The interaction of the Bax C-terminal domain with negatively charged lipids modifies the secondary structure and changes its way of insertion into membranes

Journal of Structural Biology

Volumn 164, Issue 1, 2008, Pages 146-152

  Ausili, Alessio ^a   Torrecillas, Alejandro ^a   Martínez Senac, María M ^a   Corbalán García, Senena ^a   Gómez Fernández, Juan C ^a  

^a UNIVERSITY OF MURCIA   (Spain)

Author keywords

Apoptosis; ATR FTIR; Bax; Infrared spectroscopy

Indexed keywords

GERMANIUM; MEMBRANE PROTEIN; PHOSPHATIDYLCHOLINE; PHOSPHATIDYLGLYCEROL; PHOSPHATIDYLINOSITOL; PROTEIN BAX;

ALPHA HELIX; AMINO ACID SEQUENCE; ARTICLE; BETA SHEET; CARBOXY TERMINAL SEQUENCE; FLUORESCENCE RESONANCE ENERGY TRANSFER; INFRARED SPECTROSCOPY; LIPID COMPOSITION; LIPID VESICLE; MEMBRANE STRUCTURE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN LIPID INTERACTION; PROTEIN SECONDARY STRUCTURE; PROTEIN STRUCTURE; STRUCTURE ANALYSIS;

BCL-2-ASSOCIATED X PROTEIN; BINDING SITES; IONS; LIPOSOMES; MEMBRANE LIPIDS; PEPTIDE FRAGMENTS; PHOSPHOLIPIDS; PROTEIN STRUCTURE, SECONDARY; SPECTROSCOPY, FOURIER TRANSFORM INFRARED; STATIC ELECTRICITY;

EID: 51549103252     PISSN: 10478477     EISSN: 10958657     Source Type: Journal    
DOI: 10.1016/j.jsb.2008.07.004     Document Type: Article

References (55)

1. Antonsson B., Conti F., Ciavatta A., Montessuit S., Lewis S., Martinou I., Bernasconi L., Bernard A., Mermod J.J., Mazzei G., Maundrell K., Gambale F., Sadoul R., and Martinou J.C. Inhibition of Bax channel-forming activity by Bcl-2. Science 277 (1997) 370-372
2. Arokium H., Camougrand N., Vallette F.M., and Manon S. Studies of the interaction of substituted mutants of BAX with yeast mitochondria reveal that the C-terminal hydrophobic alpha-helix is a second ART sequence and plays a role in the interaction with anti-apoptotic BCL-xL. J. Biol. Chem. 279 (2004) 52566-52573
3. Arrondo J.L., Muga A., Castresana J., and Goni F.M. Quantitative studies of the structure of proteins in solution by Fourier-transform infrared spectroscopy. Prog. Biophys. Mol. Biol. 59 (1993) 23-56
4. Banuelos S., Arrondo J.L., Goni F.M., and Pifat G. Surface-core relationships in human low density lipoprotein as studied by infrared spectroscopy. J. Biol. Chem. 270 (1995) 9192-9196
5. Barth A. The infrared absorption of amino acid side chains. Prog. Biophys. Mol. Biol. 74 (2000) 141-173
6. Bechinger B., Ruysschaert J.M., and Goormaghtigh E. Membrane helix orientation from linear dichroism of infrared attenuated total reflection spectra. Biophys. J. 76 (1999) 552-563
7. Cartron P.F., Priault M., Oliver L., Meflah K., Manon S., and Vallette F.M. The N-terminal end of Bax contains a mitochondrial-targeting signal. J. Biol. Chem. 278 (2003) 11633-11641
8. Chao D.T., and Korsmeyer S.J. BCL-2 family: regulators of cell death. Annu. Rev. Immunol. 16 (1998) 395-419
9. Corbalan-Garcia S., Sanchez-Carrillo S., Garcia-Garcia J., and Gomez-Fernandez J.C. Characterization of the membrane binding mode of the C2 domain of PKC epsilon. Biochemistry 42 (2003) 11661-11668
10. Cory S., and Adams J.M. The Bcl2 family: regulators of the cellular life-or-death switch. Nat. Rev. Cancer 2 (2002) 647-656
11. Del Mar Martinez-Senac M., Corbalan-Garcia S., and Gomez-Fernandez J.C. Study of the secondary structure of the C-terminal domain of the antiapoptotic protein bcl-2 and its interaction with model membranes. Biochemistry 39 (2000) 7744-7752
12. Del Mar Martinez-Senac M., Corbalan-Garcia S., and Gomez-Fernandez J.C. Conformation of the C-terminal domain of the pro-apoptotic protein Bax and mutants and its interaction with membranes. Biochemistry 40 (2001) 9983-9992
13. Del Mar Martínez-Senac M., Villalain J., and Gómez-Fernández J.C. Structure of the Alzheimer beta-amyloid peptide (25-35) and its interaction with negatively charged phospholipid vesicles. Eur. J. Biochem. 265 (1999) 744-753
14. Er L., Lalier L., Cartron P.F., Oliver L., and Vallette F.M. Control of Bax homodimerization by its carboxyl terminus. J. Biol. Chem. 282 (2007) 24938-24947
15. Fringeli U.P., and Gunthard H.H. Infrared membrane spectroscopy. Mol. Biol. Biochem. Biophys. 31 (1981) 270-332
16. Gao G., and Dou Q.P. N-terminal cleavage of bax by calpain generates a potent proapoptotic 18-kDa fragment that promotes bcl-2-independent cytochrome C release and apoptotic cell death. J. Cell. Biochem. 80 1981 (2000) 53-72
17. Goormaghtigh E., Cabiaux V., and Ruysschaert J.M. Determination of soluble and membrane protein structure by Fourier transform infrared spectroscopy. I. Assignments and model compounds. Subcell. Biochem. 23 (1994) 329-362
18. Goormaghtigh E., Cabiaux V., and Ruysschaert J.M. Determination of soluble and membrane protein structure by Fourier transform infrared spectroscopy. III. Secondary structures. Subcell. Biochem. 23 (1994) 405-450
19. Goormaghtigh E., Raussens V., and Ruysschaert J.M. Attenuated total reflection infrared spectroscopy of proteins and lipids in biological membranes. Biochim. Biophys. Acta 1422 (1999) 105-185
20. Goping I.S., Gross A., Lavoie J.N., Nguyen M., Jemmerson R., Roth K., Korsmeyer S.J., and Shore G.C. Regulated targeting of BAX to mitochondria. J. Cell. Biol. 143 (1998) 207-215
21. Green D.R. Apoptotic pathways: paper wraps stone blunts scissors. Cell 102 (2000) 1-4
22. Hengartner M.O. The biochemistry of apoptosis. Nature 407 (2000) 770-776
23. Hernández-Caselles T.J., Villalaín J., and Gómez-Fernández J.C. Influence of liposome charge and composition on their interaction with human blood serum proteins. Mol. Cell. Biochem. 120 (1993) 119-126
24. Jacobson M.D., Weil M., and Raff M.C. Programmed cell death in animal development. Cell 88 (1997) 347-354
25. Kelekar A., and Thompson C.B. Bcl-2-family proteins: the role of the BH3 domain in apoptosis. Trends Cell Biol. 8 (1998) 324-330
26. Kroemer G. The proto-oncogene Bcl-2 and its role in regulating apoptosis. Nat. Med. 3 (1997) 614-620
27. Li H., Kolluri S.K., Gu J., Dawson M.I., Cao X., Hobbs P.D., Lin B., Chen G., Lu J., Lin F., Xie Z., Fontana J.A., Reed J.C., and Zhang X. Cytochrome c release and apoptosis induced by mitochondrial targeting of nuclear orphan receptor TR3. Science 289 (2000) 1159-1164
28. Loeffler M., and Kroemer G. The mitochondrion in cell death control: certainties and incognita. Exp. Cell Res. 256 2000 (2000) 19-26
29. Maltseva E., Kerth A., Blume A., Mohwald H., and Brezesinski G. Adsorption of amyloid beta (1-40) peptide at phospholipid monolayers. Chembiochem 6 (2005) 1817-1824
30. Marsh D., Muller M., and Schmitt F.J. Orientation of the infrared transition moments for an alpha-helix. Biophys. J. 78 (2000) 2499-2510
31. Martinez-Senac Mdel M., Corbalan-Garcia S., and Gomez-Fernandez J.C. The structure of the C-terminal domain of the pro-apoptotic protein Bak and its interaction with model membranes. Biophys. J. 82 (2002) 233-243
32. Martinou J.C., and Green D.R. Breaking the mitochondrial barrier. Nat. Rev. Mol. Cell Biol. 2 (2001) 63-67
33. Minn A.J., Velez P., Schendel S.L., Liang H., Muchmore S.W., Fesik S.W., Fill M., and Thompson C.B. Bcl-x(L) forms an ion channel in synthetic lipid membranes. Nature 385 (1997) 353-357
34. Okada H., and Mak T.W. Pathways of apoptotic and non-apoptotic death in tumour cells. Nat. Rev. Cancer 4 (2004) 592-603
35. Oltvai Z.N., Milliman C.L., and Korsmeyer S.J. Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death. Cell 74 (1993) 609-619
36. Osborne H.B., and Nabedryk-Viala E. Infrared measurements of peptide hydrogen exchange in rhodopsin. Methods Enzymol. (1982) 676-680
37. Popovic M., De Biasio A., Pintar A., and Pongor S. The intracellular region of the Notch ligand Jagged-1 gains partial structure upon binding to synthetic membranes. FEBS J. 274 (2007) 5325-5336
38. Rankin S.E., Watts A., and Pinheiro T.J. Electrostatic and hydrophobic contributions to the folding mechanism of apocytochrome c driven by the interaction with lipid. Biochemistry 37 (1998) 12588-12595
39. Reed J.C. Double identity for proteins of the Bcl-2 family. Nature 387 (1997) 773-776
40. Salomaa P., Schaleger L.L., and Long F.A. Solvent deuterium isotope effects on acid-base equilibria. J. Am. Chem. Soc. 86 (1964) 1-7
41. Sani M.A., Loudet C., Grobner G., and Dufourc E.J. 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 (2007) 100-106
42. Schinzel A., Kaufmann T., Schuler M., Martinalbo J., Grubb D., and Borner C. Conformational control of Bax localization and apoptotic activity by Pro168. J. Cell Biol. 164 (2004) 1021-1032
43. Shimizu S., Narita M., and Tsujimoto Y. Bcl-2 family proteins regulate the release of apoptogenic cytochrome c by the mitochondrial channel VDAC. Nature 399 (1999) 483-487
44. Sperka-Gottlieb C.D., Hermetter A., Paltauf F., and Daum G. Lipid topology and physical properties of the outer mitochondrial membrane of the yeast, Saccharomyces cerevisiae. Biochim. Biophys. Acta 946 (1988) 227-234
45. Suzuki M., Youle R.J., and Tjandra N. Structure of Bax: coregulation of dimer formation and intracellular localization. Cell 103 (2000) 645-654
46. Thompson C.B. Apoptosis in the pathogenesis and treatment of disease. Science 267 (1995) 1456-1462
47. Torrecillas A., Corbalan-Garcia S., and Gomez-Fernandez J.C. Structural study of the C2 domains of the classical PKC isoenzymes using infrared spectroscopy and two-dimensional infrared correlation spectroscopy. Biochemistry 42 (2003) 11669-11681
48. Torrecillas A., Corbalan-Garcia S., and Gomez-Fernandez J.C. An infrared spectroscopic study of the secondary structure of protein kinase C alpha and its thermal denaturation. Biochemistry 43 (2004) 2332-2344
49. Torrecillas A., Martinez-Senac M.M., Ausili A., Corbalan-Garcia S., and Gomez-Fernandez J.C. Interaction of the C-terminal domain of Bcl-2 family proteins with model membranes. Biochim. Biophys. Acta 1768 (2007) 2931-2939
50. Torrecillas A., Martinez-Senac M.M., Goormaghtigh E., de Godos A., Corbalan-Garcia S., and Gomez-Fernandez J.C. Modulation of the membrane orientation and secondary structure of the C-terminal domains of Bak and Bcl-2 by lipids. Biochemistry 44 (2005) 10796-10809
51. Vaux D.L., Haecker G., and Strasser A. An evolutionary perspective on apoptosis. Cell 76 (1994) 777-779
52. 2+-ATPase of sarcoplasmic reticulum. Biochim. Biophys. Acta 978 (1989) 305-312
53. Wolter K.G., Hsu Y.T., Smith C.L., Nechushtan A., Xi X.G., and Youle R.J. Movement of Bax from the cytosol to mitochondria during apoptosis. J. Cell Biol. 139 (1997) 1281-1292
54. Yin X.M., Oltvai Z.N., and Korsmeyer S.J. BH1 and BH2 domains of Bcl-2 are required for inhibition of apoptosis and heterodimerization with Bax. Nature 369 (1994) 321-323
55. Youle R.J., and Strasser A. The BCL-2 protein family: opposing activities that mediate cell death. Nat. Rev. Mol. Cell Biol. 9 (2008) 47-59