Cellular and Molecular Life Sciences

, Volume 71, Issue 4, pp 615–627

Fate choice of post-natal mesoderm progenitors: skeletal versus cardiac muscle plasticity

  • Domiziana Costamagna
  • Mattia Quattrocelli
  • Robin Duelen
  • Vardine Sahakyan
  • Ilaria Perini
  • Giacomo Palazzolo
  • Maurilio Sampaolesi
Review

Abstract

Regenerative medicine for skeletal and cardiac muscles still constitutes a fascinating and ambitious frontier. In this perspective, understanding the possibilities of intrinsic cell plasticity, present in post-natal muscles, is vital to define and improve novel therapeutic strategies for acute and chronic diseases. In addition, many somatic stem cells are now crossing the boundaries of basic/translational research to enter the first clinical trials. However, it is still an open question whether a lineage switch between skeletal and cardiac adult myogenesis is possible. Therefore, this review focuses on resident somatic stem cells of post-natal skeletal and cardiac muscles and their plastic potential toward the two lineages. Furthermore, examples of myogenic lineage switch in adult stem cells are also reported and discussed.

Keywords

Skeletal muscle Cardiac muscle Resident stem cells Myogenic regeneration Muscular dystrophy Lineage switch 

References

  1. 1.
    Biressi S, Molinaro M, Cossu G (2007) Cellular heterogeneity during vertebrate skeletal muscle development. Dev Biol 308:281–293. doi:10.1016/j.ydbio.2007.06.006 PubMedGoogle Scholar
  2. 2.
    Aulehla A, Pourquie O (2006) On periodicity and directionality of somitogenesis. Anat Embryol (Berl) 211(Suppl 1):3–8. doi:10.1007/s00429-006-0124-y Google Scholar
  3. 3.
    Kahane N, Cinnamon Y, Bachelet I, Kalcheim C (2001) The third wave of myotome colonization by mitotically competent progenitors: regulating the balance between differentiation and proliferation during muscle development. Development 128:2187–2198PubMedGoogle Scholar
  4. 4.
    Abu-Issa R, Kirby ML (2007) Heart field: from mesoderm to heart tube. Annu Rev Cell Dev Biol 23:45–68. doi:10.1146/annurev.cellbio.23.090506.123331 PubMedGoogle Scholar
  5. 5.
    Bober E, Franz T, Arnold HH, Gruss P, Tremblay P (1994) Pax-3 is required for the development of limb muscles: a possible role for the migration of dermomyotomal muscle progenitor cells. Development 120:603–612PubMedGoogle Scholar
  6. 6.
    Tremblay P, Gruss P (1994) Pax: genes for mice and men. Pharmacol Ther 61:205–226PubMedGoogle Scholar
  7. 7.
    Seale P, Sabourin LA, Girgis-Gabardo A, Mansouri A, Gruss P, Rudnicki MA (2000) Pax7 is required for the specification of myogenic satellite cells. Cell 102:777–786PubMedGoogle Scholar
  8. 8.
    Edmondson DG, Olson EN (1989) A gene with homology to the myc similarity region of MyoD1 is expressed during myogenesis and is sufficient to activate the muscle differentiation program. Genes Dev 3:628–640PubMedGoogle Scholar
  9. 9.
    Buckingham M, Relaix F (2007) The role of Pax genes in the development of tissues and organs: Pax3 and Pax7 regulate muscle progenitor cell functions. Annu Rev Cell Dev Biol 23:645–673. doi:10.1146/annurev.cellbio.23.090506.123438 PubMedGoogle Scholar
  10. 10.
    Saga Y, Kitajima S, Miyagawa-Tomita S (2000) Mesp1 expression is the earliest sign of cardiovascular development. Trends Cardiovasc Med 10:345–352PubMedGoogle Scholar
  11. 11.
    Chan SS, Shi X, Toyama A, Arpke RW, Dandapat A, Iacovino M, Kang J, Le G, Hagen HR, Garry DJ et al (2013) Mesp1 patterns mesoderm into cardiac, hematopoietic, or skeletal myogenic progenitors in a context-dependent manner. Cell Stem Cell 12:587–601. doi:10.1016/j.stem.2013.03.004 PubMedGoogle Scholar
  12. 12.
    Morin S, Charron F, Robitaille L, Nemer M (2000) GATA-dependent recruitment of MEF2 proteins to target promoters. EMBO J 19:2046–2055. doi:10.1093/emboj/19.9.2046 PubMedGoogle Scholar
  13. 13.
    Belaguli NS, Sepulveda JL, Nigam V, Charron F, Nemer M, Schwartz RJ (2000) Cardiac tissue enriched factors serum response factor and GATA-4 are mutual coregulators. Mol Cell Biol 20:7550–7558PubMedCentralPubMedGoogle Scholar
  14. 14.
    Ghosh TK, Song FF, Packham EA, Buxton S, Robinson TE, Ronksley J, Self T, Bonser AJ, Brook JD (2009) Physical interaction between TBX5 and MEF2C is required for early heart development. Mol Cell Biol 8:2205–2218Google Scholar
  15. 15.
    Ieda M, Fu JD, Delgado-Olguin P, Vedantham V, Hayashi Y, Bruneau BG, Srivastava D (2010) Direct reprogramming of fibroblasts into functional cardiomyocytes by defined factors. Cell 142:375–386. doi:10.1016/j.cell.2010.07.002 PubMedCentralPubMedGoogle Scholar
  16. 16.
    Vincentz JW, Barnes RM, Firulli AB (2011) Hand factors as regulators of cardiac morphogenesis and implications for congenital heart defects. Birth Defects Res A Clin Mol Teratol 91:485–494. doi:10.1002/bdra.20796 PubMedCentralPubMedGoogle Scholar
  17. 17.
    Mauro A (1961) Satellite cell of skeletal muscle fibers. J Biophys Biochem Cytol 9:493–495PubMedCentralPubMedGoogle Scholar
  18. 18.
    Tedesco FS, Dellavalle A, Diaz-Manera J, Messina G, Cossu G (2010) Repairing skeletal muscle: regenerative potential of skeletal muscle stem cells. J Clin Invest 120:11–19. doi:10.1172/JCI40373 PubMedCentralPubMedGoogle Scholar
  19. 19.
    Beauchamp JR, Heslop L, Yu DS, Tajbakhsh S, Kelly RG, Wernig A, Buckingham ME, Partridge TA, Zammit PS (2000) Expression of CD34 and Myf5 defines the majority of quiescent adult skeletal muscle satellite cells. J Cell Biol 151:1221–1234PubMedGoogle Scholar
  20. 20.
    Zammit PS, Golding JP, Nagata Y, Hudon V, Partridge TA, Beauchamp JR (2004) Muscle satellite cells adopt divergent fates: a mechanism for self-renewal? J Cell Biol 166:347–357. doi:10.1083/jcb.200312007 PubMedGoogle Scholar
  21. 21.
    Asakura A, Komaki M, Rudnicki M (2001) Muscle satellite cells are multipotential stem cells that exhibit myogenic, osteogenic, and adipogenic differentiation. Differentiation 68:245–253PubMedGoogle Scholar
  22. 22.
    Csete M, Walikonis J, Slawny N, Wei Y, Korsnes S, Doyle JC, Wold B (2001) Oxygen-mediated regulation of skeletal muscle satellite cell proliferation and adipogenesis in culture. J Cell Physiol 189:189–196. doi:10.1002/jcp.10016 PubMedGoogle Scholar
  23. 23.
    Day K, Shefer G, Shearer A, Yablonka-Reuveni Z (2010) The depletion of skeletal muscle satellite cells with age is concomitant with reduced capacity of single progenitors to produce reserve progeny. Dev Biol 340:330–343. doi:10.1016/j.ydbio.2010.01.006 PubMedCentralPubMedGoogle Scholar
  24. 24.
    Starkey JD, Yamamoto M, Yamamoto S, Goldhamer DJ (2011) Skeletal muscle satellite cells are committed to myogenesis and do not spontaneously adopt nonmyogenic fates. J Histochem Cytochem 59:33–46. doi:10.1369/jhc.2010.956995 PubMedGoogle Scholar
  25. 25.
    Ono Y, Calhabeu F, Morgan JE, Katagiri T, Amthor H, Zammit PS (2011) BMP signalling permits population expansion by preventing premature myogenic differentiation in muscle satellite cells. Cell Death Differ 18:222–234. doi:10.1038/cdd.2010.95 PubMedGoogle Scholar
  26. 26.
    Braun T, Rudnicki MA, Arnold HH, Jaenisch R (1992) Targeted inactivation of the muscle regulatory gene Myf-5 results in abnormal rib development and perinatal death. Cell 71:369–382PubMedGoogle Scholar
  27. 27.
    Rudnicki MA, Schnegelsberg PN, Stead RH, Braun T, Arnold HH, Jaenisch R (1993) MyoD or Myf-5 is required for the formation of skeletal muscle. Cell 75:1351–1359PubMedGoogle Scholar
  28. 28.
    Zhang Y, Fujii J, Phillips MS, Chen HS, Karpati G, Yee WC, Schrank B, Cornblath DR, Boylan KB, MacLennan DH (1995) Characterization of cDNA and genomic DNA encoding SERCA1, the Ca(2+)-ATPase of human fast-twitch skeletal muscle sarcoplasmic reticulum, and its elimination as a candidate gene for Brody disease. Genomics 30:415–424. doi:10.1006/geno.1995.1259 PubMedGoogle Scholar
  29. 29.
    Kassar-Duchossoy L, Gayraud-Morel B, Gomes D, Rocancourt D, Buckingham M, Shinin V, Tajbakhsh S (2004) Mrf4 determines skeletal muscle identity in Myf5: Myod double-mutant mice. Nature 431:466–471. doi:10.1038/nature02876 PubMedGoogle Scholar
  30. 30.
    Valdez MR, Richardson JA, Klein WH, Olson EN (2000) Failure of Myf5 to support myogenic differentiation without myogenin, MyoD, and MRF4. Dev Biol 219:287–298. doi:10.1006/dbio.2000.9621 PubMedGoogle Scholar
  31. 31.
    Parker MH, von Maltzahn J, Bakkar N, Al-Joubori B, Ishibashi J, Guttridge D, Rudnicki MA (2012) MyoD-dependent regulation of NF-kappaB activity couples cell-cycle withdrawal to myogenic differentiation. Skelet Muscle 2:6. doi:10.1186/2044-5040-2-6 PubMedCentralPubMedGoogle Scholar
  32. 32.
    Imai S, Johnson FB, Marciniak RA, McVey M, Park PU, Guarente L (2000) Sir2: an NAD-dependent histone deacetylase that connects chromatin silencing, metabolism, and aging. Cold Spring Harb Symp Quant Biol 65:297–302PubMedGoogle Scholar
  33. 33.
    Fulco M, Schiltz RL, Iezzi S, King MT, Zhao P, Kashiwaya Y, Hoffman E, Veech RL, Sartorelli V (2003) Sir2 regulates skeletal muscle differentiation as a potential sensor of the redox state. Mol Cell 12:51–62PubMedGoogle Scholar
  34. 34.
    Fulco M, Cen Y, Zhao P, Hoffman EP, McBurney MW, Sauve AA, Sartorelli V (2008) Glucose restriction inhibits skeletal myoblast differentiation by activating SIRT1 through AMPK-mediated regulation of Nampt. Dev Cell 14:661–673. doi:10.1016/j.devcel.2008.02.004 PubMedCentralPubMedGoogle Scholar
  35. 35.
    Rathbone CR, Booth FW, Lees SJ (2009) Sirt1 increases skeletal muscle precursor cell proliferation. Eur J Cell Biol 88:35–44. doi:10.1016/j.ejcb.2008.08.003 PubMedCentralPubMedGoogle Scholar
  36. 36.
    Palacios D, Mozzetta C, Consalvi S, Caretti G, Saccone V, Proserpio V, Marquez VE, Valente S, Mai A, Forcales SV et al (2010) TNF/p38alpha/polycomb signaling to Pax7 locus in satellite cells links inflammation to the epigenetic control of muscle regeneration. Cell Stem Cell 7:455–469. doi:10.1016/j.stem.2010.08.013 PubMedCentralPubMedGoogle Scholar
  37. 37.
    Kim HK, Lee YS, Sivaprasad U, Malhotra A, Dutta A (2006) Muscle-specific microRNA miR-206 promotes muscle differentiation. J Cell Biol 174:677–687. doi:10.1083/jcb.200603008 PubMedGoogle Scholar
  38. 38.
    Crist CG, Montarras D, Pallafacchina G, Rocancourt D, Cumano A, Conway SJ, Buckingham M (2009) Muscle stem cell behavior is modified by microRNA-27 regulation of Pax3 expression. Proc Natl Acad Sci USA 106:13383–13387. doi:10.1073/pnas.0900210106 PubMedGoogle Scholar
  39. 39.
    Cheung TH, Quach NL, Charville GW, Liu L, Park L, Edalati A, Yoo B, Hoang P, Rando TA (2012) Maintenance of muscle stem-cell quiescence by microRNA-489. Nature 482:524–528. doi:10.1038/nature10834 PubMedCentralPubMedGoogle Scholar
  40. 40.
    van Leeuwen S, Mikkers H (2010) Long non-coding RNAs: guardians of development. Differentiation 80:175–183. doi:10.1016/j.diff.2010.07.003 PubMedGoogle Scholar
  41. 41.
    Cesana M, Cacchiarelli D, Legnini I, Santini T, Sthandier O, Chinappi M, Tramontano A, Bozzoni I (2011) A long noncoding RNA controls muscle differentiation by functioning as a competing endogenous RNA. Cell 147:358–369. doi:10.1016/j.cell.2011.09.028 PubMedCentralPubMedGoogle Scholar
  42. 42.
    Quattrocelli M, Cassano M, Crippa S, Perini I, Sampaolesi M (2010) Cell therapy strategies and improvements for muscular dystrophy. Cell Death Differ 17:1222–1229. doi:10.1038/cdd.2009.160 PubMedGoogle Scholar
  43. 43.
    Sampaolesi M, Torrente Y, Innocenzi A, Tonlorenzi R, D’Antona G, Pellegrino MA, Barresi R, Bresolin N, De Angelis MG, Campbell KP et al (2003) Cell therapy of alpha-sarcoglycan null dystrophic mice through intra-arterial delivery of mesoangioblasts. Science 301:487–492. doi:10.1126/science.1082254 PubMedGoogle Scholar
  44. 44.
    Sampaolesi M, Blot S, D’Antona G, Granger N, Tonlorenzi R, Innocenzi A, Mognol P, Thibaud JL, Galvez BG, Barthelemy I et al (2006) Mesoangioblast stem cells ameliorate muscle function in dystrophic dogs. Nature 444:574–579. doi:10.1038/nature05282 PubMedGoogle Scholar
  45. 45.
    Dellavalle A, Sampaolesi M, Tonlorenzi R, Tagliafico E, Sacchetti B, Perani L, Innocenzi A, Galvez BG, Messina G, Morosetti R et al (2007) Pericytes of human skeletal muscle are myogenic precursors distinct from satellite cells. Nat Cell Biol 9:255–267. doi:10.1038/ncb1542 PubMedGoogle Scholar
  46. 46.
    Minasi MG, Riminucci M, De Angelis L, Borello U, Berarducci B, Innocenzi A, Caprioli A, Sirabella D, Baiocchi M, De Maria R et al (2002) The meso-angioblast: a multipotent, self-renewing cell that originates from the dorsal aorta and differentiates into most mesodermal tissues. Development 129:2773–2783PubMedGoogle Scholar
  47. 47.
    Tonlorenzi R, Dellavalle A, Schnapp E, Cossu G, Sampaolesi M (2007) Isolation and characterization of mesoangioblasts from mouse, dog, and human tissues. Curr Protoc Stem Cell Biol Chapter 2:Unit 2B 1. doi:10.1002/9780470151808.sc02b01s3 PubMedGoogle Scholar
  48. 48.
    Quattrocelli M, Palazzolo G, Perini I, Crippa S, Cassano M, Sampaolesi M (2012) Mouse and human mesoangioblasts: isolation and characterization from adult skeletal muscles. Methods Mol Biol 798:65–76. doi:10.1007/978-1-61779-343-1_4 PubMedGoogle Scholar
  49. 49.
    Relaix F, Montarras D, Zaffran S, Gayraud-Morel B, Rocancourt D, Tajbakhsh S, Mansouri A, Cumano A, Buckingham M (2006) Pax3 and Pax7 have distinct and overlapping functions in adult muscle progenitor cells. J Cell Biol 172:91–102. doi:10.1083/jcb.200508044 PubMedGoogle Scholar
  50. 50.
    Mitchell KJ, Pannerec A, Cadot B, Parlakian A, Besson V, Gomes ER, Marazzi G, Sassoon DA (2010) Identification and characterization of a non-satellite cell muscle resident progenitor during postnatal development. Nat Cell Biol 12:257–266. doi:10.1038/ncb2025 PubMedGoogle Scholar
  51. 51.
    Joe AW, Yi L, Natarajan A, Le Grand F, So L, Wang J, Rudnicki MA, Rossi FM (2010) Muscle injury activates resident fibro/adipogenic progenitors that facilitate myogenesis. Nat Cell Biol 12:153–163. doi:10.1038/ncb2015 PubMedGoogle Scholar
  52. 52.
    Uezumi A, Fukada S, Yamamoto N, Takeda S, Tsuchida K (2010) Mesenchymal progenitors distinct from satellite cells contribute to ectopic fat cell formation in skeletal muscle. Nat Cell Biol 12:143–152. doi:10.1038/ncb2014 PubMedGoogle Scholar
  53. 53.
    Liu W, Liu Y, Lai X, Kuang S (2012) Intramuscular adipose is derived from a non-Pax3 lineage and required for efficient regeneration of skeletal muscles. Dev Biol 361:27–38. doi:10.1016/j.ydbio.2011.10.011 PubMedCentralPubMedGoogle Scholar
  54. 54.
    Mozzetta C, Consalvi S, Saccone V, Tierney M, Diamantini A, Mitchell KJ, Marazzi G, Borsellino G, Battistini L, Sassoon D et al (2013) Fibroadipogenic progenitors mediate the ability of HDAC inhibitors to promote regeneration in dystrophic muscles of young, but not old Mdx mice. EMBO Mol Med 5:626–639. doi:10.1002/emmm.201202096 PubMedCentralPubMedGoogle Scholar
  55. 55.
    Beltrami AP, Urbanek K, Kajstura J, Yan SM, Finato N, Bussani R, Nadal-Ginard B, Silvestri F, Leri A, Beltrami CA et al (2001) Evidence that human cardiac myocytes divide after myocardial infarction. N Engl J Med 344:1750–1757. doi:10.1056/NEJM200106073442303 PubMedGoogle Scholar
  56. 56.
    Bergmann O, Bhardwaj RD, Bernard S, Zdunek S, Barnabe-Heider F, Walsh S, Zupicich J, Alkass K, Buchholz BA, Druid H et al (2009) Evidence for cardiomyocyte renewal in humans. Science 324:98–102. doi:10.1126/science.1164680 PubMedCentralPubMedGoogle Scholar
  57. 57.
    Senyo SE, Steinhauser ML, Pizzimenti CL, Yang VK, Cai L, Wang M, Wu TD, Guerquin-Kern JL, Lechene CP, Lee RT (2013) Mammalian heart renewal by pre-existing cardiomyocytes. Nature 493:433–436. doi:10.1038/nature11682 PubMedCentralPubMedGoogle Scholar
  58. 58.
    Hsieh PC, Segers VF, Davis ME, MacGillivray C, Gannon J, Molkentin JD, Robbins J, Lee RT (2007) Evidence from a genetic fate-mapping study that stem cells refresh adult mammalian cardiomyocytes after injury. Nat Med 13:970–974. doi:10.1038/nm1618 PubMedCentralPubMedGoogle Scholar
  59. 59.
    Anversa P, Kajstura J, Rota M, Leri A (2013) Regenerating new heart with stem cells. J Clin Invest 123:62–70. doi:10.1172/JCI63068 PubMedCentralPubMedGoogle Scholar
  60. 60.
    Urbanek K, Cesselli D, Rota M, Nascimbene A, De Angelis A, Hosoda T, Bearzi C, Boni A, Bolli R, Kajstura J et al (2006) Stem cell niches in the adult mouse heart. Proc Natl Acad Sci USA 103:9226–9231. doi:10.1073/pnas.0600635103 PubMedGoogle Scholar
  61. 61.
    Beltrami AP, Barlucchi L, Torella D, Baker M, Limana F, Chimenti S, Kasahara H, Rota M, Musso E, Urbanek K et al (2003) Adult cardiac stem cells are multipotent and support myocardial regeneration. Cell 114:763–776PubMedGoogle Scholar
  62. 62.
    Hosoda T, D’Amario D, Cabral-Da-Silva MC, Zheng H, Padin-Iruegas ME, Ogorek B, Ferreira-Martins J, Yasuzawa-Amano S, Amano K, Ide-Iwata N et al (2009) Clonality of mouse and human cardiomyogenesis in vivo. Proc Natl Acad Sci USA 106:17169–17174. doi:10.1073/pnas.0903089106 PubMedGoogle Scholar
  63. 63.
    Chugh AR, Beache GM, Loughran JH, Mewton N, Elmore JB, Kajstura J, Pappas P, Tatooles A, Stoddard MF, Lima JA, Slaughter MS, Anversa P, Bolli R (2012) Administration of cardiac stem cells in patients with ischemic cardiomyopathy: the SCIPIO trial: surgical aspects and interim analysis of myocardial function and viability by magnetic resonance. Circulation 126(11 Suppl 1):S54–S64. doi:10.1161/CIRCULATIONAHA.112.092627 PubMedCentralPubMedGoogle Scholar
  64. 64.
    Gonzalez A, Rota M, Nurzynska D, Misao Y, Tillmanns J, Ojaimi C, Padin-Iruegas ME, Muller P, Esposito G, Bearzi C et al (2008) Activation of cardiac progenitor cells reverses the failing heart senescent phenotype and prolongs lifespan. Circ Res 102:597–606. doi:10.1161/CIRCRESAHA.107.165464 PubMedGoogle Scholar
  65. 65.
    Torella D, Rota M, Nurzynska D, Musso E, Monsen A, Shiraishi I, Zias E, Walsh K, Rosenzweig A, Sussman MA et al (2004) Cardiac stem cell and myocyte aging, heart failure, and insulin-like growth factor-1 overexpression. Circ Res 94:514–524. doi:10.1161/01.RES.0000117306.10142.50 PubMedGoogle Scholar
  66. 66.
    Linke A, Muller P, Nurzynska D, Casarsa C, Torella D, Nascimbene A, Castaldo C, Cascapera S, Bohm M, Quaini F et al (2005) Stem cells in the dog heart are self-renewing, clonogenic, and multipotent and regenerate infarcted myocardium, improving cardiac function. Proc Natl Acad Sci USA 102:8966–8971. doi:10.1073/pnas.0502678102 PubMedGoogle Scholar
  67. 67.
    Urbanek K, Torella D, Sheikh F, De Angelis A, Nurzynska D, Silvestri F, Beltrami CA, Bussani R, Beltrami AP, Quaini F et al (2005) Myocardial regeneration by activation of multipotent cardiac stem cells in ischemic heart failure. Proc Natl Acad Sci USA 102:8692–8697. doi:10.1073/pnas.0500169102 PubMedGoogle Scholar
  68. 68.
    Oh H, Chi X, Bradfute SB, Mishina Y, Pocius J, Michael LH, Behringer RR, Schwartz RJ, Entman ML, Schneider MD (2004) Cardiac muscle plasticity in adult and embryo by heart-derived progenitor cells. Ann N Y Acad Sci 1015:182–189. doi:10.1196/annals.1302.015 PubMedGoogle Scholar
  69. 69.
    Oh H, Bradfute SB, Gallardo TD, Nakamura T, Gaussin V, Mishina Y, Pocius J, Michael LH, Behringer RR, Garry DJ et al (2003) Cardiac progenitor cells from adult myocardium: homing, differentiation, and fusion after infarction. Proc Natl Acad Sci USA 100:12313–12318. doi:10.1073/pnas.2132126100 PubMedGoogle Scholar
  70. 70.
    Matsuura K, Honda A, Nagai T, Fukushima N, Iwanaga K, Tokunaga M, Shimizu T, Okano T, Kasanuki H, Hagiwara N et al (2009) Transplantation of cardiac progenitor cells ameliorates cardiac dysfunction after myocardial infarction in mice. J Clin Invest 119:2204–2217. doi:10.1172/JCI37456 PubMedCentralPubMedGoogle Scholar
  71. 71.
    Matsuura K, Nagai T, Nishigaki N, Oyama T, Nishi J, Wada H, Sano M, Toko H, Akazawa H, Sato T et al (2004) Adult cardiac Sca-1-positive cells differentiate into beating cardiomyocytes. J Biol Chem 279:11384–11391. doi:10.1074/jbc.M310822200 PubMedGoogle Scholar
  72. 72.
    Wang X, Hu Q, Nakamura Y, Lee J, Zhang G, From AH, Zhang J (2006) The role of the sca-1+/CD31- cardiac progenitor cell population in postinfarction left ventricular remodeling. Stem Cells 24:1779–1788. doi:10.1634/stemcells.2005-0386 PubMedGoogle Scholar
  73. 73.
    Messina E, De Angelis L, Frati G, Morrone S, Chimenti S, Fiordaliso F, Salio M, Battaglia M, Latronico MV, Coletta M et al (2004) Isolation and expansion of adult cardiac stem cells from human and murine heart. Circ Res 95:911–921. doi:10.1161/01.RES.0000147315.71699.51 PubMedGoogle Scholar
  74. 74.
    Smith RR, Barile L, Cho HC, Leppo MK, Hare JM, Messina E, Giacomello A, Abraham MR, Marban E (2007) Regenerative potential of cardiosphere-derived cells expanded from percutaneous endomyocardial biopsy specimens. Circulation 115:896–908. doi:10.1161/CIRCULATIONAHA.106.655209 PubMedGoogle Scholar
  75. 75.
    Malliaras K, Li TS, Luthringer D, Terrovitis J, Cheng K, Chakravarty T, Galang G, Zhang Y, Schoenhoff F, Van Eyk J et al (2012) Safety and efficacy of allogeneic cell therapy in infarcted rats transplanted with mismatched cardiosphere-derived cells. Circulation 125:100–112. doi:10.1161/CIRCULATIONAHA.111.042598 PubMedCentralPubMedGoogle Scholar
  76. 76.
    Makkar RR, Smith RR, Cheng K, Malliaras K, Thomson LE, Berman D, Czer LS, Marban L, Mendizabal A, Johnston PV et al (2012) Intracoronary cardiosphere-derived cells for heart regeneration after myocardial infarction (CADUCEUS): a prospective, randomised phase 1 trial. Lancet 379:895–904. doi:10.1016/S0140-6736(12)60195-0 PubMedGoogle Scholar
  77. 77.
    Moretti A, Caron L, Nakano A, Lam JT, Bernshausen A, Chen Y, Qyang Y, Bu L, Sasaki M, Martin-Puig S et al (2006) Multipotent embryonic isl1+ progenitor cells lead to cardiac, smooth muscle, and endothelial cell diversification. Cell 127:1151–1165. doi:10.1016/j.cell.2006.10.029 PubMedGoogle Scholar
  78. 78.
    Bu L, Jiang X, Martin-Puig S, Caron L, Zhu S, Shao Y, Roberts DJ, Huang PL, Domian IJ, Chien KR (2009) Human ISL1 heart progenitors generate diverse multipotent cardiovascular cell lineages. Nature 460:113–117. doi:10.1038/nature08191 PubMedGoogle Scholar
  79. 79.
    Laugwitz KL, Moretti A, Lam J, Gruber P, Chen Y, Woodard S, Lin LZ, Cai CL, Lu MM, Reth M et al (2005) Postnatal isl1+ cardioblasts enter fully differentiated cardiomyocyte lineages. Nature 433:647–653. doi:10.1038/nature03215 PubMedGoogle Scholar
  80. 80.
    Zhou B, Ma Q, Rajagopal S, Wu SM, Domian I, Rivera-Feliciano J, Jiang D, von Gise A, Ikeda S, Chien KR et al (2008) Epicardial progenitors contribute to the cardiomyocyte lineage in the developing heart. Nature 454:109–113. doi:10.1038/nature07060 PubMedCentralPubMedGoogle Scholar
  81. 81.
    Smart N, Risebro CA, Melville AA, Moses K, Schwartz RJ, Chien KR, Riley PR (2007) Thymosin beta4 induces adult epicardial progenitor mobilization and neovascularization. Nature 445:177–182. doi:10.1038/nature05383 PubMedGoogle Scholar
  82. 82.
    Smart N, Bollini S, Dube KN, Vieira JM, Zhou B, Davidson S, Yellon D, Riegler J, Price AN, Lythgoe MF et al (2011) De novo cardiomyocytes from within the activated adult heart after injury. Nature 474:640–644. doi:10.1038/nature10188 PubMedCentralPubMedGoogle Scholar
  83. 83.
    Galvez BG, Covarello D, Tolorenzi R, Brunelli S, Dellavalle A, Crippa S, Mohammed SA, Scialla L, Cuccovillo I, Molla F et al (2009) Human cardiac mesoangioblasts isolated from hypertrophic cardiomyopathies are greatly reduced in proliferation and differentiation potency. Cardiovasc Res 83:707–716. doi:10.1093/cvr/cvp159 PubMedGoogle Scholar
  84. 84.
    Galvez BG, Sampaolesi M, Barbuti A, Crespi A, Covarello D, Brunelli S, Dellavalle A, Crippa S, Balconi G, Cuccovillo I et al (2008) Cardiac mesoangioblasts are committed, self-renewable progenitors, associated with small vessels of juvenile mouse ventricle. Cell Death Differ 15:1417–1428. doi:10.1038/cdd.2008.75 PubMedGoogle Scholar
  85. 85.
    Casssano M, Berardi E, Crippa S, Toelen J, Barthelemy I, Micheletti R, Chuah M, Vandendriessche T, Debyser Z, Blot S et al (2012) Alteration of cardiac progenitor cell potency in GRMD dogs. Cell Transpl 21:1945–1967. doi:10.3727/096368912X638919 Google Scholar
  86. 86.
    Chun JL, O’Brien R, Song MH, Wondrasch BF, Berry SE (2013) Injection of vessel-derived stem cells prevents dilated cardiomyopathy and promotes angiogenesis and endogenous cardiac stem cell proliferation in mdx/utrn−/− but not aged mdx mouse models for duchenne muscular dystrophy. Stem Cells Transl Med 2:68–80. doi:10.5966/sctm.2012-0107 PubMedCentralPubMedGoogle Scholar
  87. 87.
    Wang L, Kamath A, Frye J, Iwamoto GA, Chun JL, Berry SE (2012) Aorta-derived mesoangioblasts differentiate into the oligodendrocytes by inhibition of the rho kinase signaling pathway. Stem Cells Dev 21:1069–1089. doi:10.1089/scd.2011.0124 PubMedGoogle Scholar
  88. 88.
    Mendez-Ferrer S, Ellison GM, Torella D, Nadal-Ginard B (2006) Resident progenitors and bone marrow stem cells in myocardial renewal and repair. Nat Clin Pract Cardiovasc Med 3(Suppl 1):S83–S89. doi:10.1038/ncpcardio0415 PubMedGoogle Scholar
  89. 89.
    Herzog EL, Chai L, Krause DS (2003) Plasticity of marrow-derived stem cells. Blood 102:3483–3493. doi:10.1182/blood-2003-05-1664 PubMedGoogle Scholar
  90. 90.
    Wakitani S, Saito T, Caplan AI (1995) Myogenic cells derived from rat bone marrow mesenchymal stem cells exposed to 5-azacytidine. Muscle Nerve 18:1417–1426. doi:10.1002/mus.880181212 PubMedGoogle Scholar
  91. 91.
    Gridley DS, Pecaut MJ (2006) Whole-body irradiation and long-term modification of bone marrow-derived cell populations by low- and high-LET radiation. In Vivo 20:781–789PubMedGoogle Scholar
  92. 92.
    Haynesworth SE, Baber MA, Caplan AI (1996) Cytokine expression by human marrow-derived mesenchymal progenitor cells in vitro: effects of dexamethasone and IL-1 alpha. J Cell Physiol 166:585–592. doi:10.1002/(SICI)1097-4652(199603)166:3<585:AID-JCP13>3.0.CO;2-6 PubMedGoogle Scholar
  93. 93.
    Sordi V, Malosio ML, Marchesi F, Mercalli A, Melzi R, Giordano T, Belmonte N, Ferrari G, Leone BE, Bertuzzi F et al (2005) Bone marrow mesenchymal stem cells express a restricted set of functionally active chemokine receptors capable of promoting migration to pancreatic islets. Blood 106:419–427. doi:10.1182/blood-2004-09-3507 PubMedGoogle Scholar
  94. 94.
    Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, Moorman MA, Simonetti DW, Craig S, Marshak DR (1999) Multilineage potential of adult human mesenchymal stem cells. Science 284:143–147PubMedGoogle Scholar
  95. 95.
    Ferrari G, Cusella-De Angelis G, Coletta M, Paolucci E, Stornaiuolo A, Cossu G, Mavilio F (1998) Muscle regeneration by bone marrow-derived myogenic progenitors. Science 279:1528–1530PubMedGoogle Scholar
  96. 96.
    Asakura A, Rudnicki MA (2002) Side population cells from diverse adult tissues are capable of in vitro hematopoietic differentiation. Exp Hematol 30:1339–1345PubMedGoogle Scholar
  97. 97.
    Polesskaya A, Seale P, Rudnicki MA (2003) Wnt signaling induces the myogenic specification of resident CD45+ adult stem cells during muscle regeneration. Cell 113:841–852PubMedGoogle Scholar
  98. 98.
    LaBarge MA, Blau HM (2002) Biological progression from adult bone marrow to mononucleate muscle stem cell to multinucleate muscle fiber in response to injury. Cell 111:589–601PubMedGoogle Scholar
  99. 99.
    Partridge T (2005) Versatility and commitment in muscle. J Physiol 562:646. doi:10.1113/jphysiol.2004.080671 PubMedGoogle Scholar
  100. 100.
    Wernig G, Janzen V, Schafer R, Zweyer M, Knauf U, Hoegemeier O, Mundegar RR, Garbe S, Stier S, Franz T et al (2005) The vast majority of bone-marrow-derived cells integrated into mdx muscle fibers are silent despite long-term engraftment. Proc Natl Acad Sci USA 102:11852–11857. doi:10.1073/pnas.0502507102 PubMedGoogle Scholar
  101. 101.
    Salah-Mohellibi N, Millet G, Andre-Schmutz I, Desforges B, Olaso R, Roblot N, Courageot S, Bensimon G, Cavazzana-Calvo M, Melki J (2006) Bone marrow transplantation attenuates the myopathic phenotype of a muscular mouse model of spinal muscular atrophy. Stem Cells 24:2723–2732. doi:10.1634/stemcells.2006-0170 PubMedGoogle Scholar
  102. 102.
    Dezawa M, Ishikawa H, Itokazu Y, Yoshihara T, Hoshino M, Takeda S, Ide C, Nabeshima Y (2005) Bone marrow stromal cells generate muscle cells and repair muscle degeneration. Science 309:314–317. doi:10.1126/science.1110364 PubMedGoogle Scholar
  103. 103.
    Orlic D, Kajstura J, Chimenti S, Jakoniuk I, Anderson SM, Li B, Pickel J, McKay R, Nadal-Ginard B, Bodine DM et al (2001) Bone marrow cells regenerate infarcted myocardium. Nature 410:701–705. doi:10.1038/35070587 PubMedGoogle Scholar
  104. 104.
    Lapidos KA, Chen YE, Earley JU, Heydemann A, Huber JM, Chien M, Ma A, McNally EM (2004) Transplanted hematopoietic stem cells demonstrate impaired sarcoglycan expression after engraftment into cardiac and skeletal muscle. J Clin Invest 114:1577–1585. doi:10.1172/JCI23071 PubMedCentralPubMedGoogle Scholar
  105. 105.
    Kudo FA, Nishibe T, Nishibe M, Yasuda K (2003) Autologous transplantation of peripheral blood endothelial progenitor cells (CD34+) for therapeutic angiogenesis in patients with critical limb ischemia. Int Angiol 22:344–348PubMedGoogle Scholar
  106. 106.
    Kawamoto A, Gwon HC, Iwaguro H, Yamaguchi JI, Uchida S, Masuda H, Silver M, Ma H, Kearney M, Isner JM et al (2001) Therapeutic potential of ex vivo expanded endothelial progenitor cells for myocardial ischemia. Circulation 103:634–637PubMedGoogle Scholar
  107. 107.
    Badorff C, Brandes RP, Popp R, Rupp S, Urbich C, Aicher A, Fleming I, Busse R, Zeiher AM, Dimmeler S (2003) Transdifferentiation of blood-derived human adult endothelial progenitor cells into functionally active cardiomyocytes. Circulation 107:1024–1032PubMedGoogle Scholar
  108. 108.
    Tzahor E, Lassar AB (2001) Wnt signals from the neural tube block ectopic cardiogenesis. Genes Dev 15:255–260PubMedGoogle Scholar
  109. 109.
    Tirosh-Finkel L, Elhanany H, Rinon A, Tzahor E (2006) Mesoderm progenitor cells of common origin contribute to the head musculature and the cardiac outflow tract. Development 133:1943–1953. doi:10.1242/dev.02365 PubMedGoogle Scholar
  110. 110.
    Winitsky SO, Gopal TV, Hassanzadeh S, Takahashi H, Gryder D, Rogawski MA, Takeda K, Yu ZX, Xu YH, Epstein ND (2005) Adult murine skeletal muscle contains cells that can differentiate into beating cardiomyocytes in vitro. PLoS Biol 3:e87. doi:10.1371/journal.pbio.0030087 PubMedCentralPubMedGoogle Scholar
  111. 111.
    Tamaki T, Akatsuka A, Ando K, Nakamura Y, Matsuzawa H, Hotta T, Roy RR, Edgerton VR (2002) Identification of myogenic-endothelial progenitor cells in the interstitial spaces of skeletal muscle. J Cell Biol 157:571–577. doi:10.1083/jcb.200112106 PubMedGoogle Scholar
  112. 112.
    Tamaki T, Uchiyama Y, Okada Y, Ishikawa T, Sato M, Akatsuka A, Asahara T (2005) Functional recovery of damaged skeletal muscle through synchronized vasculogenesis, myogenesis, and neurogenesis by muscle-derived stem cells. Circulation 112:2857–2866. doi:10.1161/CIRCULATIONAHA.105.554832 PubMedGoogle Scholar
  113. 113.
    Tamaki T, Akatsuka A, Okada Y, Uchiyama Y, Tono K, Wada M, Hoshi A, Iwaguro H, Iwasaki H, Oyamada A et al (2008) Cardiomyocyte formation by skeletal muscle-derived multi-myogenic stem cells after transplantation into infarcted myocardium. PLoS One 3:e1789. doi:10.1371/journal.pone.0001789 PubMedCentralPubMedGoogle Scholar
  114. 114.
    Crippa S, Cassano M, Sampaolesi M (2012) Role of miRNAs in muscle stem cell biology: proliferation, differentiation and death. Curr Pharm Des 18:1718–1729PubMedGoogle Scholar
  115. 115.
    Crippa S, Cassano M, Messina G, Galli D, Galvez BG, Curk T, Altomare C, Ronzoni F, Toelen J, Gijsbers R et al (2011) miR669a and miR669q prevent skeletal muscle differentiation in postnatal cardiac progenitors. J Cell Biol 193:1197–1212. doi:10.1083/jcb.201011099 PubMedGoogle Scholar
  116. 116.
    Murry CE, Wiseman RW, Schwartz SM, Hauschka SD (1996) Skeletal myoblast transplantation for repair of myocardial necrosis. J Clin Invest 98:2512–2523. doi:10.1172/JCI119070 PubMedCentralPubMedGoogle Scholar
  117. 117.
    Taylor DA, Atkins BZ, Hungspreugs P, Jones TR, Reedy MC, Hutcheson KA, Glower DD, Kraus WE (1998) Regenerating functional myocardium: improved performance after skeletal myoblast transplantation. Nat Med 4:929–933PubMedGoogle Scholar
  118. 118.
    Menasche P, Hagege AA, Scorsin M, Pouzet B, Desnos M, Duboc D, Schwartz K, Vilquin JT, Marolleau JP (2001) Myoblast transplantation for heart failure. Lancet 357:279–280. doi:10.1016/S0140-6736(00)03617-5 PubMedGoogle Scholar
  119. 119.
    Gavira JJ, Herreros J, Perez A, Garcia-Velloso MJ, Barba J, Martin-Herrero F, Canizo C, Martin-Arnau A, Marti-Climent JM, Hernandez M et al (2006) Autologous skeletal myoblast transplantation in patients with nonacute myocardial infarction: 1-year follow-up. J Thorac Cardiovasc Surg 131:799–804. doi:10.1016/j.jtcvs.2005.11.030 PubMedGoogle Scholar
  120. 120.
    Menasche P, Alfieri O, Janssens S, McKenna W, Reichenspurner H, Trinquart L, Vilquin JT, Marolleau JP, Seymour B, Larghero J et al (2008) The myoblast autologous grafting in ischemic cardiomyopathy (MAGIC) trial: first randomized placebo-controlled study of myoblast transplantation. Circulation 117:1189–1200. doi:10.1161/CIRCULATIONAHA.107.734103 PubMedGoogle Scholar
  121. 121.
    Narita T, Shintani Y, Ikebe C, Kaneko M, Harada N, Tshuma N, Takahashi K, Campbell NG, Coppen SR, Yashiro K et al (2012) The use of cell-sheet technique eliminates arrhythmogenicity of skeletal myoblast-based therapy to the heart with enhanced therapeutic effects. Int J Cardiol. doi:10.1016/j.ijcard.2012.09.081 Google Scholar
  122. 122.
    Uchinaka A, Kawaguchi N, Hamada Y, Mori S, Miyagawa S, Saito A, Sawa Y, Matsuura N (2013) Transplantation of myoblast sheets that secrete the novel peptide SVVYGLR improves cardiac function in failing hearts. Cardiovasc Res. doi:10.1093/cvr/cvt088 PubMedGoogle Scholar

Copyright information

© Springer Basel 2013

Authors and Affiliations

  • Domiziana Costamagna
    • 1
  • Mattia Quattrocelli
    • 1
  • Robin Duelen
    • 1
  • Vardine Sahakyan
    • 1
  • Ilaria Perini
    • 1
  • Giacomo Palazzolo
    • 1
  • Maurilio Sampaolesi
    • 1
  1. 1.Translational Cardiomyology Lab, Department of Development and Regeneration, Stem Cell Institute Leuven, Embryo and Stem Cell BiologyKU LeuvenLeuvenBelgium

Personalised recommendations