Advertisement

Nutritional Control of the Germline Development in Caenorhabditis elegans

  • Masamitsu Fukuyama
Chapter
Part of the Diversity and Commonality in Animals book series (DCA)

Abstract

Food is an ultimate regulator of animal reproduction. Because of its invariant cell lineage, ease of synchronized culture, and powerful genetics, the nematode Caenorhabditis elegans (C. elegans) has served as an excellent model system for delineating the genetic pathways that mediate the nutritional regulation of germline development. C. elegans possesses multiple nutritional checkpoints during post-embryonic development that temporally arrest developmental programs in the germline and somatic stem/progenitor cells. The insulin/insulin-like growth factor (IGF) signaling (IIS) pathway and other factors such as adenosine monophosphate (AMP)-activated kinase (AMPK) and mechanistic (or mammalian) Target of Rapamycin Complex 1 (mTORC1) constitute the signaling network dedicated to regulating developmental quiescence of the germline. Furthermore, additional nutrient-responsive pathways adjust the size of the germline stem/progenitor cell pool by altering the balance between self-renewal and differentiation, as well as the balance between cellular survival and death. These findings illustrate the molecular mechanisms that coordinate germline development with the dietary environment by altering the behavior of its stem/progenitor cells.

Keywords

Caenorhabditis elegans Germline Nutrition Insulin/insulin-like growth factor signaling pathway Quiescence Diapause 

Notes

Acknowledgement

I would like to thank the reviewers for their careful review of the manuscript and for their insightful, constructive suggestions for improving the manuscript.

References

  1. Albert PS, Riddle DL (1988) Mutants of Caenorhabditis elegans that form dauer-like larvae. Dev Biol 126:270–293.  https://doi.org/10.1016/0012-1606(88)90138-8 CrossRefPubMedGoogle Scholar
  2. Albert PS, Albert PS, Brown SJ, Brown SJ, Riddle DL, Riddle DL (1981) Sensory control of dauer larva formation in Caenorhabditis elegans. J Comp Neurol 198:435–451CrossRefPubMedGoogle Scholar
  3. Ambros V (1999) Cell cycle-dependent sequencing of cell fate decisions in Caenorhabditis elegans vulva precursor cells. Development 126:1947–1956PubMedGoogle Scholar
  4. Angelo G, Van Gilst MR (2009) Starvation protects germline stem cells and extends reproductive longevity in C. elegans. Science 326:954–958.  https://doi.org/10.1126/science.1178343 CrossRefPubMedGoogle Scholar
  5. Antebi A, Culotti JG, Hedgecock EM (1998) daf-12 regulates developmental age and the dauer alternative in Caenorhabditis elegans. Development 125:1191–1205PubMedGoogle Scholar
  6. Antebi A, Yeh WH, Tait D et al (2000) daf-12 encodes a nuclear receptor that regulates the dauer diapause and developmental age in C. elegans. Genes Dev 14:1512–1527PubMedPubMedCentralGoogle Scholar
  7. Apfeld J, Kenyon C (1998) Cell nonautonomy of C. elegans daf-2 function in the regulation of diapause and life span. Cell 95:199–210.  https://doi.org/10.1016/S0092-8674(00)81751-1 CrossRefPubMedGoogle Scholar
  8. Asaoka-Taguchi M, Yamada M, Nakamura A et al (1999) Maternal Pumilio acts together with Nanos in germline development in Drosophila embryos. Nat Cell Biol 1:431–437.  https://doi.org/10.1038/15666 CrossRefPubMedGoogle Scholar
  9. Austin J, Kimble J (1987) glp-1 Is required in the germ line for regulation of the decision between mitosis and meiosis in C. elegans. Cell 51:589–599.  https://doi.org/10.1016/0092-8674(87)90128-0 CrossRefPubMedGoogle Scholar
  10. Baugh LR (2013) To grow or not to grow: nutritional control of development during Caenorhabditis elegans L1 arrest. Genetics 194:539–555.  https://doi.org/10.1534/genetics.113.150847 CrossRefPubMedPubMedCentralGoogle Scholar
  11. Baugh LR, Sternberg PW (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.  https://doi.org/10.1016/j.cub.2006.03.021 CrossRefPubMedGoogle Scholar
  12. Berry LW, Westlund B, Schedl T (1997) Germ-line tumor formation caused by activation of glp-1, a Caenorhabditis elegans member of the Notch family of receptors. Development 124:925–936PubMedGoogle Scholar
  13. Biggs WH, Meisenhelder J, Hunter T et al (1999) Protein kinase B/Akt-mediated phosphorylation promotes nuclear exclusion of the winged helix transcription factor FKHR1. Proc Natl Acad Sci U S A 96:7421–7426CrossRefPubMedPubMedCentralGoogle Scholar
  14. Birnby DA, Link EM, Vowels JJ et al (2000) A transmembrane guanylyl cyclase (DAF-11) and Hsp90 (DAF-21) regulate a common set of chemosensory behaviors in Caenorhabditis elegans. Genetics 155:85–104.  https://doi.org/10.1006/jmbi.1990.9999 CrossRefPubMedPubMedCentralGoogle Scholar
  15. Brisbin S, Liu J, Boudreau J et al (2009) A role for C. elegans Eph RTK signaling in PTEN regulation. Dev Cell 17:459–469.  https://doi.org/10.1016/j.devcel.2009.08.009 CrossRefPubMedGoogle Scholar
  16. Bronson FH, Rissman EF (1986) The biology of puberty. Biol Rev Camb Philos Soc 61:157–195CrossRefPubMedGoogle Scholar
  17. Brunborg G, Williamson DH (1978) The relevance of the nuclear division cycle to radiosensitivity in yeast. Mol Gen Genet 162:277–286CrossRefPubMedGoogle Scholar
  18. Brunet A, Bonni A, Zigmond MJ et al (1999) Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96:857–868.  https://doi.org/10.1016/S0092-8674(00)80595-4 CrossRefPubMedGoogle Scholar
  19. Butcher RA, Fujita M, Schroeder FC, Clardy J (2007) Small-molecule pheromones that control dauer development in Caenorhabditis elegans. Nat Chem Biol 3:420–422.  https://doi.org/10.1038/nchembio.2007.3 CrossRefPubMedGoogle Scholar
  20. Butcher RA, Ragains JR, Kim E, Clardy J (2008) A potent dauer pheromone component in Caenorhabditis elegans that acts synergistically with other components. Proc Natl Acad Sci U S A 105:14288–14292.  https://doi.org/10.1073/pnas.0806676105 CrossRefPubMedPubMedCentralGoogle Scholar
  21. Butcher RA, Ragains JR, Clardy J (2009a) An indole-containing dauer pheromone component with unusual dauer inhibitory activity at higher concentrations. Org Lett 11:3100–3103.  https://doi.org/10.1021/ol901011c CrossRefPubMedPubMedCentralGoogle Scholar
  22. Butcher RA, Ragains JR, Li W et al (2009b) Biosynthesis of the Caenorhabditis elegans dauer pheromone. Proc Natl Acad Sci U S A 106:1875–1879.  https://doi.org/10.1073/pnas.0810338106 CrossRefPubMedPubMedCentralGoogle Scholar
  23. Cassada RC, Russell RL (1975) The dauerlarva, a post-embryonic developmental variant of the nematode Caenorhabditis elegans. Dev Biol 46:326–342CrossRefPubMedGoogle Scholar
  24. Castro PV, Khare S, Young BD, Clarke SG (2012) Caenorhabditis elegans battling starvation stress: low levels of ethanol prolong lifespan in L1 larvae. PLoS One 7:e29984.  https://doi.org/10.1371/journal.pone.0029984 CrossRefPubMedPubMedCentralGoogle Scholar
  25. Chell JM, Brand AH (2010) Nutrition-responsive glia control exit of neural stem cells from quiescence. Cell 143:1161–1173.  https://doi.org/10.1016/j.cell.2010.12.007 CrossRefPubMedPubMedCentralGoogle Scholar
  26. Chen Y, Baugh LR (2014) Ins-4 and daf-28 function redundantly to regulate C. elegans L1 arrest. Dev Biol 394:314–326.  https://doi.org/10.1016/j.ydbio.2014.08.002 CrossRefPubMedGoogle Scholar
  27. Cheung TH, Rando TA (2013) Molecular regulation of stem cell quiescence. Nat Rev Mol Cell Biol 14:329–340.  https://doi.org/10.1038/nrm3591 CrossRefPubMedGoogle Scholar
  28. Clejan I, Boerckel J, Ahmed S (2006) Developmental modulation of nonhomologous end joining in Caenorhabditis elegans. Genetics 173:1301–1317.  https://doi.org/10.1534/genetics.106.058628 CrossRefPubMedPubMedCentralGoogle Scholar
  29. Coburn CM, Bargmann CI (1996) A putative cyclic nucleotide-gated channel is required for sensory development and function in C. elegans. Neuron 17:695–706CrossRefPubMedGoogle Scholar
  30. Cornils A, Gloeck M, Chen Z et al (2011) Specific insulin-like peptides encode sensory information to regulate distinct developmental processes. Development 138:1183–1193.  https://doi.org/10.1242/dev.060905 CrossRefPubMedPubMedCentralGoogle Scholar
  31. Cox MM (2001) Historical overview: searching for replication help in all of the rec places. Proc Natl Acad Sci U S A 98:8173–8180.  https://doi.org/10.1073/pnas.131004998 CrossRefPubMedPubMedCentralGoogle Scholar
  32. da Graca LS, Zimmerman KK, Mitchell MC et al (2004) DAF-5 is a Ski oncoprotein homolog that functions in a neuronal TGF-β pathway to regulate C. elegans dauer development. Development 131:435–446.  https://doi.org/10.1242/dev.00922 CrossRefPubMedGoogle Scholar
  33. Dalfó D, Michaelson D, Hubbard EJA (2012) Sensory regulation of the C. elegans germline through TGF-β-dependent signaling in the niche. Curr Biol 22:712–719.  https://doi.org/10.1016/j.cub.2012.02.064 CrossRefPubMedPubMedCentralGoogle Scholar
  34. Duret L, Guex N, Peitsch MC, Bairoch A (1998) New insulin-like proteins with atypical disulfide bond pattern characterized in Caenorhabditis elegans by comparative sequence analysis and homology modeling. Genome Res 8:348–353.  https://doi.org/10.1101/gr.8.4.348 CrossRefPubMedGoogle Scholar
  35. Euling S, Ambros V (1996) Reversal of cell fate determination in Caenorhabditis elegans vulval development. Development 122:2507–2515PubMedGoogle Scholar
  36. Félix M-A, Duveau F (2012) Population dynamics and habitat sharing of natural populations of Caenorhabditis elegans and C. briggsae. BMC Biol 10:59.  https://doi.org/10.1186/1741-7007-10-59 CrossRefPubMedPubMedCentralGoogle Scholar
  37. Fernandes de Abreu DA, Caballero A, Fardel P et al (2014) An insulin-to-insulin regulatory network orchestrates phenotypic specificity in development and physiology. PLoS Genet 10:e1004225.  https://doi.org/10.1371/journal.pgen.1004225 CrossRefPubMedPubMedCentralGoogle Scholar
  38. Fielenbach N, Antebi A (2008) C. elegans dauer formation and the molecular basis of plasticity. Genes Dev 22:2149–2165.  https://doi.org/10.1101/gad.1701508 CrossRefPubMedPubMedCentralGoogle Scholar
  39. Fingar DC, Richardson CJ, Tee AR et al (2004) mTOR controls cell cycle progression through its cell growth effectors S6K1 and 4E-BP1/eukaryotic translation initiation factor 4E. Mol Cell Biol 24:200–216.  https://doi.org/10.1128/MCB.24.1.200-216.2004 CrossRefPubMedPubMedCentralGoogle Scholar
  40. Foley EA, Kapoor TM (2013) Microtubule attachment and spindle assembly checkpoint signalling at the kinetochore. Nat Rev Mol Cell Biol 14:25–37.  https://doi.org/10.1038/nrm3494 CrossRefPubMedPubMedCentralGoogle Scholar
  41. Frézal L, Félix M-A (2015) C. elegans outside the Petri dish. elife 4:e05849.  https://doi.org/10.7554/eLife.05849 CrossRefPubMedCentralGoogle Scholar
  42. Fukuyama M, Rougvie AE, Rothman JH (2006) C. elegans DAF-18/PTEN mediates nutrient-dependent arrest of cell cycle and growth in the germline. Curr Biol 16:773–779.  https://doi.org/10.1016/j.cub.2006.02.073 CrossRefPubMedGoogle Scholar
  43. Fukuyama M, Sakuma K, Park R et al (2012) C. elegans AMPKs promote survival and arrest germline development during nutrient stress. Biol Open 1:929–936.  https://doi.org/10.1242/bio.2012836 CrossRefPubMedPubMedCentralGoogle Scholar
  44. Fukuyama M, Kontani K, Katada T, Rougvie AE (2015) The C. elegans hypodermis couples progenitor cell quiescence to the dietary state. Curr Biol 25:1241–1248.  https://doi.org/10.1016/j.cub.2015.03.016 CrossRefPubMedGoogle Scholar
  45. Furuta T, Tuck S, Kirchner J et al (2000) EMB-30: an APC4 homologue required for metaphase-to-anaphase transitions during meiosis and mitosis in Caenorhabditis elegans. Mol Biol Cell 11:1401–1419CrossRefPubMedPubMedCentralGoogle Scholar
  46. Gems D, Sutton AJ, Sundermeyer ML et al (1998) Two pleiotropic classes of daf-2 mutation affect larval arrest, adult behavior, reproduction and longevity in Caenorhabditis elegans. Genetics 150:129–155PubMedPubMedCentralGoogle Scholar
  47. Gerhold AR, Ryan J, Vallée-Trudeau J-N et al (2015) Investigating the regulation of stem and progenitor cell mitotic progression by in situ imaging. Curr Biol 25:1123–1134.  https://doi.org/10.1016/j.cub.2015.02.054 CrossRefPubMedGoogle Scholar
  48. Gerisch B, Antebi A (2004) Hormonal signals produced by DAF-9/cytochrome P450 regulate C. elegans dauer diapause in response to environmental cues. Development 131:1765–1776.  https://doi.org/10.1242/dev.01068 CrossRefPubMedGoogle Scholar
  49. Gerisch B, Weitzel C, Kober-Eisermann C et al (2001) A hormonal signaling pathway influencing C. elegans metabolism, reproductive development, and life span. Dev Cell 1:841–851CrossRefPubMedGoogle Scholar
  50. Giaccia A, Weinstein R, Hu J, Stamato TD (1985) Cell cycle-dependent repair of double-strand DNA breaks in a γ-ray-sensitive Chinese hamster cell. Somat Cell Mol Genet 11:485–491CrossRefPubMedGoogle Scholar
  51. Golden JW, Riddle DL (1982) A pheromone influences larval development in the nematode Caenorhabditis elegans. Science 218:578–580CrossRefPubMedGoogle Scholar
  52. Golden JW, Riddle DL (1984) The Caenorhabditis elegans dauer larva: developmental effects of pheromone, food, and temperature. Dev Biol 102:368–378.  https://doi.org/10.1016/0012-1606(84)90201-X CrossRefPubMedGoogle Scholar
  53. Golden JW, Riddle DL (1985) A gene affecting production of the Caenorhabditis elegans dauer-inducing pheromone. Mol Gen Genet 198:534–536CrossRefPubMedGoogle Scholar
  54. Gottlieb S, Ruvkun G (1994) daf-2, daf-16 and daf-23: genetically interacting genes controlling Dauer formation in Caenorhabditis elegans. Genetics 137:107–120PubMedPubMedCentralGoogle Scholar
  55. Greer EL, Dowlatshahi D, Banko MR et al (2007) An AMPK-FOXO pathway mediates longevity induced by a novel method of dietary restriction in C. elegans. Curr Biol 17:1646–1656.  https://doi.org/10.1016/j.cub.2007.08.047 CrossRefPubMedPubMedCentralGoogle Scholar
  56. Groszer M, Erickson R, Scripture-Adams DD et al (2006) PTEN negatively regulates neural stem cell self-renewal by modulating G0-G1 cell cycle entry. Proc Natl Acad Sci U S A 103:111–116.  https://doi.org/10.1073/pnas.0509939103 CrossRefPubMedGoogle Scholar
  57. Gwinn DM, Shackelford DB, Egan DF et al (2008) AMPK phosphorylation of raptor mediates a metabolic checkpoint. Mol Cell 30:214–226.  https://doi.org/10.1016/j.molcel.2008.03.003 CrossRefPubMedPubMedCentralGoogle Scholar
  58. Hara K, Yonezawa K, Weng Q-P et al (1998) Amino acid sufficiency and mTOR regulate p70 S6 kinase and eIF-4E BP1 through a common effector mechanism. J Biol Chem 273:14484–14494.  https://doi.org/10.1074/jbc.273.23.14484 CrossRefPubMedGoogle Scholar
  59. Hara K, Maruki Y, Long X et al (2002) Raptor, a binding partner of target of rapamycin (TOR), mediates TOR action. Cell 110:177–189.  https://doi.org/10.1016/S0092-8674(02)00833-4 CrossRefPubMedGoogle Scholar
  60. Hatzfeld J, Williamson DH (1974) Cell-cycle dependent changes in sensitivity to γ-rays in synchronously dividing yeast culture. Exp Cell Res 84:431–435.  https://doi.org/10.1016/0014-4827(74)90426-1 CrossRefPubMedGoogle Scholar
  61. Hawley SA, Boudeau J, Reid JL et al (2003) Complexes between the LKB1 tumor suppressor, STRADα/β and MO25α/β are upstream kinases in the AMP-activated protein kinase cascade. J Biol 2:28.  https://doi.org/10.1186/1475-4924-2-28 CrossRefPubMedPubMedCentralGoogle Scholar
  62. Hedgecock EM, White JG (1985) Polyploid tissues in the nematode Caenorhabditis elegans. Dev Biol 107:128–133.  https://doi.org/10.1016/0012-1606(85)90381-1 CrossRefPubMedGoogle Scholar
  63. Hedgecock EM, Culotti JG, Hall DH, Stern BD (1987) Genetics of cell and axon migrations in Caenorhabditis elegans. Development 100:365–382PubMedGoogle Scholar
  64. Hemminki A, Markie D, Tomlinson I et al (1998) A serine/threonine kinase gene defective in Peutz-Jeghers syndrome. Nature 391:184–187.  https://doi.org/10.1038/34432 CrossRefPubMedGoogle Scholar
  65. Henderson ST, Gao D, Lambie EJ, Kimble J (1994) lag-2 may encode a signaling ligand for the GLP-1 and LIN-12 receptors of C. elegans. Development 120:2913–2924PubMedGoogle Scholar
  66. Hinz JM, Yamada NA, Salazar EP et al (2005) Influence of double-strand-break repair pathways on radiosensitivity throughout the cell cycle in CHO cells. DNA Repair 4:782–792.  https://doi.org/10.1016/j.dnarep.2005.03.005 CrossRefPubMedGoogle Scholar
  67. Hirsh D, Oppenheim D, Klass M (1976) Development of the reproductive system of Caenorhabditis elegans. Dev Biol 49:200–219.  https://doi.org/10.1016/0012-1606(76)90267-0 CrossRefPubMedGoogle Scholar
  68. Hodgkin J, Horvitz HR, Brenner S (1979) Nondisjunction mutants of the nematode CAENORHABDITIS ELEGANS. Genetics 91:67–94PubMedPubMedCentralGoogle Scholar
  69. Hong Y, Roy R, Ambros V (1998) Developmental regulation of a cyclin-dependent kinase inhibitor controls postembryonic cell cycle progression in Caenorhabditis elegans. Development 125:3585–3597PubMedGoogle Scholar
  70. Hong S-P, Leiper FC, Woods A et al (2003) Activation of yeast Snf1 and mammalian AMP-activated protein kinase by upstream kinases. Proc Natl Acad Sci U S A 100:8839–8843.  https://doi.org/10.1073/pnas.1533136100 CrossRefPubMedPubMedCentralGoogle Scholar
  71. Hsu H-J, Drummond-Barbosa D (2009) Insulin levels control female germline stem cell maintenance via the niche in Drosophila. Proc Natl Acad Sci U S A 106:1117–1121.  https://doi.org/10.1073/pnas.0809144106 CrossRefPubMedPubMedCentralGoogle Scholar
  72. Hsu H-J, Drummond-Barbosa D (2011) Insulin signals control the competence of the Drosophila female germline stem cell niche to respond to Notch ligands. Dev Biol 350:290–300.  https://doi.org/10.1016/j.ydbio.2010.11.032 CrossRefPubMedGoogle Scholar
  73. Hsu H-J, LaFever L, Drummond-Barbosa D (2008) Diet controls normal and tumorous germline stem cells via insulin-dependent and -independent mechanisms in Drosophila. Dev Biol 313:700–712.  https://doi.org/10.1016/j.ydbio.2007.11.006 CrossRefPubMedGoogle Scholar
  74. Hubbard EJA, Korta DZ, Dalfó D (2013) Physiological control of germline development. Adv Exp Med Biol 757:101–131.  https://doi.org/10.1007/978-1-4614-4015-4_5 CrossRefPubMedPubMedCentralGoogle Scholar
  75. Hung WL, Hung WL, Wang Y et al (2014) A Caenorhabditis elegans developmental decision requires insulin signaling-mediated neuron-intestine communication. Development 141:1767–1779.  https://doi.org/10.1242/dev.103846 CrossRefPubMedPubMedCentralGoogle Scholar
  76. Inoki K, Li Y, Zhu T et al (2002) TSC2 is phosphorylated and inhibited by Akt and suppresses mTOR signalling. Nat Cell Biol 4:648–657.  https://doi.org/10.1038/ncb839 CrossRefPubMedGoogle Scholar
  77. Inoki K, Zhu T, Guan K-L (2003) TSC2 mediates cellular energy response to control cell growth and survival. Cell 115:577–590.  https://doi.org/10.1016/S0092-8674(03)00929-2 CrossRefPubMedPubMedCentralGoogle Scholar
  78. Inoue T, Thomas JH (2000) Targets of TGF-β signaling in Caenorhabditis elegans dauer formation. Dev Biol 217:192–204.  https://doi.org/10.1006/dbio.1999.9545 CrossRefPubMedGoogle Scholar
  79. Iser WB, Gami MS, Wolkow CA (2007) Insulin signaling in Caenorhabditis elegans regulates both endocrine-like and cell-autonomous outputs. Dev Biol 303:434–447.  https://doi.org/10.1016/j.ydbio.2006.04.467 CrossRefPubMedGoogle Scholar
  80. Jazayeri A, Falck J, Lukas C et al (2005) ATM- and cell cycle-dependent regulation of ATR in response to DNA double-strand breaks. Nat Cell Biol 8:37–45.  https://doi.org/10.1038/ncb1337 CrossRefPubMedGoogle Scholar
  81. Jeggo PA (1990) Studies on mammalian mutants defective in rejoining double-strand breaks in DNA. Mutat Res 239:1–16CrossRefPubMedGoogle Scholar
  82. Jenne DE, Reimann H, Nezu J et al (1998) Peutz-Jeghers syndrome is caused by mutations in a novel serine threonine kinase. Nat Genet 18:38–43.  https://doi.org/10.1038/ng0198-38 CrossRefPubMedGoogle Scholar
  83. Jeong P-Y, Jung M, Yim Y-H et al (2005) Chemical structure and biological activity of the Caenorhabditis elegans dauer-inducing pheromone. Nature 433:541–545.  https://doi.org/10.1038/nature03201 CrossRefPubMedGoogle Scholar
  84. Jia K, Albert PS, Riddle DL (2002) DAF-9, a cytochrome P450 regulating C. elegans larval development and adult longevity. Development 129:221–231PubMedGoogle Scholar
  85. Jia K, Chen D, Riddle DL (2004) The TOR pathway interacts with the insulin signaling pathway to regulate C. elegans larval development, metabolism and life span. Development 131:3897–3906.  https://doi.org/10.1242/dev.01255 CrossRefPubMedGoogle Scholar
  86. Johnson TE, Mitchell DH, Kline S et al (1984) Arresting development arrests aging in the nematode Caenorhabditis elegans. Mech Ageing Dev 28:23–40CrossRefPubMedGoogle Scholar
  87. Kadyk LC, Hartwell LH (1992) Sister chromatids are preferred over homologs as substrates for recombinational repair in Saccharomyces cerevisiae. Genetics 132:387–402PubMedPubMedCentralGoogle Scholar
  88. Kawano T, Ito Y, Ishiguro M et al (2000) Molecular cloning and characterization of a new insulin/IGF-like peptide of the nematode Caenorhabditis elegans. Biochem Biophys Res Commun 273:431–436.  https://doi.org/10.1006/bbrc.2000.2971 CrossRefPubMedGoogle Scholar
  89. Kershner A, Crittenden SL, Friend K et al (2013) Germline stem cells and their regulation in the nematode Caenorhabditis elegans. Adv Exp Med Biol 786:29–46.  https://doi.org/10.1007/978-94-007-6621-1_3 CrossRefPubMedGoogle Scholar
  90. Killian DJ, Hubbard EJA (2005) Caenorhabditis elegans germline patterning requires coordinated development of the somatic gonadal sheath and the germ line. Dev Biol 279:322–335.  https://doi.org/10.1016/j.ydbio.2004.12.021 CrossRefPubMedGoogle Scholar
  91. Kim E, Goraksha-Hicks P, Li L et al (2008) Regulation of TORC1 by Rag GTPases in nutrient response. Nat Cell Biol 10:935–945.  https://doi.org/10.1038/ncb1753 CrossRefPubMedPubMedCentralGoogle Scholar
  92. Kim K, Sato K, Shibuya M et al (2009) Two chemoreceptors mediate developmental effects of dauer pheromone in C. elegans. Science 326:994–998.  https://doi.org/10.1126/science.1176331 CrossRefPubMedPubMedCentralGoogle Scholar
  93. Kimble J, Crittenden SL (2005) Germline proliferation and its control. WormBook 1–14. doi:  https://doi.org/10.1895/wormbook.1.13.1
  94. Kimble J, Hirsh D (1979) The postembryonic cell lineages of the hermaphrodite and male gonads in Caenorhabditis elegans. Dev Biol 70:396–417CrossRefPubMedGoogle Scholar
  95. Kimble JE, White JG (1981) On the control of germ cell development in Caenorhabditis elegans. Dev Biol 81:208–219CrossRefPubMedGoogle Scholar
  96. Kimura KD, Tissenbaum HA, Liu Y, Ruvkun G (1997) daf-2, an insulin receptor-like gene that regulates longevity and diapause in Caenorhabditis elegans. Science 277:942–946CrossRefPubMedGoogle Scholar
  97. Kitagawa R, Rose AM (1999) Components of the spindle-assembly checkpoint are essential in Caenorhabditis elegans. Nat Cell Biol 1:514–521.  https://doi.org/10.1038/70309 CrossRefPubMedGoogle Scholar
  98. Kitagawa R, Law E, Tang L, Rose AM (2002) The Cdc20 homolog, FZY-1, and its interacting protein, IFY-1, are required for proper chromosome segregation in Caenorhabditis elegans. Curr Biol 12:2118–2123CrossRefPubMedGoogle Scholar
  99. Klass M, Hirsh D (1976) Non-ageing developmental variant of Caenorhabditis elegans. Nature 260:523–525.  https://doi.org/10.1038/260523a0 CrossRefPubMedGoogle Scholar
  100. Klass M, Wolf N, Hirsh D (1976) Development of the male reproductive system and sexual transformation in the nematode Caenorhabditis elegans. Dev Biol 52:1–18.  https://doi.org/10.1016/0012-1606(76)90002-6 CrossRefPubMedGoogle Scholar
  101. Kniazeva M, Crawford QT, Seiber M et al (2004) Monomethyl branched-chain fatty acids play an essential role in Caenorhabditis elegans development. PLoS Biol 2:E257.  https://doi.org/10.1371/journal.pbio.0020257 CrossRefPubMedPubMedCentralGoogle Scholar
  102. Kniazeva M, Euler T, Han M (2008) A branched-chain fatty acid is involved in post-embryonic growth control in parallel to the insulin receptor pathway and its biosynthesis is feedback-regulated in C. elegans. Genes Dev 22:2102–2110.  https://doi.org/10.1101/gad.1692008 CrossRefPubMedPubMedCentralGoogle Scholar
  103. Kobayashi S, Yamada M, Asaoka M, Kitamura T (1996) Essential role of the posterior morphogen nanos for germline development in Drosophila. Nature 380:708–711.  https://doi.org/10.1038/380708a0 CrossRefPubMedGoogle Scholar
  104. Komatsu H, Mori I, Rhee JS et al (1996) Mutations in a cyclic nucleotide-gated channel lead to abnormal thermosensation and chemosensation in C. elegans. Neuron 17:707–718CrossRefPubMedGoogle Scholar
  105. Kops GJ, de Ruiter ND, De Vries-Smits AM et al (1999) Direct control of the forkhead transcription factor AFX by protein kinase B. Nature 398:630–634.  https://doi.org/10.1038/19328 CrossRefPubMedGoogle Scholar
  106. Korta DZ, Tuck S, Hubbard EJA (2012) S6K links cell fate, cell cycle and nutrient response in C. elegans germline stem/progenitor cells. Development 139:859–870.  https://doi.org/10.1242/dev.074047 CrossRefPubMedPubMedCentralGoogle Scholar
  107. Kumsta C, Hansen M (2012) C. elegans rrf-1 mutations maintain RNAi efficiency in the soma in addition to the germline. PLoS One 7:e35428.  https://doi.org/10.1371/journal.pone.0035428 CrossRefPubMedPubMedCentralGoogle Scholar
  108. LaFever L, Drummond-Barbosa D (2005) Direct control of germline stem cell division and cyst growth by neural insulin in Drosophila. Science 309:1071–1073.  https://doi.org/10.1126/science.1111410 CrossRefPubMedPubMedCentralGoogle Scholar
  109. LaFever L, Feoktistov A, Hsu H-J, 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.  https://doi.org/10.1242/dev.050351 CrossRefPubMedPubMedCentralGoogle Scholar
  110. Lakowski B, Hekimi S (1998) The genetics of caloric restriction in Caenorhabditis elegans. Proc Natl Acad Sci 95:13091–13096.  https://doi.org/10.1073/pnas.95.22.13091 CrossRefPubMedGoogle Scholar
  111. Laplante M, Sabatini DM (2012) mTOR signaling in growth control and disease. Cell 149:274–293.  https://doi.org/10.1016/j.cell.2012.03.017 CrossRefPubMedPubMedCentralGoogle Scholar
  112. Larsen PL, Albert PS, Riddle DL (1995) Genes that regulate both development and longevity in Caenorhabditis elegans. Genetics 139:1567–1583PubMedPubMedCentralGoogle Scholar
  113. Láscarez-Lagunas LI, Silva-García CG, Dinkova TD, Navarro RE (2014) LIN-35/Rb causes starvation-induced germ cell apoptosis via CED-9/Bcl2 downregulation in Caenorhabditis elegans. Mol Cell Biol 34:2499–2516.  https://doi.org/10.1128/MCB.01532-13 CrossRefPubMedPubMedCentralGoogle Scholar
  114. Lee H, Cho JS, Lambacher N et al (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.  https://doi.org/10.1074/jbc.M709115200 CrossRefPubMedPubMedCentralGoogle Scholar
  115. Li W, Kennedy SG, Ruvkun G (2003) daf-28 encodes a C. elegans insulin superfamily member that is regulated by environmental cues and acts in the DAF-2 signaling pathway. Genes Dev 17:844–858.  https://doi.org/10.1101/gad.1066503 CrossRefPubMedPubMedCentralGoogle Scholar
  116. Li Y, Inoki K, Guan K-L (2004) Biochemical and functional characterizations of small GTPase Rheb and TSC2 GAP activity. Mol Cell Biol 24:7965–7975.  https://doi.org/10.1128/MCB.24.18.7965-7975.2004 CrossRefPubMedPubMedCentralGoogle Scholar
  117. Libina N, Berman JR, Kenyon C (2003) Tissue-specific activities of C. elegans DAF-16 in the regulation of lifespan. Cell 115:489–502.  https://doi.org/10.1016/S0092-8674(03)00889-4 CrossRefPubMedGoogle Scholar
  118. Lieber MR (2010) The mechanism of double-strand DNA break repair by the nonhomologous DNA end-joining pathway. Annu Rev Biochem 79:181–211.  https://doi.org/10.1146/annurev.biochem.052308.093131 CrossRefPubMedPubMedCentralGoogle Scholar
  119. Lin K, Dorman JB, Rodan A, Kenyon C (1997) daf-16: an HNF-3/forkhead family member that can function to double the life-span of Caenorhabditis elegans. Science 278:1319–1322CrossRefPubMedGoogle Scholar
  120. Liu Z, Ambros V (1991) Alternative temporal control systems for hypodermal cell differentiation in Caenorhabditis elegans. Nature 350:162–165.  https://doi.org/10.1038/350162a0 CrossRefPubMedGoogle Scholar
  121. Long X, Spycher C, Han ZS et al (2002) TOR deficiency in C. elegans causes developmental arrest and intestinal atrophy by inhibition of mRNA translation. Curr Biol 12:1448–1461.  https://doi.org/10.1016/S0960-9822(02)01091-6 CrossRefPubMedGoogle Scholar
  122. Long X, Lin Y, Ortiz-Vega S et al (2005) Rheb binds and regulates the mTOR kinase. Curr Biol 15:702–713.  https://doi.org/10.1016/j.cub.2005.02.053 CrossRefPubMedGoogle Scholar
  123. Ludewig AH, Schroeder FC (2013) Ascaroside signaling in C. elegans. WormBook:1–22. doi:  https://doi.org/10.1895/wormbook.1.155.1
  124. Luo S, Kleemann GA, Ashraf JM et al (2010) TGF-β and insulin signaling regulate reproductive aging via oocyte and germline quality maintenance. Cell 143:299–312.  https://doi.org/10.1016/j.cell.2010.09.013 CrossRefPubMedPubMedCentralGoogle Scholar
  125. Ma XM, Blenis J (2009) Molecular mechanisms of mTOR-mediated translational control. Nat Rev Mol Cell Biol 10:307–318.  https://doi.org/10.1038/nrm2672 CrossRefPubMedGoogle Scholar
  126. Mak HY, Ruvkun G (2004) Intercellular signaling of reproductive development by the C. elegans DAF-9 cytochrome P450. Development 131:1777–1786.  https://doi.org/10.1242/dev.01069 CrossRefPubMedGoogle Scholar
  127. Masse I, Molin L, Billaud M, Solari F (2005) Lifespan and dauer regulation by tissue-specific activities of Caenorhabditis elegans DAF-18. Dev Biol 286:91–101.  https://doi.org/10.1016/j.ydbio.2005.07.010 CrossRefPubMedGoogle Scholar
  128. Matsunaga Y, Gengyo-Ando K, Mitani S et al (2012) Physiological function, expression pattern, and transcriptional regulation of a Caenorhabditis elegans insulin-like peptide, INS-18. Biochem Biophys Res Commun 423:478–483.  https://doi.org/10.1016/j.bbrc.2012.05.145 CrossRefPubMedGoogle Scholar
  129. McGrath PT, Xu Y, Ailion M et al (2011) Parallel evolution of domesticated Caenorhabditis species targets pheromone receptor genes. Nature 477:321–325.  https://doi.org/10.1038/nature10378 CrossRefPubMedPubMedCentralGoogle Scholar
  130. Meister G (2013) Argonaute proteins: functional insights and emerging roles. Nat Rev Genet 14:447–459.  https://doi.org/10.1038/nrg3462 CrossRefPubMedGoogle Scholar
  131. Michaelson D, Korta DZ, Capua Y, Hubbard EJA (2010) Insulin signaling promotes germline proliferation in C. elegans. Development 137:671–680.  https://doi.org/10.1242/dev.042523 CrossRefPubMedPubMedCentralGoogle Scholar
  132. Miyamoto K, Araki KY, Naka K et al (2007) Foxo3a is essential for maintenance of the hematopoietic stem cell pool. Cell Stem Cell 1:101–112.  https://doi.org/10.1016/j.stem.2007.02.001 CrossRefPubMedGoogle Scholar
  133. Morris JZ, Tissenbaum HA, Ruvkun G (1996) A phosphatidylinositol-3-OH kinase family member regulating longevity and diapause in Caenorhabditis elegans. Nature 382:536–539.  https://doi.org/10.1038/382536a0 CrossRefPubMedGoogle Scholar
  134. Motola DL, Cummins CL, Rottiers V et al (2006) Identification of ligands for DAF-12 that govern dauer formation and reproduction in C. elegans. Cell 124:1209–1223.  https://doi.org/10.1016/j.cell.2006.01.037 CrossRefPubMedGoogle Scholar
  135. Murakami M, Koga M, Ohshima Y (2001) DAF-7/TGF-β expression required for the normal larval development in C. elegans is controlled by a presumed guanylyl cyclase DAF-11. Mech Dev 109:27–35.  https://doi.org/10.1016/S0925-4773(01)00507-X CrossRefPubMedGoogle Scholar
  136. Murata Y, Wharton RP (1995) Binding of pumilio to maternal hunchback mRNA is required for posterior patterning in Drosophila embryos. Cell 80:747–756CrossRefGoogle Scholar
  137. Murphy CT, Hu PJ (2013) Insulin/insulin-like growth factor signaling in C. elegans. WormBook 1–43. doi:  https://doi.org/10.1895/wormbook.1.164.1
  138. Nadarajan S, Govindan JA, McGovern M et al (2009) MSP and GLP-1/Notch signaling coordinately regulate actomyosin-dependent cytoplasmic streaming and oocyte growth in C. elegans. Development 136:2223–2234.  https://doi.org/10.1242/dev.034603 CrossRefPubMedPubMedCentralGoogle Scholar
  139. Naka K, Hoshii T, Muraguchi T et al (2010) TGF-β-FOXO signalling maintains leukaemia-initiating cells in chronic myeloid leukaemia. Nature 463:676–680.  https://doi.org/10.1038/nature08734 CrossRefPubMedGoogle Scholar
  140. Nakae J, Park BC, Accili D (1999) Insulin stimulates phosphorylation of the forkhead transcription factor FKHR on serine 253 through a Wortmannin-sensitive pathway. J Biol Chem 274:15982–15985.  https://doi.org/10.1074/jbc.274.23.15982 CrossRefPubMedGoogle Scholar
  141. Narbonne P, Roy R (2006a) Inhibition of germline proliferation during C. elegans dauer development requires PTEN, LKB1 and AMPK signalling. Development 133:611–619.  https://doi.org/10.1242/dev.02232 CrossRefPubMedGoogle Scholar
  142. Narbonne P, Roy R (2006b) Regulation of germline stem cell proliferation downstream of nutrient sensing. Cell Div 1:29.  https://doi.org/10.1186/1747-1028-1-29 CrossRefPubMedPubMedCentralGoogle Scholar
  143. Narbonne P, Hyenne V, Li S et al (2010) Differential requirements for STRAD in LKB1-dependent functions in C. elegans. Development 137:661–670.  https://doi.org/10.1242/dev.042044 CrossRefPubMedGoogle Scholar
  144. Ogg S, Paradis S, Gottlieb S et al (1997) The fork head transcription factor DAF-16 transduces insulin-like metabolic and longevity signals in C. elegans. Nature 389:994–999.  https://doi.org/10.1038/40194 CrossRefPubMedGoogle Scholar
  145. Ogg S, Ruvkun G (1998) The C. elegans PTEN homolog, DAF-18, acts in the insulin receptor-like metabolic signaling pathway. Mol Cell 2:887–893CrossRefPubMedGoogle Scholar
  146. Park D, Estevez A, Riddle DL (2010) Antagonistic Smad transcription factors control the dauer/non-dauer switch in C. elegans. Development 137:477–485.  https://doi.org/10.1242/dev.043752 CrossRefPubMedPubMedCentralGoogle Scholar
  147. Pauklin S, Vallier L (2013) The cell-cycle state of stem cells determines cell fate propensity. Cell 155:135–147.  https://doi.org/10.1016/j.cell.2013.08.031 CrossRefPubMedPubMedCentralGoogle Scholar
  148. Pfeiffer P, Goedecke W, Obe G (2000) Mechanisms of DNA double-strand break repair and their potential to induce chromosomal aberrations. Mutagenesis 15:289–302CrossRefPubMedGoogle Scholar
  149. Pierce SB, Costa M, Wisotzkey R et al (2001) Regulation of DAF-2 receptor signaling by human insulin and ins-1, a member of the unusually large and diverse C. elegans insulin gene family. Genes Dev 15:672–686.  https://doi.org/10.1101/gad.867301 CrossRefPubMedPubMedCentralGoogle Scholar
  150. Popham JD, Webster JM (1979) Aspects of the fine structure of the dauer larva of the nematode Caenorhabditis elegans. Can J Zool 57:794–800.  https://doi.org/10.1139/z79-098 CrossRefGoogle Scholar
  151. Potter CJ, Pedraza LG, Xu T (2002) Akt regulates growth by directly phosphorylating Tsc2. Nat Cell Biol 4:658–665.  https://doi.org/10.1038/ncb840 CrossRefPubMedGoogle Scholar
  152. Pungaliya C, Srinivasan J, Fox BW et al (2009) A shortcut to identifying small molecule signals that regulate behavior and development in Caenorhabditis elegans. Proc Natl Acad Sci U S A 106:7708–7713.  https://doi.org/10.1073/pnas.0811918106 CrossRefPubMedPubMedCentralGoogle Scholar
  153. Radimerski T, Montagne J, Rintelen F et al (2002) dS6K-regulated cell growth is dPKB/dPI(3)K-independent, but requires dPDK1. Nat Cell Biol 4:251–255CrossRefPubMedGoogle Scholar
  154. Ren P, Lim CS, Johnsen R et al (1996) Control of C. elegans larval development by neuronal expression of a TGF-β homolog. Science 274:1389–1391CrossRefPubMedGoogle Scholar
  155. Rena G, Guo S, Cichy SC et al (1999) Phosphorylation of the transcription factor forkhead family member FKHR by protein kinase B. J Biol Chem 274:17179–17183.  https://doi.org/10.1074/jbc.274.24.17179 CrossRefPubMedGoogle Scholar
  156. Renault VM, Rafalski VA, Morgan AA et al (2009) FoxO3 regulates neural stem cell homeostasis. Cell Stem Cell 5:527–539.  https://doi.org/10.1016/j.stem.2009.09.014 CrossRefPubMedPubMedCentralGoogle Scholar
  157. Riddle DL, Albert PS (1997) Genetic and environmental regulation of dauer larva development. In: Riddle DL, Blumenthal T, Meyer BJ et al (eds) C. ELEGANS II, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, pp 739–768Google Scholar
  158. Riddle DL, Swanson MM, Albert PS (1981) Interacting genes in nematode dauer larva formation. Nature 290:668–671CrossRefPubMedGoogle Scholar
  159. Ritter AD, Shen Y, Fuxman Bass J et al (2013) Complex expression dynamics and robustness in C. elegans insulin networks. Genome Res 23:954–965.  https://doi.org/10.1101/gr.150466.112 CrossRefPubMedPubMedCentralGoogle Scholar
  160. Rothkamm K, Krüger I, Thompson LH, Löbrich M (2003) Pathways of DNA double-strand break repair during the mammalian cell cycle. Mol Cell Biol 23:5706–5715.  https://doi.org/10.1128/MCB.23.16.5706-5715.2003 CrossRefPubMedPubMedCentralGoogle Scholar
  161. Ruaud A-F, Bessereau J-L (2006) Activation of nicotinic receptors uncouples a developmental timer from the molting timer in C. elegans. Development 133:2211–2222.  https://doi.org/10.1242/dev.02392 CrossRefPubMedGoogle Scholar
  162. Salinas LS, Maldonado E, Navarro RE (2006) Stress-induced germ cell apoptosis by a p53 independent pathway in Caenorhabditis elegans. Cell Death Differ 13:2129–2139.  https://doi.org/10.1038/sj.cdd.4401976 CrossRefPubMedGoogle Scholar
  163. Sancak Y, Thoreen CC, Peterson TR et al (2007) PRAS40 is an insulin-regulated inhibitor of the mTORC1 protein kinase. Mol Cell 25:903–915.  https://doi.org/10.1016/j.molcel.2007.03.003 CrossRefPubMedGoogle Scholar
  164. Sancak Y, Peterson TR, Shaul YD et al (2008) The Rag GTPases bind raptor and mediate amino acid signaling to mTORC1. Science 320:1496–1501.  https://doi.org/10.1126/science.1157535 CrossRefPubMedPubMedCentralGoogle Scholar
  165. Schackwitz WS, Inoue T, Thomas JH (1996) Chemosensory neurons function in parallel to mediate a pheromone response in C. elegans. Neuron 17:719–728CrossRefPubMedGoogle Scholar
  166. Schaner CE, Deshpande G, Schedl PD, Kelly WG (2003) A conserved chromatin architecture marks and maintains the restricted germ cell lineage in worms and flies. Dev Cell 5:747–757CrossRefPubMedPubMedCentralGoogle Scholar
  167. Schindler AJ, Baugh LR, Sherwood DR (2014) Identification of late larval stage developmental checkpoints in Caenorhabditis elegans regulated by insulin/IGF and steroid hormone signaling pathways. PLoS Genet 10:e1004426.  https://doi.org/10.1371/journal.pgen.1004426 CrossRefPubMedPubMedCentralGoogle Scholar
  168. Seidel HS, Kimble J (2011) The oogenic germline starvation response in C. elegans. PLoS One 6:e28074.  https://doi.org/10.1371/journal.pone.0028074 CrossRefPubMedPubMedCentralGoogle Scholar
  169. Seki Y, Yamaji M, Yabuta Y et al (2007) Cellular dynamics associated with the genome-wide epigenetic reprogramming in migrating primordial germ cells in mice. Development 134:2627–2638.  https://doi.org/10.1242/dev.005611 CrossRefPubMedGoogle Scholar
  170. Sela Y, Molotski N, Golan S et al (2012) Human embryonic stem cells exhibit increased propensity to differentiate during the G1 phase prior to phosphorylation of retinoblastoma protein. Stem Cells 30:1097–1108.  https://doi.org/10.1002/stem.1078 CrossRefPubMedGoogle Scholar
  171. Sengupta S, Peterson TR, Sabatini DM (2010) Regulation of the mTOR complex 1 pathway by nutrients, growth factors, and stress. Mol Cell 40:310–322.  https://doi.org/10.1016/j.molcel.2010.09.026 CrossRefPubMedPubMedCentralGoogle Scholar
  172. Shaw RJ, Kosmatka M, Bardeesy N et al (2004) The tumor suppressor LKB1 kinase directly activates AMP-activated kinase and regulates apoptosis in response to energy stress. Proc Natl Acad Sci U S A 101:3329–3335.  https://doi.org/10.1073/pnas.0308061100 CrossRefPubMedPubMedCentralGoogle Scholar
  173. Shyh-Chang N, Daley GQ, Cantley LC (2013) Stem cell metabolism in tissue development and aging. Development 140:2535–2547.  https://doi.org/10.1242/dev.091777 CrossRefPubMedPubMedCentralGoogle Scholar
  174. Sijen T, Fleenor J, Simmer F et al (2001) On the role of RNA amplification in dsRNA-triggered gene silencing. Cell 107:465–476.  https://doi.org/10.1016/S0092-8674(01)00576-1 CrossRefPubMedGoogle Scholar
  175. Snow MI, Larsen PL (2000) Structure and expression of daf-12: a nuclear hormone receptor with three isoforms that are involved in development and aging in Caenorhabditis elegans. BBA-Gene Struct Expr 1494:104–116.  https://doi.org/10.1016/S0167-4781(00)00224-4 CrossRefGoogle Scholar
  176. Sonoda J, Wharton RP (1999) Recruitment of Nanos to hunchback mRNA by Pumilio. Genes Dev 13:2704–2712.  https://doi.org/10.1093/emboj/16.4.834 CrossRefPubMedPubMedCentralGoogle Scholar
  177. Sousa-Nunes R, Yee LL, Gould AP (2011) Fat cells reactivate quiescent neuroblasts via TOR and glial insulin relays in Drosophila. Nature 471:508–512.  https://doi.org/10.1038/nature09867 CrossRefPubMedPubMedCentralGoogle Scholar
  178. Srinivasan J, von SH R, Bose N et al (2012) A modular library of small molecule signals regulates social behaviors in Caenorhabditis elegans. PLoS Biol 10:e1001237.  https://doi.org/10.1371/journal.pbio.1001237 CrossRefPubMedPubMedCentralGoogle Scholar
  179. Stein KK, Davis ES, Hays T, Golden A (2007) Components of the spindle assembly checkpoint regulate the anaphase-promoting complex during meiosis in Caenorhabditis elegans. Genetics 175:107–123.  https://doi.org/10.1534/genetics.106.059105 CrossRefPubMedPubMedCentralGoogle Scholar
  180. Su TT, Campbell SD, O'Farrell PH (1998) The cell cycle program in germ cells of the Drosophila embryo. Dev Biol 196:160–170.  https://doi.org/10.1006/dbio.1998.8855 CrossRefPubMedGoogle Scholar
  181. Subramaniam K, Seydoux G (1999) nos-1 and nos-2, two genes related to Drosophila nanos, regulate primordial germ cell development and survival in Caenorhabditis elegans. Development 126:4861–4871PubMedGoogle Scholar
  182. Sulston JE, Schierenberg E, White JG, Thomson JN (1983) The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev Biol 100:64–119CrossRefPubMedGoogle Scholar
  183. Sun P, Quan Z, Zhang B et al (2010) TSC1/2 tumour suppressor complex maintains Drosophila germline stem cells by preventing differentiation. Development 137:2461–2469.  https://doi.org/10.1242/dev.051466 CrossRefPubMedGoogle Scholar
  184. Symington LS, Gautier J (2011) Double-strand break end resection and repair pathway choice. Annu Rev Genet 45:247–271.  https://doi.org/10.1146/annurev-genet-110410-132435 CrossRefPubMedGoogle Scholar
  185. Takata M, Sasaki MS, Sonoda E et al (1998) Homologous recombination and non-homologous end-joining pathways of DNA double-strand break repair have overlapping roles in the maintenance of chromosomal integrity in vertebrate cells. EMBO J 17:5497–5508.  https://doi.org/10.1093/emboj/17.18.5497 CrossRefPubMedPubMedCentralGoogle Scholar
  186. Tang ED, Nuñez G, Barr FG, Guan KL (1999) Negative regulation of the forkhead transcription factor FKHR by Akt. J Biol Chem 274:16741–16746.  https://doi.org/10.1074/jbc.274.24.16741 CrossRefPubMedGoogle Scholar
  187. Tennessen JM, Thummel CS (2011) Coordinating growth and maturation – insights from Drosophila. Curr Biol 21:R750–R757.  https://doi.org/10.1016/j.cub.2011.06.033 CrossRefPubMedPubMedCentralGoogle Scholar
  188. Terasima T, Tolmach LJ (1961) Changes in x-ray sensitivity of HeLa cells during the division cycle. Nature 190:1210–1211CrossRefPubMedGoogle Scholar
  189. Thomas JH, Birnby DA, Vowels JJ (1993) Evidence for parallel processing of sensory information controlling dauer formation in Caenorhabditis elegans. Genetics 134:1105–1117PubMedPubMedCentralGoogle Scholar
  190. Tothova Z, Kollipara R, Huntly BJ et al (2007) FoxOs are critical mediators of hematopoietic stem cell resistance to physiologic oxidative stress. Cell 128:325–339.  https://doi.org/10.1016/j.cell.2007.01.003 CrossRefPubMedGoogle Scholar
  191. Van Gilst MR, Hadjivassiliou H, Jolly A, Yamamoto KR (2005a) Nuclear hormone receptor NHR-49 controls fat consumption and fatty acid composition in C. elegans. PLoS Biol 3:e53.  https://doi.org/10.1371/journal.pbio.0030053 CrossRefPubMedPubMedCentralGoogle Scholar
  192. Van Gilst MR, Hadjivassiliou H, Yamamoto KR (2005b) A Caenorhabditis elegans nutrient response system partially dependent on nuclear receptor NHR-49. Proc Natl Acad Sci U S A 102:13496–13501.  https://doi.org/10.1073/pnas.0506234102 CrossRefPubMedPubMedCentralGoogle Scholar
  193. Vowels JJ, Thomas JH (1992) Genetic analysis of chemosensory control of dauer formation in Caenorhabditis elegans. Genetics 130:105–123PubMedPubMedCentralGoogle Scholar
  194. Watanabe S, Yamamoto TG, 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.  https://doi.org/10.1038/emboj.2008.32 CrossRefPubMedPubMedCentralGoogle Scholar
  195. Wolkow CA, Kimura KD, Lee MS, Ruvkun G (2000) Regulation of C. elegans life-span by insulinlike signaling in the nervous system. Science 290:147–150.  https://doi.org/10.1126/science.290.5489.147 CrossRefPubMedGoogle Scholar
  196. Woods A, Johnstone SR, Dickerson K et al (2003) LKB1 is the upstream kinase in the AMP-activated protein kinase cascade. Curr Biol 13:2004–2008.  https://doi.org/10.1016/j.cub.2003.10.031 CrossRefPubMedGoogle Scholar
  197. Yilmaz ÖH, Valdez R, Theisen BK et al (2006) Pten dependence distinguishes haematopoietic stem cells from leukaemia-initiating cells. Nature 441:475–482.  https://doi.org/10.1038/nature04703 CrossRefPubMedGoogle Scholar
  198. Yilmaz ÖH, Katajisto P, Lamming DW et al (2012) mTORC1 in the Paneth cell niche couples intestinal stem-cell function to calorie intake. Nature 486:490–495.  https://doi.org/10.1038/nature11163 CrossRefPubMedPubMedCentralGoogle Scholar
  199. Zhu H, Shen H, Sewell AK et al (2013) A novel sphingolipid-TORC1 pathway critically promotes postembryonic development in Caenorhabditis elegans. elife 2:e00429.  https://doi.org/10.7554/eLife.00429 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Japan KK, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Laboratory of Physiological Chemistry, Graduate School of Pharmaceutical SciencesUniversity of TokyoTokyoJapan

Personalised recommendations