Lipid packing variations induced by pH in cardiolipin-containing bilayers: The driving force for the cristae-like shape instability

Biochimica et Biophysica Acta - Biomembranes

Volumn 1808, Issue 11, 2011, Pages 2724-2733

  Khalifat, Nada ^a   Fournier, Jean Baptiste ^b   Angelova, Miglena I ^a,b   Puff, Nicolas ^a,b  

^a SORBONNE UNIVERSITÉ   (France)

^b UNIVERSITÉ PARIS DIDEROT   (France)

Author keywords

Cardiolipin; Curvature instability; GUV; Laurdan; Mitochondrion; pH

Indexed keywords

CARDIOLIPIN; LAURDAN;

CONTROLLED STUDY; FLUORESCENCE ANALYSIS; FORCE; LIPID BILAYER; LIPID MONOLAYER; MEMBRANE VESICLE; MITOCHONDRIAL MEMBRANE POTENTIAL; MOLECULAR DYNAMICS; PARTICLE SIZE; PH MEASUREMENT; PRIORITY JOURNAL; REVIEW; SURFACE CHARGE;

CARDIOLIPINS; HYDROGEN-ION CONCENTRATION; LIPID BILAYERS; MICROSCOPY; UNILAMELLAR LIPOSOMES;

EID: 80052265277     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2011.07.013     Document Type: Article

References (54)

1. T.H. Haines A new look at cardiolipin Biochimica et Biophysica Acta 1788 2009 1997 2002
2. R.N. Lewis, and R.N. McElhaney The physicochemical properties of cardiolipin bilayers and cardiolipin-containing lipid membranes Biochimica et Biophysica Acta 1788 2009 2069 2079
3. K.C. Huang, R. Mukhopadhyay, and N.S. Wingreen A curvature-mediated mechanism for localization of lipids to bacterial poles PLoS Computational Biology 2 2006 e151
4. K.E. McAuley, P.K. Fyfe, J.P. Ridge, N.W. Isaacs, R.J. Cogdell, and M.R. Jones Structural details of an interaction between cardiolipin and an integral membrane protein Proceedings of the National Academy of Sciences of the United States of America 96 1999 14706 14711 (Pubitemid 30019704)
5. M. Dahlberg Polymorphic phase behavior of cardiolipin derivatives studied by coarse-grained molecular dynamics The Journal of Physical Chemistry 111 2007 7194 7200 (Pubitemid 47152505)
6. R.N. Lewis, and R.N. McElhaney Surface charge markedly attenuates the nonlamellar phase-forming propensities of lipid bilayer membranes: calorimetric and (31)P-nuclear magnetic resonance studies of mixtures of cationic, anionic, and zwitterionic lipids Biophysical Journal 79 2000 1455 1464
7. M. Kates, S.Y.Z. Jing-Yi, D. Gosser, and H.T. Haines pH-Dissociation characteristics of cardiolipin and its 2′-deoxy analogue Lipids 28 1993 Springer Heidelberg 877
8. S. Nichols-Smith, and T. Kuhl Electrostatic interactions between model mitochondrial membranes Colloids and Surfaces 41 2005 121 127 (Pubitemid 40298825)
9. K.S. Eble, W.B. Coleman, R.R. Hantgan, and C.C. Cunningham Tightly associated cardiolipin in the bovine heart mitochondrial ATP synthase as analyzed by 31P nuclear magnetic resonance spectroscopy The Journal of Biological Chemistry 265 1990 19434 19440 (Pubitemid 120013882)
10. L.I. Horvath, M. Drees, K. Beyer, M. Klingenberg, and D. Marsh Lipid-protein interactions in ADP-ATP carrier/egg phosphatidylcholine recombinants studied by spin-label ESR spectroscopy Biochemistry 29 1990 10664 10669
11. K. Pfeiffer, V. Gohil, R.A. Stuart, C. Hunte, U. Brandt, M.L. Greenberg, and H. Schägger Cardiolipin stabilizes respiratory chain supercomplexes The Journal of Biological Chemistry 278 2003 52873 52880 (Pubitemid 38035887)
12. N.C. Robinson Functional binding of cardiolipin to cytochrome c oxidase Journal of Bioenergetics and Biomembranes 25 1993 153 163 (Pubitemid 23133523)
13. J. Llopis, J.M. McCaffery, A. Miyawaki, M.G. Farquhar, and R.Y. Tsien Measurement of cytosolic, mitochondrial, and Golgi pH in single living cells with green fluorescent proteins Proceedings of the National Academy of Sciences of the United States of America 95 1998 6803 6808 (Pubitemid 28278061)
14. T.H. Haines, and N.A. Dencher Cardiolipin: a proton trap for oxidative phosphorylation FEBS Letters 528 2002 35 39 (Pubitemid 35257995)
15. D.C. Logan The mitochondrial compartment Journal of Experimental Botany 57 2006 1225 1243
16. C.A. Mannella, M. Marko, and K. Buttle Reconsidering mitochondrial structure: new views of an old organelle Trends in Biochemical Sciences 22 1997 37 38 (Pubitemid 27076802)
17. T.G. Frey, C.W. Renken, and G.A. Perkins Insight into mitochondrial structure and function from electron tomography Biochimica et Biophysica Acta 1555 2002 196 203 (Pubitemid 35246028)
18. C.A. Mannella The relevance of mitochondrial membrane topology to mitochondrial function Biochimica et Biophysica Acta 1762 2006 140 147 (Pubitemid 43006021)
19. C.A. Mannella Structure and dynamics of the mitochondrial inner membrane cristae Biochimica et Biophysica Acta 1763 2006 542 548 (Pubitemid 44015951)
20. N.V. Dudkina, J. Heinemeyer, W. Keegstra, E.J. Boekema, and H.P. Braun Structure of dimeric ATP synthase from mitochondria: an angular association of monomers induces the strong curvature of the inner membrane FEBS Letters 579 2005 5769 5772 (Pubitemid 41455662)
21. M.F. Giraud, P. Paumard, V. Soubannier, J. Vaillier, G. Arselin, B. Salin, J. Schaeffer, D. Brethes, J.P. di Rago, and J. Velours Is there a relationship between the supramolecular organization of the mitochondrial ATP synthase and the formation of cristae? Biochimica et Biophysica Acta 1555 2002 174 180 (Pubitemid 35246024)
22. M. Strauss, G. Hofhaus, R.R. Schroder, and W. Kuhlbrandt Dimer ribbons of ATP synthase shape the inner mitochondrial membrane The EMBO Journal 27 2008 1154 1160 (Pubitemid 351508145)
23. E. Mileykovskaya, and W. Dowhan Cardiolipin membrane domains in prokaryotes and eukaryotes Biochimica et Biophysica Acta 1788 2009 2084 2091
24. D. Acehan, Y. Xu, D.L. Stokes, and M. Schlame Comparison of lymphoblast mitochondria from normal subjects and patients with Barth syndrome using electron microscopic tomography Laboratory Investigation 87 2006 40 48 (Pubitemid 44973652)
25. M. Dahlberg, and A. Maliniak Molecular dynamics simulations of cardiolipin bilayers The Journal of Physical Chemistry 112 2008 11655 11663
26. M. Dahlberg, and A. Maliniak Mechanical properties of coarse-grained bilayers formed by cardiolipin and zwitterionic lipids Journal of Chemical Theory and Computation 6 2010 1638 1649
27. T. Rog, H. Martinez-Seara, N. Munck, M. Oresic, M. Karttunen, and I. Vattulainen Role of cardiolipins in the inner mitochondrial membrane: insight gained through atom-scale simulations The Journal of Physical Chemistry 113 2009 3413 3422
28. O. Domenech, L. Redondo, L. Picas, A. Morros, M.T. Montero, and J. Hernandez-Borrell Atomic force microscopy characterization of supported planar bilayers that mimic the mitochondrial inner membrane Journal of Molecular Recognition 20 2007 546 553
29. O. Domenech, F. Sanz, M.T. Montero, and J. Hernandez-Borrell Thermodynamic and structural study of the main phospholipid components comprising the mitochondrial inner membrane Biochimica et Biophysica Acta 1758 2006 213 221 (Pubitemid 44294662)
30. S. Nichols-Smith, S.Y. Teh, and T.L. Kuhl Thermodynamic and mechanical properties of model mitochondrial membranes Biochimica et Biophysica Acta 1663 2004 82 88 (Pubitemid 38625582)
31. S. Sennato, F. Bordi, C. Cametti, C. Coluzza, A. Desideri, and S. Rufini Evidence of domain formation in cardiolipin-glycerophospholipid mixed monolayers. A thermodynamic and AFM study The Journal of Physical Chemistry 109 2005 15950 15957 (Pubitemid 41321513)
32. C.A. Mannella, M. Marko, and K. Buttle Reconsidering mitochondrial structure: new views of an old organelle Trends in Biochemical Sciences 22 1997 37 38 (Pubitemid 27076802)
33. R.J.P. Williams Mitochondria and chloroplasts: localized and delocalized bioenergetic transduction Trends in Biochemical Sciences 25 2000 479
34. N. Khalifat, N. Puff, S. Bonneau, J.-B. Fournier, and M.I. Angelova Membrane deformation under local pH gradient: mimicking mitochondrial cristae dynamics Biophysical Journal 2008 biophysj.108.136077
35. A.F. Bitbol, J.B. Fournier, M.I. Angelova, and N. Puff Dynamical membrane curvature instability controlled by intermonolayer friction Journal of Physics. Condensed Matter 23 2011 284102
36. J.B. Fournier, N. Khalifat, N. Puff, and M.I. Angelova Chemically triggered ejection of membrane tubules controlled by intermonolayer friction Physical Review Letters 102 2009 018102
37. L.A. Bagatolli, T. Parasassi, G.D. Fidelio, and E. Gratton A model for the interaction of 6-lauroyl-2-(N,N-dimethylamino)naphthalene with lipid environments: implications for spectral properties Photochemistry and Photobiology 70 1999 557 564 (Pubitemid 129555823)
38. K. Christensen, H.S. Bose, F.M. Harris, W.L. Miller, and J.D. Bell Binding of steroidogenic acute regulatory protein to synthetic membranes suggests an active molten globule The Journal of Biological Chemistry 276 2001 17044 17051
39. T. Nyholm, M. Nylund, A. Soderholm, and J.P. Slotte Properties of palmitoyl phosphatidylcholine, sphingomyelin, and dihydrosphingomyelin bilayer membranes as reported by different fluorescent reporter molecules Biophysical Journal 84 2003 987 997 (Pubitemid 36133424)
40. T. Parasassi, G. De Stasio, A. d'Ubaldo, and E. Gratton Phase fluctuation in phospholipid membranes revealed by Laurdan fluorescence Biophysical Journal 57 1990 1179 1186 (Pubitemid 20203441)
41. R.C. MacDonald, R.I. MacDonald, B.P. Menco, K. Takeshita, N.K. Subbarao, and L.R. Hu Small-volume extrusion apparatus for preparation of large, unilamellar vesicles Biochimica et Biophysica Acta 1061 1991 297 303
42. D.E. Budil, S. Lee, S. Saxena, and J.H. Freed Nonlinear-least-squares analysis of slow-motion EPR spectra in one and two dimensions using a modified Levenberg-Marquardt algorithm Journal of Magnetic Resonance, Series A 120 1996 155 189 (Pubitemid 126751752)
43. M.I. Angelova, and D.S. Dimitrov A mechanism of liposome electroformation Progress in Colloid and Polymer Science 76 1988 59 67
44. N. Puff, A. Lamaziere, M. Seigneuret, G. Trugnan, and M.I. Angelova HDLs induce raft domain vanishing in heterogeneous giant vesicles Chemistry and Physics of Lipids 133 2005 195 202 (Pubitemid 40092118)
45. A. Bruce Skeletal muscle lipids. II. Changes in phospholipid composition in man from fetal to middle age Journal of Lipid Research 15 1974 103 108
46. G. Daum, and J.E. Vance Import of lipids into mitochondria Progress in Lipid Research 36 1997 103 130 (Pubitemid 28045908)
47. B. Gomez Jr., and N.C. Robinson Quantitative determination of cardiolipin in mitochondrial electron transferring complexes by silicic acid high-performance liquid chromatography Analytical Biochemistry 267 1999 212 216 (Pubitemid 29061824)
48. Q.-P. Chen, and Q.-T. Li Effect of cardiolipin on proton permeability of phospholipid liposomes: the role of hydration at the lipid-water interface Archives of Biochemistry and Biophysics 389 2001 201 206 (Pubitemid 32881946)
49. P. Soucaille, M. Prats, J.F. Tocanne, and J. Teissie Use of a fluorescein derivative of phosphatidylethanolamine as a pH probe at water/lipid interfaces Biochimica et Biophysica Acta 939 1988 289 294 (Pubitemid 18088778)
50. J.-F. Tocanne, and J. Teissié Ionization of phospholipids and phospholipid-supported interfacial lateral diffusion of protons in membrane model systems Biochimica et Biophysica Acta (BBA) - Reviews on Biomembranes 1031 1990 111 142
51. Y. Zhou, and R.M. Raphael Solution pH alters mechanical and electrical properties of phosphatidylcholine membranes: relation between interfacial electrostatics, intramembrane potential, and bending elasticity Biophysical Journal 92 2007 2451 2462 (Pubitemid 46536427)
52. N. Vila-Romeu, M. Nieto-Suárez, and M. Broniatowski The interaction of cyclodextrins with phosphatidylethanolamine Langmuir monolayers: influence of the spreading solvent and subphase conditions Thin Solid Films 516 2008 8852 8859
53. M. Fujiwara, R.H. Grubbs, and J.D. Baldeschwieler Characterization of pH-dependent poly(acrylic acid) complexation with phospholipid vesicles Journal of Colloid and Interface Science 185 1997 210 216 (Pubitemid 27462730)
54. Y. Nozaki, and C. Tanford Proton and hydroxide ion permeability of phospholipid vesicles Proceedings of the National Academy of Sciences 78 1981 4324 4328