Essential, non-redundant roles of B-Raf and Raf-1 in Ras-driven skin tumorigenesis

Oncogene

Volumn 32, Issue 19, 2013, Pages 2483-2492

  Kern, F ^a   Doma, E ^a   Rupp, C ^a   Niault, T ^a   Baccarini, M ^a  

^a UNIVERSITY OF VIENNA   (Austria)

Author keywords

B Raf; conditional ablation; epidermis; Raf 1; Ras driven skin tumorigenesis

Indexed keywords

B RAF KINASE; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLETHANOLAMINE BINDING PROTEIN; RAS PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARCINOGENESIS; CELL PROLIFERATION; CONTROLLED STUDY; HUMAN; MELANOMA; MOUSE; NONHUMAN; PRIORITY JOURNAL; SKIN TUMOR;

ANIMALS; CELL LINE, TUMOR; CELL TRANSFORMATION, NEOPLASTIC; MICE; MICE, TRANSGENIC; PROTO-ONCOGENE PROTEINS B-RAF; PROTO-ONCOGENE PROTEINS C-RAF; SIGNAL TRANSDUCTION; SKIN NEOPLASMS;

EID: 84877630310     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2012.254     Document Type: Article

References (44)

1. Kern F, Niault T, Baccarini M. Ras and Raf pathways in epidermis development and carcinogenesis. Br J Cancer 2011; 104: 229-234.
2. Khavari TA, Rinn J. Ras/Erk MAPK signaling in epidermal homeostasis and neoplasia. Cell Cycle 2007; 6: 2928-2931.
3. Oki-Idouchi CE, Lorenzo PS. Transgenic overexpression of RasGRP1 in mouse epidermis results in spontaneous tumors of the skin. Cancer Res 2007; 67: 276-280.
4. Vitale-Cross L, Amornphimoltham P, Fisher G, Molinolo AA, Gutkind JS. Conditional expression of K-ras in an epithelial compartment that includes the stem cells is sufficient to promote squamous cell carcinogenesis. Cancer Res 2004; 64: 8804-8807.
5. Sibilia M, Fleischmann A, Behrens A, Stingl L, Carroll J, Watt FM et al. The EGF receptor provides an essential survival signal for SOS-dependent skin tumor development. Cell 2000; 102: 211-220.
6. Wang Z, Pedersen E, Basse A, Lefever T, Peyrollier K, Kapoor S et al. Rac1 is crucial for Ras-dependent skin tumor formation by controlling Pak1-Mek-Erk hyper-activation and hyperproliferation in vivo. Oncogene 2010.
7. Murayama K, Kimura T, Tarutani M, Tomooka M, Hayashi R, Okabe M et al. Akt activation induces epidermal hyperplasia and proliferation of epidermal progenitors. Oncogene 2007; 26: 4882-4888.
8. Malliri A, van der Kammen RA, Clark K, van der Valk M, Michiels F, Collard JG. Mice deficient in the Rac activator Tiam1 are resistant to Ras-induced skin tumours. Nature 2002; 417: 867-871.
9. Gupta S, Ramjaun AR, Haiko P, Wang Y, Warne PH, Nicke B et al. Binding of ras to phosphoinositide 3-kinase p110alpha is required for ras-driven tumorigenesis in mice. Cell 2007; 129: 957-968.
10. Gonzalez-Garcia A, Pritchard CA, Paterson HF, Mavria G, Stamp G, Marshall CJ. RalGDS is required for tumor formation in a model of skin carcinogenesis. Cancer Cell 2005; 7: 219-226.
11. Galabova-Kovacs G, Matzen D, Piazzolla D, Meissl K, Plyushch T, Chen AP et al. Essential role of B-Raf in ERK activation during extraembryonic development. Proc Natl Acad Sci USA. 2006; 103: 1325-1330.
12. Ehrenreiter K, Piazzolla D, Velamoor V, Sobczak I, Small JV, Takeda J et al. Raf-1 regulates Rho signaling and cell migration. J Cell Biol 2005; 168: 955-964.
13. Scholl FA, Dumesic PA, Barragan DI, Harada K, Bissonauth V, Charron J et al. Mek1/2 MAPK kinases are essential for Mammalian development, homeostasis, and Raf-induced hyperplasia. Dev Cell 2007; 12: 615-629.
14. Dumesic PA, Scholl FA, Barragan DI, Khavari PA, Erk1/2 MAP. kinases are required for epidermal G2/M progression. J Cell Biol 2009; 185: 409-422.
15. Scholl FA, Dumesic PA, Barragan DI, Charron J, Khavari PA. Mek1/2 gene dosage determines tissue response to oncogenic Ras signaling in the skin. Oncogene 2009; 28: 1485-1495.
16. Scholl FA, Dumesic PA, Barragan DI, Harada K, Charron J, Khavari PA. Selective role for Mek1 but not Mek2 in the induction of epidermal neoplasia. Cancer Res 2009; 69: 3772-3778.
17. Bourcier C, Jacquel A, Hess J, Peyrottes I, Angel P, Hofman P et al. p44 mitogen-activated protein kinase (extracellular signal-regulated kinase 1)-dependent signaling contributes to epithelial skin carcinogenesis. Cancer Res 2006; 66: 2700-2707.
18. Ehrenreiter K, Kern F, Velamoor V, Meissl K, Galabova-Kovacs G, Sibilia M et al. Raf-1 addiction in Ras-induced skin carcinogenesis. Cancer Cell 2009; 16: 149-160.
19. Riva C, Lavieille JP, Reyt E, Brambilla E, Lunardi J, Brambilla C. Differential c-myc, c-jun, c-raf and p53 expression in squamous cell carcinoma of the head and neck: Implication in drug and radioresistance. Eur J Cancer B Oral Oncol 1995; 31: 384-391.
20. Wimmer R, Baccarini M. Partner exchange: protein-protein interactions in the Raf pathway. Trends Biochem Sci 2010; 35: 660-668.
21. Niault TS, Baccarini M. Targets of Raf in tumorigenesis. Carcinogenesis 2010; 31: 1165-1174.
22. Flaherty KT, Puzanov I, Kim KB, Ribas A, McArthur GA, Sosman JA et al. Inhibition of mutated, activated BRAF in metastatic melanoma. N Engl J Med 2010; 363: 809-819.
23. Bollag G, Hirth P, Tsai J, Zhang J, Ibrahim PN, Cho H et al. Clinical efficacy of a RAF inhibitor needs broad target blockade in BRAF-mutant melanoma. Nature 2010; 467: 596-599.
24. Cichowski K, Janne PA. Drug discovery: Inhibitors that activate. Nature 2010; 464: 358-359.
25. Brower V. BRAF inhibitors: research accelerates in wake of positive findings. J Natl Cancer Inst 2010; 102: 214-215.
26. Poulikakos PI, Zhang C, Bollag G, Shokat KM, Rosen N. RAF inhibitors transactivate RAF dimers and ERK signalling in cells with wild-type BRAF. Nature 2010; 464: 427-430.
27. Hatzivassiliou G, Song K, Yen I, Brandhuber BJ, Anderson DJ, Alvarado R et al. RAF inhibitors prime wild-type RAF to activate the MAPK pathway and enhance growth. Nature 2010; 464: 431-435.
28. Su F, Viros A, Milagre C, Trunzer K, Bollag G, Spleiss O et al. RAS mutations in cutaneous squamous-cell carcinomas in patients treated with BRAF inhibitors. N Engl J Med 2012; 366: 207-215.
29. Indra AK, Warot X, Brocard J, Bornert JM, Xiao JH, Chambon P et al. Temporally-controlled site-specific mutagenesis in the basal layer of the epidermis: comparison of the recombinase activity of the tamoxifen-inducible Cre-ER(T) and Cre-ER(T2) recombinases. Nucleic Acids Res 1999; 27: 4324-4327.
30. Ise K, Nakamura K, Nakao K, Shimizu S, Harada H, Ichise T et al. Targeted deletion of the H-ras gene decreases tumor formation in mouse skin carcinogenesis. Oncogene 2000; 19: 2951-2956.
31. Dajee M, Lazarov M, Zhang JY, Cai T, Green CL, Russell AJ et al. NF-kappaB blockade and oncogenic Ras trigger invasive human epidermal neoplasia. Nature 2003; 421: 639-643.
32. Quintanilla M, Brown K, Ramsden M, Balmain A. Carcinogen-specific mutation and amplification of Ha-ras during mouse skin carcinogenesis. Nature 1986; 322: 78-80.
33. Lichtenberger BM, Tan PK, Niederleithner H, Ferrara N, Petzelbauer P, Sibilia M. Autocrine VEGF signaling synergizes with EGFR in tumor cells to promote epithelial cancer development. Cell 2010; 140: 268-279.
34. Maurer G, Tarkowski B, Baccarini M. Raf kinases in cancer-roles and therapeutic opportunities. Oncogene 2011; 30: 3477-3488.
35. Lock FE, Hotchin NA. Distinct roles for ROCK1 and ROCK2 in the regulation of keratinocyte differentiation. PLoS ONE 2009; 4: e8190.
36. McMullan R, Lax S, Robertson VH, Radford DJ, Broad S, Watt FM et al. Keratinocyte differentiation is regulated by the Rho and ROCK signaling pathway. Curr Biol 2003; 13: 2185-2189.
37. Honma M, Benitah SA, Watt FM. Role of LIM kinases in normal and psoriatic human epidermis. Mol Biol Cell 2006; 17: 1888-1896.
38. Karreth FA, Frese KK, Denicola GM, Baccarini M, Tuveson DA. C-Raf is required for the initiation of lung cancer by K-Ras. Cancer Discov 2011; 1: 128-136.
39. Blasco RB, Francoz S, Santamaria D, Canamero M, Dubus P, Charron J et al. c-Raf, but not B-Raf, is essential for development of K-Ras oncogene-driven non-small cell lung carcinoma. Cancer Cell 2011; 19: 652-663.
40. Ridky TW, Khavari PA. Pathways sufficient to induce epidermal carcinogenesis. Cell Cycle 2004; 3: 621-624.
41. Solit DB, Rosen N. Resistance to BRAF inhibition in melanomas. N Engl J Med 2011; 364: 772-774.
42. Downward J. Targeting RAF: trials and tribulations. Nat Med 2011; 17: 286-288.
43. Montagut C, Sharma SV, Shioda T, McDermott U, Ulman M, Ulkus LE et al. Elevated CRAF as a potential mechanism of acquired resistance to BRAF inhibition in melanoma. Cancer Res 2008; 68: 4853-4861.
44. Heidorn SJ, Milagre C, Whittaker S, Nourry A, Niculescu-Duvas I, Dhomen N et al. Kinase-dead BRAF and oncogenic RAS cooperate to drive tumor progression through CRAF. Cell 2010; 140: 209-221.