Cardiac aging - Getting to the stem of the problem

Journal of Molecular and Cellular Cardiology

Volumn 83, Issue , 2015, Pages 32-36

  Hariharan, Nirmala ^a   Sussman, Mark A ^a  

^a SAN DIEGO STATE UNIVERSITY   (United States)

Author keywords

Aging; Cardiac stem progenitor cells; Heart

Indexed keywords

CARDIAC STEM CELL; CELL AGING; CELL CYCLE ARREST; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL RENEWAL; HEART DISEASE; HEART FAILURE; HUMAN; ISCHEMIC CARDIOMYOPATHY; MESENCHYMAL STEM CELL; MUSCLE STEM CELL; NONHUMAN; PRIORITY JOURNAL; REVIEW; SENESCENCE; SKELETAL MUSCLE SATELLITE CELL; STEM CELL NICHE; AGING; ANIMAL; CARDIAC MUSCLE; CARDIOMYOPATHIES; GENETICS; METABOLISM; MOUSE; PATHOLOGY; PHYSIOLOGY; SPECIES DIFFERENCE; STEM CELL; STEM CELL TRANSPLANTATION;

AGING; ANIMALS; CARDIOMYOPATHIES; CELL DIFFERENTIATION; CELL PROLIFERATION; HUMANS; MICE; MYOCARDIUM; SPECIES SPECIFICITY; STEM CELL NICHE; STEM CELL TRANSPLANTATION; STEM CELLS;

EID: 84937978904     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2015.04.008     Document Type: Review

References (64)

1. Go A.S., Mozaffarian D., Roger V.L., Benjamin E.J., Berry J.D., Blaha M.J., et al. Heart disease and stroke statistics-2014 update: a report from the American Heart Association. Circulation 2014, 129:e28-e292.
2. Lopez-Otin C., Blasco M.A., Partridge L., Serrano M., Kroemer G. The hallmarks of aging. Cell 2013, 153:1194-1217.
3. Anversa P., Rota M., Urbanek K., Hosoda T., Sonnenblick E.H., Leri A., et al. Myocardial aging-a stem cell problem. Basic Res Cardiol 2005, 100:482-493.
4. Sussman M.A., Anversa P. Myocardial aging and senescence: where have the stem cells gone?. Annu Rev Physiol 2004, 66:29-48.
5. Ho A.D., Wagner W., Mahlknecht U. Stem cells and ageing. The potential of stem cells to overcome age-related deteriorations of the body in regenerative medicine. EMBO Rep 2005, [6 Spec No:S35-8].
6. Sharpless N.E., DePinho R.A. How stem cells age and why this makes us grow old. Nat Rev Mol Cell Biol 2007, 8:703-713.
7. Smith J.A., Daniel R. Stem cells and aging: a chicken-or-the-egg issue?. Aging Dis 2012, 3:260-268.
8. Beltrami A.P., Barlucchi L., Torella D., Baker M., Limana F., Chimenti S., et al. Adult cardiac stem cells are multipotent and support myocardial regeneration. Cell 2003, 114:763-776.
9. Uchida S., De Gaspari P., Kostin S., Jenniches K., Kilic A., Izumiya Y., et al. Sca1-derived cells are a source of myocardial renewal in the murine adult heart. Stem Cell Rep 2013, 1:397-410.
10. Pfister O., Mouquet F., Jain M., Summer R., Helmes M., Fine A., et al. CD31- but Not CD31+ cardiac side population cells exhibit functional cardiomyogenic differentiation. Circ Res 2005, 97:52-61.
11. Cai C.L., Liang X., Shi Y., Chu P.H., Pfaff S.L., Chen J., et al. Isl1 identifies a cardiac progenitor population that proliferates prior to differentiation and contributes a majority of cells to the heart. Dev Cell 2003, 5:877-889.
12. Laugwitz K.L., Moretti A., Lam J., Gruber P., Chen Y., Woodard S., et al. Postnatal isl1+ cardioblasts enter fully differentiated cardiomyocyte lineages. Nature 2005, 433:647-653.
13. Ellison G.M., Galuppo V., Vicinanza C., Aquila I., Waring C.D., Leone A., et al. Cardiac stem and progenitor cell identification: different markers for the same cell?. Front Biosci 2010, 2:641-652.
14. Smith R.R., Barile L., Cho H.C., Leppo M.K., Hare J.M., Messina E., et al. Regenerative potential of cardiosphere-derived cells expanded from percutaneous endomyocardial biopsy specimens. Circulation 2007, 115:896-908.
15. Bollini S., Smart N., Riley P.R. Resident cardiac progenitor cells: at the heart of regeneration. J Mol Cell Cardiol 2011, 50:296-303.
16. Leri A., Kajstura J., Anversa P. Role of cardiac stem cells in cardiac pathophysiology: a paradigm shift in human myocardial biology. Circ Res 2011, 109:941-961.
17. Karantalis V., DiFede D.L., Gerstenblith G., Pham S., Symes J., Zambrano J.P., et al. Autologous mesenchymal stem cells produce concordant improvements in regional function, tissue perfusion, and fibrotic burden when administered to patients undergoing coronary artery bypass grafting: the Prospective Randomized Study of Mesenchymal Stem Cell Therapy in Patients Undergoing Cardiac Surgery (PROMETHEUS) trial. Circ Res 2014, 114:1302-1310.
18. Heldman A.W., DiFede D.L., Fishman J.E., Zambrano J.P., Trachtenberg B.H., Karantalis V., et al. Transendocardial mesenchymal stem cells and mononuclear bone marrow cells for ischemic cardiomyopathy: the TAC-HFT randomized trial. JAMA 2014, 311:62-73.
19. Hare J.M., Fishman J.E., Gerstenblith G., DiFede Velazquez D.L., Zambrano J.P., Suncion V.Y., et al. Comparison of allogeneic vs autologous bone marrow-derived mesenchymal stem cells delivered by transendocardial injection in patients with ischemic cardiomyopathy: the POSEIDON randomized trial. JAMA 2012, 308:2369-2379.
20. Bolli R., Chugh A.R., D'Amario D., Loughran J.H., Stoddard M.F., Ikram S., et al. Cardiac stem cells in patients with ischaemic cardiomyopathy (SCIPIO): initial results of a randomised phase 1 trial. Lancet 2011, 378:1847-1857.
21. Makkar R.R., Smith R.R., Cheng K., Malliaras K., Thomson L.E., Berman D., et al. Intracoronary cardiosphere-derived cells for heart regeneration after myocardial infarction (CADUCEUS): a prospective, randomised phase 1 trial. Lancet 2012, 379:895-904.
22. Mohsin S., Siddiqi S., Collins B., Sussman M.A. Empowering adult stem cells for myocardial regeneration. Circ Res 2011, 109:1415-1428.
23. Cesselli D., Beltrami A.P., D'Aurizio F., Marcon P., Bergamin N., Toffoletto B., et al. Effects of age and heart failure on human cardiac stem cell function. Am J Pathol 2011, 179:349-366.
24. Lavasani M., Robinson A.R., Lu A., Song M., Feduska J.M., Ahani B., et al. Muscle-derived stem/progenitor cell dysfunction limits healthspan and lifespan in a murine progeria model. Nat Commun 2012, 3:608.
25. Sinha M., Jang Y.C., Oh J., Khong D., Wu E.Y., Manohar R., et al. Restoring systemic GDF11 levels reverses age-related dysfunction in mouse skeletal muscle. Science 2014, 344:649-652.
26. Katsimpardi L., Litterman N.K., Schein P.A., Miller C.M., Loffredo F.S., Wojtkiewicz G.R., et al. Vascular and neurogenic rejuvenation of the aging mouse brain by young systemic factors. Science 2014, 344:630-634.
27. Cosgrove B.D., Gilbert P.M., Porpiglia E., Mourkioti F., Lee S.P., Corbel S.Y., et al. Rejuvenation of the muscle stem cell population restores strength to injured aged muscles. Nat Med 2014, 20:255-264.
28. Torella D., Rota M., Nurzynska D., Musso E., Monsen A., Shiraishi I., et al. Cardiac stem cell and myocyte aging, heart failure, and insulin-like growth factor-1 overexpression. Circ Res 2004, 94:514-524.
29. Gonzalez A., Rota M., Nurzynska D., Misao Y., Tillmanns J., Ojaimi C., et al. Activation of cardiac progenitor cells reverses the failing heart senescent phenotype and prolongs lifespan. Circ Res 2008, 102:597-606.
30. Hariharan N., Quijada P., Mohsin S., Joyo A., Samse K., Monsanto M., et al. Nucleostemin rejuvenates cardiac progenitor cells and antagonizes myocardial aging. J Am Coll Cardiol 2015, 65:133-147.
31. Mohsin S., Khan M., Nguyen J., Alkatib M., Siddiqi S., Hariharan N., et al. Rejuvenation of human cardiac progenitor cells with Pim-1 kinase. Circ Res 2013, 113:1169-1179.
32. Goichberg P., Kannappan R., Cimini M., Bai Y., Sanada F., Sorrentino A., et al. Age-associated defects in EphA2 signaling impair the migration of human cardiac progenitor cells. Circulation 2013, 128:2211-2223.
33. Mohsin S., Wu J.C., Sussman M.A. Predicting the future with stem cells. Circulation 2014, 129:136-138.
34. D'Amario D., Leone A.M., Iaconelli A., Luciani N., Gaudino M., Kannappan R., et al. Growth properties of cardiac stem cells are a novel biomarker of patients' outcome after coronary bypass surgery. Circulation 2014, 129:157-172.
35. Urbanek K., Quaini F., Tasca G., Torella D., Castaldo C., Nadal-Ginard B., et al. Intense myocyte formation from cardiac stem cells in human cardiac hypertrophy. Proc Natl Acad Sci U S A 2003, 100:10440-10445.
36. Loffredo F.S., Steinhauser M.L., Jay S.M., Gannon J., Pancoast J.R., Yalamanchi P., et al. Growth differentiation factor 11 is a circulating factor that reverses age-related cardiac hypertrophy. Cell 2013, 153:828-839.
37. Golpanian S., El-Khorazaty J., Mendizabal A., DiFede D.L., Suncion V.Y., Karantalis V., et al. Effect of aging on human mesenchymal stem cell therapy in ischemic cardiomyopathy patients. J Am Coll Cardiol 2015, 65:125-132.
38. Hatzistergos K.E., Quevedo H., Oskouei B.N., Hu Q., Feigenbaum G.S., Margitich I.S., et al. Bone marrow mesenchymal stem cells stimulate cardiac stem cell proliferation and differentiation. Circ Res 2010, 107:913-922.
39. Williams A.R., Hatzistergos K.E., Addicott B., McCall F., Carvalho D., Suncion V., et al. Enhanced effect of combining human cardiac stem cells and bone marrow mesenchymal stem cells to reduce infarct size and to restore cardiac function after myocardial infarction. Circulation 2013, 127:213-223.
40. Cheung T.H., Rando T.A. Molecular regulation of stem cell quiescence. Nat Rev Mol Cell Biol 2013, 14:329-340.
41. Urbanek K., Cesselli D., Rota M., Nascimbene A., De Angelis A., Hosoda T., et al. Stem cell niches in the adult mouse heart. Proc Natl Acad Sci U S A 2006, 103:9226-9231.
42. Rodgers J.T., King K.Y., Brett J.O., Cromie M.J., Charville G.W., Maguire K.K., et al. mTORC1 controls the adaptive transition of quiescent stem cells from G0 to G(Alert). Nature 2014, 510:393-396.
43. Chakkalakal J.V., Jones K.M., Basson M.A., Brack A.S. The aged niche disrupts muscle stem cell quiescence. Nature 2012, 490:355-360.
44. Sousa-Victor P., Gutarra S., Garcia-Prat L., Rodriguez-Ubreva J., Ortet L., Ruiz-Bonilla V., et al. Geriatric muscle stem cells switch reversible quiescence into senescence. Nature 2014, 506:316-321.
45. D'Amario D., Cabral-Da-Silva M.C., Zheng H., Fiorini C., Goichberg P., Steadman E., et al. Insulin-like growth factor-1 receptor identifies a pool of human cardiac stem cells with superior therapeutic potential for myocardial regeneration. Circ Res 2011, 108:1467-1481.
46. Sanada F., Kim J., Czarna A., Chan N.Y., Signore S., Ogorek B., et al. c-Kit-positive cardiac stem cells nested in hypoxic niches are activated by stem cell factor reversing the aging myopathy. Circ Res 2014, 114:41-55.
47. Leri A., Rota M., Hosoda T., Goichberg P., Anversa P. Cardiac stem cell niches. Stem Cell Res 2014, 13:631-646.
48. Sundararaman B., Avitabile D., Konstandin M.H., Cottage C.T., Gude N., Sussman M.A. Asymmetric chromatid segregation in cardiac progenitor cells is enhanced by Pim-1 kinase. Circ Res 2012, 110:1169-1173.
49. Kajstura J., Bai Y., Cappetta D., Kim J., Arranto C., Sanada F., et al. Tracking chromatid segregation to identify human cardiac stem cells that regenerate extensively the infarcted myocardium. Circ Res 2012, 111:894-906.
50. Rocheteau P., Gayraud-Morel B., Siegl-Cachedenier I., Blasco M.A., Tajbakhsh S. A subpopulation of adult skeletal muscle stem cells retains all template DNA strands after cell division. Cell 2012, 148:112-125.
51. Anversa P., Leri A., Kajstura J. Biased DNA segregation during stem cell division. Circ Res 2012, 110:1403-1407.
52. Sun D., Luo M., Jeong M., Rodriguez B., Xia Z., Hannah R., et al. Epigenomic profiling of young and aged HSCs reveals concerted changes during aging that reinforce self-renewal. Cell Stem Cell 2014, 14:673-688.
53. Zhou Y., Kim J., Yuan X., Braun T. Epigenetic modifications of stem cells: a paradigm for the control of cardiac progenitor cells. Circ Res 2011, 109:1067-1081.
54. Senyo S.E., Steinhauser M.L., Pizzimenti C.L., Yang V.K., Cai L., Wang M., et al. Mammalian heart renewal by pre-existing cardiomyocytes. Nature 2013, 493:433-436.
55. van Berlo J.H., Kanisicak O., Maillet M., Vagnozzi R.J., Karch J., Lin S.C., et al. c-kit+cells minimally contribute cardiomyocytes to the heart. Nature 2014, 509:337-341.
56. Ellison G.M., Vicinanza C., Smith A.J., Aquila I., Leone A., Waring C.D., et al. Adult c-kit(pos) cardiac stem cells are necessary and sufficient for functional cardiac regeneration and repair. Cell 2013, 154:827-842.
57. Nadal-Ginard B., Ellison G.M., Torella D. Response to Molkentin's letter to the editor regarding article, "the absence of evidence is not evidence of absence: the pitfalls of Cre knock-ins in the c-kit locus". Circ Res 2014, 115:e38-e39.
58. Nadal-Ginard B., Ellison G.M., Torella D. Absence of evidence is not evidence of absence: pitfalls of cre knock-ins in the c-Kit locus. Circ Res 2014, 115:415-418.
59. Molkentin J.D. Letter by Molkentin regarding article, "The absence of evidence is not evidence of absence: the pitfalls of Cre Knock-Ins in the c-Kit Locus". Circ Res 2014, 115:e21-e23.
60. Molkentin J.D., Houser S.R. Response to Torella et al. Circ Res 2014, 114:e27.
61. Torella D., Ellison G.M., Nadal-Ginard B. Adult c-kit(pos) cardiac stem cells fulfill Koch's postulates as causal agents for cardiac regeneration. Circ Res 2014, 114:e24-e26.
62. Cottage C.T., Neidig L., Sundararaman B., Din S., Joyo A.Y., Bailey B., et al. Increased mitotic rate coincident with transient telomere lengthening resulting from Pim-1 overexpression in cardiac progenitor cells. Stem Cells 2012, 30:2512-2522.
63. Hong K.U., Guo Y., Li Q.H., Cao P., Al-Maqtari T., Vajravelu B.N., et al. c-kit+cardiac stem cells alleviate post-myocardial infarction left ventricular dysfunction despite poor engraftment and negligible retention in the recipient heart. PLoS ONE 2014, 9:e96725.
64. Nigro P., Perrucci G.L., Gowran A., Zanobini M., Capogrossi M.C., Pompilio G. c-kit cells: the tell-tale heart of cardiac regeneration. Cell Mol Life Sci 2015, 72(9):1725-1740.