Caveolin-1 hydrophobic segment peptides insertion into membrane mimetic systems: Role of Proline residue

Biochimica et Biophysica Acta - Biomembranes

Volumn 1818, Issue 1, 2012, Pages 12-18

  Aoki, Satoko ^a   Epand, Richard M ^a  

^a MCMASTER UNIVERSITY MEDICAL CENTRE   (Canada)

Author keywords

Caveolin 1; Hydrophobic segment; Monotopic protein; Re entrant helix; Transmembrane helix

Indexed keywords

CAVEOLIN 1; LYSINE; PROLINE;

ALPHA HELIX; AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; CAVEOLA; CIRCULAR DICHROISM; CONTROLLED STUDY; FLUORESCENCE ANALYSIS; GENE INSERTION; HYDROPHOBICITY; LIGHT SCATTERING; LIPID COMPOSITION; MICELLE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; TRANSPORT VESICLE;

ALANINE; AMINO ACID SEQUENCE; BIOMIMETICS; CAVEOLAE; CAVEOLIN 1; CHOLESTEROL; CIRCULAR DICHROISM; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; LIPID BILAYERS; LIPOSOMES; MOLECULAR SEQUENCE DATA; PEPTIDES; PROLINE; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; SPECTROMETRY, FLUORESCENCE;

EID: 80054874988     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2011.09.009     Document Type: Article

References (54)

1. R.G. Anderson The caveolae membrane system Annu. Rev. Biochem. 67 1998 199 225 (Pubitemid 28411129)
2. A.W. Cohen, T.P. Combs, P.E. Scherer, and M.P. Lisanti Role of caveolin and caveolae in insulin signaling and diabetes Am. J. Physiol. 285 2003 E1151 E1160 (Pubitemid 37464364)
3. P. Liu, M. Rudick, and R.G. Anderson Multiple functions of caveolin-1 J. Biol. Chem. 277 2002 41295 41298 (Pubitemid 35257426)
4. M. Isshiki, and R.G. Anderson Function of caveolae in Ca2+ entry and Ca2+-dependent signal transduction Traffic (Copenhagen, Denmark) 4 2003 717 723 (Pubitemid 37361853)
5. M. Isshiki, and R.G. Anderson Calcium signal transduction from caveolae Cell Calcium 26 1999 201 208 (Pubitemid 30003784)
6. P. Liu, Y. Ying, Y. Zhao, D.I. Mundy, M. Zhu, and R.G. Anderson Chinese hamster ovary K2 cell lipid droplets appear to be metabolic organelles involved in membrane traffic J. Biol. Chem. 279 2004 3787 3792 (Pubitemid 38140623)
7. C.J. Fielding, and P.E. Fielding Relationship between cholesterol trafficking and signaling in rafts and caveolae Biochim. Biophys. Acta 1610 2003 219 228 (Pubitemid 36324466)
8. F. Acconcia, P. Ascenzi, A. Bocedi, E. Spisni, V. Tomasi, A. Trentalance, P. Visca, and M. Marino Palmitoylation-dependent estrogen receptor alpha membrane localization: regulation by 17beta-estradiol Mol. Biol. Cell 16 2005 231 237 (Pubitemid 40028339)
9. P. Liu, Y. Ying, and R.G. Anderson Platelet-derived growth factor activates mitogen-activated protein kinase in isolated caveolae Proc. Natl. Acad. Sci. U.S.A. 94 1997 13666 13670 (Pubitemid 28009640)
10. C. Mineo, G.L. James, E.J. Smart, and R.G. Anderson Localization of epidermal growth factor-stimulated Ras/Raf-1 interaction to caveolae membrane J. Biol. Chem. 271 1996 11930 11935 (Pubitemid 26157268)
11. J.P. Gratton, P. Bernatchez, and W.C. Sessa Caveolae and caveolins in the cardiovascular system Circ. Res. 94 2004 1408 1417 (Pubitemid 38780313)
12. T.M. Williams, F. Medina, I. Badano, R.B. Hazan, J. Hutchinson, W.J. Muller, N.G. Chopra, P.E. Scherer, R.G. Pestell, and M.P. Lisanti Caveolin-1 gene disruption promotes mammary tumorigenesis and dramatically enhances lung metastasis in vivo. Role of Cav-1 in cell invasiveness and matrix metalloproteinase (MMP-2/9) secretion J. Biol. Chem. 279 2004 51630 51646 (Pubitemid 40017914)
13. T.M. Williams, and M.P. Lisanti Caveolin-1 in oncogenic transformation, cancer, and metastasis Am. J. Physiol. Cell Physiol. 288 2005 C494 C506 (Pubitemid 40229478)
14. S.B. Gaudreault, D. Dea, and J. Poirier Increased caveolin-1 expression in Alzheimer's disease brain Neurobiol. Aging 25 2004 753 759 (Pubitemid 38698250)
15. R. Hnasko, and M.P. Lisanti The biology of caveolae: lessons from caveolin knockout mice and implications for human disease Mol. Interv. 3 2003 445 464
16. P.G. Frank, S.E. Woodman, D.S. Park, and M.P. Lisanti Caveolin, caveolae, and endothelial cell function Arterioscler. Thromb. Vasc. Biol. 23 2003 1161 1168 (Pubitemid 36871269)
17. K. Simons, and R. Ehehalt Cholesterol, lipid rafts, and disease J. Clin. Invest. 110 2002 597 603 (Pubitemid 34988781)
18. T.M. Williams, and M.P. Lisanti The caveolin proteins Genome Biol. 5 2004 214
19. T. Okamoto, A. Schlegel, P.E. Scherer, and M.P. Lisanti Caveolins, a family of scaffolding proteins for organizing "preassembled signaling complexes" at the plasma membrane J. Biol. Chem. 273 1998 5419 5422 (Pubitemid 28123999)
20. A. Schlegel, and M.P. Lisanti A molecular dissection of caveolin-1 membrane attachment and oligomerization. Two separate regions of the caveolin-1 C-terminal domain mediate membrane binding and oligomer/oligomer interactions in vivo J. Biol. Chem. 275 2000 21605 21617 (Pubitemid 30481867)
21. S. Aoki, A. Thomas, M. Decaffmeyer, R. Brasseur, and R.M. Epand The role of proline in the membrane re-entrant helix of caveolin-1 J. Biol. Chem. 285 2010 33371 33380
22. S. Li, K.S. Song, and M.P. Lisanti Expression and characterization of recombinant caveolin. Purification by polyhistidine tagging and cholesterol-dependent incorporation into defined lipid membranes J. Biol. Chem. 271 1996 568 573
23. A. Schlegel, R.B. Schwab, P.E. Scherer, and M.P. Lisanti A role for the caveolin scaffolding domain in mediating the membrane attachment of caveolin-1. The caveolin scaffolding domain is both necessary and sufficient for membrane binding in vitro J. Biol. Chem. 274 1999 22660 22667
24. M. Sargiacomo, P.E. Scherer, Z. Tang, E. Kubler, K.S. Song, M.C. Sanders, and M.P. Lisanti Oligomeric structure of caveolin: implications for caveolae membrane organization Proc. Natl. Acad. Sci. U.S.A. 92 1995 9407 9411
25. B. Christiaens, S. Symoens, S. Verheyden, Y. Engelborghs, A. Joliot, A. Prochiantz, J. Vandekerckhove, M. Rosseneu, and B. Vanloo Tryptophan fluorescence study of the interaction of penetratin peptides with model membranes Eur. J. Biochem./FEBS 269 2002 2918 2926 (Pubitemid 34754020)
26. A.H. Pande, S. Qin, K.N. Nemec, X. He, and S.A. Tatulian Isoform-specific membrane insertion of secretory phospholipase A2 and functional implications Biochemistry 45 2006 12436 12447 (Pubitemid 44583686)
27. S.S. Antollini, Y. Xu, H. Jiang, and F.J. Barrantes Fluorescence and molecular dynamics studies of the acetylcholine receptor gammaM4 transmembrane peptide in reconstituted systems Mol. Membr. Biol. 22 2005 471 483
28. Y.M. Coic, M. Vincent, J. Gallay, F. Baleux, F. Mousson, V. Beswick, J.M. Neumann, and B. de Foresta Single-spanning membrane protein insertion in membrane mimetic systems: role and localization of aromatic residues Eur. Biophys. J. 35 2005 27 39 (Pubitemid 41667023)
29. B. de Foresta, M. Vincent, J. Gallay, and M. Garrigos Interaction with membrane mimics of transmembrane fragments 16 and 17 from the human multidrug resistance ABC transporter 1 (hMRP1/ABCC1) and two of their tryptophan variants Biochim. Biophys. Acta 1798 2010 401 414
30. A. Chattopadhyay, and E. London Parallax method for direct measurement of membrane penetration depth utilizing fluorescence quenching by spin-labeled phospholipids Biochemistry 26 1987 39 45
31. E. London, and G.W. Feigenson Fluorescence quenching in model membranes. 2. Determination of local lipid environment of the calcium adenosinetriphosphatase from sarcoplasmic reticulum Biochemistry 20 1981 1939 1948
32. E. London, and G.W. Feigenson Fluorescence quenching in model membranes. 1. Characterization of quenching caused by a spin-labeled phospholipid Biochemistry 20 1981 1932 1938
33. M.R. Eftink, and C.A. Ghiron Exposure of tryptophanyl residues in proteins. Quantitative determination by fluorescence quenching studies Biochemistry 15 1976 672 680
34. J.R. Lakowicz Principles of Fluorescence Spectroscopy Third Edition 2006 Springer Science + Business Media LLC, New York
35. G. Deleage, F.F. Clerc, and B. Roux ANTHEPROT: IBM PC and Apple Macintosh versions Comput. Appl. Biosci. 5 1989 159 160 (Pubitemid 19111832)
36. E. Glukhov, Y.V. Shulga, R.F. Epand, A.O. Dicu, M.K. Topham, C.M. Deber, and R.M. Epand Membrane interactions of the hydrophobic segment of diacylglycerol kinase epsilon Biochim. Biophys. Acta 1768 2007 2549 2558 (Pubitemid 47532034)
37. R.A. Melnyk, A.W. Partridge, and C.M. Deber Transmembrane domain mediated self-assembly of major coat protein subunits from Ff bacteriophage J. Mol. Biol. 315 2002 63 72 (Pubitemid 34722111)
38. R.A. Melnyk, A.W. Partridge, and C.M. Deber Retention of native-like oligomerization states in transmembrane segment peptides: application to the Escherichia coli aspartate receptor Biochemistry 40 2001 11106 11113 (Pubitemid 32847978)
39. C. Wang, and C.M. Deber Peptide mimics of the M13 coat protein transmembrane segment. retention of helix-helix interaction motifs J. Biol. Chem. 275 2000 16155 16159 (Pubitemid 30366926)
40. W.K. Subczynski, M. Pasenkiewicz-Gierula, R.N. McElhaney, J.S. Hyde, and A. Kusumi Molecular dynamics of 1-palmitoyl-2-oleoylphosphatidylcholine membranes containing transmembrane alpha-helical peptides with alternating leucine and alanine residues Biochemistry 42 2003 3939 3948 (Pubitemid 36402687)
41. R.A. Melnyk, A.W. Partridge, J. Yip, Y. Wu, N.K. Goto, and C.M. Deber Polar residue tagging of transmembrane peptides Biopolymers 71 2003 675 685 (Pubitemid 38325778)
42. M.R. de Planque, B.B. Bonev, J.A. Demmers, D.V. Greathouse, R.E. Koeppe II, F. Separovic, A. Watts, and J.A. Killian Interfacial anchor properties of tryptophan residues in transmembrane peptides can dominate over hydrophobic matching effects in peptide-lipid interactions Biochemistry 42 2003 5341 5348 (Pubitemid 36560430)
43. L.P. Liu, and C.M. Deber Anionic phospholipids modulate peptide insertion into membranes Biochemistry 36 1997 5476 5482 (Pubitemid 27200044)
44. A.S. Ladokhin, S. Jayasinghe, and S.H. White How to measure and analyze tryptophan fluorescence in membranes properly, and why bother? Anal. Biochem. 285 2000 235 245
45. S. Taneva, J.E. Johnson, and R.B. Cornell Lipid-induced conformational switch in the membrane binding domain of CTP:phosphocholine cytidylyltransferase: a circular dichroism study Biochemistry 42 2003 11768 11776 (Pubitemid 37243638)
46. E.A. Bryson, S.E. Rankin, M. Carey, A. Watts, and T.J. Pinheiro Folding of apocytochrome c in lipid micelles: formation of alpha-helix precedes membrane insertion Biochemistry 38 1999 9758 9767
47. H.H. de Jongh, and B. de Kruijff The conformational changes of apocytochrome c upon binding to phospholipid vesicles and micelles of phospholipid based detergents: a circular dichroism study Biochim. Biophys. Acta 1029 1990 105 112 (Pubitemid 20346428)
48. A. Gow, W. Auton, and R. Smith Interactions between bovine myelin basic protein and zwitterionic lysophospholipids Biochemistry 29 1990 1142 1147 (Pubitemid 20053834)
49. S.E. Rankin, A. Watts, and T.J. Pinheiro Electrostatic and hydrophobic contributions to the folding mechanism of apocytochrome c driven by the interaction with lipid Biochemistry 37 1998 12588 12595 (Pubitemid 28427543)
50. J.P. Hennessey Jr. , and W.C. Johnson Jr. Information content in the circular dichroism of proteins Biochemistry 20 1981 1085 1094
51. K.G. Rothberg, J.E. Heuser, W.C. Donzell, Y.S. Ying, J.R. Glenney, and R.G. Anderson Caveolin, a protein component of caveolae membrane coats Cell 68 1992 673 682
52. E. Spisni, V. Tomasi, A. Cestaro, and S.C. Tosatto Structural insights into the function of human caveolin 1 Biochem. Biophys. Res. Commun. 338 2005 1383 1390 (Pubitemid 41608405)
53. A. Karsan, J. Blonder, J. Law, E. Yaquian, D.A. Lucas, T.P. Conrads, and T. Veenstra Proteomic analysis of lipid microdomains from lipopolysaccharide- activated human endothelial cells J. Proteome Res. 4 2005 349 357 (Pubitemid 40548139)
54. R.M. Epand, B.G. Sayer, and R.F. Epand Caveolin scaffolding region and cholesterol-rich domains in membranes J. Mol. Biol. 345 2005 339 350 (Pubitemid 39574855)