Substrate specificity of MarP, a periplasmic protease required for resistance to acid and oxidative stress in Mycobacterium tuberculosis

Journal of Biological Chemistry

Volumn 288, Issue 18, 2013, Pages 12489-12499

  Small, Jennifer L ^a   O'Donoghue, Anthony J ^b   Boritsch, Eva C ^a   Tsodikov, Oleg V ^c   Knudsen, Giselle M ^b   Vandal, Omar ^a   Craik, Charles S ^b   Ehrt, Sabine ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF MICHIGAN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMBINATORIAL LIBRARY; ENZYMATIC PROPERTIES; HYDROPHOBIC RESIDUES; KINETIC PROPERTIES; MYCOBACTERIUM TUBERCULOSIS; STRUCTURAL STUDIES; SUBSTRATE SPECIFICITY; TRANSMEMBRANE HELICES;

ACID RESISTANCE; AMINO ACIDS; COVALENT BONDS; MASS SPECTROMETRY; TUBES (COMPONENTS);

SUBSTRATES;

ALANINE; ARGININE; ASPARAGINE; CYSTEINE; LEUCINE; PROTEIN MARP; RECOMBINANT ENZYME; SERINE PROTEINASE; TRYPTOPHAN; UNCLASSIFIED DRUG;

ACIDITY; ARTICLE; CONTROLLED STUDY; CYTOPLASM; ENZYME KINETICS; ENZYME LOCALIZATION; ENZYME SPECIFICITY; ENZYME SUBSTRATE; GENE MUTATION; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; OXIDATIVE STRESS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DOMAIN;

MULTIPLEX SUBSTRATE PROFILING; MYCOBACTERIUM TUBERCULOSIS; PEPTIDE BIOSYNTHESIS; PEPTIDES; PH REGULATION; POSITIONAL-SCANNING SYNTHETIC COMBINATORIAL LIBRARY; SERINE PROTEASE; STRESS RESPONSE;

HYDROGEN-ION CONCENTRATION; MUTATION; MYCOBACTERIUM TUBERCULOSIS; OXIDATIVE STRESS; PEPTIDE HYDROLASES; PERIPLASMIC PROTEINS; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; SUBSTRATE SPECIFICITY;

MYCOBACTERIUM TUBERCULOSIS;

EID: 84877117930     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.456541     Document Type: Article

References (58)

1. WHO (2011) Global Tuberculosis Control, http://www.who.int/tb/ publications/global-report/en/index.html
2. Sherman, D. R., Sabo, P. J., Hickey, M. J., Arain, T. M., Mahairas, G. G., Yuan, Y., Barry, C. E., 3rd, and Stover, C. K. (1995) Disparate responses to oxidative stress in saprophytic and pathogenic mycobacteria. Proc. Natl. Acad. Sci. U.S.A. 92, 6625-6629
3. Vandal, O. H., Pierini, L. M., Schnappinger, D., Nathan, C. F., and Ehrt, S. (2008) A membrane protein preserves intrabacterial pH in intraphagosomal Mycobacterium tuberculosis. Nat. Med. 14, 849-854
4. Vandal, O. H., Roberts, J. A., Odaira, T., Schnappinger, D., Nathan, C. F., and Ehrt, S. (2009) Acid-susceptible mutants of Mycobacterium tuberculosis share hypersusceptibility to cell wall and oxidative stress and to the host environment. J. Bacteriol. 191, 625-631
5. Ehrt, S., and Schnappinger, D. (2009) Mycobacterial survival strategies in the phagosome. Defence against host stresses. Cell. Microbiol. 11, 1170-1178
6. Armstrong, J. A., and Hart, P. D. (1971) Response of cultured macrophages to Mycobacterium tuberculosis, with observations on fusion of lysosomes with phagosomes. J. Exp. Med. 134, 713-740
7. Clemens, D. L., and Horwitz, M. A. (1995) Characterization of the Mycobacterium tuberculosis phagosome and evidence that phagosomal maturation is inhibited. J. Exp. Med. 181, 257-270
8. Sturgill-Koszycki, S., Schlesinger, P. H., Chakraborty, P., Haddix, P. L., Collins, H. L., Fok, A. K., Allen, R. D., Gluck, S. L., Heuser, J., and Russell, D. G. (1994) Lack of acidification in Mycobacterium phagosomes produced by exclusion of the vesicular proton-ATPase. Science 263, 678-681
9. Ohkuma, S., and Poole, B. (1978) Fluorescence probe measurement of the intralysosomal pH in living cells and the perturbation of pH by various agents. Proc. Natl. Acad. Sci. U.S.A. 75, 3327-3331 (Pubitemid 8389720)
10. Schaible, U. E., Sturgill-Koszycki, S., Schlesinger, P. H., and Russell, D. G. (1998) Cytokine activation leads to acidification and increases maturation of Mycobacterium avium-containing phagosomes in murine macrophages. J. Immunol. 160, 1290-1296 (Pubitemid 28093427)
11. Via, L. E., Fratti, R. A., McFalone, M., Pagan-Ramos, E., Deretic, D., and Deretic, V. (1998) Effects of cytokines on mycobacterial phagosome maturation. J. Cell Sci. 111, 897-905 (Pubitemid 28196073)
12. MacMicking, J. D. (2003) Immune control of tuberculosis by IFN-γ-inducible LRG-47. Science 302, 654-659
13. Huynh, K. K., and Grinstein, S. (2007) Regulation of vacuolar pH and its modulation by some microbial species. Microbiol. Mol. Biol. Rev. 71, 452-462 (Pubitemid 47429280)
14. Foster, J. W. (1999) When protons attack. Microbial strategies of acid adaptation. Curr. Opin. Microbiol. 2, 170-174
15. Cotter, P. D., and Hill, C. (2003) Surviving the acid test. Responses of gram-positive bacteria to low pH. Microbiol. Mol. Biol. Rev. 67, 429-453 (Pubitemid 37122528)
16. Buchmeier, N., Blanc-Potard, A., Ehrt, S., Piddington, D., Riley, L., and Groisman, E. A. (2000) A parallel intraphagosomal survival strategy shared by Mycobacterium tuberculosis and Salmonella enterica. Mol. Microbiol. 35, 1375-1382 (Pubitemid 30175513)
17. Song, H., Huff, J., Janik, K., Walter, K., Keller, C., Ehlers, S., Bossmann, S. H., and Niederweis, M. (2011) Expression of the ompATb operon accelerates ammonia secretion and adaptation of Mycobacterium tuberculosis to acidic environments. Mol. Microbiol. 80, 900-918
18. Rohde, K. H., Abramovitch, R. B., and Russell, D. G. (2007) Mycobacterium tuberculosis invasion of macrophages. Linking bacterial gene expression to environmental cues. Cell Host Microbe 2, 352-364 (Pubitemid 350056395)
19. Abramovitch, R. B., Rohde, K. H., Hsu, F.-F., and Russell, D. G. (2011) aprABC. A Mycobacterium tuberculosis complex-specific locus that modulates pH-driven adaptation to the macrophage phagosome. Mol. Microbiol. 80, 678-694
20. Biswas, T., Small, J., Vandal, O., Odaira, T., Deng, H., Ehrt, S., and Tsodikov, O. V. (2010) Structural insight into serine protease Rv3671c that protects M. tuberculosis from oxidative and acidic stress. Structure 18, 1353-1363
21. Ribeiro-Guimarães, M. L., and Pessolani, M. C. (2007) Comparative genomics of mycobacterial proteases. Microb. Pathog. 43, 173-178
22. Sonnhammer, E. L., von Heijne, G., and Krogh, A. (1998) A hidden Markov model for predicting transmembrane helices in protein sequences. Proc. Int. Conf. Intell. Syst. Mol. Biol. 6, 175-182
23. Hoffmann, C., Leis, A., Niederweis, M., Plitzko, J. M., and Engelhardt, H. (2008) Disclosure of the mycobacterial outer membrane. Cryo-electron tomography and vitreous sections reveal the lipid bilayer structure. Proc. Natl. Acad. Sci. U.S.A. 105, 3963-3967 (Pubitemid 351723507)
24. Zuber, B., Chami, M., Houssin, C., Dubochet, J., Griffiths, G., and Daffé, M. (2008) Direct visualization of the outer membrane of mycobacteria and corynebacteria in their native state. J. Bacteriol. 190, 5672-5680
25. Clausen, T., Southan, C., and Ehrmann, M. (2002) The HtrA family of proteases. Implications for protein composition and cell fate. Mol. Cell 10, 443-455 (Pubitemid 35284166)
26. Skorko-Glonek, J., Zurawa-Janicka, D., Koper, T., Jarzab, M., Figaj, D., Glaza, P., and Lipinska, B. (2013) HtrA protease family as therapeutic targets. Curr. Pharm. Des. 19, 977-1009
27. Krojer, T., Garrido-Franco, M., Huber, R., Ehrmann, M., and Clausen, T. (2002) Crystal structure of DegP (HtrA) reveals a new protease-chaperone machine. Nature 416, 455-459 (Pubitemid 34272883)
28. Cole, S. T., Brosch, R., Parkhill, J., Garnier, T., Churcher, C., Harris, D., Gordon, S. V., Eiglmeier, K., Gas, S., Barry, C. E., 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, M. A., Rajandream, M. A., Rogers, J., Rutter, S., Seeger, K., Skelton, J., Squares, R., Squares, S., Sulston, J. E., Taylor, K., Whitehead, S., and Barrell, B. G. (1998) Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393, 537-544 (Pubitemid 28319235)
29. Mohamedmohaideen, N. N., Palaninathan, S. K., Morin, P. M., Williams, B. J., Braunstein, M., Tichy, S. E., Locker, J., Russell, D. H., Jacobs, W. R., Jr., and Sacchettini, J. C. (2008) Structure and function of the virulence-associated High Temperature Requirement A of Mycobacterium tuberculosis. Biochemistry 47, 6092-6102 (Pubitemid 351812822)
30. White, M. J., He, H., Penoske, R. M., Twining, S. S., and Zahrt, T. C. (2010) PepD participates in the mycobacterial stress response mediated through MprAB and SigE. J. Bacteriol. 192, 1498-1510
31. Kim, D. Y., and Kim, K. K. (2005) Structure and function of HtrA family proteins, the key players in protein quality control. J. Biochem. Mol. Biol. 38, 266-274
32. Choe, Y., Leonetti, F., Greenbaum, D. C., Lecaille, F., Bogyo, M., Brömme, D., Ellman, J. A., and Craik, C. S. (2006) Substrate profiling of cysteine proteases using a combinatorial peptide library identifies functionally unique specificities. J. Biol. Chem. 281, 12824-12832 (Pubitemid 43855375)
33. O'Donoghue, A. J., Eroy-Reveles, A. A., Knudsen, G. M., Ingram, J., Zhou, M., Statnekov, J. B., Greninger, A. L., Hostetter, D. R., Qu, G., Maltby, D. A., Anderson, M. O., Derisi, J. L., McKerrow, J. H., Burlingame, A. L., and Craik, C. S. (2012) Global identification of peptidase specificity by multiplex substrate profiling. Nat. Methods 9, 1095-1100
34. Braunstein, M., Griffin, T. J., IV, Kriakov, J. I., Friedman, S. T., Grindley, N. D., and Jacobs, W. R., Jr. (2000) Identification of genes encoding exported Mycobacterium tuberculosis proteins using a Tn552′phoA in vitro transposition system. J. Bacteriol. 182, 2732-2740 (Pubitemid 30246902)
35. Chalkley, R. J., Baker, P. R., Medzihradszky, K. F., Lynn, A. J., and Burlingame, A. L. (2008) In-depth analysis of tandem mass spectrometry data from disparate instrument types. Mol. Cell. Proteomics 7, 2386-2398
36. Colaert, N., Helsens, K., Martens, L., Vandekerckhove, J., and Gevaert, K. (2009) Improved visualization of protein consensus sequences by iceLogo. Nat. Methods 6, 786-787
37. Emsley, P., and Cowtan, K. (2004) Coot. Model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132 (Pubitemid 41742764)
38. Unni, S., Huang, Y., Hanson, R. M., Tobias, M., Krishnan, S., Li, W. W., Nielsen, J. E., and Baker, N. A. (2011) Web servers and services for electrostatics calculations with APBS and PDB2PQR. J. Comput. Chem. 32, 1488-1491
39. Manoil, C., and Beckwith, J. (1986) A genetic approach to analyzing membrane protein topology. Science 233, 1403-1408 (Pubitemid 17169373)
40. Goldman, B. S., Beck, D. L., Monika, E. M., and Kranz, R. G. (1998) Transmembrane heme delivery systems. Proc. Natl. Acad. Sci. U.S.A. 95, 5003-5008 (Pubitemid 28208540)
41. Harris, J. L., Backes, B. J., Leonetti, F., Mahrus, S., Ellman, J. A., and Craik, C. S. (2000) Rapid and general profiling of protease specificity by using combinatorial fluorogenic substrate libraries. Proc. Natl. Acad. Sci. U.S.A. 97, 7754-7759 (Pubitemid 30460720)
42. Sojka, D., Franta, Z., Frantová, H., Bartosová, P., Horn, M., Váchová, J., O'Donoghue, A. J., Eroy-Reveles, A. A., Craik, C. S., Knudsen, G. M., Caffrey, C. R., McKerrow, J. H., Mares, M., and Kopácek, P. (2012) Characterization of gut-associated cathepsin D hemoglobinase from tick Ixodes ricinus (IrCD1). J. Biol. Chem. 287, 21152-21163
43. Makinoshima, H., and Glickman, M. S. (2005) Regulation of Mycobacterium tuberculosis cell envelope composition and virulence by intramembrane proteolysis. Nature 436, 406-409 (Pubitemid 41059051)
44. Sklar, J. G., Makinoshima, H., Schneider, J. S., and Glickman, M. S. (2010) M. tuberculosis intramembrane protease Rip1 controls transcription through three anti-sigma factor substrates. Mol. Microbiol. 77, 605-617
45. Gandotra, S., Schnappinger, D., Monteleone, M., Hillen, W., and Ehrt, S. (2007) In vivo gene silencing identifies the Mycobacterium tuberculosis proteasome as essential for the bacteria to persist in mice. Nat. Med. 13, 1515-1520 (Pubitemid 350224249)
46. Raju, R. M., Unnikrishnan, M., Rubin, D. H., Krishnamoorthy, V., Kandror, O., Akopian, T. N., Goldberg, A. L., and Rubin, E. J. (2012) Mycobacterium tuberculosis ClpP1 and ClpP2 function together in protein degradation and are required for viability in vitro and during infection. PLoS Pathog. 8, e1002511
47. Ohol, Y. M., Goetz, D. H., Chan, K., Shiloh, M. U., Craik, C. S., and Cox, J. S. (2010) Mycobacterium tuberculosis MycP1 protease plays a dual role in regulation of ESX-1 secretion and virulence. Cell Host Microbe 7, 210-220
48. Wilks, J. C., and Slonczewski, J. L. (2007) pH of the cytoplasm and periplasm of Escherichia coli. Rapid measurement by green fluorescent protein fluorimetry. J. Bacteriol. 189, 5601-5607 (Pubitemid 47206406)
49. Sawa, J., Malet, H., Krojer, T., Canellas, F., Ehrmann, M., and Clausen, T. (2011) Molecular adaptation of the DegQ protease to exert protein quality control in the bacterial cell envelope. J. Biol. Chem. 286, 30680-30690
50. Hedstrom, L. (2002) Serine protease mechanism and specificity. Chem. Rev. 102, 4501-4524
51. Jabaiah, A. M., Getz, J. A., Witkowski, W. A., Hardy, J. A., and Daugherty, P. S. (2012) Identification of protease exosite-interacting peptides that enhance substrate cleavage kinetics. Biol. Chem. 393, 933-941
52. Darby, N., and Creighton, T. E. (1995) Disulfide Bonds in Protein Folding and Stability. pp. 219-252, Humana Press Inc., Totowa, NJ
53. Wedemeyer, W. J., Welker, E., Narayan, M., and Scheraga, H. A. (2000) Disulfide bonds and protein folding. Biochemistry 39, 7032
54. Ito, K., and Inaba, K. (2008) The disulfide bond formation (Dsb) system. Curr. Opin. Struct. Biol. 18, 450-458
55. Dutton, R. J., Boyd, D., Berkmen, M., and Beckwith, J. (2008) Bacterial species exhibit diversity in their mechanisms and capacity for protein disulfide bond formation. Proc. Natl. Acad. Sci. U.S.A. 105, 11933-11938
56. Dutton, R. J., Wayman, A., Wei, J. R., Rubin, E. J., Beckwith, J., and Boyd, D. (2010) Inhibition of bacterial disulfide bond formation by the anticoagulant warfarin. Proc. Natl. Acad. Sci. U.S.A. 107, 297-301
57. Skórko-Glonek, J., Sobiecka-Szkatuła, A., and Lipińska, B. (2006) Characterization of disulfide exchange between DsbA and HtrA proteins from Escherichia coli. Acta Biochim. Pol. 53, 585-589
58. Skórko-Glonek, J., Zurawa, D., Tanfani, F., Scirè, A., Wawrzynów, A., Narkiewicz, J., Bertoli, E., and Lipińska, B. (2003) The N-terminal region of HtrA heat shock protease from Escherichia coli is essential for stabilization of HtrA primary structure and maintaining of its oligomeric structure. Biochim. Biophys. Acta 1649, 171-182