C. Elegans AMPKs promote survival and arrest germline development during nutrient stress

Biology Open

Volumn 1, Issue 10, 2012, Pages 929-936

  Fukuyama, Masamitsu ^a,b   Sakuma, Kensuke ^a   Park, Riyong ^a   Kasuga, Hidefumi ^a   Nagaya, Ryotaro ^a   Atsumi, Yuriko ^a   Shimomura, Yumi ^a   Takahashi, Shinya ^a   Kajiho, Hiroaki ^a   Rougvie, Ann ^b   Kontani, Kenji ^a   Katada, Toshiaki ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b UNIVERSITY OF MINNESOTA   (United States)

Author keywords

AMPK; Diapause; Stem cell

Indexed keywords

EID: 84964892932     PISSN: None     EISSN: 20466390     Source Type: Journal    
DOI: 10.1242/bio.2012836     Document Type: Article

References (75)

1. Angelo, G. and Van Gilst, M. R. (2009). Starvation protects germline stem cells and extends reproductive longevity in C. Elegans. Science 326, 954-958.
2. Apfeld, J., O'Connor, G., McDonagh, T., DiStefano, P. S. and Curtis, R. (2004). The AMP-activated protein kinase AAK-2 links energy levels and insulin-like signals to lifespan in C. Elegans. Genes Dev. 18, 3004-3009.
3. Baugh, L. R. and Sternberg, P. W. (2006). DAF-16/FOXO regulates transcription of cki-1/Cip/Kip and repression of lin-4 during C. Elegans L1 arrest. Curr. Biol. 16, 780-785.
4. Behrends, C., Sowa, M. E., Gygi, S. P. and Harper, J. W. (2010). Network organization of the human autophagy system. Nature 466, 68-76.
5. Braeckman, B. P., Houthoofd, K. and Vanfleteren, J. R. (2009). Intermediary metabolism. In Worm Book (ed. The C. Elegans Research Community), 1-24.
6. Brenner, S. (1974). The genetics of Caenorhabditis elegans. Genetics 77, 71-94.
7. Brisbin, S., Liu, J., Boudreau, J., Peng, J., Evangelista, M. and Chin-Sang, I. (2009). A role for C. Elegans Eph RTK signaling in PTEN regulation. Dev. Cell 17, 459-469.
8. Castro, P. V., Khare, S., Young, B. D. and Clarke, S. G. (2012). Caenorhabditis elegans battling starvation stress: low levels of ethanol prolong lifespan in L1 larvae. PLoS ONE 7, e29984.
9. Egan, D. F., Shackelford, D. B., Mihaylova, M. M., Gelino, S., Kohnz, R. A., Mair, W., Vasquez, D. S., Joshi, A., Gwinn, D. M., Taylor, R. et al. (2011). Phosphorylation of ULK1 (hATG1) by AMP-activated protein kinase connects energy sensing to mitophagy. Science 331, 456-461.
10. Fay, D. S., Keenan, S. and Han, M. (2002). fzr-1 and lin-35/Rb function redundantly to control cell proliferation in C. Elegans as revealed by a nonbiased synthetic screen. Genes Dev. 16, 503-517.
11. Fukuyama, M., Rougvie, A. E. and Rothman, J. H. (2006). C. Elegans DAF-18/PTEN mediates nutrient-dependent arrest of cell cycle and growth in the germline. Curr. Biol. 16, 773-779.
12. Garami, A., Zwartkruis, F. J., Nobukuni, T., Joaquin, M., Roccio, M., Stocker, H., Kozma, S. C., Hafen, E., Bos, J. L. and Thomas, G. (2003). Insulin activation of Rheb, a mediator of mTOR/S6K/4E-BP signaling, is inhibited by TSC1 and 2. Mol. Cell 11, 1457-1466.
13. Gaur, S., Chen, L., Yang, L., Wu, X., Un, F. and Yen, Y. (2011). Inhibitors of mTOR overcome drug resistance from topoisomerase II inhibitors in solid tumors. Cancer Lett. 311, 20-28.
14. Greer, E. L., Dowlatshahi, D., Banko, M. R., Villen, J., Hoang, K., Blanchard, D., Gygi, S. P. and Brunet, A. (2007). An AMPK-FOXO pathway mediates longevity induced by a novel method of dietary restriction in C. Elegans. Curr. Biol. 17, 1646-1656.
15. Gwinn, D. M., Shackelford, D. B., Egan, D. F., Mihaylova, M. M., Mery, A., Vasquez, D. S., Turk, B. E. and Shaw, R. J. (2008). AMPK phosphorylation of raptor mediates a metabolic checkpoint. Mol. Cell 30, 214-226.
16. Hardie, D. G. (2011). AMP-activated protein kinase: an energy sensor that regulates all aspects of cell function. Genes Dev. 25, 1895-1908.
17. Hewes, R. S. and Taghert, P. H. (2001). Neuropeptides and neuropeptide receptors in the Drosophila melanogaster genome. Genome Res. 11, 1126-1142.
18. Imamura, K., Ogura, T., Kishimoto, A., Kaminishi, M. and Esumi, H. (2001). Cell cycle regulation via p53 phosphorylation by a 5′-AMP activated protein kinase activator, 5-aminoimidazole-4-carboxamide-1-beta-D-ribofuranoside, in a human hepatocellular carcinoma cell line. Biochem. Biophys. Res. Commun. 287, 562-567.
19. Inoki, K., Li, Y., Xu, T. and Guan, K. L. (2003a). Rheb GTPase is a direct target of TSC2 GAP activity and regulates mTOR signaling. Genes Dev. 17, 1829-1834.
20. Inoki, K., Zhu, T. and Guan, K. L. (2003b). TSC2 mediates cellular energy response to control cell growth and survival. Cell 115, 577-590.
21. Jia, K., Chen, D. and Riddle, D. L. (2004). The TOR pathway interacts with the insulin signaling pathway to regulate C. Elegans larval development, metabolism and life span. Development 131, 3897-3906.
22. Johnson, T. E., Mitchell, D. H., Kline, S., Kemal, R. and Foy, J. (1984). Arresting development arrests aging in the nematode Caenorhabditis elegans. Mech. Ageing Dev. 28, 23-40.
23. Jones, R. G., Plas, D. R., Kubek, S., Buzzai, M., Mu, J., Xu, Y., Birnbaum, M. J. and Thompson, C. B. (2005). AMP-activated protein kinase induces a p53-dependent metabolic checkpoint. Mol. Cell 18, 283-293.
24. Kahn, B. B., Alquier, T., Carling, D. and Hardie, D. G. (2005). AMP-activated protein kinase: ancient energy gauge provides clues to modern understanding of metabolism. Cell Metab. 1, 15-25.
25. Kamath, R. S., Fraser, A. G., Dong, Y., Poulin, G., Durbin, R., Gotta, M., Kanapin, A., Le Bot, N., Moreno, S., Sohrmann, M. et al. (2003). Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 421, 231-237.
26. Kapoor, V., Zaharieva, M. M., Das, S. N. and Berger, M. R. (2012). Erufosine simultaneously induces apoptosis and autophagy by modulating the Akt-mTOR signaling pathway in oral squamous cell carcinoma. Cancer Lett. 319, 39-48.
27. Kawasaki, I., Shim, Y. H., Kirchner, J., Kaminker, J., Wood, W. B. and Strome, S. (1998). PGL-1, a predicted RNA-binding component of germ granules, is essential for fertility in C. Elegans. Cell 94, 635-645.
28. Kim, E., Goraksha-Hicks, P., Li, L., Neufeld, T. P. and Guan, K. L. (2008). Regulation of TORC1 by Rag GTPases in nutrient response. Nat. Cell Biol. 10, 935-945.
29. Kim, J., Kundu, M., Viollet, B. and Guan, K. L. (2011). AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat. Cell Biol. 13, 132-141.
30. Kimble, J. and Hirsh, D. (1979). The postembryonic cell lineages of the hermaphrodite and male gonads in Caenorhabditis elegans. Dev. Biol. 70, 396-417.
31. Korta, D. Z., Tuck, S. and Hubbard, E. J. (2012). S6K links cell fate, cell cycle and nutrient response in C. Elegans germline stem/progenitor cells. Development 139, 859-870.
32. Kumsta, C. and Hansen, M. (2012). C. Elegans rrf-1 mutations maintain RNAi efficiency in the soma in addition to the germline. PLoS ONE 7, e35428.
33. LaFever, L., Feoktistov, A., Hsu, H. J. and Drummond-Barbosa, D. (2010). Specific roles of Target of rapamycin in the control of stem cells and their progeny in the Drosophila ovary. Development 137, 2117-2126.
34. Laplante, M. and Sabatini, D. M. (2012). mTOR signaling in growth control and disease. Cell 149, 274-293.
35. Lee, H., Cho, J. S., Lambacher, N., Lee, J., Lee, S. J., Lee, T. H., Gartner, A. and Koo, H. S. (2008). The Caenorhabditis elegans AMP-activated protein kinase AAK-2 is phosphorylated by LKB1 and is required for resistance to oxidative stress and for normal motility and foraging behavior. J. Biol. Chem. 283, 14988-14993.
36. Li, C., Nelson, L. S., Kim, K., Nathoo, A. and Hart, A. C. (1999). Neuropeptide gene families in the nematode Caenorhabditis elegans. Ann. N. Y. Acad. Sci. 897, 239-252.
37. Li, Y., Inoki, K. and Guan, K. L. (2004). Biochemical and functional characterizations of small GTPase Rheb and TSC2 GAP activity. Mol. Cell. Biol. 24, 7965-7975.
38. Liang, J., Shao, S. H., Xu, Z. X., Hennessy, B., Ding, Z., Larrea, M., Kondo, S., Dumont, D. J., Gutterman, J. U., Walker, C. L. et al. (2007). The energy sensing LKB1-AMPK pathway regulates p27(kip1) phosphorylation mediating the decision to enter autophagy or apoptosis. Nat. Cell Biol. 9, 218-224.
39. Long, X., Spycher, C., Han, Z. S., Rose, A. M., Müller, F. and Avruch, J. (2002). TOR deficiency in C. Elegans causes developmental arrest and intestinal atrophy by inhibition of mRNA translation. Curr. Biol. 12, 1448-1461.
40. Lu, N. C., Hugenberg, G., Briggs, G. M. and Stokstad, E. L. (1978). The growthpromoting activity of several lipid-related compounds in the free-living nematode Caenorhabditis briggsae. Proc. Soc. Exp. Biol. Med. 158, 187-191.
41. Maehama, T. and Dixon, J. E. (1998). The tumor suppressor, PTEN/MMAC1, dephosphorylates the lipid second messenger, phosphatidylinositol 3,4,5-trisphosphate. J. Biol. Chem. 273, 13375-13378.
42. Mello, C. C., Kramer, J. M., Stinchcomb, D. and Ambros, V. (1991). Efficient gene transfer in C. Elegans: extrachromosomal maintenance and integration of transforming sequences. EMBO J. 10, 3959-3970.
43. Mihaylova, V. T., Borland, C. Z., Manjarrez, L., Stern, M. J. and Sun, H. (1999). The PTEN tumor suppressor homolog in Caenorhabditis elegans regulates longevity and dauer formation in an insulin receptor-like signaling pathway. Proc. Natl. Acad. Sci. USA 96, 7427-7432.
44. Minokoshi, Y., Alquier, T., Furukawa, N., Kim, Y. B., Lee, A., Xue, B., Mu, J., Foufelle, F., Ferré, P., Birnbaum, M. J. et al. (2004). AMP-kinase regulates food intake by responding to hormonal and nutrient signals in the hypothalamus. Nature 428, 569-574.
45. Nakashima, A., Maruki, Y., Imamura, Y., Kondo, C., Kawamata, T., Kawanishi, I., Takata, H., Matsuura, A., Lee, K. S. and Kikkawa, U et al. (2008). The yeast Tor signaling pathway is involved in G2/M transition via polo-kinase. PLoS ONE 3, e2223.
46. Nakashima, N., Noguchi, E. and Nishimoto, T. (1999). Saccharomyces cerevisiae putative G protein, Gtr1p, which forms complexes with itself and a novel protein designated as Gtr2p, negatively regulates the Ran/Gsp1p G protein cycle through Gtr2p. Genetics 152, 853-867.
47. Narbonne, P. and Roy, R. (2006). Inhibition of germline proliferation during C. Elegans dauer development requires PTEN, LKB1 and AMPK signalling. Development 133, 611-619.
48. Narbonne, P. and Roy, R. (2009). Caenorhabditis elegans dauers need LKB1/AMPK to ration lipid reserves and ensure long-term survival. Nature 457, 210-214.
49. Neshat, M. S., Mellinghoff, I. K., Tran, C., Stiles, B., Thomas, G., Petersen, R., Frost, P., Gibbons, J. J., Wu, H. and Sawyers, C. L. (2001). Enhanced sensitivity of PTEN-deficient tumors to inhibition of FRAP/mTOR. Proc. Natl. Acad. Sci. USA 98, 10314-10319.
50. Nukazuka, A., Tamaki, S., Matsumoto, K., Oda, Y., Fujisawa, H. and Takagi, S. (2011). A shift of the TOR adaptor from Rictor towards Raptor by semaphorin in C. Elegans. Nat Commun 2, 484.
51. Ogg, S. and Ruvkun, G. (1998). The C. Elegans PTEN homolog, DAF-18, acts in the insulin receptor-like metabolic signaling pathway. Mol. Cell 2, 887-893.
52. Podsypanina, K., Lee, R. T., Politis, C., Hennessy, I., Crane, A., Puc, J., Neshat, M., Wang, H., Yang, L., Gibbons, J. et al. (2001). An inhibitor of mTOR reduces neoplasia and normalizes p70/S6 kinase activity in Pten+/- mice. Proc. Natl. Acad. Sci. USA 98, 10320-10325.
53. Reddy, P., Liu, L., Adhikari, D., Jagarlamudi, K., Rajareddy, S., Shen, Y., Du, C., Tang, W., Hämäläinen, T., Peng, S. L. et al. (2008). Oocyte-specific deletion of Pten causes premature activation of the primordial follicle pool. Science 319, 611-613.
54. Riddle, D. L. and Albert, P. S. (1997). Genetic and environmental regulation of dauer larva development. In C. Elegans II (ed. D. L. Riddle, T. Blumenthal, B. J. Meyer and J. R. Priess), 2nd edition, pp. 739-768. Plainview, NY: Cold Spring Harbor Laboratory Press.
55. Robida-Stubbs, S., Glover-Cutter, K., Lamming, D. W., Mizunuma, M., Narasimhan, S. D., Neumann-Haefelin, E., Sabatini, D. M. and Blackwell, T. K. (2012). TOR signaling and rapamycin influence longevity by regulating SKN-1/Nrf and DAF-16/FoxO. Cell Metab. 15, 713-724.
56. Russell, R. C., Fang, C. and Guan, K. L. (2011). An emerging role for TOR signaling in mammalian tissue and stem cell physiology. Development 138, 3343-3356.
57. Sancak, Y., Peterson, T. R., Shaul, Y. D., Lindquist, R. A., Thoreen, C. C., Bar-Peled, L. and Sabatini, D. M. (2008). The Rag GTPases bind raptor and mediate amino acid signaling to mTORC1. Science 320, 1496-1501.
58. Saucedo, L. J., Gao, X., Chiarelli, D. A., Li, L., Pan, D. and Edgar, B. A. (2003). Rheb promotes cell growth as a component of the insulin/TOR signalling network. Nat. Cell Biol. 5, 566-571.
59. Schreiber, M. A., Pierce-Shimomura, J. T., Chan, S., Parry, D. and McIntire, S. L. (2010). Manipulation of behavioral decline in Caenorhabditis elegans with the Rag GTPase raga-1. PLoS Genet. 6, e1000972.
60. Schulz, T. J., Zarse, K., Voigt, A., Urban, N., Birringer, M. and Ristow, M. (2007). Glucose restriction extends Caenorhabditis elegans life span by inducing mitochondrial respiration and increasing oxidative stress. Cell Metab. 6, 280-293.
61. Seidel, H. S. and Kimble, J. (2011). The oogenic germline starvation response in C. Elegans. PLoS ONE 6, e28074.
62. Sekiguchi, T., Hirose, E., Nakashima, N., Ii, M. and Nishimoto, T. (2001). Novel G proteins, Rag C and Rag D, interact with GTP-binding proteins, Rag A and Rag B. J. Biol. Chem. 276, 7246-7257.
63. Shackelford, D. B. and Shaw, R. J. (2009). The LKB1-AMPK pathway: metabolism and growth control in tumour suppression. Nat. Rev. Cancer 9, 563-575.
64. Sigmond, T., Barna, J., Tóth, M. L., Takács-Vellai, K., Pásti, G., Kovács, A. L. and Vellai, T. (2008). Autophagy in Caenorhabditis elegans. Methods Enzymol. 451, 521-540.
65. Sijen, T., Fleenor, J., Simmer, F., Thijssen, K. L., Parrish, S., Timmons, L., Plasterk, R. H. and Fire, A. (2001). On the role of RNA amplification in dsRNAtriggered gene silencing. Cell 107, 465-476.
66. Stocker, H., Radimerski, T., Schindelholz, B., Wittwer, F., Belawat, P., Daram, P., Breuer, S., Thomas, G. and Hafen, E. (2003). Rheb is an essential regulator of S6K in controlling cell growth in Drosophila. Nat. Cell Biol. 5, 559-566.
67. Tee, A. R., Manning, B. D., Roux, P. P., Cantley, L. C. and Blenis, J. (2003). Tuberous sclerosis complex gene products, Tuberin and Hamartin, control mTOR signaling by acting as a GTPase-activating protein complex toward Rheb. Curr. Biol. 13, 1259-1268.
68. Wang, Z., Wilson, W. A., Fujino, M. A. and Roach, P. J. (2001). Antagonistic controls of autophagy and glycogen accumulation by Snf1p, the yeast homolog of AMPactivated protein kinase, and the cyclin-dependent kinase Pho85p. Mol. Cell. Biol. 21, 5742-5752.
69. Watanabe, S., Yamamoto, T. G. and Kitagawa, R. (2008). Spindle assembly checkpoint gene mdf-1 regulates germ cell proliferation in response to nutrition signals in C. Elegans. EMBO J. 27, 1085-1096.
70. Wullschleger, S., Loewith, R. and Hall, M. N. (2006). TOR signaling in growth and metabolism. Cell 124, 471-484.
71. Yilmaz, O. H., Valdez, R., Theisen, B. K., Guo, W., Ferguson, D. O., Wu, H. and Morrison, S. J. (2006). Pten dependence distinguishes haematopoietic stem cells from leukaemia-initiating cells. Nature 441, 475-482.
72. Zhang, J., Grindley, J. C., Yin, T., Jayasinghe, S., He, X. C., Ross, J. T., Haug, J. S., Rupp, D., Porter-Westpfahl, K. S., Wiedemann, L. M. et al. (2006). PTEN maintains haematopoietic stem cells and acts in lineage choice and leukaemia prevention. Nature 441, 518-522.
73. Zhang, S. O., Box, A. C., Xu, N., Le Men, J., Yu, J., Guo, F., Trimble, R. and Mak, H. Y. (2010). Genetic and dietary regulation of lipid droplet expansion in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 107, 4640-4645.
74. Zoncu, R., Efeyan, A. and Sabatini, D. M. (2011). mTOR: from growth signal integration to cancer, diabetes and ageing. Nat. Rev. Mol. Cell Biol. 12, 21-35.
75. Zong, H., Ren, J. M., Young, L. H., Pypaert, M., Mu, J., Birnbaum, M. J. and Shulman, G. I. (2002). AMP kinase is required for mitochondrial biogenesis in skeletal muscle in response to chronic energy deprivation. Proc. Natl. Acad. Sci. USA 99, 15983-15987.