Metastasis-suppressor genes in clinical practice: Lost in translation?

Nature Reviews Clinical Oncology

Volumn 8, Issue 6, 2011, Pages 333-342

  Shoushtari, Alexander N ^a   Szmulewitz, Russell Z ^a   Rinker Schaeffer, Carrie W ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CONNECTIVE TISSUE GROWTH FACTOR; GUANINE NUCLEOTIDE DISSOCIATION INHIBITOR; MEDROXYPROGESTERONE ACETATE; MESSENGER RNA; NUCLEOSIDE DIPHOSPHATE KINASE NM23; PHOSPHATIDYLETHANOLAMINE BINDING PROTEIN; PROTEIN; REVERSION INDUCING CYSTEINE RICH PROTEIN WITH KAZAL MOTIF; RHO GDP DISSOCIATION INHIBITOR BETA; UNCLASSIFIED DRUG;

BREAST CANCER; CANCER GROWTH; CANCER MORTALITY; CANCER RISK; CANCER SURVIVAL; CLINICAL PRACTICE; CTGF GENE; DRUG MEGADOSE; GENE EXPRESSION; HUMAN; METASTASIS SUPPRESSOR GENE; NM23 GENE; NONHUMAN; PATIENT CARE; PATIENT SELECTION; PEBP1 GENE; PHARMACOGENETICS; PRIORITY JOURNAL; PROGNOSIS; RECK GENE; REVIEW; RHOGDI2 GENE; SUPPRESSOR GENE; TREATMENT RESPONSE;

GENES, TUMOR SUPPRESSOR; HUMANS; NEOPLASM METASTASIS; NEOPLASMS; SIGNAL TRANSDUCTION;

EID: 79958072990     PISSN: 17594774     EISSN: 17594782     Source Type: Journal    
DOI: 10.1038/nrclinonc.2011.65     Document Type: Review

References (161)

1. 125I-5-iodo-2'-deoxyuridine. J. Natl Cancer Inst. 45, 773-782 (1970).
2. Fidler, I. J. Tumor heterogeneity and the biology of cancer invasion and metastasis. Cancer Res. 38, 2651-2660 (1978). (Pubitemid 9001502)
3. Chambers, A. F., Groom, A. C. & MacDonald, I. C. Dissemination and growth of cancer cells in metastatic sites. Nat. Rev. Cancer 2, 563-572 (2002). (Pubitemid 37328923)
4. Klein, C. A. The metastasis cascade. Science 321, 1785-1787 (2008).
5. Podsypanina, K. et al. Seeding and propagation of untransformed mouse mammary cells in the lung. Science 321, 1841-1844 (2008).
6. Marshall, J. C., Collins, J., Marino, N. & Steeg, P. The Nm23-H1 metastasis suppressor as a translational target. Eur. J. Cancer 46, 1278-1282 (2010).
7. Rinker-Schaeffer, C. W., O'Keefe, J. P., Welch, D. R. & Theodorescu, D. Metastasis suppressor proteins: discovery, molecular mechanisms, and clinical application. Clin. Cancer Res. 12, 3882-3889 (2006). (Pubitemid 44078070)
8. Smith, S. C. & Theodorescu, D. Learning therapeutic lessons from metastasis suppressor proteins. Nat. Rev. Cancer 9, 253-264 (2009).
9. Ludwig, J. A. & Weinstein, J. N. Biomarkers in cancer staging, prognosis and treatment selection. Nat. Rev. Cancer 5, 845-856 (2005). (Pubitemid 41746029)
10. Ross, J. S. et al. The Her-2/neu gene and protein in breast cancer 2003: biomarker and target of therapy. Oncologist 8, 307-325 (2003). (Pubitemid 36929717)
11. Sotiriou, C. & Pusztai, L. Gene-expression signatures in breast cancer. N. Engl. J. Med. 360, 790-800 (2009).
12. Paik, S. et al. A multigene assay to predict recurrence of tamoxifen-treated, node-negative breast cancer. N. Engl. J. Med. 351, 2817-2826 (2004). (Pubitemid 40051905)
13. Goldstein, L. J. et al. Prognostic utility of the 21-gene assay in hormone receptor-positive operable breast cancer compared with classical clinicopathologic features. J. Clin. Oncol. 26, 4063-4071 (2008).
14. Mamounas, E. P. et al. Association between the 21-gene recurrence score assay and risk of locoregional recurrence in node-negative, estrogen receptor-positive breast cancer: results from NSABP B-14 and NSABP B-20. J. Clin. Oncol. 28, 1677-1683 (2010).
15. Carlson, R. W. et al. Breast cancer. Clinical practice guidelines in oncology. J. Natl Compr. Canc. Netw. 7, 122-192 (2009).
16. van 't Veer, L. J. et al. Gene expression profiling predicts clinical outcome of breast cancer. Nature 415, 530-536 (2002).
17. van de Vijver, M. H. et al. A gene-expression signature as a predictor of survival in breast cancer. N. Engl. J. Med. 347, 1999-2009 (2002).
18. Straver, M. E. et al. The 70-gene signature as a response predictor for neoadjuvant chemotherapy in breast cancer. Breast Cancer Res. Treat. 119, 551-558 (2010).
19. Steeg, P. S., Horak, C. E. & Miller, K. D. Clinical-translational approaches to the Nm23-H1 metastasis suppressor. Clin. Cancer Res. 14, 5006-5012 (2008).
20. Bevilacqua, G., Sobel, M. E., Liotta, L. A. & Steeg, P. S. Association of low nm23 RNA levels in human primary infiltrating ductal breast carcinomas with lymph node involvement and other histopathological indicators of high metastatic potential. Cancer Res. 49, 5185-5190 (1989). (Pubitemid 19239366)
21. Hennessy, C. et al. Expression of the antimetastatic gene nm23 in human breast cancer: an association with good prognosis. J. Natl Cancer Inst. 83, 281-285 (1991).
22. Toulas, C. et al. Potential prognostic value in human breast cancer of cytosolic Nme1 protein detection using an original hen specific antibody. Br. J. Cancer 73, 630-635 (1996). (Pubitemid 26068868)
23. Charpin, C. et al. Prognostic significance of Nm23/NDPK expression in breast carcinoma, assessed on 10-year follow-up by automated and quantitative immunocytochemical assays. J. Pathol. 184, 401-407 (1998). (Pubitemid 28179899)
24. Leone, A. et al. Somatic allelic deletion of nm23 in human cancer. Cancer Res. 51, 2490-2493 (1991).
25. Cropp, C. S. et al. NME1 protein expression and loss of heterozygosity mutations in primary human breast tumors. J. Natl Cancer Inst. 86, 1167-1169 (1994). (Pubitemid 24249303)
26. Ouatas, T., Clare, S. E., Hartsough, M. T., De La Rosa, A. & Steeg, P. S. MMTV-associated transcription factor binding sites increase nm23-H1 metastasis suppressor gene expression in human breast carcinoma cell lines. Clin. Exp. Metastasis 19, 35-42 (2002). (Pubitemid 34208352)
27. Qu, S. et al. Genetic polymorphisms of metastasis suppressor gene NME1 and breast cancer survival. Clin. Cancer Res. 14, 4787-4793 (2008).
28. Zafon, C. et al. nm23-H1 immunoreactivity as a prognostic factor in differentiated thyroid carcinoma. J. Clin. Endocrinol. Metab. 86, 3975-3980 (2001). (Pubitemid 32756007)
29. Wang, L. S., Chow, K. C., Lien, Y. C., Kuo, K. T. & Li, W. Y. Prognostic significance of nm23-H1 expression in esophageal squamous cell carcinoma. Eur. J. Cardiothorac. Surg. 26, 419-424 (2004).
30. Iizuka, N. et al. NM23-H1 and NM23-H2 messenger RNA abundance in human hepatocellular carcinoma. Cancer Res. 55, 652-657 (1995).
31. Hsu, N. Y. et al. Expression of nm23 in the primary tumor and the metastatic regional lymph nodes of patients with gastric cardiac cancer. Clin. Cancer Res. 5, 1752-1757 (1999).
32. Niitsu, N., Nakamine, H., Okamoto, M., Tamaru, J. I. & Hirano, M. A clinicopathological study of nm23-H1 expression in classical Hodgkin's lymphoma. Ann. Oncol. 19, 1941-1946 (2008).
33. Viel, A. et al. Suppressive role of the metastasis-related nm23-H1 gene in human ovarian carcinomas: association of high messenger RNA expression with lack of lymph node metastasis. Cancer Res. 55, 2645-2650 (1995).
34. Scambia, G. et al. nm23 in ovarian cancer: correlation with clinical outcome and other clinicopathologic and biochemical prognostic parameters. J. Clin. Oncol. 14, 334-342 (1996). (Pubitemid 26053263)
35. Schneider, J. et al. nm23-H1 expression defines a high-risk subpopulation of patients with early-stage epithelial ovarian carcinoma. Br. J. Cancer 82, 1662-1670 (2000). (Pubitemid 30229576)
36. Youn, B. S. et al. NM23 as a prognostic biomarker in ovarian serous carcinoma. Mod. Pathol. 21, 885-892 (2008). (Pubitemid 351896663)
37. Hailat, N. et al. High levels of p19/nm23 protein in neuroblastoma are associated with advanced stage disease and with N-myc gene amplification. J. Clin. Invest. 88, 341-345 (1991).
38. Nakamori, S. et al. Expression of nucleoside diphosphate kinase/nm23 gene product in human pancreatic cancer: an association with lymph node metastasis and tumor invasion. Clin. Exp. Metastasis 11, 151-158 (1993). (Pubitemid 23080158)
39. Kitayama, H., Sugimoto, Y., Matsuzaki, T., Ikawa, Y. & Noda, M. A ras-related gene with transformation suppressor activity. Cell 56, 77-84 (1989). (Pubitemid 19033515)
40. Oh, J. et al. The membrane-anchored MMP inhibitor RECK is a key regulator of extracellular matrix integrity and angiogenesis. Cell 107, 789-800 (2001). (Pubitemid 34033671)
41. Takeuchi, T. et al. The membrane-anchored matrix metalloproteinase (MMP) regulator RECK in combination with MMP-9 serves as an informative prognostic indicator for colorectal cancer. Clin. Cancer Res. 10, 5572-5579 (2004). (Pubitemid 39100498)
42. van der Jagt, M. F. et al. Correlation of reversion-inducing cysteine-rich protein with kazal motifs (RECK) and extracellular matrix metalloproteinase inducer (EMMPRIN), with MMP-2, MMP-9, and survival in colorectal cancer. Cancer Lett. 237, 289-297 (2006).
43. Masui, T. et al. RECK expression in pancreatic cancer: its correlation with lower invasiveness and better prognosis. Clin. Cancer Res. 9, 1779-1784 (2003). (Pubitemid 36554604)
44. Span, P. N. et al. Matrix metalloproteinase inhibitor reversion-inducing cysteine-rich protein with Kazal motifs: a prognostic marker for good clinical outcome in human breast carcinoma. Cancer 97, 2710-2715 (2003). (Pubitemid 36605137)
45. Takenaka, K. et al. Expression of a novel matrix metalloproteinase regulator, RECK, and its clinical significance in resected non-small cell lung cancer. Eur. J. Cancer 40, 1617-1623 (2004). (Pubitemid 38757753)
46. Riddick, A. C. et al. Identification of degradome components associated with prostate cancer progression by expression analysis of human prostatic tissues. Br. J. Cancer 92, 2171-2180 (2005). (Pubitemid 40966253)
47. Schuierer, M. M., Bataille, F., Hagan, S., Kolch, W. & Bosserhoff, A. K. Reduction in Raf kinase inhibitor protein expression is associated with increased Ras-extracellular signal-regulated kinase signaling in melanoma cell lines. Cancer Res. 64, 5186-5192 (2004). (Pubitemid 39006537)
48. Fu, Z. et al. Effects of raf kinase inhibitor protein expression on suppression of prostate cancer metastasis. J. Natl Cancer Inst. 95, 878-889 (2003). (Pubitemid 36833879)
49. Al-Mulla, F. et al. Raf kinase inhibitor protein expression in a survival analysis of colorectal cancer patients. J. Clin. Oncol. 24, 5672-5679 (2006). (Pubitemid 46631308)
50. Hagan, S. et al. Reduction of Raf-1 kinase inhibitor protein expression correlates with breast cancer metastasis. Clin. Cancer Res. 11, 7392-7397 (2005). (Pubitemid 41507699)
51. Fu, Z. et al. Metastasis suppressor gene Raf kinase inhibitor protein (RKIP) is a novel prognostic marker in prostate cancer. Prostate 66, 248-256 (2006). (Pubitemid 43191224)
52. + tumor-infiltrating lymphocytes. Clin. Cancer Res. 14, 3792-3797 (2008).
53. Chang, C. C. et al. Connective tissue growth factor and its role in lung adenocarcinoma invasion and metastasis. J. Natl Cancer Inst. 96, 364-375 (2004).
54. Chen, P. P. et al. Expression of Cyr61, CTGF, and WISP-1 correlates with clinical features of lung cancer. PLoS ONE 2, e534 (2007).
55. Lin, B. R. et al. Connective tissue growth factor inhibits metastasis and acts as an independent prognostic marker in colorectal cancer. Gastroenterology 128, 9-23 (2005).
56. Alvarez, H. et al. Serial analysis of gene expression identifies connective tissue growth factor expression as a prognostic biomarker in gallbladder cancer. Clin. Cancer Res. 14, 2631-2638 (2008).
57. Liu, L. Y., Han, Y. C., Wu, S. H. & Lv, Z. H. Expression of connective tissue growth factor in tumor tissues is an independent predictor of poor prognosis in patients with gastric cancer. World J. Gastroenterol. 14, 2110-2114 (2008).
58. Dornhöfer, N. et al. Connective tissue growth factor-specific monoclonal antibody therapy inhibits pancreatic tumor growth and metastasis. Cancer Res. 66, 5816-5827 (2006). (Pubitemid 43927136)
59. Kang, Y. et al. A multigenic program mediating breast cancer metastasis to bone. Cancer Cell 3, 537-549 (2003). (Pubitemid 36808649)
60. Gildea, J. J. et al. RhoGDI2 is an invasion and metastasis suppressor gene in human cancer. Cancer Res. 62, 6418-6423 (2002). (Pubitemid 35364098)
61. Harding, M. A. et al. Functional genomic comparison of lineage-related human bladder cancer cell lines with differing tumorigenic and metastatic potentials by spectral karyotyping, comparative genomic hybridization, and a novel method of positional expression profiling. Cancer Res. 62, 6981-6989 (2002). (Pubitemid 35424090)
62. Theodorescu, D. et al. Reduced expression of metastasis suppressor RhoGDI2 is associated with decreased survival for patients with bladder cancer. Clin. Cancer Res. 10, 3800-3806 (2004). (Pubitemid 38697615)
63. Cho, H. J. et al. RhoGDI2 expression is associated with tumor growth and malignant progression of gastric cancer. Clin. Cancer Res. 15, 2612-2619 (2009).
64. Ferguson, A. W. et al. Increased sensitivity to cisplatin by nm23-transfected tumor cell lines. Cancer Res. 56, 2931-2935 (1996). (Pubitemid 26199734)
65. Iizuka, N. et al. The nm23-H1 gene as a predictor of sensitivity to chemotherapeutic agents in oesophageal squamous cell carcinoma. Br. J. Cancer 81, 469-475 (1999). (Pubitemid 29458801)
66. Titus, B. et al. Endothelin axis is a target of the lung metastasis suppressor gene RhoGDI2. Cancer Res. 65, 7320-7327 (2005). (Pubitemid 41161264)
67. Ouatas, T., Halverson, D. & Steeg, P. S. Dexamethasone and medroxyprogesterone acetate elevate Nm23-H1 metastasis suppressor gene expression in metastatic human breast carcinoma cells: new uses for old compounds. Clin. Cancer Res. 9, 3763-3772 (2003). (Pubitemid 37169246)
68. Palmieri, D. et al. Medroxyprogesterone acetate elevation of Nm23-H1 metastasis suppressor expression in hormone receptor-negative breast cancer. J. Natl Cancer Inst. 97, 632-642 (2005).
69. Horak, C. E. et al. Nm23-H1 suppresses tumor cell motility by down-regulating the lysophosphatidic acid receptor EDG2. Cancer Res. 67, 7238-7246 (2007). (Pubitemid 47206552)
70. Horak, C. E. et al. Nm23-H1 suppresses metastasis by inhibiting expression of the lysophosphatidic acid receptor EDG2. Cancer Res. 67, 11751-11759 (2007).
71. Boucharaba, A. et al. The type 1 lysophosphatidic acid receptor is a target for therapy in bone metastases. Proc. Natl Acad. Sci. USA 103, 9643-9648 (2006). (Pubitemid 43955878)
72. Carducci, M. A. et al. Effect of endothelin-A receptor blockade with atrasentan on tumor progression in men with hormone-refractory prostate cancer: a randomized, phase II, placebo-controlled trial. J. Clin. Oncol. 21, 679-689 (2003). (Pubitemid 46621903)
73. Nelson, J. B. et al. Phase 3, randomized, controlled trial of atrasentan in patients with nonmetastatic, hormone-refractory prostate cancer. Cancer 113, 2478-2487 (2008).
74. Jennings, L., Van Deerlin, V. M. & Gulley, M. L. Recommended principles and practices for validating clinical molecular pathology tests. Arch. Pathol. Lab. Med. 133, 743-755 (2009).
75. Khleif, S. N., Doroshow, J. H. & Hait, W. N. AACR-FDA-NCI Cancer Biomarkers Collaborative consensus report: advancing the use of biomarkers in cancer drug development. Clin. Cancer Res. 16, 3299-3318 (2010).
76. Luo, J., Solimini, N. L. & Elledge, S. J. Principles of cancer therapy: oncogene and non-oncogene addiction. Cell 136, 823-837 (2009).
77. Weinstein, I. B. & Joe, A. K. Mechanisms of disease: Oncogene addiction - a rationale for molecular targeting in cancer therapy. Nat. Clin. Pract. Oncol. 3, 448-457 (2006). (Pubitemid 44203817)
78. Ohtaki, T. et al. Metastasis suppressor gene KiSS-1 encodes peptide ligand of a G-protein-coupled receptor. Nature 411, 613-617 (2001). (Pubitemid 32531412)
79. Al-Mulla, F. et al. Raf kinase inhibitor protein RKIP enhances signaling by glycogen synthase kinase-3β. Cancer Res. 71, 1334-1343 (2011).
80. 2-terminal kinase activating kinase 1/mitogen-activated protein kinase kinase 4-mediated inhibition of SKOV3ip.1 ovarian cancer metastasis involves growth arrest and p21 up-regulation. Cancer Res. 68, 2166-2175 (2008). (Pubitemid 351521789)
81. 2-terminal kinase kinases JNKK1/MKK4 and MKK7. Cancer Res. 65, 10984-10991 (2005). (Pubitemid 41713368)
82. Alderisio, M. et al. Nm23-H1 protein, DNA-ploidy and S-phase fraction in relation to overall survival and disease free survival in transitional cell carcinoma of the bladder. Anticancer Res. 18, 4225-4230 (1998). (Pubitemid 29043638)
83. Chow, N. H., Liu, H. S. & Chan, S. H. The role of nm23-H1 in the progression of transitional cell bladder cancer. Clin. Cancer Res. 6, 3595-3599 (2000).
84. Heimann, R., Ferguson, D. J. & Hellman, S. The relationship between nm23, angiogenesis, and the metastatic proclivity of node-negative breast cancer. Cancer Res. 58, 2766-2771 (1998). (Pubitemid 28311906)
85. Royds, J. A., Stephenson, T. J., Rees, R. C., Shorthouse, A. J. & Silcocks, P. B. Nm23 protein expression in ductal in situ and invasive human breast carcinoma. J. Natl Cancer Inst. 85, 727-731 (1993). (Pubitemid 23133594)
86. Tokunaga, Y. et al. Reduced expression of nm23-H1, but not of nm23-H2, is concordant with the frequency of lymph-node metastasis of human breast cancer. Int. J. Cancer 55, 66-71 (1993). (Pubitemid 23261708)
87. Cohn, K. H. et al. Association of nm23-H1 allelic deletions with distant metastases in colorectal carcinoma. Lancet 338, 722-724 (1991).
88. Dursun, A., Akyürek, N., Gunel, N. & Yamac, D. Prognostic implication of nm23-H1 expression in colorectal carcinomas. Pathology 34, 427-432 (2002). (Pubitemid 35205244)
89. Bertucci, F. et al. Gene expression profiling of colon cancer by DNA microarrays and correlation with histoclinical parameters. Oncogene 23, 1377-1391 (2004). (Pubitemid 38406833)
90. Myeroff, L. L. & Markowitz, S. D. Increased nm23-H1 and nm23-H2 messenger RNA expression and absence of mutations in colon carcinomas of low and high metastatic potential. J. Natl Cancer Inst. 85, 147-152 (1993). (Pubitemid 23028719)
91. Lamb, R. F., Going, J. J., Pickford, I. & Birnie, G. D. Allelic imbalance at NME1 in microdissected primary and metastatic human colorectal carcinomas is frequent but not associated with metastasis to lymph nodes or liver. Cancer Res. 56, 916-920 (1996). (Pubitemid 26055485)
92. Günther, K. et al. Prediction of distant metastases after curative surgery for rectal cancer. J. Surg. Res. 103, 68-78 (2002). (Pubitemid 34953394)
93. Berney, C. R., Fisher, R. J., Yang, J., Russell, P. J. & Crowe, P. J. Protein markers in colorectal cancer: predictors of liver metastasis. Ann. Surg. 230, 179-184 (1999). (Pubitemid 30191883)
94. Kodera, Y. et al. Expression of nm23 H-1 RNA levels in human gastric cancer tissues. A negative correlation with nodal metastasis. Cancer 73, 259-265 (1994). (Pubitemid 24030599)
95. Müller, W., Schneiders, A., Hommel, G. & Gabbert, H. E. Expression of nm23 in gastric carcinoma: association with tumor progression and poor prognosis. Cancer 83, 2481-2487 (1998). (Pubitemid 29019566)
96. Gunduz, M. et al. nm23 Protein expression in larynx cancer and the relationship with metastasis. Eur. J. Cancer 33, 2338-2341 (1997). (Pubitemid 28129173)
97. Guo, X. et al. nm23-H1 expression in nasopharyngeal carcinoma: correlation with clinical outcome. Int. J. Cancer 79, 596-600 (1998). (Pubitemid 28549470)
98. Wang, Y. F. et al. Prognostic significance of nm23-H1 expression in oral squamous cell carcinoma. Br. J. Cancer 90, 2186-2193 (2004).
99. Yamaguchi, A. et al. Expression of human nm23-H1 and nm23-H2 proteins in hepatocellular carcinoma. Cancer 73, 2280-2284 (1994). (Pubitemid 24129109)
100. Guo, H. et al. Prognostic significance of co-expression of nm23 and p57 protein in hepatocellular carcinoma. Hepatol. Res. 40, 1107-1116 (2010).
101. An, R. et al. Expressions of nucleoside diphosphate kinase (nm23) in tumor tissues are related with metastasis and length of survival of patients with hepatocellular carcinoma. Biomed. Environ. Sci. 23, 267-272 (2010).
102. Sarris, M. et al. Cytoplasmic expression of nm23 predicts the potential for cerebral metastasis in patients with primary cutaneous melanoma. Melanoma Res. 14, 23-27 (2004). (Pubitemid 38392410)
103. Döme, B., Somlai, B. & Timár, J. The loss of NM23 protein in malignant melanoma predicts lymphatic spread without affecting survival. Anticancer Res. 20, 3971-3974 (2000). (Pubitemid 32002307)
104. Xerri, L. et al. NM23 expression in metastasis of malignant melanoma is a predictive prognostic parameter correlated with survival. Br. J. Cancer 70, 1224-1228 (1994). (Pubitemid 24358967)
105. Pacifico, M. D. et al. nm23 as a prognostic marker in primary cutaneous melanoma: evaluation using tissue microarray in a patient group with long-term follow-up. Melanoma Res. 15, 435-440 (2005). (Pubitemid 41558954)
106. Kawakubo, Y., Sato, Y., Koh, T., Kono, H. & Kameya, T. Expression of nm23 protein in pulmonary adenocarcinomas: inverse correlation to tumor progression. Lung Cancer 17, 103-113 (1997). (Pubitemid 27261495)
107. Ohta, Y., Nozawa, H., Tanaka, Y., Oda, M. & Watanabe, Y. Increased vascular endothelial growth factor and vascular endothelial growth factor-c and decreased nm23 expression associated with microdissemination in the lymph nodes in stage I non-small cell lung cancer. J. Thorac. Cardiovasc. Surg. 119, 804-813 (2000). (Pubitemid 30395479)
108. Goncharuk, V. N. et al. Co-downregulation of PTEN, KAI-1, and nm23-H1 tumor/metastasis suppressor proteins in non-small cell lung cancer. Ann. Diagn. Pathol. 8, 6-16 (2004). (Pubitemid 38199173)
109. Hsu, N. Y. et al. Prognostic significance of expression of nm23-H1 and focal adhesion kinase in non-small cell lung cancer. Oncol. Rep. 18, 81-85 (2007).
110. Baekelandt, M., Holm, R., Tropé, C. G., Nesland, J. M. & Kristensen, G. B. The significance of metastasis-related factors cathepsin-D and nm23 in advanced ovarian cancer. Ann. Oncol. 10, 1335-1341 (1999).
111. Tas, F. et al. Prognostic role of nm23 gene expression in patients with ovarian cancer. Am. J. Clin. Oncol. 25, 164-167 (2002). (Pubitemid 34293070)
112. Ohshio, G. et al. Immunohistochemical expression of nm23 gene product, nucleotide diphosphate kinase, in pancreatic neoplasms. Int. J. Pancreatol. 22, 59-66 (1997). (Pubitemid 27494938)
113. Chatterjee, D., Sabo, E., Tavares, R. & Resnick, M. B. Inverse association between Raf Kinase Inhibitory Protein and signal transducers and activators of transcription 3 expression in gastric adenocarcinoma patients: implications for clinical outcome. Clin. Cancer Res. 14, 2994-3001 (2008).
114. Martinho, O. et al. Loss of RKIP expression is associated with poor survival in GISTs. Virchows Arch. 455, 277-284 (2009).
115. Ruan, L. et al. Raf kinase inhibitor protein correlates with sensitivity of nasopharyngeal carcinoma to radiotherapy. J. Cell Biochem. 110, 975-981 (2010).
116. Xu, Y. F. et al. PEBP1 downregulation is associated to poor prognosis in HCC related to hepatitis B infection. J. Hepatol. 53, 872-879 (2010).
117. Wu, Z., Conaway, M., Gioeli, D., Weber, M. J. & Theodorescu, D. Conditional expression of PTEN alters the androgen responsiveness of prostate cancer cells. Prostate 66, 1114-1123 (2006). (Pubitemid 43939216)
118. Song, S. Y., Son, H. J., Nam, E., Rhee, J. C. & Park, C. Expression of reversion-inducing-cysteine-rich protein with Kazal motifs (RECK) as a prognostic indicator in gastric cancer. Eur. J. Cancer 42, 101-108 (2006). (Pubitemid 41814539)
119. Namwat, N. et al. Downregulation of reversion-inducing-cysteine-rich protein with Kazal motifs (RECK) is associated with enhanced expression of matrix metalloproteinases and cholangiocarcinoma metastases. J. Gastroenterol. doi:10.1007/s00535-010-0345-y.
120. Takenaka, K. et al. Prognostic significance of reversion-inducing cysteine-rich protein with Kazal motifs expression in resected pathologic stage IIIA N2 non-small-cell lung cancer. Ann. Surg. Oncol. 12, 817-824 (2005). (Pubitemid 41355934)
121. Rabien, A. et al. Decreased RECK expression indicating proteolytic imbalance in prostate cancer is associated with higher tumor aggressiveness and risk of prostate-specific antigen relapse after radical prostatectomy. Eur. Urol. 51, 1259-1266 (2007). (Pubitemid 46436286)
122. Zhou, Z. Q. et al. Expression and prognostic significance of THBS1, Cyr61 and CTGF in esophageal squamous cell carcinoma. BMC Cancer 9, 291 (2009).
123. Xie, D. et al. Levels of expression of CYR61 and CTGF are prognostic for tumor progression and survival of individuals with gliomas. Clin. Cancer Res. 10, 2072-2081 (2004). (Pubitemid 38375569)
124. Huang, C. I. et al. Correlation of reduction in MRP-1/CD9 and KAI1/CD82 expression with recurrences in breast cancer patients. Am. J. Pathol. 153, 973-983 (1998).
125. Muneyuki, T., Watanabe, M., Yamanaka, M., Shiraishi, T. & Isaji, S. KAI1/CD82 expression as a prognosic factor in sporadic colorectal cancer. Anticancer Res. 21, 3581-3587 (2001). (Pubitemid 34224268)
126. Hashida, H. et al. Clinical significance of transmembrane 4 superfamily in colon cancer. Br. J. Cancer 89, 158-167 (2003). (Pubitemid 36897952)
127. Liu, F. S. et al. KAI1 metastasis suppressor protein is down-regulated during the progression of human endometrial cancer. Clin. Cancer Res. 9, 1393-1398 (2003).
128. Farhadieh, R. D. et al. Down-regulation of KAI1/CD82 protein expression in oral cancer correlates with reduced disease free survival and overall patient survival. Cancer Lett. 213, 91-98 (2004). (Pubitemid 39127412)
129. Adachi, M. et al. Correlation of KAI1/CD82 gene expression with good prognosis in patients with non-small cell lung cancer. Cancer Res. 56, 1751-1755 (1996). (Pubitemid 26118208)
130. Adachi, M. et al. Novel staging protocol for non-small-cell lung cancers according to MRP-1/CD9 and KAI1/CD82 gene expression. J. Clin. Oncol. 16, 1397-1406 (1998). (Pubitemid 28175757)
131. Schindl, M., Birner, P., Breitenecker, G. & Oberhuber, G. Downregulation of KAI1 metastasis suppressor protein is associated with a dismal prognosis in epithelial ovarian cancer. Gynecol. Oncol. 83, 244-248 (2001). (Pubitemid 33033060)
132. Liu, F. S. et al. Frequent down-regulation and lack of mutation of the KAI1 metastasis suppressor gene in epithelial ovarian carcinoma. Gynecol. Oncol. 78, 10-15 (2000).
133. Sho, M. et al. Transmembrane 4 superfamily as a prognostic factor in pancreatic cancer. Int. J. Cancer 79, 509-516 (1998). (Pubitemid 28445274)
134. Sanchez-Carbayo, M. et al. Gene discovery in bladder cancer progression using cDNA microarrays. Am. J. Pathol. 163, 505-516 (2003). (Pubitemid 36909413)
135. Marot, D. et al. High tumoral levels of Kiss1 and G-protein-coupled receptor 54 expression are correlated with poor prognosis of estrogen receptor-positive breast tumors. Endocr. Relat. Cancer 14, 691-702 (2007). (Pubitemid 350074058)
136. Ikeguchi, M., Yamaguchi, K. & Kaibara, N. Clinical significance of the loss of KiSS-1 and orphan G-protein-coupled receptor (hOT7T175) gene expression in esophageal squamous cell carcinoma. Clin. Cancer Res. 10, 1379-1383 (2004). (Pubitemid 38365232)
137. Dhar, D. K. et al. Downregulation of KiSS-1 expression is responsible for tumor invasion and worse prognosis in gastric carcinoma. Int. J. Cancer 111, 868-872 (2004). (Pubitemid 39096235)
138. Ikeguchi, M., Hirooka, Y. & Kaibara, N. Quantitative reverse transcriptase polymerase chain reaction analysis for KiSS-1 and orphan G-protein-coupled receptor (hOT7T175) gene expression in hepatocellular carcinoma. J. Cancer Res. Clin. Oncol. 129, 531-535 (2003). (Pubitemid 37211194)
139. Schmid, K. et al. KiSS-1 overexpression as an independent prognostic marker in hepatocellular carcinoma: an immunohistochemical study. Virchows Arch. 450, 143-149 (2007). (Pubitemid 46295235)
140. Zheng, S. et al. Expression of KISS1 and MMP-9 in non-small cell lung cancer and their relations to metastasis and survival. Anticancer Res. 30, 713-718 (2010).
141. Prentice, L. M. et al. Kisspeptin and GPR54 immunoreactivity in a cohort of 518 patients defines favourable prognosis and clear cell subtype in ovarian carcinoma. BMC Med. 5, 33 (2007).
142. Hu, L. D., Zou, H. F., Zhan, S. X. & Cao, K. M. Biphasic expression of RhoGDI2 in the progression of breast cancer and its negative relation with lymph node metastasis. Oncol. Rep. 17, 1383-1389 (2007).
143. Kim, H. L. et al. Mitogen-activated protein kinase kinase 4 metastasis suppressor gene expression is inversely related to histological pattern in advancing human prostatic cancers. Cancer Res. 61, 2833-2837 (2001). (Pubitemid 32691920)
144. Lotan, T. L. et al. Up-regulation of MKK4, MKK6 and MKK7 during prostate cancer progression: an important role for SAPK signalling in prostatic neoplasia. J. Pathol. 212, 386-394 (2007). (Pubitemid 47099015)
145. Zhang, Z. et al. Reduced expression of the breast cancer metastasis suppressor 1 mRNA is correlated with poor progress in breast cancer. Clin. Cancer Res. 12, 6410-6414 (2006). (Pubitemid 44799712)
146. Pingoud-Meier, C. et al. Loss of caspase-8 protein expression correlates with unfavorable survival outcome in childhood medulloblastoma. Clin. Cancer Res. 9, 6401-6409 (2003). (Pubitemid 38031826)
147. Fulda, S. et al. Loss of caspase-8 expression does not correlate with MYCN amplification, aggressive disease, or prognosis in neuroblastoma. Cancer Res. 66, 10016-10023 (2006). (Pubitemid 44672054)
148. Lujambio, A. et al. A microRNA DNA methylation signature for human cancer metastasis. Proc. Natl Acad. Sci. USA 105, 13556-13561 (2008).
149. Tavazoie, S. F. et al. Endogenous human microRNAs that suppress breast cancer metastasis. Nature 451, 147-152 (2008).
150. Yanaihara, N. et al. Unique microRNA molecular profiles in lung cancer diagnosis and prognosis. Cancer Cell 9, 189-198 (2006). (Pubitemid 43357945)
151. Li, J. et al. Inhibition of ovarian cancer metastasis by adeno-associated virus-mediated gene transfer of nm23H1 in an orthotopic implantation model. Cancer Gene Ther. 13, 266-272 (2006). (Pubitemid 43255763)
152. Li, Z. et al. Nanoparticle delivery of anti-metastatic NM23-H1 gene improves chemotherapy in a mouse tumor model. Cancer Gene Ther. 16, 423-429 (2009).
153. Xu, J. H., Guo, X. Z., Ren, L. N., Shao, L. C. & Liu, M. P. KAI1 is a potential target for anti-metastasis in pancreatic cancer cells. World J. Gastroenterol. 14, 1126-1132 (2008).
154. Takeda, T. et al. Adenoviral transduction of MRP-1/CD9 and KAI1/CD82 inhibits lymph node metastasis in orthotopic lung cancer model. Cancer Res. 67, 1744-1749 (2007). (Pubitemid 46383401)
155. Bandyopadhyay, S. et al. PTEN up-regulates the tumor metastasis suppressor gene Drg-1 in prostate and breast cancer. Cancer Res. 64, 7655-7660 (2004). (Pubitemid 39446890)
156. Wu, Y. et al. Src phosphorylation of RhoGDI2 regulates its metastasis suppressor function. Proc. Natl Acad. Sci. USA 106, 5807-5812 (2009).
157. Bandyopadhyay, S. et al. Role of the putative tumor metastasis suppressor gene Drg-1 in breast cancer progression. Oncogene 23, 5675-5681 (2004). (Pubitemid 39093045)
158. Hartsough, M. T. et al. Elevation of breast carcinoma Nm23-H1 metastasis suppressor gene expression and reduced motility by DNA methylation inhibition. Cancer Res. 61, 2320-2327 (2001). (Pubitemid 32692066)
159. Beach, S. et al. Snail is a repressor of RKIP transcription in metastatic prostate cancer cells. Oncogene 27, 2243-2248 (2008). (Pubitemid 351483382)
160. Baritaki, S. et al. Inhibition of epithelial to mesenchymal transition in metastatic prostate cancer cells by the novel proteasome inhibitor, NPI-0052: pivotal roles of Snail repression and RKIP induction. Oncogene 28, 3573-3585 (2009).
161. Baritaki, S., Yeung, K., Palladino, M., Berenson, J. & Bonavida, B. Pivotal roles of snail inhibition and RKIP induction by the proteasome inhibitor NPI-0052 in tumor cell chemoimmuno-sensitization. Cancer Res. 69, 8376-8385 (2009).