Satellite cell-mediated angiogenesis in vitro coincides with a functional hypoxia-inducible factor pathway

American Journal of Physiology - Cell Physiology

Volumn 296, Issue 6, 2009, Pages

  Rhoads, R P ^a,b   Johnson, R M ^a   Rathbone, C R ^a   Liu, X ^a   Temm Grove, C ^a   Sheehan, S M ^a   Hoying, J B ^a,b   Allen, R E ^a  

^a UNIVERSITY OF ARIZONA   (United States)

^b UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

Author keywords

Skeletal muscle

Indexed keywords

HYPOXIA INDUCIBLE FACTOR; HYPOXIA INDUCIBLE FACTOR 1ALPHA; VASCULOTROPIN;

ANGIOGENESIS; ANIMAL CELL; ARTICLE; CELL CULTURE; CELL FUNCTION; CONTROLLED STUDY; GENE EXPRESSION; IN VITRO STUDY; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; SATELLITE CELL; SIGNAL TRANSDUCTION;

ADIPOSE TISSUE; ANIMALS; CELL HYPOXIA; CELLS, CULTURED; CULTURE MEDIA, CONDITIONED; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MALE; MICROVESSELS; NEOVASCULARIZATION, PHYSIOLOGIC; PARACRINE COMMUNICATION; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; SATELLITE CELLS, SKELETAL MUSCLE; SIGNAL TRANSDUCTION; TIME FACTORS; TISSUE CULTURE TECHNIQUES; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

RATTUS;

EID: 66749103763     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00391.2008     Document Type: Article

References (40)

1. Allen RE, Sheehan SM, Taylor RG, Kendall TL, Rice GM. Hepatocyte growth factor activates quiescent skeletal muscle satellite cells in vitro. J Cell Physiol 165: 307-312, 1995.
2. Allen RE, Temm-Grove CJ, Sheehan SM, Rice G. Skeletal muscle satellite cell cultures. Methods Cell Biol 52: 155-176, 1998.
3. Anderson JE. A role for nitric oxide in muscle repair: nitric oxide-mediated activation of muscle satellite cells. Mol Biol Cell 11: 1859-1874, 2000. (Pubitemid 30307918)
4. Christov C, Chretien F, Abou-Khalil R, Bassez G, Vallet G, Authier FJ, Bassaglia Y, Shinin V, Tajbakhsh S, Chazaud B, Gherardi RK. Muscle satellite cells and endothelial cells: close neighbors and privileged partners. Mol Biol Cell 18: 1397-1409, 2007. (Pubitemid 46626634)
5. Ciafre SA, Niola F, Giorda E, Farace MG, Caporossi D. CoCl(2)-simulated hypoxia in skeletal muscle cell lines: role of free radicals in gene up-regulation and induction of apoptosis. Free Radic Res 41: 391-401, 2007. (Pubitemid 46470937)
6. Dehne N, Kerkweg U, Otto T, Fandrey J. The HIF-1 response to simulated ischemia in mouse skeletal muscle cells neither enhances glycolysis nor prevents myotube cell death. Am J Physiol Regul Integr Comp Physiol 293: R1693-R1701, 2007. (Pubitemid 47535788)
7. Dery MA, Michaud MD, Richard DE. Hypoxia-inducible factor 1: regulation by hypoxic and non-hypoxic activators. Int J Biochem Cell Biol 37: 535-540, 2005. (Pubitemid 40022930)
8. Dimmeler S, Dernbach E, Zeiher AM. Phosphorylation of the endothelial nitric oxide synthase at ser-1177 is required for VEGF-induced endothelial cell migration. FEBS Lett 477: 258-262, 2000. (Pubitemid 30450177)
9. Distler JH, Hirth A, Kurowska-Stolarska M, Gay RE, Gay S, Distler O. Angiogenic and angiostatic factors in the molecular control of angiogenesis. Q J Nucl Med 47: 149-161, 2003. (Pubitemid 37279152)
10. Feldser D, Agani F, Iyer NV, Pak B, Ferreira G, Semenza GL. Reciprocal positive regulation of hypoxia-inducible factor 1alpha and insulin-like growth factor 2. Cancer Res 59: 3915-3918, 1999. (Pubitemid 29393552)
11. Gerber HP, McMurtrey A, Kowalski J, Yan M, Keyt BA, Dixit V, Ferrara N. 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 273: 30336-30343, 1998. (Pubitemid 28545503)
12. Germani A, Di Carlo A, Mangoni A, Straino S, Giacinti C, Turrini P, Biglioli P, Capogrossi MC. Vascular endothelial growth factor modulates skeletal myoblast function. Am J Pathol 163: 1417-1428, 2003. (Pubitemid 37175089)
13. Hansen-Smith FM, Carlson BM. Cellular responses to free grafting of the extensor digitorum longus muscle of the rat. J Neurol Sci 41: 149-173, 1979. (Pubitemid 9125191)
14. Hansen-Smith FM, Carlson BM, Irwin KL. Revascularization of the freely grafted extensor digitorum longus muscle in the rat. Am J Anat 158: 65-82, 1980. (Pubitemid 10092900)
15. Hoying JB, Boswell CA, Williams SK. Angiogenic potential of microvessel fragments established in three-dimensional collagen gels. In Vitro Cell Dev Biol Anim 32: 409-419, 1996. (Pubitemid 26269495)
16. Kastner S, Elias MC, Rivera AJ, Yablonka-Reuveni Z. Gene expression patterns of the fibroblast growth factors and their receptors during myogenesis of rat satellite cells. J Histochem Cytochem 48: 1079-1096, 2000. (Pubitemid 30640193)
17. Ke Q, Costa M. Hypoxia-inducible factor-1 (HIF-1). Mol Pharmacol 70: 1469-1480, 2006. (Pubitemid 44776406)
18. Kubis HP, Hanke N, Scheibe RJ, Gros G. Accumulation and nuclear import of HIF1 alpha during high and low oxygen concentration in skeletal muscle cells in primary culture. Biochim Biophys Acta 1745: 187-195, 2005. (Pubitemid 41207891)
19. Markley JM, Faulkner JA, Carlson BM. Regeneration of skeletal muscle after grafting in monkeys. Plast Reconstr Surg 62: 415-422, 1978. (Pubitemid 9047279)
20. Mauro A. Satellite cell of skeletal muscle fibers. J Biophys Biochem Cytol 9: 493-495, 1961.
21. Phillips GD, Knighton DR. Angiogenic activity in damaged skeletal muscle. Proc Soc Exp Biol Med 193: 197-202, 1990.
22. Presta M, Dell'Era P, Mitola S, Moroni E, Ronca R, Rusnati M. Fibroblast growth factor/fibroblast growth factor receptor system in angiogenesis. Cytokine Growth Factor Rev 16: 159-178, 2005. (Pubitemid 40616114)
23. Rissanen TT, Vajanto I, Hiltunen MO, Rutanen J, Kettunen MI, Niemi M, Leppanen P, Turunen MP, Markkanen JE, Arve K, Alhava E, Kauppinen RA, Yla-Herttuala S. 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 160: 1393-1403, 2002. (Pubitemid 34411643)
24. Sandau KB, Fandrey J, Brune B. Accumulation of HIF-1alpha under the influence of nitric oxide. Blood 97: 1009-1015, 2001. (Pubitemid 32154286)
25. Schultz E, Gibson MC, Champion T. Satellite cells are mitotically quiescent in mature mouse muscle: an EM and radioautographic study. J Exp Zool 206: 451-456, 1978.
26. 2 homeostasis by hypoxiainducible factor 1. Annu Rev Cell Dev Biol 15: 551-578, 1999.
27. Senger DR, Galli SJ, Dvorak AM, Perruzzi CA, Harvey VS, Dvorak HF. Tumor cells secrete a vascular permeability factor that promotes accumulation of ascites fluid. Science 219: 983-985, 1983.
28. Shepherd BR, Chen HY, Smith CM, Gruionu G, Williams SK, Hoying JB. Rapid perfusion and network remodeling in a microvascular construct after implantation. Arterioscler Thromb Vasc Biol 24: 898-904, 2004. (Pubitemid 38620869)
29. Shi YH, Wang YX, Bingle L, Gong LH, Heng WJ, Li Y, Fang WG. In vitro study of HIF-1 activation and VEGF release by bFGF in the T47D breast cancer cell line under normoxic conditions: involvement of PI-3K/Akt and MEK1/ERK pathways. J Pathol 205: 530-536, 2005. (Pubitemid 40361343)
30. Stroka DM, Burkhardt T, Desbaillets I, Wenger RH, Neil DA, Bauer C, Gassmann M, Candinas D. HIF-1 is expressed in normoxic tissue and displays an organ-specific regulation under systemic hypoxia. FASEB J 15: 2445-2453, 2001. (Pubitemid 33063172)
31. Tacchini L, De Ponti C, Matteucci E, Follis R, Desiderio MA. Hepatocyte growth factor-activated NF-kappaB regulates HIF-1 activity and ODC expression, implicated in survival, differently in different carcinoma cell lines. Carcinogenesis 25: 2089-2100, 2004. (Pubitemid 39534845)
32. Tacchini L, Matteucci E, De PC, Desiderio MA. Hepatocyte growth factor signaling regulates transactivation of genes belonging to the plasminogen activation system via hypoxia inducible factor-1. Exp Cell Res 290: 391-401, 2003. (Pubitemid 37272181)
33. Tatsumi R, Anderson JE, Nevoret CJ, Halevy O, Allen RE. HGF/SF is present in normal adult skeletal muscle and is capable of activating satellite cells. Dev Biol 194: 114-128, 1998. (Pubitemid 28115263)
34. Tatsumi R, Liu X, Pulido A, Morales M, Sakata T, Dial S, Hattori A, Ikeuchi Y, Allen RE. Satellite cell activation in stretched skeletal muscle and the role of nitric oxide and hepatocyte growth factor. Am J Physiol Cell Physiol 290: C1487-C1494, 2006. (Pubitemid 43830788)
35. Tian H, McKnight SL, Russell DW. Endothelial PAS domain protein 1 (EPAS1), a transcription factor selectively expressed in endothelial cells. Genes Dev 11: 72-82, 1997. (Pubitemid 27043825)
36. Tuomisto TT, Rissanen TT, Vajanto I, Korkeela A, Rutanen J, Yla-Herttuala S. HIF-VEGF-VEGFR-2, TNF-alpha and IGF pathways are upregulated in critical human skeletal muscle ischemia as studied with DNA array. Atherosclerosis 174: 111-120, 2004. (Pubitemid 38595448)
37. Van Belle E, Witzenbichler B, Chen D, Silver M, Chang L, Schwall R, Isner JM. Potentiated angiogenic effect of scatter factor/hepatocyte growth factor via induction of vascular endothelial growth factor: the case for paracrine amplification of angiogenesis. Circulation 97: 381-390, 1998. (Pubitemid 28074339)
38. Vartanian KB, Chen HY, Kennedy J, Beck SK, Ryaby JT, Wang H, Hoying JB. The non-proteolytically active thrombin peptide TP508 stimulates angiogenic sprouting. J Cell Physiol 206: 175-180, 2006. (Pubitemid 41740729)
39. Wagers AJ, Conboy IM. Cellular and molecular signatures of muscle regeneration: current concepts and controversies in adult myogenesis. Cell 122: 659-667, 2005. (Pubitemid 41242632)
40. Zelzer E, Levy Y, Kahana C, Shilo BZ, Rubinstein M, Cohen B. Insulin induces transcription of target genes through the hypoxia-inducible factor HIF-1alpha/ARNT. EMBO J 17: 5085-5094, 1998. (Pubitemid 28408474)