Skip to main content
SpringerLink
Log in

Both Hoxc13 orthologs are functionally important for zebrafish tail fin regeneration

  • Original Article
  • Published:
Development Genes and Evolution Aims and scope Submit manuscript

Abstract

Hox genes are re-expressed during regeneration in many species. Given their important role in body plan development, it has been assumed, but not directly shown, that they play a functional role in regeneration. In this paper we show that morpholino-mediated knockdown of either Hoxc13a or Hoxc13b during the process of zebrafish tail fin regeneration results in a significant reduction of regenerative outgrowth. Furthermore, cellular proliferation within the blastema is directly affected in both knockdowns. Hence, similar to the demonstration of unique functions of multiple Hox genes during limb formation, both Hoxc13 orthologs have distinct functions in regeneration.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Amores A, Force A, Yan YL, Joly L, Amemiya C, Fritz A, Ho RK, Langeland J, Prince V, Wang YL, Westerfield M, Ekker M, Postlethwait JH (1998) Zebrafish hox clusters and vertebrate genome evolution. Science 282(5394):1711–1714

    Article  PubMed  CAS  Google Scholar 

  • Bai S, Thummel R, Godwin AR, Nagase H, Itoh Y, Li L, Evans R, McDermott J, Seiki M, Sarras MP Jr (2005) Matrix metalloproteinase expression and function during fin regeneration in zebrafish: analysis of MT1-MMP, MMP2 and TIMP2. Matrix Biol 24(4):247–260

    Article  PubMed  CAS  Google Scholar 

  • Bayascas JR, Castillo E, Munoz-Marmol AM, Salo E (1997) Planarian Hox genes: novel patterns of expression during regeneration. Development 124(1):141–148

    PubMed  CAS  Google Scholar 

  • Christen B, Beck CW, Lombardo A, Slack JM (2003) Regeneration-specific expression pattern of three posterior Hox genes. Dev Dyn 226(2):349–355

    Article  PubMed  CAS  Google Scholar 

  • Detrich HW, Westerfield M, Zon LI (1999) Methods in cell biology: the zebrafish: biology. Academic, New York, NY

    Google Scholar 

  • Dollé P, Izpisúa-Belmonte JC, Falkenstein H, Renucci A, Duboule D (1989) Coordinate expression of the murine Hox-5 complex homoeobox-containing genes during limb pattern formation. Nature 342(6251):767–772

    Article  PubMed  Google Scholar 

  • Dollé P, Izpisúa-Belmonte JC, Brown JM, Tickle C, Duboule D (1991) HOX-4 genes and the morphogenesis of mammalian genitalia. Genes Dev 5(10):1767–1777

    PubMed  Google Scholar 

  • Geraudie J, Borday Birraux V (2003) Posterior hoxa genes expression during zebrafish bony fin ray development and regeneration suggests their involvement in scleroblast differentiation. Dev Genes Evol 213(4):182–186

    PubMed  CAS  Google Scholar 

  • Godwin AR, Capecchi MR (1998) Hoxc13 mutant mice lack external hair. Genes Dev 12(1):11–20

    PubMed  CAS  Google Scholar 

  • Han M, Yang X, Farrington JE, Muneoka K (2003) Digit regeneration is regulated by Msx1 and BMP4 in fetal mice. Development 130(21):5123–5132

    Article  PubMed  CAS  Google Scholar 

  • Johnson SL, Weston JA (1995) Temperature-sensitive mutations that cause stage-specific defects in zebrafish fin regeneration. Genetics 141(4):1583–1595

    PubMed  CAS  Google Scholar 

  • Katogi R, Nakatani Y, Shin-i T, Kohara Y, Inohaya K, Kudo A (2004) Large-scale analysis of the genes involved in fin regeneration and blastema formation in the medaka, Oryzias latipes. Mech Dev 121(7–8):861–872

    Article  PubMed  CAS  Google Scholar 

  • McGinnis W, Krumlauf R (1992) Homeobox genes and axial patterning. Cell 68(2):283–302

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Nicolas S, Papillon D, Perez Y, Caubit X, Le Parco Y (2003) The spatial restrictions of 5′ HoxC genes expression are maintained in adult newt spinal cord. Biol Cell 95(9):589–594

    Article  PubMed  CAS  Google Scholar 

  • Orii H, Kato K, Umesono Y, Sakurai T, Agata K, Watanabe K (1999) The planarian HOM/HOX homeobox genes (Plox) expressed along the anteroposterior axis. Dev Biol 210(2):456–468

    Article  PubMed  CAS  Google Scholar 

  • Prince V (2002) The Hox Paradox: more complex(es) than imagined. Dev Biol 249(1):1–15

    Article  PubMed  CAS  Google Scholar 

  • Savard P, Gates PB, Brockes JP (1988) Position dependent expression of a homeobox gene transcript in relation to amphibian limb regeneration. EMBO J 7(13):4275–4282

    PubMed  CAS  Google Scholar 

  • Schughart K, Kappen C, Ruddle FH (1989) Duplication of large genomic regions during the evolution of vertebrate homeobox genes. Proc Natl Acad Sci USA 86(18):7067–7071

    Article  PubMed  CAS  Google Scholar 

  • Thummel R, Li L, Tanase C, Sarras MP Jr, Godwin AR (2004) Differences in expression pattern and function between zebrafish hoxc13 orthologs: recruitment of Hoxc13b into an early embryonic role. Dev Biol 274(2):318–333

    Article  PubMed  CAS  Google Scholar 

  • Thummel R, Bai S, Sarras MP Jr, Song P, McDermott J, Brewer J, Perry M, Zhang X, Hyde DR, Godwin AR (2006) Inhibition of zebrafish fin regeneration using in vivo electroporation of morpholinos against fgfr1 and msxb. Dev Dyn 235(2):336–346

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Wellik DM, Hawkes PJ, Capecchi MR (2002) Hox11 paralogous genes are essential for metanephric kidney induction. Genes Dev 16(11):1423–1432

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

This study was sponsored by a grant from the National Institutes of Health, Grant number: AR39189, AR47233, and DK61373.

Author information

Author notes

  1. Michael P. Sarras Jr.

    Present address: Department of Cell Biology and Anatomy, Rosalind Franklin University of Medicine and Science, North Chicago, IL, USA

Authors and Affiliations

  1. Department of Molecular and Integrative Physiology, University of Kansas Medical Center, Kansas City, KS, USA

    Ryan Thummel & Alan R. Godwin

  2. Center for Zebrafish Research and Department of Biological Sciences, University of Notre Dame, Notre Dame, IN, 46556, USA

    Ryan Thummel

  3. Department of Anatomy and Cell Biology, University of Kansas Medical Center, Kansas City, KS, USA

    Mila Ju & Michael P. Sarras Jr.

Authors
  1. Ryan Thummel
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mila Ju
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Michael P. Sarras Jr.
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Alan R. Godwin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ryan Thummel.

Additional information

Communicated by M. Hammerschmidt

Rights and permissions

Reprints and permissions

About this article

Cite this article

Thummel, R., Ju, M., Sarras, M.P. et al. Both Hoxc13 orthologs are functionally important for zebrafish tail fin regeneration. Dev Genes Evol 217, 413–420 (2007). https://doi.org/10.1007/s00427-007-0154-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00427-007-0154-3

Keywords

Search

Navigation