162
Views
0
CrossRef citations to date
0
Altmetric
ORIGINAL RESEARCH

Oral Delivery of Photopolymerizable Nanogels Loaded with Gemcitabine for Pancreatic Cancer Therapy: Formulation Design, and in vitro and in vivo Evaluations

, , , , ORCID Icon, & ORCID Icon show all
Pages 3753-3772 | Received 02 Dec 2023, Accepted 19 Apr 2024, Published online: 24 Apr 2024

References

  • Sung H, Ferlay J, Siegel RL, et al. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2021;71(3):209–249. doi:10.3322/caac.21660
  • Reni M, Cordio S, Milandri C, et al. Gemcitabine versus cisplatin, epirubicin, fluorouracil, and gemcitabine in advanced pancreatic cancer: a randomised controlled multicentre Phase III trial. Lancet Oncol. 2005;6(6):369–376. doi:10.1016/S1470-2045(05)70175-3
  • Abbruzzese JL, Grunewald R, Weeks EA, et al. A Phase I clinical, plasma, and cellular pharmacology study of gemcitabine. J Clin Oncol. 1991;9(3):491–498. doi:10.1200/JCO.1991.9.3.491
  • Reid JM, Qu W, Safgren SL, et al. Phase I trial and pharmacokinetics of gemcitabine in children with advanced solid tumors. J Clin Oncol. 2004;22(12):2445–2451. doi:10.1200/JCO.2004.10.142
  • Moog R, Burger A, Brandl M, et al. Change in pharmacokinetic and pharmacodynamic behavior of gemcitabine in human tumor xenografts upon entrapment in vesicular phospholipid gels. Cancer Chemother Pharmacol. 2002;49(5):356–366. doi:10.1007/s00280-002-0428-4
  • Immordino ML, Brusa P, Rocco F, Arpicco S, Ceruti M, Cattel L. Preparation, characterization, cytotoxicity and pharmacokinetics of liposomes containing lipophilic gemcitabine prodrugs. J Control Release. 2004;100(3):331–346. doi:10.1016/j.jconrel.2004.09.001
  • Derakhshandeh K, Fathi S. Role of chitosan nanoparticles in the oral absorption of Gemcitabine. Int J Pharm. 2012;437(1–2):172–177. doi:10.1016/j.ijpharm.2012.08.008
  • Kawazoe H, Mori N, Ido S, et al. Liquid formulation of gemcitabine increases venous pain in patients with cancer: a retrospective study. Clin Ther. 2020;42(4):712–719. doi:10.1016/j.clinthera.2020.02.010
  • Arciero V, Luo J, Parmar A, et al. Real-world cost-effectiveness of first-line gemcitabine plus nab-paclitaxel vs FOLFIRINOX in patients with advanced pancreatic cancer. JNCI Cancer Spectr. 2022;6(4). doi:10.1093/jncics/pkac047
  • Plunkett W, Huang P, Xu YZ, Heinemann V, Grunewald R, Gandhi V. Gemcitabine: metabolism, mechanisms of action, and self-potentiation. Semin Oncol. 1995;22(4):3–10.
  • Samanta K, Setua S, Kumari S, Jaggi M, Yallapu MM, Chauhan SC. Gemcitabine combination nano therapies for pancreatic cancer. Pharmaceutics. 2019;11(11):574. doi:10.3390/pharmaceutics11110574
  • Tan M, Luo J, Tian Y. Delivering curcumin and gemcitabine in one nanoparticle platform for colon cancer therapy. RSC Adv. 2014;4(106):61948–61959. doi:10.1039/C4RA10431E
  • Semaan A, Maitra A. Rebooting pancreatic cancer knowledge and treatment options. Nat Rev Gastroenterol Hepatol. 2018;15(2):76–78. doi:10.1038/nrgastro.2017.182
  • Adiseshaiah PP, Crist RM, Hook SS, McNeil SE. Nanomedicine strategies to overcome the pathophysiological barriers of pancreatic cancer. Nat Rev Clin Oncol. 2016;13(12):750–765. doi:10.1038/nrclinonc.2016.119
  • Bastiancich C, Vanvarenberg K, Ucakar B, et al. Lauroyl-gemcitabine-loaded lipid nanocapsule hydrogel for the treatment of glioblastoma. J Control Release. 2016;225:283–293. doi:10.1016/j.jconrel.2016.01.054
  • Bastiancich C, Bianco J, Vanvarenberg K, et al. Injectable nanomedicine hydrogel for local chemotherapy of glioblastoma after surgical resection. J Control Release. 2017;264:45–54. doi:10.1016/j.jconrel.2017.08.019
  • Qin L, Ling G, Peng F, et al. Black phosphorus nanosheets and gemcitabine encapsulated thermo-sensitive hydrogel for synergistic photothermal-chemotherapy. J Colloid Interface Sci. 2019;556:232–238. doi:10.1016/j.jcis.2019.08.058
  • Schneible JD, Shi K, Young AT, et al. Modified graphene oxide (GO) particles in peptide hydrogels: a hybrid system enabling scheduled delivery of synergistic combinations of chemotherapeutics. J Mater Chem B. 2020;8(17):3852. doi:10.1039/D0TB00064G
  • Moysan E, González-Fernández Y, Lautram N, Béjaud J, Bastiat G, Benoit JP. An innovative hydrogel of gemcitabine-loaded lipid nanocapsules: when the drug is a key player of the nanomedicine structure. Soft Matter. 2014;10(11):1767–1777. doi:10.1039/c3sm52781f
  • Bilalis P, Skoulas D, Karatzas A, et al. Self-healing pH- and enzyme stimuli-responsive hydrogels for targeted delivery of gemcitabine to treat pancreatic cancer. Biomacromolecules. 2018;19(9):3840–3852. doi:10.1021/acs.biomac.8b00959
  • Wang J, Leng Q, Li Y, et al. Injectable hyaluronic acid hydrogel for the co-delivery of gemcitabine nanoparticles and cisplatin for malignant ascites therapy. J Biomed Nanotechnol. 2020;16(12):1727–1739. doi:10.1166/jbn.2020.3002
  • Wu W, Dai Y, Liu H, et al. Local release of gemcitabine via in situ UV-crosslinked lipid-strengthened hydrogel for inhibiting osteosarcoma. Drug Deliv. 2018;25(1):1642. doi:10.1080/10717544.2018.1497105
  • Wang W, Wang B, Liu S, et al. Bioreducible polymer nanocarrier based on multivalent choline phosphate for enhanced cellular uptake and intracellular delivery of doxorubicin. ACS Appl Mater Interfaces. 2017;9(19):15986–15994. doi:10.1021/acsami.7b03317
  • Bastiancich C, Bozzato E, Luyten U, Danhier F, Bastiat G, Préat V. Drug combination using an injectable nanomedicine hydrogel for glioblastoma treatment. Int J Pharm. 2019;559:220–227. doi:10.1016/j.ijpharm.2019.01.042
  • Zhuang B, Chen T, Xiao Z, Jin Y. Drug-loaded implantable surgical cavity-adaptive hydrogels for prevention of local tumor recurrence. Int J Pharm. 2020;577:119048. doi:10.1016/j.ijpharm.2020.119048
  • Schneible JD, Young AT, Daniele MA, Menegatti S. Chitosan hydrogels for synergistic delivery of chemotherapeutics to triple negative breast cancer cells and spheroids. Pharm Res. 2020;37(7). doi:10.1007/s11095-020-02864-2
  • Shabana AM, Kambhampati SP, ching HR, Kannan RM, Kokkoli E. Thermosensitive and biodegradable hydrogel encapsulating targeted nanoparticles for the sustained co-delivery of gemcitabine and paclitaxel to pancreatic cancer cells. Int J Pharm. 2021;593:120139. doi:10.1016/j.ijpharm.2020.120139
  • Wang C, Zhang G, Liu G, Hu J, Liu S. Photo- and thermo-responsive multicompartment hydrogels for synergistic delivery of gemcitabine and doxorubicin. J Control Release. 2017;259:149–159. doi:10.1016/j.jconrel.2016.11.007
  • Date AA, Hanes J, Ensign LM. Nanoparticles for oral delivery: design, evaluation and state-of-The-art. J Control Release. 2016;240:504–526. doi:10.1016/j.jconrel.2016.06.016
  • Des Rieux A, Fievez V, Garinot M, Schneider YJ, Préat V. Nanoparticles as potential oral delivery systems of proteins and vaccines: a mechanistic approach. J Control Release. 2006;116(1):1–27. doi:10.1016/j.jconrel.2006.08.013
  • Ensign LM, Cone R, Hanes J. Oral drug delivery with polymeric nanoparticles: the gastrointestinal mucus barriers. Adv Drug Deliv Rev. 2012;64(6):557–570. doi:10.1016/j.addr.2011.12.009
  • Kim KS, Suzuki K, Cho H, Youn YS, Bae YH. Oral nanoparticles exhibit specific high-efficiency intestinal uptake and lymphatic transport. ACS Nano. 2018;12(9):8893–8900. doi:10.1021/acsnano.8b04315
  • Beloqui A, Des Rieux A, Préat V. Mechanisms of transport of polymeric and lipidic nanoparticles across the intestinal barrier. Adv Drug Deliv Rev. 2016;106(Pt B):242–255. doi:10.1016/j.addr.2016.04.014
  • Jin L, Wang Q, Chen J, Wang Z, Xin H, Zhang D. Efficient delivery of therapeutic siRNA by Fe3O4 magnetic nanoparticles into oral cancer cells. Pharmaceutics. 2019;11(11):615. doi:10.3390/pharmaceutics11110615
  • Zhang W, Zheng N, Chen L, et al. Effect of shape on mesoporous silica nanoparticles for oral delivery of indomethacin. Pharmaceutics. 2019;11(1):4.
  • Lamson NG, Berger A, Fein KC, Whitehead KA. Anionic nanoparticles enable the oral delivery of proteins by enhancing intestinal permeability. Nat Biomed Eng. 2020;4(1):84–96. doi:10.1038/s41551-019-0465-5
  • Du X, Yin S, Xu L, et al. Polylysine and cysteine functionalized chitosan nanoparticle as an efficient platform for oral delivery of paclitaxel. Carbohydr Polym. 2020;229:115484. doi:10.1016/j.carbpol.2019.115484
  • Sorasitthiyanukarn FN, Muangnoi C, Ratnatilaka Na Bhuket P, Rojsitthisak P, Rojsitthisak P. Chitosan/alginate nanoparticles as a promising approach for oral delivery of curcumin diglutaric acid for cancer treatment. Mater Sci Eng C Mater Biol Appl. 2018;93:178–190. doi:10.1016/j.msec.2018.07.069
  • Khan AA, Mudassir J, Akhtar S, Murugaiyah V, Darwis Y. Freeze-dried lopinavir-loaded nanostructured lipid carriers for enhanced cellular uptake and bioavailability: statistical optimization, in vitro and in vivo evaluations. Pharmaceutics. 2019;11(2):97. doi:10.3390/pharmaceutics11020097
  • Hanurry EY, Mekonnen TW, Andrgie AT, et al. Biotin-decorated PAMAM G4.5 dendrimer nanoparticles to enhance the delivery, anti-proliferative, and apoptotic effects of chemotherapeutic drug in cancer cells. Pharmaceutics. 2020;12(5):443. doi:10.3390/pharmaceutics12050443
  • Peppas NA, Bures P, Leobandung W, Ichikawa H. Hydrogels in pharmaceutical formulations. Eur J Pharm Biopharm. 2000;50(1):27–46. doi:10.1016/S0939-6411(00)00090-4
  • Qiu Y, Park K. Environment-sensitive hydrogels for drug delivery. Adv Drug Deliv Rev. 2001;53(3):321–339. doi:10.1016/S0169-409X(01)00203-4
  • Peppas NA, Hilt JZ, Khademhosseini A, Langer R. Hydrogels in biology and medicine: from molecular principles to bionanotechnology. Adv Mater. 2006;18(11):1345–1360. doi:10.1002/adma.200501612
  • Hoare TR, Kohane DS. Hydrogels in drug delivery: progress and challenges. Polymer. 2008;49(8):1993–2007. doi:10.1016/j.polymer.2008.01.027
  • Li J, Mooney DJ. Designing hydrogels for controlled drug delivery. Nature Rev Mater. 2016;1(12):1–17. doi:10.1038/natrevmats.2016.71
  • Chen W, Zou Y, Zhong Z, Haag R. Cyclo(RGD)-decorated reduction-responsive nanogels mediate targeted chemotherapy of integrin overexpressing human glioblastoma in vivo. Small. 2017;13(6):1601997.
  • Cuggino JC, Molina M, Wedepohl S, Igarzabal CIA, Calderón M, Gugliotta LM. Responsive nanogels for application as smart carriers in endocytic pH-triggered drug delivery systems. Eur Polym J. 2016;78:14–24. doi:10.1016/j.eurpolymj.2016.02.022
  • Cuggino JC, Gatti G, Picchio ML, Maccioni M, Gugliotta LM, Alvarez Igarzabal CI. Dually responsive nanogels as smart carriers for improving the therapeutic index of doxorubicin for breast cancer. Eur Polym J. 2019;116:445–452. doi:10.1016/j.eurpolymj.2019.04.031
  • Hajebi S, Rabiee N, Bagherzadeh M, et al. Stimulus-responsive polymeric nanogels as smart drug delivery systems. Acta Biomater. 2019;92:1. doi:10.1016/j.actbio.2019.05.018
  • Liu B, Thayumanavan S. Substituent effects on the pH sensitivity of acetals and ketals and their correlation with encapsulation stability in polymeric nanogels. J Am Chem Soc. 2017;139(6):2306–2317. doi:10.1021/jacs.6b11181
  • Liechty WB, Peppas NA. Expert opinion: responsive polymer nanoparticles in cancer therapy. Eur J Pharm Biopharm. 2012;80(2):241–246. doi:10.1016/j.ejpb.2011.08.004
  • Maya S, Sarmento B, Nair A, Rejinold N, Nair S, Jayakumar R. Smart stimuli sensitive nanogels in cancer drug delivery and imaging: a review. Curr Pharm Des. 2013;19(41):7203–7218. doi:10.2174/138161281941131219124142
  • Oishi M, Nagasaki Y. Stimuli-responsive smart nanogels for cancer diagnostics and therapy. Nanomedicine. 2010;5(3):451–468. doi:10.2217/nnm.10.18
  • Li C, Obireddy SR, Lai WF. Preparation and use of nanogels as carriers of drugs. Drug Deliv. 2021;28(1):1594. doi:10.1080/10717544.2021.1955042
  • Cuggino JC, Blanco ERO, Gugliotta LM, Alvarez Igarzabal CI, Calderón M. Crossing biological barriers with nanogels to improve drug delivery performance. J Control Release. 2019;307:221–246. doi:10.1016/j.jconrel.2019.06.005
  • Kersey FR, Merkel TJ, Perry JL, Napier ME, Desimone JM. Effect of aspect ratio and deformability on nanoparticle extravasation through nanopores. Langmuir. 2012;28(23):8773–8781. doi:10.1021/la301279v
  • Shirahama H, Lee BH, Tan LP, Cho NJ. Precise tuning of facile one-pot gelatin methacryloyl (GelMA) synthesis. Sci Rep. 2016;6(1):1–11. doi:10.1038/srep31036
  • Hoch E, Hirth T, Tovar GEM, Borchers K. Chemical tailoring of gelatin to adjust its chemical and physical properties for functional bioprinting. J Mater Chem B. 2013;1(41):5675–5685. doi:10.1039/c3tb20745e
  • Kang MG, Lee MY, Cha JM, et al. Nanogels derived from fish gelatin: application to drug delivery system. Mar Drugs. 2019;17(4):246. doi:10.3390/md17040246
  • Kim J, Gauvin R, Yoon HJ, et al. Skin penetration-inducing gelatin methacryloyl nanogels for transdermal macromolecule delivery. Macromol Res. 2016;24(12):1115–1125. doi:10.1007/s13233-016-4147-9
  • Novakova I, Subileau EA, Toegel S, et al. Transport rankings of non-steroidal antiinflammatory drugs across blood-brain barrier in vitro models. PLoS One. 2014;9(1):e86806. doi:10.1371/journal.pone.0086806
  • Krishnamoorthy S, Noorani B, Xu C. Effects of encapsulated cells on the physical–mechanical properties and microstructure of gelatin methacrylate hydrogels. Int J Mol Sci. 2019;20(20):5061. doi:10.3390/ijms20205061
  • Lee BH, Shirahama H, Cho NJ, Tan LP. Efficient and controllable synthesis of highly substituted gelatin methacrylamide for mechanically stiff hydrogels. RSC Adv. 2015;5(128):106094–106097. doi:10.1039/C5RA22028A
  • Sun M, Sun X, Wang Z, Guo S, Yu G, Yang H. Synthesis and properties of gelatin methacryloyl (GelMA) hydrogels and their recent applications in load-bearing tissue. Polymers. 2018;10(11):1290. doi:10.3390/polym10111290
  • Pinelli F, Ferracin F, Perale G, Rossi F. Synthesis and applications of nanogels via covalent cross-linking strategies. Adv Chem Engineer. 2023;62:35–58.
  • Rizwan M, Yahya R, Hassan A, et al. pH sensitive hydrogels in drug delivery: brief history, properties, swelling, and release mechanism, material selection and applications. Polymers. 2017;9(4):137.
  • Bashir S, Hina M, Iqbal J, et al. Fundamental concepts of hydrogels: synthesis, properties, and their applications. Polymers. 2020;12(11):1–60. doi:10.3390/POLYM12112702
  • Jacob S, Nair AB, Shah J, Sreeharsha N, Gupta S, Shinu P. Emerging role of hydrogels in drug delivery systems, tissue engineering and wound management. Pharmaceutics. 2021;13(3):357. doi:10.3390/pharmaceutics13030357
  • Cheng G, Zielonka J, McAllister D, Tsai S, Dwinell MB, Kalyanaraman B. Profiling and targeting of cellular bioenergetics: inhibition of pancreatic cancer cell proliferation. Br J Cancer. 2014;111(1):85–93. doi:10.1038/bjc.2014.272
  • Jaidev LR, Krishnan UM, Sethuraman S. Gemcitabine loaded biodegradable PLGA nanospheres for in vitro pancreatic cancer therapy. Mater Sci Eng C Mater Biol Appl. 2015;47:40–47. doi:10.1016/j.msec.2014.11.027
  • Srinivasan B, Kolli AR, Esch MB, Abaci HE, Shuler ML, Hickman JJ. TEER measurement techniques for in vitro barrier model systems. J Lab Autom. 2015;20(2):107–126. doi:10.1177/2211068214561025
  • Derissen EJB, Huitema ADR, Rosing H, Schellens JHM, Beijnen JH. Intracellular pharmacokinetics of gemcitabine, its deaminated metabolite 2′,2′‐difluorodeoxyuridine and their nucleotides. Br J Clin Pharmacol. 2018;84(6):1279. doi:10.1111/bcp.13557
  • Wang Y, Fan W, Dai X, et al. Enhanced tumor delivery of gemcitabine via PEG-DSPE/TPGS mixed micelles. Mol Pharm. 2014;11(4):1140–1150. doi:10.1021/mp4005904
  • Soni KS, Desale SS, Bronich TK. Nanogels: an overview of properties, biomedical applications and obstacles to clinical translation. J Control Release. 2016;240:109. doi:10.1016/j.jconrel.2015.11.009