Skip to main content

Calcium Signaling by cADPR in Cardiac Myocytes

  • Chapter
Cyclic ADP-Ribose and NAADP

Abstract

The heart is a muscular organ, composed of electrically connected excitable cells that act in a coordinated, syncytial fashion to pump blood to the other tissues of the body. Since Ringer’s observation in 1883 that Ca2+ is essential for contraction of the heart [1], major advancements have been made in elucidating the mechanisms by which electrical excitation of the myocardium (the cardiac action potential, initiated by the pacemaker region) is linked to mechanical contraction of the heart, and it is now well established that Ca2+ ions play the fundamental role in this coupling of excitation to contraction.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Ringer S. 1883. A further contribution regarding the influence of the different constituents of the blood on the contraction of the heart. J. Physiol. 4: 29–42.

    PubMed  CAS  Google Scholar 

  2. Bers DM. 2001. Excitation-contraction coupling and cardiac contractile force (2nd ed). Kluwer Academic, Dordrecht, Norwell, MA.

    Book  Google Scholar 

  3. Tada M, Yamada M, Kadoma M, Inui M and Ohmori F. 1982. Ca2+ transport by cardiac sarcoplasmic reticulum and phosphorylation of phospholamban. Mol. Cell. Biochem. 46: 74–95.

    Article  Google Scholar 

  4. Scott BT, Simmerman HKB, Collins JH, Nadal-Ginard B and Jones LR. 1988. Complete amino acid sequence of canine cardiac calsequestrin deduced by cDNA cloning. J. Biol. Chem. 263: 8958–8964.

    PubMed  CAS  Google Scholar 

  5. Zucchi R and Ronca-Testoni S. 1997. The sarcoplasmic reticulum Ca2+ channel/ryanodine receptor: modulation by endogenous effectors, drugs and disease states. Pharmacol. Rev. 49:1–51.

    PubMed  CAS  Google Scholar 

  6. Otsu K, Willard HF, Khanna VK, Zorzato F, Green NM and MacLennan DH. 1990. Molecular cloning of cDNA encoding the Ca2+ release channel (ryanodine receptor) of rabbit cardiac muscle sarcoplasmic reticulum. J. Biol. Chem. 265: 13472–13483.

    PubMed  CAS  Google Scholar 

  7. Sorrentino V and Volpe P. 1993. Ryanodine receptors: how many, where and why? Trends Pharmacol. Sci. 14: 98–103.

    Article  PubMed  CAS  Google Scholar 

  8. Rousseau E and Meissner G. 1989. Single cardiac sarcoplasmic reticulum Ca2+-release channel: activation by caffeine. Am. J. Physiol. 256: H328–H333.

    PubMed  CAS  Google Scholar 

  9. Rapundalo ST. 1998. Cardiac protein phosphorylation: functional and pathophysiological correlates. Cardiovasc. Res. 38: 559–588.

    Article  PubMed  CAS  Google Scholar 

  10. Rakovic S, Galione A, Ashamu GA, Potter BVL and Terrar DA. 1996. A specific cyclic ADP-ribose antagonist inhibits cardiac excitation-contraction coupling. Curr. Biol. 6: 989–996.

    Article  PubMed  CAS  Google Scholar 

  11. Walseth TF and Lee HC. 1993. Synthesis and characterization of antagonists of cyclic-ADP-ribose-induced Ca2+ release. Biochim. Biophys. Acta 1178: 235–242.

    Article  PubMed  CAS  Google Scholar 

  12. lino S, Cui Y, Galione A and Terrar DA. 1997. Actions of cADP-ribose and its antagonists on contraction in guinea pig isolated ventricular myocytes. Influence of temperature. Circ. Res. 81: 879–884.

    Article  PubMed  CAS  Google Scholar 

  13. Cui Y, Galione A and Terrar DA. 1999. Effects of photoreleased cADP-ribose on calcium transients and calcium sparks in myocytes isolated from guinea-pig and rat ventricle. Biochem. J. 342: 269–273.

    Article  PubMed  CAS  Google Scholar 

  14. Prakash YS, Kannan MS, Walseth TF and Sieck GC. 2000. cADP ribose and [Ca2+]i regulation in rat cardiac myocytes. Am. J. Physiol. Heart Circ. Physiol. 279: H1482–H1489.

    PubMed  Google Scholar 

  15. Guo X, Laflamme MA and Becker PL. 1996. Cyclic ADP-ribose does not regulate sarcoplasmic reticulum Ca2+ release in intact cardiac myocytes. Circ. Res. 79: 147–151.

    Article  PubMed  CAS  Google Scholar 

  16. Rakovic S, Cui Y, Iino S, Galione A, Ashamu GA, Potter BVL and Terrar DA. 1999. An antagonist of cADP-ribose inhibits arrhythmogenic oscillations of intracellular Ca2+ in heart cells. J. Biol. Chem. 274: 17820–17827.

    Article  PubMed  CAS  Google Scholar 

  17. Lee HC, Aarhus R, Graeff RM, Gurnack ME and Walseth TF. 1994. Cyclic ADP-ribose activation of the ryanodine receptor is mediated by calmodulin. Nature 370: 307–309.

    Article  PubMed  CAS  Google Scholar 

  18. Lee HC Aarhus R and Graeff RM. 1995. Sensitization of calcium-induced calcium release by cyclic ADP-ribose and calmodulin. J. Biol. Chem. 270: 9060–9066.

    Article  PubMed  CAS  Google Scholar 

  19. Tanaka Y and Tashjian A. 1995. Calmodulin is a selective mediator of Ca2+-induced Ca2+ release via the ryanodine receptor-like Ca2+ channel triggered by cyclic ADP-ribose. Proc. Natl. Acad. Sci. USA 92: 3244–3248.

    Article  PubMed  CAS  Google Scholar 

  20. Takasawa S, Ishida A, Nata K, Nakagawa K, Noguchi N, Tohgo A, Kato I, Yonekura H, Fujisawa H and Okamoto H. 1995. Requirement of calmodulin-dependent protein kinase II in cyclic ADP-ribose-mediated intracellular Ca2+ mobilization. J. Biol. Chem. 270: 30257–30259.

    Article  PubMed  CAS  Google Scholar 

  21. Rakovic S, Cui Y, Galione A and Terrar DA. 2002. Requirement of calmodulin for actions of cADPR in guinea-pig ventricular myocytes. Biophys. J. 82: 57a.

    Google Scholar 

  22. Okabe E, Tsujimoto Y and Kobayashi Y. 2000. Calmodulin and cyclic ADP-ribose interaction in Ca2+ signaling related to cardiac sarcoplasmic reticulum: superoxide anion radical-triggered Ca2+ release. Antioxid. Redox. Signal 2: 47–54.

    Article  PubMed  CAS  Google Scholar 

  23. Kumasaka S, Shoji H and Okabe E. 1999. Novel mechanisms involved in superoxide anion radical-triggered Ca2+ release from cardiac sarcoplasmic reticulum linked to cyclic ADP-ribose stimulation. Antioxid. Redox. Signal 1: 55–69.

    Article  PubMed  CAS  Google Scholar 

  24. Timerman AP, Jayaraman T, Wiederrecht G, Onoue H, Marks AR and Fleischer S. 1994. The ryanodine receptor from canine heart sarcoplasmic reticulum is associated with a novel FK-506 binding protein. Biochem. Biophys. Res. Commun. 198: 701–706.

    Article  PubMed  CAS  Google Scholar 

  25. McCall E, Li L, Satoh H, Shannon TR, Blatter LA and Bers DM. 1996. Effects of FK-506 on contraction and Ca2+ transients in rat cardiac myocytes. Circ. Res. 79: 1110–1121.

    Article  PubMed  CAS  Google Scholar 

  26. Xiao RP, Valdivia HH, Bogdanov K, Valdivia C, Lakatta EG and Cheng H. 1997. The immunophilin FK506-binding protein modulates Ca2+ release channel closure in rat heart. J. Physiol. 500: 343–354.

    PubMed  CAS  Google Scholar 

  27. Noguchi N, Takasawa S, Nata K, Tohgo A, Kato I, Ikehata F, Yonekura H and Okamoto H. 1997. Cyclic ADP-ribose binds to FK506-binding protein 12.6 to release Ca2+ from islet microsomes. J. Biol. Chem. 272: 3133–3136.

    Article  PubMed  CAS  Google Scholar 

  28. Xin H-B, Ji GJ, Deng K-Y, Fleischer S and Kotlikoff MI. 2002. FK506 binding protein 12.6 plays a central role in cyclic ADP-ribose triggered Ca2+-induced Ca2+ release via type 2 ryanodine receptor in mouse cardiac myocytes. Biophys. J. 82: 59a.

    Google Scholar 

  29. Timerman AP, Wiederrecht G, Marcy A and Fleischer S. 1995. Characterization of an exchange reaction between soluble FKBP-12 and the FKBP ryanodine receptor complex. J. Biol. Chem. 270: 2451–2459.

    Article  PubMed  CAS  Google Scholar 

  30. Meszaros LG, Bak J and Chu A. 1993. Cyclic ADP-ribose as an endogenous regulator of the non-skeletal type ryanodine receptor Ca2+ channel. Nature 364: 76–79.

    Article  PubMed  CAS  Google Scholar 

  31. Sitsapesan R, McGarry SJ and Williams AJ. 1994. Cyclic ADP-ribose competes with ATP for the adenine nucleotide binding site on the cardiac ryanodine receptor Ca2+-release channel. Circ. Res. 75: 596–600.

    Article  PubMed  CAS  Google Scholar 

  32. Sitsapesan R, McGarry SJ and Williams AJ. 1995. Cyclic ADP-ribose, the ryanodine receptor and Ca2+ release. Trends Pharmacol. Sci. 16: 386–391.

    Article  PubMed  CAS  Google Scholar 

  33. Bak J, Billington RA, Timar G, Dutton AC and Genazzani AA. 2001. NAADP receptors are present and functional in the heart. Curr. Biol. 11: 987–990.

    Article  PubMed  CAS  Google Scholar 

  34. Fruen BR, Mickelson JR, Shomer NH, Velez P and Louis CF. 1994. Cyclic ADP-ribose does not affect cardiac or skeletal muscle ryanodine receptors. FEBS Lett. 352: 123–126.

    Article  PubMed  CAS  Google Scholar 

  35. Copello JA, Qi Y, Jeyakumar LH, Ogunbunmi E and Fleischer S. 2001. Lack of effect of cADP-ribose and NAADP on the activity of skeletal muscle and heart ryanodine receptors. Cell Calcium 30: 269–284.

    Article  PubMed  CAS  Google Scholar 

  36. Graeff RM, Podein RJ, Aarhus R and Lee HC. 1995. Magnesium ions but not ATP inhibit cyclic ADP-ribose-induced calcium release. Biochem. Biophys. Res. Commun. 206: 786–791.

    Article  PubMed  CAS  Google Scholar 

  37. Walseth TF, Aarhus R, Kerr JA and Lee HC. 1993. Identification of cyclic ADP-ribose-binding proteins by photoaffinity labeling. J. Biol. Chem. 268: 26686–26691.

    PubMed  CAS  Google Scholar 

  38. Lukyanenko V and Gyorke S. 1999. Ca2+ sparks and Ca2+ waves in saponin-permeabilized rat ventricular myocytes. J. Physiol. 521: 575–585.

    Article  PubMed  CAS  Google Scholar 

  39. Lukyanenko V, Gyorke I, Wiesner TF and Gyorke S. 2001. Potentiation of Ca2+ release by cADP-ribose in the heart is mediated by enhanced SR Ca2+ uptake into the sarcoplasmic reticulum. Circ. Res. 89: 614–622.

    Article  PubMed  CAS  Google Scholar 

  40. Trafford AW, Diaz ME and Eisner DA. 1998. Stimulation of Ca2+-induced Ca2+ release only transiently increases the systolic Ca2+ transient: measurements of Ca2+ fluxes and sarcoplasmic reticulum Ca2+. Cardiovasc. Res. 37: 710–717.

    Article  PubMed  CAS  Google Scholar 

  41. Rakovic S, Galione A and Terrar DA. Unpublished observations.

    Google Scholar 

  42. MacGregor AT, Rakovic S, Galione A and Terrar DA. Unpublished observations.

    Google Scholar 

  43. Lahouratate P, Guibert J and Faivre JF. 1997. cADP-ribose releases Ca2+ from cardiac sarcoplasmic reticulum independently of ryanodine receptor. Am. J. Physiol. 273: H1082–H1089.

    PubMed  Google Scholar 

  44. Galione A, Lee HC and Busa WB. 1991. Ca2+-induced Ca2+ release in sea urchin egg homogenates: modulation by cyclic ADP-ribose. Science 253: 1143–1146.

    Article  PubMed  CAS  Google Scholar 

  45. Morrissette J, Heisermann G, Cleary J, Ruoho A and Coronado R. 1993. Cyclic ADP-ribose induced Ca2+ release in rabbit skeletal muscle sarcoplasmic reticulum. FEBS Lett. 330: 270–274.

    Article  PubMed  CAS  Google Scholar 

  46. Rusinko N and Lee HC. 1989. Widespread occurrence in animal tissue of an enzyme catalyzing the conversion of NAD+ into a cyclic metabolite with intracellular Ca2+ mobilizing activity. J. Biol. Chem. 264: 11725–11731.

    PubMed  CAS  Google Scholar 

  47. Walseth TF, Aarhus R, Zeleznikar RJ Jr and Lee HC. 1991. Determination of endogenous levels of cyclic ADP-ribose in rat tissues. Biochim. Biophys. Acta 1094: 113–120.

    Article  PubMed  CAS  Google Scholar 

  48. Meszaros V, Socci R and Meszaros LG. 1995. The kinetics of cyclic ADP-ribose formation in heart muscle. Biochem. Biophys. Res. Commun. 210: 452–456.

    Article  PubMed  CAS  Google Scholar 

  49. Meszaros LG, Wrenn RW and Varadi G. 1997. Sarcoplasmic reticulum-associated and protein kinase C-regulated ADP-ribosyl cyclase in cardiac muscle. Biochem. Biophys. Resi. 234: 252–256.

    Article  CAS  Google Scholar 

  50. Higashida H, Egorova A, Higashida C, Zhong ZG, Yokoyama S, Noda M and Zhang JS. 1999. Sympathetic potentiation of cyclic ADP-ribose formation in rat cardiac myocytes. J. Biol. Chem. 274: 33348–33354.

    Article  PubMed  CAS  Google Scholar 

  51. Heath BM, Galione A and Terrar DA. 1999. Regulation of cyclic ADP-ribose (cADPR) production by protein kinase A in cardiac ventricular microsomes prepared from guinea-pig heart. Br. J. Pharmacol. 126: 204P.

    Google Scholar 

  52. Sethi JK, Empson RM and Galione A. 1996. Nicotinamide inhibits cyclic ADP-ribose-mediated calcium signalling in sea urchin eggs. Biochem. J. 319: 613–617.

    PubMed  CAS  Google Scholar 

  53. Rakovic S, Galione A, Terrar DA. Unpublished observations.

    Google Scholar 

  54. Lancashire H, Nankivell P, Rakovic S, Galione A and Terrar DA. Unpublished observations.

    Google Scholar 

  55. Thomas JM, Churchill GC, Terrar DA and Galione A. Unpublished observations.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2002 Springer Science+Business Media New York

About this chapter

Cite this chapter

Rakovic, S., Terrar, D.A. (2002). Calcium Signaling by cADPR in Cardiac Myocytes. In: Lee, H.C. (eds) Cyclic ADP-Ribose and NAADP. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-0269-2_15

Download citation

  • DOI: https://doi.org/10.1007/978-1-4615-0269-2_15

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4613-4996-9

  • Online ISBN: 978-1-4615-0269-2

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics