Unexpected role for dosage compensation in the control of dauer arrest, insulin-like signaling, and foxo transcription factor activity in Caenorhabditis elegans

Genetics

Volumn 194, Issue 3, 2013, Pages 619-629

  Dumas, Kathleen J ^a   Delaney, Colin E ^a   Flibotte, Stephane ^d   Moerman, Donald G ^d   Csankovszki, Gyorgyi ^c   Hu, Patrick J ^a,b  

^a Life Sciences Institute   (United States)

^b Departments of Cell and Developmental Biology   (United States)

^c UNIVERSITY OF MICHIGAN   (United States)

^d UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR FOXO;

ARTICLE; CAENORHABDITIS ELEGANS; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE MUTATION; HERMAPHRODITISM; INSULIN LIKE ACTIVITY; MUTANT; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REGULATOR GENE;

ANIMALIA; CAENORHABDITIS ELEGANS;

EID: 84879774283     PISSN: 00166731     EISSN: 19432631     Source Type: Journal    
DOI: 10.1534/genetics.113.149948     Document Type: Article

References (63)

1. Ailion, M., and J. H. Thomas, 2003 Isolation and characterization of high-temperature-induced Dauer formation mutants in Cae-norhabditis elegans. Genetics 165: 127-144.
2. Alam, H., T. W. Williams, K. J. Dumas, C. Guo, S. Yoshina et al., 2010 EAK-7 controls development and life span by regulating nuclear DAF-16/FoxO activity. Cell Metab. 12: 30-41.
3. Antebi, A., W. H. Yeh, D. Tait, E. M. Hedgecock, and D. L. Riddle, 2000 daf-12 encodes a nuclear receptor that regulates the da-uer diapause and developmental age in C. elegans. Genes Dev. 14: 1512-1527.
4. Chen, X., R. McClusky, J. Chen, S. W. Beaven, P. Tontonoz et al., 2012 The number of X chromosomes causes sex differences in adiposity in mice. PLoS Genet. 8: e1002709.
5. Da Graca, L. S., K. K. Zimmerman, M. C. Mitchell, M. Kozhan-Gorodetska, K. Sekiewicz et al., 2004 DAF-5 is a Ski oncopro-tein homolog that functions in a neuronal TGF-beta pathway to regulate C. elegans dauer development. Development 131: 435-446.
6. Davis, M. W., M. Hammarlund, T. Harrach, P. Hullett, S. Olsen et al., 2005 Rapid single nucleotide polymorphism mapping in C. elegans. BMC Genomics 6: 118.
7. Dawes, H. E., D. S. Berlin, D. M. Lapidus, C. Nusbaum, T. L. Davis et al., 1999 Dosage compensation proteins targeted to X chro-mosomes by a determinant of hermaphrodite fate. Science 284: 1800-1804.
8. De Stasio, E. A., and S. Dorman, 2001 Optimization of ENU mu-tagenesis of Caenorhabditis elegans. Mutat. Res. 495: 81-88.
9. Dumas, K. J., C. Guo, X. Wang, K. B. Burkhart, E. J. Adams et al., 2010 Functional divergence of dafachronic acid pathways in the control of C. elegans development and lifespan. Dev. Biol. 340: 605-612.
10. Estevez, M., L. Attisano, J. L. Wrana, P. S. Albert, J. Massague et al., 1993 The daf-4 gene encodes a bone morphogenetic protein receptor controlling C. elegans dauer larva development. Nature 365: 644-649.
11. Fielenbach, N., and A. Antebi, 2008 C. elegans dauer formation and the molecular basis of plasticity. Genes Dev. 22: 2149-2165.
12. Gentilini, D., D. Castaldi, D. Mari, D. Monti, C. Franceschi et al., 2012 Age-dependent skewing of X chromosome inactivation ap-pears delayed in centenarians' offspring: Is there a role for allelic imbalance in healthy aging and longevity? Aging Cell 11: 277-283.
13. Georgi, L. L., P. S. Albert, and D. L. Riddle, 1990 daf-1, a C. elegans gene controlling dauer larva development, encodes a novel receptor protein kinase. Cell 61: 635-645.
14. Gerisch, B., and A. Antebi, 2004 Hormonal signals produced by DAF-9/cytochrome P450 regulate C. elegans dauer diapause in response to environmental cues. Development 131: 1765-1776.
15. Gerisch, B., C. Weitzel, C. Kober-Eisermann, V. Rottiers, and A. Antebi, 2001 A hormonal signaling pathway influencing C. elegans metabolism, reproductive development, and life span. Dev. Cell 1: 841-851.
16. Gottlieb, S., and G. Ruvkun, 1994 daf-2, daf-16 and daf-23: ge-netically interacting genes controlling Dauer formation in Cae-norhabditis elegans. Genetics 137: 107-120.
17. Henderson, S. T., and T. E. Johnson, 2001 daf-16 integrates de-velopmental and environmental inputs to mediate aging in the nematode Caenorhabditis elegans. Curr. Biol. 11: 1975-1980.
18. Hertweck, M., C. Gobel, and R. Baumeister, 2004 C. elegans SGK-1 is the critical component in the Akt/PKB kinase complex to control stress response and life span. Dev. Cell 6: 577-588.
19. Hu, P. J., J. Xu, and G. Ruvkun, 2006 Two membrane-associated tyrosine phosphatase homologs potentiate C. elegans AKT-1/ PKB signaling. PLoS Genet. 2: e99.
20. Inoue, T., and J. H. Thomas, 2000 Targets of TGF-beta signaling in Caenorhabditis elegans dauer formation. Dev. Biol. 217: 192-204.
21. Jans, J., J. M. Gladden, E. J. Ralston, C. S. Pickle, A. H. Michel et al., 2009 A condensin-like dosage compensation complex acts at a distance to control expression throughout the genome. Genes Dev. 23: 602-618.
22. Jia, K., P. S. Albert, and D. L. Riddle, 2002 DAF-9, a cytochrome P450 regulating C. elegans larval development and adult longev-ity. Development 129: 221-231.
23. Kamath, R. S., M. Martinez-Campos, P. Zipperlen, A. G. Fraser, and J. Ahringer, 2001 Effectiveness of specific RNA-mediated in-terference through ingested double-stranded RNA in Caeno-rhabditis elegans. Genome Biol. 2: 1-10.
24. Kenyon, C. J., 2010 The genetics of ageing. Nature 464: 504-512.
25. Kimura, K. D., H. A. Tissenbaum, Y. Liu, and G. Ruvkun, 1997 daf-2, an insulin receptor-like gene that regulates longevity and diapause in Caenorhabditis elegans. Science 277: 942-946.
26. Larsen, P. L., P. S. Albert, and D. L. Riddle, 1995 Genes that regulate both development and longevity in Caenorhabditis ele-gans. Genetics 139: 1567-1583.
27. Li, H., and R. Durbin, 2009 Fast and accurate short read align-ment with Burrows-Wheeler transform. Bioinformatics 25: 1754-1760.
28. Lin, K., J. B. Dorman, A. Rodan, and C. Kenyon, 1997 daf-16: an HNF-3/forkhead family member that can function to double the life-span of Caenorhabditis elegans. Science 278: 1319-1322.
29. Lin, K., H. Hsin, N. Libina, and C. Kenyon, 2001 Regulation of the Caenorhabditis elegans longevity protein DAF-16 by insulin/IGF-1 and germline signaling. Nat. Genet. 28: 139-145.
30. Li, J., G. Brown, M. Ailion, S. Lee, and J. H. Thomas, 2004 NCR-1 and NCR-2, the C. elegans homologs of the human Niemann-Pick type C1 disease protein, function upstream of DAF-9 in the dauer formation pathways. Development 131: 5741-5752.
31. Li, J., M. Tewari, M. Vidal, and S. S. Lee, 2007 The 14-3-3 protein FTT-2 regulates DAF-16 in Caenorhabditis elegans. Dev. Biol. 301: 82-91.
32. Li, H., B. Handsaker, A. Wysoker, T. Fennell, J. Ruan et al., 2009 The sequence alignment/map format and SAMtools. Bi-oinformatics 25: 2078-2079.
33. Mak, H. Y., and G. Ruvkun, 2004 Intercellular signaling of repro-ductive development by the C. elegans DAF-9 cytochrome P450. Development 131: 1777-1786.
34. Meyer, B. J., 2010 Targeting X chromosomes for repression. Curr. Opin. Genet. Dev. 20: 179-189.
35. Meyer, B. J., and L. P. Casson, 1986 Caenorhabditis elegans com-pensates for the difference in X chromosome dosage between the sexes by regulating transcript levels. Cell 47: 871-881.
36. Morris, J. Z., H. A. Tissenbaum, and G. Ruvkun, 1996 A phospha-tidylinositol-3-OH kinase family member regulating longevity and diapause in Caenorhabditis elegans. Nature 382: 536-539.
37. Motola, D. L., C. L. Cummins, V. Rottiers, K. K. Sharma, T. Li et al., 2006 Identification of ligands for DAF-12 that govern dauer formation and reproduction in C. elegans. Cell 124: 1209-1223.
38. Murphy, C. T., S. A. McCarroll, C. I. Bargmann, A. Fraser, R. S. Kamath et al., 2003 Genes that act downstream of DAF-16 to influence the lifespan of Caenorhabditis elegans. Nature 424: 277-283.
39. Nolan, T., R. E. Hands, and S. A. Bustin, 2006 Quantification of mRNA using real-time RT-PCR. Nat. Protoc. 1: 1559-1582.
40. Nusbaum, C., and B. J. Meyer, 1989 The Caenorhabditis elegans gene sdc-2 controls sex determination and dosage compensation in XX animals. Genetics 122: 579-593.
41. Oh, S. W., A. Mukhopadhyay, B. L. Dixit, T. Raha, M. R. Green et al., 2006 Identification of direct DAF-16 targets controlling lon-gevity, metabolism and diapause by chromatin immunoprecipi-tation. Nat. Genet. 38: 251-257.
42. Paradis, S., and G. Ruvkun, 1998 Caenorhabditis elegans Akt/PKB transduces insulin receptor-like signals from AGE-1 PI3 kinase to the DAF-16 transcription factor. Genes Dev. 12: 2488-2498.
43. Paradis, S., M. Ailion, A. Toker, J. H. Thomas, and G. Ruvkun, 1999 A PDK1 homolog is necessary and sufficient to transducer AGE-1 PI3 kinase signals that regulate diapause in Caenorhab-ditis elegans. Genes Dev. 13: 1438-1452.
44. Park, D., A. Estevez, and D. L. Riddle, 2010 Antagonistic Smad transcription factors control the dauer/non-dauer switch in C. elegans. Development 137: 477-485.
45. Patterson, G. I., A. Koweek, A. Wong, Y. Liu, and G. Ruvkun, 1997 The DAF-3 Smad protein antagonizes TGF-beta-related receptor signaling in the Caenorhabditis elegans dauer pathway. Genes Dev. 11: 2679-2690.
46. Plenefisch, J. D., L. DeLong, and B. J. Meyer, 1989 Genes that implement the hermaphrodite mode of dosage compensation in Caenorhabditis elegans. Genetics 121: 57-76.
47. Ren, P., C. S. Lim, R. Johnsen, P. S. Albert, D. Pilgrim et al., 1996 Control of C. elegans larval development by neuronal expression of a TGF-beta homolog. Science 274: 1389-1391.
48. Riddle, D. L., 1988 The dauer larva, pp. 393-412 in The Nematode Caenorhabditis elegans, edited by W. B. Wood. Cold Spring Har-bor Laboratory Press, Plainview, NY.
49. Riddle, D. L., M. M. Swanson, and P. S. Albert, 1981 Interacting genes in nematode dauer larva formation. Nature 290: 668-671.
50. Rottiers, V., D. L. Motola, B. Gerisch, C. L. Cummins, K. Nishiwaki et al., 2006 Hormonal control of C. elegans dauer formation and life span by a Rieske-like oxygenase. Dev. Cell 10: 473-482.
51. Sharma, K. K., Z. Wang, D. L. Motola, C. L. Cummins, D. J. Mangelsdorf et al., 2009 Synthesis and activity of dafachronic acid ligands for the C. elegans DAF-12 nuclear hormone receptor. Mol. Endocrinol. 23: 640-648.
52. Tewari, M., P. J. Hu, J. S. Ahn, N. Ayivi-Guedehoussou, P. O. Vidalain et al., 2004 Systematic interactome mapping and genetic per-turbation analysis of a C. elegans TGF-beta signaling network. Mol. Cell 13: 469-482.
53. Tsai, W. C., N. Bhattacharyya, L. Y. Han, J. A. Hanover, and M. M. Rechler, 2003 Insulin inhibition of transcription stimulated by the forkhead protein Foxo1 is not solely due to nuclear exclu-sion. Endocrinology 144: 5615-5622.
54. Tsai, C. J., D. G. Mets, M. R. Albrecht, P. Nix, A. Chan et al., 2008 Meiotic crossover number and distribution are regulated by a dosage compensation protein that resembles a condensing subunit. Genes Dev. 22: 194-211.
55. Vowels, J. J., and J. H. Thomas, 1992 Genetic analysis of chemo-sensory control of dauer formation in Caenorhabditis elegans. Genetics 130: 105-123.
56. Wicks, S. R., R. T. Yeh, W. R. Gish, R. H. Waterston, and R. H. Plasterk, 2001 Rapid gene mapping in Caenorhabditis elegans using a high density polymorphism map. Nat. Genet. 28: 160-164.
57. Williams, T. W., K. J. Dumas, and P. J. Hu, 2010 EAK proteins: novel conserved regulators of C. elegans lifespan. Aging 2: 742-747.
58. Wolkow, C. A., M. J. Munoz, D. L. Riddle, and G. Ruvkun, 2002 Insulin receptor substrate and p55 orthologous adaptor proteins function in the Caenorhabditis elegans daf-2/insulin-like signaling pathway. J. Biol. Chem. 277: 49591-49597.
59. Wollam, J., L. Magomedova, D. B. Magner, Y. Shen, V. Rottiers et al., 2011 The Rieske oxygenase DAF-36 functions as a cho-lesterol 7-desaturase in steroidogenic pathways governing lon-gevity. Aging Cell 10: 879-884.
60. Wollam, J., D. B. Magner, L. Magomedova, E. Rass, Y. Shen et al., 2012 A novel 3-hydroxysteroid dehydrogenase that regu-lates reproductive development and longevity. PLoS Biol. 10: e1001305.
61. Yabe, T., N. Suzuki, T. Furukawa, T. Ishihara, and I. Katsura, 2005 Multidrug resistance-associated protein MRP-1 regulates dauer diapause by its export activity in Caenorhabditis elegans. Development 132: 3197-3207.
62. Yonker, S. A., and B. J. Meyer, 2003 Recruitment of C. elegans dosage compensation proteins for gene-specific vs. chromo-some-wide repression. Development 130: 6519-6532.
63. Zhang, Y., J. Xu, C. Puscau, Y. Kim, X. Wang et al., 2008 Caenorhabditis elegans EAK-3 inhibits dauer arrest via nonautonomous regula-tion of nuclear DAF-16/FoxO activity. Dev. Biol. 315: 290-302.