Plasma membrane phosphoinositide organization by protein electrostatics

Nature

Volumn 438, Issue 7068, 2005, Pages 605-611

  McLaughlin, Stuart ^a   Murray, Diana ^b  

^a STONY BROOK UNIVERSITY   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOLOGY; ELECTROSTATICS; ENZYMES; PHOSPHOLIPIDS; PROTEINS;

FLUID BILAYER; MEMBRANE PROTEINS; PHOSPHATIDYLINOSITOL 4;

CELL MEMBRANES;

CALCIUM; PHOSPHATIDYLINOSITIDE; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; PROTEIN;

MEMBRANE; PROTEIN;

BILAYER MEMBRANE; CALCIUM CELL LEVEL; ENDOCYTOSIS; ENZYME ACTIVATION; EXOCYTOSIS; LIPID BILAYER; PHOSPHOINOSITIDE METABOLISM; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; REVIEW; SECOND MESSENGER; STRUCTURE ANALYSIS;

EID: 28444477387     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature04398     Document Type: Review

References (85)

1. Berridge, M. J. & Irvine, R. F. Inositol trisphosphate, a novel second messenger in cellular signal transduction. Nature 312, 315-321 (1984).
2. Berridge, M. J. & Irvine, R. F. Inositol phosphates and cell signalling. Nature 341, 197-205 (1989).
3. Rhee, S. G. Regulation of phosphoinositide-specific phospholipase C. Annu. Rev. Biochem. 70, 281-312 (2001).
4. Rebecchi, M. J. & Pentyala, S. N. Structure, function, and control of phosphoinositide-specific phospholipase C. Physiol. Rev. 80, 1291-1335 (2000).
5. 2+ oscillations and egg activation in mammals is a novel phospholipase C: PLCQ. Reproduction 127, 431-439 (2004).
6. Cantley, L. C. The phosphoinositide 3-kinase pathway. Science 296, 1655-1657 (2002).
7. Cho, W. & Stahelin, R. V. Membrane-protein interactions in cell signaling and membrane trafficking. Annu. Rev. Biophys. Biomol. Struct. 34, 119-151 (2005).
8. DiNitto, J. P., Cronin, T. C. & Lambright, D. G. Membrane recognition and targeting by lipid-binding domains. Sci. STKE 2003, re16 (2003).
9. Lemmon, M. A. Phosphoinositide recognition domains. Traffic 4, 201-213 (2003).
10. Hurley, J. H. & Meyer, T. Subcellular targeting by membrane lipids. Curr. Opin. Cell Biol. 13, 146-152 (2001).
11. Sun, B. C. & Hille, B. Regulation of ion channels by phosphatidylinositol 4,5-bisphosphate. Curr. Opin. Neurobiol. 15, 370-378 (2005).
12. Hilgemann, D. W. Biochemistry. Oily barbarians breach ion channel gates. Science 304, 223-224 (2004).
13. Honing, S. et al. Phosphatidylinositol-(4,5)-bisphosphate regulates sorting signal recognition by the clathrin-associated adaptor complex AP2. Mol. Cell 18, 519-531 (2005).
14. Wenk, M. R. & De Camilli, P. Protein-lipid interactions and phosphoinositide metabolism in membrane traffic: insights from vesicle recycling in nerve terminals. Proc. Natl Acad. Sci. USA 101, 8262-8269 (2004).
15. Simonsen, A., Wurmser, A. E., Emr, S. D. & Stenmark, H. The role of phosphoinositides in membrane transport. Curr. Opin. Cell Biol. 13, 485-492 (2001).
16. Botelho, R. J. et al. Localized biphasic changes in phosphatidylinositol- 4,5-bisphosphate at sites of phagocytosis. J. Cell Biol. 151, 1353-1368 (2000).
17. 2 as being important in exocytosis. J. Biol. Chem. 275, 17878-17885 (2000).
18. 2 regulation of surface membrane traffic. Curr. Opin. Cell Biol. 13, 493-499 (2001).
19. 2 synthesis in nerve terminals produces defects in synaptic vesicle trafficking. Nature 431, 415-422 (2004).
20. Janmey, P. A. & Lindberg, U. Cytoskeletal regulation: rich in lipids. Nature Rev. Mol. Cell Biol. 5, 658-666 (2004).
21. 2 density. Mol. Cell 17, 181-191 (2005).
22. Raucher, D. et al. Phosphatidylinositol 4,5-bisphosphate functions as a second messenger that regulates cytoskeleton-plasma membrane adhesion. Cell 100, 221-228 (2000).
23. Sciorra, V. A. et al. Dual role for phosphoinositides in regulation of yeast and mammalian phospholipase D enzymes. J. Cell Biol. 159, 1039-1049 (2002).
24. Hinchliffe, K. A., Ciruela, A. & Irvine, R. F. PIPkins, their substrates and their products: new functions for old enzymes. Biochim. Biophys. Acta 1436, 87-104 (1998).
25. 2 signaling in lipid domains: a critical re-evaluation. EMBO J. 24, 1664-1673 (2005).
26. 2-dependent microdomain assemblies capture microtubules to promote and control leading edge motility. J. Cell Biol. 169, 151-165 (2005).
27. Berridge, M. J., Bootman, M. D. & Roderick, H. L. Calcium signalling: dynamics, homeostasis and remodelling. Nature Rev. Mol. Cell Biol. 4, 517-529 (2003).
28. Laux, T. et al. GAP43, MARCKS, and CAP23 modulate PI(4,5)P2 at plasmalemmal rafts, and regulate cell cortex actin dynamics through a common mechanism. J. Cell Biol. 149, 1455-1472 (2000).
29. Dunker, A. K. et al. Intrinsically disordered protein. J. Mol. Graph. Model. 19, 26-59 (2001).
30. Uversky, V. N. What does it mean to be natively unfolded? Eur. J. Biochem. 269, 2-12 (2002).
31. Aderem, A. The MARCKS brothers: a family of protein kinase C substrates. Cell 71, 713-716 (1992).
32. Blackshear, P. J. The MARCKS family of cellular protein kinase C substrates. J. Biol. Chem. 268, 1501-1504 (1993).
33. McLaughlin, S. & Aderem, A. The myristoyl-electrostatic switch: a modulator of reversible protein-membrane interactions. Trends Biochem. Sci. 20, 272-276 (1995).
34. Arbuzova, A., Schmitz, A. A. & Vergeres, G. Cross-talk unfolded: MARCKS proteins. Biochem. J. 362, 1-12 (2002).
35. Sundaram, M., Cook, H. W. & Byers, D. M. The MARCKS family of phospholipid binding proteins: regulation of phospholipase D and other cellular components. Biochem. Cell Biol. 82, 191-200 (2004).
36. Taniguchi, H. & Manenti, S. Interaction of myristoylated alanine-rich protein kinase C substrate (MARCKS) with membrane phospholipids. J. Biol. Chem. 268, 9960-9963 (1993).
37. Kim, J., Shishido, T., Jiang, X., Aderem, A. & McLaughlin, S. Phosphorylation, high ionic strength, and calmodulin reverse the binding of MARCKS to phospholipid vesicles. J. Biol. Chem. 269, 28214-28219 (1994).
38. Rusu, L., Gambhir, A., McLaughlin, S. & Radler, J. Fluorescence correlation spectroscopy studies of peptide and protein binding to phospholipid vesicles. Biophys. J. 87, 1044-1053 (2004).
39. 2 on phospholipid membranes by basic/aromatic regions of proteins. Biophys. J. 86, 2188-2207 (2004).
40. Arbuzova, A., Murray, D. & McLaughlin, S. MARCKS, membranes, and calmodulin: kinetics of their interaction. Biochim. Biophys. Acta 1376, 369-379 (1998).
41. Ohmori, S. et al. Importance of protein kinase C targeting for the phosphorylation of its substrate, myristoylated alanine-rich C-kinase substrate. J. Biol. Chem. 275, 26449-26457 (2000).
42. Qin, Z. & Cafiso, D. S. Membrane structure of protein kinase C and calmodulin binding domain of myristoylated alanine rich C kinase substrate determined by site-directed spin labeling. Biochemistry 35, 2917-2925 (1996).
43. Wang, J., Arbuzova, A., Hangyas-Mihalyne, G. & McLaughlin, S. The effector domain of myristoylated alanine-rich C kinase substrate binds strongly to phosphatidylinositol 4,5-bisphosphate. J. Biol. Chem. 276, 5012-5019 (2001).
44. Victor, K., Jacob, J. & Cafiso, D. S. Interactions controlling the membrane binding of basic protein domains: phenylalanine and the attachment of the myristoylated alanine-rich C-kinase substrate protein to interfaces. Biochemistry 38, 12527-12536 (1999).
45. Zhang, W., Crocker, E., McLaughlin, S. & Smith, S. O. 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 (2003).
46. Ellena, J. F., Burnitz, M. C. & Cafiso, D. S. Location of the myristoylated alanine-rich C-kinase substrate (MARCKS) effector domain in negatively charged phospholipid bicelles. Biophys. J. 85, 2442-2448 (2003).
47. White, S. H. & Wimley, W. C. Membrane protein folding and stability: physical principles. Annu. Rev. Biophys. Biomol. Struct. 28, 319-365 (1999).
48. Clapperton, J. A., Martin, S. R., Smerdon, S. J., Gamblin, S. J. & Bayley, P. M. Structure of the complex of calmodulin with the target sequence of calmodulin-dependent protein kinase I: studies of the kinase activation mechanism. Biochemistry 41, 14669-14679 (2002).
49. Porumb, T., Crivici, A., Blackshear, P. J. & Ikura, M. Calcium binding and conformational properties of calmodulin complexed with peptides derived from myristoylated alanine-rich C kinase substrate (MARCKS) and MARCKS-related protein (MRP). Eur. Biophys. J. 25, 239-247 (1997).
50. 2+-calmodulin. Nature Struct. Biol. 10, 226-231 (2003).
51. Benowitz, L. I. & Routtenberg, A. GAP-43: an intrinsic determinant of neuronal development and plasticity. Trends Neurosci. 20, 84-91 (1997).
52. Liu, Y. C. & Storm, D. R. Regulation of free calmodulin levels by neuromodulin: neuron growth and regeneration. Trends Pharmacol. Sci. 11, 107-111 (1990).
53. Liang, X., Lu, Y., Neubert, T. A. & Resh, M. D. Mass spectrometric analysis of GAP-43/neuromodulin reveals the presence of a variety of fatty acylated species. J. Biol. Chem. 277, 33032-33040 (2002).
54. Skene, J. H. & Virag, I. Posttranslational membrane attachment and dynamic fatty acylation of a neuronal growth cone protein, GAP-43. J. Cell Biol. 108, 613-624 (1989).
55. Persechini, A. & Stemmer, P. M. Calmodulin is a limiting factor in the cell. Trends Cardiovasc. Med. 12, 3-37 (2002).
56. 2+. Cell Calcium 35, 415-425 (2004).
57. Isotani, E. et al. Real-time evaluation of myosin light chain kinase activation in smooth muscle tissues from a transgenic calmodulin-biosensor mouse. Proc. Natl Acad. Sci. USA 101, 6279-6284 (2004).
58. Wang, J. et al. Lateral sequestration of phosphatidylinositol 4,5-bisphosphate by the basic effector domain of myristoylated alanine-rich C kinase substrate is due to nonspecific electrostatic interactions. J. Biol. Chem. 277, 34401-34412 (2002).
59. Holthuis, J. C. & Levine, T. P. Lipid traffic: floppy drives and a superhighway. Nature Rev. Mol. Cell Biol. 6, 209-220 (2005).
60. 2 and proteins: interactions, organization, and information flow. Annu. Rev. Biophys. Biomol. Struct 31, 151-175 (2002).
61. McLaughlin, S. The electrostatic properties of membranes. Annu. Rev. Biophys. Biophys. Chem. 18, 113-136 (1989).
62. Ben-Tal, N., Honig, B., Peitzsch, R. M., Denisov, G. & McLaughlin, S. Binding of small basic peptides to membranes containing acidic lipids: theoretical models and experimental results. Biophys. J. 71, 561-575 (1996).
63. Murray, D., Arbuzova, A., Honig, B. & McLaughlin, S. The role of electrostatic and nonpolar interactions in the association of peripheral proteins with membranes. Curr. Top. Membr. 52, 271-302 (2002).
64. 2 by membrane-adsorbed basic peptides. Biophys. J. 86, 1969-1986 (2004).
65. McLaughlin, S., Smith, S. O., Hayman, M. J. & Murray, D. An electrostatic engine model for autoinhibition and activation of the epidermal growth factor receptor (EGFR/ErbB) family. J. Gen. Physiol. 126, 41-53 (2005).
66. Wollmuth, L. P. & Sobolevsky, A. I. Structure and gating of the glutamate receptor ion channel. Trends Neurosci. 27, 321-328 (2004).
67. Ehlers, M. D., Zhang, S., Bernhadt, J. P. & Huganir, R. L. Inactivation of NMDA receptors by direct interaction of calmodulin with the NR1 subunit. Cell 84, 745-755 (1996).
68. Ferguson, K. M. Active and inactive conformations of the epidermal growth factor receptor. Biochem. Soc. Trans. 32, 742-745 (2004).
69. Uyemura, T., Takagi, H., Yanagida, T. & Sako, Y. Single-molecule analysis of epidermal growth factor signaling that leads to ultrasensitive calcium response. Biophys. J. 88, 3720-3730 (2005).
70. De Matteis, M. A. & Godi, A. PI-loting membrane traffic. Nature Cell Biol. 6, 487-492 (2004).
71. Honda, A. et al. Phosphatidylinositol 4-phosphate 5-kinase 4 is a downstream effector of the small G protein ARF6 in membrane ruffle formation. Cell 99, 521-532 (1999).
72. Tall, E. G., Spector, I., Pentyala, S. N., Bitter, I. & Rebecchi, M. J. Dynamics of phosphatidylinositol 4,5-bisphosphate in actin-rich structures. Curr. Biol. 10, 743-746 (2000).
73. Watt, S. A., Kular, G., Fleming, I. N., Downes, C. P. & Lucocq, J. M. Subcellular localization of phosphatidylinositol 4,5-bisphosphate using the pleckstrin homology domain of phospholipase C 61. Biochem. J. 363, 657-666 (2002).
74. 2 hydrolysis inhibits cortical actin dynamics: regulation at a global but not at a micrometer scale. Mol. Biol. Cell 13, 3257-3267 (2002).
75. Doughman, R. L., Firestone, A. J. & Anderson, R. A. Phosphatidylinositol phosphate kinases put PI4,5P2 in its place. J. Membr. Biol. 194, 77-89 (2003).
76. 2+- calmodulin and protein kinase Cs: a hypothetical synthesis of their conflicting convergences on shared substrate domains. Trends Neurosci. 22, 12-16 (1999).
77. Van Haastert, P. J. & Devreotes, P. N. Chemotaxis: signalling the way forward. Nature Rev. Mol. Cell Biol. 5, 626-634 (2004).
78. Singh, S. M. & Murray, D. Molecular modeling of the membrane targeting of phospholipase C pleckstrin homology domains. Protein Sci. 12, 1934-1953 (2003).
79. Gallagher, K. & Sharp, K. Electrostatic contributions to heat capacity changes of DNA-ligand binding. Biophys. J. 75, 769-776 (1998).
80. Nicholls, A., Sharp, K. A. & Honig, B. Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins 11, 281-296 (1991).
81. Hunter, T., Ling, N. & Cooper, J. A. Protein kinase C phosphorylation of the EGF receptor at a threonine residue close to the cytoplasmic face of the plasma membrane. Nature 311, 480-483 (1984).
82. Ullrich, A. et al. Human epidermal growth factor receptor cDNA sequence and aberrant expression of the amplified gene in A431 epidermoid carcinoma cells. Nature 309, 418-425 (1984).
83. Li, H., Ruano, M. J. & Villalobo, A. Endogenous calmodulin interacts with the epidermal growth factor receptor in living cells. FEBS Lett. 559, 175-180 (2004).
84. Graff, J. M., Young, T. N., Johnson, J. D. & Blackshear, P. J. Phosphorylation-regulated calmodulin binding to a prominent cellular substrate for protein kinase C. J. Biol. Chem. 264, 21818-21823 (1989).
85. Yamniuk, A. P. & Vogel, H. J. Calmodulin's flexibility allows for promiscuity in its interactions with target proteins and peptides. Mol. Biotechnol. 27, 33-57 (2004).