Cholesterol favors the anchorage of human dystrophin repeats 16 to 21 in membrane at physiological surface pressure

Biochimica et Biophysica Acta - Biomembranes

Volumn 1838, Issue 5, 2014, Pages 1266-1273

  Ameziane Le Hir, Sarah ^a,b,c   Raguénès Nicol, Céline ^a,b,c   Paboeuf, Gilles ^a,c   Nicolas, Aurélie ^a,b,c   Le Rumeur, Elisabeth ^a,b,c   Vié, Véronique ^a,c  

^a UNIVERSITÉ DE RENNES 1   (France)

^b UNIVERSITÉ DE RENNES 1   (France)

^c UNIVERSITÉ EUROPÉENNE DE BRETAGNE   (France)

Author keywords

Atomic force microscopy; CRAC sequence; Langmuir film; Muscular dystrophy; Protein lipid interaction; Spectrin superfamily

Indexed keywords

ANIONIC LIPID; CHOLESTEROL; DYSTROPHIN; LIPID; UNCLASSIFIED DRUG; ZWITTERIONIC LIPID;

ARTICLE; CONSENSUS SEQUENCE; CONTROLLED STUDY; HUMAN; HYDROPHILICITY; LANGMUIR BLODGETT FILM; LIPID MONOLAYER; LIQUID; MEMBRANE BINDING; MEMBRANE FLUIDITY; MOLECULAR RECOGNITION; NUCLEOTIDE SEQUENCE; PRESSURE GRADIENT; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN LIPID INTERACTION; SARCOLEMMA; STATIC ELECTRICITY; SURFACE PROPERTY;

ATOMIC FORCE MICROSCOPY; CRAC SEQUENCE; LANGMUIR FILM; MUSCULAR DYSTROPHY; PROTEIN LIPID INTERACTION; SPECTRIN SUPERFAMILY;

CELL MEMBRANE; CHOLESTEROL; DYSTROPHIN; HUMANS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; LIPID METABOLISM; MEMBRANE PROTEINS; MODELS, MOLECULAR; PRESSURE; PROTEIN BINDING; STATIC ELECTRICITY; SURFACE PROPERTIES;

EID: 84894579683     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2014.01.010     Document Type: Article

References (64)

1. M. Koenig, E.P. Hoffman, C.J. Bertelson, A.P. Monaco, C. Feener, and L.M. Kunkel Complete cloning of the Duchenne muscular dystrophy (DMD) cDNA and preliminary genomic organization of the DMD gene in normal and affected individuals Cell 50 1987 509 517
2. F. Pons, N. Augier, R. Heilig, J. Leger, D. Mornet, and J.J. Leger Isolated dystrophin molecules as seen by electron microscopy Proc. Natl. Acad. Sci. U. S. A. 87 1990 7851 7855
3. M. Muthu, K.A. Richardson, and A.J. Sutherland-Smith The crystal structures of dystrophin and utrophin spectrin repeats: implications for domain boundaries PLoS. One. 7 2012 e40066
4. M. Koenig, A.H. Beggs, M. Moyer, S. Scherpf, K. Heindrich, T. Bettecken, G. Meng, C.R. Muller, M. Lindlof, and H. Kaariainen et al. The molecular basis for Duchenne versus Becker muscular dystrophy: correlation of severity with type of deletion Am. J. Hum. Genet. 45 1989 498 506
5. K.S. Vishwanatha, Y.P. Wang, H.T. Keutmann, R.E. Mains, and B.A. Eipper Structural organization of the nine spectrin repeats of Kalirin Biochemistry 51 2012 5663 5673
6. W. Diakowski, A. Prychidny, M. Swistak, M. Nietubyc, K. Bialkowska, J. Szopa, and A.F. Sikorski Brain spectrin (fodrin) interacts with phospholipids as revealed by intrinsic fluorescence quenching and monolayer experiments Biochem. J. 338 Pt 1 1999 83 90
7. R.I. MacDonald Temperature and ionic effects on the interaction of erythroid spectrin with phosphatidylserine membranes Biochemistry 32 1993 6957 6964
8. R. Maksymiw, S.F. Sui, H. Gaub, and E. Sackmann Electrostatic coupling of spectrin dimers to phosphatidylserine containing lipid lamellae Biochemistry 26 1987 2983 2990
9. P.J. O'Toole, C. Wolfe, S. Ladha, and R.J. Cherry Rapid diffusion of spectrin bound to a lipid surface Biochim. Biophys. Acta 1419 1999 64 70
10. W. Diakowski, L. Ozimek, E. Bielska, S. Bem, M. Langner, and A.F. Sikorski Cholesterol affects spectrin-phospholipid interactions in a manner different from changes resulting from alterations in membrane fluidity due to fatty acyl chain composition Biochim. Biophys. Acta 1758 2006 4 12
11. S. Legardinier, C. Raguenes-Nicol, C. Tascon, C. Rocher, S. Hardy, J.F. Hubert, and E. Le Rumeur Mapping of the lipid-binding and stability properties of the central rod domain of human dystrophin J. Mol. Biol. 389 2009 546 558
12. V. Vie, S. Legardinier, L. Chieze, O. Le Bihan, Y. Qin, J. Sarkis, J.F. Hubert, A. Renault, B. Desbat, and E. Le Rumeur Specific anchoring modes of two distinct dystrophin rod sub-domains interacting in phospholipid Langmuir films studied by atomic force microscopy and PM-IRRAS Biochim. Biophys. Acta 1798 2010 1503 1511
13. M. Koenig, and L.M. Kunkel Detailed analysis of the repeat domain of dystrophin reveals four potential hinge segments that may confer flexibility J. Biol. Chem. 265 1990 4560 4566
14. N. Sahni, K. Mangat, E. Le Rumeur, and N. Menhart Exon edited dystrophin rods in the hinge 3 region Biochim. Biophys. Acta 1824 2012 1080 1089
15. G.B. Banks, L.M. Judge, J.M. Allen, and J.S. Chamberlain The polyproline site in hinge 2 influences the functional capacity of truncated dystrophins PLoS Genet. 6 2010 e1000958
16. A. Carsana, G. Frisso, M.R. Tremolaterra, R. Lanzillo, D.F. Vitale, L. Santoro, and F. Salvatore Analysis of dystrophin gene deletions indicates that the hinge III region of the protein correlates with disease severity Ann. Hum. Genet. 69 2005 253 259
17. A. Nicolas, C. Lucchetti-Miganeh, R.B. Yaou, J.C. Kaplan, J. Chelly, F. Leturcq, F. Barloy-Hubler, and E. Le Rumeur Assessment of the structural and functional impact of in-frame mutations of the DMD gene, using the tools included in the eDystrophin online database Orphanet. J. Rare Dis. 7 2012 45
18. Y. Lai, G.D. Thomas, Y. Yue, H.T. Yang, D. Li, C. Long, L. Judge, B. Bostick, J.S. Chamberlain, R.L. Terjung, and D. Duan Dystrophins carrying spectrin-like repeats 16 and 17 anchor nNOS to the sarcolemma and enhance exercise performance in a mouse model of muscular dystrophy J. Clin. Invest. 119 2009 624 635
19. D. Li, Y. Yue, Y. Lai, C.H. Hakim, and D. Duan Nitrosative stress elicited by nNOSmicro delocalization inhibits muscle force in dystrophin-null mice J. Pathol. 223 2011 88 98
20. J.M. Ervasti Dystrophin, its interactions with other proteins, and implications for muscular dystrophy Biochim. Biophys. Acta 1772 2007 108 117
21. J. Vega-Moreno, A. Tirado-Cortes, R. Alvarez, C. Irles, J. Mas-Oliva, and A. Ortega Cholesterol depletion uncouples beta-dystroglycans from discrete sarcolemmal domains, reducing the mechanical activity of skeletal muscle Cell. Physiol. Biochem. 29 2012 905 918
22. J.H. Davis, J.J. Clair, and J. Juhasz Phase equilibria in DOPC/DPPC-d62/cholesterol mixtures Biophys. J. 96 2009 521 539
23. R.J. Schroeder, S.N. Ahmed, Y. Zhu, E. London, and D.A. Brown Cholesterol and sphingolipid enhance the Triton X-100 insolubility of glycosylphosphatidylinositol-anchored proteins by promoting the formation of detergent-insoluble ordered membrane domains J. Biol. Chem. 273 1998 1150 1157
24. X.M. Li, M.M. Momsen, J.M. Smaby, H.L. Brockman, and R.E. Brown Cholesterol decreases the interfacial elasticity and detergent solubility of sphingomyelins Biochemistry 40 2001 5954 5963
25. R.B. Gennis Biomembranes: Molecular Structure and Function 1988 Springer
26. W. Guyer, and K. Bloch Phosphatidylcholine and cholesterol interactions in model membranes Chem. Phys. Lipids. 33 1983 313 322
27. R.M. Epand Cholesterol-rich domains: preface Biochim. Biophys. Acta Biomembr. 1610 2003 155 156
28. R. MacDonald The relationship and interactions between lipid bilayers, vesicles, and lipid monolayers at the air/water interface M. Rosoff, Vesicles 1996 CRC Press New York 3 48
29. D. Marsh Lateral pressure in membranes Biochim. Biophys. Acta 1286 1996 183 223
30. H. Li, and V. Papadopoulos Peripheral-type benzodiazepine receptor function in cholesterol transport. Identification of a putative cholesterol recognition/interaction amino acid sequence and consensus pattern Endocrinology 139 1998 4991 4997
31. E. Kahana, P.J. Marsh, A.J. Henry, M. Way, and W.B. Gratzer Conformation and phasing of dystrophin structural repeats J. Mol. Biol. 235 1994 1271 1277
32. S.J. Winder, T.J. Gibson, and J. Kendrick-Jones Dystrophin and utrophin: the missing links! FEBS Lett. 369 1995 27 33
33. S. Legardinier, J.F. Hubert, O. Le Bihan, C. Tascon, C. Rocher, C. Raguenes-Nicol, A. Bondon, S. Hardy, and E. Le Rumeur Sub-domains of the dystrophin rod domain display contrasting lipid-binding and stability properties Biochim. Biophys. Acta 1784 2008 672 682
34. N. Greenfield, and G.D. Fasman Computed circular dichroism spectra for the evaluation of protein conformation Biochemistry 8 1969 4108 4116
35. B. Berge, and A. Renault Ellipsometry study of 2D crystallization of 1-alcohol monolayers at the water surface Europhys. Lett. 21 1993 773 777
36. C. Bottier, J. Gean, B. Desbat, A. Renault, D. Marion, and V. Vie Structure and orientation of puroindolines into wheat galactolipid monolayers Langmuir 24 2008 10901 10909
37. L. Chieze, V.M. Bolanos-Garcia, M. Pinot, B. Desbat, A. Renault, S. Beaufils, and V. Vie Fluid and condensed ApoA-I/phospholipid monolayers provide insights into ApoA-I membrane insertion J. Mol. Biol. 410 2011 60 76
38. Y. Zhang I-TASSER server for protein 3D structure prediction BMC Bioinforma. 9 2008 40
39. B. Legrand, E. Giudice, A. Nicolas, O. Delalande, and E. Le Rumeur Computational study of the human dystrophin repeats: interaction properties and molecular dynamics PLoS One 6 2011 e23819
40. T.V. Pyrkov, A.O. Chugunov, N.A. Krylov, D.E. Nolde, and R.G. Efremov PLATINUM: a web tool for analysis of hydrophobic/hydrophilic organization of biomolecular complexes Bioinformatics 25 2009 1201 1202
41. N.A. Baker, D. Sept, S. Joseph, M.J. Holst, and J.A. McCammon Electrostatics of nanosystems: application to microtubules and the ribosome Proc. Natl. Acad. Sci. U.S.A. 98 2001 10037 10041
42. R.I. MacDonald, and E.V. Pozharski Free energies of urea and of thermal unfolding show that two tandem repeats of spectrin are thermodynamically more stable than a single repeat Biochemistry 40 2001 3974 3984
43. G.C. Chen, and J.P. Kane Circular dichroism of lipoprotein lipids Methods Enzymol. 128 1986 519 527
44. N.E. Zhou, C.M. Kay, and R.S. Hodges Synthetic model proteins. Positional effects of interchain hydrophobic interactions on stability of two-stranded alpha-helical coiled-coils J. Biol. Chem. 267 1992 2664 2670
45. Y. Desfougeres, A. Saint-Jalmes, A. Salonen, V. Vie, S. Beaufils, S. Pezennec, B. Desbat, V. Lechevalier, and F. Nau Strong improvement of interfacial properties can result from slight structural modifications of proteins: the case of native and dry-heated lysozyme Langmuir 27 2011 14947 14957
46. P. Calvez, S. Bussieres, D. Eric, and C. Salesse Parameters modulating the maximum insertion pressure of proteins and peptides in lipid monolayers Biochimie 91 2009 718 733
47. V. Vié, N. Van Mau, E. Lesniewska, J.P. Goudonnet, F. Heitz, and C. Le Grimellec Distribution of ganglioside GM1 between two-component, two-phase phosphatidylcholine monolayers Langmuir 14 1998 4574 4583
48. N. Jamin, J.M. Neumann, M.A. Ostuni, T.K. Vu, Z.X. Yao, S. Murail, J.C. Robert, C. Giatzakis, V. Papadopoulos, and J.J. Lacapere Characterization of the cholesterol recognition amino acid consensus sequence of the peripheral-type benzodiazepine receptor Mol. Endocrinol. 19 2005 588 594
49. J. Sarkis, J.F. Hubert, B. Legrand, E. Robert, A. Cheron, J. Jardin, E. Hitti, E. Le Rumeur, and V. Vie Spectrin-like repeats 11-15 of human dystrophin show adaptations to a lipidic environment J. Biol. Chem. 286 2011 30481 30491
50. C. DeWolf, P. McCauley, A.F. Sikorski, C.P. Winlove, A.I. Bailey, E. Kahana, J.C. Pinder, and W.B. Gratzer Interaction of dystrophin fragments with model membranes Biophys. J. 72 1997 2599 2604
51. E. Le Rumeur, J.F. Hubert, and S.J. Winder A new twist to coiled coil FEBS Lett. 586 2012 2717 2722
52. S. Manno, Y. Takakuwa, and N. Mohandas Identification of a functional role for lipid asymmetry in biological membranes: phosphatidylserine-skeletal protein interactions modulate membrane stability Proc. Natl. Acad. Sci. U. S. A. 99 2002 1943 1948
53. R. Saxena, and A. Chattopadhyay Membrane cholesterol stabilizes the human serotonin(1A) receptor Biochim. Biophys. Acta 1818 2012 2936 2942
54. A. Ciana, C. Balduini, and G. Minetti Detergent-resistant membranes in human erythrocytes and their connection to the membrane-skeleton J. Biosci. 30 2005 317 328
55. M. Grzybek, A. Chorzalska, E. Bok, A. Hryniewicz-Jankowska, A. Czogalla, W. Diakowski, and A.F. Sikorski Spectrin-phospholipid interactions. Existence of multiple kinds of binding sites? Chem. Phys. Lipids 141 2006 133 141
56. D.D. Doyle, G. Goings, J. Upshaw-Earley, S.K. Ambler, A. Mondul, H.C. Palfrey, and E. Page Dystrophin associates with caveolae of rat cardiac myocytes: relationship to dystroglycan Circ. Res. 87 2000 480 488
57. H.M. McConnell, and A. Radhakrishnan Condensed complexes of cholesterol and phospholipids Biochim. Biophys. Acta Biomembr. 1610 2003 159 173
58. J.R. Silvius Role of cholesterol in lipid raft formation: lessons from lipid model systems Biochim. Biophys. Acta Biomembr. 1610 2003 174 183
59. A. Radhakrishnan, and H.M. McConnell Electric field effect on cholesterol-phospholipid complexes Proc. Natl. Acad. Sci. U. S. A. 97 2000 1073 1078
60. J.R. Silvius Cholesterol modulation of lipid intermixing in phospholipid and glycosphingolipid mixtures. Evaluation using fluorescent lipid probes and brominated lipid quenchers Biochemistry 31 1992 3398 3408
61. J.A. Killian Hydrophobic mismatch between proteins and lipids in membranes Biochim. Biophys. Acta 1376 1998 401 415
62. R. Phillips, T. Ursell, P. Wiggins, and P. Sens Emerging roles for lipids in shaping membrane-protein function Nature 459 2009 379 385
63. R.M. Epand, A. Thomas, R. Brasseur, and R.F. Epand Cholesterol interaction with proteins that partition into membrane domains: an overview Subcell. Biochem. 51 2010 253 278
64. C.H. Lai, C.K. Lai, Y.J. Lin, C.L. Hung, C.H. Chu, C.L. Feng, C.S. Chang, and H.L. Su Characterization of putative cholesterol recognition/interaction amino acid consensus-like motif of Campylobacter jejuni cytolethal distending toxin C PLoS One 8 2013 e66202