The Nuclear Receptor DAF-12 Regulates Nutrient Metabolism and Reproductive Growth in Nematodes

PLoS Genetics

Volumn 11, Issue 3, 2015, Pages

  Wang, Zhu ^a   Stoltzfus, Jonathan ^b   You, Young jai ^c   Ranjit, Najju ^b   Tang, Hao ^c   Xie, Yang ^c   Lok, James B ^b   Mangelsdorf, David J ^a,c   Kliewer, Steven A ^a,c  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DAF 12 PROTEIN; REGULATOR PROTEIN; TRANSCRIPTOME; UNCLASSIFIED DRUG; CAENORHABDITIS ELEGANS PROTEIN; CELL RECEPTOR; DAF-12 PROTEIN, C ELEGANS; FATTY ACID; HELMINTH PROTEIN;

ADAPTATION; AEROBIC METABOLISM; ARTICLE; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; DAF 12 GENE; DEVELOPMENTAL GENE; ENERGY METABOLISM; FATTY ACID METABOLISM; GENE ACTIVATION; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENE TARGETING; GENETIC CODE; LARVAL STAGE; METABOLIC REGULATION; MOLECULAR DYNAMICS; NONHUMAN; NUTRIENT; PROTEIN EXPRESSION; REGULATOR GENE; REPRODUCTIVE BEHAVIOR; STRONGYLOIDES STERCORALIS; ANIMAL; GROWTH, DEVELOPMENT AND AGING; METABOLISM;

CAENORHABDITIS ELEGANS; NEMATODA; STRONGYLOIDES STERCORALIS;

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; FATTY ACIDS; HELMINTH PROTEINS; RECEPTORS, CYTOPLASMIC AND NUCLEAR; STRONGYLOIDES STERCORALIS;

EID: 84926216351     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1005027     Document Type: Article

References (46)

1. Wang J, Kim SK, (2003) Global analysis of dauer gene expression in Caenorhabditis elegans. Development 130: 1621–1634. 12620986
2. Riddle DL, Albert PS, Riddle DL, Blumenthal T, Meyer BJ, Priess JR, (1997) Genetic and Environmental Regulation of Dauer Larva Development. In: C. ELEGANS II. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press pp. 739–768.
3. Hotez PJ, Brooker S, Bethony JM, Bottazzi ME, Loukas A, Xiao S, (2004) Hookworm infection. N Engl J Med 351: 799–807. 15317893
4. Viney ME, Lok JB. Strongyloides spp. (May 23, 2007), WormBook, ed. The C. elegans Research Community, doi/10.1895/wormbook.1.141.1.
5. Motola DL, Cummins CL, Rottiers V, Sharma KK, Li T, Li Y, et al. (2006) Identification of ligands for DAF-12 that govern dauer formation and reproduction in C. elegans. Cell 124: 1209–1223. 16529801
6. Sharma KK, Wang Z, Motola DL, Cummins CL, Mangelsdorf DJ, Auchus RJ, (2009) Synthesis and activity of dafachronic acid ligands for the C. elegans DAF-12 nuclear hormone receptor. Mol Endocrinol 23: 640–648. doi: 10.1210/me.2008-0415 19196833
7. Mahanti P, Bose N, Bethke A, Judkins JC, Wollam J, Dumas KJ, et al. (2014) Comparative metabolomics reveals endogenous ligands of DAF-12, a nuclear hormone receptor, regulating C. elegans development and lifespan. Cell Metab 19: 73–83. doi: 10.1016/j.cmet.2013.11.024 24411940
8. Ludewig AH, Kober-Eisermann C, Weitzel C, Bethke A, Neubert K, Gerisch B, et al. (2004) A novel nuclear receptor/coregulator complex controls C. elegans lipid metabolism, larval development, and aging. Genes Dev 18: 2120–2133. 15314028
9. Antebi A, Yeh WH, Tait D, Hedgecock EM, Riddle DL, (2000) daf-12 encodes a nuclear receptor that regulates the dauer diapause and developmental age in C. elegans. Genes Dev 14: 1512–1527. 10859169
10. Brand A, Hawdon JM, (2004) Phosphoinositide-3-OH-kinase inhibitor LY294002 prevents activation of Ancylostoma caninum and Ancylostoma ceylanicum third-stage infective larvae. Int J Parasitol 34: 909–914. 15217729
11. Castelletto ML, Massey HC, Jr.Lok JB, (2009) Morphogenesis of Strongyloides stercoralis infective larvae requires the DAF-16 ortholog FKTF-1. PLoS Pathog 5: e1000370. doi: 10.1371/journal.ppat.1000370 19360119
12. Ogawa A, Streit A, Antebi A, Sommer RJ, (2009) A conserved endocrine mechanism controls the formation of dauer and infective larvae in nematodes. Curr Biol 19: 67–71. doi: 10.1016/j.cub.2008.11.063 19110431
13. Stoltzfus JD, Massey HC, Jr.Nolan TJ, Griffith SD, Lok JB, (2012) Strongyloides stercoralis age-1: a potential regulator of infective larval development in a parasitic nematode. PLoS One 7: e38587. doi: 10.1371/journal.pone.0038587 22701676
14. Tissenbaum HA, Hawdon J, Perregaux M, Hotez P, Guarente L, Ruvkun G, (2000) A common muscarinic pathway for diapause recovery in the distantly related nematode species Caenorhabditis elegans and Ancylostoma caninum. Proc Natl Acad Sci U S A 97: 460–465. 10618440
15. Wang Z, Zhou XE, Motola DL, Gao X, Suino-Powell K, Conneely A, et al. (2009) Identification of the nuclear receptor DAF-12 as a therapeutic target in parasitic nematodes. Proc Natl Acad Sci U S A 106: 9138–9143. doi: 10.1073/pnas.0904064106 19497877
16. Braeckman BP, Houthoofd K, Vanfleteren JR. Intermediary metabolism (February 16, 2009), WormBook, ed. The C. elegans Research Community, doi/10.1895/wormbook.1.146.1.
17. Burnell AM, Houthoofd K, O'Hanlon K, Vanfleteren JR, (2005) Alternate metabolism during the dauer stage of the nematode Caenorhabditis elegans. Exp Gerontol 40: 850–856. 16221538
18. Liu F, Thatcher JD, Epstein HF, (1997) Induction of glyoxylate cycle expression in Caenorhabditis elegans: a fasting response throughout larval development. Biochemistry 36: 255–260. 8993341
19. Van Gilst MR, Hadjivassiliou H, Jolly A, Yamamoto KR, (2005) Nuclear hormone receptor NHR-49 controls fat consumption and fatty acid composition in C. elegans. PLoS Biol 3: e53. 15719061
20. Van Gilst MR, Hadjivassiliou H, Yamamoto KR, (2005) A Caenorhabditis elegans nutrient response system partially dependent on nuclear receptor NHR-49. Proc Natl Acad Sci U S A 102: 13496–13501. 16157872
21. Van Voorhies WA, (2002) The influence of metabolic rate on longevity in the nematode Caenorhabditis elegans. Aging Cell 1: 91–101. 12882338
22. Narbonne P, Roy R, (2009) Caenorhabditis elegans dauers need LKB1/AMPK to ration lipid reserves and ensure long-term survival. Nature 457: 210–214. doi: 10.1038/nature07536 19052547
23. Clark FE, (1969) Ancylostoma caninum: food reserves and changes in chemical composition with age in third stage larvae. Exp Parasitol 24: 1–8. 5774099
24. Costello LC, Grollman S, (1958) Oxygen requirements of Strongyloides papillosus infective larvae. Exp Parasitol 7: 319–327. 13537941
25. Bethke A, Fielenbach N, Wang Z, Mangelsdorf DJ, Antebi A, (2009) Nuclear hormone receptor regulation of microRNAs controls developmental progression. Science 324: 95–98. doi: 10.1126/science.1164899 19342589
26. Fielenbach N, Guardavaccaro D, Neubert K, Chan T, Li D, Feng Q, et al. (2007) DRE-1: an evolutionarily conserved F box protein that regulates C. elegans developmental age. Dev Cell 12: 443–455. 17336909
27. Hochbaum D, Zhang Y, Stuckenholz C, Labhart P, Alexiadis V, Martin R, et al. (2011) DAF-12 regulates a connected network of genes to ensure robust developmental decisions. PLoS Genet 7: e1002179. doi: 10.1371/journal.pgen.1002179 21814518
28. Hammell CM, Karp X, Ambros V, (2009) A feedback circuit involving let-7-family miRNAs and DAF-12 integrates environmental signals and developmental timing in Caenorhabditis elegans. Proc Natl Acad Sci U S A 106: 18668–18673. doi: 10.1073/pnas.0908131106 19828440
29. Fisher AL, Lithgow GJ, (2006) The nuclear hormone receptor DAF-12 has opposing effects on Caenorhabditis elegans lifespan and regulates genes repressed in multiple long-lived worms. Aging Cell 5: 127–138. 16626392
30. 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 22081913
31. 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 23239738
32. Schedl T, Riddle DL, Blumenthal T, Meyer BJ, Priess JR, (1997) Developmental Genetics of the Germ Line. In: C. ELEGANS II. 2nd ed. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press. pp. 241–269.
33. Huang DW, Sherman BT, Lempicki RA, (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4: 44–57. doi: 10.1038/nprot.2008.211 19131956
34. Tepper RG, Ashraf J, Kaletsky R, Kleemann G, Murphy CT, Bussemaker HJ, (2013) PQM-1 complements DAF-16 as a key transcriptional regulator of DAF-2-mediated development and longevity. Cell 154: 676–690. doi: 10.1016/j.cell.2013.07.006 23911329
35. Hannich JT, Entchev EV, Mende F, Boytchev H, Martin R, Zagoriy V, et al. (2009) Methylation of the sterol nucleus by STRM-1 regulates dauer larva formation in Caenorhabditis elegans. Dev Cell 16: 833–843. doi: 10.1016/j.devcel.2009.04.012 19531354
36. Shostak Y, Van Gilst MR, Antebi A, Yamamoto KR, (2004) Identification of C. elegans DAF-12-binding sites, response elements, and target genes. Genes Dev 18: 2529–2544. 15489294
37. Shi Y, Burn P, (2004) Lipid metabolic enzymes: emerging drug targets for the treatment of obesity. Nat Rev Drug Discov 3: 695–710. 15286736
38. Murphy CT, McCarroll SA, Bargmann CI, Fraser A, Kamath RS, Ahringer J, et al. (2003) Genes that act downstream of DAF-16 to influence the lifespan of Caenorhabditis elegans. Nature 424: 277–283. 12845331
39. O'Rourke EJ, Soukas AA, Carr CE, Ruvkun G, (2009) C. elegans major fats are stored in vesicles distinct from lysosome-related organelles. Cell Metab 10: 430–435. doi: 10.1016/j.cmet.2009.10.002 19883620
40. Angelo G, Van Gilst MR, (2009) Starvation protects germline stem cells and extends reproductive longevity in C. elegans. Science 326: 954–958. doi: 10.1126/science.1178343 19713489
41. Taylor CM, Wang Q, Rosa BA, Huang SC, Powell K, Schedl T, et al. (2013) Discovery of anthelmintic drug targets and drugs using chokepoints in nematode metabolic pathways. PLoS Pathog 9: e1003505. doi: 10.1371/journal.ppat.1003505 23935495
42. Huang SC, Freitas TC, Amiel E, Everts B, Pearce EL, Lok JB, et al. (2012) Fatty acid oxidation is essential for egg production by the parasitic flatworm Schistosoma mansoni. PLoS Pathog 8: e1002996. doi: 10.1371/journal.ppat.1002996 23133378
43. Stoltzfus JD, Minot S, Berriman M, Nolan TJ, Lok JB, (2012) RNAseq analysis of the parasitic nematode Strongyloides stercoralis reveals divergent regulation of canonical dauer pathways. PLoS Negl Trop Dis 6: e1854. doi: 10.1371/journal.pntd.0001854 23145190
44. Elle IC, Rodkaer SV, Fredens J, Faergeman NJ, (2012) A method for measuring fatty acid oxidation in C. elegans. Worm 1: 26–30. doi: 10.4161/worm.19564 24058820
45. Raizen D, Song BM, Trojanowski N, You YJ. Methods for measuring pharyngeal behaviors WormBook, ed. The C. elegans Research Community, doi/10.1895/wormbook.1.154.1.
46. Tibshirani R, Chu G, Narasimhan B, Li J (2011) samr: SAM: Significance Analysis of Microarrays. R package version 2.0. http://CRANR-projectorg/package=samr.