Diverse insulin-like peptides in Caenorhabditis elegans

Main Article Content

Yohei Matsunaga Takashi Iwasaki Tsuyoshi Kawano

Abstract

Peptide hormones are conserved in living organisms to modulate homeostasis. To elucidate molecular mechanisms in the synthesis, secretion, and functions of peptide hormones, model organisms have been used. Caenorhabditis elegans, one of model organisms, is a good tool since: 1) genome size of the worm is small with over 40% homology to human genome, 2) numerous genetics methods are available, and 3) the worms are transparent throughout the life cycle, so that the secretion of peptide hormones can be followed at cellular level in living preparations by Green Fluorescent Protein tagged peptides. This review reports the structures, physiological functions, and secretion of insulin-like peptides, one family of peptide hormones, with our latest findings in the model organism, Caenorhabditis elegans.

Article Details

How to Cite
MATSUNAGA, Yohei; IWASAKI, Takashi; KAWANO, Tsuyoshi. Diverse insulin-like peptides in Caenorhabditis elegans. International Biology Review, [S.l.], v. 1, n. 1, may 2017. ISSN 2572-7168. Available at: <https://esmed.org/MRA/ibr/article/view/1276>. Date accessed: 20 apr. 2024. doi: https://doi.org/10.18103/ibr.v1i1.1276.
Keywords
Caenorhabditis elegans; insulin-like peptides; physiological function; secretion; structure
Section
Articles

References

1. Klass MR. A method for the isolation of longevity mutants in the nematode Caenorhabditis elegans and initial results. Mech Ageing Dev. 22 (3-4) 1993, 279-286.

2. Friedman DB, Johnson TE. A mutation in the age-1 gene in Caenorhabditis elegans lengthens life and reduces hermaphrodite fertility. Genetics. 118 (1) 1988, 75-86.

3. Friedman DB, Johnson TE. Three mutants that extend both mean and maximum life span of the nematode, Caenorhabditis elegans, define the age-1 gene. J. Gerontol. 43 (4) 1988, 102-109.

4. Johnson TE. Increased life-span of age-1 mutants in Caenorhabditis elegans and lower Gompertz rate of aging. Science 249 (4971) 1990, 908-912.

5. Brogiolo W, Stocker H, Ikeya T, Rintelen F, Fernandez R, and Hafen E. An evolutionarily conserved function of the Drosophila insulin receptor and insulin-like peptides in growth control. Curr Biol. 11 (4) 2001, 213-221.

6. Rulifson EJ, Kim SK, Nusse R. Ablation of insulin-producing neurons in flies: growth and diabetic phenotypes. Science 296 (5570) 2002, 1118-1120.

7. Tatar M, Kopelman A, Epstein D, Tu MP, Yin CM, Garofalo RS. A mutant Drosophila insulin receptor homolog that extends life-span and impairs neuroendocrine function. Science 292 (5514) 2001, 107–110.

8. 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. 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 (6) 2001, 672-686.

9. Li W, Kennedy SG, Ruvkun, G. daf-28 encodes a C. elegans insulin superfamily member that is regulated by environmental cues and acts in the DAF-2 signaling pathway. Genes Dev. 17 (7) 2003, 844–858.

10. Husson SJ, Mertens I, Janssen T, Lindemans M, Schoofs L. Neuropeptidergic signaling in the nematode Caenorhabditis elegans. Prog Neurobiol. 82 (1) 2007, 33-55.

11. C. elegans Sequencing Consortium. Genome sequence of the nematode C. elegans: a platform for investigating biology. Science 282 (5396) 1998, 2012-2008.

12. Fire A, Xu S, Montgomery MK, Kostas SA, Driver SE, Mello CC. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391 (6669) 1998, 806-811.

13. Zwaal RR, Broeks A, van Meurs J, Groenen JT, Plasterk RH. Target-selected gene inactivation in Caenorhabditis elegans by using a frozen transposon insertion mutant bank. Proc Natl Acad Sci U S A. 90 (16) 1993, 7431-7435.

14. Kenyon C, Chang J, Gensch E, Rudner A, Tabtiang R. A C. elegans mutant that lives twice as long as wild type. Nature 366 (6454) 1993, 461-464.

15. Barbieri M, Bonafè M, Franceschi C, Paolisso G. Insulin/IGF-I-signaling pathway: an evolutionarily conserved mechanism of longevity from yeast to humans. Am J Physiol Endocrinol Metab. 285 (5) 2003, 1064-1071.

16. Kimura KD, Tissenbaum HA, Liu Y, Ruvkun G. daf-2, an insulin receptor-like gene that regulates longevity and diapause in Caenorhabditis elegans. Science 277 (5328) 1997, 942-946.

17. Kawano T, Takuwa K, Nakajima T, Kimura Y. Insulin-like peptides of C. elegans. Worm Breeder’s Gazette 15 (2) 1998, 47.

18. Duret L, Guex N, Peitsch MC, Bairoch A. New insulin-like proteins with atypical disulfide bond pattern characterized in Caenorhabditis elegans by comparative sequence analysis and homology modeling. Genome Res. 8 (4) 1998, 348-353.

19. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 215 (3) 1990, 403-410.

20. Pearson WR, Lipman DJ. Improved tools for biological sequence comparison. Proc Natl Acad Sci U S A. 85 (8) 1988, 2444-2448.

21. Eddy SR1, Mitchison G, Durbin R. Maximum discrimination hidden Markov models of sequence consensus. J Comput Biol. 2 (1) 1995, 9-23.

22. Orci L, Ravazzola M, Storch MJ, Anderson RG, Vassalli JD, Perrelet A. Proteolytic maturation of insulin is a post-Golgi event which occurs in acidifying clathrin-coated secretory vesicles. Cell 49 (6) 1987, 865–868

23. Malide D, Seidah NG, Chretien M, Bendayan M. Electron microscopic immunocytochemical evidence for the involvement of the convertases PC1 and PC2 in the processing of proinsulin in pancreatic beta-cells. J Histo Cyto. 43 (1) 1995, 11–19

24. Thacker C, Rose AM. A look at the Caenorhabditis elegans Kex2/Subtilisin-like proprotein convertase family. Bioessays 22 (6) 2000, 545-553.

25. Thacker C, Srayko M, Rose AM. Mutational analysis of bli-4/kpc-4 reveals critical residues required for proprotein convertase function in C. elegans. Gene 252 (1-2) 2000, 15-25.

26. Kass J, Jacob TC, Kim P, Kaplan JM. The EGL-3 proprotein convertase regulates mechanosensory responses of Caenorhabditis elegans. J Neurosci. 21 (23) 2001, 9265-9272.

27. Hung WL, Hwang C, Gao S, Liao EH, Chitturi J, Wang Y, Li H, Stigloher C, Bessereau JL, Zhen M. Attenuation of insulin signalling contributes to FSN-1-mediated regulation of synapse development. EMBO J 32 (12) 2013, 1745-1760.

28. Hung WL, Wang Y, Chitturi J, Zhen M. A Caenorhabditis elegans developmental decision requires insulin signaling-mediated neuron-intestine communication. Development 141 (8) 2014, 1767-1779.

29. Salzberg Y, Ramirez-Suarez NJ, Bülow HE. The proprotein convertase KPC-1/furin controls branching and self-avoidance of sensory dendrites in Caenorhabditis elegans. PLoS Genet. 10 (9) 2014, e1004657.

30. Polex-Wolf J, Yeo GS, O'Rahilly S. Impaired prohormone processing: a grand unified theory for features of Prader-Willi syndrome? J Clin Invest. 127 (1) 2017, 98-99.

31. Kawano T, Ito Y, Ishiguro M, Takuwa K, Nakajima T, Kimura Y. Molecular cloning and characterization of a new insulin/IGF-like peptide of the nematode Caenorhabditis elegans. Biochem. Biophys. Res. Commun. 273 (2) 2000, 431-436.

32. Matsunaga Y, Gengyo-Ando K, Mitani S, Iwasaki T, Kawano T. Physiological function, expression pattern, and transcriptional regulation of a Caenorhabditis elegans insulin-like peptide, INS-18. Biochem. Biophys. Res. Commun. 423 (3) 2012, 478-483

33. Morris JZ, Tissenbaum HA, Ruvkun G. A phosphatidylinositol-3-OH kinase family member regulating longevity and diapause in Caenorhabditis elegans. Nature 382 (6591) 1996, 536-539.

34. Paradis S, Ruvkun G. Caenorhabditis elegans Akt/PKB transduces insulin receptor-like signals from AGE-1 PI3 kinase to the DAF-16 transcription factor. Genes Dev. 12 (16) 1998, 2488-2498.

35. Paradis S, Ailion M, Toker A, Thomas JH, Ruvkun G. A PDK1 homolog is necessary and sufficient to transduce AGE-1 PI3 kinase signals that regulate diapause in Caenorhabditis elegans. Genes Dev. 13 (11) 1999, 1438-1452.

36. Ogg S, Paradis S, Gottlieb S, Patterson GI, Lee L, Tissenbaum HA, Ruvkun G. The Fork head transcription factor DAF-16 transduces insulin-like metabolic and longevity signals in C. elegans. Nature 389 (6654) 1997, 994-999.

37. Henderson ST, Johnson TE. daf-16 integrates developmental and environmental inputs to mediate aging in the nematode Caenorhabditis elegans. Curr Biol. 11 (24) 2001, 1975-1980.

38. Lee RY, Hench J, Ruvkun G. Regulation of C. elegans DAF-16 and its human ortholog FKHRL1 by the daf-2 insulin-like signaling pathway. Curr Biol. 11 (24) 2001, 1950-1957.

39. Lin K, Hsin H, Libina N, Kenyon C. Regulation of the Caenorhabditis elegans longevity protein DAF-16 by insulin/IGF-1 and germline signaling. Nat Genet. 28 (2) 2001, 139-145.

40. Matsunaga Y, Ito H, Kawano T. Proceedings: Physiological Function of INS-12, One of the Type-γ Insulin-like peptides, in C. elegans. Peptide Science 2009. 2010, 459-462.

41. Matsunaga Y, Nakajima K, Gengyo-Ando K, Mitani S, Iwasaki T, Kawano T. A Caenorhabditis elegans insulin-like peptide, INS-17: its physiological function and expression pattern. Biosci. Biotechnol. Biochem. 76 (11) 2012, 2168-2172.

42. Matsukawa T, Matsunaga Y, Iwasaki T, Nagata K, Tanokura M, Kawano T. Proceedings: Comparison of physiological function between antagonistic insulin-like peptides, INS-23 and INS-18, in Caenorhabditis elegans. Peptide Science 2016. 2017, in press.

43. Malone EA, Inoue T, Thomas JH. Genetic analysis of the roles of daf-28 and age-1 in regulating Caenorhabditis elegans dauer formation. Genetics 143 (3) 1996, 1193-1205.

44. Murphy CT, McCarroll SA, Bargmann CI, Fraser A, Kamath RS, Ahringer J, Li H, Kenyon C. Genes that act downstream of DAF-16 to influence the lifespan of Caenorhabditis elegans. Nature 424 (6946) 2003, 277-283.

45. Cornils A, Gloeck M, Chen Z, Zhang Y, Alcedo J. Specific insulin-like peptides encode sensory information to regulate distinct developmental processes. Development 138 (6) 2011, 1183-1193.

46. Kurz CL, Tan MW. Regulation of aging and innate immunity in C. elegans. Aging Cell 3 (4) 2004, 185-193.

47. Kaletsky R, Murphy CT. The role of insulin/IGF-like signaling in C. elegans longevity and aging. Dis. Model Mech. 3 (7-8) 2010, 415-419.

48. Kenyon C. A pathway that links reproductive status to lifespan in Caenorhabditis elegans. Ann. N Y Acad Sci. 2010 Aug;1204 2010, 156-162.

49. Michaelson D, Korta DZ, Capua Y, Hubbard EJ. Insulin signaling promotes germline proliferation in C. elegans. Development 137 (4) 2010, 671-680

50. Tissenbaum HA. Genetics, life span, health span, and the aging process in Caenorhabditis elegans. J Gerontol. (A) Biol. Sci. Med. Sci. 67 (5) 2012, 503-510.

51. Sasakura H, Mori I. Behavioral plasticity, learning, and memory in C. elegans. Curr. Opin. Neurobiol. 23 (1) 2013, 92-99.

52. Kodama E, Kuhara A, Mohri-Shiomi A, Kimura KD, Okumura M, Tomioka M, Iino Y, Mori I. Insulin-like signaling and the neural circuit for integrative behavior in C. elegans. Genes Dev. 20 (21) 2006, 2955-2960.

53. Tomioka M, Adachi T, Suzuki H, Kunitomo H, Schafer WR, Iino Y. The insulin/PI 3-kinase pathway regulates salt chemotaxis learning in Caenorhabditis elegans. Neuron 51 (5) 2006, 613-625.

54. Haque R, Nazir A. Identification and functional characterization of a putative IDE, C28F5.4 (ceIDE-1), in Caenorhabditis elegans: Implications for Alzheimer's disease. Biochim. Biophys. Acta 1860 (11 Pt A) 2016, 2454-2462

55. Austin J, Kimble J. glp-1 is required in the germ line for regulation of the decision between mitosis and meiosis in C. elegans. Cell 51 (4) 1987, 589-599.

56. VanDussen KL, Carulli AJ, Keeley TM, Patel SR, Puthoff BJ, Magness ST, Tran IT, Maillard I, Siebel C, Kolterud Å, Grosse AS, Gumucio DL, Ernst SA, Tsai YH, Dempsey PJ, Samuelson LC. Notch signaling modulates proliferation and differentiation of intestinal crypt base columnar stem cells. Development 139 (3) 2012, 488-497

57. Fernandes de Abreu DA, Caballero A, Fardel P, Stroustrup N, Chen Z, Lee K, Keyes WD, Nash ZM, López-Moyado IF, Vaggi F, Cornils A, Regenass M, Neagu A, Ostojic I, Liu C, Cho Y, Sifoglu D, Shen Y, Fontana W, Lu H, Csikasz-Nagy A, Murphy CT, Antebi A, Blanc E, Apfeld J, Zhang Y, Alcedo J, Ch'ng Q. An insulin-to-insulin regulatory network orchestrates phenotypic specificity in development and physiology. PLoS Genet. 2014 10 (3) 2014, e1004225.

58. Hua QX, Nakagawa SH, Wilken J, Ramos RR, Jia W, Bass J, Weiss MA. A divergent INS protein in Caenorhabditis elegans structurally resembles human insulin and activates the human insulin receptor. Genes Dev. 2003 17 (7) 2003, 826-831.

59. Liu T, Zimmerman KK, Patterson GI. Regulation of signaling genes by TGFbeta during entry into dauer diapause in C. elegans. BMC Dev. Biol. 4 (11) 2004.

60. Iwasaki T, Komatsu M, Fujimori T, Kawano T. Proceedings: Functional analysis of INS-6, one of the insulin-like peptides in C. elegans using primary culture. Peptide Science 2011. 2012, 369-372.

61. Suckale J, Solimena M. Pancreas islets in metabolic signaling focus on the beta-cell. Front. Biosci. May (13) 2008, 7156-7171.

62. Derbinski J, Schulte A, Kyewski B, Klein L. Promiscuous gene expression in medullary thymic epithelial cells mirrors the peripheral self. Nat Immunol. 2 (11) 2001, 1032-1039.

63. Deltour L, Leduque P, Blume N, Madsen O, Dubois P, Jami J, Bucchini D. Differential expression of the two nonallelic proinsulin genes in the developing mouse embryo. Proc. Natl. Acad. Sci. U S A. 90 (2) 1003, 527-531.

64. Devaskar SU, Giddings SJ, Rajakumar PA, Carnaghi LR, Menon RK, Zahm DS. Insulin gene expression and insulin synthesis in mammalian neuronal cells. J Biol. Chem. 269 (11) 1994, 8445-8454.

65. Kao G, Nordenson C, Still M, Rönnlund A, Tuck S, Naredi P. ASNA-1 positively regulates insulin secretion in C. elegans and mammalian cells. Cell 128 (3) 2007, 577-587.

66. Matsunaga Y, Honda Y, Honda S, Iwasaki T, Qadota H, Benian GM, Kawano T. Diapause is associated with a change in the polarity of secretion of insulin-like peptides. Nat Commun. Feb (7) 2016, 10573.

67. Clark ME, Kelner GS, Turbeville LA, Boyer A, Arden KC, Maki RA. ADAMTS9, a novel member of the ADAM-TS/ metallospondin gene family. Genomics 67(3) 2000, 343-350.

68. Somerville RP, Longpre JM, Jungers KA, Engle JM, Ross M, Evanko S, Wight TN, Leduc R, Apte SS. Characterization of ADAMTS-9 and ADAMTS-20 as a distinct ADAMTS subfamily related to Caenorhabditis elegans GON-1. J Biol. Chem. 2278 (11) 2003, 9503-9513.

69. Yoshina S, Mitani S. Loss of C. elegans GON-1, an ADAMTS9 Homolog, Decreases Secretion Resulting in Altered Lifespan and Dauer Formation. PLoS One 10 (7) 2015, e0133966

70. Grarup N, Andersen G, Krarup NT, Albrechtsen A, Schmitz O, Jørgensen T, Borch-Johnsen K, Hansen T, Pedersen O. Association testing of novel type 2 diabetes risk alleles in the JAZF1, CDC123/CAMK1D, TSPAN8, THADA, ADAMTS9, and NOTCH2 loci with insulin release, insulin sensitivity, and obesity in a population-based sample of 4,516 glucose-tolerant middle-aged Danes. Diabetes 57 (9) 2008, 2534-2540.

71. Zeggini E, Scott LJ, Saxena R, Voight BF, Marchini JL, Hu T, de Bakker PI, Abecasis GR, Almgren P, Andersen G, Ardlie K, Boström KB, Bergman RN, Bonnycastle LL, Borch-Johnsen K, Burtt NP, Chen H, Chines PS, Daly MJ, Deodhar P, Ding CJ, Doney AS, Duren WL, Elliott KS, Erdos MR, Frayling TM, Freathy RM, Gianniny L, Grallert H, Grarup N, Groves CJ, Guiducci C, Hansen T, Herder C, Hitman GA, Hughes TE, Isomaa B, Jackson AU, Jørgensen T, Kong A, Kubalanza K, Kuruvilla FG, Kuusisto J, Langenberg C, Lango H, Lauritzen T, Li Y, Lindgren CM, Lyssenko V, Marvelle AF, Meisinger C, Midthjell K, Mohlke KL, Morken MA, Morris AD, Narisu N, Nilsson P, Owen KR, Palmer CN, Payne F, Perry JR, Pettersen E, Platou C, Prokopenko I, Qi L, Qin L, Rayner NW, Rees M, Roix JJ, Sandbaek A, Shields B, Sjögren M, Steinthorsdottir V, Stringham HM, Swift AJ, Thorleifsson G, Thorsteinsdottir U, Timpson NJ, Tuomi T, Tuomilehto J, Walker M, Watanabe RM, Weedon MN, Willer CJ; Wellcome Trust Case Control Consortium, Illig T, Hveem K, Hu FB, Laakso M, Stefansson K, Pedersen O, Wareham NJ, Barroso I, Hattersley AT, Collins FS, Groop L, McCarthy MI, Boehnke M, Altshuler D. Meta-analysis of genome-wide association data and large-scale replication identifies additional susceptibility loci for type 2 diabetes. Nat Genet. 40 (5) 2008, 638-645.

72. Suckale J, Solimena M. The insulin secretory granule as a signaling hub. Trends Endocrinol. Metab. 21 (10) 2010, 599-609.

73. Tomioka M, Naito Y, Kuroyanagi H, Iino Y. Splicing factors control C. elegans behavioural learning in a single neuron by producing DAF-2c recdeptor. Nat Commun. 7 2016, 11645.

74. Hsu SY, Nakabayashi K, Nishi S, Kumagai J, Kudo M, Sherwood OD, Hsueh AJ. Activation of orphan receptors by the hormone relaxin. Science 295 (5555) 2002, 671-674.

75. Mita M, Yoshikuni M, Ohno K, Shibata Y, Paul-Prasanth B, Pitchayawasin S, Isobe M, Nagahama Y.A relaxin-like peptide purified from radial nerves induces oocyte maturation and ovulation in the starfish, Asterina pectinifera. Proc. Natl. Acad. Sci. U S A. 106 (23) 2009, 9507-9512.

76. Mita M, Haraguchi S, Watanabe M, Takeshige Y, Yamamoto K, Tsutsui K. Involvement of Gas-proteins in the action of relaxin-like gonad-stimulating substance on starfish ovarian follicle cells. Gen. Comp. Endocrinol. 205 2014, 80-87.

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