Interaction of α1-syntrophin with multiple isoforms of heterotrimeric G protein α subunits

FEBS Journal

Volumn 275, Issue 1, 2008, Pages 22-33

  Okumura, Akiko ^a   Nagai, Katsuya ^a   Okumura, Nobuaki ^a  

^a OSAKA UNIVERSITY   (Japan)

Author keywords

1 syntrophin; Dystrophin glycoprotein; G protein; Neuronal nitric oxide synthase; pH domain

Indexed keywords

ALPHA1 SYNTOPHIN; CYCLIC AMP; DYSTROBREVIN; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; HETEROTRIMERIC GUANINE NUCLEOTIDE BINDING PROTEIN; NEURONAL NITRIC OXIDE SYNTHASE; SYNTROPHIN; UNCLASSIFIED DRUG; CALCIUM BINDING PROTEIN; ISOPROTEIN; MEMBRANE PROTEIN; MUSCLE PROTEIN; SYNTROPHIN ALPHA1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; DOWN REGULATION; MASS SPECTROMETRY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; ANIMAL; BINDING SITE; CELL STRAIN COS1; CERCOPITHECUS; GENETICS; MALE; METABOLISM; RAT; RNA INTERFERENCE; WISTAR RAT;

ANIMALS; BINDING SITES; CALCIUM-BINDING PROTEINS; CERCOPITHECUS AETHIOPS; COS CELLS; DOWN-REGULATION; GTP-BINDING PROTEIN ALPHA SUBUNITS; MALE; MASS SPECTROMETRY; MEMBRANE PROTEINS; MICE; MUSCLE PROTEINS; PROTEIN ISOFORMS; RATS; RATS, WISTAR; RNA INTERFERENCE;

EID: 37349007254     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2007.06174.x     Document Type: Article

References (56)

1. Froehner SC (1984) Peripheral proteins of postsynaptic membranes from Torpedo electric organ identified with monoclonal antibodies. J Cell Biol 99, 88 96.
2. -associated protein, differ in primary structure and tissue distribution. Neuron 11, 531 540.
3. Ahn AH, Yoshida M, Anderson MS, Feener CA, Selig S, Hagiwara Y, Ozawa E Kunkel LM (1994) Cloning of human basic A1, a distinct 59-kDa dystrophin-associated protein encoded on chromosome 8q23-24. Proc Natl Acad Sci USA 91, 4446 4450.
4. Yang B, Ibraghimov-Beskrovnaya O, Moomaw CR, Slaughter CA Campbell KP (1994) Heterogeneity of the 59-kDa dystrophin-associated protein revealed by cDNA cloning and expression. J Biol Chem 269, 6040 6044.
5. Adams ME, Dwyer TM, Dowler LL, White RA Froehner SC (1995) Mouse alpha 1- and beta 2-syntrophin gene structure, chromosome localization, and homology with a discs large domain. J Biol Chem 270, 25859 25865.
6. Ahn AH, Freener CA, Gussoni E, Yoshida M, Ozawa E Kunkel LM (1996) The three human syntrophin genes are expressed in diverse tissues, have distinct chromosomal locations, and each bind to dystrophin and its relatives. J Biol Chem 271, 2724 2730.
7. Piluso G, Mirabella M, Ricci E, Belsito A, Abbondanza C, Servidei S, Puca AA, Tonali P, Puca GA Nigro V (2000) Gamma1- and gamma2-syntrophins, two novel dystrophin-binding proteins localized in neuronal cells. J Biol Chem 275, 15851 15860.
8. Dalkilic I Kunkel LM (2003) Muscular dystrophies: genes to pathogenesis. Curr Opin Genet Dev 13, 231 238.
9. Banks GB, Fuhrer C, Adams ME Froehner SC (2003) The postsynaptic submembrane machinery at the neuromuscular junction: requirement for rapsyn and the utrophin/dystrophin-associated complex. J Neurocytol 32, 709 726.
10. Campbell KP Kahl SD (1989) Association of dystrophin and an integral membrane glycoprotein. Nature 338, 259 262.
11. Yoshida M Ozawa E (1990) Glycoprotein complex anchoring dystrophin to sarcolemma. J Biochem (Tokyo) 108, 748 752.
12. Kramarcy NR, Vidal A, Froehner SC Sealock R (1994) Association of utrophin and multiple dystrophin short forms with the mammalian M(r) 58,000 dystrophin-associated protein (syntrophin). J Biol Chem 269, 2870 2876.
13. Ahn AH Kunkel LM (1995) Syntrophin binds to an alternatively spliced exon of dystrophin. J Cell Biol 128, 363 371.
14. Yang B, Jung D, Rafael JA, Chamberlain JS Campbell KP (1995) Identification of alpha-syntrophin binding to syntrophin triplet, dystrophin, and utrophin. J Biol Chem 270, 4975 4978.
15. Kachinsky AM, Froehner SC Milgram SL (1999) A PDZ-containing scaffold related to the dystrophin complex at the basolateral membrane of epithelial cells. J Cell Biol 145, 391 402.
16. Lidov HG, Byers TJ, Watkins SC Kunkel LM (1990) Localization of dystrophin to postsynaptic regions of central nervous system cortical neurons. Nature 348, 725 728.
17. Claudepierre T, Dalloz C, Mornet D, Matsumura K, Sahel J Rendon A (2000) Characterization of the intermolecular associations of the dystrophin-associated glycoprotein complex in retinal Muller glial cells. J Cell Sci 113, 3409 3417.
18. Haenggi T Fritschy JM (2006) Role of dystrophin and utrophin for assembly and function of the dystrophin glycoprotein complex in non-muscle tissue. Cell Mol Life Sci 63, 1614 1631.
19. Blake DJ, Hawkes R, Benson MA Beesley PW (1999) Different dystrophin-like complexes are expressed in neurons and glia. J Cell Biol 147, 645 658.
20. Alessi A, Bragg AD, Percival JM, Yoo J, Albrecht DE, Froehner SC Adams ME (2006) Gamma-syntrophin scaffolding is spatially and functionally distinct from that of the alpha/beta syntrophins. Exp Cell Res 312, 3084 3095.
21. Connors NC, Adams ME, Froehner SC Kofuji P (2004) The potassium channel Kir4.1 associates with the dystrophin-glycoprotein complex via alpha-syntrophin in glia. J Biol Chem 279, 28387 28392.
22. Bragg AD, Amiry-Moghaddam M, Ottersen OP, Adams ME Froehner SC (2006) Assembly of a perivascular astrocyte protein scaffold at the mammalian blood-brain barrier is dependent on alpha-syntrophin. Glia 53, 879 890.
23. Puwarawuttipanit W, Bragg AD, Frydenlund DS, Mylonakou MN, Nagelhus EA, Peters MF, Kotchabhakdi N, Adams ME, Froehner SC Haug FM (2006) Differential effect of alpha-syntrophin knockout on aquaporin-4 and Kir4.1 expression in retinal macroglial cells in mice. Neuroscience 137, 165 175.
24. Blake DJ Kroger S (2000) The neurobiology of Duchenne muscular dystrophy: learning lessons from muscle? Trends Neurosci 23, 92 99.
25. Mehler MF (2000) Brain dystrophin, neurogenetics and mental retardation. Brain Res Rev 32, 277 307.
26. Anderson JL, Head SI, Rae C Morley JW (2002) Brain function in Duchenne muscular dystrophy. Brain 125, 4 13.
27. Schultz J, Hoffmuller U, Krause G, Ashurst J, Macias MJ, Schmieder P, Schneider-Mergener J Oschkinat H (1998) Specific interactions between the syntrophin PDZ domain and voltage-gated sodium channels. Nat Struct Biol 5, 19 24.
28. Gee SH, Madhavan R, Levinson SR, Caldwell JH, Sealock R Froehner SC (1998) Interaction of muscle and brain sodium channels with multiple members of the syntrophin family of dystrophin-associated proteins. J Neurosci 18, 128 137.
29. Leonoudakis D, Conti LR, Anderson S, Radeke CM, McGuire LM, Adams ME, Froehner SC, Yates JR III. Vandenberg CA (2004) Protein trafficking and anchoring complexes revealed by proteomic analysis of inward rectifier potassium channel (Kir2.x)-associated proteins. J Biol Chem 279, 22331 22346.
30. Vandebrouck A, Sabourin J, Rivet J, Balghi H, Sebille S, Kitzis A, Raymond G, Cognard C, Bourmeyster N Constantin B (2007) Regulation of capacitative calcium entries by alpha1-syntrophin: association of TRPC1 with dystrophin complex and the PDZ domain of alpha1-syntrophin. FASEB J 21, 608 617.
31. Neely JD, Amiry-Moghaddam M, Ottersen OP, Froehner SC, Agre P Adams ME. (2001) Syntrophin-dependent expression and localization of Aquaporin-4 water channel protein. Proc Natl Acad Sci USA 98, 14108 14113.
32. Hasegawa M, Cuenda A, Spillantini MG, Thomas GM, Buee-Scherrer V, Cohen P Goedert M (1999) Stress-activated protein kinase-3 interacts with the PDZ domain of alpha1-syntrophin. A mechanism for specific substrate recognition. J Biol Chem 274, 12626 12631.
33. Lumeng C, Phelps S, Crawford GE, Walden PD, Barald K Chamberlain JS (1999) Interactions between beta 2-syntrophin and a family of microtubule-associated serine/threonine kinases. Nat Neurosci 2, 611 617.
34. Hogan A, Shepherd L, Chabot J, Quenneville S, Prescott SM, Topham MK Gee SH (2001) Interaction of gamma 1-syntrophin with diacylglycerol kinase-zeta. Regulation of nuclear localization by PDZ interactions. J Biol Chem 276, 26526 26533.
35. Ou Y, Strege P, Miller SM, Makielski J, Ackerman M, Gibbons SJ Farrugia G (2003) Syntrophin gamma 2 regulates SCN5A gating by a PDZ domain-mediated interaction. J Biol Chem 278, 1915 1923.
36. Brenman JE, Chao DS, Gee SH, McGee AW, Craven SE, Santillano DR, Wu Z, Huang F, Xia H Peters MF (1996) Interaction of nitric oxide synthase with the postsynaptic density protein PSD-95 and alpha1-syntrophin mediated by PDZ domains. Cell 84, 757 767.
37. Hashida-Okumura A, Okumura N, Iwamatsu A, Buijs RM, Romijn HJ Nagai K (1999) Interaction of neuronal nitric-oxide synthase with alpha1-syntrophin in rat brain. J Biol Chem 274, 11736 11741.
38. Hashida-Okumura A, Nagai K, Okumura N Nakagawa H (1995) Activation of neuronal nitric oxide synthase by flavin adenine dinucleotide. Biochem Mol Biol Int 35, 1339 1348.
39. Hashida-Okumura A, Nagai K, Okumura N, Hibino H, Niijima A Nakagawa H (1995) Hypotensive effect of FAD and its mechanism: involvement of nitric oxide synthase activation. J Clin Biochem Nutr 18, 97 109.
40. Williams JC, Armesilla AL, Mohamed TM, Hagarty CL, McIntyre FH, Schomburg S, Zaki AO, Oceandy D, Cartwright EJ Buch MH (2006) The sarcolemmal calcium pump, alpha-1 syntrophin, and neuronal nitric-oxide synthase are parts of a macromolecular protein complex. J Biol Chem 281, 23341 23348.
41. Lemmon MA (2004) Pleckstrin homology domains: not just for phosphoinositides. Biochem Soc Trans 32, 707 711.
42. Rossman KL, Worthylake DK, Snyder JT, Siderovski DP, Campbell SL Sondek J (2002) A crystallographic view of interactions between Dbs and Cdc42: PH domain-assisted guanine nucleotide exchange. EMBO J 21, 1315 1326.
43. Lodowski DT, Pitcher JA, Capel WD, Lefkowitz RJ Tesmer JJ (2003) Keeping G proteins at bay: a complex between G protein-coupled receptor kinase 2 and Gbetagamma. Science 300, 1256 1262.
44. Russo C, Gao Y, Mancini P, Vanni C, Porotto M, Falasca M, Torrisi MR, Zheng Y Eva A (2001) Modulation of oncogenic DBL activity by phosphoinositol phosphate binding to pleckstrin homology domain. J Biol Chem 276, 19524 19531.
45. Joseph RE Norris FA (2005) Substrate specificity and recognition is conferred by the pleckstrin homology domain of the Dbl family guanine nucleotide exchange factor P-Rex2. J Biol Chem 280, 27508 27512.
46. Chockalingam PS, Gee SH Jarrett HW (1999) Pleckstrin homology domain of mouse alpha 1-syntrophin binds phosphatidylinositol 4,5-bisphosphate. Biochemistry 38, 5596 5602.
47. Iwata Y, Pan Y, Yoshida T, Hanada H Shigekawa M. (1998) Alpha1-syntrophin has distinct binding sites for actin and calmodulin. FEBS Lett 423, 173 177.
48. Zhou YW, Thomason DB, Gullberg D Jarrett HW (2006) Binding of laminin alpha1-chain LG4-5 domain to alpha-dystroglycan causes tyrosine phosphorylation of syntrophin to initiate Rac1 signaling. Biochem 45, 2042 2052.
49. Zhou YW, Oak SA, Senogles SE Jarrett HW (2005) Laminin-alpha1 globular domains 3 and 4 induce heterotrimeric G protein binding to alpha-syntrophin's PDZ domain and alter intracellular Ca2+ in muscle. Am J Physiol Cell Physiol 288, C377 C388.
50. Yakubchyk Y, Abramovici H, Maillet JC, Daher E, Obagi C, Parks RJ, Topham MK Gee SH (2005) Regulation of neurite outgrowth in N1E-115 cells through PDZ-mediated recruitment of diacylglycerol kinase zeta. Mol Cell Biol 25, 7289 7302.
51. Chen Z, Hague C, Hall RA Minneman KP (2006) Syntrophins regulate alpha1D-adrenergic receptors through a PDZ domain-mediated interaction. J Biol Chem 281, 12414 12420.
52. Froehner SC, Adams ME, Peters MF Gee SH (1997) Syntrophins: modular adapter proteins at the neuromuscular junction and the sarcolemma. Soc Gen Physiol Ser 52, 197 207.
53. Rossman KL Sondek J (2005) Larger than Dbl: new structural insights into RhoA activation. Trends Biochem Sci 30, 163 165.
54. Yan J, Wen W, Xu W, Long JF, Adams ME, Froehner SC Zhang M (2005) Structure of the split PH domain and distinct lipid-binding properties of the PH-PDZ supramodule of alpha-syntrophin. EMBO J 24, 3985 3995.
55. Hu RG, Sheng J, Qi X, Xu Z, Takahashi TT Varshavsky A (2005) The N-end rule pathway as a nitric oxide sensor controlling the levels of multiple regulators. Nature 437, 981 986.
56. Okumura N, Hashida-Okumura A, Kita K, Matsubae M, Matsubara T, Takao T Nagai K (2005) Proteomic analysis of slow- and fast-twitch skeletal muscles. Proteomics 5, 2896 2906.