The structure of human apolipoprotein E2, E3 and E4 in solution. 2. Multidomain organization correlates with the stability of apoE structure

Biophysical Chemistry

Volumn 119, Issue 2, 2006, Pages 170-185

  Clément Collin, Vanessa ^a   Barbier, Anne ^a,b   Dergunov, Alexander D ^c   Visvikis, Athanase ^b   Siest, Gérard ^b   Desmadril, Michel ^d   Takahashi, Masa ^e   Aggerbeck, Lawrence P ^a  

^a CNRS   (France)

^b Centre du Medicament URA CNRS 597   (France)

^c NATIONAL MEDICAL RESEARCH CENTER FOR THERAPY AND PREVENTIVE MEDICINE   (Russian Federation)

^d UNIVERSITÉ PARIS SACLAY   (France)

^e INSTITUT CURIE   (France)

Author keywords

Apolipoprotein E; Domain structure; Protein conformation; Secondary and tertiary structure

Indexed keywords

APOLIPOPROTEIN E2; APOLIPOPROTEIN E3; APOLIPOPROTEIN E4;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CIRCULAR DICHROISM; CONTROLLED STUDY; DENATURATION; FLUORESCENCE; GEL PERMEATION CHROMATOGRAPHY; HUMAN; MATHEMATICAL ANALYSIS; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN SECONDARY STRUCTURE; PROTEIN STABILITY; PROTEIN STRUCTURE; ULTRAVIOLET RADIATION;

APOLIPOPROTEIN E2; APOLIPOPROTEIN E3; APOLIPOPROTEIN E4; APOLIPOPROTEINS E; CHROMATOGRAPHY, GEL; CIRCULAR DICHROISM; GUANIDINE; HUMANS; PARTICLE SIZE; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; SENSITIVITY AND SPECIFICITY; SOLUTIONS; SPECTROMETRY, FLUORESCENCE; SPECTROPHOTOMETRY, ULTRAVIOLET; TEMPERATURE;

EID: 30844471542     PISSN: 03014622     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bpc.2005.07.009     Document Type: Article

References (53)

1. A. Barbier, V. Clement-Collin, A.D. Dergunov, A. Visvikis, G. Siest, and L.P. Aggerbeck The structure of three recombinant apolipoprotein E isoforms in solution: 1. Tertiary and quaternary structure Biophys. Chemist. 119 2005 174 185 10.1016/j.bpc.2005.07.010
2. C. Wilson, M.R. Wardell, K.H. Weisgraber, R.W. Mahley, and D.A. Agard Three-dimensional structure of the LDL receptor-binding domain of human apolipoprotein E Science 252 1991 1817 1822
3. L.P. Aggerbeck, J.R. Wetterau, K.H. Weisgraber, C.S. Wu, and F.T. Lindgren Human apolipoprotein E3 in aqueous solution: II. Properties of the amino- and carboxyl-terminal domains J. Biol. Chem. 263 1988 6249 6258
4. A.D. Dergunov, V.V. Shuvaev, and E.V. Yanushevskaja Quaternary structure of apolipoprotein E in solution: fluorimetric, chromatographic and immunochemical studies Biol. Chem. Hoppe-Seyler 373 1992 323 331
5. A.D. Dergunov, Y.Y. Vorotnikova, S. Visvikis, and G. Siest Homo- and hetero-complexes of exchangeable apolipoproteins in solution and in lipid-bound form Spectrochim. Acta, Part A 59 2003 1127 1137
6. H. Saito, P. Dhanasekaran, F. Baldwin, K.H. Weisgraber, S. Lund-Katz, and M.C. Phillips Lipid binding-induced conformational change in human apolipoprotein E. Evidence for two lipid-bound states on spherical particles J. Biol. Chem. 276 2001 40949 40954
7. H. Saito, P. Dhanasekaran, D. Nguyen, P. Holvoet, S. Lund-Katz, and M.C. Phillips Domain structure and lipid interaction in human apolipoproteins A-I and E, a general model J. Biol. Chem. 278 2003 23227 23232
8. V. Clement-Collin, A. Leroy, C. Monteilhet, and L.P. Aggerbeck Mimicking lipid-binding-induced conformational changes in the human apolipoprotein E N-terminal receptor binding domain effects of low pH and propanol Eur. J. Biochem. 264 1999 358 368
9. C.A. Fisher, V. Narayanaswami, and R.O. Ryan The lipid-associated conformation of the low density lipoprotein receptor binding domain of human apolipoprotein E J. Biol. Chem. 275 2000 33601 33606
10. B. Lu, J.A. Morrow, and K.H. Weisgraber Conformational reorganization of the four-helix bundle of human apolipoprotein E in binding to phospholipid J. Biol. Chem. 275 2000 20775 20781
11. V. Raussens, C.A. Fisher, E. Goormaghtigh, R.O. Ryan, and J.M. Ryusschaert The low density lipoprotein receptor active conformation of apolipoprotein E. Helix organization in N-terminal domain-phospholipid disc particles J. Biol. Chem. 273 1998 25825 25830
12. V. Raussens, C.M. Slupsky, R.O. Ryan, and B.D. Sykes NMR structure and dynamics of a receptor-active apolipoprotein E peptide J. Biol. Chem. 277 2002 29172 29180
13. V. Raussens, C.M. Slupsky, B.D. Sykes, and R.O. Ryan Lipid-bound structure of an apolipoprotein E-derived peptide J. Biol. Chem. 278 2003 25998 26006
14. P.M. Weers, V. Narayanaswami, and R.O. Ryan Modulation of the lipid binding properties of the N-terminal domain of human apolipoprotein E3 Eur. J. Biochem. 268 2001 3728 3735
15. S. Lund-Katz, S. Wehrli, M. Zaiou, Y. Newhouse, K.H. Weisgraber, and M.C. Phillips Effects of polymorphism on the microenvironment of the LDL receptor-binding region of human apoE J. Lipid Res. 42 2001 894 901
16. M. Perugini, P. Schuck, and G.J. Howlett Self-association of human apolipoprotein E3 and E4 in the presence and absence of phospholipid J. Biol. Chem. 275 2000 36758 36765
17. T. Pillot, M. Goethals, J. Najib, C. Labeur, L. Lins, J. Chambaz, R. Brasseur, J. Vandekerckhove, and M. Rosseneu Beta-amyloid peptide interacts specifically with the carboxy-terminal domain of human apolipoprotein E: relevance to Alzheimer's disease J. Neurochem. 72 1999 230 237
18. L.M. Dong, C. Wilson, M.R. Wardell, T. Simmons, R.W. Mahley, K.H. Weisgraber, and D.A. Agard Human apolipoprotein E. Role of arginine 61 in mediating the lipoprotein preferences of the E3 and E4 isoforms J. Biol. Chem. 269 1994 22358 22365
19. L.M. Dong, and K.H. Weisgraber Human apolipoprotein E4 domain interaction. Arginine 61 and glutamic acid 255 interact to direct the preference for very low density lipoproteins J. Biol. Chem. 271 1996 19053 19057
20. M.A. Perugini, P. Schuck, and G.J. Howlett Differences in the binding capacity of human apolipoprotein E3 and E4 to size-fractionated lipid emulsions Eur. J. Biochem. 269 2002 5939 5949
21. H. Saito, P. Dhanasekaran, F. Baldwin, K.H. Weisgraber, M.C. Phillips, and S. Lund-Katz Effects of polymorphism on the lipid interaction of human apolipoprotein E J. Biol. Chem. 278 2003 40723 40729
22. M.L. Segall, P. Dhanasekaran, F. Baldwin, G.M. Anantharamaiah, K.H. Weisgraber, M.C. Phillips, and S. Lund-Katz Influence of apoE domain structure and polymorphism on the kinetics of phospholipid vesicle solubilization J. Lipid Res. 43 2002 1688 1700
23. L.M. Dong, T.L. Innerarity, K.S. Arnold, Y.M. Newhouse, and K.H. Weisgraber The carboxyl terminus in apolipoprotein E2 and the seven amino acid repeat in apolipoprotein E-Leiden: role in receptor-binding activity J. Lipid Res. 39 1998 1173 1180
24. J.A. Morrow, M.L. Segall, S. Lund-Katz, M.C. Phillips, M. Knapp, B. Rupp, and K.H. Weisgraber Differences in stability among the human apolipoprotein E isoforms determined by the amino-terminal domain Biochemistry 39 2000 11657 11666
25. J.R. Wetterau, L.P. Aggerbeck, S.C. Rall Jr., and K.H. Weisgraber Human apolipoprotein E3 in aqueous solution: I. Evidence for two structural domains J. Biol. Chem. 263 1988 6240 6248
26. Y. Fang, O. Gursky, and D. Atkinson Structural studies of N- and C-terminally truncated human apolipoprotein A-I Biochemistry 42 2003 6881 6890
27. O. Gursky, and D. Atkinson Thermal unfolding of human high-density apolipoprotein A-1: implications for a lipid-free molten globular state Proc. Natl. Acad. Sci. U. S. A. 93 1996 2991 2995
28. M. Suurkuusk, and D. Hallen Denaturation of apolipoprotein A-I and the monomer form of apolipoprotein A-I (Milano) Eur. J. Biochem. 265 1999 346 352
29. O. Gursky, and D. Atkinson High- and low-temperature unfolding of human high-density apolipoprotein A-2 Protein Sci. 5 1996 1874 1882
30. O. Gursky, and D. Atkinson Thermodynamic analysis of human plasma apolipoprotein C-1: high-temperature unfolding and low-temperature oligomer dissociation Biochemistry 37 1998 1283 1291
31. P. Acharya, M.L. Segall, M. Zaiou, J. Morrow, K.H. Weisgraber, M.C. Phillips, S. Lund-Katz, and J. Snow Comparison of the stabilities and unfolding pathways of human apolipoprotein E isoforms by differential scanning calorimetry and circular dichroism Biochim. Biophys. Acta 1584 2002 9 19
32. J.A. Morrow, D.M. Hatters, B. Lu, P. Hochtl, K.A. Oberg, B. Rupp, and K.H. Weisgraber Apolipoprotein E4 forms a molten globule. A potential basis for its association with disease J. Biol. Chem. 277 2002 50380 50385
33. N. Choy, V. Raussens, and V. Narayanaswami Inter-molecular coiled-coil formation in human apolipoprotein E C-terminal domain J. Mol. Biol. 334 2003 527 539
34. G. Wang, G.K. Pierens, W.D. Treleaven, J.T. Sparrow, and R.J. Cushley Conformations of human apolipoprotein E(263-286) and E(267-289) in aqueous solutions of sodium dodecyl sulfate by CD and 1H NMR Biochemistry 35 1996 10358 10366
35. T. Pillot, A. Barbier, A. Visvikis, K. Lozac'h, M. Rosseneu, J. Vandekerckhove, and G. Siest Single-step purification of two functional human apolipoprotein E variants hyperexpressed in Escherichia coli Protein Expr. Purif. 7 1996 407 414
36. A. Barbier, A. Visvikis, F. Mathieu, L. Diez, L.M. Havekes, and G. Siest Characterization of three human apolipoprotein E isoforms (E2, E3 and E4) expressed in Escherichia coli Eur. J. Clin. Chem. Clin. Biochem. 35 1997 581 589
37. C. Monteilhet, N. Lachacinski, and L.P. Aggerbeck Cytoplasmic and periplasmic production of human apolipoprotein E in Escherichia coli using natural and bacterial signal peptides Gene 125 1993 223 228
38. K.H. Weisgraber, S.C. Rall Jr., and R.W. Mahley Human E apoprotein heterogeneity. Cysteine-arginine interchanges in the amino acid sequence of the apo-E isoforms J. Biol. Chem. 256 1981 9077 9083
39. P. Pajot Fluorescence of proteins in 6-M guanidine hydrochloride. A method for the quantitative determination of tryptophan Eur. J. Biochem. 63 1976 263 269
40. H.J. Pownall, and J.B. Massey Spectroscopic studies of lipoproteins Methods Enzymol. 128 1986 515 518
41. Y.H. Chen, J.T. Yang, and H.M. Martinez Determination of the secondary structures of proteins by circular dichroism and optical rotatory dispersion Biochemistry 11 1972 4120 4131
42. C.A. Royer, C.J. Mann, and C.R. Matthews Resolution of the fluorescence equilibrium unfolding profile of trp aporepressor using single tryptophan mutants Protein Sci. 2 1993 1844 1852
43. M. Le Maire, L.P. Aggerbeck, C. Monteilhet, J.P. Andersen, and J.V. Moller The use of high-performance liquid chromatography for the determination of size and molecular weight of proteins: a caution and a list of membrane proteins suitable as standards Anal. Biochem. 154 1986 525 535
44. V.N. Uversky Use of fast protein size-exclusion liquid chromatography to study the unfolding of proteins which denature through the molten globule Biochemistry 32 1993 13288 13298
45. C. Tanford Protein denaturation Adv. Protein Chem. 23 1968 121 282
46. S.W. Tendian, D.G. Myszka, R.W. Sweet, I.M. Chaiken, and C.G. Brouillette Interdomain communication of T-cell CD4 studied by absorbance and fluorescence difference spectroscopy measurements of urea-induced unfolding Biochemistry 34 1995 6464 6474
47. C.R. Matthews, and M.M. Crisanti Urea-induced unfolding of the alpha subunit of tryptophan synthase: evidence for a multistate process Biochemistry 20 1981 784 792
48. S. Yokoyama, Y. Kawai, S. Tajima, and A. Yamamoto Behavior of human apolipoprotein E in aqueous solutions and at interfaces J. Biol. Chem. 260 1985 16375 16382
49. A. Jonas, A. Steinmetz, and L. Churgay The number of amphipathic alpha-helical segments of apolipoproteins A-I, E, and A-IV determines the size and functional properties of their reconstituted lipoprotein particles J. Biol. Chem. 268 1993 1596 1602
50. V.N. Uversky, and O.B. Ptitsyn Further evidence on the equilibrium "pre-molten globule state": four-state guanidinium chloride-induced unfolding of carbonic anhydrase B at low temperature J. Mol. Biol. 255 1996 215 228
51. K.H. Weisgraber Apolipoprotein E: structure-function relationships Adv. Protein Chem. 45 1994 249 302
52. D.R. Breiter, M.R. Kanost, M.M. Benning, G. Wesenberg, J.H. Law, M.A. Wells, I. Rayment, and H.M. Holden Molecular structure of an apolipoprotein determined at 2.5-A resolution Biochemistry 30 1991 603 608
53. H.C. Hung, Y.H. Chen, G.Y. Liu, H.J. Lee, and G.G. Chang Equilibrium protein folding-unfolding process involving multiple intermediates Bull. Math. Biol. 65 2003 553 570