Inactivation of Rb in stromal fibroblasts promotes epithelial cell invasion

EMBO Journal

Volumn 31, Issue 14, 2012, Pages 3092-3103

  Pickard, Adam ^a   Cichon, Ann Christin ^a   Barry, Anna ^a   Kieran, Declan ^a   Patel, Daksha ^a   Hamilton, Peter ^a   Salto Tellez, Manuel ^a   James, Jacqueline ^a   McCance, Dennis J ^a  

^a QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

Author keywords

invasion; keratinocyte growth factor; MMP1; retinoblastoma; stroma

Indexed keywords

ACTIN; CYCLIN DEPENDENT KINASE 6; FIBROBLAST GROWTH FACTOR 2B; FIBROBLAST GROWTH FACTOR 2C; FIBROBLAST GROWTH FACTOR 6; FIBROBLAST GROWTH FACTOR RECEPTOR 2; GELATINASE A; GELATINASE B; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; GROWTH FACTOR; INTERSTITIAL COLLAGENASE; KERATINOCYTE GROWTH FACTOR; MATRIX METALLOPROTEINASE 14; PROTEIN KINASE B; PROTEIN P107; PROTEIN P130; RETINOBLASTOMA PROTEIN; TRANSCRIPTION FACTOR ETS 2; UNCLASSIFIED DRUG;

ARTICLE; CELL INVASION; CELL PROLIFERATION; CELL TRANSFORMATION; CONTROLLED STUDY; ENZYME INDUCTION; EPITHELIUM CELL; FIBROBLAST; HEAD AND NECK CANCER; HUMAN; HUMAN CELL; OROPHARYNX CANCER; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; STROMA CELL; STROMAL FIBROBLAST; TUMOR GROWTH; UPREGULATION;

CELL LINE, TRANSFORMED; CELL TRANSFORMATION, NEOPLASTIC; EPITHELIAL CELLS; FIBROBLAST GROWTH FACTOR 7; FIBROBLASTS; HUMANS; MATRIX METALLOPROTEINASE 1; PROTO-ONCOGENE PROTEIN C-ETS-2; PROTO-ONCOGENE PROTEINS C-AKT; RETINOBLASTOMA PROTEIN;

EID: 84864123893     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2012.153     Document Type: Article

References (61)

1. Bergamaschi A, Tagliabue E, Sorlie T, Naume B, Triulzi T, Orlandi R, Russnes HG, Nesland JM, Tammi R, Auvinen P, Kosma VM, Menard S, Borresen-Dale AL (2008) Extracellular matrix signature identifies breast cancer subgroups with different clinical outcome. J Pathol 214: 357-367 (Pubitemid 351212391)
2. Bhowmick NA, Neilson EG, Moses HL (2004) Stromal fibroblasts in cancer initiation and progression. Nature 432: 332-337 (Pubitemid 39551661)
3. Borsig L (2010) Heparin as an inhibitor of cancer progression. Prog Mol Biol Translational Sci 93: 335-349
4. Brauchle M, Angermeyer K, Hubner G, Werner S (1994) Large induction of keratinocyte growth factor expression by serum growth factors and pro-inflammatory cytokines in cultured fibroblasts. Oncogene 9: 3199-3204 (Pubitemid 24338446)
5. Buttice G, Duterque-Coquillaud M, Basuyaux JP, Carrere S, Kurkinen M, Stehelin D (1996) Erg, an Ets-family member, differentially regulates human collagenase1 (MMP1) and stromelysin1 (MMP3) gene expression by physically interacting with the Fos/Jun complex. Oncogene 13: 2297-2306 (Pubitemid 27026012)
6. 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 (Pubitemid 24198284)
7. Cully M, You H, Levine AJ, Mak TW (2006) Beyond PTEN mutations: the PI3K pathway as an integrator of multiple inputs during tumorigenesis. Nat Rev 6: 184-192 (Pubitemid 43292562)
8. De Bellis A, Crescioli C, Grappone C, Milani S, Ghiandi P, Forti G, Serio M (1998) Expression and cellular localization of keratinocyte growth factor and its receptor in human hyperplastic prostate tissue. J Clin Endocrinol Metab 83: 2186-2191 (Pubitemid 28496357)
9. de Bruin A, Wu L, Saavedra HI, Wilson P, Yang Y, Rosol TJ, Weinstein M, Robinson ML, Leone G (2003) Rb function in extraembryonic lineages suppresses apoptosis in the CNS of Rbdeficient mice. Proc Nat Acad Sci USA 100: 6546-6551 (Pubitemid 36666618)
10. Dutt A, Salvesen HB, Chen TH, Ramos AH, Onofrio RC, Hatton C, Nicoletti R, Winckler W, Grewal R, Hanna M, Wyhs N, Ziaugra L, Richter DJ, Trovik J, Engelsen IB, Stefansson IM, Fennell T, Cibulskis K, Zody MC, Akslen LA et al (2008) Drug-sensitive FGFR2 mutations in endometrial carcinoma. Proc Nat Acad Sci USA 105: 8713-8717 (Pubitemid 351987745)
11. Eng C, Leone G, Orloff MS, Ostroviski MC (2009) Genomic alterations in tumor stroma. Cancer Res 69: 6759-6764
12. Finak G, Bertos N, Pepin F, Sadekova S, Souleimanova M, Zhao H, Chen H, Omeroglu G, Meterissian S, Omeroglu A, Hallett M, Park M (2008) Stromal gene expression predicts clinical outcome in breast cancer. Nat Med 14: 518-527 (Pubitemid 351655218)
13. 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 (Pubitemid 43923439)
14. Fowles LF, Martin ML, Nelsen L, Stacey KJ, Redd D, Clark YM, Nagamine Y, McMahon M, Hume DA, Ostrowski MC (1998) Persistent activation of mitogen-activated protein kinases p42 and p44 and ets-2 phosphorylation in response to colonystimulating factor 1/c-fms signaling. Mol Cell Biol 18: 5148-5156 (Pubitemid 28388098)
15. Friedl P, Wolf K (2008) Tube travel: the role of proteases in individual and collective cancer cell invasion. Cancer Res 68: 7247-7249
16. Incassati A, Patel D, McCance DJ (2006) Induction of tetraploidy through loss of p53 and upregulation of Plk1 by human papillomavirus type-16 E6. Oncogene 25: 2444-2451
17. Iwano M, Plieth D, Danoff TM, Xue C, Okada H, Neilson EG (2002) Evidence that fibroblasts derive from epithelium during tissue fibrosis. J Clin Invest 110: 341-350 (Pubitemid 34847966)
18. Jameson JM, Cauvi G, Sharp LL, Witherden DA, Havran WL (2005) Gammadelta T cell-induced hyaluronan production by epithelial cells regulates inflammation. J Exp Med 201: 1269-1279 (Pubitemid 40629070)
19. Jiao W, Lin HM, Datta J, Braunschweig T, Chung JY, Hewitt SM, Rane SG (2008) Aberrant nucleocytoplasmic localization of the retinoblastoma tumor suppressor protein in human cancer correlates with moderate/poor tumor differentiation. Oncogene 27: 3156-3164 (Pubitemid 351693165)
20. Kalluri R, Zeisberg M (2006) Fibroblasts in cancer. Nat Rev 6: 392-401
21. Kessenbrock K, Plaks V, Werb Z (2010) Matrix metalloproteinases: regulators of the tumor microenvironment. Cell 141: 52-67
22. Knerer B, Formanek M, Schickinger B, Martinek H, Kornfehl J (1998) Different KGF expression in squamous cell carcinomas of the head and neck and in normal mucosa. Acta Otolaryngol 118: 438-442 (Pubitemid 28273190)
23. Kunii K, Davis L, Gorenstein J, Hatch H, Yashiro M, Di Bacco A, Elbi C, Lutterbach B (2008) FGFR2-amplified gastric cancer cell lines require FGFR2 and Erbb3 signaling for growth and survival. Cancer Res 68: 2340-2348 (Pubitemid 351521808)
24. Leung HY, Mehta P, Gray LB, Collins AT, Robson CN, Neal DE (1997) Keratinocyte growth factor expression in hormone insensitive prostate cancer. Oncogene 15: 1115-1120 (Pubitemid 27401967)
25. Lipinski MM, Macleod KF, Williams BO, Mullaney TL, Crowley D, Jacks T (2001) Cell-autonomous and non-cell-autonomous functions of the Rb tumor suppressor in developing central nervous system. EMBO J 20: 3402-3413 (Pubitemid 32634348)
26. Littlepage LE, Egeblad M, Werb Z (2005) Coevolution of cancer and stromal cellular responses. Cancer Cell 7: 499-500 (Pubitemid 40799241)
27. Liu Y, Hu T, Shen J, Li SF, Lin JW, Zheng XH, Gao QH, Zhou HM (2006) Separation, cultivation and biological characteristics of oral carcinoma-associated fibroblasts. Oral Dis 12: 375-380 (Pubitemid 43926815)
28. Liu H, Knabb JR, Spike BT, Macleod KF (2009) Elevated poly-(ADP-ribose)-polymerase activity sensitizes retinoblastomadeficient cells to DNA damage-induced necrosis. Mol Cancer Res 7: 1099-1109
29. Maandag EC, van der Valk M, Vlaar M, Feltkamp C, O'Brien J, van Roon M, van der Lugt N, Berns A, te Riele H (1994) Developmental rescue of an embryonic-lethal mutation in the retinoblastoma gene in chimeric mice. EMBO J 13: 4260-4268 (Pubitemid 24295198)
30. Maas-Szabowski N, Shimotoyodome A, Fusenig NE (1999) Keratinocyte growth regulation in fibroblast cocultures via a double paracrine mechanism. J Cell Sci 112(Pt 12): 1843-1853 (Pubitemid 29338810)
31. Manavi M, Hudelist G, Fink-Retter A, Gschwandtler-Kaulich D, Pischinger K, Czerwenka K (2007) Gene profiling in Pap-cell smears of high-risk human papillomavirus-positive squamous cervical carcinoma. Gynecol Oncol 105: 418-426 (Pubitemid 46590336)
32. McCance DJ (2005) Human papillomaviruses and cell signaling. Sci STKE 2005: pE29
33. McCance DJ, Kopan R, Fuchs E, Laimins LA (1988) Human papillomavirus type 16 alters human epithelial cell differentiation in vitro. Proc Nat Acad Sci USA 85: 7169-7173
34. Menges CW, Baglia LA, Lapoint R, McCance DJ (2006) Human papillomavirus type 16 E7 up-regulates AKT activity through the retinoblastoma protein. Cancer Res 66: 5555-5559 (Pubitemid 43927104)
35. Mercier I, Casimiro MC, Wang C, Rosenberg AL, Quong J, Minkeu A, Allen KG, Danilo C, Sotgia F, Bonuccelli G, Jasmin JF, Xu H, Bosco E, Aronow B, Witkiewicz A, Pestell RG, Knudsen ES, Lisanti MP (2008) Human breast cancer-associated fibroblasts (CAFs) show caveolin-1 downregulation and RB tumor suppressor functional inactivation: implications for the response to hormonal therapy. Cancer Biol Ther 7: 1212-1225
36. Mittnacht S, Weinberg RA (1991) G1/S phosphorylation of the retinoblastoma protein is associated with an altered affinity for the nuclear compartment. Cell 65: 381-393 (Pubitemid 121002048)
37. Narayan G, Bourdon V, Chaganti S, Arias-Pulido H, Nandula SV, Rao PH, Gissmann L, Durst M, Schneider A, Pothuri B, Mansukhani M, Basso K, Chaganti RS, Murty VV (2007) Gene dosage alterations revealed by cDNA microarray analysis in cervical cancer: identification of candidate amplified and overexpressed genes. Genes Chromosomes Cancer 46: 373-384 (Pubitemid 46411328)
38. Niu J, Chang Z, Peng B, Xia Q, Lu W, Huang P, Tsao MS, Chiao PJ (2007) Keratinocyte growth factor/fibroblast growth factor-7-regulated cell migration and invasion through activation of NF-kappaB transcription factors. J Biol Chem 282: 6001-6011 (Pubitemid 47100871)
39. Orimo A, Weinberg RA (2006) Stromal fibroblasts in cancer: a novel tumor-promoting cell type. Cell Cycle 5: 1597-1601 (Pubitemid 44285243)
40. Ostman A, Augsten M (2009) Cancer-associated fibroblasts and tumor growth-bystanders turning into key players. Curr Opin Genet Dev 19: 67-73
41. Pickard A, Wong PP, McCance DJ (2010) Acetylation of Rb by PCAF is required for nuclear localization and keratinocyte differentiation. J Cell Sci 123: 3718-3726
42. Ron D, Bottaro DP, Finch PW, Morris D, Rubin JS, Aaronson SA (1993) Expression of biologically active recombinant keratinocyte growth factor. Structure/function analysis of amino-terminal truncation mutants. J Biol Chem 268: 2984-2988 (Pubitemid 23057938)
43. Ropiquet F, Huguenin S, Villette JM, Ronfle V, Le Brun G, Maitland NJ, Cussenot O, Fiet J, Berthon P (1999) FGF7/KGF triggers cell transformation and invasion on immortalised human prostatic epithelial PNT1A cells. Int J Cancer 82: 237-243 (Pubitemid 29293783)
44. Shin EY, Ma EK, Kim CK, Kwak SJ, Kim EG (2002) Src/ERK but not phospholipase D is involved in keratinocyte growth factor-stimulated secretion of matrix metalloprotease-9 and urokinase-type plasminogen activator in SNU-16 human stomach cancer cell. J Cancer Res Clin Oncol 128: 596-602
45. Siddiqi I, Funatomi H, Kobrin MS, Friess H, Buchler MW, Korc M (1995) Increased expression of keratinocyte growth factor in human pancreatic cancer. Biochem Biophys Res Commun 215: 309-315
46. Smith JL, Schaffner AE, Hofmeister JK, Hartman M, Wei G, Forsthoefel D, Hume DA, Ostrowski MC (2000) ets-2 is a target for an akt (protein kinase B)/jun N-terminal kinase signaling pathway in macrophages of motheaten-viable mutant mice. Mol Cell Biol 20: 8026-8034
47. Sugimoto H, Mundel TM, Kieran MW, Kalluri R (2006) Identification of fibroblast heterogeneity in the tumor microenvironment. Cancer Biol Ther 5: 1640-1646
48. Takeda M, Arao T, Yokote H, Komatsu T, Yanagihara K, Sasaki H, Yamada Y, Tamura T, Fukuoka K, Kimura H, Saijo N, Nishio K (2007) AZD2171 shows potent antitumor activity against gastric cancer over-expressing fibroblast growth factor receptor 2/keratinocyte growth factor receptor. Clin Cancer Res 13: 3051-3057 (Pubitemid 46849582)
49. Tang A, Gilchrest BA (1996) Regulation of keratinocyte growth factor gene expression in human skin fibroblasts. J Dermatol Sci 11: 41-50 (Pubitemid 26040551)
50. Trimboli AJ, Cantemir-Stone CZ, Li F, Wallace JA, Merchant A, Creasap N, Thompson JC, Caserta E, Wang H, Chong JL, Naidu S, Wei G, Sharma SM, Stephens JA, Fernandez SA, Gurcan MN, Weinstein MB, Barsky SH, Yee L, Rosol TJ et al (2009) Pten in stromal fibroblasts suppresses mammary epithelial tumours. Nature 461: 1084-1091
51. Turner N, Grose R (2010) Fibroblast growth factor signalling: from development to cancer. Nat Rev Cancer 10: 116-129
52. Watanabe M, Ishiwata T, Nishigai K, Moriyama Y, Asano G (2000) Overexpression of keratinocyte growth factor in cancer cells and enterochromaffin cells in human colorectal cancer. Pathol Int 50: 363-372 (Pubitemid 30451479)
53. Weng LP, Brown JL, Baker KM, Ostrowski MC, Eng C (2002) PTEN blocks insulin-mediated ETS-2 phosphorylation through MAP kinase, independently of the phosphoinositide 3-kinase pathway. Hum Mol Genet 11: 1687-1696 (Pubitemid 34812090)
54. Westbrook TF, Nguyen DX, Thrash BR, McCance DJ (2002) E7 abolishes raf-induced arrest via mislocalization of p21(Cip1). Mol Cell Biol 22: 7041-7052
55. Whyatt D, Grosveld F (2002) Cell-nonautonomous function of the retinoblastoma tumour suppressor protein: new interpretations of old phenotypes. EMBO Rep 3: 130-135 (Pubitemid 34213489)
56. Williams BO, Schmitt EM, Remington L, Bronson RT, Albert DM, Weinberg RA, Jacks T (1994) Extensive contribution of Rbdeficient cells to adult chimeric mice with limited histopathological consequences. EMBO J 13: 4251-4259 (Pubitemid 24295197)
57. Wu L, de Bruin A, Saavedra HI, Starovic M, Trimboli A, Yang Y, Opavska J, Wilson P, Thompson JC, Ostrowski MC, Rosol TJ, Woollett LA, Weinstein M, Cross JC, Robinson ML, Leone G (2003) Extra-embryonic function of Rb is essential for embryonic development and viability. Nature 421: 942-947 (Pubitemid 36288025)
58. Yamashita K, Mori M, Kataoka A, Inoue H, Sugimachi K (2001) The clinical significance of MMP-1 expression in oesophageal carcinoma. Br J Cancer 84: 276-282 (Pubitemid 32113457)
59. Zhang J, Chen L, Xiao M, Wang C, Qin Z (2011) FSP1+ fibroblasts promote skin carcinogenesis by maintaining MCP-1-mediated macrophage infiltration and chronic inflammation. Am J Pathol 178: 382-390
60. Zheng J, Siren V, Vaheri A (1996) Keratinocyte growth factor enhances urokinase-type plasminogen activator activity in HPV16 DNA-immortalized human uterine exocervical epithelial cells. Eur J Cell Biol 69: 128-134 (Pubitemid 26052523)
61. Zimmermann S, Moelling K (1999) Phosphorylation and regulation of Raf by Akt (protein kinase B). Science 286: 1741-1744 (Pubitemid 129515882)