Combined A20 and tripartite motif-containing 44 as poor prognostic factors for breast cancer patients of the Japanese population.

Publisher: Published by Blackwell Scientific Publications for the Japanese Society of Pathology Country of Publication: Australia NLM ID: 9431380 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1440-1827 (Electronic) Linking ISSN: 13205463 NLM ISO Abbreviation: Pathol Int Subsets: MEDLINE

Original Publication: Carlton South, Vic., Australia : Published by Blackwell Scientific Publications for the Japanese Society of Pathology, c1994-

Breast Neoplasms*/metabolism ; Breast Neoplasms*/pathology ; Intracellular Signaling Peptides and Proteins*/analysis ; Prognosis* ; Tripartite Motif Proteins*/analysis ; Tumor Necrosis Factor alpha-Induced Protein 3*/analysis; Biomarkers, Tumor/analysis ; Female ; Humans ; Immunohistochemistry ; Japan

We previously reported that a strong immunoreactivity of tripartite motif-containing 44 (TRIM44) predicts the poor prognosis of patients with invasive breast cancer, and proposed that TRIM44 activates nuclear factor-κB (NF-κB) signaling as a causative mechanism. In the present study, we examined the clinicopathological roles of A20, which is known to be an NF-κB responsive gene, with TRIM44, in an updated cohort. Tissue samples of invasive breast cancer were obtained from 140 Japanese female breast cancer patients who underwent surgical treatment. Immunoreactivities of A20 and TRIM44 were analyzed using specific antibodies for each protein. A positive A20 immunoreactivity was significantly associated with a shorter disease-free survival (P = 0.043) and was positively correlated with TRIM44 immunoreactivity (P = 0.039). Combined use of the immunoreactivities for two proteins revealed that double-positive status for both A20 and TRIM44 immunoreactivities was associated with a shorter disease-free survival (P = 0.012) and was an independent factor for poor prognosis. These results indicate that a combined A20 and TRIM44 immunoreactivity predicted the prognosis of patients with invasive breast cancer. Moreover, the positive correlation between A20 and TRIM44 immunoreactivities suggested that the activation of NF-κB signaling by TRIM44 could occur in clinical breast cancer tissues.
(© 2020 Japanese Society of Pathology and John Wiley & Sons Australia, Ltd.)

Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 2018; 68: 394-424.
Ullah MF. Breast cancer: Current perspectives on the disease status. Adv Exp Med Biol 2019; 1152: 51-64.
National comprehensive cancer network (NCCN) guideline for treatment of breast cancerAvailable from: https://www.nccn.org/professionals/physician_gls/default.aspx#site. (Accessed September 21 2020.).
Kawabata H, Azuma K, Ikeda K et al. TRIM44 is a poor prognostic factor for breast cancer patients as a modulator of NF-κB signaling. Int J Mol Sci 2017; 18, 1931.
Hatakeyama S. TRIM proteins and cancer. Nat Rev Cancer 2011; 11: 792-804.
Urano T, Usui T, Takeda S et al. TRIM44 interacts with and stabilizes terf, a TRIM ubiquitin E3 ligase. Biochem Biophys Res Commun 2009; 383: 263-68.
Coornaert B, Carpentier I, Beyaert R. A20: Central gatekeeper in inflammation and immunity. J Biol Chem 2009; 284: 8217-21.
Dixit VM, Green S, Sarma V et al. Tumor necrosis factor-alpha induction of novel gene products in human endothelial cells including a macrophage-specific chemotaxin. J Biol Chem 1990; 265: 2973-78.
Wertz IE, O'Rourke KM, Zhou H et al. De-ubiquitination and ubiquitin ligase domains of A20 downregulate NF-kappaB signalling. Nature 2004; 430: 694-99.
Hitotsumatsu O, Ahmad RC, Tavares R et al. The ubiquitin-editing enzyme A20 restricts nucleotide-binding oligomerization domain containing 2-triggered signals. Immunity 2008; 28: 381-90.
Mauro C, Pacifico F, Lavorgna A et al. ABIN-1 binds to NEMO/IKKgamma and co-operates with A20 in inhibiting NF-kappaB. J Biol Chem 2006; 281: 18482-88.
Boone DL, Turer EE, Lee EG et al. The ubiquitin-modifying enzyme A20 is required for termination of Toll-like receptor responses. Nat Immunol 2004; 5: 1052-60.
Lee EG, Boone DL, Chai S et al. Failure to regulate TNF-induced NF- kappaB and cell death responses in A20-deficient mice. Science 2000; 289: 2350-54.
Hjelmeland AB, Wu Q, Wickman S et al. Targeting A20 decreases glioma stem cell survival and tumor growth. PLoS Biol 2010; 8: e1000319.
Hadisaputri YE, Miyazaki T, Yokobori T et al. TNFAIP3 overexpression is an independent factor for poor survival in esophageal squamous cell carcinoma. Int J Oncol 2017; 50: 1002-10.
Wang Y, Wan M, Zhou Q et al. The prognostic role of SOCS3 and A20 in human cholangiocarcinoma. PLoS One 2015; 10: e0141165.
Yoon CI, Ahn SG, Bae SJ et al. High A20 expression negatively impacts survival in patient with breast cancer. PLoS One 2019; 14: e0221721.
Ujihira T, Ikeda K, Suzuki T et al. MicroRNA-574-3p, identified by microRNA library-based functional screening, modulates tamoxifen response in breast cancer. Sci Rep 2015; 5: 7641.
Yamada Y, Takayama K, Fujimura T et al. A novel prognostic factor TRIM44 promotes cell proliferation and migration, and inhibits apoptosis in testicular germ cell tumor. Cancer Sci 2017; 108: 32-41.
Azuma K, Horie K, Inoue S, Ouchi Y, Sakai R. Analysis of estrogen receptor alpha signaling complex at the plasma membrane. FEBS Lett 2004; 577: 339-44.
The Japanese Breast Cancer Society. General Rules for Clinical and Pathological Recording of Breast Cancer, 17th edn. Tokyo: Kanehara, 2012; (in Japanese).
Sakamoto G, Inaji H, Akiyama F et al. General rules for clinical and pathological recording of breast cancer 2005. Breast Cancer 2005; 12: S1-27.
Lakhani S, Ellis I, Schnitt S et al. WHO Classification of Tumours of the Breast, 4th edn. Lyon: IARC Press, 2012.
Sobin LH, Gospodarowicz MK, Wittekind C. TNM Classification of Malignant Tumors, 7th edn. Oxford: Wiley-Blackwell, 2010.
Hammond MEH, Hayes DF, Dowsett M et al. Pathologists guideline recommendations for immunohistochemical testing of estrogen and progesterone receptors in breast cancer. J Clin Oncol 2010; 28: 2784-95.
Wolff AC, Hammond MEH, Hicks DG et al. Recommendations for human epidermal growth factor receptor 2 testing in breast cancer: American Society of Clinical Oncology/College of American Pathologists clinical practice guideline update. J Clin Oncol 2013; 31: 3997-4013.
Kanda Y. Investigation of the freely available easy-to-use software ‘EZR’ for medical statistics. Bone Marrow Transplant 2013; 48: 452-58.
Peng R, Zhang PF, Zhang C et al. Elevated TRIM44 promotes intrahepatic cholangiocarcinoma progression by inducing cell EMT via MAPK signaling. Cancer Med 2018; 7: 796-808.
Li P, Yin H, Meng F, Liu S, Liu H, Ma R. High TRIM44 expression in endometrial carcinoma is associated with a poorer patient outcome. Pathol Res Pract 2018; 214: 727-31.
Wang H, Fang ZL, Zhang GH, Ma X. TRIM44, a crucial target of miR-410, functions as a potential oncogene in osteosarcoma. Onco Targets Ther 2018; 11: 3637-47.
Liu S, Yin H, Ji H, Zhu J, Ma R. Overexpression of TRIM44 is an independent marker for predicting poor prognosis in epithelial ovarian cancer. Exp Ther Med 2018; 16: 3034-40.
Liu S, Meng F, Ding J et al. High TRIM44 expression as a valuable biomarker for diagnosis and prognosis in cervical cancer. Biosci Rep 2019; 39: BSR20181639.
Wei CY, Wang L, Zhu MX et al. TRIM44 activates the AKT/mTOR signal pathway to induce melanoma progression by stabilizing TLR4. J Exp Clin Cancer Res 2019; 38: 137.
Yamada Y, Kimura N, Takayama K et al. TRIM44 promotes cell proliferation and migration by inhibiting FRK in renal cell carcinoma. Cancer Sci 2020; 111: 881-90.
Xing Y, Meng Q, Chen X et al. TRIM44 promotes proliferation and metastasis in non-small cell lung cancer via mTOR signaling pathway. Oncotarget 2016; 7: 30479-91.
Zhu X, Wu Y, Miao X et al. High expression of TRIM44 is associated with enhanced cell proliferation, migration, invasion, and resistance to doxorubicin in hepatocellular carcinoma. Tumour Biol 2016; 37: 14615-28.
Luo Q, Lin H, Ye X, Huang J, Lu S, Xu L. Trim44 facilitates the migration and invasion of human lung cancer cells via the NF-κB signaling pathway. Int J Clin Oncol 2015; 20: 508-17.
Zhou Y, Eppenberger-Castori S, Marx C et al. Activation of nuclear factor-kappaB (NFkappaB) identifies a high-risk subset of hormone-dependent breast cancers. Int J Biochem Cell Biol 2005; 37: 1130-44.
Frasor J, Weaver A, Pradhan M et al. Positive cross-talk between estrogen receptor and NF-kappaB in breast cancer. Cancer Res 2009; 69: 8918-25.
Franco HL, Nagari A, Kraus WL. TNFα signaling exposes latent estrogen receptor binding sites to alter the breast cancer cell transcriptome. Mol Cell 2015; 58: 21-34.
Yamamoto M, Taguchi Y, Ito-Kureha T, Semba K, Yamaguchi N, Inoue J. NF-κB non-cell-autonomously regulates cancer stem cell populations in the basal-like breast cancer subtype. Nat Commun 2013; 4: 2299.
Visvader JE, Lindeman GJ. Cancer stem cells in solid tumours: Accumulating evidence and unresolved questions. Nat Rev Cancer 2008; 8: 755-68.
Lim SO, Li CW, Xia W et al. Deubiquitination and stabilization of PD-L1 by CSN5. Cancer Cell 2016; 30: 925-39.
Honma K, Tsuzuki S, Nakagawa M et al. TNFAIP3/A20 functions as a novel tumor suppressor gene in several subtypes of non-Hodgkin lymphomas. Blood 2009; 114: 2467-75.
Chanudet E, Ye H, Ferry J et al. A20 deletion is associated with copy number gain at the TNFA/B/C locus and occurs preferentially in translocation-negative MALT lymphoma of the ocular adnexa and salivary glands. J Pathol 2009; 217: 420-30.
Wang S, Wen F, Wiley GB, Kinter MT, Gaffney PM. An enhancer element harboring variants associated with systemic lupus erythematosus engages the TNFAIP3 promoter to influence A20 expression. PLoS Genet 2013; 9: e1003750.
Altonsy MO, Sasse SK, Phang TL, Gerber AN. Context-dependent cooperation between nuclear factor κB (NF-κB) and the glucocorticoid receptor at a TNFAIP3 intronic enhancer: A mechanism to maintain negative feedback control of inflammation. J Biol Chem 2014; 289: 8231-39.
Lee JH, Jung SM, Yang KM et al. A20 promotes metastasis of aggressive basal-like breast cancers through multi-monoubiquitylation of Snail1. Nat Cell Biol 2017; 19: 1260-73.
Vendrell JA, Ghayad S, Ben-Larbi S, Dumontet C, Mechti N, Cohen PA. A20/TNFAIP3, a new estrogen-regulated gene that confers tamoxifen resistance in breast cancer cells. Oncogene 2007; 26: 4656-67.
Lee E, Ouzounova M, Piranlioglu R et al. The pleiotropic effects of TNFα in breast cancer subtypes is regulated by TNFAIP3/A20. Oncogene 2019; 38: 469-82.

Okinaka Memorial Institute for Medical Research; Takeda Science Foundation; 17K10571 Japan Society for the Promotion of Science; 20K08954 Japan Society for the Promotion of Science

Keywords: TNFα-induced protein 3; breast cancer; immunoreactivity; nuclear factor kappa-B signaling; tripartite motif-containing 44

0 (Biomarkers, Tumor)
0 (Intracellular Signaling Peptides and Proteins)
0 (TRIM44 protein, human)
0 (Tripartite Motif Proteins)
EC 3.4.19.12 (Tumor Necrosis Factor alpha-Induced Protein 3)

Date Created: 20201107 Date Completed: 20211014 Latest Revision: 20211014

20231215

10.1111/pin.13047

33159706