How do helix–helix interactions help determine the folds of membrane proteins? Perspectives from the study of homo‐oligomeric helical bundles
10.1110/ps.0236503
Crossref journal-article
Wiley
Protein Science (311)
Abstract

AbstractThe final, structure‐determining step in the folding of membrane proteins involves the coalescence of preformed transmembrane helices to form the native tertiary structure. Here, we review recent studies on small peptide and protein systems that are providing quantitative data on the interactions that drive this process. Gel electrophoresis, analytical ultracentrifugation, and fluorescence resonance energy transfer (FRET) are useful methods for examining the assembly of homo‐oligomeric transmembrane helical proteins. These methods have been used to study the assembly of the M2 proton channel from influenza A virus, glycophorin, phospholamban, and several designed membrane proteins—all of which have a single transmembrane helix that is sufficient for association into a transmembrane helical bundle. These systems are being studied to determine the relative thermodynamic contributions of van der Waals interactions, conformational entropy, and polar interactions in the stabilization of membrane proteins. Although the database of thermodynamic information is not yet large, a few generalities are beginning to emerge concerning the energetic differences between membrane and water‐soluble proteins: the packing of apolar side chains in the interior of helical membrane proteins plays a smaller, but nevertheless significant, role in stabilizing their structure. Polar, hydrogen‐bonded interactions occur less frequently, but, nevertheless, they often provide a strong driving force for folding helix–helix pairs in membrane proteins. These studies are laying the groundwork for the design of sequence motifs that dictate the association of membrane helices.

Bibliography

DeGrado, W. F., Gratkowski, H., & Lear, J. D. (2003). How do helix–helix interactions help determine the folds of membrane proteins? Perspectives from the study of homo‐oligomeric helical bundles. Protein Science, 12(4), 647–665. Portico.

Authors 3
  1. William F. DeGrado (first)
  2. Holly Gratkowski (additional)
  3. James D. Lear (additional)
References 187 Referenced 134
  1. 10.1021/bi020486r
  2. 10.1006/jmbi.2001.4908
  3. 10.1002/prot.10071
  4. 10.1038/nsb0295-154
  5. 10.1002/(SICI)1097-0134(199611)26:3<257::AID-PROT2>3.0.CO;2-B
  6. 10.1021/bi002829w
  7. 10.1002/j.1460-2075.1994.tb06801.x
  8. 10.1006/jmbi.1995.0263
  9. 10.1007/s002329900172
  10. 10.1016/0958-1669(94)90048-5
  11. 10.1002/(SICI)1097-0282(1998)47:1<31::AID-BIP5>3.0.CO;2-Y
  12. 10.1021/cr0000473
  13. 10.1073/pnas.85.15.5394
  14. 10.1016/0092-8674(86)90779-8
  15. 10.1006/viro.1998.9552
  16. 10.1074/jbc.272.4.2031
  17. 10.1016/S0021-9258(19)84957-8 / J. Biol. Chem. / Synthetic peptides mimic the assembly of transmembrane glycoproteins by Bormann B.‐J. (1989)
  18. 10.1006/jmbi.1997.1279
  19. 10.1038/72454
  20. 10.1016/S0959-440X(00)00223-2
  21. 10.1002/pro.5560070423
  22. 10.1002/(SICI)1097-0134(199610)26:2<134::AID-PROT3>3.0.CO;2-G
  23. 10.1126/science.270.5238.935
  24. 10.1016/S0006-3495(99)76956-0
  25. 10.1021/bi9909039
  26. 10.1021/bi011268l
  27. 10.1021/bi011269d
  28. 10.1021/bi011776v
  29. 10.1038/72440
  30. 10.1021/bi960080c
  31. {'key': 'e_1_2_15_32_1', 'first-page': '171', 'article-title': 'Influenza‐virus M2 protein and hemagglutinin conformation changes during intracellular‐transport', 'volume': '39', 'author': 'Ciampor F.', 'year': '1995', 'journal-title': 'Acta Virol.'} / Acta Virol. / Influenza‐virus M2 protein and hemagglutinin conformation changes during intracellular‐transport by Ciampor F. (1995)
  32. 10.1002/prot.340070102
  33. 10.1073/pnas.081069198
  34. {'key': 'e_1_2_15_35_1', 'first-page': '277', 'article-title': 'CFTR degradation and aggregation', 'volume': '70', 'author': 'Corboy M.J.', 'year': '2002', 'journal-title': 'Methods Mol. Med.'} / Methods Mol. Med. / CFTR degradation and aggregation by Corboy M.J. (2002)
  35. 10.1021/bi961955q
  36. 10.1006/jmbi.2001.5353
  37. 10.1073/pnas.90.24.11648
  38. 10.1034/j.1399-3011.1999.00118.x
  39. 10.1021/ja00311a076
  40. 10.1126/science.2464850
  41. 10.1146/annurev.biochem.68.1.779
  42. 10.1002/pro.5560041101
  43. 10.1016/0042-6822(92)91239-Q
  44. 10.1006/jmbi.1993.1170
  45. 10.1073/pnas.97.11.5796
  46. 10.1021/bi0107694
  47. 10.1016/0092-8674(81)90136-7
  48. 10.1006/jmbi.1999.3126
  49. 10.1016/S0022-2836(02)00590-9
  50. 10.1016/S0076-6879(00)23361-2
  51. 10.1002/prot.1151
  52. 10.1073/pnas.251367498
  53. 10.1006/jmbi.1997.1236
  54. 10.1016/S1359-0278(98)00061-3
  55. 10.1016/S0006-3495(00)76572-6
  56. 10.1021/bi0000972
  57. 10.1016/S0021-9258(18)51579-9 / J. Biol. Chem. / Expression and site‐specific mutagenesis of phospholamban. Studies of residues involved in phosphorylation and pentamer formation by Fujii J. (1989)
  58. 10.1073/pnas.93.22.12155
  59. 10.1021/bi9707584
  60. 10.1038/nsb1296-1002
  61. 10.1038/nsb0696-510
  62. 10.1038/nsb1296-1011
  63. 10.1073/pnas.98.3.880
  64. 10.1016/S0006-3495(02)73930-1
  65. 10.1126/science.8248779
  66. 10.1038/371080a0
  67. 10.1002/j.1460-2075.1985.tb04038.x
  68. 10.1074/jbc.M102495200
  69. 10.1002/pro.5560030206
  70. 10.1021/bi9605191
  71. 10.1139/o96-015
  72. 10.1021/bi011267t
  73. 10.1016/0042-6822(91)90115-R
  74. 10.1128/jvi.69.2.1219-1225.1995 / J. Virology / Analysis of the posttranslational modifications of the influenza‐virus M(2) protein by Holsinger L.J. (1995)
  75. 10.1016/S0065-3233(08)60331-9
  76. 10.1016/S0969-2126(96)00085-8
  77. 10.1016/S0959-440X(98)80158-9
  78. 10.1016/S0006-3495(99)77009-8
  79. 10.1021/bi980642n
  80. 10.1021/bi011016k
  81. 10.1021/bi0200763
  82. 10.1021/bi990720m
  83. 10.1016/S0006-3495(97)78279-1
  84. 10.1006/jmbi.1998.2512
  85. 10.1111/j.1432-1033.1997.00540.x
  86. 10.1074/jbc.M910092199
  87. 10.1006/viro.1997.8451
  88. 10.1006/jmbi.1993.1066
  89. 10.1074/jbc.273.35.22453
  90. 10.1002/(SICI)1097-0134(19980501)31:2<150::AID-PROT5>3.0.CO;2-Q
  91. 10.1006/jmbi.1996.0595
  92. 10.1021/bi963095j
  93. {'key': 'e_1_2_15_94_1', 'first-page': '90', 'volume-title': 'Analytical ultracentrifugation in biochemistry and polymer science', 'author': 'Laue T.', 'year': '1992'} / Analytical ultracentrifugation in biochemistry and polymer science by Laue T. (1992)
  94. 10.1126/science.2453923
  95. 10.1007/978-1-4614-7515-6_15
  96. 10.1017/S0033583500004522
  97. 10.1016/S0021-9258(18)42569-0 / J. Biol. Chem. / Glycophorin A dimerization is driven by specific interactions between transmembrane α helices by Lemmon M.A. (1991)
  98. 10.1021/bi00166a002
  99. 10.1038/nsb0394-157
  100. 10.1021/bi0026573
  101. 10.1021/bi9801053
  102. 10.1016/S0006-3495(99)77411-4
  103. 10.1073/pnas.221463098
  104. 10.1002/(SICI)1097-0282(1998)47:1<41::AID-BIP6>3.0.CO;2-X
  105. 10.1074/jbc.273.37.23645
  106. 10.1016/S0021-9258(18)34529-0 / J. Biol. Chem. / Denaturation and renaturation of bacteriorhodopsin by London E. (1982)
  107. 10.1074/jbc.M100600200
  108. 10.1016/S0006-3495(96)79735-7
  109. 10.1126/science.276.5309.131
  110. 10.1126/science.274.5288.761
  111. 10.1021/bi010642e
  112. 10.1002/pro.5560050712
  113. 10.1016/0958-1669(95)80066-2
  114. 10.1073/pnas.94.7.2833
  115. 10.1021/bi9707180
  116. 10.1006/jmbi.2001.4900
  117. 10.1021/bi981269m
  118. 10.1006/geno.1997.4967
  119. 10.1126/science.273.5276.810
  120. 10.1021/bi0028441
  121. 10.1126/science.1948029
  122. 10.1016/0022-2836(92)90121-Y
  123. 10.1096/fasebj.10.1.8566551
  124. 10.1110/ps.52101
  125. 10.1021/bi00082a007
  126. 10.1021/bi00189a025
  127. 10.1073/pnas.94.21.11301
  128. 10.1021/bi00469a001
  129. 10.1146/annurev.biochem.69.1.881
  130. 10.1002/j.1460-2075.1986.tb04603.x
  131. 10.1021/bi981795d
  132. 10.1002/(SICI)1097-0134(20000201)38:2<121::AID-PROT1>3.0.CO;2-M
  133. 10.1126/science.2667138
  134. 10.1073/pnas.96.3.863
  135. 10.1006/jmbi.1999.3489
  136. 10.1073/pnas.94.10.5000
  137. 10.1021/bi001799u
  138. 10.1073/pnas.92.10.4577
  139. 10.1016/S1359-0278(98)00011-X
  140. 10.1016/S0014-5793(96)01146-5
  141. 10.1006/jmbi.1999.3488
  142. 10.1073/pnas.161280798
  143. 10.1002/prot.340150302
  144. 10.1016/S0968-0004(00)89101-X
  145. 10.1073/pnas.101130498
  146. 10.1146/annurev.biophys.31.101101.140922
  147. 10.1074/jbc.271.10.5941
  148. 10.1038/nsb0396-252
  149. 10.1021/bi010357v
  150. 10.1016/S0006-3495(02)75590-2
  151. 10.1021/bi951087h
  152. 10.1073/pnas.92.2.452
  153. 10.1016/S0014-5793(00)01429-0
  154. 10.1002/(SICI)1097-0134(19990701)36:1<135::AID-PROT11>3.0.CO;2-I
  155. 10.1038/87569
  156. 10.1016/0304-4157(76)90009-5
  157. 10.1021/bi00708a021
  158. 10.1074/jbc.M206582200
  159. 10.1016/S0076-6879(73)27017-9
  160. 10.1038/89631
  161. 10.1021/bi025695q
  162. 10.1021/bi00615a025
  163. 10.1006/jmbi.2000.3885
  164. 10.1016/S0006-3495(00)76547-7
  165. 10.1021/bi00166a003
  166. 10.1006/jmbi.2000.3866
  167. 10.1016/0022-2836(77)90042-0
  168. 10.1017/S0033583500003541
  169. 10.1002/pro.5560020306
  170. 10.1110/ps.8.11.2312
  171. 10.1074/jbc.M000723200
  172. 10.1110/ps.17901
  173. 10.1038/339230a0
  174. 10.1146/annurev.biophys.28.1.319
  175. 10.1083/jcb.145.3.481
  176. {'key': 'e_1_2_15_177_1', 'first-page': '381', 'article-title': 'A protein sequence that can encode native structure by disfavoring alternate conformations', 'volume': '9', 'author': 'Wigley W.C.', 'year': '2002', 'journal-title': 'Nat. Struct. Biol.'} / Nat. Struct. Biol. / A protein sequence that can encode native structure by disfavoring alternate conformations by Wigley W.C. (2002)
  177. 10.1021/bi992746j
  178. 10.1016/S0006-3495(79)85171-1
  179. 10.1055/s-0037-1616229
  180. 10.1002/pro.5560070117
  181. 10.1021/bi011161y
  182. 10.1016/S0014-5793(98)00988-0
  183. 10.1016/S0014-5793(00)01522-2
  184. 10.1038/81919
  185. 10.1073/pnas.041593698
  186. 10.1110/ps.34201
  187. 10.1006/jmbi.2000.3936
Dates
Type When
Created 22 years, 5 months ago (March 20, 2003, 3:05 p.m.)
Deposited 1 year, 10 months ago (Oct. 9, 2023, 11:12 p.m.)
Indexed 1 week, 1 day ago (Aug. 21, 2025, 2:03 p.m.)
Issued 22 years, 4 months ago (April 1, 2003)
Published 22 years, 4 months ago (April 1, 2003)
Published Online 16 years, 7 months ago (Jan. 1, 2009)
Published Print 22 years, 4 months ago (April 1, 2003)
Funders 0

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@article{DeGrado_2003, title={How do helix–helix interactions help determine the folds of membrane proteins? Perspectives from the study of homo‐oligomeric helical bundles}, volume={12}, ISSN={1469-896X}, url={http://dx.doi.org/10.1110/ps.0236503}, DOI={10.1110/ps.0236503}, number={4}, journal={Protein Science}, publisher={Wiley}, author={DeGrado, William F. and Gratkowski, Holly and Lear, James D.}, year={2003}, month=apr, pages={647–665} }