TRPS1: a highly sensitive and specific marker for breast carcinoma, especially for triple-negative breast cancer.
Journal
Modern pathology : an official journal of the United States and Canadian Academy of Pathology, Inc
ISSN: 1530-0285
Titre abrégé: Mod Pathol
Pays: United States
ID NLM: 8806605
Informations de publication
Date de publication:
04 2021
04 2021
Historique:
received:
06
08
2020
accepted:
22
09
2020
revised:
15
09
2020
pubmed:
5
10
2020
medline:
19
11
2021
entrez:
4
10
2020
Statut:
ppublish
Résumé
Currently there is no highly specific and sensitive marker to identify breast cancer-the most common malignancy in women. Breast cancer can be categorized as estrogen receptor (ER)/progesterone receptor (PR)-positive luminal, human epidermal growth factor receptor 2 (HER2)-positive, or triple-negative breast cancer (TNBC) types based on the expression of ER, PR, and HER2. Although GATA3 is the most widely used tumor marker at present to determine the breast origin, which has been shown to be an excellent marker for ER-positive and low-grade breast cancer, but it does not work well for TNBC with sensitivity as low as <20% in metaplastic breast carcinoma. In the current study, through TCGA data mining we identified trichorhinophalangeal syndrome type 1 (TRPS1) as a specific gene for breast carcinoma across 31 solid tumor types. Moreover, high mRNA level of TRPS1 was found in all four subtypes of breast carcinoma including ER/PR-positive luminal A and B types, HER2-positive type, and basal-type/TNBC. We then analyzed TRPS1 expression in 479 cases of various types of breast cancer using immunochemistry staining, and found that TRPS1 and GATA3 had comparable positive expression in ER-positive (98% vs. 95%) and HER2-positive (87% vs. 88%) breast carcinomas. However, TRPS1 which was highly expressed in TNBC, was significantly higher than GATA3 expression in metaplastic (86% vs. 21%) and nonmetaplastic (86% vs. 51%) TNBC. In addition, TRPS1 expression was evaluated in 1234 cases of solid tumor from different organs. In contrast to the high expression of GATA3 in urothelial carcinoma, TRPS1 showed no or little expression in urothelial carcinomas or in other tumor types including lung adenocarcinoma, pancreatic adenocarcinoma, colon and gastric adenocarcinoma, renal cell carcinoma, melanoma, and ovarian carcinoma. These findings suggest that TRPS1 is a highly sensitive and specific marker for breast carcinoma and can be used as a great diagnostic tool, especially for TNBC.
Identifiants
pubmed: 33011748
doi: 10.1038/s41379-020-00692-8
pii: S0893-3952(22)00639-1
doi:
Substances chimiques
Biomarkers, Tumor
0
GATA3 Transcription Factor
0
GATA3 protein, human
0
Repressor Proteins
0
TRPS1 protein, human
0
Types de publication
Comparative Study
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
710-719Subventions
Organisme : NCI NIH HHS
ID : P30 CA016672
Pays : United States
Références
Redig AJ, McAllister SS. Breast cancer as a systemic disease: a view of metastasis. J Intern Med. 2013;274:113–26.
doi: 10.1111/joim.12084
Siegel RL, Miller KD, Jemal A. Cancer statistics, 2020. CA Cancer J Clin. 2020;70:7–30.
Cancer Genome Atlas N. Comprehensive molecular portraits of human breast tumours. Nature. 2012;490:61–70.
doi: 10.1038/nature11412
Goldhirsch A, Winer EP, Coates AS, Gelber RD, Piccart-Gebhart M, Thurlimann B, et al. Personalizing the treatment of women with early breast cancer: highlights of the St Gallen International Expert Consensus on the Primary Therapy of Early Breast Cancer 2013. Ann Oncol. 2013;24:2206–23.
doi: 10.1093/annonc/mdt303
Perou CM, Sorlie T, Eisen MB, van de Rijn M, Jeffrey SS, Rees CA, et al. Molecular portraits of human breast tumours. Nature. 2000;406:747–52.
doi: 10.1038/35021093
Foulkes WD, Smith IE, Reis-Filho JS. Triple-negative breast cancer. N. Engl J Med. 2010;363:1938–48.
doi: 10.1056/NEJMra1001389
Cimino-Mathews A, Subhawong AP, Illei PB, Sharma R, Halushka MK, Vang R, et al. GATA3 expression in breast carcinoma: utility in triple-negative, sarcomatoid, and metastatic carcinomas. Hum Pathol. 2013;44:1341–9.
doi: 10.1016/j.humpath.2012.11.003
Gown AM, Fulton RS, Kandalaft PL. Markers of metastatic carcinoma of breast origin. Histopathology. 2016;68:86–95.
doi: 10.1111/his.12877
Huo L, Gong Y, Guo M, Gilcrease MZ, Wu Y, Zhang H, et al. GATA-binding protein 3 enhances the utility of gross cystic disease fluid protein-15 and mammaglobin A in triple-negative breast cancer by immunohistochemistry. Histopathology. 2015;67:245–54.
doi: 10.1111/his.12645
Kandalaft PL, Simon RA, Isacson C, Gown AM. Comparative sensitivities and specificities of antibodies to breast markers GCDFP-15, mammaglobin A, and different clones of antibodies to GATA-3: a study of 338 tumors using whole sections. Appl Immunohistochem Mol Morphol. 2016;24:609–14.
doi: 10.1097/PAI.0000000000000237
Miettinen M, McCue PA, Sarlomo-Rikala M, Rys J, Czapiewski P, Wazny K, et al. GATA3: a multispecific but potentially useful marker in surgical pathology: a systematic analysis of 2500 epithelial and nonepithelial tumors. Am J Surg Pathol. 2014;38:13–22.
doi: 10.1097/PAS.0b013e3182a0218f
Wendroth SM, Mentrikoski MJ, Wick MR. GATA3 expression in morphologic subtypes of breast carcinoma: a comparison with gross cystic disease fluid protein 15 and mammaglobin. Ann Diagn Pathol. 2015;19:6–9.
doi: 10.1016/j.anndiagpath.2014.12.001
Allison KH, Hammond MEH, Dowsett M, McKernin SE, Carey LA, Fitzgibbons PL, et al. Estrogen and progesterone receptor testing in breast cancer: American society of clinical oncology/college of American pathologists guideline update. Arch Pathol Lab Med. 2020;144:545–63.
doi: 10.5858/arpa.2019-0904-SA
Wolff AC, Hammond MEH, Allison KH, Harvey BE, Mangu PB, Bartlett JMS, et al. Human epidermal growth factor receptor 2 testing in breast cancer: American society of clinical oncology/college of American pathologists clinical practice guideline focused update. Arch Pathol Lab Med. 2018;142:1364–82.
doi: 10.5858/arpa.2018-0902-SA
Hoch RV, Thompson DA, Baker RJ, Weigel RJ. GATA-3 is expressed in association with estrogen receptor in breast cancer. Int J Cancer. 1999;84:122–8.
doi: 10.1002/(SICI)1097-0215(19990420)84:2<122::AID-IJC5>3.0.CO;2-S
Patient RK, McGhee JD. The GATA family (vertebrates and invertebrates). Curr Opin Genet Dev. 2002;12:416–22.
doi: 10.1016/S0959-437X(02)00319-2
Kouros-Mehr H, Slorach EM, Sternlicht MD, Werb Z. GATA-3 maintains the differentiation of the luminal cell fate in the mammary gland. Cell. 2006;127:1041–55.
doi: 10.1016/j.cell.2006.09.048
Asselin-Labat ML, Sutherland KD, Barker H, Thomas R, Shackleton M, Forrest NC, et al. Gata-3 is an essential regulator of mammary-gland morphogenesis and luminal-cell differentiation. Nat Cell Biol. 2007;9:201–9.
doi: 10.1038/ncb1530
Kouros-Mehr H, Kim JW, Bechis SK, Werb Z. GATA-3 and the regulation of the mammary luminal cell fate. Curr Opin Cell Biol. 2008;20:164–70.
doi: 10.1016/j.ceb.2008.02.003
Wuelling M, Kaiser FJ, Buelens LA, Braunholz D, Shivdasani RA, Depping R, et al. Trps1, a regulator of chondrocyte proliferation and differentiation, interacts with the activator form of Gli3. Dev Biol. 2009;328:40–53.
doi: 10.1016/j.ydbio.2009.01.012
Izumi K, Takagi M, Parikh AS, Hahn A, Miskovsky SN, Nishimura G, et al. Late manifestations of tricho-rhino-pharangeal syndrome in a patient: expanded skeletal phenotype in adulthood. Am J Med Genet A. 2010;152A:2115–9.
doi: 10.1002/ajmg.a.33511
Ito T, Shimomura Y, Farooq M, Suzuki N, Sakabe J, Tokura Y. Trichorhinophalangeal syndrome with low expression of TRPS1 on epidermal and hair follicle epithelial cells. J Dermatol. 2013;40:396–8.
doi: 10.1111/1346-8138.12111
Witwicki RM, Ekram MB, Qiu X, Janiszewska M, Shu S, Kwon M, et al. TRPS1 is a lineage-specific transcriptional dependency in breast cancer. Cell Rep. 2018;25:1255–67.
doi: 10.1016/j.celrep.2018.10.023
Cornelissen LM, Drenth AP, van der Burg E, de Bruijn R, Pritchard CEJ, Huijbers IJ, et al. TRPS1 acts as a context-dependent regulator of mammary epithelial cell growth/differentiation and breast cancer development. Genes Dev. 2020;34:179–93.
doi: 10.1101/gad.331371.119
Radvanyi L, Singh-Sandhu D, Gallichan S, Lovitt C, Pedyczak A, Mallo G, et al. The gene associated with trichorhinophalangeal syndrome in humans is overexpressed in breast cancer. Proc Natl Acad Sci USA. 2005;102:11005–10.
doi: 10.1073/pnas.0500904102
Chen JQ, Litton J, Xiao L, Zhang HZ, Warneke CL, Wu Y, et al. Quantitative immunohistochemical analysis and prognostic significance of TRPS-1, a new GATA transcription factor family member, in breast cancer. Horm. Cancer. 2010;1:21–33.
Chen JQ, Bao Y, Litton J, Xiao L, Zhang HZ, Warneke CL, et al. Expression and relevance of TRPS-1: a new GATA transcription factor in breast cancer. Horm Cancer. 2011;2:132–43.
doi: 10.1007/s12672-011-0067-5
Liang Y, Heitzman J, Kamat AM, Dinney CP, Czerniak B, Guo CC. Differential expression of GATA-3 in urothelial carcinoma variants. Hum Pathol. 2014;45:1466–72.
doi: 10.1016/j.humpath.2014.02.023
Liu H, Shi J, Wilkerson ML, Lin F. Immunohistochemical evaluation of GATA3 expression in tumors and normal tissues: a useful immunomarker for breast and urothelial carcinomas. Am J Clin Pathol. 2012;138:57–64.
doi: 10.1309/AJCP5UAFMSA9ZQBZ
DeLair DF, Corben AD, Catalano JP, Vallejo CE, Brogi E, Tan LK. Non-mammary metastases to the breast and axilla: a study of 85 cases. Mod Pathol. 2013;26:343–9.
doi: 10.1038/modpathol.2012.191
Kilgore MR, Bosch DE, Adamson KH, Swanson PE, Dintzis SM, Rendi MH. Unexpected PAX8 immunoreactivity in metastatic high-grade breast cacner. Appl Immunohistochem Mol Morphol. 2019;27:637–43.
doi: 10.1097/PAI.0000000000000707
Schwartz LE, Begum S, Westra WH, Bishop JA. GATA3 immunohistochemical expression in salivary gland neoplasms. Head Neck Pathol. 2013;7:311–5.
doi: 10.1007/s12105-013-0442-3