Skip to main content
Top
Published in: Cancer Cell International 1/2020

01-12-2020 | Breast Cancer | Review

Pathological role of ion channels and transporters in the development and progression of triple-negative breast cancer

Authors: Chengli Lu, Zhiyuan Ma, Xiaoming Cheng, Huichao Wu, Biguang Tuo, Xuemei Liu, Taolang Li

Published in: Cancer Cell International | Issue 1/2020

Login to get access

Abstract

Breast cancer is a common malignancy in women. Among breast cancer types, triple-negative breast cancer (TNBC) tends to affect younger women, is prone to axillary lymph node, lung, and bone metastases; and has a high recurrence rate. Due to a lack of classic biomarkers, the currently available treatments are surgery and chemotherapy; no targeted standard treatment options are available. Therefore, it is urgent to find a novel and effective therapeutic target. As alteration of ion channels and transporters in normal mammary cells may affect cell growth, resulting in the development and progression of TNBC, ion channels and transporters may be promising new therapeutic targets for TNBC. This review summarizes ion channels and transporters related to TNBC and may provide new tumor biomarkers and help in the development of novel targeted therapies.
Literature
1.
go back to reference DeSantis CE, Ma J, Gaudet MM, Newman LA, Miller KD, Goding Sauer A, Jemal A, Siegel RL. Breast cancer statistics, 2019. CA Cancer J Clin. 2019;69(6):438–51.PubMedCrossRef DeSantis CE, Ma J, Gaudet MM, Newman LA, Miller KD, Goding Sauer A, Jemal A, Siegel RL. Breast cancer statistics, 2019. CA Cancer J Clin. 2019;69(6):438–51.PubMedCrossRef
2.
go back to reference Fitzmaurice C, Abate D, Abbasi N, Abbastabar H, Abd-Allah F, Abdel-Rahman O, Abdelalim A, Abdoli A, Abdollahpour I, Abdulle ASM, et al. Global, regional, and national cancer incidence, mortality, years of life lost, years lived with disability, and disability-adjusted life-years for 29 cancer groups, 1990 to 2017: a systematic analysis for the global burden of disease study. JAMA Oncol. 2019;5(12):1749–68.PubMedCentralCrossRefPubMed Fitzmaurice C, Abate D, Abbasi N, Abbastabar H, Abd-Allah F, Abdel-Rahman O, Abdelalim A, Abdoli A, Abdollahpour I, Abdulle ASM, et al. Global, regional, and national cancer incidence, mortality, years of life lost, years lived with disability, and disability-adjusted life-years for 29 cancer groups, 1990 to 2017: a systematic analysis for the global burden of disease study. JAMA Oncol. 2019;5(12):1749–68.PubMedCentralCrossRefPubMed
3.
go back to reference Jafari SH, Saadatpour Z, Salmaninejad A, Momeni F, Mokhtari M, Nahand JS, Rahmati M, Mirzaei H, Kianmehr M. Breast cancer diagnosis: imaging techniques and biochemical markers. J Cell Physiol. 2018;233(7):5200–13.PubMedCrossRef Jafari SH, Saadatpour Z, Salmaninejad A, Momeni F, Mokhtari M, Nahand JS, Rahmati M, Mirzaei H, Kianmehr M. Breast cancer diagnosis: imaging techniques and biochemical markers. J Cell Physiol. 2018;233(7):5200–13.PubMedCrossRef
4.
go back to reference Dai X, Li T, Bai Z, Yang Y, Liu X, Zhan J, Shi B. Breast cancer intrinsic subtype classification, clinical use and future trends. Am J Cancer Res. 2015;5(10):2929–43.PubMedPubMedCentral Dai X, Li T, Bai Z, Yang Y, Liu X, Zhan J, Shi B. Breast cancer intrinsic subtype classification, clinical use and future trends. Am J Cancer Res. 2015;5(10):2929–43.PubMedPubMedCentral
5.
go back to reference Sørlie T, Perou CM, Tibshirani R, Aas T, Geisler S, Johnsen H, Hastie T, Eisen MB, van de Rijn M, Jeffrey SS, et al. Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc Natl Acad Sci USA. 2001;98(19):10869–74.PubMedCrossRefPubMedCentral Sørlie T, Perou CM, Tibshirani R, Aas T, Geisler S, Johnsen H, Hastie T, Eisen MB, van de Rijn M, Jeffrey SS, et al. Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc Natl Acad Sci USA. 2001;98(19):10869–74.PubMedCrossRefPubMedCentral
6.
go back to reference Lehmann BD, Bauer JA, Chen X, Sanders ME, Chakravarthy AB, Shyr Y, Pietenpol JA. Identification of human triple-negative breast cancer subtypes and preclinical models for selection of targeted therapies. J Clin Invest. 2011;121(7):2750–67.PubMedPubMedCentralCrossRef Lehmann BD, Bauer JA, Chen X, Sanders ME, Chakravarthy AB, Shyr Y, Pietenpol JA. Identification of human triple-negative breast cancer subtypes and preclinical models for selection of targeted therapies. J Clin Invest. 2011;121(7):2750–67.PubMedPubMedCentralCrossRef
7.
go back to reference Burstein MD, Tsimelzon A, Poage GM, Covington KR, Contreras A, Fuqua SA, Savage MI, Osborne CK, Hilsenbeck SG, Chang JC, et al. Comprehensive genomic analysis identifies novel subtypes and targets of triple-negative breast cancer. Clin Cancer Res. 2015;21(7):1688–98.PubMedCrossRef Burstein MD, Tsimelzon A, Poage GM, Covington KR, Contreras A, Fuqua SA, Savage MI, Osborne CK, Hilsenbeck SG, Chang JC, et al. Comprehensive genomic analysis identifies novel subtypes and targets of triple-negative breast cancer. Clin Cancer Res. 2015;21(7):1688–98.PubMedCrossRef
9.
go back to reference Ciriello G, Gatza ML, Beck AH, Wilkerson MD, Rhie SK, Pastore A, Zhang H, McLellan M, Yau C, Kandoth C, et al. Comprehensive molecular portraits of invasive lobular breast cancer. Cell. 2015;163(2):506–19.PubMedPubMedCentralCrossRef Ciriello G, Gatza ML, Beck AH, Wilkerson MD, Rhie SK, Pastore A, Zhang H, McLellan M, Yau C, Kandoth C, et al. Comprehensive molecular portraits of invasive lobular breast cancer. Cell. 2015;163(2):506–19.PubMedPubMedCentralCrossRef
10.
go back to reference Ma Z, Yuan D, Cheng X, Tuo B, Liu X, Li T. Function of ion transporters in maintaining acid-base homeostasis of the mammary gland and the pathophysiological role in breast cancer. Am J Physiol Regul Integr Comp Physiol. 2020;318(1):R98-r111.PubMedCrossRef Ma Z, Yuan D, Cheng X, Tuo B, Liu X, Li T. Function of ion transporters in maintaining acid-base homeostasis of the mammary gland and the pathophysiological role in breast cancer. Am J Physiol Regul Integr Comp Physiol. 2020;318(1):R98-r111.PubMedCrossRef
11.
go back to reference Lin Y, Chang G, Wang J, Jin W, Wang L, Li H, Ma L, Li Q, Pang T. NHE1 mediates MDA-MB-231 cells invasion through the regulation of MT1-MMP. Exp Cell Res. 2011;317(14):2031–40.PubMedCrossRef Lin Y, Chang G, Wang J, Jin W, Wang L, Li H, Ma L, Li Q, Pang T. NHE1 mediates MDA-MB-231 cells invasion through the regulation of MT1-MMP. Exp Cell Res. 2011;317(14):2031–40.PubMedCrossRef
12.
go back to reference Wang J, Xu H, Wang Q, Zhang H, Lin Y, Zhang H, Li Q, Pang T. CIAPIN1 targets Na+/H+ exchanger 1 to mediate MDA-MB-231 cells’ metastasis through regulation of MMPs via ERK1/2 signaling pathway. Exp Cell Res. 2015;333(1):60–72.PubMedCrossRef Wang J, Xu H, Wang Q, Zhang H, Lin Y, Zhang H, Li Q, Pang T. CIAPIN1 targets Na+/H+ exchanger 1 to mediate MDA-MB-231 cells’ metastasis through regulation of MMPs via ERK1/2 signaling pathway. Exp Cell Res. 2015;333(1):60–72.PubMedCrossRef
13.
go back to reference Yu C, Wang Y, Peng J, Shen Q, Chen M, Tang W, Li X, Cai C, Wang B, Cai S, et al. Mitochondrial calcium uniporter as a target of microRNA-340 and promoter of metastasis via enhancing the Warburg effect. Oncotarget. 2017;8(48):83831–44.PubMedPubMedCentralCrossRef Yu C, Wang Y, Peng J, Shen Q, Chen M, Tang W, Li X, Cai C, Wang B, Cai S, et al. Mitochondrial calcium uniporter as a target of microRNA-340 and promoter of metastasis via enhancing the Warburg effect. Oncotarget. 2017;8(48):83831–44.PubMedPubMedCentralCrossRef
14.
go back to reference Alvarez-Baron CP, Jonsson P, Thomas C, Dryer SE, Williams C. The two-pore domain potassium channel KCNK5: induction by estrogen receptor alpha and role in proliferation of breast cancer cells. Mol Endocrinol. 2011;25(8):1326–36.PubMedPubMedCentralCrossRef Alvarez-Baron CP, Jonsson P, Thomas C, Dryer SE, Williams C. The two-pore domain potassium channel KCNK5: induction by estrogen receptor alpha and role in proliferation of breast cancer cells. Mol Endocrinol. 2011;25(8):1326–36.PubMedPubMedCentralCrossRef
15.
go back to reference Wang L, Zhang Y, Wu X, Yu G. Aquaporins: new targets for cancer therapy. Technol Cancer Res Treat. 2016;15(6):821–8.PubMedCrossRef Wang L, Zhang Y, Wu X, Yu G. Aquaporins: new targets for cancer therapy. Technol Cancer Res Treat. 2016;15(6):821–8.PubMedCrossRef
16.
go back to reference Nagaraju GP, Basha R, Rajitha B, Alese OB, Alam A, Pattnaik S, El-Rayes B. Aquaporins: their role in gastrointestinal malignancies. Cancer Lett. 2016;373(1):12–8.PubMedCrossRef Nagaraju GP, Basha R, Rajitha B, Alese OB, Alam A, Pattnaik S, El-Rayes B. Aquaporins: their role in gastrointestinal malignancies. Cancer Lett. 2016;373(1):12–8.PubMedCrossRef
18.
go back to reference Alistar A, Chou JW, Nagalla S, Black MA, D’Agostino R Jr, Miller LD. Dual roles for immune metagenes in breast cancer prognosis and therapy prediction. Genome Med. 2014;6(10):80.PubMedPubMedCentralCrossRef Alistar A, Chou JW, Nagalla S, Black MA, D’Agostino R Jr, Miller LD. Dual roles for immune metagenes in breast cancer prognosis and therapy prediction. Genome Med. 2014;6(10):80.PubMedPubMedCentralCrossRef
19.
go back to reference Mobasheri A, Barrett-Jolley R. Aquaporin water channels in the mammary gland: from physiology to pathophysiology and neoplasia. J Mammary Gland Biol Neoplasia. 2014;19(1):91–102.PubMedCrossRef Mobasheri A, Barrett-Jolley R. Aquaporin water channels in the mammary gland: from physiology to pathophysiology and neoplasia. J Mammary Gland Biol Neoplasia. 2014;19(1):91–102.PubMedCrossRef
20.
go back to reference Grimm SL, Rosen JM. The role of C/EBPbeta in mammary gland development and breast cancer. J Mammary Gland Biol Neoplasia. 2003;8(2):191–204.PubMedCrossRef Grimm SL, Rosen JM. The role of C/EBPbeta in mammary gland development and breast cancer. J Mammary Gland Biol Neoplasia. 2003;8(2):191–204.PubMedCrossRef
21.
go back to reference Papadopoulos MC, Saadoun S. Key roles of aquaporins in tumor biology. Biochim Biophys Acta. 2015;1848(10 Pt B):2576–83.PubMedCrossRef Papadopoulos MC, Saadoun S. Key roles of aquaporins in tumor biology. Biochim Biophys Acta. 2015;1848(10 Pt B):2576–83.PubMedCrossRef
23.
go back to reference Kasa P, Farran B, Prasad GLV, Nagaraju GP. Aquaporins in female specific cancers. Gene. 2019;700:60–4.PubMedCrossRef Kasa P, Farran B, Prasad GLV, Nagaraju GP. Aquaporins in female specific cancers. Gene. 2019;700:60–4.PubMedCrossRef
24.
go back to reference Tomita Y, Dorward H, Yool AJ, Smith E, Townsend AR, Price TJ, Hardingham JE. Role of aquaporin 1 signalling in cancer development and progression. Int J Mol Sci. 2017;18(2):299.PubMedCentralCrossRef Tomita Y, Dorward H, Yool AJ, Smith E, Townsend AR, Price TJ, Hardingham JE. Role of aquaporin 1 signalling in cancer development and progression. Int J Mol Sci. 2017;18(2):299.PubMedCentralCrossRef
25.
go back to reference Otterbach F, Callies R, Adamzik M, Kimmig R, Siffert W, Schmid KW, Bankfalvi A. Aquaporin 1 (AQP1) expression is a novel characteristic feature of a particularly aggressive subgroup of basal-like breast carcinomas. Breast Cancer Res Treat. 2010;120(1):67–76.PubMedCrossRef Otterbach F, Callies R, Adamzik M, Kimmig R, Siffert W, Schmid KW, Bankfalvi A. Aquaporin 1 (AQP1) expression is a novel characteristic feature of a particularly aggressive subgroup of basal-like breast carcinomas. Breast Cancer Res Treat. 2010;120(1):67–76.PubMedCrossRef
26.
go back to reference Shi Z, Zhang T, Luo L, Zhao H, Cheng J, Xiang J, Zhao C. Aquaporins in human breast cancer: identification and involvement in carcinogenesis of breast cancer. J Surg Oncol. 2012;106(3):267–72.PubMedCrossRef Shi Z, Zhang T, Luo L, Zhao H, Cheng J, Xiang J, Zhao C. Aquaporins in human breast cancer: identification and involvement in carcinogenesis of breast cancer. J Surg Oncol. 2012;106(3):267–72.PubMedCrossRef
27.
28.
go back to reference Eirew P, Stingl J, Raouf A, Turashvili G, Aparicio S, Emerman JT, Eaves CJ. A method for quantifying normal human mammary epithelial stem cells with in vivo regenerative ability. Nat Med. 2008;14(12):1384–9.PubMedCrossRef Eirew P, Stingl J, Raouf A, Turashvili G, Aparicio S, Emerman JT, Eaves CJ. A method for quantifying normal human mammary epithelial stem cells with in vivo regenerative ability. Nat Med. 2008;14(12):1384–9.PubMedCrossRef
29.
go back to reference Hu J, Verkman AS. Increased migration and metastatic potential of tumor cells expressing aquaporin water channels. Faseb J. 2006;20(11):1892–4.PubMedCrossRef Hu J, Verkman AS. Increased migration and metastatic potential of tumor cells expressing aquaporin water channels. Faseb J. 2006;20(11):1892–4.PubMedCrossRef
30.
go back to reference Esteva-Font C, Jin BJ, Verkman AS. Aquaporin-1 gene deletion reduces breast tumor growth and lung metastasis in tumor-producing MMTV-PyVT mice. Faseb J. 2014;28(3):1446–53.PubMedPubMedCentralCrossRef Esteva-Font C, Jin BJ, Verkman AS. Aquaporin-1 gene deletion reduces breast tumor growth and lung metastasis in tumor-producing MMTV-PyVT mice. Faseb J. 2014;28(3):1446–53.PubMedPubMedCentralCrossRef
31.
go back to reference Abreu-Rodríguez I, Sánchez Silva R, Martins AP, Soveral G, Toledo-Aral JJ, López-Barneo J, Echevarría M. Functional and transcriptional induction of aquaporin-1 gene by hypoxia; analysis of promoter and role of Hif-1α. PLoS ONE. 2011;6(12):e28385.PubMedPubMedCentralCrossRef Abreu-Rodríguez I, Sánchez Silva R, Martins AP, Soveral G, Toledo-Aral JJ, López-Barneo J, Echevarría M. Functional and transcriptional induction of aquaporin-1 gene by hypoxia; analysis of promoter and role of Hif-1α. PLoS ONE. 2011;6(12):e28385.PubMedPubMedCentralCrossRef
32.
go back to reference Palethorpe HM, Smith E, Tomita Y, Nakhjavani M, Yool AJ, Price TJ, Young JP, Townsend AR, Hardingham JE. Bacopasides I and II act in synergy to inhibit the growth, migration and invasion of breast cancer cell lines. Molecules. 2019;24(19):3539.PubMedCentralCrossRef Palethorpe HM, Smith E, Tomita Y, Nakhjavani M, Yool AJ, Price TJ, Young JP, Townsend AR, Hardingham JE. Bacopasides I and II act in synergy to inhibit the growth, migration and invasion of breast cancer cell lines. Molecules. 2019;24(19):3539.PubMedCentralCrossRef
33.
go back to reference Nakhjavani M, Palethorpe HM, Tomita Y, Smith E, Price TJ, Yool AJ, Pei JV, Townsend AR, Hardingham JE. Stereoselective anti-cancer activities of ginsenoside Rg3 on triple negative breast cancer cell models. Pharmaceuticals (Basel). 2019;12(3):117.CrossRef Nakhjavani M, Palethorpe HM, Tomita Y, Smith E, Price TJ, Yool AJ, Pei JV, Townsend AR, Hardingham JE. Stereoselective anti-cancer activities of ginsenoside Rg3 on triple negative breast cancer cell models. Pharmaceuticals (Basel). 2019;12(3):117.CrossRef
34.
go back to reference Zhu Z, Jiao L, Li T, Wang H, Wei W, Qian H. Expression of AQP3 and AQP5 as a prognostic marker in triple-negative breast cancer. Oncol Lett. 2018;16(2):2661–7.PubMedPubMedCentral Zhu Z, Jiao L, Li T, Wang H, Wei W, Qian H. Expression of AQP3 and AQP5 as a prognostic marker in triple-negative breast cancer. Oncol Lett. 2018;16(2):2661–7.PubMedPubMedCentral
35.
go back to reference Cao XC, Zhang WR, Cao WF, Liu BW, Zhang F, Zhao HM, Meng R, Zhang L, Niu RF, Hao XS, et al. Aquaporin3 is required for FGF-2-induced migration of human breast cancers. PLoS ONE. 2013;8(2):e56735.PubMedPubMedCentralCrossRef Cao XC, Zhang WR, Cao WF, Liu BW, Zhang F, Zhao HM, Meng R, Zhang L, Niu RF, Hao XS, et al. Aquaporin3 is required for FGF-2-induced migration of human breast cancers. PLoS ONE. 2013;8(2):e56735.PubMedPubMedCentralCrossRef
36.
go back to reference Arif M, Kitchen P, Conner MT, Hill EJ, Nagel D, Bill RM, Dunmore SJ, Armesilla AL, Gross S, Carmichael AR, et al. Downregulation of aquaporin 3 inhibits cellular proliferation, migration and invasion in the MDA-MB-231 breast cancer cell line. Oncol Lett. 2018;16(1):713–20.PubMedPubMedCentral Arif M, Kitchen P, Conner MT, Hill EJ, Nagel D, Bill RM, Dunmore SJ, Armesilla AL, Gross S, Carmichael AR, et al. Downregulation of aquaporin 3 inhibits cellular proliferation, migration and invasion in the MDA-MB-231 breast cancer cell line. Oncol Lett. 2018;16(1):713–20.PubMedPubMedCentral
37.
go back to reference Starborg M, Gell K, Brundell E, Höög C. The murine Ki-67 cell proliferation antigen accumulates in the nucleolar and heterochromatic regions of interphase cells and at the periphery of the mitotic chromosomes in a process essential for cell cycle progression. J Cell Sci. 1996;109(Pt 1):143–53.PubMed Starborg M, Gell K, Brundell E, Höög C. The murine Ki-67 cell proliferation antigen accumulates in the nucleolar and heterochromatic regions of interphase cells and at the periphery of the mitotic chromosomes in a process essential for cell cycle progression. J Cell Sci. 1996;109(Pt 1):143–53.PubMed
38.
go back to reference Li LT, Jiang G, Chen Q, Zheng JN. Ki67 is a promising molecular target in the diagnosis of cancer (review). Mol Med Rep. 2015;11(3):1566–72.PubMedCrossRef Li LT, Jiang G, Chen Q, Zheng JN. Ki67 is a promising molecular target in the diagnosis of cancer (review). Mol Med Rep. 2015;11(3):1566–72.PubMedCrossRef
39.
go back to reference Hug MJ, Tamada T, Bridges RJ. CFTR and bicarbonate secretion by [correction of to] epithelial cells. News Physiol Sci. 2003;18:38–42.PubMed Hug MJ, Tamada T, Bridges RJ. CFTR and bicarbonate secretion by [correction of to] epithelial cells. News Physiol Sci. 2003;18:38–42.PubMed
40.
go back to reference Shcheynikov N, Kim KH, Kim KM, Dorwart MR, Ko SB, Goto H, Naruse S, Thomas PJ, Muallem S. Dynamic control of cystic fibrosis transmembrane conductance regulator Cl(-)/HCO3(-) selectivity by external Cl(-). J Biol Chem. 2004;279(21):21857–65.PubMedCrossRef Shcheynikov N, Kim KH, Kim KM, Dorwart MR, Ko SB, Goto H, Naruse S, Thomas PJ, Muallem S. Dynamic control of cystic fibrosis transmembrane conductance regulator Cl(-)/HCO3(-) selectivity by external Cl(-). J Biol Chem. 2004;279(21):21857–65.PubMedCrossRef
41.
go back to reference Day BJ, van Heeckeren AM, Min E, Velsor LW. Role for cystic fibrosis transmembrane conductance regulator protein in a glutathione response to bronchopulmonary pseudomonas infection. Infect Immun. 2004;72(4):2045–51.PubMedPubMedCentralCrossRef Day BJ, van Heeckeren AM, Min E, Velsor LW. Role for cystic fibrosis transmembrane conductance regulator protein in a glutathione response to bronchopulmonary pseudomonas infection. Infect Immun. 2004;72(4):2045–51.PubMedPubMedCentralCrossRef
42.
go back to reference Conner GE, Wijkstrom-Frei C, Randell SH, Fernandez VE, Salathe M. The lactoperoxidase system links anion transport to host defense in cystic fibrosis. FEBS Lett. 2007;581(2):271–8.PubMedCrossRef Conner GE, Wijkstrom-Frei C, Randell SH, Fernandez VE, Salathe M. The lactoperoxidase system links anion transport to host defense in cystic fibrosis. FEBS Lett. 2007;581(2):271–8.PubMedCrossRef
43.
go back to reference LeSimple P, Liao J, Robert R, Gruenert DC, Hanrahan JW. Cystic fibrosis transmembrane conductance regulator trafficking modulates the barrier function of airway epithelial cell monolayers. J Physiol. 2010;588(Pt 8):1195–209.PubMedPubMedCentralCrossRef LeSimple P, Liao J, Robert R, Gruenert DC, Hanrahan JW. Cystic fibrosis transmembrane conductance regulator trafficking modulates the barrier function of airway epithelial cell monolayers. J Physiol. 2010;588(Pt 8):1195–209.PubMedPubMedCentralCrossRef
44.
go back to reference Peng X, Wu Z, Yu L, Li J, Xu W, Chan HC, Zhang Y, Hu L. Overexpression of cystic fibrosis transmembrane conductance regulator (CFTR) is associated with human cervical cancer malignancy, progression and prognosis. Gynecol Oncol. 2012;125(2):470–6.PubMedCrossRef Peng X, Wu Z, Yu L, Li J, Xu W, Chan HC, Zhang Y, Hu L. Overexpression of cystic fibrosis transmembrane conductance regulator (CFTR) is associated with human cervical cancer malignancy, progression and prognosis. Gynecol Oncol. 2012;125(2):470–6.PubMedCrossRef
45.
go back to reference Sun TT, Wang Y, Cheng H, Xiao HZ, Xiang JJ, Zhang JT, Yu SB, Martin TA, Ye L, Tsang LL, et al. Disrupted interaction between CFTR and AF-6/afadin aggravates malignant phenotypes of colon cancer. Biochim Biophys Acta. 2014;1843(3):618–28.PubMedCrossRef Sun TT, Wang Y, Cheng H, Xiao HZ, Xiang JJ, Zhang JT, Yu SB, Martin TA, Ye L, Tsang LL, et al. Disrupted interaction between CFTR and AF-6/afadin aggravates malignant phenotypes of colon cancer. Biochim Biophys Acta. 2014;1843(3):618–28.PubMedCrossRef
46.
go back to reference Xie C, Jiang XH, Zhang JT, Sun TT, Dong JD, Sanders AJ, Diao RY, Wang Y, Fok KL, Tsang LL, et al. CFTR suppresses tumor progression through miR-193b targeting urokinase plasminogen activator (uPA) in prostate cancer. Oncogene. 2013;32(18):2282–91, 91.e1-7.PubMedCrossRef Xie C, Jiang XH, Zhang JT, Sun TT, Dong JD, Sanders AJ, Diao RY, Wang Y, Fok KL, Tsang LL, et al. CFTR suppresses tumor progression through miR-193b targeting urokinase plasminogen activator (uPA) in prostate cancer. Oncogene. 2013;32(18):2282–91, 91.e1-7.PubMedCrossRef
47.
go back to reference Zhang JT, Jiang XH, Xie C, Cheng H, Da Dong J, Wang Y, Fok KL, Zhang XH, Sun TT, Tsang LL, et al. Downregulation of CFTR promotes epithelial-to-mesenchymal transition and is associated with poor prognosis of breast cancer. Biochim Biophys Acta. 2013;1833(12):2961–9.PubMedCrossRef Zhang JT, Jiang XH, Xie C, Cheng H, Da Dong J, Wang Y, Fok KL, Zhang XH, Sun TT, Tsang LL, et al. Downregulation of CFTR promotes epithelial-to-mesenchymal transition and is associated with poor prognosis of breast cancer. Biochim Biophys Acta. 2013;1833(12):2961–9.PubMedCrossRef
48.
go back to reference Turashvili G, Bouchal J, Baumforth K, Wei W, Dziechciarkova M, Ehrmann J, Klein J, Fridman E, Skarda J, Srovnal J, et al. Novel markers for differentiation of lobular and ductal invasive breast carcinomas by laser microdissection and microarray analysis. BMC Cancer. 2007;7:55.PubMedPubMedCentralCrossRef Turashvili G, Bouchal J, Baumforth K, Wei W, Dziechciarkova M, Ehrmann J, Klein J, Fridman E, Skarda J, Srovnal J, et al. Novel markers for differentiation of lobular and ductal invasive breast carcinomas by laser microdissection and microarray analysis. BMC Cancer. 2007;7:55.PubMedPubMedCentralCrossRef
49.
go back to reference Prulière-Escabasse V, Fanen P, Dazy AC, Lechapt-Zalcman E, Rideau D, Edelman A, Escudier E, Coste A. TGF-beta 1 downregulates CFTR expression and function in nasal polyps of non-CF patients. Am J Physiol Lung Cell Mol Physiol. 2005;288(1):L77–83.PubMedCrossRef Prulière-Escabasse V, Fanen P, Dazy AC, Lechapt-Zalcman E, Rideau D, Edelman A, Escudier E, Coste A. TGF-beta 1 downregulates CFTR expression and function in nasal polyps of non-CF patients. Am J Physiol Lung Cell Mol Physiol. 2005;288(1):L77–83.PubMedCrossRef
50.
go back to reference Howe KL, Wang A, Hunter MM, Stanton BA, McKay DM. TGFbeta down-regulation of the CFTR: a means to limit epithelial chloride secretion. Exp Cell Res. 2004;298(2):473–84.PubMedCrossRef Howe KL, Wang A, Hunter MM, Stanton BA, McKay DM. TGFbeta down-regulation of the CFTR: a means to limit epithelial chloride secretion. Exp Cell Res. 2004;298(2):473–84.PubMedCrossRef
51.
go back to reference Sandoval J, Esteller M. Cancer epigenomics: beyond genomics. Curr Opin Genet Dev. 2012;22(1):50–5.PubMedCrossRef Sandoval J, Esteller M. Cancer epigenomics: beyond genomics. Curr Opin Genet Dev. 2012;22(1):50–5.PubMedCrossRef
52.
go back to reference Liu K, Dong F, Gao H, Guo Y, Li H, Yang F, Zhao P, Dai Y, Wang J, Zhou W, et al. Promoter hypermethylation of the CFTR gene as a novel diagnostic and prognostic marker of breast cancer. Cell Biol Int. 2020;44(2):603–9.PubMedCrossRef Liu K, Dong F, Gao H, Guo Y, Li H, Yang F, Zhao P, Dai Y, Wang J, Zhou W, et al. Promoter hypermethylation of the CFTR gene as a novel diagnostic and prognostic marker of breast cancer. Cell Biol Int. 2020;44(2):603–9.PubMedCrossRef
53.
go back to reference Sabirzhanova I, Boinot C, Guggino WB, Cebotaru L. Syntaxin 8 and the Endoplasmic Reticulum Processing of ∆F508-CFTR. Cell Physiol Biochem. 2018;51(3):1489–99.PubMedCrossRef Sabirzhanova I, Boinot C, Guggino WB, Cebotaru L. Syntaxin 8 and the Endoplasmic Reticulum Processing of ∆F508-CFTR. Cell Physiol Biochem. 2018;51(3):1489–99.PubMedCrossRef
54.
go back to reference Southey MC, Batten L, Andersen CR, McCredie MR, Giles GG, Dite G, Hopper JL, Venter DJ. CFTR deltaF508 carrier status, risk of breast cancer before the age of 40 and histological grading in a population-based case-control study. Int J Cancer. 1998;79(5):487–9.PubMedCrossRef Southey MC, Batten L, Andersen CR, McCredie MR, Giles GG, Dite G, Hopper JL, Venter DJ. CFTR deltaF508 carrier status, risk of breast cancer before the age of 40 and histological grading in a population-based case-control study. Int J Cancer. 1998;79(5):487–9.PubMedCrossRef
55.
go back to reference Abeyrathne PD, Chami M, Stahlberg H. Biochemical and biophysical approaches to study the structure and function of the chloride channel (ClC) family of proteins. Biochimie. 2016;128–129:154–62.PubMedCrossRef Abeyrathne PD, Chami M, Stahlberg H. Biochemical and biophysical approaches to study the structure and function of the chloride channel (ClC) family of proteins. Biochimie. 2016;128–129:154–62.PubMedCrossRef
57.
go back to reference Stölting G, Fischer M, Fahlke C. CLC channel function and dysfunction in health and disease. Front Physiol. 2014;5:378.PubMedPubMedCentral Stölting G, Fischer M, Fahlke C. CLC channel function and dysfunction in health and disease. Front Physiol. 2014;5:378.PubMedPubMedCentral
58.
go back to reference Guzman RE, Grieschat M, Fahlke C, Alekov AK. ClC-3 is an intracellular chloride/proton exchanger with large voltage-dependent nonlinear capacitance. ACS Chem Neurosci. 2013;4(6):994–1003.PubMedPubMedCentralCrossRef Guzman RE, Grieschat M, Fahlke C, Alekov AK. ClC-3 is an intracellular chloride/proton exchanger with large voltage-dependent nonlinear capacitance. ACS Chem Neurosci. 2013;4(6):994–1003.PubMedPubMedCentralCrossRef
59.
go back to reference Zheng Y, Chen Z, Gu Z, Yang X, Yu M, Zhao C, Lin J, Xu P, Zhu L, Jacob TJC, et al. Starvation-induced autophagy is up-regulated via ROS-mediated ClC-3 chloride channel activation in the nasopharyngeal carcinoma cell line CNE-2Z. Biochem J. 2019;476(9):1323–33.PubMedCrossRef Zheng Y, Chen Z, Gu Z, Yang X, Yu M, Zhao C, Lin J, Xu P, Zhu L, Jacob TJC, et al. Starvation-induced autophagy is up-regulated via ROS-mediated ClC-3 chloride channel activation in the nasopharyngeal carcinoma cell line CNE-2Z. Biochem J. 2019;476(9):1323–33.PubMedCrossRef
60.
go back to reference Zhou FM, Huang YY, Tian T, Li XY, Tang YB. Knockdown of Chloride Channel-3 Inhibits Breast Cancer Growth In Vitro and In Vivo. J Breast Cancer. 2018;21(2):103–11.PubMedPubMedCentralCrossRef Zhou FM, Huang YY, Tian T, Li XY, Tang YB. Knockdown of Chloride Channel-3 Inhibits Breast Cancer Growth In Vitro and In Vivo. J Breast Cancer. 2018;21(2):103–11.PubMedPubMedCentralCrossRef
61.
go back to reference Yang H, Ma L, Wang Y, Zuo W, Li B, Yang Y, Chen Y, Chen L, Wang L, Zhu L. Activation of ClC-3 chloride channel by 17β-estradiol relies on the estrogen receptor α expression in breast cancer. J Cell Physiol. 2018;233(2):1071–81.PubMedCrossRef Yang H, Ma L, Wang Y, Zuo W, Li B, Yang Y, Chen Y, Chen L, Wang L, Zhu L. Activation of ClC-3 chloride channel by 17β-estradiol relies on the estrogen receptor α expression in breast cancer. J Cell Physiol. 2018;233(2):1071–81.PubMedCrossRef
62.
go back to reference Cross BM, Breitwieser GE, Reinhardt TA, Rao R. Cellular calcium dynamics in lactation and breast cancer: from physiology to pathology. Am J Physiol Cell Physiol. 2014;306(6):C515-26.PubMedCrossRef Cross BM, Breitwieser GE, Reinhardt TA, Rao R. Cellular calcium dynamics in lactation and breast cancer: from physiology to pathology. Am J Physiol Cell Physiol. 2014;306(6):C515-26.PubMedCrossRef
63.
go back to reference Cui C, Merritt R, Fu L, Pan Z. Targeting calcium signaling in cancer therapy. Acta Pharm Sin B. 2017;7(1):3–17.PubMedCrossRef Cui C, Merritt R, Fu L, Pan Z. Targeting calcium signaling in cancer therapy. Acta Pharm Sin B. 2017;7(1):3–17.PubMedCrossRef
64.
go back to reference Smedler E, Uhlén P. Frequency decoding of calcium oscillations. Biochim Biophys Acta. 2014;1840(3):964–9.PubMedCrossRef Smedler E, Uhlén P. Frequency decoding of calcium oscillations. Biochim Biophys Acta. 2014;1840(3):964–9.PubMedCrossRef
65.
go back to reference Papp B, Brouland JP. Altered endoplasmic reticulum calcium pump expression during breast tumorigenesis. Breast Cancer. 2011;5:163–74.PubMedPubMedCentral Papp B, Brouland JP. Altered endoplasmic reticulum calcium pump expression during breast tumorigenesis. Breast Cancer. 2011;5:163–74.PubMedPubMedCentral
66.
go back to reference Cross BM, Hack A, Reinhardt TA, Rao R. SPCA2 regulates Orai1 trafficking and store independent Ca2 + entry in a model of lactation. PLoS One. 2013;8(6):e67348.PubMedPubMedCentralCrossRef Cross BM, Hack A, Reinhardt TA, Rao R. SPCA2 regulates Orai1 trafficking and store independent Ca2 + entry in a model of lactation. PLoS One. 2013;8(6):e67348.PubMedPubMedCentralCrossRef
67.
go back to reference Marchi S, Pinton P. Alterations of calcium homeostasis in cancer cells. Curr Opin Pharmacol. 2016;29:1–6.PubMedCrossRef Marchi S, Pinton P. Alterations of calcium homeostasis in cancer cells. Curr Opin Pharmacol. 2016;29:1–6.PubMedCrossRef
68.
go back to reference O’Grady S, Morgan MP. Calcium transport and signalling in breast cancer: Functional and prognostic significance. Semin Cancer Biol. 2019. O’Grady S, Morgan MP. Calcium transport and signalling in breast cancer: Functional and prognostic significance. Semin Cancer Biol. 2019.
69.
go back to reference Makena MR, Rao R. Subtype specific targeting of calcium signaling in breast cancer. Cell Calcium. 2020;85:102109.PubMedCrossRef Makena MR, Rao R. Subtype specific targeting of calcium signaling in breast cancer. Cell Calcium. 2020;85:102109.PubMedCrossRef
70.
go back to reference Ong EC, Nesin V, Long CL, Bai CX, Guz JL, Ivanov IP, Abramowitz J, Birnbaumer L, Humphrey MB, Tsiokas L. A TRPC1 protein-dependent pathway regulates osteoclast formation and function. J Biol Chem. 2013;288(31):22219–32.PubMedPubMedCentralCrossRef Ong EC, Nesin V, Long CL, Bai CX, Guz JL, Ivanov IP, Abramowitz J, Birnbaumer L, Humphrey MB, Tsiokas L. A TRPC1 protein-dependent pathway regulates osteoclast formation and function. J Biol Chem. 2013;288(31):22219–32.PubMedPubMedCentralCrossRef
71.
go back to reference Motiani RK, Abdullaev IF, Trebak M. A novel native store-operated calcium channel encoded by Orai3: selective requirement of Orai3 versus Orai1 in estrogen receptor-positive versus estrogen receptor-negative breast cancer cells. J Biol Chem. 2010;285(25):19173–83.PubMedPubMedCentralCrossRef Motiani RK, Abdullaev IF, Trebak M. A novel native store-operated calcium channel encoded by Orai3: selective requirement of Orai3 versus Orai1 in estrogen receptor-positive versus estrogen receptor-negative breast cancer cells. J Biol Chem. 2010;285(25):19173–83.PubMedPubMedCentralCrossRef
72.
go back to reference McAndrew D, Grice DM, Peters AA, Davis FM, Stewart T, Rice M, Smart CE, Brown MA, Kenny PA, Roberts-Thomson SJ, et al. ORAI1-mediated calcium influx in lactation and in breast cancer. Mol Cancer Ther. 2011;10(3):448–60.PubMedCrossRef McAndrew D, Grice DM, Peters AA, Davis FM, Stewart T, Rice M, Smart CE, Brown MA, Kenny PA, Roberts-Thomson SJ, et al. ORAI1-mediated calcium influx in lactation and in breast cancer. Mol Cancer Ther. 2011;10(3):448–60.PubMedCrossRef
73.
go back to reference Yang Y, Jiang Z, Wang B, Chang L, Liu J, Zhang L, Gu L. Expression of STIM1 is associated with tumor aggressiveness and poor prognosis in breast cancer. Pathol Res Pract. 2017;213(9):1043–7.PubMedCrossRef Yang Y, Jiang Z, Wang B, Chang L, Liu J, Zhang L, Gu L. Expression of STIM1 is associated with tumor aggressiveness and poor prognosis in breast cancer. Pathol Res Pract. 2017;213(9):1043–7.PubMedCrossRef
74.
go back to reference Liu X, Wang T, Wang Y, Chen Z, Hua D, Yao X, Ma X, Zhang P. Orai1 is critical for Notch-driven aggressiveness under hypoxic conditions in triple-negative breast cancers. Biochim Biophys Acta Mol Basis Dis. 2018;1864(4 Pt A):975–86.PubMedCrossRef Liu X, Wang T, Wang Y, Chen Z, Hua D, Yao X, Ma X, Zhang P. Orai1 is critical for Notch-driven aggressiveness under hypoxic conditions in triple-negative breast cancers. Biochim Biophys Acta Mol Basis Dis. 2018;1864(4 Pt A):975–86.PubMedCrossRef
75.
go back to reference Mognol GP, Carneiro FR, Robbs BK, Faget DV, Viola JP. Cell cycle and apoptosis regulation by NFAT transcription factors: new roles for an old player. Cell Death Dis. 2016;7(4):e2199.PubMedPubMedCentralCrossRef Mognol GP, Carneiro FR, Robbs BK, Faget DV, Viola JP. Cell cycle and apoptosis regulation by NFAT transcription factors: new roles for an old player. Cell Death Dis. 2016;7(4):e2199.PubMedPubMedCentralCrossRef
76.
go back to reference Yang S, Zhang JJ, Huang XY. Orai1 and STIM1 are critical for breast tumor cell migration and metastasis. Cancer Cell. 2009;15(2):124–34.PubMedCrossRef Yang S, Zhang JJ, Huang XY. Orai1 and STIM1 are critical for breast tumor cell migration and metastasis. Cancer Cell. 2009;15(2):124–34.PubMedCrossRef
77.
go back to reference Cheng H, Wang S, Feng R. STIM1 plays an important role in TGF-β-induced suppression of breast cancer cell proliferation. Oncotarget. 2016;7(13):16866–78.PubMedPubMedCentralCrossRef Cheng H, Wang S, Feng R. STIM1 plays an important role in TGF-β-induced suppression of breast cancer cell proliferation. Oncotarget. 2016;7(13):16866–78.PubMedPubMedCentralCrossRef
78.
go back to reference Chakraborty S, Ghosh S, Banerjee B, Santra A, Adhikary A, Misra AK, Sen PC. Phemindole, a synthetic Di-indole derivative maneuvers the store operated calcium entry (SOCE) to induce potent anti-carcinogenic activity in human triple negative breast cancer cells. Front Pharmacol. 2016;7:114.PubMedPubMedCentralCrossRef Chakraborty S, Ghosh S, Banerjee B, Santra A, Adhikary A, Misra AK, Sen PC. Phemindole, a synthetic Di-indole derivative maneuvers the store operated calcium entry (SOCE) to induce potent anti-carcinogenic activity in human triple negative breast cancer cells. Front Pharmacol. 2016;7:114.PubMedPubMedCentralCrossRef
79.
go back to reference Didiasova M, Zakrzewicz D, Magdolen V, Nagaraj C, Bálint Z, Rohde M, Preissner KT, Wygrecka M. STIM1/ORAI1-mediated Ca2 + influx regulates enolase-1 exteriorization. J Biol Chem. 2015;290(19):11983–99.PubMedPubMedCentralCrossRef Didiasova M, Zakrzewicz D, Magdolen V, Nagaraj C, Bálint Z, Rohde M, Preissner KT, Wygrecka M. STIM1/ORAI1-mediated Ca2 + influx regulates enolase-1 exteriorization. J Biol Chem. 2015;290(19):11983–99.PubMedPubMedCentralCrossRef
80.
go back to reference Wuytack F, Raeymaekers L, Missiaen L. PMR1/SPCA Ca2 + pumps and the role of the Golgi apparatus as a Ca2 + store. Pflugers Arch. 2003;446(2):148–53.PubMedCrossRef Wuytack F, Raeymaekers L, Missiaen L. PMR1/SPCA Ca2 + pumps and the role of the Golgi apparatus as a Ca2 + store. Pflugers Arch. 2003;446(2):148–53.PubMedCrossRef
81.
go back to reference Dang D, Prasad H, Rao R. Secretory pathway Ca(2+) -ATPases promote in vitro microcalcifications in breast cancer cells. Mol Carcinog. 2017;56(11):2474–85.PubMedPubMedCentralCrossRef Dang D, Prasad H, Rao R. Secretory pathway Ca(2+) -ATPases promote in vitro microcalcifications in breast cancer cells. Mol Carcinog. 2017;56(11):2474–85.PubMedPubMedCentralCrossRef
82.
go back to reference Grice DM, Vetter I, Faddy HM, Kenny PA, Roberts-Thomson SJ, Monteith GR. Golgi calcium pump secretory pathway calcium ATPase 1 (SPCA1) is a key regulator of insulin-like growth factor receptor (IGF1R) processing in the basal-like breast cancer cell line MDA-MB-231. J Biol Chem. 2010;285(48):37458–66.PubMedPubMedCentralCrossRef Grice DM, Vetter I, Faddy HM, Kenny PA, Roberts-Thomson SJ, Monteith GR. Golgi calcium pump secretory pathway calcium ATPase 1 (SPCA1) is a key regulator of insulin-like growth factor receptor (IGF1R) processing in the basal-like breast cancer cell line MDA-MB-231. J Biol Chem. 2010;285(48):37458–66.PubMedPubMedCentralCrossRef
83.
go back to reference Bruchim I, Attias Z, Werner H. Targeting the IGF1 axis in cancer proliferation. Expert Opin Ther Targets. 2009;13(10):1179–92.PubMedCrossRef Bruchim I, Attias Z, Werner H. Targeting the IGF1 axis in cancer proliferation. Expert Opin Ther Targets. 2009;13(10):1179–92.PubMedCrossRef
84.
go back to reference Hall DD, Wu Y, Domann FE, Spitz DR, Anderson ME. Mitochondrial calcium uniporter activity is dispensable for MDA-MB-231 breast carcinoma cell survival. PLoS One. 2014;9(5):e96866.PubMedPubMedCentralCrossRef Hall DD, Wu Y, Domann FE, Spitz DR, Anderson ME. Mitochondrial calcium uniporter activity is dispensable for MDA-MB-231 breast carcinoma cell survival. PLoS One. 2014;9(5):e96866.PubMedPubMedCentralCrossRef
85.
go back to reference Shi Z, Li Y, Qian X, Hu Y, Liu J, Zhang S, Zhang J. MiR-340 inhibits triple-negative breast cancer progression by reversing EZH2 mediated miRNAs dysregulated expressions. J Cancer. 2017;8(15):3037–48.PubMedPubMedCentralCrossRef Shi Z, Li Y, Qian X, Hu Y, Liu J, Zhang S, Zhang J. MiR-340 inhibits triple-negative breast cancer progression by reversing EZH2 mediated miRNAs dysregulated expressions. J Cancer. 2017;8(15):3037–48.PubMedPubMedCentralCrossRef
86.
go back to reference Tosatto A, Sommaggio R, Kummerow C, Bentham RB, Blacker TS, Berecz T, Duchen MR, Rosato A, Bogeski I, Szabadkai G, et al. The mitochondrial calcium uniporter regulates breast cancer progression via HIF-1α. EMBO Mol Med. 2016;8(5):569–85.PubMedPubMedCentralCrossRef Tosatto A, Sommaggio R, Kummerow C, Bentham RB, Blacker TS, Berecz T, Duchen MR, Rosato A, Bogeski I, Szabadkai G, et al. The mitochondrial calcium uniporter regulates breast cancer progression via HIF-1α. EMBO Mol Med. 2016;8(5):569–85.PubMedPubMedCentralCrossRef
87.
go back to reference Tang S, Wang X, Shen Q, Yang X, Yu C, Cai C, Cai G, Meng X, Zou F. Mitochondrial Ca2+ uniporter is critical for store-operated Ca2+ entry-dependent breast cancer cell migration. Biochem Biophys Res Commun. 2015;458(1):186–93.PubMedCrossRef Tang S, Wang X, Shen Q, Yang X, Yu C, Cai C, Cai G, Meng X, Zou F. Mitochondrial Ca2+ uniporter is critical for store-operated Ca2+ entry-dependent breast cancer cell migration. Biochem Biophys Res Commun. 2015;458(1):186–93.PubMedCrossRef
88.
go back to reference Peters AA, Simpson PT, Bassett JJ, Lee JM, Da Silva L, Reid LE, Song S, Parat MO, Lakhani SR, Kenny PA, et al. Calcium channel TRPV6 as a potential therapeutic target in estrogen receptor-negative breast cancer. Mol Cancer Ther. 2012;11(10):2158–68.PubMedCrossRef Peters AA, Simpson PT, Bassett JJ, Lee JM, Da Silva L, Reid LE, Song S, Parat MO, Lakhani SR, Kenny PA, et al. Calcium channel TRPV6 as a potential therapeutic target in estrogen receptor-negative breast cancer. Mol Cancer Ther. 2012;11(10):2158–68.PubMedCrossRef
89.
go back to reference Tian C, Zhu R, Zhu L, Qiu T, Cao Z, Kang T. Potassium channels: structures, diseases, and modulators. Chem Biol Drug Des. 2014;83(1):1–26.PubMedCrossRef Tian C, Zhu R, Zhu L, Qiu T, Cao Z, Kang T. Potassium channels: structures, diseases, and modulators. Chem Biol Drug Des. 2014;83(1):1–26.PubMedCrossRef
90.
go back to reference Choi M, Scholl UI, Yue P, Björklund P, Zhao B, Nelson-Williams C, Ji W, Cho Y, Patel A, Men CJ, et al. K+ channel mutations in adrenal aldosterone-producing adenomas and hereditary hypertension. Science. 2011;331(6018):768–72.PubMedPubMedCentralCrossRef Choi M, Scholl UI, Yue P, Björklund P, Zhao B, Nelson-Williams C, Ji W, Cho Y, Patel A, Men CJ, et al. K+ channel mutations in adrenal aldosterone-producing adenomas and hereditary hypertension. Science. 2011;331(6018):768–72.PubMedPubMedCentralCrossRef
91.
go back to reference Urrego D, Tomczak AP, Zahed F, Stühmer W, Pardo LA. Potassium channels in cell cycle and cell proliferation. Philos Trans R Soc Lond B Biol Sci. 2014;369(1638):20130094.PubMedPubMedCentralCrossRef Urrego D, Tomczak AP, Zahed F, Stühmer W, Pardo LA. Potassium channels in cell cycle and cell proliferation. Philos Trans R Soc Lond B Biol Sci. 2014;369(1638):20130094.PubMedPubMedCentralCrossRef
92.
go back to reference Plummer HK, Yu Q, Cakir Y, Schuller HM. Expression of inwardly rectifying potassium channels (GIRKs) and beta-adrenergic regulation of breast cancer cell lines. BMC Cancer. 2004;4:93.PubMedPubMedCentralCrossRef Plummer HK, Yu Q, Cakir Y, Schuller HM. Expression of inwardly rectifying potassium channels (GIRKs) and beta-adrenergic regulation of breast cancer cell lines. BMC Cancer. 2004;4:93.PubMedPubMedCentralCrossRef
95.
go back to reference Comes N, Serrano-Albarrás A, Capera J, Serrano-Novillo C, Condom E, Ramón YCS, Ferreres JC, Felipe A. Involvement of potassium channels in the progression of cancer to a more malignant phenotype. Biochim Biophys Acta. 2015;1848(10 Pt B):2477–92.PubMedCrossRef Comes N, Serrano-Albarrás A, Capera J, Serrano-Novillo C, Condom E, Ramón YCS, Ferreres JC, Felipe A. Involvement of potassium channels in the progression of cancer to a more malignant phenotype. Biochim Biophys Acta. 2015;1848(10 Pt B):2477–92.PubMedCrossRef
96.
go back to reference Iorio J, Meattini I, Bianchi S, Bernini M, Maragna V, Dominici L, Casella D, Vezzosi V, Orzalesi L, Nori J, et al. hERG1 channel expression associates with molecular subtypes and prognosis in breast cancer. Cancer Cell Int. 2018;18:93.PubMedPubMedCentralCrossRef Iorio J, Meattini I, Bianchi S, Bernini M, Maragna V, Dominici L, Casella D, Vezzosi V, Orzalesi L, Nori J, et al. hERG1 channel expression associates with molecular subtypes and prognosis in breast cancer. Cancer Cell Int. 2018;18:93.PubMedPubMedCentralCrossRef
97.
go back to reference Crociani O, Guasti L, Balzi M, Becchetti A, Wanke E, Olivotto M, Wymore RS, Arcangeli A. Cell cycle-dependent expression of HERG1 and HERG1B isoforms in tumor cells. J Biol Chem. 2003;278(5):2947–55.PubMedCrossRef Crociani O, Guasti L, Balzi M, Becchetti A, Wanke E, Olivotto M, Wymore RS, Arcangeli A. Cell cycle-dependent expression of HERG1 and HERG1B isoforms in tumor cells. J Biol Chem. 2003;278(5):2947–55.PubMedCrossRef
98.
go back to reference Lansu K, Gentile S. Potassium channel activation inhibits proliferation of breast cancer cells by activating a senescence program. Cell Death Dis. 2013;4(6):e652.PubMedPubMedCentralCrossRef Lansu K, Gentile S. Potassium channel activation inhibits proliferation of breast cancer cells by activating a senescence program. Cell Death Dis. 2013;4(6):e652.PubMedPubMedCentralCrossRef
99.
go back to reference Breuer EK, Fukushiro-Lopes D, Dalheim A, Burnette M, Zartman J, Kaja S, Wells C, Campo L, Curtis KJ, Romero-Moreno R, et al. Potassium channel activity controls breast cancer metastasis by affecting β-catenin signaling. Cell Death Dis. 2019;10(3):180.PubMedPubMedCentralCrossRef Breuer EK, Fukushiro-Lopes D, Dalheim A, Burnette M, Zartman J, Kaja S, Wells C, Campo L, Curtis KJ, Romero-Moreno R, et al. Potassium channel activity controls breast cancer metastasis by affecting β-catenin signaling. Cell Death Dis. 2019;10(3):180.PubMedPubMedCentralCrossRef
100.
go back to reference Fukushiro-Lopes DF, Hegel AD, Rao V, Wyatt D, Baker A, Breuer EK, Osipo C, Zartman JJ, Burnette M, Kaja S, et al. Preclinical study of a Kv11.1 potassium channel activator as antineoplastic approach for breast cancer. Oncotarget. 2018;9(3):3321–37.PubMedCrossRef Fukushiro-Lopes DF, Hegel AD, Rao V, Wyatt D, Baker A, Breuer EK, Osipo C, Zartman JJ, Burnette M, Kaja S, et al. Preclinical study of a Kv11.1 potassium channel activator as antineoplastic approach for breast cancer. Oncotarget. 2018;9(3):3321–37.PubMedCrossRef
101.
go back to reference Dookeran KA, Zhang W, Stayner L, Argos M. Associations of two-pore domain potassium channels and triple negative breast cancer subtype in The Cancer Genome Atlas: systematic evaluation of gene expression and methylation. BMC Res Notes. 2017;10(1):475.PubMedPubMedCentralCrossRef Dookeran KA, Zhang W, Stayner L, Argos M. Associations of two-pore domain potassium channels and triple negative breast cancer subtype in The Cancer Genome Atlas: systematic evaluation of gene expression and methylation. BMC Res Notes. 2017;10(1):475.PubMedPubMedCentralCrossRef
102.
go back to reference Linzell JL, Peaker M. The distribution and movements of carbon dioxide, carbonic acid and bicarbonate between blood and milk in the goat. J Physiol. 1975;244(3):771–82.PubMedPubMedCentralCrossRef Linzell JL, Peaker M. The distribution and movements of carbon dioxide, carbonic acid and bicarbonate between blood and milk in the goat. J Physiol. 1975;244(3):771–82.PubMedPubMedCentralCrossRef
103.
go back to reference Pedersen SF, Stock C. Ion channels and transporters in cancer: pathophysiology, regulation, and clinical potential. Cancer Res. 2013;73(6):1658–61.PubMedCrossRef Pedersen SF, Stock C. Ion channels and transporters in cancer: pathophysiology, regulation, and clinical potential. Cancer Res. 2013;73(6):1658–61.PubMedCrossRef
104.
go back to reference Andersen AP, Moreira JM, Pedersen SF. Interactions of ion transporters and channels with cancer cell metabolism and the tumour microenvironment. Philos Trans R Soc Lond B Biol Sci. 2014;369(1638):20130098.PubMedPubMedCentralCrossRef Andersen AP, Moreira JM, Pedersen SF. Interactions of ion transporters and channels with cancer cell metabolism and the tumour microenvironment. Philos Trans R Soc Lond B Biol Sci. 2014;369(1638):20130098.PubMedPubMedCentralCrossRef
105.
go back to reference Wakabayashi S, Hisamitsu T, Nakamura TY. Regulation of the cardiac Na+/H+ exchanger in health and disease. J Mol Cell Cardiol. 2013;61:68–76.PubMedCrossRef Wakabayashi S, Hisamitsu T, Nakamura TY. Regulation of the cardiac Na+/H+ exchanger in health and disease. J Mol Cell Cardiol. 2013;61:68–76.PubMedCrossRef
106.
go back to reference Alves C, Lee BL, Sykes BD, Fliegel L. Structural and functional analysis of the transmembrane segment pair VI and VII of the NHE1 isoform of the Na+/H + exchanger. Biochemistry. 2014;53(22):3658–70.PubMedCrossRef Alves C, Lee BL, Sykes BD, Fliegel L. Structural and functional analysis of the transmembrane segment pair VI and VII of the NHE1 isoform of the Na+/H + exchanger. Biochemistry. 2014;53(22):3658–70.PubMedCrossRef
107.
go back to reference Lee SH, Kim T, Park ES, Yang S, Jeong D, Choi Y, Rho J. NHE10, an osteoclast-specific member of the Na+/H + exchanger family, regulates osteoclast differentiation and survival [corrected]. Biochem Biophys Res Commun. 2008;369(2):320–6.PubMedCrossRef Lee SH, Kim T, Park ES, Yang S, Jeong D, Choi Y, Rho J. NHE10, an osteoclast-specific member of the Na+/H + exchanger family, regulates osteoclast differentiation and survival [corrected]. Biochem Biophys Res Commun. 2008;369(2):320–6.PubMedCrossRef
108.
go back to reference Jenkins EC Jr, Debnath S, Gundry S, Gundry S, Uyar U, Fata JE. Intracellular pH regulation by Na+/H+ exchanger-1 (NHE1) is required for growth factor-induced mammary branching morphogenesis. Dev Biol. 2012;365(1):71–81.PubMedCrossRef Jenkins EC Jr, Debnath S, Gundry S, Gundry S, Uyar U, Fata JE. Intracellular pH regulation by Na+/H+ exchanger-1 (NHE1) is required for growth factor-induced mammary branching morphogenesis. Dev Biol. 2012;365(1):71–81.PubMedCrossRef
109.
go back to reference Martin C, Pedersen SF, Schwab A, Stock C. Intracellular pH gradients in migrating cells. Am J Physiol Cell Physiol. 2011;300(3):C490-5.PubMedCrossRef Martin C, Pedersen SF, Schwab A, Stock C. Intracellular pH gradients in migrating cells. Am J Physiol Cell Physiol. 2011;300(3):C490-5.PubMedCrossRef
110.
go back to reference Reshkin SJ, Cardone RA, Harguindey S. Na+−H + exchanger, pH regulation and cancer. Recent Pat Anticancer Drug Discov. 2013;8(1):85–99.PubMedCrossRef Reshkin SJ, Cardone RA, Harguindey S. Na+−H + exchanger, pH regulation and cancer. Recent Pat Anticancer Drug Discov. 2013;8(1):85–99.PubMedCrossRef
111.
go back to reference Greco MR, Antelmi E, Busco G, Guerra L, Rubino R, Casavola V, Reshkin SJ, Cardone RA. Protease activity at invadopodial focal digestive areas is dependent on NHE1-driven acidic pHe. Oncol Rep. 2014;31(2):940–6.PubMedCrossRef Greco MR, Antelmi E, Busco G, Guerra L, Rubino R, Casavola V, Reshkin SJ, Cardone RA. Protease activity at invadopodial focal digestive areas is dependent on NHE1-driven acidic pHe. Oncol Rep. 2014;31(2):940–6.PubMedCrossRef
112.
go back to reference Amith SR, Wilkinson JM, Baksh S, Fliegel L. The Na+/H+ exchanger (NHE1) as a novel co-adjuvant target in paclitaxel therapy of triple-negative breast cancer cells. Oncotarget. 2015;6(2):1262–75.PubMedCrossRef Amith SR, Wilkinson JM, Baksh S, Fliegel L. The Na+/H+ exchanger (NHE1) as a novel co-adjuvant target in paclitaxel therapy of triple-negative breast cancer cells. Oncotarget. 2015;6(2):1262–75.PubMedCrossRef
113.
go back to reference Amith SR, Wilkinson JM, Fliegel L. Assessing Na(+)/H(+) exchange and cell effector functionality in metastatic breast cancer. Biochim Open. 2016;2:16–23.PubMedPubMedCentralCrossRef Amith SR, Wilkinson JM, Fliegel L. Assessing Na(+)/H(+) exchange and cell effector functionality in metastatic breast cancer. Biochim Open. 2016;2:16–23.PubMedPubMedCentralCrossRef
114.
go back to reference Andersen AP, Flinck M, Oernbo EK, Pedersen NB, Viuff BM, Pedersen SF. Roles of acid-extruding ion transporters in regulation of breast cancer cell growth in a 3-dimensional microenvironment. Mol Cancer. 2016;15(1):45.PubMedPubMedCentralCrossRef Andersen AP, Flinck M, Oernbo EK, Pedersen NB, Viuff BM, Pedersen SF. Roles of acid-extruding ion transporters in regulation of breast cancer cell growth in a 3-dimensional microenvironment. Mol Cancer. 2016;15(1):45.PubMedPubMedCentralCrossRef
115.
go back to reference Andersen AP, Samsøe-Petersen J, Oernbo EK, Boedtkjer E, Moreira JMA, Kveiborg M, Pedersen SF. The net acid extruders NHE1, NBCn1 and MCT4 promote mammary tumor growth through distinct but overlapping mechanisms. Int J Cancer. 2018;142(12):2529–42.PubMedCrossRef Andersen AP, Samsøe-Petersen J, Oernbo EK, Boedtkjer E, Moreira JMA, Kveiborg M, Pedersen SF. The net acid extruders NHE1, NBCn1 and MCT4 promote mammary tumor growth through distinct but overlapping mechanisms. Int J Cancer. 2018;142(12):2529–42.PubMedCrossRef
116.
go back to reference Mihaila RG. A minireview on NHE1 inhibitors. A rediscovered hope in oncohematology. Biomed Pap Med Fac Univ Palacky Olomouc Czech Repub. 2015;159(4):519–26.PubMedCrossRef Mihaila RG. A minireview on NHE1 inhibitors. A rediscovered hope in oncohematology. Biomed Pap Med Fac Univ Palacky Olomouc Czech Repub. 2015;159(4):519–26.PubMedCrossRef
117.
go back to reference Harguindey S, Arranz JL, Polo Orozco JD, Rauch C, Fais S, Cardone RA, Reshkin SJ. Cariporide and other new and powerful NHE1 inhibitors as potentially selective anticancer drugs–an integral molecular/biochemical/metabolic/clinical approach after one hundred years of cancer research. J Transl Med. 2013;11:282.PubMedPubMedCentralCrossRef Harguindey S, Arranz JL, Polo Orozco JD, Rauch C, Fais S, Cardone RA, Reshkin SJ. Cariporide and other new and powerful NHE1 inhibitors as potentially selective anticancer drugs–an integral molecular/biochemical/metabolic/clinical approach after one hundred years of cancer research. J Transl Med. 2013;11:282.PubMedPubMedCentralCrossRef
118.
go back to reference Amith SR, Wilkinson JM, Fliegel L. KR-33028, a potent inhibitor of the Na(+)/H(+) exchanger NHE1, suppresses metastatic potential of triple-negative breast cancer cells. Biochem Pharmacol. 2016;118:31–9.PubMedCrossRef Amith SR, Wilkinson JM, Fliegel L. KR-33028, a potent inhibitor of the Na(+)/H(+) exchanger NHE1, suppresses metastatic potential of triple-negative breast cancer cells. Biochem Pharmacol. 2016;118:31–9.PubMedCrossRef
119.
go back to reference Parks SK, Pouyssegur J. The Na(+)/HCO3(-) Co-transporter SLC4A4 plays a role in growth and migration of colon and breast cancer cells. J Cell Physiol. 2015;230(8):1954–63.PubMedCrossRef Parks SK, Pouyssegur J. The Na(+)/HCO3(-) Co-transporter SLC4A4 plays a role in growth and migration of colon and breast cancer cells. J Cell Physiol. 2015;230(8):1954–63.PubMedCrossRef
Metadata
Title
Pathological role of ion channels and transporters in the development and progression of triple-negative breast cancer
Authors
Chengli Lu
Zhiyuan Ma
Xiaoming Cheng
Huichao Wu
Biguang Tuo
Xuemei Liu
Taolang Li
Publication date
01-12-2020
Publisher
BioMed Central
Published in
Cancer Cell International / Issue 1/2020
Electronic ISSN: 1475-2867
DOI
https://doi.org/10.1186/s12935-020-01464-9

Other articles of this Issue 1/2020

Cancer Cell International 1/2020 Go to the issue
Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras
Prof. Fabrice Barlesi
Developed by: Springer Medicine