Upregulation of the hyperpolarization-activated current increases pacemaker activity of the sinoatrial node and heart rate during pregnancy in mice

Circulation

Volumn 127, Issue 20, 2013, Pages 2009-2020

  El Khoury, Nabil ^a,b   Mathieu, Sophie ^a,b   Marger, Laurine ^a,b   Ross, Jenna ^a,b   El Gebeily, Gracia ^a,b   Ethier, Nathalie ^a,b   Fiset, Céline ^a,b  

^a MONTREAL HEART INSTITUTE   (Canada)

^b UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

heart rate; ion channels; pacemakers, biological; pregnancy; sinoatrial node

Indexed keywords

CATECHOLAMINE; ISOPRENALINE; RELAXIN;

ADRENERGIC STIMULATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTERIAL PRESSURE; ARTICLE; AUTONOMIC INNERVATION; CONTROLLED STUDY; ELECTROCARDIOGRAPHY; FEMALE; HEART DEPOLARIZATION; HEART MUSCLE POTENTIAL; HEART RATE; HEMODYNAMICS; HYPERPOLARIZATION; MOUSE; NONHUMAN; PACEMAKER; PREGNANCY; PRIORITY JOURNAL; PROTEIN EXPRESSION; SINUS NODE; UPREGULATION; VOLTAGE CLAMP;

HEART RATE; ION CHANNELS; PACEMAKERS, BIOLOGICAL; PREGNANCY; SINOATRIAL NODE;

ANIMALS; CYCLIC NUCLEOTIDE-GATED CATION CHANNELS; FEMALE; HEART CONDUCTION SYSTEM; HEART RATE; HYPERPOLARIZATION-ACTIVATED CYCLIC NUCLEOTIDE-GATED CHANNELS; ION CHANNELS; MICE; POTASSIUM CHANNELS; PREGNANCY; SINOATRIAL NODE; UP-REGULATION;

EID: 84877989745     PISSN: 00097322     EISSN: 15244539     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.113.001689     Document Type: Article

References (50)

1. Rashba EJ, Zareba W, Moss AJ, Hall WJ, Robinson J, Locati EH, Schwartz PJ, Andrews M. Infuence of pregnancy on the risk for cardiac events in patients with hereditary long QT syndrome. LQTS Investigators. Circulation. 1998;97:451-456.
2. Larsen JA, Kadish AH. Effects of gender on cardiac arrhythmias. J Car-diovasc Electrophysiol. 1998;9:655-664.
3. Wolbrette D. Treatment of arrhythmias during pregnancy. Curr Womens Health Rep. 2003;3:135-139.
4. Gowda RM, Khan IA, Mehta NJ, Vasavada BC, Sacchi TJ. Cardiac arrhythmias in pregnancy: clinical and therapeutic considerations. Int J Car-diol. 2003;88:129-133.
5. Hunter S, Robson SC. Adaptation of the maternal heart in pregnancy. Br Heart J. 1992;68:540-543.
6. Adamson DL, Nelson-Piercy C. Managing palpitations and arrhythmias during pregnancy. Heart. 2007;93:1630-1636.
7. Burkart TA, Conti JB. Cardiac arrhythmias during pregnancy. Curr Treat Options Cardiovasc Med. 2010;12:457-471.
8. Thornburg KL, Jacobson SL, Giraud GD, Morton MJ. Hemodynamic changes in pregnancy. Semin Perinatol. 2000;24:11-14.
9. Speranza G, Verlato G, Albiero A. Autonomic changes during pregnancy: assessment by spectral heart rate variability analysis. J Electrocardiol. 1998;31:101-109.
10. Ekholm EM, Erkkola RU. Autonomic cardiovascular control in pregnan-c y. Eur J Obstet Gynecol Reprod Biol. 1996;64:29-36.
11. Opthof T. The normal range and determinants of the intrinsic heart rate in man. Cardiovasc Res. 2000;45:177-184.
12. Irisawa H, Brown HF, Giles W. Cardiac pacemaking in the sinoatrial node. Physiol Rev. 1993;73:197-227.
13. Vinogradova TM, Zhou YY, Maltsev V, Lyashkov A, Stern M, Lakatta EG. Rhythmic ryanodine receptor Ca2+ releases during diastolic depolarization of sinoatrial pacemaker cells do not require membrane depolarization. Circ Res. 2004;94:802-809.
14. Maltsev VA, Vinogradova TM, Lakatta EG. The emergence of a general theory of the initiation and strength of the heartbeat. J Pharmacol Sci. 2006;100:338-369.
15. Mangoni ME, Nargeot J. Genesis and regulation of the heart automaticity. Physiol Rev. 2008;88:919-982.
16. Marionneau C, Couette B, Liu J, Li H, Mangoni ME, Nargeot J, Lei M, Escande D, Demolombe S. Specifc pattern of ionic channel gene expression associated with pacemaker activity in the mouse heart. J Physiol (Lond). 2005;562(Pt 1):223-234.
17. Baruscotti M, Bucchi A, Viscomi C, Mandelli G, Consalez G, Gnecchi-Rusconi T, Montano N, Casali KR, Micheloni S, Barbuti A, DiFrancesco D. Deep bradycardia and heart block caused by inducible cardiac-specifc knockout of the pacemaker channel gene Hcn4. Proc Natl Acad Sci USA. 2011;108:1705-1710.
18. Baruscotti M, Barbuti A, Bucchi A. The cardiac pacemaker current. J Mol Cell Cardiol. 2010;48:55-64.
19. DiFrancesco D, Tortora P. Direct activation of cardiac pacemaker channels by intracellular cyclic AMP. Nature. 1991;351:145-147.
20. Berul CI, McConnell BK, Wakimoto H, Moskowitz IP, Maguire CT, Semsarian C, Vargas MM, Gehrmann J, Seidman CE, Seidman JG. Ventricular arrhythmia vulnerability in cardiomyopathic mice with homozygous mutant Myosin-binding protein C gene. Circulation. 2001;104:2734-2739.
21. Brouillette J, Lupien MA, St-Michel C, Fiset C. Characterization of ventricular repolarization in male and female guinea pigs. J Mol Cell Cardiol. 2007;42:357-366.
22. Mangoni ME, Nargeot J. Properties of the hyperpolarization-activated current (I(f)) in isolated mouse sino-atrial cells. Cardiovasc Res. 2001;52:51-64.
23. Qu Y, Whitaker GM, Hove-Madsen L, Tibbits GF, Accili EA. Hyperpo-larization-activated cyclic nucleotide-modulated 'HCN' channels confer regular and faster rhythmicity to beating mouse embryonic stem cells. J Physiol (Lond). 2008;586:701-716.
24. Harzheim D, Pfeiffer KH, Fabritz L, Kremmer E, Buch T, Waisman A, Kirchhof P, Kaupp UB, Seifert R. Cardiac pacemaker function of HCN4 channels in mice is confned to embryonic development and requires cyclic AMP. EMBO J. 2008;27:692-703.
25. Grandy SA, Trépanier-Boulay V, Fiset C. Postnatal development has a marked effect on ventricular repolarization in mice. Am J Physiol Heart Circ Physiol. 2007;293:H2168-H2177.
26. Clapp JF III, Capeless E. Cardiovascular function before, during, and after the frst and subsequent pregnancies. Am J Cardiol. 1997;80: 1469-1473.
27. Ekholm EM, Erkkola RU, Piha SJ, Jalonen JO, Metsälä TH, Antila KJ. Changes in autonomic cardiovascular control in mid-pregnancy. Clin Physiol. 1992;12:527-536.
28. Han X, Habuchi Y, Giles WR. Relaxin increases heart rate by modulating calcium current in cardiac pacemaker cells. Circ Res. 1994;74:537-541.
29. Bootsma M, Swenne CA, Van Bolhuis HH, Chang PC, Cats VM, Bruschke AV. Heart rate and heart rate variability as indexes of sympathovagal balance. Am J Physiol. 1994;266(4 Pt 2):H1565-H1571.
30. Rautaharju PM, Zhou SH, Wong S, Calhoun HP, Berenson GS, Prineas R, Davignon A. Sex differences in the evolution of the electrocardiographic QT interval with age. Can J Cardiol. 1992;8:690-695.
31. Peters RW, Gold MR. The infuence of gender on arrhythmias. Cardiol Rev. 2004;12:97-105.
32. Bazett H. An analysis of the time-relations of electrocardiograms. Heart. 1920;7:353-70.
33. Burke JH, Goldberger JJ, Ehlert FA, Kruse JT, Parker MA, Kadish AH. Gender differences in heart rate before and after autonomic blockade: evidence against an intrinsic gender effect. Am J Med. 1996; 100:537-543.
34. Ng AV, Callister R, Johnson DG, Seals DR. Age and gender infuence muscle sympathetic nerve activity at rest in healthy humans. Hypertension. 1993;21:498-503.
35. Fei DT, Gross MC, Lofgren JL, Mora-Worms M, Chen AB. Cyclic AMP response to recombinant human relaxin by cultured human endometrial cells-a specifc and high throughput in vitro bioassay. Biochem Biophys Res Commun. 1990;170:214-222.
36. Osheroff PL, Ling VT, Vandlen RL, Cronin MJ, Lofgren JA. Preparation of biologically active 32P-labeled human relaxin. Displaceable binding to rat uterus, cervix, and brain. J Biol Chem. 1990;265:9396-9401.
37. Moosmang S, Stieber J, Zong X, Biel M, Hofmann F, Ludwig A. Cellular expression and functional characterization of four hyperpolarization-acti-vated pacemaker channels in cardiac and neuronal tissues. Eur J Biochem. 2001;268:1646-1652.
38. Qu J, Kryukova Y, Potapova IA, Doronin SV, Larsen M, Krishnamurthy G, Cohen IS, Robinson RB. MiRP1 modulates HCN2 channel expression and gating in cardiac myocytes. J Biol Chem. 2004;279:43497-43502.
39. Altomare C, Terragni B, Brioschi C, Milanesi R, Pagliuca C, Viscomi C, Moroni A, Baruscotti M, DiFrancesco D. Heteromeric HCN1-HCN4 channels: a comparison with native pacemaker channels from the rabbit sinoatrial node. J Physiol (Lond). 2003;549(Pt 2):347-359.
40. Piot C, Lemaire S, Albat B, Seguin J, Nargeot J, Richard S. High frequency-induced upregulation of human cardiac calcium currents. Circulation. 1996;93:120-128.
41. Zingman LV, Zhu Z, Sierra A, Stepniak E, Burnett CM, Maksymov G, Anderson ME, Coetzee WA, Hodgson-Zingman DM. Exercise-induced expression of cardiac ATP-sensitive potassium channels promotes action potential shortening and energy conservation. J Mol Cell Cardiol. 2011;51:72-81.
42. Lüthi A, McCormick DA. Modulation of a pacemaker current through Ca(2+)-induced stimulation of cAMP production. Nat Neurosci. 1999;2:634-641.
43. Eghbali M, Deva R, Alioua A, Minosyan TY, Ruan H, Wang Y, Toro L, Stefani E. Molecular and functional signature of heart hypertrophy during pregnancy. Circ Res. 2005;96:1208-1216.
44. Song M, Helguera G, Eghbali M, Zhu N, Zarei MM, Olcese R, Toro L, Stefani E. Remodeling of Kv4.3 potassium channel gene expression under the control of sex hormones. J Biol Chem. 2001;276:31883-31890.
45. Clapp JF III. Maternal heart rate in pregnancy. Am J Obstet Gynecol. 1985;152(6 Pt 1):659-660.
46. Myerburg RJ, Cox MM, Interian A Jr, Mitrani R, Girgis I, Dylewski J, Castellanos A. Cycling of inducibility of paroxysmal supraventricular tachycardia in women and its implications for timing of electrophysiologic procedures. Am J Cardiol. 1999;83: 1049-1054.
47. Miyoshi H, Yamaoka K, Garfeld RE, Ohama K. Identifcation of a non-selective cation channel current in myometrial cells isolated from pregnant rats. Pfugers Arch. 2004;447:457-464.
48. Chu Z, Takagi H, Moenter SM. Hyperpolarization-activated currents in gonadotropin-releasing hormone (GnRH) neurons contribute to intrinsic excitability and are regulated by gonadal steroid feedback. J Neurosci. 2010;30:13373-13383.
49. Wu WW, Adelman JP, Maylie J. Ovarian hormone defciency reduces intrinsic excitability and abolishes acute estrogen sensitivity in hippocampal CA1 pyramidal neurons. J Neurosci. 2011;31: 2638-2648.
50. Elzwiei F, Bassien-Capsa V, St-Louis J, Chorvatova A. Regulation of the sodium pump during cardiomyocyte adaptation to pregnancy. Exp Physiol. 2013;98:183-192.