Polarized HLA Class I Expression on Renal Tubules Hinders the Detection of Donor-Specific Urinary Extracellular Vesicles

References

• Halloran PF, Chang J, Famulski K, et al. Disappearance of T cell-mediated rejection despite continued antibody-mediated rejection in late kidney transplant recipients. J Am Soc Nephrol. 2015;26(7):1711–1720. doi:10.1681/ASN.2014060588
   PubMed Web of Science ®Google Scholar
• Verhoeven JGHP, Boer K, Van Schaik RHN, et al. Liquid biopsies to monitor solid organ transplant function: a review of new biomarkers. Ther Drug Monit. 2018;40(5):515–525. doi:10.1097/FTD.0000000000000549
   PubMed Web of Science ®Google Scholar
• Poggio ED, McClelland RL, Blank KN, et al. Systematic review and meta-analysis of native kidney biopsy complications. Clin J Am Soc Nephrol. 2020;15(11):1595–1602. doi:10.2215/CJN.04710420
   PubMed Web of Science ®Google Scholar
• MacGinley R, Champion De Crespigny PJ, Gutman T, et al. KHA-CARI Guideline recommendations for renal biopsy. Nephrology. 2019;24(12):1205–1213. doi:10.1111/nep.13662
   PubMed Web of Science ®Google Scholar
• Sailliet N, Ullah M, Dupuy A, et al. Extracellular Vesicles in Transplantation. Front Immunol. 2022:13. doi:10.3389/FIMMU.2022.800018
   Google Scholar
• Correll VL, Otto JJ, Risi CM, et al. Optimization of small extracellular vesicle isolation from expressed prostatic secretions in urine for in-depth proteomic analysis. J Extracell Vesicles. 2022;11(2). doi:10.1002/jev2.12184
   PubMed Web of Science ®Google Scholar
• Théry C, Witwer KW, Aikawa E, et al. Minimal information for studies of extracellular vesicles 2018 (MISEV2018): a position statement of the International Society for Extracellular Vesicles and update of the MISEV2014 guidelines. J Extracell Vesicles. 2018;7(1):2001–3078. doi:10.1080/20013078.2018.1535750
   Web of Science ®Google Scholar
• de Freitas RCC, Hirata RDC, Hirata MH, Aikawa E. Circulating extracellular vesicles as biomarkers and drug delivery vehicles in cardiovascular diseases. Biomolecules. 2021;11(3):1–20. doi:10.3390/biom11030388
   Web of Science ®Google Scholar
• Quaglia M, Dellepiane S, Guglielmetti G, Merlotti G, Castellano G, Cantaluppi V. Extracellular Vesicles as Mediators of Cellular Crosstalk Between Immune System and Kidney Graft. Front Immunol. 2020;11:74. doi:10.3389/fimmu.2020.00074
   PubMed Web of Science ®Google Scholar
• Admyre C, Grunewald J, Thyberg J, et al. Exosomes with major histocompatibility complex class II and co-stimulatory molecules are present in human BAL fluid. Eur Respir J. 2003;22(4):578–583. doi:10.1183/09031936.03.00041703
   PubMed Web of Science ®Google Scholar
• Hosseini‐Beheshti E, Grau GER. Extracellular vesicles as mediators of immunopathology in infectious diseases. Immunol Cell Biol. 2018;96(7):694–703. doi:10.1111/imcb.12044
   Web of Science ®Google Scholar
• Zhang Y, Ge T, Huang M, et al. Extracellular Vesicles Expressing CD19 Antigen Improve Expansion and Efficacy of CD19-Targeted CAR-T Cells. Int J Nanomed. 2023;18:49–63. doi:10.2147/IJN.S390720
   PubMed Web of Science ®Google Scholar
• Sedej I, Štalekar M, Tušek Žnidarič M, et al. Extracellular vesicle-bound DNA in urine is indicative of kidney allograft injury. J Extracell Vesicles. 2022;11(9). doi:10.1002/jev2.12268
   PubMed Web of Science ®Google Scholar
• Jung HY, Lee CH, Choi JY, et al. Potential urinary extracellular vesicle protein biomarkers of chronic active antibody-mediated rejection in kidney transplant recipients. J Chromatogr B. 2020. doi:10.1016/j.jchromb.2019.121958
   PubMed Web of Science ®Google Scholar
• Xu K, Liu Q, Wu K, et al. Extracellular vesicles as potential biomarkers and therapeutic approaches in autoimmune diseases. J Transl Med. 2020;18(1):1–8. doi:10.1186/S12967-020-02609-0/FIGURES/2
   PubMed Web of Science ®Google Scholar
• Braun F, Rinschen M, Buchner D, et al. The proteomic landscape of small urinary extracellular vesicles during kidney transplantation. J Extracell Vesicles. 2020;10(1):e12026. doi:10.1002/jev2.12026
   PubMed Web of Science ®Google Scholar
• Hariharan S, Israni AK, Danovitch G. Long-Term Survival after Kidney Transplantation. N Engl J Med. 2021;385(8):729–743. doi:10.1056/nejmra2014530
   PubMed Web of Science ®Google Scholar
• Wu L, Boer K, Woud WW, Udomkarnjananun S, Hesselink DA, Baan CC. Urinary extracellular vesicles are a novel tool to monitor allograft function in kidney transplantation: a systematic review. Int J Mol Sci. 2021;22(19):10499. doi:10.3390/ijms221910499
   PubMed Web of Science ®Google Scholar
• Boegel S, Löwer M, Bukur T, Sorn P, Castle JC, Sahin U. HLA and proteasome expression body map. BMC Med Genomics. 2018;11(1):1–12. doi:10.1186/s12920-018-0354-x
   PubMedGoogle Scholar
• Häyry P, Von Willebrand E, Andersson LC. Expression of HLA‐ABC and ‐DR Locus Antigens on Human Kidney, Endothelial, Tubular and Glomerular Cells. Scand J Immunol. 1980;11(3):303–310. doi:10.1111/j.1365-3083.1980.tb00238.x
   PubMed Web of Science ®Google Scholar
• Woud WW, Hesselink DA, Hoogduijn MJ, Baan CC, Boer K. Direct detection of circulating donor-derived extracellular vesicles in kidney transplant recipients. Sci Rep. 2022;12(1):21973. doi:10.1038/s41598-022-26580-6
   PubMed Web of Science ®Google Scholar
• Görgens A, Bremer M, Ferrer-Tur R, et al. Optimisation of imaging flow cytometry for the analysis of single extracellular vesicles by using fluorescence-tagged vesicles as biological reference material. J Extracell Vesicles. 2019;8(1):1587567. doi:10.1080/20013078.2019.1587567
   PubMed Web of Science ®Google Scholar
• Wu L, Woud WW, Baan CC, et al. Isolation-free measurement of single urinary extracellular vesicles by imaging flow cytometry. Nanomedicine Nanotechnology, Biol Med. 2023:48. doi:10.1016/j.nano.2022.102638
   Web of Science ®Google Scholar
• Woud WW, van der PE, Mul E, et al. An imaging flow cytometry-based methodology for the analysis of single extracellular vesicles in unprocessed human plasma. Commun Biol. 2022;40(1):633. doi:10.1101/2022.02.24.481807
   Google Scholar
• Pisitkun T, Shen R, Knepper MA. Identification and proteomic profiling of exosomes in human urine. Proc Natl Acad Sci U S A. 2004;101(36):13368–13373. doi:10.1073/pnas.0403453101
   PubMed Web of Science ®Google Scholar
• Svenningsen P, Sabaratnam R, Jensen BL. Urinary extracellular vesicles: origin, role as intercellular messengers and biomarkers; efficient sorting and potential treatment options. Acta Physiol. 2020;228(1):e13346. doi:10.1111/apha.13346
   PubMed Web of Science ®Google Scholar
• Evans PR, Trickett LP, Smith JL, MacIver AG, Tate D, Slapak M. Varying expression of major histocompatibility complex antigens on human renal endothelium and epithelium. Br J Exp Pathol. 1985;66(1):79–87.
   PubMedGoogle Scholar
• Gonzalez-Galarza F, McCabe A, Santos E, et al. The Allele Frequency Net Database [Search HLA Allele Frequencies]. Available form: http://allelefrequencies.net/hla6006a.asp?hla_locus_type=Classical&hla_locus=&hla_allele1=&hla_allele2=&hla_selection=&hla_pop_selection=&hla_population=2572&hla_country=Indonesia&hla_dataset=&hla_region=&hla_ethnic=&hla_study=&hla_order=order_1&hla_sampl. Accessed November 16, 2022.
   Google Scholar
• Hou L, Enriquez E, Persaud M, Steiner N, Oudshoorn M, Hurley CK. Next generation sequencing characterizes HLA diversity in a registry population from the Netherlands. Hla. 2019;93(6):474–483. doi:10.1111/tan.13535
   PubMed Web of Science ®Google Scholar
• Song S, Han M, Zhang H, Wang Y, Jiang H. Full screening and accurate subtyping of HLA-A*02 alleles through group-specific amplification and mono-allelic sequencing. Cell Mol Immunol. 2013;10(6):490–496. doi:10.1038/cmi.2013.33
   PubMed Web of Science ®Google Scholar
• Van Deun J, Mestdagh P, Agostinis P, et al. EV-TRACK: transparent reporting and centralizing knowledge in extracellular vesicle research. Int J Med. 2017;14(3):228–232.
   Google Scholar
• Francke MI, Andrews LM, Lan Le H, et al. Monitoring intracellular tacrolimus concentrations and its relationship with rejection in the early phase after renal transplantation. Clin Biochem. 2022;101:9–15. doi:10.1016/J.CLINBIOCHEM.2021.12.002
   PubMed Web of Science ®Google Scholar
• Lee SS, Won JH, Lim GJ, et al. A novel population of extracellular vesicles smaller than exosomes promotes cell proliferation. Cell Commun Signal. 2019;17(1):1–15. doi:10.1186/S12964-019-0401-Z
   PubMed Web of Science ®Google Scholar
• Brennan K, Martin K, FitzGerald SP, et al. A comparison of methods for the isolation and separation of extracellular vesicles from protein and lipid particles in human serum. Sci Rep. 2020;10(1). doi:10.1038/s41598-020-57497-7
   Web of Science ®Google Scholar
• Blijdorp CJ, Hartjes TA, Wei K, et al. Nephron mass determines the excretion rate of urinary extracellular vesicles. J Extracell Vesicles. 2022;11(1). doi:10.1002/JEV2.12181
   PubMed Web of Science ®Google Scholar
• Wachalska M, Koppers-Lalic D, van Eijndhoven M, et al. Protein Complexes in Urine Interfere with Extracellular Vesicle Biomarker Studies. J Circ Biomarkers. 2016;5:1–6. doi:10.5772/62579
   PubMedGoogle Scholar
• van der Pol E, Coumans FAW, Grootemaat AE, et al. Particle size distribution of exosomes and microvesicles determined by transmission electron microscopy, flow cytometry, nanoparticle tracking analysis, and resistive pulse sensing. J Thromb Haemost. 2014;12(7):1182–1192. doi:10.1111/jth.12602
   PubMed Web of Science ®Google Scholar
• Welsh JA, Van Der Pol E, Arkesteijn GJA, et al. MIFlowCyt-EV: a framework for standardized reporting of extracellular vesicle flow cytometry experiments. J Extracell Vesicles. 2020;9(1). doi:10.1080/20013078.2020.1713526
   Web of Science ®Google Scholar
• Duijvesz D, Versluis CYL, Van Der Fels CAM, et al. Immuno-based detection of extracellular vesicles in urine as diagnostic marker for prostate cancer. Int J Cancer. 2015;137(12):2869–2878. doi:10.1002/ijc.29664
   PubMed Web of Science ®Google Scholar
• Reiner AT, Tan S, Agreiter C, et al. EV-Associated MMP9 in High-Grade Serous Ovarian Cancer Is Preferentially Localized to Annexin V-Binding EVs. Dis Markers. 2017;2017. doi:10.1155/2017/9653194
   PubMed Web of Science ®Google Scholar
• Iancu CV, Tivol WF, Schooler JB, et al. Electron cryotomography sample preparation using the Vitrobot. Nat Protoc. 2007;1(6):2813–2819. doi:10.1038/nprot.2006.432
   Web of Science ®Google Scholar
• Shankar AS, Du Z, Mora HT, et al. Kidney Organoids Are Capable of Forming Tumors, but Not Teratomas. Stem Cells. 2022;40(6):577. doi:10.1093/STMCLS/SXAC009
   PubMed Web of Science ®Google Scholar
• Blijdorp CJ, Tutakhel OAZ, Hartjes TA, et al. Comparing approaches to normalize, quantify, and characterize urinary extracellular vesicles. J Am Soc Nephrol. 2021;32(5):1210–1226. doi:10.1681/ASN.2020081142
   PubMed Web of Science ®Google Scholar
• El-Awar NR, Akaza T, Terasaki PI, Nguyen A. Human leukocyte antigen class I epitopes: update to 103 total epitopes, including the C locus. Transplantation. 2007;84(4):532–540. doi:10.1097/01.tp.0000278721.97037.1e
   PubMed Web of Science ®Google Scholar
• Verbalis JG. Disorders of body water homeostasis. Best Pract Res Clin Endocrinol Metab. 2003;17(4):471–503. doi:10.1016/S1521-690X(03)00049-6
   PubMed Web of Science ®Google Scholar
• Yuana Y, Koning RI, Kuil ME, et al. Cryo‐electron microscopy of extracellular vesicles in fresh plasma. J Extracell Vesicles. 2013;2(1). doi:10.3402/jev.v2i0.21494
   PubMedGoogle Scholar
• Hancock WW, Kraft N, Atkins RC. The immunohistochemical demonstration of major histocompatibility antigens in the human kidney using monoclonal antibodies. Pathology. 1982;14(4):409–414. doi:10.3109/00313028209092120
   PubMed Web of Science ®Google Scholar
• Roberts JP, Wolfe RA, Bragg-Gresham JL, et al. Effect of Changing the Priority for HLA Matching on the Rates and Outcomes of Kidney Transplantation in Minority Groups. N Engl J Med. 2004;350(6):545–551. doi:10.1056/nejmoa025056
   PubMed Web of Science ®Google Scholar
• Cimorelli M, Nieuwland R, Varga Z, van der Pol E. Standardized procedure to measure the size distribution of extracellular vesicles together with other particles in biofluids with microfluidic resistive pulse sensing. PLoS One. 2021;16(4). doi:10.1371/JOURNAL.PONE.0249603
   PubMed Web of Science ®Google Scholar
• Song S, Manook M, Kwun J, Jackson AM, Knechtle SJ, Kelsoe G. Allo-Specific Humoral Responses: new Methods for Screening Donor-Specific Antibody and Characterization of HLA-Specific Memory B Cells. Front Immunol. 2021;12:2708. doi:10.3389/FIMMU.2021.705140/BIBTEX
   Web of Science ®Google Scholar
• Li DF, Yang MF, Xu J, et al. Extracellular Vesicles: the Next Generation Theranostic Nanomedicine for Inflammatory Bowel Disease. Int J Nanomed. 2022;17:3893. doi:10.2147/IJN.S370784
   PubMed Web of Science ®Google Scholar
• Bauzá-Martinez J, Heck AJR, Wu W. HLA-B and cysteinylated ligands distinguish the antigen presentation landscape of extracellular vesicles. Commun Biol. 2021;4(1). doi:10.1038/s42003-021-02364-y
   PubMed Web of Science ®Google Scholar
• Soares Lindoso R, Yousef Yengej FA, Voellmy F, et al. Differentiated kidney tubular cell-derived extracellular vesicles enhance maturation of tubuloids Journal of Nanobiotechnology Translational statement. J Nanobiotechnology. 2022;20:326. doi:10.1186/s12951-022-01506-6
   PubMed Web of Science ®Google Scholar
• Wang X, Wilkinson R, Kildey K, et al. Molecular and functional profiling of apical versus basolateral small extracellular vesicles derived from primary human proximal tubular epithelial cells under inflammatory conditions. J Extracell Vesicles. 2021;10(4). doi:10.1002/jev2.12064
   Web of Science ®Google Scholar
• Wu Q, Poulsen SB, Murali SK, et al. Large-scale proteomic assessment of urinary extracellular vesicles highlights their reliability in reflecting protein changes in the kidney. J Am Soc Nephrol. 2021;32(9):2195–2209. doi:10.1681/ASN.2020071035
   PubMed Web of Science ®Google Scholar
• Hernandez BJ, Skiba NP, Plößl K, et al. Polarized Desmosome and Hemidesmosome Shedding via Exosomes is an Early Indicator of Outer Blood-Retina Barrier Dysfunction. J Extracell Biol. 2023;2:e116. doi:10.1101/2023.06.12.544677
   PubMedGoogle Scholar
• Higashijima Y, Sonoda H, Takahashi S, Kondo H, Shigemura K, Ikeda M. Excretion of urinary exosomal AQP2 in rats is regulated by vasopressin and urinary pH. Am J Physiol - Ren Physiol. 2013;305(10). doi:10.1152/ajprenal.00249.2013
   PubMed Web of Science ®Google Scholar
• Oshikawa S, Sonoda H, Ikeda M. Aquaporins in urinary extracellular vesicles (Exosomes). Int J Mol Sci. 2016;17(6):957. doi:10.3390/ijms17060957
   PubMed Web of Science ®Google Scholar
• Miyazawa Y, Mikami S, Yamamoto K, et al. AQP2 in human urine is predominantly localized to exosomes with preserved water channel activities. Clin Exp Nephrol. 2018;22(4):782–788. doi:10.1007/s10157-018-1538-6
   PubMed Web of Science ®Google Scholar
• Salih M, Fenton RA, Knipscheer J, et al. An immunoassay for urinary extracellular vesicles. Am J Physiol - Ren Physiol. 2016;310(3):796–801. doi:10.1152/ajprenal.00463.2015
   Google Scholar
• Isaksson GL, Nielsen MB, Hinrichs GR, et al. Proteinuria is accompanied by intratubular complement activation and apical membrane deposition of C3dg and C5b-9 in kidney transplant recipients. Am J Physiol - Ren Physiol. 2022;322(2):F150–F163. doi:10.1152/AJPRENAL.00300.2021
   PubMed Web of Science ®Google Scholar
• Vos RDE, Wolf-peeters CDE, Van Den Oord JJ, Desmet V. Original Articles Ultrastructural Immunocytochemical Demonstration of HLA Class I Antigens in Human Pathological Liver Tissue. Hepatology. 1985;5(6):1071–1075. doi:10.1002/hep.1840050602
   PubMed Web of Science ®Google Scholar
• Dimuccio V, Ranghino A, Barbato LP, et al. Urinary CD133+ extracellular vesicles are decreased in kidney transplanted patients with slow graft function and vascular damage. PLoS One. 2014;9(8):e104490. doi:10.1371/journal.pone.0104490
   PubMed Web of Science ®Google Scholar
• Singh PB, Brown RE, Roser B. Class I transplantation antigens in solution in body fluids and in the urine. Individuality signals to the environment. J Exp Med. 1988;168(1):195–211. doi:10.1084/JEM.168.1.195
   PubMed Web of Science ®Google Scholar