MicroRNAs as non-invasive biomarkers of heart transplant rejection

European Heart Journal

Volumn 35, Issue 45, 2014, Pages 3194-3202

  Van Huyen, Jean Paul Duong ^a,b,c   Tible, Marion ^a,b   Gay, Arnaud ^d   Guillemain, Romain ^e   Aubert, Olivier ^a   Varnous, Shaida ^f   Iserin, Franck ^c   Rouvier, Philippe ^f   François, Arnaud ^d   Vernerey, Dewi ^a   Loyer, Xavier ^a   Leprince, Pascal ^f   Empana, Jean Philippe ^a   Bruneval, Patrick ^a,b,e   Loupy, Alexandre ^a,b   Jouven, Xavier ^a,b  

^a PARIS CARDIOVASCULAR RESEARCH CENTER   (France)

^b APHP   (France)

^c HÔPITAL NECKER ENFANTS MALADES   (France)

^d ROUEN UNIVERSITY HOSPITAL   (France)

^e HÔPITAL EUROPÉEN GEORGES POMPIDOU   (France)

^f ASSISTANCE PUBLIQUE HÔPITAUX DE PARIS   (France)

Author keywords

Biomarker; Heart transplantation; MicroRNA; Molecular medicine; Non invasive; Personalized medicine; Transplant rejection

Indexed keywords

AZATHIOPRINE; BIOLOGICAL MARKER; CALCINEURIN INHIBITOR; HLA ANTIBODY; MAMMALIAN TARGET OF RAPAMYCIN INHIBITOR; MICRORNA; MICRORNA 10A; MICRORNA 142 3P; MICRORNA 155; MICRORNA 21; MICRORNA 31; MICRORNA 451; MICRORNA 92A; MYCOPHENOLIC ACID; STEROID; UNCLASSIFIED DRUG;

AGE; AREA UNDER THE CURVE; ARTICLE; CARDIAC GRAFT REJECTION; COHORT ANALYSIS; CONTROLLED STUDY; DIAGNOSTIC TEST ACCURACY STUDY; ENDOTHELIUM; FEMALE; GENDER; GENE EXPRESSION; GRAFT RECIPIENT; HEART MUSCLE BIOPSY; HEART TRANSPLANTATION; HUMAN; HUMAN TISSUE; IMMUNOSUPPRESSIVE TREATMENT; INFLAMMATION; ISCHEMIC HEART DISEASE; MAJOR CLINICAL STUDY; MALE; ORGAN DONOR; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; RECEIVER OPERATING CHARACTERISTIC; RNA EXTRACTION; SEROLOGY; STEROID THERAPY; TISSUE SPECIFICITY; ADULT; AGED; ALLOGRAFT; ALLOTRANSPLANTATION; CLINICAL TRIAL; COMPARATIVE STUDY; GRAFT REJECTION; HEART DISEASES; METABOLISM; MIDDLE AGED; MULTICENTER STUDY; PERSONALIZED MEDICINE; RANDOMIZED CONTROLLED TRIAL;

ADULT; AGED; ALLOGRAFTS; BIOLOGICAL MARKERS; GRAFT REJECTION; HEART DISEASES; HEART TRANSPLANTATION; HUMANS; INDIVIDUALIZED MEDICINE; MALE; MICRORNAS; MIDDLE AGED; ROC CURVE; TRANSPLANTATION, HOMOLOGOUS;

EID: 84922149721     PISSN: 0195668X     EISSN: 15229645     Source Type: Journal    
DOI: 10.1093/eurheartj/ehu346     Document Type: Article

References (50)

1. Lund LH, Edwards LB, Kucheryavaya AY, Dipchand AI, Benden C, Christie JD, Dobbels F, Kirk R, Rahmel AO, Yusen RD, Stehlik J, International Society for H, LungT. The Registry of the International Society for Heart and Lung Transplantation: Thirtieth Official Adult Heart Transplant Report-2013; focus theme: age. J Heart Lung Transplant 2013;32:951-964.
2. Gradek WQ, D'Amico C, Smith AL, Vega D, Book WM. Routine surveillance endomyocardial biopsy continues to detect significant rejection late after heart transplantation. J Heart Lung Transplant 2001;20:497-502.
3. WuGW, Kobashigawa JA, Fishbein MC,Patel JK, Kittleson MM,Reed EF, Kiyosaki KK, Ardehali A. Asymptomatic antibody-mediated rejection after heart transplantation predicts poor outcomes. J Heart Lung Transplant 2009;28:417-422.
4. Loupy A, Cazes A, Guillemain R, Amrein C, Hedjoudje A, Tible M, Pezzella V, Fabiani JN, Suberbielle C, Nochy D, Hill GS, Empana JP, Jouven X, Bruneval P, Duong Van Huyen JP. Very late heart transplant rejection is associated with microvascular injury, complement deposition and progression to cardiac allograft vasculopathy. Am J Transplant 2011;11:1478-1487.
5. Kobashigawa JA. The future of heart transplantation. Am J Transplant 2012;12: 2875-2891.
6. Deng MC, Eisen HJ, Mehra MR, Billingham M, Marboe CC, Berry G, Kobashigawa J, Johnson FL, Starling RC, Murali S, Pauly DF, Baron H, Wohlgemuth JG, Woodward RN, Klingler TM,Walther D, Lal PG, Rosenberg S, Hunt S, Investigators C. Noninvasive discrimination of rejection in cardiac allograft recipients using gene expression profiling. Am J Transplant 2006;6:150-160.
7. Pham MX, Teuteberg JJ, Kfoury AG, Starling RC, Deng MC, Cappola TP, Kao A, Anderson AS, Cotts WG, Ewald GA, Baran DA, Bogaev RC, Elashoff B, Baron H, Yee J, Valantine HA, Group IS. Gene-expression profiling for rejection surveillance after cardiac transplantation. N Engl J Med 2010;362:1890-1900.
8. Pritchard CC, Cheng HH, Tewari M. MicroRNA profiling: approaches and considerations. Nat Rev Genet 2012;13:358-369.
9. Mendell JT, Olson EN. MicroRNAs in stress signaling and human disease. Cell 2012; 148:1172-1187.
10. Penzkofer D, Bonauer A, Fischer A, Tups A, Brandes RP, Zeiher AM, Dimmeler S. Phenotypic characterization of miR-92a2/2 mice reveals an important function of miR-92a in skeletal development. PLoS One 2014;9:e101153.
11. Porrello ER, Mahmoud AI, Simpson E, Johnson BA, Grinsfelder D, Canseco D, Mammen PP, Rothermel BA, Olson EN, Sadek HA. Regulation of neonatal and adult mammalian heart regeneration by the miR-15 family. Proc Natl Acad Sci USA 2013;110:187-192.
12. Jin C, Zhao Y, Yu L, Xu S, Fu G. MicroRNA-21 mediates the rapamycin-induced suppression of endothelial proliferation and migration. FEBS Lett 2013;587:378-385.
13. Fabbri M, Paone A, Calore F, Galli R, Gaudio E, Santhanam R, Lovat F, Fadda P, Mao C, Nuovo GJ, Zanesi N, Crawford M, Ozer GH, Wernicke D, Alder H, Caligiuri MA, Nana-Sinkam P, Perrotti D, Croce CM. MicroRNAs bind to Toll-like receptors to induce prometastatic inflammatory response. Proc Natl Acad Sci USA 2012;109: E2110-6.
14. Chen L, Wang Y, Pan Y, Zhang L, Shen C, Qin G, Ashraf M, Weintraub N, Ma G, Tang Y. Cardiac progenitor-derived exosomes protect ischemic myocardium from acute ischemia/reperfusion injury. Biochem Biophys Res Commun 2013;431: 566-571.
15. Sun D, Yu F, Ma Y, Zhao R, Chen X, Zhu J, ZhangCY, Chen J, Zhang J. MicroRNA-31 activates the RAS pathway and functions as an oncogenic MicroRNA in human colorectal cancer by repressing RAS p21 GTPase activating protein 1 (RASA1). J Biol Chem 2013;288:9508-9518.
16. Sun Y, Tawara I, Zhao M, Qin ZS, Toubai T, Mathewson N, Tamaki H, Nieves E, Chinnaiyan AM, Reddy P. Allogeneic T cell responses are regulated by a specific miRNA-mRNA network. J Clin Invest 2013;123:4739-4754.
17. Takahashi H, Kanno T, Nakayamada S, Hirahara K, Sciume G, Muljo SA, Kuchen S, Casellas R, Wei L, Kanno Y, O'Shea JJ. TGF-beta and retinoic acid induce the microRNA miR-10a, which targets Bcl-6 and constrains the plasticity of helper T cells. Nat Immunol 2012;13:587-595.
18. Trotta R, Chen L, Ciarlariello D, Josyula S, Mao C, Costinean S, Yu L, Butchar JP, Tridandapani S, Croce CM, CaligiuriMA. miR-155 regulates IFN-gamma production in natural killer cells. Blood 2012;119:3478-3485.
19. Anglicheau D, Sharma VK, Ding R, Hummel A, Snopkowski C, Dadhania D, Seshan SV, Suthanthiran M. MicroRNA expression profiles predictive of human renal allograft status. Proc Natl Acad Sci USA 2009;106:5330-5335.
20. Wei L, Wang M, Qu X, Mah A, Xiong X, Harris AG, Phillips LK, Martinez OM, Krams SM. Differential expression of microRNAs during allograft rejection. Am J Transplant 2012;12:1113-1123.
21. Stewart S, Winters GL, Fishbein MC, Tazelaar HD, Kobashigawa J, Abrams J, Andersen CB, Angelini A, Berry GJ, Burke MM, Demetris AJ, Hammond E, Itescu S, Marboe CC, McManus B, Reed EF, Reinsmoen NL, Rodriguez ER, Rose AG, Rose M, Suciu-Focia N, Zeevi A, Billingham ME. Revision of the 1990 working formulation for the standardization of nomenclature in the diagnosis of heart rejection. J Heart Lung Transplant 2005;24:1710-1720.
22. Berry GJ, Burke MM, Andersen C, Bruneval P, Fedrigo M, Fishbein MC, Goddard M, Hammond EH, Leone O, Marboe C, Miller D, Neil D, Rassl D, Revelo MP, Rice A, Rene Rodriguez E, Stewart S, Tan CD, Winters GL, West L, Mehra MR, Angelini A. The 2013 International Society for Heart and Lung Transplantation Working Formulation for the standardization of nomenclature in the pathologic diagnosis of antibody-mediated rejection in heart transplantation. J Heart Lung Transplant 2013;32:1147-1162.
23. Lefaucheur C, Loupy A, Vernerey D, Duong-Van-Huyen JP, Suberbielle C, Anglicheau D, Verine J, Beuscart T, Nochy D, Bruneval P, Charron D, Delahousse M, Empana JP, Hill GS, Glotz D, Legendre C, Jouven X. Antibodymediated vascular rejection of kidney allografts: a population-based study. Lancet 2013;381:313-319.
24. Loupy A, Lefaucheur C, Vernerey D, Prugger C, Duong van Huyen JP, Mooney N, Suberbielle C, Fremeaux-Bacchi V, Mejean A, Desgrandchamps F, Anglicheau D, Nochy D, Charron D, Empana JP, Delahousse M, Legendre C, Glotz D, Hill GS, Zeevi A, Jouven X. Complement-binding anti-HLA antibodies and kidney-Allograft survival. N Engl J Med 2013;369:1215-1226.
25. Danger R, Paul C, Giral M, Lavault A, Foucher Y, Degauque N, Pallier A, Durand M, Castagnet S, Duong Van Huyen JP, Delahousse M, Renaudin K, Soulillou JP, Brouard S. Expression of miR-142-5p in peripheral blood mononuclear cells from renal transplant patients with chronic antibody-mediated rejection. PLoS One 2013;8:e60702.
26. Danger R, Pallier A, Giral M, Martinez-Llordella M, Lozano JJ, Degauque N, Sanchez-Fueyo A, Soulillou JP, Brouard S. Upregulation of miR-142-3p in peripheral blood mononuclear cells of operationally tolerant patients with a renal transplant. J Am Soc Nephrol 2012;23:597-606.
27. Moldovan L, Batte KE, Trgovcich J, Wisler J, Marsh CB, PiperM. Methodological challenges in utilizing miRNAs as circulating biomarkers. J Cell Mol Med 2014;18: 371-390.
28. Qin B, Yang H, Xiao B. Role of microRNAs in endothelial inflammation and senescence. Mol Biol Rep 2012;39:4509-4518.
29. Fish JE, Srivastava D. MicroRNAs: opening a new vein in angiogenesis research. Sci Signal 2009;2:pe1.
30. Karunakaran D, Rayner KJ. MicroRNAs in cardiovascular health: from order to disorder. Endocrinology 2013;154:4000-4009.
31. Loyer X, Potteaux S, VionAC, Guerin CL, Boulkroun S, Rautou PE, Ramkhelawon B, Esposito B, Dalloz M, Paul JL, Julia P, Maccario J, Boulanger CM, Mallat Z, Tedgui A. Inhibition of microRNA-92a prevents endothelial dysfunction and atherosclerosis in mice. Circ Res 2014;114:434-443.
32. Gilad S, Meiri E, Yogev Y, Benjamin S, Lebanony D, Yerushalmi N, Benjamin H, Kushnir M, Cholakh H, Melamed N, Bentwich Z, Hod M, Goren Y, Chajut A. Serum microRNAs are promising novel biomarkers. PLoS One 2008;3:e3148.
33. Weber M, Baker MB, Moore JP, Searles CD. MiR-21 is induced in endothelial cells by shear stress and modulates apoptosis and eNOS activity. Biochem Biophys Res Commun 2010;393:643-648.
34. Ji X, Takahashi R, Hiura Y, Hirokawa G, Fukushima Y, Iwai N. Plasma miR-208 as a biomarker of myocardial injury. Clin Chem 2009;55:1944-1949.
35. Fang Y, Shi C, Manduchi E, Civelek M, Davies PF. MicroRNA-10a regulation of proinflammatory phenotype in athero-susceptible endothelium in vivo and in vitro. Proc Natl Acad Sci USA 2010;107:13450-5.
36. Lind EF, Ohashi PS. Mir-155, a central modulator of T-cell responses. Eur J Immunol 2014;44:11-15.
37. Sullivan RP, Fogel LA, Leong JW, Schneider SE,Wong R, Romee R, Thai TH, Sexl V, Matkovich SJ, DornGWII, French AR, Fehniger TA. MicroRNA-155 tunes both the threshold and extent ofNKcell activation via targeting of multiple signaling pathways. J Immunol 2013;191:5904-5913.
38. Feng Z, Xia Y, Zhang M, Zheng J. MicroRNA-155 regulates T cell proliferation through targeting GSK3beta in cardiac allograft rejection in a murine transplantation model. Cell Immunol 2013;281:141-149.
39. Sun X, Icli B, Wara AK, Belkin N, He S, Kobzik L, Hunninghake GM, Vera MP, Registry M, Blackwell TS, Baron RM, Feinberg MW. MicroRNA-181b regulates NF-kappaB-mediated vascular inflammation. J Clin Invest 2012;122:1973-1990.
40. Kelada S, Sethupathy P, OkoyeIS, Kistasis E, Czieso S, White SD, Chou D, Martens C, Ricklefs SM, Virtaneva K, Sturdevant DE, Porcella SF, Belkaid Y, Wynn TA, Wilson MS. miR-182 and miR-10a are key regulators of Treg specialisation and stability during Schistosome and Leishmania-Associated inflammation. PLoS Pathog 2013;9:e1003451.
41. Wang X, Zhu H, Zhang X, Liu Y, Chen J, Medvedovic M, Li H, Weiss MJ, Ren X, Fan GC. Loss of the miR-144/451 cluster impairs ischaemic preconditioningmediated cardioprotection by targeting Rac-1. Cardiovasc Res 2012;94:379-390.
42. HamburgMA, Collins FS. The path to personalized medicine.NEngl J Med 2010;363: 301-304.
43. Mengel M, Campbell P, Gebel H, Randhawa P, Rodriguez ER, Colvin R, Conway J, Hachem R, Halloran PF, Keshavjee S, Nickerson P, Murphey C, O'Leary J, Reeve J, Tinckam K, Reed EF. Precision diagnostics in transplantation: from bench to bedside. Am J Transplant 2013;13:562-568.
44. Sellares J, Reeve J, Loupy A, Mengel M, Sis B, Skene A, de Freitas DG, Kreepala C, Hidalgo LG, Famulski KS, Halloran PF. Molecular diagnosis of antibody-mediated rejection in human kidney transplants. Am J Transplant 2013;13:971-983.
45. Halloran PF, Pereira AB, Chang J, Matas A, Picton M, De Freitas D, Bromberg J, Seron D, Sellares J, Einecke G, Reeve J. Microarray diagnosis of antibody-mediated rejection in kidney transplant biopsies: an international prospective study (INTERCOM). Am J Transplant 2013;13:2865-2874.
46. Matignon M, Ding R, Dadhania DM, Mueller FB, Hartono C, Snopkowski C, Li C, Lee JR, Sjoberg D, Seshan SV, Sharma VK, Yang H, Nour B, Vickers AJ, Suthanthiran M, Muthukumar T. Urinary cell mRNA profiles and differential diagnosis of acute kidney graft dysfunction. J Am Soc Nephrol 2014;25:1586-1597.
47. Suthanthiran M, Schwartz JE, Ding R, Abecassis M, Dadhania D, Samstein B, Knechtle SJ, Friedewald J, Becker YT, Sharma VK, Williams NM, Chang CS, Hoang C, Muthukumar T, August P, Keslar KS, Fairchild RL, Hricik DE, Heeger PS, Han L, Liu J, Riggs M, Ikle DN, Bridges ND, Shaked A, Clinical Trials in Organ Transplantation 04 Study I. Urinary-cell mRNA profile and acute cellular rejection in kidney allografts. N Engl J Med 2013;369:20-31.
48. Urbich C, Kuehbacher A, Dimmeler S. Role of microRNAs in vascular diseases, inflammation, and angiogenesis. Cardiovasc Res 2008;79:581-588.
49. Suarez Y, Wang C, Manes TD, Pober JS. Cutting edge: TNF-induced microRNAs regulate TNF-induced expression of E-selectin and intercellular adhesion molecule-1 on human endothelial cells: feedback control of inflammation. J Immunol 2010;184:21-25.
50. Zhang L, Zhou M,WangY, HuangW, Qin G,Weintraub NL, TangY. miR-92a inhibits vascular smooth muscle cell apoptosis: role of the MKK4-JNK pathway. Apoptosis 2014;19:975-983.