Exosomes and the kidney: Blaming the messenger

Nephrology

Volumn 18, Issue 1, 2013, Pages 1-10

  Fang, Doreen Y P ^a   King, Hamish W ^a   Li, Jordan Y Z ^a   Gleadle, Jonathan M ^a  

^a FLINDERS UNIVERSITY   (Australia)

Author keywords

biomarker; exosome; kidney disease; microRNA; microvesicle

Indexed keywords

ALPHA SYNUCLEIN; AQUAPORIN 2; CD63 ANTIGEN; CD81 ANTIGEN; CD82 ANTIGEN; CD9 ANTIGEN; CELL ADHESION MOLECULE; CYTOSKELETON PROTEIN; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 90; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MESSENGER RNA; MICRORNA; PROSTAGLANDIN; RNA; TRANSFERRIN;

BIOGENESIS; BLOOD SAMPLING; BODY FLUID; CANCER GROWTH; CANCER IMMUNOTHERAPY; CELL COMMUNICATION; CELL DIFFERENTIATION; CELL MATURATION; CELL STRESS; CYTOSKELETON; EXOSOME; GROWTH; HUMAN; IMMUNE SYSTEM; IMMUNOCOMPETENT CELL; IMMUNOMODULATION; IN VIVO STUDY; KIDNEY CANCER; KIDNEY CELL; KIDNEY DISEASE; LIPID RAFT; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN SECRETION; REGULATORY T LYMPHOCYTE; RETICULOCYTE; REVIEW; SIGNAL TRANSDUCTION; ULTRACENTRIFUGATION; URINALYSIS;

EXOSOMES; HUMANS; KIDNEY; KIDNEY DISEASES;

EID: 84872849084     PISSN: 13205358     EISSN: 14401797     Source Type: Journal    
DOI: 10.1111/nep.12005     Document Type: Review

References (106)

1. Heijnen HF, Schiel AE, Fijnheer R, Geuze HJ, Sixma JJ,. Activated platelets release two types of membrane vesicles: Microvesicles by surface shedding and exosomes derived from exocytosis of multivesicular bodies and alpha-granules. Blood 1999; 94: 3791-3799.
2. Gyorgy B, Szabo TG, Pasztoi M, et al. Membrane vesicles, current state-of-the-art: Emerging role of extracellular vesicles. Cell. Mol. Life Sci. 2011; 68: 2667-2688.
3. Lee TH, D'Asti E, Magnus N, Al-Nedawi K, Meehan B, Rak J,. Microvesicles as mediators of intercellular communication in cancer-The emerging science of cellular 'debris'. Semin. Immunopathol. 2011; 33: 455-467.
4. Mause SF, Weber C,. Microparticles: Protagonists of a novel communication network for intercellular information exchange. Circ. Res. 2010; 107: 1047-1057.
5. VanWijk MJ, VanBavel E, Sturk A, Nieuwland R,. Microparticles in cardiovascular diseases. Cardiovasc. Res. 2003; 59: 277-287.
6. Mathivanan S, Ji H, Simpson RJ,. Exosomes: Extracellular organelles important in intercellular communication. J. Proteomics 2010; 73: 1907-1920.
7. Subra C, Grand D, Laulagnier K, et al. Exosomes account for vesicle-mediated transcellular transport of activatable phospholipases and prostaglandins. J. Lipid Res. 2010; 51: 2105-2120.
8. 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.
9. Pigati L, Yaddanapudi SCS, Iyengar R, et al. Selective release of MicroRNA species from normal and malignant mammary epithelial cells. PLoS ONE 2010; 5: e13515.
10. Skog J, Würdinger T, van, Rijn S, et al. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat. Cell Biol. 2008; 10: 1470-1476.
11. Arroyo JD, Chevillet JR, Kroh EM, et al. Argonaute2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma. Proc. Natl Acad. Sci. U.S.A. 2011; 108: 5003-5008.
12. Turchinovich A, Weiz L, Langheinz A, Burwinkel B,. Characterization of extracellular circulating microRNA. Nucleic Acids Res. 2011; 39: 7223-7233.
13. Wang K, Zhang S, Weber J, Baxter D, Galas DJ,. Export of microRNAs and microRNA-protective protein by mammalian cells. Nucleic Acids Res. 2010; 38: 7248-7259.
14. Pan BT, Blostein R, Johnstone RM,. Loss of the transferrin receptor during the maturation of sheep reticulocytes in vitro. An immunological approach. Biochem. J. 1983; 210: 37-47.
15. Théry C, Duban L, Segura E, Veron P, Lantz O, Amigorena S,. Indirect activation of naive CD4+ T cells by dendritic cell-derived exosomes. Nat. Immunol. 2002; 3: 1156-1162.
16. Xiang X, Poliakov A, Liu C, et al. Induction of myeloid-derived suppressor cells by tumor exosomes. Int. J. Cancer 2009; 124: 2621-2633.
17. Tamai K, Tanaka N, Nakano T, et al. Exosome secretion of dendritic cells is regulated by Hrs, an ESCRT-0 protein. Biochem. Biophys. Res. Commun. 2010; 399: 384-390.
18. Savina A, Fader CM, Damiani MT, Colombo MI,. Rab11 promotes docking and fusion of multivesicular bodies in a calcium-dependent manner. Traffic 2005; 6: 131-143.
19. Ostrowski M, Carmo NB, Krumeich S, et al. Rab27a and Rab27b control different steps of the exosome secretion pathway. Nat. Cell Biol. 2010; 12: 19-30.
20. Trajkovic K, Hsu C, Chiantia S, et al. Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science 2008; 319: 1244-1247.
21. King HW, Michael MZ, Gleadle JM,. Hypoxic enhancement of exosome release by breast cancer cells. BMC Cancer 2012; 12: 421.
22. Parolini I, Federici C, Raggi C, et al. Microenvironmental pH is a key factor for exosome traffic in tumor cells. J. Biol. Chem. 2009; 284: 34211-34222.
23. Clayton A, Turkes A, Navabi H, Mason MD, Tabi Z,. Induction of heat shock proteins in B-cell exosomes. J. Cell Sci. 2005; 118: 3631-3638.
24. Hedlund M, Nagaeva O, Kargl D, Baranov V, Mincheva-Nilsson L,. Thermal- and oxidative stress causes enhanced release of NKG2D ligand-bearing immunosuppressive exosomes in leukemia/lymphoma T and B cells. PLoS ONE 2011; 6: e16899.
25. Hao S, Bai O, Yuan J, Qureshi M, Xiang J,. Dendritic cell-derived exosomes stimulate stronger CD8+ CTL responses and antitumor immunity than tumor cell-derived exosomes. Cell. Mol. Immunol. 2006; 3: 205-211.
26. Théry C, Amigorena S, Raposo G, Clayton A,. Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr. Protoc. Cell Biol. 2006; 30: 3.22.1-3.22.29.
27. Rani S, O'Brien K, Kelleher FC, et al. Isolation of exosomes for subsequent mRNA, MicroRNA, and protein profiling. Methods Mol. Biol. 2011; 784: 181-195.
28. Clayton A, Court J, Navabi H, et al. Analysis of antigen presenting cell derived exosomes, based on immuno-magnetic isolation and flow cytometry. J. Immunol. Methods 2001; 247: 163-174.
29. Grant R, Ansa-Addo E, Stratton D, et al. A filtration-based protocol to isolate human Plasma Membrane-derived Vesicles and exosomes from blood plasma. J. Immunol. Methods 2011; 371: 143-151.
30. Chen C, Skog J, Hsu C-H, et al. Microfluidic isolation and transcriptome analysis of serum microvesicles. Lab Chip 2010; 10: 505-511.
31. Taylor DD, Zacharias W, Gercel-Taylor C,. Exosome isolation for proteomic analyses and RNA profiling. Methods Mol. Biol. 2011; 728: 235-246.
32. Théry C, Boussac M, Véron P, et al. Proteomic analysis of dendritic cell-derived exosomes: A secreted subcellular compartment distinct from apoptotic vesicles. J. Immunol. 2001; 166: 7309-7318.
33. Cantin R, Diou J, Bélanger D, Tremblay AM, Gilbert C,. Discrimination between exosomes and HIV-1: Purification of both vesicles from cell-free supernatants. J. Immunol. Methods 2008; 338: 21-30.
34. Lenassi M, Cagney G, Liao M, et al. HIV Nef is secreted in exosomes and triggers apoptosis in bystander CD4+ T cells. Traffic 2010; 11: 110-122.
35. Alvarez ML, Khosroheidari M, Kanchi Ravi R, Distefano JK,. Comparison of protein, microRNA, and mRNA yields using different methods of urinary exosome isolation for the discovery of kidney disease biomarkers. Kidney Int. 2012; 82: 1024-1032.
36. Mathivanan S, Fahner CJ, Reid GE, Simpson RJ,. ExoCarta 2012: Database of exosomal proteins, RNA and lipids. Nucleic Acids Res. 2011; 40: D1241-1244.
37. Savina A, Furlán M, Vidal M, Colombo MI,. Exosome release is regulated by a calcium-dependent mechanism in K562 cells. J. Biol. Chem. 2003; 278: 20083-20090.
38. Lancaster GI, Febbraio MA,. Exosome-dependent trafficking of HSP70. J. Biol. Chem. 2005; 280: 23349-23355.
39. Hood JL, Pan H, Lanza GM, Wickline SA,. Paracrine induction of endothelium by tumor exosomes. Lab. Invest. 2009; 89: 1317-1328.
40. Koumangoye RB, Sakwe AM, Goodwin JS, Patel T, Ochieng J,. Detachment of breast tumor cells induces rapid secretion of exosomes which subsequently mediate cellular adhesion and spreading. PLoS ONE 2011; 6: e24234.
41. Dragovic RA, Gardiner C, Brooks AS, et al. Sizing and phenotyping of cellular vesicles using Nanoparticle Tracking Analysis. Nanomedicine 2011; 7: 780-788.
42. Sokolova V, Ludwig A-K, Hornung S, et al. Characterisation of exosomes derived from human cells by nanoparticle tracking analysis and scanning electron microscopy. Colloids Surf. B. Biointerfaces 2011; 87: 146-150.
43. Fernandez-Llama P, Khositseth S, Gonzales PA, Star RA, Pisitkun T, Knepper MA,. Tamm-Horsfall protein and urinary exosome isolation. Kidney Int. 2010; 77: 736-742.
44. Zhou H, Yuen PS, Pisitkun T, et al. Collection, storage, preservation, and normalization of human urinary exosomes for biomarker discovery. Kidney Int. 2006; 69: 1471-1476.
45. Rood IM, Deegens JK, Merchant ML, et al. Comparison of three methods for isolation of urinary microvesicles to identify biomarkers of nephrotic syndrome. Kidney Int. 2010; 78: 810-816.
46. Pan BT, Johnstone RM,. Fate of the transferrin receptor during maturation of sheep reticulocytes in vitro: Selective externalization of the receptor. Cell 1983; 33: 967-978.
47. Trams EG, Lauter CJ, Salem N Jr, Heine U,. Exfoliation of membrane ecto-enzymes in the form of micro-vesicles. Biochim. Biophys. Acta 1981; 645: 63-70.
48. Fitzner D, Schnaars M, van, Rossum D, et al. Selective transfer of exosomes from oligodendrocytes to microglia by macropinocytosis. J. Cell Sci. 2011; 124: 447-458.
49. Pegtel DM, Cosmopoulos K, Thorley-Lawson DA, et al. Functional delivery of viral miRNAs via exosomes. Proc. Natl Acad. Sci. U.S.A. 2010; 107: 6328-6333.
50. Harding C, Heuser J, Stahl P,. Receptor-mediated endocytosis of transferrin and recycling of the transferrin receptor in rat reticulocytes. J. Cell Biol. 1983; 97: 329-339.
51. Pan B-T, Teng K, Wu C, Adam M, Johnstone RM,. Electron microscopic evidence for externalisation of the transferrin receptor in vesicular form in sheep reticulocytes. J. Cell Biol. 1985; 101: 942-948.
52. Johnstone RM, Mathew A, Mason AB, Teng K,. Exosome formation during maturation of mammalian and avian reticulocytes: Evidence that exosome release is a major route for externalization of obsolete membrane proteins. J. Cell. Physiol. 1991; 147: 27-36.
53. Chairoungdua A, Smith DL, Pochard P, Hull M, Caplan MJ,. Exosome release of β-catenin: A novel mechanism that antagonizes Wnt signaling. J. Cell Biol. 2010; 190: 1079-1091.
54. Chaput N, Théry C,. Exosomes: Immune properties and potential clinical implementations. Semin. Immunopathol. 2010; 33: 419-440.
55. Iero M, Valenti R, Huber V, et al. Tumour-released exosomes and their implications in cancer immunity. Cell Death Differ. 2007; 15: 80-88.
56. Raposo G, Nijman HW, Stoorvogel W, et al. B lymphocytes secrete antigen-presenting vesicles. J. Exp. Med. 1996; 183: 1161-1172.
57. Walker JD, Maier CL, Pober JS,. Cytomegalovirus-infected human endothelial cells can stimulate allogeneic CD4+ memory T cells by releasing antigenic exosomes. J. Immunol. 2009; 182: 1548-1559.
58. Alonso R, Mazzeo C, Rodriguez MC, et al. Diacylglycerol kinase α regulates the formation and polarisation of mature multivesicular bodies involved in the secretion of Fas ligand-containing exosomes in T lymphocytes. Cell Death Differ. 2011; 18: 1161-1173.
59. 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: 1-13.
60. Izquierdo-Useros N, Naranjo-Gomez M, Archer J, et al. Capture and transfer of HIV-1 particles by mature dendritic cells converges with the exosome-dissemination pathway. Blood 2009; 113: 2732-2741.
61. Fevrier B, Raposo G,. Exosomes: Endosomal-derived vesicles shipping extracellular messages. Curr. Opin. Cell Biol. 2004; 16: 415-421.
62. Keller S, König A-K, Marmé F, et al. Systemic presence and tumor-growth promoting effect of ovarian carcinoma released exosomes. Cancer Lett. 2009; 278: 73-81.
63. Jung T, Castellana D, Klingbeil P, et al. CD44v6 dependence of premetastatic niche preparation by exosomes. Neoplasia 2009; 11: 1093-1105.
64. Hood JL, San RS, Wickline SA,. Exosomes released by melanoma cells prepare sentinel lymph nodes for tumor metastasis. Cancer Res. 2011; 71: 3792-3801.
65. Antonyak MA, Li B, Boroughs LK, et al. Cancer cell-derived microvesicles induce transformation by transferring tissue transglutaminase and fibronectin to recipient cells. Proc. Natl Acad. Sci. U.S.A. 2011; 108: 4852-4857.
66. Cho JA, Park H, Lim EH, Lee KW,. Exosomes from breast cancer cells can convert adipose tissue-derived mesenchymal stem cells into myofibroblast-like cells. Int. J. Oncol. 2011; 40: 130-138.
67. Grange C, Tapparo M, Collino F, et al. Microvesicles released from human renal cancer stem cells stimulate angiogenesis and formation of lung premetastatic niche. Cancer Res. 2011; 71: 5346-5356.
68. Yang C, Kim S-H, Bianco NR, Robbins PD,. Tumor-derived exosomes confer antigen-specific immunosuppression in a murine delayed-type hypersensitivity model. PLoS ONE 2011; 6: e22517.
69. Szajnik M, Czystowska M, Szczepanski MJ, Mandapathil M, Whiteside TL,. Tumor-derived microvesicles induce, expand and up-regulate biological activities of human regulatory T cells (Treg). PLoS ONE 2010; 5: e11469.
70. 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.
71. Simpson RJ, Lim JW, Moritz RL, Mathivanan S,. Exosomes: Proteomic insights and diagnostic potential. Expert Rev. Proteomics 2009; 6: 267-283.
72. Pisitkun T, Shen RF, Knepper MA,. Identification and proteomic profiling of exosomes in human urine. Proc. Natl Acad. Sci. U.S.A. 2004; 101: 13368-13373.
73. Dimov I, Jankovic Velickovic L, Stefanovic V,. Urinary exosomes. ScientificWorldJournal 2009; 9: 1107-1118.
74. Gonzales P, Pisitkun T, Knepper MA,. Urinary exosomes: Is there a future? Nephrol. Dial. Transplant. 2008; 23: 1799-1801.
75. Keller S, Rupp C, Stoeck A, et al. CD24 is a marker of exosomes secreted into urine and amniotic fluid. Kidney Int. 2007; 72: 1095-1102.
76. van Balkom BW, Pisitkun T, Verhaar MC, Knepper MA,. Exosomes and the kidney: Prospects for diagnosis and therapy of renal diseases. Kidney Int. 2011; 80: 1138-1145.
77. Pisitkun T, Johnstone R, Knepper MA,. Discovery of urinary biomarkers. Mol. Cell. Proteomics 2006; 5: 1760-1771.
78. Street JM, Birkhoff W, Menzies RI, Webb DJ, Bailey MA, Dear JW,. Exosomal transmission of functional aquaporin 2 in kidney cortical collecting duct cells. J. Physiol. 2011; 589: 6119-6127.
79. Barry OP, FitzGerald GA,. Mechanisms of cellular activation by platelet microparticles. Thromb. Haemost. 1999; 82: 794-800.
80. Fox JE,. Shedding of adhesion receptors from the surface of activated platelets. Blood Coagul. Fibrinolysis 1994; 5: 291-304.
81. Aatonen M, Gronholm M, Siljander PR,. Platelet-derived microvesicles: Multitalented participants in intercellular communication. Semin. Thromb. Hemost. 2012; 38: 102-113.
82. 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: 3365-3374.
83. Reynolds JL, Joannides AJ, Skepper JN, et al. Human vascular smooth muscle cells undergo vesicle-mediated calcification in response to changes in extracellular calcium and phosphate concentrations: A potential mechanism for accelerated vascular calcification in ESRD. J. Am. Soc. Nephrol. 2004; 15: 2857-2867.
84. Smith ER, Ford ML, Tomlinson LA, Rajkumar C, McMahon LP, Holt SG,. Phosphorylated fetuin-A-containing calciprotein particles are associated with aortic stiffness and a procalcific milieu in patients with pre-dialysis CKD. Nephrol. Dial. Transplant. 2012; 27: 1957-1966.
85. Amabile N, Guerin AP, Leroyer A, et al. Circulating endothelial microparticles are associated with vascular dysfunction in patients with end-stage renal failure. J. Am. Soc. Nephrol. 2005; 16: 3381-3388.
86. 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.
87. Boulanger CM, Amabile N, Guerin AP, et al. In vivo shear stress determines circulating levels of endothelial microparticles in end-stage renal disease. Hypertension 2007; 49: 902-908.
88. Anderson HC, Mulhall D, Garimella R,. Role of extracellular membrane vesicles in the pathogenesis of various diseases, including cancer, renal diseases, atherosclerosis, and arthritis. Lab. Invest. 2010; 90: 1549-1557.
89. Montecalvo A, Shufesky WJ, Stolz DB, et al. Exosomes as a short-range mechanism to spread alloantigen between dendritic cells during T cell allorecognition. J. Immunol. 2008; 180: 3081-3090.
90. Peche H, Heslan M, Usal C, Amigorena S, Cuturi MC,. Presentation of donor major histocompatibility complex antigens by bone marrow dendritic cell-derived exosomes modulates allograft rejection. Transplantation 2003; 76: 1503-1510.
91. Gonzales PA, Pisitkun T, Hoffert JD, et al. Large-scale proteomics and phosphoproteomics of urinary exosomes. J. Am. Soc. Nephrol. 2009; 20: 363-379.
92. Hogan MC, Manganelli L, Woollard JR, et al. Characterization of PKD protein-positive exosome-like vesicles. J. Am. Soc. Nephrol. 2009; 20: 278-288.
93. Zhou H, Cheruvanky A, Hu X, et al. Urinary exosomal transcription factors, a new class of biomarkers for renal disease. Kidney Int. 2008; 74: 613-621.
94. Moon PG, Lee JE, You S, et al. Proteomic analysis of urinary exosomes from patients of early IgA nephropathy and thin basement membrane nephropathy. Proteomics 2011; 11: 2459-2475.
95. Zhou H, Pisitkun T, Aponte A, et al. Exosomal Fetuin-A identified by proteomics: A novel urinary biomarker for detecting acute kidney injury. Kidney Int. 2006; 70: 1847-1857.
96. Sonoda H, Yokota-Ikeda N, Oshikawa S, et al. Decreased abundance of urinary exosomal aquaporin-1 in renal ischemia-reperfusion injury. Am. J. Physiol. Renal Physiol. 2009; 297: F1006-1016.
97. Ramirez-Alvarado M, Ward CJ, Huang BQ, et al. Differences in immunoglobulin light chain species found in urinary exosomes in light chain amyloidosis (Al). PLoS ONE 2012; 7: e38061.
98. Miranda KC, Bond DT, McKee M, et al. Nucleic acids within urinary exosomes/microvesicles are potential biomarkers for renal disease. Kidney Int. 2010; 78: 191-199.
99. Navarro-Munoz M, Ibernon M, Perez V, et al. Messenger RNA expression of B7-1 and NPHS1 in urinary sediment could be useful to differentiate between minimal-change disease and focal segmental glomerulosclerosis in adult patients. Nephrol. Dial. Transplant. 2011; 26: 3914-3923.
100. van Ham SM, Heutinck KM, Jorritsma T, et al. Urinary granzyme A mRNA is a biomarker to diagnose subclinical and acute cellular rejection in kidney transplant recipients. Kidney Int. 2010; 78: 1033-1040.
101. 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.
102. Gatti S, Bruno S, Deregibus MC, et al. Microvesicles derived from human adult mesenchymal stem cells protect against ischaemia-reperfusion-induced acute and chronic kidney injury. Nephrol. Dial. Transplant. 2011; 26: 1474-1483.
103. Biancone L, Bruno S, Deregibus MC, Tetta C, Camussi G,. Therapeutic potential of mesenchymal stem cell-derived microvesicles. Nephrol. Dial. Transplant. 2012; 27: 3037-3042.
104. Viaud S, Thery C, Ploix S, et al. Dendritic cell-derived exosomes for cancer immunotherapy: What's next? Cancer Res. 2010; 70: 1281-1285.
105. Altieri SL, Khan AN, Tomasi TB,. Exosomes from plasmacytoma cells as a tumor vaccine. J. Immunother. 2004; 27: 282-288.
106. Marleau AM, Chen CS, Joyce JA, Tullis RH,. Exosome removal as a therapeutic adjuvant in cancer. J. Transl. Med. 2012; 10: 134.