Skip to main content

Advertisement

Log in

Involvement of JNK in the Embryonic Development and Organogenesis in Zebrafish

  • Original Article
  • Published:
Marine Biotechnology Aims and scope Submit manuscript

Abstract

c-Jun N-terminal kinase (JNK) is one of the mitogen-activated protein kinases. Previous studies showed that the JNK is involved in signaling pathways initiating cell cycle, and eventually, causing apoptosis through persistent activation in mammals. In this article, it is further revealed that the jnk1 gene is closely related with the embryonic development and organogenesis in zebrafish. RT-PCR and Western blot analysis show that there were distinct expression patterns of JNK at the different developmental stages as well as in the various tissues in zebrafish. Knockdown of jnk1 by RNA interference (RNAi) resulted in high lethal, serious retardation and malformations of embryos in zebrafish. SP600125, a JNK-specific inhibitor, gives rise to high mortality in zebrafish, similar to that caused by the jnk1 RNA interference. SP600125 is also responsible for the severe abnormality of organs, especially the skeletal system, such as skull, mandible deficiency, and cyrtosis heterauxesis. The results also indicate that the inhibition of JNK by SP600125 suppresses the ovarian differentiation during the embryo development in zebrafish. Overall, our study demonstrates that the jnk1 gene is required for ovary differentiation and development in the zebrafish, and down-regulated JNK directly inhibits ovary differentiation during early ontogenetic stages.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Adachi YT, O'Connor MB (2002) Morphogenetic apoptosis: a mechanism for correcting discontinuities in morphogen gradients. Dev Biol 251:74–90

    Article  Google Scholar 

  • Bennett BL, Sasaki DT, Murray BW (2001) SP600125, an anthrapyrazolone inhibitor of Jun N-terminal kinase. Proc Natl Acad Sci U S A 98:13681–13686

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Celil AB, Campbell PG et al (2005) BMP-2 and insulin-like growth factor-I mediate Osterix (Osx) expression in human mesenchymal stem cells via the MAPK and protein kinase signaling pathways. J Biol Chem 280:31353–31359

    Article  CAS  PubMed  Google Scholar 

  • Chambon JP, Nakayama A, Takamura K et al (2007) ERK- and JNK-signalling regulate gene networks that stimulate metamorphosis and apoptosis in tail tissues of ascidian tadpoles. Development 134:1203–1219

    Article  CAS  PubMed  Google Scholar 

  • Chen LL, Xiao YM, Zhao RR, Liu Y (2006) A report about the new development of gonad in Monopterus albus. Acta Hydrobiol Sin 30:621–624

    Google Scholar 

  • Drivenes Ø, Taranger GL, Edvardsen RB (2012) Gene expression profiling of Atlantic cod (Gadus morhua) embryogenesis using microarray. Mar Biotechnol 14(2):167–176

    Article  CAS  PubMed  Google Scholar 

  • Fernández CG, Roufidou C, Antonopoulou E, Sarropoulou E (2012) Expression of developmental-stage-specific genes in the gilthead sea bream Sparus aurata L. Mar Biotechnol (NY) 15(3):313–320

    Article  Google Scholar 

  • Fukuda K, Tesch GH, Nikolic PDJ (2008) c-Jun amino terminal kinase 1 deficient mice are protected from streptozotocin-induced islet injury. Biochem Biophys Res Commun 366:710–716

    Article  CAS  PubMed  Google Scholar 

  • Guicheux J, Lemonnier J, Ghayor C et al (2003) Activation of p38 mitogen-activated protein kinase and c-Jun-NH2-terminal kinase by BMP-2 and their implication in the stimulation of osteoblastic cell differentiation. J Bone Miner Res 18:2060–2068

    Article  CAS  PubMed  Google Scholar 

  • Gupta S, Barrett T, Whitmarsh AJ, Cavanagh J, Sluss HK, De′rijard B, Davis RJ (1996) Selective interaction of JNK protein kinase isoforms with transcription factors. EMBO J 15:2760–2770

    PubMed Central  CAS  PubMed  Google Scholar 

  • Hanks SK, Quinn AM, Hunter T (1988) The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. Science 241:42–52

    Article  CAS  PubMed  Google Scholar 

  • Johnson GL, Nakamura K (2007) The c-jun kinase/stress-activated pathway: regulation, function and role in human disease. Biochim Biophys Acta 1773:1341–1348

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Liu D, Liu S, You C, Chen L, Liu Z, Liu L, Wang J, Liu Y (2010) Identification and expression analysis of genes involved in early ovary development in diploid gynogenetic hybrids of red crucian carp x common carp. Mar Biotechnol 12(2):186–194

    Article  CAS  PubMed  Google Scholar 

  • Nateri AS, Spencer DB, Behrens A (2005) Interaction of phosphorylated c-Jun with TCF4 regulates intestinal cancer development. Nature 437:281–285

    Article  CAS  PubMed  Google Scholar 

  • Piferrer F, Ribas L, Díaz N (2012) Genomic approaches to study genetic and environmental influences on fish sex determination and differentiation. Mar Biotechnol 14(5):591–604

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ribera J, Ayala V, Casas C (2007) Involvement of c-Jun-JNK pathways in the regulation of programmed cell death of developing chick embryo spinal cord motoneurons. Dev Neurosci 29:438–451

    Article  CAS  PubMed  Google Scholar 

  • Sakurai T, Maeda S, Chang L et al (2006) Loss of hepatic NFkappa B activity enhances chemical hepatocarcinogenesis through sustained c-Jun N-terminal kinase 1 activation. Proc Natl Acad Sci U S A 103:10544–10551

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Savage MJ, Lin YG, Ciallella JR et al (2002) Activation of c-Jun N-terminal kinase and p38 in an Alzheimer's disease model is associated with a myloid deposition. J Neurosci 22:3376–3385

    CAS  PubMed  Google Scholar 

  • Storling J, Binzer J, Andersson AK et al (2005) Nitric oxide contributes to cytokine-induced apoptosis in pancreatic beta cells via potentiation of JNK activity and inhibition of Akt. Diabetologia 48:2039–2050

    Article  CAS  PubMed  Google Scholar 

  • Suzuki A, Ghayor C, Guicheux J et al (2006) Enhanced expression of the inorganic phosphate transporter Pit-1 is involved in BMP-2-induced matrix mineralization in osteoblast-like cells. J Bone Miner Res 21:674–683

    Article  CAS  PubMed  Google Scholar 

  • Sykiotis GP, Bohmann D (2008) Stress-activated protein kinases. Springer Berlin, Heidelberg, pp 225–241

    Book  Google Scholar 

  • Uhlirova M, Jasper H, Bohmann D (2005) Non-cell-autonomous induction of tissue overgrowth by JNK/Ras cooperation in a Drosophila tumor model. Proc Natl Acad Sci U S A 102:13123–13128

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wilhelm M, Xu Z, Kukekov NV et al (2007) Proapoptotic nix activates the JNK pathway by interacting with POSH and mediates death in a Parkinson's disease model. J Biol Chem 282:1288–1295

    Article  CAS  PubMed  Google Scholar 

  • Winn RA, Marek L, Han SY et al (2005) Restoration of Wnt-7a expression reverses non-small cell lung cancer cellular transformation through frizzled-9-mediated growth inhibition and promotion of cell differentiation. J Biol Chem 280:19625–19634

    Article  CAS  PubMed  Google Scholar 

  • Xiao YM (1993) Study on the reproductive biology of Monopterus albus (Zuiew): 1. Early gonadogenesis and structure change in Monopterus albus. Acta Sci Nat Univ Norm Hunan 16:346–349

    Google Scholar 

  • Xiao YM (1995) Study on the reproductive biology of Monopterus albus (Zuiew): 2. Female development of Monopterus albus. Acta Sci Nat Univ Norm Hunan 18:45–51

    Google Scholar 

  • Xiao YM, Liu Y (1995) Study on the histology in sex changing from intersex to male of Monopterus albus (Zuiew). Chin J Fish 19:297–301

    Google Scholar 

  • Xiao YM, Chen LL, Liu J, Liu WB, Chen HG, Zou LJ et al (2010) Contrast expression patterns of jnk1 during sex reversal of the rice-field eel. J Exp Zool Mol Dev Evol 314B:242–256

    CAS  Google Scholar 

  • Xu P, McIntyre LM, Scardina J, Wheeler PA, Thorgaard GH, Nichols KM (2011) Transcriptome profiling of embryonic development rate in rainbow trout advanced backcross introgression lines. Mar Biotechnol 13(2):215–231

    Article  CAS  PubMed  Google Scholar 

  • Yúfera M, Halm S, Beltran S, Fusté B, Planas JV, Martínez-Rodríguez G (2012) Transcriptomic characterization of the larval stage in gilthead seabream (Sparus aurata) by 454 pyrosequencing. Mar Biotechnol 14(4):423–435

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This research is supported by the National Basic Research Program of China (2012CB22305, Y. M. Xiao) and the National Science Foundation of China (31172399, 30871908, Y. M. Xiao). The authors would like to express their thanks to the anonymous referees for their constructive comments on the paper, which have greatly improved its presentation.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yamei Xiao.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Xiao, Y., Zhou, Y., Xiong, Z. et al. Involvement of JNK in the Embryonic Development and Organogenesis in Zebrafish. Mar Biotechnol 15, 716–725 (2013). https://doi.org/10.1007/s10126-013-9520-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10126-013-9520-5

Keywords

Navigation