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

Volumn 27, Issue 4, 2009, Pages 949-960

  Shi, Ming ^a   Ishikawa, Masakazu ^a   Kamei, Naosuke ^a,b   Nakasa, Tomoyuki ^a   Adachi, Nobuo ^a   Deie, Masataka ^a   Asahara, Takayuki ^c   Ochi, Mitsuo ^a  

^a HIROSHIMA UNIVERSITY   (Japan)

^b RIKEN Center for Biosystems Dynamics Research   (Japan)

^c TOKAI UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

CD1331 cells; Endothelial progenitor cell; Muscle regeneration; Peripheral blood; Vasculogenesis

Indexed keywords

CD133 ANTIGEN; GRANULOCYTE COLONY STIMULATING FACTOR; PHOSPHATE BUFFERED SALINE;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CAPILLARY DENSITY; CELL DIFFERENTIATION; CELL FRACTIONATION; CONTROLLED STUDY; ENDOTHELIUM CELL; EXPERIMENTAL MODEL; FEMALE; GENE EXPRESSION; IMMUNOFLUORESCENCE; MICROENVIRONMENT; MUSCLE CELL; MUSCLE DEVELOPMENT; MUSCLE INJURY; MUSCLE REGENERATION; MYOFIBROSIS; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; RAT; TIBIALIS ANTERIOR MUSCLE;

ADULT; ANIMALS; ANTIGENS, CD; CELL DIFFERENTIATION; ENDOTHELIAL CELLS; FEMALE; FIBROSIS; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION; GLYCOPROTEINS; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HEMATOPOIETIC STEM CELLS; HUMANS; MALE; MUSCLE, SKELETAL; NEOVASCULARIZATION, PHYSIOLOGIC; PEPTIDES; RATS; RATS, NUDE; REGENERATION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

RATTUS;

EID: 65649141534     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1002/stem.4     Document Type: Article

References (55)

1. Chan YS, Li Y, Foster W et al. The use of suramin, an antifibrotic agent, to improve muscle recovery after strain injury. Am J Sports Med 2005;33:43-51. (Pubitemid 40039558)
2. Bernasconi P, Di Blasi C, Mora M et al. Transforming growth factorbeta1 and fibrosis in congenital muscular dystrophies. Neuromuscul Disord 1999;9:28-33. (Pubitemid 29079470)
3. Pardanaud L, Yassine F, Dieterlen-Lievre F.Relationship between vasculogenesis, angiogenesis and haematopoiesis during avian ontogeny. Development 1989;105:473-485. (Pubitemid 19093155)
4. Risau W, Sariola H, Zerwes HG et al. Vasculogenesis and angiogenesis in embryonic-stem-cell-derived embryoid bodies. Development 1988;102:471-4778. (Pubitemid 18062480)
5. Asahara T, Murohara T, Sullivan A et al. Isolation of putative progenitor endothelial cells for angiogenesis. Science 1997;275: 964-967. (Pubitemid 27087709)
6. Asahara T, Masuda H, Takahashi T et al. Bone marrow origin of endothelial progenitor cells responsible for postnatal vasculogenesis in physiological and pathological neovascularization. Circ Res 1999;85: 221-228. (Pubitemid 29377293)
7. Chan YS, Li Y, Foster W et al. The use of suramin, an antifibrotic agent, to improve muscle recovery after strain injury. Am J Sports Med 2005;33:43-51. (Pubitemid 30390303)
8. + cells after stroke enhances neurogenesis via angiogenesis in a mouse model. J Clin Invest 2004;114:330-338. (Pubitemid 39071605)
9. + blood cells accelerate vascularization and healing of diabetic mouse skin wounds. J Vasc Res 2003;40:368-377. (Pubitemid 37188106)
10. Matsumoto T, Kawamoto A, Kuroda R et al. Therapeutic potential of vasculogenesis and osteogenesis promoted by peripheral blood Cd34- positive cells for functional bone healing. Am J Pathol 2006;169: 1440-1457.
11. Tei K, Matsumoto T, Mifune Y et al. Administrations of peripheral blood CD34-positive cells contribute to medial collateral ligament healing via vasculogenesis. Stem Cells 2008;26:819-830.
12. + cells from human peripheral blood promote corticospinal axon regeneration. Neuroreport 2008;19:799-803.
13. + cells derived from human peripheral blood can promote regeneration of peripheral nerve. J Neurosurg 2008 [Epub ahead of print].
14. Iwasaki H, Kawamoto A, Ishikawa M et al. Dose-dependent contribution of CD34-positive cell transplantation to concurrent vasculogenesis and cardiomyogenesis for functional regenerative recovery after myocardial infarction. Circulation 2006;113:1311-1325. (Pubitemid 43739453)
15. Yin AH, Miraglia S, Zaniani ED et al. AC133, a novel marker for human hematopoietic stem and progenitor cells. Blood 1997;90: 5002-5012. (Pubitemid 28007217)
16. Miraglia S, Godfrey W, Yin AH et al. A novel five-transmembrane hematopoietic stem cell antigen: Isolation, characterization, and molecular cloning. Blood 1997;90:5013-5021. (Pubitemid 28007218)
17. Bhatia M, Bonnet D, Murdoch B et al. A newly discovered class of human hematopoietic cells with SCID-repopulating activity. Nat Med 1998;4:1038-1045. (Pubitemid 28417336)
18. Fujisaki T, Berger MG, Rose-John S et al. Rapid differentiation of a rare subset of adult human Lin-CD34-CD38- cells stimulated by multiple growth factors in vitro. Blood 1999;94:1926-1932.
19. Gallacher L, Murdoch B, Wu DM et al. Isolation and characterization of human CD34(-)Lin(-) and CD34(+)Lin(-) hematopoietic stem cells using cell surface markers AC133 and CD7. Blood 2000;95: 2813-2820. (Pubitemid 30235890)
20. + human cord blood cells. J Hematother StemCell Res 2000;9:827-840. (Pubitemid 32110281)
21. Mizrak D, Brittan M, Alison MR.CD133: Molecule of the moment. J Pathol 2008;214:3-9.
22. Natsu K, Ochi M, Mochizuki Y et al. Allogenic bone marrow-derived mesenchymal stromal cells promote the regeneration of injured skeletal muscle without differentiation intomyofibers. Tissue Eng 2004;10:1093-1112. (Pubitemid 39223789)
23. Foster W, Li Y, Usas A et al. Gamma interferon as an antifibrosis agent in skeletal muscle. J Orthop Res 2003;21:798-804. (Pubitemid 37045557)
24. Sato K, Li Y, Foster W et al. Improvement of muscle healing through enhancement of muscle regeneration and prevention of fibrosis. Muscle Nerve 2003;28:365-372.
25. Fukushima K, Badiani N, Usas A et al. The use of an antifibrosis agent to improve muscle recovery after laceration. Am J Sports Med 2001;29:394-402. (Pubitemid 32661352)
26. Li Y, Foster W, Deasy B et al. TGF-b1 induces the differentiation of myogenic cells into fibrotic cells in injured skeletal muscle, a key event in muscle fibrogenesis. Am J Pathol 2004;164:895-907.
27. Stratos I, Rotter R, Eipel C et al. Granulocyte-colony stimulating factor enhances muscle proliferation and strength following skeletal muscle injury in rats. J Appl Physiol 2007;103:1857-1863. (Pubitemid 350033874)
28. Seale P, Sabourin LA, Girqis-Gabardo A et al. Pax7 is required for the specification of myogenic satellite cells. Cell 2000;102:777-786.
29. Peault B, Rudnicki M, Torrente Y et al. Stem and progenitor cells in skeletal muscle development, maintenance, and therapy. Mol Ther 2007;15:867-877. (Pubitemid 46621645)
30. Sjöberg G, Jiang WQ, Ringertz NR et al. Colocalization of nestin and vimentin/desmin in skeletal muscle cells demonstrated by threedimensional fluorescence digital imaging microscopy. Exp Cell Res 1994;214:447-458. (Pubitemid 24310802)
31. Maharaj AS, Saint-Geniez M, Maldonado AE et al. Vascular endothelial growth factor localization in the adult. Am J Pathol 2006;168:639-648. (Pubitemid 43271161)
32. Arsic N, Zacchigna S, Zentilin L et al. Vascular endothelial growth factor stimulates skeletal muscle regeneration in vivo. Mol Ther 2004; 10:844-854. (Pubitemid 39419911)
33. Storkebaum E, Lambrechts D, Carmeliet P.VEGF: Once regarded as a specific angiogenic factor, now implicated in neuroprotection. Bioessays 2004;26:943-954. (Pubitemid 39273068)
34. Rissanen TT, Vajanto I, Hiltunen MO et al. Expression of vascular endothelial growth factor and vascular endothelial growth factor receptor- 2 (KDR/Flk-1) in ischemic skeletal muscle and its regeneration. Am J Pathol 2002;160:1393-1403. (Pubitemid 34411643)
35. Smythe GM, Lai MC, Grounds MD et al. Adeno-associated virusmediated vascular endothelial growth factor gene therapy in skeletal muscle before transplantation promotes revascularization of regenerating muscle. Tissue Eng 2002;8:879-891. (Pubitemid 35239766)
36. Prior BM, Yang HT, Terjung RL.What makes vessels grow with exercise training?J Appl Physiol 2004;97:1119-1128. (Pubitemid 39121441)
37. Yan H, Guo Y, Zhang P et al. Superior neovascularization and muscle regeneration in ischemic skeletal muscles following VEGF gene transfer by rAAV1 pseudotyped vectors. Biochem Biophys Res Commun 2005;336:287-298. (Pubitemid 41253433)
38. Wagatsuma A.Endogenous expression of angiogenesis-related factors in response to muscle injury. Mol Cell Biochem 2007;298: 151-159. (Pubitemid 46605292)
39. Xia JH, Xie AN, Zhang KL et al. The vascular endothelial growth factor expression and vascular regeneration in infarcted myocardium by skeletal muscle satellite cells. Chin Med J 2006;119:117-121. (Pubitemid 43796927)
40. Bryan BA, Walshe TE, Mitchell DC et al. Coordinated vascular endothelial growth factor expression and signaling during skeletal myogenic differentiation. Mol Biol Cell 2008;19:994-1006.
41. Tateno K, Minamino T, Toko H et al. Critical roles of musclesecreted angiogenic factors in therapeutic neovascularization. Circ Res 2006;98:1194-1202. (Pubitemid 43948106)
42. Nikolaou PK, Macdonald BL, Glisson RR et al. Biomechanical and histological evaluation of muscle after controlled strain injury. J Sports Med 1987;15:9-14. (Pubitemid 17011025)
43. Taylor DC, Dalton JD Jr,Seaber AV et al. Experimental muscle strain injury: Early functional and structural deficits and the increased risk for reinjury. Am J Sports Med 1993;21:190-194. (Pubitemid 23096797)
44. Menetrey J, Kasemkijwattana C, Fu FH et al. Suturing versus immobilization of a muscle laceration. A morphological and functional study in a mouse model. Am J Sports Med 1999;27:222-229. (Pubitemid 29138545)
45. Border WA, Noble NA.Transforming growth factor beta in tissue fibrosis. N Engl J Med 1994;331:1286-1292.
46. Bernasconi P, Torchiana E, Confalonieri P et al. Expression of transforming growth factor-beta 1 in dystrophic patient muscles correlates with fibrosis: Pathogenetic role of a fibrogenic cytokine. J Clin Invest 1996;96:1137-1144.
47. Bernasconi P, Di Blasi C, Mora M et al. Transforming growth factorbeta1 and fibrosis in congenital muscular dystrophies. Neuromuscul Disord 1999;9:28-33. (Pubitemid 29079470)
48. Olguin HC, Olwin BB.Pax-7 up-regulation inhibits myogenesis and cell cycle progression in satellite cells: A potential mechanism for self-renewal. Dev Biol 2004;275:375-388. (Pubitemid 40292025)
49. Oustanina S, Hause G, Braun T.Pax7 directs postnatal renewal and propagation of myogenic satellite cells but not their specification. EMBO J 2004;23:3430-3439. (Pubitemid 39209166)
50. Zammit PS, Golding JP, Nagata Y.Muscle satellite cells adopt divergent fates: A mechanism for self-renewal?J Cell Biol 2004;166:347-357. (Pubitemid 39031238)
51. Kuang S, Charge SB, Seale P et al. Distinct roles for Pax7 and Pax3 in adult regenerative myogenesis. J Cell Biol 2006;172:103-113. (Pubitemid 43042633)
52. Shinin V, Gayraud-Morel B, Gomes D et al. Asymmetric division and cosegregation of template DNA strands in adult muscle satellite cells. Nat Cell Biol 2006;8:677-687.
53. Olguin HC, Yang Z, Tapscott SJ et al. Reciprocal inhibition between Pax7 and muscle regulatory factors modulates myogenic cell fate determination. J Cell Biol 2007;177:769-779. (Pubitemid 46873084)
54. Gayraud-Morel B, Chretien F, Flamant P et al. A role for the myogenic determination gene Myf5 in adult regenerative myogenesis. Dev Biol 2007;312:13-28. (Pubitemid 350180743)
55. Messina S, Mazzeo A, Bitto A et al. VEGF overexpression via adenoassociated virus gene transfer promotes skeletal muscle regeneration and enhances muscle function in mdx mice. FASEB J 2007;21: 3737-3746. (Pubitemid 350075161)