Modulating tumor hypoxia by nanomedicine for effective cancer therapy

Journal of Cellular Physiology

Volumn 233, Issue 3, 2018, Pages 2019-2031

  Jahanban Esfahlan, Rana ^a,b   de la Guardia, Miguel ^c   Ahmadi, Delshad ^a   Yousefi, Bahman ^a,d  

^a TABRIZ UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^b TABRIZ UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^c UNIVERSITY OF VALENCIA   (Spain)

^d TABRIZ UNIVERSITY OF MEDICAL SCIENCES   (Iran)

Author keywords

cancer; chemotherapy; hypoxia; nanocarriers; nanomedicine

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1ALPHA; NANOCARRIER; OXYGEN; DRUG CARRIER; NANOMATERIAL;

ANAEROBE; CANCER RESISTANCE; CANCER THERAPY; HUMAN; MALIGNANT NEOPLASM; NANOMEDICINE; NONHUMAN; OXYGENATION; PRIORITY JOURNAL; PROTEIN TARGETING; REOXYGENATION; REVIEW; TUMOR HYPOXIA; VASCULAR TUMOR; CELL HYPOXIA; DRUG EFFECTS; METABOLISM; NEOPLASM; NEOVASCULARIZATION (PATHOLOGY); PATHOLOGY;

CELL HYPOXIA; DRUG CARRIERS; HUMANS; NANOMEDICINE; NANOSTRUCTURES; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; OXYGEN; TUMOR HYPOXIA;

EID: 85019003010     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.25859     Document Type: Review

References (105)

1. Abbasi, M. M., Jahanban-Esfahlan, R., Monfaredan, A., Seidi, K., Hamishehkar, H., & Khiavi, M. M. (2014). Oral and IV dosages of doxorubicin-methotrexate loaded-nanoparticles inhibit progression of oral cancer by down-regulation of matrix methaloproteinase 2 expression in vivo. Asian Pacific Journal of Cancer Prevention, 15(24), 10705–10711.
2. Abbasi, M. M., Khiavi, M. M., Monfaredan, A., Hamishehkar, H., Seidi, K., & Jahanban-Esfahlan, R. (2014). DOX-MTX-NPs augment p53 mRNA expression in OSCC model in rat: Effects of IV and oral routes. Asian Pacific Journal of Cancer Prevention, 15(19), 8377–8382.
3. Abbasi, M. M., Monfaredan, A., Hamishehkar, H., & Jahanban-Esfahlan, R. (2014). New formulated “DOX-MTX-loaded nanoparticles” down- regulate HER2 gene expression and improve the clinical outcome in OSCCs model in rat: The effect of IV and oral modalities. Asian Pacific Journal of Cancer Prevention, 15(21), 9355–9360.
4. Abbasi, M. M., Monfaredan, A., Hamishehkar, H., Seidi, K., & Jahanban- Esfahlan, R. (2014). Novel DOX-MTX nanoparticles improve oral SCC clinical outcome by down regulation of lymph dissemination factor VEGF-C expression in vivo: Oral and IV modalities. Asian Pacific Journal of Cancer Prevention, 15(15), 6227–6232.
5. Ahmad, Z., Lv, S., Tang, Z., Shah, A., & Chen, X. (2016). Methoxy poly (ethylene glycol)-block-poly (glutamic acid)-graft-6-(2-nitroimidazole) hexyl amine nanoparticles for potential hypoxia-responsive delivery of doxorubicin. Journal of Biomaterials Science Polymer Edition, 27(1), 40–54.
6. Baban, C. K., Cronin, M., O'Hanlon, D., O'Sullivan, G. C., & Tangney, M. (2010). Bacteria as vectors for gene therapy of cancer. Bioengineered Bugs, 1(6), 385–394.
7. Babu, A., Templeton, A. K., Munshi, A., & Ramesh, R. (2014). Nanodrug delivery systems: A promising technology for detection, diagnosis, and treatment of cancer. AAPS PharmSciTech, 15(3), 709–721.
8. Bakalova, R., Ohba, H., Zhelev, Z., Ishikawa, M., & Baba, Y. (2004). Quantum dots as photosensitizers? Nature Biotechnology, 22(11), 1360–1361.
9. Barker, H. E., Paget, J. T. E., Khan, A. A., & Harrington, K. J. (2015). The tumour microenvironment after radiotherapy: Mechanisms of resistance and recurrence. Nature Reviews Cancer, 15(7), 409–425.
10. Bennewith, K. L., & Dedhar, S. (2011). Targeting hypoxic tumour cells to overcome metastasis. BMC Cancer, 11, 504.
11. Breier, G., Licht, A. H., Nicolaus, A., Klotzsche, A., Wielockx, B., & Kirsnerova, Z. (2007). HIF in vascular development and tumour angiogenesis. Novartis Foundation Symposium, 283, 126–133.
12. Brown, J. M. (2007). Tumor hypoxia in cancer therapy. Methods in Enzymology, 435, 297–321.
13. Brown, J. M., & Wilson, W. R. (2004). Exploiting tumour hypoxia in cancer treatment. Nature Reviews Cancer, 4(6), 437–447.
14. Cardoso, M. M., Peca, I. N., & Roque, A. C. (2012). Antibody-conjugated nanoparticles for therapeutic applications. Current Medicinal Chemistry, 19(19), 3103–3127.
15. Carmeliet, P., & Jain, R. K. (2011). Principles and mechanisms of vessel normalization for cancer and other angiogenic diseases. Nature Reviews Drug Discovery, 10(6), 417–427.
16. Casas, A., Di Venosa, G., Hasan, T., & Batlle, A. (2011). Mechanisms of resistance to photodynamic therapy. Current Medicinal Chemistry, 18(16), 2486–2515.
17. Cazares-Korner, C., Pires, I. M., Swallow, I. D., Grayer, S. C., O'Connor, L. J., Olcina, M. M., … Hammond, E. M. (2013). CH-01 is a hypoxia-activated prodrug that sensitizes cells to hypoxia/reoxygenation through inhibition of Chk1 and Aurora A. ACS Chemical Biology, 8(7), 1451–1459.
18. Chauhan, V. P., Stylianopoulos, T., Martin, J. D., Popović, Z., Chen, O., Kamoun, W. S., … Jain, R. K. (2012). Normalization of tumour blood vessels improves the delivery of nanomedicines in a size-dependent manner. Nature Nanotechnology, 7(6), 383–388.
19. Chen, H., Tian, J., He, W., & Guo, Z. (2015). H2O2-activatable and O2-evolving nanoparticles for highly efficient and selective photodynamic therapy against hypoxic tumor cells. Journal of the American Chemical Society, 137(4), 1539–1547.
20. Chen, Q., Feng, L., Liu, J., Zhu, W., Dong, Z., Wu, Y., & Liu, Z. (2016). Intelligent albumin-MnO2 nanoparticles as pH-/H2 O2 −Responsive dissociable nanocarriers to modulate tumor hypoxia for effective combination therapy. Advanced Materials (Deerfield Beach, Fla), 28(33), 7129–7136.
21. Cheng, Y., Cheng, H., Jiang, C., Qiu, X., Wang, K., Huan, W., … Hu, Y. (2015). Perfluorocarbon nanoparticles enhance reactive oxygen levels and tumour growth inhibition in photodynamic therapy. Nature Communications, 6, 8785.
22. Cooper, D. R., Bekah, D., & Nadeau, J. L. (2014). Gold nanoparticles and their alternatives for radiation therapy enhancement. Frontiers in Chemistry, 2, 86.
23. Cosse, J. P., & Michiels, C. (2008). Tumour hypoxia affects the responsiveness of cancer cells to chemotherapy and promotes cancer progression. Anti-cancer Agents in Medicinal Chemistry, 8(7), 790–797.
24. Cronin, M., Stanton, R. M., Francis, K. P., & Tangney, M. (2012). Bacterial vectors for imaging and cancer gene therapy: A review. Cancer Gene Therapy, 19(11), 731–740.
25. Denny, W. A. (2000). The role of hypoxia-activated prodrugs in cancer therapy. The Lancet Oncology, 1(1), 25–29.
26. Estanqueiro, M., Amaral, M. H., Conceicao, J., & Sousa Lobo, J. M. (2015). Nanotechnological carriers for cancer chemotherapy: The state of the art. Colloids and Surfaces B, Biointerfaces, 126, 631–648.
27. Felfoul, O., Mohammadi, M., Taherkhani, S., de Lanauze, D., Zhong Xu, Y., Loghin, D., … Martel, S. (2016). Magneto-aerotactic bacteria deliver drug-containing nanoliposomes to tumour hypoxic regions. Nature Nanotechnology, 11(11), 941–947.
28. Foehrenbacher, A., Secomb, T. W., Wilson, W. R., & Hicks, K. O. (2013). Design of optimized hypoxia-activated prodrugs using pharmacokinetic/pharmacodynamic modeling. Frontiers in Oncology, 3, 314.
29. Gao, S., Wang, G., Qin, Z., Wang, X., Zhao, G., Ma, Q., & Zhu, L. (2016a). Oxygen-generating hybrid nanoparticles to enhance fluorescent/photoacoustic/ultrasound imaging guided tumor photodynamic therapy. Biomaterials, 112, 324–335.
30. Gao, S., Zhang, L., Wang, G., Yang, K., Chen, M., Tian, R., … Zhu, L. (2016b). Hybrid graphene/Au activatable theranostic agent for multimodalities imaging guided enhanced photothermal therapy. Biomaterials, 79, 36–45.
31. Ge, J., Lan, M., Zhou, B., Liu, W., Guo, L., Wang, H., … Han, X. (2014a). A graphene quantum dot photodynamic therapy agent with high singlet oxygen generation. Nature Communications, 5, 4596.
32. Ge, J., Lan, M., Zhou, B., Liu, W., Guo, L., Wang, H., … Han, X. (2014b). A graphene quantum dot photodynamic therapy agent with high singlet oxygen generation. Nature Communications, 5, 4596.
33. Goel, S., Wong, A. H. -K., & Jain, R. K. (2012). Vascular normalization as a therapeutic strategy for malignant and nonmalignant disease. Cold Spring Harbor Perspectives in Medicine, 2(3), a006486.
34. Guise, C. P., Mowday, A. M., Ashoorzadeh, A., Yuan, R., Lin, W. H., Wu, D. H., … Ding, K. (2014). Bioreductive prodrugs as cancer therapeutics: Targeting tumor hypoxia. Chinese Journal of Cancer, 33(2), 80–86.
35. Henderson, B. W., & Fingar, V. H. (1987). Relationship of tumor hypoxia and response to photodynamic treatment in an experimental mouse tumor. Cancer Research, 47(12), 3110–3114.
36. Höckel, M., & Vaupel, P. (2001). Tumor hypoxia: Definitions and current clinical, biologic, and molecular aspects. Journal of the National Cancer Institute, 93(4), 266–276.
37. Horsman, M. R., Mortensen, L. S., Petersen, J. B., Busk, M., & Overgaard, J. (2012). Imaging hypoxia to improve radiotherapy outcome. Nature Reviews Clinical Oncology, 9(12), 674–687.
38. Huang, G., & Chen, L. (2010). Recombinant human endostatin improves anti-tumor efficacy of paclitaxel by normalizing tumor vasculature in Lewis lung carcinoma. Journal of Cancer Research and Clinical Oncology, 136(8), 1201–1211.
39. Huang, L., Zhang, Q. H., Ao, Q. L., Xing, H., Lu, Y. P., & Ma, D. (2007). Effect of hypoxia on the chemotherapeutic sensitivity of human ovarian cancer cells to paclitaxel and its mechanism. Zhonghua Zhong Liu Za Zhi [Chinese Journal of Oncology], 29(2), 96–100.
40. Huang, W. C., Chiang, W. H., Cheng, Y. H., Lin, W. C., Yu, C. F., Yen, C. Y., … Chiu, H. C. (2015). Tumortropic monocyte-mediated delivery of echogenic polymer bubbles and therapeutic vesicles for chemotherapy of tumor hypoxia. Biomaterials, 71, 71–83.
41. Huang, W. C., Shen, M. Y., Chen, H. H., Lin, S. C., Chiang, W. H., Wu, P. H., … Chiu, H. C. (2015). Monocytic delivery of therapeutic oxygen bubbles for dual-modality treatment of tumor hypoxia. Journal of Controlled Release: Official Journal of the Controlled Release Society, 220(Pt B), 738–750.
42. Ikeda, Y., Hisano, H., Nishikawa, Y., & Nagasaki, Y. (2016). Targeting and treatment of tumor hypoxia by newly designed prodrug possessing high permeability in solid tumors. Molecular Pharmaceutics, 13(7), 2283–2289.
43. Jahanban-Esfahlan, R., Seidi, K., & Zarghami, N. (2017). Tumor vascular infarction: Prospects and challenges. Int J Hematol, 105(3), 244–256.
44. Jain, K. K. (2001). Use of bacteria as anticancer agents. Expert Opinion on Biological Therapy, 1(2), 291–300.
45. Jain, R. K., & Forbes, N. S. (2001). Can engineered bacteria help control cancer. Proceedings of the National Academy of Sciences of the United States of America, 98(26), 14748–14750.
46. Karimaian, A., Majidinia, M., Bannazadeh Baghi, H., & Yousefi, B. (2017). The crosstalk between Wnt/β-catenin signaling pathway with DNA damage response and oxidative stress: Implications in cancer therapy. DNA Repair, 51(3), 14–19.
47. Kim, H., Mun, S., & Choi, Y. (2013). Photosensitizer-conjugated polymeric nanoparticles for redox-responsive fluorescence imaging and photodynamic therapy. Journal of Materials Chemistry B, 1(4), 429–431.
48. Kim, Y., Lin, Q., Glazer, P. M., & Yun, Z. (2009). Hypoxic tumor microenvironment and cancer cell differentiation. Current Molecular Medicine, 9(4), 425–434.
49. Kizaka-Kondoh, S., Inoue, M., Harada, H., & Hiraoka, M. (2003). Tumor hypoxia: A target for selective cancer therapy. Cancer Science, 94(12), 1021–1028.
50. Kopecka, J., Porto, S., Lusa, S., Gazzano, E., Salzano, G., Giordano, A., … Riganti, C. (2015). Self-assembling nanoparticles encapsulating zoledronic acid revert multidrug resistance in cancer cells. Oncotarget, 6(31), 31461–31478.
51. Kulkarni, P., Haldar, M. K., Katti, P., Dawes, C., You, S., Choi, Y., & Mallik, S. (2016). Hypoxia responsive, tumor penetrating lipid nanoparticles for delivery of chemotherapeutics to pancreatic cancer cell spheroids. Bioconjugate Chemistry, 27(8), 1830–1838.
52. Kulkarni, P., Haldar, M. K., You, S., Choi, Y., & Mallik, S. (2016). Hypoxia-Responsive polymersomes for drug delivery to hypoxic pancreatic cancer cells. Biomacromolecules, 17(8), 2507–2513.
53. Kumar, S., Aaron, J., & Sokolov, K. (2008). Directional conjugation of antibodies to nanoparticles for synthesis of multiplexed optical contrast agents with both delivery and targeting moieties. Nature Protocols, 3(2), 314–320.
54. Lara, P. C., Lloret, M., Clavo, B., Apolinario, R. M., Henríquez-Hernández, L. A., Bordón, E., … Rey, A. (2009). Severe hypoxia induces chemo-resistance in clinical cervical tumors through MVP over-expression. Radiation Oncology, 4(1), 29.
55. Lemmon, M. J., van Zijl, P., Fox, M. E., Mauchline, M. L., Giaccia, A. J., Minton, N. P., & Brown, J. M. (1997). Anaerobic bacteria as a gene delivery system that is controlled by the tumor microenvironment. Gene Therapy, 4(8), 791–796.
56. Li, J., Huo, M., Wang, J., Zhou, J., Mohammad, J. M., Zhang, Y., … Zhang, Q. (2012). Redox-sensitive micelles self-assembled from amphiphilic hyaluronic acid-deoxycholic acid conjugates for targeted intracellular delivery of paclitaxel. Biomaterials, 33(7), 2310–2320.
57. Li, J., Yin, T., Wang, L., Yin, L., Zhou, J., & Huo, M. (2015). Biological evaluation of redox-sensitive micelles based on hyaluronic acid-deoxycholic acid conjugates for tumor-specific delivery of paclitaxel. International Journal of Pharmaceutics, 483(1-2), 38–48.
58. Li, W., Zhao, X., Du, B., Li, X., Liu, S., Yang, X. Y., … Pan, Y. (2016). Gold nanoparticle-Mediated targeted delivery of recombinant human endostatin normalizes tumour vasculature and improves cancer therapy. Scientific Reports, 6, 30619.
59. Liang, D., Miller, G. H., & Tranmer, G. K. (2015). Hypoxia activated prodrugs: Factors influencing design and development. Current Medicinal Chemistry, 22(37), 4313–4325.
60. Liu, F. S. (2009). Mechanisms of chemotherapeutic drug resistance in cancer therapy-a quick review. Taiwanese Journal of Obstetrics & Gynecology, 48(3), 239–244.
61. Liu, P., Zhang, H., Wu, X., Guo, L., Wang, F., Xia, G., … Li, X. (2016). Tf-PEG-PLL-PLGA nanoparticles enhanced chemosensitivity for hypoxia-responsive tumor cells. OncoTargets and Therapy, 9, 5049–5059.
62. Liu, Z., Chen, W., Li, Y., & Xu, Q. (2016). Integrin alphavbeta3-targeted C-dot nanocomposites as multifunctional agents for cell targeting and photoacoustic imaging of superficial malignant tumors. Analytical Chemistry, 88(23), 11955–11962.
63. Liu, Z.-j, Semenza, G. L., & Zhang, H.-f (2015). Hypoxia-inducible factor 1 and breast cancer metastasis. Journal of Zhejiang University Science B, 16(1), 32–43.
64. Luo, C. H., Huang, C. T., Su, C. H., & Yeh, C. S. (2016). Bacteria-mediated hypoxia-specific delivery of nanoparticles for tumors imaging and therapy. Nano Letters, 16(6), 3493–3499.
65. Luo, Z., Zheng, M., Zhao, P., Chen, Z., Siu, F., Gong, P., … Cai, L. (2016). Self-monitoring artificial red cells with sufficient oxygen supply for enhanced photodynamic therapy. Scientific Reports, 6, 23393.
66. Mantovani, A., & Allavena, P. (2015). The interaction of anticancer therapies with tumor-associated macrophages. The Journal of Experimental Medicine, 212(4), 435–445.
67. Majidinia, M., & Yousefi, B. (2016a). Long non-coding RNAs in cancer drug resistance development. DNA Repair, 45, 25–33.
68. Majidinia, M., & Yousefi, B. (2016b). DNA damage response regulation by microRNAs as a therapeutic target in cancer. DNA Repair, 47, 1–11.
69. Majidinia, M., & Yousefi, B. (2017). Breast tumor stroma: A driving force in the development of resistance to therapies. Chemical Biology and Drug Design, https://doi.org/10.1111/cbdd.12893. [Epub ahead of print].
70. Masson, N., & Ratcliffe, P. J. (2014). Hypoxia signaling pathways in cancer metabolism: The importance of co-selecting interconnected physiological pathways. Cancer & Metabolism, 2(1), 3.
71. Mathew, A., Maekawa, T., & Sakthikumar, D. (2015). Aptamers in targeted nanotherapy. Current Topics in Medicinal Chemistry, 15(12), 1102–1114.
72. Moding, E. J., Kastan, M. B., & Kirsch, D. G. (2013). Strategies for optimizing the response of cancer and normal tissues to radiation. Nature Reviews Drug Discovery, 12(7), 526–542.
73. Molina, A. M., Morales-Cruz, M., Benitez, M., Berrios, K., Figueroa, C. M., & Griebenow, K. (2016). Redox-sensitive cross-linking enhances albumin nanoparticle function as delivery system for photodynamic cancer therapy. Journal of Nanomedicine & Nanotechnology, 6(3).
74. Paolicchi, E., Gemignani, F., Krstic-Demonacos, M., Dedhar, S., Mutti, L., & Landi, S. (2016). Targeting hypoxic response for cancer therapy. Oncotarget, 7(12), 13464–13478.
75. Patyar, S., Joshi, R., Byrav, D. S., Prakash, A., Medhi, B., & Das, B. K. (2010). Bacteria in cancer therapy: A novel experimental strategy. Journal of Biomedical Science, 17(1), 21.
76. Perche, F., Biswas, S., Patel, N. R., & Torchilin, V. P. (2016). Hypoxia-Responsive copolymer for siRNA delivery. Methods in Molecular Biology (Clifton, NJ), 1372, 139–162.
77. Perez-Herrero, E., & Fernandez-Medarde, A. (2015). Advanced targeted therapies in cancer: Drug nanocarriers, the future of chemotherapy. European Journal of Pharmaceutics and Biopharmaceutics: Official Journal of Arbeitsgemeinschaft Fur Pharmazeutische Verfahrenstechnik eV, 93, 52–79.
78. Philip, B., Ito, K., Moreno-Sanchez, R., & Ralph, S. J. (2013). HIF expression and the role of hypoxic microenvironments within primary tumours as protective sites driving cancer stem cell renewal and metastatic progression. Carcinogenesis, 34(8), 1699–1707.
79. Phillips, R. M. (2016). Targeting the hypoxic fraction of tumours using hypoxia-activated prodrugs. Cancer Chemotherapy and Pharmacology, 77(3), 441–457.
80. Prasad, P., Gordijo, C. R., Abbasi, A. Z., Maeda, A., Ip, A., Rauth, A. M., … Wu, X. Y. (2014). Multifunctional albumin-MnO(2) nanoparticles modulate solid tumor microenvironment by attenuating hypoxia, acidosis, vascular endothelial growth factor and enhance radiation response. ACS Nano, 8(4), 3202–3212.
81. Rauth, A. M., Melo, T., & Misra, V. (1998). Bioreductive therapies: An overview of drugs and their mechanisms of action. International Journal of Radiation Oncology, Biology, Physics, 42(4), 755–762.
82. Rockwell, S., Dobrucki, I. T., Kim, E. Y., Marrison, S. T., & Vu, V. T. (2009). Hypoxia and radiation therapy: Past history, ongoing research, and future promise. Current Molecular Medicine, 9(4), 442–458.
83. Rofstad, E. K., Sundfor, K., Lyng, H., & Trope, C. G. (2000). Hypoxia-induced treatment failure in advanced squamous cell carcinoma of the uterine cervix is primarily due to hypoxia-induced radiation resistance rather than hypoxia-induced metastasis. British Journal of Cancer, 83(3), 354–359.
84. Semenza, G. L. (2008). Hypoxia-inducible factor 1 and cancer pathogenesis. IUBMB Life, 60(9), 591–597.
85. Semenza, G. L. (2009). Regulation of cancer cell metabolism by hypoxia-inducible factor 1. Seminars in Cancer Biology, 19(1), 12–16.
86. Semenza, G. L. (2010). HIF-1: upstream and downstream of cancer metabolism. Current Opinion in Genetics & Development, 20(1), 51–56.
87. Shannon, A. M., Bouchier-Hayes, D. J., Condron, C. M., & Toomey, D. (2003). Tumour hypoxia, chemotherapeutic resistance and hypoxia-related therapies. Cancer Treatment Reviews, 29(4), 297–307.
88. Simon, J. M. (2007). Hypoxia and angiogenesis. Bulletin Du Cancer 94 Spec No, S160–S165.
89. Song, G., Liang, C., Yi, X., Zhao, Q., Cheng, L., Yang, K., & Liu, Z. (2016). Perfluorocarbon-Loaded hollow Bi2Se3 nanoparticles for timely supply of oxygen under near-Infrared light to enhance the radiotherapy of cancer. Advanced Materials (Deerfield beach. Fla), 28(14), 2716–2723.
90. Song, X., Feng, L., Liang, C., Yang, K., & Liu, Z. (2016). Ultrasound triggered tumor oxygenation with oxygen-Shuttle nanoperfluorocarbon to overcome hypoxia-Associated resistance in cancer therapies. Nano Letters, 16(10), 6145–6153.
91. Sun, H., & Zu, Y. (2015). Aptamers and their applications in nanomedicine. Small (Weinheim an Der Bergstrasse, Germany), 11(20), 2352–2364.
92. Thambi, T., Park, J. H., & Lee, D. S. (2016). Hypoxia-responsive nanocarriers for cancer imaging and therapy: Recent approaches and future perspectives. Chemical Communications (Cambridge, England), 52(55), 8492–8500.
93. Tromberg, B. J., Kimel, S., Orenstein, A., Barker, S. J., Hyatt, J., Nelson, J. S., … Berns, M. W. (1990). Tumor oxygen tension during photodynamic therapy. Journal of Photochemistry and Photobiology B: Biology, 5(1), 121–126.
94. Tsai, Y. P., & Wu, K. J. (2012). Hypoxia-regulated target genes implicated in tumor metastasis. Journal of Biomedical Science, 19, 102.
95. Vinogradov, S., Warren, G., & Wei, X. (2014). Macrophages associated with tumors as potential targets and therapeutic intermediates. Nanomedicine (London, England), 9(5), 695–707.
96. Wei, M. Q., Mengesha, A., Good, D., & Anne, J. (2008). Bacterial targeted tumour therapy-dawn of a new era. Cancer Letters, 259(1), 16–27.
97. Wicki, A., Witzigmann, D., Balasubramanian, V., & Huwyler, J. (2015). Nanomedicine in cancer therapy: Challenges, opportunities, and clinical applications. Journal of Controlled Release: Official Journal of the Controlled Release Society, 200, 138–157.
98. Xu, L., Qiu, X., Zhang, Y., Cao, K., Zhao, X., Wu, J., & Guo, H. (2016). Liposome encapsulated perfluorohexane enhances radiotherapy in mice without additional oxygen supply. Journal of Translational Medicine, 14, 268.
99. Yin, T., Wang, L., Yin, L., Zhou, J., & Huo, M. (2015). Co-delivery of hydrophobic paclitaxel and hydrophilic AURKA specific siRNA by redox-sensitive micelles for effective treatment of breast cancer. Biomaterials, 61, 10–25.
100. Yin, T., Wu, Q., Wang, L., Yin, L., Zhou, J., & Huo, M. (2015). Well-Defined redox-Sensitive polyethene glycol-Paclitaxel prodrug conjugate for tumor-Specific delivery of paclitaxel using octreotide for tumor targeting. Molecular Pharmaceutics, 12(8), 3020–3031.
101. Yousefi, B., Zarghami, N., Samadi, N., & Majidinia, M. (2016). Peroxisome proliferator-Activated receptors and their ligands in cancer drug-Resistance: Opportunity or challenge. Anti-Cancer Agents in Medicinal Chemistry, 16(12), 1541–1548.
102. Zheng, D., Seferos, D. S., Giljohann, D. A., Patel, P. C., & Mirkin, C. A. (2009). Aptamer nano-flares for molecular detection in living cells. Nano Letters, 9(9), 3258–3261.
103. Zheng, D. W., Li, B., Li, C. X., Fan, J. X., Lei, Q., Li, C., … Zhang, X. Z. (2016). Carbon-Dot-Decorated carbon nitride nanoparticles for enhanced photodynamic therapy against hypoxic tumor via water splitting. ACS Nano, 10(9), 8715–8722.
104. Zhou, G., Li, L., Xing, J., Jalde, S., Li, Y., Cai, J., … Ji, M. (2016). Redox responsive liposomal nanohybrid cerasomes for intracellular drug delivery. Colloids and Surfaces B, Biointerfaces, 148, 518–525.
105. Zhu, W., Dong, Z., Fu, T., Liu, J., Chen, Q., Li, Y., … Liu, Z. (2016). Modulation of hypoxia in solid tumor microenvironment with MnO2 nanoparticles to enhance photodynamic therapy. Advanced Functional Materials, 26(30), 5490–5498.