Kisspeptin-10, a KISS1-derived decapeptide, inhibits tumor angiogenesis by suppressing Sp1-mediated VEGF expression and FAK/Rho GTPase activation

Cancer Research

Volumn 69, Issue 17, 2009, Pages 7062-7070

  Cho, Sung Gook ^a,c   Yi, Zhengfang ^a,b   Pang, Xiufeng ^a,b   Yi, Tingfang ^a   Wang, Ying ^a   Luo, Jian ^b   Wu, Zirong ^b   Li, Dali ^b   Liu, Mingyao ^a,b,c  

^a TEXAS A AND M HEALTH SCIENCE CENTER   (United States)

^b EAST CHINA NORMAL UNIVERSITY   (China)

^c TEXAS A AND M UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

KISSPEPTIN 10; METASTIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; TRANSCRIPTION FACTOR SP1; VASCULOTROPIN;

ANIMAL CELL; ARTICLE; CARCINOGENESIS; CELL INVASION; CELL LEVEL; CELL MIGRATION; CHORIOALLANTOIS; CONTROLLED STUDY; CORNEA CELL; DRUG INHIBITION; ENDOTHELIUM CELL; ENZYME ACTIVATION; GENE EXPRESSION; HUMAN; HUMAN CELL; MOLECULAR MECHANICS; NONHUMAN; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN BINDING; UMBILICAL VEIN;

ANGIOGENESIS INHIBITORS; ANIMALS; CELL ADHESION; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; CHICK EMBRYO; CHORIOALLANTOIC MEMBRANE; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOTHELIAL CELLS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FOCAL ADHESION KINASE 1; HUMANS; MICE; NEOPLASMS, EXPERIMENTAL; NEOVASCULARIZATION, PATHOLOGIC; NEOVASCULARIZATION, PHYSIOLOGIC; OLIGOPEPTIDES; TUMOR SUPPRESSOR PROTEINS; VASCULAR ENDOTHELIAL GROWTH FACTOR A; WOUND HEALING; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 70149121279     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-09-0476     Document Type: Article

References (50)

1. Yi T, Yi Z, Cho SG, et al. Gambogic acid inhibits angiogenesis and prostate tumor growth by suppressing vascular endothelial growth factor receptor 2 signaling. Cancer Res 2008;68:1843-1850
2. Bhat TA, Singh RP. Tumor angiogenesis - a potential target in cancer chemoprevention. Food Chem Toxicol 2008;46:1334-1345 (Pubitemid 351258200)
3. Breen EC. VEGF in biological control. J Cell Biochem 2007;102:1358-1367
4. Nagy JA, Dvorak AM, Dvorak HF. VEGF-A and the induction of pathological angiogenesis. Annu Rev Pathol 2007;2:251-275
5. Barr MP, Bouchier-Hayes DJ, Harmey JJ. Vascular endothelial growth factor is an autocrine survival factor for breast tumour cells under hypoxia. Int J Oncol 2008;32:41-48
6. Schafer G, Cramer T, Suske G, Kemmner W, Wiedenmann B, Hocker M. Oxidative stress regulates vascular endothelial growth factor-A gene transcription through Sp1- and Sp3-dependent activation of two proximal GC-rich promoter elements. J Biol Chem 2003;278:8190-8198 (Pubitemid 36800562)
7. Abdelrahim M, Smith R, III, Burghardt R, Safe S. Role of Sp proteins in regulation of vascular endothelial growth factor expression and proliferation of pancreatic cancer cells. Cancer Res 2004;64:6740-6749 (Pubitemid 39297937)
8. Finkenzeller G, Sparacio A, Technau A, Marme D, Siemeister G. Sp1 recognition sites in the proximal promoter of the human vascular endothelial growth factor gene are essential for platelet-derived growth factor-induced gene expression. Oncogene 1997;15:669-676 (Pubitemid 27389929)
9. Pore N, Liu S, Shu HK, et al. Sp1 is involved in Akt-mediated induction of VEGF expression through an HIF-1-independent mechanism. Mol Biol Cell 2004;15:4841-4853 (Pubitemid 39392201)
10. Shi Q, Le X, Abbruzzese JL, et al. Constitutive Sp1 activity is essential for differential constitutive expression of vascular endothelial growth factor in human pancreatic adenocarcinoma. Cancer Res 2001;61:4143-4154 (Pubitemid 32720983)
11. Zhang J, Jia Z, Li Q, et al. Elevated expression of vascular endothelial growth factor correlates with increased angiogenesis and decreased progression-free survival among patients with low-grade neuroendocrine tumors. Cancer 2007;109:1478-1486 (Pubitemid 46595681)
12. Rudge JS, Holash J, Hylton D, et al. Inaugural article: VEGF Trap complex formation measures production rates of VEGF, providing a biomarker for predicting efficacious angiogenic blockade. Proc Natl Acad Sci U S A 2007;104:18363-18370 (Pubitemid 350210713)
13. Li D, Yu W, Liu M. Regulation of KiSS1 gene expression. Peptides 2009;30:130-138
14. Kotani M, Detheux M, Vandenbogaerde A, et al. The metastasis suppressor gene KiSS-1 encodes kisspeptins, the natural ligands of the orphan G protein-coupled receptor GPR54. J Biol Chem 2001;276:34631-34636 (Pubitemid 37384458)
15. Ohtaki T, Shintani Y, Honda S, et al. Metastasis suppressor gene KiSS-1 encodes peptide ligand of a G-protein- coupled receptor. Nature 2001;411:613-617 (Pubitemid 32531412)
16. Lee JH, Miele ME, Hicks DJ, et al. KiSS-1, a novel human malignant melanoma metastasis-suppressor gene. J Natl Cancer Inst 1996;88:1731-1737
17. Lee JH, Welch DR. Suppression of metastasis in human breast carcinoma MDA-MB-435 cells after transfection with the metastasis suppressor gene, KiSS-1. Cancer Res 1997;57:2384-2387
18. Stafford LJ, Xia C, Ma W, Cai Y, Liu M. Identification and characterization of mouse metastasis-suppressor KiSS1 and its G-protein-coupled receptor. Cancer Res 2002;62:5399-5404
19. Sanchez-Carbayo M, Capodieci P, Cordon-Cardo C. Tumor suppressor role of KiSS-1 in bladder cancer: loss of KiSS-1 expression is associated with bladder cancer progression and clinical outcome. Am J Pathol 2003;162:609-617 (Pubitemid 36267867)
20. Dittmer A, Vetter M, Schunke D, et al. Parathyroid hormone-related protein regulates tumor-relevant genes in breast cancer cells. J Biol Chem 2006;281:14563-14572 (Pubitemid 43855159)
21. Jiang T, Zhang SL, Lin B, Meng LR, Gao H. Expression and clinical significance of KISS-1 and GPR54 mRNA in endometrial carcinoma. Zhonghua Zhong Liu Za Zhi 2005;27:229-231
22. Nicolle G, Comperat E, Nicolaiew N, Cancel-Tassin G, Cussenot O. Metastin (KISS-1) and metastin-coupled receptor (GPR54) expression in transitional cell carcinoma of the bladder. Ann Oncol 2007;18:605-607 (Pubitemid 46359649)
23. Sanchez-Carbayo M, Belbin TJ, Scotlandi K, et al. Expression profiling of osteosarcoma cells transfected with MDR1 and NEO genes: regulation of cell adhesion, apoptosis, and tumor suppression-related genes. Lab Invest 2003;83:507-517 (Pubitemid 36457705)
24. Nash KT, Phadke PA, Navenot JM, et al. Requirement of KISS1 secretion for multiple organ metastasis suppression and maintenance of tumor dormancy. J Natl Cancer Inst 2007;99:309-321
25. Ohta S, Lai EW, Pang AL, et al. Downregulation of metastasis suppressor genes in malignant pheochromocytoma. Int J Cancer 2005;114:139-143 (Pubitemid 40194319)
26. 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 2004;10:1379-1383 (Pubitemid 38365232)
27. Jiang Y, Berk M, Singh LS, et al. KiSS1 suppresses metastasis in human ovarian cancer via inhibition of protein kinase Ca. Clin Exp Metastasis 2005;22:369-376 (Pubitemid 41609296)
28. Dhar DK, Naora H, Kubota H, et al. Downregulation of KiSS-1 expression is responsible for tumor invasion and worse prognosis in gastric carcinoma. Int J Cancer 2004;111:868-872 (Pubitemid 39096235)
29. Masui T, Doi R, Mori T, et al. Metastin and its variant forms suppress migration of pancreatic cancer cells. Biochem Biophys Res Commun 2004;315:85-92. (Pubitemid 38175189)
30. Marot D, Bieche I, Aumas C, 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 2007;14:691-702. (Pubitemid 350074058)
31. Martin TA, Watkins G, Jiang WG. KiSS-1 expression in human breast cancer. Clin Exp Metastasis 2005;22:503-511 (Pubitemid 41750702)
32. 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 2003;129:531-535 (Pubitemid 37211194)
33. Seminara SB, Messager S, Chatzidaki EE, et al. The GPR54 gene as a regulator of puberty. N Engl J Med 2003;349:1614-1627
34. Zhang C, Roepke TA, Kelly MJ, Ronnekleiv OK. Kisspeptin depolarizes gonadotropin-releasing hormone neurons through activation of TRPC-like cationic channels. J Neurosci 2008;28:4423-4434
35. Colledge WH. GPR54 and puberty. Trends Endocrinol Metab 2004;15:448-453
36. Seminara SB, Kaiser UB. New gatekeepers of reproduction: GPR54 and its cognate ligand, KiSS-1. Endocrinology 2005;146:1686-1688
37. d'Anglemont de Tassigny X, Fagg LA, Dixon JP, et al. Hypogonadotropic hypogonadism in mice lacking a functional Kiss1 gene. Proc Natl Acad Sci U S A 2007;104:10714-10719
38. d'Anglemont de Tassigny X, Fagg LA, Carlton MB, Colledge WH. Kisspeptin can stimulate gonadotropin-releasing hormone (GnRH) release by a direct action at GnRH nerve terminals. Endocrinology 2008;149:3926-3932
39. Thompson EL, Patterson M, Murphy KG, et al. Central and peripheral administration of kisspeptin-10 stimulates the hypothalamic-pituitary-gonadal axis. J Neuroendocrinol 2004;16:850-858 (Pubitemid 39489998)
40. Bilban M, Ghaffari-Tabrizi N, Hintermann E, et al. Kisspeptin-10, a KiSS-1/metastin-derived decapeptide, is a physiological invasion inhibitor of primary human trophoblasts. J Cell Sci 2004;117:1319-1328 (Pubitemid 38559810)
41. Mead EJ, Maguire JJ, Kuc RE, Davenport AP. Kisspeptins are novel potent vasoconstrictors in humans, with a discrete localization of their receptor, G protein-coupled receptor 54, to atherosclerosis-prone vessels. Endocrinology 2007;148:140-147
42. Yi T, Cho SG, Yi Z, et al. Thymoquinone inhibits tumor angiogenesis and tumor growth through suppressing AKT and extracellular signal-regulated kinase signaling pathways. Mol Cancer Ther 2008;7:1789-1796
43. Yi ZF, Cho SG, Zhao H, et al. A novel peptide from human apolipoprotein(a) inhibits angiogenesis and tumor growth by targeting c-Src phosphorylation in VEGF-induced human umbilical endothelial cells. Int J Cancer 2009;124:843-852
44. Kenyon BM, Voest EE, Chen CC, Flynn E, Folkman J, D'Amato RJ. A model of angiogenesis in the mouse cornea. Invest Ophthalmol Vis Sci 1996;37:1625-1632
45. Mie Lee Y, Kim SH, Kim HS, et al. Inhibition of hypoxia-induced angiogenesis by FK228, a specific histone deacetylase inhibitor, via suppression of HIF- 1a activity. Biochem Biophys Res Commun 2003;300:241-246
46. Tournaire R, Simon MP, le Noble F, Eichmann A, England P, Pouyssegur J. A short synthetic peptide inhibits signal transduction, migration and angiogenesis mediated by Tie2 receptor. EMBO Rep 2004;5:262-267 (Pubitemid 38500105)
47. Kruger EA, Duray PH, Price DK, Pluda JM, Figg WD. Approaches to preclinical screening of antiangiogenic agents. Semin Oncol 2001;28:570-576
48. Takino T, Nakada M, Miyamori H, et al. JSAP1/JIP3 cooperates with focal adhesion kinase to regulate c-Jun N-terminal kinase and cell migration. J Biol Chem 2005;280:37772-37781 (Pubitemid 41642387)
49. Hauck CR, Hsia DA, Puente XS, Cheresh DA, Schlaepfer DD. FRNK blocks v-Src-stimulated invasion and experimental metastases without effects on cell motility or growth. EMBO J 2002;21:6289-6302
50. Avraham HK, Lee TH, Koh Y, et al. Vascular endothelial growth factor regulates focal adhesion assembly in human brain microvascular endothelial cells through activation of the focal adhesion kinase and related adhesion focal tyrosine kinase. J Biol Chem 2003;278:36661 8. (Pubitemid 37139998)