ICAM-1-targeted, Lcn2 siRNA-encapsulating liposomes are potent anti-angiogenic agents for triple negative breast cancer

Theranostics

Volumn 6, Issue 1, 2016, Pages 1-13

  Guo, Peng ^a,b   Yang, Jiang ^b   Jia, Di ^b   Moses, Marsha A ^b   Auguste, Debra T ^a,b  

^a City University of New York   (United States)

^b BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

Angiogenesis; ICAM 1; Lipocalin 2; Liposomal siRNA; Triple negative breast cancer

Indexed keywords

ANGIOGENESIS INHIBITOR; IMMUNOLIPOSOME; INTERCELLULAR ADHESION MOLECULE 1; NEUTROPHIL GELATINASE ASSOCIATED LIPOCALIN; SMALL INTERFERING RNA; VASCULOTROPIN; ACUTE PHASE PROTEIN; LCN2 PROTEIN, HUMAN; LIPOCALIN; LIPOSOME; ONCOPROTEIN; VASCULOTROPIN A; VEGFA PROTEIN, HUMAN;

ANGIOGENESIS; ARTICLE; CANCER CELL LINE; CANCER INHIBITION; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; DRUG DELIVERY SYSTEM; DRUG EFFICACY; DRUG FORMULATION; DRUG POTENCY; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; HYDRODYNAMICS; IN VITRO STUDY; IN VIVO STUDY; MCF 10A CELL LINE; MDA MB 231 CELL LINE; NANOENCAPSULATION; NEOVASCULARIZATION (PATHOLOGY); PHOTON CORRELATION SPECTROSCOPY; PROTEIN TARGETING; TRIPLE NEGATIVE BREAST CANCER; ZETA POTENTIAL; ANTAGONISTS AND INHIBITORS; CELL MOTION; DRUG EFFECTS; METABOLISM; MOLECULARLY TARGETED THERAPY; MURINE LEUKEMIA VIRUS; PHYSIOLOGY; PROCEDURES; SECRETION (PROCESS); TRIPLE NEGATIVE BREAST NEOPLASMS; TUMOR CELL LINE;

ACUTE-PHASE PROTEINS; ANGIOGENESIS INHIBITORS; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; ENDOTHELIAL CELLS; HUMANS; INTERCELLULAR ADHESION MOLECULE-1; LEUKEMIA VIRUS, MURINE; LIPOCALIN-2; LIPOCALINS; LIPOSOMES; MOLECULAR TARGETED THERAPY; PROTO-ONCOGENE PROTEINS; RNA, SMALL INTERFERING; TRIPLE NEGATIVE BREAST NEOPLASMS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84954315100     PISSN: None     EISSN: 18387640     Source Type: Journal    
DOI: 10.7150/thno.12167     Document Type: Article

References (58)

1. Kim DH, Rossi JJ. Strategies for silencing human disease using RNA interference. Nat Rev Genet. 2007;8:173-84.
2. Devi GR. siRNA-based approaches in cancer therapy. Cancer Gene Ther. 2006;13:819-29.
3. Oh Y-K, Park TG. siRNA delivery systems for cancer treatment. Adv Drug Deliv Rev. 2009;61:850-62.
4. Morrissey DV, Lockridge JA, Shaw L, Blanchard K, Jensen K, Breen W, et al. Potent and persistent in vivo anti-HBV activity of chemically modified siRNAs. Nat Biotechnol. 2005;23:1002-7.
5. Liu X, Madhankumar AB, Slagle-Webb B, Sheehan JM, Surguladze N, Connor JR. Heavy chain ferritin siRNA delivered by cationic liposomes increases sensitivity of cancer cells to chemotherapeutic agents. Cancer Res. 2011;71:2240-9.
6. Yonenaga N, Kenjo E, Asai T, Tsuruta A, Shimizu K, Dewa T, et al. RGD-based active targeting of novel polycation liposomes bearing siRNA for cancer treatment. J Controlled Release. 2012;160:177-81.
7. Meng H, Mai WX, Zhang H, Xue M, Xia T, Lin S, et al. Codelivery of an optimal drug/siRNA combination using mesoporous silica nanoparticles to overcome drug resistance in breast cancer in vitro and in vivo. ACS Nano. 2013;7:994-1005.
8. Dahlman JE, Barnes C, Khan OF, Thiriot A, Jhunjunwala S, Shaw TE, et al. In vivo endothelial siRNA delivery using polymeric nanoparticles with low molecular weight. Nat Nanotechnol. 2014;9:648-55.
9. Foulkes WD, Smith IE, Reis-Filho JS. Triple-Negative Breast Cancer. N Engl J Med. 2010;363:1938-48.
10. Ovcaricek T, Frkovic S, Matos E, Mozina B, Borstnar S. Triple negative breast cancer-prognostic factors and survival. Radiol Oncol. 2011;45.
11. Slamon D, Eiermann W, Robert N, Pienkowski T, Martin M, Press M, et al. Adjuvant trastuzumab in HER2-positive breast cancer. N Engl J Med. 2011;365:1273-83.
12. Yu K-D, Wu J, Shen Z-Z, Shao Z-M. Hazard of breast cancer-specific mortality among women with estrogen receptor-positive breast cancer after five years from diagnosis: implication for extended endocrine therapy. J Clin Endocrinol Metab. 2012;97:E2201-9.
13. Guo P, Huang J, Wang L, Jia D, Yang J, Dillon DA, et al. ICAM-1 as a molecular target for triple negative breast cancer. Proc Natl Acad Sci. 2014;111:14710-5.
14. Folkman J. Tumor angiogenesis: therapeutic implications. N Engl J Med. 1971;285:1182-6.
15. Harper J, Moses MA. Molecular regulation of tumor angiogenesis: mechanisms and therapeutic implications. EXS. 2006;223-68.
16. Roy R, Zhang B, Moses MA. Making the cut: protease-mediated regulation of angiogenesis. Exp Cell Res. 2006;312:608-22.
17. Fernández CA, Yan L, Louis G, Yang J, Kutok JL, Moses MA. The matrix metalloproteinase-9/neutrophil gelatinase-associated lipocalin complex plays a role in breast tumor growth and is present in the urine of breast cancer patients. Clin Cancer Res 2005;11:5390-5.
18. Yang J, McNeish B, Butterfield C, Moses MA. Lipocalin 2 is a novel regulator of angiogenesis in human breast cancer. FASEB J. 2013;27:45-50.
19. Yang J, Moses MA. Lipocalin 2: a multifaceted modulator of human cancer. Cell Cycle Georget Tex. 2009;8:2347-52.
20. Yang J, Bielenberg DR, Rodig SJ, Doiron R, Clifton MC, Kung AL, et al. Lipocalin 2 promotes breast cancer progression. Proc Natl Acad Sci. 2009;106:3913-8.
21. Guo P, You J-O, Yang J, Jia D, Moses MA, Auguste DT. Inhibiting metastatic breast cancer cell migration via the synergy of targeted, pH-triggered siRNA delivery and chemokine axis blockade. Mol Pharm. 2014;11:755-65.
22. Guo P, You J-O, Yang J, Moses MA, Auguste DT. Using breast cancer cell CXCR4 surface expression to predict liposome binding and cytotoxicity. Biomaterials. 2012;33:8104-10.
23. Fernandez CA. Structural and Functional Uncoupling of the enzymatic and angiogenic inhibitory activities of tissue inhibitor of metalloproteinase-2 (TIMP-2): Loop is a novel angiogenesis inhibitor. J Biol Chem. 2003;278:40989-95.
24. Foradori MJ, Chen Q, Fernandez CA, Harper J, Li X, Tsang PCW, et al. Matrilin-1 is an inhibitor of neovascularization. J Biol Chem. 2014;289:14301-9.
25. Roy R, Rodig S, Bielenberg D, Zurakowski D, Moses MA. ADAM12 transmembrane and secreted isoforms promote breast tumor growth: a distinct role for ADAM12-S protein in tumor metastasis. J Biol Chem. 2011;286:20758-68.
26. Akino T, Han X, Nakayama H, McNeish B, Zurakowski D, Mammoto A, et al. Netrin-1 promotes medulloblastoma cell invasiveness and angiogenesis, and demonstrates elevated expression in tumor tissue and urine of patients with pediatric medulloblastoma. Cancer Res. 2014;74:3716-26.
27. Moses MA, Sudhalter J, Langer R. Identification of an inhibitor of neovascularization from cartilage. Science. 1990;248:1408-10.
28. Moses MA, Wiederschain D, Wu I, Fernandez CA, Ghazizadeh V, Lane WS, et al. Troponin I is present in human cartilage and inhibits angiogenesis. Proc Natl Acad Sci. 1999;96:2645-50.
29. Ponce ML, Kleinmann HK. The Chick Chorioallantoic Membrane as an In Vivo Angiogenesis Model. In: Bonifacino JS, Dasso M, Harford JB, Lippincott-Schwartz J, Yamada KM, editors. Curr Protoc Cell Biol. Hoboken, NJ, USA: John Wiley & Sons, Inc.; 2003.
30. You J-O, Almeda D, Ye GJ, Auguste DT. Bioresponsive matrices in drug delivery. J Biol Eng. 2010;4:15.
31. Hillaireau H, Couvreur P. Nanocarriers' entry into the cell: relevance to drug delivery. Cell Mol Life Sci. 2009;66:2873-96.
32. Photos PJ, Bacakova L, Discher B, Bates FS, Discher DE. Polymer vesicles in vivo: correlations with PEG molecular weight. J Control Release Off J Control Release Soc. 2003;90:323-34.
33. Harris JM, Chess RB. Effect of pegylation on pharmaceuticals. Nat Rev Drug Discov. 2003;2:214-21.
34. Liu D, Mori A, Huang L. Role of liposome size and RES blockade in controlling biodistribution and tumor uptake of GM1-containing liposomes. Biochim Biophys Acta. 1992;1104:95-101.
35. Nagayasu A, Uchiyama K, Kiwada H. The size of liposomes: a factor which affects their targeting efficiency to tumors and therapeutic activity of liposomal antitumor drugs. Adv Drug Deliv Rev. 1999;40:75-87.
36. Uhlen M, Oksvold P, Fagerberg L, Lundberg E, Jonasson K, Forsberg M, et al. Towards a knowledge-based Human Protein Atlas. Nat Biotechnol. 2010;28:1248-50.
37. Gao J, Liu W, Xia Y, Li W, Sun J, Chen H, et al. The promotion of siRNA delivery to breast cancer overexpressing epidermal growth factor receptor through anti-EGFR antibody conjugation by immunoliposomes. Biomaterials. 2011;32:3459-70.
38. Leung D, Cachianes G, Kuang W, Goeddel D, Ferrara N. Vascular endothelial growth factor is a secreted angiogenic mitogen. Science. 1989;246:1306-9.
39. Carneiro A, Falcão M, Azevedo I, Falcão Reis F, Soares R. Multiple effects of bevacizumab in angiogenesis: implications for its use in age-related macular degeneration. Acta Ophthalmol (Copenh). 2009;87:517-23.
40. Sharma RK, Balaiya S, Chalam KV. Bevacizumab suppression of establishment of micrometastases in experimental ocular melanoma. Invest Ophthalmol Vis Sci. 2010;51:6906-6906.
41. Han YS, Lee JE, Jung JW, Lee JS. Inhibitory effects of bevacizumab on angiogenesis and corneal neovascularization. Graefes Arch Clin Exp Ophthalmol. 2009;247:541-8.
42. Moses MA, Harper J, Fernández CA. A role for antiangiogenic therapy in breast cancer. Curr Oncol Rep. 2004;6:42-8.
43. Schiffelers RM. Cancer siRNA therapy by tumor selective delivery with ligand-targeted sterically stabilized nanoparticle. Nucleic Acids Res. 2004;32:e149-e149.
44. Wickham T, Futch K. Abstract P5-18-09: A Phase I Study of MM-302, a HER2-targeted Liposomal Doxorubicin, in Patients with Advanced, HER2-Positive Breast Cancer. Cancer Res. 2012;72:P5-18-09.
45. Geretti E, Reynolds J, Hendriks B, Eckelhofer I, Espelin C, Gaddy D, et al. Abstract C90: HER2-targeted liposomal doxorubicin MM-302 has a favorable cardiosafety profile in preclinical models. Mol Cancer Ther. 2011;10:C90-C90.
46. Hendriks B, Shields A, Siegel BA, Miller K, Munster P, Ma C, et al. 55P * PET/CT imaging of 64Cu-labelled HER2 liposomal doxorubicin (64Cu-MM-302) quantifies variability of liposomal drug delivery to diverse tumor lesions in HER2-positive breast cancer patients. Ann Oncol. 2014;25:i19-i19.
47. O'Brien MER. Reduced cardiotoxicity and comparable efficacy in a phase III trial of pegylated liposomal doxorubicin HCl (CAELYXTM/Doxil") versus conventional doxorubicin for first-line treatment of metastatic breast cancer. Ann Oncol. 2004;15:440-9.
48. Liu Y, Zhu Y-H, Mao C-Q, Dou S, Shen S, Tan Z-B, et al. Triple negative breast cancer therapy with CDK1 siRNA delivered by cationic lipid assisted PEG-PLA nanoparticles. J Controlled Release. 2014;192:114-21.
49. Deng ZJ, Morton SW, Ben-Akiva E, Dreaden EC, Shopsowitz KE, Hammond PT. Layer-by-layer nanoparticles for systemic codelivery of an anticancer drug and siRNA for potential triple-negative breast cancer treatment. ACS Nano. 2013;7:9571-84.
50. Kim J-H, Kim Y-S, Park K, Kang E, Lee S, Nam HY, et al. Self-assembled glycol chitosan nanoparticles for the sustained and prolonged delivery of antiangiogenic small peptide drugs in cancer therapy. Biomaterials. 2008;29:1920-30.
51. Raskopf E, Vogt A, Sauerbruch T, Schmitz V. siRNA targeting VEGF inhibits hepatocellular carcinoma growth and tumor angiogenesis in vivo. J Hepatol. 2008;49:977-84.
52. Di Paolo D, Pastorino F, Zuccari G, Caffa I, Loi M, Marimpietri D, et al. Enhanced anti-tumor and anti-angiogenic efficacy of a novel liposomal fenretinide on human neuroblastoma. J Controlled Release. 2013;170:445-51.
53. Kümler I, Christiansen OG, Nielsen DL. A systematic review of bevacizumab efficacy in breast cancer. Cancer Treat Rev. 2014;40:960-73.
54. Mackey JR, Kerbel RS, Gelmon KA, McLeod DM, Chia SK, Rayson D, et al. Controlling angiogenesis in breast cancer: a systematic review of anti-angiogenic trials. Cancer Treat Rev. 2012;38:673-88.
55. Mikhaylov G, Mikac U, Magaeva AA, Itin VI, Naiden EP, Psakhye I, et al. Ferri-liposomes as an MRI-visible drug-delivery system for targeting tumours and their microenvironment. Nat Nanotechnol. 2011;6:594-602.
56. Petersen AL, Binderup T, Rasmussen P, Henriksen JR, Elema DR, Kjær A, et al. 64Cu loaded liposomes as positron emission tomography imaging agents. Biomaterials. 2011;32:2334-41.
57. Mura S, Nicolas J, Couvreur P. Stimuli-responsive nanocarriers for drug delivery. Nat Mater. 2013;12:991-1003.
58. Ganta S, Devalapally H, Shahiwala A, Amiji M. A review of stimuli-responsive nanocarriers for drug and gene delivery. J Controlled Release. 2008;126:187-204.