Molecular landscape of T cell-mediated rejection in human kidney transplants: Prominence of CTLA4 and PD ligands

American Journal of Transplantation

Volumn 14, Issue 11, 2014, Pages 2565-2576

  Venner, J M ^a,b   Famulski, K S ^a,c   Badr, D ^a,b   Hidalgo, L G ^a,c   Chang, J ^a   Halloran, P F ^a,b  

^a UNIVERSITY OF ALBERTA   (Canada)

^b UNIVERSITY OF ALBERTA   (Canada)

^c UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Basic (laboratory) research science, biopsy; costimulation; kidney (allograft) function dysfunction; kidney transplantation nephrology immunobiology; rejection: antibody mediated (ABMR); rejection: T cell mediated (TCMR); translational research science

Indexed keywords

ADAM PROTEIN; ANKYRIN; APC PROTEIN; CD28 ANTIGEN; CD72 ANTIGEN; CD86 ANTIGEN; CD8ALPHA ANTIGEN; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; GAMMA INTERFERON; GAMMA INTERFERON RECEPTOR 1; INFLAMMASOME; PROGRAMMED DEATH 1 LIGAND 1; SIGNALING LYMPHOCYTE ACTIVATION MOLECULE ASSOCIATED PROTEIN; T LYMPHOCYTE RECEPTOR; CD274 PROTEIN, HUMAN; CTLA4 PROTEIN, HUMAN; LIGAND; MESSENGER RNA;

ADOLESCENT; ADULT; AGED; ANTIBODY MEDIATED REJECTION; ANTIGEN PRESENTING CELL; ARTICLE; B LYMPHOCYTE; CELL ACTIVATION; CHILD; DENDRITIC CELL; EFFECTOR CELL; FEMALE; GENE EXPRESSION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IMMUNOSTIMULATION; INNATE IMMUNITY; KIDNEY BIOPSY; KIDNEY GRAFT; KIDNEY GRAFT REJECTION; KIDNEY INJURY; KIDNEY PARENCHYMA; KIDNEY TRANSPLANTATION; MACROPHAGE; MAJOR CLINICAL STUDY; MALE; MICROARRAY ANALYSIS; MONOCYTE; NATURAL KILLER CELL; SIGNAL TRANSDUCTION; T CELL MEDIATED REJECTION; T LYMPHOCYTE; VALIDATION STUDY; GENETICS; GRAFT REJECTION; IMMUNOLOGY; MIDDLE AGED; VERY ELDERLY; YOUNG ADULT;

ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; ANTIGENS, CD274; CHILD; CTLA-4 ANTIGEN; FEMALE; GRAFT REJECTION; HUMANS; KIDNEY TRANSPLANTATION; LIGANDS; MALE; MIDDLE AGED; RNA, MESSENGER; T-LYMPHOCYTES; YOUNG ADULT;

EID: 84911988581     PISSN: 16006135     EISSN: 16006143     Source Type: Journal    
DOI: 10.1111/ajt.12946     Document Type: Article

References (60)

1. Sullivan RJ, Lorusso PM, Flaherty KT., The intersection of immune-directed and molecularly targeted therapy in advanced melanoma: Where we have been, are, and will be. Clin Cancer Res 2013; 19: 5283-5291.
2. Krensky AM, Weiss A, Crabtree G, Davis MM, Parham P., T-lymphocyte-antigen interactions in transplant rejection. N Engl J Med 1990; 322: 510-517.
3. Sharma VK, Bologa RM, Li BG, et al. Molecular executors of cell death differential intrarenal expression of Fas ligand, Fas, granzyme B, and perforin during acute and/or chronic rejection of human renal allografts. Transplant 1996; 62: 1860-1866.
4. Halloran PF., T cell mediated rejection of kidney transplants: A personal viewpoint. Am J Transplant 2010; 10: 1126-1134.
5. Walch JM, Zeng Q, Li Q, et al. Cognate antigen directs CD8+ T cell migration to vascularized transplants. J Clin Invest 2013; 123: 2663-2671.
6. Adams AB, Williams MA, Jones TR, et al. Heterologous immunity provides a potent barrier to transplantation tolerance. J Clin Invest 2003; 111: 1887-1895.
7. Glimcher LH, Townsend MJ, Sullivan BM, Lord GM., Recent developments in the transcriptional regulation of cytolytic effector cells. Nat Rev Immunol 2004; 4: 900-911.
8. Latz E, Xiao TS, Stutz A., Activation and regulation of the inflammasomes. Nat Rev Immunol 2013; 13: 397-411.
9. Famulski KS, Reeve J, de Freitas DG, Kreepala C, Chang J, Halloran PF., Kidney transplants with progressing chronic kidney diseases express high levels of acute kidney injury transcripts. Am J Transplant 2013; 13: 634-644.
10. Einecke G, Kayser D, Vanslambrouck JM, et al. Loss of solute carriers in T cell mediated rejection in mouse and human kidneys: An active epithelial injury-repair response. Am J Transplant 2010; 10: 2241-2251.
11. Halloran PF, Wadgymar A, Ritchie S, Falk J, Solez K, Srinivasa NS., The significance of the anti-class I antibody response. I. Clinical and pathologic features of anti-class I-mediated rejection. Transplant 1990; 49: 85-91.
12. Reeve J, Einecke G, Mengel M, et al. Diagnosing rejection in renal transplants: A comparison of molecular- and histopathology-based approaches. Am J Transplant 2009; 9: 1802-1810.
13. Halloran PF, de Freitas DG, Einecke G, et al. The molecular phenotype of kidney transplants. Am J Transplant 2010; 10: 2215-2222.
14. Einecke G, Sis B, Reeve J, et al. Antibody-mediated microcirculation injury is the major cause of late kidney transplant failure. Am J Transplant 2009; 9: 2520-2531.
15. Sarwal M, Chua MS, Kambham N, et al. Molecular heterogeneity in acute renal allograft rejection identified by DNA microarray profiling. N Engl J Med 2003; 349: 125-138.
16. Flechner SM, Kurian SM, Head SR, et al. Kidney transplant rejection and tissue injury by gene profiling of biopsies and peripheral blood lymphocytes. Am J Transplant 2004; 4: 1475-1489.
17. Saint-Mezard P, Berthier CC, Zhang H, et al. Analysis of independent microarray datasets of renal biopsies identifies a robust transcript signature of acute allograft rejection. Transplant Int 2009; 22: 293-302.
18. Reeve J, Sellares J, Mengel M, et al. Molecular diagnosis of T cell-mediated rejection in human kidney transplant biopsies. Am J Transplant 2013; 13: 645-655.
19. Halloran PF, Pereira AB, Chang J, et al. Potential impact of microarray diagnosis of T cell-mediated rejection in kidney transplants: The INTERCOM study. Am J Transplant 2013; 13: 2352-2363.
20. Haas M, Sis B, Racusen LC, et al. Banff 2013 meeting report: Inclusion of C4d-negative antibody-mediated rejection and antibody-associated arterial lesions. Am J Transplant 2014; 14: 272-283.
21. R Core Team. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing, 2014. Available at: http://www.r-project.org/. Accessed August 13, 2014.
22. Gentleman R, Carey VJ, Bates DM, et al. Bioconductor: Open software development for computational biology and bioinformatics. Genome Biol 2004; 5: R80. Available at: http://www.bioconductor.org/. Accessed August 13, 2014.
23. Hidalgo LG, Einecke G, Allanach K, Halloran PF., The transcriptome of human cytotoxic T cells: Similarities and disparities among allostimulated CD4(+) CTL, CD8(+) CTL and NK cells. Am J Transplant 2008; 8: 627-636.
24. Nagler A, Lanier LL, Cwirla S, Phillips JH., Comparative studies of human FcRIII-positive and negative natural killer cells. J Immunol 1989; 143: 3183-3191.
25. Hidalgo LG, Sellares J, Sis B, Mengel M, Chang J, Halloran PF., Interpreting NK cell transcripts versus T cell transcripts in renal transplant biopsies. Am J Transplant 2012; 12: 1180-1191.
26. Sallusto F, Lanzavecchia A., Efficient presentation of soluble antigen by cultured human dendritic cells is maintained by granulocyte/macrophage colony-stimulating factor plus interleukin 4 and downregulated by tumor necrosis factor α. J Exp Med 1994; 179: 1109-1118.
27. Mueller CG, Rissoan MC, Salinas B, et al. Polymerase chain reaction selects a novel disintegrin proteinase from CD40-activated germinal center dendritic cells. J Exp Med 1997; 186: 655-663.
28. van Lieshout AW, van der Voort R, le Blanc LM, et al. Novel insights in the regulation of CCL18 secretion by monocytes and dendritic cells via cytokines, toll-like receptors and rheumatoid synovial fluid. BMC Immunol 2006; 7: 23.
29. Hidalgo LG, Sis B, Sellares J, et al. NK cell transcripts and NK cells in kidney biopsies from patients with donor-specific antibodies: Evidence for NK cell involvement in antibody-mediated rejection. Am J Transplant 2010; 10: 1812-1822.
30. Ein-Dor L, Kela I, Getz G, Givol D, Domany E., Outcome signature genes in breast cancer: Is there a unique set ? Bioinformatics 2005; 21: 171-178.
31. Jackson JA, Kim EJ, Begley B, et al. Urinary chemokines CXCL9 and CXCL10 are noninvasive markers of renal allograft rejection and BK viral infection. Am J Transplant 2011; 11: 2228-2234.
32. Hu H, Aizenstein BD, Puchalski A, Burmania JA, Hamawy MM, Knechtle SJ., Elevation of CXCR3-binding chemokines in urine indicates acute renal-allograft dysfunction. Am J Transplant 2004; 4: 432-437.
33. Strehlau J, Pavlakis M, Lipman M, et al. Quantitative detection of immune activation transcripts as a diagnostic tool in kidney transplantation. Proc Natl Acad Sci U S A 1997; 94: 695-700.
34. Kotsch K, Mashreghi MF, Bold G, et al. Enhanced granulysin mRNA expression in urinary sediment in early and delayed acute renal allograft rejection. Transplant 2013; 77: 1866-1875.
35. Li B, Hartono C, Ding R, et al. Noninvasive diagnosis of renal-allograft rejection by measurement of messenger RNA for perforin and granzyme B in urine. N Engl J Med 2001; 344: 947-954.
36. Famulski KS, Einecke G, Reeve J, et al. Changes in the transcriptome in allograft rejection: IFN-γ induced transcripts in mouse kidney allografts. Am J Transplant 2006; 6: 1342-1354.
37. Famulski KS, Einecke G, Sis B, et al. Defining the canonical form of T-cell-mediated rejection in human kidney transplants. Am J Transplant 2010; 10: 810-820.
38. Famulski KS, de Freitas DG, Kreepala C, et al. Molecular phenotypes of acute kidney injury in human kidney transplants. J Am Soc Nephrol 2012; 23: 948-958.
39. Bromley SK, Burack WR, Johnson KG, et al. The immunological synapse. Ann Rev Immunol 2001; 19: 375-396.
40. Riley JL, Mao M, Kobayashi S, et al. Modulation of TCR-induced transcriptional profiles by ligation of CD28, ICOS, and CTLA-4 receptors. Proc Natl Acad Sci U S A 2002; 99: 11790-11795.
41. Cham CM, Xu H, O'Keefe JP, Rivas FV, Zagouras P, Gajewski TF., Gene array and protein expression profiles suggest post-transcriptional regulation during CD8(+) T cell differentiation. J Biol Chem 2003; 278: 17044-17052.
42. Wang M, Windgassen D, Papoutsakis ET., Comparative analysis of transcriptional profiling of CD3+, CD4+ and CD8+ T cells identifies novel immune response players in T-cell activation. BMC Genomics 2008; 9: 225.
43. Smeets RL, Fleuren WWM, He XH, et al. Molecular pathway profiling of T lymphocyte signal transduction pathways; Th1 and Th2 genomic fingerprints are defined by TCR and CD28-mediated signaling. BMC Immunol 2012; 13: 12.
44. Jarvis LB, Goodall JC, Gaston JSH., Human leukocyte antigen class I-restricted immunosuppression by human CD8(+) regulatory T cells requires CTLA-4-mediated interaction with dendritic cells. Hum Immunol 2008; 69: 687-95.
45. Slifka MK, Whitton JL., Activated and memory CD8+ T cells can be distinguished by their cytokine profiles and phenotypic markers. J Immunol 2000; 164: 208-216.
46. London CA, Lodge MP, Abbas AK., Functional responses and costimulator dependence of memory CD4(+) T cells. J Immunol 2000; 164: 265-272.
47. O'Keefe JP, Blaine K, Alegre ML, Gajewski TF., Formation of a central supramolecular activation cluster is not required for activation of naive CD8(+) T cells. Proc Natl Acad Sci U S A 2004; 101: 9351-9356.
48. Hoffman SC, Hale DA, Kleiner DE, et al. Functionally significant renal allograft rejection is defined by transcriptional criteria. Am J Transplant 2005; 5: 573-581.
49. Vincenti F, Charpentier B, Vanrenterghem Y, et al. A phase III study of belatacept-based immunosuppression regimens versus cyclosporine in renal transplant recipients (BENEFIT study). Am J Transplant 2010; 10: 535-546.
50. Zhang Y, Chung Y, Bishop C, et al. Regulation of T cell activation and tolerance by PDL2. Proc Natl Acad Sci U S A 2006; 103: 11695-11700.
51. Okazaki T, Chikuma S, Iwai Y, Fagarasan S, Honjo T., A rheostat for immune responses: The unique properties of PD-1 and their advantages for clinical application. Nat Immunol 2013; 14: 1212-1218.
52. Lund J, Olsen OH, Sorensen ES, Stennicke HR, Petersen HH, Overgaard MT., ADAMDEC1 is a metzincin metalloprotease with dampened proteolytic activity. J Biol Chem 2013; 288: 21367-21375.
53. Vandenabeele S, Hochrein H, Mavaddat N, Winkel K, Shortman K., Human thymus contains 2 distinct dendritic cell populations. Blood 2001; 97: 1733-1741.
54. Crouser ED, Culver DA, Knox KS, et al. Gene expression profiling identifies MMP-12 and ADAMDEC1 as potential pathogenic mediators of pulmonary sarcoidosis. Am J Respir Crit Care Med 2009; 179: 929-938.
55. Andersen CB, Ladefoged SD, Larsen S., Acute kidney graft rejection. A morphological and immunohistological study on "zero-hour" and follow-up biopsies with special emphasis on cellular infiltrates and adhesion molecules. APMIS 1994; 102: 23-37.
56. Meehan SM, McCluskey RT, Pascual M, et al. Cytotoxicity and apoptosis in human renal allografts: Identification, distribution, and quantitation of cells with a cytotoxic granule protein GMP-17 (TIA-1) and cells with fragmented nuclear DNA. Lab Invest 1997; 76: 639-649.
57. Volk HD, Sawitzki B, Reinke P., Molecular analysis of renal allograft biopsies-More than a nice toy for researchers ? Am J Transplant 2013; 13: 539-540.
58. Govindan R, Ding L, Griffith M, et al. Genomic landscape of non-small cell lung cancer in smokers and never-smokers. Cell 2012; 150: 1121-1134.
59. Seok J, Warren HS, Cuenca AG, et al. Genomic responses in mouse models poorly mimic human inflammatory diseases. Proc Natl Acad Sci U S A 2013; 110: 3507-3512.
60. Nature Medicine Editorial. Of men, not mice. Nat Med 2013; 19: 379.