Skip to main content
SpringerLink
Log in

Stem Cells and Stem Cell Niches in Tissue Homeostasis: Lessons from the Expanding Stem Cell Populations of Drosophila

  • Chapter
Regulatory Networks in Stem Cells

Part of the book series: Stem Cell Biology and Regenerative Medicine ((STEMCELL))

  • 1310 Accesses

Abstract

New stem cell populations and their niches have been discovered continuously in Drosophila, changing the view that the adult Drosophila body consists primarily of post-mitotic organs and is not suited for the study of dynamic tissue homeostasis. With a century of genetics history as well as many sophisticated tools for the genetic analysis of cellular and developmental biology, Drosophila has now emerged as an impressive model system in which to study stem cell biology in great detail.

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 189.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 249.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 329.99
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

  1. Clarke MF, Fuller M. Stem cells and cancer: two faces of eve. Cell. 2006;124(6):1111–5.

    Article  PubMed  CAS  Google Scholar 

  2. Spradling A, Drummond-Barbosa D, Kai T. Stem cells find their niche. Nature. 2001;414(6859):98–104.

    Article  PubMed  CAS  Google Scholar 

  3. Fuchs E, Tumbar T, Guasch G. Socializing with the neighbors: stem cells and their niche. Cell. 2004;116(6):769–78.

    Article  PubMed  CAS  Google Scholar 

  4. Kirkwood TB. Understanding the odd science of aging. Cell. 2005;120(4):437–47.

    Article  PubMed  CAS  Google Scholar 

  5. Campisi J, d’Adda di Fagagna F. Cellular senescence: when bad things happen to good cells. Nat Rev Mol Cell Biol. 2007;8(9):729–40.

    Article  PubMed  CAS  Google Scholar 

  6. Molofsky AV, Slutsky SG, Joseph NM, et al. Increasing p16INK4a expression decreases forebrain progenitors and neurogenesis during ageing. Nature. 2006;443(7110):448–52.

    Article  PubMed  CAS  Google Scholar 

  7. Janzen V, Forkert R, Fleming HE, et al. Stem-cell ageing modified by the cyclin-dependent kinase inhibitor p16INK4a. Nature. 2006;443(7110):421–6.

    PubMed  CAS  Google Scholar 

  8. Krishnamurthy J, Ramsey MR, Ligon KL, et al. p16INK4a induces an age-dependent decline in islet regenerative potential. Nature. 2006;443(7110):453–7.

    Article  PubMed  CAS  Google Scholar 

  9. Morrison SJ, Kimble J. Asymmetric and symmetric stem-cell divisions in development and cancer. Nature. 2006;441(7097): 1068–74.

    Article  PubMed  CAS  Google Scholar 

  10. Moore KA, Lemischka IR. Stem cells and their niches. Science. 2006;311(5769):1880–5.

    Article  PubMed  CAS  Google Scholar 

  11. Song X, Zhu CH, Doan C, Xie T. Germline stem cells anchored by adherens junctions in the Drosophila ovary niches. Science. 2002;296(5574):1855–7.

    Article  PubMed  CAS  Google Scholar 

  12. Chen D, McKearin D. Dpp signaling silences bam transcription directly to establish asymmetric divisions of germline stem cells. Curr Biol. 2003;13(20):1786–91.

    Article  PubMed  CAS  Google Scholar 

  13. Chen D, McKearin DM. A discrete transcriptional silencer in the bam gene determines asymmetric division of the Drosophila germline stem cell. Development. 2003;130(6):1159–70.

    Article  PubMed  CAS  Google Scholar 

  14. Kai T, Spradling A. Differentiating germ cells can revert into functional stem cells in Drosophila melanogaster ovaries. Nature. 2004;428(6982):564–9.

    Article  PubMed  CAS  Google Scholar 

  15. Brawley C, Matunis E. Regeneration of male germline stem cells by spermatogonial dedifferentiation in vivo. Science. 2004;304(5675):1331–4.

    Article  PubMed  CAS  Google Scholar 

  16. Decotto E, Spradling AC. The Drosophila ovarian and testis stem cell niches: similar somatic stem cells and signals. Dev Cell. 2005;9(4):501–10.

    Article  PubMed  CAS  Google Scholar 

  17. Margolis J, Spradling A. Identification and behavior of epithelial stem cells in the Drosophila ovary. Development. 1995;121(11): 3797–807.

    PubMed  CAS  Google Scholar 

  18. Forbes AJ, Lin H, Ingham PW, Spradling AC. Hedgehog is required for the proliferation and specification of ovarian somatic cells prior to egg chamber formation in Drosophila. Development. 1996;122(4):1125–35.

    PubMed  CAS  Google Scholar 

  19. Song X, Xie T. DE-cadherin-mediated cell adhesion is essential for maintaining somatic stem cells in the Drosophila ovary. Proc Natl Acad Sci U S A. 2002; 99(23):14813–8.

    Article  PubMed  CAS  Google Scholar 

  20. Nystul T, Spradling A. An Epithelial Nihce in the Drosophila ovary undergoes long-range stem cell replacement. Cell Stem Cell. 2007;1(3):277–85.

    Article  PubMed  CAS  Google Scholar 

  21. Fuller MT. Spermatogenesis. In: Bate M, Martinez-Arias, A. editors. The development of drosophila melanogaster. New York: Cold Spring Harbor Laboratory Press; 1993. pp. 71–147.

    Google Scholar 

  22. Tulina N, Matunis E. Control of stem cell self-renewal in Drosophila spermatogenesis by JAK-STAT signaling. Science. 2001;294(5551):2546–9.

    Article  PubMed  CAS  Google Scholar 

  23. Kiger AA, Jones DL, Schulz C, Rogers MB, Fuller MT. Stem cell self-renewal specified by JAK-STAT activation in response to a support cell cue. Science. 2001;294(5551):2542–5.

    Article  PubMed  CAS  Google Scholar 

  24. Yamashita YM, Jones DL, Fuller MT. Orientation of asymmetric stem cell division by the APC tumor suppressor and centrosome. Science. 2003;301(5639):1547–50.

    Article  PubMed  CAS  Google Scholar 

  25. Harrison DA, McCoon PE, Binari R, Gilman M, Perrimon N. Drosophila unpaired encodes a secreted protein that activates the JAK signaling pathway. Genes Dev. 1998;12(20): 3252–63.

    Article  PubMed  CAS  Google Scholar 

  26. Schulz C, Kiger AA, Tazuke SI, et al. A misexpression screen reveals effects of bag-of-marbles and TGFbeta class signaling on the Drosophila male germ-line stem cell lineage. Genetics. 2004;167(2):707–23.

    Article  PubMed  CAS  Google Scholar 

  27. Kawase E, Wong MD, Ding BC, Xie T. Gbb/Bmp signaling is essential for maintaining germline stem cells and for repressing bam transcription in the Drosophila testis. Development. 2004;131(6):1365–75.

    Article  PubMed  CAS  Google Scholar 

  28. Shivdasani AA, Ingham PW. Regulation of stem cell maintenance and transit amplifying cell proliferation by tgf-Beta signaling in Drosophila spermatogenesis. Curr Biol. 2003;13(23): 2065–72.

    Article  PubMed  CAS  Google Scholar 

  29. Kiger AA, White-Cooper H, Fuller MT. Somatic support cells restrict germline stem cell self-renewal and promote differentiation. Nature. 2000;407(6805):750–4.

    Article  PubMed  CAS  Google Scholar 

  30. Schulz C, Wood CG, Jones DL, Tazuke SI, Fuller MT. Signaling from germ cells mediated by the rhomboid homolog stet organizes encapsulation by somatic support cells. Development. 2002;129(19):4523–34.

    PubMed  CAS  Google Scholar 

  31. Sarkar A, Parikh N, Hearn SA, Fuller MT, Tazuke SI, Schulz C. Antagonistic roles of Rac and Rho in organizing the germ cell microenvironment. Curr Biol. 2007;17(14):1253–8.

    Article  PubMed  CAS  Google Scholar 

  32. Evans CJ, Hartenstein V, Banerjee U. Thicker than blood: conserved mechanisms in Drosophila and vertebrate hematopoiesis. Dev Cell. 2003;5(5):673–90.

    Article  PubMed  CAS  Google Scholar 

  33. Lebestky T, Chang T, Hartenstein V, Banerjee U. Specification of Drosophila hematopoietic lineage by conserved transcription factors. Science. 2000;288(5463):146–9.

    Article  PubMed  CAS  Google Scholar 

  34. Lebestky T, Jung SH, Banerjee U. A Serrate-expressing signaling center controls Drosophila hematopoiesis. Genes Dev. 2003;17(3):348–53.

    Article  PubMed  CAS  Google Scholar 

  35. Mandal L, Martinez-Agosto JA, Evans CJ, Hartenstein V, Banerjee U. A Hedgehog- and Antennapedia-dependent niche maintains Drosophila haematopoietic precursors. Nature. 2007; 446(7133):320–4.

    Article  PubMed  CAS  Google Scholar 

  36. Krzemien J, Dubois L, Makki R, Meister M, Vincent A, Crozatier M. Control of blood cell homeostasis in Drosophila larvae by the posterior signalling centre. Nature. 2007;446(7133):325–8.

    Article  PubMed  CAS  Google Scholar 

  37. Yu F, Kuo CT, Jan YN. Drosophila neuroblast asymmetric cell division: recent advances and implications for stem cell biology. Neuron. 2006;51(1):13–20.

    Article  PubMed  CAS  Google Scholar 

  38. Lee CY, Andersen RO, Cabernard C, et al. Drosophila Aurora-A kinase inhibits neuroblast self-renewal by regulating aPKC/Numb cortical polarity and spindle orientation. Genes Dev. 2006;20(24):3464–74.

    Article  PubMed  CAS  Google Scholar 

  39. Berdnik D, Torok T, Gonzalez-Gaitan M, Knoblich JA. The endocytic protein alpha-Adaptin is required for numb-mediated asymmetric cell division in Drosophila. Dev Cell. 2002;3(2):221–31.

    Article  PubMed  CAS  Google Scholar 

  40. Micchelli CA, Perrimon N. Evidence that stem cells reside in the adult Drosophila midgut epithelium. Nature. 2006;439(7075): 475–9.

    Article  PubMed  CAS  Google Scholar 

  41. Ohlstein B, Spradling A. The adult Drosophila posterior midgut is maintained by pluripotent stem cells. Nature. 2006;439(7075): 470–4.

    Article  PubMed  CAS  Google Scholar 

  42. Ohlstein B, Spradling A. Multipotent Drosophila intestinal stem cells specify daughter cell fates by differential notch signaling. Science. 2007;315(5814):988–92.

    Article  PubMed  CAS  Google Scholar 

  43. Singh SR, Liu W, Hou SX. The adult Drosophila malpighian tubules are maintained by multipotent stem cells. Cell Stem Cell. 2007;1(2):191–203.

    Article  PubMed  CAS  Google Scholar 

  44. Yamashita YM, Mahowald AP, Perlin JR, Fuller MT. Asymmetric inheritance of mother versus daughter centrosome in stem cell division. Science. 2007;315(5811):518–21.

    Article  PubMed  CAS  Google Scholar 

  45. Lambert JD, Nagy LM. Asymmetric inheritance of centrosomally localized mRNAs during embryonic cleavages. Nature. 2002;420(6916):682–6.

    Article  PubMed  CAS  Google Scholar 

  46. Bienz M. Spindles cotton on to junctions, APC and EB1. Nat Cell Biol. 2001;3(3):E67–8.

    Article  PubMed  CAS  Google Scholar 

  47. Rusan NM, Peifer M. A role for a novel centrosome cycle in asymmetric cell division. J Cell Biol. 2007;177(1):13–20.

    Article  PubMed  CAS  Google Scholar 

  48. Rebollo E, Sampaio P, Januschke J, Llamazares S, Varmark H, Gonzalez C. Functionally unequal centrosomes drive spindle orientation in asymmetrically dividing Drosophila neural stem cells. Dev Cell. 2007;12(3):467–74.

    Article  PubMed  CAS  Google Scholar 

  49. Kaltschmidt JA, Davidson CM, Brown NH, Brand AH. Rotation and asymmetry of the mitotic spindle direct asymmetric cell division in the developing central nervous system. Nat Cell Biol. 2000;2(1):7–12.

    Article  PubMed  CAS  Google Scholar 

  50. Siegrist SE, Doe CQ. Extrinsic cues orient the cell division axis in Drosophila embryonic neuroblasts. Development. 2006;133(3):529–36.

    Article  PubMed  CAS  Google Scholar 

  51. Lechler T, Fuchs E. Asymmetric cell divisions promote stratification and differentiation of mammalian skin. Nature. 2005;437(7056):275–80.

    Article  PubMed  CAS  Google Scholar 

  52. Deng W, Lin H. Spectrosomes and fusomes anchor mitotic spindles during asymmetric germ cell divisions and facilitate the formation of a polarized microtubule array for oocyte specification in Drosophila. Dev Biol. 1997;189(1):79–94.

    Article  PubMed  CAS  Google Scholar 

  53. Stevens NR, Raposo AA, Basto R, St Johnston D, Raff JW. From stem cell to embryo without centrioles. Curr Biol. 2007;17(17):1498–503.

    Article  PubMed  CAS  Google Scholar 

  54. Xie T, Spradling AC. A niche maintaining germ line stem cells in the Drosophila ovary. Science. 2000;290(5490):328–30.

    Article  PubMed  CAS  Google Scholar 

  55. Helfand SL, Rogina B. Molecular genetics of aging in the fly: is this the end of the beginning? Bioessays. 2003;25(2):134–41.

    Article  PubMed  CAS  Google Scholar 

  56. Boyle M, Wong C, Rocha M, Jones DL. Decline in self-renewal factors contributes to aging of the stem cell niche in the Drosophila testis. Cell Stem Cell. 2007;1(4):470–8.

    Article  PubMed  CAS  Google Scholar 

  57. Pan L, Chen S, Weng C, et al. Stem cell aging is controlled both intrinsically and extrinsically in the Drosophila ovary. Cell Stem Cell. 2007;1(4):458–69.

    Article  PubMed  CAS  Google Scholar 

  58. Wallenfang MR, Nayak R, DiNardo S. Dynamics of the male germline stem cell population during aging of Drosophila melanogaster. Aging Cell. 2006;5(4):297–304.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Center for Stem Cell Biology, Life Sciences Institute and Department of Cell and Developmental Biology, University of Michigan, Ann Arbor, 210 Washtenaw Avenue, Rm 5403, Ann Arbor, MI 48104

    Yukiko M. Yamashita

Authors
  1. Yukiko M. Yamashita
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yukiko M. Yamashita .

Editor information

Editors and Affiliations

  1. Memorial Sloan-Kettering Cancer Center, New York, NY, USA

    Vinagolu K. Rajasekhar MSc, MPhil, PhD

  2. Invitrogen Corporation, Frederick, MD, USA

    Mohan C. Vemuri Ph.D.

Rights and permissions

Reprints and permissions

Copyright information

© 2009 Humana Press, a part of Springer Science+Business Media, LLC, a part of Springer Science+Business Media, LLC

About this chapter

Cite this chapter

Yamashita, Y.M. (2009). Stem Cells and Stem Cell Niches in Tissue Homeostasis: Lessons from the Expanding Stem Cell Populations of Drosophila . In: Rajasekhar, V.K., Vemuri, M.C. (eds) Regulatory Networks in Stem Cells. Stem Cell Biology and Regenerative Medicine. Humana Press. https://doi.org/10.1007/978-1-60327-227-8_13

Download citation

Publish with us

Policies and ethics

Search

Navigation