Oligomeric state study of prokaryotic rhomboid proteases

Biochimica et Biophysica Acta - Biomembranes

Volumn 1818, Issue 12, 2012, Pages 3090-3097

  Sampathkumar, Padmapriya ^a   Mak, Michelle W ^a   Fischer Witholt, Sarah J ^a   Guigard, Emmanuel ^a   Kay, Cyril M ^a   Lemieux, M Joanne ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Dimerization; GlpG; Intramembrane protease; Oligomerization; Rhomboid peptidase; Rhomboid protease

Indexed keywords

DETERGENT; DODECYLMALTOSIDE; MONOMER; PROTEIN ECGLPG; PROTEIN HIGLPG; PROTEIN YQGP; PROTEINASE; TETRAMER; UNCLASSIFIED DRUG;

ARTICLE; BACILLUS SUBTILIS; CONTROLLED STUDY; ESCHERICHIA COLI; GEL FILTRATION; HAEMOPHILUS INFLUENZAE; LIPID BILAYER; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN CROSS LINKING; PROTEIN DOMAIN;

BACILLUS SUBTILIS; BACTERIAL PROTEINS; DNA-BINDING PROTEINS; ENDOPEPTIDASES; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; HAEMOPHILUS INFLUENZAE; LIPID BILAYERS; MEMBRANE PROTEINS; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY;

BACILLUS SUBTILIS; ESCHERICHIA COLI; HAEMOPHILUS INFLUENZAE; PROKARYOTA;

EID: 84865574683     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2012.08.004     Document Type: Article

References (58)

1. A.J. Barrett, N.D. Rawlings, and E.A. O'Brien The MEROPS database as a protease information system J. Struct. Biol. 134 2001 95 102
2. J.D. Wasserman, S. Urban, and M. Freeman A family of rhomboid-like genes: Drosophila rhomboid-1 and roughoid/rhomboid-3 cooperate to activate EGF receptor signaling Genes Dev. 14 2000 1651 1663
3. J.C. Pascall, and K.D. Brown Characterization of a mammalian cDNA encoding a protein with high sequence similarity to the Drosophila regulatory protein rhomboid FEBS Lett. 429 1998 337 340
4. M. Freeman Rhomboid proteases and their biological functions Annu. Rev. Genet. 42 2008 191 210
5. S. Urban, G. Brown, and M. Freeman EGF receptor signalling protects smooth-cuticle cells from apoptosis during Drosophila ventral epidermis development Development 131 2004 1835 1845
6. Z. Yan, H. Zou, F. Tian, J.R. Grandis, A.J. Mixson, P.Y. Lu, and L.Y. Li Human rhomboid family-1 gene silencing causes apoptosis or autophagy to epithelial cancer cells and inhibits xenograft tumor growth Mol. Cancer Ther. 7 2008 1355 1364
7. H. Zou, S.M. Thomas, Z.W. Yan, J.R. Grandis, A. Vogt, and L.Y. Li Human rhomboid family-1 gene RHBDF1 participates in GPCR-mediated transactivation of EGFR growth signals in head and neck squamous cancer cells FASEB J. 23 2009 425 432
8. M.C. Abba, E. Lacunza, M.I. Nunez, A. Colussi, M. Isla-Larrain, A. Segal-Eiras, M.V. Croce, and C.M. Aldaz Rhomboid domain containing 2 (RHBDD2): a novel cancer-related gene over-expressed in breast cancer Biochim. Biophys. Acta 1792 2009 988 997
9. C. Adrain, K. Strisovsky, M. Zettl, L. Hu, M.K. Lemberg, and M. Freeman Mammalian EGF receptor activation by the rhomboid protease RHBDL2 EMBO Rep. 12 2011 421 427
10. C.P. Blobel ADAMs: key components in EGFR signalling and development Nat. Rev. Mol. Cell Biol. 6 2005 32 43
11. G.A. McQuibban, S. Saurya, and M. Freeman Mitochondrial membrane remodelling regulated by a conserved rhomboid protease Nature 423 2003 537 541
12. R.B. Hill, and L. Pellegrini The PARL family of mitochondrial rhomboid proteases Semin. Cell Dev. Biol. 21 2010 582 592
13. G.A. McQuibban The PARLance of Parkinson disease Autophagy 2011 790 792
14. C. Frezza, S. Cipolat, O. Martins de Brito, M. Micaroni, G.V. Beznoussenko, T. Rudka, D. Bartoli, R.S. Polishuck, N.N. Danial, B. De Strooper, and L. Scorrano OPA1 controls apoptotic cristae remodeling independently from mitochondrial fusion Cell 126 2006 177 189
15. I.M. Vera, W.L. Beatty, P. Sinnis, and K. Kim Plasmodium protease ROM1 is important for proper formation of the parasitophorous vacuole PLoS Pathog. 7 2011 e1002197
16. S. Urban, D. Schlieper, and M. Freeman Conservation of intramembrane proteolytic activity and substrate specificity in prokaryotic and eukaryotic rhomboids Curr. Biol. 12 2002 1507 1512
17. P.N. Rather, X. Ding, R.R. Baca-DeLancey, and S. Siddiqui Providencia stuartii genes activated by cell-to-cell signaling and identification of a gene required for production or activity of an extracellular factor J. Bacteriol. 181 1999 7185 7191
18. R.E. Dalbey, P. Wang, and J.M. van Dijl Membrane proteases in the bacterial protein secretion and quality control pathway Microbiol. Mol. Biol. Rev. 76 2012 311 330
19. A. Camilli, and B.L. Bassler Bacterial small-molecule signaling pathways Science 311 2006 1113 1116
20. L.R. Mesak, F.M. Mesak, and M.K. Dahl Expression of a novel gene, gluP, is essential for normal Bacillus subtilis cell division and contributes to glucose export BMC Microbiol. 4 2004 13
21. K.M. Clemmer, G.M. Sturgill, A. Veenstra, and P.N. Rather Functional characterization of Escherichia coli GlpG and additional rhomboid proteins using an aarA mutant of Providencia stuartii J. Bacteriol. 188 2006 3415 3419
22. M.J. Lemieux, S.J. Fischer, M.M. Cherney, K.S. Bateman, and M.N.G. James Rhomboid peptidase from Haemophilus influenzae: insights into the mechanism of intramembrane proteolysis from the crystal structure PNAS 104 3 2006 750 754
23. Y. Wang, Y. Zhang, and Y. Ha Crystal structure of a rhomboid family intramembrane protease Nature 444 2006 179 180
24. Z. Wu, N. Yan, L. Feng, A. Oberstein, H. Yan, R.P. Baker, L. Gu, P.D. Jeffrey, S. Urban, and Y. Shi Structural analysis of a rhomboid family intramembrane protease reveals a gating mechanism for substrate entry Nat. Struct. Mol. Biol. 13 2006 1084 1091
25. A. Ben-Shem, D. Fass, and E. Bibi Structural basis for intramembrane proteolysis by rhomboid serine proteases Proc. Natl. Acad. Sci. U.S.A. 104 2007 462 466
26. K.R. Vinothkumar Structure of rhomboid protease in a lipid environment J. Mol. Biol. 407 2011 232 247
27. M.K. Lemberg, J. Menendez, A. Misik, M. Garcia, C.M. Koth, and M. Freeman Mechanism of intramembrane proteolysis investigated with purified rhomboid proteases EMBO J. 24 2005 464 472
28. S. Maegawa, K. Ito, and Y. Akiyama Proteolytic action of GlpG, a rhomboid protease in the Escherichia coli cytoplasmic membrane Biochemistry 44 2005 13543 13552
29. O.D. Ekici, M. Paetzel, and R.E. Dalbey Unconventional serine proteases: variations on the catalytic Ser/His/Asp triad configuration Protein Sci. 17 2008 2023 2037
30. K.R. Vinothkumar, K. Strisovsky, A. Andreeva, Y. Christova, S. Verhelst, and M. Freeman The structural basis for catalysis and substrate specificity of a rhomboid protease EMBO J. 29 2011 3797 3809
31. Y. Xue, S. Chowdhury, X. Liu, Y. Akiyama, J. Ellman, and Y. Ha Conformational change in rhomboid protease GlpG induced by inhibitor binding to its S′ subsites Biochemistry 51 2012 3723 3731
32. Y. Xue, and Y. Ha Catalytic mechanism of rhomboid protease GlpG probed by 3,4-dichloroisocoumarin and diisopropyl fluorophosphonate J. Biol. Chem. 287 2012 3099 3107
33. C.L. Brooks, C. Lazareno-Saez, J.S. Lamoureux, M.W. Mak, and M.J. Lemieux Insights into substrate gating in H. influenzae rhomboid J. Mol. Biol. 407 2011 687 697
34. R.P. Baker, K. Young, L. Feng, Y. Shi, and S. Urban Enzymatic analysis of a rhomboid intramembrane protease implicates transmembrane helix 5 as the lateral substrate gate Proc. Natl. Acad. Sci. U.S.A. 104 2007 8257 8262
35. S. Urban, and M.S. Wolfe Reconstitution of intramembrane proteolysis in vitro reveals that pure rhomboid is sufficient for catalysis and specificity Proc. Natl. Acad. Sci. U.S.A. 102 2005 1883 1888
36. + antiporter of Escherichia coli in the membrane and its functional and structural consequences Biochemistry 40 2001 3403 3412
37. + antiporter NhaA at the dimer interface inhibits antiporter activity Biochem. J. 426 2010 99 108
38. J.M. Salhany, R.L. Sloan, and K.S. Cordes The carboxyl side chain of glutamate 681 interacts with a chloride binding modifier site that allosterically modulates the dimeric conformational state of band 3 (AE1). Implications for the mechanism of anion/proton cotransport Biochemistry 42 2003 1589 1602
39. T.M. Laue, and W.F. Stafford III Modern applications of analytical ultracentrifugation Annu. Rev. Biophys. Biomol. Struct. 28 1999 75 100
40. M.L. Johnson, J.J. Correia, D.A. Yphantis, and H.R. Halvorson Analysis of data from the analytical ultracentrifuge by nonlinear least-squares techniques Biophys. J. 36 1981 575 588
41. T.M. Laue, B.D. Shah, T.M. Ridgeway, and S.L. Pelletier Analytical Ultracentrifugation in Biochemistry and Polymer Science 1991 R. Soc. Chem Cambridge, UK
42. F. Reiss-Husson Crystallization of Membrane Proteins 1991 IRL Press Oxford
43. T.C. Laurent, and J. Killander A theory of gel filtration and its experimental verification J. Chromatogr. 14 1964 303 316
44. M.J. Lemieux, S.J. Fischer, M.M. Cherney, K.S. Bateman, and M.N. James The crystal structure of the rhomboid peptidase from Haemophilus influenzae provides insight into intramembrane proteolysis Proc. Natl. Acad. Sci. U.S.A. 104 2007 750 754
45. M.J. Lemieux, J. Song, M.J. Kim, Y. Huang, A. Villa, M. Auer, X.D. Li, and D.N. Wang Three-dimensional crystallization of the Escherichia coli glycerol-3-phosphate transporter: a member of the major facilitator superfamily Protein Sci. 12 2003 2748 2756
46. R.H. Friesen, J. Knol, and B. Poolman Quaternary structure of the lactose transport protein of Streptococcus thermophilus in the detergent-solubilized and membrane-reconstituted state J. Biol. Chem. 275 2000 33527 33535
47. M.K. Lemberg, and M. Freeman Functional and evolutionary implications of enhanced genomic analysis of rhomboid intramembrane proteases Genome Res. 17 2007 1634 1646
48. M. Auer, M.J. Kim, M.J. Lemieux, A. Villa, J. Song, X.D. Li, and D.N. Wang High-yield expression and functional analysis of Escherichia coli glycerol-3-phosphate transporter Biochemistry 40 2001 6628 6635
49. K. Strisovsky, H.J. Sharpe, and M. Freeman Sequence-specific intramembrane proteolysis: identification of a recognition motif in rhomboid substrates Mol. Cell 36 2009 1048 1059
50. K.R. Vinothkumar Structure of rhomboid protease in a lipid environment J. Mol. Biol. 407 2011 232 247
51. E. Padan, L. Kozachkov, K. Herz, and A. Rimon NhaA crystal structure: functional-structural insights J. Exp. Biol. 212 2009 1593 1603
52. K.A. Williams Three-dimensional structure of the ion-coupled transport protein NhaA Nature 403 2000 112 115
53. + antiporter of E. coli Biophys. J. 89 2005 1328 1338
54. + antiporter and insights into mechanism of action and regulation by pH Nature 435 2005 1197 1202
55. + J. Biol. Chem. 282 2007 26810 26821
56. + antiporter J. Biol. Chem. 284 2009 6337 6347
57. J.M. Salhany Stilbenedisulfonate binding kinetics to band 3 (AE 1): relationship between transport and stilbenedisulfonate binding sites and role of subunit interactions in transport Blood Cells Mol. Dis. 27 2001 127 134
58. X. Lei, K. Ahn, L. Zhu, I. Ubarretxena-Belandia, and Y.M. Li Soluble oligomers of the intramembrane serine protease YqgP are catalytically active in the absence of detergents Biochemistry 47 2008 11920 11929