Proteomics analysis reveals a Th17-prone cell population in presymptomatic graft-versus-host disease

JCI Insight

Volumn 1, Issue 6, 2016, Pages

  Li, Wei ^a   Liu, Liangyi ^a   Gomez, Aurelie ^b   Zhang, Jilu ^a   Ramadan, Abdulraouf ^a   Zhang, Qing ^c   Choi, Sung W ^b   Zhang, Peng ^b   Greenson, Joel K ^b   Liu, Chen ^d   Jiang, Di ^e   Virts, Elizabeth ^a   Kelich, Stephanie L ^a   Chu, Hong Wei ^e   Flynn, Ryan ^f   Blazar, Bruce R ^f   Hanenberg, Helmut ^a   Hanash, Samir ^g   Paczesny, Sophie ^a  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

^c USA   (United States)

^d ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

^e DEPARTMENT OF MEDICINE   (United States)

^f UNIVERSITY OF MINNESOTA   (United States)

^g UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 85135870334     PISSN: None     EISSN: 23793708     Source Type: Journal    
DOI: 10.1172/jci.insight.86660     Document Type: Article

References (77)

1. Horowitz MM, et al. Graft-versus-leukemia reactions after bone marrow transplantation. Blood. 1990;75(3):555–562.
2. Warren EH, Deeg HJ. Dissecting graft-versus-leukemia from graft-versus-host-disease using novel strategies. Tissue Antigens. 2013;81(4):183–193.
3. Blazar BR, Murphy WJ, Abedi M. Advances in graft-versus-host disease biology and therapy. Nat Rev Immunol. 2012;12(6):443–458.
4. Deeg HJ, Antin JH. The clinical spectrum of acute graft-versus-host disease. Semin Hematol. 2006;43(1):24–31.
5. Cutler C, Antin JH. Manifestation and treatment of acute graft-versus-host-disease. In: Appelbaum F, Forman SJ, Negrin RS, Blume KG, eds. Thomas’ Hematopoietic Cell Transplantation. 4th ed. Hoboken, New Jersey, USA: Blackwell Publishing Ltd; 2009:1287–1303.
6. Martin PJ, et al. Increasingly frequent diagnosis of acute gastrointestinal graft-versus-host disease after allogeneic hematopoietic cell transplantation. Biol Blood Marrow Transpl. 2004;10(5):320–327.
7. MacMillan ML, et al. Response of 443 patients to steroids as primary therapy for acute graft-versus-host disease: comparison of grading systems. Biol Blood Marrow Transplant. 2002;8(7):387–394.
8. Paczesny S, et al. A biomarker panel for acute graft-versus-host disease. Blood. 2009;113(2):273–278.
9. Ferrara JL, et al. Regenerating islet-derived 3-α is a biomarker of gastrointestinal graft-versus-host disease. Blood. 2011;118(25):6702–6708.
10. Vander Lugt MT, et al. ST2 as a marker for risk of therapy-resistant graft-versus-host disease and death. N Engl J Med. 2013;369(6):529–539.
11. Hansen JA, et al. A novel soluble form of Tim-3 associated with severe graft-versus-host disease. Biol Blood Marrow Transplant. 2013;19(9):1323–1330.
12. McDonald GB, Tabellini L, Storer BE, Lawler RL, Martin PJ, Hansen JA. Plasma biomarkers of acute GVHD and nonrelapse mortality: predictive value of measurements before GVHD onset and treatment. Blood. 2015;126(1):113–120.
13. Levine JE, et al. A prognostic score for acute graft-versus-host disease based on biomarkers: a multicenter study. Lancet Haematol. 2015;2(1):e21–e29.
14. MacMillan ML, et al. A refined risk score for acute graft-versus-host disease that predicts response to initial therapy, survival, and transplant-related mortality. Biol Blood Marrow Transplant. 2015;21(4):761–767.
15. Lehmann JM, Riethmuller G, Johnson JP. MUC18, a marker of tumor progression in human melanoma, shows sequence similarity to the neural cell adhesion molecules of the immunoglobulin superfamily. Proc Natl Acad Sci U S A. 1989;86(24):9891–9895.
16. Lehmann JM, Holzmann B, Breitbart EW, Schmiegelow P, Riethmuller G, Johnson JP. Discrimination between benign and malignant cells of melanocytic lineage by two novel antigens, a glycoprotein with a molecular weight of 113,000 and a protein with a molecular weight of 76,000. Cancer Res. 1987;47(3):841–845.
17. Tsiolakidou G, Koutroubakis IE, Tzardi M, Kouroumalis EA. Increased expression of VEGF and CD146 in patients with inflammatory bowel disease. Dig Liver Dis. 2008;40(8):673–679.
18. Bardin N, et al. Increased expression of CD146, a new marker of the endothelial junction in active inflammatory bowel disease. Inflamm Bowel Dis. 2006;12(1):16–21.
19. Elshal MF, et al. A unique population of effector memory lymphocytes identified by CD146 having a distinct immunophenotypic and genomic profile. BMC Immunol. 2007;8:29.
20. Pickl WF, et al. MUC18/MCAM (CD146), an activation antigen of human T lymphocytes. J Immunol. 1997;158(5):2107–2115.
21. Elshal MF, Khan SS, Takahashi Y, Solomon MA, McCoy JP Jr. CD146 (Mel-CAM), an adhesion marker of endothelial cells, is a novel marker of lymphocyte subset activation in normal peripheral blood. Blood. 2005;106(8):2923–2924.
22. Larochelle C, et al. Melanoma cell adhesion molecule identifies encephalitogenic T lymphocytes and promotes their recruitment to the central nervous system. Brain. 2012;135(pt 10):2906–2924.
23. Guezguez B, Vigneron P, Lamerant N, Kieda C, Jaffredo T, Dunon D. Dual role of melanoma cell adhesion molecule (MCAM)/CD146 in lymphocyte endothelium interaction: MCAM/CD146 promotes rolling via microvilli induction in lymphocyte and is an endothelial adhesion receptor. J Immunol. 2007;179(10):6673–6685.
24. Xing S, et al. Targeting endothelial CD146 attenuates colitis and prevents colitis-associated carcinogenesis. Am J Pathol. 2014;184(5):1604–1616.
25. Schulz-Knappe P, et al. HCC-1, a novel chemokine from human plasma. J Exp Med. 1996;183(1):295–299.
26. Blain KY, et al. Structural and functional characterization of CC chemokine CCL14. Biochemistry. 2007;46(35):10008–10015.
27. Kotarsky K, et al. A novel role for constitutively expressed epithelial-derived chemokines as antibacterial peptides in the intestinal mucosa. Mucosal Immunol. 2010;3(1):40–48.
28. Detheux M, et al. Natural proteolytic processing of hemofiltrate CC chemokine 1 generates a potent CC chemokine receptor (CCR)1 and CCR5 agonist with anti-HIV properties. J Exp Med. 2000;192(10):1501–1508.
29. Wysocki CA, et al. Differential roles for CCR5 expression on donor T cells during graft-versus-host disease based on pretransplant conditioning. J Immunol. 2004;173(2):845–854.
30. Murai M, et al. Peyer’s patch is the essential site in initiating murine acute and lethal graft-versus-host reaction. Nat Immunol. 2003;4(2):154–160.
31. Palmer LA, et al. Chemokine receptor CCR5 mediates alloimmune responses in graft-versus-host disease. Biol Blood Marrow Transplant. 2010;16(3):311–319.
32. Reshef RLS, et al. Blockade of lymphocyte chemotaxis in visceral graft-versus-host disease. N Engl J Med. 2012;367(2):135–145.
33. Paczesny S, et al. Elafin is a biomarker of graft-versus-host disease of the skin. Sci Transl Med. 2010;2(13):13ra2.
34. Dagur PK, et al. MCAM-expressing CD4(+) T cells in peripheral blood secrete IL-17A and are significantly elevated in inflammatory autoimmune diseases. J Autoimmun. 2011;37(4):319–327.
35. Sallusto F, Lenig D, Forster R, Lipp M, Lanzavecchia A. Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature. 1999;401(6754):708–712.
36. Muranski P, et al. Th17 cells are long lived and retain a stem cell-like molecular signature. Immunity. 2011;35(6):972–985.
37. Wei S, Zhao E, Kryczek I, Zou W. Th17 cells have stem cell-like features and promote long-term immunity. Oncoimmunology. 2012;1(4):516–519.
38. Paulos CM, et al. The inducible costimulator (ICOS) is critical for the development of human T(H)17 cells. Sci Transl Med. 2010;2(55):55ra78.
39. Loetscher P, et al. CCR5 is characteristic of Th1 lymphocytes. Nature. 1998;391(6665):344–345.
40. Bossard C, et al. Plasmacytoid dendritic cells and Th17 immune response contribution in gastrointestinal acute graft-versus-host disease. Leukemia. 2012;26(7):1471–1474.
41. Annunziato F, et al. Phenotypic and functional features of human Th17 cells. J Exp Med. 2007;204(8):1849–1861.
42. Awasthi A, et al. Cutting edge: IL-23 receptor gfp reporter mice reveal distinct populations of IL-17-producing cells. J Immunol. 2009;182(10):5904–5908.
43. Das R, et al. Blockade of interleukin-23 signaling results in targeted protection of the colon and allows for separation of graft-versus-host and graft-versus-leukemia responses. Blood. 2010;115(25):5249–5258.
44. Lee Y, et al. Induction and molecular signature of pathogenic TH17 cells. Nat Immunol. 2012;13(10):991–999.
45. Kryczek I, et al. Human TH17 cells are long-lived effector memory cells. Sci Transl Med. 2011;3(104):104ra0.
46. + T cell STAT3 phosphorylation precedes acute GVHD, and subsequent Th17 tissue invasion correlates with GVHD severity and therapeutic response. J Leukoc Biol. 2015;97(4):807–819.
47. Fulton LM, et al. Attenuation of acute graft-versus-host disease in the absence of the transcription factor RORγt. J Immunol. 2012;189(4):1765–1772.
48. Yu Y, et al. Prevention of GVHD while sparing GVL effect by targeting Th1 and Th17 transcription factor T-bet and RORγt in mice. Blood. 2011;118(18):5011–5020.
49. Despoix N, et al. Mouse CD146/MCAM is a marker of natural killer cell maturation. Eur J Immunol. 2008;38(10):2855–2864.
50. + regulatory T cells preserve graft-versus-tumor activity while inhibiting graft-versus-host disease after bone marrow transplantation. Nat Med. 2003;9(9):1144–1150.
51. Magenau JM, et al. Frequency of CD4(+)CD25(hi)FOXP3(+) regulatory T cells has diagnostic and prognostic value as a biomarker for acute graft-versus-host-disease. Biol Blood Marrow Transplant. 2010;16(7):907–914.
52. Miura Y, et al. Association of Foxp3 regulatory gene expression with graft-versus-host disease. Blood. 2004;104(7):2187–2193.
53. Rezvani K, et al. High donor FOXP3-positive regulatory T-cell (Treg) content is associated with a low risk of GVHD following HLA-matched allogeneic SCT. Blood. 2006;108(4):1291–1297.
54. Duan H, et al. Targeting endothelial CD146 attenuates neuroinflammation by limiting lymphocyte extravasation to the CNS. Sci Rep. 2013;3:1687.
55. Flanagan K, et al. Laminin-411 is a vascular ligand for MCAM and facilitates TH17 cell entry into the CNS. PLoS One. 2012;7(7):e40443.
56. Ukena SN, et al. Human regulatory T cells in allogeneic stem cell transplantation. Blood. 2011;118(13):e82–e92.
57. Golovina TN, et al. CD28 costimulation is essential for human T regulatory expansion and function. J Immunol. 2008;181(4):2855–2868.
58. Weaver CT, Harrington LE, Mangan PR, Gavrieli M, Murphy KM. Th17: an effector CD4 T cell lineage with regulatory T cell ties. Immunity. 2006;24(6):677–688.
59. Nelson MH, et al. The inducible costimulator augments Tc17 cell responses to self and tumor tissue. J Immunol. 2015;194(4):1737–1747.
60. Zhang J, et al. ST2 blockade reduces sST2-producing T cells while maintaining protective mST2-expressing T cells during graft-versus-host disease. Sci Transl Med. 2015;7(308):308ra160.
61. Reichenbach DK, et al. The IL-33/ST2 axis augments effector T-cell responses during acute GVHD. Blood. 2015;125(20):3183–3192.
62. + T cells that induce GVHD without antileukemic effects. Blood. 2015;126(13):1609–1620.
63. Serody JS, Hill GR. The IL-17 differentiation pathway and its role in transplant outcome. Biol Blood Marrow Transplant. 2012;18(1 suppl):S56–S61.
64. Schneider-Hohendorf T, et al. VLA-4 blockade promotes differential routes into human CNS involving PSGL-1 rolling of T cells and MCAM-adhesion of TH17 cells. J Exp Med. 2014;211(9):1833–1846.
65. van der Waart AB, van der Velden WJ, Blijlevens NM, Dolstra H. Targeting the IL17 pathway for the prevention of graft-versus-host disease. Biol Blood Marrow Transplant. 2014;20(6):752–759.
66. Taylor PA, et al. Targeting of inducible costimulator (ICOS) expressed on alloreactive T cells down-regulates graft-versus-host disease (GVHD) and facilitates engraftment of allogeneic bone marrow (BM). Blood. 2005;105(8):3372–3380.
67. Tajima N, et al. JTA-009, a fully human antibody against human AILIM/ICOS, ameliorates graft-vs-host reaction in SCID mice grafted with human PBMCs. Exp Hematol. 2008;36(11):1514–1523.
68. + T cells. Cancer Res. 2012;72(23):6130–6141.
69. Hanauer DA, Mei Q, Law J, Khanna R, Zheng K. Supporting information retrieval from electronic health records: A report of University of Michigan’s nine-year experience in developing and using the Electronic Medical Record Search Engine (EMERSE). J Biomed Inform. 2015;55:290–300.
70. Lerner KG, Kao GF, Storb R, Buckner CD, Clift RA, Thomas ED. Histopathology of graft-vs.-host reaction (GvHR) in human recipients of marrow from HL-A-matched sibling donors. Transplant Proc. 1974;6(4):367–371.
71. Wiek C, et al. Identification of amino acid determinants in CYP4B1 for optimal catalytic processing of 4-ipomeanol. Biochem J. 2015;465(1):103–114.
72. Hanenberg H, Xiao XL, Dilloo D, Hashino K, Kato I, Williams DA. Colocalization of retrovirus and target cells on specific fibronectin fragments increases genetic transduction of mammalian cells. Nat Med. 1996;2(8):876–882.
73. Wu Q, et al. A novel function of MUC18: amplification of lung inflammation during bacterial infection. Am J Pathol. 2013;182(3):819–827.
74. Tawara I, et al. Interleukin-6 modulates graft-versus-host responses after experimental allogeneic bone marrow transplantation. Clin Cancer Res. 2011;17(1):77–88.
75. Reddy P, et al. Histone deacetylase inhibition modulates indoleamine 2,3-dioxygenase-dependent DC functions and regulates experimental graft-versus-host disease in mice. J Clin Invest. 2008;118(7):2562–2573.
76. Cooke KR, et al. An experimental model of idiopathic pneumonia syndrome after bone marrow transplantation: I. The roles of minor H antigens and endotoxin. Blood. 1996;88(8):3230–3239.
77. Fine JP, Gray RJ. A proportional hazards model for the subdistribution of a competing risk. J Am Stat Assoc. 1999;94:496–509.