Blood feeding and Plasmodium infection alters the miRNome of Anopheles stephensi

PLoS One. 2014 May 27;9(5):e98402. doi: 10.1371/journal.pone.0098402. eCollection 2014.

Abstract

Blood feeding is an integral process required for physiological functions and propagation of the malaria vector Anopheles. During blood feeding, presence of the malaria parasite, Plasmodium in the blood induces several host effector molecules including microRNAs which play important roles in the development and maturation of the parasite within the mosquito. The present study was undertaken to elucidate the dynamic expression of miRNAs during gonotrophic cycle and parasite development in Anopheles stephensi. Using next generation sequencing technology, we identified 126 miRNAs of which 17 were novel miRNAs. The miRNAs were further validated by northern hybridization and cloning. Blood feeding and parasitized blood feeding in the mosquitoes revealed regulation of 13 and 16 miRNAs respectively. Expression profiling of these miRNAs revealed that significant miRNAs were down-regulated upon parasitized blood feeding with a repertoire of miRNAs showing stage specific up-regulation. Expression profiles of significantly modulated miRNAs were further validated by real time PCR. Target prediction of regulated miRNAs revealed overlapping targeting by different miRNAs. These targets included several metabolic pathways including metabolic, redox homeostasis and protein processing machinery components. Our analysis revealed tight regulation of specific miRNAs post blood feeding and parasite infection in An. stephensi. Such regulated expression suggests possible role of these miRNAs during gonotrophic cycle in mosquito. Another set of miRNAs were also significantly regulated at 42 h and 5 days post infection indicating parasite stage-specific role of host miRNAs. This study will result in better understanding of the role of miRNAs during gonotrophic cycle and parasite development in mosquito and can probably facilitate in devising novel malaria control strategies at vector level.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Anopheles / classification
  • Anopheles / genetics*
  • Anopheles / parasitology*
  • Feeding Behavior
  • Female
  • Gene Expression Regulation
  • High-Throughput Nucleotide Sequencing
  • Host-Parasite Interactions
  • Malaria / genetics
  • Malaria / parasitology
  • MicroRNAs / genetics*
  • Sequence Analysis, RNA

Substances

  • MicroRNAs

Grants and funding

The study was funded through Science and Engineering Research Board (SERB) Young Scientist grant (SR/FT/LS-109/2011) awarded to SS and through ICGEB internal funds. SS is a recipient of Ramanujan Fellowship, Department of Science and Technology, Government of India and their support is duly acknowledged. SJ and VR are recipients of senior research fellowships from the Council of Scientific and Industrial Research, India. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.