Control of metabolic homeostasis by stress signaling is mediated by the Lipocalin NLaz

PLoS Genetics

Volumn 5, Issue 4, 2009, Pages

  Hull Thompson, Julie ^a   Muffat, Julien ^b   Sanchez, Diego ^c   Walker, David W ^b,d   Benzer, Seymour ^b   Ganfornina, Maria D ^c   Jasper, Heinrich ^a  

^a UNIVERSITY OF ROCHESTER   (United States)

^b CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^c UNIVERSITY OF VALLADOLID   (Spain)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APOLIPOPROTEIN D; INSULIN; LIPOCALIN; NEURAL LAZARILLO PROTEIN; RETINOL BINDING PROTEIN 4; SOMATOMEDIN; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG; CARRIER PROTEIN; DROSOPHILA PROTEIN; GLUCOSE; MEMBRANE PROTEIN; NEURAL LAZARILLO PROTEIN, DROSOPHILA;

ARTICLE; DROSOPHILA; GENE ACTIVITY; GENE FUNCTION; GENE OVEREXPRESSION; GENE REPRESSION; GENETIC TRANSCRIPTION; GROWTH INHIBITION; HOMEOSTASIS; INSULIN SENSITIVITY; LARVA; LIFESPAN; METABOLIC DISORDER; METABOLISM; NONHUMAN; PHENOTYPE; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; STARVATION; STRESS; ANIMAL; DROSOPHILA MELANOGASTER; FEMALE; GENETICS; MALE; PHYSIOLOGICAL STRESS; PHYSIOLOGY; TRANSCRIPTION INITIATION;

METAZOA; VERTEBRATA;

ANIMALS; CARRIER PROTEINS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEMALE; GLUCOSE; HOMEOSTASIS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MALE; MEMBRANE GLYCOPROTEINS; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL; TRANSCRIPTIONAL ACTIVATION;

EID: 65649089080     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1000460     Document Type: Article

References (59)

1. Kloting N, Bluher M (2005) Extended longevity and insulin signaling in adipose tissue. Exp Gerontol 40: 126-133.
2. Kahn SE, Hull RL, Utzschneider KM (2006) Mechanisms linking obesity to insulin resistance and type 2 diabetes. Nature 444: 840-846.
3. Russell SJ, Kahn CR (2007) Endocrine regulation of ageing. Nat Rev Mol Cell Biol 8: 681-691.
4. Wang MC, Bohmann D, Jasper H (2005) JNK extends life span and limits growth by antagonizing cellular and organism-wide responses to insulin signaling. Cell 121: 115-125.
5. van der Pluijm I, Garinis GA, Brandt RM, Gorgels TG, Wijnhoven SW, et al. (2007) Impaired genome maintenance suppresses the growth hormone-insulinlike growth factor 1 axis in mice with Cockayne syndrome. PLoS Biol 5: e2.
6. Niedernhofer LJ, Garinis GA, Raams A, Lalai AS, Robinson AR, et al. (2006) A new progeroid syndrome reveals that genotoxic stress suppresses the somatotroph axis. Nature 444: 1038-1043.
7. Baumeister R, Schaffitzel E, Hertweck M (2006) Endocrine signaling in Caenorhabditis elegans controls stress response and longevity. J Endocrinol 190: 191-202.
8. Tatar M, Yin C (2001) Slow aging during insect reproductive diapause: why butterflies, grasshoppers and flies are like worms. Exp Gerontol 36: 723-738.
9. Hotamisligil GS (2006) Inflammation and metabolic disorders. Nature 444: 860-867.
10. Oh SW, Mukhopadhyay A, Svrzikapa N, Jiang F, Davis RJ, et al. (2005) JNK regulates lifespan in Caenorhabditis elegans by modulating nuclear translocation of forkhead transcription factor/DAF-16. Proc Natl Acad Sci U S A 102: 4494-4499.
11. Essers MA, Weijzen S, de Vries-Smits AM, Saarloos I, de Ruiter ND, et al. (2004) FOXO transcription factor activation by oxidative stress mediated by the small GTPase Ral and JNK. Embo J 23: 4802-4812.
12. Aguirre V, Uchida T, Yenush L, Davis RJ, White MF (2000) The c-Jun NH(2)- terminal kinase promotes insulin resistance during association with insulin receptor substrate-1 and phosphorylation of Ser(307). J Biol Chem 275: 9047-9054.
13. Hirosumi J, Tuncman G, Chang L, Gorgun CZ, Uysal KT, et al. (2002) A central role for JNK in obesity and insulin resistance. Nature 420: 333-336.
14. Hwangbo DS, Gersham B, Tu MP, Palmer M, Tatar M (2004) Drosophila dFOXO controls lifespan and regulates insulin signalling in brain and fat body. Nature 429: 562-566.
15. Giannakou ME, Goss M, Junger MA, Hafen E, Leevers SJ, et al. (2004) Longlived Drosophila with overexpressed dFOXO in adult fat body. Science 305: 361.
16. Sabio G, Das M, Mora A, Zhang Z, Jun JY, et al. (2008) A stress signaling pathway in adipose tissue regulates hepatic insulin resistance. Science 322: 1539-1543.
17. Abel ED, Peroni O, Kim JK, Kim YB, Boss O, et al. (2001) Adipose-selective targeting of the GLUT4 gene impairs insulin action in muscle and liver. Nature 409: 729-733.
18. Yang Q, Graham TE, Mody N, Preitner F, Peroni OD, et al. (2005) Serum retinol binding protein 4 contributes to insulin resistance in obesity and type 2 diabetes. Nature 436: 356-362.
19. Graham TE, Yang Q, Bluher M, Hammarstedt A, Ciaraldi TP, et al. (2006) Retinol-binding protein 4 and insulin resistance in lean, obese, and diabetic subjects. N Engl J Med 354: 2552-2563.
20. Munkhtulga L, Nakayama K, Utsumi N, Yanagisawa Y, Gotoh T, et al. (2006) Identification of a regulatory SNP in the retinol binding protein 4 gene associated with type 2 diabetes in Mongolia. Hum Genet.
21. Flower DR (1996) The lipocalin protein family: structure and function. Biochem J 318 (Pt 1): 1-14.
22. Åkerström B, Borregaard N, Flower DR, Salier JP (2006) Austin, TX: Lipocalins Landes Bioscience.
23. Ganfornina MD, Gutierrez G, Bastiani M, Sanchez D (2000) A phylogenetic analysis of the lipocalin protein family. Mol Biol Evol 17: 114-126.
24. Sanchez D, Ganfornina MD, Gutierrez G, Marin A (2003) Exon-intron structure and evolution of the Lipocalin gene family. Mol Biol Evol 20: 775-783.
25. van Dam RM, Hu FB (2007) Lipocalins and insulin resistance: etiological role of retinol-binding protein 4 and lipocalin-2? Clin Chem 53: 5-7.
26. Yan QW, Yang Q, Mody N, Graham TE, Hsu CH, et al. (2007) The adipokine lipocalin 2 is regulated by obesity and promotes insulin resistance. Diabetes 56: 2533-2540.
27. Ganfornina MD, Do Carmo S, Lora JM, Torres-Schumann S, Vogel M, et al. (2008) Apolipoprotein D is involved in the mechanisms regulating protection from oxidative stress. Aging Cell.
28. Muffat J, Walker DW, Benzer S (2008) Human ApoD, an apolipoprotein upregulated in neurodegenerative diseases, extends lifespan and increases stress resistance in Drosophila. Proc Natl Acad Sci U S A 105: 7088-7093.
29. Loerch PM, Lu T, Dakin KA, Vann JM, Isaacs A, et al. (2008) Evolution of the aging brain transcriptome and synaptic regulation. PLoS ONE 3: e3329.
30. Do Carmo S, Fournier D, Mounier C, Rassart E (2009) Human apolipoprotein D overexpression in transgenic mice induces insulin resistance and alters lipid metabolism. Am J Physiol Endocrinol Metab.
31. Ganfornina MD, Sanchez D, Bastiani MJ (1995) Lazarillo, a new GPI-linked surface lipocalin, is restricted to a subset of neurons in the grasshopper embryo. Development 121: 123-134.
32. Walker DW, Muffat J, Rundel C, Benzer S (2006) Overexpression of a Drosophila homolog of apolipoprotein D leads to increased stress resistance and extended lifespan. Curr Biol 16: 674-679.
33. Sanchez D, Lopez-Arias B, Torroja L, Canal I, Wang X, et al. (2006) Loss of glial lazarillo, a homolog of apolipoprotein D, reduces lifespan and stress resistance in Drosophila. Curr Biol 16: 680-686.
34. Sanchez D, Ganfornina MD, Torres-Schumann S, Speese SD, Lora JM, et al. (2000) Characterization of two novel lipocalins expressed in the Drosophila embryonic nervous system. Int J Dev Biol 44: 349-359.
35. Wang MC, Bohmann D, Jasper H (2003) JNK signaling confers tolerance to oxidative stress and extends lifespan in Drosophila. Dev Cell 5: 811-816.
36. Zinke I, Kirchner C, Chao LC, Tetzlaff MT, Pankratz MJ (1999) Suppression of food intake and growth by amino acids in Drosophila: the role of pumpless, a fat body expressed gene with homology to vertebrate glycine cleavage system. Development 126: 5275-5284.
37. Oldham S, Stocker H, Laffargue M, Wittwer F, Wymann M, et al. (2002) The Drosophila insulin/IGF receptor controls growth and size by modulating PtdInsP(3) levels. Development 129: 4103-4109.
38. Bohni R, Riesgo-Escovar J, Oldham S, Brogiolo W, Stocker H, et al. (1999) Autonomous control of cell and organ size by CHICO, a Drosophila homolog of vertebrate IRS1-4. Cell 97: 865-875.
39. Clancy DJ, Gems D, Harshman LG, Oldham S, Stocker H, et al. (2001) Extension of life-span by loss of CHICO, a Drosophila insulin receptor substrate protein. Science 292: 104-106.
40. Broughton SJ, Piper MD, Ikeya T, Bass TM, Jacobson J, et al. (2005) Longer lifespan, altered metabolism, and stress resistance in Drosophila from ablation of cells making insulin-like ligands. Proc Natl Acad Sci U S A 102: 3105-3110.
41. Rulifson EJ, Kim SK, Nusse R (2002) Ablation of insulin-producing neurons in flies: growth and diabetic phenotypes. Science 296: 1118-1120.
42. Gershman B, Puig O, Hang L, Peitzsch RM, Tatar M, et al. (2007) Highresolution dynamics of the transcriptional response to nutrition in Drosophila: a key role for dFOXO. Physiol Genomics 29: 24-34.
43. McGuire SE, Le PT, Osborn AJ, Matsumoto K, Davis RL (2003) Spatiotemporal rescue of memory dysfunction in Drosophila. Science 302: 1765-1768.
44. Rong YS, Titen SW, Xie HB, Golic MM, Bastiani M, et al. (2002) Targeted mutagenesis by homologous recombination in D. melanogaster. Genes Dev 16: 1568-1581.
45. Kimbrell DA, Hice C, Bolduc C, Kleinhesselink K, Beckingham K (2002) The Dorothy enhancer has Tinman binding sites and drives hopscotch-induced tumor formation. Genesis 34: 23-28.
46. Karpac J, Jasper H (2009) Insulin and JNK: optimizing metabolic homeostasis and lifespan. Trends Endocrinol Metab in press.
47. Libert S, Chao Y, Zwiener J, Pletcher SD (2008) Realized immune response is enhanced in long-lived puc and chico mutants but is unaffected by dietary restriction. Mol Immunol 45: 810-817.
48. Agaisse H, Petersen UM, Boutros M, Mathey-Prevot B, Perrimon N (2003) Signaling role of hemocytes in Drosophila JAK/STAT-dependent response to septic injury. Dev Cell 5: 441-450.
49. Lemaitre B, Hoffmann J (2007) The host defense of Drosophila melanogaster. Annu Rev Immunol 25: 697-743.
50. Britton JS, Lockwood WK, Li L, Cohen SM, Edgar BA (2002) Drosophila's insulin/PI3-kinase pathway coordinates cellular metabolism with nutritional conditions. Dev Cell 2: 239-249.
51. Junger MA, Rintelen F, Stocker H, Wasserman JD, Vegh M, et al. (2003) The Drosophila Forkhead transcription factor FOXO mediates the reduction in cell number associated with reduced insulin signaling. J Biol 2: 20.
52. Puig O, Marr MT, Ruhf ML, Tjian R (2003) Control of cell number by Drosophila FOXO: downstream and feedback regulation of the insulin receptor pathway. Genes Dev 17: 2006-2020.
53. Vihervaara T, Puig O (2008) dFOXO regulates transcription of a Drosophila acid lipase. J Mol Biol 376: 1215-1223.
54. Libina N, Berman JR, Kenyon C (2003) Tissue-specific activities of C. elegans DAF-16 in the regulation of lifespan. Cell 115: 489-502.
55. Bluher M, Kahn BB, Kahn CR (2003) Extended longevity in mice lacking the insulin receptor in adipose tissue. Science 299: 572-574.
56. Colombani J, Raisin S, Pantalacci S, Radimerski T, Montagne J, et al. (2003) A nutrient sensor mechanism controls Drosophila growth. Cell 114: 739-749.
57. Hotamisligil GS (2005) Role of endoplasmic reticulum stress and c-Jun NH2-terminal kinase pathways in inflammation and origin of obesity and diabetes. Diabetes 54 Suppl 2: S73-78.
58. Dionne MS, Pham LN, Shirasu-Hiza M, Schneider DS (2006) Akt and FOXO dysregulation contribute to infection-induced wasting in Drosophila. Curr Biol 16: 1977-1985.
59. Wang Y, Lam KS, Kraegen EW, Sweeney G, Zhang J, et al. (2007) Lipocalin-2 is an inflammatory marker closely associated with obesity, insulin resistance, and hyperglycemia in humans. Clin Chem 53: 34-41.