Morphological features of atrial myocardium embryonic development and its changes caused by hypoxia effect

Keywords: cardiogenesis; atria; ultrastructure of cardiomyocytes; rats.

Abstract

Mortality and morbidity during the prenatal period of development remain a real problem at the present time. The Scientific Committee EURO-PERISTAT has revealed that mortality of fetuses associated with congenital abnormalities is on average 15–20% across Europe. Hypoxia is one of the top causes of death of fetuses. Since the heart begins to function before birth, influence of teratogenic factors leads to formation of anomalies of its development. Congenital heart defects are the most common of these and occur with a frequency of 24%. Abnormalities associated with the atrium occur with frequency of 6.4 per 10,000 cases. Investigation of structural changes of the atrial myocardium is a key for understanding of pathogenic mechanisms of cardiovascular diseases that are caused by influence of hypoxia. Nowadays, a great deal of research is being dedicated to normal cardiogenesis and much less work is focused on abnormal heart development. There are numerous teratogenic factors such as alcohol, retinoic acid, hyperthermia, hypoxia that are most common causes of heart diseases. The attention of researchers has been predominantly focused on study of changes of the ventricular myocardium under the effect of hypoxia. It is known that the atrium is different from the ventricles by derivation, development and structure. Therefore, the effects of pathological factors on the atrial myocardium will be different as complared to their effect on the ventricles. Also, almost all research has focused on study of consequences of hypoxia at the late stages of cardiogenesis. However, the greatest number of abnormalities is associated with the early embryonic period, as structures that continue development are more sensitive to the effects of harmful factors. Thus, comparative analysis of scientific research devoted to morphological study of atrial myocardium transformations on the cellular and ultrastructural levels under the influence of hypoxia during the stages of cardiogenesis is an important task.

References

Altimiras, J., & Phu, L. (2000). Lack of physiological plasticity in the early chi cken embryo exposed to acute hypoxia. The Journal of Experimental Zoology, 286(5), 450–456.

Antonova, L. V., Matveeva, V. G., & Ponasenko, A. V. (2012). Izmenenie proli ferativnoj aktivnosti i zhiznesposobnosti endotelial'nyh kletok cheloveka v uslovijah gipoksii i posledujushhej re-oksigenacii [Changes of proliferative activity and viability of human endothelial cells under hypoxia and further re-oxygenation]. Fundamentalnye Issledovanija, 7, 273–277 (in Russian).

Araujo Júnior, E., Rolo, L. C., Rocha, L. A., Machado Nardozz, L. M., & Moron, A. F. (2014). The value of 3D and 4D assessments of the fetal heart. Interna tional Journal of Women's Health, 6, 501–507.

Arjamaa, O., & Nikinmaa, M. (2011). Hypoxia regulates the natriuretic peptide system. International Journal of Physiology, Pathophysiology and Pharmaco logy, 3(3), 191–201.

Azar, N., Nasser, M., Sabban, M. E., Bitar, H., Obeid, M., Dbaibo, G. S., & Bitar, F. F. (2003). Cardiac growth patterns in response to chronic hypoxia in a neo natal rat model mimicking cyanotic heart disease. Experimental and Clinical Cardiology, 8(4), 189–194.

Bhattacharya, S., Macdonald, S. T., & Farthing, C. R. (2006). Molecular mecha nisms controlling the coupled development of myocardium and coronary vasculature. Clinical Science, 111, 35–46.

Bogers, A. J., Gittenberger-de Groot, A. C., Poelmann, R. E., Péault, B. M., & Huysmans, H. A. (1989). Development of the origin of the coronary arteries, a matter of ingrowth or outgrowth. Anatomy and Embryology, 180, 437–441.

Breckenridge, R. A., Piotrowska, I., Ng, K. E., Ragan, T. J., West, J. A., Kotech, S., Towers, N., Bennett, M., Kienesberger, P. C., Smolenski, R. T., Siddall, H. K., Offer, J. L., Mocanu, M. M., Yelon, D. M., Dyck, J. R., Griffin, J. L., Abramov, A. Y., Gould, A. P., & Mohun, T. J. (2013). Hypoxic regulation of hand 1 con trols the fetal-neonatal switch in cardiac metabolism. PLoS Biology, (9), 1–11.

Bruneau, B. G. (2003). The developing heart and congenital heart defects: A make or break situation. Clinical Genetics, 63(4), 252–261.

Bugrova, M. L., Yakovleva, E. I., & Abrosimov, D. A. (2012). Vzaimosvjaz' in tensivnosti sinteza, nakoplenija i sekrecii predserdnogo natrijureticheskogo peptida kardiomiocitov s urovnem reguljacii serdechnogo ritma u krys v uslovijah rannego postper-fuzionnogo perioda [Correlation of intensity of synthesis, accumulation and secretion of atrial natriuretic peptide in cardio myocyte with level of heart rate regulation in rats during the early post-perfusion period]. Biomedicinskie Issledovanija, 3, 26–29 (in Russian).

Casserly, B., Pietras, L., Schuyler, J., Wang, R., Hill, N. S., & Klinger, J. R. (2010). Cardiac atria are the primary source of ANP release in hypoxia adapted rats. Life Sciences, 87(11–12), 382–389.

Chan, T., & Burggren, W. (2005). Hypoxic incubation creates differential mor phological effects during specific developmental critical windows in the embryo of the chicken (Gallus gallus). Respiratory, Physiology and Neuro biology, 145(2–3), 251–263.

Christoffels, V. M., Habets, P. E., Franco, D., Campione, M., de Jong, F., Lamers, W. H., Bao, Z. Z., Palmer, S., Biben, C., Harvey, R. P., & Moorman, A. F. (2000). Chamber formation and morphogenesis in the developing mamma lian heart. Developmental Biology, 223(2), 266–278.

Clément, S., Stouffs, M., Bettiol, E., Kampf, S., Krause, K. H., Chaponnier, C., & Jaconi, M. (2007). Expression and function of alpha-smooth muscle actin du ring embryonic-stem-cell-derived cardiomyocyte differentiation. Journal of Cell Science, 120, 229–238.

Clerico, A., Giannoni, A., Vittorini, S., & Passino, C. (2011). Thirty years of the heart as an endocrine organ: Physiological role and clinical utility of cardiac natriuretic hormones. American Journal of Physiology. Heart and Circulatory Physiology, 301(1), 12–20.

Cury, D. P., Dias, F. J., Sosthenes, M. C., Dos Santos Haemmerle, C. A., Ogawa, K., Da Silva, M. C., Mardegan Issa, J. P., Iyomasa, M. M., & Watanabe, I. S. (2013). Morphometric, quantitative, and three-dimensional analysis of the heart muscle fibers of old rats: Transmission electron microscopy and high-resolution scanning electron microscopy methods. Microscopy Research and Technique, 6(2), 184–195.

de Bold, A. J. (2011). Thirty years of research on atrial natriuretic factor: Historical background and emerging concepts. Canadian Journal of Physiology and Pharmacology, 89(8), 527–531.

Dong, Y., & Thompson, L. P. (2006). Differential expression of endothelial nitric oxide synthase in coronary and cardiac tissue in hypoxic fetal guinea pig hearts. Journal of the Society for Gynecologic Investigation, 13(7), 483–490.

Elmstedt, N. N., Johnson, J. J., Lind, B. B., Ferm-Widlund, K. K., Herling, L. L., Westgren, M. M., & Brodin, L. Å. (2013). Reference values for fetal tissue velocity imaging and a new approach to evaluate fetal myocardial function. Cardiovascular Ultrasound, 16(11), 29.

European Society of Gynecology (ESG), Association for European Paediatric Cardiology (AEPC), German Society for Gender Medicine (DGesGM), Regitz-Zagrosek, V., Blomstrom Lundqvist, C., Borghi, C., Cifkova, R., Ferreira, R., Foidart, J. M., Gibbs, J. S., Gohlke-Baerwolf, C., Gorenek, B., Iung, B., Kirby, M., Maas, A. H., Morais, J., Nihoyannopoulos, P., Pieper, P. G., Presbitero, P., Roos-Hesselink, J. W., Schaufelberger, M., Seeland, U., & Torracca, L. (2011). ESC Committee for Practice Guidelines. ESC Guideli nes on the management of cardiovascular diseases during pregnancy: The task force on the management of cardiovascular diseases during pregnancy of the European Society of Cardiology (ESC). European Heart Journal, 32(24), 3147–3197.

Fujii, Y., Ishino, K., Tomii, T., Kanamitsu, H., Fujita, Y., Mitsui, H., & Sano, S. (2011). Atrionatriuretic peptide improves left ventricular function after myo cardial global ischemia-reperfusion in hypoxic hearts. Artifical Organs, 36(4), 379–386.

Gama, E. F., de Carvalho, C. A., Liberti, E. A., & de Souza, R. R. (2007). Atrial natriuretic peptide (ANP)-granules in the guinea pig atrial and auricular cardiocytes: An immunocytochemical and ultrastructural morphometric com parative study. Annals of Anatomy, 189, 457–464.

Gilbert, S. H., Benoist, D., Benson, A. P., White, E., Tanner, S. F., Holden, A. V., Dobrzynski, H., Bernus, O., & Radjenovic, A. (2012). Visualization and quan tification of whole rat heart laminar structure using high-spatial resolution contrast-enhanced MRI. American Journal of Physiology. Heart and Circu latory Physiology, 302(1), H287–H298.

Gindes, L., Matsui, H., & Achiron, R. (2012). Comparison of ex-vivo high-resolu tion episcopic microscopy with in-vivo four-dimensional high-resolution transvaginal sonography of the first-trimester fetal heart. Ultrasound in Obs tetrics and Gynecoly, 39(2), 196–202.

Gittenberger-de Groot, A. C., Bartelings, M. M., Deruiter, M. C., & Poelmann, R. E. (2005). Basics of cardiac development for the understanding of congenital heart malformations. Pediatric Researches, 57(2), 169–176.

Giussani, D. A., Camm, E. J., Niu, Y., Richter, H. G., Blanco C. E., Gottschalk, R., Blake, E. Z., Horder, K. A., Thakor, A. S., Hansell, J. A., Kane, A. D., Wooding, F. B., Cross, C. M., & Herrera, E. A. (2012). Developmental prog ramming of cardiovascular dysfunction by prenatalhypoxia and oxidative stress. PLoS One, 7(2), 310–317.

Giussani, D. A., Niu, Y., Herrera, E. A., Richter, H. G., Camm, E. J., Thakor, A. S., Kane, A. D., Hansell, J. A., Brain, K. L., Skeffington, K. L., Itani, N., Wooding, F. B., Cross, C. M., & Allison, B. J. (2014). Heart disease link to fetal hypoxia and oxidative stress. Advances in Experimental Medicine and Biology, 814, 77–87.

Goenezen, S., Rennie, M. Y., Rugonyi, S. N. (2012). Biomechanics of early cardiac development. Biomechanical Modelling Mechanobiology, 11(8), 1187–1204.

Goodlett, T. (2011). The volumetric analysis of cardiac chambers and three-di mensional cardiac reconstruction during chicken embryo cardiogenesis. Mor phologia, 5(2), 39–44.

Gössl, M., Zamir, M., & Ritman, E. L. (2004). Vasa vasorum growth in the coro nary arteries of newborn pigs. Anatomy and Embryology, 208(5), 351–357.

Gu Shi, Jenkins, M. W., & Peterson, L. M. (2012). Optical сoherence tomography captures rapid hemodynamic responses to acute hypoxia in the cardiovascu lar system of early embryos. Developmental Dynamics, 241(3), 534–544.

Hernandez-Andrade, E., Benavides-Serralde, J. A., Cruz-Martinez, R., Welsh, A., & Mancilla-Ramirez, J. (2012). Evaluation of conventional Doppler fetal cardiac function parameters: E/A ratios, outflow tracts, and myocardial per formance index. Fetal Diagnosis and Therapy, 32(1–2), 22–29.

Hongmei, W., Ying, Z., Ailu, C., & Wei, S. (2012). Novel application of four-di mensional sonography with B-flow imaging and spatiotemporal image cor relation in the assessment of fetal congenital heart defects. Echocardiography (Mount Kisco, N.Y.), 29(5), 614–619.

Hutchins, G. M., Kessler-Hanna, A., & Moore, G. W. (1988). Development of the coronary arteries in the embryonic human heart. Circulation, 77(6), 1250–1257.

Jacob, M., Saller, T., Chappell, D., Rehm, M., Welsch, U., & Becker, B. F. (2013). Physiological levels of A-, B- and C-type natriuretic peptide shed the endo thelial glycocalyx and enhance vascular permeability. Basic Research in Car diology, 108(3), 347.

Jopling, C., Suñé, G., Faucherre, A., Fabregat, C., & Izpisua Belmonte, J. C. (2012). Hypoxia induces myocardial regeneration in zebrafish. Circulation, 126, 3017–3027.

Klotz, L., Norman, S., Vieira, J. M., Masters, M., Rohling, M., Dubé, K. N., Bollini, S., Matsuzaki, F., Carr, C. A., & Riley, P. R. (2014). Cardiac lymphatics are heterogeneous in origin and respond to injury. Nature, 522(7554), 62–67.

Knaapen, M. W., Vrolijk, B. C., & Wenink, A. C. (1997). Ultrastructural changes of the myocardium in the embryonic rat heart. The Anatomical Record, 248(2), 233–262.

Kobayashi, T., Maeda, S., Ichise, N., Sato, T., Iwase, T., Seki, S., Yamada, Y., & Tohse, N. (2011). The beginning of the calcium transient in rat embryonic heart. The Journal of Physiological Sciences, 61(2), 141–149.

Korostyshevskaya, I. M., & Maksimov, V. F. (2013). Vozrastnye osobennosti miojendokrinnyh kletok serdca u krys v norme i pri nasledstvennoj giperten zii [Age features of myoendocrine heart cells of rats in normal and hereditary hypertension]. Ontogenez, 44(2), 1–13 (in Russian).

Korostyshevskaya, I. M., Maksimov, V. F., & Kurganov, S. A. (2013). Vozmozh nosti ul'trastrukturnoj ocenki sekretornoj aktivnosti predserdnyh kardiomioci tov [Сapability of ultrastructural assessment of atrial cardiomyocyte secretory activity]. Citologija, 55(8), 539–547 (in Russian).

Kozlov, V. A., Tverdohleb, I. V., Shponka, I. S., & Mishalov, V. D. (1995). Mor fologiya razvivayushhegosya serdca (struktura, ultrastruktura, metabolizm) [Morphology of the developing heart (structure, ultrastructure, metabolism)]. Dnepropetrovsk (in Russian).

Kuhn, M. (2012). Endothelial actions of atrial and B-type natriuretic peptides. British Journal of Pharmacology, 166(2), 522–531.

Lamers, W. H., & Moorman, A. F. (2002). Cardiac septation: A late contribution of the embryonic primary myocardium to heart morphogenesis. Circulation Research, 91(2), 93–103.

Lockhart, M., Wirrig, E., & Phelps, A. (2011). Extracellular matrix and heart de velopment. Birth defects research. Part A, Clinical and Molecular Teratology, 91(6), 535–550.

Maksimov, V. F., & Korostyshevskaya, I. M. (2012). Morfogenez i reakcija na gipoksiju miojendokrinnyh kletok predserdija u kurinyh jembrionov (Gallus gallus) [Morphogenesis and reaction to hypoxia of myoendocrine cells of atria of chicken embryos (Gallus gallus)]. Zhurnal Evoljucionnoj Biohimii i Fiziologii, 48(5), 502–508 (in Russian).

Maksimov, V. F., Korostyshevskaya, I. M., & Markel, A. I. (2013). Natryjurety cheskye peptydy serdca y arteryal'naja gypertenzyja: Eksperymental'noe issledovanye [Natriuretic peptides of the heart and arterial hypertension: An experimental study]. Vestnik RAMN, 1, 4–9.

Marei, H. E. (2002). Fine structural and immunohistochemical localization of car diac hormones (ANP) in ringht atrium and hypothalamus of the white rat. European Journal of Morphology, 40, 37–41.

Mashtalir, M. A., & Tverdokhlib, I. V. (2007). Normal'nyj ta anomal'nyj kardioge nez: Uchast' pozasercevyh klitynnyh populjacij [Normal and abnormal car diogenesis: Participation of extracardiac cell populations]. Morphology, 1(1), 84–88 (in Ukrainian).

Matsui, H., Mohun, T., & Gardiner, H. M. (2009). Three-dimensional reconstruc tion imaging of the human foetal heart in the first trimester. European Heart Journal, 31(4), 415.

McCutcheon, I. E., Metcalfe, J., Metzenberg, A. B., & Ettinger, T. (1982). Organ growth in hyperoxic and hypoxic chick embryos. Respiration Physiology, 50(2), 153–163.

McKenzie, J. C., Kelley, K. B., Merisko-Liversidge, E. M., Kennedy, J., & Klein, R. M. (1994). Developmental pattern of ventricular atrial natriuretic peptide (ANP) expression in chronically hypoxic rats as an indicator of the hypertro phic process. Journal of Molecular and Cellular Cardiology, 26(6), 753–767.

Momoi, N., Tinney, J. P., Keller, B. B., & Tobita, K. (2012). Maternal hypoxia and caffeine exposure depress fetal cardiovascular function during primary organogenesis. The Journal of Obstetrics and Gynaecology Research, 38(12), 1343–1351.

Muñoz-Chápuli, R., González-Iriarte, M., Carmona, R., Atencia, G., Macías, D., & Pérez-Pomares, J. M. (2002). Cellular precursors of the coronary arteries. Texas Heart Institute Journal, 29, 243–249.

Nesbitt, T., Lemley, A., Davis, J., Yost, M. J., Goodwin, R. L., & Potts, J. D. (2006). Epicardial development in the rat: A new perspective. Microscopy and Microanalysis, 12, 390–398.

Nichols, M., Townsend, N., Luengo-Fernandez, R., Leal, J., Graj, A., Scarborough, P., & Rayner, M. (2012). European cardiovascular disease statistics 2012. European Heart Network, Brussels, European Society of Cardiology, Sophia Antipolis.

Nieman, B. J., & Turnbull, D. H. (2010). Ultrasound and magnetic resonance microimaging of mouse development. Methods in Enzymology, 476, 379–400.

Oxford, E. M., Danko, C. G., Kornreich, B. G., Maass, K., Hemsley, S. A., Ras kolnikov, D., Fox, P. R., Delmar, M., & Moïse, N. S. (2011). Ultrastructural changes in cardiac myocytes from Boxer dogs with arrhythmogenic right ventricular cardiomyopathy. Journal of Veterinary Cardiology, 13(2), 101–113.

Patterson, A. J., & Zhang, L. (2010). Hypoxia and fetal heart development. Current Molecular Medicine, 10(7), 653–666.

Pires-Gomes, A. A. S., & Pérez-Pomares, J. M. (2013). The epicardium and artery formation. Journal Development Biology, 1, 186–202.

Porter, G. A., Hom, J., Hoffman, D., Quintanilla, R., de Mesy Bentley, K., & Sheu, S. S. (2011). Bioenergetics, mitochondria, and cardiac myocyte differentiation. Pro gress in Pediatric, 31(2), 75–81.

Price, R. L., Chintanowonges, C., Shiraishi, I., Borg, T. K., & Terracio, L. (1996). Local and regional variations in myofibrillar patterns in looping rat hearts. The Anatomical Record, 245(1), 83–93.

Ratajska, A., Ciszek, B., & Sowińska, A. (2003). Embryonic development of co ronary vasculature in rats: Corrosion casting studies. The Anatomical Record. Part A, Discoveries in Molecular, Cellular, and Evolutionary Biology, 270(2), 109–116.

Raxcheeva, M. V., & Bugrova, M. L. (2010). Izmenenie sootnoshenija granul A- i B-tipov, soderzhashhih predserdnyj i mozgovoj natrijureticheskie peptidy, v predserdnyh miocitah krys v uslovijah vazorenal'noj gipertenzii [Change in correlation of A- and B-type granules containing atrial and brain natriuretic peptides in atrial rat myocytes under conditions of renovascular hypertensi on]. Citologija, 52(8), 629–633 (in Russian).

Ream, M., Ray, A. M., Chandra, R., & Chikaraishi, D. M. (2008). Early fetal hy poxia leads to growth restriction and myocardial thinning. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology, 295(2), 583–595.

Rook, W., Johnson, C. D., Coney, A. M., & Marshall, J. M. (2014). Prenatal hy poxia leads to increased muscle sympathetic nerve activity, sympathetic hyper innervation, premature blunting of neuropeptide Y signaling, and hyperten sion in adult life. Hypertension, 64(6), 1321–1327.

Ruckman, R. N., Rosenquist, G. C., Rademaker, D. A., Morse, D. E., & Getson, P. R. (1985). The effect of graded hypoxia on the embryonic chick heart. Te ratology, 32(3), 463–472.

Saiki, Y., Konig, A., Waddell, J., & Rebeyka, I. M. (1997). Hemodynamic altera tion by fetal surgery accelerates myocyte proliferation in fetal guinea pig hearts. Surgery, 122(2), 412–419.

Samsa, L. A., Yang, B., & Liu, J. (2013). Embryonic cardiac chamber maturation: trabeculation, conduction, and cardiomyocyte proliferation. American Journal of Medical Genetics. Part C, Seminars in Medical Genetics, 163(3), 157–168.

Schaper, J., Meiser, E., & Stämmler, G. (1985). Ultrastructural morphometric ana lysis of myocardium from dogs, rats, hamsters, mice, and from human hearts. Circulation Research, 56(3), 377–391.

Schell, M. T., Spitzer, A. L., Johnson, J. A., Lee, D., & Harris, H. W. (2005). Heat shock inhibits NF-kB activation in a dose- and time-dependent manner. The Journal of Surgical Sesearch, 129(3), 90–93.

Schleich, J. M., Dillenseger, J. L., Loeuillet, L., Moulinoux, J. P., & Almange, C. (2005). Three-dimensional reconstruction and morphologic measurements of human embryonic hearts: a new diagnostic and quantitative method appli cable to fetuses younger than 13 weeks of gestation. Pediatric and Develop mental Pathology, 8(4), 463–473.

Schotten, U., Verheule, S., Kirchhof, P., & Goette, A. (2011). Pathophysiological mechanisms of atrial fibrillation: A translationalappraisal. Physiological Reviews, 91, 265–325.

Sergeeva, I. A., Hooijkaas, I. B., Van Der Made, I., Jong, W. M., Creemers, E. E., & Christoffels, V. M. (2014). A transgenic mouse model for the simultaneous monitoring of ANF and BNP gene activity during heart development and disease. Cardiovascular Research, 101(1), 78–86.

Shatorna, V. F., Shponka, I. S., Abdul-Ohly, L. V., & Savenkova, O. O. (2010). Krytychni periody kardiohenezu [Critical periods of cardiogenesis]. Porohy, Dnipropetrovsk (in Ukrainian).

Shevchenko, K. M., & Tverdokhlib, I. V. (2012). Ontogenetychni osoblyvosti sekretornogo aparatu peredserdnogo miokarda shhuriv [Ontogenetic features of the secretory apparatus of the atrial myocardium in rats]. Morphology, 6(3), 72–77 (in Ukrainian).

Shponka, I. S. (1996). Gistogeneticheskie processy v razvivayushhemsya miokarde mlekopitayushhih [Histogenetic processes in the developing mammalian myocardium]. Porogi, Dnepropetrovsk (in Russian).

Silkina, Y. V. (2010). Gistogenetychni peretvorennja providnoi' systemy sercja [His togenetic transformation of conducting system ofthe heart]. Morphology, 4(3), 50–66 (in Ukrainian).

Sugishita, Y., Leifer, D. W., Agani, F., Watanabe, M., & Fisher, S. A. (2004). Hy poxia-responsive signaling regulates the apoptosis-dependent remodeling of the embryonic avian cardiac outflow tract. Developmental Biology, 273(2), 285–296.

Takei, Y., Inoue, K., Trajanovska, S., & Donald, J. A. (2011). B-type natriuretic peptide (BNP), not ANP, is the principal cardiac natriuretic peptide in verteb rates as revealed by comparative studies. General and Comparative Endocri nology, 171, 258–266.

Tobón, C., Ruiz-Villa, C. A., Heidenreich, E., Romero, L, Hornero, F., & Saiz, J. (2013). A three-dimensional human atrial model with fiber orientation. Electro grams and arrhythmic activation patterns relationship. PLoS One, 8(2), e50883.

Tomanek, R, J., & Zheng, W. (2002). Role of growth factors incoronary morpho genesis. Texas Heart Institute Journal, 29(4), 250–254.

Tomanek, R. J., Haung, L., Suvarna, P. R., O'Brien, L. C., Ratajska, A., & Sandra, A. (1996). Coronary vascularization during development in the rat and its rela tionship to basic fibroblast growth. Cardiovascular Researches, 31, 116–126.

Tomanek, R. J., Ratajska, A., Kitten, G. T., Yue, X., & Sandra, A. (1999). Vascular endothelial growth factor expression coincideswith coronary vasculogenesis and angiogenesis. Developmental Dynamics, 215(1), 54–61.

Tong, W., Xiong, F., Li, Y., & Zhang, L. (2013). Hypoxia inhibits cardiomyocyte proliferation in fetal rat hearts via upregulating TIMP-4. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology, 304(8), 613–620.

Tong, W., Xue, Q., Li, Y., & Zhang, L. (2011). Maternal hypoxia alters matrix metalloproteinase expression patterns and causes cardiac remodeling in fetal and neonatal rats. American Journal of Physiology. Heart and Circulatory Physiology, 301(5), 2113–2121.

Tonne, J. M., Campbell, J. M., Cataliotti, A., Ohmine, S., Thatava, T., Sakuma, T., Macheret, F., Huntley, B. K., Burnett, J. C., & Ikeda, Y. (2011). Secretion of glycosylated pro-B-type natriuretic peptide from normal cardiomyocytes. Clinical Chemistry, 57(6), 864–873.

Tverdokhlib, I. V. (2007). Prostorova rekonstrukcija biologichnyh ob'jektiv za dopo mogoju komp'juternogo modeljuvannja [Dimensional reconstruction of biologi cal objects using computer modeling]. Morphology, 1(1), 135–139 (in Ukrainian).

Wilhide, M. E., Tranter, M., Ren, X., Chen, J., Sartor, M. A., Medvedovic, M., & Jones, W. K. (2011). Identification of a NF-κB cardioprotective gene program: NF-κB regulation of Hsp70.1 contributes to cardioprotection after permanent coronary occlusion. Journal of Molecular and Cellular Cardiology, 51(1), 82–89.

Writing Committee, Smith, S.C., Collins, A., Ferrari, R., Holmes, D. R., Logstrup, S., McGhie, D. V., Ralston, J., Sacco, R. L., Stam, H., Taubert, K., Wood, D. A., & Zoghbi, W. A. (2012). Our time: A call to save preventable death from cardiovascular disease (heart disease and stroke). Global Heart, 60, 2343–2348.

Yu, J., Zhu, M. Z., Cheng, B. Y., Lu, S. Y., & Dong, M. Q. (2003). Study on the mechanism of how vasonatrin peptide can attenuate the growth-promoting effect of hypoxia in cardiac fibroblast. Zhongguo Ying Yong Sheng Li Xue Za Zhi i. Chinese Journal of Applied Physiology, 19(1), 8–11.

Yunge, L., Ballak, M., Beuzeron, J., Lacasse, J., & Cantin, M. (1980). Ultrastructural cytochemistry of atrial and ventricular cardiocytes of the bullforg. Relationship of specific granules with reninlike activity of the myocardium. Canadian Journal of Physiology and Pharmacology, 58, 1463–1476.

Zadnipryanyj, I. V., & Tretyakova, O. S. (2011). Strukturnaja perestrojka miokarda pri perinatal'noj gipoksii v uslovijah jeksperimenta [Structural remodeling of myocardum during perinatal hypoxia under experimental conditions]. Crimean Journal of Experimental and Clinical Medicine, 1(1), 40–45 (in Russian).

Zhang, F., & Pasumarthi, K. B. (2007). Ultrastructural and immunocharacterization of undifferentiated myocardial cells in the developing mouse heart. Journal of Cellular and Molecular Medicine, 11(3), 552–560.

Zhang, W., Chen, H., Qu, X., Chang, C. P., & Shou, W. (2005). Myocardial hete rogeneity in permissiveness for epicardium-derived cells and endothelial pre cursor cells along the developing heart tube at the onset of coronary vascula rization. American Journal of Medical Genetics, 282(2), 120–129.

Zhang, W., Chen, H., Qu, X., Chang, C. P., & Shou, W. (2013). Molecular mec hanism of ventricular trabeculation/compaction and the pathogenesis of the left ventricular noncompaction cardiomyopathy (LVNC). American Journal of Medical Genetics. Part C, Seminars in Medical Genetics, 163(3), 144–156.

Published
2019-03-18
How to Cite
Shevchenko, K. M. (2019). Morphological features of atrial myocardium embryonic development and its changes caused by hypoxia effect . Regulatory Mechanisms in Biosystems, 10(1), 129-135. https://doi.org/10.15421/021920