Interstitial volume modulates the conduction velocity-gap junction relationship

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 302, Issue 1, 2012, Pages

  Veeraraghavan, Rengasayee ^a   Salama, Mohamed E ^a   Poelzing, Steven ^a  

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

Author keywords

Arrhythmia; Cable theory; Cardiac conduction

Indexed keywords

ALBUMIN; CARBENOXOLONE; MANNITOL;

ACTION POTENTIAL; ALBUMIN BLOOD LEVEL; ANIMAL CELL; ANIMAL TISSUE; ANISOTROPY; ARTICLE; CELL SIZE; CONTROLLED STUDY; EXPERIMENTAL GUINEA PIG; GAP JUNCTION; HEART LEFT VENTRICLE; HEART MUSCLE; HEART RIGHT VENTRICLE; HEART VENTRICLE TACHYCARDIA; HISTOPATHOLOGY; INTERSTITIAL FLUID; MALE; MOTOR NERVE CONDUCTION; NONHUMAN; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; VELOCITY;

EID: 84255167093     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00868.2011     Document Type: Article

References (45)

1. Akar FG, Nass RD, Hahn S, Cingolani E, Shah M, Hesketh GG, DiSilvestre D, Tunin RS, Kass DA, Tomaselli GF. Dynamic changes in conduction velocity and gap junction properties during development of pacing-induced heart failure. Am J Physiol Heart Circ Physiol 293: H1223-H1230, 2007.
2. Arbel ER, Prabhu R, Ramesh V, Pick R, Glick G. A perfused canine right bundle branch-septal model for electrophysiological studies. Am J Physiol Heart Circ Physiol 236: H379-H384, 1979.
3. Aslanidi OV, Clayton RH, Lambert JL, Holden AV. Dynamical and cellular electrophysiological mechanisms of ECG changes during isch-aemia. J Theor Biol 237: 369-381, 2005.
4. Bayly PV, KenKnight BH, Rogers JM, Hillsley RE, Ideker RE, Smith WM. Estimation of conduction velocity vector fields from epicardial mapping data. IEEE Trans Biomed Eng 45: 563-571, 1998.
5. Beardslee MA, Lerner DL, Tadros PN, Laing JG, Beyer EC, Yamada KA, Kleber AG, Schuessler RB, Saffitz JE. Dephosphorylation and intracellular redistribution of ventricular connexin43 during electrical uncoupling induced by ischemia. Circ Res 87: 656-662, 2000.
6. Beauchamp P, Choby C, Desplantez T, de Peyer K, Green K, Yamada KA, Weingart R, Saffitz JE, Kleber AG. Electrical propagation in synthetic ventricular myocyte strands from germline connexin43 knockout mice. Circ Res 95: 170-178, 2004.
7. Boyle A, Maurer MS, Sobotka PA. Myocellular and interstitial edema and circulating volume expansion as a cause of morbidity and mortality in heart failure. J Card Fail 13: 133-136, 2007.
8. Bukauskas FF, Elfgang C, Willecke K, Weingart R. Biophysical properties of gap junction channels formed by mouse connexin40 in induced pairs of transfected human HeLa cells. Biophys J 68: 2289-2298, 1995.
9. Cabo C, Boyden PA. Extracellular space attenuates the effect of gap junctional remodeling on wave propagation: a computational study. Bio-phys J 96: 3092-3101, 2009.
10. Cascio WE, Yang H, Muller-Borer BJ, Johnson TA. Ischemia-induced arrhythmia: the role of connexins, gap junctions, and attendant changes in impulse propagation. J Electrocardiol 38: 55-59, 2005.
11. Danik SB, Liu F, Zhang J, Suk HJ, Morley GE, Fishman GI, Gutstein DE. Modulation of cardiac gap junction expression and arrhythmic susceptibility. Circ Res 95: 1035-1041, 2004.
12. de Groot JR, Veenstra T, Verkerk AO, Wilders R, Smits JP, Wilms-Schopman FJ, Wiegerinck RF, Bourier J, Belterman CN, Coronel R, Verheijck EE. Conduction slowing by the gap junctional uncoupler carbenoxolone. Cardiovasc Res 60: 288-297, 2003.
13. Drakos SG, Kfoury AG, Hammond EH, Reid BB, Revelo MP, Ras-musson BY, Whitehead KJ, Salama ME, Selzman CH, Stehlik J, Clayson SE, Bristow MR, Renlund DG, Li DY. Impact of mechanical unloading on microvasculature and associated central remodeling features of the failing human heart. J Am Coll Cardiol 56: 382-391, 2010.
14. Eloff BC, Lerner DL, Yamada KA, Schuessler RB, Saffitz JE, Rosen-baum DS. High resolution optical mapping reveals conduction slowing in connexin43 deficient mice. Cardiovasc Res 51: 681-690, 2001.
15. Fleischhauer J, Lehmann L, Kleber AG. Electrical resistances of interstitial and microvascular space as determinants of the extracellular electrical field and velocity of propagation in ventricular myocardium. Circulation 92: 587-594, 1995.
16. Girouard SD, Laurita KR, Rosenbaum DS. Unique properties of cardiac action potentials recorded with voltage-sensitive dyes. J Cardio-vasc Electrophysiol 7: 1024-1038, 1996.
17. Girouard SD, Pastore JM, Laurita KR, Gregory KW, Rosenbaum DS. Optical mapping in a new guinea pig model of ventricular tachycardia reveals mechanisms for multiple wavelengths in a single reentrant circuit. Circulation 93: 603-613, 1996.
18. Guerrero PA, Schuessler RB, Davis LM, Beyer EC, Johnson CM, Yamada KA, Saffitz JE. Slow ventricular conduction in mice heterozygous for a connexin43 null mutation. J Clin Invest 99: 1991-1998, 1997.
19. Gutstein DE, Morley GE, Tamaddon H, Vaidya D, Schneider MD, Chen J, Chien KR, Stuhlmann H, Fishman GI. Conduction slowing and sudden arrhythmic death in mice with cardiac-restricted inactivation of connexin43. Circ Res 88: 333-339, 2001.
20. Haraguchi Y, Shimizu T, Yamato M, Kikuchi A, Okano T. Electrical coupling of cardiomyocyte sheets occurs rapidly via functional gap junction formation. Biomaterials 27: 4765-4774, 2006.
21. Jacob M, Bruegger D, Rehm M, Stoeckelhuber M, Welsch U, Conzen P, Becker BF. The endothelial glycocalyx affords compatibility of Starling's principle and high cardiac interstitial albumin levels. Cardiovasc Res 73: 575-586, 2007.
22. Jacob M, Paul O, Mehringer L, Chappell D, Rehm M, Welsch U, Kaczmarek I, Conzen P, Becker BF. Albumin augmentation improves condition of guinea pig hearts after 4 h of cold ischemia. Transplantation 87: 956-965, 2009.
23. Jongsma HJ, Wilders R. Gap junctions in cardiovascular disease. Circ Res 86: 1193-1197, 2000.
24. Kleber AG, Rudy Y. Basic mechanisms of cardiac impulse propagation and associated arrhythmias. Physiol Rev 84: 431-488, 2004.
25. Lin J, Keener JP. Modeling electrical activity of myocardial cells incorporating the effects of ephaptic coupling. Proc Natl Acad Sci USA 107: 20935-20940, 2010.
26. McIntyre H, Fry CH. Abnormal action potential conduction in isolated human hypertrophied left ventricular myocardium. J Cardiovasc Electro-physiol 8: 887-894, 1997.
27. McNary TG, Sohn K, Taccardi B, Sachse FB. Experimental and computational studies of strain-conduction velocity relationships in cardiac tissue. Prog Biophys Mol Biol 97: 383-400, 2008.
28. Mehlhorn U, Geissler HJ, Laine GA, Allen SJ. Myocardial fluid balance. Eur J Cardiothorac Surg 20: 1220-1230, 2001.
29. Morley GE, Vaidya D, Samie FH, Lo C, Delmar M, Jalife J. Characterization of conduction in the ventricles of normal and heterozygous Cx43 knockout mice using optical mapping. J Cardiovasc Electrophysiol 10: 1361-1375, 1999.
30. Poelzing S, Veeraraghavan R. Heterogeneous ventricular chamber response to hypokalemia and inward rectifier potassium channel blockade underlies bifurcated T wave in guinea pig. Am J Physiol Heart Circ Physiol 292: H3043-H3051, 2007.
31. Qin H, Kay MW, Chattipakorn N, Redden DT, Ideker RE, Rogers JM. Effects of heart isolation, voltage-sensitive dye, and electromechanical uncoupling agents on ventricular fibrillation. Am J Physiol Heart Circ Physiol 284: H1818-H1826, 2003.
32. Rohr S, Kucera JP, Kleber AG. Slow conduction in cardiac tissue, I: effects of a reduction of excitability versus a reduction of electrical coupling on microconduction. Circ Res 83: 781-794, 1998.
33. Ruifrok AC, Johnston DA. Quantification of histochemical staining by color deconvolution. Anal Quant Cytol Histol 23: 291-299, 2001.
34. Seidel T, Salameh A, Dhein S. A simulation study of cellular hypertrophy and connexin lateralization in cardiac tissue. Biophys J 99: 2821-2830, 2010.
35. Smithen C, Christodoulou J, Killip T, Brachfeld N. Metabolic and hemodynamic consequences of mannitol following myocardial anoxia. Am J Physiol 229: 847-852, 1975.
36. Spach MS, Heidlage JF, Barr RC, Dolber PC. Cell size and communication: role in structural and electrical development and remodeling of the heart. Heart Rhythm 1: 500-515, 2004.
37. Sperelakis N. An electric field mechanism for transmission of excitation between myocardial cells. Circ Res 91: 985-987, 2002.
38. Stein M, van Veen TA, Remme CA, Boulaksil M, Noorman M, van Stuijvenberg L, van der Nagel R, Bezzina CR, Hauer RN, de Bakker JM, van Rijen HV. Combined reduction of intercellular coupling and membrane excitability differentially affects transverse and longitudinal cardiac conduction. Cardiovasc Res 83: 52-60, 2009.
39. Stevens AP, Hlady V, Dull RO. Fluorescence correlation spectroscopy can probe albumin dynamics inside lung endothelial glycocalyx. Am J Physiol Lung Cell Mol Physiol 293: L328-L335, 2007.
40. Teman CJ, Wilson AR, Perkins SL, Hickman K, Prchal JT, Salama ME. Quantification of fibrosis and osteosclerosis in myeloproliferative neoplasms: a computer-assisted image study. Leuk Res 34: 871-876, 2010.
41. Thomas SP, Kucera JP, Bircher-Lehmann L, Rudy Y, Saffitz JE, Kleber AG. Impulse propagation in synthetic strands of neonatal cardiac myocytes with genetically reduced levels of connexin43. Circ Res 92: 1209-1216, 2003.
42. Vaidya D, Tamaddon HS, Lo CW, Taffet SM, Delmar M, Morley GE, Jalife J. Null mutation of connexin43 causes slow propagation of ventricular activation in the late stages of mouse embryonic development. Circ Res 88: 1196-1202, 2001.
43. van den Berg BM, Vink H, Spaan JA. The endothelial glycocalyx protects against myocardial edema. Circ Res 92: 592-594, 2003.
44. van Rijen HV, Eckardt D, Degen J, Theis M, Ott T, Willecke K, Jongsma HJ, Opthof T, de Bakker JM. Slow conduction and enhanced anisotropy increase the propensity for ventricular tachyarrhythmias in adult mice with induced deletion of connexin43. Circulation 109: 1048- 1055, 2004.
45. Veeraraghavan R, Poelzing S. Mechanisms underlying increased right ventricular conduction sensitivity to flecainide challenge. Cardiovasc Res 77: 749-756, 2008.