Pacific White Shrimp (Litopenaeus vannamei) Vitellogenesis-Inhibiting Hormone (VIH) Is Predominantly Expressed in the Brain and Negatively Regulates Hepatopancreatic Vitellogenin (VTG) Gene Expression1

Jan 24, 2014Biology of reproduction

Brain hormone in Pacific white shrimp reduces egg yolk protein gene activity in the liver-like organ

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Abstract

Injection of recombinant vitellogenesis-inhibiting hormone (VIH) reversed ovarian growth induced by eyestalk ablation.

Ovarian maturation in crustaceans is driven by oogenesis and vitellogenesis.
The peptide hormone VIH is identified as the most potent negative regulator of crustacean reproduction.
Cloning of VIH cDNA from Pacific white shrimp indicates its classification as part of the type II crustacean hyperglycemic hormone family.
Both the brain and eyestalk are significant sources of VIH mRNA expression in shrimp.
Endogenous factors in the hemolymph, brain, and eyestalk suppress hepatopancreatic vitellogenin (VTG) gene expression.
Unilateral eyestalk ablation decreases mRNA levels of VIH in the brain, affecting VTG expression.

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Ovarian maturation in crustaceans is temporally orchestrated by two processes: oogenesis and vitellogenesis. The peptide hormone vitellogenesis-inhibiting hormone (VIH), by far the most potent negative regulator of crustacean reproduction known, critically modulates crustacean ovarian maturation by suppressing vitellogenin (VTG) synthesis. In this study, cDNA encoding VIH was cloned from the eyestalk of Pacific white shrimp, Litopenaeus vannamei, a highly significant commercial culture species. Phylogenetic analysis suggests that L. vannamei VIH (lvVIH) can be classified as a member of the type II crustacean hyperglycemic hormone family. Northern blot and RT-PCR results reveal that both the brain and eyestalk were the major sources for lvVIH mRNA expression. In in vitro experiments on primary culture of shrimp hepatopancreatic cells, it was confirmed that some endogenous inhibitory factors existed in L. vannamei hemolymph, brain, and eyestalk that suppressed hepatopancreatic VTG gene expression. Purified recombinant lvVIH protein was effective in inhibiting VTG mRNA expression in both in vitro primary hepatopancreatic cell culture and in vivo injection experiments. Injection of recombinant VIH could also reverse ovarian growth induced by eyestalk ablation. Furthermore, unilateral eyestalk ablation reduced the mRNA level of lvVIH in the brain but not in the remaining contralateral eyestalk. Our study, as a whole, provides new insights on VIH regulation of shrimp reproduction: 1) the brain and eyestalk are both important sites of VIH expression and therefore possible coregulators of hepatopancreatic VTG mRNA expression and 2) eyestalk ablation could increase hepatopancreatic VTG expression by transcriptionally abolishing eyestalk-derived VIH and diminishing brain-derived VIH.

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Pacific White Shrimp (Litopenaeus vannamei) Vitellogenesis-Inhibiting Hormone (VIH) Is Predominantly Expressed in the Brain and Negatively Regulates Hepatopancreatic Vitellogenin (VTG) Gene Expression1

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