Phosphorylation and dephosphorylation of calsequestrin on CK2-sensitive sites in heart

Molecular and Cellular Biochemistry

Volumn 266, Issue 1-2, 2004, Pages 209-217

  Ram, Michal L ^a   Kiarash, Arash ^a   Marsh, James D ^a   Cala, Steven E ^a  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Calsequestrin; CK2; Glycosylation; Phosphorylation; Reticulum

Indexed keywords

CALSEQUESTRIN; CASEIN KINASE II; MANNOSE; PHOSPHATE; PHOSPHOPROTEIN PHOSPHATASE; PHOSPHORUS 32; SERINE;

ADENOVIRUS; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL COMPARTMENTALIZATION; CELL FREE SYSTEM; CELL LABELING; CELL PERMEABILIZATION; CLUSTER ANALYSIS; CONCENTRATION RESPONSE; CONTROLLED STUDY; DOG; ENZYME ACTIVITY; GENE OVEREXPRESSION; HEART MUSCLE CELL; INTRACELLULAR TRANSPORT; MASS SPECTROMETRY; MEMBRANE VESICLE; MICROSOME; NONHUMAN; PROTEIN DEPHOSPHORYLATION; PROTEIN METABOLISM; PROTEIN PHOSPHORYLATION; PROTEIN PURIFICATION; RAT; REACTION ANALYSIS; SENSITIVITY ANALYSIS;

ADENOVIRIDAE; ANIMALS; CALCIUM; CALSEQUESTRIN; CASEIN KINASE II; DOGS; GLYCOSYLATION; MYOCARDIUM; MYOCYTES, CARDIAC; PHOSPHATES; PHOSPHOPROTEIN PHOSPHATASE; PHOSPHORYLATION; RATS; RATS, SPRAGUE-DAWLEY; SARCOPLASMIC RETICULUM;

EID: 9444263762     PISSN: 03008177     EISSN: None     Source Type: Journal    
DOI: 10.1023/B:MCBI.0000049164.28580.56     Document Type: Article

References (56)

1. MacLennan DH, Wong PT: Isolation of a calcium-sequestering protein from sarcoplasmic reticulum. Proc Natl Acad Sci USA 68: 1231-1235, 1971
2. Ikemoto N, Bhatnager GM, Gergely J: Fractionation of solubilized sarcoplasmic reticulum. Biochem Biophys Res Commun 44: 1510-1517, 1971
3. Campbell KP, MacLennan DH, Jorgensen AO, Mintzer MC: Purification and characterization of calsequestrin from canine cardiac sarcoplasmic reticulum and identification of the 53,000 dalton glycoprotein. J Biol Chem 258: 1197-1204, 1983
4. Scott BT, Simmerman HK, Collins JH, Nadal-Ginard B, Jones LR: Complete amino acid sequence of canine cardiac calsequestrin deduced by cDNA cloning. J Biol Chem 263: 8958-8964, 1988
5. Jones LR, Cala SE: Biochemical evidence for functional heterogeneity of cardiac sarcoplasmic reticulum vesicles. J Biol Chem 256: 11809-11818, 1981
6. Jorgensen AO, Shen AC, Campbell KP: Ultrastructural localization of calsequestrin in adult rat atrial and ventricular muscle cells. J Cell Biol 101: 257-268, 1985
7. Terentyev D, Viatchenko-Karpinski S, Gyorke I, Volpe P, Williams SC, Gyorke S: Calsequestrin determines the functional size and stability of cardiac intracellular calcium stores: Mechanism for hereditary arrhythmia. Proc Natl Acad Sci USA 100: 11759-11764, 2003
8. Jones LR, Zhang L, Sanborn K, Jorgensen AO, Kelley J: Purification, primary structure, and immunological characterization of the 26-kDa calsequestrin binding protein (junctin) from cardiac junctional sarcoplasmic reticulum. J Biol Chem 270: 30787-30796, 1995
9. Guo W, Jorgensen AO, Jones LR, Campbell KP: Biochemical characterization and molecular cloning of cardiac triadin. J Biol Chem 271: 458-465, 1996
10. Kobayashi YM, Jones LR: Identification of triadin 1 as the predominant triadin isoform expressed in mammalian myocardium. J Biol Chem 274: 28660-28668, 1999
11. Cala SE, Jones LR: Phosphorylation of cardiac and skeletal muscle calsequestrin isoforms by casein kinase II. Demonstration of a cluster of unique rapidly phosphorylated sites in cardiac calsequestrin. J Biol Chem 266: 391-398, 1991
12. O'Brian JJ, Ram ML, Kiarash A, Cala SE: Mass spectrometry of cardiac calsequestrin characterizes microheterogeneity unique to heart and indicative of complex intracellular transit. J Biol Chem 277: 37154-37160, 2002
13. Ellingsen O, Davidoff AJ, Prasad SK, Berger HJ, Springhorn JP, Marsh JD, Kelly RA, Smith TW: Adult rat ventricular myocytes cultured in defined medium: Phenotype and electromechanical function. Am J Physiol 265: H747-H754, 1993
14. Gintant GA: Regional differences in IK density in canine left ventricle: Role of IK's in electrical heterogeneity. Am J Physiol 268: H604-H613, 1995
15. Laemmli UK: Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685, 1970
16. Cala SE, Miles K: Phosphorylation of the cardiac isoform of calsequestrin in cultured rat myotubes and rat skeletal muscle. Biochim Biophys Acta 1118: 277-287, 1992
17. Burnette WN: "Western blotting": Electrophoretic transfer of proteins from sodium dodecyl sulfate-polyacrylamide gels to unmodified nitrocellulose and radiographic detection with antibody and radioiodinated protein A. Anal Biochem 112: 195-203, 1981
18. Lowry HO, Rosebrough NJ, Farr AL, Randall RJ: Protein measurements with folin phenol reagent. J Biol Chem 193: 265-275, 1951
19. Milan AM, Waddington RJ, Embery G: Fluoride alters casein kinase II and alkaline phosphatase activity in vitro with potential implications for dentine mineralization. Arch Oral Biol 46: 343-351, 2001
20. Fujiki Y, Hubbard AL, Fowler S, Lazarow PB: Isolation of intracellular membranes by means of sodium carbonate treatment: Application to endoplasmic reticulum. J Cell Biol 93: 97-102, 1982
21. Howell KE, Palade GE: Hepatic Golgi fractions resolved into membrane and content subfractions. J Cell Biol 92: 822-832, 1982
22. 2+-dependent elution from phenyl-sepharose. J Biol Chem 258: 11932-11936, 1983
23. Helenius A, Aebi M: Intracellular functions of N-linked glycans. Science 291: 2364-2369, 2001
24. Parodi AJ: Role of N-oligosaccharide endoplasmic reticulum processing reactions in glycoprotein folding and degradation. Biochem J 348: 1-13, 2000
25. Martina JA, Daniotti JL, Maccioni HJ: Influence of N glycosylation and N-glycan trimming on the activity and intracellular traffic of GD3 synthase. J Biol Chem 273: 3725-3731, 1998
26. Herscovics A: Importance of glycosidases in mammalian glycoprotein biosynthesis. Biochim Biophys Acta 1473: 96-107, 1999
27. Moremen KW: Golgi alpha-mannosidase II deficiency in vertebrate systems: Implications for asparagine-linked oligosaccharide processing in mammals. Biochim Biophys Acta 1573: 225-235, 2002
28. Dutta K, Carmody MW, Cala SE, Davidoff AJ: Depressed PKA activity contributes to impaired SERCA function and is linked to the pathogenesis of glucose-induced cardiomyopathy. J Mol Cell Cardiol 34: 985-996, 2002
29. Allende JE, Allende CC: Protein kinases. 4. Protein kinase CK2: An enzyme with multiple substrates and a puzzling regulation. EASEB J 9: 313-323, 1995
30. Mauxion F, Le Borgne R, Munier-Lehmann H, Hoflack B: A casein kinase II phosphorylation site in the cytoplasmic domain of the cation-dependent mannose 6-phosphate receptor determines the high affinity interaction of the AP-1 Golgi assembly proteins with membranes. J Biol Chem 271: 2171-2178, 1996
31. Honing S, Griffith J, Geuze HJ, Hunziker W: The tyrosine-based lysosomal targeting signal in lamp-1 mediates sorting into Golgi-derived clathrin-coated vesicles. EMBO J 15: 5230-5239, 1996
32. Petersen CM, Nielsen MS, Nykjaer A, Jacobsen L, Tommerup N, Rasmussen HH, Roigaard H, Gliemann J, Madsen P, Moestrup SK: Molecular identification of a novel candidate sorting receptor purified from human brain by receptor-associated protein affinity chromatography. J Biol Chem 272: 3599-3605, 1997
33. Alconada A, Bauer U, Hoflack B: A tyrosine-based motif and a casein kinase II phosphorylation site regulate the intracellular trafficking of the varicella-zoster virus glycoprotein I, a protein localized in the trans-Golgi network. EMBO J 15: 6096-6110, 1996
34. Wan L, Molloy SS, Thomas L, Liu G, Xiang Y, Rybak SL, Thomas G: PACS-1 defines a novel gene family of cytosolic sorting proteins required for trans-Golgi network localization. Cell 94: 205-216, 1998
35. Schubert U, Henklein P, Boldyreff B, Wingender E, Strebel K, Porstmann T: The human immunodeficiency virus type 1 encoded Vpu protein is phosphorylated by casein kinase-2 (CK-2) at positions Ser52 and Ser56 within a predicted alpha-helix-turn-alpha-helix-motif. J Mol Biol 236: 16-25, 1994
36. Waites CL, Mehta A, Tan PK, Thomas G, Edwards RH, Krantz DE: An acidic motif retains vesicular monoamine transporter 2 on large dense core vesicles. J Cell Biol 152: 1159-1168, 2001
37. 2+-adenosine triphosphatase on membrane-bound polyribosomes. Can J Biochem 56: 452-456, 1978
38. 2+-adenosine triphosphatase and calsequestrin. J Biol Chem 255: 11839-11846, 1980
39. Hiegel L, Ohnishi M, Carpenter MR, Khanna VK, Reithmeier RA, MacLennan DH: Amino acid sequence of rabbit fast-twitch skeletal muscle calsequestrin deduced from cDNA and peptide sequencing. Proc Natl Acad Sci USA 84: 1167-1171, 1987
40. Veis A, Sfeir C, Wu CB: Phosphorylation of the proteins of the extracellular matrix of mineralized tissues by casein kinase-like activity. Crit Rev Oral Biol Med 8: 360-379, 1997
41. Sfeir C, Veis A: Casein kinase localization in the endoplasmic reticulum of the ROS 17/2.8 cell line. J Bone Miner Res 10: 607-615, 1995
42. May LT, Sehgal PB: Phosphorylation of interleukin-6 at serine54: An early event in the secretory pathway in human fibroblasts. Biochem Biophys Res Commun 185: 524-530, 1992
43. Fish KN, Soderberg-Naucler C, Nelson JA: Steady-state plasma membrane expression of human cytomegalovirus gB is determined by the phosphorylation state of Ser900. J Virol 72: 6657-6664, 1998
44. Bingham EW, Farrel HM, Jr.: Casein kinase from the Golgi apparatus of lactating mammary gland. J Biol Chem 249: 3647-3651, 1974
45. Lasa M, Marin O, Pinna LA: Rat liver Golgi apparatus contains a protein kinase similar to the casein kinase of lactating mammary gland. Eur J Biochem 243: 719-725, 1997
46. Lasa M, Chang PL, Prince CW, Pinna LA: Phosphorylation of osteopontin by Golgi apparatus casein kinase. Biochem Biophys Res Commun 240: 602-605, 1997
47. Pasqualini E, Caillol N, Valette A, Lloubes R, Verine A, Lombardo D: Phosphorylation of the rat pancreatic bile-salt-dependent lipase by casein kinase II is essential for secretion. Biochem J 345: 121-128, 2000
48. Swift LL: Role of the Golgi apparatus in the phosphorylation of apolipoprotein B. J Biol Chem 271: 31491-31495, 1996
49. Ma J, Simonovic M, Qian R, Colley KJ: Sialyltransferase isoforms are phosphorylated in the cis-medial Golgi on serine and threonine residues in their luminal sequences. J Biol Chem 274: 8046-8052, 1999
50. Meggio F, Boulton AP, Marchiori F, Borin G, Lennon DP, Calderan A, Pinna LA: Substrate-specificity determinants for a membrane-bound casein kinase of lactating mammary gland. A study with synthetic peptides. Eur J Biochem 177: 281-284, 1988
51. Meggio F, Marin O, Pinna LA: Substrate specificity of protein kinase CK2. Cell Mol Biol Res 40: 401-409, 1994
52. Munro S, Pelham HR: A C-terminal signal prevents secretion of luminal ER proteins. Cell 48: 899-907, 1987
53. Semenza JC, Hardwick KG, Dean N, Pelham HR: ERD2, a yeast gene required for the receptor-mediated retrieval of luminal ER proteins from the secretory pathway. Cell 61: 1349-1357, 1990
54. Cala SE, Jones LR: GRP94 resides within cardiac sarcoplasmic reticulum vesicles and is phosphorylated by casein kinase II. J Biol Chem 269: 5926-5931, 1994
55. Terentyev D, Viatchenko-Karpinski S, Gyorke I, Volpe P, Williams SC, Gyorke S: Calsequestrin determines the functional size and stability of cardiac intracellular calcium stores: Mechanism for hereditary arrhythmia. Proc Natl Acad Sci USA 100: 11759-11764, 2003
56. Kiarash A, Kelly C, Phinney B, Valdivia H, Abrams J, Cala S: Defective glycosylation of calsequestrin in heart failure. Cardiovasc Res 63: 264-272, 2004