Percutaneous Delivery of Oncogel for Targeted Liver Tumor Ablation and Controlled Release of Therapeutics.
ablation
biomaterial
drug delivery
intratumoral
liver cancer
Journal
Advanced materials (Deerfield Beach, Fla.)
ISSN: 1521-4095
Titre abrégé: Adv Mater
Pays: Germany
ID NLM: 9885358
Informations de publication
Date de publication:
15 Aug 2024
15 Aug 2024
Historique:
revised:
30
07
2024
received:
28
04
2024
medline:
16
8
2024
pubmed:
16
8
2024
entrez:
16
8
2024
Statut:
aheadofprint
Résumé
Advanced-stage liver cancers are associated with poor prognosis and have limited treatment options, often leading the patient to hospice care. Percutaneous intratumoral injection of anticancer agents has emerged as a potential alternative to systemic therapy to overcome tumor barriers, increase bioavailability, potentiate immunotherapy, and avoid systemic toxicity, which advanced-stage cancer patients cannot tolerate. Here, an injectable OncoGel (OG) comprising of a nanocomposite hydrogel loaded with an ionic liquid (IL) is developed for achieving a predictable and uniform tumor ablation and long-term slow release of anticancer agents into the ablation zone. Rigorous mechanical, physiochemical, drug release, cytotoxicity experiments, and ex vivo human tissue testing identify an injectable version of the OG with bactericidal properties against highly resistant bacteria. Intratumoral injection of OG loaded with Nivolumab (Nivo) and doxorubicin (Dox) into highly malignant tumor models in mice, rats, and rabbits demonstrates enhanced survival and tumor regression associated with robust tissue ablation and drug distribution throughout the tumor. Mass cytometry and proteomic studies in a mouse model of colorectal cancer that often metastasizes to the liver indicate an enhanced anticancer immune response following the intratumoral injection of OG. OG may augment immunotherapy and potentially improve outcomes in liver cancer patients.
Identifiants
pubmed: 39148179
doi: 10.1002/adma.202406080
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
e2406080Subventions
Organisme : NIH HHS
ID : R01CA257558
Pays : United States
Organisme : NIH HHS
ID : R01HL140951
Pays : United States
Organisme : NIH HHS
ID : R01DK130566
Pays : United States
Organisme : NIH HHS
ID : R01HL165176
Pays : United States
Organisme : NIH HHS
ID : R01HL137193
Pays : United States
Organisme : Mayo Clinic: Christian Haub Family Career Development Award and the Mayo Clinic Clinician Investigator Award
Informations de copyright
© 2024 The Authors. Advanced Materials published by Wiley‐VCH GmbH.
Références
A. Villanueva, N. Engl. J. Med. 2019, 380, 1450.
a) W. J. Jeng, G. V. Papatheodoridis, A. S. F. Lok, Lancet 2023, 401, 1039;
b) N. Ganne‐Carrie, P. Nahon, J Hepatol 2019, 70, 284;
c) N. Mahmud, Z. Fricker, R. A. Hubbard, G. N. Ioannou, J. D. Lewis, T. H. Taddei, K. D. Rothstein, M. Serper, D. S. Goldberg, D. E. Kaplan, Hepatology 2021, 73, 204.
a) J. Bruix, L. G. da Fonseca, M. Reig, Nat. Rev. Gastroenterol. Hepatol. 2019, 16, 617;
b) F. Spada, N. Fazio, G. Bonomo, L. Monfardini, P. D. Vigna, D. Radice, S. Boselli, F. Orsi, Ecancermedicalscience 2012, 6, 280;
c) M. Ringelhan, D. Pfister, T. O'Connor, E. Pikarsky, M. Heikenwalder, Nat. Immunol. 2018, 19, 222.
M. S. Dendy, J. M. Ludwig, S. M. Stein, H. S. Kim, Liver cancer 2019, 8, 326.
J. J. Hu, H. Albadawi, Z. F. Zhang, M. A. Salomao, S. Gunduz, S. Rehman, L. D'Amone, J. L. Mayer, F. Omenetto, R. Oklu, Adv. Mater. 2022, 34.
a) J. A. Marin‐Acevedo, R. M. Chirila, R. S. Dronca, Mayo Clin Proc 2019, 94, 1321;
b) G. Varricchi, G. Marone, V. Mercurio, M. R. Galdiero, D. Bonaduce, C. G. Tocchetti, Curr. Med. Chem. 2018, 25, 1327;
c) S. S. Mahmood, M. G. Fradley, J. V. Cohen, A. Nohria, K. L. Reynolds, L. M. Heinzerling, R. J. Sullivan, R. Damrongwatanasuk, C. L. Chen, D. Gupta, M. C. Kirchberger, M. Awadalla, M. Z. O. Hassan, J. J. Moslehi, S. P. Shah, S. Ganatra, P. Thavendiranathan, D. P. Lawrence, J. D. Groarke, T. G. Neilan, J Am Coll Cardiol 2018, 71, 1755.
a) R. A. Sheth, R. Murthy, D. S. Hong, S. Patel, M. J. Overman, A. Diab, P. Hwu, A. Tam, JAMA Netw Open 2020, 3, 207911;
b) O. Hamid, R. Ismail, I. Puzanov, Oncologist 2020, 25, e423.
R. K. Avery, H. Albadawi, M. Akbari, Y. S. Zhang, M. J. Duggan, D. V. Sahani, B. D. Olsen, A. Khademhosseini, R. Oklu, Sci. Transl. Med. 2016, 8, 365ra156.
a) K. Egorova, V. Ananikov, J. Mol. Liq. 2018, 272;
b) A. Julio, R. Caparica, S. A. Costa Lima, A. S. Fernandes, C. Rosado, D. M. F. Prazeres, S. Reis, T. Santos de Almeida, P. Fonte, Nanomaterials 2019, 9, 1148;
c) M. Reslan, V. Kayser, Biophys. Rev. 2018, 10, 781;
d) M. Reslan, V. Ranganathan, D. R. Macfarlane, V. Kayser, Chem Commun. 2018, 54, 10622;
e) M. Riaz, M. Akhlaq, S. Naz, M. Uroos, RSC Adv. 2022, 12, 25977.
S. Honary, F. Zahir, Trop. J. Pharm. Res. 2013, 12, 255.
B. Kim, G. Han, B. J. Toley, C. K. Kim, V. M. Rotello, N. S. Forbes, Nat. Nanotechnol. 2010, 5, 465.
a) Y. Shi, Z. Zhao, K. Peng, Y. Gao, D. Wu, J. Kim, S. Mitragotri, Adv. Healthcare Mater. 2021, 10, 2001455;
b) E. E. L. Tanner, K. N. Ibsen, S. Mitragotri, J. Controlled Release 2018, 286, 137.
a) C. Schroder, Top Curr Chem 2017, 375, 25;
b) X. Tadeo, B. Lopez‐Mendez, D. Castano, T. Trigueros, O. Millet, Biophys. J. 2009, 97, 2595.
a) H. Weingartner, C. Cabrele, C. Herrmann, Phys. Chem. Chem. Phys. 2012, 14, 415;
b) H. Zhao, J. Chem. Technol. Biotechnol. 2016, 91, 25.
S. Wang, Y. Wu, R. Guo, Y. Huang, S. Wen, M. Shen, J. Wang, X. Shi, Langmuir 2013, 29, 5030.
G. Kiaee, N. Dimitrakakis, S. Sharifzadeh, H. J. Kim, R. K. Avery, K. M. Moghaddam, R. Haghniaz, E. P. Yalcintas, N. R. Barros, S. Karamikamkar, A. Libanori, A. Khademhosseini, P. Khoshakhlagh, Adv. Healthcare Mater. 2022, 11, 2102054.
a) F. Mpekris, J. W. Baish, T. Stylianopoulos, R. K. Jain, P Natl. Acad. Sci. USA 2017, 114, 1994.
b) T. Stylianopoulos, R. K. Jain, Proc. Natl. Acad. Sci. USA 2013, 110, 18632.
a) K. Bakshi, S. Mitra, V. K. Sharma, M. S. K. Jayadev, V. G. Sakai, R. Mukhopadhyay, A. Gupta, S. K. Ghosh, Biochim Biophys Acta Biomembr 2020, 1862, 183103;
b) D. Wang, H. J. Galla, P. Drucker, Biophys. Rev. 2018, 10, 735.
R. Wan, X. Xia, P. Wang, W. Huo, H. Dong, Z. Chang, Toxicol. In Vitro 2018, 52, 201805013.
a) X. Li, J. Ma, J. Wang, Ecotoxicol. Environ. Saf. 2015, 120, 342;
b) P. Kumari, V. V. S. Pillai, A. Benedetto, Biophys. Rev. 2020, 12, 1187.
C. K. Y. Ng, E. Dazert, T. Boldanova, M. Coto‐Llerena, S. Nuciforo, C. Ercan, A. Suslov, M. A. Meier, T. Bock, A. Schmidt, S. Ketterer, X. Wang, S. Wieland, M. S. Matter, M. Colombi, S. Piscuoglio, L. M. Terracciano, M. N. Hall, M. H. Heim, Nat. Commun. 2022, 13, 2436.
J. Fares, M. Y. Fares, H. H. Khachfe, H. A. Salhab, Y. Fares, Signal Transduct Target Ther 2020, 5, 28.
H. Albadawi, Z. Zhang, I. Altun, J. Hu, L. Jamal, K. N. Ibsen, E. E. L. Tanner, S. Mitragotri, R. Oklu, Sci. Transl. Med. 2021, 13, eabe3889.
A. I. Valderrama‐Trevino, B. Barrera‐Mera, J. C. Ceballos‐Villalva, E. E. Montalvo‐Jave, Euroasian J Hepatogastroenterol 2017, 7, 166.
M. Efremova, D. Rieder, V. Klepsch, P. Charoentong, F. Finotello, H. Hackl, N. Hermann‐Kleiter, M. Lower, G. Baier, A. Krogsdam, Z. Trajanoski, Nat. Commun. 2018, 9, 32.
a) R. A. Charalel, A. I. Mushlin, X. Zheng, J. Mao, R. C. Carlos, R. S. Brown Jr., B. E. Fortune, A. D. Talenfeld, D. C. Madoff, S. Ibrahim, M. S. Johnson, A. Sedrakyan, J Vasc Interv Radiol 2023, 34, 1997.
b) K. V. Rolston, Infect Dis Ther 2017, 6, 69.
J. Hu, I. Altun, Z. Zhang, H. Albadawi, M. A. Salomao, J. L. Mayer, L. Hemachandra, S. Rehman, R. Oklu, Adv. Mater. 2020, 32, 2002611.
H. Albadawi, I. Altun, J. Hu, Z. Zhang, A. Panda, H. J. Kim, A. Khademhosseini, R. Oklu, Adv. Sci. 2020, 8, 2003327.
J. Hu, H. Albadawi, Z. Zhang, M. A. Salomao, S. Gunduz, S. Rehman, L. D'Amone, J. L. Mayer, F. Omenetto, R. Oklu, Adv. Mater. 2022, 34, 2106865.
T. W. Powers, B. A. Neely, Y. Shao, H. Tang, D. A. Troyer, A. S. Mehta, B. B. Haab, R. R. Drake, PLoS One 2014, 9, 106255.
J. R. Wisniewski, A. Zougman, N. Nagaraj, M. Mann, Nat. Methods 2009, 6, 359.
A. I. Nesvizhskii, A. Keller, E. Kolker, R. Aebersold, Anal. Chem. 2003, 75, 4646.
a) A. Faustino‐Rocha, P. A. Oliveira, J. Pinho‐Oliveira, C. Teixeira‐Guedes, R. Soares‐Maia, R. G. da Costa, B. Colaco, M. J. Pires, J. Colaco, R. Ferreira, M. Ginja, Lab Anim 2013, 42, 217;
b) Y. Guo, R. Klein, R. A. Omary, G. Y. Yang, A. C. Larson, Am. J. Transl. Res. 2010, 3, 114;
c) A. B. Novikoff, Cancer Res. 1957, 17, 1010.
H. Lang, G. K. Wolf, M. Prokop, B. Nuber, A. Weimann, R. Raab, W. G. Zoller, Chirurg 1999, 70, 246.
a) J. H. Kwon, Gut Liver 2010, 4, S105;
b) R. Lencioni, Hepatology 2010, 52, 762;
c) X. D. Lin, L. W. Lin, Hepatobiliary Pancreat Dis Int 2006, 5, 16.
J. H. Chen, Y. C. Lin, Y. S. Huang, T. J. Chen, W. Y. Lin, K. W. Han, Lab. Anim. 2004, 38, 79.
T. W. Clark, Tech Vasc Interv Radiol 2007, 10, 58.
Q. Yu, S. Huang, Z. Wu, J. Zheng, X. Chen, L. Nie, J Nucl Med 2020, 61, 1079.