Sdf-1 (CXCL12) improves skeletal muscle regeneration via the mobilisation of Cxcr4 and CD34 expressing cells

Biology of the Cell

Volumn 104, Issue 12, 2012, Pages 722-737

  Brzoska, Edyta ^a   Kowalewska, Magdalena ^b   Markowska Zagrajek, Agnieszka ^a   Kowalski, Kamil ^a   Archacka, Karolina ^a   Zimowska, Malgorzata ^a   Grabowska, Iwona ^a   Czerwińska, Areta M ^a   Czarnecka Góra, Magdalena ^a   Stremińska, Wladyslawa ^a   Jańczyk Ilach, Katarzyna ^a   Ciemerych, Maria A ^a  

^a UNIVERSITY OF WARSAW   (Poland)

^b INSTITUTE OF ONCOLOGY   (Poland)

Author keywords

Cxcr4; Differentiation; Myoblast; Sdf 1 (CXCL12); Skeletal muscle

Indexed keywords

CD34 ANTIGEN; CHEMOKINE RECEPTOR CXCR4; GELATINASE A; GELATINASE B; MESSENGER RNA; MYOD1 PROTEIN; MYOGENIC FACTOR 5; MYOGENIN; STROMAL CELL DERIVED FACTOR 1; TRANSCRIPTION FACTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME ACTIVITY; MUSCLE REGENERATION; MYOBLAST; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SKELETAL MUSCLE; SKELETAL MUSCLE SATELLITE CELL; SOLEUS MUSCLE;

ANIMALS; ANTIGENS, CD34; CELL PROLIFERATION; CHEMOKINE CXCL12; EXTRACELLULAR MATRIX; GENE EXPRESSION REGULATION; MALE; MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASE 9; MUSCLE PROTEINS; MUSCLE, SKELETAL; RATS; RECEPTORS, CXCR4; REGENERATION; SATELLITE CELLS, SKELETAL MUSCLE;

EID: 84870434818     PISSN: 02484900     EISSN: 1768322X     Source Type: Journal    
DOI: 10.1111/boc.201200022     Document Type: Article

References (70)

1. Abbott, J.D., Huang, Y., Liu, D., Hickey, R., Krause, D.S. and Giordano, F.J. (2004) Stromal cell-derived factor-1alpha plays a critical role in stem cell recruitment to the heart after myocardial infarction but is not sufficient to induce homing in the absence of injury. Circulation 110, 3300-3305
2. Abedi, M., Foster, B.M., Wood, K.D., Colvin, G.A., McLean, S.D., Johnson, K.W. and Greer, D.A. (2007) Haematopoietic stem cells participate in muscle regeneration. Br. J. Haematol. 138, 792-801
3. Aiuti, A., Webb, I.J., Bleul, C., Springer, T. and Gutierrez-Ramos, J.C. (1997) The chemokine SDF-1 is a chemoattractant for human CD34+ hematopoietic progenitor cells and provides a new mechanism to explain the mobilization of CD34+ progenitors to peripheral blood. J. Exp. Med. 185, 111-120
4. Barberi, T., Bradbury, M., Dincer, Z., Panagiotakos, G., Socci, N.D. and Studer, L. (2007) Derivation of engraftable skeletal myoblasts from human embryonic stem cells. Nat. Med. 13, 642-648
5. Bassaglia, Y. and Gautron, J. (1995) Fast and slow rat muscles degenerate and regenerate differently after whole crush injury. J. Muscle Res. Cell Motil. 16, 420-429
6. Blau, H.M., Pavlath, G.K., Hardeman, E.C., Chiu, C.P., Silberstein, L., Webster, S.G., Miller, S.C. and Webster, C. (1985) Plasticity of the differentiated state. Science 230, 758-766
7. Bleul, C.C., Fuhlbrigge, R.C., Casasnovas, J.M., Aiuti, A. and Springer, T.A. (1996) A highly efficacious lymphocyte chemoattractant, stromal cell-derived factor 1 (SDF-1). J. Exp. Med. 184, 1101-1109
8. Brzoska, E., Ciemerych, M.A., Przewozniak, M. and Zimowska, M. (2011) Regulation of muscle stem cells activation-the role of growth factors and extracellular matrix. Vitam Horm 87, 239-276
9. Brzoska, E., Grabowska, I., Hoser, G., Streminska, W., Wasilewska, D., Machaj, E.K., Pojda, Z., Moraczewski, J. and Kawiak, J. (2006) Participation of stem cells from human cord blood in skeletal muscle regeneration of SCID mice. Exp. Hematol. 34, 1262-1270
10. Chamberlain, J.S., Jaynes, J.B. and Hauschka, S.D. (1985) Regulation of creatine kinase induction in differentiating mouse myoblasts. Mol. Cell. Biol. 5, 484-492
11. Ciemerych, M.A., Archacka, K., Grabowska, I. and Przewozniak, M. (2011). Cell cycle regulation during proliferation and differentiation of mammalian muscle precursor cells. In: Cell Cycle in Development, Results and Problems in Cell Differentiation, vol. 53; (J.Z. Kubiak, Ed.), pp.498-507, Berlin/Heidelberg, Germany: Springer-Verlag
12. Cote, C.K., DiMezzo, T.L., Banks, D.J., France, B., Bradley, K.A. and Welkos, S.L. (2008) Early interactions between fully virulent Bacillus anthracis and macrophages that influence the balance between spore clearance and development of a lethal infection. Microbes Infect. 10, 613-619
13. Darabi, R., Gehlbach, K., Bachoo, R.M., Kamath, S., Osawa, M., Kamm, K.E., Kyba, M. and Perlingeiro, R.C. (2008) Functional skeletal muscle regeneration from differentiating embryonic stem cells. Nat. Med. 14, 134-143
14. De Bari, C., Dell'Accio, F., Vandenabeele, F., Vermeesch, J.R., Raymackers, J.M. and Luyten, F.P. (2003) Skeletal muscle repair by adult human mesenchymal stem cells from synovial membrane. J. Cell Biol. 160, 909-918
15. Dellavalle, A., Sampaolesi, M., Tonlorenzi, R., Tagliafico, E., Sacchetti, B., Perani, L., Innocenzi, A., Galvez, B.G., Messina, G., Morosetti, R., Li, S., Belicchi, M., Peretti, G., Chamberlain, J.S., Wright, W.E., Torrente, Y., Ferrari, S., Bianco, P. and Cossu, G. (2007) Pericytes of human skeletal muscle are myogenic precursors distinct from satellite cells. Nat. Cell Biol. 9, 255-267
16. Dreyfus, P.A., Chretien, F., Chazaud, B., Kirova, Y., Caramelle, P., Garcia, L., Butler-Browne, G. and Gherardi, R.K. (2004) Adult bone marrow-derived stem cells in muscle connective tissue and satellite cell niches. Am. J. Pathol. 164, 773-779
17. Fadini, G.P., Sartore, S., Schiavon, M., Albiero, M., Baesso, I., Cabrelle, A., Agostini, C. and Avogaro, A. (2006) Diabetes impairs progenitor cell mobilisation after hindlimb ischaemia-reperfusion injury in rats. Diabetologia 49, 3075-3084
18. Galvez, B.G., Sampaolesi, M., Brunelli, S., Covarello, D., Gavina, M., Rossi, B., Constantin, G., Torrente, Y. and Cossu, G. (2006) Complete repair of dystrophic skeletal muscle by mesoangioblasts with enhanced migration ability. J. Cell Biol. 174, 231-243
19. Gao, H., Priebe, W., Glod, J. and Banerjee, D. (2009) Activation of signal transducers and activators of transcription 3 and focal adhesion kinase by stromal cell-derived factor 1 is required for migration of human mesenchymal stem cells in response to tumor cell-conditioned medium. Stem Cells 27, 857-865
20. Gavina, M., Belicchi, M., Rossi, B., Ottoboni, L., Colombo, F., Meregalli, M., Battistelli, M., Forzenigo, L., Biondetti, P., Pisati, F., Parolini, D., Farini, A., Issekutz, A.C., Bresolin, N., Rustichelli, F., Constantin, G. and Torrente, Y. (2006) VCAM-1 expression on dystrophic muscle vessels has a critical role in the recruitment of human blood-derived CD133+ stem cells after intra-arterial transplantation. Blood 108, 2857-2866
21. Gomperts, B.N., Belperio, J.A., Rao, P.N., Randell, S.H., Fishbein, M.C., Burdick, M.D. and Strieter, R.M. (2006) Circulating progenitor epithelial cells traffic via CXCR4/CXCL12 in response to airway injury. J. Immunol. 176, 1916-1927
22. Grabowska, I., Brzoska, E., Gawrysiak, A., Streminska, W., Moraczewski, J., Polanski, Z., Hoser, G., Kawiak, J., Machaj, E.K., Pojda, Z. and Ciemerych, M.A. (2012) Restricted myogenic potential of mesenchymal stromal cells isolated from umbilical cord. Cell Transplant 21, in press
23. Grymula, K., Tarnowski, M., Wysoczynski, M., Drukala, J., Barr, F.G., Ratajczak, J., Kucia, M. and Ratajczak, M.Z. (2010) Overlapping and distinct role of CXCR7-SDF-1/ITAC and CXCR4-SDF-1 axes in regulating metastatic behavior of human rhabdomyosarcomas. Int. J. Cancer 127, 2554-2568
24. Guttinger, M., Tafi, E., Battaglia, M., Coletta, M. and Cossu, G. (2006) Allogeneic mesoangioblasts give rise to alpha-sarcoglycan expressing fibers when transplanted into dystrophic mice. Exp. Cell Res. 312, 3872-3879
25. Hess, D., Li, L., Martin, M., Sakano, S., Hill, D., Strutt, B., Thyssen, S., Gray, D.A. and Bhatia, M. (2003) Bone marrow-derived stem cells initiate pancreatic regeneration. Nat. Biotechnol. 21, 763-770
26. Horsley, V. and Pavlath, G.K. (2004) Forming a multinucleated cell: molecules that regulate myoblast fusion. Cells Tissues Organs 176, 67-78
27. Kamochi, H., Kurokawa, M.S., Yoshikawa, H., Ueda, Y., Masuda, C., Takada, E., Watanabe, K., Sakakibara, M., Natuki, Y., Kimura, K., Beppu, M., Aoki, H. and Suzuki, N. (2006) Transplantation of myocyte precursors derived from embryonic stem cells transfected with IGFII gene in a mouse model of muscle injury. Transplantation 82, 516-526
28. Kijowski, J., Baj-Krzyworzeka, M., Majka, M., Reca, R., Marquez, L.A., Christofidou-Solomidou, M., Janowska-Wieczorek, A. and Ratajczak, M.Z. (2001) The SDF-1-CXCR4 axis stimulates VEGF secretion and activates integrins but does not affect proliferation and survival in lymphohematopoietic cells. Stem Cells 19, 453-466
29. Kollet, O., Shivtiel, S., Chen, Y.Q., Suriawinata, J., Thung, S.N., Dabeva, M.D., Kahn, J., Spiegel, A., Dar, A., Samira, S., Goichberg, P., Kalinkovich, A., Arenzana-Seisdedos, F., Nagler, A., Hardan, I., Revel, M., Shafritz, D.A. and Lapidot, T. (2003) HGF, SDF-1, and MMP-9 are involved in stress-induced human CD34+ stem cell recruitment to the liver. J. Clin. Invest. 112, 160-169
30. Kucia, M., Dawn, B., Hunt, G., Guo, Y., Wysoczynski, M., Majka, M., Ratajczak, J., Rezzoug, F., Ildstad, S.T., Bolli, R. and Ratajczak, M.Z. (2004a) Cells expressing early cardiac markers reside in the bone marrow and are mobilized into the peripheral blood after myocardial infarction. Circ. Res. 95, 1191-1199
31. Kucia, M., Jankowski, K., Reca, R., Wysoczynski, M., Bandura, L., Allendorf, D.J., Zhang, J., Ratajczak, J. and Ratajczak, M.Z. (2004b) CXCR4-SDF-1 signalling, locomotion, chemotaxis and adhesion. J. Mol. Histol. 35, 233-245
32. Kucia, M., Ratajczak, J., Reca, R., Janowska-Wieczorek, A. and Ratajczak, M.Z. (2004c) Tissue-specific muscle, neural and liver stem/progenitor cells reside in the bone marrow, respond to an SDF-1 gradient and are mobilized into peripheral blood during stress and tissue injury. Blood Cells Mol. Dis. 32, 52-57
33. Kucia, M., Wojakowski, W., Reca, R., Machalinski, B., Gozdzik, J., Majka, M., Baran, J., Ratajczak, J. and Ratajczak, M.Z. (2006) The migration of bone marrow-derived non-hematopoietic tissue-committed stem cells is regulated in an SDF-1-, HGF-, and LIF-dependent manner. Arch. Immunol. Ther. Exp. (Warsz) 54, 121-135
34. Kuliszewski, M.A., Kobulnik, J., Lindner, J.R., Stewart, D.J. and Leong-Poi, H. (2011) Vascular gene transfer of SDF-1 promotes endothelial progenitor cell engraftment and enhances angiogenesis in ischemic muscle. Mol. Ther. 19, 895-902
35. LaBarge, M.A. and Blau, H.M. (2002) Biological progression from adult bone marrow to mononucleate muscle stem cell to multinucleate muscle fiber in response to injury. Cell 111, 589-601
36. Majka, M., Ratajczak, J., Kowalska, M.A. and Ratajczak, M.Z. (2000) Binding of stromal derived factor-1alpha (SDF-1alpha) to CXCR4 chemokine receptor in normal human megakaryoblasts but not in platelets induces phosphorylation of mitogen-activated protein kinase p42/44 (MAPK), ELK-1 transcription factor and serine/threonine kinase AKT. Eur. J. Haematol. 64, 164-172
37. Maksym, R.B., Tarnowski, M., Grymula, K., Tarnowska, J., Wysoczynski, M., Liu, R., Czerny, B., Ratajczak, J., Kucia, M. and Ratajczak, M.Z. (2009) The role of stromal-derived factor-1-CXCR7 axis in development and cancer. Eur. J. Pharmacol. 625, 31-40
38. Melchionna, R., Di Carlo, A., De Mori, R., Cappuzzello, C., Barberi, L., Musaro, A., Cencioni, C., Fujii, N., Tamamura, H., Crescenzi, M., Capogrossi, M.C., Napolitano, M. and Germani, A. (2010) Induction of myogenic differentiation by SDF-1 via CXCR4 and CXCR7 receptors. Muscle Nerve 41, 828-835
39. Mitchell, K.J., Pannerec, A., Cadot, B., Parlakian, A., Besson, V., Gomes, E.R., Marazzi, G. and Sassoon, D.A. (2010) Identification and characterization of a non-satellite cell muscle resident progenitor during postnatal development. Nat. Cell Biol. 12, 257-266
40. Mizuno, Y., Chang, H., Umeda, K., Niwa, A., Iwasa, T., Awaya, T., Fukada, S., Yamamoto, H., Yamanaka, S., Nakahata, T. and Heike, T. (2010) Generation of skeletal muscle stem/progenitor cells from murine induced pluripotent stem cells. FASEB J. 24, 2245-2253
41. Moore, M.A., Hattori, K., Heissig, B., Shieh, J.H., Dias, S., Crystal, R.G. and Rafii, S. (2001) Mobilization of endothelial and hematopoietic stem and progenitor cells by adenovector-mediated elevation of serum levels of SDF-1, VEGF, and angiopoietin-1. Ann. N. Y. Acad. Sci. 938, 36-45; discussion 45-37
42. Moraczewski, J., Martelly, I. and Gautron, J. (1988) Phorbol ester binding to isolated muscle satellite cells compared to fetal myogenic cells from the rat. Monogr. Dev. Biol. 21, 78-83
43. Morosetti, R., Gidaro, T., Broccolini, A., Gliubizzi, C., Sancricca, C., Tonali, P.A., Ricci, E. and Mirabella, M. (2010) Mesoangioblasts from facioscapulohumeral muscular dystrophy display in vivo a variable myogenic ability predictable by their in vitro behavior. Cell Transplant. 20, 1299-1313
44. Odemis, V., Boosmann, K., Dieterlen, M.T. and Engele, J. (2007) The chemokine SDF1 controls multiple steps of myogenesis through atypical PKCzeta. J. Cell Sci. 120, 4050-4059
45. Odemis, V., Boosmann, K., Heinen, A., Kury, P. and Engele, J. (2010) CXCR7 is an active component of SDF-1 signalling in astrocytes and Schwann cells. J. Cell Sci. 123, 1081-1088
46. Palermo, A.T., Labarge, M.A., Doyonnas, R., Pomerantz, J. and Blau, H.M. (2005) Bone marrow contribution to skeletal muscle: a physiological response to stress. Dev. Biol. 279, 336-344
47. Pallafacchina, G., Francois, S., Regnault, B., Czarny, B., Dive, V., Cumano, A., Montarras, D. and Buckingham, M. (2010) An adult tissue-specific stem cell in its niche: a gene profiling analysis of in vivo quiescent and activated muscle satellite cells. Stem Cell Res. 4, 77-91
48. Perez, A.L., Bachrach, E., Illigens, B.M., Jun, S.J., Bagden, E., Steffen, L., Flint, A., McGowan, F.X., Del Nido, P., Montecino-Rodriguez, E., Tidball, J.G. and Kunkel, L.M. (2009) CXCR4 enhances engraftment of muscle progenitor cells. Muscle Nerve 40, 562-572
49. Ratajczak, M.Z., Kucia, M., Reca, R., Majka, M., Janowska-Wieczorek, A. and Ratajczak, J. (2004) Stem cell plasticity revisited: CXCR4-positive cells expressing mRNA for early muscle, liver and neural cells 'hide out' in the bone marrow. Leukemia 18, 29-40
50. Ratajczak, M.Z., Majka, M., Kucia, M., Drukala, J., Pietrzkowski, Z., Peiper, S. and Janowska-Wieczorek, A. (2003) Expression of functional CXCR4 by muscle satellite cells and secretion of SDF-1 by muscle-derived fibroblasts is associated with the presence of both muscle progenitors in bone marrow and hematopoietic stem/progenitor cells in muscles. Stem Cells 21, 363-371
51. Ratajczak, M.Z., Zuba-Surma, E., Kucia, M., Reca, R., Wojakowski, W. and Ratajczak, J. (2006) The pleiotropic effects of the SDF-1-CXCR4 axis in organogenesis, regeneration and tumorigenesis. Leukemia 20, 1915-1924
52. Rosenblatt, J.D., Lunt, A.I., Parry, D.J. and Partridge, T.A. (1995) Culturing satellite cells from living single muscle fiber explants. In Vitro Cell. Dev. Biol. Anim. 31, 773-779
53. 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
54. Sampaolesi, M., Torrente, Y., Innocenzi, A., Tonlorenzi, R., D'Antona, G., Pellegrino, M.A., Barresi, R., Bresolin, N., De Angelis, M.G., Campbell, K.P., Bottinelli, R. and Cossu, G. (2003) Cell therapy of alpha-sarcoglycan null dystrophic mice through intra-arterial delivery of mesoangioblasts. Science 301, 487-492
55. Shi, M., Ishikawa, M., Kamei, N., Nakasa, T., Adachi, N., Deie, M., Asahara, T. and Ochi, M. (2009) Acceleration of skeletal muscle regeneration in a rat skeletal muscle injury model by local injection of human peripheral blood-derived CD133-positive cells. Stem Cells 27, 949-960
56. Smith, C., Halvorsen, B., Otterdal, K., Waehre, T., Yndestad, A., Fevang, B., Sandberg, W.J., Breland, U.M., Froland, S.S., Oie, E., Gullestad, L., Damas, J.K. and Aukrust, P. (2008) High levels and inflammatory effects of soluble CXC ligand 16 (CXCL16) in coronary artery disease: down-regulatory effects of statins. Cardiovasc. Res. 79, 195-203
57. Son, B.R., Marquez-Curtis, L.A., Kucia, M., Wysoczynski, M., Turner, A.R., Ratajczak, J., Ratajczak, M.Z. and Janowska-Wieczorek, A. (2006) Migration of bone marrow and cord blood mesenchymal stem cells in vitro is regulated by stromal-derived factor-1-CXCR4 and hepatocyte growth factor-c-met axes and involves matrix metalloproteinases. Stem Cells 24, 1254-1264
58. Stauber, W.T., Fritz, V.K. and Dahlmann, B. (1990) Extracellular matrix changes following blunt trauma to rat skeletal muscles. Exp. Mol. Pathol. 52, 69-86
59. Tanaka, K.K., Hall, J.K., Troy, A.A., Cornelison, D.D., Majka, S.M. and Olwin, B.B. (2009) Syndecan-4-expressing muscle progenitor cells in the SP engraft as satellite cells during muscle regeneration. Cell Stem Cell 4, 217-225
60. Tidball, J.G. (1995) Inflammatory cell response to acute muscle injury. Med. Sci. Sports Exerc. 27, 1022-1032
61. Togel, F., Isaac, J., Hu, Z., Weiss, K. and Westenfelder, C. (2005) Renal SDF-1 signals mobilization and homing of CXCR4-positive cells to the kidney after ischemic injury. Kidney Int. 67, 1772-1784
62. Torrente, Y., Belicchi, M., Sampaolesi, M., Pisati, F., Meregalli, M., D'Antona, G., Tonlorenzi, R., Porretti, L., Gavina, M., Mamchaoui, K., Pellegrino, M.A., Furling, D., Mouly, V., Butler-Browne, G.S., Bottinelli, R., Cossu, G. and Bresolin, N. (2004) Human circulating AC133(+) stem cells restore dystrophin expression and ameliorate function in dystrophic skeletal muscle. J. Clin. Invest. 114, 182-195
63. Vandesompele, J., De Preter, K., Pattyn, F., Poppe, B., Van Roy, N., De Paepe, A. and Speleman, F. (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 3, RESEARCH0034
64. Welle, S., Bhatt, K. and Thornton, C.A. (1999) Inventory of high-abundance mRNAs in skeletal muscle of normal men. Genome Res. 9, 506-513
65. Wojakowski, W., Tendera, M., Michalowska, A., Majka, M., Kucia, M., Maslankiewicz, K., Wyderka, R., Ochala, A. and Ratajczak, M.Z. (2004) Mobilization of CD34/CXCR4+, CD34/CD117+, c-met+ stem cells, and mononuclear cells expressing early cardiac, muscle, and endothelial markers into peripheral blood in patients with acute myocardial infarction. Circulation 110, 3213-3220
66. Wright, D.E., Bowman, E.P., Wagers, A.J., Butcher, E.C. and Weissman, I.L. (2002) Hematopoietic stem cells are uniquely selective in their migratory response to chemokines. J. Exp. Med. 195, 1145-1154
67. Yaffe, D. and Saxel, O. (1977) Serial passaging and differentiation of myogenic cells isolated from dystrophic mouse muscle. Nature 270, 725-727
68. Zammit, P.S. (2008) All muscle satellite cells are equal, but are some more equal than others? J. Cell Sci. 121, 2975-2982
69. Zimowska, M., Brzoska, E., Swierczynska, M., Streminska, W. and Moraczewski, J. (2008) Distinct patterns of MMP-9 and MMP-2 activity in slow and fast twitch skeletal muscle regeneration in vivo. Int. J. Dev. Biol. 52, 307-314
70. Zimowska, M., Duchesnay, A., Dragun, P., Oberbek, A., Moraczewski, J. and Martelly, I. (2009) Immunoneutralization of TGFbeta1 improves skeletal muscle regeneration: effects on myoblast differentiation and glycosaminoglycan content. Int. J. Cell Biol. 2009, 659372