Improving cancer therapies by targeting the physical and chemical hallmarks of the tumor microenvironment

Cancer Letters

Volumn 380, Issue 1, 2016, Pages 330-339

  Ivey, Jill W ^a   Bonakdar, Mohammad ^b   Kanitkar, Akanksha ^a   Davalos, Rafael V ^a,b   Verbridge, Scott S ^a  

^a VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

^b Virginia Polytechnic Institute and State University   (United States)

Author keywords

Chemcical tumor microenvironment; Electroporation therapy; Physical tumor microenvironment; Tumor microenvironment targeting

Indexed keywords

ANGIOGENESIS INHIBITOR; BICARBONATE; BIOLOGICAL MARKER; GLYCERYL TRINITRATE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; TUMOR ANTIGEN; ANTINEOPLASTIC AGENT; DRUG CARRIER;

ACIDITY; ANGIOGENESIS; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; BACILLUS; BACTERIAL SPORE; BIFIDOBACTERIUM; BLOOD VESSEL PERMEABILITY; BREAST CANCER; CANCER CELL; CANCER THERAPY; CELL CYCLE ARREST; CELL KILLING; CLOSTRIDIUM; DISEASE MARKER; DRUG EFFICACY; ELECTROPORATION; ENDOTHELIUM CELL; ENHANCED PERMEABILITY AND RETENTION; GENETIC HETEROGENEITY; GLYCOLYSIS; HIGH FREQUENCY IRREVERSIBLE ELECTROPORATION; HIGH INTENSITY FOCUSED ULTRASOUND; HUMAN; HYPOXIA; IRREVERSIBLE ELECTROPORATION; LISTERIA; MYCOBACTERIUM; NANOSECOND PULSED ELECTRIC FIELD; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN TARGETING; PULSED ELECTRIC FIELD; RADIOFREQUENCY ABLATION; SALMONELLA; SHORT SURVEY; TUMOR ABLATION; TUMOR GROWTH; TUMOR MICROENVIRONMENT; VASCULAR ENDOTHELIUM; ABLATION THERAPY; ANIMAL; DRUG DELIVERY SYSTEM; DRUG RESISTANCE; METABOLISM; NEOPLASMS; PATHOLOGY; PH; PROCEDURES; TUMOR HYPOXIA;

ABLATION TECHNIQUES; ANIMALS; ANTINEOPLASTIC AGENTS; DRUG CARRIERS; DRUG DELIVERY SYSTEMS; DRUG RESISTANCE, NEOPLASM; HUMANS; HYDROGEN-ION CONCENTRATION; NEOPLASMS; TUMOR HYPOXIA; TUMOR MICROENVIRONMENT;

EID: 84954306847     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2015.12.019     Document Type: Review

References (148)

1. [1] Malik, I.A., Naz, N., Sheikh, N., Khan, S., Moriconi, F., Blaschke, M., et al. Comparison of changes in gene expression of transferrin receptor-1 and other iron-regulatory proteins in rat liver and brain during acute-phase response. Cell Tissue Res 344 (2011), 299–312.
2. [2] Di Fiore, P.P., Pierce, J.H., Fleming, T.P., Hazan, R., Ullrich, A., King, C.R., et al. Overexpression of the human EGF receptor confers an EGF-dependent transformed phenotype to NIH 3T3 cells. Cell 51 (1987), 1063–1070.
3. [3] Kraus, M.H., Popescu, N., Amsbaugh, S., King, C.R., Overexpression of the EGF receptor-related proto-oncogene erbB-2 in human mammary tumor cell lines by different molecular mechanisms. EMBO J., 6, 1987, 605.
4. [4] Hynes, N.E., Lane, H.A., ERBB receptors and cancer: the complexity of targeted inhibitors. Nat. Rev. Cancer 5 (2005), 341–354.
5. [5] Singh, S.K., Hawkins, C., Clarke, I.D., Squire, J.A., Bayani, J., Hide, T., et al. Identification of human brain tumour initiating cells. Nature 432 (2004), 396–401.
6. [6] Al-Hajj, M., Wicha, M.S., Benito-Hernandez, A., Morrison, S.J., Clarke, M.F., Prospective identification of tumorigenic breast cancer cells. PNAS 100 (2003), 3983–3988.
7. [7] Ricci-Vitiani, L., Lombardi, D.G., Pilozzi, E., Biffoni, M., Todaro, M., Peschle, C., et al. Identification and expansion of human colon-cancer-initiating cells. Nature 445 (2007), 111–115.
8. [8] Dick, D., Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat. Med 3 (1997), 730–737.
9. [9] Caceres-Cortes, J., Mindeni, M., Patersoni, B., Caligiuri, M.A., A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature, 367, 1994, 17.
10. [10] Höckel, M., Vaupel, P., Tumor hypoxia: definitions and current clinical, biologic, and molecular aspects. J. Natl Cancer Inst 93 (2001), 266–276.
11. [11] Shannon, A.M., Bouchier-Hayes, D.J., Condron, C.M., Toomey, D., Tumour hypoxia, chemotherapeutic resistance and hypoxia-related therapies. Cancer Treat. Rev 29 (2003), 297–307.
12. [12] Carmeliet, P., Jain, R.K., Angiogenesis in cancer and other diseases. Nature 407 (2000), 249–257.
13. [13] Vaupel, P., Kallinowski, F., Okunieff, P., Blood flow, oxygen and nutrient supply, and metabolic microenvironment of human tumors: a review. Cancer Res 49 (1989), 6449–6465.
14. [14] Stylianopoulos, T., Martin, J.D., Chauhan, V.P., Jain, S.R., Diop-Frimpong, B., Bardeesy, N., et al. Causes, consequences, and remedies for growth-induced solid stress in murine and human tumors. PNAS 109 (2012), 15101–15108.
15. [15] Karagiannis, G.S., Poutahidis, T., Erdman, S.E., Kirsch, R., Riddell, R.H., Diamandis, E.P., Cancer-associated fibroblasts drive the progression of metastasis through both paracrine and mechanical pressure on cancer tissue. Mol. Cancer Res 10 (2012), 1403–1418.
16. [16] Masuzaki, R., Tateishi, R., Yoshida, H., Sato, T., Ohki, T., Goto, T., et al. Assessing liver tumor stiffness by transient elastography. Hepatol. Int 1 (2007), 394–397.
17. [17] Paszek, M.J., Zahir, N., Johnson, K.R., Lakins, J.N., Rozenberg, G.I., Gefen, A., et al. Tensional homeostasis and the malignant phenotype. Cancer Cell 8 (2005), 241–254.
18. [18] Tuxhorn, J.A., Ayala, G.E., Smith, M.J., Smith, V.C., Dang, T.D., Rowley, D.R., Reactive stroma in human prostate cancer induction of myofibroblast phenotype and extracellular matrix remodeling. Clin. Cancer Res 8 (2002), 2912–2923.
19. [19] Krouskop, T.A., Wheeler, T.M., Kallel, F., Garra, B.S., Hall, T., Elastic moduli of breast and prostate tissues under compression. Ultrason. Imaging 20 (1998), 260–274.
20. [20] Faria, E.C., Ma, N., Gazi, E., Gardner, P., Brown, M., Clarke, N.W., et al. Measurement of elastic properties of prostate cancer cells using AFM. Analyst 133 (2008), 1498–1500.
21. [21] Suresh, S., Biomechanics and biophysics of cancer cells. Acta Mater 55 (2007), 3989–4014.
22. [22] Jain, R.K., Martin, J.D., Stylianopoulos, T., The role of mechanical forces in tumor growth and therapy. Annu. Rev. Biomed. Eng, 16, 2014, 321.
23. [23] Goel, S., Duda, D.G., Xu, L., Munn, L.L., Boucher, Y., Fukumura, D., et al. Normalization of the vasculature for treatment of cancer and other diseases. Physiol. Rev 91 (2011), 1071–1121.
24. [24] Boucher, Y., Kirkwood, J.M., Opacic, D., Desantis, M., Jain, R.K., Interstitial hypertension in superficial metastatic melanomas in humans. Cancer Res 51 (1991), 6691–6694.
25. [25] Boucher, Y., Baxter, L.T., Jain, R.K., Interstitial pressure gradients in tissue-isolated and subcutaneous tumors: implications for therapy. Cancer Res 50 (1990), 4478–4484.
26. [26] Less, J.R., Posner, M.C., Boucher, Y., Borochovitz, D., Wolmark, N., Jain, R.K., Interstitial hypertension in human breast and colorectal tumors. Cancer Res 52 (1992), 6371–6374.
27. [27] Roh, H., Boucher, Y., Kalnicki, S., Buchsbaum, R., Bloomer, W., Jain, R., Interstitial hypertension in carcinoma of uterine cervix in patients: possible correlation with tumor oxygenation and radiation response. Cancer Res 51 (1991), 6695–6698.
28. [28] Boucher, Y., Leunig, M., Jain, R.K., Tumor angiogenesis and interstitial hypertension. Cancer Res 56 (1996), 4264–4266.
29. [29] Jain, R.K., Tong, R.T., Munn, L.L., Effect of vascular normalization by antiangiogenic therapy on interstitial hypertension, peritumor edema, and lymphatic metastasis: insights from a mathematical model. Cancer Res 67 (2007), 2729–2735.
30. [30] Cure, J., Cancer an electrical phenomenon, Resonant. 1991.
31. [31] Stern, R., Milestone, B., Gatenby, R., Carcinogenesis and the plasma membrane. Med. Hypotheses 52 (1999), 367–372.
32. [32] Cone, C.D., Unified theory on the basic mechanism of normal mitotic control and oncogenesis. J. Theor. Biol 30 (1971), 151–181.
33. [33] Niemtzow, R.C., Transmembrane potentials and characteristics of immune and tumor cells. 1985, CRC Press LLC.
34. [34] Zhao, Y., Zhao, X.T., Chen, D.Y., Luo, Y.N., Jiang, M., Wei, C., et al. Tumor cell characterization and classification based on cellular specific membrane capacitance and cytoplasm conductivity. Biosens. Bioelectron 57 (2014), 245–253.
35. [35] Brennan, D.J., Rexhepaj, E., O'Brien, S.L., McSherry, E., O'Connor, D.P., Fagan, A., et al. Altered cytoplasmic-to-nuclear ratio of survivin is a prognostic indicator in breast cancer. Clin. Cancer Res 14 (2008), 2681–2689.
36. [36] Louis, D.N., Ohgaki, H., Wiestler, O.D., Cavenee, W.K., Burger, P.C., Jouvet, A., et al. The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol 114 (2007), 97–109.
37. [37] Ko, L., Koestner, A., Wechsler, W., Morphological characterization of nitrosourea-induced glioma cell lines and clones. Acta Neuropathol 51 (1980), 23–31.
38. [38] Maroulakou, I.G., Anver, M., Garrett, L., Green, J.E., Prostate and mammary adenocarcinoma in transgenic mice carrying a rat C3 (1) simian virus 40 large tumor antigen fusion gene. PNAS 91 (1994), 11236–11240.
39. [39] Blad, B., Baldetorp, B., Impedance spectra of tumour tissue in comparison with normal tissue; a possible clinical application for electrical impedance tomography. Physiol. Meas, 17, 1996, A105.
40. [40] Foster, K., Schepps, J., Dielectric properties of tumor and normal tissues at radio through microwave frequencies. J. Microw. Power 16 (1981), 107–119.
41. [41] Laufer, S., Ivorra, A., Reuter, V.E., Rubinsky, B., Solomon, S.B., Electrical impedance characterization of normal and cancerous human hepatic tissue. Physiol. Meas, 31, 2010, 995.
42. [42] Da Silva, J.E., De Sá, J.M., Jossinet, J., Classification of breast tissue by electrical impedance spectroscopy. Med. Biol. Eng. Comput 38 (2000), 26–30.
43. [43] Jossinet, J., Variability of impedivity in normal and pathological breast tissue. Med. Biol. Eng. Comput 34 (1996), 346–350.
44. [44] Toso, S., Piccoli, A., Gusella, M., Menon, D., Bononi, A., Crepaldi, G., et al. Altered tissue electric properties in lung cancer patients as detected by bioelectric impedance vector analysis. Nutrition 16 (2000), 120–124.
45. [45] Andreev, O.A., Engelman, D.M., Reshetnyak, Y.K., pH-sensitive membrane peptides (pHLIPs) as a novel class of delivery agents. Mol. Membr. Biol 27 (2010), 341–352.
46. [46] Andreev, O.A., Engelman, D.M., Reshetnyak, Y.K., Targeting diseased tissues by pHLIP insertion at low cell surface pH. Front. Physiol, 5, 2014.
47. [47] Andreev, O.A., Dupuy, A.D., Segala, M., Sandugu, S., Serra, D.A., Chichester, C.O., et al. Mechanism and uses of a membrane peptide that targets tumors and other acidic tissues in vivo. PNAS 104 (2007), 7893–7898.
48. [48] Yao, L., Daniels, J., Wijesinghe, D., Andreev, O.A., Reshetnyak, Y.K., pHLIP®-mediated delivery of PEGylated liposomes to cancer cells. J. Control. Release 167 (2013), 228–237.
49. [49] Wijesinghe, D., Arachchige, M.C., Lu, A., Reshetnyak, Y.K., Andreev, O.A., pH dependent transfer of nano-pores into membrane of cancer cells to induce apoptosis. Sci. Rep, 3, 2013.
50. [50] Yao, L., Daniels, J., Moshnikova, A., Kuznetsov, S., Ahmed, A., Engelman, D.M., et al. pHLIP peptide targets nanogold particles to tumors. PNAS 110 (2013), 465–470.
51. [51] Cheng, C.J., Bahal, R., Babar, I.A., Pincus, Z., Barrera, F., Liu, C., et al. MicroRNA silencing for cancer therapy targeted to the tumour microenvironment. Nature 518 (2015), 107–110.
52. [52] Han, L., Guo, Y., Ma, H., He, X., Kuang, Y., Zhang, N., et al. Acid active receptor-specific peptide ligand for in vivo tumor-targeted delivery. Small 9 (2013), 3647–3658.
53. [53] Yang, X.-Z., Du, J.-Z., Dou, S., Mao, C.-Q., Long, H.-Y., Wang, J., Sheddable ternary nanoparticles for tumor acidity-targeted siRNA delivery. ACS Nano 6 (2011), 771–781.
54. [54] Du, J.Z., Sun, T.M., Song, W.J., Wu, J., Wang, J., A tumor-acidity-activated charge-conversional nanogel as an intelligent vehicle for promoted tumoral-cell uptake and drug delivery. Angew. Chem. Int. Ed. Engl 122 (2010), 3703–3708.
55. [55] Robey, I.F., Baggett, B.K., Kirkpatrick, N.D., Roe, D.J., Dosescu, J., Sloane, B.F., et al. Bicarbonate increases tumor pH and inhibits spontaneous metastases. Cancer Res 69 (2009), 2260–2268.
56. [56] Hashim, A.I., Cornnell, H.H., Ribeiro, M.D.L.C., Abrahams, D., Cunningham, J., Lloyd, M., et al. Reduction of metastasis using a non-volatile buffer. Clin. Exp. Metastasis 28 (2011), 841–849.
57. [57] Brown, J.M., Wilson, W.R., Exploiting tumour hypoxia in cancer treatment. Nat. Rev. Cancer 4 (2004), 437–447.
58. [58] Wilson, W.R., Hay, M.P., Targeting hypoxia in cancer therapy. Nat. Rev. Cancer 11 (2011), 393–410.
59. [59] Brown, J.M., Hypoxic cytotoxic agents: a new approach to cancer chemotherapy. Drug Resist. Updat 3 (2000), 7–13.
60. [60] Iyer, V., Szybalski, W., Mitomycins and porfiromycin: chemical mechanism of activation and cross-linking of DNA. Science 145 (1964), 55–58.
61. [61] Rockwell, S., Kennedy, K.A., Sartorelli, A.C., Mitomycin-C as a prototype bioreductive alkylating agent: in vitro studies of metabolism and cytotoxicity. Int. J. Radiat. Oncol. Biol. Phys 8 (1982), 753–755.
62. [62] Haffty, B.G., Son, Y.H., Sasaki, C.T., Papac, R., Fischer, D., Rockwell, S., et al. Mitomycin C as an adjunct to postoperative radiation therapy in squamous cell carcinoma of the head and neck: results from two randomized clinical trials. Int. J. Radiat. Oncol. Biol. Phys 27 (1993), 241–250.
63. [63] Brown, J.M., Tumor hypoxia in cancer therapy. Methods Enzymol 435 (2007), 295–321.
64. [64] Talks, K.L., Turley, H., Gatter, K.C., Maxwell, P.H., Pugh, C.W., Ratcliffe, P.J., et al. The expression and distribution of the hypoxia-inducible factors HIF-1α and HIF-2α in normal human tissues, cancers, and tumor-associated macrophages. AM J. Pathol 157 (2000), 411–421.
65. [65] Negus, R., Turner, L., Burke, F., Balkwill, F.R., Hypoxia down-regulates MCP-1 expression: implications for macrophage distribution in tumors. J. Leukoc. Biol 63 (1998), 758–765.
66. [66] Bingle, L., Brown, N., Lewis, C., The role of tumour-associated macrophages in tumour progression: implications for new anticancer therapies. J. Pathol 196 (2002), 254–265.
67. [67] Griffiths, L., Binley, K., Iqball, S., Kan, O., Maxwell, P., Ratcliffe, P., et al. The macrophage-a novel system to deliver gene therapy to pathological hypoxia. Gene Ther 7 (2000), 255–262.
68. [68] Fox, M., Lemmon, M., Mauchline, M., Davis, T., Giaccia, A., Minton, N., et al. Anaerobic bacteria as a delivery system for cancer gene therapy: in vitro activation of 5-fluorocytosine by genetically engineered clostridia. Gene Ther 3 (1996), 173–178.
69. [69] Liu, S., Xu, X., Zeng, X., Li, L., Chen, Q., Li, J., Tumor-targeting bacterial therapy: a potential treatment for oral cancer (Review). Oncol. Lett 8 (2014), 2359–2366.
70. [70] Malmgren, R.A., Flanigan, C.C., Localization of the vegetative form of Clostridium tetani in mouse tumors following intravenous spore administration. Cancer Res 15 (1955), 473–478.
71. [71] Moese, J., Moese, G., Oncolysis by clostridia. I. Activity of Clostridium butyricum (M-55) and other nonpathogenic clostridia against the Ehrlich carcinoma. Cancer Res 24 (1964), 212–216.
72. [72] Liu, S., Minton, N., Giaccia, A., Brown, J., Anticancer efficacy of systemically delivered anaerobic bacteria as gene therapy vectors targeting tumor hypoxia/necrosis. Gene Ther 9 (2002), 291–296.
73. [73] Zhao, L., Ching, L., Kestell, P., Baguley, B., The antitumour activity of 5, 6-dimethylxanthenone-4-acetic acid (DMXAA) in TNF receptor-1 knockout mice. Br. J. Cancer 87 (2002), 465–470.
74. [74] Dang, L.H., Bettegowda, C., Huso, D.L., Kinzler, K.W., Vogelstein, B., Combination bacteriolytic therapy for the treatment of experimental tumors. PNAS 98 (2001), 15155–15160.
75. [75] Matsumura, Y., Maeda, H., A new concept for macromolecular therapeutics in cancer chemotherapy: mechanism of tumoritropic accumulation of proteins and the antitumor agent smancs. Cancer Res 46 (1986), 6387–6392.
76. [76] Maeda, H., The enhanced permeability and retention (EPR) effect in tumor vasculature: the key role of tumor-selective macromolecular drug targeting. Adv. Enzyme Regul 41 (2001), 189–207.
77. [77] Seki, T., Fang, J., Maeda, H., Tumor-targeted macromolecular drug delivery based on the enhanced permeability and retention effect in solid tumor. Pharmaceutical Perspectives of Cancer Therapeutics, 2009, Springer, 93–120.
78. [78] Maeda, H., Bharate, G., Daruwalla, J., Polymeric drugs for efficient tumor-targeted drug delivery based on EPR-effect. Eur. J. Pharm. Biopharm 71 (2009), 409–419.
79. [79] Maeda, H., Greish, K., Fang, J., The EPR effect and polymeric drugs: a paradigm shift for cancer chemotherapy in the 21st century. Polymer Therapeutics II, 2006, Springer, 103–121.
80. [80] Iyer, A.K., Khaled, G., Fang, J., Maeda, H., Exploiting the enhanced permeability and retention effect for tumor targeting. Drug Discov. Today 11 (2006), 812–818.
81. [81] Noguchi, Y., Wu, J., Duncan, R., Strohalm, J., Ulbrich, K., Akaike, T., et al. Early phase tumor accumulation of macromolecules: a great difference in clearance rate between tumor and normal tissues. Jpn J. Cancer Res 89 (1998), 307–314.
82. [82] Vicent, M.J., Ringsdorf, H., Duncan, R., Polymer therapeutics: clinical applications and challenges for development. Adv. Drug Deliv. Rev 61 (2009), 1117–1120.
83. [83] Duncan, R., The dawning era of polymer therapeutics. Nat. Rev. Drug Discov 2 (2003), 347–360.
84. [84] Robey, I.F., Baggett, B.K., Kirkpatrick, N.D., Roe, D.J., Dosescu, J., Sloane, B.F., et al. Bicarbonate increases tumor pH and inhibits spontaneous metastases. Cancer Res 69 (2009), 2260–2268.
85. [85] Nagamitsu, A., Greish, K., Maeda, H., Elevating blood pressure as a strategy to increase tumor-targeted delivery of macromolecular drug SMANCS: cases of advanced solid tumors. Jpn J. Clin. Oncol, 2009 hyp074.
86. [86] Li, C., Miyamoto, Y., Kojima, Y., Maeda, H., Augmentation of tumour delivery of macromolecular drugs with reduced bone marrow delivery by elevating blood pressure. Br. J. Cancer, 67, 1993, 975.
87. [87] Kojima, H., Urano, Y., Kikuchi, K., Higuchi, T., Hirata, Y., Nagano, T., Fluorescent indicators for imaging nitric oxide production. Angew. Chem. Int. Ed. Engl 38 (1999), 3209–3212.
88. [88] Seki, T., Fang, J., Maeda, H., Enhanced delivery of macromolecular antitumor drugs to tumors by nitroglycerin application. Cancer Sci 100 (2009), 2426–2430.
89. [89] Rubinsky, B., Irreversible Electroporation. 2009, Springer Science & Business Media.
90. [90] Davalos, R.V., Mir, L., Rubinsky, B., Tissue ablation with irreversible electroporation. Ann. Biomed. Eng 33 (2005), 223–231.
91. [91] Arena, C.B., Szot, C.S., Garcia, P.A., Rylander, M.N., Davalos, R.V., A three-dimensional in vitro tumor platform for modeling therapeutic irreversible electroporation. Biophys. J. 103 (2012), 2033–2042.
92. [92] Ellis, T.L., Garcia, P.A., Rossmeisl, J.H. Jr., Henao-Guerrero, N., Robertson, J., Davalos, R.V., Nonthermal irreversible electroporation for intracranial surgical applications: laboratory investigation. J. Neurosurg 114 (2011), 681–688.
93. [93] Neal, R.E., Millar, J.L., Kavnoudias, H., Royce, P., Rosenfeldt, F., Pham, A., et al. In vivo characterization and numerical simulation of prostate properties for non-thermal irreversible electroporation ablation. Prostate 74 (2014), 458–468.
94. [94] Garcia, P.A., Rossmeisl, J.H. Jr., Neal, R.E. II, Ellis, T.L., Olson, J.D., Henao-Guerrero, N., et al. Intracranial nonthermal irreversible electroporation: in vivo analysis. J. Membr. Biol 236 (2010), 127–136.
95. [95] Chen, J., Zheng, Y., Tan, Q., Shojaei-Baghini, E., Zhang, Y.L., Li, J., et al. Classification of cell types using a microfluidic device for mechanical and electrical measurement on single cells. Lab Chip 11 (2011), 3174–3181.
96. [96] Shafiee, H., Sano, M.B., Henslee, E.A., Caldwell, J.L., Davalos, R.V., Selective isolation of live/dead cells using contactless dielectrophoresis (cDEP). Lab Chip 10 (2010), 438–445.
97. [97] Salmanzadeh, A., Romero, L., Shafiee, H., Gallo-Villanueva, R.C., Stremler, M.A., Cramer, S.D., et al. Isolation of prostate tumor initiating cells (TICs) through their dielectrophoretic signature. Lab Chip 12 (2012), 182–189.
98. [98] Agarwal, A., Zudans, I., Weber, E.A., Olofsson, J., Orwar, O., Weber, S.G., Effect of cell size and shape on single-cell electroporation. Anal. Chem 79 (2007), 3589–3596.
99. [99] Arena, C.B., Sano, M.B., Rossmeisl, J.H., Caldwell, J.L., Garcia, P.A., Rylander, M.N., et al. High-frequency irreversible electroporation (H-FIRE) for non-thermal ablation without muscle contraction. Biomed. Eng. Online, 10, 2011, 102.
100. [100] Sano, M.B., Arena, C.B., DeWitt, M.R., Saur, D., Davalos, R.V., In-vitro bipolar nano-and microsecond electro-pulse bursts for irreversible electroporation therapies. Bioelectrochemistry 100 (2014), 69–79.
101. [101] Ivey, J.W., Latouche, E.L., Sano, M.B., Davalos, R.V., Verbridge, S.S., Targeted cellular ablation based on the morphology of malignant cells. Scientific Reports, 2015.
102. [102] Bhonsle, S.P., Arena, C.B., Sweeney, D.C., Davalos, R.V., Mitigation of impedance changes due to electroporation therapy using bursts of high-frequency bipolar pulses. Biomed. Eng. Online, 14, 2015, S3.
103. [103] Davalos, R.V., Otten, D.M., Mir, L.M., Rubinsky, B., Electrical impedance tomography for imaging tissue electroporation. IEEE Trans. Biomed. Eng 51 (2004), 761–767.
104. [104] Bonakdar, M., Latouche, E.L., Mahajan, R.L., Davalos, R.V., The feasibility of a smart surgical probe for verification of ire treatments using electrical impedance spectroscopy. IEEE Trans. Biomed Eng 62 (2015), 2674–2684.
105. [105] Garon, E.B., Sawcer, D., Vernier, P.T., Tang, T., Sun, Y., Marcu, L., et al. In vitro and in vivo evaluation and a case report of intense nanosecond pulsed electric field as a local therapy for human malignancies. Int. J. Cancer 121 (2007), 675–682.
106. [106] Chen, N., Schoenbach, K.H., Kolb, J.F., Swanson, R.J., Garner, A.L., Yang, J., et al. Leukemic cell intracellular responses to nanosecond electric fields. Biochem. Biophys. Res. Commun 317 (2004), 421–427.
107. [107] Yang, W., Wu, Y., Yin, D., Koeffler, H., Sawcer, D., Vernier, P., et al. Differential sensitivities of malignant and normal skin cells to nanosecond pulsed electric fields. Technol. Cancer Res. Treat 10 (2011), 281–286.
108. [108] Merla, C., Paffi, A., Apollonio, F., Leveque, P., d'Inzeo, G., Liberti, M., Microdosimetry for nanosecond pulsed electric field applications: a parametric study for a single cell. IEEE Trans. Biomed Eng 58 (2011), 1294–1302.
109. [109] Kirson, E.D., Gurvich, Z., Schneiderman, R., Dekel, E., Itzhaki, A., Wasserman, Y., et al. Disruption of cancer cell replication by alternating electric fields. Cancer Res 64 (2004), 3288–3295.
110. [110] Gera, N., Yang, A., Holtzman, T., Lee, S., Wong, E., Swanson, K., Tumor treating fields perturb the localization of septins and cause aberrant mitotic exit. PLoS ONE, 10, 2015, e0125269.
111. [111] Davies, A.M., Weinberg, U., Palti, Y., Tumor treating fields: a new frontier in cancer therapy. Ann. N. Y. Acad. Sci 1291 (2013), 86–95.
112. [112] Robins, H.I., Steeves, R.A., Clark, A.W., Martin, P.A., Miller, K., Dennis, W.H., Differential sensitivity of AKR murine leukemia and normal bone marrow cells to hyperthermia. Cancer Res 43 (1983), 4951–4955.
113. [113] Gerweck, L.E., Modification of cell lethality at elevated temperatures the pH effect. Radiat. Res 70 (1977), 224–235.
114. [114] Song, C.W., Park, H., Ross, B.D., Intra-and Extracellular pH in Solid Tumors, Antiangiogenic Agents in Cancer Therapy. 1999, Springer, 51–64.
115. [115] Song, C.W., Lyons, J.C., Griffin, R.J., Makepeace, C.M., Cragoe, E.J., Increase in thermosensitivity of tumor cells by lowering intracellular pH. Cancer Res 53 (1993), 1599–1601.
116. [116] Kitai, R., Kabuto, M., Kubota, T., Kobayashi, H., Matsumoto, H., Hayashi, S., et al. Sensitization to hyperthermia by intracellular acidification. J. Neurooncol 39 (1998), 197–203.
117. [117] Yamagata, M., Tannock, I., The chronic administration of drugs that inhibit the regulation of intracellular pH: in vitro and anti-tumour effects. Br. J. Cancer, 73, 1996, 1328.
118. [118] Lyons, J.C., Ross, B.D., Song, C.W., Enhancement of hyperthermia effect in vivo by amiloride and DIDS. Int. J. Radiat. Oncol. Biol. Phys 25 (1993), 95–103.
119. [119] Ahmed, M., Liu, Z., Afzal, K.S., Weeks, D., Lobo, S.M., Kruskal, J.B., et al. Radiofrequency ablation: effect of surrounding tissue composition on coagulation necrosis in a Canine Tumor Model 1. Radiology 230 (2004), 761–767.
120. [120] Goldberg, S.N., Radiofrequency tumor ablation: principles and techniques. Eur. J. Ultrasound 13 (2001), 129–147.
121. [121] LeVeen, H.H., Wapnick, S., Piccone, V., Falk, G., Ahmed, N., Tumor eradication by radiofrequency therapy: response in 21 patients. JAMA 235 (1976), 2198–2200.
122. [122] Liu, Z., Ahmed, M., Weinstein, Y., Yi, M., Mahajan, R.L., Goldberg, S.N., Characterization of the RF ablation-induced ‘oven effect’: the importance of background tissue thermal conductivity on tissue heating. Int. J. Hyperthermia 22 (2006), 327–342.
123. [123] Livraghi, T., Goldberg, S., Meloni, F., Solbiati, L., Gazelle, G., Hepatocellular carcinoma: comparison of efficacy between percutaneous ethanol instillation and radiofrequency. Radiology 210 (1999), 655–663.
124. [124] Liu, Z., Ahmed, M., Sabir, A., Humphries, S., Goldberg, S., Computer modeling of the effect of perfusion on heating patterns in radiofrequency tumor ablation. Int. J. Hyperthermia 23 (2007), 49–58.
125. [125] Ahmed, M., Liu, Z., Humphries, S., Nahum Goldberg, S., Computer modeling of the combined effects of perfusion, electrical conductivity, and thermal conductivity on tissue heating patterns in radiofrequency tumor ablation. Int. J. Hyperthermia 24 (2008), 577–588.
126. [126] Lagendijk, J.J., Hofman, P., Schipper, J., Perfusion analyses in advanced breast carcinoma during hyperthermia. Int. J. Hyperthermia, 4, 1988, 479.
127. [127] Song, C.W., Rhee, J.G., Levitt, S.H., Blood flow in normal tissues and tumors during hyperthermia. J. Natl Cancer Inst 64 (1980), 119–124.
128. [128] ter Haar, G., Coussios, C., High intensity focused ultrasound: physical principles and devices. Int. J. Hyperthermia 23 (2007), 89–104.
129. [129] Hoyt, K., Castaneda, B., Zhang, M., Nigwekar, P., di Sant'Agnese, P.A., Joseph, J.V., et al. Tissue elasticity properties as biomarkers for prostate cancer. Cancer Biomark, 4, 2008, 213.
130. [130] Garteiser, P., Doblas, S., Daire, J.-L., Wagner, M., Leitao, H., Vilgrain, V., et al. MR elastography of liver tumours: value of viscoelastic properties for tumour characterisation. Eur. Radiol 22 (2012), 2169–2177.
131. [131] Xu, J., Bigelow, T.A., Experimental investigation of the effect of stiffness, exposure time and scan direction on the dimension of ultrasound histotripsy lesions. Ultrasound Med. Biol 37 (2011), 1865–1873.
132. [132] Hoogenboom, M., Eikelenboom, D., den Brok, M.H., Heerschap, A., Fütterer, J.J., Adema, G.J., Mechanical high-intensity focused ultrasound destruction of soft tissue: working mechanisms and physiologic effects. Ultrasound Med. Biol 41 (2015), 1500–1517.
133. [133] Bae, Y.H., Park, K., Targeted drug delivery to tumors: myths, reality and possibility. J. Control. Release 153 (2011), 198–205.
134. [134] Byrne, J.D., Jajja, M.N.R., O'Neill, A.T., Bickford, L.R., Keeler, A.W., Hyder, N., et al. Local iontophoretic administration of cytotoxic therapies to solid tumors. Sci. Transl. Med, 7, 2015, 273ra214.
135. [135] Gothelf, A., Mir, L.M., Gehl, J., Electrochemotherapy: results of cancer treatment using enhanced delivery of bleomycin by electroporation. Cancer Treat. Rev 29 (2003), 371–387.
136. [136] Xia, C., Meng, Q., Liu, L.-Z., Rojanasakul, Y., Wang, X.-R., Jiang, B.-H., Reactive oxygen species regulate angiogenesis and tumor growth through vascular endothelial growth factor. Cancer Res 67 (2007), 10823–10830.
137. [137] Sayin, V.I., Ibrahim, M.X., Larsson, E., Nilsson, J.A., Lindahl, P., Bergo, M.O., Antioxidants accelerate lung cancer progression in mice. Science Translational Medicine, 6, 2014, 221ra215.
138. [138] Ebos, J.M.L., Kerbel, R.S., Antiangiogenic therapy: impact on invasion, disease progression, and metastasis. Nat. Rev. Clin. Oncol 8 (2011), 210–221.
139. [139] Rapisarda, A., Melillo, G., Role of the hypoxic tumor microenvironment in the resistance to anti-angiogenic therapies. Drug Resist. Updat 12 (2009), 74–80.
140. [140] Pàez-Ribes, M., Allen, E., Hudock, J., Takeda, T., Okuyama, H., Viñals, F., et al. Antiangiogenic therapy elicits malignant progression of tumors to increased local invasion and distant metastasis. Cancer Cell 15 (2009), 220–231.
141. [141] Keith, B., Simon, M.C., Hypoxia inducible factors, stem cells and cancer. Cell 129 (2007), 465–472.
142. [142] Kirson, E.D., Dbalý, V., Tovaryš, F., Vymazal, J., Soustiel, J.F., Itzhaki, A., et al. Alternating electric fields arrest cell proliferation in animal tumor models and human brain tumors. PNAS 104 (2007), 10152–10157.
143. [143] Carey, R., Holland, J., Whang, H., Neter, E., Bryant, B., Clostridial oncolysis in man. Eur. J. Cancer 3:1967 (1965), 37–46.
144. [144] Toso, J.F., Gill, V.J., Hwu, P., Marincola, F.M., Restifo, N.P., Schwartzentruber, D.J., et al. Phase I study of the intravenous administration of attenuated Salmonella typhimurium to patients with metastatic melanoma. J. Clin. Oncol 20 (2002), 142–152.
145. [145] Binley, K., Askham, Z., Martin, L., Spearman, H., Day, D., Kingsman, S., et al. Hypoxia-mediated tumour targeting. Gene Ther 10 (2003), 540–549.
146. [146] Goldberg, S.N., Ahmed, M., Gazelle, G.S., Kruskal, J.B., Huertas, J.C., Halpern, E.F., et al. Radio-frequency thermal ablation with NaCl solution injection: effect of electrical conductivity on tissue heating and coagulation – phantom and porcine liver study 1. Radiology 219 (2001), 157–165.
147. [147] Edd, J.F., Davalos, R.V., Mathematical modeling of irreversible electroporation for treatment planning. Technol. Cancer Res. Treat 6 (2007), 275–286.
148. [148] DeBruin, K.A., Krassowska, W., Modeling electroporation in a Single cell. I. effects of field strength and rest potential. Biophys. J. 77 (1999), 1213–1224.