Skip to main content
Top
Published in: Acta Neuropathologica Communications 1/2024

Open Access 01-12-2024 | Research

Therapeutic potential of targeting Nrf2 by panobinostat in pituitary neuroendocrine tumors

Authors: Yijun Cheng, Yuting Dai, Hao Tang, Xingyu Lu, Jing Xie, Wanqun Xie, Qianqian Zhang, Yanting Liu, Shaojian Lin, Hong Yao, Hanbing Shang, Kun Yang, Hongyi Liu, Xuefeng Wu, Jianming Zhang, Xun Zhang, Li Xue, Zhe Bao Wu

Published in: Acta Neuropathologica Communications | Issue 1/2024

Login to get access

Abstract

We aimed to identify the druggable cell-intrinsic vulnerabilities and target-based drug therapies for PitNETs using the high-throughput drug screening (HTS) and genomic sequencing methods. We examined 9 patient-derived PitNET primary cells in HTS. Based on the screening results, the potential target genes were analyzed with genomic sequencing from a total of 180 PitNETs. We identified and verified one of the most potentially effective drugs, which targeted the Histone deacetylases (HDACs) both in in vitro and in vivo PitNET models. Further RNA sequencing revealed underlying molecular mechanisms following treatment with the representative HDACs inhibitor, Panobinostat. The HTS generated a total of 20,736 single-agent dose responses which were enriched among multiple inhibitors for various oncogenic targets, including HDACs, PI3K, mTOR, and proteasome. Among these drugs, HDAC inhibitors (HDACIs) were, on average, the most potent drug class. Further studies using in vitro, in vivo, and isolated PitNET primary cell models validated HDACIs, especially Panobinostat, as a promising therapeutic agent. Transcriptional surveys revealed substantial alterations to the Nrf2 signaling following Panobinostat treatment. Moreover, Nrf2 is highly expressed in PitNETs. The combination of Panobinostat and Nrf2 inhibitor ML385 had a synergistic effect on PitNET suppression. The current study revealed a class of effective anti-PitNET drugs, HDACIs, based on the HTS and genomic sequencing. One of the representative compounds, Panobinostat, may be a potential drug for PitNET treatment via Nrf2-mediated redox modulation. Combination of Panobinostat and ML385 further enhance the effectiveness for PitNET treatment.
Appendix
Available only for authorised users
Literature
2.
3.
go back to reference Yang Q, Li X (2019) Molecular network basis of invasive pituitary adenoma: a review. Front Endocrinol (Lausanne) 10:7CrossRefPubMed Yang Q, Li X (2019) Molecular network basis of invasive pituitary adenoma: a review. Front Endocrinol (Lausanne) 10:7CrossRefPubMed
4.
go back to reference Gheorghiu ML, Negreanu F, Fleseriu M (2020) Updates in the medical treatment of pituitary adenomas. Horm Metab Res 52(1):8–24CrossRefPubMed Gheorghiu ML, Negreanu F, Fleseriu M (2020) Updates in the medical treatment of pituitary adenomas. Horm Metab Res 52(1):8–24CrossRefPubMed
5.
go back to reference Maiter D (2019) Management of dopamine agonist-resistant prolactinoma. Neuroendocrinology 109:42–50CrossRefPubMed Maiter D (2019) Management of dopamine agonist-resistant prolactinoma. Neuroendocrinology 109:42–50CrossRefPubMed
7.
go back to reference Wang Z, Zang C, Cui K et al (2009) Genome-wide mapping of HATs and HDACs reveals distinct functions in active and inactive genes. Cell 138(5):1019–1031CrossRefPubMedPubMedCentral Wang Z, Zang C, Cui K et al (2009) Genome-wide mapping of HATs and HDACs reveals distinct functions in active and inactive genes. Cell 138(5):1019–1031CrossRefPubMedPubMedCentral
9.
go back to reference Richardson PG, Moreau P, Laubach JP et al (2017) Deacetylase inhibitors as a novel modality in the treatment of multiple myeloma. Pharmacol Res 117:185–191CrossRefPubMed Richardson PG, Moreau P, Laubach JP et al (2017) Deacetylase inhibitors as a novel modality in the treatment of multiple myeloma. Pharmacol Res 117:185–191CrossRefPubMed
10.
11.
go back to reference Yao H, Xie W, Dai Y et al (2022) TRIM65 determines the fate of a novel subtype of pituitary neuroendocrine tumors via ubiquitination and degradation of TPIT. Neuro Oncol 24(8):1286–1297CrossRefPubMedPubMedCentral Yao H, Xie W, Dai Y et al (2022) TRIM65 determines the fate of a novel subtype of pituitary neuroendocrine tumors via ubiquitination and degradation of TPIT. Neuro Oncol 24(8):1286–1297CrossRefPubMedPubMedCentral
12.
go back to reference Lamb LS, Sim HW, McCormack AI (2020) Exploring the role of novel medical therapies for aggressive pituitary tumors: a review of the literature-"are we there yet?". Cancers (Basel) 12(2):308CrossRefPubMed Lamb LS, Sim HW, McCormack AI (2020) Exploring the role of novel medical therapies for aggressive pituitary tumors: a review of the literature-"are we there yet?". Cancers (Basel) 12(2):308CrossRefPubMed
13.
go back to reference Tzogani K, van Hennik P, Walsh I et al (2018) EMA review of Panobinostat (Farydak) for the treatment of adult patients with relapsed and/or refractory multiple myeloma. Oncologist 23(5):631–636CrossRefPubMed Tzogani K, van Hennik P, Walsh I et al (2018) EMA review of Panobinostat (Farydak) for the treatment of adult patients with relapsed and/or refractory multiple myeloma. Oncologist 23(5):631–636CrossRefPubMed
14.
go back to reference Nguyen TTT, Zhang Y, Shang E et al (2020) HDAC inhibitors elicit metabolic reprogramming by targeting super-enhancers in glioblastoma models. J Clin Investig 130(7):3699–3716CrossRefPubMedPubMedCentral Nguyen TTT, Zhang Y, Shang E et al (2020) HDAC inhibitors elicit metabolic reprogramming by targeting super-enhancers in glioblastoma models. J Clin Investig 130(7):3699–3716CrossRefPubMedPubMedCentral
15.
go back to reference Mishra P, Paital B, Jena S et al (2019) Possible activation of NRF2 by vitamin E/Curcumin against altered thyroid hormone induced oxidative stress via NFĸB/AKT/mTOR/KEAP1 signalling in rat heart. Sci Rep 9(1):7408CrossRefPubMedPubMedCentral Mishra P, Paital B, Jena S et al (2019) Possible activation of NRF2 by vitamin E/Curcumin against altered thyroid hormone induced oxidative stress via NFĸB/AKT/mTOR/KEAP1 signalling in rat heart. Sci Rep 9(1):7408CrossRefPubMedPubMedCentral
16.
go back to reference Wu ZR, Yan L, Liu YT et al (2018) Inhibition of mTORC1 by lncRNA H19 via disrupting 4E-BP1/Raptor interaction in pituitary tumours. Nat Commun 9(1):4624CrossRefPubMedPubMedCentral Wu ZR, Yan L, Liu YT et al (2018) Inhibition of mTORC1 by lncRNA H19 via disrupting 4E-BP1/Raptor interaction in pituitary tumours. Nat Commun 9(1):4624CrossRefPubMedPubMedCentral
17.
go back to reference Tanaka K, Yu HA, Yang S et al (2021) Targeting Aurora B kinase prevents and overcomes resistance to EGFR inhibitors in lung cancer by enhancing BIM- and PUMA-mediated apoptosis. Cancer Cell 39(9):1245–1261CrossRefPubMedPubMedCentral Tanaka K, Yu HA, Yang S et al (2021) Targeting Aurora B kinase prevents and overcomes resistance to EGFR inhibitors in lung cancer by enhancing BIM- and PUMA-mediated apoptosis. Cancer Cell 39(9):1245–1261CrossRefPubMedPubMedCentral
18.
go back to reference Rusert JM, Juarez EF, Brabetz S et al (2020) Functional precision medicine identifies new therapeutic candidates for medulloblastoma. Cancer Res 80(23):5393–5407CrossRefPubMedPubMedCentral Rusert JM, Juarez EF, Brabetz S et al (2020) Functional precision medicine identifies new therapeutic candidates for medulloblastoma. Cancer Res 80(23):5393–5407CrossRefPubMedPubMedCentral
19.
go back to reference Nakada Y, Kageyama K, Sugiyama A et al (2015) Inhibitory effects of trichostatin A on adrenocorticotropic hormone production and proliferation of corticotroph tumor AtT-20 cells. Endocr J 62(12):1083–1090CrossRefPubMed Nakada Y, Kageyama K, Sugiyama A et al (2015) Inhibitory effects of trichostatin A on adrenocorticotropic hormone production and proliferation of corticotroph tumor AtT-20 cells. Endocr J 62(12):1083–1090CrossRefPubMed
20.
go back to reference Zhang D, Damoiseaux R, Babayan L et al (2021) Targeting corticotroph HDAC and PI3-Kinase in cushing disease. J Clin Endocrinol Metab 106(1):e232-246CrossRefPubMed Zhang D, Damoiseaux R, Babayan L et al (2021) Targeting corticotroph HDAC and PI3-Kinase in cushing disease. J Clin Endocrinol Metab 106(1):e232-246CrossRefPubMed
21.
go back to reference Hagiwara R, Kageyama K, Niioka K et al (2021) Involvement of histone deacetylase 1/2 in adrenocorticotropic hormone synthesis and proliferation of corticotroph tumor AtT-20 cells. Peptides 136:170441CrossRefPubMed Hagiwara R, Kageyama K, Niioka K et al (2021) Involvement of histone deacetylase 1/2 in adrenocorticotropic hormone synthesis and proliferation of corticotroph tumor AtT-20 cells. Peptides 136:170441CrossRefPubMed
22.
go back to reference Wang W, Fu L, Li S et al (2017) Histone deacetylase 11 suppresses p53 expression in pituitary tumor cells. Cell Biol Int 41(12):1290–1295CrossRefPubMed Wang W, Fu L, Li S et al (2017) Histone deacetylase 11 suppresses p53 expression in pituitary tumor cells. Cell Biol Int 41(12):1290–1295CrossRefPubMed
23.
24.
go back to reference Hu B, Younes A, Westin JR et al (2018) Phase-I and randomized phase-II trial of panobinostat in combination with ICE (ifosfamide, carboplatin, etoposide) in relapsed or refractory classical Hodgkin lymphoma. Leuk Lymphoma 59(4):863–870CrossRefPubMed Hu B, Younes A, Westin JR et al (2018) Phase-I and randomized phase-II trial of panobinostat in combination with ICE (ifosfamide, carboplatin, etoposide) in relapsed or refractory classical Hodgkin lymphoma. Leuk Lymphoma 59(4):863–870CrossRefPubMed
25.
go back to reference Thomas S, Aggarwal R, Jahan T et al (2016) A phase I trial of panobinostat and epirubicin in solid tumors with a dose expansion in patients with sarcoma. Ann Oncol 27(5):947–952CrossRefPubMedPubMedCentral Thomas S, Aggarwal R, Jahan T et al (2016) A phase I trial of panobinostat and epirubicin in solid tumors with a dose expansion in patients with sarcoma. Ann Oncol 27(5):947–952CrossRefPubMedPubMedCentral
26.
go back to reference Lin GL, Wilson KM, Ceribelli M et al (2019) Therapeutic strategies for diffuse midline glioma from high-throughput combination drug screening. Sci Transl Med 11(519):eaaw0064CrossRefPubMedPubMedCentral Lin GL, Wilson KM, Ceribelli M et al (2019) Therapeutic strategies for diffuse midline glioma from high-throughput combination drug screening. Sci Transl Med 11(519):eaaw0064CrossRefPubMedPubMedCentral
27.
go back to reference Ibrahim N, Buchbinder EI, Granter SR et al (2016) A phase I trial of panobinostat (LBH589) in patients with metastatic melanoma. Cancer Med 5(11):3041–3050CrossRefPubMedPubMedCentral Ibrahim N, Buchbinder EI, Granter SR et al (2016) A phase I trial of panobinostat (LBH589) in patients with metastatic melanoma. Cancer Med 5(11):3041–3050CrossRefPubMedPubMedCentral
28.
go back to reference Xiao L, Somers K, Murray J et al (2021) Dual targeting of chromatin stability by the curaxin CBL0137 and histone deacetylase inhibitor panobinostat shows significant preclinical efficacy in neuroblastoma. Clin Cancer Res 27(15):4338–4352CrossRefPubMedPubMedCentral Xiao L, Somers K, Murray J et al (2021) Dual targeting of chromatin stability by the curaxin CBL0137 and histone deacetylase inhibitor panobinostat shows significant preclinical efficacy in neuroblastoma. Clin Cancer Res 27(15):4338–4352CrossRefPubMedPubMedCentral
29.
go back to reference Cheng YW, Liao LD, Yang Q et al (2018) The histone deacetylase inhibitor panobinostat exerts anticancer effects on esophageal squamous cell carcinoma cells by inducing cell cycle arrest. Cell Biochem Funct 36(8):398–407CrossRefPubMed Cheng YW, Liao LD, Yang Q et al (2018) The histone deacetylase inhibitor panobinostat exerts anticancer effects on esophageal squamous cell carcinoma cells by inducing cell cycle arrest. Cell Biochem Funct 36(8):398–407CrossRefPubMed
30.
go back to reference Waghela BN, Vaidya FU, Pathak C (2021) Upregulation of NOX-2 and Nrf-2 promotes 5-Fluorouracil resistance of human colon carcinoma (HCT-116) cells. Biochemistry 86(3):262–274PubMed Waghela BN, Vaidya FU, Pathak C (2021) Upregulation of NOX-2 and Nrf-2 promotes 5-Fluorouracil resistance of human colon carcinoma (HCT-116) cells. Biochemistry 86(3):262–274PubMed
31.
go back to reference Dai C, Liang S, Sun B et al (2020) The progress of immunotherapy in refractory pituitary adenomas and pituitary carcinomas. Front Endocrinol (Lausanne) 11:608422CrossRefPubMed Dai C, Liang S, Sun B et al (2020) The progress of immunotherapy in refractory pituitary adenomas and pituitary carcinomas. Front Endocrinol (Lausanne) 11:608422CrossRefPubMed
32.
go back to reference Lin SJ, Wu ZR, Cao L et al (2017) Pituitary tumor suppression by combination of cabergoline and chloroquine. J Clin Endocrinol Metab 102(10):3692–3703CrossRefPubMed Lin SJ, Wu ZR, Cao L et al (2017) Pituitary tumor suppression by combination of cabergoline and chloroquine. J Clin Endocrinol Metab 102(10):3692–3703CrossRefPubMed
33.
go back to reference Lin S, Han C, Lou X et al (2022) Hydroxychloroquine overcomes cabergoline resistance in a patient with lactotroph pituitary neuroendocrine tumor: a case report. Front Endocrinol 13:955100CrossRef Lin S, Han C, Lou X et al (2022) Hydroxychloroquine overcomes cabergoline resistance in a patient with lactotroph pituitary neuroendocrine tumor: a case report. Front Endocrinol 13:955100CrossRef
34.
go back to reference Singh A, Venkannagari S, Oh KH et al (2016) Small molecule inhibitor of NRF2 selectively intervenes therapeutic resistance in KEAP1-deficient NSCLC tumors. ACS Chem Biol 11(11):3214–3225CrossRefPubMedPubMedCentral Singh A, Venkannagari S, Oh KH et al (2016) Small molecule inhibitor of NRF2 selectively intervenes therapeutic resistance in KEAP1-deficient NSCLC tumors. ACS Chem Biol 11(11):3214–3225CrossRefPubMedPubMedCentral
35.
go back to reference Qin S, He X, Lin H et al (2021) Nrf2 inhibition sensitizes breast cancer stem cells to ionizing radiation via suppressing DNA repair. Free Radic Biol Med 169:238–247CrossRefPubMedPubMedCentral Qin S, He X, Lin H et al (2021) Nrf2 inhibition sensitizes breast cancer stem cells to ionizing radiation via suppressing DNA repair. Free Radic Biol Med 169:238–247CrossRefPubMedPubMedCentral
36.
go back to reference Liu H, Xu X, Wu R et al (2021) Antioral squamous cell carcinoma effects of carvacrol via inhibiting inflammation, proliferation, and migration related to Nrf2/Keap1 pathway. Biomed Res Int 2021:6616547PubMedPubMedCentral Liu H, Xu X, Wu R et al (2021) Antioral squamous cell carcinoma effects of carvacrol via inhibiting inflammation, proliferation, and migration related to Nrf2/Keap1 pathway. Biomed Res Int 2021:6616547PubMedPubMedCentral
37.
go back to reference Zhang Y, Xin Z, Dong B et al (2022) Combination of the NRF2 inhibitor and autophagy inhibitor significantly inhibited tumorigenicity of castration-resistant prostate cancer. Comput Math Methods Med 2022:4182401PubMedPubMedCentral Zhang Y, Xin Z, Dong B et al (2022) Combination of the NRF2 inhibitor and autophagy inhibitor significantly inhibited tumorigenicity of castration-resistant prostate cancer. Comput Math Methods Med 2022:4182401PubMedPubMedCentral
Metadata
Title
Therapeutic potential of targeting Nrf2 by panobinostat in pituitary neuroendocrine tumors
Authors
Yijun Cheng
Yuting Dai
Hao Tang
Xingyu Lu
Jing Xie
Wanqun Xie
Qianqian Zhang
Yanting Liu
Shaojian Lin
Hong Yao
Hanbing Shang
Kun Yang
Hongyi Liu
Xuefeng Wu
Jianming Zhang
Xun Zhang
Li Xue
Zhe Bao Wu
Publication date
01-12-2024
Publisher
BioMed Central
Published in
Acta Neuropathologica Communications / Issue 1/2024
Electronic ISSN: 2051-5960
DOI
https://doi.org/10.1186/s40478-024-01775-2

Other articles of this Issue 1/2024

Acta Neuropathologica Communications 1/2024 Go to the issue