The EF-hand Ca2+-binding protein p22 associates with microtubules in an N-myristoylation-dependent manner

Molecular Biology of the Cell

Volumn 10, Issue 10, 1999, Pages 3473-3488

  Timm, Sandy ^a   Titus, Brian ^a   Bernd, Karen ^b   Barroso, Margarida ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

^b DAVIDSON COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCINEURIN; CALCIUM BINDING PROTEIN; CALMODULIN; GLOBULAR PROTEIN;

ANIMAL CELL; ARTICLE; CELL FUNCTION; CELL MEMBRANE TRANSPORT; CONTROLLED STUDY; CYTOSKELETON; INTERPHASE; MICROTUBULE; MITOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; RAT; REGULATORY MECHANISM;

ANIMALIA;

EID: 0032830852     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.10.10.3473     Document Type: Article

References (103)

1. r 190,000. J. Biol. Chem. 265, 13849-13855.
2. 2+ binding to recoverin. J. Biol. Chem. 270, 4526-4533.
3. Apodaca, G., Enrich, C., and Mostov, K.E. (1994). The calmodulin antagonist, W-13, alters transcytosis, recycling, and the morphology of the endocytic pathway in Madin-Darby canine kidney cells. J. Biol. Chem. 269, 19005-19013.
4. 2+-binding protein, p22, is required for constitutive membrane traffic. J. Biol. Chem. 271, 10183-10187.
5. Barroso, M., Nelson, D.S., and Sztul, E. (1995). Transcytosis-associated protein (TAP)/p115 is a general fusion factor required for binding of vesicles to acceptor membranes. Proc. Natl. Acad. Sci. USA 92, 527-531.
6. Bashour, A.-M., and Bloom, G.S. (1998). 58K, a microrubule-binding Golgi protein, is a formiminotransferase cyclodeaminase. J. Biol. Chem. 273, 19612-19617.
7. Blocker, A., Griffiths, G., Olivo, J.-C., Hyman, A.A., and Severin, F.F. (1998). A role for microtubule dynamics in phagosome movement. J. Cell Sci. 111, 303-312.
8. Blocker, A., Severin, F.F., Habermann, A., Hyman, A.A., Griffiths, G., and Burkhardt, J.K. (1996). Microtubule-associated protein-dependent binding of phagosomes to microtubules. J. Biol. Chem. 271, 3803-3811.
9. Bloom, G.S., and Goldstein, L.S.B. (1998). Cruising along microtubule highways: how membranes move through the secretory pathway. J. Cell Biol. 140, 1277-1280.
10. Brown, S.W., Levinson, W., and Spudich, J.A. (1976). Cytoskeletal elements of chick embryo fibroblasts revealed by detergent extraction. J Supramol. Struct. 5, 119-130.
11. Carman, C.V., Som, T., Kim, C.M., and Benovic, J.L. (1998). Binding and phosphorylation of tubulin by G protein-coupled receptor kinases. J. Biol. Chem. 273, 20308-20316.
12. Chamberlain, L.H., Roth, D., Morgan, A., and Burgoyne, R.D. (1995). Distinct effects of alpha-SNAP, 14-3-3 proteins, and calmodulin on priming and triggering of regulated exocytosis. J. Cell Biol. 130, 1063-1070.
13. Chow, M., Newman, J.F., Filman, D., Hogle, J.M., Rowlands, D.J., and Brown, F. (1987). Myristylation of picornavirus capsid protein VP4 and its structural significance. Nature 327, 482-486.
14. Cole, N.B., and Lippincott-Schwartz, J. (1995). Organization of organelles and membrane traffic by microtubules. Curr. Opin. Cell Biol. 7, 55-64.
15. Colombo, M.I., Beron, W., and Stahl, P.D. (1997). Calmodulin regulates endosome fusion. J. Biol. Chem. 272, 7707-7712.
16. Cramer, L.P., and Mitchison, T.J. (1995). Myosin is involved in postmitotic cell spreading. J. Cell Biol. 131, 179-189.
17. de Figueiredo, P., and Brown, W.J. (1995). A role for calmodulin in organelle membrane tubulation. Mol. Biol. Cell 6, 871-887.
18. Franco, M., Chardin, P., Chabre, M., and Paris, S. (1996). Myristoylation-facilitated binding of the G protein ARF1GDP to membrane phospholipids is required for its activation by a soluble nucleotide exchange factor. J. Biol. Chem. 271, 1573-1578.
19. Fujii, T., Nakamura, A., Ogoma, Y., Kondo, Y., and Arai, T. (1990). Selective purification of microtubule-associated proteins 1 and 2 from rat brain using poly(L-aspartic acid). Anal. Biochem. 184, 268-273.
20. Gelfand, V.I., and Bershadsky, A.D. (1991). Microtubule dynamics: mechanism, regulation, and function. Annu. Rev. Cell Biol. 7, 93-116.
21. Gill, S.R., Schroer, T.A., Szilak, I., Steuer, E.R., Sheetz, M.P., and Cleveland, D.W. (1991). Dynactin, a conserved, ubiquitously expressed component of an activator of vesicle motility mediated by cytoplasmic dynein. J. Cell Biol. 115, 1639-1650.
22. Glaven, J.A., Whitehead, I., Bagrodia, S., Kay, R., and Cerione, R.A. (1999). The Dbl-related protein, Lfc, localizes to microtubules and mediates the activation of Rac signaling pathways in cells. J. Biol. Chem. 274, 2279-2285.
23. Gonzalez, M., Cambiazo, V., and Maccioni, R.B. (1998). The interaction of Mip-90 with microtubules and actin filaments in human fibroblasts. Exp. Cell Res. 239, 243-253.
24. Goodson, H.V., Valetti, C., and Kreis, T.E. (1997). Motors and membrane traffic. Curr. Opin. Cell Biol. 9, 18-28.
25. Grasso, J.A., Bruno, M., Yates, A.A., Wei, L.T., and Epstein, P.M. (1990). Calmodulin dependence of transferrin receptor recycling in rat reticulocytes. Biochem. J. 266, 261-272.
26. Gu, Y., Oyama, F., and Ihara, Y. (1996). Tau is widely expressed in rat tissues. J. Neurochem. 67, 1235-1244.
27. Gundersen, G.G., and Cook, T. (1999). Microtubules and signal transduction. Curr. Opin. Cell Biol. 11, 81-94.
28. Hennig, D., Scales, S.J., Moreau, A., Murley, L.L., DeMey, J., and Kreis, T.E. (1998). A formiminotransferase cyclodeaminase isoform is localized to the Golgi complex and can mediate interaction of trans-Golgi network-derived vesicles with microtubules. J. Biol. Chem. 273, 19602-19611.
29. Henriquez, J.P., Cambiazo, V., and Maccioni, R.B. (1996). Tubulin domains for the interaction of microtubule associated protein DMAP-85 from Drosophila melanogaster. Mol. Cell. Biochem. 158, 149-159.
30. Holleran, E.A., Karki, S., and Holzbaur, E.L.F. (1998). The role of the dynactin complex in intracellular motility. Int. Rev. Cytol. 182, 69-110.
31. Hunziker, W. (1994). The calmodulin antagonist W-7 affects transcytosis, lysosomal transport, and recycling but not endocytosis. J. Biol. Chem. 269, 29003-29009.
32. Iino S., Kobayashi S., Okazaki K., and Hidaka H. (1995a). Immunohistochemical localization of neurocalcin in the rat inner ear. Brain Res. 680, 128-134.
33. Iino, S., Kobayashi, S., Okazaki, K., and Hidaka, H. (1995b). Neurocalcin-immunoreactive receptor cells in the rat olfactory epithelium and vomeronasal organ. Neurosci. Lett. 191, 91-94.
34. 2+-binding and conformational response in EF-hand proteins. Trends Biochem. Sci. 21, 14-17.
35. Ivanenkov, V.V., Jamieson, G.A., Gruenstein, E., and Dimlich, R.V. (1995). Characterization of S-100b binding epitopes. Identification of a novel target, the actin capping protein, CapZ. J. Biol. Chem. 270, 14651-14658.
36. 2+-binding proteins 1: EF-hands. Protein Profile 1, 343-517.
37. Kennedy, M.T., Brockman, H., and Rusnak, F. (1996). Contributions of myristoylation to calcineurin structure/function. J. Biol. Chem. 271, 26517-26521.
38. Kerboeuf, D., Le Berre, A., Dedieu, J.-C., and Cohen, J. (1993). Calmodulin is essential for assembling links necessary for exocytotic membrane fusion in Paramecium. EMBO J. 12, 3385-3390.
39. Kibble, A.V., and Burgoyne, R.D. (1996). Calmodulin increases the initial rate of exocytosis in adrenal chromaffin cells. Pflügers Arch. Eur. J. Physiol. 431, 464-466.
40. Kilby, P.M., Van-Eldik, L.J., and Roberts, G.C. (1997). Identification of the binding site on S100B protein for the actin capping protein CapZ. Protein Sci. 6, 2494-2503.
41. 2+-binding light chain within Chlamydomonas outer arm dynein. J. Cell Sci. 108, 3757-3764.
42. Klee, C.B., Draetta, G.F., and Hubbard, J.M. (1988). Calcineurin. Adv. Enzymol. 61, 149-200.
43. Klopfenstein, D.R.C., Kappeler, F., and Hauri, H.-P. (1998). A novel direct interaction of endoplasmic reticulum with microtubules. EMBO J. 17, 6168-6177.
44. Kosik, K.S., Crandall, J.E., Mufson, E.J., and Neve, R.L. (1989). Tau in situ hybridization in normal and Alzheimer brain: localization in the somatodendritic compartment. Ann. Neurol. 26, 352-361.
45. Kosik, K.S., Orecchio, L.D., Binder, L., Trojanowski, J.Q., Lee, V.M., and Lee, G. (1988). Epitopes that span the tau molecule are shared with paired helical filaments. Neuron 1, 817-825.
46. 2+-independent calmodulin requirement for endocytosis in yeast. EMBO J. 13, 5539-5546.
47. Kuznetsov S.A., and Gelfand, V.I. (1986). Bovine brain kinesin is a microtubule-activated ATPase. Proc. Natl. Acad. Sci. USA 83, 8530-8534.
48. Lenz, S.E., Braunewell, K.H., Weise, C., Nedlina-Chittka, A., and Gundelfinger, E.D. (1996). The neuronal EF-hand Ca(2+)-binding protein VILIP: interaction with cell membrane and actin-based cytoskeleton. Biochem. Biophys. Res. Commun. 225, 1078-1083.
49. Lewis, S.A., Ivanov, I.E., Lee, G.H., and Cowan, N.J. (1989). Organization of microtubules in dendrites and axons is determined by a short hydrophobic zipper in microtubule-associated proteins MAP2 and tau. Nature 342, 498-505.
50. Liao, H., Li, Y., Brautigan, D.L., and Gundersen, G.G. (1998). Protein phosphatase 1 is targeted to microtubules by the microtubule-associated protein Tau. J. Biol. Chem. 273, 21901-21908.
51. Lin, X., and Barber, D.L. (1996). A calcineurin homologous protein inhibits GTPase-stimulated Na-H exchange. Proc. Natl. Acad. Sci. USA 93, 12631-12636.
52. Maccioni, R.B., and Cambiazo, V. (1995). Role of microtubule-associated proteins in the control of microtubule assembly. Physiol. Rev. 75, 835-864.
53. Mandelkow, E., and Mandelkow, E.-M. (1995). Microtubules and microtubule-associated proteins. Curr. Opin. Cell Biol. 7, 72-81.
54. Martone, M.E., Edelmann, V.M., Ellisman, M.H., and Nef, P. (1999). Cellular and subcellular distribution of the calcium-binding protein NCS-1 in the CNS of the rat. Cell Tissue Res. 295, 395-407.
55. Masson, D., and Kreis, T.E. (1993). Identification and molecular characterization of E-MAP-115, a novel microtubule-associated protein predominantly expressed in epithelial cells. J. Cell Biol. 123, 357-371.
56. McFerran, B.W., Graham, M.E., and Burgoyne, R.D. (1998). Neuronal Ca2+ sensor 1, the mammalian homologue of frequenin is expressed in chromaffin and PC12 cells and regulates neurosecretion from dense-core granules. J. Biol. Chem. 273, 22768-22772.
57. Michalik, L., Neuville P., Vanier, M.T., and Launay J.F. (1993). Biochemical and immunochemical identification of a microtubule-binding protein from bovine pancreas. Cell Motil. Cytoskeleton 25, 381-390.
58. Michalik, L., Neuville, P., Vanier, M.T., and Launay, J.F. (1995). Pancreatic tau related maps: biochemical and immunofluorescence analysis in a tumoral cell line. Mol. Cell. Biochem. 143, 107-112.
59. Nakamura, A., Arai, T., Kondo, Y., Fujii, T. (1989). Inhibitory effects of poly(L-aspartic acid) on the assembly of brain microtubules and the interaction of microtubule-associated protein 2 with F-actin in vitro. J. Biochem. (Tokyo) 106, 93-97.
60. Nakayama, S., and Kretsinger, R.H. (1994). Evolution of the EF-hand family of proteins. Annu. Rev. Biophys. Biomol. Struct. 23, 473-507.
61. Narasimhulu, S.B., and Reddy, A.S. (1998). Characterization of microtubule binding domains in the Arabidopsis kinesin-like calmodulin binding protein. Plant Cell 10, 957-965.
62. Naren, A.P., Nelson, D.J., Xie, W., Jovov, B., Pevsner, J., Bennett, M.K., Benos, D.J., Quick, M.W., and Kirk, K.L. (1997). Regulation of CFTR chloride channels by syntaxin and Munc18 isoforms. Nature 390, 302-305.
63. Niclas, J., Allan, V.J., and Vale, R.D. (1996). Cell cycle regulation of dynein association with membranes modulates microtubule-based organelle transport. J. Cell Biol. 133, 585-593.
64. Noble, M., Lewis, S.A., and Cowan, N.J. (1989). The microtubule binding domain of microtubule-associated protein MAP1B contains a repeated sequence motif unrelated to that of MAP2 and tau. J. Cell Biol. 109, 3367-3376.
65. Obar, R.A., Dingus, J., Bayley, H., and Vallee, R.B. (1989). The RII subunit of cAMP-dependent protein kinase binds to a common amino-terminal domain in microtubule-associated proteins 2A, 2B, and 2C. Neuron 3, 639-645.
66. 2+-binding protein frequenin. Proc. Natl. Acad. Sci. USA 92, 8001-8005.
67. Ookata, K., Hisanaga, S., Bulinski, J.C., Murofushi, H., Aizawa, H., Itoh, T.J., Hotani, H., Okumura, E., Tachibana, K., and Kishimoto, T. (1995). MAP4 is the in vivo substrate for CDC2 kinase in HeLa cells: identification of an M-phase specific and a cell cycle-independent phosphorylation site in MAP4. J. Cell Biol. 128, 849-862.
68. Osborn, M., and Weber, K. (1977). The display of microtubules in transformed cells. Cell 12, 561-571.
69. Paoletti, A., Moudjou, M., Paintrand, M., Salisbury, J.L., and Bornens, M. (1996). Most of centrin in animal cells is not centrosome-associated and centrosomal centrin is confined to the distal lumen of centrioles. J. Cell Sci. 109, 3089-3102.
70. Paschal, B.M., Shpetner, H.S., and Vallee, R.B. (1987). MAP 1C is a microtubule-activated ATPase which translocates microtubules in vitro and has dynein-like properties. J. Cell Biol. 105, 1273-1282.
71. Paschal, B.M., Shpetner, H.S., and Vallee, R.B. (1991). Purification of brain cytoplasmic dynein and characterization of its in vitro properties. Methods Enzymol. 196, 181-191.
72. Pierre, P., Scheel, J., Rickard, J.E., and Kreis, T.E. (1992). CLIP-170 links endocytic vesicles to microtubules. Cell 70, 887-900.
73. Pitcher, J.A., Hall, R.A., Daaka, Y., Zhang, J., Ferguson, S.S.G., Hester, S., Miller, S., Caron, M.G., Lefkowitz, R.J., and Barak, L.S. (1998). The G protein-coupled receptor kinase 2 is a microtubule-associated protein kinase that phosphorylates tubulin. J. Biol. Chem. 273, 12316-12324.
74. 2+-binding proteins in the retina. Trends Neurosci. 19, 547-554.
75. 2+-binding protein that modulates synaptic efficacy in the Drosophila nervous system. Neuron 11, 15-28.
76. Richter-Landsberg, C., and Heinrich, M. (1995). S-100 immunoreactivity in rat brain glial cultures is associated with both astrocytes and oligodendrocytes. J. Neurosci. Res. 42, 657-665.
77. Rickard, J.E., and Kreis, T.E. (1991). Binding of pp170 to microtubules is regulated by phosphorylation. Biol. Chem. 266, 17597-17605.
78. Roychowdhury, S., and Rasenick, M.M. (1997). G proteins b1γ2 subunits promote microtubule assembly. J. Biol. Chem. 272, 31576-31581.
79. Rubino, H.M., Dammerman, M., Shafit-Zagardo, B., and Erlichman J. (1989). Localization and characterization of the binding site for the regulatory subunit of type II cAMP-dependent protein kinase on MAP2. Neuron 3, 631-638.
80. Salisbury, J.L. (1995). Centrin, centrosomes, and mitotic spindle poles. Curr. Opin. Cell Biol. 7, 39-45.
81. 2+-binding proteins: functions and pathology. Trends Biochem. Sci. 21, 134-140.
82. Schoenfeld, T.A., and Obart, R.A. (1994). Diverse distribution and function of fibrous microtubule-associated proteins in the nervous system. Int. Rev. Cytol. 151, 67-137.
83. Schroer, T.A., Steuer, E.R., and Sheetz, M.P. (1989). Cytoplasmic dynein is a minus end-directed motor for membranous organelles. Cell 56, 937-946.
84. Sider, J.R., Mandato, C.A., Weber, K.L., Zandy, A.J., Beach, D., Finst, R.J., Skoble, J., and Bement, W.M. (1999). Direct observation of microtubule-f-actin interaction in cell free lysates. J. Cell Sci. 112, 1947-1956.
85. Song, J., Hirschman, J., Gunn, K., and Dohlman, H.G. (1996). Regulation of membrane and subunit interactions by N-myristoylation of a G protein alpha subunit in yeast. J. Biol. Chem. 271, 20273-20283.
86. Sontag, E., Numbhakdi-Craig, V., Bloom, G.S., and Mumby, M.C. (1995). A novel pool of protein phosphatase 2A is associated with microtubules and is regulated during the cell cycle. J. Cell Biol. 128, 1131-1144.
87. Sontag, E., Nunbhakdi-Craig, V., Lee, G., Bloom, G.S., and Mumby, M.C. (1996). Regulation of the phosphorylation state and microtubule-binding activity of Tau by protein phosphatase 2A. Cell 17, 1201-1207.
88. Swierczynski, S.L., and Blackshear, P.J. (1995). Membrane association of the myristoylated alanine-rich C kinase substrate (MARCKS) protein. Mutational analysis provides evidence for complex interactions. J. Biol. Chem. 270, 13436-13445.
89. Sztul, E. (1992). Transcytotic vesicle fusion with plasma membrane. Methods Enzymol. 219, 44-52.
90. Sztul, E., Colombo, M., Stahl, P., and Samanta, R. (1993). Control of protein traffic between distinct plasma membrane domains: requirement for a novel 108,000 protein in the fusion of transcytotic vesicles with the apical plasma membrane. J. Biol. Chem. 268, 1876-1885.
91. Sztul, E., Kaplin, A., Saucan, L., and Palade, G. (1991). Protein traffic between distinct plasma membrane domains: isolation and characterization of vesicular carriers involved in transcytosis. Cell 64, 81-89.
92. 2+-free state. Nature 376, 444-447.
93. Thissen, J.A., Gross, J.M., Subramanian, K., Meyer, T., and Casey, P.J. (1997). Prenylation-dependent association of Ki-Ras with microtubules. J. Biol. Chem. 272, 30362-30370.
94. Ulitzur, N., Rancano, C., and Pfeffer, S.R. (1997). Biochemical characterization of mapmodulin, a protein that binds microtubule-associated proteins. J. Biol. Chem. 272, 30577-30582.
95. Vale, R.D., Reese, T.S., and Sheetz, M.P. (1985). Identification of a novel force-generating protein, kinesin, involved in microtubule-based motility. Cell 42, 39-50.
96. Vallee, R.B. (1986). Purification of brain microtubules and microtubule-associated protein 1 using taxol. Methods Enzymol. 134, 104-115.
97. Vallee, R.B., and Sheetz, M.P. (1996). Targeting of motor proteins. Science 271, 1539-1544.
98. Wang, J.H., and Kelly, P.T. (1995). Postsynaptic injection of CA2+/ CaM induces synaptic potentiation requiring CaMKII and PKC activity. Neuron 15, 443-452.
99. Waterman-Storer, C.M., and Salmon, E.D. (1998). Endoplasmic reticulum membrane tubules are distributed by microtubules in living cells using three distinct mechanisms. Curr. Biol. 14, 798-806.
100. Williams, R.C., and Lee, J.C. (1982). Preparation of tubulin from brain. Methods Enzymol. 85, 376-385.
101. Yonemoto, W., McGlone, M.L., and Taylor, S.S. (1993). N-myristoylation of the catalytic subunit of cAMP-dependent protein kinase conveys structural stability. J. Biol. Chem. 268, 2348-2352.
102. Zheng, P., Eastman, J., Pol, S.V., and Pimplikar, S.W. (1998). PAT-1, a microrubule-interacting protein, recognizes the basolateral sorting signal of amyloid precursor protein. Proc. Natl. Acad. Sci. USA 95, 14745-14750.
103. 2+-myristoyl protein switch. Proc. Natl. Acad. Sci. USA 89, 11569-11573.