A deregulated intestinal cell cycle program disrupts tissue homeostasis without affecting longevity in drosophila

Journal of Biological Chemistry

Volumn 289, Issue 41, 2014, Pages 28719-28729

  Petkau, Kristina ^a   Parsons, Brendon D ^a   Duggal, Aashna ^a   Foley, Edan ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CELL DEATH; CELL PROLIFERATION; CELLS; CYTOLOGY; STEM CELLS; TISSUE;

ADULT STEM CELLS; COMPLEX RELATIONSHIPS; DEGREE OF PLASTICITY; DROSOPHILA MELANOGASTER; EPITHELIAL BARRIER; INTESTINAL CELLS; MODEL SYSTEM; TISSUE DAMAGE;

TISSUE HOMEOSTASIS;

TRANSCRIPTION FACTOR GAL4; BIOLOGICAL MARKER; DACAPO PROTEIN, DROSOPHILA; DROSOPHILA PROTEIN; ESCARGOT PROTEIN, DROSOPHILA; MYOSIN HEAVY CHAIN; NUCLEAR PROTEIN;

ADULT STEM CELL; ANIMAL CELL; ARTICLE; CELL CYCLE; CELL DEATH; CELL DIVISION; CELL PROLIFERATION; CELL SHAPE; CELL STRUCTURE; DROSOPHILA; ENDOREDUPLICATION; IMMUNOFLUORESCENCE; INTESTINE CELL; INTESTINE DISTENSION; INTESTINE FUNCTION; LIFESPAN; LONGEVITY; MIDGUT; NONHUMAN; PHENOTYPIC VARIATION; PROTEIN EXPRESSION; STEM CELL; TISSUE METABOLISM; TRANSMISSION ELECTRON MICROSCOPY; ANIMAL; CELL DIFFERENTIATION; DROSOPHILA MELANOGASTER; FEMALE; GENE EXPRESSION REGULATION; GENETICS; HOMEOSTASIS; INTESTINE; MALE; METABOLISM; MICROBIOLOGY; PATHOLOGY; PHYSIOLOGY; PSEUDOMONAS;

ADULT STEM CELLS; ANIMALS; BIOLOGICAL MARKERS; CELL CYCLE; CELL DEATH; CELL DIFFERENTIATION; CELL PROLIFERATION; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; ENTEROCYTES; FEMALE; GENE EXPRESSION REGULATION; HOMEOSTASIS; INTESTINES; LONGEVITY; MALE; MYOSIN HEAVY CHAINS; NUCLEAR PROTEINS; PSEUDOMONAS;

EID: 84907842149     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.578708     Document Type: Article

References (61)

1. Buffie, C. G., and Pamer, E. G. (2013) Microbiota-mediated colonization resistance against intestinal pathogens. Nat. Rev. Immunol. 13, 790-801
2. Chen, V. L., and Kasper, D. L. (2014) Interactions between the intestinal microbiota and innate lymphoid cells. Gut Microbes 5, 129-140
3. Clemente, J. C., Ursell, L. K., Parfrey, L. W., and Knight, R. (2012) The impact of the gut microbiota on human health: an integrative view. Cell 148, 1258-1270
4. Lee, W. J., and Brey, P. T. (2013) How microbiomes influence metazoan development: insights from history and Drosophila modeling of gut-microbe interactions. Annu. Rev. Cell Dev. Biol. 29, 571-592
5. Montiel-Castro, A. J., González-Cervantes, R. M., Bravo-Ruiseco, G., and Pacheco-López, G. (2013) The microbiota-gut-brain axis: neurobehavioral correlates, health and sociality. Front. Integr. Neurosci. 7, 70
6. Ayyaz, A., and Jasper, H. (2013) Intestinal inflammation and stem cell homeostasis in aging Drosophila melanogaster. Front. Cell. Infect. Microbiol. 3, 98
7. Buchon, N., Broderick, N. A., and Lemaitre, B. (2013) Gut homeostasis in a microbial world: insights from Drosophila melanogaster. Nat. Rev. Microbiol. 11, 615-626
8. Lemaitre, B., and Miguel-Aliaga, I. (2013) The digestive tract of Drosophila melanogaster. Annu. Rev. Genet. 47, 377-404
9. Micchelli, C. A., and Perrimon, N. (2006) Evidence that stem cells reside in the adult Drosophila midgut epithelium. Nature 439, 475-479
10. O'Brien, L. E., Soliman, S. S., Li, X., and Bilder, D. (2011) Altered modes of stem cell division drive adaptive intestinal growth. Cell 147, 603-614
11. Ohlstein, B., and Spradling, A. (2006) The adult Drosophila posterior midgut is maintained by pluripotent stem cells. Nature 439, 470-474
12. Amcheslavsky, A., Ito, N., Jiang, J., and Ip, Y. T. (2011) Tuberous sclerosis complex and Myc coordinate the growth and division of Drosophila intestinal stem cells. J. Cell Biol. 193, 695-710
13. Biteau, B., Hochmuth, C. E., and Jasper, H. (2011) Maintaining tissue homeostasis: dynamic control of somatic stem cell activity. Cell Stem Cell 9, 402-411
14. Biteau, B., and Jasper, H. (2011) EGF signaling regulates the proliferation of intestinal stem cells in Drosophila. Development 138, 1045-1055
15. Bond, D., and Foley, E. (2012) Autocrine platelet-derived growth factorvascular endothelial growth factor receptor-related (Pvr) pathway activity controls intestinal stem cell proliferation in the adult Drosophila midgut. J. Biol. Chem. 287, 27359-27370
16. Cordero, J. B., Stefanatos, R. K., Myant, K., Vidal, M., and Sansom, O. J. (2012) Non-autonomous crosstalk between the Jak/Stat and Egfr pathways mediates Apc1-driven intestinal stem cell hyperplasia in the Drosophila adult midgut. Development 139, 4524-4535
17. Cordero, J. B., Stefanatos, R. K., Scopelliti, A., Vidal, M., and Sansom, O. J. (2012) Inducible progenitor-derived Wingless regulates adult midgut regeneration in Drosophila. EMBO J. 31, 3901-3917
18. Jiang, H., and Edgar, B. A. (2009) EGFR signaling regulates the proliferation of Drosophila adult midgut progenitors. Development 136, 483-493
19. Jiang, H., and Edgar, B. A. (2011) Intestinal stem cells in the adult Drosophila midgut. Exp. Cell Res. 317, 2780-2788
20. Jiang, H., Grenley, M. O., Bravo, M. J., Blumhagen, R. Z., and Edgar, B. A. (2011) EGFR/Ras/MAPK signaling mediates adult midgut epithelial homeostasis and regeneration in Drosophila. Cell Stem Cell 8, 84-95
21. Jiang, H., Patel, P. H., Kohlmaier, A., Grenley, M. O., McEwen, D. G., and Edgar, B. A. (2009) Cytokine/Jak/Stat signaling mediates regeneration and homeostasis in the Drosophila midgut. Cell 137, 1343-1355
22. Kapuria, S., Karpac, J., Biteau, B., Hwangbo, D., and Jasper, H. (2012) Notch-mediated suppression of TSC2 expression regulates cell differentiation in the Drosophila intestinal stem cell lineage. PLoS Genet. 8, e1003045
23. Li, Z., Zhang, Y., Han, L., Shi, L., and Lin, X. (2013) Trachea-derived Dpp controls adult midgut homeostasis in Drosophila. Dev. Cell 24, 133-143
24. Lin, G., Xu, N., and Xi, R. (2008) Paracrine Wingless signalling controls self-renewal of Drosophila intestinal stem cells. Nature 455, 1119-1123
25. Park, J. S., Kim, Y. S., and Yoo, M. A. (2009) The role of p38b MAPK in age-related modulation of intestinal stem cell proliferation and differentiation in Drosophila. Aging 1, 637-651
26. Quan, Z., Sun, P., Lin, G., and Xi, R. (2013) TSC1/2 regulates intestinal stem cell maintenance and lineage differentiation through Rheb-TORC1- S6K but independently of nutritional status or Notch regulation. J. Cell Sci. 126, 3884-3892
27. Takashima, S., and Hartenstein, V. (2012) Genetic control of intestinal stem cell specification and development: a comparative view. Stem Cell Rev. 8, 597-608
28. Takashima, S., Mkrtchyan, M., Younossi-Hartenstein, A., Merriam, J. R., and Hartenstein, V. (2008) The behaviour of Drosophila adult hindgut stem cells is controlled by Wnt and Hh signalling. Nature 454, 651-655
29. Xu, N., Wang, S. Q., Tan, D., Gao, Y., Lin, G., and Xi, R. (2011) EGFR, Wingless and JAK/STAT signaling cooperatively maintain Drosophila intestinal stem cells. Dev. Biol. 354, 31-43
30. Shaw, R. L., Kohlmaier, A., Polesello, C., Veelken, C., Edgar, B. A., and Tapon, N. (2010) The Hippo pathway regulates intestinal stem cell proliferation during Drosophila adult midgut regeneration. Development 137, 4147-4158
31. Biteau, B., Hochmuth, C. E., and Jasper, H. (2008) JNK activity in somatic stem cells causes loss of tissue homeostasis in the aging Drosophila gut. Cell Stem Cell 3, 442-455
32. Buchon, N., Broderick, N. A., Chakrabarti, S., and Lemaitre, B. (2009) Invasive and indigenous microbiota impact intestinal stem cell activity through multiple pathways in Drosophila. Genes Dev. 23, 2333-2344
33. Buchon, N., Broderick, N. A., Kuraishi, T., and Lemaitre, B. (2010) Drosophila EGFR pathway coordinates stem cell proliferation and gut remodeling following infection. BMC Biol. 8, 152
34. Buchon, N., Broderick, N. A., Poidevin, M., Pradervand, S., and Lemaitre, B. (2009) Drosophila intestinal response to bacterial infection: activation of host defense and stem cell proliferation. Cell Host Microbe 5, 200-211
35. Chatterjee, M., and Ip, Y. T. (2009) Pathogenic stimulation of intestinal stem cell response in Drosophila. J. Cell. Physiol. 220, 664-671
36. Guo, Z., Driver, I., and Ohlstein, B. (2013) Injury-induced BMP signaling negatively regulates Drosophila midgut homeostasis. J. Cell Biol. 201, 945-961
37. Karpac, J., Hull-Thompson, J., Falleur, M., and Jasper, H. (2009) JNK signaling in insulin-producing cells is required for adaptive responses to stress in Drosophila. Aging Cell 8, 288-295
38. Karpowicz, P., Perez, J., and Perrimon, N. (2010) The Hippo tumor suppressor pathway regulates intestinal stem cell regeneration. Development 137, 4135-4145
39. Ren, F., Wang, B., Yue, T., Yun, E. Y., Ip, Y. T., and Jiang, J. (2010) Hippo signaling regulates Drosophila intestine stem cell proliferation through multiple pathways. Proc. Natl. Acad. Sci. U.S.A. 107, 21064-21069
40. Staley, B. K., and Irvine, K. D. (2010) Warts and Yorkie mediate intestinal regeneration by influencing stem cell proliferation. Curr. Biol. 20, 1580-1587
41. Liu, W., Singh, S. R., and Hou, S. X. (2010) JAK-STAT is restrained by Notch to control cell proliferation of the Drosophila intestinal stem cells. J. Cell. Biochem. 109, 992-999
42. Ohlstein, B., and Spradling, A. (2007) Multipotent Drosophila intestinal stem cells specify daughter cell fates by differential notch signaling. Science 315, 988-992
43. Takashima, S., Adams, K. L., Ortiz, P. A., Ying, C. T., Moridzadeh, R., Younossi-Hartenstein, A., and Hartenstein, V. (2011) Development of the Drosophila entero-endocrine lineage and its specification by the Notch signaling pathway. Dev. Biol. 353, 161-172
44. Biteau, B., Karpac, J., Supoyo, S., Degennaro, M., Lehmann, R., and Jasper, H. (2010) Lifespan extension by preserving proliferative homeostasis in Drosophila. PLoS Genet. 6, e1001159
45. Hochmuth, C. E., Biteau, B., Bohmann, D., and Jasper, H. (2011) Redox regulation by Keap1 and Nrf2 controls intestinal stem cell proliferation in Drosophila. Cell Stem Cell 8, 188-199
46. Rera, M., Clark, R. I., and Walker, D. W. (2012) Intestinal barrier dysfunction links metabolic and inflammatory markers of aging to death in Drosophila. Proc. Natl. Acad. Sci. U.S.A. 109, 21528-21533
47. Ren, C., Webster, P., Finkel, S. E., and Tower, J. (2007) Increased internal and external bacterial load during Drosophila aging without life-span trade-off. Cell Metab. 6, 144-152
48. Ha, E. M., Lee, K. A., Park, S. H., Kim, S. H., Nam, H. J., Lee, H. Y., Kang, D., and Lee, W. J. (2009) Regulation of DUOX by the Gαq-phospholipase Cββ-Ca2+ pathway in Drosophila gut immunity. Dev. Cell 16, 386-397
49. Ha, E. M., Lee, K. A., Seo, Y. Y., Kim, S. H., Lim, J. H., Oh, B. H., Kim, J., and Lee, W. J. (2009) Coordination of multiple dual oxidase-regulatory pathways in responses to commensal and infectious microbes in Drosophila gut. Nat. Immunol. 10, 949-957
50. Ha, E. M., Oh, C. T., Bae, Y. S., and Lee, W. J. (2005) A direct role for dual oxidase in Drosophila gut immunity. Science 310, 847-850
51. Wong, C. N., Ng, P., and Douglas, A. E. (2011) Low-diversity bacterial community in the gut of the fruitfly Drosophila melanogaster. Environ. Microbiol. 13, 1889-1900
52. Brummel, T., Ching, A., Seroude, L., Simon, A. F., and Benzer, S. (2004) Drosophila lifespan enhancement by exogenous bacteria. Proc. Natl. Acad. Sci. U.S.A. 101, 12974-12979
53. Ryu, J. H., Kim, S. H., Lee, H. Y., Bai, J. Y., Nam, Y. D., Bae, J. W., Lee, D. G., Shin, S. C., Ha, E. M., and Lee, W. J. (2008) Innate immune homeostasis by the homeobox gene Caudal and commensal-gut mutualism in Drosophila. Science 319, 777-782
54. Duchek, P., and Rørth, P. (2001) Guidance of cell migration by EGF receptor signaling during Drosophila oogenesis. Science 291, 131-133
55. Lane, M. E., Sauer, K., Wallace, K., Jan, Y. N., Lehner, C. F., and Vaessin, H. (1996) Dacapo, a cyclin-dependent kinase inhibitor, stops cell proliferation during Drosophila development. Cell 87, 1225-1235
56. Guntermann, S., and Foley, E. (2011) The protein Dredd is an essential component of the c-Jun N-terminal kinase pathway in the Drosophila immune response. J. Biol. Chem. 286, 30284-30294
57. Vodovar, N., Vinals, M., Liehl, P., Basset, A., Degrouard, J., Spellman, P., Boccard, F., and Lemaitre, B. (2005) Drosophila host defense after oral infection by an entomopathogenic Pseudomonas species. Proc. Natl. Acad. Sci. U.S.A. 102, 11414-11419
58. Ferrandon, D. (2013) The complementary facets of epithelial host defenses in the genetic model organism Drosophila melanogaster: from resistance to resilience. Curr. Opin. Immunol. 25, 59-70
59. Stronach, B. (2005) Dissecting JNK signaling, one KKKinase at a time. Dev. Dyn. 232, 575-584
60. Kannan, K., and Fridell, Y. W. (2013) Functional implications of Drosophila insulin-like peptides in metabolism, aging, and dietary restriction. Front. Physiol. 4, 288
61. Gartner, L. P. (1973) Ultrastructural examination of ageing and radiationinduced life-span shortening in adult Drosophila melanogaster. Int. J. Radiat. Biol. Relat. Stud. Phys. Chem. Med. 23, 23-39