Impact of tumor HER2/ERBB2 expression level on HER2-targeted liposomal doxorubicin-mediated drug delivery: Multiple low-affinity interactions lead to a threshold effect

Molecular Cancer Therapeutics

Volumn 12, Issue 9, 2013, Pages 1816-1828

  Hendriks, Bart S ^a   Klinz, Stephan G ^a   Reynolds, Joseph G ^a   Espelin, Christopher W ^a   Gaddy, Daniel F ^a   Wickham, T J ^a  

^a MERRIMACK PHARMACEUTICALS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DOXORUBICIN; EPIDERMAL GROWTH FACTOR RECEPTOR 2; NANOPARTICLE;

ARTICLE; CELL KINETICS; DRUG DELIVERY SYSTEM; DRUG RECEPTOR BINDING; FLOW CYTOMETRY; HEART MUSCLE CELL; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; ANTIBIOTICS, ANTINEOPLASTIC; CELL LINE, TUMOR; DOXORUBICIN; DRUG DELIVERY SYSTEMS; HUMANS; LIPOSOMES; MICE; MOLECULAR TARGETED THERAPY; NEOPLASMS; RECEPTOR, ERBB-2;

EID: 84884522580     PISSN: 15357163     EISSN: 15388514     Source Type: Journal    
DOI: 10.1158/1535-7163.MCT-13-0180     Document Type: Article

References (49)

1. Paszko E, Senge MO. Immunoliposomes. Curr Med Chem 2012;19: 5239-77.
2. Mamot C, Ritschard R, Wicki A, Stehle G, Dieterle T, Bubendorf L, et al. Tolerability, safety, pharmacokinetics, and efficacy of doxorubicin- loaded anti-EGFR immunoliposomes in advanced solid tumours: a phase 1 dose-escalation study. Lancet Oncol 2012;13: 1234-41.
3. Mamot C, Drummond DC, Greiser U, Hong K, Kirpotin DB, Marks JD, et al. Epidermal growth factor receptor (EGFR)-targeted immunoliposomes mediate specific and efficient drug delivery to EGFRand EGFRvIII-overexpressing tumor cells. Cancer Res 2003;63: 3154-61.
4. Lee RJ, Low PS. Delivery of liposomes into cultured KB cells via folate receptor-mediated endocytosis. J Biol Chem 1994;269:3198-204.
5. Zhai G, Wu J, Yu B, Guo C, Yang X, Lee RJ. A transferrin receptortargeted liposomal formulation for docetaxel. J Nanosci Nanotechnol 2010;10:5129-36.
6. Dunne M, Zheng J, Rosenblat J, Jaffray DA, Allen C. APN/CD13- targeting as a strategy to alter the tumor accumulation of liposomes. J Control Release 2011;154:298-305.
7. Pastorino F, Di Paolo D, Piccardi F, Nico B, Ribatti D, Daga A, et al. Enhanced antitumor efficacy of clinical-grade vasculature-targeted liposomal doxorubicin. Clin Cancer Res 2008;14:7320-9.
8. Brignole C, Marimpietri D, Di Paolo D, Perri P, Morandi F, Pastorino F, et al. Therapeutic targeting of TLR9 inhibits cell growth and induces apoptosis in neuroblastoma. Cancer Res 2010;70:9816-26.
9. Wang L, Su W, Liu Z, Zhou M, Chen S, Chen Y, et al. CD44 antibodytargeted liposomal nanoparticles for molecular imaging and therapy of hepatocellular carcinoma. Biomaterials 2012;33:5107-14.
10. Mitchell MJ, Chen CS, Ponmudi V, Hughes AD, King MR. E-selectin liposomal and nanotube-targeted delivery of doxorubicin to circulating tumor cells. J Control Release 2012;160:609-17.
11. Shroff K, Kokkoli E. PEGylated liposomal doxorubicin targeted to alpha5beta1-expressing MDA-MB-231 breast cancer cells. Langmuir 2012;28:4729-36.
12. Petersen AL, Binderup T, Jolck RI, Rasmussen P, Henriksen JR, Pfeifer AK, et al. Positron emission tomography evaluation of somatostatin receptor targeted 64Cu-TATE-liposomes in a human neuroendocrine carcinoma mouse model. J Control Release 2012;160:254-63.
13. Slamon DJ, Clark GM, Wong SG, Levin WJ, Ullrich A, McGuire WL. Human breast cancer: correlation of relapse and survival with amplification of the HER-2/neu oncogene. Science 1987;235:177-82.
14. Scholl S, Beuzeboc P, Pouillart P. TargetingHER2in other tumor types. Ann Oncol 2001;12(Suppl 1):S81-7.
15. Ross JS, Fletcher JA, Linette GP, Stec J, Clark E, Ayers M, et al. The Her-2/neu gene and protein in breast cancer 2003: biomarker and target of therapy. Oncologist 2003;8:307-25.
16. Koltz BR, Hicks DG, Whitney-Miller CL. HER2 testing in gastric and esophageal adenocarcinoma: new diagnostic challenges arising from new therapeutic options. Biotech Histochem 2012;87:40-5.
17. HercepTest Interpretation Manual - Breast. (Dako, Carpinteria, CA) Literature Order No. 29036. Available from: http://www.dako.com/us/29036- herceptest-interpretation-manual-breast-ihc-us.pdf.
18. Rossi V, Sarotto I, Maggiorotto F, Berchialla P, Kubatzki F, Tomasi N, et al. Moderate immunohistochemical expression of HER-2 (2+) without HER-2 gene amplification is a negative prognostic factor in early breast cancer. Oncologist 2012;17:1418-25.
19. NSABP Protocol B-47. A Randomized Phase III Trial of Adjuvant Therapy Comparing Chemotherapy Alone (Six Cycles of Docetaxel Plus Cyclophosphamide or Four Cycles of Doxorubicin Plus Cyclophosphamide Followed by Weekly Paclitaxel) to Chemotherapy Plus Trastuzumab in Women with Node-Positive or High-Risk Node-Negative HER2-Low Invasive Breast Cancer. Available from: http://www.nsabp.pitt.edu/B-47.asp.
20. Kunz PL, Mojtahed A, Fisher GA, Ford JM, Chang DT, Balise RR, et al. HER2 expression in gastric and gastroesophageal junction adenocarcinoma in a US population: clinicopathologic analysis with proposed approach to HER2 assessment. Appl Immunohistochem Mol Morphol 2012;20:13-24.
21. Munster P, Miller K, Krop IE, Dhindsa N, Niyikiza C, Nielsen U, et al. A phase 1 study of MM-302, a HER2-targeted liposomal doxorubicin, in patients with advanced HER2-positive (HER2+) breast cancer. In: Proceedings of the Thirty-Fifth Annual CTRC-AACR San Antonio Breast Cancer Symposium; 2012 Dec 4-8; San Antonio, TX. Philadelphia (PA): AACR. Cancer Res 2012;72(24 Suppl):Abstract nr P5-18-09.
22. Reynolds JG, Geretti E, Hendriks BS, Lee H, Leonard SC, Klinz SG, et al. HER2-targeted liposomal doxorubicin displays enhanced antitumorigenic effects without associated cardiotoxicity. Toxicol Appl Pharmacol 2012;262:1-10.
23. Neve RM, Nielsen UB, Kirpotin DB, Poul MA, Marks JD, Benz CC. Biological effects of anti-ErbB2 single chain antibodies selected for internalizing function. Biochem Biophys Res Commun 2001;280: 274-9.
24. Pommier Y, Leo E, Zhang H, Marchand C. DNA topoisomerases and their poisoning by anticancer and antibacterial drugs. Chem Biol 2010; 17:421-33.
25. Peer D, Karp JM, Hong S, Farokhzad OC, Margalit R, Langer R. Nanocarriers as an emerging platform for cancer therapy. Nat Nanotechnol 2007;2:751-60.
26. 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.
27. 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.
28. Nielsen UB, Kirpotin DB, Pickering EM, Hong K, Park JW, Refaat Shalaby M, et al. Therapeutic efficacy of anti-ErbB2 immunoliposomes targeted by a phage antibody selected for cellular endocytosis. Biochim Biophys Acta 2002;1591:109-18.
29. Park JW, Hong K, Kirpotin DB, Colbern G, Shalaby R, Baselga J, et al. Anti-HER2 immunoliposomes: enhanced efficacy attributable to targeted delivery. Clin Cancer Res 2002;8:1172-81.
30. Nellis DF, Giardina SL, Janini GM, Shenoy SR, Marks JD, Tsai R, et al. Preclinical manufacture of anti-HER2 liposome-inserting, scFv-PEGlipid conjugate. 2. Conjugate micelle identity, purity, stability, and potency analysis. Biotechnol Prog 2005;21:221-32.
31. Nellis DF, Ekstrom DL, Kirpotin DB, Zhu J, Andersson R, Broadt TL, et al. Preclinical manufacture of an anti-HER2 scFv-PEG-DSPE, liposome- inserting conjugate. 1. Gram-scale production and purification. Biotechnol Prog 2005;21:205-20.
32. Millard BL, Niepel M, Menden MP, Muhlich JL, Sorger PK. Adaptive informatics for multifactorial and high-content biological data. Nat Methods 2011;8:487-93.
33. Hendriks BS, Opresko LK, Wiley HS, Lauffenburger D. Coregulation of epidermal growth factor receptor/human epidermal growth factor receptor 2 (HER2) levels and locations: quantitative analysis of HER2 overexpression effects. Cancer Res 2003;63:1130-7.
34. Eytan GD, Kuchel PW. Mechanism of action of P-glycoprotein in relation to passive membrane permeation. Int Rev Cytol 1999;190: 175-250.
35. Hendriks BS, Reynolds JG, Klinz SG, Geretti E, Lee H, Leonard SC, et al. Multi-scale kinetic modeling of liposomal doxorubicin delivery quantifies the role of tumor and drug-specific parameters in local delivery to tumors. Clin Pharmacol: Pharmacometrics & Sys Pharmacol 2012;1:e15.
36. Wickham TJ, Granados RR, Wood HA, Hammer DA, Shuler ML. General analysis of receptor-mediated viral attachment to cell surfaces. Biophys J 1990;58:1501-16.
37. Austin CD, De Maziere AM, Pisacane PI, van Dijk SM, Eigenbrot C, Sliwkowski MX, et al. Endocytosis and sorting of ErbB2 and the site of action of cancer therapeutics trastuzumab and geldanamycin. Mol Biol Cell 2004;15:5268-82.
38. Alcantara CS, Yang CH, Steiner TS, Barrett LJ, Lima AA, Chappell CL, et al. Interleukin-8, tumor necrosis factor-alpha, and lactoferrin in immunocompetent hosts with experimental and Brazilian children with acquired cryptosporidiosis. Am J Trop Med Hyg 2003;68: 325-8.
39. Kinoshita A, Kobayashi D, Hibino Y, Isago T, Uchino K, Yagi K, et al. Regulation of CMV promoter-driven exogenous gene expression with doxorubicin in genetically modified cells. J Pharm Pharmacol 2008;60: 1659-65.
40. Kim KI, Kang JH, Chung JK, Lee YJ, Jeong JM, Lee DS, et al. Doxorubicin enhances the expression of transgene under control of the CMV promoter in anaplastic thyroid carcinoma cells. J Nucl Med 2007;48:1553-61.
41. Nagy P, Friedlander E, Tanner M, Kapanen AI, Carraway KL, Isola J, et al. Decreased accessibility and lack of activation of ErbB2 in JIMT-1, a herceptin-resistant, MUC4-expressing breast cancer cell line. Cancer Res 2005;65:473-82.
42. Li Y, Zhang Q, Tian R, Wang Q, Zhao JJ, Iglehart JD, et al. Lysosomal transmembrane protein LAPTM4B promotes autophagy and tolerance to metabolic stress in cancer cells. Cancer Res 2011; 71:7481-9.
43. Kirpotin D, Park JW, Hong K, Zalipsky S, Li WL, Carter P, et al. Sterically stabilized anti-HER2 immunoliposomes: design and targeting to human breast cancer cells in vitro. Biochemistry 1997;36: 66-75.
44. Park JW, Hong K, Carter P, Asgari H, Guo LY, Keller GA, et al. Development of anti-p185HER2 immunoliposomes for cancer therapy. Proc Natl Acad Sci U S A 1995;92:1327-31.
45. Hertel PB, Tu D, Ejlertsen B, Jensen MB, Balslev E, Jiang S, et al. TIMP- 1 in combination with HER2 and TOP2A for prediction of benefit from adjuvant anthracyclines in high-risk breast cancer patients. Breast Cancer Res Treat 2012;132:225-34.
46. Ejlertsen B, Jensen MB, Nielsen KV, Balslev E, Rasmussen BB, Willemoe GL, et al. HER2, TOP2A, and TIMP-1 and responsiveness to adjuvant anthracycline-containing chemotherapy in high-risk breast cancer patients. J Clin Oncol 2010;28:984-90.
47. Bezler M, Hengstler JG, Ullrich A. Inhibition of doxorubicin-induced HER3-PI3K-AKT signalling enhances apoptosis of ovarian cancer cells. Mol Oncol 2012;6:516-29.
48. Li Y, Zou L, Li Q, Haibe-Kains B, Tian R, Desmedt C, et al. Amplification of LAPTM4B andYWHAZcontributes to chemotherapy resistance and recurrence of breast cancer. Nat Med 2010;16:214-8.
49. Onsum M, Geretti E, Paragas V, Kudla A, Moulis S, Luus L, et al. Single cell quantitative HER2 measurement in patient samples identifies heterogeneity and distinct sub-groups within traditionally-defined HER2-positive patients. Am J Pathol. In press, 2013.