Structural analysis of a rhomboid family intramembrane protease reveals a gating mechanism for substrate entry (original) (raw)

• Brown, M.S., Ye, J., Rawson, R.B. & Goldstein, J.L. Regulated intramembrane proteolysis: a control mechanism conserved from bacteria to humans. Cell 100, 391–398 (2000).
  Article CAS Google Scholar
• Urban, S. & Freeman, M. Intramembrane proteolysis controls diverse signalling pathways throughout evolution. Curr. Opin. Genet. Dev. 12, 512–518 (2002).
  Article CAS Google Scholar
• Wolfe, M.S. & Kopan, R. Intramembrane proteolysis: theme and variations. Science 305, 1119–1123 (2004).
  Article CAS Google Scholar
• Ebinu, J.O. & Yankner, B.A.A. RIP tide in neuronal signal transduction. Neuron 34, 499–502 (2002).
  Article CAS Google Scholar
• Ehrmann, M. & Clausen, T. Proteolysis as a regulatory mechanism. Annu. Rev. Genet. 38, 709–724 (2004).
  Article CAS Google Scholar
• Rawson, R.B. Regulated intramembrane proteolysis: from the endoplasmic reticulum to the nucleus. Essays Biochem. 38, 155–168 (2002).
  Article CAS Google Scholar
• Brown, M.S. & Goldstein, J.L. The SREBP pathway: regulation of cholesterol metabolism by proteolysis of a membrane-bound transcription factor. Cell 89, 331–340 (1997).
  Article CAS Google Scholar
• Rawson, R.B. Complementation cloning of S2P, a gene encoding a putative metalloprotease required for intramembrane cleavage of SREBPs. Mol. Cell 1, 47–57 (1997).
  Article CAS Google Scholar
• Mattson, M.P. Pathways towards and away from Alzheimer's disease. Nature 430, 631–639 (2004).
  Article CAS Google Scholar
• Xia, W. & Wolfe, M.S. Intramembrane proteolysis by presenilin and presenilin-like proteases. J. Cell Sci. 116, 2839–2844 (2003).
  Article CAS Google Scholar
• Urban, S., Lee, J.R. & Freeman, M. Drosophila rhomboid-1 defines a family of putative intramembrane serine proteases. Cell 107, 173–182 (2001).
  Article CAS Google Scholar
• Urban, S., Lee, J.R. & Freeman, M. A family of Rhomboid intramembrane proteases activates all Drosophila membrane-tethered EGF ligands. EMBO J. 21, 4277–4286 (2002).
  Article CAS Google Scholar
• 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, 1651–1663 (2000).
  CAS PubMed PubMed Central Google Scholar
• Lee, J.R., Urban, S., Garvey, C. & Freeman, M. Regulated intracellular ligand transport and proteolysis control EGF signal activation in Drosophila. Cell 107, 161–171 (2001).
  Article CAS Google Scholar
• Cipolat, S. et al. Mitochondrial rhomboid PARL regulates cytochrome c release during apoptosis via OPA1-dependent cristae remodeling. Cell 126, 163–175 (2006).
  Article CAS Google Scholar
• Pellegrini, L. et al. PAMP and PARL, two novel putative metalloproteases interacting with the COOH-terminus of Presenilin-1 and -2. J. Alzheimers Dis. 3, 181–190 (2001).
  Article CAS Google Scholar
• Ishihara, N., Fujita, Y., Oka, T. & Mihara, K. Regulation of mitochondrial morphology through proteolytic cleavage of OPA1. EMBO J. 25, 2966–2977 (2006).
  Article CAS Google Scholar
• McQuibban, G.A., Saurya, S. & Freeman, M. Mitochondrial membrane remodelling regulated by a conserved rhomboid protease. Nature 423, 537–541 (2003).
  Article CAS Google Scholar
• Brossier, F., Jewett, T.J., Sibley, L.D. & Urban, S. A spatially localized rhomboid protease cleaves cell surface adhesins essential for invasion by Toxoplasma. Proc. Natl. Acad. Sci. USA 102, 4146–4151 (2005).
  Article CAS Google Scholar
• Gallio, M., Sturgill, G., Rather, P. & Kylsten, P. A conserved mechanism for extracellular signaling in eukaryotes and prokaryotes. Proc. Natl. Acad. Sci. USA 99, 12208–12213 (2002).
  Article CAS Google Scholar
• Maegawa, S., Ito, K. & Akiyama, Y. Proteolytic action of GlpG, a rhomboid protease in the Escherichia coli cytoplasmic membrane. Biochemistry 44, 13543–13552 (2005).
  Article CAS Google Scholar
• Lemberg, M.K. et al. Mechanism of intramembrane proteolysis investigated with purified rhomboid proteases. EMBO J. 24, 464–472 (2005).
  Article CAS Google Scholar
• Urban, S. & 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, 1883–1888 (2005).
  Article CAS Google Scholar
• Wang, Y., Zhang, Y. & Ha, Y. Crystal structure of a rhomboid family intramembrane protease. Nature, advance online publication 11 October 2006 (doi:10.1038/nature05255).
• Koonin, E.V. et al. The rhomboids: a nearly ubiquitous family of intramembrane serine proteases that probably evolved by multiple ancient horizontal gene transfers. Genome Biol. 4, R19 (2003).
  Article Google Scholar
• Daley, D.O. et al. Global topology analysis of the Escherichia coli inner membrane proteome. Science 308, 1321–1323 (2005).
  Article CAS Google Scholar
• O'Donnell, R.A. et al. Intramembrane proteolysis mediates shedding of a key adhesin during erythrocyte invasion by the malaria parasite. J. Cell Biol. 174, 1023–1033 (2006).
  Article CAS Google Scholar
• Zhou, X.W., Blackman, M.J., Howell, S.A. & Carruthers, V.B. Proteomic analysis of cleavage events reveals a dynamic two-step mechanism for proteolysis of a key parasite adhesive complex. Mol. Cell. Proteomics 3, 565–576 (2004).
  Article CAS Google Scholar
• Opitz, C. et al. Intramembrane cleavage of microneme proteins at the surface of the apicomplexan parasite Toxoplasma gondii. EMBO J. 21, 1577–1585 (2002).
  Article CAS Google Scholar
• Urban, S. & Freeman, M. Substrate specificity of rhomboid intramembrane proteases is governed by helix-breaking residues in the substrate transmembrane domain. Mol. Cell 11, 1425–1434 (2003).
  Article CAS Google Scholar
• Howell, S.A. et al. Distinct mechanisms govern proteolytic shedding of a key invasion protein in apicomplexan pathogens. Mol. Microbiol. 57, 1342–1356 (2005).
  Article CAS Google Scholar
• van den Berg, B. et al. X-ray structure of a protein-conducting channel. Nature 427, 36–44 (2004).
  Article CAS Google Scholar
• Lazarov, V.K. et al. Electron microscopic structure of purified, active gamma-secretase reveals an aqueous intramembrane chamber and two pores. Proc. Natl. Acad. Sci. USA 103, 6889–6894 (2006).
  Article CAS Google Scholar
• Ogura, T. et al. Three-dimensional structure of the gamma-secretase complex. Biochem. Biophys. Res. Commun. 343, 525–534 (2006).
  Article CAS Google Scholar
• Otwinowski, Z. & Minor, W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307–326 (1997).
  Article CAS Google Scholar
• McCoy, A.J., Grosse-Kunstleve, R.W., Storoni, L.C. & Read, R.J. Likelihood-enhanced fast translation functions. Acta Crystallogr. D Biol. Crystallogr. 61, 458–464 (2005).
  Article Google Scholar
• Jones, T.A., Zou, J.-Y., Cowan, S.W. & Kjeldgaard, M. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A 47, 110–119 (1991).
  Article Google Scholar
• Brunger, A.T. et al. Crystallography and NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 54, 905–921 (1998).
  Article CAS Google Scholar
• Chen, F. et al. Translocation of C. elegans CED-4 to nuclear membranes during programmed cell death. Science 287, 1485–1489 (2000).
  Article CAS Google Scholar
• Nicholls, A., Sharp, K.A. & Honig, B. Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins Struct. Funct. Genet. 11, 281–296 (1991).
  Article CAS Google Scholar
• Kraulis, P.J. Molscript: a program to produce both detailed and schematic plots of protein structures. J. Appl. Cryst. 24, 946–950 (1991).
  Article Google Scholar