The non-catalytic "cap domain" of a mycobacterial metallophosphoesterase regulates its expression and localization in the cell

Journal of Biological Chemistry

Volumn 289, Issue 32, 2014, Pages 22470-22481

  Matange, Nishad ^a   Podobnik, Marjetka ^b   Visweswariah, Sandhya S ^a  

^a INDIAN INSTITUTE OF SCIENCE   (India)

^b NATIONAL INSTITUTE OF CHEMISTRY   (Slovenia)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY;

ACTIVE SITE; BIOLOGICAL FUNCTIONS; C TERMINUS; CELL ENVELOPES; CELLULAR FUNCTION; METALLOPHOSPHOESTERASE; MYCOBACTERIAL; NON-CATALYTIC;

BIOLOGY;

BACTERIAL PROTEIN; CYCLIC AMP; PHOSPHODIESTERASE; RECOMBINANT PROTEIN;

AMINO ACID SEQUENCE; CELL MEMBRANE; CELL WALL; CHEMICAL STRUCTURE; CHEMISTRY; ENZYME ACTIVE SITE; ENZYMOLOGY; GENETICS; METABOLISM; MOLECULAR GENETICS; MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS; PROTEIN CONFORMATION; PROTEIN TERTIARY STRUCTURE; SEQUENCE HOMOLOGY; SITE DIRECTED MUTAGENESIS;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; CATALYTIC DOMAIN; CELL MEMBRANE; CELL WALL; CYCLIC AMP; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS; PHOSPHORIC DIESTER HYDROLASES; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 84905842669     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.578328     Document Type: Article

References (43)

1. Richter, W. (2002) 3′,5 Cyclic nucleotide phosphodiesterases class III: members, structure, and catalytic mechanism. Proteins 46, 278-286
2. Tyagi, R., Shenoy, A. R., and Visweswariah, S. S. (2009) Characterization of an evolutionarily conserved metallophosphoesterase that is expressed in the fetal brain and associated with the WAGR syndrome. J. Biol. Chem. 284, 5217-5228
3. Connelly, J. C., and Leach, D. R. (2002) Tethering on the brink: the evolutionarily conserved Mre11-Rad50 complex. Trends Biochem. Sci. 27, 410-418
4. Khalid, M. F., Damha, M. J., Shuman, S., and Schwer, B. (2005) Structurefunction analysis of yeastRNAdebranching enzyme (Dbr1), a manganesedependent phosphodiesterase. Nucleic Acids Res. 33, 6349-6360
5. Wang, L. K., Smith, P., and Shuman, S. (2013) Structure and mechanism of the 2′,3 phosphatase component of the bacterial Pnkp-Hen1 RNA repair system. Nucleic Acids Res. 41, 5864-5873
6. Imamura, R., Yamanaka, K., Ogura, T., Hiraga, S., Fujita, N., Ishihama, A., and Niki, H. (1996) Identification of the cpdA gene encoding cyclic 3′,5-adenosine monophosphate phosphodiesterase in Escherichia coli. J. Biol. Chem. 271, 25423-25429
7. Keppetipola, N., and Shuman, S. (2008) A phosphate-binding histidine of binuclear metallophosphodiesterase enzymes is a determinant of 2′,3-cyclic nucleotide phosphodiesterase activity. J. Biol. Chem. 283, 30942-30949
8. Shenoy, A. R., Sreenath, N., Podobnik, M., Kovacevic, M., and Visweswariah, S. S. (2005) The Rv0805 gene from Mycobacterium tuberculosis encodes a 3′,5-cyclic nucleotide phosphodiesterase: biochemical and mutational analysis. Biochemistry 44, 15695-15704
9. McLoughlin, S. Y., Jackson, C., Liu, J. W., and Ollis, D. L. (2004) Growth of Escherichia coli coexpressing phosphotriesterase and glycerophosphodiester phosphodiesterase using paraoxon as the sole phosphorus source. Appl. Environ. Microbiol. 70, 404-412
10. Collins, B. M., Skinner, C. F., Watson, P. J., Seaman, M. N., and Owen, D. J. (2005) Vps29 has a phosphoesterase fold that acts as a protein interaction scaffold for retromer assembly. Nat. Struct. Mol. Biol. 12, 594-602
11. Dermol, U., Janardan, V., Tyagi, R., Visweswariah, S. S., and Podobnik, M. (2011) Unique utilization of a phosphoprotein phosphatase fold by a mammalian phosphodiesterase associated with WAGR syndrome. J. Mol. Biol. 412, 481-494
12. Jackson, C. J., Carr, P. D., Liu, J. W., Watt, S. J., Beck, J. L., and Ollis, D. L. (2007) The structure and function of a novel glycerophosphodiesterase from Enterobacter aerogenes. J. Mol. Biol. 367, 1047-1062
13. Kim, Y. G., Jeong, J. H., Ha, N. C., and Kim, K. J. (2011) Structural and functional analysis of the Lmo2642 cyclic nucleotide phosphodiesterase from Listeria monocytogenes. Proteins 79, 1205-1214
14. Miller, D. J., Shuvalova, L., Evdokimova, E., Savchenko, A., Yakunin, A. F., and Anderson, W. F. (2007) Structural and biochemical characterization of a novel Mn2-dependent phosphodiesterase encoded by the yfcE gene. Protein Sci. 16, 1338-1348
15. Park, Y. B., Chae, J., Kim, Y. C., and Cho, Y. (2011) Crystal structure of human Mre11: understanding tumorigenic mutations. Structure 19, 1591-1602
16. Daumann, L. J., Schenk, G., Ollis, D. L., and Gahan, L. R. (2014) Spectroscopic and mechanistic studies of dinuclear metallohydrolases and their biomimetic complexes. Dalton Trans. 43, 910-928
17. Podobnik, M., Tyagi, R., Matange, N., Dermol, U., Gupta, A. K., Mattoo, R., Seshadri, K., and Visweswariah, S. S. (2009) A mycobacterial cyclic AMP phosphodiesterase that moonlights as a modifier of cell wall permeability. J. Biol. Chem. 284, 32846-32857
18. Shenoy, A. R., Capuder, M., Draskovic, P., Lamba, D., Visweswariah, S. S., and Podobnik, M. (2007) Structural and biochemical analysis of the Rv0805 cyclic nucleotide phosphodiesterase from Mycobacterium tuberculosis. J. Mol. Biol. 365, 211-225
19. Matange, N., Hunt, D. M., Buxton, R. S., and Visweswariah, S. S. (2013) Overexpression of the Rv0805 phosphodiesterase elicits a cAMP-independent transcriptional response. Tuberculosis 93, 492-500
20. Hopfner, K. P., Karcher, A., Craig, L., Woo, T. T., Carney, J. P., and Tainer, J. A. (2001) Structural biochemistry and interaction architecture of the DNAdouble-strand break repair Mre11 nuclease and Rad50-ATPase. Cell 105, 473-485
21. Tamura, K., Stecher, G., Peterson, D., Filipski, A., and Kumar, S. (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30, 2725-2729
22. Braunstein, M., Brown, A. M., Kurtz, S., and Jacobs, W. R., Jr. (2001) Two nonredundant SecA homologues function in mycobacteria. J. Bacteriol. 183, 6979-6990
23. Delogu, G., Bua, A., Pusceddu, C., Parra, M., Fadda, G., Brennan, M. J., and Zanetti, S. (2004) Expression and purification of recombinant methylated HBHA in Mycobacterium smegmatis. FEMS Microbiol. Lett. 239, 33-39
24. Dass, B. K., Sharma, R., Shenoy, A. R., Mattoo, R., and Visweswariah, S. S. (2008) Cyclic AMP in mycobacteria: characterization and functional role of the Rv1647 ortholog in Mycobacterium smegmatis. J. Bacteriol. 190, 3824-3834
25. Rezwan, M., Lanéelle, M. A., Sander, P., and Daffé, M. (2007) Breaking down the wall: fractionation of mycobacteria. J. Microbiol. Methods 68, 32-39
26. Andersson, C. S., Lundgren, C. A., Magnúsdóttir, A., Ge, C., Wieslander, A., Martinez Molina, D., and Högbom, M. (2012) The Mycobacterium tuberculosis very long chain fatty acyl-CoA synthetase: structural basis for housing lipid substrates longer than the enzyme. Structure 20, 1062-1070
27. Braunstein, M., Espinosa, B. J., Chan, J., Belisle, J. T., and Jacobs, W. R., Jr. (2003) SecA2 functions in the secretion of superoxide dismutase A and in the virulence of Mycobacterium tuberculosis. Mol. Microbiol. 48, 453-464
28. Feltcher, M. E., Gibbons, H. S., Ligon, L. S., and Braunstein, M. (2013) Protein export by the mycobacterial SecA2 system is determined by the preprotein mature domain. J. Bacteriol. 195, 672-681
29. 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
30. Trülzsch, K., Roggenkamp, A., Pelludat, C., Rakin, A., Jacobi, C., and Heesemann, J. (2001) Cloning and characterization of the gene encoding periplasmic 2′,3-cyclic phosphodiesterase of Yersinia enterocolitica O:8. Microbiology 147, 203-213
31. Monteferrante, C. G., Miethke, M., van der Ploeg, R., Glasner, C., and van Dijl, J. M. (2012) Specific targeting of the metallophosphoesterase YkuE to the bacillus cell wall requires the twin-arginine translocation system. J. Biol. Chem. 287, 29789-29800
32. Müller, J. P., and Wagner, M. (1999) Localisation of the cell wall-associated phosphodiesterase PhoD of Bacillus subtilis. FEMS Microbiol. Lett. 180, 287-296
33. Posey, J. E., Shinnick, T. M., and Quinn, F. D. (2006) Characterization of the twin-arginine translocase secretion system of Mycobacterium smegmatis. J. Bacteriol. 188, 1332-1340
34. Daleke, M. H., Ummels, R., Bawono, P., Heringa, J., Vandenbroucke-Grauls, C. M., Luirink, J., and Bitter, W. (2012) General secretion signal for the mycobacterial type VII secretion pathway. Proc. Natl. Acad. Sci. U.S.A. 109, 11342-11347
35. Cascioferro, A., Delogu, G., Colone, M., Sali, M., Stringaro, A., Arancia, G., Fadda, G., Palù, G., and Manganelli, R. (2007) PE is a functional domain responsible for protein translocation and localization on mycobacterial cell wall. Mol. Microbiol. 66, 1536-1547
36. Brennan, P. J. (2003) Structure, function, and biogenesis of the cell wall of Mycobacterium tuberculosis. Tuberculosis 83, 91-97
37. Yao, Y., Barghava, N., Kim, J., Niederweis, M., and Marassi, F. M. (2012) Molecular structure and peptidoglycan recognition of Mycobacterium tuberculosis ArfA (Rv0899). J. Mol. Biol. 416, 208-220
38. Li, J., Shi, C., Gao, Y., Wu, K., Shi, P., Lai, C., Chen, L., Wu, F., and Tian, C. (2012) Structural studies of Mycobacterium tuberculosis Rv0899 reveal a monomeric membrane-anchoring protein with two separate domains. J. Mol. Biol. 415, 382-392
39. Kocíncová, D., Sondén, B., de Mendonça-Lima, L., Gicquel, B., and Reyrat, J. M. (2004) The Erp protein is anchored at the surface by a carboxyterminal hydrophobic domain and is important for cell-wall structure in Mycobacterium smegmatis. FEMS Microbiol. Lett. 231, 191-196
40. Barthe, P., Mukamolova, G. V., Roumestand, C., and Cohen-Gonsaud, M. (2010) The structure of PknB extracellular PASTA domain from Mycobacterium tuberculosis suggests a ligand-dependent kinase activation. Structure 18, 606-615
41. Schiller, C. B., Lammens, K., Guerini, I., Coordes, B., Feldmann, H., Schlauderer, F., Möckel, C., Schele, A., Strässer, K., Jackson, S. P., and Hopfner, K. P. (2012) Structure of Mre11-Nbs1 complex yields insights into ataxia-telangiectasia-like disease mutations and DNA damage signaling. Nat. Struct. Mol. Biol. 19, 693-700
42. Barth, E., Gora, K. V., Gebendorfer, K. M., Settele, F., Jakob, U., and Winter, J. (2009) Interplay of cellular cAMP levels,S activity and oxidative stress resistance in Escherichia coli. Microbiology 155, 1680-1689
43. Fuchs, E. L., Brutinel, E. D., Klem, E. R., Fehr, A. R., Yahr, T. L., and Wolfgang, M. C. (2010) In vitro and in vivo characterization of the Pseudomonas aeruginosa cyclic AMP (cAMP) phosphodiesterase CpdA, required for cAMP homeostasis and virulence factor regulation. J. Bacteriol. 192, 2779-2790