Assembly of the M2 Tetramer Is Strongly Modulated by Lipid Chain Length

Biophysical Journal

Volumn 99, Issue 6, 2010, Pages 1810-1817

  Schick, Sandra ^a,d   Chen, Lirong ^a   Li, Edwin ^a,e   Lin, Janice ^a   Köper, Ingo ^b,c   Hristova, Kalina ^a  

^a Johns Hopkins University   (United States)

^b FLINDERS UNIVERSITY   (Australia)

^c MAX PLANCK INSTITUTE FOR POLYMER RESEARCH   (Germany)

^d JOHANNES GUTENBERG UNIVERSITY   (Germany)

^e SAINT JOSEPH S UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ERO; ORTHOMYXOVIRIDAE;

EID: 77957331606     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2010.07.026     Document Type: Article

References (63)

1. White, S. H., and W. C. Wimley. 1999. Membrane protein folding and stability: physical principles. Annu. Rev. Biophys. Biomol. Struct. 28:319-365.
2. White, S. H., A. S. Ladokhin, K. Hristova. 2001. How membranes shape protein structure. J. Biol. Chem. 276:32395-32398.
3. Hong, H., N. H. Joh, L. K. Tamm. 2009. Methods for measuring the thermodynamic stability of membrane proteins. Methods Enzymol. 455:213-236.
4. Mackenzie, K. R. 2006. Folding and stability of a-helical integral membrane proteins. Chem. Rev. 106:1931-1977.
5. Han, X., K. Hristova, and W. C. Wimley. 2008. Protein folding in membranes: insights from neutron diffraction studies of a membrane β-sheet oligomer. Biophys. J. 94:492-505.
6. Opekarová, M., and W. Tanner. 2003. Specific lipid requirements of membrane proteins-a putative bottleneck in heterologous expression. Biochim. Biophys. Acta. 1610:11-22.
7. Botelho, A. V., N. J. Gibson, M. F. Brown. 2002. Conformational energetics of rhodopsin modulated by nonlamellar-forming lipids. Biochemistry. 41:6354-6368.
8. Botelho, A. V., T. Huber, M. F. Brown. 2006. Curvature and hydro- phobic forces drive oligomerization and modulate activity of rhodopsin in membranes. Biophys. J. 91:4464-4477.
9. You, M., E. Li, K. Hristova. 2005. FRET in liposomes: measurements of TM helix dimerization in the native bilayer environment. Anal. Biochem. 340:154-164.
10. Duong, M. T., T. M. Jaszewski, K. R. MacKenzie. 2007. Changes in apparent free energy of helix-helix dimerization in a biological membrane due to point mutations. J. Mol. Biol. 371:422-434.
11. Cristian, L., J. D. Lear, and W. F. DeGrado. 2003. Use of thiol-disulfide equilibria to measure the energetics of assembly of transmembrane helices in phospholipid bilayers. Proc. Natl. Acad. Sci. USA. 100:14772-14777.
12. Chen, L., L. Novicky, K. Hristova. 2010. Measuring the energetics of membrane protein dimerization in mammalian membranes. J. Am. Chem. Soc. 132:3628-3635.
13. Lamb, R. A., S. L. Zebedee, and C. D. Richardson. 1985. Influenza virus M2 protein is an integral membrane protein expressed on the infected-cell surface. Cell. 40:627-633.
14. Takeuchi, K., and R. A. Lamb. 1994. Influenza virus M2 protein ion channel activity stabilizes the native form of fowl plague virus hemag- glutinin during intracellular transport. J. Virol. 68:911-919.
15. Chizhmakov, I. V., F. M. Geraghty, A. J. Hay. 1996. Selective proton permeability and pH regulation of the influenza virus M2 channel expressed in mouse erythroleukaemia cells. J. Physiol. 494:329-336.
16. Wharton, S. A., R. B. Belshe, A. J. Hay. 1994. Role of virion M2 protein in influenza virus uncoating: specific reduction in the rate of membrane fusion between virus and liposomes by amantadine. J. Gen. Virol. 75:945-948.
17. Ciampor, F., P. M. Bayley, A. J. Hay. 1992. Evidence that the aman- tadine-induced, M2-mediated conversion of influenza A virus hemagglu- tinin to the low pH conformation occurs in an acidic trans Golgi compartment. Virology. 188:14-24.
18. Sugrue, R. J., G. Bahadur, A. J. Hay. 1990. Specific structural alteration of the influenza haemagglutinin by amantadine. EMBO J. 9:3469-3476.
19. Pinto, L. H., G. R. Dieckmann, W. F. DeGrado. 1997. A functionally defined model for the M2 proton channel of influenza A virus suggests a mechanism for its ion selectivity. Proc. Natl. Acad. Sci. USA. 94:11301-11306.
20. Pinto, L. H., and R. A. Lamb. 2006. The M2 proton channels of influenza A and B viruses. J. Biol. Chem. 281:8997-9000.
21. Stouffer, A. L., C. L. Ma, W. F. DeGrado. 2008. The interplay of functional tuning, drug resistance, and thermodynamic stability in the evolution of the M2 proton channel from the influenza A virus. Structure. 16:1067-1076.
22. Ma, C. L., A. L. Polishchuk, L. H. Pinto. 2009. Identification of the functional core of the influenza A virus A/M2 proton-selective ion channel. Proc. Natl. Acad. Sci. USA. 106:12283-12288.
23. Duff, K. C., S. M. Kelly, J. P. Bradshaw. 1992. The secondary structure of influenza A M2 transmembrane domain. A circular dichroism study. FEBS Lett. 311:256-258.
24. Tosteson, M. T., L. H. Pinto, R. A. Lamb. 1994. Reconstitution of the influenza virus M2 ion channel in lipid bilayers. J. Membr. Biol. 142:117-126.
25. Duff, K. C., and R. H. Ashley. 1992. The transmembrane domain of influenza A M2 protein forms amantadine-sensitive proton channels in planar lipid bilayers. Virology. 190:485-489.
26. Duff, K. C., P. J. Gilchrist, J. P. Bradshaw. 1994. Neutron diffraction reveals the site of amantadine blockade in the influenza A M2 ion channel. Virology. 202:287-293.
27. Salom, D., B. R. Hill, W. F. DeGrado. 2000. pH-dependent tetrame- rization and amantadine binding of the transmembrane helix of M2 from the influenza A virus. Biochemistry. 39:14160-14170.
28. Stouffer, A. L., R. Acharya, W. F. DeGrado. 2008. Structural basis for the function and inhibition of an influenza virus proton channel. Nature. 451:596-599.
29. Tian, C. L., K. Tobler, T. A. Cross. 2002. Expression and initial structural insights from solid-state NMR of the M2 proton channel from influenza A virus. Biochemistry. 41:11294-11300.
30. Nishimura, K., S. G. Kim, T. A. Cross. 2002. The closed state of aH+ channel helical bundle combining precise orientational and distance restraints from solid state NMR. Biochemistry. 41:13170-13177.
31. Kovacs, F. A., and T. A. Cross. 1997. Transmembrane four-helix bundle of influenza A M2 protein channel: structural implications from helix tilt and orientation. Biophys. J. 73:2511-2517.
32. Kovacs, F. A., J. K. Denny, T. A. Cross. 2000. Helix tilt of the M2 transmembrane peptide from influenza A virus: an intrinsic property. J. Mol. Biol. 295:117-125.
33. Schnell, J. R., and J. J. Chou. 2008. Structure and mechanism ofthe M2 proton channel of influenza A virus. Nature. 451:591-595.
34. Hu, J., R. Fu, T. A. Cross. 2006. Histidines, heart of the hydrogen ion channel from influenza A virus: toward an understanding of conductance and proton selectivity. Proc. Natl. Acad. Sci. USA. 103:6865-6870.
35. Cady, S. D., T. V. Mishanina, and M. Hong. 2009. Structure of amantadine-bound M2 transmembrane peptide of influenza A in lipid bila- yers from magic-angle-spinning solid-state NMR: the role of Ser31 in amantadine binding. J. Mol. Biol. 385:1127-1141.
36. Wang, C., K. Takeuchi, R. A. Lamb. 1993. Ion channel activity of influenza A virus M2 protein: characterization of the amantadine block. J. Virol. 67:5585-5594.
37. Wang, C., R. A. Lamb, and L. H. Pinto. 1994. Direct measurement of the influenza A virus M2 protein ion channel activity in mammalian cells. Virology. 205:133-140.
38. Vijayvergiya, V., R. Wilson, D. D. Busath. 2004. Proton conductance of influenza virus M2 protein in planar lipid bilayers. Biophys. J. 87:1697-1704.
39. Duong-Ly, K. C., V. Nanda, K. P. Howard. 2005. The conformation of the pore region of the M2 proton channel depends on lipid bilayer environment. Protein Sci. 14:856-861.
40. Holsinger, L. J., and R. A. Lamb. 1991. Influenza virus M2 integral membrane protein is a homotetramer stabilized by formation of disul- fide bonds. Virology. 183:32-43.
41. Castrucci, M. R., M. Hughes, Y. Kawaoka. 1997. The cysteine residues of the M2 protein are not required for influenza A virus replication. Virology. 238:128-134.
42. Merzlyakov, M., and K. Hristova. 2008. Forster resonance energy transfer measurements of transmembrane helix dimerization energetics. Methods Enzymol. 450:107-127.
43. de Planque, M. R. R., and J. A. Killian. 2003. Protein-lipid interactions studied with designed transmembrane peptides: role of hydrophobic matching and interfacial anchoring. Mol. Membr. Biol. 20:271-284 (Review).
44. Iwamoto, T., M. You, K. Hristova. 2005. Synthesis and initial characterization of FGFR3 transmembrane domain: consequences of sequence modifications. Biochim. Biophys. Acta. 1668:240-247.
45. Adair, B. D., and D. M. Engelman. 1994. Glycophorin A helical trans- membrane domains dimerize in phospholipid bilayers: a resonance energy transfer study. Biochemistry. 33:5539-5544.
46. Li, M., L. G. Reddy, D. D. Thomas. 1999. A fluorescence energy transfer method for analyzing protein oligomeric structure: application to phospholamban. Biophys. J. 76:2587-2599.
47. Raicu, V., D. B. Jansma, J. D. Friesen. 2005. Protein interaction quantified in vivo by spectrally resolved fluorescence resonance energy transfer. Biochem. J. 385:265-277.
48. Chen, L., M. Merzlyakov, K. Hristova. 2009. Energetics of ErbB1 transmembrane domain dimerization in lipid bilayers. Biophys. J. 96:4622-4630.
49. Duysens, L. N. M. 1956. The flattening of the absorption spectrum of suspensions, as compared to that of solutions. Biochim. Biophys. Acta. 19:1-12.
50. Wallace, B. A., and D. Mao. 1984. Circular dichroism analyses of membrane proteins: an examination of differential light scattering and absorption flattening effects in large membrane vesicles and membrane sheets. Anal. Biochem. 142:317-328.
51. Wallace, B. A., and C. L. Teeters. 1987. Differential absorption flattening optical effects are significant in the circular dichroism spectra of large membrane fragments. Biochemistry. 26:65-70.
52. Hristova, K., W. C. Wimley, S. H. White. 1999. An amphipathic α-helix at a membrane interface: a structural study using a novel X-ray diffraction method. J. Mol. Biol. 290:99-117.
53. Hristova, K., C. E. Dempsey, and S. H. White. 2001. Structure, location, and lipid perturbations of melittin at the membrane interface. Biophys. J. 80:801-811.
54. Han, X., M. Mihailescu, and K. Hristova. 2006. Neutron diffraction studies of fluid bilayers with transmembrane proteins: structural conse quences of the achondroplasia mutation. Biophys. J. 91:3736-3747.
55. Merzlyakov, M., L. Chen, and K. Hristova. 2007. Studies of receptor tyrosine kinase transmembrane domain interactions: the EmEx-FRET method. J. Membr. Biol. 215:93-103.
56. Li, E., M. You, and K. Hristova. 2005. Sodium dodecyl sulfate-poly- acrylamide gel electrophoresis and Forster resonance energy transfer suggest weak interactions between FGFR3 TM domains in the absence of extracellular domains and ligands. Biochemistry. 44:352-360.
57. Posokhov, Y. O., M. Merzlyakov, A. S. Ladokhin. 2008. A simple "proximity" correction for Forster resonance energy transfer efficiency determination in membranes using lifetime measurements. Anal. Bio- chem. 380:134-136.
58. Wolber, P. K., and B. S. Hudson. 1979. An analytic solution to the Forster energy transfer problem in two dimensions. Biophys. J. 28:197-210.
59. Li, E., and K. Hristova. 2004. Imaging Forster resonance energy transfer measurements of transmembrane helix interactions in lipid bilayers on a solid support. Langmuir. 20:9053-9060.
60. Reference deleted in proof.
61. Hessa, T., S. H. White, and G. von Heijne. 2005. Membrane insertion of a potassium-channel voltage sensor. Science. 307:1427.
62. Hessa, T., H. Kim, G. von Heijne. 2005. Recognition of transmem- brane helices by the endoplasmic reticulum translocon. Nature. 433:377-381.
63. Snider, C., S. Jayasinghe, S. H. White. 2009. MPEx: a tool for exploring membrane proteins. Protein Sci. 18:2624-2628.