MicroRNA Expression Profile in Human Macrophages in Response to Leishmania major Infection

PLoS Neglected Tropical Diseases

Volumn 7, Issue 10, 2013, Pages

  Lemaire, Julien ^a   Mkannez, Ghada ^b,c   Guerfali, Fatma Z ^b,c   Gustin, Cindy ^a   Attia, Hanène ^b,c   Sghaier, Rabiaa M ^b,c   Miled, Slimane Ben ^b,c   Benkahla, Alia ^b,c   Ben Othman, Rym ^b,c   Bruno, Roman ^e   Cazenave, Pierre Andre ^f   Checkmeneva, Elena ^g   Daskalaki, Adriani ^g   Gabdoulline, Razif ^g   Ghedira, Kais ^b,c   Guzani Tabbane, Lamia ^b,c   Herwig, Ralf ^h   Hide, Winston ^i,j   Hofmann, Oliver ^i,j   Hornischer, Klaus ^g   Jauregui, Ruy ^g   Kel, Alexander ^l   Kiselev, Ilya ^l   Kolpakov, Fedor ^l   Kondrakhin, Yuriy ^l   Kutumova, Elena ^l   Land, Sigrid ^g   Liebich, Ines ^g   Manchon, Laurent ^e   Matys, Volker ^g   Michael, Holger ^g   Noguier, Florian ^e   Pierrat, Fabien ^e   Piquemal, David ^e   Rabhi, Imen ^b,c   Rabhi, Sameh ^b,c   Rasche, Axel ^h   Regnault, Béatrice ^k   Ryabova, Anna ^l   Schacherer, Frank ^g   Sharipov, Ruslan ^l   Stegmaier, Philip ^g   Tiffin, Nicki ⁱ   Tolstykh, Nikita ^l   Trentin, Bernadette ^e   Valeev, Tagir ^l   Voss, Nico ^g   Wierling, Christoph ^h   Yevshin, Ivan ^l   Dellagi, Koussay ^b,c,d   Laouini, Dhafer ^b,c   Renard, Patricia ^a   more..

^a University of Namur   (Belgium)

^b PASTEUR INSTITUTE OF TUNIS   (Tunisia)

^c UNIVERSITY OF TUNIS EL MANAR   (Tunisia)

^d INSTITUT DE RECHERCHE POUR LE DÉVELOPPEMENT   (France)

^e Skuldtech   (France)

^f UNIVERSITÉ PIERRE ET MARIE CURIE   (France)

^g BIOBASE GMBH   (Germany)

^h MAX PLANCK INSTITUTE FOR MOLECULAR GENETICS   (Germany)

ⁱ UNIVERSITY OF THE WESTERN CAPE   (South Africa)

^j HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^k INSTITUT PASTEUR   (France)

^l Institute of Systems Biology Ltd   (Russian Federation)

more..

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; EPIDERMAL GROWTH FACTOR RECEPTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; LIPOPHOSPHOGLYCAN; MICRORNA; MICRORNA 132; MICRORNA 140; MICRORNA 146A; MICRORNA 146B; MICRORNA 155; MICRORNA 210; MICRORNA 22; MICRORNA 23B; MICRORNA 25; MICRORNA 26A; MICRORNA 28; MICRORNA 331; MICRORNA 486; MICRORNA 502; MYC PROTEIN; NATURAL RESISTANCE ASSOCIATED MACROPHAGE PROTEIN 1; PHOSPHATIDYLINOSITOL 3, 4, 5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN BCL 2; PROTEIN P50; PROTEIN P53; SYNAPTOTAGMIN I; TOLL LIKE RECEPTOR 4; UNCLASSIFIED DRUG; UNINDEXED DRUG;

ARTICLE; BIOINFORMATICS; CELL DIFFERENTIATION; CELL PHAGOCYTOSIS; CHEMOLUMINESCENCE; CLUSTER ANALYSIS; CONTROLLED STUDY; DENSITY GRADIENT CENTRIFUGATION; DOWN REGULATION; DYNAMICS; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; LEISHMANIASIS; MACROPHAGE; NORMAL HUMAN; PARASITE LOAD; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ISOLATION; WESTERN BLOTTING;

BLOOD DONORS; CELLS, CULTURED; GENE EXPRESSION PROFILING; HEALTHY VOLUNTEERS; HOST-PATHOGEN INTERACTIONS; HUMANS; LEISHMANIA MAJOR; MACROPHAGES; MICRORNAS;

EID: 84887300103     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0002478     Document Type: Article

References (88)

1. Murray HW, Berman JD, Davies CR, Saravia NG, (2005) Advances in leishmaniasis. Lancet 366: 1561-1577.
2. Duclos S, Desjardins M, (2000) Subversion of a young phagosome: the survival strategies of intracellular pathogens. Cell Microbiol 2: 365-377.
3. Olivier M, Gregory DJ, Forget G, (2005) Subversion mechanisms by which Leishmania parasites can escape the host immune response: a signaling point of view. Clin Microbiol Rev 18: 293-305.
4. Peters NC, Sacks DL, (2009) The impact of vector-mediated neutrophil recruitment on cutaneous leishmaniasis. Cell Microbiol 11: 1290-1296.
5. Moreno I, Dominguez M, Cabanes D, Aizpurua C, Torano A, (2010) Kinetic analysis of ex vivo human blood infection by Leishmania. PLoS Negl Trop Dis 4: e743.
6. Reiner NE, Ng W, McMaster WR, (1987) Parasite-accessory cell interactions in murine leishmaniasis. II. Leishmania donovani suppresses macrophage expression of class I and class II major histocompatibility complex gene products. J Immunol 138: 1926-1932.
7. Kaye PM, Rogers NJ, Curry AJ, Scott JC, (1994) Deficient expression of co-stimulatory molecules on Leishmania-infected macrophages. Eur J Immunol 24: 2850-2854.
8. Bhardwaj S, Srivastava N, Sudan R, Saha B, (2010) Leishmania interferes with host cell signaling to devise a survival strategy. J Biomed Biotechnol 2010: 109189.
9. Shadab M, Ali N, (2011) Evasion of Host Defence by Leishmania donovani: Subversion of Signaling Pathways. Mol Biol Int 2011: 343961.
10. Shio MT, Hassani K, Isnard A, Ralph B, Contreras I, et al. (2012) Host cell signalling and leishmania mechanisms of evasion. J Trop Med 2012: 819512.
11. Bogdan C, (2008) Mechanisms and consequences of persistence of intracellular pathogens: leishmaniasis as an example. Cell Microbiol 10: 1221-1234.
12. Teixeira MJ, Teixeira CR, Andrade BB, Barral-Netto M, Barral A, (2006) Chemokines in host-parasite interactions in leishmaniasis. Trends Parasitol 22: 32-40.
13. McConville MJ, Naderer T, (2011) Metabolic pathways required for the intracellular survival of Leishmania. Annu Rev Microbiol 65: 543-561.
14. Moore KJ, Matlashewski G, (1994) Intracellular infection by Leishmania donovani inhibits macrophage apoptosis. J Immunol 152: 2930-2937.
15. Guerfali FZ, Laouini D, Guizani-Tabbane L, Ottones F, Ben-Aissa K, et al. (2008) Simultaneous gene expression profiling in human macrophages infected with Leishmania major parasites using SAGE. BMC Genomics 9: 238.
16. Akarid K, Arnoult D, Micic-Polianski J, Sif J, Estaquier J, et al. (2004) Leishmania major-mediated prevention of programmed cell death induction in infected macrophages is associated with the repression of mitochondrial release of cytochrome c. J Leukoc Biol 76: 95-103.
17. Ruhland A, Leal N, Kima PE, (2007) Leishmania promastigotes activate PI3K/Akt signalling to confer host cell resistance to apoptosis. Cell Microbiol 9: 84-96.
18. Barbato C, Arisi I, Frizzo ME, Brandi R, Da Sacco L, et al. (2009) Computational challenges in miRNA target predictions: to be or not to be a true target? J Biomed Biotechnol 2009: 803069.
19. Krek A, Grun D, Poy MN, Wolf R, Rosenberg L, et al. (2005) Combinatorial microRNA target predictions. Nat Genet 37: 495-500.
20. Lewis BP, Burge CB, Bartel DP, (2005) Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120: 15-20.
21. Scaria V, Hariharan M, Maiti S, Pillai B, Brahmachari SK, (2006) Host-virus interaction: a new role for microRNAs. Retrovirology 3: 68.
22. Skalsky RL, Cullen BR, (2010) Viruses, microRNAs, and host interactions. Annu Rev Microbiol 64: 123-141.
23. Katiyar-Agarwal S, Jin H, (2010) Role of small RNAs in host-microbe interactions. Annu Rev Phytopathol 48: 225-246.
24. Eulalio A, Schulte L, Vogel J, (2012) The mammalian microRNA response to bacterial infections. RNA Biol 9: 742-750.
25. Hakimi MA, Cannella D, (2011) Apicomplexan parasites and subversion of the host cell microRNA pathway. Trends Parasitol 27: 481-486.
26. Zeiner GM, Norman KL, Thomson JM, Hammond SM, Boothroyd JC, (2010) Toxoplasma gondii infection specifically increases the levels of key host microRNAs. PLoS One 5: e8742.
27. Nahid MA, Satoh M, Chan EK, (2011) MicroRNA in TLR signaling and endotoxin tolerance. Cell Mol Immunol 8: 388-403.
28. Liu Y, Kao WJ, (2002) Human macrophage adhesion on fibronectin: the role of substratum and intracellular signalling kinases. Cell Signal 14: 145-152.
29. Spath GF, Beverley SM, (2001) A lipophosphoglycan-independent method for isolation of infective Leishmania metacyclic promastigotes by density gradient centrifugation. Exp Parasitol 99: 97-103.
30. Hulten LM, Olson FJ, Aberg H, Carlsson J, Karlstrom L, et al. (2010) 15-Lipoxygenase-2 is expressed in macrophages in human carotid plaques and regulated by hypoxia-inducible factor-1alpha. Eur J Clin Invest 40: 11-17.
31. Daigneault M, Preston JA, Marriott HM, Whyte MK, Dockrell DH, (2010) The identification of markers of macrophage differentiation in PMA-stimulated THP-1 cells and monocyte-derived macrophages. PLoS One 5: e8668.
32. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, et al. (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3: RESEARCH0034.
33. Saeed AI, Sharov V, White J, Li J, Liang W, et al. (2003) TM4: a free, open-source system for microarray data management and analysis. Biotechniques 34: 374-378.
34. Dweep H, Sticht C, Pandey P, Gretz N, (2011) miRWalk-database: prediction of possible miRNA binding sites by "walking" the genes of three genomes. J Biomed Inform 44: 839-847.
35. Lynn DJ, Winsor GL, Chan C, Richard N, Laird MR, et al. (2008) InnateDB: facilitating systems-level analyses of the mammalian innate immune response. Mol Syst Biol 4: 218.
36. Maere S, Heymans K, Kuiper M, (2005) BiNGO: a Cytoscape plugin to assess overrepresentation of gene ontology categories in biological networks. Bioinformatics 21: 3448-3449.
37. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, et al. (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13: 2498-2504.
38. Smoot ME, Ono K, Ruscheinski J, Wang PL, Ideker T, (2011) Cytoscape 2.8: new features for data integration and network visualization. Bioinformatics 27: 431-432.
39. Wang J, Lu M, Qiu C, Cui Q, (2010) TransmiR: a transcription factor-microRNA regulation database. Nucleic Acids Res 38: D119-122.
40. Whitney AR, Diehn M, Popper SJ, Alizadeh AA, Boldrick JC, et al. (2003) Individuality and variation in gene expression patterns in human blood. Proc Natl Acad Sci U S A 100: 1896-1901.
41. Turan N, Katari S, Coutifaris C, Sapienza C, (2010) Explaining inter-individual variability in phenotype: is epigenetics up to the challenge? Epigenetics 5: 16-19.
42. Stratz C, Nuhrenberg TG, Binder H, Valina CM, Trenk D, et al. (2012) Micro-array profiling exhibits remarkable intra-individual stability of human platelet micro-RNA. Thromb Haemost 107: 634-641.
43. Nandan D, Camargo de Oliveira C, Moeenrezakhanlou A, Lopez M, Silverman JM, et al. (2012) Myeloid cell IL-10 production in response to leishmania involves inactivation of glycogen synthase kinase-3beta downstream of phosphatidylinositol-3 kinase. J Immunol 188: 367-378.
44. Singh AK, Mukhopadhyay C, Biswas S, Singh VK, Mukhopadhyay CK, (2012) Intracellular pathogen Leishmania donovani activates hypoxia inducible factor-1 by dual mechanism for survival advantage within macrophage. PLoS One 7: e38489.
45. Calegari-Silva TC, Pereira RM, De-Melo LD, Saraiva EM, Soares DC, et al. (2009) NF-kappaB-mediated repression of iNOS expression in Leishmania amazonensis macrophage infection. Immunol Lett 127: 19-26.
46. Cheng AM, Byrom MW, Shelton J, Ford LP, (2005) Antisense inhibition of human miRNAs and indications for an involvement of miRNA in cell growth and apoptosis. Nucleic Acids Res 33: 1290-1297.
47. Crawford M, Batte K, Yu L, Wu X, Nuovo GJ, et al. (2009) MicroRNA 133B targets pro-survival molecules MCL-1 and BCL2L2 in lung cancer. Biochem Biophys Res Commun 388: 483-489.
48. Chan YC, Banerjee J, Choi SY, Sen CK, (2012) miR-210: the master hypoxamir. Microcirculation 19: 215-223.
49. Degrossoli A, Bosetto MC, Lima CB, Giorgio S, (2007) Expression of hypoxia-inducible factor 1alpha in mononuclear phagocytes infected with Leishmania amazonensis. Immunol Lett 114: 119-125.
50. Bazzoni F, Rossato M, Fabbri M, Gaudiosi D, Mirolo M, et al. (2009) Induction and regulatory function of miR-9 in human monocytes and neutrophils exposed to proinflammatory signals. Proc Natl Acad Sci U S A 106: 5282-5287.
51. Quinn SR, O'Neill LA, (2011) A trio of microRNAs that control Toll-like receptor signalling. Int Immunol 23: 421-425.
52. Taganov KD, Boldin MP, Chang KJ, Baltimore D, (2006) NF-kappaB-dependent induction of microRNA miR-146, an inhibitor targeted to signaling proteins of innate immune responses. Proc Natl Acad Sci U S A 103: 12481-12486.
53. Tili E, Michaille JJ, Cimino A, Costinean S, Dumitru CD, et al. (2007) Modulation of miR-155 and miR-125b levels following lipopolysaccharide/TNF-alpha stimulation and their possible roles in regulating the response to endotoxin shock. J Immunol 179: 5082-5089.
54. O'Connell RM, Taganov KD, Boldin MP, Cheng G, Baltimore D, (2007) MicroRNA-155 is induced during the macrophage inflammatory response. Proc Natl Acad Sci U S A 104: 1604-1609.
55. Ceppi M, Pereira PM, Dunand-Sauthier I, Barras E, Reith W, et al. (2009) MicroRNA-155 modulates the interleukin-1 signaling pathway in activated human monocyte-derived dendritic cells. Proc Natl Acad Sci U S A 106: 2735-2740.
56. Schulte LN, Westermann AJ, Vogel J, (2012) Differential activation and functional specialization of miR-146 and miR-155 in innate immune sensing. Nucleic Acids Res 41: 542-553.
57. Wanet A, Tacheny A, Arnould T, Renard P, (2012) miR-212/132 expression and functions: within and beyond the neuronal compartment. Nucleic Acids Res 40: 4742-4753.
58. Faria MS, Reis FC, Lima AP, (2012) Toll-like receptors in leishmania infections: guardians or promoters? J Parasitol Res 2012: 930257.
59. Gallego C, Golenbock D, Gomez MA, Saravia NG, (2011) Toll-like receptors participate in macrophage activation and intracellular control of Leishmania (Viannia) panamensis. Infect Immun 79: 2871-2879.
60. Srivastav S, Kar S, Chande AG, Mukhopadhyaya R, Das PK, (2012) Leishmania donovani exploits host deubiquitinating enzyme A20, a negative regulator of TLR signaling, to subvert host immune response. J Immunol 189: 924-934.
61. Reinhard K, Huber M, Lohoff M, Visekruna A, (2012) The role of NF-kappaB activation during protection against Leishmania infection. Int J Med Microbiol 302: 230-235.
62. Ji J, Sun J, Soong L, (2003) Impaired expression of inflammatory cytokines and chemokines at early stages of infection with Leishmania amazonensis. Infect Immun 71: 4278-4288.
63. Gregory DJ, Godbout M, Contreras I, Forget G, Olivier M, (2008) A novel form of NF-kappaB is induced by Leishmania infection: involvement in macrophage gene expression. Eur J Immunol 38: 1071-1081.
64. Neves BM, Silvestre R, Resende M, Ouaissi A, Cunha J, et al. (2010) Activation of phosphatidylinositol 3-kinase/Akt and impairment of nuclear factor-kappaB: molecular mechanisms behind the arrested maturation/activation state of Leishmania infantum-infected dendritic cells. Am J Pathol 177: 2898-2911.
65. Guizani-Tabbane L, Ben-Aissa K, Belghith M, Sassi A, Dellagi K, (2004) Leishmania major amastigotes induce p50/c-Rel NF-kappa B transcription factor in human macrophages: involvement in cytokine synthesis. Infect Immun 72: 2582-2589.
66. Filipowicz W, Bhattacharyya SN, Sonenberg N, (2008) Mechanisms of post-transcriptional regulation by microRNAs: are the answers in sight? Nat Rev Genet 9: 102-114.
67. Guo H, Ingolia NT, Weissman JS, Bartel DP, (2010) Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature 466: 835-840.
68. Huntzinger E, Izaurralde E, (2011) Gene silencing by microRNAs: contributions of translational repression and mRNA decay. Nat Rev Genet 12: 99-110.
69. Kumar R, Bumb RA, Salotra P, (2010) Evaluation of localized and systemic immune responses in cutaneous leishmaniasis caused by Leishmania tropica: interleukin-8, monocyte chemotactic protein-1 and nitric oxide are major regulatory factors. Immunology 130: 193-201.
70. Ritter U, Moll H, (2000) Monocyte chemotactic protein-1 stimulates the killing of leishmania major by human monocytes, acts synergistically with IFN-gamma and is antagonized by IL-4. Eur J Immunol 30: 3111-3120.
71. Brandonisio O, Panaro MA, Fumarola I, Sisto M, Leogrande D, et al. (2002) Macrophage chemotactic protein-1 and macrophage inflammatory protein-1 alpha induce nitric oxide release and enhance parasite killing in Leishmania infantum-infected human macrophages. Clin Exp Med 2: 125-129.
72. Vargas-Inchaustegui DA, Hogg AE, Tulliano G, Llanos-Cuentas A, Arevalo J, et al. (2010) CXCL10 production by human monocytes in response to Leishmania braziliensis infection. Infect Immun 78: 301-308.
73. Ritter U, Korner H, (2002) Divergent expression of inflammatory dermal chemokines in cutaneous leishmaniasis. Parasite Immunol 24: 295-301.
74. Tan G, Shi Y, Wu ZH, (2012) MicroRNA-22 promotes cell survival upon UV radiation by repressing PTEN. Biochem Biophys Res Commun 417: 546-551.
75. Zhang H, Zuo Z, Lu X, Wang L, Wang H, et al. (2012) MiR-25 regulates apoptosis by targeting Bim in human ovarian cancer. Oncol Rep 27: 594-598.
76. Koch M, Mollenkopf HJ, Klemm U, Meyer TF, (2012) Induction of microRNA-155 is TLR- and type IV secretion system-dependent in macrophages and inhibits DNA-damage induced apoptosis. Proc Natl Acad Sci U S A 109: E1153-1162.
77. Kulshreshtha R, Ferracin M, Wojcik SE, Garzon R, Alder H, et al. (2007) A microRNA signature of hypoxia. Mol Cell Biol 27: 1859-1867.
78. Yang Z, Wu L, Zhu X, Xu J, Jin R, et al. (2013) MiR-29a modulates the angiogenic properties of human endothelial cells. Biochem Biophys Res Commun 434: 143-149.
79. Peng H, Hamanaka RB, Katsnelson J, Hao LL, Yang W, et al. (2012) MicroRNA-31 targets FIH-1 to positively regulate corneal epithelial glycogen metabolism. FASEB J 26: 3140-3147.
80. Babar IA, Czochor J, Steinmetz A, Weidhaas JB, Glazer PM, et al. (2011) Inhibition of hypoxia-induced miR-155 radiosensitizes hypoxic lung cancer cells. Cancer Biol Ther 12: 908-914.
81. Aga E, Katschinski DM, van Zandbergen G, Laufs H, Hansen B, et al. (2002) Inhibition of the spontaneous apoptosis of neutrophil granulocytes by the intracellular parasite Leishmania major. J Immunol 169: 898-905.
82. Valdes-Reyes L, Argueta J, Moran J, Salaiza N, Hernandez J, et al. (2009) Leishmania mexicana: inhibition of camptothecin-induced apoptosis of monocyte-derived dendritic cells. Exp Parasitol 121: 199-207.
83. Lisi S, Sisto M, Acquafredda A, Spinelli R, Schiavone M, et al. (2005) Infection with Leishmania infantum Inhibits actinomycin D-induced apoptosis of human monocytic cell line U-937. J Eukaryot Microbiol 52: 211-217.
84. Kim HW, Haider HK, Jiang S, Ashraf M, (2009) Ischemic preconditioning augments survival of stem cells via miR-210 expression by targeting caspase-8-associated protein 2. J Biol Chem 284: 33161-33168.
85. Gou D, Ramchandran R, Peng X, Yao L, Kang K, et al. (2012) miR-210 has an anti-apoptotic effect in pulmonary artery smooth muscle cells during hypoxia. Am J Physiol Lung Cell Mol Physiol.
86. Yang W, Sun T, Cao J, Liu F, Tian Y, et al. (2012) Downregulation of miR-210 expression inhibits proliferation, induces apoptosis and enhances radiosensitivity in hypoxic human hepatoma cells in vitro. Exp Cell Res 318: 944-954.
87. Qi J, Qiao Y, Wang P, Li S, Zhao W, et al. (2012) microRNA-210 negatively regulates LPS-induced production of proinflammatory cytokines by targeting NF-kappaB1 in murine macrophages. FEBS Lett 586: 1201-1207.
88. Ghosh J, Bose M, Roy S, Bhattacharyya SN, (2013) Leishmania donovani targets Dicer1 to downregulate miR-122, lower serum cholesterol, and facilitate murine liver infection. Cell Host Microbe 13: 277-288.