Transcript Slide 1
Molecular associations of IFTA Michael Mengel Alberta Transplant Applied Genomics Centre University of Alberta, Edmonton Canada ATAGC TSI Interstitial fibrosis and tubular atrophy (IFTA) in renal allografts IFTA with inflammation Issues with doing analysis for the causes / associates of IFTA • • Most studies group comparisons “sick vs. well”, i.e. biopsies with moderate to severe IFTA are compared to normal biopsies without IFTA: starting with the extreme phenotypes Cave! The first group generally has a lot of other pathologies while the others are really normal, thus it’s difficult to see whether the findings are related to IFTA or to a co-existing finding, e.g. interstitial inflammation or time post transplant Example 1 of a “sick vs. well” study Title: “Molecular pathways involved in loss of kidney graft function with tubular atrophy and interstitial fibrosis.” Mol Med. 2008 May-Jun;14(5-6):276-85. Scoring inflammation in renal allograft biopsies 100% Cortex nodular perivascular subcapsular 10% i-Banff 5% 3% 25% = Banff i-score 1 40% non-scarred compartment 3% 40% i-IFTA absolute scoring “67% i-IFTA” relative scoring 5% 60% IFTA compartment according to current Banff rules Material and Methods • • • 129 biopsies for cause classified according to Banff ‘97 Semi-quantitative assessment as absolute percentages of: – i-Banff = inflammation in non scarred cortex – i-IFTA = inflammation in IFTA – nodular – perivascular – IFTA Correlation of extent of histological lesions with gene expression data from microarrays and allograft survival Infiltrates in biopsies for cause are time dependent 100 fibrosis/atrophy i-Banff 90 i-IFTA 80 % cortex involved 70 60 50 40 30 20 10 0 1 6 11 16 3 months 21 26 31 36 41 46 51 8 months 56 61 66 71 76 81 86 27 months 91 96 101 106 111 116 121 126 79 months 246 months 129 biopsies ordered by time post TX Mengel et al. Am J Transplant. 2009 Jan;9(1):169-78. Infiltrates and time in BFC 30 p<0.0001 mean % cortex involved 25 p<0.0001 20 nodular perivascular 15 i-Banff i-IFTA IFTA 10 5 0 <6 months post TX, n=42 >6 months post TX, n=87 Inflammation in fibrosis/atrophy is associated with worse allograft survival B A uninflamed IFTA i <25% inflamed IFTA i-Banff p=0.02 i-IFTA p<0.05 + Inclusion criteria: IFTA >5%, i-Banff <25% graft survival ≥50% of fibrosis/atrophy show infiltrates 69.6% <50% of fibrosis/atrophy show infiltrates 93.5% censored biopsies with n 46 31 77 + i-Banff >25%, i-IFTA <25% i-IFTA >25%, i-Banff <25% both <25% censored graft survival 69.2% 60.0% 88.7% n 13 20 71 104 Table 1: Correlations between Infiltrate types and Pathogenesis Based Transcript sets (PBTs) Gene sets*# i-Banff t-score i-IFTA IFTA nodular perivascular T-cell associated (CATs) 0.534 0.484 0.284 0.246 0.298 ns γ-Interferon dependent (GRITs) 0.532 0.441 0.258 0.211 0.241 ns Kidney parenchyma associated (KTs) -0.296 -0.303 -0.199 -0.156 ns ns Injury and repair associated (IRITs) 0.379 0.355 0.246 0.206 ns ns Immunoglobulin associated (IGTs) 0.174 ns 0.434 0.398 0.336 ns B-cell associated (BATs) 0.281 0.279 0.423 0.387 0.355 ns # given is the highest r-value revealed for one PBT of each particular biological process *Spearman correlation, p<0.001 Correlations* between individual genes and histological lesions 484 probesets 249 probesets 202 probesets 172 probesets 34 probesets 100 not otherwise annotated 90 Endothelial activation 80 B-cell / Ig associated Injury B-cell Mac i-Banff Banff t-score i-IFTA Injury T-cell 10 Injury *r>0.4, p<0.001: no correlations between any genes and perivascular infiltrates at this cut-off B-cell 20 Macrophage associated T-cell associated T-cell 30 Kidney parenchyma associated Interferon-γ dependent B-cell 40 γ-IFN 50 γ-IFN Mac 60 Injury and repair associated T-cell % contribution 70 Injury 0 fibrosis/atrophy nodular Figure 3: Overlap in gene expression between infiltrate types i-Banff 244 240 116 cytotoxic T cell associated 54 not annotated 39 γ-interferon dependent 14 Injury and Repair induced 17 macrophage associated 132 i-IFTA 70 84 not annotated 26 B cell associated 15 Injury and Repair induced 3 cytotoxic T cell associated 3 Kidney parenchymal 1 Endothelial activation t-score 9 IFTA 40 Genes (top 25) correlating with fibrosis/atrophy and i-IFTA Gene symbol CPA3 TPSB2 ABCA8 TPSAB1 GABRP FCER1A AGR2 NEGR1 ADAMTSL3 NLGN4X ENAH SNAP25 PAPLN BCMP11 SVEP1 PDE5A ZFPM2 MS4A2 C7 ROBO1 CHODL CXCL6 RGS13 PPIF CABP1 Gene name mast cell carboxypeptidase A3 mast cell tryptase beta 2 ABC transporters - ATP-binding cassette, sub-family A (ABC1), member 8 mast cell tryptase alpha/beta 1 gamma-aminobutyric acid (GABA) A receptor receptor for Fc fragment of IgE, high affinity I, expressed predominantely on mast cells anterior gradient homolog 2 neuronal growth regulator 1 ADAMTS-like 3 neuroligin 4 cytoskeleton regulatory protein hMena synaptosomal-associated protein papilin AGR3 = anterior gradient homolog 3 sushi, von Willebrand factor type A, EGF and pentraxin domain containing 1 phosphodiesterase 5A zinc finger protein, multitype 2 Fc fragment of IgE, high affinity I, receptor for; beta polypeptide Complement compnent 7 roundabout, axon guidance receptor, homolog 1 chondrolectin chemokine (C-X-C motif) ligand 6 (granulocyte chemotactic protein 2) regulator of G-protein signaling 13 peptidylprolyl isomerase F (cyclophilin F, CYP3; Cyp-D) calcium binding protein 1 Correlation* r-value 0.619 0.566 0.564 0.555 0.554 0.547 0.523 0.509 0.503 0.499 0.497 0.497 0.486 0.485 0.484 0.479 0.474 0.47 0.468 0.467 0.466 0.466 0.462 -0.47 -0.49 Confirmation by immunohistochemistry 70 p 0.006 65 60 55 i-Banff i-non-IFTA 50 45 i-IFTA i-IFTA p 0.02 % 40 35 30 25 20 p 0.006 15 p 0.0004 10 p 0.05 5 0 % T cells (CD3+) % Macropahges (CD68+) % B cells (CD20+) % plasma cells (CD138+) % IgG4 plasma cells (IgG4+) % mast cells (tryptase+) Mast cell associate transcript set (MACAT) 4 mast cell associated transcripts – CPA3 (Carboxypeptidase 3) – TPSB2 (Tryptase beta 2) – TPSAB1 ( Tryptase alpha-beta 1) – FCER1A (Fc fragment of IgE, high affinity I, receptor) Mast cell associated transcripts are a molecular correlate of IFTA Mast cell PBT score 2.5 p<0.0001 2 Mast cell transcripts correlate with 1.5 time post TX: r=0.55, p <0.01 1 0.5 i-IFTA: r=0.63, p <0.01 IFTA: r=0.61, p <0.01 delta GFR: r= -0.35, p <0.0001 0 i-Banff i-non-IFTA <25%,n=109 n=109 <25%, i-Banff i-non-IFTA >25%,n=20 n=20 >25%, i-IFTA <25%, n=102 i-IFTA >25%, n=27 IFTA <25%, n=87 IFTA >25%, n=42 In biopsies with IFTA increased expression of Mast cell associated transcript is associated with worse allograft survival low mast cell scores p=0.01 high mast cell scores + Inclusion criteria: at least IFTA grade I graft survival n high* MACAT score 71.2% 29 low* MACATscore 96.6% 59 censored 88 *low = lowest tertile of MACAT score of the included 88 biopsies *high = intermediate and highest tertile of MACAT score of the included 88 biopsies Summary IFTA and infiltrates • There are two inflammatory compartments in renal allografts: – i-Banff (non-scarred): • time-independent, T-cell, γ-interferon, macrophage associated, prognostic relevant – i-IFTA (scarred): • time-dependent, T-cell, γ-interferon, macrophage + B-cell, mast cell associated, prognostic relevant Relationship between IFTA and function in native kidneys Relationship between IFTA and function in renal allografts (biopsies for cause) Kasiske et al. Kidney Int. 1991;40:514-524 Molecular correlates of eGFR at the time of biopsy GFR transcript set Annotation of probesets (% of total of correlating probesets) 45 n = 144 GFRT Negative GFRT Positive g 0.09 -0.10 cg 0.03 0.03 i 0.33** -0.32** ci 0.29** -0.20** t 0.16 -0.19* 10 ct 0.29** -0.20* 5 v -0.02 -0.02 cv -0.09 0.17* ah -0.17* 0.21* mm 0.17 0.05 PTC 0.07 -0.08 eGFR at Biopsy -0.54** 0.50** Functional deterioration from baseline (delta eGFR) -0.28** -0.30** 40 35 n = 224 30 25 Histologic lesions (Banff scores)* 20 15 0 Negative Correlation IMATs IGTs CISTs GSTs BATs GRIT1 GRIT2 KT1 IRITD5 IRITD3 IRITD1 CMATs CATs Positive Correlation (Mactrophage activation) (Plasma cell infiltration) (severe injury) (severe injury) (B cell infiltration) (Ifng effects) (Ifng effects) (Parenchymal transcripts) (Injury) (Injury) (Injury) (Macrophage infiltration) (T cell infiltration) Renal function Bunnang and Einecke et al. J Am Soc Nephrol. 2009 (5):1149-60 Significant overlap between injury / repair / and IFTA associated transcripts Am J Transplant. 2007 Nov;7(11):2483-95. Numerous “fibrosis genes” are associated with injury and repair Early IRITs Intermediate IRITs Late IRITs Category % of genes in the list % of genes in the list % of genes in the list Response to stress (832) 4.8 7.4 9.1 Morphogenesis (n=951) 5.2 8.0 6.9 Organ development (991) 3.8 8.9 8.7 Embryonic kidney (n=904) 7.1 10.6 6.1 Ureteric bud vs mesenchyme (n=933) 6.7 12.6 7.4 Embryonic mesenchyme (n=951) 2.9 9.7 11.3 Mesenchyme vs ureteric bud (n=751) 4.8 8.0 19.9 Cell cycle and cell proliferation (n=1008) 2.4 8.3 10.4 Tgfb1/fibrogenesis (n=48) 1.9 3.2 6.1 Collagen (n=36) 0.5 1.1 4.3 ECM (n=431) 1.9 4.0 12.1 Molecular changes in protocol biopsies Background and Hypothesis early protocol biopsy subclinical pathology = harbinger of more severe, clinical overt, irreversible pathology therapeutic intervention prevention of irreversible chronic allograft damage assessment of the subclinical molecular phenotype of an allograft to further corroborate this hypothesis No molecular evidence for EMT in the onset of IFTA in early protocol biopsies J Am Soc Nephrol. 2008 Aug;19(8):1571-83. Molecular associates of subclinical IFTA at 12-months in clinically uncomplicated living donor kidney transplants Transplantation. 2007 Jun 15;83(11):1466-76 PBT-annotation of top 100 transcripts correlating* in 6-week protocol biopsies with future onset of IFTA in 6-month protocol biopsies 100% 90% 80% Endothel associated transcripts 70% TGF-β related transcripts 60% kidney parenchymal transcripts 50% injury induced transcripts 40% interferon-γ inducible transcripts 30% macrophage associated transcripts B cell associated transcripts 20% NK cell associated transcripts 10% T cell associated transcripts 0% correlated with onset of IFTA at 6-months correlated with delta clearance 6-weeks to correlated with prevalence of acute post TX 12-months rejection between 6-weeks and 12-months after transplantation *Spearman correlation, p<0.001 PBT-annotation of top 100 transcripts correlating* with future end points in PB 100% 90% 80% Endothel associated transcripts 70% TGF-β related transcripts 60% kidney parenchymal transcripts 50% injury induced transcripts 40% interferon-γ inducible transcripts 30% macrophage associated transcripts B cell associated transcripts 20% NK cell associated transcripts 10% T cell associated transcripts 0% correlated with onset of IFTA at 6-months correlated with delta clearance 6-weeks to correlated with prevalence of acute post TX 12-months rejection between 6-weeks and 12-months after transplantation *Spearman correlation, p<0.001 Conclusions: Molecules and IFTA • • • • IFTA by histology is associated with inflammation and injury / repair molecules = sign of active/progressive IFTA or attempt to recovery? Conclusion about cause for IFTA is yet not possible Some molecular correlates (e.g. mast cells) might be used as a measurement for IFTA More detailed resolution of the overall molecular disturbance might provide potential therapeutic targets for a non-cause specific anti IFTA treatment Outlook • Test reproducibility for IF, TA, i-Banff, iIFTA, and total i-score: – if feasible, reporting of the different inflammatory and morphological compartments might allow to design new clinical trials – i-Banff and i-IFTA might be amenable to different therapies