Nutritional energy stimulates NAD+ production to promote tankyrase-mediated PARsylation in insulinoma cells

PLoS ONE

Volumn 10, Issue 4, 2015, Pages

  Zhong, Linlin ^a,b   Yeh, Tsung Yin J ^b   Hao, Jun ^b,c   Pourtabatabaei, Nasim ^b   Mahata, Sushil K ^a,b   Shao, Jianhua ^d   Chessler, Steven D ^e   Chi, Nai Wen ^a,b  

^a VA SAN DIEGO HEALTHCARE SYSTEM   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^c HEBEI MEDICAL UNIVERSITY   (China)

^d UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; AMINO ACID; GLUCOSE; NICOTINAMIDE ADENINE DINUCLEOTIDE; NICOTINAMIDE NUCLEOTIDE; NICOTINAMIDE PHOSPHORIBOSYLTRANSFERASE; PROTEASOME; PYRUVIC ACID; SIRTUIN; TANKYRASE; UBIQUITIN; ACRYLAMIDE DERIVATIVE; N-(4-(1-BENZOYLPIPERIDIN-4-YL)BUTYL)-3-(PYRIDIN-3-YL)ACRYLAMIDE; PIPERIDINE DERIVATIVE; TANKYRASE 1, RAT; TNKS PROTEIN, HUMAN;

ADENOSINE DIPHOSPHATE RIBOSYLATION; ANIMAL CELL; ARTICLE; CATALYSIS; CELL ENERGY; CELL STIMULATION; CONTROLLED STUDY; ENERGY METABOLISM; ENZYME REGULATION; HUMAN; HUMAN CELL; IN VITRO STUDY; INSULINOMA; MOUSE; NONHUMAN; PROTEIN CONTENT; PROTEIN DEGRADATION; PURINE SYNTHESIS; SIGNAL TRANSDUCTION; 3T3 CELL LINE; ANIMAL; CHEMISTRY; GENETICS; HEK293 CELL LINE; PATHOLOGY; PROTEIN PROCESSING; RAT;

3T3 CELLS; ACRYLAMIDES; ADENOSINE TRIPHOSPHATE; ANIMALS; CATALYSIS; ENERGY METABOLISM; GLUCOSE; HEK293 CELLS; HUMANS; INSULINOMA; MICE; NAD; NICOTINAMIDE PHOSPHORIBOSYLTRANSFERASE; PIPERIDINES; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN PROCESSING, POST-TRANSLATIONAL; RATS; TANKYRASES; UBIQUITIN;

EID: 84929485531     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0122948     Document Type: Article

References (50)

1. Mouchiroud L, Houtkooper RH, Auwerx J (2013) NAD(+) metabolism: a therapeutic target for age-related metabolic disease. Crit Rev Biochem Mol Biol 48: 397-408. doi: 10.3109/10409238.2013.789479 PMID: 23742622
2. Lehtio L, Chi NW, Krauss S (2013) Tankyrases as drug targets. FEBS J 280: 3576-3593. doi: 10.1111/febs.12320 PMID: 23648170
3. Seimiya H, Muramatsu Y, Smith S, Tsuruo T (2004) Functional subdomain in the ankyrin domain of tankyrase1 required for poly(ADP-ribosyl)ation of TRF1 and telomere elongation. Mol Cell Biol 24: 1944-1955. PMID: 14966275
4. Huang SM, Mishina YM, Liu S, Cheung A, Stegmeier F, et al. (2009) Tankyrase inhibition stabilizes axin and antagonizes Wnt signalling. Nature 461: 614-620. doi: 10.1038/nature08356 PMID: 19759537
5. Guo HL, Zhang C, Liu Q, Li Q, Lian G, et al. (2012) The Axin/TNKS complex interacts with KIF3A and is required for insulin-stimulated GLUT4 translocation. Cell Res 22: 1246-1257. doi: 10.1038/cr.2012.52 PMID: 22473005
6. Yeh TY, Sbodio JI, Tsun ZY, Luo B, Chi NW (2007) Insulin-stimulated exocytosis of GLUT4 is enhanced by IRAP and its partner tankyrase. Biochem J 402: 279-290. PMID: 17059388
7. Yeh TY, Sbodio JI, Nguyen MT, Meyer TN, Lee RM, et al. (2005) Tankyrase-1 overexpression reduces genotoxin-induced cell death by inhibiting PARP1. Mol Cell Biochem 276: 183-192. PMID: 16132700
8. Yeh TY, Meyer TN, Schwesinger C, Tsun ZY, Lee RM, et al. (2006) Tankyrase recruitment to the lateral membrane in polarized epithelial cells: regulation by cell-cell contact and protein poly(ADP-ribosyl) ation. Biochem J 399: 415-425. PMID: 16884355
9. Zhang Y, Liu S, Mickanin C, Feng Y, Charlat O, et al. (2011) RNF146 is a poly(ADP-ribose)-directed E3 ligase that regulates axin degradation and Wnt signalling. Nat Cell Biol 13: 623-629. doi: 10.1038/ncb2222 PMID: 21478859
10. Chi NW, Lodish HF (2000) Tankyrase is a Golgi-associated mitogen-activated protein kinase substrate that interacts with IRAP in GLUT4 vesicles. J Biol Chem 275: 38437-38444. PMID: 10988299
11. Canto C, Auwerx J (2012) Targeting sirtuin 1 to improve metabolism: all you need is NAD(+)? Pharmacol Rev 64: 166-187. doi: 10.1124/pr.110.003905 PMID: 22106091
12. Peek CB, Affinati AH, Ramsey KM, Kuo HY, Yu W, et al. (2013) Circadian clock NAD+ cycle drives mitochondrial oxidative metabolism in mice. Science 342: 1243417. doi: 10.1126/science.1243417 PMID: 24051248
13. Rippmann JF, Damm K, Schnapp A (2002) Functional characterization of the poly(ADP-ribose) polymerase activity of tankyrase 1, a potential regulator of telomere length. J Mol Biol 323: 217-224. PMID: 12381316
14. Burgos ES (2011) NAMPT in regulated NAD biosynthesis and its pivotal role in human metabolism. Curr Med Chem 18: 1947-1961. PMID: 21517777
15. Fulco M, Cen Y, Zhao P, Hoffman EP, McBurney MW, et al. (2008) Glucose restriction inhibits skeletal myoblast differentiation by activating SIRT1 through AMPK-mediated regulation of Nampt. Dev Cell 14: 661-673. doi: 10.1016/j.devcel.2008.02.004 PMID: 18477450
16. Burgos ES, Ho MC, Almo SC, Schramm VL (2009) A phosphoenzyme mimic, overlapping catalytic sites and reaction coordinate motion for human NAMPT. Proc Natl Acad Sci U S A 106: 13748-13753. doi: 10.1073/pnas.0903898106 PMID: 19666527
17. Hara N, Yamada K, Shibata T, Osago H, Tsuchiya M (2011) Nicotinamide phosphoribosyltransferase/visfatin does not catalyze nicotinamide mononucleotide formation in blood plasma. PLoS One 6: e22781. doi: 10.1371/journal.pone.0022781 PMID: 21826208
18. Wang T, Zhang X, Bheda P, Revollo JR, Imai S, et al. (2006) Structure of Nampt/PBEF/visfatin, a mammalian NAD+ biosynthetic enzyme. Nat Struct Mol Biol 13: 661-662. PMID: 16783373
19. Zhao Y, Liu XZ, Tian WW, Guan YF, Wang P, et al. (2014) Extracellular visfatin has nicotinamide phosphoribosyltransferase enzymatic activity and is neuroprotective against ischemic injury. CNS Neurosci Ther 20: 539-547. doi: 10.1111/cns.12273 PMID: 24750959
20. Wiederkehr A, Wollheim CB (2012) Mitochondrial signals drive insulin secretion in the pancreatic betacell. Mol Cell Endocrinol 353: 128-137. doi: 10.1016/j.mce.2011.07.016 PMID: 21784130
21. Kover K, Tong PY, Watkins D, Clements M, Stehno-Bittel L, et al. (2013) Expression and regulation of nampt in human islets. PLoS One 8: e58767. doi: 10.1371/journal.pone.0058767 PMID: 23536823
22. Haigis MC, Mostoslavsky R, Haigis KM, Fahie K, Christodoulou DC, et al. (2006) SIRT4 inhibits glutamate dehydrogenase and opposes the effects of calorie restriction in pancreatic beta cells. Cell 126: 941-954. PMID: 16959573
23. Bordone L, Motta MC, Picard F, Robinson A, Jhala US, et al. (2006) Sirt1 regulates insulin secretion by repressing UCP2 in pancreatic beta cells. PLoS Biol 4: e31. PMID: 16366736
24. Suckow AT, Craige B, Faundez V, Cain WJ, Chessler SD (2010) An AP-3-dependent mechanism drives synaptic-like microvesicle biogenesis in pancreatic islet beta-cells. Am J Physiol Endocrinol Metab 299: E23-32. doi: 10.1152/ajpendo.00664.2009 PMID: 20442321
25. Lee YS, Morinaga H, Kim JJ, LagakosW, Taylor S, et al. (2013) The fractalkine/CX3CR1 system regulates beta cell function and insulin secretion. Cell 153: 413-425. doi: 10.1016/j.cell.2013.03.001 PMID: 23582329
26. Grimsby J, Sarabu R, Corbett WL, Haynes NE, Bizzarro FT, et al. (2003) Allosteric activators of glucokinase: potential role in diabetes therapy. Science 301: 370-373. PMID: 12869762
27. Kamitani T, Kito K, Fukuda-Kamitani T, Yeh ET (2001) Targeting of NEDD8 and its conjugates for proteasomal degradation by NUB1. J Biol Chem 276: 46655-46660. PMID: 11585840
28. Germain M, Affar EB, D'Amours D, Dixit VM, Salvesen GS, et al. (1999) Cleavage of automodified poly (ADP-ribose) polymerase during apoptosis. Evidence for involvement of caspase-7. J Biol Chem 274: 28379-28384. PMID: 10497198
29. Yeh TY, Beiswenger KK, Li P, Bolin KE, Lee RM, et al. (2009) Hypermetabolism, hyperphagia, and reduced adiposity in tankyrase-deficient mice. Diabetes 58: 2476-2485. doi: 10.2337/db08-1781 PMID: 19651815
30. Caton PW, Richardson SJ, Kieswich J, Bugliani M, Holland ML, et al. (2013) Sirtuin 3 regulates mouse pancreatic beta cell function and is suppressed in pancreatic islets isolated from human type 2 diabetic patients. Diabetologia 56: 1068-1077. doi: 10.1007/s00125-013-2851-y PMID: 23397292
31. Tan B, Young DA, Lu ZH, Wang T, Meier TI, et al. (2013) Pharmacological inhibition of nicotinamide phosphoribosyltransferase (NAMPT), an enzyme essential for NAD+ biosynthesis, in human cancer cells: metabolic basis and potential clinical implications. J Biol Chem 288: 3500-3511. doi: 10.1074/jbc.M112.394510 PMID: 23239881
32. Houtkooper RH, Canto C, Wanders RJ, Auwerx J (2010) The secret life of NAD+: an old metabolite controlling new metabolic signaling pathways. Endocr Rev 31: 194-223. doi: 10.1210/er.2009-0026 PMID: 20007326
33. Virag L, Szabo C (2002) The therapeutic potential of poly(ADP-ribose) polymerase inhibitors. Pharmacol Rev 54: 375-429. PMID: 12223530
34. Service FJ (1995) Hypoglycemic disorders. N Engl J Med 332: 1144-1152. PMID: 7700289
35. Nathan DM, Davidson MB, DeFronzo RA, Heine RJ, Henry RR, et al. (2007) Impaired fasting glucose and impaired glucose tolerance: implications for care. Diabetes Care 30: 753-759. PMID: 17327355
36. Idevall-Hagren O, Barg S, Gylfe E, Tengholm A (2010) cAMP mediators of pulsatile insulin secretion from glucose-stimulated single beta-cells. J Biol Chem 285: 23007-23018. doi: 10.1074/jbc.M109.095992 PMID: 20498366
37. Dezaki K, Damdindorj B, Sone H, Dyachok O, Tengholm A, et al. (2011) Ghrelin attenuates cAMP-PKA signaling to evoke insulinostatic cascade in islet beta-cells. Diabetes 60: 2315-2324. doi: 10.2337/db11-0368 PMID: 21788571
38. Goehring I, Gerencser AA, Schmidt S, Brand MD, Mulder H, et al. (2012) Plasma membrane potential oscillations in insulin secreting Ins-1 832/13 cells do not require glycolysis and are not initiated by fluctuations in mitochondrial bioenergetics. J Biol Chem 287: 15706-15717. doi: 10.1074/jbc.M111.314567 PMID: 22418435
39. Chang P, Coughlin M, Mitchison TJ (2005) Tankyrase-1 polymerization of poly(ADP-ribose) is required for spindle structure and function. Nat Cell Biol 7: 1133-1139. PMID: 16244666
40. Matschinsky FM (2005) Glucokinase, glucose homeostasis, and diabetes mellitus. Curr Diab Rep 5: 171-176. PMID: 15929862
41. Lee SJ, Kim HE, Choi SE, Shin HC, Kwag WJ, et al. (2009) Involvement of Ca2+/calmodulin kinase II (CaMK II) in genistein-induced potentiation of leucine/glutamine-stimulated insulin secretion. Mol Cells 28: 167-174. doi: 10.1007/s10059-009-0119-7 PMID: 19756396
42. Furst P, Albers S, Stehle P (1989) Availability of glutamine supplied intravenously as alanylglutamine. Metabolism 38: 67-72. PMID: 2668705
43. Lau C, Dolle C, Gossmann TI, Agledal L, Niere M, et al. (2010) Isoform-specific targeting and interaction domains in human nicotinamide mononucleotide adenylyltransferases. J Biol Chem 285: 18868-18876. doi: 10.1074/jbc.M110.107631 PMID: 20388704
44. Feng X, Koh DW (2013) Roles of poly(ADP-ribose) glycohydrolase in DNA damage and apoptosis. Int Rev Cell Mol Biol 304: 227-281. doi: 10.1016/B978-0-12-407696-9.00005-1 PMID: 23809438
45. Chen D, Bruno J, Easlon E, Lin SJ, Cheng HL, et al. (2008) Tissue-specific regulation of SIRT1 by calorie restriction. Genes Dev 22: 1753-1757. doi: 10.1101/gad.1650608 PMID: 18550784
46. Shimoyama M, Ohota M, Kakehi K, Ueda I (1970) Increase of NAD glycohydrolase activity and decrease of NAD concentration in rat liver during fasting. Biochim Biophys Acta 215: 207-209. PMID: 4321965
47. Kronfeld DS, Raggi F (1964) Nicotinamide coenzyme concentrations in livers of normal, starved and alloxan-diabetic rats. Biochem J 93: 517-520. PMID: 4378756
48. Ramsey KM, Yoshino J, Brace CS, Abrassart D, Kobayashi Y, et al. (2009) Circadian clock feedback cycle through NAMPT-mediated NAD+ biosynthesis. Science 324: 651-654. doi: 10.1126/science.1171641 PMID: 19299583
49. Sbodio JI, Chi NW (2002) Identification of a tankyrase-binding motif shared by IRAP, TAB182, and human TRF1 but not mouse TRF1. NuMA contains this RxxPDG motif and is a novel tankyrase partner. The Journal of biological chemistry. 277: 31887-92. PMID: 12080061
50. Johnson D, Shepherd RM, Gill D, Gorman T, Smith DM, et al. (2007) Glucose-dependent modulation of insulin secretion and intracellular calcium ions by GKA50, a glucokinase activator. Diabetes. 56: 1694-702. PMID: 17360975