Cardiac and systemic rejuvenation after cardiosphere-derived cell therapy in senescent rats

European Heart Journal

Volumn 38, Issue 39, 2017, Pages 2957-2967

  Grigorian Shamagian, Lilian ^a   Liu, Weixin ^a   Fereydooni, Soraya ^a   Middleton, Ryan C ^a   Valle, Jackelyn ^a   Cho, Jae Hyung ^a   Marbán, Eduardo ^a  

^a CEDARS SINAI MEDICAL CENTER   (United States)

Author keywords

Aging; Cardiosphere derived cells; Cell therapy; Diastolic dysfunction; Rejuvenation

Indexed keywords

BIOLOGICAL MARKER; BRAIN NATRIURETIC PEPTIDE; INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 6; PHOSPHATE BUFFERED SALINE; TELOMERASE; TRANSCRIPTOME;

AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD EXAMINATION; CARDIAC MUSCLE CELL; CARDIAC STEM CELL; CARDIOSPHERE DERIVED CELL; CELL CULTURE; CELL THERAPY; CONTROLLED STUDY; DIASTOLIC DYSFUNCTION; ECHOCARDIOGRAPHY; ENZYME ACTIVITY; EXOSOME; GENE EXPRESSION; HAIR GROWTH; HEART FUNCTION; HEART MUSCLE FIBROSIS; HEART VENTRICLE ENDDIASTOLIC PRESSURE; HEART VENTRICLE HYPERTROPHY; HEART VENTRICLE VOLUME; HEMODYNAMICS; HISTOPATHOLOGY; HUMAN; HUMAN CELL; IN VITRO STUDY; INFLAMMATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; RAT; STRUCTURE ANALYSIS; TELOMERE LENGTH; TRANSCRIPTOMICS; TREADMILL TEST; WEIGHT REDUCTION; AGED; ANALYSIS OF VARIANCE; ANIMAL; BIOLOGICAL THERAPY; CELL AGING; CYTOLOGY; FETAL STEM CELL; FISCHER 344 RAT; HEART; MIDDLE AGED; MULTICELLULAR SPHEROID; PHYSIOLOGY; PROCEDURES; REGENERATION; REJUVENATION; SPRAGUE DAWLEY RAT; STEM CELL TRANSPLANTATION; TELOMERE;

AGED; ANALYSIS OF VARIANCE; ANIMALS; CELL- AND TISSUE-BASED THERAPY; CELLULAR SENESCENCE; FETAL STEM CELLS; HEART; HUMANS; MIDDLE AGED; MYOCYTES, CARDIAC; PHYSICAL CONDITIONING, ANIMAL; RATS, INBRED F344; RATS, SPRAGUE-DAWLEY; REGENERATION; REJUVENATION; SPHEROIDS, CELLULAR; STEM CELL TRANSPLANTATION; TELOMERE;

EID: 85032488155     PISSN: 0195668X     EISSN: 15229645     Source Type: Journal    
DOI: 10.1093/eurheartj/ehx454     Document Type: Article

References (31)

1. Terzic A, Waldman S. Chronic diseases: the emerging pandemic. Clin Transl Sci 2011;4:225-226.
2. Erusalimsky JD, Kurz DJ. Cellular senescence in vivo: its relevance in ageing and cardiovascular disease. Exp Gerontol 2005;40:634-642.
3. Lopez-Otin C, Blasco M, Partridge L, Serrano M, Kroemer G. The hallmarks of aging. Cell 2013;153:1194-1217.
4. Leri A, Franco S, Zacheo A, Barlucchi L, Chimenti S, Limana F, Blasco M. Ablation of telomerase and telomere loss leads to cardiac dilatation and heart failure associated with p53 upregulation. EMBO J 2003;22:131-139.
5. Aix E, Gutierrez O, Sanchez-Ferrer C, Aguado T, Flores I. Postnatal telomere dysfunction induces cardiomyocyte cell-cycle arrest through p21 activation. J Cell Biol 2016;213:571-583.
6. Senni M, Paulus WJ, Gavazzi A, Fraser AG, D-?ez J, Solomon SD, Smiseth OA, Guazzi M, Lam CS, Maggioni AP, Tschöpe C, Metra M, Hummel SL, Edelmann F, Ambrosio G, Stewart Coats AJ, Filippatos GS, Gheorghiade M, Anker SD, Levy D, Pfeffer MA, Stough WG, Pieske BM. New strategies for heart failure with preserved ejection fraction: the importance of targeted therapies for heart failure phenotypes. Eur Heart J 2014;35:2797-2815.
7. Camichi GG, Savarese G, Akhmedov A, Luscher TF. Molecular mechanism of endothelial and vascular aging: implications for cardiovascular disease. Eur Heart J 2015;36:3392-3403.
8. Kane GC, Karon BL, Mahoney DW, Redfield MM, Roger VL, Burnett JC Jr, Jacobsen SJ, Rodeheffer RJ. Progression of left ventricular diastolic dysfunction and risk of heart failure. JAMA 2011;306:856-863.
9. Loffredo F, Steinhauser M, Jay SM, Gannon J, Pancoast JR, Yalamanchi P, Sinha M, Dall'Osso C, Khong D, Shadrach JL, Miller CM, Singer BS, Stewart A, Psychogios N, Gerszten RE, Hartigan AJ, Kim MJ, Serwold T, Wagers AJ, Lee RT. Growth differentiation factor 11 is a circulating factor that reverses age-related cardiac hypertrophy. Cell 2013;153:828-839.
10. Ocampo A, Reddy P, Martinez-Redondo P, Platero-Luengo A, Hatanaka F, Hishida T, Li M, Lam D, Kurita M, Beyret E, Araoka T, Vazquez-Ferrer E, Donoso D, Roman JL, Xu J, Rodriguez Esteban C, Nunez G, Nunez Delicado E, Campistol JM, Guillen I, Guillen P, Izpisua Belmonte JC. In vivo amelioration of age-associated hallmarks by partial reprogramming. Cell 2016;167:1719-1733.
11. Marban E. Breakthroughs in cell therapy for heart disease: focus on cardiosphere-derived cells. Mayo Clin Proc 2014;89:850-858.
12. Ibrahim AG, Cheng K, Marban E. Exosomes as critical agents of cardiac regeneration triggered by cell therapy. Stem Cell Reports 2014;8:606-619.
13. Gallet R, de Couto G, Simsolo E, Valle J, Sun B, Liu W, Tseliou E, Zile MR, Marban E. Cardiosphere-derived cells reverse heart failure with preserved ejection fraction in rats by decreasing fibrosis and inflammation. JACC Basic Transl Sci 2016;1:14-28.
14. Tseliou E, de Couto G, Terrovitis J, Sun B, Weixin L, Marban L, Marban E. Angiogenesis, cardiomyocyte proliferation and anti-fibrotic effects underlie structural preservation postinfarction by intramyocardially-injected cardiospheres. PLoS One 2014;9:e88590.
15. Aminzadeh MA, Tseliou E, Sun B, Cheng K, Malliaras K, Makkar RR, Marban E. Therapeutic efficacy of cardiosphere-derived cells in a transgenic mouse model of non-ischaemic dilated cardiomyopathy. Eur Heart J 2015;36:751-762.
16. Makkar RR, Smith RR, Cheng K, Malliaras K, Thomson LE, Berman D, Czer LS, Marban L, Mendizabal A, Johnston PV, Russell SD, Schuleri KH, Lardo AC, Gerstenblith G, Marban E. Intracoronary cardiosphere-derived cells for heart regeneration after myocardial infarction (CADUCEUS): a prospective, randomised phase 1 trial. Lancet 2012;379:895-904.
17. Smith R, Barile L, Cheol Cho H, Leppo MK, Hare JM, Messina E, Giacomello A, Abraham MR, Marban E. Regenerative potential of cardiosphere-derived cells expanded from percutaneous endomyocardial biopsy specimens. Circulation 2007;115:896-908.
18. de Couto G, Liu W, Tseliou E, Sun B, Makkar N, Kanazawa H, Arditi M, Marban E. Macrophages mediate cardioprotective cellular postconditioning in acute myocardial infarction. J Clin Invest 2015;125:3147-3162.
19. Lasry A, Ben-Neriah Y. Senescence-associated inflammatory responses: aging and cancer perspectives. Trends Immunol 2015;36:217-228.
20. Bock JS, Gottlieb SS. Cardiorenal syndrome: new perspectives. Circulation 2010; 121:2592-2600.
21. Madonna R, De Caterina R, Willerson J, Geng Y. Biological function and clinical potential of telomerase and associated proteins in cardiovascular tissue repair and regeneration. Eur Heart J 2011;32:1190-1196.
22. Borlaug B. The pathophysiology of heart failure with preserved ejection fraction. Nat Rev Cardiol 2014;11:507-515.
23. Fujimoto N, Hastings L, Bhella S, Shibata S, Gandhi K, Carrick-Ranson G, Levine BD. Effect of ageing on left ventricular compliance and distensibility in healthy sedentary humans. J Physiol 2012;590:1871-1880.
24. Hees PS, Fleg JL, Lakatta EG, Shapiro EP. Left ventricular remodeling with age in normal men versus women: novel insights using three-dimensional magnetic resonance imaging. Am J Cardiol 2002;90:1231-1236.
25. Waller BF. The old-age heart: normal aging changes which can produce or mimic cardiac disease. Clin Cardiol 1988;11:513-517.
26. Bar C, Bernardes de Jesus B, Serrano R, Tejera A, Ayuso E, Jimenez V, Formentini I, Bobadilla M, Mizrahi J, de Martino A, Gomez G, Pisano D, Mulero F, Wollert KC, Bosch F, Blasco MA. Telomerase expression confers cardioprotection in the adult mouse heart after acute myocardial infarction. Nat Commun 2014;5:5863.
27. Bednarek D, Gonzalez-Rosa JM, Guzman-Mart?nez G, Gutiérrez-Gutiérrez O, Aguado T, Sanchez-Ferrer C, Marques IJ, Galardi-Castilla M, de Diego I, Gomez MJ, Cortés A, Zapata A, Jiménez-Borreguero LJ, Mercader N, Flores I. Telomerase is essential for zebrafish heart regeneration. Cell Rep 2015;12: 1691-1703.
28. Coppé JP, Desprez P, Krtolica A, Campisi J. The senescence-associated secretory phenotype: the dark side of tumor suppression. Annu Rev Pathol 2010; 5:99-118.
29. Tchkonia T, Zhu Y, van Deursen J, Campisi J, Kirkland J. Cellular senescence and the senescent secretory phenotype: therapeutic opportunities. J Clin Invest 2013; 123:966-972.
30. Murach KA, McCarthy JJ. MicroRNAs, heart failure, and aging: potential interactions with skeletal muscle. Heart Fail Rev 2017; 22:209-218.
31. Tseliou E, Fouad J, Reich H, Slipczuk L, de Couto G, Aminzadeh M, Middleton R, Valle J, Weixin L, Marban E. Fibroblasts rendered antifibrotic, antiapoptotic, and angiogenic by priming with cardiosphere-derived extracellular membrane vesicles. J Am Coll Cardiol 2015;66:599-611.