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Research Paper

Time-course full profiling of circulating miRNAs in neurologically deceased organ donors: a proof of concept study to understand the onset of the cytokine storm

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Pages 1546-1561 | Received 17 Aug 2021, Accepted 03 May 2022, Published online: 21 May 2022

References

  • Organ Donation and Transplantation Activities 2019 Report. Global Observatory on Donation and Transplantation (GODT) those 2019 data are based on the Global Observatory on Donation and Transplantation (GODT) data, produced by the WHO-ONT collaboration.
  • Lodhi SA, Lamb KE, Meier-Kriesche HU. Solid organ allograft survival improvement in the United States: the long-term does not mirror the dramatic short-term success. Am J Transplant. 2011;11:1226–1235.
  • Terasaki PI, Cecka JM, Gjertson DW, et al. High survival rates of kidney transplants from spousal and living unrelated donors. N Engl J Med. 1995;333:333–336.
  • Hariharan S, Johnson CP, Bresnahan BA, et al. Improved graft survival after renal transplantation in the United States, 1988 to 1996. N Engl J Med. 2000;342:605–612.
  • Kosieradzki M, Rowiński W. Ischemia/reperfusion injury in kidney transplantation: mechanisms and prevention. Transplant Proc. 2008;40:3279–3288.
  • Smith M. Physiologic changes during brain stem death–lessons for management of the organ donor. J Heart Lung Transplant. 2004;23:S217–222.
  • Barklin A. Systemic inflammation in the brain-dead organ donor. Acta Anaesthesiol Scand. 2009;53:425–435.
  • Cohen O, La Zerda DJ D, Beygui R, et al. Donor brain death mechanisms and outcomes after heart transplantation. Transplant Proc. 2007;39:2964–2969.
  • Saito T, Takahashi H, Kaneda H, et al. Impact of cytokine expression in the pre-implanted donor lung on the development of chronic lung allograft dysfunction subtypes: cytokines in pre-implant donor lung and CLAD. Am J Transplant. 2013;13:3192–3201.
  • Weiss S, Kotsch K, Francuski M, et al. Brain death activates donor organs and is associated with a worse I/R injury after liver transplantation. Am J Transplant. 2007;7:1584–1593.
  • Sánchez-Fructuoso AI, Prats D, Marques M, et al. Does donor brain death influence acute vascular rejection in the kidney transplant? Transplantation. 2004;78:142–146.
  • Fijter JWD, Mallat MJK, Doxiadis IIN, et al. Increased immunogenicity and cause of graft loss of old donor kidneys. J Am Soc Nephrol. 2001;12:1538–1546.
  • Wolfe RA, Ashby VB, Milford EL, et al. Comparison of mortality in all patients on dialysis, patients on dialysis awaiting transplantation, and recipients of a first cadaveric transplant. N Engl J Med. 1999;341:1725–1730.
  • Cheung KP, Kasimsetty SG, McKay DB. Innate immunity in donor procurement. Curr Opin Organ Transplant. 2013;18:154–160.
  • McLaughlin PJ, Aikawa AA, Davies HM, et al. Tumour necrosis factor in renal transplantation. Transplant Proc. 1991;23(1 Pt 2):1289–1290.
  • Sonkar GK, Usha, Singh RG. Evaluation of serum tumor necrosis factor alpha and its correlation with histology in chronic kidney disease, stable renal transplant and rejection cases. Saudi J Kidney Dis Transpl. 2009;20(6):1000–1004.
  • Wiggins MC, Bracher M, Mall A, et al. Tumour necrosis factor levels during acute rejection and acute tubular necrosis in renal transplant recipients. Transpl Immunol. 2000;8:211–215.
  • Senturk Ciftci H, Demir E, Savran Karadeniz M, et al. Serum and Urinary Levels of Tumor Necrosis Factor-Alpha in Renal Transplant Patients. Exp Clin Transplant. 2018;16(6):671–675.
  • Watts RP, Thom O, Fraser JF. Inflammatory signalling associated with brain dead organ donation: from brain injury to brain stem death and posttransplant ischaemia reperfusion injury. J Transplant. 2013;2013:521369.
  • Field M, Dronavalli V, Mistry P, et al. Urinary biomarkers of acute kidney injury in deceased organ donors - kidney injury molecule-1 as an adjunct to predicting outcome. Clin Transplant. 2014;28:808–815.
  • Mascia L, Mastromauro I, Viberti S, et al. Management to optimize organ procurement in brain dead donors. Minerva anestesiologica. 2009;75(3):125–133.
  • Shah VR. Aggressive management of multiorgan donor. Transplant Proc. 2008;40:1087–1090.
  • Dikdan GS, Mora-Esteves C, Koneru B. Review of randomized clinical trials of donor management and organ preservation in deceased donors: opportunities and issues. Transplantation. 2012;94:425–441.
  • Mitchell PS, Parkin RK, Kroh EM, et al. Circulating microRNAs as stable blood-based markers for cancer detection. Proc Natl Acad Sci USA. 2008;105:10513–10518.
  • Atif H, Hicks SD. A review of microRNA biomarkers in traumatic brain injury. J Exp Neurosci. 2019;13:117906951983228.
  • Mori MA, Ludwig RG, Garcia-Martin R, et al. Extracellular miRNAs: from Biomarkers to Mediators of Physiology and Disease. Cell Metab. 2019;30(4):656–673.
  • O’Brien J, Hayder H, Zayed Y, et al. Overview of microRNA Biogenesis, Mechanisms of Actions, and Circulation. Front Endocrinol (Lausanne). 2018;9:402.
  • Ledeganck KJ, Gielis EM, Abramowicz D, et al. MicroRNAs in AKI and kidney transplantation. Clin J Am Soc Nephrol. 2019;14:454–468.
  • Mas VR, Dumur CI, Scian MJ, et al. MicroRNAs as biomarkers in solid organ transplantation. Am J Transplant. 2013;13:11–19.
  • Barry CT. Organ transplantation and microRNA expression [Internet]. In: MicroRNA in Regenerative Medicine. Elsevier; 2015 [cited 2021 Jan 12]. 835–862. Available from: https://linkinghub.elsevier.com/retrieve/pii/B9780124055445000320
  • Khalid U, Newbury LJ, Simpson K, et al. A urinary microRNA panel that is an early predictive biomarker of delayed graft function following kidney transplantation. Sci Rep. 2019;9:3584.
  • Wilflingseder J, Jelencsics K, Bergmeister H, et al. Inhibition ameliorates ischemic acute kidney injury. Am J Pathol. 2017;187:70–79. miR-182-5p.
  • Tao J, Yang X, Han Z, et al. Serum microRNA-99a helps detect acute rejection in renal transplantation. Transplant Proc. 2015;47:1683–1687.
  • Lorenzen JM, Volkmann I, Fiedler J, et al. Urinary miR-210 as a mediator of acute T-cell mediated rejection in renal allograft recipients. Am J Transplant. 2011;11:2221–2227.
  • Ball IM, Hornby L, Rochwerg B, et al. Management of the neurologically deceased organ donor: a Canadian clinical practice guideline. Cmaj. 2020;192:E361–9.
  • D’Aragon F, Lamontagne F, Cook D, et al. Variability in deceased donor care in Canada: a report of the Canada-DONATE cohort study. Can J Anaesth. 2020;67:992–1004.
  • Shemie SD. Severe brain injury to neurological determination of death: Canadian forum recommendations. Can Med Assoc J. 2006;174:S1–12.
  • Cordoba J, Dhawan A, Larsen FS, et al.; European Association for the Study of the LiverElectronic address: Clinical practice guidelines panel, Wendon, Panel members. EASL clinical practical guidelines on the management of acute (fulminant) liver failure. J Hepatol. 2017;66:1047–1081.
  • Tworoger SS, Yasui Y, Chang L, et al. Specimen allocation in longitudinal biomarker studies: controlling subject-specific effects by design. Cancer Epidemiol Biomarkers Prev. 2004;13(7):1257–1260.
  • Azarpira N, Nikeghbalian S, Kazemi K, et al. Association of increased plasma interleukin-6 and TNF-α levels in donors with the complication rates in liver transplant recipients. International Journal of Organ Transplantation Medicine. 2013;4(1):9–14.
  • Venkateswaran RV, Dronavalli V, Lambert PA, et al. The proinflammatory environment in potential heart and lung donors: prevalence and impact of donor management and hormonal therapy. Transplantation. 2009;88:582–588.
  • Burgos KL, Javaherian A, Bomprezzi R, et al. Identification of extracellular miRNA in human cerebrospinal fluid by next-generation sequencing. RNA. 2013;19:712–722.
  • Rozowsky J, Kitchen RR, Park JJ, et al. exceRpt: a comprehensive analytic platform for extracellular RNA profiling. Cell Syst. 2019;8:352–357.e3.
  • Oksanen J, Blanchet G, Friendly M, et al. vegan: Community Ecology Package [Internet]. 2020. Available from: https://CRAN.R-project.org/package=vegan
  • McMurdie PJ, Holmes S. phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE. 2013;8:e61217.
  • Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15:550.
  • R Core Team. R: a language and environment for statistical computing [Internet]. Vienna Austria: R Foundation for Statistical Computing; 2013. Available from: http://www.R-project.org/
  • Hadley W. ggplot2: Elegant graphics for data analysis [Internet]. Springer-Verlag New York; 2016. Available from: https://ggplot2.tidyverse.org
  • Waskom M, Botvinnik O, Gelbart M, et al. mwaskom/seaborn: v0.11.0 (Sepetmber 2020) [Internet]. Zenodo; 2020 cited 2020 Nov 27]. Available from 2020 Nov 27: https://zenodo.org/record/592845
  • RStudioTeam. RStudio: integrated development for R. RStudio [Internet]. PBC, Boston MA: 2020. Available from http://www.rstudio.com/
  • Vlachos IS, Zagganas K, Paraskevopoulou MD, et al. DIANA-miRPath v3.0: deciphering microRNA function with experimental support. Nucleic Acids Res. 2015;43:W460–466.
  • Kanehisa M, Goto S. KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 2000;28:27–30.
  • Klein SL, Flanagan KL. Sex differences in immune responses. Nat Rev Immunol. 2016;16:626–638.
  • Tarrant JM. Blood cytokines as biomarkers of in vivo toxicity in preclinical safety assessment: considerations for their use. Toxicol Sci. 2010;117:4–16.
  • Moreno-Martinez L, Calvo AC, Muñoz MJ, et al. Are circulating cytokines reliable biomarkers for amyotrophic lateral sclerosis? Ijms. 2019;20:2759.
  • Banerjee S, Cui H, Xie N, et al. Regulates differential activation of macrophages and inflammation. J Biol Chem. 2013;288:35428–35436. miR-125a-5p.
  • Li J, He W, Wang Y, et al. miR-103a-3p alleviates oxidative stress, apoptosis, and immune disorder in oxygen-glucose deprivation-treated BV2 microglial cells and rats with cerebral ischemia-reperfusion injury by targeting high mobility group box 1. Ann Transl Med. 2020;8:1296.
  • Zhang H, Lu X, Hao Y, et al. MicroRNA-26a-5p alleviates neuronal apoptosis and brain injury in intracerebral hemorrhage by targeting RAN binding protein 9. Acta Histochem. 2020;122:151571.
  • Wei R, Zhang L, Hu W, et al. Long non-coding RNA AK038897 aggravates cerebral ischemia/reperfusion injury via acting as a ceRNA for miR-26a-5p to target DAPK1. Exp Neurol. 2019;314:100–110.
  • Leprivier G, Remke M, Rotblat B, et al. The eEF2 kinase confers resistance to nutrient deprivation by blocking translation elongation. Cell. 2013;153:1064–1079.
  • Kameshima S, Okada M, Yamawaki H. Eukaryotic elongation factor 2 (eEF2) kinase/eEF2 plays protective roles against glucose deprivation-induced cell death in H9c2 cardiomyoblasts. Apoptosis. 2019;24:359–368.
  • Bouma HR, Ketelaar ME, Yard BA, et al. AMP-activated protein kinase as a target for preconditioning in transplantation medicine. Transplantation. 2010;90:353–358.
  • Kanellis J, Ma FY, Kandane-Rathnayake R, et al. JNK signalling in human and experimental renal ischaemia/reperfusion injury. Nephrol Dialysis Transplantation. 2010;25:2898–2908.
  • Hess J, Angel P, Schorpp-Kistner M. AP-1 subunits: quarrel and harmony among siblings. J Cell Sci. 2004;117:5965–5973.
  • Raivich G, Behrens A. Role of the AP-1 transcription factor c-Jun in developing, adult and injured brain. Prog Neurobiol. 2006;78:347–363.
  • Weston CR, Davis RJ. The JNK signal transduction pathway. Curr Opin Cell Biol. 2007;19:142–149.
  • Ventura -J-J. JNK potentiates TNF-stimulated necrosis by increasing the production of cytotoxic reactive oxygen species. Genes Dev. 2004;18:2905–2915.
  • Xu Y, Liu M, Peng B, et al. Protective effects of SP600125 on renal ischemia-reperfusion injury in rats. J Surg Res. 2011;169:e77–84.
  • Yao Q, Chen Y, Zhou X. The roles of microRNAs in epigenetic regulation. Curr Opin Chem Biol. 2019;51:11–17.
  • Sohel MH. Extracellular/circulating microRNAs: release mechanisms, functions and challenges. Achievements in the Life Sciences. 2016; 10:175–186.
  • Bär C, Thum T, de Gonzalo-calvo D. Circulating miRNAs as mediators in cell-to-cell communication. Epigenomics. 2019;11:111–113.
  • Boon RA, Vickers KC. Intercellular transport of microRNAs. Arterioscler Thromb Vasc Biol. 2013;33:186–192.
  • Zisoulis DG, Kai ZS, Chang RK, et al. Autoregulation of microRNA biogenesis by let-7 and argonaute. Nature. 2012;486:541–544.
  • Stavast C, Erkeland S. The non-canonical aspects of microRNAs: many roads to gene regulation. Cells. 2019;8:1465.
  • Xiao M, Li J, Li W, et al. MicroRNAs activate gene transcription epigenetically as an enhancer trigger. RNA Biol. 2017;14:1326–1334.
  • Weinberg MS, Morris KV. Transcriptional gene silencing in humans. Nucleic Acids Res. 2016;44:6505–6517.
  • L-c L. Chromatin remodeling by the small RNA machinery in mammalian cells. Epigenetics. 2014;9:45–52.
  • Hansen TB, Wiklund ED, Bramsen JB, et al. miRNA-dependent gene silencing involving Ago2-mediated cleavage of a circular antisense RNA: miRNA mediated cleavage of circular antisense RNA. EMBO J. 2011;30:45–52.
  • Liang H, Zhang J, Zen K, et al. Nuclear microRNAs and their unconventional role in regulating non-coding RNAs. Protein Cell. 2013;4:325–330.
  • Salmanidis M, Pillman K, Goodall G, et al. Direct transcriptional regulation by nuclear microRNAs. Int J Biochem Cell Biol. 2014;54:304–311.
  • Leucci E, Patella F, Waage J, et al. microRNA-9 targets the long non-coding RNA MALAT1 for degradation in the nucleus. Sci Rep. 2013;3:2535.
  • Chiyomaru T, Fukuhara S, Saini S, et al. Long non-coding RNA HOTAIR is targeted and regulated by miR-141 in human cancer cells. J Biol Chem. 2014;289:12550–12565.
  • Tam S, Tsao M-S, McPherson JD. Optimization of miRNA-seq data preprocessing. Brief Bioinform. 2015;16:950–963.
  • Shi Y, He M. Differential gene expression identified by RNA-Seq and qPCR in two sizes of pearl oyster (Pinctada fucata). Gene. 2014;538:313–322.
  • Wu AR, Neff NF, Kalisky T, et al. Quantitative assessment of single-cell RNA-sequencing methods. Nat Methods. 2014;11:12550–12556.
  • Griffith M, Griffith OL, Mwenifumbo J, et al. Alternative expression analysis by RNA sequencing. Nat Methods. 2010;7:843–847.
  • Everaert C, Luypaert M, Maag JLV, et al. Benchmarking of RNA-sequencing analysis workflows using whole-transcriptome RT-qPCR expression data. Sci Rep. 2017;7:1559.

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