Inflammation-induced endothelial cell-derived extracellular vesicles modulate the cellular status of pericytes

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Yamamoto, Seiji ^a   Niida, Shumpei ^b   Azuma, Erika ^a,c   Yanagibashi, Tsutomu ^a,d   Muramatsu, Masashi ^b,e   Huang, Ting Ting ^a   Sagara, Hiroshi ^f   Higaki, Sayuri ^b   Ikutani, Masashi ^a   Nagai, Yoshinori ^a   Takatsu, Kiyoshi ^a,d   Miyazaki, Kenji ^g   Hamashima, Takeru ^a   Mori, Hisashi ^a   Matsuda, Naoyuki ^h   Ishii, Yoko ^a   Sasahara, Masakiyo ^a  

^a UNIVERSITY OF TOYAMA   (Japan)

^b NATIONAL CENTER FOR GERIATRICS AND GERONTOLOGY   (Japan)

^c ASTELLAS PHARMA INC   (Japan)

^d Toyama Prefectural Institute for Pharmaceutical Research   (Japan)

^e ROSWELL PARK CANCER INSTITUTE   (United States)

^f UNIVERSITY OF TOKYO   (Japan)

^g JICHI MEDICAL UNIVERSITY   (Japan)

^h NAGOYA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; MICRORNA;

ANIMAL; CELL COMMUNICATION; ENDOTHELIUM CELL; EXOSOME; GENE EXPRESSION PROFILING; GENETICS; INFLAMMATION; METABOLISM; MOUSE; PERICYTE;

ANIMALS; CELL COMMUNICATION; ENDOTHELIAL CELLS; EXTRACELLULAR VESICLES; GENE EXPRESSION PROFILING; INFLAMMATION; MICE; MICRORNAS; PERICYTES; RNA, MESSENGER;

EID: 84923368860     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep08505     Document Type: Article

References (64)

1. Raposo, G. & Stoorvogel, W. Extracellular vesicles: exosomes, microvesicles, and friends. J Cell Biol 200, 373-383 (2013).
2. Gould, S. J. & Raposo, G. As we wait: coping with an imperfect nomenclature for extracellular vesicles. J Extracell Vesicles 2, 20389 (2013).
3. Kosaka, N., Iguchi, H. & Ochiya, T. Circulating microRNA in body fluid: a new potential biomarker for cancer diagnosis and prognosis. Cancer Sci 101, 2087-2092 (2010).
4. Beyer, C. & Pisetsky, D. S. The role of microparticles in the pathogenesis of rheumatic diseases. Nat Rev Rheumatol 6, 21-29 (2010).
5. Antonyak, M. A. et al. Cancer cell-derived microvesicles induce transformation by transferring tissue transglutaminase and fibronectin to recipient cells. Proc Natl Acad Sci U S A 108, 4852-4857 (2011).
6. Ratajczak, J., Wysoczynski, M., Hayek, F., Janowska-Wieczorek, A. & Ratajczak, M. Z. Membrane-derived microvesicles: important and underappreciated mediators of cell-to-cell communication. Leukemia 20, 1487-1495 (2006).
7. Kawamoto, T. et al. Tumor-derived microvesicles induce proangiogenic phenotype in endothelial cells via endocytosis. PLoS One 7, e34045 (2012).
8. Thery, C. Exosomes: secreted vesicles and intercellular communications. F1000 Biol Rep 3, 15 (2011).
9. Mostefai, H. A. et al. Circulating microparticles from patients with septic shock exert protective role in vascular function. Am J Respir Crit Care Med 178, 1148-1155 (2008).
10. Simak, J., Gelderman, M. P., Yu, H., Wright, V. & Baird, A. E. Circulating endothelial microparticles in acute ischemic stroke: a link to severity, lesion volume and outcome. J Thromb Haemost 4, 1296-1302 (2006).
11. Petrozella, L. et al. Endothelial microparticles and the antiangiogenic state in preeclampsia and the postpartum period. Am J Obstet Gynecol 207, 140 e120-146 (2012).
12. Boulanger, C. M., Amabile, N. & Tedgui, A. Circulating microparticles: a potential prognostic marker for atherosclerotic vascular disease. Hypertension 48, 180-186 (2006).
13. Koga, H. et al. Elevated levels of VE-cadherin-positive endothelial microparticles in patients with type 2 diabetes mellitus and coronary artery disease. J Am Coll Cardiol 45, 1622-1630 (2005).
14. Agouni, A. et al. Endothelial dysfunction caused by circulating microparticles from patients with metabolic syndrome. Am J Pathol 173, 1210-1219 (2008).
15. Martinez, M. C., Tesse, A., Zobairi, F. & Andriantsitohaina, R. Shed membrane microparticles from circulating and vascular cells in regulating vascular function. Am J Physiol Heart Circ Physiol 288, H1004-1009 (2005).
16. Bartel, D. P. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116, 281-297 (2004).
17. Bartel, D. P. MicroRNAs: target recognition and regulatory functions. Cell 136, 215-233 (2009).
18. Montgomery, R. L. & van Rooij, E. MicroRNA regulation as a therapeutic strategy for cardiovascular disease. Curr Drug Targets 11, 936-942 (2010).
19. Small, E. M. & Olson, E. N. Pervasive roles of microRNAs in cardiovascular biology. Nature 469, 336-342 (2011).
20. Hassan, F. et al. MiR-101 and miR-144 regulate the expression of the CFTR chloride channel in the lung. PLoS One 7, e50837 (2012).
21. Lee, K. S. et al. Functional role of NF-kappaB in expression of human endothelial nitric oxide synthase. Biochem Biophys Res Commun 448, 101-107 (2014).
22. Armulik, A., Genove, G. & Betsholtz, C. Pericytes: developmental, physiological, and pathological perspectives, problems, and promises. Dev Cell 21, 193-215 (2011).
23. Armulik, A. et al. Pericytes regulate the blood-brain barrier. Nature 468, 557-561 (2010).
24. Daneman, R., Zhou, L., Kebede, A. A. & Barres, B. A. Pericytes are required for blood-brain barrier integrity during embryogenesis. Nature 468, 562-566 (2010).
25. Bell, R. D. et al. Pericytes control key neurovascular functions and neuronal phenotype in the adult brain and during brain aging. Neuron 68, 409-427 (2010).
26. Winkler, E. A., Bell, R. D. & Zlokovic, B. V. Central nervous system pericytes in health and disease. Nat Neurosci 14, 1398-1405 (2011).
27. Rincon, M. Interleukin-6: from an inflammatory marker to a target for inflammatory diseases. Trends Immunol 33, 571-577 (2012).
28. Hua, S. Targeting sites of inflammation: intercellular adhesion molecule-1 as a target for novel inflammatory therapies. Front Pharmacol 4, 127 (2013).
29. Sprague, A. H. & Khalil, R. A. Inflammatory cytokines in vascular dysfunction and vascular disease. Biochem Pharmacol 78, 539-552 (2009).
30. Bannerman, D. D. & Goldblum, S. E. Mechanisms of bacterial lipopolysaccharide induced endothelial apoptosis. Am J Physiol Lung Cell Mol Physiol 284, L899-914 (2003).
31. Dignat-George, F. & Boulanger, C. M. The many faces of endothelial microparticles. Arterioscler Thromb Vasc Biol 31, 27-33 (2011).
32. Shai, E. & Varon, D. Development, cell differentiation, angiogenesis-microparticles and their roles in angiogenesis. Arterioscler Thromb Vasc Biol 31, 10-14 (2011).
33. Fujita, Y., Kuwano, K., Ochiya, T. & Takeshita, F. The impact of extracellular vesicle-encapsulated circulating microRNAs in lung cancer research. Biomed Res Int 2014, 486413 (2014).
34. Albanese, J. & Dainiak, N. Modulation of intercellular communication mediated at the cell surface and on extracellular, plasma membrane-derived vesicles by ionizing radiation. Exp Hematol 31, 455-464 (2003).
35. Delabranche, X., Berger, A., Boisrame-Helms, J. & Meziani, F. Microparticles and infectious diseases. Med Mal Infect 42, 335-343 (2012).
36. Armulik, A., Abramsson, A. & Betsholtz, C. Endothelial/pericyte interactions. Circ Res 97, 512-523 (2005).
37. Darland, D. C. et al. Pericyte production of cell-associated VEGF is differentiation-dependent and is associated with endothelial survival. Dev Biol 264, 275-288 (2003).
38. Yonekura, H. et al. Placenta growth factor and vascular endothelial growth factor B and C expression in microvascular endothelial cells and pericytes. Implication in autocrine and paracrine regulation of angiogenesis. J Biol Chem 274, 35172-35178 (1999).
39. de Nigris, F. et al. CXCR4/YY1 inhibition impairs VEGF network and angiogenesis during malignancy. Proc Natl Acad Sci U S A 107, 14484-14489 (2010).
40. Barteneva, N. S., Maltsev, N. & Vorobjev, I. A. Microvesicles and intercellular communication in the context of parasitism. Front Cell Infect Microbiol 3, 49 (2013).
41. Sahoo, S. & Losordo, D. W. Exosomes and cardiac repair after myocardial infarction. Circ Res 114, 333-344 (2014).
42. 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).
43. Skog, J. et al. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol 10, 1470-1476 (2008).
44. Iglesias, D. M. et al. Stem cell microvesicles transfer cystinosin to human cystinotic cells and reduce cystine accumulation in vitro. PLoS One 7, e42840 (2012).
45. Curtis, A. M. et al. p38 mitogen-activated protein kinase targets the production of proinflammatory endothelial microparticles. J Thromb Haemost 7, 701-709 (2009).
46. Chen, T., Guo, J., Yang, M., Zhu, X. & Cao, X. Chemokine-containing exosomes are released from heat-stressed tumor cells via lipid raft-dependent pathway and act as efficient tumor vaccine. J Immunol 186, 2219-2228 (2011).
47. Tetta, C., Bruno, S., Fonsato, V., Deregibus, M. C. & Camussi, G. The role of microvesicles in tissue repair. Organogenesis 7, 105-115 (2011).
48. Ratajczak, J. et al. Embryonic stem cell-derived microvesicles reprogram hematopoietic progenitors: evidence for horizontal transfer of mRNAand protein delivery. Leukemia 20, 847-856 (2006).
49. Thery, C., Amigorena, S., Raposo, G. & Clayton, A. Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr Protoc Cell Biol Chapter 3, Unit 3 22 (2006).
50. Ronquist, G. K., Larsson, A., Stavreus-Evers, A. & Ronquist, G. Prostasomes are heterogeneous regarding size and appearance but affiliated to one DNAcontaining exosome family. Prostate 72, 1736-1745 (2012).
51. Guescini, M., Genedani, S., Stocchi, V. & Agnati, L. F. Astrocytes and Glioblastoma cells release exosomes carrying mtDNA. J Neural Transm 117, 1-4 (2010).
52. Balaj, L. et al. Tumour microvesicles contain retrotransposon elements and amplified oncogene sequences. Nat Commun 2, 180 (2011).
53. Rak, J. & Guha, A. Extracellular vesicles-vehicles that spread cancer genes. Bioessays 34, 489-497 (2012).
54. Waldenstrom, A., Genneback, N., Hellman, U. & Ronquist, G. Cardiomyocyte microvesicles contain DNA/RNA and convey biological messages to target cells. PLoS One 7, e34653 (2012).
55. Peinado, H. et al. Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET. Nat Med 18, 883-891 (2012).
56. Al-Nedawi, K., Meehan, B., Kerbel, R. S., Allison, A. C. & Rak, J. Endothelial expression of autocrine VEGF upon the uptake of tumor-derived microvesicles containing oncogenic EGFR. Proc Natl Acad Sci U S A 106, 3794-3799 (2009).
57. Aliotta, J. M. et al. Microvesicle entry into marrow cells mediates tissue-specific changes in mRNAby direct delivery of mRNAand induction of transcription. Exp Hematol 38, 233-245 (2010).
58. Takahashi, H. & Shibuya, M. The vascular endothelial growth factor (VEGF)/VEGF receptor system and its role under physiological and pathological conditions. Clin Sci (Lond) 109, 227-241 (2005).
59. Cao, Y. Positive and negativemodulation of angiogenesis by VEGFR1 ligands. Sci Signal 2, re1 (2009).
60. Zhang, F. et al. VEGF-B is dispensable for blood vessel growth but critical for their survival, and VEGF-B targeting inhibits pathological angiogenesis. Proc Natl Acad Sci U S A 106, 6152-6157 (2009).
61. Boscolo, E., Mulliken, J. B. & Bischoff, J. VEGFR-1 mediates endothelial differentiation and formation of blood vessels in a murine model of infantile hemangioma. Am J Pathol 179, 2266-2277 (2011).
62. Muramatsu, M., Yamamoto, S., Osawa, T. & Shibuya, M. Vascular endothelial growth factor receptor-1 signaling promotes mobilization of macrophage lineage cells from bone marrow and stimulates solid tumor growth. Cancer Res 70, 8211-8221 (2010).
63. Cao, R. et al. VEGFR1-mediated pericyte ablation links VEGF and PlGF to cancerassociated retinopathy. Proc Natl Acad Sci U S A 107, 856-861 (2010).
64. Yamamoto, S. et al. Essential role of Shp2-binding sites on FRS2alpha for corticogenesis and for FGF2-dependent proliferation of neural progenitor cells. Proc Natl Acad Sci U S A 102, 15983-15988 (2005).