Restriction of lipid motion in membranes triggered by β-sheet aggregation of the anti-apoptotic BH4 domain

FEBS Journal

Volumn 275, Issue 3, 2008, Pages 561-572

  Sani, Marc Antoine ^a,b   Castano, Sabine ^a   Dufourc, Erick J ^a   Gröbner, Gerhard ^b  

^a CNRS   (France)

^b UMEÅ UNIVERSITY   (Sweden)

Author keywords

Apoptosis; BH4 domain; Membrane; Protein lipid interactions; Solid state NMR

Indexed keywords

LIPOSOME; PEPTIDES AND PROTEINS; PROTEIN BCL 2; PROTEIN BH4; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; BETA SHEET; DIFFERENTIAL SCANNING CALORIMETRY; MEMBRANE STABILIZATION; MITOCHONDRIAL MEMBRANE; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN SECONDARY STRUCTURE; TEMPERATURE;

APOPTOSIS; HUMANS; MAGNETIC RESONANCE SPECTROSCOPY; MEMBRANE LIPIDS; MITOCHONDRIAL MEMBRANES; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; PROTO-ONCOGENE PROTEINS C-BCL-2; TEMPERATURE;

EID: 38149031026     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2007.06222.x     Document Type: Article

References (69)

1. Costantini P, Jacotot E, Decaudin D Kroemer G (2000) Mitochondrion as a novel target of anticancer chemotherapy. J Natl Cancer Inst 92, 1042 1053.
2. Hengartner MO (2000) The biochemistry of apoptosis. Nature 407, 770 776.
3. Okada H Mak TW (2004) Pathways of apoptotic and non-apoptotic death in tumour cells. Nat Rev Cancer 4, 592 603.
4. Thompson CB (1995) Apoptosis in the pathogenesis and treatment of disease. Science 267, 1456 1462.
5. Ono M, Sawa Y, Ryugo M, Alechine AN, Shimizu S, Sugioka R, Tsujimoto Y Matsuda H (2005) BH4 peptide derivative from Bcl-xL attenuates ischemia/reperfusion injury thorough anti-apoptotic mechanism in rat hearts. Eur J Cardiothorac Surg 27, 117 121.
6. Kerr JF, Wyllie AH Currie AR (1972) Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Vancer 26, 239 257.
7. Cory S Adams JM (2002) The BCL2 family: regulators of the cellular life-or-death switch. Nat Rev Cancer 2, 647 656.
8. Jacotot E, Ravagnan L, Loeffler M, Ferri KF, Vieira HL, Zamzami N, Costantini P, Druillennec S, Hoebeke J, Briand JP et al. (2000) The HIV-1 viral protein R induces apoptosis via a direct effect on the mitochondrial permeability transition pore. J Exp Med 191, 33 46.
9. Finucane DM, Bossy-Wetzel E, Waterhouse NJ, Cotter TG Green DR (1999) Bax-induced caspase activation and apoptosis via cytochrome c release from mitochondria is inhibitable by Bcl-xL. J Biol Chem 274, 2225 2233.
10. Li H, Kolluri SK, Gu J, Dawson MI, Cao X, Hobbs PD, Lin B, Chen G, Lu J, Lin F et al. (2000) Cytochrome c release and apoptosis induced by mitochondrial targeting of nuclear orphan receptor TR3. Science 289, 1159 1164.
11. Shimizu S, Narita M Tsujimoto Y (1999) Bcl-2 family proteins regulate the release of apoptogenic cytochrome c by the mitochondrial channel VDAC. Nature 399, 483 487.
12. Hanada M, Aime-Sempe C, Sato T Reed JC (1995) Structure-function analysis of Bcl-2 protein. Identification of conserved domains important for homodimerization with Bcl-2 and heterodimerization with Bax. J Biol Chem 270, 11962 11969.
13. Mikhailov V, Mikhailova M, Pulkrabek DJ, Dong Z, Venkatachalam MA Saikumar P (2001) Bcl-2 prevents Bax oligomerization in the mitochondrial outer membrane. J Biol Chem 276, 18361 18374.
14. Hotchkiss RS, McConnell KW, Bullok K, Davis CG, Chang KC, Schwulst SJ, Dunne JC, Dietz GP, Bahr M, McDunn JE et al. (2006) TAT-BH4 and TAT-Bcl-xL peptides protect against sepsis-induced lymphocyte apoptosis in vivo. J Immunol 176, 5471 5477.
15. Klein D, Ribeiro MM, Mendoza V, Jayaraman S, Kenyon NS, Pileggi A, Molano RD, Inverardi L, Ricordi C Pastori RL (2004) Delivery of Bcl-XL or its BH4 domain by protein transduction inhibits apoptosis in human islets. Biochem Biophys Res Commun 323, 473 478.
16. Sugioka R, Shimizu S, Funatsu T, Tamagawa H, Sawa Y, Kawakami T Tsujimoto Y (2003) BH4-domain peptide from Bcl-xL exerts anti-apoptotic activity in vivo. Oncogene 22, 8432 8440.
17. Shimizu S, Konishi A, Kodama T Tsujimoto Y (2000) BH4 domain of antiapoptotic Bcl-2 family members closes voltage-dependent anion channel and inhibits apoptotic mitochondrial changes and cell death. Proc Natl Acad Sci USA 97, 3100 3105.
18. Baines CP, Kaiser RA, Sheiko T, Craigen WJ Molkentin JD (2007) Voltage-dependent anion channels are dispensable for mitochondrial-dependent cell death. Nat Cell Biol 9, 550 555.
19. Jurgensmeier JM, Xie Z, Deveraux Q, Ellerby L, Bredesen D Reed JC (1998) Bax directly induces release of cytochrome c from isolated mitochondria. Proc Natl Acad Sci USA 95, 4997 5002.
20. Yethon JA, Epand RF, Leber B, Epand RM Andrews DW (2003) Interaction with a membrane surface triggers a reversible conformational change in Bax normally associated with induction of apoptosis. J Biol Chem 278, 48935 48941.
21. Green DR Reed JC (1998) Mitochondria and apoptosis. Science 281, 1309 1312.
22. Loeffler M Kroemer G (2000) The mitochondrion in cell death control: certainties and incognita. Exp Cell Res 256, 19 26.
23. Kroemer G Reed JC (2000) Mitochondrial control of cell death. Nat Med 6, 513 519.
24. Zamzami N Kroemer G (2001) The mitochondrion in apoptosis: how Pandora's box opens. Nat Rev Mol Cell Biol 2, 67 71.
25. Mabrey S Sturtevant JM (1976) Investigation of phase transitions of lipids and lipid mixtures by high sensitivity differential scanning calorimetry. Proc Natl Acad Sci USA 73, 3862 3866.
26. Ivanova VP, Makarov IM, Schaffer TE Heimburg T (2003) Analyzing heat capacity profiles of peptide-containing membranes: cluster formation of gramicidin A. Biophys J 84, 2427 2439.
27. Sturtevant JM (1982) A scanning calorimetric study of small molecule-lipid bilayer mixtures. Proc Natl Acad Sci USA 79, 3963 3967.
28. Davis JH (1983) The description of membrane lipid conformation, order and dynamics by H-2-Nmr. Biochim Biophys Acta 737, 117 171.
29. Seelig J Macdonald PM (1987) Phospholipids and proteins in biological membranes. Deuterium NMR as a method to study structure, dynamics, and interactions. Acc Chem Res 20, 221 228.
30. Dufourc EJ, Parish EJ, Chitrakorn S Smith ICP (1984) Structural and dynamical details of cholesterol-lipid interaction as revealed by deuterium NMR. Biochemistry 23, 6062 6071.
31. Dufourc EJ, Maillet JC, Pott T Leonard A (1993) P-31 NMR methods for investigating phospholipid-based molecular-structure and dynamics. Phosphorus Sulfur and Silicon 77, 673 676.
32. Dufourc EJ, Mayer C, Stohrer J Kothe G (1992) P-31 and H-1-NMR pulse sequences to measure lineshapes, T1z and T2e relaxation-times in biological-membranes. J Chim Phys Pcb 89, 243 252.
33. Seelig J (1978) 31P nuclear magnetic resonance and the head group structure of phospholipids in membranes. Biochim Biophys Acta 515, 105 140.
34. Lindstrom F, Williamson PT Grobner G (2005) Molecular insight into the electrostatic membrane surface potential by 14n/31p MAS NMR spectroscopy: nociceptin-lipid association. J Am Chem Soc 127, 6610 6616.
35. Rothgeb TM Oldfield E (1981) Nitrogen-14 nuclear magnetic resonance spectroscopy as a probe of lipid bilayer headgroup structure. J Biol Chem 256, 6004 6009.
36. Goormaghtigh E, Cabiaux V Ruysschaert JM (1994) Determination of soluble and membrane protein structure by Fourier transform infrared spectroscopy. III. Secondary structures. Subcell Biochem 23, 329 450.
37. Surewicz WK, Mantsch HH Chapman D (1993) Determination of protein secondary structure by Fourier transform infrared spectroscopy: a critical assessment. Biochemistry 32, 389 394.
38. Moore WH Krimm S (1976) Vibrational analysis of peptides, polypeptides, and proteins. II. beta-poly(L-alanine) and beta-poly(L-anaylglycine). Biopolymers 15, 2465 2483.
39. Goormaghtigh E, Cabiaux V Ruysschaert JM (1990) Secondary structure and dosage of soluble and membrane-proteins by attenuated total reflection Fourier-transform infrared-spectroscopy on hydrated films. Eur J Biochem 193, 409 420.
40. Goormaghtigh E, Raussens V Ruysschaert JM (1999) Attenuated total reflection infrared spectroscopy of proteins and lipids in biological membranes. Biochim Biophys Acta 1422, 105 185.
41. Castano S Desbat B (2005) Structure and orientation study of fusion peptide FP23 of gp41 from HIV-1 alone or inserted into various lipid membrane models (mono-, bi- and multibi-layers) by FT-IR spectroscopies and Brewster angle microscopy. Biochim Biophys Acta 1715, 81 95.
42. Heimburg T (2000) A model for the lipid pretransition: coupling of ripple formation with the chain-melting transition. Biophys J 78, 1154 1165.
43. Leonard A, Escrive C, Laguerre M, Pebay-Peyroula E, Neri W, Pott T, Katsaras J Dufourc EJ (2001) Location of cholesterol in DMPC membranes. A comparative study by neutron diffraction and molecular mechanics simulation. Langmuir 17, 2019 2030.
44. Weisz K, Grobner G, Mayer C, Stohrer J Kothe G (1992) Deuteron nuclear-magnetic-resonance study of the dynamic organization of phospholipid cholesterol bilayer-membranes - molecular-properties and viscoelastic behavior. Biochemistry 31, 1100 1112.
45. Dufourc EJ, Mayer C, Stohrer J, Althoff G Kothe G (1992) Dynamics of phosphate head groups in biomembranes - comprehensive analysis using P-31 nuclear-magnetic-resonance lineshape and relaxation-time measurements. Biophys J 61, 42 57.
46. Jarrell HC, Byrd RA Smith IC (1981) Analysis of the composition of mixed lipid phases by the moments of 2H NMR spectra. Biophys J 34, 451 463.
47. Lewis RN, Mak N McElhaney RN (1987) A differential scanning calorimetric study of the thermotropic phase behavior of model membranes composed of phosphatidylcholines containing linear saturated fatty acyl chains. Biochemistry 26, 6118 6126.
48. Mason JT (1998) Investigation of phase transitions in bilayer membranes. Methods Enzymol 295, 468 494.
49. Pukala TL, Boland MP, Gehman JD, Kuhn-Nentwig L, Separovic F Bowie JH (2007) Solution structure and interaction of cupiennin 1a, a spider venom peptide, with phospholipid bilayers. Biochemistry 46, 3576 3585.
50. Carbone MA Macdonald PM (1996) Cardiotoxin II segregates phosphatidylglycerol from mixtures with phosphatidylcholine: P-31 and H-2 NMR spectroscopic evidence. Biochemistry 35, 3368 3378.
51. Lindstrom F, Bokvist M, Sparrman T Grobner G (2002) Association of amyloid-beta peptide with membrane surfaces monitored by solid state NMR. Phys Chem Chem Phys 4, 5524 5530.
52. Semchyschyn DJ Macdonald PM (2004) Conformational response of the phosphatidylcholine headgroup to bilayer surface charge: torsion angle constraints from dipolar and quadrupolar couplings in bicelles. Magn Reson Chem 42, 89 104.
53. Smith R, Separovic F, Bennett FC Cornell BA (1992) Melittin-induced changes in lipid multilayers. A solid-state NMR study. Biophys J 63, 469 474.
54. Petros AM, Medek A, Nettesheim DG, Kim DH, Yoon HS, Swift K, Matayoshi ED, Oltersdorf T Fesik SW (2001) Solution structure of the antiapoptotic protein bcl-2. Proc Natl Acad Sci USA 98, 3012 3017.
55. Khemtemourian L, Sani MA, Bathany K, Grobner G Dufourc EJ (2006) Synthesis and secondary structure in membranes of the Bcl-2 anti-apoptotic domain BH4. J Pept Sci 12, 58 64.
56. Terzi E, Holzemann G Seelig J (1995) Self-association of beta-amyloid peptide (1-40) in solution and binding to lipid membranes. J Mol Biol 252, 633 642.
57. Terzi E, Holzemann G Seelig J (1997) Interaction of Alzheimer beta-amyloid peptide(1-40) with lipid membranes. Biochemistry 36, 14845 14852.
58. Constantinides PP, Inouchi N, Tritton TR, Sartorelli AC Sturtevant JM (1986) A scanning calorimetric study of the interaction of anthracyclines with neutral and acidic phospholipids alone and in binary mixtures. J Biol Chem 261, 10196 10203.
59. Halstenberg S, Heimburg T, Hianik T, Kaatze U Krivanek R (1998) Cholesterol-induced variations in the volume and enthalpy fluctuations of lipid bilayers. Biophys J 75, 264 271.
60. Heimburg T Biltonen RL (1996) A Monte Carlo simulation study of protein-induced heat capacity changes and lipid-induced protein clustering. Biophys J 70, 84 96.
61. Ivanova VP Heimburg T (2001) Histogram method to obtain heat capacities in lipid monolayers, curved bilayers, and membranes containing peptides. Phys Rev E 63, 1914 1926.
62. Huster D, Scheidt HA, Arnold K, Herrmann A Muller P (2005) Desmosterol may replace cholesterol in lipid membranes. Biophys J 88, 1838 1844.
63. Marsan MP, Muller I, Ramos C, Rodriguez F, Dufourc EJ, Czaplicki J Milon A (1999) Cholesterol orientation and dynamics in dimyristoylphosphatidylcholine bilayers: a solid state deuterium NMR analysis. Biophys J 76, 351 359.
64. Sani MA, Loudet C, Grobner G Dufourc EJ (2006) Pro-apoptotic bax-alpha1 synthesis and evidence for beta-sheet to alpha-helix conformational change as triggered by negatively charged lipid membranes. J Pept Sci 13, 100 106.
65. Epand RM Sturtevant JM (1981) A calorimetric study of peptide-phospholipid interactions: the glucagon-dimyristoylphosphatidylcholine complex. Biochemistry 20, 4603 4606.
66. Schuster B, Prassl R, Nigon F, Chapman MJ Laggner P (1995) Core lipid structure is a major determinant of the oxidative resistance of low density lipoprotein. Proc Natl Acad Sci USA 92, 2509 2513.
67. Davis JH (1979) Deuterium magnetic resonance study of the gel and liquid crystalline phases of dipalmitoyl phosphatidylcholine. Biophys J 27, 339 358.
68. Beck JG, Mathieu D, Loudet C, Buchoux S Dufourc EJ (2007) Plant sterols in 'rafts': a better way to regulate thermal shock to membranes. FASEB J 21, 1714 1723.
69. 14. J Chem Phys 55, 5829 5831.