Stem cells to tissue: Molecular, cellular and anatomical heterogeneity in skeletal muscle

Current Opinion in Genetics and Development

Volumn 13, Issue 4, 2003, Pages 413-422

  Tajbakhsh, Shahragim ^a  

^a INSTITUT PASTEUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL; BIOLOGICAL MODEL; CELL DIFFERENTIATION; CELL FUSION; CELL GROWTH; CELL HETEROGENEITY; CELL LINEAGE; CELL POPULATION; CELL REGENERATION; DEVELOPMENTAL STAGE; EMBRYOLOGY; GENETIC ANALYSIS; HUMAN; MOLECULAR BIOLOGY; MUSCLE CELL; MUSCLE DEVELOPMENT; MYOTOME; NONHUMAN; PERINATAL PERIOD; PHYSIOLOGY; POSTNATAL GROWTH; PRIORITY JOURNAL; REVIEW; SATELLITE CELL; SKELETAL MUSCLE; SKELETAL MUSCLE SATELLITE CELL; SOMITE; STEM CELL; TISSUE DIFFERENTIATION;

ANIMALIA;

EID: 0042847335     PISSN: 0959437X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-437X(03)00090-X     Document Type: Review

References (84)

1. Christ B., Ordahl C.P. Early stages of chick somite development. Anat. Embryol (Berl.). 191:1995;381-396.
2. Gossler A, Hrabe de Angelis M (ed): Somitogenesis; 1997.
3. Pourquie O., Spitz F., Gonzalez F., Duboule D., Mueller G.M., O'Day T., Watchko J.F., Ontell M. Vertebrate segmentation: lunatic transcriptional regulation. Curr. Biol. 12:2002;R699-R701.
4. Scaal M., Prols F., Fuchtbauer E.M., Patel K., Hornik C., Kohler T., Christ B., Brand-Saberi B. BMPs induce dermal markers and ectopic feather tracts. Mech. Dev. 110:2002;51-60.
5. Brent A.E., Schweitzer R., Tabin C.J. A somitic compartment of tendon progenitors. Cell. 113:2003;235-248 A nice study pointing to a new somitic compartment, comprising tendons which will link the axial skeletal muscle to cartilage and bone elements, as described by scleraxis expression. The tendon precursors arise from the sclerotome, adjacent to, and dependent on, the myotome through FGF signalling. These cells are confined to the anterior and posterior boundaries of the somite.
6. Edom-Vovard F., Schuler B., Bonnin M.A., Teillet M.A., Duprez D. Fgf4 positively regulates scleraxis and tenascin expression in chick limb tendons. Dev. Biol. 247:2002;351-366.
7. Marics I., Padilla F., Guillemot J.F., Scaal M., Marcelle C. FGFR4 signaling is a necessary step in limb muscle differentiation. Development. 129:2002;4559-4569.
8. Tajbakhsh S., Cossu G. Establishing myogenic identity during somitogenesis. Curr. Opin. Genet. Dev. 7:1997;634-641.
9. Sporle R. Epaxial-adaxial-hypaxial regionalisation of the vertebrate somite: evidence for a somitic organiser and a mirror-image duplication. Dev. Genes Evol. 211:2001;198-217.
10. Tajbakhsh S. The genetics of murine skeletal muscle biogenesis. Results Probl. Cell Differ. 38:2002;61-79.
11. Kahane N., Cinnamon Y., Kalcheim C. The roles of cell migration and myofiber intercalation in patterning formation of the postmitotic myotome. Development. 129:2002;2675-2687 This study provides new evidence for the first two waves of myotome formation: a first wave by 'pioneer' cells extending the entire dorsoventral extent of the myotome, and a second wave which enters the myotome from the anterior and posterior dermomyotome lips to intercalate between existing differentiated myocytes.
12. Venters S.J., Thorsteinsdottir S., Duxson M.J. Early development of the myotome in the mouse. Dev. Dyn. 216:1999;219-232.
13. Denetclaw W.F. Jr., Berdougo E., Venters S.J., Ordahl C.P. Morphogenetic cell movements in the middle region of the dermomyotome dorsomedial lip associated with patterning and growth of the primary epaxial myotome. Development. 128:2001;1745-1755.
14. Venters S.J., Ordahl C.P. Persistent myogenic capacity of the dermomyotome dorsomedial lip and restriction of myogenic competence. Development. 129:2002;3873-3885 These authors provide evidence that the dorsomedial dermomyotome lip drives myotome growth and is the principal source of myogenic progenitors for dorsal myotome formation.
15. Cinnamon Y., Kahane N., Bachelet I., Kalcheim C. The sub-lip domain-a distinct pathway for myotome precursors that demonstrate rostral-caudal migration. Development. 128:2001;341-351.
16. Tajbakhsh S., Sporle R. Somite development: constructing the vertebrate body. Cell. 92:1998;9-16.
17. Kahane N., Cinnamon Y., Bachelet I., Kalcheim C. The third wave of myotome colonization by mitotically competent progenitors: regulating the balance between differentiation and proliferation during muscle development. Development. 128:2001;2187-2198.
18. Eloy-Trinquet S., Nicolas J.F. Clonal separation and regionalisation during formation of the medial and lateral myotomes in the mouse embryo. Development. 129:2002;111-122.
19. Eloy-Trinquet S., Nicolas J.F. Cell coherence during production of the presomitic mesoderm and somitogenesis in the mouse embryo. Development. 129:2002;3609-3619 Using a retrospective lineage marking approach in the mouse, these authors provide evidence supporting previous studies in the chick, and suggest that ancestors of the myotome are highly regionalized in the presomitic mesoderm, somite and myotome, and that the dermo(myotome) grows coherently by the intercalation of future generations of cells into the structure.
20. Tajbakhsh S., Rocancourt D., Cossu G., Buckingham M. Redefining the genetic hierarchies controlling skeletal myogenesis: Pax-3 and Myf-5 act upstream of MyoD. Cell. 89:1997;127-138.
21. Stockdale F.E. Myogenic cell lineages. Dev. Biol. 154:1992;284-298.
22. Dunglison G.F., Scotting P.J., Wigmore P.M. Rat embryonic myoblasts are restricted to forming primary fibres while later myogenic populations are pluripotent. Mech. Dev. 87:1999;11-19.
23. Schwander M., Leu M., Stumm M., Dorchies O.M., Ruegg U.T., Schittny J., Muller U. beta1 integrins regulate myoblast fusion and sarcomere assembly. Dev. Cell. 4:2003;673-685 Using a conditional Cre which expresses in myoblasts, these authors provide evidence that β1 integrins are required for myoblast-myoblast fusion.
24. Horsley V., Jansen K.M., Mills S.T., Pavlath G.K. IL-4 Acts as a myoblast recruitment factor during mammalian muscle growth. Cell. 113:2003;483-494 An elegant study demonstrating that IL-4 secreted by myotubes under the action of the NFAT2c transcription factor directs myoblast-myotube fusion via the IL-4α receptor. The presence of a reduced number of myonuclei in some myofibres of IL-4 and IL-4α receptor knock-out mice suggests that an alternate pathway is operating to direct this type of fusion.
25. Cachaco A.S., Chuva de Sousa Lopes S.M., Kuikman I., Bajanca F., Abe K., Baudoin C., Sonnenberg A., Mummery C.L., Thorsteinsdottir S. Knock-in of integrin beta 1D affects primary but not secondary myogenesis in mice. Development. 130:2003;1659-1671.
26. Armand O., Boutineau A.M., Mauger A., Pautou M.P., Kieny M. Origin of satellite cells in avian skeletal muscles. Arch. Anat. Microsc. Morphol. Exp. 72:1983;163-181.
27. Kardon G., Campbell J.K., Tabin C.J. Local extrinsic signals determine muscle and endothelial cell fate and patterning in the vertebrate limb. Dev. Cell. 3:2002;533-545 A nice study using a complex retroviral library to transduce limb level somites suggests that skeletal muscle and endothelial cells have a common ancestor in the somite. This study also provides evidence that skeletal muscle patterning is largely determined by local extrinsic cues in the limb and is not governed prior to progenitor cell migration from the somite as had been suggested previously.
28. Sordella R., Jiang W., Chen G.C., Curto M., Settleman J. Modulation of Rho GTPase signaling regulates a switch between adipogenesis and myogenesis. Cell. 113:2003;147-158.
29. Zammit P., Beauchamp J. The skeletal muscle satellite cell: stem cell or son of stem cell? Differentiation. 68:2001;193-204.
30. Potten C.S., Booth C. Keratinocyte stem cells: a commentary. J. Invest. Dermatol. 119:2002;888-899.
31. Asakura A., Komaki M., Rudnicki M. Muscle satellite cells are multipotential stem cells that exhibit myogenic, osteogenic, and adipogenic differentiation. Differentiation. 68:2001;245-253.
32. Wada M.R., Inagawa-Ogashiwa M., Shimizu S., Yasumoto S., Hashimoto N. Generation of different fates from multipotent muscle stem cells. Development. 129:2002;2987-2995.
33. Seale P., Sabourin L.A., Girgis-Gabardo A., Mansouri A., Gruss P., Rudnicki M.A. Pax7 is required for the specification of myogenic satellite cells. Cell. 102:2000;777-786.
34. Mansouri A., Stoykova A., Torres M., Gruss P. Dysgenesis of cephalic neural crest derivatives in Pax7-/- mutant mice. Development. 122:1996;831-838.
35. Zammit P.S., Heslop L., Hudon V., Rosenblatt J.D., Tajbakhsh S., Buckingham M.E., Beauchamp J.R., Partridge T.A. Kinetics of myoblast proliferation show that resident satellite cells are competent to fully regenerate skeletal muscle fibers. Exp. Cell Res. 281:2002;39-49.
36. Knoblich J.A. Mechanisms of asymmetric cell division during animal development. Curr. Opin. Cell Biol. 9:1997;833-841.
37. Conboy I.M., Rando T.A. The regulation of Notch signaling controls satellite cell activation and cell fate determination in postnatal myogenesis. Dev. Cell. 3:2002;397-409 This study provides evidence that the Notch signalling pathway governs satellite cell proliferation and differentiation. Further, it is suggested that the asymmetric cell fate determinant Numb drives satellite cell differentiation by antagonising Notch.
38. Huang R., Zhi Q., Christ B. The relationship between limb muscle and endothelial cells migrating from single somite. Anat. Embryol. (Berl.). 206:2003;283-289 Single somite transplantation studies provide evidence that endothelial and skeletal muscle progenitors migrate from the somite to the wing and that considerable intermingling of their descendants takes place throughout the anterior-posterior and dorsal-ventral axes.
39. Weintraub H., Davis R., Tapscott S., Thayer M., Krause M., Benezra R., Blackwell T.K., Turner D., Rupp R., Hollenberg S.et al. The MyoD gene family: nodal point during specification of the muscle cell lineage. Science. 251:1991;761-766.
40. Borycki A.G., Emerson C.P. Jr. Multiple tissue interactions and signal transduction pathways control somite myogenesis. Curr. Top. Dev. Biol. 48:2000;165-224.
41. Borycki A.G., Brunk B., Tajbakhsh S., Buckingham M., Chiang C., Emerson C.P. Jr. Sonic hedgehog controls epaxial muscle determination through Myf5 activation. Development. 126:1999;4053-4063.
42. Kruger M., Mennerich D., Fees S., Schafer R., Mundlos S., Braun T. Sonic hedgehog is a survival factor for hypaxial muscles during mouse development. Development. 128:2001;743-752.
43. Marcelle C., Ahlgren S., Bronner-Fraser M. In vivo regulation of somite differentiation and proliferation by Sonic Hedgehog. Dev. Biol. 214:1999;277-287.
44. Gustafsson M.K., Pan H., Pinney D.F., Liu Y., Lewandowski A., Epstein D.J., Emerson C.P. Jr. Myf5 is a direct target of long-range Shh signaling and Gli regulation for muscle specification. Genes Dev. 16:2002;114-126 Evidence is provided suggesting that Shh signalling, via a Gli-binding site in the epaxial enhancer of the Myf5 gene, drives Myf5 expression in the dermomyotome of the somite.
45. Teboul L., Hadchouel J., Daubas P., Summerbell D., Buckingham M., Rigby P.W. The early epaxial enhancer is essential for the initial expression of the skeletal muscle determination gene Myf5 but not for subsequent, multiple phases of somitic myogenesis. Development. 129:2002;4571-4580.
46. Summerbell D., Halai C., Rigby P.W. Expression of the myogenic regulatory factor Mrf4 precedes or is contemporaneous with that of Myf5 in the somitic bud. Mech. Dev. 117:2002;331-335 The 'differentiation' gene Mrf4 was found to be expressed in the somite prior to overt myotome formation. This finding is also discussed in [10] (see also legend to Figure 1).
47. Hadchouel J, Carvajal JJ, Daubas P, Bajard L, Rocancourt D, Cox D, Summerbell D, Tajbakhsh S, Rigby PWJ, Buckingham M: Analysis of a key regulatory region upstream of the Myf5 gene reveals multiple phases of myogenesis, orchestrated at each site by elements dispersed throughout the locus. Development 2003, in press.
48. Burke A.C., Nowicki J.L., White P.H., Farkas D.R., McFadden E.E., Chapman D.L. A new view of patterning domains in the vertebrate mesoderm. Dev. Cell. 4:2003;159-165 New subdivisions of somite derivatives are presented to explain why in some cases, mutant and transgenic studies reveal phenotypes that cannot be explained along the traditional epaxial/hypaxial definitions.
49. Spitz F., Gonzalez F., Duboule D. A global control region defines a chromosomal regulatory landscape containing the HoxD cluster. Cell. 113:2003;405-417 Analysis of the Hoxd cluster points to enhancer regulatory domains which are located up to 250 kbp distal to the gene. It is suggested that genes falling within the influence of such regulatory domains would fortutiously adopt their expression pattern.
50. Chen J.C., Ramachandran R., Goldhamer D.J. Essential and redundant functions of the MyoD distal regulatory region revealed by targeted mutagenesis. Dev. Biol. 245:2002;213-223.
51. Relaix F., Buckingham M. From insect eye to vertebrate muscle: redeployment of a regulatory network. Genes Dev. 13:1999;3171-3178.
52. Laclef C., Hamard G., Demignon J., Souil E., Houbron C., Maire P. Altered myogenesis in Six1-deficient mice. Development. 130:2003;2239-2252.
53. Lu J.R., Bassel-Duby R., Hawkins A., Chang P., Valdez R., Wu H., Gan L., Shelton J.M., Richardson J.A., Olson E.N. Control of facial muscle development by MyoR and capsulin. Science. 298:2002;2378-2381 Analysis of double mutant mice for these repressors reveals a role for these genes in directing the establishment of first-arch derived head muscles. This study provides another nice example of how sub-regions of the body are under the control of specific genetic regulatory networks.
54. Van Swearingen J., Lance-Jones C. Slow and fast muscle fibers are preferentially derived from myoblasts migrating into the chick limb bud at different developmental times. Dev. Biol. 170:1995;321-337.
55. Nikovits W. Jr., Cann G.M., Huang R., Christ B., Stockdale F.E. Patterning of fast and slow fibers within embryonic muscles is established independently of signals from the surrounding mesenchyme. Development. 128:2001;2537-2544.
56. Rees E., Young R.D., Evans D.J. Spatial and temporal contribution of somitic myoblasts to avian hind limb muscles. Dev. Biol. 253:2003;264-278.
57. Lin J., Wu H., Tarr P.T., Zhang C.Y., Wu Z., Boss O., Michael L.F., Puigserver P., Isotani E., Olson E.et al. Transcriptional co-activator PGC-1α drives the formation of slow-twitch muscle fibres. Nature. 418:2002;797-801 Remarkably, expression of physiological levels of the transcriptional co-activator PGC-1α in skeletal muscles of transgenic mice was sufficient to drive fast muscles to change their character to a slow-twitch oxidative phenotype.
58. Birchmeier C., Brohmann H. Genes that control the development of migrating muscle precursor cells. Curr. Opin. Cell Biol. 12:2000;725-730.
59. Mootoosamy R.C., Dietrich S. Distinct regulatory cascades for head and trunk myogenesis. Development. 129:2002;573-583.
60. Ferrari G, Cusella-De Angelis G, Coletta M, Paolucci E, Stornaiuolo A, Cossu G, Mavilio F: Muscle regeneration by bone marrow-derived myogenic progenitors. [see comments] [published erratum appears in Science 1998 Aug 14;281:923]. Science 1998, 279:1528-1530.
61. Krause D.S., Theise N.D., Collector M.I., Henegariu O., Hwang S., Gardner R., Neutzel S., Sharkis S.J. Multi-organ, multi-lineage engraftment by a single bone marrow-derived stem cell. Cell. 105:2001;369-377.
62. Wagers A.J., Sherwood R.I., Christensen J.L., Weissman I.L. Little evidence for developmental plasticity of adult hematopoietic stem cells. Science. 297:2002;2256-2259.
63. Theise N.D., Krause D.S., Sharkis S. Comment on 'Little evidence for developmental plasticity of adult hematopoietic stem cells'. Science. 299:2003;1317.
64. Gussoni E., Soneoka Y., Strickland C.D., Buzney E.A., Khan M.K., Flint A.F., Kunkel L.M., Mulligan R.C. Dystrophin expression in the mdx mouse restored by stem cell transplantation. Nature. 401:1999;390-394.
65. Jackson K.A., Mi T., Goodell M.A. Hematopoietic potential of stem cells isolated from murine skeletal muscle. Proc. Natl. Acad. Sci. U.S.A. 96:1999;14482-14486.
66. Kawada H., Ogawa M. Bone marrow origin of hematopoietic progenitors and stem cells in murine muscle. Blood. 98:2001;2008-2013.
67. Asakura A., Seale P., Girgis-Gabardo A., Rudnicki M.A. Myogenic specification of side population cells in skeletal muscle. J. Cell Biol. 159:2002;123-134 Muscle side-population cells were isolated by FACS and shown to be CD45 positive and to have hematopoietic potential, but they did not form skeletal muscle autonomously in vitro. These cells could give rise to a satellite cell after intramuscular injection.
68. McKinney-Freeman S.L., Jackson K.A., Camargo F.D., Ferrari G., Mavilio F., Goodell M.A. Muscle-derived hematopoietic stem cells are hematopoietic in origin. Proc. Natl. Acad. Sci. U.S.A. 99:2002;1341-1346.
69. Tamaki T., Akatsuka A., Ando K., Nakamura Y., Matsuzawa H., Hotta T., Roy R.R., Edgerton V.R. Identification of myogenic-endothelial progenitor cells in the interstitial spaces of skeletal muscle. J. Cell Biol. 157:2002;571-577.
70. Qu-Petersen Z., Deasy B., Jankowski R., Ikezawa M., Cummins J., Pruchnic R., Mytinger J., Cao B., Gates C., Wernig A.et al. Identification of a novel population of muscle stem cells in mice: potential for muscle regeneration. J. Cell Biol. 157:2002;851-864.
71. LaBarge M.A., Blau H.M. Biological progression from adult bone marrow to mononucleate muscle stem cell to multinucleate muscle fiber in response to injury. Cell. 111:2002;589-601 Following a two step injury regime involving irradiation to eliminate endogenous satellite cells and exercise induced muscle damage for their activation, adult bone marrow derived stem cells were found to transit via a satellite cell to give rise to differentiated myotubes. This phenomenon occurred independent of cell fusion.
72. Ying Q.L., Nichols J., Evans E.P., Smith A.G. Changing potency by spontaneous fusion. Nature. 416:2002;545-548 An important study providing evidence that neuronal stem cells can change fate to non-neuronal derivatives by spontaneous cell fusion, thereby suggesting that the often reported transdifferentiation or plasticity attributed to regenerative stem cells may in some cases be explained by cell-cell fusion.
73. Wang X., Willenbring H., Akkari Y., Torimaru Y., Foster M., Al-Dhalimy M., Lagasse E., Finegold M., Olson S., Grompe M. Cell fusion is the principal source of bone-marrow-derived hepatocytes. Nature. 422:2003;897-901.
74. Vassilopoulos G., Wang P.R., Russell D.W. Transplanted bone marrow regenerates liver by cell fusion. Nature. 422:2003;901-904.
75. Minasi M.G., Riminucci M., De Angelis L., Borello U., Berarducci B., Innocenzi A., Caprioli A., Sirabella D., Baiocchi M., De Maria R.et al. The meso-angioblast: a multipotent, self-renewing cell that originates from the dorsal aorta and differentiates into most mesodermal tissues. Development. 129:2002;2773-2783 This study characterises a new type of regenerative multipotent stem cell associated with the vasculature and proposes that such vessel associated stem cells may be an important delivery route in the regeneration of various tissues and organs.
76. Mueller G.M., O'Day T., Watchko J.F., Ontell M. Effect of injecting primary myoblasts versus putative muscle-derived stem cells on mass and force generation in mdx mice. Hum. Gene. Ther. 13:2002;1081-1090.
77. Jockusch H., Voigt S. Migration of adult myogenic precursor cells as revealed by GFP/nLacZ labelling of mouse transplantation chimeras. J. Cell Sci. 116:2003;1611-1616.
78. Mezey E., Key S., Vogelsang G., Szalayova I., Lange G.D., Crain B. Transplanted bone marrow generates new neurons in human brains. Proc. Natl. Acad. Sci. U.S.A. 100:2003;1364-1369.
79. Weimann J.M., Charlton C.A., Brazelton T.R., Hackman R.C., Blau H.M. Contribution of transplanted bone marrow cells to Purkinje neurons in human adult brains. Proc. Natl. Acad. Sci. U.S.A. 100:2003;2088-2093.
80. Lu QL, Mann CJ, Lou F, Bou-Gharios G, Morris GE, Xue S, Fletcher S, Partridge TA, Wilton SD: Functional amounts of dystrophin produced by skipping the mutated exon in the mdx dystrophic mouse. Nature Medicine 2003, in press.
81. Bogdanovich S., Krag T.O., Barton E.R., Morris L.D., Whittemore L.A., Ahima R.S., Khurana T.S. Functional improvement of dystrophic muscle by myostatin blockade. Nature. 420:2002;418-421 This study, along with [82], provide evidence that the dystrophic phenotype can be ameliorated by increasing muscle mass and force through the inhibition of myostatin function via intraperitoneal injections of neutralising antibodies.
82. Wagner K.R., McPherron A.C., Winik N., Lee S.J. Loss of myostatin attenuates severity of muscular dystrophy in mdx mice. Ann. Neurol. 52:2002;832-836.
83. Zammit P.S., Partridge T.A. Sizing up muscular dystrophy. Nat. Med. 8:2002;1355-1356.
84. Beauchamp J.R., Heslop L., Yu D.S., Tajbakhsh S., Kelly R.G., Wernig A., Buckingham M.E., Partridge T.A., Zammit P.S. Expression of CD34 and Myf5 defines the majority of quiescent adult skeletal muscle satellite cells. J. Cell Biol. 151:2000;1221-1234.