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Host–Plasmodium Interaction:Role of RNAi


Affiliations
1 ICMR-National Institute of Research in Tribal Health, Jabalpur 482 003, India
 

Malaria is a global health problem that afflicts an estimated 90 million people worldwide. Significant improvement in the understanding of Plasmodium life cycle has been achieved, yet multitude of clinical effects seen in malaria remains unanswered. MicroRNAs (miRNAs) have been implicated in the pathogenesis of malaria. These miRNAs act as post-transcriptional regulators and control host’s cellular factors needed for Plasmodium multiplication and suppress immune responses. Dysregulated miRNA expression has been linked to malaria pathogenesis through modulation of signalling pathways involved in processes such as proliferation, metabolism, gene expression and immune response in the host. In humans, Plasmodium infection severely affects hepatic functions and erythrocytic life span while severe infection with P. falciparum can lead to cerebral pathology. The present review aims to gain insight into the contribution of miRNAs to the exo-erythrocytic and erythrocytic stage pathology of Plasmodium infection and coordinated regulation in Plasmodium-mediated progression to cerebral pathology.

Keywords

Cerebral Pathology, MicroRNAs, Plasmodium.
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  • Kuo, C. H. and Kissinger, J. C., Consistent and contrasting properties of lineage-specific genes in the apicomplexan parasites Plasmodium and Theileria. BMC Evol. Biol., 2008, 8, 108.

  • Igweh, J. C., Biology of malaria parasites. In Malaria Parasites (ed. Okwa, O.), IntechOpen, 2012; doi:10.5772/34260.

  • van de Sand, C. et al., The liver stage of Plasmodium berghei inhibits host cell apoptosis. Mol. Microbiol., 2005, 58, 731–742.

  • Vaughan, A. M., Aly, A. S. and Kappe, S. H., Malaria parasite pre-erythrocytic stage infection: gliding and hiding. Cell Host. Microbe., 2008, 4, 209–218.

  • Baer, K., Klotz, C., Kappe, S. H., Schnieder, T. and Frevert, U., Release of hepatic Plasmodium yoelii merozoites into the pulmonary microvasculature. PLOS Pathog., 2007, 3, e171.

  • World Malaria Report. WHO, 2013; http://www.who.int/malaria/ publications/world_malaria_report_2013/en/

  • NBVDCP, 2014; http://www.nvbdcp.gov.in/index4.php?lang=0&linkid=420&lid=3699

  • Idro, R., Marsh, K., John, C. C. and Newton, C. R. J., Cerebral malaria, mechanisms of brain injury and strategies for improved neuro-cognitive outcome. Pediatr. Res., 2010, 68, 8.

  • Fabian, M. R., Sonenberg, N. and Filipowicz, W., Regulation of mRNA translation and stability by microRNAs. Annu. Rev. Biochem., 2010, 79, 351–379.

  • Baum, J. et al., Molecular genetics and comparative genomics reveal RNAi is not functional in malaria parasites. Nucl. Acids Res., 2009, 37, 3788–3798.

  • Goldie, B. J. and Cairns, M. J., Post-transcriptional trafficking and regulation of neuronal gene expression. Mol. Neurobiol., 2012, 45, 99–108.

  • Cejka, D., Losert, D. and Wacheck, V., Short interfering RNA (siRNA): tool or therapeutic? Clin. Sci. (London), 2006, 110, 47– 58.

  • Liu, J., Valencia-Sanchez, M. A., Hannon, G. J. and Parker, R., MicroRNA-dependent localization of targeted mRNAs to mammalian P-bodies. Nat. Cell Biol., 2005, 7, 719–723.

  • Orom, U. A., Nielsen, F. C. and Lund, A. H., MicroRNA-10a binds the 5′ UTR of ribosomal protein mRNAs and enhances their translation. Mol. Cell, 2008, 30, 460–471.

  • Tavazoie, S. F. et al., Endogenous human microRNAs that suppress breast cancer metastasis. Nature, 2008, 451, 147– 152.

  • Nicoloso, M. S., Spizzo, R., Shimizu, M., Rossi, S. and Calin, G. A., MicroRNAs – the micro steering wheel of tumour metastases. Nat. Rev. Cancer, 2009, 9, 293–302.

  • Vasudevan, S., Tong, Y. and Steitz, J. A., Switching from repression to activation: microRNAs can up-regulate translation. Science, 2007, 318, 1931–1934.

  • Hwang, H. W., Wentzel, E. A. and Mendell, J. T., A hexanucleotide element directs microRNA nuclear import. Science, 2007, 315, 97–100.

  • Younger, S. T. and Corey, D. R., Transcriptional gene silencing in mammalian cells by miRNA mimics that target gene promoters. Nucleic Acids Res., 2011, 39, 5682–5691.

  • Iorio, M. V., Piovan, C. and Croce, C. M., Interplay between microRNAs and the epigenetic machinery: an intricate network. Biochim. Biophys. Acta, 2010, 1799, 694–701.

  • Kozomara, A. and Griffiths-Jones, S., miRBase: annotating high confidence microRNAs using deep sequencing data. Nucleic Acids Res., 2014, 42.

  • Kozomara, A. and Griffiths-Jones, S., miRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Res., 2011, 39.

  • Bi, Y., Liu, G. and Yang, R., MicroRNAs: novel regulators during the immune response. J. Cell Physiol., 2009, 218, 467–472.

  • O’Connell, R. M., Taganov, K. D., Boldin, M. P., Cheng, G. and Baltimore, D., MicroRNA-155 is induced during the macrophage inflammatory response. Proc. Natl. Acad. Sci. USA, 2007, 104, 1604–1609.

  • Lindsay, M. A., MicroRNAs and the immune response. Trends Immunol., 2008, 29, 343–351.

  • Chen, X. M., Splinter, P. L., O’Hara S. P. and LaRusso, N. F., A cellular micro-RNA, let-7i, regulates Toll-like receptor 4 expression and contributes to cholangiocyte immune responses against Cryptosporidium parvum infection. J. Biol. Chem., 2007, 282, 28929–28938.

  • Hu, G., Zhou, R., Liu, J., Gong, A. Y. and Chen, X. M., MicroRNA-98 and let-7 regulate expression of suppressor of cytokine signaling 4 in biliary epithelial cells in response to Cryptosporidium parvum infection. J. Infect. Dis., 2010, 202, 125–135.

  • Larsen, L. and Ropke, C., Suppressors of cytokine signalling: SOCS. APMIS, 2002, 110, 833–844.

  • Cai, Y., Chen, H., Jin, L., You, Y. and Shen, J., STAT3-dependent transactivation of miRNA genes following Toxoplasma gondii infection in macrophage. Parasit Vectors, 2013, 6, 356.

  • Kerr, T. A. and Davidson, N. O., Therapeutic RNA manipulation in liver disease. Hepatology, 2010, 51, 1055–1061.

  • Wang, K. et al., Circulating microRNAs, potential biomarkers for drug-induced liver injury. Proc. Natl. Acad. Sci. USA, 2009, 106, 4402–4407.

  • Chen, X. M., MicroRNA signatures in liver diseases. World J Gastroenterol., 2009, 15, 1665–1672.

  • Haramati, S., et al., MicroRNA as repressors of stress-induced anxiety: the case of amygdalar miR-34. J. Neurosci., 2011, 31, 14191–14203.

  • Feng, W. and Feng, Y., MicroRNAs in neural cell development and brain diseases. Sci. China Life Sci., 2011, 54, 1103–1112.

  • Lee, S. T. et al., miR-206 regulates brain-derived neurotrophic factor in Alzheimer disease model. Ann. Neurol., 2012, 72, 269– 277.

  • Krichevsky, A. M., King, K. S., Donahue, C. P., Khrapko, K. and Kosik, K. S., A microRNA array reveals extensive regulation of microRNAs during brain development. RNA, 2003, 9, 1274– 1281.

  • Hakimi, M. A. and Menard, R., Do apicomplexan parasites hijack the host cell microRNA pathway for their intracellular development? F1000 Biol Rep 2, 2010, 42, 1–3.

  • Luder, C. G., Stanway, R. R., Chaussepied, M., Langsley, G. and Heussler, V. T., Intracellular survival of apicomplexan parasites and host cell modification. Int. J Parasitol., 2009, 39, 163–173.

  • Rathjen, T., Nicol, C., McConkey, G. and Dalmay, T., Analysis of short RNAs in the malaria parasite and its red blood cell host. FEBS Lett., 2006, 580, 5185–5188.

  • Pfeffer, S. et al., Identification of microRNAs of the herpesvirus family. Nat Meth., 2005, 2, 269–276.

  • Bogerd, H. P. et al., A mammalian herpesvirus uses noncanonical expression and processing mechanisms to generate viral MicroRNAs. Mol. Cell, 2010, 37, 135–142.

  • Rouha, H., Thurner, C. and Mandl, C. W., Functional microRNA generated from a cytoplasmic RNA virus. Nucleic Acids Res., 2010, 38, 8328–8337.

  • Hartgers, F. C. et al., Enhanced Toll-like receptor responsiveness associated with mitogen-activated protein kinase activation in Plasmodium falciparum-infected children. Infect Immun., 2008, 76, 5149–5157.

  • Paroo, Z., Ye, X., Chen, S. and Liu, Q., Phosphorylation of the human microRNA-generating complex mediates MAPK/Erk signaling. Cell, 2009, 139, 112–122.

  • Dave, R. S. and Khalili, K., Morphine treatment of human monocyte-derived macrophages induces differential miRNA and protein expression: impact on inflammation and oxidative stress in the central nervous system. J. Cell Biochem., 2010, 110, 834– 845.

  • Lourembam, S. D., Sawian, C. E. and Baruah, S., Dysregulation of cytokines expression in complicated falciparum malaria with increased TGF-beta and IFN-gamma and decreased IL-2 and IL12. Cytokine, 2013, 64, 503–508.

  • Davis, B. N., Hilyard, A. C., Lagna, G. and Hata, A., SMAD proteins control DROSHA-mediated microRNA maturation. Nature, 2008, 454, 56–61.

  • Delić, D., Dkhil, M., Al-Quraishy, S. and Wunderlich, F., Hepatic miRNA expression reprogrammed by Plasmodium chabaudi malaria. Parasitol Res., 2011, 108, 1111–1121.

  • Liu, J., Wu, C. P., Lu, B. F. and Jiang, J. T., Mechanism of T cell regulation by microRNAs. Cancer Biol. Med., 2013, 10, 131– 137.

  • Sonkoly, E., Stahle, M. and Pivarcsi, A., MicroRNAs and immunity: novel players in the regulation of normal immune function and inflammation. Semin. Cancer Biol., 2008, 18, 131– 140.

  • Kozaki, K., Imoto, I., Mogi, S., Omura, K. and Inazawa, J., Exploration of tumor-suppressive microRNAs silenced by DNA hypermethylation in oral cancer. Cancer Res., 2008, 68, 2094– 2105.

  • Wang, A., Qianchuan, H. and Yan, Z., Systematically dissecting the global mechanism of miRNA functions in mouse pluripotent stem cells. BMC Genomics, 2015, 16, 1–15

  • Langhorne, J., Quin, S. J. and Sanni, L. A., Mouse models of blood-stage malaria infections: immune responses and cytokines involved in protection and pathology. Chem. Immunol., 2002, 80, 204–228.

  • Hammerschmidt-Kamper, C. E., Deciphering the interplay between exo-erythrocytic Plasmodium berghei parasites and the host hepatic miRNA expression Doctoral. Heidelberg: University of Heidelberg, 2012, p. 162.

  • Hong, L. et al., MicroRNA-21: a therapeutic target for reversing drug resistance in cancer. Exp. Opin. Ther Targets, 2013, 17, 1073–1080.

  • Chan, J. A., Krichevsky, A. M. and Kosik, K. S., MicroRNA-21 is an antiapoptotic factor in human glioblastoma cells. Cancer Res., 2005, 65, 6029–6033.

  • Quinn, S. R. and O'Neill, L. A., A trio of microRNAs that control Toll-like receptor signalling. Int. Immunol., 2011, 23, 421– 425.

  • Moschos, S. A. et al., Expression profiling in vivo demonstrates rapid changes in lung microRNA levels following lipopolysaccharideinduced inflammation but not in the anti-inflammatory action of glucocorticoids. BMC Genomics, 2007, 8, 240.

  • Ren, M. et al., Correlation between hepatitis B virus protein and microRNA processor drosha in cells expressing HBV. Antiviral Res., 2012, 94, 225–231.

  • Wu, J. F. et al., Down-regulation of dicer in hepatocellular carcinoma. Med. Oncol., 2011, 28, 804–809.

  • Perlmann, P. and Troye-Blomberg, M. (eds), Malaria and the immune system in humans, Malaria Immunology, Karger Publishers, 2002, vol. 80, pp. 229–242.

  • Su, X. Z. et al., The large diverse gene family var encodes proteins involved in cytoadherence and antigenic variation of Plasmodium falciparum-infected erythrocytes. Cell, 1995, 82, 89– 100.

  • El-Assaad, F. et al., Differential microRNA expression in experimental cerebral and noncerebral malaria. Infect Immun., 2011, 79, 2379–2384.

  • Zhang, M. et al., Inhibition of microRNA let-7i depresses maturation and functional state of dendritic cells in response to lipopolysaccharide stimulation via targeting suppressor of cytokine signaling 1. J. Immunol., 2011, 187, 1674–1683.

  • Kimura, A. et al., Suppressor of cytokine signaling-1 selectively inhibits LPS-induced IL-6 production by regulating JAK-STAT. Proc. Natl. Acad. Sci. USA, 2005, 102, 17089–17094.

  • Yu, H., Liu, W., Lai, N., Chen, H., Yu, C., Lu, M. and Huang, H., MicroRNA let-7i can control TLR4 expression and affect IFNgamma. In 37th Congress of IUPS (Birmingham, UK). Proc 37th IUPS, PCA198, 2013.

  • Chhabra, R., Adlakha, Y. K., Hariharan, M., Scaria, V. and Saini, N., Upregulation of miR-23a-27a-24-2 cluster induces caspasedependent and -independent apoptosis in human embryonic kidney cells. PLOS ONE, 2009, 4, e5848.

  • Pedersen, I. and David, M., MicroRNAs in the immune response. Cytokine, 2008, 43, 391–394.

  • Xiao, C. et al., MiR-150 controls B cell differentiation by targeting the transcription factor c-Myb. Cell, 2007, 131, 146– 159.

  • Friedman, M. J., Erythrocytic mechanism of sickle cell resistance to malaria. Proc. Natl. Acad. Sci. USA, 1978, 75, 1994–1997.

  • LaMonte, G. et al., Translocation of sickle cell erythrocyte microRNAs into Plasmodium falciparum inhibits parasite translation and contributes to malaria resistance. Cell Host Microbe., 2012, 12, 187–199.

  • Mourier, T. et al., Genome-wide discovery and verification of novel structured RNAs in Plasmodium falciparum. Genome Res., 2008, 18, 281–292.

  • Lagier-Tourenne, C., Polymenidou, M. and Cleveland, D. W., TDP-43 and FUS/TLS: emerging roles in RNA processing and neurodegeneration. Hum. Mol. Genet, 2010, 19, R46–R64.

  • Andersson, M. K. et al., The multifunctional FUS, EWS and TAF15 proto-oncoproteins show cell type-specific expression patterns and involvement in cell spreading and stress response. BMC Cell Biol., 2008, 9, 37.

  • Ou, S. H., Wu, F., Harrich, D., Garcia-Martinez, L. F. and Gaynor, R. B., Cloning and characterization of a novel cellular protein, TDP-43, that binds to human immunodeficiency virus type 1 TAR DNA sequence motifs. J. Virol., 1995, 69, 3584–3596.

  • Ayala, Y. M. et al., Human, drosophila, and C. elegans TDP43: nucleic acid binding properties and splicing regulatory function. J. Mol. Biol., 2005, 348, 575–588.

  • Ayala, Y. M. et al., Structural determinants of the cellular localization and shuttling of TDP-43. J. Cell Sci., 2008, 121, 3778–3785.

  • Ménard, R., Medicine: knockout malaria vaccine? Nature, 2005, 433, 2.

  • Siomi, H. and Siomi, M. C., Posttranscriptional regulation of microRNA biogenesis in animals. Mol. Cell, 2010, 38, 323– 332.

  • Chen, C. Y., Chang, J. T., Ho, Y. F. and Shyu, A. B., MiR-26 down-regulates TNF-alpha/NF-kappaB signalling and IL-6 expression by silencing HMGA1 and MALT1. Nucl. Acids Res., 2016, 44, 3772–3787.

  • Kim, S. J., Gregersen, P. K. and Diamond, B., Regulation of dendritic cell activation by microRNA let-7c and BLIMP1. J. Clin. Invest., 2013, 123, 823–833.

  • Schulte, L. N., Eulalio, A., Mollenkopf, H. J., Reinhardt, R. and Vogel, J., Analysis of the host microRNA response to Salmonella uncovers the control of major cytokines by the let-7 family. EMBO J., 2011, 30, 1977–1989.

  • Hu, G. et al., MicroRNA-98 and let-7 confer cholangiocyte expression of cytokine-inducible Src homology 2-containing protein in response to microbial challenge. J. Immunol., 2009, 183, 1617–1624.

  • Lehmann, S. M. et al., 2012, An unconventional role for miRNA: let-7 activates Toll-like receptor 7 and causes neurodegeneration. Nat. Neurosci., 2012, 15, 827–835.

  • Dai, X. et al., MicroRNA-193a-3p Reduces intestinal inflammation in response to microbiota via down-regulation of colonic PepT1. J. Biol. Chem., 2015, 290, 16099–16115.

  • Wong, J. J. et al., RBM3 regulates temperature sensitive miR142-5p and miR-143 (thermomiRs), which target immune genes and control fever. Nucleic Acids Res., 2016, 44, 2888–2897.

  • Chiu, C. C. and Wu, W. S., Investigation of microRNAs in mouse macrophage responses to lipopolysaccharide-stimulation by combining gene expression with microRNA-target information. BMC Genomics 2015, 16(Suppl. 12), S13.

  • Petriv, O. I. et al., Comprehensive microRNA expression profiling of the hematopoietic hierarchy. Proc. Natl. Acad. Sci. USA, 2010, 107, 15443–15448.

  • Zou, T. et al., The role of microtubule-associated protein 1S in SOCS3 regulation of IL-6 signaling. FEBS Lett., 2008, 582, 4015–4022.

  • Qiang, J. et al., Effects of exposure to Streptococcus iniae on microRNA expression in the head kidney of genetically improved farmed tilapia (Oreochromis niloticus). BMC Genomics, 2017, 18, 190.

  • Rouas, R. et al., Human natural Treg microRNA signature: role of microRNA-31 and microRNA-21 in FOXP3 expression. Eur. J. Immunol., 2009, 39, 1608–1618.

  • Hu, X. et al., Genome-wide analyses of microRNA profiling in interleukin-27 treated monocyte-derived human dendritic cells using deep sequencing: a pilot study. Int. J. Mol. Sci., 2017, 18, 1–4.

  • Zehavi, L. et al., MiR-377 targets E2F3 and alters the NF-κB signaling pathway through MAP3K7 in malignant melanoma. Mol. Cancer, 2015, 14, 68.

  • Reddycherla, A. V. et al., miR-20a inhibits TCR-mediated signaling and cytokine production in human naive CD4+ T cells. PLOS ONE, 2015, 10, e0125311.

  • Luo, Y. et al., Sfmbt2 10th intron-hosted miR-466(a/e)-3p are important epigenetic regulators of Nfat5 signaling, osmoregulation and urine concentration in mice. Biochim. Biophys. Acta, 2014, 1839, 97–106.

  • Barker, K. R. et al., miR-155 modifies inflammation, endothelial activation and blood-brain barrier dysfunction in cerebral malaria. Mol. Med., 2017, 23, 24–33.

  • Agarwal, V., Bell, G. W., Nam, J.-W. and Bartel, D. P., Predicting effective microRNA target sites in mammalian mRNAs. Elife 4, 2015.

  • Betel, D., Koppal, A., Agius, P., Sander, C. and Leslie, C., Comprehensive modeling of microRNA targets predicts functional non-conserved and non-canonical sites. Genome Biol., 2010, 11, R90.

  • Wong, N. and Wang, X., miRDB: an online resource for microRNA target prediction and functional annotations. Nucl. Acids Res., 2014, 43, D146–D152.

  • Dweep, H., Sticht, C., Pandey, P. and Gretz, N., miRWalk†database: prediction of possible miRNA binding sites by â€oewalking†the genes of three genomes. J. Biomed. Inf., 2011, 44, 839–847.


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  • Host–Plasmodium Interaction:Role of RNAi

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Authors

Rohit Shrivastava
ICMR-National Institute of Research in Tribal Health, Jabalpur 482 003, India
S. Rajasubramaniam
ICMR-National Institute of Research in Tribal Health, Jabalpur 482 003, India

Abstract


Malaria is a global health problem that afflicts an estimated 90 million people worldwide. Significant improvement in the understanding of Plasmodium life cycle has been achieved, yet multitude of clinical effects seen in malaria remains unanswered. MicroRNAs (miRNAs) have been implicated in the pathogenesis of malaria. These miRNAs act as post-transcriptional regulators and control host’s cellular factors needed for Plasmodium multiplication and suppress immune responses. Dysregulated miRNA expression has been linked to malaria pathogenesis through modulation of signalling pathways involved in processes such as proliferation, metabolism, gene expression and immune response in the host. In humans, Plasmodium infection severely affects hepatic functions and erythrocytic life span while severe infection with P. falciparum can lead to cerebral pathology. The present review aims to gain insight into the contribution of miRNAs to the exo-erythrocytic and erythrocytic stage pathology of Plasmodium infection and coordinated regulation in Plasmodium-mediated progression to cerebral pathology.

Keywords


Cerebral Pathology, MicroRNAs, Plasmodium.

References





DOI: https://doi.org/10.18520/cs%2Fv115%2Fi12%2F2219-2231