Helix orientations in membrane-associated Bcl-XL determined by 15N-solid-state NMR spectroscopy

European Biophysics Journal

Volumn 37, Issue 1, 2007, Pages 71-80

  Aisenbrey, Christopher ^a,b   Sudheendra, U S ^a   Ridley, Helen ^c   Bertani, Philippe ^a   Marquette, Arnaud ^a   Nedelkina, Svetlana ^a   Lakey, Jeremy H ^c   Bechinger, Burkhard ^a  

^a UNIVERSITÉ LOUIS PASTEUR   (France)

^b UMEÅ UNIVERSITY   (Sweden)

^c NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

Apoptosis; Cancer; Helix tilt angle; Membrane protein structure; Oriented lipid bilayer; Protein protein interactions; Topology

Indexed keywords

PROTEIN BCL X;

ARTICLE; MEMBRANE POTENTIAL; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN INTERACTION;

BCL-X PROTEIN; COMPUTER SIMULATION; LIPID BILAYERS; MAGNETIC RESONANCE SPECTROSCOPY; MEMBRANE FLUIDITY; MODELS, CHEMICAL; MODELS, MOLECULAR; NITROGEN ISOTOPES; PROTEIN CONFORMATION;

EID: 36349002883     PISSN: 01757571     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00249-007-0165-z     Document Type: Article

References (50)

1. Adams JM, Cory S (2001) Life-or-death decisions by the Bcl-2 protein family. Trends Biochem Sci 26:61-68
2. Aisenbrey C, Bechinger B (2004a) Investigations of peptide rotational diffusion in aligned membranes by 2H and 15N solid-state NMR spectroscopy. J Am Chem Soc 126:16676-16683
3. Aisenbrey C, Bechinger B (2004b) Tilt and rotational pitch angles of membrane-inserted polypeptides from combined 15N and 2H solid-state NMR spectroscopy. Biochemistry 43:10502-10512
4. Aisenbrey C, Harzer U, Bauer-Manz G, Bär G, Husmal Chotimah IN, Bertani P, Sizun C, Kuhn A, Bechinger B (2006) Proton-decoupled 15N and 31P solid-state NMR investigations of the Pf3 coat protein in oriented phospholipid bilayers. FEBS J 273:817-828
5. Anderluh G, Gokce I, Lakey JH (2003) Expression of proteins using the third domain of the Escherichia coli periplasmic-protein TolA as a fusion partner. Protein Expr Purif 28:173-181
6. Antonsson B, Contin F, Ciavatta A, Montesuit S, Elwis S, Marinou I, Bernasconi L, Bernard A, Mermod JJ, Mazzei G (1997) Inhibition of Bax channel-forming activity by Bcl-2. Science 277:370-372
7. α- fluorenyllmethoxycarbonylamino-acids on polyamide supports. Synthesis of substance P and of acyl carrier proteins 65-74 decapeptide. J Chem Soc Perkin Trans I 538-546
8. Basanez G, Nechushtan A, Drozhinin O, Chanturiya A, Choe E, Tutt S, Wood KA, Hsu Y, Zimmerberg J, Youle RJ (1999) Bax, but not Bcl-xL, decreases the lifetime of planar phospholipid bilayer membranes at subnanomolar concentrations. Proc Natl Acad Sci USA 96:5492-5497
9. Bechinger B, Opella SJ (1991) Flat-coil probe for NMR spectroscopy of oriented membrane samples. J Magn Reson 95:585-588
10. Bechinger B, Sizun C (2003) Alignment and structural analysis of membrane polypeptides by 15N and 31P solid-state NMR spectroscopy. Concepts Magn Reson 18A:130-145
11. Bechinger B, Aisenbrey C, Bertani P (2004) Topology, structure and dynamics of membrane-associated peptides by solid-state NMR spectroscopy. Biochim Biophys Acta 1666:190-204
12. Borner C (2003) The Bcl-2 protein family: sensors and checkpoints for life-or-death decisions. Mol Immunol 39:615-647
13. Butler LM, Hewett PJ, Fitridge RA, Cowled PA (1999) Deregulation of apoptosis in colorectal carcinoma: theoretical and therapeutic implications. Aust N Z J Surg 69:88-94
14. Carpino LA, Han GY (1972) The 9-fluorenylmethoxycarbonylamino-protecting group. J Org Chem 37: 3404
15. Chao DT, Korsmeyer SJ (1998) BCL-2 family: regulators of cell death Ann Rev Immunol 16:395-419
16. Choe S, Bennett MJ, Fujii G, Curmi PM, Kantardjieff KA, Collier RJ, Eisenberg D (1992) The crystal structure of diphtheria toxin. Nature 357:216-222
17. Cross TA (1997) Solid-state nuclear magnetic resonance characterization of gramicidin channel structure. Meth Enzymol 289:672-696
18. Day CL, Chen L, Richardson SJ, Harrison PJ, Huang DC, Hinds MG (2005) Solution structure of prosurvival mcl-1 and characterization of its binding by proapoptotic bh3-only ligands. J Biol Chem 280:4738-4744
19. Denisov AY, Madiraju MS, Chen G, Khadir A, Beauparlant P, Attardo G, Shore GC, Gehring K (2003) Solution structure of human BCL-w: modulation of ligand binding by the C-terminal helix. J Biol Chem 278:21124-21128
20. Franzin CM, Choi J, Zhai D, Reed JC, Marassi FM (2004) Structural studies of apoptosis and ion transport regulatory proteins in membranes. Magn Reson Chem 42:172-179
21. Garcia-Saez AJ, Mingarro I, Perez-Paya E, Salgado J (2004) Membrane-insertion fragments of Bcl-xL, Bax, and Bid. Biochemistry 43:10930-10943
22. Haack T, Mutter M (1992) Serine derived oxazolidines as secondary structure disrupting, solubilizing building blocks in peptide synthesis. Tetrahedron Lett 33:1589-1592
23. Häcker G, Vaux DL (1995) Apoptosis: a sticky business. Curr Biol 5:622-624
24. Hinds MG, Lackmann M, Skea GL, Harrison PJ, Huang DC, Day CL (2003) The structure of Bcl-w reveals a role for the C-terminal residues in modulating biological activity. EMBO J 22:1497-1507
25. Huang Q, Petros AM, Virgin HW, Fesik SW, Olejniczak ET (2002) Solution structure of a Bcl-2 homolog from Kaposi sarcoma virus. Proc Natl Acad Sci USA 99:3428-3433
26. Huang Q, Petros AM, Virgin HW, Fesik SW, Olejniczak ET (2003) Solution structure of the BHRF1 protein from Epstein-Barr virus, a homolog of human Bcl-2. J Mol Biol 332:1123-1130
27. Kaufmann T, Schlipf S, Sanz J, Neubert K, Stein R, Borner C (2003) Characterization of the signal that directs Bcl-x(L), but not Bcl-2, to the mitochondrial outer membrane. J Cell Biol 160:53-64
28. Kim PK, Annis MG, Dlugosz PJ, Leber B, Andrews DW (2004) During apoptosis bcl-2 changes membrane topology at both the endoplasmic reticulum and mitochondria. Mol Cell 14:523-529
29. Kluck RM, Bossy-Wetzel E, Green DR, Newmeyer DD (1997) The release of cytochrome c friom mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science 275:1132-1136
30. Levitt MH, Suter D, Ernst RR (1986) Spin dynamics and thermodynamics in solid-state NMR cross polarization J Chem Phys 84:4243-4255
31. Losonczi JA, Olejniczak ET, Betz SF, Harlan JE, Mack J, Fesik SW (2000) NMR studies of the anti-apoptotic protein Bcl-x(L) in micelles. Biochemistry 39:11024-11033
32. Merry DE, Korsmeyer SJ (1997) Bcl-2 gene family in the nervous system. Annu Rev Neurosci 20:245-267
33. L forms an ion channel in synthetic lipid membranes. Nature 385:353-357
34. Muchmore SW, Sattler M, Liang H, Meadows RP, Harlan JE, Yoon HS, Nettesheim D, Chang BS, Thompson CB, Wong SL, Ng SL, Fesik SW (1996) X-ray and NMR structure of human Bcl-xL, an inhibitor of programmed cell death. Nature 381:335-341
35. O'Brien FEM (1948) The control of humidity by saturated salt solutions. J Sci Instr 25:73-76
36. Parker MW, Postma JP, Pattus F, Tucker AD, Tsernoglou D (1992) Refined structure of the pore-forming domain of colicin A at 2.4 A resolution. J Mol Biol 224:639-657
37. Petros AM, Olejniczak ET, Fesik SW (2004) Structural biology of the Bcl-2 family of proteins. Biochim Biophys Acta 1644:83-94
38. Phillips AJ, Crowe JD, Ramsdale M (2006) Ras pathway signaling accelerates programmed cell death in the pathogenic fungus Candida albicans. Proc Natl Acad Sci USA 103:726-731
39. Priault M, Camougrand N, Chaudhuri B, Manon S (1999) Role of the C-terminal domain of Bax and Bcl-XL in their localization and function in yeast cells. FEBS Lett 443:225-228
40. Prongidi Fix L (2005) Structural and thermodynamic investigations of membrane-associated polypeptides and peptide/DNA transfection complexes. Ph.D thesis, University Louis Pasteur Strasbourg
41. Sattler M, Liang H, Nettesheim D, Meadows RP, Harlan JE, Eberstadt M, Yoon HS, Shuker SB, Chang BS, Minn AJ, Thompson CB, Fesik SW (1997) Structure of Bcl-xL-Bak peptide complex: recognition between regulators of apoptosis. Science 275:983-986
42. Schendel SL, Xie Z, Montal MO, Matsuyama SMMRJC (1997) Channel-formation by anti-apoptotic protein Bcl-2. Proc Natl Acad Sci USA 93:5113-5118
43. Schendel SL, Montal M, Reed JC (1998) Bcl-2 family proteins as ion-channels. Cell Death Differ 5:372-380
44. Schlesinger PH, Gross A, Yin X-M, Yamamoto K, Saito M, Waksman G, Korsmeyer SJ (1997) Comparison of the ion-channel characteristics of proapototic Bax and antiapoptotic Bcl-2. Proc Natl Acad Sci USA 94:11357-11362
45. Suzuki M, Youle RJ, Tjandra N (2000) Structure of Bax: coregulation of dimer formation and intracellular localization. Cell 103:645-654
46. Thuduppathy GR, Hill RB (2006) Acid destabilization of the solution conformation of Bcl-xL does not drive its pH-dependent insertion into membranes. Protein Sci 15:248-257
47. Thuduppathy GR, Craig JW, Kholodenko V, Schon A, Hill RB (2006) Evidence that membrane insertion of the cytosolic domain of Bcl-x(L) is governed by an electrostatic mechanism. J Mol Biol 359:1045-1058
48. Vetter IR, Parker MW, Tucker AD, Lakey JH, Pattus F, Tsernoglou D (1998) Crystal structure of a colicin N fragment suggests a model for toxicity. Structure 6:863-874
49. Zamzami N, Susin SA, Marchetti P, Hirsch T, Gomez-Monterrey I, Castedo M, Kroemer G (1996) Mitochondrial control of nuclear apoptosis. J Exp Med 183:1533-1544
50. Zoratti M, Szabo I (1995) The mitochondrail permeability transition. Biochim Biophys Acta 1241:139-176