Exosome-transported microRNAs of helminth origin: New tools for allergic and autoimmune diseases therapy?

Parasite Immunology

Volumn 37, Issue 4, 2015, Pages 208-214

  Siles Lucas, M ^a   Morchon, R ^b   Simon, F ^b   Manzano Roman, R ^a  

^a INSTITUTO DE RECURSOS NATURALES Y AGROBIOLOGÍA DE SALAMANCA   (Spain)

^b UNIVERSITY OF SALAMANCA   (Spain)

Author keywords

Diseases; Exosomes; Helminths; MiRNAs; Therapeutics

Indexed keywords

MICRORNA; HELMINTH RNA;

ALLERGIC DISEASE; ARTICLE; AUTOIMMUNE DISEASE; CELL COMMUNICATION; CELL EXPANSION; DISEASE EXACERBATION; DOWN REGULATION; EXOSOME; HELMINTH; HELMINTHIASIS; HOST CELL; HOST PARASITE INTERACTION; HUMAN; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; IMMUNOMODULATION; IMMUNOREGULATION; IMMUNOSTIMULATION; INFLAMMATION; INNATE IMMUNITY; INTERNALIZATION; MEDIATOR RELEASE; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; TH2 CELL; ANIMAL; AUTOIMMUNE DISEASES; CHEMISTRY; CLASSIFICATION; CYTOLOGY; HYPERSENSITIVITY; IMMUNOLOGY; PARASITOLOGY;

VERMES;

ANIMALS; AUTOIMMUNE DISEASES; EXOSOMES; HELMINTHIASIS; HELMINTHS; HUMANS; HYPERSENSITIVITY; INFLAMMATION; MICRORNAS; RNA, HELMINTH; T-LYMPHOCYTES, REGULATORY;

EID: 84924814941     PISSN: 01419838     EISSN: 13653024     Source Type: Journal    
DOI: 10.1111/pim.12182     Document Type: Article

References (70)

1. Maizels RM, McSorley HJ & Smyth DJ. Helminths in the hygiene hypothesis: sooner or later? Clin Exp Immunol 2014; 177: 38-46.
2. Olszak T, An D, Zeissig S, et al. Microbial exposure during early life has persistent effects on natural killer T cell function. Science 2012; 336: 489-493.
3. von Hertzen L, Hanski I & Haahtela T. Natural immunity. Biodiversity loss and inflammatory diseases are two global megatrends that might be related. EMBO Rep 2011; 12: 1089-1093.
4. Finlay CM, Walsh KP & Mills KH. Induction of regulatory cells by helminth parasites: exploitation for the treatment of inflammatory diseases. Immunol Rev 2014; 259: 206-230.
5. Tilp C, Kapur V, Loging W & Erb KJ. Prerequisites for the pharmaceutical industry to develop and commercialise helminths and helminth-derived product therapy. Int J Parasitol 2013; 43: 319-325.
6. Khan AR & Fallon PG. Helminth therapies: translating the unknown unknowns to known knowns. Int J Parasitol 2013; 43: 293-299.
7. Camussi G, Deregibus MC, Bruno S, Cantaluppi V & Biancone L. Exosomes/microvesicles as a mechanism of cell-to-cell communication. Kidney Int 2010; 78: 838-848.
8. Buck AH, Coakley G, Simbari F, et al. Exosomes secreted by nematode parasites transfer small RNAs to mammalian cells and modulate innate immunity. Nat Commun 2014; 5: 5488.
9. Montaner S, Galiano A, Trelis M, et al. The role of extracellular vesicles in modulating the host immune response during parasitic infections. Front Immunol 2014; 5: 433.
10. Bernal D, Trelis M, Montaner S, et al. Surface analysis of Dicrocoelium dendriticum. The molecular characterization of exosomes reveals the presence of miRNAs. J Proteomics 2014; 105: 232-241.
11. Manzano-Román R & Siles-Lucas M. MicroRNAs in parasitic diseases: potential for diagnosis and targeting. Mol Biochem Parasitol 2012; 186: 81-86.
12. Chua JH, Armugam A & Jeyaseelan K. MicroRNAs: biogenesis, function and applications. Curr Opin Mol Ther 2009; 11: 189-199.
13. Mobergslien A & Sioud M. Exosome-derived miRNAs and cellular miRNAs activate innate immunity. J Innate Immun 2014; 6: 105-110.
14. Rebane A & Akdis CA. MicroRNAs: essential players in the regulation of inflammation. J Allergy Clin Immunol 2013; 132: 15-26.
15. Gracias DT & Katsikis PD. MicroRNAs: key components of immune regulation. Adv Exp Med Biol 2011; 780: 15-26.
16. Mishra PK, Palma M, Bleich D, Loke P & Gause WC. Systemic impact of intestinal helminth infections. Mucosal Immunol 2014; 7: 753-762.
17. Caraballo L & Zakzuk J. The evolution of the Th2 immune responses and its relationships with parasitic diseases and allergy. Biomedica 2012; 32: 145-157.
18. Diaz A & Allen JE. Mapping immune response profiles: the emerging scenario from helminth immunology. Eur J Immunol 2007; 37: 3319-3326.
19. Allen JE & Maizels RM. Diversity and dialogue in immunity to helminths. Nat Rev Immunol 2011; 11: 375-388.
20. Citro A, Barnaba V & Martini H. From T cell apoptosis to chronic immune activation in inflammatory diseases. Int Arch Allergy Immunol 2014; 164: 140-146.
21. Maizels RM & Smith KA. Regulatory T cells in infection. Adv Immunol 2011; 112: 73-136.
22. Nono JK, Pletinckx K, Lutz MB & Brehm K. Excretory/secretory-products of Echinococcus multilocularis larvae induce apoptosis and tolerogenic properties in dendritic cells in vitro. PLoS Negl Trop Dis 2012; 6: e1516.
23. Park HK, Cho MK, Choi SH, Kim YS & Yu HS. Trichinella spiralis: infection reduces airway allergic inflammation in mice. Exp Parasitol 2011; 127: 539-544.
24. Yang X, Yang Y, Wang Y, et al. Excretory/secretory products from Trichinella spiralis adult worms ameliorate DSS-induced colitis in mice. PLoS ONE 2014; 9: e96454.
25. Ilic N1, Gruden-Movsesijan A & Sofronic-Milosavljevic L. Trichinella spiralis: shaping the immune response. Immunol Res 2012; 52: 111-119.
26. Hartmann S, Schnoeller C, Dahten A, et al. Gastrointestinal nematode infection interferes with experimental allergic airway inflammation but not atopic dermatitis. Clin Exp Allergy 2009; 39: 1585-1596.
27. Leung J, Hang L, Blum A, Setiawan T, Stoyanoff K & Weinstock J. Heligmosomoides polygyrus abrogates antigen-specific gut injury in a murine model of inflammatory bowel disease. Inflamm Bowel Dis 2012; 18: 1447-1455.
28. Croese J, Giacomin P, Navarro S, et al. Experimental hookworm infection and gluten microchallenge promote tolerance in celiac disease. J Allergy Clin Immunol 2014; 6749: 01010.
29. Lund ME, O'Brien BA, Hutchinson AT, et al. Secreted proteins from the helminth Fasciola hepatica inhibit the initiation of autoreactive T cell responses and prevent diabetes in the NOD mouse. PLoS ONE 2014; 9: e86289.
30. + regulatory T cells delay expulsion of intestinal nematodes by suppression of IL-9-driven mast cell activation in BALB/c but not in C57BL/6 mice. PLoS Pathog 2014; 10: e1003913.
31. Song X, Shen J, Wen H, et al. Impact of Schistosoma japonicum infection on collagen-induced arthritis in DBA/1 mice: a murine model of human rheumatoid arthritis. PLoS ONE 2011; 6: e23453.
32. Liu JY, Li LY, Yang XZ, et al. Adoptive transfer of dendritic cells isolated from helminth-infected mice enhanced T regulatory cell responses in airway allergic inflammation. Parasite Immunol 2011; 33: 525-534.
33. Pacifico LG1, Marinho FA, Fonseca CT, et al. Schistosoma mansoni antigens modulate experimental allergic asthma in a murine model: a major role for CD4+ CD25+ Foxp3+ T cells independent of interleukin-10. Infect Immun 2009; 77: 98-107.
34. Correale J & Farez MF. Parasite infections in multiple sclerosis modulate immune responses through a retinoic acid-dependent pathway. J Immunol 2013; 191: 3827-3837.
35. Schabussova I1, Ul-Haq O, Hoflehner E, et al. Oesophagostomum dentatum extract modulates T cell-dependent immune responses to bystander antigens and prevents the development of allergy in mice. PLoS ONE 2013; 8: e67544.
36. Rzepecka J, Siebeke I, Coltherd JC, et al. The helminth product, ES-62, protects against airway inflammation by resetting the Th cell phenotype. Int J Parasitol 2013; 43: 211-223.
37. Katoh S, Oomizu S, Niki T, et al. Possible regulatory role of galectin-9 on Ascaris suum-induced eosinophilic lung inflammation in mice. Int Arch Allergy Immunol 2012; 158(Suppl 1): 58-65.
38. Adalid-Peralta L, Fleury A, Garcia-Ibarra TM, et al. Human neurocysticercosis: in vivo expansion of peripheral regulatory T cells and their recruitment in the central nervous system. J Parasitol 2012; 98: 142-148.
39. Jeong YI, Kim SH, Ju JW, et al. Clonorchis sinensis-derived total protein attenuates airway inflammation in murine asthma model by inducing regulatory T cells and modulating dendritic cell functions. Biochem Biophys Res Commun 2011; 407: 793-800.
40. Cho MK, Lee CH & Yu HS. Amelioration of intestinal colitis by macrophage migration inhibitory factor isolated from intestinal parasites through toll-like receptor 2. Parasite Immunol 2011; 33: 265-275.
41. Hubner MP, Stocker JT & Mitre E. Inhibition of type 1 diabetes in filaria-infected nonobese diabetic mice is associated with a T helper type 2 shift and induction of FoxP3+ regulatory T cells. Immunology 2009; 127: 512-522.
42. Garlanda C, Anders HJ & Mantovani A. TIR8/SIGIRR: an IL-1R/TLR family member with regulatory functions in inflammation and T cell polarization. Trends Immunol 2009; 30: 439-446.
43. Jeker LT, Zhou X, Blelloch R & Bluestone JA. DGCR8-mediated production of canonical microRNAs is critical for regulatory T cell function and stability. PLoS ONE 2013; 8: e66282.
44. Magen E, Borkow G, Bentwich Z, Mishal J & Scharf S. Can worms defend our hearts? Chronic helminthic infections may attenuate the development of cardiovascular diseases. Med Hypotheses 2005; 64: 904-909.
45. Magen E, Bychkov V, Ginovker A & Kashuba E. Chronic Opisthorchis felineus infection attenuates atherosclerosis-an autopsy study. Int J Parasitol 2013; 43: 819-824.
46. Jin B, Sun T, Yu XH, Yang YX & Yeo AE. The effects of TLR activation on T-cell development and differentiation. Clin Dev Immunol 2012; 2012: 836485.
47. Vukman KV, Adams PN, Metz M, Maurer M & O'Neill SM. Fasciola hepatica tegumental coat impairs mast cells' ability to drive Th1 immune responses. J Immunol 2013; 190: 2873-2879.
48. Denzer K, Kleijmeer MJ, Heijnen HF, Stoorvogel W & Geuze HJ. Exosome: from internal vesicle of the multivesicular body to intercellular signaling device. J Cell Sci 2000; 113(Pt 19): 3365-3374.
49. Chaput N & Thery C. Exosomes: immune properties and potential clinical implementations. Semin Immunopathol 2011; 33: 419-440.
50. Agarwal A, Fanelli G, Letizia M, et al. Regulatory T cell-derived exosomes: possible therapeutic and diagnostic tools in transplantation. Front Immunol 2014; 5: 555.
51. Tili E, Michaille JJ, Cimino A, et al. 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 2007; 179: 5082-5089.
52. Xue X, Sun J, Zhang Q, Wang Z, Huang Y & Pan W. Identification and characterization of novel microRNAs from Schistosoma japonicum. PLoS ONE 2008; 3: e4034.
53. Fabbri M, Paone A, Calore F, Galli R & Croce CM. A new role for microRNAs, as ligands of Toll-like receptors. RNA Biol 2013; 10: 169-174.
54. Klinker MW, Lizzio V, Reed TJ, Fox DA & Lundy SK. Human B cell-derived lymphoblastoid cell lines constitutively produce fas ligand and secrete MHCII(+)FasL(+) killer exosomes. Front Immunol 2014; 5: 144.
55. Whiteside TL. Immune modulation of T-cell and NK (natural killer) cell activities by TEXs (tumour-derived exosomes). Biochem Soc Trans 2013; 41: 245-251.
56. Luchetti F, Canonico B, Arcangeletti M, et al. Fas signalling promotes intercellular communication in T cells. PLoS ONE 2012; 7: e35766.
57. Fleury A, Martinez MC & Le Lay S. Extracellular vesicles as therapeutic tools in cardiovascular diseases. Front Immunol 2014; 5: 370.
58. Robbins PD & Morelli AE. Regulation of immune responses by extracellular vesicles. Nat Rev Immunol 2014; 14: 195-208.
59. Alvarez-Erviti L, Seow Y, Yin H, Betts C, Lakhal S & Wood MJ. Delivery of siRNA to the mouse brain by systemic injection of targeted exosomes. Nat Biotechnol 2011; 29: 341-345.
60. Ohno S, Takanashi M, Sudo K, et al. Systemically injected exosomes targeted to EGFR deliver antitumor microRNA to breast cancer cells. Mol Ther 2013; 21: 185-191.
61. Tan A, Rajadas J & Seifalian AM. Exosomes as nano-theranostic delivery platforms for gene therapy. Adv Drug Deliv Rev 2013; 65: 357-367.
62. Mittelbrunn M, Gutierrez-Vazquez C, Villarroya-Beltri C, et al. Unidirectional transfer of microRNA-loaded exosomes from T cells to antigen-presenting cells. Nat Commun 2011; 2: 282.
63. Akao Y, Iio A, Itoh T, et al. Microvesicle-mediated RNA molecule delivery system using monocytes/macrophages. Mol Ther 2011; 19: 395-399.
64. Wahlgren J, De L Karlson T, Brisslert M, et al. Plasma exosomes can deliver exogenous short interfering RNA to monocytes and lymphocytes. Nucleic Acids Res 2012; 40: e130.
65. Hood JL, Scott MJ & Wickline SA. Maximizing exosome colloidal stability following electroporation. Anal Biochem 2014; 448: 41-49.
66. Kooijmans SA, Stremersch S, Braeckmans K, et al. Electroporation-induced siRNA precipitation obscures the efficiency of siRNA loading into extracellular vesicles. J Control Release 2013; 172: 229-238.
67. Jo W, Jeong D, Kim J, et al. Microfluidic fabrication of cell-derived nanovesicles as endogenous RNA carriers. Lab Chip 2014; 14: 1261-1269.
68. Pawitan JA. The possible use of RNA interference in diagnosis and treatment of various diseases. Int J Clin Pract 2009; 63: 1378-1385.
69. Chevillet JR, Kang Q, Ruf IK, et al. Quantitative and stoichiometric analysis of the microRNA content of exosomes. Proc Natl Acad Sci USA 2014; 111: 14888-14893.
70. Cortez MA, Bueso-Ramos C, Ferdin J, Lopez-Berestein G, Sood AK & Calin GA. MicroRNAs in body fluids-the mix of hormones and biomarkers. Nat Rev Clin Oncol 2011; 8: 467-477.