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Ghassemi F, Delrish E, Jabbarvand M, Lashay A, Asadi Amoli F, Atyabi F, Sadat Mirzazadeh Tekie F, Dinarvand R, Heidari Keshel S, Soleimani M. The Antitumor Effect of Topotecan Loaded Thiolated Chitosan-Dextran Nanoparticles for Intravitreal Chemotherapy: A Xenograft Retinoblastoma Model. JOVR [Internet]. 2023Feb.13 [cited 2024May2];18(1):68–80. Available from: https://knepublishing.com/index.php/JOVR/article/view/12727
https://doi.org/10.18502/jovr.v18i1.12727
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authors
-
Fariba Ghassemi
Fariba Ghassemi
MD. Translational Ophthalmology Research Center (TORC), Farabi Eye Hospital, Tehran University of Medical Sciences, Qazvin Square, Tehran 13366, Iran.
-
Elham Delrish
Elham Delrish
Translational Ophthalmology Research Centre (TORC), Farabi Eye Hospital, Tehran University of Medical Sciences, Tehran, Iran
-
Mahmoud Jabbarvand
Mahmoud Jabbarvand
Translational Ophthalmology Research Centre (TORC), Farabi Eye Hospital, Tehran University of Medical Sciences, Tehran, Iran
-
Alireza Lashay
Alireza Lashay
Translational Ophthalmology Research Centre (TORC), Farabi Eye Hospital, Tehran University of Medical Sciences, Tehran, Iran
-
Fahimeh Asadi Amoli
Fahimeh Asadi Amoli
Department of pathology, Farabi Eye Hospital, Tehran University of Medical Sciences, Tehran, Iran
-
Fatemeh Atyabi
Fatemeh Atyabi
Nanotechnology Research Centre, Faculty of Pharmacy, Tehran University of Medical Sciences, Tehran, Iran
-
Farnaz Sadat Mirzazadeh Tekie
Farnaz Sadat Mirzazadeh Tekie
Nanotechnology Research Centre, Faculty of Pharmacy, Tehran University of Medical Sciences, Tehran, Iran
-
Rassoul Dinarvand
Rassoul Dinarvand
Nanotechnology Research Centre, Faculty of Pharmacy, Tehran University of Medical Sciences, Tehran, Iran
-
Saeed Heidari Keshel
Saeed Heidari Keshel
Department of Tissue Engineering and Applied Cell Science, School of Advanced Technologies in Medicine, Shahid Beheshti University of Medical Sciences, Tehran, Iran
-
Masoud Soleimani
Masoud Soleimani
Department of Hematology, School of Medical Sciences, Tarbiat Modares University, Tehran, Iran
Published Date
- Feb 13, 2023
The Antitumor Effect of Topotecan Loaded Thiolated Chitosan-Dextran Nanoparticles for Intravitreal Chemotherapy: A Xenograft Retinoblastoma Model
Abstract
Purpose: This research intended to fabricate the thiolated chitosan-dextran nanoparticles (NPs) containing topotecan (TPH-CMD-TCS-NPs) to assess the ability of NPs in improving the efficacy of intravitreal chemotherapy of retinoblastoma in a rabbit xenograft model.
Methods: The coacervation process was used to produce the NPs. The cellular uptake of Cyanine-3 (CY3)-labeled NPs were investigated in human retinoblastoma Y79 cells using confocal microscopy. Also, the prepared TPH-CMD-TCS-NPs were tested in vitro by the tetrazolium dyes II (XTT) and flow cytometry in order to assess their cytotoxicity. In addition, a rabbit xenograft model of retinoblastoma was developed to test the antitumor effectiveness of TPH-CMD-TCS-NPs through intravitreal administration.
Results: NPs had a mean diameter, polydispersity index, and zeta potential of 30 ± 4 nm, 0.24 ± 0.03 and +10 ± 3 mV, respectively. NPs (IC50s 40.40 compared to 126.20 nM, P = 0.022) were more effective than free topotecan as a dose-based feature. The tumor reaction to intravitreal chemotherapy with NPs was measured by evaluating the percentage of necrosis in the tumor tissue (91 ± 2%) and vitreous seeds (89 ± 9%) through hematoxylin and eosin (H&E) staining. In comparison with the control group, the TPHCMD- TCs-NPs treated group showed a significant decrease in tumor volume seven days after the intravitreal injection (P = 0.039). No significant changes were found in the ERG parameters after the intravitreal injection of TPH-CMD-TCs-NPs or TPH (P > 0.05).
Conclusion: This investigation revealed definitive antitumor efficacy of TPH-CMD-TCSNPs by intravitreal administration in the rabbit xenograft retinoblastoma model.
Keywords:
Chemotherapy, Intravitreal, Nanoparticles, Ocular Malignancy, Retinoblastoma, Topotecan
References
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9. Abramson DH, Fabius AW, Francis JH, Marr BP, Dunkel IJ, Brodie SE, et al. Ophthalmic artery chemosurgery for eyes with advanced retinoblastoma. Ophthalmic Genet 2017;38:16–21.
10. Francis JH, Marr BP, Brodie SE, Gobin YP, Abramson DH. Tethered vitreous seeds following intravitreal melphalan for retinoblastoma. JAMA Ophthalmol 2014;132:1024– 1025.
11. Francis JH, Brodie SE, Marr B, Zabor EC, Mondesire- Crump I, Abramson DH. Efficacy and toxicity of intravitreous chemotherapy for retinoblastoma: Fouryear experience. Ophthalmology 2017;124:488–495.
12. Ghassemi F, Shields CL. Intravitreal melphalan for refractory or recurrent vitreous seeding from retinoblastoma. Arch Ophthalmol 2012;130:1268–1271.
13. Rinaudo M. Chitin and chitosan: Properties and applications. Prog Polym Sci 2006;31:603–632.
14. Azuma K, Izumi R, Osaki T, Ifuku S, Morimoto M, Saimoto H, et al. Chitin, chitosan, and its derivatives for wound healing: Old and new materials. J Funct Biomater 2015;6:104–142.
15. Zhang C, Ding Y, Yu LL, Ping Q. Polymeric micelle systems of hydroxycamptothecin based onamphiphilic N-alkyl-N-trimethyl chitosan derivatives. Colloids Surf B Biointerfaces 2007;55:192–199.
16. Bei YY, Yuan Z-Q, Zhang L, Zhou X-F, Chen W-L, Xia P, et al. Novel self-assembled micelles based on palmitoyltrimethyl- chitosan for efficient delivery of harmine toliver cancer. Expert Opin Drug Deliv 2014;11:843–854.
17. Bernkop-Schnurch A. Thiomers: A new generation of mucoadhesive polymers. Adv Drug Deliv Rev 2005;57:1569–1582.
18. Nácher-Vázquez M, Ballesteros N, Canales A, Saint- Jean SR, ]Pérez-Prieto SI, Prieto A, et al. Dextrans produced by lactic acid bacteria exhibit antiviral and immunomodulatory activity against salmonid viruses. Carbohydr Polym 2015;124:292–301.
19. Shin JM, Song SH, Vijayakameswara Rao N, Lee ES, Ko H, Park JH. A carboxymethyl dextran-based polymeric conjugate as the antigen carrier for cancer immunotherapy. Biomater Res 2018;22:21.
20. Vasić K, Knez Ž, Konstantinova EA, Kokorin AI, Gyergyek S, Leitgeb M. Structural and magnetic characteristics of carboxymethyl dextran coated magnetic nanoparticles: From characterization to immobilization application. React Funct Polym 2020;104481.
21. Brave M, Dagher R, Farrell A, Abraham S, Ramchandani R, Gobburu J, et al. Topotecan in combination with cisplatin for the treatment of stage IVB, recurrent, or persistent cervical cancer. Oncology 2006;20:1401–1404.
22. Nicum SJ, O’Brien ME, Topotecan for the treatment of small-cell lung cancer. Expert Rev Anticancer Ther 2007;7:795–801.
23. Wethington SL, Wright JD, Herzog TJ. Key role of topoisomerase I inhibitors in the treatment of recurrent and refractory epithelial ovarian carcinoma. Expert Rev Anticancer Ther 2008;8:819–831.
24. Laurie NA, Gray JK, Zhang J, Leggas M, Relling M, Egorin M, et al. Topotecan combination chemotherapy in two new rodent models of retinoblastoma. Clin Cancer Res 2005;11:7569–7578.
25. Chantada GL, Fandiño AC, Casak SJ, Mato G, Manzitti J, Schvartzman E. Activity of topotecan in retinoblastoma. Ophthalmic Genet 2004;25:37–43.
26. Mallipatna AC, Dimaras H, Chan HS, Héon E, Gallie BL. Periocular topotecan for intraocular retinoblastoma. Arch Ophthalmol 2011;129:738–745.
27. Ghassemi F, Shields CL, Ghadimi H, Khodabandeh A, Roohipoor R. Combined intravitreal melphalan and topotecan for refractory or recurrent vitreous seeding from retinoblastoma. JAMA Ophthalmol 2014;132:936–941.
28. Padhi S, Mirza MA, Verma D, Khuroo T, Panda AK, Talegaonkar S, et al. Revisiting the nanoformulation design approach for effective delivery of topotecan in its stable form: An appraisal of its in vitro behavior and tumor amelioration potential. Drug Deliv 2015;23:1–11.
29. Zhang L, Hu Y, Jiang X, Yang C, Lu W, Yang YH. Camptothecinderivativeloaded poly(caprolactoneco- lactide)-b-PEG-b-poly(caprolactone-co-lactide) nanoparticles and their biodistribution in mice. J Control Release 2004;96:135–148.
30. Sieval AB, Thanou M, Kotze AF, Verhoef JC, Brussee J, Junginger HE. NMR preparation characterization of highly substituted N-trimethyl chitosan chloride. Carbohydr Polym 1998;36:157–165.
31. Snyman D, Hamman JH, Kotze JS, Rollings JE. The relationship between the absolute molecular weight and the degree of quaternization of N-trimethyl chitosan chloride. Carbohydr Polym 2002;50:145–150.
32. Margit DH, Constantia EK, Bernkop-Schnürch A. In vitro evaluation of the viscoelastic properties of chitosan– thioglycolic acid conjugates. Eur J Pharm Biopharm 2003;55:185–190.
33. Roldo M, Hornof M, Caliceti P, Bernkop-Schnürch A. Mucoadhesive thiolated chitosans as platforms for oral controlled drug delivery: synthesis an in vitro evaluation. Eur J Pharm Biopharm 2004;57:115–121.
34. Tekie FSM, Kiani M, Zakerian A, Pilevarian F, Assali A, Soleimani M, et al. Nano polyelectrolytecomplexes of carboxymethyl dextran and chitosan to improve chitosan-mediated delivery of miR-145. Carbohydr Polym 2017;159:66–75.
35. Nagarajana E , Shanmugasundarama P, Ravichandirana V, Vijayalakshmi A, Senthilnathan B, Masilamani K. Development and evaluation of chitosan based polymeric nanoparticles of an antiulcer drug lansoprazole. J Appl Pharm Sci 2015;5:020–025.
36. Liu Y, Chen X, Ding J, Yu L, Ma D, Ding J. Improved solubility and bioactivity of camptothecin family antitumor drugs with supramolecular encapsulation by water soluble pillar[6]arene. ACS Omega 2017;2:5283−5288.
37. Kang SJ, Grossniklaus HE. Rabbit model of retinoblastoma. J Biomed Biotechnol 2011;394730:1–6.
38. De Britto D, Celi Goy R, CampanaFilho SP, Assis OBG. Quaternary salts of chitosan: History, antimicrobial features, and prospects. Int J Carbohydr Chem 2011;312539:12.
39. Zhu X, Su M, Tang S, Wang L, Liang X, Meng F, et al. Synthesis of thiolated chitosan and preparation nanoparticles with sodium alginate for ocular drug delivery. Mol Vis 2012;18:1973–1982.
40. Mourya VK, Inamdar NN. Chitosan-modifications and applications: Opportunities galore. React Funct Polym 2008;68:1013–1051.
41. Snyman D, Hamman JH, Kotze AF. Evaluation of the mucoadhesive properties of N-trimethyl chitosan chloride. Drug Dev Ind Pharm 2003;29:61–69.
42. Kamalzare S, Noormohammadi Z, Rahimi P, Atyabi F, Irani S, Tekie FSM, et al. Carboxymethyl dextrantrimethyl chitosan coated superparamagnetic iron oxide nanoparticles: An effective siRNA delivery system for HIV-1 Nef. J Cell Physiol 2019;1–12.
43. Vasić K, Knez Ž, Konstantinova EA, Kokorin AI, Gyergyek S, Leitgeb M. Structural and magnetic characteristics of carboxymethyl dextran coated magnetic nanoparticles: From characterization to immobilization application. React Funct Polym 2020:104481.
44. Jadidi-Niaragh F, Atyabi F, Rastegari A, Kheshtchin N, Arab S, Hassannia H, et al. CD73 specific siRNA loaded chitosan lactate nanoparticles potentiate the antitumor effect of a dendritic cell vaccine in 4T1 breast cancer bearing mice. J Control Release 2017;246:46–59.
2. Antoneli CB, Ribeiro KC, Steinhorst F, R S Novaes PE, Chojniak MM, Malogolowkin M. Treatment of retinoblastoma patients with chemoreduction plus local therapy: Experience of the AC Camargo Hospital, Brazil. J Pediatr Hematol Oncol 2006;28:342–345. 3. Shields CL, Kaliki S, Al-Dahmash S, Rojanaporn D, Leahey A, Griffin G, et al. Management of advanced retinoblastoma with intravenous chemotherapy then intraarterial chemotherapy as alternative to enucleation. Retina 2013;33:2103–2109.
4. Munier FL, Gaillard MC, Balmer A, Soliman S, Podilsky G, Moulin AP, et al. Intravitreal chemotherapy for vitreous disease in retinoblastoma revisited: From prohibition to conditional indications. Br J Ophthalmol 2012;96:1078– 1083.
5. Shields CL, Fulco EM, Arias JD, Alarcon C, Pellegrini M, Rishi P, et al. Retinoblastoma frontiers with intravenous, intraarterial, periocular, and intravitreal chemotherapy. Eye 2013;27:253–264.
6. Shields CL, Manjandavida FP, Lally SE, Pieretti G, Arepalli SA, Caywood EH, et al. Intra-arterial chemotherapy for retinoblastoma in 70 eyes: Outcomes based on the international classification of retinoblastoma. Ophthalmology 2014;121:1453–1460.
7. Gobin YP, Dunkel IJ, Marr BP, Brodie SE, Abramson DH. Intra-arterial chemotherapy for the management of retinoblastoma: Four-year experience. Arch Ophthalmol 2011;129:732–737.
8. Shields CL, Honavar SG, Meadows AT, Shields JA, Demirci H, Singh A, et al. Chemoreduction plus focal therapy for retinoblastoma: Factors predictive of need for treatment with external beam radiotherapy or enucleation. Am J Ophthalmol 2002;133:657–664.
9. Abramson DH, Fabius AW, Francis JH, Marr BP, Dunkel IJ, Brodie SE, et al. Ophthalmic artery chemosurgery for eyes with advanced retinoblastoma. Ophthalmic Genet 2017;38:16–21.
10. Francis JH, Marr BP, Brodie SE, Gobin YP, Abramson DH. Tethered vitreous seeds following intravitreal melphalan for retinoblastoma. JAMA Ophthalmol 2014;132:1024– 1025.
11. Francis JH, Brodie SE, Marr B, Zabor EC, Mondesire- Crump I, Abramson DH. Efficacy and toxicity of intravitreous chemotherapy for retinoblastoma: Fouryear experience. Ophthalmology 2017;124:488–495.
12. Ghassemi F, Shields CL. Intravitreal melphalan for refractory or recurrent vitreous seeding from retinoblastoma. Arch Ophthalmol 2012;130:1268–1271.
13. Rinaudo M. Chitin and chitosan: Properties and applications. Prog Polym Sci 2006;31:603–632.
14. Azuma K, Izumi R, Osaki T, Ifuku S, Morimoto M, Saimoto H, et al. Chitin, chitosan, and its derivatives for wound healing: Old and new materials. J Funct Biomater 2015;6:104–142.
15. Zhang C, Ding Y, Yu LL, Ping Q. Polymeric micelle systems of hydroxycamptothecin based onamphiphilic N-alkyl-N-trimethyl chitosan derivatives. Colloids Surf B Biointerfaces 2007;55:192–199.
16. Bei YY, Yuan Z-Q, Zhang L, Zhou X-F, Chen W-L, Xia P, et al. Novel self-assembled micelles based on palmitoyltrimethyl- chitosan for efficient delivery of harmine toliver cancer. Expert Opin Drug Deliv 2014;11:843–854.
17. Bernkop-Schnurch A. Thiomers: A new generation of mucoadhesive polymers. Adv Drug Deliv Rev 2005;57:1569–1582.
18. Nácher-Vázquez M, Ballesteros N, Canales A, Saint- Jean SR, ]Pérez-Prieto SI, Prieto A, et al. Dextrans produced by lactic acid bacteria exhibit antiviral and immunomodulatory activity against salmonid viruses. Carbohydr Polym 2015;124:292–301.
19. Shin JM, Song SH, Vijayakameswara Rao N, Lee ES, Ko H, Park JH. A carboxymethyl dextran-based polymeric conjugate as the antigen carrier for cancer immunotherapy. Biomater Res 2018;22:21.
20. Vasić K, Knez Ž, Konstantinova EA, Kokorin AI, Gyergyek S, Leitgeb M. Structural and magnetic characteristics of carboxymethyl dextran coated magnetic nanoparticles: From characterization to immobilization application. React Funct Polym 2020;104481.
21. Brave M, Dagher R, Farrell A, Abraham S, Ramchandani R, Gobburu J, et al. Topotecan in combination with cisplatin for the treatment of stage IVB, recurrent, or persistent cervical cancer. Oncology 2006;20:1401–1404.
22. Nicum SJ, O’Brien ME, Topotecan for the treatment of small-cell lung cancer. Expert Rev Anticancer Ther 2007;7:795–801.
23. Wethington SL, Wright JD, Herzog TJ. Key role of topoisomerase I inhibitors in the treatment of recurrent and refractory epithelial ovarian carcinoma. Expert Rev Anticancer Ther 2008;8:819–831.
24. Laurie NA, Gray JK, Zhang J, Leggas M, Relling M, Egorin M, et al. Topotecan combination chemotherapy in two new rodent models of retinoblastoma. Clin Cancer Res 2005;11:7569–7578.
25. Chantada GL, Fandiño AC, Casak SJ, Mato G, Manzitti J, Schvartzman E. Activity of topotecan in retinoblastoma. Ophthalmic Genet 2004;25:37–43.
26. Mallipatna AC, Dimaras H, Chan HS, Héon E, Gallie BL. Periocular topotecan for intraocular retinoblastoma. Arch Ophthalmol 2011;129:738–745.
27. Ghassemi F, Shields CL, Ghadimi H, Khodabandeh A, Roohipoor R. Combined intravitreal melphalan and topotecan for refractory or recurrent vitreous seeding from retinoblastoma. JAMA Ophthalmol 2014;132:936–941.
28. Padhi S, Mirza MA, Verma D, Khuroo T, Panda AK, Talegaonkar S, et al. Revisiting the nanoformulation design approach for effective delivery of topotecan in its stable form: An appraisal of its in vitro behavior and tumor amelioration potential. Drug Deliv 2015;23:1–11.
29. Zhang L, Hu Y, Jiang X, Yang C, Lu W, Yang YH. Camptothecinderivativeloaded poly(caprolactoneco- lactide)-b-PEG-b-poly(caprolactone-co-lactide) nanoparticles and their biodistribution in mice. J Control Release 2004;96:135–148.
30. Sieval AB, Thanou M, Kotze AF, Verhoef JC, Brussee J, Junginger HE. NMR preparation characterization of highly substituted N-trimethyl chitosan chloride. Carbohydr Polym 1998;36:157–165.
31. Snyman D, Hamman JH, Kotze JS, Rollings JE. The relationship between the absolute molecular weight and the degree of quaternization of N-trimethyl chitosan chloride. Carbohydr Polym 2002;50:145–150.
32. Margit DH, Constantia EK, Bernkop-Schnürch A. In vitro evaluation of the viscoelastic properties of chitosan– thioglycolic acid conjugates. Eur J Pharm Biopharm 2003;55:185–190.
33. Roldo M, Hornof M, Caliceti P, Bernkop-Schnürch A. Mucoadhesive thiolated chitosans as platforms for oral controlled drug delivery: synthesis an in vitro evaluation. Eur J Pharm Biopharm 2004;57:115–121.
34. Tekie FSM, Kiani M, Zakerian A, Pilevarian F, Assali A, Soleimani M, et al. Nano polyelectrolytecomplexes of carboxymethyl dextran and chitosan to improve chitosan-mediated delivery of miR-145. Carbohydr Polym 2017;159:66–75.
35. Nagarajana E , Shanmugasundarama P, Ravichandirana V, Vijayalakshmi A, Senthilnathan B, Masilamani K. Development and evaluation of chitosan based polymeric nanoparticles of an antiulcer drug lansoprazole. J Appl Pharm Sci 2015;5:020–025.
36. Liu Y, Chen X, Ding J, Yu L, Ma D, Ding J. Improved solubility and bioactivity of camptothecin family antitumor drugs with supramolecular encapsulation by water soluble pillar[6]arene. ACS Omega 2017;2:5283−5288.
37. Kang SJ, Grossniklaus HE. Rabbit model of retinoblastoma. J Biomed Biotechnol 2011;394730:1–6.
38. De Britto D, Celi Goy R, CampanaFilho SP, Assis OBG. Quaternary salts of chitosan: History, antimicrobial features, and prospects. Int J Carbohydr Chem 2011;312539:12.
39. Zhu X, Su M, Tang S, Wang L, Liang X, Meng F, et al. Synthesis of thiolated chitosan and preparation nanoparticles with sodium alginate for ocular drug delivery. Mol Vis 2012;18:1973–1982.
40. Mourya VK, Inamdar NN. Chitosan-modifications and applications: Opportunities galore. React Funct Polym 2008;68:1013–1051.
41. Snyman D, Hamman JH, Kotze AF. Evaluation of the mucoadhesive properties of N-trimethyl chitosan chloride. Drug Dev Ind Pharm 2003;29:61–69.
42. Kamalzare S, Noormohammadi Z, Rahimi P, Atyabi F, Irani S, Tekie FSM, et al. Carboxymethyl dextrantrimethyl chitosan coated superparamagnetic iron oxide nanoparticles: An effective siRNA delivery system for HIV-1 Nef. J Cell Physiol 2019;1–12.
43. Vasić K, Knez Ž, Konstantinova EA, Kokorin AI, Gyergyek S, Leitgeb M. Structural and magnetic characteristics of carboxymethyl dextran coated magnetic nanoparticles: From characterization to immobilization application. React Funct Polym 2020:104481.
44. Jadidi-Niaragh F, Atyabi F, Rastegari A, Kheshtchin N, Arab S, Hassannia H, et al. CD73 specific siRNA loaded chitosan lactate nanoparticles potentiate the antitumor effect of a dendritic cell vaccine in 4T1 breast cancer bearing mice. J Control Release 2017;246:46–59.