Table of Contents Author Guidelines Submit a Manuscript
BioMed Research International
Volume 2018, Article ID 1981568, 10 pages
https://doi.org/10.1155/2018/1981568
Review Article

Current Knowledge and Recent Advances of Right Ventricular Molecular Biology and Metabolism from Congenital Heart Disease to Chronic Pulmonary Hypertension

1Research and Innovation Unit, RHU BioArt Lung 2020, Marie Lannelongue Hospital, Paris-Sud University, Le Plessis-Robinson, France
2Cardiac Surgery, Marie Lannelongue Hospital, Paris-Sud University, Le Plessis-Robinson, France
3Division of Cardiovascular Medicine, Stanford Cardiovascular Institute, Stanford University School of Medicine, Stanford, CA, USA
4Thoracic and Vascular Surgery and Heart and Lung Transplantation, Marie Lannelongue Hospital, Paris-Sud University, Le Plessis-Robinson, France

Correspondence should be addressed to Julien Guihaire; moc.liamg@eriahiugneiluj

Received 1 September 2017; Accepted 20 December 2017; Published 17 January 2018

Academic Editor: Utako Yokoyama

Copyright © 2018 Samantha Guimaron et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. J. Guihaire, H. Bogaard, E. Flécher et al., “Experimental models of right heart failure: a window for translational research in pulmonary hypertension,” Seminars in Respiratory and Critical Care Medicine, vol. 34, no. 5, pp. 689–699, 2013. View at Publisher · View at Google Scholar · View at Scopus
  2. J. Guihaire, P. E. Noly, S. Schrepfer, and O. Mercier, “Advancing knowledge of right ventricular pathophysiology in chronic pressure overload: Insights from experimental studies,” Archives of Cardiovascular Diseases, vol. 108, no. 10, pp. 519–529, 2015. View at Publisher · View at Google Scholar · View at Scopus
  3. N. F. Voelkel, R. A. Quaife, L. A. Leinwand et al., “Right ventricular function and failure: report of a National Heart, Lung, and Blood Institute working group on cellular and molecular mechanisms of right heart failure,” Circulation, vol. 114, no. 17, pp. 1883–1891, 2006. View at Publisher · View at Google Scholar · View at Scopus
  4. W. F. Friedman, “The intrinsic physiologic properties of the developing heart,” Progress in Cardiovascular Diseases, vol. 15, no. 1, pp. 87–111, 1972. View at Publisher · View at Google Scholar
  5. L. Lopez, M. S. Cohen, R. H. Anderson et al., “Unnatural history of the right ventricle in patients with congenitally malformed hearts,” Cardiology in the Young, vol. 20, supplement 3, pp. 107–112, 2010. View at Publisher · View at Google Scholar
  6. D. Iacobazzi, M.-S. Suleiman, M. Ghorbel, S. J. George, M. Caputo, and R. M. Tulloh, “Cellular and molecular basis of RV hypertrophy in congenital heart disease,” Heart, vol. 102, no. 1, pp. 12–17, 2016. View at Publisher · View at Google Scholar · View at Scopus
  7. N. Galie, M. Humbert, J. L. Vachiery et al., “2015 ESC/ERS Guidelines for the diagnosis and treatment of pulmonary hypertension: the joint task force for the diagnosis and treatment of pulmonary hypertension of the european society of cardiology (ESC) and the european respiratory society (ERS),” in European Heart Journal, Association for European Paediatric and Congenital Cardiology (AEPC) and International Society for Heart and Lung Transplantation (ISHLT), Eds., vol. 37, pp. 67–119, 2016. View at Google Scholar
  8. B. Sztrymf, R. Souza, L. Bertoletti et al., “Prognostic factors of acute heart failure in patients with pulmonary arterial hypertension,” European Respiratory Journal, vol. 35, no. 6, pp. 1286–1293, 2010. View at Publisher · View at Google Scholar · View at Scopus
  9. W. T. Abraham, K. F. Adams, G. C. Fonarow et al., “In-hospital mortality in patients with acute decompensated heart failure requiring intravenous vasoactive medications: an analysis from the acute decompensated heart failure national registry (ADHERE),” Journal of the American College of Cardiology, vol. 46, no. 1, pp. 57–64, 2005. View at Publisher · View at Google Scholar · View at Scopus
  10. J. J. Ryan and S. L. Archer, “The right ventricle in pulmonary arterial hypertension: disorders of metabolism, angiogenesis and adrenergic signaling in right ventricular failure,” Circulation Research, vol. 115, no. 1, pp. 176–188, 2014. View at Publisher · View at Google Scholar · View at Scopus
  11. M. Humbert, O. Sitbon, A. Chaouat et al., “Survival in patients with idiopathic, familial, and anorexigen-associated pulmonary arterial hypertension in the modern management era,” Circulation, vol. 122, no. 2, pp. 156–163, 2010. View at Publisher · View at Google Scholar · View at Scopus
  12. A. Vonk-Noordegraaf, F. Haddad, K. M. Chin et al., “Right heart adaptation to pulmonary arterial hypertension: physiology and pathobiology,” Journal of the American College of Cardiology, vol. 62, no. 25, pp. D22–D33, 2013. View at Publisher · View at Google Scholar · View at Scopus
  13. M. Amsallem, T. Kuznetsova, K. Hanneman, A. Denault, and F. Haddad, “Right heart imaging in patients with heart failure: a tale of two ventricles,” Current Opinion in Cardiology, vol. 31, no. 5, pp. 469–482, 2016. View at Publisher · View at Google Scholar · View at Scopus
  14. A. Gómez, D. Bialostozky, A. Zajarias et al., “Right ventricular ischemia in patients with primary pulmonary hypertension,” Journal of the American College of Cardiology, vol. 38, no. 4, pp. 1137–1142, 2001. View at Publisher · View at Google Scholar · View at Scopus
  15. A. Vonk Noordegraaf and N. Galiè, “The role of the right ventricle in pulmonary arterial hypertension,” European Respiratory Review, vol. 20, no. 122, pp. 243–253, 2011. View at Publisher · View at Google Scholar · View at Scopus
  16. J. Guihaire, F. Haddad, O. Mercier, D. J. Murphy, J. C. Wu, and E. Fadel, “The right heart in congenital heart disease, mechanisms and recent advances,” Journal of Clinical & Experimental Cardiology, vol. 1, no. 8, pp. 1–11, 2012. View at Publisher · View at Google Scholar
  17. W. E. Hopkins, L. L. Ochoa, G. W. Richardson, and E. P. Trulock, “Comparison of the hemodynamics and survival of adults with severe primary pulmonary hypertension or Eisenmenger syndrome,” The Journal of Heart and Lung Transplantation, vol. 15, no. 1 I, pp. 100–105, 1996. View at Google Scholar · View at Scopus
  18. B. Rondelet, C. Dewachter, F. Kerbaul et al., “Prolonged overcirculation-induced pulmonary arterial hypertension as a cause of right ventricular failure,” European Heart Journal, vol. 33, no. 8, pp. 1017–1026, 2012. View at Publisher · View at Google Scholar · View at Scopus
  19. G. Sutendra, P. Dromparis, R. Paulin et al., “A metabolic remodeling in right ventricular hypertrophy is associated with decreased angiogenesis and a transition from a compensated to a decompensated state in pulmonary hypertension,” Journal of Molecular Medicine, vol. 91, no. 11, pp. 1315–1327, 2013. View at Publisher · View at Google Scholar · View at Scopus
  20. N. F. Voelkel, J. Gomez-Arroyo, A. Abbate, H. J. Bogaard, and M. R. Nicolls, “Pathobiology of pulmonary arterial hypertension and right ventricular failure,” European Respiratory Journal, vol. 40, no. 6, pp. 1555–1565, 2012. View at Publisher · View at Google Scholar · View at Scopus
  21. J. J. Ryan and S. L. Archer, “Emerging concepts in the molecular basis of pulmonary arterial hypertension. Part I: metabolic plasticity and mitochondrial dynamics in the pulmonary circulation and right ventricle in pulmonary arterial hypertension,” Circulation, vol. 131, no. 19, pp. 1691–1702, 2015. View at Publisher · View at Google Scholar · View at Scopus
  22. N. F. Voelkel, “The right ventricle in health and diseas,” Respiratory Medicine, 2015. View at Google Scholar
  23. R. G. Kelly, “Building the right ventricle,” Circulation Research, vol. 100, no. 7, pp. 943–945, 2007. View at Publisher · View at Google Scholar · View at Scopus
  24. S. E. Altin and P. C. Schulze, “Metabolism of the right ventricle and the response to hypertrophy and failure,” Progress in Cardiovascular Diseases, vol. 55, no. 2, pp. 229–233, 2012. View at Publisher · View at Google Scholar · View at Scopus
  25. D. J. Fisher, M. A. Heymann, and A. M. Rudolph, “Regional myocardial blood flow and oxygen delivery in fetal, newborn, and adult sheep,” American Journal of Physiology-Heart and Circulatory Physiology, vol. 243, no. 5, pp. H729–H731, 1982. View at Publisher · View at Google Scholar
  26. B. D. Lowes, W. Minobe, W. T. Abraham et al., “Changes in gene expression in the intact human heart: downregulation of α-myosin heavy chain in hypertrophied, failing ventricular myocardium,” The Journal of Clinical Investigation, vol. 100, no. 9, pp. 2315–2324, 1997. View at Publisher · View at Google Scholar · View at Scopus
  27. Y. Wu, W. Feng, H. Zhang et al., “Ca 2+-regulatory proteins in cardiomyocytes from the right ventricle in children with congenital heart disease,” Journal of Translational Medicine, vol. 10, no. 1, article 67, 2012. View at Publisher · View at Google Scholar · View at Scopus
  28. P. Dromparis, G. Sutendra, and E. D. Michelakis, “The role of mitochondria in pulmonary vascular remodeling,” Journal of Molecular Medicine, vol. 88, no. 10, pp. 1003–1010, 2010. View at Publisher · View at Google Scholar · View at Scopus
  29. S. Shah, T. Gupta, and R. Ahmad, “Managing heart failure in transposition of the great arteries,” The Ochsner Journal, vol. 15, no. 3, pp. 290–296, 2015. View at Google Scholar · View at Scopus
  30. E. Di Pietro, M. C. De Angelis, F. Esposito et al., “An imbalance between protective and detrimental molecular pathways is associated with right ventricular dysfunction in congenital heart diseases with outflow obstruction,” International Journal of Cardiology, vol. 172, no. 3, pp. e519–e521, 2014. View at Publisher · View at Google Scholar · View at Scopus
  31. M. Sano, T. Minamino, H. Toko et al., “p53-induced inhibition of Hif-1 causes cardiac dysfunction during pressure overload,” Nature, vol. 446, 2007. View at Google Scholar
  32. S. Bonnet, E. D. Michelakis, C. J. Porter et al., “An Abnormal mitochondrial-hypoxia inducible factor-1α-Kv channel pathway disrupts oxygen sensing and triggers pulmonary arterial hypertension in fawn hooded rats: Similarities to human pulmonary arterial hypertension,” Circulation, vol. 113, no. 22, pp. 2630–2641, 2006. View at Publisher · View at Google Scholar · View at Scopus
  33. J. Gomez-Arroyo, S. Mizuno, K. Szczepanek et al., “Metabolic gene remodeling and mitochondrial dysfunction in failing right ventricular hypertrophy secondary to pulmonary arterial hypertension,” Circulation: Heart Failure, vol. 6, no. 1, pp. 136–144, 2013. View at Publisher · View at Google Scholar · View at Scopus
  34. G. Sutendra, P. Dromparis, A. Kinnaird et al., “Mitochondrial activation by inhibition of PDKII suppresses HIF1a signaling and angiogenesis in cancer,” Oncogene, vol. 32, no. 13, pp. 1638–1650, 2013. View at Publisher · View at Google Scholar · View at Scopus
  35. H. J. Bogaard, K. Abe, A. V. Noordegmaf, and N. F. Voelkel, “The right ventricle under pressure: cellular and molecular mechanisms of right-heart failure in pulmonary hypertension,” CHEST, vol. 135, no. 3, pp. 794–804, 2009. View at Publisher · View at Google Scholar · View at Scopus
  36. H. J. Bogaard, R. Natarajan, S. C. Henderson et al., “Chronic pulmonary artery pressure elevation is insufficient to explain right heart failure,” Circulation, vol. 120, no. 20, pp. 1951–1960, 2009. View at Publisher · View at Google Scholar · View at Scopus
  37. S. L. Archer, Y. Fang, J. J. Ryan, and L. Piao, “Metabolism and bioenergetics in the right ventricle and pulmonary vasculature in pulmonary hypertension,” Pulmonary Circulation, vol. 3, no. 1, pp. 144–152, 2013. View at Publisher · View at Google Scholar
  38. L. Tian, M. Neuber-Hess, J. Mewburn et al., “Ischemia-induced Drp1 and Fis1-mediated mitochondrial fission and right ventricular dysfunction in pulmonary hypertension,” Journal of Molecular Medicine, vol. 95, no. 4, pp. 381–393, 2017. View at Publisher · View at Google Scholar · View at Scopus
  39. K. Sagawa, “The end-systolic pressure-volume relation of the ventricle: definition, modifications and clinical use,” Circulation, vol. 63, no. 6 I, pp. 1223–1227, 1981. View at Publisher · View at Google Scholar · View at Scopus
  40. B. A. Maron, R. T. Zamanian, and A. B. Waxman, “Pulmonary hypertension,” Basic Science to Clinical Medicine, pp. 1–371, 2015. View at Publisher · View at Google Scholar · View at Scopus
  41. D. Boulate, O. Mercier, J. Guihaire et al., “Pulmonary circulatory—right ventricular uncoupling: new insights into pulmonary hypertension pathophysiology,” Pulmonary Hypertension: Basic Science to Clinical Medicine, 2016. View at Publisher · View at Google Scholar · View at Scopus
  42. L. Piao, Y.-H. Fang, V. J. J. Cadete et al., “The inhibition of pyruvate dehydrogenase kinase improves impaired cardiac function and electrical remodeling in two models of right ventricular hypertrophy: resuscitating the hibernating right ventricle,” Journal of Molecular Medicine, vol. 88, no. 1, pp. 47–60, 2010. View at Publisher · View at Google Scholar · View at Scopus
  43. G. Hagan, M. Southwood, C. Treacy et al., “(18)FDG PET imaging can quantify increased cellular metabolism in pulmonary arterial hypertension: A proof-of-principle study,” Pulmonary Circulation, vol. 1, no. 4, pp. 448–455, 2011. View at Publisher · View at Google Scholar
  44. M. Oikawa, Y. Kagaya, H. Otani et al., “Increased [18F]fluorodeoxyglucose accumulation in right ventricular free wall in patients with pulmonary hypertension and the effect of epoprostenol,” Journal of the American College of Cardiology, vol. 45, no. 11, pp. 1849–1855, 2005. View at Publisher · View at Google Scholar · View at Scopus
  45. E. L. Lundgrin, M. M. Park, J. Sharp et al., “Fasting 2-deoxy-2-[18F]fluoro-D-glucose positron emission tomography to detect metabolic changes in pulmonary arterial hypertension hearts over 1 year,” Annals of the American Thoracic Society, vol. 10, no. 1, pp. 1–9, 2013. View at Publisher · View at Google Scholar · View at Scopus
  46. E. L. Brittain, M. Talati, J. P. Fessel et al., “Fatty acid metabolic defects and right ventricular lipotoxicity in human pulmonary arterial hypertension,” Circulation, vol. 133, no. 20, pp. 1936–1944, 2016. View at Publisher · View at Google Scholar · View at Scopus
  47. S. Bokhari, A. Raina, E. B. Rosenweig et al., “PET imaging may provide a novel biomarker and understanding of right ventricular dysfunction in patients with idiopathic pulmonary arterial hypertension,” Circulation: Cardiovascular Imaging, vol. 4, no. 6, pp. 641–647, 2011. View at Publisher · View at Google Scholar · View at Scopus
  48. M. M. Can, C. Kaymaz, I. H. Tanboga et al., “Increased right ventricular glucose metabolism in patients with pulmonary arterial hypertension,” Clinical Nuclear Medicine, vol. 36, no. 9, pp. 743–748, 2011. View at Publisher · View at Google Scholar · View at Scopus
  49. S. Tatebe, Y. Fukumoto, M. Oikawa-Wakayama et al., “Enhanced [18F]fluorodeoxyglucose accumulation in the right ventricular free wall predicts long-term prognosis of patients with pulmonary hypertension: a preliminary observational study,” European Heart Journal—Cardiovascular Imaging, vol. 15, no. 6, pp. 666–672, 2014. View at Publisher · View at Google Scholar · View at Scopus
  50. G. Marsboom, C. Wietholt, C. R. Haney et al., “Lung 18F-fluorodeoxyglucose positron emission tomography for diagnosis and monitoring of pulmonary arterial hypertension,” American Journal of Respiratory and Critical Care Medicine, vol. 185, no. 6, pp. 670–679, 2012. View at Publisher · View at Google Scholar · View at Scopus
  51. W. Li, L. Wang, C.-M. Xiong et al., “The prognostic value of 18F-FDG uptake ratio between the right and left ventricles in idiopathic pulmonary arterial hypertension,” Clinical Nuclear Medicine, vol. 40, no. 11, pp. 859–863, 2015. View at Publisher · View at Google Scholar · View at Scopus
  52. R. M. Tuder, L. A. Davis, and B. B. Graham, “Targeting energetic metabolism: a new frontier in the pathogenesis and treatment of pulmonary hypertension,” American Journal of Respiratory and Critical Care Medicine, vol. 185, no. 3, pp. 260–266, 2012. View at Publisher · View at Google Scholar · View at Scopus
  53. L. Piao, V. K. Sidhu, Y.-H. Fang et al., “FOXO1-mediated upregulation of pyruvate dehydrogenase kinase-4 (PDK4) decreases glucose oxidation and impairs right ventricular function in pulmonary hypertension: therapeutic benefits of dichloroacetate.,” Journal of Molecular Medicine, vol. 91, no. 3, pp. 333–346, 2013. View at Publisher · View at Google Scholar · View at Scopus
  54. Y.-H. Fang, L. Piao, Z. Hong et al., “Therapeutic inhibition of fatty acid oxidation in right ventricular hypertrophy: exploiting Randle's cycle,” Journal of Molecular Medicine, vol. 90, no. 1, pp. 31–43, 2012. View at Publisher · View at Google Scholar · View at Scopus