4.6 Article

Mechanisms for type-II vitellogenesis-inhibiting hormone suppression of vitellogenin transcription in shrimp hepatopancreas: Crosstalk of GC/cGMP pathway with different MAPK-dependent cascades

Journal

PLOS ONE
Volume 13, Issue 3, Pages -

Publisher

PUBLIC LIBRARY SCIENCE
DOI: 10.1371/journal.pone.0194459

Keywords

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Funding

  1. National Natural Science Foundation of China [31402287, 31602135]
  2. Guangdong Province Program [2016A020210062, 2017B030314052, 2017A030310429, 2013B091300020, 2014B030301064, 2015B020231007, 2016A030310112]
  3. Science & Technology Promoting Projects for Oceanic & Fishery in Guangdong Province [A201601A03]
  4. National High Technology Research & Development Program of China (863 Program) [2012AA10A404-4]
  5. Science and Technology Service Network Initiative of the Chinese Academy of Sciences [KFJ-SW-STS-146]
  6. National Share & Service Platform Construction Program for Aquaculture Germplasm and Resources [2017DKA30470]

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Vitellogenesis is the process of yolk formation via accumulating vitellin (Vn) with nutrients in the oocytes. Expression of vitellogenin (Vg), the precursor of Vn, is one of the indicators for the start of vitellogenesis. In Pacific white shrimp (Litopenaeus vannamel), the type-II vitellogenesis-inhibiting hormone (VIH-2) effectively suppresses hepatopancreatic Vg mRNA expression. In this study, we demonstrate the increasing transcript levels of hepatopancreatic Vg during L. vannamei ovarian development, suggesting that the hepatopancreas-derived Vg/Nn may also contribute to vitellogenesis in this species. Using a combination of in vivo injections and in vitro primary cell cultures, we provide evidences that the inhibition of VIH-2 on hepatopancreatic Vg gene expression is mediated through a functional coupling of the GC/cGMP pathway with different MAPK-dependent cascades in female shrimp. In VIH-2 signaling, the NO-independent GC/cGMP/PKG cascades were upstream of the MAPKs. Activations of the MAPK signal by VIH-2 include the phosphorylation of JNK and the mRNA/protein expression of P(38)MAPK. Additionally, the cAMP/PKA pathway is another positive intracellular signal for hepatopancreatic Vg mRNA expression but is independent of its VIH-2 regulation. Our findings establish a model for the signal transduction mechanism of Vg regulation by VIH and shed light on the biological functions and signaling of the CHH family in crustaceans.

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