Metastasis Suppressors and the Tumor Microenvironment

Wolf K, Wu YI, Liu Y et al (2007) Multi-step pericellular proteolysis controls the transition from individual to collective cancer cell invasion. Nat Cell Biol 9:893–904

Friedl P, Wolf K (2003) Tumour-cell invasion and migration: Diversity and escape mechanisms. Nat Rev Cancer 3:362–374

Weiss L, Orr FW, Honn KW (1989) Interactions between cancer cells and the microvasculature: A rate regulator for metastasis. Clin Exp Metastasis 7:127–167

Weiss L (1990) Metastatic inefficiencyAdv Cancer Res. 54:159–211

Rennebeck G, Martelli M, Kyprianou N (2005) Anoikis and survival connections in the tumor microenvironment: Is there a role in prostate cancer metastasis? Cancer Res 65:11230–11235

Wang SL, El-Deiry WS (2003) TRAIL and apoptosis induction by TNF-family death receptors. Oncogene 22:8628–8633

Fidler IJ (1974) Immune stimulation-inhibition of experimental cancer metastasis. Cancer Res 34:491–498

Hehlgans S, Haase M, Cordes N (2007) Signalling via integrins: Implications for cell survival and anticancer strategies. Biochim Biophys Acta Rev Cancer 1775:163–180

Cavallaro U, Christofori G (2001) Cell adhesion in tumor invasion and metastasis: loss of the glue is not enough. Biochim Biophys Acta Rev Cancer 1552:39–45

Pauli BU, Augustin-Voss HG, El-Sabban ME et al (1990) Organ-preference of metastasis. The role of endothelial cell adhesion molecules. Cancer Metastasis Rev 9:175–189

Nicolson GL (1988) Organ specificity of tumor metastasis: role of preferential adhesion, invasion and growth of malignant cells at specific secondary sites. Cancer Metastasis Rev 7:143–188

Hart IR (1982) “Seed and soil” revisited: mechanisms of site-specific metastasis. Cancer Metastasis Rev 1:5–16

Ruffini PA, Morandi P, Cabioglu N et al (2007) Manipulating the chemokine–chemokine receptor network to treat cancer. Cancer 109:2392–2404

Naumov GN, MacDonald IC, Chambers AF et al (2001) Solitary cancer cells as a possible source of tumour dormancy? Semin Cancer Biol 11:271–276

Al Mehdi AB, Tozawa K, Fisher AB et al (2000) Intravascular origin of metastasis from the proliferation of endothelium-attached tumor cells: a new model for metastasis. Nat Med 6:100–102

Townson JL, Chambers AF (2006) Dormancy of solitary metastatic cells. Cell Cycle 5:1744–1750

Chambers AF, Groom AC, MacDonald IC (2002) Dissemination and growth of cancer cells in metastatic sites. Nat Rev Cancer 2:563–572

Eccles SA, Welch DR (2007) Metastasis: recent discoveries and novel treatment strategies. Lancet 369:1742–1757

Welch DR (2007) Do we need to redefine a cancer metastasis and staging definitions? Breast Disease 26:3–12

Chambers AF, Matrisian LM (1997) Changing views of the role of matrix metalloproteinases in metastasis. J Natl Cancer Inst 89:1260–1270

Vaidya KS, Welch DR (2007) Metastasis suppressors and their roles in breast carcinoma. J Mamm Gland Biol Neopl 12:175–190

Rinker-Schaeffer CW, O’Keefe JP, Welch DR et al (2006) Metastasis suppressor proteins: Discovery, Molecular mechanisms and Clinical Application. Clin Cancer Res 12:3382–3389

Guarino M, Rubino B, Ballabio G (2007) The role of epithelial–mesenchymal transition in cancer pathology. Pathology 39:305–318

Graff JR, Gabrielson E, Fujii H et al (2000) Methylation patterns of the E-cadherin 5′ CpG island are unstable and reflect the dynamic, heterogeneous loss of E-cadherin expression during metastatic progression. J Biol Chem 275:2727–2732

Graff JR, Greenberg VE, Herman JG et al (1998) Distinct patterns of E-cadherin CpG island methylation in papillary, follicular, Hurthle’s cell, and poorly differentiated human thyroid carcinoma. Cancer Res 58:2063–2066

Hugo H, Ackland ML, Blick T et al (2007) Epithelial–mesenchymal and mesenchymal–epithelial transitions in carcinoma progression. J Cell Physiol 213:374–383

Potter JD (2007) Morphogens, morphostats, microarchitecture and malignancy. Nat Rev Cancer 7:464–474

Hay ED (2005) The mesenchymal cell, its role in the embryo, and the remarkable signaling mechanisms that create it. Dev Dyn 233:706–720

Thiery JP (2002) Epithelial–mesenchymal transitions in tumour progression. Nat Rev Cancer 2:442–454

Foty RA, Steinberg MS(2004) Cadherin-mediated cell–cell adhesion and tissue segregation in relation to malignancy. Int J Dev Biol 48:397–409

Kashima T, Nakamura K, Kawaguchi J et al (2003) Overexpression of cadherins suppresses pulmonary metastasis of osteosarcoma in vivo. Int J Cancer 104:147–154

Puisieux A, Valsesia-Wittmann S, Ansieau S (2006) A twist for survival and cancer progression. Br J Cancer 94:13–17

Yang J, Mani SA, Weinberg RA (2006) Exploring a new twist on tumor metastasis. Cancer Res 66:4549–4552

Weaver AM (2006) Invadopodia: specialized cell structures for cancer invasion. Clin Exp Metastasis 23:97–105

Christiansen JJ, Rajasekaran AK (2006) Reassessing epithelial to mesenchymal transition as a prerequisite for carcinoma invasion and metastasis. Cancer Res 66:8319–8326

Tarin D (2005) The fallacy of epithelial mesenchymal transition in neoplasia Cancer Res 65: 5996–6000

Tarin D (2005) Carcinoma invasion and metastasis: A role for epithelial–mesenchymal transition? Response. Cancer Res 65:5995–5995

Lin X, Tombler E, Nelson PJ et al (1996) A novel src- and ras-suppressed protein kinase C substrate associated with cytoskeletal architecture. J Biol Chem 271:28430–28438

Gelman IH, Lee K, Tombler E et al (1998) Control of cytoskeletal architecture by the src-suppressed C kinase substrate, SSeCKS. Cell Motil Cytoskelet 41:1–17

Xia W, Unger P, Miller L et al (2001) The Src-suppressed C kinase substrate, SSeCKS, is a potential metastasis inhibitor in prostate cancer. Cancer Res 61:5644–5651

Lin X, Nelson P, Gelman IH (2000) SSeCKS, a major protein kinase C substrate with tumor suppressor activity, regulates G(1)–>S progression by controlling the expression and cellular compartmentalization of cyclin D. Mol Cell Biol 20:7259–7272

Xia W, Gelman IH (2002) Mitogen-induced, FAK-dependent tyrosine phosphorylation of the SSeCKS scaffolding protein. Exp Cell Res 277:139–151

Steeg PS, Bevilacqua G, Kopper L et al (1988) Evidence for a novel gene associated with low tumor metastatic potential. J Natl Cancer Inst 80:200–204

Pozzatti R, Muschel RJ, Williams J et al (1986) Primary rat embryo cells transformed by one or two oncogenes show different metastatic potentials. Science 232:223–227

Hartsough MT, Steeg PS (2000) Nm23/nucleoside diphosphate kinase in human cancers. J Bioenerg Biomembranes 32:301–308

Freije JM, MacDonald NJ, Steeg PS (1998) Nm23 and tumour metastasis: basic and translational advances. Biochem Soc Symp 63:261–271

McDermott WG, Boissan M, Lacombe ML et al (2007) Nm23-H1 homologs suppress tumor cell motility and anchorage independent growth. Clin Exp Metastasis. doi:10.1007/s10585-007-9128-0

Hailat N, Keim DR, Melhem RF et al (1991) 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

Fournier HN, Dupé-Manet S, Bouvard D et al (2002) Integrin cytoplasmic domain-associated protein 1α (ICAP-1α) interacts directly with the metastasis suppressor nm23-H2, and both proteins are targeted to newly formed cell adhesion sites upon integrin engagement. J Biol Chem 277:20895–20902

Tee YT, Chen GD, Lin LY et al (2006) Nm23-H1: a metastasis-associated gene. Taiwan J Obstet Gynecol 45:107–113

Otsuki Y, Tanaka M, Yoshii S et al (2001) Tumor metastasis suppressor nm23H1 regulates Rac1 GTPase by interaction with Tiam1. Proc Natl Acad Sci 98:4385–4390

Kuppers DA, Lan K, Knight JS et al (2005) Regulation of matrix metalloproteinase 9 expression by Epstein-Barr virus nuclear antigen 3C and the suppressor of metastasis Nm23-H1. J Virol 79:9714–9724

Che G, Chen J, Liu L et al (2006) Transfection of nm23-H1 increased expression of beta-Catenin, E-Cadherin and TIMP-1 and decreased the expression of MMP-2, CD44v6 and VEGF and inhibited the metastatic potential of human non-small cell lung cancer cell line L9981. Neoplasma 53:530–537

Horak CE, Lee JH, Elkahloun AG et al (2007) Nm23-H1 suppresses tumor cell motility by down-regulating the lysophosphatidic acid receptor EDG2. Cancer Res 67:7238–7246

Kishi J, Tanaka R, Koiwai O et al (1994) Gelatinases and metalloproteinase inhibitor secreted by murine colonic carcinoma cells with differing metastatic potential. Cell Biol Int 18:165–170

Li H, Fang W, Shi Z (1997) Effects of TIMP-2 gene transfection on biological behaviors of a metastatic human lung carcinoma cell line. Zhonghua Yi Xue Za Zhi 77:652–656

Lopez-Otin C, Matrisian LM (2007) Emerging roles of proteases in tumour suppression. Nat Rev Cancer 7:800–808

Takahashi C, Sheng Z, Horan TP et al (1998) Regulation of matrix metalloproteinase-9 and inhibition of tumor invasion by the membrane-anchored glycoprotein RECK. Proc Natl Acad Sci 95:13221–13226

Noda M, Oh J, Takahashi R et al (2003) RECK: a novel suppressor of malignancy linking oncogenic signaling to extracellular matrix remodeling. Cancer Metastasis Rev 22:167–175

Correa TCS, Brohem CA, Winnischofer SMB et al (2006) Downregulation of the RECK-tumor and metastasis suppressor gene in glioma invasiveness. J Cell Biochem 99:156–167

Span PN, Sweep CGJF, Manders P et al (2003) 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

Oh J, Seo DW, Diaz T et al (2004) Tissue inhibitors of metalloproteinase 2 inhibits endothelial cell migration through increased expression of RECK. Cancer Res 64:9062–9069

Noda M, Takahashi C (2007) Recklessness as a hallmark of aggressive cancer. Cancer Sci 98:1659–1665

Chang HC, Cho CY, Hung WC (2006) Silencing of the metastasis suppressor RECK by RAS oncogene is mediated by DNA methyltransferase 3b-induced promoter methylation. Cancer Res 66:8413–8420

Chang HC, Liu LT, Hung WC (2004) Involvement of histone deacetylation in ras-induced down-regulation of the metastasis suppressor RECK. Cell Signal 16:675–679

Liu LT, Chang HC, Chiang LC et al (2003) Histone deacetylase inhibitor up-regulates RECK to inhibit MMP-2 activation and cancer cell invasion. Cancer Res 63:3069–3072

Oh J, Takahashi R, Kondo S et al (2001) The membrane-anchored MMP inhibitor RECK is a key regulator of extracellular matrix integrity and angiogenesis. Cell 107:789–800

Li SL, Gao DL, Zhao ZH et al (2007) Correlation of matrix metalloproteinase suppressor genes RECK, VEGF, and CD105 with angiogenesis and biological behavior in esophageal squamous cell carcinoma. World J Gastroenterol 13:6076–6081

Dong JT, Lamb PW, Rinker-Schaeffer CW et al (1995) KAI1, a metastasis suppressor gene for prostate cancer on human chromosome 11p11.2. Science 268:884–886

Liu WM, Zhang XA (2006) KAI1/CD82, a tumor metastasis suppressor. Cancer Lett 240:183–194

Kauffman EC, Robinson VL, Stadler WM et al (2003) Metastasis suppression: the evolving role of metastasis suppressor genes for regulating cancer cell growth at the secondary site. J Urol 169:1122–1133

Jee BK, Park KM, Surendran S et al (2006) KAI1/CD82 suppresses tumor invasion by MMP9 inactivation via TIMP1 up-regulation in the H1299 human lung carcinoma cell line. Biochem Biophys Res Commun 342:655–661

Bandyopadhyay S, Zhan R, Chaudhuri A et al (2006) Interaction of KAI1 on tumor cells with DARC on vascular endothelium leads to metastasis suppression. Nat Med 12:933–938

Seraj MJ, Samant RS, Verderame MF et al (2000) Functional evidence for a novel human breast carcinoma metastasis suppressor, BRMS1, encoded at chromosome 11q13. Cancer Res 60:2764–2769

Shevde LA, Samant RS, Goldberg SF et al (2002) Suppression of human melanoma metastasis by the metastasis suppressor gene, BRMS1. Exp Cell Res 273:229–239

Zhang S, Lin QD, DI W (2006) Suppression of human ovarian carcinoma metastasis by the metastasis-suppressor gene, BRMS1. Int J Gynecol Cancer 16:522–531

Lombardi G, Di Cristofano C, Capodanno A et al (2006) High level of messenger RNA for BRMS1 in primary breast carcinomas is associated with poor prognosis. Int J Cancer 120:1169–1178

Zhang Z, Yamashita H, Toyama T et al (2006) Reduced expression of the breast cancer metastasis suppressor 1 mRNA is correlated with poor progress in breast cancer. Clin Cancer Res 12:6410–6414

Ohta S, Lai EW, Pang ALY et al (2005) Downregulation of metastasis suppressor genes in malignant pheochromocytoma. Int J Cancer 114:139–143

Stark AM, Tongers K, Maass N et al (2004) Reduced metastasis-suppressor gene mRNA-expression in breast cancer brain metastases. J Cancer Res Clin Oncol 131:191–198

Kelly LM, Buggy Y, Hill A et al (2005) Expression of the breast cancer metastasis suppressor gene, BRMS1, in human breast carcinoma: lack of correlation with metastasis to axillary lymph nodes. Tumor Biol 26:213–216

Hicks DG, Yoder BJ, Short S et al (2006) Loss of BRMS1 protein expression predicts reduced disease-free survival in hormone receptor negative and HER2 positive subsets of breast cancer. Clin Cancer Res 12:6702–6708

Hurst DR, Mehta A, Moore BP et al (2006) Breast cancer metastasis suppressor 1 (BRMS1) is stabilized by the Hsp90 chaperone. Biochem Biophys Res Commun 348:1429–1435

Meehan WJ, Samant RS, Hopper JE et al (2004) Breast cancer metastasis suppressor 1 (BRMS1) forms complexes with retinoblastoma-binding protein 1 (RBP1) and the mSin3 histone deacetylase complex and represses transcription. J Biol Chem 279:1562–1569

Champine PJ, Michaelson J, Weimer B et al (2007) Microarray analysis reveals potential mechanisms of BRMS1-mediated metastasis suppression. Clin Exp Metastasis 24:551–565

Liu Y, Smith PW, Jones DR (2006) Breast cancer metastasis suppressor 1 functions as a corepressor by enhancing histone deacetylase 1-mediated deacetylation of RelA/p65 and promoting apoptosis. Mol Cell Biol 26:8683–8696

Phadke PA, Vaidya KS, Nash KT et al (2008) BRMS1 suppresses breast cancer experimental metastasis to multiple organs by inhibiting several steps of the metastatic process. Am J Pathol (in press)

Simon AM (1999) Gap junctions: more roles and new structural data. Trends Cell Biol 9:169–170

Samant RS, Seraj MJ, Saunders MM et al (2001) Analysis of mechanisms underlying BRMS1 suppression of metastasis. Clin Exp Metastasis 18:683–693

Saunders MM, Seraj MJ, Li ZY et al (2001) Breast cancer metastatic potential correlates with a breakdown in homospecific and heterospecific gap junctional intercellular communication. Cancer Res 61:1765–1767

Kapoor P, Saunders MM, Li Z et al (2004) Breast cancer metastatic potential: Correlation with increased heterotypic gap junctional intercellular communication between breast cancer cells and osteoblastic cells. Int J Cancer 111:693–697

Rinker-Schaeffer CW, Hawkins AL, Ru N et al (1994) Differential suppression of mammary and prostate cancer metastasis by human chromosomes 17 and 11. Cancer Res 54:6249–6256

Chekmareva MA, Hollowell CP, Smith RC et al (1997) Localization of prostate cancer metastasis-suppressor activity on human chromosome 17. Prostate 33:271–280

Yoshida BA, Dubauskas Z, Chekmareva MA et al (1999) Identification and characterization of candidate prostate cancer metastasis-suppressor genes encoded on human chromosome 17. Cancer Res 59:5483–5487

Yoshida BA, Dubauskas Z, Chekmareva MA et al (1999) Mitogen-activated protein kinase kinase 4/stress-activated protein/Erk kinase 1 (MKK4/SEK1), a prostate cancer metastasis suppressor gene encoded by human chromosome 17. Cancer Res 59:5483–5487

Kim HL, Van der Griend DJ, Yang X et al (2001) 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

Yamada SD, Hickson JA, Hrobowski Y et al (2002) Mitogen-activated protein kinase kinase 4 (MKK4) acts as a metastasis suppressor gene in human ovarian carcinoma. Cancer Res 62:6717–6723

Hickson JA, Huo D, Vander Griend DJ et al (2006) The p38 Kinases MKK4 and MKK6 suppress metastatic colonization in human ovarian carcinoma. Cancer Res 66:2264–2270

Vander Griend DJ, Kocherginsky M, Hickson JA et al (2005) Suppression of metastatic colonization by the context-dependent activation of the c-jun NH2-terminal kinase kinases JNKK1/MKK4 and MKK7. Cancer Res 65:10984–10991

Vander Griend DJ, Rinker-Schaeffer CW (2004) A new look at an old problem: the survival and organ-specific growth of metastases. Sci STKE 2004:216pe3

Aguirre-Ghiso JA (2006) The problem of cancer dormancy – understanding the basic mechanisms and identifying therapeutic opportunities. Cell Cycle 5:1740–1743

Aguirre-Ghiso JA, Estrada Y, Liu D et al (2003) ERK(MAPK) activity as a determinant of tumor growth and dormancy; regulation by p38(SAPK). Cancer Res 63:1684–1695

Lee J-H, Miele ME, Hicks DJ et al (1996) KiSS-1, a novel human malignant melanoma metastasis-suppressor gene. J Natl Cancer Inst 88:1731–1737

Nash KT, Welch DR (2006) The KISS1 metastasis suppressor: mechanistic insights and clinical utility. Front Biosci 11:647–659

Nash KT, Phadke PA, Navenot J-M et al (2007) KISS1 metastasis suppressor secretion, multiple organ metastasis suppression, and maintenance of tumor dormancy. J Natl Cancer Inst 99:309–321

Kotani M, Detheux M, Vandenbogaerde A et al (2001) The metastasis suppressor gene KiSS-1 encodes kisspeptins, the natural ligands of the orphan G protein-coupled receptor GPR54. J Biol Chem 276:34631–34636

Muir AI, Chamberlain L, Elshourbagy NA et al (2001) AXOR12: A novel human G protein-coupled receptor, activated by the peptide KiSS-1. J Biol Chem 276:28969–28975

Ohtaki T, Shintani Y, Honda S et al (2001) Metastasis suppressor gene KiSS1 encodes peptide ligand of a G-protein-coupled receptor. Nature 411:613–617