Cardiac stem cell hybrids enhance myocardial repair

Circulation Research

Volumn 117, Issue 8, 2015, Pages 695-706

  Quijada, Pearl ^a   Salunga, Hazel T ^a   Hariharan, Nirmala ^b   Cubillo, Jonathan D ^a   El Sayed, Farid G ^a   Moshref, Maryam ^a   Bala, Kristin M ^a   Emathinger, Jacqueline M ^a   De La Torre, Andrea ^a   Ormachea, Lucia ^a   Alvarez, Roberto ^a   Gude, Natalie A ^a   Sussman, Mark A ^a  

^a SAN DIEGO STATE UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cell fusion; Mesenchymal stromal cells; Myocardial infarction; Myocytes, cardiac; Stem cells

Indexed keywords

INTERLEUKIN 6; PROTEIN P16; PROTEIN P53; STROMAL CELL DERIVED FACTOR 1; BIOLOGICAL MARKER;

ADULT STEM CELL; ANIMAL CELL; ARTERIAL WALL THICKNESS; ARTICLE; CAPILLARY DENSITY; CARDIAC STEM CELL; CELL COUNT; CELL CYCLE ARREST; CELL DEATH; CELL DIFFERENTIATION; CELL FUSION; CELL POPULATION; CELL PROLIFERATION; CELL REGENERATION; CELL SURVIVAL; CELL TRANSFER; COCULTURE; CONTROLLED STUDY; ENGRAFTMENT; FLUORESCENCE ACTIVATED CELL SORTING; GENE EXPRESSION; GENETIC ENGINEERING; HEART EJECTION FRACTION; HEART FUNCTION; HEART INFARCTION; HEART MUSCLE CELL; HEART MUSCLE INJURY; IN VITRO STUDY; MESENCHYMAL STEM CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; ANGIOGENESIS; ANIMAL; ANTERIOR WALL MYOCARDIAL INFARCTION; CARDIAC MUSCLE CELL; CELL CULTURE; CELL SIZE; COMPARATIVE STUDY; CONVALESCENCE; DISEASE MODEL; FEMALE; GENETIC TRANSFECTION; GRAFT SURVIVAL; HEART CONTRACTION; HEART LEFT VENTRICLE FUNCTION; HEART STROKE VOLUME; HEART VENTRICLE; HISTOCOMPATIBILITY; MESENCHYMAL STEM CELL TRANSPLANTATION; METABOLISM; NEWBORN; PARACRINE SIGNALING; PATHOLOGY; PATHOPHYSIOLOGY; PHENOTYPE; RAT; REGENERATION; TIME FACTOR; TRANSPLANTATION;

ANIMALS; ANIMALS, NEWBORN; ANTERIOR WALL MYOCARDIAL INFARCTION; BIOMARKERS; CELL PROLIFERATION; CELL SIZE; CELL SURVIVAL; CELLS, CULTURED; COCULTURE TECHNIQUES; DISEASE MODELS, ANIMAL; FEMALE; GRAFT SURVIVAL; HEART VENTRICLES; MESENCHYMAL STEM CELL TRANSPLANTATION; MICE; MYOCARDIAL CONTRACTION; MYOCYTES, CARDIAC; NEOVASCULARIZATION, PHYSIOLOGIC; PARACRINE COMMUNICATION; PHENOTYPE; RATS; RECOVERY OF FUNCTION; REGENERATION; STROKE VOLUME; TIME FACTORS; TRANSFECTION; TRANSPLANTATION CHIMERA; VENTRICULAR FUNCTION, LEFT;

EID: 85047290173     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.115.306838     Document Type: Article

References (43)

1. Hong KU, Guo Y, Li QH, Cao P, Al-Maqtari T, Vajravelu BN, Du J, Book MJ, Zhu X, Nong Y, Bhatnagar A, Bolli R. 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. doi: 10.1371/journal.pone.0096725.
2. Fischer KM, Cottage CT, Wu W, Din S, Gude NA, Avitabile D, Quijada P, Collins BL, Fransioli J, Sussman MA. Enhancement of myocardial regeneration through genetic engineering of cardiac progenitor cells expressing Pim-1 kinase. Circulation. 2009;120:2077-2087. doi: 10.1161/CIRCULATIONAHA.109.884403.
3. Mohsin S, Khan M, Toko H, et al. Human cardiac progenitor cells engineered with Pim-I kinase enhance myocardial repair. J Am Coll Cardiol. 2012;60:1278-1287. doi: 10.1016/j.jacc.2012.04.047.
4. Leri A, Kajstura J, Anversa P. Cardiac stem cells and mechanisms of myocardial regeneration. Physiol Rev. 2005;85:1373-1416. doi: 10.1152/physrev.00013.2005.
5. van Berlo JH, Kanisicak O, Maillet M, Vagnozzi RJ, Karch J, Lin SC, Middleton RC, Marbán E, Molkentin JD. c-kit+ cells minimally contribute cardiomyocytes to the heart. Nature. 2014;509:337-341. doi: 10.1038/nature13309.
6. Bolli R, Chugh AR, D'Amario D, et al. Cardiac stem cells in patients with ischaemic cardiomyopathy (SCIPIO): initial results of a randomised phase 1 trial. Lancet. 2011;378:1847-1857. doi: 10.1016/S0140-6736(11)61590-0.
7. Sanganalmath SK, Bolli R. Cell therapy for heart failure: a comprehensive overview of experimental and clinical studies, current challenges, and future directions. Circ Res. 2013;113:810-834. doi: 10.1161/CIRCRESAHA.113.300219.
8. Hare JM, Fishman JE, Gerstenblith G, 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. doi: 10.1001/jama.2012.25321.
9. Wang Y, Chen X, Cao W, Shi Y. Plasticity of mesenchymal stem cells in immunomodulation: pathological and therapeutic implications. Nat Immunol. 2014;15:1009-1016. doi: 10.1038/ni.3002.
10. Hatzistergos KE, Quevedo H, Oskouei BN, et al. Bone marrow mesenchymal stem cells stimulate cardiac stem cell proliferation and differentiation. Circ Res. 2010;107:913-922. doi: 10.1161/CIRCRESAHA.110.222703.
11. Williams AR, Hatzistergos KE, Addicott B, McCall F, Carvalho D, Suncion V, Morales AR, Da Silva J, Sussman MA, Heldman AW, Hare JM. 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. doi: 10.1161/CIRCULATIONAHA.112.131110.
12. Alvarez-Dolado M, Pardal R, Garcia-Verdugo JM, Fike JR, Lee HO, Pfeffer K, Lois C, Morrison SJ, Alvarez-Buylla A. Fusion of bone-marrow- derived cells with Purkinje neurons, cardiomyocytes and hepatocytes. Nature. 2003;425:968-973. doi: 10.1038/nature02069.
13. Johansson CB, Youssef S, Koleckar K, Holbrook C, Doyonnas R, Corbel SY, Steinman L, Rossi FM, Blau HM. Extensive fusion of haematopoietic cells with Purkinje neurons in response to chronic inflammation. Nat Cell Biol. 2008;10:575-583. doi: 10.1038/ncb1720.
14. Yang WJ, Li SH, Weisel RD, Liu SM, Li RK. Cell fusion contributes to the rescue of apoptotic cardiomyocytes by bone marrow cells. J Cell Mol Med. 2012;16:3085-3095. doi: 10.1111/j.1582-4934.2012.01600.x.
15. Soza-Ried J, Fisher AG. Reprogramming somatic cells towards pluripotency by cellular fusion. Curr Opin Genet Dev. 2012;22:459-465. doi: 10.1016/j.gde.2012.07.005.
16. Tsubouchi T, Soza-Ried J, Brown K, Piccolo FM, Cantone I, Landeira D, Bagci H, Hochegger H, Merkenschlager M, Fisher AG. DNA synthesis is required for reprogramming mediated by stem cell fusion. Cell. 2013;152:873-883. doi: 10.1016/j.cell.2013.01.012.
17. Acquistapace A, Bru T, Lesault PF, Figeac F, Coudert AE, le Coz O, Christov C, Baudin X, Auber F, Yiou R, Dubois-Randé JL, Rodriguez AM. Human mesenchymal stem cells reprogram adult cardiomyocytes toward a progenitor-like state through partial cell fusion and mitochondria transfer. Stem Cells. 2011;29:812-824. doi: 10.1002/stem.632.
18. Takei S, Yamamoto M, Cui L, Yue F, Johkura K, Ogiwara N, Iinuma H, Okinaga K, Sasaki K. Phenotype-specific cells with proliferative potential are produced by polyethylene glycol-induced fusion of mouse embryonic stem cells with fetal cardiomyocytes. Cell Transplant. 2005;14:701-708.
19. Islam MQ, Meirelles Lda S, Nardi NB, Magnusson P, Islam K. Polyethylene glycol-mediated fusion between primary mouse mesenchymal stem cells and mouse fibroblasts generates hybrid cells with increased proliferation and altered differentiation. Stem Cells Dev. 2006;15:905-919. doi: 10.1089/scd.2006.15.905.
20. Davani S, Marandin A, Mersin N, Royer B, Kantelip B, Herve P, Etievent JP, Kantelip JP. Mesenchymal progenitor cells differentiate into an endothelial phenotype, enhance vascular density, and improve heart function in a rat cellular cardiomyoplasty model. Circulation. 2003;108 Suppl 1:II253-258.
21. Zaruba MM, Franz WM. Role of the SDF-1-CXCR4 axis in stem cellbased therapies for ischemic cardiomyopathy. Expert Opin Biol Ther. 2010;10:321-335. doi: 10.1517/14712590903460286.
22. Zacchigna S, Giacca M. Extra- and intracellular factors regulating cardiomyocyte proliferation in postnatal life. Cardiovasc Res. 2014;102:312-320. doi: 10.1093/cvr/cvu057.
23. Fontes JA, Rose NR, Čiháková D. The varying faces of IL-6: From cardiac protection to cardiac failure. Cytokine. 2015;74:62-68. doi: 10.1016/j. cyto.2014.12.024.
24. Endo J, Sano M, Fujita J, Hayashida K, Yuasa S, Aoyama N, Takehara Y, Kato O, Makino S, Ogawa S, Fukuda K. Bone marrow derived cells are involved in the pathogenesis of cardiac hypertrophy in response to pressure overload. Circulation. 2007;116:1176-1184. doi: 10.1161/CIRCULATIONAHA.106.650903.
25. Wu JM, Hsueh YC, Ch'ang HJ, Luo CY, Wu LW, Nakauchi H, Hsieh PC. Circulating cells contribute to cardiomyocyte regeneration after injury. Circ Res. 2015;116:633-641. doi: 10.1161/CIRCRESAHA.116.304564.
26. Pajcini KV, Pomerantz JH, Alkan O, Doyonnas R, Blau HM. Myoblasts and macrophages share molecular components that contribute to cell-cell fusion. J Cell Biol. 2008;180:1005-1019. doi: 10.1083/jcb.200707191.
27. Hochreiter-Hufford AE, Lee CS, Kinchen JM, Sokolowski JD, Arandjelovic S, Call JA, Klibanov AL, Yan Z, Mandell JW, Ravichandran KS. Phosphatidylserine receptor BAI1 and apoptotic cells as new promoters of myoblast fusion. Nature. 2013;497:263-267. doi: 10.1038/nature12135.
28. Estrada JC, Torres Y, Benguría A, Dopazo A, Roche E, Carrera-Quintanar L, Pérez RA, Enríquez JA, Torres R, Ramírez JC, Samper E, Bernad A. Human mesenchymal stem cell-replicative senescence and oxidative stress are closely linked to aneuploidy. Cell Death Dis. 2013;4:e691. doi: 10.1038/cddis.2013.211.
29. Peterson SE, Westra JW, Rehen SK, Young H, Bushman DM, Paczkowski CM, Yung YC, Lynch CL, Tran HT, Nickey KS, Wang YC, Laurent LC, Loring JF, Carpenter MK, Chun J. Normal human pluripotent stem cell lines exhibit pervasive mosaic aneuploidy. PLoS One. 2011;6:e23018. doi: 10.1371/journal.pone.0023018.
30. Boheler KR, Joodi RN, Qiao H, Juhasz O, Urick AL, Chuppa SL, Gundry RL, Wersto RP, Zhou R. Embryonic stem cell-derived cardiomyocyte heterogeneity and the isolation of immature and committed cells for cardiac remodeling and regeneration. Stem Cells Int. 2011;2011:214203. doi: 10.4061/2011/214203.
31. Pavlath GK, Blau HM. Expression of muscle genes in heterokaryons depends on gene dosage. J Cell Biol. 1986;102:124-130.
32. Islam MQ, Ringe J, Reichmann E, Migotti R, Sittinger M, da S Meirelles L, Nardi NB, Magnusson P, Islam K. Functional characterization of cell hybrids generated by induced fusion of primary porcine mesenchymal stem cells with an immortal murine cell line. Cell Tissue Res. 2006;326:123-137. doi: 10.1007/s00441-006-0224-2.
33. Islam MQ, Panduri V, Islam K. Generation of somatic cell hybrids for the production of biologically active factors that stimulate proliferation of other cells. Cell Prolif. 2007;40:91-105. doi: 10.1111/j.1365-2184.2007.00422.x.
34. Foshay KM, Looney TJ, Chari S, Mao FF, Lee JH, Zhang L, Fernandes CJ, Baker SW, Clift KL, Gaetz J, Di CG, Xiang AP, Lahn BT. Embryonic stem cells induce pluripotency in somatic cell fusion through biphasic reprogramming. Mol Cell. 2012;46:159-170. doi: 10.1016/j. molcel.2012.02.013.
35. Dong F, Harvey J, Finan A, Weber K, Agarwal U, Penn MS. Myocardial CXCR4 expression is required for mesenchymal stem cell mediated repair following acute myocardial infarction. Circulation. 2012;126:314-324. doi: 10.1161/CIRCULATIONAHA.111.082453.
36. Taghavi S, Sharp TE, 3rd, Duran JM, Makarewich CA, Berretta RM, Starosta T, Kubo H, Barbe M, Houser SR. Autologous c-kit+ mesenchymal stem cell injections provide superior therapeutic benefit as compared to c-kit+ cardiac-derived stem cells in a feline model of isoproterenolinduced cardiomyopathy [published online ahead of print February 11, 2015]. Clin Transl Sci. doi: 10.1111/cts.12251. http://onlinelibrary.wiley. com/doi/10.1111/cts.12251/abstract.
37. Poynter JA, Herrmann JL, Manukyan MC, Wang Y, Abarbanell AM, Weil BR, Brewster BD, Meldrum DR. Intracoronary mesenchymal stem cells promote postischemic myocardial functional recovery, decrease inflammation, and reduce apoptosis via a signal transducer and activator of transcription 3 mechanism. J Am Coll Surg. 2011;213:253-260. doi: 10.1016/j.jamcollsurg.2011.04.005.
38. Usunier B, Benderitter M, Tamarat R, Chapel A. Management of fibrosis: the mesenchymal stromal cells breakthrough. Stem Cells Int. 2014;2014:340257. doi: 10.1155/2014/340257.
39. Yee K, Malliaras K, Kanazawa H, et al. Allogeneic cardiospheres delivered via percutaneous transendocardial injection increase viable myocardium, decrease scar size, and attenuate cardiac dilatation in porcine ischemic cardiomyopathy. PLoS One. 2014;9:e113805. doi: 10.1371/journal.pone.0113805.
40. Quijada P, Sussman MA. Making it stick: chasing the optimal stem cells for cardiac regeneration. Expert Rev Cardiovasc Ther. 2014;12:1275-1288. doi: 10.1586/14779072.2014.972941.
41. Chong JJ, Yang X, Don CW, et al. Human embryonic-stem-cell-derived cardiomyocytes regenerate non-human primate hearts. Nature. 2014;510:273-277. doi: 10.1038/nature13233.
42. Nauta AJ, Fibbe WE. Immunomodulatory properties of mesenchymal stromal cells. Blood. 2007;110:3499-3506. doi: 10.1182/blood-2007-02-069716.
43. Tat PA, Sumer H, Pralong D, Verma PJ. The efficiency of cell fusionbased reprogramming is affected by the somatic cell type and the in vitro age of somatic cells. Cell Reprogram. 2011;13:331-344. doi: 10.1089/cell.2011.0002.