Metastasis: The evasion of apoptosis

Apoptosis, Cell Signaling, and Human Diseases

Volumn 1, Issue , 2007, Pages 63-96

  Horak, Christine E ^a   Bronder, Julie L ^a   Bouadis, Amina ^a   Steeg, Patricia S ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

anoikis; apoptosis; Bcl 2 family; chemotherapeutic resistance; DAP kinase; maspin; Metastasis; molecularly targeted therapy; TNF family; transcription factors

Indexed keywords

EID: 53749101106     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-1-59745-200-7_3     Document Type: Chapter

References (197)

1. Entschladen F, Drell TLt, Lang K, Joseph J, Zaenker KS. Tumour-cell migration, invasion, and metastasis: navigation by neurotransmitters. Lancet Oncol 2004;5(4):254-258.
2. Weiss L. Metastatic inefficiency. Adv Cancer Res 1990;54:159-211.
3. Luzzi KJ, MacDonald IC, Schmidt EE, et al. Multistep nature of metastatic inefficiency: dormancy of solitary cells after successful extravasation and limited survival of early micrometastases. Am J Pathol 1998;153(3):865-873.
4. Malaguarnera L. Implications of apoptosis regulators in tumorigenesis. Cancer Metastasis Rev 2004;23(3-4):367-387.
5. Tenjo T, Toyoda M, Okuda J, et al. Prognostic significance of p27(kip1) protein expression and spontaneous apoptosis in patients with colorectal adenocarcinomas. Oncology 2000; 58(1):45-51.
6. Yamasaki F, Tokunaga O, Sugimori H. Apoptotic index in ovarian carcinoma: correlation with clinicopathologic factors and prognosis. Gynecol Oncol 1997;66(3):439-448.
7. Shibata H, Matsubara O. Apoptosis as an independent prognostic indicator in squamous cell carcinoma of the esophagus. Pathol Int 2001;51(7):498-503.
8. Sugamura K, Makino M, Kaibara N. Apoptosis as a prognostic factor in colorectal carcinoma. Surg Today 1998;28(2):145-150.
9. Richter EN, Oevermann K, Buentig N, Storkel S, Dallmann I, Atzpodien J. Primary apoptosis as a prognostic index for the classification of metastatic renal cell carcinoma. J Urol 2002;168(2):460-464.
10. Ohtani M, Isozaki H, Fujii K, et al. Impact of the expression of cyclin-dependent kinase inhibitor p27Kip1 and apoptosis in tumor cells on the overall survival of patients with non-early stage gastric carcinoma. Cancer 1999;85(8):1711-1718.
11. Ito Y, Matsuura N, Sakon M, et al. Both cell proliferation and apoptosis significantly predict shortened disease-free survival in hepatocellular carcinoma. Br J Cancer 1999;81(4):747-751.
12. Glinsky G, Glinsky V, Ivanova A, Hueser C. Apoptosis and metastasis: increased apoptosis resistance of metastatic cancer cells is associated with the profound deficiency of apoptosis execution mechanisms. Cancer Lett 1997;115(2):185-193.
13. Townson JL, Naumov GN, Chambers AF. The role of apoptosis in tumor progression and metastasis. Curr Mol Med 2003;3(7):631-642.
14. Holmgren L, O'Reilly M, Folkman J. Dormancy of micrometastases: balanced proliferation and apoptosis in the presence of angiogenesis suppression. Nat Med 1995;1(2):149-153.
15. Naumov GN, MacDonald IC, Chambers AF, Groom AC. Solitary cancer cells as a possible source of tumour dormancy? Semin Cancer Biol 2001;11(4):271-276.
16. Fernandez Y, Gu B, Martinez A, Torregrosa A, Sierra A. Inhibition of apoptosis in human breast cancer cells: role in tumor progression to the metastatic state. Int J Cancer 2002;101(4):317-326.
17. Khanna C, Hunter K. Modeling metastasis in vivo. Carcinogenesis 2005;26(3):513-523.
18. Eggert A, Grotzer M, Zuzak T, et al. Resistance to Tumor Necrosis Factor-related apop-tosis-inducing apoptosis in neuroblastoma cells correlates with a loss of Caspase-8 expression. Cancer Res 2001;61:1314-1319.
19. Grotzer M, Eggert A, Zuzak T, et al. Resistance to TRAIL-induced apoptosis in primitive neuroectodermal brain tumor cells correlates with a loss of caspase-8 expression. Oncogene 2000;19:4604-4610.
20. Pingoud-Meier C, Lang D, Janss A, et al. Loss of Caspase-8 protein expression correlates with unfavorable survival outcome in childhood medulloblastoma. Clin Cancer Res 2003; 9:6401-6409.
21. Shin MS, Kim HS, Lee SH, et al. Alterations of Fas-pathway genes associated with nodal metastasis in non-small cell lung cancer. Oncogene 2002;21:4129-4136.
22. Koomagi R, Volm M. Relationship between the expression of caspase-3 and the clinical outcome of patients with non-small cell lung cancer. Anticancer Res 2000;20(1B):493-496.
23. Volm M, Koomagi R. Prognostic relevance of c-Myc and caspase-3 for patients with non-small cell lung cancer. Oncology Reports 2000;7(1):95-98.
24. Sun B, Zhang J, Wang B, et al. Analysis of in vivo patterns of caspase 3 gene expression in primary hepatocellular carcinoma and its relationship to p21WAF1 expression and hepatic apoptosis. World J Gastroenterol 2000;6(3):356-360.
25. Sun H, Zheng H, Yang X, et al. Expression of PTEN and Caspase-3 and their clinicopatho-logical significance in primary gastric malignant lymphoma. Chin Med Sci J 2004;19(1):19-24.
26. Isobe N, Onodera H, Mori A, et al. Caspase-3 expression in human gastric carcinoma and its clinical significance. Oncology 2004;66(3):201-209.
27. Schimmer AD. Inhibitor of apoptosis proteins: translating basic knowledge into clinical practice. Cancer Res 2004;64(20):7183-7190.
28. Tanaka K, Iwamoto S, Gon G, Nohara T, Iwamoto M, Tanigawa N. Expression of survivin and its relationship to loss of apoptosis in breast carcinomas. Clin Cancer Res 2000;6(1): 127-134.
29. Kato J, Kuwabara Y, Mitani M, et al. Expression of survivin in esophageal cancer: correlation with the prognosis and response to chemotherapy. Int J Cancer 2001;95(2):92-95.
30. Chen W, Liu Q, Fu J, Kang S. Expression of survivin and its significance in colorectal cancer. World J Gastroenterol 2004;10(19):2886-2889.
31. Jaattela M. Escaping cell death: survival proteins in cancer. Exp Cell Res 1999;248(1): 30-43.
32. Kishi H, Igawa M, Kikuno N, Yoshino T, Urakami S, Shiina H. Expression of the survivin gene in prostate cancer: correlation with clinicopathological characteristics, proliferative activity and apoptosis. J Urol 2004;171(5):1855-1860.
33. Agui T, McConkey DJ, Tanigawa N. Comparative study of various biological parameters, including expression of survivin, between primary and metastatic human colonic adenocarcinomas. Anticancer Res 2002;22(3):1769-1776.
34. Levy-Strumpf N, Kimchi A. Death associated proteins (DAPs): from gene identification to the analysis of their apoptotic and tumor suppressive functions. Oncogene 1998;17(25): 3331-3340.
35. Raveh T, Kimchi A. DAP Kinase-A proapoptotic gene that functions as a tumor suppressor. Exp Cell Res 2001;264:185-192.
36. Inbal B, Cohen O, Polak-Charcon S, et al. DAP kinase links the control of apoptosis to metastasis. Nature 1997;390(6656):180-184.
37. Kogel D, Reimertz C, Mech P, et al. Dlk/ZIP kinase-induced apoptosis in human medul-lablastoma cells: requirement of the mitochondrial apoptosis pathway. Br J Cancer 2001;85(11):1801-1808.
38. Levy D, Plu-Bureau G, Decroix Y, et al. Death-associated protein kinase loss of expression is a new marker for breast cancer prognosis. Clin Cancer Res 2004;10(9):3124-3130.
39. Ng M. Death associated protein kinase: From regulation of apoptosis to tumor suppressive functions and B cell malignancies. Apoptosis 2002;7(3):261-270.
40. Kim D, Nelson H, Wiencke J, et al. Promoter methylation of DAP-kinase: association with advanced stage in non-small cell lung cancer. Oncogene 2001;20:1765-1770.
41. Gonzalez-Gomez P, Bello M, Alonso M, et al. Frequent death-associated protein-kinase promoter hypermethylation in brain metastases of solid tumors. Oncol Rep 2003;10(4): 1031-1033.
42. Baldi A, Santini D, Russo P, et al. Analysis of APAF-1 expression in human cutaneous melanoma progression. Exp Dermatol 2004;13(2):93-97.
43. Soengas M, Capodieci P, Polsky D, et al. Inactivation of the apoptosis effector Apaf-1 in malignant melanoma. Nature 2001;409(6817):201-211.
44. Umetani N, Fujimoto A, Takeuchi H, Shinozaki M, Bilchik A, Hoon D. Allelic imbalance of APAF-1 locus at 12q23 is related to progression of colorectal carcinoma. Oncogene 2004;23:8292-8300.
45. Reed J. Mechanisms of apoptosis avoidance in cancer. Cuu Opin Oncol 1999;11(1):68-75.
46. Bold RJ, Virudachalam S, McConkey DJ. BCL2 expression correlates with metastatic potential in pancreatic cancer cell lines. Cancer 2001;92(5):1122-1129.
47. Furuya Y, Krajewski S, Epstein JI, Reed JC, Isaacs JT. Expression of bcl-2 and the progression of human and rodent prostatic cancers. Clin Cancer Res 1996;2(2):389-398.
48. Takaoka A, Adachi M, Okuda H, et al. Anti-cell death activity promotes pulmonary metastasis of melanoma cells. Oncogene 1997;14(24):2971-2977.
49. Pinkas J, Martin SS, Leder P. Bcl-2-mediated cell survival promotes metastasis of EpH4 betaMEKDD mammary epithelial cells. Mol Cancer Res 2004;2(10):551-556.
50. Sierra A, Lloveras B, Castellsague X, Moreno L, Garcia-Ramirez M, Fabra A. Bcl-2 expression is associated with lymph node metastasis in human ductal breast carcinoma. Int J Cancer 1995;60(1):54-60.
51. Le MG, Mathieu MC, Douc-Rasy S, et al. c-myc, p53 and bcl-2, apoptosis-related genes in infiltrating breast carcinomas: evidence of a link between bcl-2 protein over-expression and a lower risk of metastasis and death in operable patients. Int J Cancer 1999;84(6): 562-567.
52. Zellweger T, Ninck C, Bloch M, et al. Expression patterns of potential therapeutic targets in prostate cancer. Int J Cancer 2005;113(4):619-628.
53. Martin SS, Ridgeway AG, Pinkas J, et al. A cytoskeleton-based functional genetic screen identifies Bcl-xL as an enhancer of metastasis, but not primary tumor growth. Oncogene 2004;23(26):4641-4645.
54. Fernandez Y, Espana L, Manas S, Fabra A, Sierra A. Bcl-xL promotes metastasis of breast cancer cells by induction of cytokines resistance. Cell Death Differ 2000;7(4):350-359.
55. Espana L, Fernandez Y, Rubio N, Torregrosa A, Blanco J, Sierra A. Overexpression of Bcl-x(L) in Human Breast Cancer Cells Enhances Organ-Selective Lymph Node Metastasis. Breast Cancer Res Treat 2004;87(1):33-44.
56. Gu B, Espana L, Mendez O, Torregrosa A, Sierra A. Organ-selective chemoresistance in metastasis from human breast cancer cells: inhibition of apoptosis, genetic variability and microenvironment at the metastatic focus. Carcinogenesis 2004;25(12):2293-2301.
57. Olopade OI, Adeyanju MO, Safa AR, et al. Overexpression of BCL-x protein in primary breast cancer is associated with high tumor grade and nodal metastases. Cancer J Sci Am 1997;3(4):230-237.
58. McConkey DJ, Greene G, Pettaway CA. Apoptosis resistance increases with metastatic potential in cells of the human LNCaP prostate carcinoma line. Cancer Res 1996;56(24): 5594-5599.
59. Krajewski S, Blomqvist C, Franssila K, et al. Reduced expression of proapoptotic gene BAX is associated with poor response rates to combination chemotherapy and shorter survival in women with metastatic breast adenocarcinoma. Cancer Res 1995;55(19):4471-4478.
60. Ogura E, Senzaki H, Yamamoto D, et al. Prognostic significance of Bcl-2, Bcl-xL/S, Bax and Bak expressions in colorectal carcinomas. Oncol Rep 1999;6(2):365-369.
61. Ito T, Fujieda S, Tsuzuki H, et al. Decreased expression of Bax is correlated with poor prognosis in oral and oropharyngeal carcinoma. Cancer Lett 1999;140(1-2):81-91.
62. Wu J, Shao ZM, Shen ZZ, et al. Significance of Apoptosis and Apoptotic-Related Proteins, Bcl-2, and Bax in Primary Breast Cancer. Breast J 2000;6(1):44-52.
63. Sheng S. The promise and challenge toward the clinical application of maspin in cancer. Frontiers Bioscience 2004;9:2733-2745.
64. Jiang N, Meng Y, Zhang S, Mensah-Osman E, Sheng S. Maspin sensitizes breast carcinoma cells to induce apoptosis. Oncogene 2002;21:4089-4098.
65. Liu J, Yin S, Reddy N, Spencer C, Sheng S. Bax mediates the apoptosis-sensitizing effect of maspin. Cancer Res 2004;64(5):1703-1711.
66. Li Z, Shi H, Zhang M. Targeted expression of maspin in tumor vasculatures induces endothelial cell apoptosis. Oncogene 2005;24(12):2008-2019.
67. Latha K, Zhang W, Cella N, Shi H, Zhang M. Maspin mediates increased tumor cell apoptosis upon induction of the mitochondrial permeability transition. Mol Cell Biol 2005;25(5):1737-1748.
68. Shi H, Zhang W, Liang R, et al. Modeling human breast cancer metastasis in mice: maspin as a paradigm. Histol Histopathol 2003;18:201-206.
69. Zhang M, Shi Y, Magit D, Furth PA, Sager R. Reduced mammary tumor progression in WAP-TAg/WAP-maspin bitransgenic mice. Oncogene 2000;19(52):6053-6058.
70. Shi H, Zhang W, Liang R, et al. Blocking tumor growth, invasion, and metastasis by maspin in a syngeneic breast cancer model. Cancer Res 2001;61(18):6945-6951.
71. Shi H, Liang R, Templeton N, Zhang M. Inhibition of breast tumor progression by systemic delivery of the maspin gene in a syngeneic tumor model. Mol Ther 2002;5(6):755-761.
72. Maass N, Hojo T, Rosel F, Ikeda T, Jonat W, Nagasaki K. Down regulation of the tumor suppressor gene maspin in breast carcinoma is associated with a higher risk of distant metastasis. Clin Biochem 2001;34(4):303-307.
73. Maass N, Teffner M, Rosel F, et al. Decline in the expression of the serine proteinase inhibitor maspin is associated with tumour progression in ductal carcinomas of the breast. J Pathol 2001;195(3):321-326.
74. Wang M, Yang Y, Li X, Dong F, Li Y Maspin expression and its clinicopathological significance in tumorigenesis and progression of gastric cancer. World J Gastroenterol 2004;10(5):634-637.
75. Maass N, Biallek M, Rosel F, et al. Hypermethylation and histone deacetylation lead to silencing of the maspin gene in human breast cancer. Biochem Biophys Res Commun 2002;297(1):125-128.
76. Primeau M, Gagnon J, Momparler R. Synergistic antineoplastic action of DNA methyla-tion inhibitor 5-AZA-2'-deoxycytidine and histone deacetylase inhibitor depsipeptide on human breast carcinoma cells. Int J Cancer 2003;103(2):177-184.
77. Akiyama Y, Maesawa C, Ogasawara S, Terashima M, Masuda T. Cell-type-specific repression of the maspin gene is disrupted frequently by demethylation at the promoter region in gastric intestinal metaplasia and cancer cells. Am J Pathol 2003;163(5):1911-1919.
78. Boltze C, Schneider-Stock R, Quednow C, et al. Silencing of the maspin gene by promoter hypermethylation in thyroid cancer. Int J Mol Med 2003;12(4):479-484.
79. Sato N, Fukushima N, Matsubayashi H, Goggins M. Identification of maspin and S100P as novel hypomethylation targets in pancreatic cancer using global gene expression profiling. Oncogene 2004;23(8):1531-1538.
80. Wang S, El-Deiry W. TRAIL and apoptosis induction by TNF-family death receptors. Oncogene 2003;22:8628-8633.
81. LeBlanc H, Lawrence D, Varfolomeev E, et al. Tumor-cell resistance to death receptor-induced apoptosis through mutational inactivation of the proapoptotic Bcl-2 homolog Bax. Nat Med 2002;8(3):274-281.
82. Deng Y, Lin Y, Wu X. TRAIL-induced apoptosis recquires Bax-dependent mitochondrial release of Smac/DIABLO. Gene Dev 2002;16:33-45.
83. Kim K, Lee Y Amiloride augments TRAIL-induced apoptotic death by inhibiting phosphorylation of kinases and phosphatases associated with P13K-Akt pathway. Oncogene 2005; 24:355-366.
84. Harper N, Hughes M, Farrow S, Cohen G, MacFarlane M. Protein kinase C modulates tumor necrosis factor-related apoptosis-inducing ligand-induced apoptosis by targeting the apical events of death receptor signaling. J Biol Chem 2003;278(45):44, 338-44, 347.
85. Frese S, Pirnia F, Miescher D, et al. PG490-mediated sensitization of lung cancer cells to Apo2L/TRAIL-induced apoptosis requires activation of ERK2. Oncogene 2003;22(25): 5427-5435.
86. Thakkar H, Chen X, Tyan F, et al. Pro-survival function of Akt/protein kinase B in prostate cancer cells. Relationship with TRAIL resistance. J Biol Chem 2001;276(42): 38, 361-38, 369.
87. Owen-Schaub L, van Golen K, Hill L, Price J. Fas and Fas ligand interactions suppress melanoma lung metastasis. J Exp Med 1998;188(9):1717-1723.
88. Hedlund T, Duke R, Schleicher M, Miller G. Fas-mediated apoptosis in seven human prostate cancer cell lines: correlation with tumor stage. Prostate 1998;36(2):92-101.
89. Monti P, Marchesi F, Reni M, et al. A comprehensive in vitro characterization of pancreatic ductal carcinoma cell line biological behavior and its correlation with the structural and genetic profile. Virchows Arch 2004.
90. Worth L, Lafleur E, Jia S, Kleinerman E. Fas expression inversely correlates with metastatic potential in osteosarcoma cells. Oncol Rep 2002;9(4):823-827.
91. Ogawa S, Nagao M, Kanehiro H, et al. The breakdown of apoptotic mechanism in the development and progression of colorectal carcinoma. Anticancer Res 2004;24(3a): 1569-1579.
92. Wang W, Chen P, Hsiao H, Wang H, Liang W, Su Y Overexpression of the thymosin beta-4 gene is associated with increased invasion of SW480 colon carcinoma cells and the distant metastasis of human colorectal carcinoma. Oncogene 2004;23(39):6666-6671.
93. Nagao M, Nakajima Y, Hisanaga M, et al. The alteration of Fas receptor and ligand system in hepatocellular carcinomas: How do hepatoma cells escape from the host immune surveillance in vitro? Hepatology 1999;30(2):413-421.
94. Qin L, Tang Z. The prognostic molecular markers in hepatocellular carcinoma. World J Gastroenterol 2002;8(3):385-392.
95. Munakata S, Enomoto T, Tsujimoto M, et al. Expressions of Fas ligand and other apop-tosis-related genes and their prognostic significance in epithelial ovarian neoplasms. Br J Cancer 2000;82(8):1446-1452.
96. Ueno T, Toi M, Tominaga T. Circulating soluble Fas concentration in breast cancer patients. Clin Cancer Res 1999;5:3529-3533.
97. Bewick M, Conlon M, Parissenti A, et al. Soluble Fad (CD95) is a prognostic factor in patients with metastatic breast cancer undergoing high-dose chemotherapy and autologous stem cell transplantation. J Hematother Stem Cell Res 2001;10(6):759-768.
98. Mouawad R, Khayat D, Soubrane C. Plasma Fas ligand, an inducer of apoptosis, and plasma soluble Fas, an inhibitor of apoptosis, in advanced melanoma. Melanoma Res 2000;10(5):461-467.
99. Wu Y, Han B, Sheng H, et al. Clinical significance of detecting elevated serum DcR3/TR6/M68 in malignant tumor patients. Int J Cancer 2003;105:724-732.
100. Mottolese M, Buglioni S, Bracalenti C, et al. Prognostic relevance of altered Fas (CD95)-system in human breast cancer. Int J Cancer 2000;89(2):127-132.
101. Mann B, Gratchev A, Bohm C, et al. FasL is more frequently expressed in liver metastases of colorectal cancer than in matched primary carcinomas. Br J Cancer 1999;79(7-8): 1262-1269.
102. Okada K, Komuta K, Hashimoto S, Matsuzaki S, Kanematsu T, Koji T. Frequency of apop-tosis of tumor-infiltrating lymphocytes induced by fas counterattack in human colorectal carcinoma and its correlation with prognosis. Clin Cancer Res 2000;6(9):3560-3564.
103. Koyama S, Koike N, Adachi S. Fas receptor counterattack against tumor-infiltrating lymphocytes in vivo as a mechanism of immune escape in gastric carcinoma. J Cancer Res Clin Oncol 2001;127(1):20-26.
104. Pan G, Ni J, Wei Y, Yu G, Gentz R, Dixit V. An antagonist decoy receptor and a death domain-containing receptor for TRAIL. Science 1997;277:815-818.
105. Takeda K, Hayakawa M, Smyth M, et al. Involvement of tumor necrosis factor-related apoptosis-inducing ligand in surveillance of tumor metastasis by liver natural killer cells. Nature Medicine 2001;7(1):94-100.
106. Cretney E, Takeda K, Yagita H, Glaccum M, Peschon J, Smyth M. Increased susceptibility to tumor initiation and metastasis in TNF-related apoptosis-inducing ligand-deficient mice. J Immunol 2002;168(3):1356-1361.
107. Abdollahi T. Potential for TRAIL as a therapeutic agent in ovarian cancer. Vitam Horm 2004;67:347-364.
108. Kaliberov S, Kaliberova L, Stockard C, Grizzle W, Buchsbaum D. Adenovirus-mediated FLT1-targeted proapoptotic gene therapy of human prostate cancer. Mol Ther 2004;10(6): 1059-1070.
109. Yamashita Y, Shimada M, Tanaka S, Okamamoto M, Miyazaki J, Sugimachi K. Electro-poration-mediated tumor necrosis factor-related apoptosis-inducing ligand (TRAIL)/Apo2L gene therapy for hepatocellular carcinoma. Hum Gene Ther 2002;13:275-286.
110. Lin T, Zhang L, Davis J, et al. Combination of TRAIL gene therapy and chemotherapy enhances antitumor and antimetastasis effects in chemosensitive and chemoresitant breast cancers. Mol Ther 2003;8(3):441-448.
111. Zhang XD, Franco A, Myers K, Gray C, Nguyen T, Hersey P. Relation of TNF-related apoptosis-inducing ligand (TRAIL) receptor and FLICE-inhibitory protein expression to TRAIL-induced apoptosis of melanoma. Cancer Res 1999;59(11):2747-2753.
112. Vigneswaran N, Wu J, Nagaraj N, Adler-Storthz K, Zacharias W. Differential susceptibility of metastatic and primary oral cancer cells to TRAIL-induced apoptosis. Int J Oncol 2005;26(1):103-112.
113. Shin M, Kim H, Lee S, et al. Mutations of tumor necrosis factor-related apoptosis-inducing ligand receptor 1 (TRAIL-R1) and receptor 2 (TRAIL-R2) genes in metastatic breast cancers. Cancer Res 2001;61(13):4942-4946.
114. Koyama S, Koike N, Adachi S. Expression of TNF-related apoptosis-inducing ligand (TRAIL) and its receptors in gastric carcinoma and tumor-infiltrating lymphocytes: a possible mechanism of immune evasion of the tumor. J Cancer Res Clin Oncol 2002;128:73-79.
115. Nyambo R, Cross N, Lippitt J, et al. Human bone marrow stromal cells protect prostate cancer cells from TRAIL-induced apoptosis. J Bone Min Res 2004;19(10):1712-1721.
116. Bharti AC, Aggarwal BB. Nuclear factor-kappa B and cancer: its role in prevention and therapy. Biochem Pharmacol 2002;64(5-6):883-888.
117. Orlowski RZ, Baldwin AS, Jr. NF-kappaB as a therapeutic target in cancer. Trends Mol Med 2002;8(8):385-389.
118. Dong G, Loukinova E, Chen Z, et al. Molecular profiling of transformed and metastatic murine squamous carcinoma cells by differential display and cDNA microarray reveals altered expression of multiple genes related to growth, apoptosis, angiogenesis, and the NF-kappaB signal pathway. Cancer Res 2001;61(12):4797-4808.
119. Huber MA, Azoitei N, Baumann B, et al. NF-kappaB is essential for epithelial-mesenchymal transition and metastasis in a model of breast cancer progression. J Clin Invest 2004; 114(4):569-581.
120. Nakshatri H, Bhat-Nakshatri P, Martin DA, Goulet RJ, Jr, Sledge GW, Jr. Constitutive activation of NF-kappaB during progression of breast cancer to hormone-independent growth. Mol Cell Biol 1997;17(7):3629-3639.
121. Biswas DK, Shi Q, Baily S, et al. NF-kappa B activation in human breast cancer specimens and its role in cell proliferation and apoptosis. Proc Natl Acad Sci USA 2004;101(27): 10, 137-10, 142.
122. Fujioka S, Sclabas GM, Schmidt C, et al. Function of nuclear factor kappaB in pancreatic cancer metastasis. Clin Cancer Res 2003;9(1):346-354.
123. Sunwoo JB, Chen Z, Dong G, et al. Novel proteasome inhibitor PS-341 inhibits activation of nuclear factor-kappa B, cell survival, tumor growth, and angiogenesis in squamous cell carcinoma. Clin Cancer Res 2001;7(5):1419-1428.
124. Scaife CL, Kuang J, Wills JC, et al. Nuclear factor kappaB inhibitors induce adhesion-dependent colon cancer apoptosis: implications for metastasis. Cancer Res 2002;62(23): 6870-6878.
125. Oren M. Decision making by p53: life, death and cancer. Cell Death Differ 2003;10(4): 431-442.
126. Vousden KH, Lu X. Live or let die: the cell's response to p53. Nat Rev Cancer 2002; 2(8):594-604.
127. Xu H, el-Gewely MR. P53-responsive genes and the potential for cancer diagnostics and therapeutics development. Biotechnol Annu Rev 2001;7:131-164.
128. Thompson TC, Park SH, Timme TL, et al. Loss of p53 function leads to metastasis in ras+myc-initiated mouse prostate cancer. Oncogene 1995;10(5):869-879.
129. Nikiforov MA, Hagen K, Ossovskaya VS, et al. p53 modulation of anchorage independent growth and experimental metastasis. Oncogene 1996;13(8):1709-1719.
130. Sierra A, Castellsague X, Escobedo A, et al. Bcl-2 with loss of apoptosis allows accumulation of genetic alterations: a pathway to metastatic progression in human breast cancer. Int J Cancer 2000;89(2):142-147.
131. Schuster N, Krieglstein K. Mechanisms of TGF-beta-mediated apoptosis. Cell Tissue Res 2002;307(1):1-14.
132. Wakefield LM, Roberts AB. TGF-beta signaling: positive and negative effects on tumori-genesis. Curr Opin Genet Dev 2002;12(1):22-29.
133. Siegel PM, Massague J. Cytostatic and apoptotic actions of TGF-beta in homeostasis and cancer. Nat Rev Cancer 2003;3(11):807-821.
134. Copland JA, Luxon BA, Ajani L, et al. Genomic profiling identifies alterations in TGF-beta signaling through loss of TGF-beta receptor expression in human renal cell carcinogenesis and progression. Oncogene 2003;22(39):8053-8062.
135. Gemma A, Takenaka K, Hosoya Y, et al. Altered expression of several genes in highly metastatic subpopulations of a human pulmonary adenocarcinoma cell line. Eur J Cancer 2001;37(12):1554-1561.
136. Tu WH, Thomas TZ, Masumori N, et al. The loss of TGF-beta signaling promotes prostate cancer metastasis. Neoplasia 2003;5(3):267-277.
137. Ramachandra M, Atencio I, Rahman A, et al. Restoration of transforming growth factor Beta signaling by functional expression of smad4 induces anoikis. Cancer Res 2002; 62(21):6045-6051.
138. Chen T, Carter D, Garrigue-Antar L, Reiss M. Transforming growth factor beta type I receptor kinase mutant associated with metastatic breast cancer. Cancer Res 1998; 58(21):4805-4810.
139. Wikstrom P, Stattin P, Franck-Lissbrant I, Damber JE, Bergh A. Transforming growth factor beta1 is associated with angiogenesis, metastasis, and poor clinical outcome in prostate cancer. Prostate 1998;37(1):19-29.
140. Reiss M. TGF-beta and cancer. Microbes Infect 1999;1(15):1327-1347.
141. Zhu Z, Sanchez-Sweatman O, Huang X, et al. Anoikis and metastatic potential of cloud-man S91 melanoma cells. Cancer Res 2001;61(4):1707-1716.
142. Yawata A, Adachi M, Okuda H, et al. Prolonged cell survival enhances peritoneal dissemination of gastric cancer cells. Oncogene 1998;16(20):2681- 2686.
143. Swan E, Jasser S, Holsinger F, Doan D, Bucana C, Myers J. Acquisition of anoikis resistance is a critical step in the progression of oral tongue cancer. Oral Oncol 2003;39: 648-655.
144. Jiang K, Sun J, Cheng J, Djeu J, Wei S, Sebti S. Akt mediates Ras downregulation of RhoB, a suppressor of transformation, invasion, and metastasis. Mol Cell Biol 2004;24(12):5565-5576.
145. Itoh N, Semba S, Ito M, Takeda H, Kawata S, Yamakawa M. Phosphorylation of Akt/PKB is required for suppression of cancer cell apoptosis and tumor progression in human colorectal carcinoma. Cancer 2002;94(12):3127-3134.
146. Walsh M, Thamilselvan V, Grotelueschen R, Farhana L, Basson M. Absence of adhesion triggers differential FAK and SAPKp38 signals in SW620 human colon cancer cells that may inhibit adhesiveness and lead to cell death. Cell Physiol Biochem 2003;13(3): 135-146.
147. Frisch S, Vuori K, Kelaita D, Sicks S. A role for Jun-N-terminal kinase in anoikis; suppression by bcl-2 and crmA. J Cell Biol 1996;135(5):1377-1382.
148. Rosen K, Shi W, Calabretta B, Filmus J. Cell detachment triggers p38 mitogen-activated protein kinase-dependent overexpression of Fas ligand J Biol Chem 2002;277(48): 46, 123-46, 130.
149. Marco R, Diaz-Montero C, Wygant J, Kleinerman E, McIntyre B. Alpha-integrin increases anoikis of human osteosarcoma cells. J Cell Biochem 2003;88:1038-1047.
150. Bao S, Ouyang G, Bai X, et al. Periostin potently promotes metastatic growth of colon cancer by augmenting cell survival via the Akt/PKB pathway. Cancer Cell 2004;5(4):329-339.
151. Raz A, Geiger B. Altered organization of cell-substrate contacts and membrane-associated cytoskeleton in tumor cell variants exhibiting different metastatic capabilities. Cancer Res 1982;42(12):5183-5190.
152. Rodriguez Fernandez J, Geiger B, Salomon D, Sabanay I, Zoller M, Ben-Ze'ev A. Suppression of tumorigenicity in transformed cells after transfection with vinculin cDNA. J Cell Biol 1992;119(2):427-438.
153. Subauste M, Pertz O, Adamson E, Turner C, Junger S, Hahn K. Vinculin modulation of paxillin-FAK interactions regulates ERK control survival and motility. J Cell Biol 2004; 165(3):371-381.
154. Duxbury M, Ito H, Zinner M, Ashley S, Whang E. Focal adhesion kinase gene silencing promotes anoikis and suppresses metastasis of human pancreatic adenocarcinoma cells. Surgery 2004;135(5):555-562.
155. Kurenova E, Xu L, Yang X, et al. Focal Adhesion kinase suppresses apoptosis by binding to the death domain of receptor-interacting protein. Mol Cell Biol 2004;24(10):4361-4371.
156. Windham T, Parikh N, Siwak D, et al. Src activation regulates anoikis in human colon tumor cell lines. Oncogene 2002;21:7797-7807.
157. Griffiths G, Koh M, Brunton V, et al. Expression of kinase-defective mutants of c-Src in human metastatic colon cancer cells decreases Bcl-xL and increases oxaliplatin-and Fas-induced apoptosis. J BIol Chem 2004;279(44):46, 113-46, 121.
158. Wei L, Yang Y, Zhang X, Yu Q. Anchorage-independent phosphorylation of p130(Cas) protects lung adenocarcinoma cells from anoikis. J Cell Biochem 2002;87(4):439-449.
159. Zeng Q, Chen S, You Z, et al. Hepatocyte growth factor inhibits anoikis in head and neck squamous cell carcinoma cells by activation of ERK and Akt signaling independent of NFkappa B. J Biol Chem 2002;277(28):25, 203-25, 208.
160. Duxbury M, Ito H, Zinner M, Ashley S, Whang E. EphA2: a determinant of malignant cellular behavior and a potential therapeutic target in pancreatic adenocarcinoma. Oncogene 2004;23:1448-1456.
161. Douma S, van Laar T, Zevenhoven J, Meuwissen R, van Garderen E, Peeper D. Suppression of anoikis and induction of metastasis by the neurotrophic receptor TrkB. Nature 2004; 430:1034-1040.
162. Dionne C, Camoratto A, Jani J, et al. Cell cycle-independent death of prostate adenocarcinoma is induced by the trk tyrosine kinase inhibitor CEP-751 (KT6587). Clin Cancer Res 1998;4(8):1887-1898.
163. Aoyama M, Asai K, Shishikura T, et al. Human neuroblastomas with unfavorable biologies express high levels of brain-derived neurotrophic factor mRNA and a variety of its variants. Cancer Lett 2001;164(1):51-60.
164. Eggert A, Grotzer M, Ikegaki N, et al. Expression of the neurotrophin receptor TrkB is associated with unfavorable outcome in Wilms' tumor. J Clin Oncol 2001;19(3):689-696.
165. Weeraratna A, Dalrymple S, Lamb J, et al. Pan-trk inhibition decreases metastasis and enhances host survival in experimental models as a result of its selective induction of apoptosis of prostate cancer cells. Clin Cancer Res 2001;7:2237-2245.
166. Xiong HQ, Ajani JA. Treatment of colorectal cancer metastasis: the role of chemotherapy. Cancer Metastasis Rev 2004;23(1-2):145-163.
167. Goulian M, Bleile B, Tseng BY. Methotrexate-induced misincorporation of uracil into DNA. Proc Natl Acad Sci USA 1980;77(4):1956-1960.
168. Libra M, Navolanic PM, Talamini R, et al. Thymidylate synthetase mRNA levels are increased in liver metastases of colorectal cancer patients resistant to fluoropyrimidine-based chemotherapy. BMC Cancer 2004;4(1):11.
169. Peters GJ, van Triest B, Backus HH, Kuiper CM, van der Wilt CL, Pinedo HM. Molecular downstream events and induction of thymidylate synthase in mutant and wild-type p53 colon cancer cell lines after treatment with 5-fluorouracil and the thymidylate synthase inhibitor raltitrexed. Eur J Cancer 2000;36(7):916-924.
170. de Angelis PM, Fjell B, Kravik KL, et al. Molecular characterizations of derivatives of HCT116 colorectal cancer cells that are resistant to the chemotherapeutic agent 5-fluorouracil. Int J Oncol 2004;24(5):1279-1288.
171. Cao S, Lu K, Toth K, Slocum HK, Shirasaka T, Rustum YM. Persistent induction of apoptosis and suppression of mitosis as the basis for curative therapy with S-1, an oral 5-fluorouracil prodrug in a colorectal tumor model. Clin Cancer Res 1999;5(2):267-274.
172. Mori T, Fujiwara Y, Yano M, et al. Prevention of peritoneal metastasis of human gastric cancer cells in nude mice by S-1, a novel oral derivative of 5-Fluorouracil. Oncology 2003; 64(2):176-182.
173. Hiraga T, Ueda A, Tamura D, et al. Effects of oral UFT combined with or without zole-dronic acid on bone metastasis in the 4T1/luc mouse breast cancer. Int J Cancer 2003;106(6):973-979.
174. Herbst RS, Khuri FR. Mode of action of docetaxel-A basis for combination with novel anticancer agents. Cancer Treat Rev 2003;29(5):407-415.
175. Yen WC, Wientjes MG, Au JL. Differential effect of taxol in rat primary and metastatic prostate tumors: site-dependent pharmacodynamics. Pharm Res 1996;13(9):1305-1312.
176. Wang F, Cao Y, Zhao W, Liu H, Fu Z, Han R. Taxol inhibits melanoma metastases through apoptosis induction, angiogenesis inhibition, and restoration of E-cadherin and nm23 expression. J Pharmacol Sci 2003;93(2):197-203.
177. Jadeski LC, Chakraborty C, Lala PK. Role of nitric oxide in tumour progression with special reference to a murine breast cancer model. Can J Physiol Pharmacol 2002;80(2): 125-135.
178. Xie K, Huang S. Contribution of nitric oxide-mediated apoptosis to cancer metastasis inefficiency. Free Radic Biol Med 2003;34(8):969-986.
179. Dong Z, Staroselsky AH, Qi X, Xie K, Fidler IJ. Inverse correlation between expression of inducible nitric oxide synthase activity and production of metastasis in K-1735 murine melanoma cells. Cancer Res 1994;54(3):789-793.
180. Wang B, Wei D, Crum VE, et al. A novel model system for studying the double-edged roles of nitric oxide production in pancreatic cancer growth and metastasis. Oncogene 2003;22(12):1771-1782.
181. Jadeski LC, Hum KO, Chakraborty C, Lala PK. Nitric oxide promotes murine mammary tumour growth and metastasis by stimulating tumour cell migration, invasiveness and angiogenesis. Int J Cancer 2000;86(1):30-39.
182. Wei D, Richardson EL, Zhu K, et al. Direct demonstration of negative regulation of tumor growth and metastasis by host-inducible nitric oxide synthase. Cancer Res 2003;63(14): 3855-3529.
183. Shi Q, Xiong Q, Wang B, Le X, Khan NA, Xie K. Influence of nitric oxide synthase II gene disruption on tumor growth and metastasis. Cancer Res 2000;60(10):2579-2583.
184. Puhakka A, Kinnula V, Napankangas U, et al. High expression of nitric oxide synthases is a favorable prognostic sign in non-small cell lung carcinoma. Apmis 2003;111(12):1137-1146.
185. Bold R, Termuhlen P, McConkey D. Apoptosis, cancer and cancer therapy. Surg Oncol 1997;6(3):133-142.
186. Foster B, Coffey H, Morin M, Rastinejad F Pharmacological rescue of mutant p53 conformation and function. Science 1999;286(5449):2507-2510.
187. Zhang J. Apoptosis-based anticancer drugs. Nat Rev Drug Discov 2002;1(2):101-102.
188. Sova P, Ren X, Ni S, et al. A tumor-targeted and conditionally replicating oncolytic adenovirus vactor expressing TRAIL for treatment of liver metastases. Mol Ther 2003;9(4): 496-509.
189. Reed J. Apoptosis-targeted therapies for cancer. Cancer Cell 2003;3:17-22.
190. Ashkenazi A, Pai R, Fong S, et al. Safety and antitumor activity of recombinant soluble Apo2 ligand. J Clin Invest 1999;104(2):155-162.
191. Almond J, Cohen G. The proteasome: a novel target for cancer chemotherapy. Leukemia 2002;16:433-443.
192. Singh SK, Hawkins C, Clarke ID, et al. Identification of human brain tumour initiating cells. Nature 2004;432(7015):396-401.
193. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA 2003;100(7): 3983-3988.
194. Al-Hajj M, Clarke MF. Self-renewal and solid tumor stem cells. Oncogene 2004;23(43): 7274-7282.
195. Welm BE, Tepera SB, Venezia T, Graubert TA, Rosen JM, Goodell MA. Sca-1(pos) cells in the mouse mammary gland represent an enriched progenitor cell population. Dev Biol 2002;245(1):42-56.
196. Smalley M, Ashworth A. Stem cells and breast cancer: A field in transit. Nat Rev Cancer 2003;3(11):832-844.
197. Al-Hajj M, Becker MW, Wicha M, Weissman I, Clarke MF. Therapeutic implications of cancer stem cells. Curr Opin Genet Dev 2004;14(1):43-47.