Changes in phenotypic patterns of blood monocytes after kidney transplantation and during acute rejection

. 2021 Nov 29 ; 70 (5) : 709-721. [epub] 20210910

Jazyk angličtina Země Česko Médium print-electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid34505523

Peripheral blood monocytes, which serve as precursors for tissue macrophages and dendritic cells (DC), play a key role in the immune response to kidney allograft, reparation processes and homeostasis regulation. In this prospective study, we used multicolor flow cytometry to monitor the phenotypic patterns of peripheral monocytes in subjects with uncomplicated outcomes and those with acute rejection. We found a reciprocal increase in the proportion of "classical monocytes" (CD14+CD16-) along with a decline in pro-inflammatory "intermediary" (CD14+CD16+) and "non-classical" (CD14lowCD16+) monocytes in subjects with normal outcomes. In subjects with acute rejection, we observed no reduction in "intermediary" monocytes and no increase in "classical" monocytes. Patients with uncomplicated outcomes exhibited downregulated HLA-DR in all three monocyte subpopulations. However, non-classical monocytes were unaffected in subjects with acute rejection. Expression of CD47 was downregulated after transplantation, while patients with antibody-mediated rejection and donor-specific antibodies showed higher pre-transplant values. In monocytes isolated at the time of biopsy, CD47 expression was higher in individuals with acute rejection compared to patients with normal outcomes one year post-transplant. Expression of CD209 (DC-SIGN) and the proportion of CD163+CD206+ subpopulations were upregulated during the first week after kidney transplantation. CD209 was also upregulated in samples taken on the day of biopsy confirming acute rejection. Our data demonstrate that kidney allograft transplantation is associated with phenotypic changes in peripheral blood monocytes during acute rejection.

Zobrazit více v PubMed

APPEL SH, WELLHAUSEN SR, MONTGOMERY R, DEWEESE RC, POLK HC., JR Experimental and clinical significance of endotoxin-dependent HLA-DR expression on monocytes. J Surgical Res. 1989;47:39–44. doi: 10.1016/0022-4804(89)90045-0. PubMed DOI

AZAD AK, RAJARAM MV, SCHLESINGER LS. Exploitation of the macrophage mannose receptor (CD206) in infectious disease diagnostics and therapeutics. J Cytol Mol Biol. 2014;1:1000003. doi: 10.13188/2325-4653.1000003. PubMed DOI PMC

BENNER B, SCARBERRY L, SUAREZ-KELLY LP, DUGGAN MC, CAMPBELL AR, SMITH E, LAPURGA G, JIANG K, BUTCHAR JP, TRIDANDAPANI S, HOWARD JH, BAIOCCHI RA, MACE TA, CARSON WE., 3RD Generation of monocyte-derived tumor-associated macrophages using tumor-conditioned media provides a novel method to study tumor-associated macrophages in vitro. J Immunother Cancer. 2019;7:140. doi: 10.1186/s40425-019-0622-0. PubMed DOI PMC

BRUNIALTI MK, SANTOS MC, RIGATO O, MACHADO FR, SILVA E, SALOMAO R. Increased percentages of T helper cells producing IL-17 and monocytes expressing markers of alternative activation in patients with sepsis. PLoS One. 2012;7:e37393. doi: 10.1371/journal.pone.0037393. PubMed DOI PMC

BULLWINKEL J, LUDEMANN A, DEBARRY J, SINGH PB. Epigenotype switching at the CD14 and CD209 genes during differentiation of human monocytes to dendritic cells. Epigenetics. 2011;6:45–51. doi: 10.4161/epi.6.1.13314. PubMed DOI

CHO J-H, YOON Y-D, JANG HM, KWON E, JUNG H-Y, CHOI J-Y, PARK S-H, KIM Y-L, KIM HK, HUH S, WON D-I, KIM C-D. Immunologic Monitoring of T-lymphocyte Subsets and Hla-Dr-Positive Monocytes in Kidney Transplant Recipients: A Prospective, Observational Cohort Study. Medicine (Baltimore) 2015;94:e1902. doi: 10.1097/MD.0000000000001902. PubMed DOI PMC

CHOMETON TQ, SIQUEIRA MDS, SANT ANNA JC, ALMEIDA MR, GANDINI M, MARTINS De ALMEIDA NOGUEIRA AC, ANTAS PRZ. A protocol for rapid monocyte isolation and generation of singular human monocyte-derived dendritic cells. PLoS One. 2020;15:e0231132. doi: 10.1371/journal.pone.0231132. PubMed DOI PMC

CURNOVA L, MEZEROVA K, SVACHOVA V, FIALOVA M, NOVOTNY M, CECRDLOVA E, VIKLICKY O, STRIZ I. Up-regulation of CD163 expression in subpopulations of blood monocytes after kidney allograft transplantation. Physiol Res. 2020;69:885–896. doi: 10.33549/physiolres.934531. PubMed DOI PMC

DELUCE-KAKWATA-NKOR N, LAMENDOUR L, CHABOT V, HERAUD A, IVANOVIC Z, HALARY F, DEHAUT F, VELGE-ROUSSEL F. Differentiation of human dendritic cell subsets for immune tolerance induction. Transfus Clin Biol. 2018;25:90–95. doi: 10.1016/j.tracli.2017.08.002. PubMed DOI

GAINARU G, PAPADOPOULOS A, TSANGARIS I, LADA M, GIAMARELLOS-BOURBOULIS EJ, PISTIKI A. Increases in inflammatory and CD14(dim)/CD16(pos)/CD45(pos) patrolling monocytes in sepsis: correlation with final outcome. Crit Care. 2018;22:56. doi: 10.1186/s13054-018-1977-1. PubMed DOI PMC

GILL J, DONG J, ROSE C, GILL JS. The risk of allograft failure and the survival benefit of kidney transplantation are complicated by delayed graft function. Kidney Int. 2016;89:1331–1336. doi: 10.1016/j.kint.2016.01.028. PubMed DOI

GORDON S, TAYLOR PR. Monocyte and macrophage heterogeneity. Nat Rev Immunol. 2005;5:953–964. doi: 10.1038/nri1733. PubMed DOI

GOSSEZ M, RIMMELE T, ANDRIEU T, DEBORD S, BAYLE F, MALCUS C, POITEVIN-LATER F, MONNERET G, VENET F. Proof of concept study of mass cytometry in septic shock patients reveals novel immune alterations. Sci Rep. 2018;8:17296. doi: 10.1038/s41598-018-35932-0. PubMed DOI PMC

GRANELLI-PIPERNO A, PRITSKER A, PACK M, SHIMELIOVICH I, ARRIGHI JF, PARK CG, TRUMPFHELLER C, PIGUET V, MORAN TM, STEINMAN RM. Dendritic cell-specific intercellular adhesion molecule 3-grabbing nonintegrin/CD209 is abundant on macrophages in the normal human lymph node and is not required for dendritic cell stimulation of the mixed leukocyte reaction. J Immunol. 2005;175:4265–4273. doi: 10.4049/jimmunol.175.7.4265. PubMed DOI PMC

GUILLÉN-GÓMEZ E, GUIRADO L, BELMONTE X, MADERUELO A, SANTÍN S, JUAREZ C, ARS E, FACUNDO C, BALLARÍN JA, VIDAL S, DÍAZ-ENCARNACIÓN MM. Monocyte implication in renal allograft dysfunction. Clin Exp Immunol. 2014;175:323–331. doi: 10.1111/cei.12228. PubMed DOI PMC

HAAS M, LOUPY A, LEFAUCHEUR C, ROUFOSSE C, GLOTZ D, SERON D, NANKIVELL BJ, HALLORAN PF, COLVIN RB, AKALIN E, ALACHKAR N, BAGNASCO S, BOUATOU Y, BECKER JU, CORNELL LD, DUONG Van HUYEN JP, GIBSON IW, KRAUS ES, MANNON RB, NAESENS M, 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. PubMed DOI PMC

HOU J, WANG X, ZHANG M, WANG M, GAO P, JIANG Y. Circulating CD14(+)CD163(+)CD209(+) M2-like monocytes are associated with the severity of infection in Helicobacter pylori-positive patients. Mol Immunol. 2019;108:13–22. doi: 10.1016/j.molimm.2019.01.017. PubMed DOI

HOU J, ZHANG M, DING Y, WANG X, LI T, GAO P, JIANG Y. Circulating CD14(+)CD163(+)CD206(+) M2 monocytes are increased in patients with early stage of idiopathic membranous nephropathy. Mediators Inflamm. 2018;2018:5270657. doi: 10.1155/2018/5270657. PubMed DOI PMC

HU W, LIN J, LIAN X, YU F, LIU W, WU Y, FANG X, LIANG X, HAO W. M2a and M2b macrophages predominate in kidney tissues and M2 subpopulations were associated with the severity of disease of IgAN patients. Clin Immunol. 2019;205:8–15. doi: 10.1016/j.clim.2019.05.005. PubMed DOI

KAWAMURA S, OHTEKI T. Monopoiesis in humans and mice. Int Immunol. 2018;30:503–509. doi: 10.1093/intimm/dxy063. PubMed DOI

LIN Y, MANNING PT, JIA J, GAUT JP, XIAO Z, CAPOCCIA BJ, CHEN C-C, HIEBSCH RR, UPADHYA G, MOHANAKUMAR T, FRAZIER WA, CHAPMAN WC. CD47 blockade reduces ischemia-reperfusion injury and improves outcomes in a rat kidney transplant model. Transplantation. 2014;98:394–401. doi: 10.1097/TP.0000000000000252. PubMed DOI PMC

MANIECKI MB, MOLLER HJ, MOESTRUP SK, MOLLER BK. CD163 positive subsets of blood dendritic cells: the scavenging macrophage receptors CD163 and CD91 are coexpressed on human dendritic cells and monocytes. Immunobiology. 2006;211:407–417. doi: 10.1016/j.imbio.2006.05.019. PubMed DOI

MAYER A, LEE S, JUNG F, GRUTZ G, LENDLEIN A, HIEBL B. CD14+ CD163+ IL-10+ monocytes/macrophages: Pro-angiogenic and non pro-inflammatory isolation, enrichment and long-term secretion profile. Clin Hemorheol Microcirc. 2010;46:217–223. doi: 10.3233/CH-2010-1348. PubMed DOI

MENGOS AE, GASTINEAU DA, GUSTAFSON MP. The CD14(+)HLA-DR(lo/neg) Monocyte. An immunosuppressive phenotype that restrains responses to cancer immunotherapy. Front Immunol. 2019;10:1147. doi: 10.3389/fimmu.2019.01147. PubMed DOI PMC

MENON MC, HEEGER PS. Donor SIRP-alpha polymorphisms: widening the innate-to-adaptive continuum in allograft rejection. Kidney Int. 2017;92:1305–1308. doi: 10.1016/j.kint.2017.10.006. PubMed DOI

MERINO A, BUENDIA P, MARTIN-MALO A, ALJAMA P, RAMIREZ R, CARRACEDO J. Senescent CD14+CD16+ monocytes exhibit proinflammatory and proatherosclerotic activity. J Immunol. 2011;186:1809–1815. doi: 10.4049/jimmunol.1001866. PubMed DOI

MIN D, BROOKS B, WONG J, AAMIDOR S, SEEHOO R, SUTANTO S, HARRISBERG B, YUE DK, TWIGG SM, McLENNAN SV. Monocyte CD163 is altered in association with diabetic complications: possible protective role. J Leukoc Biol. 2016;100:1375–1383. doi: 10.1189/jlb.3A1015-461RR. PubMed DOI

MONNERET G, VENET F. Sepsis-induced immune alterations monitoring by flow cytometry as a promising tool for individualized therapy. Cytometry B Clin Cytom. 2016;90:376–386. doi: 10.1002/cyto.b.21270. PubMed DOI

OLDENBORG PA. CD47: A cell surface glycoprotein which regulates multiple functions of hematopoietic cells in health and disease. ISRN Hematol. 2013;2013:614619. doi: 10.1155/2013/614619. PubMed DOI PMC

PASSOS LS, GAZZINELLI-GUIMARAES PH, OLIVEIRA MENDES TA, GUIMARAES AC, SILVEIRA LEMOS DD, RICCI ND, GONCALVES R, BARTHOLOMEU DC, FUJIWARA RT, BUENO LL. Regulatory monocytes in helminth infections: insights from the modulation during human hookworm infection. BMC Infect Dis. 2017;17:253. doi: 10.1186/s12879-017-2366-0. PubMed DOI PMC

PENGAM S, DURAND J, USAL C, GAUTTIER V, DILEK N, MARTINET B, DAGUIN V, MARY C, THEPENIER V, TEPPAZ G, RENAUDIN K, BLANCHO G, VANHOVE N, POIRIER N. SIRPalpha/CD47 axis controls the maintenance of transplant tolerance sustained by myeloid-derived suppressor cells. Am J Transplant. 2019;19:3263–3275. doi: 10.1111/ajt.15497. PubMed DOI

RAVENHILL BJ, SODAY L, HOUGHTON J, ANTROBUS R, WEEKES MP. Comprehensive cell surface proteomics defines markers of classical, intermediate and non-classical monocytes. Sci Rep. 2020;10:4560. doi: 10.1038/s41598-020-61356-w. PubMed DOI PMC

REINKE P, VOLK HD. Diagnostic and predictive value of an immune monitoring program for complications after kidney transplantation. Urol Int. 1992;49:69–75. doi: 10.1159/000282398. PubMed DOI

ROGACEV KS, ZAWADA AM, HUNDSDORFER J, ACHENBACH M, HELD G, FLISER D, HEINE GH. Immunosuppression and monocyte subsets. Nephrol Dial Transplant. 2015;30:143–153. doi: 10.1093/ndt/gfu315. PubMed DOI

SEKERKOVA A, KREPSOVA E, BRABCOVA E, SLATINSKA J, VIKLICKY O, LANSKA V, STRIZ I. CD14+CD16+ and CD14+CD163+ monocyte subpopulations in kidney allograft transplantation. BMC Immunol. 2014;15:4. doi: 10.1186/1471-2172-15-4. PubMed DOI PMC

STRIZOVA Z, VACHTENHEIM J, JR, SNAJDAUF M, LISCHKE R, BARTUNKOVA J, SMRZ D. Tumoral and paratumoral NK cells and CD8(+) T cells of esophageal carcinoma patients express high levels of CD47. Sci Rep. 2020;10:13936. doi: 10.1038/s41598-020-70771-y. PubMed DOI PMC

STURGE J, TODD SK, KOGIANNI G, McCARTHY A, ISACKE CM. Mannose receptor regulation of macrophage cell migration. J Leukoc Biol. 2007;82:585–593. doi: 10.1189/jlb.0107053. PubMed DOI

TARIQUE AA, LOGAN J, THOMAS E, HOLT PG, SLY PD, FANTINO E. Phenotypic, functional, and plasticity features of classical and alternatively activated human macrophages. Am J Respir Cell Mol Biol. 2015;53:676–688. doi: 10.1165/rcmb.2015-0012OC. PubMed DOI

ULRICH C, HEINE GH, GERHART MK, KOHLER H, GIRNDT M. Proinflammatory CD14+CD16+ monocytes are associated with subclinical atherosclerosis in renal transplant patients. Am J Transplant. 2008;8:103–110. doi: 10.1111/j.1600-6143.2007.02035.x. PubMed DOI

Van den BERK JM, OLDENBURGER RH, Van den BERG AP, KLOMPMAKER IJ, MESANDER G, Van SON WJ, Van der BIJ W, SLOOF MJ, THE TH. Low HLA-DR expression on monocytes as a prognostic marker for bacterial sepsis after liver transplantation. Transplantation. 1997;63:1846–1848. doi: 10.1097/00007890-199706270-00026. PubMed DOI

Van den BOSCH TPP, HILBRANDS LB, KRAAIJEVELD R, LITJENS NHR, REZAEE F, NIEBOER D, STEYERBERG EW, Van GESTEL JA, ROELEN DL, CLAHSEN-Van GRONINGEN MC, BAAN CC, ROWSHANI AT. Pretransplant numbers of CD16(+) Monocytes as a novel biomarker to predict acute rejection after kidney transplantation: A pilot study. Am J Transplant. 2017;17:2659–2667. doi: 10.1111/ajt.14280. PubMed DOI

VEILLETTE A, CHEN J. SIRPalpha-CD47 Immune checkpoint blockade in anticancer therapy. Trends Immunol. 2018;39:173–184. doi: 10.1016/j.it.2017.12.005. PubMed DOI

VEREYKEN EJ, KRAAIJ MD, BAAN CC, REZAEE F, WEIMAR W, WOOD KJ, LEENEN PJ, ROWSHANI AT. A shift towards pro-inflammatory CD16+ monocyte subsets with preserved cytokine production potential after kidney transplantation. PLoS One. 2013;8:e70152. doi: 10.1371/journal.pone.0070152. PubMed DOI PMC

WANG GQ, ZHANG Y, WU HQ, ZHANG WW, ZHANG J, WANG GY, XIAO SC, XIA ZF. Reduction of CD47 on monocytes correlates with MODS in burn patients. Burns. 2011;37:94–98. doi: 10.1016/j.burns.2010.04.007. PubMed DOI

WOHLFAHRTOVA M, TYCOVA I, HONSOVA E, LODEREROVA A, VIKLICKY O. Molecular patterns of subclinical and clinical rejection of kidney allograft: quantity matters. Kidney Blood Press Res. 2015;40:244–257. doi: 10.1159/000368500. PubMed DOI

XU M, WANG X, BANAN B, CHIRUMBOLE DL, GARCIA-AROZ S, BALAKRISHNAN A, NAYAK DK, ZHANG Z, JIA J, UPADHYA GA, GAUT JP, HIEBSCH R, MANNING PT, WU N, LIN Y, CHAPMAN WC. Anti-CD47 monoclonal antibody therapy reduces ischemia-reperfusion injury of renal allografts in a porcine model of donation after cardiac death. Am J Transplant. 2018;18:855–867. doi: 10.1111/ajt.14567. PubMed DOI PMC

XUE D, HE X, ZHOU C, XU X, XU R, XU N. Correlation between CD14+CD16++ monocytes in peripheral blood and hypertriglyceridemia after allograft renal transplantation. Transplant Proc. 2013;45:3279–3283. doi: 10.1016/j.transproceed.2013.08.022. PubMed DOI

YURYEVA K, SALTYKOVA I, OGORODOVA L, KIRILLOVA N, KULIKOV E, KOROTKAYA E, IAKOVLEVA Y, FEOKTISTOV I, SAZONOV, RYZHOV S. Expression of adenosine receptors in monocytes from patients with bronchial asthma. Biochem Biophy Res Commun. 2015;464:1314–1320. doi: 10.1016/j.bbrc.2015.07.141. PubMed DOI PMC

ZHAO D, ABOU-DAYA KI, DAI H, OBERBARNSCHEIDT MH, LI XC, LAKKIS FG. Innate allorecognition and memory in transplantation. Front Immunol. 2020;11:918. doi: 10.3389/fimmu.2020.00918. PubMed DOI PMC

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...