Lipid-mediated regulation of SKN-1/Nrf in response to germ cell absence

eLife

Volumn 4, Issue JULY2015, 2015, Pages

  Steinbaugh, Michael J ^a,b   Narasimhan, Sri Devi ^a,b   Robida Stubbs, Stacey ^a,b   Moronetti Mazzeo, Lorenza E ^a,b   Dreyfuss, Jonathan M ^a,c   Hourihan, John M ^a,b   Raghavan, Prashant ^a,b   Operaña, Theresa N ^a,b   Esmaillie, Reza ^a,b   Blackwell, T Keith ^a,b  

^a JOSLIN DIABETES CENTER   (United States)

^b HARVARD STEM CELL INSTITUTE   (United States)

^c Boston University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEASOME; SKINHEAD 1 PROTEIN; SYNAPTOPHYSIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR DAF 16; TRIACYLGLYCEROL; TRIACYLGLYCEROL LIPASE; UNCLASSIFIED DRUG; CAENORHABDITIS ELEGANS PROTEIN; DNA BINDING PROTEIN; SKN-1 PROTEIN, C ELEGANS;

ARTICLE; EGG YOLK; ENZYME ACTIVITY; EXTRACELLULAR MATRIX; GERM CELL; LIFESPAN; LIPID METABOLISM; LIPID STORAGE; LONGEVITY; NONHUMAN; OXIDATIVE STRESS; REPRODUCTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA SEQUENCE; STRESS; SURVIVAL; ANIMAL; CAENORHABDITIS ELEGANS; GENE EXPRESSION REGULATION; METABOLISM; PHYSIOLOGY;

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION; GERM CELLS; LIPID METABOLISM; TRANSCRIPTION FACTORS;

EID: 84940501621     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.07836     Document Type: Article

References (124)

1. Ackerman D, Gems D. 2012. The mystery of C. elegans aging: an emerging role for fat. Distant parallels between C. elegans aging and metabolic syndrome? Bioessays 34:466-471. doi: 10.1002/bies.201100189.
2. Adler BJ, Kaushansky K, Rubin CT. 2014. Obesity-driven disruption of haematopoiesis and the bone marrow niche. Nature Reviews. Endocrinology 10:737-748. doi: 10.1038/nrendo.2014.169.
3. Alper S, McElwee MK, Apfeld J, Lackford B, Freedman JH, Schwartz DA. 2010. The Caenorhabditis elegans germ line regulates distinct signaling pathways to control lifespan and innate immunity. The Journal of Biological Chemistry 285:1822-1828. doi: 10.1074/jbc.M109.057323.
4. An JH, Blackwell TK. 2003. SKN-1 links C. elegans mesendodermal specification to a conserved oxidative stress response. Genes & Development 17:1882-1893. doi: 10.1101/gad.1107803.
5. Anders S, McCarthy DJ, Chen Y, Okoniewski M, Smyth GK, Huber W, Robinson MD. 2013. Count-based differential expression analysis of RNA sequencing data using R and Bioconductor. Nature Protocols 8: 1765-1786. doi: 10.1038/nprot.2013.099.
6. Antebi A. 2013. Regulation of longevity by the reproductive system. Experimental Gerontology 48:596-602. doi: 10.1016/j.exger.2012.09.009.
7. Arantes-Oliveira N, Apfeld J, Dillin A, Kenyon C. 2002. Regulation of life-span by germ-line stem cells in Caenorhabditis elegans. Science 295:502-505. doi: 10.1126/science.1065768.
8. Ben-Zvi A, Miller EA, Morimoto RI. 2009. Collapse of proteostasis represents an early molecular event in Caenorhabditis elegans aging. Proceedings of the National Academy of Sciences of USA 106:14914-14919. doi: 10.1073/pnas.0902882106.
9. Benjamini Y, Hochberg Y. 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal statistical Society. Series B (Methodological) 57:289-300. doi: 10.2307/2346101.
10. Berman JR, Kenyon C. 2006. Germ-cell loss extends C. elegans life span through regulation of DAF-16 by kri-1 and lipophilic-hormone signaling. Cell 124:1055-1068. doi: 10.1016/j.cell.2006.01.039.
11. Bishop NA, Guarente L. 2007. Two neurons mediate diet-restriction-induced longevity in C. elegans. Nature 447: 545-549. doi: 10.1038/nature05904.
12. Bowerman B, Eaton BA, Priess JR. 1992. skn-1, a maternally expressed gene required to specify the fate of ventral blastomeres in the early C. elegans embryo. Cell 68:1061-1075. doi: 10.1016/0092-8674(92)90078-Q.
13. Brenner S. 1974. The genetics of Caenorhabditis elegans. Genetics 77:71-94.
14. Chikina MD, Huttenhower C, Murphy CT, Troyanskaya OG. 2009. Global prediction of tissue-specific gene expression and context-dependent gene networks in Caenorhabditis elegans. PLOS Computational Biology 5: e1000417. doi: 10.1371/journal.pcbi.1000417.
15. Choe KP, Przybysz AJ, Strange K. 2009. The WD40 repeat protein WDR-23 functions with the CUL4/DDB1 ubiquitin ligase to regulate nuclear abundance and activity of SKN-1 in Caenorhabditis elegans. Molecular and Cellular Biology 29:2704-2715. doi: 10.1128/MCB.01811-08.
16. Chondrogianni N, Georgila K, Kourtis N, Tavernarakis N, Gonos ES. 2015. 20S proteasome activation promotes life span extension and resistance to proteotoxicity in Caenorhabditis elegans. FASEB Journal: Official Publication of the Federation of American Societies for Experimental Biology 29:611-622. doi: 10.1096/fj.14-252189.
17. Cohen JC, Horton JD, Hobbs HH. 2011. Human fatty liver disease: old questions and new insights. Science 332: 1519-1523. doi: 10.1126/science.1204265.
18. Curran SP, Ruvkun G. 2007. Lifespan regulation by evolutionarily conserved genes essential for viability. PLOS Genetics 3:e56. doi: 10.1371/journal.pgen.0030056.
19. Dennis G Jr, Sherman BT, Hosack DA, Yang J, Gao W, Lane HC, Lempicki RA. 2003. DAVID: database for annotation, visualization, and integrated discovery. Genome Biology 4:P3. doi: 10.1186/gb-2003-4-5-p3.
20. Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, Batut P, Chaisson M, Gingeras TR. 2013. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29:15-21. doi: 10.1093/bioinformatics/bts635.
21. Dorsett M, Westlund B, Schedl T. 2009. METT-10, a putative methyltransferase, inhibits germ cell proliferative fate in Caenorhabditis elegans. Genetics 183:233-247. doi: 10.1534/genetics.109.105270.
22. Durinck S, Moreau Y, Kasprzyk A, Davis S, De Moor B, Brazma A, Huber W. 2005. BioMart and Bioconductor: a powerful link between biological databases and microarray data analysis. Bioinformatics 21:3439-3440. doi: 10. 1093/bioinformatics/bti525.
23. Durinck S, Spellman PT, Birney E, Huber W. 2009. Mapping identifiers for the integration of genomic datasets with the R/Bioconductor package biomaRt. Nature Protocols 4:1184-1191. doi: 10.1038/nprot.2009.97.
24. Ewald CY, Landis JN, Abate JP, Murphy CT, Blackwell TK. 2015. Dauer-independent insulin/IGF-1-signalling implicates collagen remodelling in longevity. Nature 519:97-101. doi: 10.1038/nature14021.
25. Flatt T, Min KJ, D'Alterio C, Villa-Cuesta E, Cumbers J, Lehmann R, Jones DL, Tatar M. 2008. Drosophila germ-line modulation of insulin signaling and lifespan. Proceedings of the National Academy of Sciences of USA 105: 6368-6373. doi: 10.1073/pnas.0709128105.
26. Folick A, Oakley HD, Yu Y, Armstrong EH, Kumari M, Sanor L, Moore DD, Ortlund EA, Zechner R, Wang MC. 2015. Aging. Lysosomal signaling molecules regulate longevity in Caenorhabditis elegans. Science 347:83-86. doi: 10. 1126/science.1258857.
27. Fu J, Gaetani S, Oveisi F, Lo Verme J, Serrano A, Rodriguez De Fonseca F, Rosengarth A, Luecke H, Di Giacomo B, Tarzia G, Piomelli D. 2003. Oleylethanolamide regulates feeding and body weight through activation of the nuclear receptor PPAR-alpha. Nature 425:90-93. doi: 10.1038/nature01921.
28. Furuyama T, Nakazawa T, Nakano I, Mori N. 2000. Identification of the differential distribution patterns of mRNAs and consensus binding sequences for mouse DAF-16 homologues. The Biochemical Journal 349:629-634. doi: 10.1042/0264-6021:3490629.
29. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, Ellis B, Gautier L, Ge Y, Gentry J, Hornik K, Hothorn T, Huber W, Iacus S, Irizarry R, Leisch F, Li C, Maechler M, Rossini AJ, Sawitzki G, Smith C, Smyth G, Tierney L, Yang JY, Zhang J. 2004. Bioconductor: open software development for computational biology and bioinformatics. Genome Biology 5:R80. doi: 10.1186/gb-2004-5-10-r80.
30. Gerstein MB, Lu ZJ, Van Nostrand EL, Cheng C, Arshinoff BI, Liu T, Yip KY, Robilotto R, Rechtsteiner A, Ikegami K, Alves P, Chateigner A, Perry M, Morris M, Auerbach RK, Feng X, Leng J, Vielle A, Niu W, Rhrissorrakrai K, Agarwal A, Alexander RP, Barber G, Brdlik CM, Brennan J, Brouillet JJ, Carr A, Cheung MS, Clawson H, Contrino S, Dannenberg LO, Dernburg AF, Desai A, Dick L, Dosé AC, Du J, Egelhofer T, Ercan S, Euskirchen G, Ewing B, Feingold EA, Gassmann R, Good PJ, Green P, Gullier F, Gutwein M, Guyer MS, Habegger L, Han T, Henikoff JG, Henz SR, Hinrichs A, Holster H, Hyman T, Iniguez AL, Janette J, Jensen M, Kato M, Kent WJ, Kephart E, Khivansara V, Khurana E, Kim JK, Kolasinska-Zwierz P, Lai EC, Latorre I, Leahey A, Lewis S, Lloyd P, Lochovsky L, Lowdon RF, Lubling Y, Lyne R, MacCoss M, Mackowiak SD, Mangone M, McKay S, Mecenas D, Merrihew G, Miller DM III, Muroyama A, Murray JI, Ooi SL, Pham H, Phippen T, Preston EA, Rajewsky N, Rätsch G, Rosenbaum H, Rozowsky J, Rutherford K, Ruzanov P, Sarov M, Sasidharan R, Sboner A, Scheid P, Segal E, Shin H, Shou C, Slack FJ, Slightam C, Smith R, Spencer WC, Stinson EO, Taing S, Takasaki T, Vafeados D, Voronina K, Wang G, Washington NL, Whittle CM, Wu B, Yan KK, Zeller G, Zha Z, Zhong M, Zhou X, modENCODE Consortium, Ahringer J, Strome S, Gunsalus KC, Micklem G, Liu XS, Reinke AV, Kim SK, Hillier LW, Henikoff S, Piano F, Snyder M, Stein L, Lieb JD, Waterston RH. 2010. Integrative analysis of the Caenorhabditis elegans genome by the modENCODE project. Science 330:1775-1787. doi: 10.1126/science.1196914.
31. Ghazi A, Henis-Korenblit S, Kenyon C. 2009. A transcription elongation factor that links signals from the reproductive system to lifespan extension in Caenorhabditis elegans. PLOS Genetics 5:e1000639. doi: 10.1371/ journal.pgen.1000639.
32. Glickman MH, Ciechanover A. 2002. The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction. Physiological Reviews 82:373-428. doi: 10.1152/physrev.00027.2001.
33. Goldberg AL. 2003. Protein degradation and protection against misfolded or damaged proteins. Nature 426: 895-899. doi: 10.1038/nature02263.
34. Goudeau J, Bellemin S, Toselli-Mollereau E, Shamalnasab M, Chen Y, Aguilaniu H. 2011. Fatty acid desaturation links germ cell loss to longevity through NHR-80/HNF4 in C. elegans. PLOS Biology 9:e1000599. doi: 10.1371/ journal.pbio.1000599.
35. Grant B, Hirsh D. 1999. Receptor-mediated endocytosis in the Caenorhabditis elegans oocyte. Molecular Biology of the Cell 10:4311-4326. doi: 10.1091/mbc.10.12.4311.
36. Han S, Brunet A. 2015. Cell biology. Lysosomal lipid lengthens life span. Science 347:32-33. doi: 10.1126/science.aaa4565.
37. Hansen M, Flatt T, Aguilaniu H. 2013. Reproduction, fat metabolism, and life span: what is the connection? Cell Metabolism 17:10-19. doi: 10.1016/j.cmet.2012.12.003.
38. Hayes JD, Dinkova-Kostova AT. 2014. The Nrf2 regulatory network provides an interface between redox and intermediary metabolism. Trends in Biochemical Sciences 39:199-218. doi: 10.1016/j.tibs.2014.02.002.
39. Henderson ST, Johnson TE. 2001. daf-16 integrates developmental and environmental inputs to mediate aging in the nematode Caenorhabditis elegans. Current Biology 11:1975-1980. doi: 10.1016/S0960-9822(01)00594-2.
40. Hoogewijs D, Houthoofd K, Matthijssens F, Vandesompele J, Vanfleteren JR. 2008. Selection and validation of a set of reliable reference genes for quantitative sod gene expression analysis in C. elegans. BMC Molecular Biology 9:9. doi: 10.1186/1471-2199-9-9.
41. Hsin H, Kenyon C. 1999. Signals from the reproductive system regulate the lifespan of C. elegans. Nature 399: 362-366. doi: 10.1038/20694.
42. Inoue H, Hisamoto N, An JH, Oliveira RP, Nishida E, Blackwell TK, Matsumoto K. 2005. The C. elegans p38 MAPK pathway regulates nuclear localization of the transcription factor SKN-1 in oxidative stress response. Genes & Development 19:2278-2283. doi: 10.1101/gad.1324805.
43. Jones DL, Wagers AJ. 2008. No place like home: anatomy and function of the stem cell niche. Nature Reviews. Molecular Cell Biology 9:11-21. doi: 10.1038/nrm2319.
44. Kamath RS, Martinez-Campos M, Zipperlen P, Fraser AG, Ahringer J. 2001. Effectiveness of specific RNAmediated interference through ingested double-stranded RNA in Caenorhabditis elegans. Genome Biology 2: RESEA-RCH0002. doi: 10.1186/gb-2000-2-1-research0002.
45. Kel AE, Gossling E, Reuter I, Cheremushkin E, Kel-Margoulis OV, Wingender E. 2003. MATCH: a tool for searching transcription factor binding sites in DNA sequences. Nucleic Acids Research 31:3576-3579. doi: 10.1093/nar/ gkg585.
46. Kenyon CJ. 2010. The genetics of ageing. Nature 464:504-512. doi: 10.1038/nature08980.
47. Kimble J, Crittenden SL. 2005. Germline proliferation and its control. Wormbook 1-14. doi: 10.1895/wormbook.1.13.1.
48. Kisselev AF, Goldberg AL. 2005. Monitoring activity and inhibition of 26S proteasomes with fluorogenic peptide substrates. Methods Enzymol 398:364-378. doi: 10.1016/S0076-6879(05)98030-0.
49. Kniazeva M, Han M. 2013. Fat chance for longevity. Genes & Development 27:351-354. doi: 10.1101/gad. 214189.113.
50. Kokatnur MG, Oalmann MC, Johnson WD, Malcom GT, Strong JP. 1979. Fatty acid composition of human adipose tissue from two anatomical sites in a biracial community. The American Journal of Clinical Nutrition 32: 2198-2205.
51. Lapierre LR, Gelino S, Melendez A, Hansen M. 2011. Autophagy and lipid metabolism coordinately modulate life span in germline-less C. elegans. Current Biology 21:1507-1514. doi: 10.1016/j.cub.2011.07.042.
52. Law CW, Chen Y, Shi W, Smyth GK. 2014. voom: precision weights unlock linear model analysis tools for RNA-seq read counts. Genome Biology 15:R29. doi: 10.1186/gb-2014-15-2-r29.
53. Lawrence M, Huber W, Pages H, Aboyoun P, Carlson M, Gentleman R, Morgan MT, Carey VJ. 2013. Software for computing and annotating genomic ranges. PLOS Computational Biology 9:e1003118. doi: 10.1371/journal.pcbi. 1003118.
54. Lee CS, Ho DV, Chan JY. 2013. Nuclear factor-erythroid 2-related factor 1 regulates expression of proteasome genes in hepatocytes and protects against endoplasmic reticulum stress and steatosis in mice. The FEBS Journal 280:3609-3620. doi: 10.1111/febs.12350.
55. Leiser SF, Miller RA. 2010. Nrf2 signaling, a mechanism for cellular stress resistance in long-lived mice. Molecular and Cellular Biology 30:871-884. doi: 10.1128/MCB.01145-09.
56. Li X, Matilainen O, Jin C, Glover-Cutter KM, Holmberg CI, Blackwell TK. 2011. Specific SKN-1/Nrf stress responses to perturbations in translation elongation and proteasome activity. PLOS Genetics 7:e1002119. doi: 10.1371/ journal.pgen.1002119.
57. Liao Y, Smyth GK, Shi W. 2013. The Subread aligner: fast, accurate and scalable read mapping by seed-and-vote. Nucleic Acids Research 41:e108. doi: 10.1093/nar/gkt214.
58. Liao Y, Smyth GK, Shi W. 2014. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 30:923-930. doi: 10.1093/bioinformatics/btt656.
59. Libina N, Berman JR, Kenyon C. 2003. Tissue-specific activities of C. elegans DAF-16 in the regulation of lifespan. Cell 115:489-502. doi: 10.1016/S0092-8674(03)00889-4.
60. Lim JH, Gerhart-Hines Z, Dominy JE, Lee Y, Kim S, Tabata M, Xiang YK, Puigserver P. 2013. Oleic acid stimulates complete oxidation of fatty acids through protein kinase A-dependent activation of SIRT1-PGC1alpha complex. The Journal of Biological Chemistry 288:7117-7126. doi: 10.1074/jbc.M112.415729.
61. Lin K, Hsin H, Libina N, Kenyon C. 2001. Regulation of the Caenorhabditis elegans longevity protein DAF-16 by insulin/IGF-1 and germline signaling. Nature Genetics 28:139-145. doi: 10.1038/88850.
62. Link CD, Johnson CJ. 2002. Reporter transgenes for study of oxidant stress in Caenorhabditis elegans. Methods Enzymol 353:497-505. doi: 10.1016/S0076-6879(02)53072-X.
63. Matys V, Kel-Margoulis OV, Fricke E, Liebich I, Land S, Barre-Dirrie A, Reuter I, Chekmenev D, Krull M, Hornischer K, Voss N, Stegmaier P, Lewicki-Potapov B, Saxel H, Kel AE, Wingender E. 2006. TRANSFAC and its module TRANSCompel: transcriptional gene regulation in eukaryotes. Nucleic Acids Research 34:D108-D110. doi: 10. 1093/nar/gkj143.
64. McCormick M, Chen K, Ramaswamy P, Kenyon C. 2012. New genes that extend Caenorhabditis elegans' lifespan in response to reproductive signals. Aging Cell 11:192-202. doi: 10.1111/j.1474-9726.2011.00768.x.
65. Mercier E, Gottardo R. 2014. MotIV: Motif Identification and Validation. http://bioconductor.org/packages/MotIV/.
66. Min KJ, Lee CK, Park HN. 2012. The lifespan of Korean eunuchs. Current Biology 22:R792-R793. doi: 10.1016/j. cub.2012.06.036.
67. Mitchell DH, Stiles JW, Santelli J, Sanadi DR. 1979. Synchronous growth and aging of Caenorhabditis elegans in the presence of fluorodeoxyuridine. Journal of Gerontology 34:28-36. doi: 10.1093/geronj/34.1.28.
68. Mizunuma M, Neumann-Haefelin E, Moroz N, Li Y, Blackwell TK. 2014. mTORC2-SGK-1 acts in two environmentally responsive pathways with opposing effects on longevity. Aging Cell 13:869-878. doi: 10.1111/ acel.12248.
69. Moerman DG, Williams BD. 2006. Sarcomere assembly in C. elegans muscle. Wormbook 1-16. doi: 10.1895/ wormbook.1.81.1.
70. Moroz N, Carmona JJ, Anderson E, Hart AC, Sinclair DA, Blackwell TK. 2014. Dietary restriction involves NAD(+)-dependent mechanisms and a shift toward oxidative metabolism. Aging Cell 13:1075-1085. doi: 10.1111/acel. 12273.
71. Murphy CT, McCarroll SA, Bargmann CI, Fraser A, Kamath RS, Ahringer J, Li H, Kenyon C. 2003. Genes that act downstream of DAF-16 to influence the lifespan of Caenorhabditis elegans. Nature 424:277-283. doi: 10.1038/ nature01789.
72. Muruganandan S, Sinal CJ. 2014. The impact of bone marrow adipocytes on osteoblast and osteoclast differentiation. IUBMB Life 66:147-155. doi: 10.1002/iub.1254.
73. Na H, Zhang P, Chen Y, Zhu X, Liu Y, Author, Xie K, Xu N, Yang F, Yu Y, et al. 2015. Identification of lipid droplet structure-like/Resident proteins in Caenorhabditis elegans. Biochimica et Biophysica Acta S0167-S4889. doi: 10. 1016/j.bbamcr.2015.05.020.
74. National Research Council. 1976. Fat content and composition of animal products. Washington, DC: Printing and Publishing Office, National Academy of Sciences.
75. Na H, Zhang P, Chen Y, Zhu X, Liu Y, Liu Y, Xie K, Xu N, Yang F, Yu Y, Cichello S, Mak HY, Wang MC, Zhang H, Liu P. 2011. Diverse transcription factor binding features revealed by genome-wide ChIP-seq in C. elegans. Genome Research 21:245-254. doi: 10.1101/gr.114587.110.
76. O'Rourke EJ, Kuballa P, Xavier R, Ruvkun G. 2013. omega-6 Polyunsaturated fatty acids extend life span through the activation of autophagy. Genes & Development 27:429-440. doi: 10.1101/gad.205294.112.
77. O'Rourke EJ, Ruvkun G. 2013. MXL-3 and HLH-30 transcriptionally link lipolysis and autophagy to nutrient availability. Nature Cell Biology 15:668-676. doi: 10.1038/ncb2741.
78. O'Rourke EJ, Soukas AA, Carr CE, Ruvkun G. 2009. C. elegans major fats are stored in vesicles distinct from lysosome-related organelles. Cell Metabolism 10:430-435. doi: 10.1016/j.cmet.2009.10.002.
79. Okada K, Warabi E, Sugimoto H, Horie M, Gotoh N, Tokushige K, Hashimoto E, Utsunomiya H, Takahashi H, Ishii T, Yamamoto M, Shoda J. 2013. Deletion of Nrf2 leads to rapid progression of steatohepatitis in mice fed atherogenic plus high-fat diet. Journal of Gastroenterology 48:620-632. doi: 10.1007/s00535-012-0659-z.
80. Oliveira RP, Porter Abate J, Dilks K, Landis J, Ashraf J, Murphy CT, Blackwell TK. 2009. Condition-adapted stress and longevity gene regulation by Caenorhabditis elegans SKN-1/Nrf. Aging Cell 8:524-541. doi: 10.1111/j.1474-9726.2009.00501.x.
81. Ou J, Brodsky M, Wolfe S, Zhu LJ. 2013. motifStack: Plot stacked logos for single or multiple DNA, RNA and amino acid sequence. http://bioconductor.org/packages/motifStack/.
82. Paek J, Lo JY, Narasimhan SD, Nguyen TN, Glover-Cutter K, Robida-Stubbs S, Suzuki T, Yamamoto M, Blackwell TK, Curran SP. 2012. Mitochondrial SKN-1/Nrf mediates a conserved starvation response. Cell Metabolism 16: 526-537. doi: 10.1016/j.cmet.2012.09.007.
83. Pang S, Lynn DA, Lo JY, Paek J, Curran SP. 2014. SKN-1 and Nrf2 couples proline catabolism with lipid metabolism during nutrient deprivation. Nature Communications 5:5048. doi: 10.1038/ncomms6048.
84. Park SK, Tedesco PM, Johnson TE. 2009. Oxidative stress and longevity in Caenorhabditis elegans as mediated by SKN-1. Aging Cell 8:258-269. doi: 10.1111/j.1474-9726.2009.00473.x.
85. Partridge L, Gems D, Withers DJ. 2005. Sex and death: what is the connection? Cell 120:461-472. doi: 10.1016/j. cell.2005.01.026.
86. Porta-de-la-Riva M, Fontrodona L, Villanueva A, Ceron J. 2012. Basic Caenorhabditis elegans methods: synchronization and observation. Journal of Visualized Experiments e4019. doi: 10.3791/4019.
87. Pulak R. 2006. Techniques for analysis, sorting, and dispensing of C. elegans on the COPAS flow-sorting system. Methods in Molecular Biology 351:275-286. doi: 10.1385/1-59745-151-7:275.
88. R Core Team. 2014. R: a language and environment for statistical computing. Vienna, Austria. http://www.R-project.org/.
89. Radhakrishnan SK, den Besten W, Deshaies RJ. 2014. p97-dependent retrotranslocation and proteolytic processing govern formation of active Nrf1 upon proteasome inhibition. eLife 3:e01856. doi: 10.7554/eLife. 01856.
90. Radhakrishnan SK, Lee CS, Young P, Beskow A, Chan JY, Deshaies RJ. 2010. Transcription factor Nrf1 mediates the proteasome recovery pathway after proteasome inhibition in mammalian cells. Molecular Cell 38:17-28. doi: 10.1016/j.molcel.2010.02.029.
91. Ratnappan R, Amrit FR, Chen SW, Gill H, Holden K, Ward J, Yamamoto KR, Olsen CP, Ghazi A. 2014. Germline signals deploy NHR-49 to modulate fatty-acid beta-oxidation and desaturation in somatic tissues of C. elegans. PLOS Genetics 10:e1004829. doi: 10.1371/journal.pgen.1004829.
92. Richmond J. 2005. Synaptic function. Wormbook 1-14. doi: 10.1895/wormbook.1.69.1.
93. Robida-Stubbs S, Glover-Cutter K, Lamming DW, Mizunuma M, Narasimhan SD, Neumann-Haefelin E, Sabatini DM, Blackwell TK. 2012. TOR signaling and rapamycin influence longevity by regulating SKN-1/Nrf and DAF-16/ FoxO. Cell Metabolism 15:713-724. doi: 10.1016/j.cmet.2012.04.007.
94. Sandelin A, Alkema W, Engstrom P, Wasserman WW, Lenhard B. 2004. JASPAR: an open-access database for eukaryotic transcription factor binding profiles. Nucleic Acids Research 32:D91-D94. doi: 10.1093/nar/gkh012.
95. Schmeisser S, Schmeisser K, Weimer S, Groth M, Priebe S, Fazius E, Kuhlow D, Pick D, Einax JW, Guthke R, Platzer M, Zarse K, Ristow M. 2013. Mitochondrial hormesis links low-dose arsenite exposure to lifespan extension. Aging Cell 12:508-517. doi: 10.1111/acel.12076.
96. Sha Z, Goldberg AL. 2014. Proteasome-mediated processing of Nrf1 is essential for coordinate induction of all proteasome subunits and p97. Current Biology 24:1573-1583. doi: 10.1016/j.cub.2014.06.004.
97. Shannon P. 2014. MotifDb: An annotated collection of protein-DNA binding sequence motifs. http://bioconductor. org/packages/MotifDb/.
98. Shaye DD, Greenwald I. 2011. OrthoList: a compendium of C. elegans genes with human orthologs. PLOS ONE 6: e20085. doi: 10.1371/journal.pone.0020085.
99. Shen Y, Wollam J, Magner D, Karalay O, Antebi A. 2012. A steroid receptor-microRNA switch regulates life span in response to signals from the gonad. Science 338:1472-1476. doi: 10.1126/science.1228967.
100. Smyth GK. 2005. limma: linear models for microarray data. Computational Biology Solutions Using R and Bioconductor, Statistics for Biology and Health. p. 397-420. doi: 10.1007/0-387-29362-0_23.
101. Staab TA, Griffen TC, Corcoran C, Evgrafov O, Knowles JA, Sieburth D. 2013a. The conserved SKN-1/Nrf2 stress response pathway regulates synaptic function in Caenorhabditis elegans. PLOS Genetics 9:e1003354. doi: 10. 1371/journal.pgen.1003354.
102. Staab TA, Griffen TC, Corcoran C, Evgrafov O, Knowles JA, Sieburth D. 2013b. SKN-1 from the JASPAR CORE database. JASPAR MA0547.1. http://jaspar.genereg.net/cgi-bin/jaspar_db.pl?rm=browse&db=core&tax_group=nematodes.
103. Steffen J, Seeger M, Koch A, Kruger E. 2010. Proteasomal degradation is transcriptionally controlled by TCF11 via an ERAD-dependent feedback loop. Molecular Cell 40:147-158. doi: 10.1016/j.molcel.2010.09.012.
104. Steinbaugh MJ, Sun LY, Bartke A, Miller RA. 2012. Activation of genes involved in xenobiotic metabolism is a shared signature of mouse models with extended lifespan. American Journal of Physiology. Endocrinology and Metabolism 303:E488-E495. doi: 10.1152/ajpendo.00110.2012.
105. Steinbaugh MJ, Dreyfuss JM, Blackwell TK. 2015. RNA-seq analysis of germline stem cell removal and loss of SKN-1 in C. elegans. NCBI Gene Expression Omnibus GSE63075. http://www.ncbi.nlm.nih.gov/geo/query/acc. cgi?acc=GSE63075.
106. Sykiotis GP, Bohmann D. 2010. Stress-activated cap'n'collar transcription factors in aging and human disease. Science Signaling 3:re3. doi: 10.1126/scisignal.3112re3.
107. Tsujita T, Peirce V, Baird L, Matsuyama Y, Takaku M, Walsh SV, Griffin JL, Uruno A, Yamamoto M, Hayes JD. 2014. Transcription factor Nrf1 negatively regulates the cystine/glutamate transporter and lipid-metabolizing enzymes. Molecular and Cellular Biology 34:3800-3816. doi: 10.1128/MCB.00110-14.
108. Tullet JM, Hertweck M, An JH, Baker J, Hwang JY, Liu S, Oliveira RP, Baumeister R, Blackwell TK. 2008. Direct inhibition of the longevity-promoting factor SKN-1 by insulin-like signaling in C. elegans. Cell 132:1025-1038. doi: 10.1016/j.cell.2008.01.030.
109. Vilchez D, Morantte I, Liu Z, Douglas PM, Merkwirth C, Rodrigues AP, Manning G, Dillin A. 2012. RPN-6 determines C. elegans longevity under proteotoxic stress conditions. Nature 489:263-268. doi: 10.1038/ nature11315.
110. Wang MC, O'Rourke EJ, Ruvkun G. 2008. Fat metabolism links germline stem cells and longevity in C. elegans. Science 322:957-960. doi: 10.1126/science.1162011.
111. Warnes GR, Bolker B, Bonebakker L, Gentleman R, Liaw WHA, Lumley T, Maechler M, Magnusson A, Moeller S, Schwartz M, Venables B. 2014. gplots: various R programming tools for plotting data. http://CRAN.R-project.org/ package=gplots.
112. Xu Z, Chen L, Leung L, Yen TS, Lee C, Chan JY. 2005. Liver-specific inactivation of the Nrf1 gene in adult mouse leads to nonalcoholic steatohepatitis and hepatic neoplasia. Proceedings of the National Academy of Sciences of USA 102:4120-4125. doi: 10.1073/pnas.0500660102.
113. Yang F, Vought BW, Satterlee JS, Walker AK, Jim Sun ZY, Watts JL, DeBeaumont R, Saito RM, Hyberts SG, Yang S, Macol C, Iyer L, Tjian R, van den Heuvel S, Hart AC, Wagner G, Näär AM. 2006. An ARC/Mediator subunit required for SREBP control of cholesterol and lipid homeostasis. Nature 442:700-704. doi: 10.1038/nature04942.
114. Yen K, Le TT, Bansal A, Narasimhan SD, Cheng JX, Tissenbaum HA. 2010. A comparative study of fat storage quantitation in nematode Caenorhabditis elegans using label and label-free methods. PLOS ONE 5:e12810. doi: 10.1371/journal.pone.0012810.
115. Zarse K, Schmeisser S, Groth M, Priebe S, Beuster G, Kuhlow D, Guthke R, Platzer M, Kahn CR, Ristow M. 2012. Impaired insulin/IGF1 signaling extends life span by promoting mitochondrial L-proline catabolism to induce a transient ROS signal. Cell Metabolism 15:451-465. doi: 10.1016/j.cmet.2012.02.013.
116. Zhang P, Na H, Liu Z, Zhang S, Xue P, Chen Y, Pu J, Peng G, Huang X, Yang F, Xie Z, Xu T, Xu P, Ou G, Zhang SO, Liu P. 2012. Proteomic study and marker protein identification of Caenorhabditis elegans lipid droplets. Molecular & Cellular Proteomics 11:317-328. doi: 10.1074/mcp.M111.016345.
117. Zhong M, Snyder M, Slightam C, Kim S, Murray J, Waterston R, Gerstein M, Niu W, Janette J, Raha D, Agarwal A, Reinke V, Sarov M, Hyman A. 2011a. Identification of Transcription Factor SKN-1::GFP Binding Regions in L1. modMine modENCODE_2622. http://intermine.modencode.org/release-33/report.do?id=77000137.
118. Zhong M, Snyder M, Slightam C, Kim S, Murray J, Waterston R, Gerstein M, Niu W, Janette J, Raha D, Agarwal A, Reinke V, Sarov M, Hyman A. 2011b. Identification of Transcription Factor SKN-1::GFP Binding Regions in L1. NCBI Gene Expression Omnibus GSE25810. http://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE25810.
119. Zhong M, Snyder M, Slightam C, Kim S, Murray J, Waterston R, Gerstein M, Niu W, Janette J, Raha D, Agarwal A, Reinke V, Sarov M, Hyman A. 2013a. Identification of Transcription Factor SKN-1::GFP Binding Regions in L2. modMine mod ENCODE_3369. http://intermine.modencode.org/release-33/report.do?id=77000379.
120. Zhong M, Snyder M, Slightam C, Kim S, Murray J, Waterston R, Gerstein M, Niu W, Janette J, Raha D, Agarwal A, Reinke V, Sarov M, Hyman A. 2013b. Identification of Transcription Factor SKN-1::GFP Binding Regions in L3. modMine modENCODE_3838. http://intermine.modencode.org/release-33/report.do?id=77000500.
121. Zhong M, Snyder M, Slightam C, Kim S, Murray J, Waterston R, Gerstein M, Niu W, Janette J, Raha D, Agarwal A, Reinke V, Sarov M, Hyman A. 2013c. Identification of Transcription Factor SKN-1::GFP Binding Regions in L4. modMine modENCODE_4631. http://intermine.modencode.org/release-33/report.do?id=77000600.
122. Zhong M, Snyder M, Slightam C, Kim S, Murray J, Waterston R, Gerstein M, Niu W, Janette J, Raha D, Agarwal A, Reinke V, Sarov M, Hyman A. 2013d. Identification of Transcription Factor SKN-1::GFP Binding Regions in L3. NCBI Gene Expression Omnibus GSE48710. http://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE48710.
123. Zhong M, Snyder M, Slightam C, Kim S, Murray J, Waterston R, Gerstein M, Niu W, Janette J, Raha D, Agarwal A, Reinke V, Sarov M, Hyman A. 2013e. Snyder_SKN-1_GFP_L4. NCBI Gene Expression Omnibus GSE46772. http:// www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE46772.
124. Zhu LJ, Gazin C, Lawson ND, Pages H, Lin SM, Lapointe DS, Green MR. 2010. ChIPpeakAnno: a Bioconductor package to annotate ChIP-seq and ChIP-chip data. BMC Bioinformatics 11:237. doi: 10.1186/1471-2105-11-237.