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Epithelial cell-turnover ensures robust coordination of tissue growth in Drosophila ribosomal protein mutants


Autoři: Nanami Akai aff001;  Shizue Ohsawa aff001;  Yukari Sando aff001;  Tatsushi Igaki aff001
Působiště autorů: Laboratory of Genetics, Graduate School of Biostudies, Kyoto University, Kyoto, Japan aff001;  Group of Genetics, Division of Biological Science, Graduate School of Science, Nagoya University, Nagoya, Japan aff002
Vyšlo v časopise: Epithelial cell-turnover ensures robust coordination of tissue growth in Drosophila ribosomal protein mutants. PLoS Genet 17(1): e1009300. doi:10.1371/journal.pgen.1009300
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1009300

Souhrn

Highly reproducible tissue development is achieved by robust, time-dependent coordination of cell proliferation and cell death. To study the mechanisms underlying robust tissue growth, we analyzed the developmental process of wing imaginal discs in Drosophila Minute mutants, a series of heterozygous mutants for a ribosomal protein gene. Minute animals show significant developmental delay during the larval period but develop into essentially normal flies, suggesting there exists a mechanism ensuring robust tissue growth during abnormally prolonged developmental time. Surprisingly, we found that both cell death and compensatory cell proliferation were dramatically increased in developing wing pouches of Minute animals. Blocking the cell-turnover by inhibiting cell death resulted in morphological defects, indicating the essential role of cell-turnover in Minute wing morphogenesis. Our analyses showed that Minute wing discs elevate Wg expression and JNK-mediated Dilp8 expression that causes developmental delay, both of which are necessary for the induction of cell-turnover. Furthermore, forced increase in Wg expression together with developmental delay caused by ecdysone depletion induced cell-turnover in the wing pouches of non-Minute animals. Our findings suggest a novel paradigm for robust coordination of tissue growth by cell-turnover, which is induced when developmental time axis is distorted.

Klíčová slova:

Animal wings – Cell death – Cell proliferation – Cell staining – Drosophila melanogaster – Genetics – Larvae – Morphogenesis


Zdroje

1. Waddington CH. The epigenotype. 1942. Int J Epidemiol. 2012;41(1):10–3. doi: 10.1093/ije/dyr184 22186258

2. Haynie JL, PJ B. The effects of X-rays on the proliferation dynamics of cells in the imaginal wing disc ofDrosophila melanogaster. Wilehm Roux Arch Dev Biol. 1977;183(2):85–100. doi: 10.1007/BF00848779 28304897

3. Fan Y, Bergmann A. Apoptosis-induced compensatory proliferation. The Cell is dead. Long live the Cell! Trends Cell Biol. 2008;18(10):467–73. doi: 10.1016/j.tcb.2008.08.001 18774295

4. Morata G, Shlevkov E, Perez-Garijo A. Mitogenic signaling from apoptotic cells in Drosophila. Dev Growth Differ. 2011;53(2):168–76. doi: 10.1111/j.1440-169X.2010.01225.x 21338343

5. Andersen DS, Colombani J, Leopold P. Drosophila growth and development: keeping things in proportion. Cell cycle (Georgetown, Tex). 2012;11(16):2971–2. doi: 10.4161/cc.21466 22871728

6. Parker NF, Shingleton AW. The coordination of growth among Drosophila organs in response to localized growth-perturbation. Developmental biology. 2011;357(2):318–25. doi: 10.1016/j.ydbio.2011.07.002 21777576

7. Brehme KS. A Study of the Effect on Development of "Minute" Mutations in Drosophila Melanogaster. Genetics. 1939;24(2):131–61. 17246916

8. Lambertsson A. The minute genes in Drosophila and their molecular functions. Adv Genet. 1998;38:69–134. doi: 10.1016/s0065-2660(08)60142-x 9677706

9. Morata G, Ripoll P. Minutes: mutants of drosophila autonomously affecting cell division rate. Developmental biology. 1975;42(2):211–21. doi: 10.1016/0012-1606(75)90330-9 1116643

10. Biyasheva A, Do TV, Lu Y, Vaskova M, Andres AJ. Glue secretion in the Drosophila salivary gland: a model for steroid-regulated exocytosis. Developmental biology. 2001;231(1):234–51. doi: 10.1006/dbio.2000.0126 11180965

11. Sakaue-Sawano A, Ohtawa K, Hama H, Kawano M, Ogawa M, Miyawaki A. Tracing the silhouette of individual cells in S/G2/M phases with fluorescence. Chem Biol. 2008;15(12):1243–8. doi: 10.1016/j.chembiol.2008.10.015 19101468

12. Nakajima Y, Kuranaga E, Sugimura K, Miyawaki A, Miura M. Nonautonomous apoptosis is triggered by local cell cycle progression during epithelial replacement in Drosophila. Molecular and cellular biology. 2011;31(12):2499–512. doi: 10.1128/MCB.01046-10 21482673

13. Williams DW, Kondo S, Krzyzanowska A, Hiromi Y, Truman JW. Local caspase activity directs engulfment of dendrites during pruning. Nature neuroscience. 2006;9(10):1234–6. doi: 10.1038/nn1774 16980964

14. Liang CJ, Chang YC, Chang HC, Wang CK, Hung YC, Lin YE, et al. Derlin-1 regulates mutant VCP-linked pathogenesis and endoplasmic reticulum stress-induced apoptosis. PLoS Genet. 2014;10(9):e1004675. doi: 10.1371/journal.pgen.1004675 25255315

15. Florentin A, Arama E. Caspase levels and execution efficiencies determine the apoptotic potential of the cell. The Journal of cell biology. 2012;196(4):513–27. doi: 10.1083/jcb.201107133 22351928

16. Shinoda N, Obata F, Zhang L, Miura M. Drosophila SETDB1 and caspase cooperatively fine-tune cell fate determination of sensory organ precursor. Genes Cells. 2016;21(4):378–86. doi: 10.1111/gtc.12348 26914287

17. Enomoto M, Kizawa D, Ohsawa S, Igaki T. JNK signaling is converted from anti- to pro-tumor pathway by Ras-mediated switch of Warts activity. Developmental biology. 2015;403(2):162–71. doi: 10.1016/j.ydbio.2015.05.001 25967126

18. Ohsawa S, Sato Y, Enomoto M, Nakamura M, Betsumiya A, Igaki T. Mitochondrial defect drives non-autonomous tumour progression through Hippo signalling in Drosophila. Nature. 2012;490(7421):547–51. doi: 10.1038/nature11452 23023132

19. Ohsawa S, Sugimura K, Takino K, Xu T, Miyawaki A, Igaki T. Elimination of oncogenic neighbors by JNK-mediated engulfment in Drosophila. Developmental cell. 2011;20(3):315–28. doi: 10.1016/j.devcel.2011.02.007 21397843

20. Gorelick-Ashkenazi A, Weiss R, Sapozhnikov L, Florentin A, Tarayrah-Ibraheim L, Dweik D, et al. Caspases maintain tissue integrity by an apoptosis-independent inhibition of cell migration and invasion. Nature communications. 2018;9(1):2806. doi: 10.1038/s41467-018-05204-6 30022065

21. Hay BA, Wolff T, Rubin GM. Expression of baculovirus P35 prevents cell death in Drosophila. Development. 1994;120(8):2121–9. 7925015

22. Ryoo HD, Bergmann A. The role of apoptosis-induced proliferation for regeneration and cancer. Cold Spring Harbor perspectives in biology. 2012;4(8):a008797. doi: 10.1101/cshperspect.a008797 22855725

23. Perez-Garijo A, Martin FA, Struhl G, Morata G. Dpp signaling and the induction of neoplastic tumors by caspase-inhibited apoptotic cells in Drosophila. Proceedings of the National Academy of Sciences of the United States of America. 2005;102(49):17664–9. doi: 10.1073/pnas.0508966102 16314564

24. Brown NH, Gregory SL, Martin-Bermudo MD. Integrins as mediators of morphogenesis in Drosophila. Developmental biology. 2000;223(1):1–16. doi: 10.1006/dbio.2000.9711 10864456

25. White K, Grether ME, Abrams JM, Young L, Farrell K, Steller H. Genetic control of programmed cell death in Drosophila. Science (New York, NY). 1994;264(5159):677–83. doi: 10.1126/science.8171319 8171319

26. Grether ME, Abrams JM, Agapite J, White K, Steller H. The head involution defective gene of Drosophila melanogaster functions in programmed cell death. Genes & development. 1995;9(14):1694–708. doi: 10.1101/gad.9.14.1694 7622034

27. Chen P, Nordstrom W, Gish B, Abrams JM. grim, a novel cell death gene in Drosophila. Genes & development. 1996;10(14):1773–82. doi: 10.1101/gad.10.14.1773 8698237

28. Meier P, Silke J, Leevers SJ, Evan GI. The Drosophila caspase DRONC is regulated by DIAP1. The EMBO journal. 2000;19(4):598–611. doi: 10.1093/emboj/19.4.598 10675329

29. Swarup S, Verheyen EM. Wnt/Wingless signaling in Drosophila. Cold Spring Harbor perspectives in biology. 2012;4(6). doi: 10.1101/cshperspect.a007930 22535229

30. Gonsalves FC, DasGupta R. Function of the wingless signaling pathway in Drosophila. Methods in molecular biology (Clifton, NJ). 2008;469:115–25. doi: 10.1007/978-1-60327-469-2_10 19109707

31. Zeng YA, Verheyen EM. Nemo is an inducible antagonist of Wingless signaling during Drosophila wing development. Development. 2004;131(12):2911–20. doi: 10.1242/dev.01177 15169756

32. Choi KW, Benzer S. Rotation of photoreceptor clusters in the developing Drosophila eye requires the nemo gene. Cell. 1994;78(1):125–36. doi: 10.1016/0092-8674(94)90579-7 8033204

33. Zeng W, Wharton KA Jr, Mack JA, Wang K, Gadbaw M, Suyama K, et al. naked cuticle encodes an inducible antagonist of Wnt signalling. Nature. 2000;403(6771):789–95. doi: 10.1038/35001615 10693810

34. Vincent JP, Kolahgar G, Gagliardi M, Piddini E. Steep differences in wingless signaling trigger Myc-independent competitive cell interactions. Developmental cell. 2011;21(2):366–74. doi: 10.1016/j.devcel.2011.06.021 21839923

35. van de Wetering M, Cavallo R, Dooijes D, van Beest M, van Es J, Loureiro J, et al. Armadillo coactivates transcription driven by the product of the Drosophila segment polarity gene dTCF. Cell. 1997;88(6):789–99. doi: 10.1016/s0092-8674(00)81925-x 9118222

36. Theisen H, Purcell J, Bennett M, Kansagara D, Syed A, Marsh JL. dishevelled is required during wingless signaling to establish both cell polarity and cell identity. Development. 1994;120(2):347–60. 8149913

37. Krasnow RE, Adler PN. A single frizzled protein has a dual function in tissue polarity. Development. 1994;120(7):1883–93. 7924994

38. Klingensmith J, Nusse R, Perrimon N. The Drosophila segment polarity gene dishevelled encodes a novel protein required for response to the wingless signal. Genes & development. 1994;8(1):118–30. doi: 10.1101/gad.8.1.118 8288125

39. Dong Y, Friedrich M. Comparative analysis of Wingless patterning in the embryonic grasshopper eye. Dev Genes Evol. 2005;215(4):177–97. doi: 10.1007/s00427-004-0465-6 15747130

40. Baena-Lopez LA, Franch-Marro X, Vincent JP. Wingless promotes proliferative growth in a gradient-independent manner. Science signaling. 2009;2(91):ra60. doi: 10.1126/scisignal.2000360 19809090

41. Garelli A, Gontijo AM, Miguela V, Caparros E, Dominguez M. Imaginal discs secrete insulin-like peptide 8 to mediate plasticity of growth and maturation. Science (New York, NY). 2012;336(6081):579–82.

42. Colombani J, Andersen DS, Leopold P. Secreted peptide Dilp8 coordinates Drosophila tissue growth with developmental timing. Science (New York, NY). 2012;336(6081):582–5. doi: 10.1126/science.1216689 22556251

43. Skinner A, Khan SJ, Smith-Bolton RK. Trithorax regulates systemic signaling during Drosophila imaginal disc regeneration. Development. 2015;142(20):3500–11. doi: 10.1242/dev.122564 26487779

44. Kulshammer E, Mundorf J, Kilinc M, Frommolt P, Wagle P, Uhlirova M. Interplay among Drosophila transcription factors Ets21c, Fos and Ftz-F1 drives JNK-mediated tumor malignancy. Disease models & mechanisms. 2015;8(10):1279–93. doi: 10.1242/dmm.020719 26398940

45. Demay Y, Perochon J, Szuplewski S, Mignotte B, Gaumer S. The PERK pathway independently triggers apoptosis and a Rac1/Slpr/JNK/Dilp8 signaling favoring tissue homeostasis in a chronic ER stress Drosophila model. Cell death & disease. 2014;5:e1452.

46. Chatterjee N, Bohmann D. A versatile PhiC31 based reporter system for measuring AP-1 and Nrf2 signaling in Drosophila and in tissue culture. PloS one. 2012;7(4):e34063. doi: 10.1371/journal.pone.0034063 22509270

47. Mattila J, Omelyanchuk L, Kyttala S, Turunen H, Nokkala S. Role of Jun N-terminal Kinase (JNK) signaling in the wound healing and regeneration of a Drosophila melanogaster wing imaginal disc. The International journal of developmental biology. 2005;49(4):391–9. doi: 10.1387/ijdb.052006jm 15968584

48. Lin JI MN, Kalcina M, Tchoubrieva E, Stewart MJ, Marygold SJ, Walker CD, Thomas G, Leevers SJ, Pearson RB, Quinn LM, Hannan RD. Drosophila ribosomal protein mutants control tissue growth non-autonomously via effects on the prothoracic gland and ecdysone. PLoS Genet. 2011;7(12). doi: 10.1371/journal.pgen.1002408 22194697

49. Gaziova I, Bonnette PC, Henrich VC, Jindra M. Cell-autonomous roles of the ecdysoneless gene in Drosophila development and oogenesis. Development. 2004;131(11):2715–25. doi: 10.1242/dev.01143 15128659

50. Parkin CA, Burnet B. Growth arrest of Drosophila melanogaster on erg-2 and erg-6 sterol mutant strains of Saccharomyces cerevisiae. ScienceDirect. 1986(32):463–71.

51. Bos M, Burnet B, Farrow R, Woods RA. Development of Drosophila on sterol mutants of the yeast Saccharomyces cerevisiae. Genet Res. 1976;28(2):163–76. doi: 10.1017/s0016672300016840 795728

52. Igaki T, Pastor-Pareja JC, Aonuma H, Miura M, Xu T. Intrinsic tumor suppression and epithelial maintenance by endocytic activation of Eiger/TNF signaling in Drosophila. Developmental cell. 2009;16(3):458–65. doi: 10.1016/j.devcel.2009.01.002 19289090

53. Smith-Bolton RK, Worley MI, Kanda H, Hariharan IK. Regenerative growth in Drosophila imaginal discs is regulated by Wingless and Myc. Developmental cell. 2009;16(6):797–809. doi: 10.1016/j.devcel.2009.04.015 19531351

54. Rutherford SL, Lindquist S. Hsp90 as a capacitor for morphological evolution. Nature. 1998;396(6709):336–42. doi: 10.1038/24550 9845070

55. Rohner N, Jarosz DF, Kowalko JE, Yoshizawa M, Jeffery WR, Borowsky RL, et al. Cryptic variation in morphological evolution: HSP90 as a capacitor for loss of eyes in cavefish. Science (New York, NY). 2013;342(6164):1372–5. doi: 10.1126/science.1240276 24337296

56. Queitsch C, Sangster TA, Lindquist S. Hsp90 as a capacitor of phenotypic variation. Nature. 2002;417(6889):618–24. doi: 10.1038/nature749 12050657

57. Stern DL, Emlen DJ. The developmental basis for allometry in insects. Development. 1999;126(6):1091–101. 10021329

58. Merino MM, Levayer R, Moreno E. Survival of the Fittest: Essential Roles of Cell Competition in Development, Aging, and Cancer. Trends Cell Biol. 2016;26(10):776–88. doi: 10.1016/j.tcb.2016.05.009 27319281

59. Di Gregorio A, Bowling S, Rodriguez TA. Cell Competition and Its Role in the Regulation of Cell Fitness from Development to Cancer. Developmental cell. 2016;38(6):621–34. doi: 10.1016/j.devcel.2016.08.012 27676435

60. Amoyel M, Bach EA. Cell competition: how to eliminate your neighbours. Development. 2014;141(5):988–1000. doi: 10.1242/dev.079129 24550108

61. Katsuyama T, Comoglio F, Seimiya M, Cabuy E, Paro R. During Drosophila disc regeneration, JAK/STAT coordinates cell proliferation with Dilp8-mediated developmental delay. Proceedings of the National Academy of Sciences of the United States of America. 2015;112(18):E2327–36. doi: 10.1073/pnas.1423074112 25902518

62. Xue S, Barna M. Specialized ribosomes: a new frontier in gene regulation and organismal biology. Nat Rev Mol Cell Biol. 2012;13(6):355–69. doi: 10.1038/nrm3359 22617470

63. Bolze A, Mahlaoui N, Byun M, Turner B, Trede N, Ellis SR, et al. Ribosomal protein SA haploinsufficiency in humans with isolated congenital asplenia. Science (New York, NY). 2013;340(6135):976–8. doi: 10.1126/science.1234864 23579497

64. Bilder D, Perrimon N. Localization of apical epithelial determinants by the basolateral PDZ protein Scribble. Nature. 2000;403(6770):676–80. doi: 10.1038/35001108 10688207

65. Martin-Blanco E, Gampel A, Ring J, Virdee K, Kirov N, Tolkovsky AM, et al. puckered encodes a phosphatase that mediates a feedback loop regulating JNK activity during dorsal closure in Drosophila. Genes & development. 1998;12(4):557–70. doi: 10.1101/gad.12.4.557 9472024

66. Akai N, Igaki T, Ohsawa S. Wingless signaling regulates winner/loser status in Minute cell competition. Genes Cells. 2018;23(3):234–40. doi: 10.1111/gtc.12568 29431244

67. Iida C, Ohsawa S, Taniguchi K, Yamamoto M, Morata G, Igaki T. JNK-mediated Slit-Robo signaling facilitates epithelial wound repair by extruding dying cells. Scientific reports. 2019;9(1):19549. doi: 10.1038/s41598-019-56137-z 31863086

68. Aldaz S, Escudero LM, Freeman M. Live imaging of Drosophila imaginal disc development. Proceedings of the National Academy of Sciences of the United States of America. 2010;107(32):14217–22. doi: 10.1073/pnas.1008623107 20660765

69. Debat V, Cornette R, Korol AB, Nevo E, Soulet D, David JR. Multidimensional analysis of Drosophila wing variation in Evolution Canyon. Journal of genetics. 2008;87(4):407–19. doi: 10.1007/s12041-008-0063-x 19147930


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