64Cu-MM-302 positron emission tomography quantifies variability of enhanced permeability and retention of nanoparticles in relation to treatment response in patients with metastatic breast cancer

Clinical Cancer Research

Volumn 23, Issue 15, 2017, Pages 4190-4202

  Lee, Helen ^a   Shields, Anthony F ^b   Siegel, Barry A ^c   Miller, Kathy D ^d   Krop, Ian ^e   Ma, Cynthia X ^c   Lorusso, Patricia M ^f   Munster, Pamela N ^g   Campbell, Karen ^a   Gaddy, Daniel F ^a   Leonard, Shannon C ^a   Geretti, Elena ^a,h   Blocker, Stephanie J ^b   Kirpotin, Dmitri B ^a   Moyo, Victor ^a,i   Wickham, Thomas J ^a,j   Hendriks, Bart S ^a  

^a MERRIMACK PHARMACEUTICALS   (United States)

^b KARMANOS CANCER INSTITUTE   (United States)

^c Washington University in St Louis School of Medicine   (United States)

^d INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e DANA FARBER CANCER INSTITUTE   (United States)

^f YALE CANCER CENTER   (United States)

^g UNIVERSITY OF CALIFORNIA   (United States)

^h Torque Inc   (United States)

ⁱ LEAF Pharmaceuticals   (United States)

^j Rubius Therapeutics   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

COPPER 64; CYCLOPHOSPHAMIDE; DOXORUBICIN; HER2 TARGETED PEGYLATED LIPOSOMAL DOXORUBICIN CU 64; NANOPARTICLE; TRASTUZUMAB; UNCLASSIFIED DRUG; COPPER; EPIDERMAL GROWTH FACTOR RECEPTOR 2; ERBB2 PROTEIN, HUMAN; MACROGOL DERIVATIVE;

ADULT; AGED; ARTICLE; CLINICAL ARTICLE; DOSIMETRY; DRUG ACCUMULATION; DRUG CLEARANCE; DRUG DELIVERY SYSTEM; DRUG DISTRIBUTION; DRUG HALF LIFE; DRUG PENETRATION; DRUG RETENTION; DRUG STABILITY; DRUG TISSUE LEVEL; DRUG UPTAKE; FEMALE; HUMAN; HUMAN EPIDERMAL GROWTH FACTOR RECEPTOR 2 POSITIVE BREAST CANCER; ISOTOPE LABELING; LIVER; LOADING DRUG DOSE; METASTATIC BREAST CANCER; MULTIPLE CYCLE TREATMENT; PHASE 1 CLINICAL TRIAL; POSITRON EMISSION TOMOGRAPHY-COMPUTED TOMOGRAPHY; PRIORITY JOURNAL; SPLEEN; TREATMENT RESPONSE; ADOLESCENT; ANALOGS AND DERIVATIVES; BLOOD; BONE TUMOR; BRAIN TUMOR; BREAST TUMOR; CELL MEMBRANE PERMEABILITY; CHEMISTRY; CLINICAL TRIAL; DIAGNOSTIC IMAGING; DRUG EFFECT; METASTASIS; MIDDLE AGED; PATHOLOGY; RADIATION RESPONSE; SECONDARY;

ADOLESCENT; ADULT; AGED; BONE NEOPLASMS; BRAIN NEOPLASMS; BREAST NEOPLASMS; CELL MEMBRANE PERMEABILITY; COPPER RADIOISOTOPES; CYCLOPHOSPHAMIDE; DOXORUBICIN; FEMALE; HUMANS; LIVER; MIDDLE AGED; NANOPARTICLES; NEOPLASM METASTASIS; POLYETHYLENE GLYCOLS; POSITRON EMISSION TOMOGRAPHY COMPUTED TOMOGRAPHY; RECEPTOR, ERBB-2; SPLEEN; TRASTUZUMAB;

EID: 85019987693     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-16-3193     Document Type: Article

References (50)

1. Matsumura Y, Maeda H. A new concept for macromolecular therapeutics in cancer chemotherapy: mechanism of tumoritropic accumulation of proteins and the antitumor agent smancs. Cancer Res 1986;46:6387–92.
2. Zheng J, Jaffray D, Allen C. Quantitative CT imaging of the spatial and temporal distribution of liposomes in a rabbit tumor model. Mol Pharm 2009;6:571–80.
3. Prabhakar U, Blakey DC, Maeda H, Jain RK, Sevick-Muraca EM, Zamboni WC, et al. Challenges and key considerations of the enhanced permeability and retention effect (EPR) for nanomedicine drug delivery in oncology. Cancer Res 2013;73:2412–7.
4. Maeda H. Toward a full understanding of the EPR effect in primary and metastatic tumors as well as issues related to its heterogeneity. Adv Drug Deliv Rev 2015;91:3–6.
5. Hansen AE, Petersen AL, Henriksen JR, Boerresen B, Rasmussen P, Elema DR, et al. Positron emission tomography based elucidation of the enhanced permeability and retention effect in dogs with cancer using copper-64 liposomes. ACS Nano 2015;9:6985–95.
6. Greish K. Enhanced permeability and retention of macromolecular drugs in solid tumors: a royal gate for targeted anticancer nanomedicines. J Drug Target 2007;15:457–64.
7. Nehoff H, Parayath NN, Domanovitch L, Taurin S, Greish K. Nanomedicine for drug targeting: strategies beyond the enhanced permeability and retention effect. Int J Nanomedicine 2014;9:2539–55.
8. Drummond DC, Meyer O, Hong K, Kirpotin DB, Papahadjopoulos D. Optimizing liposomes for delivery of chemotherapeutic agents to solid tumors. Pharmacol Rev 1999;51:691–743.
9. Bertrand N, Wu J, Xu X, Kamaly N, Farokhzad OC. Cancer nanotechnology: the impact of passive and active targeting in the era of modern cancer biology. Adv Drug Deliv Rev 2013;66:2–25.
10. Kirpotin DB, Drummond DC, Shao Y, Shalaby MR, Hong K, Nielsen UB, et al. Antibody targeting of long-circulating lipidic nanoparticles does not increase tumor localization but does increase internalization in animal models. Cancer Res 2006;66:6732–40.
11. Reynolds JG, Geretti E, Hendriks BS, Lee H, Leonard SC, Klinz SG, et al. HER2-targeted liposomal doxorubicin displays enhanced anti-tumori-genic effects without associated cardiotoxicity. Toxicol Appl Pharmacol 2012;262:1–10.
12. Espelin CW, Leonard SC, Geretti E, Wickham TJ, Hendriks BS. Dual HER2 targeting with trastuzumab and liposomal-encapsulated doxorubicin (MM-302) demonstrates synergistic antitumor activity in breast and gastric cancer. Cancer Res 2016;76:1517–27.
13. Pirollo KF, Chang EH. Does a targeting ligand influence nanoparticle tumor localization or uptake? Trends Biotechnol 2008;26:552–8.
14. Hong M, Zhu S, Jiang Y, Tang G, Pei Y. Efficient tumor targeting of hydroxycamptothecin loaded PEGylated niosomes modified with trans-ferrin. J Control Release 2009;133:96–102.
15. Duskey JT, Rice KG. Nanoparticle ligand presentation for targeting solid tumors. AAPS PharmSciTech 2014;15:1345–54.
16. Tunggal JK, Cowan DS, Shaikh H, Tannock IF. Penetration of anticancer drugs through solid tissue: a factor that limits the effectiveness of chemotherapy for solid tumors. Clin Cancer Res 1999;5: 1583–6.
17. Hsueh W-A, Kesner AL, Gangloff A, Pegram MD, Beryt M, Czernin J, et al. Predicting chemotherapy response to paclitaxel with 18F-Fluoropaclitaxel and PET. J Nucl Med 2006;47:1995–9.
18. Kesner AL, Hsueh W-A, Htet NL, Pio BS, Czernin J, Pegram MD, et al. Biodistribution and predictive value of 18F-fluorocyclophosphamide in mice bearing human breast cancer xenografts. J Nucl Med 2007;48: 2021–7.
19. Schmidt MM, Wittrup KD. A modeling analysis of the effects of molecular size and binding affinity on tumor targeting. Mol Cancer Ther 2009;8: 2861–71.
20. Hendriks BS, Reynolds JG, Klinz SG, Geretti E, Lee H, Leonard SC, et al. Multiscale kinetic modeling of liposomal Doxorubicin delivery quantifies the role of tumor and drug-specific parameters in local delivery to tumors. CPT Pharmacometrics Syst Pharmacol 2012;1:e15.
21. Karathanasis E, Suryanarayanan S, Balusu SR, McNeeley K, Sechopoulos I, Karellas A, et al. Imaging nanoprobe for prediction of outcome of nanoparticle chemotherapy by using mammography. Radiology 2009;250: 398–406.
22. Perez-Medina C, Abdel-Atti D, Tang J, Zhao Y, Fayad ZA, Lewis JS, et al. Nanoreporter PET predicts the efficacy of anti-cancer nanotherapy. Nat Commun 2016;7:11838.
23. Miller MA, Gadde S, Pfirschke C, Engblom C, Sprachman MM, Kohler RH, et al. Predicting therapeutic nanomedicine efficacy using a companion magnetic resonance imaging nanoparticle. Sci Transl Med 2015;7:1–13.
24. Geretti E, Leonard SC, Dumont N, Lee H, Zheng J, De Souza R, et al. Cyclophosphamide-mediated tumor priming for enhanced delivery and antitumor activity of HER2-targeted liposomal doxorubicin (MM-302). Mol Cancer Ther 2015;14:2060–71.
25. Lee H, Zheng J, Gaddy D, Orcutt KD, Leonard S, Geretti E, et al. A gradient-loadable 64Cu-chelator for quantifying tumor deposition kinetics of nano-liposomal therapeutics by positron emission tomography. Nanomedicine 2014;11:155–65.
26. Lorusso P, Krop IE, Miller K, Ma C, Siegel BA, Shields AF, et al. A phase 1 study of MM-302, a HER2-targeted PEGylated liposomal doxorubicin, in patients with HER2-positive metastatic breast cancer (MBC). 2015. Available from: http://www.merrimack.com/sites/default/files/posters/MM-302%20-%20AACR%20presentation%20-%20FINAL% 20-%2020APR2015.pdf.
27. Munster P, Miller K, Krop IE, Dhindsa N, Niyikiza C, Odueyungbo A, etal. A phase 1 study of MM-302, a HER2-targeted liposomal doxorubicin, in patients with advanced HER2-positive (HER2+) breast cancer. 2012. Available from: http://www.merrimack.com/sites/default/files/posters/MM-302%20Phase%201%20SABCS%202012%20FINAL.pdf.
28. McAuliffe MJ, Lalonde FM, McGarry D, Gandler W, Csaky K, Trus BL. Medical Image Processing, Analysis and Visualization in clinical research. In: Proceedings of the 14th IEEE Symposium on Computer-Based Medical Systems; 2001 Jul 26–27; Bethesda, MD. New York, NY: IEEE; 2001. p 381–6.
29. Foster DM. Developing and testing integrated multicompartment models to describe a single-input multiple-output study using the SAAM II software system. Adv Exp Med Biol 1998;445:59–78.
30. Stabin MG, Siegel JA. Physical models and dose factors for use in internal dose assessment. Health Phys 2003;85:294–310.
31. Stabin MG, Sparks RB, Crowe E. OLINDA/EXM: the second-generation personal computer software for internal dose assessment in nuclear medicine. J Nucl Med 2005;46:1023–7.
32. Gaddy DF, Lee H, Zheng J, Jaffray DA, Wickham TJ, Hendriks BS. Whole-body organ-level and kidney micro-dosimetric evaluations of 64Cu-loaded HER2/ErbB2-targeted liposomal doxorubicin 64Cu-MM-302 in rodents and primates. EJNMMI Res 2015;5:24.
33. Baxter LT, Zhu H, Mackensen DG, Butler WF, Jain RK. Biodistribution of monoclonal antibodies: scale-up from mouse to human using a physiologically based pharmacokinetic model. Cancer Res 1995;55: 4611–22.
34. Gabizon AA, Tzemach D, Mak L, Bronstein M, Horowitz AT. Dose dependency of pharmacokinetics and therapeutic efficacy of pegylated liposomal doxorubicin (DOXIL) in murine models. J Drug Target 2002;10:539–48.
35. Jokerst JV, Lobovkina T, Zare RN, Gambhir SS. Nanoparticle PEGylation for imaging and therapy. Nanomedicine (Lond) 2011;6:715–28.
36. Delille J-P, Slanetz PJ, Yeh ED, Kopans DB, Garrido L. Breast cancer: regional blood flow and blood volume measured with magnetic susceptibility-based MR imaging–initial results. Radiology 2002;223:558–65.
37. Jain RK. Determinants of tumor blood flow: a review. Cancer Res 1988; 48:2641–58.
38. Brix G, Bahner ML, Hoffmann U, Horvath A, Schreiber W. Regional blood flow, capillary permeability, and compartmental volumes: measurement with dynamic CT–initial experience. Radiology 1999;210:269–76.
39. Maeda H. Macromolecular therapeutics in cancer treatment: the EPR effect and beyond. J Control Release 2012;164:138–44.
40. Koukourakis MI, Koukouraki S, Giatromanolaki A, Kakolyris S, Georgou-lias V, Velidaki A, et al. High intratumoral accumulation of stealth liposomal doxorubicin in sarcomas–rationale for combination with radiotherapy. Acta Oncol 2000;39:207–11.
41. Koukourakis MI, Koukouraki S, Fezoulidis I, Kelekis N, Kyrias G, Archi-mandritis S, et al. High intratumoural accumulation of stealth liposomal doxorubicin (Caelyx) in glioblastomas and in metastatic brain tumours. Br J Cancer 2000;83:1281–6.
42. Arrieta O, Medina LA, Estrada-Lobato E, Hernandez-Pedro N, Villanueva-Rodríguez G, Martínez-Barrera L, et al. First-line chemotherapy with liposomal doxorubicin plus cisplatin for patients with advanced malignant pleural mesothelioma: phase II trial. Br J Cancer 2012;106:1027–32.
43. Arrieta O, Medina L-A, Estrada-Lobato E, Ramírez-Tirado L-A, Mendoza-García V-O, de la Garza-Salazar J. High liposomal doxorubicin tumour tissue distribution, as determined by radiopharmaceutical labelling with (99m)Tc-LD, is associated with the response and survival of patients with unresectable pleural mesothelioma treated with a combination of liposomal. Cancer Chemother Pharmacol 2014;74:211–5.
44. Bae YH, Park K. Targeted drug delivery to tumors: myths, reality and possibility. J Control Release 2011;153:198–205.
45. Nichols JW, Bae YH. Odyssey of a cancer nanoparticle: from injection site to site of action. Nano Today 2012;7:606–18.
46. Tamura K, Kurihara H, Yonemori K, Tsuda H, Suzuki J, Kono Y, et al.,64Cu-DOTA-trastuzumab PET imaging in patients with HER2-positive breast cancer. J Nucl Med 2013;54:1869–75.
47. Dijkers EC, Oude Munnink TH, Kosterink JG, Brouwers AH, Jager PL, de Jong JR, et al. Biodistribution of 89Zr-trastuzumab and PET imaging of HER2-positive lesions in patients with metastatic breast cancer. Clin Pharmacol Ther 2010;87:586–92.
48. Siegal T, Horowitz A, Gabizon AA. Doxorubicin encapsulated in sterically stabilized liposomes for the treatment of a brain tumor model: biodistribution and therapeutic efficacy. J Neurosurg 1995;83:1029–37.
49. Lockman PR, Mittapalli RK, Taskar KS, Rudraraju V, Gril B, Bohn KA, et al. Heterogeneous blood-tumor barrier permeability determines drug efficacy in experimental brain metastases of breast cancer. Clin Cancer Res 2010;16:5664–78.
50. Sharma US, Sharma A, Chau RI, Straubinger RM. Liposome-mediated therapy of intracranial brain tumors in a rat model. Pharm Res 1997; 14:992–8.