Have a personal or library account? Click to login
The prognostic significance of tumor-immune microenvironment in ascites of patients with high-grade serous carcinoma Cover

The prognostic significance of tumor-immune microenvironment in ascites of patients with high-grade serous carcinoma

Open Access
|Nov 2023

References

  1. Auer K, Bachmayr-Heyda A, Sukhbaatar N, Aust S, Schmetterer KG, Meier SM, et al. Role of the immune system in the peritoneal tumor spread of high grade serous ovarian cancer. Oncotarget 2016; 7: 61336–54. doi: 10.18632/oncotarget.11038
  2. Wefers C, Duiveman-de Boer T, Yigit R, Zusterzeel PLM, van Altena AM, Massuger LFAG, et al. Survival of ovarian cancer patients is independent of the presence of DC and T cell subsets in ascites. Front Immunol 2019; 11: 3156–65. doi: 10.3389/fimmu.2018.03156
  3. du Bois A, Quinn M, Thigpen T, Vermorken J, Avall-Lundqvist E, Bookman M, et al. 2004 consensus statements on the management of ovarian cancer: final document of the 3rd international gynecologic cancer intergroup ovarian cancer consensus conference (GCIG OCCC 2004). Ann Oncol 2005; 16(Suppl 8): viii7–12. doi: 10.1093/annonc/mdi961
  4. Zhu C, Xu Z, Zhang T, Qian L, Xiao W, Wei H, et al. Updates of pathogenesis, diagnostic and therapeutic perspectives for ovarian clear cell carcinoma. J Cancer 2021; 12: 2295–316. doi: 10.7150/jca.53395
  5. Zhang L, Conejo-Garcia JR, Katsaros D, Gimotty PA, Massobrio M, Regnani G, et al. Intratumoral T cells, recurrence, and survival in epithelial ovarian cancer. N Engl J Med 2003; 348: 203–13. doi: 10.1056/NEJMoa020177
  6. Webb JR, Milne K, Watson P, Deleeuw RJ, Nelson BH. Tumor-infiltrating lymphocytes expressing the tissue resident memory marker CD103 are associated with increased survival in high-grade serous ovarian cancer. Clin Cancer Res 2014; 20: 434–44. doi: 10.1158/1078-0432.CCR-13-1877
  7. Gupta P, Chen C, Chaluvally-Raghavan P, Pradeep SB. Cells as an immune-regulatory signature in ovarian cancer. Cancers 2019; 11: 894–903. doi: 10.3390/cancers11070894
  8. Gupta V, Yull F, Khabele D. Bipolar tumor-associated macrophages in ovarian cancer as targets for therapy. Cancers 2018; 10: 366–98. doi: 10.3390/cancers10100366
  9. Piętak P, Pietrzyk N, Pawłowska A, Suszczyk D, Bednarek W, Kotarski J, et al. The meaning of PD-1/PD-L1 pathway in ovarian cancer pathogenesis. Wiad Lek 2018; 71: 1089–94.
  10. Preston CC, Maurer MJ, Oberg AL, Visscher DW, Kalli KR, Hartmann LC, et al. The ratios of CD8+ T cells to CD4+CD25+ FOXP3+ and FOXP3 T cells correlate with poor clinical outcome in human serous ovarian cancer. PLoS One 2013; 8: e80063. doi: 10.1371/journal.pone.0080063
  11. Nakano M, Ito M, Tanaka R, Yamaguchi K, Ariyama H, Mitsugi K, et al. PD-1+ TIM-3+ T cells in malignant ascites predict prognosis of gastrointestinal cancer. Cancer Sci 2018; 109: 2986–92. doi: 10.1111/cas.13723
  12. Miceska S, Škof E, Novaković S, Stegel V, Jeričević A, Grčar Kuzmanov B, et al. Cytopathological assessment is an accurate method for identifying immunophenotypic features and BRCA1/2 mutations of high-grade serous carcinoma from ascites. Cancer Cytopathol 2023; 131: 188–97. doi: 10.1002/cncy.22664
  13. Brozic A, Pohar Marinsek Z, Novakovic S, Kloboves Prevodnik V. Inconclusive flow cytometric surface light chain results can cytoplasmic light chains, Bcl-2 expression and PCR clonality analysis improve accuracy of cytological diagnoses in B-cell lymphomas? Diagn Pathol 2015; 20: 191–201. doi: 10.1186/s13000-015-0427-5
  14. Hoogstad-van Evert JS, Bekkers R, Ottevanger N, Jansen JH, Massuger L, Dolstra H. Harnessing natural killer cells for the treatment of ovarian cancer. Gynecol Oncol 2020; 157: 810–6. doi: 10.1016/j.ygyno.2020.03.020
  15. Ford CE, Werner B, Hacker NF, Warton K. The untapped potential of ascites in ovarian cancer research and treatment. Br J Cancer 2020; 123: 9–16. doi: 10.1038/s41416-020-0875-x
  16. Sato S, Matsushita H, Shintani D, Kobayashi Y, Fujieda N, Yabuno A, et al. Association between effector-type regulatory T cells and immune checkpoint expression on CD8+ T cells in malignant ascites from epithelial ovarian cancer. BMC Cancer 2022; 22: 437–45. doi: 10.1186/s12885-022-09534-z
  17. Steitz AM, Steffes A, Finkernagel F, Unger A, Sommerfeld L, Jansen JM, et al. Tumor-associated macrophages promote ovarian cancer cell migration by secreting transforming growth factor beta induced (TGFBI) and tenascin C. Cell Death Dis 2020; 11: 249–63. doi: 10.1038/s41419-020-2438-8
  18. Curiel TJ, Cheng P, Mottram P, Alvarez X, Moons L, Evdemon-Hogan M, et al. Dendritic cell subsets differentially regulate angiogenesis in human ovarian cancer. Cancer Res 2004; 64: 5535–8. doi: 10.1158/0008-5472.CAN-04-1272
  19. Almeida-Nunes DL, Mendes-Frias A, Silvestre R, Dinis-Oliveira RJ, Ricardo S. Immune tumor microenvironment in ovarian cancer ascites. Int J Mol Sci 2022; 23: 10692–714. doi: 10.3390/ijms231810692
  20. Sato E, Olson SH, Ahn J, Bundy B, Nishikawa H, Qian F, et al. Intraepithelial CD8+ tumor-infiltrating lymphocytes and a high CD8+/regulatory T cell ratio are associated with favorable prognosis in ovarian cancer. Proc Natl Acad Sci U S A 2005; 102: 18538–43. doi: 10.1073/pnas.0509182102
  21. Ning F, Cole CB, Annunziata CM. Driving immune responses in the ovarian tumor microenvironment. Front Oncol 2021; 10: 604084. doi: 10.3389/fonc.2020.604084
  22. Singh M, Loftus T, Webb E, Benencia F. Minireview: regulatory T cells and ovarian cancer. Immunol Invest 2016; 45: 712–20. doi: 10.1080/08820139.2016.1186689
  23. Knutson KL, Maurer MJ, Preston CC, Moysich KB, Goergen K, Hawthorne KM, et al. Regulatory T cells, inherited variation, and clinical outcome in epithelial ovarian cancer. Cancer Immunol Immunother 2015; 64: 1495–504. doi: 10.1007/s00262-015-1753-x
  24. Hoffmann JC, Schön MP. Integrin αE(CD103)β7 in epithelial cancer. Cancers 2021; 13: 6211–29. doi: 10.3390/cancers13246211
  25. Laumont CM, Wouters MCA, Smazynski J, Gierc NS, Chavez EA, Chong LC, et al. Single-cell profiles and prognostic impact of tumor-infiltrating lymphocytes coexpressing CD39, CD103, and PD-1 in ovarian cancer. Clin Cancer Res 2021; 27: 4089–100. doi: 10.1158/1078-0432.CCR-20-4394
  26. Webb JR, Wick DA, Nielsen JS, Tran E, Milne K, McMurtrie E, et al. Profound elevation of CD8+ T cells expressing the intraepithelial lymphocyte marker CD103 (alphaE/beta7 Integrin) in high-grade serous ovarian cancer. Gynecol Oncol 2010; 118: 228–36. doi: 10.1016/j.ygyno.2010.05.016
  27. Bösmüller HC, Wagner P, Peper JK, Schuster H, Pham DL, Greif K, et al. Combined immunoscore of CD103 and CD3 identifies long-term survivors in high-grade serous ovarian cancer. Int J Gynecol Cancer 2016; 26: 671–9. doi: 10.1097/IGC.0000000000000672
  28. Dong HP, Elstrand MB, Holth A, Silins I, Berner A, Trope CG, et al. NK- and B-cell infiltration correlates with worse outcome in metastatic ovarian carcinoma. Am J Clin Pathol 2006; 125: 451–8.
  29. Wei X, Jin Y, Tian Y, Zhang H, Wu J, Lu W, et al. Regulatory B cells contribute to the impaired antitumor immunity in ovarian cancer patients. Tumour Biol 2016; 37: 6581–8. doi: 10.1007/s13277-015-4538-0
  30. Nielsen JS, Sahota RA, Milne K, Kost SE, Nesslinger NJ, Watson PH, et al. CD20+ tumor-infiltrating lymphocytes have an atypical CD27-memory phenotype and together with CD8+ T cells promote favorable prognosis in ovarian cancer. Clin Cancer Res 2012; 18: 3281–92. doi: 10.1158/1078-0432.CCR-12-0234
  31. Truxova I, Kasikova L, Hensler M, Skapa P, Laco J, Pecen L, et al. Mature dendritic cells correlate with favorable immune infiltrate and improved prognosis in ovarian carcinoma patients. J Immunother Cancer 2018; 6: 139–51. doi: 10.1186/s40425-018-0446-3
  32. Labidi-Galy SI, Sisirak V, Meeus P, Gobert M, Treilleux I, Bajard A, et al. Quantitative and functional alterations of plasmacytoid dendritic cells contribute to immune tolerance in ovarian cancer. Cancer Res 2011; 71: 5423–34. doi: 10.1158/0008-5472.CAN-11-0367
  33. Ning F, Cole CB, Annunziata CM. Driving immune responses in the ovarian tumor microenvironment. Front Oncol 2021; 10: 604084–98. doi: 10.3389/fonc.2020.604084
  34. Nersesian S, Glazebrook H, Toulany J, Grantham SR, Boudreau JE. Naturally killing the silent killer: NK cell-based immunotherapy for ovarian cancer. Front Immunol 2019; 10: 1782–97. doi: 10.3389/fimmu.2019.01782
  35. Romee R, Foley B, Lenvik T, Wang Y, Zhang B, Ankarlo D, et al. NK cell CD16 surface expression and function is regulated by a disintegrin and metalloprotease-17 (ADAM17). Blood 2013; 121: 3599–608. doi: 10.1182/blood-2012-04-425397
  36. Larionova I, Tuguzbaeva G, Ponomaryova A, Stakheyeva M, Cherdyntseva N, Pavlov V, et al. Tumor-associated macrophages in human breast, colorectal, lung, ovarian and prostate cancers. Front Oncol 2020; 10: 566511–44. doi: 10.3389/fonc.2020.566511
  37. Hoover AA, Hufnagel DH, Harris W, Bullock K, Glass EB, Liu E, et al. Increased canonical NF-kappaB signaling specifically in macrophages is sufficient to limit tumor progression in syngeneic murine models of ovarian cancer. BMC Cancer 2020; 20: 970–85. doi: 10.1186/s12885-020-07450-8
  38. Nowak M, Klink M. The role of tumor-associated macrophages in the progression and chemoresistance of ovarian cancer. Cells 2020; 9: 1299–300. doi: 10.3390/cells9051299
  39. Osborn G, Stavraka C, Adams R, Sayasneh A, Ghosh S, Montes A, et al. Macrophages in ovarian cancer and their interactions with monoclonal antibody therapies. Clin Exp Immunol 2022; 209: 4–21. doi: 10.1093/cei/uxab020
  40. Leary A, Tan D, Ledermann J. Immune checkpoint inhibitors in ovarian cancer: where do we stand? Ther Adv Med Oncol 2021; 13: 17588359211039899. doi: 10.1177/17588359211039899
  41. Imai Y, Hasegawa K, Matsushita H, Fujieda N, Sato S, Miyagi E, et al. Expression of multiple immune checkpoint molecules on T cells in malignant ascites from epithelial ovarian carcinoma. Oncol Lett 2018; 15: 6457–68. doi: 10.3892/ol.2018.8101
  42. Pawłowska A, Suszczyk D, Tarkowski R, Paduch R, Kotarski J, Wertel I. et al. Programmed death-1 receptor (PD-1) as a potential prognosis biomarker for ovarian cancer patients. Cancer Manag Res 2020; 12: 9691–709. doi: 10.2147/CMAR.S263010
  43. Darb-Esfahani S, Kunze CA, Kulbe H, Sehouli J, Wienert S, Lindner J, et al. Prognostic impact of programmed cell death-1 (PD-1) and PD-ligand 1 (PD-L1) expression in cancer cells and tumor-infiltrating lymphocytes in ovarian high grade serous carcinoma. Oncotarget 2016; 7: 1486–99. doi: 10.18632/oncotarget.6429
  44. Xu M, Zhang B, Zhang M, Liu Y, Yin FL, Liu X, et al. Clinical relevance of expression of B7-H1 and B7-H4 in ovarian cancer. Oncol Lett 2016; 11: 2815–19. doi: 10.3892/ol.2016.4301
  45. Cai J, Wang D, Zhang G, Guo X. The role Of PD-1/PD-L1 axis in Treg development and function: Implications for cancer immunotherapy. Onco Targets Ther 2019; 12: 8437–45. doi: 10.2147/OTT.S221340
DOI: https://doi.org/10.2478/raon-2023-0046 | Journal eISSN: 1581-3207 | Journal ISSN: 1318-2099
Language: English
Page range: 493 - 506
Submitted on: Jun 27, 2023
|
Accepted on: Aug 13, 2023
|
Published on: Nov 30, 2023
In partnership with: Paradigm Publishing Services
Publication frequency: 4 issues per year

© 2023 Simona Miceska, Erik Skof, Simon Bucek, Cvetka Grasic Kuhar, Gorana Gasljevic, Spela Smrkolj, Veronika Kloboves Prevodnik, published by Association of Radiology and Oncology
This work is licensed under the Creative Commons Attribution 4.0 License.