Evidence for the possible biological significance of the igf-1 gene alternative splicing in prostate cancer

Frontiers in Endocrinology

Volumn 4, Issue MAR, 2013, Pages

  Philippou, Anastassios ^a   Armakolas, Athanasios ^a   Koutsilieris, Michael ^a  

^a UNIVERSITY OF ATHENS MEDICAL SCHOOL   (Greece)

Author keywords

Apoptosis; Cancer progression; Cell survival; Human IGF I isoforms; IGF I bioactivity; IGF I peptides; IGF I receptors; IGF I signaling

Indexed keywords

DEXAMETHASONE; FIBROBLAST GROWTH FACTOR; METALLOPROTEINASE; MITOGEN ACTIVATED PROTEIN KINASE; PROSTATE SPECIFIC ANTIGEN; SOMATOMEDIN A; SOMATOMEDIN B; SOMATOMEDIN BINDING PROTEIN; SOMATOMEDIN C; SOMATOSTATIN DERIVATIVE; TRANSCRIPTION FACTOR; TRANSFORMING GROWTH FACTOR BETA; UROKINASE;

APOPTOSIS; CANCER GROWTH; CARCINOGENESIS; CELL DIFFERENTIATION; CELL GROWTH; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; GENE EXPRESSION; GENETIC TRANSCRIPTION; HUMAN; NONHUMAN; PATHOPHYSIOLOGY; PROSTATE CANCER; PROSTATIC INTRAEPITHELIAL NEOPLASIA; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REVIEW; RNA SPLICING;

EID: 84884192210     PISSN: None     EISSN: 16642392     Source Type: Journal    
DOI: 10.3389/fendo.2013.00031     Document Type: Review

References (150)

1. Armakolas, A., Philippou, A., Panteleakou, Z., Nezos, A., Sourla, A., Petraki, C., et al. (2010). Preferential expression of IGF-1Ec (MGF) transcript in cancerous tissues of human prostate: evidence for a novel and autonomous growth factor activity of MGF E peptide in human prostate cancer cells. Prostate 70, 1233-1242.
2. Balmanno, K., and Cook, S. J. (2009). Tumour cell survival signalling by the ERK1/2 pathway. Cell Death Differ. 16, 368-377.
3. Barton, E. R. (2006). The ABCs of IGF-I isoforms, impact on muscle hypertrophy and implications for repair. Appl. Physiol. Nutr. Metab. 31, 791-797.
4. Barton, E. R., DeMeo, J., and Lei, H. (2010). The insulin-like growth factor (IGF)-I E-peptides are required for isoform-specific gene expression and muscle hypertrophy after local IGF-I production. J. Appl. Physiol. 108, 1069-1076.
5. Baserga, R. (1999). The IGF-I receptor in cancer research. Exp. Cell Res. 253, 1-6.
6. Baserga, R. (2000). The contradictions of the insulin-like growth factor 1 receptor. Oncogene 19, 5574-5581.
7. Baserga, R., Peruzzi, F., and Reiss, K. (2003). The IGF-1 receptor in cancer biology. Int. J. Cancer 107, 873-877.
8. Baserga, R., Resnicoff, M., and Dews, M. (1997). The IGF-I receptor and cancer. Endocrine 7, 99-102.
9. Baxter, R. C. (2000). Insulin-like growth factor (IGF)-binding proteins, interactions with IGFs and intrinsic bioactivities. Am. J. Physiol. Endocrinol. Metab. 278, E967-E976.
10. Baxter, R. C., Martin, J. L., and Beniac, V. A. (1989). High molecular weight insulin-like growth factor binding protein complex. Purification and properties of the acid-labile subunit from human serum. J. Biol. Chem. 264, 11843-11848.
11. Bloor, C. A., Knight, R. A., Kedia, R. K., Spiteri, M. A., and Allen, J. T. (2001). Differential mRNA expression of insulin-like growth factor-1 splice variants in patients with idiopathic pulmonary fibrosis and pulmonary sarcoidosis. Am. J. Respir. Crit. Care Med. 164, 265-272.
12. Blume-Jensen, P., and Hunter, T. (2001). Oncogenic kinase signalling. Nature 411, 355-365.
13. Bodart, J. F. (2010). Extracellular-regulated kinase-mitogen-activated protein kinase cascade: unsolved issues. J. Cell. Biochem. 109, 850-857.
14. Bogdanos, J., Karamanolakis, D., Tenta, R., Tsintavis, A., Milathianakis, C., Mitsiades, C., et al. (2003). Endocrine/paracrine/autocrine survival factor activity of bone microenvironment participates in the development of androgen ablation and chemotherapy refractoriness of prostate cancer metastasis in skeleton. Endocr. Relat. Cancer 10, 279-289.
15. Brisson, B. K., and Barton, E. R. (2012). Insulin-like growth factor-I E-peptide activity is dependent on the IGF-I receptor. PLoS ONE 7, e45588. doi:10.1371/journal.pone.0045588
16. Burfeind, P., Chernicky, C. L., Rininsland, F., and Ilan, J. (1996). Antisense RNA to the type I insulin-like growth factor receptor suppresses tumor growth and prevents invasion by rat prostate cancer cells in vivo. Proc. Natl. Acad. Sci. U.S.A. 93, 7263-7268.
17. Byron, S. A., Horwitz, K. B., Richer, J. K., Lange, C. A., Zhang, X., and Yee, D. (2006). Insulin receptor substrates mediate distinct biological responses to insulin-like growth factor receptor activation in breast cancer cells. Br. J. Cancer 95, 1220-1228.
18. Cardillo, M. R., Monti, S., Di Silverio, F., Gentile, V., Sciarra, F., and Toscano, V. (2003). Insulin-like growth factor (IGF)-I, IGF-II and IGF type I receptor (IGFR-I) expression in prostatic cancer. Anticancer Res. 23, 3825-3835.
19. Carson, J. P., Kulik, G., and Weber, M. J. (1999). Antiapoptotic signaling in LNCaP prostate cancer cells, a survival signaling pathway independent of phosphatidylinositol 3'-kinase and Akt/protein kinase B. Cancer Res. 59, 1449-1453.
20. Chan, J. M., Stampfer, M. J., Giovannucci, E., Gann, P. H., Ma, J., Wilkinson, P., et al. (1998). Plasma insulin-like growth factor-I and prostate cancer risk, a prospective study. Science 279, 563-566.
21. Chen, M. J., Chiou, P. P., Lin, P., Lin, C. M., Siri, S., Peck, K., et al. (2007). Suppression of growth and cancer-induced angiogenesis of aggressive human breast cancer cells (MDA-MB-231) on the chorioallantoic membrane of developing chicken embryos by E-peptide of pro-IGF-I. J. Cell. Biochem. 101, 1316-1327.
22. Chew, S. L., Lavender, P., Clark, A. J., and Ross, R. J. (1995). An alternatively spliced human insulin-like growth factor-I transcript with hepatic tissue expression that diverts away from the mitogenic IBE1 peptide. Endocrinology 136, 1939-1944.
23. Chott, A., Sun, Z., Morganstern, D., Pan, J., Li, T., Susani, M., et al. (1999). Tyrosine kinases expressed in vivo by human prostate cancer bone marrow metastases and loss of the type 1 insulin-like growth factor receptor. Am. J. Pathol. 155, 1271-1279.
24. Cohen, P. (2006). Overview of the IGF-I system. Horm. Res. 65(Suppl. 1), 3-8.
25. Cohen, P., Peehl, D. M., Graves, H. C., and Rosenfeld, R. G. (1994). Biological effects of prostate specific antigen as an insulin-like growth factor binding protein-3 protease. J. Endocrinol. 142, 407-415.
26. Cohen, P., Peehl, D. M., Lamson, G., and Rosenfeld, R. G. (1991). Insulin-like growth factors (IGFs), IGF receptors, and IGF-binding proteins in primary cultures of prostate epithelial cells. J. Clin. Endocrinol. Metab. 73, 401-407.
27. Crews, C. M., and Erikson, R. L. (1993). Extracellular signals and reversible protein phosphorylation, what to Mek of it all. Cell 74, 215-217.
28. Davis, R. J. (1995). Transcriptional regulation by MAP kinases. Mol. Reprod. Dev. 42, 459-467.
29. De Meyts, P., and Whittaker, J. (2002). Structural biology of insulin and IGF1 receptors, implications for drug design. Nat. Rev. Drug Discov. 1, 769-783.
30. Deng, M., Zhang, B., Wang, K., Liu, F., Xiao, H., Zhao, J., et al. (2011). Mechano growth factor E peptide promotes osteoblasts proliferation and bone-defect healing in rabbits. Int. Orthop. 35, 1099-1106.
31. Denley, A., Cosgrove, L. J., Booker, G. W., Wallace, J. C., and Forbes, B. E. (2005). Molecular interactions of the IGF system. Cytokine Growth Factor Rev. 16, 421- 439.
32. Dhanasekaran, S. M., Barrette, T. R., Ghosh, D., Shah, R., Varambally, S., Kurachi, K., et al. (2001). Delineation of prognostic biomarkers in prostate cancer. Nature 412, 822-826.
33. DiGiovanni, J., Kiguchi, K., Frijhoff, A., Wilker, E., Bol, D. K., Beltran, L., et al. (2000). Deregulated expression of insulin-like growth factor 1 in prostate epithelium leads to neoplasia in transgenic mice. Proc. Natl. Acad. Sci. U.S.A. 97, 3455-3460.
34. Dimopoulos, M. A., Kiamouris, C., Gika, D., Deliveliotis, C., Giannopoulos, A., Zervas, A., et al. (2004). Combination of LHRH analog with somatostatin analog and dexamethasone versus chemotherapy in hormone-refractory prostate cancer, a randomized phase II study. Urology 63, 120-125.
35. Djakiew, D. (2000). Dysregulated expression of growth factors and their receptors in the development of prostate cancer. Prostate 42, 150-160.
36. Djavan, B., Waldert, M., Seitz, C., and Marberger, M. (2001). Insulin-like growth factors and prostate cancer. World J. Urol. 19, 225-233.
37. Dluzniewska, J., Sarnowska, A., Beresewicz, M., Johnson, I., Srai, S. K., Ramesh, B., et al. (2005). A strong neuroprotective effect of the autonomous C-terminal peptide of IGF-1 Ec (MGF) in brain ischemia. FASEB J. 19, 1896-1898.
38. Duan, C., Ren, H., and Gao, S. (2010). Insulin-like growth factors (IGFs), IGF receptors, and IGF-binding proteins, roles in skeletal muscle growth and differentiation. Gen. Comp. Endocrinol. 167, 344-351.
39. Duguay, S. J. (1999). Post-translational processing of insulin-like growth factors. Horm. Metab. Res. 31, 43-49.
40. Duguay, S. J., Lai-Zhang, J., and Steiner, D. F. (1995). Mutational analysis of the insulin-like growth factor I prohormone processing site. J. Biol. Chem. 270, 17566- 17574.
41. Federici, M., Porzio, O., Zucaro, L., Fusco, A., Borboni, P., Lauro, D., et al. (1997). Distribution of insulin/insulin-like growth factor-I hybrid receptors in human tissues. Mol. Cell. Endocrinol. 129, 121-126.
42. Furlanetto, R. W., Harwell, S. E., and Frick, K. K. (1994). Insulin-like growth factor-I induces cyclin-D1 expression in MG63 human osteosarcoma cells in vitro. Mol. Endocrinol. 8, 510-517.
43. Garcia, G. E., Nicole, A., Bhaskaran, S., Gupta, A., Kyprianou, N., and Kumar, A. P. (2006). Akt-and CREB-mediated prostate cancer cell proliferation inhibition by Nexrutine, a Phellodendron amurense extract. Neoplasia 8, 523-533.
44. Gentile, M. A., Nantermet, P. V., Vogel, R. L., Phillips, R., Holder, D., Hodor, P., et al. (2010). Androgen-mediated improvement of body composition and muscle function involves a novel early transcriptional program including IGF1, mechano growth factor, and induction of {beta}-catenin. J. Mol. Endocrinol. 44, 55-73.
45. Gilmour, R. S. (1994). The implications of insulin-like growth factor mRNA heterogeneity. J. Endocrinol. 140, 1-3.
46. Grimberg, A., and Cohen, P. (1999). Growth hormone and prostate cancer, guilty by association?. J. Endocrinol. Invest. 22, 64-73.
47. 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.
48. Harman, S. M., Metter, E. J., Blackman, M. R., Landis, P. K., and Carter, H. B. (2000). Serum levels of insulin-like growth factor I (IGF-I), IGF-II, IGF-binding protein-3, and prostate-specific antigen as predictors of clinical prostate cancer. J. Clin. Endocrinol. Metab. 85, 4258-4265.
49. Hede, M. S., Salimova, E., Piszczek, A., Perlas, E., Winn, N., Nastasi, T., et al. (2012). E-peptides control bioavailability of IGF-1. PLoS ONE 7, e51152. doi:10.1371/journal.pone.0051152
50. Hellawell, G. O., and Brewster, S. F. (2002). Growth factors and their receptors in prostate cancer. BJU Int. 89, 230-240.
51. Hellawell, G. O., Turner, G. D., Davies, D. R., Poulsom, R., Brewster, S. F., and MacAulay, V. M. (2002). Expression of the type 1 insulin-like growth factor receptor is up-regulated in primary prostate cancer and commonly persists in metastatic disease. Cancer Res. 62, 2942-2950.
52. Jansen, M., van Schaik, F. M., Ricker, A. T., Bullock, B., Woods, D. E., Gabbay, K. H., et al. (1983). Sequence of cDNA encoding human insulin-like growth factor I precursor. Nature 306, 609-611.
53. Jones, J. I., and Clemmons, D. R. (1995). Insulin-like growth factors and their binding proteins, biological actions. Endocr. Rev. 16, 3-34.
54. Kajanne, R., Miettinen, P., Tenhunen, M., and Leppa, S. (2009). Transcription factor AP-1 promotes growth and radioresistance in prostate cancer cells. Int. J. Oncol. 35, 1175-1182.
55. Kaleko, M., Rutter, W. J., and Miller, A. D. (1990). Overexpression of the human insulinlike growth factor I receptor promotes ligand-dependent neoplastic transformation. Mol. Cell. Biol. 10, 464-473.
56. Kaminska, B., Gozdz, A., Zawadzka, M., Ellert-Miklaszewska, A., and Lipko, M. (2009). MAPK signal transduction underlying brain inflammation and gliosis as therapeutic target. Anat. Rec. (Hoboken) 292, 1902-1913.
57. Karamanolakis, D., Bogdanos, J., Sourla, A., Milathianakis, C., Tsintavis, A., Lembessis, P., et al. (2002). Molecular evidence-based use of bone resorption-targeted therapy in prostate cancer patients at high risk for bone involvement. Mol. Med. 8, 667-675.
58. Kasprzak, A., Szaflarski, W., Szmeja, J., Andrzejewska, M., Przybyszewska, W., Kaczmarek, E., et al. (2012). Differential expression of IGF-1 mRNA isoforms in colorectal carcinoma and normal colon tissue. Int. J. Oncol. 42, 305-316.
59. Katopodis, H., Philippou, A., Tenta, R., Doillon, C., Papachroni, K. K., Papavassiliou, A. G., et al. (2009). MG-63 osteoblast-like cells enhance the osteoprotegerin expression of PC-3 prostate cancer cells. Anticancer Res. 29, 4013-4018.
60. Kawada, M., Inoue, H., Masuda, T., and Ikeda, D. (2006). Insulin-like growth factor I secreted from prostate stromal cells mediates tumor-stromal cell interactions of prostate cancer. Cancer Res. 66, 4419-4425.
61. Khosravi, J., Diamandi, A., Mistry, J., and Scorilas, A. (2001). Insulin-like growth factor I (IGF-I) and IGF-binding protein-3 in benign prostatic hyperplasia and prostate cancer. J. Clin. Endocrinol. Metab. 86, 694-699.
62. Kim, E. K., and Choi, E. J. (2010). Pathological roles of MAPK signaling pathways in human diseases. Biochim. Biophys. Acta 1802, 396-405.
63. Koczorowska, M. M., Kwasniewska, A., and Gozdzicka-Jozefiak, A. (2011). IGF1 mRNA isoform expression in the cervix of HPV-positive women with pre-cancerous and cancer lesions. Exp. Ther. Med. 2, 149-156.
64. Kojima, S., Inahara, M., Suzuki, H., Ichikawa, T., and Furuya, Y. (2009). Implications of insulin-like growth factor-I for prostate cancer therapies. Int. J. Urol. 16, 161 -167.
65. Kooijman, R. (2006). Regulation of apoptosis by insulin-like growth factor (IGF)-I. Cytokine Growth Factor Rev. 17, 305-323.
66. Koutsilieris, M. (1993). Osteoblastic metastasis in advanced prostate cancer. Anticancer Res. 13, 443-449.
67. Koutsilieris, M. (1995). Skeletal metastases in advanced prostate cancer, cell biology and therapy. Crit. Rev. Oncol. Hematol. 18, 51-64.
68. Koutsilieris, M., Akoum, A., Lazure, C., Frenette, G., and Lemay, A. (1995). N-terminal truncated forms of insulin-like growth factor binding protein-3 in the peritoneal fluid of women without laparoscopic evidence of endometriosis. Le groupe d'investigation en gynecologie. Fertil. Steril. 63, 314-321.
69. Koutsilieris, M., Laroche, B., Thabet, M., and Fradet, Y. (1990). The assessment of disease aggressivity in stage D2 prostate cancer patients (review). Anticancer Res. 10, 333-336.
70. Koutsilieris, M., Mitsiades, C., Dimopoulos, T., Ioannidis, A., Ntounis, A., and Lambou, T. (2001). A combination therapy of dexamethasone and somatostatin analog reintroduces objective clinical responses to LHRH analog in androgen ablation-refractory prostate cancer patients. J. Clin. Endocrinol. Metab. 86, 5729-5736.
71. Koutsilieris, M., Mitsiades, C., Lembessis, P., and Sourla, A. (2000a). Cancer and bone repair mechanism, clinical applications for hormone refractory prostate cancer. J. Musculoskelet. Neuronal Interact. 1, 15-17.
72. Koutsilieris, M., Mitsiades, C., and Sourla, A. (2000b). Insulin-like growth factor I and urokinase-type plasminogen activator bioregulation system as a survival mechanism of prostate cancer cells in osteoblastic metastases, development of anti-survival factor therapy for hormone-refractory prostate cancer. Mol. Med. 6, 251- 267.
73. Koutsilieris, M., Rabbani, S. A., Bennett, H. P., and Goltzman, D. (1987). Characteristics of prostate-derived growth factors for cells of the osteoblast phenotype. J. Clin. Invest. 80, 941-946.
74. Koutsilieris, M., Rabbani, S. A., and Goltzman, D. (1986). Selective osteoblast mitogens can be extracted from prostatic tissue. Prostate 9, 109-115.
75. Krueckl, S. L., Sikes, R. A., Edlund, N. M., Bell, R. H., Hurtado-Coll, A., Fazli, L., et al. (2004). Increased insulin-like growth factor I receptor expression and signaling are components of androgen-independent progression in a lineage-derived prostate cancer progression model. Cancer Res. 64, 8620-8629.
76. Kuo, Y. H., and Chen, T. T. (2002). Novel activities of pro-IGF-I E peptides, regulation of morphological differentiation and anchorage-independent growth in human neuroblastoma cells. Exp. Cell Res. 280, 75-89.
77. Kuo, Y. H., and Chen, T. T. (2003). Specific cell surface binding sites shared by human Pro-IGF-I Eb-peptides and rainbow trout Pro-IGF-I Ea-4-peptide. Gen. Comp. Endocrinol. 132, 231-240.
78. Laviola, L., Natalicchio, A., and Giorgino, F. (2007). The IGF-I signaling pathway. Curr. Pharm. Des. 13, 663-669.
79. Le Roith, D., Bondy, C., Yakar, S., Liu, J. L., and Butler, A. (2001). The somatomedin hypothesis, 2001. Endocr. Rev. 22, 53-74.
80. LeRoith, D., and Roberts, C. T. Jr. (2003). The insulin-like growth factor system and cancer. Cancer Lett. 195, 127-137.
81. Maroni, P. D., Koul, S., Meacham, R. B., and Koul, H. K. (2004). Mitogen activated protein kinase signal transduction pathways in the prostate. Cell Commun. Signal 2, 5.
82. Meinbach, D. S., and Lokeshwar, B. L. (2006). Insulin-like growth factors and their binding proteins in prostate cancer, cause or consequence?. Urol. Oncol. 24, 294- 306.
83. Milingos, D. S., Philippou, A., Armakolas, A., Papageorgiou, E., Sourla, A., Protopapas, A., et al. (2010). Insulinlike growth factor-1Ec (MGF) expression in eutopic and ectopic endometrium, characterization of the MGF E-peptide actions in vitro. Mol. Med. 17, 21-28.
84. Mills, P., Lafreniere, J. F., Benabdallah, B. F., El Fahime el, M., and Tremblay, J. P. (2007). A new pro-migratory activity on human myogenic precursor cells for a synthetic peptide within the E domain of the mechano growth factor. Exp. Cell Res. 313, 527-537.
85. Mitsiades, C., Sourla, A., Doillon, C., Lembessis, P., and Koutsilieris, M. (2000). Three-dimensional type I collagen co-culture systems for the study of cell-cell interactions and treatment response in bone metastases. J. Musculoskelet. Neuronal Interact. 1, 153-155.
86. Mitsiades, C. S., Bogdanos, J., Karamanolakis, D., Milathianakis, C., Dimopoulos, T., and Koutsilieris, M. (2006). Randomized controlled clinical trial of a combination of somatostatin analog and dexamethasone plus zoledronate vs. zoledronate in patients with androgen ablation-refractory prostate cancer. Anticancer Res. 26, 3693-3700.
87. Monti, S., Proietti-Pannunzi, L., Sciarra, A., Lolli, F., Falasca, P., Poggi, M., et al. (2007). The IGF axis in prostate cancer. Curr. Pharm. Des. 13, 719-727.
88. Moschos, S. J., and Mantzoros, C. S. (2002). The role of the IGF system in cancer, from basic to clinical studies and clinical applications. Oncology 63, 317-332.
89. Mourkioti, F., and Rosenthal, N. (2005). IGF-1, inflammation and stem cells, interactions during muscle regeneration. Trends Immunol. 26, 535-542.
90. Nakae, J., Kido, Y., and Accili, D. (2001). Distinct and overlapping functions of insulin and IGF-I receptors. Endocr. Rev. 22, 818-835.
91. Nickerson, T., Chang, F., Lorimer, D., Smeekens, S. P., Sawyers, C. L., and Pollak, M. (2001). In vivo progression of LAPC-9 and LNCaP prostate cancer models to androgen independence is associated with increased expression of insulin-like growth factor I (IGF-I) and IGF-I receptor (IGF-IR). Cancer Res. 61, 6276-6280.
92. Nickerson, T., Huynh, H., and Pollak, M. (1997). Insulin-like growth factor binding protein-3 induces apoptosis in MCF7 breast cancer cells. Biochem. Biophys. Res. Commun. 237, 690-693.
93. Nimptsch, K., Platz, E. A., Pollak, M. N., Kenfield, S. A., Stampfer, M. J., Willett, W. C., et al. (2011). Plasma insulin-like growth factor 1 is positively associated with low-grade prostate cancer in the Health Professionals Follow-up Study 1993-2004. Int. J. Cancer 128, 660-667.
94. Oh, Y. (1997). IGFBPs and neoplastic models. New concepts for roles of IGFBPs in regulation of cancer cell growth. Endocrine 7, 111-113.
95. Okazaki, R., Durham, S. K., Riggs, B. L., and Conover, C. A. (1995). Transforming growth factor-beta and forskolin increase all classes of insulin-like growth factor-I transcripts in normal human osteoblast-like cells. Biochem. Biophys. Res. Commun. 207, 963-970.
96. Ozkan, E. E. (2011). Plasma and tissue insulin-like growth factor-I receptor (IGF-IR) as a prognostic marker for prostate cancer and anti-IGF-IR agents as novel therapeutic strategy for refractory cases, a review. Mol. Cell. Endocrinol. 344, 1-24.
97. Papageorgiou, E., Pitulis, N., Manoussakis, M., Lembessis, P., and Koutsilieris, M. (2008). Rosiglitazone attenuates insulin-like growth factor 1 receptor survival signaling in PC-3 cells. Mol. Med. 14, 403-411.
98. Papageorgiou, E., Pitulis, N., Msaouel, P., Lembessis, P., and Koutsilieris, M. (2007). The non-genomic crosstalk between PPAR-gamma ligands and ERK1/2 in cancer cell lines. Expert Opin. Ther. Targets 11, 1071-1085.
99. Papatsoris, A. G., Karamouzis, M. V., and Papavassiliou, A. G. (2005). Novel insights into the implication of the IGF-1 network in prostate cancer. Trends. Mol. Med. 11, 52-55.
100. Papatsoris, A. G., Karamouzis, M. V., and Papavassiliou, A. G. (2007). The power and promise of "rewiring" the mitogen-activated protein kinase network in prostate cancer therapeutics. Mol. Cancer Ther. 6, 811-819.
101. Papatsoris, A. G., and Papavassiliou, A. G. (2001). Prostate cancer, horizons in the development of novel anti-cancer strategies. Curr. Med. Chem. Anticancer Agents 1, 47-70.
102. Peehl, D. M., Cohen, P., and Rosenfeld, R. G. (1996). The role of insulin-like growth factors in prostate biology. J. Androl. 17, 2-4.
103. Peruzzi, F., Prisco, M., Dews, M., Salomoni, P., Grassilli, E., Romano, G., et al. (1999). Multiple signaling pathways of the insulin-like growth factor 1 receptor in protection from apoptosis. Mol. Cell. Biol. 19, 7203-7215.
104. Pfeffer, L. A., Brisson, B. K., Lei, H., and Barton, E. R. (2009). The insulin-like growth factor (IGF)-I E-peptides modulate cell entry of the mature IGF-I protein. Mol. Biol. Cell 20, 3810-3817.
105. Philippou, A., Armakolas, A., Panteleakou, Z., Pissimissis, N., Nezos, A., Theos, A., et al. (2011). IGF1Ec expression in MG-63 human osteoblast-like osteosarcoma cells. Anticancer Res. 31, 4259-4265.
106. Philippou, A., Halapas, A., Maridaki, M., and Koutsilieris, M. (2007). Type I insulin-like growth factor receptor signaling in skeletal muscle regeneration and hypertrophy. J. Musculoskelet. Neuronal. Interact. 7, 208-218.
107. Philippou, A., Papageorgiou, E., Bogdanis, G., Halapas, A., Sourla, A., Maridaki, M., et al. (2009). Expression of IGF-1 isoforms after exercise-induced muscle damage in humans, characterization of the MGF E peptide actions in vitro. In vivo 23, 567-575.
108. Philippou, A., Stavropoulou, A., Sourla, A., Pissimissis, N., Halapas, A., Maridaki, M., et al. (2008). Characterization of a rabbit antihuman mechano growth factor (MGF) polyclonal antibody against the last 24 amino acids of the E domain. In vivo 22, 27-35.
109. Pitulis, N., Papageorgiou, E., Tenta, R., Lembessis, P., and Koutsilieris, M. (2009). IL-6 and PPARgamma signalling in human PC-3 prostate cancer cells. Anticancer Res. 29, 2331-2337.
110. Plymate, S. R., Bae, V. L., Maddison, L., Quinn, L. S., and Ware, J. L. (1997). Reexpression of the type 1 insulin-like growth factor receptor inhibits the malignant phenotype of simian virus 40 T antigen immortalized human prostate epithelial cells. Endocrinology 138, 1728-1735.
111. Polychronakos, C., Janthly, U., Lehoux, J. G., and Koutsilieris, M. (1991). Mitogenic effects of insulin and insulin-like growth factors on PA-III rat prostate adenocarcinoma cells, characterization of the receptors involved. Prostate 19, 313-321.
112. Quesada, A., Micevych, P., and Handforth, A. (2009). C-terminal mechano growth factor protects dopamine neurons, a novel peptide that induces heme oxygenase- 1. Exp. Neurol. 220, 255-266.
113. Quesada, A., Ogi, J., Schultz, J., and Handforth, A. (2011). C-terminal mechano-growth factor induces heme oxygenase-1-mediated neuroprotection of SH-SY5Y cells via the protein kinase C/Nrf2 pathway. J. Neurosci. Res. 89, 394-405.
114. Reyes-Moreno, C., and Koutsilieris, M. (1997). Glucocorticoid receptor function possibly modulates cell-cell interactions in osteoblastic metastases on rat skeleton. Clin. Exp. Metastasis 15, 205-217.
115. Reyes-Moreno, C., Sourla, A., Choki, I., Doillon, C., and Koutsilieris, M. (1998). Osteoblast-derived survival factors protect PC-3 human prostate cancer cells from adriamycin apoptosis. Urology 52, 341-347.
116. Reynolds, A. R., and Kyprianou, N. (2006). Growth factor signalling in prostatic growth, significance in tumour development and therapeutic targeting. Br. J. Pharmacol. 147(Suppl. 2), S144-S152.
117. Rotwein, P. (1986). Two insulin-like growth factor I messenger RNAs are expressed in human liver. Proc. Natl. Acad. Sci. U.S.A. 83, 77-81.
118. Rotwein, P., Pollock, K. M., Didier, D. K., and Krivi, G. G. (1986). Organization and sequence of the human insulin-like growth factor I gene. Alternative RNA processing produces two insulin-like growth factor I precursor peptides. J. Biol. Chem. 261, 4828-4832.
119. Rowlands, M. A., Holly, J. M., Gunnell, D., Donovan, J., Lane, J. A., Hamdy, F., et al. (2012). Circulating insulin-like growth factors and IGF-binding proteins in PSA -detected prostate cancer, the large case-control study Protect. Cancer Res. 72, 503-515.
120. Ryan, C. J., Haqq, C. M., Simko, J., Nonaka, D. F., Chan, J. M., Weinberg, V., et al. (2007). Expression of insulin-like growth factor-1 receptor in local and metastatic prostate cancer. Urol. Oncol. 25, 134-140.
121. Sachdev, D., and Yee, D. (2007). Disrupting insulin-like growth factor signaling as a potential cancer therapy. Mol. Cancer Ther. 6, 1-12.
122. Samani, A. A., Yakar, S., LeRoith, D., and Brodt, P. (2007). The role of the IGF system in cancer growth and metastasis, overview and recent insights. Endocr. Rev. 28, 20-47.
123. Shaneyfelt, T., Husein, R., Bubley, G., and Mantzoros, C. S. (2000). Hormonal predictors of prostate cancer, a meta-analysis. J. Clin. Oncol. 18, 847-853.
124. Shavlakadze, T., Winn, N., Rosenthal, N., and Grounds, M. D. (2005). Reconciling data from transgenic mice that overexpress IGF-I specifically in skeletal muscle. Growth Horm. IGF Res. 15, 4-18.
125. Shi, R., Berkel, H. J., and Yu, H. (2001). Insulin-like growth factor-I and prostate cancer, a meta-analysis. Br. J. Cancer 85, 991-996.
126. Siddle, K., Urso, B., Niesler, C. A., Cope, D. L., Molina, L., Surinya, K. H., et al. (2001). Specificity in ligand binding and intracellular signalling by insulin and insulinlike growth factor receptors. Biochem. Soc. Trans. 29, 513-525.
127. Siegfried, J. M., Kasprzyk, P. G., Treston, A. M., Mulshine, J. L., Quinn, K. A., and Cuttitta, F. (1992). A mitogenic peptide amide encoded within the E peptide domain of the insulin-like growth factor IB prohormone. Proc. Natl. Acad. Sci. U.S.A. 89, 8107-8111.
128. Soos, M. A., Nave, B. T., and Siddle, K. (1993). Immunological studies of type I IGF receptors and insulin receptors, characterisation of hybrid and atypical receptor subtypes. Adv. Exp. Med. Biol. 343, 145-157.
129. Sourla, A., Doillon, C., and Koutsilieris, M. (1996). Three-dimensional type I collagen gel system containing MG-63 osteoblasts-like cells as a model for studying local bone reaction caused by metastatic cancer cells. Anticancer Res. 16, 2773-2780.
130. Stattin, P., Bylund, A., Rinaldi, S., Biessy, C., Dechaud, H., Stenman, U. H., et al. (2000). Plasma insulin-like growth factor-I, insulin-like growth factor-binding proteins, and prostate cancer risk, a prospective study. J. Natl. Cancer Inst. 92, 1910-1917.
131. Stattin, P., Rinaldi, S., Biessy, C., Stenman, U. H., Hallmans, G., and Kaaks, R. (2004). High levels of circulating insulin-like growth factor-I increase prostate cancer risk, a prospective study in a population-based nonscreened cohort. J. Clin. Oncol. 22, 3104-3112.
132. Stavropoulou, A., Halapas, A., Sourla, A., Philippou, A., Papageorgiou, E., Papalois, A., et al. (2009). IGF-1 expression in infarcted myocardium and MGF E peptide actions in rat cardiomyocytes in vitro. Mol. Med. 15, 127-135.
133. Steelman, L. S., Chappell, W. H., Abrams, S. L., Kempf, R. C., Long, J., Laidler, P., et al. (2011). Roles of the Raf/MEK/ERK and PI3K/PTEN/Akt/mTOR pathways in controlling growth and sensitivity to therapy-implications for cancer and aging. Aging (Albany NY) 3, 192-222.
134. Stewart, L. V., and Weigel, N. L. (2005). Role of insulin-like growth factor binding proteins in 1alpha,25-dihydroxyvitamin D(3)-induced growth inhibition of human prostate cancer cells. Prostate 64, 9-19.
135. Taguchi, A., and White, M. F. (2008). Insulin-like signaling, nutrient homeostasis, and life span. Annu. Rev. Physiol. 70, 191-212.
136. Temmerman, L., Slonimsky, E., and Rosenthal, N. (2010). Class 2 IGF-1 isoforms are dispensable for viability, growth and maintenance of IGF-1 serum levels. Growth Horm. IGF Res. 20, 255-263.
137. Tenta, R., Katopodis, H., Chatziioannou, A., Pilalis, E., Calvo, E., Luu-The, V., et al. (2007). Microarray analysis of survival pathways in human PC-3 prostate cancer cells. Cancer Genomics Proteomics 4, 309-318.
138. Tenta, R., Sotiriou, E., Pitulis, N., Thyphronitis, G., and Koutsilieris, M. (2005a). Prostate cancer cell survival pathways activated by bone metastasis microenvironment. J. Musculoskelet. Neuronal Interact. 5, 135-144.
139. Tenta, R., Sourla, A., Lembessis, P., Luu-The, V., and Koutsilieris, M. (2005b). Bone microenvironment-related growth factors, zoledronic acid and dexamethasone differentially modulate PTHrP expression in PC-3 prostate cancer cells. Horm. Metab. Res. 37, 593-601.
140. Tenta, R., Tiblalexi, D., Sotiriou, E., Lembessis, P., Manoussakis, M., and Koutsilieris, M. (2004). Bone microenvironment-related growth factors modulate differentially the anticancer actions of zoledronic acid and doxorubicin on PC-3 prostate cancer cells. Prostate 59, 120-131.
141. Wallis, M. (2009). New insulin-like growth factor (IGF).-precursor sequences from mammalian genomes, the molecular evolution of IGFs and associated peptides in primates. Growth Horm. IGF Res. 19, 12-23.
142. Wang, Y. Z., and Wong, Y. C. (1998). Sex hormone-induced prostatic carcinogenesis in the noble rat, the role of insulin-like growth factor-I (IGF-I) and vascular endothelial growth factor (VEGF) in the development of prostate cancer. Prostate 35, 165-177.
143. Werner, H., and Bruchim, I. (2009). The insulin-like growth factor-I receptor as an oncogene. Arch. Physiol. Biochem. 115, 58-71.
144. Werner, H., and LeRoith, D. (1996). The role of the insulin-like growth factor system in human cancer. Adv. Cancer Res. 68, 183-223.
145. Wetterau, L. A., Francis, M. J., Ma, L., and Cohen, P. (2003). Insulin-like growth factor I stimulates telomerase activity in prostate cancer cells. J. Clin. Endocrinol. Metab. 88, 3354-3359.
146. Whitmarsh, A. J. (2007). Regulation of gene transcription by mitogen-activated protein kinase signaling pathways. Biochim. Biophys. Acta 1773, 1285-1298.
147. Woodson, K., Tangrea, J. A., Pollak, M., Copeland, T. D., Taylor, P. R., Virtamo, J., et al. (2003). Serum insulin-like growth factor I, tumor marker or etiologic factor?. A prospective study of prostate cancer among Finnish men. Cancer Res. 63, 3991-3994.
148. Wu, J. D., Haugk, K., Woodke, L., Nelson, P., Coleman, I., and Plymate, S. R. (2006). Interaction of IGF signaling and the androgen receptor in prostate cancer progression. J. Cell. Biochem. 99, 392-401.
149. Wu, S. F., Sun, H. Z., Tu, Z. H., and Wu, H. Y. (2001). Inhibition of cultured rat prostatic epithelial cell growth by epristeride in vitro. Acta Pharmacol. Sin. 22, 257- 263.
150. Yu, H., and Rohan, T. (2000). Role of the insulin-like growth factor family in cancer development and progression. J. Natl. Cancer Inst. 92, 1472-1489.