ERK-activated CK-2 triggers blastema formation during appendage regeneration.

Xiao-Shuai Zhang, Lin Wei, Wei Zhang, Fei-Xue Zhang, Lin Li, Liang Li, Yejie Wen, Jia-Hui Zhang, Suning Liu, Dongwei Yuan, Yanmei Liu, Chonghua Ren, Sheng Li
Author Information
  1. Xiao-Shuai Zhang: Guangdong Provincial Key Laboratory of Insect Developmental Biology and Applied Technology, Guangzhou Key Laboratory of Insect Development Regulation and Application Research, Institute of Insect Science and Technology & School of Life Sciences, South China Normal University, Guangzhou 510631, China. ORCID
  2. Lin Wei: Guangdong Provincial Key Laboratory of Insect Developmental Biology and Applied Technology, Guangzhou Key Laboratory of Insect Development Regulation and Application Research, Institute of Insect Science and Technology & School of Life Sciences, South China Normal University, Guangzhou 510631, China. ORCID
  3. Wei Zhang: Guangdong Provincial Key Laboratory of Insect Developmental Biology and Applied Technology, Guangzhou Key Laboratory of Insect Development Regulation and Application Research, Institute of Insect Science and Technology & School of Life Sciences, South China Normal University, Guangzhou 510631, China. ORCID
  4. Fei-Xue Zhang: Guangdong Provincial Key Laboratory of Insect Developmental Biology and Applied Technology, Guangzhou Key Laboratory of Insect Development Regulation and Application Research, Institute of Insect Science and Technology & School of Life Sciences, South China Normal University, Guangzhou 510631, China.
  5. Lin Li: Guangdong Provincial Key Laboratory of Insect Developmental Biology and Applied Technology, Guangzhou Key Laboratory of Insect Development Regulation and Application Research, Institute of Insect Science and Technology & School of Life Sciences, South China Normal University, Guangzhou 510631, China.
  6. Liang Li: Guangdong Provincial Key Laboratory of Insect Developmental Biology and Applied Technology, Guangzhou Key Laboratory of Insect Development Regulation and Application Research, Institute of Insect Science and Technology & School of Life Sciences, South China Normal University, Guangzhou 510631, China. ORCID
  7. Yejie Wen: Guangdong Provincial Key Laboratory of Insect Developmental Biology and Applied Technology, Guangzhou Key Laboratory of Insect Development Regulation and Application Research, Institute of Insect Science and Technology & School of Life Sciences, South China Normal University, Guangzhou 510631, China.
  8. Jia-Hui Zhang: Guangdong Provincial Key Laboratory of Insect Developmental Biology and Applied Technology, Guangzhou Key Laboratory of Insect Development Regulation and Application Research, Institute of Insect Science and Technology & School of Life Sciences, South China Normal University, Guangzhou 510631, China. ORCID
  9. Suning Liu: Guangdong Provincial Key Laboratory of Insect Developmental Biology and Applied Technology, Guangzhou Key Laboratory of Insect Development Regulation and Application Research, Institute of Insect Science and Technology & School of Life Sciences, South China Normal University, Guangzhou 510631, China. ORCID
  10. Dongwei Yuan: Guangdong Provincial Key Laboratory of Insect Developmental Biology and Applied Technology, Guangzhou Key Laboratory of Insect Development Regulation and Application Research, Institute of Insect Science and Technology & School of Life Sciences, South China Normal University, Guangzhou 510631, China. ORCID
  11. Yanmei Liu: Key Laboratory of Brain, Cognition and Education Sciences, Ministry of Education, Institute for Brain Research and Rehabilitation, South China Normal University, Guangzhou 510631, China. ORCID
  12. Chonghua Ren: Guangdong Provincial Key Laboratory of Insect Developmental Biology and Applied Technology, Guangzhou Key Laboratory of Insect Development Regulation and Application Research, Institute of Insect Science and Technology & School of Life Sciences, South China Normal University, Guangzhou 510631, China. ORCID
  13. Sheng Li: Guangdong Provincial Key Laboratory of Insect Developmental Biology and Applied Technology, Guangzhou Key Laboratory of Insect Development Regulation and Application Research, Institute of Insect Science and Technology & School of Life Sciences, South China Normal University, Guangzhou 510631, China. ORCID

Abstract

Appendage regeneration relies on the formation of blastema, a heterogeneous cellular structure formed at the injury site. However, little is known about the early injury-activated signaling pathways that trigger blastema formation during appendage regeneration. Here, we provide compelling evidence that the extracellular signal-regulated kinase (ERK)-activated casein kinase 2 (CK-2), which has not been previously implicated in appendage regeneration, triggers blastema formation during leg regeneration in the American cockroach, . After amputation, CK-2 undergoes rapid activation through ERK-induced phosphorylation within blastema cells. RNAi knockdown of severely impairs blastema formation by repressing cell proliferation through down-regulating mitosis-related genes. Evolutionarily, the regenerative role of CK-2 is conserved in zebrafish caudal fin regeneration via promoting blastema cell proliferation. Together, we find and demonstrate that the ERK-activated CK-2 triggers blastema formation in both cockroach and zebrafish, helping explore initiation factors during appendage regeneration.

References

  1. Development. 2009 Jul;136(13):2235-45 [PMID: 19474149]
  2. Biochem Biophys Res Commun. 2011 Apr 22;407(4):680-6 [PMID: 21440529]
  3. Dev Biol. 2008 Jul 1;319(1):46-55 [PMID: 18486122]
  4. Nat Commun. 2021 Dec 9;12(1):7153 [PMID: 34887421]
  5. Nat Commun. 2022 May 18;13(1):2726 [PMID: 35585061]
  6. Nat Rev Genet. 2020 Sep;21(9):511-525 [PMID: 32504079]
  7. Elife. 2020 Jan 14;9: [PMID: 31934849]
  8. Cell. 1995 Jan 27;80(2):179-85 [PMID: 7834738]
  9. J Biol Chem. 2023 Mar;299(3):102950 [PMID: 36717080]
  10. Cell Mol Life Sci. 2021 Mar;78(5):2185-2197 [PMID: 32909120]
  11. Development. 2011 Jun;138(12):2417-27 [PMID: 21610023]
  12. Nature. 2021 Feb;590(7844):129-133 [PMID: 33408418]
  13. Mech Dev. 2002 Jun;114(1-2):27-35 [PMID: 12175487]
  14. Nature. 2009 Jul 2;460(7251):60-5 [PMID: 19571878]
  15. Cell Rep. 2018 Nov 27;25(9):2577-2590.e3 [PMID: 30485821]
  16. Cell Rep. 2024 Feb 27;43(3):113889 [PMID: 38416646]
  17. Development. 2022 Apr 15;149(8): [PMID: 34622924]
  18. Curr Biol. 2019 Dec 2;29(23):R1252-R1268 [PMID: 31794762]
  19. Cell Regen. 2023 Mar 2;12(1):9 [PMID: 36859631]
  20. Sci Rep. 2015 Feb 11;5:8387 [PMID: 25669615]
  21. Enzymes. 2016;39:231-54 [PMID: 27241932]
  22. Nature. 2002 Dec 19-26;420(6917):816-20 [PMID: 12447397]
  23. Nat Rev Genet. 2010 Oct;11(10):710-22 [PMID: 20838411]
  24. Science. 2011 May 13;332(6031):852-5 [PMID: 21566195]
  25. Cell Rep. 2013 Mar 28;3(3):607-14 [PMID: 23478024]
  26. Elife. 2021 May 18;10: [PMID: 34003110]
  27. PLoS Genet. 2015 Oct 23;11(10):e1005595 [PMID: 26496642]
  28. Curr Biol. 2020 Jun 8;30(11):2166-2174.e3 [PMID: 32386527]
  29. Proc Natl Acad Sci U S A. 2022 Aug 30;119(35):e2204122119 [PMID: 35994642]
  30. Dev Cell. 2009 Jun;16(6):797-809 [PMID: 19531351]
  31. Cell. 2016 Jun 16;165(7):1598-1608 [PMID: 27315477]
  32. Development. 2013 Mar;140(5):959-64 [PMID: 23344706]
  33. Science. 2023 Feb 24;379(6634):840-847 [PMID: 36821675]
  34. Dev Dyn. 2000 Oct;219(2):282-6 [PMID: 11002347]
  35. J Embryol Exp Morphol. 1983 Jun;75:151-64 [PMID: 6886608]
  36. Cell. 2020 Aug 6;182(3):685-712.e19 [PMID: 32645325]
  37. Nature. 1990 Feb 15;343(6259):651-3 [PMID: 2154696]
  38. Insect Biochem Mol Biol. 2021 Apr;131:103552 [PMID: 33577967]
  39. Biochim Biophys Acta Mol Cell Res. 2023 Feb;1870(2):119389 [PMID: 36372111]
  40. Nature. 2013 Aug 1;500(7460):73-6 [PMID: 23883928]
  41. Nature. 2014 Dec 11;516(7530):267-71 [PMID: 25252977]
  42. Nat Commun. 2022 Jun 14;13(1):3421 [PMID: 35701400]
  43. Dev Cell. 2018 Mar 12;44(5):582-596.e4 [PMID: 29533773]
  44. PLoS Genet. 2019 Jan 24;15(1):e1007926 [PMID: 30677014]
  45. Elife. 2022 Aug 22;11: [PMID: 35993337]
  46. Proc Natl Acad Sci U S A. 2017 Sep 12;114(37):E7832-E7840 [PMID: 28847950]
  47. Nat Commun. 2022 Aug 22;13(1):4794 [PMID: 35995781]
  48. Stem Cell Reports. 2014 Jun 19;3(1):15-23 [PMID: 25068118]
  49. Nat Commun. 2018 Mar 20;9(1):1008 [PMID: 29559629]
  50. Proc Natl Acad Sci U S A. 2015 May 5;112(18):E2327-36 [PMID: 25902518]
  51. Dev Neurobiol. 2019 May;79(5):424-436 [PMID: 30600647]
  52. Development. 2019 Jul 22;146(14): [PMID: 31332037]
  53. Sci Adv. 2022 Sep 2;8(35):eabo1215 [PMID: 36044577]
  54. Dev Growth Differ. 2010 Jan;52(1):89-99 [PMID: 19891640]
  55. Development. 2015 Dec 15;142(24):4217-29 [PMID: 26525673]
  56. Dev Cell. 2011 Jul 19;21(1):172-85 [PMID: 21763617]
  57. Dev Biol. 2007 Sep 1;309(1):56-69 [PMID: 17643406]
  58. Curr Biol. 2006 Jun 20;16(12):1171-82 [PMID: 16782007]
  59. Biochem J. 1997 May 1;323 ( Pt 3):621-7 [PMID: 9169593]
  60. Cell Regen. 2021 Apr 5;10(1):12 [PMID: 33817749]
  61. Mol Cell. 2009 Nov 25;36(4):547-59 [PMID: 19941816]
  62. Mol Biol Cell. 2023 May 15;34(6):ar60 [PMID: 36884295]
  63. Dev Biol. 2007 Apr 15;304(2):675-86 [PMID: 17303106]
  64. Mech Dev. 2006 Sep;123(9):649-64 [PMID: 16930955]
  65. Commun Biol. 2021 Apr 7;4(1):409 [PMID: 33828226]

MeSH Term

Animals
Zebrafish
Regeneration
Wound Healing
Signal Transduction
Zebrafish Proteins

Chemicals

Zebrafish Proteins

Word Cloud

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