The signaling network of tumor invasion

Histology and Histopathology

Volumn 20, Issue 2, 2005, Pages 593-602

  Wang, G K ^a   Zhang, Wei ^a  

^a UNIVERSITY OF TEXAS   (United States)

Author keywords

Crosstalk; IGFPB; Integrin; Rho; Tumor invasion

Indexed keywords

ALPHA1 INTEGRIN; ALPHA2 INTEGRIN; ANTINEOPLASTIC AGENT; BETA1 INTEGRIN; CONTORTROSTATIN; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR ANTIBODY; EPIDERMAL GROWTH FACTOR RECEPTOR KINASE INHIBITOR; GELATINASE A; GELATINASE B; INTEGRIN; INTEGRIN RECEPTOR; MATRILYSIN; PROTEIN CDC42; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; S 247; SMALL INTERFERING RNA; SNAKE VENOM; SOMATOMEDIN; SOMATOMEDIN B; SOMATOMEDIN B RECEPTOR; SOMATOMEDIN BINDING PROTEIN 1; SOMATOMEDIN BINDING PROTEIN 2; SOMATOMEDIN BINDING PROTEIN 3; SOMATOMEDIN BINDING PROTEIN 4; SOMATOMEDIN BINDING PROTEIN 5; SOMATOMEDIN BINDING PROTEIN 6; SOMATOMEDIN C; SOMATOMEDIN C RECEPTOR; UNCLASSIFIED DRUG; UNINDEXED DRUG;

BREAST CARCINOMA; CANCER INHIBITION; CANCER INVASION; CANCER RISK; CARCINOGENESIS; CELL INVASION; CLINICAL TRIAL; DRUG EFFICACY; DRUG TARGETING; GENE SILENCING; HUMAN; LIVER CELL CARCINOMA; MALIGNANT NEOPLASTIC DISEASE; NONHUMAN; PHENOTYPE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; REVIEW; RNA INTERFERENCE; SIGNAL TRANSDUCTION; STRUCTURAL HOMOLOGY; TUMOR GROWTH; TUMOR PROMOTION;

ANIMALS; FEEDBACK; HUMANS; INTEGRINS; MODELS, BIOLOGICAL; NEOPLASM INVASIVENESS; RECEPTOR CROSS-TALK; RHO GTP-BINDING PROTEINS; SIGNAL TRANSDUCTION; SOMATOMEDINS;

SERPENTES;

EID: 16344393955     PISSN: 02133911     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (90)

1. Boulle N., Logie A., Gicquel C., Perin L. and Le Bouc Y. (1998). Increased levels of insulin-like growth factor II (IGF-II) and IGF-binding protein-2 are associated with malignancy in sporadic adrenocortical tumors. J Clin. Endocrinol. Metab. 83, 1713-1720.
2. Bredin C.G., Liu Z. and Klominek J. (2003). Growth factor-enhanced expression and activity of matrix metalloproteases in human non-small cell lung cancer cell lines. Anticancer Res. 23, 4877-4884.
3. Brodt P., Fallavollita L., Khatib A.M., Samani A.A. and Zhang D. (2001). Cooperative regulation of the invasive and metastatic phenotypes by different domains of the type I insulin-like growth factor receptor beta subunit. J. Biol. Chem. 276, 33608-33615.
4. Brunet A., Bonni A., Zigmond M.J., Lin M.Z., Juo P., Hu L.S., Anderson M.J., Arden K.C., Blenis J. and Greenberg M.E. (1999). Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96, 857-868.
5. Butler A.A., Yakar S., Gewolb I.H., Karas M., Okubo Y. and LeRoith D. (1998). Insulin-like growth factor-I receptor signal transduction: at the interface between physiology and cell biology. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 121, 19-26.
6. Butt A.J., Martin J.L., Dickson K.A., McDougall F., Firth S.M. and Baxter R.C. (2004). Insulin-like growth factor binding protein-3 expression is associated with growth stimulation of T47D human breast cancer cells: the role of altered epidermal growth factor signaling. J. Clin. Endocrinol. Metab. 89, 1950-1956.
7. Carpenter C.L., Auger K.R., Chanudhuri M., Yoakim M., Schaffhausen B., Shoelson S. and Cantley L.C. (1993). Phosphoinositide 3-kinase is activated by phosphopeptides that bind to the SH2 domains of the 85-kDa subunit. J. Biol. Chem. 268, 9478-9483.
8. Catz S.D. and Johnson J.L. (2001). Transcriptional regulation of bcl-2 by nuclear factor kappaB and its significance in prostate cancer. Oncogene 20, 7342-7351.
9. Chan J.M., Stampfer M.J., Giovannucci E., Gann P.H., Ma J., Wilkinson P., Hennekens C.H. and Pollak M. (1998). Plasma insulin-like growth factor-I and prostate cancer risk: a prospective study. Science 279, 563-566.
10. Chen X.M., Wang J.Z., Fu B. and Yu L.F. (1997). RGD-containing peptides trigger apoptosis in glomerular mesangial cells of adult cells of adult human kidneys. Biochem. Biophys. Res. Commun. 234, 594-599.
11. Chung J., Bachelder R.E., Lipscomb E.A., Shaw L.M. and Mercurio A.M. (2002). Integrin (alpha6beta4) regulation of eIF-4E activity and VEGF translation: a survival mechanism for carcinoma cells. J. Cell Biol. 158, 165-174.
12. Collisson E.A., Kleer C., Wu M., De A., Gambhir S.S., Merajver S.D. and Kolodney M.S. (2003). Atorvastatin prevents RhoC isoprenylation, invasion, and metastasis in human melanoma cells. Mol. Cancer Ther. 2, 941-948.
13. Clark E.A., Golub T.R., Lander E.S. and Hynes R.O. (2000). Genomic analysis of metastasis reveals an essential role for RhoC. Nature 406, 532-535.
14. Crombet T., Osorio M., Cruz T., Roca C., del Castillo R., Mon R., Iznaga-Escobar N., Figueredo R., Koropatnick J., Renginfo E., Fernandez E., Alvarez D., Torres O., Ramos M., Leonard I., Perez R. and Lage A. (2004). Use of the humanized anti-epidermal growth factor receptor monoclonal antibody h-R3 in combination with radiotherapy in the treatment of locally advanced head and neck cancer patients. J. Clin. Oncol. 22, 1646-1654.
15. Davidson B., Goldberg I., Reich R., Tell L., Dong H.P., Trope' C.G., Risberg B. and Kopolovic J. (2003). AlphaV- and beta1-integrin subunits are commonly expressed in malignant effusions from ovarian carcinoma patients. Gynecol. Oncol. 90, 248-257.
16. Deryugina E.I., Ratnikov B.I., Postnova T.I., Rozanov D.V. and Strongin A.Y. (2002). Processing of integrin alpha(v) subunit by membrane type 1 matrix metalloproteinase stimulates migration of breast carcinoma cells on vitronectin and enhances tyrosine phosphorylation of focal adhesion kinase. J. Biol. Chem. 277, 9749-9756.
17. Diehl D., Hoeflich A., Wolf E. and Lahm H. (2004). Insulin-like growth factor (IGF)-binding protein-4 inhibits colony formation of colorectal cancer cells by IGF-independent mechanisms. Cancer Res. 64, 1600-1603.
18. Engers R., Springer E., Michiels F., Collard J.G. and Gabbert H.E. (2001). Rac affects invasion of human renal cell carcinomas by up-regulating tissue inhibitor of metalloproteinases (TIMP)-1 and TIMP-2 expression. J. Biol. Chem. 276, 41889-41897.
19. Fornaro M., Manzotti M., Tallini G., Slear A.E., Bosari S., Ruoslahti E. and Languino L.R. (1998). Beta1C integrin in epithelial cells correlates with a nonproliferative phenotype: forced expression of beta1C inhibits prostate epithelial cell proliferation. Am. J. Pathol. 153, 1079-1087.
20. Fottner Ch., Hoeflich A., Wolf E. and Weber M.M. (2004). Role of the insulin-like growth factor system in adrenocortical growth control and carcinogenesis. Horm. Metab. Res 36, 397-405.
21. Fuller G.N., Rhee C.H., Hess K.R., Caskey L.S., Wang R., Bruner J.M., Yung W.K. and Zhang W. (1999). Reactivation of insulin-like growth factor binding protein 2 expression in glioblastoma multiforme: a revelation by parallel gene expression profiling. Cancer Res. 69, 4228-4232.
22. Giese A., Loo M.A., Tran N., Haskett D., Coons S.W. and Berens M.E. (1996). Dichotomy of astrocytoma migration and proliferation. Int. J. Cancer 67, 275-282.
23. Gimond C., Baudoin C. and Sonnenberg A. (2000). Defects in adhesion and migration, but not in proliferation and differentiation, of embryonic stem cells upon replacement of integrin subunit beta1A by beta1D. Differentiation 66, 93-105.
24. Grzmil M., Hemmerlein B., Thelen P., Schweyer S. and Burfeind P. (2004). Blockade of the type I IGF receptor expression in human prostate cancer cells inhibits proliferation and invasion, up-regulates IGF binding protein-3, and suppresses MMP-2 expression. J. Pathol. 202, 50-59.
25. Hankinson S.E., Willett W.C., Colditz G.A., Hunter D.J., Michaud D.S., Deroo B., Rosner B., Speizer F.E. and Pollak M. (1998). Circulating concentrations of insulin-like growth factor-I and risk of breast cancer. Lancet 351, 1393-1396.
26. Hauck C.R., Sieg D.J., Hsia D.A., Loftus J.C., Gaarde W.A., Monia B.P. and Schlaepfer D.D. (2001). Inhibition of focal adhesion kinase expression or activity disrupts epidermal growth factor-stimulated signaling promoting the migration of invasive human carcinoma cells. Cancer Res. 61, 7079-7090.
27. Haugland H.K., Tysnes B.B. and Tysnes O.B. (1997). Adhesion and migration of human glioma cells are differently dependent on extracellular matrix molecules. Anticancer Res. 17, 1035-1042.
28. Hemler M. (1999). Extracellular matrix, anchor, and adhesion proteins. Oxford, UK: Oxford University Press. 196-212.
29. James W.G., Bullard D.C. and Hickey M.J. (2003). Critical role of the alpha 4 integrin/VCAM-1 pathway in cerebral leukocyte trafficking in lupus-prone MRL/fas(lpr) mice. J. Immunol. 170, 520-527.
30. Jones J.I., Gockerman A., Busby W.H. Jr, Wright G. and Clemmons D.R. (1993). Insulin-like growth factor binding protein 1 stimulates cell migration and binds to the alpha 5 beta 1 integrin by means of its Arg-Gly-Asp sequence. Proc. Natl. Acad. Sci. USA 90, 10553-10557.
31. Kabir-Salmani M., Shiokawa S., Akimoto Y., Sakai K. and Iwashita M. (2004). The role of alpha(5)beta(1)-integrin in the IGF-l-induced migration of extravillous trophoblast cells during the process of implantation. Mol. Hum. Reprod. 10, 91-97.
32. Khwaja A. (1999). Akt is more than just a Bad kinase. Nature 401, 33-34.
33. Kim D.W. and Choy H. (2004). Potential role for epidermal growth factor receptor inhibitors in combined-modality therapy for non-small-cell lung cancer. Int. J. Radiat. Oncol. Biol. Phys. 59(2 Suppl), 11-20.
34. Kim H.S., Ingermann A.R., Tsubaki J., Twigg S.M., Walker G.E. and Oh Y. (2004). Insulin-like growth factor-binding protein 3 induces caspase-dependent apoptosis through a death receptor-mediated pathway in MCF-7 human breast cancer cells. Cancer Res. 64, 2229-2237.
35. Kiosses W.B., Shattil S.J., Pampori N. and Schwartz M.A. (2001). Rac recruits high-affinity integrin alphavbeta3 to lamellipodia in endothelial cell migration. Nat. Cell Biol. 3, 316-320.
36. Kudlacz E., Whitney C., Andresen C., Duplantier A., Beckius G., Chupak L., Klein A., Kraus K. and Milici A. (2002). Pulmonary eosinophilia in a murine model of allergic inflammation is attenuated by small molecule alpha4betal antagonists. J. Pharmacol. Exp. Ther. 301, 747-752.
37. Levitt R.J., Buckley J., Blouin M.J., Schaub B., Triche T.J. and Pollak M. (2004). Growth inhibition of breast epithelial cells by celecoxib is associated with upregulation of insulin-like growth factor binding protein-3 expression. Biochem. Biophys. Res. Commun. 316, 421-428.
38. Lipscomb E.A., Dugan A.S., Rabinovitz I. and Mercurio A.M. (2003). Use of RNA interference to inhibit integrin (alpha6beta4)-mediated invasion and migration of breast carcinoma cells. Clin. Exp. Metastasis 20, 569-576.
39. Long L. Navab R. and Brodt P. (1998). Regulation of the Mr 72,000 type IV collagenase by the type I insulin-like growth factor receptor. Cancer Res 58, 3243-3247.
40. Ma J., Pollak M.N., Giovannucci E., Chan J.M., Tao Y., Hennekens C.H. and Stampfer M.J. (1999). Prospective study of colorectal cancer risk in men and plasma levels of insulin-like growth factor (IGF)-I and IGF-binding protein-3. J. Natl. Cancer Inst. 91, 620-625.
41. Malliri A., van der Kammen P.A., Clark K., van der Valk M., Michiels F. and Collard J.G. (2002). Mice deficient in the Rac activator Tiam1 are resistant to Ras-induced skin tumours. Nature 417, 867-871.
42. Manes T., Zheng D.Q., Tognin S., Woodard A.S., Marchisio P.C. and Languino L.R. (2003). Alpha(v)beta3 integrin expression up-regulates cdc2, which modulates cell migration. J. Cell Biol. 161, 817-826.
43. Mariotti A., Kedeshian P.A., Dans M., Curatola A.M., Gagnoux-Palacios L. and Giancotti F.G. (2001). EGF-R signaling through Fyn kinase disrupts the function of integrin alpha6beta4 at hemidesmosomes: role in epithelial cell migration and carcinoma invasion. J. Cell Biol. 155, 447-458.
44. Min Y., Adachi Y., Yamamoto H., Ito H., Itoh F., Lee C.T., Nadaf S., Carbone D.P. and Imai K. (2003). Genetic blockade of the insulin-like growth factor-I receptor: a promising strategy for human pancreatic cancer. Cancer Res. 63, 6432-6441.
45. Mira E., Manes S., Lacalle R.A., Marquez G. and Martinez-A C. (1999). Insulin-like growth factor I-triggered cell migration and invasion are mediated by matrix metalloproteinase-9. Endocrinology 140, 1657-64.
46. Miyamoto S., Yano K., Sugimoto S., Ishii G., Hasebe T., Endoh Y., Kodama K., Goya M., Chiba T. and Ochiai A. (2004). Matrix metalloproteinase-7 facilitates insulin-like growth factor bioavailability through its proteinase activity on insulin-like growth factor binding protein 3. Cancer Res. 64, 665-671.
47. Miyazaki K., Hattori Y., Umenishi F., Yasumitsu H. and Umeda M. (1990). Purification and characterization of extracellular matrix-degrading metalloproteinase, matrin (pump-1), secreted from human rectal carcinoma cell line. Cancer Res. 50, 7758-7764.
48. Moore M.G., Wetterau L.A., Francis M.J., Peehl D.M. and Cohen P. (2003). Novel stimulatory role for insulin-like growth factor binding protein-2 in prostate cancer cells. Int. J. Cancer 105, 14-19.
49. Nagashima Y., Hasegawa S., Koshikawa N., Taki A., Ichikawa Y., Kitamura H., Misugi K., Kihira Y., Matuo Y., Yasumitsu H. and Miyazaki K. (1997). Expression of matrilysin in vascular endothelial cells adjacent to matrilysin-producing tumors. Int. J. Cancer 72, 441-445.
50. Nemeth J.A., Cher M.L., Zhou Z., Mullins C., Bhagat S. and Trikha M. (2003). Inhibition of alphaVbeta3 integrin reduces angiogenesis, bone turnover, and tumor cell proliferation in experimental prostate cancer bone metastases. Clin. Exp. Metastasis 20, 413-420.
51. Nordqvist A.C. and Mathiesen T. (2002). Expression of IGF-II, IGFBP-2, -5, and -6 in meningiomas with different brain invasiveness. J. Neurooncol. 57, 19-26.
52. Novosyadlyy R., Tron K., Duclas J., Ramadori G. and Scharf J.G. (2004). Expression and regulation of the insulin-like growth factor axis components in rat liver myofibroblasts. J. Cell. Physiol. 199, 388-398.
53. Parker A., Cheville J.C., Lohse C., Cerhan J.R. and Blute M.L. (2003). Expression of insulin-like growth factor I receptor and survival in patients with clear cell renal cell carcinoma. J. Urol. 170(2 Pt 1), 420-424.
54. Pennisi P.A., Barr V., Nunez N.P., Stannard B. and Le Roith D. (2002). Reduced expression of insulin-like growth factor I receptors in MCF-7 breast cancer cells leads to a more metastatic phenotype. Cancer Res. 62, 6529-6537.
55. Pereira J.J., Meyer T., Docherty S.E., Reid H.H., Marshall J., Thompson E.W., Rossjohn J. and Price J.T. (2004). Biomolecular interaction of insulin-like growth factor (IGF) binding protein-2 with alphaVbeta3 negatively modulates IGF-1-mediated migration and tumor growth. Cancer Res. 64, 977-984.
56. Pierschbacher M.D. and Ruoslahti E. (1987). Influence of stereochemistry of the sequence Arg-Gly-Asp-Xaa on binding specificity in cell adhesion. J. Biol. Chem 262, 17294-17298.
57. Price D.J., Avraham S., Feuerstein J., Fu Y. and Avraham H.K. (2002). The invasive phenotype in HMT-3522 cells requires increased EGF receptor signaling through both PI 3-kinase and ERK 1,2 pathways. Cell Commun. Adhes. 9, 87-102.
58. Ratnikov B.I., Rozanov D.V., Postnova T.I., Baciu P.G., Zhang H., DiScipio R.G., Chestukhina G.G., Smith J.W., Deryugina E.I. and Strongin A.Y. (2002). An alternative processing of integrin alpha(v) subunit in tumor cells by membrane type-1 matrix metalloproteinase. J. Biol. Chem. 277, 7377-7385.
59. Reinmuth N., Liu W., Ahmad S.A., Fan F., Stoeltzing O., Parikh A.A., Bucana C.D., Gallick G.E., Nickols M.A., Westlin W.F. and Ellis L.M. (2003). Alphavbeta3 integrin antagonist S247 decreases colon cancer metastasis and angiogenesis and improves survival in mice. Cancer Res. 63, 2079-2087.
60. Richardsen E., Ukkonen T., Bjornsen T., Mortensen E., Egevad L. and Busch C. (2003). Overexpression of IGFBP2 is a marker for malignant transformation in prostate epithelium. Virchows Arch. 442, 329-335.
61. Ridley A.J., Paterson H.F., Johnston C.L., Diekmann D. and Hall A. (1992). The small GTP-binding protein rac regulates growth factor-induced membrane ruffling. Cell 70, 401-410.
62. Rose D.M., Grabovsky V., Alon R. and Ginsberg M.H. (2001). The affinity of integrin alpha4beta1 governs lymphocyte migration. J. Immunol. 167, 2824-2830.
63. Sahai E. and Marshall C.J. (2003). Differing modes of tumour cell invasion have distinct requirements for Rho/ROCK signalling and extracellular proteolysis. Nat. Cell Biol. 5, 711-719.
64. Saltz L.B., Meropol N.J., Loehrer P.J. Sr, Needle M.N., Kopit J., Mayer R.J. (2004). Phase II trial of cetuximab in patients with refractory colorectal cancer that expresses the epidermal growth factor receptor. J. Clin. Oncol. 22, 1201-1208.
65. Sarray S., Berthet V., Calvete J.J., Secchi J., Marvaldi J., El-Ayeb M., Marrakchi N. and Luis J. (2004). Lebectin, a novel C-type lectin from Macrovipera lebetina venom, inhibits integrin-mediated adhesion, migration and invasion of human tumour cells. Lab. Invest. 84, 573-581.
66. Schafer B., Gschwind A. and Ullrich A. (2004). Multiple G-protein-coupled receptor signals converge on the epidermal growth factor receptor to promote migration and invasion. Oncogene 23, 991-999.
67. Schmitmeier S., Markland F.S., Ritter M.R., Sawcer D.E. and Chen T.C. (2003). Functional effect of contortrostatin, a snake venom disintegrin, on human glioma cell invasion in vitro. Cell Commun. Adhes. 10, 1-16.
68. Schutt B.S., Langkamp M., Rauschnabel U., Ranke M.B. and Elmlinger M.W. (2004). Integrin-mediated action of insulin-like growth factor binding protein-2 in tumor cells. J. Mol. Endocrinol. 32, 859-868.
69. Shah N.T. and Miller V.A. (2003). Antitumor activity and tolerability of gefitinib in patients with non-small-cell lung cancer treated in an expanded access program. Clin. Lung Cancer 5, 182-186.
70. Song S.W., Fuller G.N., Khan A., Kong S., Shen W., Taylor E., Ramdas L., Lang F.F. and Zhang W. (2003). IIp45, an insulin-like growth factor binding protein 2 (IGFBP-2) binding protein, antagonizes IGFBP-2 stimulation of glioma cell invasion. Proc. Natl. Acad. Sci. USA 100, 13970-13975.
71. Soulieres D., Senzer N.N., Vokes E.E., Hidalgo M., Agarwala S.S. and Siu L.L. (2004). Multicenter phase II study of erlotinib, an oral epidermal growth factor receptor tyrosine kinase inhibitor, in patients with recurrent or metastatic squamous cell cancer of the head and neck. J. Clin. Oncol. 22, 77-85.
72. Tai Y.T., Podar K., Catley L., Tseng Y.H., Akiyama M., Shringarpure R., Burger R., Hideshima T., Chauhan D., Mitsiades N., Richardson P., Munshi N.C., Kahn C.R., Mitsiades C. and Anderson K.C. (2003). Insulin-like growth factor-1 induces adhesion and migration in human multiple myeloma cells via activation of beta1-integrin and phosphatidylinositol 3′-kinase/AKT signaling. Cancer Res. 63, 5850-5858.
73. Tang Y., Zhang D., Fallavollita L. and Brodt P. (2003). Vascular endothelial growth factor C expression and lymph node metastasis are regulated by the type I insulin-like growth factor receptor. Cancer Res. 63, 1166-1171.
74. Tennenbaum T., Belanger A.J., Glick A.B., Tamura R., Quaranta V. and Yuspa S.H. (1995). A splice variant of alpha 6 integrin is associated with malignant conversion in mouse skin tumorigenesis. Proc. Natl. Acad. Sci. USA 92, 7041-7045.
75. Tysnes B.B., Larsen L.F., Ness G.O., Mahesparan R., Edvardsen K., Garcia-Cabrera I. and Bjerkvig R. (1996). Stimulation of glioma-cell migration by laminin and inhibition by anti-alpha3 and anti-beta1 integrin antibodies. Int. J. Cancer 67, 777-784.
76. Vanhoefer U., Tewes M., Rojo F., Dirsch O., Schleucher N., Rosen O., Tillner J., Kovar A., Braun A.H., Trarbach T., Seeber S., Harstrick A. and Baselga J. (2004). Phase I study of the humanized antiepidermal growth factor receptor monoclonal antibody EMD72000 in patients with advanced solid tumors that express the epidermal growth factor receptor. J. Clin. Oncol 22, 175-184.
77. Varner J.A. and Cheresh D.A. (1996). Integrins and cancer. Curr. Opin. Cell Biol. 8, 724-730.
78. Varner J.A., Emerson D.A. and Juliano R.L. (1995). Integrin alpha5beta1 expression negatively regulates cell growth: reversal by attachment to fibronectin. Mol. Biol. Cell 6, 725-740.
79. Viatour P., Bentires-Alj M., Chariot A., Deregowski V., de Leval L., Merville M.P. and Bours V. (2003). NF- kappa B2/p100 induces Bcl-2 expression. Leukemia 17, 1349-1356.
80. Wang H., Shen S.S., Wang H., Diwan A.H., Zhang W., Fuller G.N. and Prieto V.G. (2003). Expression of insulin-like growth factor-binding protein 2 in melanocytic lesions. J. Cutan. Pathol. 30, 599-605.
81. Wang H., Wang H., Shen W., Huang H., Hu L., Ramdas L., Zhou Y.H., Liao W.S., Fuller G.N. and Zhang W. (2003). Insulin-like growth factor binding protein 2 enhances glioblastoma invasion by activating invasion-enhancing genes. Cancer Res. 63, 4315-4321.
82. Wu M., Wu Z.F., Kumar-Sinha C., Chinnaiyan A. and Merajver S.D. (2004). RhoC induces differential expression of genes involved in invasion and metastasis in MCF10A breast cells. Breast Cancer Res. Treat. 84, 3-12.
83. Yang C., Zeisberg M., Lively J.C., Nyberg P., Afdhal N. and Kalluri R. (2003). Integrin alpha1beta1 and alpha2beta1 are the key regulators of hepatocarcinoma cell invasion across the fibrotic matrix microenvironment. Cancer Res. 63, 8312-8317.
84. Yu H., Spitz M.R., Mistry J., Gu J., Hong W.K. and Wu X. (1999). Plasma levels of insulin-like growth factor-I and lung cancer risk: a case-control analysis. J. Natl. Cancer Inst. 91, 151-156.
85. Zhang D. and Brodt P. (2003). Type 1 insulin-like growth factor regulates MT1-MMP synthesis and tumor invasion via PI 3-kinase/Akt signaling. Oncogene 22, 974-982.
86. Zhao H., Dupont J., Yakar S., Karas M. and LeRoith D. (2004). PTEN inhibits cell proliferation and induces apoptosis by downregulating cell surface IGF-IR expression in prostate cancer cells. Oncogene 22, 786-794.
87. Zheng D.Q., Woodard A.S., Fornaro M., Tallini G. and Languino L.R. (1999). Prostatic carcinoma cell migration via alpha(v)beta3 integrin is modulated by a focal adhesion kinase pathway. Cancer Res. 59, 1655-1664.
88. Zheng W.H., Kar S., Dore S. and Quirion R. (2000). Insulin-like growth factor-1 (IGF-1): a neuroprotective trophic factor acting via the Akt kinase pathway. J. Neural Transm. Suppl. 60, 261-272.
89. Zhou R., Flaswinkel H., Schneider M.R., Lahm H., Hoeflich A., Wanke R. and Wolf E. (2004). Insulin-like growth factor-binding protein-4 inhibits growth of the thymus in transgenic mice. J. Mol. Endocrinol. 32, 349-364.
90. Zhuge Y. and Xu J. (2001). Rac1 mediates type I collagen-dependent MMP-2 activation. Role in cell invasion across collagen barrier. J. Biol. Chem. 276, 16248-16256.