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Hepatic miRNA expression reprogrammed by Plasmodium chabaudi malaria

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Abstract

Evidence is accumulating that miRNAs are critically implicated in the outcome of diseases, but little information is available for infectious diseases. This study investigates the hepatic miRNA signature in female C57BL/6 mice infected with self-healing Plasmodium chabaudi malaria. Primary infections result in approximately 50% peak parasitemia on day 8 p.i., approximately 80% survival, and development of protective immunity. The latter is evidenced as 100% survival and 1.5% peak parasitemia upon homolog re-infections of those mice which are still alive on day 56 after primary infection. Such immune mice exhibit increased levels of IgG2a and IgG2b isotypes and still contain P. chabaudi-infected erythrocytes in their livers as revealed by light microscopy and PCR analysis. Primary infections, but not secondary infections, induce an upregulation of hepatic mRNAs encoding IL-1β, TNFα, IFNγ, NF-κB, and iNOS, and a downregulation of mRNAs for CYP7A1 and SULT2A2, respectively. Using miRXplore microarrays containing 634 mouse miRNAs in combination with quantitative RT-PCR, the liver is found to respond to primary infections with an upregulation of the three miRNA species miR-26b, MCMV-miR-M23-1-5p, and miR-1274a, and a downregulation of the 16 miRNA species miR-101b, let-7a, let-7g, miR-193a-3p, miR-192, miR-142-5p, miR-465d, miR-677, miR-98, miR-694, miR-374*, miR-450b-5p, miR-464, miR-377, miR-20a*, and miR-466d-3p, respectively. Surprisingly, about the same pattern of miRNA expression is revealed in immune mice, and this pattern is even sustained upon homolog re-infections of immune mice. These data suggest that development of protective immunity against malarial blood stages of P. chabaudi is associated with a reprogramming of the expression of distinct miRNA species in the female mouse liver.

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Acknowledgements

This work was supported by Deutsche Forschungsgemeinschaft through GRK 1427 and the Centere of Excellence for Biodiversity Research, College of Science, King Saud University, Riyadh, Saudi Arabia.

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  1. Molecular Parasitology, Centre for Biological and Medical Research, Heinrich-Heine-University, Universitaetsstr. 1, 40225, Duesseldorf, Germany

    Denis Delić & Frank Wunderlich

  2. Zoology, College of Science, King Saud University, 11352, Riyadh, Saudi Arabia

    Mohamed Dkhil, Saleh Al-Quraishy & Frank Wunderlich

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Correspondence to Frank Wunderlich.

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ESM 1

Hy5/Hy3 false-color images after scanning of microarrays. Livers were removed from non-infected naïve mice (Nd0) and immune mice (Id0) as well as from corresponding mice after infection with P. chabaudi malaria for 8 days, respectively (Nd8/Id8). RNA was isolated, labeled, and hybridized with fluorescent Hy5 (red color). The universal reference RNA was labeled with fluorescent Hy3 (green color). Hybridization of microarrays was done with equal amounts of the four experimental samples and the universal reference. Red color indicates Hy5 fluorescence derived from the two experimental samples, i.e. signal intensity of the experimental samples is higher than that of green Hy3 fluorescence derived from the universal reference RNA. Green spots indicate that the fluorescence intensity of the universal reference is stronger than in the experimental samples. Yellow spots indicate that the signal intensities are equal for both experimental samples and universal reference. (JPG 291 KB)

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Delić, D., Dkhil, M., Al-Quraishy, S. et al. Hepatic miRNA expression reprogrammed by Plasmodium chabaudi malaria. Parasitol Res 108, 1111–1121 (2011). https://doi.org/10.1007/s00436-010-2152-z

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