Microfluidic assembly of a nano-in-micro dual drug delivery platform composed of halloysite nanotubes and a pH-responsive polymer for colon cancer therapy

Acta Biomaterialia

Volumn 48, Issue , 2017, Pages 238-246

  Li, Wei ^a   Liu, Dongfei ^a   Zhang, Hongbo ^a   Correia, Alexandra ^a   Mäkilä, Ermei ^b   Salonen, Jarno ^b   Hirvonen, Jouni ^a   Santos, Hélder A ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

^b UNIVERSITY OF TURKU   (Finland)

Author keywords

Dual delivery; Halloysite nanotubes; Microfluidics; Oral delivery; pH responsive

Indexed keywords

CELL PROLIFERATION; CONTROLLED DRUG DELIVERY; DISEASES; KAOLINITE; MICROFLUIDICS; NANOTUBES; ONCOLOGY; PARTICLE SIZE; PARTICLE SIZE ANALYSIS; TARGETED DRUG DELIVERY; YARN;

CANCER THERAPY; COLON CANCER; CONDITION; DUAL DELIVERY; GASTROINTESTINAL TRACT; HALLOYSITE NANOTUBES; ORAL DELIVERY; ORAL DRUG DELIVERY SYSTEM; PH-RESPONSIVE; PH-RESPONSIVE POLYMER;

MICROSPHERES;

ATORVASTATIN; CELECOXIB; HALLOYSITE NANOTUBE; HYDROXYPROPYLMETHYLCELLULOSE ACETATE SUCCINATE; MICROSPHERE; NANOTUBE; UNCLASSIFIED DRUG; ALUMINUM SILICATE; CLAY; POLYMER;

ARTICLE; COLON ADENOCARCINOMA; COLON CANCER; COLON CARCINOMA; CONTROLLED STUDY; DISSOLUTION; DRUG DELIVERY SYSTEM; DRUG PENETRATION; DRUG POTENTIATION; DRUG RELEASE; DRUG SOLUBILITY; HUMAN; HUMAN CELL; HYDROPHOBICITY; MICROFLUIDICS; PARTICLE SIZE; PH; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; CACO-2 CELL LINE; CELL DEATH; CELL PROLIFERATION; CELL SURVIVAL; CHEMISTRY; COLONIC NEOPLASMS; DRUG EFFECTS; HT-29 CELL LINE; PATHOLOGY; PERMEABILITY; PROCEDURES; ULTRASTRUCTURE;

ALUMINUM SILICATES; ATORVASTATIN CALCIUM; CACO-2 CELLS; CELECOXIB; CELL DEATH; CELL PROLIFERATION; CELL SURVIVAL; COLONIC NEOPLASMS; DRUG DELIVERY SYSTEMS; DRUG LIBERATION; HT29 CELLS; HUMANS; HYDROGEN-ION CONCENTRATION; MICROFLUIDICS; MICROSPHERES; NANOTUBES; PERMEABILITY; POLYMERS;

EID: 85006305733     PISSN: 17427061     EISSN: 18787568     Source Type: Journal    
DOI: 10.1016/j.actbio.2016.10.042     Document Type: Article

References (52)

1. [1] Thanki, K., Gangwal, R.P., Sangamwar, A.T., Jain, S., Oral delivery of anticancer drugs: challenges and opportunities. J. Controlled Release 170 (2013), 15–40.
2. [2] Goldberg, M., Gomez-Orellana, I., Challenges for the oral delivery of macromolecules. Nat. Rev. Drug Discovery 2 (2003), 289–295.
3. [3] Ghaffarian, R., Pérez-Herrero, E., Oh, H., Raghavan, S.R., Muro, S., Chitosan-alginate microcapsules provide gastric protection and intestinal release of ICAM-1-targeting nanocarriers, enabling gi targeting in vivo. Adv. Funct. Mater. 26 (2016), 3382–3393.
4. [4] Zhang, H., Shahbazi, M.-A., Mäkilä, E.M., da Silva, T.H., Reis, R.L., Salonen, J.J., Hirvonen, J.T., Santos, H.A., Diatom silica microparticles for sustained release and permeation enhancement following oral delivery of prednisone and mesalamine. Biomaterials 34 (2013), 9210–9219.
5. [5] Zhang, H., Liu, D., Shahbazi, M.-A., Mäkilä, E., Herranz-Blanco, B., Salonen, J., Hirvonen, J., Santos, H.A., Fabrication of a multifunctional nano-in-micro drug delivery platform by microfluidic templated encapsulation of porous silicon in polymer matrix. Adv. Mater. 26 (2014), 4497–4503.
6. [6] Fox, C.B., Kim, J., Le, L.V., Nemeth, C.L., Chirra, H.D., Desai, T.A., Micro/nanofabricated platforms for oral drug delivery. J. Controlled Release 219 (2015), 431–444.
7. [7] Lvov, Y., Wang, W., Zhang, L., Fakhrullin, R., Halloysite clay nanotubes for loading and sustained release of functional compounds. Adv. Mater. 28 (2016), 1227–1250.
8. [8] Jana, S., Das, S., Ghosh, C., Maity, A., Pradhan, M., Halloysite nanotubes capturing isotope selective atmospheric CO2. Sci. Rep., 5, 2015, 8711.
9. [9] Dai, J., Wei, X., Cao, Z., Zhou, Z., Yu, P., Pan, J., Zou, T., Li, C., Yan, Y., Highly-controllable imprinted polymer nanoshell at the surface of magnetic halloysite nanotubes for selective recognition and rapid adsorption of tetracycline. RSC Adv. 4 (2014), 7967–7978.
10. [10] Xue, J., Niu, Y., Gong, M., Shi, R., Chen, D., Zhang, L., Lvov, Y., Electrospun microfiber membranes embedded with drug-loaded clay nanotubes for sustained antimicrobial protection. ACS Nano 9 (2015), 1600–1612.
11. [11] Naumenko, E.A., Guryanov, I.D., Yendluri, R., Lvov, Y.M., Fakhrullin, R.F., Clay nanotube-biopolymer composite scaffolds for tissue engineering. Nanoscale 8 (2016), 7257–7271.
12. [12] Qi, R.L., Guo, R., Zheng, F.Y., Liu, H., Yu, J.Y., Shi, X.Y., Controlled release and antibacterial activity of antibiotic-loaded electrospun halloysite/poly(lactic-co-glycolic acid) composite nanofibers. Colloids Surf. B 110 (2013), 148–155.
13. [13] Liu, M., Wu, C., Jiao, Y., Xiong, S., Zhou, C., Chitosan-halloysite nanotubes nanocomposite scaffolds for tissue engineering. J. Mater. Chem. B 1 (2013), 2078–2089.
14. [14] Lvov, Y.M., Shchukin, D.G., Mohwald, H., Price, R.R., Halloysite clay nanotubes for controlled release of protective agents. ACS Nano 2 (2008), 814–820.
15. [15] Qi, R.L., Guo, R., Shen, M.W., Cao, X.Y., Zhang, L.Q., Xu, J.J., Yu, J.Y., Shi, X.Y., Electrospun poly(lactic-co-glycolicacid)/halloysite nanotube composite nanofibers for drug encapsulation and sustained release. J. Mater. Chem. 20 (2010), 10622–10629.
16. [16] Wang, Y., Deen, I., Zhitomirsky, I., Electrophoretic deposition of polyacrylic acid and composite films containing nanotubes and oxide particles. J. Colloid Interface Sci. 362 (2011), 367–374.
17. [17] Mitchell, M.J., Chen, C.S., Ponmudi, V., Hughes, A.D., King, M.R., E-selectin liposomal and nanotube-targeted delivery of doxorubicin to circulating tumor cells. J. Control. Release 160 (2012), 609–617.
18. [18] Vergaro, V., Lvov, Y.M., Leporatti, S., Halloysite clay nanotubes for resveratrol delivery to cancer cells. Macromol. Biosci. 12 (2012), 1265–1271.
19. [19] Dzamukova, M.R., Naumenko, E.A., Lvov, Y.M., Fakhrullin, R.F., Enzyme-activated intracellular drug delivery with tubule clay nanoformulation. Sci. Rep., 5, 2015, 10560.
20. [20] Vergaro, V., Abdullayev, E., Lvov, Y.M., Zeitoun, A., Cingolani, R., Rinaldi, R., Leporatti, S., Cytocompatibility and uptake of halloysite clay nanotubes. Biomacromolecules 11 (2010), 820–826.
21. [21] Ahmed, F.R., Shoaib, M.H., Azhar, M., Um, S.H., Yousuf, R.I., Hashmi, S., Dar, A., In-vitro assessment of cytotoxicity of halloysite nanotubes against HepG2, HCT116 and human peripheral blood lymphocytes. Colloids Surf. B 135 (2015), 50–55.
22. [22] Lai, X., Agarwal, M., Lvov, Y.M., Pachpande, C., Varahramyan, K., Witzmann, F.A., Proteomic profiling of halloysite clay nanotube exposure in intestinal cell co-culture. J. Appl. Toxicol. 33 (2013), 1316–1329.
23. [23] Zhang, Y., Gao, R., Liu, M., Yan, C., Shan, A., Adsorption of modified halloysite nanotubes in vitro and the protective effect in rats exposed to zearalenone. Arch. Anim. Nutr. 68 (2014), 320–335.
24. [24] Kırımlıoğlu, G.Y., Yazan, Y., Erol, K., Çengelli, Ünel.Ç., Gamma-aminobutyric acid loaded halloysite nanotubes and in vitro-in vivo evaluation for brain delivery. Int. J. Pharm. 495 (2015), 816–826.
25. [25] Bellani, L., Giorgetti, L., Riela, S., Lazzara, G., Scialabba, A., Massaro, M., Ecotoxicity of halloysite nanotube–supported palladium nanoparticles in Raphanus sativus L. Environ. Toxicol. Chem. 35 (2016), 2503–2510.
26. [26] Kryuchkova, M., Danilushkina, A., Lvov, Y., Fakhrullin, R., Evaluation of toxicity of nanoclays and graphene oxide in vivo: a Paramecium caudatum study. Environ. Sci. Nano 3 (2016), 442–452.
27. [27] Liu, M., Chang, Y., Yang, J., You, Y., He, R., Chen, T., Zhou, C., Functionalized halloysite nanotube by chitosan grafting for drug delivery of curcumin to achieve enhanced anticancer efficacy. J. Mater. Chem. B 4 (2016), 2253–2263.
28. [28] Fakhrullina, G.I., Akhatova, F.S., Lvov, Y.M., Fakhrullin, R.F., Toxicity of halloysite clay nanotubes in vivo: a Caenorhabditis elegans study. Environ. Sci. Nano 2 (2015), 54–59.
29. [29] Tully, J., Yendluri, R., Lvov, Y., Halloysite clay nanotubes for enzyme immobilization. Biomacromolecules 17 (2015), 615–621.
30. [30] Price BPGYLR, R., In-vitro release characteristics of tetracycline HCl, khellin and nicotinamide adenine dineculeotide from halloysite; a cylindrical mineral. J. Microencapsulation 18 (2001), 713–722.
31. [31] Fan, L., Zhang, J., Wang, A., In situ generation of sodium alginate/hydroxyapatite/halloysite nanotubes nanocomposite hydrogel beads as drug-controlled release matrices. J. Mater. Chem. B, 1, 2013, 6261.
32. [32] de Kruif, J.K., Ledergerber, G., Garofalo, C., Fasler-Kan, E., Kuentz, M., On prilled nanotubes-in-microgel oral systems for protein delivery. Eur. J. Pharm. Biopharm. 101 (2016), 90–102.
33. [33] Abdullayev, E., Joshi, A., Wei, W., Zhao, Y., Lvov, Y., Enlargement of halloysite clay nanotube lumen by selective etching of aluminum oxide. ACS Nano 6 (2012), 7216–7226.
34. [34] Forsgren, J., Jämstorp, E., Bredenberg, S., Engqvist, H., Strømme, M., A ceramic drug delivery vehicle for oral administration of highly potent opioids. J. Pharm. Sci. 99 (2010), 219–226.
35. [35] Lvov, Y.M., DeVilliers, M.M., Fakhrullin, R.F., The application of halloysite tubule nanoclay in drug delivery. Expert Opin. Drug. Delivery 13 (2016), 977–986.
36. [36] Liu, D., Zhang, H., Herranz-Blanco, B., Mäkilä, E., Lehto, V.-P., Salonen, J., Hirvonen, J., Santos, H.A., Microfluidic assembly of monodisperse multistage pH-responsive polymer/porous silicon composites for precisely controlled multi-drug delivery. Small 10 (2014), 2029–2038.
37. [37] Hasani-Sadrabadi, M.M., Taranejoo, S., Dashtimoghadam, E., Bahlakeh, G., Majedi, F.S., VanDersarl, J.J., Janmaleki, M., Sharifi, F., Bertsch, A., Hourigan, K., Tayebi, L., Renaud, P., Jacob, K.I., Microfluidic manipulation of core/shell nanoparticles for oral delivery of chemotherapeutics: a new treatment approach for colorectal cancer. Adv. Mater. 28 (2016), 4134–4141.
38. [38] Imperiale, J.C., Nejamkin, P., del, Sole, M.J., Lanusse, E., Sosnik, C., A. Novel protease inhibitor-loaded nanoparticle-in-microparticle delivery system leads to a dramatic improvement of the oral pharmacokinetics in dogs. Biomaterials 37 (2015), 383–394.
39. [39] Li, W., Jan, Z., Ding, Y., Liu, Y., Janko, C., Pischetsrieder, M., Alexiou, C., Boccaccini, A.R., Facile preparation of multifunctional superparamagnetic PHBV microspheres containing SPIONs for biomedical applications. Sci. Rep., 6, 2016, 23140.
40. [40] Fan, D., De Rosa, E., Murphy, M.B., Peng, Y., Smid, C.A., Chiappini, C., Liu, X., Simmons, P., Weiner, B.K., Ferrari, M., Tasciotti, E., Mesoporous silicon-PLGA composite microspheres for the double controlled release of biomolecules for orthopedic tissue engineering. Adv. Funct. Mater. 22 (2012), 282–293.
41. [41] Duncanson, W.J., Lin, T., Abate, A.R., Seiffert, S., Shah, R.K., Weitz, D.A., Microfluidic synthesis of advanced microparticles for encapsulation and controlled release. Lab Chip 12 (2012), 2135–2145.
42. [42] Teh, S.-Y., Lin, R., Hung, L.-H., Lee, A.P., Droplet microfluidics. Lab Chip 8 (2008), 198–220.
43. [43] Araújo, F., Shrestha, N., Shahbazi, M.-A., Liu, D., Herranz-Blanco, B., Mäkilä, E.M., Salonen, J.J., Hirvonen, J.T., Granja, P.L., Sarmento, B., Santos, H.A., Microfluidic assembly of a multifunctional tailorable composite system designed for site specific combined oral delivery of peptide drugs. ACS Nano 9 (2015), 8291–8302.
44. [44] Fontana, F., Ferreira, M.P.A., Correia, A., Hirvonen, J., Santos, H.A., Microfluidics as a cutting-edge technique for drug delivery applications. J. Drug. Delivery Sci. Technol. 34 (2016), 76–87.
45. [45] Xiao, H., Yang, C.S., Combination regimen with statins and NSAIDs: a promising strategy for cancer chemoprevention. Int. J. Cancer 123 (2008), 983–990.
46. [46] Reddy, B.S., Wang, C.X., Kong, A.N., Khor, T.O., Zheng, X., Steele, V.E., Kopelovich, L., Rao, C.V., Prevention of azoxymethane-induced colon cancer by combination of low doses of atorvastatin, aspirin, and celecoxib in F 344 rats. Int. Cancer Res. 66 (2006), 4542–4546.
47. [47] Xiao, H., Zhang, Q., Lin, Y., Reddy, B.S., Yang, C.S., Combination of atorvastatin and celecoxib synergistically induces cell cycle arrest and apoptosis in colon cancer cells. Int. J. Cancer 122 (2008), 2115–2124.
48. [48] Brunauer, S., Emmett, P.H., Teller, E., Adsorption of gases in multimolecular layers. J. Am. Chem. Soc. 60 (1938), 309–319.
49. [49] Chu, L.Y., Kim, J.W., Shah, R.K., Weitz, D.A., Monodisperse thermoresponsive microgels with tunable volume-phase transition kinetics. Adv. Funct. Mater. 17 (2007), 3499–3504.
50. [50] Liu, D., Bimbo, L.M., Mäkilä, E., Villanova, F., Kaasalainen, M., Herranz, B., Caramella, C.M., Lehto, V.-P., Salonen, J., Herzig, K.-H., Hirvonen, J., Santos, H.A., Co-delivery of a hydrophobic small molecule and a hydrophilic peptide by porous silicon nanoparticles. J. Control. Release 170 (2013), 268–278.
51. [51] Massaro, M., Riela, S., Baiamonte, C., Blanco, J.L.J., Giordano, C., Lo Meo, P., Milioto, S., Noto, R., Parisi, F., Pizzolanti, G., Lazzara, G., Dual drug-loaded halloysite hybrid-based glycocluster for sustained release of hydrophobic molecules. RSC Adv. 6 (2016), 87935–87944.
52. [52] Hilgendorf, C., Spahn-Langguth, H., Regårdh, C.G., Lipka, E., Amidon, G.L., Langguth, P., Caco-2 versus Caco-2/HT29-MTX Co-cultured cell lines: permeabilities via diffusion, inside- and outside-directed carrier-mediated transport. J. Pharm. Sci. 89 (2000), 63–75.