Hematopoietic Akt2 deficiency attenuates the progression of atherosclerosis

FASEB Journal

Volumn 29, Issue 2, 2015, Pages 597-610

  Rotllan, Noemi ^a,b   Chamorro Jorganes, Aránzazu ^a,b   Araldi, Elisa ^a,b   Wanschel, Amarylis C ^b   Aryal, Binod ^a,b   Aranda, Juan F ^a,b   Goedeke, Leigh ^a,b   Salerno, Alessandro G ^b   Ramírez, Cristina M ^a,b   Sessa, William C ^a   Suárez, Yajaira ^a,b   Fernández Hernando, Carlos ^a,b  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Insulin resistance

Indexed keywords

CHOLESTEROL; COLONY STIMULATING FACTOR 1; GLUCOSE; MONOCYTE CHEMOTACTIC PROTEIN 1; PROTEIN KINASE B BETA; AKT2 PROTEIN, MOUSE; CYTOKINE; GLUCOSE BLOOD LEVEL; INSULIN; LIPID; LOW DENSITY LIPOPROTEIN; LOW DENSITY LIPOPROTEIN RECEPTOR; OXIDIZED LOW DENSITY LIPOPROTEIN; PROTEIN KINASE B;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATHEROSCLEROTIC PLAQUE; BONE MARROW TRANSPLANTATION; CELL ISOLATION; CHOLESTEROL BLOOD LEVEL; CHOLESTEROL METABOLISM; CONTROLLED STUDY; DISEASE COURSE; ENZYME DEFICIENCY; GERM LINE; GLUCOSE BLOOD LEVEL; IN VITRO STUDY; MACROPHAGE MIGRATION; MALE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN KINASE B BETA DEFICIENCY; PROTEIN TARGETING; WILD TYPE; ANIMAL; ATHEROSCLEROSIS; BLOOD; BONE MARROW CELL; C57BL MOUSE; CELL MOTION; CHEMISTRY; CONFOCAL MICROSCOPY; CYTOLOGY; DEFICIENCY; FLUORESCENCE MICROSCOPY; GENETICS; INFLAMMATION; KNOCKOUT MOUSE; LEUKOCYTE; MACROPHAGE; METABOLISM; PATHOPHYSIOLOGY;

MUS;

ANIMALS; ATHEROSCLEROSIS; BLOOD GLUCOSE; BONE MARROW CELLS; BONE MARROW TRANSPLANTATION; CELL MOVEMENT; CHOLESTEROL; CYTOKINES; DISEASE PROGRESSION; INFLAMMATION; INSULIN; LEUKOCYTES; LIPIDS; LIPOPROTEINS, LDL; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROSCOPY, CONFOCAL; MICROSCOPY, FLUORESCENCE; PLAQUE, ATHEROSCLEROTIC; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTORS, LDL;

EID: 84937421179     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.14-262097     Document Type: Article

References (35)

1. Bornfeldt, K. E., and Tabas, I. (2011) Insulin resistance, hyperglycemia, and atherosclerosis. Cell Metab. 14, 575-585
2. Tabas, I., Tall, A., and Accili, D. (2010) The impact of macrophage insulin resistance on advanced atherosclerotic plaque progression. Circ. Res. 106, 58-67
3. Cohen, D. E., and Fisher, E. A. (2013) Lipoprotein metabolism, dyslipidemia, and nonalcoholic fatty liver disease. Semin. Liver Dis. 33, 380-388
4. Fernández-Hernando, C., Ackah, E., Yu, J., Suárez, Y., Murata, T., Iwakiri, Y., Prendergast, J., Miao, R. Q., Birnbaum, M. J., and Sessa, W. C. (2007) Loss of Akt1 leads to severe atherosclerosis and occlusive coronary artery disease. Cell Metab. 6, 446-457
5. Fernández-Hernando, C., József, L., Jenkins, D., Di Lorenzo, A., and Sessa, W. C. (2009) Absence of Akt1 reduces vascular smooth muscle cell migration and survival and induces features of plaque vulnerability and cardiac dysfunction during atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 29, 2033-2040
6. Han, S., Liang, C. P., DeVries-Seimon, T., Ranalletta, M., Welch, C. L., Collins-Fletcher, K., Accili, D., Tabas, I., and Tall, A. R. (2006) Macrophage insulin receptor deficiency increases ER stress-induced apoptosis and necrotic core formation in advanced atherosclerotic lesions. Cell Metab. 3, 257-266
7. Rask-Madsen, C., Li, Q., Freund, B., Feather, D., Abramov, R., Wu, I. H., Chen, K., Yamamoto-Hiraoka, J., Goldenbogen, J., Sotiropoulos, K. B., Clermont, A., Geraldes, P., Dall'Osso, C., Wagers, A. J., Huang, P. L., Rekhter, M., Scalia, R., Kahn, C. R., and King, G. L. (2010) Loss of insulin signaling in vascular endothelial cells accelerates atherosclerosis in apolipoprotein E null mice. Cell Metab. 11, 379-389
8. Tsuchiya, K., Tanaka, J., Shuiqing, Y., Welch, C. L., DePinho, R. A., Tabas, I., Tall, A. R., Goldberg, I. J., and Accili, D. (2012) FoxOs integrate pleiotropic actions of insulin in vascular endothelium to protect mice from atherosclerosis. Cell Metab. 15, 372-381
9. Bae, S. S., Cho, H., Mu, J., and Birnbaum, M. J. (2003) Isoform-specific regulation of insulin-dependent glucose uptake by Akt/protein kinase B. J. Biol. Chem. 278, 49530-49536
10. Leavens, K. F., and Birnbaum, M. J. (2011) Insulin signaling to hepatic lipid metabolism in health and disease. Crit. Rev. Biochem. Mol. Biol. 46, 200-215
11. Cho, H., Mu, J., Kim, J. K., Thorvaldsen, J. L., Chu, Q., Crenshaw III, E. B., Kaestner, K. H., Bartolomei, M. S., Shulman, G. I., and Birnbaum, M. J. (2001) Insulin resistance and a diabetes mellituslike syndrome in mice lacking the protein kinase Akt2 (PKB beta). Science 292, 1728-1731
12. Cho, H., Thorvaldsen, J. L., Chu, Q., Feng, F., and Birnbaum, M. J. (2001) Akt1/PKBalpha is required for normal growth but dispensable for maintenance of glucose homeostasis in mice. J. Biol. Chem. 276, 38349-38352
13. Easton, R. M., Cho, H., Roovers, K., Shineman, D. W., Mizrahi, M., Forman, M. S., Lee, V. M., Szabolcs, M., de Jong, R., Oltersdorf, T., Ludwig, T., Efstratiadis, A., and Birnbaum, M. J. (2005) Role for Akt3/protein kinase Bgamma in attainment of normal brain size. Mol. Cell. Biol. 25, 1869-1878
14. Ackah, E., Yu, J., Zoellner, S., Iwakiri, Y., Skurk, C., Shibata, R., Ouchi, N., Easton, R. M., Galasso, G., Birnbaum, M. J., Walsh, K., and Sessa, W. C. (2005) Akt1/protein kinase Balpha is critical for ischemic and VEGF-mediated angiogenesis. J. Clin. Invest. 115, 2119-2127
15. Chen, J., Somanath, P. R., Razorenova, O., Chen, W. S., Hay, N., Bornstein, P., and Byzova, T. V. (2005) Akt1 regulates pathological angiogenesis, vascular maturation and permeability in vivo. Nat. Med. 11, 1188-1196
16. Shiojima, I., Sato, K., Izumiya, Y., Schiekofer, S., Ito, M., Liao, R., Colucci, W. S., and Walsh, K. (2005) Disruption of coordinated cardiac hypertrophy and angiogenesis contributes to the transition to heart failure. J. Clin. Invest. 115, 2108-2118
17. González-Navarro, H., Vinué, A., Vila-Caballer, M., Fortuño, A., Beloqui, O., Zalba, G., Burks, D., Díez, J., and Andrés, V. (2008) Molecular mechanisms of atherosclerosis in metabolic syndrome: role of reduced IRS2-dependent signaling. Arterioscler. Thromb. Vasc. Biol. 28, 2187-2194
18. Arranz, A., Doxaki, C., Vergadi, E., Martinez de la Torre, Y., Vaporidi, K., Lagoudaki, E. D., Ieronymaki, E., Androulidaki, A., Venihaki, M., Margioris, A. N., Stathopoulos, E. N., Tsichlis, P. N., and Tsatsanis, C. (2012) Akt1 and Akt2 protein kinases differentially contribute to macrophage polarization. Proc. Natl. Acad. Sci. USA 109, 9517-9522
19. Vergadi, E., Vaporidi, K., Theodorakis, E. E., Doxaki, C., Lagoudaki, E., Ieronymaki, E., Alexaki, V. I., Helms, M., Kondili, E., Soennichsen, B., Stathopoulos, E. N., Margioris, A. N., Georgopoulos, D., and Tsatsanis, C. (2014) Akt2 deficiency protects from acute lung injury via alternative macrophage activation and miR-146a induction in mice. J. Immunol. 192, 394-406
20. Glass, C. K., and Witztum, J. L. (2001) Atherosclerosis. the road ahead. Cell 104, 503-516
21. Lusis, A. J. (2000) Atherosclerosis. Nature 407, 233-241
22. Locati, M., Mantovani, A., and Sica, A. (2013) Macrophage activation and polarization as an adaptive component of innate immunity. Adv. Immunol. 120, 163-184
23. Martinez, F. O., Gordon, S., Locati, M., and Mantovani, A. (2006) Transcriptional profiling of the human monocyte-to-macrophage differentiation and polarization: new molecules and patterns of gene expression. J. Immunol. 177, 7303-7311
24. Moore, K. J., Sheedy, F. J., and Fisher, E. A. (2013) Macrophagesin atherosclerosis: a dynamic balance. Nat. Rev. Immunol. 13, 709-721
25. Ridley, A. J. (2008) Regulation of macrophage adhesion and migration by Rho GTP-binding proteins. J. Microsc. 231, 518-523
26. Ridley, A. J. (2011) Life at the leading edge. Cell 145, 1012-1022
27. Manning, B. D., and Cantley, L. C. (2007) AKT/PKB signaling: navigating downstream. Cell 129, 1261-1274
28. Rensing, K. L., de Jager, S. C., Stroes, E. S., Vos, M., Twickler, M. T., Dallinga-Thie, G. M., de Vries, C. J., Kuiper, J., Bot, I., and von der Thüsen, J. H. (2014) Akt2/LDLr double knockout mice display impaired glucose tolerance and develop more complex atherosclerotic plaques than LDLr knockout mice. Cardiovasc. Res. 101, 277-287
29. Ding, L., Biswas, S., Morton, R. E., Smith, J. D., Hay, N., Byzova, T. V., Febbraio, M., and Podrez, E. A. (2012) Akt3 deficiency in macrophages promotes foam cell formation and atherosclerosis in mice. Cell Metab. 15, 861-872
30. Huang, C. X., Zhang, Y. L., Wang, J. F., Jiang, J. Y., and Bao, J. L. (2013) MCP-1 impacts RCT by repressing ABCA1, ABCG1, and SR-BI through PI3K/Akt posttranslational regulation in HepG2 cells. J. Lipid Res. 54, 1231-1240
31. Gerszten, R. E., Friedrich, E. B., Matsui, T., Hung, R. R., Li, L., Force, T., and Rosenzweig, A. (2001) Role of phosphoinositide 3-kinase in monocyte recruitment under flow conditions. J. Biol. Chem. 276, 26846-26851
32. Zhou, G. L., Tucker, D. F., Bae, S. S., Bhatheja, K., Birnbaum, M. J., and Field, J. (2006) Opposing roles for Akt1 and Akt2 in Rac/Pak signaling and cell migration. J. Biol. Chem. 281, 36443-36453
33. Zhang, B., Ma, Y., Guo, H., Sun, B., Niu, R., Ying, G., and Zhang, N. (2009) Akt2 is required for macrophage chemotaxis. Eur. J. Immunol. 39, 894-901
34. Li, J., Kim, K., Hahm, E., Molokie, R., Hay, N., Gordeuk, V. R., Du, X., and Cho, J. (2014) Neutrophil AKT2 regulates heterotypic cell-cell interactions during vascular inflammation. J. Clin. Invest. 124, 1483-1496
35. Chen, J., Tang, H., Hay, N., Xu, J., and Ye, R. D. (2010) Akt isoforms differentially regulate neutrophil functions. Blood 115, 4237-4246