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Short Communication

Nuclear hormone receptors as mediators of metabolic adaptability following reproductive perturbations

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Article: e1151609 | Received 24 Sep 2015, Accepted 01 Feb 2016, Published online: 22 Mar 2016

References

  • Storlien L, Oakes ND, Kelley DE. Metabolic flexibility. Proc Nutrit Soc 2004; 63:363-8; PMID:15294056; http://dx.doi.org/10.1079/PNS2004349
  • Ghazi A. Transcriptional networks that mediate signals from reproductive tissues to influence lifespan. Genesis 2013; 51:1-15; PMID:22945891; http://dx.doi.org/10.1002/dvg.22345
  • Hansen M, Flatt T, Aguilaniu H. Reproduction, fat metabolism, and life span: what is the connection? Cell Metabol 2013; 17:10-9; PMID:23312280; http://dx.doi.org/10.1016/j.cmet.2012.12.003
  • Kenyon C. A pathway that links reproductive status to lifespan in Caenorhabditis elegans. Ann N Y Acad Sci 2010; 1204:156-62; PMID:20738286; http://dx.doi.org/10.1111/j.1749-6632.2010.05640.x
  • Maures TJ, Booth LN, Benayoun BA, Izrayelit Y, Schroeder FC, Brunet A. Males shorten the life span of C. elegans hermaphrodites via secreted compounds. Science 2014; 343:541-4; PMID:24292626; http://dx.doi.org/10.1126/science.1244160
  • Shi C, Murphy CT. Mating induces shrinking and death in Caenorhabditis mothers. Science 2014; 343:536-40; PMID:24356112; http://dx.doi.org/10.1126/science.1242958
  • Hsin H, Kenyon C. Signals from the reproductive system regulate the lifespan of C. elegans. Nature 1999; 399:362-6; PMID:10360574; http://dx.doi.org/10.1038/20694
  • Kirkwood TB. Evolution of ageing. Nature 1977; 270:301-4; PMID:593350; http://dx.doi.org/10.1038/270301a0
  • Le Cunff Y, Baudisch A, Pakdaman K. Evolution of aging: individual life history trade-offs and population heterogeneity account for mortality patterns across species. J Evol Biol 2014; 27:1706-20; PMID:24925106; http://dx.doi.org/10.1111/jeb.12423
  • Min KJ, Lee CK, Park HN. The lifespan of Korean eunuchs. Curr Biol 2012; 22:R792-3; PMID:23017989; http://dx.doi.org/10.1016/j.cub.2012.06.036
  • 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 2001; 292:107-10; PMID:11292875; http://dx.doi.org/10.1126/science.1057987
  • Keith SA, Ghazi A. Recent discoveries in the reproductive control of aging. Curr Genet Med Rep 2014; 3:26-34; http://dx.doi.org/10.1007/s40142-014-0060-8
  • Gwynne DT. Sexual conflict over nuptial gifts in insects. Annu Rev Entomol 2008; 53:83-101; PMID:17680720; http://dx.doi.org/10.1146/annurev.ento.53.103106.093423
  • Arantes-Oliveira N, Apfeld J, Dillin A, Kenyon C. Regulation of life-span by germ-line stem cells in Caenorhabditis elegans. Science 2002; 295:502-5; PMID:11799246; http://dx.doi.org/10.1126/science.1065768
  • Ghazi A, Henis-Korenblit S, Kenyon C. A transcription elongation factor that links signals from the reproductive system to lifespan extension in Caenorhabditis elegans. PLoS Genet 2009; 5:e1000639; PMID:19749979; http://dx.doi.org/10.1371/journal.pgen.1000639
  • Hansen M, Hsu AL, Dillin A, Kenyon C. New genes tied to endocrine, metabolic, and dietary regulation of lifespan from a Caenorhabditis elegans genomic RNAi screen. PLoS Genet 2005; 1:119-28; PMID:16103914; http://dx.doi.org/10.1371/journal.pgen.0010017
  • Lapierre LR, De Magalhaes Filho CD, McQuary PR, Chu CC, Visvikis O, Chang JT, Gelino S, Ong B, Davis AE, Irazoqui JE, et al. The TFEB orthologue HLH-30 regulates autophagy and modulates longevity in Caenorhabditis elegans. Nat Commun 2013; 4:2267; PMID:23925298
  • Lapierre LR, Gelino S, Melendez A, Hansen M. Autophagy and lipid metabolism coordinately modulate life span in germline-less C. elegans. Curr Biol 2011; 21:1507-14; PMID:21906946; http://dx.doi.org/10.1016/j.cub.2011.07.042
  • Steinbaugh MJ, Narasimhan SD, Robida-Stubbs S, Moronetti Mazzeo LE, Dreyfuss JM, Hourihan JM, Raghavan P, Operana TN, Esmaillie R, Blackwell TK. Lipid-mediated regulation of SKN-1/Nrf in response to germ cell absence. Elife 2015; 4; PMID:26196144; http://dx.doi.org/10.7554/eLife.07836
  • Gerisch B, Rottiers V, Li D, Motola DL, Cummins CL, Lehrach H, Mangelsdorf DJ, Antebi A. A bile acid-like steroid modulates Caenorhabditis elegans lifespan through nuclear receptor signaling. Proc Natl Acad Sci U S A 2007; 104:5014-9; PMID:17360327; http://dx.doi.org/10.1073/pnas.0700847104
  • Goudeau J, Bellemin S, Toselli-Mollereau E, Shamalnasab M, Chen Y, Aguilaniu H. Fatty acid desaturation links germ cell loss to longevity through NHR-80/HNF4 in C. elegans. PLoS Biol 2011; 9:e1000599; PMID:21423649; http://dx.doi.org/10.1371/journal.pbio.1000599
  • Ratnappan R, Amrit FR, Chen SW, Gill H, Holden K, Ward J, Yamamoto KR, Olsen CP, Ghazi A. Germline signals deploy NHR-49 to modulate fatty-acid beta-oxidation and desaturation in somatic tissues of C. elegans. PLoS Gen 2014; 10:e1004829; PMID:25474470; http://dx.doi.org/10.1371/journal.pgen.1004829
  • McCormick M, Chen K, Ramaswamy P, Kenyon C. New genes that extend Caenorhabditis elegans' lifespan in response to reproductive signals. Aging Cell 2012; 11:192-202; PMID:22081913; http://dx.doi.org/10.1111/j.1474-9726.2011.00768.x
  • Wang MC, O'Rourke EJ, Ruvkun G. Fat metabolism links germline stem cells and longevity in C. elegans. Science 2008; 322:957-60; PMID:18988854; http://dx.doi.org/10.1126/science.1162011
  • Zhang P, Judy M, Lee SJ, Kenyon C. Direct and indirect gene regulation by a life-extending FOXO protein in C. elegans: roles for GATA factors and lipid gene regulators. Cell Metabol 2013; 17:85-100; PMID:23312285; http://dx.doi.org/10.1016/j.cmet.2012.12.013
  • Evans RM, Mangelsdorf DJ. Nuclear Receptors, RXR, and the Big Bang. Cell 2014; 157:255-66; PMID:24679540; http://dx.doi.org/10.1016/j.cell.2014.03.012
  • Antebi A. Nuclear receptor signal transduction in C. elegans. Worm Book 2015:1-49; PMID:26069085; http://dx.doi.org/10.1895/wormbook.1.64.2
  • Taubert S, Ward JD, Yamamoto KR. Nuclear hormone receptors in nematodes: evolution and function. Mol Cell Endocrinol 2011; 334:49-55; PMID:20438802; http://dx.doi.org/10.1016/j.mce.2010.04.021
  • Van Gilst MR, Hadjivassiliou H, Jolly A, Yamamoto KR. Nuclear hormone receptor NHR-49 controls fat consumption and fatty acid composition in C. elegans. PLoS Biol 2005; 3:e53; PMID:15719061; http://dx.doi.org/10.1371/journal.pbio.0030053
  • Van Gilst MR, Hadjivassiliou H, Yamamoto KR. A Caenorhabditis elegans nutrient response system partially dependent on nuclear receptor NHR-49. Proc Natl Acad Sci U S A 2005; 102:13496-501; PMID:16157872; http://dx.doi.org/10.1073/pnas.0506234102
  • Burkewitz K, Morantte I, Weir HJ, Yeo R, Zhang Y, Huynh FK, Ilkayeva OR, Hirschey MD, Grant AR, Mair WB. Neuronal CRTC-1 governs systemic mitochondrial metabolism and lifespan via a catecholamine signal. Cell 2015; 160:842-55; PMID:25723162; http://dx.doi.org/10.1016/j.cell.2015.02.004
  • Folick A, Oakley HD, Yu Y, Armstrong EH, Kumari M, Sanor L, Moore DD, Ortlund EA, Zechner R, Wang MC. Aging. Lysosomal signaling molecules regulate longevity in Caenorhabditis elegans. Science 2015; 347:83-6; PMID:25554789; http://dx.doi.org/10.1126/science.1258857
  • Ma DK, Li Z, Lu AY, Sun F, Chen S, Rothe M, Menzel R, Sun F, Horvitz HR. Acyl-CoA Dehydrogenase Drives Heat Adaptation by Sequestering Fatty Acids. Cell 2015; 161:1152-63; PMID:25981666; http://dx.doi.org/10.1016/j.cell.2015.04.026
  • Poulsen L, Siersbaek M, Mandrup S. PPARs: fatty acid sensors controlling metabolism. Semin Cell Dev Biol 2012; 23:631-9; PMID:22273692; http://dx.doi.org/10.1016/j.semcdb.2012.01.003
  • Angelo G, Van Gilst MR. Starvation protects germline stem cells and extends reproductive longevity in C. elegans. Science 2009; 326:954-8; PMID:19713489; http://dx.doi.org/10.1126/science.1178343
  • Amrit FRG, Steenkiste EM, Ratnappan R, Chen S-W, McClendon TBH, Kostka D, Yanowitz JL, Olsen CP, & Ghazi A. (2016). DAF-16 and TCER-1 facilitate adaptation to germline loss by restoring lipid homeostasis and repressing reproductive physiology in C. elegans. PLoS Genet. 10(12):e1005788; PMID: 26862916; http://dx.doi./org/10.1371/journal.pgen.1005788
  • Brock TJ, Browse J, Watts JL. Genetic regulation of unsaturated fatty acid composition in C. elegans. PLoS genetics 2006; 2:e108; PMID:16839188
  • Arda HE, Taubert S, MacNeil LT, Conine CC, Tsuda B, Van Gilst M, Sequerra R, Doucette-Stamm L, Yamamoto KR, Walhout AJ. Functional modularity of nuclear hormone receptors in a Caenorhabditis elegans metabolic gene regulatory network. Mol Syst Biol 2010; 6:367; PMID:20461074; http://dx.doi.org/10.1038/msb.2010.23
  • Pathare PP, Lin A, Bornfeldt KE, Taubert S, Van Gilst MR. Coordinate regulation of lipid metabolism by novel nuclear receptor partnerships. PLoS genetics 2012; 8:e1002645; PMID:22511885; http://dx.doi.org/10.1371/journal.pgen.1002645
  • Reece-Hoyes JS, Pons C, Diallo A, Mori A, Shrestha S, Kadreppa S, Nelson J, Diprima S, Dricot A, Lajoie BR, et al. Extensive rewiring and complex evolutionary dynamics in a C. elegans multiparameter transcription factor network. Mol Cell 2013; 51:116-27; PMID:23791784; http://dx.doi.org/10.1016/j.molcel.2013.05.018
  • Libina N, Berman JR, Kenyon C. Tissue-specific activities of C. elegans DAF-16 in the regulation of lifespan. Cell 2003; 115:489-502; PMID:14622602; http://dx.doi.org/10.1016/S0092-8674(03)00889-4
  • Oh SW, Mukhopadhyay A, Dixit BL, Raha T, Green MR, Tissenbaum HA. Identification of direct DAF-16 targets controlling longevity, metabolism and diapause by chromatin immunoprecipitation. Nat Genet 2006; 38:251-7; PMID:16380712; http://dx.doi.org/10.1038/ng0406-398
  • Taubert S, Van Gilst MR, Hansen M, Yamamoto KR. A Mediator subunit, MDT-15, integrates regulation of fatty acid metabolism by NHR-49-dependent and -independent pathways in C. elegans. Genes Dev 2006; 20:1137-49; PMID:16651656; http://dx.doi.org/10.1101/gad.1395406
  • 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; 424:277-83; PMID:12845331; http://dx.doi.org/10.1038/nature01789
  • Berman JR, Kenyon C. Germ-cell loss extends C. elegans life span through regulation of DAF-16 by kri-1 and lipophilic-hormone signaling. Cell 2006; 124:1055-68; PMID:16530050; http://dx.doi.org/10.1016/j.cell.2006.01.039
  • Zhou YP, Grill V. Long term exposure to fatty acids and ketones inhibits B-cell functions in human pancreatic islets of Langerhans. J Clin Endocrinol Metab 1995; 80:1584-90; PMID:7745004
  • Kraegen EW, Cooney GJ. Free fatty acids and skeletal muscle insulin resistance. Curr Opin Lipidol 2008; 19:235-41; PMID:18460913; http://dx.doi.org/10.1097/01.mol.0000319118.44995.9a
  • Busch AK, Gurisik E, Cordery DV, Sudlow M, Denyer GS, Laybutt DR, Hughes WE, Biden TJ. Increased fatty acid desaturation and enhanced expression of stearoyl coenzyme A desaturase protects pancreatic beta-cells from lipoapoptosis. Diabetes 2005; 54:2917-24; PMID:16186393; http://dx.doi.org/10.2337/diabetes.54.10.2917
  • Peter A, Weigert C, Staiger H, Rittig K, Cegan A, Lutz P, Machicao F, Haring HU, Schleicher E. Induction of stearoyl-CoA desaturase protects human arterial endothelial cells against lipotoxicity. Am J Physiol Endocrinol Metab 2008; 295:E339-49; PMID:18523127; http://dx.doi.org/10.1152/ajpendo.00022.2008
  • Rockenfeller P, Ring J, Muschett V, Beranek A, Buettner S, Carmona-Gutierrez D, Eisenberg T, Khoury C, Rechberger G, Kohlwein SD, et al. Fatty acids trigger mitochondrion-dependent necrosis. Cell Cycle 2010; 9:2836-42; PMID:20647757; http://dx.doi.org/10.4161/cc.9.14.12346
  • Unger RH, Clark GO, Scherer PE, Orci L. Lipid homeostasis, lipotoxicity and the metabolic syndrome. Biochim Biophys Acta 2010; 1801:209-14; PMID:19948243; http://dx.doi.org/10.1016/j.bbalip.2009.10.006
  • Pai T, Yeh YY. Stearic acid unlike shorter-chain saturated fatty acids is poorly utilized for triacylglycerol synthesis and beta-oxidation in cultured rat hepatocytes. Lipids 1996; 31:159-64; PMID:8835403; http://dx.doi.org/10.1007/BF02522615
  • Nikawa J, Tanabe T, Ogiwara H, Shiba T, Numa S. Inhibitory effects of long-chain acyl coenzyme A analogues on rat liver acetyl coenzyme A carboxylase. FEBS Lett 1979; 102:223-6; PMID:37122; http://dx.doi.org/10.1016/0014-5793(79)80005-8
  • O'Rourke EJ, Soukas AA, Carr CE, Ruvkun G. C. elegans major fats are stored in vesicles distinct from lysosome-related organelles. Cell metabolism 2009; 10:430-5; PMID:19883620; http://dx.doi.org/10.1016/j.cmet.2009.10.002
  • Berryman DE, List EO, Coschigano KT, Behar K, Kim JK, Kopchick JJ. Comparing adiposity profiles in three mouse models with altered GH signaling. Growth Horm IGF Res 2004; 14:309-18; PMID:15231300; http://dx.doi.org/10.1016/j.ghir.2004.02.005
  • Judd ET, Wessels FJ, Drewry MD, Grove M, Wright K, Hahn DA, Hatle JD. Ovariectomy in grasshoppers increases somatic storage, but proportional allocation of ingested nutrients to somatic tissues is unchanged. Aging Cell 2011; 10:972-9; PMID:21834847; http://dx.doi.org/10.1111/j.1474-9726.2011.00737.x
  • Naukkarinen J, Heinonen S, Hakkarainen A, Lundbom J, Vuolteenaho K, Saarinen L, Hautaniemi S, Rodriguez A, Fruhbeck G, Pajunen P, et al. Characterising metabolically healthy obesity in weight-discordant monozygotic twins. Diabetologia 2014; 57:167-76; PMID:24100782; http://dx.doi.org/10.1007/s00125-013-3066-y
  • Gonzalez-Covarrubias V, Beekman M, Uh HW, Dane A, Troost J, Paliukhovich I, van der Kloet FM, Houwing-Duistermaat J, Vreeken RJ, Hankemeier T, et al. Lipidomics of familial longevity. Aging Cell 2013; 12:426-34; PMID:23451766; http://dx.doi.org/10.1111/acel.12064
  • Chauhan V, Sheikh A, Chauhan A, Tsiouris J, Malik M, Vaughan M. Changes during hibernation in different phospholipid and free and esterified cholesterol serum levels in black bears. Biochimie 2002; 84:1031-4; PMID:12504283; http://dx.doi.org/10.1016/S0300-9084(02)00006-8
  • Geiser F, McAllan BM, Kenagy GJ. The degree of dietary fatty acid unsaturation affects torpor patterns and lipid composition of a hibernator. J Comp Physiol B 1994; 164:299-305; PMID:7962785; http://dx.doi.org/10.1007/BF00346446
  • Ferreira CR, Saraiva SA, Catharino RR, Garcia JS, Gozzo FC, Sanvido GB, Santos LF, Lo Turco EG, Pontes JH, Basso AC, et al. Single embryo and oocyte lipid fingerprinting by mass spectrometry. J Lipid Res 2010; 51:1218-27; PMID:19965589; http://dx.doi.org/10.1194/jlr.D001768
  • Matorras R, Ruiz JI, Mendoza R, Ruiz N, Sanjurjo P, Rodriguez-Escudero FJ. Fatty acid composition of fertilization-failed human oocytes. Hum Reprod 1998; 13:2227-30; PMID:9756301; http://dx.doi.org/10.1093/humrep/13.8.2227
  • McEvoy TG, Coull GD, Broadbent PJ, Hutchinson JS, Speake BK. Fatty acid composition of lipids in immature cattle, pig and sheep oocytes with intact zona pellucida. J Reprod Fertil 2000; 118:163-70; PMID:10793638; http://dx.doi.org/10.1530/reprod/118.1.163
  • Barter PJ, Rye KA. Is there a role for fibrates in the management of dyslipidemia in the metabolic syndrome? Arterioscler Thromb Vasc Biol 2008; 28:39-46; PMID:17717290; http://dx.doi.org/10.1161/ATVBAHA.107.148817
  • Yang J, Chen L, Zhang X, Zhou Y, Zhang D, Huo M, Guan Y. PPARs and Female Reproduction: Evidence from Genetically Manipulated Mice. PPAR Res 2008; 2008:723243; PMID:18401459
  • Stunes AK, Westbroek I, Gustafsson BI, Fossmark R, Waarsing JH, Eriksen EF, Petzold C, Reseland JE, Syversen U. The peroxisome proliferator-activated receptor (PPAR) alpha agonist fenofibrate maintains bone mass, while the PPAR gamma agonist pioglitazone exaggerates bone loss, in ovariectomized rats. BMC Endocr Disord 2011; 11:11; PMID:21615901; http://dx.doi.org/10.1186/1472-6823-11-11
  • Amrit FR, Ratnappan R, Keith SA, Ghazi A. The C. elegans lifespan assay toolkit. Methods 2014; 68:465-75; PMID:24727064; http://dx.doi.org/10.1016/j.ymeth.2014.04.002
  • Reboul J, Vaglio P, Rual JF, Lamesch P, Martinez M, Armstrong CM, Li S, Jacotot L, Bertin N, Janky R, et al. C. elegans ORFeome version 1.1: experimental verification of the genome annotation and resource for proteome-scale protein expression. Nat Genet 2003; 34:35-41; PMID:12679813; http://dx.doi.org/10.1038/ng1140
  • Deplancke B, Vermeirssen V, Arda HE, Martinez NJ, Walhout AJ. Gateway-compatible yeast one-hybrid screens. CSH Protoc 2006; 2006:pdb.prot4590-pdb.prot4590 PMID:22485967; http://dx.doi.org/10.1 101/pdb.prot4590

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