Login Register Cart 0
Generic placeholder image

Current Medicinal Chemistry

Editor-in-Chief

ISSN (Print): 0929-8673
ISSN (Online): 1875-533X

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe Translate in Chinese
Research Article

Celecoxib and Dimethylcelecoxib Block Oxidative Phosphorylation, Epithelial-Mesenchymal Transition and Invasiveness in Breast Cancer Stem Cells

Author(s): Juan Carlos Gallardo-Pérez*, Alhelí Adán-Ladrón de Guevara, Marco Antonio García-Amezcua, Diana Xochiquetzal Robledo-Cadena, Silvia Cecilia Pacheco-Velázquez, Javier Alejandro Belmont-Díaz, Jorge Luis Vargas-Navarro, Rafael Moreno-Sánchez and Sara Rodríguez-Enríquez*

Volume 29, Issue 15, 2022

Published on: 12 January, 2022

Page: [2719 - 2735] Pages: 17

DOI: 10.2174/0929867328666211005124015

Price: $65

Abstract

Background: The major hurdles for successful cancer treatment are drug resistance and invasiveness developed by breast cancer stem cells (BCSC).

Objective: As these two processes are highly energy-dependent, the identification of the main ATP supplier required for stem cell viability may result advantageous in the design of new therapeutic strategies to deter malignant carcinomas.

Methods: The energy metabolism (glycolysis and oxidative phosphorylation, OxPhos) was systematically analyzed by assessing relevant protein contents, enzyme activities, and pathway fluxes in BCSC. Once identified as the main ATP supplier, selective energy inhibitors and canonical breast cancer drugs were used to block stem cell viability and metastatic properties.

Results: OxPhos and glycolytic protein contents, as well as HK and LDH activities were several times higher in BCSC than in their parental line, MCF-7 cells. However, CS, GDH, COX activities, and both energy metabolism pathway fluxes were significantly lower (38-86%) in BCSC than in MCF-7 cells. OxPhos was the main ATP provider (>85%) in BCSC. Accordingly, oligomycin (a specific and potent canonical OxPhos inhibitor) and other non-canonical drugs with inhibitory effect on OxPhos (celecoxib, dimethylcelecoxib) significantly decreased BCSC viability, levels of epithelial-mesenchymal transition proteins, invasiveness, and induced ROS over-production, with IC50 values ranging from 1 to 20 μM in 24 h treatment. In contrast, glycolytic inhibitors (gossypol, iodoacetic acid, 3-bromopyruvate, 2-deoxyglucose) and canonical chemotherapeutic drugs (paclitaxel, doxorubicin, cisplatin) were much less effective against BCSC viability (IC50> 100 μM).

Conclusion: These results indicated that the use of some NSAIDs may be a promising alternative therapeutic strategy to target BCSC.

Keywords: Breast cancer stem cells, celecoxib, glycolysis, oxidative phosphorylation, paclitaxel, stem cells.

« Previous Next »
[1]
Osborne, C.; Tripathy, D. Aromatase inhibitors: rationale and use in breast cancer. Annu. Rev. Med., 2005, 56, 103-116.
[http://dx.doi.org/10.1146/annurev.med.56.062804.103324] [PMID: 15660504]
[2]
Nounou, M.I.; ElAmrawy, F.; Ahmed, N.; Abdelraouf, K.; Goda, S.; Syed-Sha-Qhattal, H. Breast cancer: conventional diagnosis and treatment modalities and recent patents and technologies. Breast Cancer (Auckl.), 2015, 9(Suppl. 2), 17-34.
[http://dx.doi.org/10.4137/BCBCR.S29420] [PMID: 26462242]
[3]
Waks, A.G.; Winer, E.P. Breast cancer treatment: A review. JAMA, 2019, 321(3), 288-300.
[http://dx.doi.org/10.1001/jama.2018.19323] [PMID: 30667505]
[4]
Fillmore, C.M.; Kuperwasser, C. Human breast cancer cell lines contain stem-like cells that self-renew, give rise to phenotypically diverse progeny and survive chemotherapy. Breast Cancer Res., 2008, 10(2), R25.
[http://dx.doi.org/10.1186/bcr1982] [PMID: 18366788]
[5]
Kakarala, M.; Wicha, M.S. Implications of the cancer stem-cell hypothesis for breast cancer prevention and therapy. J. Clin. Oncol., 2008, 26(17), 2813-2820.
[http://dx.doi.org/10.1200/JCO.2008.16.3931] [PMID: 18539959]
[6]
Kong, D.; Li, Y.; Wang, Z.; Sarkar, F.H. Cancer stem cells and epithelial-to-mesenchymal transition (EMT)-phenotypic cells: Are they cousins or twins? Cancers (Basel), 2011, 3(1), 716-729.
[http://dx.doi.org/10.3390/cancers30100716] [PMID: 21643534]
[7]
Mimeault, M.; Batra, S.K. Molecular biomarkers of cancer stem/progenitor cells associated with progression, metastases, and treatment resistance of aggressive cancers. Cancer Epidemiol. Biomarkers Prev., 2014, 23(2), 234-254.
[http://dx.doi.org/10.1158/1055-9965.EPI-13-0785] [PMID: 24273063]
[8]
Ponti, D.; Costa, A.; Zaffaroni, N.; Pratesi, G.; Petrangolini, G.; Coradini, D.; Pilotti, S.; Pierotti, M.A.; Daidone, M.G. Isolation and in vitro propagation of tumorigenic breast cancer cells with stem/progenitor cell properties. Cancer Res., 2005, 65(13), 5506-5511.
[http://dx.doi.org/10.1158/0008-5472.CAN-05-0626] [PMID: 15994920]
[9]
Cojoc, M.; Mäbert, K.; Muders, M.H.; Dubrovska, A. A role for cancer stem cells in therapy resistance: cellular and molecular mechanisms. Semin. Cancer Biol., 2015, 31, 16-27.
[http://dx.doi.org/10.1016/j.semcancer.2014.06.004] [PMID: 24956577]
[10]
Rodríguez-Enríquez, S.; Hernández-Esquivel, L.; Marín-Hernández, A.; El Hafidi, M.; Gallardo-Pérez, J.C.; Hernández-Reséndiz, I.; Rodríguez-Zavala, J.S.; Pacheco-Velázquez, S.C.; Moreno-Sánchez, R. Mitochondrial free fatty acid β-oxidation supports oxidative phosphorylation and proliferation in cancer cells. Int. J. Biochem. Cell Biol., 2015, 65, 209-221.
[http://dx.doi.org/10.1016/j.biocel.2015.06.010] [PMID: 26073129]
[11]
Pritchard, R.; Rodríguez-Enríquez, S.; Pacheco-Velázquez, S.C.; Bortnik, V.; Moreno-Sánchez, R.; Ralph, S. Celecoxib inhibits mitochondrial O2 consumption, promoting ROS dependent death of murine and human metastatic cancer cells via the apoptotic signalling pathway. Biochem. Pharmacol., 2018, 154, 318-334.
[http://dx.doi.org/10.1016/j.bcp.2018.05.013] [PMID: 29800556]
[12]
Pacheco-Velázquez, S.C.; Robledo-Cadena, D.X.; Hernández-Reséndiz, I.; Gallardo-Pérez, J.C.; Moreno-Sánchez, R.; Rodríguez-Enríquez, S. Energy metabolism drugs block triple negative breast metastatic cancer cell phenotype. Mol. Pharm., 2018, 15(6), 2151-2164.
[http://dx.doi.org/10.1021/acs.molpharmaceut.8b00015] [PMID: 29746779]
[13]
Robledo-Cadena, D.X.; Gallardo-Pérez, J.C.; Dávila-Borja, V.; Pacheco-Velázquez, S.C.; Belmont-Díaz, J.A.; Ralph, S.J.; Blanco-Carpintero, B.A.; Moreno-Sánchez, R.; Rodríguez-Enríquez, S. Non-steroidal anti-inflammatory drugs increase cisplatin, paclitaxel, and doxorubicin efficacy against human cervix cancer cells. Pharmaceuticals (Basel), 2020, 13(12), 463.
[http://dx.doi.org/10.3390/ph13120463] [PMID: 33333716]
[14]
Lamb, R.; Harrison, H.; Hulit, J.; Smith, D.L.; Lisanti, M.P.; Sotgia, F. Mitochondria as new therapeutic targets for eradicating cancer stem cells: Quantitative proteomics and functional validation via MCT1/2 inhibition. Oncotarget, 2014, 5(22), 11029-11037.
[http://dx.doi.org/10.18632/oncotarget.2789] [PMID: 25415228]
[15]
Pastò, A.; Bellio, C.; Pilotto, G.; Ciminale, V.; Silic-Benussi, M.; Guzzo, G.; Rasola, A.; Frasson, C.; Nardo, G.; Zulato, E.; Nicoletto, M.O.; Manicone, M.; Indraccolo, S.; Amadori, A. Cancer stem cells from epithelial ovarian cancer patients privilege oxidative phosphorylation, and resist glucose deprivation. Oncotarget, 2014, 5(12), 4305-4319.
[http://dx.doi.org/10.18632/oncotarget.2010] [PMID: 24946808]
[16]
Vlashi, E.; Lagadec, C.; Vergnes, L.; Reue, K.; Frohnen, P.; Chan, M.; Alhiyari, Y.; Dratver, M.B.; Pajonk, F. Metabolic differences in breast cancer stem cells and differentiated progeny. Breast Cancer Res. Treat., 2014, 146(3), 525-534.
[http://dx.doi.org/10.1007/s10549-014-3051-2] [PMID: 25007966]
[17]
De Luca, A.; Fiorillo, M.; Peiris-Pagès, M.; Ozsvari, B.; Smith, D.L.; Sanchez-Alvarez, R.; Martinez-Outschoorn, U.E.; Cappello, A.R.; Pezzi, V.; Lisanti, M.P.; Sotgia, F. Mitochondrial biogenesis is required for the anchorage-independent survival and propagation of stem-like cancer cells. Oncotarget, 2015, 6(17), 14777-14795.
[http://dx.doi.org/10.18632/oncotarget.4401] [PMID: 26087310]
[18]
Zhou, Y.; Zhou, Y.; Shingu, T.; Feng, L.; Chen, Z.; Ogasawara, M.; Keating, M.J.; Kondo, S.; Huang, P. Metabolic alterations in highly tumorigenic glioblastoma cells: preference for hypoxia and high dependency on glycolysis. J. Biol. Chem., 2011, 286(37), 32843-32853.
[http://dx.doi.org/10.1074/jbc.M111.260935] [PMID: 21795717]
[19]
Emmink, B.L.; Verheem, A.; Van Houdt, W.J.; Steller, E.J.; Govaert, K.M.; Pham, T.V.; Piersma, S.R.; Borel Rinkes, I.H.; Jimenez, C.R.; Kranenburg, O. The secretome of colon cancer stem cells contains drug-metabolizing enzymes. J. Proteomics, 2013, 91, 84-96.
[http://dx.doi.org/10.1016/j.jprot.2013.06.027] [PMID: 23835434]
[20]
Ciavardelli, D.; Rossi, C.; Barcaroli, D.; Volpe, S.; Consalvo, A.; Zucchelli, M.; De Cola, A.; Scavo, E.; Carollo, R.; D’Agostino, D.; Forlì, F.; D’Aguanno, S.; Todaro, M.; Stassi, G.; Di Ilio, C.; De Laurenzi, V.; Urbani, A. Breast cancer stem cells rely on fermentative glycolysis and are sensitive to 2-deoxyglucose treatment. Cell Death Dis., 2014, 5, e1336.
[http://dx.doi.org/10.1038/cddis.2014.285] [PMID: 25032859]
[21]
Palorini, R.; Votta, G.; Balestrieri, C.; Monestiroli, A.; Olivieri, S.; Vento, R.; Chiaradonna, F. Energy metabolism characterization of a novel cancer stem cell-like line 3AB-OS. J. Cell. Biochem., 2014, 115(2), 368-379.
[http://dx.doi.org/10.1002/jcb.24671] [PMID: 24030970]
[22]
Shen, Y.A.; Wang, C.Y.; Hsieh, Y.T.; Chen, Y.J.; Wei, Y.H. Metabolic reprogramming orchestrates cancer stem cell properties in nasopharyngeal carcinoma. Cell Cycle, 2015, 14(1), 86-98.
[http://dx.doi.org/10.4161/15384101.2014.974419] [PMID: 25483072]
[23]
Ford, L.A.; Roelofs, A.J.; Anavi-Goffer, S.; Mowat, L.; Simpson, D.G.; Irving, A.J.; Rogers, M.J.; Rajnicek, A.M.; Ross, R.A. A role for L-alpha-lysophosphatidylinositol and GPR55 in the modulation of migration, orientation and polarization of human breast cancer cells. Br. J. Pharmacol., 2010, 160(3), 762-771.
[http://dx.doi.org/10.1111/j.1476-5381.2010.00743.x] [PMID: 20590578]
[24]
Brinkley, B.R.; Beall, P.T.; Wible, L.J.; Mace, M.L.; Turner, D.S.; Cailleau, R.M. Variations in cell form and cytoskeleton in human breast carcinoma cells in vitro. Cancer Res., 1980, 40(9), 3118-3129.
[PMID: 7000337]
[25]
Gallardo-Pérez, J.C.; Adán-Ladrón de Guevara, A.; Marín-Hernández, A.; Moreno-Sánchez, R.; Rodríguez-Enríquez, S. HPI/AMF inhibition halts the development of the aggressive phenotype of breast cancer stem cells. Biochim. Biophys. Acta Mol. Cell Res., 2017, 1864(10), 1679-1690.
[http://dx.doi.org/10.1016/j.bbamcr.2017.06.015] [PMID: 28648642]
[26]
Marín-Hernández, A.; Gallardo-Pérez, J.C.; López-Ramírez, S.Y.; García-García, J.D.; Rodríguez-Zavala, J.S.; Ruiz-Ramírez, L.; Gracia-Mora, I.; Zentella-Dehesa, A.; Sosa-Garrocho, M.; Macías-Silva, M.; Moreno-Sánchez, R.; Rodríguez-Enríquez, S. Casiopeina II-gly and bromo-pyruvate inhibition of tumor hexokinase, glycolysis, and oxidative phosphorylation. Arch. Toxicol., 2012, 86(5), 753-766.
[http://dx.doi.org/10.1007/s00204-012-0809-3] [PMID: 22349057]
[27]
Hernández-Reséndiz, I.; Román-Rosales, A.; García-Villa, E.; López-Macay, A.; Pineda, E.; Saavedra, E.; Gallardo-Pérez, J.C.; Alvarez-Ríos, E.; Gariglio, P.; Moreno-Sánchez, R.; Rodríguez-Enríquez, S. Dual regulation of energy metabolism by p53 in human cervix and breast cancer cells. Biochim. Biophys. Acta, 2015, 1853(12), 3266-3278.
[http://dx.doi.org/10.1016/j.bbamcr.2015.09.033] [PMID: 26434996]
[28]
Nakashima, R.A.; Paggi, M.G.; Pedersen, P.L. Contributions of glycolysis and oxidative phosphorylation to adenosine 5′-triphosphate production in AS-30D hepatoma cells. Cancer Res., 1984, 44(12 Pt 1), 5702-5706.
[PMID: 6498833]
[29]
Rodríguez-Enríquez, S.; Carreño-Fuentes, L.; Gallardo-Pérez, J.C.; Saavedra, E.; Quezada, H.; Vega, A.; Marín-Hernández, A.; Olín-Sandoval, V.; Torres-Márquez, M.E.; Moreno-Sánchez, R. Oxidative phosphorylation is impaired by prolonged hypoxia in breast and possibly in cervix carcinoma. Int. J. Biochem. Cell Biol., 2010, 42(10), 1744-1751.
[http://dx.doi.org/10.1016/j.biocel.2010.07.010] [PMID: 20654728]
[30]
Marín-Hernández, Á.; Gallardo-Pérez, J.C.; Hernández-Reséndiz, I.; Del Mazo-Monsalvo, I.; Robledo-Cadena, D.X.; Moreno-Sánchez, R.; Rodríguez-Enríquez, S. Hypoglycemia enhances epithelial-mesenchymal transition and invasiveness, and restrains the Warburg phenotype, in hypoxic HeLa cell cultures and microspheroids. J. Cell. Physiol., 2017, 232(6), 1346-1359.
[http://dx.doi.org/10.1002/jcp.25617] [PMID: 27661776]
[31]
Isnaini, I.; Permatasari, N.; Mintaroem, K.; Prihardina, B.; Widodo, M.A. Oxidants-Antioxidants Profile in the Breast Cancer Cell Line MCF-7. Asian Pac. J. Cancer Prev., 2018, 19(11), 3175-3178.
[http://dx.doi.org/10.31557/APJCP.2018.19.11.3175] [PMID: 30486606]
[32]
Rodríguez-Enríquez, S.; Pacheco-Velázquez, S.C.; Marín-Hernández, Á.; Gallardo-Pérez, J.C.; Robledo-Cadena, D.X.; Hernández-Reséndiz, I.; García-García, J.D.; Belmont-Díaz, J.; López-Marure, R.; Hernández-Esquivel, L.; Sánchez-Thomas, R.; Moreno-Sánchez, R. Resveratrol inhibits cancer cell proliferation by impairing oxidative phosphorylation and inducing oxidative stress. Toxicol. Appl. Pharmacol., 2019, 370, 65-77.
[http://dx.doi.org/10.1016/j.taap.2019.03.008] [PMID: 30878505]
[33]
Plumb, J.A. Cell sensitivity assays : the MTT assay. Methods Mol. Med., 1999, 28, 25-30.
[PMID: 21374024]
[34]
Krzywinski, M.; Altman, N.; Blainey, P. Points of significance: nested designs. For studies with hierarchical noise sources, use a nested analysis of variance approach. Nat. Methods, 2014, 11(10), 977-978.
[http://dx.doi.org/10.1038/nmeth.3137] [PMID: 25392877]
[35]
Bensaad, K.; Tsuruta, A.; Selak, M.A.; Vidal, M.N.; Nakano, K.; Bartrons, R.; Gottlieb, E.; Vousden, K.H. TIGAR, a p53-inducible regulator of glycolysis and apoptosis. Cell, 2006, 126(1), 107-120.
[http://dx.doi.org/10.1016/j.cell.2006.05.036] [PMID: 16839880]
[36]
Luo, Z.; Zang, M.; Guo, W. AMPK as a metabolic tumor suppressor: control of metabolism and cell growth. Future Oncol., 2010, 6(3), 457-470.
[http://dx.doi.org/10.2217/fon.09.174] [PMID: 20222801]
[37]
Moreno-Sánchez, R.; Saavedra, E.; Gallardo-Pérez, J.C.; Rumjanek, F.D.; Rodríguez-Enríquez, S. Understanding the cancer cell phenotype beyond the limitations of current omics analyses. FEBS J., 2016, 283(1), 54-73.
[http://dx.doi.org/10.1111/febs.13535] [PMID: 26417966]
[38]
Kramar, R.; Hohenegger, M.; Srour, A.N.; Khanakah, G. Oligomycin toxicity in intact rats. Agents Actions, 1984, 15(5-6), 660-663.
[http://dx.doi.org/10.1007/BF01966788] [PMID: 6532186]
[39]
Mikirova, N.A.; Kesari, S.; Ichim, T.E.; Riordan, N.H. Effect of Infla-Kine supplementation on the gene expression of inflammatory markers in peripheral mononuclear cells and on C-reactive protein in blood. J. Transl. Med., 2017, 15(1), 213.
[http://dx.doi.org/10.1186/s12967-017-1315-4] [PMID: 29058588]
[40]
Rodríguez-Enríquez, S.; Hernández-Esquivel, L.; Marín-Hernández, A.; Dong, L.F.; Akporiaye, E.T.; Neuzil, J.; Ralph, S.J.; Moreno-Sánchez, R. Molecular mechanism for the selective impairment of cancer mitochondrial function by a mitochondrially targeted vitamin E analogue. Biochim. Biophys. Acta, 2012, 1817(9), 1597-1607.
[http://dx.doi.org/10.1016/j.bbabio.2012.05.005] [PMID: 22627082]
[41]
Ralph, S.J.; Nozuhur, S.; ALHulais, R.A.; Rodríguez-Enríquez, S.; Moreno-Sánchez, R. Repurposing drugs as pro-oxidant redox modifiers to eliminate cancer stem cells and improve the treatment of advanced stage cancers. Med. Res. Rev., 2019, 39(6), 2397-2426.
[http://dx.doi.org/10.1002/med.21589] [PMID: 31111530]
[42]
Visvader, J.E.; Lindeman, G.J. Cancer stem cells: current status and evolving complexities. Cell Stem Cell, 2012, 10(6), 717-728.
[http://dx.doi.org/10.1016/j.stem.2012.05.007] [PMID: 22704512]
[43]
Prieto-Vila, M.; Takahashi, R.U.; Usuba, W.; Kohama, I.; Ochiya, T. Drug resistance driven by cancer stem cells and their niche. Int. J. Mol. Sci., 2017, 18(12), 2574.
[http://dx.doi.org/10.3390/ijms18122574] [PMID: 29194401]
[44]
Rabinovich, I.; Sebastião, A.P.M.; Lima, R.S.; Urban, C.A.; Junior, E.S.; Anselmi, K.F.; Elifio-Esposito, S.; De Noronha, L.; Moreno-Amaral, A.N. Cancer stem cell markers ALDH1 and CD44+/CD24- phenotype and their prognosis impact in invasive ductal carcinoma. Eur. J. Histochem., 2018, 62(3), 2943.
[http://dx.doi.org/10.4081/ejh.2018.2943] [PMID: 30362671]
[45]
Dean, M. ABC transporters, drug resistance, and cancer stem cells. J. Mammary Gland Biol. Neoplasia, 2009, 14(1), 3-9.
[http://dx.doi.org/10.1007/s10911-009-9109-9] [PMID: 19224345]
[46]
Bao, B.; Ahmad, A.; Kong, D.; Ali, S.; Azmi, A.S.; Li, Y.; Banerjee, S.; Padhye, S.; Sarkar, F.H. Hypoxia induced aggressiveness of prostate cancer cells is linked with deregulated expression of VEGF, IL-6 and miRNAs that are attenuated by CDF. PLoS One, 2012, 7(8), e43726.
[http://dx.doi.org/10.1371/journal.pone.0043726] [PMID: 22952749]
[47]
Flavahan, W.A.; Wu, Q.; Hitomi, M.; Rahim, N.; Kim, Y.; Sloan, A.E.; Weil, R.J.; Nakano, I.; Sarkaria, J.N.; Stringer, B.W.; Day, B.W.; Li, M.; Lathia, J.D.; Rich, J.N.; Hjelmeland, A.B. Brain tumor initiating cells adapt to restricted nutrition through preferential glucose uptake. Nat. Neurosci., 2013, 16(10), 1373-1382.
[http://dx.doi.org/10.1038/nn.3510] [PMID: 23995067]
[48]
Perona, R.; López-Ayllón, B.D.; de Castro Carpeño, J.; Belda-Iniesta, C. A role for cancer stem cells in drug resistance and metastasis in non-small-cell lung cancer. Clin. Transl. Oncol., 2011, 13(5), 289-293.
[http://dx.doi.org/10.1007/s12094-011-0656-3] [PMID: 21596655]
[49]
Annett, S.; Robson, T. Targeting cancer stem cells in the clinic: Current status and perspectives. Pharmacol. Ther., 2018, 187, 13-30.
[http://dx.doi.org/10.1016/j.pharmthera.2018.02.001] [PMID: 29421575]
[50]
Naujokat, C.; Laufer, S. Targeting cancer stem cells with defined compounds and drugs. J. Cancer Res. Updates, 2013, 2, 36-67.
[http://dx.doi.org/10.6000/1929-2279.2013.02.01.7]
[51]
Ghasemi, F.; Sarabi, P.Z.; Athari, S.S.; Esmaeilzadeh, A. Therapeutics strategies against cancer stem cell in breast cancer. Int. J. Biochem. Cell Biol., 2019, 109, 76-81.
[http://dx.doi.org/10.1016/j.biocel.2019.01.015] [PMID: 30772480]
[52]
Recht, A.; Gray, R.; Davidson, N.E.; Fowble, B.L.; Solin, L.J.; Cummings, F.J.; Falkson, G.; Falkson, H.C.; Taylor, S.G., IV; Tormey, D.C. Locoregional failure 10 years after mastectomy and adjuvant chemotherapy with or without tamoxifen without irradiation: experience of the Eastern Cooperative Oncology Group. J. Clin. Oncol., 1999, 17(6), 1689-1700.
[http://dx.doi.org/10.1200/JCO.1999.17.6.1689] [PMID: 10561205]
[53]
Ambili, R. Toxicities of anticancer drugs and its management. Int. J. Basic Clin. Pharmacol., 2012, 1, 2-12.
[http://dx.doi.org/10.5455/2319-2003.ijbcp000812]
[54]
Horio, A.; Fujita, T.; Hayashi, H.; Hattori, M.; Kondou, N.; Yamada, M.; Adachi, E.; Ushio, A.; Gondou, N.; Sueta, A.; Yatabe, Y.; Iwata, H. High recurrence risk and use of adjuvant trastuzumab in patients with small, HER2-positive, node-negative breast cancers. Int. J. Clin. Oncol., 2012, 17(2), 131-136.
[http://dx.doi.org/10.1007/s10147-011-0269-4] [PMID: 21681642]
[55]
Woodward, W.A.; Strom, E.A.; Tucker, S.L.; Katz, A.; McNeese, M.D.; Perkins, G.H.; Buzdar, A.U.; Hortobagyi, G.N.; Hunt, K.K.; Sahin, A.; Meric, F.; Sneige, N.; Buchholz, T.A. Locoregional recurrence after doxorubicin-based chemotherapy and postmastectomy: Implications for breast cancer patients with early-stage disease and predictors for recurrence after postmastectomy radiation. Int. J. Radiat. Oncol. Biol. Phys., 2003, 57(2), 336-344.
[http://dx.doi.org/10.1016/S0360-3016(03)00593-5] [PMID: 12957243]
[56]
Weinberg, S.E.; Chandel, N.S. Targeting mitochondria metabolism for cancer therapy. Nat. Chem. Biol., 2015, 11(1), 9-15.
[http://dx.doi.org/10.1038/nchembio.1712] [PMID: 25517383]
[57]
Rodríguez-Enríquez, S.; Marín-Hernández, A.; Gallardo-Pérez, J.C.; Carreño-Fuentes, L.; Moreno-Sánchez, R. Targeting of cancer energy metabolism. Mol. Nutr. Food Res., 2009, 53(1), 29-48.
[http://dx.doi.org/10.1002/mnfr.200700470] [PMID: 19123180]
[58]
Ashton, T.M.; McKenna, W.G.; Kunz-Schughart, L.A.; Higgins, G.S. Oxidative phosphorylation as an emerging target in cancer therapy. Clin. Cancer Res., 2018, 24(11), 2482-2490.
[http://dx.doi.org/10.1158/1078-0432.CCR-17-3070] [PMID: 29420223]
[59]
Xu, Y.; Xue, D.; Bankhead, A., III; Neamati, N. Why all the fuss about oxidative phosphorylation (OXPHOS)? J. Med. Chem., 2020, 63(23), 14276-14307.
[http://dx.doi.org/10.1021/acs.jmedchem.0c01013] [PMID: 33103432]
[60]
Whitaker-Menezes, D.; Martinez-Outschoorn, U.E.; Flomenberg, N.; Birbe, R.C.; Witkiewicz, A.K.; Howell, A.; Pavlides, S.; Tsirigos, A.; Ertel, A.; Pestell, R.G.; Broda, P.; Minetti, C.; Lisanti, M.P.; Sotgia, F. Hyperactivation of oxidative mitochondrial metabolism in epithelial cancer cells in situ: Visualizing the therapeutic effects of metformin in tumor tissue. Cell Cycle, 2011, 10(23), 4047-4064.
[http://dx.doi.org/10.4161/cc.10.23.18151] [PMID: 22134189]
[61]
Caro, P.; Kishan, A.U.; Norberg, E.; Stanley, I.A.; Chapuy, B.; Ficarro, S.B.; Polak, K.; Tondera, D.; Gounarides, J.; Yin, H.; Zhou, F.; Green, M.R.; Chen, L.; Monti, S.; Marto, J.A.; Shipp, M.A.; Danial, N.N. Metabolic signatures uncover distinct targets in molecular subsets of diffuse large B cell lymphoma. Cancer Cell, 2012, 22(4), 547-560.
[http://dx.doi.org/10.1016/j.ccr.2012.08.014] [PMID: 23079663]
[62]
Birkenmeier, K.; Dröse, S.; Wittig, I.; Winkelmann, R.; Käfer, V.; Döring, C.; Hartmann, S.; Wenz, T.; Reichert, A.S.; Brandt, U.; Hansmann, M.L. Hodgkin and Reed-Sternberg cells of classical Hodgkin lymphoma are highly dependent on oxidative phosphorylation. Int. J. Cancer, 2016, 138(9), 2231-2246.
[http://dx.doi.org/10.1002/ijc.29934] [PMID: 26595876]
[63]
Barrientos, A.; Fontanesi, F.; Díaz, F. Evaluation of the mitochondrial respiratory chain and oxidative phosphorylation system using polarography and spectrophotometric enzyme assays. Curr. Protoc. Hum. Genet., 2009, 19, 3.
[http://dx.doi.org/10.1002/0471142905.hg1903s63] [PMID: 19806590]
[64]
Zhang, J.; Nuebel, E.; Wisidagama, D.R.; Setoguchi, K.; Hong, J.S.; Van Horn, C.M.; Imam, S.S.; Vergnes, L.; Malone, C.S.; Koehler, C.M.; Teitell, M.A. Measuring energy metabolism in cultured cells, including human pluripotent stem cells and differentiated cells. Nat. Protoc., 2012, 7(6), 1068-1085.
[http://dx.doi.org/10.1038/nprot.2012.048] [PMID: 22576106]
[65]
Al-Dhfyan, A.; Alhoshani, A.; Korashy, H.M. Aryl hydrocarbon receptor/cytochrome P450 1A1 pathway mediates breast cancer stem cells expansion through PTEN inhibition and β-Catenin and Akt activation. Mol. Cancer, 2017, 16(1), 14-32.
[http://dx.doi.org/10.1186/s12943-016-0570-y] [PMID: 28103884]
[66]
Corbet, C. Stem cell metabolism in cancer and healthy tissues: Pyruvate in the limelight. Front. Pharmacol., 2018, 8, 958.
[http://dx.doi.org/10.3389/fphar.2017.00958] [PMID: 29403375]
[67]
De Francesco, E.M.; Sotgia, F.; Lisanti, M.P. Cancer stem cells (CSCs): metabolic strategies for their identification and eradication. Biochem. J., 2018, 475(9), 1611-1634.
[http://dx.doi.org/10.1042/BCJ20170164] [PMID: 29743249]
[68]
Sánchez-Aragó, M.; Chamorro, M.; Cuezva, J.M. Selection of cancer cells with repressed mitochondria triggers colon cancer progression. Carcinogenesis, 2010, 31(4), 567-576.
[http://dx.doi.org/10.1093/carcin/bgq012] [PMID: 20080835]
[69]
Simsek, T.; Kocabas, F.; Zheng, J.; Deberardinis, R.J.; Mahmoud, A.I.; Olson, E.N.; Schneider, J.W.; Zhang, C.C.; Sadek, H.A. The distinct metabolic profile of hematopoietic stem cells reflects their location in a hypoxic niche. Cell Stem Cell, 2010, 7(3), 380-390.
[http://dx.doi.org/10.1016/j.stem.2010.07.011] [PMID: 20804973]
[70]
Kato, T.; Fujino, H.; Oyama, S.; Kawashima, T.; Murayama, T. Indomethacin induces cellular morphological change and migration via epithelial-mesenchymal transition in A549 human lung cancer cells: a novel cyclooxygenase-inhibition-independent effect. Biochem. Pharmacol., 2011, 82(11), 1781-1791.
[http://dx.doi.org/10.1016/j.bcp.2011.07.096] [PMID: 21840302]
[71]
Wang, Z.L.; Fan, Z.Q.; Jiang, H.D.; Qu, J.M. Selective Cox-2 inhibitor celecoxib induces epithelial-mesenchymal transition in human lung cancer cells via activating MEK-ERK signaling. Carcinogenesis, 2013, 34(3), 638-646.
[http://dx.doi.org/10.1093/carcin/bgs367] [PMID: 23172668]
[72]
Behr, C.A.; Hesketh, A.J.; Barlow, M.; Glick, R.D.; Symons, M.; Steinberg, B.M.; Soffer, S.Z. Celecoxib inhibits Ewing sarcoma cell migration via actin modulation. J. Surg. Res., 2015, 198(2), 424-433.
[http://dx.doi.org/10.1016/j.jss.2015.03.085] [PMID: 25934222]
[73]
Mandujano-Tinoco, E.A.; Gallardo-Pérez, J.C.; Marín-Hernández, A.; Moreno-Sánchez, R.; Rodríguez-Enríquez, S. Anti-mitochondrial therapy in human breast cancer multi-cellular spheroids. Biochim. Biophys. Acta, 2013, 1833(3), 541-551.
[http://dx.doi.org/10.1016/j.bbamcr.2012.11.013] [PMID: 23195224]
[74]
Harris, R.E.; Chlebowski, R.T.; Jackson, R.D.; Frid, D.J.; Ascenseo, J.L.; Anderson, G.; Loar, A.; Rodabough, R.J.; White, E.; McTiernan, A. Women's Health Initiative, Breast cancer and nonsteroidal anti-inflammatory drugs: prospective results from the Women's Health Initiative. Cancer Res., 2003, 63(18), 6096-6101.
[PMID: 14522941]
[75]
Takkouche, B.; Regueira-Méndez, C.; Etminan, M. Breast cancer and use of nonsteroidal anti-inflammatory drugs: a meta-analysis. J. Natl. Cancer Inst., 2008, 100(20), 1439-1447.
[http://dx.doi.org/10.1093/jnci/djn324] [PMID: 18840819]
[76]
Brasky, T.M.; Bonner, M.R.; Moysich, K.B.; Ambrosone, C.B.; Nie, J.; Tao, M.H.; Edge, S.B.; Kallakury, B.V.; Marian, C.; Trevisan, M.; Shields, P.G.; Freudenheim, J.L. Non-steroidal anti-inflammatory drug (NSAID) use and breast cancer risk in the Western New York Exposures and Breast Cancer (WEB) Study. Cancer Causes Control, 2010, 21(9), 1503-1512.
[http://dx.doi.org/10.1007/s10552-010-9579-5] [PMID: 20499154]
[77]
Coombes, R.C.; Tovey, H.; Kilburn, L.; Mansi, J.; Palmieri, C.; Bartlett, J.; Hicks, J.; Makris, A.; Evans, A.; Loibl, S. A phase III multicentre double blind randomised trial of celecoxib versus placebo in primary breast cancer patients (REACT – Randomised European celecoxib trial). Cancer Res., 2018, 78, GS3.
[78]
Seo, A.M.; Hong, S.W.; Shin, J.S.; Park, I.C.; Hong, N.J.; Kim, D.J.; Lee, W.K.; Lee, W.J.; Jin, D.H.; Lee, M.S. Sulindac induces apoptotic cell death in susceptible human breast cancer cells through, at least in part, inhibition of IKKbeta. Apoptosis, 2009, 14(7), 913-922.
[http://dx.doi.org/10.1007/s10495-009-0367-1] [PMID: 19526344]
[79]
Scheper, M.A.; Nikitakis, N.G.; Chaisuparat, R.; Montaner, S.; Sauk, J.J. Sulindac induces apoptosis and inhibits tumor growth in vivo in head and neck squamous cell carcinoma. Neoplasia, 2007, 9(3), 192-199.
[http://dx.doi.org/10.1593/neo.06781] [PMID: 17401459]
[80]
Hood, W.F.; Gierse, J.K.; Isakson, P.C.; Kiefer, J.R.; Kurumbail, R.G.; Seibert, K.; Monahan, J.B. Characterization of celecoxib and valdecoxib binding to cyclooxygenase. Mol. Pharmacol., 2003, 63(4), 870-877.
[http://dx.doi.org/10.1124/mol.63.4.870] [PMID: 12644588]
[81]
Koki, A.T.; Masferrer, J.L. Celecoxib: a specific COX-2 inhibitor with anticancer properties. Cancer Contr., 2002, 9(2)(Suppl.), 28-35.
[http://dx.doi.org/10.1177/107327480200902S04] [PMID: 11965228]
[82]
Kismet, K.; Akay, M.T.; Abbasoglu, O.; Ercan, A. Celecoxib: a potent cyclooxygenase-2 inhibitor in cancer prevention. Cancer Detect. Prev., 2004, 28(2), 127-142.
[http://dx.doi.org/10.1016/j.cdp.2003.12.005] [PMID: 15068837]
[83]
Ramer, R.; Walther, U.; Borchert, P.; Laufer, S.; Linnebacher, M.; Hinz, B. Induction but not inhibition of COX-2 confers human lung cancer cell apoptosis by celecoxib. J. Lipid Res., 2013, 54(11), 3116-3129.
[http://dx.doi.org/10.1194/jlr.M042283] [PMID: 23943857]
[84]
Schönthal, A.H. Antitumor properties of dimethyl-celecoxib, a derivative of celecoxib that does not inhibit cyclooxygenase-2: implications for glioma therapy. Neurosurg. Focus, 2006, 20(4), E21.
[http://dx.doi.org/10.3171/foc.2006.20.4.14] [PMID: 16709027]
[85]
Ralph, S.J.; Rodríguez-Enríquez, S.; Neuzil, J.; Saavedra, E.; Moreno-Sánchez, R. The causes of cancer revisited: “mitochondrial malignancy” and ROS-induced oncogenic transformation - why mitochondria are targets for cancer therapy. Mol. Aspects Med., 2010, 31(2), 145-170.
[http://dx.doi.org/10.1016/j.mam.2010.02.008] [PMID: 20206201]
[86]
Moreno-Sánchez, R.; Hernández-Esquivel, L.; Rivero-Segura, N.A.; Marín-Hernández, A.; Neuzil, J.; Ralph, S.J.; Rodríguez-Enríquez, S. Reactive oxygen species are generated by the respiratory complex II--evidence for lack of contribution of the reverse electron flow in complex I. FEBS J., 2013, 280(3), 927-938.
[http://dx.doi.org/10.1111/febs.12086] [PMID: 23206332]
[87]
Yang, Y.; Karakhanova, S.; Hartwig, W.; D’Haese, J.G.; Philippov, P.P.; Werner, J.; Bazhin, A.V. Mitochondria and mitochondrial ROS in cancer: Novel targets for anticancer therapy. J. Cell. Physiol., 2016, 231(12), 2570-2581.
[http://dx.doi.org/10.1002/jcp.25349] [PMID: 26895995]
[88]
Wang, C.; Shao, L.; Pan, C.; Ye, J.; Ding, Z.; Wu, J.; Du, Q.; Ren, Y.; Zhu, C. Elevated level of mitochondrial reactive oxygen species via fatty acid β-oxidation in cancer stem cells promotes cancer metastasis by inducing epithelial-mesenchymal transition. Stem Cell Res. Ther., 2019, 10(1), 175.
[http://dx.doi.org/10.1186/s13287-019-1265-2] [PMID: 31196164]
[89]
Nishikawa, M.; Hashida, M.; Takakura, Y. Catalase delivery for inhibiting ROS-mediated tissue injury and tumor metastasis. Adv. Drug Deliv. Rev., 2009, 61(4), 319-326.
[http://dx.doi.org/10.1016/j.addr.2009.01.001] [PMID: 19385054]
[90]
Li, W.; Ma, Q.; Li, J.; Guo, K.; Liu, H.; Han, L.; Ma, G. Hyperglycemia enhances the invasive and migratory activity of pancreatic cancer cells via hydrogen peroxide. Oncol. Rep., 2011, 25(5), 1279-1287.
[PMID: 21249318]
[91]
Storz, P. Reactive oxygen species in tumor progression. Front. Biosci., 2005, 10, 1881-1896.
[http://dx.doi.org/10.2741/1667] [PMID: 15769673]
[92]
Reuter, S.; Gupta, S.C.; Chaturvedi, M.M.; Aggarwal, B.B. Oxidative stress, inflammation, and cancer: how are they linked? Free Radic. Biol. Med., 2010, 49(11), 1603-1616.
[http://dx.doi.org/10.1016/j.freeradbiomed.2010.09.006] [PMID: 20840865]
[93]
Aggarwal, V.; Tuli, H.S.; Varol, A.; Thakral, F.; Yerer, M.B.; Sak, K.; Varol, M.; Jain, A.; Khan, M.A.; Sethi, G. Role of reactive oxygen species in cancer progression: molecular mechanisms and recent advancements. Biomolecules, 2019, 9(11), 735.
[http://dx.doi.org/10.3390/biom9110735] [PMID: 31766246]
[94]
Backhus, L.M.; Petasis, N.A.; Uddin, J.; Schönthal, A.H.; Bart, R.D.; Lin, Y.; Starnes, V.A.; Bremner, R.M. Dimethyl celecoxib as a novel non-cyclooxygenase 2 therapy in the treatment of non-small cell lung cancer. J. Thorac. Cardiovasc. Surg., 2005, 130(5), 1406-1412.
[http://dx.doi.org/10.1016/j.jtcvs.2005.07.018] [PMID: 16256796]

Rights & Permissions Print Cite
Article Metrics
26
1
© 2024 Bentham Science Publishers | Privacy Policy