Release of Small RNA-containing Exosome-like Vesicles from the Human Filarial Parasite Brugia malayi

PLoS Neglected Tropical Diseases

Volumn 9, Issue 9, 2015, Pages

  Zamanian, Mostafa ^a,b   Fraser, Lisa M ^a   Agbedanu, Prince N ^a   Harischandra, Hiruni ^a   Moorhead, Andrew R ^c   Day, Tim A ^a   Bartholomay, Lyric C ^d   Kimber, Michael J ^a  

^a IOWA STATE UNIVERSITY   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

^c UNIVERSITY OF GEORGIA   (United States)

^d UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLONY STIMULATING FACTOR 1; EOTAXIN; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; GRANULOCYTE COLONY STIMULATING FACTOR; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 13; INTERLEUKIN 15; INTERLEUKIN 17; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 3; INTERLEUKIN 4; INTERLEUKIN 5; INTERLEUKIN 6; INTERLEUKIN 7; INTERLEUKIN 9; LEUKEMIA INHIBITORY FACTOR RECEPTOR; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; MICRORNA; MONOCYTE CHEMOTACTIC PROTEIN 1; RANTES; SMALL NUCLEAR RNA; TUMOR NECROSIS FACTOR ALPHA; UNINDEXED DRUG; VASCULOTROPIN; HELMINTH PROTEIN; SMALL UNTRANSLATED RNA;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD SAMPLING; BRUGIA MALAYI; CELL STRUCTURE; CELL TRACKING; CELL VACUOLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; EXOSOME; FEMALE; GENE SEQUENCE; IMMUNE RESPONSE; LIQUID CHROMATOGRAPHY; MACROPHAGE; MALE; MASS SPECTROMETRY; NONHUMAN; PARASITE VIABILITY; PHENOTYPE; PROTEOMICS; RNA BINDING; RNA ISOLATION; TRANSMISSION ELECTRON MICROSCOPY; ANIMAL; CELL LINE; CHEMISTRY; ELECTRON MICROSCOPY; IMMUNOLOGY; METABOLISM; PHAGOCYTOSIS; ULTRASTRUCTURE;

ANIMALS; BRUGIA MALAYI; CELL LINE; EXOSOMES; HELMINTH PROTEINS; MACROPHAGES; MICROSCOPY, ELECTRON; PHAGOCYTOSIS; RNA, SMALL UNTRANSLATED;

EID: 84943178967     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0004069     Document Type: Article

References (72)

1. Global programme to eliminate lymphatic filariasis: progress report, 2011. Weekly Epidemiological Record. 2012 Sep;87(37):346–356. 22977953
2. Bartholomay LC, Christensen BM, Klei TR, Rajan TV, Vector-parasite interactions in mosquito-borne filariasis. The Filaria. Springer Science & Business Media; 2002.
3. Erickson SM, Xi Z, Mayhew GF, Ramirez JL, Aliota MT, Christensen BM, et al. Mosquito infection responses to developing filarial worms. PLoS Neglected Tropical Diseases. 2009;3(10):e529. doi: 10.1371/journal.pntd.0000529 19823571
4. Allen JE, Maizels RM, Diversity and dialogue in immunity to helminths. Nature reviews Immunology. 2011 Jun;11(6):375–388. doi: 10.1038/nri2992 21610741
5. Maizels RM, Pearce EJ, Artis D, Yazdanbakhsh M, Wynn TA, Regulation of pathogenesis and immunity in helminth infections. The Journal of Experimental Medicine. 2009 Sep;206(10):2059–2066. doi: 10.1084/jem.20091903 19770272
6. van Riet E, Hartgers FC, Yazdanbakhsh M, Chronic helminth infections induce immunomodulation: Consequences and mechanisms. Immunobiology. 2007 Jun;212(6):475–490. doi: 10.1016/j.imbio.2007.03.009 17544832
7. Hoerauf A, Satoguina J, Saeftel M, Specht S, Immunomodulation by filarial nematodes. Parasite Immunology. 2005 Oct;27(10–11):417–429. doi: 10.1111/j.1365-3024.2005.00792.x 16179035
8. Devaney E, Osborne J, The third-stage larva (L3) of Brugia: its role in immune modulation and protective immunity. Microbes and Infection. 2000 Sep;2(11):1363–1371. doi: 10.1016/S1286-4579(00)01290-9 11018453
9. Zang X, Yazdanbakhsh M, Jiang H, Kanost MR, Maizels RM, A novel serpin expressed by blood-borne microfilariae of the parasitic nematode Brugia malayi inhibits human neutrophil serine proteinases. Blood. 1999 Aug;94(4):1418–1428. 10438730
10. Zang X, Atmadja AK, Gray P, Allen JE, Gray CA, Lawrence RA, et al. The serpin secreted by Brugia malayi microfilariae, Bm-SPN-2, elicits strong, but short-lived, immune responses in mice and humans. Journal of immunology (Baltimore, Md: 1950). 2000 Nov;165(9):5161–5169. doi: 10.4049/jimmunol.165.9.5161
11. Falcone FH, Loke P, Zang X, MacDonald AS, Maizels RM, Allen JE, A Brugia malayi homolog of macrophage migration inhibitory factor reveals an important link between macrophages and eosinophil recruitment during nematode infection. Journal of immunology (Baltimore, Md: 1950). 2001 Nov;167(9):5348–5354. doi: 10.4049/jimmunol.167.9.5348
12. Zang X, Taylor P, Wang JM, Meyer DJ, Scott AL, Walkinshaw MD, et al. Homologues of human macrophage migration inhibitory factor from a parasitic nematode. Gene cloning, protein activity, and crystal structure. The Journal of biological chemistry. 2002 Nov;277(46):44261–44267. doi: 10.1074/jbc.M204655200 12221083
13. Hewitson JP, Harcus YM, Curwen RS, Dowle AA, Atmadja AK, Ashton PD, et al. The secretome of the filarial parasite, Brugia malayi: proteomic profile of adult excretory-secretory products. Molecular and Biochemical Parasitology. 2008 Jul;160(1):8–21. doi: 10.1016/j.molbiopara.2008.02.007 18439691
14. Moreno Y, Geary TG, Stage- and gender-specific proteomic analysis of Brugia malayi excretory-secretory products. PLoS Neglected Tropical Diseases. 2008;2(10):e326. doi: 10.1371/journal.pntd.0000326 18958170
15. Bennuru S, Semnani R, Meng Z, Ribeiro JMC, Veenstra TD, Nutman TB, Brugia malayi excreted/secreted proteins at the host/parasite interface: stage- and gender-specific proteomic profiling. PLoS Neglected Tropical Diseases. 2009;3(4):e410. doi: 10.1371/journal.pntd.0000410 19352421
16. Geary J, Satti M, Moreno Y, Madrill N, Whitten D, Headley SA, et al. First analysis of the secretome of the canine heartworm, Dirofilaria immitis. Parasites & vectors. 2012;5(1):140. doi: 10.1186/1756-3305-5-140
17. Tawill S, Le Goff L, Ali F, Blaxter M, Allen JE, Both free-living and parasitic nematodes induce a characteristic Th2 response that is dependent on the presence of intact glycans. Infection and immunity. 2004 Jan;72(1):398–407. doi: 10.1128/IAI.72.1.398-407.2004 14688121
18. Valadi H, Ekström K, Bossios A, Sjöstrand M, Lee JJ, Lötvall JO, Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nature cell biology. 2007 Jun;9(6):654–659. doi: 10.1038/ncb1596 17486113
19. Mittelbrunn M, Gutiérrez-Vázquez C, Villarroya-Beltri C, González S, Sánchez-Cabo F, González MÁ, et al. Unidirectional transfer of microRNA-loaded exosomes from T cells to antigen-presenting cells. Nature communications. 2011;2:282. doi: 10.1038/ncomms1285 21505438
20. Vickers KC, Palmisano BT, Shoucri BM, Shamburek RD, Remaley AT, Corrigendum: MicroRNAs are transported in plasma and delivered to recipient cells by high-density lipoproteins. Nature cell biology. 2014 Dec;17(1):104–104. doi: 10.1038/ncb3074
21. Montecalvo A, Larregina AT, Shufesky WJ, Stolz DB, Sullivan MLG, Karlsson JM, et al. Mechanism of transfer of functional microRNAs between mouse dendritic cells via exosomes. Blood. 2012 Jan;119(3):756–766. doi: 10.1182/blood-2011-02-338004 22031862
22. Chen X, Liang H, Zhang J, Zen K, Zhang CY, Secreted microRNAs: a new form of intercellular communication. Trends in cell biology. 2012 Mar;22(3):125–132. doi: 10.1016/j.tcb.2011.12.001 22260888
23. Kalra H, Simpson RJ, Ji H, Aikawa E, Altevogt P, Askenase P, et al. Vesiclepedia: a compendium for extracellular vesicles with continuous community annotation. PLoS biology. 2012;10(12):e1001450. doi: 10.1371/journal.pbio.1001450 23271954
24. van Niel G, Porto-Carreiro I, Simoes S, Raposo G, Exosomes: a common pathway for a specialized function. Journal of biochemistry. 2006 Jul;140(1):13–21. doi: 10.1093/jb/mvj128 16877764
25. Lakkaraju A, Rodriguez-Boulan E, Itinerant exosomes: emerging roles in cell and tissue polarity. Trends in cell biology. 2008 May;18(5):199–209. doi: 10.1016/j.tcb.2008.03.002 18396047
26. Buck AH, Coakley G, Simbari F, McSorley HJ, Quintana JF, Le Bihan T, et al. Exosomes secreted by nematode parasites transfer small RNAs to mammalian cells and modulate innate immunity. Nature communications. 2014;5:5488. doi: 10.1038/ncomms6488 25421927
27. Twu O, de Miguel N, Lustig G, Stevens GC, Vashisht AA, Wohlschlegel JA, et al. Trichomonas vaginalis Exosomes Deliver Cargo to Host Cells and Mediate Host Parasite Interactions. PLoS Pathogens. 2013;9(7):e1003482. doi: 10.1371/journal.ppat.1003482 23853596
28. Marcilla A, Trelis M, Cortés A, Sotillo J, Cantalapiedra F, Minguez MT, et al. Extracellular vesicles from parasitic helminths contain specific excretory/secretory proteins and are internalized in intestinal host cells. PLoS ONE. 2012;7(9):e45974. doi: 10.1371/journal.pone.0045974 23029346
29. Bernal D, Trelis M, Montaner S, Cantalapiedra F, Galiano A, Hackenberg M, et al. Surface analysis of Dicrocoelium dendriticum. The molecular characterization of exosomes reveals the presence of miRNAs. Journal of proteomics. 2014 Jun;105:232–241. doi: 10.1016/j.jprot.2014.02.012 24561797
30. Silverman JM, Clos J, de’Oliveira CC, Shirvani O, Fang Y, Wang C, et al. An exosome-based secretion pathway is responsible for protein export from Leishmania and communication with macrophages. Journal of cell science. 2010 Mar;123(Pt 6):842–852. doi: 10.1242/jcs.056465 20159964
31. Chen XM, Splinter PL, O’Hara SP, LaRusso NF, A cellular micro-RNA, let-7i, regulates Toll-like receptor 4 expression and contributes to cholangiocyte immune responses against Cryptosporidium parvum infection. The Journal of biological chemistry. 2007 Sep;282(39):28929–28938. doi: 10.1074/jbc.M702633200 17660297
32. Kumar M, Ahmad T, Sharma A, Mabalirajan U, Kulshreshtha A, Agrawal A, et al. Let-7 microRNA-mediated regulation of IL-13 and allergic airway inflammation. The Journal of allergy and clinical immunology. 2011 Nov;128(5):1077–85. e1–10 doi: 10.1016/j.jaci.2011.04.034 21616524
33. Banerjee S, Xie N, Cui H, Tan Z, Yang S, Icyuz M, et al. MicroRNA let-7c regulates macrophage polarization. Journal of immunology (Baltimore, Md: 1950). 2013 Jun;190(12):6542–6549. doi: 10.4049/jimmunol.1202496
34. Lodish HF, Zhou B, Liu G, Chen CZ, Micromanagement of the immune system by microRNAs. Nature reviews Immunology. 2008 Feb;8(2):120–130. doi: 10.1038/nri2252 18204468
35. Simpson RJ, Kalra H, Mathivanan S, ExoCarta as a resource for exosomal research. Journal of extracellular vesicles. 2012;1(0):569. doi: 10.3402/jev.v1i0.18374
36. Chen CY, Hogan MC, Ward CJ, Purification of exosome-like vesicles from urine. Methods in enzymology. 2013;524:225–241. doi: 10.1016/B978-0-12-397945-2.00013-5 23498743
37. Bennuru S, Semnani R, Meng Z, Ribeiro JM, Veenstra TD, Nutman TB, Brugia malayi excreted/secreted proteins at the host/parasite interface: stage-and gender-specific proteomic profiling. PLoS neglected tropical diseases. 2009;3(4):e410. doi: 10.1371/journal.pntd.0000410 19352421
38. Huntley RP, Sawford T, Mutowo-Meullenet P, Shypitsyna A, Bonilla C, Martin MJ, et al. The GOA database: Gene Ontology annotation updates for 2015. Nucleic Acids Research. 2015 Jan;43(Database issue):D1057–63. doi: 10.1093/nar/gku1113 25378336
39. Binns D, Dimmer E, Huntley R, Barrell D, O’Donovan C, Apweiler R, QuickGO: a web-based tool for Gene Ontology searching. Bioinformatics. 2009 Nov;25(22):3045–3046. doi: 10.1093/bioinformatics/btp536 19744993
40. Guiliano DB, Hong X, McKerrow JH, Blaxter ML, Oksov Y, Liu J, et al. A gene family of cathepsin L-like proteases of filarial nematodes are associated with larval molting and cuticle and eggshell remodeling. Molecular and biochemical parasitology. 2004;136(2):227–242. doi: 10.1016/j.molbiopara.2004.03.015 15478801
41. Ford L, Zhang J, Liu J, Hashmi S, Fuhrman JA, Oksov Y, et al. Functional analysis of the cathepsin-like cysteine protease genes in adult Brugia malayi using RNA interference. PLoS Neglected tropical diseases. 2009;3(2):e377. doi: 10.1371/journal.pntd.0000377 19190745
42. Song C, Gallup JM, Day TA, Bartholomay LC, Kimber MJ, Development of an in vivo RNAi protocol to investigate gene function in the filarial nematode, Brugia malayi. PLoS pathogens. 2010;6(12):e1001239. doi: 10.1371/journal.ppat.1001239 21203489
43. Lustigman S, Zhang J, Liu J, Oksov Y, Hashmi S, RNA interference targeting cathepsin L and Z-like cysteine proteases of Onchocerca volvulus confirmed their essential function during L3 molting. Molecular and biochemical parasitology. 2004;138(2):165–170. doi: 10.1016/j.molbiopara.2004.08.003 15555728
44. Rhoads M, Fetterer R, Developmentally regulated secretion of cathepsin L-like cysteine proteases by Haemonchus contortus. The Journal of parasitology. 1995;p. 505–512. doi: 10.2307/3283844 7623189
45. Dalton JP, Neill SO, Stack C, Collins P, Walshe A, Sekiya M, et al. Fasciola hepatica cathepsin L-like proteases: biology, function, and potential in the development of first generation liver fluke vaccines. International journal for parasitology. 2003;33(11):1173–1181. doi: 10.1016/S0020-7519(03)00171-1 13678633
46. Marcilla A, Trelis M, Cortés A, Sotillo J, Cantalapiedra F, Minguez MT, et al. Extracellular vesicles from parasitic helminths contain specific excretory/secretory proteins and are internalized in intestinal host cells. PLoS One. 2012;7(9):e45974. doi: 10.1371/journal.pone.0045974 23029346
47. Friedländer MR, Mackowiak SD, Li N, Chen W, Rajewsky N, miRDeep2 accurately identifies known and hundreds of novel microRNA genes in seven animal clades. Nucleic Acids Research. 2012 Jan;40(1):37–52. doi: 10.1093/nar/gkr688 21911355
48. Tritten L, Burkman E, Moorhead A, Satti M, Geary J, Mackenzie C, et al. Detection of circulating parasite-derived microRNAs in filarial infections. PLoS neglected tropical diseases. 2014;8(7):e2971. doi: 10.1371/journal.pntd.0002971 25033073
49. Tritten L, O’Neill M, Nutting C, Wanji S, Njouendoui A, Fombad F, et al. Loa loa and Onchocerca ochengi miRNAs detected in host circulation. Molecular and biochemical parasitology. 2014;198(1):14–17. doi: 10.1016/j.molbiopara.2014.11.001 25461483
50. Quintana JF, Makepeace BL, Babayan SA, Ivens A, Pfarr KM, Blaxter M, et al. Extracellular Onchocerca-derived small RNAs in host nodules and blood. Parasites & vectors. 2015;8(1):58. doi: 10.1186/s13071-015-0656-1
51. Johnson SM, Grosshans H, Shingara J, Byrom M, Jarvis R, Cheng A, et al. RAS Is Regulated by the let-7 MicroRNA Family. Cell. 2005 Mar;120(5):635–647. doi: 10.1016/j.cell.2005.01.014 15766527
52. Johnson CD, Esquela-Kerscher A, Stefani G, Byrom M, Kelnar K, Ovcharenko D, et al. The let-7 microRNA represses cell proliferation pathways in human cells. Cancer research. 2007 Aug;67(16):7713–7722. doi: 10.1158/0008-5472.CAN-07-1083 17699775
53. Roush S, Slack FJ, The let-7 family of microRNAs. Trends in cell biology. 2008 Oct;18(10):505–516. doi: 10.1016/j.tcb.2008.07.007 18774294
54. Schulte LN, Eulalio A, Mollenkopf HJ, Reinhardt R, Vogel J, Analysis of the host microRNA response to Salmonella uncovers the control of major cytokines by the let-7 family. The EMBO Journal. 2011 May;30(10):1977–1989. doi: 10.1038/emboj.2011.94 21468030
55. Androulidaki A, Iliopoulos D, Arranz A, Doxaki C, Schworer S, Zacharioudaki V, et al. The Kinase Akt1 Controls Macrophage Response to Lipopolysaccharide by Regulating MicroRNAs. Immunity. 2009 Aug;31(2):220–231. doi: 10.1016/j.immuni.2009.06.024 19699171
56. Liu G, Abraham E, MicroRNAs in immune response and macrophage polarization. Arteriosclerosis, Thrombosis, and Vascular Biology. 2013 Feb;33(2):170–177. doi: 10.1161/ATVBAHA.112.300068 23325473
57. van Helden SFG, van Leeuwen FN, Figdor CG, Human and murine model cell lines for dendritic cell biology evaluated. Immunology letters. 2008 May;117(2):191–197. doi: 10.1016/j.imlet.2008.02.003 18384885
58. Feng D, Zhao WL, Ye YY, Bai XC, Liu RQ, Chang LF, et al. Cellular internalization of exosomes occurs through phagocytosis. Traffic. 2010;11(5):675–687. doi: 10.1111/j.1600-0854.2010.01041.x 20136776
59. Atay S, Gercel-Taylor C, Taylor DD, Human Trophoblast-Derived Exosomal Fibronectin Induces Pro-Inflammatory Il-1β Production by Macrophages. American Journal of Reproductive Immunology. 2011;66(4):259–269. doi: 10.1111/j.1600-0897.2011.00995.x 21410811
60. Taylor MJ, Cross HF, Bilo K, Inflammatory responses induced by the filarial nematode Brugia malayi are mediated by lipopolysaccharide-like activity from endosymbiotic Wolbachia bacteria. The Journal of Experimental Medicine. 2000 Apr;191(8):1429–1436. doi: 10.1084/jem.191.8.1429 10770808
61. Osborne J, Hunter SJ, Devaney E, Anti-interleukin-4 modulation of the Th2 polarized response to the parasitic nematode Brugia pahangi. Infection and immunity. 1996;64(9):3461–3466. 8751885
62. Allen JE, Macdonald AS, Profound suppression of cellular proliferation mediated by the secretions of nematodes. Parasite immunology. 1998;20(5):241–247. doi: 10.1046/j.1365-3024.1998.00151.x 9651925
63. Weinkopff T, Mackenzie C, Eversole R, Lammie PJ, Filarial Excretory-Secretory Products Induce Human Monocytes to Produce Lymphangiogenic Mediators. PLoS neglected tropical diseases. 2014;8(7):e2893. doi: 10.1371/journal.pntd.0002893 25010672
64. Amano F, Akamatsu Y, A lipopolysaccharide (LPS)-resistant mutant isolated from a macrophagelike cell line, J774.1, exhibits an altered activated-macrophage phenotype in response to LPS. Infection and immunity. 1991 Jun;59(6):2166–2174. 1645329
65. Anand PK, Anand E, Bleck CK, Anes E, Griffiths G, Exosomal Hsp70 induces a pro-inflammatory response to foreign particles including mycobacteria. PLoS One. 2010;5(4):e10136. doi: 10.1371/journal.pone.0010136 20405033
66. Atay S, Gercel-Taylor C, Suttles J, Mor G, Taylor DD, Trophoblast-Derived Exosomes Mediate Monocyte Recruitment and Differentiation. American Journal of Reproductive Immunology. 2011;65(1):65–77. doi: 10.1111/j.1600-0897.2010.00880.x 20560914
67. Macdonald W, Selection of a strain of Aedes-aegypti susceptible to infectionwith semi-periodic Brugia-malayi. Annals of Tropical Medicine and Parasitology. 1962;56(3):368.
68. Filipe V, Hawe A, Jiskoot W, Critical evaluation of Nanoparticle Tracking Analysis (NTA) by NanoSight for the measurement of nanoparticles and protein aggregates. Pharmaceutical research. 2010;27(5):796–810. doi: 10.1007/s11095-010-0073-2 20204471
69. Gordon A, Hannon G. Fastx-toolkit. FASTQ/A short-reads pre-processing tools. 2010; Available: http://hannonlab.cshl.edu/fastx_toolkit
70. Griffiths-Jones S, Saini HK, van Dongen S, Enright AJ, miRBase: tools for microRNA genomics. Nucleic Acids Research. 2008 Jan;36(Database issue):D154–8. doi: 10.1093/nar/gkm952 17991681
71. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ, Basic local alignment search tool. Journal of Molecular Biology. 1990 Oct;215(3):403–410. doi: 10.1016/S0022-2836(05)80360-2 2231712
72. Wickham, H. ggplot2; 2009.