Induction of Δnp63 by the newly identified keratinocyte-specific transforming growth factor β signaling pathway with Smad2 and IκB kinase α in squamous cell carcinoma

Neoplasia

Volumn 12, Issue 12, 2010, Pages 969-979

  Fukunishi, Nahoko ^a   Katoh, Iyoko ^b   Tomimori, Yoshiya ^c,e   Tsukinoki, Keiichi ^d   Hata, Ryu Ichiro ^d   Nakao, Atsuhito ^b   Ikawa, Yoji ^c,f   Kurata, Shun Ichi ^a  

^a TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^b UNIVERSITY OF YAMANASHI   (Japan)

^c INST OF PHYS AND CHEMICAL RESEARCH   (Japan)

^d KANAGAWA DENTAL COLLEGE   (Japan)

^e Oriental Yeast Co Ltd   (Japan)

^f NATIONAL INSTITUTE OF HEALTH SCIENCES   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

I KAPPA B KINASE ALPHA; PROTEIN P63; SMAD2 PROTEIN; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL CELL; ARTICLE; BINDING SITE; CELL ACTIVATION; CELL STRAIN HEPG2; CONTROLLED STUDY; DISEASE COURSE; ENZYME ACTIVATION; GENE AMPLIFICATION; GENE SILENCING; GENE TARGETING; HUMAN; HUMAN CELL; KERATINOCYTE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; SITE DIRECTED MUTAGENESIS; SQUAMOUS CELL CARCINOMA; TRANSCRIPTION INITIATION SITE; WESTERN BLOTTING;

EID: 78649816004     PISSN: 15228002     EISSN: 14765586     Source Type: Journal    
DOI: 10.1593/neo.101054     Document Type: Article

References (47)

1. Osada M, Ohba M, Kawahara C, Ishioka C, Kanamaru R, Katoh I, Ikawa Y, Nimura Y, Nakagawara A, Obinata M, et al. (1998). Cloning and functional analysis of human p51, which structurally and functionally resembles p53. Nat Med 4, 839-843.
2. Yang A, Kaghad M, Wang Y, Gillett E, Fleming MD, Dotsch V, Andrews NC, Caput D, and McKeon F (1998). p63, a p53 homolog at 3q27-29, encodes multiple products with transactivating, death-inducing, and dominant-negative activities. Mol Cell 2, 305-316.
3. Mills AA, Zheng B, Wang XJ, Vogel H, Roop DR, and Bradley A (1999). p63 is a p53 homologue required for limb and epidermal morphogenesis. Nature 398, 708-713.
4. Yang A, Schweitzer R, Sun D, Kaghad M, Walker N, Bronson RT, Tabin C, Sharpe A, Caput D, Crum C, et al. (1999). p63 is essential for regenerative proliferation in limb, craniofacial and epithelial development. Nature 398, 714-718.
5. Pellegrini G, Dellambra E, Golisano O, Martinelli E, Fantozzi I, Bondanza S, Ponzin D, McKeon F, and De Luca M (2001). p63 identifies keratinocyte stem cells. Proc Natl Acad Sci USA 98, 3156-3161.
6. Senoo M, Pinto F, Crum CP, and McKeon F (2007). p63 is essential for the proliferative potential of stem cells in stratified epithelia. Cell 129, 523-536.
7. Barbareschi M, Pecciarini L, Cangi MG, Macri E, Rizzo A, Viale G, and Doglioni C (2001). p63, a p53 homologue, is a selective nuclear marker of myoepithelial cells of the human breast. Am J Surg Pathol 25, 1054-1060.
8. Hibi K, Trink B, Patturajan M, Westra WH, Caballero OL, Hill DE, Ratovitski EA, Jen J, and Sidransky D (2000). AIS is an oncogene amplified in squamous cell carcinoma. Proc Natl Acad Sci USA 97, 5462-5467.
9. Quade BJ, Yang A, Wang Y, Sun D, Park J, Sheets EE, Cviko A, Federschneider JM, Peters R, McKeon FD, et al. (2001). Expression of the p53 homologue p63 in early cervical neoplasia. Gynecol Oncol 80, 24-29.
10. Koga F, Kawakami S, Kumagai J, Takizawa T, Ando N, Arai G, Kageyama Y, and Kihara K (2003). Impaired ΔNp63 expression associates with reduced β-catenin and aggressive phenotypes of urothelial neoplasms. Br J Cancer 88, 740-747.
11. Higashikawa K, Yoneda S, Tobiume K, Taki M, Shigeishi H, and Kamata N (2007). Snail-induced down-regulation of ΔNp63α acquires invasive phenotype of human squamous cell carcinoma. Cancer Res 67, 9207-9213.
12. Fukushima H, Koga F, Kawakami S, Fujii Y, Yoshida S, Ratovitski E, Trink B, and Kihara K (2009). Loss of ΔNp63α promotes invasion of urothelial carcinomas via N-cadherin/Src homology and collagen/extracellular signal-regulated kinase pathway. Cancer Res 69, 9263-9270.
13. Barbieri CE, Tang LJ, Brown KA, and Pietenpol JA (2006). Loss of p63 leads to increased cell migration and up-regulation of genes involved in invasion and metastasis. Cancer Res 66, 7589-7597.
14. Kurata S, Okuyama T, Osada M, Watanabe T, Tomimori Y, Sato S, Iwai A, Tsuji T, Ikawa Y, and Katoh I (2004). p51/p63 Controls subunit α3 of the major epidermis integrin anchoring the stem cells to the niche. J Biol Chem 279, 50069-50077.
15. Okuyama T, Kurata S, Tomimori Y, Fukunishi N, Sato S, Osada M, Tsukinoki K, Jin HF, Yamashita A, Ito M, et al. (2008). p63(TP63) elicits strong transactivation of the MFG-E8/lactadherin/BA46 gene through interactions between the TA and ΔN isoforms. Oncogene 27, 308-317.
16. Carroll DK, Carroll JS, Leong CO, Cheng F, Brown M, Mills AA, Brugge JS, and Ellisen LW (2006). p63 regulates an adhesion programme and cell survival in epithelial cells. Nat Cell Biol 8, 551-561.
17. Osada M, Park HL, Nagakawa Y, Yamashita K, Fomenkov A, Kim MS, Wu G, Nomoto S, Trink B, and Sidransky D (2005). Differential recognition of response elements determines target gene specificity for p53 and p63. Mol Cell Biol 25, 6077-6089.
18. Koster MI, Dai D, Marinari B, Sano Y, Costanzo A, Karin M, and Roop DR (2007). p63 induces key target genes required for epidermal morphogenesis. Proc Natl Acad Sci USA 104, 3255-3260.
19. Okuyama R, Ogawa E, Nagoshi H, Yabuki M, Kurihara A, Terui T, Aiba S, Obinata M, Tagami H, and Ikawa S (2007). p53 homologue, p51/p63, maintains the immaturity of keratinocyte stem cells by inhibiting Notch1 activity. Oncogene 26, 4478-4488.
20. Bakkers J, Hild M, Kramer C, Furutani-Seiki M, and Hammerschmidt M (2002). Zebrafish ΔNp63 is a direct target of Bmp signaling and encodes a transcriptional repressor blocking neural specification in the ventral ectoderm. Dev Cell 2, 617-627.
21. Zhang YE (2009). Non-Smad pathways in TGF-β signaling. Cell Res 19, 128-139.
22. Ranganathan P, Agrawal A, Bhushan R, Chavalmane A, Kalathur R, Takahashi T, and Kondaiah P (2007). Expression profiling of genes regulated by TGF-β: differential regulation in normal and tumour cells. BMC Genomics 8, 98.
23. Descargues P, Sil AK, Sano Y, Korchynskyi O, Han G, Owens P, Wang X-J, and Karin M (2008). IKKα is a critical coregulator of a Smad4-independent TGFβ- Smad2/3 signaling pathway that controls keratinocyte differentiation. Proc Natl Acad Sci USA 105, 2487-2492.
24. Descargues P, Sil AK, and Karin M (2008). IKKα, a critical regulator of epidermal differentiation and a suppressor of skin cancer. EMBO J 27, 2639-2647.
25. Hu Y, Baud V, Delhase M, Zhang P, Deerinck T, Ellisman M, Johnson R, and Karin M (1999). Abnormal morphogenesis but intact IKK activation in mice lacking the IKKα subunit of IκB kinase. Science 284, 316-320.
26. Takeda K, Takeuchi O, Tsujimura T, Itami S, Adachi O, Kawai T, Sanjo H, Yoshikawa K, Terada N, and Akira S (1999). Limb and skin abnormalities in mice lacking IKK. Science 284, 313-316.
27. Marinari B, Moretti F, Botti E, Giustizieri ML, Descargues P, Giunta A, Stolfi C, Ballaro C, Papoutsaki M, Alema S, et al. (2008). The tumor suppressor activity of IKKα in stratified epithelia is exerted in part via the TGF-α antipro-liferative pathway. Proc Natl Acad Sci USA 105, 17091-17096.
28. Candi E, Terrinoni A, Rufini A, Chikh A, Lena AM, Suzuki Y, Sayan BS, Knight RA, and Melino G (2006). p63 is upstream of IKKα in epidermal development. J Cell Sci 119, 4617-4622.
29. Marinari B, Ballaro C, Koster MI, Giustizieri ML, Moretti F, Crosti F, Papoutsaki M, Karin M, Alema S, Chimenti S, et al. (2008). IKKα is a p63 transcriptional targetinvolvedin the pathogenesis of ectodermaldysplasias.J Invest Dermatol 129, 60-69.
30. Tomimori Y, Katoh I, Kurata S, Okuyama T, Kamiyama R, and Ikawa Y (2004). Evolutionarily conserved expression pattern and trans-regulating activity of Xenopus p51/p63. Biochem Biophys Res Commun 313, 230-236.
31. Nakao A, Imamura T, Souchelnytskyi S, Kawabata M, Ishisaki A, Oeda E, Tamaki K, Hanai J, Heldin CH, Miyazono K, et al. (1997). TGF-β receptor-mediated signalling through Smad2, Smad3 and Smad4. EMBO J 16, 5353-5362.
32. Grande M, Franzen A, Karlsson J-O, Ericson LE, Heldin N-E, and Nilsson M (2002). Transforming growth factor-β and epidermal growth factor synergistically stimulate epithelial to mesenchymal transition (EMT) through a MEK-dependent mechanism in primary cultured pig thyrocytes. J Cell Sci 115, 4227-4236.
33. Lopez-Rovira T, Chalaux E, Massague J, Rosa JL, and Ventura F (2002).Directbind- ingofsmad1andsmad4totwodistinctmotifsmediatesbonemorphogeneticprotein- specific transcriptional activation of Id1 gene. J Biol Chem 277, 3176-3185.
34. De Angelis T, Noe A, Chatterjee M, and Mulholland J (2002). Stromelysin-1 activation correlates with invasiveness in squamous cell carcinoma. J Invest Dermatol 118,759-766.
35. Zhang W, Matrisian L, Holmbeck K, Vick C, and Rosenthal E (2006). Fibro- blast-derived MT1-MMP promotes tumor progression in vitro and in vivo. BMC Cancer 6, 52.
36. Daniel EB, Haleh M, Luma A-S, Ricardo Lopez De C, John AR, and Andres JPK-S (2001). Elevated furin expression in aggressive human head and neck tumors and tumor cell lines. Mol Carcinog 31, 224-232.
37. Hummer BT, Bartlett C, Henry E, and Weissman BE (2003). Expression of Smad4 in the FaDu cell line partially restores TGF-β growth inhibition but is not sufficient to regulate fibronectin expression or suppress tumorigenicity. J Cell Physiol 194, 289-302.
38. Reiss M, Stash EB, Vellucci VF, and Zhou ZL (1991). Activation of the autocrine transforming growth factor α pathway in human squamous carcinoma cells. Cancer Res 51, 6254-6262.
39. Jensen KB, Jones J, and Watt FM (2008). A stem cell gene expression profile of human squamous cell carcinomas. Cancer Lett 272, 23-31.
40. Rheinwald JG and Beckett MA (1980). Defective terminal differentiation in culture as a consistent and selectable character of malignant human keratinocytes. Cell 22, 629-632.
41. Fynan TM, Morgan D, Yuspa SH, Longley BJ Jr, Zhou ZL, and Reiss M (1994). Restoration of differentiation and suppression of tumorigenicity in somatic cell hybrids of human squamous carcinoma cells and keratinocytes. Cell Growth Differ 5, 1293-1300.
42. Thiery JP, Acloque H, Huang RYJ, and Nieto MA (2009). Epithelial-mesenchymal transitions in development and disease. Cell 139, 871-890.
43. Bassi DE, Zhang J, Cenna J, Litwin S, Cukierman E, and Klein-Szanto AJ (2010). Proprotein convertase inhibition results in decreased skin cell proliferation, tumorigenesis, and metastasis. Neoplasia 12, 516-526.
44. Neiva KG, Zhang Z, Miyazawa M, Warner KA, Karl E, and Nor JE (2009). Cross talk initiated by endothelial cells enhances migration and inhibits anoikis of squamous cell carcinoma cells through STAT3/Akt/ERK signaling. Neoplasia 11,583-593.
45. Hembruff SL, Jokar I, Yang L, and Cheng N (2009). Loss of transforming growth factor-β signaling in mammary fibroblasts enhances CCL2 secretion to promote mammary tumor progression through macrophage-dependent and -independent mechanisms. Neoplasia 12, 425-433.
46. Liu B, Xia X, Zhu F, Park E, Carbajal S, Kiguchi K, DiGiovanni J, Fischer SM, and Hu Y (2008). IKKα is required to maintain skin homeostasis and prevent skin cancer. Cancer Cell 14, 212-225.
47. Ghioni P, D'Alessandra Y, Mansueto G, Jaffray E, Hay RT, La Mantia G, and Guerrini L (2005). The protein stability and transcriptional activity of p63α are regulated by SUMO-1 conjugation. Cell Cycle 4, 183-190.