Transitions of protein traffic from cardiac ER to junctional SR

Journal of Molecular and Cellular Cardiology

Volumn 81, Issue , 2015, Pages 34-45

  Sleiman, Naama H ^a   McFarland, Timothy P ^a   Jones, Larry R ^b   Cala, Steven E ^a  

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

^b INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Junctin; Junctional sarcoplasmic reticulum; Rough ER; Smooth ER; Triadin

Indexed keywords

JUNCTIN; MEMBRANE PROTEIN; TRIADIN; UNCLASSIFIED DRUG; CALCIUM BINDING PROTEIN; CARRIER PROTEIN; FLUORESCENT PROTEIN 583; HYBRID PROTEIN; MIXED FUNCTION OXIDASE; MUSCLE PROTEIN; PHOTOPROTEIN;

ADULT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CARDIAC ENDOPLASMIC RETICULUM; CELL LABELING; CELL NUCLEUS; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; FLUORESCENCE MICROSCOPY; HEART MUSCLE CELL; INTRACELLULAR TRANSPORT; JUNCTIONAL SARCOPLASMIC RETICULUM; MALE; MICROTUBULE; NONHUMAN; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN POLYMERIZATION; PROTEIN TARGETING; PROTEIN TRANSPORT; RAT; ROUGH ENDOPLASMIC RETICULUM; SARCOPLASMIC RETICULUM; SMOOTH ENDOPLASMIC RETICULUM; STEADY STATE; ANIMAL; CARDIAC MUSCLE; CARDIAC MUSCLE CELL; CLASSIFICATION; CYTOLOGY; DOG; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; REPORTER GENE; SIGNAL TRANSDUCTION; TRANSGENE; ULTRASTRUCTURE;

RATTUS;

ANIMALS; CALCIUM-BINDING PROTEINS; CARRIER PROTEINS; CELL NUCLEUS; DOGS; GENE EXPRESSION REGULATION; GENES, REPORTER; LUMINESCENT PROTEINS; MEMBRANE PROTEINS; MICROSCOPY, FLUORESCENCE; MICROTUBULES; MIXED FUNCTION OXYGENASES; MUSCLE PROTEINS; MYOCARDIUM; MYOCYTES, CARDIAC; PROTEIN TRANSPORT; RATS; RECOMBINANT FUSION PROTEINS; SARCOPLASMIC RETICULUM; SIGNAL TRANSDUCTION; TRANSGENES;

EID: 84922470894     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2014.12.025     Document Type: Article

References (62)

1. Sommer J.R., Jennings R.B. Ultrastructure of cardiac muscle. The heart and cardiovascular system 1986, 61-100. Raven Press, New York. H.A. Fozzard (Ed.).
2. Franzini-Armstrong C. Structure of sarcoplasmic reticulum. Fed Proc 1980, 39:2403-2409.
3. Fleischer S., Inui M. Biochemistry and biophysics of excitation-contraction coupling. Annu Rev Biophys Biophys Chem 1989, 18:333-364.
4. Bers D.M., Shannon T.R. Calcium movements inside the sarcoplasmic reticulum of cardiac myocytes. J Mol Cell Cardiol 2013, 58:59-66.
5. Cala S.E., Scott B.T., Jones L.R. Intralumenal sarcoplasmic reticulum Ca(2+)-binding proteins. Semin Cell Biol 1990, 1:265-275.
6. Franzini-Armstrong C. The sarcoplasmic reticulum and the control of muscle contraction. FASEB J 1999, 13(Suppl. 2):S266-S270.
7. Jorgensen A.O., Shen A.C., Campbell K.P. Ultrastructural localization of calsequestrin in adult rat atrial and ventricular muscle cells. J Cell Biol 1985, 101:257-268.
8. Ones L.R., Cala S.E. Biochemical evidence for functional heterogeneity of cardiac sarcoplasmic reticulum vesicles. J Biol Chem 1981, 256:11809-11818.
9. Diaz M.E., Graham H.K., O'Neill S.C., Trafford A.W., Eisner D.A. The control of sarcoplasmic reticulum Ca content in cardiac muscle. Cell Calcium 2005, 38:391-396.
10. Franzini-Armstrong C., Jorgensen A.O. Structure and development of E-C coupling units in skeletal muscle. Annu Rev Physiol 1994, 56:509-534.
11. 2+ release channels and their regulation by endogenous effectors. Annu Rev Physiol 1994, 56:485-508.
12. Campbell K.P., MacLennan D.H., Jorgensen A.O., Mintzer M.C. Purification and characterization of calsequestrin from canine cardiac sarcoplasmic reticulum and identification of the 53,000 dalton glycoprotein. J Biol Chem 1983, 258:1197-1204.
13. Guo W., Jorgensen A.O., Jones L.R., Campbell K.P. Biochemical characterization and molecular cloning of cardiac triadin. J Biol Chem 1996, 271:458-465.
14. Kobayashi Y.M., Jones L.R. Identification of triadin 1 as the predominant triadin isoform expressed in mammalian myocardium. J Biol Chem 1999, 274:28660-28668.
15. Kobayashi Y.M., Alseikhan B.A., Jones L.R. Localization and characterization of the calsequestrin-binding domain of triadin 1. Evidence for a charged beta-strand in mediating the protein-protein interaction. J Biol Chem 2000, 275:17639-17646.
16. Jones L.R., Zhang L., Sanborn K., Jorgensen A.O., Kelley J. Purification, primary structure, and immunological characterization of the 26-kDa calsequestrin binding protein (junctin) from cardiac junctional sarcoplasmic reticulum. J Biol Chem 1995, 270:30787-30796.
17. 2+-ATPase of the sarcoplasmic reticulum in adult rat papillary muscle. J Cell Biol 1982, 93:883-892.
18. McFarland T.P., Milstein M.L., Cala S.E. Rough endoplasmic reticulum to junctional sarcoplasmic reticulum trafficking of calsequestrin in adult cardiomyocytes. J Mol Cell Cardiol 2010, 556-564. [MS ID#: JOCES/2009/061572].
19. Houle T.D., Ram M.L., McMurray W.J., Cala S.E. Different endoplasmic reticulum trafficking and processing pathways for calsequestrin (CSQ) and epitope-tagged CSQ. Exp Cell Res 2006, 312:4150-4161. [Epub 2006 Sep 20].
20. Milstein M.L., Houle T.D., Cala S.E. Calsequestrin isoforms localize to different ER subcompartments: evidence for polymer and heteropolymer-dependent localization. Exp Cell Res 2009, 315:523-534.
21. Vega A.L., Yuan C., Votaw V.S., Santana L.F. Dynamic changes in sarcoplasmic reticulum structure in ventricular myocytes. J Biomed Biotechnol 2011, 2011:382586.
22. Kabaeva Z., Zhao M., Michele D.E. Blebbistatin extends culture life of adult mouse cardiac myocytes and allows efficient and stable transgene expression. Am J Physiol Heart Circ Physiol 2008, 294:H1667-H1674.
23. Ram M.L., Kiarash A., Marsh J.D., Cala S.E. Phosphorylation and dephosphorylation of calsequestrin on CK2-sensitive sites in heart. Mol Cell Biochem 2004, 266:209-217.
24. Terentyev D., Cala S.E., Houle T.D., Viatchenko-Karpinski S., Gyorke I., Terentyeva R., et al. Triadin overexpression stimulates excitation-contraction coupling and increases predisposition to cellular arrhythmia in cardiac myocytes. Circ Res 2005, 96:651-658. [Epub 2005 Feb 24].
25. He T.C., Zhou S., da Costa L.T., Yu J., Kinzler K.W., Vogelstein B. A simplified system for generating recombinant adenoviruses. Proc Natl Acad Sci U S A 1998, 95:2509-2514.
26. Zhang L., Kelley J., Schmeisser G., Kobayashi Y.M., Jones L.R. Complex formation between junctin, triadin, calsequestrin, and the ryanodine receptor. Proteins of the cardiac junctional sarcoplasmic reticulum membrane. J Biol Chem 1997, 272:23389-23397.
27. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227:680-685.
28. Guo A., Cala S.E., Song L.S. Calsequestrin accumulation in rough endoplasmic reticulum promotes perinuclear Ca2+ release. J Biol Chem 2012, 287:16670-16680.
29. Campbell R.E., Tour O., Palmer A.E., Steinbach P.A., Baird G.S., Zacharias D.A., et al. A monomeric red fluorescent protein. Proc Natl Acad Sci U S A 2002, 99:7877-7882.
30. Mitchell R.D., Simmerman H.K., Jones L.R. Ca2+ binding effects on protein conformation and protein interactions of canine cardiac calsequestrin. J Biol Chem 1988, 263:1376-1381.
31. Houle T.D., Ram M.L., Cala S.E. Calsequestrin mutant D307H exhibits depressed binding to its protein targets and a depressed response to calcium. Cardiovasc Res 2004, 64:227-233.
32. Oddoux S., Zaal K.J., Tate V., Kenea A., Nandkeolyar S.A., Reid E., et al. Microtubules that form the stationary lattice of muscle fibers are dynamic and nucleated at Golgi elements. J Cell Biol 2013, 203:205-213.
33. Prins K.W., Humston J.L., Mehta A., Tate V., Ralston E., Ervasti J.M. Dystrophin is a microtubule-associated protein. J Cell Biol 2009, 186:363-369.
34. O'Brian J.J., Ram M.L., Kiarash A., Cala S.E. Mass spectrometry of cardiac calsequestrin characterizes microheterogeneity unique to heart and indicative of complex intracellular transit. J Biol Chem 2002, 277:37154-37160.
35. Kiarash A., Kelly C., Phinney B., Valdivia H., Abrams J., Cala S. Defective glycosylation of calsequestrin in heart failure. Cardiovasc Res 2004, 63:264-272.
36. Jacob S., Sleiman N.H., Kern S., Jones L.R., Sala-Mercado J.A., McFarland T.P., et al. Altered calsequestrin glycan processing is common to diverse models of canine heart failure. Mol Cell Biochem 2013, 377:11-21.
37. Milstein M.L., McFarland T.P., Marsh J.D., Cala S.E. Inefficient glycosylation leads to high steady-state levels of actively degrading cardiac triadin-1. J Biol Chem 2008, 283:1929-1935.
38. McFarland T.P., Sleiman N.H., Yaeger D.B., Cala S.E. The cytosolic protein kinase CK2 phosphorylates cardiac calsequestrin in intact cells. Mol Cell Biochem 2011, 353:81-91.
39. Escobar M., Cardenas C., Colavita K., Petrenko N.B., Franzini-Armstrong C. Structural evidence for perinuclear calcium microdomains in cardiac myocytes. J Mol Cell Cardiol 2011, 50:451-459.
40. Nissinen M., Kaisto T., Salmela P., Peltonen J., Metsikko K. Restricted distribution of mRNAs encoding a sarcoplasmic reticulum or transverse tubule protein in skeletal myofibers. J Histochem Cytochem 2005, 53:217-227.
41. Slade A.M., Severs N.J. Rough endoplasmic reticulum in the adult mammalian cardiac muscle cell. J Submicrosc Cytol 1985, 17:531-536.
42. Ogata T., Yamasaki Y. High-resolution scanning electron microscopic studies on the three-dimensional structure of the transverse-axial tubular system, sarcoplasmic reticulum and intercalated disc of the rat myocardium. Anat Rec 1990, 228:277-287.
43. 2+ blinks: rapid nanoscopic store calcium signaling. Proc Natl Acad Sci U S A 2005, 102:3099-3104.
44. Hayashi T., Martone M.E., Yu Z., Thor A., Doi M., Holst M.J., et al. Three-dimensional electron microscopy reveals new details of membrane systems for Ca2+ signaling in the heart. J Cell Sci 2009, 122:1005-1013.
45. Forbes M.S., van Neil E.E. Membrane systems of guinea pig myocardium: ultrastructure and morphometric studies. Anat Rec 1988, 222:362-379.
46. Jayasinghe I., Crossman D., Soeller C., Cannell M. Comparison of the organization of T-tubules, sarcoplasmic reticulum and ryanodine receptors in rat and human ventricular myocardium. Clin Exp Pharmacol Physiol 2012, 39:469-476.
47. Pinali C., Bennett H., Davenport J.B., Trafford A.W., Kitmitto A. Three-dimensional reconstruction of cardiac sarcoplasmic reticulum reveals a continuous network linking transverse-tubules: this organization is perturbed in heart failure. Circ Res 2013, 113:1219-1230.
48. Soeller C., Baddeley D. Super-resolution imaging of EC coupling protein distribution in the heart. J Mol Cell Cardiol 2013, 58:32-40.
49. Asghari P., Schulson M., Scriven D.R., Martens G., Moore E.D. Axial tubules of rat ventricular myocytes form multiple junctions with the sarcoplasmic reticulum. Biophys J 2009, 96:4651-4660.
50. Porter K.R., Palade G.E. Studies on the endoplasmic reticulum. III. Its form and distribution in striated muscle cells. J Biophys Biochem Cytol 1957, 3:269-300.
51. Kaisto T., Metsikko K. Distribution of the endoplasmic reticulum and its relationship with the sarcoplasmic reticulum in skeletal myofibers. Exp Cell Res 2003, 289:47-57.
52. Volpe P., Villa A., Podini P., Martini A., Nori A., Panzeri M.C., et al. The endoplasmic reticulum-sarcoplasmic reticulum connection: distribution of endoplasmic reticulum markers in the sarcoplasmic reticulum of skeletal muscle fibers. Proc Natl Acad Sci U S A 1992, 89:6142-6146.
53. Zanetti G., Pahuja K.B., Studer S., Shim S., Schekman R. COPII and the regulation of protein sorting in mammals. Nat Cell Biol 2012, 14:20-28.
54. Ikonov A.V., Hauri H.P., Lauring B., Kreibich G. Climp-63-mediated binding of microtubules to the ER affects the lateral mobility of translocon complexes. J Cell Sci 2007, 120:2248-2258.
55. Bola B., Allan V. How and why does the endoplasmic reticulum move?. Biochem Soc Trans 2009, 37:961-965.
56. Fu M.M., Holzbaur E.L. Integrated regulation of motor-driven organelle transport by scaffolding proteins. Trends Cell Biol 2014, 10:564-574.
57. Allan V.J. Cytoplasmic dynein. Biochem Soc Trans 2011, 39:1169-1178.
58. Hirokawa N., Noda Y., Tanaka Y., Niwa S. Kinesin superfamily motor proteins and intracellular transport. Nat Rev Mol Cell Biol 2009, 10:682-696.
59. Zadeh A.D., Cheng Y., Xu H., Wong N., Wang Z., Goonasekara C., et al. Kif5b is an essential forward trafficking motor for the Kv1.5 cardiac potassium channel. J Physiol 2009, 587:4565-4574.
60. Kronebusch P.J., Singer S.J. The microtubule-organizing complex and the Golgi apparatus are co-localized around the entire nuclear envelope of interphase cardiac myocytes. J Cell Sci 1987, 88(Pt 1):25-34.
61. Zhang C., Chen B., Guo A., Zhu Y., Miller J.D., Gao S., et al. Microtubule-mediated defects in junctophilin-2 trafficking contribute to myocyte transverse-tubule remodeling and Ca2+ handling dysfunction in heart failure. Circulation 2014, 129:1742-1750.
62. Guo A., Zhang X., Iyer V.R., Chen B., Zhang C., Kutschke W.J., et al. Overexpression of junctophilin-2 does not enhance baseline function but attenuates heart failure development after cardiac stress. Proc Natl Acad Sci U S A 2014, 111:12240-12245.