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Frontiers of Medicine

ISSN 2095-0217

ISSN 2095-0225(Online)

CN 11-5983/R

Postal Subscription Code 80-967

2018 Impact Factor: 1.847

Front. Med.    2019, Vol. 13 Issue (3) : 298-313    https://doi.org/10.1007/s11684-018-0636-x
REVIEW
HLA and lung transplantation
Liya Ju1(), Caroline Suberbielle2, Xiaofan Li3, Nuala Mooney3,4, Dominique Charron1,2,4,5
1. HLA et Medecine, “Jean Dausset” Laboratory Network, Hôpital Saint-Louis, Paris, France
2. Laboratoire Histocompatibilité, Hôpital Saint-Louis, Paris, France
3. INSERM U1160, Hôpital Saint-Louis, Université Paris Diderot, Sorbonne Paris Cité, France
4. Labex Transplantex, Strasbourg, France
5. Shanghai Jiao Tong University School of Medicine, Shanghai 200025, China
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Abstract

Lung transplantation is increasingly practiced for patients with end-stage lung disease. The successful outcome of solid organ transplantation today is severely impeded by the production of alloantibodies, mainly directed against the protein products of the HLA complex of the organ donor. While the association between antibody mediated rejection and allograft damage has been well established in renal and heart transplantation, it has not yet been well characterized in lung transplantation. This review addresses the question of HLA matching in lung transplantation and current knowledge of the allogenicity of different HLA class I and II antigens. The role of the antibody mediated immune response is discussed as well as the importance of pre-transplant or de novo post-transplant circulating antibodies. Finally, potential mechanisms, which may act individually or in combination, of antibody mediated damage to solid organ transplants are considered.

Keywords human leukocyte antigen class I and II      lung transplantation      mismatch      obliterans bronchiolitis      alloantibody      antibody mediated rejection     
Corresponding Authors: Liya Ju   
Just Accepted Date: 10 May 2018   Online First Date: 05 July 2018    Issue Date: 05 June 2019
 Cite this article:   
Liya Ju,Caroline Suberbielle,Xiaofan Li, et al. HLA and lung transplantation[J]. Front. Med., 2019, 13(3): 298-313.
 URL:  
http://academic.hep.com.cn/fmd/EN/10.1007/s11684-018-0636-x
http://academic.hep.com.cn/fmd/EN/Y2019/V13/I3/298
HLA Loci Clinical outcome References
HLA-A, -B and-DR
MM≥4
Poor patient survival
Poor graft survival
Idiopathic pulmonary fibrosis
Obliterative bronchiolitis
[8,9,12,13]
[7]
[13]
[13,14]
HLA-A
MM≥1
Obliterative bronchiolitis
Poor graft survival
Poor patient survival
[15,16,18]
[17]
[9,12,18,19]
HLA-B
MM≥1
Poor graft survival
Obliterative bronchiolitis
Bronchopulmonary sequestration
Acute rejection
[7]
[17,19]
[13,14]
[9,20]
HLA-DR
MM≥1
Obliterative bronchiolitis
Poor graft survival
Poor patient survival
[20]
[2123]
[13]
Other loci (HLA-C, HLA-DQ)
MM≥1
Poor graft survival [24]
Tab.1  Effect of HLA mismatch (MM) on clinical outcome after lung transplantation
Fig.1  Presence of pre-existing anti HLA antibodies is a key factor in acute rejection after lung transplantation. The analysis of pre-existing anti-HLA antibodies is highly recommended before lung transplantation.
Methods Cross-match Screening Sensitivity Comment
CDC Yes Yes + Requires donor cells
FC Yes Yes ++ Requires donor cells
ELISA No Yes ++ Can be generic and specific
LUM No Yes +++/++ Can be generic and phenotypic
LUM SAB No Yes +++ Comprehensive allele specification
PRA No Yes ++ Generic test only
Tab.2  Testing methods of HLA antibodies in lung transplantation
Fig.2  De novo HLA-class I and-class II donor specific antibodies in the clinical outcome after lung transplantation. Both de novo DSA anti class I and class II can induce the poor survival of lung transplantation. De novo HLA-DQ DSA are more frequent than HLA-DR DSA.
Fig.3  Proposed mechanisms of anti HLA antibodies inducing lung rejection. Antibodies binding to “cells” can harm the allograft by several mechanisms: direct signaling in endothelial/epithelial cells may lead to increased recruitment of innate cells and/or leukocyte activation following increased production of soluble factors (and potentially by activation of adhesion molecules).
MFI≥500 Positive threshold
MFI= 500–2000 Weak
MFI= 2000– 8000* Moderate
MFI≥8000 Strong
* MFI≥5000 is considered as being clinically significant and a trigger for treatment [102].
Tab.3  Mean fluorescent intensity (MFI) of HLA-DSA in lung transplantation
Recommendations for lung transplantation
✓ Systematic testing of pre-existing anti HLA antibody in varity list of patients
✓ HLA typing during or after LTX to obtain the degree of mismatches in order to predict the clinical outcome risks
✓ Regularity detection of HLA antibody level of dnDSA could be outcome indicator
✓ Anti-DQ dnDSA may be biomarker of CLAD, BOS and AMR
Tab.4  Recommendations for lung transplantation
1 RD Yusen, LB Edwards, AY Kucheryavaya, C Benden, AI Dipchand, F Dobbels, SB Goldfarb, BJ Levvey, LH Lund, B Meiser, J; International Society for Heart and Lung Transplantation Stehlik. The registry of the International Society for Heart and Lung Transplantation: thirty-first adult lung and heart-lung transplant report—2014; focus theme: retransplantation. J Heart Lung Transplant 2014; 33(10): 1009–1024
https://doi.org/10.1016/j.healun.2014.08.004 pmid: 25242125
2 Organ Procurement and Transplantation Network (OPTN) and Scientific Registry of Transplant Recipients(SRTR). OPTN/SRTR 2010 Annual Data Report. Rockville, MD: Department of Health and Human Services, Health Resources and Services Administration, Healthcare Systems Bureau, Division of Transplantation, 2011
3 DJ Levine, AR Glanville, C Aboyoun, J Belperio, C Benden, GJ Berry, R Hachem, D Hayes Jr, D Neil, NL Reinsmoen, LD Snyder, S Sweet, D Tyan, G Verleden, G Westall, RD Yusen, M Zamora, A Zeevi. Antibody-mediated rejection of the lung: a consensus report of the International Society for Heart and Lung Transplantation. J Heart Lung Transplant 2016; 35(4): 397–406
https://doi.org/10.1016/j.healun.2016.01.1223 pmid: 27044531
4 W McManigle, EN Pavlisko, T Martinu. Acute cellular and antibody-mediated allograft rejection. Semin Respir Crit Care Med 2013; 34(3): 320–335
https://doi.org/10.1055/s-0033-1348471 pmid: 23821507
5 C Auffray, D Charron, L Hood. Predictive, preventive, personalized and participatory medicine: back to the future. Genome Med 2010; 2(8): 57
https://doi.org/10.1186/gm178 pmid: 20804580
6 J Robinson, JA Halliwell, JH Hayhurst, P Flicek, P Parham, SGE Marsh. The IPD and IMGT/HLA database: allele variant databases. Nucleic Acids Res 2015;43(Database issue):D423–431 doi: 10.1093/nar/gku1161
7 W Wisser, T Wekerle, G Zlabinger, O Senbaclavaci, A Zuckermann, W Klepetko, E Wolner. Influence of human leukocyte antigen matching on long-term outcome after lung transplantation. J Heart Lung Transplant 1996; 15(12): 1209–1216
pmid: 8981206
8 JMA Smits, BJA Mertens, HC Van Houwelingen, A Haverich, GG Persijn, G Laufer. Predictors of lung transplant survival in eurotransplant. Am J Transplant 2003; 3(11): 1400–1406
https://doi.org/10.1046/j.1600-6143.2003.00231.X pmid: 14525601
9 MA Quantz, LE Bennett, DM Meyer, RJ Novick. Does human leukocyte antigen matching influence the outcome of lung transplantation? An analysis of 3,549 lung transplantations. J Heart Lung Transplant 2000; 19(5): 473–479
https://doi.org/10.1016/S1053-2498(00)00081-4 pmid: 10808155
10 JY Wong, B Tait, B Levvey, A Griffiths, DS Esmore, GI Snell, TJ Williams, TC Kotsimbos. Epstein-Barr virus primary mismatching and HLA matching: key risk factors for post lung transplant lymphoproliferative disease. Transplantation 2004; 78(2): 205–210
https://doi.org/10.1097/01.TP.0000128611.71038.0C pmid: 15280679
11 NA Bakker , GW van Imhoff, EA Verschuuren, WJ van Son, JJ van der Heide, SP Lems , NJ Veeger, PM Kluin , HC Kluin-Nelemans, BG Hepkema . HLA antigens and post renal transplant lymphoproliferative disease: HLA-B matching is critical. Transplantation 2005; 80(5):595–599
pmid: 16177631
12 G Opelz, C Süsal, A Ruhenstroth, B Döhler. Impact of HLA compatibility on lung transplant survival and evidence for an HLA restriction phenomenon: a collaborative transplant study report. Transplantation 2010; 90(8): 912–917
https://doi.org/10.1097/TP.0b013e3181f2c981 pmid: 20808265
13 D Jr Hayes, BA Whitson, SN Ghadiali, JD Tobias, HM Mansour, SM Black. Influence of HLA mismatching on survival in lung transplantation. Lung 2015; 193(5): 789–797
https://doi.org/10.1007/s00408-015-9768-9 pmid: 26220289
14 D Jr Hayes, SM Black, JD Tobias, BT Kopp, SE Kirkby, HM Mansour, BA Whitson. Influence of human leukocyte antigen mismatching on bronchiolitis obliterans syndrome in lung transplantation. J Heart Lung Transplant. 2016; 35(2):186–194
https://doi.org/10.1016/j.healun.2015.08.022
15 AL Harjula, JC Baldwin, AR Glanville, H Tazelaar, PE Oyer, EB Stinson, NE Shumway. Human leukocyte antigen compatibility in heart-lung transplantation. J Heart Transplant 1987; 6(3): 162–166
pmid: 3116183
16 S Sundaresan, T Mohanakumar, MA Smith, EP Trulock, J Lynch, D Phelan, JD Cooper, GA Patterson. HLA-A locus mismatches and development of antibodies to HLA after lung transplantation correlate with the development of bronchiolitis obliterans syndrome. Transplantation 1998; 65(5): 648–653
https://doi.org/10.1097/00007890-199803150-00008 pmid: 9521198
17 O Brugière, G Thabut, C Suberbielle, M Reynaud-Gaubert, P Thomas, C Pison, C Saint Raymond, JF Mornex, M Bertocchi, C Dromer, JF Velly, M Stern, B Philippe, G Dauriat, G Biondi, Y Castier, M Fournier. Relative impact of human leukocyte antigen mismatching and graft ischemic time after lung transplantation. J Heart Lung Transplant 2008; 27(6): 628–634
https://doi.org/10.1016/j.healun.2008.02.013 pmid: 18503962
18 M Peltz, L Bennett Edwards, ME Jessen, F Torres, DM Meyer. Impact of HLA class I and class II mismatching on lung transplant recipient mortality, rejection, and bronchiolitis obliterans. J Heart Lung Transplant 2006; 25(suppl): S112
https://doi.org/10.1016/j.healun.2005.11.205
19 W Chalermskulrat, IP Neuringer, JL Schmitz, DJ Catellier, MJ Gurka, SH Randell, RM Aris. Human leukocyte antigen mismatches predispose to the severity of bronchiolitis obliterans syndrome after lung transplantation. Chest 2003; 123(6): 1825–1831
https://doi.org/10.1378/chest.123.6.1825 pmid: 12796156
20 LL Schulman, AD Weinberg, C McGregor, ME Galantowicz, NM Suciu-Foca, S Itescu. Mismatches at the HLA-DR and HLA-B loci are risk factors for acute rejection after lung transplantation. Am J Respir Crit Care Med 1998; 157(6 Pt 1): 1833–1837
https://doi.org/10.1164/ajrccm.157.6.9707007 pmid: 9620914
21 Y Iwaki, Y Yoshida, B Griffith. The HLA matching effect in lung transplantation. Transplantation 1993; 56(6): 1528–1564
https://doi.org/10.1097/00007890-199312000-00047 pmid: 8279029
22 RB Love, KC Meyer, LD Devito-Haynes, S Ulschmid, GE Leverson, W Van Der Bij, WJ De Boer, BG Hepkema, RD Cornwell, DS Woolley, WJ Burlingham. Effect of HLA-DR mismatch on lung transplant outcome. J Heart Lung Transplant 2001; 20(2): 177
https://doi.org/10.1016/S1053-2498(00)00356-9 pmid: 11250286
23 L Wan, DF Chen. The influence of HLA antigen mismatch and epitope mismathe on lung transplant survival: analysis of OPTN data after LAS allocation. Hum Immunol 2015; 76: 124–167
https://doi.org/10.1016/j.humimm.2015.07.174
24 RJ Butts, AJ Savage, PJ Nietert, M Kavarana, O Moussa, AL Burnette, AM Atz. Effect of human leukocyte antigen-C and-DQ matching on pediatric heart transplant graft survival. J Heart Lung Transplant 2014; 33(12): 1282–1287
https://doi.org/10.1016/j.healun.2014.07.014 pmid: 25128416
25 B Afzali, G Lombardi, RI Lechler. Pathways of major histocompatibility complex allorecognition. Curr Opin Organ Transplant 2008; 13(4): 438–444
https://doi.org/10.1097/MOT.0b013e328309ee31 pmid: 18685342
26 OB Herrera, D Golshayan, R Tibbott, F Salcido Ochoa, MJ James, FM Marelli-Berg, RI Lechler. A novel pathway of alloantigen presentation by dendritic cells. J Immunol 2004; 173(8): 4828–4837
https://doi.org/10.4049/jimmunol.173.8.4828 pmid: 15470023
27 RA Shilling, DS Wilkes. Immunobiology of chronic lung allograft dysfunction: new insights from the bench and beyond. Am J Transplant 2009; 9(8): 1714–1718
https://doi.org/10.1111/j.1600-6143.2009.02690.x pmid: 19519813
28 RR Hachem. Lung allograft rejection: diagnosis and management. CurrOpinOrgan Transplant 2009;14(5):477–482
https://doi.org/DOI: 10.1097/MOT.0b013e32832fb981
29 JS Pober, D Jane-wit, L Qin, G Tellides. Interacting mechanisms in the pathogenesis of cardiac allograft vasculopathy. Arterioscler Thromb Vasc Biol 2014; 34(8): 1609–1614
https://doi.org/10.1161/ATVBAHA.114.302818 pmid: 24903097
30 MM DeNicola, SS Weigt, JA Belperio, EF Reed, DJ Ross, WD Wallace. Pathologic findings in lung allografts with anti-HLA antibodies. J Heart Lung Transplant 2013; 32(3): 326–332
https://doi.org/10.1016/j.healun.2012.11.018 pmid: 23313559
31 J Visentin, A Chartier, L Massara, G Linares, G Guidicelli, E Blanchard, M Parrens, H Begueret, C Dromer, JL Taupin. Lung intragraft donor-specific antibodies as a risk factor for graft loss. J Heart Lung Transplant 2016; 35(12): 1418–1426
https://doi.org/10.1016/j.healun.2016.06.010 pmid: 27450460
32 R Hachem. Antibody-mediated lung transplant rejection. Curr Respir Care Rep 2012; 1(3): 157–161
https://doi.org/10.1007/s13665-012-0019-8 pmid: 23002428
33 2004 Annual Report of the U.S. Organ Procurement and Transplantation Network and the Scientific Registry of Transplant Recipients: Transplant Data 1994–2003. Department of Health and Human Services, Health Resources and Services Administration, Healthcare Systems Bureau, Division of Transplantation, Rockville, MD; United Network for Organ Sharing, Richmond, VA; University Renal Research and Education Association, Ann Arbor, MI
34 CL Lau, SM Palmer, KE Posther, DN Howell, NL Reinsmoen, HT Massey, VF Tapson, JJ Jaggers, TA D’Amico, RD Davis Jr. Influence of panel-reactive antibodies on posttransplant outcomes in lung transplant recipients. Ann Thorac Surg 2000; 69(5): 1520–1524
https://doi.org/10.1016/S0003-4975(00)01224-8 pmid: 10881834
35 AS Shah, L Nwakanma, C Simpkins, J Williams, DC Chang, JV Conte. Pretransplant panel reactive antibodies in human lung transplantation: an analysis of over 10,000 patients. Ann Thorac Surg 2008; 85(6): 1919–1924
https://doi.org/10.1016/j.athoracsur.2008.02.011 pmid: 18498795
36 AA Mangi, DP Mason, ER Nowicki, LH Batizy, SC Murthy, DJ Pidwell, RK Avery, KR McCurry, GB Pettersson, EH Blackstone. Predictors of acute rejection after lung transplantation. Ann Thorac Surg 2011; 91(6): 1754–1762
https://doi.org/10.1016/j.athoracsur.2011.01.076 pmid: 21536252
37 TO Hirche, C Knoop, H Hebestreit. Practical guidelines: lung transplantation in patients with cystic fibrosis. Pulm Med 2014; 2014:621342
38 JK Choi, J Kearns, HI Palevsky, KT Montone, LR Kaiser, CM Zmijewski, JE Tomaszewski. Hyperacute rejection of a pulmonary allograft. Immediate clinical and pathologic findings. Am J Respir Crit Care Med 1999; 160(3): 1015–1018
https://doi.org/10.1164/ajrccm.160.3.9706115 pmid: 10471633
39 AE Frost, CT Jammal, PT Cagle. Hyperacute rejection following lung transplantation. Chest 1996; 110(2): 559–562
https://doi.org/10.1378/chest.110.2.559 pmid: 8697867
40 HB Bittner, J Dunitz, M Hertz, MR 3rd Bolman, SJ Park. Hyperacute rejection in single lung transplantation—case report of successful management by means of plasmapheresis and antithymocyte globulin treatment. Transplantation 2001; 71(5): 649–651
https://doi.org/10.1097/00007890-200103150-00012 pmid: 11292295
41 E Masson, M Stern, J Chabod, C Thévenin, F Gonin, JM Rebibou, P Tiberghien. Hyperacute rejection after lung transplantation caused by undetected low-titer anti-HLA antibodies. J Heart Lung Transplant 2007; 26(6): 642–645
https://doi.org/10.1016/j.healun.2007.03.007 pmid: 17543791
42 A Loupy, C Lefaucheur, D Vernerey, C Prugger, JP Duong van Huyen, N Mooney, C Suberbielle, V Frémeaux-Bacchi, A Méjean, F Desgrandchamps, D Anglicheau, D Nochy, D Charron, JP Empana, M Delahousse, C Legendre, D Glotz, GS Hill, A Zeevi, X Jouven. Complement-binding anti-HLA antibodies and kidney-allograft survival. N Engl J Med 2013; 369(13): 1215–1226
https://doi.org/10.1056/NEJMoa1302506 pmid: 24066742
43 A Sicard, S Ducreux, M Rabeyrin, L Couzi, B McGregor, L Badet, JY Scoazec, T Bachelet, S Lepreux, J Visentin, P Merville, V Fremeaux-Bacchi, E Morelon, JL Taupin, V Dubois, O Thaunat. Detection of C3d-binding donor-specific anti-HLA antibodies at diagnosis of humoral rejection predicts renal graft loss. J Am Soc Nephrol 2015; 26(2): 457–467
https://doi.org/10.1681/ASN.2013101144 pmid: 25125383
44 AR Tambur, FH Claas. HLA epitopes as viewed by antibodies: what is it all about? Am J Transplant 2015; 15(5): 1148–1154
https://doi.org/10.1111/ajt.13192 pmid: 25708017
45 Q Zhang, JM Cecka, DW Gjertson, P Ge, ML Rose, JK Patel, A Ardehali, JA Kobashigawa, MC Fishbein, EF Reed. HLA and MICA: targets of antibody-mediated rejection in heart transplantation. Transplantation 2011; 91(10): 1153–1158
https://doi.org/10.1097/TP.0b013e3182157d60 pmid: 21544036
46 RR Hachem, RD Yusen, BF Meyers, AA Aloush, T Mohanakumar, GA Patterson, EP Trulock. Anti-human leukocyte antigen antibodies and preemptive antibody-directed therapy after lung transplantation. J Heart Lung Transplant 2010; 29(9): 973–980
https://doi.org/10.1016/j.healun.2010.05.006 pmid: 20558084
47 LJ Lobo, RM Aris, J Schmitz, IP Neuringer. Donor-specific antibodies are associated with antibody-mediated rejection, acute cellular rejection, bronchiolitis obliterans syndrome, and cystic fibrosis after lung transplantation. J Heart Lung Transplant 2013; 32(1): 70–77
https://doi.org/10.1016/j.healun.2012.10.007 pmid: 23260706
48 LD Snyder, Z Wang, DF Chen, NL Reinsmoen, CA Finlen-Copeland, WA Davis, DW Zaas, SM Palmer. Implications for human leukocyte antigen antibodies after lung transplantation: a 10-year experience in 441 patients. Chest 2013; 144(1): 226–233
https://doi.org/10.1378/chest.12-0587 pmid: 23328795
49 AL Girnita, KR McCurry, AT Iacono, R Duquesnoy, TE Corcoran, M Awad, KJ Spichty, SA Yousem, G Burckart, JH Dauber, BP Griffith, A Zeevi. HLA-specific antibodies are associated with high-grade and persistent-recurrent lung allograft acute rejection. J Heart Lung Transplant 2004; 23(10): 1135–1141
https://doi.org/10.1016/j.healun.2003.08.030 pmid: 15477106
50 SM Palmer, RD Davis, D Hadjiliadis, MI Hertz, DN Howell, FE Ward, K Savik, NL Reinsmoen. Development of an antibody specific to major histocompatibility antigens detectable by flow cytometry after lung transplant is associated with bronchiolitis obliterans syndrome. Transplantation 2002; 74(6): 799–804
https://doi.org/10.1097/00007890-200209270-00011 pmid: 12364858
51 EP Trulock, JD Christie, LB Edwards, MM Boucek, P Aurora, DO Taylor, F Dobbels, AO Rahmel, BM Keck, MI Hertz. Registry of the International Society for Heart and Lung Transplantation: twenty-fourth official adult lung and heart-lung transplantation report—2007. J Heart Lung Transplant 2007; 26(8): 782–795
https://doi.org/10.1016/j.healun.2007.06.003 pmid: 17692782
52 BD Tait, C Süsal, HM Gebel, PW Nickerson, AA Zachary, FH Claas, EF Reed, RA Bray, P Campbell, JR Chapman, PT Coates, RB Colvin, E Cozzi, II Doxiadis, SV Fuggle, J Gill, D Glotz, N Lachmann, T Mohanakumar, N Suciu-Foca, S Sumitran-Holgersson, K Tanabe, CJ Taylor, DB Tyan, A Webster, A Zeevi, G Opelz. Consensus guidelines on the testing and clinical management issues associated with HLA and non-HLA antibodies in transplantation. Transplantation 2013; 95(1): 19–47
https://doi.org/10.1097/TP.0b013e31827a19cc pmid: 23238534
53 A Jaramillo, MA Smith, D Phelan, S Sundaresan, EP Trulock, JP Lynch, JD Cooper, GA Patterson, T Mohanakumar. Development of ELISA-detected anti-HLA antibodies precedes the development of bronchiolitis obliterans syndrome and correlates with progressive decline in pulmonary function after lung transplantation. Transplantation 1999; 67(8): 1155–1161
https://doi.org/10.1097/00007890-199904270-00012 pmid: 10232567
54 AL Girnita, R Duquesnoy. YousemSA, Iacono AT, Corcoran TE, Buzoianu M, Johnson B, Spichty KJ, Dauber JH, Burckart G, Griffith BP, McCurry KR, Zeevi A. HLA-specific antibodies are risk factors forlymphocytic bronchiolitis and chronic lung allograft dysfunction. Am J Transplant 2005; 5: 131–138
https://doi.org/10.1111/j.1600-6143.2004.00650.x pmid: 15636621
55 F Cardarelli, M Pascual, N Tolkoff-Rubin, FL Delmonico, W Wong, DA Schoenfeld, H Zhang, AB Cosimi, SL Saidman. Prevalence and significance of anti-HLA and donor-specific antibodies long-term after renal transplantation. Transpl Int 2005; 18(5): 532–540
https://doi.org/10.1111/j.1432-2277.2005.00085.x pmid: 15819801
56 N Lachmann, PI Terasaki, C Schönemann. Donor-specific HLA antibodies in chronic renal allograft rejection: a prospective trial with a four-year follow-up. Clin Transpl 2006; 2006:171–199
pmid: 18365377
57 HG Otten, MC Verhaar, HP Borst, RJ Hené, AD van Zuilen. Pretransplant donor-specific HLA class-I and-II antibodies are associated with an increased risk for kidney graft failure. Am J Transplant 2012; 12(6): 1618–1623
https://doi.org/10.1111/j.1600-6143.2011.03985.x pmid: 22404993
58 SI Reznik, A Jaramillo, L Zhang, GA Patterson, JD Cooper, T Mohanakumar. Anti-HLA antibody binding to HLA class I molecules induces proliferation of airway epithelial cells: a potential mechanism for bronchiolitis obliterans syndrome. J Thorac Cardiovasc Surg 2000; 119(1): 39–45
https://doi.org/10.1016/S0022-5223(00)70215-7 pmid: 10612759
59 M Kim, KR Townsend, IG Wood, S Boukedes, I Guleria, S Gabardi, S El-Chemaly, PC Camp, AK Chandraker, EL Milford, HJ Goldberg. Impact of pretransplant anti-HLA antibodies on outcomes in lung transplant candidates. Am J Respir Crit Care Med 2014; 189(10): 1234–1239
https://doi.org/10.1164/rccm.201312-2160OC pmid: 24749479
60 C Wiebe, D Pochinco, TD Blydt-Hansen, J Ho, PE Birk, M Karpinski, A Goldberg, LJ Storsley, IW Gibson, DN Rush, PW Nickerson. Class II HLA epitope matching—a strategy to minimize de novo donor-specific antibody development and improve outcomes. Am J Transpl 2013; 13: 3114–3122
61 RB Colvin. Antibody-mediated renal allograft rejection: diagnosis and pathogenesis. J Am Soc Nephrol 2007; 18(4): 1046–1056
https://doi.org/10.1681/ASN.2007010073 pmid: 17360947
62 EY Song, YJ Lee, J Hyun, YS Kim, C Ahn, J Ha, SJ Kim, MH Park. Clinical relevance of pretransplant HLA class II donor-specific antibodies in renal transplantation patients with negative T-cell cytotoxicity crossmatches. Ann Lab Med 2012; 32(2): 139–144
https://doi.org/10.3343/alm.2012.32.2.139 pmid: 22389881
63 M Bieri, M Oroszlan, A Farkas, N Ligeti, J Bieri, P Mohacsi. Anti-HLA I antibodies induce VEGF production by endothelial cells, which increases proliferation and paracellular permeability. Int J Biochem Cell Biol 2009; 41(12): 2422–2430
https://doi.org/10.1016/j.biocel.2009.06.009 pmid: 19577661
64 C Lefaucheur, A Loupy, GS Hill, J Andrade, D Nochy, C Antoine, C Gautreau, D Charron, D Glotz, C Suberbielle-Boissel. Preexisting donor-specific HLA antibodies predict outcome in kidney transplantation. J Am Soc Nephrol 2010; 21(8): 1398–1406
https://doi.org/10.1681/ASN.2009101065 pmid: 20634297
65 C Lefaucheur, C Antoine, C Suberbielle, D Glotz. Mastering the risk of HLA antibodies in kidney transplantation: an algorithm based on pretransplant single-antigen flow bead techniques. Am J Transplant 2011; 11(8): 1592–1598
https://doi.org/10.1111/j.1600-6143.2011.03560.x pmid: 21668626
66 S Safavi, DR Robinson, S Soresi, M Carby, JD Smith. De novo donor HLA-specific antibodies predict development of bronchiolitis obliterans syndrome after lung transplantation. J Heart Lung Transplant 2014; 33(12): 1273–1281
https://doi.org/10.1016/j.healun.2014.07.012 pmid: 25130554
67 CA Witt, JP Gaut, RD Yusen, DE Byers, JA Iuppa, K Bennett Bain, G Alexander Patterson, T Mohanakumar, EP Trulock, RR Hachem. Acute antibody-mediated rejection after lung transplantation. J Heart Lung Transplant 2013; 32(10): 1034–1040
https://doi.org/10.1016/j.healun.2013.07.004 pmid: 23953920
68 JD Smith, NR Banner, IM Hamour, M Ozawa, A Goh, D Robinson, PI Terasaki, ML Rose. De novo donor HLA-specific antibodies after heart transplantation are an independent predictor of poor patient survival. Am J Transplant 2011; 11(2): 312–319
https://doi.org/10.1111/j.1600-6143.2010.03383.x pmid: 21219570
69 A Roux, I Bendib Le Lan, S Holifanjaniaina, KA Thomas, AM Hamid, C Picard, D Grenet, S De Miranda, B Douvry, L Beaumont-Azuar, E Sage, J Devaquet, E Cuquemelle, M Le Guen, R Spreafico, C Suberbielle-Boissel, M Stern, F; Foch Lung Transplantation Group. ParquinAntibody-mediated rejection in lung transplantation: clinical outcomes and donor-specific antibody characteristics. Am J Transplant 2016; 16(4): 1216–1228
https://doi.org/10.1111/ajt.13589 pmid: 26845386
70 D Kopchaliiska, J Kukreja, G Dincheva, E Bush, L Leard, J Singer, M Brzezinski, S Hays, R Rajalingam. IVIG infusion deplete donor-specific HLA antibodies in lung transplant recipients: a single-center experience. Hum Immunol 2015; 76(Suppl): 14–37
71 M Stern, H Hirsch, A Cusini, C van Delden, O Manuel, P Meylan, K Boggian, NJ Mueller, M Dickenmann; Members of Swiss Transplant Cohort Study. Cytomegalovirus serology and replication remain associated with solid organ graft rejection and graft loss in the era of prophylactic treatment. Transplantation 2014; 98(9): 1013–1018
https://doi.org/10.1097/TP.0000000000000160 pmid: 24837540
72 L Baxter-Lowe, J Singer, S Hays, J Kukreja, J Golden, L Leard .Late after lung transplantation many patients have donor-specific HLA antibodies (DSA) and high DSA levels appear to be associated with poor outcomes. Am J Transplant 2013; 13 (suppl 5) [abstract]
73 A Zeevi, M Marrari, K Spichty, M Morrell, C Gries, J McDyer, J Pilewski, D Zaldonis, J Bhama, N Shigemura, S Yousem, R Duquesnoy, J D’Cunha, C Bermudez. Increased frequency of class II HLA-DQ donor-specific antibodies is associated with mixed cellular and humoral rejection in lungtransplantation. J Heart Lung Transplant 2013; 32(4 4S): S76
https://doi.org/10.1016/j.healun.2013.01.190
74 JM Tikkanen, LG Singer, SJ Kim, Y Li, M Binnie, C Chaparro, CW Chow, T Martinu, S Azad, S Keshavjee, K Tinckam. De novo DQ donor-specific antibodies are associated with chronic lung allograft dysfunction after lung transplantation. Am J Respir Crit Care Med 2016; 194(5): 596–606
https://doi.org/10.1164/rccm.201509-1857OC pmid: 26967790
75 A Loupy, C Lefaucheur, D Vernerey, C Prugger, JP Duong van Huyen, N Mooney, C Suberbielle, V Frémeaux-Bacchi, A Méjean, F Desgrandchamps, D Anglicheau, D Nochy, D Charron, JP Empana, M Delahousse, C Legendre, D Glotz, GS Hill, A Zeevi, X Jouven. Complement-binding anti-HLA antibodies and kidney-allograft survival. N Engl J Med 2013; 369(13): 1215–1226
https://doi.org/10.1056/NEJMoa1302506 pmid: 24066742
76 M Yell, BL Muth, DB Kaufman, A Djamali, TM Ellis. C1q binding activity of de novo donor-specific HLA antibodies in renal transplant recipients with and without antibody-mediated rejection. Transplantation 2015; 99(6): 1151–1155
https://doi.org/10.1097/TP.0000000000000699 pmid: 25839705
77 A Sicard, S Ducreux, M Rabeyrin, L Couzi, B McGregor, L Badet, JY Scoazec, T Bachelet, S Lepreux, J Visentin, P Merville, V Fremeaux-Bacchi, E Morelon, JL Taupin, V Dubois, O Thaunat. Detection of C3d-binding donor-specific anti-HLA antibodies at diagnosis of humoral rejection predicts renal graft loss. J Am Soc Nephrol 2015; 26(2): 457–467
https://doi.org/10.1681/ASN.2013101144 pmid: 25125383
78 MG Strainic, J Liu, D Huang, F An, PN Lalli, N Muqim, VS Shapiro, GR Dubyak, PS Heeger, ME Medof. Locally produced complement fragments C5a and C3a provide both costimulatory and survival signals to naive CD4+ T cells. Immunity 2008; 28(3): 425–435
https://doi.org/10.1016/j.immuni.2008.02.001 pmid: 18328742
79 GP Westall, GI Snell, C McLean, T Kotsimbos, T Williams, C Magro. C3d and C4d deposition early after lung transplantation. J Heart Lung Transplant 2008; 27(7): 722–728
https://doi.org/10.1016/j.healun.2008.03.018 pmid: 18582800
80 EJ Lepin, Q Zhang, X Zhang, PT Jindra, LS Hong, P Ayele, MV Peralta, DW Gjertson, JA Kobashigawa, WD Wallace, MC Fishbein, EF Reed. Phosphorylated S6 ribosomal protein: a novel biomarker of antibody-mediated rejection in heart allografts. Am J Transplant 2006; 6(7): 1560–1571
https://doi.org/10.1111/j.1600-6143.2006.01355.x pmid: 16827856
81 T Hirohashi, CM Chase, P Della Pelle, D Sebastian, A Alessandrini, JC Madsen, PS Russell, RB Colvin. A novel pathway of chronic allograft rejection mediated by NK cells and alloantibody. Am J Transplant 2012; 12(2): 313–321
https://doi.org/10.1111/j.1600-6143.2011.03836.x pmid: 22070565
82 X Zhang, EF Reed. Effect of antibodies on endothelium. Am J Transplant 2009; 9(11): 2459–2465
https://doi.org/10.1111/j.1600-6143.2009.02819.x pmid: 19775314
83 F Li, J Wei, NM Valenzuela, C Lai, Q Zhang, D Gjertson, MC Fishbein, JA Kobashigawa, M Deng, EF Reed. Phosphorylated S6 kinase and S6 ribosomal protein are diagnostic markers of antibody-mediated rejection in heart allografts. J Heart Lung Transplant 2015; 34(4): 580–587
https://doi.org/10.1016/j.healun.2014.09.047 pmid: 25511749
84 S Le Bas-Bernardet, S Coupel, A Chauveau, JP Soulillou, B Charreau. Vascular endothelial cells evade apoptosis triggered by human leukocyte antigen-DR ligation mediated by allospecific antibodies. Transplantation 2004; 78(12): 1729–1739
https://doi.org/10.1097/01.TP.0000147339.31581.99 pmid: 15614145
85 J Lion, C Taflin, AR Cross, M Robledo-Sarmiento, E Mariotto, A Savenay, M Carmagnat, C Suberbielle, D Charron, A Haziot, D Glotz, N Mooney. HLA class II antibody activation of endothelial cells promotes Th17 and disrupts regulatory T lymphocyte expansion. Am J Transplant 2016; 16(5): 1408–1420
https://doi.org/10.1111/ajt.13644 pmid: 26614587
86 C Deteix, V Attuil-Audenis, A Duthey, N Patey, B McGregor, V Dubois, G Caligiuri, S Graff-Dubois, E Morelon, O Thaunat. Intragraft Th17 infiltrate promotes lymphoid neogenesis and hastens clinical chronic rejection. J Immunol 2010; 184(9): 5344–5351
https://doi.org/10.4049/jimmunol.0902999 pmid: 20357253
87 HI Basha, S Ramachandran, V Tiriveedhi, M Takenaka, V Subramanian, DS Nath, N Benshoff, GA Patterson, T Mohanakumar. Critical role for IL-17A/F in the immunopathogenesis of obliterans airway disease induced by anti-MHC I antibodies. Transplantation 2013; 95(2): 293–300
https://doi.org/10.1097/TP.0b013e3182772244 pmid: 23325004
88 D Jane-wit, TD Manes, T Yi, L Qin, P Clark, NC Kirkiles-Smith, P Abrahimi, J Devalliere, G Moeckel, S Kulkarni, G Tellides, JS Pober. Alloantibody and complement promote T cell-mediated cardiac allograft vasculopathy through noncanonical nuclear factor-kB signaling in endothelial cells. Circulation 2013; 128(23): 2504–2516 doi:10.1161/CIRCULATIONAHA.113.002972
pmid: 24045046
89 M Mezzetti, M Soloperto, A Fasoli, S Mattoli. Human bronchial epithelial cells modulate CD3 and mitogen-induced DNA synthesis in T cells but function poorly as antigen-presenting cells compared to pulmonary macrophages. J Allergy Clin Immunol 1991; 87(5): 930–938
https://doi.org/10.1016/0091-6749(91)90414-J pmid: 1827479
90 AC Cunningham, JG Zhang, JV Moy, S Ali, JA Kirby. A comparison of the antigen-presenting capabilities of class II MHC-expressing human lung epithelial and endothelial cells. Immunology 1997; 91(3): 458–463
https://doi.org/10.1046/j.1365-2567.1997.d01-2249.x pmid: 9301537
91 LG Hidalgo, J Sellares, B Sis, M Mengel, J Chang, PF Halloran. Interpreting NK cell transcripts versus T cell transcripts in renal transplant biopsies. Am J Transplant 2012; 12(5): 1180–1191
https://doi.org/10.1111/j.1600-6143.2011.03970.x pmid: 22390872
92 MD Parkes, PF Halloran, LG Hidalgo. Evidence for CD16a-mediated NK cell stimulation in antibody-mediated kidney transplant rejection. Transplantation 2017; 101(4): e102–e111
https://doi.org/10.1097/TP.0000000000001586 pmid: 27906829
93 D Saini, N Angaswamy, V Tiriveedhi, N Fukami, S Ramachandran, R Hachem, E Trulock, B Meyers, A Patterson, T Mohanakumar. Synergistic effect of antibodies to human leukocyte antigens and defensins in pathogenesis of bronchiolitis obliterans syndrome after human lung transplantation. J Heart Lung Transplant 2010; 29(12): 1330–1336
https://doi.org/10.1016/j.healun.2010.05.036 pmid: 20691611
94 N Fukami, S Ramachandran, D Saini, M Walter, W Chapman, GA Patterson, T Mohanakumar. Antibodies to MHC class I induce autoimmunity: role in the pathogenesis of chronic rejection. J Immunol 2009; 182(1): 309–318
https://doi.org/10.4049/jimmunol.182.1.309 pmid: 19109162
95 A Jaramillo, CR Smith, T Maruyama, L Zhang, GA Patterson, T Mohanakumar. Anti-HLA class I antibody binding to airway epithelial cells induces production of fibrogenic growth factors and apoptotic cell death: a possible mechanism for bronchiolitis obliterans syndrome. Hum Immunol 2003; 64(5): 521–529
https://doi.org/10.1016/S0198-8859(03)00038-7 pmid: 12691702
96 GS Hill, D Nochy, P Bruneval, JP Duong van Huyen, D Glotz, C Suberbielle, J Zuber, D Anglicheau, JP Empana, C Legendre, A Loupy. Donor-specific antibodies accelerate arteriosclerosis after kidney transplantation. J Am Soc Nephrol 2011; 22(5): 975–983
https://doi.org/10.1681/ASN.2010070777 pmid: 21493773
97 T Maruyama, A Jaramillo, K Narayanan, T Higuchi, T Mohanakumar. Induction of obliterans airway disease by anti-HLA class I antibodies. Am J Transplant 2005; 5(9): 2126–2134
https://doi.org/10.1111/j.1600-6143.2005.00999.x pmid: 16095491
98 Y Yamada, Y Sekine, S Yoshida, K Yasufuku, I Petrache, HL Benson, DD Brand, I Yoshino, DS Wilkes. Type V collagen-induced oral tolerance plus low-dose cyclosporine prevents rejection of MHC class I and II incompatible lung allografts. J Immunol 2009; 183(1): 237–245
https://doi.org/10.4049/jimmunol.0804028 pmid: 19542435
99 Z Xu, DK Nayak, N Benshoff, R Hachem, AE Gelman, T Mohanakumar. De novo-developed antibodies to donor MHC antigens lead to dysregulation of microRNAs and induction of MHC class II. J Immunol 2015; 194(12): 6133–6143
https://doi.org/10.4049/jimmunol.1401848 pmid: 25941328
100 DK Nayak, F Zhou, M Xu, J Huang, M Tsuji, J Yu, R Hachem, AE Gelman, RM Bremner, MA Smith, T Mohanakumar. Zbtb7a induction in alveolar macrophages is implicated in anti-HLA-mediated lung allograft rejection. Sci Transl Med 2017; 9(398): eaal1243
https://doi.org/10.1126/scitranslmed.aal1243 pmid: 28701473
101 S Otani, AK Davis, L Cantwell, S Ivulich, A Pham, MA Paraskeva, GI Snell, GP Westall. Evolving experience of treating antibody-mediated rejection following lung transplantation. Transpl Immunol 2014; 31(2): 75–80
https://doi.org/10.1016/j.trim.2014.06.004 pmid: 25004453
102 GE Rodey, TC Fuller. Public epitopes and the antigenic structure of the HLA molecules. Crit Rev Immunol 1987; 7(3): 229–267
pmid: 2441930
103 MA Ayala García, B González Yebra, AL López Flores, E Guaní Guerra. The major histocompatibility complex in transplantation. J Transplant 2012; 2012: 842141
https://doi.org/10.1155/2012/842141 pmid: 22778908
104 G Opelz, J Mytilineos, S Scherer, H Dunckley, J Trejaut, J Chapman, D Middleton, D Savage, O Fischer, JD Bignon, JC Bensa, E Albert, H; Noreen The Collaborative Transplant Study. Survival of DNA HLA-DR typed and matched cadaver kidney transplants. Lancet 1991; 338(8765): 461–463
https://doi.org/10.1016/0140-6736(91)90540-6 pmid: 1678443
105 SK Takemoto, PI Terasaki, DW Gjertson, JM Cecka. Twelve years’ experience with national sharing of HLA-matched cadaveric kidneys for transplantation. N Engl J Med 2000; 343(15): 1078–1084
https://doi.org/10.1056/NEJM200010123431504 pmid: 11027742
106 P Rubinstein. HLA matching for bone marrow transplantation—how much is enough? N Engl J Med 2001; 345(25): 1842–1844
https://doi.org/10.1056/NEJM200112203452511 pmid: 11752363
107 T Kawase, K Matsuo, K Kashiwase, H Inoko, H Saji, S Ogawa, S Kato, T Sasazuki, Y Kodera, Y Morishima; Japan Marrow Donor Program.. HLA mismatch combinations associated with decreased risk of relapse: implications for the molecular mechanism. Blood 2009; 113: 2851–2858
https://doi.org/10.1182/blood-2008-08-171934 pmid: 18997170
108 N Chin, M Paraskeva, E Paul, L Cantwell, B Levvey, T Williams, G Snell, G Westall. Comparative analysis of how immune sensitization is defined prior to lung transplantation. Hum Immunol 2015; 76(10): 711–716
https://doi.org/10.1016/j.humimm.2015.09.025 pmid: 26429328
109 CM Burton, M Iversen, N Milman, M Zemtsovski, J Carlsen, D Steinbrüchel, J Mortensen, CB Andersen. Outcome of lung transplanted patients with primary graft dysfunction. Eur J Cardiothorac Surg 2007; 31(1): 75–82
https://doi.org/10.1016/j.ejcts.2006.10.024 pmid: 17134909
[1] Fei Gao, Jingyu Chen, Dong Wei, Bo Wu, Min Zhou. Lung transplantation for bronchiolitis obliterans syndrome after allogenic hematopoietic stem cell transplantation[J]. Front. Med., 2018, 12(2): 224-228.
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