[go: up one dir, main page]
Skip to main content

Advertisement

SpringerLink
Log in

Pro-inflammatory cytokines interleukin-1 beta, interleukin 6, and tumor necrosis factor-alpha alter the expression and function of ABCG2 in cervix and gastric cancer cells

  • Published:
Molecular and Cellular Biochemistry Aims and scope Submit manuscript

Abstract

The ATP-binding cassette sub-family G member 2 (ABCG2) is implicated as a member of multidrug resistant proteins in tumors, mediating efflux of a wide spectrum of anticancer drugs. Pro-inflammatory cytokines, which are present within the micro-environment of tumors and inflammation, are able to modulate the expressions and activities of different drug transporters. This study was aimed to evaluate the short-term (72-h treatment) effects of interleukin-1β (IL-1β), tumor necrosis factor-α (TNF-α), and interleukin-6 (IL-6) on the expression and function of ABCG2 in cervix carcinoma and gastric cancer cells. Effects of pro-inflammatory cytokines on mRNA, protein expression, and function of ABCG2 were studied using real time RT-PCR and flow cytometry methods, respectively. HeLa cells treated with IL-1β, IL-6, or TNF-α showed decrements in ABCG2 mRNA levels without any changes in protein expression and function of ABCG2. IL-6 and TNF-α had no effects on mRNA, protein expression, and function of ABCG2 in EPG85-257 cells. Although IL-1β did not alter ABCG2 at mRNA or protein levels in EPG85-257 cells, it augmented function of ABCG2 in these cells. Mitoxantrone accumulation was also amplified in IL-1β-, IL-6- or TNF-α-treated HeLa cells and in IL-1β-treated EPG85-257 cells. In conclusion, pro-inflammatory cytokines were able to modulate the expression of ABCG2 at transcriptional and post-transcriptional levels in human cervix and gastric cancer cells.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Teodori E, Dei S, Scapecchi S, Gualtieri F (2002) The medicinal chemistry of multidrug resistance (MDR) reversing drugs. Farmaco 57:385–415

    Article  PubMed  CAS  Google Scholar 

  2. Choi CH (2005) ABC transporters as multidrug resistance mechanisms and the development of chemosensitizers for their reversal. Cancer Cell Int 5:30

    Article  PubMed  Google Scholar 

  3. Huls M, Russel FG, Masereeuw R (2009) The role of ATP binding cassette transporters in tissue defense and organ regeneration. J Pharmacol Exp Ther 328:3–9

    Article  PubMed  CAS  Google Scholar 

  4. Sarkadi B, Ozvegy-Laczka C, Nemet K, Varadi A (2004) ABCG2:a transporter for all seasons. FEBS Lett 567:116–120

    Article  PubMed  CAS  Google Scholar 

  5. Maliepaard M, Scheffer GL, Faneyte IF, van Gastelen MA, Pijnenborg AC, Schinkel AH, van De Vijver MJ, Scheper RJ, Schellens JH (2001) Subcellular localization and distribution of the breast cancer resistance protein transporter in normal human tissues. Cancer Res 61:3458–3464

    PubMed  CAS  Google Scholar 

  6. Diestra JE, Scheffer GL, Catala I, Maliepaard M, Schellens JH, Scheper RJ, Germa-Lluch JR, Izquierdo MA (2002) Frequent expression of the multi-drug resistance-associated protein BCRP/MXR/ABCP/ABCG2 in human tumours detected by the BXP-21 monoclonal antibody in paraffin-embedded material. J Pathol 198:213–219

    Article  PubMed  CAS  Google Scholar 

  7. Ross DD, Karp JE, Chen TT, Doyle LA (2000) Expression of breast cancer resistance protein in blast cells from patients with acute leukemia. Blood 96:365–368

    PubMed  CAS  Google Scholar 

  8. Mao Q, Unadkat JD (2005) Role of the breast cancer resistance protein (ABCG2) in drug transport. Aaps J 7:E118–E133

    Article  PubMed  CAS  Google Scholar 

  9. Allen JD, Schinkel AH (2002) Multidrug resistance and pharmacological protection mediated by the breast cancer resistance protein (BCRP/ABCG2). Mol Cancer Ther 1:427–434

    Article  PubMed  CAS  Google Scholar 

  10. Ho EA, Piquette-Miller M (2006) Regulation of multidrug resistance by pro-inflammatory cytokines. Curr Cancer Drug Targets 6:295–311

    Article  PubMed  CAS  Google Scholar 

  11. Philip M, Rowley DA, Schreiber H (2004) Inflammation as a tumor promoter in cancer induction. Semin Cancer Biol 14:433–439

    Article  PubMed  CAS  Google Scholar 

  12. Haddad JJ (2002) Cytokines and related receptor-mediated signaling pathways. Biochem Biophys Res Commun 297:700–713

    Article  PubMed  CAS  Google Scholar 

  13. Dinarello CA (2000) Proinflammatory cytokines. Chest 118:503–508

    Article  PubMed  CAS  Google Scholar 

  14. Caruso C, Lio D, Cavallone L, Franceschi C (2004) Aging, longevity, inflammation, and cancer. Ann N Y Acad Sci 1028:1–13

    Article  PubMed  CAS  Google Scholar 

  15. Wilson J, Balkwill F (2002) The role of cytokines in the epithelial cancer microenvironment. Semin Cancer Biol 12:113–120

    Article  PubMed  CAS  Google Scholar 

  16. McRae MP, Brouwer KL, Kashuba AD (2003) Cytokine regulation of P-glycoprotein. Drug Metab Rev 35:19–33

    Article  PubMed  CAS  Google Scholar 

  17. Assenat E, Gerbal-chaloin S, Maurel P, Vilarem MJ, Pascussi JM (2006) Is nuclear factor kappa-B the missing link between inflammation, cancer and alteration in hepatic drug metabolism in patients with cancer? Eur J Cancer 42:785–792

    Article  PubMed  CAS  Google Scholar 

  18. Vee ML, Lecureur V, Stieger B, Fardel O (2009) Regulation of drug transporter expression in human hepatocytes exposed to the proinflammatory cytokines tumor necrosis factor-alpha or interleukin-6. Drug Metab Dispos 37:685–693

    Article  PubMed  Google Scholar 

  19. Malekshah OM, Bahrami AR, Afshari JT, Mosaffa F, Behravan J (2011) Correlation between PXR and ABCG2 patterns of mRNA expression in a MCF7 breast carcinoma cell derivative upon induction by proinflammatory cytokines. DNA Cell Biol 30:25–31

    Article  PubMed  CAS  Google Scholar 

  20. Mosaffa F, Lage H, Afshari JT, Behravan J (2009) Interleukin-1 beta and tumor necrosis factor-alpha increase ABCG2 expression in MCF-7 breast carcinoma cell line and its mitoxantrone-resistant derivative, MCF-7/MX. Inflamm Res 58:669–676

    Article  PubMed  CAS  Google Scholar 

  21. Tahara E (2008) Abnormal growth factor/cytokine network in gastric cancer. Cancer Microenviron 1:85–91. doi:10.1007/s12307-008-0008-1

    Article  PubMed  Google Scholar 

  22. Munagala R, Nagarajan B (2008) Alterations in cytokine levels in cervical carcinoma patients through radiation therapy. Current Science 94:1292–1296

    CAS  Google Scholar 

  23. Hilders CG, Houbiers JG, van Ravenswaay Claasen HH, Veldhuizen RW, Fleuren GJ (1993) Association between HLA-expression and infiltration of immune cells in cervical carcinoma. Lab Invest 69:651–659

    PubMed  CAS  Google Scholar 

  24. Minderman H, Suvannasankha A, O’Loughlin KL, Scheffer GL, Scheper RJ, Robey RW, Baer MR (2002) Flow cytometric analysis of breast cancer resistance protein expression and function. Cytometry 48:59–65

    Article  PubMed  CAS  Google Scholar 

  25. Elahian F, Kalalinia F, Behravan J (2009) Dexamethasone downregulates BCRP mRNA and protein expression in breast cancer cell lines. Oncol Res 18:9–15

    Article  PubMed  CAS  Google Scholar 

  26. Kalalinia F, Elahian F, Behravan J (2010) 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

    Article  PubMed  Google Scholar 

  27. 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

    Article  PubMed  CAS  Google Scholar 

  28. Slaviero KA, Clarke SJ, Rivory LP (2003) Inflammatory response: an unrecognised source of variability in the pharmacokinetics and pharmacodynamics of cancer chemotherapy. Lancet Oncol 4:224–232

    Article  PubMed  CAS  Google Scholar 

  29. Evseenko DA, Paxton JW, Keelan JA (2007) Independent regulation of apical and basolateral drug transporter expression and function in placental trophoblasts by cytokines, steroids, and growth factors. Drug Metab Dispos 35:595–601

    Article  PubMed  CAS  Google Scholar 

  30. Englund G, Jacobson A, Rorsman F, Artursson P, Kindmark A, Ronnblom A (2007) Efflux transporters in ulcerative colitis: decreased expression of BCRP (ABCG2) and Pgp (ABCB1). Inflamm Bowel Dis 13:291–297

    Article  PubMed  Google Scholar 

  31. Poller B, Drewe J, Krahenbuhl S, Huwyler J, Gutmann H (2010) Regulation of BCRP (ABCG2) and P-glycoprotein (ABCB1) by cytokines in a model of the human blood-brain barrier. Cell Mol Neurobiol 30:63–70

    Article  PubMed  CAS  Google Scholar 

  32. von Wedel-Parlow M, Wolte P, Galla HJ (2009) Regulation of major efflux transporters under inflammatory conditions at the blood-brain barrier in vitro. J Neurochem 111:111–118

    Article  Google Scholar 

  33. Takara K, Obata Y, Yoshikawa E, Kitada N, Sakaeda T, Ohnishi N, Yokoyama T (2006) Molecular changes to HeLa cells on continuous exposure to cisplatin or paclitaxel. Cancer Chemother Pharmacol 58:785–793

    Article  PubMed  CAS  Google Scholar 

  34. Yasumoto K, Okamoto S, Mukaida N, Murakami S, Mai M, Matsushima K (1992) Tumor necrosis factor alpha and interferon gamma synergistically induce interleukin 8 production in a human gastric cancer cell line through acting concurrently on AP-1 and NF-kB-like binding sites of the interleukin 8 gene. J Biol Chem 267:22506–22511

    PubMed  CAS  Google Scholar 

  35. Lee G, Piquette-Miller M (2001) Influence of IL-6 on MDR and MRP-mediated multidrug resistance in human hepatoma cells. Can J Physiol Pharmacol 79:876–884

    Article  PubMed  CAS  Google Scholar 

  36. Kaszubiac A (2007) Adenoviraler Transfer von anti-MDR1 shRNAs Implikationen für die Gentherapie multidrug-resistenter Tumoren. Ph.D.Thesis

  37. Stein U, Walther W, Laurencot CM, Scheffer GL, Scheper RJ, Shoemaker RH (1997) Tumor necrosis factor-alpha and expression of the multidrug resistance-associated genes LRP and MRP. J Natl Cancer Inst 89:807–813

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgment

The authors thank the Research Council of Mashhad University of Medical Sciences for providing financial support of this project.

Author information

Authors and Affiliations

  1. Biotechnology Research Centers, Mashhad University of Medical Sciences, Mashhad, Iran

    Fatemeh Mosaffa, Fatemeh Kalalinia & Javad Behravan

  2. Department of Pharmaceutical Biotechnology, School of Pharmacy, Mashhad University of Medical Sciences, P.O. Box: 91775-1365, Mashhad, IRAN

    Fatemeh Mosaffa, Fatemeh Kalalinia & Javad Behravan

  3. Institute of Pathology, Charite′ Campus Mitte, Humboldt University, 10117, Berlin, Germany

    Herman Lage

  4. Immunology Research Centers, Mashhad University of Medical Sciences, Mashhad, Iran

    Jalil Tavakol Afshari

Authors
  1. Fatemeh Mosaffa
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Fatemeh Kalalinia
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Herman Lage
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jalil Tavakol Afshari
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Javad Behravan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Fatemeh Mosaffa or Javad Behravan.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mosaffa, F., Kalalinia, F., Lage, H. et al. Pro-inflammatory cytokines interleukin-1 beta, interleukin 6, and tumor necrosis factor-alpha alter the expression and function of ABCG2 in cervix and gastric cancer cells. Mol Cell Biochem 363, 385–393 (2012). https://doi.org/10.1007/s11010-011-1191-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11010-011-1191-9

Keywords

Search

Navigation