Enhancement in efferocytosis of oxidized low-density lipoprotein-induced apoptotic RAW264.7 cells through Sirt1-mediated autophagy

International Journal of Molecular Medicine

Volumn 33, Issue 3, 2014, Pages 523-533

  Liu, Baoxin ^a   Zhang, Buchun ^a,b   Guo, Rong ^a   Li, Shuang ^a   Xu, Yawei ^a  

^a TONGJI UNIVERSITY   (China)

^b XUZHOU MEDICAL UNIVERSITY   (China)

Author keywords

Apoptosis; Atherosclerosis; Autophagy; Efferocytosis; RAW264.7; Sirt1

Indexed keywords

APOPTOSIS; ATHEROSCLEROSIS; AUTOPHAGY; CELL LINE; GENE EXPRESSION REGULATION; HUMANS; LIPOPROTEINS, LDL; MOLECULAR TARGETED THERAPY; SIRTUIN 1; STILBENES;

EID: 84893849787     PISSN: 11073756     EISSN: 1791244X     Source Type: Journal    
DOI: 10.3892/ijmm.2013.1609     Document Type: Article

References (59)

1. Gersh BJ, Sliwa K, Mayosi BM and Yusuf S: Novel therapeutic concepts: The epidemic of cardiovascular disease in the developing world: Global implications. Eur Heart J 31: 642-648, 2010.
2. Moore KJ and Tabas I: Macrophages in the pathogenesis of atherosclerosis. Cell 145: 341-355, 2011.
3. Gautier EL, Jakubzick C and Randolph GJ: Regulation of the migration and survival of monocyte subsets by chemokine receptors and its relevance to atherosclerosis. Arterioscler Thromb Vasc Biol 29: 1412-1418, 2009.
4. Gerrity RG: The role of the monocyte in atherogenesis: I. Transition of blood-borne monocytes into foam cells in fatty lesions. Am J Pathol 103: 181-190, 1981.
5. Swirski FK, Pittet MJ, Kircher MF, Aikawa E, Jaffer FA, Libby P and Weissleder R: Monocyte accumulation in mouse atherogenesis is progressive and proportional to extent of disease. Proc Natl Acad Sci USA 103: 10340-10345, 2006.
6. Ylä-Herttuala S, Palinski W, Rosenfeld ME, Parthasarathy S, Carew TE, Butler S, Witztum JL and Steinberg D: Evidence for the presence of oxidatively modified low density lipoprotein in atherosclerotic lesions of rabbit and man. J Clin Invest 84: 1086-1095, 1989.
7. Colles SM, Maxson JM, Carlson SG and Chisolm GM: Oxidized LDL-induced injury and apoptosis in atherosclerosis. Potential roles for oxysterols. Trends Cardiovasc Med 11: 131-138, 2001.
8. Salvayre R, Auge N, Benoist H and Negre-Salvayre A: Oxidized low-density lipoprotein-induced apoptosis. Biochim Biophys Acta 1585: 213-221, 2002.
9. Napoli C: Oxidation of LDL, atherogenesis, and apoptosis. Ann NY Acad Sci 1010: 698-709, 2003.
10. Stoneman VE and Bennett MR: Role of apoptosis in atherosclerosis and its therapeutic implications. Clin Sci (Lond) 107: 343-354, 2004.
11. Tabas I: Apoptosis and efferocytosis in mouse models of atherosclerosis. Curr Drug Targets 8: 1288-1296, 2007.
12. Seimon T and Tabas I: Mechanisms and consequences of macrophage apoptosis in atherosclerosis. J Lipid Res 50: S382-S387, 2009.
13. Verheye S, Martinet W, Kockx MM, Knaapen MW, Salu K, Timmermans JP, Ellis JT, Kilpatrick DL and De Meyer GR: Selective clearance of macrophages in atherosclerotic plaques by autophagy. J Am Coll Cardiol 49: 706-715, 2007.
14. De Meyer I, Martinet W, Schrijvers DM, Timmermans JP, Bult H and De Meyer GR: Toll-like receptor 7 stimulation by imiquimod induces macrophage autophagy and inflammation in atherosclerotic plaques. Basic Res Cardiol 107: 269, 2012.
15. Razani B, Feng C, Coleman T, Emanuel R, Wen H, Hwang S, Ting JP, Virgin HW, Kastan MB and Semenkovich CF: Autophagy links inflammasomes to atherosclerotic progression. Cell Metab 15: 534-544, 2012.
16. Liao X, Sluimer JC, Wang Y, Subramanian M, Brown K, Pattison JS, Robbins J, Martinez J and Tabas I: Macrophage autophagy plays a protective role in advanced atherosclerosis. Cell Metab 15: 545-553, 2012.
17. Axe EL, Walker SA, Manifava M, Chandra P, Roderick HL, Habermann A, Griffiths G and Ktistakis NT: Autophagosome formation from membrane compartments enriched in phosphatidylinositol 3-phosphate and dynamically connected to the endoplasmic reticulum. J Cell Biol 182: 685-701, 2008.
18. Hayashi-Nishino M, Fujita N, Noda T, Yamaguchi A, Yoshimori T and Yamamoto A: A subdomain of the endoplasmic reticulum forms a cradle for autophagosome formation. Nat Cell Biol 11: 1433-1437, 2009.
19. Hailey DW, Rambold AS, Satpute-Krishnan P, Mitra K, Sougrat R, Kim PK and Lippincott-Schwartz J: Mitochondria supply membranes for autophagosome biogenesis during starvation. Cell 141: 656-667, 2010.
20. Tooze SA and Yoshimori T: The origin of the autophagosomal membrane. Nat Cell Biol 12: 831-835, 2010.
21. Ravikumar B, Moreau K, Jahreiss L, Puri C and Rubinsztein DC: Plasma membrane contributes to the formation of pre-autophagosomal structures. Nat Cell Biol 12: 747-757, 2010.
22. Goligorsky MS: SIRTing out the link between autophagy and ageing. Nephrol Dial Transplant 25: 2434-2436, 2010.
23. Schrijvers DM, De Meyer GR and Martinet W: Autophagy in atherosclerosis: A potential drug target for plaque stabilization. Arterioscler Thromb Vasc Biol 31: 2787-2791, 2011.
24. Martinet W and De Meyer GR: Autophagy in atherosclerosis: A cell survival and death phenomenon with therapeutic potential. Circ Res 104: 304-317, 2009.
25. Martinez J, Almendinger J, Oberst A, Ness R, Dillon CP, Fitzgerald P, Hengartner MO and Green DR: Microtubule-associated protein 1 light chain 3 alpha (LC3)-associated phagocytosis is required for the efficient clearance of dead cells. Proc Natl Acad Sci USA 108: 17396-17401, 2011.
26. Yu W, Fu YC, Chen CJ, Wang X and Wang W: SIRT1: A novel target to prevent atherosclerosis. J Cell Biochem 108: 10-13, 2009.
27. Norata GD, Marchesi P, Passamonti S, Pirillo A, Violi F and Catapano AL: Anti-inflammatory and anti-atherogenic effects of cathechin, caffeic acid and trans-resveratrol in apolipoprotein E deficient mice. Atherosclerosis 191: 265-271, 2007.
28. Wang Z, Zou J, Cao K, Hsieh TC, Huang Y and Wu JM: Dealcoholized red wine containing known amounts of resveratrol suppresses atherosclerosis in hypercholesterolemic rabbits without affecting plasma lipid levels. Int J Mol Med 16: 533-540, 2005.
29. Zhang QJ, Wang Z, Chen HZ, Zhou S, Zheng W, Liu G, Wei YS, Cai H, Liu DP and Liang CC. Endothelium-specific overexpression of class III deacetylase SIRT1 decreases atherosclerosis in apolipoprotein E-deficient mice. Cardiovasc Res 80: 191-199, 2008.
30. Li L, Zhang HN, Chen HZ, Gao P, Zhu LH, Li HL, Lv X, Zhang QJ, Zhang R, Wang Z, She ZG, Zhang R, Wei YS, Du GH, Liu DP and Liang CC: SIRT1 acts as a modulator of neointima formation following vascular injury in mice. Circ Res 108: 1180-1189, 2011.
31. Houtkooper RH, Pirinen E and Auwerx J: Sirtuins as regulators of metabolism and healthspan. Nat Rev Mol Cell Biol 13: 225-238, 2012.
32. Mattagajasingh I, Kim CS, Naqvi A, Yamamori T, Hoffman TA, Jung SB, DeRicco J, Kasuno K and Irani K: SIRT1 promotes endothelium-dependent vascular relaxation by activating endothelial nitric oxide synthase. Proc Natl Acad Sci USA 104: 14855-14860, 2007.
33. Brunet A, Sweeney LB, Sturgill JF, Chua KF, Greer PL, Lin Y, Tran H, Ross SE, Mostoslavsky R, Cohen HY, Hu LS, Cheng HL, Jedrychowski MP, Gygi SP, Sinclair DA, Alt FW and Greenberg ME: Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase. Science 303: 2011-2015, 2004.
34. Stein S and Matter CM: Protective roles of SIRT1 in atherosclerosis. Cell Cycle 10: 640-647, 2011.
35. Lee IH, Cao L, Mostoslavsky R, Lombard DB, Liu J, Bruns NE, Tsokos M, Alt FW and Finkel T: A role for the NAD-dependent deacetylase Sirt1 in the regulation of autophagy. Proc Natl Acad Sci USA 105: 3374-3379, 2008.
36. Kockx MM, De Meyer GR, Buyssens N, Knaapen MW, Bult H and Herman AG: Cell composition, replication, and apoptosis in atherosclerotic plaques after 6 months of cholesterol withdrawal. Circ Res 83: 378-387, 1998.
37. Nowicki M, Zabirnyk O, Duerrschmidt N, Borlak J and Spanel-Borowski K: No upregulation of lectin-like oxidized low-density lipoprotein receptor-l in serum-deprived EAhy926 endothelial cells under oxLDL exposure, but increase in autophagy. Eur J Cell Biol 86: 605-615, 2007.
38. Yoshimori T: Autophage: A regulated bulk degradation process inside cells. Biochem Biophys Res Commm 313: 453-458, 2004.
39. Singh R and Cuervo AM: Autophagy in the cellular energetic balance. Cell Metab 13: 495-504, 2011.
40. Singh R, Kaushik S, Wang Y, Xiang Y, Novak I, Komatsu M, Tanaka K, Cuervo AM and Czaja MJ: Autophagy regulates lipid metabolism. Nature 458: 1131-1135, 2009.
41. Singh R and Cuervo AM: Lipophagy: Connecting autophagy and lipid metabolism. Int J Cell Biol 2012: 282041, 2012.
42. Liu K and Czaja MJ: Regulation of lipid stores and metabolism by lipophagy. Cell Death Differ 20: 3-11, 2013.
43. Ouimet M, Franklin V, Mak E, Liao X, Tabas I and Marcel YL: Autophagy regulates cholesterol efflux from macrophage foam cells via lysosomal acid lipase. Cell Metab 13: 655-667, 2011.
44. Kiffin R, Bandyopadhyay U and Cuervo AM: Oxidative stress and autophagy. Antioxid Redox Signal 8: 152-162, 2006.
45. Ohsumi Y: Molecular dissection of autophagy: Two ubiquitin-like systems. Nat Rev Mol Cell Biol 2: 211-216, 2001.
46. Shintani T and Klionsky DJ: Autophagy in health and disease: A double-edged sword. Science 306: 990-995, 2004.
47. Lum JJ, DeBerardinis RJ and Thompson CB: Autophagy in metazoans: Cell survival in the land of plenty. Nat Rev Mol Cell Biol 6: 439-448, 2005.
48. Li S, Sun Y, Liang CP, Thorp EB, Han S, Jehle AW, Saraswathi V, Pridgen B, Kanter JE, Li R, Welch CL, Hasty AH, Bornfeldt KE, Breslow JL, Tabas I and Tall AR: Defective phagocytosis of apoptotic cells by macrophages in atherosclerotic lesions of ob/ob mice and reversal by a fish oil diet. Circ Res 105: 1072-1082, 2009.
49. Yancey PG, Blakemore J, Ding L, Fan D, Overton CD, Zhang Y, Linton MF and Fazio S: Macrophage LRP-1 controls plaque cellularity by regulating efferocytosis and Akt activation. Arterioscler Thromb Vasc Biol 30: 787-795, 2010.
50. Jehle AW, Gardai SJ, Li S, Linsel-Nitschke P, Morimoto K, Janssen WJ, Vandivier RW, Wang N, Greenberg S, Dale BM, Qin C, Henson PM and Tall AR: ATP-binding cassette transporter A7 enhances phagocytosis of apoptotic cells and associated ERK signaling in macrophages. J Cell Biol 174: 547-556, 2006.
51. He X, Andersson G, Lindgren U and Li Y: Resveratrol prevents RANKL-induced osteoclast differentiation of murine osteoclast progenitor RAW 264.7 cells through inhibition of ROS production. Biochem Biophys Res Commun 401: 356-362, 2010.
52. Peled T, Shoham H, Aschengrau D, Yackoubov D, Frei G, Rosenheimer GN, Lerrer B, Cohen HY, Nagler A, Fibach E and Peled A: Nicotinamide, a SIRT1 inhibitor, inhibits differentiation and facilitates expansion of hematopoietic progenitor cells with enhanced bone marrow homing and engraftment. Exp Hematol 40: 342-355, 2012.
53. Zhang JG, Zhao G, Qin Q, Wang B, Liu L, Liu Y, Deng SC, Tian K and Wang CY: Nicotinamide prohibits proliferation and enhances chemosensitivity of pancreatic cancer cells through deregulating SIRT1 and Ras/Akt pathways. Pancreatology 13: 140-146, 2013.
54. Stein S, Lohmann C, Schäfer N, Hofmann J, Rohrer L, Besler C, Rothgiesser KM, Becher B, Hottiger MO, Borén J, McBurney MW, Landmesser U, Lüscher TF and Matter CM: SIRT1 decreases Lox-1-mediated foam cell formation in athero-genesis. Eur Heart J 31: 2301-2309, 2010.
55. Guarente L: Franklin H. Epstein Lecture: Sirtuins, aging, and medicine. N Engl J Med 364: 2235-2244, 2011.
56. Chen Lf, Fischle W, Verdin E and Greene WC: Duration of nuclear NF-kappaB action regulated by reversible acetylation. Science 293: 1653-1657, 2001.
57. Albani D, Polito L, Batelli S, De Mauro S, Fracasso C, Martelli G, Colombo L, Manzoni C, Salmona M, Caccia S, Negro A and Forloni G: The SIRT1 activator resveratrol protects SK-N-BE cells from oxidative stress and against toxicity caused by alpha-synuclein or amyloid-beta (1-42) peptide. J Neurochem 110: 1445-1456, 2009.
58. Wu Y, Li X, Zhu JX, Xie W, Le W, Fan Z, Jankovic J and Pan T: Resveratrol-activated AMPK/SIRT1/autophagy in cellular models of Parkinson's disease. Neurosignals 19: 163-174, 2011.
59. Takeda-Watanabe A, Kitada M, Kanasaki K and Koya D: SIRT1 inactivation induces inflammation through the dysregulation of autophagy in human THP-1 cells. Biochem Biophys Res Commun 427: 191-196, 2012.