Fetal stem cells and skeletal muscle regeneration: A therapeutic approach

Frontiers in Aging Neuroscience

Volumn 6, Issue AUG, 2014, Pages

  Michela, Pozzobon ^a   Chiara, Franzin ^a   Martina, Piccoli ^a   Paolo, De Coppi ^b  

^a Fondazione Istituto di Ricerca Pediatrica Città della Speranza   (Italy)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Amniotic fluid; Cell therapy; Cord blood; Fetal cells; Muscle dystrophies; Placenta

Indexed keywords

AMNION FLUID; ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CORD BLOOD STEM CELL TRANSPLANTATION; FETAL STEM CELL; HUMAN; IMMUNOMODULATION; IN VIVO STUDY; MUSCLE DISEASE; MUSCLE REGENERATION; NONHUMAN; PLACENTA; SKELETAL MUSCLE; SKELETAL MUSCLE SATELLITE CELL; STEM CELL EXPANSION; STEM CELL NICHE; STEM CELL TRANSPLANTATION; UMBILICAL CORD BLOOD; WHARTON JELLY;

EID: 84906228496     PISSN: None     EISSN: 16634365     Source Type: Journal    
DOI: 10.3389/fnagi.2014.00222     Document Type: Article

References (81)

1. Akizawa, Y., Kanno, H., Kawamichi, Y., Matsuda, Y., Ohta, H., Fujii, H., Matsui, H., and Saito, K. (2013). Enhanced expression of myogenic differentiation factors and skeletal muscle proteins in human amnion-derived cells via the forced expression of MYOD1. Brain Dev 35, 349-355. doi: S0387-7604(12)00130-1 [pii] 10.1016/j.braindev.2012.05.012.
2. Anzalone, R., Lo Iacono, M., Corrao, S., Magno, F., Loria, T., Cappello, F., Zummo, G., Farina, F., and La Rocca, G. (2010). New emerging potentials for human Wharton's jelly mesenchymal stem cells: immunological features and hepatocyte-like differentiative capacity. Stem Cells Dev 19, 423-438. doi: 10.1089/scd.2009.0299.
3. Ballen, K.K. (2005). New trends in umbilical cord blood transplantation. Blood 105, 3786-3792. doi: 2004-10-4125 [pii] 10.1182/blood-2004-10-4125.
4. Battula, V.L., Treml, S., Abele, H., and Buhring, H.J. (2008). Prospective isolation and characterization of mesenchymal stem cells from human placenta using a frizzled-9-specific monoclonal antibody. Differentiation 76, 326-336. doi: S0301-4681(09)60077-3 [pii] 10.1111/j.1432-0436.2007.00225.x.
5. Berardi, E., Annibali, D., Cassano, M., Crippa, S., and Sampaolesi, M. (2014). Molecular and cellbased therapies for muscle degenerations: a road under construction. Front Physiol 5, 119. doi: 10.3389/fphys.2014.00119.
6. Bittner, R.E., Anderson, L.V., Burkhardt, E., Bashir, R., Vafiadaki, E., Ivanova, S., Raffelsberger, T., Maerk, I., Hoger, H., Jung, M., Karbasiyan, M., Storch, M., Lassmann, H., Moss, J.A., Davison, K., Harrison, R., Bushby, K.M., and Reis, A. (1999). Dysferlin deletion in SJL mice (SJL-Dysf) defines a natural model for limb girdle muscular dystrophy 2B. Nat Genet 23, 141-142. doi: 10.1038/13770.
7. Bollini, S., Cheung, K.K., Riegler, J., Dong, X., Smart, N., Ghionzoli, M., Loukogeorgakis, S.P., Maghsoudlou, P., Dube, K.N., Riley, P.R., Lythgoe, M.F., and De Coppi, P. (2011). Amniotic fluid stem cells are cardioprotective following acute myocardial infarction. Stem Cells Dev 20, 1985-1994. doi: 10.1089/scd.2010.0424.
8. Brooke, G., Tong, H., Levesque, J.P., and Atkinson, K. (2008). Molecular trafficking mechanisms of multipotent mesenchymal stem cells derived from human bone marrow and placenta. Stem Cells Dev 17, 929-940. doi: 10.1089/scd.2007.0156.
9. Broxmeyer, H.E. (2010). Will iPS cells enhance therapeutic applicability of cord blood cells and banking? Cell Stem Cell 6, 21-24. doi: S1934-5909(09)00631-6 [pii] 10.1016/j.stem.2009.12.008.
10. Broxmeyer, H.E., Douglas, G.W., Hangoc, G., Cooper, S., Bard, J., English, D., Arny, M., Thomas, L., and Boyse, E.A. (1989). Human umbilical cord blood as a potential source of transplantable hematopoietic stem/progenitor cells. Proc Natl Acad Sci U S A 86, 3828-3832.
11. Brunstein, C.G., Baker, K.S., and Wagner, J.E. (2007). Umbilical cord blood transplantation for myeloid malignancies. Curr Opin Hematol 14, 162-169. doi: 10.1097/MOH.0b013e32802f7da4 00062752-200703000-00012 [pii].
12. Bujang-Safawi, E., Halim, A.S., Khoo, T.L., and Dorai, A.A. (2010). Dried irradiated human amniotic membrane as a biological dressing for facial burns--a 7-year case series. Burns 36, 876-882. doi: S0305-4179(09)00413-6 [pii] 10.1016/j.burns.2009.07.001.
13. Bulfield, G., Siller, W.G., Wight, P.A., and Moore, K.J. (1984). X chromosome-linked muscular dystrophy (mdx) in the mouse. Proc Natl Acad Sci U S A 81, 1189-1192.
14. Cairo, M.S., and Wagner, J.E. (1997). Placental and/or umbilical cord blood: an alternative source of hematopoietic stem cells for transplantation. Blood 90, 4665-4678.
15. Cargnoni, A., Gibelli, L., Tosini, A., Signoroni, P.B., Nassuato, C., Arienti, D., Lombardi, G., Albertini, A., Wengler, G.S., and Parolini, O. (2009). Transplantation of allogeneic and xenogeneic placenta-derived cells reduces bleomycin-induced lung fibrosis. Cell Transplant 18, 405-422. doi: 10.3727/096368909788809857.
16. Carraro, G., Perin, L., Sedrakyan, S., Giuliani, S., Tiozzo, C., Lee, J., Turcatel, G., De Langhe, S.P., Driscoll, B., Bellusci, S., Minoo, P., Atala, A., De Filippo, R.E., and Warburton, D. (2008). Human amniotic fluid stem cells can integrate and differentiate into epithelial lung lineages. Stem Cells 26, 2902-2911. doi: 2008-0090 [pii] 10.1634/stemcells.2008-0090.
17. Chang, Y.J., Shih, D.T., Tseng, C.P., Hsieh, T.B., Lee, D.C., and Hwang, S.M. (2006). Disparate mesenchyme-lineage tendencies in mesenchymal stem cells from human bone marrow and umbilical cord blood. Stem Cells 24, 679-685. doi: 2004-0308 [pii] 10.1634/stemcells.2004-0308.
18. Cifuentes-Diaz, C., Frugier, T., Tiziano, F.D., Lacene, E., Roblot, N., Joshi, V., Moreau, M.H., and Melki, J. (2001). Deletion of murine SMN exon 7 directed to skeletal muscle leads to severe muscular dystrophy. J Cell Biol 152, 1107-1114.
19. Conconi, M.T., Burra, P., Di Liddo, R., Calore, C., Turetta, M., Bellini, S., Bo, P., Nussdorfer, G.G., and Parnigotto, P.P. (2006). CD105(+) cells from Wharton's jelly show in vitro and in vivo myogenic differentiative potential. Int J Mol Med 18, 1089-1096.
20. Darabi, R., Arpke, R.W., Irion, S., Dimos, J.T., Grskovic, M., Kyba, M., and Perlingeiro, R.C. (2012). Human ES- and iPS-derived myogenic progenitors restore DYSTROPHIN and improve contractility upon transplantation in dystrophic mice. Cell Stem Cell 10, 610-619. doi: S1934-5909(12)00074-4 [pii] 10.1016/j.stem.2012.02.015.
21. De Coppi, P., Bartsch, G., Jr., Siddiqui, M.M., Xu, T., Santos, C.C., Perin, L., Mostoslavsky, G., Serre, A.C., Snyder, E.Y., Yoo, J.J., Furth, M.E., Soker, S., and Atala, A. (2007). Isolation of amniotic stem cell lines with potential for therapy. Nat Biotechnol 25, 100-106. doi: nbt1274 [pii] 10.1038/nbt1274.
22. Dekaris, I., and Gabric, N. (2009). Preparation and preservation of amniotic membrane. Dev Ophthalmol 43, 97-104. doi: 000223842 [pii] 10.1159/000223842.
23. Dellavalle, A., Maroli, G., Covarello, D., Azzoni, E., Innocenzi, A., Perani, L., Antonini, S., Sambasivan, R., Brunelli, S., Tajbakhsh, S., and Cossu, G. (2011). Pericytes resident in postnatal skeletal muscle differentiate into muscle fibres and generate satellite cells. Nat Commun 2, 499. doi: ncomms1508 [pii] 10.1038/ncomms1508.
24. Di Trapani, M., Bassi, G., Ricciardi, M., Fontana, E., Bifari, F., Pacelli, L., Giacomello, L., Pozzobon, M., Feron, F., De Coppi, P., Anversa, P., Fumagalli, G., Decimo, I., Menard, C., Tarte, K., and Krampera, M. (2013). Comparative study of immune regulatory properties of stem cells derived from different tissues. Stem Cells Dev 22, 2990-3002. doi: 10.1089/scd.2013.0204.
25. Ditadi, A., De Coppi, P., Picone, O., Gautreau, L., Smati, R., Six, E., Bonhomme, D., Ezine, S., Frydman, R., Cavazzana-Calvo, M., and Andre-Schmutz, I. (2009). Human and murine amniotic fluid c-Kit+Lin- cells display hematopoietic activity. Blood 113, 3953-3960. doi: blood-2008-10-182105 [pii] 10.1182/blood-2008-10-182105.
26. Duclos, F., Straub, V., Moore, S.A., Venzke, D.P., Hrstka, R.F., Crosbie, R.H., Durbeej, M., Lebakken, C.S., Ettinger, A.J., Van Der Meulen, J., Holt, K.H., Lim, L.E., Sanes, J.R., Davidson, B.L., Faulkner, J.A., Williamson, R., and Campbell, K.P. (1998). Progressive muscular dystrophy in alpha-sarcoglycan-deficient mice. J Cell Biol 142, 1461-1471.
27. Ende, M., and Ende, N. (1972). Hematopoietic transplantation by means of fetal (cord) blood. A new method. Va Med Mon (1918) 99, 276-280.
28. Feldkotter, M., Schwarzer, V., Wirth, R., Wienker, T.F., and Wirth, B. (2002). Quantitative analyses of SMN1 and SMN2 based on real-time lightCycler PCR: fast and highly reliable carrier testing and prediction of severity of spinal muscular atrophy. Am J Hum Genet 70, 358-368. doi: S0002-9297(07)63951-2 [pii] 10.1086/338627.
29. Ferguson, V.L., and Dodson, R.B. (2009). Bioengineering aspects of the umbilical cord. Eur J Obstet Gynecol Reprod Biol 144 Suppl 1, S108-113. doi: S0301-2115(09)00133-X [pii] 10.1016/j.ejogrb.2009.02.024.
30. Ferrari, G., Cusella-De Angelis, G., Coletta, M., Paolucci, E., Stornaiuolo, A., Cossu, G., and Mavilio, F. (1998). Muscle regeneration by bone marrow-derived myogenic progenitors. Science 279, 1528-1530.
31. Filareto, A., Darabi, R., and Perlingeiro, R.C. (2013). Engraftment of ES-Derived Myogenic Progenitors in a Severe Mouse Model of Muscular Dystrophy. J Stem Cell Res Ther 10. doi: 10.4172/2157-7633.S10-001.
32. Fukuchi, Y., Nakajima, H., Sugiyama, D., Hirose, I., Kitamura, T., and Tsuji, K. (2004). Human placenta-derived cells have mesenchymal stem/progenitor cell potential. Stem Cells 22, 649- 658. doi: 10.1634/stemcells.22-5-649 22/5/649 [pii].
33. Gekas, J., Walther, G., Skuk, D., Bujold, E., Harvey, I., and Bertrand, O.F. (2010). In vitro and in vivo study of human amniotic fluid-derived stem cell differentiation into myogenic lineage. Clin Exp Med 10, 1-6. doi: 10.1007/s10238-009-0060-2.
34. Gilliam, T.C., Brzustowicz, L.M., Castilla, L.H., Lehner, T., Penchaszadeh, G.K., Daniels, R.J., Byth, B.C., Knowles, J., Hislop, J.E., Shapira, Y., and et al. (1990). Genetic homogeneity between acute and chronic forms of spinal muscular atrophy. Nature 345, 823-825. doi: 10.1038/345823a0.
35. Gussoni, E., Soneoka, Y., Strickland, C.D., Buzney, E.A., Khan, M.K., Flint, A.F., Kunkel, L.M., and Mulligan, R.C. (1999). Dystrophin expression in the mdx mouse restored by stem cell transplantation. Nature 401, 390-394. doi: 10.1038/43919.
36. Huang, Y.C., Yang, Z.M., Chen, X.H., Tan, M.Y., Wang, J., Li, X.Q., Xie, H.Q., and Deng, L. (2009). Isolation of mesenchymal stem cells from human placental decidua basalis and resistance to hypoxia and serum deprivation. Stem Cell Rev 5, 247-255. doi: 10.1007/s12015-009-9069-x.
37. Hwang, W.Y., Samuel, M., Tan, D., Koh, L.P., Lim, W., and Linn, Y.C. (2007). A meta-analysis of unrelated donor umbilical cord blood transplantation versus unrelated donor bone marrow transplantation in adult and pediatric patients. Biol Blood Marrow Transplant 13, 444-453. doi: S1083-8791(06)00757-9 [pii] 10.1016/j.bbmt.2006.11.005.
38. In 'T Anker, P.S., Noort, W.A., Scherjon, S.A., Kleijburg-Van Der Keur, C., Kruisselbrink, A.B., Van Bezooijen, R.L., Beekhuizen, W., Willemze, R., Kanhai, H.H., and Fibbe, W.E. (2003). Mesenchymal stem cells in human second-trimester bone marrow, liver, lung, and spleen exhibit a similar immunophenotype but a heterogeneous multilineage differentiation potential. Haematologica 88, 845-852.
39. Izsvak, Z., Chuah, M.K., Vandendriessche, T., and Ivics, Z. (2009). Efficient stable gene transfer into human cells by the Sleeping Beauty transposon vectors. Methods 49, 287-297. doi: S1046-2023(09)00168-6 [pii] 10.1016/j.ymeth.2009.07.001.
40. Kawamichi, Y., Cui, C.H., Toyoda, M., Makino, H., Horie, A., Takahashi, Y., Matsumoto, K., Saito, H., Ohta, H., Saito, K., and Umezawa, A. (2010). Cells of extraembryonic mesodermal origin confer human dystrophin in the mdx model of Duchenne muscular dystrophy. J Cell Physiol 223, 695-702. doi: 10.1002/jcp.22076.
41. Kharraz, Y., Guerra, J., Pessina, P., Serrano, A.L., and Munoz-Canoves, P. (2014). Understanding the Process of Fibrosis in Duchenne Muscular Dystrophy. Biomed Res Int 2014, 965631. doi: 10.1155/2014/965631.
42. Kim, D.K., Fujiki, Y., Fukushima, T., Ema, H., Shibuya, A., and Nakauchi, H. (1999). Comparison of hematopoietic activities of human bone marrow and umbilical cord blood CD34 positive and negative cells. Stem Cells 17, 286-294. doi: 10.1002/stem.170286.
43. Kim, J.A., Shon, Y.H., Lim, J.O., Yoo, J.J., Shin, H.I., and Park, E.K. (2013). MYOD mediates skeletal myogenic differentiation of human amniotic fluid stem cells and regeneration of muscle injury. Stem Cell Res Ther 4, 147. doi: scrt358 [pii] 10.1186/scrt358.
44. Kong, K.Y., Ren, J., Kraus, M., Finklestein, S.P., and Brown, R.H., Jr. (2004). Human umbilical cord blood cells differentiate into muscle in sjl muscular dystrophy mice. Stem Cells 22, 981-993. doi: 22/6/981 [pii] 10.1634/stemcells.22-6-981.
45. Koponen, J.K., Kekarainen, T., S, E.H., Laitinen, A., Nystedt, J., Laine, J., and Yla-Herttuala, S. (2007). Umbilical cord blood-derived progenitor cells enhance muscle regeneration in mouse hindlimb ischemia model. Mol Ther 15, 2172-2177. doi: 6300302 [pii] 10.1038/sj.mt.6300302.
46. Kucia, M., Halasa, M., Wysoczynski, M., Baskiewicz-Masiuk, M., Moldenhawer, S., Zuba-Surma, E., Czajka, R., Wojakowski, W., Machalinski, B., and Ratajczak, M.Z. (2007). Morphological and molecular characterization of novel population of CXCR4+ SSEA-4+ Oct-4+ very small embryonic-like cells purified from human cord blood: preliminary report. Leukemia 21, 297-303. doi: 2404470 [pii] 10.1038/sj.leu.2404470.
47. Lapan, A.D., Rozkalne, A., and Gussoni, E. (2012). Human fetal skeletal muscle contains a myogenic side population that expresses the melanoma cell-adhesion molecule. Hum Mol Genet 21, 3668-3680. doi: dds196 [pii] 10.1093/hmg/dds196.
48. Lefebvre, S., Burglen, L., Reboullet, S., Clermont, O., Burlet, P., Viollet, L., Benichou, B., Cruaud, C., Millasseau, P., Zeviani, M., and et al. (1995). Identification and characterization of a spinal muscular atrophy-determining gene. Cell 80, 155-165. doi: 0092-8674(95)90460-3 [pii].
49. Leung, D.G., and Wagner, K.R. (2013). Therapeutic advances in muscular dystrophy. Ann Neurol 74, 404-411. doi: 10.1002/ana.23989.
50. Liu, J., Wallace, L.M., Garwick-Coppens, S.E., Sloboda, D.D., Davis, C.S., Hakim, C.H., Hauser, M.A., Brooks, S.V., Mendell, J.R., and Harper, S.Q. (2014). RNAi-mediated Gene Silencing of Mutant Myotilin Improves Myopathy in LGMD1A Mice. Mol Ther Nucleic Acids 3, e160. doi: mtna201413 [pii] 10.1038/mtna.2014.13.
51. Lorson, C.L., Strasswimmer, J., Yao, J.M., Baleja, J.D., Hahnen, E., Wirth, B., Le, T., Burghes, A.H., and Androphy, E.J. (1998). SMN oligomerization defect correlates with spinal muscular atrophy severity. Nat Genet 19, 63-66. doi: 10.1038/ng0598-63.
52. Ma, X., Zhang, S., Zhou, J., Chen, B., Shang, Y., Gao, T., Wang, X., Xie, H., and Chen, F. (2012). Clone-derived human AF-amniotic fluid stem cells are capable of skeletal myogenic differentiation in vitro and in vivo. J Tissue Eng Regen Med 6, 598-613. doi: 10.1002/term.462.
53. Mcguckin, C., Jurga, M., Ali, H., Strbad, M., and Forraz, N. (2008). Culture of embryonic-like stem cells from human umbilical cord blood and onward differentiation to neural cells in vitro. Nat Protoc 3, 1046-1055. doi: nprot.2008.69 [pii] 10.1038/nprot.2008.69.
54. Mcguckin, C.P., Forraz, N., Baradez, M.O., Navran, S., Zhao, J., Urban, R., Tilton, R., and Denner, L. (2005). Production of stem cells with embryonic characteristics from human umbilical cord blood. Cell Prolif 38, 245-255. doi: CPR346 [pii] 10.1111/j.1365-2184.2005.00346.x.
55. Miki, T., Lehmann, T., Cai, H., Stolz, D.B., and Strom, S.C. (2005). Stem cell characteristics of amniotic epithelial cells. Stem Cells 23, 1549-1559. doi: 2004-0357 [pii] 10.1634/stemcells.2004-0357.
56. Miki, T., Mitamura, K., Ross, M.A., Stolz, D.B., and Strom, S.C. (2007). Identification of stem cell marker-positive cells by immunofluorescence in term human amnion. J Reprod Immunol 75, 91-96. doi: S0165-0378(07)00067-8 [pii] 10.1016/j.jri.2007.03.017.
57. Mitsuhashi, S., and Kang, P.B. (2012). Update on the genetics of limb girdle muscular dystrophy. Semin Pediatr Neurol 19, 211-218. doi: S1071-9091(12)00076-9 [pii] 10.1016/j.spen.2012.09.008.
58. Nicole, S., Desforges, B., Millet, G., Lesbordes, J., Cifuentes-Diaz, C., Vertes, D., Cao, M.L., De Backer, F., Languille, L., Roblot, N., Joshi, V., Gillis, J.M., and Melki, J. (2003). Intact satellite cells lead to remarkable protection against Smn gene defect in differentiated skeletal muscle. J Cell Biol 161, 571-582. doi: 10.1083/jcb.200210117 jcb.200210117 [pii].
59. Nunes, V.A., Cavacana, N., Canovas, M., Strauss, B.E., and Zatz, M. (2007). Stem cells from umbilical cord blood differentiate into myotubes and express dystrophin in vitro only after exposure to in vivo muscle environment. Biol Cell 99, 185-196. doi: BC20060075 [pii] 10.1042/BC20060075.
60. Park, T.S., Gavina, M., Chen, C.W., Sun, B., Teng, P.N., Huard, J., Deasy, B.M., Zimmerlin, L., and Peault, B. (2010). Placental perivascular cells for human muscle regeneration. Stem Cells Dev 20, 451-463. doi: 10.1089/scd.2010.0354.
61. Partridge, T.A., Morgan, J.E., Coulton, G.R., Hoffman, E.P., and Kunkel, L.M. (1989). Conversion of mdx myofibres from dystrophin-negative to -positive by injection of normal myoblasts. Nature 337, 176-179. doi: 10.1038/337176a0.
62. Pesce, M., Orlandi, A., Iachininoto, M.G., Straino, S., Torella, A.R., Rizzuti, V., Pompilio, G., Bonanno, G., Scambia, G., and Capogrossi, M.C. (2003). Myoendothelial differentiation of human umbilical cord blood-derived stem cells in ischemic limb tissues. Circ Res 93, e51- 62. doi: 10.1161/01.RES.0000090624.04507.45 01.RES.0000090624.04507.45 [pii].
63. Piccoli, M., Franzin, C., Bertin, E., Urbani, L., Blaauw, B., Repele, A., Taschin, E., Cenedese, A., Zanon, G.F., Andre-Schmutz, I., Rosato, A., Melki, J., Cavazzana-Calvo, M., Pozzobon, M., and De Coppi, P. (2012). Amniotic fluid stem cells restore the muscle cell niche in a HSACre, Smn(F7/F7) mouse model. Stem Cells 30, 1675-1684. doi: 10.1002/stem.1134.
64. Pipes, B.L., Tsang, T., Peng, S.X., Fiederlein, R., Graham, M., and Harris, D.T. (2006). Telomere length changes after umbilical cord blood transplant. Transfusion 46, 1038-1043. doi: TRF00839 [pii] 10.1111/j.1537-2995.2006.00839.x.
65. Pozzobon, M., Piccoli, M., and De Coppi, P. (2014). Stem cells from fetal membranes and amniotic fluid: markers for cell isolation and therapy. Cell Tissue Bank 15, 199-211. doi: 10.1007/s10561-014-9428-y.
66. Preitschopf, A., Zwickl, H., Li, K., Lubec, G., Joo, G., Rosner, M., Hengstschlager, M., and Mikula, M. (2012). Chondrogenic differentiation of amniotic fluid stem cells and their potential for regenerative therapy. Stem Cell Rev 8, 1267-1274. doi: 10.1007/s12015-012-9405-4.
67. Prusa, A.R., and Hengstschlager, M. (2002). Amniotic fluid cells and human stem cell research: a new connection. Med Sci Monit 8, RA253-257. doi: 2933 [pii].
68. Prusa, A.R., Marton, E., Rosner, M., Bernaschek, G., and Hengstschlager, M. (2003). Oct-4- expressing cells in human amniotic fluid: a new source for stem cell research? Hum Reprod 18, 1489-1493.
69. Rota, C., Imberti, B., Pozzobon, M., Piccoli, M., De Coppi, P., Atala, A., Gagliardini, E., Xinaris, C., Benedetti, V., Fabricio, A.S., Squarcina, E., Abbate, M., Benigni, A., Remuzzi, G., and Morigi, M. (2011). Human amniotic fluid stem cell preconditioning improves their regenerative potential. Stem Cells Dev 21, 1911-1923. doi: 10.1089/scd.2011.0333.
70. Sacco, A., Mourkioti, F., Tran, R., Choi, J., Llewellyn, M., Kraft, P., Shkreli, M., Delp, S., Pomerantz, J.H., Artandi, S.E., and Blau, H.M. (2010). Short telomeres and stem cell exhaustion model Duchenne muscular dystrophy in mdx/mTR mice. Cell 143, 1059-1071. doi: S0092-8674(10)01361-9 [pii] 10.1016/j.cell.2010.11.039.
71. Sakai, H., Sato, T., Sakurai, H., Yamamoto, T., Hanaoka, K., Montarras, D., and Sehara-Fujisawa, A. (2013). Fetal skeletal muscle progenitors have regenerative capacity after intramuscular engraftment in dystrophin deficient mice. PLoS One 8, e63016. doi: 10.1371/journal.pone.0063016 PONE-D-13-02128 [pii].
72. Salah-Mohellibi, N., Millet, G., Andre-Schmutz, I., Desforges, B., Olaso, R., Roblot, N., Courageot, S., Bensimon, G., Cavazzana-Calvo, M., and 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: 2006-0170 [pii] 10.1634/stemcells.2006-0170.
73. Sampaolesi, M., Blot, S., D'antona, G., Granger, N., Tonlorenzi, R., Innocenzi, A., Mognol, P., Thibaud, J.L., Galvez, B.G., Barthelemy, I., Perani, L., Mantero, S., Guttinger, M., Pansarasa, O., Rinaldi, C., Cusella De Angelis, M.G., Torrente, Y., Bordignon, C., Bottinelli, R., and Cossu, G. (2006). Mesoangioblast stem cells ameliorate muscle function in dystrophic dogs. Nature 444, 574-579. doi: nature05282 [pii] 10.1038/nature05282.
74. Schoemans, H., Theunissen, K., Maertens, J., Boogaerts, M., Verfaillie, C., and Wagner, J. (2006). Adult umbilical cord blood transplantation: a comprehensive review. Bone Marrow Transplant 38, 83-93. doi: 1705403 [pii] 10.1038/sj.bmt.1705403.
75. Tedesco, F.S., Gerli, M.F., Perani, L., Benedetti, S., Ungaro, F., Cassano, M., Antonini, S., Tagliafico, E., Artusi, V., Longa, E., Tonlorenzi, R., Ragazzi, M., Calderazzi, G., Hoshiya, H., Cappellari, O., Mora, M., Schoser, B., Schneiderat, P., Oshimura, M., Bottinelli, R., Sampaolesi, M., Torrente, Y., Broccoli, V., and Cossu, G. (2012). Transplantation of genetically corrected human iPSC-derived progenitors in mice with limb-girdle muscular dystrophy. Sci Transl Med 4, 140ra189. doi: 4/140/140ra89 [pii] 10.1126/scitranslmed.3003541.
76. Toda, A., Okabe, M., Yoshida, T., and Nikaido, T. (2007). The potential of amniotic membrane/amnion-derived cells for regeneration of various tissues. J Pharmacol Sci 105, 215-228. doi: JST.JSTAGE/jphs/CR0070034 [pii].
77. Wang, M., Yang, Y., Yang, D., Luo, F., Liang, W., Guo, S., and Xu, J. (2009). The immunomodulatory activity of human umbilical cord blood-derived mesenchymal stem cells in vitro. Immunology 126, 220-232. doi: IMM2891 [pii] 10.1111/j.1365-2567.2008.02891.x.
78. Wilschut, K.J., Ling, V.B., and Bernstein, H.S. (2012). Concise review: stem cell therapy for muscular dystrophies. Stem Cells Transl Med 1, 833-842. doi: sctm.2012-0071 [pii] 10.5966/sctm.2012-0071.
79. Yang, D.Y., Sheu, M.L., Su, H.L., Cheng, F.C., Chen, Y.J., Chen, C.J., Chiu, W.T., Yiin, J.J., Sheehan, J., and Pan, H.C. (2012). Dual regeneration of muscle and nerve by intravenous administration of human amniotic fluid-derived mesenchymal stem cells regulated by stromal cell-derived factor-1alpha in a sciatic nerve injury model. J Neurosurg 116, 1357- 1367. doi: 10.3171/2012.2.JNS111360.
80. Zhao, Y., Jiang, Z., Zhao, T., Ye, M., Hu, C., Yin, Z., Li, H., Zhang, Y., Diao, Y., Li, Y., Chen, Y., Sun, X., Fisk, M.B., Skidgel, R., Holterman, M., Prabhakar, B., and Mazzone, T. (2012). Reversal of type 1 diabetes via islet beta cell regeneration following immune modulation by cord blood-derived multipotent stem cells. BMC Med 10, 3. doi: 1741-7015-10-3 [pii] 10.1186/1741-7015-10-3.
81. Zuba-Surma, E.K., Klich, I., Greco, N., Laughlin, M.J., Ratajczak, J., and Ratajczak, M.Z. (2009). Optimization of isolation and further characterization of umbilical-cord-blood-derived very small embryonic/ epiblast-like stem cells (VSELs). Eur J Haematol 84, 34-46. doi: EJH1352 [pii] 10.1111/j.1600-0609.2009.01352.x.