Abstract
Drug resistance as a remarkable issue in cancer treatment is associated with inflammation which occurs through complex chemical reactions in the tumor microenvironment. Recent studies have implicated that glucocorticoids and NSAIDs are mainly useful combinations for inflammatory response modulation in chemotherapeutic protocols for cancer treatment. Immunosuppressive actions of glucocorticoids and NSAIDs are mainly mediated by the transrepression or activation regulation of inflammatory genes with different DNA-bound transcription factors including AP-1, NFAT, NF-κB, STAT and also, varying functions of COX enzymes in cancer cells. Interestingly, many investigations have proved the benefits of these anti-inflammatory agents in the quenching of multidrug resistance pathways. Numerous analyses on the ABC transporter promoters showed conserved nucleotide sequences with several DNA response elements that participate in transcriptional regulation. Furthermore, genetic variations in nucleotide sequences of membrane transporters were strongly associated with changes in these transporters' expression or function and a substantial impact on systemic drug exposure and toxicity. It appeared that several polymorphisms in MDR transporter genes especially MDR1 have influenced the regulatory mechanisms and explained differences in glucocorticoid responses.
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Abbreviations
- ABC transporters:
-
ATP-binding cassette transporters
- ABCC:
-
ATP-binding cassette transporters sub-family C
- ABCA:
-
ATP-binding cassette transporters sub-family A
- ABCG:
-
ATP-binding cassette transporters sub-family G
- AC:
-
Adenylyl cyclase
- AP-1,2:
-
Activating protein-1 and 2
- BCRP:
-
Breast cancer resistance protein
- C/EBP:
-
CCAAT-enhancer-binding proteins
- COX:
-
Cyclooxygenase
- CRE:
-
CAMP response element
- CYP3A4:
-
Cytochrome P450 3A4
- ERE:
-
Estrogen response element
- FKBP51:
-
FK506 binding protein
- 5-FU:
-
5-Fluorouracil
- γ-GCSh:
-
γ-Glutamylcystein synthetase heavy subunit
- G-protein:
-
Guanosine triphosphate-binding proteins
- GRE:
-
Glucocorticoid response elements
- 11b-HSD1:
-
11B-hydroxysteroid dehydrogenase type 1
- HSE:
-
Heat shock element
- HSP:
-
Heat shock protein
- JAK:
-
Janus kinase
- JNK:
-
C-Jun N-terminal Kinase
- LOX:
-
Lipoxygenase
- MAPK:
-
Mitogen-activated protein kinase
- MDR:
-
Multi drug resistance
- MRP:
-
Multidrug-resistance-related protein
- nGRE:
-
Negative GRE
- NF-κB:
-
Nuclear factor-κB
- NSAIDs:
-
Nonsteroidal anti-inflammatory drugs
- P-gp:
-
P-glycoprotein
- PKC:
-
Protein kinase C
- PXR:
-
Pregnane X receptor
- PRE:
-
Progesterone response element
- ROS:
-
Reactive oxygen species
- RXR:
-
Retinoid X receptor
- SNP:
-
Single nucleotide polymorphism
- SP-1:
-
Specificity protein 1
- SP/KLF:
-
Specificity protein/Kruppel-like factor
- SRE:
-
Sterol regulatory element
- STAT:
-
Signal transducers and activators of transcription
- TdT:
-
Terminal deoxynucleotidyl transferase
- TNF-α:
-
Tumor necrosis factor-α
- TPA:
-
12-O-Tetradecanoylphorbol-13-acetate
- TSS:
-
Transcription start sites
References
Abdellatif KRA, Abdelall EKA, Fadaly WAA, Kamel GM (2016) Synthesis, cyclooxygenase inhibition, anti-inflammatory evaluation and ulcerogenic liability of new 1,3,5-triarylpyrazoline and 1,5-diarylpyrazole derivatives as selective COX-2 inhibitors. Bioorg Med Chem Lett 26:406–412. https://doi.org/10.1016/j.bmcl.2015.11.105
Adamska A, Falasca M (2018) ATP-binding cassette transporters in progression and clinical outcome of pancreatic cancer: what is the way forward? World J Gastroenterol 24:3222–3238. https://doi.org/10.3748/wjg.v24.i29.3222
Agundez JA, Garcia-Martin E, Martinez C (2009) Genetically based impairment in CYP2C8- and CYP2C9-dependent NSAID metabolism as a risk factor for gastrointestinal bleeding: is a combination of pharmacogenomics and metabolomics required to improve personalized medicine? Expert Opin Drug Metab Toxicol 5:607–620. https://doi.org/10.1517/17425250902970998
Ahmed S, Zhou Z, Zhou J, Chen SQ (2016) Pharmacogenomics of drug metabolizing enzymes and transporters: relevance to precision medicine. Genom Proteom Bioinform 14:298–313. https://doi.org/10.1016/j.gpb.2016.03.008
Al Argan R, Saskin A, Yang JW, D'Agostino MD, Rivera J (2018) Glucocorticoid resistance syndrome caused by a novel NR3C1 point mutation. Endocr J 65:1139–1146. https://doi.org/10.1507/endocrj.EJ18-0135
Alameh G et al (2019) In vitro modulation of multidrug resistance by pregnane steroids and in vivo inhibition of tumour development by 7alpha-OBz-11alpha(R)-OTHP-5beta-pregnanedione in K562/R7 and H295R cell xenografts. J Enzyme Inhib Med Chem 34:684–691. https://doi.org/10.1080/14756366.2019.1575825
Angelini A, Iezzi M, Di Febbo C, Di Ilio C, Cuccurullo F, Porreca E (2008) Reversal of P-glycoprotein-mediated multidrug resistance in human sarcoma MES-SA/Dx-5 cells by nonsteroidal anti-inflammatory drugs. Oncol Rep 20:731–735
Bai XM et al (2010) Prostaglandin E2 upregulates survivin expression via the EP1 receptor in hepatocellular carcinoma cells. Life Sci 86:214–223. https://doi.org/10.1016/j.lfs.2009.12.009
Bark H, Choi CH (2010) PSC833, cyclosporine analogue, downregulates MDR1 expression by activating JNK/c-Jun/AP-1 and suppressing NF-kappaB. Cancer Chemother Pharmacol 65:1131–1136. https://doi.org/10.1007/s00280-009-1121-7
Barnes PJ (2011) Glucocorticosteroids: current and future directions. Br J Pharmacol 163:29–43. https://doi.org/10.1111/j.1476-5381.2010.01199.x
Begicevic RR, Falasca M (2017) ABC Transporters in cancer stem cells: beyond chemoresistance. Int J Mol Sci. https://doi.org/10.3390/ijms18112362
Brune K, Patrignani P (2015) New insights into the use of currently available non-steroidal anti-inflammatory drugs. J Pain Res 8:105–118. https://doi.org/10.2147/JPR.S75160
Burnett BP, Levy RM (2012) 5-Lipoxygenase metabolic contributions to NSAID-induced organ toxicity. Adv Ther 29:79–98. https://doi.org/10.1007/s12325-011-0100-7
Chaikomon K, Chattong S, Chaiya T, Tiwawech D, Sritana-Anant Y, Sereemaspun A, Manotham K (2018) Doxorubicin-conjugated dexamethasone induced MCF-7 apoptosis without entering the nucleus and able to overcome MDR-1-induced resistance. Drug Des Dev Ther 12:2361–2369. https://doi.org/10.2147/DDDT.S168588
Chan GN, Saldivia V, Yang Y, Pang H, de Lannoy I, Bendayan R (2013) vivo induction of P-glycoprotein expression at the mouse blood-brain barrier: an intracerebral microdialysis study. J Neurochem 127:342–352. https://doi.org/10.1111/jnc.12344
Charlier C, Michaux C (2003) Dual inhibition of cyclooxygenase-2 (COX-2) and 5-lipoxygenase (5-LOX) as a new strategy to provide safer non-steroidal anti-inflammatory drugs. Eur J Med Chem 38:645–659. https://doi.org/10.1016/s0223-5234(03)00115-6
Chen KG, Sikic BI (2012) Molecular pathways: regulation and therapeutic implications of multidrug resistance. Clin Cancer Res 18:1863–1869. https://doi.org/10.1158/1078-0432.CCR-11-1590
Chen M, Yu L, Gu C, Zhong D, Wu S, Liu S (2013) Celecoxib antagonizes the cytotoxic effect of cisplatin in human gastric cancer cells by decreasing intracellular cisplatin accumulation. Cancer Lett 329:189–196. https://doi.org/10.1016/j.canlet.2012.10.030
Chen Q, Bian Y, Zeng S (2014) Involvement of AP-1 and NF-kappaB in the up-regulation of P-gp in vinblastine resistant Caco-2 cells. Drug Metab Pharmacokinet 29:223–226. https://doi.org/10.2133/dmpk.dmpk-13-sh-068
Chen SF, Zhang ZY, Zhang JL (2015) Meloxicam increases intracellular accumulation of doxorubicin via downregulation of multidrug resistance-associated protein 1 (MRP1) in A549 cells. Genet Mol Res 14:14548–14560. https://doi.org/10.4238/2015.November.18.18
Chen N, Cui D, Wang Q, Wen Z, Finkelman RD, Welty D (2018) In vitro drug-drug interactions of budesonide: inhibition and induction of transporters and cytochrome P450 enzymes. Xenobiotica 48:637–646. https://doi.org/10.1080/00498254.2017.1344911
Cooray HC, Shahi S, Cahn AP, van Veen HW, Hladky SB, Barrand MA (2006) Modulation of p-glycoprotein and breast cancer resistance protein by some prescribed corticosteroids. Eur J Pharmacol 531:25–33
Corsello SM et al (2020) Discovering the anti-cancer potential of non-oncology drugs by systematic viability profiling. Nat Cancer 1:235–248. https://doi.org/10.1038/s43018-019-0018-6
Cruz-Topete D, Cidlowski JA (2018) Glucocorticoids: molecular mechanisms of action. In: Riccardi C, Levi-Schaffer F, Tiligada E (eds) Immunopharmacology and inflammation. Springer, Cham. https://doi.org/10.1007/978-3-319-77658-3_1
de Ravel MR et al (2015) Synthesis of new steroidal inhibitors of P-glycoprotein-mediated multidrug resistance and biological evaluation on K562/R7 erythroleukemia cells. J Med Chem 58:1832–1845. https://doi.org/10.1021/jm501676v
de Ruiter RD et al (2014) Adrenal insufficiency during treatment for childhood acute lymphoblastic leukemia is associated with glucocorticoid receptor polymorphisms ER22/23EK and BclI. Haematologica 99:e136–137. https://doi.org/10.3324/haematol.2014.105056
Dharmapuri G, Doneti R, Philip GH, Kalle AM (2015) Celecoxib sensitizes imatinib-resistant K562 cells to imatinib by inhibiting MRP1–5, ABCA2 and ABCG2 transporters via Wnt and Ras signaling pathways. Leuk Res 39:696–701. https://doi.org/10.1016/j.leukres.2015.02.013
Ding XZ, Hennig R, Adrian TE (2003) Lipoxygenase and cyclooxygenase metabolism: new insights in treatment and chemoprevention of pancreatic cancer. Mol Cancer 2:10. https://doi.org/10.1186/1476-4598-2-10
Dujic T et al (2012) Association between 11beta-hydroxysteroid dehydrogenase type 1 gene polymorphisms and metabolic syndrome in Bosnian population. Biochem Med (Zagreb) 22:76–85
Eckert D, Buhl S, Weber S, Jager R, Schorle H (2005) The AP-2 family of transcription factors. Genome Biol 6:246. https://doi.org/10.1186/gb-2005-6-13-246
Eclov RJ, Kim MJ, Smith R, Ahituv N, Kroetz DL (2018) Rare variants in the ABCG2 promoter modulate in vivo activity. Drug Metab Dispos 46:636–642. https://doi.org/10.1124/dmd.117.079541
Eferl R, Wagner EF (2003) AP-1: a double-edged sword in tumorigenesis. Nat Rev Cancer 3:859–868. https://doi.org/10.1038/nrc1209
Elahian F, Kalalinia F, Behravan J (2009) Dexamethasone downregulates BCRP mRNA and protein expression in breast cancer cell lines. Oncol Res 18:9–15. https://doi.org/10.3727/096504009789745674
Elahian F, Kalalinia F, Behravan J (2010) Evaluation of indomethacin and dexamethasone effects on BCRP-mediated drug resistance in MCF-7 parental and resistant cell lines. Drug Chem Toxicol 33:113–119. https://doi.org/10.3109/01480540903390000
El-Awady RA, Saleh EM, Ezz M, Elsayed AM (2011) Interaction of celecoxib with different anti-cancer drugs is antagonistic in breast but not in other cancer cells. Toxicol Appl Pharmacol 255:271–286. https://doi.org/10.1016/j.taap.2011.06.019
El-Fattah Ibrahim SA, Abudu A, Johnson E, Aftab N, Conrad S, Fluck M (2019) Correction: the role of AP-1 in self-sufficient proliferation and migration of cancer cells and its potential impact on an autocrine/paracrine loop. Oncotarget 10:799. https://doi.org/10.18632/oncotarget.26636
Escoter-Torres L, Caratti G, Mechtidou A, Tuckermann J, Uhlenhaut NH, Vettorazzi S (2019) Fighting the fire: mechanisms of inflammatory gene regulation by the glucocorticoid receptor. Front Immunol 10:1859. https://doi.org/10.3389/fimmu.2019.01859
Fujii T et al (2014) The common functional FKBP5 variant rs1360780 is associated with altered cognitive function in aged individuals. Sci Rep 4:6696. https://doi.org/10.1038/srep06696
Fuksa L et al (2010) Dexamethasone reduces methotrexate biliary elimination and potentiates its hepatotoxicity in rats. Toxicology 267:165–171. https://doi.org/10.1016/j.tox.2009.11.010
Galigniana NM, Ballmer LT, Toneatto J, Erlejman AG, Lagadari M, Galigniana MD (2012) Regulation of the glucocorticoid response to stress-related disorders by the Hsp90-binding immunophilin FKBP51. J Neurochem 122:4–18. https://doi.org/10.1111/j.1471-4159.2012.07775.x
Gasic V et al (2018) Pharmacogenomic markers of glucocorticoid response in the initial phase of remission induction therapy in childhood acute lymphoblastic leukemia. Radiol Oncol 52:296–306. https://doi.org/10.2478/raon-2018-0034
Gillet JP, Gottesman MM (2010) Mechanisms of multidrug resistance in cancer. Methods Mol Biol 596:47–76. https://doi.org/10.1007/978-1-60761-416-6_4
Gromnicova R, Romero I, Male D (2012) Transcriptional control of the multi-drug transporter ABCB1 by transcription factor Sp3 in different human tissues. PLoS ONE 7:e48189. https://doi.org/10.1371/journal.pone.0048189
Gu X, Manautou JE (2010) Regulation of hepatic ABCC transporters by xenobiotics and in disease states. Drug Metab Rev 42:482–538. https://doi.org/10.3109/03602531003654915
Guo T, Huang J, Huan C, He F, Zhang Y, Bhutto ZA, Wang L (2018) Cloning and transcriptional activity analysis of the porcine Abcb1 gene promoter: transcription factor Sp1 regulates the expression of porcine Abcb1. Front Pharmacol 9:373. https://doi.org/10.3389/fphar.2018.00373
Gupta MK, Singh R, Banerjee M (2016) Cytokine gene polymorphisms and their association with cervical cancer: a North Indian study. Egypt J Med Hum Genet 17:155–163
Harasim-Symbor E, Konstantynowicz-Nowicka K, Chabowski A (2016) Additive effects of dexamethasone and palmitate on hepatic lipid accumulation and secretion. J Mol Endocrinol 57:261–273. https://doi.org/10.1530/JME-16-0108
Hasegawa K et al (2013) Overcoming paclitaxel resistance in uterine endometrial cancer using a COX-2 inhibitor. Oncol Rep 30:2937–2944. https://doi.org/10.3892/or.2013.2790
Hilovska L, Jendzelovsky R, Fedorocko P (2015) Potency of non-steroidal anti-inflammatory drugs in chemotherapy. Mol Clin Oncol 3:3–12. https://doi.org/10.3892/mco.2014.446
Honorat M et al (2011) MRP8/ABCC11 expression is regulated by dexamethasone in breast cancer cells and is associated to progesterone receptor status in breast tumors. Int J Breast Cancer 2011:807380. https://doi.org/10.4061/2011/807380
Ihunnah CA, Jiang M, Xie W (2011) Nuclear receptor PXR, transcriptional circuits and metabolic relevance. Biochim Biophys Acta 1812:956–963. https://doi.org/10.1016/j.bbadis.2011.01.014
Imai Y, Ishikawa E, Asada S, Sugimoto Y (2005) Estrogen-mediated post transcriptional down-regulation of breast cancer resistance protein/ABCG2. Cancer Res 65:596–604
Iqbal M, Audette MC, Petropoulos S, Gibb W, Matthews SG (2012) Placental drug transporters and their role in fetal protection. Placenta 33:137–142. https://doi.org/10.1016/j.placenta.2012.01.008
Jala VR, Bodduluri SR, Satpathy SR, Chheda Z, Sharma RK, Haribabu B (2017) The yin and yang of leukotriene B4 mediated inflammation in cancer. Semin Immunol 33:58–64. https://doi.org/10.1016/j.smim.2017.09.005
Jaramillo AC, Al Saig F, Cloos J, Jansen G, Peters GJ (2018) How to overcome ATP-binding cassette drug efflux transporter-mediated drug resistance. Cancer Drug Resist 1:6–29
Ji W, Wang B, Fan Q, Xu C, He Y, Chen Y (2017) Chemosensitizing indomethacin-conjugated dextran-based micelles for effective delivery of paclitaxel in resistant breast cancer therapy. PLoS ONE 12:e0180037. https://doi.org/10.1371/journal.pone.0180037
Kadmiel M, Cidlowski JA (2013) Glucocorticoid receptor signaling in health and disease. Trends Pharmacol Sci 34:518–530. https://doi.org/10.1016/j.tips.2013.07.003
Kalalinia F, Elahian F, Behravan J (2011) Potential role of cyclooxygenase-2 on the regulation of the drug efflux transporter ABCG2 in breast cancer cell lines. J Cancer Res Clin Oncol 137:321–330. https://doi.org/10.1007/s00432-010-0893-9
Kalalinia F, Elahian F, Mosaffa F, Behravan J (2014) Celecoxib up regulates the expression of drug efflux transporter ABCG2 in breast cancer cell lines. Iran J Pharm Res 13:1393–1401
Kim HG et al (2011) Metformin inhibits P-glycoprotein expression via the NF-kappaB pathway and CRE transcriptional activity through AMPK activation. Br J Pharmacol 162:1096–1108. https://doi.org/10.1111/j.1476-5381.2010.01101.x
Kobayashi M et al (2013) Regulation of multidrug resistance protein 2 (MRP2, ABCC2) expression by statins: involvement of SREBP-mediated gene regulation. Int J Pharm 452:36–41. https://doi.org/10.1016/j.ijpharm.2013.04.019
Kolasa T et al (1997) Nonsteroidal anti-inflammatory drugs as scaffolds for the design of 5-lipoxygenase inhibitors. J Med Chem 40:819–824. https://doi.org/10.1021/jm9606150
Lee YS, Kim H, Wu TX, Wang XM, Dionne RA (2006) Genetically mediated interindividual variation in analgesic responses to cyclooxygenase inhibitory drugs. Clin Pharmacol Ther 79:407–418. https://doi.org/10.1016/j.clpt.2006.01.013
Lee JP, Hahn HS, Hwang SJ, Choi JY, Park JS, Lee IH, Kim TJ (2013) Selective cyclooxygenase inhibitors increase paclitaxel sensitivity in taxane-resistant ovarian cancer by suppressing P-glycoprotein expression. J Gynecol Oncol 24:273–279. https://doi.org/10.3802/jgo.2013.24.3.273
Leslie EM, Deeley RG, Cole SP (2005) Multidrug resistance proteins: role of P-glycoprotein, MRP1, MRP2, and BCRP (ABCG2) in tissue defense. Toxicol Appl Pharmacol 204:216–237. https://doi.org/10.1016/j.taap.2004.10.012
Li L, Davie JR (2010) The role of Sp1 and Sp3 in normal and cancer cell biology. Ann Anat 192:275–283. https://doi.org/10.1016/j.aanat.2010.07.010
Li J, Hao Q, Cao W, Vadgama JV, Wu Y (2018) Celecoxib in breast cancer prevention and therapy. Cancer Manag Res 10:4653–4667. https://doi.org/10.2147/CMAR.S178567
Lim JS, Park Y, Lee BM, Kim HS, Yoon S (2016) Co-treatment with celecoxib or NS398 strongly sensitizes resistant cancer cells to antimitotic drugs independent of P-gp inhibition. Anticancer Res 36:5063–5070. https://doi.org/10.21873/anticanres.11075
Lima RA, Candido EB, de Melo FP, Piedade JB, Vidigal PV, Silva LM, da Silva Filho AL (2015) Gene expression profile of ABC transporters and cytotoxic effect of ibuprofen and acetaminophen in an epithelial ovarian cancer cell line in vitro. Rev Bras Ginecol Obstet 37:283–290. https://doi.org/10.1590/SO100-720320150005292
Liu F, Liu S, He S, Xie Z, Zu X, Jiang Y (2010) Survivin transcription is associated with P-glycoprotein/MDR1 overexpression in the multidrug resistance of MCF-7 breast cancer cells. Oncol Rep 23:1469–1475. https://doi.org/10.3892/or_00000786
Louis S (2011) Goodman & Gilman's pharmacological basis of therapeutics. McGraw-Hill, New York
Ma M et al (2018) Celecoxib enhances sensitivity to chemotherapy drugs of T-cell lymphoma. Oncol Lett 15:4649–4656. https://doi.org/10.3892/ol.2018.7897
Maeng HJ, Lee WJ, Jin QR, Chang JE, Shim WS (2014) Upregulation of COX-2 in the lung cancer promotes overexpression of multidrug resistance protein 4 (MRP4) via PGE2-dependent pathway. Eur J Pharm Sci 62:189–196. https://doi.org/10.1016/j.ejps.2014.05.023
Magee DJ, Jhanji S, Poulogiannis G, Farquhar-Smith P, Brown MRD (2019) Nonsteroidal anti-inflammatory drugs and pain in cancer patients: a systematic review and reappraisal of the evidence. Br J Anaesth 123:e412–e423. https://doi.org/10.1016/j.bja.2019.02.028
Mahdizadeh S, Karimi G, Behravan J, Arabzadeh S, Lage H, Kalalinia F (2016) Crocin suppresses multidrug resistance in MRP overexpressing ovarian cancer cell line. Daru 24:17. https://doi.org/10.1186/s40199-016-0155-8
Maier A, Zimmermann C, Beglinger C, Drewe J, Gutmann H (2007) Effects of budesonide on P-glycoprotein expression in intestinal cell lines. Br J Pharmacol 150:361–368. https://doi.org/10.1038/sj.bjp.0706992
Manceau S et al (2012) Expression and induction by dexamethasone of ABC transporters and nuclear receptors in a human T-lymphocyte cell line. J Chemother 24:48–55. https://doi.org/10.1179/1120009X12Z.00000000010
Manohar CF et al (2004) MYCN-mediated regulation of the MRP1 promoter in human neuroblastoma. Oncogene 23:753–762. https://doi.org/10.1038/sj.onc.1207151
Martel-Pelletier J, Lajeunesse D, Reboul P, Pelletier JP (2003) Therapeutic role of dual inhibitors of 5-LOX and COX, selective and non-selective non-steroidal anti-inflammatory drugs. Ann Rheum Dis 62:501–509. https://doi.org/10.1136/ard.62.6.501
Meek IL, Van de Laar MA, Vonkeman EH (2010) Non-steroidal anti-inflammatory drugs: an overview of cardiovascular risks. Pharmaceuticals (Basel) 3:2146–2162. https://doi.org/10.3390/ph3072146
Mirzaei SA, Dinmohammadi F, Alizadeh A, Elahian F (2019) Inflammatory pathway interactions and cancer multidrug resistance regulation. Life Sci 235:116825. https://doi.org/10.1016/j.lfs.2019.116825
Mitre-Aguilar IB, Cabrera-Quintero AJ, Zentella-Dehesa A (2015) Genomic and non-genomic effects of glucocorticoids: implications for breast cancer. Int J Clin Exp Pathol 8:1–10
Mizushima T (2010) Molecular mechanism for various pharmacological activities of NSAIDS. Pharmaceuticals (Basel) 3:1614–1636. https://doi.org/10.3390/ph3051614
Mohn C, Hacker HG, Hilger RA, Gutschow M, Jaehde U (2013) Defining the role of MRP-mediated efflux and glutathione in detoxification of oxaliplatin. Pharmazie 68:622–627
Molnar A, Patocs A, Liko I, Nyiro G, Racz K, Toth M, Sarman B (2018) An unexpected, mild phenotype of glucocorticoid resistance associated with glucocorticoid receptor gene mutation case report and review of the literature. BMC Med Genet 19:37. https://doi.org/10.1186/s12881-018-0552-6
Monostory K, Dvorak Z (2011) Steroid regulation of drug-metabolizing cytochromes P450. Curr Drug Metab 12:154–172. https://doi.org/10.2174/138920011795016854
Nakanishi T, Ross DD (2012) Breast cancer resistance protein (BCRP/ABCG2): its role in multidrug resistance and regulation of its gene expression. Chin J Cancer 31:73–99. https://doi.org/10.5732/cjc.011.10320
Nicolaides NC, Galata Z, Kino T, Chrousos GP, Charmandari E (2010) The human glucocorticoid receptor: molecular basis of biologic function. Steroids 75:1–12. https://doi.org/10.1016/j.steroids.2009.09.002
P JJ, Manju SL, Ethiraj KR, Elias G (2018) Safer anti-inflammatory therapy through dual COX-2/5-LOX inhibitors: a structure-based approach. Eur J Pharm Sci 121:356–381. https://doi.org/10.1016/j.ejps.2018.06.003
Pagliarulo V et al (2013) The interaction of celecoxib with MDR transporters enhances the activity of mitomycin C in a bladder cancer cell line. Mol Cancer 12:47. https://doi.org/10.1186/1476-4598-12-47
Pariante CM (2008) The role of multi-drug resistance p-glycoprotein in glucocorticoid function: studies in animals and relevance in humans. Eur J Pharmacol 583:263–271. https://doi.org/10.1016/j.ejphar.2007.11.067
Patel VA, Dunn MJ, Sorokin A (2002) Regulation of MDR-1 (P-glycoprotein) by cyclooxygenase-2. J Biol Chem 277:38915–38920. https://doi.org/10.1074/jbc.M206855200
Pavek P, Merino G, Wagenaar E, Bolscher E, Novotna M, Jonker JW, Schinkel AH (2005) Human breast cancer resistance protein: interactions with steroid drugs, hormones, the dietary carcinogen 2-amino-1-methyl-6-phenylimidazo(4,5-b)pyridine, and transport of cimetidine. J Pharmacol Exp Ther 312:144–152. https://doi.org/10.1124/jpet.104.073916
Pellikainen JM, Kosma VM (2007) Activator protein-2 in carcinogenesis with a special reference to breast cancer—a mini review. Int J Cancer 120:2061–2067. https://doi.org/10.1002/ijc.22648
Petropoulos S, Gibb W, Matthews SG (2011a) Breast cancer-resistance protein (BCRP1) in the fetal mouse brain: development and glucocorticoid regulation. Biol Reprod 84:783–789. https://doi.org/10.1095/biolreprod.110.088468
Petropoulos S, Gibb W, Matthews SG (2011b) Glucocorticoid regulation of placental breast cancer resistance protein (Bcrp1) in the mouse. Reprod Sci 18:631–639. https://doi.org/10.1177/1933719110395399
Prevoo B, Miller DS, van de Water FM, Wever KE, Russel FG, Flik G, Masereeuw R (2011) Rapid, nongenomic stimulation of multidrug resistance protein 2 (Mrp2) activity by glucocorticoids in renal proximal tubule. J Pharmacol Exp Ther 338:362–371. https://doi.org/10.1124/jpet.111.179689
Qosa H, Miller DS, Pasinelli P, Trotti D (2015) Regulation of ABC efflux transporters at blood-brain barrier in health and neurological disorders. Brain Res 1628:298–316. https://doi.org/10.1016/j.brainres.2015.07.005
Raguz S, Tamburo De Bella M, Tripuraneni G, Slade MJ, Higgins CF, Coombes RC, Yague E (2004) Activation of the MDR1 upstream promoter in breast carcinoma as a surrogate for metastatic invasion. Clin Cancer Res 10:2776–2783. https://doi.org/10.1158/1078-0432.ccr-03-0517
Ralph SJ, Nozuhur S, Moreno-Sánchez R, Rodríguez-Enríquez S, Pritchard R (2018) NSAID celecoxib: a potent mitochondrial pro-oxidant cytotoxic agent sensitizing metastatic cancers and cancer stem cells to chemotherapy. J Cancer Metastasis Treat 4:1–26
Ramaseri Sunder S et al (2012) IL-10 high producing genotype predisposes HIV infected individuals to TB infection. Hum Immunol 73:605–611. https://doi.org/10.1016/j.humimm.2012.03.012
Reimondo G et al (2016) Analysis of BCLI, N363S and ER22/23EK polymorphisms of the glucocorticoid receptor gene in adrenal incidentalomas. PLoS ONE 11:e0162437. https://doi.org/10.1371/journal.pone.0162437
Sampson A, Peterson BG, Tan KW, Iram SH (2019) Doxorubicin as a fluorescent reporter identifies novel MRP1 (ABCC1) inhibitors missed by calcein-based high content screening of anticancer agents. Biomed Pharmacother 118:109289. https://doi.org/10.1016/j.biopha.2019.109289
Scotto KW (2003) Transcriptional regulation of ABC drug transporters. Oncogene 22:7496–7511. https://doi.org/10.1038/sj.onc.1206950
Scotto KW, Egan DA (1998) Transcriptional regulation of MDR genes. Cytotechnology 27:257–269. https://doi.org/10.1023/A:1008032716628
Shimano H (2001) Sterol regulatory element-binding proteins (SREBPs): transcriptional regulators of lipid synthetic genes. Prog Lipid Res 40:439–452. https://doi.org/10.1016/s0163-7827(01)00010-8
Sobolewski C, Cerella C, Dicato M, Ghibelli L, Diederich M (2010) The role of cyclooxygenase-2 in cell proliferation and cell death in human malignancies. Int J Cell Biol 2010:215158. https://doi.org/10.1155/2010/215158
Stejskalová L, Vrzal R, Rulcová A, Dvořák Z, Pávek P (2013) Effects of glucocorticoids on cytochrome P450 1A1 (CYP1A1) expression in isolated human placental trophoblast. J Appl Biomed 11:163–172
Tarling EJ, Edwards PA (2011) ATP binding cassette transporter G1 (ABCG1) is an intracellular sterol transporter. Proc Natl Acad Sci USA 108:19719–19724. https://doi.org/10.1073/pnas.1113021108
Tatebe S, Sinicrope FA, Kuo MT (2002) Induction of multidrug resistance proteins MRP1 and MRP3 and gamma-glutamylcysteine synthetase gene expression by nonsteroidal anti-inflammatory drugs in human colon cancer cells. Biochem Biophys Res Commun 290:1427–1433. https://doi.org/10.1006/bbrc.2002.6367
Thun MJ, Jacobs EJ, Patrono C (2012) The role of aspirin in cancer prevention. Nat Rev Clin Oncol 9:259–267. https://doi.org/10.1038/nrclinonc.2011.199
Tolson AH, Wang H (2010) Regulation of drug-metabolizing enzymes by xenobiotic receptors: PXR and CAR. Adv Drug Deliv Rev 62:1238–1249. https://doi.org/10.1016/j.addr.2010.08.006
Tsubaki M, Takeda T, Tomonari Y, Koumoto YI, Imano M, Satou T, Nishida S (2019) Overexpression of HIF-1alpha contributes to melphalan resistance in multiple myeloma cells by activation of ERK1/2 Akt, and NF-kappaB. Lab Invest 99:72–84. https://doi.org/10.1038/s41374-018-0114-8
Verhoeven F, Prati C, Maguin-Gate K, Wendling D, Demougeot C (2016) Glucocorticoids and endothelial function in inflammatory diseases: focus on rheumatoid arthritis. Arthritis Res Ther 18:258. https://doi.org/10.1186/s13075-016-1157-0
Wang B, Ngoi S, Wang J, Chong SS, Lee CG (2006) The promoter region of the MDR1 gene is largely invariant, but different single nucleotide polymorphism haplotypes affect MDR1 promoter activity differently in different cell lines. Mol Pharmacol 70:267–276. https://doi.org/10.1124/mol.105.019810
Wang J et al (2012) Contrasting effects of diclofenac and ibuprofen on active imatinib uptake into leukaemic cells. Br J Cancer 106:1772–1778. https://doi.org/10.1038/bjc.2012.173
Wang J, Seebacher N, Shi H, Kan Q, Duan Z (2017) Novel strategies to prevent the development of multidrug resistance (MDR) in cancer. Oncotarget 8:84559–84571. https://doi.org/10.18632/oncotarget.19187
Wang X, Sun D, Tai J, Chen S, Yu M, Ren D, Wang L (2018) TFAP2C promotes stemness and chemotherapeutic resistance in colorectal cancer via inactivating hippo signaling pathway. J Exp Clin Cancer Res 37:27. https://doi.org/10.1186/s13046-018-0683-9
Webb T, Carter J, Roberts JL, Poklepovic A, McGuire WP, Booth L, Dent P (2015) Celecoxib enhances [sorafenib + sildenafil] lethality in cancer cells and reverts platinum chemotherapy resistance. Cancer Biol Ther 16:1660–1670. https://doi.org/10.1080/15384047.2015.1099769
Whyte-Allman SK, Hoque MT, Jenabian MA, Routy JP, Bendayan R (2017) Xenobiotic nuclear receptors pregnane X receptor and constitutive androstane receptor regulate antiretroviral drug efflux transporters at the blood-testis barrier. J Pharmacol Exp Ther 363:324–335. https://doi.org/10.1124/jpet.117.243584
Wu KC, Lin CJ (2019) The regulation of drug-metabolizing enzymes and membrane transporters by inflammation: evidences in inflammatory diseases and age-related disorders. J Food Drug Anal 27:48–59. https://doi.org/10.1016/j.jfda.2018.11.005
Wu WK, Sung JJ, Lee CW, Yu J, Cho CH (2010) Cyclooxygenase-2 in tumorigenesis of gastrointestinal cancers: an update on the molecular mechanisms. Cancer Lett 295:7–16. https://doi.org/10.1016/j.canlet.2010.03.015
Wyatt JE, Pettit WL, Harirforoosh S (2012) Pharmacogenetics of nonsteroidal anti-inflammatory drugs. Pharmacogenom J 12:462–467. https://doi.org/10.1038/tpj.2012.40
Xing K, Gu B, Zhang P, Wu X (2015) Dexamethasone enhances programmed cell death 1 (PD-1) expression during T cell activation: an insight into the optimum application of glucocorticoids in anti-cancer therapy. BMC Immunol 16:39. https://doi.org/10.1186/s12865-015-0103-2
Yamagishi N et al (2014) Increased expression of sorcin is associated with multidrug resistance in leukemia cells via up-regulation of MDR1 expression through cAMP response element-binding protein. Biochem Biophys Res Commun 448:430–436. https://doi.org/10.1016/j.bbrc.2014.04.125
Yan YX, Li WZ, Huang YQ, Liao WX (2012) The COX-2 inhibitor Celecoxib enhances the sensitivity of KB/VCR oral cancer cell lines to Vincristine by down-regulating P-glycoprotein expression and function. Prostaglandins Other Lipid Mediat 97:29–35. https://doi.org/10.1016/j.prostaglandins.2011.07.007
Ye CG et al (2011) Indomethacin and SC236 enhance the cytotoxicity of doxorubicin in human hepatocellular carcinoma cells via inhibiting P-glycoprotein and MRP1 expression. Cancer Lett 304:90–96. https://doi.org/10.1016/j.canlet.2011.01.025
Yiannakopoulou E (2013) Pharmacogenomics of acetylsalicylic acid and other nonsteroidal anti-inflammatory agents: clinical implications. Eur J Clin Pharmacol 69:1369–1373. https://doi.org/10.1007/s00228-013-1477-9
Zarghi A, Arfaei S (2011) Selective COX-2 inhibitors: a review of their structure-activity relationships. Iran J Pharm Res 10:655–683
Zhang XQ et al (2015) Synergic effect between 5fluorouracil and celecoxib on hypoxic gastric cancer cells. Mol Med Rep 11:1160–1166. https://doi.org/10.3892/mmr.2014.2783
Zhang Z, Chen F, Shang L (2018) Advances in antitumor effects of NSAIDs. Cancer Manag Res 10:4631–4640. https://doi.org/10.2147/CMAR.S175212
Zhu FS, Chen XM, Huang ZG, Wang ZR, Zhang DW, Zhang X (2010) Rofecoxib augments anticancer effects by reversing intrinsic multidrug resistance gene expression in BGC-823 gastric cancer cells. J Dig Dis 11:34–42. https://doi.org/10.1111/j.1751-2980.2009.00411.x
Zielinska KA, Van Moortel L, Opdenakker G, De Bosscher K, Van den Steen PE (2016) Endothelial response to glucocorticoids in inflammatory diseases. Front Immunol 7:592. https://doi.org/10.3389/fimmu.2016.00592
Ziemann C, Schafer D, Rudell G, Kahl GF, Hirsch-Ernst KI (2002) The cyclooxygenase system participates in functional mdr1b overexpression in primary rat hepatocyte cultures. Hepatology 35:579–588. https://doi.org/10.1053/jhep.2002.31778
Acknowledgements
We would like to thank Professor M. Hashemzadeh (Department of Medical Genetics), Professor M. Ghatrehsamani (Department of Medical Immunology), and Bita Jafari (the graphic designer) for their valuable feedback and suggestions. We thank the anonymous reviewers for their thoughtful comments, which have helped improving the quality of the article.
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This work was supported by the Shahrekord University of Medical Sciences under Grant SKUMS-5204.
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Gholamian Dehkordi, N., Mirzaei, S.A. & Elahian, F. Pharmacodynamic mechanisms of anti-inflammatory drugs on the chemosensitization of multidrug-resistant cancers and the pharmacogenetics effectiveness. Inflammopharmacol 29, 49–74 (2021). https://doi.org/10.1007/s10787-020-00765-9
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DOI: https://doi.org/10.1007/s10787-020-00765-9