Partial reconstitution of humoral immunity and fewer infections in patients with chronic lymphocytic leukemia treated with ibrutinib

Blood

Volumn 126, Issue 19, 2015, Pages 2213-2219

  Sun, Clare ^a   Tian, Xin ^a   Lee, Yuh Shan ^a   Gunti, Sreenivasulu ^b   Lipsky, Andrew ^a   Herman, Sarah E M ^a   Salem, Dalia ^c   Stetler Stevenson, Maryalice ^c   Yuan, Constance ^c   Kardava, Lela ^d   Moir, Susan ^d   Maric, Irina ^e   Valdez, Janet ^a   Soto, Susan ^a   Marti, Gerald E ^f   Farooqui, Mohammed Z ^a   Notkins, Abner L ^b   Wiestner, Adrian ^a   Aue, Georg ^a  

^a NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

^b NATIONAL INSTITUTE OF DENTAL AND CRANIOFACIAL RESEARCH   (United States)

^c NATIONAL CANCER INSTITUTE   (United States)

^d NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^e NATIONAL INSTITUTES OF HEALTH   (United States)

^f CENTER FOR DEVICES AND RADIOLOGICAL HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

B LYMPHOCYTE RECEPTOR; BRUTON TYROSINE KINASE; IBRUTINIB; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; AGAMMAGLOBULINAEMIA TYROSINE KINASE; IMMUNOGLOBULIN; PROTEIN TYROSINE KINASE; PYRAZOLE DERIVATIVE; PYRIMIDINE DERIVATIVE;

ADULT; AGED; ARTICLE; BONE MARROW; CANCER PATIENT; CHRONIC LYMPHATIC LEUKEMIA; DRUG EFFICACY; GASTROINTESTINAL INFECTION; GERMLINE MUTATION; HUMAN; HUMAN CELL; HUMORAL IMMUNITY; IMMUNOGLOBULIN BLOOD LEVEL; IMMUNOGLOBULIN DEFICIENCY; IMMUNOREGULATION; INFECTION; INFECTION RATE; LIGHT CHAIN; MAJOR CLINICAL STUDY; MORBIDITY; PHASE 2 CLINICAL TRIAL (TOPIC); PRE B LYMPHOCYTE; PRIORITY JOURNAL; RESPIRATORY TRACT INFECTION; SIGNAL TRANSDUCTION; SKIN INFECTION; TREATMENT DURATION; UROGENITAL TRACT INFECTION; ANTAGONISTS AND INHIBITORS; B LYMPHOCYTE; BLOOD; CLINICAL TRIAL; CONVALESCENCE; DRUG EFFECTS; FEMALE; FOLLOW UP; IMMUNOLOGY; LEUKEMIA, LYMPHOCYTIC, CHRONIC, B-CELL; MALE; METABOLISM; TIME FACTOR; VERY ELDERLY;

AGED; AGED, 80 AND OVER; B-LYMPHOCYTES; BONE MARROW; FEMALE; FOLLOW-UP STUDIES; HUMANS; IMMUNITY, HUMORAL; IMMUNOGLOBULINS; INFECTION; LEUKEMIA, LYMPHOCYTIC, CHRONIC, B-CELL; MALE; PROTEIN-TYROSINE KINASES; PYRAZOLES; PYRIMIDINES; RECOVERY OF FUNCTION; TIME FACTORS;

EID: 84949008471     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2015-04-639203     Document Type: Article

References (50)

1. Morrison VA. Infectious complications in patients with chronic lymphocytic leukemia: pathogenesis, spectrum of infection, and approaches to prophylaxis. Clin Lymphoma Myeloma. 2009;9(5): 365-370.
2. Zinneman HH, Hall WH, Heller BI. Acquired agammaglobulinemia: report of three cases. J Am Med Assoc. 1954;156(15):1390-1393.
3. Jim RT, Reinhard EH. Agammaglobulinemia and chronic lymphocytic leukemia. Ann Intern Med. 1956;44(4):790-796.
4. Hamblin AD, Hamblin TJ. The immunodeficiency of chronic lymphocytic leukaemia. Br Med Bull. 2008;87:49-62.
5. Freeman JA, Crassini KR, Best OG, et al. Immunoglobulin G subclass deficiency and infection risk in 150 patients with chronic lymphocytic leukemia. Leuk Lymphoma. 2013; 54(1):99-104.
6. Griffiths H, Lea J, Bunch C, Lee M, Chapel H. Predictors of infection in chronic lymphocytic leukaemia (CLL). Clin Exp Immunol. 1992;89(3): 374-377.
7. Sampalo A, Navas G, Medina F, Segundo C, Cámara C, Brieva JA. Chronic lymphocytic leukemia B cells inhibit spontaneous Ig production by autologous bone marrow cells: role of CD95-CD95L interaction. Blood. 2000;96(9):3168-3174.
8. Motta M, Chiarini M, Ghidini C, et al. Quantification of newly produced B and T lymphocytes in untreated chronic lymphocytic leukemia patients. J Transl Med. 2010;8:111.
9. Kunicka JE, Platsoucas CD. Defective helper function of purified T4 cells and excessive suppressor activity of purified T8 cells in patients with B-cell chronic lymphocytic leukemia. T4 suppressor effector cells are present in certain patients. Blood. 1988;71(6):1551-1560.
10. Chiorazzi N, Fu SM, Montazeri G, Kunkel HG, Rai K, Gee T. T cell helper defect in patients with chronic lymphocytic leukemia. J Immunol. 1979;122(3):1087-1090.
11. Kay NE, Perri RT. Evidence that large granular lymphocytes from B-CLL patients with hypogammaglobulinemia down-regulate B-cell immunoglobulin synthesis. Blood. 1989;73(4): 1016-1019.
12. Cerutti A, Kim EC, Shah S, et al. Dysregulation of CD301 T cells by leukemia impairs isotype switching in normal B cells. Nat Immunol. 2001; 2(2):150-156.
13. Keating MJ, O'Brien S, Albitar M, et al. Early results of a chemoimmunotherapy regimen of fludarabine, cyclophosphamide, and rituximab as initial therapy for chronic lymphocytic leukemia. J Clin Oncol. 2005;23(18):4079-4088.
14. Hallek M, Fischer K, Fingerle-Rowson G, et al; International Group of Investigators; German Chronic Lymphocytic Leukaemia Study Group. Addition of rituximab to fludarabine and cyclophosphamide in patients with chronic lymphocytic leukaemia: a randomised, openlabel, phase 3 trial. Lancet. 2010;376(9747): 1164-1174.
15. Gea-Banacloche JC. Rituximab-associated infections. Semin Hematol. 2010;47(2):187-198.
16. Tam CS, O'Brien S, Wierda W, et al. Long-term results of the fludarabine, cyclophosphamide, and rituximab regimen as initial therapy of chronic lymphocytic leukemia. Blood. 2008;112(4): 975-980.
17. Niemann CU, Wiestner A. B-cell receptor signaling as a driver of lymphoma development and evolution. Semin Cancer Biol. 2013;23(6): 410-421.
18. Herishanu Y, Pérez-Galán P, Liu D, et al. The lymph node microenvironment promotes B-cell receptor signaling, NF-kappaB activation, and tumor proliferation in chronic lymphocytic leukemia. Blood. 2011;117(2):563-574.
19. Herishanu Y, Katz BZ, Lipsky A, Wiestner A. Biology of chronic lymphocytic leukemia in different microenvironments: clinical and therapeutic implications. Hematol Oncol Clin North Am. 2013;27(2):173-206.
20. Advani RH, Buggy JJ, Sharman JP, et al. Bruton tyrosine kinase inhibitor ibrutinib (PCI-32765) has significant activity in patients with relapsed/refractory B-cell malignancies. J Clin Oncol. 2013; 31(1):88-94.
21. Wiestner A. Targeting B-cell receptor signaling for anticancer therapy: the Bruton's tyrosine kinase inhibitor ibrutinib induces impressive responses in B-cell malignancies. J Clin Oncol. 2013;31(1): 128-130.
22. Wiestner A. Emerging role of kinase-targeted strategies in chronic lymphocytic leukemia. Blood. 2012;120(24):4684-4691.
23. Byrd JC, Furman RR, Coutre SE, et al. Targeting BTK with ibrutinib in relapsed chronic lymphocytic leukemia. N Engl J Med. 2013;369(1):32-42.
24. Farooqui MZ, Valdez J, Martyr S, et al. Ibrutinib for previously untreated and relapsed or refractory chronic lymphocytic leukaemia with TP53 aberrations: a phase 2, single-arm trial. Lancet Oncol. 2015;16(2):169-176.
25. Tripsas CK, Yang G, Cao Y, et al. A prospective multicenter study of the Bruton's tyrosine kinase inhibitor ibrutinib in patients with relapsed or refractory Waldenstrom's macroglobulinemia [abstract]. Blood. 2013;122(21). Abstract 67.
26. Wiestner A. BCR pathway inhibition as therapy for chronic lymphocytic leukemia and lymphoplasmacytic lymphoma. Hematology (Am Soc Hematol Educ Program). 2014;2014(1): 125-134.
27. Treon SP, Tripsas CK, Meid K, et al. Ibrutinib in previously treated Waldenström's macroglobulinemia. N Engl J Med. 2015;372(15): 1430-1440.
28. Ponader S, Burger JA. Bruton's tyrosine kinase: from X-linked agammaglobulinemia toward targeted therapy for B-cell malignancies. J Clin Oncol. 2014;32(17):1830-1839.
29. O'Brien S, Furman RR, Coutre SE, et al. Ibrutinib as initial therapy for elderly patients with chronic lymphocytic leukaemia or small lymphocytic lymphoma: an open-label, multicentre, phase 1b/2 trial. Lancet Oncol. 2014;15(1):48-58.
30. Byrd JC, Brown JR, O'Brien S, et al; RESONATE Investigators. Ibrutinib versus ofatumumab in previously treated chronic lymphoid leukemia. N Engl J Med. 2014;371(3):213-223.
31. Herman SE, Niemann CU, Farooqui M, et al. Ibrutinib-induced lymphocytosis in patients with chronic lymphocytic leukemia: correlative analyses from a phase II study. Leukemia. 2014; 28(11):2188-2196.
32. Chuang-Stein C. Some issues concerning the normalization of laboratory data based on reference ranges. Drug Inf J. 2001;35(1):153-156.
33. Jasper GA, Arun I, Venzon D, et al. Variables affecting the quantitation of CD22 in neoplastic B cells. Cytometry B Clin Cytom. 2011;80(2): 83-90.
34. Rawstron AC, Villamor N, Ritgen M, et al. International standardized approach for flow cytometric residual disease monitoring in chronic lymphocytic leukaemia. Leukemia. 2007;21(5): 956-964.
35. Cook RJ, Lawless JF. The statistical analysis of recurrent events. New York, NY: Springer; 2007.
36. Andersen PK, Gill RD. Cox regression-model for counting-processes - a large sample study. Ann Stat. 1982;10(4):1100-1120.
37. Hervé M, Xu K, Ng YS, et al. Unmutated and mutated chronic lymphocytic leukemias derive from self-reactive B cell precursors despite expressing different antibody reactivity. J Clin Invest. 2005;115(6):1636-1643.
38. Moir S, De Ravin SS, Santich BH, et al. Humans with chronic granulomatous disease maintain humoral immunologic memory despite low frequencies of circulating memory B cells. Blood. 2012;120(24):4850-4858.
39. Mackay F, Schneider P. Cracking the BAFF code. Nat Rev Immunol. 2009;9(7):491-502.
40. Kreuzaler M, Rauch M, Salzer U, et al. Soluble BAFF levels inversely correlate with peripheral B cell numbers and the expression of BAFF receptors. J Immunol. 2012;188(1):497-503.
41. Bojarska-Junak A, Hus I, Chocholska S, et al. BAFF and APRIL expression in B-cell chronic lymphocytic leukemia: correlation with biological and clinical features. Leuk Res. 2009;33(10): 1319-1327.
42. Claudio E, Brown K, Park S, Wang H, Siebenlist U. BAFF-induced NEMO-independent processing of NF-kappa B2 in maturing B cells. Nat Immunol. 2002;3(10):958-965.
43. Novak AJ, Bram RJ, Kay NE, Jelinek DF. Aberrant expression of B-lymphocyte stimulator by B chronic lymphocytic leukemia cells: a mechanism for survival. Blood. 2002;100(8): 2973-2979.
44. Nishio M, Endo T, Tsukada N, et al. Nurselike cells express BAFF and APRIL, which can promote survival of chronic lymphocytic leukemia cells via a paracrine pathway distinct from that of SDF-1alpha. Blood. 2005;106(3):1012-1020.
45. Herman SE, Gordon AL, Hertlein E, et al. Bruton tyrosine kinase represents a promising therapeutic target for treatment of chronic lymphocytic leukemia and is effectively targeted by PCI-32765. Blood. 2011;117(23):6287-6296.
46. Herman SE, Mustafa RZ, Gyamfi JA, et al. Ibrutinib inhibits BCR and NF-kB signaling and reduces tumor proliferation in tissue-resident cells of patients with CLL. Blood. 2014;123(21): 3286-3295.
47. Yel L. Selective IgA deficiency. J Clin Immunol. 2010;30(1):10-16.
48. Ng YS, Wardemann H, Chelnis J, Cunningham-Rundles C, Meffre E. Bruton's tyrosine kinase is essential for human B cell tolerance. J Exp Med. 2004;200(7):927-934.
49. Notkins AL. Polyreactivity of antibody molecules. Trends Immunol. 2004;25(4):174-179.
50. Zhou ZH, Zhang Y, Hu YF, Wahl LM, Cisar JO, Notkins AL. The broad antibacterial activity of the natural antibody repertoire is due to polyreactive antibodies. Cell Host Microbe. 2007;1(1):51-61.