Temporal response of positive and negative regulators in response to acute and chronic exercise training in mice

Journal of Physiology

Volumn 591, Issue 20, 2013, Pages 5157-5169

  Olenich, Sara A ^a   Gutierrez Reed, Navarre ^b   Audet, Gerald N ^a   Olfert, Mark I ^a  

^a WEST VIRGINIA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENDOSTATIN; GELATINASE A; MITOGENIC AGENT; NUCLEOLIN; THROMBOSPONDIN 1; VASCULOTROPIN A;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EXERCISE INTENSITY; EXERCISE PHYSIOLOGY; MALE; MOUSE; MUSCLE CAPILLARY; MUSCLE DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; REGULATORY MECHANISM; RUNNING;

ANIMALS; ENDOSTATINS; MALE; MATRIX METALLOPROTEINASE 2; MICE; MICE, INBRED C57BL; MUSCLE, SKELETAL; NEOVASCULARIZATION, PHYSIOLOGIC; PHOSPHOPROTEINS; PHYSICAL EXERTION; RNA-BINDING PROTEINS; THROMBOSPONDIN 1; TIME FACTORS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84885426010     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2013.254979     Document Type: Article

References (56)

1. Audet GN, Fulks D, Stricker JC & Olfert IM (2013). Chronic delivery of a thrombospondin-1 mimetic decreases skeletal muscle capillarity in mice. PLoS One 8, e55953.
2. Bloor CM (2005). Angiogenesis during exercise and training. Angiogenesis 8, 263-271.
3. Bornstein P (1992). Thrombospondins: structure and regulation of expression. FASEB J 6, 3290-3299. [Published erratum appears in FASEB J (1993) 1, 237.
4. Breen EC, Johnson EC, Wagner H, Tseng HM, Sung LA & Wagner PD (1996). Angiogenic growth factor mRNA responses in muscle to a single bout of exercise. J Appl Physiol 81, 355-361.
5. Brixius K, Schoenberger S, Ladage D, Knigge H, Falkowski G, Hellmich M, Graf C, Latsch J, Montie GL, Prede GL & Bloch W (2008). Long-term endurance exercise decreases antiangiogenic endostatin signalling in overweight men aged 50-60 years. Br J Sports Med 42, 126-129.
6. Brown MD & Hudlicka O (2003). Modulation of physiological angiogenesis in skeletal muscle by mechanical forces: involvement of VEGF and metalloproteinases. Angiogenesis 6, 1-14.
7. Carmeli E, Haimovitz T & Nemcovsky EC (2007). Cathepsin D and MMP-9 activity increase following a high intensity exercise in hind limb muscles of young rats. J Basic Clin Physiol Pharmacol 18, 79-86.
8. Carmeli E, Moas M, Lennon S & Powers SK (2005). High intensity exercise increases expression of matrix metalloproteinases in fast skeletal muscle fibres. Exp Physiol 90, 613-619.
9. Christian S, Pilch J, Akerman ME, Porkka K, Laakkonen P & Ruoslahti E (2003). Nucleolin expressed at the cell surface is a marker of endothelial cells in angiogenic blood vessels. J Cell Biol 163, 871-878.
10. Drummond GB (2009). Reporting ethical matters in The Journal of Physiology: standards and advice. J Physiol 587, 713-719.
11. Egginton S (2009). Invited review: activity-induced angiogenesis. Pflugers Arch 457, 963-977.
12. Fahling M, Steege A, Perlewitz A, Nafz B, Mrowka R, Persson PB & Thiele BJ (2005). Role of nucleolin in posttranscriptional control of MMP-9 expression. Biochim Biophys Acta 1731, 32-40.
13. Gavin TP, Robinson CB, Yeager RC, England JA, Nifong LW & Hickner RC (2004). Angiogenic growth factor response to acute systemic exercise in human skeletal muscle. J Appl Physiol 96, 19-24.
14. Gu J-W, Gadonski G, Wang J, Makey I & Adair T (2004). Exercise increases endostatin in circulation of healthy volunteers. BMC Physiol 4, 2.
15. Gustafsson T, Ameln H, Fischer H, Sundberg CJ, Timmons JA & Jansson E (2005). VEGF-A splice variants and related receptor expression in human skeletal muscle following submaximal exercise. J Appl Physiol 98, 2137-2146.
16. Gustafsson T, Puntschart A, Kaijser L, Jansson E & Sundberg CJ (1999). Exercise-induced expression of angiogenesis-related transcription and growth factors in human skeletal muscle. Am J Physiol Heart Circ Physiol 276, H679-H685.
17. Gustafsson T & Sundberg CJ (2000). Expression of angiogenic growth factors in human skeletal muscle in response to a singular bout of exercise. Am J Physiol Heart Circ Physiol 279, H3144-H3145.
18. Haas TL, Milkiewicz M, Davis SJ, Zhou AL, Egginton S, Brown MD, Madri JA & Hudlicka O (2000). Matrix metalloproteinase activity is required for activity-induced angiogenesis in rat skeletal muscle. Am J Physiol Heart Circ Physiol 279, H1540-H1547.
19. Hoier B, Nordsborg N, Andersen S, Jensen L, Nybo L, Bangsbo J & Hellsten Y (2012). Pro- and anti-angiogenic factors in human skeletal muscle in response to acute exercise and training. J Physiol 590, 595-606.
20. Hoier B, Passos M, Bangsbo J & Hellsten Y (2013). Intense intermittent exercise provides weak stimulus for vascular endothelial growth factor secretion and capillary growth in skeletal muscle. Exp Physiol 98, 585-597.
21. Howlett RA, Kirkton SD, Gonzalez NC, Wagner HE, Britton SL, Koch LG & Wagner PD (2009). Peripheral oxygen transport and utilization in rats following continued selective breeding for endurance running capacity. J Appl Physiol 106, 1819-1825.
22. Høydal MA, Wisløff U, Kemi OJ & Ellingsen Ø (2007). Running speed and maximal oxygen uptake in rats and mice: practical implications for exercise training. Eur J Cardiovasc Prev Rehabil 14, 753-760.
23. Huang Y, Shi H, Zhou H, Song X, Yuan S & Luo Y (2006). The angiogenic function of nucleolin is mediated by vascular endothelial growth factor and nonmuscle myosin. Blood 107, 3564-3571.
24. Hudlicka O, Brown M & Egginton S (1992). Angiogenesis in skeletal and cardiac muscle. Physiol Rev 72, 369-417.
25. Levy AP (1999). A cellular paradigm for the failure to increase vascular endothelial growth factor in chronically hypoxic states. Coron Artery Dis 10, 427-430.
26. Lloyd PG, Prior BM, Li H, Yang HT & Terjung RL (2005). 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.
27. Lloyd PG, Prior BM, Yang HT & Terjung RL (2003). Angiogenic growth factor expression in rat skeletal muscle in response to exercise training. Am J Physiol Heart Circ Physiol 284, H1668-H1678.
28. Malek MH & Olfert IM (2009). Global deletion of thrombospondin-1 increases cardiac and skeletal muscle capillarity and exercise capacity. Exp Physiol 94, 749-760.
29. Malek MH, Olfert IM & Esposito F (2010). Detraining losses of skeletal muscle capillarization are associated with vascular endothelial growth factor protein expression in rats. Exp Physiol 95, 359-368.
30. Mathieu-Costello O & Hepple RT (2002). Muscle structural capacity for oxygen flux from capillary to fiber mitochondria. Exerc Sport Sci Rev 30, 80-84.
31. Mrazkova O, Grim M & Carlson BM (1986). Enzymatic heterogeneity of the capillary bed of rat skeletal muscles. Am J Anat 177, 141-148.
32. Olfert IM & Birot O (2011). Importance of anti-angiogenic factors in the regulation of skeletal muscle angiogenesis. Microcirculation 18, 316-330.
33. Olfert IM, Breen EC, Gavin TP & Wagner PD (2006). Temporal thrombospondin-1 mRNA response in skeletal msucle exposed to acute and chronic exercise. Growth Factors 24, 253-259.
34. Olfert IM, Breen EC, Mathieu-Costello O & Wagner PD (2001a). Chronic hypoxia attenuates resting and exercise-induced VEGF, flt-1, and flk-1, mRNA levels in skeletal muscle. J Appl Physiol 90, 1532-1538.
35. Olfert IM, Breen EC, Mathieu-Costello O & Wagner PD (2001b). Skeletal muscle capillarity and angiogenic mRNA levels after exercise training in normoxia and chronic hypoxia. J Appl Physiol 91, 1176-1184.
36. Olfert IM, Howlett RA, Tang K, Dalton ND, Gu Y, Peterson KL, Wagner PD & Breen EC (2009). Muscle-specific VEGF deficiency greatly reduces exercise endurance in mice. J Physiol 578, 1755-1767.
37. Olfert IM, Howlett RA, Wagner PD & Breen EC (2010). Myocyte vascular endothelial growth factor is required for exercise-induced skeletal muscle angiogenesis. Am J Physiol Regul Integr Comp Physiol 299, R1059-R1067.
38. Prior BM, Yang HT & Terjung RL (2004). What makes vessels grow with exercise training J Appl Physiol 97, 1119-1128.
39. Richardson RS, Wagner H, Mudaliar SRD, Henry R, Noyszewski EA & Wagner PD (1999). Human VEGF gene expression in skeletal muscle: effect of acute normoxic and hypoxic exercise. Am J Physiol Heart Circ Physiol 277, H2247-H2252.
40. Richardson RS, Wagner H, Mudaliar SRD, Saucedo E, Henry R & Wagner PD (2000). Exercise adaptation attenuates VEGF gene expression in human skeletal muscle. Am J Physiol Heart Circ Physiol 279, H772-H778.
41. Roudier E, Gineste C, Wazna A, Dehghan K, Desplanches D & Birot O (2010). Angio-adaptation in unloaded skeletal muscle: new insights into an early and muscle type-specific dynamic process. J Physiol 588, 4579-4591.
42. Rullman E, Norrbom J, Stromberg A, Wagsater D, Rundqvist H, Haas T & Gustafsson T (2009). Endurance exercise activates matrix metalloproteinases in human skeletal muscle. J Appl Physiol 106, 804-812.
43. Rullman E, Olsson K, Wagsater D & Gustafsson T (2013). Circulating MMP-9 during exercise in humans. Eur J Appl Physiol 113, 1249-1255.
44. Rullman E, Rundqvist H, Wagsater D, Fischer H, Eriksson P, Sundberg CJ, Jansson E & Gustafsson T (2007). A single bout of exercise activates matrix metalloproteinase in human skeletal muscle. J Appl Physiol 102, 2346-2351.
45. Ryan NA, Zwetsloot KA, Westerkamp LM, Hickner RC, Pofahl WE & Gavin TP (2006). Lower skeletal muscle capillarization and VEGF expression in aged vs. young men. J Appl Physiol 100, 178-185.
46. Shi H, Huang Y, Zhou H, Song X, Yuan S, Fu Y & Luo Y (2007). Nucleolin is a receptor that mediates antiangiogenic and antitumor activity of endostatin. Blood 110, 2899-2906.
47. Snyder GK (1987). Muscle capillarity in chicks following hypoxia. Comp Biochem Physiol A Comp Physiol 87, 819-822.
48. Snyder GK, Farrelly C & Coelho JR (1992). Adaptations in skeletal muscle capillarity following changes in oxygen supply and changes in oxygen demands. Eur J Appl Physiol 65, 158-163.
49. Song N, Ding Y, Zhuo W, He T, Fu Z, Chen Y, Song X, Fu Y & Luo Y (2012). The nuclear translocation of endostatin is mediated by its receptor nucleolin in endothelial cells. Angiogenesis 15, 697-711.
50. Srivastava M & Pollard HB (1999). Molecular dissection of nucleolin's role in growth and cell proliferation: new insights. FASEB J 13, 1911-1922.
51. Suhr F, Brixius K, de Marees M, Bolck B, Kleinoder H, Achtzehn S, Bloch W & Mester J (2007). Effects of short-term vibration and hypoxia during high-intensity cycling exercise on circulating levels of angiogenic regulators in humans. J Appl Physiol 103, 474-483.
52. Suhr F, Rosenwick C, Vassiliadis A, Bloch W & Brixius K (2010). Regulation of extracellular matrix compounds involved in angiogenic processes in short- and long-track elite runners. Scand J Med Sci Sports 20, 441-448.
53. Tang K, Breen EC & Wagner PD (2002). Hu protein R-mediated posttranscriptional regulation of VEGF expression in rat gastrocnemius muscle. Am J Physiol Heart Circ Physiol 283, H1497-H1504.
54. Wagner PD (1996). Determinants of maximal oxygen transport and utilization. Annu Rev Physiol 58, 21-50.
55. Waters RE, Rotevatn S, Li P, Annex BH & Yan Z (2004). Voluntary running induces fiber type-specific angiogenesis in mouse skeletal muscle. Am J Physiol Cell Physiol 287, C1342-C1348.
56. Williams JL, Cartland D, Rudge JS & Egginton S (2006). VEGF trap abolishes shear stress- and overload-dependent angiogenesis in skeletal muscle. Microcirculation 13, 499-509.