VEGF-A splice variants and related receptor expression in human skeletal muscle following submaximal exercise

Journal of Applied Physiology

Volumn 98, Issue 6, 2005, Pages 2137-2146

  Gustafsson, T ^a   Ameln, H ^a   Fischer, H ^a   Sundberg, C J ^a   Timmons, J A ^a,b   Jansson, E ^a  

^a KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^b KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Angiogenesis; Ischemia; Vascular endothelial growth factor

Indexed keywords

MESSENGER RNA; NEUROPILIN 1; VASCULOTROPIN A; VASCULOTROPIN RECEPTOR; VASCULOTROPIN RECEPTOR 1; VASCULOTROPIN RECEPTOR 2;

ADULT; ANGIOGENESIS; ARTICLE; BLOOD FLOW; CONTROLLED STUDY; EXERCISE; GENE EXPRESSION; HUMAN; HUMAN EXPERIMENT; ISCHEMIA; LEG BLOOD FLOW; MUSCLE BIOPSY; NORMAL HUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; SKELETAL MUSCLE; TRANSLATION REGULATION;

ADAPTATION, PHYSIOLOGICAL; ADOLESCENT; ADULT; BLOOD FLOW VELOCITY; DNA, RECOMBINANT; EXERCISE TEST; EXERTION; GENE EXPRESSION REGULATION; HUMANS; MALE; MUSCLE CONTRACTION; MUSCLE, SKELETAL; RECEPTORS, VASCULAR ENDOTHELIAL GROWTH FACTOR; REPERFUSION INJURY; VARIATION (GENETICS); VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 19444386664     PISSN: 87507587     EISSN: None     Source Type: Journal    
DOI: 10.1152/japplphysiol.01402.2004     Document Type: Article

References (53)

1. Adair TH, Gay WJ, and Montani JP. Growth regulation of the vascular system: evidence for a metabolic hypothesis. Am J Physiol Regul Integr Comp Physiol 259: R393-R404, 1990.
2. Ameln H, Gustafsson T, Sundberg CJ, Poellinger L, Jansson E, Okamoto K, and Makino Y. Physiological activation of hypoxia inducible factor-1 in human skeletal muscle. FASEB J In press.
3. Bates DO, Cui TG, Doughty JM, Winkler M, Sugiono M, Shields JD, Peat D, Gillatt D, and Harper SJ. VEGF165b, an inhibitory splice variant of vascular endothelial growth factor, is down-regulated in renal cell carcinoma. Cancer Res 62: 4123-4131, 2002.
4. Birot OJ, Koulmann N, Peinnequin A, and Bigard XA. Exercise-induced expression of vascular endothelial growth factor mRNA in rat skeletal muscle is dependent on fibre type. J Physiol 552: 213-221, 2003.
5. Breen EC, Johnson EC, Wagner H, Tseng HM, Sung LA, and Wagner PD. Angiogenic growth factor mRNA responses in muscle to a single bout of exercise. J Appl Physiol 81: 355-361, 1996.
6. Carmeliet P, Ng YS, Nuyens D, Theilmeier G, Brusselmans K, Cornelissen I, Ehler E, Kakkar VV, Stalmans I, Mattot V, Perriard JC, Dewerchin M, Flameng W, Nagy A, Lupu F, Moons L, Collen D, D'Amore PA, and Shima DT. Impaired myocardial angiogenesis and ischemic cardiomyopathy in mice lacking the vascular endothelial growth factor isoforms VEGF164 and VEGF188. Nat Med 5: 495-502, 1999.
7. Chomczynski P and Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162: 156-159, 1987.
8. Cui TG, Foster RR, Saleem M, Mathieson PW, Gillatt DA, Bates DO, and Harper SJ. Differentiated human podocytes endogenously express an inhibitory isoform of vascular endothelial growth factor (VEGF165b) mRNA and protein. Am J Physiol Renal Physiol 286: F767-F773, 2004.
9. Eiken O and Bjurstedt H. Dynamic exercise in man as influenced by experimental restriction of blood flow in the working muscles. Acta Physiol Scand 131: 339-345, 1987.
10. Elson DA, Thurston G, Huang LE, Ginzinger DG, McDonald DM, Johnson RS, and Arbeit JM. Induction of hypervascularity without leakage or inflammation in transgenic mice overexpressing hypoxia-inducible factor 1 alpha. Genes Dev 15: 2520-2532, 2001.
11. Essen B and Haggmark T. Lactate concentration in type I and II muscle fibers during muscular contraction in man. Acta Physiol Scand 95: 344-346, 1975.
12. Essen B, Jansson E, Henriksson J, Taylor AW, and Saltin B. Metabolic characteristics of fiber types in human skeletal muscle. Acta Physiol Scand 95: 153-165, 1975.
13. Forsythe JA, Jiang BH, Iyer NV, Agani F, Leung SW, Koos RD, and Semenza GL. Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol Cell Biol 16: 4604-4613, 1996.
14. Gavin TP and Wagner PD. Attenuation of the exercise-induced increase in skeletal muscle Fit-1 mRNA by nitric oxide synthase inhibition. Acta Physiol Scand 175: 201-209, 2002.
15. Gavin TP, Robinson CB, Yeager RC, England JA, Nifong LW, and Hickner RC. Angiogenic growth factor response to acute systemic exercise in human skeletal muscle. J Appl Physiol 96: 19-24, 2004.
16. Gerber HP, Condorelli F, Park J, and Ferrara N. Differential transcriptional regulation of the two vascular endothelial growth factor receptor genes. Fit-1, but not Flk-1/KDR, is up-regulated by hypoxia. J Biol Chem 272: 23659-23667, 1997.
17. Greenhaff PL, Soderlund K, Ren JM, and Hultman E. Energy metabolism in single human muscle fibers during intermittent contraction with occluded circulation. J Physiol 460: 443-453, 1993.
18. Gustafsson T, Knutsson A, Puntschart A, Kaijser L, Nordqvist AC, Sundberg CJ, and Jansson E. Increased expression of vascular endothelial growth factor in human skeletal muscle in response to short-term one-legged exercise training. Pflügers Arch 444: 752-759, 2002.
19. Gustafsson T, Puntschart A, Kaijser L, Jansson E, and Sundberg CJ. Exercise-induced expression of angiogenesis-related transcription and growth factors in human skeletal muscle. Am J Physiol Heart Circ Physiol 276: H679-H685, 1999.
20. Hennequin LF, Stokes ES, Thomas AP, Johnstone C, Ple PA, Ogilvie DJ, Dukes M, Wedge SR, Kendrew J, and Curwen JO. Novel 4-anilinoquinazolines with C-7 basic side chains: design and structure activity relationship of a series of potent, orally active, VEGF receptor tyrosine kinase inhibitors. J Med Chem 45: 1300-1312, 2002.
21. Hiscock N, Fischer CP, Pilegaard H, and Pedersen BK. Vascular endothelial growth factor mRNA expression and arteriovenous balance in response to prolonged, submaximal exercise in humans. Am J Physiol Heart Circ Physiol 285: H1759-H1763, 2003.
22. Höffner L, Nielsen JJ, Langberg H, and Hellsten Y. Exercise but not prostanoids enhance levels of vascular endothelial growth factor and other proliferative agents in human skeletal muscle interstitium. J Physiol 550: 217-225, 2003.
23. Houck KA, Ferrara N, Winer J, Cachianes G, Li B, and Leung DW. The vascular endothelial growth factor family: identification of a fourth molecular species and characterization of alternative splicing of RNA. Mol Endocrinol 5: 1806-1814, 1991.
24. Ishida S, Shinoda K, Kawashima S, Oguchi Y, Okada Y, and Ikeda E. Coexpression of VEGF receptors VEGF-R2 and neuropilin-1 in proliferative diabetic retinopathy. Invest Ophthalmol Vis Sci 41: 1649-1656. 2000.
25. Jensen L, Bangsbo J, and Hellsten Y. Effect of high intensity training on capillarization and presence of angiogenic factors in human skeletal muscle. J Physiol 557: 571-582, 2004.
26. Jensen L, Pilegaard H, Neufer PD, and Hellsten Y. Effect of acute exercise and exercise training on VEGF splice variants in human skeletal muscle. Am J Physiol Regul Integr Comp Physiol 287: R397-R402, 2004.
27. 2 tension. Am J Physiol Cell Physiol 271: C1172-C1180, 1996.
28. Levy NS, Chung S, Furneaux H, and Levy AP. Hypoxic stabilization of vascular endothelial growth factor mRNA by the RNA-binding protein HuR. J Biol Chem 273: 6417-6423, 1998.
29. Lloyd PG, Prior BM, Li H, Yang HT, and Terjung RL. VEGF receptor antagonism blocks arteriogenesis, but only partially inhibits angiogenesis, in skeletal muscle of exercise trained rats. Am J Physiol Heart Circ Physiol 288: H759-H768, 2005.
30. Lloyd PG, Prior BM, Yang HT, and Terjung RL. Angiogenic growth factor expression in rat skeletal muscle in response to exercise training. Am J Physiol Heart Circ Physiol 284: H1668-H1678, 2003.
31. Neufeld G, Cohen T, Gengrinovitch S, and Poltorak Z. Vascular endothelial growth factor (VEGF) and its receptors. FASEB J 13: 9-22, 1999.
32. Ng YS, Rohan R, Sunday ME, Demello DE, and D'Amore PA. Differential expression of VEGF isoforms in mouse during development and in the adult. Dev Dyn 220: 112-121, 2001.
33. Oh H, Takagi H, Otani A, Koyama S, Kemmochi S, Uemura A, and Honda Y. Selective induction of neuropilin-1 by vascular endothelial growth factor (VEGF): a mechanism contributing to VEGF-induced angiogenesis. Proc Natl Acad Sci USA 99: 383-388, 2002.
34. Olfert IM, Breen EC, Mathieu-Costello O, and Wagner PD. Skeletal muscle capillarity and angiogenic mRNA levels after exercise training in normoxia and chronic hypoxia. J Appl Physiol 91: 1176-1184, 2001.
35. Park JE, Keller GA, and Ferrara N. The vascular endothelial growth factor (VEGF) isoforms: differential deposition into the subepithelial extracellular matrix and bioactivity of extracellular matrix-bound VEGF. Mol Biol Cell 4: 1317-1326, 1993.
36. 2 transport. J Clin Invest 96: 1916-1926, 1995.
37. Richardson RS, Wagner H, Mudaliar SR, Henry R, Noyszewski EA, and Wagner PD. Human VEGF gene expression in skeletal muscle: effect of acute normoxic and hypoxic exercise. Am J Physiol Heart Circ Physiol 277: H2247-H2252, 1999.
38. Richardson RS, Wagner H, Mudaliar SR, Saucedo E, Henry R, and Wagner PD. Exercise adaptation attenuates VEGF gene expression in human skeletal muscle. Am J Physiol Heart Circ Physiol 279: H772-H778, 2000.
39. Rissanen TT, Vajanto I, Hiltunen MO, Rutanen J, Kettunen MI, Niemi M, Leppanen P, Turunen MP, Markkanen JE, Arve K, Alhava E, Kauppinen RA, and 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.
40. Saltin B and Gollnick PD. Skeletal muscle adaptability: significance for metabolism and performance. In: Handbook of Physiology. Skeletal Muscle. Bethesda, MD: Am. Physiol. Soc., 1983, sect. 10, chapt. 19, p. 539-554.
41. Shen BQ, Lee DY, Gerber HP, Keyt BA, Ferrara N, and Zioncheck TF. Homologous up-regulation of KDR/Flk-1 receptor expression by vascular endothelial growth factor in vitro. J Biol Chem 273: 29979-29985, 1998.
42. Shibuya M, Nobuyuki L, and Claesson-Welsh L. Structure and function of VEGF receptor-1 and 2. In: Vascular Growth Factors and Angiogenesis, edited by Claesson-Welsh L. Berlin: Springer-Verlag, 1999.
43. Soker S, Takashima S, Miao HQ, Neufeld G, and Klagsbrun M. Neuropilin-1 is expressed by endothelial and tumor cells as an isoform-specific receptor for vascular endothelial growth factor. Cell 9: 735-745, 1998.
44. Stalmans I, Ng YS, Rohan R, Fruttiger M, Bouche A, Yuce A, Fujisawa H, Hermans B, Shani M, Jansen S, Hicklin D, Anderson DJ, Gardiner T, Hammes HP, Moons L, Dewerchin M, Collen D, Carmeliet P, and D'Amore PA. Arteriolar and venular patterning in retinas of mice selectively expressing VEGF isoforms. J Clin Invest 109: 327-336, 2002.
45. Stamm S. Signals and their transduction pathways regulating alternative splicing: a new dimension of the human genome. Hum Mol Genet 11: 2409-2416, 2002.
46. Sundberg CJ. Exercise and training during graded leg ischaemia in healthy man with special reference to effects on skeletal muscle. Acta Physiol Scand 615, Suppl: 1-50, 1994.
47. Tang K, Breen EC, and Wagner PD. Hu protein R-mediated posttranscriptional regulation of VEGF expression in rat gastrocnemius muscle. Am J Physiol Heart Circ Physiol 283: H1497-H1504, 2002.
48. Tang K, Breen EC, Gerber HP, Ferrara NM, and Wagner PD. Capillary regression in vascular endothelial growth factor-deficient skeletal muscle. Physiol Genomics 18: 63-69, 2004.
49. Tang K, Breen EC, Wagner H, Brutsaert TD, Gassmann M, and Wagner PD. HIF and VEGF relationships in response to hypoxia and sciatic nerve stimulation in rat gastrocnemius. Respir Physiol Neurobiol 144: 71-80, 2004.
50. Timmons JA, Constantin-Teodosiu D, Poucher SM, and Greenhaff PL. Acetyl group availability influences phosphocreatine degradation even during intense muscle contraction. J Physiol 561: 851-859, 2004.
51. Veikkola T, Karkkainen M, Claesson-Welsh L, and Alitalo K. Regulation of angiogenesis via vascular endothelial growth factor receptors. Cancer Res 60: 203-212, 2000.
52. Winer J, Jung CK, Shackel I, and Williams PM. Development and validation of real-time quantitative reverse transcriptase-polymerase chain reaction for monitoring gene expression in cardiac myocytes in vitro. Anal Biochem 270: 41-49, 1999.
53. Yang HT, Ogilvie RW, and Terjung RL. Low-intensity training produces muscle adaptations in rats with femoral artery stenosis. J Appl Physiol 71: 1822-1829, 1991.