AAV8-Mediated in vivo overexpression of miR-155 enhances the protective capacity of genetically attenuated malarial parasites

Molecular Therapy

Volumn 22, Issue 12, 2014, Pages 2130-2141

  Hentzschel, Franziska ^a   Hammerschmidt Kamper, Christiane ^a   Börner, Kathleen ^a   Heiss, Kirsten ^a   Knapp, Bettina ^b,c,d,e   Sattler, Julia M ^a   Kaderali, Lars ^b,c,d   Castoldi, Mirco ^f   Bindman, Julia G ^g   Malato, Yann ^h   Willenbring, Holger ^g,h   Mueller, Ann Kristin ^a   Grimm, Dirk ^a,c  

^a UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c Network Cluster of Excellence   (Germany)

^d DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^e INSTITUTE OF EPIDEMIOLOGY   (Germany)

^f UNIVERSITY HOSPITAL DÜSSELDORF   (Germany)

^g UNIVERSITY OF CALIFORNIA   (United States)

^h UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; GENETICALLY ATTENUATED MALARIAL PARASITE VACCINE; MALARIA VACCINE; MICRORNA 155; PARVOVIRUS VECTOR; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; LIVE VACCINE; MESSENGER RNA; MICRORNA; MIRN155 MICRORNA, HUMAN;

ADENO ASSOCIATED VIRUS 8; ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; KUPFFER CELL; LIVER CELL; MALARIA; MALE; MOUSE; NONHUMAN; SPOROZOITE; UPREGULATION; ADMINISTRATION AND DOSAGE; ANIMAL; DEPENDOPARVOVIRUS; DISEASE MODEL; GENE VECTOR; GENETICS; HEK293 CELL LINE; HUMAN; IMMUNOLOGY; LIVER; METABOLISM; PATHOGENICITY; PATHOLOGY; PLASMODIUM BERGHEI;

ADENO-ASSOCIATED VIRUS - 8; MAMMALIA; MURINAE; MUS; PLASMODIUM PARASITES; PROTOZOA;

ANIMALS; DEPENDOVIRUS; DISEASE MODELS, ANIMAL; GENETIC VECTORS; HEK293 CELLS; HUMANS; LIVER; MALARIA; MALARIA VACCINES; MALE; MICE; MICRORNAS; PLASMODIUM BERGHEI; RNA, MESSENGER; UP-REGULATION; VACCINES, ATTENUATED;

EID: 84927177580     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2014.172     Document Type: Article

References (58)

1. Murray, CJ, Rosenfeld, LC, Lim, SS, Andrews, KG, Foreman, KJ, Haring, D et al. (2012). Global malaria mortality between 1980 and 2010: a systematic analysis. Lancet 379: 413-431.
2. Snow, RW, Guerra, CA, Noor, AM, Myint, HY and Hay, SI (2005). The global distribution of clinical episodes of Plasmodium falciparum malaria. Nature 434: 214-217.
3. Lingelbach, K and Joiner, KA (1998). The parasitophorous vacuole membrane surrounding Plasmodium and Toxoplasma: an unusual compartment in infected cells. J Cell Sci 111 (Pt 11): 1467-1475.
4. Rodrigues, CD, Hannus, M, Prudncio, M, Martin, C, Gonalves, LA, Portugal, S et al. (2008). Host scavenger receptor SR-BI plays a dual role in the establishment of malaria parasite liver infection. Cell Host Microbe 4: 271-282.
5. Mikolajczak, SA, Jacobs-Lorena, V, MacKellar, DC, Camargo, N and Kappe, SH (2007). L-FABP is a critical host factor for successful malaria liver stage development. Int J Parasitol 37: 483-489.
6. Liehl, P, Zuzarte-Lus, V, Chan, J, Zillinger, T, Baptista, F, Carapau, D et al. (2014). Hostcell sensors for Plasmodium activate innate immunity against liver-stage infection. Nat Med 20: 47-53.
7. Nussenzweig, RS, Vanderberg, J, Most, H and Orton, C (1967). Protective immunity produced by the injection of x-irradiated sporozoites of plasmodium berghei. Nature 216: 160-162.
8. Mueller, AK, Labaied, M, Kappe, SH and Matuschewski, K (2005). Genetically modified Plasmodium parasites as a protective experimental malaria vaccine. Nature 433: 164-167.
9. Hoffman, SL, Goh, LM, Luke, TC, Schneider, I, Le, TP, Doolan, DL et al. (2002). Protection of humans against malaria by immunization with radiation-attenuated Plasmodium falciparum sporozoites. J Infect Dis 185: 1155-1164.
10. Seder, RA, Chang, LJ, Enama, ME, Zephir, KL, Sarwar, UN, Gordon, IJ et al.; VRC 312 Study Team. (2013). Protection against malaria by intravenous immunization with a nonreplicating sporozoite vaccine. Science 341: 1359-1365.
11. Mueller, AK, Deckert, M, Heiss, K, Goetz, K, Matuschewski, K and Schlter, D (2007). Genetically attenuated Plasmodium berghei liver stages persist and elicit sterile protection primarily via CD8 T cells. Am J Pathol 171: 107-115.
12. Jobe, O, Lumsden, J, Mueller, AK, Williams, J, Silva-Rivera, H, Kappe, SH et al. (2007). Genetically attenuated Plasmodium berghei liver stages induce sterile protracted protection that is mediated by major histocompatibility complex Class I-dependent interferon-gamma-producing CD8+ T cells. J Infect Dis 196: 599-607.
13. Trimnell, A, Takagi, A, Gupta, M, Richie, TL, Kappe, SH and Wang, R (2009). Genetically attenuated parasite vaccines induce contact-dependent CD8+ T cell killing of Plasmodium yoelii liver stage-infected hepatocytes. J Immunol 183: 5870-5878.
14. Nganou-Makamdop, K, van Gemert, GJ, Arens, T, Hermsen, CC and Sauerwein, RW (2012). Long term protection after immunization with P. berghei sporozoites correlates with sustained IFN? responses of hepatic CD8+ memory T cells. PLoS ONE 7: e36508.
15. Schofield, L, Villaquiran, J, Ferreira, A, Schellekens, H, Nussenzweig, R and Nussenzweig, V (1987). Gamma interferon, CD8+ T cells and antibodies required for immunity to malaria sporozoites. Nature 330: 664-666.
16. Skalsky, RL and Cullen, BR (2010). Viruses, microRNAs, and host interactions. Annu Rev Microbiol 64: 123-141.
17. Tili, E, Michaille, JJ and Croce, CM (2013). MicroRNAs play a central role in molecular dysfunctions linking inflammation with cancer. Immunol Rev 253: 167-184.
18. Thorn, CF, Lu, ZY and Whitehead, AS (2004). Regulation of the human acute phase serum amyloid A genes by tumour necrosis factor-alpha, interleukin-6 and glucocorticoids in hepatic and epithelial cell lines. Scand J Immunol 59: 152-158.
19. Jopling, C (2012). Liver-specific microRNA-122: Biogenesis and function. RNA Biol 9: 137-142.
20. Chen, CZ, Schaffert, S, Fragoso, R and Loh, C (2013). Regulation of immune responses and tolerance: the microRNA perspective. Immunol Rev 253: 112-128.
21. Tarun, AS, Baer, K, Dumpit, RF, Gray, S, Lejarcegui, N, Frevert, U et al. (2006). Quantitative isolation and in vivo imaging of malaria parasite liver stages. Int J Parasitol 36: 1283-1293.
22. Pradel, G and Frevert, U (2001). Malaria sporozoites actively enter and pass through rat Kupffer cells prior to hepatocyte invasion. Hepatology 33: 1154-1165.
23. OConnell, RM, Taganov, KD, Boldin, MP, Cheng, G and Baltimore, D (2007). MicroRNA-155 is induced during the macrophage inflammatory response. Proc Natl Acad Sci USA 104: 1604-1609.
24. Kutty, RK, Nagineni, CN, Samuel, W, Vijayasarathy, C, Hooks, JJ and Redmond, TM (2010). Inflammatory cytokines regulate microRNA-155 expression in human retinal pigment epithelial cells by activating JAK/STAT pathway. Biochem Biophys Res Commun 402: 390-395.
25. OConnell, RM, Chaudhuri, AA, Rao, DS and Baltimore, D (2009). Inositol phosphatase SHIP1 is a primary target of miR-155. Proc Natl Acad Sci USA 106: 7113-7118.
26. Wang, P, Hou, J, Lin, L, Wang, C, Liu, X, Li, D et al. (2010). Inducible microRNA-155 feedback promotes type I IFN signaling in antiviral innate immunity by targeting suppressor of cytokine signaling 1. J Immunol 185: 6226-6233.
27. van Dijk, R, Montenegro-Miranda, PS, Riviere, C, Schilderink, R, ten Bloemendaal, L, van Gorp, J et al. (2013). Polyinosinic acid blocks adeno-associated virus macrophage endocytosis in vitro and enhances adeno-associated virus liver-directed gene therapy in vivo. Hum Gene Ther 24: 807-813.
28. Grimm, D, Streetz, KL, Jopling, CL, Storm, TA, Pandey, K, Davis, CR et al. (2006). Fatality in mice due to oversaturation of cellular microRNA/short hairpin RNA pathways. Nature 441: 537-541.
29. Faraoni, I, Antonetti, FR, Cardone, J and Bonmassar, E (2009). miR-155 gene: a typical multifunctional microRNA. Biochim Biophys Acta 1792: 497-505.
30. Monk, CE, Hutvagner, G and Arthur, JS (2010). Regulation of miRNA transcription in macrophages in response to Candida albicans. PLoS ONE 5: e13669.
31. Bala, S, Tilahun, Y, Taha, O, Alao, H, Kodys, K, Catalano, D et al. (2012). Increased microRNA-155 expression in the serum and peripheral monocytes in chronic HCV infection. J Transl Med 10: 151.
32. Ghorpade, DS, Leyland, R, Kurowska-Stolarska, M, Patil, SA and Balaji, KN (2012). MicroRNA-155 is required for Mycobacterium bovis BCG-mediated apoptosis of macrophages. Mol Cell Biol 32: 2239-2253.
33. Cai, P, Piao, X, Liu, S, Hou, N, Wang, H and Chen, Q (2013). MicroRNA-gene expression network in murine liver during Schistosoma japonicum infection. PLoS ONE 8: e67037.
34. Cremer, TJ, Ravneberg, DH, Clay, CD, Piper-Hunter, MG, Marsh, CB, Elton, TS et al. (2009). MiR-155 induction by F. novicida but not the virulent F. tularensis results in SHIP down-regulation and enhanced pro-inflammatory cytokine response. PLoS ONE 4: e8508.
35. Rodriguez, A, Vigorito, E, Clare, S, Warren, MV, Couttet, P, Soond, DR et al. (2007). Requirement of bic/microRNA-155 for normal immune function. Science 316: 608-611.
36. Oertli, M, Engler, DB, Kohler, E, Koch, M, Meyer, TF and Mller, A (2011). MicroRNA-155 is essential for the T cell-mediated control of Helicobacter pylori infection and for the induction of chronic Gastritis and Colitis. J Immunol 187: 3578-3586.
37. Vigorito, E, Perks, KL, Abreu-Goodger, C, Bunting, S, Xiang, Z, Kohlhaas, S et al. (2007). microRNA-155 regulates the generation of immunoglobulin class-switched plasma cells. Immunity 27: 847-859.
38. Thai, TH, Calado, DP, Casola, S, Ansel, KM, Xiao, C, Xue, Y et al. (2007). Regulation of the germinal center response by microRNA-155. Science 316: 604-608.
39. OConnell, RM, Kahn, D, Gibson, WS, Round, JL, Scholz, RL, Chaudhuri, AA et al. (2010). MicroRNA-155 promotes autoimmune inflammation by enhancing inflammatory T cell development. Immunity 33: 607-619.
40. Gracias, DT, Stelekati, E, Hope, JL, Boesteanu, AC, Doering, TA, Norton, J et al. (2013). The microRNA miR-155 controls CD8(+) T cell responses by regulating interferon signaling. Nat Immunol 14: 593-602.
41. Zhang, Y, Wei, W, Cheng, N, Wang, K, Li, B, Jiang, X et al. (2012). Hepatitis C virusinduced up-regulation of microRNA-155 promotes hepatocarcinogenesis by activating Wnt signaling. Hepatology 56: 1631-1640.
42. Chang, S, Wang, RH, Akagi, K, Kim, KA, Martin, BK, Cavallone, L et al.; Kathleen Cuningham Foundation Consortium for Research into Familial Breast Cancer (kConFab). (2011). Tumor suppressor BRCA1 epigenetically controls oncogenic microRNA-155. Nat Med 17: 1275-1282.
43. OConnell, RM, Rao, DS, Chaudhuri, AA, Boldin, MP, Taganov, KD, Nicoll, J et al. (2008). Sustained expression of microRNA-155 in hematopoietic stem cells causes a myeloproliferative disorder. J Exp Med 205: 585-594.
44. Kurowska-Stolarska, M, Alivernini, S, Ballantine, LE, Asquith, DL, Millar, NL, Gilchrist, DS et al. (2011). MicroRNA-155 as a proinflammatory regulator in clinical and experimental arthritis. Proc Natl Acad Sci USA 108: 11193-11198.
45. Worm, J, Stenvang, J, Petri, A, Frederiksen, KS, Obad, S, Elmn, J et al. (2009). Silencing of microRNA-155 in mice during acute inflammatory response leads to derepression of c/ebp Beta and down-regulation of G-CSF. Nucleic Acids Res 37: 5784-5792.
46. Huffaker, TB, Hu, R, Runtsch, MC, Bake, E, Chen, X, Zhao, J et al. (2012). Epistasis between microRNAs 155 and 146a during T cell-mediated antitumor immunity. Cell Rep 2: 1697-1709.
47. Clare, S, John, V, Walker, AW, Hill, JL, Abreu-Goodger, C, Hale, C et al. (2013). Enhanced susceptibility to Citrobacter rodentium infection in microRNA-155-deficient mice. Infect Immun 81: 723-732.
48. Miller, AM, Gilchrist, DS, Nijjar, J, Araldi, E, Ramirez, CM, Lavery, CA et al. (2013). MiR-155 has a protective role in the development of non-alcoholic hepatosteatosis in mice. PLoS ONE 8: e72324.
49. Aucher, A, Rudnicka, D and Davis, DM (2013). MicroRNAs transfer from human macrophages to hepato-carcinoma cells and inhibit proliferation. J Immunol 191: 6250-6260.
50. Kota, J, Chivukula, RR, ODonnell, KA, Wentzel, EA, Montgomery, CL, Hwang, HW et al. (2009). Therapeutic microRNA delivery suppresses tumorigenesis in a murine liver cancer model. Cell 137: 1005-1017.
51. Janssen, HL, Reesink, HW, Lawitz, EJ, Zeuzem, S, Rodriguez-Torres, M, Patel, K et al. (2013). Treatment of HCV infection by targeting microRNA. N Engl J Med 368: 1685-1694.
52. Ebert, MS, Neilson, JR and Sharp, PA (2007). MicroRNA sponges: competitive inhibitors of small RNAs in mammalian cells. Nat Methods 4: 721-726.
53. Heymans, S, Corsten, MF, Verhesen, W, Carai, P, van Leeuwen, RE, Custers, K et al. (2013). Macrophage microRNA-155 promotes cardiac hypertrophy and failure. Circulation 128: 1420-1432.
54. Schrmann, N, Trabuco, LG, Bender, C, Russell, RB and Grimm, D (2013). Molecular dissection of human Argonaute proteins by DNA shuffling. Nat Struct Mol Biol 20: 818-826.
55. Brner, K, Niopek, D, Cotugno, G, Kaldenbach, M, Pankert, T, Willemsen, J et al. (2013). Robust RNAi enhancement via human Argonaute-2 overexpression from plasmids, viral vectors and cell lines. Nucleic Acids Res 41: e199.
56. Castoldi, M, Vujic Spasic, M, Altamura, S, Elmn, J, Lindow, M, Kiss, J et al. (2011). The liver-specific microRNA miR-122 controls systemic iron homeostasis in mice. J Clin Invest 121: 1386-1396.
57. Hellemans, J, Mortier, G, De Paepe, A, Speleman, F and Vandesompele, J (2007). qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biol 8: R19.
58. Froh, M, Konno, A and Thurman, RG (2003). Isolation of liver Kupffer cells. Curr Protoc Toxicol Chapter 14: Unit14.4.