Advertisement

Environmental Science and Pollution Research

, Volume 25, Issue 36, pp 36545–36554 | Cite as

Heat processing effect of luteolin on anti-metastasis activity of human glioblastoma cells U87

  • Dorra El Gueder
  • Mouna Maatouk
  • Zahar Kalboussi
  • Zaineb Daouefi
  • Hind Chaaban
  • Irina Ioannou
  • Kamel Ghedira
  • Leila Chekir Ghedira
  • José Luis
Research Article
  • 27 Downloads

Abstract

Among the flavonoïds, luteolin is a flavone that has been identified in many plants. It is known for its apoptotic potential with damage to DNA and cell cycle blockage. Many studies have shown that luteolin has anti-oxidant, anti-inflammatory, and anti-cancer activities. However, it is known that heat treatment (boiling, cooking, and treating with microwaves …) can influence the structure of flavonoïds, which often leads to changes in their activities. The present study was conducted to study the effect of heated luteolin on anti-tumor activity of glioblastoma cells U87. Glioblastoma cell viability was evaluated by MTT assay. Adhesion assay was performed on different protein matrices (collagen type 1, vitronectin, fibronectin, and poly-L-lysine); migration assay was determined by modified Boyden chambers and videomicroscopy, and finally, angiogenesis was tested in vitro by capillary network formation on Matrigel™. The results obtained show that the thermal treatment significantly reduces its cytotoxic activity and ability to inhibit cell adhesion to different protein matrices. It was also found that the heat processed significantly reduced the ability of luteolin to inhibit cell migration, cell invasion, and endothelial cell angiogenesis (HMEC-1). This suggests that heat treated luteolin has a lower anti-tumor potential than native luteolin.

Graphical abstract

Keywords

Heat processing Glioblastoma Adhesion Migration Invasion Angiogenesis 

Abbreviations

DNA

Deoxyribonucleic

MTT

Thiazolyl blue tetrazolium bromide

U87

Human glioblastoma cells

HMEC-1

Human microvascular endothelial cells

DMSO

Dimethyl sulfoxide

FBS

Fetal bovine serum

CO2

Carbon dioxide

IC50

Half maximal inhibitory concentration

ECM

Extracellular matrix

BSA

Bovine serum albumin

SDS

Sodium dodecyl sulfate

GBM8401

Human brain glioblastoma cell

LNM35

Human lung cancer cells

MCF-7

Human breast cancer cell

MDAMB231-1833

Human breast cancer cell

PC-3

Human prostate cancer cell

Lut

Luteolin

Lut-T

Heated luteolin

EMEM

Eagle’s minimum essential medium

Notes

Author contributions

Dorra El Gueder was responsible for the conception and design, testing and data acquisition, analysis, and data interpretation and drafted the manuscript.

Mouna Maatouk, Zahar Kalboussi, Dhouafi Zaineb, Hind Chaabane, and Irina Ioannou were involved in drafting the manuscript.

Kamel Ghedira, Leila Chekir Ghedira, and Jose Luis have contribution to conception and revised it critically for important intellectual content.

Funding information

The authors acknowledge the «Ministère Tunisienne de l’Enseignement Supérieur et de la Recherche Scientifique» for the financial support of this study. This research was supported by the Institut National de la Santé et de la Recherche Médicale (INSERM) and by grants from SIRIC (INCa, Institut National du Cancer).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Attoub S, Hassan AH, Vanhoecke B, Iratni R, Takahashi T, Gaben A-M, Bracke M, Awad S, John A, Kamalboor HA (2011) Inhibition of cell survival, invasion, tumor growth and histone deacetylase activity by the dietary flavonoid luteolin in human epithelioid cancer cells. Eur J Pharmacol 651:18–25CrossRefGoogle Scholar
  2. Brusselmans K, Vrolix R, Verhoeven G, Swinnen JV (2005) Induction of cancer cell apoptosis by flavonoids is associated with their ability to inhibit fatty acid synthase activity. J Biol Chem 280:5636–5645CrossRefGoogle Scholar
  3. Buchner N, Krumbein A, Rohn S, Kroh LW (2006) Effect of thermal processing on the flavonols rutin and quercetin. Rapid Commun Mass Spectrom 20:3229–3235CrossRefGoogle Scholar
  4. Chaaban H, Ioannou I, Chebil L, Slimane M, Gerardin C, Paris C, Charbonnel C, Chekir L, Ghoul M (2017a) Effect of heat processing on thermal stability and antioxidant activity of six flavonoids. J Food Process Preserv 41Google Scholar
  5. Chaaban H, Ioannou I, Chebil L, Slimane M, Gérardin C, Paris C, Charbonnel C, Chekir L, Ghoul M (2017b) Effect of heat processing on thermal stability and antioxidant activity of six flavonoids. J Food Process PreservGoogle Scholar
  6. Chaaban H, Ioannou I, Chebil L, Slimane M, Gérardin C, Paris C, Charbonnel C, Chekir L, Ghoul M (2017c) Effect of heat processing on thermal stability and antioxidant activity of six flavonoids. J Food Process Preserv 41:e13203Google Scholar
  7. Chabner BA, Roberts TG (2005) Chemotherapy and the war on cancer. Nat Rev Cancer 5:65–72CrossRefGoogle Scholar
  8. Crozier A, Lean ME, McDonald MS, Black C (1997) Quantitative analysis of the flavonoid content of commercial tomatoes, onions, lettuce, and celery. J Agric Food Chem 45:590–595CrossRefGoogle Scholar
  9. Dall’Acqua S, Miolo G, Innocenti G, Caffieri S (2012) The photodegradation of quercetin: relation to oxidation. Molecules 17:8898–8907CrossRefGoogle Scholar
  10. Delamarre E, Taboubi S, Mathieu S, Bérenguer C, Rigot V, Lissitzky J-C, Figarella-Branger D, Ouafik LH, Luis J (2009) Expression of integrin α6β1 enhances tumorigenesis in glioma cells. Am J Pathol 175:844–855CrossRefGoogle Scholar
  11. Dietrych-Szostak D, Oleszek W (1999) Effect of processing on the flavonoid content in buckwheat (Fagopyrum e sculentum Möench) grain. J Agric Food Chem 47:4384–4387Google Scholar
  12. Goodenberger ML, Jenkins RB (2012) Genetics of adult glioma. Cancer Genet 205:613–621CrossRefGoogle Scholar
  13. Hartmann C, Hentschel B, Tatagiba M, Schramm J, Schnell O, Seidel C, Stein R, Reifenberger G, Pietsch T, von Deimling A (2011) Molecular markers in low-grade gliomas: predictive or prognostic? Clin Cancer Res 17:4588–4599CrossRefGoogle Scholar
  14. Jeon Y-W, Suh YJ (2013) Synergistic apoptotic effect of celecoxib and luteolin on breast cancer cells. Oncol Rep 29:819–825CrossRefGoogle Scholar
  15. Ko W, Kang T, Lee S, Kim Y, Lee B (2002) Effects of luteolin on the inhibition of proliferation and induction of apoptosis in human myeloid leukaemia cells. Phytother Res 16:295–298CrossRefGoogle Scholar
  16. Kuti JO, Konuru HB (2004) Antioxidant capacity and phenolic content in leaf extracts of tree spinach (Cnidoscolus spp.). J Agric Food Chem 52:117–121CrossRefGoogle Scholar
  17. Lee L-T, Huang Y-T, Hwang J-J, Lee P, Ke F-C, Nair MP, Kanadaswam C, Lee M-T (2001) Blockade of the epidermal growth factor receptor tyrosine kinase activity by quercetin and luteolin leads to growth inhibition and apoptosis of pancreatic tumor cells. Anticancer Res 22:1615–1627Google Scholar
  18. Leung HW-C, Wu C-H, Lin C-H, Lee H-Z (2005) Luteolin induced DNA damage leading to human lung squamous carcinoma CH27 cell apoptosis. Eur J Pharmacol 508:77–83CrossRefGoogle Scholar
  19. Lin Y, Shi R, Wang X, Shen H-M (2008) Luteolin, a flavonoid with potential for cancer prevention and therapy. Curr Cancer Drug Targets 8:634–646CrossRefGoogle Scholar
  20. Lopez-Lazaro M (2009) Distribution and biological activities of the flavonoid luteolin. Mini Rev Med Chem 9:31–59CrossRefGoogle Scholar
  21. Maatouk M, Elgueder D, Mustapha N, Chaaban H, Bzéouich IM, Loannou I, Kilani S, Ghoul M, Ghedira K, Chekir-Ghedira L (2016) Effect of heated naringenin on immunomodulatory properties and cellular antioxidant activity. Cell Stress Chaperones 21:1101–1109CrossRefGoogle Scholar
  22. Makris DP, Rossiter JT (2000) Heat-induced, metal-catalyzed oxidative degradation of quercetin and rutin (quercetin 3-O-rhamnosylglucoside) in aqueous model systems. J Agric Food Chem 48:3830–3838Google Scholar
  23. Mamelak AN, Jacoby DB (2007) Targeted delivery of antitumoral therapy to glioma and other malignancies with synthetic chlorotoxin (TM-601). Expert Opin Drug Deliv 4:175–186CrossRefGoogle Scholar
  24. Mokdad-Bzeouich I, Kovacic H, Ghedira K, Chebil L, Ghoul M, Chekir-Ghedira L, Luis J (2016) Esculin and its oligomer fractions inhibit adhesion and migration of U87 glioblastoma cells and in vitro angiogenesis. Tumor Biol 37:3657–3664CrossRefGoogle Scholar
  25. Monasterio A, Urdaci MC, Pinchuk IV, Lopez-Moratalla N, Martinez-Irujo JJ (2004) Flavonoids induce apoptosis in human leukemia U937 cells through caspase-and caspase-calpain-dependent pathways. Nutr Cancer 50:90–100CrossRefGoogle Scholar
  26. Morgan LL (2015) The epidemiology of glioma in adults: a “state of the science” review. Neuro-oncology, nou358Google Scholar
  27. Morjen M, Kallech-Ziri O, Bazaa A, Othman H, Mabrouk K, Zouari-Kessentini R, Sanz L, Calvete JJ, Srairi-Abid N, El Ayeb M (2013) PIVL, a new serine protease inhibitor from Macrovipera lebetina transmediterranea venom, impairs motility of human glioblastoma cells. Matrix Biol 32:52–62CrossRefGoogle Scholar
  28. Naber HP, Wiercinska E, ten Dijke P, van Laar T (2011) Spheroid assay to measure TGF-β-induced invasion. J Vis Exp:e3337Google Scholar
  29. Nam N-H, Kim Y, You Y-J, Hong D-H, Kim H-M, Ahn B-Z (2002) Preliminary structure–antiangiogenic activity relationships of 4-senecioyloxymethyl-6, 7-dimethoxycoumarin. Bioorg Med Chem Lett 12:2345–2348CrossRefGoogle Scholar
  30. Nicoli M, Anese M, Parpinel M (1999) Influence of processing on the antioxidant properties of fruit and vegetables. Trends Food Sci Technol 10:94–100Google Scholar
  31. Parise LV, Lee JW, Juliano RL (2000) New aspects of integrin signaling in cancer. Seminars in cancer biology. Elsevier, pp 407–414Google Scholar
  32. Pilorget A, Conesa M, Sarray S, Michaud-Levesque J, Daoud S, Kim KS, Demeule M, Marvaldi J, El Ayeb M, Marrakchi N (2007) Lebectin, a Macrovipera lebetina venom-derived C-type lectin, inhibits angiogenesis both in vitro and in vivo. J Cell Physiol 211:307–315CrossRefGoogle Scholar
  33. Pourroy B, Honoré S, Pasquier E, Bourgarel-Rey V, Kruczynski A, Briand C, Braguer D (2006) Antiangiogenic concentrations of vinflunine increase the interphase microtubule dynamics and decrease the motility of endothelial cells. Cancer Res 66:3256–3263CrossRefGoogle Scholar
  34. Ramešová Š, Sokolová R, Tarábek J, Degano I (2013) The oxidation of luteolin, the natural flavonoid dye. Electrochim Acta 110:646–654CrossRefGoogle Scholar
  35. Rigot V, Lehmann M, André F, Daemi N, Marvaldi J, Luis J (1998) Integrin ligation and PKC activation are required for migration of colon carcinoma cells. J Cell Sci 111:3119–3127Google Scholar
  36. Rohn S, Buchner N, Driemel G, Rauser M, Kroh LW (2007) Thermal degradation of onion quercetin glucosides under roasting conditions. J Agric Food Chem 55:1568–1573Google Scholar
  37. Ross JA, Kasum CM (2002) Dietary flavonoids: bioavailability, metabolic effects, and safety. Annu Rev Nutr 22:19–34Google Scholar
  38. Ruan J-S, Liu Y-P, Zhang L, Yan L-G, Fan F-T, Shen C-S, Wang A-Y, Zheng S-Z, Wang S-M, Lu Y (2012) Luteolin reduces the invasive potential of malignant melanoma cells by targeting β3 integrin and the epithelial-mesenchymal transition. Acta Pharmacol Sin 33:1325–1331CrossRefGoogle Scholar
  39. Sadok A, Bourgarel-Rey V, Gattacceca F, Penel C, Lehmann M, Kovacic H (2008) Nox1-dependent superoxide production controls colon adenocarcinoma cell migration. Biochim Biophys Acta 1783:23–33CrossRefGoogle Scholar
  40. Seguin L, Desgrosellier JS, Weis SM, Cheresh DA (2015) Integrins and cancer: regulators of cancer stemness, metastasis, and drug resistance. Trends Cell Biol 25:234–240CrossRefGoogle Scholar
  41. Sehmer EA, Hall G, Greenberg DC, O'Hara C, Wallingford SC, Wright KA, Green AC (2014) Incidence of glioma in a northwestern region of England, 2006–2010. Neuro-oncology, not301Google Scholar
  42. Silva JP, Gomes AC, Coutinho OP (2008) Oxidative DNA damage protection and repair by polyphenolic compounds in PC12 cells. Eur J Pharmacol 601:50–60CrossRefGoogle Scholar
  43. Sottile J (2004) Regulation of angiogenesis by extracellular matrix. Biochimica et Biophysica Acta (BBA)-Reviews on Cancer 1654:13–22CrossRefGoogle Scholar
  44. Tsai Y-D, Chen H-J, Hsu H-F, Lu K, Liang C-L, Liliang P-C, Wang K-W, Wang H-K, Wang C-P, Houng J-Y (2013) Luteolin inhibits proliferation of human glioblastoma cells via induction of cell cycle arrest and apoptosis. J Taiwan Inst Chem Eng 44:837–845CrossRefGoogle Scholar
  45. Vigneswaran K, Neill S, Hadjipanayis CG (2015) Beyond the World Health Organization grading of infiltrating gliomas: advances in the molecular genetics of glioma classification. Ann Transl Med 3Google Scholar
  46. Wiercinska E, Naber HP, Pardali E, van der Pluijm G, van Dam H, Ten Dijke P (2011) The TGF-β/Smad pathway induces breast cancer cell invasion through the up-regulation of matrix metalloproteinase 2 and 9 in a spheroid invasion model system. Breast Cancer Res Treat 128:657–666CrossRefGoogle Scholar
  47. Yeh S, Ho J, Lui C, Huang Y, Hsiung C, Huang E (2014) Treatment outcomes and prognostic factors in patients with supratentorial low-grade gliomas. Br J RadiolGoogle Scholar
  48. Yin F, Giuliano AE, Van Herle AJ (1999) Growth inhibitory effects of flavonoids in human thyroid cancer cell lines. Thyroid 9:369–376CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Dorra El Gueder
    • 1
    • 2
  • Mouna Maatouk
    • 2
  • Zahar Kalboussi
    • 2
  • Zaineb Daouefi
    • 1
    • 2
  • Hind Chaaban
    • 3
  • Irina Ioannou
    • 3
  • Kamel Ghedira
    • 4
  • Leila Chekir Ghedira
    • 2
  • José Luis
    • 5
  1. 1.Faculty of Sciences of TunisUniversity of Tunis El ManarTunisTunisia
  2. 2.Faculty of Dental Medicine, Unity of Bioactive and Natural Substances and Biotechnology UR17ES49University of MonastirMonastirTunisia
  3. 3.National School of Agronomy and Food Industries, Laboratory of Bimolecular EngineeringNational Polytechnics Institute of Lorraine ENSAIA-INPLNancyFrance
  4. 4.Faculty of Pharmacy, Department of Pharmaceutical SciencesUniversity of MonastirMonastirTunisia
  5. 5.CNRS, Institut de NeurophysiopathologieAix Marseille UniversityMarseilleFrance

Personalised recommendations