Why adult stem cell functionality declines with age? Studies from the fruit fly drosophila melanogaster model organism

Current Genomics

Volumn 15, Issue 3, 2014, Pages 231-236

  Gonen, Oren ^a   Toledano, Hila ^a  

^a UNIVERSITY OF HAIFA   (Israel)

Author keywords

Adult stem cells; Aging; Drosophila; Niche

Indexed keywords

BONE MORPHOGENETIC PROTEIN; REACTIVE OXYGEN METABOLITE; STRESS ACTIVATED PROTEIN KINASE; SUPEROXIDE DISMUTASE; TRANSCRIPTION FACTOR FOXO; UVOMORULIN; VASCULOTROPIN;

ADULT STEM CELL; AGING; ARTICLE; CELL DIFFERENTIATION; CELL DIVISION; CELL FATE; CELL FUNCTION; CELL LINEAGE; CELL MIGRATION; CELL PROLIFERATION; CELL REGENERATION; CELL RENEWAL; DAUGHTER CELL; DROSOPHILA MELANOGASTER; ENTEROBLAST CELL; ENTEROENDOCRINE CELL; GERMLINE STEM CELL; INTESTINAL STEM CELL; NONHUMAN; OXIDATIVE STRESS; PHENOTYPE; SIGNAL TRANSDUCTION; STEM CELL NICHE;

DROSOPHILA MELANOGASTER;

EID: 84922323035     PISSN: 13892029     EISSN: 18755488     Source Type: Journal    
DOI: 10.2174/1389202915666140421213243     Document Type: Article

References (60)

1. [1] Morrison, S.J.; Spradling, A.C. Stem cells and niches: mechanisms that promote stem cell maintenance throughout life. Cell, 2008, 132(4), 598-611.
2. [2] Jones, D.L.; Rando, T.A. Emerging models and paradigms for stem cell ageing. Nat. Cell. Biol., 2011, 13(5), 506-12.
3. [3] Rando, T.A. Stem cells, ageing and the quest for immortality. Nature, 2006, 441, (7097), 1080-6.
4. [4] Signer, R.A.; Morrison, S.J. Mechanisms that regulate stem cell aging and life span. Cell Stem Cell, 2013, 12, (2), 152-65.
5. [5] Jones, D.L.; Wagers, A.J. No place like home: anatomy and function of the stem cell niche. Nat. Rev. Mol. Cell Biol,. 2008, 9(1), 11-21.
6. [6] Shim, J.; Gururaja-Rao, S.; Banerjee, U. Nutritional regulation of stem and progenitor cells in Drosophila. Development, 2013, 140 (23), 4647-56.
7. [7] Villeda, S.A.; Luo, J.; Mosher, K.I.; Zou, B.; Britschgi, M.; Bieri, G.; Stan, T.M.; Fainberg, N.; Ding, Z.; Eggel, A.; Lucin, K.M.; Czirr, E.; Park, J.S.; Couillard-Despres, S.; Aigner, L.; Li, G.; Peskind, E.R.; Kaye, J.A.; Quinn, J.F.; Galasko, D.R.; Xie, X.S.; Rando, T.A.; Wyss-Coray, T. The ageing systemic milieu negatively regulates neurogenesis and cognitive function. Nature, 2011, 477(7362), 90-4.
8. [8] Homem, C.C.; Knoblich, J.A. Drosophila neuroblasts: a model for stem cell biology. Development, 2012, 139(23), 4297-310.
9. [9] Shim, J.; Mukherjee, T.; Banerjee, U. Direct sensing of systemic and nutritional signals by haematopoietic progenitors in Drosophila. Nat Cell Biol., 2012, 14(4), 394-400.
10. [10] Jiang, H.; Edgar, B.A. Intestinal stem cells in the adult Drosophila midgut. Exp. Cell Res., 2011, 317(19), 2780-8.
11. [11] Singh, S.R.; Liu, W.; Hou, S.X. The adult Drosophila malpighian tubules are maintained by multipotent stem cells. Cell Stem Cell 2007, 1(2), 191-203.
12. [12] Fuller, M.T.; Spradling, A.C. Male and female Drosophila germline stem cells: two versions of immortality. Science, 2007, 316(5823), 402-4.
13. [13] Spradling, A.; Fuller, M.T.; Braun, R.E.; Yoshida, S. Germline stem cells. Cold Spring Harb. Perspect Biol., 2011, 3(11), a002642.
14. [14] Kiger, A.A.; Jones, D.L.; Schulz, C.; Rogers, M.B.; Fuller, M.T. Stem cell self-renewal specified by JAK-STAT activation in response to a support cell cue. Science, 2001, 294(5551), 2542-5.
15. [15] Leatherman, J.L.; Dinardo, S. Germline self-renewal requires cyst stem cells and stat regulates niche adhesion in Drosophila testes. Nat. Cell Biol., 2010, 12(8), 806-11.
16. [16] Tulina, N.; Matunis, E. Control of stem cell self-renewal in Drosophila spermatogenesis by JAK-STAT signaling. Science, 2001, 294(5551), 2546-9.
17. [17] Amoyel, M.; Sanny, J.; Burel, M.; Bach, E.A. Hedgehog is required for CySC self-renewal but does not contribute to the GSC niche in the Drosophila testis. Development, 2013, 140(1), 56-65.
18. [18] Insco, M.L.; Leon, A.; Tam, C.H.; McKearin, D.M.; Fuller, M.T. Accumulation of a differentiation regulator specifies transit amplifying division number in an adult stem cell lineage. Proc. Natl. Acad. Sci. U S A., 2009, 106(52), 22311-6.
19. [19] Wallenfang, M.R.; Nayak, R.; DiNardo, S. Dynamics of the male germline stem cell population during aging of Drosophila melanogaster. Aging Cell, 2006, 5(4), 297-304.
20. [20] Brawley, C.; Matunis, E. Regeneration of male germline stem cells by spermatogonial dedifferentiation in vivo. Science, 2004, 304(5675), 1331-4.
21. [21] Cheng, J.; Turkel, N.; Hemati, N.; Fuller, M.T.; Hunt, A.J.; Yamashita, Y.M. Centrosome misorientation reduces stem cell division during ageing. Nature, 2008, 456(7222), 599-604.
22. [22] Sheng, X.R.; Matunis, E. Live imaging of the Drosophila sper matogonial stem cell niche reveals novel mechanisms regulating germline stem cell output. Development, 2011, 138(16), 3367-76.
23. [23] Boyle, M.; Wong, C.; Rocha, M.; Jones, D.L. Decline in selfrenewal factors contributes to aging of the stem cell niche in the Drosophila testis. Cell Stem Cell, 2007, 1(4), 470-8.
24. [24] Yamashita, Y.M.; Jones, D.L.; Fuller, M.T. Orientation of asymmetric stem cell division by the APC tumor suppressor and centrosome. Science, 2003, 301(5639), 1547-50.
25. [25] Yamashita, Y.M.; Mahowald, A.P.; Perlin, J.R.; Fuller, M.T. Asymmetric inheritance of mother versus daughter centrosome in stem cell division. Science, 2007, 315(5811), 518-21.
26. [26] Sheng, X.R.; Brawley, C.M.; Matunis, E.L. Dedifferentiating spermatogonia outcompete somatic stem cells for niche occupancy in the Drosophila testis. Cell Stem Cell, 2009, 5(2), 191-203.
27. [27] Inaba, M.; Yuan, H.; Yamashita, Y.M. String (Cdc25) regulates stem cell maintenance, proliferation and aging in Drosophila testis. Development, 2011, 138(23), 5079-86.
28. [28] Ambros, V. MicroRNAs and developmental timing. Curr. Opin. Genet. Dev., 2011, 21(4), 511-7.
29. [29] Sempere, L.F.; Dubrovsky, E.B.; Dubrovskaya, V.A.; Berger, E. M.; Ambros, V. The expression of the let-7 small regulatory RNA is controlled by ecdysone during metamorphosis in Drosophila melanogaster. Dev. Biol., 2002, 244(1), 170-9.
30. [30] Toledano, H.; D'Alterio, C.; Czech, B.; Levine, E.; Jones, D.L. The let-7-Imp axis regulates ageing of the Drosophila testis stem-cell niche. Nature, 2012, 485(7400), 605-10.
31. [31] Gonczy, P.; Matunis, E.; DiNardo, S. bag-of-marbles and benign gonial cell neoplasm act in the germline to restrict proliferation during Drosophila spermatogenesis. Development, 1997, 124(21), 4361-71.
32. [32] Le Bras, S.; Van Doren, M. Development of the male germline stem cell niche in Drosophila. Dev. Biol., 2006, 294(1), 92-103.
33. [33] Gilboa, L.; Lehmann, R. How different is Venus from Mars? The genetics of germ-line stem cells in Drosophila females and males. Development, 2004, 131(20), 4895-905.
34. [34] Morris, L.X.; Spradling, A.C. Long-term live imaging provides new insight into stem cell regulation and germline-soma coordination in the Drosophila ovary. Development, 2011, 138(11), 2207-15.
35. [35] Kai, T.; Spradling, A. Differentiating germ cells can revert into functional stem cells in Drosophila melanogaster ovaries. Nature, 2004, 428(6982), 564-9.
36. [36] 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.
37. [37] Song, X.; Zhu, C.H.; Doan, C.; Xie, T. Germline stem cells anchored by adherens junctions in the Drosophila ovary niches. Science, 2002, 296(5574), 1855-7.
38. [38] 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.
39. [39] Nystul, T.; Spradling, A. Regulation of epithelial stem cell replacement and follicle formation in the Drosophila ovary. Genetics, 2010, 184(2), 503-15.
40. [40] Pan, L.; Chen, S.; Weng, C.; Call, G.; Zhu, D.; Tang, H.; Zhang, N.; Xie, T. Stem cell aging is controlled both intrinsically and extrinsically in the Drosophila ovary. Cell Stem Cell, 2007, 1(4), 458-69.
41. [41] Zhao, R.; Xuan, Y.; Li, X.; Xi, R. Age-related changes of germline stem cell activity, niche signaling activity and egg production in Drosophila. Aging Cell, 2008, 7(3), 344-54.
42. [42] Hsin, H.; Kenyon, C. Signals from the reproductive system regulate the lifespan of C. elegans. Nature, 1999, 399(6734), 362-6.
43. [43] Arantes-Oliveira, N.; Apfeld, J.; Dillin, A.; Kenyon, C. Regulation of life-span by germ-line stem cells in Caenorhabditis elegans. Science, 2002, 295(5554), 502-5.
44. [44] Flatt, T.; Min, K.J.; D'Alterio, C.; Villa-Cuesta, E.; Cumbers, J.; Lehmann, R.; Jones, D.L.; Tatar, M. Drosophila germ-line modulation of insulin signaling and lifespan. Proc. Natl. Acad. Sci. U S A., 2008, 105(17), 6368-73.
45. [45] Barnes, A.I.; Boone, J.M.; Jacobson, J.; Partridge, L.; Chapman, T. No extension of lifespan by ablation of germ line in Drosophila. Proc. Biol. Sci., 2006, 273(1589), 939-47.
46. [46] Buchon, N.; Osman, D.; David, F.P.; Fang, H.Y.; Boquete, J.P.; Deplancke, B.; Lemaitre, B. Morphological and molecular characterization of adult midgut compartmentalization in Drosophila. Cell Rep., 2013, 3(5), 1725-38.
47. [47] Ohlstein, B.; Spradling, A. The adult Drosophila posterior midgut is maintained by pluripotent stem cells. Nature, 2006, 439(7075), 470-4.
48. [48] Ohlstein, B.; Spradling, A. Multipotent Drosophila intestinal stem cells specify daughter cell fates by differential notch signaling. Science, 2007, 315(5814), 988-92.
49. [49] Micchelli, C.A.; Perrimon, N. Evidence that stem cells reside in theadult Drosophila midgut epithelium. Nature, 2006, 439(7075), 475-9.
50. [50] Biteau, B.; Hochmuth, C.E.; Jasper, H. JNK activity in somatic stem cells causes loss of tissue homeostasis in the aging Drosophila gut. Cell Stem Cell, 2008, 3(4), 442-55.
51. [51] Biteau, B.; Karpac, J.; Supoyo, S.; Degennaro, M.; Lehmann, R.; Jasper, H. Lifespan extension by preserving proliferative homeostasis in Drosophila. PLoS Genet., 2010, 6(10), e1001159.
52. [52] Choi, N.H.; Kim, J.G.; Yang, D.J.; Kim, Y.S.; Yoo, M.A. Age related changes in Drosophila midgut are associated with PVF2, a PDGF/VEGF-like growth factor. Aging Cell, 2008, 7(3), 318-34.
53. [53] Choi, Y.J.; Hwang, M.S.; Park, J.S.; Bae, S.K.; Kim, Y.S.; Yoo, M. A. Age-related upregulation of Drosophila caudal gene via NFkappaB in the adult posterior midgut. Biochim. Biophys. Acta., 2008, 1780(10), 1093-100.
54. [54] Hur, J.H.; Bahadorani, S.; Graniel, J.; Koehler, C.L.; Ulgherait, M.; Rera, M.; Jones, D.L.; Walker, D.W. Increased longevity mediated by yeast NDI1 expression in Drosophila intestinal stem and progenitor cells. Aging (Albany NY), 2013, 5(9), 662-81.
55. [55] Rera, M.; Bahadorani, S.; Cho, J.; Koehler, C.L.; Ulgherait, M.; Hur, J.H.; Ansari, W.S.; Lo, T. Jr.; Jones, D.L.; Walker, D.W. Modulation of longevity and tissue homeostasis by the Drosophila PGC-1 homolog. Cell Metab., 2011, 14(5), 623-34.
56. [56] Ren, C.; Webster, P.; Finkel, S.E.; Tower, J. Increased internal and external bacterial load during Drosophila aging without life-span trade-off. Cell Metab., 2007, 6(2), 144-52.
57. [57] Ha, E.M.; Lee, K.A.; Seo, Y.Y.; Kim, S.H.; Lim, J.H.; Oh, B.H.; Kim, J.; Lee, W.J. Coordination of multiple dual oxidaseregulatory pathways in responses to commensal and infectious microbes in drosophila gut. Nat. Immunol., 2009, 10(9), 949-57.
58. [58] Buchon, N.; Broderick, N.A.; Chakrabarti, S.; Lemaitre, B. Invasive and indigenous microbiota impact intestinal stem cell activity through multiple pathways in Drosophila. Genes Dev., 2009, 23(19), 2333-44.
59. [59] Guo, L.; Karpac, J.; Tran, S.L.; Jasper, H. PGRP-SC2 promotes gut immune homeostasis to limit commensal dysbiosis and extend lifespan. Cell, 2014, 156(1-2), 109-22.
60. [60] Marianes, A.; Spradling, A.C. Physiological and stem cell com partmentalization within the Drosophila midgut. Elife., 2013, 2, e00886.