daf-16/FOXO and glod-4/glyoxalase-1 are required for the life-prolonging effect of human insulin under high glucose conditions in Caenorhabditis elegans

Diabetologia

Volumn 58, Issue 2, 2015, Pages 393-401

  Mendler, Michael ^a   Schlotterer, Andreas ^a   Ibrahim, Youssef ^a   Kukudov, Georgi ^a   Fleming, Thomas ^a   Bierhaus, Angelika ^a   Riedinger, Christin ^a   Schwenger, Vedat ^a   Herzig, Stephan ^a   Hecker, Markus ^a   Tyedmers, Jens ^a   Nawroth, Peter P ^a   Morcos, Michael ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

Diabetic neuropathy; Glycation AGE; Insulin action; Oxidative stress ROS; Transcription factors

Indexed keywords

ADVANCED GLYCATION END PRODUCT; GLOD 4 PROTEIN; GLUCOSE; GLYOXALASE; GLYOXALASE 1; HUMAN INSULIN; HYDROLASE; INSULIN ASPART; INSULIN DETEMIR; REACTIVE OXYGEN METABOLITE; SUPEROXIDE DISMUTASE; TRANSCRIPTION FACTOR DAF 16; TRANSCRIPTION FACTOR FOXO; UNCLASSIFIED DRUG; CAENORHABDITIS ELEGANS PROTEIN; DAF-16 PROTEIN, C ELEGANS; FORKHEAD TRANSCRIPTION FACTOR; LACTOYLGLUTATHIONE LYASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; DIABETES MELLITUS; DIABETIC PATIENT; DRUG EFFECT; ENZYME ACTIVITY; FUNCTIONAL DISEASE; GENE OVEREXPRESSION; GENE REPRESSION; HUMAN; INSULIN TREATMENT; LIFE EXTENSION; LIFESPAN; NEMATODE; NERVE CELL LESION; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; ANIMAL; DNA DAMAGE; DNA REPAIR; GENE EXPRESSION REGULATION; LONGEVITY; METABOLISM; SIGNAL TRANSDUCTION;

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; DNA DAMAGE; DNA REPAIR; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; INSULIN, REGULAR, HUMAN; LACTOYLGLUTATHIONE LYASE; LONGEVITY; SIGNAL TRANSDUCTION;

EID: 84920784087     PISSN: 0012186X     EISSN: 14320428     Source Type: Journal    
DOI: 10.1007/s00125-014-3415-5     Document Type: Article

References (38)

1. Holzenberger M (2009) IGF-1 receptors in the brain control longevity in mice. Med Sci (Paris) 25:371–376 [article in French]
2. Kenyon C, Chang J, Gensch E, Rudner A, Tabtiang R (1993) A C. elegans mutant that lives twice as long as wild type. Nature 366:461–464
3. Narayanan RP, Siddals KW, Heald AH, Gibson JM (2013) Interactions of the IGF system with diabetes and its vascular complications. Exp Clin Endocrinol Diabetes 121:255–261
4. Tatar M, Kopelman A, Epstein D, Tu MP, Yin CM, Garofalo RS (2001) A mutant Drosophila insulin receptor homolog that extends life-span and impairs neuroendocrine function. Science 292:107–110
5. Nawroth PP, Rudofsky G, Humpert P (2010) Have we understood diabetes? New tasks for diagnosis and therapy. Exp Clin Endocrinol Diabetes 118:1–3
6. Lee SJ, Murphy CT, Kenyon C (2009) Glucose shortens the life span of C. elegans by downregulating DAF-16/FOXO activity and aquaporin gene expression. Cell Metab 10:379–391
7. Mendler M, Schlotterer A, Morcos M, Nawroth PP (2012) Understanding diabetic polyneuropathy and longevity: what can we learn from the nematode Caenorhabditis elegans? Exp Clin Endocrinol Diabetes 120:182–183
8. Schlotterer A, Kukudov G, Bozorgmehr F et al (2009) C. elegans as model for the study of high glucose-mediated life span reduction. Diabetes 58:2450–2456
9. Schulz TJ, Zarse K, Voigt A, Urban N, Birringer M, Ristow M (2007) Glucose restriction extends Caenorhabditis elegans life span by inducing mitochondrial respiration and increasing oxidative stress. Cell Metab 6:280–293
10. Thornalley PJ (2003) Glyoxalase I–structure, function and a critical role in the enzymatic defence against glycation. Biochem Soc Trans 31:1343–1348
11. Bierhaus A, Fleming T, Stoyanov S et al (2012) Methylglyoxal modification of Nav1.8 facilitates nociceptive neuron firing and causes hyperalgesia in diabetic neuropathy. Nat Med 18:926–933
12. Fleming T, Cuny J, Nawroth G et al (2012) Is diabetes an acquired disorder of reactive glucose metabolites and their intermediates? Diabetologia 55:1151–1155
13. Fleming TH, Humpert PM, Nawroth PP, Bierhaus A (2011) Reactive metabolites and AGE/RAGE-mediated cellular dysfunction affect the aging process: a mini-review. Gerontology 57:435–443
14. Schlotterer A, Hamann A, Kukudov G et al (2010) Apurinic/apyrimidinic endonuclease 1, p53, and thioredoxin are linked in control of aging in C. elegans. Aging Cell 9:420–432
15. Vander Jagt DL (2008) Methylglyoxal, diabetes mellitus and diabetic complications. Drug Metabol Drug Interact 23:93–124
16. Morcos M, Du X, Pfisterer F et al (2008) Glyoxalase-1 prevents mitochondrial protein modification and enhances lifespan in Caenorhabditis elegans. Aging Cell 7:260–269
17. Kenyon C (2005) The plasticity of aging: insights from long-lived mutants. Cell 120:449–460
18. Kimura KD, Tissenbaum HA, Liu Y, Ruvkun G (1997) daf-2, an insulin receptor-like gene that regulates longevity and diapause in Caenorhabditis elegans. Science 277:942–946
19. Pierce SB, Costa M, Wisotzkey R et al (2001) Regulation of DAF-2 receptor signaling by human insulin and ins-1, a member of the unusually large and diverse C. elegans insulin gene family. Genes Dev 15:672–686
20. Altun-Gultekin Z, Andachi Y, Tsalik EL, Pilgrim D, Kohara Y, Hobert O (2001) A regulatory cascade of three homeobox genes, ceh-10, ttx-3 and ceh-23, controls cell fate specification of a defined interneuron class in C. elegans. Development 128:1951–1969
21. McLellan AC, Thornalley PJ, Benn J, Sonksen PH (1994) Glyoxalase system in clinical diabetes mellitus and correlation with diabetic complications. Clin Sci (Lond) 87:21–29
22. Racker E (1951) The mechanism of action of glyoxalase. J Biol Chem 190:685–696
23. Abramoff MD, Magelhaes PJ, Ram SJ (2004) Image processing with ImageJ. Biophoton Int 11:36–42
24. Schumacher B, Schertel C, Wittenburg N et al (2005) C. elegans ced-13 can promote apoptosis and is induced in response to DNA damage. Cell Death Differ 12:153–161
25. Herrmann BL, Kasser C, Keuthage W, Huptas M, Dette H, Klute A (2013) Comparison of insulin aspart vs. regular human insulin with or without insulin detemir concerning adipozytokines and metabolic effects in patients with type 2 diabetes mellitus. Exp Clin Endocrinol Diabetes 121:210–213
26. Yin D (1996) Biochemical basis of lipofuscin, ceroid, and age pigment-like fluorophores. Free Radic Biol Med 21:871–888
27. Gerstbrein B, Stamatas G, Kollias N, Driscoll M (2005) In vivo spectrofluorimetry reveals endogenous biomarkers that report healthspan and dietary restriction in Caenorhabditis elegans. Aging Cell 4:127–137
28. Priebe S, Menzel U, Zarse K et al (2013) Extension of life span by impaired glucose metabolism in Caenorhabditis elegans is accompanied by structural rearrangements of the transcriptomic network. PLoS One 8:e77776
29. Honda Y, Honda S (1999) The daf-2 gene network for longevity regulates oxidative stress resistance and Mn-superoxide dismutase gene expression in Caenorhabditis elegans. FASEB J 13:1385–1393
30. Zarse K, Schmeisser S, Groth M et al (2012) Impaired insulin/IGF1 signaling extends life span by promoting mitochondrial L-proline catabolism to induce a transient ROS signal. Cell Metab 15:451–465
31. Schmoll D, Walker KS, Alessi DR et al (2000) Regulation of glucose-6-phosphatase gene expression by protein kinase Balpha and the forkhead transcription factor FKHR. Evidence for insulin response unit-dependent and -independent effects of insulin on promoter activity. J Biol Chem 275:36324–36333
32. Hall RK, Yamasaki T, Kucera T, Waltner-Law M, O'Brien R, Granner DK (2000) Regulation of phosphoenolpyruvate carboxykinase and insulin-like growth factor-binding protein-1 gene expression by insulin. The role of winged helix/forkhead proteins. J Biol Chem 275:30169–30175
33. Matsumoto M, Pocai A, Rossetti L, Depinho RA, Accili D (2007) Impaired regulation of hepatic glucose production in mice lacking the forkhead transcription factor Foxo1 in liver. Cell Metab 6:208–216
34. Skriver MV, Borch-Johnsen K, Lauritzen T, Sandbaek A (2010) HbA1c as predictor of all-cause mortality in individuals at high risk of diabetes with normal glucose tolerance, identified by screening: a follow-up study of the Anglo-Danish-Dutch Study of Intensive Treatment in People with Screen-Detected Diabetes in Primary Care (ADDITION), Denmark. Diabetologia 53:2328–2333
35. Ahmed N, Thornalley PJ, Dawczynski J et al (2003) Methylglyoxal-derived hydroimidazolone advanced glycation end-products of human lens proteins. Invest Ophthalmol Vis Sci 44:5287–5292
36. Genuth S, Sun W, Cleary P et al (2005) Glycation and carboxymethyllysine levels in skin collagen predict the risk of future 10-year progression of diabetic retinopathy and nephropathy in the diabetes control and complications trial and epidemiology of diabetes interventions and complications participants with type 1 diabetes. Diabetes 54:3103–3111
37. Birkenmeier G, Stegemann C, Hoffmann R, Gunther R, Huse K, Birkemeyer C (2010) Posttranslational modification of human glyoxalase 1 indicates redox-dependent regulation. PLoS One 5:e10399
38. Reger MA, Watson GS, Green PS et al (2008) Intranasal insulin administration dose-dependently modulates verbal memory and plasma amyloid-beta in memory-impaired older adults. J Alzheimers Dis 13:323–331