Combined CSL and p53 downregulation promotes cancer-associated fibroblast activation

Nature Cell Biology

Volumn 17, Issue 9, 2015, Pages 1193-1204

  Procopio, Maria Giuseppina ^a   Laszlo, Csaba ^a   Al Labban, Dania ^a   Kim, Dong Eun ^a   Bordignon, Pino ^a   Jo, Seung Hee ^b   Goruppi, Sandro ^b   Menietti, Elena ^a   Ostano, Paola ^c   Ala, Ugo ^d   Provero, Paolo ^d   Hoetzenecker, Wolfram ^e   Neel, Victor ^b   Kilarski, Witold W ^f   Swartz, Melody A ^f   Brisken, Cathrin ^f   Lefort, Karine ^a,g   Dotto, G Paolo ^a,b  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c Laboratory of Cancer Genomics   (Italy)

^d UNIVERSITY OF TURIN   (Italy)

^e UNIVERSITY OF ZURICH   (Switzerland)

^f EPFL   (Switzerland)

^g LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

DNA BINDING PROTEIN; FIBROBLAST GROWTH FACTOR; PROTEIN CSL; PROTEIN P53; UNCLASSIFIED DRUG; FIBROBLAST GROWTH FACTOR RECEPTOR; IMMUNOGLOBULIN J RECOMBINATION SIGNAL SEQUENCE BINDING PROTEIN; RBPJ PROTEIN, HUMAN; TP53 PROTEIN, HUMAN;

ACTINIC KERATOSIS; ANIMAL CELL; ARTICLE; CANCER ASSOCIATED FIBROBLAST; CELL ACTIVATION; CELL AGING; CELL EXPANSION; CONTROLLED STUDY; DOWN REGULATION; FIBROBLAST; HUMAN; HUMAN CELL; MALE; MOUSE; MOUTH MUCOSA; NONHUMAN; PRECANCER; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; SQUAMOUS CELL CARCINOMA; STROMA CELL; ANIMAL; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PATHOLOGY; PHYSIOLOGY; SKIN TUMOR; TUMOR CELL LINE;

ANIMALS; CARCINOMA, SQUAMOUS CELL; CELL AGING; CELL LINE, TUMOR; DOWN-REGULATION; FIBROBLASTS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IMMUNOGLOBULIN J RECOMBINATION SIGNAL SEQUENCE-BINDING PROTEIN; MICE; RECEPTORS, FIBROBLAST GROWTH FACTOR; SIGNAL TRANSDUCTION; SKIN NEOPLASMS; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84940589899     PISSN: 14657392     EISSN: 14764679     Source Type: Journal    
DOI: 10.1038/ncb3228     Document Type: Article

References (69)

1. Bissell, M. J., & Hines, W. C. Why dont we get more cancer? A proposed role of the microenvironment in restraining cancer progression. Nat. Med. 17, 320-329 (2011
2. Gatenby, R. Perspective: finding cancers first principles. Nature. 491, S55 (2012
3. Martincorena, I., et al. Tumor evolution. High burden and pervasive positive selection of somatic mutations in normal human skin. Science. 348, 880-886 (2015
4. Lopez-Otin, C., Blasco, M. A., Partridge, L., Serrano, M., & Kroemer, G. The hallmarks of aging. Cell. 153, 1194-1217 (2013
5. Campisi, J., Andersen, J. K., Kapahi, P., & Melov, S. Cellular senescence: a link between cancer and age-related degenerative disease?. Semin. Cancer Biol. 21, 354-359 (2011
6. Kuilman, T., & Peeper, D. S. Senescence-messaging secretome: SMS-ing cellular stress. Nat. Rev. Cancer. 9, 81-94 (2009
7. van Deursen, J. M. The role of senescent cells in ageing. Nature. 509, 439-446 (2014
8. Junttila, M. R., & de Sauvage, F. J. Influence of tumour micro-environment heterogeneity on therapeutic response. Nature. 501, 346-354 (2013
9. Polanska, U. M., & Orimo, A. Carcinoma-Associated fibroblasts: non-neoplastic tumour-promoting mesenchymal cells. J. Cell Physiol. 228, 1651-1657 (2013
10. Hoenicke, L., & Zender, L. Immune surveillance of senescent cells-biological significance in cancer-And non-cancer pathologies. Carcinogenesis. 33, 1123-1126 (2012
11. Bar, J., Moskovits, N., & Oren, M. Involvement of stromal p53 in tumor-stroma interactions. Semin. Cell Dev. Biol. 21, 47-54 (2010
12. Polyak, K., Haviv, I., & Campbell, I. G. Co-evolution of tumor cells and their microenvironment. Trends Genet. 25, 30-38 (2009
13. Tlsty, T. D., & Coussens, L. M. Tumor stroma and regulation of cancer development. Annu. Rev. Pathol. 1, 119-150 (2006
14. Weinberg, R. A. Coevolution in the tumor microenvironment. Nat. Genet. 40, 494-495 (2008
15. Coppe, J. P., et al. Tumor suppressor and aging biomarker p16(INK4a) induces cellular senescence without the associated inflammatory secretory phenotype. J. Biol. Chem. 286, 36396-36403 (2011
16. Kopan, R., & Ilagan, M. X. The canonical Notch signaling pathway: unfolding the activation mechanism. Cell. 137, 216-233 (2009
17. Hu, B., et al. Multifocal epithelial tumors and field cancerization from loss of mesenchymal CSL signaling. Cell. 149, 1207-1220 (2012
18. Ng, Y. Z., et al. Fibroblast-derived dermal matrix drives development of aggressive cutaneous squamous cell carcinoma in patients with recessive dystrophic epidermolysis bullosa. Cancer Res. 72, 3522-3534 (2012
19. Costea, D. E., et al. Identification of two distinct carcinoma-Associated fibroblast subtypes with differential tumor-promoting abilities in oral squamous cell carcinoma. Cancer Res. 73, 3888-3901 (2013
20. Hosein, A. N., et al. Breast carcinoma-Associated fibroblasts rarely contain p53 mutations or chromosomal aberrations. Cancer Res. 70, 5770-5777 (2010
21. Navab, R., et al. Prognostic gene-expression signature of carcinoma-Associated fibroblasts in non-small cell lung cancer. Proc. Natl Acad. Sci. USA. 108, 7160-7165 (2011
22. Iannello, A., Thompson, T. W., Ardolino, M., Lowe, S. W., & Raulet, D. H. p53-dependent chemokine production by senescent tumor cells supports NKG2Ddependent tumor elimination by natural killer cells. J. Exp. Med. 210, 2057-2069 (2013
23. Novakova, Z., et al. Cytokine expression and signaling in drug-induced cellular senescence. Oncogene. 29, 273-284 (2010
24. Yoon, I. K., et al. Exploration of replicative senescence-Associated genes in human dermal fibroblasts by cDNA microarray technology. Exp. Gerontol. 39, 1369-1378 (2004
25. Freund, A., Patil, C. K., & Campisi, J. p38MAPK is a novel DNA damage responseindependent regulator of the senescence-Associated secretory phenotype. EMBO J 30 1536-1548 2011
26. Hinz, B., et al. Recent developments in myofibroblast biology: paradigms for connective tissue remodeling. Am. J. Pathol. 180, 1340-1355 (2012
27. Riley, T., Sontag, E., Chen, P., & Levine, A. Transcriptional control of human p53-regulated genes. Nat. Rev. Mol. Cell Biol. 9, 402-412 (2008
28. Wienken, C. J., Baaske, P., Rothbauer, U., Braun, D., & Duhr, S. Protein-binding assays in biological liquids using microscale thermophoresis. Nat. commun. 1, 100 (2010
29. Lill, N. L., Grossman, S. R., Ginsberg, D., DeCaprio, J., & Livingston, D. M. Binding and modulation of p53 by p300/CBP coactivators. Nature. 387, 823-827 (1997
30. Katoh, M., & Nakagama, H. FGF receptors: cancer biology and therapeutics. Med. Res. Rev. 34, 280-300 (2014
31. Zhou, W., et al. Periostin secreted by glioblastoma stem cells recruits M2 tumourassociated macrophages and promotes malignant growth. Nat. Cell Biol. 17, 170-182 (2015
32. Erez, N., Truitt, M., Olson, P., Arron, S. T., & Hanahan, D. Cancer-Associated Fibroblasts Are Activated in Incipient Neoplasia to Orchestrate Tumor-Promoting Inflammation in an NF-B-Dependent Manner. Cancer Cell. 17, 135-147 (2010
33. Quante, M., et al. Bone marrow-derived myofibroblasts contribute to the mesenchymal stem cell niche and promote tumor growth. Cancer Cell. 19, 257-272 (2011
34. Dotto, G. P. Multifocal epithelial tumors and field cancerization: stroma as a primary determinant. J. Clin. Invest. 124, 1446-1453 (2014
35. Salem, A. F., et al. Cigarette smoke metabolically promotes cancer, via autophagy and premature aging in the host stromal microenvironment. Cell Cycle. 12, 818-825 (2013
36. Castel, D., et al. Dynamic binding of RBPJ is determined by Notch signaling status. Genes Dev. 27, 1059-1071 (2013
37. Johnson, J. E., & Macdonald, R. J. Notch-independent functions of CSL. Curr. Top. Dev. Biol. 97, 55-74 (2011
38. Dotto, G. P. Crosstalk of Notch with p53 and p63 in cancer growth control. Nat. Rev. Cancer. 9, 587-595 (2009
39. Chene, P. Inhibition of the p53-MDM2 interaction: targeting a protein-protein interface. Mol. Cancer Res. 2, 20-28 (2004
40. Del Bianco, C., Aster, J. C., & Blacklow, S. C. Mutational and energetic studies of Notch. 1 transcription complexes. J. Mol. Biol. 376, 131-140 (2008
41. Friedmann, D. R., Wilson, J. J., & Kovall, R. A. RAM-induced allostery facilitates assembly of a notch pathway active transcription complex. J. Biol. Chem. 283, 14781-14791 (2008
42. Lujambio, A., et al. Non-cell-Autonomous tumor suppression by p53. Cell. 153, 449-460 (2013
43. Cooks, T., et al. Mutant p53 prolongs NF-kappaB activation and promotes chronic inflammation and inflammation-Associated colorectal cancer. Cancer cell. 23, 634-646 (2013
44. Devgan, V., Mammucari, C., Millar, S. E., Brisken, C., & Dotto, G. P. p21WAF1/Cip1 is a negative transcriptional regulator of Wnt4 expression downstream of Notch1 activation. Genes Dev 19 1485-1495 2005
45. Dotto, G. P. p21WAF1/Cip1: more than a break to the cell cycle?. Biochim. Biophys. Acta. 87483, 1-14 (2000
46. Warfel, N. A., & El-Deiry, W. S. p21WAF1 and tumourigenesis: 20 years after. Curr. Opin. Oncol. 25, 52-58 (2013
47. Sun, Y., Zeng, X. R., Wenger, L., Firestein, G. S., & Cheung, H. S. P53 down-regulates matrix metalloproteinase-1 by targeting the communications between AP-1 and the basal transcription complex. J. Cell. Biochem. 92, 258-269 (2004
48. Boggs, K., & Reisman, D. C/EBP-participates in regulating transcription of the p53 gene in response to mitogen stimulation. J. Biol. Chem. 282, 7982-7990 (2007
49. Bruno, T., et al. Che-1 phosphorylation by ATM/ATR and Chk2 kinases activates p53 transcription and the G2/M checkpoint. Cancer Cell. 10, 473-486 (2006
50. Kolev, V., et al. EGFR signalling as a negative regulator of Notch1 gene transcription and function in proliferating keratinocytes and cancer. Nat. Cell Biol. 10, 902-911 (2008
51. Phan, R. T., & Dalla-Favera, R. The BCL6 proto-oncogene suppresses p53 expression in germinal-centre B cells. Nature. 432, 635-639 (2004
52. Reisman, D., & Loging, W. T. Transcriptional regulation of the p53 tumor suppressor gene. Semin. Cancer Biol. 8, 317-324 (1998
53. Rowland, B. D., Bernards, R., & Peeper, D. S. The KLF4 tumour suppressor is a transcriptional repressor of p53 that acts as a context-dependent oncogene. Nat. Cell Biol. 7, 1074-1082 (2005
54. Shaulian, E., & Karin, M. AP-1 in cell proliferation and survival. Oncogene. 20, 2390-2400 (2001
55. Stepniak, E., et al. c-Jun/AP-1 controls liver regeneration by repressing p53/p21 and p38 MAPK activity. Genes Dev 20 2306-2314 2006
56. Malchers, F., et al. Cell-Autonomous and non-cell-Autonomous mechanisms of transformation by amplified FGFR1 in lung cancer. Cancer Discov. 4, 246-257 (2014
57. Lefort, K., et al. Notch1 is a p53 target gene involved in human keratinocyte tumor suppression through negative regulation of ROCK1/2 and MRCKalpha kinases. Genes Dev. 21, 562-577 (2007
58. Hu, B., et al. Control of hair follicle cell fate by underlying mesenchyme through a CSL-Wnt5a-FoxN1 regulatory axis. Genes Dev. 24, 1519-1532 (2010
59. Lefort, K., et al. Notch1 is a p53 target gene involved in human keratinocyte tumor suppression through negative regulation of ROCK1/2 and MRCKalpha kinases. Genes Dev. 21, 562-577 (2007
60. Restivo, G., et al. IRF6 is a mediator of Notch pro-differentiation and tumour suppressive function in keratinocytes. EMBO J. 30, 4571-4585 (2011
61. Rheinwald, J. G., & Beckett, M. A. Tumorigenic keratinocyte lines requiring anchorage and fibroblast support cultures from human squamous cell carcinomas. Cancer Res. 41, 1657-1663 (1981
62. Gioanni, J., et al. Two new human tumor cell lines derived from squamous cell carcinomas of the tongue: establishment, characterization and response to cytotoxic treatment. Eur. J. Cancer Clin. Oncol. 24, 1445-1455 (1988
63. Wu, X., et al. Opposing roles for calcineurin and ATF3 in squamous skin cancer. Nature. 465, 368-372 (2010
64. el-Deiry, W. S., et al. WAF1, a potential mediator of p53 tumor suppression. Cell. 75, 817-825 (1993
65. Shalem, O., et al. Genome-scale CRISPR-Cas9 knockout screening in human cells. Science. 343, 84-87 (2014
66. Wu, L., et al. MAML1, a human homologue of Drosophila mastermind, is a transcriptional co-Activator for NOTCH receptors. Nat. Genet. 26, 484-489 (2000
67. Lefort, K., et al A miR-34a-SIRT6 axis in the squamous cell differentiation network. EMBO J 32 2248-2263 2013
68. Kilarski, W. W., et al. Intravital immunofluorescence for visualizing the microcirculatory and immune microenvironments in the mouse ear dermis. PLoS ONE. 8, e57135 (2013
69. Smyth, G. K. Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol. 3, a3 (2004