Targeted nanoparticles for image-guided treatment of triple-negative breast cancer: Clinical significance and technological advances

Wiley Interdisciplinary Reviews: Nanomedicine and Nanobiotechnology

Volumn 7, Issue 6, 2015, Pages 797-816

  Miller Kleinhenz, Jasmine M ^a   Bozeman, Erica N ^a   Yang, Lily ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CULTURE; CELL MEMBRANES; CELL PROLIFERATION; CONTROLLED DRUG DELIVERY; DIAGNOSIS; DISEASES; ENDOTHELIAL CELLS; MEDICAL IMAGING; MEDICAL NANOTECHNOLOGY; MOLECULAR PHYSICS; NANOPARTICLES; THERANOSTICS; TUMORS;

CELL SURFACE RECEPTORS; ENHANCED PERMEABILITY AND RETENTION EFFECT; IMAGE-GUIDED TREATMENTS; MULTI-FUNCTIONAL NANOPARTICLES; NON-INVASIVE IMAGING; TARGETED NANOPARTICLE; TECHNOLOGICAL ADVANCES; TRIPLE-NEGATIVE BREAST CANCERS;

TARGETED DRUG DELIVERY;

BIOLOGICAL MARKER; CARBON NANOTUBE; CELL SURFACE RECEPTOR; CHEMOKINE RECEPTOR CXCR4; DOCETAXEL; EPIDERMAL GROWTH FACTOR RECEPTOR; FOLATE RECEPTOR; GOLD NANOPARTICLE; GROWTH FACTOR RECEPTOR; HERMES ANTIGEN; LIPOSOME; MUCIN 1; NANOPARTICLE; PACLITAXEL; SOMATOMEDIN RECEPTOR; ULTRASMALL SUPERPARAMAGNETIC IRON OXIDE; UROKINASE RECEPTOR; CD44 PROTEIN, HUMAN; CXCR4 PROTEIN, HUMAN; DRUG CARRIER; EGFR PROTEIN, HUMAN; FOLATE RECEPTOR 1; MUC1 PROTEIN, HUMAN; SOMATOMEDIN C RECEPTOR; WNT PROTEIN;

CANCER THERAPY; CELL SURFACE; DRUG DELIVERY SYSTEM; ENDOTHELIUM CELL; FIBROBLAST; HUMAN; MACROPHAGE; NANOMEDICINE; NANOTECHNOLOGY; NONHUMAN; POLYMERIZATION; PRIORITY JOURNAL; REVIEW; TRIPLE NEGATIVE BREAST CANCER; TUMOR MICROENVIRONMENT; WNT SIGNALING PATHWAY; ANIMAL; BREAST NEOPLASMS; CANCER TRANSPLANTATION; CHEMISTRY; FEMALE; METABOLISM; MOUSE; NUCLEAR MAGNETIC RESONANCE IMAGING; PERMEABILITY; PROCEDURES; PROGNOSIS; TRIPLE NEGATIVE BREAST NEOPLASMS;

ANIMALS; ANTIGENS, CD44; BREAST NEOPLASMS; DRUG CARRIERS; DRUG DELIVERY SYSTEMS; FEMALE; FOLATE RECEPTOR 1; HUMANS; LIPOSOMES; MAGNETIC RESONANCE IMAGING; MICE; MUCIN-1; NANOMEDICINE; NANOPARTICLES; NANOTUBES, CARBON; NEOPLASM TRANSPLANTATION; PERMEABILITY; PROGNOSIS; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTOR, IGF TYPE 1; RECEPTORS, CXCR4; RECEPTORS, UROKINASE PLASMINOGEN ACTIVATOR; TRIPLE NEGATIVE BREAST NEOPLASMS; WNT PROTEINS;

EID: 84943818330     PISSN: 19395116     EISSN: 19390041     Source Type: Journal    
DOI: 10.1002/wnan.1343     Document Type: Review

References (137)

1. Siegel R, Ma J, Zou Z, Jemal A. Cancer statistics, 2014. CA Cancer J Clin 2014, 64:9-29.
2. Ferlay J, Soerjomataram I, Ervik M, Dikshit R, Eser S, Mathers C, Rebelo M, Parkin DM, Forman D, Bray F. Cancer Incidence and Mortality Worldwide: IARC CancerBase No. 11. Lyon: IARC; 2013. Available at: http://globocan.iarc.fr.
3. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin 2011, 61:69-90.
4. Sorlie T, Perou CM, Tibshirani R, Aas T, Geisler S, Johnsen H, Hastie T, Eisen MB, van de Rijn M, Jeffrey SS, et al. Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc Natl Acad Sci USA 2001, 98:10869-10874.
5. Nielsen TO, Hsu FD, Jensen K, Cheang M, Karaca G, Hu Z, Hernandez-Boussard T, Livasy C, Cowan D, Dressler L, et al. Immunohistochemical and clinical characterization of the basal-like subtype of invasive breast carcinoma. Clin Cancer Res 2004, 10:5367-5374.
6. Prat A, Adamo B, Cheang MC, Anders CK, Carey LA, Perou CM. Molecular characterization of basal-like and non-basal-like triple-negative breast cancer. Oncologist 2013, 18:123-133.
7. Baselga J, Cortes J, Kim SB, Im SA, Hegg R, Im YH, Roman L, Pedrini JL, Pienkowski T, Knott A, et al. Pertuzumab plus trastuzumab plus docetaxel for metastatic breast cancer. N Engl J Med 2012, 366:109-119.
8. Early Breast Cancer Trialists' Collaborative Group. Effects of chemotherapy and hormonal therapy for early breast cancer on recurrence and 15-year survival: an overview of the randomised trials. Lancet 2005, 365:1687-1717.
9. Carey LA, Perou CM, Livasy CA, Dressler LG, Cowan D, Conway K, Karaca G, Troester MA, Tse CK, Edmiston S, et al. Race, breast cancer subtypes, and survival in the Carolina Breast Cancer Study. JAMA 2006, 295:2492-2502.
10. Bauer KR, Brown M, Cress RD, Parise CA, Caggiano V. Descriptive analysis of estrogen receptor (ER)-negative, progesterone receptor (PR)-negative, and HER2-negative invasive breast cancer, the so-called triple-negative phenotype: a population-based study from the California Cancer Registry. Cancer 2007, 109:1721-1728.
11. Foulkes WD, Stefansson IM, Chappuis PO, Begin LR, Goffin JR, Wong N, Trudel M, Akslen LA. Germline BRCA1 mutations and a basal epithelial phenotype in breast cancer. J Natl Cancer Inst 2003, 95:1482-1485.
12. Dogan BE, Gonzalez-Angulo AM, Gilcrease M, Dryden MJ, Yang WT. Multimodality imaging of triple receptor-negative tumors with mammography, ultrasound, and MRI. AJR Am J Roentgenol 2010, 194:1160-1166.
13. Oakman C, Viale G, Di Leo A. Management of triple negative breast cancer. Breast 2010, 19:312-321.
14. Dent R, Trudeau M, Pritchard KI, Hanna WM, Kahn HK, Sawka CA, Lickley LA, Rawlinson E, Sun P, Narod SA. Triple-negative breast cancer: clinical features and patterns of recurrence. Clin Cancer Res 2007, 13:4429-4434.
15. Liedtke C, Mazouni C, Hess KR, Andre F, Tordai A, Mejia JA, Symmans WF, Gonzalez-Angulo AM, Hennessy B, Green M, et al. Response to neoadjuvant therapy and long-term survival in patients with triple-negative breast cancer. J Clin Oncol 2008, 26:1275-1281.
16. Dent R, Hanna WM, Trudeau M, Rawlinson E, Sun P, Narod SA. Pattern of metastatic spread in triple-negative breast cancer. Breast Cancer Res Treat 2009, 115:423-428.
17. Haffty BG, Yang Q, Reiss M, Kearney T, Higgins SA, Weidhaas J, Harris L, Hait W, Toppmeyer D. Locoregional relapse and distant metastasis in conservatively managed triple negative early-stage breast cancer. J Clin Oncol 2006, 24:5652-5657.
18. Isakoff SJ. Triple-negative breast cancer: role of specific chemotherapy agents. Cancer J 2010, 16:53-61.
19. Adkins FC, Gonzalez-Angulo AM, Lei X, Hernandez-Aya LF, Mittendorf EA, Litton JK, Wagner J, Hunt KK, Woodward WA, Meric-Bernstam F. Triple-negative breast cancer is not a contraindication for breast conservation. Ann Surg Oncol 2011, 18:3164-3173.
20. Li X, Lewis MT, Huang J, Gutierrez C, Osborne CK, Wu MF, Hilsenbeck SG, Pavlick A, Zhang X, Chamness GC, et al. Intrinsic resistance of tumorigenic breast cancer cells to chemotherapy. J Natl Cancer Inst 2008, 100:672-679.
21. Guarneri V, Broglio K, Kau SW, Cristofanilli M, Buzdar AU, Valero V, Buchholz T, Meric F, Middleton L, Hortobagyi GN, et al. Prognostic value of pathologic complete response after primary chemotherapy in relation to hormone receptor status and other factors. J Clin Oncol 2006, 24:1037-1044.
22. Prat A, Perou CM. Deconstructing the molecular portraits of breast cancer. Mol Oncol 2011, 5:5-23.
23. Lehmann BD, Bauer JA, Chen X, Sanders ME, Chakravarthy AB, Shyr Y, Pietenpol JA. Identification of human triple-negative breast cancer subtypes and preclinical models for selection of targeted therapies. J Clin Invest 2011, 121:2750-2767.
24. Masuda H, Baggerly KA, Wang Y, Zhang Y, Gonzalez-Angulo AM, Meric-Bernstam F, Valero V, Lehmann BD, Pietenpol JA, Hortobagyi GN, et al. Differential response to neoadjuvant chemotherapy among 7 triple-negative breast cancer molecular subtypes. Clin Cancer Res 2013, 19:5533-5540.
25. Prat A, Lluch A, Albanell J, Barry WT, Fan C, Chacon JI, Parker JS, Calvo L, Plazaola A, Arcusa A, et al. Predicting response and survival in chemotherapy-treated triple-negative breast cancer. Br J Cancer 2014, 111:1532-1541.
26. Kennedy RD, Quinn JE, Mullan PB, Johnston PG, Harkin DP. The role of BRCA1 in the cellular response to chemotherapy. J Natl Cancer Inst 2004, 96:1659-1668.
27. Loi S, Pommey S, Haibe-Kains B, Beavis PA, Darcy PK, Smyth MJ, Stagg J. CD73 promotes anthracycline resistance and poor prognosis in triple negative breast cancer. Proc Natl Acad Sci USA 2013, 110:11091-11096.
28. Chekhun VF, Zhylchuk VE, Lukyanova NY, Vorontsova AL, Kudryavets YI. Expression of drug resistance proteins in triple-receptor-negative tumors as the basis of individualized therapy of the breast cancer patients. Exp Oncol 2009, 31:123-124.
29. Soma CE, Dubernet C, Bentolila D, Benita S, Couvreur P. Reversion of multidrug resistance by co-encapsulation of doxorubicin and cyclosporin A in polyalkylcyanoacrylate nanoparticles. Biomaterials 2000, 21:1-7.
30. Kobayashi H, Watanabe R, Choyke PL. Improving conventional enhanced permeability and retention (EPR) effects; what is the appropriate target? Theranostics 2013, 4:81-89.
31. Maeda H, Wu J, Sawa T, Matsumura Y, Hori K. Tumor vascular permeability and the EPR effect in macromolecular therapeutics: a review. J Control Release 2000, 65:271-284.
32. Yang WT, Dryden M, Broglio K, Gilcrease M, Dawood S, Dempsey PJ, Valero V, Hortobagyi G, Atchley D, Arun B. Mammographic features of triple receptor-negative primary breast cancers in young premenopausal women. Breast Cancer Res Treat 2008, 111:405-410.
33. de Kruijf EM, van Nes JG, van de Velde CJ, Putter H, Smit VT, Liefers GJ, Kuppen PJ, Tollenaar RA, Mesker WE. Tumor-stroma ratio in the primary tumor is a prognostic factor in early breast cancer patients, especially in triple-negative carcinoma patients. Breast Cancer Res Treat 2011, 125:687-696.
34. Jain RK, Stylianopoulos T. Delivering nanomedicine to solid tumors. Nat Rev Clin Oncol 2010, 7:653-664.
35. Sykes EA, Chen J, Zheng G, Chan WC. Investigating the impact of nanoparticle size on active and passive tumor targeting efficiency. ACS Nano 2014, 8:5696-5706.
36. 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 2014, 66:2-25.
37. Mazar AP. Urokinase plasminogen activator receptor choreographs multiple ligand interactions: implications for tumor progression and therapy. Clin Cancer Res 2008, 14:5649-5655.
38. Nielsen BS, Rank F, Illemann M, Lund LR, Dano K. Stromal cells associated with early invasive foci in human mammary ductal carcinoma in situ coexpress urokinase and urokinase receptor. Int J Cancer 2007, 120:2086-2095.
39. Pyke C, Graem N, Ralfkiaer E, Ronne E, Hoyer-Hansen G, Brunner N, Dano K. Receptor for urokinase is present in tumor-associated macrophages in ductal breast carcinoma. Cancer Res 1993, 53:1911-1915.
40. Han B, Nakamura M, Mori I, Nakamura Y, Kakudo K. Urokinase-type plasminogen activator system and breast cancer (Review). Oncol Rep 2005, 14:105-112.
41. Yang L, Peng XH, Wang YA, Wang X, Cao Z, Ni C, Karna P, Zhang X, Wood WC, Gao X, et al. Receptor-targeted nanoparticles for in vivo imaging of breast cancer. Clin Cancer Res 2009, 15:4722-4732.
42. Yang L, Sajja HK, Cao Z, Qian W, Bender L, Marcus AI, Lipowska M, Wood WC, Wang YA. uPAR-targeted optical imaging contrasts as theranostic agents for tumor margin detection. Theranostics 2013, 4:106-118.
43. LeBeau AM, Duriseti S, Murphy ST, Pepin F, Hann B, Gray JW, VanBrocklin HF, Craik CS. Targeting uPAR with antagonistic recombinant human antibodies in aggressive breast cancer. Cancer Res 2013, 73:2070-2081.
44. Meijer-van Gelder ME, Look MP, Peters HA, Schmitt M, Brunner N, Harbeck N, Klijn JG, Foekens JA. Urokinase-type plasminogen activator system in breast cancer: association with tamoxifen therapy in recurrent disease. Cancer Res 2004, 64:4563-4568.
45. LeBeau AM, Sevillano N, King ML, Duriseti S, Murphy ST, Craik CS, Murphy LL, VanBrocklin HF. Imaging the urokinase plasminongen activator receptor in preclinical breast cancer models of acquired drug resistance. Theranostics 2014, 4:267-279.
46. Tan DS, Marchio C, Jones RL, Savage K, Smith IE, Dowsett M, Reis-Filho JS. Triple negative breast cancer: molecular profiling and prognostic impact in adjuvant anthracycline-treated patients. Breast Cancer Res Treat 2008, 111:27-44.
47. Viale G, Rotmensz N, Maisonneuve P, Bottiglieri L, Montagna E, Luini A, Veronesi P, Intra M, Torrisi R, Cardillo A, et al. Invasive ductal carcinoma of the breast with the "triple-negative" phenotype: prognostic implications of EGFR immunoreactivity. Breast Cancer Res Treat 2009, 116:317-328.
48. Masuda H, Zhang D, Bartholomeusz C, Doihara H, Hortobagyi GN, Ueno NT. Role of epidermal growth factor receptor in breast cancer. Breast Cancer Res Treat 2012, 136:331-345.
49. Baselga J, Gomez P, Greil R, Braga S, Climent MA, Wardley AM, Kaufman B, Stemmer SM, Pego A, Chan A, et al. Randomized phase II study of the anti-epidermal growth factor receptor monoclonal antibody cetuximab with cisplatin versus cisplatin alone in patients with metastatic triple-negative breast cancer. J Clin Oncol 2013, 31:2586-2592.
50. Dickler MN, Cobleigh MA, Miller KD, Klein PM, Winer EP. Efficacy and safety of erlotinib in patients with locally advanced or metastatic breast cancer. Breast Cancer Res Treat 2009, 115:115-121.
51. Filmus J, Trent JM, Pollak MN, Buick RN. Epidermal growth factor receptor gene-amplified MDA-468 breast cancer cell line and its nonamplified variants. Mol Cell Biol 1987, 7:251-257.
52. Fitzpatrick SL, LaChance MP, Schultz GS. Characterization of epidermal growth factor receptor and action on human breast cancer cells in culture. Cancer Res 1984, 44:3442-3447.
53. Pollak MN, Schernhammer ES, Hankinson SE. Insulin-like growth factors and neoplasia. Nat Rev Cancer 2004, 4:505-518.
54. Resnik JL, Reichart DB, Huey K, Webster NJ, Seely BL. Elevated insulin-like growth factor I receptor autophosphorylation and kinase activity in human breast cancer. Cancer Res 1998, 58:1159-1164.
55. Yerushalmi R, Gelmon KA, Leung S, Gao D, Cheang M, Pollak M, Turashvili G, Gilks BC, Kennecke H. Insulin-like growth factor receptor (IGF-1R) in breast cancer subtypes. Breast Cancer Res Treat 2012, 132:131-142.
56. Law JH, Habibi G, Hu K, Masoudi H, Wang MY, Stratford AL, Park E, Gee JM, Finlay P, Jones HE, et al. Phosphorylated insulin-like growth factor-i/insulin receptor is present in all breast cancer subtypes and is related to poor survival. Cancer Res 2008, 68:10238-10246.
57. Litzenburger BC, Creighton CJ, Tsimelzon A, Chan BT, Hilsenbeck SG, Wang T, Carboni JM, Gottardis MM, Huang F, Chang JC, et al. High IGF-IR activity in triple-negative breast cancer cell lines and tumorgrafts correlates with sensitivity to anti-IGF-IR therapy. Clin Cancer Res 2011, 17:2314-2327.
58. Balko JM, Giltnane JM, Wang K, Schwarz LJ, Young CD, Cook RS, Owens P, Sanders ME, Kuba MG, Sanchez V, et al. Molecular profiling of the residual disease of triple-negative breast cancers after neoadjuvant chemotherapy identifies actionable therapeutic targets. Cancer Discov 2014, 4:232-245.
59. Yang L, Wu X, Wang Y, Zhang K, Wu J, Yuan YC, Deng X, Chen L, Kim CC, Lau S, et al. FZD7 has a critical role in cell proliferation in triple negative breast cancer. Oncogene 2011, 30:4437-4446.
60. Bilir B, Kucuk O, Moreno CS. Wnt signaling blockage inhibits cell proliferation and migration, and induces apoptosis in triple-negative breast cancer cells. J Transl Med 2013, 11:280.
61. Dey N, Barwick BG, Moreno CS, Ordanic-Kodani M, Chen Z, Oprea-Ilies G, Tang W, Catzavelos C, Kerstann KF, Sledge GW Jr, et al. Wnt signaling in triple negative breast cancer is associated with metastasis. BMC Cancer 2013, 13:537.
62. Yang L, Perez AA, Fujie S, Warden C, Li J, Wang Y, Yung B, Chen YR, Liu X, Zhang H, et al. Wnt modulates MCL1 to control cell survival in triple negative breast cancer. BMC Cancer 2014, 14:124.
63. Willnow TE, Nykjaer A, Herz J. Lipoprotein receptors: new roles for ancient proteins. Nat Cell Biol 1999, 1:E157-E162.
64. Siroy A, Abdul-Karim FW, Miedler J, Fong N, Fu P, Gilmore H, Baar J. MUC1 is expressed at high frequency in early-stage basal-like triple-negative breast cancer. Hum Pathol 2013, 44:2159-2166.
65. Ren J, Agata N, Chen D, Li Y, Yu WH, Huang L, Raina D, Chen W, Kharbanda S, Kufe D. Human MUC1 carcinoma-associated protein confers resistance to genotoxic anticancer agents. Cancer Cell 2004, 5:163-175.
66. Kufe DW. MUC1-C oncoprotein as a target in breast cancer: activation of signaling pathways and therapeutic approaches. Oncogene 2013, 32:1073-1081.
67. Raina D, Ahmad R, Joshi MD, Yin L, Wu Z, Kawano T, Vasir B, Avigan D, Kharbanda S, Kufe D. Direct targeting of the mucin 1 oncoprotein blocks survival and tumorigenicity of human breast carcinoma cells. Cancer Res 2009, 69:5133-5141.
68. Alam M, Rajabi H, Ahmad R, Jin C, Kufe D. Targeting the MUC1-C oncoprotein inhibits self-renewal capacity of breast cancer cells. Oncotarget 2014, 5:2622-2634.
69. Tammi RH, Kultti A, Kosma VM, Pirinen R, Auvinen P, Tammi MI. Hyaluronan in human tumors: pathobiological and prognostic messages from cell-associated and stromal hyaluronan. Semin Cancer Biol 2008, 18:288-295.
70. Auvinen P, Rilla K, Tumelius R, Tammi M, Sironen R, Soini Y, Kosma VM, Mannermaa A, Viikari J, Tammi R. Hyaluronan synthases (HAS1-3) in stromal and malignant cells correlate with breast cancer grade and predict patient survival. Breast Cancer Res Treat 2014, 143:277-286.
71. Idowu MO, Kmieciak M, Dumur C, Burton RS, Grimes MM, Powers CN, Manjili MH. CD44(+)/CD24(-/low) cancer stem/progenitor cells are more abundant in triple-negative invasive breast carcinoma phenotype and are associated with poor outcome. Hum Pathol 2012, 43:364-373.
72. Culty M, Nguyen HA, Underhill CB. The hyaluronan receptor (CD44) participates in the uptake and degradation of hyaluronan. J Cell Biol 1992, 116:1055-1062.
73. Misra S, Heldin P, Hascall VC, Karamanos NK, Skandalis SS, Markwald RR, Ghatak S. Hyaluronan-CD44 interactions as potential targets for cancer therapy. FEBS J 2011, 278:1429-1443.
74. O'Shannessy DJ, Somers EB, Maltzman J, Smale R, Fu YS. Folate receptor α (FRA) expression in breast cancer: identification of a new molecular subtype and association with triple negative disease. Springerplus 2012, 1:22.
75. Leamon CP, Reddy JA. Folate-targeted chemotherapy. Adv Drug Deliv Rev 2004, 56:1127-1141.
76. Zhang Z, Wang J, Tacha DE, Li P, Bremer RE, Chen H, Wei B, Xiao X, Da J, Skinner K, et al. Folate receptor α associated with triple-negative breast cancer and poor prognosis. Arch Pathol Lab Med 2014, 138:890-895.
77. Leamon CP, Low PS. Folate-mediated targeting: from diagnostics to drug and gene delivery. Drug Discov Today 2001, 6:44-51.
78. Chu QD, Panu L, Holm NT, Li BD, Johnson LW, Zhang S. High chemokine receptor CXCR4 level in triple negative breast cancer specimens predicts poor clinical outcome. J Surg Res 2010, 159:689-695.
79. Chen HW, Du CW, Wei XL, Khoo US, Zhang GJ. Cytoplasmic CXCR4 high-expression exhibits distinct poor clinicopathological characteristics and predicts poor prognosis in triple-negative breast cancer. Curr Mol Med 2013, 13:410-416.
80. Orimo A, Gupta PB, Sgroi DC, Arenzana-Seisdedos F, Delaunay T, Naeem R, Carey VJ, Richardson AL, Weinberg RA. Stromal fibroblasts present in invasive human breast carcinomas promote tumor growth and angiogenesis through elevated SDF-1/CXCL12 secretion. Cell 2005, 121:335-348.
81. Kojima Y, Acar A, Eaton EN, Mellody KT, Scheel C, Ben-Porath I, Onder TT, Wang ZC, Richardson AL, Weinberg RA, et al. Autocrine TGF-β and stromal cell-derived factor-1 (SDF-1) signaling drives the evolution of tumor-promoting mammary stromal myofibroblasts. Proc Natl Acad Sci USA 2010, 107:20009-20014.
82. Liang Z, Zhan W, Zhu A, Yoon Y, Lin S, Sasaki M, Klapproth JM, Yang H, Grossniklaus HE, Xu J, et al. Development of a unique small molecule modulator of CXCR4. PLoS One 2012, 7:e34038.
83. Sajja HK, East MP, Mao H, Wang YA, Nie S, Yang L. Development of multifunctional nanoparticles for targeted drug delivery and noninvasive imaging of therapeutic effect. Curr Drug Discov Technol 2009, 6:43-51.
84. O'Brien ME, Wigler N, Inbar M, Rosso R, Grischke E, Santoro A, Catane R, Kieback DG, Tomczak P, Ackland SP, et al. 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 2004, 15:440-449.
85. Huober J, Fett W, Nusch A, Neise M, Schmidt M, Wischnik A, Gerhardt S, Goehler T, Luck HJ, Rost A. A multicentric observational trial of pegylated liposomal doxorubicin for metastatic breast cancer. BMC Cancer 2010, 10:2.
86. Gradishar WJ. Albumin-bound paclitaxel: a next-generation taxane. Expert Opin Pharmacother 2006, 7:1041-1053.
87. Yamamoto Y, Kawano I, Iwase H. Nab-paclitaxel for the treatment of breast cancer: efficacy, safety, and approval. Onco Targets Ther 2011, 4:123-136.
88. Miele E, Spinelli GP, Miele E, Tomao F, Tomao S. Albumin-bound formulation of paclitaxel (Abraxane ABI-007) in the treatment of breast cancer. Int J Nanomedicine 2009, 4:99-105.
89. Allen TM, Cullis PR. Liposomal drug delivery systems: from concept to clinical applications. Adv Drug Deliv Rev 2013, 65:36-48.
90. Ahn RW, Chen F, Chen H, Stern ST, Clogston JD, Patri AK, Raja MR, Swindell EP, Parimi V, Cryns VL, et al. A novel nanoparticulate formulation of arsenic trioxide with enhanced therapeutic efficacy in a murine model of breast cancer. Clin Cancer Res 2010, 16:3607-3617.
91. Lee ES, Gao Z, Bae YH. Recent progress in tumor pH targeting nanotechnology. J Control Release 2008, 132:164-170.
92. Awada A, Bondarenko IN, Bonneterre J, Nowara E, Ferrero JM, Bakshi AV, Wilke C, Piccart M, CT4002 Study Group. A randomized controlled phase II trial of a novel composition of paclitaxel embedded into neutral and cationic lipids targeting tumor endothelial cells in advanced triple-negative breast cancer (TNBC). Ann Oncol 2014, 25:824-831.
93. Mamot C, Ritschard R, Wicki A, Kung W, Schuller J, Herrmann R, Rochlitz C. Immunoliposomal delivery of doxorubicin can overcome multidrug resistance mechanisms in EGFR-overexpressing tumor cells. J Drug Target 2012, 20:422-432.
94. Guo P, You JO, 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, 11:755-765.
95. Gao ZG, Tian L, Hu J, Park IS, Bae YH. Prevention of metastasis in a 4T1 murine breast cancer model by doxorubicin carried by folate conjugated pH sensitive polymeric micelles. J Control Release 2011, 152:84-89.
96. Luk BT, Fang RH, Zhang L. Lipid- and polymer-based nanostructures for cancer theranostics. Theranostics 2012, 2:1117-1126.
97. Dai W, Yang F, Ma L, Fan Y, He B, He Q, Wang X, Zhang H, Zhang Q. Combined mTOR inhibitor rapamycin and doxorubicin-loaded cyclic octapeptide modified liposomes for targeting integrin α3 in triple-negative breast cancer. Biomaterials 2014, 35:5347-5358.
98. Li S, Goins B, Hrycushko BA, Phillips WT, Bao A. Feasibility of eradication of breast cancer cells remaining in postlumpectomy cavity and draining lymph nodes following intracavitary injection of radioactive immunoliposomes. Mol Pharm 2012, 9:2513-2522.
99. Sepehri N, Rouhani H, Tavassolian F, Montazeri H, Khoshayand MR, Ghahremani MH, Ostad SN, Atyabi F, Dinarvand R. SN38 polymeric nanoparticles: in vitro cytotoxicity and in vivo antitumor efficacy in xenograft balb/c model with breast cancer versus irinotecan. Int J Pharm 2014, 471:485-497.
100. Schluep T, Hwang J, Cheng J, Heidel JD, Bartlett DW, Hollister B, Davis ME. Preclinical efficacy of the camptothecin-polymer conjugate IT-101 in multiple cancer models. Clin Cancer Res 2006, 12:1606-1614.
101. Young C, Schluep T, Hwang J, Eliasof S. CRLX101 (formerly IT-101)-a novel nanopharmaceutical of camptothecin in clinical development. Curr Bioact Compd 2011, 7:8-14.
102. Li Y, Jin M, Shao S, Huang W, Yang F, Chen W, Zhang S, Xia G, Gao Z. Small-sized polymeric micelles incorporating docetaxel suppress distant metastases in the clinically-relevant 4T1 mouse breast cancer model. BMC Cancer 2014, 14:329.
103. Johnstone TC, Kulak N, Pridgen EM, Farokhzad OC, Langer R, Lippard SJ. Nanoparticle encapsulation of mitaplatin and the effect thereof on in vivo properties. ACS Nano 2013, 7:5675-5683.
104. Lee SM, Ahn RW, Chen F, Fought AJ, O'Halloran TV, Cryns VL, Nguyen ST. Biological evaluation of pH-responsive polymer-caged nanobins for breast cancer therapy. ACS Nano 2010, 4:4971-4978.
105. Deng X, Cao M, Zhang J, Hu K, Yin Z, Zhou Z, Xiao X, Yang Y, Sheng W, Wu Y, et al. Hyaluronic acid-chitosan nanoparticles for co-delivery of MiR-34a and doxorubicin in therapy against triple negative breast cancer. Biomaterials 2014, 35:4333-4344.
106. Swaminathan SK, Roger E, Toti U, Niu L, Ohlfest JR, Panyam J. CD133-targeted paclitaxel delivery inhibits local tumor recurrence in a mouse model of breast cancer. J Control Release 2013, 171:280-287.
107. Zhou W, Zhou Y, Wu J, Liu Z, Zhao H, Liu J, Ding J. Aptamer-nanoparticle bioconjugates enhance intracellular delivery of vinorelbine to breast cancer cells. J Drug Target 2014, 22:57-66.
108. Kulhari H, Pooja D, Shrivastava S, Naidu VGM, Sistla R. Peptide conjugated polymeric nanoparticles as a carrier for targeted delivery of docetaxel. Colloids Surf B Biointerfaces 2014, 117:166-173.
109. Milane L, Duan Z, Amiji M. Therapeutic efficacy and safety of paclitaxel/lonidamine loaded EGFR-targeted nanoparticles for the treatment of multi-drug resistant cancer. PLoS One 2011, 6:e24075.
110. Milane L, Duan ZF, Amiji M. Pharmacokinetics and biodistribution of lonidamine/paclitaxel loaded, EGFR-targeted nanoparticles in an orthotopic animal model of multi-drug resistant breast cancer. Nanomedicine 2011, 7:435-444.
111. Dreaden EC, Morton SW, Shopsowitz KE, Choi JH, Deng ZJ, Cho NJ, Hammond PT. Bimodal tumor-targeting from microenvironment responsive hyaluronan layer-by-layer (LbL) nanoparticles. ACS Nano 2014, 8:8374-8382.
112. Huang J, Zhang H, Yu Y, Chen Y, Wang D, Zhang G, Zhou G, Liu J, Sun Z, Sun D, et al. Biodegradable self-assembled nanoparticles of poly (D, L-lactide-co-glycolide)/hyaluronic acid block copolymers for target delivery of docetaxel to breast cancer. Biomaterials 2014, 35:550-566.
113. Geng J, Sun C, Liu J, Liao LD, Yuan Y, Thakor N, Wang J, Liu B. Biocompatible conjugated polymer nanoparticles for efficient photothermal tumor therapy. Small (Epub ahead of print; 2014 Nov 3). doi:10.1002/smll.201402092.
114. Guo J, Hong H, Chen G, Shi S, Zheng Q, Zhang Y, Theuer CP, Barnhart TE, Cai W, Gong S. Image-guided and tumor-targeted drug delivery with radiolabeled unimolecular micelles. Biomaterials 2013, 34:8323-8332.
115. Liu Z, Chen K, Davis C, Sherlock S, Cao Q, Chen X, Dai H. Drug delivery with carbon nanotubes for in vivo cancer treatment. Cancer Res 2008, 68:6652-6660.
116. Robinson JT, Welsher K, Tabakman SM, Sherlock SP, Wang H, Luong R, Dai H. High performance in vivo near-IR (>1 mum) imaging and photothermal cancer therapy with carbon nanotubes. Nano Res 2010, 3:779-793.
117. Liu Z, Tabakman S, Sherlock S, Li X, Chen Z, Jiang K, Fan S, Dai H. Multiplexed five-color molecular imaging of cancer cells and tumor tissues with carbon nanotube Raman tags in the near-infrared. Nano Res 2010, 3:222-233.
118. De la Zerda A, Zavaleta C, Keren S, Vaithilingam S, Bodapati S, Liu Z, Levi J, Smith BR, Ma TJ, Oralkan O, et al. Carbon nanotubes as photoacoustic molecular imaging agents in living mice. Nat Nanotechnol 2008, 3:557-562.
119. Ayala-Orozco C, Urban C, Bishnoi S, Urban A, Charron H, Mitchell T, Shea M, Nanda S, Schiff R, Halas N, et al. Sub-100 nm gold nanomatryoshkas improve photo-thermal therapy efficacy in large and highly aggressive triple negative breast tumors. J Control Release 2014, 191:90-97.
120. Wang D, Xu Z, Yu H, Chen X, Feng B, Cui Z, Lin B, Yin Q, Zhang Z, Chen C, et al. Treatment of metastatic breast cancer by combination of chemotherapy and photothermal ablation using doxorubicin-loaded DNA wrapped gold nanorods. Biomaterials 2014, 35:8374-8384.
121. You J, Zhang G, Li C. Exceptionally high payload of doxorubicin in hollow gold nanospheres for near-infrared light-triggered drug release. ACS Nano 2010, 4:1033-1041.
122. Bulte JW, Kraitchman DL. Iron oxide MR contrast agents for molecular and cellular imaging. NMR Biomed 2004, 17:484-499.
123. Schultz JF, Bell JD, Goldstein RM, Kuhn JA, McCarty TM. Hepatic tumor imaging using iron oxide MRI: comparison with computed tomography, clinical impact, and cost analysis. Ann Surg Oncol 1999, 6:691-698.
124. Harisinghani MG, Barentsz J, Hahn PF, Deserno WM, Tabatabaei S, van de Kaa CH, de la Rosette J, Weissleder R. Noninvasive detection of clinically occult lymph-node metastases in prostate cancer. N Engl J Med 2003, 348:2491-2499.
125. McCarthy JR, Weissleder R. Multifunctional magnetic nanoparticles for targeted imaging and therapy. Adv Drug Deliv Rev 2008, 60:1241-1251.
126. Medarova Z, Rashkovetsky L, Pantazopoulos P, Moore A. Multiparametric monitoring of tumor response to chemotherapy by noninvasive imaging. Cancer Res 2009, 69:1182-1189.
127. Yang L, Cao Z, Sajja HK, Mao H, Wang L, Geng H, Xu H, Jiang T, Wood WC, Nie S, et al. Development of receptor targeted magnetic iron oxide nanoparticles for efficient drug delivery and tumor imaging. J Biomed Nanotechnol 2008, 4:439-449.
128. Wang L, Zhong X, Qian W, Huang J, Cao Z, Yu Q, Lipowska M, Lin R, Wang A, Yang L, et al. Ultrashort echo time (UTE) imaging of receptor targeted magnetic iron oxide nanoparticles in mouse tumor models. J Magn Reson Imaging 2014, 40:1071-1081.
129. He Y, Zhang L, Zhu D, Song C. Design of multifunctional magnetic iron oxide nanoparticles/mitoxantrone-loaded liposomes for both magnetic resonance imaging and targeted cancer therapy. Int J Nanomedicine 2014, 9:4055-4066.
130. Xi L, Zhou G, Gao N, Yang L, Gonzalo D, Hughes S, Jiang H. Photoacoustic and fluorescence image-guided surgery using a multifunctional targeted nanoprobe. Ann Surg Oncol 2014, 21:1602-1609.
131. Cao Z, Lee GY, Wang A, Sajja HK, Wang L, Long R, Barwick BG, Leyland-Jones BR, Wood WC, Nie S, et al. Theranostic nanoparticles for targeted therapy of triple negative breast cancer and for monitoring therapeutic response by MRI. Cancer Res 2010, 70:5482.
132. Guo P, Huang J, Wang L, Jia D, Yang J, Dillon DA, Zurakowski D, Mao H, Moses MA, Auguste DT. ICAM-1 as a molecular target for triple negative breast cancer. Proc Natl Acad Sci USA 2014, 111:14710-14715.
133. https://clinicaltrials.gov/ct2/show/NCT01770353. (Accessed January 3, 2015).
134. Herold CI, Anders CK. New targets for triple-negative breast cancer. Oncology (Williston Park) 2013, 27:846-854.
135. Lehmann BD, Pietenpol JA. Identification and use of biomarkers in treatment strategies for triple-negative breast cancer subtypes. J Pathol 2014, 232:142-150.
136. Xie J, Lee S, Chen X. Nanoparticle-based theranostic agents. Adv Drug Deliv Rev 2010, 62:1064-1079.
137. Zhang X, Bloch S, Akers W, Achilefu S. Near-infrared molecular probes for in vivo imaging. Curr Protoc Cytom 2012, Chapter 12:Unit12.27. doi:10.1002/0471142956.cy1227s60.