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Published in: Reviews in Endocrine and Metabolic Disorders 3/2021

Open Access 01-09-2021 | Valproate

Epigenetic regulation of somatostatin and somatostatin receptors in neuroendocrine tumors and other types of cancer

Authors: M.J. Klomp, S.U. Dalm, M. de Jong, R.A. Feelders, J. Hofland, L.J. Hofland

Published in: Reviews in Endocrine and Metabolic Disorders | Issue 3/2021

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Abstract

Both somatostatin (SST) and somatostatin receptors (SSTRs) are proteins with important functions in both physiological tissue and in tumors, particularly in neuroendocrine tumors (NETs). NETs are frequently characterized by high SSTRs expression levels. SST analogues (SSAs) that bind and activate SSTR have anti-proliferative and anti-secretory activity, thereby reducing both the growth as well as the hormonal symptoms of NETs. Moreover, the high expression levels of SSTR type-2 (SSTR2) in NETs is a powerful target for therapy with radiolabeled SSAs. Due to the important role of both SST and SSTRs, it is of great importance to elucidate the mechanisms involved in regulating their expression in NETs, as well as in other types of tumors. The field of epigenetics recently gained interest in NET research, highlighting the importance of this process in regulating the expression of gene and protein expression. In this review we will discuss the role of the epigenetic machinery in controlling the expression of both SSTRs and the neuropeptide SST. Particular attention will be given to the epigenetic regulation of these proteins in NETs, whereas the involvement of the epigenetic machinery in other types of cancer will be discussed as well. In addition, we will discuss the possibility to target enzymes involved in the epigenetic machinery to modify the expression of the SST-system, thereby possibly improving therapeutic options.
Literature
1.
go back to reference Olias G, Viollet C, Kusserow H, Epelbaum J, Meyerhof W. Regulation and function of somatostatin receptors. J Neurochem. 2004;89:1057–91.PubMedCrossRef Olias G, Viollet C, Kusserow H, Epelbaum J, Meyerhof W. Regulation and function of somatostatin receptors. J Neurochem. 2004;89:1057–91.PubMedCrossRef
2.
4.
go back to reference Günther T, Tulipano G, Dournaud P, Bousquet C, Csaba Z, Kreienkamp H-J, et al. International Union of Basic and Clinical Pharmacology. CV. Somatostatin receptors: structure, function, ligands, and new nomenclature. Pharmacol Rev. 2018;70:763–835.PubMedPubMedCentralCrossRef Günther T, Tulipano G, Dournaud P, Bousquet C, Csaba Z, Kreienkamp H-J, et al. International Union of Basic and Clinical Pharmacology. CV. Somatostatin receptors: structure, function, ligands, and new nomenclature. Pharmacol Rev. 2018;70:763–835.PubMedPubMedCentralCrossRef
5.
go back to reference Gatto F, Barbieri F, Arvigo M, Thellung S, Amaru J, Albertelli M, et al. Biological and biochemical basis of the differential efficacy of first and second generation Somatostatin receptor ligands in neuroendocrine neoplasms. Int J Mol Sci. 2019;20:3940.PubMedCentralCrossRef Gatto F, Barbieri F, Arvigo M, Thellung S, Amaru J, Albertelli M, et al. Biological and biochemical basis of the differential efficacy of first and second generation Somatostatin receptor ligands in neuroendocrine neoplasms. Int J Mol Sci. 2019;20:3940.PubMedCentralCrossRef
6.
go back to reference Barbieri F, Bajetto A, Pattarozzi A, Gatti M, Würth R, Thellung S, et al. Peptide receptor targeting in cancer: the somatostatin paradigm. Int J Pept. 2013;2013:926295.PubMedPubMedCentralCrossRef Barbieri F, Bajetto A, Pattarozzi A, Gatti M, Würth R, Thellung S, et al. Peptide receptor targeting in cancer: the somatostatin paradigm. Int J Pept. 2013;2013:926295.PubMedPubMedCentralCrossRef
7.
go back to reference Qian ZR, Li T, Ter-Minassian M, Yang J, Chan JA, Brais LK, et al. Association between Somatostatin receptor expression and clinical outcomes in neuroendocrine tumors. Pancreas. 2016;45:1386–93.PubMedPubMedCentralCrossRef Qian ZR, Li T, Ter-Minassian M, Yang J, Chan JA, Brais LK, et al. Association between Somatostatin receptor expression and clinical outcomes in neuroendocrine tumors. Pancreas. 2016;45:1386–93.PubMedPubMedCentralCrossRef
8.
go back to reference Papotti M, Bongiovanni M, Volante M, Allia E, Landolfi S, Helboe L, et al. Expression of somatostatin receptor types 1-5 in 81 cases of gastrointestinal and pancreatic endocrine tumors. A correlative immunohistochemical and reverse-transcriptase polymerase chain reaction analysis. Virchows Arch. 2002;440:461–75.PubMedCrossRef Papotti M, Bongiovanni M, Volante M, Allia E, Landolfi S, Helboe L, et al. Expression of somatostatin receptor types 1-5 in 81 cases of gastrointestinal and pancreatic endocrine tumors. A correlative immunohistochemical and reverse-transcriptase polymerase chain reaction analysis. Virchows Arch. 2002;440:461–75.PubMedCrossRef
9.
go back to reference Evans AA, Crook T, Laws SA, Gough AC, Royle GT, Primrose JN. Analysis of somatostatin receptor subtype mRNA expression in human breast cancer. Br J Cancer. 1997;75:798–803.PubMedPubMedCentralCrossRef Evans AA, Crook T, Laws SA, Gough AC, Royle GT, Primrose JN. Analysis of somatostatin receptor subtype mRNA expression in human breast cancer. Br J Cancer. 1997;75:798–803.PubMedPubMedCentralCrossRef
10.
go back to reference Qiu C-Z, Wang C, Huang Z-X, Zhu S-Z, Wu Y-Y, Qiu J-L. Relationship between somatostatin receptor subtype expression and clinicopathology, Ki-67, Bcl-2 and p53 in colorectal cancer. World J Gastroenterol. 2006;12:2011–5.PubMedPubMedCentralCrossRef Qiu C-Z, Wang C, Huang Z-X, Zhu S-Z, Wu Y-Y, Qiu J-L. Relationship between somatostatin receptor subtype expression and clinicopathology, Ki-67, Bcl-2 and p53 in colorectal cancer. World J Gastroenterol. 2006;12:2011–5.PubMedPubMedCentralCrossRef
11.
go back to reference Hennigs JK, Müller J, Adam M, Spin JM, Riedel E, Graefen M, et al. Loss of somatostatin receptor subtype 2 in prostate cancer is linked to an aggressive cancer phenotype, high tumor cell proliferation and predicts early metastatic and biochemical relapse. PLoS One. 2014;9:e100469.PubMedPubMedCentralCrossRef Hennigs JK, Müller J, Adam M, Spin JM, Riedel E, Graefen M, et al. Loss of somatostatin receptor subtype 2 in prostate cancer is linked to an aggressive cancer phenotype, high tumor cell proliferation and predicts early metastatic and biochemical relapse. PLoS One. 2014;9:e100469.PubMedPubMedCentralCrossRef
12.
go back to reference Werner C, Dirsch O, Dahmen U, Grimm M-O, Schulz S, Lupp A. Evaluation of Somatostatin and CXCR4 Receptor Expression in a Large Set of Prostate Cancer Samples Using Tissue Microarrays and Well-Characterized Monoclonal Antibodies. Transl Oncol. 2020;13:100801.PubMedPubMedCentralCrossRef Werner C, Dirsch O, Dahmen U, Grimm M-O, Schulz S, Lupp A. Evaluation of Somatostatin and CXCR4 Receptor Expression in a Large Set of Prostate Cancer Samples Using Tissue Microarrays and Well-Characterized Monoclonal Antibodies. Transl Oncol. 2020;13:100801.PubMedPubMedCentralCrossRef
13.
go back to reference Stafford ND, Condon LT, Rogers MJ, MacDonald AW, Atkin SL. The expression of somatostatin receptors 1 and 2 in benign, pre-malignant and malignant laryngeal lesions. Clin Otolaryngol Allied Sci. 2003;28:314–9.PubMedCrossRef Stafford ND, Condon LT, Rogers MJ, MacDonald AW, Atkin SL. The expression of somatostatin receptors 1 and 2 in benign, pre-malignant and malignant laryngeal lesions. Clin Otolaryngol Allied Sci. 2003;28:314–9.PubMedCrossRef
14.
go back to reference Zou Y, Tan H, Zhao Y, Zhou Y, Cao L. Expression and selective activation of somatostatin receptor subtypes induces cell cycle arrest in cancer cells. Oncol Lett. 2019;17:1723–31.PubMed Zou Y, Tan H, Zhao Y, Zhou Y, Cao L. Expression and selective activation of somatostatin receptor subtypes induces cell cycle arrest in cancer cells. Oncol Lett. 2019;17:1723–31.PubMed
15.
go back to reference Singh S, Granberg D, Wolin E, Warner R, Sissons M, Kolarova T, et al. Patient-reported burden of a neuroendocrine tumor (NET) diagnosis: results from the first global survey of patients with NETs. J Glob Oncol. 2016;3:43–53.PubMedPubMedCentralCrossRef Singh S, Granberg D, Wolin E, Warner R, Sissons M, Kolarova T, et al. Patient-reported burden of a neuroendocrine tumor (NET) diagnosis: results from the first global survey of patients with NETs. J Glob Oncol. 2016;3:43–53.PubMedPubMedCentralCrossRef
16.
go back to reference Zandee WT, de Herder WW. The evolution of neuroendocrine tumor treatment reflected by ENETS guidelines. Neuroendocrinology. 2018;106:357–65.PubMedCrossRef Zandee WT, de Herder WW. The evolution of neuroendocrine tumor treatment reflected by ENETS guidelines. Neuroendocrinology. 2018;106:357–65.PubMedCrossRef
17.
go back to reference Hofland J, Kaltsas G, de Herder WW. Advances in the diagnosis and Management of Well-Differentiated Neuroendocrine Neoplasms. Endocr Rev. 2020;41:371–403.PubMedCentralCrossRef Hofland J, Kaltsas G, de Herder WW. Advances in the diagnosis and Management of Well-Differentiated Neuroendocrine Neoplasms. Endocr Rev. 2020;41:371–403.PubMedCentralCrossRef
18.
go back to reference Mizutani G, Nakanishi Y, Watanabe N, Honma T, Obana Y, Seki T, et al. Expression of Somatostatin receptor (SSTR) subtypes (SSTR-1, 2A, 3, 4 and 5) in neuroendocrine tumors using real-time RT-PCR method and immunohistochemistry. Acta Histochem Cytochem. 2012;45:167–76.PubMedPubMedCentralCrossRef Mizutani G, Nakanishi Y, Watanabe N, Honma T, Obana Y, Seki T, et al. Expression of Somatostatin receptor (SSTR) subtypes (SSTR-1, 2A, 3, 4 and 5) in neuroendocrine tumors using real-time RT-PCR method and immunohistochemistry. Acta Histochem Cytochem. 2012;45:167–76.PubMedPubMedCentralCrossRef
19.
go back to reference Stueven AK, Kayser A, Wetz C, Amthauer H, Wree A, Tacke F, et al. Somatostatin analogues in the treatment of neuroendocrine tumors: past. Present and Future Int J Mol Sci. 2019;20:3049.CrossRef Stueven AK, Kayser A, Wetz C, Amthauer H, Wree A, Tacke F, et al. Somatostatin analogues in the treatment of neuroendocrine tumors: past. Present and Future Int J Mol Sci. 2019;20:3049.CrossRef
20.
go back to reference Bergsma H, van Vliet EI, Teunissen JJ, Kam BL, de Herder WW, Peeters RP, et al. Peptide receptor radionuclide therapy (PRRT) for GEP-NETs. Best Pract Res Clin Gastroenterol. 2012;26:867–81.PubMedCrossRef Bergsma H, van Vliet EI, Teunissen JJ, Kam BL, de Herder WW, Peeters RP, et al. Peptide receptor radionuclide therapy (PRRT) for GEP-NETs. Best Pract Res Clin Gastroenterol. 2012;26:867–81.PubMedCrossRef
21.
go back to reference Van Essen M, Krenning EP, De Jong M, Valkema R, Kwekkeboom DJ. Peptide receptor radionuclide therapy with radiolabelled somatostatin analogues in patients with somatostatin receptor positive tumours. Acta Oncol. 2007;46:723–34.PubMedCrossRef Van Essen M, Krenning EP, De Jong M, Valkema R, Kwekkeboom DJ. Peptide receptor radionuclide therapy with radiolabelled somatostatin analogues in patients with somatostatin receptor positive tumours. Acta Oncol. 2007;46:723–34.PubMedCrossRef
22.
go back to reference Ruszniewski P, Valle JW, Lombard-Bohas C, Cuthbertson DJ, Perros P, Holubec L, et al. Patient-reported outcomes with lanreotide autogel/depot for carcinoid syndrome: an international observational study. Dig Liver Dis. 2016;48:552–8.PubMedCrossRef Ruszniewski P, Valle JW, Lombard-Bohas C, Cuthbertson DJ, Perros P, Holubec L, et al. Patient-reported outcomes with lanreotide autogel/depot for carcinoid syndrome: an international observational study. Dig Liver Dis. 2016;48:552–8.PubMedCrossRef
23.
go back to reference O'Toole D, Ducreux M, Bommelaer G, Wemeau JL, Bouche O, Catus F, et al. Treatment of carcinoid syndrome: a prospective crossover evaluation of lanreotide versus octreotide in terms of efficacy, patient acceptability, and tolerance. Cancer. 2000;88:770–6.PubMedCrossRef O'Toole D, Ducreux M, Bommelaer G, Wemeau JL, Bouche O, Catus F, et al. Treatment of carcinoid syndrome: a prospective crossover evaluation of lanreotide versus octreotide in terms of efficacy, patient acceptability, and tolerance. Cancer. 2000;88:770–6.PubMedCrossRef
24.
go back to reference Appetecchia M, Baldelli R. Somatostatin analogues in the treatment of gastroenteropancreatic neuroendocrine tumours, current aspects and new perspectives. J Exp Clin Cancer Res. 2010;29:19.PubMedPubMedCentralCrossRef Appetecchia M, Baldelli R. Somatostatin analogues in the treatment of gastroenteropancreatic neuroendocrine tumours, current aspects and new perspectives. J Exp Clin Cancer Res. 2010;29:19.PubMedPubMedCentralCrossRef
25.
go back to reference Rinke A, Muller HH, Schade-Brittinger C, Klose KJ, Barth P, Wied M, et al. Placebo-controlled, double-blind, prospective, randomized study on the effect of octreotide LAR in the control of tumor growth in patients with metastatic neuroendocrine midgut tumors: a report from the PROMID study group. J Clin Oncol. 2009;27:4656–63.PubMedCrossRef Rinke A, Muller HH, Schade-Brittinger C, Klose KJ, Barth P, Wied M, et al. Placebo-controlled, double-blind, prospective, randomized study on the effect of octreotide LAR in the control of tumor growth in patients with metastatic neuroendocrine midgut tumors: a report from the PROMID study group. J Clin Oncol. 2009;27:4656–63.PubMedCrossRef
26.
go back to reference Caplin ME, Pavel M, Cwikla JB, Phan AT, Raderer M, Sedlackova E, et al. Lanreotide in metastatic enteropancreatic neuroendocrine tumors. N Engl J Med. 2014;371:224–33.PubMedCrossRef Caplin ME, Pavel M, Cwikla JB, Phan AT, Raderer M, Sedlackova E, et al. Lanreotide in metastatic enteropancreatic neuroendocrine tumors. N Engl J Med. 2014;371:224–33.PubMedCrossRef
27.
go back to reference Brabander T, van der Zwan WA, Teunissen JJM, Kam BLR, Feelders RA, de Herder WW, et al. Long-Term Efficacy, Survival, and Safety of [177Lu-DOTA0,Tyr3]octreotate in Patients with Gastroenteropancreatic and Bronchial Neuroendocrine Tumors. Clin Cancer Res. 2017;23:4617–24.PubMedCrossRef Brabander T, van der Zwan WA, Teunissen JJM, Kam BLR, Feelders RA, de Herder WW, et al. Long-Term Efficacy, Survival, and Safety of [177Lu-DOTA0,Tyr3]octreotate in Patients with Gastroenteropancreatic and Bronchial Neuroendocrine Tumors. Clin Cancer Res. 2017;23:4617–24.PubMedCrossRef
28.
go back to reference Kwekkeboom DJ, de Herder WW, Kam BL, van Eijck CH, van Essen M, Kooij PP, et al. Treatment With the Radiolabeled Somatostatin Analog [177Lu-DOTA0,Tyr3]Octreotate: Toxicity, Efficacy, and Survival. J Clin Oncol. 2008;26:2124–30.PubMedCrossRef Kwekkeboom DJ, de Herder WW, Kam BL, van Eijck CH, van Essen M, Kooij PP, et al. Treatment With the Radiolabeled Somatostatin Analog [177Lu-DOTA0,Tyr3]Octreotate: Toxicity, Efficacy, and Survival. J Clin Oncol. 2008;26:2124–30.PubMedCrossRef
29.
go back to reference Strosberg J, El-Haddad G, Wolin E, Hendifar A, Yao J, Chasen B, et al. Phase 3 trial of (177)Lu-Dotatate for Midgut neuroendocrine tumors. N Engl J Med. 2017;376:125–35.PubMedPubMedCentralCrossRef Strosberg J, El-Haddad G, Wolin E, Hendifar A, Yao J, Chasen B, et al. Phase 3 trial of (177)Lu-Dotatate for Midgut neuroendocrine tumors. N Engl J Med. 2017;376:125–35.PubMedPubMedCentralCrossRef
30.
go back to reference van Vliet EI, van Eijck CH, de Krijger RR, Nieveen van Dijkum EJ, Teunissen JJ, Kam BL, et al. Neoadjuvant Treatment of Nonfunctioning Pancreatic Neuroendocrine Tumors with [177Lu-DOTA0,Tyr3]Octreotate. J Nucl Med. 2015;56:1647–53.PubMedCrossRef van Vliet EI, van Eijck CH, de Krijger RR, Nieveen van Dijkum EJ, Teunissen JJ, Kam BL, et al. Neoadjuvant Treatment of Nonfunctioning Pancreatic Neuroendocrine Tumors with [177Lu-DOTA0,Tyr3]Octreotate. J Nucl Med. 2015;56:1647–53.PubMedCrossRef
31.
go back to reference Kwekkeboom DJ, Teunissen JJ, Bakker WH, Kooij PP, de Herder WW, Feelders RA, et al. Radiolabeled Somatostatin Analog [177Lu-DOTA0,Tyr3]Octreotate in Patients With Endocrine Gastroenteropancreatic Tumors. J Clin Oncol. 2005;23:2754–62.PubMedCrossRef Kwekkeboom DJ, Teunissen JJ, Bakker WH, Kooij PP, de Herder WW, Feelders RA, et al. Radiolabeled Somatostatin Analog [177Lu-DOTA0,Tyr3]Octreotate in Patients With Endocrine Gastroenteropancreatic Tumors. J Clin Oncol. 2005;23:2754–62.PubMedCrossRef
32.
go back to reference Righi L, Volante M, Tavaglione V, Bille A, Daniele L, Angusti T, et al. Somatostatin receptor tissue distribution in lung neuroendocrine tumours: a clinicopathologic and immunohistochemical study of 218 'clinically aggressive' cases. Ann Oncol. 2010;21:548–55.PubMedCrossRef Righi L, Volante M, Tavaglione V, Bille A, Daniele L, Angusti T, et al. Somatostatin receptor tissue distribution in lung neuroendocrine tumours: a clinicopathologic and immunohistochemical study of 218 'clinically aggressive' cases. Ann Oncol. 2010;21:548–55.PubMedCrossRef
33.
go back to reference Diakatou E, Kaltsas G, Tzivras M, Kanakis G, Papaliodi E, Kontogeorgos G. Somatostatin and dopamine receptor profile of gastroenteropancreatic neuroendocrine tumors: an immunohistochemical study. Endocr Pathol. 2011;22:24–30.PubMedCrossRef Diakatou E, Kaltsas G, Tzivras M, Kanakis G, Papaliodi E, Kontogeorgos G. Somatostatin and dopamine receptor profile of gastroenteropancreatic neuroendocrine tumors: an immunohistochemical study. Endocr Pathol. 2011;22:24–30.PubMedCrossRef
34.
go back to reference Di Domenico A, Wiedmer T, Marinoni I, Perren A. Genetic and epigenetic drivers of neuroendocrine tumours (NET). Endocr Relat Cancer. 2017;24:R315–R34.PubMedCrossRef Di Domenico A, Wiedmer T, Marinoni I, Perren A. Genetic and epigenetic drivers of neuroendocrine tumours (NET). Endocr Relat Cancer. 2017;24:R315–R34.PubMedCrossRef
37.
39.
go back to reference Jeffries MA, Sawalha AH. Autoimmune disease in the epigenetic era: how has epigenetics changed our understanding of disease and how can we expect the field to evolve? Expert Rev Clin Immunol. 2015;11:45–58.PubMedPubMedCentralCrossRef Jeffries MA, Sawalha AH. Autoimmune disease in the epigenetic era: how has epigenetics changed our understanding of disease and how can we expect the field to evolve? Expert Rev Clin Immunol. 2015;11:45–58.PubMedPubMedCentralCrossRef
40.
go back to reference Finnerty BM, Gray KD, Moore MD, Zarnegar R, Fahey Iii TJ. Epigenetics of gastroenteropancreatic neuroendocrine tumors: a clinicopathologic perspective. World J Gastrointest Oncol. 2017;9:341–53.PubMedPubMedCentralCrossRef Finnerty BM, Gray KD, Moore MD, Zarnegar R, Fahey Iii TJ. Epigenetics of gastroenteropancreatic neuroendocrine tumors: a clinicopathologic perspective. World J Gastrointest Oncol. 2017;9:341–53.PubMedPubMedCentralCrossRef
42.
go back to reference Maleszewska M, Kaminska B. Is glioblastoma an epigenetic malignancy? Cancers (Basel). 2013;5:1120–39.CrossRef Maleszewska M, Kaminska B. Is glioblastoma an epigenetic malignancy? Cancers (Basel). 2013;5:1120–39.CrossRef
43.
go back to reference Alaskhar Alhamwe B, Khalaila R, Wolf J, von Bülow V, Harb H, Alhamdan F, et al. Histone modifications and their role in epigenetics of atopy and allergic diseases. Allergy Asthma Clin Immunol. 2018;14:39.PubMedPubMedCentralCrossRef Alaskhar Alhamwe B, Khalaila R, Wolf J, von Bülow V, Harb H, Alhamdan F, et al. Histone modifications and their role in epigenetics of atopy and allergic diseases. Allergy Asthma Clin Immunol. 2018;14:39.PubMedPubMedCentralCrossRef
44.
go back to reference Moore LD, Le T, Fan G. DNA methylation and its basic function. Neuropsychopharmacology. 2013;38:23–38.PubMedCrossRef Moore LD, Le T, Fan G. DNA methylation and its basic function. Neuropsychopharmacology. 2013;38:23–38.PubMedCrossRef
45.
go back to reference Hervouet E, Peixoto P, Delage-Mourroux R, Boyer-Guittaut M, Cartron P-F. Specific or not specific recruitment of DNMTs for DNA methylation, an epigenetic dilemma. Clin Epigenetics. 2018;10:17.PubMedPubMedCentralCrossRef Hervouet E, Peixoto P, Delage-Mourroux R, Boyer-Guittaut M, Cartron P-F. Specific or not specific recruitment of DNMTs for DNA methylation, an epigenetic dilemma. Clin Epigenetics. 2018;10:17.PubMedPubMedCentralCrossRef
46.
go back to reference Hessmann E, Johnsen S, Siveke J, Ellenrieder V. Epigenetic treatment of pancreatic cancer: is there a therapeutic perspective on the horizon? Gut. 2016;66:168–79.PubMedCrossRef Hessmann E, Johnsen S, Siveke J, Ellenrieder V. Epigenetic treatment of pancreatic cancer: is there a therapeutic perspective on the horizon? Gut. 2016;66:168–79.PubMedCrossRef
48.
go back to reference Klieser E, Urbas R, Stattner S, Primavesi F, Jager T, Dinnewitzer A, et al. Comprehensive immunohistochemical analysis of histone deacetylases in pancreatic neuroendocrine tumors: HDAC5 as a predictor of poor clinical outcome. Hum Pathol. 2017;65:41–52.PubMedCrossRef Klieser E, Urbas R, Stattner S, Primavesi F, Jager T, Dinnewitzer A, et al. Comprehensive immunohistochemical analysis of histone deacetylases in pancreatic neuroendocrine tumors: HDAC5 as a predictor of poor clinical outcome. Hum Pathol. 2017;65:41–52.PubMedCrossRef
49.
go back to reference Alvarez MJ, Subramaniam PS, Tang LH, Grunn A, Aburi M, Rieckhof G, et al. A precision oncology approach to the pharmacological targeting of mechanistic dependencies in neuroendocrine tumors. Nat Genet. 2018;50:979–89.PubMedPubMedCentralCrossRef Alvarez MJ, Subramaniam PS, Tang LH, Grunn A, Aburi M, Rieckhof G, et al. A precision oncology approach to the pharmacological targeting of mechanistic dependencies in neuroendocrine tumors. Nat Genet. 2018;50:979–89.PubMedPubMedCentralCrossRef
51.
go back to reference Petersenn S, Rasch AC, Presch S, Beil FU, Schulte HM. Genomic structure and transcriptional regulation of the human somatostatin receptor type 2. Mol Cell Endocrinol. 1999;157:75–85.PubMedCrossRef Petersenn S, Rasch AC, Presch S, Beil FU, Schulte HM. Genomic structure and transcriptional regulation of the human somatostatin receptor type 2. Mol Cell Endocrinol. 1999;157:75–85.PubMedCrossRef
52.
go back to reference Xu Y, Berelowitz M, Bruno JF. Characterization of the promoter region of the human somatostatin receptor subtype 2 gene and localization of sequences required for estrogen-responsiveness. Mol Cell Endocrinol. 1998;139:71–7.PubMedCrossRef Xu Y, Berelowitz M, Bruno JF. Characterization of the promoter region of the human somatostatin receptor subtype 2 gene and localization of sequences required for estrogen-responsiveness. Mol Cell Endocrinol. 1998;139:71–7.PubMedCrossRef
53.
go back to reference Pscherer A, Dorflinger U, Kirfel J, Gawlas K, Ruschoff J, Buettner R, et al. The helix-loop-helix transcription factor SEF-2 regulates the activity of a novel initiator element in the promoter of the human somatostatin receptor II gene. EMBO J. 1996;15:6680–90.PubMedPubMedCentralCrossRef Pscherer A, Dorflinger U, Kirfel J, Gawlas K, Ruschoff J, Buettner R, et al. The helix-loop-helix transcription factor SEF-2 regulates the activity of a novel initiator element in the promoter of the human somatostatin receptor II gene. EMBO J. 1996;15:6680–90.PubMedPubMedCentralCrossRef
54.
go back to reference Torrisani J, Hanoun N, Laurell H, Lopez F, Maoret JJ, Souque A, et al. Identification of an upstream promoter of the human somatostatin receptor, hSSTR2, which is controlled by epigenetic modifications. Endocrinology. 2008;149:3137–47.PubMedCrossRef Torrisani J, Hanoun N, Laurell H, Lopez F, Maoret JJ, Souque A, et al. Identification of an upstream promoter of the human somatostatin receptor, hSSTR2, which is controlled by epigenetic modifications. Endocrinology. 2008;149:3137–47.PubMedCrossRef
55.
go back to reference Veenstra MJ, van Koetsveld PM, Dogan F, Farrell WE, Feelders RA, Lamberts SWJ, et al. Epidrug-induced upregulation of functional somatostatin type 2 receptors in human pancreatic neuroendocrine tumor cells. Oncotarget. 2018;9:14791–802.PubMedCrossRef Veenstra MJ, van Koetsveld PM, Dogan F, Farrell WE, Feelders RA, Lamberts SWJ, et al. Epidrug-induced upregulation of functional somatostatin type 2 receptors in human pancreatic neuroendocrine tumor cells. Oncotarget. 2018;9:14791–802.PubMedCrossRef
56.
go back to reference Wanek J, Gaisberger M, Beyreis M, Mayr C, Helm K, Primavesi F, et al. Pharmacological inhibition of class IIA HDACs by LMK-235 in pancreatic neuroendocrine tumor cells. Int J Mol Sci. 2018;19:3128.PubMedCentralCrossRef Wanek J, Gaisberger M, Beyreis M, Mayr C, Helm K, Primavesi F, et al. Pharmacological inhibition of class IIA HDACs by LMK-235 in pancreatic neuroendocrine tumor cells. Int J Mol Sci. 2018;19:3128.PubMedCentralCrossRef
57.
go back to reference Taelman VF, Radojewski P, Marincek N, Ben-Shlomo A, Grotzky A, Olariu CI, et al. Upregulation of key molecules for targeted imaging and therapy. J Nucl Med. 2016;57:1805–10.PubMedCrossRef Taelman VF, Radojewski P, Marincek N, Ben-Shlomo A, Grotzky A, Olariu CI, et al. Upregulation of key molecules for targeted imaging and therapy. J Nucl Med. 2016;57:1805–10.PubMedCrossRef
58.
go back to reference Jin XF, Auernhammer CJ, Ilhan H, Lindner S, Nölting S, Maurer J, et al. Combination of 5-fluorouracil with epigenetic modifiers induces radiosensitization, somatostatin receptor 2 expression, and radioligand binding in neuroendocrine tumor cells in vitro. J Nucl Med. 2019;60:1240–6.PubMedCrossRef Jin XF, Auernhammer CJ, Ilhan H, Lindner S, Nölting S, Maurer J, et al. Combination of 5-fluorouracil with epigenetic modifiers induces radiosensitization, somatostatin receptor 2 expression, and radioligand binding in neuroendocrine tumor cells in vitro. J Nucl Med. 2019;60:1240–6.PubMedCrossRef
59.
go back to reference Guenter R, Aweda T, Carmona Matos DM, Jang S, Whitt J, Cheng Y-Q, et al. Overexpression of somatostatin receptor type 2 in neuroendocrine tumors for improved Ga68-DOTATATE imaging and treatment. Surgery. 2019;167:189–96.PubMedCrossRef Guenter R, Aweda T, Carmona Matos DM, Jang S, Whitt J, Cheng Y-Q, et al. Overexpression of somatostatin receptor type 2 in neuroendocrine tumors for improved Ga68-DOTATATE imaging and treatment. Surgery. 2019;167:189–96.PubMedCrossRef
60.
go back to reference Sun L, Qian Q, Sun G, Mackey LV, Fuselier JA, Coy DH, et al. Valproic acid induces NET cell growth arrest and enhances tumor suppression of the receptor-targeted peptide-drug conjugate via activating somatostatin receptor type II. J Drug Target. 2016;24:169–77.PubMedCrossRef Sun L, Qian Q, Sun G, Mackey LV, Fuselier JA, Coy DH, et al. Valproic acid induces NET cell growth arrest and enhances tumor suppression of the receptor-targeted peptide-drug conjugate via activating somatostatin receptor type II. J Drug Target. 2016;24:169–77.PubMedCrossRef
61.
go back to reference Arvidsson Y, Johanson V, Pfragner R, Wangberg B, Nilsson O. Cytotoxic effects of Valproic acid on neuroendocrine tumour cells. Neuroendocrinology. 2016;103:578–91.PubMedCrossRef Arvidsson Y, Johanson V, Pfragner R, Wangberg B, Nilsson O. Cytotoxic effects of Valproic acid on neuroendocrine tumour cells. Neuroendocrinology. 2016;103:578–91.PubMedCrossRef
62.
go back to reference Li SC, Martijn C, Cui T, Essaghir A, Luque RM, Demoulin JB, et al. The somatostatin analogue octreotide inhibits growth of small intestine neuroendocrine tumour cells. PLoS One. 2012;7:e48411.PubMedPubMedCentralCrossRef Li SC, Martijn C, Cui T, Essaghir A, Luque RM, Demoulin JB, et al. The somatostatin analogue octreotide inhibits growth of small intestine neuroendocrine tumour cells. PLoS One. 2012;7:e48411.PubMedPubMedCentralCrossRef
63.
go back to reference Hofving T, Arvidsson Y, Almobarak B, Inge L, Pfragner R, Persson M, et al. The neuroendocrine phenotype, genomic profile and therapeutic sensitivity of GEPNET cell lines. Endocr Relat Cancer. 2018;25:367–80.PubMedPubMedCentralCrossRef Hofving T, Arvidsson Y, Almobarak B, Inge L, Pfragner R, Persson M, et al. The neuroendocrine phenotype, genomic profile and therapeutic sensitivity of GEPNET cell lines. Endocr Relat Cancer. 2018;25:367–80.PubMedPubMedCentralCrossRef
64.
go back to reference Alvarez MJ, Yan P, Alpaugh ML, Bowden M, Sicinska E, Zhou CW, et al. Reply to ‘H-STS, L-STS and KRJ-I are not authentic GEPNET cell lines’. Nat Genet. 2019;51:1427–8.PubMedPubMedCentralCrossRef Alvarez MJ, Yan P, Alpaugh ML, Bowden M, Sicinska E, Zhou CW, et al. Reply to ‘H-STS, L-STS and KRJ-I are not authentic GEPNET cell lines’. Nat Genet. 2019;51:1427–8.PubMedPubMedCentralCrossRef
65.
go back to reference Guenter RE, Aweda T, Carmona Matos DM, Whitt J, Chang AW, Cheng EY, et al. Pulmonary Carcinoid Surface Receptor Modulation Using Histone Deacetylase Inhibitors. Cancers (Basel). 2019;11:767.CrossRef Guenter RE, Aweda T, Carmona Matos DM, Whitt J, Chang AW, Cheng EY, et al. Pulmonary Carcinoid Surface Receptor Modulation Using Histone Deacetylase Inhibitors. Cancers (Basel). 2019;11:767.CrossRef
66.
go back to reference Chen G, Jaskula-Sztul R, Harrison A, Dammalapati A, Xu W, Cheng Y, et al. KE108-conjugated unimolecular micelles loaded with a novel HDAC inhibitor thailandepsin-a for targeted neuroendocrine cancer therapy. Biomaterials. 2016;97:22–33.PubMedPubMedCentralCrossRef Chen G, Jaskula-Sztul R, Harrison A, Dammalapati A, Xu W, Cheng Y, et al. KE108-conjugated unimolecular micelles loaded with a novel HDAC inhibitor thailandepsin-a for targeted neuroendocrine cancer therapy. Biomaterials. 2016;97:22–33.PubMedPubMedCentralCrossRef
67.
go back to reference Jaskula-Sztul R, Chen G, Dammalapati A, Harrison A, Tang W, Gong S, et al. AB3-loaded and tumor-targeted Unimolecular micelles for medullary thyroid Cancer treatment. J Mater Chem B. 2017;5:151–9.PubMedCrossRef Jaskula-Sztul R, Chen G, Dammalapati A, Harrison A, Tang W, Gong S, et al. AB3-loaded and tumor-targeted Unimolecular micelles for medullary thyroid Cancer treatment. J Mater Chem B. 2017;5:151–9.PubMedCrossRef
68.
go back to reference Jaskula-Sztul R, Xu W, Chen G, Harrison A, Dammalapati A, Nair R, et al. Thailandepsin A-loaded and octreotide-functionalized unimolecular micelles for targeted neuroendocrine cancer therapy. Biomaterials. 2016;91:1–10.PubMedPubMedCentralCrossRef Jaskula-Sztul R, Xu W, Chen G, Harrison A, Dammalapati A, Nair R, et al. Thailandepsin A-loaded and octreotide-functionalized unimolecular micelles for targeted neuroendocrine cancer therapy. Biomaterials. 2016;91:1–10.PubMedPubMedCentralCrossRef
69.
go back to reference Liu J, Li H, Sun L, Wang Z, Xing C, Yuan Y. Aberrantly methylated-differentially expressed genes and pathways in colorectal cancer. Cancer Cell Int. 2017;17:75.PubMedPubMedCentralCrossRef Liu J, Li H, Sun L, Wang Z, Xing C, Yuan Y. Aberrantly methylated-differentially expressed genes and pathways in colorectal cancer. Cancer Cell Int. 2017;17:75.PubMedPubMedCentralCrossRef
70.
go back to reference Misawa K, Misawa Y, Kondo H, Mochizuki D, Imai A, Fukushima H, et al. Aberrant methylation inactivates somatostatin and somatostatin receptor type 1 in head and neck squamous cell carcinoma. PLoS One. 2015;10:e0118588.PubMedPubMedCentralCrossRef Misawa K, Misawa Y, Kondo H, Mochizuki D, Imai A, Fukushima H, et al. Aberrant methylation inactivates somatostatin and somatostatin receptor type 1 in head and neck squamous cell carcinoma. PLoS One. 2015;10:e0118588.PubMedPubMedCentralCrossRef
71.
go back to reference Shen Z, Chen X, Li Q, Zhou C, Li J, Ye H, et al. SSTR2 promoter hypermethylation is associated with the risk and progression of laryngeal squamous cell carcinoma in males. Diagn Pathol. 2016;11:10.PubMedPubMedCentralCrossRef Shen Z, Chen X, Li Q, Zhou C, Li J, Ye H, et al. SSTR2 promoter hypermethylation is associated with the risk and progression of laryngeal squamous cell carcinoma in males. Diagn Pathol. 2016;11:10.PubMedPubMedCentralCrossRef
72.
go back to reference Zhao J, Liang Q, Cheung KF, Kang W, Lung RWM, Tong JHM, et al. Genome-wide identification of Epstein-Barr virus-driven promoter methylation profiles of human genes in gastric cancer cells. Cancer. 2013;119:304–12.PubMedCrossRef Zhao J, Liang Q, Cheung KF, Kang W, Lung RWM, Tong JHM, et al. Genome-wide identification of Epstein-Barr virus-driven promoter methylation profiles of human genes in gastric cancer cells. Cancer. 2013;119:304–12.PubMedCrossRef
73.
go back to reference Shi X, Li X, Chen L, Wang C. Analysis of somatostatin receptors and somatostatin promoter methylation in human gastric cancer. Oncol Lett. 2013;6:1794–8.PubMedPubMedCentralCrossRef Shi X, Li X, Chen L, Wang C. Analysis of somatostatin receptors and somatostatin promoter methylation in human gastric cancer. Oncol Lett. 2013;6:1794–8.PubMedPubMedCentralCrossRef
74.
go back to reference Kim HJ, Kang TW, Haam K, Kim M, Kim SK, Kim SY, et al. Whole genome MBD-seq and RRBS analyses reveal that hypermethylation of gastrointestinal hormone receptors is associated with gastric carcinogenesis. Exp Mol Med. 2018;50:1–14.PubMedPubMedCentral Kim HJ, Kang TW, Haam K, Kim M, Kim SK, Kim SY, et al. Whole genome MBD-seq and RRBS analyses reveal that hypermethylation of gastrointestinal hormone receptors is associated with gastric carcinogenesis. Exp Mol Med. 2018;50:1–14.PubMedPubMedCentral
75.
go back to reference Sun G, Mackey LV, Coy DH, Yu CY, Sun L. The histone deacetylase inhibitor vaproic acid induces cell growth arrest in hepatocellular carcinoma cells via suppressing notch signaling. J Cancer. 2015;6:996–1004.PubMedPubMedCentralCrossRef Sun G, Mackey LV, Coy DH, Yu CY, Sun L. The histone deacetylase inhibitor vaproic acid induces cell growth arrest in hepatocellular carcinoma cells via suppressing notch signaling. J Cancer. 2015;6:996–1004.PubMedPubMedCentralCrossRef
76.
go back to reference Sun L, He Q, Tsai C, Lei J, Chen J, Makcey LV, et al. HDAC inhibitors suppressed small cell lung cancer cell growth and enhanced the suppressive effects of receptor-targeting cytotoxins via upregulating somatostatin receptor II. Am J Transl Res. 2018;10:545–53.PubMedPubMedCentral Sun L, He Q, Tsai C, Lei J, Chen J, Makcey LV, et al. HDAC inhibitors suppressed small cell lung cancer cell growth and enhanced the suppressive effects of receptor-targeting cytotoxins via upregulating somatostatin receptor II. Am J Transl Res. 2018;10:545–53.PubMedPubMedCentral
77.
go back to reference Franko-Tobin LG, Mackey LV, Huang W, Song X, Jin B, Luo J, et al. Notch1-mediated tumor suppression in cervical cancer with the involvement of SST signaling and its application in enhanced SSTR-targeted therapeutics. Oncologist. 2012;17:220–32.PubMedPubMedCentralCrossRef Franko-Tobin LG, Mackey LV, Huang W, Song X, Jin B, Luo J, et al. Notch1-mediated tumor suppression in cervical cancer with the involvement of SST signaling and its application in enhanced SSTR-targeted therapeutics. Oncologist. 2012;17:220–32.PubMedPubMedCentralCrossRef
78.
go back to reference Tsai C, Leslie JS, Franko-Tobin LG, Prasnal MC, Yang T, Vienna Mackey L, et al. Valproic acid suppresses cervical cancer tumor progression possibly via activating Notch1 signaling and enhances receptor-targeted cancer chemotherapeutic via activating somatostatin receptor type II. Arch Gynecol Obstet. 2013;288:393–400.PubMedCrossRef Tsai C, Leslie JS, Franko-Tobin LG, Prasnal MC, Yang T, Vienna Mackey L, et al. Valproic acid suppresses cervical cancer tumor progression possibly via activating Notch1 signaling and enhances receptor-targeted cancer chemotherapeutic via activating somatostatin receptor type II. Arch Gynecol Obstet. 2013;288:393–400.PubMedCrossRef
79.
go back to reference Gailhouste L, Liew LC, Hatada I, Nakagama H, Ochiya T. Epigenetic reprogramming using 5-azacytidine promotes an anti-cancer response in pancreatic adenocarcinoma cells. Cell Death Dis. 2018;9:468.PubMedPubMedCentralCrossRef Gailhouste L, Liew LC, Hatada I, Nakagama H, Ochiya T. Epigenetic reprogramming using 5-azacytidine promotes an anti-cancer response in pancreatic adenocarcinoma cells. Cell Death Dis. 2018;9:468.PubMedPubMedCentralCrossRef
80.
go back to reference Wang B, Zhao L, Chi W, Cao H, Cui W, Meng W. Aberrant methylation-mediated downregulation of lncRNA SSTR5-AS1 promotes progression and metastasis of laryngeal squamous cell carcinoma. Epigenetics Chromatin. 2019;12:35.PubMedPubMedCentralCrossRef Wang B, Zhao L, Chi W, Cao H, Cui W, Meng W. Aberrant methylation-mediated downregulation of lncRNA SSTR5-AS1 promotes progression and metastasis of laryngeal squamous cell carcinoma. Epigenetics Chromatin. 2019;12:35.PubMedPubMedCentralCrossRef
81.
go back to reference Liu Z, Marquez M, Nilsson S, Holmberg AR. Incubation with somatostatin, 5-aza decitabine and trichostatin up-regulates somatostatin receptor expression in prostate cancer cells. Oncol Rep. 2008;20:151–4.PubMed Liu Z, Marquez M, Nilsson S, Holmberg AR. Incubation with somatostatin, 5-aza decitabine and trichostatin up-regulates somatostatin receptor expression in prostate cancer cells. Oncol Rep. 2008;20:151–4.PubMed
82.
go back to reference White-Al Habeeb NMA, Ho LT, Olkhov-Mitsel E, Kron K, Pethe V, Lehman M, et al. Integrated analysis of epigenomic and genomic changes by DNA methylation dependent mechanisms provides potential novel biomarkers for prostate cancer. Oncotarget. 2014;5:7858–69.PubMedPubMedCentralCrossRef White-Al Habeeb NMA, Ho LT, Olkhov-Mitsel E, Kron K, Pethe V, Lehman M, et al. Integrated analysis of epigenomic and genomic changes by DNA methylation dependent mechanisms provides potential novel biomarkers for prostate cancer. Oncotarget. 2014;5:7858–69.PubMedPubMedCentralCrossRef
83.
go back to reference Zhao J, Liang Q, Cheung KF, Kang W, Dong Y, Lung RWM, et al. Somatostatin receptor 1, a novel EBV-associated CpG hypermethylated gene, contributes to the pathogenesis of EBV-associated gastric cancer. Br J Cancer. 2013;108:2557–64.PubMedPubMedCentralCrossRef Zhao J, Liang Q, Cheung KF, Kang W, Dong Y, Lung RWM, et al. Somatostatin receptor 1, a novel EBV-associated CpG hypermethylated gene, contributes to the pathogenesis of EBV-associated gastric cancer. Br J Cancer. 2013;108:2557–64.PubMedPubMedCentralCrossRef
84.
go back to reference Chen W, Ding R, Tang J, Li H, Chen C, Zhang Y, et al. Knocking out SST gene of BGC823 gastric Cancer cell by CRISPR/Cas9 enhances migration, invasion and expression of SEMA5A and KLF2. Cancer Manag Res. 2020;12:1313–21.PubMedPubMedCentralCrossRef Chen W, Ding R, Tang J, Li H, Chen C, Zhang Y, et al. Knocking out SST gene of BGC823 gastric Cancer cell by CRISPR/Cas9 enhances migration, invasion and expression of SEMA5A and KLF2. Cancer Manag Res. 2020;12:1313–21.PubMedPubMedCentralCrossRef
85.
go back to reference Pyronnet S, Bousquet C, Najib S, Azar R, Laklai H, Susini C. Antitumor effects of somatostatin. Mol Cell Endocrinol. 2008;286:230–7.PubMedCrossRef Pyronnet S, Bousquet C, Najib S, Azar R, Laklai H, Susini C. Antitumor effects of somatostatin. Mol Cell Endocrinol. 2008;286:230–7.PubMedCrossRef
86.
go back to reference Wu J, Gu Y, Xiao Y, Xia C, Li H, Kang Y, et al. Characterization of DNA methylation associated gene regulatory networks during stomach Cancer progression. Front Genet. 2018;9:711.PubMedCrossRef Wu J, Gu Y, Xiao Y, Xia C, Li H, Kang Y, et al. Characterization of DNA methylation associated gene regulatory networks during stomach Cancer progression. Front Genet. 2018;9:711.PubMedCrossRef
87.
go back to reference Jackson K, Soutto M, Peng D, Hu T, Marshal D, El-Rifai W. Epigenetic silencing of somatostatin in gastric cancer. Dig Dis Sci. 2011;56:125–30.PubMedCrossRef Jackson K, Soutto M, Peng D, Hu T, Marshal D, El-Rifai W. Epigenetic silencing of somatostatin in gastric cancer. Dig Dis Sci. 2011;56:125–30.PubMedCrossRef
88.
go back to reference Li H, Liu JW, Liu S, Yuan Y, Sun LP. Bioinformatics-based identification of methylated-differentially expressed genes and related pathways in gastric Cancer. Dig Dis Sci. 2017;62:3029–39.PubMedCrossRef Li H, Liu JW, Liu S, Yuan Y, Sun LP. Bioinformatics-based identification of methylated-differentially expressed genes and related pathways in gastric Cancer. Dig Dis Sci. 2017;62:3029–39.PubMedCrossRef
89.
go back to reference Zhang X, Yang JJ, Kim YS, Kim KY, Ahn WS, Yang S. An 8-gene signature, including methylated and down-regulated glutathione peroxidase 3, of gastric cancer. Int J Oncol. 2010;36:405–14.PubMed Zhang X, Yang JJ, Kim YS, Kim KY, Ahn WS, Yang S. An 8-gene signature, including methylated and down-regulated glutathione peroxidase 3, of gastric cancer. Int J Oncol. 2010;36:405–14.PubMed
90.
go back to reference Ricketts CJ, Morris MR, Gentle D, Brown M, Wake N, Woodward ER, et al. Genome-wide CpG island methylation analysis implicates novel genes in the pathogenesis of renal cell carcinoma. Epigenetics. 2012;7:278–90.PubMedPubMedCentralCrossRef Ricketts CJ, Morris MR, Gentle D, Brown M, Wake N, Woodward ER, et al. Genome-wide CpG island methylation analysis implicates novel genes in the pathogenesis of renal cell carcinoma. Epigenetics. 2012;7:278–90.PubMedPubMedCentralCrossRef
91.
go back to reference Morris MR, Gentle D, Abdulrahman M, Clarke N, Brown M, Kishida T, et al. Functional epigenomics approach to identify methylated candidate tumour suppressor genes in renal cell carcinoma. Br J Cancer. 2008;98:496–501.PubMedPubMedCentralCrossRef Morris MR, Gentle D, Abdulrahman M, Clarke N, Brown M, Kishida T, et al. Functional epigenomics approach to identify methylated candidate tumour suppressor genes in renal cell carcinoma. Br J Cancer. 2008;98:496–501.PubMedPubMedCentralCrossRef
92.
go back to reference Patai ÁV, Valcz G, Hollósi P, Kalmár A, Péterfia B, Patai Á, et al. Comprehensive DNA methylation analysis reveals a common ten-gene methylation signature in colorectal adenomas and carcinomas. PLoS One. 2015;10:e0133836.PubMedPubMedCentralCrossRef Patai ÁV, Valcz G, Hollósi P, Kalmár A, Péterfia B, Patai Á, et al. Comprehensive DNA methylation analysis reveals a common ten-gene methylation signature in colorectal adenomas and carcinomas. PLoS One. 2015;10:e0133836.PubMedPubMedCentralCrossRef
93.
go back to reference Leiszter K, Sipos F, Galamb O, Krenács T, Veres G, Wichmann B, et al. Promoter hypermethylation-related reduced somatostatin production promotes uncontrolled cell proliferation in colorectal cancer. PLoS One. 2015;10:e0118332.PubMedPubMedCentralCrossRef Leiszter K, Sipos F, Galamb O, Krenács T, Veres G, Wichmann B, et al. Promoter hypermethylation-related reduced somatostatin production promotes uncontrolled cell proliferation in colorectal cancer. PLoS One. 2015;10:e0118332.PubMedPubMedCentralCrossRef
94.
go back to reference Patai ÁV, Barták BK, Péterfia B, Micsik T, Horváth R, Sumánszki C, et al. Comprehensive DNA methylation and mutation analyses reveal a methylation signature in colorectal sessile serrated adenomas. Pathol Oncol Res. 2017;23:589–94.PubMedCrossRef Patai ÁV, Barták BK, Péterfia B, Micsik T, Horváth R, Sumánszki C, et al. Comprehensive DNA methylation and mutation analyses reveal a methylation signature in colorectal sessile serrated adenomas. Pathol Oncol Res. 2017;23:589–94.PubMedCrossRef
95.
go back to reference Kok-Sin T, Mokhtar NM, Ali Hassan NZ, Sagap I, Mohamed Rose I, Harun R, et al. Identification of diagnostic markers in colorectal cancer via integrative epigenomics and genomics data. Oncol Rep. 2015;34:22–32.PubMedPubMedCentralCrossRef Kok-Sin T, Mokhtar NM, Ali Hassan NZ, Sagap I, Mohamed Rose I, Harun R, et al. Identification of diagnostic markers in colorectal cancer via integrative epigenomics and genomics data. Oncol Rep. 2015;34:22–32.PubMedPubMedCentralCrossRef
96.
go back to reference Mori Y, Cai K, Cheng Y, Wang S, Paun B, Hamilton JP, et al. A genome-wide search identifies epigenetic silencing of Somatostatin, Tachykinin-1, and 5 other genes in Colon Cancer. Gastroenterology. 2006;131:797–808.PubMedCrossRef Mori Y, Cai K, Cheng Y, Wang S, Paun B, Hamilton JP, et al. A genome-wide search identifies epigenetic silencing of Somatostatin, Tachykinin-1, and 5 other genes in Colon Cancer. Gastroenterology. 2006;131:797–808.PubMedCrossRef
97.
go back to reference Zhang M, Lv X, Jiang Y, Li G, Qiao Q. Identification of aberrantly methylated differentially expressed genes in glioblastoma multiforme and their association with patient survival. Exp Ther Med. 2019;18:2140–52.PubMedPubMedCentral Zhang M, Lv X, Jiang Y, Li G, Qiao Q. Identification of aberrantly methylated differentially expressed genes in glioblastoma multiforme and their association with patient survival. Exp Ther Med. 2019;18:2140–52.PubMedPubMedCentral
98.
go back to reference Ongenaert M, Wisman GB, Volders HH, Koning AJ, Zee AG, van Criekinge W, et al. Discovery of DNA methylation markers in cervical cancer using relaxation ranking. BMC Med Genet. 2008;1:57. Ongenaert M, Wisman GB, Volders HH, Koning AJ, Zee AG, van Criekinge W, et al. Discovery of DNA methylation markers in cervical cancer using relaxation ranking. BMC Med Genet. 2008;1:57.
99.
go back to reference van der Zee RP, Richel O, van Noesel CJM, Novianti PW, Ciocanea-Teodorescu I, van Splunter AP, et al. Host cell deoxyribonucleic acid methylation markers for the detection of high-grade anal intraepithelial Neoplasia and anal Cancer. Clin Infect Dis. 2019;68:1110–7.PubMedCrossRef van der Zee RP, Richel O, van Noesel CJM, Novianti PW, Ciocanea-Teodorescu I, van Splunter AP, et al. Host cell deoxyribonucleic acid methylation markers for the detection of high-grade anal intraepithelial Neoplasia and anal Cancer. Clin Infect Dis. 2019;68:1110–7.PubMedCrossRef
100.
go back to reference Jin Z, Mori Y, Hamilton JP, Olaru A, Sato F, Yang J, et al. Hypermethylation of the somatostatin promoter is a common, early event in human esophageal carcinogenesis. Cancer. 2008;112:43–9.PubMedCrossRef Jin Z, Mori Y, Hamilton JP, Olaru A, Sato F, Yang J, et al. Hypermethylation of the somatostatin promoter is a common, early event in human esophageal carcinogenesis. Cancer. 2008;112:43–9.PubMedCrossRef
101.
go back to reference Zhang Z, Tang H, Wang Z, Zhang B, Liu W, Lu H, et al. MiR-185 targets the DNA methyltransferases 1 and regulates global DNA methylation in human glioma. Mol Cancer. 2011;10:124.PubMedPubMedCentralCrossRef Zhang Z, Tang H, Wang Z, Zhang B, Liu W, Lu H, et al. MiR-185 targets the DNA methyltransferases 1 and regulates global DNA methylation in human glioma. Mol Cancer. 2011;10:124.PubMedPubMedCentralCrossRef
102.
go back to reference Misawa K, Mima M, Imai A, Mochizuki D, Misawa Y, Endo S, et al. The neuropeptide genes SST, TAC1, HCRT, NPY, and GAL are powerful epigenetic biomarkers in head and neck cancer: a site-specific analysis. Clin Epigenetics. 2018;10:52.PubMedPubMedCentralCrossRef Misawa K, Mima M, Imai A, Mochizuki D, Misawa Y, Endo S, et al. The neuropeptide genes SST, TAC1, HCRT, NPY, and GAL are powerful epigenetic biomarkers in head and neck cancer: a site-specific analysis. Clin Epigenetics. 2018;10:52.PubMedPubMedCentralCrossRef
103.
go back to reference Misawa K, Mochizuki D, Imai A, Endo S, Mima M, Misawa Y, et al. Prognostic value of aberrant promoter hypermethylation of tumor-related genes in early-stage head and neck cancer. Oncotarget. 2016;7:26087–98.PubMedPubMedCentralCrossRef Misawa K, Mochizuki D, Imai A, Endo S, Mima M, Misawa Y, et al. Prognostic value of aberrant promoter hypermethylation of tumor-related genes in early-stage head and neck cancer. Oncotarget. 2016;7:26087–98.PubMedPubMedCentralCrossRef
104.
go back to reference Marek L, Hamacher A, Hansen FK, Kuna K, Gohlke H, Kassack MU, et al. Histone deacetylase (HDAC) inhibitors with a novel connecting unit linker region reveal a selectivity profile for HDAC4 and HDAC5 with improved activity against chemoresistant cancer cells. J Med Chem. 2013;56:427–36.PubMedCrossRef Marek L, Hamacher A, Hansen FK, Kuna K, Gohlke H, Kassack MU, et al. Histone deacetylase (HDAC) inhibitors with a novel connecting unit linker region reveal a selectivity profile for HDAC4 and HDAC5 with improved activity against chemoresistant cancer cells. J Med Chem. 2013;56:427–36.PubMedCrossRef
105.
go back to reference Jang S, Yu XM, Odorico S, Clark M, Jaskula-Sztul R, Schienebeck CM, et al. Novel analogs targeting histone deacetylase suppress aggressive thyroid cancer cell growth and induce re-differentiation. Cancer Gene Ther. 2015;22:410–6.PubMedCrossRef Jang S, Yu XM, Odorico S, Clark M, Jaskula-Sztul R, Schienebeck CM, et al. Novel analogs targeting histone deacetylase suppress aggressive thyroid cancer cell growth and induce re-differentiation. Cancer Gene Ther. 2015;22:410–6.PubMedCrossRef
106.
go back to reference Wang C, Henkes LM, Doughty LB, He M, Wang D, Meyer-Almes FJ, et al. Thailandepsins: bacterial products with potent histone deacetylase inhibitory activities and broad-spectrum antiproliferative activities. J Nat Prod. 2011;74:2031–8.PubMedPubMedCentralCrossRef Wang C, Henkes LM, Doughty LB, He M, Wang D, Meyer-Almes FJ, et al. Thailandepsins: bacterial products with potent histone deacetylase inhibitory activities and broad-spectrum antiproliferative activities. J Nat Prod. 2011;74:2031–8.PubMedPubMedCentralCrossRef
Metadata
Title
Epigenetic regulation of somatostatin and somatostatin receptors in neuroendocrine tumors and other types of cancer
Authors
M.J. Klomp
S.U. Dalm
M. de Jong
R.A. Feelders
J. Hofland
L.J. Hofland
Publication date
01-09-2021
Publisher
Springer US
Published in
Reviews in Endocrine and Metabolic Disorders / Issue 3/2021
Print ISSN: 1389-9155
Electronic ISSN: 1573-2606
DOI
https://doi.org/10.1007/s11154-020-09607-z

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