Mutant p53 amplifies epidermal growth factor receptor family signaling to promote mammary tumorigenesis

Molecular Cancer Research

Volumn 13, Issue 4, 2015, Pages 743-754

  Yallowitz, Alisha R ^a   Li, Dun ^a   Lobko, Anthony ^a   Mott, Daniel ^a   Nemajerova, Alice ^a   Marchenko, Natalia ^a  

^a STONY BROOK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; PROTEIN P53; EGFR PROTEIN, MOUSE; EPIDERMAL GROWTH FACTOR RECEPTOR 2; ERBB2 PROTEIN, MOUSE; TP53 PROTEIN, HUMAN;

ALLELE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREAST CARCINOGENESIS; CANCER SURVIVAL; CELL PROLIFERATION; CONTROLLED STUDY; GENE AMPLIFICATION; GENE MUTATION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; ANIMAL; BREAST TUMOR; CANCER STEM CELL; EXPERIMENTAL MAMMARY NEOPLASM; FEMALE; GENETICS; METABOLISM; MUTATION; PAGET NIPPLE DISEASE; PATHOLOGY; SURVIVAL; TUMOR CELL LINE;

ANIMALIA;

ANIMALS; BREAST NEOPLASMS; CARCINOMA, DUCTAL, BREAST; CELL LINE, TUMOR; CELL PROLIFERATION; FEMALE; HUMANS; MAMMARY NEOPLASMS, EXPERIMENTAL; MICE; MUTATION; NEOPLASTIC STEM CELLS; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTOR, ERBB-2; SIGNAL TRANSDUCTION; SURVIVAL ANALYSIS; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84928023426     PISSN: 15417786     EISSN: 15573125     Source Type: Journal    
DOI: 10.1158/1541-7786.MCR-14-0360     Document Type: Article

References (50)

1. Cancer Genome Atlas N. Comprehensive molecular portraits of human breast tumours. Nature 2012;490:61-70.
2. Masciari S, Dillon DA, Rath M, Robson M, Weitzel JN, Balmana J, et al. Breast cancer phenotype in women with TP53 germline mutations: a Li-Fraumeni syndrome consortium effort. Breast Cancer Res Treat 2012; 133:1125-30.
3. Melhem-Bertrandt A, Bojadzieva J, Ready KJ, Obeid E, Liu DD, Gutierrez-Barrera AM, et al. Early onset HER2-positive breast cancer is associated with germline TP53 mutations. Cancer 2012;118:908-13.
4. Yamashita H, Nishio M, Toyama T, Sugiura H, Zhang Z, Kobayashi S, et al. Coexistence of HER2 over-expression and p53 protein accumulation is a strong prognostic molecular marker in breast cancer. Breast Cancer Res 2004;6:R24-30.
5. Rahko E, Blanco G, Soini Y, Bloigu R, Jukkola A. A mutant TP53 gene status is associated with a poor prognosis and anthracycline-resistance in breast cancer patients. Eur J Cancer 2003;39:447-53.
6. Boulanger CA, Wagner KU, Smith GH. Parity-induced mouse mammary epithelial cells are pluripotent, self-renewing and sensitive to TGF-beta1 expression. Oncogene 2005;24:552-60.
7. Liu S, Wicha MS. Targeting breast cancer stem cells. J Clin Oncol 2010; 28:4006-12.
8. Cicalese A, Bonizzi G, Pasi CE, Faretta M, Ronzoni S, Giulini B, et al. The tumor suppressor p53 regulates polarity of self-renewing divisions in mammary stem cells. Cell 2009;138:1083-95.
9. Sarig R, Rivlin N, Brosh R, Bornstein C, Kamer I, Ezra O, et al. Mutant p53 facilitates somatic cell reprogramming and augments the malignant potential of reprogrammed cells. J Exp Med 2010;207:2127-40.
10. Hanel W, Marchenko N, Xu S, Xiaofeng Yu S,Weng W, Moll U. Twohot spot mutant p53 mouse models display differential gain of function in tumorigenesis. Cell Death Differ 2013;20:898-909.
11. Lu X, Liu DP, Xu Y. The gain of function of p53 cancer mutant in promoting mammary tumorigenesis. Oncogene 2013;32:2900-9.
12. Yarden Y, Pines G. The ERBB network: at last, cancer therapy meets systems biology. Nat Rev Cancer 2012;12:553-63.
13. Sachdev JC, Jahanzeb M. Blockade of the HER family of receptors in the treatment of HER2-positive metastatic breast cancer. Clin Breast Cancer 2012;12:19-29.
14. Korkaya H, Paulson A, Iovino F, Wicha MS. HER2 regulates the mammary stem/progenitor cell population driving tumorigenesis and invasion. Oncogene 2008;27:6120-30.
15. Magnifico A, Albano L, Campaner S, Delia D, Castiglioni F, Gasparini P, et al. Tumor-initiating cells of HER2-positive carcinoma cell lines express the highest oncoprotein levels and are sensitive to trastuzumab. Clin Cancer Res 2009;15:2010-21.
16. Li X, Lewis MT, Huang J, Gutierrez C, Osborne CK, Wu MF, et al. Intrinsic resistance of tumorigenic breast cancer cells to chemotherapy. JNatl Cancer Inst 2008;100:672-9.
17. Mimeault M, Batra SK. Altered gene products involved in the malignant reprogramming of cancer stem/progenitor cells and multitargeted therapies. Mol Aspects Med 2014;39:3-32.
18. Li D, Marchenko ND, Schulz R, Fischer V, Velasco-Hernandez T, Talos F, et al. Functional inactivation of endogenous MDM2 and CHIP by HSP90 causes aberrant stabilization of mutant p53 in human cancer cells. Mol Cancer Res 2011;9:577-88.
19. Dontu G, Abdallah WM, Foley JM, Jackson KW, ClarkeMF, KawamuraMJ, et al. In vitro propagation and transcriptional profiling of humanmammary stem/progenitor cells. Genes Dev 2003;17:1253-70.
20. Lang GA, Iwakuma T, Suh YA, Liu G, Rao VA, Parant JM, et al. Gain of function of a p53 hot spot mutation in a mouse model of Li-Fraumeni syndrome. Cell 2004;119:861-72.
21. Evans SC, Viswanathan M, Grier JD, NarayanaM, El-Naggar AK, Lozano G. An alternatively splicedHDM2 product increases p53 activity by inhibiting HDM2. Oncogene 2001;20:4041-9.
22. Olive KP, Tuveson DA, Ruhe ZC, Yin B, Willis NA, Bronson RT, et al.Mutant p53 gain of function in two mouse models of Li-Fraumeni syndrome. Cell 2004;119:847-60.
23. Muller WJ, Sinn E, Pattengale PK, Wallace R, Leder P. Single-step induction of mammary adenocarcinoma in transgenic mice bearing the activated cneu oncogene. Cell 1988;54:105-15.
24. Brosh R, Rotter V. When mutants gain new powers: news from the mutant p53 field. Nat Rev Cancer 2009;9:701-13.
25. Suh YA, Post SM, Elizondo-Fraire AC, Maccio DR, Jackson JG, El-Naggar AK, et al. Multiple stress signals activate mutant p53 in vivo. Cancer Res 2011;71:7168-75.
26. Terzian T, Suh YA, Iwakuma T, Post SM, Neumann M, Lang GA, et al. The inherent instability of mutant p53 is alleviated byMdm2or p16INK4a loss. Genes Dev 2008;22:1337-44.
27. Lo PK, KanojiaD, Liu X, SinghUP, Berger FG,WangQ, et al. CD49f and CD61 identify Her2/neu-induced mammary tumor-initiating cells that are potentially derived from luminal progenitors and maintained by the integrin-TGFβeta signaling. Oncogene 2012;31:2614-26.
28. Lim E, Wu D, Pal B, Bouras T, Asselin-Labat ML, Vaillant F, et al. Transcriptome analyses of mouse and human mammary cell subpopulations reveal multiple conserved genes and pathways. Breast Cancer Resbreast cancer 2010;12:R21.
29. Henry MD, Triplett AA, Oh KB, Smith GH, Wagner KU. Parity-induced mammary epithelial cells facilitate tumorigenesis in MMTV-neu transgenic mice. Oncogene 2004;23:6980-5.
30. Ginestier C, Hur MH, Charafe-Jauffret E, Monville F, Dutcher J, Brown M, et al. ALDH1 is amarker of normal and malignant humanmammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell 2007;1: 555-67.
31. Van Keymeulen A, Rocha AS, Ousset M, Beck B, Bouvencourt G, Rock J, et al. Distinct stem cells contribute to mammary gland development and maintenance. Nature 2011;479:189-93.
32. Matulka LA, Triplett AA, Wagner KU. Parity-induced mammary epithelial cells are multipotent and express cell surfacemarkers associated with stem cells. Dev Biol 2007;303:29-44.
33. Wagner KU, Boulanger CA, Henry MD, Sgagias M, Hennighausen L, Smith GH. An adjunctmammary epithelial cell population in parous females: its role in functional adaptation and tissue renewal. Development 2002;129: 1377-86.
34. Guo W, Keckesova Z, Donaher JL, Shibue T, Tischler V, Reinhardt F, et al. Slug and Sox9 cooperatively determine the mammary stem cell state. Cell 2012;148:1015-28.
35. Muthuswamy SK, Li D, Lelievre S, Bissell MJ, Brugge JS. ErbB2, but not ErbB1, reinitiates proliferation and induces luminal repopulation in epithelial acini. Nat Cell Biol 2001;3:785-92.
36. Charafe-Jauffret E, Ginestier C, Iovino F, Wicinski J, Cervera N, Finetti P, et al. Breast cancer cell lines contain functional cancer stem cells with metastatic capacity and a distinctmolecular signature. Cancer Res 2009;69: 1302-13.
37. Li D, Yallowitz A, Ozog L, Marchenko N. A gain-of-function mutant p53-HSF1 feed forward circuit governs adaptation of cancer cells to proteotoxic stress. Cell Death Dis 2014;5:e1194.
38. Muller PA, Caswell PT, Doyle B, Iwanicki MP, Tan EH, Karim S, et al. Mutant p53 drives invasion by promoting integrin recycling. Cell 2009; 139:1327-41.
39. Adorno M, Cordenonsi M, Montagner M, Dupont S,Wong C, Hann B, et al. A Mutant-p53/Smad complex opposes p63 to empower TGFβeta-induced metastasis. Cell 2009;137:87-98.
40. Wood ER, Truesdale AT, McDonald OB, Yuan D, Hassell A, Dickerson SH, et al. A unique structure for epidermal growth factor receptor bound to GW572016 (Lapatinib): relationships among protein conformation, inhibitor off-rate, and receptor activity in tumor cells. Cancer Res 2004;64: 6652-9.
41. Song H, Hollstein M, Xu Y. p53 gain-of-function cancer mutants induce genetic instability by inactivating ATM. Nat Cell Biol 2007;9:573-80.
42. Mizuno H, Spike BT, Wahl GM, Levine AJ. Inactivation of p53 in breast cancers correlates with stem cell transcriptional signatures. Proc Natl Acad Sci U S A 2010;107:22745-50.
43. Coradini D, Fornili M, Ambrogi F, Boracchi P, Biganzoli E. TP53 mutation, epithelial-mesenchymal transition, and stemlike features in breast cancer subtypes. J Biomed Biotechnol 2012;2012:254085.
44. Li B, Rosen JM, McMenamin-Balano J, Muller WJ, Perkins AS. neu/ERBB2 cooperates with p53-172H during mammary tumorigenesis in transgenic mice. Mol Cell Biol 1997;17:3155-63.
45. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY, et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 2008;133:704-15.
46. Weissmueller S, Manchado E, Saborowski M, Morris JPt, Wagenblast E, Davis CA, et al.Mutant p53 drives pancreatic cancer metastasis through cell-autonomous PDGF receptor beta signaling. Cell 2014;157: 382-94.
47. Lenfert E, Maenz C, Heinlein C, Jannasch K, Schumacher U, Pantel K, et al. Mutant p53 promotes epithelial-mesenchymal plasticity and enhances metastasis in mammary carcinomas of WAP-T mice. Int J Cancer 2015;136:E521-33.
48. Whitesell L, Lindquist S. Inhibiting the transcription factor HSF1 as an anticancer strategy. Expert Opin Ther Targets 2009;13:469-78.
49. Bissell MJ, Radisky DC, Rizki A, Weaver VM, Petersen OW. The organizing principle: microenvironmental influences in the normal and malignant breast. Differentiation 2002;70:537-46.
50. Freed-Pastor WA, Mizuno H, Zhao X, Langerod A, Moon SH, Rodriguez-Barrueco R, et al. Mutant p53 disrupts mammary tissue architecture via the mevalonate pathway. Cell 2012;148:244-58.