Identification of Late Larval Stage Developmental Checkpoints in Regulated by Insulin/IGF and Steroid Hormone Signaling Pathways

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Organisms in the wild often face long periods in which food is scarce. This may occur due to seasonal effects, loss of territory, or changes in predator-to-prey ratio. During periods of scarcity, organisms undergo adaptations to conserve resources and prolong survival. When nutrient deprivation occurs during development, physical growth and maturation to adulthood is delayed. These effects are also observed in malnourished individuals, who are smaller and reach puberty at later ages. Developmental arrest in response to nutrient scarcity requires a means of sensing changing nutrient conditions and coordinating an organism-wide response. How this occurs is not well understood. We assessed the developmental response to nutrient withdrawal in the nematode worm Caenorhabditis elegans. By removing food in the late larval stages, a period of extensive tissue formation, we have uncovered previously unknown checkpoints that occur at precise times in development. Diverse tissues and cellular processes arrest at the checkpoints. Insulin-like signaling and steroid hormone signaling regulate tissue arrest following nutrient withdrawal. These pathways are conserved in mammals and are linked to growth processes and diseases. Given that the pathways that respond to nutrition are conserved in animals, it is possible that similar checkpoints may also be important in human development.

Vyšlo v časopise: Identification of Late Larval Stage Developmental Checkpoints in Regulated by Insulin/IGF and Steroid Hormone Signaling Pathways. PLoS Genet 10(6): e32767. doi:10.1371/journal.pgen.1004426
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004426

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Zdroje

1. TennessenJM, ThummelCS (2011) Coordinating growth and maturation - insights from Drosophila. Curr Biol 21: R750–757.

2. BaughLR (2013) To grow or not to grow: nutritional control of development during Caenorhabditis elegans L1 arrest. Genetics 194: 539–555.

3. HuPJ (2007) Dauer. WormBook 1–19.

4. McCueMD (2010) Starvation physiology: reviewing the different strategies animals use to survive a common challenge. Comp Biochem Physiol A Mol Integr Physiol 156: 1–18.

5. GoldenJW, RiddleDL (1984) The Caenorhabditis elegans dauer larva: developmental effects of pheromone, food, and temperature. Dev Biol 102: 368–378.

6. JohnsonTE, MitchellDH, KlineS, KemalR, FoyJ (1984) Arresting development arrests aging in the nematode Caenorhabditis elegans. Mech Ageing Dev 28: 23–40.

7. BaughLR, SternbergPW (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.

8. RuaudAF, BessereauJL (2006) Activation of nicotinic receptors uncouples a developmental timer from the molting timer in C. elegans. Development 133: 2211–2222.

9. AngeloG, Van GilstMR (2009) Starvation protects germline stem cells and extends reproductive longevity in C. elegans. Science 326: 954–958.

10. SeidelHS, KimbleJ (2011) The oogenic germline starvation response in C. elegans. PLoS One 6: e28074.

11. GemsD, SuttonAJ, SundermeyerML, AlbertPS, KingKV, et al. (1998) Two pleiotropic classes of daf-2 mutation affect larval arrest, adult behavior, reproduction and longevity in Caenorhabditis elegans. Genetics 150: 129–155.

12. VowelsJJ, ThomasJH (1992) Genetic analysis of chemosensory control of dauer formation in Caenorhabditis elegans. Genetics 130: 105–123.

13. HendersonST, JohnsonTE (2001) daf-16 integrates developmental and environmental inputs to mediate aging in the nematode Caenorhabditis elegans. Curr Biol 11: 1975–1980.

14. OhSW, MukhopadhyayA, DixitBL, RahaT, GreenMR, et al. (2006) Identification of direct DAF-16 targets controlling longevity, metabolism and diapause by chromatin immunoprecipitation. Nat Genet 38: 251–257.

15. McElweeJ, BubbK, ThomasJH (2003) Transcriptional outputs of the Caenorhabditis elegans forkhead protein DAF-16. Aging Cell 2: 111–121.

16. KasugaH, FukuyamaM, KitazawaA, KontaniK, KatadaT (2013) The microRNA miR-235 couples blast-cell quiescence to the nutritional state. Nature 497: 503–506.

17. AntebiA (2013) Steroid regulation of C. elegans diapause, developmental timing, and longevity. Curr Top Dev Biol 105: 181–212.

18. MotolaDL, CumminsCL, RottiersV, SharmaKK, LiT, et al. (2006) Identification of ligands for DAF-12 that govern dauer formation and reproduction in C. elegans. Cell 124: 1209–1223.

19. GerischB, AntebiA (2004) Hormonal signals produced by DAF-9/cytochrome P450 regulate C. elegans dauer diapause in response to environmental cues. Development 131: 1765–1776.

20. JiaK, AlbertPS, RiddleDL (2002) DAF-9, a cytochrome P450 regulating C. elegans larval development and adult longevity. Development 129: 221–231.

21. MakHY, RuvkunG (2004) Intercellular signaling of reproductive development by the C. elegans DAF-9 cytochrome P450. Development 131: 1777–1786.

22. SchindlerAJ, SherwoodDR (2013) Morphogenesis of the Caenorhabditis elegans vulva. WIREs Dev Biol 2: 75–95.

23. SherwoodDR, SternbergPW (2003) Anchor cell invasion into the vulval epithelium in C. elegans. Dev Cell 5: 21–31.

24. HsinH, KenyonC (1999) Signals from the reproductive system regulate the lifespan of C. elegans. Nature 399: 362–366.

25. CurranSP, WuX, RiedelCG, RuvkunG (2009) A soma-to-germline transformation in long-lived Caenorhabditis elegans mutants. Nature 459: 1079–1084.

26. Arantes-OliveiraN, ApfeldJ, DillinA, KenyonC (2002) Regulation of life-span by germ-line stem cells in Caenorhabditis elegans. Science 295: 502–505.

27. GreenwaldIS, SternbergPW, HorvitzHR (1983) The lin-12 locus specifies cell fates in Caenorhabditis elegans. Cell 34: 435–444.

28. SternbergPW, HorvitzHR (1986) Pattern formation during vulval development in C. elegans. Cell 44: 761–772.

29. BurdineRD, BrandaCS, SternMJ (1998) EGL-17(FGF) expression coordinates the attraction of the migrating sex myoblasts with vulval induction in C. elegans. Development 125: 1083–1093.

30. BersetT, HoierEF, BattuG, CanevasciniS, HajnalA (2001) Notch inhibition of RAS signaling through MAP kinase phosphatase LIP-1 during C. elegans vulval development. Science 291: 1055–1058.

31. EulingS, AmbrosV (1996) Reversal of cell fate determination in Caenorhabditis elegans vulval development. Development 122: 2507–2515.

32. MatyashV, EntchevEV, MendeF, Wilsch-BrauningerM, ThieleC, et al. (2004) Sterol-derived hormone(s) controls entry into diapause in Caenorhabditis elegans by consecutive activation of DAF-12 and DAF-16. PLoS Biol 2: e280.

33. Sharma-KishoreR, WhiteJG, SouthgateE, PodbilewiczB (1999) Formation of the vulva in Caenorhabditis elegans: a paradigm for organogenesis. Development 126: 691–699.

34. KoppenM, SimskeJS, SimsPA, FiresteinBL, HallDH, et al. (2001) Cooperative regulation of AJM-1 controls junctional integrity in Caenorhabditis elegans epithelia. Nat Cell Biol 3: 983–991.

35. AbrahanteJE, DaulAL, LiM, VolkML, TennessenJM, et al. (2003) The Caenorhabditis elegans hunchback-like gene lin-57/hbl-1 controls developmental time and is regulated by microRNAs. Dev Cell 4: 625–637.

36. SinghR, SulstonJE (1978) Some observations on moulting in Caenorhabditis elegans. Nematologica 24: 63–71.

37. JohnstoneIL, BarryJD (1996) Temporal reiteration of a precise gene expression pattern during nematode development. EMBO J 15: 3633–3639.

38. FrandAR, RusselS, RuvkunG (2005) Functional genomic analysis of C. elegans molting. PLoS Biol 3: e312.

39. MeliVS, OsunaB, RuvkunG, FrandAR (2010) MLT-10 defines a family of DUF644 and proline-rich repeat proteins involved in the molting cycle of Caenorhabditis elegans. Mol Biol Cell 21: 1648–1661.

40. BaughLR, DemodenaJ, SternbergPW (2009) RNA Pol II accumulates at promoters of growth genes during developmental arrest. Science 324: 92–94.

41. TaguchiA, WhiteMF (2008) Insulin-like signaling, nutrient homeostasis, and life span. Annu Rev Physiol 70: 191–212.

42. LibinaN, BermanJR, KenyonC (2003) Tissue-specific activities of C. elegans DAF-16 in the regulation of lifespan. Cell 115: 489–502.

43. ZhangP, JudyM, LeeSJ, KenyonC (2013) Direct and Indirect Gene Regulation by a Life-Extending FOXO Protein in C. elegans: Roles for GATA Factors and Lipid Gene Regulators. Cell Metab 17: 85–100.

44. QiW, HuangX, Neumann-HaefelinE, SchulzeE, BaumeisterR (2012) Cell-nonautonomous signaling of FOXO/DAF-16 to the stem cells of Caenorhabditis elegans. PLoS Genet 8: e1002836.

45. TimmonsL, CourtDL, FireA (2001) Ingestion of bacterially expressed dsRNAs can produce specific and potent genetic interference in Caenorhabditis elegans. Gene 263: 103–112.

46. CalixtoA, ChelurD, TopalidouI, ChenX, ChalfieM (2010) Enhanced neuronal RNAi in C. elegans using SID-1. Nat Methods 7: 554–559.

47. GerischB, WeitzelC, Kober-EisermannC, RottiersV, AntebiA (2001) A hormonal signaling pathway influencing C. elegans metabolism, reproductive development, and life span. Dev Cell 1: 841–851.

48. AntebiA, YehWH, TaitD, HedgecockEM, RiddleDL (2000) daf-12 encodes a nuclear receptor that regulates the dauer diapause and developmental age in C. elegans. Genes Dev 14: 1512–1527.

49. HagedornEJ, SherwoodDR (2011) Cell invasion through basement membrane: the anchor cell breaches the barrier. Curr Opin Cell Biol 23: 589–596.

50. CallierV, NijhoutHF (2011) Control of body size by oxygen supply reveals size-dependent and size-independent mechanisms of molting and metamorphosis. Proc Natl Acad Sci U S A 108: 14664–14669.

51. HemmiA, JormalainenV (2004) Genetic and environmental variation in performance of a marine isopod: effects of eutrophication. Oecologia 140: 302–311.

52. BraendleC, FelixMA (2008) Plasticity and errors of a robust developmental system in different environments. Dev Cell 15: 714–724.

53. KnightCG, PatelMN, AzevedoRB, LeroiAM (2002) A novel mode of ecdysozoan growth in Caenorhabditis elegans. Evol Dev 4: 16–27.

54. OggS, ParadisS, GottliebS, PattersonGI, LeeL, et al. (1997) The Fork head transcription factor DAF-16 transduces insulin-like metabolic and longevity signals in C. elegans. Nature 389: 994–999.

55. BroueF, LiereP, KenyonC, BaulieuEE (2007) A steroid hormone that extends the lifespan of Caenorhabditis elegans. Aging Cell 6: 87–94.

56. JeongMH, KawasakiI, ShimYH (2010) A circulatory transcriptional regulation among daf-9, daf-12, and daf-16 mediates larval development upon cholesterol starvation in Caenorhabditis elegans. Dev Dyn 239: 1931–1940.

57. WangJ, KimSK (2003) Global analysis of dauer gene expression in Caenorhabditis elegans. Development 130: 1621–1634.

58. BaughLR, KurhanewiczN, SternbergPW (2011) Sensitive and precise quantification of insulin-like mRNA expression in Caenorhabditis elegans. PLoS One 6: e18086.

59. ByerlyL, CassadaRC, RussellRL (1976) The life cycle of the nematode Caenorhabditis elegans. I. Wild-type growth and reproduction. Dev Biol 51: 23–33.

60. FujisawaT, HayakawaE (2012) Peptide signaling in Hydra. Int J Dev Biol 56: 543–550.

61. BridghamJT, EickGN, LarrouxC, DeshpandeK, HarmsMJ, et al. (2010) Protein evolution by molecular tinkering: diversification of the nuclear receptor superfamily from a ligand-dependent ancestor. PLoS Biol 8: e1000497.

62. AtwoodCS, BowenRL (2011) The reproductive-cell cycle theory of aging: an update. Exp Gerontol 46: 100–107.

63. LindsayRS, BennettPH (2001) Type 2 diabetes, the thrifty phenotype - an overview. Br Med Bull 60: 21–32.

64. LundquistEA, HermanRK, ShawJE, BargmannCI (1998) UNC-115, a conserved protein with predicted LIM and actin-binding domains, mediates axon guidance in C. elegans. Neuron 21: 385–392.

65. QadotaH, InoueM, HikitaT, KoppenM, HardinJD, et al. (2007) Establishment of a tissue-specific RNAi system in C. elegans. Gene 400: 166–173.