Prodding the beast: Assessing the impact of treatment-induced metastasis

Cancer Research

Volumn 75, Issue 17, 2015, Pages 3427-3435

  Ebos, John M L ^a  

^a ROSWELL PARK CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOGENESIS INHIBITOR; BEVACIZUMAB; CILENGITIDE; SUNITINIB;

ANTIANGIOGENIC ACTIVITY; BREAST CARCINOMA; CANCER CHEMOTHERAPY; CANCER RADIOTHERAPY; CLINICAL EFFECTIVENESS; COLON CANCER; COLORECTAL CARCINOMA; HUMAN; KIDNEY CARCINOMA; MALIGNANT NEOPLASTIC DISEASE; METASTASIS; METASTASIS POTENTIAL; NONHUMAN; OVERALL SURVIVAL; PATHOGENESIS; PRIORITY JOURNAL; REVIEW; TREATMENT INDUCED METASTASIS; TRIPLE NEGATIVE BREAST CANCER; TUMOR INVASION; TUMOR MICROENVIRONMENT; DNA DAMAGE; DRUG EFFECTS; NEOPLASMS, SECOND PRIMARY; PATHOLOGY; RADIATION RESPONSE; SECONDARY;

ANGIOGENESIS INHIBITORS; DNA DAMAGE; HUMANS; NEOPLASMS, SECOND PRIMARY; TUMOR MICROENVIRONMENT;

EID: 84942879643     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-15-0308     Document Type: Review

References (152)

1. Ruegg C, Monnier Y, Kuonen F, Imaizumi N. Radiation-induced modifications of the tumor microenvironment promote metastasis. Bull Cancer 2011;98:47-57.
2. von Essen CF. Radiation enhancement of metastasis: a review. Clin Exp Metastasis 1991;9:77-104.
3. McAllister SS, Weinberg RA. The tumour-induced systemic environment as a critical regulator of cancer progression and metastasis. Nat Cell Biol 2014;16:717-27.
4. Marcucci F, Bellone M, Caserta CA, Corti A. Pushing tumor cells towards a malignant phenotype: stimuli from the microenvironment, intercellular communications and alternative roads. Int J Cancer 2014;135:1265-76.
5. Talmadge JE, Singh RK, Fidler IJ, Raz A. Murine models to evaluate novel and conventional therapeutic strategies for cancer. Am J Pathol 2007;170: 793-804.
6. Teicher BA. Tumor models for efficacy determination. Mol Cancer Ther 2006;5:2435-43.
7. Francia G, Cruz-Munoz W, Man S, Xu P, Kerbel RS. Mouse models of advanced spontaneous metastasis for experimental therapeutics. Nat Rev Cancer 2011;11:135-41.
8. Nguyen DX, Bos PD, Massague J.Metastasis: from dissemination to organspecific colonization. Nat Rev Cancer 2009;9:274-84.
9. Hoffman RM. Imaging cancer dynamics in vivo at the tumor and cellular level with fluorescent proteins. Clin Exp Metastasis 2009;26:345-55.
10. Wilmanns C, Fan D, O'Brian CA, Bucana CD, Fidler IJ. Orthotopic and ectopic organ environments differentially influence the sensitivity of murine colon carcinoma cells to doxorubicin and 5-fluorouracil. Int J Cancer 1992;52:98-104.
11. Day CP, Carter J, Bonomi C, Hollingshead M, Merlino G. Preclinical therapeutic response of residual metastatic disease is distinct from its primary tumor of origin. Int J Cancer 2012;130:190-9.
12. Steeg PS, Theodorescu D. Metastasis: a therapeutic target for cancer. Nat Clin Pract Oncol 2008;5:206-19.
13. Bernier J, Hall EJ, Giaccia A. Radiation oncology: a century of achievements. Nat Rev Cancer 2004;4:737-47.
14. Kaplan HS, Murphy ED. The effect of local roentgen irradiation on the biological behavior of a transplantable mouse carcinoma; increased frequency of pulmonary metastasis. J Natl Cancer Inst 1949;9:407-13.
15. Brown JM,Marsa GW. Effect of dose fractionation on the enhancement by radiation or cyclophosphamide of artificial pulmonary metastases. Br J Cancer 1978;37:1020-5.
16. Kuonen F, Secondini C, Ruegg C. Molecular pathways: emerging pathways mediating growth, invasion, andmetastasis of tumors progressing in an irradiated microenvironment. Clin Cancer Res 2012;18:5196-202.
17. van den Brenk HA, Crowe MC, Stone MG. Reactions of the tumour bed to lethally irradiated tumour cells, and the Revesz effect. Br J Cancer 1977;36:94-104.
18. Mothersill C, Seymour CB. Radiation-induced bystander effects-implications for cancer. Nat Rev Cancer 2004;4:158-64.
19. Kaminski JM, Shinohara E, Summers JB, Niermann KJ, Morimoto A, Brousal J. The controversial abscopal effect. Cancer Treat Rev 2005;31: 159-72.
20. Wu YJ, Muldoon LL, Dickey DT, Lewin SJ, Varallyay CG, Neuwelt EA. Cyclophosphamide enhances human tumor growth in nude rat xenografted tumor models. Neoplasia 2009;11:187-95.
21. Yamauchi K, YangM, Hayashi K, Jiang P, Yamamoto N, Tsuchiya H, et al. Induction of cancer metastasis by cyclophosphamide pretreatment of host mice: an opposite effect of chemotherapy. Cancer Res 2008;68: 516-20.
22. Carmel RJ, Brown JM. The effect of cyclophosphamide and other drugs on the incidence of pulmonary metastases in mice. Cancer Res 1977;37: 145-51.
23. van Putten LM, Kram LK, van Dierendonck HH, Smink T, Fuzy M. Enhancement by drugs of metastatic lung nodule formation after intravenous tumour cell injection. Int J Cancer 1975;15:588-95.
24. Coffey JC, Wang JH, Smith MJ, Bouchier-Hayes D, Cotter TG, Redmond HP. Excisional surgery for cancer cure: therapy at a cost. Lancet Oncol 2003;4:760-8.
25. Paget S. The distribution of secondary growths in cancer of the breast. Lancet 1889;133:571-3.
26. Barcellos-Hoff MH. The potential influence of radiation-induced microenvironments in neoplastic progression. J Mammary Gland Biol Neoplasia 1998;3:165-75.
27. Sun Y, Nelson PS. Molecular pathways: involving microenvironment damage responses in cancer therapy resistance. Clin Cancer Res 2012;18: 4019-25.
28. Barcellos-Hoff MH, Park C, Wright EG. Radiation and the microenvironment-tumorigenesis and therapy. Nat Rev Cancer 2005;5:867-75.
29. Rodier F, Coppe JP, Patil CK, Hoeijmakers WA,Munoz DP, Raza SR, et al. Persistent DNA damage signalling triggers senescence-Associated inflammatory cytokine secretion. Nat Cell Biol 2009;11:973-9.
30. Coppe JP, Desprez PY, Krtolica A, Campisi J. The senescence-Associated secretory phenotype: the dark side of tumor suppression. Annu Rev Pathol 2010;5:99-118.
31. Pribluda A, Elyada E,Wiener Z, Hamza H, Goldstein RE, BitonM, et al. A senescence-inflammatory switch from cancer-inhibitory to cancer-promoting mechanism. Cancer Cell 2013;24:242-56.
32. Daenen LG, Roodhart JM, van Amersfoort M, Dehnad M, Roessingh W, Ulfman LH, et al. Chemotherapy enhances metastasis formation via VEGFR-1-expressing endothelial cells. Cancer Res 2011;71: 6976-85.
33. Sun Y, Campisi J, HiganoC, Beer TM, Porter P, Coleman I, et al. Treatmentinduced damage to the tumor microenvironment promotes prostate cancer therapy resistance through WNT16B. Nat Med 2012;18:1359-68.
34. Katz OB, Shaked Y. Host effects contributing to cancer therapy resistance. Drug Resist Updat 2015;19:33-42.
35. Daenen LG, Houthuijzen JM, Cirkel GA, Roodhart JM, Shaked Y, Voest EE. Treatment-induced host-mediated mechanisms reducing the efficacy of antitumor therapies. Oncogene 2014;33:1341-7.
36. Rofstad EK, Mathiesen B, Henriksen K, Kindem K, Galappathi K. The tumor bed effect: increased metastatic dissemination from hypoxiainduced up-regulation of metastasis-promoting gene products. Cancer Res 2005;65:2387-96.
37. Olson OC, Joyce JA.Microenvironment-mediated resistance to anticancer therapies. Cell Res 2013;23:179-81.
38. Jain RK. Antiangiogenesis strategies revisited: from starving tumors to alleviating hypoxia. Cancer Cell 2014;26:605-22.
39. Ebos JM, Kerbel RS. Antiangiogenic therapy: impact on invasion, disease progression, and metastasis. Nat Rev Clin Oncol 2011;8:210-21.
40. Ebos JM, Lee CR, Cruz-Munoz W, Bjarnason GA, Christensen JG, Kerbel RS. Accelerated metastasis after short-term treatment with a potent inhibitor of tumor angiogenesis. Cancer Cell 2009;15:232-9.
41. Paez-Ribes M, Allen E, Hudock J, Takeda T, Okuyama H, Vinals F, et al. Antiangiogenic therapy elicits malignant progression of tumors to increased local invasion and distant metastasis. Cancer Cell 2009;15: 220-31.
42. Mittal K, Ebos J, Rini B. Angiogenesis and the tumor microenvironment: vascular endothelial growth factor and beyond. Semin Oncol 2014; 41:235-51.
43. Cooke VG, LeBleu VS, Keskin D, Khan Z, O'Connell JT, Teng Y, et al. Pericyte depletion results in hypoxia-Associated epithelial-to-mesenchymal transition and metastasis mediated by met signaling pathway. Cancer Cell 2012;21:66-81.
44. Chung AS, Kowanetz M, Wu X, Zhuang G, Ngu H, Finkle D, et al. Differential drug class-specificmetastatic effects following treatment with a panel of angiogenesis inhibitors. J Pathol 2012;227:404-16.
45. Welti JC, Powles T, Foo S, Gourlaouen M, Preece N, Foster J, et al. Contrasting effects of sunitinib within in vivo models of metastasis. Angiogenesis 2012;15:623-41.
46. Lu KV, Chang JP, Parachoniak CA, Pandika MM, Aghi MK, Meyronet D, et al. VEGF inhibits tumor cell invasion and mesenchymal transition through a MET/VEGFR2 complex. Cancer Cell 2012;22:21-35.
47. Sennino B, Ishiguro-Oonuma T, Wei Y, Naylor RM, Williamson CW, Bhagwandin V, et al. Suppression of tumor invasion and metastasis by concurrent inhibition of c-Met and VEGF signaling in pancreatic neuroendocrine tumors. Cancer Discov 2012;2:270-87.
48. Shojaei F, Simmons BH, Lee JH, Lappin PB, Christensen JG. HGF/c-Met pathway is one of the mediators of sunitinib-induced tumor cell typedependent metastasis. Cancer Lett 2012;320:48-55.
49. Yakes FM, Chen J, Tan J, Yamaguchi K, Shi Y, Yu P, et al. Cabozantinib (XL184), a novel MET and VEGFR2 inhibitor, simultaneously suppresses metastasis, angiogenesis, and tumor growth. Mol Cancer Ther 2011;10: 2298-308.
50. Sennino B, Ishiguro-Oonuma T, Schriver BJ, Christensen JG, McDonald DM. Inhibition of c-Met reduces lymphatic metastasis in RIP-Tag2 transgenic mice. Cancer Res 2013;73:3692-703.
51. Xu Y, Li Q, Li XY, Yang QY, Xu WW, Liu GL. Short-term anti-vascular endothelial growth factor treatment elicits vasculogenic mimicry formation of tumors to accelerate metastasis. J Exp Clin Cancer Res 2012;31:16.
52. Zhang D, Sun B, Zhao X,Ma Y, Ji R,GuQ, et al. Twist1 expression induced by sunitinib accelerates tumor cell vasculogenic mimicry by increasing the population of CD133+ cells in triple-negative breast cancer. Mol Cancer 2014;13:207.
53. Takeda T, Okuyama H, Nishizawa Y, Tomita S, Inoue M. Hypoxia inducible factor-1alpha is necessary for invasive phenotype in Vegfdeleted islet cell tumors. Sci Rep 2012;2:494.
54. Sounni NE, Cimino J, Blacher S, Primac I, Truong A, Mazzucchelli G, et al. Blocking lipid synthesis overcomes tumor regrowth and metastasis after antiangiogenic therapy withdrawal. Cell Metab 2014;20:280-94.
55. Aguilera KY, Rivera LB, Hur H, Carbon JG, Toombs JE, Goldstein CD, et al. Collagen signaling enhances tumor progression after anti-VEGF therapy in a murine model of pancreatic ductal adenocarcinoma. Cancer Res 2014;74:1032-44.
56. Zhu XD, Sun HC, Xu HX, Kong LQ, Chai ZT, Lu L, et al. Antiangiogenic therapy promoted metastasis of hepatocellular carcinoma by suppressing host-derived interleukin-12b in mouse models. Angiogenesis 2013;16: 809-20.
57. Grepin R, Guyot M, Jacquin M, Durivault J, Chamorey E, Sudaka A, et al. Acceleration of clear cell renal cell carcinoma growth in mice following bevacizumab/Avastin treatment: the role of CXCL cytokines. Oncogene 2012;31:1683-94.
58. Zhang W, Sun HC, Wang WQ, Zhang QB, Zhuang PY, Xiong YQ, et al. Sorafenib down-regulates expression of HTATIP2 to promote invasiveness and metastasis of orthotopic hepatocellular carcinoma tumors in mice. Gastroenterology 2012;143:1641-9.
59. Lu L, Sun HC, Zhang W, Chai ZT, Zhu XD, Kong LQ, et al. Aspirin minimized the pro-metastasis effect of sorafenib and improved survival by up-regulating HTATIP2 in hepatocellular carcinoma. PLoS ONE 2013;8:e65023.
60. Hammond E, Brandt R, Dredge K. PG545, a heparan sulfate mimetic, reduces heparanase expression in vivo, blocks spontaneous metastases and enhances overall survival in the 4T1 breast carcinoma model. PLoS ONE 2012;7:e52175.
61. Maione F, Capano S, Regano D, Zentilin L, Giacca M, Casanovas O, et al. Semaphorin 3A overcomes cancer hypoxia and metastatic dissemination induced by antiangiogenic treatment in mice. J Clin Invest 2012;122: 1832-48.
62. Casazza A, Kigel B, Maione F, Capparuccia L, Kessler O, Giraudo E, et al. Tumour growth inhibition and anti-metastatic activity of a mutated furinresistant Semaphorin 3E isoform. EMBO Mol Med 2012;4:234-50.
63. Zhang QB, Sun HC, Zhang KZ, Jia QA, Bu Y, Wang M, et al. Suppression of natural killer cells by sorafenib contributes to prometastatic effects in hepatocellular carcinoma. PLoS ONE 2013;8:e55945.
64. He S, Lamers GE, Beenakker JW, Cui C, Ghotra VP, Danen EH, et al. Neutrophil-mediated experimental metastasis is enhanced by VEGFR inhibition in a zebrafish xenograft model. J Pathol 2012;227:431-45.
65. Conley SJ, Gheordunescu E, Kakarala P, Newman B, Korkaya H, Heath AN, et al. Antiangiogenic agents increase breast cancer stem cells via the generation of tumor hypoxia. Proc Natl Acad Sci U S A 2012;109:2784-9.
66. Singh M, Couto SS, Forrest WF, Lima A, Cheng JH, Molina R, et al. Anti-VEGF antibody therapy does not promote metastasis in genetically engineered mouse tumour models. J Pathol 2012;227:417-30.
67. Ebos JM, Pili R. Mind the Gap: potential for rebounds during antiangiogenic treatment breaks. Clin Cancer Res 2012;18:3719-21.
68. Mancuso MR, Davis R, Norberg SM, O'Brien S, Sennino B, Nakahara T, et al. Rapid vascular regrowth in tumors after reversal of VEGF inhibition. J Clin Invest 2006;116:2610-21.
69. Griffioen AW, Mans LA, de Graaf AM, Nowak-Sliwinska P, de Hoog CL, de Jong TA, et al. Rapid angiogenesis onset after discontinuation of sunitinib treatment of renal cell carcinoma patients. Clin Cancer Res 2012;18: 3961-71.
70. Qian BZ, Li J, Zhang H, Kitamura T, Zhang J, Campion LR, et al. CCL2 recruits inflammatory monocytes to facilitate breast-tumour metastasis. Nature 2011;475:222-5.
71. Bonapace L, Coissieux MM, Wyckoff J, Mertz KD, Varga Z, Junt T, et al. Cessation of CCL2 inhibition accelerates breast cancer metastasis by promoting angiogenesis. Nature 2014;515:130-3.
72. Keklikoglou I, De PalmaM. Cancer: metastasis risk after anti-macrophage therapy. Nature 2014;515:46-7.
73. Miles D, Harbeck N, Escudier B, Hurwitz H, Saltz L, Van Cutsem E, et al. Disease course patterns after discontinuation of bevacizumab: pooled analysis of randomized phase III trials. J Clin Oncol 2010;29:83-8.
74. Blagoev KB, Wilkerson J, Stein WD, Motzer RJ, Bates SE, Fojo AT. Sunitinib does not accelerate tumor growth in patients with metastatic renal cell carcinoma. Cell Rep 2013;3:277-81.
75. Eisele G, Wick A, Eisele AC, Clement PM, Tonn J, Tabatabai G, et al. Cilengitide treatment of newly diagnosed glioblastoma patients does not alter patterns of progression. J Neurooncol 2014;117:141-5.
76. Reynolds AR, Hart IR, Watson AR, Welti JC, Silva RG, Robinson SD, et al. Stimulation of tumor growth and angiogenesis by low concentrations of RGD-mimetic integrin inhibitors. Nat Med 2009;15:392-400.
77. Das Thakur M, Pryer NK, Singh M. Mouse tumour models to guide drug development and identify resistance mechanisms. J Pathol 2014;232: 103-11.
78. deGramont A, Van CE, Schmoll HJ, Tabernero J, Clarke S, Moore MJ, et al. Bevacizumab plus oxaliplatin-based chemotherapy as adjuvant treatment for colon cancer (AVANT): a phase 3 randomised controlled trial. Lancet Oncol 2012;13:1225-33.
79. Cameron D, Brown J, Dent R, Jackisch C, Mackey J, Pivot X, et al. Adjuvant bevacizumab-containing therapy in triple-negative breast cancer (BEATRICE): primary results of a randomised, phase 3 trial. Lancet Oncol 2013;14:933-42.
80. Haas NB, Manola J, Uzzo RG, Atkins MB, Wilding G, Pins M, et al. Initial results from ASSURE (E2805): Adjuvant sorafenib or sunitinib for unfavorable renal carcinoma, an ECOG-ACRIN-led, NCTN phase III trial. J Clin Oncol 33, 2015 (suppl 7; abstr 403).
81. Bruix J. TT, Mazzaferro V, Chau G, Yang J, Kudo M, Cai J, et al. STORM: A phase III randomized, double-blind, placebo-controlled trial of adjuvant sorafenib after resection or ablation to prevent recurrence of hepatocellular carcinoma (HCC). J Clin Oncol 32, 2014 (15Suppl):4006.
82. Oyan B. Why do targeted agents not work in the adjuvant setting in colon cancer Expert Rev Anticancer Ther 2012;12:1337-45.
83. McMillan TJ, Hart IR. Enhanced experimental metastatic capacity of a murine melanoma following pre-treatment with anticancer drugs. Clin Exp Metastasis 1986;4:285-92.
84. Xiong W, Ren ZG, Qiu SJ, Sun HC, Wang L, Liu BB, et al. Residual hepatocellular carcinoma after oxaliplatin treatment has increased metastatic potential in a nude mouse model and is attenuated by Songyou Yin. BMC Cancer 2010;10:219.
85. McMillan TJ, Rao J, Hart IR. Enhancement of experimental metastasis by pretreatment of tumour cells with hydroxyurea. Int J Cancer 1986; 38:61-5.
86. Steel GG, Adams K. Enhancement by cytotoxic agents of artificial pulmonary metastasis. Br J Cancer 1977;36:653-8.
87. Vollmer TL, Conley FK. Effect of cyclophosphamide on survival of mice and incidence of metastatic tumor following intravenous and intracardial inoculation of tumor cells. Cancer Res 1984;44:3902-6.
88. Lev DC, Onn A, Melinkova VO, Miller C, Stone V, Ruiz M, et al. Exposure of melanoma cells to dacarbazine results in enhanced tumor growth and metastasis in vivo. J Clin Oncol 2004;22:2092-100.
89. Brown JM, Parker ET. Host treatments affecting artificial pulmonary metastases: interpretation of loss of radioactively labelled cells from lungs. Br J Cancer 1979;40:677-88.
90. Biswas S, Guix M, Rinehart C, Dugger TC, Chytil A, Moses HL, et al. Inhibition of TGF-beta with neutralizing antibodies prevents radiationinduced acceleration of metastatic cancer progression. J Clin Invest 2007;117:1305-13.
91. Orr FW, Adamson IYR, Young L. Promotion of pulmonary metastasis in mice by bleomycin-induced endothelial injury. Cancer Res 1986;46: 891-7.
92. Dubravsky NB, Dubrawsky C, Jampolis S, Mason K, Hunter N, Withers HR. Long-term effects of pulmonary damage in mice on lung weight, compliance, hydroxyproline content and formation of metastases. Br J Radiol 1981;54:1075-80.
93. Gingis-Velitski S, Loven D, Benayoun L, Munster M, Bril R, Voloshin T, et al. Host response to short-term, single-Agent chemotherapy induces matrix metalloproteinase-9 expression and accelerates metastasis inmice. Cancer Res 2011;71:6986-96.
94. Man S, Zhang Y, Gao W, Yan L, Ma C. Cyclophosphamide promotes pulmonary metastasis on mouse lung adenocarcinoma. Clin Exp Metastasis 2008;25:855-64.
95. Moore JV, Dixon B. Metastasis of a transplantable mammary tumour in rats treated with cyclophosphamide and/or irradiation. Br J Cancer 1977;36:221-6.
96. Withers HR, Milas L. Influence of preirradiation of lung on development of artificial pulmonary metastases of fibrosarcoma in mice. Cancer Res 1973;33:1931-6.
97. Brown JM. The effect of lung irradiation on the incidence of pulmonary metastases in mice. Br J Radiol 1973;46:613-8.
98. Dao TL, Yogo H. Enhancement of pulmonary metastases by x-irradiation in rats bearing mammary cancer. Cancer 1967;20:2020-5.
99. Peters LJ. Letter: the potentiating effect of prior local irradiation of the lungs on the development of pulmonary metastases. Br J Radiol 1974;47:827-9.
100. Peters LJ, Mason K, McBride WH, Patt YZ. Enhancement of lung colonyforming efficiency by local thoracic irradiation: interpretation of labeled cell studies. Radiology 1978;126:499-505.
101. HirataH, Tanaka K. Artificial metastases and decrease of fibrinolysis in the nude mouse lung after hemithoracic irradiation. Clin Exp Metastasis 1984;2:311-9.
102. Suzuki N. Spontaneous versus artificial lung metastasis: discrepant effect of whole-body irradiation in NFSA2ALM and NFSA1SLMtumor systems. J Natl Cancer Inst 1983;71:835-9.
103. Tanaka Y. Effect of lung irradiation on the incidence of pulmonary metastases and its mechanism. Acta Radiol Ther Phys Biol 1976;15: 142-8.
104. Thompson SC. Tumour colony growth in the irradiated mouse lung. Br J Cancer 1974;30:337-41.
105. Van den Brenk HA, Sharpington C. Effect of local x-irradiation of a primary sarcoma in the rat on dissemination and growth of metastases: dose-response characteristics. Br J Cancer 1971;25:812-30.
106. Milas L, Hunter N, Basic I, Withers HR. Protection by corynebacterium granulosum against radiation-induced enhancement of artificial pulmonary metastases of a murine fibrosarcoma. J Natl Cancer Inst 1974;52: 1875-80.
107. Van den Brenk HA, Kelly H. Stimulation of growth of metastases by local x-irradiation in kidney and liver. Br J Cancer 1973;28:349-53.
108. Van den Brenk HA, Burch WM, Orton C, Sharpington C. Stimulation of clonogenic growth of tumour cells and metastases in the lungs by local xradiation. Br J Cancer 1973;27:291-306.
109. Fidler IJ, Zeidman I. Enhancement of experimental metastasis by x-ray: a possible mechanism. J Med 1972;3:172-7.
110. Zeidman I, Fidler IJ. Effect of irradiation on experimental metastases via lymph and blood streams. J Med 1970;1:9-14.
111. Fisher ER, Fisher B. Effects of x-irradiation on parameters of tumor growth, histology, and ultrastructure. Cancer 1969;24:39-55.
112. Koike A, Nakazato H, Moore GE. The fate of Ehrlich cells injected into the portal system. Cancer 1963;16:716-20.
113. Sofia Vala I, Martins LR, Imaizumi N, Nunes RJ, Rino J, Kuonen F, et al. Low doses of ionizing radiation promote tumor growth and metastasis by enhancing angiogenesis. PLoS ONE 2010;5:e11222.
114. Kaae S. Metastatic frequency of spontaneous mammary carcinoma in mice following biopsy and following local roentgen irradiation. Cancer Res 1953;13:744-7.
115. Rappaport DS, Brown JM. Influence of localized preinoculation irradiation of the foot on lymphatic metastasis from a primary tumor growing in the foot. Radiat Res 1979;78:108-21.
116. Camphausen K, Moses MA, Beecken WD, Khan MK, Folkman J, O'Reilly MS. Radiation therapy to a primary tumor accelerates metastatic growth in mice. Cancer Res 2001;61:2207-11.
117. de Ruiter J, Cramer SJ, Lelieveld P, van Putten LM. Comparison of metastatic disease after local tumour treatment with radiotherapy or surgery in various tumour models. Eur J Cancer Clin Oncol 1982;18: 281-9.
118. Milas L, HirataH, Hunter N, Peters LJ. Effect of radiation-induced injury of tumor bed stroma on metastatic spread of murine sarcomas and carcinomas. Cancer Res 1988;48:2116-20.
119. Monnier Y, Farmer P, Bieler G, Imaizumi N, Sengstag T, Alghisi GC, et al. CYR61 and alphaVbeta5 integrin cooperate to promote invasion and metastasis of tumors growing in preirradiated stroma. Cancer Res 2008;68:7323-31.
120. Rofstad EK, Mathiesen B, Galappathi K. Increased metastatic dissemination in human melanoma xenografts after subcurative radiation treatment: radiation-induced increase in fraction of hypoxic cells and hypoxiainduced up-regulation of urokinase-type plasminogen activator receptor. Cancer Res 2004;64:13-8.
121. Jia JB, Wang WQ, Sun HC, Liu L, Zhu XD, Kong LQ, et al. A novel tripeptide, tyroserleutide, inhibits irradiation-induced invasiveness and metastasis of hepatocellular carcinoma in nude mice. Invest New Drugs 2011;29:861-72.
122. Murphy ED, Kaplan HS. Enhancement of metastasis of a mouse mammary carcinoma following roentgen irradiation. Am J Pathol 1948;24: 673.
123. Yamagishi N, Teshima-Kondo S, Masuda K, Nishida K, Kuwano Y, Dang DT, et al. Chronic inhibition of tumor cell-derived VEGF enhances the malignant phenotype of colorectal cancer cells. BMC Cancer 2013;13:229.
124. van MalensteinH, Dekervel J, Verslype C, Van CutsemE,Windmolders P, Nevens F, et al. Long-term exposure to sorafenib of liver cancer cells induces resistance with epithelial-to-mesenchymal transition, increased invasion and risk of rebound growth. Cancer Lett 2013;329:74-83.
125. Kennel SJ, Lankford TK, Ullrich RL, Jamasbi RJ. Enhancement of lung colony formation by treatment of mice with monoclonal antibodies to pulmonary capillary endothelial cells. Cancer Res 1988;48:4964-8.
126. Pool SE, Bison S, Koelewijn SJ, van der Graaf LM, Melis M, Krenning EP, et al. mTOR inhibitor RAD001 promotes metastasis in a rat model of pancreatic neuroendocrine cancer. Cancer Res 2013;73:12-8.
127. Yin T, He S, Ye T, Shen G, Wan Y, Wang Y. Antiangiogenic therapy using sunitinib combined with rapamycin retards tumor growth but promotes metastasis. Transl Oncol 2014;7:221-9.
128. Kruger A, Soeltl R, Sopov I, Kopitz C, Arlt M, Magdolen V, et al. Hydroxamate-type matrix metalloproteinase inhibitor batimastat promotes liver metastasis. Cancer Res 2001;61:1272-5.
129. Al SahafO, Wang JH, Browne TJ, Cotter TG, Redmond HP. Surgical injury enhances the expression of genes that mediate breast cancer metastasis to the lung. Ann Surg 2010;252:1037-43.
130. Baker DG, Masterson TM, Pace R, Constable WC, Wanebo H. The influence of the surgical wound on local tumor recurrence. Surgery 1989;106:525-32.
131. Hofer SO, Shrayer D, Reichner JS, Hoekstra HJ, Wanebo HJ. Woundinduced tumor progression: a probable role in recurrence after tumor resection. Arch Surg 1998;133:383-9.
132. Hobson J, Gummadidala P, Silverstrim B, Grier D, Bunn J, James T, et al. Acute inflammation induced by the biopsy of mouse mammary tumors promotes the development of metastasis. Breast Cancer Res Treat 2013;139:391-401.
133. Kubera M, Grygier B, Arteta B, Urbanska K, Basta-KaimA, Budziszewska B, et al. Age-dependent stimulatory effect of desipramine and fluoxetine pretreatment on metastasis formation by B16F10 melanoma in male C57BL/6 mice. Pharmacol Rep 2009;61:1113-26.
134. Orr FW, Adamson IY, Young L. Pulmonary inflammation generates chemotactic activity for tumor cells and promotes lung metastasis. Am Rev Respir Dis 1985;131:607-11.
135. Florentin I, Nolibe D, Giroud JP. Acute non-immunological inflammation inhibits natural killer (NK) activity in the lungs and enhances metastatic development. Int J Exp Pathol 1991;72:83-95.
136. Adamson IY, Young L, Orr FW. Tumor metastasis after hyperoxic injury and repair of the pulmonary endothelium. Lab Invest 1987;57:71-7.
137. Pidgeon GP, Harmey JH, Kay E, Da Costa M, Redmond HP, Bouchier-Hayes DJ. The role of endotoxin/lipopolysaccharide in surgically induced tumour growth in a murine model of metastatic disease. Br J Cancer 1999;81:1311-7.
138. Harmey JH, Bucana CD, Lu W, Byrne AM, McDonnell S, Lynch C, et al. Lipopolysaccharide-induced metastatic growth is associated with increased angiogenesis, vascular permeability and tumor cell invasion. Int J Cancer 2002;101:415-22.
139. Cairns RA, Hill RP. Acute hypoxia enhances spontaneous lymph node metastasis in an orthotopic murine model of human cervical carcinoma. Cancer Res 2004;64:2054-61.
140. Cairns RA, Kalliomaki T, Hill RP. Acute (cyclic) hypoxia enhances spontaneous metastasis of KHT murine tumors. Cancer Res 2001;61: 8903-8.
141. Rofstad EK, Gaustad JV, Egeland TA, Mathiesen B, Galappathi K. Tumors exposed to acute cyclic hypoxic stress show enhanced angiogenesis, perfusion and metastatic dissemination. Int J Cancer 2010;127:1535-46.
142. Simon RH, Arbo TE. Morphine increases metastatic tumor growth. Brain Res Bull 1986;16:363-7.
143. Farooqui M, Li Y, Rogers T, Poonawala T,Griffin RJ, Song CW, et al. COX-2 inhibitor celecoxib prevents chronic morphine-induced promotion of angiogenesis, tumour growth, metastasis and mortality, without compromising analgesia. Br J Cancer 2007;97:1523-31.
144. Shewell J, Thompson SC. The effect of hyperbaric oxygen treatment on pulmonary metastasis in the C3H mouse. Eur J Cancer 1980;16: 253-9.
145. Nathanson SD, Haas GP, Bobrowski R, Lee M, Tilley B, Schultz L, et al. Regional lymph node and pulmonary metastases after local hyperthermia of melanomas in C57BL/6 mice. Int J Radiat Oncol Biol Phys 1987;13: 243-9.
146. Baker D, Sager H, Constable W. The influence of levamisole and hyperthermia on the incidence of metastases from an X-irradiated tumor. Cancer Invest 1986;4:287-92.
147. Walker A, McCallumHM, Wheldon TE, Nias AH, Abdelaal AS. Promotion of metastasis of C3H mouse mammary carcinoma by local hyperthermia. Br J Cancer 1978;38:561-3.
148. Yerushalmi A. Influence on metastatic spread of whole-body or local tumor hyperthermia. Eur J Cancer 1976;12:455-63.
149. Ajibade AA, Kirk JS, Karasik E, Gillard B, Moser MT, Johnson CS, et al. Early growth inhibition is followed by increased metastatic disease with vitaminD( calcitriol) treatment in the TRAMP model of prostate cancer. PLoS ONE 2014;9:e89555.
150. Sayin VI, Ibrahim MX, Larsson E, Nilsson JA, Lindahl P, Bergo MO. Antioxidants accelerate lung cancer progression in mice. Sci Transl Med 2014;6:221ra15.
151. Zhuang PY, Zhang JB, Zhang W, Zhu XD, Liang Y, Xu HX, et al. Long-term interferon-Alpha treatment suppresses tumor growth but promotes metastasis capacity in hepatocellular carcinoma. J Cancer Res Clin Oncol 2010;136:1891-900.
152. Ben-Eliyahu S, Yirmiya R, Liebeskind JC, Taylor AN, Gale RP. Stress increases metastatic spread of a mammary tumor in rats: evidence for mediation by the immune system. Brain Behav Immun 1991;5: 193-205.