OpenLB
Open Library of Bioscience
Advanced Search
Cell death & disease
08 10, 2017;8 (8): e2979.

TNF signaling and macrophages govern fin regeneration in zebrafish larvae.

Mai Nguyen-Chi, Béryl Laplace-Builhé, Jana Travnickova, Patricia Luz-Crawford, Gautier Tejedor, Georges Lutfalla, Karima Kissa, Christian Jorgensen, Farida Djouad
Author Information
  1. Mai Nguyen-Chi: IRMB, INSERM, Univ Montpellier, Montpellier, France.
  2. Béryl Laplace-Builhé: IRMB, INSERM, Univ Montpellier, Montpellier, France.
  3. Jana Travnickova: Laboratorio de Immunologia Celular y Molecular, Facultad de Medicina, Universidad de Los Andes, Santiago, Chile.
  4. Patricia Luz-Crawford: IRMB, INSERM, Univ Montpellier, Montpellier, France.
  5. Gautier Tejedor: IRMB, INSERM, Univ Montpellier, Montpellier, France.
  6. Georges Lutfalla: DIMNP, CNRS, Univ Montpellier, Montpellier, France.
  7. Karima Kissa: DIMNP, CNRS, Univ Montpellier, Montpellier, France. ORCID
  8. Christian Jorgensen: IRMB, INSERM, Univ Montpellier, Montpellier, France.
  9. Farida Djouad: IRMB, INSERM, Univ Montpellier, Montpellier, France.
PMID: 28796253 DOI: 10.1038/cddis.2017.374

Abstract

Macrophages are essential for appendage regeneration after amputation in regenerative species. The molecular mechanisms through which macrophages orchestrate blastema formation and regeneration are still unclear. Here, we use the genetically tractable and transparent zebrafish larvae to study the functions of polarized macrophage subsets during caudal fin regeneration. After caudal fin amputation, we show an early and transient accumulation of pro-inflammatory macrophages concomitant with the accumulation of non-inflammatory macrophages which, in contrast to pro-inflammatory macrophages, remain associated to the fin until the end of the regeneration. Chemical and genetic depletion of macrophages suggested that early recruited macrophages that express TNFα are critical for blastema formation. Combining parabiosis and morpholino knockdown strategies, we show that TNFα/TNFR1 signaling pathway is required for the fin regeneration. Our study reveals that TNFR1 has a necessary and direct role in blastema cell activation suggesting that macrophage subset balance provides the accurate TNFα signal to prime regeneration in zebrafish.

References

  1. J Biol Chem. 2012 Jul 20;287(30):25353-60 [PMID: 22573321]
  2. Development. 2015 Jun 15;142(12):2136-46 [PMID: 26015541]
  3. Dev Dyn. 2003 Feb;226(2):190-201 [PMID: 12557198]
  4. PLoS Genet. 2012;8(10):e1003014 [PMID: 23133395]
  5. Dis Model Mech. 2014 Jul;7(7):871-82 [PMID: 24973754]
  6. J Neurosci. 2013 Apr 10;33(15):6524-39 [PMID: 23575850]
  7. Nat Immunol. 2010 Oct;11(10):889-96 [PMID: 20856220]
  8. J Clin Invest. 2012 Mar;122(3):787-95 [PMID: 22378047]
  9. Elife. 2015 Jul 08;4:e07288 [PMID: 26154973]
  10. Dis Model Mech. 2013 Mar;6(2):383-96 [PMID: 22956347]
  11. J Cell Biol. 2013 Mar 4;200(5):667-79 [PMID: 23460678]
  12. Elife. 2015 May 05;4:null [PMID: 25942455]
  13. Stem Cells. 2013 Feb;31(2):384-96 [PMID: 23169615]
  14. Dev Biol. 2015 Mar 1;399(1):80-90 [PMID: 25533245]
  15. J Biol Chem. 2007 Nov 30;282(48):35202-10 [PMID: 17848559]
  16. Trends Cell Biol. 2005 Nov;15(11):599-607 [PMID: 16202600]
  17. Proc Natl Acad Sci U S A. 2013 Jun 4;110(23):9415-20 [PMID: 23690624]
  18. Dev Dyn. 1995 Jul;203(3):253-310 [PMID: 8589427]
  19. PLoS One. 2012;7(12):e51766 [PMID: 23284763]
  20. Blood. 2006 Dec 15;108(13):3976-8 [PMID: 16926288]
  21. Curr Mol Med. 2001 Jul;1(3):317-24 [PMID: 11899080]
  22. Nat Commun. 2015 Feb 17;6:6227 [PMID: 25686881]
  23. FEBS J. 2013 Sep;280(17):4118-30 [PMID: 23384231]
  24. Cell Immunol. 1996 Jul 10;171(1):140-6 [PMID: 8660849]
  25. Nature. 2013 Apr 25;496(7446):445-55 [PMID: 23619691]
  26. Nat Rev Genet. 2006 Nov;7(11):873-84 [PMID: 17047686]
  27. Dev Biol. 2007 Apr 15;304(2):811-24 [PMID: 17335798]
  28. Methods Enzymol. 2012;506:135-56 [PMID: 22341223]
  29. Mediators Inflamm. 2015;2015:816460 [PMID: 26089604]
  30. Nature. 2009 Jun 18;459(7249):996-9 [PMID: 19494811]
  31. Adv Wound Care (New Rochelle). 2012 Feb;1(1):10-16 [PMID: 24527272]
  32. Transplant Proc. 2007 Jul-Aug;39(6):1761-4 [PMID: 17692605]
  33. Blood. 2011 Jan 27;117(4):e49-56 [PMID: 21084707]
  34. Surgery. 1991 Aug;110(2):192-8 [PMID: 1858029]
  35. Gerontology. 2010;56(2):231-40 [PMID: 19923791]
  36. J Exp Med. 2007 May 14;204(5):1057-69 [PMID: 17485518]
  37. J Neurosci. 2014 Oct 22;34(43):14403-19 [PMID: 25339752]
  38. J Immunol. 2009 Sep 15;183(6):3924-31 [PMID: 19717522]
  39. PLoS Pathog. 2013;9(9):e1003619 [PMID: 24039582]
  40. Nat Methods. 2013 Mar;10(3):256-8 [PMID: 23377378]
  41. Nat Rev Immunol. 2003 Jan;3(1):23-35 [PMID: 12511873]
  42. Trends Genet. 2013 Nov;29(11):611-20 [PMID: 23927865]
  43. Dev Dyn. 2004 Dec;231(4):693-9 [PMID: 15499559]
  44. Development. 2014 Jul;141(13):2581-91 [PMID: 24961798]
  45. Elife. 2017 Feb 23;6:null [PMID: 28229859]
  46. Immunobiology. 2014 Mar;219(3):172-8 [PMID: 24080029]

MeSH Term

Animals
Animals, Genetically Modified
Extremities
Larva
Macrophages
Receptors, Tumor Necrosis Factor, Type I
Regeneration
Signal Transduction
Tumor Necrosis Factor-alpha
Zebrafish
Zebrafish Proteins

Chemicals

Receptors, Tumor Necrosis Factor, Type I
Tumor Necrosis Factor-alpha
Zebrafish Proteins
Journal Article Research Support, Non-U.S. Gov't
Article has an altmetric score of 3

Word Cloud

Created with Highcharts 10.0.0regenerationmacrophagesfinblastemazebrafishamputationformationlarvaestudymacrophagecaudalshowearlyaccumulationpro-inflammatoryTNFαsignalingMacrophagesessentialappendageregenerativespeciesmolecularmechanismsorchestratestillunclearusegeneticallytractabletransparentfunctionspolarizedsubsetstransientconcomitantnon-inflammatorycontrastremainassociatedendChemicalgeneticdepletionsuggestedrecruitedexpresscriticalCombiningparabiosismorpholinoknockdownstrategiesTNFα/TNFR1pathwayrequiredrevealsTNFR1necessarydirectrolecellactivationsuggestingsubsetbalanceprovidesaccuratesignalprimeTNFgovern

Similar Articles

Cited By