Control of autophagy maturation by acid sphingomyelinase in mouse coronary arterial smooth muscle cells: Protective role in atherosclerosis

Journal of Molecular Medicine

Volumn 92, Issue 5, 2014, Pages 473-485

  Li, Xiang ^a   Xu, Ming ^a   Pitzer, Ashley L ^a   Xia, Min ^a   Boini, Krishna M ^a   Li, Pin Lan ^a   Zhang, Yang ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

Author keywords

Acid sphingomyelinase; Atherosclerosis; Autophagic flux; coronary arterial smooth muscle cell; Coronary artery; Lysosome

Indexed keywords

7 OXOCHOLESTEROL; CATHEPSIN; CELL MARKER; LC3B PROTEIN; PROTEIN P62; SPHINGOMYELIN PHOSPHODIESTERASE; UNCLASSIFIED DRUG; ACID SPHINGOMYELINASE-1;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ARTICLE; ATHEROGENESIS; ATHEROSCLEROSIS; AUTOPHAGOSOME; AUTOPHAGY; CELL MATURATION; CELL PROLIFERATION ASSAY; CORONARY ARTERIAL SMOOTH MUSCLE CELL; FLOW CYTOMETRY; FLUORESCENCE RESONANCE ENERGY TRANSFER; HEART PROTECTION; LYSOSOME; MALE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; SELECTIVE AUTOPHAGY; VASCULAR SMOOTH MUSCLE; WESTERN BLOTTING; ANIMAL; CELL CULTURE; CELL DIFFERENTIATION; CELL PROLIFERATION; CORONARY BLOOD VESSEL; ENZYMOLOGY; GENE DELETION; GENETICS; METABOLISM; PATHOLOGY; SMOOTH MUSCLE FIBER; UPREGULATION;

ANIMALS; ATHEROSCLEROSIS; AUTOPHAGY; CATHEPSINS; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; CORONARY VESSELS; GENE DELETION; LYSOSOMES; MICE; MYOCYTES, SMOOTH MUSCLE; SPHINGOMYELIN PHOSPHODIESTERASE; UP-REGULATION;

EID: 84899907083     PISSN: 09462716     EISSN: 14321440     Source Type: Journal    
DOI: 10.1007/s00109-014-1120-y     Document Type: Article

References (58)

1. Zhang Y, Li X, Becker KA, Gulbins E (2009) Ceramide-enriched membrane domains - structure and function. Biochim Biophys Acta 1788:178-183
2. Leger AJ, Mosquea LM, Li L, Chuang W, Pacheco J, Taylor K, Luo Z, Piepenhagen P, Ziegler R, Moreland R et al (2011) Adeno-associated virus-mediated expression of acid sphingomyelinase decreases atherosclerotic lesion formation in apolipoprotein E(-/-) mice. J Gene Med 13:324-332
3. Devlin CM, Leventhal AR, Kuriakose G, Schuchman EH, Williams KJ, Tabas I (2008) Acid sphingomyelinase promotes lipoprotein retention within early atheromata and accelerates lesion progression. Arterioscler Thromb Vasc Biol 28:1723-1730
4. Schissel SL, Keesler GA, Schuchman EH, Williams KJ, Tabas I (1998) The cellular trafficking and zinc dependence of secretory and lysosomal sphingomyelinase, two products of the acid sphingomyelinase gene. J Biol Chem 273:18250-18259
5. Tabas I, Williams KJ, Boren J (2007) Subendothelial lipoprotein retention as the initiating process in atherosclerosis: update and therapeutic implications. Circulation 116:1832-1844
6. Oorni K, Posio P, Ala-Korpela M, Jauhiainen M, Kovanen PT (2005) Sphingomyelinase induces aggregation and fusion of small very low-density lipoprotein and intermediate-density lipoprotein particles and increases their retention to human arterial proteoglycans. Arterioscler Thromb Vasc Biol 25:1678-1683
7. Leventhal AR, Chen W, Tall AR, Tabas I (2001) Acid sphingomyelinase- deficient macrophages have defective cholesterol trafficking and efflux. J Biol Chem 276:44976-44983
8. Liu J, Huan C, Chakraborty M, Zhang H, Lu D, Kuo MS, Cao G, Jiang XC (2009) Macrophage sphingomyelin synthase 2 deficiency decreases atherosclerosis in mice. Circ Res 105:295-303
9. McGovern MM, Pohl-Worgall T, Deckelbaum RJ, Simpson W, Mendelson D, Desnick RJ, Schuchman EH, Wasserstein MP (2004) Lipid abnormalities in children with types A and B Niemann Pick disease. J Pediatr 145:77-81
10. Fuster JJ, Fernandez P, Gonzalez-Navarro H, Silvestre C, Nabah YN, Andres V (2010) Control of cell proliferation in atherosclerosis: insights from animal models and human studies. Cardiovasc Res 86:254-264
11. Lacolley P, Regnault V, Nicoletti A, Li Z, Michel JB (2012) The vascular smooth muscle cell in arterial pathology: a cell that can take on multiple roles. Cardiovasc Res 95:194-204
12. Klionsky DJ, Emr SD (2000) Autophagy as a regulated pathway of cellular degradation. Science 290:1717-1721
13. Wei YM, Li X, Xu M, Abais JM, Chen Y, Riebling CR, Boini KM, Li PL, Zhang Y (2013) Enhancement of autophagy by simvastatin through inhibition of Rac1-mTOR signaling pathway in coronary arterial myocytes. Cell Physiol Biochem 31:925-937
14. Levine B, Kroemer G (2008) Autophagy in the pathogenesis of disease. Cell 132:27-42
15. Klionsky DJ (2007) Autophagy: from phenomenology to molecular understanding in less than a decade. Nat RevMol Cell Biol 8:931-937
16. Bampton ET, Goemans CG, Niranjan D, Mizushima N, Tolkovsky AM (2005) The dynamics of autophagy visualized in live cells: from autophagosome formation to fusion with endo/lysosomes. Autophagy 1:23-36
17. Xie Z, Klionsky DJ (2007) Autophagosome formation: core machinery and adaptations. Nat Cell Biol 9:1102-1109
18. Boini KM, Xia M, Li C, Zhang C, Payne LP, Abais JM, Poklis JL, Hylemon PB, Li PL (2011) Acid sphingomyelinase gene deficiency ameliorates the hyperhomocysteinemia-induced glomerular injury in mice. Am J Pathol 179:2210-2219
19. Li X, Han WQ, Boini KM, Xia M, Zhang Y, Li PL (2013) TRAIL death receptor 4 signaling via lysosome fusion and membrane raft clustering in coronary arterial endothelial cells: evidence from ASM knockout mice. J Mol Med (Berl) 91:25-36
20. Lemaitre V, Soloway PD, D'Armiento J (2003) Increased medial degradation with pseudo-aneurysm formation in apolipoprotein Eknockout mice deficient in tissue inhibitor of metalloproteinases-1. Circulation 107:333-338
21. Park TS, Panek RL, Mueller SB, Hanselman JC, Rosebury WS, Robertson AW, Kindt EK, Homan R, Karathanasis SK, Rekhter MD (2004) Inhibition of sphingomyelin synthesis reduces atherogenesis in apolipoprotein E-knockout mice. Circulation 110:3465-3471
22. Bjursell M, Gerdin AK, Lelliott CJ, Egecioglu E, Elmgren A, Tornell J, Oscarsson J, Bohlooly YM (2008) Acutely reduced locomotor activity is a major contributor to Western diet-induced obesity in mice. Am J Physiol Endocrinol Metab 294:E251-E260
23. Wei YM, Li X, Xiong J, Abais JM, Xia M, Boini KM, Zhang Y, Li PL (2013) Attenuation by statins ofmembrane raft-redox signaling in coronary arterial endothelium. J Pharmacol Exp Ther 345:170-179
24. Becker KA, Henry B, Ziobro R, Tummler B, Gulbins E, Grassme H (2012) Role of CD95 in pulmonary inflammation and infection in cystic fibrosis. J Mol Med (Berl) 90:1011-1023
25. Xu M, Zhang Y, Xia M, Li XX, Ritter JK, Zhang F, Li PL (2012) NAD(P)H oxidase-dependent intracellular and extracellular O2*-production in coronary arterial myocytes from CD38 knockout mice. Free Radic Biol Med 52:357-365
26. Zhang Y, Li X, Carpinteiro A, Gulbins E (2008) Acid sphingomyelinase amplifies redox signaling in Pseudomonas aeruginosa-induced macrophage apoptosis. J Immunol 181:4247-4254
27. Zhang C, Boini KM, Xia M, Abais JM, Li X, Liu Q, Li PL (2012) Activation of Nod-like receptor protein 3 inflammasomes turns on podocyte injury and glomerular sclerosis in hyperhomocysteinemia. Hypertension 60:154-162
28. Raben N, Shea L, Hill V, Plotz P (2009) Monitoring autophagy in lysosomal storage disorders. Methods Enzymol 453:417-449
29. Zhang Y, Li X, Carpinteiro A, Goettel JA, Soddemann M, Gulbins E (2011) Kinase suppressor of Ras-1 protects against pulmonary Pseudomonas aeruginosa infections. Nat Med 17:341-346
30. Jin S, Yi F, Zhang F, Poklis JL, Li PL (2008) Lysosomal targeting and trafficking of acid sphingomyelinase to lipid raft platforms in coronary endothelial cells. Arterioscler Thromb Vasc Biol 28:2056-2062
31. Ding Z, Wang X, Schnackenberg L, Khaidakov M, Liu S, Singla S, Dai Y, Mehta JL (2013) Regulation of autophagy and apoptosis in response to ox-LDL in vascular smooth muscle cells, and the modulatory effects of the microRNA hsa-let-7g. Int J Cardiol 168:1378-1385
32. Zhou C, Zhong W, Zhou J, Sheng F, Fang Z, Wei Y, Chen Y, Deng X, Xia B, Lin J (2012) Monitoring autophagic flux by an improved tandem fluorescent-tagged LC3 (mTagRFP-mWasabi-LC3) reveals that high-dose rapamycin impairs autophagic flux in cancer cells. Autophagy 8:1215-1226
33. Jahreiss L, Menzies FM, Rubinsztein DC (2008) The itinerary of autophagosomes: from peripheral formation to kiss-and-run fusion with lysosomes. Traffic 9:574-587
34. Yue W, Hamai A, Tonelli G, Bauvy C, Nicolas V, Tharinger H, Codogno P, Mehrpour M (2013) Inhibition of the autophagic flux by salinomycin in breast cancer stem-like/progenitor cells interferes with their maintenance. Autophagy 9:714-729
35. Liao PL, Cheng YW, Li CH, Wang YT, Kang JJ (2010) 7-Ketocholesterol and cholesterol-5alpha,6alpha-epoxide induce smooth muscle cell migration and proliferation through the epidermal growth factor receptor/phosphoinositide 3-kinase/Akt signaling pathways. Toxicol Lett 197:88-96
36. Pedruzzi E, Guichard C, Ollivier V, Driss F, Fay M, Prunet C, Marie JC, Pouzet C, Samadi M, Elbim C et al (2004) NAD(P)H oxidase Nox-4 mediates 7-ketocholesterol-induced endoplasmic reticulum stress and apoptosis in human aortic smooth muscle cells. Mol Cell Biol 24:10703-10717
37. Kabeya Y, Mizushima N, Ueno T, Yamamoto A, Kirisako T, Noda T, Kominami E, Ohsumi Y, Yoshimori T (2000) LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J 19:5720-5728
38. Pankiv S, Clausen TH, Lamark T, Brech A, Bruun JA, Outzen H, Overvatn A, Bjorkoy G, Johansen T (2007) p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J Biol Chem 282:24131-24145
39. Park MA, Zhang G, Martin AP, Hamed H, Mitchell C, Hylemon PB, Graf M, Rahmani M, Ryan K, Liu X et al (2008) Vorinostat and sorafenib increase ER stress, autophagy and apoptosis via ceramide-dependent CD95 and PERK activation. Cancer Biol Ther 7:1648-1662
40. Taniguchi M, Kitatani K, Kondo T, Hashimoto-Nishimura M, Asano S, Hayashi A, Mitsutake S, Igarashi Y, Umehara H, Takeya H et al (2012) Regulation of autophagy and its associated cell death by "sphingolipid rheostat": reciprocal role of ceramide and sphingosine 1-phosphate in the mammalian target of rapamycin pathway. J Biol Chem 287:39898-39910
41. Glunde K, Guggino SE, Solaiyappan M, Pathak AP, Ichikawa Y, Bhujwalla ZM (2003) Extracellular acidification alters lysosomal trafficking in human breast cancer cells. Neoplasia 5:533-545
42. Trajkovic K, Dhaunchak AS, Goncalves JT, Wenzel D, Schneider A, Bunt G, Nave KA, Simons M (2006) Neuron to glia signaling triggers myelin membrane exocytosis from endosomal storage sites. J Cell Biol 172:937-948
43. Shen D, Wang X, Li X, Zhang X, Yao Z, Dibble S, Dong XP, Yu T, Lieberman AP, Showalter HD et al (2012) Lipid storage disorders block lysosomal trafficking by inhibiting a TRP channel and lysosomal calcium release. Nat Commun 3:731
44. Yamamoto M, Suzuki SO, Himeno M (2010) The effects of dynein inhibition on the autophagic pathway in glioma cells. Neuropathology 30:1-6
45. Xu M, Li XX, Xiong J, Xia M, Gulbins E, Zhang Y, Li PL (2013) Regulation of autophagic flux by dynein-mediated autophagosomes trafficking in mouse coronary arterial myocytes. Biochim Biophys Acta 1833:3228-3236
46. Schramm M, Herz J, Haas A, Kronke M, Utermohlen O (2008) Acid sphingomyelinase is required for efficient phago-lysosomal fusion. Cell Microbiol 10:1839-1853
47. Trajkovic K, Hsu C, Chiantia S, Rajendran L, Wenzel D, Wieland F, Schwille P, Brugger B, Simons M (2008) Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science 319:1244-1247
48. Zeidan YH, Jenkins RW, Hannun YA (2008) Remodeling of cellular cytoskeleton by the acid sphingomyelinase/ceramide pathway. J Cell Biol 181:335-350
49. Lee YG, Lee J, Cho JY(2010) Cell-permeable ceramides act as novel regulators of U937 cell-cell adhesion mediated by CD29, CD98, and CD147. Immunobiology 215:294-303
50. Widau RC, Jin Y, Dixon SA, Wadzinski BE, Gallagher PJ (2010) Protein phosphatase 2A (PP2A) holoenzymes regulate death-associated protein kinase (DAPK) in ceramide-induced anoikis. J Biol Chem 285:13827-13838
51. Sentelle RD, Senkal CE, Jiang W, Ponnusamy S, Gencer S, Selvam SP, Ramshesh VK, Peterson YK, Lemasters JJ, Szulc ZM et al (2012) Ceramide targets autophagosomes tomitochondria and induces lethal mitophagy. Nat Chem Biol 8:831-838
52. Patschan S, Chen J, Polotskaia A, Mendelev N, Cheng J, Patschan D, Goligorsky MS (2008) Lipid mediators of autophagy in stress-induced premature senescence of endothelial cells. Am J Physiol Heart Circ Physiol 294:H1119-H1129
53. Moles A, Tarrats N, Fernandez-Checa JC, Mari M (2012) Cathepsin B overexpression due to acid sphingomyelinase ablation promotes liver fibrosis in Niemann-Pick disease. J Biol Chem 287:1178-1188
54. Dong N, Zhu Q, Zhang P, Zhu C, Wang M, Li W, Liu J, Liu Y, Ma B, Wu K (2012) Autophagy downregulates thrombin-induced VSMCs proliferation through lysosomal pathway. Int J Cardiol 159:156-158
55. Hu P, Lai D, Lu P, Gao J, He H (2012) ERK and Akt signaling pathways are involved in advanced glycation end product-induced autophagy in rat vascular smooth muscle cells. Int J Mol Med 29:613-618
56. Maor I, Mandel H, Aviram M (1995) Macrophage uptake of oxidized LDL inhibits lysosomal sphingomyelinase, thus causing the accumulation of unesterified cholesterol-sphingomyelin-rich particles in the lysosomes. A possible role for 7-Ketocholesterol. Arterioscler Thromb Vasc Biol 15:1378-1387
57. Thurberg BL, Wasserstein MP, Schiano T, O'Brien F, Richards S, Cox GF, McGovern MM (2012) Liver and skin histopathology in adults with acid sphingomyelinase deficiency (Niemann-Pick disease type B). Am J Surg Pathol 36:1234-1246
58. Savic R, He X, Fiel I, Schuchman EH (2013) Recombinant human acid sphingomyelinase as an adjuvant to sorafenib treatment of experimental liver cancer. PLoS One 8:e65620