Sucrose esters increase drug penetration, but do not inhibit P-glycoprotein in Caco-2 intestinal epithelial cells

Journal of Pharmaceutical Sciences

Volumn 103, Issue 10, 2014, Pages 3107-3119

  Kiss, Lóránd ^a,b   Hellinger, Éva ^c   Pilbat, Ana Maria ^d   Kittel, Ágnes ^a   Tö Rök, Zsolt ^d   Furedi, ^a   Szakács, Gergely ^a   Veszelka, Szilvia ^a   Sipos, Péter ^b   Ózsvári, B Éla ^e   Puskás, László G ^e   Vastag, Monika ^c   Szabó RÉVÉSZ, Piroska ^b   Deli, Mária A ^a  

^a INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^b UNIVERSITY OF SZEGED   (Hungary)

^c GEDEON RICHTER LTD   (Hungary)

^d INSTITUTE OF BIOCHEMISTRY   (Hungary)

^e AVIDIN LTD   (Hungary)

Author keywords

Absorption enhancer; Caco 2 cells; Drug permeability; Efflux pumps; Epithelial; Membrane fluidity; P glycoprotein; Sucrose ester; Tight junction; Toxicity

Indexed keywords

ATENOLOL; CREMOPHOR; F ACTIN; FLUORESCEIN; LACTATE DEHYDROGENASE; LAURIC ACID DERIVATIVE; MULTIDRUG RESISTANCE PROTEIN; MYRISTIC ACID DERIVATIVE; PALMITIC ACID DERIVATIVE; POLYSORBATE 80; PROTEIN ZO1; RHODAMINE 123; SUCROSE ESTER DERIVATIVE; VINBLASTINE; ESTER; SUCROSE;

ARTICLE; CACO 2 CELL LINE; CELL DEATH; CELL JUNCTION; CELL MEMBRANE; CELL ULTRASTRUCTURE; CELL VIABILITY; CONTROLLED STUDY; DRUG ABSORPTION; DRUG PENETRATION; ELECTRIC RESISTANCE; ELECTRON MICROSCOPY; ENZYME RELEASE; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IMPEDANCE; MEMBRANE FLUIDITY; MICROFILAMENT; MTT ASSAY; TIGHT JUNCTION; TOXICITY TESTING; CHEMISTRY; DRUG EFFECTS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; INTESTINE MUCOSA; METABOLISM;

CACO-2 CELLS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; ESTERS; HUMANS; INTESTINAL MUCOSA; MEMBRANE FLUIDITY; P-GLYCOPROTEIN; SUCROSE;

EID: 84923372710     PISSN: 00223549     EISSN: 15206017     Source Type: Journal    
DOI: 10.1002/jps.24085     Document Type: Article

References (70)

1. Strickley RG. 2004. Solubilizing excipients in oral and injectable formulations. Pharm Res 21:201-230.
2. Zhao X, Liu JP, Zhang X, Li Y. 2006. Enhancement of transdermal delivery of theophylline using microemulsion vehicle. Int J Pharm 327:58-64.
3. Rege BD, Yu LX, Hussain AS, Polli JE. 2001. Effect of common excipients on Caco-2 transport of low-permeability drugs. J Pharm Sci 90:1776-1786.
4. Deli MA. 2009. Potential use of tight junction modulators to reversibly open membranous barriers and improve drug delivery. Biochim Biophys Acta 1788:892-910.
5. Gelderblom H, Verweij J, Nooter K, Sparreboom A. 2001. Cremophor EL: The drawbacks and advantages of vehicle selection for drug formulation. Eur J Cancer 37:1590-1598.
6. Kiss L, Walter FR, Bocsik A, Veszelka S, Ó zsvá ri B, Puská s LG, Szab ó-R év ész P, Deli MA. 2013. Kinetic analysis of the toxicity of pharmaceutical excipients Cremophor EL and RH40 on endothelial and epithelial cells. J Pharm Sci 102:1173-1181.
7. Daud é D, Remaud-Sim éon M, Andr é I. 2012. Sucrose analogs: An attractive (bio)source for glycodiversification. Nat Prod Rep 29:945-960.
8. Chung O, Pomeranz Y, Goforth DR, Shogren MD, Finney KF. 1976. Improved sucrose esters in breadmaking. Cereal Chem 53:615-625.
9. Garti N, Aserin A, Fanun M. 2000. Non-ionic sucrose esters microemulsions for food applications. Part 1. Water solubilization. Colloids Surf A Physicochem Eng Asp 164:27-38.
10. Muratsubaki Y. 2006. Cosmetics and materials. Application expansion in bidirection with other fields. Applied technology from cosmetics: Applied technology of sucrose fatty acid ester to cosmetics. Eng Mater 54:48-51.
11. Szu Prime Ts A, Szab ó-R év ész P. 2012. Sucrose esters as natural surfactants in drug delivery systems-A mini-review. Int J Pharm 433: 1-9.
12. Yamato K, Takahashi Y, Akiyama H, Tsuji K, Onishi H, Machida Y. 2009. Effect of penetration enhancers on transdermal delivery of propofol. Biol Pharm Bull 32:677-683.
13. Thevenin M, Grossiord JL, Poelman M. 1996. Sucrose esters/ cosurfactant microemulsion systems for transdermal delivery: Assessment of bicontinuous structures. Int J Pharm 137:177-186.
14. Lehmann L, Keipert S, Gloor M. 2001. Effects of microemulsions on the stratum corneum and hydrocortisone penetration. Eur J Pharm Biopharm 52:129-136.
15. Garti N, Clement V, Leser M, Aserin A, Fanun M. 1999. Sucrose ester microemulsions. J Mol Liq 80:253-296.
16. Mollee HM, Steenvoorden DP, De Vringer T, Crommelin DJ. 2001. The influence of the incorporation of cholesterol and water on the particle size, bilayer thickness, melting behavior, and relative sucrose ester composition of reversed vesicles. J Pharm Sci 90:588-598.
17. Chansanroj K, Betz G. 2010. Sucrose esters with various hydrophilic-lipophilic properties: Novel controlled release agents for oral drug delivery matrix tablets prepared by direct compaction. Acta Biomater 6:3101-3109.
18. Takaishi N, Satsu H, Shimizu M. 2006. Enhanced daunomycin accumulation in human intestinal Caco-2 cells from non-ionic food emulsifiers unrelated to the P-glycoprotein inhibitory mechanism. Biosci Biotechnol Biochem 70:2703-2711.
19. Nakada Y, Awata N, Nakamichi C, Sugimoto I. 1988. The effect of additives on the oral mucosal absorption of human calcitonin in rats. J Pharmacobiodyn 11:395-401.
20. Ganem-Quintanar A, Quintanar-Guerrero D, Falson-Rieg F, Buri P. 1998. Ex vivo oral mucosal permeation of lidocaine hydrochloride with sucrose fatty acid esters as absorption enhancers. Int J Pharm 173:203-210.
21. Lerk P, Sucker H. 1993. Application of sucrose laurate, a new pharmaceutical excipient, in peroral formulations of cyclosporin A. Int J Pharm 92:197-202.
22. Onishi H, Imura Y, Uchida M, Machida Y. 2012. Enhancement potential of sucrose laurate (L-1695) on intestinal absorption of watersoluble high molecular weight compounds. Curr Drug Deliv 9:487-494.
23. Cornaire G, Woodley J, Hermann P, Cloarec A, Arellano C, Houin G. 2004. Impact of excipients on the absorption of P-glycoprotein substrates in vitro and in vivo. Int J Pharm 278:119-131.
24. Hanke U, May K, Rozehnal V, Nagel S, Siegmund W, Weitschies W. 2010. Commonly used nonionic surfactants interact differently with the human efflux transporters ABCB1 (p-glycoprotein) and ABCC2 (MRP2). Eur J Pharm Biopharm 76:260-268.
25. Artursson P, Palm K, Luthman K. 2001. Caco-2 monolayers in experimental and theoretical predictions of drug transport. Adv Drug Deliv Rev 46:27-43.
26. Hellinger E, Bakk ML, P ócza P, Tihanyi K, Vastag M. 2010. Drug penetration model of vinblastine-treated Caco-2 cultures. Eur J Pharm Sci 41:96-106.
27. Hellinger E, Veszelka S, Tó th AE, Walter F, Kittel Á, Bakk ML, Tihanyi K, H áda V, Nakagawa S, Duy TDH, Niwa M, Deli MA, VastagM. 2012. Comparison of brain capillary endothelial cell-based and epithelial (MDCK-MDR1, Caco-2, and VB-Caco-2) cell-based surrogate blood-brain barrier penetration models. Eur J Pharm Biopharm 82:340-351.
28. Englund G, Rorsman F, R önnblom A, Karlbom U, Lazorova L, Gr° asj ö J, Kindmark A, Artursson P. 2006. Regional levels of drug transporters along the human intestinal tract: Co-expression of ABC and SLC transporters and comparison with Caco-2 cells. Eur J Pharm Sci 29:269-277.
29. Hayeshi R, Hilgendorf C, Artursson P, Augustijns P, Brodin B, Dehertogh P, Fisher K, Fossati L, Hovenkamp E, Korjamo T, Masungi C, Maubon N, Mols R, M? ullertz A, Mönkkönen J, O'Driscoll C, Oppers-Tiemissen HM, Ragnarsson EG, Rooseboom M, Ungell AL. 2008. Comparison of drug transporter gene expression and functionality in Caco-2 cells from 10 different laboratories. Eur J Pharm Sci 35:383-396.
30. Chen G, Jaffrézou JP, Fleming WH, Durán GE, Sikic BI. 1994. Prevalence of multidrug resistance related to activation of the mdr1 gene in human sarcoma mutants derived by single-step doxorubicin selection. Cancer Res 54:4980-4987.
31. Benson K, Cramer S, Galla HJ. 2013. Impedance-based cell monitoring: Barrier properties and beyond. Fluids Barriers CNS 10:5.
32. Atienza JM, Yu N, Kirstein SL, Xi B, Wang X, Xu X, Abassi YA. 2006. Dynamic and label-free cell-based assays using the real-time cell electronic sensing system. Assay Drug Dev Technol 4:597-607.
33. Ó zsvá ri B, Puská s LG, Nagy LI, Kanizsai I, Gyuris M, Madá csi R, Feh ér LZ, Ger o″ D, Szab ó C. 2010. A cell-microelectronic sensing technique for the screening of cytoprotective compounds. Int J Mol Med 25:525-530.
34. Kü rti L, Veszelka S, Bocsik A, Dung NTK, Ó zsvá ri B, Puská s LG, Kittel A7, Szabó -Ré vé sz P, Deli MA. 2012. The effect of sucrose esters on a culture model of the nasal barrier. Toxicol In Vitro 26:445-454.
35. T ör ök Z, Horv áth I, Goloubinoff P, Kov ács E, Glatz A, Balogh G, Vígh L. 1997. Evidence for a lipochaperonin: Association of active protein-folding GroESL oligomers with lipids can stabilize membranes under heat shock conditions. Proc Natl Acad Sci USA 94:2192-2197.
36. Balogh G, Maulucci G, Gombos I, Horv áth I, T ör ök Z, P éter M, Fodor E, P ali T, Benk o″ S, Parasassi T, De Spirito M, Harwood JL, Vígh L. 2011. Heat stress causes spatially-distinct membrane re-modelling in K562 leukemia cells. PLoS One 6:e21182.
37. Juvale K, Pape VF, Wiese M. 2012. Investigation of chalcones and benzochalcones as inhibitors of breast cancer resistance protein. Bioorg Med Chem 20:346-355.
38. T? urk D, Hall M D, Chu B F, Ludwig J A, Fales H M, Gottesman M, Szak ács G. 2009. Identification of compounds selectively killing multidrug-resistant cancer cells. Cancer Res 69:8293-8301.
39. Kar ászi E, Jakab K, Homolya L, Szak ács G, Holl ó Z, Telek B, Kiss A, Rejt ô L, Nahajevszky S, Sarkadi B, Kappelmayer J. 2001. Calcein assay for multidrug resistance reliably predicts therapy response and survival rate in acute myeloid leukaemia. Br J Haematol 112:308-314.
40. Weis M, Mortensen SA, Rassing MR, Møller-Sonnergaard J, Poulsen G, Rasmussen SN. 1994. Bioavailability of four oral coenzyme Q10 formulations in healthy volunteers. Mol Aspects Med 15(Suppl):s273-s280.
41. Mercke Odeberg J, Lignell A, Pettersson A, H öglund P. 2003. Oral bioavailability of the antioxidant astaxanthin in humans is enhanced by incorporation of lipid based formulations. Eur J Pharm Sci 19:299-304.
42. Legen I, Kristl A. 2004. D-glucose triggers multidrug resistanceassociated protein (MRP)-mediated secretion of fluorescein across rat jejunum in vitro. Pharm Res 21:635-640.
43. Schinkel AH, Jonker JW. 2003. Mammalian drug efflux transporters of the ATP binding cassette (ABC) family: An overview. Adv Drug Deliv Rev 55:3-29.
44. Sz u″ts A, L áng P, Ambrus R, Kiss L, Deli MA, Szab ó-R év ész P. 2011. Applicability of sucrose laurate as surfactant in solid dispersions prepared by melt technology. Int J Pharm 410:107-110.
45. Mine Y, Zhang JW. 2003. Surfactants enhance the tight-junction permeability of food allergens in human intestinal epithelial Caco-2 cells. Int Arch Allergy Immunol 130:135-142.
46. Liu Y, Peterson DA, Kimura H, Schubert D. 1997. Mechanism of cellular 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide (MTT) reduction. J Neurochem 69:581-593.
47. Berry J, Turner D. 1960. The enzymatic hydrolysis and tissue oxidation of fatty acid esters of sucrose. J Am Oil Chem Soc 37:302-305.
48. Shigeoka T, Izawa O, Kitazawa K, Yamauchi F, Murata T. 1984. Studies on the metabolic fate of sucrose esters in rats. Food Chem Toxicol 22:409-414.
49. Noker PE, Lin TH, Hill DL, Shigeoka T. 1997. Metabolism of 14C-labelled sucrose esters of stearic acid in rats. Food Chem Toxicol 35:589-595.
50. Christiansen A, Backensfeld T, K ?uhn S,Weitschies W. 2011. Investigating the stability of the nonionic surfactants tocopheryl polyethylene glycol succinate and sucrose laurate by HPLC-MS, DAD, and CAD. J Pharm Sci 100:1773-1782.
51. Okumura H, Kitazawa N, Wada S, Hotta H. 2011. Stability of sucrose fatty acid esters under acidic and basic conditions. J Oleo Sci 60:313-320.
52. Marciello M, Mateo C, Guisan JM. 2011. Full enzymatic hydrolysis of commercial sucrose laurate by immobilized-stabilized derivatives of lipase from Thermomyces lanuginosa. Colloids Surf B Biointerfaces 84:556-560.
53. Christiansen A, Backensfeld T, Weitschies W. 2010. Effects of nonionic surfactants on in vitro triglyceride digestion and their susceptibility to digestion by pancreatic enzymes. Eur J Pharm Sci 41:376-382.
54. van Tellingen O, Beijnen JH, Verweij J, Scherrenburg EJ, Nooijen WJ, Sparreboom A. 1999. Rapid esterase-sensitive breakdown of polysorbate 80 and its impact on the plasma pharmacokinetics of docetaxel and metabolites in mice. Clin Cancer Res 5:2918-2924.
55. Cs áki KF. 2011. Synthetic surfactant food additives can cause intestinal barrier dysfunction. Med Hypotheses 76:676-681.
56. Yu H, Hu YQ, Ip FCF, Zuo Z, Han YF, Ip NY. 2011. Intestinal transport of bis(12)-hupyridone in Caco-2 cells and its improved permeability by the surfactant Brij-35. Biopharm Drug Dispos 32:140-150.
57. Takahashi Y, Kondo H, Yasuda T, Watanabe T, Kobayashi S, Yokohama S. 2002. Common solubilizers to estimate the Caco-2 transport of poorly water-soluble drugs. Int J Pharm 246:85-94.
58. Wu CY, Benet LZ. 2005. Predicting drug disposition via application of BCS: Transport/absorption/ elimination interplay and development of a biopharmaceutics drug disposition classification system. Pharm Res 22:11-23.
59. Nerurkar MM, Ho NF, Burton PS, Vidmar TJ, Borchardt RT. 1997. Mechanistic roles of neutral surfactants on concurrent polarized and passive membrane transport of a model peptide in Caco-2 cells. J Pharm Sci 86:813-821.
60. Horv át S, Feh ér A, Wolburg H, Sipos P, Veszelka S, T óth A, Kiss L, Kurunczi A, Balogh G, K ürti L, Er o″s I, Szab ó-R év ész P, Deli MA. 2009. Sodium hyaluronate as a mucoadhesive component in nasal formulation enhances delivery of molecules to brain tissue. Eur J Pharm Biopharm 72:252-259.
61. Lichtenberger LM, Zhou Y, Dial EJ, Raphael RM. 2006. NSAID injury to the gastrointestinal tract: Evidence that NSAIDs interact with phospholipids to weaken the hydrophobic surface barrier and induce the formation of unstable pores in membranes. J Pharm Pharmacol 58:1421-1428.
62. Peetla C, Vijayaraghavalu S, Labhasetwar V. 2013. Biophysics of cell membrane lipids in cancer drug resistance: Implications for drug transport and drug delivery with nanoparticles. Adv Drug Deliv Rev 65:1686-1698.
63. Aungst BJ. 2000. Intestinal permeation enhancers. J Pharm Sci 89:429-442.
64. Rege BD, Kao JPY, Polli JE. 2002. Effects of nonionic surfactants on membrane transporters in Caco-2 cell monolayers. Eur J Pharm Sci 16:237-246.
65. Nerurkar MM, Ho NF, Burton PS, Vidmar TJ, Borchardt RT. 1997. Mechanistic roles of neutral surfactants on concurrent polarized and passive membrane transport of a model peptide in Caco-2 cells. J Pharm Sci 86(7):813-821.
66. Darby RA, Callaghan R, McMahon RM. 2011. P-glycoprotein inhibition: The past, the present and the future. Curr Drug Metab 12:722-731.
67. Engel A, Oswald S, Siegmund W, Keiser M. 2012. Pharmaceutical excipients influence the function of human uptake transporting proteins. Mol Pharm 9:2577-2581.
68. Hugger ED, Novak BL, Burton PS, Audus KL, Borchardt RT. 2002. A comparison of commonly used polyethoxylated pharmaceutical excipients on their ability to inhibit P-glycoprotein activity in vitro. J Pharm Sci 91:1991-2002.
69. Bogman K, Erne-Brand F, Alsenz J, Drewe J. 2003. The role of surfactants in the reversal of active transport mediated by multidrug resistance proteins. J Pharm Sci 92:1250-1261.
70. Yamagata T, Kusuhara H, Morishita M, Takayama K, Benameur H, Sugiyama Y. 2007. Effect of excipients on breast cancer resistance protein substrate uptake activity. J Control Release 124:1-5.