Sonic hedgehog regulates angiogenesis and myogenesis during post-natal skeletal muscle regeneration

Journal of Cellular and Molecular Medicine

Volumn 13, Issue 8 B, 2009, Pages 2424-2435

  Straface, Giuseppe ^a   Aprahamian, Tamar ^b   Flex, Andrea ^a   Gaetani, Eleonora ^a   Biscetti, Federico ^a   Smith, Roy C ^c   Pecorini, Giovanni ^a   Pola, Enrico ^a   Angelini, Flavia ^a   Stigliano, Egidio ^a   Castellot Jr , John J ^c   Losordo, Douglas W ^d   Pola, Roberto ^a,c,e  

^a CATHOLIC UNIVERSITY   (Italy)

^b BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d NORTHWESTERN UNIVERSITY   (United States)

^e OASI RESEARCH INSTITUTE IRCCS   (Italy)

Author keywords

Angiogenesis; Myogenesis; Skeletal muscle regeneration; Sonic hedgehog

Indexed keywords

SHH PROTEIN, MOUSE; SONIC HEDGEHOG PROTEIN;

ANGIOGENESIS; ANIMAL; ARTICLE; C57BL MOUSE; MOUSE; PHYSIOLOGY; REGENERATION; SKELETAL MUSCLE; VASCULARIZATION;

ANIMALS; HEDGEHOG PROTEINS; MICE; MICE, INBRED C57BL; MUSCLE, SKELETAL; NEOVASCULARIZATION, PHYSIOLOGIC; REGENERATION;

ERINACEIDAE;

EID: 72949097878     PISSN: 15821838     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1582-4934.2008.00440.x     Document Type: Article

References (54)

1. Kogerman P, Grimm T, Kogerman L, et al. Mammalian suppressor-of-fused modulates nuclear-cytoplasmic shuttling of Gli-1. Nat Cell Biol. 1999 1 : 312 319.
2. Borycki AG, Brunk B, Tajbakhsh S, et al. Sonic hedgehog controls epaxial muscle determination through Myf5 activation. Development. 1999 126 : 4053 4063.
3. Kruger M, Mennerich D, Fees S, et al. Sonic hedgehog is a survival factor for hypaxial muscles during mouse development. Development. 2001 128 : 743 752.
4. Pola R, Ling LE, Aprahamian TR, et al. Postnatal recapitulation of embryonic hedgehog pathway in response to skeletal muscle ischemia. Circulation. 2003 108 : 479 485.
5. Kusano KF, Pola R, Murayama T, et al. Sonic hedgehog myocardial gene therapy: tissue repair through transient reconstitution of embryonic signaling. Nat Med. 2005 11 : 1197 1204.
6. Pola R, Ling LE, Silver M, et al. The morphogen Sonic hedgehog is an indirect angiogenic agent upregulating two families of angiogenic growth factors. Nat Med. 2001 7 : 706 711.
7. Kusano KF, Allendoerfer KL, Munger W, et al. Sonic hedgehog induces arteriogenesis in diabetic vasa nervorum and restores function in diabetic neuropathy. Arterioscler Thromb Vasc Biol. 2004 24 : 2102 2107.
8. Mitchell CA, McGeachie JK, Grounds MD. Cellular differences in the regeneration of murine skeletal muscle: a quantitative histological study in SJL/J and BALB/c mice. Cell Tissue Res. 1992 269 : 159 166.
9. Hirata A, Masuda S, Tamura T, et al. Expression profiling of cytokines and related genes in regenerating skeletal muscle after cardiotoxin injection: a role for osteopontin. Am J Pathol. 2003 163 : 203 215.
10. Cooper MK, Porter JA, Young KE, et al. Teratogen-mediated inhibition of target tissue response to Shh signaling. Science. 1998 280 : 1603 1607.
11. Taipale J, Chen JK, Cooper MK, et al. Effects of oncogenic mutations in Smoothened and Patched can be reversed by cyclopamine. Nature. 2000 406 : 1005 1009.
12. Berman DM, Karhadkar SS, Hallahan AR, et al. Medulloblastoma growth inhibition by hedgehog pathway blockade. Science. 2002 297 : 1559 1561.
13. Incardona JP, Gaffield W, Kapur RP, et al. The teratogenic Veratrum alkaloid cyclopamine inhibits sonic hedgehog signal transduction. Development. 1998 125 : 3553 3562.
14. Koleva M, Kappler R, Vogler M, et al. Pleiotropic effects of sonic hedgehog on muscle satellite cells. Cell Mol Life Sci. 2005 62 : 1863 1870.
15. McMahon CD, Popovic L, Oldham JM, et al. Myostatin-deficient mice lose more skeletal muscle mass than wild-type controls during hindlimb suspension. Am J Physiol Endocrinol Metab. 2003 285 : E82 7.
16. Pola R, Aprahamian TR, Bosch-Marce M, et al. Age-dependent VEGF expression and intraneural neovascularization during regeneration of peripheral nerves. Neurobiol Aging. 2004 25 : 1361 1368.
17. Desgranges P, Barbaud C, Caruelle JP, et al. A substituted dextran enhances muscle fiber survival and regeneration in ischemic and denervated rat EDL muscle. FASEB J. 1999 13 : 761 766
18. Wagatsuma A, Tamaki H, Ogita F. Sequential expression of vascular endothelial growth factor, Flt-1, and KDR/Flk-1 in regenerating mouse skeletal muscle. Physiol Res. 2006 55 : 633 640.
19. Wagatsuma A. Endogenous expression of angiogenesis-related factors in response to muscle injury. Mol Cell Biochem. 2007 298 : 151 159.
20. Brzóska E, Grabowska I, Hoser G, et al. Participation of stem cells from human cord blood in skeletal muscle regeneration of SCID mice. Exp Hematol. 2006 34 : 1262 1270.
21. Florini JR, Ewton DZ, Coolican SA. Growth hormone and the insulin-like growth factor system in myogenesis. Endocr Rev. 1996 17 : 481 517.
22. Seale P, Rudnicki MA. A new look at the origin, function, and "stem-cell" status of muscle satellite cells. Dev Biol. 2000 15 218 : 115 124.
23. Adams GR, Haddad F. The relationships among IGF-1, DNA content, and protein accumulation during skeletal muscle hypertrophy. J Appl Physiol. 1996 81 : 2509 2516.
24. Adams GR, McCue SA. Localized infusion of IGF-I results in skeletal muscle hypertrophy in rats. J Appl Physiol. 1998 84 : 1716 1722.
25. Elia D, Madhala D, Ardon E, et al. Sonic hedgehog promotes proliferation and differentiation of adult muscle cells: Involvement of MAPK/ERK and PI3K/Akt pathways. Biochim Biophys Acta. 2007 1773 : 1438 1446.
26. Asai J, Takenaka H, Kusano KF, et al. Topical sonic hedgehog gene therapy accelerates wound healing in diabetes by enhancing endothelial progenitor cell-mediated microvascular remodeling. Circulation. 2006 113 : 2413 2424.
27. Levy V, Lindon C, Harfe BD, et al. Distinct stem cell populations regenerate the follicle and interfollicular epidermis. Dev Cell. 2005 9 : 855 861.
28. Miyaji T, Nakase T, Iwasaki M, et al. Expression and distribution of transcripts for sonic hedgehog in the early phase of fracture repair. Histochem Cell Biol. 2003 119 : 233 237.
29. Saika S, Muragaki Y, Okada Y, et al. Sonic hedgehog expression and role in healing corneal epithelium. Invest Ophthalmol Vis Sci. 2004 45 : 2577 2585.
30. Akazawa C, Tsuzuki H, Nakamura Y, et al. The upregulated expression of sonic hedgehog in motor neurons after rat facial nerve axotomy. J Neurosci. 2004 24 : 7923 7930.
31. Bambakidis NC, Wang RZ, Franic L, et al. Sonic hedgehog-induced neural precursor proliferation after adult rodent spinal cord injury. J Neurosurg. 2003 99 : 70 5.
32. Bunn JR, Canning J, Burke G, et al. Production of consistent crush lesions in murine quadriceps muscle-a biomechanical, histomorphological and immunohistochemical study. J Orthop Res. 2004 22 : 1336 1344.
33. Ochoa O, Sun D, Reyes-Reyna SM, et al. Delayed angiogenesis and VEGF production in CCR2 -/- mice during impaired skeletal muscle regeneration. Am J Physiol Regul Integr Comp Physiol. 2007 293 : R651 61.
34. Smythe GM, Lai MC, Grounds MD, et al. Adeno-associated virus-mediated vascular endothelial growth factor gene therapy in skeletal muscle before transplantation promotes revascularization of regenerating muscle. Tissue Eng. 2002 8 : 879 891.
35. Germani A, Di Carlo A, Mangoni A, et al. Vascular endothelial growth factor modulates skeletal myoblast function. Am. J. Pathol. 2003 163 : 1417 1428.
36. Messina S, Mazzeo A, Bitto A, et al. VEGF overexpression via adeno-associated virus gene transfer promotes skeletal muscle regeneration and enhances muscle function in mdx mice. FASEB J. 2007 21 : 3737 3746.
37. Odemis V, Lamp E, Pezeshki G, et al. Mice deficient in the chemokine receptor CXCR4 exhibit impaired limb innervation and myogenesis. Mol Cell Neurosci. 2005 30 : 494 405.
38. De Paepe B, Creus KK, De Bleecker JL. Chemokines in idiopathic inflammatory myopathies. Front Biosci. 2008 13 : 2548 2577.
39. Ratajczak MZ, Majka M, Kucia M, et al. 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 2003 21 : 363 371.
40. 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 : 255 267.
41. Cossu G, Mavilio F. Myogenic stem cells for the therapy of primary myopathies: wishful thinking or therapeutic perspective J Clin Invest. 2000 105 : 1669 1674.
42. Elia D, Madhala D, Ardon E, et al. Sonic hedgehog promotes proliferation and differentiation of adult muscle cells: involvement of MAPK/ERK and PI3K/Akt pathways. Biochim Biophys Acta. 2007 1773 : 1438 1446.
43. Borycki A, Brown AM, Emerson CP Jr. Shh and Wnt signaling pathways converge to control Gli gene activation in avian somites. Development. 2000 127 : 2075 2087.
44. Gustafsson MK, Pan H, Pinney DF, et al. Myf5 is a direct target of long-range Shh signaling and Gli regulation for muscle specification. Genes Dev. 2002 16 : 114 126.
45. McDermott A, Gustafsson M, Elsam T, et al. Gli2 and Gli3 have redundant and context-dependent function in skeletal muscle formation. Development. 2005 132 : 345 357.
46. Holowacz T, Zeng L, Lassar AB. Asymmetric localization of numb in the chick somite and the influence of myogenic signals. Dev Dyn. 2006 235 : 633 645.
47. Borello U, Berarducci B, Murphy P, et al. The Wnt/beta-catenin pathway regulates Gli-mediated Myf5 expression during somitogenesis. Development. 2006 133 : 3723 3732.
48. Takahashi A, Kureishi Y, Yang J, et al. Myogenic Akt signaling regulates blood vessel recruitment during myofiber growth. Mol Cell Biol. 2002 22 : 4803 4814.
49. Gerber HP, McMurtrey A, Kowalski J, et al. Vascular endothelial growth factor regulates endothelial cell survival through the phosphatidylinositol 3′-kinase/Akt signal transduction pathway. Requirement for Flk-1/KDR activation. J Biol Chem. 1998 273 : 30336 30343.
50. Fujio Y, Guo K, Mano T, et al. Cell cycle withdrawal promotes myogenic induction of Akt, a positive modulator of myocyte survival. Mol Cell Biol. 1999 19 : 5073 5082.
51. Alessi DR, Andjelkovic M, Caudwell B, et al. Mechanism of activation of protein kinase B by insulin and IGF-1. EMBO J. 1996 15 : 6541 6551.
52. Bodine SC, Stitt TN, Gonzalez M, et al. Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy in vivo. Nat Cell Biol. 2001 3 : 1014 1019.
53. Rommel C, Bodine SC, Clarke BA, et al. Mediation of IGF-1-induced skeletal myotube hypertrophy by PI(3)K/Akt/mTOR and PI(3)K/Akt/GSK3 pathways. Nat Cell Biol. 2001 3 : 1009 1013.
54. Mourkioti F, Rosenthal N. IGF-1, inflammation and stem cells: interactions during muscle regeneration. Trends Immunol. 2005 26 : 535 542.