1,719
Views
0
CrossRef citations to date
0
Altmetric
Review

Applications of Transcriptomics in the Research of Antibody-Mediated Rejection in Kidney Transplantation: Progress and Perspectives

ORCID Icon
Article: 2131357 | Received 28 Jul 2022, Accepted 28 Sep 2022, Published online: 19 Oct 2022

References

  • Tsai HI, Yu HP. A review of nationwide population study of organ transplantation in Taiwan. Acta Anaesthesiol Taiwan. 2016;54(70–74):70–13. doi:10.1016/j.aat.2016.05.003.
  • Wekerle T, Segev D, Lechler R, Oberbauer R. Strategies for long-term preservation of kidney graft function. Lancet. 2017;389(2152–2162):2152–62. doi:10.1016/S0140-6736(17)31283-7.
  • Hart A, Singh D, Brown SJ, Wang JH, Kasiske BL. Incidence, risk factors, treatment, and consequences of antibody-mediated kidney transplant rejection: a systematic review. Clin Transplant. 2021;35(e14320). doi:10.1111/ctr.14320.
  • Gaston RS, Cecka JM, Kasiske BL, Fieberg AM, Leduc R, Cosio FC, Gourishankar S, Grande J, Halloran P, Hunsicker L, et al. Evidence for antibody-mediated injury as a major determinant of late kidney allograft failure. Transplantation. 2010;90(68–74). doi:10.1097/TP.0b013e3181e065de
  • DeWolf S, Alloimmune SM. T cells in transplantation. J Clin Invest. 2017;127(2473–2481):2473–81. doi:10.1172/JCI90595.
  • Becker LE, Morath C, Suesal C. Immune mechanisms of acute and chronic rejection. Clin Biochem. 2016;49(320–323):320–23. doi:10.1016/j.clinbiochem.2016.02.001.
  • Herrera OB, Golshayan D, Tibbott R, Ochoa FS, James MJ, Marelli-Berg FM, Lechler RI. A novel pathway of alloantigen presentation by dendritic cells. J Immunol. 2004;173(4828–4837). doi:10.4049/jimmunol.173.8.4828.
  • Vinuesa CG, Linterman MA, Yu D, MacLennan IC. Follicular helper T cells. Annu Rev Immunol. 2016;34(335–368):335–68. doi:10.1146/annurev-immunol-041015-055605.
  • Leibler C, et al. Control of humoral response in renal transplantation by belatacept depends on a direct effect on B cells and impaired T follicular helper-B cell crosstalk. J Am Soc Nephrol. 2018;29(1049–1062):1049–62. doi:10.1681/ASN.2017060679.
  • Wallin EF. Follicular regulatory T. Cells and antibody responses in transplantation. Transplantation. 2018;102(1614–1623):1614–23. doi:10.1097/TP.0000000000002224.
  • Louis K, Macedo C, Metes D. Targeting T follicular helper cells to control humoral allogeneic immunity. Transplantation. 2021;105(11):e168–e180. doi:10.1097/TP.0000000000003776.
  • Chong AS, Sciammas R. Memory B cells in transplantation. Transplantation. 2015;99(21–28):21–28. doi:10.1097/TP.0000000000000545.
  • Kim MY, Brennan DC. Therapies for chronic allograft rejection. Front Pharmacol. 2021;12(651222). doi:10.3389/fphar.2021.651222.
  • Zhang R. Donor-Specific antibodies in kidney transplant recipients. Clin J Am Soc Nephrol. 2018;13(182–192):182–92. doi:10.2215/CJN.00700117.
  • Colvin RB, Smith RN. Antibody-mediated organ-allograft rejection. Nat Rev Immunol. 2005;5(807–817):807–17. doi:10.1038/nri1702.
  • Cross AR, Glotz D, Mooney N. The role of the endothelium during antibody-Mediated rejection: from victim to accomplice. Front Immunol. 2018;9(106). doi:10.3389/fimmu.2018.00106.
  • Jeannet M, Pinn VW, Flax MH, Winn HJ, Russell PS. Humoral antibodies in renal allotransplantation in man. N Engl J Med. 1970;282(111–117):111–17. doi:10.1056/NEJM197001152820301.
  • Feucht HE, et al. Vascular deposition of complement-split products in kidney allografts with cell-mediated rejection. Clin Exp Immunol. 1991;86(464–470). doi:10.1111/j.1365-2249.1991.tb02954.x
  • Loupy A, Mengel M, Haas M. Thirty years of the international Banff classification for allograft pathology: the past, present, and future of kidney transplant diagnostics. Kidney Int. 2022;101(678–691). doi:10.1016/j.kint.2021.11.028.
  • Loupy A, Haas M, Roufosse C, Naesens M, Adam B, Afrouzian M, Akalin E, Alachkar N, Bagnasco S, Becker JU, et al. The Banff 2019 kidney meeting report (I): updates on and clarification of criteria for T cell- and antibody-mediated rejection. Am J Transplant. 2020;20:2318–31. doi:10.1111/ajt.15898.
  • Solez K, Colvin RB, Racusen LC, Haas M, Sis B, Mengel M, Halloran PF, Baldwin W, Banfi G, Collins AB, et al. Banff 07 classification of renal allograft pathology: updates and future directions. Am J Transplant. 2008;8(753–760). doi:10.1111/j.1600-6143.2008.02159.x
  • Correa RR, Machado JR, da Silva MV, Helmo FR, Guimarães CSO, Rocha LP, Faleiros ACG, Dos Reis MA. The importance of C4d in biopsies of kidney transplant recipients. Clin Dev Immunol. 2013;2013(678180). doi:10.1155/2013/678180.
  • Jeong HJ. Diagnosis of renal transplant rejection: Banff classification and beyond. Kidney Res Clin Pract. 2020;39(17–31):17–31. doi:10.23876/j.krcp.20.003.
  • Haas M. The revised (2013) Banff classification for antibody-Mediated rejection of renal allografts: update, difficulties, and future considerations. Am J Transplant. 2016;16(1352–1357):1352–57. doi:10.1111/ajt.13661.
  • Loupy A, et al. The Banff 2015 kidney meeting report: current challenges in rejection classification and prospects for adopting molecular pathology. Am J Transplant. 2017;17(28–41):28–41. doi:10.1111/ajt.14107.
  • Haas M, Loupy A, Lefaucheur C, Roufosse C, Glotz D, Seron D, Nankivell BJ, Halloran PF, Colvin RB, Akalin E, et al. The Banff 2017 kidney meeting report: revised diagnostic criteria for chronic active T cell-mediated rejection, antibody-mediated rejection, and prospects for integrative endpoints for next-generation clinical trials. Am J Transplant. 2018;18(293–307). doi:10.1111/ajt.14625
  • Solar-Cafaggi D, Marino L, Uribe-Uribe N, Morales-Buenrostro LE. Antibody-mediated rejection in the Banff classifications of 2007 and 2017: a comparison of renal graft loss prediction capability. Transpl Immunol. 2018;51(40–44):40–44. doi:10.1016/j.trim.2018.08.008.
  • Wan SS, Ying TD, Wyburn K, Roberts DM, Wyld M, Chadban SJ. The treatment of antibody-mediated rejection in kidney transplantation: an updated systematic review and meta-Analysis. Transplantation. 2018;102(557–568). doi:10.1097/TP.0000000000002049.
  • Khan SA, Al-Riyami, D., Abed, Y. W. A. M., Mohammed, S., Al-Riyami, M., & Al-Lawati, N. M. Successful salvage treatment of resistant acute antibody-mediated kidney transplant rejection with eculizumab. Sultan Qaboos Univ Med J. 2016;16(e371–374):e371–37. doi:10.18295/squmj.2016.16.03.020.
  • Tan EK, Bentall A, Dean PG, Shaheen MF, Stegall MD, Schinstock CA. Use of eculizumab for active antibody-mediated rejection that occurs early post-kidney transplantation: a consecutive series of 15 cases. Transplantation. 2019;103(2397–2404). doi:10.1097/TP.0000000000002639.
  • Kulkarni S, Kirkiles-Smith NC, Deng YH, Formica RN, Moeckel G, Broecker V, Bow L, Tomlin R, Pober JS. Eculizumab therapy for chronic antibody-Mediated injury in kidney transplant recipients: a pilot randomized controlled trial. Am J Transplant. 2017;17(682–691). doi:10.1111/ajt.14001.
  • Thareja G, Yang H, Hayat S, Mueller FB, Lee JR, Lubetzky M, Dadhania DM, Belkadi A, Seshan SV, Suhre K, et al. Single nucleotide variant counts computed from RNA sequencing and cellular traffic into human kidney allografts. Am J Transplant. 2018;18(2429–2442). doi:10.1111/ajt.14870
  • Deepak S, Kottapalli KR, Rakwal R, Oros G, Rangappa KS, Iwahashi H, Masuo Y, Agrawal GK. Real-Time PCR: revolutionizing detection and expression analysis of genes. Curr Genomics. 2007;8(234–251). doi:10.2174/138920207781386960.
  • Strehlau J, Pavlakis M, Lipman M, Shapiro M, Vasconcellos L, Harmon W, Strom T. Quantitative detection of immune activation transcripts as a diagnostic tool in kidney transplantation. Proc Natl Acad Sci U S A. 1997;94(695–700). doi:10.1073/pnas.94.2.695.
  • Suthanthiran M. Clinical application of molecular biology: a study of allograft rejection with polymerase chain reaction. Am J Med Sci. 1997;313(264–267):264–67. doi:10.1097/00000441-199705000-00003.
  • Schena M, Shalon D, Davis RW, Brown PO. Quantitative monitoring of gene expression patterns with a complementary DNA microarray. Science. 1995;270(467–470):467–70. doi:10.1126/science.270.5235.467.
  • Sarwal M, Chua M-S, Kambham N, Hsieh S-C, Satterwhite T, Masek M, Salvatierra O. Molecular heterogeneity in acute renal allograft rejection identified by DNA microarray profiling. N Engl J Med. 2003;349(125–138). doi:10.1056/NEJMoa035588.
  • Flechner SM, Kurian SM, Head SR, Sharp SM, Whisenant TC, Zhang J, Chismar JD, Horvath S, Mondala T, Gilmartin T, et al. Kidney transplant rejection and tissue injury by gene profiling of biopsies and peripheral blood lymphocytes. Am J Transplant. 2004;4(1475–1489). doi:10.1111/j.1600-6143.2004.00526.x
  • Halloran PF, De Freitas DG, Einecke G, Famulski KS, Hidalgo LG, Mengel M, Reeve J, Sellares J, Sis B. The molecular phenotype of kidney transplants. Am J Transplant. 2010;10(2215–2222). doi:10.1111/j.1600-6143.2010.03267.x.
  • Sis B, et al. Endothelial gene expression in kidney transplants with alloantibody indicates antibody-mediated damage despite lack of C4d staining. Am J Transplant. 2009;9(2312–2323):2312–23. doi:10.1111/j.1600-6143.2009.02761.x.
  • Sellares J, Reeve J, Loupy A, Mengel M, Sis B, Skene A, de Freitas DG, Kreepala C, Hidalgo LG, Famulski KS, et al. Molecular diagnosis of antibody-mediated rejection in human kidney transplants. Am J Transplant. 2013;13(971–983). doi:10.1111/ajt.12150
  • Halloran PF, Pereira, A. B., Chang, J., Matas, A., Picton, M., De Freitas, D. & Reeve, J. Microarray diagnosis of antibody-mediated rejection in kidney transplant biopsies: an international prospective study (INTERCOM). Am J Transplant. 2013;13(2865–2874). doi:10.1111/ajt.12465
  • Halloran PF, Famulski KS, Reeve J. Molecular assessment of disease states in kidney transplant biopsy samples. Nat Rev Nephrol. 2016;12(534–548):534–48. doi:10.1038/nrneph.2016.85.
  • Halloran PF, Reeve J, Akalin E, Aubert O, Bohmig GA, Brennan D, Bromberg J, Einecke G, Eskandary F, Gosset C, et al. Real time central assessment of kidney transplant indication biopsies by microarrays: the INTERCOMEX study. Am J Transplant. 2017;17(2851–2862). doi:10.1111/ajt.14329
  • Allanach K, Mengel, M., Einecke, G., Sis, B., Hidalgo, L. G., Mueller, T., & Halloran, P. F. Comparing microarray versus RT-PCR assessment of renal allograft biopsies: similar performance despite different dynamic ranges. Am J Transplant. 2008;8(1006–1015):1006–15. doi:10.1111/j.1600-6143.2008.02199.x.
  • Park WD, Stegall MD. A meta-analysis of kidney microarray datasets: investigation of cytokine gene detection and correlation with rt-PCR and detection thresholds. BMC Genomics. 2007;8(88):88. doi:10.1186/1471-2164-8-88.
  • Wang Z, Gerstein M, Snyder M. RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet. 2009;10(57–63):57–63. doi:10.1038/nrg2484.
  • Stark R, Grzelak M, Hadfield J. RNA sequencing: the teenage years. Nat Rev Genet. 2019;20(631–656):631–56. doi:10.1038/s41576-019-0150-2.
  • Pineda S, Sur S, Sigdel T, Nguyen M, Crespo E, Torija A, Meneghini M, Gomà M, Sirota M, Bestard O, et al. Peripheral blood RNA sequencing unravels a differential signature of coding and noncoding genes by types of kidney allograft rejection. Kidney Int Rep. 2020;5(1706–1721). doi:10.1016/j.ekir.2020.07.023
  • Wang X, Mitra, N., Secundino, I., Banda, K., Cruz, P., Padler-Karavani, V. & Young, A. Specific inactivation of two immunomodulatory SIGLEC genes during human evolution. Proc Natl Acad Sci U S A. 2012;109(9935–9940). doi:10.1073/pnas.1119459109
  • Dooley BJ, Verma A, Ding R, Yang H, Muthukumar T, Lubetzky M, Shankaranarayanan D, Elemento O, Suthanthiran M. Urinary cell transcriptome profiling and identification of ITM2A, SLAMF6, and IKZF3 as biomarkers of acute rejection in human kidney allografts. Transplant Direct. 2020;6(e588). doi:10.1097/TXD.0000000000001035.
  • Randhawa PS. The molecular microscope diagnostic system (MMDx) in transplantation: a pathologist’s perspective. Am J Transplant. 2020;20(1965–1966):1965–66. doi:10.1111/ajt.15887.
  • Chen L, Lee JW, Chou C-L, Nair AV, Battistone MA, Păunescu TG, Merkulova M, Breton S, Verlander JW, Wall SM, et al. Transcriptomes of major renal collecting duct cell types in mouse identified by single-cell RNA-seq. Proc Natl Acad Sci U S A. 2017;114:E9989–E9998. doi:10.1073/pnas.1710964114.
  • Choi J, Aubert O, Vo A, Loupy A, Haas M, Puliyanda D, Kim I, Louie S, Kang A, Peng A, et al. Assessment of Tocilizumab (Anti-Interleukin-6 receptor monoclonal) as a potential treatment for chronic antibody-Mediated rejection and transplant glomerulopathy in HLA-Sensitized renal allograft recipients. Am J Transplant. 2017;17(9):2381–89. doi:10.1111/ajt.14228.
  • Mathews DV, Wakwe WC, Kim SC, Lowe MC, Breeden C, Roberts ME, Farris AB, Strobert EA, Jenkins JB, Larsen CP, et al. Belatacept-Resistant rejection is associated with CD28 + memory CD8 T cells. Am J Transplant. 2017;17(2285–2299). doi:10.1111/ajt.14349
  • Liao J, Yu Z, Chen Y, Bao M, Zou C, Zhang H, Liu D, Li T, Zhang Q, Li J, et al. Single-cell RNA sequencing of human kidney. Sci Data. 2020;7(4). doi:10.1038/s41597-019-0351-8
  • Park J, Shrestha R, Qiu C, Kondo A, Huang S, Werth M, Li M, Barasch J, Suszták K. Single-cell transcriptomics of the mouse kidney reveals potential cellular targets of kidney disease. Science. 2018;360(758–763). doi:10.1126/science.aar2131.
  • Tang F, Barbacioru C, Wang Y, Nordman E, Lee C, Xu N, Wang X, Bodeau J, Tuch BB, Siddiqui A, et al. mRNA-Seq whole-transcriptome analysis of a single cell. Nature Methods. 2009;6(377–382). doi:10.1038/nmeth.1315
  • Denyer T, Timmermans MCP. High-throughput single-cell RNA sequencing. Trends Plant Sci. 2022;27(104–105). doi:10.1016/j.tplants.2021.09.003.
  • Al-Awqati Q, Oliver JA. Stem cells in the kidney. Kidney Int. 2002;61(387–395):387–95. doi:10.1046/j.1523-1755.2002.00164.x.
  • Trailin A, Mrazova P, Hruba P, Voska L, Sticova E, Slavcev A, Novotny M, Kocik M, Viklicky O. Chronic active antibody-mediated rejection is associated with the upregulation of interstitial but not glomerular transcripts. Front Immunol. 2021;12(729558). doi:10.3389/fimmu.2021.729558.
  • Haque A, Engel J, Teichmann SA, Lonnberg T. A practical guide to single-cell RNA-sequencing for biomedical research and clinical applications. Genome Med. 2017;9(75). doi:10.1186/s13073-017-0467-4.
  • Wang Y, Wang JY, Schnieke A, Fischer K. Advances in single-cell sequencing: insights from organ transplantation. Mil Med Res. 2021;8(45). doi:10.1186/s40779-021-00336-1.
  • Tian B, Li LQ. Single-Cell sequencing and its applications in liver cancer. Front Oncol. 2022;12(857037). doi:10.3389/fonc.2022.857037.
  • Srinivasan M, Sedmak D, Jewell S. Effect of fixatives and tissue processing on the content and integrity of nucleic acids. Am J Pathol. 2002;161(1961–1971):1961–71. doi:10.1016/S0002-9440(10)64472-0.
  • Alles J, Karaiskos N, Praktiknjo SD, Grosswendt S, Wahle P, Ruffault P-L, Ayoub S, Schreyer L, Boltengagen A, Birchmeier C, et al. Cell fixation and preservation for droplet-based single-cell transcriptomics. BMC Biol. 2017;15(44). doi:10.1186/s12915-017-0383-5
  • Rao DA, Arazi A, Wofsy D, Diamond B. Design and application of single-cell RNA sequencing to study kidney immune cells in lupus nephritis. Nat Rev Nephrol. 2020;16(238–250):238–50. doi:10.1038/s41581-019-0232-6.
  • Wu H, Humphreys BD. The promise of single-cell RNA sequencing for kidney disease investigation. Kidney Int. 2017;92(1334–1342):1334–42. doi:10.1016/j.kint.2017.06.033.
  • Heng TS, Painter MW, Elpek K, Lukacs-Kornek V, Mauermann N, Turley SJ, Koller D, Kim FS, Wagers AJ, Asinovski N; Immunological Genome Project, C. The immunological genome project: networks of gene expression in immune cells. Nat Immunol. 2008;9(1091–1094). doi:10.1038/ni1008-1091.
  • Dangi A, Natesh NR, Husain I, Ji Z, Barisoni L, Kwun J, Shen X, Thorp EB, Luo X. Single cell transcriptomics of mouse kidney transplants reveals a myeloid cell pathway for transplant rejection. JCI Insight. 2020:5. doi:10.1172/jci.insight.141321.
  • Wu H, Malone AF, Donnelly EL, Kirita Y, Uchimura K, Ramakrishnan SM, Gaut JP, Humphreys BD. Single-Cell transcriptomics of a human kidney allograft biopsy specimen defines a diverse inflammatory response. J Am Soc Nephrol. 2018;29(2069–2080). doi:10.1681/ASN.2018020125.
  • Liu Y, Hu J, Liu D, Zhou S, Liao J, Liao G, Yang S, Guo Z, Li Y, Li S, et al. Single-cell analysis reveals immune landscape in kidneys of patients with chronic transplant rejection. Theranostics. 2020;10(8851–8862). doi:10.7150/thno.48201
  • Malone AF, Wu H, Fronick C, Fulton R, Gaut JP, Humphreys BD. Harnessing expressed single nucleotide variation and single cell RNA sequencing to define immune cell chimerism in the rejecting kidney transplant. J Am Soc Nephrol. 2020;31(1977–1986). doi:10.1681/ASN.2020030326.
  • Kong F, Ye, S., Zhong, Z., Zhou, X., Zhou, W., Liu, Z. & Ye, Q. Single-Cell transcriptome analysis of chronic antibody-mediated rejection after renal transplantation. Front Immunol. 2021;12(767618). doi:10.3389/fimmu.2021.767618
  • Asano Y, Daccache J, Jain D, Ko K, Kinloch A, Veselits M, Wolfgeher D, Chang A, Josephson M, Cunningham P, et al. Innate-like self-reactive B cells infiltrate human renal allografts during transplant rejection. Nat Commun. 2021;12(4372). doi:10.1038/s41467-021-24615-6
  • Zimmerman KA, Bentley, M. R., Lever, J. M., Li, Z., Crossman, D. K., Song, C. J. & Yoder, B. K. Single-Cell RNA sequencing identifies candidate renal resident macrophage gene expression signatures across species. J Am Soc Nephrol. 2019;30(767–781):767–81. doi:10.1681/ASN.2018090931.
  • Chen G, Ning B, Single-Cell ST. RNA-Seq Technologies and Related Computational Data Analysis. Front Genet. 2019;10(317). doi:10.3389/fgene.2019.00317.
  • Zheng GX, Terry JM, Belgrader P, Ryvkin P, Bent ZW, Wilson R, Ziraldo SB, Wheeler TD, McDermott GP, Zhu J, et al. Massively parallel digital transcriptional profiling of single cells. Nat Commun. 2017;8(14049). doi:10.1038/ncomms14049
  • Zhang X, Li T, Liu F, Chen Y, Yao J, Li Z, Huang Y, Wang J. Comparative analysis of droplet-Based Ultra-High-Throughput single-Cell RNA-Seq systems. Mol Cell. 2019;73:130–42. doi:10.1016/j.molcel.2018.10.020.
  • Muthukumar T,YH, Belkadi A, Thareja G, Li C, Snopkowski C, Chen K, Salinas T, Lubetzky M, Lee J, Dadhania D, et al. Single cell RNA-Sequencing of urinary cells and defining the immune landscape of rejection in human kidney allografts [abstract]. Am J Transplant. 2021;21(suppl 3):32–36. https://atcmeetingabstracts.com/abstract/single-cell-rna-sequencing-of-urinary-cells-and-defining-the-immune-landscape-of-rejection-in-human-kidney-allografts/.
  • Shen Q, Wang Y, Chen J, Ma L, Huang X, Tang SCW, Lan H, Jiang H, Chen J. Single-Cell RNA sequencing reveals the immunological profiles of renal allograft rejection in mice. Front Immunol. 2021;12(693608). doi:10.3389/fimmu.2021.693608.
  • Stewart BJ, Ferdinand JR, Clatworthy MR. Using single-cell technologies to map the human immune system - implications for nephrology. Nat Rev Nephrol. 2020;16(112–128):112–28. doi:10.1038/s41581-019-0227-3.
  • Malone AF. Monocytes and macrophages in kidney transplantation and insights from single cell RNA-Seq studies. Kidney360. 2021;2(1654–1659):1654–59. doi:10.34067/KID.0003842021.