Skip to main content
Top
Published in: Cellular Oncology 6/2013

01-12-2013 | Original Paper

PEGylated liposomal Gemcitabine: insights into a potential breast cancer therapeutic

Authors: Anne-Laure Papa, Almas Sidiqui, Sri Uma Aisvarya Balasubramanian, Sasmit Sarangi, Matthew Luchette, Shiladitya Sengupta, Rania Harfouche

Published in: Cellular Oncology | Issue 6/2013

Login to get access

Abstract

Purpose

Nanoencapsulation of chemotherapeutics is an established method to target breast tumors and has been shown to enhance the efficacy of therapy in various animal models. During the past two decades, the nucleoside analog Gemcitabine has been under investigation to treat both recalcitrant and localized breast cancer, often in combination with other chemotherapeutics. In this study, we investigated the chemotherapeutic efficacy of a novel Gemcitabine-encapsulated liposome previously formulated by our group, GemPo, on both sensitive (4T1) and recalcitrant (MDA-MB-231) breast cancer cell lines.

Methods

Gemcitabine free drug and liposomal Gemcitabine were compared both in vitro and in vivo using breast cancer models.

Results

We demonstrated that GemPo differently hindered the growth, survival and migration of breast cancer cells, according to their drug sensitivities. Specifically, whereas GemPo was a more potent cytotoxic and apoptotic agent in sensitive breast cancer cells, it more potently inhibited cell migration in the resistant cell line. However, GemPo still acted as a more potent inhibitor of migration, in comparison with free Gemcitabine, irrespective of cell sensitivity. Administration of GemPo in a 4T1-bearing mouse model inhibited tumor growth while increasing mice survival, as compared with free Gemcitabine and a vehicle control. Interestingly, the inclusion of a mitotic inhibitor, Paclitaxel, synergized only with free Gemcitabine in this model, yet was as effective as GemPo alone. However, inclusion of Paclitaxel with GemPo significantly improved mouse survival.

Conclusions

Our study is the first to demonstrate the pleiotropic effects of Gemcitabine and Gemcitabine-loaded nanoparticles in breast cancer, and opens the door for a novel treatment for breast cancer patients.
Appendix
Available only for authorised users
Literature
1.
go back to reference American Cancer Society, Cancer Facts & Figures 2013 (American Cancer Society, Atlanta, 2013) American Cancer Society, Cancer Facts & Figures 2013 (American Cancer Society, Atlanta, 2013)
2.
go back to reference R.H. Johnson, F.L. Chien, A. Bleyer, Incidence of breast cancer with distant involvement among women in the United States, 1976 to 2009. JAMA: J. Am. Med. Assoc. 309, 800–805 (2013)CrossRef R.H. Johnson, F.L. Chien, A. Bleyer, Incidence of breast cancer with distant involvement among women in the United States, 1976 to 2009. JAMA: J. Am. Med. Assoc. 309, 800–805 (2013)CrossRef
3.
go back to reference R. Harfouche, S. Basu, S. Soni et al., Nanoparticle-mediated targeting of phosphatidylinositol-3-kinase signaling inhibits angiogenesis. Angiogenesis 12, 325–338 (2009)PubMedCrossRef R. Harfouche, S. Basu, S. Soni et al., Nanoparticle-mediated targeting of phosphatidylinositol-3-kinase signaling inhibits angiogenesis. Angiogenesis 12, 325–338 (2009)PubMedCrossRef
4.
go back to reference A. Paraskar, S. Soni, B. Roy et al., Rationally designed oxaliplatin-nanoparticle for enhanced antitumor efficacy. Nanotechnology 23, 075103 (2012)PubMedCrossRef A. Paraskar, S. Soni, B. Roy et al., Rationally designed oxaliplatin-nanoparticle for enhanced antitumor efficacy. Nanotechnology 23, 075103 (2012)PubMedCrossRef
5.
go back to reference M. Wang, M. Thanou, Targeting nanoparticles to cancer. Pharmacol. Res. Off. J. Ital. Pharmacol. Soc. 62, 90–99 (2010) M. Wang, M. Thanou, Targeting nanoparticles to cancer. Pharmacol. Res. Off. J. Ital. Pharmacol. Soc. 62, 90–99 (2010)
7.
go back to reference Y.C. Barenholz, D. Peer, Liposomes, lipid biophysics, and sphingolipid research: from basic to translation research. Chem. Phys. Lipids 165, 363–364 (2012)PubMedCrossRef Y.C. Barenholz, D. Peer, Liposomes, lipid biophysics, and sphingolipid research: from basic to translation research. Chem. Phys. Lipids 165, 363–364 (2012)PubMedCrossRef
8.
go back to reference J.A. Silverman, S.R. Deitcher, Marqibo((R)) (vincristine sulfate liposome injection) improves the pharmacokinetics and pharmacodynamics of vincristine. Cancer Chemother. Pharmacol. 71, 555–564 (2013)PubMedCrossRef J.A. Silverman, S.R. Deitcher, Marqibo((R)) (vincristine sulfate liposome injection) improves the pharmacokinetics and pharmacodynamics of vincristine. Cancer Chemother. Pharmacol. 71, 555–564 (2013)PubMedCrossRef
9.
go back to reference H.A. Burris 3rd, M.J. Moore, J. Andersen et al., Improvements in survival and clinical benefit with gemcitabine as first-line therapy for patients with advanced pancreas cancer: a randomized trial. J. Clin. Oncol. Off. J. Am. Soc. Clin. Oncol. 15, 2403–2413 (1997) H.A. Burris 3rd, M.J. Moore, J. Andersen et al., Improvements in survival and clinical benefit with gemcitabine as first-line therapy for patients with advanced pancreas cancer: a randomized trial. J. Clin. Oncol. Off. J. Am. Soc. Clin. Oncol. 15, 2403–2413 (1997)
10.
go back to reference J.L. Van Laethem, C. Verslype, J.L. Iovanna et al., New strategies and designs in pancreatic cancer research: consensus guidelines report from a European expert panel. Ann. Oncol. Off. J. Eur. Soc. Med. Oncol. / ESMO 23, 570–576 (2012)CrossRef J.L. Van Laethem, C. Verslype, J.L. Iovanna et al., New strategies and designs in pancreatic cancer research: consensus guidelines report from a European expert panel. Ann. Oncol. Off. J. Eur. Soc. Med. Oncol. / ESMO 23, 570–576 (2012)CrossRef
11.
go back to reference G.V. Scagliotti, P. Parikh, J. von Pawel et al., Phase III study comparing cisplatin plus gemcitabine with cisplatin plus pemetrexed in chemotherapy-naive patients with advanced-stage non-small-cell lung cancer. J. Clin. Oncol. Off. J. Am. Soc. Clin. Oncol. 26, 3543–3551 (2008)CrossRef G.V. Scagliotti, P. Parikh, J. von Pawel et al., Phase III study comparing cisplatin plus gemcitabine with cisplatin plus pemetrexed in chemotherapy-naive patients with advanced-stage non-small-cell lung cancer. J. Clin. Oncol. Off. J. Am. Soc. Clin. Oncol. 26, 3543–3551 (2008)CrossRef
12.
go back to reference J. Pfisterer, M. Plante, I. Vergote et al., Gemcitabine plus carboplatin compared with carboplatin in patients with platinum-sensitive recurrent ovarian cancer: an intergroup trial of the AGO-OVAR, the NCIC CTG, and the EORTC GCG. J. Clin. Oncol. Off. J. Am. Soc. Clin. Oncol. 24, 4699–4707 (2006)CrossRef J. Pfisterer, M. Plante, I. Vergote et al., Gemcitabine plus carboplatin compared with carboplatin in patients with platinum-sensitive recurrent ovarian cancer: an intergroup trial of the AGO-OVAR, the NCIC CTG, and the EORTC GCG. J. Clin. Oncol. Off. J. Am. Soc. Clin. Oncol. 24, 4699–4707 (2006)CrossRef
13.
go back to reference A.M. Murad, R.C. Guimaraes, B.C. Aragao et al., Phase II trial of the use of paclitaxel and gemcitabine as a salvage treatment in metastatic breast cancer. Am. J. Clin. Oncol. 24, 264–268 (2001)PubMedCrossRef A.M. Murad, R.C. Guimaraes, B.C. Aragao et al., Phase II trial of the use of paclitaxel and gemcitabine as a salvage treatment in metastatic breast cancer. Am. J. Clin. Oncol. 24, 264–268 (2001)PubMedCrossRef
14.
go back to reference P. Vici, A. Fabi, G. Metro et al., Phase I-II trial of prolonged gemcitabine infusion plus paclitaxel as a biweekly schedule for advanced breast cancer patients pretreated with anthracyclines. Cancer Chemother. Pharmacol. 67, 687–693 (2011)PubMedCrossRef P. Vici, A. Fabi, G. Metro et al., Phase I-II trial of prolonged gemcitabine infusion plus paclitaxel as a biweekly schedule for advanced breast cancer patients pretreated with anthracyclines. Cancer Chemother. Pharmacol. 67, 687–693 (2011)PubMedCrossRef
15.
go back to reference K.S. Albain, S.M. Nag, G. Calderillo-Ruiz et al., Gemcitabine plus Paclitaxel versus Paclitaxel monotherapy in patients with metastatic breast cancer and prior anthracycline treatment. J. Clin. Oncol. Off. J. Am. Soc. Clin. Oncol. 26, 3950–3957 (2008)CrossRef K.S. Albain, S.M. Nag, G. Calderillo-Ruiz et al., Gemcitabine plus Paclitaxel versus Paclitaxel monotherapy in patients with metastatic breast cancer and prior anthracycline treatment. J. Clin. Oncol. Off. J. Am. Soc. Clin. Oncol. 26, 3950–3957 (2008)CrossRef
16.
go back to reference A.L. Papa, S. Basu, P. Sengupta et al., Mechanistic studies of Gemcitabine-loaded nanoplatforms in resistant pancreatic cancer cells. BMC Cancer 12, 419 (2012)PubMedCrossRef A.L. Papa, S. Basu, P. Sengupta et al., Mechanistic studies of Gemcitabine-loaded nanoplatforms in resistant pancreatic cancer cells. BMC Cancer 12, 419 (2012)PubMedCrossRef
17.
go back to reference G. Haran, R. Cohen, L.K. Bar et al., Transmembrane ammonium sulfate gradients in liposomes produce efficient and stable entrapment of amphipathic weak bases. Biochim. Biophys. Acta 1151, 201–215 (1993)PubMedCrossRef G. Haran, R. Cohen, L.K. Bar et al., Transmembrane ammonium sulfate gradients in liposomes produce efficient and stable entrapment of amphipathic weak bases. Biochim. Biophys. Acta 1151, 201–215 (1993)PubMedCrossRef
18.
go back to reference K. Pliarchopoulou, D. Pectasides, Pancreatic cancer: current and future treatment strategies. Cancer Treat. Rev. 35, 431–436 (2009)PubMedCrossRef K. Pliarchopoulou, D. Pectasides, Pancreatic cancer: current and future treatment strategies. Cancer Treat. Rev. 35, 431–436 (2009)PubMedCrossRef
19.
go back to reference M.R. Kano, Y. Bae, C. Iwata et al., Improvement of cancer-targeting therapy, using nanocarriers for intractable solid tumors by inhibition of TGF-beta signaling. Proc. Natl. Acad. Sci. U. S. A. 104, 3460–3465 (2007)PubMedCrossRef M.R. Kano, Y. Bae, C. Iwata et al., Improvement of cancer-targeting therapy, using nanocarriers for intractable solid tumors by inhibition of TGF-beta signaling. Proc. Natl. Acad. Sci. U. S. A. 104, 3460–3465 (2007)PubMedCrossRef
20.
go back to reference M. Gaumet, A. Vargas, R. Gurny et al., Nanoparticles for drug delivery: the need for precision in reporting particle size parameters. Eur. J. Pharm. Biopharm. Off. J. Arbeitsgemeinschaft fur Pharmazeutische Verfahrenstechnik e.V 69, 1–9 (2008) M. Gaumet, A. Vargas, R. Gurny et al., Nanoparticles for drug delivery: the need for precision in reporting particle size parameters. Eur. J. Pharm. Biopharm. Off. J. Arbeitsgemeinschaft fur Pharmazeutische Verfahrenstechnik e.V 69, 1–9 (2008)
21.
go back to reference T. Lammers, V. Subr, K. Ulbrich et al., Simultaneous delivery of doxorubicin and gemcitabine to tumors in vivo using prototypic polymeric drug carriers. Biomaterials 30, 3466–3475 (2009)PubMedCrossRef T. Lammers, V. Subr, K. Ulbrich et al., Simultaneous delivery of doxorubicin and gemcitabine to tumors in vivo using prototypic polymeric drug carriers. Biomaterials 30, 3466–3475 (2009)PubMedCrossRef
22.
go back to reference D. Cosco, A. Bulotta, M. Ventura et al., In vivo activity of gemcitabine-loaded PEGylated small unilamellar liposomes against pancreatic cancer. Cancer Chemother. Pharmacol. 64, 1009–1020 (2009)PubMedCrossRef D. Cosco, A. Bulotta, M. Ventura et al., In vivo activity of gemcitabine-loaded PEGylated small unilamellar liposomes against pancreatic cancer. Cancer Chemother. Pharmacol. 64, 1009–1020 (2009)PubMedCrossRef
23.
go back to reference R.J. Gillies, Z. Liu, Z. Bhujwalla, 31P-MRS measurements of extracellular pH of tumors using 3-aminopropylphosphonate. Am. J. Physiol. 267, C195–C203 (1994)PubMed R.J. Gillies, Z. Liu, Z. Bhujwalla, 31P-MRS measurements of extracellular pH of tumors using 3-aminopropylphosphonate. Am. J. Physiol. 267, C195–C203 (1994)PubMed
24.
go back to reference V. Estrella, T. Chen, M. Lloyd et al., Acidity generated by the tumor microenvironment drives local invasion. Cancer Res. 73, 1524–1535 (2013)PubMedCrossRef V. Estrella, T. Chen, M. Lloyd et al., Acidity generated by the tumor microenvironment drives local invasion. Cancer Res. 73, 1524–1535 (2013)PubMedCrossRef
25.
go back to reference R.R. Arvizo, O.R. Miranda, D.F. Moyano et al., Modulating pharmacokinetics, tumor uptake and biodistribution by engineered nanoparticles. PloS One 6, e24374 (2011)PubMedCrossRef R.R. Arvizo, O.R. Miranda, D.F. Moyano et al., Modulating pharmacokinetics, tumor uptake and biodistribution by engineered nanoparticles. PloS One 6, e24374 (2011)PubMedCrossRef
26.
go back to reference S. Lerch, M. Dass, A. Musyanovych, et al., Polymeric nanoparticles of different sizes overcome the cell membrane barrier. Eur. J. Pharm. Biopharm. Off. J. Arbeitsgemeinschaft fur Pharmazeutische Verfahrenstechnik e.V, (2013) S. Lerch, M. Dass, A. Musyanovych, et al., Polymeric nanoparticles of different sizes overcome the cell membrane barrier. Eur. J. Pharm. Biopharm. Off. J. Arbeitsgemeinschaft fur Pharmazeutische Verfahrenstechnik e.V, (2013)
27.
go back to reference R. Luo, B. Neu, S.S. Venkatraman, Surface functionalization of nanoparticles to control cell interactions and drug release. Small 8, 2585–2594 (2012)PubMedCrossRef R. Luo, B. Neu, S.S. Venkatraman, Surface functionalization of nanoparticles to control cell interactions and drug release. Small 8, 2585–2594 (2012)PubMedCrossRef
28.
go back to reference C. Celia, N. Malara, R. Terracciano et al., Liposomal delivery improves the growth-inhibitory and apoptotic activity of low doses of gemcitabine in multiple myeloma cancer cells. Nanomed. Nanotechnol. Biol. Med. 4, 155–166 (2008)CrossRef C. Celia, N. Malara, R. Terracciano et al., Liposomal delivery improves the growth-inhibitory and apoptotic activity of low doses of gemcitabine in multiple myeloma cancer cells. Nanomed. Nanotechnol. Biol. Med. 4, 155–166 (2008)CrossRef
29.
go back to reference J. Suh, K.L. Choy, S.K. Lai et al., PEGylation of nanoparticles improves their cytoplasmic transport. Int. J. Nanomedicine 2, 735–741 (2007)PubMed J. Suh, K.L. Choy, S.K. Lai et al., PEGylation of nanoparticles improves their cytoplasmic transport. Int. J. Nanomedicine 2, 735–741 (2007)PubMed
30.
go back to reference M.R. Almofti, H. Harashima, Y. Shinohara et al., Cationic liposome-mediated gene delivery: biophysical study and mechanism of internalization. Arch. Biochem. Biophys. 410, 246–253 (2003)PubMedCrossRef M.R. Almofti, H. Harashima, Y. Shinohara et al., Cationic liposome-mediated gene delivery: biophysical study and mechanism of internalization. Arch. Biochem. Biophys. 410, 246–253 (2003)PubMedCrossRef
31.
go back to reference M. Kapoor, D.J. Burgess, Cellular uptake mechanisms of novel anionic siRNA lipoplexes. Pharm. Res. 30, 1161–1175 (2013)PubMedCrossRef M. Kapoor, D.J. Burgess, Cellular uptake mechanisms of novel anionic siRNA lipoplexes. Pharm. Res. 30, 1161–1175 (2013)PubMedCrossRef
32.
go back to reference J. Rejman, V. Oberle, I.S. Zuhorn et al., Size-dependent internalization of particles via the pathways of clathrin- and caveolae-mediated endocytosis. Biochem. J. 377, 159–169 (2004)PubMedCrossRef J. Rejman, V. Oberle, I.S. Zuhorn et al., Size-dependent internalization of particles via the pathways of clathrin- and caveolae-mediated endocytosis. Biochem. J. 377, 159–169 (2004)PubMedCrossRef
33.
go back to reference K. Quint, M. Tonigold, P. Di Fazio et al., Pancreatic cancer cells surviving gemcitabine treatment express markers of stem cell differentiation and epithelial-mesenchymal transition. Int. J. Oncol. 41, 2093–2102 (2012)PubMed K. Quint, M. Tonigold, P. Di Fazio et al., Pancreatic cancer cells surviving gemcitabine treatment express markers of stem cell differentiation and epithelial-mesenchymal transition. Int. J. Oncol. 41, 2093–2102 (2012)PubMed
34.
go back to reference F.M. Kievit, F.Y. Wang, C. Fang et al., Doxorubicin loaded iron oxide nanoparticles overcome multidrug resistance in cancer in vitro. J. Control. Release Off. J. Control. Release Soc. 152, 76–83 (2011)CrossRef F.M. Kievit, F.Y. Wang, C. Fang et al., Doxorubicin loaded iron oxide nanoparticles overcome multidrug resistance in cancer in vitro. J. Control. Release Off. J. Control. Release Soc. 152, 76–83 (2011)CrossRef
35.
go back to reference X. Dong, R.J. Mumper, Nanomedicinal strategies to treat multidrug-resistant tumors: current progress. Nanomedicine (Lond) 5, 597–615 (2010)CrossRef X. Dong, R.J. Mumper, Nanomedicinal strategies to treat multidrug-resistant tumors: current progress. Nanomedicine (Lond) 5, 597–615 (2010)CrossRef
36.
go back to reference V. Adamo, V. Lorusso, R. Rossello et al., Pegylated liposomal doxorubicin and gemcitabine in the front-line treatment of recurrent/metastatic breast cancer: a multicentre phase II study. Br. J. Cancer 98, 1916–1921 (2008)PubMedCrossRef V. Adamo, V. Lorusso, R. Rossello et al., Pegylated liposomal doxorubicin and gemcitabine in the front-line treatment of recurrent/metastatic breast cancer: a multicentre phase II study. Br. J. Cancer 98, 1916–1921 (2008)PubMedCrossRef
37.
go back to reference A.M. Storniolo, S.R. Allerheiligen, H.L. Pearce, Preclinical, pharmacologic, and phase I studies of gemcitabine. Semin. Oncol. 24, S7-2–S7-7 (1997) A.M. Storniolo, S.R. Allerheiligen, H.L. Pearce, Preclinical, pharmacologic, and phase I studies of gemcitabine. Semin. Oncol. 24, S7-2–S7-7 (1997)
38.
go back to reference R. Graeser, C. Bornmann, N. Esser et al., Antimetastatic effects of liposomal gemcitabine and empty liposomes in an orthotopic mouse model of pancreatic cancer. Pancreas 38, 330–337 (2009)PubMedCrossRef R. Graeser, C. Bornmann, N. Esser et al., Antimetastatic effects of liposomal gemcitabine and empty liposomes in an orthotopic mouse model of pancreatic cancer. Pancreas 38, 330–337 (2009)PubMedCrossRef
39.
go back to reference W.J. Gradishar, S. Tjulandin, N. Davidson et al., Phase III trial of nanoparticle albumin-bound paclitaxel compared with polyethylated castor oil-based paclitaxel in women with breast cancer. J. Clin. Oncol. Off. J. Am. Soc. Clin. Oncol. 23, 7794–7803 (2005)CrossRef W.J. Gradishar, S. Tjulandin, N. Davidson et al., Phase III trial of nanoparticle albumin-bound paclitaxel compared with polyethylated castor oil-based paclitaxel in women with breast cancer. J. Clin. Oncol. Off. J. Am. Soc. Clin. Oncol. 23, 7794–7803 (2005)CrossRef
40.
go back to reference W.J. Gradishar, D. Krasnojon, S. Cheporov et al., Significantly longer progression-free survival with nab-paclitaxel compared with docetaxel as first-line therapy for metastatic breast cancer. J. Clin. Oncol. Off. J. Am. Soc. Clin. Oncol. 27, 3611–3619 (2009)CrossRef W.J. Gradishar, D. Krasnojon, S. Cheporov et al., Significantly longer progression-free survival with nab-paclitaxel compared with docetaxel as first-line therapy for metastatic breast cancer. J. Clin. Oncol. Off. J. Am. Soc. Clin. Oncol. 27, 3611–3619 (2009)CrossRef
Metadata
Title
PEGylated liposomal Gemcitabine: insights into a potential breast cancer therapeutic
Authors
Anne-Laure Papa
Almas Sidiqui
Sri Uma Aisvarya Balasubramanian
Sasmit Sarangi
Matthew Luchette
Shiladitya Sengupta
Rania Harfouche
Publication date
01-12-2013
Publisher
Springer Netherlands
Published in
Cellular Oncology / Issue 6/2013
Print ISSN: 2211-3428
Electronic ISSN: 2211-3436
DOI
https://doi.org/10.1007/s13402-013-0146-4

Other articles of this Issue 6/2013

Cellular Oncology 6/2013 Go to the issue
Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras
Prof. Fabrice Barlesi
Developed by: Springer Medicine