Gravin dynamics regulates the subcellular distribution of PKA

Experimental Cell Research

Volumn 315, Issue 7, 2009, Pages 1247-1259

  Yan, Xiaohong ^a   Walkiewicz, Magdalena ^a   Carlson, Jennifer ^a   Leiphon, Laura ^a   Grove, Bryon ^a  

^a UNIVERSITY OF NORTH DAKOTA SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

Author keywords

AKAP12; Confocal microscopy; Fluorescent proteins; Gravin; PKA; PKC

Indexed keywords

AMINO ACID; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP DEPENDENT PROTEIN KINASE ANCHORING PROTEIN; GRAVIN PROTEIN; GREEN FLUORESCENT PROTEIN; PHORBOL ESTER; PROTEIN KINASE C; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CELL MEMBRANE; CELL TYPE; CELL VACUOLE; CELLULAR DISTRIBUTION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN CELL; MOLECULAR DYNAMICS; MUTANT; MYRISTYLATION; PRIORITY JOURNAL; PROTEIN TARGETING; QUANTITATIVE ANALYSIS;

RATTUS;

A KINASE ANCHOR PROTEINS; ANIMALS; CELL CYCLE PROTEINS; CELL LINE, TUMOR; CELL MEMBRANE; CYCLIC AMP-DEPENDENT PROTEIN KINASES; ENZYME ACTIVATION; HUMANS; PROTEIN KINASE C; RECOMBINANT FUSION PROTEINS; SUBCELLULAR FRACTIONS;

EID: 63049128289     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2008.12.026     Document Type: Article

References (45)

1. Fraser I.D., Tavalin S.J., Lester L.B., Langeberg L.K., Westphal A.M., Dean R.A., Marrion N.V., and Scott J.D. A novel lipid-anchored A-kinase anchoring protein facilitates cAMP-responsive membrane events. EMBO J. 17 (1998) 2261-2272
2. Dell'Acqua M.L., Faux M.C., Thorburn J., Thorburn A., and Scott J.D. Membrane-targeting sequences on AKAP79 bind phosphatidylinositol-4, 5-bisphosphate. EMBO J. 17 (1998) 2246-2260
3. Westphal R.S., Soderling S.H., Alto N.M., Langeberg L.K., and Scott J.D. Scar/WAVE-1, a Wiskott-Aldrich syndrome protein, assembles an actin-associated multi-kinase scaffold. EMBO J. 19 (2000) 4589-4600
4. Affaitati A., Cardone L., de Cristofaro T., Carlucci A., Ginsberg M.D., Varrone S., Gottesman M.E., Avvedimento E.V., and Feliciello A. Essential role of A-kinase anchor protein 121 for cAMP signaling to mitochondria. J. Biol. Chem. 278 (2003) 4286-4294
5. Cardone L., de Cristofaro T., Affaitati A., Garbi C., Ginsberg M.D., Saviano M., Varrone S., Rubin C.S., Gottesman M.E., Avvedimento E.V., and Feliciello A. A-kinase anchor protein 84/121 are targeted to mitochondria and mitotic spindles by overlapping amino-terminal motifs. J. Mol. Biol. 320 (2002) 663-675
6. Kapiloff M.S., Schillace R.V., Westphal A.M., and Scott J.D. mAKAP: an A-kinase anchoring protein targeted to the nuclear membrane of differentiated myocytes. J. Cell Sci. 112 Pt 16 (1999) 2725-2736
7. Wong W., and Scott J.D. AKAP signalling complexes: focal points in space and time. Nat. Rev., Mol. Cell Biol. 5 (2004) 959-970
8. Gordon T., Grove B., Loftus J.C., O'Toole T., McMillan R., Lindstrom J., and Ginsberg M.H. Molecular cloning and preliminary characterization of a novel cytoplasmic antigen recognized by myasthenia gravis sera. J. Clin. Invest. 90 (1992) 992-999
9. Nauert J.B., Klauck T.M., Langeberg L.K., and Scott J.D. Gravin, an autoantigen recognized by serum from myasthenia gravis patients, is a kinase scaffold protein. Curr. Biol. 7 (1996) 52-62
10. Grove B.D., and Bruchey A.K. Intracellular distribution of gravin, a PKA and PKC binding protein, in vascular endothelial cells. J. Vasc. Res. 38 (2001) 163-175
11. Piontek J., and Brandt R. Differential and regulated binding of cAMP-dependent protein kinase and protein kinase C isoenzymes to gravin in human model neurons: evidence that gravin provides a dynamic platform for the localization for kinases during neuronal development. J. Biol. Chem. 278 (2003) 38970-38979
12. Fan G., Shumay E., Wang H., and Malbon C.C. The scaffold protein gravin (cAMP-dependent protein kinase-anchoring protein 250) binds the β 2-adrenergic receptor via the receptor cytoplasmic Arg-329 to Leu-413 domain and provides a mobile scaffold during desensitization. J. Biol. Chem. 276 (2001) 24005-24014
13. 2-adrenergic receptor desensitization and resensitization. J. Biol. Chem. 275 (2000) 19025-19034
14. Shih M., Lin F., Scott J.D., Wang H.Y., and Malbon C.C. Dynamic complexes of β2-adrenergic receptors with protein kinases and phosphatases and the role of gravin. J. Biol. Chem. 274 (1999) 1588-1595
15. Tao J., Wang H.Y., and Malbon C.C. Protein kinase A regulates AKAP250 (gravin) scaffold binding to the β2-adrenergic receptor. EMBO J. 22 (2003) 6419-6429
16. Willoughby D., Wong W., Schaack J., Scott J.D., and Cooper D.M. An anchored PKA and PDE4 complex regulates subplasmalemmal cAMP dynamics. EMBO J. 25 (2006) 2051-2061
17. Tao J., Shumay E., McLaughlin S., Wang H.Y., and Malbon C.C. Regulation of AKAP-membrane interactions by calcium. J. Biol. Chem. 281 (2006) 23932-23944
18. Lin X., and Gelman I.H. Calmodulin and cyclin D anchoring sites on the Src-suppressed C kinase substrate, SSeCKS. Biochem. Biophys. Res. Commun. 290 (2002) 1368-1375
19. Lin X., Nelson P., and Gelman I.H. SSeCKS, a major protein kinase C substrate with tumor suppressor activity, regulates G1 → S progression by controlling the expression and cellular compartmentalization of cyclin D. Mol. Cell Biol. 20 (2000) 7259-7272
20. Gelman I.H. The role of SSeCKS/gravin/AKAP12 scaffolding proteins in the spaciotemporal control of signaling pathways in oncogenesis and development. Front. Biosci. 7 (2002) d1782-d1797
21. Gelman I.H., Lee K., Tombler E., Gordon R., and Lin X. Control of cytoskeletal architecture by the src-suppressed C kinase substrate, SSeCKS. Cell Motil. Cytoskelet. 41 (1998) 1-17
22. Gelman I.H., Tombler E., and Vargas Jr. J. A role for SSeCKS, a major protein kinase C substrate with tumour suppressor activity, in cytoskeletal architecture, formation of migratory processes, and cell migration during embryogenesis. Histochem. J. 32 (2000) 13-26
23. Nelson P.J., Moissoglu K., Vargas Jr. J., Klotman P.E., and Gelman I.H. Involvement of the protein kinase C substrate, SSeCKS, in the actin-based stellate morphology of mesangial cells. J. Cell Sci. 112 (1999) 361-370
24. Su B., Zheng Q., Vaughan M.M., Bu Y., and Gelman I.H. SSeCKS metastasis-suppressing activity in MatLyLu prostate cancer cells correlates with vascular endothelial growth factor inhibition. Cancer Res. 66 (2006) 5599-5607
25. Xia W., Unger P., Miller L., Nelson J., and Gelman I.H. The Src-suppressed C kinase substrate, SSeCKS, is a potential metastasis inhibitor in prostate cancer. Cancer Res. 61 (2001) 5644-5651
26. Weiser D.C., Julien K.R., Lang J.S., and Kimelman D. Cell shape regulation by gravin requires N-terminal membrane effector domains. Biochem. Biophys. Res. Commun. 375 (2008) 512-516
27. Lee S.W., Kim W.J., Choi Y.K., Song H.S., Son M.J., Gelman I.H., Kim Y.J., and Kim K.W. SSeCKS regulates angiogenesis and tight junction formation in blood-brain barrier. Nat. Med. 9 (2003) 900-906
28. Towbin H., Staehelin T., and Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets; procedure and some applications. Proc. Natl. Acad. Sci. U. S. A. 76 (1979) 4350-4354
29. Grove B., Bowditch R., Gordon T., del Zoppo G., and Ginsberg M. Restricted endothelial cell expression of gravin in vivo. Anat. Rec. 239 (1994) 231-242
30. Lin X., Tombler E., Nelson P.J., Ross M., and Gelman I.H. A novel src- and ras-suppressed protein kinase C substrate associated with cytoskeletal architecture. J. Biol. Chem. 271 (1996) 28430-28438
31. Wassler M.J., Foote C.I., Gelman I.H., and Shur B.D. Functional interaction between the SSeCKS scaffolding protein and the cytoplasmic domain of β1,4-galactosyltransferase. J. Cell. Sci. 114 (2001) 2291-2300
32. Streb J.W., Kitchen C.M., Gelman I.H., and Miano J.M. Multiple promoters direct expression of three AKAP12 isoforms with distinct subcellular and tissue distribution profiles. J. Biol. Chem. 279 (2004) 56014-56023
33. Arbuzova A., Schmitz A.A., and Vergeres G. Cross-talk unfolded: MARCKS proteins. Biochem. J. 362 (2002) 1-12
34. Gambhir A., Hangyas-Mihalyne G., Zaitseva I., Cafiso D.S., Wang J., Murray D., Pentyala S.N., Smith S.O., and McLaughlin S. Electrostatic sequestration of PIP2 on phospholipid membranes by basic/aromatic regions of proteins. Biophys. J. 86 (2004) 2188-2207
35. McLaughlin S., and Aderem A. The myristoyl-electrostatic switch: a modulator of reversible protein-membrane interactions. Trends Biochem. Sci. 20 (1995) 272-276
36. Seykora J.T., Myat M.M., Allen L.A., Ravetch J.V., and Aderem A. Molecular determinants of the myristoyl-electrostatic switch of MARCKS. J. Biol. Chem. 271 (1996) 18797-18802
37. Selvakumar P., Lakshmikuttyamma A., Shrivastav A., Das S.B., Dimmock J.R., and Sharma R.K. Potential role of N-myristoyltransferase in cancer. Prog. Lipid Res. 46 (2007) 1-36
38. Resh M.D. Fatty acylation of proteins: new insights into membrane targeting of myristoylated and palmitoylated proteins. Biochim. Biophys. Acta 1451 (1999) 1-16
39. Resh M.D. Membrane targeting of lipid modified signal transduction proteins. Sub-cell. Biochem. 37 (2004) 217-232
40. Burgoyne R.D. The neuronal calcium-sensor proteins. Biochim. Biophys. Acta 1742 (2004) 59-68
41. O'Callaghan D.W., and Burgoyne R.D. Role of myristoylation in the intracellular targeting of neuronal calcium sensor (NCS) proteins. Biochem. Soc. Trans. 31 (2003) 963-965
42. O'Callaghan D.W., Hasdemir B., Leighton M., and Burgoyne R.D. Residues within the myristoylation motif determine intracellular targeting of the neuronal Ca2+ sensor protein KChIP1 to post-ER transport vesicles and traffic of Kv4 K+ channels. J. Cell Sci. 116 (2003) 4833-4845
43. O'Callaghan D.W., Haynes L.P., and Burgoyne R.D. High-affinity interaction of the N-terminal myristoylation motif of the neuronal calcium sensor protein hippocalcin with phosphatidylinositol 4,5-bisphosphate. Biochem. J. 391 (2005) 231-238
44. O'Callaghan D.W., Ivings L., Weiss J.L., Ashby M.C., Tepikin A.V., and Burgoyne R.D. Differential use of myristoyl groups on neuronal calcium sensor proteins as a determinant of spatio-temporal aspects of Ca2+ signal transduction. J. Biol. Chem. 277 (2002) 14227-14237
45. Streb J.W., and Miano J.M. Cross-species sequence analysis reveals multiple charged residue-rich domains that regulate nuclear/cytoplasmic partitioning and membrane localization of A kinase anchoring protein 12 (SSeCKS/gravin). J. Biol. Chem. 280 (2005) 28007-28014