Canine lymphoma as a comparative model for human non-Hodgkin lymphoma: Recent progress and applications

Veterinary Immunology and Immunopathology

Volumn 159, Issue 3-4, 2014, Pages 192-201

  Ito, Daisuke ^a,b   Frantz, Aric M ^a,b   Modiano, Jaime F ^a,b  

^a UNIVERSITY OF MINNESOTA   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD133 ANTIGEN; CD34 ANTIGEN; CYANOCOBALAMIN; IMMUNOGLOBULIN HEAVY CHAIN; PROCASPASE 3; ANTINEOPLASTIC AGENT;

ARTICLE; B CELL LYMPHOMA; BURKITT LYMPHOMA; CANCER CLASSIFICATION; CANCER GROWTH; CANINE LYMPHOMA; CANINE MODEL; CHRONIC LYMPHATIC LEUKEMIA; DOG; FOLLICULAR LYMPHOMA; GENE EXPRESSION PROFILING; GENETIC ENGINEERING; HUMAN T CELL LEUKEMIA VIRUS; LARGE CELL LYMPHOMA; MANTLE CELL LYMPHOMA; MARGINAL ZONE LYMPHOMA; MOLECULAR PATHOLOGY; NONHODGKIN LYMPHOMA; NONHUMAN; ONCOGENE MYC; PERIPHERAL T CELL LYMPHOMA; T CELL LYMPHOMA; WORLD HEALTH ORGANIZATION; ANIMAL; DISEASE MODEL; HUMAN; IMMUNOLOGY; LYMPHOMA; LYMPHOMA, NON-HODGKIN; VETERINARY;

CANIS FAMILIARIS;

ANIMALS; ANTINEOPLASTIC AGENTS; DISEASE MODELS, ANIMAL; DOGS; HUMANS; LYMPHOMA; LYMPHOMA, NON-HODGKIN;

EID: 84900520514     PISSN: 01652427     EISSN: 18732534     Source Type: Journal    
DOI: 10.1016/j.vetimm.2014.02.016     Document Type: Article

References (75)

1. Alizadeh A.A., Eisen M.B., Davis R.E., Ma C., Lossos I.S., Rosenwald A., Boldrick J.C., Sabet H., Tran T., Yu X., Powell J.I., Yang L., Marti G.E., Moore T., Hudson J., Lu L., Lewis D.B., Tibshirani R., Sherlock G., Chan W.C., Greiner T.C., Weisenburger D.D., Armitage J.O., Warnke R., Levy R., Wilson W., Grever M.R., Byrd J.C., Botstein D., Brown P.O., Staudt L.M. Distinct types of diffuse large B-cell lymphoma identified by gene expression profiling. Nature 2000, 403:503-511.
2. Alvarez C.E., Akey J.M. Copy number variation in the domestic dog. Mamm. Genome Official J. Int. Mamm. Genome Soc. 2012, 23:144-163.
3. Andersen N.S., Larsen J.K., Christiansen J., Pedersen L.B., Christophersen N.S., Geisler C.H., Jurlander J. Soluble CD40 ligand induces selective proliferation of lymphoma cells in primary mantle cell lymphoma cell cultures. Blood 2000, 96:2219-2225.
4. Anon A clinical evaluation of the International Lymphoma Study Group classification of non-Hodgkin's lymphoma. The non-Hodgkin's lymphoma classification project. Blood 1997, 89:3909-3918.
5. Bernt K.M., Armstrong S.A. Leukemia stem cells and human acute lymphoblastic leukemia. Semin. Hematol. 2009, 46:33-38.
6. Breen M., Modiano J.F. Evolutionarily conserved cytogenetic changes in hematological malignancies of dogs and humans - man and his best friend share more than companionship. Chromosome Res. 2008, 16:145-154.
7. Castor A., Nilsson L., Astrand-Grundström I., Buitenhuis M., Ramirez C., Anderson K., Strömbeck B., Garwicz S., Békássy A.N., Schmiegelow K., Lausen B., Hokland P., Lehmann S., Juliusson G., Johansson B., Jacobsen S.E.W. Distinct patterns of hematopoietic stem cell involvement in acute lymphoblastic leukemia. Nat. Med. 2005, 11:630-637.
8. Challa A., Eliopoulos A.G., Holder M.J., Burguete A.S., Pound J.D., Chamba A., Grafton G., Armitage R.J., Gregory C.D., Martinez-Valdez H., Young L., Gordon J. Population depletion activates autonomous CD154-dependent survival in biopsylike Burkitt lymphoma cells. Blood 2002, 99:3411-3418.
9. Chao M.P., Alizadeh A.A., Tang C., Myklebust J.H., Varghese B., Gill S., Jan M., Cha A.C., Chan C.K., Tan B.T., Park C.Y., Zhao F., Kohrt H.E., Malumbres R., Briones J., Gascoyne R.D., Lossos I.S., Levy R., Weissman I.L., Majeti R. Anti-CD47 antibody synergizes with rituximab to promote phagocytosis and eradicate non-hodgkin lymphoma. Cell 2010, 142:699-713.
10. Cox C.V., Diamanti P., Evely R.S., Kearns P.R., Blair A. Expression of CD133 on leukemia-initiating cells in childhood ALL. Blood 2009, 113:3287-3296.
11. Cox C.V., Evely R.S., Oakhill A., Pamphilon D.H., Goulden N.J., Blair A. Characterization of acute lymphoblastic leukemia progenitor cells. Blood 2004, 104:2919-2925.
12. Davis R.E., Brown K.D., Siebenlist U., Staudt L.M. Constitutive nuclear factor kappaB activity is required for survival of activated B cell-like diffuse large B cell lymphoma cells. J. Exp. Med. 2001, 194:1861-1874.
13. Deng C., Pan B., O'Connor O.A. Brentuximab vedotin. Clin. Cancer Res. 2013, 19:22-27.
14. Dobson J.M., Samuel S., Milstein H., Rogers K., Wood J.L. Canine neoplasia in the UK: estimates of incidence rates from a population of insured dogs. J. Small Anim. Pract. 2002, 43:240-246.
15. Dorn C.R., Taylor D.O., Hibbard H.H. Epizootiologic characteristics of canine and feline leukemia and lymphoma. Am. J. Vet. Res. 1967, 28:993-1001.
16. Dorn C.R., Taylor D.O., Schneider R., Hibbard H.H., Klauber M.R. Survey of animal neoplasms in Alameda and Contra Costa Counties. California. II. Cancer morbidity in dogs and cats from Alameda County. J. Natl. Cancer Inst. 1968, 40:307-318.
17. Edwards D.S., Henley W.E., Harding E.F., Dobson J.M., Wood J.L.N. Breed incidence of lymphoma in a UK population of insured dogs. Vet. Comp. Oncol. 2003, 1:200-206.
18. Ferry J.A. Burkitt's lymphoma: clinicopathologic features and differential diagnosis. Oncologist 2006, 11:375-383.
19. Frantz A.M., Sarver A.L., Ito D., Phang T.L., Karimpour-Fard A., Scott M.C., Valli V.E.O., Lindblad-Toh K., Burgess K.E., Husbands B.D., Henson M.S., Borgatti A., Kisseberth W.C., Hunter L.E., Breen M., O'Brien T.D., Modiano J.F. Molecular profiling reveals prognostically significant subtypes of canine lymphoma. Vet. Pathol. 2012, 50:693-703.
20. Garrett L.D., Thamm D.H., Chun R., Dudley R., Vail D.M. Evaluation of a 6-month chemotherapy protocol with no maintenance therapy for dogs with lymphoma. J. Vet. Int. Med. Am College Vet. Int. Med. 2002, 16:704-709.
21. Gaurnier-Hausser A., Patel R., Baldwin A.S., May M.J., Mason N.J. NEMO-binding domain peptide inhibits constitutive NF-(B activity and reduces tumor burden in a canine model of relapsed, refractory diffuse large B-cell lymphoma. Clin. Cancer Res. 2011, 17:4661-4671.
22. Glickman L., Glickman N., Thorpe R. The Golden Retriever Club of America National Health Survey 1998-1999. The Golden Retriever Club of America National Health Survey 1999, (Available from: ).
23. Honigberg L.A., Smith A.M., Sirisawad M., Verner E., Loury D., Chang B., Li S., Pan Z., Thamm D.H., Miller R.A., Buggy J.J. The Bruton tyrosine kinase inhibitor PCI-32765 blocks B-cell activation and is efficacious in models of autoimmune disease and B-cell malignancy. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:13075-13080.
24. Hotfilder M., Röttgers S., Rosemann A., Jürgens H., Harbott J., Vormoor J. Immature CD34+CD19- progenitor/stem cells in TEL/AML1-positive acute lymphoblastic leukemia are genetically and functionally normal. Blood 2002, 100:640-646.
25. Howlader N., Noone A.M., Krapcho M., Neyman N., Aminou R., Altekruse S.F., Kosary C.L., Ruhl J., Tatalovich Z., Cho H., Mariotto A., Eisner M.P., Lewis D.R., Chen H.S., Feuer E.J., Cronin K.A. SEER Cancer Statistics Review 1975-2009 (Vintage 2009 Populations) 2012, National Cancer Institute, Bethesda, MD.
26. Huang S.-H., Kozak P.J., Kim J., Habineza-Ndikuyeze G., Meade C., Gaurnier-Hausser A., Patel R., Robertson E., Mason N.J. Evidence of an oncogenic gammaherpesvirus in domestic dogs. Virology 2012, 427:107-117.
27. Ito D., Endicott M.M., Jubala C.M., Helm K.M., Burnett R.C., Husbands B.D., Borgatti A., Henson M.S., Burgess K.E., Bell J.S., Kisseberth W.C., Valli V.E., Cutter G.R., Avery A.C., Hahn K.A., O'Brien T.D., Modiano J.F. A tumor-related lymphoid progenitor population supports hierarchical tumor organization in canine B-cell lymphoma. J. Vet. Int. Med. Am. College Vet. Int. Med. 2011, 25:890-896.
28. Ito D., Frantz A.M., Williams C., Thomas R., Burnett R.C., Avery A.C., Breen M., Mason N.J., O'Brien T.D., Modiano J.F. CD40 ligand is necessary and sufficient to support primary diffuse large B-cell lymphoma cells in culture: a tool for in vitropreclinical studies with primary B-cell malignancies. Leuk. Lymphoma 2012, 53:1390-1398.
29. Ito D., Modiano J.F., Childress M.O., Mason N.J., Leary J.F., O'Brien T.D., Henson M.S., Borgatti A., Krick E., Stuebner K., Winter A., Stewart J.C., Lahrman S.A., Meyers J.L., Ruetz S. Targeting Lymphoid Progenitor Cells in Canine B-Cell Lymphoma Using Neoadjuvant ABCB1 Transporter Inhibition and Doxorubicin Chemotherapy 2013, The 2013 American College of Veterinary Internal Medicine Forum, Seattle, WA.
30. Itoh T., Shiota M., Takanashi M., Hojo I., Satoh H., Matsuzawa A., Moriyama T., Watanabe T., Hirai K., Mori S. Engraftment of human non-Hodgkin lymphomas in mice with severe combined immunodeficiency. Cancer 1993, 72:2686-2694.
31. Keller E.T., MacEwen E.G., Rosenthal R.C., Helfand S.C., Fox L.E. Evaluation of prognostic factors and sequential combination chemotherapy with doxorubicin for canine lymphoma. J. Vet. Int. Med Am. College Vet. Int. Med. 1993, 7:289-295.
32. Khanna C., Lindblad-Toh K., Vail D., London C., Bergman P., Barber L., Breen M., Kitchell B., McNeil E., Modiano J.F., Niemi S., Comstock K.E., Ostrander E., Westmoreland S., Withrow S. The dog as a cancer model. Nat. Biotechnol. 2006, 24:1065-1066.
33. Kisseberth W.C., Nadella M.V.P., Breen M., Thomas R., Duke S.E., Murahari S., Kosarek C.E., Vernau W., Avery A.C., Burkhard M.J., Rosol T.J. A novel canine lymphoma cell line: a translational and comparative model for lymphoma research. Leuk. Res. 2007, 31:1709-1720.
34. le Viseur C., Hotfilder M., Bomken S., Wilson K., Röttgers S., Schrauder A., Rosemann A., Irving J., Stam R.W., Shultz L.D., Harbott J., Jürgens H., Schrappe M., Pieters R., Vormoor J. In childhood acute lymphoblastic leukemia, blasts at different stages of immunophenotypic maturation have stem cell properties. Cancer Cell 2008, 14:47-58.
35. Lee C.G., Das B., Lin T.L., Grimes C., Zhang X., Lavezzi T., Huang L., Cole J., Yau L., Li L. A rare fraction of drug-resistant follicular lymphoma cancer stem cells interacts with follicular dendritic cells to maintain tumourigenic potential. Br. J. Haematol. 2012, 158:79-90.
36. London C., Bernabe L.F., Barnard S., Kisseberth W.C., Borgatti A., Henson M., Wilson H., Jensen K., Ito D., Modiano J.F., Bear M.D., Pennell M.L., Saint-Martin J.R., McCauley D., Kauffman M., Shacham S. Preclinical evaluation of the novel, orally bioavailable selective inhibitor of nuclear export (SINE) KPT-335 in spontaneous canine cancer: results of a Phase I study. PloS One 2014, 9:e87585.
37. Lossos I.S., Czerwinski D.K., Alizadeh A.A., Wechser M.A., Tibshirani R., Botstein D., Levy R. Prediction of survival in diffuse large-B-cell lymphoma based on the expression of six genes. N. Engl. J. Med. 2004, 350:1828-1837.
38. MacDonald V.S., Thamm D.H., Kurzman I.D., Turek M.M., Vail D.M. Does l-asparaginase influence efficacy or toxicity when added to a standard CHOP protocol for dogs with lymphoma?. J. Vet. Int. Med Am. College Vet. Int. Med. 2005, 19:732-736.
39. Marconato L., Gelain M.E., Comazzi S. The dog as a possible animal model for human non-Hodgkin lymphoma: a review. Hematol. Oncol. 2012, 30:1-9.
40. Mason N.J., Coughlin C.M., Overley B., Cohen J.N., Mitchell E.L., Colligon T.A., Clifford C.A., Zurbriggen A., Sorenmo K.U., Vonderheide R.H. RNA-loaded CD40-activated B cells stimulate antigen-specific T-cell responses in dogs with spontaneous lymphoma. Gene Ther. 2008, 15:955-965.
41. Mato A.R., Feldman T., Goy A. Proteasome inhibition and combination therapy for non-Hodgkin's lymphoma: from bench to bedside. Oncologist 2012, 17:694-707.
42. Merlo D.F., Rossi L., Pellegrino C., Ceppi M., Cardellino U., Capurro C., Ratto A., Sambucco P.L., Sestito V., Tanara G., Bocchini V. Cancer incidence in pet dogs: findings of the Animal Tumor Registry of Genoa, Italy. J. Vet. Int. Med Am. College Vet. Int. Med. 2008, 22:976-984.
43. Modiano J.F., Breen M., Avery A.C., London C.A. Breed-specific canine lymphoproliferative diseases. The Dog and its Genome 2006, 439-450. Cold Spring Harbor Laboratory Press, Cold Spring Harbor. E.A. Ostrander, U. Giger, K. Lindblad-Toh (Eds.).
44. Modiano J.F., Breen M., Burnett R.C., Parker H.G., Inusah S., Thomas R., Avery P.R., Lindblad-Toh K., Ostrander E.A., Cutter G.C., Avery A.C. Distinct B-cell and T-cell lymphoproliferative disease prevalence among dog breeds indicates heritable risk. Cancer Res. 2005, 65:5654-5661.
45. Müller A.M.S., Ihorst G., Mertelsmann R., Engelhardt M. Epidemiology of non-Hodgkin's lymphoma (NHL): trends, geographic distribution, and etiology. Ann. Hematol. 2004, 84:1-12.
46. Nguyen L.V., Vanner R., Dirks P., Eaves C.J. Cancer stem cells: an evolving concept. Nat. Rev. Cancer 2012, 12:133-143.
47. Onions D.E. A prospective survey of familial canine lymphosarcoma. J. Natl. Cancer Inst. 1984, 72:909-912.
48. Paoloni M., Khanna C. Translation of new cancer treatments from pet dogs to humans. Nat. Rev. Cancer 2008, 8:147-156.
49. Peterson Q.P., Hsu D.C., Novotny C.J., West D.C., Kim D., Schmit J.M., Dirikolu L., Hergenrother P.J., Fan T.M. Discovery and canine preclinical assessment of a nontoxic procaspase-3-activating compound. Cancer Res. 2010, 70:7232-7241.
50. Pham L.V., Tamayo A.T., Yoshimura L.C., Lo P., Terry N., Reid P.S., Ford R.J. A CD40 Signalosome anchored in lipid rafts leads to constitutive activation of NF-kappaB and autonomous cell growth in B cell lymphomas. Immunity 2002, 16:37-50.
51. Planken E.V., Dijkstra N.H., Willemze R., Kluin-Nelemans J.C. Proliferation of B cell malignancies in all stages of differentiation upon stimulation in the 'CD40 system'. Leukemia 1996, 10:488-493.
52. Ponce F., Marchal T., Magnol J.P., Turinelli V., Ledieu D., Bonnefont C., Pastor M., Delignette M.L., Fournel-Fleury C. A morphological study of 608 cases of canine malignant lymphoma in France with a focus on comparative similarities between canine and human lymphoma morphology. Vet. Pathol. 2010, 47:414-433.
53. Priester W.A., McKay F.W. The occurrence of tumors in domestic animals. Natl. Cancer Inst. Monogr. 1980, 54:1-210.
54. Ritt M.G. Epidemiology of hematopoietic neoplasia. Schalm's Veterinary Hematology 2010, 427-432. Wiley-Blackwell, Ames, IA. sixth ed. D.J. Weiss, J.K. Wardrop (Eds.).
55. Rosenwald A., Wright G., Chan W.C., Connors J.M., Campo E., Fisher R.I., Gascoyne R.D., Muller-Hermelink H.K., Smeland E.B., Giltnane J.M., Hurt E.M., Zhao H., Averett L., Yang L., Wilson W.H., Jaffe E.S., Simon R., Klausner R.D., Powell J., Duffey P.L., Longo D.L., Greiner T.C., Weisenburger D.D., Sanger W.G., Dave B.J., Lynch J.C., Vose J., Armitage J.O., Montserrat E., López-Guillermo A., Grogan T.M., Miller T.P., LeBlanc M., Ott G., Kvaloy S., Delabie J., Holte H., Krajci P., Stokke T., Staudt L.M., Project L.L.M.P. The use of molecular profiling to predict survival after chemotherapy for diffuse large-B-cell lymphoma. N. Engl. J. Med. 2002, 346:1937-1947.
56. Rütgen B.C., Hammer S.E., Gerner W., Christian M., de Arespacochaga A.G., Willmann M., Kleiter M., Schwendenwein I., Saalmüller A. Establishment and characterization of a novel canine B-cell line derived from a spontaneously occurring diffuse large cell lymphoma. Leuk. Res. 2010, 34:932-938.
57. Rütgen B.C., Willenbrock S., Reimann-Berg N., Walter I., Fuchs-Baumgartinger A., Wagner S., Kovacic B., Essler S.E., Schwendenwein I., Nolte I., Saalmüller A., Escobar H.M. Authentication of primordial characteristics of the CLBL-1 cell line prove the integrity of a canine B-cell lymphoma in a murine in vivo model. PLoS One 2012, 7:e40078.
58. Safran N., Perk K., Eyal O., Dahlberg J.E. Isolation and preliminary characterisation of a novel retrovirus isolated from a leukaemic dog. Res. Vet. Sci. 1992, 52:250-255.
59. Schacam S., Barnard S., Kisseberth W., Ito D., Jensen K., Borgatti A., Henson M., Wilson H., McCauley D., Modiano J.F., Kauffman M., London C. Results of a Phase I Dose Escalation Study of the Novel, Oral CRM1 Selective Inhibitor of Nuclear Export (SINE) KPT-335 in Dogs with Spontaneous Non-Hodgkin's Lymphomas (NHL) 2012, 54th Annual Meeting of the American Society for Hematology, Atlanta, GA.
60. Shipp M.A., Ross K.N., Tamayo P., Weng A.P., Kutok J.L., Aguiar R.C.T., Gaasenbeek M., Angelo M., Reich M., Pinkus G.S., Ray T.S., Koval M.A., Last K.W., Norton A., Lister T.A., Mesirov J., Neuberg D.S., Lander E.S., Aster J.C., Golub T.R. Diffuse large B-cell lymphoma outcome prediction by gene-expression profiling and supervised machine learning. Nat. Med. 2002, 8:68-74.
61. Shultz L.D., Lyons B.L., Burzenski L.M., Gott B., Chen X., Chaleff S., Kotb M., Gillies S.D., King M., Mangada J., Greiner D.L., Handgretinger R. Human lymphoid and myeloid cell development in NOD/LtSz-scid IL2R gamma null mice engrafted with mobilized human hemopoietic stem cells. J. Immunol. 2005, 174:6477-6489.
62. Swerdlow S.H., Campo E., Harris N.L., Jaffe E.S., Pileri S.A., Stein H., Thiele J., Vardiman J.W. WHO classification of tumours of haematopoietic and lymphoid tissues 2008, International Agency for Research on Cancer, Lyon, France. fourth ed.
63. Teske E. Canine malignant lymphoma: a review and comparison with human non-Hodgkin's lymphoma. Vet. Quart. 1994, 16:209-219.
64. Teske E., de Vos J.P., Egberink H.F., Vos J.H. Clustering in canine malignant lymphoma. Vet. Quart. 1994, 16:134-136.
65. Thomas R., Seiser E.L., Motsinger-Reif A., Borst L., Valli V.E., Kelley K., Suter S.E., Argyle D., Burgess K., Bell J., Lindblad-Toh K., Modiano J.F., Breen M. Refining tumor-associated aneuploidy through 'genomic recoding' of recurrent DNA copy number aberrations in 150 canine non-Hodgkin lymphomas. Leuk. Lymphoma 2011, 52:1321-1335.
66. Thomas R., Seiser E.L., Motsinger-Reif A., Borst L., Valli V.E., Kelley K., Suter S.E., Argyle D., Burgess K., Bell J., Lindblad-Toh K., Modiano J.F., Breen M. Refining tumor-associated aneuploidy through 'genomic recoding' of recurrent DNA copy number aberrations in 150 canine non-Hodgkin lymphomas. Leuk. Lymphoma 2011, 52:1321-1335.
67. Tomley F.M., Armstrong S.J., Mahy B.W., Owen L.N. Reverse transcriptase activity and particles of retroviral density in cultured canine lymphosarcoma supernatants. Br. J. Cancer 1983, 47:277-284.
68. Tonomura N., Thomas R., Megquier K., Perloski M., Swofford R., Davis B., Barber L., Burgess K., Azuma C., Modiano J.F., Breen M., Lindblad-Toh K. GWAS Identifies Risk Loci for Two Hematologic Malignancies in Golden Retriever 2012, The 6th International Conference on Advances in Canine and Feline Genomics and Inherited Disease, Visby, Sweden.
69. Traullé C., Coiffier B.B. Evolving role of rituximab in the treatment of patients with non-Hodgkin's lymphoma. Future Oncol. 2005, 1:297-306.
70. Valli V.E. Histological Classification of Hematopoietic Tumors of Domestic Animals 2002, Armed Forces Institute of Pathology, Washington, DC.
71. Valli V.E., Myint M.S., Barthel A., Bienzle D., Caswell J., Colbatzky F., Durham A., Ehrhart E.J., Johnson Y., Jones C., Kiupel M., Labelle P., Lester S., Miller M., Moore P., Moroff S., Roccabianca P., Ramos-Vara J., Ross A., Scase T., Tvedten H., Vernau W. Classification of canine malignant lymphomas according to the world health organization criteria. Vet. Pathol. 2011, 48:198-211.
72. Vega F., Davuluri Y., Cho-Vega J.H., Singh R.R., Ma S., Wang R.-Y., Multani A.S., Drakos I., Pham L., Lee Y.-C.L., Shen L., Ambrus J., Medeiros L.J., Ford R.J. Side population of a murine mantle cell lymphoma model contains tumor-initiating cells responsible for lymphoma maintenance and dissemination. J. Cell Mol. Med. 2009, 14:1532-1545.
73. Visser H.P., Tewis M., Willemze R., Kluin-Nelemans J.C. Mantle cell lymphoma proliferates upon IL-10 in the CD40 system. Leukemia 2000, 14:1483-1489.
74. Wang Y., Liu Y., Malek S.N., Zheng P., Liu Y. Targeting HIF1α eliminates cancer stem cells in hematological malignancies. Cell Stem Cell 2011, 8:399-411.
75. 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, 31:128-130.