Specialized impulse conduction pathway in the alligator heart
Jazyk angličtina Země Anglie, Velká Británie Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
29565246
PubMed Central
PMC5940360
DOI
10.7554/elife.32120
PII: 32120
Knihovny.cz E-zdroje
- Klíčová slova
- American alligator, Tbx3, Ventricular septum, conduction system, developmental biology, evolution, evolutionary biology, genomics, stem cells,
- MeSH
- aligátoři a krokodýli embryologie genetika fyziologie MeSH
- embryo nesavčí metabolismus MeSH
- Hisův svazek embryologie metabolismus fyziologie MeSH
- hybridizace in situ MeSH
- mezikomorová přepážka embryologie metabolismus fyziologie MeSH
- modely kardiovaskulární MeSH
- převodní systém srdeční embryologie fyziologie MeSH
- proteiny T-boxu genetika metabolismus MeSH
- Purkyňova vlákna embryologie metabolismus fyziologie MeSH
- srdce embryologie fyziologie MeSH
- srdeční frekvence genetika fyziologie MeSH
- srdeční komory embryologie metabolismus MeSH
- vývojová regulace genové exprese MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- proteiny T-boxu MeSH
Mammals and birds have a specialized cardiac atrioventricular conduction system enabling rapid activation of both ventricles. This system may have evolved together with high heart rates to support their endothermic state (warm-bloodedness) and is seemingly lacking in ectothermic vertebrates from which first mammals then birds independently evolved. Here, we studied the conduction system in crocodiles (Alligator mississippiensis), the only ectothermic vertebrates with a full ventricular septum. We identified homologues of mammalian conduction system markers (Tbx3-Tbx5, Scn5a, Gja5, Nppa-Nppb) and show the presence of a functional atrioventricular bundle. The ventricular Purkinje network, however, was absent and slow ventricular conduction relied on trabecular myocardium, as it does in other ectothermic vertebrates. We propose the evolution of the atrioventricular bundle followed full ventricular septum formation prior to the development of high heart rates and endothermy. In contrast, the evolution of the ventricular Purkinje network is strongly associated with high heart rates and endothermy.
Department of Biological Sciences University of North Texas Denton United States
Department of Biomedical Engineering George Washington University Washington DC United States
Zobrazit více v PubMed
Aanhaanen WT, Mommersteeg MT, Norden J, Wakker V, de Gier-de Vries C, Anderson RH, Kispert A, Moorman AF, Christoffels VM. Developmental origin, growth, and three-dimensional architecture of the atrioventricular conduction axis of the mouse heart. Circulation Research. 2010;107:728–736. doi: 10.1161/CIRCRESAHA.110.222992. PubMed DOI
Alanís J, Benítez D, López E, Martínez-Palomo A. Impulse propagation through the cardiac junctional regions of the axolotl and the turtle. The Japanese Journal of Physiology. 1973;23:149–164. doi: 10.2170/jjphysiol.23.149. PubMed DOI
Arnolds DE, Liu F, Fahrenbach JP, Kim GH, Schillinger KJ, Smemo S, McNally EM, Nobrega MA, Patel VV, Moskowitz IP. TBX5 drives Scn5a expression to regulate cardiac conduction system function. Journal of Clinical Investigation. 2012;122:2509–2518. doi: 10.1172/JCI62617. PubMed DOI PMC
Burggren WW, Dubansky B, Bautista NM. 2 - Cardiovascular Development in Embryonic and Larval Fishes. In: Gamperl A. K, Gillis T. E, Farrell A. P, Brauner C. J, editors. Fish Physiology. Academic Press; 2017. pp. 107–184. DOI
Chi NC, Shaw RM, Jungblut B, Huisken J, Ferrer T, Arnaout R, Scott I, Beis D, Xiao T, Baier H, Jan LY, Tristani-Firouzi M, Stainier DY. Genetic and physiologic dissection of the vertebrate cardiac conduction system. PLoS Biology. 2008;6:e109. doi: 10.1371/journal.pbio.0060109. PubMed DOI PMC
Chiodi V, Bortolami R. The Conducting System of the Vertebrate Heart. Edizioni Calderini Bologna; 1967.
Christian E, Grigg GC. Electrical activation of the ventricular myocardium of the crocodile Crocodylus johnstoni: a combined microscopic and electrophysiological study. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology. 1999;123:17–23. doi: 10.1016/S1095-6433(99)00024-0. PubMed DOI
Chuck ET, Meyers K, France D, Creazzo TL, Morley GE. Transitions in ventricular activation revealed by two-dimensional optical mapping. The Anatomical Record. 2004;280:990–1000. doi: 10.1002/ar.a.20083. PubMed DOI
Crick SJ, Sheppard MN, Ho SY, Gebstein L, Anderson RH. Anatomy of the pig heart: comparisons with normal human cardiac structure. Journal of Anatomy. 1998;193 (Pt 1):105–119. doi: 10.1046/j.1469-7580.1998.19310105.x. PubMed DOI PMC
Davies F, Francis ET, King TS. Electrocardiogram of the crocodilian heart. Nature. 1951;167:146. doi: 10.1038/167146a0. PubMed DOI
Davies F, Francis ET, King TS. The conducting (connecting) system of the crocodilian heart. Journal of Anatomy. 1952;86:152–161. PubMed PMC
Davies F, Francis ET. The conducting system of the vertebrate heart. Biological Reviews. 1946;21:173–188. doi: 10.1111/j.1469-185X.1946.tb00323.x. PubMed DOI
Detweiler DK. The Mammalian Electrocardiogram: Comparative Features. In: Macfarlane P, van Oosterom A, Pahlm O, Kligfield P, Janse M, Camm J, editors. Comprehensive Electrocardiology. London: Springer; 2010. pp. 1909–1947. DOI
Efimov IR, Sidorov V, Cheng Y, Wollenzier B. Evidence of three-dimensional scroll waves with ribbon-shaped filament as a mechanism of ventricular tachycardia in the isolated rabbit heart. Journal of Cardiovascular Electrophysiology. 1999;10:1452–1462. doi: 10.1111/j.1540-8167.1999.tb00204.x. PubMed DOI
Farrell AP, Smith F. Cardiac form, function and physiology. Fish Physiology. 2017;36:155–264. doi: 10.1016/bs.fp.2017.07.001. DOI
Ferguson MWJ. Reproductive biology and embryology of the crocodilians. In: Gans C, Billett F, Maderson P. F. A, editors. Development A. Biology of the Reptilia. New York, Chichester, Brisbane, Toronto, Singapore: John Wiley & sons; 1985. pp. 331–491.
Gillers BS, Chiplunkar A, Aly H, Valenta T, Basler K, Christoffels VM, Efimov IR, Boukens BJ, Rentschler S. Canonical wnt signaling regulates atrioventricular junction programming and electrophysiological properties. Circulation Research. 2015;116:398–406. doi: 10.1161/CIRCRESAHA.116.304731. PubMed DOI PMC
Greil A. Beitrage zur vergelichenden anatomie und entwicklungsgeschichte des herzens und des trauncus arteriosus der wirbelthiere. MorphJahrbuch. 1903;31:123–310.
Hamburger V, Hamilton HL. A series of normal stages in the development of the chick embryo. 1951. Developmental Dynamics. 1992;195:231–272. doi: 10.1002/aja.1001950404. PubMed DOI
Heaton-Jones TG, King RR. Characterization of the Electrocardiogram of the American Alligator (Alligator mississippiensis) Journal of Zoo and Wildlife Medicine. 1994;25:40–47.
Hoogaars WM, Tessari A, Moorman AF, de Boer PA, Hagoort J, Soufan AT, Campione M, Christoffels VM. The transcriptional repressor Tbx3 delineates the developing central conduction system of the heart. Cardiovascular Research. 2004;62:489–499. doi: 10.1016/j.cardiores.2004.01.030. PubMed DOI
Houweling AC, Somi S, Massink MP, Groenen MA, Moorman AF, Christoffels VM. Comparative analysis of the natriuretic peptide precursor gene cluster in vertebrates reveals loss of ANF and retention of CNP-3 in chicken. Developmental Dynamics. 2005;233:1076–1082. doi: 10.1002/dvdy.20423. PubMed DOI
Icardo JM. Heart morphology and anatomy. Fish Physiology. 2017;36:1–54. doi: 10.1016/bs.fp.2017.05.002. DOI
Jensen B, Boukens B, Wang T, Moorman A, Christoffels V. Evolution of the sinus venosus from fish to human. Journal of Cardiovascular Development and Disease. 2014;1:14–28. doi: 10.3390/jcdd1010014. DOI
Jensen B, Boukens BJ, Postma AV, Gunst QD, van den Hoff MJ, Moorman AF, Wang T, Christoffels VM. Identifying the evolutionary building blocks of the cardiac conduction system. PLoS ONE. 2012;7:e44231. doi: 10.1371/journal.pone.0044231. PubMed DOI PMC
Jensen B, van der Wal AC, Moorman AFM, Christoffels VM. Excessive trabeculations in noncompaction do not have the embryonic identity. International Journal of Cardiology. 2017b;227:325–330. doi: 10.1016/j.ijcard.2016.11.089. PubMed DOI
Jensen B, Vesterskov S, Boukens BJ, Nielsen JM, Moorman AFM, Christoffels VM, Wang T. Morpho-functional characterization of the systemic venous pole of the reptile heart. Scientific Reports. 2017a;7:6644. doi: 10.1038/s41598-017-06291-z. PubMed DOI PMC
Keith A, Flack M. The form and nature of the muscular connections between the primary divisions of the vertebrate heart. Journal of Anatomy and Physiology. 1907;41:172–189. PubMed PMC
Koibuchi N, Chin MT. CHF1/Hey2 plays a pivotal role in left ventricular maturation through suppression of ectopic atrial gene expression. Circulation Research. 2007;100:850–855. doi: 10.1161/01.RES.0000261693.13269.bf. PubMed DOI
Laughner JI, Ng FS, Sulkin MS, Arthur RM, Efimov IR. Processing and analysis of cardiac optical mapping data obtained with potentiometric dyes. American Journal of Physiology-Heart and Circulatory Physiology. 2012;303:H753–H765. doi: 10.1152/ajpheart.00404.2012. PubMed DOI PMC
Lillywhite HB, Zippel KC, Farrell AP. Resting and maximal heart rates in ectothermic vertebrates. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology. 1999;124:369–382. doi: 10.1016/S1095-6433(99)00129-4. PubMed DOI
Mathur PN. The heart and the conducting (connecting) system of Crocodilus porosus (Schneider) The Journal of Animal Morphology and Physiology. 1971;18:84–90.
Miquerol L, Meysen S, Mangoni M, Bois P, van Rijen HV, Abran P, Jongsma H, Nargeot J, Gros D. Architectural and functional asymmetry of the His-Purkinje system of the murine heart. Cardiovascular Research. 2004;63:77–86. doi: 10.1016/j.cardiores.2004.03.007. PubMed DOI
Miquerol L, Moreno-Rascon N, Beyer S, Dupays L, Meilhac SM, Buckingham ME, Franco D, Kelly RG. Biphasic development of the mammalian ventricular conduction system. Circulation Research. 2010;107:153–161. doi: 10.1161/CIRCRESAHA.110.218156. PubMed DOI
Moorman AF, Houweling AC, de Boer PA, Christoffels VM. Sensitive nonradioactive detection of mRNA in tissue sections: novel application of the whole-mount in situ hybridization protocol. Journal of Histochemistry & Cytochemistry. 2001;49:1–8. doi: 10.1177/002215540104900101. PubMed DOI
Moskowitz IP, Pizard A, Patel VV, Bruneau BG, Kim JB, Kupershmidt S, Roden D, Berul CI, Seidman CE, Seidman JG. The T-Box transcription factor Tbx5 is required for the patterning and maturation of the murine cardiac conduction system. Development. 2004;131:4107–4116. doi: 10.1242/dev.01265. PubMed DOI
Pallante BA, Giovannone S, Fang-Yu L, Zhang J, Liu N, Kang G, Dun W, Boyden PA, Fishman GI. Contactin-2 expression in the cardiac Purkinje fiber network. Circulation: Arrhythmia and Electrophysiology. 2010;3:186–194. doi: 10.1161/CIRCEP.109.928820. PubMed DOI PMC
Park DS, Fishman GI. Development and function of the cardiac conduction system in health and disease. Journal of Cardiovascular Development and Disease. 2017;4 doi: 10.3390/jcdd4020007. PubMed DOI PMC
Reckova M, Rosengarten C, deAlmeida A, Stanley CP, Wessels A, Gourdie RG, Thompson RP, Sedmera D. Hemodynamics is a key epigenetic factor in development of the cardiac conduction system. Circulation Research. 2003;93:77–85. doi: 10.1161/01.RES.0000079488.91342.B7. PubMed DOI
Remme CA, Verkerk AO, Hoogaars WM, Aanhaanen WT, Scicluna BP, Annink C, van den Hoff MJ, Wilde AA, van Veen TA, Veldkamp MW, de Bakker JM, Christoffels VM, Bezzina CR. The cardiac sodium channel displays differential distribution in the conduction system and transmural heterogeneity in the murine ventricular myocardium. Basic Research in Cardiology. 2009;104:511–522. doi: 10.1007/s00395-009-0012-8. PubMed DOI PMC
Rentschler S, Vaidya DM, Tamaddon H, Degenhardt K, Sassoon D, Morley GE, Jalife J, Fishman GI. Visualization and functional characterization of the developing murine cardiac conduction system. Development. 2001;128:1785–1792. PubMed PMC
Smeets JL, Allessie MA, Lammers WJ, Bonke FI, Hollen J. The wavelength of the cardiac impulse and reentrant arrhythmias in isolated rabbit atrium. The role of heart rate, autonomic transmitters, temperature, and potassium. Circulation Research. 1986;58:96–108. doi: 10.1161/01.RES.58.1.96. PubMed DOI
Swett FH. The connecting systems of the reptile heart?alligator. The Anatomical Record. 1923;26:129–140. doi: 10.1002/ar.1090260207. DOI
Syme DA, Gamperl K, Jones DR. Delayed depolarization of the cog-wheel valve and pulmonary-to-systemic shunting in alligators. The Journal of Experimental Biology. 2002;205:1843–1851. PubMed
Takei Y, Inoue K, Trajanovska S, Donald JA. B-type natriuretic peptide (BNP), not ANP, is the principal cardiac natriuretic peptide in vertebrates as revealed by comparative studies. General and Comparative Endocrinology. 2011;171:258–266. doi: 10.1016/j.ygcen.2011.02.021. PubMed DOI
Tessadori F, van Weerd JH, Burkhard SB, Verkerk AO, de Pater E, Boukens BJ, Vink A, Christoffels VM, Bakkers J. Identification and functional characterization of cardiac pacemaker cells in zebrafish. PLoS ONE. 2012;7:e47644. doi: 10.1371/journal.pone.0047644. PubMed DOI PMC
Trajanovska S, Donald JA. Molecular cloning of natriuretic peptides from the heart of reptiles: loss of ANP in diapsid reptiles and birds. General and Comparative Endocrinology. 2008;156:339–346. doi: 10.1016/j.ygcen.2008.01.013. PubMed DOI
van Weerd JH, Christoffels VM. The formation and function of the cardiac conduction system. Development. 2016;143:197–210. doi: 10.1242/dev.124883. PubMed DOI
Walton RD, Bernus O. Towards depth-resolved optical imaging of cardiac electrical activity. Advances in Experimental Medicine and Biology. 2015;859:405–423. doi: 10.1007/978-3-319-17641-3_16. PubMed DOI
Wang Z-X, Sun N-Z, Mao W-P, Chen J-P, Huang G-Q. An analysis of electrocardiogram of alligator sinensis. Comparative Biochemistry and Physiology Part A: Physiology. 1991;98:89–95. doi: 10.1016/0300-9629(91)90582-W. DOI
Hemodynamics During Development and Postnatal Life
Low incidence of atrial septal defects in nonmammalian vertebrates
Trabecular Architecture Determines Impulse Propagation Through the Early Embryonic Mouse Heart