Tumor-Associated Macrophage-Mediated Targeted Therapy of Triple-Negative Breast Cancer

Molecular Pharmaceutics

Volumn 13, Issue 6, 2016, Pages 1833-1842

  Niu, Mengmeng ^a   Valdes, Solange ^a   Naguib, Youssef W ^a   Hursting, Stephen D ^b   Cui, Zhengrong ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^b University of North Carolina at Chapel Hill   (United States)

Author keywords

macrophage depletion; Nanoparticles; tumor growth inhibition

Indexed keywords

DOXORUBICIN; MANNOSE; NANOPARTICLE; ZOLEDRONIC ACID; ANTINEOPLASTIC AGENT; MACROGOL DERIVATIVE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER INHIBITION; CELL DENSITY; CELL PROLIFERATION; CONTROLLED STUDY; DRUG EFFECT; DRUG TARGETING; FEMALE; MOLECULARLY TARGETED THERAPY; MOUSE; NONHUMAN; PRIORITY JOURNAL; TRIPLE NEGATIVE BREAST CANCER; TUMOR ASSOCIATED LEUKOCYTE; TUMOR GROWTH; ANIMAL; C57BL MOUSE; CELL LINE; CHEMISTRY; DRUG EFFECTS; MACROPHAGE; PARTICLE SIZE; TRIPLE NEGATIVE BREAST NEOPLASMS; TUMOR CELL LINE;

ANIMALS; ANTINEOPLASTIC AGENTS; CELL LINE; CELL LINE, TUMOR; DOXORUBICIN; FEMALE; MACROPHAGES; MICE; MICE, INBRED C57BL; NANOPARTICLES; PARTICLE SIZE; POLYETHYLENE GLYCOLS; TRIPLE NEGATIVE BREAST NEOPLASMS;

EID: 84973646350     PISSN: 15438384     EISSN: 15438392     Source Type: Journal    
DOI: 10.1021/acs.molpharmaceut.5b00987     Document Type: Article

References (43)

1. Dong, H.; Claffey, K. P.; Brocke, S.; Epstein, P. M. Inhibition of breast cancer cell migration by activation of cAMP signaling Breast Cancer Res. Treat. 2015, 152 (1) 17-28 10.1007/s10549-015-3445-9
2. Santos, C.; Sanz-Pamplona, R.; Nadal, E.; Grasselli, J.; Pernas, S.; Dienstmann, R.; Moreno, V.; Tabernero, J.; Salazar, R. Intrinsic cancer subtypes - next steps into personalized medicine Cell. Oncol. 2015, 38 (1) 3-16 10.1007/s13402-014-0203-7
3. Dent, R.; Trudeau, M.; Pritchard, K. I.; Hanna, W. M.; Kahn, H. K.; Sawka, C. A.; Lickley, L. A.; Rawlinson, E.; Sun, P.; Narod, S. A. Triple-negative breast cancer: clinical features and patterns of recurrence Clin. Cancer Res. 2007, 13 (15) 4429-4434 10.1158/1078-0432.CCR-06-3045
4. Onitilo, A. A.; Engel, J. M.; Greenlee, R. T.; Mukesh, B. N. Breast cancer subtypes based on ER/PR and Her2 expression: comparison of clinicopathologic features and survival Clin. Med. Res. 2009, 7 (1-2) 4-13 10.3121/cmr.2008.825
5. Kallel, I.; Rebai, M.; Khabir, A.; Rebai, A. What common biomarkers characterize a triple-negative profile in breast cancer? Pathol. Biol. 2015, 63 (4-5) 224-9 10.1016/j.patbio.2015.07.005
6. Rakha, E. A.; Chan, S. Metastatic triple-negative breast cancer Clin oncol (R Coll Radiol) 2011, 23 (9) 587-600 10.1016/j.clon.2011.03.013
7. Prat, A.; Parker, J. S.; Karginova, O.; Fan, C.; Livasy, C.; Herschkowitz, J. I.; He, X.; Perou, C. M. Phenotypic and molecular characterization of the claudin-low intrinsic subtype of breast cancer Breast Cancer Res. 2010, 12 (5) R68 10.1186/bcr2635
8. Gucalp, A.; Traina, T. A. Triple-negative breast cancer: role of the androgen receptor Cancer J. 2010, 16 (1) 62-5 10.1097/PPO.0b013e3181ce4ae1
9. Longo, R.; Torino, F.; Gasparini, G. Targeted therapy of breast cancer Curr. Pharm. Des. 2007, 13 (5) 497-517 10.2174/138161207780162890
10. Reis-Filho, J. S.; Tutt, A. N. Triple negative tumours: a critical review Histopathology 2008, 52 (1) 108-18 10.1111/j.1365-2559.2007.02889.x
11. Yagata, H.; Kajiura, Y.; Yamauchi, H. Current strategy for triple-negative breast cancer: appropriate combination of surgery, radiation, and chemotherapy Breast Cancer 2011, 18 (3) 165-73 10.1007/s12282-011-0254-9
12. Pollard, J. W. Tumour-educated macrophages promote tumour progression and metastasis Nat. Rev. Cancer 2004, 4 (1) 71-8 10.1038/nrc1256
13. Condeelis, J.; Pollard, J. W. Macrophages: obligate partners for tumor cell migration, invasion, and metastasis Cell 2006, 124 (2) 263-6 10.1016/j.cell.2006.01.007
14. Xuan, Q. J.; Wang, J. X.; Nanding, A.; Wang, Z. P.; Liu, H.; Lian, X.; Zhang, Q. Y. Tumor-associated macrophages are correlated with tamoxifen resistance in the postmenopausal breast cancer patients Pathol. Oncol. Res. 2014, 20 (3) 619-24 10.1007/s12253-013-9740-z
15. Weizman, N.; Krelin, Y.; Shabtay-Orbach, A.; Amit, M.; Binenbaum, Y.; Wong, R. J.; Gil, Z. Macrophages mediate gemcitabine resistance of pancreatic adenocarcinoma by upregulating cytidine deaminase Oncogene 2014, 33 (29) 3812-9 10.1038/onc.2013.357
16. Amit, M.; Gil, Z. Macrophages increase the resistance of pancreatic adenocarcinoma cells to gemcitabine by upregulating cytidine deaminase Oncoimmunology 2013, 2 (12) e27231 10.4161/onci.27231
17. Yang, C.; He, L.; He, P.; Liu, Y.; Wang, W.; He, Y.; Du, Y.; Gao, F. Increased drug resistance in breast cancer by tumor-associated macrophages through IL-10/STAT3/bcl-2 signaling pathway Med. Oncol. 2015, 32 (2) 352 10.1007/s12032-014-0352-6
18. Zheng, Y.; Yang, J.; Qian, J.; Qiu, P.; Hanabuchi, S.; Lu, Y.; Wang, Z.; Liu, Z.; Li, H.; He, J.; Lin, P.; Weber, D.; Davis, R. E.; Kwak, L.; Cai, Z.; Yi, Q. PSGL-1/selectin and ICAM-1/CD18 interactions are involved in macrophage-induced drug resistance in myeloma Leukemia 2013, 27 (3) 702-10 10.1038/leu.2012.272
19. Medrek, C.; Ponten, F.; Jirstrom, K.; Leandersson, K. The presence of tumor associated macrophages in tumor stroma as a prognostic marker for breast cancer patients BMC Cancer 2012, 12, 306 10.1186/1471-2407-12-306
20. DeNardo, D. G.; Brennan, D. J.; Rexhepaj, E.; Ruffell, B.; Shiao, S. L.; Madden, S. F.; Gallagher, W. M.; Wadhwani, N.; Keil, S. D.; Junaid, S. A.; Rugo, H. S.; Hwang, E. S.; Jirstrom, K.; West, B. L.; Coussens, L. M. Leukocyte complexity predicts breast cancer survival and functionally regulates response to chemotherapy Cancer Discovery 2011, 1 (1) 54-67 10.1158/2159-8274.CD-10-0028
21. Yuan, Z. Y.; Luo, R. Z.; Peng, R. J.; Wang, S. S.; Xue, C. High infiltration of tumor-associated macrophages in triple-negative breast cancer is associated with a higher risk of distant metastasis OncoTargets Ther. 2014, 7, 1475-80 10.2147/OTT.S61838
22. Zhang, Y.; Cheng, S.; Zhang, M.; Zhen, L.; Pang, D.; Zhang, Q.; Li, Z. High-infiltration of tumor-associated macrophages predicts unfavorable clinical outcome for node-negative breast cancer PLoS One 2013, 8 (9) e76147 10.1371/journal.pone.0076147
23. Cannarile, M. A.; Ries, C. H.; Hoves, S.; Ruttinger, D. Targeting tumor-associated macrophages in cancer therapy and understanding their complexity Oncoimmunology 2014, 3 (9) e955356 10.4161/21624011.2014.955356
24. Pei, Y.; Yeo, Y. Drug delivery to macrophages: Challenges and opportunities. J. Controlled Release 2015, DOI: 10.1016/j.jconrel.2015.12.014.
25. Li, X.; Yao, W.; Yuan, Y.; Chen, P.; Li, B.; Li, J.; Chu, R.; Song, H.; Xie, D.; Jiang, X.; Wang, H. Targeting of tumour-infiltrating macrophages via CCL2/CCR2 signalling as a therapeutic strategy against hepatocellular carcinoma. Gut 2015, DOI: 10.1136/gutjnl-2015-310514.
26. Niu, M.; Naguib, Y. W.; Aldayel, A. M.; Shi, Y. C.; Hursting, S. D.; Hersh, M. A.; Cui, Z. Biodistribution and in vivo activities of tumor-associated macrophage-targeting nanoparticles incorporated with doxorubicin Mol. Pharmaceutics 2014, 11 (12) 4425-36 10.1021/mp500565q
27. Zhu, S.; Niu, M.; O'Mary, H.; Cui, Z. Targeting of Tumor-Associated Macrophages Made Possible by PEG-Sheddable, Mannose-Modified Nanoparticles Mol. Pharmaceutics 2013, 10 (9) 3525-3530 10.1021/mp400216r
28. Zhu, S.; Wonganan, P.; Lansakara, P. D.; O'Mary, H. L.; Li, Y.; Cui, Z. The effect of the acid-sensitivity of 4-(N)-stearoyl gemcitabine-loaded micelles on drug resistance caused by RRM1 overexpression Biomaterials 2013, 34 (9) 2327-2339 10.1016/j.biomaterials.2012.11.053
29. Dunlap, S. M.; Chiao, L. J.; Nogueira, L.; Usary, J.; Perou, C. M.; Varticovski, L.; Hursting, S. D. Dietary energy balance modulates epithelial-to-mesenchymal transition and tumor progression in murine claudin-low and basal-like mammary tumor models Cancer Prev. Res. 2012, 5 (7) 930-42 10.1158/1940-6207.CAPR-12-0034
30. Ford, N. A.; Nunez, N. P.; Holcomb, V. B.; Hursting, S. D. IGF1 dependence of dietary energy balance effects on murine Met1 mammary tumor progression, epithelial-to-mesenchymal transition, and chemokine expression Endocr.-Relat. Cancer 2013, 20 (1) 39-51 10.1530/ERC-12-0329
31. Guy, C. T.; Webster, M. A.; Schaller, M.; Parsons, T. J.; Cardiff, R. D.; Muller, W. J. Expression of the neu protooncogene in the mammary epithelium of transgenic mice induces metastatic disease Proc. Natl. Acad. Sci. U. S. A. 1992, 89 (22) 10578-82 10.1073/pnas.89.22.10578
32. Tsukamoto, A. S.; Grosschedl, R.; Guzman, R. C.; Parslow, T.; Varmus, H. E. Expression of the int-1 gene in transgenic mice is associated with mammary gland hyperplasia and adenocarcinomas in male and female mice Cell 1988, 55 (4) 619-25 10.1016/0092-8674(88)90220-6
33. Fuchs-Young, R.; Shirley, S. H.; Lambertz, I.; Colby, J. K.; Tian, J.; Johnston, D.; Gimenez-Conti, I. B.; Donehower, L. A.; Conti, C. J.; Hursting, S. D. P53 genotype as a determinant of ER expression and tamoxifen response in the MMTV-Wnt-1 model of mammary carcinogenesis Breast Cancer Res. Treat. 2011, 130 (2) 399-408 10.1007/s10549-010-1308-y
34. Naguib, Y. W.; Rodriguez, B. L.; Li, X.; Hursting, S. D.; Williams, R. O., 3rd; Cui, Z. Solid lipid nanoparticle formulations of docetaxel prepared with high melting point triglycerides: in vitro and in vivo evaluation Mol. Pharmaceutics 2014, 11 (4) 1239-49 10.1021/mp4006968
35. Ries, C. H.; Cannarile, M. A.; Hoves, S.; Benz, J.; Wartha, K.; Runza, V.; Rey-Giraud, F.; Pradel, L. P.; Feuerhake, F.; Klaman, I.; Jones, T.; Jucknischke, U.; Scheiblich, S.; Kaluza, K.; Gorr, I. H.; Walz, A.; Abiraj, K.; Cassier, P. A.; Sica, A.; Gomez-Roca, C.; de Visser, K. E.; Italiano, A.; Le Tourneau, C.; Delord, J. P.; Levitsky, H.; Blay, J. Y.; Ruttinger, D. Targeting tumor-associated macrophages with anti-CSF-1R antibody reveals a strategy for cancer therapy Cancer Cell 2014, 25 (6) 846-59 10.1016/j.ccr.2014.05.016
36. Katara, G. K.; Kulshrestha, A.; Jaiswal, M. K.; Pamarthy, S.; Gilman-Sachs, A.; Beaman, K. D. Inhibition of vacuolar ATPase subunit in tumor cells delays tumor growth by decreasing the essential macrophage population in the tumor microenvironment Oncogene 2016, 35 (8) 1058-65 10.1038/onc.2015.159
37. Olsson, A.; Nakhle, J.; Sundstedt, A.; Plas, P.; Bauchet, A. L.; Pierron, V.; Bruetschy, L.; Deronic, A.; Torngren, M.; Liberg, D.; Schmidlin, F.; Leanderson, T. Tasquinimod triggers an early change in the polarization of tumor associated macrophages in the tumor microenvironment J. Immunother Cancer 2015, 3, 53 10.1186/s40425-015-0098-5
38. Sant Cruz Biotechnology. Macrophage Marker(RM0029-11H3)Data Sheet. http://datasheets.scbt.com/sc-101447.pdf.
39. Sabatino, R.; Antonelli, A.; Battistelli, S.; Schwendener, R.; Magnani, M.; Rossi, L. Macrophage depletion by free bisphosphonates and zoledronate-loaded red blood cells PLoS One 2014, 9 (6) e101260 10.1371/journal.pone.0101260
40. Rogers, M. J.; Chilton, K. M.; Coxon, F. P.; Lawry, J.; Smith, M. O.; Suri, S.; Russell, R. G. Bisphosphonates induce apoptosis in mouse macrophage-like cells in vitro by a nitric oxide-independent mechanism J. Bone Miner. Res. 1996, 11 (10) 1482-91 10.1002/jbmr.5650111015
41. Fairweather, D.; Cihakova, D. Alternatively activated macrophages in infection and autoimmunity J. Autoimmun. 2009, 33 (3-4) 222-30 10.1016/j.jaut.2009.09.012
42. Jeong, S. K.; Kim, J. S.; Lee, C. G.; Park, Y. S.; Kim, S. D.; Yoon, S. O.; Han, D. H.; Lee, K. Y.; Jeong, M. H.; Jo, W. S. Tumor associated macrophages provide the survival resistance of tumor cells to hypoxic microenvironmental condition through IL-6 receptor-mediated signals. Immunobiology 2015, DOI: 10.1016/j.imbio.2015.11.010.
43. Hu, W.; Li, X.; Zhang, C.; Yang, Y.; Jiang, J.; Wu, C. Tumor-associated macrophages in cancers Clin. Transl. Oncol. 2016, 18 (3) 251-258 10.1007/s12094-015-1373-0