{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,20]],"date-time":"2026-07-20T14:21:05Z","timestamp":1784557265510,"version":"3.55.0"},"reference-count":58,"publisher":"Bioscientifica","issue":"10","content-domain":{"domain":["erc.bioscientifica.com"],"crossmark-restriction":true},"short-container-title":[],"published-print":{"date-parts":[[2023,7,26]]},"abstract":"<jats:p>\n                    Pheochromocytomas\/paragangliomas (PPGLs) are neuroendocrine tumours, mostly resulting from mutations in predisposing genes. Mutations of succinate dehydrogenase (SDH) subunit B (SDHB) are associated with high probability of metastatic disease. Since bioelectrical properties and signalling in cancer are an emerging field, we investigated the metabolic, functional and electrophysiological characteristics in human succinate dehydrogenase subunit B (SDHB)-deficient pheochromocytoma cells. These cells exhibited reduced SDH function with elevated succinate-to-fumarate ratio and reduced intracellular ATP levels. The analysis of membrane passive properties revealed a more hyperpolarized membrane potential and a lower cell capacitance of SDHB-deficient cells compared to the parental ones. These bioelectrical changes were associated with reduced proliferation and adhesion capacity of SDHB-deficient cells. Only in SDHB-deficient cells, we also observed an increased amplitude of potassium currents suggesting an activation of ATP-sensitive potassium channels (K\n                    <jats:sub>ATP<\/jats:sub>\n                    ). Indeed, exposure of the SDHB-deficient cells to glibenclamide, a specific K\n                    <jats:sub>ATP<\/jats:sub>\n                    inhibitor, or to ATP caused normalization of potassium current features and altered proliferation and adhesion. In this work, we show for the first time that reduced intracellular ATP levels in SDHB-deficient chromaffin cells impaired cell bioelectrical properties, which, in turn, are associated with an increased cell aggressiveness. Moreover, we first ever demonstrated that glibenclamide not only reduced the outward potassium currents in SDHB-deficient cells but increased their growth capacity, reduced their ability to migrate and shifted their phenotype towards one more similar to that of parental one.\n                  <\/jats:p>","DOI":"10.1530\/erc-23-0167","type":"journal-article","created":{"date-parts":[[2023,7,26]],"date-time":"2023-07-26T07:37:57Z","timestamp":1690357077000},"update-policy":"https:\/\/doi.org\/10.1530\/crossmarkpolicy-8","source":"Crossref","is-referenced-by-count":1,"title":["The aggressiveness of succinate dehydrogenase subunit B-deficient chromaffin cells is reduced when their bioelectrical properties are restored by glibenclamide"],"prefix":"10.1530","volume":"30","author":[{"given":"Francesca","family":"Amore","sequence":"first","affiliation":[{"name":"Department Experimental and Clinical Biomedical Sciences, University of Florence, Florence, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rachele","family":"Garella","sequence":"additional","affiliation":[{"name":"Department Experimental and Clinical Medicine, University of Florence, Florence, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alice","family":"Santi","sequence":"additional","affiliation":[{"name":"Department Experimental and Clinical Biomedical Sciences, University of Florence, Florence, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Daniele","family":"Guasti","sequence":"additional","affiliation":[{"name":"Department of Experimental and Clinical Medicine, Imaging Platform, University of Florence, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Serena","family":"Martinelli","sequence":"additional","affiliation":[{"name":"Department Experimental and Clinical Biomedical Sciences, University of Florence, Florence, Italy"},{"name":"Centro di Ricerca e Innovazione sulle Patologie Surrenaliche, AOU Careggi, Florence, Italy"},{"name":"ENS@T Center of Excellence, Florence, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Letizia","family":"Canu","sequence":"additional","affiliation":[{"name":"Department Experimental and Clinical Biomedical Sciences, University of Florence, Florence, Italy"},{"name":"Centro di Ricerca e Innovazione sulle Patologie Surrenaliche, AOU Careggi, Florence, Italy"},{"name":"ENS@T Center of Excellence, Florence, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Daniele","family":"Bani","sequence":"additional","affiliation":[{"name":"Department of Experimental and Clinical Medicine, Imaging Platform, University of Florence, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jiri","family":"Neuzil","sequence":"additional","affiliation":[{"name":"Institute of Biotechnology, Czech Academy of Sciences, Prague-West, Czech Republic"},{"name":"School of Pharmacy and Medical Science, Griffith University, Southport, Queensland, Australia"},{"name":"Faculty of Science and 1st Medical Faculty, Charles University, Prague, Czech Republic"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mario","family":"Maggi","sequence":"additional","affiliation":[{"name":"Department Experimental and Clinical Biomedical Sciences, University of Florence, Florence, Italy"},{"name":"Centro di Ricerca e Innovazione sulle Patologie Surrenaliche, AOU Careggi, Florence, Italy"},{"name":"ENS@T Center of Excellence, Florence, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Roberta","family":"Squecco","sequence":"additional","affiliation":[{"name":"Department Experimental and Clinical Medicine, University of Florence, Florence, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3826-2714","authenticated-orcid":true,"given":"Elena","family":"Rapizzi","sequence":"additional","affiliation":[{"name":"Department Experimental and Clinical Medicine, University of Florence, Florence, Italy"},{"name":"Centro di Ricerca e Innovazione sulle Patologie Surrenaliche, AOU Careggi, Florence, Italy"},{"name":"ENS@T Center of Excellence, Florence, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"416","reference":[{"key":"bib1","series-title":"Cancer Letters","first-page":"99","article-title":"Expression and activity of potassium ion channels in human prostate cancer","volume":"186","author":"Abdul","year":"2002","unstructured":"Abdul M & Hoosein N2002Expression and activity of potassium ion channels in human prostate cancer. Cancer Letters18699\u2013105. (https:\/\/doi.org\/10.1016\/s0304-3835(0200348-8)"},{"key":"bib2","series-title":"Anticancer Research","first-page":"3347","article-title":"Activity of potassium channel-blockers in breast cancer","volume":"23","author":"Abdul","year":"2003","unstructured":"Abdul MSanto A & Hoosein N2003Activity of potassium channel-blockers in breast cancer. Anticancer Research233347\u20133351."},{"key":"bib3","series-title":"Cancer Cell International","first-page":"23","article-title":"Abnormal expression, localization and interaction of canonical transient receptor potential ion channels in human breast cancer cell lines and tissues: a potential target for breast cancer diagnosis and therapy","volume":"9","author":"Aydar","year":"2009","unstructured":"Aydar EYeo SDjamgoz M & Palmer C2009Abnormal expression, localization and interaction of canonical transient receptor potential ion channels in human breast cancer cell lines and tissues: a potential target for breast cancer diagnosis and therapy. Cancer Cell International923. (https:\/\/doi.org\/10.1186\/1475-2867-9-23)"},{"key":"bib4","series-title":"American Journal of Physiology. Cell Physiology","first-page":"C255","article-title":"Ion channels and transporters in cancer. 1. Ion channels and cell proliferation in cancer","volume":"301","author":"Becchetti","year":"2011","unstructured":"Becchetti A2011Ion channels and transporters in cancer. 1. Ion channels and cell proliferation in cancer. American Journal of Physiology. Cell Physiology301C255\u2013C265. (https:\/\/doi.org\/10.1152\/ajpcell.00047.2011)"},{"key":"bib5","series-title":"Journal of Biological Chemistry","first-page":"21414","article-title":"The assembly factor SDHAF2 is dispensable for flavination of the catalytic subunit of mitochondrial Complex II in breast cancer cells","volume":"291","author":"Bezawork-Geleta","year":"2016","unstructured":"Bezawork-Geleta ADong LRohlena J & Neuzil J2016The assembly factor SDHAF2 is dispensable for flavination of the catalytic subunit of mitochondrial Complex II in breast cancer cells. Journal of Biological Chemistry29121414\u201321420. (https:\/\/doi.org\/10.1074\/jbc.C116.755017)"},{"key":"bib6","series-title":"Cell Cycle","first-page":"3527","article-title":"Bioelectric controls of cell proliferation: ion channels, membrane voltage and the cell cycle","volume":"8","author":"Blackiston","year":"2009","unstructured":"Blackiston DJMcLaughlin KA & Levin M2009Bioelectric controls of cell proliferation: ion channels, membrane voltage and the cell cycle. Cell Cycle83527\u20133536. (https:\/\/doi.org\/10.4161\/cc.8.21.9888)"},{"key":"bib7","series-title":"Best Practice and Research. Clinical Endocrinology and Metabolism","first-page":"101416","article-title":"An overview of 20 years of genetic studies in pheochromocytoma and paraganglioma","volume":"34","author":"Buffet","year":"2020","unstructured":"Buffet ABurnichon NFavier J & Gimenez-Roqueplo AP2020An overview of 20 years of genetic studies in pheochromocytoma and paraganglioma. Best Practice and Research. Clinical Endocrinology and Metabolism34101416. (https:\/\/doi.org\/10.1016\/j.beem.2020.101416)"},{"key":"bib8","series-title":"Brain Research. Brain Research Reviews","first-page":"282","article-title":"Targeting mitochondrial ATP-sensitive potassium channels--a novel approach to neuroprotection","volume":"46","author":"Busija","year":"2004","unstructured":"Busija DWLacza ZRajapakse NShimizu KKis BBari FDomoki F & Horiguchi T2004Targeting mitochondrial ATP-sensitive potassium channels--a novel approach to neuroprotection. Brain Research. Brain Research Reviews46282\u2013294. (https:\/\/doi.org\/10.1016\/j.brainresrev.2004.06.011)"},{"key":"bib9","series-title":"Journal of Experimental Biology","article-title":"Mitochondrial KATP channels stabilize intracellular Ca2+ during hypoxia in retinal horizontal cells of goldfish (Carassius auratus)","volume":"224","author":"Country","year":"2021","unstructured":"Country MW & Jonz MG2021Mitochondrial KATP channels stabilize intracellular Ca2+ during hypoxia in retinal horizontal cells of goldfish (Carassius auratus). Journal of Experimental Biology224. (https:\/\/doi.org\/10.1242\/jeb.242634)"},{"key":"bib10","series-title":"Endocrine-Related Cancer","first-page":"555","article-title":"The microenvironment induces collective migration in SDHB-silenced mouse pheochromocytoma spheroids","volume":"24","author":"D'Antongiovanni","year":"2017","unstructured":"D'Antongiovanni VMartinelli SRichter SCanu LGuasti DMello TRomagnoli PPacak KEisenhofer GMannelli M, 2017The microenvironment induces collective migration in SDHB-silenced mouse pheochromocytoma spheroids. Endocrine-Related Cancer24555\u2013564. (https:\/\/doi.org\/10.1530\/ERC-17-0212)"},{"key":"bib11","series-title":"Current Opinion in Oncology","first-page":"23","article-title":"An update on adult forms of hereditary pheochromocytomas and paragangliomas","volume":"33","author":"Dariane","year":"2021","unstructured":"Dariane CGoncalves JTimsit MO & Favier J2021An update on adult forms of hereditary pheochromocytomas and paragangliomas. Current Opinion in Oncology3323\u201332. (https:\/\/doi.org\/10.1097\/CCO.0000000000000694)"},{"key":"bib12","series-title":"Stem Cells","first-page":"1679","article-title":"Searching for classical brown fat in humans: development of a novel human fetal brown stem cell model","volume":"34","author":"Di Franco","year":"2016","unstructured":"Di Franco AGuasti DSquecco RMazzanti BRossi FIdrizaj EGallego-Escuredo JMVillarroya FBani DForti G, 2016Searching for classical brown fat in humans: development of a novel human fetal brown stem cell model. Stem Cells341679\u20131691. (https:\/\/doi.org\/10.1002\/stem.2336)"},{"key":"bib13","series-title":"Journal of Pathology","first-page":"480","article-title":"SDHD mutations in head and neck paragangliomas result in destabilization of complex II in the mitochondrial respiratory chain with loss of enzymatic activity and abnormal mitochondrial morphology","volume":"201","author":"Douwes Dekker","year":"2003","unstructured":"Douwes Dekker PBHogendoorn PCKuipers-Dijkshoorn NPrins FAvan Duinen SGTaschner PEvan der Mey AG & Cornelisse CJ2003SDHD mutations in head and neck paragangliomas result in destabilization of complex II in the mitochondrial respiratory chain with loss of enzymatic activity and abnormal mitochondrial morphology. Journal of Pathology201480\u2013486. (https:\/\/doi.org\/10.1002\/path.1461)"},{"key":"bib14","series-title":"Progress in Biophysics and Molecular Biology","first-page":"1","article-title":"Role of potassium channels in mitogenesis","volume":"59","author":"Dubois","year":"1993","unstructured":"Dubois JM & Rouzaire-Dubois B1993Role of potassium channels in mitogenesis. Progress in Biophysics and Molecular Biology591\u201321. (https:\/\/doi.org\/10.1016\/0079-6107(9390005-5)"},{"key":"bib15","series-title":"PLoS One","first-page":"e40949","article-title":"Warburg effect's manifestation in aggressive pheochromocytomas and paragangliomas: insights from a mouse cell model applied to human tumor tissue","volume":"7","author":"Fliedner","year":"2012","unstructured":"Fliedner SMKaludercic NJiang XSHansikova HHajkova ZSladkova JLimpuangthip ABacklund PSWesley RMartiniova L, 2012Warburg effect's manifestation in aggressive pheochromocytomas and paragangliomas: insights from a mouse cell model applied to human tumor tissue. PLoS One7e40949. (https:\/\/doi.org\/10.1371\/journal.pone.0040949)"},{"key":"bib16","series-title":"Journal of Cellular Physiology","first-page":"296","article-title":"Cytoskeleton\/stretch-activated ion channel interaction regulates myogenic differentiation of skeletal myoblasts","volume":"211","author":"Formigli","year":"2007","unstructured":"Formigli LMeacci ESassoli CSquecco RNosi DChellini FNaro FFrancini F & Zecchi-Orlandini S2007Cytoskeleton\/stretch-activated ion channel interaction regulates myogenic differentiation of skeletal myoblasts. Journal of Cellular Physiology211296\u2013306. (https:\/\/doi.org\/10.1002\/jcp.20936)"},{"key":"bib17","series-title":"Expert Opinion on Investigational Drugs","first-page":"853","article-title":"Enemies or weapons in hands: investigational anti-diabetic drug glibenclamide and cancer risk","volume":"26","author":"Gao","year":"2017","unstructured":"Gao RYang T & Xu W2017Enemies or weapons in hands: investigational anti-diabetic drug glibenclamide and cancer risk. Expert Opinion on Investigational Drugs26853\u2013864. (https:\/\/doi.org\/10.1080\/13543784.2017.1333104)"},{"key":"bib18","series-title":"PLoS One","first-page":"e65624","article-title":"Progenitor cell line (hPheo1) derived from a human pheochromocytoma tumor","volume":"8","author":"Ghayee","year":"2013","unstructured":"Ghayee HKBhagwandin VJStastny VClick ADing LHMizrachi DZou YSChari RLam WLBachoo RM, 2013Progenitor cell line (hPheo1) derived from a human pheochromocytoma tumor. PLoS One8e65624. (https:\/\/doi.org\/10.1371\/journal.pone.0065624)"},{"key":"bib19","series-title":"Histology and Histopathology","first-page":"1247","article-title":"Intermediate conductance Ca2+ activated K+ channels are expressed and functional in breast adenocarcinomas: correlation with tumour grade and metastasis status","volume":"25","author":"Haren","year":"2010","unstructured":"Haren NKhorsi HFaouzi MAhidouch ASevestre H & Ouadid-Ahidouch H2010Intermediate conductance Ca2+ activated K+ channels are expressed and functional in breast adenocarcinomas: correlation with tumour grade and metastasis status. Histology and Histopathology251247\u20131255. (https:\/\/doi.org\/10.14670\/HH-25.1247)"},{"key":"bib20","series-title":"Cancers (Basel)","article-title":"New insights on the genetics of pheochromocytoma and paraganglioma and its clinical implications","volume":"14","author":"Jhawar","year":"2022","unstructured":"Jhawar SArakawa YKumar SVarghese DKim YSRoper NElloumi FPommier YPacak K & Del Rivero J2022New insights on the genetics of pheochromocytoma and paraganglioma and its clinical implications. Cancers (Basel)14. (https:\/\/doi.org\/10.3390\/cancers14030594)"},{"key":"bib21","series-title":"Journal of Hypertension","first-page":"1443","article-title":"Genetics, diagnosis, management and future directions of research of phaeochromocytoma and paraganglioma: a position statement and consensus of the Working Group on Endocrine Hypertension of the European Society of Hypertension","volume":"38","author":"Lenders","year":"2020","unstructured":"Lenders JWMKerstens MNAmar LPrejbisz ARobledo MTaieb DPacak KCrona JZelinka TMannelli M, 2020Genetics, diagnosis, management and future directions of research of phaeochromocytoma and paraganglioma: a position statement and consensus of the Working Group on Endocrine Hypertension of the European Society of Hypertension. Journal of Hypertension381443\u20131456. (https:\/\/doi.org\/10.1097\/HJH.0000000000002438)"},{"key":"bib22","series-title":"Methods","first-page":"402","article-title":"Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method","volume":"25","author":"Livak","year":"2001","unstructured":"Livak KJ & Schmittgen TD2001Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods25402\u2013408. (https:\/\/doi.org\/10.1006\/meth.2001.1262)"},{"key":"bib23","series-title":"Journal of Clinical Endocrinology and Metabolism","first-page":"E954","article-title":"Epithelial to mesenchymal transition is activated in metastatic pheochromocytomas and paragangliomas caused by SDHB gene mutations","volume":"97","author":"Loriot","year":"2012","unstructured":"Loriot CBurnichon NGadessaud NVescovo LAmar LLib\u00e9 RBertherat JPlouin PFJeunemaitre XGimenez-Roqueplo AP, 2012Epithelial to mesenchymal transition is activated in metastatic pheochromocytomas and paragangliomas caused by SDHB gene mutations. Journal of Clinical Endocrinology and Metabolism97E954\u2013E962. (https:\/\/doi.org\/10.1210\/jc.2011-3437)"},{"key":"bib24","series-title":"Oncotarget","first-page":"32955","article-title":"Deciphering the molecular basis of invasiveness in Sdhb-deficient cells","volume":"6","author":"Loriot","year":"2015","unstructured":"Loriot CDomingues MBerger AMenara MRuel MMorin ACastro-Vega LJLetouz\u00e9 \u00c9Martinelli CBemelmans AP, 2015Deciphering the molecular basis of invasiveness in Sdhb-deficient cells. Oncotarget632955\u201332965. (https:\/\/doi.org\/10.18632\/oncotarget.5106)"},{"key":"bib25","series-title":"PLoS One","first-page":"e71716","article-title":"Exendin-4 induces cell adhesion and differentiation and counteracts the invasive potential of human neuroblastoma cells","volume":"8","author":"Luciani","year":"2013","unstructured":"Luciani PDeledda CBenvenuti SSquecco RCellai IFibbi BMarone IMGiuliani CModi GFrancini F, 2013Exendin-4 induces cell adhesion and differentiation and counteracts the invasive potential of human neuroblastoma cells. PLoS One8e71716. (https:\/\/doi.org\/10.1371\/journal.pone.0071716)"},{"key":"bib26","series-title":"Glia","first-page":"39","article-title":"Changes in ion channel expression accompany cell cycle progression of spinal cord astrocytes","volume":"30","author":"MacFarlane","year":"2000","unstructured":"MacFarlane SN & Sontheimer H2000Changes in ion channel expression accompany cell cycle progression of spinal cord astrocytes. Glia3039\u201348. (https:\/\/doi.org\/10.1002\/(sici)1098-1136(200003)30:1<39::aid-glia5>3.0.co;2-s)"},{"key":"bib27","series-title":"Journal of Biological Chemistry","first-page":"26050","article-title":"KATP channels regulate mitogenically induced proliferation in primary rat hepatocytes and human liver cell lines. Implications for liver growth control and potential therapeutic targeting","volume":"275","author":"Malhi","year":"2000","unstructured":"Malhi HIrani ANRajvanshi PSuadicani SOSpray DCMcDonald TV & Gupta S2000KATP channels regulate mitogenically induced proliferation in primary rat hepatocytes and human liver cell lines. Implications for liver growth control and potential therapeutic targeting. Journal of Biological Chemistry27526050\u201326057. (https:\/\/doi.org\/10.1074\/jbc.M001576200)"},{"key":"bib28","series-title":"CNS and Neurological Disorders Drug Targets","first-page":"130","article-title":"ATP-sensitive potassium channel subunits in neuroinflammation: novel drug targets in neurodegenerative disorders","volume":"21","author":"Maqoud","year":"2022","unstructured":"Maqoud FScala RHoxha MZappacosta B & Tricarico D2022ATP-sensitive potassium channel subunits in neuroinflammation: novel drug targets in neurodegenerative disorders. CNS and Neurological Disorders Drug Targets21130\u2013149. (https:\/\/doi.org\/10.2174\/1871527320666210119095626)"},{"key":"bib29","series-title":"Molecular and Cellular Endocrinology","first-page":"111594","article-title":"SDHB and SDHD silenced pheochromocytoma spheroids respond differently to tumour microenvironment and their aggressiveness is inhibited by impairing stroma metabolism","volume":"547","author":"Martinelli","year":"2022","unstructured":"Martinelli SRiverso MMello TAmore FParri MSimeone IMannelli MMaggi M & Rapizzi E2022SDHB and SDHD silenced pheochromocytoma spheroids respond differently to tumour microenvironment and their aggressiveness is inhibited by impairing stroma metabolism. Molecular and Cellular Endocrinology547111594. (https:\/\/doi.org\/10.1016\/j.mce.2022.111594)"},{"key":"bib30","series-title":"Frontiers in Endocrinology (Lausanne)","first-page":"589451","article-title":"Succinate mediates tumorigenic effects via Succinate Receptor 1: Potential for New Targeted Treatment Strategies in Succinate Dehydrogenase Deficient Paragangliomas","volume":"12","author":"Matlac","year":"2021","unstructured":"Matlac DMHadrava Vanova KBechmann NRichter SFolberth JGhayee HKGe GBAbunimer LWesley RAherrahrou R, 2021Succinate mediates tumorigenic effects via Succinate Receptor 1: Potential for New Targeted Treatment Strategies in Succinate Dehydrogenase Deficient Paragangliomas. Frontiers in Endocrinology (Lausanne)12589451. (https:\/\/doi.org\/10.3389\/fendo.2021.589451)"},{"key":"bib31","series-title":"Scientific Reports","first-page":"18772","article-title":"Low adherent cancer cell subpopulations are enriched in tumorigenic and metastatic epithelial-to-mesenchymal transition-induced cancer stem-like cells","volume":"6","author":"Morata-Tarifa","year":"2016","unstructured":"Morata-Tarifa CJim\u00e9nez GGarc\u00eda MAEntrena JMGri\u00f1\u00e1n-Lis\u00f3n CAguilera MPicon-Ruiz M & Marchal JA2016Low adherent cancer cell subpopulations are enriched in tumorigenic and metastatic epithelial-to-mesenchymal transition-induced cancer stem-like cells. Scientific Reports618772. (https:\/\/doi.org\/10.1038\/srep18772)"},{"key":"bib32","series-title":"Nature","first-page":"470","article-title":"KATP channels as molecular sensors of cellular metabolism","volume":"440","author":"Nichols","year":"2006","unstructured":"Nichols CG2006KATP channels as molecular sensors of cellular metabolism. Nature440470\u2013476. (https:\/\/doi.org\/10.1038\/nature04711)"},{"key":"bib33","series-title":"Developmental Neurobiology","first-page":"253","article-title":"Cystic fibrosis transmembrane conductance regulator modulates synaptic chloride homeostasis in motoneurons of the rat spinal cord during neonatal development","volume":"71","author":"Ostroumov","year":"2011","unstructured":"Ostroumov ASimonetti M & Nistri A2011Cystic fibrosis transmembrane conductance regulator modulates synaptic chloride homeostasis in motoneurons of the rat spinal cord during neonatal development. Developmental Neurobiology71253\u2013268. (https:\/\/doi.org\/10.1002\/dneu.20855)"},{"key":"bib34","series-title":"Trends in Cell Biology","first-page":"212","article-title":"EMT transition states during tumor progression and metastasis","volume":"29","author":"Pastushenko","year":"2019","unstructured":"Pastushenko I & Blanpain C2019EMT transition states during tumor progression and metastasis. Trends in Cell Biology29212\u2013226. (https:\/\/doi.org\/10.1016\/j.tcb.2018.12.001)"},{"key":"bib35","series-title":"EBiomedicine","first-page":"103767","article-title":"Potassium channel-driven bioelectric signalling regulates metastasis in triple-negative breast cancer","volume":"75","author":"Payne","year":"2022","unstructured":"Payne SLRam PSrinivasan DHLe TTLevin M & Oudin MJ2022Potassium channel-driven bioelectric signalling regulates metastasis in triple-negative breast cancer. EBiomedicine75103767. (https:\/\/doi.org\/10.1016\/j.ebiom.2021.103767)"},{"key":"bib36","series-title":"Biosensors and Bioelectronics","first-page":"1449","article-title":"Tracking cancer cell proliferation on a CMOS capacitance sensor chip","volume":"23","author":"Prakash","year":"2008","unstructured":"Prakash SB & Abshire P2008Tracking cancer cell proliferation on a CMOS capacitance sensor chip. Biosensors and Bioelectronics231449\u20131457. (https:\/\/doi.org\/10.1016\/j.bios.2007.12.015)."},{"key":"bib37","series-title":"Journal of General Physiology","first-page":"389","article-title":"Activation of the K(ATP) channel by Mg-nucleotide interaction with SUR1","volume":"136","author":"Proks","year":"2010","unstructured":"Proks Pde Wet H & Ashcroft FM2010Activation of the K(ATP) channel by Mg-nucleotide interaction with SUR1. Journal of General Physiology136389\u2013405. (https:\/\/doi.org\/10.1085\/jgp.201010475)"},{"key":"bib38","series-title":"Clinical Cancer Research","first-page":"3787","article-title":"Genotype-specific abnormalities in mitochondrial function associate with distinct profiles of energy metabolism and catecholamine content in pheochromocytoma and paraganglioma","volume":"19","author":"Rao","year":"2013","unstructured":"Rao JUEngelke UFRodenburg RJWevers RAPacak KEisenhofer GQin NKusters BGoudswaard AGLenders JW, 2013Genotype-specific abnormalities in mitochondrial function associate with distinct profiles of energy metabolism and catecholamine content in pheochromocytoma and paraganglioma. Clinical Cancer Research193787\u20133795. (https:\/\/doi.org\/10.1158\/1078-0432.CCR-12-3922)"},{"key":"bib39","series-title":"Hormones and Cancer","first-page":"174","article-title":"Succinate dehydrogenase subunit B mutations modify human neuroblastoma cell metabolism and proliferation","volume":"5","author":"Rapizzi","year":"2014","unstructured":"Rapizzi EErcolino TFucci RZampetti BFelici RGuasti DMorandi AGiannoni EGiach\u00e9 VBani D, 2014Succinate dehydrogenase subunit B mutations modify human neuroblastoma cell metabolism and proliferation. Hormones and Cancer5174\u2013184. (https:\/\/doi.org\/10.1007\/s12672-014-0172-3)"},{"key":"bib40","series-title":"Endocrine-Related Cancer","first-page":"409","article-title":"Role of microenvironment on neuroblastoma SK-N-AS SDHB-silenced cell metabolism and function","volume":"22","author":"Rapizzi","year":"2015","unstructured":"Rapizzi EFucci RGiannoni ECanu LRichter SCirri P & Mannelli M2015Role of microenvironment on neuroblastoma SK-N-AS SDHB-silenced cell metabolism and function. Endocrine-Related Cancer22409\u2013417. (https:\/\/doi.org\/10.1530\/ERC-14-0479)"},{"key":"bib41","series-title":"Brain Research. Developmental Brain Research","first-page":"267","article-title":"Somatostatin potentiates voltage-dependent K+ and Ca2+ channel expression induced by nerve growth factor in PC12 cells","volume":"112","author":"Rhie","year":"1999","unstructured":"Rhie DJYi SYHahn SJSim SSJo YH & Kim MS1999Somatostatin potentiates voltage-dependent K+ and Ca2+ channel expression induced by nerve growth factor in PC12 cells. Brain Research. Developmental Brain Research112267\u2013274. (https:\/\/doi.org\/10.1016\/s0165-3806(9800175-8)"},{"key":"bib42","series-title":"Journal of Clinical Endocrinology and Metabolism","first-page":"3903","article-title":"Krebs cycle metabolite profiling for identification and stratification of pheochromocytomas\/paragangliomas due to succinate dehydrogenase deficiency","volume":"99","author":"Richter","year":"2014","unstructured":"Richter SPeitzsch MRapizzi ELenders JWQin Nde Cubas AASchiavi FRao JUBeuschlein FQuinkler M, 2014Krebs cycle metabolite profiling for identification and stratification of pheochromocytomas\/paragangliomas due to succinate dehydrogenase deficiency. Journal of Clinical Endocrinology and Metabolism993903\u20133911. (https:\/\/doi.org\/10.1210\/jc.2014-2151)"},{"key":"bib43","series-title":"Cell and Tissue Research","first-page":"473","article-title":"Primary fibroblast co-culture stimulates growth and metabolism in Sdhb-impaired mouse pheochromocytoma MTT cells","volume":"374","author":"Richter","year":"2018","unstructured":"Richter SD'Antongiovanni VMartinelli SBechmann NRiverso MPoitz DMPacak KEisenhofer GMannelli M & Rapizzi E2018Primary fibroblast co-culture stimulates growth and metabolism in Sdhb-impaired mouse pheochromocytoma MTT cells. Cell and Tissue Research374473\u2013485. (https:\/\/doi.org\/10.1007\/s00441-018-2907-x)"},{"key":"bib44","series-title":"International Journal of Molecular Sciences","article-title":"Activation of RAS signalling is associated with altered cell adhesion in phaeochromocytoma","volume":"21","author":"Rossitti","year":"2020","unstructured":"Rossitti HMDutta RKLarsson CGhayee HKS\u00f6derkvist P & Gimm O2020Activation of RAS signalling is associated with altered cell adhesion in phaeochromocytoma. International Journal of Molecular Sciences21. (https:\/\/doi.org\/10.3390\/ijms21218072)"},{"key":"bib45","series-title":"American Journal of Physiology. Cell Physiology","first-page":"C160","article-title":"Role for stress fiber contraction in surface tension development and stretch-activated channel regulation in C2C12 myoblasts","volume":"295","author":"Sbrana","year":"2008","unstructured":"Sbrana FSassoli CMeacci ENosi DSquecco RPaternostro FTiribilli BZecchi-Orlandini SFrancini F & Formigli L2008Role for stress fiber contraction in surface tension development and stretch-activated channel regulation in C2C12 myoblasts. American Journal of Physiology. Cell Physiology295C160\u2013C172. (https:\/\/doi.org\/10.1152\/ajpcell.00014.2008)"},{"key":"bib46","series-title":"Food and Chemical Toxicology","first-page":"110804","article-title":"Role of ATP-sensitive potassium channels and inflammatory response of basilar artery smooth muscle cells in subarachnoid hemorrhage of rabbit and immune-modulation by shikonin","volume":"134","author":"Shi","year":"2019","unstructured":"Shi XZhen LDing HChen JZhang S & Fu Y2019Role of ATP-sensitive potassium channels and inflammatory response of basilar artery smooth muscle cells in subarachnoid hemorrhage of rabbit and immune-modulation by shikonin. Food and Chemical Toxicology134110804. (https:\/\/doi.org\/10.1016\/j.fct.2019.110804)"},{"key":"bib47","series-title":"Cells","article-title":"Platelet-rich plasma modulates gap junction functionality and connexin 43 and 26 expression during TGF-\u03b21-induced fibroblast to myofibroblast transition: clues for counteracting fibrosis","volume":"9","author":"Squecco","year":"2020","unstructured":"Squecco RChellini FIdrizaj ETani AGarella RPancani SPavan PBambi FZecchi-Orlandini S & Sassoli C2020Platelet-rich plasma modulates gap junction functionality and connexin 43 and 26 expression during TGF-\u03b21-induced fibroblast to myofibroblast transition: clues for counteracting fibrosis. Cells9. (https:\/\/doi.org\/10.3390\/cells9051199)"},{"key":"bib48","series-title":"Stem Cell Reviews and Reports","first-page":"231","article-title":"Role of membrane potential in the regulation of cell proliferation and differentiation","volume":"5","author":"Sundelacruz","year":"2009","unstructured":"Sundelacruz SLevin M & Kaplan DL2009Role of membrane potential in the regulation of cell proliferation and differentiation. Stem Cell Reviews and Reports5231\u2013246. (https:\/\/doi.org\/10.1007\/s12015-009-9080-2)"},{"key":"bib49","series-title":"International Journal of Molecular Sciences","article-title":"Loss of SDHB induces a metabolic switch in the hPheo1 cell line toward enhanced OXPHOS","volume":"23","author":"Tabebi","year":"2022","unstructured":"Tabebi MKumar Dutta RSkoglund CS\u00f6derkvist P & Gimm O2022Loss of SDHB induces a metabolic switch in the hPheo1 cell line toward enhanced OXPHOS. International Journal of Molecular Sciences23. (https:\/\/doi.org\/10.3390\/ijms23010560)"},{"key":"bib50","series-title":"Biochimica et Biophysica Acta","first-page":"1086","article-title":"Succinate, an intermediate in metabolism, signal transduction, ROS, hypoxia, and tumorigenesis","volume":"1857","author":"Tretter","year":"2016","unstructured":"Tretter LPatocs A & Chinopoulos C2016Succinate, an intermediate in metabolism, signal transduction, ROS, hypoxia, and tumorigenesis. Biochimica et Biophysica Acta18571086\u20131101. (https:\/\/doi.org\/10.1016\/j.bbabio.2016.03.012)"},{"key":"bib51","series-title":"Stem Cells and Development","first-page":"1175","article-title":"Enrichment for breast cancer cells with stem\/progenitor properties by differential adhesion","volume":"19","author":"Walia","year":"2010","unstructured":"Walia V & Elble RC2010Enrichment for breast cancer cells with stem\/progenitor properties by differential adhesion. Stem Cells and Development191175\u20131182. (https:\/\/doi.org\/10.1089\/scd.2009.0430)"},{"key":"bib52","series-title":"Frontiers in Pharmacology","first-page":"868401","article-title":"Functional regulation of KATP Channels and Mutant Insight Into Clinical Therapeutic Strategies in Cardiovascular Diseases","volume":"13","author":"Wang","year":"2022","unstructured":"Wang ZBian WYan Y & Zhang DM2022Functional regulation of KATP Channels and Mutant Insight Into Clinical Therapeutic Strategies in Cardiovascular Diseases. Frontiers in Pharmacology13868401. (https:\/\/doi.org\/10.3389\/fphar.2022.868401)"},{"key":"bib53","series-title":"Journal of General Physiology","first-page":"519","article-title":"The metabolism of tumors in the body","volume":"8","author":"Warburg","year":"1927","unstructured":"Warburg OWind F & Negelein E1927The metabolism of tumors in the body. Journal of General Physiology8519\u2013530. (https:\/\/doi.org\/10.1085\/jgp.8.6.519)"},{"key":"bib54","series-title":"Journal of Membrane Biology","first-page":"257","article-title":"Membrane potassium channels and human bladder tumor cells: II. Growth properties","volume":"161","author":"Wondergem","year":"1998","unstructured":"Wondergem RCregan MStrickler LMiller R & Suttles J1998Membrane potassium channels and human bladder tumor cells: II. Growth properties. Journal of Membrane Biology161257\u2013262. (https:\/\/doi.org\/10.1007\/s002329900332)"},{"key":"bib55","series-title":"Frontiers in Physiology","first-page":"185","article-title":"Membrane potential and cancer progression","volume":"4","author":"Yang","year":"2013","unstructured":"Yang M & Brackenbury WJ2013Membrane potential and cancer progression. Frontiers in Physiology4185. (https:\/\/doi.org\/10.3389\/fphys.2013.00185)"},{"key":"bib56","series-title":"FEBS Letters","first-page":"1504","article-title":"Suppression of cellular invasion by glybenclamide through inhibited secretion of platelet-derived growth factor in ovarian clear cell carcinoma ES-2 cells","volume":"586","author":"Yasukagawa","year":"2012","unstructured":"Yasukagawa TNiwa YSimizu S & Umezawa K2012Suppression of cellular invasion by glybenclamide through inhibited secretion of platelet-derived growth factor in ovarian clear cell carcinoma ES-2 cells. FEBS Letters5861504\u20131509. (https:\/\/doi.org\/10.1016\/j.febslet.2012.04.007)"},{"key":"bib57","series-title":"Brain Research Bulletin","first-page":"1","article-title":"Therapeutic potential of ATP-sensitive potassium channels in Parkinson's disease","volume":"169","author":"Zhao","year":"2021","unstructured":"Zhao SWang M & Ma Z2021Therapeutic potential of ATP-sensitive potassium channels in Parkinson's disease. Brain Research Bulletin1691\u20137. (https:\/\/doi.org\/10.1016\/j.brainresbull.2021.01.003)"},{"issue":"Supplement","key":"bib58","series-title":"Journal of Cancer Research and Therapeutics","first-page":"S421","article-title":"A modified method by differential adhesion and serum-free culture medium for enrichment of cancer stem cells","volume":"14","author":"Zhu","year":"2018","unstructured":"Zhu YTWang CYPang SYLei CYLuo Y & Tan WL2018A modified method by differential adhesion and serum-free culture medium for enrichment of cancer stem cells. Journal of Cancer Research and Therapeutics14(Supplement) S421\u2013S426. (https:\/\/doi.org\/10.4103\/0973-1482.174533)"}],"container-title":["Endocrine-Related Cancer"],"original-title":[],"link":[{"URL":"https:\/\/erc.bioscientifica.com\/view\/journals\/erc\/30\/10\/ERC-23-0167.xml","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/erc.bioscientifica.com\/view\/journals\/erc\/30\/10\/ERC-23-0167.xml","content-type":"text\/html","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/erc.bioscientifica.com\/view\/journals\/erc\/30\/10\/ERC-23-0167.xml","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,7,20]],"date-time":"2026-07-20T13:56:39Z","timestamp":1784555799000},"score":1,"resource":{"primary":{"URL":"http:\/\/journals.bioscientifica.com\/erc\/article\/25693"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,7,26]]},"references-count":58,"journal-issue":{"issue":"10"},"URL":"https:\/\/doi.org\/10.1530\/erc-23-0167","relation":{},"ISSN":["1351-0088","1479-6821"],"issn-type":[{"value":"1351-0088","type":"print"},{"value":"1479-6821","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,7,26]]}}}