Reduction of endocytosis and EGFR signaling is associated with the switch from isolated to clustered apoptosis during epithelial tissue remodeling in Drosophila.

Publisher: Public Library of Science Country of Publication: United States NLM ID: 101183755 Publication Model: eCollection Cited Medium: Internet ISSN: 1545-7885 (Electronic) Linking ISSN: 15449173 NLM ISO Abbreviation: PLoS Biol Subsets: MEDLINE

Original Publication: San Francisco, CA : Public Library of Science, [2003]-

Endocytosis*/physiology ; Apoptosis* ; ErbB Receptors*/metabolism ; Drosophila Proteins*/metabolism ; Drosophila Proteins*/genetics ; Signal Transduction* ; Drosophila melanogaster*/metabolism ; Drosophila melanogaster*/genetics; Animals ; Extracellular Signal-Regulated MAP Kinases/metabolism ; Larva/metabolism ; Metamorphosis, Biological/physiology ; Receptors, Invertebrate Peptide/metabolism ; Receptors, Invertebrate Peptide/genetics ; Epithelium/metabolism ; Epidermal Cells/metabolism ; Drosophila/metabolism

Epithelial tissues undergo cell turnover both during development and for homeostatic maintenance. Removal of cells is coordinated with the increase in number of newly dividing cells to maintain barrier function of the tissue. In Drosophila metamorphosis, larval epidermal cells (LECs) are replaced by adult precursor cells called histoblasts. Removal of LECs must counterbalance the exponentially increasing adult histoblasts. Previous work showed that the LEC removal accelerates as endocytic activity decreases throughout all LECs. Here, we show that the acceleration is accompanied by a mode switching from isolated single-cell apoptosis to clustered ones induced by the endocytic activity reduction. We identify the epidermal growth factor receptor (EGFR) pathway via extracellular-signal regulated kinase (ERK) activity as the main components downstream of endocytic activity in LECs. The reduced ERK activity, caused by the decrease in endocytic activity, is responsible for the apoptotic mode switching. Initially, ERK is transiently activated in normal LECs surrounding a single apoptotic LEC in a ligand-dependent manner, preventing clustered cell death. Following the reduction of endocytic activity, LEC apoptosis events do not provoke these transient ERK up-regulations, resulting in the acceleration of the cell elimination rate by frequent clustered apoptosis. These findings contrasted with the common perspective that clustered apoptosis is disadvantageous. Instead, switching to clustered apoptosis is required to accommodate the growth of neighboring tissues.
Competing Interests: The authors have declared that no competing interests exist.
(Copyright: © 2024 Yuswan et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.)

Nature. 2017 Apr 12;544(7649):212-216. (PMID: 28406198)
Dev Cell. 2020 Jun 22;53(6):646-660.e8. (PMID: 32497487)
Cell Death Dis. 2017 May 11;8(5):e2787. (PMID: 28492553)
Genes Dev. 1996 Sep 15;10(18):2302-13. (PMID: 8824589)
EMBO J. 2002 Aug 15;21(16):4287-96. (PMID: 12169631)
Development. 2020 Sep 2;147(17):. (PMID: 32878903)
J Cell Biol. 2017 Mar 6;216(3):559-570. (PMID: 28174204)
Cancers (Basel). 2017 Feb 07;9(2):. (PMID: 28178204)
Curr Biol. 2001 Nov 27;11(23):1847-57. (PMID: 11728307)
Methods. 2017 Feb 15;115:80-90. (PMID: 27713081)
Philos Trans R Soc Lond B Biol Sci. 2017 May 19;372(1720):. (PMID: 28348253)
Science. 1994 Apr 29;264(5159):677-83. (PMID: 8171319)
J Neurobiol. 2001 May;47(2):81-92. (PMID: 11291099)
Mech Dev. 1998 Dec;79(1-2):73-82. (PMID: 10349622)
Science. 1996 Oct 11;274(5285):252-5. (PMID: 8824191)
Dev Cell. 2018 Jul 16;46(2):162-172.e5. (PMID: 29983336)
Dev Cell. 2022 Sep 26;57(18):2153-2167.e6. (PMID: 36113484)
J Cell Sci. 2013 Oct 1;126(Pt 19):4469-78. (PMID: 23902690)
Nat Commun. 2021 Nov 12;12(1):6572. (PMID: 34772930)
Elife. 2022 Sep 12;11:. (PMID: 36094159)
Cell. 2004 Feb 6;116(3):445-56. (PMID: 15016378)
Curr Biol. 2021 Sep 27;31(18):R1098-R1110. (PMID: 34582821)
J Comp Neurol. 1983 Jun 1;216(4):445-52. (PMID: 6875047)
Oncotarget. 2018 Feb 15;9(19):14939-14958. (PMID: 29599917)
Evodevo. 2022 Jun 6;13(1):13. (PMID: 35668535)
Cell. 2001 Mar 9;104(5):699-708. (PMID: 11257224)
Nature. 2017 Aug 31;548(7669):588-591. (PMID: 28847000)
Dev Biol. 2012 Mar 1;363(1):179-90. (PMID: 22230614)
Development. 2007 Jan;134(2):367-79. (PMID: 17166923)
Development. 2017 Jan 1;144(1):95-105. (PMID: 27888195)
J Cell Sci. 2009 Oct 1;122(Pt 19):3433-9. (PMID: 19759283)
IUBMB Life. 2006 Nov;58(11):621-31. (PMID: 17085381)
EMBO J. 2000 Oct 16;19(20):5418-28. (PMID: 11032809)
Curr Biol. 2019 Jan 7;29(1):23-34.e8. (PMID: 30554899)
Curr Opin Cell Biol. 2011 Aug;23(4):393-403. (PMID: 21474295)
EMBO Rep. 2019 Oct 4;20(10):e47734. (PMID: 31448519)
Proc Natl Acad Sci U S A. 2006 Jul 5;103(27):10283-10288. (PMID: 16801533)
Development. 2020 Mar 11;147(5):. (PMID: 32161061)
Development. 1997 Oct;124(19):3871-80. (PMID: 9367443)
Curr Biol. 2022 Mar 28;32(6):1285-1300.e4. (PMID: 35167804)
Cell Death Differ. 2020 Jan;27(1):1-14. (PMID: 31745213)
J Biol Chem. 2011 Oct 7;286(40):35196-208. (PMID: 21832070)
Nature. 2012 Apr 15;484(7395):546-9. (PMID: 22504183)
Mol Cell Biol. 2011 Jun;31(12):2499-512. (PMID: 21482673)
Curr Biol. 2010 Apr 13;20(7):643-8. (PMID: 20346676)
Biol Cell. 2021 Aug;113(8):344-373. (PMID: 33788963)
Am J Physiol Lung Cell Mol Physiol. 2002 May;282(5):L883-91. (PMID: 11943650)
Dev Biol. 2013 Nov 15;383(2):275-84. (PMID: 24051228)
Nat Commun. 2019 Sep 27;10(1):4402. (PMID: 31562306)
Genetics. 2004 Jun;167(2):687-98. (PMID: 15238521)
Cell Death Differ. 2009 Mar;16(3):368-77. (PMID: 18846109)
Dev Cell. 2023 Feb 27;58(4):267-277.e5. (PMID: 36800994)
PLoS Biol. 2018 Oct 31;16(10):e3000027. (PMID: 30379844)
J Cell Sci. 2003 Sep 1;116(Pt 17):3583-90. (PMID: 12876219)
Dev Cell. 2021 Jun 21;56(12):1712-1726.e6. (PMID: 34081908)
Development. 2020 Apr 14;147(7):. (PMID: 32156754)
J Embryol Exp Morphol. 1980 Dec;60:1-31. (PMID: 6796636)
J Cell Biol. 2001 Feb 5;152(3):633-43. (PMID: 11157988)
J Biol Chem. 2001 May 11;276(19):16484-90. (PMID: 11278665)
Cell Mol Life Sci. 2016 May;73(9):1825-43. (PMID: 26935860)
Biochim Biophys Acta. 2007 Aug;1773(8):1161-76. (PMID: 17306385)
Cell. 1993 Oct 8;75(1):165-74. (PMID: 7691414)
J Cell Sci. 2012 Mar 1;125(Pt 5):1081-7. (PMID: 22492984)
Mech Dev. 2001 Apr;102(1-2):193-203. (PMID: 11287192)
Sci Rep. 2017 Mar 21;7:44767. (PMID: 28322231)
Nat Cell Biol. 2003 Jul;5(7):647-54. (PMID: 12792650)
EMBO J. 2005 Nov 2;24(21):3793-806. (PMID: 16222340)
Dev Cell. 2021 Jun 21;56(12):1700-1711.e8. (PMID: 34081909)
Dev Growth Differ. 2011 Feb;53(2):202-12. (PMID: 21338346)
Am J Physiol Heart Circ Physiol. 2000 Feb;278(2):H521-9. (PMID: 10666084)
Dev Cell. 2023 Jul 24;58(14):1282-1298.e7. (PMID: 37315563)
Cell Death Differ. 2002 Sep;9(9):963-71. (PMID: 12181747)
Science. 1996 Dec 20;274(5295):2086-9. (PMID: 8953040)
Mol Cell. 2000 Mar;5(3):445-55. (PMID: 10882130)
J Cell Biol. 2006 Apr 10;173(1):95-106. (PMID: 16606693)
Nature. 2012 Apr 15;484(7395):542-5. (PMID: 22504180)
FASEB J. 1995 Jun;9(9):726-35. (PMID: 7601337)
Cell Rep. 2019 Jun 4;27(10):3049-3061.e6. (PMID: 31167147)
Curr Biol. 2016 Mar 7;26(5):670-7. (PMID: 26898471)
Proc Natl Acad Sci U S A. 2013 Mar 26;110(13):5058-63. (PMID: 23479629)
Development. 2014 Nov;141(21):4110-4. (PMID: 25336739)
Biomol Concepts. 2017 Sep 26;8(3-4):179-183. (PMID: 28873065)

EC 2.7.10.1 (ErbB Receptors)
0 (Drosophila Proteins)
EC 2.7.10.1 (Egfr protein, Drosophila)
EC 2.7.11.24 (Extracellular Signal-Regulated MAP Kinases)
0 (Receptors, Invertebrate Peptide)

Date Created: 20241014 Date Completed: 20241014 Latest Revision: 20241016

20241017

PMC11472926

10.1371/journal.pbio.3002823

39401187