The Processing of Human Rhomboid Intramembrane Serine Protease RHBDL2 Is Required for Its Proteolytic Activity

Journal of Molecular Biology

Volumn 394, Issue 5, 2009, Pages 815-825

  Lei, Xiaojun ^a,b   Li, Yue Ming ^a,b  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b Weill Cornell Graduate School of Biomedical Sciences   (United States)

Author keywords

proenzyme activation; regulated intramembrane proteolysis; rhomboids; serine proteases; signal transduction

Indexed keywords

ARGININE; PROTEIN RHBDL2; SERINE PROTEINASE; SULFONAMIDE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL STRAIN COS1; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME MODIFICATION; ENZYME REGULATION; ENZYME STRUCTURE; ENZYME SYNTHESIS; IMMUNOFLUORESCENCE TEST; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; WESTERN BLOTTING;

EID: 70449642213     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2009.10.025     Document Type: Article

References (31)

1. Freeman M., Kimmel B.E., and Rubin G.M. Identifying targets of the rough homeobox gene of Drosophila: evidence that rhomboid functions in eye development. Development 116 (1992) 335-346
2. Gallio M., Sturgill G., Rather P., and Kylsten P. A conserved mechanism for extracellular signaling in eukaryotes and prokaryotes. Proc. Natl Acad. Sci. USA 99 (2002) 12208-12213
3. Dimmer K.S., Fritz S., Fuchs F., Messerschmitt M., Weinbach N., Neupert W., and Westermann B. Genetic basis of mitochondrial function and morphology in Saccharomyces cerevisiae. Mol. Biol. Cell 13 (2002) 847-853
4. McQuibban G.A., Saurya S., and Freeman M. Mitochondrial membrane remodelling regulated by a conserved rhomboid protease. Nature 423 (2003) 537-541
5. Frezza C., Cipolat S., Martins de Brito O., Micaroni M., Beznoussenko G.V., Rudka T., et al. OPA1 controls apoptotic cristae remodeling independently from mitochondrial fusion. Cell 126 (2006) 177-189
6. Lemberg M.K., Menendez J., Misik A., Garcia M., Koth C.M., and Freeman M. Mechanism of intramembrane proteolysis investigated with purified rhomboid proteases. EMBO J. 24 (2005) 464-472
7. Urban S., and Wolfe M.S. Reconstitution of intramembrane proteolysis in vitro reveals that pure rhomboid is sufficient for catalysis and specificity. Proc. Natl Acad. Sci. USA 102 (2005) 1883-1888
8. Wang Y., Zhang Y., and Ha Y. Crystal structure of a rhomboid family intramembrane protease. Nature 444 (2006) 179-180
9. Wu Z., Yan N., Feng L., Oberstein A., Yan H., Baker R.P., et al. Structural analysis of a rhomboid family intramembrane protease reveals a gating mechanism for substrate entry. Nat. Struct. Mol. Biol. 13 (2006) 1084-1091
10. Ben-Shem A., Fass D., and Bibi E. Structural basis for intramembrane proteolysis by rhomboid serine proteases. Proc. Natl Acad. Sci. USA 104 (2007) 462-466
11. Lemieux M.J., Fischer S.J., Cherney M.M., Bateman K.S., and James M.N. The crystal structure of the rhomboid peptidase from Haemophilus influenzae provides insight into intramembrane proteolysis. Proc. Natl Acad. Sci. USA 104 (2007) 750-754
12. Lei X., Ahn K., Zhu L., Ubarretxena-Belandia I., and Li Y.M. Soluble oligomers of the intramembrane serine protease YqgP are catalytically active in the absence of detergents. Biochemistry 47 (2008) 11920-11929
13. Koonin E.V., Makarova K.S., Rogozin I.B., Davidovic L., Letellier M.C., and Pellegrini L. The rhomboids: a nearly ubiquitous family of intramembrane serine proteases that probably evolved by multiple ancient horizontal gene transfers. Genome Biol. 4 (2003) R19
14. Lee J.R., Urban S., Garvey C.F., and Freeman M. Regulated intracellular ligand transport and proteolysis control EGF signal activation in Drosophila. Cell 107 (2001) 161-171
15. Urban S., Lee J.R., and Freeman M. Drosophila rhomboid-1 defines a family of putative intramembrane serine proteases. Cell 107 (2001) 173-182
16. Pascall J.C., Luck J.E., and Brown K.D. Expression in mammalian cell cultures reveals interdependent, but distinct, functions for Star and Rhomboid proteins in the processing of the Drosophila transforming-growth-factor-alpha homologue Spitz. Biochem. J. 363 (2002) 347-352
17. Tsruya R., Schlesinger A., Reich A., Gabay L., Sapir A., and Shilo B.Z. Intracellular trafficking by Star regulates cleavage of the Drosophila EGF receptor ligand Spitz. Genes Dev. 16 (2002) 222-234
18. Rawson R.B. The SREBP pathway-insights from Insigs and insects. Nat. Rev. Mol. Cell. Biol. 4 (2003) 631-640
19. Tsruya R., Wojtalla A., Carmon S., Yogev S., Reich A., Bibi E., et al. Rhomboid cleaves Star to regulate the levels of secreted Spitz. EMBO J. 26 (2007) 1211-1220
20. Lemberg M.K., and Freeman M. Functional and evolutionary implications of enhanced genomic analysis of rhomboid intramembrane proteases. Genome Res. 17 (2007) 1634-1646
21. Thinakaran G., Borchelt D.R., Lee M.K., Slunt H.H., Spitzer L., Kim G., et al. Endoproteolysis of presenilin 1 and accumulation of processed derivatives in vivo. Neuron 17 (1996) 181-190
22. Lewis S.J., Smith A.L., Neduvelil J.G., Stevenson G.I., Lindon M.J., Jones A.B., et al. A novel series of potent gamma-secretase inhibitors based on a benzobicyclo[4.2.1]nonane core. Bioorg. Med. Chem. Lett. 15 (2005) 373-378
23. Fan X., Matsui W., Khaki L., Stearns D., Chun J., Li Y.M., and Eberhart C.G. Notch pathway inhibition depletes stem-like cells and blocks engraftment in embryonal brain tumors. Cancer Res. 66 (2006) 7445-7452
24. Walsh C. Posttranslational Modification of Proteins: Expanding Nature's Inventory (2006), Roberts and Company Publishers, Englewood, CO
25. Wang Y., Maegawa S., Akiyama Y., and Ha Y. The role of L1 loop in the mechanism of rhomboid intramembrane protease GlpG. J. Mol. Biol. 374 (2007) 1104-1113
26. Del Rio A., Dutta K., Chavez J., Ubarretxena-Belandia I., and Ghose R. Solution structure and dynamics of the N-terminal cytosolic domain of rhomboid intramembrane protease from Pseudomonas aeruginosa: insights into a functional role in intramembrane proteolysis. J. Mol. Biol. 365 (2007) 109-122
27. Shi X.P., Chen E., Yin K.C., Na S., Garsky V.M., Lai M.T., et al. The pro domain of beta-secretase does not confer strict zymogen-like properties but does assist proper folding of the protease domain. J. Biol. Chem. 276 (2001) 10366-10373
28. Silen J.L., Frank D., Fujishige A., Bone R., and Agard D.A. Analysis of prepro-alpha-lytic protease expression in Escherichia coli reveals that the pro region is required for activity. J. Bacteriol. 171 (1989) 1320-1325
29. Eder J., Rheinnecker M., and Fersht A.R. Folding of subtilisin BPN′: characterization of a folding intermediate. Biochemistry 32 (1993) 18-26
30. Wolfe M.S., Xia W., Ostaszewski B.L., Diehl T.S., Kimberly W.T., and Selkoe D.J. Two transmembrane aspartates in presenilin-1 required for presenilin endoproteolysis and gamma-secretase activity. Nature 398 (1999) 513-517
31. Li Y.M., Xu M., Lai M.T., Huang Q., Castro J.L., DiMuzio-Mower J., et al. Photoactivated gamma-secretase inhibitors directed to the active site covalently label presenilin 1. Nature 405 (2000) 689-694