SSeCKS metastasis-suppressing activity in MatLyLu prostate cancer cells correlates with vascular endothelial growth factor inhibition

Cancer Research

Volumn 66, Issue 11, 2006, Pages 5599-5607

  Su, Bing ^a   Zheng, Qiao ^a   Vaughan, Mary M ^a   Bu, Yahao ^a   Gelman, Irwin H ^a  

^a ROSWELL PARK CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOGENIC FACTOR; ANGIOPOIETIN; COLLAGEN 18A1; ENDOSTATIN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; KERATINOCYTE GROWTH FACTOR; OSTEOPONTIN; PLATELET DERIVED GROWTH FACTOR BETA RECEPTOR; SCAFFOLD PROTEIN; SRC SUPPRESSED PROTEIN KINASE C SUBSTRATE; TENASCIN; TETRACYCLINE; UNCLASSIFIED DRUG; VASCULOTROPIN 121; VASCULOTROPIN 165; VASOSTATIN;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIANGIOGENIC ACTIVITY; ARTICLE; CANCER CELL; CARCINOGENESIS; CONTROLLED STUDY; DOWN REGULATION; DRUG MECHANISM; FEMALE; GENE OVEREXPRESSION; IN VITRO STUDY; IN VIVO STUDY; LUNG METASTASIS; METASTASIS INHIBITION; NEOVASCULARIZATION (PATHOLOGY); NONHUMAN; PRIORITY JOURNAL; PROSTATE CANCER; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION;

ANIMALS; CELL CYCLE PROTEINS; CELL LINE, TUMOR; FEMALE; GENE EXPRESSION PROFILING; HUMANS; MALE; MICE; MICE, NUDE; NEOPLASM METASTASIS; NEOVASCULARIZATION, PATHOLOGIC; NIH 3T3 CELLS; PROSTATIC NEOPLASMS; PROTEINS; RATS; STROMAL CELLS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 33745229237     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-05-4123     Document Type: Article

References (58)

1. Lin X, Nelson PJ, Frankfort B, Tombler E, Johnson R, Gelman IH. Isolation and characterization of a novel mitogenic regulatory gene, 322, which is transcriptionally suppressed in cells transformed by src and ras. Mol Cell Biol 1995;15:2754-62.
2. Gordon T, Grove B, Loftus JC, et al. Molecular cloning and prelimnary characteriztion of a novel cytoplasmic antigen recognized by myasthenia gravis sera. J Clin Invest 1992;90:992-9.
3. Gelman IH. The role of the SSeCKS/Gravin/AKAP12 scaffolding proteins in the spaciotemporal control of signaling pathways in oncogenesis and development. Front Biosci 2002;7:1782-97.
4. Nauert J, Klauck T, Langeberg LK, Scott JD. Gravin, an autoantigen recognized by serum from myasthenia gravis patients, is a kinase scaffolding protein. Curr Biol 1997;7:52-62.
5. Wan M, Sun T, Vyas R, Zheng J, Granada E, Dubeau L. Suppression of tumorigenicity in human ovarian cancer cell lines is controlled by a 2 cM fragment in chromosomal region 6q24-q25. Oncogene 1999;18:1545-51.
6. Xia W, Unger P, Miller L, Nelson J, Gelman IH. The Src-suppressed C kinase substrate, SSeCKS, is a potential metastasis inhibitor in prostate cancer. Cancer Res 2001;15:5644-51.
7. Alcock HE, Stephenson TJ, Royds JA, Hammond DW. Analysis of colorectal tumor progression by microdissection and comparative genomic hybridization. Genes Chromosomes Cancer 2003;37:369-80.
8. Abdollahi A, Pisarcik D, Roberts D, Weinstein J, Cairns P, Hamilton TC. LOT1 (PLAGL1/ZAC1), the candidate tumor suppressor gene at chromosome 6q24-25, is epigenetically regulated in cancer. J Biol Chem 2003;278:6041-9.
9. Mazurenko N, Attaleb M, Gritsko T, et al. High resolution mapping of chromosome 6 deletions in cervical cancer. Oncol Rep 1999;6:859-63.
10. Hyytinen ER, Thalmann GN, Zhau HE, et al. Genetic changes associated with the acquisition of androgen-independent growth, tumorigenicity and metastatic potential in a prostate cancer model. Br J Cancer 1997;75:190-5.
11. Petersen S, Aninat-Meyer M, Schluns K, Gellert K, Dietel M, Petersen I. Chromosomal alterations in the clonal evolution to the metastatic stage of squamous cell carcinomas of the lung. Br J Cancer 2000;82:65-73.
12. Lin X, Gelman IH. Re-expression of the major protein kinase C substrate, SSeCKS, suppresses v-src-induced morphological transformation and tumorigenesis. Cancer Res 1997;57:2304-12.
13. Welsh JB, Zarrinkar PP, Sapinoso LM, et al. Analysis of gene expression profiles in normal and neoplastic ovarian tissue samples identifies candidate molecular markers of epithelial ovarian cancer. Proc Natl Acad Sci U S A 2001;98:1176-81.
14. Perou CM, Sorlie T, Eisen MB, et al. Molecular portraits of human breast tumours. Nature JID-0410462 2000;406:747-52.
15. Shevde LA, Welch DR. Metastasis suppressor pathways-an evolving paradigm. Cancer Lett 2003;198:1-20.
16. Hanahan D, Weinberg RA. The hallmarks of cancer. Cell 2000;100:57-70.
17. Kerbel RS. Inhibition of tumor angiogenesis as a strategy to circumvent acquired resistance to anticancer therapeutic agents. Bioessays 1991;13:31-6.
18. Lee SW, Kim WJ, Choi YK, et al. SSeCKS regulates angiogenesis and tight junction formation in bloodbrain barrier. Nat Med 2003;9:900-6.
19. Isaacs JT, Isaacs WB, Feitz WFJ, Scheres J. Establishment and characterization of seven Dunning rat prostatic cancer cell lines and their use in developing methods for predicting metastatic abilities of prostatic cancer. Prostate 1986;9:261-81.
20. Lin X, Nelson P, German IH. Regulation of G->S Progression by the SSeCKS Tumor Suppressor: Control of Cyclin D Expression and Cellular Compartmentalization. Mol Cell Biol 2000;20:7259-72.
21. Ory DS, Neugeboren BA, Mulligan RC. A stable human-derived packaging cell line for production of high titer retrovirus/vesicular stomatitis virus G pseudotypes. Proc Natl Acad Sci U S A 1996;93:11400-6.
22. Haggstrom S, Bergh A, Damber JE. Vascular endothelial growth factor content in metastasizing and nonmetastasizing Dunning prostatic adenocarcinoma. Prostate 2000;45:42-50.
23. Lin X, Tombler E, Nelson PJ, Ross M, Gelman IH. A novel src- and ras-suppressed protein kinase C substrate associated with cytoskeletal architecture. J Biol Chem 1996;271:28430-8.
24. Holmgren L, O'Reilly MS, Folkman J. Dormancy of micrometastases: balanced proliferation and apoptosis in the presence of angiogenesis suppression. Nat Med 1995;1:149-53.
25. Ferrara N. Molecular and biological properties of vascular endothelial growth factor. J Mol Med 1999;77:527-43.
26. Ferrara N, Carver-Moore K, Chen H, et al. Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature 1996;380:439-42.
27. Ferrara N, LeCouter J, Lin R. Endocrine gland vascular endothelial growth factor (EG-VEGF) and the hypothesis of tissue-specific regulation of angiogenesis. Endocr Res 2002;28:763-4.
28. Schlessinger J. New roles for Src kinases in control of cell survival and angiogenesis. Cell 2000;100:293-6.
29. Rofstad EK, Halsor EF. Vascular endothelial growth factor, interleukin 8, platelet-derived endothelial cell growth factor, and basic fibroblast growth factor promote angiogenesis and metastasis in human melanoma xenografts. Cancer Res 2000;60:4932-8.
30. Kano MR, Morishita Y, Iwata C, et al. VEGF-A and FGF-2 synergistically promote neoangiogenesis through enhancement of endogenous PDGF-B-PDGFRβ signaling. J Cell Sci 2005;118:3759-68.
31. Dong J, Grunstein J, Tejada M, et al. VEGF-null cells require PDGFRα signaling-mediated stromal fibroblast recruitment for tumorigenesis. EMBO J 2004;23:2800-10.
32. Gerber HP, Kowalski J, Sherman D, Eberhard DA, Ferrara N. Complete inhibition of rhabdomyosarcoma xenograft growth and neovascularization requires blockade of both tumor and host vascular endothelial growth factor. Cancer Res 2000;60:6253-8.
33. Viloria-Petit A, Miquerol L, Yu JL, et al. Contrasting effects of VEGF gene disruption in embryonic stem cell-derived versus oncogene-induced tumors. EMBO J 2003;22:4091-102.
34. Claffey KP, Brown LF, del Aguila LF, et al. Expression of vascular permeability factor/vascular endothelial growth factor by melanoma cells increases tumor growth, angiogenesis, and experimental metastasis. Cancer Res 1996;56:172-81.
35. Mori A, Arii S, Furutani M, et al. Vascular endothelial growth factor-induced tumor angiogenesis and tumorigenicity in relation to metastasis in a HT1080 human fibrosarcoma cell model. Int J Cancer 1999;80:738-43.
36. Zhang HT, Scott PA, Morbidelli L, et al. The 121 amino acid isoform of vascular endothelial growth factor is more strongly tumorigenic than other splice variants in vivo. Br J Cancer 2000;83:63-8.
37. Guo P, Xu L, Pan S, et al. Vascular endothelial growth factor isoforms display distinct activities in promoting tumor angiogenesis at different anatomic sites. Cancer Res 2001;61:8569-77.
38. Yu JL, Rak JW, Klement G, Kerbel RS. Vascular endothelial growth factor isoform expression as a determinant of blood vessel patterning in human melanoma xenografts. Cancer Res 2002;62:1838-46.
39. Hanahan D, Christofori G, Naik P, Arbeit J. Transgenic mouse models of tumour angiogenesis: the angiogenic switch, its molecular controls, and prospects for preclinical therapeutic models. Eur J Cancer 1996;32A:2386-93.
40. Doll JA, Reiher FK, Crawford SE, Pins MR, Campbell SC, Bouck NP. Thrombospondin-1, vascular endothelial growth factor and fibroblast growth factor-2 are key functional regulators of angiogenesis in the prostate. Prostate 2001;49:293-305.
41. Dallol A, Agathanggelou A, Tommasi S, Pfeifer GP, Maher ER, Lauf F. Involvement of the RASSF1A tumor suppressor gene in controlling cell migration. Cancer Res 2005;65:7653-9.
42. Kunapuli P, Kasyapa CS, Hawthorn L, Cowell JK. LGI1, a putative tumor metastasis suppressor gene, controls in vitro invasiveness and expression of matrix metalloproteinases in glioma cells through the ERK1/2 pathway. J Biol Chem 2004;279:23151-7.
43. Amsellem V, Kryszke MH, Hervy M, et al. The actin cytoskeleton-associated protein zyxin acts as a tumor suppressor in Ewing tumor cells. Exp Cell Res 2005;304:443-56.
44. Zetter BR. Angiogenesis and tumor metastasis. Annu Rev Med 1998;49:407-24.
45. McMahon G. VEGF receptor signaling in tumor angiogenesis. Oncologist 2000;5 Suppl 1:3-10.
46. Veikkola T, Alitalo K. VEGFs, receptors and angiogenesis. Semin Cancer Biol 1999;9:211-20.
47. Gerber HP, Ferrara N. The role of VEGF in normal and neoplastic hematopoiesis. J Mol Med 2003;81:20-31.
48. Kaplan RN, Riba RD, Zacharoulis S, et al. VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche. Nature 2005;438:820-7.
49. Weis S, Cui J, Barnes L, Cheresh D. Endothelial barrier disruption by VEGF-mediated Src activity potentiates tumor cell extravasation and metastasis. J Cell Biol 2004;167:223-9.
50. Graells J, Vinyals A, Figueras A, et al. Overproduction of VEGF concomitantly expressed with its receptors promotes growth and survival of melanoma cells through MAPK and PI3K signaling. J Invest Dermatol 2004;123:1151-61.
51. Zhang L, Yang N, Garcia JR, et al. Generation of a syngeneic mouse model to study the effects of vascular endothelial growth factor in ovarian carcinoma. Am J Pathol 2002;161:2295-309.
52. Yu XM, Lo CY, Chan WF, Lam KY, Leung P, Luk JM. Increased expression of vascular endothelial growth factor C in papillary thyroid carcinoma correlates with cervical lymph node metastases. Clin Cancer Res 2005;11:8063-9.
53. Bjorndahl MA, Cao R, Burton JB, et al. Vascular endothelial growth factor-a promotes peritumoral lymphangiogenesis and lymphatic metastasis. Cancer Res 2005;65:9261-8.
54. Von Marschall Z, Scholz A, Stacker SA, et al. Vascular endothelial growth factor-D induces lymphangiogenesis and lymphatic metastasis in models of ductal pancreatic cancer. Int J Oncol 2005;27:669-79.
55. Jain RK. Normalization of tumor vasculature: an emerging concept in antiangiogenic therapy. Science 2005;307:58-62.
56. Eliceiri BP, Paul R, Schwartzberg PL, Hood JD, Leng J, Cheresh DA. Selective requirement for Src kinases during VEGF-induced angiogenesis and vascular permeability. Mol Cell 1999;4:915-24.
57. Maxwell PH, Wiesener MS, Chang GW, et al. The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature 1999;399:271-5.
58. Zundel W, Schindler C, Haas-Kogan D, et al. Loss of PTEN facilitates HIF-1-mediated gene expression. Genes Dev 2000;14:391-6.