Exosomes as nanocarriers for systemic delivery of the Helicobacter pylori virulence factor CagA

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Shimoda, Asako ^a,b   Ueda, Koji ^c   Nishiumi, Shin ^d   Murata Kamiya, Naoko ^e   Mukai, Sada Atsu ^a,b   Sawada, Shin Ichi ^a,b   Azuma, Takeshi ^d   Hatakeyama, Masanori ^e   Akiyoshi, Kazunari ^a,b  

^a KYOTO UNIVERSITY   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c UNIVERSITY OF TOKYO   (Japan)

^d KOBE UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^e UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ANTIGEN; BACTERIAL PROTEIN; BIOLOGICAL MARKER; CAGA PROTEIN, HELICOBACTER PYLORI; VIRULENCE FACTOR;

CELL LINE; COMPLICATION; EXOSOME; GENETICS; HELICOBACTER INFECTION; HELICOBACTER PYLORI; HUMAN; LIQUID CHROMATOGRAPHY; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; PROTEIN TRANSPORT; STOMACH NEOPLASMS; TANDEM MASS SPECTROMETRY; TRANSPORT AT THE CELLULAR LEVEL;

ANTIGENS, BACTERIAL; BACTERIAL PROTEINS; BIOLOGICAL TRANSPORT; BIOMARKERS; CELL LINE; CHROMATOGRAPHY, LIQUID; EXOSOMES; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; HUMANS; PROTEIN TRANSPORT; STOMACH NEOPLASMS; TANDEM MASS SPECTROMETRY; VIRULENCE FACTORS;

EID: 84954517903     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep18346     Document Type: Article

References (60)

1. Polk, D. B., Peek, R. M. Jr. Helicobacter pylori: gastric cancer and beyond. Nat. Rev. Cancer. 10, 403-414 (2010).
2. Bornschein, J., Malfertheiner, P. Helicobacter pylori and gastric cancer. Dig. Dis. 32, 249-264 (2014).
3. Conteduca, V. et al. H. pylori infection and gastric cancer: state of the art (review). Int. J. Oncol. 42, 5-18 (2013).
4. Hatakeyama, M. Helicobacter pylori CagA and gastric cancer: a paradigm for hit-and-run carcinogenesis. Cell Host Microbe. 15, 306-316 (2014).
5. Azuma, T. Helicobacter pylori CagA protein variation associated with gastric cancer in Asia. J. Gastroenterol. 39, 97-103 (2004).
6. Alfizah, H., Ramelah, M. Variant of Helicobacter pylori CagA proteins induce different magnitude of morphological changes in gastric epithelial cells. Malays. J. Pathol. 34, 29-34 (2012).
7. Higashi, H. et al. Helicobacter pylori CagA induces Ras-independent morphogenetic response through SHP-2 recruitment and activation. J. Biol. Chem. 279, 17205-17216 (2004).
8. Murata-Kamiya, N. et al. Helicobacter pylori CagA interacts with E-cadherin and deregulates the beta-catenin signal that promotes intestinal transdifferentiation in gastric epithelial cells. Oncogene. 26, 4617-4626 (2007).
9. Saito, Y., Murata-Kamiya, N., Hirayama, T., Ohba, Y., Hatakeyama, M. Conversion of Helicobacter pylori CagA from senescence inducer to oncogenic driver through polarity-dependent regulation of p21. J. Exp. Med. 207, 2157-2174 (2010).
10. Murata-Kamiya, N., Kikuchi, K., Hayashi, T., Higashi, H., Hatakeyama, M. Helicobacter pylori exploits host membrane phosphatidylserine for delivery, localization, and pathophysiological action of the CagA oncoprotein. Cell Host Microbe. 7, 399-411 (2010).
11. Nagase, L., Murata-Kamiya, N., Hatakeyama, M. Potentiation of Helicobacter pylori CagA protein virulence through homodimerization. J. Biol. Chem. 286, 33622-33631 (2011).
12. Lee, K. S. et al. Helicobacter pylori CagA triggers expression of the bactericidal lectin REG3 via gastric STAT3 activation. PLoS One. 7, e30786 (2012).
13. Ohnishi, N. et al. Transgenic expression of Helicobacter pylori CagA induces gastrointestinal and hematopoietic neoplasms in mouse. Proc. Natl. Acad. Sci. USA 105, 1003-1008 (2008).
14. Izzotti, A., Durando, P., Ansaldi, F., Gianiorio, F., Pulliero, A. Interaction between Helicobacter pylori, diet, and genetic polymorphisms as related to non-cancer diseases. Mutat. Res. 667, 142-157 (2009).
15. Francesco, F. Helicobacter pylori and extragastric diseases. Best Pract. Res. Clin. Gastroenterol. 21, 325-334 (2007).
16. Gasbarrini, A. et al. Regression of autoimmune thrombocytopenia after eradication of Helicobacter pylori. Lancet. 352, 878 (1998).
17. Takahashi, T. et al. Molecular mimicry by Helicobacter pylori CagA protein may be involved in the pathogenesis of H. pylori-associated chronic idiopathic thrombocytopenic purpura. Br. J. Maematol. 124, 91-96 (2004).
18. Weller, C. et al. Role or inflammation in gastrointestinal tract in aetiology and pathogenesis of idiopathic parkinsonism. FEMS Immunol. Med. Microbiol. 44, 129-135 (2005).
19. Ameriso, A. F., Fridman, E. A., Leiguarda, R. C., Sevlever, G. E. Detection of Helicobacter pylori in human carotid atherosclerotic plaques. Stroke. 32, 385-391 (2001).
20. Izadi, M. et al. Helicobacter species in the atherosclerotic plaques of patients with coronary artery disease. Cardiovasc. Pathol. 21, 307-311 (2012).
21. Pasceri, V. et al. Association of virulent Helicobacter pylori strains with ischemic heart disease. Circulation. 97, 1675-1679 (1998).
22. Pasceri, V. et al. Virulent strains of Helicobacter pylori and vascular diseases: a meta-analysis. Am. Heart J. 151, 1215-1222 (2006).
23. Franceschi, F. et al. CagA antigen of Helicobacter pylori and coronary instability: insight from a clinico-pathological study and a meta-analysis of 4241 cases. Atherosclerosis. 202, 535-542 (2009).
24. Wang, Z. W. et al. Helicobacter pylori infection contributes to high risk of ischemic stroke: evidence from a meta-analysis. J. Neurol. 259, 2527-2537 (2012).
25. De Bastiani, R. et al. High prevalence of Cag-A positive H. pylori strains in ischemic stroke: a primary care multicenter study. Helicobacter. 13, 274-277 (2008).
26. Cremonini, F., Gabrielli, M., Gasbarrini, G., Pola, P., Gasbarrini, A. The relationship between chronic H. pylori infection, CagA seropositivity and stroke: meta-analysis. Atherosclerosis. 173, 253-259 (2004).
27. Ponzetto, A. et al. Pre-eclampsia is associated with Helicobacter pylori seropositivity in Italy. J. Hypertens. 24, 2445-2449 (2006).
28. Tersigni, C. et al. Insights into the role of Helicobacter pylori infection in preeclampsia: from the bench to the bedside. Front. Immunol. 5, 484 (2014).
29. Tickner, J. A., Urquhart, A. J., Stephenson, S. A., Richard, D. J., O'Byrne, K. J. Functions and therapeutic roles of exosomes in cancer. Front. Oncol. 4, 127 (2014).
30. Thy, C., Zitvogel, L., Amigorena, S. Exosomes: composition, biogenesis and function. Nat. Rev. Immunol. 2, 569-579 (2002).
31. Borges, F. T., Reis, L. A., Schor, N. Extracellular vesicles: structure, function, and potential clinical uses in renal diseases. N. Braz. J. Med. Biol. Res. 46, 824-830 (2013).
32. Azmi, A. S., Bao, B., Sarkar, F. H. Exosomes in cancer development, metastasis, and drug resistance: a comprehensive review. Cancer Metastasis Rev. 32, 623-642 (2013).
33. Valadi, H. et al. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat. Cell Biol. 9, 654-659 (2007).
34. Mittelbrunn, M. et al. Unidirectional transfer of microRNA-loaded exosomes from T cells to antigen-presenting cells. Nat. Commun. 2, 282 (2011).
35. Wang, W. T., Chen, Y. Q. Circulating miRNAs in cancer: from detection to therapy. J. Hematol. Oncol. 7, 86 (2014).
36. Bellingham, S. A., Guo, B. B., Coleman, B. M., Hill, A. F., Panaretakis, T. Exosomes: vehicles for the transfer of toxic proteins associated with neurodegenerative diseases Front. Physiol. 3, 124 (2012).
37. Campbell, T. D., Khan, M., Huang, M. B., Bond, V. C., Powell, M. D. HIV-1 Nef protein is secreted into vesicles that can fuse with target cells and virions. Ethn. Dis. 18, S214-9 (2008).
38. Jaworski, E. et al. Human T-lymphotropic virus type 1-infected cells secrete exosomes that contain Tax protein. J. Biol. Chem. 289, 22284-22305 (2014).
39. Simons, M., Raposo, G. Exosomes-vesicular carriers for intercellular communication. Curr. Opin. Cell Biol. 21, 575-581 (2009).
40. Khatua, A. K., Taylor, H. E., Hildreth, J. E., Popik, W. Exosomes packaging APOBEC3G confer human immunodeficiency virus resistance to recipient cells. J. Virol. 83, 512-521 (2009).
41. Klibi, J. et al. Blood diffusion and Th1-suppressive effects of galectin-9-containing exosomes released by Epstein-Barr virus-infected nasopharyngeal carcinoma cells. Blood. 113, 1957-1966 (2009).
42. Ishikawa, S., Ohta, T., Hatakeyama, M. Stability of Helicobacter pylori CagA oncoprotein in human gastric epithelial cells. FEBS Lett. 583, 2414-2418 (2009).
43. Manolakis, A., Kapsoritakis, A. N., Potamianos, S. P. A review of the postulated mechanisms concerning the association of Helicobacter pylori with ischemic heart disease. Helicobacter. 12, 287-297 (2007).
44. Franceschi, F. et al. Cross-reactivity of anti-CagA antibodies with vascular wall antigens: possible pathogenic link between Helicobacter pylori infection and atherosclerosis. Circulation. 106, 430-434 (2002).
45. Rožankovi, P. B. et al. Influence of CagA-positive Helicobacter pylori strains on atherosclerotic carotid disease. J. Neurol. 258, 753-761 (2011).
46. Mehmet, N. et al. Serum and gastric fluid levels of cytokines and nitrates in gastric diseases infected with Helicobacter pylori. New Microbiol. 27, 139-148 (2004).
47. Franzini, M., Corti, A., Fierabracci, V., Pompella, A. Helicobacter, gamma-glutamyltransferase and cancer: further intriguing connections. World J. Gastroenterol. 20, 18057-18058 (2014).
48. Zhang, G. et al. Effects of Helicobacter suis-glutamyl transpeptidase on lymphocytes: modulation by glutamine and glutathione supplementation and outer membrane vesicles as a putative delivery route of the enzyme. PLoS One. 8, e77966 (2013).
49. Fiocca, R. et al. Release of Helicobacter pylori vacuolating cytotoxin by both a specific secretion pathway and budding of outer membrane vesicles. Uptake of released toxin and vesicles by gastric epithelium. J. Pathol. 188, 220-226 (1999).
50. Schwechheimer, C., Kuehn, M. J. Outer-membrane vesicles from Gram-negative bacteria: biogenesis and functions. Nat Rev Microbiol. 13, 605-619 (2015).
51. Silverman, J. M., Reiner, N. E. Exosomes and other microvesicles in infection biology: organelles with unanticipated phenotypes. Cell Microbiol. 13, 1-9 (2011).
52. Mulcahy, L. A., Pink, R. C., Carter, D. R. Routes and mechanisms of extracellular vesicle uptake. J. Extracell. Vesicles. 3, 24641 (2014).
53. Backert, S., Naumann, M. What a disorder: proinflammatory signaling pathways induced by Helicobacter pylori. Trends Microbiol. 18, 479-486 (2010).
54. Suzuki, N. et al. Mutual reinforcement of inflammation and carcinogenesis by the Helicobacter pylori CagA oncoprotein. Sci. Rep. 5, 10024 (2015).
55. Pateras, I., Giaginis, C., Tsigris, C., Patsouris, E., Theocharis, S. NF-B signaling at the crossroads of inflammation and atherogenesis: searching for new therapeutic links. Expert Opin. Ther. Targets. 18, 1089-1101 (2014).
56. Franceschi, F., Christodoulides, N., Kroll, M. H., Genta, R. M. Helicobacter pylori and idiopathic thrombocytopenic purpura. Ann. Intern. Med. 140, 766-767 (2004).
57. Hatakeyama, M. Helicobacter pylori CagA and gastric cancer: a paradigm for hit-and-run carcinogenesis. Cell Host Microbe. 15, 306-316 (2014).
58. Strofilas, A. et al. Association of Helicobacter pylori infection and colon cancer. J. Clin. Med. Res. 4, 172-176 (2012).
59. Risch, H. A. et al. Helicobacter pylori seropositivities and risk of pancreatic carcinoma. Cancer Epidemiol. Biomarkers Prev. 23, 172-178 (2014).
60. Thy, C., Amigorena, S., Raposo, G., Clayton, A. Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr. Protoc. Cell Biol. Apr; Chapter 3:Unit 3.22. (2006).