Divergent and convergent roles for insulin-like peptides in the worm, fly and mammalian nervous systems

Invertebrate Neuroscience

Volumn 14, Issue 2, 2014, Pages 71-78

  Lau, Hiu E ^a,b   Chalasani, Sreekanth H ^a,b  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

Author keywords

Behavior; C. elegans; D. melanogaster; Insulin; Mammals; Nervous system

Indexed keywords

INSULIN; PEPTIDE;

ANIMAL; ANNELID; CHEMISTRY; DIPTERA; EVOLUTION; HUMAN; MAMMAL; METABOLISM; NERVOUS SYSTEM;

ANIMALS; ANNELIDA; BIOLOGICAL EVOLUTION; DIPTERA; HUMANS; INSULIN; MAMMALS; NERVOUS SYSTEM; PEPTIDES;

EID: 84891527494     PISSN: 13542516     EISSN: 14391104     Source Type: Journal    
DOI: 10.1007/s10158-013-0166-9     Document Type: Review

References (66)

1. Accili D, Arden KC (2004) FoxOs at the crossroads of cellular metabolism, differentiation, and transformation. Cell 117:421–426
2. Ahmadian G, Ju W, Liu L, Wyszynski M, Lee SH, Dunah AW, Taghibiglou C, Wang Y, Lu J, Wong TP, Sheng M, Wang YT (2004) Tyrosine phosphorylation of GluR2 is required for insulin-stimulated AMPA receptor endocytosis and LTD. EMBO J 23:1040–1050
3. Banks WA (2004) The source of cerebral insulin. Eur J Pharmacol 490:5–12
4. Bargmann CI (2012) Beyond the connectome: how neuromodulators shape neural circuits. BioEssays 34:458–465
5. Barres BA, Hart IK, Coles HS, Burne JF, Voyvodic JT, Richardson WD, Raff MC (1992) Cell death and control of cell survival in the oligodendrocyte lineage. Cell 70:31–46
6. Baskin DG, Figlewicz Lattemann D, Seeley RJ, Woods SC, Porte D Jr, Schwartz MW (1999) Insulin and leptin: dual adiposity signals to the brain for the regulation of food intake and body weight. Brain Res 848:114–123
7. Bedarkar S, Turnell WG, Blundell TL, Schwabe C (1977) Relaxin has conformational homology with insulin. Nature 270:449–451
8. Bell GI, Pictet RL, Rutter WJ, Cordell B, Tischer E, Goodman HM (1980) Sequence of the human insulin gene. Nature 284:26–32
9. Blair LA, Marshall J (1997) IGF-1 modulates N and L calcium channels in a PI 3-kinase-dependent manner. Neuron 19:421–429
10. Bliss M (1993) Rewriting medical history: Charles Best and the Banting and Best myth. J Hist Med Allied Sci 48:253–274
11. Brogiolo W, Stocker H, Ikeya T, Rintelen F, Fernandez R, Hafen E (2001) An evolutionarily conserved function of the Drosophila insulin receptor and insulin-like peptides in growth control. Curr Biol 11:213–221
12. Broughton SJ, Piper MD, Ikeya T, Bass TM, Jacobson J, Driege Y, Martinez P, Hafen E, Withers DJ, Leevers SJ, Partridge L (2005) Longer lifespan, altered metabolism, and stress resistance in Drosophila from ablation of cells making insulin-like ligands. Proc Natl Acad Sci USA 102:3105–3110
13. Bullesbach EE, Schwabe C (1995) A novel Leydig cell cDNA-derived protein is a relaxin-like factor. J Biol Chem 270:16011–16015
14. Cassada RC, Russell RL (1975) The dauerlarva, a post-embryonic developmental variant of the nematode Caenorhabditis elegans. Dev Biol 46:326–342
15. Chalasani SH, Kato S, Albrecht DR, Nakagawa T, Abbott LF, Bargmann CI (2010) Neuropeptide feedback modifies odor-evoked dynamics in Caenorhabditis elegans olfactory neurons. Nat Neurosci 13:615–621
16. Chassin D, Laurent A, Janneau JL, Berger R, Bellet D (1995) Cloning of a new member of the insulin gene superfamily (INSL4) expressed in human placenta. Genomics 29:465–470
17. Cheetham SW, Brand AH (2013) Cell biology. Insulin finds its niche. Science 340:817–818
18. Chen Z, Hendricks M, Cornils A, Maier W, Alcedo J, Zhang Y (2013) Two insulin-like peptides antagonistically regulate aversive olfactory learning in C. elegans. Neuron 77:572–585
19. Chiu SL, Cline HT (2010) Insulin receptor signaling in the development of neuronal structure and function. Neural Dev 5:7
20. Colombani J, Andersen DS, Leopold P (2012) Secreted peptide Dilp8 coordinates Drosophila tissue growth with developmental timing. Science 336:582–585
21. Cornils A, Gloeck M, Chen Z, Zhang Y, Alcedo J (2011) Specific insulin-like peptides encode sensory information to regulate distinct developmental processes. Development 138:1183–1193
22. Fernandez AM, Torres-Aleman I (2012) The many faces of insulin-like peptide signalling in the brain. Nat Rev Neurosci 13:225–239
23. Freychet P, Roth J, Neville DM Jr (1971) Insulin receptors in the liver: specific binding of (125 I)insulin to the plasma membrane and its relation to insulin bioactivity. Proc Natl Acad Sci USA 68:1833–1837
24. Gao Q, Horvath TL (2007) Neurobiology of feeding and energy expenditure. Annu Rev Neurosci 30:367–398
25. Harper ME, Ullrich A, Saunders GF (1981) Localization of the human insulin gene to the distal end of the short arm of chromosome 11. Proc Natl Acad Sci USA 78:4458–4460
26. Hawkes C, Kar S (2004) The insulin-like growth factor-II/mannose-6-phosphate receptor: structure, distribution and function in the central nervous system. Brain Res Brain Res Rev 44:117–140
27. Hodge RD, D’Ercole AJ, O’Kusky JR (2004) Insulin-like growth factor-I accelerates the cell cycle by decreasing G1 phase length and increases cell cycle reentry in the embryonic cerebral cortex. J Neurosci 24:10201–10210
28. Hung WL, Hwang C, Gao S, Liao EH, Chitturi J, Wang Y, Li H, Stigloher C, Bessereau JL, Zhen M (2013) Attenuation of insulin signalling contributes to FSN-1-mediated regulation of synapse development. EMBO J 32:1745–1760
29. Ikeya T, Galic M, Belawat P, Nairz K, Hafen E (2002) Nutrient-dependent expression of insulin-like peptides from neuroendocrine cells in the CNS contributes to growth regulation in Drosophila. Curr Biol 12:1293–1300
30. Kahn CR, Freychet P, Roth J, Neville DM Jr (1974) Quantitative aspects of the insulin-receptor interaction in liver plasma membranes. J Biol Chem 249:2249–2257
31. 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
32. Langlais P, Dong LQ, Ramos FJ, Hu D, Li Y, Quon MJ, Liu F (2004) Negative regulation of insulin-stimulated mitogen-activated protein kinase signaling by Grb10. Mol Endocrinol 18:350–358
33. Leevers SJ, Weinkove D, MacDougall LK, Hafen E, Waterfield MD (1996) The Drosophila phosphoinositide 3-kinase Dp110 promotes cell growth. EMBO J 15:6584–6594
34. Leinwand SG, Chalasani SH (2013) Neuropeptide signaling remodels chemosensory circuit composition in Caenorhabditis elegans. Nat Neurosci 16:1461–1467
35. Lin K, Dorman JB, Rodan A, Kenyon C (1997) daf-16: an HNF-3/forkhead family member that can function to double the life-span of Caenorhabditis elegans. Science 278:1319–1322
36. Marks DR, Tucker K, Cavallin MA, Mast TG, Fadool DA (2009) Awake intranasal insulin delivery modifies protein complexes and alters memory, anxiety, and olfactory behaviors. J Neurosci 29:6734–6751
37. Massague J, Pilch PF, Czech MP (1980) Electrophoretic resolution of three major insulin receptor structures with unique subunit stoichiometries. Proc Natl Acad Sci USA 77:7137–7141
38. Morris JZ, Tissenbaum HA, Ruvkun G (1996) A phosphatidylinositol-3-OH kinase family member regulating longevity and diapause in Caenorhabditis elegans. Nature 382:536–539
39. Murray-Rust J, McLeod AN, Blundell TL, Wood SP (1992) Structure and evolution of insulins: implications for receptor binding. BioEssays 14:325–331
40. Oda S, Tomioka M, Iino Y (2011) Neuronal plasticity regulated by the insulin-like signaling pathway underlies salt chemotaxis learning in Caenorhabditis elegans. J Neurophysiol 106:301–308
41. Owerbach D, Bell GI, Rutter WJ, Shows TB (1980) The insulin gene is located on chromosome 11 in humans. Nature 286:82–84
42. Ozdinler PH, Macklis JD (2006) IGF-I specifically enhances axon outgrowth of corticospinal motor neurons. Nat Neurosci 9:1371–1381
43. Paradis S, Ruvkun G (1998) Caenorhabditis elegans Akt/PKB transduces insulin receptor-like signals from AGE-1 PI3 kinase to the DAF-16 transcription factor. Genes Dev 12:2488–2498
44. Paradis S, Ailion M, Toker A, Thomas JH, Ruvkun G (1999) A PDK1 homolog is necessary and sufficient to transduce AGE-1 PI3 kinase signals that regulate diapause in Caenorhabditis elegans. Genes Dev 13:1438–1452
45. Pierce SB, Costa M, Wisotzkey R, Devadhar S, Homburger SA, Buchman AR, Ferguson KC, Heller J, Platt DM, Pasquinelli AA, Liu LX, Doberstein SK, Ruvkun G (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
46. Poltilove RM, Jacobs AR, Haft CR, Xu P, Taylor SI (2000) Characterization of Drosophila insulin receptor substrate. J Biol Chem 275:23346–23354
47. Rinderknecht E, Humbel RE (1976) Polypeptides with nonsuppressible insulin-like and cell-growth promoting activities in human serum: isolation, chemical characterization, and some biological properties of forms I and II. Proc Natl Acad Sci USA 73:2365–2369
48. Rinderknecht E, Humbel RE (1978) The amino acid sequence of human insulin-like growth factor I and its structural homology with proinsulin. J Biol Chem 253:2769–2776
49. Ritter AD, Shen Y, Fuxman Bass J, Jeyaraj S, Deplancke B, Mukhopadhyay A, Xu J, Driscoll M, Tissenbaum HA, Walhout AJ (2013) Complex expression dynamics and robustness in C. elegans insulin networks. Genome Res 23:954–965
50. Root CM, Ko KI, Jafari A, Wang JW (2011) Presynaptic facilitation by neuropeptide signaling mediates odor-driven food search. Cell 145:133–144
51. Rulifson EJ, Kim SK, Nusse R (2002) Ablation of insulin-producing neurons in flies: growth and diabetic phenotypes. Science 296:1118–1120
52. Schwartz MW, Seeley RJ, Campfield LA, Burn P, Baskin DG (1996) Identification of targets of leptin action in rat hypothalamus. J Clin Invest 98:1101–1106
53. Scolnick JA, Cui K, Duggan CD, Xuan S, Yuan XB, Efstratiadis A, Ngai J (2008) Role of IGF signaling in olfactory sensory map formation and axon guidance. Neuron 57:847–857
54. Silva JP, von Meyenn F, Howell J, Thorens B, Wolfrum C, Stoffel M (2009) Regulation of adaptive behaviour during fasting by hypothalamic Foxa2. Nature 462:646–650
55. Slack C, Giannakou ME, Foley A, Goss M, Partridge L (2011) dFOXO-independent effects of reduced insulin-like signaling in Drosophila. Aging Cell 10:735–748
56. Staveley BE, Ruel L, Jin J, Stambolic V, Mastronardi FG, Heitzler P, Woodgett JR, Manoukian AS (1998) Genetic analysis of protein kinase B (AKT) in Drosophila. Curr Biol 8:599–602
57. Tomioka M, Adachi T, Suzuki H, Kunitomo H, Schafer WR, Iino Y (2006) The insulin/PI 3-kinase pathway regulates salt chemotaxis learning in Caenorhabditis elegans. Neuron 51:613–625
58. Torres-Aleman I, Pons S, Arevalo MA (1994) The insulin-like growth factor I system in the rat cerebellum: developmental regulation and role in neuronal survival and differentiation. J Neurosci Res 39:117–126
59. Vashisth H, Abrams CF (2010) All-atom structural models for complexes of insulin-like growth factors IGF1 and IGF2 with their cognate receptor. J Mol Biol 400:645–658
60. Wang YT, Linden DJ (2000) Expression of cerebellar long-term depression requires postsynaptic clathrin-mediated endocytosis. Neuron 25:635–647
61. Werz C, Kohler K, Hafen E, Stocker H (2009) The Drosophila SH2B family adaptor Lnk acts in parallel to chico in the insulin signaling pathway. PLoS Genet 5:e1000596
62. Wolkow CA, Munoz MJ, Riddle DL, Ruvkun G (2002) Insulin receptor substrate and p55 orthologous adaptor proteins function in the Caenorhabditis elegans daf-2/insulin-like signaling pathway. J Biol Chem 277:49591–49597
63. Woods SC, Chavez M, Park CR, Riedy C, Kaiyala K, Richardson RD, Figlewicz DP, Schwartz MW, Porte D Jr, Seeley RJ (1996) The evaluation of insulin as a metabolic signal influencing behavior via the brain. Neurosci Biobehav Rev 20:139–144
64. Wu Q, Zhang Y, Xu J, Shen P (2005) Regulation of hunger-driven behaviors by neural ribosomal S6 kinase in Drosophila. Proc Natl Acad Sci USA 102:13289–13294
65. Zhang Y, Lu H, Bargmann CI (2005) Pathogenic bacteria induce aversive olfactory learning in Caenorhabditis elegans. Nature 438:179–184
66. Zhao XL, Campos AR (2012) Insulin signalling in mushroom body neurons regulates feeding behaviour in Drosophila larvae. J Exp Biol 215:2696–2702