Role of chirality in peptide-induced formation of cholesterol-rich domains

Biochemical Journal

Volumn 390, Issue 2, 2005, Pages 541-548

  Epand, Richard M ^a   Rychnovsky, Scott D ^b   Belani, Jitendra D ^b   Epand, Raquel F ^a  

^a MCMASTER UNIVERSITY   (Canada)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Chirality; Cholesterol; Cholesterol enantiomer; CRAC motif; Membrane domain; Neuronal axonal membrane protein (NAP 22)

Indexed keywords

AMINO ACIDS; BIOLOGICAL MEMBRANES; ISOMERS; PHASE TRANSITIONS; PHOSPHOLIPIDS; POLYPEPTIDES; PROTEINS;

CHIRALITY; CHOLESTEROL ENANTIOMERS; CRAC MOTIF; MEMBRANE DOMAIN; NEURONAL AXONAL MEMBRANE PROTEIN (NAP-22);

CHOLESTEROL;

1 STEAROYL 2 OLEOYLPHOSPHATIDYLCHOLINE; ACETYLLEUCYLTRYPTOPHANYLTYROSYLISOLEUCYLLYSINAMIDE; CHOLESTEROL; MEMBRANE PROTEIN; MYRISTOYLGLYCYLGLYCYLLYSYLLEUCYLSERYLLYSYLLYSYLLYSYLLYSYLGLYSYLTYROSYLASPARAGINYLVALYLASPARAGINYLASPARTYLGLUTAMYLLYSYLALANYLLYSINAMIDE; PEPTIDE; PHOSPHATIDYLCHOLINE; PROTEIN NAP 22; UNCLASSIFIED DRUG;

ARTICLE; CHEMICAL STRUCTURE; CHIRALITY; CIRCULAR DICHROISM; ENANTIOMER; ENTHALPY; NUCLEAR MAGNETIC RESONANCE; NUCLEAR OVERHAUSER EFFECT; PHASE TRANSITION; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION;

AMINO ACID SEQUENCE; CALORIMETRY, DIFFERENTIAL SCANNING; CHOLESTEROL; CIRCULAR DICHROISM; MEMBRANE MICRODOMAINS; MYRISTIC ACID; NERVE TISSUE PROTEINS; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PEPTIDE FRAGMENTS; PHOSPHATIDYLINOSITOL PHOSPHATES; REPRESSOR PROTEINS;

EID: 25144446241     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20050649     Document Type: Article

References (42)

1. Simons, K. and Vaz, W. L. C. (2004) Model systems, lipid rafts, and cell membranes. Annu. Rev. Biophys. Biomol. Struct. 33, 269-295
2. Epand, R. M. (2004) Do proteins facilitate the formation of cholesterol-rich domains? Biochim. Biophys. Acta 1666, 227-238
3. Epand, R. M., Maekawa, S., Yip, C. M. and Epand, R. F. (2001) Protein-induced formation of cholesterol-rich domains. Biochemistry 40, 10514-10521
4. Epand, R. M., Sayer, B. G. and Epand, R. F. (2003) Peptide-induced formation of cholesterol-rich domains. Biochemistry 42, 14677-14689
5. Frey, D., Laux, T., Xu, L., Schneider, C. and Caroni, P. (2000) Shared and unique roles of CAP23 and GAP43 in actin regulation, neurite outgrowth, and anatomical plasticity. J. Cell Biol. 149, 1443-1454
6. Zakharov, V. V., Capony, J. P., Derancourt, J., Kropolova, E. S., Novitskaya, V. A., Bogdanova, M. N. and Mosevitsky, M. I. (2003) Natural N-terminal fragments of brain abundant myristoylated protein BASP1. Biochim. Biophys. Acta Gen. Subj. 1622, 14-19
7. Melkonian, K. A., Ostermeyer, A. G., Chen, J. Z., Roth, M. G. and Brown, D. A. (1999) Role of lipid modifications in targeting proteins to detergent-resistant membrane rafts. Many raft proteins are acylated, while few are prenylated. J. Biol. Chem. 274, 3910-3917
8. Zacharias, D. A., Violin, J. D., Newton, A. C. and Tsien, R. Y. (2002) Partitioning of lipid-modified monomeric GFPs into membrane microdomains of live cells. Science 296, 913-916
9. Epand, R. M., Vuong, P., Yip, C. M., Maekawa, S. and Epand, R. F. (2004) Cholesterol-dependent partitioning of PtdIns(4,5)P-2 into membrane domains by the N-terminal fragment of NAP-22 (neuronal axonal myristoylated membrane protein of 22 kDa). Biochemical J. 379, 527-532
10. Salzwedel, K., West, J. T. and Hunter, E. (1999) A conserved tryptophan-rich motif in the membrane-proximal region of the human immunodeficiency virus type 1 gp41 ectodomain is important for Env-mediated fusion and virus infectivity. J. Virol. 73, 2469-2480
11. Saez-Cirion, A., Nir, S., Lorizate, M., Agirre, A., Cruz, A., Perez-Gil, J. and Nieva, J. L. (2002) Sphingomyelin and cholesterol promote HIV-1 gp41 pretransmembrane sequence surface aggregation and membrane restructuring. J. Biol. Chem. 277, 21776-21785
12. Saez-Cirion, A., Arrondo, J. L., Gomara, M. J., Lorizate, M., Iloro, I., Melikyan, G. and Nieva, J. L. (2003) Structural and functional roles of HIV-1 gp41 pretransmembrane sequence segmentation. Biophys. J. 85, 3769-3780
13. Li, H., Yao, Z., Degenhardt, B., Teper, G. and Papadopoulos, V. (2001) Cholesterol binding at the cholesterol recognition/interaction amino acid consensus (CRAC) of the peripheral-type benzodiazepine receptor and inhibition of steroidogenesis by an HIV TAT-CRAC peptide. Proc. Natl. Acad. Sci. U.S.A. 98, 1267-1272
14. Zhang, W., Crocker, E., McLaughlin, S. and Smith, S. O. (2003) Binding of peptides with basic and aromatic residues to bilayer membranes: phenylalanine in the myristoylated alanine-rich C kinase substrate effector domain penetrates into the hydrophobic core of the bilayer. J. Biol. Chem. 278, 21459-21466
15. Rychnovsky, S. D. and Mickus, D. E. (1992) Synthesis of ent-cholesterol, the unnatural enantiomer. J. Org. Chem. 57, 2732-2736
16. Sober, H. A. (ed.) (1970) in Handbook of Biochemistry: Selected Data for Molecular Biology, p. B75-B76, The Chemical Rubber Co., Cleveland, OH
17. Gambhir, A., Hangyas-Mihalyne, G., Zaitseva, I., Cafiso, D. S., Wang, J., Murray, D., Pentyala, S. N., Smith, S. O. and McLaughlin, S. (2004) Electrostatic sequestration of PIP2 on phospholipid membranes by basic/aromatic regions of proteins. Biophys. J. 86, 2188-2207
18. Privalov, G., Kavina, V., Freire, E. and Privalov, P. L. (1995) Precise scanning calorimeter for studying thermal properties of biological macromolecules in dilute solution. Anal. Biochem. 232, 79-85
19. Forbes, J., Bowers, J., Shan, X., Moran, L., Oldfield, E. and Moscarello, M. A. (1988) Some new developments in solid-state nuclear magnetic resonance spectroscopy studies of lipids and biological membranes, including the effects of cholesterol in model and natural systems. J. Chem. Soc., Faraday Trans. 84, 3821-3849
20. Guo, W. and Hamilton, J. A. (1996) 13C MAS NMR studies of crystalline cholesterol and lipid mixtures modeling atherosclerotic plaques. Biophys. J. 71, 2857-2868
21. Arnold, M. R., Kremer, W., Ludemann, H. D. and Kalbitzer, H. R. (2002) 1H-NMR parameters of common amino acid residues measured in aqueous solutions of the linear tetrapeptides Gly-Gly-X-Ala at pressures between 0.1 and 200 MPa. Biophys. Chem. 96, 129-140
22. Wiener, M. C. and White, S. H. (1992) Structure of a fluid dioleoylphosphatidylcholine bilayer determined by joint refinement of x-ray and neutron diffraction data. III. Complete structure. Biophys. J. 61, 437-447
23. Feller, S. E., Brown, C. A., Nizza, D. T. and Gawrisch, K. (2002) Nuclear Overhauser enhancement spectroscopy cross-relaxation rates and ethanol distribution across membranes. Biophys. J. 82, 1396-1404
24. Pastor, R. W., Venable, R. M. and Feller, S. E. (2002) Lipid bilayers, NMR relaxation, and computer simulations. Acc. Chem. Res. 35, 438-446
25. Lalitha, S., Kumar, A. S., Stine, K. J. and Covey, D. F. (2001) Chirality in membranes: first evidence that enantioselective interactions between cholesterol and cell membrane lipids can be a determinant of membrane physical properties. J. Supramol. Chem. 1, 53-61
26. Lalitha, S., Kumar, A. S., Stine, K. J. and Covey, D. F. (2001) Enantiospecificity of sterol-lipid interactions: first evidence that the absolute configuration of cholesterol affects the physical properties of cholesterol-sphingomyelin membranes. Chem. Commun. 1192-1193
27. Westover, E. J., Covey, D. F., Brockman, H. L., Brown, R. E. and Pike, L. J. (2003) Cholesterol depletion results in site-specific increases in epidermal growth factor receptor phosphorylation due to membrane level effects. Studies with cholesterol enantiomers. J. Biol. Chem. 278, 51125-51133
28. Westover, E. J. and Covey, D. F. (2004) The enantiomer of cholesterol. J. Membr. Biol. 202, 61-72
29. Crowder, C. M., Westover, E. J., Kumar, A. S., Ostlund, Jr, R. E. and Covey, D. F. (2001) Enantiospecificity of cholesterol function in vivo. J. Biol. Chem. 276, 44369-44372
30. Geva, M., Izhaky, D., Mickus, D. E., Rychnovsky, S. D. and Addadi, L. (2001) Stereoselective recognition of monolayers of cholesterol, ent-cholesterol, and epicholesterol by an antibody. ChemBioChem. 2, 265-271
31. Li, Y., Ge, M., Ciani, L., Kuriakose, G., Westover, E. J., Dura, M., Covey, D. F., Freed, J. H., Maxfield, F. R., Lytton, J. and Tabas, I. (2004) Enrichment of endoplasmic reticulum with cholesterol inhibits sarcoplasmic-endoplasmic reticulum calcium ATPase-2b activity in parallel with increased order of membrane lipids: implications for depletion of endoplasmic reticulum calcium stores and apoptosis in cholesterol-loaded macrophages. J. Biol. Chem. 279, 37030-37039
32. Zitzer, A., Westover, E. J., Covey, D. F. and Palmer, M. (2003) Differential interaction of the two cholesterol-dependent, membrane-damaging toxins, streptolysin O and Vibrio cholerae cytolysin with enantiomeric cholesterol. FEBS Lett. 553, 229-231
33. Richter, R. K., Mickus, D. E., Rychnovsky, S. D. and Molinski, T. F. (2004) Differential modulation of the antifungal activity of amphotericin B by natural and ent-cholesterol. Bioorg. Med. Chem. Lett. 14, 115-118
34. Luker, G. D., Pica, C. M., Kumar, A. S., Covey, D. F. and Piwnica-Worms, D. (2000) Effects of cholesterol and enantiomeric cholesterol on P-glycoprotein localization and function in low-density membrane domains. Biochemistry 39, 7651-7661
35. Wade, D., Silberring, J., Soliymani, R., Heikkinen, S., Kilpelainen, I., Lankinen, H. and Kuusela, P. (2000) Antibacterial activities of temporin A analogs. FEBS. Lett. 479, 6-9
36. Torres-Larios, A., Gurrola, G. B., Zamudio, F. Z. and Possani, L. D. (2000) Hadrurin, a new antimicrobial peptide from the venom of the scorpion Hadrurus aztecus. Eur. J. Biochem. 267, 5023-5031
37. Bucki, R., Pastore, J. J., Randhawa, P., Vegners, R., Weiner, D. J. and Janmey, P. A. (2004) Antibacterial activities of rhodamine B-conjugated gelsolin-derived peptides compared to those of the antimicrobial peptides cathelicidin LL37, magainin II, and melittin. Antimicrob. Agents. Chemother. 48, 1526-1533
38. Epand, R. F., Sayer, B. G. and Epand, R. M. (2005) Induction of raft-like domains by a myristoylated NAP-22 peptide and its Tyr mutant. FEBS. J. 272, 1792-1803
39. Plesniak, L. A., Parducho, J. I., Ziebart, A., Geierstanger, B. H., Whiles, J. A., Melacini, G. and Jennings, P. A. (2004) Orientation and helical conformation of a tissue-specific hunter-killer peptide in micelles. Protein Sci. 13, 1988-1996
40. Suchyna, T. M., Tape, S. E., Koeppe, R. E., Andersen, O. S., Sachs, F. and Gottlieb, P. A. (2004) Bilayer-dependent inhibition of mechanosensitive channels by neuroactive peptide enantiomers. Nature (London) 430, 235-240
41. Gerber, D., Quintana, F. J., Bloch, I., Cohen, I. R. and Shai, Y. (2005) D-enantiomer peptide of the TCRalpha transmembrane domain inhibits T-cell activation in vitro and in vivo. FASEB. J. 19, 1190-1192
42. Sal-Man, N., Gerber, D. and Shai, Y. (2004) Hetero-assembly between all-L- and all-D-amino acid transmembrane domains: forces involved and implication for inactivation of membrane proteins. J. Mol. Biol. 344, 855-864