Transient 1a Induction Defines the Wound Epidermis during Zebrafish Fin Regeneration

English version České info

Unlike mammals, adult teleost fish and urodele amphibians can fully regenerate lost appendages. Understanding what initiates regeneration in these vertebrates is of great interest to the scientific community. It has long been known that the epidermis that forms quickly over an amputated limb stump is critical for initiating regenerative programs. Yet, little of understood of the molecular and cellular mechanisms by which a simple adult epithelium transforms into this key signaling source. Here, we performed a large-scale, unbiased genetic screen for epithelial signaling deficiencies during the regeneration of amputated adult zebrafish fins, from which we identified several new mutants. One gene identified from this screen disrupts a specific component of the extracellular matrix material Laminin, Laminin beta 1a, a factor that we find to be dispensable in uninjured adult animals but required for all stages fin regeneration. Transient induction of this component by amputation polarizes the basal layer of the nascent epithelium, and, in turn, facilitates the synthesis of signaling factors, the positioning of ligand receptors, and the patterning of new bone cells. We also find that normal induction of Laminin beta 1a by injury relies on the function of Fibroblast growth factors, secreted polypeptide signals that are released early upon injury. Our results identify key early steps in the endogenous program for vertebrate appendage regeneration.

Vyšlo v časopise: Transient 1a Induction Defines the Wound Epidermis during Zebrafish Fin Regeneration. PLoS Genet 11(8): e32767. doi:10.1371/journal.pgen.1005437
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005437

Souhrn

Zdroje

1. Johnson SL, Weston JA. Temperature-sensitive mutations that cause stage-specific defects in Zebrafish fin regeneration. Genetics. 1995;141(4):1583–95. 8601496.

2. Becker T, Wullimann MF, Becker CG, Bernhardt RR, Schachner M. Axonal regrowth after spinal cord transection in adult zebrafish. J Comp Neurol. 1997;377(4):577–95. 9007194.

3. Vihtelic TS, Hyde DR. Light-induced rod and cone cell death and regeneration in the adult albino zebrafish (Danio rerio) retina. J Neurobiol. 2000;44(3):289–307. 10942883.

4. Diep CQ, Ma D, Deo RC, Holm TM, Naylor RW, Arora N, et al. Identification of adult nephron progenitors capable of kidney regeneration in zebrafish. Nature. 2011;470(7332):95–100. doi: 10.1038/nature09669 21270795.

5. Goldshmit Y, Sztal TE, Jusuf PR, Hall TE, Nguyen-Chi M, Currie PD. Fgf-dependent glial cell bridges facilitate spinal cord regeneration in zebrafish. J Neurosci. 2012;32(22):7477–92. doi: 10.1523/JNEUROSCI.0758-12.2012 22649227.

6. Kizil C, Kyritsis N, Dudczig S, Kroehne V, Freudenreich D, Kaslin J, et al. Regenerative neurogenesis from neural progenitor cells requires injury-induced expression of Gata3. Dev Cell. 2012;23(6):1230–7. doi: 10.1016/j.devcel.2012.10.014 23168169.

7. Poss KD, Wilson LG, Keating MT. Heart regeneration in zebrafish. Science. 2002;298(5601):2188–90. doi: 10.1126/science.1077857 12481136.

8. Poss KD. Advances in understanding tissue regenerative capacity and mechanisms in animals. Nat Rev Genet. 2010;11(10):710–22. doi: 10.1038/nrg2879 20838411.

9. Poleo G, Brown CW, Laforest L, Akimenko MA. Cell proliferation and movement during early fin regeneration in zebrafish. Dev Dyn. 2001;221(4):380–90. doi: 10.1002/dvdy.1152 11500975.

10. Santos-Ruiz L, Santamaria JA, Ruiz-Sanchez J, Becerra J. Cell proliferation during blastema formation in the regenerating teleost fin. Dev Dyn. 2002;223(2):262–72. doi: 10.1002/dvdy.10055 11836790.

11. Mescher AL. Effects on adult newt limb regeneration of partial and complete skin flaps over the amputation surface. J Exp Zool. 1976;195(1):117–28. doi: 10.1002/jez.1401950111 1255117.

12. Thornton CS. The effect of apical cap removal on limb regeneration in Amblystoma larvae. J Exp Zool. 1957;134(2):357–81. 13428959.

13. Tassava RA, Garling DJ. Regenerative responses in larval axolotl limbs with skin grafts over the amputation surface. J Exp Zool. 1979;208(1):97–110. doi: 10.1002/jez.1402080111 381569.

14. Yoshinari N, Kawakami A. Mature and juvenile tissue models of regeneration in small fish species. Biol Bull. 2011;221(1):62–78. 21876111.

15. Quint E, Smith A, Avaron F, Laforest L, Miles J, Gaffield W, et al. Bone patterning is altered in the regenerating zebrafish caudal fin after ectopic expression of sonic hedgehog and bmp2b or exposure to cyclopamine. Proc Natl Acad Sci U S A. 2002;99(13):8713–8. doi: 10.1073/pnas.122571799 12060710.

16. Stewart S, Gomez AW, Armstrong BE, Henner A, Stankunas K. Sequential and opposing activities of Wnt and BMP coordinate zebrafish bone regeneration. Cell Rep. 2014;6(3):482–98. doi: 10.1016/j.celrep.2014.01.010 24485659.

17. Wehner D, Cizelsky W, Vasudevaro MD, Ozhan G, Haase C, Kagermeier-Schenk B, et al. Wnt/beta-catenin signaling defines organizing centers that orchestrate growth and differentiation of the regenerating zebrafish caudal fin. Cell Rep. 2014;6(3):467–81. doi: 10.1016/j.celrep.2013.12.036 24485658.

18. Stoick-Cooper CL, Weidinger G, Riehle KJ, Hubbert C, Major MB, Fausto N, et al. Distinct Wnt signaling pathways have opposing roles in appendage regeneration. Development. 2007;134(3):479–89. doi: 10.1242/dev.001123 17185322.

19. Kawakami Y, Rodriguez Esteban C, Raya M, Kawakami H, Marti M, Dubova I, et al. Wnt/beta-catenin signaling regulates vertebrate limb regeneration. Genes Dev. 2006;20(23):3232–7. doi: 10.1101/gad.1475106 17114576.

20. Whitehead GG, Makino S, Lien CL, Keating MT. fgf20 is essential for initiating zebrafish fin regeneration. Science. 2005;310(5756):1957–60. doi: 10.1126/science.1117637 16373575.

21. Chablais F, Jazwinska A. IGF signaling between blastema and wound epidermis is required for fin regeneration. Development. 2010;137(6):871–9. doi: 10.1242/dev.043885 20179093.

22. Poss KD, Shen J, Nechiporuk A, McMahon G, Thisse B, Thisse C, et al. Roles for Fgf signaling during zebrafish fin regeneration. Dev Biol. 2000;222(2):347–58. doi: 10.1006/dbio.2000.9722 10837124.

23. Jazwinska A, Badakov R, Keating MT. Activin-betaA signaling is required for zebrafish fin regeneration. Curr Biol. 2007;17(16):1390–5. doi: 10.1016/j.cub.2007.07.019 17683938.

24. Grotek B, Wehner D, Weidinger G. Notch signaling coordinates cellular proliferation with differentiation during zebrafish fin regeneration. Development. 2013;140(7):1412–23. doi: 10.1242/dev.087452 23462472.

25. Munch J, Gonzalez-Rajal A, de la Pompa JL. Notch regulates blastema proliferation and prevents differentiation during adult zebrafish fin regeneration. Development. 2013;140(7):1402–11. doi: 10.1242/dev.087346 23344707.

26. Blum N, Begemann G. Retinoic acid signaling controls the formation, proliferation and survival of the blastema during adult zebrafish fin regeneration. Development. 2012;139(1):107–16. doi: 10.1242/dev.065391 22096078.

27. Kujawski S, Lin W, Kitte F, Bormel M, Fuchs S, Arulmozhivarman G, et al. Calcineurin regulates coordinated outgrowth of zebrafish regenerating fins. Dev Cell. 2014;28(5):573–87. doi: 10.1016/j.devcel.2014.01.019 24561038.

28. Poss KD, Nechiporuk A, Hillam AM, Johnson SL, Keating MT. Mps1 defines a proximal blastemal proliferative compartment essential for zebrafish fin regeneration. Development. 2002;129(22):5141–9. 12399306.

29. Streisinger G, Singer F, Walker C, Knauber D, Dower N. Segregation analyses and gene-centromere distances in zebrafish. Genetics. 1986;112(2):311–9. 3455686.

30. Poss KD, Shen J, Keating MT. Induction of lef1 during zebrafish fin regeneration. Dev Dyn. 2000;219(2):282–6. doi: 10.1002/1097-0177(2000)9999:9999<::AID-DVDY1045>3.0.CO;2-C 11002347.

31. Lee Y, Hami D, De Val S, Kagermeier-Schenk B, Wills AA, Black BL, et al. Maintenance of blastemal proliferation by functionally diverse epidermis in regenerating zebrafish fins. Dev Biol. 2009;331(2):270–80. doi: 10.1016/j.ydbio.2009.05.545 19445916.

32. Nechiporuk A, Poss KD, Johnson SL, Keating MT. Positional cloning of a temperature-sensitive mutant emmental reveals a role for sly1 during cell proliferation in zebrafish fin regeneration. Dev Biol. 2003;258(2):291–306. 12798289.

33. Makino S, Whitehead GG, Lien CL, Kim S, Jhawar P, Kono A, et al. Heat-shock protein 60 is required for blastema formation and maintenance during regeneration. Proc Natl Acad Sci U S A. 2005;102(41):14599–604. doi: 10.1073/pnas.0507408102 16204379.

34. Wills AA, Kidd AR 3rd, Lepilina A, Poss KD. Fgfs control homeostatic regeneration in adult zebrafish fins. Development. 2008;135(18):3063–70. doi: 10.1242/dev.024588 18701543.

35. Singh SP, Holdway JE, Poss KD. Regeneration of amputated zebrafish fin rays from de novo osteoblasts. Dev Cell. 2012;22(4):879–86. doi: 10.1016/j.devcel.2012.03.006 22516203.

36. Ryan S, Willer J, Marjoram L, Bagwell J, Mankiewicz J, Leshchiner I, et al. Rapid identification of kidney cyst mutations by whole exome sequencing in zebrafish. Development. 2013;140(21):4445–51. doi: 10.1242/dev.101170 24130329.

37. Leshchiner I, Alexa K, Kelsey P, Adzhubei I, Austin-Tse CA, Cooney JD, et al. Mutation mapping and identification by whole-genome sequencing. Genome Res. 2012;22(8):1541–8. doi: 10.1101/gr.135541.111 22555591.

38. Meyer A, Van de Peer Y. From 2R to 3R: evidence for a fish-specific genome duplication (FSGD). Bioessays. 2005;27(9):937–45. doi: 10.1002/bies.20293 16108068.

39. Yurchenco PD, Cheng YS. Self-assembly and calcium-binding sites in laminin. A three-arm interaction model. J Biol Chem. 1993;268(23):17286–99. 8349613.

40. Odenthal U, Haehn S, Tunggal P, Merkl B, Schomburg D, Frie C, et al. Molecular analysis of laminin N-terminal domains mediating self-interactions. J Biol Chem. 2004;279(43):44504–12. doi: 10.1074/jbc.M402455200 15310759.

41. Parsons MJ, Pollard SM, Saude L, Feldman B, Coutinho P, Hirst EM, et al. Zebrafish mutants identify an essential role for laminins in notochord formation. Development. 2002;129(13):3137–46. 12070089.

42. Hochgreb-Hagele T, Yin C, Koo DE, Bronner ME, Stainier DY. Laminin beta1a controls distinct steps during the establishment of digestive organ laterality. Development. 2013;140(13):2734–45. doi: 10.1242/dev.097618 23757411

43. McCaffrey LM, Macara IG. Signaling pathways in cell polarity. Cold Spring Harb Perspect Biol. 2012;4(6). doi: 10.1101/cshperspect.a009654 22553378.

44. O'Brien LE, Jou TS, Pollack AL, Zhang Q, Hansen SH, Yurchenco P, et al. Rac1 orientates epithelial apical polarity through effects on basolateral laminin assembly. Nat Cell Biol. 2001;3(9):831–8. doi: 10.1038/ncb0901-831 11533663.

45. Klein G, Langegger M, Timpl R, Ekblom P. Role of laminin A chain in the development of epithelial cell polarity. Cell. 1988;55(2):331–41. 3048705.

46. Rasmussen JP, Reddy SS, Priess JR. Laminin is required to orient epithelial polarity in the C. elegans pharynx. Development. 2012;139(11):2050–60. doi: 10.1242/dev.078360 22535412.

47. Li X, Chen Y, Scheele S, Arman E, Haffner-Krausz R, Ekblom P, et al. Fibroblast growth factor signaling and basement membrane assembly are connected during epithelial morphogenesis of the embryoid body. J Cell Biol. 2001;153(4):811–22. 11352941.

48. Lee Y, Grill S, Sanchez A, Murphy-Ryan M, Poss KD. Fgf signaling instructs position-dependent growth rate during zebrafish fin regeneration. Development. 2005;132(23):5173–83. doi: 10.1242/dev.02101 16251209.

49. Wehner D, Weidinger G. Signaling networks organizing regenerative growth of the zebrafish fin. Trends Genet. 2015. doi: 10.1016/j.tig.2015.03.012 25929514.

50. Contreras EG, Gaete M, Sanchez N, Carrasco H, Larrain J. Early requirement of Hyaluronan for tail regeneration in Xenopus tadpoles. Development. 2009;136(17):2987–96. doi: 10.1242/dev.035501 19666825.

51. Mercer SE, Odelberg SJ, Simon HG. A dynamic spatiotemporal extracellular matrix facilitates epicardial-mediated vertebrate heart regeneration. Dev Biol. 2013;382(2):457–69. doi: 10.1016/j.ydbio.2013.08.002 23939298.

52. Wang J, Karra R, Dickson AL, Poss KD. Fibronectin is deposited by injury-activated epicardial cells and is necessary for zebrafish heart regeneration. Dev Biol. 2013;382(2):427–35. doi: 10.1016/j.ydbio.2013.08.012 23988577.

53. Webb AE, Sanderford J, Frank D, Talbot WS, Driever W, Kimelman D. Laminin alpha5 is essential for the formation of the zebrafish fins. Dev Biol. 2007;311(2):369–82. doi: 10.1016/j.ydbio.2007.08.034 17919534.

54. Carney TJ, Feitosa NM, Sonntag C, Slanchev K, Kluger J, Kiyozumi D, et al. Genetic analysis of fin development in zebrafish identifies furin and hemicentin1 as potential novel fraser syndrome disease genes. PLoS Genet. 2010;6(4):e1000907. doi: 10.1371/journal.pgen.1000907 20419147.

55. Domogatskaya A, Rodin S, Tryggvason K. Functional diversity of laminins. Annu Rev Cell Dev Biol. 2012;28:523–53. doi: 10.1146/annurev-cellbio-101011-155750 23057746.

56. Nagendran M, Arora P, Gori P, Mulay A, Ray S, Jacob T, et al. Canonical Wnt signalling regulates epithelial patterning by modulating levels of laminins in zebrafish appendages. Development. 2014. doi: 10.1242/dev.118703 25519245.

57. Rohner N, Bercsenyi M, Orban L, Kolanczyk ME, Linke D, Brand M, et al. Duplication of fgfr1 permits Fgf signaling to serve as a target for selection during domestication. Curr Biol. 2009;19(19):1642–7. doi: 10.1016/j.cub.2009.07.065 19733072.

58. Trevarrow B. Techniques for optimizing the creation of mutations in zebrafish using N-ethyl-N-nitrosourea. Lab Anim (NY). 2011;40(11):353–61. doi: 10.1038/laban1111-353 22012195.

59. Salic A, Mitchison TJ. A chemical method for fast and sensitive detection of DNA synthesis in vivo. Proc Natl Acad Sci U S A. 2008;105(7):2415–20. doi: 10.1073/pnas.0712168105 18272492.

60. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 2001;25(4):402–8. doi: 10.1006/meth.2001.1262 11846609.