Morphofunctional features of inflammation in the ovary after exposure to local electron irradiation and platelet-rich plasma administration

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Abstract

BACKGROUND: Radiotherapy for malignant neoplasms of the pelvic organs can lead to radiation-induced damage to healthy ovarian tissue, premature ovarian failure, and infertility. Research on reactive changes in the ovaries in response to electron irradiation and testing of radioprotective agents, such as platelet-rich plasma, remains relevant.

AIM: This study aimed to assess the inflammatory response in the ovary after platelet-rich plasma administration in a radiation-induced ovarian failure model.

MATERIALS AND METHODS: Fragments of the ovaries of four groups (I, control (n=10); II, fractional irradiation with electrons in a total dose of 20 Gy (n=10); III, fractional irradiation with electrons in a total dose of 20 Gy + platelet-rich plasma (n=10), and IV, platelet-rich plasma (n=10)) were studied histologically and immunohistochemically using antibodies to pro- (interleukin [IL]-1 and IL-6) and anti-inflammatory (IL-4, IL-10) cytokines, as well as CD3 and CD20.

RESULTS: The immunohistochemical study revealed that electron irradiation led to an increase in the expression of both pro- and anti-inflammatory cytokines and the number of CD3+ and CD20+ immunocompetent cells in the interstitial tissue of the ovaries, fractionally irradiated with electrons at a total dose of 20 Gy. The T-cell component was predominant over the B-cell component. Moreover, pre-irradiation administration of platelet-rich plasma contributed to a smaller change in the degree of morphological changes, expression of pro- (IL-1 and IL-6) and anti-inflammatory (IL-4 and IL-10) cytokines, and proportion of CD3+ and CD20+ immunocompetent cells in the interstitial tissue of the ovaries. In addition, the T-cell component of immunity was predominant.

CONCLUSION: Components of platelet-rich plasma, having anti-inflammatory and radioprotective properties, reduce the severity of inflammatory response (based on expression levels of pro- and anti-inflammatory cytokines) and number of T and Bimmunocompetent cells, which slow down the development of radiation-induced ovarian failure when exposed to fractional local irradiation with electrons in a total dose of 20 Gy.

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About the authors

Grigory A. Demyashkin

The First Sechenov Moscow State Medical University; National Medical Research Radiological Center of the Ministry of Health of the Russian Federation

Author for correspondence.
Email: dr.dga@mail.ru
ORCID iD: 0000-0001-8447-2600
SPIN-code: 5157-0177

MD, Dr. Sci. (Medicine)

Russian Federation, Moscow; Obninsk

Zaira M. Murtazalieva

The First Sechenov Moscow State Medical University

Email: ZARIA.ALIEVA.90@bk.ru
ORCID iD: 0009-0000-2361-7618
Russian Federation, Moscow

Ekaterina N. Pugacheva

The First Sechenov Moscow State Medical University

Email: rouzella@mail.ru
ORCID iD: 0009-0009-2268-3838
Russian Federation, Moscow

Matvey A. Vadyukhin

The First Sechenov Moscow State Medical University

Email: vma20@mail.ru
ORCID iD: 0000-0002-6235-1020
SPIN-code: 9485-7722
Russian Federation, Moscow

Milana M. Shukiurova

The First Sechenov Moscow State Medical University

Email: Milana.Shukyurova@gmail.com
ORCID iD: 0009-0009-7740-9190
Russian Federation, Moscow

Sergey N. Koryakin

National Medical Research Radiological Center of the Ministry of Health of the Russian Federation

Email: korsernic@mail.ru
ORCID iD: 0000-0003-0128-4538
SPIN-code: 8153-5789

Cand. Sci. (Biology)

Russian Federation, Obninsk

Arina A. Proskuriakova

The First Sechenov Moscow State Medical University

Email: proskuryakova-02@list.ru
ORCID iD: 0009-0002-7319-7492
Russian Federation, Moscow

References

  1. practice of radiation oncology: a narrative review. Ecancermedicalscience. 2022;16:1461. doi: 10.3332/ecancer.2022.1461
  2. Di Maggio FM, Minafra L, Forte GI, et al. Portrait of inflammatory response to ionizing radiation treatment. J Inflamm (Lond). 2015;12:14. doi: 10.1186/s12950-015-0058-3
  3. Linard C, Ropenga A, Vozenin-Brotons MC, et al. Abdominal irradiation increases inflammatory cytokine expression and activates NF-kappaB in rat ileal muscularis layer. Am J Physiol Gastrointest Liver Physiol. 2003;285(3): G556–G565. doi: 10.1152/ajpgi.00094.2003
  4. Fu Y, Wang Y, Du L, et al. Resveratrol inhibits ionising irradiation-induced inflammation in MSCs by activating SIRT1 and limiting NLRP-3 inflammasome activation. Int J Mol Sci. 2013;14(7):14105–14118. doi: 10.3390/ijms140714105
  5. Reisz JA, Bansal N, Qian J, Zhao W, Furdui CM. Effects of ionizing radiation on biological molecules — mechanisms of damage and emerging methods of detection. Antioxid Redox Signal. 2014;21(2):260–292. doi: 10.1089/ars.2013.5489
  6. Najafi M, Motevaseli E, Shirazi A, et al. Mechanisms of inflammatory responses to radiation and normal tissues toxicity: clinical implications. Int J Radiat Biol. 2018;94(4):335–356. doi: 10.1080/09553002.2018.1440092
  7. Yahyapour R, Motevaseli E, Rezaeyan A, et al. Reduction-oxidation (redox) system in radiation-induced normal tissue injury: molecular mechanisms and implications in radiation therapeutics. Clin Transl Oncol. 2018;20(8):975–988. doi: 10.1007/s12094-017-1828-6
  8. Mantawy EM, Said RS, Abdel-Aziz AK. Mechanistic approach of the inhibitory effect of chrysin on inflammatory and apoptotic events implicated in radiation-induced premature ovarian failure: emphasis on TGF-β/MAPKs signaling pathway. Biomed Pharmacother. 2019;109:293–303. doi: 10.1016/j.biopha.2018.10.092
  9. Du Y, Carranza Z, Luan Y, et al. Evidence of cancer therapy-induced chronic inflammation in the ovary across multiple species: a potential cause of persistent tissue damage and follicle depletion. J Reprod Immunol. 2022;150:103491. doi: 10.1016/j.jri.2022.103491
  10. Onder GO, Balcioglu E, Baran M, et al. The different doses of radiation therapy-induced damage to the ovarian environment in rats. Int J Radiat Biol. 2021;97(3):367–375. doi: 10.1080/09553002.2021.1864497
  11. Zhang Q, Wei Z, Weng H, et al. Folic Acid preconditioning alleviated radiation-induced ovarian dysfunction in female mice. Front Nutr. 2022;9:854655. doi: 10.3389/fnut.2022.854655
  12. Demyashkin GA, Vadyukhin MA, Shekin VI. The influence of platelet-derived growth factors on the proliferation of germinal epithelium after local irradiation with electrons. J Reprod Infertil. 2023;24(2):94–100. doi: 10.18502/jri.v24i2.12494
  13. Ozcan P, Takmaz T, Tok OE, et al. The protective effect of platelet-rich plasma administrated on ovarian function in female rats with Cy-induced ovarian damage. J Assist Reprod Genet. 2020;37(4):865–873. doi: 10.1007/s10815-020-01689-7
  14. Kim S, Kim SW, Han SJ, et al. Molecular mechanism and prevention strategy of chemotherapy- and radiotherapy-induced ovarian damage. Int J Mol Sci. 2021;22(14):7484. doi: 10.3390/ijms22147484
  15. Yahyapour R, Amini P, Rezapour S, et al. Radiation-induced inflammation and autoimmune diseases. Mil Med Res. 2018;5(1):9. doi: 10.1186/s40779-018-0156-7
  16. He L, Long X, Yu N, et al. Premature ovarian insufficiency (POI) induced by dynamic intensity modulated radiation therapy via P13K-AKT-FOXO3a in rat models. Biomed Res Int. 2021;2021:7273846. doi: 10.1155/2021/7273846
  17. Gato-Calvo L, Hermida-Gómez T, Romero CR, et al. Anti-inflammatory effects of novel standardized platelet rich plasma releasates on knee osteoarthritic chondrocytes and cartilage in vitro. Curr Pharm Biotechnol. 2019;20(11):920–933. doi: 10.2174/1389201020666190619111118
  18. Hashem HR. Regenerative and antioxidant properties of autologous platelet-rich plasma can reserve the aging process of the cornea in the rat model. Oxid Med Cell Longev. 2020;2020:4127959. doi: 10.1155/2020/4127959
  19. Abdul Ameer LA, Raheem ZJ, Abdulrazaq SS, et al. The anti-inflammatory effect of the platelet-rich plasma in the periodontal pocket. Eur J Dent. 2018;12(4):528–531. doi: 10.4103/ejd.ejd_49_18
  20. Li Y, Shao C, Zhou M, et al. Platelet-rich plasma improves lipopolysaccharide-induced inflammatory response by upgrading autophagy. European Journal of Inflammation. 2022;2022:20. doi: 10.1177/1721727X221112271
  21. Xu P, Wu Y, Zhou L, et al. Platelet-rich plasma accelerates skin wound healing by promoting re-epithelialization. Burns Trauma. 2020;8:tkaa028. doi: 10.1093/burnst/tkaa028

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2. Fig. 1. Ovaries of the control and experimental groups: on the left — hematoxylin and eosin (H&E) staining, ×200; in the center — immunohistochemical reactions with antibodies to the proinflammatory cytokine IL-1β, ×400; on the right — immunohistochemical reactions with antibodies to the anti-inflammatory cytokine IL-10, ×400. The scale bar is 25 µm. SD — summary dose, LP-PRP — leukocyte-poor platelet-rich plasma.

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3. Fig. 2. Ovaries of the control group (I), locally irradiated with electrons group (II) and pre-radiation LP-PRP group (III): on the left — immunohistochemical reactions with antibodies to CD3, ×400; on the right — immunohistochemical reactions with antibodies to CD20, ×400. The scale bar is 25 µm. SD — summary dose, LP-PRP — leukocyte-poor platelet-rich plasma.

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4. Fig. 3. Distribution of pro-inflammatory (IL-1β, IL-6) and anti-inflammatory (IL-4, IL-10) cytokines, as well as CD3+ and CD20+ lymphocytes in the ovaries of the control and experimental groups (%). SD — summary dose, LP-PRP — leukocyte-poor platelet-rich plasma. Data are presented as means ± standard error; * statistically significant differences compared to the control (p <0.05).

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