Identification of telocytes in skeletal muscle interstitium: Implication for muscle regeneration

Journal of Cellular and Molecular Medicine

Volumn 15, Issue 6, 2011, Pages 1379-1392

  Popescu, L M ^a,b   Manole, Emilia ^b   Şerboiu, Crenguţa S ^a   Manole, C G ^a,b   Suciu, Laura C ^a,b   Gherghiceanu, Mihaela ^b   Popescu, B O ^a,b  

^a CAROL DAVILA UNIVERSITY OF MEDICINE AND PHARMACY   (Romania)

^b VICTOR BABES NATIONAL INSTITUTE OF PATHOLOGY   (Romania)

Author keywords

C kit; Caveolin 1; Intercellular signalling; Interstitial cells; Muscle regeneration repair; Non satellite progenitor cell niche; Satellite cells; Shed vesicles; Striated skeletal muscle; Telocytes; Telopodes; VEGF

Indexed keywords

BIOLOGICAL MARKER; CAVEOLIN 1; STEM CELL FACTOR RECEPTOR; VASCULOTROPIN A;

ANIMAL; ARTICLE; BIOSYNTHESIS; C57BL MOUSE; CELL CULTURE; CELL DIFFERENTIATION; CYTOLOGY; HUMAN; METABOLISM; MOUSE; PHYSIOLOGY; RAT; REGENERATION; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; STROMA CELL; TRANSMISSION ELECTRON MICROSCOPY; WISTAR RAT;

ANIMALS; BIOLOGICAL MARKERS; CAVEOLIN 1; CELL DIFFERENTIATION; CELLS, CULTURED; HUMANS; MICE; MICE, INBRED C57BL; MICROSCOPY, ELECTRON, TRANSMISSION; MUSCLE, SKELETAL; PROTO-ONCOGENE PROTEINS C-KIT; RATS; RATS, WISTAR; REGENERATION; SIGNAL TRANSDUCTION; STROMAL CELLS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

RATTUS;

EID: 79957633197     PISSN: 15821838     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1582-4934.2011.01330.x     Document Type: Article

References (76)

1. Kuang S, Gillespie MA, Rudnicki MA. Niche regulation of muscle satellite cell self-renewal and differentiation. Cell Stem Cell. 2008; 2: 22-31.
2. Rennie MJ, Phillips S, Smith K. Reliability of results and interpretation of measures of 3-methylhistidine in muscle interstitium as marker of muscle proteolysis. J Appl Physiol. 2008; 105: 1380-1.
3. Perdiguero E, Sousa-Victor P, Ballestar E, et al Epigenetic regulation of myogenesis. Epigenetics. 2009; 4: 541-50.
4. Morrison JI, Borg P, Simon A. Plasticity and recovery of skeletal muscle satellite cells during limb regeneration. FASEB J. 2010; 24: 750-6.
5. Beauchamp JR, Heslop L, Yu DS, et al Expression of CD34 and Myf5 defines the majority of quiescent adult skeletal muscle satellite cells. J Cell Biol. 2000; 151: 1221-34.
6. Asakura A, Komaki M, Rudnicki M. Muscle satellite cells are multipotential stem cells that exhibit myogenic, osteogenic, and adipogenic differentiation. Differentiation. 2001; 68: 245-53.
7. Maier A, Zhou Z, Bornemann A. The expression profile of myogenic transcription factors in satellite cells from denervated rat muscle. Brain Pathol. 2002; 12: 170-7.
8. Fukada S, Higuchi S, Segawa M, et al Purification and cell-surface marker characterization of quiescent satellite cells from murine skeletal muscle by a novel monoclonal antibody. Exp Cell Res. 2004; 296: 245-55.
9. Gopinath SD, Rando TA. Stem cell review series: aging of the skeletal muscle stem cell niche. Aging Cell. 2008; 7: 590-8.
10. Rudnicki MA, Le Grand F, McKinnell I, et al The molecular regulation of muscle stem cell function. Cold Spring Harb Symp Quant Biol. 2008; 73: 323-31.
11. Collins CA, Gnocchi VF, White RB, et al Integrated functions of Pax3 and Pax7 in the regulation of proliferation, cell size and myogenic differentiation. PLoS One. 2009; 4: e4475.
12. Lepper C, Conway SJ, Fan CM. Adult satellite cells and embryonic muscle progenitors have distinct genetic requirements. Nature. 2009; 460: 627-31.
13. Biressi S, Rando TA. Heterogeneity in the muscle satellite cell population. Semin Cell Dev Biol. 2010; 21: 845-54.
14. Dodson MV, Hausman GJ, Guan L, et al Skeletal muscle stem cells from animals I. Basic cell biology. Int J Biol Sci. 2010; 6: 465-74.
15. Gill R, Hitchins L, Fletcher F, et al Sulf1A and HGF regulate satellite-cell growth. Cell Sci. 2010; 123: 1873-83.
16. Ieronimakis N, Balasundaram G, Rainey S, et al Absence of CD34 on murine skeletal muscle satellite cells marks a reversible state of activation during acute injury. PLoS One. 2010; 5: e10920.
17. Kang JS, Krauss RS. Muscle stem cells in developmental and regenerative myogenesis. Curr Opin Clin Nutr Metab Care. 2010; 13: 243-8.
18. Mitchell KJ, Pannérec A, Cadot B, et al Identification and characterization of a non-satellite cell muscle resident progenitor during postnatal development. Nat Cell Biol. 2010; 12: 257-66.
19. Ono Y, Boldrin L, Knopp P, et al Muscle satellite cells are a functionally heterogeneous population in both somite-derived and branchiomeric muscles. Dev Biol. 2010; 337: 29-41.
20. Bach AD, Arkudas A, Tjiawi J, et al A new approach to tissue engineering of vascularized skeletal muscle. J Cell Mol Med. 2006; 10: 716-26.
21. Polykandriotis E, Arkudas A, Euler S, et al Prevascularisation strategies in tissue engineering. Handchir Mikrochir Plast Chir. 2006; 38: 217-23.
22. Polykandriotis E, Horch RE, Arkudas A, et al Intrinsic versus extrinsic vascularization in tissue engineering. Adv Exp Med Biol. 2006; 585: 311-26.
23. Klumpp D, Horch RE, Kneser U, et al Engineering skeletal muscle tissue-new perspectives in vitro and in vivo. J Cell Mol Med. 2010; 14: 2622-9.
24. Brooks NE, Cadena SM, Vannier E, et al Effects of resistance exercise combined with essential amino acid supplementation and energy deficit on markers of skeletal muscle atrophy and regeneration during bed rest and active recovery. Muscle Nerve. 2010; 42: 927-35.
25. Polykandriotis E, Popescu LM, Horch RE. Regenerative medicine: then and now -an update of recent history into future possibilities. J Cell Mol Med. 2010; 14: 2350-8.
26. Rossi CA, Pozzobon M, De Coppi P. Advances in musculoskeletal tissue engineering: moving towards therapy. Organogenesis. 2010; 6: 167-72.
27. Sancricca C, Mirabella M, Gliubizzi C, et al Vessel-associated stem cells from skeletal muscle: From biology to future uses in cell therapy. World J Stem Cells. 2010; 2: 39-49.
28. Ten Broek RW, Grefte S, Von den Hoff JW. Regulatory factors and cell populations involved in skeletal muscle regeneration. J Cell Physiol. 2010; 224: 7-16.
29. Young AP, Wagers AJ. Pax3 induces differentiation of juvenile skeletal muscle stem cells without transcriptional upregulation of canonical myogenic regulatory factors. J Cell Sci. 2010; 123: 2632-9.
30. Suciu L, Popescu LM, Gherghiceanu M, et al Telocytes in human term placenta: morphology and phenotype. Cells Tissues Organs. 2010; 192: 325-39.
31. Suciu L, Nicolescu MI, Popescu LM. Cardiac telocytes: serial dynamic images in cell culture. J Cell Mol Med. 2010; 14: 2687-92.
32. Hinescu ME, Gherghiceanu M, Suciu L, et al Telocytes in pleura: two- and three-dimensional imaging by transmission electron microscopy. Cell Tissue Res. 2011; 343: 389-97.
33. Popescu LM, Gherghiceanu M, Manole CG, et al Cardiac renewing: interstitial Cajal-like cells nurse cardiomyocyte progenitors in epicardial stem cell niches. J Cell Mol Med. 2009; 13: 866-86.
34. Kostin S, Popescu LM. A distinct type of cell in myocardium: interstitial Cajal-like cells (ICLC). J Cell Mol Med. 2009; 13: 295-308.
35. Gherghiceanu M, Popescu LM. Cardiomyocyte precursors and telocytes in epicardial stem cell niche: electron microscope images. J Cell Mol Med. 2010; 14: 871-7.
36. Popescu LM, Manole CG, Gherghiceanu M, et al Telocytes in human epicardium. J Cell Mol Med. 2010; 14: 2085-93.
37. Gherghiceanu M, Manole CG, Popescu LM. Telocytes in endocardium: electron microscope evidence. J Cell Mol Med. 2010; 14: 2330-4.
38. Popescu LM, Faussone-Pellegrini MS. TELOCYTES-a case of serendipity: the winding way from Interstitial Cells of Cajal (ICC), via Interstitial Cajal-Like Cells (ICLC) to TELOCYTES. J Cell Mol Med. 2010; 14: 729-40.
39. Popescu LM, Gherghiceanu M, Kostin S, et al Telocytes and heart renewing. In: Wang P, Kuo CH, Takeda N, et al., editors, Adaptation biology and medicine: Volume 6: Cell adaptations and challenges. New Delhi: Narosa; 2011. p. 17-39.
40. Gherghiceanu M, Popescu LM. Heterocellular communication in the heart. Electron tomography of telocyte-myocyte junctions. J Cell Mol Med. 2011, in press.
41. Bani D, Formigli L, Gherghiceanu M, et al Telocytes as supporting cells for myocardial tissue organization in developing and adult heart. J Cell Mol Med. 2010; 14: 2531-8.
42. Kostin S. Myocardial telocytes: a specific new cellular entity. J Cell Mol Med. 2010; 14: 1917-21.
43. Eyden B, Curry A, Wang G. Stromal cells in the human gut show ultrastructural features of fibroblasts and smooth muscle cells but not myofibroblasts. J Cell Mol Med. 2010; doi.
44. Gittenberger-de Groot AC, Winter EM, Poelmann RE. Epicardium-derived cells (EPDCs) in development, cardiac disease and repair of ischemia. J Cell Mol Med. 2010; 14: 1056-60.
45. Faussone-Pellegrini MS, Bani D. Relationships between telocytes and cardiomyocytes during pre- and post natal life. J Cell Mol Med D. 2010; 14: 1061-3.
46. Tommila M. Granulation tissue formation. The effect of hydroxyapatite coating of cellulose on cellular differentiation. PhD Thesis, University of Turku, Finland ; 2010.
47. Zhou J, Zhang Y, Wen X, et al Telocytes accompanying cardiomyocyte in primary culture: two- and three-dimensional culture environment. J Cell Mol Med. 2010; 14: 2641-5.
48. Gevaert T, De Vos R, Everaerts W, et al Characterization of upper lamina propria interstitial cells in bladders from patients with neurogenic detrusor overactivity and bladder pain syndrome. J Cell Mol Med. 2011; doi.
49. Kostin S. Types of cardiomyocyte death and clinical outcomes in patients with heart failure. J Am Coll Cardiol. 2011; doi.
50. Radenkovic G. Two patterns of development of interstitial cells of Cajal in the human duodenum. J Cell Mol Med. 2011; doi.
51. Limana F, Capogrossi MC, Germani A. The epicardium in cardiac repair: from the stem cell view. Pharmacol Ther. 2011; 129: 82-96.
52. Carmona IC, Bartolomé MJ, Escribano CJ. Identification of telocytes in the lamina propria of rat duodenum: transmission electron microscopy. J Cell Mol Med. 2011; 15: 26-30.
53. Cantarero I, Luesma MJ, Junquera C. The primary cilium of telocytes in the vasculature: electron microscope imaging. J Cell Mol Med. 2011, in press.
54. Russell JL, Goetsch SC, Gaiano NR, et al A dynamic notch injury response activates epicardium and contributes to fibrosis repair. Circ Res. 2011; 108: 51-9.
55. Zhang YH, Zhang GW, Gu TX, et al Exogenous basic fibroblast growth factor promotes cardiac stem cell-mediated myocardial regeneration after miniswine acute myocardial infarction. Coron Artery Dis. 2011; doi.
56. Wu J, Li J, Zhang N, et al Stem cell-based therapies in ischemic heart diseases: a focus on aspects of microcirculation and inflammation. Basic Res Cardiol. 2011; doi.
57. Cismasiu VB, Radu E, Popescu LM. R-193 expression differentiates telocytes from other stromal cells. J Cell Mol Med. 2011; doi.
58. Jankowski RJ, Haluszczak C, Trucco M, et al Flow cytometric characterization of myogenic cell populations obtained via the preplate technique: potential for rapid isolation of muscle-derived stem cells. Hum Gene Ther. 2001; 12: 619-28.
59. Popescu LM. Telocytes and stem cells: a tandem in cardiac regenerative medicine. Curr Med Chem. 2011; 18: 94.
60. Clark MG, Wallis MG, Barrett EJ, et al Blood flow and muscle metabolism: a focus on insulin action. Am J Physiol Endocrinol Metab. 2003; 284: E241-58.
61. Mathew SJ, Hansen JM, Merrell AJ, et al Connective tissue fibroblasts and Tcf4 regulate myogenesis. Development. 2011; 138: 371-84.
62. Zammit PS, Partridge TA, Yablonka-Reuveni Z. The skeletal muscle satellite cell: the stem cell that came in from the cold. J Histochem Cytochem. 2006; 54: 1177-91.
63. Gnocchi VF, White RB, Ono Y, et al Further characterisation of the molecular signature of quiescent and activated mouse muscle satellite cells. PLoS One. 2009; 4: e5205.
64. Brack AS, Conboy IM, Conboy MJ, et al A temporal switch from notch to Wnt signaling in muscle stem cells is necessary for normal adult myogenesis. Cell Stem Cell. 2008; 2: 50-9.
65. Kuang S, Kuroda K, Le Grand F, et al Asymmetric self-renewal and commitment of satellite stem cells in muscle. Cell. 2007; 129: 999-1010.
66. Tsivitse S. Notch and Wnt signaling, physiological stimuli and postnatal myogenesis. Int J Biol Sci. 2010; 6: 268-81.
67. Biressi S, Rando TA. Heterogeneity in the muscle satellite cell population. Semin Cell Dev Biol. 2010; 21: 845-54.
68. Mitchell KJ, Pannérec A, Cadot B, et al Identification and characterization of a non-satellite cell muscle resident progenitor during postnatal development. Nat Cell Biol. 2010; 12: 257-66.
69. LaBarge MA, Blau HM. Biological progression from adult bone marrow to mononucleate muscle stem cell to multinucleate muscle fiber in response to injury. Cell. 2002; 111: 589-601.
70. Doyonnas R, LaBarge MA, Sacco A, et al Hematopoietic contribution to skeletal muscle regeneration by myelomonocytic precursors. Proc Natl Acad Sci U S A. 2004; 101: 13507-12.
71. Dellavalle A, Sampaolesi M, Tonlorenzi R, et al Pericytes of human skeletal muscle are myogenic precursors distinct from satellite cells. Nat Cell Biol. 2007; 9: 255-67.
72. Lee JY, Qu-Petersen Z, Cao B, et al Clonal isolation of muscle-derived cells capable of enhancing muscle regeneration and bone healing. J Cell Biol. 2000; 150: 1085-100.
73. Torrente Y, Tremblay JP, Pisati F, et al Intraarterial injection of muscle-derived CD34(+)Sca-1(+) stem cells restores dystrophin in mdx mice. J Cell Biol. 2001; 152: 335-48.
74. Asakura A, Seale P, Girgis-Gabardo A, et al Myogenic specification of side population cells in skeletal muscle. J Cell Biol. 2002; 159: 123-34.
75. - stem cells are situated hierarchically upstream of Pax7+ cells. Stem Cells Dev. 2008; 17: 653-67.
76. Waddell JN, Zhang P, Wen Y, et al Dlk1 is necessary for proper skeletal muscle development and regeneration. PLoS One. 2010; 5: e15055.