CD44 targeted chemotherapy for co-eradication of breast cancer stem cells and cancer cells using polymeric nanoparticles of salinomycin and paclitaxel

Colloids and Surfaces B: Biointerfaces

Volumn 143, Issue , 2016, Pages 532-546

  Muntimadugu, Eameema ^a   Kumar, Rajendra ^b   Saladi, Shantikumar ^a   Rafeeqi, Towseef Amin ^c   Khan, Wahid ^a  

^a NATIONAL INSTITUTE OF PHARMACEUTICAL EDUCATION AND RESEARCH NIPER   (India)

^b PANJAB UNIVERSITY   (India)

^c Central Research Institute of Unani Medicine   (India)

Author keywords

Cancer stem cells; CD44 receptors; Combinational chemotherapy; Hyaluronic acid; Paclitaxel; Polymeric nanoparticles; Salinomycin

Indexed keywords

CELL CULTURE; CELL PROLIFERATION; CHEMOTHERAPY; CYTOLOGY; CYTOTOXICITY; DISEASES; DRUG PRODUCTS; EFFICIENCY; EMULSIFICATION; HIGH RESOLUTION TRANSMISSION ELECTRON MICROSCOPY; HYALURONIC ACID; LIGHT MODULATORS; LIGHT SCATTERING; LIGHT TRANSMISSION; NANOPARTICLES; ORGANIC ACIDS; POLYMERS; STEM CELLS; TRANSMISSION ELECTRON MICROSCOPY;

CANCER STEM CELLS; CD44 RECEPTORS; PACLITAXEL; POLYMERIC NANOPARTICLES; SALINOMYCIN;

CELLS;

CATIONIC SURFACTANT; CD44 RECEPTOR; FLUORESCEIN ISOTHIOCYANATE; HYALURONIC ACID; NANOPARTICLE; PACLITAXEL; POLYGLACTIN; RECEPTOR; SALINOMYCIN; SOLVENT; UNCLASSIFIED DRUG; ANTIBODY; ANTINEOPLASTIC AGENT; CD44 PROTEIN, HUMAN; DRUG CARRIER; FLUORESCENT DYE; HERMES ANTIGEN; LACTIC ACID; POLYGLYCOLIC ACID; POLYLACTIC ACID-POLYGLYCOLIC ACID COPOLYMER; PYRAN DERIVATIVE;

ANIMAL EXPERIMENT; ANTINEOPLASTIC ACTIVITY; ARTICLE; BREAST CANCER; CANCER CELL; CANCER CHEMOTHERAPY; CANCER STEM CELL; CELL COUNT; CELL CYCLE; CELL TRANSPORT; CONTROLLED STUDY; CYTOTOXICITY TEST; DISEASE ERADICATION; DRUG DELIVERY SYSTEM; DRUG DIFFUSION; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IN VITRO STUDY; MIC50; MOLECULARLY TARGETED THERAPY; NONHUMAN; PARTICLE SIZE; PHOTON CORRELATION SPECTROSCOPY; PRIORITY JOURNAL; RAT; STAINING; STATIC ELECTRICITY; TRANSMISSION ELECTRON MICROSCOPY; ZETA POTENTIAL; CHEMISTRY; DRUG EFFECTS; DRUG FORMULATION; DRUG RELEASE; FEMALE; GENE EXPRESSION; GENETICS; IMMUNOLOGY; MCF-7 CELL LINE; PATHOLOGY; PROCEDURES;

ANTIBODIES; ANTIGENS, CD44; ANTINEOPLASTIC AGENTS; DRUG CARRIERS; DRUG COMPOUNDING; DRUG LIBERATION; FEMALE; FLUORESCEIN-5-ISOTHIOCYANATE; FLUORESCENT DYES; GENE EXPRESSION; HUMANS; HYALURONIC ACID; LACTIC ACID; MCF-7 CELLS; MOLECULAR TARGETED THERAPY; NEOPLASTIC STEM CELLS; PACLITAXEL; PARTICLE SIZE; POLYGLYCOLIC ACID; PYRANS;

EID: 84961959080     PISSN: 09277765     EISSN: 18734367     Source Type: Journal    
DOI: 10.1016/j.colsurfb.2016.03.075     Document Type: Article

References (72)

1. McDermott S.P., Wicha M.S. Targeting breast cancer stem cells. Mol. Oncol. 2010, 4:404-419.
2. Gangopadhyay S., Nandy A., Hor P., Mukhopadhyay A. Breast cancer stem cells: a novel therapeutic target. Clin. Breast Cancer 2013, 13:7-15.
3. Mimeault M., Hauke R., Batra S.K. Recent advances on the molecular mechanisms involved in the drug resistance of cancer cells and novel targeting therapies. Clin. Pharmacol. Ther. 2008, 83:673-691.
4. Hossein Ghahremani M. Targeting CD44 by hyaluronic acid-based nano drug delivery systems may eradicate cancer stem cells in human breast cancer. J. Med. Hypotheses Ideas 2011, 5:26-31.
5. Singla A.K., Garg A., Aggarwal D. Paclitaxel and its formulations. Int. J. Pharm. 2002, 235:179-192.
6. Kemper E.M., van Zandbergen A.E., Cleypool C., Mos H.A., Boogerd W., Beijnen J.H., van Tellingen O. Increased penetration of paclitaxel into the brain by inhibition of P-glycoprotein. Clin. Cancer Res. 2003, 9:2849-2855.
7. Ma P., Mumper R.J. Paclitaxel nano-delivery systems: a comprehensive review. J. Nanomed. Nanotechnol. 2013, 4:1000164.
8. Yokoyama M. Clinical applications of polymeric micelle carrier systems in chemotherapy and image diagnosis of solid tumors. J. Exp. Clin. Med. 2011, 3:151-158.
9. ® ABI-007) in the treatment of breast cancer. Int. J. Nanomed. 2009, 4:99-105.
10. Gupta P.B., Onder T.T., Jiang G., Tao K., Kuperwasser C., Weinberg R.A., Lander E.S. Identification of selective inhibitors of cancer stem cells by high-throughput screening. Cell 2009, 138:645-659.
11. Lu D., Choi M.Y., Yu J., Castro J.E., Kipps T.J., Carson D.A. Salinomycin inhibits Wnt signaling and selectively induces apoptosis in chronic lymphocytic leukemia cells. Proc. Natl. Acad. Sci. 2011, 108:13253-13257.
12. Riccioni R., Dupuis M.L., Bernabei M., Petrucci E., Pasquini L., Mariani G., Cianfriglia M., Testa U. The cancer stem cell selective inhibitor salinomycin is a p-glycoprotein inhibitor. Blood Cell. Mol. Dis. 2010, 45:86-92.
13. Kim W.K., Kim J.H., Yoon K., Kim S., Ro J., Kang H.S., Yoon S. Salinomycin a p-glycoprotein inhibitor, sensitizes radiation-treated cancer cells by increasing DNA damage and inducing G2 arrest. Invest. New Drugs 2011, 30:1311-1318.
14. Davis M.E., Shin D.M. Nanoparticle therapeutics: an emerging treatment modality for cancer. Nat. Rev. Drug Discovery 2008, 7:771-782.
15. Gatte M., Yip G.W. Heparanase, hyaluronan, and CD44 in cancers: a breast carcinoma perspective. Cancer Res. 2006, 66:10233-10237.
16. Ponta H., Sherman L., Herrlich P.A. CD44: from adhesion molecules to signalling regulators. Nat. Rev. Mol. Cell Biol. 2003, 4:33-45.
17. Al-Hajj M., Wicha M.S., Benito-Hernandez A., Morrison S.J., Clarke M.F. Prospective identification of tumorigenic breast cancer cells. Proc. Natl. Acad. Sci. 2003, 100:3983-3988.
18. Asplund T., Heldin P. Hyaluronan receptors are expressed on human malignant mesothelioma cells but not on normal mesothelial cells. Cancer Res. 1994, 54:4516-4523.
19. Jang S.H., Wientjes M.G., Au J.L.-S. Kinetics of P-glycoprotein-mediated efflux of paclitaxel. J. Pharmacol. Exp. Ther. 2001, 298:1236-1242.
20. Aydin R. Herceptin-decorated salinomycin-loaded nanoparticles for breast tumor targeting. J. Biomed. Mater. Res. A 2013, 101:1405-1415.
21. Jiang J., Chen H., Yu C., Zhang Y., Chen M., Tian S., Sun C. The promotion of salinomycin delivery to hepatocellular carcinoma cells through EGFR and CD133 aptamers conjugation by PLGA nanoparticles. Nanomedicine 2015, 10:1863-1879.
22. Ni M., Xiong M., Zhang X., Cai G., Chen H., Zeng Q., Yu Z. Poly (lactic-co-glycolic acid) nanoparticles conjugated with cD133 aptamers for targeted salinomycin delivery to cD133+ osteosarcoma cancer stem cells. Int. J. Nanomed. 2015, 10:2537.
23. Wang Q., Wu P., Ren W., Xin K., Yang Y., Xie C., Yang C., Liu Q., Yu L., Jiang X. Comparative studies of salinomycin-loaded nanoparticles prepared by nanoprecipitation and single emulsion method. Nanoscale Res. Lett. 2014, 9:1-9.
24. Yao H.j., Zhang Y.g., Sun L., Liu Y. The effect of hyaluronic acid functionalized carbon nanotubes loaded with salinomycin on gastric cancer stem cells. Biomaterials 2014, 35:9208-9223.
25. Zhao P., Dong S., Bhattacharyya J., Chen M. iTEP nanoparticle-delivered salinomycin displays an enhanced toxicity to cancer stem cells in orthotopic breast tumors. Mol. Pharm. 2014, 11:2703-2712.
26. Zhang Y., Zhang H., Wang X., Wang J., Zhang X., Zhang Q. The eradication of breast cancer and cancer stem cells using octreotide modified paclitaxel active targeting micelles and salinomycin passive targeting micelles. Biomaterials 2012, 33:679-691.
27. Kim Y.J., Liu Y., Li S., Rohrs J., Zhang R., Zhang X., Wang P. Co-eradication of breast cancer cells and cancer stem cells by cross-linked multilamellar liposomes enhances tumor treatment. Mol. Pharm. 2015, 12:2811-2822.
28. Ke X.Y., Ng V.W.L., Gao S.J., Tong Y.W., Hedrick J.L., Yang Y.Y. Co-delivery of thioridazine and doxorubicin using polymeric micelles for targeting both cancer cells and cancer stem cells. Biomaterials 2014, 35:1096-1108.
29. Wang D., Huang J., Wang X., Yu Y., Zhang H., Chen Y., Liu J., Sun Z., Zou H., Sun D. The eradication of breast cancer cells and stem cells by 8-hydroxyquinoline-loaded hyaluronan modified mesoporous silica nanoparticle-supported lipid bilayers containing docetaxel. Biomaterials 2013, 34:7662-7673.
30. Wang H., Agarwal P., Zhao S., Xu R.X., Yu J., Lu X., He X. Hyaluronic acid-decorated dual responsive nanoparticles of Pluronic F127, PLGA, and chitosan for targeted co-delivery of doxorubicin and irinotecan to eliminate cancer stem-like cells. Biomaterials 2015, 72:74-89.
31. Hariharan S., Bhardwaj V., Bala I., Sitterberg J., Bakowsky U., Kumar M.N.V.R. Design of estradiol loaded PLGA nanoparticulate formulations: a potential oral delivery system for hormone therapy. Pharm. Res. 2006, 23:184-195.
32. Almalik A., Donno R., Cadman C.J., Cellesi F., Day P.J., Tirelli N. Hyaluronic acid-coated chitosan nanoparticles: molecular weight-dependent effects on morphology and hyaluronic acid presentation. J. Controlled Release 2013, 172:1142-1150.
33. Zafar S., Negi L.M., Verma A.K., Kumar V., Tyagi A., Singh P., Iqbal Z., Talegaonkar S. Sterically stabilized polymeric nanoparticles with a combinatorial approach for multi drug resistant cancer: in vitro and in vivo investigations. Int. J. Pharm. 2014, 477:454-468.
34. Chan J.M., Zhang L., Yuet K.P., Liao G., Rhee J.W., Langer R., Farokhzad O.C. PLGA-lecithin-PEG core shell nanoparticles for controlled drug delivery. Biomaterials 2009, 30:1627-1634.
35. Tokarek K., Hueso J.L., Kuśtrowski P., Stochel G., Kyzioł A. Green synthesis of chitosan-stabilized copper nanoparticles. Eur. J. Inorg. Chem. 2013, 2013:4940-4947.
36. Jain A., Gulbake A., Shilpi S., Hurkat P., Kashaw S., Jain S.K. Development and validation of the HPLC method for simultaneous estimation of Paclitaxel and topotecan. J. Chromatogr. Sci. 2014, 52:697-703.
37. Mathur A.K. Determination of salinomycin by high-performance liquid chromatography using a precolumn derivatization technique. J. Chromatogr. A 1994, 664:284-288.
38. Neve R.M., Chin K., Fridlyand J., Yeh J., Baehner F.L., Fevr T., Clark L., Bayani N., Coppe J.-P., Tong F. A collection of breast cancer cell lines for the study of functionally distinct cancer subtypes. Cancer cell 2006, 10:515-527.
39. S.S. Katiyar, E. Muntimadugu, T.A. Rafeeqi, A.J. Domb, W. Khan, Co-delivery of rapamycin-and piperine-loaded polymeric nanoparticles for breast cancer treatment, Drug Deliv., ahead-of-print (Available online 2 June 2015) 1-9.
40. Yuan H., Miao J., Du Y.Z., You J., Hu F.Q., Zeng S. Cellular uptake of solid lipid nanoparticles and cytotoxicity of encapsulated paclitaxel in A549 cancer cells. Int. J. Pharm. 2008, 348:137-145.
41. Sheridan C., Kishimoto H., Fuchs R.K., Mehrotra S., Bhat-Nakshatri P., Turner C.H., Goulet R., Badve S., Nakshatri H. CD44+/CD24-breast cancer cells exhibit enhanced invasive properties: an early step necessary for metastasis. Breast Cancer Res. 2006, 8:R59.
42. Levy-Nissenbaum E., Khan W., Pawar R.P., Tabakman R., Naftali E., Winkler I., Kaufman O., Klapper L., Domb A.J. Pharmacokinetic and efficacy study of cisplatin and paclitaxel formulated in a new injectable poly (sebacic-co-ricinoleic acid) polymer. Eur. J. Pharm. Biopharm. 2012, 82:85-93.
43. Sparidans R.W., Lagas J.S., Schinkel A.H., Schellens J.H., Beijnen J.H. Liquid chromatography-tandem mass spectrometric assays for salinomycin in mouse plasma liver, brain and small intestinal contents and in OptiMEM cell culture medium. J. Chromatogr. B 2007, 855:200-210.
44. Litzinger D.C., Buiting A.M., van Rooijen N., Huang L. Effect of liposome size on the circulation time and intraorgan distribution of amphipathic poly (ethylene glycol)-containing liposomes. BBA Biomembr. 1994, 1190:99-107.
45. Xu Z., Gu W., Huang J., Sui H., Zhou Z., Yang Y., Yan Z., Li Y. In vitro and in vivo evaluation of actively targetable nanoparticles for paclitaxel delivery. Int. J. Pharm. 2005, 288:361-368.
46. Song K.C., Lee H.S., Choung I.Y., Cho K.I., Ahn Y., Choi E.J. The effect of type of organic phase solvents on the particle size of poly (d, l-lactide-co-glycolide) nanoparticles. Colloids Surf. A 2006, 276:162-167.
47. Vandervoort J., Ludwig A. Biocompatible stabilizers in the preparation of PLGA nanoparticles: a factorial design study. Int. J. Pharm. 2002, 238:77-92.
48. Peetla C., Labhasetwar V. Effect of molecular structure of cationic surfactants on biophysical interactions of surfactant-modified nanoparticles with a model membrane and cellular uptake. Langmuir 2009, 25:2369-2377.
49. Ahlin P., Kristl J., Kristl A., Vrecer F. Investigation of polymeric nanoparticles as carriers of enalaprilat for oral administration. Int. J. Pharm. 2002, 239:113-120.
50. N. Sharma, P. Madan, S. Lin, Effect of process and formulation variables on the preparation of parenteral paclitaxel-loaded biodegradable polymeric nanoparticles: A co-surfactant study Asian, J. Pharmaceut. Sci. (Available online 1 October 2015 in press).
51. Bhardwaj V., Ankola D.D., Gupta S.C., Schneider M., Lehr C.M., Kumar M.N.V.R. PLGA nanoparticles stabilized with cationic surfactant: safety studies and application in oral delivery of paclitaxel to treat chemical-induced breast cancer in rat. Pharm. Res. 2009, 26:2495-2503.
52. Choi K.Y., Chung H., Min K.H., Yoon H.Y., Kim K., Park J.H., Kwon I.C., Jeong S.Y. Self-assembled hyaluronic acid nanoparticles for active tumor targeting. Biomaterials 2010, 31:106-114.
53. Negi L.M., Jaggi M., Joshi V., Ronodip K., Talegaonkar S. Hyaluronic acid decorated lipid nanocarrier for MDR modulation and CD-44 targeting in colon adenocarcinoma. Int. J. Biol. Macromol. 2015, 72:569-574.
54. Shen H., Shi S., Zhang Z., Gong T., Sun X. Coating solid lipid nanoparticles with hyaluronic acid enhances antitumor activity against melanoma stem-like cells. Theranostics 2015, 5:755-771.
55. ®) from nanospheres of biodegradable polymers. J. Controlled Release 2001, 71:53-69.
56. Wischke C., Schwendeman S.P. Principles of encapsulating hydrophobic drugs in PLA/PLGA microparticles. Int. J. Pharm. 2008, 364:298-327.
57. Hines D.J., Kaplan D.L. Poly (lactic-co-glycolic) acid- controlled-release systems: experimental and modeling insights. Crit. Rev. Ther. Drug 2013, 30:257-276.
58. Fonseca C., Simoes S., Gaspar R. Paclitaxel-loaded PLGA nanoparticles: preparation, physicochemical characterization and in vitro anti-tumoral activity. J. Controlled Release 2002, 83:273-286.
59. Danhier F., Lecouturier N., Vroman B., Jerome C., Marchand-Brynaert J., Feron O., Preat V. Paclitaxel-loaded PEGylated PLGA-based nanoparticles: in vitro and in vivo evaluation. J. Controlled Release 2009, 133:11-17.
60. Holy C.E., Dang S.M., Davies J.E., Shoichet M.S. In vitro degradation of a novel poly (lactide-co-glycolide) 75/25 foam. Biomaterials 1999, 20:1177-1185.
61. Baek N., Lee J., Park K., Aqueous N. N-diethylnicotinamide (DENA) solution as a medium for accelerated release study of paclitaxel. J. Biomater. Sci. Polym. Ed. 2004, 15:527-542.
62. Kesharwani P., Xie L., Mao G., Padhye S., Iyer A.K. Hyaluronic acid-conjugated polyamidoamine dendrimers for targeted delivery of 3, 4-difluorobenzylidene curcumin to CD44 overexpressing pancreatic cancer cells. Colloids Surf. B 2015, 136:413-423.
63. Singh A., Talekar M., Tran T.-H., Samanta A., Sundaram R., Amiji M. Combinatorial approach in the design of multifunctional polymeric nano-delivery systems for cancer therapy. J. Mater. Chem. B 2014, 2:8069-8084.
64. Wang B., Yu X.-C., Xu S.-F., Xu M. Paclitaxel and etoposide co-loaded polymeric nanoparticles for the effective combination therapy against human osteosarcoma. J. Nanobiotechnol. 2015, 13:1-11.
65. Ajabnoor G., Crook T., Coley H.M. Paclitaxel resistance is associated with switch from apoptotic to autophagic cell death in MCF-7 breast cancer cells. Cell Death Dis. 2012, 3:e260.
66. Al Dhaheri Y., Attoub S., Arafat K., AbuQamar S., Eid A., Al Faresi N., Iratni R. Salinomycin induces apoptosis and senescence in breast cancer: upregulation of p21 downregulation of survivin and histone H3 and H4 hyperacetylation. BBA Gen. Subj. 2013, 1830:3121-3135.
67. Koo K., Kim H., Bae Y., Kim K., Park B., Lee C., Kim Y. Salinomycin induces cell death via inactivation of Stat3 and downregulation of Skp2. Cell Death Dis. 2013, 4:e693.
68. G.G. Powathil, M.A. Chaplain, M. Swat, Investigating the development of chemotherapeutic drug resistance in cancer: A multiscale computational study, arXiv:1407.0865 (2014).
69. Lee S.S., Lee Y.B., Oh I.J. Cellular uptake of poly (dl-lactide-co-glycolide) nanoparticles: effects of drugs and surface characteristics of nanoparticles. J. Pharm. Invest. 2015, 45:659-667.
70. Qhattal H.S.S., Liu X. Characterization of CD44-mediated cancer cell uptake and intracellular distribution of hyaluronan-grafted liposomes. Mol. Pharm. 2011, 8:1233-1246.
71. van Vlerken L.E., Duan Z., Little S.R., Seiden M.V., Amiji M.M. Biodistribution and pharmacokinetic analysis of paclitaxel and ceramide administered in multifunctional polymer-blend nanoparticles in drug resistant breast cancer model. Mol. Pharm. 2008, 5:516-526.
72. Resham K., Patel P.N., Thummuri D., Guntuku L., Shah V., Bambal R.B., Naidu V. Preclinical drug metabolism and pharmacokinetics of salinomycin, a potential candidate for targeting human cancer stem cells. Chem. Biol. Interact. 2015, 240:146-152.