Activation of the canonical Wnt/β-catenin pathway in ATF3-induced mammary tumors

PLoS ONE

Volumn 6, Issue 1, 2011, Pages

  Yan, Leqin ^a   Coletta, Luis Della ^a   Powell, K Leslie ^a   Shen, Jianjun ^a   Thames, Howard ^b   Aldaz, C Marcelo ^a   MacLeod, Michael C ^a  

^a UNIVERSITY OF TEXAS   (United States)

^b UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 3; BETA CATENIN; MESSENGER RNA; PROTEIN AXIN2; PROTEIN CCND1; PROTEIN DKK4; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR AP 1; TRANSCRIPTION FACTOR JUN; TRANSCRIPTION FACTOR SLUG; TRANSCRIPTION FACTOR SNAI1; TUMOR PROTEIN; UNCLASSIFIED DRUG; WNT PROTEIN; WNT3 PROTEIN; WNT3A PROTEIN; WNT5A PROTEIN; WNT7B PROTEIN; ONCOPROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CANCER; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; FEMALE; GENE FUNCTION; GENE LOCATION; GENE OVEREXPRESSION; GENE TARGETING; MOUSE; NONHUMAN; REPORTER GENE; TRANSCRIPTION INITIATION; TRANSCRIPTION INITIATION SITE; TRANSCRIPTION REGULATION; TRANSGENIC MOUSE; UPREGULATION; ANIMAL; EXPERIMENTAL NEOPLASM; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; HUMAN; METABOLISM; SIGNAL TRANSDUCTION;

GASTROPODA; MUS MUSCULUS;

ACTIVATING TRANSCRIPTION FACTOR 3; ANIMALS; BETA CATENIN; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MAMMARY NEOPLASMS, ANIMAL; MAMMARY NEOPLASMS, EXPERIMENTAL; MICE; MICE, TRANSGENIC; ONCOGENE PROTEIN P65(GAG-JUN); SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC; WNT PROTEINS;

EID: 79551618765     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0016515     Document Type: Article

References (58)

1. Allan AL, Albanese C, Pestell RG, LaMarre J (2001) Activating transcription factor 3 induces DNA synthesis and expression of cyclin D1 in hepatocytes. J Biol Chem 276: 27272-27280.
2. Hai T, Wolfgang CD, Marsee DK, Allen AE, Sivaprasad U (1999) ATF3 and stress responses. Gene Expr 7: 321-335.
3. Hsu JC, Bravo R, Taub R (1992) Interactions among LRF-1, JunB, c-Jun and c- Fos define a regulatory program in the G1 phase of liver regeneration. Mol Biol Cell 12: 4654-4665.
4. Wolfgang CD, Chen BP, Martindale JL, Holbrook NJ, Hai T (1997) gadd153/ Chop10, a potential target gene of the transcriptional repressor ATF3. Mol Cell Biol 17: 6700-6707.
5. Wolfgang CD, Liang G, Okamoto Y, Allen AE, Hai T (2000) Transcriptional autorepression of the stress-inducible gene ATF3. J Biol Chem 275: 16865-16870.
6. Chen BP, Liang G, Whelan J, Hai T (1994) ATF3 and ATF3 delta Zip. Transcriptional repression versus activation by alternatively spliced isoforms. J Biol Chem 269: 15819-15826.
7. Fan F, Jin S, Amundson SA, Tong T, Fan W, et al. (2002) ATF3 induction following DNA damage is regulated by distinct signaling pathways and overexpression of ATF3 protein suppresses cells growth. Oncogene 21: 7488-7496.
8. Hartman MG, Lu D, Kim ML, Kociba GJ, Shukri T, et al. (2004) Role for activating transcription factor 3 in stress-induced beta-cell apoptosis. Mol Cell Biol 24: 5721-5732.
9. Kool J, Hamdi M, Cornelissen-Steijger P, van der Eb AJ, Terleth C, et al. (2003) Induction of ATF3 by ionizing radiation is mediated via a signaling pathway that includes ATM, Nibrin1, stress-induced MAPkinases and ATF-2. Oncogene 22: 4235-4242.
10. Hamdi M, Popeijus HE, Carlotti F, Janssen JM, van der Burgt C, et al. (2008) ATF3 and Fra1 have opposite functions in JNK- and ERK-dependent DNA damage responses. DNA Repair (Amst) 7: 487-496.
11. Yan C, Wang H, Boyd DD (2002) ATF3 Represses 72-kDa Type IV Collagenase (MMP-2) Expression by Antagonizing p53-dependent trans- Activation of the Collagenase Promoter. J Biol Chem 277: 10804-10812.
12. Lu D, Wolfgang CD, Hai T (2006) Activating transcription factor 3, a stressinducible gene, suppresses Ras-stimulated tumorigenesis. J Biol Chem 281: 10473-10481.
13. Turchi L, Aberdam E, Mazure N, Pouyssegur J, Deckert M, et al. (2008) Hif- 2alpha mediates UV-induced apoptosis through a novel ATF3-dependent death pathway. Cell Death Differ 15: 1472-1480.
14. Janz M, Hummel M, Truss M, Wollert-Wulf B, Mathas S, et al. (2006) Classical Hodgkin lymphoma is characterized by high constitutive expression of activating transcription factor 3 (ATF3), which promotes viability of Hodgkin/Reed- Sternberg cells. Blood 107: 2536-2539.
15. Kawauchi J, Zhang C, Nobori K, Hashimoto Y, Adachi MT, et al. (2002) Transcriptional repressor activating transcription factor 3 protects human umbilical vein endothelial cells from tumor necrosis factor-alpha-induced apoptosis through down-regulation of p53 transcription. J Biol Chem 277: 39025-39034.
16. Nakagomi S, Suzuki Y, Namikawa K, Kiryu-Seo S, Kiyama H (2003) Expression of the activating transcription factor 3 prevents c-Jun N-terminal kinase-induced neuronal death by promoting heat shock protein 27 expression and Akt activation. J Neurosci 23: 5187-5196.
17. Nobori K, Ito H, Tamamori-Adachi M, Adachi S, Ono Y, et al. (2002) ATF3 inhibits doxorubicin-induced apoptosis in cardiac myocytes: a novel cardioprotective role of ATF3. J Mol Cell Cardiol 34: 1387-1397.
18. Perez S, Vial E, van Dam H, Castellazzi M (2001) Transcription factor ATF3 partially transforms chick embryo fibroblasts by promoting growth factorindependent proliferation. Oncogene 20: 1135-1141.
19. Yin X, Dewille JW, Hai T (2008) A potential dichotomous role of ATF3, an adaptive-response gene, in cancer development. Oncogene 27: 2118-2127.
20. Wang A, Arantes S, Conti C, McArthur M, Aldaz CM, et al. (2007) Epidermal hyperplasia and oral carcinoma in mice overexpressing the transcription factor ATF3 in basal epithelial cells. Mol Carcinog 46: 476-487.
21. Wang A, Arantes S, Yan L, Kiguchi K, McArthur MJ, et al. (2008) The transcription factor ATF3 acts as an oncogene in mouse mammary tumorigenesis. BMC Cancer 8: 268.
22. Farago M, Dominguez I, Landesman-Bollag E, Xu X, Rosner A, et al. (2005) Kinase-inactive glycogen synthase kinase 3beta promotes Wnt signaling and mammary tumorigenesis. Cancer Res 65: 5792-5801.
23. Imbert A, Eelkema R, Jordan S, Feiner H, Cowin P (2001) Delta N89 betacatenin induces precocious development, differentiation, and neoplasia in mammary gland. J Cell Biol 153: 555-568.
24. Li Q, Dashwood WM, Zhong X, Al-Fageeh M, Dashwood RH (2004) Cloning of the rat beta-catenin gene (Ctnnb1) promoter and its functional analysis compared with the Catnb and CTNNB1 promoters. Genomics 83: 231-242.
25. Miyoshi K, Shillingford JM, LeProvost F, Gounari F, Bronson R, et al. (2002) Activation of b-catenin signaling in differentiated mammary secretory cells induces transdifferentiation into epidermis and squamous metaplasias. Proc Natl Acad Sci U S A 99: 219-224.
26. Miyoshi K, Rosner A, Nozawa M, Byrd C, Morgan F, et al. (2002) Activation of different Wnt/b-catenin signaling components in mammary epithelium induces transdifferentiation and the formation of pilar tumors. Oncogene 21: 5548-55556.
27. Rosner A, Miyoshi K, Landesman-Bollag E, Xu X, Seldin DC, et al. (2002) Pathway pathology: histological differences between ErbB/Ras and Wnt pathway transgenic mammary tumors. Am J Pathol 161: 1087-1097.
28. Teuliere J, Faraldo MM, Deugnier MA, Shtutman M, Ben-Ze'ev A, et al. (2005) Targeted activation of beta-catenin signaling in basal mammary epithelial cells affects mammary development and leads to hyperplasia. Development 132: 267-277.
29. Kinzler KW, Vogelstein B (1996) Lessons from Hereditary Colorectal Cancer. Cell 87: 159-170.
30. Bienz M, Clevers H (2000) Linking colorectal cancer to Wnt signaling. Cell 103: 311-320.
31. Jin Z, Tamura G, Tsuchiya T, Sakata K, Kashiwaba M, et al. (2001) Adenomatous polyposis coli (APC) gene promoter hypermethylation in primary breast cancers. Br J Cancer 85: 69-73.
32. Virmani AK, Rathi A, Sathyanarayana UG, Padar A, Huang CX, et al. (2001) Aberrant methylation of the adenomatous polyposis coli (APC) gene promoter 1A in breast and lung carcinomas. Clin Cancer Res 7: 1998-2004.
33. Suzuki H, Toyota M, Carraway H, Gabrielson E, Ohmura T, et al. (2008) Frequent epigenetic inactivation of Wnt antagonist genes in breast cancer. Br J Cancer 98: 1147-1156.
34. Veeck J, Noetzel E, Bektas N, Jost E, Hartmann A, et al. (2008) Promoter hypermethylation of the SFRP2 gene is a high-frequent alteration and tumorspecific epigenetic marker in human breast cancer. Mol Cancer 7: 83.
35. Logan CY, Nusse R (2004) The Wnt signaling pathway in development and disease. Annu Rev Cell Dev Biol 20: 781-810.
36. Muller W, Sinn E, Pattengale P, Wallace R, Leder P (1988) Single-step induction of mammary adenocarcinoma in transgenic mice bearing the activated c-neu oncogene. Cell 54: 105-115.
37. Das Gupta R, Fuchs E (1999) Multiple roles for activated LEF/TCF transcription complexes during hair follicle development and differentiation. Development 126: 4557-4568.
38. Shtutman M, Zhurinsky J, Simcha I, Albanese C, D'Amico M, et al. (1999) The cyclin D1 gene is a target of the beta-catenin/LEF-1 pathway. Proc Natl Acad Sci U S A 96: 5522-5527.
39. Tetsu O, McCormick F (1999) Beta-catenin regulates expression of cyclin D1 in colon carcinoma cells. Nature 398: 422-426.
40. Mann B, Gelos M, Siedow A, Hanski ML, Gratchev A, et al. (1999) Target genes of beta-catenin-T cell-factor/lymphoid-enhancer-factor signaling in human colorectal carcinomas. Proc Natl Acad Sci U S A 96: 1603-1608.
41. Smeal T, Hibi M, Karin M (1994) Altering the specificity of signal transduction cascades: positive regulation of c-Jun transcriptional activity by protein kinase A. EMBO J 13: 6006-6010.
42. Jho EH, Zhang T, Domon C, Joo CK, Freund JN, et al. (2002) Wnt/betacatenin/ Tcf signaling induces the transcription of Axin2, a negative regulator of the signaling pathway. Mol Cell Biol 22: 1172-1183.
43. Bazzi H, Fantauzzo KA, Richardson GD, Jahoda CA, Christiano AM (2007) The Wnt inhibitor, Dickkopf 4, is induced by canonical Wnt signaling during ectodermal appendage morphogenesis. Dev Biol 305: 498-507.
44. Weber-Hall SJ, Phippard DJ, Neimeyer CC, Dale TC (1994) Developmental and hormonal regulation of Wnt gene expression in the mouse mammary gland. Differentiation 57: 205-214.
45. Gavin BJ, McMahon AP (1992) Differential regulation of the Wnt gene family during pregnancy and lactation suggests a role in postnatal development of the mammary gland. Mol Cell Biol 12: 2418-2423.
46. Storci G, Sansone P, Trere D, Tavolari S, Taffurelli M, et al. (2008) The basallike breast carcinoma phenotype is regulated by SLUG gene expression. J Pathol 214: 25-37.
47. Come C, Magnino F, Bibeau F, De Santa Barbara P, Becker KF, et al. (2006) Snail and slug play distinct roles during breast carcinoma progression. Clin Cancer Res 12: 5395-5402.
48. Moody SE, Perez D, Pan TC, Sarkisian CJ, Portocarrero CP, et al. (2005) The transcriptional repressor Snail promotes mammary tumor recurrence. Cancer Cell 8: 197-209.
49. Nieto MA (2002) The snail superfamily of zinc-finger transcription factors. Nat Rev Mol Cell Biol 3: 155-166.
50. Hayes MJ, Thomas D, Emmons A, Giordano TJ, Kleer CG (2008) Genetic changes of Wnt pathway genes are common events in metaplastic carcinomas of the breast. Clin Cancer Res 14: 4038-4044.
51. Veeck J, Bektas N, Hartmann A, Kristiansen G, Heindrichs U, et al. (2008) Wnt signalling in human breast cancer: expression of the putative Wnt inhibitor Dickkopf-3 (DKK3) is frequently suppressed by promoter hypermethylation in mammary tumours. Breast Cancer Res 10: R82.
52. Stemmer V, de Craene B, Berx G, Behrens J (2008) Snail promotes Wnt target gene expression and interacts with beta-catenin. Oncogene 27: 5075-5080.
53. Yook JI, Li XY, Ota I, Hu C, Kim HS, et al. (2006) A Wnt-Axin2-GSK3beta cascade regulates Snail1 activity in breast cancer cells. Nat Cell Biol 8: 1398-1406.
54. Smid M, Wang Y, Zhang Y, Sieuwerts AM, Yu J, et al. (2008) Subtypes of breast cancer show preferential site of relapse. Cancer Res 68: 3108-3114.
55. DiMeo TA, Anderson K, Phadke P, Fan C, Perou CM, et al. (2009) A novel lung metastasis signature links Wnt signaling with cancer cell self-renewal and epithelial-mesenchymal transition in basal-like breast cancer. Cancer Res 69: 5364-5373.
56. Bertolo C, Guerrero D, Vicente F, Cordoba A, Esteller M, et al. (2008) Differences and molecular immunohistochemical parameters in the subtypes of infiltrating ductal breast cancer. Am J Clin Pathol 130: 414-424.
57. Kreike B, van Kouwenhove M, Horlings H, Weigelt B, Peterse H, et al. (2007) Gene expression profiling and histopathological characterization of triplenegative/ basal-like breast carcinomas. Breast Cancer Res 9: R65.
58. Zhang M, Atkinson RL, Rosen JM (2010) Selective targeting of radiationresistant tumor-initiating cells. Proc Natl Acad Sci U S A 107: 3522-3527.