Critical role of cAMP-dependent protein kinase anchoring to the L-type calcium channel Cav1.2 via A-kinase anchor protein 150 in neurons

Biochemistry

Volumn 46, Issue 6, 2007, Pages 1635-1646

  Hall, Duane D ^a,e   Davare, Monika A ^b,c   Shi, Mei ^a   Allen, Margaret L ^d   Weisenhaus, Michael ^d   McKnight, G Stanley ^d   Hell, Johannes W ^a,b,e  

^a UNIVERSITY OF IOWA   (United States)

^b UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^c OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^d UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADRENERGIC STIMULATION; CELLULAR FUNCTIONS; GENE DISRUPTION; NEURONS; PROTEIN KINASE (PKA);

CYTOLOGY; GENETIC ENGINEERING; NEUROLOGY; PHYSIOLOGY; PROTEINS;

ENZYME KINETICS;

ADENYLATE CYCLASE; BETA 2 ADRENERGIC RECEPTOR; CALCIUM CHANNEL L TYPE; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP DEPENDENT PROTEIN KINASE ANCHORING PROTEIN; CYCLIC AMP DEPENDENT PROTEIN KINASE ANCHORING PROTEIN 150; MICROTUBULE ASSOCIATED PROTEIN 2; PROTEIN SUBUNIT; SERINE; STIMULATORY GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG; VOLTAGE GATED CALCIUM CHANNEL; VOLTAGE GATED CALCIUM CHANNEL 1.2;

ANIMAL TISSUE; ARTICLE; BETA ADRENERGIC STIMULATION; BRAIN NERVE CELL; CALCIUM SIGNALING; CHANNEL GATING; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME BINDING; ENZYME LOCALIZATION; GENE DISRUPTION; IMMUNOPRECIPITATION; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; REGULATORY MECHANISM;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AMINO ACID SEQUENCE; ANIMALS; CALCIUM CHANNELS, L-TYPE; CYCLIC AMP-DEPENDENT PROTEIN KINASES; CYTOSKELETAL PROTEINS; ISOPROTERENOL; MICE; MICE, KNOCKOUT; MICROTUBULE-ASSOCIATED PROTEINS; NEURONS; PHOSPHORYLATION; RATS; RECEPTORS, ADRENERGIC, BETA-2; SERINE; SIGNAL TRANSDUCTION;

BOVINAE; MUS; RATTUS;

EID: 33846982906     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi062217x     Document Type: Article

References (89)

1. Helton, T. D., Xu, W., and Lipscombe, D. (2005) Neuronal L-type calcium channels open quickly and are inhibited slowly, J. Neurosci. 25, 10247-10251.
2. 2+ channels in NMDA receptor-independent synaptic plasticity and spatial memory, J. Neurosci. 25, 9883-9892.
3. 2+ channels in hippocampal neurons, Nature 395, 900-905.
4. Bolshakov, V. Y., and Siegelbaum, S. A. (1994) Postsynaptic induction and presynaptic expression of hippocampal long-term depression, Science 264, 148-152.
5. 2+ channels to homosynaptic long-term depression in the CA1 region in vitro, J. Neurophysiol. 77, 1651-1655.
6. Grover, L. M., and Teyler, T. J. (1990) Two components of long-term potentiation induced by different patterns of afferent activation, Nature 347, 477-479.
7. Wang, H. X., Gerkin, R. C., Nauen, D. W., and Bi, G. Q. (2005) Coactivation and timing-dependent integration of synaptic potentiation and depression, Nat. Neurosci. 8, 187-193.
8. Dolmetsch, R. E., Pajvani, U., Fife, K., Spotts, J. M., and Greenberg, M. E. (2001) Signaling to the nucleus by an L-type calcium channel-calmodulin complex through the MAP kinase pathway, Science 294, 333-339.
9. Ghosh, A., and Greenberg, M. E. (1995) Calcium signaling in neurons: molecular mechanisms and cellular consequences, Science 268, 239-247.
10. Bean, B. P., Nowycky, M. C., and Tsien, R. W. (1984) β-Adrenergic modulation of calcium channels in frog ventricular heart cells, Nature 307, 371-375.
11. De Jongh, K. S., Murphy, B. J., Colvin, A. A., Hell, J. W., Takahashi, M., and Catterall, W. A. (1996) Specific phosphorylation of a site in the full length form of the α1 subunit of the cardiac L-type calcium channel by adenosine 3′,5′-cyclic monophosphate-dependent protein kinase, Biochemistry 35, 10392-10402.
12. Reuter, H. (1983) Calcium channel modulation by neurotransmitters, enzymes and drugs, Nature 301, 569-574.
13. Fisher, R., and Johnston, D. (1990) Differential modulation of single voltage-gated calcium channels by cholinergic and adrenergic agonists in adult hippocampal neurons, J. Neurophysiol. 64, 1291-1302.
14. Gray, R., and Johnston, D. (1987) Noradrenaline and beta-adrenoceptor agonists increase activity of voltage-dependent calcium channels in hippocampal neurons, Nature 327, 620-622.
15. Gross, R. A., Uhler, M. D., and Macdonald, R. L. (1990) The cyclic AMP-dependent protein kinase catalytic subunit selectively enhances calcium currents in rat nodose neurones, J. Physiol. 429, 483-496.
16. 2+ channels in dendritic spines by activation of beta2 adrenergic receptors, J. Neurosci. 24, 8416-8427.
17. Surmeier, D. J., Bargas, J., Hemmings, H. C., Jr., Nairn, A. C., and Greengard, P. (1995) Modulation of calcium currents by a D1 dopaminergic protein kinase/phosphatase cascade in rat neostriatal neurons, Neuron 14, 385-397.
18. Ertel, E. A., Campbell, K. P., Harpold, M. M., Hofmann, F., Mori, Y., Perez-Reyes, E., Schwartz, A., Snutch, T. P., Tanabe, T., Birnbaumer, L., Tsien, R. W., and Catterall, W. A. (2000) Nomenclature of voltage-gated calcium channels, Neuron 25, 533-535.
19. Hell, J. W., Westenbroek, R. E., Warner, C., Ahlijanian, M. K., Prystay, W., Gilbert, M. M., Snutch, T. P., and Catterall, W. A. (1993) Identification and differential subcellular localization of the neuronal class C and class D L-type calcium channel α1 subunits, J. Cell Biol. 123, 949-962.
20. Hell, J. W., Yokoyama, C. T., Wong, S. T., Warner, C., Snutch, T. P., and Catterall, W. A. (1993) Differential phosphorylation of two size forms of the neuronal class C L-type calcium channel α1 subunit, J. Biol. Chem. 268, 19451-19457.
21. 2+ channels, J. Clin. Invest. 113, 1430-1439.
22. 2+ channels, Annu. Rev. Cell Dev. Biol. 16, 521-555.
23. Viard, P., Butcher, A. J., Halet, G., Davies, A., Nurnberg, B., Heblich, F., and Dolphin, A. C. (2004) PI3K promotes voltage-dependent calcium channel trafficking to the plasma membrane, Nat. Neurosci. 7, 939-946.
24. Sculptoreanu, A., Rotman, E., Takahashi, M., Scheuer, T., and Catterall, W. A. (1993) Voltage-dependent potentiation of the activity of cardiac L-type calcium channel alpha 1 subunits due to phosphorylation by cAMP-dependent protein kinase, Proc. Natl. Acad. Sci. U.S.A. 90, 10135-10139.
25. Bunemann, M., Gerhardstein, B. L., Gao, T., and Hosey, M. M. (1999) Functional regulation of L-type calcium channels via protein kinase A-mediated phosphorylation of the beta(2) subunit, J. Biol. Chem. 274, 33851-33854.
26. Davare, M. A., Dong, F., Rubin, C. S., and Hell, J. W. (1999) The A-kinase anchor protein MAP2B and cAMP-dependent protein kinase are associated with class C L-type calcium channels in neurons, J. Biol. Chem. 274, 30280-30287.
27. Davare, M. A., and Hell, J. W. (2003) Increased phosphorylation of the neuronal L-type Ca(2+) channel Ca(v)1.2 during aging, Proc. Natl. Acad. Sci. U.S.A. 100, 16018-16023.
28. v1.2) and antagonizes channel phosphorylation by cAMP-dependent protein kinase, J. Biol. Chem. 275, 39710-39717.
29. Hell, J. W., Yokoyama, C. T., Breeze, L. J., Chavkin, C., and Catterall, W. A. (1995) Phosphorylation of presynaptic and postsynaptic calcium channels by cAMP-dependent protein kinase in hippocampal neurons, EMBO J. 14, 3036-3044.
30. 2+ channels requires membrane targeting of PKA and phosphorylation of channel subunits, Neuron 19, 185-196.
31. Hell, J. W., Westenbroek, R. E., Breeze, L. J., Wang, K. K. W., Chavkin, C., and Catterall, W. A. (1996) N-methyl-D-aspartate receptor-induced proteolytic conversion of postsynaptic class C L-type calcium channels in hippocampal neurons, Proc. Natl. Acad. Sci. U.S.A. 93, 3362-3367.
32. Hell, J. W., Westenbroek, R. E., Elliott, E. M., and Catterall, W. A. (1994) Differential phosphorylation, localization, and function of distinct α1 subunits of neuronal calcium channels. Two size forms for class B, C, and D α1 subunits with different COOH-termini, Ann. N.Y. Acad. Sci. 747, 282-293.
33. 2+ channel activity by deletions at the carboxyl terminus of the cardiac alpha 1 subunit, J. Biol. Chem. 269, 1635-1640.
34. Gray, P. C., Scott, J. D., and Catterall, W. A. (1998) Regulation of ion channels by cAMP-dependent protein kinase and A-kinase anchoring proteins, Curr. Opin. Neurobiol. 8, 330-334.
35. Rubin, C. S. (1994) A kinase anchor proteins and the intracellular targeting of signals carried by cyclic AMP, Biochim. Biophys. Acta 1224, 467-479.
36. Wong, W., and Scott, J. D. (2004) AKAP signalling complexes: focal points in space and time, Nat. Rev. Mol. Cell. Biol. 5, 959-970.
37. Hoshi, N., Langeberg, L. K., and Scott, J. D. (2005) Distinct enzyme combinations in AKAP signalling complexes permit functional diversity, Nat. Cell. Biol. 7, 1066-1073.
38. Rosenmund, C., Carr, D. W., Bergeson, S. E., Nilaver, G., Scott, J. D., and Westbrook, G. L. (1994) Anchoring of protein kinase A is required for modulation of AMPA/kainate receptors on hippocampal neurons, Nature 368, 853-856.
39. 2+ channels in skeletal muscle cells requires anchored cAMP-dependent protein kinase, Proc. Natl. Acad. Sci. U.S.A. 91, 11492-11496.
40. v1.2 channels via a leucine zipper interaction with A kinase-anchoring protein 15, Proc. Natl. Acad. Sci. U.S.A. 100, 13093-13098.
41. Vallee, R. B., DiBartolomeis, M. J., and Theurkauf, W. E. (1981) A protein kinase bound to the projection portion of MAP 2 (microtubule-associated protein 2), J Cell Biol. 90, 568-576.
42. Fraser, I. D. C., Tavalin, S. J., Lester, L. B., Langeberg, L. K., Westphal, A. M., Dean, R. A., Marrion, N. V., and Scott, J. D. (1998) A novel lipid-anchored A-kinase anchoring protein facilitates cAMP-responsive membrane events, EMBO J. 17, 2261-2272.
43. Gray, P. C., Johnson, B. D., Westenbroek, R. E., Hays, L. G., Yates, J. R., III, Scheuer, T., Catterall, W. A., and Murphy, B. J. (1998) Primary structure and function of an A kinase anchoring protein associated with calcium channels, Neuron 20, 1017-1026.
44. Gomez, L. L., Alam, S., Smith, K. E., Horne, E., and Dell'Acqua, M. L. (2002) Regulation of A-kinase anchoring protein 79/150-cAMP-dependent protein kinase postsynaptic targeting by NMDA receptor activation of calcineurin and remodeling of dendritic actin, J. Neurosci. 22, 7027-7044.
45. Gorski, J. A., Gomez, L. L., Scott, J. D., and Dell'Acqua, M. L. (2005) Association of an A-kinase-anchoring protein signaling scaffold with cadherin adhesion molecules in neurons and epithelial cells, Mol. Biol. Cell 16, 3574-3590.
46. Colledge, M., Dean, R. A., Scott, G. K., Langeberg, L. K., Huganir, R. L., and Scott, J. D. (2000) Targeting of PKA to glutamate receptors through a MAGUK-AKAP complex, Neuron 27, 107-119.
47. Mammen, A. L., Kameyama, K., Roche, K. W., and Huganir, R. L. (1997) Phosphorylation of the α-amino-3-hydroxy-5-methylisoxazole-4-propionic acid receptor GluR1 subunit by calcium/ calmodulin-dependent kinase II, J. Biol. Chem. 272, 32528-32533.
48. Roche, K. W., O'Brien, R. J., Mammen, A. L., Bernhardt, J., and Huganir, R. L. (1996) Characterization of multiple phosphorylation sites on the AMPA receptor GluR1 subunit, Neuron 16, 1179-1188.
49. Tavalin, S. J., Colledge, M., Hell, J. W., Langeberg, L. K., Huganir, R. L., and Scott, J. D. (2002) Regulation of GluR1 by the A-kinase anchoring protein 79 (AKAP79) signaling complex shares properties with long-term depression, J. Neurosci. 22, 3044-3051.
50. v1.2, Science 293, 98-101.
51. Altier, C., Dubel, S. J., Barrere, C., Jarvis, S. E., Stotz, S. C., Spaetgens, R. L., Scott, J. D., Cornet, V., De Waard, M., Zamponi, G. W., Nargeot, J., and Bourinet, E. (2002) Trafficking of L-type calcium channels mediated by the postsynaptic scaffolding protein AKAP79, J. Biol. Chem. 277, 33598-33603.
52. Burton, K. A., Treash-Osio, B., Muller, C. H., Dunphy, E. L., and McKnight, G. S. (1999) Deletion of type IIalpha regulatory subunit delocalizes protein kinase A in mouse sperm without affecting motility or fertilization, J. Biol. Chem. 274, 24131-24136.
53. Leonard, A. S., Davare, M. A., Horne, M. C., Garner, C. C., and Hell, J. W. (1998) SAP97 is associated with the α-amino-3-hydroxy-5- methylisoxazole-4-propionic acid receptor GluR1 subunit, J. Biol. Chem. 273, 19518-19524.
54. Liu, G., Shi, J., Yang, L., Cao, L., Park, S. M., Cui, J., and Marx, S. O. (2004) Assembly of a Ca(2+)-dependent BK channel signaling complex by binding to beta2 adrenergic receptor, EMBO J. 23, 2196-2205.
55. Nauert, J. B., Rigas, J. D., and Lester, L. B. (2003) Identification of an IQGAP1/AKAP79 complex in beta-cells, J. Cell. Biochem. 90, 97-108.
56. Ruehr, M. L., Russell, M. A., Ferguson, D. G., Bhat, M., Ma, J., Damron, D. S., Scott, J. D., and Bond, M. (2003) Targeting of protein kinase A by muscle A kinase-anchoring protein (mAKAP) regulates phosphorylation and function of the skeletal muscle ryanodine receptor, J Biol. Chem. 278, 24831-24836.
57. Schulze, D. H., Muqhal, M., Lederer, W. J., and Ruknudin, A. M. (2003) Sodium/calcium exchanger (NCX1) macromolecular complex, J. Biol. Chem. 278, 28849-28855.
58. v1.2 next to Ser1928, its main PKA site, is critical for Ser1928 dephosphorylation, Biochemistry 45, 3448-3459.
59. Snutch, T. P., Tomlinson, W. J., Leonard, J. P., and Gilbert, M. M. (1991) Distinct calcium channels are generated by alternative splicing and are differentially expressed in the mammalian CNS, Neuron 7, 45-57.
60. Li, Y., Ndubuka, C., and Rubin, C. S. (1996) A kinase anchor protein 75 targets regulatory (RII) subunits of cAMP-dependent protein kinase II to the cortical actin cytoskeleton in non-neuronal cells, J. Biol. Chem. 271, 16862-16869.
61. v1.2) subunit associate with and regulate L-type calcium channels containing C-terminal-truncated alpha 1C subunits, J. Biol. Chem. 276, 21089-21097.
62. Leonard, A. S., Lim, I. A., Hemsworth, D. E., Horne, M. C., and Hell, J. W. (1999) Calcium/calmodulin-dependent protein kinase II is associated with the N-methyl-D-aspartate receptor, Proc. Natl. Acad. Sci. U.S.A. 96, 3239-3244.
63. Li, Y., and Rubin, C. S. (1995) Mutagenesis of the regulatory subunit (RII beta) of cAMP-dependent protein kinase II beta reveals hydrophobic amino acids that are essential for RII beta dimerization and/or anchoring RII beta to the cytoskeleton, J. Biol. Chem. 270, 1935-1944.
64. Kapiloff, M. S., Schillace, R. V., Westphal, A. M., and Scott, J. D. (1999) mAKAP: an A-kinase anchoring protein targeted to the nuclear membrane of differentiated myocytes, J. Cell Sci. 112 (Part 16), 2725-2736.
65. Gray, P. C., Tibbs, V. C., Catterall, W. A., and Murphy, B. J. (1997) Identification of a 15-kDa cAMP-dependent protein kinase-anchoring protein associated with skeletal muscle L-type calcium channels, J. Biol. Chem. 272, 6297-6302.
66. Marx, S. O., Reiken, S., Hisamatsu, Y., Gaburjakova, M., Gaburjakova, J., Yang, Y. M., Rosemblit, N., and Marks, A. R. (2001) Phosphorylation-dependent regulation of ryanodine receptors: a novel role for leucine/isoleucine zippers, J. Cell Biol. 153, 699-708.
67. Martone, M. E., Alba, S. A., Edelman, V. M., Airey, J. A., and Ellisman, M. H. (1997) Distribution of inositol-1,4,5-trisphosphate and ryanodine receptors in rat neostriatum, Brain Res. 756, 9-21.
68. 2+ release channels in rat brain, J. Neurosci. 13, 3051-3063.
69. Emptage, N., Bliss, T. V., and Fine, A. (1999) Single synaptic events evoke NMDA receptor-mediated release of calcium from internal stores in hippocampal dendritic spines, Neuron 22, 115-124.
70. Raymond, C. R., and Redman, S. J. (2006) Spatial segregation of neuronal calcium signals encodes different forms of LTP in rat hippocampus, J. Physiol. 570, 97-111.
71. Chavis, P., Fagni, L., Lansman, J. B., and Bockaert, J. (1996) Functional coupling between ryanodine receptors and L-type calcium channels in neurons, Nature 382, 719-722.
72. Lin, J. W., Wyszynski, M., Madhavan, R., Sealock, R., Kim, J. U., and Sheng, M. (1998) Yotiao, a novel protein of neuromuscular junction and brain that interacts with specific splice variants of NMDA receptor subunit NR1, J. Neurosci. 18, 2017-2027.
73. Westphal, R. S., Tavalin, S. J., Lin, J. W., Alto, N. M., Fraser, I. D. C., Langeberg, L. K., Sheng, M., and Scott, J. D. (1999) Regulation of NMDA receptors by an associated phosphatase-kinase signaling complex, Science 285, 93-96.
74. Fraser, I. D., Cong, M., Kim, J., Rollins, E. N., Daaka, Y., Lefkowitz, R. J., and Scott, J. D. (2000) Assembly of an A kinase-anchoring protein-beta(2)-adrenergic receptor complex facilitates receptor phosphorylation and signaling, Curr. Biol. 10, 409-412.
75. Bauman, A. L., Soughayer, J., Nguyen, B. T., Willoughby, D., Carnegie, G. K., Wong, W., Hoshi, N., Langeberg, L. K., Cooper, D. M. F., Dessauer, C. W., and Scott, J. D. (2006) Dynamic regulation of cAMP synthesis through anchored PKA-adenylyl cyclase V/VI complexes, Mol. Cell 23, 925-931.
76. v1.2 calcium channels by c-Src and protein kinase A pathways, J. Biol. Chem. 281, 14015-14025.
77. 2+ channels in cardiac myocytes requires the distal carboxyl terminus of {alpha}1C but not serine 1928, Circ. Res. 98, e11-18.
78. 2+ channel currents but not for the negative shift of activation, FEBS Lett. 489, 87-91.
79. 2+ channel activation, J. Biol. Chem. 274, 12383-12390.
80. 2+ channels: Role in channel function, Trends Neurosci. 21, 148-154.
81. 2+ channel function?, Trends Pharmacol. Sci. 26, 427-436.
82. Yang, J., Drazba, J. A., Ferguson, D. G., and Bond, M. (1998) A-kinase anchoring protein 100 (AKAP100) is localized in multiple subcellular compartments in the adult rat heart, J. Cell Biol. 142, 511-522.
83. Vigil, D., Blumenthal, D. K., Brown, S., Taylor, S. S., and Trewhella, J. (2004) Differential effects of substrate on type I and type II PKA holoenzyme dissociation, Biochemistry 43, 5629-5636.
84. Yang, S., Fletcher, W. H., and Johnson, D. A. (1995) Regulation of cAMP-dependent protein kinase: enzyme activation without dissociation, Biochemistry 6267-6271.
85. Kindler, S., Schulz, B., Goedert, M., and Garner, C. C. (1990) Molecular structure of microtubule-associated protein 2b and 2c from rat brain, J. Biol. Chem. 265, 19679-19684.
86. 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.
87. 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.
88. 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.
89. Lewis, S. A., Wang, D. H., and Cowan, N. J. (1988) Microtubule-associated protein MAP2 shares a microtubule binding motif with tau protein, Science 242, 936-939.