Skip to main content

Physiological Control of Germline Development

  • Chapter
  • First Online:
Germ Cell Development in C. elegans

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 757))

Abstract

The intersection between developmental programs and environmental conditions that alter physiology is a growing area of research interest. The C. elegans germ line is emerging as a particularly sensitive and powerful model for these studies. The germ line is subject to environmentally regulated diapause points that allow worms to withstand harsh conditions both prior to and after reproduction commences. It also responds to more subtle changes in physiological conditions. Recent studies demonstrate that different aspects of germ line development are sensitive to environmental and physiological changes and that conserved signaling pathways such as the AMPK, Insulin/IGF, TGFβ, and TOR-S6K, and nuclear hormone receptor pathways mediate this sensitivity. Some of these pathways genetically interact with but appear distinct from previously characterized mechanisms of germline cell fate control such as Notch signaling. Here, we review several aspects of hermaphrodite germline development in the context of “feasting,” “food-limited,” and “fasting” conditions. We also consider connections between lifespan, metabolism and the germ line, and we comment on special considerations for examining germline development under altered environmental and physiological conditions. Finally, we summarize the major outstanding questions in the field.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Angelo G, Van Gilst MR (2009) Starvation protects germline stem cells and extends reproductive longevity in C. elegans. Science 326(5955):954–958

    PubMed  CAS  Google Scholar 

  • Arantes-Oliveira N, Apfeld J, Dillin A, Kenyon C (2002) Regulation of life-span by germ-line stem cells in Caenorhabditis elegans. Science 295(5554):502–505

    PubMed  CAS  Google Scholar 

  • 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(4):589–599

    PubMed  CAS  Google Scholar 

  • Avery L (1993) The genetics of feeding in Caenorhabditis elegans. Genetics 133(4):897–917

    PubMed  CAS  Google Scholar 

  • Bargmann CI (2006) Chemosensation in C. elegans. WormBook: 1–29

    Google Scholar 

  • Bargmann CI, Horvitz HR (1991) Chemosensory neurons with overlapping functions direct chemotaxis to multiple chemicals in C. elegans. Neuron 7(5):729–742

    PubMed  CAS  Google Scholar 

  • 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(8):780–785

    PubMed  CAS  Google Scholar 

  • Baugh LR, Demodena J, Sternberg PW (2009) RNA Pol II accumulates at promoters of growth genes during developmental arrest. Science 324(5923):92–94

    PubMed  CAS  Google Scholar 

  • Berman JR, Kenyon C (2006) Germ-cell loss extends C. elegans life span through regulation of DAF-16 by kri-1 and lipophilic-hormone signaling. Cell 124(5):1055–1068

    PubMed  CAS  Google Scholar 

  • 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(4):925–936

    PubMed  CAS  Google Scholar 

  • Blelloch R, Anna-Arriola SS, Gao D, Li Y, Hodgkin J, Kimble J (1999) The gon-1 gene is required for gonadal morphogenesis in Caenorhabditis elegans. Dev Biol 216(1):382–393

    PubMed  CAS  Google Scholar 

  • Braeckman BP, Houthoofd K, Vanfleteren JR (2009) Intermediary metabolism. WormBook: 1–24

    Google Scholar 

  • Branicky R, Desjardins D, Liu J-L, Hekimi S (2010) Lipid transport and signaling in Caenorhabditis elegans. Dev Dyn 239(5):1365–1377

    PubMed  CAS  Google Scholar 

  • Brock TJ, Browse J, Watts JL (2006) Genetic regulation of unsaturated fatty acid composition in C. elegans. PLoS Genet 2(7):e108

    PubMed  Google Scholar 

  • Burnell AM, Houthoofd K, O’Hanlon K, Vanfleteren JR (2005) Alternate metabolism during the dauer stage of the nematode Caenorhabditis elegans. Exp Gerontol 40(11):850–856

    PubMed  CAS  Google Scholar 

  • Butcher RA, Fujita M, Schroeder FC, Clardy J (2007) Small-molecule pheromones that control dauer development in Caenorhabditis elegans. Nat Chem Biol 3(7):420–422

    PubMed  CAS  Google Scholar 

  • 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 USA 105(38):14288–14292

    PubMed  CAS  Google Scholar 

  • Butcher RA, Ragains JR, Li W, Ruvkun G, Clardy J, Mak HY (2009) Biosynthesis of the Caenorhabditis elegans dauer pheromone. Proc Natl Acad Sci USA 106(6):1875–1879

    PubMed  CAS  Google Scholar 

  • Cassada RC, Russell RL (1975) The dauerlarva, a post-embryonic developmental variant of the nematode Caenorhabditis elegans. Dev Biol 46(2):326–342

    PubMed  CAS  Google Scholar 

  • Curtis R, O’Connor G, DiStefano PS (2006) Aging networks in Caenorhabditis elegans: AMP-activated protein kinase (aak-2) links multiple aging and metabolism pathways. Aging cell 5(2):119–126

    PubMed  CAS  Google Scholar 

  • Dalfó D, Michaelson D, Hubbard EJA (2012) Sensory regulation of the C. elegans germline through TGFß-dependent signaling in the niche. Curr Biol 22:712–719

    Google Scholar 

  • Darby C (2005) Interactions with microbial pathogens. WormBook: 1–15

    Google Scholar 

  • Dillin A, Crawford DK, Kenyon C (2002) Timing requirements for insulin/IGF-1 signaling in C. elegans. Science 298(5594):830–834

    PubMed  CAS  Google Scholar 

  • Drummond-Barbosa D (2008) Stem cells, their niches and the systemic environment: an aging network. Genetics 180(4):1787–1797

    PubMed  Google Scholar 

  • Drummond-Barbosa D, Spradling AC (2001) Stem cells and their progeny respond to nutritional changes during Drosophila oogenesis. Dev Biol 231(1):265–278

    PubMed  CAS  Google Scholar 

  • Edison AS (2009) Caenorhabditis elegans pheromones regulate multiple complex behaviors. Curr Opin Neurobiol 19(4):378–388

    PubMed  CAS  Google Scholar 

  • Félix M-A, Braendle C (2010) The natural history of Caenorhabditis elegans. Curr Biol 20(22):R965–R969

    PubMed  Google Scholar 

  • Fielenbach N, Antebi A (2008) C. elegans dauer formation and the molecular basis of plasticity. Genes Dev 22(16):2149–2165

    PubMed  CAS  Google Scholar 

  • Fontana L, Partridge L, Longo VD (2010) Extending healthy life span–from yeast to humans. Science 328(5976):321–326

    PubMed  CAS  Google Scholar 

  • 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(8):773–779

    PubMed  CAS  Google Scholar 

  • Gartner A, Boag PR, Blackwell TK (2008) Germline survival and apoptosis. WormBook: 1–20

    Google Scholar 

  • Golden JW, Riddle DL (1982) A pheromone influences larval development in the nematode Caenorhabditis elegans. Science 218(4572):578–580

    PubMed  CAS  Google Scholar 

  • Golden JW, Riddle DL (1984) The Caenorhabditis elegans dauer larva: developmental effects of pheromone, food, and temperature. Dev Biol 102(2):368–378

    PubMed  CAS  Google Scholar 

  • Goudeau J, Bellemin S, Toselli-Mollereau E, Shamalnasab M, Chen Y, Aguilaniu H (2011) Fatty acid desaturation links germ cell loss to longevity through NHR-80/HNF4 in C. elegans. PLoS Biol 9(3):e1000599

    PubMed  CAS  Google Scholar 

  • Grant B, Hirsh D (1999) Receptor-mediated endocytosis in the Caenorhabditis elegans oocyte. Mol Biol Cell 10(12):4311–4326

    PubMed  CAS  Google Scholar 

  • Greer EL, Brunet A (2009) Different dietary restriction regimens extend lifespan by both independent and overlapping genetic pathways in C. elegans. Aging cell 8(2):113–127

    PubMed  CAS  Google Scholar 

  • Greer EL, Dowlatshahi D, Banko MR, Villen J, Hoang K, Blanchard D, Gygi SP, Brunet A (2007) An AMPK-FOXO pathway mediates longevity induced by a novel method of dietary restriction in C. elegans. Curr Biol 17(19):1646–1656

    PubMed  CAS  Google Scholar 

  • Greer ER, Pérez CL, Van Gilst MR, Lee BH, Ashrafi K (2008) Neural and molecular dissection of a C. elegans sensory circuit that regulates fat and feeding. Cell metabolism 8(2):118–131

    PubMed  CAS  Google Scholar 

  • Greer EL, Maures TJ, Ucar D, Hauswirth AG, Mancini E, Lim JP, Benayoun BA, Shi Y, Brunet A (2011) Transgenerational epigenetic inheritance of longevity in Caenorhabditis elegans. Nature 479(7373):365–371

    PubMed  CAS  Google Scholar 

  • Grishok A, Tabara H, Mello CC (2000) Genetic requirements for inheritance of RNAi in C. elegans. Science 287(5462):2494–2497

    PubMed  CAS  Google Scholar 

  • Gumienny TL, Lambie E, Hartwieg E, Horvitz HR, Hengartner MO (1999) Genetic control of programmed cell death in the Caenorhabditis elegans hermaphrodite germline. Development 126(5):1011–1022

    PubMed  CAS  Google Scholar 

  • Hansen D, Schedl T (2012) Stem cell proliferation versus meiotic fate decision in C. elegans. Advances in Experimental Medicine and Biology 757:71–99. (Chap. 4, this volume) Springer, New York

    Google Scholar 

  • Hansen D, Hubbard EJA, Schedl T (2004) Multi-pathway control of the proliferation versus meiotic development decision in the Caenorhabditis elegans germline. Dev Biol 268(2): 342–357

    PubMed  CAS  Google Scholar 

  • Hardie DG (2011) AMP-activated protein kinase: an energy sensor that regulates all aspects of cell function. Genes Dev 25(18):1895–1908

    PubMed  CAS  Google Scholar 

  • 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(10):2913–2924

    PubMed  CAS  Google Scholar 

  • Hirsh D, Oppenheim D, Klass M (1976) Development of the reproductive system of Caenorhabditis elegans. Dev Biol 49(1):200–219

    PubMed  CAS  Google Scholar 

  • Hodgkin J, Barnes TM (1991) More is not better: brood size and population growth in a self-fertilizing nematode. Proc Roy Soc B 246(1315):19–24

    CAS  Google Scholar 

  • Holt SJ, Riddle DL (2003) SAGE surveys C. elegans carbohydrate metabolism: evidence for an anaerobic shift in the long-lived dauer larva. Mech Ageing Dev 124(7):779–800

    PubMed  CAS  Google Scholar 

  • Honjoh S, Yamamoto T, Uno M, Nishida E (2009) Signalling through RHEB-1 mediates intermittent fasting-induced longevity in C. elegans. Nature 457(7230):726–730

    PubMed  CAS  Google Scholar 

  • Hosono R, Nishimoto S, Kuno S (1989) Alterations of life span in the nematode Caenorhabditis elegans under monoxenic culture conditions. Exp Gerontol 24(3):251–264

    PubMed  CAS  Google Scholar 

  • Houthoofd K (2003) Life extension via dietary restriction is independent of the Ins/IGF-1 signalling pathway in Caenorhabditis elegans. Exp Gerontol 38(9):947–954

    PubMed  CAS  Google Scholar 

  • Houthoofd K, Vanfleteren JR (2006) The longevity effect of dietary restriction in Caenorhabditis elegans. Exp Gerontol 41(10):1026–1031

    PubMed  CAS  Google Scholar 

  • Houthoofd K, Braeckman BP, Lenaerts I, Brys K, De Vreese A, Van Eygen S, Vanfleteren JR (2002a) Axenic growth up-regulates mass-specific metabolic rate, stress resistance, and extends life span in Caenorhabditis elegans. Exp Gerontol 37(12):1371–1378

    PubMed  Google Scholar 

  • Houthoofd K, Braeckman BP, Lenaerts I, Brys K, De Vreese A, Van Eygen S, Vanfleteren JR (2002b) No reduction of metabolic rate in food restricted Caenorhabditis elegans. Exp Gerontol 37(12):1359–1369

    PubMed  Google Scholar 

  • Hsin H, Kenyon C (1999) Signals from the reproductive system regulate the lifespan of C. elegans. Nature 399(6734):362–366

    PubMed  CAS  Google Scholar 

  • 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(2):700–712

    PubMed  CAS  Google Scholar 

  • Hu PJ (2007) Dauer. WormBook: 1–19

    Google Scholar 

  • Hubbard EJ (2011) Insulin and germline proliferation in Caenorhabditis elegans. Vitam Horm 87:61–77

    PubMed  CAS  Google Scholar 

  • Hughes SE, Evason K, Xiong C, Kornfeld K (2007) Genetic and pharmacological factors that influence reproductive aging in nematodes. PLoS Genet 3(2):e25

    PubMed  Google Scholar 

  • Hughes SE, Huang C, Kornfeld K (2011) Identification of mutations that delay somatic or reproductive aging of Caenorhabditis elegans. Genetics 189(1):341–356

    PubMed  CAS  Google Scholar 

  • Jaramillo-Lambert A, Ellefson M, Villeneuve AM, Engebrecht J (2007) Differential timing of S phases, X chromosome replication, and meiotic prophase in the C. elegans germ line. Dev Biol 308(1):206–221

    PubMed  CAS  Google Scholar 

  • Jeong P-Y, Jung M, Yim Y-H, Kim H, Park M, Hong E, Lee W, Kim YH, Kim K, Paik Y-K (2005) Chemical structure and biological activity of the Caenorhabditis elegans dauer-inducing pheromone. Nature 433(7025):541–545

    PubMed  CAS  Google Scholar 

  • 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(16):3897–3906

    PubMed  CAS  Google Scholar 

  • Johnson TE, Mitchell DH, Kline S, Kemal R, Foy J (1984) Arresting development arrests aging in the nematode Caenorhabditis elegans. Mech Ageing Dev 28(1):23–40

    PubMed  CAS  Google Scholar 

  • Jones SJ, Riddle DL, Pouzyrev AT, Velculescu VE, Hillier L, Eddy SR, Stricklin SL, Baillie DL, Waterston R, Marra MA (2001) Changes in gene expression associated with developmental arrest and longevity in Caenorhabditis elegans. Genome Res 11(8):1346–1352

    PubMed  CAS  Google Scholar 

  • Kaeberlein TL, Smith ED, Tsuchiya M, Welton KL, Thomas JH, Fields S, Kennedy BK, Kaeberlein M (2006) Lifespan extension in Caenorhabditis elegans by complete removal of food. Aging cell 5(6):487–494

    PubMed  CAS  Google Scholar 

  • Kalaany NY, Sabatini DM (2009) Tumours with PI3K activation are resistant to dietary restriction. Nature 458(7239):725–731

    PubMed  CAS  Google Scholar 

  • Kang C, Avery L (2009) Systemic regulation of starvation response in Caenorhabditis elegans. Genes Dev 23(1):12–17

    PubMed  CAS  Google Scholar 

  • Kaplan F, Srinivasan J, Mahanti P, Ajredini R, Durak O, Nimalendran R, Sternberg PW, Teal PEA, Schroeder FC, Edison AS, Alborn HT (2011) Ascaroside expression in Caenorhabditis elegans is strongly dependent on diet and developmental stage. PLoS One 6(3):e17804

    PubMed  CAS  Google Scholar 

  • Kenyon CJ (2010) The genetics of ageing. Nature 464(7288):504–512

    PubMed  CAS  Google Scholar 

  • Killian DJ, Hubbard EJA (2004) C. elegans pro-1 activity is required for soma/germline interactions that influence proliferation and differentiation in the germ line. Development 131(6):1267–1278

    PubMed  CAS  Google Scholar 

  • Killian DJ, Hubbard EJA (2005) Caenorhabditis elegans germline patterning requires coordinated development of the somatic gonadal sheath and the germ line. Dev Biol 279(2):322–335

    PubMed  CAS  Google Scholar 

  • Kim S, Spike CA, Greenstein D (2012) Control of oocyte growth and meiotic maturation in C. elegans. Advances in Experimental Medicine and Biology 757:277–320. (Chap. 10, this ­volume) Springer, New York

    Google Scholar 

  • Kimble J, Hirsh D (1979) The postembryonic cell lineages of the hermaphrodite and male gonads in Caenorhabditis elegans. Dev Biol 70(2):396–417

    PubMed  CAS  Google Scholar 

  • Kimble J, Sharrock WJ (1983) Tissue-specific synthesis of yolk proteins in Caenorhabditis elegans. Dev Biol 96(1):189–196

    PubMed  CAS  Google Scholar 

  • Kimble JE, White JG (1981) On the control of germ cell development in Caenorhabditis elegans. Dev Biol 81(2):208–219

    PubMed  CAS  Google Scholar 

  • Kiontke K, Sudhaus W (2006) Ecology of Caenorhabditis species. WormBook: 1–14

    Google Scholar 

  • Klass MR (1977) Aging in the nematode Caenorhabditis elegans: major biological and environmental factors influencing life span. Mech Ageing Dev 6(6):413–429

    PubMed  CAS  Google Scholar 

  • Klass M, Hirsh D (1976) Non-ageing developmental variant of Caenorhabditis elegans. Nature 260(5551):523–525

    PubMed  CAS  Google Scholar 

  • Kleemann GA, Murphy CT (2009) The endocrine regulation of aging in Caenorhabditis elegans. Mol Cell Endocrinol 299(1):51–57

    PubMed  CAS  Google Scholar 

  • Korta DZ, Hubbard EJA (2010) Soma-germline interactions that influence germline proliferation in Caenorhabditis elegans. Dev Dyn 239(5):1449–1459

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • LaFever L, Drummond-Barbosa D (2005) Direct control of germline stem cell division and cyst growth by neural insulin in Drosophila. Science 309(5737):1071–1073

    PubMed  CAS  Google Scholar 

  • 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: 1–10

    Google Scholar 

  • Lakowski B, Hekimi S (1996) Determination of life-span in Caenorhabditis elegans by four clock genes. Science 272(5264):1010–1013

    PubMed  CAS  Google Scholar 

  • Lakowski B, Hekimi S (1998) The genetics of caloric restriction in Caenorhabditis elegans. Proc Natl Acad Sci USA 95(22):13091–13096

    PubMed  CAS  Google Scholar 

  • Landis JN, Murphy CT (2010) Integration of diverse inputs in the regulation of Caenorhabditis elegans DAF-16/FOXO. Dev Dyn 239(5):1405–1412

    PubMed  CAS  Google Scholar 

  • Lapierre LR, Gelino S, Meléndez A, Hansen M (2011) Autophagy and lipid metabolism coordinately modulate life span in germline-less C. elegans. Curr Biol 21(18):1507–1514

    PubMed  CAS  Google Scholar 

  • LeBoeuf B, Guo X, Garcia LR (2011) The effects of transient starvation persist through direct interactions between CaMKII and ether-a-go-go K  +  channels in C. elegans males. Neuroscience 175:1–17

    PubMed  CAS  Google Scholar 

  • Lee GD, Wilson MA, Zhu M, Wolkow CA, de Cabo R, Ingram DK, Zou S (2006) Dietary deprivation extends lifespan in Caenorhabditis elegans. Aging cell 5(6):515–524

    PubMed  CAS  Google Scholar 

  • Liu F, Thatcher JD, Epstein HF (1997) Induction of glyoxylate cycle expression in Caenorhabditis elegans: a fasting response throughout larval development. Biochemistry 36(1):255–260

    PubMed  CAS  Google Scholar 

  • Long X, Spycher C, Han ZS, Rose AM, Müller F, Avruch J (2002) TOR deficiency in C. elegans causes developmental arrest and intestinal atrophy by inhibition of mRNA translation. Curr Biol 12(17):1448–1461

    PubMed  CAS  Google Scholar 

  • Luo S, Kleemann GA, Ashraf JM, Shaw WM, Murphy CT (2010) TGF-β and insulin signaling regulate reproductive aging via oocyte and germline quality maintenance. Cell 143(2):299–312

    PubMed  CAS  Google Scholar 

  • Maciejowski J, Ugel N, Mishra B, Isopi M, Hubbard EJA (2006) Quantitative analysis of germline mitosis in adult C. elegans. Dev Biol 292(1):142–151

    PubMed  CAS  Google Scholar 

  • Macosko EZ, Pokala N, Feinberg EH, Chalasani SH, Butcher RA, Clardy J, Bargmann CI (2009) A hub-and-spoke circuit drives pheromone attraction and social behaviour in C. elegans. Nature 458(7242):1171–1175

    PubMed  CAS  Google Scholar 

  • MacRae TH (2010) Gene expression, metabolic regulation and stress tolerance during diapause. Cell Mol Life Sci 67(14):2405–2424

    PubMed  CAS  Google Scholar 

  • McCarter J, Bartlett B, Dang T, Schedl T (1999) On the control of oocyte meiotic maturation and ovulation in Caenorhabditis elegans. Dev Biol 205(1):111–128

    PubMed  CAS  Google Scholar 

  • McGovern M, Voutev R, Maciejowski J, Corsi AK, Hubbard EJA (2009) A “latent niche” mechanism for tumor initiation. Proc Natl Acad Sci USA 106(28):11617–11622

    PubMed  CAS  Google Scholar 

  • McGrath PT, Xu Y, Ailion M, Garrison JL, Butcher RA, Bargmann CI (2011) Parallel evolution of domesticated Caenorhabditis species targets pheromone receptor genes. Nature 477(7364):321–325

    PubMed  CAS  Google Scholar 

  • McKay RM, McKay JP, Avery L, Graff JM (2003) C. elegans: a model for exploring the genetics of fat storage. Dev Cell 4(1):131–142

    PubMed  CAS  Google Scholar 

  • Meissner B, Boll M, Daniel H, Baumeister R (2004) Deletion of the intestinal peptide transporter affects insulin and TOR signaling in Caenorhabditis elegans. J Biol Chem 279(35):36739–36745

    PubMed  CAS  Google Scholar 

  • Mendenhall AR, Wu D, Park S-K, Cypser JR, Tedesco PM, Link CD, Phillips PC, Johnson TE (2011) Genetic dissection of late-life fertility in Caenorhabditis elegans. J Gerontol A Biol Sci Med Sci 66(8):842–854

    PubMed  Google Scholar 

  • Michaelson D, Korta DZ, Capua Y, Hubbard EJA (2010) Insulin signaling promotes germline proliferation in C. elegans. Development 137(4):671–680

    PubMed  CAS  Google Scholar 

  • Mukhopadhyay A, Tissenbaum HA (2007) Reproduction and longevity: secrets revealed by C. elegans. Trends Cell Biol 17(2):65–71

    PubMed  CAS  Google Scholar 

  • Murakami M, Koga M, Ohshima Y (2001) DAF-7/TGF-beta expression required for the normal larval development in C. elegans is controlled by a presumed guanylyl cyclase DAF-11. Mech Dev 109(1):27–35

    PubMed  CAS  Google Scholar 

  • Nadarajan S, Govindan JA, McGovern M, Hubbard EJA, Greenstein D (2009) MSP and GLP-1/Notch signaling coordinately regulate actomyosin-dependent cytoplasmic streaming and oocyte growth in C. elegans. Development 136(13):2223–2234

    PubMed  CAS  Google Scholar 

  • Narbonne P, Roy R (2006) Inhibition of germline proliferation during C. elegans dauer development requires PTEN, LKB1 and AMPK signalling. Development 133(4):611–619

    PubMed  CAS  Google Scholar 

  • Narbonne P, Roy R (2009) Caenorhabditis elegans dauers need LKB1/AMPK to ration lipid reserves and ensure long-term survival. Nature 457(7226):210–214

    PubMed  CAS  Google Scholar 

  • 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(5):430–435

    PubMed  Google Scholar 

  • Onken B, Driscoll M (2010) Metformin induces a dietary restriction-like state and the oxidative stress response to extend C. elegans Healthspan via AMPK, LKB1, and SKN-1. PLoS One 5(1):e8758

    PubMed  Google Scholar 

  • Panowski SH, Wolff S, Aguilaniu H, Durieux J, Dillin A (2007) PHA-4/Foxa mediates dietrestriction-induced longevity of C. elegans. Nature 447(7144):550–555

    PubMed  CAS  Google Scholar 

  • Pazdernik N, Schedl T (2012) Introduction to germ cell development in C. elegans. Advances in Experimental Medicine and Biology 757:1–16. (Chap. 1, this volume) Springer, New York

    Google Scholar 

  • Pinkston JM, Garigan D, Hansen M, Kenyon C (2006) Mutations that increase the life span of C. elegans inhibit tumor growth. Science 313(5789):971–975

    PubMed  CAS  Google Scholar 

  • Pungaliya C, Srinivasan J, Fox BW, Malik RU, Ludewig AH, Sternberg PW, Schroeder FC (2009) A shortcut to identifying small molecule signals that regulate behavior and development in Caenorhabditis elegans. Proc Natl Acad Sci USA 106(19):7708–7713

    PubMed  CAS  Google Scholar 

  • Rae R, Iatsenko I, Witte H, Sommer RJ (2010) A subset of naturally isolated Bacillus strains show extreme virulence to the free-living nematodes Caenorhabditis elegans and Pristionchus pacificus. Environ Microbiol 12(11):3007–3021

    PubMed  CAS  Google Scholar 

  • Rechavi O, Minevich G, Hobert O (2011) Transgenerational inheritance of an acquired small RNA-based antiviral response in C. elegans. Cell 147(6):1248–1256

    PubMed  CAS  Google Scholar 

  • Reinke SN, Hu X, Sykes BD, Lemire BD (2010) Caenorhabditis elegans diet significantly affects metabolic profile, mitochondrial DNA levels, lifespan and brood size. Mol Genet Metab 100(3):274–282

    PubMed  CAS  Google Scholar 

  • Ren P, Lim CS, Johnsen R, Albert PS, Pilgrim D, Riddle DL (1996) Control of C. elegans larval development by neuronal expression of a TGF-beta homolog. Science 274(5291):1389–1391

    PubMed  CAS  Google Scholar 

  • Riddle DL, Albert PS (1997) Genetic and environmental regulation of Dauer larva development. In: Riddle DL, Blumenthal T, Meyer BJ, Priess JR (eds) C. elegans II, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor (NY)

    Google Scholar 

  • Rous P (1914) The influence of diet on transplanted and spontaneous mouse tumors. J Exp Med 20(5):433–451

    PubMed  CAS  Google Scholar 

  • Savage-Dunn C (2005) TGF-beta signaling. WormBook: 1–12

    Google Scholar 

  • Schackwitz WS, Inoue T, Thomas JH (1996) Chemosensory neurons function in parallel to mediate a pheromone response in C. elegans. Neuron 17(4):719–728

    PubMed  CAS  Google Scholar 

  • Schafer WR (2005) Egg-laying. WormBook: 1–7

    Google Scholar 

  • Schulz TJ, Zarse K, Voigt A, Urban N, Birringer M, Ristow M (2007) Glucose restriction extends Caenorhabditis elegans life span by inducing mitochondrial respiration and increasing oxidative stress. Cell Metab 6(4):280–293

    PubMed  CAS  Google Scholar 

  • Seidel HS, Kimble J (2011) The oogenic germline starvation response in C. elegans. PLoS One 6(12):e28074

    PubMed  CAS  Google Scholar 

  • Shibata Y, Branicky R, Landaverde IO, Hekimi S (2003) Redox regulation of germline and vulval development in Caenorhabditis elegans. Science 302(5651):1779–1782

    PubMed  CAS  Google Scholar 

  • Shtonda BB, Avery L (2006) Dietary choice behavior in Caenorhabditis elegans. J Exp Biol 209(Pt 1):89–102

    PubMed  Google Scholar 

  • Singh K, Chao MY, Somers GA, Komatsu H, Corkins ME, Larkins-Ford J, Tucey T, Dionne HM, Walsh MB, Beaumont EK, Hart DP, Lockery SR, Hart AC (2011) C. elegans Notch signaling regulates adult chemosensory response and larval molting quiescence. Curr Biol 21(10):825–834

    PubMed  CAS  Google Scholar 

  • Srinivasan J, Kaplan F, Ajredini R, Zachariah C, Alborn HT, Teal PEA, Malik RU, Edison AS, Sternberg PW, Schroeder FC (2008) A blend of small molecules regulates both mating and development in Caenorhabditis elegans. Nature 454(7208):1115–1118

    PubMed  CAS  Google Scholar 

  • Szewczyk NJ, Udranszky IA, Kozak E, Sunga J, Kim SK, Jacobson LA, Conley CA (2006) Delayed development and lifespan extension as features of metabolic lifestyle alteration in C. elegans under dietary restriction. J Exp Biol 209(Pt 20):4129–4139

    PubMed  CAS  Google Scholar 

  • Taguchi A, White MF (2008) Insulin-like signaling, nutrient homeostasis, and life span. Annu Rev Physiol 70:191–212

    PubMed  CAS  Google Scholar 

  • Tamai KK, Nishiwaki K (2007) bHLH transcription factors regulate organ morphogenesis via activation of an ADAMTS protease in C. elegans. Dev Biol 308(2):562–571

    PubMed  CAS  Google Scholar 

  • Tan KT, Luo SC, Ho WZ, Lee YH (2011) Insulin/IGF-1 receptor signaling enhances biosynthetic activity and fat mobilization in the initial phase of starvation in adult male C. elegans. Cell Metab 14(3):390–402

    PubMed  CAS  Google Scholar 

  • Tannenbaum A, Silverstone H (1953) Nutrition in relation to cancer. Adv Cancer Res 1:451–501

    PubMed  CAS  Google Scholar 

  • Trent C, Tsuing N, Horvitz HR (1983) Egg-laying defective mutants of the nematode Caenorhabditis elegans. Genetics 104(4):619–647

    PubMed  CAS  Google Scholar 

  • 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(2):e53

    PubMed  Google Scholar 

  • Vowels JJ, Thomas JH (1992) Genetic analysis of chemosensory control of dauer formation in Caenorhabditis elegans. Genetics 130(1):105–123

    PubMed  CAS  Google Scholar 

  • Wadsworth WG, Riddle DL (1989) Developmental regulation of energy metabolism in Caenorhabditis elegans. Dev Biol 132(1):167–173

    PubMed  CAS  Google Scholar 

  • Walker AK, Yang F, Jiang K, Ji J-Y, Watts JL, Purushotham A, Boss O, Hirsch ML, Ribich S, Smith JJ, Israelian K, Westphal CH, Rodgers JT, Shioda T, Elson SL, Mulligan P, Najafi-Shoushtari H, Black JC, Thakur JK, Kadyk LC, Whetstine JR, Mostoslavsky R, Puigserver P, Li X, Dyson NJ, Hart AC, Näär AM (2010) Conserved role of SIRT1 orthologs in fasting-dependent inhibition of the lipid/cholesterol regulator SREBP. Genes Dev 24(13):1403–1417

    PubMed  CAS  Google Scholar 

  • Wang J, Kim SK (2003) Global analysis of dauer gene expression in Caenorhabditis elegans. Development 130(8):1621–1634

    PubMed  CAS  Google Scholar 

  • Wang MC, O’Rourke EJ, Ruvkun G (2008) Fat metabolism links germline stem cells and longevity in C. elegans. Science 322(5903):957–960

    PubMed  CAS  Google Scholar 

  • Watts JL (2009) Fat synthesis and adiposity regulation in Caenorhabditis elegans. Trends Endocrinol Metab 20(2):58–65

    PubMed  CAS  Google Scholar 

  • Wolke U, Jezuit EA, Priess JR (2007) Actin-dependent cytoplasmic streaming in C. elegans oogenesis. Development 134(12):2227–2236

    PubMed  CAS  Google Scholar 

  • Wood WB, Hecht R, Carr S, Vanderslice R, Wolf N, Hirsh D (1980) Parental effects and phenotypic characterization of mutations that affect early development in Caenorhabditis elegans. Dev Biol 74(2):446–469

    PubMed  CAS  Google Scholar 

  • Wood JG, Rogina B, Lavu S, Howitz K, Helfand SL, Tatar M, Sinclair D (2004) Sirtuin activators mimic caloric restriction and delay ageing in metazoans. Nature 430(7000):686–689

    PubMed  CAS  Google Scholar 

  • Wullschleger S, Loewith R, Hall MN (2006) TOR signaling in growth and metabolism. Cell 124(3):471–484

    PubMed  CAS  Google Scholar 

  • Yamawaki TM, Berman JR, Suchanek-Kavipurapu M, McCormick M, Maria Gaglia M, Lee S-J, Kenyon C (2010) The somatic reproductive tissues of C. elegans promote longevity through steroid hormone signaling. PLoS Biol 8 (8)

    Google Scholar 

  • You Y-j, Kim J, Cobb M, Avery L (2006) Starvation activates MAP kinase through the muscarinic acetylcholine pathway in Caenorhabditis elegans pharynx. Cell Metab 3(4):237–245

    PubMed  CAS  Google Scholar 

  • You Y-j, Kim J, Raizen DM, Avery L (2008) Insulin, cGMP, and TGF-beta signals regulate food intake and quiescence in C. elegans: a model for satiety. Cell Metab 7(3):249–257

    PubMed  CAS  Google Scholar 

  • Zhang X, Zabinsky R, Teng Y, Cui M, Han M (2011) microRNAs play critical roles in the survival and recovery of Caenorhabditis elegans from starvation-induced L1 diapause. Proc Natl Acad Sci USA 108(44):17997–18002

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We especially thank Tim Schedl for discussions that catalyzed many of the ideas presented here. In addition we thank Barth Grant, Jennifer Watts, Kerry Kornfeld, Marie-Anne Félix, and David Greenstein for comments on the manuscript. We also thank members of the Hubbard lab for discussion, and National Institutes of Health grants R01GM061706, R03HD066005, T32GM07308, F30DK089697 for support.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to E. Jane Albert Hubbard .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2013 Springer Science+Business Media New York

About this chapter

Cite this chapter

Hubbard, E.J.A., Korta, D.Z., Dalfó, D. (2013). Physiological Control of Germline Development. In: Schedl, T. (eds) Germ Cell Development in C. elegans. Advances in Experimental Medicine and Biology, vol 757. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-4015-4_5

Download citation

Publish with us

Policies and ethics