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JNK signaling pathway regulates the development of ovaries and synthesis of vitellogenin (Vg) in the swimming crab Portunus trituberculatus

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Cell Stress and Chaperones Aims and scope

Abstract

The development of Portunus trituberculatus egg cells is directly related to the nutritional status of the fertilized egg, which affects the key production stages of offspring hatching. Vitellogenin plays a key role in the nutrient supply required for the development of the egg cells. The c-Jun N-terminal kinase (JNK) is an important member of the mitogen-activated protein kinase (MAPK) superfamily and plays an important role in cell proliferation, transformation, differentiation, and apoptosis. At present, there are no reports on the involvement of the JNK signaling pathway in the reproductive regulation of P. trituberculatus. In this study, rapid amplification of complementary DNA ends amplification technology was used to clone the full length of JNK complementary DNA, which has a length of 2094 bp, including an open reading frame (ORF) of 1266 bp encoding a 421-amino acid protein. The protein includes the S_TKC conserved domain with a TPY phosphorylation site, which is a typical feature of the JNK gene family. Observing tissue sections found the oocytes in the inhibitor group developed slowly, while the oocytes in the activated group showed accelerated development. Meanwhile, Portunus trituberculatus JNK and vitellogenin (Vg) genes exhibited the same trend in the hepatopancreas and ovaries, and the expression of the SP600125 group was downregulated (P < 0.05), while the anisomycin group was upregulated (P < 0.05). In addition, JNK enzyme activity and vitellin (Vn) content in the ovarian tissue showed that the JNK activity of the SP600125 group decreased, while activity increased in the anisomycin group. The accumulation of Vn content in the SP600125 group decreased, and that in the anisomycin group increased. In summary, after injection with inhibitor or activator, the JNK signaling pathway of P. trituberculatus was inhibited or activated, the accumulation of Vn in the ovary was reduced or increased, and ovarian development was inhibited or accelerated, respectively. These results indicated that the JNK signaling pathway is involved in the regulation of Vg synthesis and ovarian development in P. trituberculatus. The results of this study further add to the knowledge of the breeding biology of P. trituberculatus and provide a theoretical reference for the optimization of breeding techniques in aquaculture production systems.

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All data generated or analyzed during this study are included in this published article and its supplementary information files.

Abbreviations

AvJNK:

Armadillidium vulgare JNK gene

CsJNK:

Cryptotermes secundus JNK gene

E. sinensis :

Eriocheir sinensis

EsJNK:

Eriocheir sinensis JNK gene

LsJNK:

Laodelphax striatellus JNK gene

P. japonicus :

Penaeus japonicus

PjJNK:

Penaeus japonicus JNK gene

PnJNK:

Paracyclopina nana JNK gene

PtJNK:

Portunus trituberculatus JNK gene

P. trituberculatus :

Portunus trituberculatus

P. vannamei :

Penaeus vannamei

PvJNK:

Penaeus vannamei JNK gene

S. paramamosain :

Scylla paramamosain

SpJNK:

Scylla paramamosain JNK gene

Vg:

Vitellogenin

Vn:

Vitellin

ZnJNK:

Zootermopsis nevadensis JNK gene

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Acknowledgments

We are grateful to the anonymous reviewers for their professional review of the manuscript.

Funding

This study was sponsored by the National Natural Science Foundation of China (41806184), China Postdoctoral Science Foundation (2018M632439), Major Agriculture Program of Ningbo (2017C110007), Major Science & Technology Special Project of Zhejiang Province (no. 2016C02055-8), Ministry of Agriculture of China & China Agriculture Research System (no. CARS-48), Ningbo University Research Fund (XYL18013), and K.C. Wong Magna Fund at Ningbo University.

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Authors and Affiliations

  1. School of Marine Science, Ningbo University, Ningbo, 315211, Zhejiang, China

    Hongling Wei, Zhiming Ren, Lei Tang, Hongzhi Yao, Xing Li, Chunlin Wang, Changkao Mu, Ce Shi & Huan Wang

  2. Key Laboratory of Applied Marine Biotechnology, Ministry of Education, Ningbo University, Ningbo, 315211, Zhejiang, China

    Chunlin Wang, Changkao Mu, Ce Shi & Huan Wang

Authors
  1. Hongling Wei
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  2. Zhiming Ren
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  3. Lei Tang
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  4. Hongzhi Yao
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  5. Xing Li
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  6. Chunlin Wang
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  7. Changkao Mu
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  8. Ce Shi
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  9. Huan Wang
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Contributions

H Wang conceived and designed this study. HL Wei and ZM Ren cultivated the experimental animals. HL Wei, ZM Ren, L Tang, HZ Yao, X Li, CL Wang, CK Mu, C Shi, and H Wang performed and analyzed all experiments. HL Wei and H Wang wrote the manuscript with support from all authors. All authors read and approved the final manuscript.

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Correspondence to Huan Wang.

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The animal subjects used in the present study are crabs, which are invertebrates and are exempt from this requirement.

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Wei, H., Ren, Z., Tang, L. et al. JNK signaling pathway regulates the development of ovaries and synthesis of vitellogenin (Vg) in the swimming crab Portunus trituberculatus. Cell Stress and Chaperones 25, 441–453 (2020). https://doi.org/10.1007/s12192-020-01085-1

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