The curvature sensitivity of a membrane-binding amphipathic helix can be modulated by the charge on a flanking region

Biochemistry

Volumn 53, Issue 3, 2014, Pages 450-461

  Chong, Sharon S Y ^a   Taneva, Svetla G ^a   Lee, Joseph M C ^a,b   Cornell, Rosemary B ^a  

^a SIMON FRASER UNIVERSITY   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING STRENGTH; CHARGE REPULSION; CURVATURE SENSING; CURVATURE SENSITIVITIES; CURVED SURFACES; CYTIDYLYLTRANSFERASE; FLANKING REGIONS; MEMBRANE CURVATURE;

AMINO ACIDS; HYDROPHOBICITY; PROTEINS;

MEMBRANES;

ALPHA SYNUCLEIN; CHOLINE PHOSPHATE CYTIDYLYLTRANSFERASE; GLUTAMIC ACID; SERINE;

ARTICLE; DNA FLANKING REGION; DNA HELIX; HUMAN; HYDROPHOBICITY; IONIC STRENGTH; MEMBRANE BINDING; PHOSPHORYLATION; PRIORITY JOURNAL; STATIC ELECTRICITY;

ALPHA-SYNUCLEIN; AMINO ACID SEQUENCE; ANIMALS; CHOLINE-PHOSPHATE CYTIDYLYLTRANSFERASE; HUMANS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; LIPID BILAYERS; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; RATS; STATIC ELECTRICITY;

EID: 84893513074     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi401457r     Document Type: Article

References (80)

1. Hu, J., Shibata, Y., Voss, C., Shemesh, T., Li, Z., Coughlin, M., Kozlov, M. M., Rapoport, T. A., and Prinz, W. A. (2008) Membrane proteins of the endoplasmic reticulum induce high-curvature tubules Science 319, 1247-1250
2. Antonny, B. (2011) Mechanisms of membrane curvature sensing Annu. Rev. Biochem. 80, 101-123
3. Bigay, J. and Antonny, B. (2012) Curvature, lipid packing, and electrostatics of membrane organelles: Defining cellular territories in determining specificity Dev. Cell 23, 886-895
4. Bhatia, V. K., Hatzakis, N. S., and Stamou, D. (2010) A unifying mechanism accounts for sensing of membrane curvature by BAR domains, amphipathic helices and membrane-anchored proteins Semin. Cell Dev. Biol. 21, 381-390
5. Cui, H., Lyman, E., and Voth, G. A. (2011) Mechanism of membrane curvature sensing by amphipathic helix containing proteins Biophys. J. 100, 1271-1279
6. Drin, G. and Antonny, B. (2010) Amphipathic helices and membrane curvature FEBS Lett. 584, 1840-1847
7. Hatzakis, N. S., Bhatia, V. K., Larsen, J., Madsen, K. L., Bolinger, P. Y., Kunding, A. H., Castillo, J., Gether, U., Hedegard, P., and Stamou, D. (2009) How curved membranes recruit amphipathic helices and protein anchoring motifs Nat. Chem. Biol. 5, 835-841
8. Cornell, R. B. and Taneva, S. G. (2006) Amphipathic helices as mediators of the membrane interaction of amphitropic proteins, and as modulators of bilayer physical properties Curr. Protein Pept. Sci. 7, 539-552
9. Vanni, S., Vamparys, L., Gautier, R., Drin, G., Etchebest, C., Fuchs, P. F., and Antonny, B. (2013) Amphipathic lipid packing sensor motifs: Probing bilayer defects with hydrophobic residues Biophys. J. 104, 575-584
10. Davies, S. M., Epand, R. M., Kraayenhof, R., and Cornell, R. B. (2001) Regulation of CTP:phosphocholine cytidylyltransferase activity by the physical properties of lipid membranes: An important role for stored curvature strain energy Biochemistry 40, 10522-10531
11. Drin, G., Casella, J. F., Gautier, R., Boehmer, T., Schwartz, T. U., and Antonny, B. (2007) A general amphipathic α-helical motif for sensing membrane curvature Nat. Struct. Mol. Biol. 14, 138-146
12. Wieprecht, T., Beyermann, M., and Seelig, J. (2002) Thermodynamics of the coil-α-helix transition of amphipathic peptides in a membrane environment: The role of vesicle curvature Biophys. Chem. 96, 191-201
13. Vamparys, L., Gautier, R., Vanni, S., Bennett, W. F., Tieleman, D. P., Antonny, B., Etchebest, C., and Fuchs, P. F. (2013) Conical lipids in flat bilayers induce packing defects similar to that induced by positive curvature Biophys. J. 104, 585-593
14. Cornell, R. B. and Northwood, I. C. (2000) Regulation of CTP:phosphocholine cytidylyltransferase by amphitropism and relocalization Trends Biochem. Sci. 25, 441-447
15. Lee, J., Johnson, J., Ding, Z., Paetzel, M., and Cornell, R. B. (2009) Crystal structure of a mammalian CTP:phosphocholine cytidylyltransferase catalytic domain reveals novel active site residues within a highly conserved nucleotidyltransferase fold J. Biol. Chem. 284, 33535-33548
16. Taneva, S., Johnson, J. E., and Cornell, R. B. (2003) Lipid-induced conformational switch in the membrane binding domain of CTP:phosphocholine cytidylyltransferase: A circular dichroism study Biochemistry 42, 11768-11776
17. Friesen, J. A., Campbell, H. A., and Kent, C. (1999) Enzymatic and cellular characterization of a catalytic fragment of CTP:phosphocholine cytidylyltransferase α J. Biol. Chem. 274, 13384-13389
18. Ding, Z., Taneva, S. G., Huang, H. K., Campbell, S. A., Semenec, L., Chen, N., and Cornell, R. B. (2012) A 22-mer segment in the structurally pliable regulatory domain of metazoan CTP:phosphocholine cytidylyltransferase facilitates both silencing and activating functions J. Biol. Chem. 287, 38980-38991
19. Huang, H. K., Taneva, S. G., Lee, J., Silva, L. P., Schriemer, D. C., and Cornell, R. B. (2013) The membrane-binding domain of an amphitropic enzyme suppresses catalysis by contact with an amphipathic helix flanking its active site J. Mol. Biol. 425, 1546-1564
20. Bogan, M. J., Agnes, G. R., Pio, F., and Cornell, R. B. (2005) Interdomain and membrane interactions of CTP:phosphocholine cytidylyltransferase revealed via limited proteolysis and mass spectrometry J. Biol. Chem. 280, 19613-19624
21. MacDonald, J. I. and Kent, C. (1994) Identification of phosphorylation sites in rat liver CTP:phosphocholine cytidylyltransferase J. Biol. Chem. 269, 10529-10537
22. Kent, C. (1997) CTP:phosphocholine cytidylyltransferase Biochim. Biophys. Acta 1348, 79-90
23. Wang, Y. and Kent, C. (1995) Effects of altered phosphorylation sites on the properties of CTP:phosphocholine cytidylyltransferase J. Biol. Chem. 270, 17843-17849
24. Watkins, J. D. and Kent, C. (1991) Regulation of CTP:phosphocholine cytidylyltransferase activity and subcellular location by phosphorylation in Chinese hamster ovary cells. The effect of phospholipase C treatment J. Biol. Chem. 266, 21113-21117
25. Hatch, G. M., Jamil, H., Utal, A. K., and Vance, D. E. (1992) On the mechanism of the okadaic acid-induced inhibition of phosphatidylcholine biosynthesis in isolated rat hepatocytes J. Biol. Chem. 267, 15751-15758
26. Arnold, R. S., DePaoli-Roach, A. A., and Cornell, R. B. (1997) Binding of CTP:phosphocholine cytidylyltransferase to lipid vesicles: Diacylglycerol and enzyme dephosphorylation increase the affinity for negatively charged membranes Biochemistry 36, 6149-6156
27. Dennis, M. K., Taneva, S. G., and Cornell, R. B. (2011) The intrinsically disordered nuclear localization signal and phosphorylation segments distinguish the membrane affinity of two cytidylyltransferase isoforms J. Biol. Chem. 286, 12349-12360
28. Goulbourne, C. N., Malhas, A. N., and Vaux, D. J. (2011) The induction of a nucleoplasmic reticulum by prelamin A accumulation requires CTP:phosphocholine cytidylyltransferase-α J. Cell Sci. 124, 4253-4266
29. Malhas, A., Goulbourne, C., and Vaux, D. J. (2011) The nucleoplasmic reticulum: Form and function Trends Cell Biol. 21, 362-373
30. Gehrig, K., Cornell, R. B., and Ridgway, N. D. (2008) Expansion of the nucleoplasmic reticulum requires the coordinated activity of lamins and CTP:phosphocholine cytidylyltransferase α Mol. Biol. Cell 19, 237-247
31. Lagace, T. A. and Ridgway, N. D. (2005) The rate-limiting enzyme in phosphatidylcholine synthesis regulates proliferation of the nucleoplasmic reticulum Mol. Biol. Cell 16, 1120-1130
32. Taneva, S. G., Lee, J. M., and Cornell, R. B. (2012) The amphipathic helix of an enzyme that regulates phosphatidylcholine synthesis remodels membranes into highly curved nanotubules Biochim. Biophys. Acta 1818, 1173-1186
33. Kahle, P. J., Neumann, M., Ozmen, L., Muller, V., Jacobsen, H., Schindzielorz, A., Okochi, M., Leimer, U., van Der Putten, H., Probst, A., Kremmer, E., Kretzschmar, H. A., and Haass, C. (2000) Subcellular localization of wild-type and Parkinson's disease-associated mutant α-synuclein in human and transgenic mouse brain J. Neurosci. 20, 6365-6373
34. Burre, J., Sharma, M., Tsetsenis, T., Buchman, V., Etherton, M. R., and Sudhof, T. C. (2010) α-Synuclein promotes SNARE-complex assembly in vivo and in vitro Science 329, 1663-1667
35. Auluck, P. K., Caraveo, G., and Lindquist, S. (2010) α-Synuclein: Membrane interactions and toxicity in Parkinson's disease Annu. Rev. Cell Dev. Biol. 26, 211-233
36. Conway, K. A., Harper, J. D., and Lansbury, P. T. (1998) Accelerated in vitro fibril formation by a mutant α-synuclein linked to early-onset Parkinson disease Nat. Med. 4, 1318-1320
37. Fink, A. L. (2006) The aggregation and fibrillation of α-synuclein Acc. Chem. Res. 39, 628-634
38. Volles, M. J. and Lansbury, P. T., Jr. (2003) Zeroing in on the pathogenic form of α-synuclein and its mechanism of neurotoxicity in Parkinson's disease Biochemistry 42, 7871-7878
39. Periquet, M., Fulga, T., Myllykangas, L., Schlossmacher, M. G., and Feany, M. B. (2007) Aggregated α-synuclein mediates dopaminergic neurotoxicity in vivo J. Neurosci. 27, 3338-3346
40. Jao, C. C., Hegde, B. G., Chen, K., Haworth, I. S., and Langen, R. (2008) Structure of membrane-bound α-synuclein from site-directed spin labeling and computational refinement Proc. Natl. Acad. Sci. U.S.A. 105, 19666-19671
41. Bussell, R., Jr. and Eliezer, D. (2003) A structural and functional role for 11-mer repeats in α-synuclein and other exchangeable lipid binding proteins J. Mol. Biol. 329, 763-778
42. Davidson, W. S., Jonas, A., Clayton, D. F., and George, J. M. (1998) Stabilization of α-synuclein secondary structure upon binding to synthetic membranes J. Biol. Chem. 273, 9443-9449
43. Nuscher, B., Kamp, F., Mehnert, T., Odoy, S., Haass, C., Kahle, P. J., and Beyer, K. (2004) α-Synuclein has a high affinity for packing defects in a bilayer membrane: A thermodynamics study J. Biol. Chem. 279, 21966-21975
44. Recchia, A., Debetto, P., Negro, A., Guidolin, D., Skaper, S. D., and Giusti, P. (2004) α-Synuclein and Parkinson's disease FASEB J. 18, 617-626
45. Eliezer, D. (2013) The mysterious C-terminal tail of α-synuclein: Nanobody's guess J. Mol. Biol. 425, 2393-2396
46. Middleton, E. R. and Rhoades, E. (2010) Effects of curvature and composition on α-synuclein binding to lipid vesicles Biophys. J. 99, 2279-2288
47. Pranke, I. M., Morello, V., Bigay, J., Gibson, K., Verbavatz, J. M., Antonny, B., and Jackson, C. L. (2011) α-Synuclein and ALPS motifs are membrane curvature sensors whose contrasting chemistry mediates selective vesicle binding J. Cell Biol. 194, 89-103
48. Kjaer, L., Giehm, L., Heimburg, T., and Otzen, D. (2009) The influence of vesicle size and composition on α-synuclein structure and stability Biophys. J. 96, 2857-2870
49. Ouberai, M. M., Wang, J., Swann, M. J., Galvagnion, C., Guilliams, T., Dobson, C. M., and Welland, M. E. (2013) α-Synuclein senses lipid packing defects and induces lateral expansion of lipids leading to membrane remodeling J. Biol. Chem. 288, 20883-20895
50. Varkey, J., Isas, J. M., Mizuno, N., Jensen, M. B., Bhatia, V. K., Jao, C. C., Petrlova, J., Voss, J. C., Stamou, D. G., Steven, A. C., and Langen, R. (2010) Membrane curvature induction and tubulation are common features of synucleins and apolipoproteins J. Biol. Chem. 285, 32486-32493
51. Bisaglia, M., Tessari, I., Pinato, L., Bellanda, M., Giraudo, S., Fasano, M., Bergantino, E., Bubacco, L., and Mammi, S. (2005) A Topological Model of the Interaction between α-Synuclein and Sodium Dodecyl Sulfate Micelles Biochemistry 44, 329-339
52. Drescher, M., Veldhuis, G., van Rooijen, B. D., Milikisyants, S., Subramaniam, V., and Huber, M. (2008) Antiparallel Arrangement of the Helices of Vesicle-Bound α-Synuclein J. Am. Chem. Soc. 130, 7796-7797
53. Georgieva, E. R., Ramlall, T. F., Borbat, P. P., Freed, J. H., and Eliezer, D. (2010) The lipid-binding domain of wild type and mutant α-synuclein: Compactness and interconversion between the broken and extended helix forms J. Biol. Chem. 285, 28261-28274
54. Bartlett, G. R. (1959) Phosphorus assay in column chromatography J. Biol. Chem. 234, 466-468
55. Bradford, M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Anal. Biochem. 72, 248-254
56. Cornell, R. B. (1991) Regulation of CTP:phosphocholine cytidylyltransferase by lipids. 1. Negative surface charge dependence for activation Biochemistry 30, 5873-5880
57. Taneva, S. G., Patty, P. J., Frisken, B. J., and Cornell, R. B. (2005) CTP:phosphocholine cytidylyltransferase binds anionic phospholipid vesicles in a cross-bridging mode Biochemistry 44, 9382-9393
58. Brewer, J. M., Tetley, L., Richmond, J., Liew, F. Y., and Alexander, J. (1998) Lipid vesicle size determines the Th1 or Th2 response to entrapped antigen J. Immunol. 161, 4000-4007
59. Frederick, T. E., Chebukati, J. N., Mair, C. E., Goff, P. C., and Fanucci, G. E. (2009) Bis(monoacylglycero)phosphate forms stable small lamellar vesicle structures: Insights into vesicular body formation in endosomes Biophys. J. 96, 1847-1855
60. Matsuzaki, K., Murase, O., Sugishita, K., Yoneyama, S., Akada, K., Ueha, M., Nakamura, A., and Kobayashi, S. (2000) Optical characterization of liposomes by right angle light scattering and turbidity measurement Biochim. Biophys. Acta 1467, 219-226
61. Mayer, L. D., Hope, M. J., and Cullis, P. R. (1986) Vesicles of variable sizes produced by a rapid extrusion procedure Biochim. Biophys. Acta 858, 161-168
62. Sreerama, N. and Woody, R. W. (2000) Estimation of protein secondary structure from circular dichroism spectra: Comparison of CONTIN, SELCON, and CDSSTR methods with an expanded reference set Anal. Biochem. 287, 252-260
63. Murray, D., Hermida-Matsumoto, L., Buser, C. A., Tsang, J., Sigal, C. T., Ben-Tal, N., Honig, B., Resh, M. D., and McLaughlin, S. (1998) Electrostatics and the membrane association of Src: Theory and experiment Biochemistry 37, 2145-2159
64. Buser, C. A. and McLaughlin, S. (1998) Ultracentrifugation technique for measuring the binding of peptides and proteins to sucrose-loaded phospholipid vesicles Methods Mol. Biol. 84, 267-281
65. Mesmin, B., Drin, G., Levi, S., Rawet, M., Cassel, D., Bigay, J., and Antonny, B. (2007) Two lipid-packing sensor motifs contribute to the sensitivity of ArfGAP1 to membrane curvature Biochemistry 46, 1779-1790
66. Dowhan, W. (1997) Molecular basis for membrane phospholipid diversity: Why are there so many lipids? Annu. Rev. Biochem. 66, 199-232
67. Lim, L. and Wenk, M. R. (2009) Neuronal Membrane Lipids: Their Role in the Synaptic Vesicle Cycle. In Neural Lipids (Tettamanti, G., and Goracci, G., Eds.) pp 224-238, Springer Science.
68. Shai, Y. (1999) Mechanism of the binding, insertion and destabilization of phospholipid bilayer membranes by α-helical antimicrobial and cell non-selective membrane-lytic peptides Biochim. Biophys. Acta 1462, 55-70
69. Jensen, M. B., Bhatia, V. K., Jao, C. C., Rasmussen, J. E., Pedersen, S. L., Jensen, K. J., Langen, R., and Stamou, D. (2011) Membrane curvature sensing by amphipathic helices: A single liposome study using α-synuclein and annexin B12 J. Biol. Chem. 286, 42603-42614
70. McLaughlin, S. and Aderem, A. (1995) The myristoyl-electrostatic switch: A modulator of reversible protein-membrane interactions Trends Biochem. Sci. 20, 272-276
71. McLaughlin, S. and Murray, D. (2005) Plasma membrane phosphoinositide organization by protein electrostatics Nature 438, 605-611
72. Tamm, L. K. (1994) Physical Studies of Peptide-Bilayer Interactions. In Membrane Protein Structure (White, S. H., Ed.) pp 283-313, Springer, New York.
73. Kuwahara, T., Tonegawa, R., Ito, G., Mitani, S., and Iwatsubo, T. (2012) Phosphorylation of α-synuclein protein at Ser-129 reduces neuronal dysfunction by lowering its membrane binding property in Caenorhabditis elegans J. Biol. Chem. 287, 7098-7109
74. Visanji, N. P., Wislet-Gendebien, S., Oschipok, L. W., Zhang, G., Aubert, I., Fraser, P. E., and Tandon, A. (2011) Effect of Ser-129 phosphorylation on interaction of α-synuclein with synaptic and cellular membranes J. Biol. Chem. 286, 35863-35873
75. Sevcsik, E., Trexler, A. J., Dunn, J. M., and Rhoades, E. (2011) Allostery in a disordered protein: Oxidative modifications to α-synuclein act distally to regulate membrane binding J. Am. Chem. Soc. 133, 7152-7158
76. Gehrig, K. and Ridgway, N. D. (2011) CTP:phosphocholine cytidylyltransferase α (CCTα) and lamins alter nuclear membrane structure without affecting phosphatidylcholine synthesis Biochim. Biophys. Acta 1811, 377-385
77. Garnier-Lhomme, M., Byrne, R. D., Hobday, T. M., Gschmeissner, S., Woscholski, R., Poccia, D. L., Dufourc, E. J., and Larijani, B. (2009) Nuclear envelope remnants: Fluid membranes enriched in sterols and polyphosphoinositides PLoS One 4, e4255
78. Karanasios, E., Han, G. S., Xu, Z., Carman, G. M., and Siniossoglou, S. (2010) A phosphorylation-regulated amphipathic helix controls the membrane translocation and function of the yeast phosphatidate phosphatase Proc. Natl. Acad. Sci. U.S.A. 107, 17539-17544
79. Cabrera, M., Langemeyer, L., Mari, M., Rethmeier, R., Orban, I., Perz, A., Brocker, C., Griffith, J., Klose, D., Steinhoff, H. J., Reggiori, F., Engelbrecht-Vandre, S., and Ungermann, C. (2010) Phosphorylation of a membrane curvature-sensing motif switches function of the HOPS subunit Vps41 in membrane tethering J. Cell Biol. 191, 845-859
80. Krabben, L., Fassio, A., Bhatia, V. K., Pechstein, A., Onofri, F., Fadda, M., Messa, M., Rao, Y., Shupliakov, O., Stamou, D., Benfenati, F., and Haucke, V. (2011) Synapsin I senses membrane curvature by an amphipathic lipid packing sensor motif J. Neurosci. 31, 18149-18154