TNFα Modulates Fibroblast Growth Factor Receptor 2 Gene Expression through the pRB/E2F1 Pathway: Identification of a Non-Canonical E2F Binding Motif

PLoS ONE

Volumn 8, Issue 4, 2013, Pages

  D'Amici, Sirio ^a   Ceccarelli, Simona ^a   Vescarelli, Enrica ^a   Romano, Ferdinando ^b   Frati, Luigi ^a   Marchese, Cinzia ^a   Angeloni, Antonio ^b  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

FIBROBLAST GROWTH FACTOR RECEPTOR 2; INTERLEUKIN 1BETA; INTERLEUKIN 2; KERATINOCYTE GROWTH FACTOR RECEPTOR; MESSENGER RNA; RAF PROTEIN; RETINOBLASTOMA PROTEIN; SYNAPTOPHYSIN; TRANSCRIPTION FACTOR E2F; TRANSCRIPTION FACTOR E2F1; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; EPITHELIUM CELL; GENE; GENE DELETION; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; KERATINOCYTE GROWTH FACTOR RECEPTOR GENE; MESENCHYME CELL; MOLECULAR MODEL; PROMOTER REGION; PROTEIN BINDING; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MOTIF; RETINOBLASTOMA PROTEIN GENE; SEQUENCE ANALYSIS; SITE DIRECTED MUTAGENESIS; TRANSCRIPTION REGULATION; UPREGULATION;

BLOTTING, WESTERN; CELL LINE; CELL LINE, TUMOR; E2F1 TRANSCRIPTION FACTOR; HUMANS; IMMUNOPRECIPITATION; MICROSCOPY, FLUORESCENCE; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTOR, FIBROBLAST GROWTH FACTOR, TYPE 2; SIGNAL TRANSDUCTION; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84876163737     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0061491     Document Type: Article

References (68)

1. Donjacour AA, Cunha GR, (1991) Stromal regulation of epithelial function. Cancer Treat Res 53: 335-364.
2. Fusenig NE (1994) Epithelial-mesenchymal interactions regulate keratinocyte growth and differentiation in vitro. In: Leigh I, Lane B, Watt F, editors. The Keratinocyte Handbook. Cambridge: Cambridge University Press. 71-94.
3. Mackenzie IC (1994) Epithelial-mesenchymal interactions in the development and maintenance of epithelial tissues. In: Leigh I, Lane B, Watt F, editors. The Keratinocyte Handbook. Cambridge: Cambridge University Press. 243-257.
4. Chung LW, (1993) Implications of stromal-epithelial interaction in human prostate cancer growth, progression and differentiation. Semin Cancer Biol 4: 183-192.
5. Cullen KJ, Lippman ME, (1992) Stromal-epithelial interactions in breast cancer. Cancer Treat Res 61: 413-431.
6. Sawhney N, Garrahan N, Douglas-Jones AG, Williams ED, (1992) Epithelial-stromal interactions in tumors. A morphologic study of fibroepithelial tumors of the breast. Cancer 70: 2115-2120.
7. Nathan C, Sporn M, (1991) Cytokines in context. J Cell Biol 113: 981-986.
8. Johnson DE, Williams LT, (1993) Structural and functional diversity in the FGF receptor multigene family. Adv Cancer Res 60: 1-41.
9. Finch PW, Rubin JS, Miki T, Ron D, Aaronson SA, (1989) Human KGF is FGF-related with properties of a paracrine effector of epithelial cell growth. Science 245: 752-755.
10. Luger TA, Schwarz T, (1995) The role of cytokines and neuroendocrine hormones in cutaneous immunity and inflammation. Allergy 50: 292-302.
11. Appleton I, (1994) Wound repair: the role of cytokines and vasoactive mediators. J R Soc Med 87: 500-502.
12. Gailit J, Clark RA, (1994) Wound repair in the context of extracellular matrix. Curr Opin Cell Biol 6: 717-725.
13. Luger TA, Bhardwaj RS, Grabbe S, Schwarz T, (1996) Regulation of the immune response by epidermal cytokines and neurohormones. J Dermatol Sci 13: 5-10.
14. Werner S, Peters KG, Longaker MT, Fuller-Pace F, Banda MJ, et al. (1992) Large induction of keratinocyte growth factor expression in the dermis during wound healing. Proc Natl Acad Sci USA 89: 6896-6900.
15. Smola H, Thiekötter G, Fusenig NE, (1993) Mutual induction of growth factor gene expression by epidermal-dermal cell interaction. J Cell Biol 122: 417-429.
16. Smola H, Thiekötter G, Baur M, Stark HJ, Breitkreutz D, et al. (1994) Organotypic and epidermal-dermal co-cultures of normal human keratinocytes and dermal cells: Regulation of transforming growth factor alpha, beta1 and beta2 mRNA levels. Toxicol In Vitro 8: 641-650.
17. Werner S, Grose R, (2003) Regulation of wound healing by growth factors and cytokines. Physiol Rev 83: 835-870.
18. Chedid M, Rubin JS, Csaky KG, Aaronson SA, (1994) Regulation of keratinocyte growth factor gene expression by interleukin 1. J Biol Chem 269: 10753-10757.
19. Maas-Szabowski N, Shimotoyodome A, Fusenig NE, (1999) Keratinocyte growth regulation in fibroblast cocultures via a double paracrine mechanism. J Cell Sci 112: 1843-1853.
20. Palmieri C, Roberts-Clark D, Assadi-Sabet A, Coope RC, O'Hare M, et al. (2003) Fibroblast growth factor 7, secreted by breast fibroblasts, is an interleukin-1beta-induced paracrine growth factor for human breast cells. J Endocrinol 177: 65-81.
21. Tang A, Gilchrest BA, (1996) Regulation of keratinocyte growth factor gene expression in human skin fibroblasts. J Dermatol Sci 11: 41-50.
22. Samaniego F, Markham PD, Gendelman R, Gallo RC, Ensoli B, (1997) Inflammatory cytokines induce endothelial cells to produce and release basic fibroblast growth factor and to promote Kaposi's sarcoma-like lesions in nude mice. J Immunol 158: 1887-1894.
23. Samaniego F, Markham PD, Gendelman R, Watanabe Y, Kao V, et al. (1998) Vascular endothelial growth factor and basic fibroblast growth factor present in Kaposi's sarcoma (KS) are induced by inflammatory cytokines and synergize to promote vascular permeability and KS lesion development. Am J Pathol 152: 1433-1443.
24. Ekuni D, Firth JD, Putnins EE, (2006) Regulation of epithelial cell growth factor receptor protein and gene expression using a rat periodontitis model. J Periodontal Res 41: 340-349.
25. Marchese C, Chedid M, Dirsch OR, Csaky KG, Santanelli F, et al. (1995) Modulation of keratinocyte growth factor and its receptor in reepithelializing human skin. J Exp Med 182: 1369-1376.
26. Werner S, Breeden M, Hubner G, Greenhalgh DG, Longaker MT, (1994) Induction of keratinocyte growth factor expression is reduced and delayed during wound healing in the genetically diabetic mouse. J Invest Dermatol 103: 469-473.
27. Cottoni F, Ceccarelli S, Masala MV, Montesu MA, Satta R, et al. (2009) Overexpression of the fibroblast growth factor receptor 2-IIIc in Kaposi's sarcoma. J Dermatol Sci 53: 65-68.
28. Skroza N, Rotolo S, Ceccarelli S, Romano F, Innocenzi D, et al. (2008) Modulation of the expression of the FGFR2-IIIb and FGFR2-IIIc molecules in dermatofibroma. J Dermatol Sci 51: 53-57.
29. Yamamoto T, Katayama I, Nishioka K, (1998) Possible involvement of interleukin-1 in the pathogenesis of dermatofibroma. Acta Derm Venereol 78: 99-102.
30. Avivi A, Skorecki K, Yayon A, Givol D, (1992) Promoter region of the murine fibroblast growth factor receptor 2 (bek/KGFR) gene. Oncogene 7: 1957-1962.
31. Becker M, Bräuninger A, Wolf G, Kaufmann M, Strebhardt K, (2000) Identification and functional characterization of the human and murine fibroblast growth factor receptor 4 promoters. Biochem Biophys Res Commun 276: 493-501.
32. McEwen DG, Ornitz DM, (1998) Regulation of the fibroblast growth factor receptor 3 promoter and intron I enhancer by Sp1 family transcription factors. J Biol Chem 273: 5349-5357.
33. Saito H, Kouhara H, Kasayama S, Kishimoto T, Sato B, (1992) Characterization of the promoter region of the murine fibroblast growth factor receptor 1 gene. Biochem Biophys Res Commun 183: 688-693.
34. Slansky JE, Farnham PJ, (1996) Introduction to the E2F family: protein structure and gene regulation. Curr Top Microbiol Immunol 208: 1-30.
35. McClellan KA, Slack RS, (2007) Specific in vivo roles for E2Fs in differentiation and development. Cell Cycle 6: 2917-2927.
36. Helin K, Harlow E, Fattaey A, (1993) Inhibition of E2F-1 transactivation by direct binding of the retinoblastoma protein. Mol Cell Biol 13: 6501-6508.
37. Tashiro E, Minato Y, Maruki H, Asagiri M, Imoto M, (2003) Regulation of FGF receptor-2 expression by transcription factor E2F-1. Oncogene 22: 5630-5635.
38. Tashiro E, Maruki H, Minato Y, Doki Y, Weinstein IB, Imoto M, (2003) Overexpression of cyclin D1 contributes to malignancy by up-regulation of fibroblast growth factor receptor 1 via the pRB/E2F pathway. Cancer Res 63: 424-431.
39. Kanai M, Tashiro E, Maruki H, Minato Y, Imoto M, (2009) Transcriptional regulation of human fibroblast growth factor receptor 1 by E2F-1. Gene 438: 49-56.
40. Scuderi N, Onesti MG, Bistoni G, Ceccarelli S, Rotolo S, et al. (2008) The clinical application of autologous bioengineered skin based on a hyaluronic acid scaffold. Biomaterials 29: 1620-1629.
41. Krek W, Ewen ME, Shirodkar S, Arany Z, Kaelin WG Jr, et al. (1994) Negative regulation of the growth-promoting transcription factor E2F-1 by a stably bound cyclin A-dependent protein kinase. Cell 78: 161-172.
42. Scott RJ, Hall PA, Haldane JS, van Noorden S, Price Y, et al. (1991) A comparison of immunohistochemical markers of cell proliferation with experimentally determined growth fraction. J Pathol 165: 173-178.
43. Parkins CS, Darling JL, Gill SS, Revesz T, Thomas DG, (1991) Cell proliferation in serial biopsies through human malignant brain tumours: measurement using Ki67 antibody labelling. Br J Neurosurg 5: 289-298.
44. Nurcombe V, Smart CE, Chipperfield H, Cool SM, Boilly B, et al. (2000) The proliferative and migratory activities of breast cancer cells can be differentially regulated by heparan sulfates. J Biol Chem 275: 30009-30018.
45. Rotolo S, Ceccarelli S, Romano F, Frati L, Marchese C, et al. (2008) Silencing of keratinocyte growth factor receptor restores 5-fluorouracil and tamoxifen efficacy on responsive cancer cells. PLoS One 3: e2528.
46. Yoshimura A, (2006) Signal transduction of inflammatory cytokines and tumor development. Cancer Sci 97: 439-447.
47. Tammali R, Saxena A, Srivastava SK, Ramana KV, (2010) Aldose reductase regulates vascular smooth muscle cell proliferation by modulating G1/S phase transition of cell cycle. Endocrinology 151: 2140-2150.
48. Nevins JR, (1992) E2F: a link between the Rb tumor suppressor protein and viral oncoproteins. Science 258: 424-429.
49. Sun A, Bagella L, Tutton S, Romano G, Giordano A, (2007) From G0 to S phase: a view of the roles played by the retinoblastoma (Rb) family members in the Rb-E2F pathway. J Cell Biochem 102: 1400-1404.
50. Wang S, Nath N, Minden A, Chellappan S, (1999) Regulation of Rb and E2F by signal transduction cascades: divergent effects of JNK1 and p38 kinases. EMBO J 18: 1559-1570.
51. Fernandes DJ, Ravenhall CE, Harris T, Tran T, Vlahos R, et al. (2004) Contribution of the p38MAPK signalling pathway to proliferation in human cultured airway smooth muscle cells is mitogen-specific. Br J Pharmacol 142: 1182-1190.
52. Yeste-Velasco M, Folch J, Pallàs M, Camins A, (2009) The p38(MAPK) signaling pathway regulates neuronal apoptosis through the phosphorylation of the retinoblastoma protein. Neurochem Int 54: 99-105.
53. Read MA, Whitley MZ, Gupta S, Pierce JW, Best J, et al. (1997) Tumor necrosis factor alpha-induced E-selectin expression is activated by the nuclear factor-kappaB and c-JUN N-terminal kinase/p38 mitogen-activated protein kinase pathways. J Biol Chem 272: 2753-2761.
54. Pollock J, McFarlane SM, Connell MC, Zehavi U, Vandenabeele P, et al. (2002) TNF-alpha receptors simultaneously activate Ca2+ mobilisation and stress kinases in cultured sensory neurones. Neuropharmacology 42: 93-106.
55. Davis R, Pillai S, Lawrence N, Sebti S, Chellappan SP, (2012) TNF-α-mediated proliferation of vascular smooth muscle cells involves Raf-1-mediated inactivation of Rb and transcription of E2F1-regulated genes. Cell Cycle 11: 109-118.
56. Basilico C, Moscatelli D, (1992) The FGF family of growth factors and oncogenes. Adv Cancer Res 59: 115-165.
57. Barrientos S, Stojadinovic O, Golinko MS, Brem H, Tomic-Canic M, (2008) Growth factors and cytokines in wound healing. Wound Repair Regen 16: 585-601.
58. Rubin JS, Bottaro DP, Chedid M, Miki T, Ron D, et al. (1995) Keratinocyte growth factor as a cytokine that mediates mesenchymal-epithelial interaction. EXS 74: 191-214.
59. Werner S, (1998) Keratinocyte growth factor: a unique player in epithelial repair processes. Cytokine Growth Factor Rev 9: 153-165.
60. Sun F, Xie Q, Ma J, Yang S, Chen Q, et al. (2009) Nuclear factor Y is required for basal activation and chromatin accessibility of fibroblast growth factor receptor 2 promoter in osteoblast-like cells. J Biol Chem 284: 3136-3147.
61. Dasgupta P, Sun J, Wang S, Fusaro G, Betts V, et al. (2004) Disruption of the Rb-Raf-1 interaction inhibits tumor growth and angiogenesis. Mol Cell Biol 24: 9527-9541.
62. Dailey L, Ambrosetti D, Mansukhani A, Basilico C, (2005) Mechanisms underlying differential responses to FGF signaling. Cytokine Growth Factor Rev 16: 233-247.
63. Finch PW, Rubin JS, (2006) Keratinocyte growth factor expression and activity in cancer: implications for use in patients with solid tumors. J Natl Cancer Inst 98: 812-824.
64. Gartside MG, Chen H, Ibrahimi OA, Byron SA, Curtis AV, et al. (2009) Loss-of-function fibroblast growth factor receptor-2 mutations in melanoma. Mol Cancer Res 7: 41-54.
65. Katoh M, (2008) Cancer genomics and genetics of FGFR2 (Review). Int J Oncol 33: 233-237.
66. Katoh Y, Katoh M, (2009) FGFR2-related pathogenesis and FGFR2-targeted therapeutics (Review). Int J Mol Med 23: 307-311.
67. St Bernard R, Zheng L, Liu W, Winer D, Asa SL, et al. (2005) Fibroblast growth factor receptors as molecular targets in thyroid carcinoma. Endocrinology 146: 1145-1153.
68. Zhu X, Asa SL, Ezzat S, (2010) Genetic and epigenetic mechanisms down-regulate FGF receptor 2 to induce melanoma-associated antigen A in breast cancer. Am J Pathol 176: 2333-2343.