Overexpression of TPL2 may be a predictor of good prognosis in patients with breast invasive ductal carcinoma.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
13 10 2023
13 10 2023
Historique:
received:
07
05
2023
accepted:
11
10
2023
medline:
23
10
2023
pubmed:
14
10
2023
entrez:
13
10
2023
Statut:
epublish
Résumé
The objective of this study was to investigate the clinical significance and roles of tumor progression locus 2 (TPL2) and peptidyl-prolyl cis-trans isomerase 1 (Pin1) in the occurrence and development of breast invasive ductal carcinoma (IDC). Immunohistochemistry was used to detect the expression of TPL2 and Pin1 in human breast tissues, which included normal breast tissues (Normal), tissues with fibrocystic changes (FCC), ductal carcinoma in situ (DCIS), and IDC. The roles of TPL2 and Pin1 in the occurrence and development of IDC, as well as the correlation between their expression levels and clinicopathological parameters, were analyzed. Compared with Normal and FCC groups, the overexpression of TPL2 and Pin1 was significantly increased in DCIS and IDC groups (DCIS vs Normal: P = 0.002/P < 0.001; IDC vs Normal: P = 0.007/P = 0.003; DCIS vs. FCC: P = 0.008/P = 0.004; IDC vs. FCC: P = 0.04/P = 0.043). The expression levels of TPL2 and Pin1 were positively correlated in DCIS and IDC groups (P = 0.001, P = 0.011). In the IDC group, the Ki67 level in the TPL2 overexpression group was significantly lower than that in the TPL2 low expression group (P = 0.02). The TPL2 overexpression rate was significantly higher in IDC with histological grades 1-2 than that in IDC with histological grade 3 (P = 0.029). The TPL2 overexpression rate in IDC with tumor-node-metastasis (TNM) stage I was significantly higher than that in IDC with TNM stages II-III (P = 0.035). We conclude that TPL2 and Pin1 may synergistically promote the occurrence and development of IDC, but TPL2 overexpression may be an early molecular event in IDC development. TPL2 overexpression is significantly related with IDC with lower malignancy or earlier TNM stage, suggesting that the prognosis of IDC patients with TPL2 overexpression may be better and TPL2 overexpression may be a predictor of good prognosis in IDC.
Identifiants
pubmed: 37833434
doi: 10.1038/s41598-023-44660-z
pii: 10.1038/s41598-023-44660-z
pmc: PMC10576082
doi:
Substances chimiques
MAP3K8 protein, human
EC 2.7.11.25
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
17346Informations de copyright
© 2023. Springer Nature Limited.
Références
Nagini, S. Breast cancer: Current molecular therapeutic targets and new players. Anticancer Agents Med. Chem. 17, 152–163 (2017).
doi: 10.2174/1871520616666160502122724
pubmed: 27137076
Rojas, K. & Stuckey, A. Breast cancer epidemiology and risk factors. Clin. Obstet. Gynecol. 59, 651–672 (2016).
doi: 10.1097/GRF.0000000000000239
pubmed: 27681694
Vougioukalaki, M., Kanellis, D. C., Gkouskou, K. & Eliopoulos, A. G. Tpl2 kinase signal transduction in inflammation and cancer. Cancer Lett. 304, 80–89 (2011).
doi: 10.1016/j.canlet.2011.02.004
pubmed: 21377269
Jeong, J. H. et al. TPL2/COT/MAP3K8 (TPL2) activation promotes androgen depletion-independent (ADI) prostate cancer growth. PLoS ONE 6, e16205 (2011).
doi: 10.1371/journal.pone.0016205
pubmed: 21267413
pmcid: 3022761
Decicco-Skinner, K. L., Trovato, E. L., Simmons, J. K., Lepage, P. K. & Wiest, J. S. Loss of tumor progression locus 2 (tpl2) enhances tumorigenesis and inflammation in two-stage skin carcinogenesis. Oncogene. 30, 389–397 (2011).
doi: 10.1038/onc.2010.447
pubmed: 20935675
Pyo, J. S., Park, M. J. & Kim, C. N. TPL2 expression is correlated with distant metastasis and poor prognosis in colorectal cancer. Hum. Pathol. 79, 50–56 (2018).
doi: 10.1016/j.humpath.2018.05.003
pubmed: 29763718
Sourvinos, G., Tsatsanis, C. & Spandidos, D. A. Overexpression of the Tpl-2/Cot oncogene in human breast cancer. Oncogene. 18, 4968–4973 (1999).
doi: 10.1038/sj.onc.1202891
pubmed: 10490831
Kim, G. et al. COT phosphorylates prolyl-isomerase PIN1 to promote tumorigenesis in breast cancer. Mol. Carcinog. 54, 440–448 (2015).
doi: 10.1002/mc.22112
pubmed: 24265246
Yaffe, M. B. et al. Sequence-specific and phosphorylation-dependent proline isomerization: A potential mitotic regulatory mechanism. Science 278, 1957–1960 (1997).
doi: 10.1126/science.278.5345.1957
pubmed: 9395400
Pu, W., Zheng, Y. & Peng, Y. Prolyl isomerase Pin1 in human cancer: Function, mechanism, and significance. Front. Cell Dev. Biol. 8, 168 (2020).
doi: 10.3389/fcell.2020.00168
pubmed: 32296699
pmcid: 7136398
Wulf, G. M. et al. Pin1 is overexpressed in breast cancer and cooperates with Ras signaling in increasing the transcriptional activity of c-Jun towards cyclin D1. EMBO J. 20, 3459–3472 (2001).
doi: 10.1093/emboj/20.13.3459
pubmed: 11432833
pmcid: 125530
Rustighi, A. et al. PIN1 in breast development and cancer: A clinical perspective. Cell Death Differ. 24, 200–211 (2017).
doi: 10.1038/cdd.2016.122
pubmed: 27834957
Saeidi, S., Joo, S., Kim, S. J., Sri Venkata Jagadeesh, A. & Surh, Y. J. Interaction between Peptidyl-prolyl Cis-trans Isomerase NIMA-interacting 1 and GTP-H-Ras: implications for aggressiveness of human mammary epithelial cells and drug resistance. J. Cancer Prev. 25, 234–243 (2020).
doi: 10.15430/JCP.2020.25.4.234
pubmed: 33409256
pmcid: 7783236
Kim, K. et al. Interleukin-22 promotes epithelial cell transformation and breast tumorigenesis via MAP3K8 activation. Carcinogenesis 35, 1352–1361 (2014).
doi: 10.1093/carcin/bgu044
pubmed: 24517997
Allison, K. H. et al. WHO classification of tumors of the breast, 5th Ed. Lyon: International Agency for Research on Cancer, (2019).
Chen, J. H., Nalcioglu, O. & Su, M. Y. Fibrocystic change of the breast presenting as a focal lesion mimicking breast cancer in MR imaging. J. Magn. Reson. Imaging. 28, 1499–1505 (2008).
doi: 10.1002/jmri.21455
pubmed: 19025938
pmcid: 2597344
Soysal, S. D. et al. Genetic alterations in benign breast biopsies of subsequent breast cancer patients. Front. Med. (Lausanne). 6, 166 (2019).
doi: 10.3389/fmed.2019.00166
pubmed: 31396514
pmcid: 6667637
Allison, K. H. et al. Estrogen and progesterone receptor testing in breast cancer: ASCO/CAP guideline update. J. Clin. Oncol. 38, 1346–1366 (2020).
doi: 10.1200/JCO.19.02309
pubmed: 31928404
Gandhi, H. et al. Correlation of Robinson’s cytological grading with Elston and Ellis’ Nottingham modification of bloom Richardson score of histopathology for breast carcinoma. Maedica (Bucur). 18, 55–60 (2023).
pubmed: 37266482
pmcid: 10231175
Amin, M. B. et al. (eds) AJCC Cancer Staging Manual 8th edn. (Springer, 2017).
Patriotis, C., Makris, A., Chernoff, J. & Tsichlis, P. N. Tpl-2 acts in concert with Ras and Raf-1 to activate mitogen-activated protein kinase. Proc. Natl. Acad. Sci. U.S.A. 91, 9755–9759 (1994).
doi: 10.1073/pnas.91.21.9755
pubmed: 7937886
pmcid: 44895
Lee, H. W., Choi, H. Y., Joo, K. M. & Nam, D. H. Tumor progression locus 2 (Tpl2) kinase as a novel therapeutic target for cancer: Double-sided effects of Tpl2 on cancer. Int. J. Mol. Sci. 16, 4471–4491 (2015).
doi: 10.3390/ijms16034471
pubmed: 25723737
pmcid: 4394431
Njunge, L. W., Estania, A. P., Guo, Y., Liu, W. & Yang, L. Tumor progression locus 2 (TPL2) in tumor-promoting inflammation, tumorigenesis and tumor immunity. Theranostics 10, 8343–8364 (2020).
doi: 10.7150/thno.45848
pubmed: 32724474
pmcid: 7381748
Khanal, P., Yeung, B., Zhao, Y. & Yang, X. Identification of Prolyl isomerase Pin1 as a novel positive regulator of YAP/TAZ in breast cancer cells. Sci. Rep. 9, 6394 (2019).
doi: 10.1038/s41598-019-42767-w
pubmed: 31015482
pmcid: 6478839
Habor, V., Habor, A., Copotoiu, C. & Panţîru, A. Relaţia mastopatie fibrochistică–cancer mamar [Fibrocystic breast disease–breast cancer sequence]. Chirurgia (Bucur). 105, 191–194 (2010).
pubmed: 20540231
Røge, R., Nielsen, S., Riber-Hansen, R. & Vyberg, M. Ki-67 proliferation index in breast cancer as a function of assessment method: A NordiQC experience. Appl. Immunohistochem. Mol. Morphol. 29, 99–104 (2021).
doi: 10.1097/PAI.0000000000000846
pubmed: 32168036
Nielsen, T. O. et al. Assessment of Ki67 in breast cancer: updated recommendations from the international Ki67 in breast cancer working group. J. Natl. Cancer Inst. 113, 808–819 (2021).
doi: 10.1093/jnci/djaa201
pubmed: 33369635
Hammond, M. E. et al. American Society of Clinical Oncology/College of American pathologists guideline recommendations for immunohistochemical testing of estrogen and progesterone receptors in breast cancer. J. Clin. Oncol. Off. J. Am. Soc. Clin. Oncol. 28, 2784–2795 (2010).
doi: 10.1200/JCO.2009.25.6529
Zhang, M., Yan, M., Lv, H., Niu, L. & Zeng, H. Clinical study of first-line endocrine therapy for type ER+/PR+ and ER+/PR- advanced breast cancer. Ann. Palliat. Med. 10, 238–243 (2021).
doi: 10.21037/apm-20-2180
pubmed: 33545761
Rajbhandari, P. et al. Pin1 modulates ERα levels in breast cancer through inhibition of phosphorylation-dependent ubiquitination and degradation. Oncogene 33, 1438–1447 (2014).
doi: 10.1038/onc.2013.78
pubmed: 23542176