Trehalose inhibits solute carrier 2A (SLC2A) proteins to induce autophagy and prevent hepatic steatosis

Science Signaling

Volumn 9, Issue 416, 2016, Pages

  DeBosch, Brian J ^a   Heitmeier, Monique R ^a   Mayer, Allyson L ^a   Higgins, Cassandra B ^a   Crowley, Jan R ^a   Kraft, Thomas E ^a   Chi, Maggie ^a   Newberry, Elizabeth P ^a   Chen, Zhouji ^a   Finck, Brian N ^a   Davidson, Nicholas O ^a   Yarasheski, Kevin E ^a   Hruz, Paul W ^a   Moley, Kelle H ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACYL COENZYME A DESATURASE; ADENOSINE PHOSPHATE; GLUCOSE TRANSPORTER; GLUCOSE TRANSPORTER 1; GLUCOSE TRANSPORTER 2; GLUCOSE TRANSPORTER 3; GLUCOSE TRANSPORTER 4; GLUCOSE TRANSPORTER 8; SHORT HAIRPIN RNA; TREHALOSE; UNCLASSIFIED DRUG; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; BIOCHEMICAL ANALYSIS; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVATION; ENZYME SPECIFICITY; FATTY LIVER; FEMALE; GLUCOSE TRANSPORT; HEXOSE TRANSPORT; IC50; IN VIVO STUDY; LIPID STORAGE; LIVER CELL; LIVER CELL CULTURE; MALE; MOUSE; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; ANIMAL; GENETICS; HEK293 CELL LINE; HEP-G2 CELL LINE; HUMAN; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; AUTOPHAGY; FATTY LIVER; GLUCOSE TRANSPORT PROTEINS, FACILITATIVE; HEK293 CELLS; HEP G2 CELLS; HUMANS; MICE; MICE, KNOCKOUT; TREHALOSE;

EID: 84959345504     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.aac5472     Document Type: Article

References (36)

1. R. Loomba, A. J. Sanyal, The global NAFLD epidemic. Nat. Rev. Gastroenterol. Hepatol. 10, 686-690 (2013).
2. B. J. DeBosch, Z. Chen, J. L. Saben, B. N. Finck, K. H. Moley, Glucose transporter 8 (GLUT8) mediates fructose-induced de novo lipogenesis and macrosteatosis. J. Biol. Chem. 289, 10989-10998 (2014).
3. M. Mueckler, B. Thorens, The SLC2 (GLUT) family of membrane transporters. Mol. Aspects Med. 34, 121-138 (2013).
4. M. C. Towler, D. G. Hardie, AMP-activated protein kinase in metabolic control and insulin signaling. Circ. Res. 100, 328-341 (2007).
5. R. C. Russell, H.-X. Yuan, K.-L. Guan, Autophagy regulation by nutrient signaling. Cell Res. 24, 42-57 (2014).
6. J. Kim, M. Kundu, B. Viollet, K.-L. Guan, AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat. Cell Biol. 13, 132-141 (2011).
7. C. A. Colville, M. J. Seatter, T. J. Jess, G. W. Gould, H. M. Thomas, Kinetic analysis of the liver-type (GLUT2) and brain-type (GLUT3) glucose transporters in Xenopus oocytes: Substrate specificities and effects of transport inhibitors. Biochem. J. 290, 701-706 (1993).
8. E. Shukla, L. J. Thorat, B. B. Nath, S. M. Gaikwad, Insect trehalase: Physiological significance and potential applications. Glycobiology 25, 357-367 (2015).
9. S. Sarkar, J. E. Davies, Z. Huang, A. Tunnacliffe, D. C. Rubinsztein, Trehalose, a novel mTOR-independent autophagy enhancer, accelerates the clearance of mutant huntingtin and a-synuclein. J. Biol. Chem. 282, 5641-5652 (2007).
10. K. Castillo, M. Nassif, V. Valenzuela, F. Rojas, S. Matus, G. Mercado, F. A. Court, B. Van Zundert, C. Hetz, Trehalose delays the progression of amyotrophic lateral sclerosis by enhancing autophagy in motoneurons. Autophagy 9, 1308-1320 (2013).
11. Y. Aguib, A. Heiseke, S. Gilch, C. Riemer, M. Baier, A. Ertmer, H. M. Schätzl, Autophagy induction by trehalose counter-acts cellular prion infection. Autophagy 5, 361-369 (2009).
12. D. J. Klionsky, F. C. Abdalla, H. Abeliovich, R. T. Abraham, A. Acevedo-Arozena, K. Adeli, L. Agholme, M. Agnello, P. Agostinis, J. A. Aguirre-Ghiso, H. J. Ahn, O. Ait-Mohamed, S. Ait-Si-Ali, T. Akematsu, S. Akira, H. M. Al-Younes, M. A. Al-Zeer, M. L. Albert, R. L. Albin, J. Alegre-Abarrategui, M. F. Aleo, M. Alirezaei, A. Almasan, M. Almonte-Becerril, A. Amano, R. K. Amaravadi, S. Amarnath, A. O. Amer, N. Andrieu-Abadie, V. Anantharam, D. K. Ann, S. Anoopkumar-Dukie, H. Aoki, N. Apostolova, G. Arancia, J. P. Aris, K. Asanuma, N. Y. O. Asare, H. Ashida, V. Askanas, D. S. Askew, P. Auberger, M. Baba, S. K. Backues, E. H. Baehrecke, B. A. Bahr, X.-Y. Bai, Y. Bailly, R. Baiocchi, G. Baldini, W. Balduini, A. Ballabio, B. A. Bamber, E. T.W. Bampton, G. Juhász, C. R. Bartholomew, D. C. Bassham, R. C. Bast, H. Batoko, B.-H. Bay, I. Beau, D. M. Béchet, T. J. Begley, C. Behl, C. Behrends, S. Bekri, B. Bellaire, L. J. Bendall, L. Benetti, L. Berliocchi, H. Bernardi, F. Bernassola, S. Besteiro, I. Bhatia-Kissova, X. Bi, M. Biard-Piechaczyk, J. S. Blum, L. H. Boise, P. Bonaldo, D. L. Boone, Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 8, 445-544 (2012).
13. J. L. Schneider, A. M. Cuervo, Liver autophagy: Much more than just taking out the trash. Nat. Rev. Gastroenterol. Hepatol. 11, 187-200 (2014).
14. D. Deng, C. Xu, P. Sun, J. Wu, C. Yan, M. Hu, N. Yan, Crystal structure of the human glucose transporter GLUT1. Nature 510, 121-125 (2014).
15. A. R. Manolescu, R. Augustin, K. Moley, C. Cheeseman, A highly conserved hydrophobic motif in the exofacial vestibule of fructose transporting SLC2A proteins acts as a critical determinant of their substrate selectivity. Mol. Membr. Biol. 24, 455-463 (2007).
16. T. E. Kraft, C. Armstrong, M. R. Heitmeier, A. R. Odom, P. W. Hruz, The glucose transporter PfHT1 Is an antimalarial target of the HIV protease inhibitor lopinavir. Antimicrob. Agents Chemother. 59, 6203-6209 (2015).
17. O. H. Lowry, Amplification by enzymatic cycling. Mol. Cell. Biochem. 32, 135-146 (1980).
18. K. Omurtag, P. Esakky, B. J. Debosch, E. L. Schoeller, M. M. Chi, K. H. Moley, Modeling the effect of cigarette smoke on hexose utilization in spermatocytes. Reprod. Sci. 22, 94-101 (2015).
19. F. Moruno, E. Pérez-Jiménez, E. Knecht, Regulation of autophagy by glucose in mammalian cells. Cells 1, 372-395 (2012).
20. R. C. Hresko, T. E. Kraft, A. Tzekov, S. Wildman, P. W. Hruz, Isoform-selective inhibition of facilitative glucose transporters: Elucidation of the molecular mechanism of HIV protease inhibitor binding. J. Biol. Chem. 289, 16100-16113 (2014).
21. J. Haspel, R. S. Shaik, E. Ifedigbo, K. Nakahira, T. Dolinay, J. A. Englert, A. M. K. Choi, Characterization of macroautophagic flux in vivo using a leupeptin-based assay. Autophagy 7, 629-642 (2011).
22. R. Singh, A. M. Cuervo, Autophagy in the cellular energetic balance. Cell Metab. 13, 495-504 (2011).
23. M. A. Lanaspa, L. G. Sanchez-Lozada, C. Cicerchi, N. Li, C. A. Roncal-Jimenez, T. Ishimoto, M. Le, G. E. Garcia, J. B. Thomas, C. J. Rivard, A. Andres-Hernando, B. Hunter, G. Schreiner, B. Rodriguez-Iturbe, Y. Y. Sautin, R. J. Johnson, Uric acid stimulates fructokinase and accelerates fructose metabolism in the development of fatty liver. PLOS One 7, e47948 (2012).
24. K. Cadwell, J. Y. Liu, S. L. Brown, H. Miyoshi, J. Loh, J. K. Lennerz, C. Kishi, W. Kc, J. A. Carrero, S. Hunt, C. D. Stone, E. M. Brunt, R. J. Xavier, B. P. Sleckman, E. Li, N. Mizushima, T. S. Stappenbeck, H. W. Virgin IV, A key role for autophagy and the autophagy gene Atg16l1 in mouse and human intestinal Paneth cells. Nature 456, 259-263 (2008).
25. Y. Xie, H. Y. J. Fung, E. P. Newberry, S. Kennedy, J. Luo, R. M. Crooke, M. J. Graham, N. O. Davidson, Hepatic Mttp deletion reverses gallstone susceptibility in L-Fabp knockout mice. J. Lipid Res. 55, 540-548 (2014).
26. K. Sodhi, N. Puri, G. Favero, S. Stevens, C. Meadows, N. G. Abraham, R. Rezzani, H. Ansinelli, E. Lebovics, J. I. Shapiro, Fructose mediated non-alcoholic fatty liver is attenuated by HO-1-SIRT1 module in murine hepatocytes and mice fed a high fructose diet. PLOS One 10, e0128648 (2015).
27. B. J. DeBosch, M. Chi, K. H. Moley, Glucose transporter 8 (GLUT8) regulates enterocyte fructose transport and global mammalian fructose utilization. Endocrinology 153, 4181-4191 (2012).
28. B. J. DeBosch, Z. Chen, B. N. Finck, M. Chi, K. H. Moley, Glucose transporter-8 (GLUT8) mediates glucose intolerance and dyslipidemia in high-fructose diet-fed male mice. Mol. Endocrinol. 27, 1887-1896 (2013).
29. I. Pernicova, M. Korbonits, Metformin-mode of action and clinical implications for diabetes and cancer. Nat. Rev. Endocrinol. 10, 143-156 (2014).
30. S. Alers, A. S. Löffler, S. Wesselborg, B. Stork, Role of AMPK-mTOR-Ulk1/2 in the regulation of autophagy: Cross talk, shortcuts, and feedbacks. Mol. Cell. Biol. 32, 2-11 (2012).
31. B. Levine, G. Kroemer, Autophagy in the pathogenesis of disease. Cell 132, 27-42 (2008).
32. K. M. Tordjman, K. A. Leingang, D. E. James, M. M. Mueckler, Differential regulation of two distinct glucose transporter species expressed in 3T3-L1 adipocytes: Effect of chronic insulin and tolbutamide treatment. Proc. Natl. Acad. Sci. U.S.A. 86, 7761-7765 (1989).
33. B. J. DeBosch, O. Kluth, H. Fujiwara, A. Schürmann, K. Moley, Early-onset metabolic syndrome in mice lacking the intestinal uric acid transporter SLC2A9. Nat. Commun. 5, 4642 (2014).
34. R. Dentin, J.-P. Pégorier, F. Benhamed, F. Foufelle, P. Ferré, V. Fauveau, M. A. Magnuson, J. Girard, C. Postic, Hepatic glucokinase is required for the synergistic action of ChREBP and SREBP-1c on glycolytic and lipogenic gene expression. J. Biol. Chem. 279, 20314-20326 (2004).
35. R. Dentin, F. Benhamed, I. Hainault, V. Fauveau, F. Foufelle, J. R. B. Dyck, J. Girard, C. Postic, Liver-specific inhibition of ChREBP improves hepatic steatosis and insulin resistance in ob/ob mice. Diabetes 55, 2159-2170 (2006).
36. D. A. Fraser, J. Thoen, A. C. Rustan, O. Førre, J. Kjeldsen-Kragh, Changes in plasma free fatty acid concentrations in rheumatoid arthritis patients during fasting and their effects upon T-lymphocyte proliferation. Rheumatology. 38, 948-952 (1999).