Next generation treatment of acute graft-versus-host disease

Leukemia

Volumn 28, Issue 12, 2014, Pages 2283-2291

  Magenau, J ^a   Reddy, P ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA 1 ANTITRYPSIN; CHEMOKINE RECEPTOR CCR5; CRYOPYRIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1; INTERLEUKIN 21; INTERLEUKIN 23; INTERLEUKIN 6; JANUS KINASE 2; MICRORNA; NOTCH RECEPTOR; PROTEIN KINASE SYK; PURINERGIC P2X7 RECEPTOR; SIALIC ACID BINDING IMMUNOGLOBULIN LIKE LECTIN; STAT3 PROTEIN; TUMOR NECROSIS FACTOR ALPHA; AUTACOID; CYTOKINE; IMMUNOGLOBULIN RECEPTOR;

ACUTE GRAFT VERSUS HOST DISEASE; BIOENERGY; CELL ADHESION; CELL EXPANSION; CLINICAL TRIAL (TOPIC); DNA METHYLATION; DNA MODIFICATION; EPIGENETICS; EX VIVO STUDY; HISTONE ACETYLATION; HISTONE METHYLATION; HUMAN; IMMUNE RESPONSE; IMMUNOREGULATION; INTRACELLULAR SIGNALING; INVARIANT NATURAL KILLER T CELL; MICROBIOME; NATURAL KILLER T CELL; NEDDYLATION; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; REVIEW; TISSUE INJURY; TRANSCRIPTION REGULATION; TRANSLATION REGULATION; ACUTE DISEASE; ANIMAL; EXTRACELLULAR SPACE; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GRAFT VS HOST DISEASE; IMMUNOLOGY; INTRACELLULAR SPACE; METABOLISM; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION;

ACUTE DISEASE; ANIMALS; CYTOKINES; EXTRACELLULAR SPACE; GENE EXPRESSION REGULATION; GRAFT VS HOST DISEASE; HUMANS; INFLAMMATION MEDIATORS; INTRACELLULAR SPACE; PROTEIN BIOSYNTHESIS; RECEPTORS, IMMUNOLOGIC; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC;

EID: 84925286568     PISSN: 08876924     EISSN: 14765551     Source Type: Journal    
DOI: 10.1038/leu.2014.195     Document Type: Review

References (86)

1. Storb R, Gyurkocza B, Storer BE, Sorror ML, Blume K, Niederwieser D et al. Graft-versus-host disease and graft-versus-tumor effects after allogeneic hematopoietic cell transplantation. J Clin Oncol 2013; 31: 1530-1538.
2. Pasquini MC WZ. Current use and outcome of hematopoietic stem cell transplantation: CIBMTR Summary Slides. 2011. Available at http://wwwcibmtrorg.
3. Jagasia M, Arora M, Flowers ME, Chao NJ, McCarthy PL, Cutler CS et al. Risk factors for acute GVHD and survival after hematopoietic cell transplantation. Blood 2012; 119: 296-307.
4. Marr KA, Carter RA, Boeckh M, Martin P, Corey L. Invasive aspergillosis in allogeneic stem cell transplant recipients: changes in epidemiology and risk factors. Blood 2002; 100: 4358-4366.
5. Billingham RE. The biology of graft-versus-host reactions. Harvey Lect 1966; 62: 21-78.
6. Korngold R, Sprent J. Lethal graft-versus-host disease after bone marrow transplantation across minor histocompatibility barriers in mice. Prevention by removing mature T cells from marrow. J Exp Med 1978; 148: 1687-1698.
7. Paczesny S, Hanauer D, Sun Y, Reddy P. New perspectives on the biology of acute GVHD. Bone Marrow Transplant 2010; 45: 1-11.
8. Ruutu T, van Biezen A, Hertenstein B, Henseler A, Garderet L, Passweg J et al. Prophylaxis and treatment of GVHD after allogeneic haematopoietic SCT: a survey of centre strategies by the European Group for Blood and Marrow Transplantation. Bone Marrow Transplant 2012; 47: 1459-1464.
9. Ram R, Storb R. Pharmacologic prophylaxis regimens for acute graft-versus-host disease: past, present and future. Leuk Lymphoma 2013; 54: 1591-1601.
10. Gooley TA, Chien JW, Pergam SA, Hingorani S, Sorror ML, Boeckh M et al. Reduced mortality after allogeneic hematopoietic-cell transplantation. N Engl J Med 2010; 363: 2091-2101.
11. MacMillan ML, DeFor TE, Weisdorf DJ. The best endpoint for acute GVHD treatment trials. Blood 2010; 115: 5412-5417.
12. Antin JH, Weisdorf D, Neuberg D, Nicklow R, Clouthier S, Lee SJ et al. Interleukin-1 blockade does not prevent acute graft-versus-host disease: results of a randomized, double-blind, placebo-controlled trial of interleukin-1 receptor antagonist in allogeneic bone marrow transplantation. Blood 2002; 100: 3479-3482.
13. Levine JE, Paczesny S, Mineishi S, Braun T, Choi SW, Hutchinson RJ et al. Etanercept plus methylprednisolone as initial therapy for acute graft-versus-host disease. Blood 2008; 111: 2470-2475.
14. Chen X, Das R, Komorowski R, Beres A, Hessner MJ, Mihara M et al. Blockade of interleukin-6 signaling augments regulatory T-cell reconstitution and attenuates the severity of graft-versus-host disease. Blood 2009; 114: 891-900.
15. Tawara I, Koyama M, Liu C, Toubai T, Thomas D, Evers R et al. Interleukin-6 modulates graft-versus-host responses after experimental allogeneic bone marrow transplantation. Clin Cancer Res 2011; 17: 77-88.
16. Drobyski WR, Pasquini M, Kovatovic K, Palmer J, Douglas Rizzo J, Saad A et al. Tocilizumab for the treatment of steroid refractory graft-versus-host disease. Biol Blood Marrow Transplant 2011; 17: 1862-1868.
17. Kennedy GA, Varelias A, Vuckovic S, Zhang P, MacDonald K, Leach J et al. The addition of interleukin-6 inhibition to standard Gvhd prophylaxis prevents acute Gvhd: interim results of a phase I/II clinical study. ASH Ann Meet Absr 2013; 122: 908.
18. Bucher C, Koch L, Vogtenhuber C, Goren E, Munger M, Panoskaltsis-Mortari A et al. IL-21 blockade reduces graft-versus-host disease mortality by supporting inducible T regulatory cell generation. Blood 2009; 114: 5375-5384.
19. Hippen KL, Bucher C, Schirm DK, Bearl AM, Brender T, Mink KA et al. Blocking IL-21 signaling ameliorates xenogeneic GVHD induced by human lymphocytes. Blood 2012; 119: 619-628.
20. Das R, Chen X, Komorowski R, Hessner MJ, Drobyski WR. Interleukin-23 secretion by donor antigen-presenting cells is critical for organ-specific pathology in graft-versus-host disease. Blood 2009; 113: 2352-2362.
21. Murai M, Yoneyama H, Harada A, Yi Z, Vestergaard C, Guo B et al. Active participation of CCR5(+)CD8(+) T lymphocytes in the pathogenesis of liver injury in graft-versus-host disease. J Clin Invest 1999; 104: 49-57.
22. Bogunia-Kubik K, Duda D, Suchnicki K, Lange A. CCR5 deletion mutation and its association with the risk of developing acute graft-versus-host disease after allogeneic hematopoietic stem cell transplantation. Haematologica 2006; 91: 1628-1634.
23. Wysocki CA, Burkett SB, Panoskaltsis-Mortari A, Kirby SL, Luster AD, McKinnon K et al. Differential roles for CCR5 expression on donor T cells during graft-versushost disease based on pretransplant conditioning. J Immunol 2004; 173: 845-854.
24. Reshef R, Luger SM, Hexner EO, Loren AW, Frey NV, Nasta SD et al. Blockade of lymphocyte chemotaxis in visceral graft-versus-host disease. N Engl J Med 2012; 367: 135-145.
25. Hanash AM, Dudakov JA, Hua G, O'Connor MH, Young LF, Singer NV et al. Interleukin-22 protects intestinal stem cells from immune-mediated tissue damage and regulates sensitivity to graft versus host disease. Immunity 2012; 37: 339-350.
26. Takashima S, Kadowaki M, Aoyama K, Koyama M, Oshima T, Tomizuka K et al. The Wnt agonist R-spondin1 regulates systemic graft-versus-host disease by protecting intestinal stem cells. J Exp Med 2011; 208: 285-294.
27. Silverman EK, Sandhaus RA. Clinical practice. Alpha1-antitrypsin deficiency. N Engl J Med 2009; 360: 2749-2757.
28. Lewis EC, Shapiro L, Bowers OJ, Dinarello CA. Alpha1-antitrypsin monotherapy prolongs islet allograft survival in mice. Proc Natl Acad Sci USA 2005; 102: 12153-12158.
29. Tawara I, Sun Y, Lewis EC, Toubai T, Evers R, Nieves E et al. Alpha-1-antitrypsin monotherapy reduces graft-versus-host disease after experimental allogeneic bone marrow transplantation. Proc Natl Acad Sci USA 2012; 109: 564-569.
30. Marcondes AM, Li X, Tabellini L, Bartenstein M, Kabacka J, Sale GE et al. Inhibition of IL-32 activation by alpha-1 antitrypsin suppresses alloreactivity and increases survival in an allogeneic murine marrow transplantation model. Blood 2011; 118: 5031-5039.
31. Brennan TV, Lin L, Huang X, Cardona DM, Li Z, Dredge K et al. Heparan sulfate, an endogenous TLR4 agonist, promotes acute GVHD after allogeneic stem cell transplantation. Blood 2012; 120: 2899-2908.
32. Rodriguez-Otero P, Porcher R, Peffault de Latour R, Contreras M, Bouhnik Y, Xhaard A et al. Fecal calprotectin and alpha-1 antitrypsin predict severity and response to corticosteroids in gastrointestinal graft-versus-host disease. Blood 2012; 119: 5909-5917.
33. Shibuya A, Campbell D, Hannum C, Yssel H, Franz-Bacon K, McClanahan T et al. DNAM-1, a novel adhesion molecule involved in the cytolytic function of T lymphocytes. Immunity 1996; 4: 573-581.
34. Nabekura T, Shibuya K, Takenaka E, Kai H, Shibata K, Yamashita Y et al. Critical role of DNAX accessory molecule-1 (DNAM-1) in the development of acute graft-versus-host disease in mice. Proc Natl Acad Sci USA 2010; 107: 18593-18598.
35. Koyama M, Kuns RD, Olver SD, Lineburg KE, Lor M, Teal BE et al. Promoting regulation via the inhibition of DNAM-1 after transplantation. Blood 2013; 121: 3511-3520.
36. Zhang Y, Sandy AR, Wang J, Radojcic V, Shan GT, Tran IT et al. Notch signaling is a critical regulator of allogeneic CD4+ T-cell responses mediating graft-versus-host disease. Blood 2011; 117: 299-308.
37. Toubai T, Sun Y, Tawara I, Friedman A, Liu C, Evers R et al. Ikaros-Notch axis in host hematopoietic cells regulates experimental graft-versus-host disease. Blood 2011; 118: 192-204.
38. Wilhelm K, Ganesan J, Muller T, Durr C, Grimm M, Beilhack A et al. Graft-versushost disease is enhanced by extracellular ATP activating P2×7R. Nat Med 2010; 16: 1434-1438.
39. Jankovic D, Ganesan J, Bscheider M, Stickel N, Weber FC, Guarda G et al. The Nlrp3 inflammasome regulates acute graft-versus-host disease. J Exp Med 2013; 210: 1899-1910.
40. Crocker PR, Paulson JC, Varki A. Siglecs and their roles in the immune system. Nat Rev Immunol 2007; 7: 255-266.
41. Toubai T, Hou G, Mathewson N, Liu C, Wang Y, Oravecz-Wilson K et al. Siglec-G-CD24 axis controls the severity of graft-versus-host disease in mice. Blood 2014; 123: 3512-3523.
42. van Bekkum DW. Bone marrow transplantation. Transplant Proc 1977; 9: 147-154.
43. Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, Sargent M et al. Diversity of the human intestinal microbial flora. Science 2005; 308: 1635-1638.
44. Eriguchi Y, Takashima S, Oka H, Shimoji S, Nakamura K, Uryu H et al. Graft-versus-host disease disrupts intestinal microbial ecology by inhibiting Paneth cell production of alpha-defensins. Blood 2012; 120: 223-231.
45. Jenq RR, Ubeda C, Taur Y, Menezes CC, Khanin R, Dudakov JA et al. Regulation of intestinal inflammation by microbiota following allogeneic bone marrow transplantation. J Exp Med 2012; 209: 903-911.
46. Tawara I, Liu C, Tamaki H, Toubai T, Sun Y, Evers R et al. Influence of donor microbiota on the severity of experimental graft-versus-host-disease. Biol Blood Marrow Transplant 2013; 19: 164-168.
47. Holler E, Butzhammer P, Schmid K, Hundsrucker C, Koestler J, Peter K et al. Metagenomic analysis of the stool microbiome in patients receiving allogeneic SCT: Loss of diversity is associated with use of systemic antibiotics and more pronounced in gastrointestinal GvHD. Biol Blood Marrow Transplant 2014; 20: 640-645.
48. Levine JE, Huber E, Hammer ST, Harris AC, Greenson JK, Braun TM et al. Low Paneth cell numbers at onset of gastrointestinal graft-versus-host disease identify patients at high risk for nonrelapse mortality. Blood 2013; 122: 1505-1509.
49. Edinger M, Hoffmann P, Ermann J, Drago K, Fathman CG, Strober S et al. CD4(+)CD25(+) regulatory T cells preserve graft-versus-tumor activity while inhibiting graft-versus-host disease after bone marrow transplantation. Nat Med 2003; 9: 1144-1150.
50. Hoffmann P, Ermann J, Edinger M, Fathman CG, Strober S. Donor-type CD4(+) CD25(+) regulatory T cells suppress lethal acute graft-versus-host disease after allogeneic bone marrow transplantation. J Exp Med 2002; 196: 389-399.
51. Di Ianni M, Falzetti F, Carotti A, Terenzi A, Castellino F, Bonifacio E et al. Tregs prevent GVHD and promote immune reconstitution in HLA-haploidentical transplantation. Blood 2011; 117: 3921-3928.
52. Brunstein CG, Miller JS, Cao Q, McKenna DH, Hippen KL, Curtsinger J et al. Infusion of ex vivo expanded T regulatory cells in adults transplanted with umbilical cord blood: safety profile and detection kinetics. Blood 2011; 117: 1061-1070.
53. Chaidos A, Patterson S, Szydlo R, Chaudhry MS, Dazzi F, Kanfer E et al. Graft invariant natural killer T-cell dose predicts risk of acute graft-versus-host disease in allogeneic hematopoietic stem cell transplantation. Blood 2012; 119: 5030-5036.
54. Juno JA, Keynan Y, Fowke KR. Invariant NKT cells: regulation and function during viral infection. PLoS Pathog 2012; 8: e1002838.
55. Rubio MT, Moreira-Teixeira L, Bachy E, Bouillie M, Milpied P, Coman T et al. Early posttransplantation donor-derived invariant natural killer T-cell recovery predicts the occurrence of acute graft-versus-host disease and overall survival. Blood 2012; 120: 2144-2154.
56. Schneidawind D, Pierini A, Alvarez M, Pan Y, Baker J, Kim B et al. CD4+ invariant natural killer T cells protect from acute graft-versus-host disease lethality through a dramatic expansion of donor-derived CD4+FoxP3+ regulatory T cells. Biol Blood Marrow Transplant 2014; 20: S23.
57. Betts BC, Abdel-Wahab O, Curran St SA, Angelo ET, Koppikar P, Heller G et al. Janus kinase-2 inhibition induces durable tolerance to alloantigen by human dendritic cell-stimulated T cells yet preserves immunity to recall antigen. Blood 2011; 118: 5330-5339.
58. Spoerl S, Mathew NR, Bscheider M, Schmitt-Graeff A, Chen S, Mueller T et al. Activity of therapeutic JAK 1/2 blockade in graft-versus-host disease. Blood 2014; 123: 3832-3842.
59. Park HB, Oh K, Garmaa N, Seo MW, Byoun OJ, Lee HY et al. CP-690550, a Janus kinase inhibitor, suppresses CD4+ T-cell-mediated acute graft-versus-host disease by inhibiting the interferon-gamma pathway. Transplantation 2010; 90: 825-835.
60. Leonhardt F, Zirlik K, Buchner M, Prinz G, Hechinger AK, Gerlach UV et al. Spleen tyrosine kinase (Syk) is a potent target for GvHD prevention at different cellular levels. Leukemia 2012; 26: 1617-1629.
61. Radojcic V, Pletneva MA, Yen HR, Ivcevic S, Panoskaltsis-Mortari A, Gilliam AC et al. STAT3 signaling in CD4+ T cells is critical for the pathogenesis of chronic sclerodermatous graft-versus-host disease in a murine model. J Immunol 2010; 184: 764-774.
62. Lu SX, Alpdogan O, Lin J, Balderas R, Campos-Gonzalez R, Wang X et al. STAT-3 and ERK 1/2 phosphorylation are critical for T-cell alloactivation and graft-versushost disease. Blood 2008; 112: 5254-5258.
63. Laurence A, Amarnath S, Mariotti J, Kim YC, Foley J, Eckhaus M et al. STAT3 transcription factor promotes instability of nTreg cells and limits generation of iTreg cells during acute murine graft-versus-host disease. Immunity 2012; 37: 209-222.
64. Sun Y, Chin YE, Weisiger E, Malter C, Tawara I, Toubai T et al. Cutting edge: Negative regulation of dendritic cells through acetylation of the nonhistone protein STAT-3. J Immunol 2009; 182: 5899-5903.
65. Lawrence T. The nuclear factor NF-kappaB pathway in inflammation. Cold Spring Harb Perspect Biol 2009; 1: a001651.
66. MacDonald KP, Kuns RD, Rowe V, Morris ES, Banovic T, Bofinger H et al. Effector and regulatory T-cell function is differentially regulated by RelB within antigen-presenting cells during GVHD. Blood 2007; 109: 5049-5057.
67. Murray SE, Polesso F, Rowe AM, Basak S, Koguchi Y, Toren KG et al. NF-kappaBinducing kinase plays an essential T cell-intrinsic role in graft-versus-host disease and lethal autoimmunity in mice. J Clin Invest 2011; 121: 4775-4786.
68. Shono YTA, Liou H, Atlan-Bonnet G, Tsai J, Smith O, West M et al. Inhibition of c-Rel signaling: A novel small molecule-based therapy diminishing T cell alloactivation while preserving anti-tumor activity. ASH Annual Meeting Abstracts 2012; 120: 454.
69. Gatza E, Wahl DR, Opipari AW, Sundberg TB, Reddy P, Liu C et al. Manipulating the bioenergetics of alloreactive T cells causes their selective apoptosis and arrests graft-versus-host disease. Sci Transl Med 2011; 3: 67ra8.
70. Byersdorfer CA, Tkachev V, Opipari AW, Goodell S, Swanson J, Sandquist S et al. Effector T cells require fatty acid metabolism during murine graft-versus-host disease. Blood 2013; 122: 3230-3237.
71. Wang M, Medeiros BC, Erba HP, DeAngelo DJ, Giles FJ, Swords RT. Targeting protein neddylation: a novel therapeutic strategy for the treatment of cancer. Expert Opin Ther Targets 2011; 15: 253-264.
72. Mathewson N, Toubai T, Sun Y, Wang Y, Oravecz-Wilson K, Hou G. Targeting Sag in Donor T Cells As a Novel Strategy for Reducing GVHD. Biol Blood Marrow Transplant 2014; 20: S23.
73. Koreth J, Stevenson KE, Kim HT, McDonough SM, Bindra B, Armand P et al. Bortezomib-based graft-versus-host disease prophylaxis in HLA-mismatched unrelated donor transplantation. J Clin Oncol 2012; 30: 3202-3208.
74. Sun K, Welniak LA, Panoskaltsis-Mortari A, O'Shaughnessy MJ, Liu H, Barao I et al. Inhibition of acute graft-versus-host disease with retention of graft-versus-tumor effects by the proteasome inhibitor bortezomib. Proc Natl Acad Sci USA 2004; 101: 8120-8125.
75. Choi J, Ritchey J, Prior JL, Holt M, Shannon WD, Deych E et al. In vivo administration of hypomethylating agents mitigate graft-versus-host disease without sacrificing graft-versus-leukemia. Blood 2010; 116: 129-139.
76. de Lima M, Giralt S, Thall PF, de Padua Silva L, Jones RB, Komanduri K et al. Maintenance therapy with low-dose azacitidine after allogeneic hematopoietic stem cell transplantation for recurrent acute myelogenous leukemia or myelodysplastic syndrome: a dose and schedule finding study. Cancer 2010; 116: 5420-5431.
77. Goodyear OC, Dennis M, Jilani NY, Loke J, Siddique S, Ryan G et al. Azacitidine augments expansion of regulatory T cells after allogeneic stem cell transplantation in patients with acute myeloid leukemia (AML). Blood 2012; 119: 3361-3369.
78. Reddy P, Sun Y, Toubai T, Duran-Struuck R, Clouthier SG, Weisiger E 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: 2562-2573.
79. Jasperson LK, Bucher C, Panoskaltsis-Mortari A, Mellor AL, Munn DH, Blazar BR. Inducing the tryptophan catabolic pathway, indoleamine 2,3-dioxygenase (IDO), for suppression of graft-versus-host disease (GVHD) lethality. Blood 2009; 114: 5062-5070.
80. Wang D, Iclozan C, Liu C, Xia C, Anasetti C, Yu XZ. LBH589 enhances T cell activation in vivo and accelerates graft-versus-host disease in mice. Biol Blood Marrow Transplant 2012; 18: 1182-90 e1.
81. Choi SW, Braun T, Chang L, Ferrara JL, Pawarode A, Magenau JM et al. Vorinostat plus tacrolimus and mycophenolate to prevent graft-versus-host disease after related-donor reduced-intensity conditioning allogeneic haemopoietic stem-cell transplantation: a phase 1/2 trial. Lancet Oncol 2014; 15: 87-95.
82. He S, Wang J, Kato K, Xie F, Varambally S, Mineishi S et al. Inhibition of histone methylation arrests ongoing graft-versus-host disease in mice by selectively inducing apoptosis of alloreactive effector T cells. Blood 2012; 119: 1274-1282.
83. Ranganathan P, Heaphy CE, Costinean S, Stauffer N, Na C, Hamadani M et al. Regulation of acute graft-versus-host disease by microRNA-155. Blood 2012; 119: 4786-4797.
84. Sun Y, Varambally S, Maher CA, Cao Q, Chockley P, Toubai T et al. Targeting of microRNA-142-3p in dendritic cells regulates endotoxin-induced mortality. Blood 2011; 117: 6172-6183.
85. Sun Y, Oravecz-Wilson K, Saunders T, Wang Y, Toubai T, Mathewson N. Atypical E2F Dependent Dysregulation Of Cell Cycling By Microrna-142 Regulates T-Cell Responses and Experimental Graft-Versus-Host Disease. ASH Annual Meeting Abstracts 2013; 122: 136.
86. Sun Y, Tawara I, Zhao M, Qin ZS, Toubai T, Mathewson N et al. Allogeneic T cell responses are regulated by a specific miRNA-mRNA network. J Clin Invest 2013; 123: 4739-4754.