HCK is a survival determinant transactivated by mutated MYD88, and a direct target of ibrutinib

Yang, Guang; Buhrlage, Sara J.; Tan, Li; Liu, Xia; Chen, Jie; Xu, Lian; Tsakmaklis, Nicholas; Chen, Jiaji G.; Patterson, Christopher J.; Brown, Jennifer R.; Castillo, Jorge J.; Zhang, Wei; Zhang, Xiaofeng; Liu, Shuai; Cohen, Philip; Hunter, Zachary R.; Gray, Nathanael; Treon, Steven P.

doi:10.1182/blood-2016-01-695098

Cited by 135Chronic Lymphocytic Leukemia ResearchLymphoma Diagnosis and TreatmentMultiple Myeloma Research and Treatments

HCK is a survival determinant transactivated by mutated MYD88, and a direct target of ibrutinib

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Yang, Guang, Buhrlage, Sara J., Tan, Li, Liu, Xia, Chen, Jie, Xu, Lian, Tsakmaklis, Nicholas, Chen, Jiaji G. +10 more·2016·Blood

DOI 10.1182/blood-2016-01-695098

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Abstract

Activating mutations in MYD88 are present in ∼95% of patients with Waldenström macroglobulinemia (WM), as well as other B-cell malignancies including activated B-cell (ABC) diffuse large B-cell lymphoma (DLBCL). In WM, mutated MYD88 triggers activation of Bruton tyrosine kinase (BTK). Ibrutinib, a pleiotropic kinase inhibitor that targets BTK, is highly active in patients with mutated MYD88. We observed that mutated MYD88 WM and ABC DLBCL cell lines, as well as primary WM cells show enhanced hematopoietic cell kinase (HCK) transcription and activation, and that HCK is activated by interleukin 6 (IL-6). Over-expression of mutated MYD88 triggers HCK and IL-6 transcription, whereas knockdown of HCK reduced survival and attenuated BTK, phosphoinositide 3-kinase/AKT, and mitogen-activated protein kinase/extracellular signal-regulated kinase signaling in mutated MYD88 WM and/or ABC DLBCL cells. Ibrutinib and the more potent HCK inhibitor A419259, blocked HCK activation and induced apoptosis in mutated MYD88 WM and ABC DLBCL cells. Docking and pull-down studies confirmed that HCK was a target of ibrutinib. Ibrutinib and A419259 also blocked adenosine triphosphate binding to HCK, whereas transduction of mutated MYD88 expressing WM cells with a mutated HCK gatekeeper greatly increased the half maximal effective concentration for ibrutinib and A419259. The findings support that HCK expression and activation is triggered by mutated MYD88, supports the growth and survival of mutated MYD88 WM and ABC DLBCL cells, and is a direct target of ibrutinib. HCK represents a novel target for therapeutic development in MYD88-mutated WM and ABC DLBCL, and possibly other diseases driven by mutated MYD88.

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Ibrutinib's activity against HCK (in addition to BTK) is responsible for antiproliferative effects in L265P-MYD88-driven ABC DLBCL cells.
“Consistent with the activity of ibrutinib on other TEC family kinases, its activity against HCK (in addition to BTK) is responsible for antiproliferative effects in L265P-MYD88-driven ABC DLBCL cells. 37”
From Bruton tyrosine kinase degradation as a therapeutic strategy for cancer (2019) · cites this paper as [37]
The HCK inhibitor A419259 exhibited strong synergy with both DD-03-007 and DD-03-171 in TMD8 cells at numerous doses.
“the HCK inhibitor A419259 37 exhibited strong synergy with both DD-03-007 and DD-03-171 in TMD8 cells at numerous doses (Figure 3C).”
From Bruton tyrosine kinase degradation as a therapeutic strategy for cancer (2019) · cites this paper as [37]

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Self-citation

HCK Is a Highly Relevant Target of Ibrutinib in MYD88 Mutated Waldenstrom's Macroglobulinemia and Diffuse Large B-Cell Lymphoma
Yang, G., Buhrlage, S. J., Tan, L., Liu, X., Chen, J., Hunter, Z. R., Xu, L., Tsakmaklis, N., Chen, J. G., Patterson, C. J., et al. (2015) · Blood · doi:10.1182/blood.v126.23.705.705 · Cited by 5 · see citing works
Self-citation
Acquisition of BTK C481S Produces Resistance to Ibrutinib in MYD88 Mutated WM and ABC DLBCL Cells That Is Accompanied By ERK1/2 Hyperactivation, and Is Targeted By the Addition of the ERK1/2 Inhibitor Ulixertinib
Chen, J. G., Liu, X., Chen, J., Xu, L., Tsakmaklis, N., Demos, M. G., Patterson, C. J., Castillo, J. J., Hunter, Z. R., Treon, S. P., et al. (2016) · Blood · doi:10.1182/blood.v128.22.2764.2764 · Cited by 3 · see citing works
Self-citation
A Novel HCK Inhibitor Kin-8193 Blocks BTK Activity in BTKCys481 Mutated Ibrutinib Resistant B-Cell Lymphomas Driven By Mutated MYD88
Yang, G., Wang, J., Tan, L., Liu, X., Munshi, M. N., Chen, J. G., Xu, L., Tsakmaklis, N., Demos, M. G., Kofides, A., et al. (2018) · Blood · doi:10.1182/blood-2018-99-119171 · Cited by 2 · see citing works
Self-citation
A Novel HCK and BTK Dual Inhibitor Kin-8194 Shows Superior Activity over Ibrutinib and Overcomes BTKC481S Mediated Ibrutinib Resistance in Vitro and In Vivo in MYD88 Mutated B-Cell Lymphomas
Yang, G., Wang, J., Liu, X., Munshi, M. N., Chen, J. G., Kofides, A., Xu, L., Tsakmaklis, N., Demos, M. G., Guerrera, M. L., et al. (2019) · Blood · doi:10.1182/blood-2019-130636 · Cited by 5 · see citing works
Self-citation
Mutated MYD88 Regulates HCK Pro-Survival Signaling through JunB in MYD88 Mutated B-Lymphoma Cells
Liu, X., Chen, J. G., Munshi, M. N., Xu, L., Kofides, A., Tsakmaklis, N., Demos, M. G., Guerrera, M. L., Chan, G., Jiménez, C., et al. (2019) · Blood · doi:10.1182/blood-2019-130885
Self-citation

Authors: Yang, G., Buhrlage, S. J., Tan, L., Liu, X., Chen, J., Xu, L., Tsakmaklis, N., Chen, J. G., Patterson, C. J., Brown, J. R., Castillo, J. J., Zhang, W., Zhang, X., Liu, S., Cohen, P., Hunter, Z. R., Gray, N., & Treon, S. P.
Affiliations: Harvard University (US)
University of Massachusetts Boston (US)
University of Dundee (GB)
ORCID: Yang, Guang
Buhrlage, Sara J.
Tan, Li
Liu, Xia
Chen, Jie
Chen, Jiaji G.
Patterson, Christopher J.
Brown, Jennifer R.
Castillo, Jorge J.
Zhang, Wei
Zhang, Xiaofeng
Liu, Shuai
Cohen, Philip
Hunter, Zachary R.
Gray, Nathanael
Treon, Steven P.
Venue: Blood
Publisher: American Society of Hematology
Published: 2016-06-23
Volume: 127
Issue: 25
Pages: 3237-3252
ISSN: 0006-4971 (ISSN-L)
1528-0020
DOI: 10.1182/blood-2016-01-695098
OpenAlex: W2347186599
Cited by: 135
References: 44
Citations by year: 2026: 7 · 2025: 10 · 2024: 13 · 2023: 10 · 2022: 14 · 2021: 22 · 2020: 19 · 2019: 11 · 2018: 16 · 2017: 9 · 2016: 4
FWCI: 9.67
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: Blood (publishedVersion)
PubMed (publishedVersion)
Discovery Research Portal (University of Dundee) (submittedVersion, other-oa)
Funders: Leukemia and Lymphoma Society
Medical Research Council (MR/K000985/1)
Topics: Health Sciences › Medicine › Genetics › Chronic Lymphocytic Leukemia Research
Health Sciences › Medicine › Pathology and Forensic Medicine › Lymphoma Diagnosis and Treatment
Health Sciences › Medicine › Hematology › Multiple Myeloma Research and Treatments
Keywords: hematopoietic cell kinase, MYD88 mutation, Waldenström macroglobulinemia, ibrutinib, Bruton's tyrosine kinase, interleukin-6, cell survival, apoptosis, PI3K/Akt signaling, ERK signaling, drug resistance
MeSH terms: Adenine, Antineoplastic Agents, Cell Survival, Humans, Waldenstrom Macroglobulinemia, Piperidines, Pyrazoles, Pyrimidines, Transcriptional Activation, Interleukin-6, Gene Expression Regulation, Leukemic, Lymphoma, Large B-Cell, Diffuse, Cell Line, Tumor, Mutant Proteins, Proto-Oncogene Proteins c-hck, Myeloid Differentiation Factor 88, Molecular Targeted Therapy

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HCK is a survival determinant transactivated by mutated MYD88, and a direct target of ibrutinib

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