Recent advances in the understanding of membrane protein assembly and structure

Quarterly Reviews of Biophysics

Volumn 32, Issue 4, 1999, Pages 285-307

  Von Heijne, Gunnar ^a  

^a STOCKHOLM UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIORHODOPSIN; DOCKING PROTEIN; FUMARATE REDUCTASE; GLYCOPHORIN A; ION CHANNEL; MEMBRANE PROTEIN; PROLINE; TRANSACTIVATOR PROTEIN; UBIQUINOL CYTOCHROME C REDUCTASE;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; CARBOXY TERMINAL SEQUENCE; CELL MEMBRANE; ENDOPLASMIC RETICULUM; ESCHERICHIA COLI; GENE SEQUENCE; GENE TRANSLOCATION; GENOME; HUMAN; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEIN TERTIARY STRUCTURE; REVIEW; SEQUENCE HOMOLOGY;

ANIMALS; BACTERIAL PROTEINS; BIOPHYSICS; ENDOPLASMIC RETICULUM; ESCHERICHIA COLI; EVOLUTION; GENOME; MEMBRANE PROTEINS; MITOCHONDRIA; PROTEIN STRUCTURE, SECONDARY;

ESCHERICHIA COLI;

EID: 0033342531     PISSN: 00335835     EISSN: None     Source Type: Journal    
DOI: 10.1017/S0033583500003541     Document Type: Review

References (153)

1. ADAM, A., et al. (1999). Tim9, a new component of the TIM22/54 translocase in mitochondria. EMBO J. 18, 313-319.
2. ANDREWS, D. W. et al. (1992). The role of the N-region in signal sequence and signal-anchor function. J. biol. Chem. 267, 7761-7769.
3. ARMULIK, A. et al. (1999). Determination of the border between transmembrane and cytoplasmic domains of human integrin subunits. J. biol. Chem. 274, 37030-37034.
4. BERKS, B. C. (1996). A common export pathway for proteins binding complex redox cofactors? Mol. Microbiol. 22, 393-404.
5. BERNSTEIN, H. (1998). Membrane protein biogenesis: the exception explains the rules. Proc. natn. Acad. Sci. USA 95, 14587-14589.
6. BIBI, E. (1998). The role of the ribosome-translocon complex in translation and assembly of polytopic membrane proteins. Trends biochem. Sci. 23, 51-55.
7. BOGSCH, E. G. et al. (1998). An essential component of a novel bacterial protein export system with homologues in plastids and mitochondria. J. biol. Chem. 272, 18003-18006.
8. BOOTH, P. J. (1997). Folding α-helical membrane proteins: kinetic studies on bacteriorhodopsin. Fold Des. 2, R85-R92.
9. BOOTH, P. J. et al. (1995). Intermediates in the folding of the membrane protein bacteriorhodopsin. Nature struct. Biol. 2, 139-143.
10. BOOTH, P. J. et al. (1997). Evidence that bilayer bending rigidity affects membrane protein folding. Biochemistry 36, 197-203.
11. BOREL, A. C. & SIMON, S. M. (1996). Biogenesis of polytopic membrane proteins: membrane segments assemble with translocation channels prior to membrane integration. Cell 85, 378-389.
12. BORMANN, B. J. & ENGELMAN, D. M. (1992). Intramembrane helix-helix association in oligomerization and transmembrane signaling. A. Rev. Biophys. biomol. Struc. 21, 223-242.
13. BOWIE, J. U. (1997). Helix packing in membrane proteins. J. mol. Biol. 272, 780-789.
14. BRAUN, P. & VON HEIJNF, G. (1999). The aromatic residues Trp and Phe have different effects on the positioning of a transmembrane helix in the microsomal membrane. Biochemistry 38, 9778- 9782.
15. BROOME-SMITH, J. K. et al. (1994). Cleavable signal peptides are rarely found in bacterial cytoplasmic membrane proteins. Mol. Membr. Biol. 11, 3-8.
16. BROSIG, B. & LANGOSCH, D. (1998). The dimerization motif of the glycophorin A transmembrane segment in membranes: importance of glycine residues. Protein Sci. 7, 1052-1056.
17. BRUSS, V. et al. (1994). Post-translational alterations in transmembrane topology of the hepatitis B virus large envelope protein. EMBO J. 13, 2273-2279.
18. BUCHANAN, S. K. (1999). β-barrel proteins from bacterial outer membranes : structure, function and refolding. Curr. Opin. struct. Biol. 9, 455-461.
19. CHADDOCK, A. M. et al. (1995). A new type of signal peptide: central role of a twin-arginine motif in transfer signals for the ApH-dependent thylakoidal protein translocase. EMBO J. 14, 2715-2722.
20. CHANG, G. et al. (1998). Structure of the MscL homolog from Mycobacterium tuberculosis: a gated mechano-sensitive ion channel. Science 282, 2220-2226.
21. CHEN, M. G. & ZHANG, J. T. (1999). Topogenesis of cystic fibrosis transmembrane conductance regulator (CFTR): regulation by the amino terminal transmembrane sequences. Biochemistry 38, 5471-5477.
22. CLAROS, M. G. & VON HEIJNE, G. (1994). TopPred II: An improved software for membrane protein structure prediction. CABIOS 10, 685-686.
23. COWAN, S. W. & ROSENBUSCH, J. P. (1994). Folding pattern diversity of integral membrane proteins. Science 264, 914-916.
24. CREIGHTON, A. M. et al. (1995). A monomeric, tightly folded stromal intermediate on the Delta pH-dependent thylakoidal protein transport pathway. J. biol. Chem. 270, 1663-1669.
25. CRISTOBAL, S. et al. (1999). Competition between Sec-and TAT-dependent protein translocation in Escherichia coli. Embo J. 18, 2982-2990.
26. CRISTOBAL, S. et al. (1999b). The signal recognition particle-targeting pathway does not necessarily deliver proteins to the Sec-translocase in Escherichia coli. J. biol. Chem. 274, 20068-20070.
27. CROWLEY, K. S. et al. (1993). The signal sequence moves through a ribosomal tunnel into a noncytoplasmic aqueous environment at the ER membrane early in translocation. Cell 73, 1101-1115.
28. CROWLEY, K. S. et al. (1994). Secretory proteins move through the endoplasmic reticulum membrane via an aqueous, gated pore. Cell 78, 461-471.
29. CURRAN, A. R. et al. (1999). Modulation of folding and assembly of the membrane protein bacteriorhodopsin by intermolecular forces within the lipid bilayer. Biochemistry 38, 9328-9336.
30. DALBEY, R. D. et al. (1995). Directionality in protein translocation across membranes : The N-tail phenomenon. Trends Cell Biol. 5, 380-383.
31. DE FEA, K. A. et al. (1994). Determinants of carboxyl-terminal domain translocation during prion protein biogenesis. J. biol. Chem. 269, 16810-16820.
32. DE GIER, J.-W. L. et al. (1996). Assembly of a cytoplasmic membrane protein in Escherichia coli is dependent on the signal recognition particle. FEBS Lett. 399, 307-309.
33. DE GIER, J.-W. L. et al. (1997). The E. coli SRP: preferences of a targeting factor. FEBS Lett. 408, 1-4.
34. DE GIER, J. et al. (1998). Differential use of the signal recognition particle translocase targeting pathway for inner membrane protein assembly in Escherichia coli. Proc. natn. Acad. Sci. USA 95. 14646-14651.
35. DE PLANQUE, M. R. et al. (1999). Different membrane anchoring positions of tryptophan and lysine in synthetic transmembrane alpha-helical peptides. J. biol. Chem. 274, 20839-20846.
36. DEVOTO, A. et al. (1999). Topology, subcellular localization, and sequence diversity of the m1o family in plants [In Process Citation]. J. biol. Chem. 274, 34993-35004.
37. Do, H. et al. (1996). The cotransational integration of membrane proteins into the phospholipid bilayer is a multistep process. Cell 85, 369-378.
38. + conduction and sensitivity. Science 280, 69-77.
39. DUNLOP, J. et al. (1995). Membrane insertion and assembly of ductin: a polytopic channel with dual orientations. EMBO J. 14, 3609-3616.
40. EDMAN, K. et al. (1999). High-resolution X-ray structure of an early intermediate in the bacteriorhodopsin photocycle. Nature 401, 822-826.
41. ENDRES, M. et al. (1999). Transport of the ADP-ATP carrier of mitochondria from the TOM complex to the TIM22.54 complex. EMBO J. 18, 3214-3221.
42. FALCONE, D. et al. (1999). Negatively charged residues in the IgM stop-transfer effector sequence regulate transmembrane polypeptide integration. J. biol. Chem. 274, 33661-33670.
43. FEKKES, P. & DRIESSEN, A. (1999). Protein targeting to the bacterial cytoplasmic membrane. Microbiol. mol. Biol. Rev. 63, 161-173.
44. FISHER, L. E. et al. (1999). Detergents modulate dimerization, but not helicity, of the glycophorin A transmembrane domain. J. mol. Biol. 293, 639-651.
45. GAFVELIN, G. & VON HEIJNE, G. (1994). Topological 'frustration' in multi-spanning E. coli inner membrane proteins. Cell, 401-412.
46. GAFVELIN, G. et al. (1997). Topological rules for membrane protein assembly in eukaryotic cells. J. biol. Chem. 272, 6119-6127.
47. GLICK, B. S. & VON HEIJNE, G. (1996). Saccharomyces cerevisiae mitochondria lack a bacterial-type Sec machinery. Prot. Sci. 5, 2651-2652.
48. GODER, V. et al. (1999). Glycosylation can influence topogenesis of membrane proteins and reveals dynamic reorientation of nascent polypeptides within the translocon. J. Cell Biol. 147, 257-266.
49. HAMMAN, B. D. et al. (1998). BiP maintains the permeability barrier of the ER membrane by sealing the lumenal end of the translocon pore before and early in translocation. Cell 92, 747-758.
50. HAN, E. S. & ZHANG, J. T. (1998). Mechanism involved in generating the carboxyl-terminal half topology of P-glycoprotein. Biochemistry 37, 11996-12004.
51. HE, S. & FOX, T. D. (1997). Membrane translocation of mitochondrially coded Cox2p: distinct requirements for export of N and C termini and dependence on the conserved protein Oxa1p. Mol. Biol. Cell 8, 1449-1460.
52. HE, S. C & FOX, T. D. (1999). Mutations affecting a yeast mitochondrial inner membrane protein, Pnt1p, block export of a mitochondrially synthesized fusion protein from the matrix. Mol. Cell. Biol. 19, 6598-6607.
53. HEGDE, R. & LINGAPPA, V. (1997). Membrane protein biogenesis: Regulated complexity at the endoplasmic reticulum. Cell 91, 575-582.
54. HEGDE, R. S. & LINGAPPA, V. R. (1999). Regulation of protein biogenesis at the endoplasmic reticulum membrane. Trends Cell Biol. 9, 132-137.
55. HELL, K. et al. (1997). Oxa1p mediates the export of the N- and C-termini of pCoxII from the mitochondrial matrix to the intermembrane space. FEBS Lett. 418, 367-370.
56. HELL, K. et al. (1998). Oxa1p, an essential component of the N-tail protein export machinery in mitochondria. Proc. natn. Acad. Sci. USA 95, 2250-2255.
57. HERRMANN, J. M. et al. (1997). Insertion into the mitochondrial inner membrane of a polytopic protein, the nuclear-encoded Oxa1p. EMBO J. 16, 2217-2226.
58. HYNDS, P. J. et al. (1998). The Sec-independent twin-arginine translocation system can transport both tightly folded and malfolded proteins across the thylakoid membrane. J. biol. Chem. 273, 34868-34874.
59. ITO, K. ( 1996). The major pathway of protein translocation across membranes. Genes to Cells 1, 337-346.
60. IVERSON, T. M. et al. (1999). Structure of the Escherichia coli fumarate reductase respiratory complex. Science 284, 1961-1966.
61. 1 complex. Science 281, 64-71.
62. JAVADPOUR, M. M. et al. (1999). Helix packing in polytopic membrane proteins: role of glycine in transmembrane helix association. Biophys. J. 77, 1609-1618.
63. JOHNSON, A. E. (1997). Protein translocation at the ER membrane: a complex process becomes more so. Trends Cell Biol. 7, 90-95.
64. KIEFER, D. & KUHN, A. (1999). Hydrophobic forces drive spontaneous membrane insertion of the bacteriophage Pf3 coat protein without topological control. Embo J. 18, 6299-6306.
65. KIM, S. J. et al. (1998). Sec/SRP-independent insertion of two thylakoid membrane proteins bearing cleavable signal peptides. FEBS Lett. 424, 105-108.
66. KIM, S. J. et al. (1999). Distinct 'assisted' and 'spontaneous' mechanisms for the insertion of polytopic chlorophyll-binding proteins into the thylakoid membrane. J. biol. Chem. 274, 4715-4721.
67. KLÖSGEN, R. B. et al. (1992). Proton gradient-driven import of the 16 kDa oxygen-evolving complex protein as the full precursor protein by isolated thylakoids. Plant. mol. Biol. 18, 1031-1034.
68. KOEHLER, C. et al. (1998a). Tim9p, an essential partner subunit of Tim10p for the import of mitochondrial carrier proteins. EMBO J. 17, 6477-6486.
69. KOEHLER, C. M. et al. (1998b). Import of mitochondrial carriers mediated by essential proteins of the intermembrane space. Science 279, 369-373.
70. LANCASTER, C. R. et al. (1999). Structure of fumarate reductase from Wolinella succinogenes at 2·2 A resolution. Nature 402, 377-385.
71. LANGOSCH, D. et al. ( 1996). Dimerisation of the glycophorin A transmembrane segment in membranes probed with the ToxR transcription activator. J. mol. Biol. 263, 525-530.
72. LANYI, J. K. (1997). Mechanism of ion transport across membranes - bacteriorhodopsin as a prototype for proton pumps. J. biol. Chem. 272, 31209-31212.
73. LAU, F. W. & BOWIE, J. U. (1997). A method for assessing the stability of a membrane protein. Biochemistry 36, 5884-5892.
74. LEMMON, M. A. & ENGELMAN, D. M. (1994). Specificity and promiscuity in membrane helix interactions. FEBS Lett. 346, 17-20.
75. LEMMON, M. A. et al. (1992a). Glycophorin A dimerization is driven by specific interactions between transmembrane α-helices. J. biol. Chem. 267, 7683-7689.
76. LEMMON, M. A. et al. (1992b). Sequence specificity in the dimerization of transmembrane α-helices. Biochemistry 31, 12719-12725.
77. LEMMON, M. A. et al. (1994). A dimerization motif for transmembrane α-helices. Nature struct. Biol. 1, 157-163.
78. LEUENBERGER, D. et al. (1999). Different import pathways through the mitochondrial intermembrane space for inner membrane proteins. EMBO J. 18, 4816-4822.
79. LEVY, D. (1996). Membrane proteins which exhibit multiple topological orientations. Essay Biochem. 31, 49-60.
80. LIAO, S. et al. (1997). Both lumenal and cytosolic gating of the aqueous ER translocon pore are regulated from inside the ribosome during membrane protein integration. Cell 90, 31-41.
81. LOEPER, J. et al. (1998a). Topology inversion of CYP2D6 in the endoplasmic reticulum is not required for plasma membrane transport. Mol. Pharmacol. 53, 408-414.
82. LOEPER, J. et al. (1998b). Yeast expressed cytochrome P450 2D6 (CYP2D6) exposed on the external face of plasma membrane is functionally competent. Mol. Pharmacol. 54, 8-13.
83. LOPEZ, C. D. et al. (1990). Unusual topogenic sequence directs prion protein biogenesis. Science 248, 226-229.
84. LUECKE, H. et al. (1999). Structural changes in bacteriorhodopsin during ion transport at 2 Angstrom resolution. Science 286, 255-260.
85. LUIRINK, J. et al. ( 1992). Signal-sequence recognition by an Escherichia coli ribonucleoprotein complex. Nature 359, 741-743.
86. MACFARLANE, J. & MÜLLER, M. (1995). The functional integration of a polytopic membrane protein of Escherichia coli is dependent on the bacterial signal-recognition particle. Eur. J. Biochem. 233, 766-771.
87. MACKENZIE, K. R. & ENGELMAN, D. M. (1998). Structure-based prediction of the stability of transmembrane helix-helix interactions : the sequence dependence of glycophorin A dimerization. Proc. natn. Acad. Sci. USA 95, 3583-3590.
88. MACKENZIE, K. R. et al. (1997). A transmembrane helix dimer: structure and implications. Science 276, 131-133.
89. MONNÉ, M. et al. (1998). Positively and negatively charged residues have different effects on the position in the membrane of a model transmembrane helix. J. mol. Biol. 284, 1177-1183.
90. MONNÉ, M. et al. (1999a). N-tail translocation in a eukaryotic polytopic membrane protein-synergy between neighboring transmembrane segments. Eur. J. Biochem. 263, 264-269.
91. MONNÉ, M. et al. (1999b). A turn propensity scale for transmembrane helices. J. mol. Biol. 288, 141-145.
92. MONNÉ, M. et al. (1999c). Turns in transmembrane helices: determination of the minimal length of a 'helical hairpin' and derivation of a fine-grained turn propensity scale. J. mol. Biol. 293, 807-814.
93. MOTHES, W. et al. (1997). Molecular mechanisms of membrane protein integration into the endoplasmic reticulum. Cell 89, 523-533.
94. MOULD, R. M. & ROBINSON, C. (1991). A proton gradient is required for the transport of two lumenal oxygen-evolving proteins across the thylakoid membrane. J. biol. Chem. 266, 12189-12193.
95. NEVE, E. & INGELMAN-SUNDBERG, M. (2000). Structural determinants for the transport of CYP2E1 to the plasma membrane. J. biol. Chem. in press.
96. NILSSON, I. & VON HEIJNE, G. (1993). Determination of the distance between the oligosaccharyltransferase active site and the endoplasmic reticulum membrane. J. biol. Chem. 268, 5798-5801.
97. NILSSON, I. & VON HEIJNE, G. (1998). Breaking the camel's back: proline-induced turns in a model transmembrane helix. J. mol. biol. 284, 1185-1189.
98. NILSSON, I. et al. (1998). Proline-induced disruption of a transmembrane α- helix in its natural environment. J. mol. Biol. 284, 1165-1175.
99. NILSSON, I. et al. (2000). Distant downstream sequence determinants can control N-tail translocation during proten insertion into the ER membrane. J. Biol. Chem. 275, 6207-6213.
100. NISHIYAMA, K. et al. (1996). Inversion of the membrane topology ot SecG coupled with SecA-dependent preprotein translocation. Cell 85, 71-81.
101. OLIVER, J. et al. (1995). The Sec61 complex is essential for the insertion of proteins into the membrane of the endoplasmic reticulum. FEBS Lett. 362, 126-130.
102. OTA, K. et al. (1998). Forced transmembrane orientation of hydrophilic polypeptide segments in multispanning proteins. Molec. Cell 2, 495-503.
103. POLSCHRÖDER, M. et al. (1997). Protein translocation in the three domains of life: variations on a theme. Cell 91, 563-566.
104. POPOT, J. L. & ENGELMAN, D. M. (1990). Membrane protein folding and oligomerization the 2-stage model. Biochemistry 29, 4031-4037.
105. RAPOPORT, T. A. et al. (1996). Protein transport across the eukaryotic endoplasmic reticulum and bacterial inner membranes. A. rev. Biochem. 65, 271-303.
106. REIZER, J. et al. (1993). The MIP family of integral membrane channel proteins: sequence comparisons, evolutionary relationships, reconstructed pathway of evolution, and proposed functional differentiation of the two repeated halves of the proteins. Crit. Rev. Biochem. mol. Biol. 28, 235-257.
107. RILEY, M. L. et al. (1997). Slow alpha helix formation during folding of a membrane protein. Biochemistry 36, 192-196.
108. ROBINSON, C. et al. (1994). The presequence of a chimeric construct dictates which of two mechanisms are utilized for translocation across the thylakoid membrane: evidence for the existence of two distinct translocation systems. EMBO J. 13, 279-285.
109. ROJO, E. E. et al. (1999). N-terminal tail export from the mitochondrial matrix adherence to the prokaryotic 'positive-inside' rule of membrane protein topology. J. biol. Chem. 274, 19617-19622.
110. ROST, B. et al. (1996). Topology prediction for helical transmembrane proteins at 86% accuracy. Protein Sci. 5, 1704-1718.
111. ROUX, B. & MACKINNON, R. (1999). The cavity and pore helices in the KcsA K+ channel: electrostatic stabilization of monovalent cations. Science 285, 100-102.
112. RUSS, W. & ENGELMAN, D. (1999). TOXCAT: a measure of transmembrane helix association in a biological membrane. Proc. natn. Acad. Sci. USA 96, 863-868.
113. RUSS, W. & ENGELMAN, D. (2000). The GxxxG motif: a framework for transmembrane helix -helix association. J. mol. biol. 296, 911-919.
114. SÄÄF, A. et al. (1998). Membrane topology of the 60-kDa Oxa1p homologue from Escherichia coli. J. biol. Chem. 273, 30415-30418.
115. SÄÄF, A. et al. (1999). Divergent evolution of membrane protein topology : the Escherichia coli. RnfA and RnfE homologues. Proc. natn. Acad. Sci. USA 96, 8540-8544.
116. SANSOM, M. S. P. (1992). Proline residues in transmembrane helices of channel and transport proteins: a molecular modelling study. Prof. Engineer 5, 53-60.
117. SANTINI, C. L. et al. (1998). A novel Sec-independent periplasmic protein translocation pathway in Escherichia coli. EMBO J. 17, 101-112.
118. SARGENT, F. et al. (1998). Overlapping functions of components of a bacterial Sec-independent protein export pathway. EMBO J. 17, 3640-3650.
119. SATO, T. et al. (1990). The amino-terminal structures that determine topological orientation of cytochrome-P-450 in microsomal membrane. EMBO J. 9, 2391-2397.
120. SCHIRMER, T. (1998). General and specific porins from bacterial outer membranes. J. struct. Biol. 121, 101-109.
121. SCOTTI, P. et al. (2000). YidC, the E. coli homologue of mitochondrial Oxa1p, is a component of the Sec translocase. EMBO J. 19, 542-549.
122. SEGREST, J. P. et al. (1990). Amphipathic helix motif: classes and properties. PROTEINS 8, 103-117.
123. SELUANOV, A. & BIBI, E. (1997). FtsY, the prokaryotic signal recognition particle receptor homologue, is essential for biogenesis of membrane proteins. J. biol. Chem. 272, 2053-2055.
124. SENES, A. et al. (2000). Statistical analysis of amino acid patterns in transmembrane helices: the GxxxG motif occurs frequently in association with β-branched residues at neighboring positions. J. mol. Biol. 296, 921-936.
125. SETTLES, A. et al. (1997). Sec-independent protein translocation by the maize Hcf106 protein. Science 278, 1467-1470.
126. SIRRENBERG, C. et al. (1998). Carrier protein import into mitochondria mediated by the intermembrane proteins Tim10/Mrs11 and tim12/Mrs5. Nature 391, 912-915.
127. SONNHAMMER, E. et al. (1998). A hidden Markov model for predicting transmembrane helices in protein sequences. Intell. Syst. mol. Biol. 6, 175-182.
128. STUART, R. A. & NEUPERT, W. (1996). Topogenesis of inner membrane proteins of mitochondria. Trends biochem. Sci. 21, 261-267.
129. THOMPSON, S. J. et al. (1998). Sec-independent insertion of thylakoid membrane proteins - analysis of insertion forces and identification of a loop intermediate involving the signal peptide. J. biol. Chem. 273, 18979-18983.
130. TREUTLEIN, H. R. et al. (1992). The glycophorin A transmembrane domain dimer: sequence-specific propensity for a right-handed supercoil of helices. Biochemistry 31, 12726-12732.
131. TUSNADY, G. E. & SIMON, I. (1998). Principles governing amino acid composition of integral membrane proteins: application to topology prediction. J. mol. Biol. 283, 489-506.
132. ULBRANDT, N. D. et al. (1997). The E. coli signal recognition particle is required for the insertion of a subset ot inner membrane proteins. Cell 88, 187-196.
133. VALENT, Q. A. et al. (1997). Association of nascent membrane and presecretory proteins with Signal Recognition Particle and Trigger Factor. Molec. Microbiol. 25, 53-64.
134. VALENT, Q. A. et al. (1998). The Escherichia coli SRP and SecB targeting pathways converge at the translocon. EMBO J. 17, 2504-2512.
135. VAN DE VOSSENBERG, J. L. et al. (1998). The positive inside rule is not determined by the polarity of the delta psi (transmembrane electrical potential) [letter]. Mol. Microbiol. 29, 1125-1127.
136. VAN WIJK, K. J. et al. (1995). Evidence for SecA- and Delta pH-independent insertion of D1 into thylakoids. FEBS Lett. 368, 263-266.
137. VON HEIJNE, G. (1991). Proline kinks in transmembrane α-helices. J. mol. Biol. 218, 499-503.
138. VON HEIJNE, G. (1992). Membrane protein structure prediction hydrophobicity analysis and the positive-inside rule. J. mol. Biol. 225, 487-494.
139. VON HEIJNE, G. (1994). Sec-independent protein insertion into the inner E. coli membrane: A phenomenon in search of an explanation. FEBS Lett. 346, 69-72.
140. VON HEIJNE, G. (1996). Principles of membrane protein assembly and structure. Progr. Biophys. mol. Biol. 66, 113-139.
141. VON HEIJNE, G. (1997). Getting greasy: how transmembrane polypeptide segments integrate into the lipid bilayer. Mol. Microbiol. 24, 249-253.
142. VON HEIJNE, G. (1999). A day in the life of Dr K. or How I learned to stop worrying and love lysozyme: A tragedy in six acts. J. molec. Biol. 293, 367-379.
143. WALLIN, E. & VON HEIJNE, G. (1998). Genome-wide analysis of integral membrane proteins from eubacterial, archaean, and eukaryotic organisms. Protein Sci. 7, 1029-1038.
144. WALLIN, E. et al. (1997). Architecture of helix bundle membrane proteins: an analysis ot cytochrome c oxidase from bovine mitochondria. Protein Sci. 6, 808-815.
145. WHITLEY, P. et al. (1994). Sec-independent translocation of a 100-residues long periplasmic N-terminal tail in the E. coli inner membrane proteins ProW. EMBO J. 13, 4653-4661.
146. WHITLEY, P. et al. (1995). Sec-independent translocation of the periplasmic N-terminal tail on an E. coli inner membrane protein : position-specific effects on translocation of positively charged residues and construction of a protein with a C-terminal translocation signal. J. biol. Chem. 270, 29831-29835.
147. WU, D. & CEDERBAUM, A. I. (1992). Presence of functionally active cytochrome P-450IIE1 in the plasma membrane of rat hepatocytes. Hepatology 15, 515-524.
148. YAU, W. M. et al. (1998). The preference of tryptophan for membrane interfaces. Biochemistry 37, 14713-14718.
149. YOST, C. S. et al. (1990). Non-hydrophobic extracytoplasmic determinant of stop transfer in the prion protein. Nature 343, 669-672.
150. ZELAZNY, A. et al. (1997). The NG domain of the prokaryotic signal recognition particle receptor, FtSY, is fully functional when fused to an unrelated integral membrane polypeptide. Proc. natn. Acad. Sci. USA 94, 6025-6029.
151. ZHANG, J.-T. et al. (1998a). Dissection of de novo membrane insertion activities of internal transmembrane segments of ATP-binding cassette transporters: Toward understanding topological rules for membrane assembly ot polytopic membrane proteins. Mol. Biol. Cell 9, 853-863.
152. 1. Nature 392, 677-684.
153. ZHU, Q. S. et al. (1999). Membrane topology and cell surface targeting of microsomal epoxide hydrolase evidence for multiple topological orientations. J. biol. Chem. 274, 27898-27904.