Valdecoxib Recovers the Lipid Composition,Order and Dynamics in Colon Cancer Cell Lines Independent of COX-2 Expression: An ATR-FTIR Spectroscopy Study
Restricted accessResearch articleFirst published online January, 2017
Valdecoxib Recovers the Lipid Composition,Order and Dynamics in Colon Cancer Cell Lines Independent of COX-2 Expression: An ATR-FTIR Spectroscopy Study
Prostanoids play an important role in a variety of physiological and pathophysiological processes including inflammation and cancer. The rate-limiting step in the prostanoid biosynthesis pathway is catalyzed by cyclooxygenases (COXs). Aberrant expression of the inducible isoform COX-2 plays a significant role in colon cancer initiation and progression. In this study, we have hypothesized that COX-2 specific inhibitors such as Valdecoxib (VLX), being highly hydrophobic, may alter biophysical properties of cellular lipids. In this study, COX-2 expressing (HT29) and COX-2 non-expressing (SW620) colon cancer cell lines were treated with VLX and examined using attenuated total reflection infrared spectroscopy. The results revealed that VLX treatment decreased lipid fluidity in the cells irrespective of COX-2 expression status and affected order parameters of the lipids in both cell lines. Cluster analysis also indicated that the spectral differences between the two cell lines are profound and could be successfully differentiated. Valdecoxib treatment could enhance the composition, order and dynamics of the lipids of colon cancer cells independently of its COX-2 inhibitory mechanism. Valdecoxib has therapeutic effects upon colon cancer, therefore it can be used as an adjuvant and/or chemopreventive agent for colon cancer.
Vukobrat-BijedicZ.Husic-SelimovicA.SoficA.BijedicN.GogovB.DjuranA.RedzepovicA.SarayA.BjelogrlicI.“The Application of Current Diagnostic Protocols of Patients with Colon Cancer in Preparation for Therapy”. Acta Inform. Med2012; 20(4): 238–241.
3.
ShadanS.MohammadA.R.SarkarF.H.“The Complexities of Epidemiology and Prevention of Gastrointestinal Cancers”. Int. J. Mol. Sci2012; 13(10): 12556–12572.
CathcartM.C.O’ByrnebK.J.ReynoldsaJ.V.SullivanaJ.O.PidgeonG.P.“COX-Derived Prostanoid Pathways in Gastrointestinal Cancer Development and Progression: Novel Targets for Prevention and Intervention”. Biochim. Biophys. Acta2012; 1825(1): 49–63.
6.
PairetM.EngelhardtG.“Distinct Isoforms (COX-1 and COX-2) of Cyclooxygenase: Possible Physiological and Therapeutic Implications”. Fundam. Clin. Pharmacol1996; 10(1): 1–17.
7.
EsserR.BerryC.DuZ.DawsonJ.FoxA.FujimotoR.A.HastonW.KimbleE.F.KoehlerJ.PeppardJ.QuadrosE.QuintavallaJ.ToscanoK.UrbanL.van DuzerJ.ZhangX.ZhouS.MarshallP.J.“Preclinical Pharmacology of Lumiracoxib: A Novel Selective Inhibitor of Cyclooxygenase-2”. Brit. J. Pharma2005; 144(4): 538–550.
8.
BottingR.M.“Cyclooxygenase: Past, Present and Future”. J. Therm. Biol2006; 31(1–2): 208–219.
9.
HydeC.A.C.MissailidisS.“Inhibition of Arachidonic Acid Metabolism and its Implication on Cell Proliferation and Tumour-Angiogenesis”. Int. Immunopharmacol2009; 9(6): 701–715.
10.
H.E. Vonkeman, M.A. van de Laar. “Nonsteroidal Anti-Inflammatory Drugs: Adverse Effects and Their Prevention”. 2010. 39(4): 294–312.
11.
JendrossekV.“Targeting Apoptosis Pathways by Celecoxib in Cancer”. Cancer Lett2013; 332(2): 313–324.
12.
HunterD.J.AtukoralaI.“Valdecoxib: The Rise and Fall of a COX-2 Inhibitor”. Expert Opin. Pharmaco2013; 14(8): 1077–1086.
13.
HarrisR.E.“Cyclooxygenase-2 (Cox-2) Blockade in the Chemoprevention of Cancers of the Colon, Breast, Prostate, and Lung”. Inflammopharmacology2009; 17(2): 55–67.
14.
AshokV.DashC.RohanT.E.SprafkaJ.M.TerryP.D.“Selective Cyclooxygenase-2 (COX-2) Inhibitors and Breast Cancer Risk”. Breast2011; 20(1): 66–70.
15.
KauJ.VaishV.SanyalS.N.“COX-2 as a Molecular Target of Colon Cancer Chemoprevention: Promise and Reality”. Biomed. Aging Pathol2012; 2: 67–72.
16.
BoccaC.BozzoF.IevolellaM.MigliettaA.“A Novel Nitro-Oxy Substituted Analogue of Rofecoxib Reduces Human Colon Cancer Cell Growth”. Mol. Cell Biochem2012; 361(1–2): 105–110.
HoodW.F.GierseJ.K.IsaksonP.C.KieferJ.R.KurumbailR.G.SeibertK.MonahanJ.B.“Characterization of Celecoxib and Valdecoxib Binding to Cyclooxygenase”. Mol Pharmacol2003; 63(4): 870–877.
19.
SadeA.BanerjeeS.SevercanF.“Concentration-Dependent Differing Actions of the Nonsteroidal Anti-Inflammatory Drug, Celecoxib, in Distearoyl Phosphatidylcholine Multilamellar Vesicles”. J. Liposome Res2010; 20(2): 168–177.
20.
SadeA.TuncayS.CimenI.SevercanF.BanerjeeS.“Celecoxib Reduces Fluidity and Decreases Metastatic Potential of Colon Cancer Cell Lines Irrespective of COX-2 Expression”. Biosci. Rep2012; 23(1): 35–44.
21.
CheungT.K.TrevisanJ.KellyG.J.AshtonM.K.StringfellowF.H.TaylorE.S.SinghN.M.HirschL.M.P.MartinL.F.“Fourier-Transform Infrared Spectroscopy Discriminates a Spectral Signature of Endometriosis Independent of Inter-Individual Variation”. Analyst2011; 136(10): 2047–2055.
22.
LimasaleY.D.P.TezcanerA.OzenC.KeskinD.BanerjeeS.“Epidermal Growth Factor Receptor-Targeted Immunoliposomes for Delivery of Celecoxib to Cancer Cells”. Int. J. Pharm2015; 479(2): 364–373.
23.
GaigneauxA.RuysschaertJ.M.GoormaghtighE.“Cell Discrimination by Attenuated Total Reflection–Fourier Transform Infrared Spectroscopy: The Impact of Preprocessing of Spectra”. Appl. Spectrosc2006; 60(9): 1022–1028.
24.
OzekN.TunaS.ErsonE.SevercanF.“Characterization of microRNA-125b Expression in MCF7 Breast Cancer Cells by ATR-FTIR Spectroscopy”. Analyst2010; 135(12): 3094–3102.
25.
GasperR.MijatovicT.BenardA.DerenneA.KissR.GoormaghtighE.“FTIR Spectral Signature of the Effect of Cardiotonic Steroids with Antitumoral Properties”. Biochim. Biophys. Acta2010; 1802(11): 1087–1094.
26.
GaigneauxA.RuysschaertJ.M.GoormaghtighE.“Infrared Spectroscopy as a Tool for Discrimination Between Sensitive and Multiresistant K562 Cells”. Eur. J. Biochem2002; 269(7): 1968–1973.
27.
KorkmazF.SevercanF.“Effect of Progesterone on DPPC Membrane: Evidence for Lateral Phase Separation and Inverse Action in Lipid Dynamics”. Arch. Biochem. Biophys2005; 440(2): 141–147.
28.
LopezG.F.“Infrared Spectroscopic Study of the Interaction of Diacylglycerol with Phosphatidylserine in the Presence of Calcium”. BBA Lipid. Lipid. Met1993; 1169(3): 264–272.
29.
SevercanF.KazanciN.ZorluF.“Tamoxifen Increases Membrane Fluidity at High Concentrations”. Biosci Rep2000; 20(3): 177–184.
30.
SevercanF.SahinI.KazanciN.“Melatonin Strongly Interacts with Zwitterionic Model Membranes – Evidence from Fourier Transform Infrared Spectroscopy and Differential Scanning Calorimetry”. Biochim. Biophys. Acta2005; 1;1668(2): 215–222.
31.
VanginkelG.VanlangenH.LevineY.K.“The Membrane Fluidity Concept Revisited by Polarized Fluorescence Spectroscopy on Different Model Membranes Containing Unsaturated Lipids and Sterols”. Biochimie1989; 71(1): 23–32.
32.
RandolphT.W.“Scale-Based Normalization of Spectral Data”. Cancer Biomark2006; 2(3–4): 135–144.
33.
HelmD.LabischinskiH.SchallehnG.NaumannD.“Classification and Identification of Bacteria by Fourier-Transform Infrared Spectroscopy”. J. Gen. Microbiol1991; 137(1): 69–79.
34.
SevercanF.BozkurtO.GurbanovR.GorguluG.“FT-IR Spectroscopy in Diagnosis of Diabetes in Rat Animal Model”. J. Biophotonics2010; 3(8–9): 621–631.
35.
LaschP.HaenschW.NaumannD.DiemM.“Imaging of Colorectal Adenocarcinoma using FT-IR Microspectroscopy and Cluster Analysis”. BBA – Mol. Basis Dis2004; 1688(2): 176–186.
36.
I. Rehman, Z. Movasaghi, S. Rehman. “Vibrational Spectroscopy for Tissue Analysis”. In: Rehman I, Movasaghi Z, Rehman S. (Eds.) FT-IR and Raman Characteristic Peak Frequencies in Biological Studies, New York, USA: CRC Press, Taylor and Francis Group. (2012). pp. 213–294.
37.
KansizM.HeraudP.WoodB.BurdenF.BeardallJ.McNaughtonD.“Fourier Transform Infrared Microspectroscopy and Chemometrics as a Tool for the Discrimination of Cyanobacterial Strains”. Phytochemistry1999; 52(3): 407–417.
38.
GaripS.GozenA.G.SevercanF.“Use of Fourier Transform Infrared Spectroscopy for Rapid Comparative Analysis of Bacillus and Micrococcus Isolates”. Food Chem2009; 113(4): 1301–1307.
39.
SevercanF.GorguluG.GorguluS.T.GurayT.“Rapid Monitoring of Diabetes-Induced Lipid Peroxidation by Fourier Transform Infrared Spectroscopy: Evidence from Rat Liver Microsomal Membranes”. Anal. Biochem2005; 339(1): 36–40.
40.
LiuK.BoseR.MantschH.“Infrared Spectroscopic Study of Diabetic Platelets”. Vib. Spectrosc2002; 28(1): 131–136.
41.
LevineS.M.WetzelD.L.“Chemical Analysis of Multiple Sclerosis Lesions by FT-IR Microspectroscopy”. Free Radical Biol. Med1998; 25(1): 33–41.
42.
EnayatS.CeyhanM.S.BaşaranA.A.GürselM.BanerjeeS.“Anticarcinogenic Effects of the Ethanolic Extract of Salix aegyptiaca in Colon Cancer Cells: Involvement of Akt/PKB and MAPK Pathways”. Nutr. Cancer2013; 65(7): 1045–1058.
43.
YajimaD.MotaniH.HayakawaM.SatoY.SatoK.IwaseH.“The Relationship Between Cell Membrane Damage and Lipid Peroxidation Under the Condition of Hypoxia-Reoxygenation: Analysis of the Mechanism Using Antioxidants and Electron Transport Inhibitors”. Cell Biochem. Funct2009; 27(6): 338–343.
44.
Wong-ekkabutJ.XuZ.TriampoW.TangI.M.TielemanD.P.MonticelliL.“Effect of Lipid Peroxidation on the Properties of Lipid Bilayers: A Molecular Dynamics Study”. Biophys. J2007; 93(12): 4225–4236.
45.
R. Lewis, R.N. Mc Elhaney, H.H. Mantsch, D. Chapman, editors. Infrared Spectroscopy of Biomolecules. New York: Wiley-Liss, 1996. Pp. 159–202.
46.
CakmakG.SevercanF.ToganI.“17B-Estradiol Induced Compositional, Structural and Functional Changes on Rainbow Trout Liver, Revealed by FTIR Spectroscopy: A Comparative Study with Nonylphenol”. Aqua. Toxicol2006; 77(1): 53–63.
47.
SevercanF.“Vitamin E Decreases the Order of the Phospholipid Model Membranes in the Gel Phase: An FTIR Study”. Biosci. Rep1997; 17(2): 231–235.
48.
NicolsonL.G.“Cell Membrane Fluid–Mosaic Structure and Cancer Metastasis”. Cancer Res2015; 75(7): 1169–1176.
49.
LladóV.LópezJ.D.IbargurenM.AlonsoM.SorianoJ.B.EscribáP.V.BusquetsX.“Regulation of the Cancer Cell Membrane Lipid Composition by NaCHOleate, Effects on Cell Signaling and Therapeutical Relevance in Glioma”. BBA Biomembranes2014; 1838(6): 1619–1627.
50.
WalterM.F.JacobR.F.DayC.A.DahlborgR.WengY.J.MasonR.P.“Sulfone COX-2 Inhibitors Increase Susceptibility of Human LDL and Plasma to Oxidative Modification: Comparison to Sulfonamide COX-2 Inhibitors and NSAIDs”. Atherosclerosis2004; 177(2): 235–243.
51.
NunesC.BrezesinskiG.LimaJ.L.F.C.ReisS.LucioM.“Synchrotron SAXS and WAXS Study of the Interactions of NSAIDs with Lipid Membranes”. J. Phys. Chem2011; 115(24): 8024–8032.
52.
LichtenbergerL.M.ZhouY.JayaramanV.DoyenJ.R.O’NeilR.G.DialE.J.“Insight Into NSAID-Induced Membrane Alterations, Pathogenesis and Therapeutics: Characterization of Interaction of NSAIDs with Phosphatidylcholine”. BBA Mol. Cell Biol. L2012; 1824(7): 994–1002.
53.
EscribaP.V.Gonzalez-RosJ.M.GoniF.M.KinnunenP.K.J.VighL.Sanchez-MagranerL.“Membranes: A Meeting Point for Lipids, Proteins and Therapies”. J. Cell Mol. Med2008; 12(3): 829–875.
54.
MorenoM.M.GaridelP.SuwalskyM.HoweJ.BrandenburgK.“The Membrane-Activity of Ibuprofen, Diclofenac, and Naproxen: A Physico-Chemical Study with Lecithin Phospholipids”. Biochim. Biophys. Acta2009; 1788(6): 1296–1303.
55.
KanwarS.S.VaipheiK.NehruB.SanyalS.N.“Chemopreventive Effects of Nonsteroidal Anti-Inflammatory Drugs in the Membrane Lipid Composition and Fluidity Parameters of the 1,2-Dimethylhydrazine-Induced Colon Carcinogenesis in Rats”. Drug Chem. Toxicol2007; 30(4): 293–309.
56.
NakazawaI.IwaizumiM.“A Role of the Cancer Cell Membrane Fluidity in the Cancer Metastases: An ESR Study”. J. Exp. Med1989; 157(3): 193–198.
57.
CakmakG.ZorluF.SevercanM.SevercanF.“Screening of Protective Effect of Amifostine on Radiation-Induced Structural and Functional Variations in Rat Liver Microsomal Membranes by FT-IR Spectroscopy”. Anal. Chem2011; 83(7): 2438–2444.
58.
AcerboA.S.MillerL.M.“Assessment of the Chemical Changes induced in Human Melanoma Cells by Boric Acid Treatment using Infrared Imaging”. Analyst2009; 134(8): 1669–1674.
59.
AntoineK.M.MortazaviS.MillerA.D.MillerL.M.“Chemical Differences Are Observed in Children’s Versus Adults’ Latent Fingerprints as a Function of Time”. Forensic J. Sci2010; 55(2): 513–518.
60.
BozkurtO.SevercanM.SevercanF.“Diabetes Induces Compositional, Structural and Functional Alterations on Rat Skeletal Soleus Muscle Revealed by FTIR Spectroscopy: A Comparative Study with EDL Muscle”. Analyst2010; 135(12): 3110–3119.
61.
CakmakG.MillerL.ZorluF.SevercanF.“Amifostine, a Radioprotectant Agent, Protects Rat Brain Tissue Lipids Against 3 Ionizing Radiation Induced Damage: An FTIR Microspectroscopic Imaging Study”. Arch. Biochem. Biophys2012; 520(2): 67–73.
62.
KinderR.ZieglerC.WesselsJ.M.“γ-Irradiation and UV- C Light Induced Lipid Peroxidation: A Fourier Transform-Infrared Absorption Study”. Int. J. Radiat. Biol1997; 71(5): 561–571.
63.
LeskovjanA.C.KretlowA.MillerL.M.“Fourier Transform Infrared Imaging Showing Reduced Unsatured Lipid Content in the Hippocampus of a Mouse Model of Alzheimer’s Disease”. Anal. Chem2010; 82(7): 2711–2716.
64.
KrishnakumarN.ManoharanS.PalaniappanP.L.VenkatachalamR.M.P.ManohaM.G.A.“Chemopreventive Efficacy of Piperine in 7, 12-Dimethyl benz [a] Anthracene (DMBA)-Induced Hamster Buccal Pouch Carcinogenesis: An FT-IR Study”. Food Chem. Toxicol2009; 47(11): 2813–2820.
65.
FernandesE.CostaD.TosteS.A.LimaJ.L.F.C.ReisS.“In Vitro Scavenging Activity for Reactive Oxygen and Nitrogen Species by Nonsteroidal Anti-Inflammatory Indole, Pyrrole, and Oxazole Derivative Drugs”. Free Radic. Biol. Med2004; 37(11): 1895–1905.
66.
GreeningW.D.JiH.KappA.E.SimpsonJ.R.“Sulindac Modulates Secreted Protein Expression from LIM1215 Colon Carcinoma Cells Prior to Apoptosis”. Biochim. Biophys. Acta2013; 1834(11): 2293–2307.
67.
G. Barrera, F. Gentile, S. Pizzimenti, R.A. Canuto, M. Daga, A. Arcaro, G.P. Cetrangolo, A. Lepore, C. Ferretti, C. Dianzani, G. Muzio. “Mitochondrial Dysfunction in Cancer and Neurodegenerative Diseases: Spotlight on Fatty Acid Oxidation and Lipoperoxidation Products”. Antioxidants (Basel). 2016. 19; 5(1). pii: E7.
68.
SimmonsD.B.BottingD.B.HlaT.“Cyclooxygenase Isozymes: The Biology of Prostaglandin Synthesis and Inhibition”. Pharmacol2004; 56(3): 387–437.
69.
SmithW.UradeY.JakobssonP.J.“Enzymes of the Cyclooxygenase Pathways of Prostanoid Biosynthesis”. Chem. Rev2011; 111(10): 5821–5865.
70.
SeddonA.C.CaseyD.LawR.V.GeeA.TemplerR.H.“Drug Interactions with Lipid Membranes”. Chem. Soc. Rev2009; 38(9): 2509–2519.
71.
SzalontaiB.“Membrane Protein Dynamics: Limited Lipid Control”. PMC Biophys2009; 2(1): 1.
72.
HarisP.I.SevercanF.“FTIR Spectroscopic Characterization of Protein Structure in Aqueous and Non-Aqueous Media”. J. Mol. Catalysis B: Enzymatic1999; 7(1): 207–221.
73.
KrafftC.SobottkaS.B.SchackertG.SalzerR.“Analysis of Human Brain Tissue, Brain Tumors and Tumor Cells by Infrared Spectroscopic Mapping”. Analyst2004; 129(10): 921–925.
74.
KneippJ.LaschP.BaldaufE.BeekesM.NaumannD.“Detection of Pathological Molecular Alterations in Scrapie-Infected Hamster Brain by Fourier Transform Infrared (FT-IR) Spectroscopy”. BBA Mol. Basis Dis2000; 1501(2–3): 189–199.
75.
AkkasS.SevercanM.YilmazO.SevercanF.“Effects of Lipoic Acid Supplementation on Rat Brain Tissue: An FTIR Spectroscopic and Neural Network Study”. Food Chem2007; 105(3): 1281–1288.
