Protein transduction domain-containing microemulsions as cutaneous delivery systems for an anticancer agent

Journal of Pharmaceutical Sciences

Volumn 102, Issue 5, 2013, Pages 1476-1487

  Pepe, Dominique ^a   Mccall, Melissa ^a   Zheng, Haian ^a   Lopes, Luciana B ^a  

^a ALBANY COLLEGE OF PHARMACY AND HEALTH SCIENCES   (United States)

Author keywords

Cutaneous delivery; Microemulsion; Paclitaxel; Penetratin; Permeation enhancers; Skin; Transdermal drug delivery

Indexed keywords

OCTANOIN; PACLITAXEL; PENETRATIN; PHYTOSPHINGOSINE;

ARTICLE; DRUG DELIVERY SYSTEM; DRUG DISTRIBUTION; DRUG FORMULATION; DRUG PENETRATION; MICROEMULSION; PROTEIN DOMAIN; PROTEIN FOLDING; SIGNAL TRANSDUCTION; SKIN IRRITATION; SKIN PENETRATION; SKIN TUMOR; SKIN WATER LOSS; VISCOMETRY; ZETA POTENTIAL;

EID: 84876337580     PISSN: 00223549     EISSN: 15206017     Source Type: Journal    
DOI: 10.1002/jps.23482     Document Type: Article

References (71)

1. Heffelfinger C, Ouyang Z, Engberg A, Leffell DJ, Hanlon AM, Gordon PB, Zheng W, Zhao H, Snyder MP, Bale AE. 2012. Correlation of global microRNA expression with basal cell carcinoma subtype. G3 (Bethesda) 2(2):279-286.
2. Rubin AI, Chen EH, Ratner D. 2005. Basal-cell carcinoma. N Engl J Med 353(21):2262-2269.
3. Tull S, Nunley K, Sengelmann R. 2008. Nonsurgical treatment modalities for primary cutaneous malignancies. Dermatol Surg 34(7):859-872.
4. Khandavilli S, Panchagnula R. 2007. Nanoemulsions as versatile formulations for paclitaxel delivery: Peroral and dermal delivery studies in rats. J Invest Dermatol 127(1):154-162.
5. Ferguson T, Wilcken N, Vagg R, Ghersi D, Nowak AK. 2007. Taxanes for adjuvant treatment of early breast cancer. Cochrane Database Syst Rev (4):CD004421.
6. Kunstfeld R, Wickenhauser G, Michaelis U, Teifel M, Umek W, Naujoks K, Wolff K, Petzelbauer P. 2003. Paclitaxel encapsulated in cationic liposomes diminishes tumor angiogenesis and melanoma growth in a "humanized" SCID mouse model. J Invest Dermatol 120(3):476-482.
7. Belotti D, Vergani V, Drudis T, Borsotti P, Pitelli MR, Viale G, Giavazzi R, Taraboletti G. 1996. The microtubule-affecting drug paclitaxel has antiangiogenic activity. Clin Cancer Res 2(11):1843-1849.
8. Selimovic D, Hassan M, Haikel Y, Hengge UR. 2008. Taxol-induced mitochondrial stress in melanoma cells is mediated by activation of c-Jun N-terminal kinase (JNK) and p38 pathways via uncoupling protein 2. Cell Signal 20(2):311-322.
9. Lau DH, Xue L, Young LJ, Burke PA, Cheung AT. 1999. Paclitaxel (Taxol): An inhibitor of angiogenesis in a highly vascularized transgenic breast cancer. Cancer Biother Radiopharm 14(1):31-36.
10. Baspinar Y, Borchert HH. 2012. Penetration and release studies of positively and negatively charged nanoemulsions-is there a benefit of the positive charge? Int J Pharm 430(1-2):247-252.
11. Baspinar Y, Keck CM, Borchert HH. 2010. Development of a positively charged prednicarbate nanoemulsion. Int J Pharm 383(1-2):201-208.
12. Jones AT, Sayers EJ. 2012. Cell entry of cell penetrating peptides: Tales of tails wagging dogs. J Control Release 161(2):582-591.
13. Lopes LB, Furnish E, Komalavilas P, Seal BL, Panitch A, Bentley MV, Brophy CM. 2008. Enhanced skin penetration of P20 phosphopeptide using protein transduction domains. Eur J Pharm Biopharm 68(2):441-445.
14. Rothbard JB, Garlington S, Lin Q, Kirschberg T, Kreider E, McGrane PL, Wender PA, Khavari PA. 2000. Conjugation of arginine oligomers to cyclosporin A facilitates topical delivery and inhibition of inflammation. Nat Med 6(11):1253-1257.
15. Lopes LB, Brophy CM, Furnish E, Flynn CR, Sparks O, Komalavilas P, Joshi L, Panitch A, Bentley MV. 2005. Comparative study of the skin penetration of protein transduction domains and a conjugated peptide. Pharm Res 22(5):750-757.
16. Hosmer J, Reed R, Bentley MV, Nornoo A, Lopes LB. 2009. Microemulsions containing medium-chain glycerides as transdermal delivery systems for hydrophilic and hydrophobic drugs. AAPS PharmSciTech 10(2):589-596.
17. Junyaprasert VB, Boonme P, Songkro S, Krauel K, Rades T. 2007. Transdermal delivery of hydrophobic and hydrophilic local anesthetics from o/w and w/o Brij 97-based microemulsions. J Pharm Pharm Sci 10(3):288-298.
18. Lo YL. 2003. Relationships between the hydrophilic-lipophilic balance values of pharmaceutical excipients and their multidrug resistance modulating effect in Caco-2 cells and rat intestines. J Control Release 90(1):37-48.
19. Gottesman MM, Fojo T, Bates SE. 2002. Multidrug resistance in cancer: Role of ATP-dependent transporters. Nat Rev Cancer 2(1):48-58.
20. Hosmer JM, Steiner AA, Lopes LB. 2012. Lamellar liquid crystalline phases for cutaneous delivery of paclitaxel: Impact of the monoglyceride. Pharm Res. Published on-line: DOI: 10.1007/s11095-012-0908-0
21. Hosmer JM, Shin SH, Nornoo A, Zheng H, Lopes LB. 2011. Influence of internal structure and composition of liquid crystalline phases on topical delivery of paclitaxel. J Pharm Sci 100(4):1444-1455.
22. Hoeller S, Sperger A, Valenta C. 2009. Lecithin based nanoemulsions: A comparative study of the influence of non-ionic surfactants and the cationic phytosphingosine on physicochemical behaviour and skin permeation. Int J Pharm 370(1-2):181-186.
23. Wartewig S, Neubert RH. 2007. Properties of ceramides and their impact on the stratum corneum structure: A review. Part 1: ceramides. Skin Pharmacol Physiol 20(5):220-229.
24. Kantarci G, Ozguney I, Karasulu HY, Arzik S, Guneri T. 2007. Comparison of different water/oil microemulsions containing diclofenac sodium: Preparation, characterization, release rate, and skin irritation studies. AAPS PharmSciTech 8(4):E91.
25. Zhang J, Michniak-Kohn B. 2011. Investigation of microemulsion microstructures and their relationship to transdermal permeation of model drugs: Ketoprofen, lidocaine, and caffeine. Int J Pharm 421(1):34-44.
26. Lopes LB, Murphy N, Nornoo A. 2009. Enhancement of transdermal delivery of progesterone using medium-chain mono and diglycerides as skin penetration enhancers. Pharm Dev Technol 14(5):524-529.
27. Schmid-Wendtner MH, Korting HC. 2006. The pH of the skin surface and its impact on the barrier function. Skin Pharmacol Physiol 19(6):296-302.
28. Mahdi ES, Noor AM, Sakeena MH, Abdullah GZ, Abdulkarim MF, Sattar MA. 2011. Formulation and in vitro release evaluation of newly synthesized palm kernel oil esters-based nanoemulsion delivery system for 30% ethanolic dried extract derived from local Phyllanthus urinaria for skin antiaging. Int J Nanomed 6:2499-2512.
29. Bagley DM, Gardner JR, Holland G, Lewis RW, Vrijhof H, Walker AP. 1999. Eye irritation: Updated reference chemicals data bank. Toxicol In Vitro 13(3):505-510.
30. Kreilgaard M, Pedersen EJ, Jaroszewski JW. 2000. NMR characterisation and transdermal drug delivery potential of microemulsion systems. J Control Release 69(3):421-433.
31. Nornoo AO, Zheng H, Lopes LB, Johnson-Restrepo B, Kannan K, Reed R. 2009. Oral microemulsions of paclitaxel: In situ and pharmacokinetic studies. Eur J Pharm Biopharm 71(2):310-317.
32. Demina T, Grozdova I, Krylova O, Zhirnov A, Istratov V, Frey H, Kautz H, Melik-Nubarov N. 2005. Relationship between the structure of amphiphilic copolymers and their ability to disturb lipid bilayers. Biochemistry 44(10):4042-4054.
33. Regev R, Assaraf YG, Eytan GD. 1999. Membrane fluidization by ether, other anesthetics, and certain agents abolishes P-glycoprotein ATPase activity and modulates efflux from multidrug-resistant cells. Eur J Biochem 259(1-2):18-24.
34. Hathout RM, Woodman TJ, Mansour S, Mortada ND, Geneidi AS, Guy RH. 2010. Microemulsion formulations for the transdermal delivery of testosterone. Eur J Pharm Sci 40(3):188-196.
35. Malheiro AR, Varanda LC, Perez J, Villullas HM. 2007. The aerosol OT+n-butanol+n-heptane+water system: Phase behavior, structure characterization, and application to Pt70Fe30 nanoparticle synthesis. Langmuir 23(22):11015-11020.
36. Zielinska K, Wilk KA, Jezierski A, Jesionowski T. 2008. Microstructure and structural transition in microemulsions stabilized by aldonamide-type surfactants. J Colloid Interface Sci 321(2):408-417.
37. Podlogar F, Gasperlin M, Tomsic M, Jamnik A, Rogac MB. 2004. Structural characterisation of water-Tween 40/Imwitor 308-isopropyl myristate microemulsions using different experimental methods. Int J Pharm 276(1-2):115-128.
38. Araujo LM, Thomazine JA, Lopez RF. 2010. Development of microemulsions to topically deliver 5-aminolevulinic acid in photodynamic therapy. Eur J Pharm Biopharm 75(1):48-55.
39. Lawrence MJ, Rees GD. 2000. Microemulsion-based media as novel drug delivery systems. Adv Drug Deliv Rev 45(1):89-121.
40. Batrakova EV, Li S, Li Y, Alakhov VY, Kabanov AV. 2004. Effect of pluronic P85 on ATPase activity of drug efflux transporters. Pharm Res 21(12):2226-2233.
41. Zhu S, Huang R, Hong M, Jiang Y, Hu Z, Liu C, Pei Y. 2009. Effects of polyoxyethylene (40) stearate on the activity of P-glycoprotein and cytochrome P450. Eur J Pharm Sci 37(5):573-580.
42. Cohen-Avrahami M, Libster D, Aserin A, Garti N. 2012. Penetratin-induced transdermal delivery from H(II) mesophases of sodium diclofenac. J Control Release 159(3):419-428.
43. Peetla C, Rao KS, Labhasetwar V. 2009. Relevance of biophysical interactions of nanoparticles with a model membrane in predicting cellular uptake: Study with TAT peptide-conjugated nanoparticles. Mol Pharm 6(5):1311-1320.
44. Yilmaz E, Borchert HH. 2005. Design of a phytosphingosine-containing, positively-charged nanoemulsion as a colloidal carrier system for dermal application of ceramides. Eur J Pharm Biopharm 60(1):91-98.
45. Lehmann L, Keipert S, Gloor M. 2001. Effects of microemulsions on the stratum corneum and hydrocortisone penetration. Eur J Pharm Biopharm 52(2):129-136.
46. Loffler H, Pirker C, Aramaki J, Frosch PJ, Happle R, Effendy I. 2001. Evaluation of skin susceptibility to irritancy by routine patch testing with sodium lauryl sulfate. Eur J Dermatol 11(5):416-419.
47. Lopes LB, VanDeWall H, Li HT, Venugopal V, Li HK, Naydin S, Hosmer J, Levendusky M, Zheng H, Bentley MV, Levin R, Hass MA. 2010. Topical delivery of lycopene using microemulsions: Enhanced skin penetration and tissue antioxidant activity. J Pharm Sci 99(3):1346-1357.
48. Ayehunie S, Cannon C, Lamore S, Kubilus J, Anderson DJ, Pudney J, Klausner M. 2006. Organotypic human vaginal-ectocervical tissue model for irritation studies of spermicides, microbicides, and feminine-care products. Toxicol In Vitro 20(5):689-698.
49. Barta CA, Sachs-Barrable K, Feng F, Wasan KM. 2008. Effects of monoglycerides on P-glycoprotein: Modulation of the activity and expression in Caco-2 cell monolayers. Mol Pharm 5(5):863-875.
50. Litman T, Zeuthen T, Skovsgaard T, Stein WD. 1997. Structure-activity relationships of P-glycoprotein interacting drugs: Kinetic characterization of their effects on ATPase activity. Biochim Biophys Acta 1361(2):159-168.
51. Riganti C, Voena C, Kopecka J, Corsetto PA, Montorfano G, Enrico E, Costamagna C, Rizzo AM, Ghigo D, Bosia A. 2011. Liposome-encapsulated doxorubicin reverses drug resistance by inhibiting P-glycoprotein in human cancer cells. Mol Pharm 8(3):683-700.
52. Garcion E, Lamprecht A, Heurtault B, Paillard A, Aubert-Pouessel A, Denizot B, Menei P, Benoit JP. 2006. A new generation of anticancer, drug-loaded, colloidal vectors reverses multidrug resistance in glioma and reduces tumor progression in rats. Mol Cancer Ther 5(7):1710-1722.
53. Kruh GD. 2003. Introduction to resistance to anticancer agents. Oncogene 22(47):7262-7264.
54. Blancafort P, Tschan MP, Bergquist S, Guthy D, Brachat A, Sheeter DA, Torbett BE, Erdmann D, Barbas CF 3rd. 2008. Modulation of drug resistance by artificial transcription factors. Mol Cancer Ther 7(3):688-697.
55. Hashimoto N, Nakamichi N, Uwafuji S, Yoshida K, Sugiura T, Tsuji A, Kato Y. 2013. ATP binding cassette transporters in two distinct compartments of the skin contribute to transdermal absorption of a typical substrate. J Control Release 165(1):54-61.
56. Ito K, Nguyen HT, Kato Y, Wakayama T, Kubo Y, Iseki S, Tsuji A. 2008. P-glycoprotein (Abcb1) is involved in absorptive drug transport in skin. J Control Release 131(3):198-204.
57. Patlolla RR, Desai PR, Belay K, Singh MS. 2010. Translocation of cell penetrating peptide engrafted nanoparticles across skin layers. Biomaterials 31(21):5598-5607.
58. Schutze-Redelmeier MP, Kong S, Bally MB, Dutz JP. 2004. Antennapedia transduction sequence promotes anti tumour immunity to epicutaneously administered CTL epitopes. Vaccine 22(15-16):1985-1991.
59. Park J, Ryu J, Jin LH, Bahn JH, Kim JA, Yoon CS, Kim DW, Han KH, Eum WS, Kwon HY, Kang TC, Won MH, Kang JH, Cho SW, Choi SY. 2002. 9-polylysine protein transduction domain: Enhanced penetration efficiency of superoxide dismutase into mammalian cells and skin. Mol Cells 13(2):202-208.
60. Desai P, Patlolla RR, Singh M. 2010. Interaction of nanoparticles and cell-penetrating peptides with skin for transdermal drug delivery. Mol Membr Biol 27(7):247-259.
61. Snyder EL, Dowdy SF. 2005. Recent advances in the use of protein transduction domains for the delivery of peptides, proteins and nucleic acids in vivo. Expert Opin Drug Deliv 2(1):43-51.
62. Hou YW, Chan MH, Hsu HR, Liu BR, Chen CP, Chen HH, Lee HJ. 2007. Transdermal delivery of proteins mediated by non-covalently associated arginine-rich intracellular delivery peptides. Exp Dermatol 16(12):999-1006.
63. Morita K, Miyachi Y. 2003. Tight junctions in the skin. J Dermatol Sci 31(2):81-89.
64. Lee CC, Sun Y, Huang HW. 2010. Membrane-mediated peptide conformation change from alpha-monomers to beta-aggregates. Biophys J 98(10):2236-2245.
65. Alves ID, Correia I, Jiao CY, Sachon E, Sagan S, Lavielle S, Tollin G, Chassaing G. 2009. The interaction of cell-penetrating peptides with lipid model systems and subsequent lipid reorganization: Thermodynamic and structural characterization. J Pept Sci 15(3):200-209.
66. Alves ID, Bechara C, Walrant A, Zaltsman Y, Jiao CY, Sagan S. 2011. Relationships between membrane binding, affinity and cell internalization efficacy of a cell-penetrating peptide: Penetratin as a case study. PLoS One 6(9):e24096.
67. Ziegler A. 2008. Thermodynamic studies and binding mechanisms of cell-penetrating peptides with lipids and glycosaminoglycans. Adv Drug Deliv Rev 60(4-5):580-597.
68. Utreja P, Jain S, Tiwary AK. 2011. Localized delivery of paclitaxel using elastic liposomes: Formulation development and evaluation. Drug Deliv 18(5):367-376.
69. Panchagnula R, Desu H, Jain A, Khandavilli S. 2005. Feasibility studies of dermal delivery of paclitaxel with binary combinations of ethanol and isopropyl myristate: Role of solubility, partitioning and lipid bilayer perturbation. Farmaco 60(11-12):894-899.
70. Paolino D, Celia C, Trapasso E, Cilurzo F, Fresta M. 2012. Paclitaxel-loaded ethosomes(R): Potential treatment of squamous cell carcinoma, a malignant transformation of actinic keratoses. Eur J Pharm Biopharm 81(1):102-112.
71. Kilfoyle BE, Sheihet L, Zhang Z, Laohoo M, Kohn J, Michniak-Kohn BB. 2012. Development of paclitaxel-TyroSpheres for topical skin treatment. J Control Release 163(1):18-24.