Efficacy, durability, and response predictors of low-dose interleukin-2 therapy for chronic graft-versus-host disease

Blood

Volumn 128, Issue 1, 2016, Pages 130-137

  Koreth, John ^a   Kim, Haesook T ^b   Jones, Kyle T ^b   Lange, Paulina B ^b   Reynolds, Carol G ^b   Chammas, Marie J ^b   Dusenbury, Katherine ^b   Whangbo, Jennifer ^b   Nikiforow, Sarah ^b   Alyea, Edwin P ^b   Armand, Philippe ^b   Cutler, Corey S ^b   Ho, Vincent T ^b   Chen, Yi Bin ^c   Avigan, David ^c   Blazar, Bruce R ^d   Antin, Joseph H ^a   Ritz, Jerome ^a   Soiffer, Robert J ^a  

^a DANA FARBER CANCER INSTITUTE   (United States)

^b HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALDESLEUKIN; INTERLEUKIN 2; IL2 PROTEIN, HUMAN;

ADULT; AGED; ALLOIMMUNITY; ARTHRALGIA; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CHRONIC GRAFT VERSUS HOST DISEASE; CLINICAL ARTICLE; CLINICAL EVALUATION; COHORT ANALYSIS; DEEP VEIN THROMBOSIS; DRUG DOSE REDUCTION; DRUG EFFICACY; DRUG WITHDRAWAL; FASCIA; FATIGUE; FEMALE; FOLLOW UP; GASTROINTESTINAL TRACT; HUMAN; IMMUNE RESPONSE; IN VIVO STUDY; INJECTION SITE INDURATION; INJECTION SITE PAIN; JOINT; LIVER; LOW DRUG DOSE; LUNG; LUNG INFECTION; MALAISE; MALE; MUSCLE; MYALGIA; NATURAL KILLER CELL; PHASE 1 CLINICAL TRIAL; PHASE 2 CLINICAL TRIAL; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; RESPIRATORY SYNCYTIAL VIRUS INFECTION; SKIN; STREPTOCOCCUS VIRIDANS INFECTION; THROMBOCYTOPENIA; TREATMENT RESPONSE; BLOOD; CHRONIC DISEASE; CLINICAL TRIAL; GRAFT VS HOST DISEASE; LYMPHOCYTE COUNT; MIDDLE AGED; TIME FACTOR;

ADULT; AGED; CHRONIC DISEASE; FEMALE; FOLLOW-UP STUDIES; GRAFT VS HOST DISEASE; HUMANS; INTERLEUKIN-2; KILLER CELLS, NATURAL; LYMPHOCYTE COUNT; MALE; MIDDLE AGED; T-LYMPHOCYTES, REGULATORY; TIME FACTORS;

EID: 84977609937     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2016-02-702852     Document Type: Article

References (41)

1. Pidala J, Kurland B, Chai X, et al. Patient-reported quality of life is associated with severity of chronic graft-versus-host disease as measured by NIH criteria: Report on baseline data from the Chronic GVHD Consortium. Blood. 2011;117(17): 4651-4657.
2. Socié G, Ritz J. Current issues in chronic graft-versus-host disease. Blood. 2014;124(3): 374-384.
3. Flowers ME, Martin PJ. How we treat chronic graft-versus-host disease. Blood. 2015;125(4): 606-615.
4. Piccirillo CA, Shevach EM. Naturally-occurring CD41CD251 immunoregulatory T cells: central players in the arena of peripheral tolerance. Semin Immunol. 2004;16(2):81-88.
5. Fehérvari Z, Sakaguchi S. Development and function of CD251CD41 regulatory T cells. Curr Opin Immunol. 2004;16(2):203-208.
6. Azuma T, Takahashi T, Kunisato A, Kitamura T, Hirai H. Human CD41 CD251 regulatory T cells suppress NKT cell functions. Cancer Res. 2003; 63(15):4516-4520.
7. Cederbom L, Hall H, Ivars F. CD41CD251 regulatory T cells down-regulate co-stimulatory molecules on antigen-presenting cells. Eur J Immunol. 2000;30(6):1538-1543.
8. Maloy KJ, Salaun L, Cahill R, Dougan G, Saunders NJ, Powrie F. CD41CD251 T(R) cells suppress innate immune pathology through cytokine-dependent mechanisms. J Exp Med. 2003;197(1):111-119.
9. Serra P, Amrani A, Yamanouchi J, et al. CD40 ligation releases immature dendritic cells from the control of regulatory CD41CD251 T cells. Immunity. 2003;19(6):877-889.
10. Thornton AM, Shevach EM. CD41CD251 immunoregulatory T cells suppress polyclonal T cell activation in vitro by inhibiting interleukin 2 production. J Exp Med. 1998;188(2):287-296.
11. Janssens W, Carlier V, Wu B, VanderElst L, Jacquemin MG, Saint-Remy JM. CD41CD251 T cells lyse antigen-presenting B cells by Fas-Fas ligand interaction in an epitope-specific manner. J Immunol. 2003;171(9):4604-4612.
12. Zorn E, Kim HT, Lee SJ, et al. Reduced frequency of FOXP31 CD41CD251 regulatory T cells in patients with chronic graft-versus-host disease. Blood. 2005;106(8):2903-2911.
13. Matsuoka K, Kim HT, McDonough S, et al. Altered regulatory T cell homeostasis in patients with CD41 lymphopenia following allogeneic hematopoietic stem cell transplantation. J Clin Invest. 2010;120(5):1479-1493.
14. Buckner JH. Mechanisms of impaired regulation by CD4(1)CD25(1)FOXP3(1) regulatory T cells in human autoimmune diseases. Nat Rev Immunol. 2010;10(12):849-859.
15. Hoffmann P, Ermann J, Edinger M, Fathman CG, Strober S. Donor-type CD4(1)CD25(1) regulatory T cells suppress lethal acute graftversus- host disease after allogeneic bone marrow transplantation. J Exp Med. 2002;196(3):389-399.
16. Taylor PA, Lees CJ, Blazar BR. The infusion of ex vivo activated and expanded CD4(1)CD25(1) immune regulatory cells inhibits graft-versus-host disease lethality. Blood. 2002;99(10):3493-3499.
17. Edinger M, Hoffmann P, Ermann J, et al. CD41 CD251 regulatory T cells preserve graft-versustumor activity while inhibiting graft-versus-host disease after bone marrow transplantation. Nat Med. 2003;9(9):1144-1150.
18. Malek TR, Bayer AL. Tolerance, not immunity, crucially depends on IL-2. Nat Rev Immunol. 2004;4(9):665-674.
19. Nelson BH. IL-2, regulatory T cells, and tolerance. J Immunol. 2004;172(7):3983-3988.
20. Koreth J, Matsuoka K, Kim HT, et al. Interleukin-2 and regulatory T cells in graft-versus-host disease. N Engl J Med. 2011;365(22):2055-2066.
21. Matsuoka K, Koreth J, Kim HT, et al. Low-dose interleukin-2 therapy restores regulatory T cell homeostasis in patients with chronic graft-versushost disease. Sci Transl Med. 2013;5(179): 179ra43.
22. Filipovich AH, Weisdorf D, Pavletic S, et al. National Institutes of Health consensus development project on criteria for clinical trials in chronic graft-versus-host disease: I. Diagnosis and staging working group report. Biol Blood Marrow Transplant. 2005;11(12):945-956.
23. Pavletic SZ, Martin P, Lee SJ, et al; Response Criteria Working Group. Measuring therapeutic response in chronic graft-versus-host disease: National Institutes of Health Consensus Development Project on Criteria for Clinical Trials in Chronic Graft-versus-Host Disease: IV. Response Criteria Working Group report. Biol Blood Marrow Transplant. 2006;12(3):252-266.
24. Lee SJ, Wolff D, Kitko C, et al. Measuring therapeutic response in chronic graft-versus-host disease. National Institutes of Health consensus development project on criteria for clinical trials in chronic graft-versus-host disease: IV. The 2014 Response Criteria Working Group report. Biol Blood Marrow Transplant. 2015;21(6):984-999.
25. Lee S, Cook EF, Soiffer R, Antin JH. Development and validation of a scale to measure symptoms of chronic graft-versus-host disease. Biol Blood Marrow Transplant. 2002;8(8):444-452.
26. Gray R. A class of k-sample tests for comparing the cumulative incidence of a competing risk. Ann Stat. 1988;16:1141-1154.
27. Van Gool F, Molofsky AB, Morar MM, et al. Interleukin-5-producing group 2 innate lymphoid cells control eosinophilia induced by interleukin-2 therapy. Blood. 2014;124(24):3572-3576.
28. Brunstein CG, Miller JS, Cao Q, 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(3): 1061-1070.
29. Di Ianni M, Falzetti F, Carotti A, et al. Tregs prevent GVHD and promote immune reconstitution in HLA-haploidentical transplantation. Blood. 2011;117(14):3921-3928.
30. Brunstein CG, Miller JS, McKenna DH, et al. Umbilical cord blood-derived T regulatory cells to prevent GVHD: kinetics, toxicity profile, and clinical effect. Blood. 2016;127(8):1044-1051.
31. Ito S, Bollard CM, Carlsten M, et al. Ultra-low dose interleukin-2 promotes immune-modulating function of regulatory T cells and natural killer cells in healthy volunteers. Mol Ther. 2014;22(7): 1388-1395.
32. Kennedy-Nasser AA, Ku S, Castillo-Caro P, et al. Ultra low-dose IL-2 for GVHD prophylaxis after allogeneic hematopoietic stem cell transplantation mediates expansion of regulatory T cells without diminishing antiviral and antileukemic activity. Clin Cancer Res. 2014;20(8):2215-2225.
33. Saadoun D, Rosenzwajg M, Joly F, et al. Regulatory T-cell responses to low-dose interleukin-2 in HCV-induced vasculitis. N Engl J Med. 2011;365(22):2067-2077.
34. Hartemann A, Bensimon G, Payan CA, et al. Lowdose interleukin 2 in patients with type 1 diabetes: A phase 1/2 randomised, double-blind, placebocontrolled trial. Lancet Diabetes Endocrinol. 2013; 1(4):295-305.
35. Humrich JY, von Spee-Mayer C, Siegert E, et al. Rapid induction of clinical remission by low-dose interleukin-2 in a patient with refractory SLE. Ann Rheum Dis. 2015;74(4):791-792.
36. Castela E, Le Duff F, Butori C, et al. Effects of low-dose recombinant interleukin 2 to promote T-regulatory cells in alopecia areata. JAMA Dermatol. 2014;150(7):748-751.
37. Jacobsohn DA, Kurland BF, Pidala J, et al. Correlation between NIH composite skin score, patient-reported skin score, and outcome: Results from the Chronic GVHD Consortium. Blood. 2012; 120(13):2545-2552.
38. Ruutu T, Gratwohl A, de Witte T, et al. Prophylaxis and treatment of GVHD: EBMT-ELN working group recommendations for a standardized practice [published correction appears in Bone Marrow Transplant. 2014;49(2): 319]. Bone Marrow Transplant. 2014;49(2): 168-173.
39. Palmer JM, Lee SJ, Chai X, et al. Poor agreement between clinician response ratings and calculated response measures in patients with chronic graftversus- host disease. Biol Blood Marrow Transplant. 2012;18(11):1649-1655.
40. Olivieri A, Cimminiello M, Corradini P, et al. Longterm outcome and prospective validation of NIH response criteria in 39 patients receiving imatinib for steroid-refractory chronic GVHD. Blood. 2013; 122(25):4111-4118.
41. Palmer J, Chai X, Martin PJ, et al. Failure-free survival in a prospective cohort of patients with chronic graft-versus-host disease. Haematologica. 2015;100(5):690-695.