Atomic view of calcium-induced clustering of phosphatidylserine in mixed lipid bilayers

Biochemistry

Volumn 50, Issue 12, 2011, Pages 2264-2273

  Boettcher, John M ^a   Davis Harrison, Rebecca L ^a   Clay, Mary C ^a   Nieuwkoop, Andrew J ^a   Ohkubo, Y Zenmei ^a   Tajkhorshid, Emad ^a   Morrissey, James H ^a   Rienstra, Chad M ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIONIC LIPIDS; BI-LAYER; BILAYER COMPOSITIONS; BINDING AFFINITIES; BIOLOGICAL PROCESS; BLOOD COAGULATION; CATALYTIC ACTIVITY; CONFORMATIONAL CHANGE; CONFORMATIONAL EFFECT; COUNTERIONS; HEAD GROUPS; INTRACELLULAR SIGNALING; ISOTOPICALLY LABELED; MAGIC ANGLE SPINNING; MD SIMULATION; MEMBRANE-ASSOCIATED PROTEINS; MOLECULAR DYNAMICS SIMULATIONS; NANO SCALE; NANODISCS; PHOSPHATIDYLSERINE; PHOSPHOLIPID BILAYER; SOLID STATE NMR; STRUCTURAL EFFECT; STRUCTURE AND DYNAMICS; VESICLE FUSION;

AMINO ACIDS; ATOMIC SPECTROSCOPY; BINDING ENERGY; CALCIUM; CATALYST ACTIVITY; COAGULATION; DYES; IONS; LIPOSOMES; MOLECULAR DYNAMICS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PHOSPHOLIPIDS;

LIPID BILAYERS;

CALCIUM; CARBON 13; NITROGEN 15; PHOSPHATIDYLSERINE; PHOSPHORUS;

ARTICLE; CONFORMATIONAL TRANSITION; ISOTOPE LABELING; LIPID BILAYER; MAGIC ANGLE SPINNING; MEASUREMENT; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE; SIMULATION; SOLID STATE NUCLEAR MAGNETIC RESONANCE;

CALCIUM; LIPID BILAYERS; MAGNETIC RESONANCE SPECTROSCOPY; MOLECULAR CONFORMATION; MOLECULAR DYNAMICS SIMULATION; MOVEMENT; NANOSTRUCTURES; PHASE TRANSITION; PHOSPHATIDYLSERINES; SODIUM;

EID: 79952922725     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi1013694     Document Type: Article

References (66)

1. Gordesky, S. E. and Marinetti, G. V. (1973) The asymetric arrangement of phospholipids in the human erythrocyte membrane Biochem. Biophys. Res. Commun. 50, 1027-1031
2. Buckland, A. G. and Wilton, D. C. (2000) Anionic phospholipids, interfacial binding and the regulation of cell functions Biochim. Biophys. Acta 1483, 199-216 (Pubitemid 30029053)
3. Leventis, P. A. and Grinstein, S. (2010) The distribution and function of phosphatidylserine in cellular membranes Annu. Rev. Biophys. 39, 407-427
4. McLaughlin, S. and Murray, D. (2005) Plasma membrane phosphoinositide organization by protein electrostatics Nature 438, 605-611 (Pubitemid 41740564)
5. Yeung, T., Gilbert, G. E., Shi, J., Silvius, J., Kapus, A., and Grinstein, S. (2008) Membrane phosphatidylserine regulates surface charge and protein localization Science 319, 210-213
6. Lemmon, M. A. (2008) Membrane recognition by phospholipid-binding domains Nat. Rev. Mol. Cell. Biol. 9, 99-111 (Pubitemid 351158910)
7. Fadok, V. A., Voelker, D. R., Campbell, P. A., Cohen, J. J., Bratton, D. L., and Henson, P. M. (1992) Exposure of phosphatidylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal by macrophages J. Immunol. 148, 2207-2216
8. Zwaal, R. F., Comfurius, P., and Bevers, E. M. (2005) Surface exposure of phosphatidylserine in pathological cells Cell. Mol. Life Sci. 62, 971-988 (Pubitemid 40655614)
9. Duzgunes, N., Nir, S., Wilschut, J., Bentz, J., Newton, C., Portis, A., and Papahadjopoulos, D. (1981) Calcium- and magnesium-induced fusion of mixed phosphatidylserine/phosphatidylcholine vesicles: effect of ion binding J. Membr. Biol. 59, 115-125 (Pubitemid 11032100)
10. Feigenson, G. W. (1986) On the nature of calcium-ion binding between phosphatidylserine lamellae Biochemistry 25, 5819-5825
11. Leckband, D. E., Helm, C. A., and Israelachvili, J. (1993) Role of calcium in the adhesion and fusion of bilayers Biochemistry 32, 1127-1140 (Pubitemid 23057689)
12. 2+-induced lateral phase separations in phosphatic acid-phosphatidylcholine membranes Biochim. Biophys. Acta 352, 29-37
13. Berridge, M. J. and Irvine, R. F. (1984) Inositol trisphosphate, a novel second messenger in cellular signal transduction Nature 312, 315-321 (Pubitemid 15209307)
14. Maxfield, F. R. (2002) Plasma membrane microdomains Curr. Opin. Cell Biol. 14, 483-487 (Pubitemid 35279109)
15. Laude, A. J. and Prior, I. A. (2004) Plasma membrane microdomains: organization, function and trafficking Mol. Membr. Biol. 21, 193-205 (Pubitemid 38745648)
16. Menke, M., Gerke, V., and Steinem, C. (2005) Phosphatidylserine membrane domain clustering induced by annexin A2/S100A10 heterotetramer Biochemistry 44, 15296-15303 (Pubitemid 41683134)
17. Schultz, Z. D., Pazos, I. M., McNeil-Watson, F. K., Lewis, E. N., and Levin, I. W. (2009) Magnesium-induced lipid bilayer microdomain reorganizations: implications for membrane fusion J. Phys. Chem. B 113, 9932-9941
18. Gokhale, N. A., Abraham, A., Digman, M. A., Gratton, E., and Cho, W. (2005) Phosphoinositide specificity of and mechanism of lipid domain formation by annexin A2-p11 heterotetramer J. Biol. Chem. 280, 42831-42840 (Pubitemid 43049245)
19. 2+-induced lateral phase separation in phosphatidic acid/phosphatidylcholine monolayers as revealed by fluorescence microscopy Biochemistry 27, 3433-3437
20. Levental, I., Christian, D. A., Wang, Y. H., Madara, J. J., Discher, D. E., and Janmey, P. A. (2009) Calcium-dependent lateral organization in phosphatidylinositol 4,5-bisphosphate (PIP2)- and cholesterol-containing monolayers Biochemistry 48, 8241-8248
21. + distributions in the headgroup region of binary membranes of phosphatidylcholine and phosphatidylserine as seen by deuterium NMR Biochemistry 29, 7077-7089 (Pubitemid 20241156)
22. Roux, M. and Bloom, M. (1991) Calcium-binding by phosphatidylserine headgroups-Deuterium NMR study Biophys. J. 60, 38-44
23. 1H-NMR conformational study of phosphatidylserine diluted in perdeuterated dodecylphosphocholine micelles: evidence for a pH-induced conformational transition Biochemistry 34, 5938-5944
24. Frazier, A. A., Roller, C. R., Havelka, J. J., Hinderliter, A., and Cafiso, D. S. (2003) Membrane-bound orientation and position of the synaptotagmin I C2A domain by site-directed spin labeling Biochemistry 42, 96-105 (Pubitemid 36083855)
25. Rufener, E., Frazier, A. A., Wieser, C. M., Hinderliter, A., and Cafiso, D. S. (2005) Membrane-bound orientation and position of the synaptotagmin C2B domain determined by site-directed spin labeling Biochemistry 44, 18-28 (Pubitemid 40095703)
26. 2+ bridges the C2 membrane-binding domain of protein kinase Cα directly to phosphatidylserine EMBO J. 18, 6329-6338 (Pubitemid 29533237)
27. 2+ in membrane binding of blood coagulation factors Structure 16, 72-81
28. Sinn, C. G., Antonietti, M., and Dimova, R. (2006) Binding of calcium to phosphatidylcholine-phosphatidylserine membranes Colloids Surf., A 282, 410-419 (Pubitemid 43816812)
29. Pedersen, U. R., Leidy, C., Westh, P., and Peters, G. H. (2006) The effect of calcium on the properties of charged phospholipid bilayers Biochim. Biophys. Acta 1758, 573-582 (Pubitemid 44202289)
30. Vernier, P. T., Ziegler, M. J., and Dimova, R. (2009) Calcium binding and head group dipole angle in phosphatidylserine-phosphatidylcholine bilayers Langmuir 25, 1020-1027
31. Bayburt, T. H. and Sligar, S. G. (2003) Self-assembly of single integral membrane proteins into soluble nanoscale phospholipid bilayers Protein Sci. 12, 2476-2481 (Pubitemid 37310788)
32. Bayburt, T. H. and Sligar, S. G. (2002) Single-molecule height measurements on microsomal cytochrome P450 in nanometer-scale phospholipid bilayer disks Proc. Natl. Acad. Sci. U.S.A. 99, 6725-6730 (Pubitemid 34526200)
33. Bayburt, T. H., Grinkova, Y. V., and Sligar, S. G. (2002) Self-assembly of discoidal phospholipid bilayer nanoparticles with membrane scaffold proteins Nano Lett. 2, 853-856 (Pubitemid 135706448)
34. Bayburt, T. H., Carlson, J. W., and Sligar, S. G. (2000) Single molecule height measurements on a membrane protein in nanometer-scale phospholipid bilayer disks Langmuir 16, 5993-5997
35. Morrissey, J. H., Pureza, V., Davis-Harrison, R. L., Sligar, S. G., Ohkubo, Y. Z., and Tajkhorshid, E. (2008) Blood clotting reactions on nanoscale phospholipid bilayers Thromb. Res. 122 (Suppl. 1) S23-S26
36. Morrissey, J. H., Pureza, V., Davis-Harrison, R. L., Sligar, S. G., Rienstra, C. M., Kijac, A. Z., Ohkubo, Y. Z., and Tajkhorshid, E. (2009) Protein-membrane interactions: blood clotting on nanoscale bilayers J. Thromb. Haemostasis 7, 169-172
37. Li, Y., Kijac, A. Z., Sligar, S. G., and Rienstra, C. M. (2006) Structural analysis of nanoscale self-assembled discoidal lipid bilayers by solid-state NMR spectroscopy Biophys. J. 91, 3819-3828 (Pubitemid 44788324)
38. 3 oxidase J. Biomol. NMR 36, 55-71 (Pubitemid 44473227)
39. Kijac, A. Z., Li, Y., Sligar, S. G., and Rienstra, C. M. (2007) Magic-angle spinning solid-state NMR spectroscopy of nanodisc-embedded human CYP3A4 Biochemistry 46, 13696-13703 (Pubitemid 350223897)
40. Iwasaki, Y., Mizumoto, Y., Okada, T., Yamamoto, T., Tsutsumi, K., and Yamane, T. (2003) An aqueous suspension system for phospholipase D-mediated synthesis of PS without toxic organic solvent J. Am. Oil Chem. Soc. 80, 653-657
41. Comfurius, P. and Zwaal, R. F. A. (1977) Enzymatic synthesis of phosphatidylserine and purification by CM-cellulose column chromatography Biochim. Biophys. Acta 488, 36-42 (Pubitemid 8143459)
42. Van Geet, A. L. (1968) Calibration of the methanol and glycol nuclear magnetic resonance thermometers with a static thermistor probe Anal. Chem. 42, 2227
43. Hediger, S., Meier, B. H., Kurur, N. D., Bodenhausen, G., and Ernst, R. R. (1994) NMR cross-polarization by adiabatic passage through the Hartmann-Hahn condition (APHH) Chem. Phys. Lett. 223, 283-288
44. Bennett, A. E., Rienstra, C. M., Auger, M., Lakshmi, K. V., and Griffin, R. G. (1995) Heteronuclear decoupling in rotating solids J. Chem. Phys. 103, 6951-6958
45. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., and Bax, A. (1995) Nmrpipe: a multidimensional spectral processing system based on unix pipes J. Biomol. NMR 6, 277-293
46. Morcombe, C. R. and Zilm, K. W. (2003) Chemical shift referencing in MAS solid state NMR J. Magn. Reson. 162, 479-486
47. Goddard, T. D. and Kneller, D. G. Sparky 3, 3.106 ed., University of California, San Francisco.
48. Phillips, J. C., Braun, R., Wang, W., Gumbart, J., Tajkhorshid, E., Villa, E., Chipot, C., Skeel, R. D., Kale, L., and Schulten, K. (2005) Scalable molecular dynamics with NAMD J. Comput. Chem. 26, 1781-1802 (Pubitemid 43078511)
49. MacKerell, A. D., Bashford, D., Bellott, Dunbrack, R. L., Evanseck, J. D., Field, M. J., Fischer, S., Gao, J., Guo, H., Ha, S., Joseph-McCarthy, D., Kuchnir, L., Kuczera, K., Lau, F. T. K., Mattos, C., Michnick, S., Ngo, T., Nguyen, D. T., Prodhom, B., Reiher, W. E., Roux, B., Schlenkrich, M., Smith, J. C., Stote, R., Straub, J., Watanabe, M., Wiorkiewicz-Kuczera, J., Yin, D., and Karplus, M. (1998) All-atom empirical potential for molecular modeling and dynamics studies of proteins J. Phys. Chem. B 102, 3586-3616 (Pubitemid 128576688)
50. Darden, T. A., York, D. M., and Pedersen, L. (1993) Particle mesh Ewald: an N.log(N) method for Ewald sums in large systems J. Chem. Phys. 98, 10089-10092
51. Petrache, H. I., Tristram-Nagle, S., Gawrisch, K., Harries, D., Parsegian, V. A., and Nagle, J. F. (2004) Structure and fluctuations of charged phosphatidylserine bilayers in the absence of salt Biophys. J. 86, 1574-1586 (Pubitemid 38304847)
52. Wang, Y., Ohkubo, Y. Z., and Tajkhorshid, E. (2008) Gas conduction of lipid bilayers and membrane channels, in Current Topics in Membranes: Computational Modeling of Membrane Bilayers (Feller, S., Ed.) pp 343 - 367, Elsevier, New York.
53. Husted, C., Montez, B., Le, C., Moscarello, M. A., and Oldfield, E. (1993) C-13 magic-angle sample-spinning nuclear-magnetic-resonance studies of human myelin, and model membrane systems Magn. Reson. Med. 29, 168-178 (Pubitemid 23078509)
54. Denisov, I. G., McLean, M. A., Shaw, A. W., Grinkova, Y. V., and Sligar, S. G. (2005) Thermotropic phase transition in soluble nanoscale lipid bilayers J. Phys. Chem. B 109, 15580-15588 (Pubitemid 41260809)
55. Jacobson, K. and Papahadjopoulos, D. (1975) Phase transitions and phase separations in phospholipid membranes induced by changes in temperature, pH, and concentration of bivalent cations Biochemistry 14, 152-161
56. Silvius, J. R. and Gagne, J. (1984) Calcium-induced fusion and lateral phase separations in phosphatidylcholine-phosphatidylserine vesicles: correlation by calorimetric and fusion measurements Biochemistry 23, 3241-3247
57. Zhao, X., Eden, M., and Levitt, M. H. (2001) Recoupling of heteronuclear dipolar interactions in solid-state NMR using symmetry-based pulse sequences Chem. Phys. Lett. 342, 353-361 (Pubitemid 33628303)
58. Takegoshi, K., Nakamura, S., and Terao, T. (2001) C-13-H-1 dipolar-assisted rotational resonance in magic-angle spinning NMR Chem. Phys. Lett. 344, 631-637 (Pubitemid 33628408)
59. Morcombe, C. R., Gaponenko, V., Byrd, R. A., and Zilm, K. W. (2004) Diluting abundant spins by isotope edited radio frequency field assisted diffusion J. Am. Chem. Soc. 126, 7196-7197 (Pubitemid 38747768)
60. Hing, A., Vega, S., and Schaefer, J. (1992) Transferred-echo double-resonance NMR J. Magn. Reson. 96, 205-209
61. Lange, A., Luca, S., and Baldus, M. (2002) Structural constraints from proton-mediated rare-spin correlation spectroscopy in rotating solids J. Am. Chem. Soc. 124, 9704-9705
62. Lange, A., Seidel, K., Verdier, L., Luca, S., and Baldus, M. (2003) Analysis of proton-proton transfer dynamics in rotating solids and their use for 3D structure determination J. Am. Chem. Soc. 125, 12640-12648 (Pubitemid 37254778)
63. Jaroniec, C. P., Filip, C., and Griffin, R. G. (2002) 3D TEDOR NMR experiments for the simultaneous measurement of multiple carbon-nitrogen distances in uniformly C-13, N-15-labeled solids J. Am. Chem. Soc. 124, 10728-10742
64. Hauser, H., Pascher, I., and Sundell, S. (1988) Preferred conformation and dynamics of the glycerol backbone in phospholipids: an NMR and X-ray single-crystal analysis Biochemistry 27, 9166-9174
65. Browning, J. L. and Seelig, J. (1980) Bilayers of phosphatidylserine: deuterium and phosphorus nuclear magnetic-resonance study Biochemistry 19, 1262-1270
66. Mattai, J., Hauser, H., Demel, R. A., and Shipley, G. G. (1989) Interactions of metal ions with phosphatidylserine bilayer-membranes: effect of hydrocarbon chain unsaturation Biochemistry 28, 2322-2330 (Pubitemid 19084461)