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Cancer Chemotherapy and Pharmacology

, Volume 82, Issue 5, pp 741–755 | Cite as

Liposomal therapies in oncology: does one size fit all?

  • Isabel Sousa
  • Filipa Rodrigues
  • Hugo Prazeres
  • Raquel T. Lima
  • Paula Soares
Review Article
  • 254 Downloads

Abstract

Liposomal therapies opened the chapter of nanomedicine, in 1995, with the approval of liposomal doxorubicin (Doxil®) for the treatment of numerous types of cancer. For the first time, liposomes permitted the employment of potent chemotherapeutic agents with improved pharmacokinetic and pharmacodynamic profiles, with less undesired side effects. Liposomal therapies allow the drug encapsulation and more selective delivery in the tumor bed, particularly due to the enhanced permeation and retention effect. These unique characteristics explain why liposomal therapies are being increasingly considered as alternatives in cancer therapy and represent an important research field with the recent approval for clinical use and emergent formulations in clinical trials. Even so, the response rate of liposomal therapies varies between 5 and 71%, and they are still indistinguishably given to every patient. As already well-demonstrated for conventional chemotherapies and targeted therapies, there is also the need for predictive biomarkers that allow a better use of liposomal drugs, with higher patient quality of life. Our aim in this review was to address the approved liposomal therapies and to summarize the information concerning possible predictive markers of response in their various clinical applications, to personalize each patient treatment and maximize its efficacy.

Keywords

Cancer Drug delivery systems Liposomal therapy Nanotechnology Predictive markers 

Notes

Funding

This work was financed by FEDER—Fundo Europeu de Desenvolvimento Regional funds through the COMPETE 2020—Operacional Programme for Competitiveness and Internationalisation (POCI), Portugal 2020, and by Portuguese funds through FCT—Fundação para a Ciência e a Tecnologia/Ministério da Ciência, Tecnologia e Inovação in the framework of the project “Institute for Research and Innovation in Health Sciences” (POCI-01-0145-FEDER-007274) and the project POCI 01-0145-FEDER-031520. Further funding was obtained from the project “Advancing cancer research: from basic knowledgment to application”; NORTE-01-0145-FEDER-000029; “Projetos Estruturados de I&D&I”, funded by Norte 2020—Programa Operacional Regional do Norte.

Compliance with ethical standards

Conflicts of interest

The authors declare that they have no conflict of interest.

References

  1. 1.
    Wang AZ, Langer R, Farokhzad OC (2012) Nanoparticle delivery of cancer drugs. Annu Rev Med 63:185–198.  https://doi.org/10.1146/annurev-med-040210-162544 CrossRefPubMedGoogle Scholar
  2. 2.
    Barenholz Y (2012) Doxil (R)—the first FDA-approved nano-drug: lessons learned. J Control Release 160(2):117–134.  https://doi.org/10.1016/j.jconrel.2012.03.020 CrossRefPubMedGoogle Scholar
  3. 3.
    Cagel M, Grotz E, Bernabeu E, Moretton MA, Chiappetta DA (2017) Doxorubicin: nanotechnological overviews from bench to bedside. Drug Discov Today 22(2):270–281.  https://doi.org/10.1016/j.drudis.2016.11.005 CrossRefPubMedGoogle Scholar
  4. 4.
    D’Mello SR, Cruz CN, Chen ML, Kapoor M, Lee SL, Tyner KM (2017) The evolving landscape of drug products containing nanomaterials in the United States. Nat Nanotechnol 12(6):523–529.  https://doi.org/10.1038/nnano.2017.67 CrossRefPubMedGoogle Scholar
  5. 5.
    Allen TM, Cheng WW, Hare JI, Laginha KM (2006) Pharmacokinetics and pharmacodynamics of lipidic nano-particles in cancer. Anticancer Agents Med Chem 6(6):513–523CrossRefGoogle Scholar
  6. 6.
    Urba WJ, Hartmann LC, Longo DL, Steis RG, Smith JW, Kedar I, Creekmore S, Sznol M, Conlon K, Kopp WC et al (1990) Phase I and immunomodulatory study of a muramyl peptide, muramyl tripeptide phosphatidylethanolamine. Cancer Res 50(10):2979–2986PubMedGoogle Scholar
  7. 7.
    Veronese FM, Pasut G (2005) PEGylation, successful approach to drug delivery. Drug Discov Today 10(21):1451–1458.  https://doi.org/10.1016/S1359-6446(05)03575-0 CrossRefPubMedGoogle Scholar
  8. 8.
    Haran G, Cohen R, Bar LK, Barenholz Y (1993) Transmembrane ammonium sulfate gradients in liposomes produce efficient and stable entrapment of amphipathic weak bases. Biochim Biophys Acta 1151(2):201–215CrossRefGoogle Scholar
  9. 9.
    Prabhakar U, Maeda H, Jain RK, Sevick-Muraca EM, Zamboni W, Farokhzad OC, Barry ST, Gabizon A, Grodzinski P, Blakey DC (2013) Challenges and key considerations of the enhanced permeability and retention effect for nanomedicine drug delivery in oncology. Cancer Res 73(8):2412–2417.  https://doi.org/10.1158/0008-5472.CAN-12-4561 CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Stylianopoulos T, Jain RK (2015) Design considerations for nanotherapeutics in oncology. Nanomedicine 11(8):1893–1907.  https://doi.org/10.1016/j.nano.2015.07.015 CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Peer D, Karp JM, Hong S, Farokhzad OC, Margalit R, Langer R (2007) Nanocarriers as an emerging platform for cancer therapy. Nat Nanotechnol 2(12):751–760.  https://doi.org/10.1038/nnano.2007.387 CrossRefPubMedGoogle Scholar
  12. 12.
    Plourde K, Derbali RM, Desrosiers A, Dubath C, Vallee-Belisle A, Leblond J (2017) Aptamer-based liposomes improve specific drug loading and release. J Control Release 251:82–91.  https://doi.org/10.1016/j.jconrel.2017.02.026 CrossRefPubMedGoogle Scholar
  13. 13.
    Tran S, DeGiovanni PJ, Piel B, Rai P (2017) Cancer nanomedicine: a review of recent success in drug delivery. Clin Transl Med 6(1):44.  https://doi.org/10.1186/s40169-017-0175-0 CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Danhier F, Feron O, Preat V (2010) To exploit the tumor microenvironment: passive and active tumor targeting of nanocarriers for anti-cancer drug delivery. J Control Release 148(2):135–146.  https://doi.org/10.1016/j.jconrel.2010.08.027 CrossRefPubMedGoogle Scholar
  15. 15.
    Ruoslahti E (2012) Peptides as targeting elements and tissue penetration devices for nanoparticles. Adv Mater 24(28):3747–3756.  https://doi.org/10.1002/adma.201200454 CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Zylberberg C, Matosevic S (2016) Pharmaceutical liposomal drug delivery: a review of new delivery systems and a look at the regulatory landscape. Drug Deliv 23(9):3319–3329.  https://doi.org/10.1080/10717544.2016.1177136 CrossRefPubMedGoogle Scholar
  17. 17.
    Perez-Herrero E, Fernandez-Medarde A (2015) Advanced targeted therapies in cancer: drug nanocarriers, the future of chemotherapy. Eur J Pharm Biopharm 93:52–79.  https://doi.org/10.1016/j.ejpb.2015.03.018 CrossRefPubMedGoogle Scholar
  18. 18.
    Lammers T, Kiessling F, Hennink WE, Storm G (2012) Drug targeting to tumors: principles, pitfalls and (pre-) clinical progress. J Control Release 161(2):175–187.  https://doi.org/10.1016/j.jconrel.2011.09.063 CrossRefPubMedGoogle Scholar
  19. 19.
    Jhaveri A, Deshpande P, Torchilin V (2014) Stimuli-sensitive nanopreparations for combination cancer therapy. J Control Release 190:352–370.  https://doi.org/10.1016/j.jconrel.2014.05.002 CrossRefPubMedGoogle Scholar
  20. 20.
    Wicki A, Witzigmann D, Balasubramanian V, Huwyler J (2015) Nanomedicine in cancer therapy: challenges, opportunities, and clinical applications. J Control Release 200:138–157.  https://doi.org/10.1016/j.jconrel.2014.12.030 CrossRefPubMedGoogle Scholar
  21. 21.
    Chen KJ, Liang HF, Chen HL, Wang Y, Cheng PY, Liu HL, Xia Y, Sung HW (2013) A thermoresponsive bubble-generating liposomal system for triggering localized extracellular drug delivery. ACS Nano 7(1):438–446.  https://doi.org/10.1021/nn304474j CrossRefPubMedGoogle Scholar
  22. 22.
    Lyon PC, Griffiths LF, Lee J, Chung D, Carlisle R, Wu F, Middleton MR, Gleeson FV, Coussios CC (2017) Clinical trial protocol for TARDOX: a phase I study to investigate the feasibility of targeted release of lyso-thermosensitive liposomal doxorubicin (ThermoDox(R)) using focused ultrasound in patients with liver tumours. J Ther Ultrasound 5:28.  https://doi.org/10.1186/s40349-017-0104-0 CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Havel HA (2016) Where are the nanodrugs? An industry perspective on development of drug products containing nanomaterials. AAPS J 18(6):1351–1353.  https://doi.org/10.1208/s12248-016-9970-6 CrossRefPubMedGoogle Scholar
  24. 24.
    Sercombe L, Veerati T, Moheimani F, Wu SY, Sood AK, Hua S (2015) Advances and challenges of liposome assisted drug delivery. Front Pharmacol 6:286.  https://doi.org/10.3389/fphar.2015.00286 CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Slingerland M, Guchelaar HJ, Gelderblom H (2012) Liposomal drug formulations in cancer therapy: 15 years along the road. Drug Discov Today 17(3–4):160–166.  https://doi.org/10.1016/j.drudis.2011.09.015 CrossRefPubMedGoogle Scholar
  26. 26.
    Pandey H, Rani R, Agarwal V (2016) Liposome and their applications in cancer therapy. Braz Arch Biol Technol 59:e16150477.  https://doi.org/10.1590/1678-4324-2016150477 CrossRefGoogle Scholar
  27. 27.
    Bulbake U, Doppalapudi S, Kommineni N, Khan W (2017) Liposomal formulations in clinical use: an updated review. Pharmaceutics.  https://doi.org/10.3390/pharmaceutics9020012 CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Gabizon A, Shmeeda H, Barenholz Y (2003) Pharmacokinetics of pegylated liposomal Doxorubicin: review of animal and human studies. Clin Pharmacokinet 42(5):419–436.  https://doi.org/10.2165/00003088-200342050-00002 CrossRefPubMedGoogle Scholar
  29. 29.
    Stewart S, Jablonowski H, Goebel FD, Arasteh K, Spittle M, Rios A, Aboulafia D, Galleshaw J, Dezube BJ (1998) Randomized comparative trial of pegylated liposomal doxorubicin versus bleomycin and vincristine in the treatment of AIDS-related Kaposi’s sarcoma. International Pegylated Liposomal Doxorubicin Study Group. J Clin Oncol 16(2):683–691.  https://doi.org/10.1200/jco.1998.16.2.683 CrossRefPubMedGoogle Scholar
  30. 30.
    Pignata S, Scambia G, Savarese A, Breda E, Sorio R, Pisano C, Lorusso D, Cognetti F, Vernaglia Lombardi A, Gebbia V, Scollo P, Morabito A, Signoriello G, Perrone F (2009) Carboplatin and pegylated liposomal doxorubicin for advanced ovarian cancer: preliminary activity results of the MITO-2 phase III trial. Oncology 76(1):49–54.  https://doi.org/10.1159/000178760 CrossRefPubMedGoogle Scholar
  31. 31.
    O’Brien ME, Wigler N, Inbar M, Rosso R, Grischke E, Santoro A, Catane R, Kieback DG, Tomczak P, Ackland SP, Orlandi F, Mellars L, Alland L, Tendler C, Group CBCS (2004) Reduced cardiotoxicity and comparable efficacy in a phase III trial of pegylated liposomal doxorubicin HCl (CAELYX/Doxil) versus conventional doxorubicin for first-line treatment of metastatic breast cancer. Ann Oncol 15(3):440–449CrossRefGoogle Scholar
  32. 32.
    Rifkin RM, Gregory SA, Mohrbacher A, Hussein MA (2006) Pegylated liposomal doxorubicin, vincristine, and dexamethasone provide significant reduction in toxicity compared with doxorubicin, vincristine, and dexamethasone in patients with newly diagnosed multiple myeloma: a Phase III multicenter randomized trial. Cancer 106(4):848–858.  https://doi.org/10.1002/cncr.21662 CrossRefPubMedGoogle Scholar
  33. 33.
    Fukuda A, Tahara K, Hane Y, Matsui T, Sasaoka S, Hatahira H, Motooka Y, Hasegawa S, Naganuma M, Abe J, Nakao S, Takeuchi H, Nakamura M (2017) Comparison of the adverse event profiles of conventional and liposomal formulations of doxorubicin using the FDA adverse event reporting system. PLoS One 12(9):e0185654.  https://doi.org/10.1371/journal.pone.0185654 CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Charrois GJ, Allen TM (2004) Drug release rate influences the pharmacokinetics, biodistribution, therapeutic activity, and toxicity of pegylated liposomal doxorubicin formulations in murine breast cancer. Biochim Biophysica Acta (BBA)-Biomembr 1663(1):167–177CrossRefGoogle Scholar
  35. 35.
    Harris L, Batist G, Belt R, Rovira D, Navari R, Azarnia N, Welles L, Winer E, Group TDS (2002) Liposome-encapsulated doxorubicin compared with conventional doxorubicin in a randomized multicenter trial as first-line therapy of metastatic breast carcinoma. Cancer 94(1):25–36CrossRefGoogle Scholar
  36. 36.
    Fumagalli L, Zucchetti M, Parisi I, Vigano MG, Zecca B, Careddu A, D’Incalci M, Lazzarin A (2000) The pharmacokinetics of liposomal encapsulated daunorubicin are not modified by HAART in patients with HIV-associated Kaposi’s sarcoma. Cancer Chemother Pharmacol 45(6):495–501.  https://doi.org/10.1007/s002800051025 CrossRefPubMedGoogle Scholar
  37. 37.
    Gill PS, Wernz J, Scadden DT, Cohen P, Mukwaya GM, von Roenn JH, Jacobs M, Kempin S, Silverberg I, Gonzales G, Rarick MU, Myers AM, Shepherd F, Sawka C, Pike MC, Ross ME (1996) Randomized phase III trial of liposomal daunorubicin versus doxorubicin, bleomycin, and vincristine in AIDS-related Kaposi’s sarcoma. J Clin Oncol 14(8):2353–2364.  https://doi.org/10.1200/JCO.1996.14.8.2353 CrossRefPubMedGoogle Scholar
  38. 38.
    Jahn F, Jordan K, Behlendorf T, Globig C, Schmoll HJ, Muller-Tidow C, Jordan B (2015) Safety and efficacy of liposomal Cytarabine in the treatment of Neoplastic meningitis. Oncology 89(3):137–142.  https://doi.org/10.1159/000380913 CrossRefPubMedGoogle Scholar
  39. 39.
    Krishna R, Webb MS, St Onge G, Mayer LD (2001) Liposomal and nonliposomal drug pharmacokinetics after administration of liposome-encapsulated vincristine and their contribution to drug tissue distribution properties. J Pharmacol Exp Ther 298(3):1206–1212PubMedGoogle Scholar
  40. 40.
    Douer D (2016) Efficacy and safety of vincristine sulfate liposome injection in the treatment of adult acute lymphocytic leukemia. Oncologist 21(7):840–847.  https://doi.org/10.1634/theoncologist.2015-0391 CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Lancet JE, Uy GL, Cortes JE, Newell LF, Lin TL, Ritchie EK, Stuart RK, Strickland SA, Hogge D, Solomon SR, Stone RM, Bixby DL, Kolitz JE, Schiller GJ, Wieduwilt MJ, Ryan DH, Hoering A, Banerjee K, Chiarella M, Louie AC, Medeiros BC (2018) CPX-351 (cytarabine and daunorubicin) Liposome for Injection Versus Conventional Cytarabine Plus Daunorubicin in Older Patients With Newly Diagnosed Secondary Acute Myeloid Leukemia. J Clin Oncol.  https://doi.org/10.1200/JCO.2017.77.6112 CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Stenger M (2017) Liposome-encapsulated daunorubicin and cytarabine for AML subtypes. ASCO POST. http://www.ascopost.com/issues/december-10-2017/liposome-encapsulated-daunorubicin-and-cytarabine-for-aml-subtypes/
  43. 43.
    Wang-Gillam A, Li CP, Bodoky G, Dean A, Shan YS, Jameson G, Macarulla T, Lee KH, Cunningham D, Blanc JF, Hubner RA, Chiu CF, Schwartsmann G, Siveke JT, Braiteh F, Moyo V, Belanger B, Dhindsa N, Bayever E, Von Hoff DD, Chen LT, Group N-S (2016) Nanoliposomal irinotecan with fluorouracil and folinic acid in metastatic pancreatic cancer after previous gemcitabine-based therapy (NAPOLI-1): a global, randomised, open-label, phase 3 trial. Lancet 387(10018):545–557.  https://doi.org/10.1016/S0140-6736(15)00986-1 CrossRefPubMedGoogle Scholar
  44. 44.
    Rahman FAU, Ali S, Saif MW (2017) Update on the role of nanoliposomal irinotecan in the treatment of metastatic pancreatic cancer. Therap Adv Gastroenterol 10(7):563–572.  https://doi.org/10.1177/1756283X17705328 CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Venkatakrishnan K, Liu Y, Noe D, Mertz J, Bargfrede M, Marbury T, Farbakhsh K, Oliva C, Milton A (2014) Pharmacokinetics and pharmacodynamics of liposomal mifamurtide in adult volunteers with mild or moderate hepatic impairment. Br J Clin Pharmacol 77(6):998–1010.  https://doi.org/10.1111/bcp.12261 CrossRefPubMedGoogle Scholar
  46. 46.
    Meyers PA, Schwartz CL, Krailo MD, Healey JH, Bernstein ML, Betcher D, Ferguson WS, Gebhardt MC, Goorin AM, Harris M, Kleinerman E, Link MP, Nadel H, Nieder M, Siegal GP, Weiner MA, Wells RJ, Womer RB, Grier HE, Children’s Oncology G (2008) Osteosarcoma: the addition of muramyl tripeptide to chemotherapy improves overall survival–a report from the Children’s Oncology Group. J Clin Oncol 26(4):633–638.  https://doi.org/10.1200/JCO.2008.14.0095 CrossRefPubMedGoogle Scholar
  47. 47.
    Kleinerman ES, Gano JB, Johnston DA, Benjamin RS, Jaffe N (1995) Efficacy of liposomal muramyl tripeptide (CGP 19835A) in the treatment of relapsed osteosarcoma. Am J Clin Oncol 18(2):93–99CrossRefGoogle Scholar
  48. 48.
    Northfelt DW, Dezube BJ, Thommes JA, Miller BJ, Fischl MA, Friedman-Kien A, Kaplan LD, Du Mond C, Mamelok RD, Henry DH (1998) Pegylated-liposomal doxorubicin versus doxorubicin, bleomycin, and vincristine in the treatment of AIDS-related Kaposi’s sarcoma: results of a randomized phase III clinical trial. J Clin Oncol 16(7):2445–2451.  https://doi.org/10.1200/JCO.1998.16.7.2445 CrossRefPubMedGoogle Scholar
  49. 49.
    Gordon AN, Fleagle JT, Guthrie D, Parkin DE, Gore ME, Lacave AJ (2001) Recurrent epithelial ovarian carcinoma: a randomized phase III study of pegylated liposomal doxorubicin versus topotecan. J Clin Oncol 19(14):3312–3322.  https://doi.org/10.1200/JCO.2001.19.14.3312 CrossRefPubMedGoogle Scholar
  50. 50.
    Gibson JM, Alzghari S, Ahn C, Trantham H, La-Beck NM (2013) The role of pegylated liposomal doxorubicin in ovarian cancer: a meta-analysis of randomized clinical trials. Oncologist 18(9):1022–1031.  https://doi.org/10.1634/theoncologist.2013-0126 CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Keller AM, Mennel RG, Georgoulias VA, Nabholtz JM, Erazo A, Lluch A, Vogel CL, Kaufmann M, von Minckwitz G, Henderson IC, Mellars L, Alland L, Tendler C (2004) Randomized phase III trial of pegylated liposomal doxorubicin versus vinorelbine or mitomycin C plus vinblastine in women with taxane-refractory advanced breast cancer. J Clin Oncol 22(19):3893–3901.  https://doi.org/10.1200/JCO.2004.08.157 CrossRefPubMedGoogle Scholar
  52. 52.
    Batist G, Ramakrishnan G, Rao CS, Chandrasekharan A, Gutheil J, Guthrie T, Shah P, Khojasteh A, Nair MK, Hoelzer K, Tkaczuk K, Park YC, Lee LW (2001) Reduced cardiotoxicity and preserved antitumor efficacy of liposome-encapsulated doxorubicin and cyclophosphamide compared with conventional doxorubicin and cyclophosphamide in a randomized, multicenter trial of metastatic breast cancer. J Clin Oncol 19(5):1444–1454.  https://doi.org/10.1200/JCO.2001.19.5.1444 CrossRefPubMedGoogle Scholar
  53. 53.
    Stenger M (2012) Liposomal vincristine for adult patients with relapsed/refractory acute lymphoblastic leukemia. The ASCO Post. http://www.ascopost.com/issues/december-15-2012/liposomal-vincristine-for-adult-patients-withrelapsedrefractory-acute-lymphoblastic-leukemia/
  54. 54.
    Latagliata R, Breccia M, Fazi P, Iacobelli S, Martinelli G, Di Raimondo F, Sborgia M, Fabbiano F, Pirrotta MT, Zaccaria A, Amadori S, Caramatti C, Falzetti F, Candoni A, Mattei D, Morselli M, Alimena G, Vignetti M, Baccarani M, Mandelli F (2008) Liposomal daunorubicin versus standard daunorubicin: long term follow-up of the GIMEMA GSI 103 AMLE randomized trial in patients older than 60 years with acute myelogenous leukaemia. Br J Haematol 143(5):681–689.  https://doi.org/10.1111/j.1365-2141.2008.07400.x CrossRefPubMedGoogle Scholar
  55. 55.
    Glantz MJ, LaFollette S, Jaeckle KA, Shapiro W, Swinnen L, Rozental JR, Phuphanich S, Rogers LR, Gutheil JC, Batchelor T, Lyter D, Chamberlain M, Maria BL, Schiffer C, Bashir R, Thomas D, Cowens W, Howell SB (1999) Randomized trial of a slow-release versus a standard formulation of cytarabine for the intrathecal treatment of lymphomatous meningitis. J Clin Oncol 17(10):3110–3116.  https://doi.org/10.1200/JCO.1999.17 CrossRefPubMedGoogle Scholar
  56. 56.
    Lancet JE, Uy GL, Cortes JE, Newell LF, Lin TL, Ritchie EK, Stuart RK, Strickland SA, Hogge D, Solomon SR, Stone RM, Bixby DL, Kolitz JE, Schiller GJ, Wieduwilt MJ, Ryan DH, Hoering A, Chiarella M, Louie AC, Medeiros BC (2016) Final results of a phase III randomized trial of CPX-351 versus 7 + 3 in older patients with newly diagnosed high risk (secondary) AML. J Clin Oncol 34(15_suppl):7000.  https://doi.org/10.1200/JCO.2016.34.15_suppl.7000 CrossRefGoogle Scholar
  57. 57.
    Adiwijaya BS, Kim J, Lang I, Csoszi T, Cubillo A, Chen JS, Wong M, Park JO, Kim JS, Rau KM, Melichar B, Gallego JB, Fitzgerald J, Belanger B, Molnar I, Ma WW (2017) Population Pharmacokinetics of liposomal irinotecan in patients with cancer. Clin Pharmacol Ther 102(6):997–1005.  https://doi.org/10.1002/cpt.720 CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    Kipps E, Young K, Starling N (2017) Liposomal irinotecan in gemcitabine-refractory metastatic pancreatic cancer: efficacy, safety and place in therapy. Ther Adv Med Oncol 9(3):159–170.  https://doi.org/10.1177/1758834016688816 CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    Kager L, Potschger U, Bielack S (2010) Review of mifamurtide in the treatment of patients with osteosarcoma. Ther Clin Risk Manag 6:279–286CrossRefGoogle Scholar
  60. 60.
    Wang X, Ishida T, Kiwada H (2007) Anti-PEG IgM elicited by injection of liposomes is involved in the enhanced blood clearance of a subsequent dose of PEGylated liposomes. J Control Release 119(2):236–244.  https://doi.org/10.1016/j.jconrel.2007.02.010 CrossRefPubMedGoogle Scholar
  61. 61.
    Gill PS, Wernz J, Scadden DT, Cohen P, Mukwaya GM, von Roenn JH, Jacobs M, Kempin S, Silverberg I, Gonzales G (1996) Randomized phase III trial of liposomal daunorubicin versus doxorubicin, bleomycin, and vincristine in AIDS-related Kaposi’s sarcoma. J Clin Oncol 14(8):2353–2364CrossRefGoogle Scholar
  62. 62.
    Pathak P, Hess R, Weiss MA (2014) Liposomal vincristine for relapsed or refractory Ph-negative acute lymphoblastic leukemia: a review of literature. Ther Adv Hematol 5(1):18–24.  https://doi.org/10.1177/2040620713519016 CrossRefPubMedPubMedCentralGoogle Scholar
  63. 63.
    Alexandre J, Brown C, Coeffic D, Raban N, Pfisterer J, Maenpaa J, Chalchal H, Fitzharris B, Volgger B, Vergote I, Pisano C, Ferrero A, Pujade-Lauraine E (2012) CA-125 can be part of the tumour evaluation criteria in ovarian cancer trials: experience of the GCIG CALYPSO trial. Br J Cancer 106(4):633–637.  https://doi.org/10.1038/bjc.2011.593 CrossRefPubMedPubMedCentralGoogle Scholar
  64. 64.
    Oaknin A, Barretina P, Perez X, Jimenez L, Velasco M, Alsina M, Brunet J, Germa JR, Beltran M (2010) CA-125 response patterns in patients with recurrent ovarian cancer treated with pegylated liposomal doxorubicin (PLD). Int J Gynecol Cancer 20(1):87–91.  https://doi.org/10.1111/IGC.0b013e3181c16ba1 CrossRefPubMedGoogle Scholar
  65. 65.
    Power P, Stuart G, Oza A, Provencher D, Bentley JR, Miller WH, Pouliot JF (2009) Efficacy of pegylated liposomal doxorubicin (PLD) plus carboplatin in ovarian cancer patients who recur within six to twelve months: a phase II study. Gynecol Oncol 114(3):410–414.  https://doi.org/10.1016/j.ygyno.2009.04.037 CrossRefPubMedGoogle Scholar
  66. 66.
    Coleman RL, Gordon A, Barter J, Sun S, Rackoff W, Herzog TJ (2007) Early changes in CA125 after treatment with pegylated liposomal doxorubicin or topotecan do not always reflect best response in recurrent ovarian cancer patients. Oncologist 12(1):72–78.  https://doi.org/10.1634/theoncologist.12-1-72 CrossRefPubMedGoogle Scholar
  67. 67.
    Gossner G, Coleman RL, Mutch DG, Horowitz NS, Rader JS, Gibb RK, Powell MA, Herzog TJ (2006) CA-125 response in patients with recurrent ovarian or primary peritoneal cancer treated with pegylated liposomal doxorubicin or topotecan. Gynecol Oncol 103(1):212–218.  https://doi.org/10.1016/j.ygyno.2006.02.026 CrossRefPubMedGoogle Scholar
  68. 68.
    Tanguay JS, Ansari J, Buckley L, Fernando I (2009) Epithelial ovarian cancer: role of pegylated liposomal Doxorubicin in prolonging the platinum-free interval and cancer antigen 125 trends during treatment. Int J Gynecol Cancer 19(3):361–366.  https://doi.org/10.1111/IGC.0b013e3181a1c7aa CrossRefPubMedGoogle Scholar
  69. 69.
    Ferrandina G, Ludovisi M, Corrado G, Carone V, Petrillo M, Scambia G (2008) Prognostic role of Ca125 response criteria and RECIST criteria: analysis of results from the MITO-3 phase III trial of gemcitabine versus pegylated liposomal doxorubicin in recurrent ovarian cancer. Gynecol Oncol 109(2):187–193.  https://doi.org/10.1016/j.ygyno.2008.01.039 CrossRefPubMedGoogle Scholar
  70. 70.
    Lee CK, Friedlander M, Brown C, Gebski VJ, Georgoulopoulos A, Vergote I, Pignata S, Donadello N, Schmalfeldt B, Delva R, Mirza MR, Sauthier P, Pujade-Lauraine E, Lord SJ, Simes RJ (2011) Early decline in cancer antigen 125 as a surrogate for progression-free survival in recurrent ovarian cancer. J Natl Cancer Inst 103(17):1338–1342.  https://doi.org/10.1093/jnci/djr282 CrossRefPubMedGoogle Scholar
  71. 71.
    Fabi A, Ferretti G, Salesi N, Papaldo P, Carlini P, Ciccarese M, Di Cocco B, Cecere F, Nardoni C, Felici A, Cognetti F (2005) Can HER2 overexpression predict response to pegylated liposomal doxorubicin in metastatic breast cancer patients? Ann Oncol 16(3):516–517.  https://doi.org/10.1093/annonc/mdi078 CrossRefPubMedGoogle Scholar
  72. 72.
    Orr MS, O’Connor PM, Kohn KW (2000) Effects of c-erbB2 overexpression on the drug sensitivities of normal human mammary epithelial cells. J Natl Cancer Inst 92(12):987–994CrossRefGoogle Scholar
  73. 73.
    Gianni L, Norton L, Wolmark N, Suter TM, Bonadonna G, Hortobagyi GN (2009) Role of anthracyclines in the treatment of early breast cancer. J Clin Oncol 27(28):4798–4808.  https://doi.org/10.1200/JCO.2008.21.4791 CrossRefPubMedGoogle Scholar
  74. 74.
    Arriola E, Rodriguez-Pinilla SM, Lambros MB, Jones RL, James M, Savage K, Smith IE, Dowsett M, Reis-Filho JS (2007) Topoisomerase II alpha amplification may predict benefit from adjuvant anthracyclines in HER2 positive early breast cancer. Breast Cancer Res Treat 106(2):181–189.  https://doi.org/10.1007/s10549-006-9492-5 CrossRefPubMedGoogle Scholar
  75. 75.
    Torrisi R, Cardillo A, Cancello G, Dellapasqua S, Balduzzi A, Ghisini R, Luini A, Veronesi P, Viale G, Goldhirsch A, Colleoni M (2010) Phase II trial of combination of pegylated liposomal doxorubicin, cisplatin, and infusional 5-fluorouracil (CCF) plus trastuzumab as preoperative treatment for locally advanced and inflammatory breast cancer. Clin Breast Cancer 10(6):483–488.  https://doi.org/10.3816/CBC.2010.n.064 CrossRefPubMedGoogle Scholar
  76. 76.
    Offidani M, Corvatta L, Polloni C, Piersantelli MN, Galieni P, Visani G, Alesiani F, Catarini M, Brunori M, Burattini M, Centurioni R, Ferranti M, Giuliodori L, Candela M, Mele A, Marconi M, Leoni P (2008) Serum C-reactive protein at diagnosis and response to therapy is the most powerful factor predicting outcome of multiple myeloma treated with thalidomide/ anthracycline-based therapy. Clin Lymphoma Myeloma 8(5):294–299.  https://doi.org/10.3816/CLM.2008.n.041 CrossRefPubMedGoogle Scholar
  77. 77.
    Yokoi K, Tanei T, Godin B, van de Ven AL, Hanibuchi M, Matsunoki A, Alexander J, Ferrari M (2014) Serum biomarkers for personalization of nanotherapeutics-based therapy in different tumor and organ microenvironments. Cancer Lett 345(1):48–55.  https://doi.org/10.1016/j.canlet.2013.11.015 CrossRefPubMedGoogle Scholar
  78. 78.
    Erriquez J, Becco P, Olivero M, Ponzone R, Maggiorotto F, Ferrero A, Scalzo MS, Canuto EM, Sapino A, Verdun di Cantogno L, Bruna P, Aglietta M, Di Renzo MF, Valabrega G (2015) TOP2A gene copy gain predicts response of epithelial ovarian cancers to pegylated liposomal doxorubicin: TOP2A as marker of response to PLD in ovarian cancer. Gynecol Oncol 138(3):627–633.  https://doi.org/10.1016/j.ygyno.2015.06.025 CrossRefPubMedGoogle Scholar
  79. 79.
    Jarvinen TA, Tanner M, Rantanen V, Barlund M, Borg A, Grenman S, Isola J (2000) Amplification and deletion of topoisomerase IIalpha associate with ErbB-2 amplification and affect sensitivity to topoisomerase II inhibitor doxorubicin in breast cancer. Am J Pathol 156(3):839–847CrossRefGoogle Scholar
  80. 80.
    Du Y, Zhou Q, Yin W, Zhou L, Di G, Shen Z, Shao Z, Lu J (2011) The role of topoisomerase IIalpha in predicting sensitivity to anthracyclines in breast cancer patients: a meta-analysis of published literatures. Breast Cancer Res Treat 129(3):839–848.  https://doi.org/10.1007/s10549-011-1694-9 CrossRefPubMedGoogle Scholar
  81. 81.
    Scandinavian Breast Group T, Tanner M, Isola J, Wiklund T, Erikstein B, Kellokumpu-Lehtinen P, Malmstrom P, Wilking N, Nilsson J, Bergh J (2006) Topoisomerase IIalpha gene amplification predicts favorable treatment response to tailored and dose-escalated anthracycline-based adjuvant chemotherapy in HER-2/neu-amplified breast cancer: Scandinavian Breast Group Trial 9401. J Clin Oncol 24(16):2428–2436.  https://doi.org/10.1200/JCO.2005.02.9264 CrossRefGoogle Scholar
  82. 82.
    Durbecq V, Paesmans M, Cardoso F, Desmedt C, Di Leo A, Chan S, Friedrichs K, Pinter T, Van Belle S, Murray E, Bodrogi I, Walpole E, Lesperance B, Korec S, Crown J, Simmonds P, Perren TJ, Leroy JY, Rouas G, Sotiriou C, Piccart M, Larsimont D (2004) Topoisomerase-II alpha expression as a predictive marker in a population of advanced breast cancer patients randomly treated either with single-agent doxorubicin or single-agent docetaxel. Mol Cancer Ther 3(10):1207–1214PubMedGoogle Scholar
  83. 83.
    Li TK, Liu LF (2001) Tumor cell death induced by topoisomerase-targeting drugs. Annu Rev Pharmacol Toxicol 41:53–77.  https://doi.org/10.1146/annurev.pharmtox.41.1.53 CrossRefPubMedGoogle Scholar
  84. 84.
    Green H, Stal O, Bachmeier K, Backlund LM, Carlsson L, Hansen J, Lagerlund M, Norberg B, Franzen A, Aleskog A, Malmstrom A (2011) Pegylated liposomal doxorubicin as first-line monotherapy in elderly women with locally advanced or metastatic breast cancer: novel treatment predictive factors identified. Cancer Lett 313(2):145–153.  https://doi.org/10.1016/j.canlet.2011.07.017 CrossRefPubMedGoogle Scholar
  85. 85.
    Perrone F, Baldassarre G, Indraccolo S, Signoriello S, Chiappetta G, Esposito F, Ferrandina G, Franco R, Mezzanzanica D, Sonego M, Zulato E, Zannoni GF, Canzonieri V, Scambia G, Sorio R, Savarese A, Breda E, Scollo P, Ferro A, Tamberi S, Febbraro A, Natale D, Di Maio M, Califano D, Scognamiglio G, Lorusso D, Canevari S, Losito S, Gallo C, Pignata S (2016) Biomarker analysis of the MITO2 phase III trial of first-line treatment in ovarian cancer: predictive value of DNA-PK and phosphorylated ACC. Oncotarget 7(45):72654–72661.  https://doi.org/10.18632/oncotarget.12056 CrossRefPubMedPubMedCentralGoogle Scholar
  86. 86.
    Shin DH, Choi YJ, Park JW (2014) SIRT1 and AMPK mediate hypoxia-induced resistance of non-small cell lung cancers to cisplatin and doxorubicin. Cancer Res 74(1):298–308.  https://doi.org/10.1158/0008-5472.CAN-13-2620 CrossRefPubMedGoogle Scholar
  87. 87.
    Prazeres H, Torres J, Rodrigues F, Pinto M, Pastoriza MC, Gomes D, Cameselle-Teijeiro J, Vidal A, Martins TC, Sobrinho-Simoes M, Soares P (2011) Chromosomal, epigenetic and microRNA-mediated inactivation of LRP1B, a modulator of the extracellular environment of thyroid cancer cells. Oncogene 30(11):1302–1317.  https://doi.org/10.1038/onc.2010.512 CrossRefPubMedGoogle Scholar
  88. 88.
    Chung NS, Wasan KM (2004) Potential role of the low-density lipoprotein receptor family as mediators of cellular drug uptake. Adv Drug Deliv Rev 56(9):1315–1334.  https://doi.org/10.1016/j.addr.2003.12.003 CrossRefPubMedGoogle Scholar
  89. 89.
    Cowin PA, George J, Fereday S, Loehrer E, Van Loo P, Cullinane C, Etemadmoghadam D, Ftouni S, Galletta L, Anglesio MS, Hendley J, Bowes L, Sheppard KE, Christie EL, Pearson RB, Harnett PR, Heinzelmann-Schwarz V, Friedlander M, McNally O, Quinn M, Campbell P, deFazio A, Bowtell DD (2012) LRP1B deletion in high-grade serous ovarian cancers is associated with acquired chemotherapy resistance to liposomal doxorubicin. Aust Ovarian Cancer Res 72(16):4060–4073.  https://doi.org/10.1158/0008-5472.CAN-12-0203 CrossRefGoogle Scholar
  90. 90.
    Lopes-Rodrigues V, Seca H, Sousa D, Sousa E, Lima RT, Vasconcelos MH (2014) The network of P-glycoprotein and microRNAs interactions. Int J Cancer 135(2):253–263.  https://doi.org/10.1002/ijc.28500 CrossRefPubMedGoogle Scholar
  91. 91.
    Liu Y, Rohrs J, Wang P (2014) Advances and challenges in the use of nanoparticles to optimize PK/PD interactions of combined anti-cancer therapies. Curr Drug Metab 15(8):818–828CrossRefGoogle Scholar
  92. 92.
    Arrieta O, Medina LA, Estrada-Lobato E, Ramirez-Tirado LA, Mendoza-Garcia VO, de la Garza-Salazar J (2014) High liposomal doxorubicin tumour tissue distribution, as determined by radiopharmaceutical labelling with (99 m)Tc-LD, is associated with the response and survival of patients with unresectable pleural mesothelioma treated with a combination of liposomal doxorubicin and cisplatin. Cancer Chemother Pharmacol 74(1):211–215.  https://doi.org/10.1007/s00280-014-2477-x CrossRefPubMedGoogle Scholar
  93. 93.
    Yamada Y, Kawaguchi R, Ito F, Iwai K, Niiro E, Shigetomi H, Tanase Y, Kobayashi H (2017) Skin-mucous membrane disorder and therapeutic effect of pegylated liposomal doxorubicin in recurrent ovarian cancer. J Obstet Gynaecol Res 43(7):1194–1199.  https://doi.org/10.1111/jog.13334 CrossRefPubMedGoogle Scholar
  94. 94.
    Franchina T, Adamo B, Ricciardi GR, Caristi N, Agostino RM, Proto C, Adamo V (2012) Activity of pegylated liposomal doxorubicin in combination with gemcitabine in triple negative breast cancer with skin involvement: two case reports. Cancer Boil Therapy 13(7):472–476.  https://doi.org/10.4161/cbt.19593 CrossRefGoogle Scholar
  95. 95.
    Uriarte-Pinto M, Escolano-Pueyo A, Gimeno-Ballester V, Pascual-Martinez O, Abad-Sazatornil MR, Agustin-Ferrandez MJ (2016) Trastuzumab, non-pegylated liposomal-encapsulated doxorubicin and paclitaxel in the neoadjuvant setting of HER-2 positive breast cancer. Int J Clin Pharm 38(2):446–453.  https://doi.org/10.1007/s11096-016-0278-5 CrossRefPubMedGoogle Scholar
  96. 96.
    Kang MH et al (2014) Activity of MM-398, nanoliposomal irinotecan (nal-IRI), in Ewing's family tumor xenografts is associated with high exposure of tumor to drug and high SLFN11 expression. Clin Cancer Res 21(5):1139–1150.  https://doi.org/10.1158/1078-0432.CCR-14-1882 CrossRefGoogle Scholar
  97. 97.
    Barretina J, Caponigro G, Stransky N, Venkatesan K, Margolin AA, Kim S, Wilson CJ, Lehár J, Kryukov GV, Sonkin D, Reddy A, Liu M, Murray L, Berger MF, Monahan JE, Morais P, Meltzer J, Korejwa A, Jané-Valbuena J, Mapa FA, Thibault J, Bric-Furlong E, Raman P, Shipway A, Engels IH, Cheng J, Yu GK, Yu J, Aspesi P, de Silva M, Jagtap K, Jones MD, Wang L, Hatton C, Palescandolo E, Gupta S, Mahan S, Sougnez C, Onofrio RC, Liefeld T, MacConaill L, Winckler W, Reich M, Li N, Mesirov JP, Gabriel SB, Getz G, Ardlie K, Chan V, Myer VE, Weber BL, Porter J, Warmuth M, Finan P, Harris JL, Meyerson M, Golub TR, Morrissey MP, Sellers WR, Schlegel R, Garraway LA (2012) The cancer cell line encyclopedia enables predictive modelling of anticancer drug sensitivity. Nature 483:603.  https://doi.org/10.1038/nature11003/. https://www.nature.com/articles/nature11003#supplementary-information CrossRefGoogle Scholar
  98. 98.
    Fan YZ (2013) Development of liposomal formulations: from concept to clinical investigations. Asian J Pharm Sci 8(2):81–87.  https://doi.org/10.1016/j.ajps.2013.07.010 CrossRefGoogle Scholar
  99. 99.
    Noble GT, Stefanick JF, Ashley JD, Kiziltepe T, Bilgicer B (2014) Ligand-targeted liposome design: challenges and fundamental considerations. Trends Biotechnol 32(1):32–45.  https://doi.org/10.1016/j.tibtech.2013.09.007 CrossRefPubMedGoogle Scholar
  100. 100.
    Merino M, Zalba S, Garrido MJ (2018) Immunoliposomes in clinical oncology: State of the art and future perspectives. J Control Release 275:162–176.  https://doi.org/10.1016/j.jconrel.2018.02.015 CrossRefPubMedGoogle Scholar
  101. 101.
    Lyon PC, Gray MD, Mannaris C, Folkes LK, Stratford M, Campo L, Chung DY, Scott S, Anderson M, Goldin R (2018) Safety and feasibility of ultrasound-triggered targeted drug delivery of doxorubicin from thermosensitive liposomes in liver tumours (TARDOX): a single-centre, open-label, phase 1 trial. Lancet Oncol 19(8):1027–1039CrossRefGoogle Scholar
  102. 102.
    Tak WY, Lin S-M, Wang Y, Zheng J, Vecchione A, Park SY, Chen MH, Wong S, Xu R, Peng C-Y (2017) Phase III HEAT study adding lyso-thermosensitive liposomal doxorubicin to radiofrequency ablation in patients with unresectable hepatocellular carcinoma lesions. Clin Cancer Res 19(8):1027–1039Google Scholar
  103. 103.
    Lamichhane N, Udayakumar TS, D’Souza WD, Simone CB, Raghavan SR, Polf J, Mahmood J (2018) Liposomes: clinical applications and potential for image-guided drug delivery. Molecules.  https://doi.org/10.3390/molecules23020288 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Faculty of Medicine, University of PortoPortoPortugal
  2. 2.Department of OncologyCentro Hospitalar de S. JoãoPortoPortugal
  3. 3.i3S- Instituto de Investigação e Inovação em Saúde, Universidade do Porto (Institute for Research and Innovation in Health, University of Porto)PortoPortugal
  4. 4.Institute of Molecular Pathology and Immunology of the University of Porto (IPATIMUP)PortoPortugal
  5. 5.Department of PathologyFaculty of Medicine, University of PortoPortoPortugal

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