Unexpected roles for pRb in mouse skin carcinogenesis

Cancer Research

Volumn 65, Issue 21, 2005, Pages 9678-9686

  Ruiz, Sergio ^a,b   Santos, Mirentxu ^a   Fernanda Lara, M ^a   Segrelles, Carmen ^a   Ballestín, Claudio ^a   Paramio, Jesús M ^a,c  

^a HOSPITAL UNIVERSITARIO 12 DE OCTUBRE   (Spain)

^b UNIVERSITY OF SALAMANCA   (Spain)

^c CIEMAT   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

GENE PRODUCT; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN KINASE B; PROTEIN P19; PROTEIN P53; RETINOBLASTOMA PROTEIN; STRESS ACTIVATED PROTEIN KINASE; SYNAPTOPHYSIN; TRANSCRIPTION FACTOR E2F;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CANCER MODEL; CELL CYCLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; CHEMICAL CARCINOGENESIS; CONTROLLED STUDY; CORRELATION ANALYSIS; ENZYME ACTIVITY; GEL MOBILITY SHIFT ASSAY; GENE DELETION; GENE FUNCTION; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; KERATINOCYTE; MALIGNANT TRANSFORMATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; SKIN CARCINOGENESIS; SKIN CARCINOMA; SKIN PAPILLOMA; SQUAMOUS CELL CARCINOMA; TUMOR SUPPRESSOR GENE; TUMOR VOLUME;

9,10-DIMETHYL-1,2-BENZANTHRACENE; ANIMALS; APOPTOSIS; CARCINOGENS; CARCINOMA, SQUAMOUS CELL; CELL TRANSFORMATION, NEOPLASTIC; E2F TRANSCRIPTION FACTORS; MICE; PAPILLOMA; PHOSPHORYLATION; RETINOBLASTOMA PROTEIN; SIGNAL TRANSDUCTION; SKIN NEOPLASMS; TUMOR SUPPRESSOR PROTEIN P53;

EID: 27544507280     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-05-1853     Document Type: Article

References (54)

1. Harbour JW, Dean DC. The Rb/E2F pathway: expanding roles and emerging paradigms. Genes Dev 2000; 14:2393-409.
2. Sherr CJ. The INK4a/ARF network in tumour suppression. Nat Rev Mol Cell Biol 2001;2:731-7.
3. Sellers WR, Kaelin WG, Jr. Role of the retinoblastoma protein in the pathogenesis of human cancer. J Clin Oncol 1997;15:3301-12.
4. Dannenberg JH, Schuijff L, Dekker M, van der Valk M, Riele HT. Tissue-specific tumor suppressor activity of retinoblastoma gene homologs p107 and p130. Genes Dev 2004;18:2952-62.
5. Denning MF, Dlugosz AA, Cheng C, et al. Cross-talk between epidermal growth factor receptor and protein kinase C during calcium-induced differentiation of keratinocytes. Exp Dermatol 2000;9:192-9.
6. Robles AI, Rodriguez-Puebla ML, Glick AB, et al. Reduced skin tumor development in cyclin D1-deficient mice highlights the oncogenic ras pathway in vivo. Genes Dev 1998;12:2469-74.
7. Rodriguez-Puebla ML, Miliani de Marval PL, LaCava M, et al. Cdk4 deficiency inhibits skin tumor development but does not affect normal keratinocyte proliferation. Am J Pathol 2002;161:405-11.
8. Miliani De Marval PL, Macias E, Conti CJ, Rodriguez-Puebla ML. Enhanced malignant tumorigenesis in Cdk4 transgenic mice. Oncogene 2004;23:1863-73.
9. Sotillo R, Garcia JF, Ortega S, et al. Invasive melanoma in Cdk4-targeted mice. Proc Natl Acad Sci U S A 2001; 98:13312-7.
10. Paramio JM, Segrelles C, Ruiz S, et al. The ink4a/arf tumor suppressors cooperate with p21cip1/waf in the processes of mouse epidermal differentiation, senescence, and carcinogenesis. J Biol Chem 2001;276:44203-11.
11. Wang D, Russell J, Xu H, Johnson DG. Deregulated expression of DPI induces epidermal proliferation and enhances skin carcinogenesis. Mol Carcinog 2001;31: 90-100.
12. Wang D, Russell JL, Johnson DG. E2F4 and E2F1 have similar proliferative properties but different apoptotic and oncogenic properties in vivo. Mol Cell Biol 2000; 20:3417-24.
13. Pierce AM. Schneider-Broussard R, Gimenez-Conti IB, et al. E2F1 has both oncogenic and tumor-suppressive properties in a transgenic model. Mol Cell Biol 1999;19:6408-14.
14. Pierce AM, Fisher SM, Conti CJ, Johnson DG. Deregulated expression of E2F1 induces hyperplasia and cooperates with ras in skin tumor development. Oncogene 1998;16:1267-76.
15. Pierce AM, Gimenez-Conti IB, Schneider-Broussard R, Martinez LA, Conti CJ, Johnson DG. Increased E2F1 activity induces skin tumors in mice heterozygous and nullizygous for p53. Proc Natl Acad Sci U S A 1998; 95:8858-63.
16. Bito T, Ueda M, Ahmed NU, Nagano T, Ichihashi M. Cyclin D and retinoblastoma gene product expression in actinic keratosis and cutaneous squamous cell carcinoma in relation to p53 expression. J Cutan Pathol 1995; 22:427-34.
17. Edwards MJ, Thomas RC, Wong YL. Retinoblastoma gene expression in human non-melanoma skin cancer. J Cutan Pathol 2003;30:479-85.
18. Lee EY, Chang CY, Hu N, et al. Mice deficient for Rb are nonviable and show defects in neurogenesis and haematopoiesis. Nature 1992;359:288-94.
19. Clarke AR, Maandag ER, van Roon M, et al. Requirement for a functional Rb-1 gene in murine development. Nature 1992;359:328-30.
20. Jacks T, Fazeli A, Schmitt EM, et al. Effects of an Rb mutation in the mouse. Nature 1992;359:295-300.
21. Balsitis SJ, Sage J, Duensing S, et al. Recapitulation of the effects of the human papillomavirus type 16 E7 oncogene on mouse epithelium by somatic Rb deletion and detection of pRb-independent effects of E7 in vivo. Mol Cell Biol 2003;23:9094-103.
22. Ruiz S, Santos M. Segrelles C, et al. Unique and overlapping functions of pRb and p107 in the control of proliferation and differentiation in epidermis. Development 2004;131:2737-48.
23. Segrelles C, Ruiz S, Perez P, et al. Functional roles of Akt signaling in mouse skin tumorigenesis. Oncogene 2002;21:53-64.
24. Perez P, Page A, Jorcano JL. Role of phosphorylated p50-NF-κB in the ultraviolet response of mouse skin. Mol Carcinog 2000;27:272-9.
25. Nischt R, Roop DR, Mehrel T, et al. Aberrant expression during two-stage mouse skin carcinogenesis of a type I 47-kDa keratin, K13, normally associated with terminal differentiation of internal stratified epithelia. Mol Carcinog 1988;1:96-108.
26. Larcher F, Bauluz C, Diaz-Guerra M, et al. Aberrant expression of the simple epithelial type II keratin 8 by mouse skin carcinomas but not papillomas. Mol Carcinog 1992;6:112-21.
27. Yamasaki L. Role of the RB tumor suppressor in cancer. Cancer Treat Res 2003;115:209-39.
28. Kemp CJ, Donehower LA, Bradley A, Balmain A Reduction of p53 gene dosage does not increase initiation or promotion but enhances malignant progression of chemically induced skin tumors. Cell 1993; 74:813-22.
29. Rogoff HA, Pickering MT, Debatis ME, Jones S, Kowalik TF. E2F1 induces phosphorylation of p53 that is coincident with p53 accumulation and apoptosis. Mol Cell Biol 2002;22:5308-18.
30. Zoumpourlis V, Solakidi S, Papathoma A, Papaevangeliou D. Alterations in signal transduction pathways implicated in tumour progression during multistage mouse skin carcinogenesis. Carcinogenesis 2003;24:1159-65.
31. Suzuki A, Itami S, Ohishi M, et al. Keratinocyte-specific Pten deficiency results in epidermal hyperplasia, accelerated hair follicle morphogenesis and tumor formation. Cancer Res 2003;63:674-81.
32. Mallikarjuna G, Dhanalakshmi S, Singh RP, Agarwal C, Agarwal R. Silibinin protects against photocarcinogenesis via modulation of cell cycle regulators, mitogen-activated protein kinases, and Akt signaling. Cancer Res 2004;64:6349-56.
33. Singh RP, Tyagi AK, Zhao J, Agarwal R. Silymarin inhibits growth and causes regression of established skin tumors in SENCAR mice via modulation of mitogen-activated protein kinases and induction of apoptosis. Carcinogenesis 2002;23:499-510.
34. Paramio JM, Navarro M, Segrelles C, Gomez-Casero E, Jorcano JL. PTEN tumour suppressor is linked to the cell cycle control through the retinoblastoma protein. Oncogene 1999;18:7462-8.
35. Chaussepied M, Ginsberg D. Transcriptional regulation of AKT activation by E2F. Mol Cell 2004;16:831-7.
36. Stambolic V, MacPherson D, Sas D, et al. Regulation of PTEN transcription by p53. Mol Cell 2001;8:317-25.
37. Ryan KM, Ernst MK, Rice NR, Vousden KH. Role of NF-kB in p53-mediated programmed cell death. Nature 2000;404:892-7.
38. Phillips AC, Ernst MK, Bates S, Rice NR, Vousden KH. E2F-1 potentiates cell death by blocking antiapoptotic signaling pathways. Mol Cell 1999;4:771-81.
39. Bell S, Degitz K, Quirling M, et al. Involvement of NF-kB signalling in skin physiology and disease. Cell Signal 2003;15:1-7.
40. Seitz CS, Lin Q, Deng H, Khavari PA. Alterations in NF-kB function in transgenic epithelial tissue demonstrate a growth inhibitory role for NF-kB. Proc Natl Acad Sci U S A 1998;95:2307-12.
41. van Hogerlinden M, Auer G, Toftgard R. Inhibition of Rel/nuclear factor-kB signaling in skin results in defective DNA damage-induced cell cycle arrest and Ha-ras- and p53-independent tumor development. Oncogene 2002;21:4969-77.
42. Budunova IV, Perez P, Vaden VR, et al. Increased expression of p50-NF-kB and constitutive activation of NF-kB transcription factors during mouse skin carcinogenesis. Oncogene 1999;18:7423-31.
43. Hayden MS, Ghosh S. Signaling to NF-kB. Genes Dev 2004;18:2195-224.
44. Mittnacht S, Paterson H, Olson MF, Marshall CJ. Ras signalling is required for inactivation of the tumour suppressor pRb cell-cycle control protein. Curr Biol 1997;7:219-21.
45. Johnson DG. The paradox of E2F1: oncogene and tumor suppressor gene. Mol Carcinog 2000;27:151-7.
46. Macleod KF, Hu Y, Jacks T. Loss of Rb activates both p53-dependent and independent cell death pathways in the developing mouse nervous system. EMBO J 1996; 15:6178-88.
47. Morgenbesser SD, Williams BO, Jacks T, DePinho RA. p53-dependent apoptosis produced by Rb-deficiency in the developing mouse lens. Nature 1994; 371:72-4.
48. Pan H, Yin C, Dyson NJ, et al. Key roles for E2F1 in signaling p53-dependent apoptosis and in cell division within developing tumors. Mol Cell 1998;2:283-92.
49. Balmain A, Kemp CJ, Burns PA, et al. Functional loss of tumour suppressor genes in multistage chemical carcinogenesis. Princess Takamatsu Symp 1991;22: 97-108.
50. Marino S, Vooijs M, van Der Gulden H, Jonkers J, Berns A. Induction of medulloblastomas in p53-null mutant mice by somatic inactivation of Rb in the external granular layer cells of the cerebellum. Genes Dev 2000;14:994-1004.
51. Flesken-Nikitin A, Choi KC, Eng JP, Shmidt EN, Nikitin AY. Induction of carcinogenesis by concurrent inactivation of p53 and Rb1 in the mouse ovarian surface epithelium. Cancer Res 2003;63:3459-63.
52. Meuwissen R, Linn SC, Linnoila RI, et al. Induction of small cell lung cancer by somatic inactivation of both Trp53 and Rb1 in a conditional mouse model. Cancer Cell 2003;4:181-9.
53. She QB, Chen N, Bode AM, Flavell RA, Dong Z. Deficiency of c-Jun-NH(2)-terminal kinase-1 in mice enhances skin tumor development by 12-0-tetradecanoylphorbol-13-acetate. Cancer Res 2002;62:1343-8.
54. Shim J, Park HS, Kim MJ, et al. Rb protein down-regulates the stress-activated signals through inhibiting c-Jun N-terminal kinase/stress-activated protein kinase. J Biol Chem 2000;275:14107-11.