Sulforaphane protects human umbilical vein cells against lipotoxicity by stimulating autophagy via an AMPK-mediated pathway

Journal of Functional Foods

Volumn 15, Issue , 2015, Pages 23-34

  Wang, Ning ^a,b   Zhao, Juyang ^a   Liu, Qian ^a,c   Diao, Xinping ^a   Kong, Baohua ^a,c  

^a NORTHEAST AGRICULTURAL UNIVERSITY   (China)

^b HEILONGJIANG ACADEMY OF AGRICULTURAL SCIENCES   (China)

^c Synergetic Innovation Center of Food Safety and Nutrition   (China)

Author keywords

Autophagy; Endothelial cell; Lipotoxicity; Saturated fatty acid; Sulforaphane

Indexed keywords

MAMMALIA;

EID: 84929252067     PISSN: 17564646     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jff.2015.03.016     Document Type: Article

References (64)

1. Antonsson B. Bax and other pro-apoptotic Bcl-2 family "killer-proteins" and their victim the mitochondrion. Cell and Tissue Research 2001, 306:347-361.
2. Cacicedo J.M., Benjachareowong S., Chou E., Ruderman N.B., Ido Y. Palmitate-induced apoptosis in cultured bovine retinal pericytes: Roles of NAD(P)H oxidase, oxidant stress, and ceramide. Diabetes 2005, 54:1838-1845.
3. Carlsson M., Wessman Y., Almgren P., Groop L. High levels of nonesterified fatty acids are associated with increased familial risk of cardiovascular disease. Arteriosclerosis, Thrombosis, and Vascular Biology 2000, 20:1588-1594.
4. Chen X., Liu J., Chen S.Y. Sulforaphane protects against ethanol-induced oxidative stress and apoptosis in neural crest cells by the induction of Nrf2-mediated antioxidant response. British Journal of Pharmacology 2013, 169:437-448.
5. Chen Y.Y., Sun L.Q., Wang B.A., Zou X.M., Mu Y.M., Lu J.M. Palmitate induces autophagy in pancreatic beta-cells via endoplasmic reticulum stress and its downstream JNK pathway. International Journal of Molecular Medicine 2013, 32:1401-1406.
6. Choi S.E., Lee S.M., Lee Y.J., Li L.J., Lee S.J., Lee J.H., Kim Y., Jun H.S., Lee K.W., Kang Y. Protective role of autophagy in palmitate-induced INS-1 beta-cell death. Endocrinology 2009, 150:126-134.
7. Ciechomska I.A., Gabrusiewicz K., Szczepankiewicz A.A., Kaminska B. Endoplasmic reticulum stress triggers autophagy in malignant glioma cells undergoing cyclosporine a-induced cell death. Oncogene 2013, 32:1518-1529.
8. Cunha D.A., Hekerman P., Ladriere L., Bazarra-Castro A., Ortis F., Wakeham M.C., Moore F., Rasschaert J., Cardozo A.K., Bellomo E., Overbergh L., Mathieu C., Lupi R., Hai T., Herchuelz A., Marchetti P., Rutter G.A., Eizirik D.L., Cnop M. Initiation and execution of lipotoxic ER stress in pancreatic beta-cells. Journal of Cell Science 2008, 121:2308-2318.
9. Deng X., Xiao L., Lang W., Gao F., Ruvolo P., May W.S. Novel role for JNK as a stress-activated Bcl2 kinase. Journal of Biological Chemistry 2001, 276:23681-23688.
10. Devi J.R., Thangam E.B. Studies on antioxidant and antimicrobial activities of purified sulforaphane from Brassica oleracea var. rubra. Journal of Pharmacy Research 2012, 5:3582-3584.
11. Dias I.H., Chapple I.L., Milward M., Grant M.M., Hill E., Brown J., Griffiths H.R. Sulforaphane restores cellular glutathione levels and reduces chronic periodontitis neutrophil hyperactivity in vitro. PLoS ONE 2013, 8. e66407.
12. Dou X., Wang Z., Yao T., Song Z. Cysteine aggravates palmitate-induced cell death in hepatocytes. Life Sciences 2011, 89:878-885.
13. Egnatchik R.A., Leamy A.K., Noguchi Y., Shiota M., Young J.D. Palmitate-induced activation of mitochondrial metabolism promotes oxidative stress and apoptosis in H4IIEC3 rat hepatocytes. Metabolism: Clinical and Experimental 2014, 63:283-295.
14. Ellington A.A., Berhow M.A., Singletary K.W. Inhibition of Akt signaling and enhanced ERK1/2 activity are involved in induction of macroautophagy by triterpenoid B-group soyasaponins in colon cancer cells. Carcinogenesis 2006, 27:298-306.
15. Feldstein A.E., Canbay A., Guicciardi M.E., Higuchi H., Bronk S.F., Gores G.J. Diet associated hepatic steatosis sensitizes to Fas mediated liver injury in mice. Journal of Hepatology 2003, 39:978-983.
16. Fu J., Zhang Q., Woods C.G., Zheng H., Yang B., Qu W., Andersen M.E., Pi J. Divergent effects of sulforaphane on basal and glucose-stimulated insulin secretion in beta-cells: Role of reactive oxygen species and induction of endogenous antioxidants. Pharmaceutical Research 2013, 30:2248-2259.
17. Guo L.P., Yang R.Q., Wang Z.Y., Guo Q.H., Gu Z.X. Glucoraphanin, sulforaphane and myrosinase activity in germinating broccoli sprouts as affected by growth temperature and plant organs. Journal of Functional Foods 2014, 9:70-77.
18. Harris C., Hansen J.M. Nrf2-mediated resistance to oxidant-induced redox disruption in embryos. Birth Defects Research. Part B, Developmental and Reproductive Toxicology 2012, 95:213-218.
19. Herman-Antosiewicz A., Johnson D.E., Singh S.V. Sulforaphane causes autophagy to inhibit release of cytochrome C and apoptosis in human prostate cancer cells. Cancer Research 2006, 66:5828-5835.
20. Hickson-Bick D.L., Sparagna G.C., Buja L.M., McMillin J.B. Palmitate-induced apoptosis in neonatal cardiomyocytes is not dependent on the generation of ROS. American Journal of Physiology, Heart and Circulatory Physiology 2002, 282:H656-H664.
21. Hung C.N., Huang H.P., Lii C.K., Liu K.L., Wang C.J. Sulforaphane inhibits smooth muscle cell proliferation and migration by reducing MMP-9 activity via the Ras and RhoA/ROCK pathways. Journal of Functional Foods 2013, 5:1097-1107.
22. Ichimura Y., Waguri S., Sou Y.S., Kageyama S., Hasegawa J., Ishimura R., Saito T., Yang Y., Kouno T., Fukutomi T., Hoshii T., Hirao A., Takagi K., Mizushima T., Motohashi H., Lee M.S., Yoshimori T., Tanaka K., Yamamoto M., Komatsu M. Phosphorylation of p62 activates the Keap1-Nrf2 pathway during selective autophagy. Molecular Cell 2013, 51:618-631.
23. Jakubikova J., Sedlak J., Mithen R., Bao Y. Role of PI3K/Akt and MEK/ERK signaling pathways in sulforaphane- and erucin-induced phase II enzymes and MRP2 transcription, G2/M arrest and cell death in Caco-2 cells. Biochemical Pharmacology 2005, 69:1543-1552.
24. Kabeya Y., Mizushima N., Ueno T., Yamamoto A., Kirisako T., Noda T., Kominami E., Ohsumi Y., Yoshimori T. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO Journal 2000, 19:5720-5728.
25. Kaminski B.M., Weigert A., Brune B., Schumacher M., Wenzel U., Steinhilber D., Stein J., Ulrich S. Sulforaphane potentiates oxaliplatin-induced cell growth inhibition in colorectal cancer cells via induction of different modes of cell death. Cancer Chemotherapy and Pharmacology 2011, 67:1167-1178.
26. Katsoulieris E., Mabley J.G., Samai M., Green I.C., Chatterjee P.K. alpha-Linolenic acid protects renal cells against palmitic acid lipotoxicity via inhibition of endoplasmic reticulum stress. European Journal of Pharmacology 2009, 623:107-112.
27. Khan M.J., Rizwan Alam M., Waldeck-Weiermair M., Karsten F., Groschner L., Riederer M., Hallstrom S., Rockenfeller P., Konya V., Heinemann A., Madeo F., Graier W.F., Malli R. Inhibition of autophagy rescues palmitic acid-induced necroptosis of endothelial cells. Journal of Biological Chemistry 2012, 287:21110-21120.
28. Kim H.S., Montana V., Jang H.J., Parpura V., Kim J.A. Epigallocatechin gallate (EGCG) stimulates autophagy in vascular endothelial cells: A potential role for reducing lipid accumulation. Journal of Biological Chemistry 2013, 288:22693-22705.
29. Kim J., Kundu M., Viollet B., Guan K.L. AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nature Cell Biology 2011, 13:132-141.
30. Kimura S., Noda T., Yoshimori T. Dissection of the autophagosome maturation process by a novel reporter protein, tandem fluorescent-tagged LC3. Autophagy 2007, 3:452-460.
31. Komatsu M., Kurokawa H., Waguri S., Taguchi K., Kobayashi A., Ichimura Y., Sou Y.S., Ueno I., Sakamoto A., Tong K.I., Kim M., Nishito Y., Iemura S., Natsume T., Ueno T., Kominami E., Motohashi H., Tanaka K., Yamamoto M. The selective autophagy substrate p62 activates the stress responsive transcription factor Nrf2 through inactivation of Keap1. Nature Cell Biology 2010, 12:213-223.
32. Kung C.P., Budina A., Balaburski G., Bergenstock M.K., Murphy M. Autophagy in tumor suppression and cancer therapy. Critical Reviews in Eukaryotic Gene Expression 2011, 21:71-100.
33. Kwak M.K., Itoh K., Yamamoto M., Kensler T.W. Enhanced expression of the transcription factor Nrf2 by cancer chemopreventive agents: Role of antioxidant response element-like sequences in the nrf2 promoter. Molecular and Cellular Biology 2002, 22:2883-2892.
34. Lamark T., Kirkin V., Dikic I., Johansen T. NBR1 and p62 as cargo receptors for selective autophagy of ubiquitinated targets. Cell Cycle (Georgetown, Tex.) 2009, 8:1986-1990.
35. Las G., Serada S.B., Wikstrom J.D., Twig G., Shirihai O.S. Fatty acids suppress autophagic turnover in beta-cells. Journal of Biological Chemistry 2011, 286:42534-42544.
36. Lee A.S. The ER chaperone and signaling regulator GRP78/BiP as a monitor of endoplasmic reticulum stress. Methods (San Diego, Calif.) 2005, 35:373-381.
37. Lee J.H., Moon M.H., Jeong J.K., Park Y.G., Lee Y.J., Seol J.W., Park S.Y. Sulforaphane induced adipolysis via hormone sensitive lipase activation, regulated by AMPK signaling pathway. Biochemical and Biophysical Research Communications 2012, 426:492-497.
38. Lee J.W., Park S., Takahashi Y., Wang H.G. The association of AMPK with ULK1 regulates autophagy. PLoS ONE 2010, 5. e15394.
39. Li L., Chen Y., Gibson S.B. Starvation-induced autophagy is regulated by mitochondrial reactive oxygen species leading to AMPK activation. Cellular Signalling 2013, 25:50-65.
40. Li S., Li J., Shen C., Zhang X., Sun S., Cho M., Sun C., Song Z. tert-Butylhydroquinone (tBHQ) protects hepatocytes against lipotoxicity via inducing autophagy independently of Nrf2 activation. Biochimica et Biophysica Acta 2014, 1841:22-33.
41. Lluis L., Taltavull N., Munoz-Cortes M., Sanchez-Martos V., Romeu M., Giralt M., Molinar-Toribio E., Torres J.L., Perez-Jimenez J., Pazos M., Mendez L., Gallardo J.M., Medina I., Nogues M.R. Protective effect of the omega-3 polyunsaturated fatty acids: Eicosapentaenoic acid/docosahexaenoic acid 1:1 ratio on cardiovascular disease risk markers in rats. Lipids in Health and Disease 2013, 12:140.
42. Malhi H., Bronk S.F., Werneburg N.W., Gores G.J. Free fatty acids induce JNK-dependent hepatocyte lipoapoptosis. Journal of Biological Chemistry 2006, 281:12093-12101.
43. Mathew M., Tay E., Cusi K. Elevated plasma free fatty acids increase cardiovascular risk by inducing plasma biomarkers of endothelial activation, myeloperoxidase and PAI-1 in healthy subjects. Cardiovascular Diabetology 2010, 9:9.
44. Mei S., Ni H.M., Manley S., Bockus A., Kassel K.M., Luyendyk J.P., Copple B.L., Ding W.X. Differential roles of unsaturated and saturated fatty acids on autophagy and apoptosis in hepatocytes. The Journal of Pharmacology and Experimental Therapeutics 2011, 339:487-498.
45. Mizushima N., Ohsumi Y., Yoshimori T. Autophagosome formation in mammalian cells. Cell Structure and Function 2002, 27:421-429.
46. Neuschwander-Tetri B.A. Hepatic lipotoxicity and the pathogenesis of nonalcoholic steatohepatitis: The central role of nontriglyceride fatty acid metabolites. Hepatology (Baltimore, Md.) 2010, 52:774-788.
47. Pankiv S., Clausen T.H., Lamark T., Brech A., Bruun J.A., Outzen H., Overvatn A., Bjorkoy G., Johansen T. p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. Journal of Biological Chemistry 2007, 282:24131-24145.
48. Pfaffenbach K.T., Gentile C.L., Nivala A.M., Wang D., Wei Y., Pagliassotti M.J. Linking endoplasmic reticulum stress to cell death in hepatocytes: Roles of C/EBP homologous protein and chemical chaperones in palmitate-mediated cell death. American Journal of Physiology. Endocrinology and Metabolism 2010, 298:E1027-E1035.
49. Rao V.A., Klein S.R., Bonar S.J., Zielonka J., Mizuno N., Dickey J.S., Keller P.W., Joseph J., Kalyanaraman B., Shacter E. The antioxidant transcription factor Nrf2 negatively regulates autophagy and growth arrest induced by the anticancer redox agent mitoquinone. Journal of Biological Chemistry 2010, 285:34447-34459.
50. Shaw R.J. LKB1 and AMP-activated protein kinase control of mTOR signalling and growth. Acta Physiologica 2009, 196:65-80.
51. Shinkai Y., Sumi D., Fukami I., Ishii T., Kumagai Y. Sulforaphane, an activator of Nrf2, suppresses cellular accumulation of arsenic and its cytotoxicity in primary mouse hepatocytes. FEBS Letters 2006, 580:1771-1774.
52. Shintani T., Klionsky D.J. Autophagy in health and disease: A double-edged sword. Science 2004, 306:990-995.
53. Singh R., Cuervo A.M. Autophagy in the cellular energetic balance. Cell Metabolism 2011, 13:495-504.
54. Soardo G., Donnini D., Domenis L., Catena C., De Silvestri D., Cappello D., Dibenedetto A., Carnelutti A., Bonasia V., Pagano C., Sechi L.A. Oxidative stress is activated by free fatty acids in cultured human hepatocytes. Metabolic Syndrome and Related Disorders 2011, 9:397-401.
55. Thimmulappa R.K., Mai K.H., Srisuma S., Kensler T.W., Yamamoto M., Biswal S. Identification of Nrf2-regulated genes induced by the chemopreventive agent sulforaphane by oligonucleotide microarray. Cancer Research 2002, 62:5196-5203.
56. Wakil S.J., Abu-Elheiga L.A. Fatty acid metabolism: Target for metabolic syndrome. Journal of Lipid Research 2009, 50(Suppl.):S138-S143.
57. Wang J., Whiteman M.W., Lian H., Wang G., Singh A., Huang D., Denmark T. A non-canonical MEK/ERK signaling pathway regulates autophagy via regulating Beclin 1. Journal of Biological Chemistry 2009, 284:21412-21424.
58. Wang R.C., Wei Y., An Z., Zou Z., Xiao G., Bhagat G., White M., Reichelt J., Levine B. Akt-mediated regulation of autophagy and tumorigenesis through Beclin 1 phosphorylation. Science 2012, 338:956-959.
59. Wei C.D., Li Y., Zheng H.Y., Sun K.S., Tong Y.Q., Dai W., Wu W., Bao A.Y. Globular adiponectin protects H9c2 cells from palmitate-induced apoptosis via Akt and ERK1/2 signaling pathways. Lipids in Health and Disease 2012, 11:135.
60. Wei C.D., Li Y., Zheng H.Y., Tong Y.Q., Dai W. Palmitate induces H9c2 cell apoptosis by increasing reactive oxygen species generation and activation of the ERK1/2 signaling pathway. Molecular Medicine Reports 2013, 7:855-861.
61. Wilson K.S., Sehn L.H., Berry B., Chhanabhai M., Fitzgerald C.A., Gill K.K., Klasa R., Skinnider B., Sutherland J., Connors J.M., Gascoyne R.D. CHOP-R therapy overcomes the adverse prognostic influence of BCL-2 expression in diffuse large B-cell lymphoma. Leukemia & Lymphoma 2007, 48:1102-1109.
62. Yamagishi S., Okamoto T., Amano S., Inagaki Y., Koga K., Koga M., Choei H., Sasaki N., Kikuchi S., Takeuchi M., Makita Z. Palmitate-induced apoptosis of microvascular endothelial cells and pericytes. Molecular Medicine 2002, 8:179-184.
63. Yuzefovych L.V., Solodushko V.A., Wilson G.L., Rachek L.I. Protection from palmitate-induced mitochondrial DNA damage prevents from mitochondrial oxidative stress, mitochondrial dysfunction, apoptosis, and impaired insulin signaling in rat L6 skeletal muscle cells. Endocrinology 2012, 153:92-100.
64. Zhou H.G., Liu L., Zhang Y., Huang Y.Y., Tao Y.H., Zhang S., Su J.J., Tang Y.P., Guo Z.L., Hu R.M., Dong Q. Glutathione prevents free fatty acids-induced oxidative stress and apoptosis in human brain vascular endothelial cells through Akt pathway. CNS Neuroscience & Therapeutics 2013, 19:252-261.