Influence of physical activity on autophagy inducing and reduction of cancer incidence: critical review of physiological and metabolic mechanisms.
DOI:
https://doi.org/10.33448/rsd-v10i16.24223Keywords:
Autophagy; Exercise; Disease prevention; Cancer.Abstract
Objective: To describe the main mechanisms of autophagy stimulated by physical activity and its relationship with the reduction in the incidence of cancer. Material and methods: Data collections were carried out through the analysis of the scientific literature available in the MEDLINE, ScienceDirect and Wiley databases, independently and manually. The terms "cancer", "autophagy" and "physical activity" were used as search descriptors, and the period of time for publications covered the years 1990 to 2020. The inclusion criteria were: "works published within the scope of the study, published in the aforementioned period”. And as an exclusion criterion: “works not related to the study topic and with reports that are already outdated according to current literature”. Results: Physical activity positively influences different systems, leading to acute and chronic changes. The benefits in metabolic, immune, cancerous, cardiovascular, psychiatric and neurological pathologies are indisputable and the mechanisms are being elucidated. Autophagy mediates the digestion and recycling of obsolete cell parts during starvation and participates in a variety of physiological waste removal processes. Autophagy is able to eliminate microorganisms, toxic protein aggregates, genotoxic, playing roles during infection, aging and disease pathogenesis. Conclusion: From the analysis of the mechanisms involved in physical activity-induced autophagy, three main points were postulated: 1) Via mTORC1 inactivated by starvation, 2) Regulation by reactive oxygen species and hypoxia, 3) Regulation of autophagy by alternative pathways to mTORC1.
References
Ahlborg, G., Felig, P., Hagenfeldt, L., Hendler, R., & Wahren, J. (1974). Substrate turnover during prolonged exercise in man. Splanchnic and leg metabolism of glucose, free fatty acids, and amino acids. Journal of Clinical Investigation, 53(4), 1080–1090. https://doi.org/10.1172/JCI107645
Alexander, A., Cai, S. L., Kim, J., Nanez, A., Sahin, M., MacLean, K. H., Inoki, K., Guan, K. L., Shen, J., Person, M. D., Kusewitt, D., Mills, G. B., Kastan, M. B., & Walker, C. L. (2010). ATM signals to TSC2 in the cytoplasm to regulate mTORC1 in response to ROS. Proceedings of the National Academy of Sciences of the United States of America, 107(9), 4153–4158. https://doi.org/10.1073/pnas.0913860107
Andriolo, V., Dietrich, S., Knüppel, S., Bernigau, W., & Boeing, H. (2019). Traditional risk factors for essential hypertension: analysis of their specific combinations in the EPIC-Potsdam cohort. Scientific Reports, 9(1), 1–10. https://doi.org/10.1038/s41598-019-38783-5
Aulianida, D., Liestyasari, S. I., & Ch, S. R. (2003). Cem Bilhões de Neurônios. In Journal of Chemical Information and Modeling (Vol. 53, Issue 9).
Axe, E. L., Walker, S. A., Manifava, M., Chandra, P., Roderick, H. L., Habermann, A., Griffiths, G., & Ktistakis, N. T. (2008). Autophagosome formation from membrane compartments enriched in phosphatidylinositol 3-phosphate and dynamically connected to the endoplasmic reticulum. Journal of Cell Biology, 182(4), 685–701. https://doi.org/10.1083/jcb.200803137
Bar-Peled, L., Schweitzer, L. D., Zoncu, R., & Sabatini, D. M. (2012). Ragulator is a GEF for the rag GTPases that signal amino acid levels to mTORC1. Cell, 150(6), 1196–1208. https://doi.org/10.1016/j.cell.2012.07.032
Beyfuss, K., Erlich, A. T., Triolo, M., & Hood, D. A. (2018). The Role of p53 in Determining Mitochondrial Adaptations to Endurance Training in Skeletal Muscle. Scientific Reports, 8(1), 1–14. https://doi.org/10.1038/s41598-018-32887-0
Blair, S. N., LaMonte, M. J., & Nichaman, M. Z. (2004). The evolution of physical activity recommendations: how much is enough? The American Journal of Clinical Nutrition, 79(5), 913–920. https://doi.org/10.1093/ajcn/79.5.913s
Brambilla, P., Pozzobon, G., & Pietrobelli, A. (2011). Physical activity as the main therapeutic tool for metabolic syndrome in childhood. International Journal of Obesity, 35(1), 16–28. https://doi.org/10.1038/ijo.2010.255
Cassilhas, R. C., Tufik, S., & De Mello, M. T. (2016). Physical exercise, neuroplasticity, spatial learning and memory. Cellular and Molecular Life Sciences, 73(5), 975–983. https://doi.org/10.1007/s00018-015-2102-0
Cen, X., Chen, Y., Xu, X., Wu, R., He, F., Zhao, Q., Sun, Q., Yi, C., Wu, J., Najafov, A., & Xia, H. (2020). Pharmacological targeting of MCL-1 promotes mitophagy and improves disease pathologies in an Alzheimer’s disease mouse model. Nature Communications, 11(1). https://doi.org/10.1038/s41467-020-19547-6
Chen, X., Wang, Q., Zhang, Y., Xie, Q., & Tan, X. (2019). Physical Activity and Risk of Breast Cancer: A Meta-Analysis of 38 Cohort Studies in 45 Study Reports. Value in Health, 22(1), 104–128. https://doi.org/10.1016/j.jval.2018.06.020
Coggan, A. R., Swanson, S. C., Mendenhall, L. A., Habash, D. L., & Kien, C. L. (1995). Effect of endurance training on hepatic glycogenolysis and gluconeogenesis during prolonged exercise in men. American Journal of Physiology - Endocrinology and Metabolism, 268(3 31-3). https://doi.org/10.1152/ajpendo.1995.268.3.e375
Durcan, T. M., & Fon, E. A. (2015). USP8 and PARK2/parkin-mediated mitophagy. Autophagy, 11(2), 428–429. https://doi.org/10.1080/15548627.2015.1009794
Elizabeth, Q. (1957). Supine Leg Exercise. 1942, 294–308.
Fritzen, A. M., Madsen, A. B., Kleinert, M., Treebak, J. T., Lundsgaard, A. M., Jensen, T. E., Richter, E. A., Wojtaszewski, J., Kiens, B., & Frøsig, C. (2016). Regulation of autophagy in human skeletal muscle: Effects of exercise, exercise training and insulin stimulation. Journal of Physiology, 594(3), 745–761. https://doi.org/10.1113/JP271405
Ganley, I. G., Lam, D. H., Wang, J., Ding, X., Chen, S., & Jiang, X. (2009). ULK1·ATG13·FIP200 complex mediates mTOR signaling and is essential for autophagy. Journal of Biological Chemistry, 284(18), 12297–12305. https://doi.org/10.1074/jbc.M900573200
Guyton & Hall. (2011). Tratado de Fisiologia - Guyton 12a Edição.pdf (p. 1176).
Hale, A. N., Ledbetter, D. J., Gawriluk, T. R., & Rucker, E. B. (2013). Autophagy: Regulation and role in development. Autophagy, 9(7), 951–972. https://doi.org/10.4161/auto.24273
Halling, J. F., & Pilegaard, H. (2017). Autophagy-Dependent Beneficial Effects of Exercise. Cold Spring Harbor Perspectives in Medicine, 7(8), 1–13. https://doi.org/10.1101/cshperspect.a029777
Hanakawa, T., Immisch, I., Toma, K., Dimyan, M. A., Van Gelderen, P., & Hallett, M. (2003). Functional properties of brain areas associated with motor execution and imagery. Journal of Neurophysiology, 89(2), 989–1002. https://doi.org/10.1152/jn.00132.2002
Hansen, J. S., Pedersen, B. K., Xu, G., Lehmann, R., Weigert, C., & Plomgaard, P. (2016). Exercise-induced secretion of FGF21 and follistatin are blocked by pancreatic clamp and impaired in type 2 diabetes. Journal of Clinical Endocrinology and Metabolism, 101(7), 2816–2825. https://doi.org/10.1210/jc.2016-1681
Hardwick, R. M., Rottschy, C., Miall, R. C., & Eickhoff, S. B. (2013). A quantitative meta-analysis and review of motor learning in the human brain. NeuroImage, 67, 283–297. https://doi.org/10.1016/j.neuroimage.2012.11.020
Hargreaves, M., & Spriet, L. L. (2020). Skeletal muscle energy metabolism during exercise. Nature Metabolism, 2(9), 817–828. https://doi.org/10.1038/s42255-020-0251-4
Harrison, D. G., Widder, J., Grumbach, I., Chen, W., Weber, M., & Searles, C. (2006). Endothelial mechanotransduction, nitric oxide and vascular inflammation. Journal of Internal Medicine, 259(4), 351–363. https://doi.org/10.1111/j.1365-2796.2006.01621.x
Hawley, J. A., Hargreaves, M., Joyner, M. J., & Zierath, J. R. (2014). Integrative biology of exercise. Cell, 159(4), 738–749. https://doi.org/10.1016/j.cell.2014.10.029
Haydon, A. M. M., MacInnis, R. J., English, D. R., & Giles, G. G. (2006). Effect of physical activity and body size on survival after diagnosis with colorectal cancer. Gut, 55(1), 62–67. https://doi.org/10.1136/gut.2005.068189
He, C., Bassik, M. C., Moresi, V., Sun, K., Wei, Y., Zou, Z., An, Z., Loh, J., Fisher, J., Sun, Q., Korsmeyer, S., Packer, M., May, H. I., Hill, J. A., Virgin, H. W., Gilpin, C., Xiao, G., Bassel-Duby, R., Scherer, P. E., & Levine, B. (2012). Exercise-induced BCL2-regulated autophagy is required for muscle glucose homeostasis. Nature, 481(7382), 511–515. https://doi.org/10.1038/nature10758
He, H., Dang, Y., Dai, F., Guo, Z., Wu, J., She, X., Pei, Y., Chen, Y., Ling, W., Wu, C., Zhao, S., Liu, J. O., & Yu, L. (2003). Post-translational modifications of three members of the human MAP1LC3 family and detection of a novel type of modification for MAP1LC3B. Journal of Biological Chemistry, 278(31), 29278–29287. https://doi.org/10.1074/jbc.M303800200
Hojman, P., Gehl, J., Christensen, J. F., & Pedersen, B. K. (2017). Molecular Mechanisms Linking Exercise to Cancer Prevention and Treatment. Cell Metabolism, 27(1), 10–21. https://doi.org/10.1016/j.cmet.2017.09.015
Holczer, M., Hajdú, B., Lőrincz, T., Szarka, A., Bánhegyi, G., & Kapuy, O. (2020). Fine-tuning of AMPK–ULK1–mTORC1 regulatory triangle is crucial for autophagy oscillation. Scientific Reports, 10(1), 1–12. https://doi.org/10.1038/s41598-020-75030-8
Ichinose, M., Maeda, S., Kondo, N., & Nishiyasu, T. (2014). Blood pressure regulation II: What happens when one system must serve two masters - Oxygen delivery and pressure regulation? European Journal of Applied Physiology, 114(3), 451–465. https://doi.org/10.1007/s00421-013-2691-y
Inoki, K., Li, Y., Zhu, T., Wu, J., & Guan, K. L. (2002). TSC2 is phosphorylated and inhibited by Akt and suppresses mTOR signalling. Nature Cell Biology, 4(9), 648–657. https://doi.org/10.1038/ncb839
Itakura, E., Kishi-Itakura, C., & Mizushima, N. (2012). The hairpin-type tail-anchored SNARE syntaxin 17 targets to autophagosomes for fusion with endosomes/lysosomes. Cell, 151(6), 1256–1269. https://doi.org/10.1016/j.cell.2012.11.001
Kang, D. W., Lee, J., Suh, S. H., Ligibel, J., Courneya, K. S., & Jeon, J. Y. (2017). Effects of exercise on insulin, IGF axis, adipocytokines, and inflammatory markers in breast cancer survivors: A systematic review and meta-analysis. Cancer Epidemiology Biomarkers and Prevention, 26(3), 355–365. https://doi.org/10.1158/1055-9965.EPI-16-0602
Kang, R., Zeh, H. J., Lotze, M. T., & Tang, D. (2011). The Beclin 1 network regulates autophagy and apoptosis. Cell Death and Differentiation, 18(4), 571–580. https://doi.org/10.1038/cdd.2010.191
Kang, Y. L., Saleem, M. A., Chan, K. W., Yung, B. Y. M., & Law, H. K. W. (2014). Trehalose, an mTOR independent autophagy inducer, alleviates human podocyte injury after puromycin aminonucleoside treatment. PLoS ONE, 9(11), 1–9. https://doi.org/10.1371/journal.pone.0113520
Kaushik, S., Bandyopadhyay, U., Sridhar, S., Kiffin, R., Martinez-Vicente, M., Kon, M., Orenstein, S. J., Wong, E., & Cuervo, A. M. (2011). Chaperone-mediated autophagy at a glance. Journal of Cell Science, 124(4), 495–499. https://doi.org/10.1242/jcs.073874
Kim, M., Sujkowski, A., Namkoong, S., Gu, B., Cobb, T., Kim, B., Kowalsky, A. H., Cho, C. S., Semple, I., Ro, S. H., Davis, C., Brooks, S. V., Karin, M., Wessells, R. J., & Lee, J. H. (2020). Sestrins are evolutionarily conserved mediators of exercise benefits. Nature Communications, 11(1), 1–14. https://doi.org/10.1038/s41467-019-13442-5
Koelwyn, G. J., Zhuang, X., Tammela, T., Schietinger, A., & Jones, L. W. (2020). Exercise and immunometabolic regulation in cancer. Nature Metabolism, 2(9), 849–857. https://doi.org/10.1038/s42255-020-00277-4
Kraemer, W. J., Haekkinen, K., Newton, R. U., McCormick, M., Nindl, B. C., Volek, J. S., Gotshalk, L. A., Fleck, S. J., Campbell, W. W., Gordon, S. E., Farrell, P. A., & Evans, W. J. (1998). Acute hormonal responses to heavy resistance exercise in younger and older men. / Reponses hormonales aigues a un exercice important de resistance chez les hommes jeunes et vieux. European Journal of Applied Physiology & Occupational Physiology, 77(3), 206–211. http://articles.sirc.ca/search.cfm?id=461991%5Cnhttp://ezproxy.library.yorku.ca/login?url=http://search.ebscohost.com/login.aspx?direct=true&db=sph&AN=SPH461991&site=ehost-live%5Cnhttp://link.springer.de
Kumsta, C., Chang, J. T., Lee, R., Tan, E. P., Yang, Y., Loureiro, R., Choy, E. H., Lim, S. H. Y., Saez, I., Springhorn, A., Hoppe, T., Vilchez, D., & Hansen, M. (2019). The autophagy receptor p62/SQST-1 promotes proteostasis and longevity in C. elegans by inducing autophagy. Nature Communications, 10(1), 5648. https://doi.org/10.1038/s41467-019-13540-4
L. Brunton, L., Hilal-Dandan, R., & C. Knollmann, B. (2012). Goodman & Gilman 12a Ed., As Bases Farmacológicas da Terapêutica. 12.
Lee, S., Libman, I., Hughan, K., Kuk, J. L., Jeong, J. H., Zhang, D., & Arslanian, S. (2018). Effects of Exercise Modality on Insulin Resistance and Ectopic Fat in Adolescents with Overweight and Obesity: A Randomized Clinical Trial. The Journal of Pediatrics, 206, 91-98.e1. https://doi.org/10.1016/j.jpeds.2018.10.059
Lee, Y., Kwon, I., Jang, Y., Song, W., Cosio-Lima, L. M., & Roltsch, M. H. (2017). Potential signaling pathways of acute endurance exercise-induced cardiac autophagy and mitophagy and its possible role in cardioprotection. Journal of Physiological Sciences, 67(6), 639–654. https://doi.org/10.1007/s12576-017-0555-7
Levine, B., Klionsky, D. J., Larsson, N.-G., & Masucci, M. G. (2017). Scientific Background for the 2016 Nobel Prize in Physiology or Medicine. Proceedings of the National Academy of Sciences, 114(2), 201–205. https://doi.org/10.1073/pnas.1619876114
Levy, J. M. M., Towers, C. G., & Thorburn, A. (2017). Targeting autophagy in cancer. Nature Reviews Cancer, 17(9), 528–542. https://doi.org/10.1038/nrc.2017.53
Li, Y., Wang, Y., Kim, E., Beemiller, P., Wang, C. Y., Swanson, J., You, M., & Guan, K. L. (2007). Bnip3 mediates the hypoxia-induced inhibition on mammalian target of rapamycin by interacting with Rheb. Journal of Biological Chemistry, 282(49), 35803–35813. https://doi.org/10.1074/jbc.M705231200
Liu, Y., Nguyen, P. T., Wang, X., Zhao, Y., Meacham, C. E., Zou, Z., Bordieanu, B., Johanns, M., Vertommen, D., Wijshake, T., May, H., Xiao, G., Shoji-Kawata, S., Rider, M. H., Morrison, S. J., Mishra, P., & Levine, B. (2020). TLR9 and beclin 1 crosstalk regulates muscle AMPK activation in exercise. Nature, 578(7796), 605–609. https://doi.org/10.1038/s41586-020-1992-7
Lundsgaard, A. M., Fritzen, A. M., & Kiens, B. (2020). The importance of fatty acids as nutrients during post-exercise recovery. Nutrients, 12(2). https://doi.org/10.3390/nu12020280
Marin Bosch, B., Bringard, A., Logrieco, M. G., Lauer, E., Imobersteg, N., Thomas, A., Ferretti, G., Schwartz, S., & Igloi, K. (2020). Effect of acute physical exercise on motor sequence memory. Scientific Reports, 10(1), 1–13. https://doi.org/10.1038/s41598-020-72108-1
Matoba, K., Kotani, T., Tsutsumi, A., Tsuji, T., Mori, T., Noshiro, D., Sugita, Y., Nomura, N., Iwata, S., Ohsumi, Y., Fujimoto, T., Nakatogawa, H., Kikkawa, M., & Noda, N. N. (2020). Atg9 is a lipid scramblase that mediates autophagosomal membrane expansion. Nature Structural and Molecular Biology. https://doi.org/10.1038/s41594-020-00518-w
Matthews, C. E., Shu, X., Jin, F., Dai, Q., Hebert, J. R., Ruan, Z., Gao, Y., & Zheng, W. (2001). Lifetime physical activity and breast cancer risk in the Shanghai Breast Cancer Study. 84, 994–1001.
Mayer, M. P., & Bukau, B. (2005). Hsp70 chaperones: Cellular functions and molecular mechanism. Cellular and Molecular Life Sciences, 62(6), 670–684. https://doi.org/10.1007/s00018-004-4464-6
McConell, G. K., Sjøberg, K. A., Ceutz, F., Gliemann, L., Nyberg, M., Hellsten, Y., Frøsig, C., Kiens, B., Wojtaszewski, J. F. P., & Richter, E. A. (2020). Insulin-induced membrane permeability to glucose in human muscles at rest and following exercise. Journal of Physiology, 598(2), 303–315. https://doi.org/10.1113/JP278600
McEwan, D. G., Popovic, D., Gubas, A., Terawaki, S., Suzuki, H., Stadel, D., Coxon, F. P., MirandadeStegmann, D., Bhogaraju, S., Maddi, K., Kirchof, A., Gatti, E., Helfrich, M. H., Wakatsuki, S., Behrends, C., Pierre, P., & Dikic, I. (2015). PLEKHM1 regulates autophagosome-lysosome fusion through HOPS complex and LC3/GABARAP proteins. Molecular Cell, 57(1), 39–54. https://doi.org/10.1016/j.molcel.2014.11.006
Medbo, J. I., & Tabata, I. (1993). Anaerobic energy release in working muscle during 30 s to 3 min of exhausting bicycling. Journal of Applied Physiology, 75(4), 1654–1660. https://doi.org/10.1152/jappl.1993.75.4.1654
Mhatre V. Ho and Kelsey C. Martin, J.-A. L. (2012). Somatic mutations of the Parkinson’s disease–associated gene PARK2 in glioblastoma and other human malignancies. Bone, 23(1), 1–7. https://doi.org/10.1038/ng.491.Somatic
Michelini, L. C., O’Leary, D. S., Raven, P. B., & Nóbrega, A. C. L. (2015). Neural control of circulation and exercise: A translational approach disclosing interactions between central command, arterial baroreflex, and muscle metaboreflex. American Journal of Physiology - Heart and Circulatory Physiology, 309(3), H381–H392. https://doi.org/10.1152/ajpheart.00077.2015
Mijaljica, D., Prescott, M., & Devenish, R. J. (2011). Microautophagy in mammalian cells: RevisitiMicroautophagy in mammalian cells: Revisiting a 40-year-old conundrumng a 40-year-old conundrum. Autophagy, 7(7), 673–682. https://doi.org/10.4161/auto.7.7.14733
Moore, S. C., I-Min Lee, M., Weiderpass, E., Campbell, P. T., Sampson, J. N., Kitahara, C. M., K., S. K., Arem, H., Sesso, H., Gonzalez, Amy Berrington de, P. H., Blair, C. K., Borch, K. B., Boyd, E., Check, D. P., Fournier, A., Freedman, N. D., Gunter, M., Johannson, M., Khaw, K.-T., … Patel, A. V. (2017). Leisure-time physical activity and risk of 26 types of cancer in 1.44 million adults. Physiology & Behavior, 176(10), 139–148. https://doi.org/10.1001/jamainternmed.2016.1548.Leisure-time
Moreira, T. S., Takakura, A. C., Damasceno, R. S., Falquetto, B., Totola, L. T., Sobrinho, C. R., Ragioto, D. T., & Zolezi, F. P. (2011). Central chemoreceptors and neural mechanisms of cardiorespiratory control. Brazilian Journal of Medical and Biological Research, 44(9), 883–889. https://doi.org/10.1590/S0100-879X2011007500094
Morselli, E., Shen, S., Ruckenstuhl, C., Bauer, M. A., Mariño, G., Galluzzi, L., Criollo, A., Michaud, M., Maiuri, M. C., Chano, T., Madeo, F., & Kroemer, G. (2011). p53 inhibits autophagy by interacting with the human ortholog of yeast Atg17, RB1CC1/FIP200. Cell Cycle, 10(16), 2763–2769. https://doi.org/10.4161/cc.10.16.16868
Murphy, R. M., Watt, M. J., & Febbraio, M. A. (2020). Metabolic communication during exercise. Nature Metabolism, 2(9), 805–816. https://doi.org/10.1038/s42255-020-0258-x
Nakatogawa, H. (2020). Mechanisms governing autophagosome biogenesis. Nature Reviews Molecular Cell Biology, 21(8), 439–458. https://doi.org/10.1038/s41580-020-0241-0
Nobrega, A. C. L., O’Leary, D., Silva, B. M., Marongiu, E., Piepoli, M. F., & Crisafulli, A. (2014). Neural regulation of cardiovascular response to exercise: Role of central command and peripheral afferents. BioMed Research International, 2014. https://doi.org/10.1155/2014/478965
Ortega, E., Peters, C., Barriga, C., & Lötzerich, H. (1998). A atividade física reduz o risco de câncer? Revista Brasileira de Medicina Do Esporte, 4(3), 81–86. https://doi.org/10.1590/s1517-86921998000300003
Parolin, M. L., Chesley, A., Matsos, M. P., Spriet, L. L., Jones, N. L., & Heigenhauser, G. J. F. (1999). Regulation of skeletal muscle glycogen phosphorylase and PDH during maximal intermittent exercise. American Journal of Physiology - Endocrinology and Metabolism, 277(5 40-5). https://doi.org/10.1152/ajpendo.1999.277.5.e890
Poulogiannis, G., McIntyre, R. E., Dimitriadi, M., Apps, J. R., Wilson, C. H., Ichimura, K., Luo, F., Cantley, L. C., Wyllie, A. H., Adams, D. J., & Arends, M. J. (2010). PARK2 deletions occur frequently in sporadic colorectal cancer and accelerate adenoma development in Apc mutant mice. Proceedings of the National Academy of Sciences of the United States of America, 107(34), 15145–15150. https://doi.org/10.1073/pnas.1009941107
Qiao, S., Dennis, M., Song, X., Vadysirisack, D. D., Salunke, D., Nash, Z., Yang, Z., Liesa, M., Yoshioka, J., Matsuzawa, S. I., Shirihai, O. S., Lee, R. T., Reed, J. C., & Ellisen, L. W. (2015). A REDD1/TXNIP pro-oxidant complex regulates ATG4B activity to control stress-induced autophagy and sustain exercise capacity. Nature Communications, 6. https://doi.org/10.1038/ncomms8014
Quach, C., Song, Y., Guo, H., Li, S., Maazi, H., Fung, M., Sands, N., O’Connell, D., Restrepo-Vassalli, S., Chai, B., Nemecio, D., Punj, V., Akbari, O., Idos, G. E., Mumenthaler, S. M., Wu, N., Martin, S. E., Hagiya, A., Hicks, J., … Liang, C. (2019). A truncating mutation in the autophagy gene UVRAG drives inflammation and tumorigenesis in mice. Nature Communications, 10(1). https://doi.org/10.1038/s41467-019-13475-w
Richardson, R. S. (2003). Oxygen transport and utilization: An integration of the muscle systems. American Journal of Physiology - Advances in Physiology Education, 27(1–4), 183–191. https://doi.org/10.1152/advan.00038.2003
Rodrigues, A. Z. C., Wang, Z. M., Messi, M. L., & Delbono, O. (2019). Sympathomimetics regulate neuromuscular junction transmission through TRPV1, P/Q- and N-type Ca 2+ channels. Molecular and Cellular Neuroscience, 95(February), 59–70. https://doi.org/10.1016/j.mcn.2019.01.007
Rogov, V., Dötsch, V., Johansen, T., & Kirkin, V. (2014). Interactions between Autophagy Receptors and Ubiquitin-like Proteins Form the Molecular Basis for Selective Autophagy. Molecular Cell, 53(2), 167–178. https://doi.org/10.1016/j.molcel.2013.12.014
Romijn, J. A., Coyle, E. F., Sidossis, L. S., Gastaldelli, A., Horowitz, J. F., Endert, E., & Wolfe, R. R. (1993). Regulation of endogenous fat and carbohydrate metabolism in relation to exercise intensity and duration. American Journal of Physiology - Endocrinology and Metabolism, 265(3 28-3), 380–391. https://doi.org/10.1152/ajpendo.1993.265.3.e380
Rubinsztein, D. C., Codogno, P., & Levine, B. (2012). Autophagy modulation as a potential therapeutic target for diverse diseases. Nature Reviews Drug Discovery, 11(9), 709–730. https://doi.org/10.1038/nrd3802
Russell, R. C., Yuan, H. X., & Guan, K. L. (2014). Autophagy regulation by nutrient signaling. Cell Research, 24(1), 42–57. https://doi.org/10.1038/cr.2013.166
Sahu, R., Kaushik, S., Clement, C. C., Cannizzo, E. S., Scharf, B., Follenzi, A., Potolicchio, I., Nieves, E., Cuervo, A. M., & Santambrogio, L. (2011). Microautophagy of Cytosolic Proteins by Late Endosomes. Developmental Cell, 20(1), 131–139. https://doi.org/10.1016/j.devcel.2010.12.003
Sikorska-Siudek, K., Olȩdzka-Orȩziak, M., & Parzuchowska, B. (2006). Choroba wieńcowa wśród kobiet - Czy istnieje problem płci? Family Medicine and Primary Care Review, 8(3), 1110–1115.
Sureshbabu, A., Ryter, S. W., & Choi, M. E. (2015). Oxidative stress and autophagy: Crucial modulators of kidney injury. Redox Biology, 4, 208–214. https://doi.org/10.1016/j.redox.2015.01.001
Sylow, L., Kleinert, M., Richter, E. A., & Jensen, T. E. (2017). Exercise-stimulated glucose uptake-regulation and implications for glycaemic control. Nature Reviews Endocrinology, 13(3), 133–148. https://doi.org/10.1038/nrendo.2016.162
Takamura, A., Komatsu, M., Hara, T., Sakamoto, A., Kishi, C., Waguri, S., Eishi, Y., Hino, O., Tanaka, K., & Mizushima, N. (2011). Autophagy-deficient mice develop multiple liver tumors. Genes and Development, 25(8), 795–800. https://doi.org/10.1101/gad.2016211
Tsentsevitsky, A. N., Kovyazina, I. V., & Bukharaeva, E. A. (2019). Diverse Effects of Noradrenaline and Adrenaline on the Quantal Secretion of Acetylcholine at the Mouse Neuromuscular Junction. Neuroscience, 423, 162–171. https://doi.org/10.1016/j.neuroscience.2019.10.049
Tumbarello, D. A., Waxse, B. J., Arden, S. D., Bright, N. A., Kendrick-Jones, J., & Buss, F. (2012). Autophagy receptors link myosin VI to autophagosomes to mediate Tom1-dependent autophagosome maturation and fusion with the lysosome. Nature Cell Biology, 14(10), 1024–1035. https://doi.org/10.1038/ncb2589
Uttenweiler, A., Schwarz, H., & Mayer, A. (2005). Microautophagic vacuole invagination requires calmodulin in a Ca 2+-independent function. Journal of Biological Chemistry, 280(39), 33289–33297. https://doi.org/10.1074/jbc.M506086200
Van Loon, L. J. C., Greenhaff, P. L., Constantin-Teodosiu, D., Saris, W. H. M., & Wagenmakers, A. J. M. (2001). The effects of increasing exercise intensity on muscle fuel utilisation in humans. Journal of Physiology, 536(1), 295–304. https://doi.org/10.1111/j.1469-7793.2001.00295.x
Vanzo, R., Bartkova, J., Merchut-Maya, J. M., Hall, A., Bouchal, J., Dyrskjøt, L., Frankel, L. B., Gorgoulis, V., Maya-Mendoza, A., Jäättelä, M., & Bartek, J. (2019). Autophagy role(s) in response to oncogenes and DNA replication stress. Cell Death and Differentiation. https://doi.org/10.1038/s41418-019-0403-9
Wasserman, D. H., Spalding, J. A., Lacy, D. B., Colburn, C. A., Goldstein, R. E., & Cherrington, A. D. (1989). Glucagon is a primary controller of hepatic glycogenolysis and gluconeogenesis during muscular work. American Journal of Physiology - Endocrinology and Metabolism, 257(1). https://doi.org/10.1152/ajpendo.1989.257.1.e108
Wasserman, David H. (2009). Four grams of glucose. American Journal of Physiology - Endocrinology and Metabolism, 296(1), 11–21. https://doi.org/10.1152/ajpendo.90563.2008
Wirth, M., Joachim, J., & Tooze, S. A. (2013). Autophagosome formation-The role of ULK1 and Beclin1-PI3KC3 complexes in setting the stage. Seminars in Cancer Biology, 23(5), 301–309. https://doi.org/10.1016/j.semcancer.2013.05.007
Wu, C. A., Huang, D. Y., & Lin, W. W. (2014). Beclin-1-independent autophagy positively regulates internal ribosomal entry site-dependent translation of hypoxia-inducible factor 1α under nutrient deprivation. Oncotarget, 5(17), 7525–7539. https://doi.org/10.18632/oncotarget.2265
Yue, Z., Jin, S., Yang, C., Levine, A. J., & Heintz, N. (2003). Beclin 1, an autophagy gene essential for early embryonic development, is a haploinsufficient tumor suppressor. Proceedings of the National Academy of Sciences of the United States of America, 100(25), 15077–15082. https://doi.org/10.1073/pnas.2436255100
Zhang, Jiangwei, Kim, J., Alexander, A., Cai, S., Tripathi, D. N., Dere, R., Tee, A. R., Tait-Mulder, J., Di Nardo, A., Han, J. M., Kwiatkowski, E., Dunlop, E. A., Dodd, K. M., Folkerth, R. D., Faust, P. L., Kastan, M. B., Sahin, M., & Walker, C. L. (2013). A tuberous sclerosis complex signalling node at the peroxisome regulates mTORC1 and autophagy in response to ROS. Nature Cell Biology, 15(10), 1186–1196. https://doi.org/10.1038/ncb2822
Zhang, Jianhua. (2015). Teaching the basics of autophagy and mitophagy to redox biologists-Mechanisms and experimental approaches. Redox Biology, 4, 242–259. https://doi.org/10.1016/j.redox.2015.01.003
Zhang, X. D., Qi, L., Wu, J. C., & Qin, Z. H. (2013). DRAM1 Regulates Autophagy Flux through Lysosomes. PLoS ONE, 8(5). https://doi.org/10.1371/journal.pone.0063245
Zhou, F., Wu, Z., Zhao, M., Murtazina, R., Cai, J., Zhang, A., Li, R., Sun, D., Li, W., Zhao, L., Li, Q., Zhu, J., Cong, X., Zhou, Y., Xie, Z., Gyurkovska, V., Li, L., Huang, X., Xue, Y., … Segev, N. (2019). Rab5-dependent autophagosome closure by ESCRT. Journal of Cell Biology, 218(6), 1908–1927. https://doi.org/10.1083/JCB.201811173
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2021 Wesley Gabriel Novaes Botelho; Alcântara Ramos de Assis César; Kádima Nayara Teixeira
This work is licensed under a Creative Commons Attribution 4.0 International License.
Authors who publish with this journal agree to the following terms:
1) Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
2) Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
3) Authors are permitted and encouraged to post their work online (e.g., in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work.
