Characterization of exosome-like vesicles released from human tracheobronchial ciliated epithelium: A possible role in innate defense

FASEB Journal

Volumn 23, Issue 6, 2009, Pages 1858-1868

  Kesimer, Mehmet ^a   Scull, Margaret ^a   Brighton, Brian ^a   DeMaria, Genevieve ^a   Burns, Kimberlie ^a   O'Neal, Wanda ^a   Pickles, Raymond J ^a   Sheehan, John K ^a,b  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b CB#7248 ^*  (United States)

Author keywords

Glycocalyx; Influenza virus; Mucins; Mucus; Sialic acid

Indexed keywords

CD63 ANTIGEN; MUCIN 1; MUCIN 16; MUCIN 4; RNA; TUMOR SUSCEPTIBILITY GENE 101 PROTEIN; UNCLASSIFIED DRUG; MUCIN;

ARTICLE; CELL CULTURE; CELL ISOLATION; CILIATED EPITHELIUM; CONTROLLED STUDY; ELECTRON MICROSCOPY; EXOSOME; FLOW CYTOMETRY; HUMAN; IMMUNOBLOTTING; INFLUENZA; INFLUENZA VIRUS; INNATE IMMUNITY; LIGHT SCATTERING; MASS SPECTROMETRY; PRIORITY JOURNAL; ANIMAL; CHEMISTRY; CYTOLOGY; CYTOPLASM VESICLE; DOG; EPITHELIUM CELL; GENETICS; IMMUNOELECTRON MICROSCOPY; IMMUNOLOGY; INFLUENZA VIRUS A; ISOLATION AND PURIFICATION; METABOLISM; ORTHOMYXOVIRUS INFECTION; PATHOGENICITY; PHYSIOLOGY; RESPIRATORY TRACT MUCOSA; ULTRASTRUCTURE;

HUMAN INFLUENZA VIRUS; ORTHOMYXOVIRIDAE;

ANIMALS; CELLS, CULTURED; CYTOPLASMIC VESICLES; DOGS; EPITHELIAL CELLS; EXOSOMES; FLOW CYTOMETRY; HUMANS; IMMUNITY, INNATE; INFLUENZA A VIRUS; MICROSCOPY, IMMUNOELECTRON; MUCINS; ORTHOMYXOVIRIDAE INFECTIONS; RESPIRATORY MUCOSA; RNA;

EID: 67649365976     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.08-119131     Document Type: Article

References (55)

1. Sheehan, J. K., Kesimer, M., and Pickles, R. (2006) Innate immunity and mucus structure and function. Novartis Found. Symp. 279, 155-166; discussion 167-169, 216-219
2. Kesimer, M., Kirkham, S., Pickles, R. J., Henderson, A. G., Alexis, N. E., Demaria, G., Knight, D., Thornton, D. J., and Sheehan, J. K. (2008) Tracheobronchial air-liquid interface cell culture: a model for innate mucosal defense of the upper airways? Am. J. Physiol. Lung Cell Mol Physiol. 296, L92-L100
3. Ratajczak, J., Wysoczynski, M., Hayek, F., Janowska-Wieczorek, A., and Ratajczak, M. Z. (2006) Membrane-derived microvesicles: important and underappreciated mediators of cell-to-cell communication. Leukemia 20, 1487-1495 (Pubitemid 44264090)
4. Heijnen, H. F., Schiel, A. E., Fijnheer, R., Geuze, H. J., and Sixma, J. J. (1999) Activated platelets release two types of membrane vesicles: microvesicles by surface shedding and exosomes derived from exocytosis of multivesicular bodies and alpha-granules. Blood 94, 3791-3799
5. Hearn, P. R., Russell, R. G., and Farmer, J. (1981) The formation and orientation of brush border vesicles from rat duodenal mucosa. J. Cell Sci. 47, 227-236 (Pubitemid 11134483)
6. Piper, R. C., and Luzio, J. P. (2001) Late endosomes: sorting and partitioning in multivesicular bodies. Traffic 2, 612-621 (Pubitemid 32825700)
7. Van Niel, G., Raposo, G., Candalh, C., Boussac, M., Hershberg, R., Cerf-Bensussan, N., and Heyman, M. (2001) Intestinal epithelial cells secrete exosome-like vesicles. Gastroenterology 121, 337-349 (Pubitemid 32729381)
8. Kapsogeorgou, E. K., Abu-Helu, R. F., Moutsopoulos, H. M., and Manoussakis, M. N. (2005) Salivary gland epithelial cell exosomes: a source of autoantigenic ribonucleoproteins. Arthritis Rheum. 52, 1517-1521
9. Rieu, S., Geminard, C., Rabesandratana, H., Sainte-Marie, J., and Vidal, M. (2000) Exosomes released during reticulocyte maturation bind to fibronectin via integrin alpha4beta1. Eur. J. Biochem. 267, 583-590
10. Thery, C., Boussac, M., Veron, P., Ricciardi-Castagnoli, P., Raposo, G., Garin, J., and Amigorena, S. (2001) Proteomic analysis of dendritic cell-derived exosomes: a secreted subcellular compartment distinct from apoptotic vesicles. J. Immunol. 166, 7309-7318 (Pubitemid 32525606)
11. Escola, J. M., Kleijmeer, M. J., Stoorvogel, W., Griffith, J. M., Yoshie, O., and Geuze, H. J. (1998) Selective enrichment of tetraspan proteins on the internal vesicles of multivesicular endosomes and on exosomes secreted by human B-lymphocytes. J. Biol. Chem. 273, 20121-20127
12. Blanchard, N., Lankar, D., Faure, F., Regnault, A., Dumont, C., Raposo, G., and Hivroz, C. (2002) TCR activation of human T cells induces the production of exosomes bearing the TCR/ CD3/zeta complex. J. Immunol. 168, 3235-3241 (Pubitemid 34250383)
13. Skokos, D., Le Panse, S., Villa, I., Rousselle, J. C., Peronet, R., David, B., Namane, A., and Mecheri, S. (2001) Mast cell-dependent B and T lymphocyte activation is mediated by the secretion of immunologically active exosomes. J. Immunol. 166, 868-876 (Pubitemid 32060240)
14. Potolicchio, I., Carven, G. J., Xu, X., Stipp, C., Riese, R. J., Stern, L. J., and Santambrogio, L. (2005) Proteomic analysis of microglia- derived exosomes: metabolic role of the aminopeptidase CD13 in neuropeptide catabolism. J. Immunol. 175, 2237-2243 (Pubitemid 41113830)
15. Whiteside, T. L. (2005) Tumour-derived exosomes or microvesicles: another mechanism of tumour escape from the host immune system? Br. J. Cancer 92, 209-211
16. Wolfers, J., Lozier, A., Raposo, G., Regnault, A., Thery, C., Masurier, C., Flament, C., Pouzieux, S., Faure, F., Tursz, T., Angevin, E., Amigorena, S., and Zitvogel, L. (2001) Tumor-derived exosomes are a source of shared tumor rejection antigens for CTL cross-priming. Nat. Med. 7, 297-303
17. Pisitkun, T., Shen, R. F., and Knepper, M. A. (2004) Identification and proteomic profiling of exosomes in human urine. Proc. Natl. Acad. Sci. U. S. A. 101, 13368-13373
18. Admyre, C., Grunewald, J., Thyberg, J., Gripenback, S., Tornling, G., Eklund, A., Scheynius, A., and Gabrielsson, S. (2003) Exosomes with major histocompatibility complex class II and co-stimulatory molecules are present in human BAL fluid. Eur. Respir. J. 22, 578-583
19. Caby, M. P., Lankar, D., Vincendeau-Scherrer, C., Raposo, G., and Bonnerot, C. (2005) Exosomal-like vesicles are present in human blood plasma. Int. Immunol. 17, 879-887
20. Admyre, C., Johansson, S. M., Qazi, K. R., Filen, J. J., Lahesmaa, R., Norman, M., Neve, E. P., Scheynius, A., and Gabrielsson, S. (2007) Exosomes with immune modulatory features are present in human breast milk. J. Immunol. 179, 1969-1978
21. Aupeix, K., Hugel, B., Martin, T., Bischoff, P., Lill, H., Pasquali, J. L., and Freyssinet, J. M. (1997) The significance of shed membrane particles during programmed cell death in vitro, and in vivo, in HIV-1 infection. J. Clin. Invest. 99, 1546-1554
22. Thery, C., Zitvogel, L., and Amigorena, S. (2002) Exosomes: composition, biogenesis and function. Nat. Rev. Immunol. 2, 569-579
23. Schorey, J. S., and Bhatnagar, S. (2008) Exosome function: from tumor immunology to pathogen biology. Traffic 9, 871-881
24. Keller, S., Sanderson, M. P., Stoeck, A., and Altevogt, P. (2006) Exosomes: from biogenesis and secretion to biological function. Immunol. Lett. 107, 102-108
25. Van Niel, G., Porto-Carreiro, I., Simoes, S., and Raposo, G. (2006) Exosomes: a common pathway for a specialized function. J. Biochem. 140, 13-21 (Pubitemid 44433541)
26. Valadi, H., Ekstrom, K., Bossios, A., Sjostrand, M., Lee, J. J., and Lotvall, J. O. (2007) Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat. Cell Biol. 9, 654-659
27. Fulcher, M. L., Gabriel, S., Burns, K. A., Yankaskas, J. R., and Randell, S. H. (2005) Well-differentiated human airway epithelial cell cultures. Methods Mol. Med. 107, 183-206
28. Pickles, R. J., McCarty, D., Matsui, H., Hart, P. J., Randell, S. H., and Boucher, R. C. (1998) Limited entry of adenovirus vectors into well-differentiated airway epithelium is responsible for inefficient gene transfer. J. Virol. 72, 6014-6023 (Pubitemid 28283390)
29. Thery, C., Amigorena, S., Raposo, G., and Clayton, A. (2006) Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr. Protoc. Cell Biol. Chap. 3, Unit 3.22
30. Thornton, D. J., Howard, M., Devine, P. L., and Sheehan, J. K. (1995) Methods for separation and deglycosylation of mucin subunits. Anal. Biochem. 227, 162-167
31. Bard, M. P., Hegmans, J. P., Hemmes, A., Luider, T. M., Willemsen, R., Severijnen, L. A., van Meerbeeck, J. P., Burgers, S. A., Hoogsteden, H. C., and Lambrecht, B. N. (2004) Proteomic analysis of exosomes isolated from human malignant pleural effusions. Am. J. Respir. Cell Mol. Biol. 31, 114-121
32. Bhatnagar, S., Shinagawa, K., Castellino, F. J., and Schorey, J. S. (2007) Exosomes released from macrophages infected with intracellular pathogens stimulate a proinflammatory response in vitro and in vivo. Blood 110, 3234-3244 (Pubitemid 350106316)
33. Raposo, G., Nijman, H. W., Stoorvogel, W., Liejendekker, R., Harding, C. V., Melief, C. J., and Geuze, H. J. (1996) B lymphocytes secrete antigen-presenting vesicles. J. Exp. Med. 183, 1161-1172
34. Van Niel, G., Mallegol, J., Bevilacqua, C., Candalh, C., Brugiere, S., Tomaskovic-Crook, E., Heath, J. K., Cerf-Bensussan, N., and Heyman, M. (2003) Intestinal epithelial exosomes carry MHC class II/peptides able to inform the immune system in mice. Gut 52, 1690-1697 (Pubitemid 37510387)
35. Zitvogel, L., Regnault, A., Lozier, A., Wolfers, J., Flament, C., Tenza, D., Ricciardi-Castagnoli, P., Raposo, G., and Amigorena, S. (1998) Eradication of established murine tumors using a novel cell-free vaccine: dendritic cell-derived exosomes. Nat. Med. 4, 594-600
36. Ogawa, Y., Kanai-Azuma, M., Akimoto, Y., Kawakami, H., and Yanoshita, R. (2008) Exosome-like vesicles with dipeptidyl peptidase IV in human saliva. Biol. Pharm. Bull. 31, 1059-1062
37. Wubbolts, R., Leckie, R. S., Veenhuizen, P. T., Schwarzmann, G., Mobius, W., Hoernschemeyer, J., Slot, J. W., Geuze, H. J., and Stoorvogel, W. (2003) Proteomic and biochemical analyses of human B cell-derived exosomes. Potential implications for their function and multivesicular body formation. J. Biol. Chem. 278, 10963-10972
38. Clayton, A., Harris, C. L., Court, J., Mason, M. D., and Morgan, B. P. (2003) Antigen-presenting cell exosomes are protected from complement-mediated lysis by expression of CD55 and CD59. Eur. J. Immunol. 33, 522-531
39. Hegmans, J. P., Bard, M. P., Hemmes, A., Luider, T. M., Kleijmeer, M. J., Prins, J. B., Zitvogel, L., Burgers, S. A., Hoogsteden, H. C., and Lambrecht, B. N. (2004) Proteomic analysis of exosomes secreted by human mesothelioma cells. Am. J. Pathol. 164, 1807-1815
40. Kreda, S. M., Mall, M., Mengos, A., Rochelle, L., Yankaskas, J., Riordan, J. R., and Boucher, R. C. (2005) Characterization of wild-type and deltaF508 cystic fibrosis transmembrane regulator in human respiratory epithelia. Mol. Biol. Cell 16, 2154-2167
41. Emans, N., Gorvel, J. P., Walter, C., Gerke, V., Kellner, R., Griffiths, G., and Gruenberg, J. (1993) Annexin II is a major component of fusogenic endosomal vesicles. J. Cell Biol. 120, 1357-1369 (Pubitemid 23081683)
42. Buschow, S. I., Liefhebber, J. M., Wubbolts, R., and Stoorvogel, W. (2005) Exosomes contain ubiquitinated proteins. Blood Cells Mol. Dis. 35, 398-403
43. Hattrup, C. L., and Gendler, S. J. (2008) Structure and function of the cell surface (tethered) mucins. Annu. Rev. Physiol. 70, 431-457
44. Braga, V. M., Pemberton, L. F., Duhig, T., and Gendler, S. J. (1992) Spatial and temporal expression of an epithelial mucin, Muc-1, during mouse development. Development 115, 427-437
45. Reid, C. J., Gould, S., and Harris, A. (1997) Developmental expression of mucin genes in the human respiratory tract. Am. J. Respir. Cell Mol. Biol. 17, 592-598
46. Agrawal, B., and Longenecker, B. M. (2005) MUC1 mucin-mediated regulation of human T cells. Int. Immunol. 17, 391-399
47. Ueno, K., Koga, T., Kato, K., Golenbock, D. T., Gendler, S. J., Kai, H., and Kim, K. C. (2008) MUC1 mucin is a negative regulator of toll-like receptor signaling. Am. J. Respir. Cell Mol. Biol. 38, 263-268
48. Li, X. B., Zhang, Z. R., Schluesener, H. J., and Xu, S. Q. (2006) Role of exosomes in immune regulation. J. Cell. Mol. Med. 10, 364-375
49. Cho, J. A., Yeo, D. J., Son, H. Y., Kim, H. W., Jung, D. S., Ko, J. K., Koh, J. S., Kim, Y. N., and Kim, C. W. (2005) Exosomes: a new delivery system for tumor antigens in cancer immunotherapy. Int. J. Cancer 114, 613-622
50. Chaturvedi, P., Singh, A. P., and Batra, S. K. (2008) Structure, evolution, and biology of the MUC4 mucin. FASEB J. 22, 966-981
51. Singh, A. P., Chaturvedi, P., and Batra, S. K. (2007) Emerging roles of MUC4 in cancer: a novel target for diagnosis and therapy. Cancer Res. 67, 433-436 (Pubitemid 46192176)
52. Rump, A., Morikawa, Y., Tanaka, M., Minami, S., Umesaki, N., Takeuchi, M., and Miyajima, A. (2004) Binding of ovarian cancer antigen CA125/MUC16 to mesothelin mediates cell adhesion. J. Biol. Chem. 279, 9190-9198
53. Belisle, J. A., Gubbels, J. A., Raphael, C. A., Migneault, M., Rancourt, C., Connor, J. P., and Patankar, M. S. (2007) Peritoneal natural killer cells from epithelial ovarian cancer patients show an altered phenotype and bind to the tumour marker MUC16 (CA125). Immunology 122, 418-429 (Pubitemid 47556479)
54. Takahashi, Y., Yajima, A., Cisar, J. O., and Konishi, K. (2004) Functional analysis of the Streptococcus gordonii DL1 sialic acid-binding adhesin and its essential role in bacterial binding to platelets. Infect. Immun. 72, 3876-3882
55. Ramphal, R., and Pyle, M. (1983) Evidence for mucins and sialic acid as receptors for Pseudomonas aeruginosa in the lower respiratory tract. Infect. Immun. 41, 339-344