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Вестник Московского университета. Серия 16. Биология

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Молекулярные механизмы онтогенеза ритмоводителя сердца у позвоночных животных

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Аннотация

Небольшая группа миокардиальных клеток, формирующая естественный доминирующий пейсмекер (ритмоводитель) сердца в т.н. синоатриальном узле (САУ), обеспечивает автоматическую ритмическую работу сердца животных, включая человека, на протяжении всей жизни. Для пейсмекера сердца характерна специфическая гистологическая организация, особый паттерн экспрессии множества генов, определяющих электрофизиологический фенотип составляющих его кардиомиоцитов. Функциональное созревание пейсмекера сердца происходит в ходе всего эмбрионального периода развития, начиная с самых ранних стадий. Понимание закономерностей происхождения ритмоводителя сердца и молекулярных механизмов, контролирующих его развитие, приближает к созданию искусственных биологических пейсмекеров, осмыслению причин формирования многих сердечно-сосудистых патологий, в особенности – генетически обусловленных, связанных с дефектами развития, или приобретенных нарушений ритма сердца. Исследование эмбриогенеза САУ способствует решению проблемы репрограммирования кардиомиоцитов или соматических клеток с целью клеточной терапии при сердечно-сосудистых заболеваниях, реверсии ремоделирования миокарда. К настоящему времени достигнут значительный прогресс в понимании генетических и молекулярных путей, определяющих идентичность пейсмекерных клеток и управляющих формированием доминирующего пейсмекера сердца в ходе онтогенеза. В данном обзоре приведены сведения о ключевых группах транскрипционных факторов, молекулярных регуляторных каскадах (белков BMP, Wnt, Wt1, Slit/Robo, RhoA, подопланин, VEGF, PDGF), участвующих в (эпи)генетическом контроле развития пейсмекерных кардиомиоцитов и определении их электрофизиологического фенотипа.

Об авторах

В. С. Кузьмин
Московский государственный университет имени М.В. Ломоносова
Россия

Кузьмин Владислав Стефанович – канд. биол. наук, доц. кафедры физиологии человека и животных биологического факультета

19234, г. Москва, ул. Ленинские горы, д. 1, стр. 12

Тел.: 8-495-939-14-16



А. А. Каменский
Московский государственный университет имени М.В. Ломоносова
Россия

Каменский Андрей Александрович – докт. биол. наук, зав. кафедрой физиологии человека и животных биологического факультета

19234, г. Москва, ул. Ленинские горы, д. 1, стр. 12

Тел.: 8-495-939-14-16



Список литературы

1. Souza D.S., Barreto T. de O., Santana M.N.S., Menezes-Filho J.E., Cruz J.S., Vasconcelos C.M. Resident macrophages orchestrating heart rate // Arq. Bras. Cardiol. 2019. Vol. 112. N 5. P. 588–591.

2. Faber J.W., Boukens B.J., Oostra R.J., Moorman A.F., Christoffels V.M., Jensen B. Sinus venosus incorporation: contentious issues and operational criteria for developmental and evolutionary studies // J. Anat. 2019. Vol. 234. N 5. P. 583–591.

3. van Eif V.W.W., Stefanovic S., van Duijvenboden K., Bakker M, Wakker V, de Gier-de Vries C., Zaffran S., Verkerk A.O., Boukens B.J., Christoffels V.M. Transcriptome analysis of mouse and human sinoatrial node cells reveals a conserved genetic program // Dev. 2019. Vol. 146. N 8: dev173161.

4. Sizarov A., Devalla H.D., Anderson R.H., Passier R., Christoffels V.M., Moorman A.F. Molecular analysis of patterning of conduction tissues in the developing human heart // Circ. Arrhythmia Electrophysiol. 2011. Vol. 4. N 4. P. 532–542.

5. Burdsal C.A., Damsky C.H., Pedersen R.A. The role of E-cadherin and integrins in mesoderm differentiation and migration at the mammalian primitive streak // Dev. 1993. Vol. 118. N 3. P. 829–844.

6. Cai W., Guzzo R.M., Wei K., Willems E., Davidovics H., Mercola M. A Nodal-to-TGFβ cascade exerts biphasic control over cardiopoiesis // Circ. Res. 2012. Vol. 111. N 7. P. 876–881.

7. Mazzotta S., Neves C., Bonner R.J., Bernardo A.S., Docherty K., Hoppler S. Distinctive roles of canonical and noncanonical Wnt signaling in human embryonic cardiomyocyte development // Stem cell reports. 2016. Vol. 7. N 4. P. 764–776.

8. Steinhart Z., Angers S. Wnt signaling in development and tissue homeostasis // Dev. 2018. Vol. 145. N 11: dev146589.

9. Zaffran S., Frasch M. Early signals in cardiac development // Circ. Res. 2002. Vol. 91. N 6. P. 457–469.

10. Ciruna B., Rossant J. FGF signaling regulates mesoderm cell fate specification and morphogenetic movement at the primitive streak // Dev. Cell. 2001. Vol. 1. N 1. P. 37–49.

11. Moorman A.F.M., Christoffels V.M., Anderson R.H., van den Hoff M.J. The heart-forming fields: One or multiple? // Philos. Trans. R. Soc. B Biol. Sci. 2007. Vol. 362. N 1484. P. 1257–1265.

12. Stalsberg H., DeHaan R.L. The precardiac areas and formation of the tubular heart in the chick embryo // Dev. Biol. 1969. Vol. 19. N 2. P. 128–159.

13. Tyser R.C., Miranda A.M., Chen C.-M., Davidson S.M., Srinivas S., Riley P.R. Calcium handling precedes cardiac differentiation to initiate the first heartbeat // Elife. 2016. Vol. 5: e17113.

14. Patten B.M. Initiation and early changes in the character of the heart beat in vertebrate embryos // Physiol. Rev. 1949. Vol. 29. N 1. P. 31–47.

15. Forouhar A.S., Liebling M., Hickerson A., NasiraeiMoghaddam A., Tsai H.J., Hove J.R., Fraser S.E., Dickinson M.E., Gharib M. The embryonic vertebrate heart tube is a dynamic suction pump // Science. 2006. Vol. 312. N 5774. P. 751–753.

16. Van Mierop L.H. Location of pacemaker in chick embryo heart at the time of initiation of heartbeat // Am. J. Physiol. 1967. Vol. 212. N 2. P. 407–415.

17. Groot A.C.G., Bartelings M.M., Poelmann R.E., Haak M.C., Jongbloed M.R. Embryology of the heart and its impact on understanding fetal and neonatal heart disease // Semin. Fetal Neonatal Med. 2013. Vol. 18. N 5. P. 237–244.

18. Später D., Abramczuk M.K., Buac K., Zangi L., Stachel M.W., Clarke J., Sahara M., Ludwig A., Chien K.R. A HCN4+ cardiomyogenic progenitor derived from the first heart field and human pluripotent stem cells // Nat. Cell Biol. 2013. Vol. 15. N 9. P. 1098–1106.

19. Garcia-Frigola C., Shi Y., Evans S.M. Expression of the hyperpolarization-activated cyclic nucleotide-gated cation channel HCN4 during mouse heart development // Gene Expr. Patterns. 2003. Vol. 3. N 6. P. 777–783.

20. Christoffels V.M., Mommersteeg M.T.M., Trowe M.-O., Prall O.W., de Gier-de Vries C., Soufan A.T., Bussen M., Schuster-Gossler K., Harvey R.P., Moorman A.F., Kispert A. Formation of the venous pole of the heart from an Nkx2-5negative precursor population requires Tbx18 // Circ. Res. 2006. Vol. 98. N 12. P. 1555–1563.

21. DiFrancesco D. The role of the funny current in pacemaker activity // Circ. Res. 2010. Vol. 106. N 3. P. 434–446.

22. Aminu A.J., Petkova M., Atkinson A.J., Yanni J., Morris A.D., Simms R.T., Chen W., Yin Z., Kuniewicz M., Holda M.K., Kuzmin V.S. Further insights into the molecular complexity of the human sinus node – the role of “novel” transcription factors and microRNAs // Prog. Biophys. Mol. Biol. 2021. Vol. 15: S0079-6107(21)00038-9.

23. Jensen B., Vesterskov S., Boukens B.J., Nielsen J.M., Moorman A.F., Christoffels V.M., Wang T. Morphofunctional characterization of the systemic venous pole of the reptile heart // Sci. Rep. 2017. Vol. 7. N 1: 6644.

24. Mommersteeg M.T.M., Hoogaars W.M.H., Prall O.W.J., de Gier-de Vries C., Wiese C., Clout D.E., Papaioannou V.E., Brown N.A., Harvey R.P., Moorman A.F., Christoffels V.M. Molecular pathway for the localized formation of the sinoatrial node // Circ. Res. 2007. Vol. 100. N 3. P. 354–362.

25. Sylva M., Hoff M.J.B. Van Den, Moorman A.F.M. Development of the human heart // Am. J. Med. Genet. A. 2014. Vol. 164A. N 6. P. 1347–1371.

26. Zhou B., Ma Q., Rajagopal S., Domian I., RiveraFeliciano J., Jiang D., von Gise A., Ikeda S., Chien K.R., Pu W.T. Epicardial progenitors contribute to the cardiomyocyte lineage in the developing heart // Nature. 2008. Vol. 454. N 7200. P. 109–113.

27. Moorman A.F.M., Christoffels V.M. Cardiac chamber formation: Development, genes, and evolution // Physiol. Rev. 2003. Vol. 83. N 4. P. 1223–1267.

28. Buckingham M., Meilhac S., Zaffran S. Building the mammalian heart from two sources of myocardial cells // Nat. Rev. Genet. 2005. Vol. 6. N 11. P. 826–835.

29. Cai C.-L., Liang X., Shi Y., Chu P.H., Pfaff S.L., Chen J., Evans S. Isl1 identifies a cardiac progenitor population that proliferates prior to differentiation and contributes a majority of cells to the heart // Dev. Cell. 2003. Vol. 5. N 6. P. 877–889.

30. Snarr B.S., O’Neal J.L., Chintalapudi M.R., Wirrig E.E., Phelps A.L., Kubalak S.W., Wessels A. Isl1 expression at the venous pole identifies a novel role for the second heart field in cardiac development // Circ. Res. 2007. Vol. 101. N 10. P. 971–974.

31. Galli D., Domínguez J.N., Zaffran S., Munk A., Brown N.A., Buckingham M.E. Atrial myocardium derives from the posterior region of the second heart field, which acquires left-right identity as Pitx2c is expressed // Dev. 2008. Vol. 135. N 6. P. 1157–1167.

32. Douglas Y.L., Jongbloed M.R.M., Deruiter M.C., Gittenberger-de Groot A.C. Normal and abnormal development of pulmonary veins: state of the art and correlation with clinical entities // Int. J. Cardiol. 2011. Vol. 147. N 1. P. 13–24.

33. Kelly R.G., Brown N.A., Buckingham M.E. The arterial pole of the mouse heart forms from Fgf10-expressing cells in pharyngeal mesoderm // Dev. Cell. 2001. Vol. 1. N 3. P. 435–440.

34. Van Den Berg G., Abu-Issa R., De Boer B.A., Hutson M.R., de Boer P.A., Soufan A.T., Ruijter J.M., Kirby M.L., van den Hoff M.J., Moorman A.F. A caudal proliferating growth center contributes to both poles of the forming heart tube // Circ. Res. 2009. Vol. 104. N 2. P. 179–188.

35. Mommersteeg M.T.M., Domínguez J.N., Wiese C., Norden J., De Gier-De Vries C., Burch J.B., Kispert A., Brown N.A., Moorman A.F., Christoffels V.M. The sinus venosus progenitors separate and diversify from the first and second heart fields early in development // Cardiovasc. Res. 2010. Vol. 87. N 1. P. 92–101.

36. Bondue A., Blanpain C. Mesp1: a key regulator of cardiovascular lineage commitment // Circ. res. 2010. Vol.107. N 12. P. 575–578.

37. Groot A.C.G., Mahtab E.A.F., Hahurij N.D., Wisse L.J., Deruiter M.C., Wijffels M.C., Poelmann R.E. Nkx2.5-negative myocardium of the posterior heart field and its correlation with podoplanin expression in cells from the developing cardiac pacemaking and conduction system // Anat. Rec. 2007. Vol. 290. N 1. P.115–122.

38. Stefanovic S., Christoffels V.M. GATA-dependent transcriptional and epigenetic control of cardiac lineage specification and differentiation // Cell. Mol. Life Sci. 2015. Vol. 72. N 20. P. 3871–3881.

39. Ma Q., Zhou B., Pu W.T. Reassessment of Isl1 and Nkx2-5 cardiac fate maps using a Gata4-based reporter of Cre activity // Dev. Biol. 2008. Vol. 323. N 1. P. 98–104.

40. Wiese C., Grieskamp T., Airik R., Mommersteeg M.T., Gardiwal A., de Gier-de Vries C., Schuster-Gossler K., Moorman A.F., Kispert A., Christoffels V.M. Formation of the sinus node head and differentiation of sinus node myocardium are independently regulated by Tbx18 and Tbx3 // Circ. Res. 2009. Vol. 104. N 3. P. 388–397.

41. Sizarov A., Anderson R.H., Christoffels V.M., Moorman A.F. Three-dimensional and molecular analysis of the venous pole of the developing human heart // Circulation. 2010. Vol. 122. N 8. P. 798–807.

42. Anderson R.H., Brown N.A., Moorman A.F.M. Development and structures of the venous pole of the heart // Dev. Dyn. 2006. Vol. 235. N 1. P. 2–9.

43. Кузьмин В.С., Алексеева Н.В., Розенштраух Л.В. Миокардиальная ткань торакальных вен позвоночных животных: происхождение и контроль биоэлектрических свойств // Усп. физиол. наук. 2017. Т. 48. №3. С. 3–28.

44. Wessels A., Sedmera D. Developmental anatomy of the heart: a tale of mice and man // Physiol. Genomics. 2003. Vol. 15. N 3. P. 165–176.

45. Singh R., Hoogaars W.M., Barnett P., Grieskamp T., Rana M.S., Buermans H., Farin H.F., Petry M., Heallen T., Martin J.F., Moorman A.F. Tbx2 and Tbx3 induce atrioventricular myocardial development and endocardial cushion formation // Cell. Mol. Life Sci. 2012. Vol. 69. N 8. P. 1377–1389.

46. Liang X., Wang G., Lin L., Lowe J., Zhang Q., Bu L., Chen Y., Chen J., Sun Y., Evans S.M. HCN4 dynamically marks the first heart field and conduction system precursors // Circ. Res. 2013. Vol. 113. N 4. P. 399–407.

47. Sun C., Yu D., Ye W., Liu C., Gu S., Sinsheimer N.R., Song Z., Li X., Chen C., Song Y., Wang S. The short stature homeobox 2 (Shox2)-bone morphogenetic protein (BMP) pathway regulates dorsal mesenchymal protrusion development and its temporary function as a pacemaker during cardiogenesis // J. Biol. Chem. 2015. Vol. 290. N 4. P. 2007–2023.

48. Ivanova A.D., Samoilova D. V, Razumov A.A., Kuzmin V.S. Rat caval vein myocardium undergoes changes in conduction characteristics during postnatal ontogenesis // Pflugers Arch. 2019. Vol. 471. N 11–12. P. 1493–1503.

49. Van Mierop L.H., Gessner I.H. The morphologic development of the sinoatrial node in the mouse // Am. J. Cardiol. 1970. Vol. 25. N 2. P. 204–212.

50. Kuzmin V.S., Ivanova A.D., Potekhina V.M., Samoilova D.V., Ushenin K.S., Shvetsova A.A., Petrov A.M. The susceptibility of the rat pulmonary and caval vein myocardium to the catecholamine-induced ectopy changes oppositely in postnatal development // J. Physiol. 2021. Vol. 599. N 11. P. 2803–2821.

51. Hoogaars W.M.H., Engel A., Brons J.F., Verkerk A.O., de Lange F.J., Wong L.E., Bakker M.L., Clout D.E., Wakker V., Barnett P., Ravesloot J.H. Tbx3 controls the sinoatrial node gene program and imposes pacemaker function on the atria // Genes Dev. 2007. Vol. 21. N 9. P. 1098–1112.

52. Hoogaars W.M.H., Tessari A., Moorman A.F.M., de Boer P.A., Hagoort J., Soufan A.T., Campione M., Christoffels V.M. The transcriptional repressor Tbx3 delineates the developing central conduction system of the heart // Cardiovasc. Res. 2004. Vol. 62. N 3. P. 489–499.

53. Frank D.U., Carter K.L., Thomas K.R., Burr R.M., Bakker M.L., Coetzee W.A., Tristani-Firouzi M., Bamshad M.J., Christoffels V.M., Moon A.M. Lethal arrhythmias in Tbx3-deficient mice reveal extreme dosage sensitivity of cardiac conduction system function and homeostasis // Proc. Natl. Acad. Sci. U.S.A. 2012. Vol. 109. N 3. P. E154–E163.

54. Mohan R.A., Mommersteeg M.T.M., Domínguez J.N., Choquet C., Wakker V., de Gier-de Vries C., Boink G.J., Boukens B.J., Miquerol L., Verkerk A.O., Christoffels V.M. Embryonic Tbx3+ cardiomyocytes form the mature cardiac conduction system by progressive fate restriction // Dev. 2018. Vol. 145. N 17: dev167361.

55. Bakker M.L., Boink G.J.J., Boukens B.J., Verkerk A.O., van den Boogaard M., den Haan A.D., Hoogaars W.M., Buermans H.P., de Bakker J.M., Seppen J., Tan H.L. T-box transcription factor TBX3 reprogrammes mature cardiac myocytes into pacemaker-like cells // Cardiovasc. Res. 2012. Vol. 94. N 3. P. 439–449.

56. Wu M., Peng S., Yang J., Tu Z., Cai X., Cai C.L., Wang Z., Zhao Y. Baf250a orchestrates an epigenetic pathway to repress the Nkx2.5-directed contractile cardiomyocyte program in the sinoatrial node // Cell Res. 2014. Vol. 24. N 10. P. 1201–1213.

57. Christoffels V.M., Hoogaars W.M.H., Tessari A., Clout D.E., Moorman A.F., Campione M. T-Box transcription factor Tbx2 represses differentiation and formation of the cardiac chambers // Dev. Dyn. 2004. Vol. 229. N 4. P. 763–770.

58. Ivanova A.D., Filatova T.S., Abramochkin D.V. Atkinson A., Dobrzynski H., Kokaeva Z.G., Merzlyak E.M., Pustovit K.B., Kuzmin V.S. Attenuation of inward rectifier potassium current contributes to the α1-adrenergic receptor-induced proarrhythmicity in the caval vein myocardium // Acta Physiol. (Oxf). 2021. Vol. 231. N 4: e13597.

59. Domínguez J.N., Meilhac S.M., Bland Y.S., Buckingham M.E., Brown N.A. Asymmetric fate of the posterior part of the second heart field results in unexpected left/right contributions to both poles of the heart // Circ. Res. 2012. Vol. 111. N 10. P. 1323–1335.

60. Franco D., Campione M. The role of Pitx2 during cardiac development. Linking left-right signaling and congenital heart diseases // Trends Cardiovasc. Med. 2003. Vol. 13. N 4. P. 157–163.

61. Wang J., Klysik E., Sood S., Johnson R.L., Wehrens X.H., Martin J.F. Pitx2 prevents susceptibility to atrial arrhythmias by inhibiting left-sided pacemaker specification // Proc. Natl. Acad. Sci. U.S.A. 2010. Vol. 107. N 21. P. 9753–9758.

62. Durocher D., Dé F., Charron R., Schwartz R.J., Nemer M. The cardiac transcription factors Nkx2-5 and GATA-4 are mutual cofactors have been shown to alter transcription of target genes via binding to the consensus WGATAR sequence through a DNA-binding domain consisting of two adjacent zinc // EMBO J. 1997. Vol. 16. N 18. P. 5687–5696.

63. Garg V., Kathiriya I.S., Barnes R., Schluterman M.K., King I.N., Butler C.A., Rothrock C.R., Eapen R.S., Hirayama-Yamada K., Joo K., Matsuoka R. GATA4 mutations cause human congenital heart defects and reveal an interaction with TBX5 // Nature. 2003. Vol. 424. N 6947. P. 443–447.

64. Habets P.E.M.H., Moorman A.F.M., Clout D.E.W., van Roon M.A., Lingbeek M., van Lohuizen M., Campione M., Christoffels V.M. Cooperative action of Tbx2 and Nkx2.5 inhibits ANF expression in the atrioventricular canal: implications for cardiac chamber formation // Genes Dev. 2002. Vol. 16. N 10. P. 1234–1246.

65. Blaschke R.J., Hahurij N.D., Kuijper S., Just S., Wisse L.J., Deissler K., Maxelon T., Anastassiadis K., Spitzer J., Hardt S.E., Schöler H. Targeted mutation reveals essential functions of the homeodomain transcription factor Shox2 in sinoatrial and pacemaking development // Circulation. 2007. Vol. 115. N 14. P. 1830–1838.

66. Hoffmann S., Berger I.M., Glaser A., Bacon C., Li L., Gretz N., Steinbeisser H., Rottbauer W., Just S., Rappold G. Islet1 is a direct transcriptional target of the homeodomain transcription factor Shox2 and rescues the Shox2-mediated bradycardia // Basic Res. Cardiol. 2013. Vol. 108. N 2: 339.

67. van Eif V.W.W., Devalla H.D., Boink G.J.J., Christoffels V.M. Transcriptional regulation of the cardiac conduction system // Nat. Rev. Cardiol. 2018. Vol. 15. N 10. P. 617–630.

68. Ye W., Wang J., Song Y., Yu D., Sun C., Liu C., Chen F., Zhang Y., Wang F., Harvey R.P., Schrader L. A common Shox2-Nkx2-5 antagonistic mechanism primes the pacemaker cell fate in the pulmonary vein myocardium and sinoatrial node // Dev. 2015. Vol. 142. N 14. P. 2521–2532.

69. Potekhina V.M., Averina O.A., Razumov A.A., Kuzmin V.S., Rozenshtraukh L.V. The local repolarization heterogeneity in the murine pulmonary veins myocardium contributes to the spatial distribution of the adrenergically induced ectopic foci // J. Physiol. Sci. 2019. Vol. 69. N 6. P. 1041–1055.

70. Espinoza-lewis R.A., Yu L., He F., Liu H., Tang R., Shi J., Sun X., Martin J.F., Wang D., Yang J., Chen Y. Shox2 is essential for the differentiation of cardiac pacemaker cells by repressing Nkx2-5 // Dev. Biol. 2009. Vol. 327. N 2. P. 376–385.

71. van Wijk B., Moorman A.F.M., van den Hoff M.J.B. Role of bone morphogenetic proteins in cardiac differentiation // Cardiovasc. Res. 2007. Vol. 74. N 2. P. 244–255.

72. Ma L., Lu M.-F., Schwartz R.J., Martin J.F. Bmp2 is essential for cardiac cushion epithelial-mesenchymal transition and myocardial patterning // Dev. 2005. Vol. 132. N 24. P. 5601–5611.

73. Puskaric S., Schmitteckert S., Mori A.D., Glaser A., Schneider K.U., Bruneau B.G., Blaschke R.J., Steinbeisser H., Rappold G. Shox2 mediates Tbx5 activity by regulating Bmp4 in the pacemaker region of the developing heart // Hum. Mol. Genet. 2010. Vol. 19. N 23. P. 4625–4633.

74. Wu L., Du J., Jing X., Yan Y., Deng S., Hao Z., She Q. Bone morphogenetic protein 4 promotes the differentiation of Tbx18-positive epicardial progenitor cells to pacemaker-like cells // Exp. Ther. Med. 2019. Vol. 17. N 4. P. 2648–2656.

75. Willert K., Nusse R. Wnt proteins // Cold Spring Harb. Perspect. Biol. 2012. Vol. 4. N 9: a007864.

76. Nusse R. Wnt signaling in disease and in development // Cell Res. 2005. Vol. 15. N 1. P. 28–32.

77. Valenta T., Hausmann G., Basler K. The many faces and functions of β-catenin // EMBO J. 2012. Vol. 31. N 12. P. 2714–2736.

78. Hoppler S., Mazzotta S., Kühl M. Wnt Signaling in heart organogenesis // Wnt signaling in development and disease: Molecular mechanisms and biological functions / Eds. S. Hoppler and R.T. Moon. John Wiley & Sons, 2014. P. 293–301.

79. Norden J., Greulich F., Rudat C., Taketo M.M., Kispert A. Wnt/β-catenin signaling maintains the mesenchymal precursor pool for murine sinus horn formation // Circ. Res. 2011. Vol. 109. N 6. P. 42–50.

80. Cohen E.D., Miller M.F., Wang Z., Moon R.T., Morrisey E.E. Wnt5a and wnt11 are essential for second heart field progenitor development // Dev. 2012. Vol. 139. N 11. P. 1931–1940.

81. Martínez-Estrada O.M., Lettice L.A., Essafi A., Guadix J.A., Slight J., Velecela V., Hall E., Reichmann J., Devenney P.S., Hohenstein P., Hosen N. Wt1 is required for cardiovascular progenitor cell formation through transcriptional control of Snail and E-cadherin // Nat. Genet. 2010. Vol. 42. N 1. P. 89–93.

82. Norden J., Grieskamp T., Lausch E., van Wijk B, van den Hoff M.J., Englert C., Petry M., Mommersteeg M.T., Christoffels V.M., Niederreither K., Kispert A. Wt1 and retinoic acid signaling in the subcoelomic mesenchyme control the development of the pleuropericardial membranes and the sinus horns // Circ. Res. 2010. Vol. 106. N 7. P. 1212–1220.

83. Niederreither K., Vermot J., Messaddeq N., Schuhbaur B., Chambon P., Dollé P. Embryonic retinoic acid synthesis is essential for heart morphogenesis in the mouse // Dev. 2001. Vol. 128. N 7. P. 1019–1031.

84. Kidd T., Bland K.S., Goodman C.S. Slit is the midline repellent for the robo receptor in Drosophila // Cell. 1999. Vol. 96. N 6. P. 785–794.

85. Jones C.A., London N.R., Chen H., Park K.W., Sauvaget D., Stockton R.A., Wythe J.D., Suh W., LarrieuLahargue F., Mukouyama Y.S., Lindblom P. Robo4 stabilizes the vascular network by inhibiting pathologic angiogenesis and endothelial hyperpermeability // Nat. Med. 2008. Vol. 14. N 4. P. 448–453.

86. Ypsilanti A.R., Zagar Y., Chédotal A. Moving away from the midline: new developments for Slit and Robo // Dev. 2010. Vol. 137. N 12. P. 1939–1952.

87. Zhao J., Mommersteeg M.T.M. Slit-Robo signalling in heart development // Cardiovasc. Res. 2018. Vol. 114. N 6. P. 794–804.

88. Kruszka P., Tanpaiboon P., Neas K., Crosby K., Berger S.I., Martinez A.F., Addissie Y.A., Pongprot Y., Sittiwangkul R., Silvilairat S., Makonkawkeyoon K. Loss of function in ROBO1 is associated with tetralogy of Fallot and septal defects // J. Med. Genet. 2017. Vol. 54. N 12. P. 825–829.

89. Mommersteeg M.T.M., Andrews W.D., Ypsilanti A.R., Zelina P., Yeh M.L., Norden J., Kispert A., Chédotal A., Christoffels V.M., Parnavelas J.G. Slit-roundabout signaling regulates the development of the cardiac systemic venous return and pericardium // Circ. Res. 2013. Vol. 112. N 3. P. 465–475.

90. Medioni C., Bertrand N., Mesbah K., Hudry B., Dupays L., Wolstein O., Washkowitz A.J., Papaioannou V.E., Mohun T.J., Harvey R.P., Zaffran S. Expression of Slit and Robo genes in the developing mouse heart // Dev. Dyn. 2010. Vol. 239. N 12. P. 3303–3311.

91. Astarita J., Acton S., Turley S. Podoplanin: emerging functions in development, the immune system, and cancer // Front. Immunol. 2012. Vol. 3: 283.

92. Quintanilla M., Montero-Montero L., Renart J., Martín-Villar E. Podoplanin in inflammation and cancer // Int. J. Mol. Sci. 2019. Vol. 20. N 707: ijms20030707.

93. Mahtab E.A.F., Vicente-Steijn R., Hahurij N.D., Jongbloed M.R., Wisse L.J., DeRuiter M.C., Uhrin P., Zaujec J., Binder B.R., Schalij M.J., Poelmann R.E. Podoplanin deficient mice show a RhoA-related hypoplasia of the sinus venosus myocardium including the sinoatrial node // Dev. Dyn. 2009. Vol. 238. N 1. P. 183–193.

94. Mahtab E.A.F., Wijffels M.C.E.F., Van Den Akker N.M.S., Hahurij N.D., Lie-Venema H., Wisse L.J., DeRuiter M.C., Uhrin P., Zaujec J., Binder B.R., Schalij M.J. Cardiac malformations and myocardial abnormalities in podoplanin knockout mouse embryos: correlation with abnormal epicardial development // Dev. Dyn. 2008. Vol. 237. N 3. P. 847–857.

95. Martín-Villar E., Megías D., Castel S., Yurrita M.M., Vilaró S., Quintanilla M. Podoplanin binds ERM proteins to activate RhoA and promote epithelial-mesenchymal transition // J. Cell Sci. 2006. Vol. 119. N 21. P. 4541–4553.

96. Amin E., Dubey B.N., Zhang S.-C., Gremer L., Dvorsky R., Moll J.M., Taha M.S., Nagel-Steger L., Piekorz R.P., Somlyo A.V., Ahmadian M.R. Rho-kinase: regulation, (dys)function, and inhibition // Biol. Chem. 2013. Vol. 394. N 11. P. 1399–1410.

97. Vicente-Steijn R., S M., Kolditz D.P., Askar S.F., Bax N.A., Van Der Graaf L.M., Wisse L.J., Passier R., Pijnappels D.A., Schalij M.J., Poelmann R.E. Electrical activation of sinus venosus myocardium and expression patterns of RhoA and Isl-1 in the chick embryo // J. Cardiovasc. Electrophysiol. 2010. Vol.21. N 11. P. 1284–1292.

98. Vicente-Steijn R., Kelder T.P., Tertoolen L.G., Wisse L.J., Pijnappels D.A., Poelmann R.E., Schalij M.J., deRuiter M.C., Gittenberger-de Groot A.C., Jongbloed M.R. RHOA-ROCK signalling is necessary for lateralization and differentiation of the developing sinoatrial node // Cardiovasc. Res. 2017. Vol. 113. N 10. P. 1186–1197.

99. Carmeliet P., Ng Y.S., Nuyens D., Theilmeier G., Brusselmans K., Cornelissen I., Ehler E., Kakkar V.V., Stalmans I., Mattot V., Perriard J.C. Impaired myocardial angiogenesis and ischemic cardiomyopathy in mice lacking the vascular endothelial growth factor isoforms VEGF164 and VEGF188 // Nat. Med. 1999. Vol. 5. N 5. P. 495–502.

100. van den Akker N.M.S., Caolo V., Molin D.G.M. Cellular decisions in cardiac outflow tract and coronary development: an act by VEGF and NOTCH // Differentiation. 2012. Vol. 84. N 1. P. 62–78.

101. Calkoen E.E., Vicente-steijn R., Hahurij N.D., van Munsteren C.J., Roest A.A., DeRuiter M.C., Steendijk P., Schalij M.J., Gittenberger-de Groot A.C., Blom N.A., Jongbloed M.R. Abnormal sinoatrial node development resulting from disturbed vascular endothelial growth factor signaling // Int. J. Cardiol. 2015. Vol. 183. P. 249–257.

102. Hellström M., Phng L.-K., Gerhardt H. VEGF and Notch signaling: the yin and yang of angiogenic sprouting // Cell Adh. Migr. 2007. Vol. 1. N 3. P. 133–136.

103. Wang Y., Wu B., Lu P., Zhang D., Wu B., Varshney S., del Monte-Nieto G., Zhuang Z., Charafeddine R., Kramer A.H., Sibinga N.E. Uncontrolled angiogenic precursor expansion causes coronary artery anomalies in mice lacking Pofut1 // Nat. Commun. 2017. Vol. 8. N 1: 578.

104. Wang Y., Lu P., Jiang L., Wu B., Zhou B. Control of sinus venous valve and sinoatrial node development by endocardial NOTCH1 // Cardiovasc. Res. 2020. Vol. 116. N 8. P. 1473–1486.

105. Van Den Akker N.M.S., Lie-Venema H., Maas S., Eralp I., DeRuiter M.C., Poelmann R.E., Gittenberger-De Groot A.C. Platelet-derived growth factors in the developing avian heart and maturating coronary vasculature // Dev. Dyn. 2005. Vol. 233. N 4. P. 1579–1588.

106. Bax N.A.M., Bleyl S.B., Gallini R., Wisse L.J., Hunter J., Van Oorschot A.A., Mahtab E.A., Lie-Venema H., Goumans M.J., Betsholtz C., Gittenberger-de Groot A.C. Cardiac malformations in Pdgfralpha mutant embryos are associated with increased expression of WT1 and Nkx2.5 in the second heart field // Dev. Dyn. 2010. Vol. 239. N 8. P. 2307–2317.

107. Zheng X., Wang F., Hu X., Li H., Guan Z., Zhang Y., Hu X. PDGFRα-signaling is dispensable for the development of the sinoatrial node after its fate commitment // Front. Cell Dev. Biol. 2021. Vol. 9: 647165.

108. Zhao H., Wang F., Zhang W., Yang M., Tang Y., Wang X., Zhao Q., Huang C. Overexpression of TBX3 in human induced pluripotent stem cells (hiPSCs) increases their differentiation into cardiac pacemaker-like cells // Biomed. Pharmacother. 2020. Vol. 130: 110612.

109. Gorabi A.M., Hajighasemi S., Khori V., Soleimani M., Rajaei M., Rabbani S., Atashi A., Ghiaseddin A., Saeid A.K., Tafti H.A., Sahebkar A. Functional biological pacemaker generation by T-Box18 protein expression via stem cell and viral delivery approaches in a murine model of complete heart block // Pharmacol. Res. 2019. Vol. 141. P. 443–450.

110. Schweizer P.A., Darche F.F., Ullrich N.D., Geschwill P., Greber B., Rivinius R., Seyler C., Müller-Decker K., Draguhn A., Utikal J., Koenen M. Subtypespecific differentiation of cardiac pacemaker cell clusters from human induced pluripotent stem cells // Stem Cell Res. Ther. 2017. Vol. 8. N 1: 229.

111. Naumova N., Iop L. Bioengineering the cardiac conduction system: advances in cellular, gene, and tissue engineering for heart rhythm regeneration // Front. Bioeng. Biotechnol. 2021. Vol. 9: 673477.

112. Protze S.I., Liu J., Nussinovitch U., Ohana L., Backx P.H., Gepstein L., Keller G.M. Sinoatrial node cardiomyocytes derived from human pluripotent cells function as a biological pacemaker // Nat. Biotechnol. 2017. Vol. 35. N 1. P. 56–68.

113. Cingolani E., Goldhaber J.I., Marbán E. Next-generation pacemakers: from small devices to biological pacemakers // Nat. Rev. Cardiol. 2018. Vol. 15. N 3. P. 139–150.

114. Quan D., Huang H. In vitro study of the effects of reprogramming neonatal rat fibroblasts transfected with TBX18 on spontaneous beating in neonatal rat cardiomyocytes // Mol. Med. Rep. 2018. Vol. 18. N 6. P. 5520–5526.

115. Zhang J., Huang C. A new combination of transcription factors increases the harvesting efficiency of pacemaker-like cells // Mol. Med. Rep. 2019. Vol. 19. N 5. P. 3584–3592.

116. Goodyer W.R., Beyersdorf B.M., Paik D.T., Tian L., Li G., Buikema J.W., Chirikian O., Choi S., Venkatraman S., Adams E.L., Tessier-Lavigne M. Transcriptomic profiling of the developing cardiac conduction system at single-cell resolution // Circ. Res. 2019. Vol. 125. N 4. P. 379–397.


Рецензия

Для цитирования:


Кузьмин В.С., Каменский А.А. Молекулярные механизмы онтогенеза ритмоводителя сердца у позвоночных животных. Вестник Московского университета. Серия 16. Биология. 2021;76(4):183-201.

For citation:


Kuzmin V.S., Kamensky A.A. The molecular and cellular mechanisms of the heart pacemaker development in vertebrates. Vestnik Moskovskogo universiteta. Seriya 16. Biologiya. 2021;76(4):183-201. (In Russ.)

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