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DOI 10.34014/2227-1848-2022-3-49-60

PHENOTYPIC CHARACTERISTICS OF ANDROGEN RECEPTOR-POSITIVE CANCER IN THE TRIPLE-NEGATIVE BREAST CANCER GROUP

I.S. Panchenko1, V.V. Rodionov2, S.V. Panchenko1, M.G. Sharafutdinov1

1 Ulyanovsk State University, Ulyanovsk, Russia;

2 National Medical Research Center for Obstetrics, Gynecology and Perinatology named after academician V.I. Kulakov, Ministry of Health of the Russian Federation, Moscow, Russia

 

The aim of the paper is to reveal the phenotypic characteristics of androgen-receptor-positive breast cancer in triple-negative breast cancer.

Materials and Methods. The authors analyzed clinical and morphological tumour data in 253 patients with morphologically verified invasive triple-negative breast cancer (TNBC). The patients were treated at the Regional Clinical Oncologic Dispensary (Ulyanovsk) and the Breast Pathology Department of the National Medical Research Center for Obstetrics, Gynecology and Perinatology named after V.I. Kulakov (Moscow) from 2014 to 2021.

Results. Statistical analysis of 45 patients (18 % of the total sample) showed that androgen receptor (AR) expression in TNBC was observed in patients older than 61 years (p=0.054). It was associated with a more common stage of the disease (starting with IIB) (p=0.004), multifocal growth pattern (p=0.025), invasive lobular cancer (p=0.04), higher tumor differentiation (p<0.0001), low Ki67 level (p=0.000001), and more frequent involvement of regional lymph nodes (p=0.005). At the same time, there were no statistically significant correlations between the AR expression and menstrual function, breast lesion quadrant, and pathomorphological response after neoadjuvant polychemotherapy.

Conclusion. AR expression in TNBC occurs in patients over 61 years of age, with a locally advanced disease stage, a multifocal tumor growth pattern, an invasive lobular cancer, and well-differentiated tumors with low proliferative activity.

Key words: breast cancer, triple-negative breast cancer (TNBC), androgen receptors (AR).

 

References

  1. Katrina R. Bauer, Monica Brown, Rosemary D. Cress, Carol A. Parise, Vincent Caggiano. Descriptive analysis of estrogen receptor (ER)-negative, progesterone receptor (PR)-negative, and HER2-negative invasive breast cancer, the so-called triple-negative phenotype: a population-based study from the California Cancer Registry. Cancer. 2007; 109 (9): 1721–1728. Available at: https://pubmed.ncbi.nlm.nih.gov/17387718 (accessed: April 07, 2021). DOI: 10.1002/cncr.22618.

  2. Rebecca Dent, Maureen Trudeau, Kathleen I. Pritchard, Wedad M. Hanna, Harriet K. Kahn, Carol A. Sawka, Lavina A. Lickley, Ellen Rawlinson, Ping Sun, Steven A. Narod. Triple-negative breast cancer: clinical features and patterns of recurrence. Clin. Cancer Res. 2007; 13 (15, Pt. 1): 4429–4434. Available at: https://pubmed.ncbi.nlm.hih.gov/17671126 (accessed: April 07, 2021). DOI: 10.1158/1078-0432.CCR-06-3045.

  3. Maryam Nakhjavani, Jennifer E Hardingham, Helen M. Palethorpe, Tim J. Price, Amanda R. Townsend. Druggable Molecular Targets for the Treatment of Triple Negative Breast Cancer. J. Breast Cancer. 2019; 22 (3): 341–361. Available at: https://pubmed.ncbi.nlm.nih.gov/31598336 (accessed: April 07, 2021). DOI: 10.4048/jbc.2019.22.e39.

  4. Alis R. T. Bergin, Sherene Loi. Triple-negative breast cancer: recent treatment advances. F1000Res. 2019; 8: F1000 Faculty Rev-1342. Available at: https:// pubmed.ncbi.nlm.nih.gov/31448088 (accessed: April 16, 2021). DOI: 10.12688/f1000research.18888.1.

  5. Brain D. Lehmann, Bojana Jovanovic, Xi Chen, Monica V. Estrada, Kimberly N. Johnson, Yu Shyr, Harold L. Moses, Melinda E. Sanders, Jennifer A. Pietenpol. Refinement of Triple-Negative Breast Cancer Molecular Subtypes: Implications for Neoadjuvant Chemotherapy Selection. PLoS One. 2016; 11 (6): e0157368. Available at: https://pubmed.ncbi.nlm.nih.gov/27310713 (accessed: April 07, 2021). DOI: 10.1371/journal.pone.0157368.

  6. Jesse Lopes da Silva, Natalia Cristina Cardoso Nunes, Patricia Izetti, Guilherme Gomes de Mesquita, Andrea Cristina de Melo. Triple negative breast cancer: A thorough review of biomarkers. Crit Rev Oncol Hematol. 2020; 145: 102855. Available at: https:// pubmed.ncbi.nlm.nih.gov/31927455 (accessed: April 07, 2021). DOI: 10.1016/j.critrevonc.2019.102855.

  7. Sewha Kim, Byung-In Moon, Woosung Lim, Sanghui Park, Min Sun Cho, Sun Hee Sung. Feasibility of classification of triple negative breast cancer by immunohistochemical surrogate markers. Clin Breast Cancer. 2018; 18 (5): e1123–e1132. Available at: https:// pubmed.ncbi.nlm.nih.gov/29754847 (accessed: April 07, 2021). DOI: 10.1016/j.clbc.2018.03.012.

  8. Ugo Testa, Germana Castelli, Elvira Pelosi. Breast Cancer: A molecularly heterogenous disease needing subtype-specific treatments. Med Sci (Basel). 2020; 8 (1): 18. Available at: https://pubmed.ncbi.nlm.nih.gov/32210163 (accessed: April 07, 2021). DOI: 10.3390/medsci8010018.

  9. Matthew D. Burstein, Anna Tsimelzon, Graham M. Poage, Kyle R. Covington, Alejandro Contreras, Suzanne A.W. Fuqua, Michelle I. Savage, C. Kent Osborne, Susan G. Hilsenbeck, Jenry C. Chang, Gordon B. Mills, Ching C. Lau, Powel H. Brown. Comprehensive genomic analysis identifies novel subtypes and targets of triple-negative breast cancer. Clin Cancer Res. 2015; 21 (7): 1688–1698. Available at: https://pubmed.ncbi.nlm.nih.gov/25208879 (accessed: July 01, 2020). DOI: 10.1158/1078-0432.CCR-14-0432.

  10. Yа‑Xuan Lui, Ke-Jing Zhang, Li‑Li Tang. Clinical significance of androgen receptor expression in triple negative breast cancer‑an immunohistochemistry study. Oncol Lett. 2018; 15 (6): 10008–10016. Available at: https://pubmed.ncbi.nlm.nih.gov/29844843 (accessed: April 07, 2021). DOI: 10.3892/ol.2018.8548.

  11. Murtuza Rampurwala, Kari B. Wisinski, Ruth O'Regan R. Role of the androgen receptor in triple-negative breast cancer. Clin Adv Hematol Oncol. 2016; 14 (3): 186–193. Available at: https://pubmed.ncbi.nlm.nih.gov/27058032 (accessed: March 16, 2021). PMCID: PMC5221599.

  12. Francisco E. Vera-Badillo, Amoud J. Templeton, Paulo de Gouveia, Ivan Diaz-Padilla, Philippe L. Bedard, Mustafa Al-Mubarak, Bostjan Seruga, Ian F. Tannock, Alberto Ocana, Eitan Amir. Androgen receptor expression and outcomes in early breast cancer: a systematic review and meta-analysis. J. Natl Cancer Inst. 2014; 106 (1): 319. Available at: https://pubmed.ncbi.nlm.nih.gov/24273215 (accessed: April 20, 2022). DOI: 10.1093/jnci/djt319.

  13. Kevin H. Kensler, Elizabeth M. Poole, Yujing J. Heng, Laura C. Collins, Benjamin Glass, Andrew H. Beck, Aditi Hazra, Bernard A. Rosner, A. Heather Eliassen, Susan E. Hankinson, Eric P. Winer, Myles Brown, Rulla M. Tamimi. Androgen Receptor Expression and Breast Cancer Survival: Results From the Nurses' Health Studies. J. Natl Cancer Inst. 2019; 111 (7): 700–708. Available at: https://pubmed.ncbi.nlm.nih.gov/30445651 (accessed: April 20, 2022). DOI: 10.1093/jnci/djy173.

  14. Park S., Koo J.S., Kim M.S., Park H.S., Lee J.S., Lee J.S., Kim S.I., Park B.W., Lee K.S. Androgen receptor expression is significantly associated with better outcomes in estrogen receptor-positive breast cancers. Ann Oncol. 2011; 22 (8): 1755–1762. Available at: https://pubmed.ncbi.nlm.nih.gov/21310761 (accessed: April 20, 2022). DOI: 10.1093/annonc/mdq678.

  15. Karin Elebro, Signe Borgquist, Maria Simonsson, Andrea Markkula, Karin Jirström, Christian Ingvar, Carsten Rose, Helena Jernström. Combined Androgen and Estrogen Receptor Status in Breast Cancer: Treatment Prediction and Prognosis in a Population-Based Prospective Cohort. Clin Cancer Res. 2015; 21 (16): 3640–3650. Available at: https://pubmed.ncbi.nlm.nih.gov/25904752 (accessed: April 20, 2022). DOI: 10.1158/1078-0432.CCR-14-2564.

  16. Yoonseok Kim, Eunae Jae, Myunghee Yoon. Influence of Androgen Receptor Expression on the Survival Outcomes in Breast Cancer: A Meta-Analysis. J. Breast Cancer. 2015; 18 (2): 134–142. Available at: https://pubmed.ncbi.nlm.nih.gov/26155289 (accessed: April 20, 2022). DOI: 10.4048/jbc.2015.18.2.134.

  17. Maria Ryssdal Kraby, Marit Valla, Signe Opdahl, Olav Anton Haugen, Joanna Ewa Sawicka, Monica Jernberg Engstrom, Anna Mary Bofin. The prognostic value of androgen receptors in breast cancer subtypes. Breast Cancer Res Treat. 2018; 172 (2): 283–296. Available at: https://pubmed.ncbi.nlm.nih.gov/ 30109519 (accessed: April 10, 2021). DOI: 10.1007/s10549-018-4904-x.

  18. Ximena Garcia, Andres Elia, Lucrecia Galizzi, Maria May, Eunice Spengler, Paula Martinez Vazquez, Javier Burruchaga, Hugo Gass, Claudia Lanari, Caroline A. Lamb. Increased androgen receptor expression in estrogen receptor-positive/progesterone receptor-negative breast cancer. Breast Cancer Res Treat. 2020; 180 (1): 257–263. Available at: https://pubmed.ncbi.nlm.nih.gov/31950383 (accessed: April 10, 2021). DOI: 10.1007/s10549-020-05527-3.

  19. Yaewon Yang, Ahrum Min, Kyung-Hun Lee, Han Suk Ryu, Tae-Yong Kim, Go-Un Woo, Koung Jin Suh, Dae-Won Lee, Han-Byoel Lee, Hyeong-Gon Moon, Woonshik Han, In Ae Park, Dong-Young Noh, Seock-Ah Im. Prognostic role of androgen receptor expression in surgically resected early breast cancer patients. J. Breast Cancer. 2020; 23 (2): 182–193. Available at: https://pubmed.ncbi.nlm.nih.gov/ 32395377 (accessed: April 10, 2021). DOI: 10.4048/jbc.2020.23.e28.

  20. Ivana Mrklic, Zenon Pogorelic, Vesna Capkun, Snjezana Tomic. Expression of androgen receptors in triple negative breast carcinomas. Acta Histochem. 2013; 115 (4): 344–348. Available at: https://www.ncbi.nlm.nih.gov/23031358 (accessed: April 07, 2021). DOI: 10.1016/j.acthis.2012.09.006.

  21. Yoshinari Ogawa, Eishu Hai, Kanako Matsumoto, Katsumi Ikeda, Shinya Tokunaga, Hisashi Nagahara, Katsunobi Sakurai, Takeshi Inoue, Yukio Nishiguchi. Androgen receptor expression in breast cancer: relationship with clinicopathological factors and biomarkers. Int. J. Clin. Oncol. 2008; 13 (5): 431–435. Available at: https://www.ncbi.nlm.nih.gov/pubmed/?term=Ogawa+Y%2C+Hai+E%2C+Matsumoto+K+et+al. +Androgen+receptor (accessed: February 11, 2020). DOI: 10.1007/s10147-008-0770-6.

  22. Changjun Wang, Bo Pan, Hanjiang Zhu, Yidong Zhou, Feng Mao, Yan Lin, Qianqian Xu, Qiang Sun. Prognostic value of androgen receptor in triple negative breast cancer: a metaanalysis. Oncotarget. 2016; 7 (29): 46482–46491. Available at: https://www.ncbi.nlm.nih.gov/pubmed/27374089 (accessed: February 03, 2020). DOI: 10.18632/oncotarget.10208.

  23. Teoh P.Y., Tan G.C., Mahsin H., Wong Y.P. Androgen receptor expression in triple negative breast carcinoma and its association with the clinicopathological parameters. Malays J. Pathol. 2019; 41 (2): 125–132. Available at: https://pubmed.ncbi.nlm.nih.gov/31427547 (accessed: April 20, 2022). PMID: 31427547.

  24. Tetsuyo Maeda, Yoko Nakanishi, Yukari Hirotani, Fumi Fuchinoue, Katsuhisa Enomoto, Kenichi Sakurai, Sadao Amano, Norimichi Nemoto. Immunohistochemical co-expression status of cytokeratin 5/6, androgen receptor, and p53 as prognostic factors of adjuvant chemotherapy for triple negative breast cancer. Med. Mol. Morphol. 2016; 49 (1): 11–21. Available at: https://pubmed.ncbi.nlm.nih.gov/ 26009308 (accessed: April 05, 2021). DOI: 10.1007/s00795-015- 0109-0.

  25. Jung Eun Choi, Su Hwan Kang, Soo Jung Lee, Young Kyung Bae. Androgen receptor expression predicts decreased survival in early stage triple-negative breast cancer. Ann Surg Oncol. 2015; 22 (1): 82–89. Available at: https://pubmed.ncbi.nlm.nih.gov/25145503 (accessed: April 07, 2021). DOI: 10.1245/ s10434-014-3984-z.

  26. Keely M. McNamara, Tomomi Yoda, Yasuhiro Miki, Niramol Chanplakorn, Sansanee Wongwaisayawan, Pimpin Incharoen, Youwanush Kongdan, Lin Wang, Kiyoshi Takagi, Takagi Mayu, Yasuhiro Nakamura, Takashi Suzuki, Noriko Nemoto, Minoru Miyashita, Kentaro Tamaki, Takanori Ishida, Noriaki Ohuchi, Hironobu Sasano. Androgenic pathway in triple negative invasive ductal tumors: its correlation with tumor cell proliferation. Cancer Sci. 2013; 104 (5): 639–646. Available at: http://pubmed.ncbi.nlm.nih.gov/23373898 (accessed: April 07, 2021). DOI: 10.1111/cas.12121.

  27. Lisa M. Sutton, Dengfeng Cao, Venetia Sarode, Kyle H. Molberg, Kwame Torgbe, Barbara Haley, Yan Peng. Decreased androgen receptor expression is associated with distant metastases in patients with an

    drogen receptor-expressing triple-negative breast carcinoma. Am. J. Clin. Pathol. 2012; 138 (4): 511–516. Available at: http://pubmed.ncbi.nlm.nih.gov/23010705 (accessed: April 07, 2021). DOI: 10.1309/AJCP8AVF8FDPTZLH.

  28. Frank G.A., Zavalishina L.E., Pozharisskiy K.M. Rak molochnoy zhelezy: prakticheskoe rukovodstvo dlya vrachey [Breast Cancer: Practice Guidelines for Physicians]. Moscow; 2017. 176 (in Russian).

  29. Amrallah A. Mohammed, Fifi Mostafa Elsayed, Mohammed Algazar, Hayam E. Rashed, Abeer Hussien Anter. Neoadjuvant chemotherapy in triple negative breast cancer: correlation between androgen receptor expression and pathological response. Asian Pac. J. Cancer Prev. 2020; 21 (2): 563–568. Available at: https://pubmed.ncbi.nlm.nih.gov/32102539 (accessed: 03.04.2021). DOI: 10.31557/APJCP.2020.21.2.563.

Received 17 March 2022; accepted 25 June 2022.

 

Information about the authors

Panchenko Ivan Sergeevich, Post-graduate Student, Chair of Oncology and Radiation Diagnostics, Medical Department named after T.Z. Biktimirov, Ulyanovsk State University. 432017, Russia, Ulyanovsk, L. Tolstoy St., 42; e-mail: This email address is being protected from spambots. You need JavaScript enabled to view it., ORCID ID: http://orcid.org/0000-0001-7923-4317

Rodionov Valery Vitalievich, Doctor of Sciences (Medicine), Head of the Department of Breast Pathology, National Medical Research Center for Obstetrics, Gynecology and Perinatology named after academician
V.I. Kulakov, Ministry of Health of the Russian Federation. 117997, Russia, Moscow, Akademik Oparin St., 4; e-mail: This email address is being protected from spambots. You need JavaScript enabled to view it., ORCID ID: http://orcid.org/0000-0003-0096-7126

Panchenko Sergey Viktorovich, Candidate of Sciences (Medicinel, Associate Professor, Chair of Oncology and Radiation Diagnostics, Medical department named after T.Z. Biktimirov, Ulyanovsk State University. 432017, Russia, Ulyanovsk, L. Tolstoy St., 42; e-mail: This email address is being protected from spambots. You need JavaScript enabled to view it., ORCID: http://orcid.org/0000-0002-9006-2023

Sharafutdinov Marat Gakifovich, Candidate of Sciences (Medicine), Head of the Chair of Oncology and Radiation Diagnostics, Medical Department named after T.Z. Biktimirov, Ulyanovsk State University. 432017, Russia, Ulyanovsk, st. L. Tolstoy, 42; e-mail: This email address is being protected from spambots. You need JavaScript enabled to view it.; ORCID: http://orcid.org/0000-0002-8782-4111

 

For citation

Panchenko I.S., Rodionov V.V., Panchenko S.V., Sharafutdinov M.G. Fenotipicheskie osobennosti androgen-retseptor-pozitivnogo raka v gruppe trizhdy negativnogo raka molochnoy zhelezy [Phenotypic characteristics of androgen receptor-positive cancer in the triple-negative breast cancer group]. Ul'yanovskiy mediko-biologicheskiy zhurnal. 2022; 3: 49–60. DOI: 10.34014/2227-1848-2022-3-49-60 (in Russian).

 

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УДК 616-006.699

DOI 10.34014/2227-1848-2022-3-49-60

ФЕНОТИПИЧЕСКИЕ ОСОБЕННОСТИ АНДРОГЕН-РЕЦЕПТОР-ПОЗИТИВНОГО РАКА В ГРУППЕ ТРИЖДЫ НЕГАТИВНОГО РАКА МОЛОЧНОЙ ЖЕЛЕЗЫ

И.С. Панченко1, В.В. Родионов2, С.В. Панченко1, М.Г. Шарафутдинов1

1 ФГБОУ ВО «Ульяновский государственный университет», г. Ульяновск, Россия;

2 ФГБУ «Национальный медицинский исследовательский центр акушерства, гинекологии и перинатологии им. академика В.И. Кулакова» Министерства здравоохранения РФ, г. Москва, Россия

 

Цель. Выявить фенотипические особенности андроген-рецептор-позитивного рака молочной железы в структуре трижды негативного рака молочной железы.

Материалы и методы. Проведен анализ клинических и морфологических данных опухоли у 253 пациенток с морфологически верифицированным инвазивным трижды негативным раком молочной железы (ТНРМЖ), получавших лечение в ГУЗ Областной клинический онкологический диспансер г. Ульяновска и отделении патологии молочной железы ФГБУ «Национальный медицинский исследовательский центр акушерства, гинекологии и перинатологии им. В.И. Кулакова» в период с 2014 по 2021 г.

Результаты. Посредством статистического анализа на примере 45 чел. (18 % от общего количества выборки) было выявлено, что экспрессия андрогенных рецепторов (АР) при ТНРМЖ встречается у пациенток старше 61 года (р=0,054), ассоциируется с более распространенной стадией заболевания (начиная с IIB) (р=0,004), мультифокальным характером роста (р=0,025), инвазивным дольковым вариантом рака (р=0,04), более высокой дифференцировкой опухоли (р<0,0001), низким уровнем Ki67 (р=0,000001), более частым поражением регионарных лимфоузлов (р=0,005). Вместе с тем не было отмечено статистически значимых корреляций между экспрессией АР и менструальной функцией, квадрантом поражения молочной железы, достижением патоморфологического ответа после проведения неоадъювантной полихимиотерапии.

Выводы. Экспрессия АР при ТНРМЖ встречается у пациенток старше 61 года при местно-распространенной стадии заболевания, мультифокальном характере роста опухоли, инвазивном дольковом варианте рака, опухолях с высокой дифференцировкой и низкой пролиферативной активностью.

Ключевые слова: рак молочной железы, трижды негативный рак молочной железы (ТНРМЖ), андрогенные рецепторы (АР).

 

Литература

  1. Katrina R. Bauer, Monica Brown, Rosemary D. Cress, Carol A. Parise, Vincent Caggiano. Descriptive analysis of estrogen receptor (ER)-negative, progesterone receptor (PR)-negative, and HER2-negative invasive breast cancer, the so-called triple-negative phenotype: a population-based study from the California Cancer Registry. Cancer. 2007; 109 (9): 1721–1728. URL: https://pubmed.ncbi.nlm.nih.gov/ 17387718 (дата обращения: 07.04.2021). DOI: 10.1002/cncr.22618.

  2. Rebecca Dent, Maureen Trudeau, Kathleen I. Pritchard, Wedad M. Hanna, Harriet K. Kahn, Carol A. Sawka, Lavina A. Lickley, Ellen Rawlinson, Ping Sun, Steven A. Narod. Triple-negative breast cancer: clinical features and patterns of recurrence. Clin. Cancer Res. 2007; 13 (15, Pt. 1): 4429–4434. URL: https://pubmed.ncbi.nlm.hih.gov/17671126 (дата обращения: 07.04.2021). DOI: 10.1158/1078-0432.CCR-06-3045.

  3. Maryam Nakhjavani, Jennifer E Hardingham, Helen M. Palethorpe, Tim J. Price, Amanda R. Townsend. Druggable Molecular Targets for the Treatment of Triple Negative Breast Cancer. J. Breast Cancer. 2019; 22 (3): 341–361. URL: https://pubmed.ncbi.nlm.nih.gov/31598336 (дата обращения: 07.04.2021). DOI: 10.4048/jbc.2019.22.e39.

  4. Alis R.T. Bergin, Sherene Loi. Triple-negative breast cancer: recent treatment advances. F1000Res. 2019; 8: F1000 Faculty Rev-1342. URL: https:// pubmed.ncbi.nlm.nih.gov/31448088 (дата обращения: 16.04.2021). DOI: 10.12688/f1000research.18888.1.

  5. Brain D. Lehmann, Bojana Jovanovic, Xi Chen, Monica V. Estrada, Kimberly N. Johnson, Yu Shyr, Harold L. Moses, Melinda E. Sanders, Jennifer A. Pietenpol. Refinement of Triple-Negative Breast Cancer Molecular Subtypes: Implications for Neoadjuvant Chemotherapy Selection. PLoS One. 2016; 11 (6): e0157368. URL: https://pubmed.ncbi.nlm.nih.gov/27310713 (дата обращения: 07.04.2021). DOI: 10.1371/journal.pone.0157368.

  6. Jesse Lopes da Silva, Natalia Cristina Cardoso Nunes, Patricia Izetti, Guilherme Gomes de Mesquita, Andrea Cristina de Melo. Triple negative breast cancer: A thorough review of biomarkers. Crit Rev Oncol Hematol. 2020; 145: 102855. URL: https:// pubmed.ncbi.nlm.nih.gov/31927455 (дата обращения: 07.04.2021). DOI: 10.1016/j.critrevonc.2019.102855.

  7. Sewha Kim, Byung-In Moon, Woosung Lim, Sanghui Park, Min Sun Cho, Sun Hee Sung. Feasibility of classification of triple negative breast cancer by immunohistochemical surrogate markers. Clin Breast Cancer. 2018; 18 (5): e1123–e1132. URL: https:// pubmed.ncbi.nlm.nih.gov/29754847 (дата обращения: 07.04.2021). DOI: 10.1016/j.clbc.2018.03.012.

  8. Ugo Testa, Germana Castelli, Elvira Pelosi. Breast Cancer: A molecularly heterogenous disease needing subtype-specific treatments. Med Sci (Basel). 2020; 8 (1): 18. URL: https://pubmed.ncbi.nlm.nih.gov/ 32210163 (дата обращения: 07.04.2021). DOI: 10.3390/medsci8010018.

  9. Matthew D. Burstein, Anna Tsimelzon, Graham M. Poage, Kyle R. Covington, Alejandro Contreras, Suzanne A.W. Fuqua, Michelle I. Savage, C. Kent Osborne, Susan G. Hilsenbeck, Jenry C. Chang, Gordon B. Mills, Ching C. Lau, Powel H. Brown. Comprehensive genomic analysis identifies novel subtypes and targets of triple-negative breast cancer. Clin Cancer Res. 2015; 21 (7): 1688–1698. URL: https://pubmed.ncbi.nlm.nih.gov/25208879 (дата обращения: 01.07.2020). DOI: 10.1158/1078-0432.CCR-14-0432.

  10. Yа‑Xuan Lui, Ke-Jing Zhang, Li‑Li Tang. Clinical significance of androgen receptor expression in triple negative breast cancer‑an immunohistochemistry study. Oncol Lett. 2018; 15 (6): 10008–10016. URL: https://pubmed.ncbi.nlm.nih.gov/29844843 (дата обращения: 07.04.2021). DOI: 10.3892/ol.2018.8548.

  11. Murtuza Rampurwala, Kari B. Wisinski, Ruth O'Regan R. Role of the androgen receptor in triple-negative breast cancer. Clin Adv Hematol Oncol. 2016; 14 (3): 186–193. URL: https://pubmed.ncbi.nlm.nih.gov/27058032 (дата обращения: 16.03.2021). PMCID: PMC5221599.

  12. Francisco E. Vera-Badillo, Amoud J. Templeton, Paulo de Gouveia, Ivan Diaz-Padilla, Philippe L. Bedard, Mustafa Al-Mubarak, Bostjan Seruga, Ian F. Tannock, Alberto Ocana, Eitan Amir. Androgen receptor expression and outcomes in early breast cancer: a systematic review and meta-analysis. J. Natl Cancer Inst. 2014; 106 (1): 319. URL: https://pubmed.ncbi.nlm.nih.gov/24273215 (дата обращения: 20.04.2022). DOI: 10.1093/jnci/djt319.

  13. Kevin H. Kensler, Elizabeth M. Poole, Yujing J. Heng, Laura C. Collins, Benjamin Glass, Andrew H. Beck, Aditi Hazra, Bernard A. Rosner, A. Heather Eliassen, Susan E. Hankinson, Eric P. Winer, Myles Brown, Rulla M. Tamimi. Androgen Receptor Expression and Breast Cancer Survival: Results From the Nurses' Health Studies. J. Natl Cancer Inst. 2019; 111 (7): 700–708. URL: https://pubmed.ncbi.nlm.nih.gov/ 30445651 (дата обращения: 20.04.2022). DOI: 10.1093/jnci/djy173.

  14. Park S., Koo J.S., Kim M.S., Park H.S., Lee J.S., Lee J.S., Kim S.I., Park B.W., Lee K.S. Androgen receptor expression is significantly associated with better outcomes in estrogen receptor-positive breast cancers. Ann Oncol. 2011; 22 (8): 1755–1762. URL: https://pubmed.ncbi.nlm.nih.gov/21310761 (дата обращения: 20.04.2022). DOI: 10.1093/annonc/mdq678.

  15. Karin Elebro, Signe Borgquist, Maria Simonsson, Andrea Markkula, Karin Jirström, Christian Ingvar, Carsten Rose, Helena Jernström. Combined Androgen and Estrogen Receptor Status in Breast Cancer: Treatment Prediction and Prognosis in a Population-Based Prospective Cohort. Clin Cancer Res. 2015; 21 (16): 3640–3650. URL: https://pubmed.ncbi.nlm.nih.gov/25904752 (дата обращения: 20.04.2022). DOI: 10.1158/1078-0432.CCR-14-2564.

  16. Yoonseok Kim, Eunae Jae, Myunghee Yoon. Influence of Androgen Receptor Expression on the Survival Outcomes in Breast Cancer: A Meta-Analysis. J. Breast Cancer. 2015; 18 (2): 134–142. URL: https://pubmed.ncbi.nlm.nih.gov/26155289 (дата обращения: 20.04.2022). DOI: 10.4048/jbc.2015.18.2.134.

  17. Maria Ryssdal Kraby, Marit Valla, Signe Opdahl, Olav Anton Haugen, Joanna Ewa Sawicka, Monica Jernberg Engstrom, Anna Mary Bofin. The prognostic value of androgen receptors in breast cancer subtypes. Breast Cancer Res Treat. 2018; 172 (2): 283–296. URL: https://pubmed.ncbi.nlm.nih.gov/ 30109519 (дата обращения: 10.04.2021). DOI: 10.1007/s10549-018-4904-x.

  18. Ximena Garcia, Andres Elia, Lucrecia Galizzi, Maria May, Eunice Spengler, Paula Martinez Vazquez, Javier Burruchaga, Hugo Gass, Claudia Lanari, Caroline A. Lamb. Increased androgen receptor expression in estrogen receptor-positive/progesterone receptor-negative breast cancer. Breast Cancer Res Treat. 2020; 180 (1): 257–263. URL: https://pubmed.ncbi.nlm.nih.gov/31950383 (дата обращения: 10.04.2021). DOI: 10.1007/s10549-020-05527-3.

  19. Yaewon Yang, Ahrum Min, Kyung-Hun Lee, Han Suk Ryu, Tae-Yong Kim, Go-Un Woo, Koung Jin Suh, Dae-Won Lee, Han-Byoel Lee, Hyeong-Gon Moon, Woonshik Han, In Ae Park, Dong-Young Noh, Seock-Ah Im. Prognostic role of androgen receptor expression in surgically resected early breast cancer patients. J. Breast Cancer. 2020; 23 (2): 182–193. URL: https://pubmed.ncbi.nlm.nih.gov/32395377 (дата обращения: 10.04.2021). DOI: 10.4048/jbc.2020.23.e28.

  20. Ivana Mrklic, Zenon Pogorelic, Vesna Capkun, Snjezana Tomic. Expression of androgen receptors in triple negative breast carcinomas. Acta Histochem. 2013; 115 (4): 344–348. URL: https://www.ncbi. nlm.nih.gov/23031358 (дата обращения: 07.04.2021). DOI: 10.1016/j.acthis.2012.09.006.

  21. Yoshinari Ogawa, Eishu Hai, Kanako Matsumoto, Katsumi Ikeda, Shinya Tokunaga, Hisashi Nagahara, Katsunobi Sakurai, Takeshi Inoue, Yukio Nishiguchi. Androgen receptor expression in breast cancer: relationship with clinicopathological factors and biomarkers. Int. J. Clin. Oncol. 2008; 13 (5): 431–435. URL: https://www.ncbi.nlm.nih.gov/pubmed/?term=Ogawa+Y%2C+Hai+E%2C+Matsumoto+K+et+al. +Androgen+receptor (дата обращения: 11.02.2020). DOI: 10.1007/s10147-008-0770-6.

  22. Changjun Wang, Bo Pan, Hanjiang Zhu, Yidong Zhou, Feng Mao, Yan Lin, Qianqian Xu, Qiang Sun. Prognostic value of androgen receptor in triple negative breast cancer: a metaanalysis. Oncotarget. 2016; 7 (29): 46482–46491. URL: https://www.ncbi.nlm.nih.gov/pubmed/27374089 (дата обращения: 03.02.2020). DOI: 10.18632/oncotarget.10208.

  23. Teoh P.Y., Tan G.C., Mahsin H., Wong Y.P. Androgen receptor expression in triple negative breast carcinoma and its association with the clinicopathological parameters. Malays J. Pathol. 2019; 41 (2): 125–132. URL: https://pubmed.ncbi.nlm.nih.gov/31427547 (дата обращения: 20.04.2022).

  24. Tetsuyo Maeda, Yoko Nakanishi, Yukari Hirotani, Fumi Fuchinoue, Katsuhisa Enomoto, Kenichi Sakurai, Sadao Amano, Norimichi Nemoto. Immunohistochemical co-expression status of cytokeratin 5/6, androgen receptor, and p53 as prognostic factors of adjuvant chemotherapy for triple negative breast cancer. Med. Mol. Morphol. 2016; 49 (1): 11–21. URL: https://pubmed.ncbi.nlm.nih.gov/26009308 (дата обращения: 05.04.2021). DOI: 10.1007/s00795-015- 0109-0.

  25. Jung Eun Choi, Su Hwan Kang, Soo Jung Lee, Young Kyung Bae. Androgen receptor expression predicts decreased survival in early stage triple-negative breast cancer. Ann Surg Oncol. 2015; 22 (1): 82–89. URL: https://pubmed.ncbi.nlm.nih.gov/25145503 (дата обращения: 07.04.2021). DOI: 10.1245/s10434-014-3984-z.

  26. Keely M. McNamara, Tomomi Yoda, Yasuhiro Miki, Niramol Chanplakorn, Sansanee Wongwaisayawan, Pimpin Incharoen, Youwanush Kongdan, Lin Wang, Kiyoshi Takagi, Takagi Mayu, Yasuhiro Nakamura, Takashi Suzuki, Noriko Nemoto, Minoru Miyashita, Kentaro Tamaki, Takanori Ishida, Noriaki Ohuchi, Hironobu Sasano. Androgenic pathway in triple negative invasive ductal tumors: its correlation with tumor cell proliferation. Cancer Sci. 2013; 104 (5): 639–646. URL: http://pubmed.ncbi.nlm.nih.gov/ 23373898 (дата обращения: 07.04.2021). DOI: 10.1111/cas.12121.

  27. Lisa M. Sutton, Dengfeng Cao, Venetia Sarode, Kyle H. Molberg, Kwame Torgbe, Barbara Haley, Yan Peng. Decreased androgen receptor expression is associated with distant metastases in patients with androgen receptor-expressing triple-negative breast carcinoma. Am. J. Clin. Pathol. 2012; 138 (4): 511–516. URL: http://pubmed.ncbi.nlm.nih.gov/23010705 (дата обращения: 07.04.2021). DOI: 10.1309/ AJCP8AVF8FDPTZLH.

  28. Франк Г.А., Завалишина Л.Э., Пожарисский К.М. Рак молочной железы: практическое руководство для врачей. М.; 2017. 176.

  29. Amrallah A. Mohammed, Fifi Mostafa Elsayed, Mohammed Algazar, Hayam E. Rashed, Abeer Hussien Anter. Neoadjuvant chemotherapy in triple negative breast cancer: correlation between androgen receptor expression and pathological response. Asian Pac. J. Cancer Prev. 2020; 21 (2): 563–568. URL: https://pubmed.ncbi.nlm.nih.gov/32102539 (дата обращения: 03.04.2021). DOI: 10.31557/APJCP.2020.21.2.563.

 Поступила в редакцию 17.03.2022; принята 25.06.2022.

 

Авторский коллектив

Панченко Иван Сергеевич – аспирант кафедры онкологии и лучевой диагностики медицинского факультета им. Т.З. Биктимирова, ФГБОУ ВО «Ульяновский государственный университет». 432017, Россия, г. Ульяновск, ул. Л. Толстого, 42; e-mail: This email address is being protected from spambots. You need JavaScript enabled to view it., ORCID ID: http://orcid.org/0000-0001-7923-4317

Родионов Валерий Витальевич – доктор медицинских наук, заведующий отделением патологии молочной железы, ФГБУ «Национальный медицинский исследовательский центр акушерства, гинекологии и перинатологии им. академика В.И. Кулакова» Министерства здравоохранения РФ. 117997, Россия, г. Москва, ул. Академика Опарина, 4; e-mail: This email address is being protected from spambots. You need JavaScript enabled to view it., ORCID ID: http://orcid.org/0000-0003-0096-7126

Панченко Сергей Викторович – кандидат медицинских наук, доцент кафедры онкологии и лучевой диагностики медицинского факультета им. Т.З. Биктимирова, ФГБОУ ВО «Ульяновский государственный университет». 432017, Россия, г. Ульяновск, ул. Л. Толстого, 42; e-mail: This email address is being protected from spambots. You need JavaScript enabled to view it., ORCID: http://orcid.org/0000-0002-9006-2023

Шарафутдинов Марат Гакифович – кандидат медицинских наук, заведующий кафедрой онкологии и лучевой диагностики медицинского факультета им. Т.З. Биктимирова, ФГБОУ ВО «Ульяновский государственный университет». 432017, Россия, г. Ульяновск, ул. Л. Толстого, 42; e-mail: This email address is being protected from spambots. You need JavaScript enabled to view it.; ORCID: http://orcid.org/0000-0002-8782-4111

 

Образец цитирования

Панченко И.С., Родионов В.В., Панченко С.В., Шарафутдинов М.Г. Фенотипические особенности андроген-рецептор-позитивного рака в группе трижды негативного рака молочной железы. Ульяновский медико-биологический журнал. 2022; 3: 49–60. DOI: 10.34014/2227-1848-2022-3-49-60.