tuberculosis, is cell wall-associated and expressed during infection of macrophages. BMC Microbiol. 2002;2:30.
76. Yasir AW, Skeiky MJL, JA Guderian, R Mohamath, T Bement, MR Alderson, SG. Reed. Cloning, expression, and immunological evaluation of two putative secreted serine protease antigens of Mycobacterium tuberculosis. Infection and Immunity. 1999;67(8):3998-4007.