Diminished autophagy limits cardiac injury in mouse models of type 1 diabetes

Journal of Biological Chemistry

Volumn 288, Issue 25, 2013, Pages 18077-18092

  Xu, Xianmin ^a   Kobayashi, Satoru ^a   Chen, Kai ^a   Timm, Derek ^a   Volden, Paul ^a   Huang, Yuan ^a   Gulick, James ^b   Yue, Zhenyu ^c   Robbins, Jeffrey ^b   Epstein, Paul N ^d   Liang, Qiangrong ^a  

^a UNIVERSITY OF SOUTH DAKOTA   (United States)

^b CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^c MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^d University of Louisville School of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOPHAGY; DRUG DESIGN; HEART DISEASE; MOUSE MODELS; TYPE 1 DIABETES;

CARDIOLOGY;

HEART;

AUTOPHAGY PROTEIN 16; BAFILOMYCIN A1; BECLIN 1; GREEN FLUORESCENT PROTEIN; MEMBRANE PROTEIN; MICROTUBULE ASSOCIATED PROTEIN; MICROTUBULE ASSOCIATED PROTEIN LIGHT CHAIN 3 FORM 2; RAB PROTEIN; RAB9 PROTEIN; STREPTOZOCIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; AUTOPHAGY; CONTROLLED STUDY; DIABETIC CARDIOMYOPATHY; DISEASE EXACERBATION; DISEASE MODEL; FEMALE; GENE OVEREXPRESSION; HEART FUNCTION; HEART MUSCLE CELL; HEART PROTECTION; INSULIN DEPENDENT DIABETES MELLITUS; MALE; MITOCHONDRION; MITOPHAGY; MOUSE; NONHUMAN; OXIDATIVE STRESS; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; STREPTOZOCIN DIABETES; UPREGULATION;

ALTERNATIVE AUTOPHAGY; APOPTOSIS; AUTOPHAGY; BECLIN 1; CARDIOMYOPATHY; DIABETES; MITOCHONDRIA; MITOPHAGY; OXIDATIVE STRESS; RAB9;

ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; AUTOPHAGY; BLOTTING, WESTERN; CARRIER PROTEINS; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 1; DIABETIC CARDIOMYOPATHIES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROTUBULE-ASSOCIATED PROTEINS; MYOCARDIUM; RAB GTP-BINDING PROTEINS; REACTIVE OXYGEN SPECIES;

EID: 84880065357     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.474650     Document Type: Article

References (57)

1. Bell, D. S. (1995) Diabetic cardiomyopathy. A unique entity or a complication of coronary artery disease? Diabetes Care 18, 708-714
2. Boudina, S., and Abel, E. D. (2007) Diabetic cardiomyopathy revisited. Circulation 115, 3213-3223 (Pubitemid 47012236)
3. Poornima, I. G., Parikh, P., and Shannon, R. P. (2006) Diabetic cardiomyopathy. The search for a unifying hypothesis. Circ. Res. 98, 596-605
4. Wold, L. E., Ceylan-Isik, A. F., and Ren, J. (2005) Oxidative stress and stress signaling. Menace of diabetic cardiomyopathy. Acta Pharmacol. Sin. 26, 908-917 (Pubitemid 41153210)
5. Ye, G., Metreveli, N. S., Donthi, R. V., Xia, S., Xu, M., Carlson, E. C., and Epstein, P. N. (2004) Catalase protects cardiomyocyte function in models of type 1 and type 2 diabetes. Diabetes 53, 1336-1343 (Pubitemid 38569021)
6. Liang, Q., Carlson, E. C., Donthi, R. V., Kralik, P. M., Shen, X., and Epstein, P. N. (2002) Overexpression of metallothionein reduces diabetic cardiomyopathy. Diabetes 51, 174-181 (Pubitemid 34517995)
7. Fiordaliso, F., Bianchi, R., Staszewsky, L., Cuccovillo, I., Doni, M., Laragione, T., Salio, M., Savino, C., Melucci, S., Santangelo, F., Scanziani, E., Masson, S., Ghezzi, P., and Latini, R. (2004) Antioxidant treatment attenuates hyperglycemia-induced cardiomyocyte death in rats. J. Mol. Cell. Cardiol. 37, 959-968 (Pubitemid 39446821)
8. Ye, G., Metreveli, N. S., Ren, J., and Epstein, P. N. (2003) Metallothionein prevents diabetes-induced deficits in cardiomyocytes by inhibiting reactive oxygen species production. Diabetes 52, 777-783 (Pubitemid 36323586)
9. Johansen, J. S., Harris, A. K., Rychly, D. J., and Ergul, A. (2005) Oxidative stress and the use of antioxidants in diabetes. Linking basic science to clinical practice. Cardiovasc. Diabetol. 4, 5
10. Yusuf, S., Dagenais, G., Pogue, J., Bosch, J., and Sleight, P. (2000) Vitamin E supplementation and cardiovascular events in high-risk patients. The Heart Outcomes Prevention Evaluation Study Investigators. N. Engl. J. Med. 342, 154-160 (Pubitemid 30051646)
11. Lonn, E., Yusuf, S., Hoogwerf, B., Pogue, J., Yi, Q., Zinman, B., Bosch, J., Dagenais, G., Mann, J. F., and Gerstein, H. C. (2002) Effects of vitamin E on cardiovascular and microvascular outcomes in high-risk patients with diabetes. Results of the HOPE study and MICRO-HOPE substudy. Diabetes Care 25, 1919-1927 (Pubitemid 41071045)
12. Sacco, M., Pellegrini, F., Roncaglioni, M. C., Avanzini, F., Tognoni, G., and Nicolucci, A. (2003) Primary prevention of cardiovascular events with low-dose aspirin and vitamin E in type 2 diabetic patients. Results of the Primary Prevention Project (PPP) trial. Diabetes Care 26, 3264-3272 (Pubitemid 37466885)
13. Lonn, E., Bosch, J., Yusuf, S., Sheridan, P., Pogue, J., Arnold, J. M., Ross, C., Arnold, A., Sleight, P., Probstfield, J., and Dagenais, G. R. (2005) Effects of long-term vitamin E supplementation on cardiovascular events and cancer. A randomized controlled trial. JAMA 293, 1338-1347 (Pubitemid 40381486)
14. Terman, A., and Brunk, U. T. (2005) Autophagy in cardiac myocyte homeostasis, aging, and pathology. Cardiovasc. Res. 68, 355-365 (Pubitemid 41566555)
15. Martinet, W., Knaapen, M. W., Kockx, M. M., and De Meyer, G. R. (2007) Autophagy in cardiovascular disease. Trends Mol. Med. 13, 482-491 (Pubitemid 350086977)
16. Takagi, H., Matsui, Y., and Sadoshima, J. (2007) The role of autophagy in mediating cell survival and death during ischemia and reperfusion in the heart. Antioxid. Redox. Signal 9, 1373-1381 (Pubitemid 47255016)
17. Hamacher-Brady, A., Brady, N. R., and Gottlieb, R. A. (2006) The interplay between pro-death and pro-survival signaling pathways in myocardial ischemia/ reperfusion injury. Apoptosis meets autophagy. Cardiovasc. Drugs Ther. 20, 445-462 (Pubitemid 46150867)
18. Nakai, A., Yamaguchi, O., Takeda, T., Higuchi, Y., Hikoso, S., Taniike, M., Omiya, S., Mizote, I., Matsumura, Y., Asahi, M., Nishida, K., Hori, M., Mizushima, N., and Otsu, K. (2007) The role of autophagy in cardiomyocytes in the basal state and in response to hemodynamic stress. Nat. Med. 13, 619-624 (Pubitemid 46828485)
19. Cuervo, A. M., Bergamini, E., Brunk, U. T., Dröge, W., Ffrench, M., and Terman, A. (2005) Autophagy and aging. The importance of maintaining "clean" cells. Autophagy 1, 131-140
20. Kuma, A., Hatano, M., Matsui, M., Yamamoto, A., Nakaya, H., Yoshimori, T., Ohsumi, Y., Tokuhisa, T., and Mizushima, N. (2004) The role of autophagy during the early neonatal starvation period. Nature 432, 1032-1036 (Pubitemid 40052234)
21. Matsui, Y., Takagi, H., Qu, X., Abdellatif, M., Sakoda, H., Asano, T., Levine, B., and Sadoshima, J. (2007) Distinct roles of autophagy in the heart during ischemia and reperfusion. Roles of AMP-activated protein kinase and Beclin 1 in mediating autophagy. Circ. Res. 100, 914-922 (Pubitemid 46555697)
22. Yan, L., Vatner, D. E., Kim, S. J., Ge, H., Masurekar, M., Massover, W. H., Yang, G., Matsui, Y., Sadoshima, J., and Vatner, S. F. (2005) Autophagy in chronically ischemic myocardium. Proc. Natl. Acad. Sci. U.S.A. 102, 13807-13812 (Pubitemid 41377660)
23. Akazawa, H., Komazaki, S., Shimomura, H., Terasaki, F., Zou, Y., Takano, H., Nagai, T., and Komuro, I. (2004) Diphtheria toxin-induced autophagic cardiomyocyte death plays a pathogenic role in mouse model of heart failure. J. Biol. Chem. 279, 41095-41103 (Pubitemid 39287711)
24. Lu, L., Wu, W., Yan, J., Li, X., Yu, H., and Yu, X. (2009) Adriamycininduced autophagic cardiomyocyte death plays a pathogenic role in a rat model of heart failure. Int. J. Cardiol. 134, 82-90
25. Zhu, H., Tannous, P., Johnstone, J. L., Kong, Y., Shelton, J. M., Richardson, J. A., Le, V., Levine, B., Rothermel, B. A., and Hill, J. A. (2007) Cardiac autophagy is a maladaptive response to hemodynamic stress. J. Clin. Invest. 117, 1782-1793 (Pubitemid 47036312)
26. Tannous, P., Zhu, H., Johnstone, J. L., Shelton, J. M., Rajasekaran, N. S., Benjamin, I. J., Nguyen, L., Gerard, R. D., Levine, B., Rothermel, B. A., and Hill, J. A. (2008) Autophagy is an adaptive response in desmin-related cardiomyopathy. Proc. Natl. Acad. Sci. U.S.A. 105, 9745-9750 (Pubitemid 352031371)
27. Mizushima, N. (2005) The pleiotropic role of autophagy: From protein metabolism to bactericide. Cell Death Differ. 12, 1535-1541 (Pubitemid 41553990)
28. Meijer, A. J., and Codogno, P. (2006) Signalling and autophagy regulation in health, aging, and disease. Mol. Aspects Med. 27, 411-425 (Pubitemid 44466652)
29. Meijer, A. J., and Codogno, P. (2007) Macroautophagy. Protector in the diabetes drama? Autophagy 3, 523-526
30. Jung, H. S., Chung, K. W., Won Kim, J., Kim, J., Komatsu, M., Tanaka, K., Nguyen, Y. H., Kang, T. M., Yoon, K. H., Kim, J. W., Jeong, Y. T., Han, M. S., Lee, M. K., Kim, K. W., Shin, J., and Lee, M. S. (2008) Loss of autophagy diminishes pancreatic beta cell mass and function with resultant hyperglycemia. Cell Metab. 8, 318-324
31. Hur, K. Y., Jung, H. S., and Lee, M. S. (2010) Diabetes Obes. Metab 12, 20-26
32. Kaniuk, N. A., Kiraly, M., Bates, H., Vranic, M., Volchuk, A., and Brumell, J. H. (2007) Ubiquitinated-protein aggregates form in pancreatic beta cells during diabetes-induced oxidative stress and are regulated by autophagy. Diabetes 56, 930-939 (Pubitemid 46525060)
33. Fujimoto, K., Hanson, P. T., Tran, H., Ford, E. L., Han, Z., Johnson, J. D., Schmidt, R. E., Green, K. G., Wice, B. M., and Polonsky, K. S. (2009) Autophagy regulates pancreatic beta cell death in response to Pdx1 deficiency and nutrient deprivation. J. Biol. Chem. 284, 27664-27673
34. Xie, Z., Lau, K., Eby, B., Lozano, P., He, C., Pennington, B., Li, H., Rathi, S., Dong, Y., Tian, R., Kem, D., and Zou, M. H. (2011) Improvement of cardiac functions by chronic metformin treatment is associated with enhanced cardiac autophagy in diabetic OVE26 mice. Diabetes 60, 1770-1778
35. Mizushima, N., Yamamoto, A., Matsui, M., Yoshimori, T., and Ohsumi, Y. (2004) In vivo analysis of autophagy in response to nutrient starvation using transgenic mice expressing a fluorescent autophagosome marker. Mol. Biol. Cell 15, 1101-1111 (Pubitemid 38316219)
36. Yue, Z., Jin, S., Yang, C., Levine, A. J., and Heintz, N. (2003) Beclin 1, an autophagy gene essential for early embryonic development, is a haploinsufficient tumor suppressor. Proc. Natl. Acad. Sci. U.S.A. 100, 15077-15082 (Pubitemid 37518019)
37. Cadwell, K., Liu, J. Y., Brown, S. L., Miyoshi, H., Loh, J., Lennerz, J. K., Kishi, C., Kc, W., Carrero, J. A., Hunt, S., Stone, C. D., Brunt, E. M., Xavier, R. J., Sleckman, B. P., Li, E., Mizushima, N., Stappenbeck, T. S., and Virgin, H. W., 4th (2008) A key role for autophagy and the autophagy gene Atg16l1 in mouse and human intestinal Paneth cells. Nature 456, 259-263
38. Sanbe, A., Gulick, J., Hanks, M. C., Liang, Q., Osinska, H., and Robbins, J. (2003) Reengineering inducible cardiac-specific transgenesis with an attenuated myosin heavy chain promoter. Circ. Res. 92, 609-616 (Pubitemid 36417694)
39. Maloyan, A., Osinska, H., Lammerding, J., Lee, R. T., Cingolani, O. H., Kass, D. A., Lorenz, J. N., and Robbins, J. (2009) Biochemical and mechanical dysfunction in a mouse model of desmin-related myopathy. Circ. Res. 104, 1021-1028
40. Kobayashi, S., Mao, K., Zheng, H., Wang, X., Patterson, C., O'Connell, T. D., and Liang, Q. (2007) Diminished GATA4 protein levels contribute to hyperglycemia-induced cardiomyocyte injury. J. Biol. Chem. 282, 21945-21952 (Pubitemid 47195736)
41. Mizushima, N., and Yoshimori, T. (2007) How to interpret LC3 immunoblotting. Autophagy 3, 542-545 (Pubitemid 350060049)
42. Matsushita, M., Suzuki, N. N., Obara, K., Fujioka, Y., Ohsumi, Y., and Inagaki, F. (2007) Structure of Atg5.Atg16, a complex essential for autophagy. J. Biol. Chem. 282, 6763-6772 (Pubitemid 47100840)
43. Fujita, N., Itoh, T., Omori, H., Fukuda, M., Noda, T., and Yoshimori, T. (2008) The Atg16L complex specifies the site of LC3 lipidation for membrane biogenesis in autophagy. Mol. Biol. Cell 19, 2092-2100
44. Codogno, P., Mehrpour, M., and Proikas-Cezanne, T. (2012) Canonical and non-canonical autophagy. Variations on a common theme of selfeating? Nat. Rev. Mol. Cell Biol. 13, 7-12
45. Juenemann, K., and Reits, E. A. (2012) Alternative macroautophagic pathways. Int. J. Cell Biol. 2012, 189794
46. Nishida, Y., Arakawa, S., Fujitani, K., Yamaguchi, H., Mizuta, T., Kanaseki, T., Komatsu, M., Otsu, K., Tsujimoto, Y., and Shimizu, S. (2009) Discovery of Atg5/Atg7-independent alternative macroautophagy. Nature 461, 654-658
47. Zhang, J., and Ney, P. A. (2009) Role of BNIP3 and NIX in cell death, autophagy, and mitophagy. Cell Death Differ. 16, 939-946
48. Geisler, S., Holmström, K. M., Skujat, D., Fiesel, F. C., Rothfuss, O. C., Kahle, P. J., and Springer, W. (2010) PINK1/Parkin-mediated mitophagy is dependent on VDAC1 and p62/SQSTM1. Nat. Cell Biol. 12, 119-131
49. Narendra, D. P., Jin, S. M., Tanaka, A., Suen, D. F., Gautier, C. A., Shen, J., Cookson, M. R., and Youle, R. J. (2010) PINK1 is selectively stabilized on impaired mitochondria to activate Parkin. PLoS Biol. 8, e1000298
50. Narendra, D., Tanaka, A., Suen, D. F., and Youle, R. J. (2008) Parkin is recruited selectively to impaired mitochondria and promotes their autophagy. J. Cell Biol. 183, 795-803
51. Iwai-Kanai, E., Yuan, H., Huang, C., Sayen, M. R., Perry-Garza, C. N., Kim, L., and Gottlieb, R. A. (2008)Amethod to measure cardiac autophagic flux in vivo. Autophagy 4, 322-329 (Pubitemid 351458093)
52. Kobayashi, S., Xu, X., Chen, K., and Liang, Q. (2012) Suppression of autophagy is protective in high glucose-induced cardiomyocyte injury. Autophagy 8, 577-592
53. Thomson, D. M., Brown, J. D., Fillmore, N., Ellsworth, S. K., Jacobs, D. L., Winder, W. W., Fick, C. A., and Gordon, S. E. (2009) AMP-activated protein kinase response to contractions and treatment with the AMPK activator AICAR in young adult and old skeletal muscle. J. Physiol. 587, 2077-2086
54. Reznick, R. M., and Shulman, G. I. (2006) The role of AMP-activated protein kinase in mitochondrial biogenesis. J. Physiol. 574, 33-39 (Pubitemid 43905794)
55. Saeedi, R., Parsons, H. L., Wambolt, R. B., Paulson, K., Sharma, V., Dyck, J. R., Brownsey, R. W., and Allard, M. F. (2008) Metabolic actions of metformin in the heart can occur by AMPK-independent mechanisms. Am. J. Physiol. Heart Circ. Physiol. 294, H2497-H2506
56. Bugger, H., and Abel, E. D. (2010) Mitochondria in the diabetic heart. Cardiovasc. Res. 88, 229-240
57. Scarlatti, F., Maffei, R., Beau, I., Codogno, P., and Ghidoni, R. (2008) Role of non-canonical Beclin 1-independent autophagy in cell death induced by resveratrol in human breast cancer cells. Cell Death Differ. 15, 1318-1329 (Pubitemid 351984760)