Angiotensin II inhibits satellite cell proliferation and prevents skeletal muscle regeneration

Journal of Biological Chemistry

Volumn 288, Issue 33, 2013, Pages 23823-23832

  Yoshida, Tadashi ^a   Galvez, Sarah ^a   Tiwari, Sumit ^a   Rezk, Bashir M ^a   Semprun Prieto, Laura ^a   Higashi, Yusuke ^a   Sukhanov, Sergiy ^a   Yablonka Reuveni, Zipora ^b   Delafontaine, Patrice ^a  

^a TULANE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOTENSIN II; SATELLITE CELLS; SKELETAL MUSCLE;

CELL PROLIFERATION; NEURONS;

MUSCLE;

ANGIOTENSIN 1 RECEPTOR; ANGIOTENSIN II; MYOD PROTEIN; MYOGENIN; NOTCH RECEPTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL PROLIFERATION; CONTROLLED STUDY; FLUORESCENCE ACTIVATED CELL SORTING; MALE; MOLECULAR DYNAMICS; MOUSE; MUSCLE REGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SATELLITE CELL; SIGNAL TRANSDUCTION; SKELETAL MUSCLE;

ANGIOTENSIN II; CACHEXIA; MYOCARDIAL INFARCTION; REGENERATION; SATELLITE CELLS; SKELETAL MUSCLE; STEM CELLS;

ANGIOTENSIN II; ANIMALS; CELL COUNT; CELL CYCLE PROTEINS; CELL PROLIFERATION; DISEASE MODELS, ANIMAL; HEART FAILURE; MICE; MUSCLE, SKELETAL; RECEPTOR, ANGIOTENSIN, TYPE 1; RECEPTORS, NOTCH; REGENERATION; SATELLITE CELLS, SKELETAL MUSCLE; SIGNAL TRANSDUCTION; WASTING SYNDROME;

EID: 84882367798     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.449074     Document Type: Article

References (57)

1. Tan, B. H., and Fearon, K. C. (2008) Cachexia. Prevalence and impact in medicine. Curr. Opin. Clin. Nutr. Metab. Care 11, 400-407
2. Evans, W. J., Morley, J. E., Argilés, J., Bales, C., Baracos, V., Guttridge, D., Jatoi, A., Kalantar-Zadeh, K., Lochs, H., Mantovani, G., Marks, D., Mitch, W. E., Muscaritoli, M., Najand, A., Ponikowski, P., Rossi Fanelli, F., Schambelan, M., Schols, A., Schuster, M., Thomas, D., Wolfe, R., and Anker, S. D. (2008) Cachexia. A new definition. Clin. Nutr. 27, 793-799
3. Anker, S. D., Negassa, A., Coats, A. J., Afzal, R., Poole-Wilson, P. A., Cohn, J. N., and Yusuf, S. (2003) Prognostic importance of weight loss in chronic heart failure and the effect of treatment with angiotensin-converting- enzyme inhibitors. An observational study. Lancet 361, 1077-1083
4. Sanders, P. M., Russell, S. T., and Tisdale, M. J. (2005) Angiotensin II directly induces muscle protein catabolism through the ubiquitin-proteasome proteolytic pathway and may play a role in cancer cachexia. Br. J. Cancer 93, 425-434
5. Shrikrishna, D., Astin, R., Kemp, P. R., and Hopkinson, N. S. (2012) Reninangiotensin system blockade. A novel therapeutic approach in chronic obstructive pulmonary disease. Clin. Sci. 123, 487-498
6. Brink, M., Wellen, J., and Delafontaine, P. (1996) Angiotensin II causes weight loss and decreases circulating insulin-like growth factor I in rats through a pressor-independent mechanism. J. Clin. Invest. 97, 2509-2516
7. Brink, M., Price, S. R., Chrast, J., Bailey, J. L., Anwar, A., Mitch, W. E., and Delafontaine, P. (2001) Angiotensin II induces skeletal muscle wasting through enhanced protein degradation and down-regulates autocrine insulin-like growth factor I. Endocrinology 142, 1489-1496
8. Song, Y.-H., Li, Y., Du, J., Mitch, W. E., Rosenthal, N., and Delafontaine, P. (2005) Muscle-specific expression of IGF-1 blocks angiotensin II-induced skeletal muscle wasting. J. Clin. Invest. 115, 451-458
9. Yoshida, T., Semprun-Prieto, L., Sukhanov, S., and Delafontaine, P. (2010) IGF-1 prevents ANG II-induced skeletal muscle atrophy via Akt-and Foxo-dependent inhibition of the ubiquitin ligase atrogin-1 expression. Am. J. Physiol. Heart Circ. Physiol. 298, H1565-70
10. Yoshida, T., Semprun-Prieto, L., Wainford, R. D., Sukhanov, S., Kapusta, D. R., and Delafontaine, P. (2012) Angiotensin II reduces food intake by altering orexigenic neuropeptide expression in the mouse hypothalamus. Endocrinology 153, 1411-1420
11. Semprun-Prieto, L. C., Sukhanov, S., Yoshida, T., Rezk, B. M., Gonzalez-Villalobos, R. A., Vaughn, C., Michael Tabony, A., and Delafontaine, P. (2011) Angiotensin II induced catabolic effect and muscle atrophy are redox dependent. Biochem. Biophys. Res. Comm. 409, 217-221
12. Tabony, A. M., Yoshida, T., Galvez, S., Higashi, Y., Sukhanov, S., Chandrasekar, B., Mitch, W. E., and Delafontaine, P. (2011) Angiotensin II upregulates protein phosphatase 2C+ and inhibits AMP-activated protein kinase signaling and energy balance leading to skeletal muscle wasting. Hypertension 58, 643-649
13. Rezk, B. M., Yoshida, T., Semprun-Prieto, L., Higashi, Y., Sukhanov, S., and Delafontaine, P. (2012) Angiotensin II infusion induces marked diaphragmatic skeletal muscle atrophy. PLoS ONE 7, e30276
14. Yan, Z., Choi, S., Liu, X., Zhang, M., Schageman, J. J., Lee, S. Y., Hart, R., Lin, L., Thurmond, F. A., and Williams, R. S. (2003) Highly coordinated gene regulation in mouse skeletal muscle regeneration. J. Biol. Chem. 278, 8826-8836
15. Yablonka-Reuveni, Z., and Day, K. (2011) Regenerating the Heart: Stem Cells and the Cardiovascular System, pp. 173-200, Springer, New York
16. McCroskery, S., Thomas, M., Maxwell, L., Sharma, M., and Kambadur, R. (2003) Myostatin negatively regulates satellite cell activation and self-renewal. J. Cell Biol. 162, 1135-1147
17. Sacco, A., Doyonnas, R., Kraft, P., Vitorovic, S., and Blau, H. M. (2008) Self-renewal and expansion of single transplanted muscle stem cells. Nature 456, 502-506
18. Shefer, G., Van de Mark, D. P., Richardson, J. B., and Yablonka-Reuveni, Z. (2006) Satellite-cell pool size does matter. Defining the myogenic potency of aging skeletal muscle. Dev. Biol. 294, 50-66
19. Chakkalakal, J. V., Jones, K. M., Basson, M. A., and Brack, A. S. (2012) The aged niche disrupts muscle stem cell quiescence. Nature 490, 355-360
20. Carlson, M. E., Hsu, M., and Conboy, I. M. (2008) Imbalance between pSmad3 and Notch induces CDK inhibitors in old muscle stem cells. Nature 454, 528-532
21. Cohn, R. D., van Erp, C., Habashi, J. P., Soleimani, A. A., Klein, E. C., Lisi, M. T., Gamradt, M., ap Rhys, C. M., Holm, T. M., Loeys, B. L., Ramirez, F., Judge, D. P., Ward, C. W., and Dietz, H. C. (2007) Angiotensin II type 1 receptor blockade attenuates TGF-induced failure of muscle regeneration in multiple myopathic states. Nat. Med. 13, 204-210
22. Zhang, L., Du, J., Hu, Z., Han, G., Delafontaine, P., Garcia, G., and Mitch, W. E. (2009) IL-6 and serum amyloid A synergy mediates angiotensin II-induced muscle wasting. J. Am. Soc. Nephrol. 20, 604-612
23. Ieronimakis, N., Balasundaram, G., and Reyes, M. (2008) Direct isolation, culture and transplant of mouse skeletal muscle derived endothelial cells with angiogenic potential. PLoS ONE 3, e0001753
24. Conboy, I. M., Conboy, M. J., Smythe, G. M., and Rando, T. A. (2003) Notch-mediated restoration of regenerative potential to aged muscle. Science 302, 1575-1577
25. Conboy, I. M., and Rando, T. A. (2002) The regulation of Notch signaling controls satellite cell activation and cell fate determination in postnatal myogenesis. Dev. Cell 3, 397-409
26. Michael, L. H., Entman, M. L., Hartley, C. J., Youker, K. A., Zhu, J., Hall, S. R., Hawkins, H. K., Berens, K., and Ballantyne, C. M. (1995) Myocardial ischemia and reperfusion.Amurine model. Am. J. Physiol. 269, H2147-54
27. Day, K., Shefer, G., Shearer, A., and Yablonka-Reuveni, Z. (2010) The depletion of skeletal muscle satellite cells with age is concomitant with reduced capacity of single progenitors to produce reserve progeny. Dev. Biol. 340, 330-343
28. Irintchev, A., Zeschnigk, M., Starzinski-Powitz, A., and Wernig, A. (1994) Expression pattern of M-cadherin in normal, denervated, and regenerating mouse muscles. Dev. Dyn. 199, 326-337
29. Lütken, S. C., Kim, S. W., Jonassen, T., Marples, D., Knepper, M. A., Kwon, T.-H., Frøkiaer, J., and Nielsen, S. (2009) Changes of renal AQP2, ENaC, and NHE3 in experimentally induced heart failure. Response to angiotensin II AT1 receptor blockade. Am. J. Physiol. Renal Physiol. 297, F1678-88
30. Jin, D., Takai, S., Sakaguchi, M., Okamoto, Y., Muramatsu, M., and Miyazaki, M. (2004) An antiarrhythmic effect of a chymase inhibitor after myocardial infarction. J. Pharmacol. Exp. Ther. 309, 490-497
31. Schulze, P. C., Fang, J., Kassik, K. A., Gannon, J., Cupesi, M., MacGillivray, C., Lee, R. T., and Rosenthal, N. (2005) Transgenic overexpression of locally acting insulin-like growth factor-1 inhibits ubiquitin-mediated muscle atrophy in chronic left-ventricular dysfunction. Circ. Res. 97, 418-426
32. Segersvärd, H., Lakkisto, P., Forsten, H., Immonen, K., Kosonen, R., Palojoki, E., Kankuri, E., Harjula, A., Laine, M., and Tikkanen, I. (2013) Effects of angiotensin II blockade on cardiomyocyte regeneration after myocardial infarction in rats. J. Renin Angiotensin Aldosterone Syst., in press
33. Sun, C.-K., Chang, L.-T., Sheu, J.-J., Wang, C.-Y., Youssef, A. A., Wu, C.-J., Chua, S., and Yip, H.-K. (2007) Losartan preserves integrity of cardiac gap junctions and PGC-1 gene expression and prevents cellular apoptosis in remote area of left ventricular myocardium following acute myocardial infarction. Int. Heart J. 48, 533-546
34. Ararat, E., and Brozovich, F. V. (2009) Losartan decreases p42/44 MAPK signaling and preserves LZ+ MYPT1 expression. PLoS ONE 4, e5144
35. Pourdjabbar, A., Parker, T. G., Nguyen, Q. T., Desjardins, J.-F., Lapointe, N., Tsoporis, J. N., and Rouleau, J.-L. (2005) Effects of pre-, peri-, and postmyocardial infarction treatment with losartan in rats. Effect of dose on survival, ventricular arrhythmias, function, and remodeling. Am. J. Physiol. Heart Circ. Physiol. 288, H1997-2005
36. Johnston, A. P., Baker, J., Bellamy, L. M., McKay, B. R., De Lisio, M., and Parise, G. (2010) Regulation of muscle satellite cell activation and chemotaxis by angiotensin II. PLoS ONE 5, e15212
37. Gordon, S. E., Davis, B. S., Carlson, C. J., and Booth, F. W. (2001) ANG II is required for optimal overload-induced skeletal muscle hypertrophy. Am. J. Physiol. Endocrinol Metab 280, E150-9
38. Westerkamp, C. M., and Gordon, S. E. (2005) Angiotensin-converting enzyme inhibition attenuates myonuclear addition in overloaded slowtwitch skeletal muscle. Am. J. Physiol. Regul. Integr. Comp. Physiol. 289, R1223-31
39. Skurk, T., van Harmelen, V., and Hauner, H. (2004) Angiotensin II stimulates the release of interleukin-6 and interleukin-8 from cultured human adipocytes by activation of NFκB. Arterioscler. Thromb. Vasc. Biol. 24, 1199-1203
40. Serrano, A. L., Baeza-Raja, B., Perdiguero, E., Jardí, M., and Muñoz-Cánoves, P. (2008) Interleukin-6 is an essential regulator of satellite cellmediated skeletal muscle hypertrophy. Cell Metab. 7, 33-44
41. Shefer, G., Rauner, G., Yablonka-Reuveni, Z., and Benayahu, D. (2010) Reduced satellite cell numbers and myogenic capacity in aging can be alleviated by endurance exercise. PLoS ONE 5, e13307
42. Ten Broek, R. W., Grefte, S., and Von den Hoff, J. W. (2010) Regulatory factors and cell populations involved in skeletal muscle regeneration. J. Cell. Physiol. 224, 7-16
43. Goetsch, S. C., Hawke, T. J., Gallardo, T. D., Richardson, J. A., and Garry, D. J. (2003) Transcriptional profiling and regulation of the extracellular matrix during muscle regeneration. Physiol. Genomics 14, 261-271
44. Smith, C. A., Stauber, F., Waters, C., Alway, S. E., and Stauber, W. T. (2007) Transforming growth factor-following skeletal muscle strain injury in rats. J. Appl. Physiol. 102, 755-761
45. Vaidya, T. B., Rhodes, S. J., Taparowsky, E. J., and Konieczny, S. F. (1989) Fibroblast growth factor and transforming growth factor repress transcription of the myogenic regulatory gene MyoD1. Mol. Cell Biol. 9, 3576-3579
46. Kuang, S., Gillespie, M. A., and Rudnicki, M. A. (2008) Niche regulation of muscle satellite cell self-renewal and differentiation. Cell Stem Cell 2, 22-31
47. Fyhrquist, F., and Saijonmaa, O. (2008) Renin-angiotensin system revisited. J. Intern. Med. 264, 224-236
48. Gray, S. L., LaCroix, A. Z., Aragaki, A. K., McDermott, M., Cochrane, B. B., Kooperberg, C. L., Murray, A. M., Rodriguez, B., Black, H., Woods, N. F., and Women's Health Initiative Observational Study (2009) Angiotensinconverting enzyme inhibitor use and incident frailty in women aged 65 and older. Prospective findings from the Women's Health Initiative Observational Study. J. Am. Geriatr. Soc. 57, 297-303
49. Onder, G., Penninx, B. W., Balkrishnan, R., Fried, L. P., Chaves, P. H., Williamson, J., Carter, C., Di Bari, M., Guralnik, J. M., and Pahor, M. (2002) Relation between use of angiotensin-converting enzyme inhibitors and muscle strength and physical function in older women. An observational study. Lancet 359, 926-930
50. Di Bari, M., van de Poll-Franse, L. V., Onder, G., Kritchevsky, S. B., Newman, A., Harris, T. B., Williamson, J. D., Marchionni, N., Pahor, M., and Health, Aging and Body Composition Study (2004) Antihypertensive medications and differences in muscle mass in older persons. The Health, Aging and Body Composition Study. J. Am. Geriatr Soc. 52, 961-966
51. Sumukadas, D., Witham, M. D., Struthers, A. D., and McMurdo, M. E. (2007) Effect of perindopril on physical function in elderly people with functional impairment. A randomized controlled trial. CMAJ 177, 867-874
52. Glass, D., and Roubenoff, R. (2010) Recent advances in the biology and therapy of muscle wasting. Ann. N.Y. Acad. Sci. 1211, 25-36
53. Masson, S., Latini, R., Bevilacqua, M., Vago, T., Sessa, F., Torri, M., Anesini, A., Salio, M., Pasotti, E., Agnello, D., Santoro, L., Catania, A., Ghezzi, P., Moccetti, T., and Maggioni, A. P. (1998) Within-patient variability of hormone and cytokine concentrations in heart failure. Pharmacol. Res. 37, 213-217
54. Roig, E., Perez-Villa, F., Morales, M., Jiménez, W., Orús, J., Heras, M., and Sanz, G. (2000) Clinical implications of increased plasma angiotensin II despite ACE inhibitor therapy in patients with congestive heart failure. Eur. Heart J. 21, 53-57
55. Graziani, G., Badalamenti, S., Del Bo, A., Marabini, M., Gazzano, G., Como, G., Viganò, E., Ambroso, G., and Morganti, A. (1993) Abnormal hemodynamics and elevated angiotensin II plasma levels in polydipsic patients on regular hemodialysis treatment. Kidney Int. 44, 107-114
56. Simões e Silva, A. C., Diniz, J. S., Pereira, R. M., Pinheiro, S. V., and Santos, R. A. (2006) Circulating renin Angiotensin system in childhood chronic renal failure. Marked increase of angiotensin-(1-7) in end-stage renal disease. Pediatr. Res. 60, 734-739
57. Gonzalez-Villalobos, R. A., Seth, D. M., Satou, R., Horton, H., Ohashi, N., Miyata, K., Katsurada, A., Tran, D. V., Kobori, H., and Navar, L. G. (2008) Intrarenal angiotensin II and angiotensinogen augmentation in chronic angiotensin II-infused mice. Am. J. Physiol. Renal Physiol. 295, F772-9