Translational profiling of macrophages infected with Leishmania donovani identifies mTOR- and eIF4A-sensitive immune-related transcripts
Autoři:
Visnu Chaparro aff001; Louis-Philippe Leroux aff001; Laia Masvidal aff002; Julie Lorent aff002; Tyson E. Graber aff003; Aude Zimmermann aff001; Guillermo Arango Duque aff001; Albert Descoteaux aff001; Tommy Alain aff003; Ola Larsson aff002; Maritza Jaramillo aff001
Působiště autorů:
Institut National de la Recherche Scientifique (INRS)–Centre Armand-Frappier Santé Biotechnologie (CAFSB), Laval, Quebec, Canada
aff001; Department of Oncology-Pathology, Science for Life Laboratory, Karolinska Institutet, Stockholm, Sweden
aff002; Children's Hospital of Eastern Ontario Research Institute, Ottawa, Ontario, Canada
aff003; Department of Biochemistry, Microbiology and Immunology, University of Ottawa, Ottawa, Ontario, Canada
aff004
Vyšlo v časopise:
Translational profiling of macrophages infected with Leishmania donovani identifies mTOR- and eIF4A-sensitive immune-related transcripts. PLoS Pathog 16(6): e32767. doi:10.1371/journal.ppat.1008291
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.ppat.1008291
Souhrn
The protozoan parasite Leishmania donovani (L. donovani) causes visceral leishmaniasis, a chronic infection which is fatal when untreated. Herein, we investigated whether in addition to altering transcription, L. donovani modulates host mRNA translation to establish a successful infection. Polysome-profiling revealed that one third of protein-coding mRNAs expressed in primary mouse macrophages are differentially translated upon infection with L. donovani promastigotes or amastigotes. Gene ontology analysis identified key biological processes enriched for translationally regulated mRNAs and were predicted to be either activated (e.g. chromatin remodeling and RNA metabolism) or inhibited (e.g. intracellular trafficking and antigen presentation) upon infection. Mechanistic in silico and biochemical analyses showed selective activation mTOR- and eIF4A-dependent mRNA translation, including transcripts encoding central regulators of mRNA turnover and inflammation (i.e. PABPC1, EIF2AK2, and TGF-β). L. donovani survival within macrophages was favored under mTOR inhibition but was dampened by pharmacological blockade of eIF4A. Overall, this study uncovers a vast yet selective reprogramming of the host cell translational landscape early during L. donovani infection, and suggests that some of these changes are involved in host defense mechanisms while others are part of parasite-driven survival strategies. Further in vitro and in vivo investigation will shed light on the contribution of mTOR- and eIF4A-dependent translational programs to the outcome of visceral leishmaniasis.
Klíčová slova:
Amastigotes – Leishmania donovani – Macrophages – Messenger RNA – Parasitic diseases – Protein translation – Protozoan infections – Promastigotes
Zdroje
1. Kaye P, Scott P. Leishmaniasis: complexity at the host-pathogen interface. Nat Rev Microbiol. 2011;9(8):604–15. Epub 2011/07/13. doi: 10.1038/nrmicro2608 21747391.
2. Dayakar A, Chandrasekaran S, Kuchipudi SV, Kalangi SK. Cytokines: Key Determinants of Resistance or Disease Progression in Visceral Leishmaniasis: Opportunities for Novel Diagnostics and Immunotherapy. Front Immunol. 2019;10:670. Epub 2019/04/27. doi: 10.3389/fimmu.2019.00670 31024534; PubMed Central PMCID: PMC6459942.
3. Podinovskaia M, Descoteaux A. Leishmania and the macrophage: a multifaceted interaction. Future Microbiol. 2015;10(1):111–29. Epub 2015/01/20. doi: 10.2217/fmb.14.103 25598341.
4. Buates S, Matlashewski G. General suppression of macrophage gene expression during Leishmania donovani infection. J Immunol. 2001;166(5):3416–22. Epub 2001/02/24. doi: 10.4049/jimmunol.166.5.3416 11207299.
5. Chaussabel D, Semnani RT, McDowell MA, Sacks D, Sher A, Nutman TB. Unique gene expression profiles of human macrophages and dendritic cells to phylogenetically distinct parasites. Blood. 2003;102(2):672–81. Epub 2003/03/29. doi: 10.1182/blood-2002-10-3232 12663451.
6. Gregory DJ, Sladek R, Olivier M, Matlashewski G. Comparison of the effects of Leishmania major or Leishmania donovani infection on macrophage gene expression. Infect Immun. 2008;76(3):1186–92. Epub 2007/12/19. doi: 10.1128/IAI.01320-07 18086813; PubMed Central PMCID: PMC2258831.
7. Kong F, Saldarriaga OA, Spratt H, Osorio EY, Travi BL, Luxon BA, et al. Transcriptional Profiling in Experimental Visceral Leishmaniasis Reveals a Broad Splenic Inflammatory Environment that Conditions Macrophages toward a Disease-Promoting Phenotype. PLoS Pathog. 2017;13(1):e1006165. Epub 2017/02/01. doi: 10.1371/journal.ppat.1006165 28141856; PubMed Central PMCID: PMC5283737.
8. Shadab M, Das S, Banerjee A, Sinha R, Asad M, Kamran M, et al. RNA-Seq Revealed Expression of Many Novel Genes Associated With Leishmania donovani Persistence and Clearance in the Host Macrophage. Front Cell Infect Microbiol. 2019;9:17. Epub 2019/02/26. doi: 10.3389/fcimb.2019.00017 30805314; PubMed Central PMCID: PMC6370631.
9. Singh AK, Pandey RK, Siqueira-Neto JL, Kwon YJ, Freitas-Junior LH, Shaha C, et al. Proteomic-based approach to gain insight into reprogramming of THP-1 cells exposed to Leishmania donovani over an early temporal window. Infect Immun. 2015;83(5):1853–68. Epub 2015/02/19. doi: 10.1128/IAI.02833-14 25690103; PubMed Central PMCID: PMC4399049.
10. Piccirillo CA, Bjur E, Topisirovic I, Sonenberg N, Larsson O. Translational control of immune responses: from transcripts to translatomes. Nat Immunol. 2014;15(6):503–11. Epub 2014/05/21. doi: 10.1038/ni.2891 24840981.
11. William M, Leroux LP, Chaparro V, Graber TE, Alain T, Jaramillo M. Translational repression of Ccl5 and Cxcl10 by 4E-BP1 and 4E-BP2 restrains the ability of mouse macrophages to induce migration of activated T cells. Eur J Immunol. 2019. Epub 2019/04/30. doi: 10.1002/eji.201847857 31032899.
12. Langlais D, Cencic R, Moradin N, Kennedy JM, Ayi K, Brown LE, et al. Rocaglates as dual-targeting agents for experimental cerebral malaria. Proc Natl Acad Sci U S A. 2018;115(10):E2366–E75. Epub 2018/02/22. doi: 10.1073/pnas.1713000115 29463745; PubMed Central PMCID: PMC5877959.
13. Su X, Yu Y, Zhong Y, Giannopoulou EG, Hu X, Liu H, et al. Interferon-gamma regulates cellular metabolism and mRNA translation to potentiate macrophage activation. Nat Immunol. 2015;16(8):838–49. Epub 2015/07/07. doi: 10.1038/ni.3205 26147685; PubMed Central PMCID: PMC4509841.
14. Jackson RJ, Hellen CUT, Pestova TV. The mechanism of eukaryotic translation initiation and principles of its regulation. Nat Rev Mol Cell Biol. 2010;11(2):113–27. http://www.nature.com/nrm/journal/v11/n2/suppinfo/nrm2838_S1.html. doi: 10.1038/nrm2838 20094052
15. Meyuhas O, Kahan T. The race to decipher the top secrets of TOP mRNAs. Biochim Biophys Acta. 2015;1849(7):801–11. Epub 2014/09/23. doi: 10.1016/j.bbagrm.2014.08.015 25234618.
16. Masvidal L, Hulea L, Furic L, Topisirovic I, Larsson O. mTOR-sensitive translation: Cleared fog reveals more trees. RNA Biol. 2017:1–7. Epub 2017/03/10. doi: 10.1080/15476286.2017.1290041 28277937.
17. Sen ND, Zhou F, Harris MS, Ingolia NT, Hinnebusch AG. eIF4B stimulates translation of long mRNAs with structured 5' UTRs and low closed-loop potential but weak dependence on eIF4G. Proc Natl Acad Sci U S A. 2016;113(38):10464–72. Epub 2016/09/08. doi: 10.1073/pnas.1612398113 27601676; PubMed Central PMCID: PMC5035867.
18. Gandin V, Masvidal L, Hulea L, Gravel SP, Cargnello M, McLaughlan S, et al. nanoCAGE reveals 5' UTR features that define specific modes of translation of functionally related MTOR-sensitive mRNAs. Genome Res. 2016;26(5):636–48. Epub 2016/03/18. doi: 10.1101/gr.197566.115 26984228; PubMed Central PMCID: PMC4864462.
19. Chu J, Pelletier J. Targeting the eIF4A RNA helicase as an anti-neoplastic approach. Biochim Biophys Acta. 2015;1849(7):781–91. Epub 2014/09/23. doi: 10.1016/j.bbagrm.2014.09.006 25234619.
20. Cramer Z, Sadek J, Vazquez GG, Di Marco S, Pause A, Pelletier J, et al. eIF4A inhibition prevents the onset of cytokine-induced muscle wasting by blocking the STAT3 and iNOS pathways. Sci Rep. 2018;8(1):8414. Epub 2018/06/01. doi: 10.1038/s41598-018-26625-9 29849089; PubMed Central PMCID: PMC5976662.
21. Kaur S, Sassano A, Dolniak B, Joshi S, Majchrzak-Kita B, Baker DP, et al. Role of the Akt pathway in mRNA translation of interferon-stimulated genes. Proc Natl Acad Sci U S A. 2008;105(12):4808–13. doi: 10.1073/pnas.0710907105 18339807
22. Bhattacharya B, Chatterjee S, Devine WG, Kobzik L, Beeler AB, Porco JA Jr., et al. Fine-tuning of macrophage activation using synthetic rocaglate derivatives. Sci Rep. 2016;6:24409. Epub 2016/04/19. doi: 10.1038/srep24409 27086720; PubMed Central PMCID: PMC4834551.
23. Oertlin C, Lorent J, Murie C, Furic L, Topisirovic I, Larsson O. Generally applicable transcriptome-wide analysis of translation using anota2seq. Nucleic Acids Res. 2019. Epub 2019/03/31. doi: 10.1093/nar/gkz223 30926999.
24. Lorent J, Kusnadi EP, van Hoef V, Rebello RJ, Leibovitch M, Ristau J, et al. Translational offsetting as a mode of estrogen receptor alpha-dependent regulation of gene expression. EMBO J. 2019;38(23):e101323. Epub 2019/09/27. doi: 10.15252/embj.2018101323 31556460; PubMed Central PMCID: PMC6885737.
25. Mi H, Huang X, Muruganujan A, Tang H, Mills C, Kang D, et al. PANTHER version 11: expanded annotation data from Gene Ontology and Reactome pathways, and data analysis tool enhancements. Nucleic Acids Res. 2017;45(D1):D183–d9. Epub 2016/12/03. doi: 10.1093/nar/gkw1138 27899595; PubMed Central PMCID: PMC5210595.
26. Cheekatla SS, Aggarwal A, Naik S. mTOR signaling pathway regulates the IL-12/IL-10 axis in Leishmania donovani infection. Med Microbiol Immun. 2012;201(1):37–46. Epub 2011/05/14. doi: 10.1007/s00430-011-0202-5 21567173.
27. Fonseca BD, Smith EM, Yelle N, Alain T, Bushell M, Pause A. The ever-evolving role of mTOR in translation. Semin Cell Dev Biol. 2014;36:102–12. Epub 2014/09/30. doi: 10.1016/j.semcdb.2014.09.014 25263010.
28. Turner M, Diaz-Munoz MD. RNA-binding proteins control gene expression and cell fate in the immune system. Nat Immunol. 2018;19(2):120–9. Epub 2018/01/20. doi: 10.1038/s41590-017-0028-4 29348497.
29. Zhang X, Chen X, Liu Q, Zhang S, Hu W. Translation repression via modulation of the cytoplasmic poly(A)-binding protein in the inflammatory response. eLife. 2017;6. Epub 2017/06/22. doi: 10.7554/eLife.27786 28635594; PubMed Central PMCID: PMC5507668.
30. Pereira RM, Teixeira KL, Barreto-de-Souza V, Calegari-Silva TC, De-Melo LD, Soares DC, et al. Novel role for the double-stranded RNA-activated protein kinase PKR: modulation of macrophage infection by the protozoan parasite Leishmania. FASEB J. 2010;24(2):617–26. Epub 2009/10/09. doi: 10.1096/fj.09-140053 19812373.
31. Faria MS, Calegari-Silva TC, de Carvalho Vivarini A, Mottram JC, Lopes UG, Lima AP. Role of protein kinase R in the killing of Leishmania major by macrophages in response to neutrophil elastase and TLR4 via TNFalpha and IFNbeta. FASEB J. 2014;28(7):3050–63. Epub 2014/04/16. doi: 10.1096/fj.13-245126 24732131; PubMed Central PMCID: PMC4210457.
32. Bou-Nader C, Gordon JM, Henderson FE, Zhang J. The search for a PKR code—differential regulation of protein kinase R activity by diverse RNA and protein regulators. RNA. 2019;25(5):539–56. doi: 10.1261/rna.070169.118 30770398
33. Gal-Ben-Ari S, Barrera I, Ehrlich M, Rosenblum K. PKR: A Kinase to Remember. Front Mol Neurosci. 2018;11:480. Epub 2019/01/29. doi: 10.3389/fnmol.2018.00480 30686999; PubMed Central PMCID: PMC6333748.
34. Weichhart T, Hengstschlager M, Linke M. Regulation of innate immune cell function by mTOR. Nat Rev Immunol. 2015;15(10):599–614. Epub 2015/09/26. doi: 10.1038/nri3901 26403194.
35. Dias BT, Dias-Teixeira KL, Godinho JP, Faria MS, Calegari-Silva T, Mukhtar MM, et al. Neutrophil elastase promotes Leishmania donovani infection via interferon-beta. FASEB J. 2019;33(10):10794–807. Epub 2019/07/10. doi: 10.1096/fj.201900524R 31284755; PubMed Central PMCID: PMC6766642.
36. Cerezo M, Guemiri R, Druillennec S, Girault I, Malka-Mahieu H, Shen S, et al. Translational control of tumor immune escape via the eIF4F-STAT1-PD-L1 axis in melanoma. Nat Med. 2018;24(12):1877–86. Epub 2018/10/31. doi: 10.1038/s41591-018-0217-1 30374200.
37. Muller C, Schulte FW, Lange-Grunweller K, Obermann W, Madhugiri R, Pleschka S, et al. Broad-spectrum antiviral activity of the eIF4A inhibitor silvestrol against corona- and picornaviruses. Antiviral Res. 2018;150:123–9. Epub 2017/12/21. doi: 10.1016/j.antiviral.2017.12.010 29258862.
38. Rubio CA, Weisburd B, Holderfield M, Arias C, Fang E, DeRisi JL, et al. Transcriptome-wide characterization of the eIF4A signature highlights plasticity in translation regulation. Genome Biol. 2014;15(10):476. Epub 2014/10/03. doi: 10.1186/s13059-014-0476-1 25273840; PubMed Central PMCID: PMC4203936.
39. Wolfe AL, Singh K, Zhong Y, Drewe P, Rajasekhar VK, Sanghvi VR, et al. RNA G-quadruplexes cause eIF4A-dependent oncogene translation in cancer. Nature. 2014;513(7516):65–70. Epub 2014/08/01. doi: 10.1038/nature13485 25079319; PubMed Central PMCID: PMC4492470.
40. Modelska A, Turro E, Russell R, Beaton J, Sbarrato T, Spriggs K, et al. The malignant phenotype in breast cancer is driven by eIF4A1-mediated changes in the translational landscape. Cell Death Dis. 2015;6:e1603. Epub 2015/01/23. doi: 10.1038/cddis.2014.542 25611378; PubMed Central PMCID: PMC4669741.
41. Waldron JA, Raza F, Le Quesne J. eIF4A alleviates the translational repression mediated by classical secondary structures more than by G-quadruplexes. Nucleic Acids Res. 2018;46(6):3075–87. doi: 10.1093/nar/gky108 29471358
42. Asad M, Sabur A, Shadab M, Das S, Kamran M, Didwania N, et al. EB1-3 Chain of IL-35 Along With TGF-beta Synergistically Regulate Anti-leishmanial Immunity. Front Immunol. 2019;10:616. Epub 2019/04/30. doi: 10.3389/fimmu.2019.00616 31031744; PubMed Central PMCID: PMC6474326.
43. Mohr I, Sonenberg N. Host translation at the nexus of infection and immunity. Cell Host Microbe. 2012;12(4):470–83. Epub 2012/10/23. doi: 10.1016/j.chom.2012.09.006 23084916.
44. Leroux LP, Lorent J, Graber TE, Chaparro V, Masvidal L, Aguirre M, et al. The protozoan parasite Toxoplasma gondii selectively reprograms the host cell translatome. Infect Immun. 2018;86(9):e00244–18. Epub 2018/07/04. doi: 10.1128/IAI.00244-18 29967092.
45. Araki K, Morita M, Bederman AG, Konieczny BT, Kissick HT, Sonenberg N, et al. Translation is actively regulated during the differentiation of CD8+ effector T cells. Nat Immunol. 2017. Epub 2017/07/18. doi: 10.1038/ni.3795 28714979.
46. Holmes MJ, Shah P, Wek RC, Sullivan WJ Jr. Simultaneous Ribosome Profiling of Human Host Cells Infected with Toxoplasma gondii. mSphere. 2019;4(3). Epub 2019/06/07. doi: 10.1128/mSphere.00292-19 31167946.
47. Matheoud D, Moradin N, Bellemare-Pelletier A, Shio MT, Hong WJ, Olivier M, et al. Leishmania evades host immunity by inhibiting antigen cross-presentation through direct cleavage of the SNARE VAMP8. Cell Host Microbe. 2013;14(1):15–25. Epub 2013/07/23. doi: 10.1016/j.chom.2013.06.003 23870310.
48. Marr AK, MacIsaac JL, Jiang R, Airo AM, Kobor MS, McMaster WR. Leishmania donovani infection causes distinct epigenetic DNA methylation changes in host macrophages. PLoS Pathog. 2014;10(10):e1004419. Epub 2014/10/10. doi: 10.1371/journal.ppat.1004419 25299267; PubMed Central PMCID: PMC4192605.
49. Gardinassi LG, Garcia GR, Costa CH, Costa Silva V, de Miranda Santos IK. Blood Transcriptional Profiling Reveals Immunological Signatures of Distinct States of Infection of Humans with Leishmania infantum. PLoS Neglect Trop D. 2016;10(11):e0005123. Epub 2016/11/10. doi: 10.1371/journal.pntd.0005123 27828962; PubMed Central PMCID: PMC5102635.
50. Hentze MW, Castello A, Schwarzl T, Preiss T. A brave new world of RNA-binding proteins. Nat Rev Mol Cell Biol. 2018;19(5):327–41. Epub 2018/01/18. doi: 10.1038/nrm.2017.130 29339797.
51. Nandan D, Camargo de Oliveira C, Moeenrezakhanlou A, Lopez M, Silverman JM, Subek J, et al. Myeloid Cell IL-10 Production in Response to Leishmania Involves Inactivation of Glycogen Synthase Kinase-3β Downstream of Phosphatidylinositol-3 Kinase. J Immunol. 2012;188(1):367–78. doi: 10.4049/jimmunol.1100076 22140263
52. Zhang N, Prasad S, Huyghues Despointes CE, Young J, Kima PE. Leishmania parasitophorous vacuole membranes display phosphoinositides that create conditions for continuous Akt activation and a target for miltefosine in Leishmania infections. Cell Microbiol. 2018:e12889. Epub 2018/07/12. doi: 10.1111/cmi.12889 29993167.
53. Thomas SA, Nandan D, Kass J, Reiner NE. Countervailing, time-dependent effects on host autophagy promotes intracellular survival of Leishmania. J Biol Chem. 2018;293(7):2617–30. Epub 2017/12/23. doi: 10.1074/jbc.M117.808675 29269416; PubMed Central PMCID: PMC5818176.
54. Gray Nicola K, Hrabálková L, Scanlon JP, Smith Richard WP. Poly(A)-binding proteins and mRNA localization: who rules the roost? Biochem Soc T. 2015;43(6):1277–84. doi: 10.1042/bst20150171 26614673
55. Yu S, Wang D, Huang L, Zhang Y, Luo R, Adah D, et al. The complement receptor C5aR2 promotes protein kinase R expression and contributes to NLRP3 inflammasome activation and HMGB1 release from macrophages. J Biol Chem. 2019;294(21):8384–94. Epub 2019/04/12. doi: 10.1074/jbc.RA118.006508 30971430; PubMed Central PMCID: PMC6544858.
56. Vivarini AC, Calegari-Silva TC, Saliba AM, Boaventura VS, Franca-Costa J, Khouri R, et al. Systems Approach Reveals Nuclear Factor Erythroid 2-Related Factor 2/Protein Kinase R Crosstalk in Human Cutaneous Leishmaniasis. Front Immunol. 2017;8:1127. Epub 2017/09/30. doi: 10.3389/fimmu.2017.01127 28959260; PubMed Central PMCID: PMC5605755.
57. Gandin V, Masvidal L, Cargnello M, Gyenis L, McLaughlan S, Cai Y, et al. mTORC1 and CK2 coordinate ternary and eIF4F complex assembly. Nat Comm. 2016;7:11127. Epub 2016/04/05. doi: 10.1038/ncomms11127 27040916; PubMed Central PMCID: PMC4822005.
58. Guan BJ, van Hoef V, Jobava R, Elroy-Stein O, Valasek LS, Cargnello M, et al. A Unique ISR Program Determines Cellular Responses to Chronic Stress. Mol Cell. 2017;68(5):885–900.e6. Epub 2017/12/09. doi: 10.1016/j.molcel.2017.11.007 29220654; PubMed Central PMCID: PMC5730339.
59. Jaramillo M, Gomez MA, Larsson O, Shio MT, Topisirovic I, Contreras I, et al. Leishmania repression of host translation through mTOR cleavage is required for parasite survival and infection. Cell Host Microbe. 2011;9(4):331–41. Epub 2011/04/20. doi: 10.1016/j.chom.2011.03.008 21501832.
60. Khadir F, Shaler CR, Oryan A, Rudak PT, Mazzuca DM, Taheri T, et al. Therapeutic control of leishmaniasis by inhibitors of the mammalian target of rapamycin. PLoS Neglect Trop D. 2018;12(8):e0006701. Epub 2018/08/23. doi: 10.1371/journal.pntd.0006701 30133440.
61. Khadir F, Taheri T, Habibzadeh S, Zahedifard F, Gholami E, Heidari-Kharaji M, et al. Antileishmanial effect of rapamycin as an alternative approach to control Leishmania tropica infection. Vet Parasitol. 2019;276:108976. Epub 2019/11/19. doi: 10.1016/j.vetpar.2019.108976 31739256.
62. Di Marco S, Cammas A, Lian XJ, Kovacs EN, Ma JF, Hall DT, et al. The translation inhibitor pateamine A prevents cachexia-induced muscle wasting in mice. Nat Comm. 2012;3:896. doi: 10.1038/ncomms1899 https://www.nature.com/articles/ncomms1899#supplementary-information. 22692539
63. Singh G, Chavan HD, Dey CS. Proteomic analysis of miltefosine-resistant Leishmania reveals the possible involvement of eukaryotic initiation factor 4A (eIF4A). Int J Antimicrob Ag. 2008;31(6):584–6. Epub 2008/05/06. doi: 10.1016/j.ijantimicag.2008.01.032 18456462.
64. Naineni SK, Itoua Maiga R, Cencic R, Putnam AA, Amador LA, Rodriguez AD, et al. A Comparative Study of Small Molecules Targeting eIF4A. RNA. 2020. Epub 2020/02/06. doi: 10.1261/rna.072884.119 32014999.
65. Abdelkrim YZ, Harigua-Souiai E, Barhoumi M, Banroques J, Blondel A, Guizani I, et al. The steroid derivative 6-aminocholestanol inhibits the DEAD-box helicase eIF4A (LieIF4A) from the Trypanosomatid parasite Leishmania by perturbing the RNA and ATP binding sites. Mol Biochem Parasitol. 2018;226:9–19. Epub 2018/10/27. doi: 10.1016/j.molbiopara.2018.10.001 30365976.
66. Capelli-Peixoto J, Mule SN, Tano FT, Palmisano G, Stolf BS. Proteomics and Leishmaniasis: Potential Clinical Applications. Proteomics Clin Appl. 2019:e1800136. Epub 2019/07/28. doi: 10.1002/prca.201800136 31347770.
67. Harigua-Souiai E, Abdelkrim YZ, Bassoumi-Jamoussi I, Zakraoui O, Bouvier G, Essafi-Benkhadir K, et al. Identification of novel leishmanicidal molecules by virtual and biochemical screenings targeting Leishmania eukaryotic translation initiation factor 4A. PLoS Neglect Trop D. 2018;12(1):e0006160. Epub 2018/01/19. doi: 10.1371/journal.pntd.0006160 29346371; PubMed Central PMCID: PMC5790279.
68. Matte C, Descoteaux A. Leishmania donovani amastigotes impair gamma interferon-induced STAT1alpha nuclear translocation by blocking the interaction between STAT1alpha and importin-alpha5. Infect Immun. 2010;78(9):3736–43. Epub 2010/06/23. doi: 10.1128/IAI.00046-10 20566692; PubMed Central PMCID: PMC2937469.
69. Atayde VD, da Silva Lira Filho A, Chaparro V, Zimmermann A, Martel C, Jaramillo M, et al. Exploitation of the Leishmania exosomal pathway by Leishmania RNA virus 1. Nat Microbiol. 2019. doi: 10.1038/s41564-018-0352-y 30692670
70. Zangger H, Ronet C, Desponds C, Kuhlmann FM, Robinson J, Hartley MA, et al. Detection of Leishmania RNA virus in Leishmania parasites. PLoS Neglect Trop D. 2013;7(1):e2006. Epub 2013/01/18. doi: 10.1371/journal.pntd.0002006 23326619; PubMed Central PMCID: PMC3542153.
71. Taylor S, Wakem M, Dijkman G, Alsarraj M, Nguyen M. A practical approach to RT-qPCR-Publishing data that conform to the MIQE guidelines. Methods. 2010;50(4):S1–5. Epub 2010/03/11. doi: 10.1016/j.ymeth.2010.01.005 20215014.
72. Chaparro V, Leroux LP, Zimmermann A, Jardim A, Johnston B, Descoteaux A, et al. Leishmania donovani lipophosphoglycan increases macrophage-dependent chemotaxis of CXCR6-expressing cells via CXCL16 induction. Infect Immun. 2019;87(5):00064–19. Epub 2019/02/26. doi: 10.1128/iai.00064-19 30804103.
73. Ramskold D, Wang ET, Burge CB, Sandberg R. An abundance of ubiquitously expressed genes revealed by tissue transcriptome sequence data. PLoS Comput Biol. 2009;5(12):e1000598. Epub 2009/12/17. doi: 10.1371/journal.pcbi.1000598 20011106; PubMed Central PMCID: PMC2781110.
74. Liang S, Bellato HM, Lorent J, Lupinacci FCS, Oertlin C, van Hoef V, et al. Polysome-profiling in small tissue samples. Nucleic Acids Res. 2018;46(1):e3. Epub 2017/10/27. doi: 10.1093/nar/gkx940 29069469; PubMed Central PMCID: PMC5758873.
75. Kim D, Langmead B, Salzberg SL. HISAT: a fast spliced aligner with low memory requirements. Nat Methods. 2015;12(4):357–60. Epub 2015/03/10. doi: 10.1038/nmeth.3317 25751142; PubMed Central PMCID: PMC4655817.
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