Nanoparticle tumor localization, disruption of autophagosomal trafficking, and prolonged drug delivery improve survival in peritoneal mesothelioma

Biomaterials

Volumn 102, Issue , 2016, Pages 175-186

  Liu, Rong ^a   Colby, Aaron H ^a,b   Gilmore, Denis ^a   Schulz, Morgan ^a   Zeng, Jialiu ^b   Padera, Robert F ^a   Shirihai, Orian ^c,d   Grinstaff, Mark W ^b   Colson, Yolonda L ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b BOSTON UNIVERSITY   (United States)

^c BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

Author keywords

Autophagosome; Drug delivery; Mesothelioma; Nanoparticle; Paclitaxel; Tumor localization

Indexed keywords

ANIMALS; DRUG DELIVERY; NANOPARTICLES;

ANTI-TUMOR EFFICACY; AUTOPHAGOSOME; COMBINED MECHANISMS; INTRACELLULAR RETENTION; INTRAPERITONEAL ADMINISTRATION; MESOTHELIOMA; PACLITAXEL; TUMOR LOCALIZATION;

TUMORS;

NANOPARTICLE; PACLITAXEL; ANTINEOPLASTIC AGENT; DRUG CARRIER;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOPHAGOSOME; CELL VIABILITY; CONTROLLED STUDY; DRUG CYTOTOXICITY; DRUG DELIVERY SYSTEM; DRUG DISTRIBUTION; DRUG SPECIFICITY; DRUG TISSUE LEVEL; DRUG UPTAKE; FEMALE; HUMAN; HUMAN CELL; INTRACELLULAR TRANSPORT; MOUSE; MULTIPLE DRUG DOSE; NONHUMAN; OVERALL SURVIVAL; PERITONEUM MESOTHELIOMA; PRIORITY JOURNAL; TUMOR LOCALIZATION; ANIMAL; CHEMISTRY; DRUG EFFECTS; MESOTHELIOMA; METABOLISM; NUDE MOUSE; PATHOLOGY; PERITONEUM; PERITONEUM TUMOR; TUMOR CELL LINE;

ANIMALS; ANTINEOPLASTIC AGENTS, PHYTOGENIC; AUTOPHAGOSOMES; CELL LINE, TUMOR; DRUG CARRIERS; DRUG DELIVERY SYSTEMS; FEMALE; HUMANS; MESOTHELIOMA; MICE, NUDE; NANOPARTICLES; PACLITAXEL; PERITONEAL NEOPLASMS; PERITONEUM;

EID: 84975865195     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2016.06.031     Document Type: Article

References (64)

1. [1] Chahinian, A.P., Pajak, T.F., Holland, J.F., Norton, L., Ambinder, R.M., Mandel, E.M., Diffuse malignant mesothelioma. Prospective evaluation of 69 patients. Ann. Intern. Med. 96 (1982), 746–755.
2. [2] Law, M.R., Gregor, A., Hodson, M.E., Bloom, H.J., Turner-Warwick, M., Malignant mesothelioma of the pleura: a study of 52 treated and 64 untreated patients. Thorax 39 (1984), 255–259.
3. [3] Martini, N., McCormack, P.M., Bains, M.S., Kaiser, L.R., Burt, M.E., Hilaris, B.S., Pleural mesothelioma. Ann. Thorac. Surg. 43 (1987), 113–120.
4. [4] Garcia-Carbonero, R., Paz-Ares, L., Systemic chemotherapy in the management of malignant peritoneal mesothelioma. Eur. J. Surg. Oncol. 32 (2006), 676–681.
5. [5] Yan, T.D., Welch, L., Black, D., Sugarbaker, P.H., A systematic review on the efficacy of cytoreductive surgery combined with perioperative intraperitoneal chemotherapy for diffuse malignancy peritoneal mesothelioma. Ann. Oncol. 18 (2007), 827–834.
6. [6] Kelly, K.J., Nash, G.M., Peritoneal debulking/intraperitoneal chemotherapy-non-sarcoma. J. Surg. Oncol. 109 (2014), 14–22.
7. [7] Yan, T.D., Cao, C.Q., Munkholm-Larsen, S., A pharmacological review on intraperitoneal chemotherapy for peritoneal malignancy. World J. Gastrointest. Oncol. 2 (2010), 109–116.
8. [8] Riss, S., Mohamed, F., Dayal, S., Cecil, T., Stift, A., Bachleitner-Hofmann, T., et al. Peritoneal metastases from colorectal cancer: patient selection for cytoreductive surgery and hyperthermic intraperitoneal chemotherapy. Eur. J. Surg. Oncol. 39 (2013), 931–937.
9. [9] Coccolini, F., Cotte, E., Glehen, O., Lotti, M., Poiasina, E., Catena, F., et al. Intraperitoneal chemotherapy in advanced gastric cancer. Meta-analysis of randomized trials. Eur. J. Surg. Oncol. 40 (2014), 12–26.
10. [10] Feldman, A.L., Libutti, S.K., Pingpank, J.F., Bartlett, D.L., Beresnev, T.H., Mavroukakis, S.M., et al. Analysis of factors associated with outcome in patients with malignant peritoneal mesothelioma undergoing surgical debulking and intraperitoneal chemotherapy. J. Clin. Oncol. 21 (2003), 4560–4567.
11. [11] Yan, T.D., Edwards, G., Alderman, R., Marquardt, C.E., Sugarbaker, P.H., Morbidity and mortality assessment of cytoreductive surgery and perioperative intraperitoneal chemotherapy for diffuse malignant peritoneal mesothelioma–a prospective study of 70 consecutive cases. Ann. Surg. Oncol. 14 (2007), 515–525.
12. [12] Sugarbaker, P.H., Stuart, O.A., Vidal-Jove, J., Pessagno, A.M., DeBruijn, E.A., Pharmacokinetics of the peritoneal-plasma barrier after systemic mitomycin C administration. Cancer Treat. Res. 82 (1996), 41–52.
13. [13] Adusumilli, P.S., Cherkassky, L., Villena-Vargas, J., Colovos, C., Servais, E., Plotkin, J., et al. Regional delivery of mesothelin-targeted CAR T cell therapy generates potent and long-lasting CD4-dependent tumor immunity. Sci. Transl. Med., 6, 2014, 261 ra151.
14. [14] Flores, R.M., Pass, H.I., Seshan, V.E., Dycoco, J., Zakowski, M., Carbone, M., et al. Extrapleural pneumonectomy versus pleurectomy/decortication in the surgical management of malignant pleural mesothelioma: results in 663 patients. J. Thorac. Cardiovasc. Surg. 135 (2008), 620–626.
15. [15] Janne, P.A., Baldini, E.H., Patterns of failure following surgical resection for malignant pleural mesothelioma. Thorac. Surg. Clin. 14 (2004), 567–573.
16. [16] Maggi, G., Casadio, C., Cianci, R., Rena, O., Ruffini, E., Trimodality management of malignant pleural mesothelioma. Eur. J. Cardiothorac. Surg. 19 (2001), 346–350.
17. [17] Ruffie, P., Feld, R., Minkin, S., Cormier, Y., Boutan-Laroze, A., Ginsberg, R., et al. Diffuse malignant mesothelioma of the pleura in Ontario and Quebec: a retrospective study of 332 patients. J. Clin. Oncol. 7 (1989), 1157–1168.
18. [18] Rusch, V.W., Giroux, D., Kennedy, C., Ruffini, E., Cangir, A.K., Rice, D., et al. Initial analysis of the international association for the study of lung cancer mesothelioma database. J. Thorac. Oncol. 7 (2012), 1631–1639.
19. [19] Wang, A.Z., Langer, R., Farokhzad, O.C., Nanoparticle delivery of cancer drugs. Annu. Rev. Med. 63 (2012), 185–198.
20. [20] Petros, R.A., DeSimone, J.M., Strategies in the design of nanoparticles for therapeutic applications. Nat. Rev. Drug Discov. 9 (2010), 615–627.
21. [21] Kieler-Ferguson, H.M., Frechet, J.M., Szoka, F.C. Jr., Clinical developments of chemotherapeutic nanomedicines: polymers and liposomes for delivery of camptothecins and platinum (II) drugs. Wiley Interdiscip. Rev. Nanomed. Nanobiotechnol. 5 (2013), 130–138.
22. [22] Heidel, J.D., Davis, M.E., Clinical developments in nanotechnology for cancer therapy. Pharm. Res. 28 (2011), 187–199.
23. [23] Tibbitt, M.W., Rodell, C.B., Burdick, J.A., Anseth, K.S., Progress in material design for biomedical applications. Proc. Natl. Acad. Sci. U. S. A. 112 (2015), 14444–14451.
24. [24] Wang, Y., Byrne, J.D., Napier, M.E., DeSimone, J.M., Engineering nanomedicines using stimuli-responsive biomaterials. Adv. Drug Deliv. Rev. 64 (2012), 1021–1030.
25. [25] Torchilin, V.P., Multifunctional, stimuli-sensitive nanoparticulate systems for drug delivery. Nat. Rev. Drug Discov. 13 (2014), 813–827.
26. [26] Jensen, A.I., Binderup, T., Kumar, E.P., Kjaer, A., Rasmussen, P.H., Andresen, T.L., Positron emission tomography based analysis of long-circulating cross-linked triblock polymeric micelles in a U87MG mouse xenograft model and comparison of DOTA and CB-TE2A as chelators of copper-64. Biomacromolecules 15 (2014), 1625–1633.
27. [27] Morachis, J.M., Mahmoud, E.A., Almutairi, A., Physical and chemical strategies for therapeutic delivery by using polymeric nanoparticles. Pharmacol. Rev. 64 (2012), 505–519.
28. [28] Bae, W.K., Park, M.S., Lee, J.H., Hwang, J.E., Shim, H.J., Cho, S.H., et al. Docetaxel-loaded thermoresponsive conjugated linoleic acid-incorporated poloxamer hydrogel for the suppression of peritoneal metastasis of gastric cancer. Biomaterials 34 (2013), 1433–1441.
29. [29] Bajaj, G., Yeo, Y., Drug delivery systems for intraperitoneal therapy. Pharm. Res. 27 (2010), 735–738.
30. [30] Colson, Y.L., Liu, R., Southard, E.B., Schulz, M.D., Wade, J.E., Griset, A.P., et al. The performance of expansile nanoparticles in a murine model of peritoneal carcinomatosis. Biomaterials 32 (2011), 832–840.
31. [31] De Smet, L., Ceelen, W., Remon, J.P., Vervaet, C., Optimization of drug delivery systems for intraperitoneal therapy to extend the residence time of the chemotherapeutic agent. Sci. World J., 2013, 2013, 720858.
32. [32] Wolinsky, J.B., Colson, Y.L., Grinstaff, M.W., Local drug delivery strategies for cancer treatment: gels, nanoparticles, polymeric films, rods, and wafers. J. Control Release 159 (2012), 14–26.
33. [33] Zahedi, P., Stewart, J., De Souza, R., Piquette-Miller, M., Allen, C., An injectable depot system for sustained intraperitoneal chemotherapy of ovarian cancer results in favorable drug distribution at the whole body, peritoneal and intratumoral levels. J. Control Release 158 (2012), 379–385.
34. [34] Amoozgar, Z., Wang, L., Brandstoetter, T., Wallis, S.S., Wilson, E.M., Goldberg, M.S., Dual-layer surface coating of PLGA-based nanoparticles provides slow-release drug delivery to achieve metronomic therapy in a paclitaxel-resistant murine ovarian cancer model. Biomacromolecules 15 (2014), 4187–4194.
35. [35] Rosalia, R.A., Cruz, L.J., van Duikeren, S., Tromp, A.T., Silva, A.L., Jiskoot, W., et al. CD40-targeted dendritic cell delivery of PLGA-nanoparticle vaccines induce potent anti-tumor responses. Biomaterials 40 (2015), 88–97.
36. [36] Zentner, G.M., Rathi, R., Shih, C., McRea, J.C., Seo, M.H., Oh, H., et al. Biodegradable block copolymers for delivery of proteins and water-insoluble drugs. J. Control Release 72 (2001), 203–215.
37. [37] Sahoo, S.K., Panyam, J., Prabha, S., Labhasetwar, V., Residual polyvinyl alcohol associated with poly (D,L-lactide-co-glycolide) nanoparticles affects their physical properties and cellular uptake. J. Control Release 82 (2002), 105–114.
38. [38] Xu, P., Gullotti, E., Tong, L., Highley, C.B., Errabelli, D.R., Hasan, T., et al. Intracellular drug delivery by poly(lactic-co-glycolic acid) nanoparticles, revisited. Mol. Pharm. 6 (2009), 190–201.
39. [39] Stuart, M.A., Huck, W.T., Genzer, J., Muller, M., Ober, C., Stamm, M., et al. Emerging applications of stimuli-responsive polymer materials. Nat. Mater. 9 (2010), 101–113.
40. [40] Mura, S., Nicolas, J., Couvreur, P., Stimuli-responsive nanocarriers for drug delivery. Nat. Mater. 12 (2013), 991–1003.
41. [41] Felber, A.E., Dufresne, M.H., Leroux, J.C., pH-sensitive vesicles, polymeric micelles, and nanospheres prepared with polycarboxylates. Adv. Drug Deliv. Rev. 64 (2012), 979–992.
42. [42] Baguley, B.C., Finlay, G.J., Pharmacokinetic/cytokinetic principles in the chemotherapy of solid tumours. Clin. Exp. Pharmacol. Physiol. 22 (1995), 825–828.
43. [43] Abubaker, K., Latifi, A., Luwor, R., Nazaretian, S., Zhu, H., Quinn, M.A., et al. Short-term single treatment of chemotherapy results in the enrichment of ovarian cancer stem cell-like cells leading to an increased tumor burden. Mol. Cancer, 12, 2013, 24.
44. [44] Colby, A.H., Colson, Y.L., Grinstaff, M.W., Microscopy and tunable resistive pulse sensing characterization of the swelling of pH-responsive, polymeric expansile nanoparticles. Nanoscale 5 (2013), 3496–3504.
45. [45] Colby, A.H., Liu, R., Schulz, M.D., Padera, R.F., Colson, Y.L., Grinstaff, M.W., Two-step delivery: exploiting the partition coefficient concept to increase intratumoral paclitaxel concentrations in vivo using responsive nanoparticles. Sci. Rep., 6, 2016, 18720.
46. [46] Griset, A.P., Walpole, J., Liu, R., Gaffey, A., Colson, Y.L., Grinstaff, M.W., Expansile nanoparticles: synthesis, characterization, and in vivo efficacy of an acid-responsive polymeric drug delivery system. J. Am. Chem. Soc. 131 (2009), 2469–2471.
47. [47] Zubris, K.A., Colson, Y.L., Grinstaff, M.W., Hydrogels as intracellular depots for drug delivery. Mol. Pharm. 9 (2012), 196–200.
48. [48] Zubris, K.A., Liu, R., Colby, A., Schulz, M.D., Colson, Y.L., Grinstaff, M.W., In vitro activity of Paclitaxel-loaded polymeric expansile nanoparticles in breast cancer cells. Biomacromolecules 14 (2013), 2074–2082.
49. [49] Griset, A.P., Walpole, J., Liu, R., Gaffey, A., Colson, Y.L., Grinstaff, M.W., Expansile nanoparticles: synthesis, characterization, and In vivo efficacy of an acid-responsive polymeric drug delivery system. J. Am. Chem. Soc. 131 (2009), 2469–2471.
50. [50] Herrera, V.L., Colby, A.H., Tan, G.A., Moran, A.M., O'Brien, M.J., Colson, Y.L., et al. Evaluation of expansile nanoparticle tumor localization and efficacy in a cancer stem cell-derived model of pancreatic peritoneal carcinomatosis. Nanomedicine (London) 11 (2016), 1001–1015.
51. [51] Yoo, J.W., Chambers, E., Mitragotri, S., Factors that control the circulation time of nanoparticles in blood: challenges, solutions and future prospects. Curr. Pharm. Des. 16 (2010), 2298–2307.
52. [52] Riehemann, K., Schneider, S.W., Luger, T.A., Godin, B., Ferrari, M., Fuchs, H., Nanomedicine–challenge and perspectives. Angew. Chem. Int. Ed. Engl. 48 (2009), 872–897.
53. [53] Tanida, I., Ueno, T., Kominami, E., LC3 and autophagy. Methods Mol. Biol. 445 (2008), 77–88.
54. [54] Mohamed, F., Marchettini, P., Stuart, O.A., Sugarbaker, P.H., Pharmacokinetics and tissue distribution of intraperitoneal paclitaxel with different carrier solutions. Cancer Chemother. Pharmacol. 52 (2003), 405–410.
55. [55] Tsai, M., Lu, Z., Wang, J., Yeh, T.K., Wientjes, M.G., Au, J.L., Effects of carrier on disposition and antitumor activity of intraperitoneal Paclitaxel. Pharm. Res. 24 (2007), 1691–1701.
56. [56] Au, J.L., Li, D., Gan, Y., Gao, X., Johnson, A.L., Johnston, J., et al. Pharmacodynamics of immediate and delayed effects of paclitaxel: role of slow apoptosis and intracellular drug retention. Cancer Res. 58 (1998), 2141–2148.
57. [57] Mosesson, Y., Mills, G.B., Yarden, Y., Derailed endocytosis: an emerging feature of cancer. Nat. Rev. Cancer 8 (2008), 835–850.
58. [58] Lei, H., Hofferberth, S.C., Liu, R., Colby, A., Tevis, K.M., Catalano, P., et al. Paclitaxel-loaded expansile nanoparticles enhance chemotherapeutic drug delivery in mesothelioma 3-dimensional multicellular spheroids. J. Thorac. Cardiovasc. Surg. 149 (2015), 1417–1425.
59. [59] Lu, Z., Tsai, M., Lu, D., Wang, J., Wientjes, M.G., Au, J.L., Tumor-penetrating microparticles for intraperitoneal therapy of ovarian cancer. J. Pharmacol. Exp. Ther. 327 (2008), 673–682.
60. [60] Mizushima, N., Yoshimori, T., Levine, B., Methods in mammalian autophagy research. Cell. 140 (2010), 313–326.
61. [61] Barth, S., Glick, D., Macleod, K.F., Autophagy: assays and artifacts. J. Pathol. 221 (2010), 117–124.
62. [62] Gonzalez-Angulo, A.M., Hortobagyi, G.N., Optimal schedule of paclitaxel: weekly is better. J. Clin. Oncol. 26 (2008), 1585–1587.
63. [63] Mitchison, T.J., The proliferation rate paradox in antimitotic chemotherapy. Mol. Biol. Cell. 23 (2012), 1–6.
64. [64] Tan, G., Heqing, L., Jiangbo, C., Ming, J., Yanhong, M., Xianghe, L., et al. Apoptosis induced by low-dose paclitaxel is associated with p53 upregulation in nasopharyngeal carcinoma cells. Int. J. Cancer 97 (2002), 168–172.