ORIGINAL RESEARCH

Assessment of metastatic traits of the cells with hybrid phenotype in breast cancer

Mukhamedzhanov RK1,4, Grigoryeva ES2, Tashireva LA2, Perelmuter VM2, Zavyalova MV1,2, Savelieva OE2,3
About authors

1 Siberian State Medical University, Tomsk, Russia

2 Cancer Research Institute, Tomsk National Research Medical Center, Russian Academy of Sciences, Tomsk, Russia

3 Saint Petersburg State Pediatric Medical University, Saint Petersburg, Russia

4 Regional Children’s Clinical Hospital, Vladimir, Russia

Correspondence should be addressed: Olga E. Savelieva
Litovskaya, 2, Saint-Petersburg, 194100; ur.liam@anihcehc_aglo

About paper

Funding: the study was supported by the RSF grant № 21-15-00140.

Author contribution: Mukhamedzhanov RK — literature analysis, data acquisition and statistical processing, manuscript writing; Grigoryeva ES — data acquisition and analysis, manuscript writing; Tashireva LA — study design, manuscript editing; Perelmuter VM — data interpretation, manuscript editing; Zavyalova MV — study planning, manuscript editing; Savelieva OE — study planning and management, data analysis and interpretation, manuscript writing.

Compliance with the ethical standards: the study was approved by the Ethics Committee of the Cancer Research Institute, Tomsk National Research Medical Center (protocol № 10 of 24 April 2015) and conducted in accordance with the Federal Laws of the Russian Federation (№ 152, 323, etc.), the Declaration of Helsinki (1964) and all subsequent amendments and supplements regulating the research involving human biomaterials. The informed consent to study participation was submitted by all subjects.

Received: 2023-07-04 Accepted: 2023-08-22 Published online: 2023-08-31
|
  1. Ruiz-Rodríguez AJ, Molina-Vallejo MP, Aznar-Peralta I, González Puga C, Cañas García I, González E, et al. Deep Phenotypic Characterisation of CTCs by Combination of Microfluidic Isolation (IsoFlux) and Imaging Flow Cytometry (ImageStream). Cancers (Basel). 2021; 13 (24): 6386.
  2. Zhang Q, Kong D, Yang Z, Li G, Cheng S, Feng L, et al. Prognostic value of stem-like circulating tumor cells in patients with cancer: a systematic review and meta-analysis. Clin Exp Med. 2023. DOI: 10.1007/s10238-023-01009-0.
  3. Orrapin S, Udomruk S, Lapisatepun W, Moonmuang S, Phanphaisarn A, Phinyo P, et al. Clinical Implication of Circulating Tumor Cells Expressing Epithelial Mesenchymal Transition (EMT) and Cancer Stem Cell (CSC) Markers and Their Perspective in HCC: A Systematic Review. Cancers (Basel). 2022; 14 (14): 3373.
  4. Grigoryeva ES, Tashireva LA, Alifanov VV, Savelieva OE, Vtorushin SV, Zavyalova MV, et al. Molecular subtype conversion in CTCs as indicator of treatment adequacy associated with metastasis-free survival in breast cancer. Sci Rep. 2022; 12 (1): 20949.
  5. Fina E, Cleris L, Dugo M, Lecchi M, Ciniselli CM, Lecis D, et al. Gene signatures of circulating breast cancer cell models are a source of novel molecular determinants of metastasis and improve circulating tumor cell detection in patients. J Exp Clin Cancer Res. 2022; 41 (1): 78.
  6. Grigoryeva ES, Tashireva LA, Savelieva OE, Zavyalova MV, Popova NO, Kuznetsov GA, et al. The Association of Integrins β3, β4, and αVβ5 on Exosomes, CTCs and Tumor Cells with Localization of Distant Metastasis in Breast Cancer Patients. Int J Mol Sci. 2023; 24 (3): 2929.
  7. Hoshino A, Costa-Silva B, Shen TL, Rodrigues G, Hashimoto A, Tesic Mark M, et al. Tumour exosome integrins determine organotropic metastasis. Nature. 2015; 527 (7578): 329–35.
  8. Guan X, Ma F, Li C, Wu S, Hu S, Huang J, et al. The prognostic and therapeutic implications of circulating tumor cell phenotype detection based on epithelial-mesenchymal transition markers in the first-line chemotherapy of HER2-negative metastatic breast cancer. Cancer Commun (Lond). 2019; 39 (1): 1.
  9. Wankhede D, Grover S, Hofman P. Circulating Tumor Cells as a Predictive Biomarker in Resectable Lung Cancer: A Systematic Review and Meta-Analysis. Cancers (Basel). 2022; 14 (24): 6112.
  10. Jou HJ, Ling PY, Hsu HT. Circulating tumor cells as a "real-time liquid biopsy": Recent advances and the application in ovarian cancer. Taiwan J Obstet Gynecol. 2022; 61 (1): 34–39.
  11. Li H, Liu Q, Liang S, Yao P, Lv J, Wang G, et al. Circulating tumor cells and neutrophil-lymphocyte ratio are predictive markers for metastatic colorectal cancer patients. Transl Cancer Res. 2021; 10 (1): 288–97.
  12. Papadaki MA, Stoupis G, Theodoropoulos PA, Mavroudis D, Georgoulias V, Agelaki S. Circulating Tumor Cells with Stemness and Epithelial-to-Mesenchymal Transition Features Are Chemoresistant and Predictive of Poor Outcome in Metastatic Breast Cancer. Mol Cancer Ther. 2019; 18 (2): 437–47.
  13. Lustberg MB, Balasubramanian P, Miller B, Garcia-Villa A, Deighan C, Wu Y, et al. Heterogeneous atypical cell populations are present in blood of metastatic breast cancer patients. Breast Cancer Res. 2014; 16 (2): R23.
  14. Ishizawa K, Yamanaka M, Saiki Y, Miyauchi E, Fukushige S, Akaishi T, et al. CD45+CD326+ Cells are Predictive of Poor Prognosis in NonSmall Cell Lung Cancer Patients. Clin Cancer Res. 2019; 25 (22): 6756–63.
  15. Dittmar T, Zänker KS. Introduction. In: Dittmar T, Zänker KS. Cell Fusion in Health and Disease. Advances in Experimental Medicine and Biology, vol 950. Dordrecht: Springer, 2011; p. 1–3.
  16. Laberge GS, Duvall E, Haedicke K, Pawelek J. Leukocyte-Cancer Cell Fusion-Genesis of a Deadly Journey. Cells. 2019; 8 (2): 170.
  17. Pospelova RA. Lejkokoncentraciya v klinicheskoj praktike: diagnosticheskoe znachenie. M.: Medicina, 1973; 88 s. Russian.
  18. Agnoletto C, Corrà F, Minotti L, Baldassari F, Crudele F, Cook WJJ, et al. Heterogeneity in Circulating Tumor Cells: The Relevance of the Stem-Cell Subset. Cancers (Basel). 2019; 11 (4): 483.
  19. Noubissi FK, Ogle BM. Cancer Cell Fusion: Mechanisms Slowly Unravel. Int J Mol Sci. 2016; 17 (9): 1587.
  20. Kaur E, Rajendra J, Jadhav S, Shridhar E, Goda JS, Moiyadi A, et al. Radiation-induced homotypic cell fusions of innately resistant glioblastoma cells mediate their sustained survival and recurrence. Carcinogenesis. 2015; 36 (6): 685–95.
  21. Yan B, Wang J, Liu L. Chemotherapy promotes tumour cell hybridization in vivo. Tumour Biol. 2016; 37 (4): 5025–30.
  22. Gires O, Pan M, Schinke H, Canis M, Baeuerle PA. Expression and function of epithelial cell adhesion molecule EpCAM: where are we after 40 years? Cancer Metastasis Rev. 2020; 39 (3): 969–87.
  23. Fidanza A, Stumpf PS, Ramachandran P, Tamagno S, Babtie A, Lopez-Yrigoyen M et al. Single-cell analyses and machine learning define hematopoietic progenitor and HSC-like cells derived from human PSCs. Blood. 2020; 136 (25): 2893–904.
  24. Rodrigues M, Kosaric N, Bonham CA, Gurtner GC. Wound Healing: A Cellular Perspective. Physiol Rev. 2019; 99 (1): 665– 706.
  25. Psaila B, Lyden D. The metastatic niche: adapting the foreign soil. Nat Rev Cancer. 2009; 9 (4): 285–93.
  26. Pan B, Guo J, Liao Q, Zhao Y. β1 and β3 integrins in breast, prostate and pancreatic cancer: A novel implication. Oncol Lett. 2018; 15 (4): 5412–6.
  27. Abdel-Ghany M, Cheng HC, Elble RC, Pauli BU. The breast cancer beta 4 integrin and endothelial human CLCA2 mediate lung metastasis. J Biol Chem. 2001; 276 (27): 25438–46.
  28. Liu F, Wu Q, Dong Z, Liu K. Integrins in cancer: Emerging mechanisms and therapeutic opportunities. Pharmacol Ther. 2023; 247: 108458.
  29. Savelieva OE, Tashireva LA, Buldakov MA, Mukhamedzhanov RK, Kaigorodova EV, Denisov EV, et al. CXCR4 expression in different subsets of CTCs and single (detached) breast cancer cells. Siberian journal of oncology. 2018; 17 (4): 75–80.
  30. Ramakrishnan M, Mathur SR, Mukhopadhyay A. Fusion-derived epithelial cancer cells express hematopoietic markers and contribute to stem cell and migratory phenotype in ovarian carcinoma. Cancer Res. 2013; 73 (17): 5360–70.