Polytopic membrane protein folding and assembly in vitro and in vivo (Review)

References

• Booth, P. J., Templer, R. H., Meijberg, J. W., Allen, S. J., Lorch, M.and Curran, A.R., 2001, In vitro studies of membrane protein folding. Crit. Rev. Biochem. Mol. Biol, 36, 501 –603.
   Web of Science ®Google Scholar
• Huang, K.-S., Bayley, H., Liao, M.-J., London, E. and Khorana, H.G., 1981, Refolding of an integral membrane protein. Denaturation, renaturation and reconstitution of intact bacter- iorhodopsin and two proteolytic fragments. J. Biol. Chem., 256, 3802 -3809.
   PubMed Web of Science ®Google Scholar
• London, E.and Khorana, H.G., 1982, Denaturation and renaturation of bacteriorhodopsin in detergents and lipid-deter- gent mixtures. J. Biol. Chem., 257, 7003 -7011.
   Google Scholar
• Paulsen, H., Finkenzeller, B. and Ku¨ hlein, N., 1993, Pigments induce folding of light-harvesting chlorophyll a/b-binding protein. Eur. J. Biochem., 215, 809 –817.
   Google Scholar
• Booth, P.J. and Paulsen, H., 1996, Assembly of the light harvesting chlorophyll a/b complex in vitro .Time-resolved fluorescence measurements. Biochemistry, 35, 5103 -5108.
   Google Scholar
• Sanders, C. R., II and Landis, G. C., 1995, Reconstitution of membrane proteins into lipid-rich bilayered mixed micelles for NMR studies. Biochemistry, 34, 4030 -4040.
   Google Scholar
• Gorzelle, B. M., Nagy, J. K., Oxenoid, K., Lonzer, W. L., Cafiso, D.S. and Sanders, C. R., 1999, Reconstitutive refolding of diacylglycerol kinase, an integral membrane protein. Biochem- istry, 38, 16373–16382.
   Google Scholar
• Yerushalmi, H., Lebendiker, M. and Schuldiner, S., 1995, EmrE, an Escherichia coli 12-kDa multidrug transporter, exchanges toxic cations and H+ and is soluble in organic solvents. J. Biol. Chem., 270, 6856–6863.
   PubMed Web of Science ®Google Scholar
• Valiyaveetil, F. I., MacKinnon, R. and Muir, T. W., 2002, Semisynthesis and folding of the potassium channel KcsA. J. Am. Chem. Soc., 124, 9113 -9120.
   PubMedGoogle Scholar
• Valiyaveetil, F. I., Zhou, Y. and MacKinnon, R., 2002, Lipids in the structure, folding, and function of the KcsA K+ channel. Biochemistry, 41, 10771–10777.
   PubMed Web of Science ®Google Scholar
• Otzen, D., 2003, Folding of DsbB in mixed micelles: a kinetic analysis of the stability of a bacterial membrane protein. J. Mol. Biol., 330, 641 –649.
   Google Scholar
• Baneres, J.-L., Martin, A., Hullot, P., Girard, J.-P., Rossi, J.-C. and Parello, J., 2003, Structure-based analysis of GPCR function: conformational adaptation of both agonist and receptor upon leukotriene B4 binding to recombinant BLT1. J. Mol. Biol., 329, 801 –814.
   PubMed Web of Science ®Google Scholar
• Booth, P. J., Flitsch, S. L., Stern, L. J., Greenhalgh, D. A., Kim, P.S.and Khorana, H.G., 1995, Intermediates in the folding of the membrane protein bacteriorhodopsin. Nat. Struct. Biol., 2, 139 –143.
   Google Scholar
• Booth, P.J., Farooq, A. and Flitsch, S.L., 1996, Retinal binding during folding and assembly of the membrane protein bacter- iorhodopsin. Biochemistry, 35, 5902 -5909.
   Google Scholar
• Lau, F.W. and Bowie, J. U., 1997, A method for assessing the stability of a membrane protein. Biochemistry, 36, 5884 -5892.
   PubMed Web of Science ®Google Scholar
• Bowie, J.U., 2001, Stabilizing membrane proteins. Curr. Opin.Struct. Biol., 11, 397 –402.
   PubMed Web of Science ®Google Scholar
• Fyfe, P. K., McAuley, K. E., Roszak, A. W., Isaacs, N. W., Cogdell, R.J.and Jones, M. R., 2001, Probing the interface between membrane proteins and membrane lipids by X-ray crystallography. Trends Biochem. Sci., 26, 106 –112.
   PubMed Web of Science ®Google Scholar
• Meijberg, W.and Booth, P.J., 2002, The activation energy for insertion of transmembrane alpha-helices is dependent on membrane composition. J. Mol. Biol., 319, 839 –853.
   PubMed Web of Science ®Google Scholar
• White, S.H., 2003, Translocons, thermodynamics, and the folding of membrane proteins. FEBS Lett., 555, 116 –121.
   PubMed Web of Science ®Google Scholar
• Engelman, D. M., Chen, Y., Chin, C. N., Curran, A. R., Dixon, A.M., Dupuy, A. D., Lee, A. S., Lehnert, U., Matthews, E. E., Reshetnyak, Y.K., Senes, A.and Popot, J.L., 2003, Membrane protein folding: beyond the two stage model. FEBS Lett., 555, 122 –125.
   PubMed Web of Science ®Google Scholar
• Popot, J.-L. and Engelman, D. M., 1990, Membrane protein folding and oligomerization: the two stage model. Biochemistry, 29, 4031–4037.
   PubMed Web of Science ®Google Scholar
• Ridge, K., Lee, S. and Yao, L., 1995, In vivo assembly of rhodopsin from expressed polypeptide fragments. Proc. Natl Acad. Sci., 92, 3204 -3208.
   Google Scholar
• Lemmon, M.A.and Engelman, D. M., 1994, Specificity and promiscuity in membrane helix interactions. Quart. Rev. Bio- phys., 27, 157 –218.
   PubMed Web of Science ®Google Scholar
• Allen, S. J., Kim, J.-M., Khorana, H. G., Lu, H. and Booth, P. J., 2001, Structure and function in bacteriorhodopsin: the role of the interhelical loops in folding and stability of bacteriorhodop- sin. J. Mol. Biol., 308, 423 –435.
   Google Scholar
• Kim, J.-M., Booth, P. J., Allen, S. J. and Khorana, H. G., 2001, Structure and function in bacteriorhodopsin: the role of the interhelical loops in the folding and stability of bacteriorhodop- sin. J. Mol. Biol., 308, 409 –422.
   Google Scholar
• MacKenzie, K. R., Prestegard, J. H. and Engelman, D. M., 1997, A transmembrane helix dimer: structure and implications. Science, 276, 131 –133.
   PubMed Web of Science ®Google Scholar
• Senes, A., Gerstein, M. and Engelman, D. M., 2000, Statistical analysis of amino acid patterns in transmembrane helices: the GxxxG motif occurs frequently and in association with b-branched residues at neighbouring positions. J. Mol. Biol. ,296, 921 –936.
   PubMed Web of Science ®Google Scholar
• Russ, W.P. and Engelman, D.M., 2000, The GxxxG motif: a framework for transmembrane helix-helix association. J. Mol. Biol., 296, 911 –919.
   PubMed Web of Science ®Google Scholar
• Karnik, S.S.and Khorana, H. G., 1990, Assembly of functional rhodopsin requires a disulfide bond between cysteine residues 110 and 187. J. Biol. Chem., 265, 17520–17524.
   PubMed Web of Science ®Google Scholar
• Kaushel, S.and Khorana, H.G., 1994, Structure and function in rhodopsin.7.Point mutations associated with autosomal dominant retinitis pigmentosa. Biochemistry, 33, 6121 -6128.
   Google Scholar
• Karnik, S. S., Sakmar, T. P., Chen, H. B. and Khorana, H. G., 1998, Cysteine residues 110 and 187 are essential for the formation of correct structure in bovine rhodopsin. Proc. Natl Acad. Sci. USA, 85, 8459 -8463.
   Google Scholar
• Hwa, J., Reeves, P., Klein-Seetharaman, J., Davidson, F. and Khorana, H., 1999, Structure and function in rhodopsin: further elucidation of the role of the intra-discal cysteines, Cys-110, - 185 and -187 in rhodopsin folding and function. Proc. Natl Acad. Sci. USA, 96, 1932 –1935.
   Google Scholar
• Hwa, J., Garriga, P., Liu, X. and Khorana, H. G., 1997, Structure and function in rhodopsin: packing of the helices in the transmembrane domain and folding to a tertiary structure in the intra-discal domain are coupled. Proc. Natl Acad. Sci. USA, 94, 10571–10576.
   PubMed Web of Science ®Google Scholar
• Stojanovic, A., Hwang, I., Khorana, H. G. and Hwa, J., 2003, Retinitis pigmentosa rhodopsin mutations L125R and A164V perturb critical interhelical interactions: new insights through compensatory mutations and crystal structure analysis. J. Biol. Chem., 278, 39020–39028.
   Google Scholar
• Partridge, A.W., Therien, A.G.and Deber, C.M., 2002, Polar mutations in membrane proteins as a biophysical basis for disease. Biopolymers, 66, 350 –358.
   PubMed Web of Science ®Google Scholar
• Curran, A.R.and Engelman, D.M., 2003, Sequence motifs, polar interactions and conformational changes in helical mem- brane proteins. Curr. Opin. Struct. Biol., 13, 412 –417.
   PubMed Web of Science ®Google Scholar
• Therien, A. G., Grant, F. E. and Deber, C. M., 2001, Interhelical hydrogen bonds in the CFTR membrane domain. Nat. Struct. Biol., 8, 597 –601.
   Google Scholar
• Laird, V.and High, S., 1997, Discrete cross-linking products identified during membrane protein biosynthesis. J. Biol. Chem., 272, 1983 –1989.
   Google Scholar
• Lecomte, F. J., Ismail, N. and High, S., 2003, Making membrane proteins at the mammalian endoplasmic reticulum. Biochem. Soc. Trans., 31, 1248 -1252.
   Google Scholar
• van den Berg, B., Clemons, W. M., Jr, Collinson, I., Modis, Y., Hartmann, E., Harrison, S. C. and Rapoport, T. A., 2004, X-ray structure of a protein-conducting channel. Nature, 427, 36 –44.
   PubMed Web of Science ®Google Scholar
• Dobberstein, B.and Sinning, I., 2004, Structural biology.Surprising news from the PCC. Science, 303, 320 –322.
   Google Scholar
• Le Gall, S., Neuhof, A. and Rapoport, T., 2004, The endoplas- mic reticulum membrane is permeable to small molecules. Mol. Biol. Cell., 15, 447 –455.
   PubMed Web of Science ®Google Scholar
• Heinrich, S.U.and Rapoport, T.A., 2003, Cooperation of transmembrane segments during the integration of a double- spanning protein into the ER membrane. EMBO J., 22, 3654- 3663.
   PubMedGoogle Scholar
• Meacock, S. L., Lecomte, F. J., Crawshaw, S. G. and High, S., 2002, Different transmembrane domains associate with distinct endoplasmic reticulum components during membrane integra- tion of a polytopic protein. Mol. Biol. Cell, 13, 4114 -4129.
   Google Scholar
• Mothes, W., Heinrich, S. U., Graf, R., Nilsson, I., von Heijne, G., Brunner, J.and Rapoport, T. A., 1997, Molecular mechanism of membrane protein integration into the endoplasmic reticulum. Cell, 89, 523 –533.
   Google Scholar
• Heinrich, S. U., Mothes, W., Brunner, J. and Rapoport, T. A., 2000, The Sec61p complex mediates the integration of a membrane protein by allowing lipid partitioning of the trans- membrane domain. Cell, 102, 233 –244.
   PubMedGoogle Scholar
• High, S.and Laird, V., 1997, Membrane protein biosynthesis * all sewn up? Trends Cell Biol., 7, 206 -210.
   Google Scholar
• McCormick, P. J., Miao, Y., Shao, Y., Lin, J. and Johnson, A. E., 2003, Cotranslational protein integration into the ER membraneis mediated by the binding of nascent chains to translocon proteins. Mol. Cell, 12, 329 –341.
   PubMed Web of Science ®Google Scholar
• Kopito, R.R., 1999, Biosynthesis and degradation of CFTR. Physiol. Rev, 79, S167–173.
   PubMed Web of Science ®Google Scholar
• Loo, M. A., Jensen, T. J., Cui, L., Hou, Y., Chang, X. B. and Riordan, J.R., 1998, Perturbation of Hsp90 interaction with nascent CFTR prevents its maturation and accelerates its degradation by the proteasome. EMBO J., 17, 6879 -6887.
   PubMed Web of Science ®Google Scholar
• Meacham, G. C., Lu, Z., King, S., Sorscher, E., Tousson, A. and Cyr, D.M., 1999, The Hdj-2/Hsc70 chaperone pair facilitates early steps in CFTR biogenesis. EMBO J., 18, 1492 -1505.
   PubMed Web of Science ®Google Scholar
• Chapple, J.P.and Cheetham, M. E., 2003, The chaperone environment at the cytoplasmic face of the endoplasmic reticulum can modulate rhodopsin processing and inclusion formation. J. Biol. Chem., 278, 19087–19094.
   PubMed Web of Science ®Google Scholar
• Swanton, E., High, S. and Woodman, P., 2003, Role of calnexin in the glycan-independent quality control of proteolipid protein. EMBO J., 22, 2948 -2958.
   Google Scholar
• Rutishauser, J.and Spiess, M., 2002, Endoplasmic reticulum storage diseases. Swiss Med. Wkly, 132, 211 –222.
   Web of Science ®Google Scholar
• Ellgaard, L.and Helenius, A., 2003, Quality control in the endoplasmic reticulum. Nat. Rev. Mol. Cell Biol., 4, 181 –191.
   PubMed Web of Science ®Google Scholar
• Tector, M.and Hartl, F. U., 1999, An unstable transmembrane segment in the cystic fibrosis transmembrane conductance regulator. EMBO J., 18, 6290 -6298.
   Google Scholar
• Ellgaard, L., Molinari, M. and Helenius, A., 1999, Setting the standards: quality control in the secretory pathway. Science, 286, 1882 –1888.
   PubMed Web of Science ®Google Scholar
• High, S., Lecomte, F. J., Russell, S. J., Abell, B. M. and Oliver, J.D., 2000, Glycoprotein folding in the endoplasmic reticulum: a tale of three chaperones? FEBS Lett., 476, 38 –41.
   PubMed Web of Science ®Google Scholar
• Schrag, J. D., Procopio, D. O., Cygler, M., Thomas, D. Y. and Bergeron, J.J., 2003, Lectin control of protein folding and sorting in the secretory pathway. Trends Biochem. Sci., 28, 49 – 57.
   PubMed Web of Science ®Google Scholar
• Wang, T.and Hebert, D.N., 2003, EDEM an ER quality control receptor. Nat. Struct. Biol., 10, 319 –321.
   PubMedGoogle Scholar
• Landolt-Marticorena, C.and Reithmeier, R. A., 1994, Aspar- agine-linked oligosaccharides are localized to single extracyto- solic segments in multi-span membrane glycoproteins. Biochem. J., 302, 253 –260.
   PubMedGoogle Scholar
• Daniels, R., Kurowski, B., Johnson, A. E. and Hebert, D. N., 2003, N-linked glycans direct the cotranslational folding path- way of influenza hemagglutinin. Mol. Cell, 11, 79 –90.
   PubMed Web of Science ®Google Scholar
• Wang, Q.and Chang, A., 2003, Substrate recognition in ER- associated degradation mediated by Eps1, a member of the protein disulfide isomerase family. EMBO J., 22, 3792 -3802.
   Google Scholar
• Tsai, B., Ye, Y. and Rapoport, T. A., 2002, Retro-translocation of proteins from the endoplasmic reticulum into the cytosol. Nat. Rev. Mol. Cell Biol., 3, 246 –255.
   PubMed Web of Science ®Google Scholar
• Ye, Y., Meyer, H. H. and Rapoport, T. A., 2001, The AAAATPase Cdc48/p97 and its partners transport proteins from the ER into the cytosol. Nature, 414, 652 –656.
   PubMed Web of Science ®Google Scholar
• Wiertz, E. J., Tortorella, D., Bogyo, M., Yu, J., Mothes, W., Jones, T.R., Rapoport, T.A.and Ploegh, H.L., 1996, Sec61- mediated transfer of a membrane protein from the endoplasmic reticulum to the proteasome for destruction. Nature, 384, 432 – 438.
   Google Scholar
• VanSlyke, J.K.and Musil, L.S., 2002, Dislocation and degradation from the ER are regulated by cytosolic stress. J. Cell. Biol., 157, 381 –394.
   PubMed Web of Science ®Google Scholar
• Romisch, K., 1999, Surfing the Sec61 channel: bidirectionalprotein translocation across the ER membrane. J. Cell. Sci. ,112, 4185–4191.
   PubMedGoogle Scholar
• McCracken, A.A. and Brodsky, J.L., 2003, Evolving questions and paradigm shifts in endoplasmic-reticulum-associated de- gradation (ERAD). Bioessays, 25, 868 –877.
   Web of Science ®Google Scholar
• Haynes, C.M., Caldwell, S.and Cooper, A.A., 2002, An HRD/DER-independent ER quality control mechanism involves Rsp5p-dependent ubiquitination and ER-Golgi transport. J. Cell Biol., 158, 91 –101.
   PubMed Web of Science ®Google Scholar
• Fayadat, L.and Kopito, R.R., 2003, Recognition of a single transmembrane degron by sequential quality control check- points. Mol. Biol. Cell, 14, 1268 –1278.
   Google Scholar
• Illing, M. E., Rajan, R.S., Bence, N.F.and Kopito, R.R., 2002, A rhodopsin mutant linked to autosomal dominant retinitis pigmentosa is prone to aggregate and interacts with the ubiquitin proteasome system. J. Biol. Chem., 277, 34150 – 34160.
   Google Scholar
• Kopito, R.R.and Sitia, R., 2000, Aggresomes and Russell bodies.Symptoms of cellular indigestion? EMBO Rep., 1, 225 – 231.
   Google Scholar
• Wigley, W. C., Corboy, M. J., Cutler, T. D., Thibodeau, P. H.,Oldan, J., Lee, M. G., Rizo, J., Hunt, J. F. and Thomas, P. J., 2002, A protein sequence that can encode native structure by disfavoring alternate conformations. Nat. Struct. Biol., 9, 381 – 388.
   PubMedGoogle Scholar