Growth hormone-releasing hormone (GHRH) promotes metastatic phenotypes through EGFR/HER2 transactivation in prostate cancer cells

Molecular and Cellular Endocrinology

Volumn 446, Issue , 2017, Pages 59-69

  Muñoz Moreno, Laura ^a   Bajo, Ana M ^a   Prieto, Juan C ^a   Carmena, María J ^a  

^a UNIVERSITY OF ALCALÁ   (Spain)

Author keywords

Cell adhesion; Cell migration; GHRH; Prostate cancer; VEGF secretion

Indexed keywords

BETA CATENIN; CYCLIN D1; CYCLINE; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 2; GELATINASE A; GELATINASE B; GROWTH HORMONE RELEASING FACTOR; HERMES ANTIGEN; MYC PROTEIN; PROTEIN BAX; PROTEIN BCL 2; PROTEIN P21; PROTEIN P53; UVOMORULIN; VASCULOTROPIN; ERBB2 PROTEIN, HUMAN; MESSENGER RNA; TUMOR PROTEIN; VASCULOTROPIN A;

ARTICLE; CANCER STAGING; CELL ADHESION; CELL FUNCTION; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; G1 PHASE CELL CYCLE CHECKPOINT; G2 PHASE CELL CYCLE CHECKPOINT; HUMAN; HUMAN CELL; LNCAP CELL LINE; MALE; PC3 CELL LINE; PROSTATE CANCER CELL LINE; PROTEIN EXPRESSION; PROTEIN SECRETION; TRANSACTIVATION; UPREGULATION; CELL CYCLE; CELL MOTION; DRUG EFFECT; GENETICS; METABOLISM; METASTASIS; PATHOLOGY; PHENOTYPE; PROSTATE TUMOR; SECRETION (PROCESS); TRANSCRIPTION INITIATION; TUMOR CELL LINE;

BETA CATENIN; CELL ADHESION; CELL CYCLE; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; GROWTH HORMONE-RELEASING HORMONE; HUMANS; MALE; NEOPLASM METASTASIS; NEOPLASM PROTEINS; PHENOTYPE; PROLIFERATING CELL NUCLEAR ANTIGEN; PROSTATIC NEOPLASMS; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTOR, ERBB-2; RNA, MESSENGER; TRANSCRIPTIONAL ACTIVATION; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 85013093330     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2017.02.011     Document Type: Article

References (51)

1. Abbas, T., Dutta, A., p21 in cancer: intricate networks and multiple activities. Nat. Rev. Cancer. 9 (2009), 400–414.
2. Arya, M., Bott, S.R., Shergill, I.S., Ahmed, H.U., Williamson, M., Patel, H.R., The metastatic cascade in prostate cancer. Surg. Oncol. 15 (2006), 117–128.
3. Barabutis, N., Schally, A.V., Knocking down gene expression for growth hormone-releasing hormone inhibits proliferation of human cancer cell lines. Br. J. Cancer. 98 (2008), 1790–1796.
4. Barabutis, N., Schally, A.V., Antioxidant activity of growth hormone-releasing hormone antagonists in LNCaP human prostate cancer line. Proc. Natl. Acad. Sci. U S A. 105 (2008), 20470–20475.
5. Barabutis, N., Schally, A.V., Growth hormone-releasing hormone: extrapituitary effects in physiology and pathology. Cell. Cycle. 9 (2010), 4110–4116.
6. Berger, R., Lin, D.I., Nieto, M., Sicinska, E., Garraway, L.A., Adams, H., Signoretti, S., Hahn, W.C., Loda, M., Androgen-dependent regulation of Her-2/neu in prostate cancer cells. Cancer Res. 66 (2006), 5723–5728.
7. Barabutis, N., Siejka, A., Schally, A.V., Effects of growth hormone-releasing hormone and its agonistic and antagonistic analogs in cancer and non-cancerous cell lines. Int. J. Oncol. 36 (2010), 1285–1289.
8. Beuran, M., Negoi, I., Paun, S., Ion, A.D., Bleotu, C., Negoi, R.I., Hostiuc, S., The epithelial to mesenchymal transition in pancreatic cancer: a systematic review. Pancreatology 15 (2015), 217–225.
9. Busto, R., Schally, A.V., Varga, J.L., Garcia-Fernandez, M.O., Groot, K., Armatis, P., Szepeshazi, K., The expression of growth hormone-releasing hormone (GHRH) and splice variants of its receptor in human gastroenteropancreatic carcinomas. Proc. Natl. Acad. Sci. U S A. 99 (2002), 11866–11871.
10. Cheng, J.-C., Qiu, X., Chang, H.-M., Leung, P.C.K., HER2 mediates epidermal growth factor-induced down-regulation of E-cadherin in human ovarian cancer cells. Biochem. Biophysical Res. Commun. 434 (2013), 81–86.
11. Chiurillo, M.A., Role of the Wnt/beta-catenin pathway in gastric cancer: an in-depth literature review. World J. Exp. Med. 5 (2015), 84–102.
12. Chopin, L.K., Herington, A.C., A potential autocrine pathway for growth hormone releasing hormone (GHRH) and its receptor in human prostate cancer cell lines. Prostate 49 (2001), 116–121.
13. Ciardiello, F., Troiani, T., Bianco, R., Orditura, M., Morgillo, F., Martinelli, E., Morelli, M.P., Cascone, T., Tortora, G., Interaction between the epidermal growth factor receptor (EGFR) and the vascular endothelial growth factor (VEGF) pathways: a rational approach for multi-target anticancer therapy. Ann. Oncol., 17(Suppl. 7), 2006 vii109–14.
14. Delcourt, N., Bockaert, J., Marin, P., GPCR-jacking: from a new route in RTK signalling to a new concept in GPCR activation. Trends Pharmacol. Sci. 28 (2007), 602–607.
15. Di Lorenzo, G., Tortora, G., D'Armiento, F.P., De Rosa, G., Staibano, S., Autorino, R., D'Armiento, M., De Laurentiis, M., De Placido, S., Catalano, G., Bianco, A.R., Ciardiello, F., Expression of epidermal growth factor receptor correlates with disease relapse and progression to androgen-independence in human prostate cancer. Clin. Cancer Res. 8 (2002), 3438–3444.
16. Fahrenholtz, C.D., Rick, F.G., Garcia, M.I., Zarandi, M., Cai, R.Z., Block, N.L., Schally, A.V., Burnstein, K.L., Preclinical efficacy of growth hormone-releasing hormone antagonists for androgen-dependent and castration-resistant human prostate cancer. Proc. Natl. Acad. Sci. U S A. 111 (2014), 1084–1089.
17. Farahani, E., Patra, H.K., Jangamreddy, J.R., Rashedi, I., Kawalec, M., Rao Pariti, R.K., Batakis, P., Wiechec, E., Cell adhesion molecules and their relation to (cancer) cell stemness. Carcinogenesis 35 (2014), 747–759.
18. Garcia-Fernandez, M.O., Schally, A.V., Varga, J.L., Groot, K., Busto, R., The expression of growth hormone-releasing hormone (GHRH) and its receptor splice variants in human breast cancer lines; the evaluation of signaling mechanisms in the stimulation of cell proliferation. Breast Cancer Res. Treat. 77 (2003), 15–26.
19. Gross, J.C., Schreiner, A., Engels, K., Starzinski-Powitz, A., E-cadherin surface levels in epithelial growth factor-stimulated cells depend on adherens junction protein shrew-1. Mol. Biol. Cell. 20 (2009), 3598–3607.
20. Halmos, G., Schally, A.V., Czompoly, T., Krupa, M., Varga, J.L., Rekasi, Z., Expression of growth hormone-releasing hormone and its receptor splice variants in human prostate cancer. J. Clin. Endocrinol. Metab. 87 (2002), 4707–4714.
21. Hanahan, D., Weinberg, Robert A., Hallmarks of cancer: the next generation. Cell 144 (2011), 646–674.
22. Havt, A., Schally, A.V., Halmos, G., Varga, J.L., Toller, G.L., Horvath, J.E., Szepeshazi, K., Köster, F., Kovitz, K., Groot, K., Zarandi, M., Kanashiro, C.A., The expression of the pituitary growth hormone-releasing hormone receptor and its splice variants in normal and neoplastic human tissues. Proc. Natl. Acad. Sci. U S A. 102 (2005), 17424–17429.
23. Heerboth, S., Housman, G., Leary, M., Longacre, M., Byler, S., Lapinska, K., Willbanks, A., Sarkar, S., EMT and tumor metastasis. Clin. Transl. Med., 4, 2015, 6.
24. Howard, S., Deroo, T., Fujita, Y., Itasaki, N., A positive role of cadherin in Wnt/β-catenin signalling during epithelial-mesenchymal transition. PLoS One, 6, 2011, e23899.
25. Huber, A.H., Weis, W.I., The structure of the beta-catenin/E-cadherin complex and the molecular basis of diverse ligand recognition by beta-catenin. Cell 105 (2001), 391–402.
26. Kahán, Z., Arencibia, J.M., Csernus, V.J., Groot, K., Kineman, R.D., Robinson, W.R., Schally, A.V., Expression of growth hormone-releasing hormone (GHRH) messenger ribonucleic acid and the presence of biologically active GHRH in human breast, endometrial, and ovarian cancers. J. Clin. Endocrinol. Metab. 84 (1999), 582–589.
27. Kiaris, H., Chatzistamou, I., Papavassiliou, A.G., Schally, A.V., Growth hormone-releasing hormone: not only a neurohormone. Trends Endocrinol. Metab. 22 (2011), 311–317.
28. Le Bras, G.F., Taubenslag, K.J., Andl, C.D., The regulation of cell-cell adhesion during epithelial-mesenchymal transition, motility and tumor progression. Cell. Adh Migr. 6 (2012), 365–373.
29. Luu, H.H., Zhang, R., Haydon, R.C., Rayburn, E., Kang, Q., Si, W., Park, J.K., Wang, H., Peng, Y., Jiang, W., He, T.C., Wnt/beta-catenin signaling pathway as a novel cancer drug target. Curr. Cancer Drug Targets. 4 (2004), 653–671.
30. Maga, G., Hubscher, U., Proliferating cell nuclear antigen (PCNA): a dancer with many partners. J. Cell. Sci. 116 (2003), 3051–3060.
31. Mărgineanu, E., Cotrutz, C.E., Cotrutz, C., Correlation between E-cadherin abnormal expressions in different types of cancer and the process of metastasis. Rev. Med. Chir. Soc. Med. Nat. Iasi. 112 (2008), 432–436.
32. Mirzayans, R., Andrais, B., Scott, A., Murray, D., New insights into p53 signaling and cancer cell response to DNA damage: implications for cancer therapy. J. Biomed. Biotechnol., 2012, 2012, 170325.
33. Moldovan, G.L., Pfander, B., Jentsch, S., PCNA, the maestro of the replication fork. Cell 129 (2007), 665–679.
34. Munoz-Moreno, L., Arenas, M.I., Carmena, M.J., Schally, A.V., Prieto, J.C., Bajo, A.M., Growth hormone-releasing hormone antagonists abolish the transactivation of human epidermal growth factor receptors in advanced prostate cancer models. Invest. New Drugs. 32 (2014), 871–882.
35. Muñoz-Moreno, L., Arenas, M.I., Schally, A.V., Fernández-Martínez, A.B., Zarka, E., González-Santander, M., Carmena, M.J., Vacas, E., Prieto, J.C., Bajo, A.M., Inhibitory effects of antagonists of growth hormone-releasing hormone on growth and invasiveness of PC3 human prostate cancer. Int. J. Cancer. 132 (2013), 755–765.
36. Onder, T.T., Gupta, P.B., Mani, S.A., Yang, J., Lander, E.S., Weinberg, R.A., Loss of E-cadherin promotes metastasis via multiple downstream transcriptional pathways. Cancer Res., 68, 2008 3645–3454.
37. Orsulic, S., Huber, O., Aberle, H., Arnold, S., Kemler, R., E-cadherin binding prevents beta-catenin nuclear localization and beta-catenin/LEF-1-mediated transactivation. J. Cell. Sci. 112:Pt 8 (1999), 1237–1245.
38. Pérez-Sayáns, M., Suárez-Peñaranda, J.M., Gayoso-Diz, P., Barros-Angueira, F., Gándara-Rey, J.M., García-García, A., The role of p21Waf1/CIP1 as a Cip/Kip type cell-cycle regulator in oral squamous cell carcinoma (Review). Med. Oral Patol. Oral Cir. Bucal. 18 (2013), e219–e225.
39. Plonowski, A., Schally, A.V., Busto, R., Krupa, M., Varga, J.L., Halmos, G., Expression of growth hormone-releasing hormone (GHRH) and splice variants of GHRH receptors in human experimental prostate cancers. Pept. U. S., 2002, 1127–1133.
40. Pyne, N.J., Pyne, S., Receptor tyrosine kinase-G-protein-coupled receptor signalling platforms: out of the shadow?. Trends Pharmacol. Sci. 32 (2011), 443–450.
41. Schmalhofer, O., Brabletz, S., Brabletz, T., E-cadherin, beta-catenin, and ZEB1 in malignant progression of cancer. Cancer Metastasis Rev. 28 (2009), 151–166.
42. Siegel, R.L., Miller, K.D., Jemal, A., Cancer statistics, 2016. CA A Cancer J. Clin. 66 (2016), 7–30.
43. Siejka, A., Barabutis, N., Schally, A.V., GHRH antagonist inhibits focal adhesion kinase (FAK) and decreases expression of vascular endothelial growth factor (VEGF) in human lung cancer cells in vitro. Peptides 37 (2012), 63–68.
44. Sotomayor, S., Carmena, M.J., Schally, A.V., Varga, J.L., Sánchez-Chapado, M., Prieto, J.C., Bajo, A.M., Transactivation of HER2 by vasoactive intestinal peptide in experimental prostate cancer: antagonistic action of an analog of growth-hormone-releasing hormone. Int. J. Oncol. 31 (2007), 1223–1230.
45. Stangelberger, A., Schally, A.V., Rick, F.G., Varga, J.L., Baker, B., Zarandi, M., Halmos, G., Inhibitory effects of antagonists of growth hormone releasing hormone on experimental prostate cancers are associated with upregulation of wild-type p53 and decrease in p21 and mutant p53 proteins. Prostate 72 (2012), 555–565.
46. Stoimenov, I., Helleday, T., PCNA on the crossroad of cancer. Biochem. Soc. Trans. 37 (2009), 605–613.
47. Su, Y.J., Chang, Y.W., Lin, W.H., Liang, C.L., Lee, J.L., An aberrant nuclear localization of E-cadherin is a potent inhibitor of Wnt/[beta]-catenin-elicited promotion of the cancer stem cell phenotype. Oncogenesis, 4, 2015, e157.
48. Thakur, R., Mishra, D.P., Pharmacological modulation of beta-catenin and its applications in cancer therapy. J. Cell. Mol. Med. 17 (2013), 449–456.
49. Waga, S., Stillman, B., Cyclin-dependent kinase inhibitor p21 modulates the DNA primer-template recognition complex. Mol. Cell. Biol. 18 (1998), 4177–4187.
50. Wang, S.C., PCNA: a silent housekeeper or a potential therapeutic target?. Trends Pharmacol. Sci. 35 (2014), 178–186.
51. Zhang, Z., Liu, Z.B., Ren, W.M., Ye, X.G., Zhang, Y.Y., The miR-200 family regulates the epithelial-mesenchymal transition induced by EGF/EGFR in anaplastic thyroid cancer cells. Int. J. Mol. Med. 30 (2012), 856–862.