Cardiosphere-Derived Cells Reverse Heart Failure With Preserved Ejection Fraction in Rats by Decreasing Fibrosis and Inflammation

JACC: Basic to Translational Science

Volumn 1, Issue 1-2, 2016, Pages 14-28

  Gallet, Romain ^a   de Couto, Geoffrey ^a   Simsolo, Eli ^a   Valle, Jackelyn ^a   Sun, Baiming ^a   Liu, Weixin ^a   Tseliou, Eleni ^a   Zile, Michael R ^b   Marbán, Eduardo ^a  

^a CEDARS SINAI MEDICAL CENTER   (United States)

^b RALPH H JOHNSON VA MEDICAL CENTER   (United States)

Author keywords

animal models; cell therapy; diastolic function; heart failure with preserved ejection fraction

Indexed keywords

EID: 85008698071     PISSN: 2452302X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jacbts.2016.01.003     Document Type: Article

References (57)

1. 1 Hogg, K., Swedberg, K., McMurray, J., Heart failure with preserved left ventricular systolic function; epidemiology, clinical characteristics, and prognosis. J Am Coll Cardiol 43 (2004), 317–327.
2. 2 Lam, C.S., Donal, E., Kraigher-Krainer, E., Vasan, R.S., Epidemiology and clinical course of heart failure with preserved ejection fraction. Eur J Heart Fail 13 (2011), 18–28.
3. 3 Owan, T.E., Hodge, D.O., Herges, R.M., Jacobsen, S.J., Roger, V.L., Redfield, M.M., Trends in prevalence and outcome of heart failure with preserved ejection fraction. N Engl J Med 355 (2006), 251–259.
4. 4 Brouwers, F.P., de Boer, R.A., van der Harst, P., et al. Incidence and epidemiology of new onset heart failure with preserved vs. reduced ejection fraction in a community-based cohort: 11-year follow-up of PREVEND. Eur Heart J 34 (2013), 1424–1431.
5. 5 Tribouilloy, C., Rusinaru, D., Mahjoub, H., et al. Prognosis of heart failure with preserved ejection fraction: a 5 year prospective population-based study. Eur Heart J 29 (2008), 339–347.
6. 6 McMurray, J.J., Adamopoulos, S., Anker, S.D., et al. ESC guidelines for the diagnosis and treatment of acute and chronic heart failure 2012: the Task Force for the Diagnosis and Treatment of Acute and Chronic Heart Failure 2012 of the European Society of Cardiology. Developed in collaboration with the Heart Failure Association (HFA) of the ESC. Eur Heart J 33 (2012), 1787–1847.
7. 7 Borlaug, B.A., Paulus, W.J., Heart failure with preserved ejection fraction: pathophysiology, diagnosis, and treatment. Eur Heart J 32 (2011), 670–679.
8. 8 Zile, M.R., Baicu, C.F., Gaasch, W.H., Diastolic heart failure—abnormalities in active relaxation and passive stiffness of the left ventricle. N Engl J Med 350 (2004), 1953–1959.
9. 9 Glezeva, N., Baugh, J.A., Role of inflammation in the pathogenesis of heart failure with preserved ejection fraction and its potential as a therapeutic target. Heart Fail Rev 19 (2014), 681–694.
10. 10 Paulus, W.J., Tschope, C., A novel paradigm for heart failure with preserved ejection fraction: comorbidities drive myocardial dysfunction and remodeling through coronary microvascular endothelial inflammation. J Am Coll Cardiol 62 (2013), 263–271.
11. 11 van Empel, V., Brunner-La Rocca, H.P., Inflammation in HFpEF: key or circumstantial?. Int J Cardiol 189 (2015), 259–263.
12. 12 Zile, M.R., Baicu, C.F., Ikonomidis, J.S., et al. Myocardial stiffness in patients with heart failure and a preserved ejection fraction: contributions of collagen and titin. Circulation 131 (2015), 1247–1259.
13. 13 Westermann, D., Lindner, D., Kasner, M., et al. Cardiac inflammation contributes to changes in the extracellular matrix in patients with heart failure and normal ejection fraction. Circ Heart Fail 4 (2011), 44–52.
14. 14 Kasner, M., Westermann, D., Lopez, B., et al. Diastolic tissue Doppler indexes correlate with the degree of collagen expression and cross-linking in heart failure and normal ejection fraction. J Am Coll Cardiol 57 (2011), 977–985.
15. 15 Dorn, G.W. II, The fuzzy logic of physiological cardiac hypertrophy. Hypertension 49 (2007), 962–970.
16. 16 Aminzadeh, M.A., Tseliou, E., Sun, B., et al. Therapeutic efficacy of cardiosphere-derived cells in a transgenic mouse model of non-ischaemic dilated cardiomyopathy. Eur Heart J 36 (2015), 751–762.
17. 17 de Couto, G., Liu, W., Tseliou, E., et al. Macrophages mediate cardioprotective cellular postconditioning in acute myocardial infarction. J Clin Invest 125 (2015), 3147–3162.
18. 18 Malliaras, K., Li, T.S., Luthringer, D., et al. Safety and efficacy of allogeneic cell therapy in infarcted rats transplanted with mismatched cardiosphere-derived cells. Circulation 125 (2012), 100–112.
19. 19 Smith, R.R., Barile, L., Cho, H.C., et al. Regenerative potential of cardiosphere-derived cells expanded from percutaneous endomyocardial biopsy specimens. Circulation 115 (2007), 896–908.
20. 20 Tseliou, E., Reich, H., de Couto, G., et al. Cardiospheres reverse adverse remodeling in chronic rat myocardial infarction: roles of soluble endoglin and Tgf-beta signaling. Basic Res Cardiol, 109, 2014, 443.
21. 21 Malliaras, K., Smith, R.R., Kanazawa, H., et al. Validation of contrast-enhanced magnetic resonance imaging to monitor regenerative efficacy after cell therapy in a porcine model of convalescent myocardial infarction. Circulation 128 (2013), 2764–2775.
22. 22 Doi, R., Masuyama, T., Yamamoto, K., et al. Development of different phenotypes of hypertensive heart failure: systolic versus diastolic failure in Dahl salt-sensitive rats. J Hypertens 18 (2000), 111–120.
23. 23 Horgan, S., Watson, C., Glezeva, N., Baugh, J., Murine models of diastolic dysfunction and heart failure with preserved ejection fraction. J Card Fail 20 (2014), 984–995.
24. 24 Koshizuka, R., Ishizu, T., Kameda, Y., Kawamura, R., Seo, Y., Aonuma, K., Longitudinal strain impairment as a marker of the progression of heart failure with preserved ejection fraction in a rat model. J Am Soc Echocardiogr 26 (2013), 316–323.
25. 25 Masuyama, T., Yamamoto, K., Sakata, Y., et al. Evolving changes in Doppler mitral flow velocity pattern in rats with hypertensive hypertrophy. J Am Coll Cardiol 36 (2000), 2333–2338.
26. 26 Ishizu, T., Seo, Y., Kameda, Y., et al. Left ventricular strain and transmural distribution of structural remodeling in hypertensive heart disease. Hypertension 63 (2014), 500–506.
27. 27 Bowen, T.S., Rolim, N.P., Fischer, T., et al. Heart failure with preserved ejection fraction induces molecular, mitochondrial, histological, and functional alterations in rat respiratory and limb skeletal muscle. Eur J Heart Fail 17 (2015), 263–272.
28. 28 Bae, S., Yalamarti, B., Ke, Q., et al. Preventing progression of cardiac hypertrophy and development of heart failure by paricalcitol therapy in rats. Cardiovasc Res 91 (2011), 632–639.
29. 29 Kim, S., Yoshiyama, M., Izumi, Y., et al. Effects of combination of ACE inhibitor and angiotensin receptor blocker on cardiac remodeling, cardiac function, and survival in rat heart failure. Circulation 103 (2001), 148–154.
30. 30 Rimbaud, S., Ruiz, M., Piquereau, J., et al. Resveratrol improves survival, hemodynamics and energetics in a rat model of hypertension leading to heart failure. PLoS One, 6, 2011, e26391.
31. 31 Yazawa, H., Miyachi, M., Furukawa, M., et al. Angiotensin-converting enzyme inhibition promotes coronary angiogenesis in the failing heart of Dahl salt-sensitive hypertensive rats. J Card Fail 17 (2011), 1041–1050.
32. 32 Appleton, C.P., Hatle, L.K., Popp, R.L., Relation of transmitral flow velocity patterns to left ventricular diastolic function: new insights from a combined hemodynamic and Doppler echocardiographic study. J Am Coll Cardiol 12 (1988), 426–440.
33. 33 Kai, H., Kuwahara, F., Tokuda, K., Imaizumi, T., Diastolic dysfunction in hypertensive hearts: roles of perivascular inflammation and reactive myocardial fibrosis. Hypertens Res 28 (2005), 483–490.
34. 34 Tseliou, E., de Couto, G., Terrovitis, J., et al. Angiogenesis, cardiomyocyte proliferation and anti-fibrotic effects underlie structural preservation post-infarction by intramyocardially-injected cardiospheres. PLoS One, 9, 2014, e88590.
35. 35 Makkar, R.R., Smith, R.R., Cheng, K., et al. Intracoronary cardiosphere-derived cells for heart regeneration after myocardial infarction (CADUCEUS): a prospective, randomised phase 1 trial. Lancet 379 (2012), 895–904.
36. 36 Malliaras, K., Makkar, R.R., Smith, R.R., et al. Intracoronary cardiosphere-derived cells after myocardial infarction: evidence of therapeutic regeneration in the final 1-year results of the CADUCEUS trial (Cardiosphere-Derived Autologous Stem Cells to Reverse Ventricular Dysfunction). J Am Coll Cardiol 63 (2014), 110–122.
37. 37 Collier, P., Watson, C.J., Voon, V., et al. Can emerging biomarkers of myocardial remodelling identify asymptomatic hypertensive patients at risk for diastolic dysfunction and diastolic heart failure?. Eur J Heart Fail 13 (2011), 1087–1095.
38. 38 Goligorsky, M.S., Microvascular rarefaction: the decline and fall of blood vessels. Organogenesis 6 (2010), 1–10.
39. 39 Hoenig, M.R., Bianchi, C., Rosenzweig, A., Sellke, F.W., The cardiac microvasculature in hypertension, cardiac hypertrophy and diastolic heart failure. Curr Vasc Pharmacol 6 (2008), 292–300.
40. 40 Mohammed, S.F., Hussain, S., Mirzoyev, S.A., Edwards, W.D., Maleszewski, J.J., Redfield, M.M., Coronary microvascular rarefaction and myocardial fibrosis in heart failure with preserved ejection fraction. Circulation 131 (2015), 550–559.
41. 41 Shah, A.M., Pfeffer, M.A., The many faces of heart failure with preserved ejection fraction. Nat Rev Cardiol 9 (2012), 555–556.
42. 42 Maurer, M.S., King, D.L., El-Khoury Rumbarger, L., Packer, M., Burkhoff, D., Left heart failure with a normal ejection fraction: identification of different pathophysiologic mechanisms. J Card Fail 11 (2005), 177–187.
43. 43 Desai, A.S., Heart failure with preserved ejection fraction: time for a new approach?. J Am Coll Cardiol 62 (2013), 272–274.
44. 44 Kuwahara, F., Transforming growth factor-beta function blocking prevents myocardial fibrosis and diastolic dysfunction in pressure-overloaded rats. Circulation 106 (2002), 130–135.
45. 45 Melendez, G.C., McLarty, J.L., Levick, S.P., Du, Y., Janicki, J.S., Brower, G.L., Interleukin 6 mediates myocardial fibrosis, concentric hypertrophy, and diastolic dysfunction in rats. Hypertension 56 (2010), 225–231.
46. 46 Nicoletti, A., Heudes, D., Mandet, C., Hinglais, N., Bariety, J., Michel, J.B., Inflammatory cells and myocardial fibrosis: spatial and temporal distribution in renovascular hypertensive rats. Cardiovasc Res 32 (1996), 1096–1107.
47. 47 Sciarretta, S., Ferrucci, A., Ciavarella, G.M., et al. Markers of inflammation and fibrosis are related to cardiovascular damage in hypertensive patients with metabolic syndrome. Am J Hypertens 20 (2007), 784–791.
48. 48 Zouein, F.A., de Castro Bras, L.E., da Costa, D.V., Lindsey, M.L., Kurdi, M., Booz, G.W., Heart failure with preserved ejection fraction: emerging drug strategies. J Cardiovasc Pharmacol 62 (2013), 13–21.
49. 49 Zile, M.R., Desantis, S.M., Baicu, C.F., et al. Plasma biomarkers that reflect determinants of matrix composition identify the presence of left ventricular hypertrophy and diastolic heart failure. Circ Heart Fail 4 (2011), 246–256.
50. 50 Zannad, F., Rossignol, P., Iraqi, W., Extracellular matrix fibrotic markers in heart failure. Heart Fail Rev 15 (2010), 319–329.
51. 51 Ibrahim, A.G., Cheng, K., Marban, E., Exosomes as critical agents of cardiac regeneration triggered by cell therapy. Stem Cell Reports 2 (2014), 606–619.
52. 52 Tseliou, E., Fouad, J., Reich, H., et al. Fibroblasts rendered antifibrotic, antiapoptotic, and angiogenic by priming with cardiosphere-derived extracellular membrane vesicles. J Am Coll Cardiol 66 (2015), 599–611.
53. 53 de Couto, G., Makkar, N., Marbán, E., Cardiosphere-derived cell exosomes confer acute cardioprotection following ischemia-reperfusion injury through macrophage polarization. Circulation, 132, 2015, A16991.
54. 54 Gallet, R., Tseliou, E., Dawkins, J., et al. Intracoronary delivery of self-assembling heart-derived microtissues (cardiospheres) for prevention of adverse remodeling in a pig model of convalescent myocardial infarction. Circ Cardiovasc Interv, 8, 2015.
55. 55 Klotz, S., Hay, I., Zhang, G., Maurer, M., Wang, J., Burkhoff, D., Development of heart failure in chronic hypertensive Dahl rats: focus on heart failure with preserved ejection fraction. Hypertension 47 (2006), 901–911.
56. 56 Qu, P., Hamada, M., Ikeda, S., Hiasa, G., Shigematsu, Y., Hiwada, K., Time-course changes in left ventricular geometry and function during the development of hypertension in Dahl salt-sensitive rats. Hypertens Res 23 (2000), 613–623.
57. 57 Marban, E., Breakthroughs in cell therapy for heart disease: focus on cardiosphere-derived cells. Mayo Clin Proc 89 (2014), 850–858.