Manipulating L-type calcium channels in cardiomyocytes using split-intein protein transsplicing

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 38, 2013, Pages 15461-15466

  Subramanyam, Prakash ^a   Chang, Donald D ^a   Fang, Kun ^a   Xie, Wenjun ^a   Marks, Andrew R ^a   Colecraft, Henry M ^a  

^a Columbia University ^*  (United States)

Author keywords

CaV1.2; Gene transfer; Protein splicing; Ventricular myocytes

Indexed keywords

ADENOVIRUS VECTOR; CALCIUM CHANNEL L TYPE; CAVEOLIN 3; DIHYDROPYRIDINE; INTEIN;

ADRENERGIC SYSTEM; ARTICLE; CONTROLLED STUDY; EXCITATION CONTRACTION COUPLING; HEART MUSCLE CELL; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROCESSING; PROTEIN SUBUNIT; TRANS SPLICING;

CAV1.2; GENE TRANSFER; PROTEIN SPLICING; VENTRICULAR MYOCYTES;

ADENOVIRIDAE; ANALYSIS OF VARIANCE; CALCIUM CHANNELS, L-TYPE; GENE TRANSFER TECHNIQUES; GENETIC VECTORS; HEK293 CELLS; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; INTEINS; MICROSCOPY, CONFOCAL; MYOCYTES, CARDIAC; PATCH-CLAMP TECHNIQUES; PLASMIDS; PROTEIN SPLICING; QUANTUM DOTS;

EID: 84884342760     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1308161110     Document Type: Article

References (48)

1. Bers D (2001) Excitation-Contraction Coupling and Cardiac Contractile Force (Kluwer Academic Publishers, Dordrecht, the Netherlands), 2nd Ed, p 427.
2. Louch WE, Sheehan KA, Wolska BM (2011) Methods in cardiomyocyte isolation, culture, and gene transfer. J Mol Cell Cardiol 51(3):288-298.
3. Vinge LE, Raake PW, Koch WJ (2008) Gene therapy in heart failure. Circ Res 102(12): 1458-1470.
4. Bers DM (2002) Cardiac excitation-contraction coupling. Nature 415(6868):198-205.
5. Scriven DR, Dan P, Moore ED (2000) Distribution of proteins implicated in excitationcontraction coupling in rat ventricular myocytes. Biophys J 79(5):2682-2691.
6. Fabiato A (1983) Calcium-induced release of calcium from the cardiac sarcoplasmic reticulum. Am J Physiol 245(1):C1-C14.
7. Balijepalli RC, Foell JD, Hall DD, Hell JW, Kamp TJ (2006) Localization of cardiac L-type Ca(2+) channels to a caveolar macromolecular signaling complex is required for beta (2)-adrenergic regulation. Proc Natl Acad Sci USA 103(19):7500-7505.
8. 2+ channel antagonist inhibits hypertrophic signaling without reducing cardiac contractility. Circ Res 110(5): 669-674.
9. Shaw RM, Colecraft HM (2013) L-type calcium channel targeting and local signalling in cardiac myocytes. Cardiovasc Res 98(2):177-186.
10. Reuter H, Scholz H (1977) The regulation of the calcium conductance of cardiac muscle by adrenaline. J Physiol 264(1):49-62.
11. Miriyala J, Nguyen T, Yue DT, Colecraft HM (2008) Role of CaVbeta subunits, and lack of functional reserve, in protein kinase A modulation of cardiac CaV1.2 channels. Circ Res 102(7):e54-e64.
12. Zong X, et al. (1995) On the regulation of the expressed L-type calcium channel by cAMP-dependent phosphorylation. Pflugers Arch 430(3):340-347.
13. Catterall WA (2010) Signaling complexes of voltage-gated sodium and calcium channels. Neurosci Lett 486(2):107-116.
14. Perler FB, et al. (1994) Protein splicing elements: Inteins and exteins-a definition of terms and recommended nomenclature. Nucleic Acids Res 22(7):1125-1127.
15. Lockless SW, Muir TW (2009) Traceless protein splicing utilizing evolved split inteins. Proc Natl Acad Sci USA 106(27):10999-11004.
16. Muralidharan V, Muir TW (2006) Protein ligation: An enabling technology for the biophysical analysis of proteins. Nat Methods 3(6):429-438.
17. Iwai H, Züger S, Jin J, Tam PH (2006) Highly efficient protein trans-splicing by a naturally split DnaE intein from Nostoc punctiforme. FEBS Lett 580(7):1853-1858.
18. Zettler J, Schütz V, Mootz HD (2009) The naturally split Npu DnaE intein exhibits an extraordinarily high rate in the protein trans-splicing reaction. FEBS Lett 583(5): 909-914.
19. Catterall WA (2000) Structure and regulation of voltage-gated Ca2+ channels. Annu Rev Cell Dev Biol 16:521-555.
20. Sekine-Aizawa Y, Huganir RL (2004) Imaging of receptor trafficking by using alphabungarotoxin-binding-site-tagged receptors. Proc Natl Acad Sci USA 101(49):17114-17119.
21. Yang T, Xu X, Kernan T, Wu V, Colecraft HM (2010) Rem, a member of the RGK GTPases, inhibits recombinant CaV1.2 channels using multiple mechanisms that require distinct conformations of the GTPase. J Physiol 588(Pt 10):1665-1681.
22. He M, Bodi I, Mikala G, Schwartz A (1997) Motif III S5 of L-type calcium channels is involved in the dihydropyridine binding site. A combined radioligand binding and electrophysiological study. J Biol Chem 272(5):2629-2633.
23. Mitterdorfer J, et al. (1996) Two amino acid residues in the IIIS5 segment of L-type calcium channels differentially contribute to 1,4-dihydropyridine sensitivity. J Biol Chem 271(48):30330-30335.
24. Ahern CA, et al. (2001) Intramembrane charge movements and excitation-contraction coupling expressed by two-domain fragments of the Ca2+ channel. Proc Natl Acad Sci USA 98(12):6935-6940.
25. Flucher BE, Weiss RG, Grabner M (2002) Cooperation of two-domain Ca(2+) channel fragments in triad targeting and restoration of excitation-contraction coupling in skeletal muscle. Proc Natl Acad Sci USA 99(15):10167-10172.
26. Raghib A, et al. (2001) Dominant-negative synthesis suppression of voltage-gated calcium channel Cav2.2 induced by truncated constructs. J Neurosci 21(21):8495-8504.
27. Buraei Z, Yang J (2010) The ß subunit of voltage-gated Ca2+ channels. Physiol Rev 90(4):1461-1506.
28. Fang K, Colecraft HM (2011) Mechanism of auxiliary β-subunit- mediated membrane targeting of L-type (Ca(V)1.2) channels. J Physiol 589(Pt 18):4437-4455.
29. Bolte S, Cordelières FP (2006) A guided tour into subcellular colocalization analysis in light microscopy. J Microsc 224(Pt 3):213-232.
30. Nichols CB, et al. (2010) Sympathetic stimulation of adult cardiomyocytes requires association of AKAP5 with a subpopulation of L-type calcium channels. Circ Res 107(6):747-756.
31. Colecraft HM, et al. (2002) Novel functional properties of Ca(2+) channel beta subunits revealed by their expression in adult rat heart cells. J Physiol 541(Pt 2):435-452.
32. Luo W, et al. (1998) Transgenic approaches to define the functional role of dual site phospholamban phosphorylation. J Biol Chem 273(8):4734-4739.
33. Bünemann M, Gerhardstein BL, Gao T, Hosey MM (1999) Functional regulation of L-type calcium channels via protein kinase A-mediated phosphorylation of the beta(2) subunit. J Biol Chem 274(48):33851-33854.
34. Gao T, et al. (1997) cAMP-dependent regulation of cardiac L-type Ca2+ channels requires membrane targeting of PKA and phosphorylation of channel subunits. Neuron 19(1):185-196.
35. Brandmayr J, et al. (2012) Deletion of the C-terminal phosphorylation sites in the cardiac β-subunit does not affect the basic β-adrenergic response of the heart and the Ca(v)1.2 channel. J Biol Chem 287(27):22584-22592.
36. Lemke T, et al. (2008) Unchanged beta-adrenergic stimulation of cardiac L-type calcium channels in Ca v 1.2 phosphorylation site S1928A mutant mice. J Biol Chem 283(50):34738-34744.
37. Ganesan AN, Maack C, Johns DC, Sidor A, O'Rourke B (2006) Beta-adrenergic stimulation of L-type Ca2+ channels in cardiac myocytes requires the distal carboxyl terminus of alpha1C but not serine 1928. Circ Res 98(2):e11-e18.
38. Fuller MD, Emrick MA, Sadilek M, Scheuer T, Catterall WA (2010) Molecular mechanism of calcium channel regulation in the fight-or-flight response. Sci Signal 3(141):ra70.
39. Fu Y, et al. (2011) Deletion of the distal C terminus of CaV1.2 channels leads to loss of beta-adrenergic regulation and heart failure in vivo. J Biol Chem 286(14):12617-12626.
40. Domes K, et al. (2011) Truncation of murine CaV1.2 at Asp-1904 results in heart failure after birth. J Biol Chem 286(39):33863-33871.
41. Nerbonne JM, Kass RS (2005) Molecular physiology of cardiac repolarization. Physiol Rev 85(4):1205-1253.
42. Ganesan AN, et al. (2005) Reverse engineering the L-type Ca2+ channel alpha1c subunit in adult cardiac myocytes using novel adenoviral vectors. Biochem Biophys Res Commun 329(2):749-754.
43. Walsh KB, Zhang J, Fuseler JW, Hilliard N, Hockerman GH (2007) Adenoviral-mediated expression of dihydropyridine-insensitive L-type calcium channels in cardiac ventricular myocytes and fibroblasts. Eur J Pharmacol 565(1-3):7-16.
44. Thiel WH, et al. (2008) Proarrhythmic defects in Timothy syndrome require calmodulin kinase II. Circulation 118(22):2225-2234.
45. Dou Y, et al. (2010) Normal targeting of a tagged Kv1.5 channel acutely transfected into fresh adult cardiac myocytes by a biolistic method. Am J Physiol Cell Physiol 298(6):C1343-C1352.
46. Ferrera R, et al. (2005) Efficient and non-toxic gene transfer to cardiomyocytes using novel generation amplicon vectors derived from HSV-1. J Mol Cell Cardiol 38(1): 219-223.
47. Xu X, Colecraft HM (2009) Primary culture of adult rat heart myocytes. J Vis Exp, 10.3791/1308.
48. Tian Q, et al. (2012) Functional and morphological preservation of adult ventricular myocytes in culture by sub-micromolar cytochalasin D supplement. J Mol Cell Cardiol 52(1):113-124.