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Angiogenic growth factor mRNA responses in muscle to a single bout of exercise
Abstract
A major adaptation to exercise is new capillary formation in skeletal muscle. On the basis of angiogenesis in tumors and during development, several angiogenic growth factors may be involved, including vascular endothelial growth factor (VEGF), basic fibroblast growth factor (bFGF), and transforming growth factor-beta 1 (TGF-beta 1). In 9-wk-old female Wistar rats, mRNA expression for these three growth factors in gastrocnemius muscle was examined by quantitative Northern analysis after a single 1-h run at 15 or 20 m/min at 10 degrees incline in room air. A third group ran at 15 m/min in 12% O2, and resting control groups were included at inspired O2 fractions of 0.21 and 0.12. Exercise significantly increased mRNA levels two- to fourfold, which was evident over the first 4 h postexercise; by 8 and 24 h, mRNA levels returned to baseline. For all three factors, mRNA levels were significantly higher after exercise at 20 than at 15 m/min. Hypoxia at rest doubled VEGF and TGF-beta 1 message but had no effect on bFGF. Hypoxic exercise further raised VEGF mRNA levels but had no effect on the other factors. We suggest that VEGF, bFGF, and TGF-beta 1 may be involved in the angiogenic response to exercise and that reduced intracellular PO2 (as occurs during normoxic exercise) may be part of the stimulus to such growth factor production.
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“This paper demonstrated that a single bout of exercise can increase VEGF1 and TGFβ1 expression in muscle to promote the angiogenic response to exercise.”
From Exerkines in health, resilience and disease (2022) · cites this paper as [198]
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“In contrast to VEGF, in which peak gene expression occurs rapidly (within 0–2 h) in response to exercise (5), the peak VEGF receptor gene response to exercise may not occur until several hours after exercise (16).”
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Tang, K., Breen, E. C., Wagner, H. E., Brutsaert, T. D., Gassmann, M., & Wagner, P. D. (2004) · Respiratory Physiology & Neurobiology · doi:10.1016/j.resp.2004.04.009 · Cited by 71
Self-citationMuscle Adaptation to Altitude: Tissue Capillarity and Capacity for Aerobic Metabolism
Mathieu-Costello, O. A. (2001) · High Altitude Medicine & Biology · doi:10.1089/15270290152608598 · Cited by 67
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BackgroundResultSelf-citationRoles of Vascular Endothelial Growth Factor in Amyotrophic Lateral Sclerosis
Pronto‐Laborinho, A. C., Pinto, S., & de Carvalho, M. A. (2014) · BioMed Research International · doi:10.1155/2014/947513 · Cited by 55
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Tanner, C. B., Madsen, S. R., Hallowell, D. M., Goring, D. M. J., Moore, T. M., Hardman, S. E., Heninger, M. R., Atwood, D. R., & Thomson, D. M. (2013) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00227.2013 · Cited by 47
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“The increase in bFGF mRNA was observed immediately after electro-stimulation of the rat muscle cells which is a similar time course to that previously reported for rat skeletal muscle showing an increase in 0 h after 1 h of treadmill running [50].”
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Emmons, R. S., Niemiro, G. M., & Lisio, M. D. (2016) · Stem Cells International · doi:10.1155/2016/7131359 · Cited by 47
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BackgroundResultInfluentialSelf-citationSystemic vs. local cytokine and leukocyte responses to unilateral wrist flexion exercise
Nemet, D., Hong, S., Mills, P. J., Ziegler, M. G., HILL, M., & Cooper, D. M. (2002) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00035.2002 · Cited by 47
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Self-citationForkhead BoxO transcription factors restrain exercise‐induced angiogenesis
Slopack, D., Roudier, E. A., Liu, S. T. K., Nwadozi, E., Birot, O., & Haas, T. L. (2014) · The Journal of Physiology · doi:10.1113/jphysiol.2014.275867 · Cited by 48
“2007) and increases in VEGFA mRNA within skeletal muscle, which also remain elevated after repeated exercise bouts (Breen et al. 1996; Gustafsson et al. 1999, 2007; Richardson et al. 1999, 2000; Birot et al. 2003).”
BackgroundEffect of Resistance Training on Extracellular Matrix Adaptations in Skeletal Muscle of Older Rats
Guzzoni, V., Ribeiro, M. B. T., Lopes, G. N., Marqueti, R. D. C., de Andrade, R. V., Selistre-de-Araújo, H. S., & Durigan, J. L. Q. (2018) · Frontiers in Physiology · doi:10.3389/fphys.2018.00374 · Cited by 46
“Our findings are supported by studies that observed increases of TGFβ synthesis in different cell types (Breen et al., 1996; Cillo et al., 2000; Skutek et al., 2001), which could indicate the release of TGFβ from tissues mechanically activated during exercise training (Kjær, 2004).”
ResultAltitude, Exercise, and Skeletal Muscle Angio-Adaptive Responses to Hypoxia: A Complex Story
Lemieux, P., & Birot, O. (2021) · Frontiers in Physiology · doi:10.3389/fphys.2021.735557 · Cited by 57
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Rossiter, H. B., Howlett, R. A., Holcombe, H. H., Entin, P. L., Wagner, H. E., & Wagner, P. D. (2005) · The Journal of Physiology · doi:10.1113/jphysiol.2004.080663 · Cited by 45
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InfluentialSelf-citationPlacenta growth factor is not required for exercise-induced angiogenesis
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“Previous studies have shown elevated VEGF mRNA levels following a single exercise work bout in rodent models (Breen et al. 1996; Gavin & Wagner, 2001; Olfert et al. 2001).”
BackgroundMuscle-targeted deletion of VEGF and exercise capacity in mice
Wagner, P. D., Olfert, I. M., Tang, K., & Breen, E. C. (2005) · Respiratory Physiology & Neurobiology · doi:10.1016/j.resp.2005.09.007 · Cited by 40
Self-citationHypoxia training for sea-level performance
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“2E), which are known to have potential functional roles in endurance exercise-induced mitochondrial biogenesis/fiber-type switching (3, 5, 19, 36) and angiogenesis (9, 49), respectively.”
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BackgroundPhysiological Adaptations to Hypoxic vs. Normoxic Training during Intermittent Living High
Smet, S. D., van Herpt, P., D’Hulst, G., Thienen, R. V., Leemputte, M. V., & Hespel, P. (2017) · Frontiers in Physiology · doi:10.3389/fphys.2017.00347 · Cited by 35
“Hypoxic training has previously been postulated to stimulate capillary growth by increased nitric oxide production in conjunction with increased vasodilation and endothelial shear stress (Hudlicka and Brown, 2009; Casey and Joyner, 2012) as well as by elevated HIF-1-induced VEGF gene expression (Breen et al., 1996; Ta…”
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“A single acute bout of exercise increased the expression of VEGF mRNA [32], whereas chronic exercise training diminished its expression after acute exercise in human skeletal muscle [33].”
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“Previous work suggests that the largest increase in growth factor response to exercise is produced immediately after exercise (5); therefore, only a single measurement of MAP was made to promote the expedient removal of the muscle.”
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Self-citationVascular Growth in Hypoxic Skeletal Muscle
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Self-citationExercise training enhances basic fibroblast growth factor-induced collateral blood flow
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“This could involve the action of angiogenic growth factors, as Breen and co-workers (9) observed an increase in the expression of vascular endothelial growth factor (VEGF) after acute exercise.”
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“The VEGF mRNA response to increases in exercise intensity has been shown previously.(7,8) Exercise is essential to accelerate neovascularization and thereby elicit a healing response in the injured tendon.”
BackgroundChronic Delivery of a Thrombospondin-1 Mimetic Decreases Skeletal Muscle Capillarity in Mice
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“While there is a substantial body of evidence on the role positive angiogenic factors, such as vascular endothelial growth factor (VEGF) [1,2,3], the role of negative angiogenic factors is incomplete and poorly understood [4].”
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“Several soluble factors have been identified as regulators of SKM angiogenesis, including vascular endothelial growth factor (VEGF), angiopoietin1/2, hypoxia-inducible factor (HIF)1 , transforming growth factor (TGF)1, basic fibroblast growth factor (bFGF), and peroxisome proliterator-activated receptor coactivator-1…”
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Karakılıç, A., Yüksel, O., Kızıldağ, S., Hosgorler, F. U., Topcugil, B., Ilgın, R., Gümüş, H., Güvendi, G., Koç, B., Kandiş, S., et al. (2021) · Acta Neurobiologiae Experimentalis · doi:10.21307/ane-2021-001 · Cited by 26
“On the other hand, the lack of workload progression may diminish muscle hypoxia, which is a triggering factor for muscle VEGF elevation during exercise (Breen et al., 1996).”
BackgroundKandikattu, H. K., Venuprasad, M. P., Pal, A. K., & Khanum, F. (2014) · Industrial Crops and Products · doi:10.1016/j.indcrop.2014.01.043 · Cited by 25
Siafakas, N. M., Jordan, M. C., Wagner, H. E., et al. (2001) · European Respiratory Journal · doi:10.1183/09031936.01.17406810 · Cited by 25
Self-citationMuscle angiogenic growth factor gene responses to exercise in chronic renal failure
Wagner, P. D., Masanés, F., Wagner, H. E., Sala, E., Miró, Ò., Campistol, J. M., Marrades, R. M., Casademont, J., Torregrosa, V., & Roca, J. (2001) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.2001.281.2.r539 · Cited by 25
“In prior work, we have seen responses of these two growth factors in the normal rat (2), although they are never of the same magnitude as for VEGF.”
BackgroundMethodInfluentialSelf-citationMolecular Control of Capillary Growth in Skeletal Muscle
Haas, T. L. (2002) · Canadian Journal of Applied Physiology · doi:10.1139/h02-027 · Cited by 25
“On the other hand, VEGF mRNA and protein are induced rapidly in exercising muscle following short bouts of high intensity exercise (Breen et al., 1996; Hang et al., 1995).”
BackgroundBlottner, D., Hastermann, M., Weber, R., Lenz, R., Gambara, G., Limper, U., Rittweger, J., Bosutti, A., Degens, H., & Salanova, M. (2020) · Frontiers in Physiology · doi:10.3389/fphys.2019.01527 · Cited by 29
So, K., Li, A., Liang, Y., Zhang, L., Luo, X., Wu, L.-L., Chen, Z.-W., Wei, G.-H., Zhang, K., Du, Z.-A., et al. (2021) · Neural Regeneration Research · doi:10.4103/1673-5374.325012 · Cited by 27
Physiological Capillary Regression is not Dependent on Reducing VEGF Expression
Olfert, I. M. (2015) · Microcirculation · doi:10.1111/micc.12263 · Cited by 26
“While this approach may prove less problematic for VEGF [14,31] and TSP-1 [78] mRNA responses, which both peak within one to two hours immediately postexercise, the concept of calculating a ratio between positive and negative angiogenic regulators may ultimately prove to be of limited value if there is an absolute req…”
BackgroundRoles of adenosine and nitric oxide in skeletal muscle in acute and chronic hypoxia
Marshall, J. M. (2001) · Advances in experimental medicine and biology · doi:10.1007/978-1-4757-3401-0_23 · Cited by 24
Knapp, A. E., Goldberg, D., Delavar, H., Trisko, B. M., Tang, K., Hogan, M. C., Wagner, P. D., & Breen, E. C. (2016) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00533.2015 · Cited by 23
“Although several studies have shown that skeletal muscle VEGF expression increases in response to exercise (5, 19), and some studies have shown a link between VEGF expression and increased capillary number in exercise-trained muscle (29, 40), little attention has been given to the requirement of VEGF signaling for mai…”
BackgroundSelf-citationExercise training regulates angiogenic gene expression in white adipose tissue
Lee, H. J. (2018) · Journal of Exercise Rehabilitation · doi:10.12965/jer.1836010.005 · Cited by 22
“Indeed, both single exercise and endurance training upregulated VEGFA expression in skeletal muscle (Breen et al., 1996; Lloyd et al., 2003).”
Gavin, T. P., Westerkamp, L. M., & Zwetsloot, K. A. (2006) · Acta Physiologica · doi:10.1111/j.1748-1716.2006.01609.x · Cited by 24
“It is well established that acute aerobic exercise can increase VEGF mRNA in humans (Gustafsson et al. 1999, Richardson et al. 1999, Gavin et al. 2004, 2005, Croley et al. 2005, Ryan et al. 2006), rats (Breen et al. 1996, Gavin et al. 2000b, Gavin & Wagner 2001) and mice (Choi et al. 2005).”
BackgroundInfluentialAn acetylation rheostat for the control of muscle energy homeostasis
Menzies, K. J., & Auwerx, J. H. (2013) · Journal of Molecular Endocrinology · doi:10.1530/jme-13-0140 · Cited by 23
“An essential mediator of this pathway, vascular endothelial growth factor (VEGF), increases in response to acute exercise (Breen et al. 1996, Amaral et al. 2001).”
BackgroundAudet, G. N., Meek, T. H., Garland, T., & Olfert, I. M. (2011) · Experimental Physiology · doi:10.1113/expphysiol.2011.057711 · Cited by 23
“Given that local tissue hypoxia is thought to be among the key stimuli for the VEGF response to exercise (Levy et al. 1995; Breen et al. 1996; Richardson et al. 1999; Olfert et al. 2001), we have previously speculated that the attenuated VEGF response to an acute bout of exercise post-training is…”
BackgroundMethodInfluentialSkeletal muscle, haematological and splenic volume characteristics of elite breath-hold divers
Elia, A., Wilson, O. J., Lees, M. J., Parker, P. J., Barlow, M., Cocks, M. S., & O'Hara, J. P. (2019) · European Journal of Applied Physiology · doi:10.1007/s00421-019-04230-6 · Cited by 27
Adenosine infusion increases plasma levels of VEGF in humans
Adair, T. H., Cotten, R., Gu, J., et al. (2005) · BMC Physiology · doi:10.1186/1472-6793-5-10 · Cited by 23
“Breen et al. (1996) found a fourfold increase in VEGF mRNA at the termination of a one hour bout of treadmill exercise in rats.”
BackgroundMethodSuzuki, J. (2005) · Experimental Physiology · doi:10.1113/expphysiol.2005.031138 · Cited by 22
“1992) and in skeletal muscles in vivo (Breen et al. 1996).”
BackgroundInfluentialHypoxia and Hyperoxia Affect Serum Angiogenic Regulators in T2DM Men during Cycling
Brinkmann, C. K., Metten, A., Scriba, P., Tagarakis, C. V. M., Wahl, P., Latsch, J., Brixius, K., & Bloch, W. (2017) · International Journal of Sports Medicine · doi:10.1055/s-0042-116823 · Cited by 21
“[2] have demonstrated that VEGF mRNA levels increased through physical exercise (1-h run) in skeletal muscle of Wistar rats and reached their peak immediately post-exercise.”
BackgroundOlenich, S. A., Audet, G. N., Roberts, K. A., et al. (2014) · The Journal of Physiology · doi:10.1113/jphysiol.2014.271213 · Cited by 22
“…(VEGF) and anti-angiogenic thrombospondin-1 (TSP-1), both of which have been shown to exhibit robust mRNA response to an acute bout of exercise in rodents and humans (Breen et al. 1996; Gustafsson et al. 1999; Richardson et al. 1999; Gavin & Wagner, 2001; Olfert et al. 2006; Hoier et al. 2012).”
BackgroundFranci, C. R. (2002) · Medicina (Ribeirão Preto) · doi:10.11606/issn.2176-7262.v35i3p277-283 · Cited by 22
ACE inhibition modifies exercise‐induced pro‐angiogenic and mitochondrial gene transcript expression
van Ginkel, S., Ruoss, S., Valdivieso, P., Degens, H., Waldron, S., HAAN, A. D., & Flück, M. (2015) · Scandinavian Journal of Medicine and Science in Sports · doi:10.1111/sms.12572 · Cited by 21
“Breen et al. (1996) showed that mRNA levels of angiogenic growth factors such as VEGF in the gastrocnemius of rat were significantly increased after a bout of endurance exercise.”
Background
Metadata
- Authors
- Breen, E. C., Johnson, E. C., Wagner, H., Tseng, H. M., Sung, L. A., & Wagner, P. D.
- Affiliations
- University of California San Diego (US)
- Venue
- Journal of Applied Physiology
- Publisher
- American Physiological Society
- Published
- 1996-07-01
- Volume
- 81
- Issue
- 1
- Pages
- 355-361
- ISSN
- 0161-7567 (ISSN-L)
- 8750-7587
- 1522-1601
- OpenAlex
- W2137609684
- Cited by
- 302
- References
- 0
- Citations by year
- 2026: 3 · 2025: 1 · 2024: 3 · 2023: 2 · 2022: 5 · 2021: 8 · 2020: 7 · 2019: 6 · 2018: 5 · 2017: 5 · 2016: 15 · 2015: 21 · 2014: 13 · 2013: 13 · 2012: 13
- FWCI
- 22.86
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Applied Physiology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (5r01hl046910-04)
- National Heart, Lung, and Blood Institute (P01HL017731, 2-PO1-HL-17731, 5-RO1-HL-46910)
- Topics
- Health Sciences › Medicine › Physiology (medical) › Cardiovascular and exercise physiology
- Health Sciences › Medicine › Physiology (medical) › Exercise and Physiological Responses
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Angiogenesis and VEGF in Cancer
- Keywords
- exercise-induced angiogenesis, angiogenic factors, vascular endothelial growth factor, basic fibroblast growth factor, TGF-β1, hypoxic exercise, hypoxia, intracellular oxygen tension, mRNA expression, gastrocnemius, single bout exercise
- MeSH terms
- Animals, Hypoxia, Physical Exertion, Female, Half-Life, RNA, Messenger, Blotting, Northern, Transforming Growth Factor beta, Fibroblast Growth Factor 2, Endothelial Growth Factors, Rats, Wistar, In Situ Hybridization, Muscle, Skeletal, Rats
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