Skeletal muscle adaptation to indirect electrical stimulation: divergence between microvascular and metabolic adaptations.
angiogenesis
exercise
metabolomics
muscle stimulation
Journal
Experimental physiology
ISSN: 1469-445X
Titre abrégé: Exp Physiol
Pays: England
ID NLM: 9002940
Informations de publication
Date de publication:
06 2023
06 2023
Historique:
received:
30
01
2023
accepted:
15
03
2023
medline:
2
6
2023
pubmed:
8
4
2023
entrez:
7
4
2023
Statut:
ppublish
Résumé
What is the central question of this study? Can we manipulate muscle recruitment to differentially enhance skeletal muscle fatigue resistance? What is the main finding and its importance? Through manipulation of muscle activation patterns, it is possible to promote distinct microvascular growth. Enhancement of fatigue resistance is closely associated with the distribution of the capillaries within the muscle, not necessarily with quantity. Additionally, at the acute stages of remodelling in response to indirect electrical stimulation, the improvement in fatigue resistance appears to be primarily driven by vascular remodelling, with metabolic adaptation of secondary importance. Exercise involves a complex interaction of factors influencing muscle performance, where variations in recruitment pattern (e.g., endurance vs. resistance training) may differentially modulate the local tissue environment (i.e., oxygenation, blood flow, fuel utilization). These exercise stimuli are potent drivers of vascular and metabolic change. However, their relative contribution to adaptive remodelling of skeletal muscle and subsequent performance is unclear. Using implantable devices, indirect electrical stimulation (ES) of locomotor muscles of rat at different pacing frequencies (4, 10 and 40 Hz) was used to differentially recruit hindlimb blood flow and modulate fuel utilization. After 7 days, ES promoted significant remodelling of microvascular composition, increasing capillary density in the cortex of the tibialis anterior by 73%, 110% and 55% for the 4 Hz, 10 and 40 Hz groups, respectively. Additionally, there was remodelling of the whole muscle metabolome, including significantly elevated amino acid turnover, with muscle kynurenic acid levels doubled by pacing at 10 Hz (P < 0.05). Interestingly, the fatigue index of skeletal muscle was only significantly elevated in 10 Hz (58% increase) and 40 Hz (73% increase) ES groups, apparently linked to improved capillary distribution. These data demonstrate that manipulation of muscle recruitment pattern may be used to differentially expand the capillary network prior to altering the metabolome, emphasising the importance of local capillary supply in promoting exercise tolerance.
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
891-911Subventions
Organisme : British Heart Foundation
ID : PG/14/15/30691
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 204822/Z/16/Z
Pays : United Kingdom
Informations de copyright
© 2023 The Authors. Experimental Physiology published by John Wiley & Sons Ltd on behalf of The Physiological Society.
Références
Agudelo, L. Z., Ferreira, D. M., Dadvar, S., Cervenka, I., Ketscher, L., Izadi, M., Zhengye, L., Furrer, R., Handschin, C., & Venckunas, T. (2019). Skeletal muscle PGC-1α1 reroutes kynurenine metabolism to increase energy efficiency and fatigue-resistance. Nature Communications, 10(1), 1-12.
Allison, D. J., Nederveen, J. P., Snijders, T., Bell, K. E., Kumbhare, D., Phillips, S. M., Parise, G., & Heisz, J. J. (2019). Exercise training impacts skeletal muscle gene expression related to the kynurenine pathway. American Journal of Physiology. Cell Physiology, 316(3), C444-C448.
Al-Shammari, A. A., Gaffney, E. A., & Egginton, S. (2014). Modelling capillary oxygen supply capacity in mixed muscles: Capillary domains revisited. Journal of Theoretical Biology, 356, 47-61.
Al-Shammari, A. A., Kissane, R. W. P., Holbek, S., Mackey, A. L., Andersen, T. R., Gaffney, E. A., Kjaer, M., & Egginton, S. (2019). Integrated method for quantitative morphometry and oxygen transport modeling in striated muscle. Journal of Applied Physiology, 126(3), 544-557.
Annex, B. H., Torgan, C. E., Lin, P., Taylor, D. A., Thompson, M. A., Peters, K. G., & Kraus, W. E. (1998). Induction and maintenance of increased VEGF protein by chronic motor nerve stimulation in skeletal muscle. American Journal of Physiology. Heart and Circulatory Physiology, 274(3), H860-H867.
Bouletreau, P., Patricot, M., Saudin, F., Guiraud, M., & Mathian, B. (1987). Effects of intermittent electrical stimulations on muscle catabolism in intensive care patients. Journal of Parenteral and Enteral Nutrition, 11(6), 552-555.
Brown, M., Hudlicka, O., Makki, R., & Weiss, J. (1995). Low-molecular-mass endothelial cell-stimulating angiogenic factor in relation to capillary growth induced in rat skeletal muscle by low-frequency electrical stimulation. International Journal of Microcirculation, 15(3), 111-116.
Brownson, C., Isenberg, H., Brown, W., Salmons, S., & Edwards, Y. (1988). Changes in skeletal muscle gene transcription induced by chronic stimulation. Muscle & Nerve, 11, 1183-1189.
Calles-Escandon, J., Cunningham, J. J., Snyder, P., Jacob, R., Huszar, G., Loke, J., & Felig, P. (1984). Influence of exercise on urea, creatinine, and 3-methylhistidine excretion in normal human subjects. American Journal of Physiology. Endocrinology and Metabolism, 246(4), E334-E338.
Deveci, D., & Egginton, S. (2002). Differing mechanisms of cold-induced changes in capillary supply in m. tibialis anterior of rats and hamsters. Journal of Experimental Biology, 205(6), 829-840.
Deveci, D., Marshall, J., & Egginton, S. (2002). Chronic hypoxia induces prolonged angiogenesis in skeletal muscles of rat. Experimental Physiology, 87(3), 287-291.
Dohm, G. L., Williams, R. T., Kasperek, G. J., & van Rij, A. M. (1982). Increased excretion of urea and N tau-methylhistidine by rats and humans after a bout of exercise. Journal of Applied Physiology, 52(1), 27-33.
Egginton, S. (1988). Effect of inter-animal variation on a nested sampling design for stereological analysis of skeletal muscle. Acta Stereol, 7, 81-89.
Egginton, S. (1990). Morphometric analysis of tissue capillary supply. In Vertebrate gas exchange. pp. 73-141. Springer.
Egginton, S. (2009). Invited review: Activity-induced angiogenesis. Pflügers Archiv - European Journal of Physiology, 457(5), 963-977.
Egginton, S., & Gaffney, E. (2010). Tissue capillary supply-it's quality not quantity that counts!. Experimental Physiology, 95, 971-979.
Egginton, S., & Hudlicka, O. (1999). Early changes in performance, blood flow and capillary fine structure in rat fast muscles induced by electrical stimulation. The Journal of Physiology, 515(1), 265-275.
Goldspink, D. F., Easton, J., Winterburn, S. K., Williams, P. E., & Goldspink, G. E. (1991). The role of passive stretch and repetitive electrical stimulation in preventing skeletal muscle atrophy while reprogramming gene expression to improve fatigue resistance. Journal of Cardiac Surgery, 6(1S), 218-224.
Gondin, J., Brocca, L., Bellinzona, E., d'Antona, G., Maffiuletti, N. A., Miotti, D., Pellegrino, M. A., & Bottinelli, R. (2011). Neuromuscular electrical stimulation training induces atypical adaptations of the human skeletal muscle phenotype: A functional and proteomic analysis. Journal of Applied Physiology, 110(2), 433-450.
Graham, Z. A., Siedlik, J. A., Harlow, L., Sahbani, K., Bauman, W. A., Tawfeek, H. A., & Cardozo, C. P. (2019). Key glycolytic metabolites in paralyzed skeletal muscle are altered seven days after spinal cord injury in mice. Journal of Neurotrauma, 36(18), 2722-2731.
Grasa, J., Sierra, M., Muñoz, M., Soteras, F., Osta, R., Calvo, B., & Miana-Mena, F. (2014). On simulating sustained isometric muscle fatigue: A phenomenological model considering different fiber metabolisms. Biomechanics and Modeling in Mechanobiology, 13(6), 1373-1385.
Grundy, D. (2015). Principles and standards for reporting animal experiments in The Journal of Physiology and Experimental Physiology. Journal of Physiology, 100, 755-758. Wiley Online Library.
Hang, J., Kong, L., Gu, J., & Adair, T. (1995). VEGF gene expression is upregulated in electrically stimulated rat skeletal muscle. American Journal of Physiology. Heart and Circulatory Physiology, 269(5), H1827-H1831.
Hargreaves, D., Egginton, S., & Hudlicka, O. (1990). Changes in capillary perfusion induced by different patterns of activity in rat skeletal muscle. Microvascular Research, 40(1), 14-28.
Harris, C. I. (1981). Reappraisal of the quantitative importance of non-skeletal-muscle source of N τ-methylhistidine in urine. Biochemical Journal, 194(3), 1011-1014.
Hauton, D., Winter, J., Al-Shammari, A. A., Gaffney, E. A., Evans, R. D., & Egginton, S. (2015). Changes to both cardiac metabolism and performance accompany acute reductions in functional capillary supply. Biochimica et Biophysica Acta - General Subjects, 1850(4), 681-690.
Hawker, M., & Egginton, S. (1999). The effect of stimulation frequency on blood flow in rat fast skeletal muscles. Experimental Physiology, 84(5), 941-946.
Hoier, B., Walker, M., Passos, M., Walker, P. J., Green, A., Bangsbo, J., Askew, C. D., & Hellsten, Y. (2013). Angiogenic response to passive movement and active exercise in individuals with peripheral arterial disease. Journal of Applied Physiology, 115(12), 1777-1787.
Hudlicka, O., Aitman, T., Heilig, A., Leberer, E., Tyler, K., & Pette, D. (1984). Effects of different patterns of long-term stimulation on blood flow, fuel uptake and enzyme activities in rabbit fast skeletal muscles. Pflügers Archiv, 402(3), 306-311.
Hudlicka, O., Brown, M., Egginton, S., & Dawson, J. (1994). Effect of long-term electrical stimulation on vascular supply and fatigue in chronically ischemic muscles. Journal of Applied Physiology, 77(3), 1317-1324.
Hudlická, O., Egginton, S., & Brown, M. (1988). Capillary diffusion distances-their importance for cardiac and skeletal muscle performance. Physiology, 3(4), 134-138.
Hudlicka, O., & Tyler, K. (1984). The effect of long-term high-frequency stimulation on capillary density and fibre types in rabbit fast muscles. The Journal of Physiology, 353(1), 435-445.
Iwatsu, K., Iida, Y., Kono, Y., Yamazaki, T., Usui, A., & Yamada, S. (2017). Neuromuscular electrical stimulation may attenuate muscle proteolysis after cardiovascular surgery: A preliminary study. The Journal of Thoracic and Cardiovascular Surgery, 153(2), 373-379.e1. e371.
Jones, S., Man, W. D. C., Gao, W., Higginson, I. J., Wilcock, A., & Maddocks, M. (2016). Neuromuscular electrical stimulation for muscle weakness in adults with advanced disease. Cochrane Database of Systematic Reviews, 2016(10), CD009419.
Kissane, R. W., Al-Shammari, A. A., & Egginton, S. (2021). The importance of capillary distribution in supporting muscle function, building on Krogh's seminal ideas. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 254, 110889.
Kissane, R. W., Tickle, P. G., Doody, N. E., Al-Shammari, A. A., & Egginton, S. (2020). Distinct structural and functional angiogenic responses are induced by different mechanical stimuli. Microcirculation, 28(4), e12677.
Kissane, R. W. P., Wright, O., Al'Joboori, Y. D., Marczak, P., Ichiyama, R. M., & Egginton, S. (2019). Effects of treadmill training on microvascular remodeling in the rat after spinal cord injury. Muscle & Nerve, 59, 370-379.
Kraus, W. E., Longabaugh, J. P., & Liggett, S. B. (1992). Electrical pacing induces adenylyl cyclase in skeletal muscle independent of the beta-adrenergic receptor. American Journal of Physiology. Endocrinology and Metabolism, 263(2), E226-E230.
Kwong, W., & Vrbova, G. (1981). Effects of low-frequency electrical stimulation on fast and slow muscles of the rat. Pflügers Archiv, 391(3), 200-207.
Linderman, J. R., Kloehn, M. R., & Greene, A. S. (2000). Development of an implantable muscle stimulator: Measurement of stimulated angiogenesis and poststimulus vessel regression. Microcirculation, 7(2), 119-128.
Martin, T. P., Stein, R. B., Hoeppner, P. H., & Reid, D. C. (1992). Influence of electrical stimulation on the morphological and metabolic properties of paralyzed muscle. Journal of Applied Physiology, 72(4), 1401-1406.
McCullagh, K., Poole, R., Halestrap, A., Tipton, K., O'Brien, M., & Bonen, A. (1997). Chronic electrical stimulation increases MCT1 and lactate uptake in red and white skeletal muscle. American Journal of Physiology. Endocrinology and Metabolism, 273(2), E239-E246.
Millward, D. J., & Bates, P. C. (1983). 3-Methylhistidine turnover in the whole body, and the contribution of skeletal muscle and intestine to urinary 3-methylhistidine excretion in the adult rat. Biochemical Journal, 214(2), 607-615.
Mortensen, S. P., Winding, K. M., Iepsen, U. W., Munch, G. W., Marcussen, N., Hellsten, Y., Pedersen, B. K., & Baum, O. (2019). The effect of two exercise modalities on skeletal muscle capillary ultrastructure in individuals with type 2 diabetes. Scandinavian Journal of Medicine & Science in Sports, 29, 360-368.
Morville, T., Sahl, R. E., Moritz, T., Helge, J. W., & Clemmensen, C. (2020). Plasma metabolome profiling of resistance exercise and endurance exercise in humans. Cell Reports, 33(13), 108554.
Nagasaka, M., Kohzuki, M., Fujii, T., Kanno, S., Kawamura, T., Onodera, H., Itoyama, Y., Ichie, M., & Sato, Y. (2006). Effect of low-voltage electrical stimulation on angiogenic growth factors in ischaemic rat skeletal muscle. Clinical and Experimental Pharmacology and Physiology, 33(7), 623-627.
Olfert, I. M., Baum, O., Hellsten, Y., & Egginton, S. (2016). Advances and challenges in skeletal muscle angiogenesis. American Journal of Physiology. Heart and Circulatory Physiology, 310(3), H326-H336.
Percie du Sert, N., Hurst, V., Ahluwalia, A., Alam, S., Avey, M. T., Baker, M., Browne, W. J., Clark, A., Cuthill, I. C., & Dirnagl, U. (2020). The ARRIVE guidelines 2.0: Updated guidelines for reporting animal research. Journal of Cerebral Blood Flow & Metabolism, 40, 1769-1777.
Pette, D., Smith, M. E., Staudte, H. W., & Vrbová, G. (1973). Effects of long-term electrical stimulation on some contractile and metabolic characteristics of fast rabbit muscles. Pflügers Archiv, 338(3), 257-272.
Pette, D., & Tyler, K. (1983). Response of succinate dehydrogenase activity in fibres of rabbit tibialis anterior muscle to chronic nerve stimulation. The Journal of Physiology, 338(1), 1-9.
Salazar, C., Armenta, J. M., Cortés, D. F., & Shulaev, V. (2012). Combination of an AccQ·Tag-ultra performance liquid chromatographic method with tandem mass spectrometry for the analysis of amino acids. Amino Acid Analysis: Methods and Protocols, 828, 13-28.
Sanford, J. A., Nogiec, C. D., Lindholm, M. E., Adkins, J. N., Amar, D., Dasari, S., Drugan, J. K., Fernández, F. M., Radom-Aizik, S., & Schenk, S. (2020). Molecular transducers of physical activity consortium (MoTrPAC): Mapping the dynamic responses to exercise. Cell, 181(7), 1464-1474.
Schlittler, M., Goiny, M., Agudelo, L. Z., Venckunas, T., Brazaitis, M., Skurvydas, A., Kamandulis, S., Ruas, J. L., Erhardt, S., & Westerblad, H. (2016). Endurance exercise increases skeletal muscle kynurenine aminotransferases and plasma kynurenic acid in humans. American Journal of Physiology. Cell Physiology, 310(10), C836-C840.
Scott, O., Vrbova, G., Hyde, S., & Dubowitz, V. (1985). Effects of chronic low frequency electrical stimulation on normal human tibialis anterior muscle. Journal of Neurology, Neurosurgery & Psychiatry, 48, 774-781.
Simoneau, J., Kaufmann, M., & Pette, D. (1993). Asynchronous increases in oxidative capacity and resistance to fatigue of electrostimulated muscles of rat and rabbit. The Journal of Physiology, 460(1), 573-580.
Tickle, P. G., Hendrickse, P. W., Degens, H., & Egginton, S. (2020). Impaired skeletal muscle performance as a consequence of random functional capillary rarefaction can be restored with overload-dependent angiogenesis. The Journal of Physiology, 598(6), 1187-1203.
Wassner, S., & Li, J. (1982). N tau-methylhistidine release: Contributions of rat skeletal muscle, GI tract, and skin. American Journal of Physiology. Endocrinology and Metabolism, 243(4), E293-E297.
Wyckelsma, V., Lindkvist, W., Venckunas, T., Brazaitis, M., Kamandulis, S., Pääsuke, M., Ereline, J., Westerblad, H., & Andersson, D. (2020). Kynurenine aminotransferase isoforms display fiber-type specific expression in young and old human skeletal muscle. Experimental Gerontology, 134, 110880.
Yan, Z., Okutsu, M., Akhtar, Y. N., & Lira, V. A. (2011). Regulation of exercise-induced fiber type transformation, mitochondrial biogenesis, and angiogenesis in skeletal muscle. Journal of Applied Physiology, 110(1), 264-274.