Human muscle-derived stem/progenitor cells promote functional murine peripheral nerve regeneration

Journal of Clinical Investigation

Volumn 124, Issue 4, 2014, Pages 1745-1756

  Lavasani, Mitra ^a,b,c   Thompson, Seth D ^a,b   Pollett, Jonathan B ^a,b,d   Usas, Arvydas ^a,b   Lu, Aiping ^a,b   Stolz, Donna B ^b   Clark, Katherine A ^b   Sun, Bin ^a,b   Péault, Bruno ^a,b,e   Huard, Johnny ^a,b,c,f  

^a UNIVERSITY OF PITTSBURGH   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^c University of Pittsburgh   (United States)

^d ALLEGHENY SINGER RESEARCH INSTITUTE   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHATE BUFFERED SALINE;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CELL; CELL DIFFERENTIATION; CELL INFILTRATION; CELL ISOLATION; CONTROLLED STUDY; EXPERIMENTAL SCIATIC NERVE INJURY; FUNCTIONAL ASSESSMENT; GASTROCNEMIUS MUSCLE; GLIA CELL; GROWTH CONE; HISTOPATHOLOGY; HUMAN; HUMAN CELL; IN VITRO STUDY; MOUSE; MUSCLE ATROPHY; MUSCLE CELL; MUSCLE DERIVED STEM PROGENITOR CELL; MUSCLE MASS; MYOBLAST; NERVE ENDING; NERVE FIBER REGENERATION; NERVE REGENERATION; NONHUMAN; NORMAL HUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; SCHWANN CELL; SCIATIC NERVE INJURY; SKELETAL MUSCLE; STEM CELL; STEM CELL TRANSPLANTATION; YOUNG ADULT;

ADULT; ADULT STEM CELLS; ANIMALS; CELL DIFFERENTIATION; DISEASE MODELS, ANIMAL; HETEROGRAFTS; HUMANS; MICE; MUSCLE, SKELETAL; MUSCULAR ATROPHY; NERVE REGENERATION; NEURAL STEM CELLS; NEUROGLIA; NEURONS; SCHWANN CELLS; SCIATIC NERVE; TRANSCRIPTOME; YOUNG ADULT;

EID: 84897545125     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI44071     Document Type: Article

References (75)

1. Millesi H. Progress in peripheral nerve reconstruction. World J Surg. 1990;14(6):733-747.
2. Fu SY, Gordon T. The cellular and molecular basis of peripheral nerve regeneration. Mol Neurobiol. 1997;14(1-2):67-116. (Pubitemid 127720197)
3. Evans GR. Challenges to nerve regeneration. Semin Surg Oncol. 2000;19(3):312-318. (Pubitemid 32052856)
4. Dezawa M, Takahashi I, Esaki M, Takano M, Sawada H. Sciatic nerve regeneration in rats induced by transplantation of in vitro differentiated bone-marrow stromal cells. Eur J Neurosci. 2001;14(11):1771-1776. (Pubitemid 35463694)
5. Tohill M, Mantovani C, Wiberg M, Terenghi G. Rat bone marrow mesenchymal stem cells express glial markers and stimulate nerve regeneration. Neurosci Lett. 2004;362(3):200-203. (Pubitemid 38648941)
6. Amoh Y, et al. Human hair follicle pluripotent stem (hfPS) cells promote regeneration of peripheral-nerve injury: an advantageous alternative to ES and iPS cells. J Cell Biochem. 2009;107(5):1016-1020.
7. Walsh SK, Gordon T, Addas BM, Kemp SW, Midha R. Skin-derived precursor cells enhance peripheral nerve regeneration following chronic denervation. Exp Neurol. 2010;223(1):221-228.
8. Schaakxs D, Kalbermatten DF, Raffoul W, Wiberg M, Kingham PJ. Regenerative cell injection in denervated muscle reduces atrophy and enhances recovery following nerve repair. Muscle Nerve. 2013;47(5):691-701.
9. Reynolds BA, Weiss S. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science. 1992;255(5052):1707-1710.
10. Palmer TD, Ray J, Gage FH. FGF-2-responsive neuronal progenitors reside in proliferative and quiescent regions of the adult rodent brain. Mol Cell Neurosci. 1995;6(5):474-486.
11. Gritti A, et al. Multipotential stem cells from the adult mouse brain proliferate and self-renew in response to basic fibroblast growth factor. J Neurosci. 1996;16(3):1091-1100.
12. Romero-Ramos M, et al. Neuronal differentiation of stem cells isolated from adult muscle. J Neurosci Res. 2002;69(6):894-907. (Pubitemid 34984706)
13. Woodbury D, Schwarz EJ, Prockop DJ, Black IB. Adult rat and human bone marrow stromal cells differentiate into neurons. J Neurosci Res. 2000;61(4):364-370. (Pubitemid 30620221)
14. Black IB, Woodbury D. Adult rat and human bone marrow stromal stem cells differentiate into neurons. Blood Cells Mol Dis. 2001;27(3):632-636. (Pubitemid 32757058)
15. Kabos P, Ehtesham M, Kabosova A, Black KL, Yu JS. Generation of neural progenitor cells from whole adult bone marrow. Exp Neurol. 2002;178(2):288-293. (Pubitemid 36062638)
16. Sanchez-Ramos JR, et al. Expression of neural markers in human umbilical cord blood. Exp Neurol. 2001;171(1):109-115. (Pubitemid 32848449)
17. Buzanska L, Machaj EK, Zablocka B, Pojda Z, Domanska-Janik K. Human cord blood-derived cells attain neuronal and glial features in vitro. J Cell Sci. 2002;115(Pt 10):2131-2138. (Pubitemid 34746379)
18. Kogler G, et al. A new human somatic stem cell from placental cord blood with intrinsic pluripotent differentiation potential. J Exp Med. 2004;200(2):123-135. (Pubitemid 38982172)
19. Toma JG, et al. Isolation of multipotent adult stem cells from the dermis of mammalian skin. Nat Cell Biol. 2001;3(9):778-784. (Pubitemid 32842682)
20. Amoh Y, et al. Implanted hair follicle stem cells form Schwann cells that support repair of severed peripheral nerves. Proc Natl Acad Sci U S A. 2005;102(49):17734-17738. (Pubitemid 41803566)
21. Hunt DP, et al. A highly enriched niche of precursor cells with neuronal and glial potential within the hair follicle dermal papilla of adult skin. Stem Cells. 2008;26(1):163-172.
22. Amoh Y, et al. Human and mouse hair follicles contain both multipotent and monopotent stem cells. Cell Cycle. 2009;8(1):176-177.
23. Safford KM, et al. Neurogenic differentiation of murine and human adipose-derived stromal cells. Biochem Biophys Res Commun. 2002;294(2):371-379. (Pubitemid 34694105)
24. Safford KM, Safford SD, Gimble JM, Shetty AK, Rice HE. Characterization of neuronal/glial differentiation of murine adipose-derived adult stromal cells. Exp Neurol. 2004;187(2):319-328. (Pubitemid 38610278)
25. Fujimura J, Ogawa R, Mizuno H, Fukunaga Y, Suzuki H. Neural differentiation of adipose-derived stem cells isolated from GFP transgenic mice. Biochem Biophys Res Commun. 2005;333(1):116-121. (Pubitemid 40813454)
26. Kingham PJ, et al. Adipose-derived stem cells differentiate into a Schwann cell phenotype and promote neurite outgrowth in vitro. Exp Neurol. 2007;207(2):267-274. (Pubitemid 47432883)
27. Xu Y, et al. Neurospheres from rat adipose-derived stem cells could be induced into functional Schwann cell-like cells in vitro. BMC Neurosci. 2008;9:21.
28. Anghileri E, et al. Neuronal differentiation potential of human adipose-derived mesenchymal stem cells. Stem Cells Dev. 2008;17(5):909-916.
29. Jang S, Cho HH, Cho YB, Park JS, Jeong HS. Functional neural differentiation of human adipose tissue-derived stem cells using bFGF and forskolin. BMC Cell Biol. 2010;11:25.
30. Karbanová J, Soukup T, Suchánek J, Pytlík R, Corbeil D, Mokrý J. Characterization of dental pulp stem cells from impacted third molars cultured in low serum-containing medium. Cells Tissues Organs. 2011;193(6):344-365.
31. Kiraly M, et al. Simultaneous PKC and cAMP activation induces differentiation of human dental pulp stem cells into functionally active neurons. Neurochem Int. 2009;55(5):323-332.
32. Tamaki T, et al. Clonal multipotency of skeletal muscle-derived stem cells between mesodermal and ectodermal lineage. Stem Cells. 2007;25(9):2283-2290. (Pubitemid 47480487)
33. Vourc'h P, et al. Isolation and characterization of cells with neurogenic potential from adult skeletal muscle. Biochem Biophys Res Commun. 2004;317(3):893-901. (Pubitemid 38481456)
34. Alessandri G, et al. Isolation and culture of human muscle-derived stem cells able to differentiate into myogenic and neurogenic cell lineages. Lancet. 2004;364(9448):1872-1883. (Pubitemid 39536091)
35. Schultz SS, Lucas PA. Human stem cells isolated from adult skeletal muscle differentiate into neural phenotypes. J Neurosci Methods. 2006;152(1-2):144-155. (Pubitemid 43343485)
36. Arsic N, Mamaeva D, Lamb NJ, Fernandez A. Muscle-derived stem cells isolated as non-adherent population give rise to cardiac, skeletal muscle and neural lineages. Exp Cell Res. 2008;314(6):1266-1280.
37. Qu-Petersen Z, et al. Identification of a novel population of muscle stem cells in mice: potential for muscle regeneration. J Cell Biol. 2002;157(5):851-864. (Pubitemid 34847822)
38. Gharaibeh B, et al. Isolation of a slowly adhering cell fraction containing stem cells from murine skeletal muscle by the preplate technique. Nat Protoc. 2008;3(9):1501-1509.
39. Lavasani M, et al. Isolation of muscle-derived stem/progenitor cells based on adhesion characteristics to collagen-coated surfaces. Methods Mol Biol. 2013;976:53-65.
40. Lee JY, et al. Clonal isolation of muscle-derived cells capable of enhancing muscle regeneration and bone healing. J Cell Biol. 2000;150(5):1085-1100.
41. Deasy BM, et al. Long-term self-renewal of postnatal muscle-derived stem cells. Mol Biol Cell. 2005;16(7):3323-3333. (Pubitemid 40962601)
42. Peng H, et al. Synergistic enhancement of bone formation and healing by stem cell-expressed VEGF and bone morphogenetic protein-4. J Clin Invest. 2002;110(6):751-759.
43. Oshima H, et al. Differential myocardial infarct repair with muscle stem cells compared to myoblasts. Mol Ther. 2005;12(6):1130-1141. (Pubitemid 41723047)
44. Payne TR, et al. Regeneration of dystrophin-expressing myocytes in the mdx heart by skeletal muscle stem cells. Gene Ther. 2005;12(16):1264-1274. (Pubitemid 41195117)
45. Kuroda R, et al. Cartilage repair using bone morphogenetic protein 4 and muscle-derived stem cells. Arthritis Rheum. 2006;54(2):433-442. (Pubitemid 43228617)
46. Cao B, et al. Muscle stem cells differentiate into haematopoietic lineages but retain myogenic potential. Nat Cell Biol. 2003;5(7):640-646. (Pubitemid 36818086)
47. Urish KL, et al. Antioxidant levels represent a major determinant in the regenerative capacity of muscle stem cells. Mol Biol Cell. 2009;20(1):509-520.
48. Vella JB, Thompson SD, Bucsek MJ, Song M, Huard J. Murine and human myogenic cells identified by elevated aldehyde dehydrogenase activity: implications for muscle regeneration and repair. PLoS One. 2011;6(12):e29226.
49. Lavasani M, et al. Muscle-derived stem/progenitor cell dysfunction limits healthspan and lifespan in a murine progeria model. Nat Commun. 2012;3:608.
50. Lavasani M, Lu A, Peng H, Cummins J, Huard J. Nerve growth factor improves the muscle regeneration capacity of muscle stem cells in dystrophic muscle. Hum Gene Ther. 2006;17(2):180-192. (Pubitemid 43262034)
51. Gao X, et al. BMP2 is superior to BMP4 for promoting human muscle-derived stem cell-mediated bone regeneration in a critical-sized calvarial defect model. Cell Transplant. 2013;22(12):2393-2408.
52. Gage FH, et al. Survival and differentiation of adult neuronal progenitor cells transplanted to the adult brain. Proc Natl Acad Sci U S A. 1995;92(25):11879-11883. (Pubitemid 26014213)
53. Rosser AE, Tyers P, ter Borg M, Dunnett SB, Svendsen CN. Co-expression of MAP-2 and GFAP in cells developing from rat EGF responsive precursor cells. Brain Res Dev Brain Res. 1997;98(2):291-295. (Pubitemid 27075287)
54. Colucci-D'Amato GL, Tino A, Pernas-Alonso R, ffrench-Mullen JM, di Porzio U. Neuronal and glial properties coexist in a novel mouse CNS immortalized cell line. Exp Cell Res. 1999;252(2):383-391. (Pubitemid 29530268)
55. Feldman DH, Thinschmidt JS, Peel AL, Papke RL, Reier PJ. Differentiation of ionic currents in CNS progenitor cells: dependence upon substrate attachment and epidermal growth factor. Exp Neurol. 1996;140(2):206-217. (Pubitemid 26254901)
56. Raff MC, Abney ER, Cohen J, Lindsay R, Noble M. Two types of astrocytes in cultures of developing rat white matter: differences in morphology, surface gangliosides, and growth characteristics. J Neurosci. 1983;3(6):1289-1300. (Pubitemid 13060724)
57. Bremer M, et al. Sox10 is required for Schwann-cell homeostasis and myelin maintenance in the adult peripheral nerve. Glia. 2011;59(7):1022-1032.
58. Dezawa M. Central and peripheral nerve regeneration by transplantation of Schwann cells and transdifferentiated bone marrow stromal cells. Anat Sci Int. 2002;77(1):12-25.
59. Maiese K, Boniece I, DeMeo D, Wagner JA. Peptide growth factors protect against ischemia in culture by preventing nitric oxide toxicity. J Neurosci. 1993;13(7):3034-3040. (Pubitemid 23199228)
60. Nozaki K, Finklestein SP, Beal MF. Basic fibroblast growth factor protects against hypoxia-ischemia and NMDA neurotoxicity in neonatal rats. J Cereb Blood Flow Metab. 1993;13(2):221-228. (Pubitemid 23067455)
61. Gharaibeh B, Lavasani M, Cummins JH, Huard J. Terminal differentiation is not a major determinant for the success of stem cell therapy - cross-talk between muscle-derived stem cells and host cells. Stem Cell Res Ther. 2011;2(4):31.
62. Gharaibeh B, Deasy B, Lavasani M, Cummins JH, Li Y, Huard J. Musculoskeletal tissue injury and repair: role of stem cells, their differentiation, and paracrine effects. In: Hill JA and Olson EN, eds. Muscle: Fundamental Biology and Mechanisms of Disease. New York, New York, USA: Elsevier Academic Press; 2012:881-897.
63. Levitt TA, Loring RH, Salpeter MM. Neuronal control of acetylcholine receptor turnover rate at a vertebrate neuromuscular junction. Science. 1980;210(4469):550-551. (Pubitemid 11162126)
64. Fu SY, Gordon T. Contributing factors to poor functional recovery after delayed nerve repair: prolonged denervation. J Neurosci. 1995;15(5 Pt 2):3886-3895.
65. Sulaiman OA, Gordon T. Effects of short- and long-term Schwann cell denervation on peripheral nerve regeneration, myelination, and size. Glia. 2000;32(3):234-246.
66. Kobayashi J, et al. The effect of duration of muscle denervation on functional recovery in the rat model. Muscle Nerve. 1997;20(7):858-866. (Pubitemid 27250672)
67. Salpeter MM, Cooper DL, Levitt-Gilmour T. Degradation rates of acetylcholine receptors can be modified in the postjunctional plasma membrane of the vertebrate neuromuscular junction. J Cell Biol. 1986;103(4):1399-1403. (Pubitemid 17174162)
68. Dorshkind K, et al. Functional status of cells from lymphoid and myeloid tissues in mice with severe combined immunodeficiency disease. J Immunol. 1984;132(4):1804-1808. (Pubitemid 14168140)
69. Shibata S, et al. Peritoneal macrophages play an important role in eliminating human cells from severe combined immunodeficient mice transplanted with human peripheral blood lymphocytes. Immunology. 1998;93(4):524-532. (Pubitemid 28172625)
70. Menendez P, Bueno C, Wang L, Bhatia M. Human embryonic stem cells: potential tool for achieving immunotolerance? Stem Cell Rev. 2005;1(2):151-158. (Pubitemid 43074200)
71. Yang XF. Immunology of stem cells and cancer stem cells. Cell Mol Immunol. 2007;4(3):161-171.
72. Radfar AJ, et al. Transplantation of virally transduced cells into the dermis of immunocompetent and immunodeficient (SCID) mice to determine gene expression profile and differential donor cell survival. Wound Repair Regen. 2000;8(6):503-510. (Pubitemid 32141454)
73. Lewin-Kowalik J, Marcol W, Kotulska K, Mandera M, Klimczak A. Prevention and management of painful neuroma. Neurol Med Chir (Tokyo). 2006;46(2):62-67. (Pubitemid 43329996)
74. Chu H, Gao J, Chen CW, Huard J, Wang Y. Injectable fibroblast growth factor-2 coacervate for persistent angiogenesis. Proc Natl Acad Sci U S A. 2011;108(33):13444-13449.
75. Inserra MM, Bloch DA, Terris DJ. Functional indices for sciatic, peroneal, and posterior tibial nerve lesions in the mouse. Microsurgery. 1998;18(2):119-124. (Pubitemid 28294803)