Exosomal RNA from Mycobacterium tuberculosis-Infected Cells Is Functional in Recipient Macrophages

Traffic

Volumn 16, Issue 6, 2015, Pages 555-571

  Singh, Prachi Pratap ^a   Li, Li ^a   Schorey, Jeffrey Scott ^a  

^a UNIVERSITY OF NOTRE DAME   (United States)

Author keywords

Exosomes; Macrophage; MicroRNA; MRNA; Mycobacterium tuberculosis

Indexed keywords

BACTERIAL RNA; MESSENGER RNA; MICRORNA;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL COMMUNICATION; CONTROLLED STUDY; EXOSOME; IMMUNE RESPONSE; IMMUNOREGULATION; MACROPHAGE; MEDIATOR RELEASE; MOUSE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; ANIMAL; CELL LINE; GENETICS; METABOLISM; MICROBIOLOGY; PATHOGENICITY;

ANIMALS; CELL LINE; EXOSOMES; MACROPHAGES; MICE; MICRORNAS; MYCOBACTERIUM TUBERCULOSIS; RNA, BACTERIAL; RNA, MESSENGER;

EID: 84929291867     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/tra.12278     Document Type: Article

References (60)

1. Schorey JS, Bhatnagar S. Exosome function: from tumor immunology to pathogen biology. Traffic 2008;9:871-881.
2. Thery C, Ostrowski M, Segura E. Membrane vesicles as conveyors of immune responses. Nat Rev Immunol 2009;9:581-593.
3. Raposo G, Stoorvogel W. Extracellular vesicles: exosomes, microvesicles, and friends. J Cell Biol 2013;200:373-383.
4. Buschow SI, Nolte-'t Hoen EN, van Niel G, Pols MS, ten Broeke T, Lauwen M, Ossendorp F, Melief CJ, Raposo G, Wubbolts R, Wauben MH, Stoorvogel W. MHC II in dendritic cells is targeted to lysosomes or T cell-induced exosomes via distinct multivesicular body pathways. Traffic 2009;10:1528-1542.
5. Al-Nedawi K, Szemraj J, Cierniewski CS. Mast cell-derived exosomes activate endothelial cells to secrete plasminogen activator inhibitor type 1. Arterioscler Thromb Vasc Biol 2005;25:1744-1749.
6. Azevedo LC, Janiszewski M, Pontieri V, Pedro Mde A, Bassi E, Tucci PJ, Laurindo FR. Platelet-derived exosomes from septic shock patients induce myocardial dysfunction. Crit Care 2007;11:R120.
7. Bhatnagar S, Schorey JS. Exosomes released from infected macrophages contain Mycobacterium avium glycopeptidolipids and are proinflammatory. J Biol Chem 2007;282:25779-25789.
8. Guescini M, Genedani S, Stocchi V, Agnati LF. Astrocytes and glioblastoma cells release exosomes carrying mt DNA. J Neural Transm 2010;117:1-4.
9. Faure J, Lachenal G, Court M, Hirrlinger J, Chatellard-Causse C, Blot B, Grange J, Schoehn G, Goldberg Y, Boyer V, Kirchhoff F, Raposo G, Garin J, Sadoul R. Exosomes are released by cultured cortical neurones. Mol Cell Neurosci 2006;31:642-648.
10. Buning J, von Smolinski D, Tafazzoli K, Zimmer KP, Strobel S, Apostolaki M, Kollias G, Heath JK, Ludwig D, Gebert A. Multivesicular bodies in intestinal epithelial cells: responsible for MHC class II-restricted antigen processing and origin of exosomes. Immunology 2008;125:510-521.
11. Caby MP, Lankar D, Vincendeau-Scherrer C, Raposo G, Bonnerot C. Exosomal-like vesicles are present in human blood plasma. Int Immunol 2005;17:879-887.
12. Pisitkun T, Shen RF, Knepper MA. Identification and proteomic profiling of exosomes in human urine. Proc Natl Acad Sci USA 2004;101:13368-13373.
13. Admyre C, Johansson SM, Qazi KR, Filen JJ, Lahesmaa R, Norman M, Neve EP, Scheynius A, Gabrielsson S. Exosomes with immune modulatory features are present in human breast milk. J Immunol 2007;179:1969-1978.
14. Admyre C, Grunewald J, Thyberg J, Gripenback S, Tornling G, Eklund A, Scheynius A, Gabrielsson S. Exosomes with major histocompatibility complex class II and co-stimulatory molecules are present in human BAL fluid. Eur Res J 2003;22:578-583.
15. Michael A, Bajracharya SD, Yuen PS, Zhou H, Star RA, Illei GG, Alevizos I. Exosomes from human saliva as a source of microRNA biomarkers. Oral Dis 2010;16:34-38.
16. Lasser C, O'Neil SE, Ekerljung L, Ekstrom K, Sjostrand M, Lotvall J. RNA-containing exosomes in human nasal secretions. Am J Rhinol Allergy 2011;25:89-93.
17. Johnstone RM, Adam M, Hammond JR, Orr L, Turbide C. Vesicle formation during reticulocyte maturation. Association of plasma membrane activities with released vesicles (exosomes). J Biol Chem 1987;262:9412-9420.
18. Harding C, Heuser J, Stahl P. Endocytosis and intracellular processing of transferrin and colloidal gold-transferrin in rat reticulocytes: demonstration of a pathway for receptor shedding. Eur J Cell Biol 1984;35:256-263.
19. Raposo G, Nijman HW, Stoorvogel W, Liejendekker R, Harding CV, Melief CJ, Geuze HJ. B lymphocytes secrete antigen-presenting vesicles. J Exp Med 1996;183:1161-1172.
20. Chaput N, Thery C. Exosomes: immune properties and potential clinical implementations. Semin Immunopathol 2011;33:419-440.
21. Qazi KR, Gehrmann U, Domange Jordo E, Karlsson MC, Gabrielsson S. Antigen-loaded exosomes alone induce Th1-type memory through a B-cell-dependent mechanism. Blood 2009;113:2673-2683.
22. Lugini L, Cecchetti S, Huber V, Luciani F, Macchia G, Spadaro F, Paris L, Abalsamo L, Colone M, Molinari A, Podo F, Rivoltini L, Ramoni C, Fais S. Immune surveillance properties of human NK cell-derived exosomes. J Immunol 2012;189:2833-2842.
23. Karlsson M, Lundin S, Dahlgren U, Kahu H, Pettersson I, Telemo E. "Tolerosomes" are produced by intestinal epithelial cells. Eur J Immunol 2001;31:2892-2900.
24. Simpson RJ, Jensen SS, Lim JW. Proteomic profiling of exosomes: current perspectives. Proteomics 2008;8:4083-4099.
25. Valadi H, Ekstrom K, Bossios A, Sjostrand M, Lee JJ, Lotvall JO. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 2007;9:654-659.
26. Mittelbrunn M, Gutierrez-Vazquez C, Villarroya-Beltri C, Gonzalez S, Sanchez-Cabo F, Gonzalez MA, Bernad A, Sanchez-Madrid F. Unidirectional transfer of microRNA-loaded exosomes from T cells to antigen-presenting cells. Nat Commun 2011;2:282.
27. Montecalvo A, Larregina AT, Shufesky WJ, Stolz DB, Sullivan ML, Karlsson JM, Baty CJ, Gibson GA, Erdos G, Wang Z, Milosevic J, Tkacheva OA, Divito SJ, Jordan R, Lyons-Weiler J, et al. Mechanism of transfer of functional microRNAs between mouse dendritic cells via exosomes. Blood 2012;119:756-766.
28. Skog J, Wurdinger T, van Rijn S, Meijer DH, Gainche L, Sena-Esteves M, Curry WT Jr, Carter BS, Krichevsky AM, Breakefield XO. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol 2008;10:1470-1476.
29. Hunter MP, Ismail N, Zhang X, Aguda BD, Lee EJ, Yu L, Xiao T, Schafer J, Lee ML, Schmittgen TD, Nana-Sinkam SP, Jarjoura D, Marsh CB. Detection of microRNA expression in human peripheral blood microvesicles. PLoS One 2008;3:e3694.
30. Giri PK, Kruh NA, Dobos KM, Schorey JS. Proteomic analysis identifies highly antigenic proteins in exosomes from M. tuberculosis-infected and culture filtrate protein-treated macrophages. Proteomics 2010;10:3190-3202.
31. Giri PK, Schorey JS. Exosomes derived from M. bovis BCG infected macrophages activate antigen-specific CD4+ and CD8+ T cells in vitro and in vivo. PLoS One 2008;3:e2461.
32. Cheng Y, Schorey JS. Exosomes carrying mycobacterial antigens can protect mice against Mycobacterium tuberculosis infection. Eur J Immunol 2013;43:3279-3290.
33. Singh PP, LeMaire C, Tan JC, Zeng E, Schorey JS. Exosomes released from M. tuberculosis infected cells can suppress IFN-gamma mediated activation of naive macrophages. PLoS One 2011;6:e18564.
34. Singh PP, Smith VL, Karakousis PC, Schorey JS. Exosomes isolated from mycobacteria-infected mice or cultured macrophages can recruit and activate immune cells in vitro and in vivo. J Immunol 2012;189:777-785.
35. Singh PK, Singh AV, Chauhan DS. Current understanding on micro RNAs and its regulation in response to Mycobacterial infections. J Biomed Sci 2013;20:14.
36. Singh Y, Kaul V, Mehra A, Chatterjee S, Tousif S, Dwivedi VP, Suar M, Van Kaer L, Bishai WR, Das G. Mycobacterium tuberculosis controls microRNA-99b (miR-99b) expression in infected murine dendritic cells to modulate host immunity. J Biol Chem 2013;288:5056-5061.
37. Fu Y, Yi Z, Wu X, Li J, Xu F. Circulating microRNAs in patients with active pulmonary tuberculosis. J Clin Microbiol 2011;49:4246-4251.
38. Miotto P, Mwangoka G, Valente IC, Norbis L, Sotgiu G, Bosu R, Ambrosi A, Codecasa LR, Goletti D, Matteelli A, Ntinginya EN, Aloi F, Heinrich N, Reither K, Cirillo DM. miRNA signatures in sera of patients with active pulmonary tuberculosis. PLoS One 2013;8:e80149.
39. Qi Y, Cui L, Ge Y, Shi Z, Zhao K, Guo X, Yang D, Yu H, Cui L, Shan Y, et al. Altered serum microRNAs as biomarkers for the early diagnosis of pulmonary tuberculosis infection. BMC Infect Dis 2012;12:384-392.
40. Wang C, Yang S, Sun G, Tang X, Lu S, Neyrolles O, Gao Q. Comparative miRNA expression profiles in individuals with latent and active tuberculosis. PLoS One 2011;6:e25832.
41. Meyer SU, Pfaffl MW, Ulbrich SE. Normalization strategies for microRNA profiling experiments: a 'normal' way to a hidden layer of complexity? Biotechnol Lett 2010;32:1777-1788.
42. Bellingham SA, Coleman BM, Hill AF. Small RNA deep sequencing reveals a distinct miRNA signature released in exosomes from prion-infected neuronal cells. Nucleic Acids Res 2012;40:10937-10949.
43. Kogure T, Lin WL, Yan IK, Braconi C, Patel T. Intercellular nanovesicle-mediated microRNA transfer: a mechanism of environmental modulation of hepatocellular cancer cell growth. Hepatology 2011;54:1237-1248.
44. Saiga H, Nishimura J, Kuwata H, Okuyama M, Matsumoto S, Sato S, Matsumoto M, Akira S, Yoshikai Y, Honda K, Yamamuto M, Takeda K. Lipocalin2 dependent inhibition of mycobacterial growth in alveolar epithelium. J Immunol 2008;181:8251-8257.
45. Obregón-Henao A, Duque-Correa MA, Rojas M, García LF, Brennan PJ, Ortiz BL, Belisle JT. Stable extracellular RNA fragments of Mycobacterium tuberculosis induce early apoptosis in human monocytes via a caspase-8 dependent mechanism. PLoS One 2012;7:e29970.
46. McDonald MK, Tian Y, Qureshi RA, Gormley M, Ertel A, Gao R, Lopez EA, Alexander GM, Sacan A, Fortina P, Ajit SK. Functional significance of macrophage-derived exosomes in inflammation and pain. Pain 2014;155:1527-1539.
47. Gallo A, Tandon M, Alevizos I, Illei GG. The majority of microRNAs detectable in serum and saliva is concentrated in exosomes. PLoS One 2012;7:e30679.
48. Sinha A, Yadav AK, Chakraborty S, Kabra SK, Lodha R, Kumar M, Kulshreshtha A, Sethi T, Pandey R, Malik G, Laddha S, Mukhopadhyay A, Dash D, Ghosh B, Agrawal A. Exosome-enclosed microRNAs in exhaled breath hold potential for biomarker discovery in patients with pulmonary diseases. J Allergy Clin Immunol 2013;132:219-222.
49. Kumar R, Halder P, Sahu SK, Kumar M, Kumari M, Jana K, Ghosh Z, Sharma P, Kundu M, Basu J. Identification of a novel role of ESAT-6-dependent miR-155 induction during infection of macrophages with Mycobacterium tuberculosis. Cell Microbiol 2012;14:1620-1631.
50. Villaroya-Beltri C, Gutierrez-Vazquez C, Sanchez-Cabo F, Perez-Hernandez D, Vazquez J, Martin-Cofreces N, Martinez-Herrera DJ, Pascual-Montano A, Mittelbrum M, Sanchez-Madrid F. Sumoylated hnRNPA2B1 controls the sorting of miRNAs into exosomes through binding to specific motifs. Nat Commun 2013;4:2980.
51. Dreux M, Garaigorta U, Boyd B, Decembre E, Chung J, Whitler-Bauer C, Wieland S, Chisari FV. Short range exosomal transfer of viral RNA from infected cells to plasmacytoid dendritic cells triggers innate immunity. Cell Host Microbe 2012;12:558-570.
52. Narayanan A, Iordanskiy S, Das R, Van Duyne R, Santos S, Jaworski E, Guendel I, Sampey G, Dalby E, Iglesias-Ussel M, Popratiloff A, Hakami R, Kehn-Hall K, Young M, Subra C, et al. Exosomes derived from HIV-1-infected cells contain trans-activation response element RNA. J Biol Chem 2013;288:20014-20033.
53. Pegtel DM, Cosmopoulos K, Thorley-Lawson DA, van Eijndhovena MAJ, Hopmansa ES, Lindenberg JL, de Gruijl TD, Würdinger T, Middeldorp JM. Functional delivery of viral miRNAs via exosomes. Proc Natl Acad Sci USA 2010;107:6328-6333.
54. Manzanillo PS, Shiloh MU, Portnoy DA, Cox JS. Mycobacterium tuberculosis activates the DNA-dependent cytosolic surveillance pathway within macrophages. Cell Host Microbe 2012;11:469-480.
55. Abdullah Z, Schlee M, Roth S, Mraheil MA, Barchet W, Bottcher J, Hain T, Geiger S, Hayakawa Y, Fritz JH, Civril F, Hopfner KP, Kurts C, Ruland J, Hartmann G, et al. RIG-I detects infection with live Listeria by sensing secreted bacterial nucleic acids. EMBO J 2012;31:4153-4164.
56. Fernandes-Alnemri T, Yu JW, Juliana C, Solorzano L, Kang S, Wu J, Datta P, McCormick M, Huang L, McDermott E, Eisenlohr L, Landel CP, Alnemri ES. The AIM2 inflammasome is critical for innate immunity to Francisella tularensis. Nat Immunol 2010;11:385-393.
57. Sauer JD, Witte CE, Zemansky J, Hanson B, Lauer P, Portnoy DA. Listeria monocytogenes triggers AIM2-mediated pyroptosis upon infrequent bacteriolysis in the macrophage cytosol. Cell Host Microbe 2010;7:412-419.
58. Sander LE, Davis MJ, Boekschoten MV, Amsen D, Dascher CC, Ryffel B, Swanson JA, Muller M, Blander JM. Detection of prokaryotic mRNA signifies microbial viability and promotes immunity. Nature 2011;474:385-389.
59. Morin RD, O'Connor MD, Griffith M, Kuchenbauer F, Delaney A, Prabhu AL, Zhao Y, McDonald H, Zeng T, Hirst M, Eaves CJ, Marra MA, et al. Application of massively parallel sequencing to microRNA profiling and discovery in human embryonic stem cells. Genome Res 2008;18:610-621.
60. Draghici S, Khatri P, Tarca AL, Amin K, Done A, Voichita C, Georgescu C, Romero R. A systems biology approach for pathway level analysis. Genome Res 2007;17:1537-1545.