Substrate specificity of Rhomboid intramembrane proteases is governed by helix-breaking residues in the substrate transmembrane domain

Molecular Cell

Volumn 11, Issue 6, 2003, Pages 1425-1434

  Urban, Sinisa ^a   Freeman, Matthew ^a  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEINASE;

ARTICLE; BACTERIUM; CELL INVASION; DROSOPHILA; ENZYME SPECIFICITY; HOST CELL; HUMAN; MEMBRANE; NONHUMAN; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN MOTIF; PROTEIN TARGETING; TOXOPLASMA GONDII; VERTEBRATE;

BACTERIA (MICROORGANISMS); PROVIDENCIA; TOXOPLASMA GONDII; VERTEBRATA;

EID: 0038771224     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1097-2765(03)00181-3     Document Type: Article

References (38)

1. Arribas J., Lopez-Casillas F., Massagué J. Role of the juxtamembrane domains of the transforming growth factor-alpha precursor and the beta-amyloid precursor protein in regulated ectodomain shedding. J. Biol. Chem. 272:1997;17160-17165.
2. Bang A.G., Kintner C. Rhomboid and Star facilitate presentation and processing of the Drosophila TGF-alpha homolog Spitz. Genes Dev. 14:2000;177-186.
3. Bier E., Jan L.Y., Jan Y.N. rhomboid, a gene required for dorsoventral axis establishment and peripheral nervous system development in Drosophila melanogaster. Genes Dev. 4:1990;190-203.
4. Brown M.S., Ye J., Rawson R.B., Goldstein J.L. Regulated intramembrane proteolysis. a control mechanism conserved from bacteria to humans Cell. 100:2000;391-398.
5. Butcher D.J., Luo Z., Huang Z. The roles of side chain and backbone in protein structure probed with glycine- and sarcosine-rich synthetic leucine zipper peptides. Biochem. Biophys. Res. Commun. 265:1999;350-355.
6. Carruthers V.B., Sherman G.D., Sibley L.D. The Toxoplasma adhesive protein MIC2 is proteolytically processed at multiple sites by two parasite-derived proteases. J. Biol. Chem. 275:2000;14346-14353.
7. Chou P.Y., Fasman G.D. Empirical predictions of protein conformation. Annu. Rev. Biochem. 47:1978;251-276.
8. Gallio M., Sturgill G., Rather P., Kylsten P. A conserved mechanism for extracellular signaling in eukaryotes and prokaryotes. Proc. Natl. Acad. Sci. USA. 99:2002;12208-12213.
9. Ghiglione C., Bach E.A., Paraiso Y., Carraway K.L. 3rd, Noselli S., Perrimon N. Mechanism of activation of the Drosophila EGF Receptor by the TGFalpha ligand Gurken during oogenesis. Development. 129:2002;175-186.
10. Golembo M., Raz E., Shilo B.Z. The Drosophila embryonic midline is the site of Spitz processing, and induces activation of the EGF receptor in the ventral ectoderm. Development. 122:1996;3363-3370.
11. Guichard A., Roark M., Ronshaugen M., Bier E. brother of rhomboid, a rhomboid-related gene expressed during early drosophila oogenesis, promotes EGF-R/MAPK signaling. Dev. Biol. 226:2000;255-266.
12. Jin T., Peng L., Mirshahi T., Rohacs T., Chan K.W., Sanchez R., Logothetis D.E. The (beta)gamma subunits of G proteins gate a K(+) channel by pivoted bending of a transmembrane segment. Mol. Cell. 10:2002;469-481.
13. Lee J.R., Urban S., Garvey C.F., Freeman M. Regulated intracellular ligand transport and proteolysis control EGF signal activation in Drosophila. Cell. 107:2001;161-171.
14. Lemberg M.K., Martoglio B. Requirements for signal peptide peptidase-catalyzed intramembrane proteolysis. Mol. Cell. 10:2002;735-744.
15. Lichtenthaler S.F., Wang R., Grimm H., Uljon S.N., Masters C.L., Beyreuther K. Mechanism of the cleavage specificity of Alzheimer's disease gamma-secretase identified by phenylalanine-scanning mutagenesis of the transmembrane domain of the amyloid precursor protein. Proc. Natl. Acad. Sci. USA. 96:1999;3053-3058.
16. Liu L.P., Deber C.M. Guidelines for membrane protein engineering derived from de novo designed model peptides. Biopolymers. 47:1998;41-62.
17. Luzio J.P., Brake B., Banting G., Howell K.E., Braghetta P., Stanley K.K. Identification, sequencing and expression of an integral membrane protein of the trans-Golgi network (TGN38). Biochem. J. 270:1990;97-102.
18. Mayer U., Nusslein-Volhard C. A group of genes required for pattern formation in the ventral ectoderm of the Drosophila embryo. Genes Dev. 2:1988;1496-1511.
19. Opitz C., Di Cristina M., Reiss M., Ruppert T., Crisanti A., Soldati D. Intramembrane cleavage of microneme proteins at the surface of the apicomplexan parasite Toxoplasma gondii. EMBO J. 21:2002;1577-1585.
20. Pascall J.C., Brown K.D. Characterization of a mammalian cDNA encoding a protein with high sequence similarity to the Drosophila regulatory protein Rhomboid. FEBS Lett. 429:1998;337-340.
21. Perona J.J., Craik C.S. Evolutionary divergence of substrate specificity within the chymotrypsin-like serine protease fold. J. Biol. Chem. 272:1997;29987-29990.
22. Rather P.N., Ding X., Baca-DeLancey R.R., Siddiqui S. 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.
23. Rawson R.B., Zelenski N.G., Nijhawan D., Ye J., Sakai J., Hasan M.T., Chang T.Y., Brown M.S., Goldstein J.L. Complementation cloning of S2P, a gene encoding a putative metalloprotease required for intramembrane cleavage of SREBPs. Mol. Cell. 1:1997;47-57.
24. Reiss M., Viebig N., Brecht S., Fourmaux M.N., Soete M., Di Cristina M., Dubremetz J.F., Soldati D. Identification and characterization of an escorter for two secretory adhesins in Toxoplasma gondii. J. Cell Biol. 152:2001;563-578.
25. Rutledge B.J., Zhang K., Bier E., Jan Y.N., Perrimon N. The Drosophila spitz gene encodes a putative EGF-like growth factor involved in dorsal-ventral axis formation and neurogenesis. Genes Dev. 6:1992;1503-1517.
26. Soldati D., Dubremetz J.F., Lebrun M. Microneme proteins. structural and functional requirements to promote adhesion and invasion by the apicomplexan parasite Toxoplasma gondii Int. J. Parasitol. 31:2001;1293-1302.
27. Struhl G., Adachi A. Requirements for presenilin-dependent cleavage of notch and other transmembrane proteins. Mol. Cell. 6:2000;625-636.
28. Tsruya R., Schlesinger A., Reich A., Gabay L., Sapir A., Shilo B.Z. Intracellular trafficking by Star regulates cleavage of the Drosophila EGF receptor ligand Spitz. Genes Dev. 16:2002;222-234.
29. Ubarretxena-Belandia I., Engelman D.M. Helical membrane proteins. diversity of functions in the context of simple architecture Curr. Opin. Struct. Biol. 11:2001;370-376.
30. Urban S., Freeman M. Intramembrane proteolysis controls diverse signalling pathways throughout evolution. Curr. Opin. Genet. Dev. 12:2002;512-518.
31. Urban S., Lee J.R., Freeman M. Drosophila rhomboid-1 defines a family of putative intramembrane serine proteases. Cell. 107:2001;173-182.
32. Urban S., Lee J.R., Freeman M. A family of Rhomboid intramembrane proteases activates all membrane-tethered EGF ligands in Drosophila. EMBO J. 21:2002;4277-4286. a.
33. Urban S., Schlieper D., Freeman M. Conservation of intramembrane proteolytic activity and substrate specificity in eukaryotic and prokaryotic Rhomboids. Curr. Biol. 12:2002;1507-1512. b.
34. Wasserman J.D., Freeman M. Control of EGF receptor activation in Drosophila. Trends Cell Biol. 7:1997;431-436.
35. Wasserman J.D., Urban S., Freeman M. 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.
36. Weihofen A., Binns K., Lemberg M.K., Ashman K., Martoglio B. Identification of signal peptide peptidase, a presenilin-type aspartic protease. Science. 296:2002;2215-2218.
37. Wolfe M.S., Xia W., Ostaszewski B.L., Diehl T.S., Kimberly W.T., Selkoe D.J. Two transmembrane aspartates in presenilin-1 required for presenilin endoproteolysis and gamma-secretase activity. Nature. 398:1999;513-517.
38. Ye J., Dave U.P., Grishin N.V., Goldstein J.L., Brown M.S. Asparagine-proline sequence within membrane-spanning segment of SREBP triggers intramembrane cleavage by site-2 protease. Proc. Natl. Acad. Sci. USA. 97:2000;5123-5128.