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Nitric Oxide Reverts the Resistance to Doxorubicin in Human Colon Cancer Cells by Inhibiting the Drug Efflux
Abstract
Multidrug resistance (MDR) is a phenomenon by which cancer cells evade the cytotoxic effects of chemotherapeutic agents. It may occur through different mechanisms, but it often correlates with the overexpression of integral membrane transporters, such as P-glycoprotein (Pgp) and MDR-associated proteins (MRPs), with resulting decrease of drug accumulation and cellular death. Doxorubicin is a substrate of Pgp; it has been suggested that its ability to induce synthesis of nitric oxide (NO) could explain, at least in part, its cytotoxic effects. Culturing the human epithelial colon cell line HT29 in the presence of doxorubicin, we obtained a doxorubicin-resistant (HT29-dx) cell population: these cells accumulated less intracellular doxorubicin, were less sensitive to the cytotoxic effects of doxorubicin and cisplatin, overexpressed Pgp and MRP3, and exhibited a lower NO production (both under basal conditions and after doxorubicin stimulation). The resistance to doxorubicin could be reversed when HT29-dx cells were incubated with inducers of NO synthesis (cytokines mix, atorvastatin). Some NO donors increased the drug accumulation in HT29-dx cells in a guarosine-3′:5′-cyclic monophosphate–independent way; this effect was associated with a marked reduction of doxorubicin efflux rate in HT29 and HT29-dx cells, and tyrosine nitration in the MRP3 protein. Our results suggest that onset of MDR and impairment of NO synthesis are related; this finding could point to a new strategy to reverse doxorubicin resistance in human cancer.
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Previous works from our group has shown that statins have chemosensitizing properties in epithelial tumours.
“Previous works from our group has shown that statins have chemosensitizing properties in epithelial tumours (Riganti et al., 2005;Riganti et al., 2006;Kopecka et al., 2011).”
From The association of statins plus LDL receptor‐targeted liposome‐encapsulated doxorubicin increases in vitro drug delivery across blood–brain barrier cells (2012) · cites this paper as Riganti et al., 2005
In cancer cells, statins increase synthesis of NO, which inhibits ABC transporters efflux, and decrease amount of membrane cholesterol, which also lowers activity of Pgp/ABCB1.
“We have previously observed that in cancer cells, statins increase the synthesis of NO, which inhibits ABC transporters efflux (Riganti et al., 2005;Riganti et al., 2006;Riganti et al., 2008), and decrease the amount of membrane cholesterol, which also lowers the activity of Pgp/ABCB1 (Kopecka et al., 2011).”
From The association of statins plus LDL receptor‐targeted liposome‐encapsulated doxorubicin increases in vitro drug delivery across blood–brain barrier cells (2012) · cites this paper as Riganti et al., 2005
Citations
Cites
Multidrug resistance in cancer: role of ATP–dependent transporters
Gottesman, M. M., Fojo, T., & Bates, S. E. (2002) · Nature Reviews Cancer · doi:10.1038/nrc706 · Cited by 5,536
Overexpression of a Transporter Gene in a Multidrug-Resistant Human Lung Cancer Cell Line
Cole, S. P. C., Bhardwaj, G., Gerlach, J. H., Mackie, J. E., Grant, C. E., Almquist, K. C., Stewart, A. J., Kurz, E. U., Duncan, A. M. V., & Deeley, R. G. (1992) · Science · doi:10.1126/science.1360704 · Cited by 3,037
Nitric oxide and mitochondrial respiration
Brown, G. C. (1999) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/s0005-2728(99)00025-0 · Cited by 702
Flagged first, then by citations
Research works printed but not linked: 46
- Simon SM, Schindler M. Cell biological mechanisms of multidrug resistance in tumors. Proc Natl Acad Sci U S A 1994; 91: 3497–504. · DOI
- von Bossanyi P, Diete S, Dietzmann K. Kirches MW, Kirches E. Immunohistochemical expression of P-glycoprotein and glutathione S-transferases in cerebral gliomas and response to chemotherapy. Acta Neuropathol (Berl) 1997; 94: 605–11. · DOI
- Thomas H, Coley HM. Overcoming multidrug resistance in cancer: an update on the clinical strategy of inhibiting P-glycoprotein. Cancer Causes Control 2003; 10: 159–65. · DOI · Paper page
- Lind DS, Kontaridis MI, Edwards PD, Josephs MD, Moldawer LL, Copeland EM III. Nitric oxide contributes to Adriamycin's antitumor effect. J Surg Res 1997; 69: 283–7. · DOI
- Aldieri E, Bergandi L, Riganti C, Costamagna C, Bosia A, Ghigo D. Doxorubicin induces an increase of nitric oxide synthesis in rat cardiac cells that is inhibited by iron supplementation. Toxicol Appl Pharmacol 2002; 185: 85–90. · DOI
- Kelm M. Nitric oxide metabolism and breakdown. Biochim Biophys Acta 1999; 1411: 273–89. · DOI · Paper page
- Nathan C, Xie QW. Regulation of biosynthesis of nitric oxide. J Biol Chem 1994; 269: 13725–8. · DOI
- Wink DA, Mitchell JB. Chemical biology of nitric oxide: insights into regulatory, cytotoxic and cytoprotective mechanism of nitric oxide. Free Radic Biol Med 1998; 25: 434–56. · DOI · Paper page
- Magrinat G, Mason SN, Shami PJ, Weinberg JB. Nitric oxide modulation of human leukaemia cell differentiation and gene expression. Blood 1992; 80: 1880–4. · DOI
- Murphy MP. Nitric oxide and cell death. Biochim Biophys Acta 1999; 1411: 401–14. · DOI
- Goldstein LJ. MDR1 expression in solid tumours. Eur J Cancer 1996; 32: 1039–50. · DOI
- Riganti C, Aldieri E, Bergandi L, et al. Crocidolite asbestos inhibits pentose phosphate oxidative pathway and glucose 6-phosphate dehydrogenase activity in human lung epithelial cells. Free Radic Biol Med 2002; 32: 938–49. · DOI
- Kinnula VL, Aalto K, Raivio KO, Walles S, Linnainmaa K. Cytotoxicity of oxidants and asbestos fibers in cultured human mesothelial cells. Free Radic Biol Med 1994; 16: 169–76. · DOI
- Ghigo D, Aldieri E, Todde R, et al. Chloroquine stimulates nitric oxide synthesis in murine, porcine, and human endothelial cells. J Clin Invest 1998; 102: 595–605. · DOI
- Chomczynski P, Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 1987; 162: 156–9. · DOI
- Ueda K, Cardarelli C, Gottesman MM, Pastan I. Expression of a full length cDNA for the human MDR1 gene confers resistance to colchicines, doxorubicine and vinblastine. Proc Natl Acad Sci U S A 1987; 84: 3004–8. · DOI
- Brouillard F, Tondelier D, Edelman A, Baudouin-Legros M. Drug resistance induced by ouabain via the stimulation of MDR1 gene expression in human carcinomatous pulmonary cells. Cancer Res 2001; 62: 1693–8.
- Felley-Bosco E, Bender FC, Courjault-Gautier F, Bron C, Quest AFG. Caveolin-1 down-regulates inducible nitric oxide synthase via the proteasome pathway in human colon carcinoma cells. Proc Natl Acad Sci U S A 2000; 97: 14334–9. · DOI
- Laufs U, La Fata V, Plutzky J, Liao JK. Upregulation of endothelial nitric oxide synthase by HMG CoA reductase inhibitors. Circulation 1998; 97: 1129–35. · DOI
- Endres M, Laufs U, Huang Z, et al. Stroke protection by 3-hydroxy-3-methylglutaryl (HMG)-CoA reductase inhibitors mediated by endothelial nitric oxide synthase. Proc Natl Acad Sci U S A 1998; 95: 8880–5. · DOI
- Pfeifer A, Ruth P, Dostmann W, Sausbier M, Klatt P, Hofmann F. Structure and function of cGMP-dependent protein kinases. Rev Physiol Biochem Pharmacol 1999; 135: 105–49. · DOI
- Grandi M, Geroni C, Giuliani FC. Isolation and characterization of a human colon adenocarcinoma cell line resistant to doxorubicin. Br J Cancer 1986; 54: 515–8. · DOI
- Loe DW, Deeley RG, Cole SPC. Biology of the multidrug resistance-associated protein, MRP. Eur J Cancer 1996; 32: 945–57. · DOI
- Ambdukar SV, Kimchi-Sarfaty C, Sauna ZE, Gottesman MM. P-glycoprotein: from genomics to mechanism. Oncogene 2003; 22: 7468–85. · DOI
- Cole SPC, Sparks KE, Fraser K, et al. Pharmacological characterization of multidrug resistance MRP-transfected human tumor cells. Cancer Res 1994; 54: 5902–10.
- Scotto KW. Transcriptional regulation of ABC drug transporters. Oncogene 2003; 22: 7496–511. · DOI
- Kool M, de Haas M, Scheffer GL, et al. Analysis of expression of cMOAT (MRP2), MRP3, MRP4 and MRP5, homologues of the multidrug resistance-associated protein gene (MRP1), in human cancer cell lines. Cancer Res 1997; 57: 3537–47.
- Kool M, van der Linden M, de Haas M, et al. MRP3, an organic anion transporter able to transport anti-cancer drugs. Proc Natl Acad Sci U S A 1999; 96: 6914–9. · DOI
- Molina y Vedia L, McDonald B, Reep B, et al. Nitric-oxide induced S-nitrosylation of glyceraldehyde 3-phosphate dehydrogenase inhibits enzymatic activity and increase endogenous ADP-ribosylation. J Biol Chem 1992; 267: 24929–32. · DOI
- Stamler JS. Redox signalling: nitrosylation and related target interactions of nitric oxide. Cell 1994; 78: 931–6. · DOI · Paper page
- Stefanelli C, Pignatti C, Tantini B, et al. Nitric oxide can function as either a killer molecule or an antiapoptotic effector in cardiomyocytes. Biochim Biophys Acta 1999; 1450: 406–13. · DOI
- Zagozdzon R, Giermasz A, Golab J, Stoklosa T, Jalili A, Jakobisiak M. The potential antileukemic effects of doxorubicin and interleukin-12 combination are not dependent on nitric oxide production. Cancer Lett 1999; 147: 67–75. · DOI
- Jung ID, Lee JS, Yun SY, et al. Doxorubicin inhibits the production of nitric oxide by colorectal cancer cells. Arch Pharm Res 2002; 25: 691–6. · DOI
- Breuer W, Slotki IN, Ausiello DA, Cabantchik IZ. Induction of multidrug resistance downregulates the expression of CFTR in colon epithelial cells. Am J Physiol 1993; 265: C1711–5. · DOI
- Kunzelmann K, Slotki IN, Klein P, et al. Effects of P-glycoprotein expression on cyclic AMP and volume-activated ion fluxes and conductances in HT-29 colon adenocarcinoma cells. J Cell Physiol 1994; 161: 393–406. · DOI
- Duesberg P, Stindl R, Hehlmann R. Explaining the high mutation rate of cancer cells to drug and multidrug resistance by chromosome re-assortments that are catalyzed by aneuploidy. Proc Natl Acad Sci U S A 2000; 97: 14295–300. · DOI
- Kolyada AY, Fedtsov A, Madias NE. 3-Hydroxy-3-methylglutaryl coenzyme A reductase inhibitors upregulate inducible NO synthase expression and activity in vascular smooth muscle cells. Hypertension 2001; 38: 1024–9. · DOI
- Ikeda U, Shimpo M, Ikeda M, Minota S, Shimada K. Lipophilic statins augment inducible nitric oxide synthase expression in cytokine-stimulated cardiac myocytes. J Cardiovasc Pharmacol 2001; 38: 69–77. · DOI
- Munyappa R, Xu R, Ram JL, Sowers JR. Inhibition of Rho protein stimulates iNOS expression in rat vascular smooth muscle cells. Am J Physiol 2000; 278: H1762–8. · DOI
- Wong WWL, Tan MM, Zhenlei X, Dimitroulakos J, Minden MD, Penn LZ. Cerivastatin triggers tumor-specific apoptosis with higher efficacy than lovastatin. Clin Cancer Res 2001; 7: 2067–75.
- Li X, Liu L, Tupper JC, et al. Inhibition of protein geranylgeranylation and RhoA/RhoA kinase pathway induces apoptosis in human endothelial cells. J Biol Chem 2002; 277: 15309–16. · DOI
- Agarwal B, Bhendwal S, Halmos B, Moss SF, Ramey WG, Holt PR. Lovastatin augments apoptosis induced by chemotherapeutic agents in colon cancer cells. Clin Cancer Res 1999; 5: 2223–9.
- Wang W, Collie-Duguid E, Cassidy J. Cerivastatin enhances the cytotoxicity of 5-fluorouracil on chemosensitive and resistant colorectal cancer cell lines. FEBS Lett 2002; 531: 415–20. · DOI
- Wang E, Casciano CN, Clement RP, Johnson WW. HMG-CoA reductase inhibitors (statins) characterized as direct inhibitors of P-glycoprotein. Pharm Res 2001; 18: 800–6.
- Foster MW, McMahon TJ, Stamler JS. S-nitrosylation in health and disease. Trends Mol Med 2003; 9: 160–7. · DOI
- Di Stasi AM, Mallozzi C, Macchia G, Petrucci TC, Minetti M. Peroxynitrite induces tyrosine nitration and tyrosine phosphorylation of synaptic proteins. J Neurochem 1999; 73: 727–35. · DOI
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Pinzón‐Daza, M., Garzón, R., Couraud, P., Romero, I., Weksler, B., Ghigo, D., Bosia, A., & Riganti, C. (2012) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.2012.02103.x · Cited by 84
Self-citationTransformable Helical Self-Assembly for Cancerous Golgi Apparatus Disruption
Li, R. S., Liu, J., Shi, H., Hu, P. P., Wang, Y., Gao, P. F., Wang, J., Jia, M., Li, H., Li, Y. F., et al. (2021) · Nano Letters · doi:10.1021/acs.nanolett.1c03112 · Cited by 59
Insights into P-Glycoprotein Inhibitors: New Inducers of Immunogenic Cell Death
Kopecka, J., Godel, M., Dei, S., Giampietro, R., Belisario, D. C., Akman, M., Contino, M., Teodori, E., & Riganti, C. (2020) · Cells · doi:10.3390/cells9041033 · Cited by 41
Self-citation
Metadata
- Authors
- Riganti, C., Miraglia, E., Viarisio, D., Costamagna, C., Pescarmona, G., Ghigo, D., & Bosia, A.
- Affiliations
- Department of Genetics, Biology and Biochemistry, University of Torino, and Research Center on Experimental Medicine (CeRMS), Via Santena 5/bis, Turin, Italy
- Venue
- Cancer Research
- Published
- 2005-01-15
- Volume
- 65
- Issue
- 2
- Pages
- 516-525
- ISSN
- 0008-5472
- 1538-7445
- Cited by
- 271
- References
- 3
- Language
- en
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