Denervated muscle extract promotes recovery of muscle atrophy through activation of satellite cells. An experimental study
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摘要
Purpose: The objective of the present study was to determine whether a denervated muscle extract(DmEx) could stimulate satellite cell response in denervated muscle.Methods: Wistar rats were divided into 4 groups: normal rats, normal rats treated with DmEx, denervated rats, and denervated rats treated with DmEx. The soleus muscles were examined using immunohistochemical techniques for proliferating cell nuclear antigen, desmin, and myogenic differentiation antigen(MyoD), and electron microscopy was used for analysis of the satellite cells.Results: The results indicate that while denervation causes activation of satellite cells, DmEx also induces myogenic differentiation of cells localized in the interstitial space and the formation of new muscle fibers. Although DmEx had a similar effect in nature on innervated and denervated muscles, this response was of greater magnitude in denervated vs. intact muscles.Conclusion: Our study shows that treatment of denervated rats with DmEx potentiates the myogenic response in atrophic denervated muscles.
Purpose: The objective of the present study was to determine whether a denervated muscle extract(DmEx) could stimulate satellite cell response in denervated muscle.Methods: Wistar rats were divided into 4 groups: normal rats, normal rats treated with DmEx, denervated rats, and denervated rats treated with DmEx. The soleus muscles were examined using immunohistochemical techniques for proliferating cell nuclear antigen, desmin, and myogenic differentiation antigen(MyoD), and electron microscopy was used for analysis of the satellite cells.Results: The results indicate that while denervation causes activation of satellite cells, DmEx also induces myogenic differentiation of cells localized in the interstitial space and the formation of new muscle fibers. Although DmEx had a similar effect in nature on innervated and denervated muscles, this response was of greater magnitude in denervated vs. intact muscles.Conclusion: Our study shows that treatment of denervated rats with DmEx potentiates the myogenic response in atrophic denervated muscles.
Purpose: The objective of the present study was to determine whether a denervated muscle extract(DmEx) could stimulate satellite cell response in denervated muscle.Methods: Wistar rats were divided into 4 groups: normal rats, normal rats treated with DmEx, denervated rats, and denervated rats treated with DmEx. The soleus muscles were examined using immunohistochemical techniques for proliferating cell nuclear antigen, desmin, and myogenic differentiation antigen(MyoD), and electron microscopy was used for analysis of the satellite cells.Results: The results indicate that while denervation causes activation of satellite cells, DmEx also induces myogenic differentiation of cells localized in the interstitial space and the formation of new muscle fibers. Although DmEx had a similar effect in nature on innervated and denervated muscles, this response was of greater magnitude in denervated vs. intact muscles.Conclusion: Our study shows that treatment of denervated rats with DmEx potentiates the myogenic response in atrophic denervated muscles.
引文
1.Carraro U,Rossini K,Zanin ME,Rizi C,Mayr W,Kern H.Induced myogenesis in long-term permanent denervation:perspective role in functional electrical stimulation of denervated legs in humans.Basic Appl Myol2002;12:53-64.
2.Yablonka-Reuveni Z.The skeletal muscle satellite cell:still young and fascinating at 50.J Histochem Cytochem 2011;59:1041-59.
3.Machida S,Booth FW.Regrowth of skeletal muscle atrophied from inactivity.Med Sci Sports Exerc 2004;36:52-9.
4.Kuang S,Rudnicki MA.The emerging biology of satellite cells and their therapeutic potential.Trends Mol Med 2008;14:82-91.
5.Gayraud-Morel B,Chretien F,Tajbakhsh S.Skeletal muscle as a paradigm for regenerative biology and medicine.Regen Med 2009;4:293-319.
6.Bischoff R.Control of satellite cell proliferation.In:Griggs RC,Karpati G,editors.Myoblast transfer therapy.New York,NY:Plenum Press;1990.p.147-58.
7.Bornemann A,Maier F,Kuschel R.Satellite cells as players and targets in normal and diseased muscle.Neuropediatrics 1999;30:167-75.
8.Bischoff R,Franzini-Armstrong C.Satellite and stem cells in muscle regeneration.In:Engel AG,Franzini-Armstrong C,editors.Myology.New York,NY:McGraw-Hill;2004.p.66-86.
9.Cornelison DD.Context matters:in vivo and in vitro influences on muscle satellite cell activity.J Cell Biochem 2008;105:663-9.
10.Buonanno A,Rosenthal N.Molecular control of muscle diversity and plasticity.Dev Genet 1996;19:95-107.
11.Borisov AB,Dedkov EI,Carlson BM.Interrelations of myogenic response,progressive atrophy of muscle fibers,and cell death in denervated skeletal muscle.Anat Rec 2001;264:203-18.
12.Dedkov EI,Kostrominova TY,Borisov AB,Carlson BM.Reparative myogenesis in long-term denervated skeletal muscles of adult rats results in a reduction of the satellite cell population.Anat Rec 2001;263:139-54.
13.Carlson BM,Borisov AB,Dedkov EI,Dow D,Kostrominova TY.The biology and restorative capacity of long-term denervated skeletal muscle.Basic Appl Myol 2002;12:247-54.
14.De Angelis L,Berghella L,Coletta M,Lattanzi L,Zanchi M,Cusella-De Angelis MG,et al.Skeletal myogenic progenitors originating from embryonic dorsal aorta coexpress endothelial and myogenic markers and contribute to postnatal muscle growth and regeneration.J Cell Biol1999;147:869-78.
15.Doppler K,Mittelbronn M,Bornemann A.Myogenesis in human denervated muscle biopsies.Muscle Nerve 2008;37:79-83.
16.Schmalbruch H,Lewis DM.A comparison of the morphology of denervated with aneurally regenerated soleus muscle of rat.J Muscle Res Cell Motil 1994;15:256-66.
17.Rodrigues Ade C,Schmalbruch H.Satellite cells and myonuclei in longterm denervated rat muscles.Anat Rec 1995;243:430-7.
18.Carraro U.Modulation of trophism and fiber type expression of denervated muscle by different patterns of electrical stimulation.Basic Appl Myol 2002;12:263-72.
19.Kuschel R,Yablonka-Reuveni Z,Bornemann A.Satellite cells on isolated myofibers from normal and denervated adult rat muscle.J Histochem Cytochem 1999;47:1375-84.
20.Yoshimura K,Harii K.A regenerative change during muscle adaptation to denervation in rats.J Surg Res 1999;81:139-46.
21.Schmalbruch H,Lewis DM.Dynamics of nuclei of muscle fibers and connective tissue cells in normal and denervated rat muscles.Muscle Nerve2000;23:617-26.
22.Ehrhardt J,Morgan J.Regenerative capacity of skeletal muscle.Curr Opin Neurol 2005;18:548-53.
23.Schmalbruch H.Growth and denervation response of skeletal muscle fibers of newborn rats.Muscle Nerve 1990;13:421-32.
24.Jejurikar SS,Kuzon Jr WM.Satellite cell depletion in degenerative skeletal muscle.Apoptosis 2003;8:573-8.
25.Viguie CA,Lu DX,Huang SK,Rengen H,Carlson BM.Quantitative study of the effects of long-term denervation on the extensor digitorum longus muscle of the rat.Anat Rec 1997;248:346-54.
26.Borisov AB,Dedkov EI,Carlson BM.Abortive myogenesis in denervated skeletal muscle:differentiative properties of satellite cells,their migration,and block of terminal differentiation.Anat Embryol(Berl)2005;209:269-79.
27.van der Meer SF,Jaspers RT,Jones DA,Degens H.Time-course of changes in the myonuclear domain during denervation in young-adult and old rat gastrocnemius muscle.Muscle Nerve 2011;43:212-22.
28.Jimena I,Pe~na J,Luque E,Vaamonde R.Muscle hypertrophy experimentally induced by administration of denervated muscle extract.J Neuropathol Exp Neurol 1993;52:379-86.
29.Jimena I,Pe~na J,Luque E,Ayuso F,Vaamonde R.Myotrophic effects of muscle extracts obtained at different intervals after denervation.Neuropathol Appl Neurobiol 1998;24:217-23.
30.Pe~na J,Jimena I,Luque E,Vaamonde R.New fiber formation in rat soleus muscle following administration of denervated muscle extract.J Neurol Sci 1995;128:14-21.
31.Ag€uera E,Castilla S,Luque E,Jimena I,Leiva-Cepas F,Ruz-Caracuel I,et al.Muscular hypertrophy and atrophy in normal rats provoked by the administration of normal and denervated muscle extracts.Histol Histopathol 2016;31:1367-79.
32.Finkelstein DI,Dooley PC,Luff AR.Recovery of muscle after different periods of denervation and treatments.Muscle Nerve 1993;16:769-77.
33.Cumming WJK,Fulthorpe JJ,Hudgson P,Mahon M.Color atlas of muscle pathology.London:Mosby-Wolfe;1994.p.183-8.
34.Rantanen J,Hurme T,Lukka R,Heino J,Kalimo H.Satellite cell proliferation and the expression of myogenin and desmin in regenerating skeletal muscle:evidence for two different populations of satellite cells.Lab Invest1995;72:341-7.
35.Lawson-Smith MJ,McGeachie JK.The identification of myogenic cells in skeletal muscle,with emphasis on the use of tritiated thymidine autoradiography and desmin antibodies.J Anat 1998;192:161-71.
36.Comella JX,Sanz-Rodriguez C,Aldea M,Esquerda JE.Skeletal musclederived trophic factors prevent motoneurons from entering an active cell death program in vitro.J Neurosci 1994;14:2674-86.
37.Bischoff R.Chemotaxis of skeletal muscle satellite cells.Dev Dyn1997;208:505-15.
38.Chen G,Quinn LS.Partial characterization of skeletal myoblast mitogens in mouse crushed muscle extract.J Cell Physiol 1992;153:563-74.
39.Buonanno A,Cheng J,Venepally P,Weis J,Calvo S.Activity dependent regulation of muscle genes:repressive and stimulatory effects of innervation.Acta Physiol Scand 1998;163:17-26.
40.Tatsumi R,Anderson JE,Nevoret CJ,Halevy O,Allen RE.HGF/SF is present in normal adult skeletal muscle and is capable of activating satellite cells.Dev Biol 1998;194:114-28.
41.Wan Q,Yeung SS,Cheung KK,Au SW,Lam WW,Li YH,et al.Optimizing electrical stimulation for promoting satellite cell proliferation in muscle disuse atrophy.Am J Phys Med Rehabil 2016;95:28-38.
42.Cheng L,Lai MD,Sanderson JE,Yu CM,Li M.Enhanced fusion of myoblasts with myofibers for efficient gene delivery induced by a partially purified protein fraction from rat muscle extract.Arch Biochem Biophys2005;441:141-50.
43.Allen DL,Roy RR,Edgerton VR.Myonuclear domains in muscle adaptation and disease.Muscle Nerve 1999;22:1350-60.
44.Mc Geachie JK.Sustained cell proliferation in denervated skeletal muscle of mice.Cell Tissue Res 1989;257:455-7.
45.Carlson BM.Denervation and the aging of skeletal muscle.Basic Appl Myol 2004;14:135-9.
46.Borisov AB,Dedkov EI,Carlson BM.Differentiation of activated satellite cells in denervated muscle following single fusions in situ and in cell culture.Histochem Cell Biol 2005;124:13-23.
47.Ishido M,Kami K,Masuhara M.In vivo expression patterns of MyoD,p21,and Rb proteins in myonuclei and satellite cells of denervated rat skeletal muscle.Am J Physiol Cell Physiol 2004;287:C484-93.
48.Gundersen K,Bruusgaard JC.Nuclear domains during muscle atrophy:nuclei lost or paradigm lost?J Physiol 2008;586:2675-81.
49.Murray MA,Robbins N.Cell proliferation in denervated muscle:time course,distribution and relation to disuse.Neuroscience 1982;7:1817-22.
50.Adami N,Biral D,Caccavale S,Rossini K.Histology of the long term denervated rat muscle.Basic Appl Myol 2006;16:113-4.
51.Allen RE,Rankin LL.Regulation of satellite cells during skeletal muscle growth and development.Proc Soc Exp Biol Med 1990;194:81-6.
52.Tamaki T,Akatsuka A,Ando K,Nakamura Y,Matsuzawa H,Hotta T,et al.Identification of myogenic-endothelial progenitor cells in the interstitial spaces of skeletal muscle.J Cell Biol 2002;157:571-7.
53.Tamaki T,Akatsuka A,Yoshimura S,Roy RR,Edgerton VR.New fiber formation in the interstitial spaces of rat skeletal muscle during postnatal growth.J Histochem Cytochem 2002;50:1097-111.
54.Schultz E.Changes in the satellite cells of growing muscle following denervation.Anat Rec 1978;190:299-311.
55.Lu DX,Huang SK,Carlson BM.Electron microscopic study of long-term denervated rat skeletal muscle.Anat Rec 1997;248:355-65.
56.Collins CA,Olsen I,Zammit PS,Heslop L,Petrie A,Partridge TA,et al.Stem cell function,self-renewal,and behavioral heterogeneity of cells from the adult muscle satellite cell niche.Cell 2005;122:289-301.
57.Santa Maria L,Rojas CV,Minguell JJ.Signals from damaged but not undamaged skeletal muscle induce myogenic differentiation of rat bonemarrow-derived mesenchymal stem cells.Exp Cell Res 2004;300:418-26.
58.Peng H,Huard J.Muscle-derived stem cells for musculoskeletal tissue regeneration and repair.Transpl Immunol 2004;12:311-9.
59.Peault B,Rudnicki M,Torrente Y,Cossu G,Tremblay JP,Partridge T,et al.Stem and progenitor cells in skeletal muscle development,maintenance,and therapy.Mol Ther 2007;15:867-77.
60.Otto A,Collins-Hooper H,Patel K.The origin,molecular regulation and therapeutic potential of myogenic stem cell populations.J Anat2009;215:477-97.
61.Bianco P,Cossu G.Uno,nessuno e centomila:searching for the identity of mesodermal progenitors.Exp Cell Res 1999;251:257-63.
62.Dellavalle A,Sampaolesi M,Tonlorenzi R,Tagliafico E,Sacchetti B,Perani L,et al.Pericytes of human skeletal muscle are myogenic precursors distinct from satellite cells.Nat Cell Biol 2007;9:255-67.
63.Crisan M,Yap S,Casteilla L,Chen CW,Corselli M,Park TS,et al.Aperivascular origin for mesenchymal stem cells in multiple human organs.Cell Stem Cell 2008;3:301-13.
64.Dellavalle A,Maroli G,Covarello D,Azzoni E,Innocenzi A,Perani L,et al.Pericytes resident in postnatal skeletal muscle differentiate into muscle fibres and generate satellite cells.Nat Commun 2011;2:499.doi:10.1038/ncomms1508.
65.van Haelst U.An electron microscopic study of muscle in WerdnigHoffmann’s disease.Virchows Arch A Pathol Pathol Anat1970;351:291-305.
66.de Maruenda EC,Franzini-Armstrong C.Satellite and invasive cells in frog Sartorius muscle.Tissue Cell 1978;10:749-72.
67.Hansen-Smith FM,Picou D,Golden MH.Muscle satellite cells in malnourished and nutritionally rehabilitated children.J Neurol Sci1979;41:207-21.
68.Ontell M.Evidence for myoblastic potential of satellite cells in denervated muscle.Cell Tissue Res 1975;160:345-53.
69.Laule S,Bornemann A.Ultrastructural findings at the satellite cell-myofiber border in normal and diseased human muscle biopsy specimens.Acta Neuropathol 2001;101:435-9.
70.Bittner RE,Schofer C,Weipoltshammer K,Ivanova S,Streubel B,Hauser E,et al.Recruitment of bone-marrow-derived cells by skeletal and cardiac muscle in adult dystrophic mdx mice.Anat Embryol(Berl)1999;199:391-6.
71.Skuk D,Vilquin JT,Tremblay JP.Experimental and therapeutic approaches to muscular dystrophies.Curr Opin Neurol 2002;15:563-9.
72.Kuang S,Kuroda K,Le Grand F,Rudnicki MA.Asymmetric self-renewal and commitment of satellite stem cells in muscle.Cell 2007;129:999-1010.
73.Dhawan J,Rando TA.Stem cells in postnatal myogenesis:molecular mechanisms of satellite cell quiescence,activation and replenishment.Trends Cell Biol 2005;15:666-73.
2.Yablonka-Reuveni Z.The skeletal muscle satellite cell:still young and fascinating at 50.J Histochem Cytochem 2011;59:1041-59.
3.Machida S,Booth FW.Regrowth of skeletal muscle atrophied from inactivity.Med Sci Sports Exerc 2004;36:52-9.
4.Kuang S,Rudnicki MA.The emerging biology of satellite cells and their therapeutic potential.Trends Mol Med 2008;14:82-91.
5.Gayraud-Morel B,Chretien F,Tajbakhsh S.Skeletal muscle as a paradigm for regenerative biology and medicine.Regen Med 2009;4:293-319.
6.Bischoff R.Control of satellite cell proliferation.In:Griggs RC,Karpati G,editors.Myoblast transfer therapy.New York,NY:Plenum Press;1990.p.147-58.
7.Bornemann A,Maier F,Kuschel R.Satellite cells as players and targets in normal and diseased muscle.Neuropediatrics 1999;30:167-75.
8.Bischoff R,Franzini-Armstrong C.Satellite and stem cells in muscle regeneration.In:Engel AG,Franzini-Armstrong C,editors.Myology.New York,NY:McGraw-Hill;2004.p.66-86.
9.Cornelison DD.Context matters:in vivo and in vitro influences on muscle satellite cell activity.J Cell Biochem 2008;105:663-9.
10.Buonanno A,Rosenthal N.Molecular control of muscle diversity and plasticity.Dev Genet 1996;19:95-107.
11.Borisov AB,Dedkov EI,Carlson BM.Interrelations of myogenic response,progressive atrophy of muscle fibers,and cell death in denervated skeletal muscle.Anat Rec 2001;264:203-18.
12.Dedkov EI,Kostrominova TY,Borisov AB,Carlson BM.Reparative myogenesis in long-term denervated skeletal muscles of adult rats results in a reduction of the satellite cell population.Anat Rec 2001;263:139-54.
13.Carlson BM,Borisov AB,Dedkov EI,Dow D,Kostrominova TY.The biology and restorative capacity of long-term denervated skeletal muscle.Basic Appl Myol 2002;12:247-54.
14.De Angelis L,Berghella L,Coletta M,Lattanzi L,Zanchi M,Cusella-De Angelis MG,et al.Skeletal myogenic progenitors originating from embryonic dorsal aorta coexpress endothelial and myogenic markers and contribute to postnatal muscle growth and regeneration.J Cell Biol1999;147:869-78.
15.Doppler K,Mittelbronn M,Bornemann A.Myogenesis in human denervated muscle biopsies.Muscle Nerve 2008;37:79-83.
16.Schmalbruch H,Lewis DM.A comparison of the morphology of denervated with aneurally regenerated soleus muscle of rat.J Muscle Res Cell Motil 1994;15:256-66.
17.Rodrigues Ade C,Schmalbruch H.Satellite cells and myonuclei in longterm denervated rat muscles.Anat Rec 1995;243:430-7.
18.Carraro U.Modulation of trophism and fiber type expression of denervated muscle by different patterns of electrical stimulation.Basic Appl Myol 2002;12:263-72.
19.Kuschel R,Yablonka-Reuveni Z,Bornemann A.Satellite cells on isolated myofibers from normal and denervated adult rat muscle.J Histochem Cytochem 1999;47:1375-84.
20.Yoshimura K,Harii K.A regenerative change during muscle adaptation to denervation in rats.J Surg Res 1999;81:139-46.
21.Schmalbruch H,Lewis DM.Dynamics of nuclei of muscle fibers and connective tissue cells in normal and denervated rat muscles.Muscle Nerve2000;23:617-26.
22.Ehrhardt J,Morgan J.Regenerative capacity of skeletal muscle.Curr Opin Neurol 2005;18:548-53.
23.Schmalbruch H.Growth and denervation response of skeletal muscle fibers of newborn rats.Muscle Nerve 1990;13:421-32.
24.Jejurikar SS,Kuzon Jr WM.Satellite cell depletion in degenerative skeletal muscle.Apoptosis 2003;8:573-8.
25.Viguie CA,Lu DX,Huang SK,Rengen H,Carlson BM.Quantitative study of the effects of long-term denervation on the extensor digitorum longus muscle of the rat.Anat Rec 1997;248:346-54.
26.Borisov AB,Dedkov EI,Carlson BM.Abortive myogenesis in denervated skeletal muscle:differentiative properties of satellite cells,their migration,and block of terminal differentiation.Anat Embryol(Berl)2005;209:269-79.
27.van der Meer SF,Jaspers RT,Jones DA,Degens H.Time-course of changes in the myonuclear domain during denervation in young-adult and old rat gastrocnemius muscle.Muscle Nerve 2011;43:212-22.
28.Jimena I,Pe~na J,Luque E,Vaamonde R.Muscle hypertrophy experimentally induced by administration of denervated muscle extract.J Neuropathol Exp Neurol 1993;52:379-86.
29.Jimena I,Pe~na J,Luque E,Ayuso F,Vaamonde R.Myotrophic effects of muscle extracts obtained at different intervals after denervation.Neuropathol Appl Neurobiol 1998;24:217-23.
30.Pe~na J,Jimena I,Luque E,Vaamonde R.New fiber formation in rat soleus muscle following administration of denervated muscle extract.J Neurol Sci 1995;128:14-21.
31.Ag€uera E,Castilla S,Luque E,Jimena I,Leiva-Cepas F,Ruz-Caracuel I,et al.Muscular hypertrophy and atrophy in normal rats provoked by the administration of normal and denervated muscle extracts.Histol Histopathol 2016;31:1367-79.
32.Finkelstein DI,Dooley PC,Luff AR.Recovery of muscle after different periods of denervation and treatments.Muscle Nerve 1993;16:769-77.
33.Cumming WJK,Fulthorpe JJ,Hudgson P,Mahon M.Color atlas of muscle pathology.London:Mosby-Wolfe;1994.p.183-8.
34.Rantanen J,Hurme T,Lukka R,Heino J,Kalimo H.Satellite cell proliferation and the expression of myogenin and desmin in regenerating skeletal muscle:evidence for two different populations of satellite cells.Lab Invest1995;72:341-7.
35.Lawson-Smith MJ,McGeachie JK.The identification of myogenic cells in skeletal muscle,with emphasis on the use of tritiated thymidine autoradiography and desmin antibodies.J Anat 1998;192:161-71.
36.Comella JX,Sanz-Rodriguez C,Aldea M,Esquerda JE.Skeletal musclederived trophic factors prevent motoneurons from entering an active cell death program in vitro.J Neurosci 1994;14:2674-86.
37.Bischoff R.Chemotaxis of skeletal muscle satellite cells.Dev Dyn1997;208:505-15.
38.Chen G,Quinn LS.Partial characterization of skeletal myoblast mitogens in mouse crushed muscle extract.J Cell Physiol 1992;153:563-74.
39.Buonanno A,Cheng J,Venepally P,Weis J,Calvo S.Activity dependent regulation of muscle genes:repressive and stimulatory effects of innervation.Acta Physiol Scand 1998;163:17-26.
40.Tatsumi R,Anderson JE,Nevoret CJ,Halevy O,Allen RE.HGF/SF is present in normal adult skeletal muscle and is capable of activating satellite cells.Dev Biol 1998;194:114-28.
41.Wan Q,Yeung SS,Cheung KK,Au SW,Lam WW,Li YH,et al.Optimizing electrical stimulation for promoting satellite cell proliferation in muscle disuse atrophy.Am J Phys Med Rehabil 2016;95:28-38.
42.Cheng L,Lai MD,Sanderson JE,Yu CM,Li M.Enhanced fusion of myoblasts with myofibers for efficient gene delivery induced by a partially purified protein fraction from rat muscle extract.Arch Biochem Biophys2005;441:141-50.
43.Allen DL,Roy RR,Edgerton VR.Myonuclear domains in muscle adaptation and disease.Muscle Nerve 1999;22:1350-60.
44.Mc Geachie JK.Sustained cell proliferation in denervated skeletal muscle of mice.Cell Tissue Res 1989;257:455-7.
45.Carlson BM.Denervation and the aging of skeletal muscle.Basic Appl Myol 2004;14:135-9.
46.Borisov AB,Dedkov EI,Carlson BM.Differentiation of activated satellite cells in denervated muscle following single fusions in situ and in cell culture.Histochem Cell Biol 2005;124:13-23.
47.Ishido M,Kami K,Masuhara M.In vivo expression patterns of MyoD,p21,and Rb proteins in myonuclei and satellite cells of denervated rat skeletal muscle.Am J Physiol Cell Physiol 2004;287:C484-93.
48.Gundersen K,Bruusgaard JC.Nuclear domains during muscle atrophy:nuclei lost or paradigm lost?J Physiol 2008;586:2675-81.
49.Murray MA,Robbins N.Cell proliferation in denervated muscle:time course,distribution and relation to disuse.Neuroscience 1982;7:1817-22.
50.Adami N,Biral D,Caccavale S,Rossini K.Histology of the long term denervated rat muscle.Basic Appl Myol 2006;16:113-4.
51.Allen RE,Rankin LL.Regulation of satellite cells during skeletal muscle growth and development.Proc Soc Exp Biol Med 1990;194:81-6.
52.Tamaki T,Akatsuka A,Ando K,Nakamura Y,Matsuzawa H,Hotta T,et al.Identification of myogenic-endothelial progenitor cells in the interstitial spaces of skeletal muscle.J Cell Biol 2002;157:571-7.
53.Tamaki T,Akatsuka A,Yoshimura S,Roy RR,Edgerton VR.New fiber formation in the interstitial spaces of rat skeletal muscle during postnatal growth.J Histochem Cytochem 2002;50:1097-111.
54.Schultz E.Changes in the satellite cells of growing muscle following denervation.Anat Rec 1978;190:299-311.
55.Lu DX,Huang SK,Carlson BM.Electron microscopic study of long-term denervated rat skeletal muscle.Anat Rec 1997;248:355-65.
56.Collins CA,Olsen I,Zammit PS,Heslop L,Petrie A,Partridge TA,et al.Stem cell function,self-renewal,and behavioral heterogeneity of cells from the adult muscle satellite cell niche.Cell 2005;122:289-301.
57.Santa Maria L,Rojas CV,Minguell JJ.Signals from damaged but not undamaged skeletal muscle induce myogenic differentiation of rat bonemarrow-derived mesenchymal stem cells.Exp Cell Res 2004;300:418-26.
58.Peng H,Huard J.Muscle-derived stem cells for musculoskeletal tissue regeneration and repair.Transpl Immunol 2004;12:311-9.
59.Peault B,Rudnicki M,Torrente Y,Cossu G,Tremblay JP,Partridge T,et al.Stem and progenitor cells in skeletal muscle development,maintenance,and therapy.Mol Ther 2007;15:867-77.
60.Otto A,Collins-Hooper H,Patel K.The origin,molecular regulation and therapeutic potential of myogenic stem cell populations.J Anat2009;215:477-97.
61.Bianco P,Cossu G.Uno,nessuno e centomila:searching for the identity of mesodermal progenitors.Exp Cell Res 1999;251:257-63.
62.Dellavalle A,Sampaolesi M,Tonlorenzi R,Tagliafico E,Sacchetti B,Perani L,et al.Pericytes of human skeletal muscle are myogenic precursors distinct from satellite cells.Nat Cell Biol 2007;9:255-67.
63.Crisan M,Yap S,Casteilla L,Chen CW,Corselli M,Park TS,et al.Aperivascular origin for mesenchymal stem cells in multiple human organs.Cell Stem Cell 2008;3:301-13.
64.Dellavalle A,Maroli G,Covarello D,Azzoni E,Innocenzi A,Perani L,et al.Pericytes resident in postnatal skeletal muscle differentiate into muscle fibres and generate satellite cells.Nat Commun 2011;2:499.doi:10.1038/ncomms1508.
65.van Haelst U.An electron microscopic study of muscle in WerdnigHoffmann’s disease.Virchows Arch A Pathol Pathol Anat1970;351:291-305.
66.de Maruenda EC,Franzini-Armstrong C.Satellite and invasive cells in frog Sartorius muscle.Tissue Cell 1978;10:749-72.
67.Hansen-Smith FM,Picou D,Golden MH.Muscle satellite cells in malnourished and nutritionally rehabilitated children.J Neurol Sci1979;41:207-21.
68.Ontell M.Evidence for myoblastic potential of satellite cells in denervated muscle.Cell Tissue Res 1975;160:345-53.
69.Laule S,Bornemann A.Ultrastructural findings at the satellite cell-myofiber border in normal and diseased human muscle biopsy specimens.Acta Neuropathol 2001;101:435-9.
70.Bittner RE,Schofer C,Weipoltshammer K,Ivanova S,Streubel B,Hauser E,et al.Recruitment of bone-marrow-derived cells by skeletal and cardiac muscle in adult dystrophic mdx mice.Anat Embryol(Berl)1999;199:391-6.
71.Skuk D,Vilquin JT,Tremblay JP.Experimental and therapeutic approaches to muscular dystrophies.Curr Opin Neurol 2002;15:563-9.
72.Kuang S,Kuroda K,Le Grand F,Rudnicki MA.Asymmetric self-renewal and commitment of satellite stem cells in muscle.Cell 2007;129:999-1010.
73.Dhawan J,Rando TA.Stem cells in postnatal myogenesis:molecular mechanisms of satellite cell quiescence,activation and replenishment.Trends Cell Biol 2005;15:666-73.