RME-1 is required for lifespan extension and increased resistance to stresses associated with decreased insulin/IGF-1-like signaling in Caenorhabditis elegans

Chul-Kyu Kim, Sang-Kyu Park

Abstract


The insulin/insulin-like growth factor (IGF)-1 signaling (IIS) pathway is a conserved lifespan-modulating genetic pathway. Many genes involved in lifespan extension associated with decreased signaling of the IIS pathway have been identified. In the present study, we found a novel gene required for the effect of the IIS pathway on the stress response and aging in C. elegans. Receptor mediated endocytosis (RME)-1 is expressed ubiquitously and known to be involved in cellular endocytic transport. Knockdown of rme-1 abolished the lifespan-extending effect caused by decreased IIS. In addition, resistance to oxidative stress, heat shock and ultraviolet irradiation were significantly decreased when the expression of rme-1 was blocked. The delayed age-related decline in motility observed in age-1 mutants with defects in the IIS pathway was also modulated by RME-1. The expression of sod-3, which is positively correlated with the remaining lifespan of an individual, was decreased by rme-1 knockdown. Our study demonstrates that RME-1 is required for the anti-aging effect associated with decreased IIS. We suggest that endocytic transport could be one underlying mechanisms for longevity via the IIS pathway.

https://doi.org/10.2298/ABS160510115K

Received: May 10, 2016; Revised: June 10, 2016; Accepted: June 10, 2016; Published online: October 31, 2016

How to cite: Kim CK, Park SK. RME-1 is required for lifespan extension and increased resistance to stresses associated with decreased insulin/IGF-1-like signaling in Caenorhabditis elegans. Arch Biol Sci. 2017;69(3):417-25.


Keywords


C. elegans; insulin/IGF-1-like signaling pathway; lifespan; RME-1; stress response

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References


Fossel M. Telomerase and the aging cell: implications for human health. JAMA. 1998;279(21):1732-35.

Sohal RS, Weindruch R. Oxidative stress, caloric restriction, and aging. Science. 1996;273(5271):59-63.

Herman D. Aging: a theory based on free radical and radiation chemistry. J Gerontol. 1956;11(3):298-300.

Shigenaga MK, Hagen TM, Ames BN. Oxidative damage and mitochondrial decay in aging. Proc Natl Acad Sci U S A. 1994;91(23):10771-8.

Kenyon C, Chang J, Gensch E, Rudner A, Tabtiang R. A C. elegans mutant that lives twice as long as wild type. Nature. 1993;366(6454):461-4.

Lapierre LR, Hansen M. Lessons from C. elegans: signaling pathways for longevity. Trends Endocrinol Metab. 2012;23(12):637-44.

Barbieri M, Bonafe 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. 2003;285(5):E1064-E1071.

Halaschek-Wiener J, Khattra JS, McKay S, Pouzyrev A, Stott JM, Yang GS, Holt RA, Jones SJ, Marra MA, Brooks-Wilson AR, Riddle DL. Analysis of long-lived C. elegans daf-2 mutants using serial analysis of gene expression. Genome Res. 2005;15(5):603-15.

McElwee J, Bubb K, Thomas JH. Transcriptional outputs of the Caenorhabditis elegans forkhead protein DAF-16. Aging Cell. 2003;2(2):111-21.

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. 2003;424(6946):277-83.

Lin SX, Grant B, Hirsh D, Maxfield FR. Rme-1 regulates the distribution and function of the endocytic recycling compartment in mammalian cells. Nat Cell Biol. 2001;3(6):567-72.

Lee DW, Zhao X, Scarselletta S, Schweinsberg PJ, Eisenberg E, Grant BD, Greene LE. ATP binding regulates oligomerization and endosome association of RME-1 family proteins. J Biol Chem. 2005;280(17):17213-20.

Sato M, Sato K, Fonarev P, Huang CJ, Liou W, Grant BD. Caenorhabditis elegans RME-6 is a novel regulator of RAB-5 at the clathrin-coated pit. Nat Cell Biol. 2005;7(6):559-69.

Zhang Y, Grant B, Hirsh D. RME-8, a conserved J-domain protein, is required for endocytosis in Caenorhabditis elegans. Mol Biol Cell. 2001;12(7):2011-21.

Fujibayashi A, Taguchi T, Misaki R, Ohtani M, Dohmae N, Takio K, Yamada M, Gu J, Yamakami M, Fukuda M, Waguri S, Uchiyama Y, Yoshimori T, Sekiguchi K. Human RME-8 is involved in membrane trafficking through early endosomes. Cell Struct Funct. 2008;33(1):35-50.

Silady RA, Kato T, Lukowitz W, Sieber P, Tasaka M, Somerville CR. The gravitropism defective 2 mutants of Arabidopsis are deficient in a protein implicated in endocytosis in Caenorhabditis elegans. Plant Physiol. 2004;136(2):3095-103.

Kamath RS, Fraser AG, Dong Y, Poulin G, Durbin R, Gotta M, Kanapin A, Le Bot N, Moreno S, Sohrmann M, Welchman DP, Zipperlen P, Ahringer J. Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature. 2003;421(6920):231-7.

Peto R, Peto J. Asymptotically efficient rank invariant test procedures. J Royal Stac Soc Ser A. 1972;135(2):185-207.

Larsen PL. Aging and resistance to oxidative damage in Caenorhabditis elegans. Proc Natl Acad Sci U S A. 1993;90(19):8905-9.

Van Raamsdonk JM, Hekimi S. Reactive Oxygen Species and Aging in Caenorhabditis elegans: Causal or Casual Relationship? Antioxid Redox Signal. 2010;13(12):1911-53.

Johnson TE, Henderson S, Murakami S, de Castro E, de Castro SH, Cypser J, Rikke B, Tedesco P, Link C. Longevity genes in the nematode Caenorhabditis elegans also mediate increased resistance to stress and prevent disease. J Inherit Metab Dis. 2002;25(3):197-206.

Park SK, Tedesco PM, Johnson TE. Oxidative stress and longevity in Caenorhabditis elegans as mediated by SKN-1. Aging Cell. 2009;8(3):258-69.

Weisiger RA, Fridovich I. Superoxide dismutase. Organelle specificity. J Biol Chem. 1973;248(10):3582-92.

Honda Y, Honda S. The daf-2 gene network for longevity regulates oxidative stress resistance and Mn-superoxide dismutase gene expression in Caenorhabditis elegans. FASEB J. 1999;13(11):1385-93.

Sanchez-Blanco A, Kim SK. Variable pathogenicity determines individual lifespan in Caenorhabditis elegans. PLoS Genet. 2011;7(4):e1002047.

Caplan S, Naslavsky N, Hartnell LM, Lodge R, Polishchuk RS, Donaldson JG, Bonifacino JS. A tubular EHD1-containing compartment involved in the recycling of major histocompatibility complex class I molecules to the plasma membrane. EMBO J. 2002;21(11):2557-2267.

Guilherme A, Soriano NA, Furcinitti PS, Czech MP. Role of EHD1 and EHBP1 in perinuclear sorting and insulin-regulated GLUT4 recycling in 3T3-L1 adipocytes. J Biol Chem. 2004;279(38):40062-75.

Kumar J, Park KC, Awasthi A, Prasad B. Silymarin extends lifespan and reduces proteotoxicity in C. elegans Alzheimer's model. CNS Neurol Disord Drug Targets. 2015;14(2):295-302.

Yang YL, Loh KS, Liou BY, Chu IH, Kuo CJ, Chen HD, Chen CS. SESN-1 is a positive regulator of lifespan in Caenorhabditis elegans. Exp Gerontol. 2013;48(3):371-9.

Hughes SE, Evason K, Xiong C, Kornfeld K. Genetic and pharmacological factors that influence reproductive aging in nematodes. PLoS Genet. 2007;3(2):e25.

Hsin H, Kenyon C. Signals from the reproductive system regulate the lifespan of C. elegans. Nature. 1999;399(6734):362-366.

Gruber J, Tang SY, Halliwell B. Evidence for a trade-off between survival and fitness caused by resveratrol treatment of Caenorhabditis elegans. Ann N Y Acad Sci. 2007;1100:530-42.

Park JK, Kim CK, Gong SK, Yu AR, Lee MY, Park SK. Acanthopanax sessiliflorus stem confers increased resistance to environmental stresses and lifespan extension in Caenorhabditis elegans. Nutr Res Pract. 2014;8(5):526-32.

Oh SI, Park JK, Park SK. Lifespan extension and increased resistance to environmental stressors by N-acetyl-L-cysteine in Caenorhabditis elegans. Clinics (Sao Paulo). 2015;70(5):380-6.

Hars ES, Qi H, Ryazanov AG, Jin S, Cai L, Hu C, Liu LF. Autophagy regulates ageing in C. elegans. Autophagy. 2007;3(2):93-5.

Melendez A, Talloczy Z, Seaman M, Eskelinen EL, Hall DH, Levine B. Autophagy genes are essential for dauer development and life-span extension in C. elegans. Science. 2003;301(5638):1387-91.

Juhasz G, Erdi B, Sass M, Neufeld TP. Atg7-dependent autophagy promotes neuronal health, stress tolerance, and longevity but is dispensable for metamorphosis in Drosophila. Genes Dev. 2007;21(23):3061-6.

Simonsen A, Cumming RC, Brech A, Isakson P, Schubert DR, Finley KD. Promoting basal levels of autophagy in the nervous system enhances longevity and oxidant resistance in adult Drosophila. Autophagy. 2008;4(2):176-84.


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