BMP-gated cell-cycle progression drives anoikis during mesenchymal collective migration.

Item request has been placed! ×
Item request cannot be made. ×
loading   Processing Request
  • Author(s): Macabenta F;Macabenta F; Sun HT; Sun HT; Stathopoulos A; Stathopoulos A
  • Source:
    Developmental cell [Dev Cell] 2022 Jul 25; Vol. 57 (14), pp. 1683-1693.e3. Date of Electronic Publication: 2022 Jun 15.
  • Publication Type:
    Journal Article; Research Support, N.I.H., Extramural; Research Support, Non-U.S. Gov't
  • Language:
    English
  • Additional Information
    • Source:
      Publisher: Cell Press Country of Publication: United States NLM ID: 101120028 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1878-1551 (Electronic) Linking ISSN: 15345807 NLM ISO Abbreviation: Dev Cell Subsets: MEDLINE
    • Publication Information:
      Original Publication: Cambridge, Mass. : Cell Press, c2001-
    • Subject Terms:
    • Abstract:
      Tissue homeostasis involves the elimination of abnormal cells to avoid compromised patterning and function. Although quality control through cell competition is well studied in epithelial tissues, it is unknown if and how homeostasis is regulated in mesenchymal collectives. Here, we demonstrate that collectively migrating Drosophila muscle precursors utilize both fibroblast growth factor (FGF) and bone morphogenetic protein (BMP) signaling to promote homeostasis via anoikis, a form of cell death in response to substrate de-adhesion. Cell-cycle-regulated expression of the cell death gene head involution defective is responsible for caudal visceral mesoderm (CVM) anoikis. The secreted BMP ligand drives cell-cycle progression via a visceral mesoderm-specific cdc25/string enhancer to synchronize collective proliferation, as well as apoptosis of cells that have lost access to substrate-derived FGF. Perturbation of BMP-dependent cell-cycle progression is sufficient to confer anoikis resistance to mismigrating cells and thus facilitate invasion of other tissues. This BMP-gated cell-cycle checkpoint defines a quality control mechanism during mesenchymal collective migration.
      Competing Interests: Declaration of interests The authors declare no competing interests.
      (Copyright © 2022 Elsevier Inc. All rights reserved.)
    • References:
      Nature. 2012 Oct 25;490(7421):547-51. (PMID: 23023132)
      Development. 1990 Dec;110(4):1041-50. (PMID: 1983114)
      Development. 1994 Nov;120(11):3131-43. (PMID: 7720557)
      Cell. 1990 Aug 10;62(3):469-80. (PMID: 2199063)
      Nat Cell Biol. 2007 Jan;9(1):57-63. (PMID: 17143268)
      Cell. 2012 Feb 3;148(3):473-86. (PMID: 22304916)
      Nat Cell Biol. 2002 Jun;4(6):416-24. (PMID: 12021767)
      Cell. 1994 Feb 11;76(3):461-75. (PMID: 7906203)
      Development. 1990 Dec;110(4):1031-40. (PMID: 1983113)
      Biochim Biophys Acta. 2013 Dec;1833(12):3481-3498. (PMID: 23830918)
      Behav Res Methods. 2009 Nov;41(4):1149-60. (PMID: 19897823)
      Genetics. 1994 Sep;138(1):165-78. (PMID: 8001784)
      J Cell Biol. 2016 Jan 18;212(2):143-55. (PMID: 26783298)
      Science. 2005 Mar 18;307(5716):1785-9. (PMID: 15774762)
      Genes Dev. 1991 Oct;5(10):1881-91. (PMID: 1655572)
      Genes Dev. 1996 Jul 15;10(14):1773-82. (PMID: 8698237)
      Am J Pathol. 2005 Oct;167(4):1093-103. (PMID: 16192644)
      PLoS Genet. 2016 Mar 04;12(3):e1005909. (PMID: 26942411)
      Development. 2016 Sep 1;143(17):3206-15. (PMID: 27578182)
      Dev Biol. 2003 May 15;257(2):249-62. (PMID: 12729556)
      Genes Dev. 2007 Oct 1;21(19):2448-60. (PMID: 17908931)
      Development. 2012 Feb;139(4):699-708. (PMID: 22219352)
      Nature. 1995 Mar 30;374(6521):464-7. (PMID: 7700357)
      Proc Natl Acad Sci U S A. 1993 May 1;90(9):3899-903. (PMID: 8097881)
      Proc Natl Acad Sci U S A. 1997 May 13;94(10):5131-6. (PMID: 9144202)
      Cell. 2000 May 26;101(5):511-22. (PMID: 10850493)
      Genetics. 1989 Jul;122(3):643-52. (PMID: 2503418)
      Development. 2018 Oct 1;145(19):. (PMID: 30190277)
      Cell. 1994 Jul 29;78(2):251-61. (PMID: 8044839)
      Nat Cell Biol. 2002 Jun;4(6):432-8. (PMID: 12021769)
      Cell. 1999 Aug 20;98(4):453-63. (PMID: 10481910)
      Elife. 2017 Aug 04;6:. (PMID: 28826503)
      Dev Biol. 2013 Apr 15;376(2):245-59. (PMID: 23380635)
      Dev Biol. 2012 Aug 1;368(1):28-43. (PMID: 22609944)
      Apoptosis. 2009 Aug;14(8):943-9. (PMID: 19554451)
      Genes Dev. 1995 Jul 15;9(14):1694-708. (PMID: 7622034)
      Curr Biol. 2020 Aug 17;30(16):3141-3153.e5. (PMID: 32619487)
      Genes Dev. 1998 May 15;12(10):1495-503. (PMID: 9585509)
      Eur J Biochem. 1990 Aug 28;192(1):87-93. (PMID: 2401299)
      Nat Methods. 2012 Jun 28;9(7):676-82. (PMID: 22743772)
      Mol Cell. 1998 Oct;2(4):515-25. (PMID: 9809073)
      PLoS Genet. 2012;8(8):e1002831. (PMID: 22916021)
      Mech Dev. 1997 Dec;69(1-2):115-24. (PMID: 9486535)
      Elife. 2019 Feb 08;8:. (PMID: 30735120)
      Dev Dyn. 1994 Jan;199(1):28-44. (PMID: 8167377)
      Development. 2010 Jul;137(13):2167-75. (PMID: 20530544)
      Nat Cell Biol. 2002 Jun;4(6):439-44. (PMID: 12021770)
      Cell Mol Life Sci. 2013 Oct;70(19):3481-92. (PMID: 23314710)
      Cell Rep. 2014 Apr 24;7(2):588-598. (PMID: 24726363)
      Apoptosis. 2002 Apr;7(2):163-6. (PMID: 11865200)
      Nature. 2015 Nov 19;527(7578):375-8. (PMID: 26550824)
      Development. 2005 Jun;132(11):2645-56. (PMID: 15872004)
      Nature. 2009 Nov 5;462(7269):65-70. (PMID: 19890324)
      Am J Physiol Lung Cell Mol Physiol. 2003 Sep;285(3):L740-54. (PMID: 12740218)
      Science. 1996 Feb 9;271(5250):805-7. (PMID: 8628996)
      Mech Dev. 2017 Dec;148:40-55. (PMID: 28428068)
      EMBO J. 1994 Aug 1;13(15):3561-9. (PMID: 7914871)
      Genome Res. 2021 Oct;31(10):1938-1951. (PMID: 34389661)
      Genes Dev. 1996 Dec 1;10(23):3003-17. (PMID: 8957001)
      Cell. 1998 Oct 30;95(3):331-41. (PMID: 9814704)
      Curr Opin Genet Dev. 2019 Aug;57:39-46. (PMID: 31404788)
      EMBO J. 2000 Feb 15;19(4):589-97. (PMID: 10675328)
      Cell. 1998 Oct 30;95(3):319-29. (PMID: 9814703)
      Nature. 2014 Aug 7;512(7512):91-5. (PMID: 24896182)
      Dev Cell. 2005 Oct;9(4):463-75. (PMID: 16198289)
      Nat Cell Biol. 2013 Jul;15(7):763-72. (PMID: 23770678)
      Cell. 1994 Jul 29;78(2):239-50. (PMID: 8044838)
      Development. 2019 Jul 16;146(14):. (PMID: 31239242)
      Dev Dyn. 2004 Oct;231(2):342-8. (PMID: 15366011)
      Genetics. 1995 Sep;141(1):271-81. (PMID: 8536976)
      Curr Opin Cell Biol. 2012 Oct;24(5):677-84. (PMID: 22944726)
      Dev Biol. 2009 Feb 15;326(2):347-56. (PMID: 19100727)
    • Grant Information:
      R01 HD100189 United States HD NICHD NIH HHS
    • Contributed Indexing:
      Keywords: BMP signaling; FGF signaling; anoikis; caudal visceral mesoderm; cell cycle; cell death; cell migration; decapentaplegic; tolkin
    • Accession Number:
      0 (Bone Morphogenetic Proteins)
      62031-54-3 (Fibroblast Growth Factors)
    • Publication Date:
      Date Created: 20220616 Date Completed: 20220801 Latest Revision: 20230726
    • Publication Date:
      20240105
    • Accession Number:
      PMC9339487
    • Accession Number:
      10.1016/j.devcel.2022.05.017
    • Accession Number:
      35709766