Coupled Ca2+/H+ transport by cytoplasmic buffers regulates local Ca2+ and H+ ion signaling

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

Volumn 110, Issue 22, 2013, Pages

  Swietach, Pawel ^a   Youm, Jae Boum ^a,b   Saegusa, Noriko ^c   Leem, Chae Hun ^d   Spitzer, Kenneth W ^a   Vaughan Jones, Richard D ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b Inje University   (South Korea)

^c UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^d University of Ulsan College of Medicine   (South Korea)

Author keywords

Calcium; Dual Microperfusion; Heart; Mobile Buffer; Ph

Indexed keywords

ACETIC ACID; ADENOSINE TRIPHOSPHATE; CALCIUM ION; PROTON; CALCIUM; DIPEPTIDE; HISTIDINE;

ACIDOSIS; ANIMAL TISSUE; ARTICLE; CALCIUM CELL LEVEL; CALCIUM SIGNALING; CALCIUM TRANSPORT; CELL METABOLISM; CELL PH; CONTROLLED STUDY; EVOKED RESPONSE; FLUORESCENCE IMAGING; GLYCOLYSIS; HEART MITOCHONDRION; HEART MUSCLE CELL; HYPERPOLARIZATION; IN VITRO STUDY; ION EXCHANGE; METABOLIC INHIBITION; METABOLIC STRESS; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL RESPIRATION; NONHUMAN; OXIDATIVE COUPLING; PERFUSION; PRIORITY JOURNAL; PROTON TRANSPORT; RAT; SARCOPLASMIC RETICULUM; ANIMAL; CYTOPLASM; DUAL MICROPERFUSION; FLUORESCENCE MICROSCOPY; FLUOROMETRY; HEART; METABOLISM; MOBILE BUFFER; PH; PHYSIOLOGY;

CALCIUM; DUAL MICROPERFUSION; HEART; MOBILE BUFFER; PH;

ADENOSINE TRIPHOSPHATE; ANIMALS; CALCIUM SIGNALING; CYTOPLASM; DIPEPTIDES; FLUOROMETRY; HISTIDINE; MICROSCOPY, FLUORESCENCE; MYOCYTES, CARDIAC; PROTONS; RATS;

MLCS; MLOWN;

EID: 84878454612     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1222433110     Document Type: Article

References (46)

1. Clapham DE (2007) Calcium signaling. Cell 131(6):1047-1058.
2. Boron WF (2004) Regulation of intracellular pH. Adv Physiol Educ 28(1-4):160-179.
3. Bers DM (2002) Cardiac excitation-contraction coupling. Nature 415(6868):198-205.
4. Vaughan-Jones RD, Spitzer KW, Swietach P (2009) Intracellular pH regulation in heart. J Mol Cell Cardiol 46(3):318-331.
5. Mandel F, Kranias EG, Grassi de Gende A, Sumida M, Schwartz A (1982) The effect of pH on the transient-state kinetics of Ca2+-Mg2+-ATPase of cardiac sarcoplasmic reticulum. A comparison with skeletal sarcoplasmic reticulum. Circ Res 50(2):310-317.
6. Choi HS, Trafford AW, Orchard CH, Eisner DA (2000) The effect of acidosis on systolic Ca2+ and sarcoplasmic reticulum calcium content in isolated rat ventricular myocytes. J Physiol 529(Pt 3):661-668.
7. Bountra C, Vaughan-Jones RD (1989) Effect of intracellular and extracellular pH on contraction in isolated, mammalian cardiac muscle. J Physiol 418:163-187.
8. Harrison SM, Frampton JE, McCall E, Boyett MR, Orchard CH (1992) Contraction and intracellular Ca2+, Na+ and H+ during acidosis in rat ventricular myocytes. Am J Physiol 262(2 Pt 1):C348-C357.
9. Gambassi G, et al. (1993) Effects of acidosis on resting cytosolic and mitochondrial Ca2+ in mammalian myocardium. J Gen Physiol 102(3):575-597.
10. Kushmerick MJ, Podolsky RJ (1969) Ionic mobility in muscle cells. Science 166(3910): 1297-1298.
11. Vaughan-Jones RD, Peercy BE, Keener JP, Spitzer KW (2002) Intrinsic H(+) ion mobility in the rabbit ventricular myocyte. J Physiol 541(Pt 1):139-158.
12. Bassani RA, Bassani JW, Bers DM (1992) Mitochondrial and sarcolemmal Ca2+ transport reduce [Ca2+]i during caffeine contractures in rabbit cardiac myocytes. J Physiol 453:591-608.
13. Swietach P, Vaughan-Jones RD (2005) Spatial regulation of intracellular pH in the ventricular myocyte. Ann N Y Acad Sci 1047:271-282.
14. Swietach P, Leem CH, Spitzer KW, Vaughan-Jones RD (2005) Experimental generation and computational modeling of intracellular pH gradients in cardiac myocytes. Biophys J 88(4):3018-3037.
15. Cheng H, Lederer WJ, Cannell MB (1993) Calcium sparks: Elementary events underlying excitation-contraction coupling in heart muscle. Science 262(5134): 740-744.
16. Higgins ER, Cannell MB, Sneyd J (2006) A buffering SERCA pump in models of calcium dynamics. Biophys J 91(1):151-163.
17. Jiang D, Zhao L, Clapham DE (2009) Genome-wide RNAi screen identifies Letm1 as a mitochondrial Ca2+/H+ antiporter. Science 326(5949):144-147.
18. Swietach P, Spitzer KW, Vaughan-Jones RD (2007) pH-Dependence of extrinsic and intrinsic H(+)-ion mobility in the rat ventricular myocyte, investigated using flash photolysis of a caged-H(+) compound. Biophys J 92(2):641-653.
19. Cordeiro JM, et al. (2001) Location of the initiation site of calcium transients and sparks in rabbit heart Purkinje cells. J Physiol 531(Pt 2):301-314.
20. O'Dowd JJ, Robins DJ, Miller DJ (1988) Detection, characterisation, and quantification of carnosine and other histidyl derivatives in cardiac and skeletal muscle. Biochim Biophys Acta 967(2):241-249.
21. House JR, Miller DJ, O'Dowd JJ (1989) Differences in the distribution of the imidazoles of rat heart between atria and ventricles. J Physiol 417:162.P.
22. Swietach P, Vaughan-Jones RD (2005) Relationship between intracellular pH and proton mobility in rat and guinea-pig ventricular myocytes. J Physiol 566(Pt 3): 793-806.
23. O'Dowd JJ, Cairns MT, Trainor M, Robins DJ, Miller DJ (1990) Analysis of carnosine, homocarnosine, and other histidyl derivatives in rat brain. J Neurochem 55(2): 446-452.
24. Brini M, Carafoli E (2009) Calcium pumps in health and disease. Physiol Rev 89(4): 1341-1378.
25. Swietach P, Camelliti P, Hulikova A, Kohl P, Vaughan-Jones RD (2010) Spatial regulation of intracellular pH in multicellular strands of neonatal rat cardiomyocytes. Cardiovasc Res 85(4):729-738.
26. Baran EJ (2000) Metal complexes of carnosine. Biochemistry (Mosc) 65(7):789-797.
27. Almulla HA, Bush PG, Steele MG, Ellis D, Flatman PW (2006) Loading rat heart myocytes with Mg2+ using low-[Na+] solutions. J Physiol 575(Pt 2):443-454.
28. Lazdunski M, Frelin C, Vigne P (1985) The sodium/hydrogen exchange system in cardiac cells: Its biochemical and pharmacological properties and its role in regulating internal concentrations of sodium and internal pH. J Mol Cell Cardiol 17(11): 1029-1042.
29. Bers DM, Ellis D (1982) Intracellular calcium and sodium activity in sheep heart Purkinje fibres. Effect of changes of external sodium and intracellular pH. Pflugers Arch 393(2):171-178.
30. Kohmoto O, Spitzer KW, Movsesian MA, Barry WH (1990) Effects of intracellular acidosis on [Ca2+]i transients, transsarcolemmal Ca2+ fluxes, and contraction in ventricular myocytes. Circ Res 66(3):622-632.
31. Kushmerick MJ (1997) Multiple equilibria of cations with metabolites in muscle bioenergetics. Am J Physiol 272(5 Pt 1):C1739-C1747.
32. Minta A, Kao JP, Tsien RY (1989) Fluorescent indicators for cytosolic calcium based on rhodamine and fluorescein chromophores. J Biol Chem 264(14):8171-8178.
33. Garciarena CD, Ma YL, Swietach P, Huc L, Vaughan-Jones RD (2013) Sarcolemmal localisation of Na+/H+ exchange and Na+-HCO3 -co-transport influences the spatial regulation of intracellular pH in rat ventricular myocytes. J Physiol, jphysiol.2012. 249664.
34. Xiong JW, Zhu L, Jiao X, Liu SS (2010) Evidence for DeltapH surface component (DeltapH(S)) of proton motive force in ATP synthesis of mitochondria. Biochim Biophys Acta 1800(3):213-222.
35. Yurkov VI, Fadeeva MS, Yaguzhinsky LS (2005) Proton transfer through the membrane-water interfaces in uncoupled mitochondria. Biochemistry (Mosc) 70(2): 195-199.
36. Swietach P, Rossini A, Spitzer KW, Vaughan-Jones RD (2007) H+ ion activation and inactivation of the ventricular gap junction: A basis for spatial regulation of intracellular pH. Circ Res 100(7):1045-1054.
37. Cannell MB, Kong CH (2012) Local control in cardiac E-C coupling. J Mol Cell Cardiol 52(2):298-303.
38. Valent I, Zahradníková A, Pavelková J, Zahradník I (2007) Spatial and temporal Ca2+, Mg2+ and ATP2-dynamics in cardiac dyads during calcium release. Biochim Biophys Acta 1768(1):155-166.
39. Biffo S, Grillo M, Margolis FL (1990) Cellular localization of carnosine-like and anserinelike immunoreactivities in rodent and avian central nervous system. Neuroscience 35(3): 637-651.
40. Stewart AK, Boyd CA, Vaughan-Jones RD (1999) A novel role for carbonic anhydrase: Cytoplasmic pH gradient dissipation in mouse small intestinal enterocytes. J Physiol 516(Pt 1):209-217.
41. Ro HA, Carson JH (2004) pH microdomains in oligodendrocytes. J Biol Chem 279(35): 37115-37123.
42. Martin C, Pedersen SF, Schwab A, Stock C (2011) Intracellular pH gradients in migrating cells. Am J Physiol Cell Physiol 300(3):C490-C495.
43. Schwiening CJ, Willoughby D (2002) Depolarization-induced pH microdomains and their relationship to calcium transients in isolated snail neurones. J Physiol 538(Pt 2): 371-382.
44. Willoughby D, Schwiening CJ (2002) Electrically evoked dendritic pH transients in rat cerebellar Purkinje cells. J Physiol 544(Pt 2):487-499.
45. Johnson DE, Casey JR (2011) Cytosolic H+ microdomain developed around AE1 during AE1-mediated Cl-/HCO3 -exchange. J Physiol 589(Pt 7):1551-1569.
46. Bednarczyk P, Barker GD, Halestrap AP (2008) Determination of the rate of K(+) movement through potassium channels in isolated rat heart and liver mitochondria. Biochim Biophys Acta 1777(6):540-548.