Acute environmental hypoxia induces LC3 lipidation in a genotype-dependent manner

FASEB Journal

Volumn 28, Issue 2, 2014, Pages 1022-1034

  Masschelein, Evi ^a   Van Thienen, Ruud ^a   D'Hulst, Gommaar ^a   Hespel, Peter ^a   Thomis, Martine ^a   Deldicque, Louise ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

Autophagy; Exercise; Monozygotic twin design; P62

Indexed keywords

HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; INSULIN; MAMMALIAN TARGET OF RAPAMYCIN; MICROTUBULE ASSOCIATED PROTEIN 1; MICROTUBULE ASSOCIATED PROTEIN 1 LIGHT CHAIN 3 TYPE 2; PROTEIN KINASE B; PROTEIN P62; UBIQUITIN; UNCLASSIFIED DRUG; BNIP3 PROTEIN, HUMAN; DDIT4 PROTEIN, HUMAN; FBXO32 PROTEIN, HUMAN; MAP1LC3A PROTEIN, HUMAN; MEMBRANE PROTEIN; MICROTUBULE ASSOCIATED PROTEIN; MUSCLE PROTEIN; ONCOPROTEIN; TRANSCRIPTION FACTOR; UBIQUITIN PROTEIN LIGASE;

ADULT; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; CHEMICAL MODIFICATION; CYCLING; DEPHOSPHORYLATION; DNA SYNTHESIS; ENVIRONMENT; ENZYME PHOSPHORYLATION; GENE EXPRESSION; GENOTYPE; HUMAN; HUMAN EXPERIMENT; HUMAN TISSUE; HYPOXIA; INSULIN BLOOD LEVEL; LIGHT CHAIN; LIPIDATION; MONOZYGOTIC TWINS; MUSCLE BIOPSY; MUSCLE DEVELOPMENT; MUSCLE GROWTH; MUSCLE TISSUE; NORMAL HUMAN; PRIORITY JOURNAL; PROTEIN METABOLISM; REST; SATELLITE CELL; TISSUE OXYGENATION; ANOXIA; EXERCISE; GENETICS; METABOLISM; MONOZYGOTIC TWIN DESIGN; P62; PATHOPHYSIOLOGY; PHYSIOLOGY; TWINS; WESTERN BLOTTING; YOUNG ADULT;

AUTOPHAGY; EXERCISE; MONOZYGOTIC TWIN DESIGN; P62;

ADULT; ANOXIA; AUTOPHAGY; BLOTTING, WESTERN; EXERCISE; GENOTYPE; HUMANS; MEMBRANE PROTEINS; MICROTUBULE-ASSOCIATED PROTEINS; MUSCLE PROTEINS; PROTO-ONCOGENE PROTEINS; SKP CULLIN F-BOX PROTEIN LIGASES; TRANSCRIPTION FACTORS; YOUNG ADULT;

EID: 84897034750     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.13-239863     Document Type: Article

References (65)

1. Grocott, M. P., Martin, D. S., Levett, D. Z., McMorrow, R., Windsor, J., and Montgomery, H. E. (2009) Arterial blood gases and oxygen content in climbers on Mount Everest. N. Engl. J. Med. 360, 140-149
2. Baldi, S., Aquilani, R., Pinna, G. D., Poggi, P., De Martini, A., and Bruschi, C. (2010) Fat-free mass change after nutritional rehabilitation in weight losing COPD: role of insulin, C-reactive protein and tissue hypoxia. Int. J. Chron. Obstruct. Pulmon. Dis. 5, 29-39
3. Garvey, J. F., Taylor, C. T., and McNicholas, W. T. (2009) Cardiovascular disease in obstructive sleep apnoea syndrome: the role of intermittent hypoxia and inflammation. Eur. Respir. J. 33, 1195-1205
4. Grocott, M., Montgomery, H., and Vercueil, A. (2007) Highaltitude physiology and pathophysiology: implications and relevance for intensive care medicine. Crit. Care 11, 203
5. Beall, C. M. (2007) Two routes to functional adaptation: Tibetan and Andean high-altitude natives. Proc. Natl. Acad. Sci. U. S. A. 104(Suppl. 1), 8655-8660
6. Beall, C. M. (2006) Andean, Tibetan, and Ethiopian patterns of adaptation to high-altitude hypoxia. Integr. Comp. Biol. 46, 18-24
7. Simonson, T. S., Yang, Y., Huff, C. D., Yun, H., Qin, G., Witherspoon, D. J., Bai, Z., Lorenzo, F. R., Xing, J., Jorde, L. B., Prchal, J. T., and Ge, R. (2010) Genetic evidence for highaltitude adaptation in Tibet. Science 329, 72-75
8. Bigham, A., Bauchet, M., Pinto, D., Mao, X., Akey, J. M., Mei, R., Scherer, S. W., Julian, C. G., Wilson, M. J., Lopez, H. D., Brutsaert, T., Parra, E. J., Moore, L. G., and Shriver, M. D. (2010) Identifying signatures of natural selection in Tibetan and Andean populations using dense genome scan data. PLoS Genet. 6, e1001116
9. Grocott, M., and Montgomery, H. (2008) Genetophysiology: using genetic strategies to explore hypoxic adaptation. High Alt. Med. Biol. 9, 123-129
10. Martin, D. S., Levett, D. Z., Grocott, M. P., and Montgomery, H. E. (2010) Variation in human performance in the hypoxic mountain environment. Exp. Physiol. 95, 463-470
11. Koumenis, C., and Wouters, B. G. (2006) "Translating" tumor hypoxia: unfolded protein response (UPR)-dependent and UPR-independent pathways. Mol. Cancer Res. 4, 423-436
12. Liu, L., Cash, T. P., Jones, R. G., Keith, B., Thompson, C. B., and Simon, M. C. (2006) Hypoxia-induced energy stress regulates mRNA translation and cell growth. Mol. Cell 21, 521-531
13. Brugarolas, J., Lei, K., Hurley, R. L., Manning, B. D., Reiling, J. H., Hafen, E., Witters, L. A., Ellisen, L. W., and Kaelin, W. G., Jr. (2004) Regulation of mTOR function in response to hypoxia by REDD1 and the TSC1/TSC2 tumor suppressor complex. Genes Dev. 18, 2893-2904
14. Chaudhary, P., Suryakumar, G., Prasad, R., Singh, S. N., Ali, S., and Ilavazhagan, G. (2012) Chronic hypobaric hypoxia mediated skeletal muscle atrophy: role of ubiquitin-proteasome pathway and calpains. Mol. Cell. Biochem. 364, 101-113
15. Chaillou, T., Koulmann, N., Simler, N., Meunier, A., Serrurier, B., Chapot, R., Peinnequin, A., Beaudry, M., and Bigard, X. (2012) Hypoxia transiently affects skeletal muscle hypertrophy in a functional overload model. Am. J. Physiol. 302, R643-R654
16. Chaillou, T., Koulmann, N., Meunier, A., Malgoyre, A., Serrurier, B., Beaudry, M., and Bigard, X. (2013) Effect of hypoxia exposure on the phenotypic adaptation in remodelling skeletal muscle submitted to functional overload. [E-pub ahead of print] Acta Physiol. (Oxf.) doi:10.1111/apha.12110
17. Favier, F. B., Costes, F., Defour, A., Bonnefoy, R., Lefai, E., Bauge, S., Peinnequin, A., Benoit, H., and Freyssenet, D. (2010) Downregulation of Akt/mammalian target of rapamycin pathway in skeletal muscle is associated with increased REDD1 expression in response to chronic hypoxia. Am. J. Physiol. 298, R1659-R1666
18. Bodine, S. C., Latres, E., Baumhueter, S., Lai, V. K., Nunez, L., Clarke, B. A., Poueymirou, W. T., Panaro, F. J., Na, E., Dharmarajan, K., Pan, Z. Q., Valenzuela, D. M., DeChiara, T. M., Stitt, T. N., Yancopoulos, G. D., and Glass, D. J. (2001) Identification of ubiquitin ligases required for skeletal muscle atrophy. Science 294, 1704-1708
19. Bonaldo, P., and Sandri, M. (2013) Cellular and molecular mechanisms of muscle atrophy. Dis. Models Mech. 6, 25-39
20. Tanida, I. (2011) Autophagosome formation and molecular mechanism of autophagy. Antioxid. Redox Signal. 14, 2201-2214
21. Ichimura, Y., and Komatsu, M. (2010) Selective degradation of p62 by autophagy. Semin. Immunopathol. 32, 431-436
22. Martinelli, M., Winterhalder, R., Cerretelli, P., Howald, H., and Hoppeler, H. (1990) Muscle lipofuscin content and satellite cell volume is increased after high altitude exposure in humans. Experientia 46, 672-676
23. Westerterp-Plantenga, M. S., Westerterp, K. R., Rubbens, M., Verwegen, C. R., Richelet, J. P., and Gardette, B. (1999) Appetite at "high altitude" [Operation Everest III (Comex-'97)]: a simulated ascent of Mount Everest. J. Appl. Physiol. 87, 391-399
24. Nicholson, A. N., Smith, P. A., Stone, B. M., Bradwell, A. R., and Coote, J. H. (1988) Altitude insomnia: studies during an expedition to the Himalayas. Sleep 11, 354-361
25. D'Hulst, G., Jamart, C., Van Thienen, R., Hespel, P., Francaux, M., and Deldicque, L. (2013) Effect of acute environmental hypoxia on protein metabolism in human skeletal muscle. Acta Physiol. (Oxf.) 208, 251-264
26. Ferrari, M., Mottola, L., and Quaresima, V. (2004) Principles, techniques, and limitations of near infrared spectroscopy. Can. J. Appl. Physiol. 29, 463-487
27. Deldicque, L., De Bock, K., Maris, M., Ramaekers, M., Nielens, H., Francaux, M., and Hespel, P. (2010) Increased p70s6k phosphorylation during intake of a protein-carbohydrate drink following resistance exercise in the fasted state. Eur. J. Appl. Physiol. 108, 791-800
28. Jamart, C., Raymackers, J. M., Li, A. G., Deldicque, L., and Francaux, M. (2011) Prevention of muscle disuse atrophy by MG132 proteasome inhibitor. Muscle Nerve 43, 708-716
29. Vincent, B., Windelinckx, A., Nielens, H., Ramaekers, M., Van Leemputte, M., Hespel, P., and Thomis, M. A. (2010) Protective role of actinin-3 in the response to an acute eccentric exercise bout. J. Appl. Physiol. 109, 564-573
30. Vandesompele, J., De Preter, K., Pattyn, F., Poppe, B., Van Roy, N., De Paepe, A., and Speleman, F. (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 3, RESEARCH0034
31. Bouchard, C., Perusse, L., and Leblanc, C. (1990) Using MZ twins in experimental research to test for the presence of a genotype-environment interaction effect. Acta Genet. Med. Gemellol. (Roma) 39:85-89
32. Koumenis, C., Bi, M., Ye, J., Feldman, D., and Koong, A. C. (2007) Hypoxia and the unfolded protein response. Methods Enzymol. 435, 275-293
33. Barth, S., Glick, D., and Macleod, K. F. (2010) Autophagy: assays and artifacts. J. Pathol. 221, 117-124
34. Bjorkoy, G., Lamark, T., Pankiv, S., Overvatn, A., Brech, A., and Johansen, T. (2009) Monitoring autophagic degradation of p62/SQSTM1. Methods Enzymol. 452, 181-197
35. Zhang, J., and Ney, P. A. (2009) Role of BNIP3 and NIX in cell death, autophagy, and mitophagy. Cell Death Differ. 16, 939-946
36. Stitt, T. N., Drujan, D., Clarke, B. A., Panaro, F., Timofeyva, Y., Kline, W. O., Gonzalez, M., Yancopoulos, G. D., and Glass, D. J. (2004) The IGF-1/PI3K/Akt pathway prevents expression of muscle atrophy-induced ubiquitin ligases by inhibiting FOXO transcription factors. Mol. Cell 14, 395-403
37. Baserga, R. (1991) Growth regulation of the PCNA gene. J. Cell Sci. 98(Pt. 4), 433-436
38. Hoppeler, H., Kleinert, E., Schlegel, C., Claassen, H., Howald, H., Kayar, S. R., and Cerretelli, P. (1990) Morphological adaptations of human skeletal muscle to chronic hypoxia. Int. J. Sports Med. 11(Suppl. 1):S3-S9
39. Hoppeler, H., and Vogt, M. (2001) Muscle tissue adaptations to hypoxia. J. Exp. Biol. 204, 3133-3139
40. Schols, A. M., Broekhuizen, R., Weling-Scheepers, C. A., and Wouters, E. F. (2005) Body composition and mortality in chronic obstructive pulmonary disease. Am. J. Clin. Nutr. 82, 53-59
41. Giordano, F. J. (2005) Oxygen, oxidative stress, hypoxia, and heart failure. J. Clin. Invest. 115, 500-508
42. Klionsky, D. J., Abeliovich, H., Agostinis, P., Agrawal, D. K., Aliev, G., Askew, D. S., Baba, M., Baehrecke, E. H., Bahr, B. A., Ballabio, A., Bamber, B. A., Bassham, D. C., Bergamini, E., Bi, X., Biard-Piechaczyk, M., Blum, J. S., Bredesen, D. E., Brodsky, J. L., Brumell, J. H., Brunk, U. T., Bursch, W., Camougrand, N., Cebollero, E., Cecconi, F., Chen, Y., Chin, L. S., Choi, A., Chu, C. T., Chung, J., Clarke, P. G., Clark, R. S., Clarke, S. G., Clave, C., Cleveland, J. L., Codogno, P., Colombo, M. I., Coto-Montes, A., Cregg, J. M., Cuervo, A. M., Debnath, J., Demarchi, F., Dennis, P. B., Dennis, P. A., Deretic, V., Devenish, R. J., Di, S. F., Dice, J. F., Difiglia, M., Dinesh-Kumar, S., Distelhorst, C. W., Djavaheri-Mergny, M., Dorsey, F. C., Droge, W., Dron, M., Dunn, W. A., Jr., Duszenko, M., Eissa, N. T., Elazar, Z., Esclatine, A., Eskelinen, E. L., Fesus, L., Finley, K. D., Fuentes, J. M., Fueyo, J., Fujisaki, K., Galliot, B., Gao, F. B., Gewirtz, D. A., Gibson, S. B., Gohla, A., Goldberg, A. L., Gonzalez, R., Gonzalez-Estevez, C., Gorski, S., Gottlieb, R. A., Haussinger, D., He, Y. W., Heidenreich, K., Hill, J. A., Hoyer-Hansen, M., Hu, X., Huang, W. P., Iwasaki, A., Jaattela, M., Jackson, W. T., Jiang, X., Jin, S., Johansen, T., Jung, J. U., Kadowaki, M., Kang, C., Kelekar, A., Kessel, D. H., Kiel, J. A., Kim, H. P., Kimchi, A., Kinsella, T. J., Kiselyov, K., Kitamoto, K., Knecht, E., Komatsu, M., Kominami, E., Kondo, S., Kovacs, A. L., Kroemer, G., Kuan, C. Y., Kumar, R., Kundu, M., Landry, J., Laporte, M., Le, W., Lei, H. Y., Lenardo, M. J., Levine, B., Lieberman, A., Lim, K. L., Lin, F. C., Liou, W., Liu, L. F., Lopez-Berestein, G., Lopez-Otin, C., Lu, B., Macleod, K. F., Malorni, W., Martinet, W., Matsuoka, K., Mautner, J., Meijer, A. J., Melendez, A., Michels, P., Miotto, G., Mistiaen, W. P., Mizushima, N., Mograbi, B., Monastyrska, I., Moore, M. N., Moreira, P. I., Moriyasu, Y., Motyl, T., Munz, C., Murphy, L. O., Naqvi, N. I., Neufeld, T. P., Nishino, I., Nixon, R. A., Noda, T., Nurnberg, B., Ogawa, M., Oleinick, N. L., Olsen, L. J., Ozpolat, B., Paglin, S., Palmer, G. E., Papassideri, I., Parkes, M., Perlmutter, D. H., Perry, G., Piacentini, M., Pinkas-Kramarski, R., Prescott, M., Proikas-Cezanne, T., Raben, N., Rami, A., Reggiori, F., Rohrer, B., Rubinsztein, D. C., Ryan, K. M., Sadoshima, J., Sakagami, H., Sakai, Y., Sandri, M., Sasakawa, C., Sass, M., Schneider, C., Seglen, P. O., Seleverstov, O., Settleman, J., Shacka, J. J., Shapiro, I. M., Sibirny, A., Silva-Zacarin, E. C., Simon, H. U., Simone, C., Simonsen, A., Smith, M. A., Spanel- Borowski, K., Srinivas, V., Steeves, M., Stenmark, H., Stromhaug, P. E., Subauste, C. S., Sugimoto, S., Sulzer, D., Suzuki, T., Swanson, M. S., Tabas, I., Takeshita, F., Talbot, N. J., Talloczy, Z., Tanaka, K., Tanaka, K., TanidaI., Taylor, G. S., Taylor, J. P., Terman, A., Tettamanti, G., Thompson, C. B., Thumm, M., Tolkovsky, A. M., Tooze, S. A., Truant, R., Tumanovska, L. V., Uchiyama, Y., Ueno, T., Uzcategui, N. L., van der Klei, I., Vaquero, E. C., Vellai, T., Vogel, M. W., Wang, H. G., Webster, P., Wiley, J. W., Xi, Z., Xiao, G., Yahalom, J., Yang, J. M., Yap, G., Yin, X. M., Yoshimori, T., Yu, L., Yue, Z., Yuzaki, M., Zabirnyk, O., Zheng, X., Zhu, X., and Deter, R. L. (2008) Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy 4, 151-175
43. Jamart, C., Benoit, N., Raymackers, J. M., Kim, H. J., Kim, C. K., and Francaux, M. (2012) Autophagy-related and autophagyregulatory genes are induced in human muscle after ultraendurance exercise. Eur. J. Appl. Physiol. 112, 3173-3177
44. Mammucari, C., Milan, G., Romanello, V., Masiero, E., Rudolf, R., Del, P. P., Burden, S. J., Di, L. R., Sandri, C., Zhao, J., Goldberg, A. L., Schiaffino, S., and Sandri, M. (2007) FoxO3 controls autophagy in skeletal muscle in vivo. Cell Metab. 6, 458-471
45. Chaudhary, P., Suryakumar, G., Prasad, R., Singh, S. N., Ali, S., and Ilavazhagan, G. (2012) Effect of acute hypobaric hypoxia on skeletal muscle protein turnover. Al Ameen J. Med. Sci. 5, 355-361
46. Zhao, J., Brault, J. J., Schild, A., Cao, P., Sandri, M., Schiaffino, S., Lecker, S. H., and Goldberg, A. L. (2007) FoxO3 coordinately activates protein degradation by the autophagic/lysosomal and proteasomal pathways in atrophying muscle cells. Cell Metab. 6, 472-483
47. Van Der Heide, L. P., Hoekman, M. F., and Smidt, M. P. (2004) The ins and outs of FoxO shuttling: mechanisms of FoxO translocation and transcriptional regulation. Biochem. J. 380, 297-309
48. Lacey, R. J., Cable, H. C., James, R. F., London, N. J., Scarpello, J. H., and Morgan, N. G. (1993) Concentration-dependent effects of adrenaline on the profile of insulin secretion from isolated human islets of Langerhans. J. Endocrinol. 138, 555-563
49. Arsham, A. M., Howell, J. J., and Simon, M. C. (2003) A novel hypoxia-inducible factor-independent hypoxic response regulating mammalian target of rapamycin and its targets. J. Biol. Chem. 278, 29655-29660
50. Preedy, V. R., Smith, D. M., and Sugden, P. H. (1985) The effects of 6 hours of hypoxia on protein synthesis in rat tissues in vivo and in vitro. Biochem. J. 228, 179-185
51. Preedy, V. R., and Sugden, P. H. (1989) The effects of fasting or hypoxia on rates of protein synthesis in vivo in subcellular fractions of rat heart and gastrocnemius muscle. Biochem. J. 257, 519-527
52. Vigano, A., Ripamonti, M., De Palma, S., Capitanio, D., Vasso, M., Wait, R., Lundby, C., Cerretelli, P., and Gelfi, C. (2008) Proteins modulation in human skeletal muscle in the early phase of adaptation to hypobaric hypoxia. Proteomics 8, 4668-4679
53. Rennie, M. J., Babij, P., Sutton, J. R., Tonkins, W. J., Read, W. W., Ford, C., and Halliday, D. (1983) Effects of acute hypoxia on forearm leucine metabolism. Prog. Clin. Biol. Res. 136, 317-323
54. Etheridge, T., Atherton, P. J., Wilkinson, D., Selby, A., Rankin, D., Webborn, N., Smith, K., and Watt, P. W. (2011) Effects of hypoxia on muscle protein synthesis and anabolic signaling at rest and in response to acute resistance exercise. Am. J. Physiol. Endocrinol. Metab. 301, E697-E702
55. Imoberdorf, R., Garlick, P. J., McNurlan, M. A., Casella, G. A., Marini, J. C., Turgay, M., Bartsch, P., and Ballmer, P. E. (2006) Skeletal muscle protein synthesis after active or passive ascent to high altitude. Med. Sci. Sports Exerc. 38, 1082-1087
56. Egan, B., Carson, B. P., Garcia-Roves, P. M., Chibalin, A. V., Sarsfield, F. M., Barron, N., McCaffrey, N., Moyna, N. M., Zierath, J. R., and O'Gorman, D. J. (2010) Exercise intensitydependent regulation of peroxisome proliferator-activated receptor coactivator-1 mRNA abundance is associated with differential activation of upstream signalling kinases in human skeletal muscle. J. Physiol. 588, 1779-1790
57. Sriwijitkamol, A., Coletta, D. K., Wajcberg, E., Balbontin, G. B., Reyna, S. M., Barrientes, J., Eagan, P. A., Jenkinson, C. P., Cersosimo, E., DeFronzo, R. A., Sakamoto, K., and Musi, N. (2007) Effect of acute exercise on AMPK signaling in skeletal muscle of subjects with type 2 diabetes: a time-course and dose-response study. Diabetes 56, 836-848
58. Amirouche, A., Durieux, A. C., Banzet, S., Koulmann, N., Bonnefoy, R., Mouret, C., Bigard, X., Peinnequin, A., and Freyssenet, D. (2009) Down-regulation of Akt/mammalian target of rapamycin signaling pathway in response to myostatin overexpression in skeletal muscle. Endocrinology 150, 286-294
59. Hayot, M., Rodriguez, J., Vernus, B., Carnac, G., Jean, E., Allen, D., Goret, L., Obert, P., Candau, R., and Bonnieu, A. (2011) Myostatin up-regulation is associated with the skeletal muscle response to hypoxic stimuli. Mol. Cell. Endocrinol. 332, 38-47
60. Thomis, M. A., Beunen, G. P., Maes, H. H., Blimkie, C. J., Van, L. M., Claessens, A. L., Marchal, G., Willems, E., and Vlietinck, R. F. (1998) Strength training: importance of genetic factors. Med. Sci. Sports Exerc. 30, 724-731
61. Schiaffino, S., Dyar, K. A., Ciciliot, S., Blaauw, B., and Sandri, M. (2013) Mechanisms regulating skeletal muscle growth and atrophy. FEBS J. 280, 4294-4314
62. Ciciliot, S., and Schiaffino, S. (2010) Regeneration of mammalian skeletal muscle. Basic mechanisms and clinical implications. Curr. Pharm. Des. 16, 906-914
63. Macaluso, F., and Myburgh, K. H. (2012) Current evidence that exercise can increase the number of adult stem cells. J. Muscle Res. Cell Motil. 33, 187-198
64. Csete, M., Walikonis, J., Slawny, N., Wei, Y., Korsnes, S., Doyle, J. C., and Wold, B. (2001) Oxygen-mediated regulation of skeletal muscle satellite cell proliferation and adipogenesis in culture. J. Cell. Physiol. 189, 189-196
65. Koning, M., Werker, P. M., van Luyn, M. J., and Harmsen, M. C. (2011) Hypoxia promotes proliferation of human myogenic satellite cells: a potential benefactor in tissue engineering of skeletal muscle. Tissue Eng. A 17, 1747-1758