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Article

Sonodynamic therapy improves anti‑tumor immune effect by increasing the infiltration of CD8+ T cells and altering tumor blood vessels in murine B16F10 melanoma xenograft

  • Authors:
    • Yan Peng
    • Limin Jia
    • Shan Wang
    • Wenwu Cao
    • Jinhua Zheng
  • View Affiliations / Copyright

    Affiliations: Department of Anatomy, Basic Medical Science College, Harbin Medical University, Harbin, Heilongjiang 150081, P.R. China, Department of Anatomy, Basic Medical Science College, Harbin Medical University, Harbin, Heilongjiang 150081, P.R. China, Department of Oral Pathology, Stomatological Hospital, Harbin Medical University, Harbin, Heilongjiang 150001, P.R. China, Condensed Matter Science and Technology Institute, and Department of Physics, Harbin Institute of Technology, Harbin, Heilongjiang 150080, P.R. China
  • Pages: 2163-2170
    |
    Published online on: August 1, 2018
       https://doi.org/10.3892/or.2018.6612
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Abstract

Sonodynamic therapy (SDT) uses a combination of sonosensitizers and low‑intensity therapeutic ultrasound to destroy tumor cells. However, its effects on the tumor microenvironment, particularly on the immune state, remain unknown. The purpose of the present study was to examine the capacity and potency of the antitumor immunity induced by SDT. In the present study, sonosensitizer, 5‑aminolevulinic acid (5‑ALA), and/or ultrasound (US) were used to treat mouse B16F10 melanoma xenograft (1.0 MHz, 0.8 W/cm2, 10% duty cycle) and human umbilical vein endothelial cells (HUVECs; 0.87 MHz, 0.6 W/cm2, 60% duty cycle). Various immune cells, and proteins associated with the immunoregulation such as forkhead Box P3 (Foxp3), cytotoxic T‑lymphocyte associated protein 4 (CTLA‑4), and CD80 were detected by immunofluorescence staining and western blotting. The effect of SDT on blood vessels which were located in the central and peripheral area of tumor tissues was observed by transmission electron microscopy, immunohistochemical and immunofluorescence staining. The effect of SDT on intercellular adhesion molecule‑1 (ICAM‑1) expression on HUVECs was detected by western blotting and reverse transcription‑semi‑quantitative polymerase chain reaction. The results revealed that SDT inhibited tumor growth and improved outcomes. The mean inhibition rate of tumor volume in the US + ALA group was 43.8% and median survival was 45 days in US + ALA group vs. 27.5 days in the control group. SDT increased the number of CD45+ cells, in particular CD8+ and CD68+ cells and upregulated the expression of CD80 in the tumor tissues. The expression levels of Foxp3 and CTLA‑4 were downregulated following SDT. The endothelial cells of tumor central were damaged, but the lumen area of the tumor peripheral vessels (TPVs) and the expression of ICAM‑1 on HUVECs were increased after SDT. The results indicated that SDT improved the outcomes of melanoma‑loading mice, increased the infiltration of CD8+ T cells and downregulates the expression of Foxp3 and CTLA‑4 in mouse melanoma tissues. Furthermore, SDT increased the lumen area of TPVs in murine xenograft and the expression of ICAM‑1 on HUVECs, which may be beneficial to the transendothelial migration of immune cells and the anti‑tumor immune response.
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1 

Rosenthal I, Sostaric JZ and Riesz P: Sonodynamic therapy - a review of the synergistic effects of drugs and ultrasound. Ultrason Sonochem. 11:349–363. 2004.PubMed/NCBI

2 

Shibaguchi H, Tsuru H and Kuroki M and Kuroki M: Sonodynamic cancer therapy: A non-invasive and repeatable approach using low-intensity ultrasound with a sonosensitizer. Anticancer Res. 31:2425–2429. 2011.PubMed/NCBI

3 

Li Y, Wang P, Zhao P, Zhu S, Wang X and Liu Q: Apoptosis induced by sonodynamic treatment by protoporphyrin IX on MDA-MB-231 cells. Ultrasonics. 52:490–496. 2012. View Article : Google Scholar : PubMed/NCBI

4 

Wang X, Leung AW, Jiang Y, Yu H, Li X and Xu C: Hypocrellin B-mediated sonodynamic action induces apoptosis of hepatocellular carcinoma cells. Ultrasonics. 52:543–546. 2012. View Article : Google Scholar : PubMed/NCBI

5 

Wang X, Liu Q, Wang Z, Wang P, Zhao P, Zhao X, Yang L and Li Y: Role of autophagy in sonodynamic therapy-induced cytotoxicity in S180 cells. Ultrasound Med Biol. 36:1933–1946. 2010. View Article : Google Scholar : PubMed/NCBI

6 

Su X, Wang P, Yang S, Zhang K, Liu Q and Wang X: Sonodynamic therapy induces the interplay between apoptosis and autophagy in K562 cells through ROS. Int J Biochem Cell Biol. 60:82–92. 2015. View Article : Google Scholar : PubMed/NCBI

7 

Lv Y, Zheng J, Zhou Q, Jia L, Wang C, Liu N, Zhao H, Ji H, Li B and Cao W: Antiproliferative and Apoptosis-inducing effect of exo-Protoporphyrin IX based sonodynamic therapy on human oral squamous cell carcinoma. Sci Rep. 7:409672017. View Article : Google Scholar : PubMed/NCBI

8 

Hu Z, Fan H, Lv G, Zhou Q, Yang B, Zheng J and Cao W: 5-Aminolevulinic acid-mediated sonodynamic therapy induces anti-tumor effects in malignant melanoma via p53-miR-34a-Sirt1 axis. J Dermatol Sci. 79:155–162. 2015. View Article : Google Scholar : PubMed/NCBI

9 

Li Y, Zhou Q, Hu Z, Yang B, Li Q, Wang J, Zheng J and Cao W: 5-Aminolevulinic acid-based sonodynamic therapy induces the apoptosis of osteosarcoma in mice. PLoS One. 10:e01320742015. View Article : Google Scholar : PubMed/NCBI

10 

Gao Z, Zheng J, Yang B, Wang Z, Fan H, Lv Y, Li H, Jia L and Cao W: Sonodynamic therapy inhibits angiogenesis and tumor growth in a xenograft mouse model. Cancer Lett. 335:93–99. 2013. View Article : Google Scholar : PubMed/NCBI

11 

Wang S, Hu Z, Wang X, Gu C, Gao Z, Cao W and Zheng J: 5-Aminolevulinic acid-mediated sonodynamic therapy reverses macrophage and dendritic cell passivity in murine melanoma xenografts. Ultrasound Med Biol. 40:2125–2133. 2014. View Article : Google Scholar : PubMed/NCBI

12 

Rosenberg SA, Spiess P and Lafreniere R: A new approach to the adoptive immunotherapy of cancer with tumor-infiltrating lymphocytes. Science. 233:1318–1321. 1986. View Article : Google Scholar : PubMed/NCBI

13 

Griffith KD, Read EJ, Carrasquillo JA, Carter CS, Yang JC, Fisher B, Aebersold P, Packard BS, Yu MY and Rosenberg SA: In vivo distribution of adoptively transferred indium-111-labeled tumor infiltrating lymphocytes and peripheral blood lymphocytes in patients with metastatic melanoma. J Natl Cancer Inst. 81:1709–1717. 1989. View Article : Google Scholar : PubMed/NCBI

14 

Balkwill F, Charles KA and Mantovani A: Smoldering and polarized inflammation in the initiation and promotion of malignant disease. Cancer Cell. 7:211–217. 2005. View Article : Google Scholar : PubMed/NCBI

15 

Galon J, Mlecnik B, Bindea G, Angell HK, Berger A, Lagorce C, Lugli A, Zlobec I, Hartmann A, Bifulco C, et al: Towards the introduction of the ‘Immunoscore’ in the classification of malignant tumours. J Pathol. 232:199–209. 2014. View Article : Google Scholar : PubMed/NCBI

16 

Lv Y, Fang M, Zheng J, Yang B, Li H, Xiuzigao Z, Song W, Chen Y and Cao W: Low-intensity ultrasound combined with 5-aminolevulinic acid administration in the treatment of human tongue squamous carcinoma. Cell Physiol Biochem. 30:321–333. 2012. View Article : Google Scholar : PubMed/NCBI

17 

Tanchot C, Terme M, Pere H, Tran T, Benhamouda N, Strioga M, Banissi C, Galluzzi L, Kroemer G and Tartour E: Tumor-infiltrating regulatory T cells: Phenotype, role, mechanism of expansion in situ and clinical significance. Cancer Microenviron. 6:147–157. 2013. View Article : Google Scholar : PubMed/NCBI

18 

Zhang L and Zhao Y: The regulation of Foxp3 expression in regulatory CD4(+)CD25(+)T cells: Multiple pathways on the road. J Cell Physiol. 211:590–597. 2007. View Article : Google Scholar : PubMed/NCBI

19 

Marson A, Kretschmer K, Frampton GM, Jacobsen ES, Polansky JK, MacIsaac KD, Levine SS, Fraenkel E, von Boehmer H and Young RA: Foxp3 occupancy and regulation of key target genes during T-cell stimulation. Nature. 445:931–935. 2007. View Article : Google Scholar : PubMed/NCBI

20 

Son CH, Bae JH, Shin DY, Lee HR, Choi YJ, Jo WS, Jung Ho M, Kang CD, Yang K and Park YS: CTLA-4 blockade enhances antitumor immunity of intratumoral injection of immature dendritic cells into irradiated tumor in a mouse colon cancer model. J Immunother. 37:1–7. 2014. View Article : Google Scholar : PubMed/NCBI

21 

Sharpe AH: Mechanisms of costimulation. Immunol Rev. 229:5–11. 2009. View Article : Google Scholar : PubMed/NCBI

22 

Mauri D and Pichler WJ: Involvement of CD80 in the generation of CD4+ cytotoxic T cells. Immunol Res. 15:126–140. 1996. View Article : Google Scholar : PubMed/NCBI

23 

Carriere V, Colisson R, Jiguet-Jiglaire C, Bellard E, Bouche G, Al Saati T, Amalric F, Girard JP and M'Rini C: Cancer cells regulate lymphocyte recruitment and leukocyte-endothelium interactions in the tumor-draining lymph node. Cancer Res. 65:11639–11648. 2005. View Article : Google Scholar : PubMed/NCBI

24 

Griffioen AW, Damen CA, Martinotti S, Blijham GH and Groenewegen G: Endothelial intercellular adhesion molecule-1 expression is suppressed in human malignancies: The role of angiogenic factors. Cancer Res. 56:1111–1117. 1996.PubMed/NCBI

25 

Bandyopadhyay S, Quinn TJ, Scandiuzzi L, Basu I, Partanen A, Tomé WA, Macian F and Guha C: Low-intensity focused ultrasound induces reversal of tumor-induced T cell tolerance and prevents immune escape. J Immunol. 196:1964–1976. 2016. View Article : Google Scholar : PubMed/NCBI

26 

Liu HL, Hsieh HY, Lu LA, Kang CW, Wu MF and Lin CY: Low-pressure pulsed focused ultrasound with microbubbles promotes an anticancer immunological response. J Transl Med. 10:2212012. View Article : Google Scholar : PubMed/NCBI

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Copy and paste a formatted citation
Spandidos Publications style
Peng Y, Jia L, Wang S, Cao W and Zheng J: Sonodynamic therapy improves anti‑tumor immune effect by increasing the infiltration of CD8+ T cells and altering tumor blood vessels in murine B16F10 melanoma xenograft. Oncol Rep 40: 2163-2170, 2018.
APA
Peng, Y., Jia, L., Wang, S., Cao, W., & Zheng, J. (2018). Sonodynamic therapy improves anti‑tumor immune effect by increasing the infiltration of CD8+ T cells and altering tumor blood vessels in murine B16F10 melanoma xenograft. Oncology Reports, 40, 2163-2170. https://doi.org/10.3892/or.2018.6612
MLA
Peng, Y., Jia, L., Wang, S., Cao, W., Zheng, J."Sonodynamic therapy improves anti‑tumor immune effect by increasing the infiltration of CD8+ T cells and altering tumor blood vessels in murine B16F10 melanoma xenograft". Oncology Reports 40.4 (2018): 2163-2170.
Chicago
Peng, Y., Jia, L., Wang, S., Cao, W., Zheng, J."Sonodynamic therapy improves anti‑tumor immune effect by increasing the infiltration of CD8+ T cells and altering tumor blood vessels in murine B16F10 melanoma xenograft". Oncology Reports 40, no. 4 (2018): 2163-2170. https://doi.org/10.3892/or.2018.6612
Copy and paste a formatted citation
x
Spandidos Publications style
Peng Y, Jia L, Wang S, Cao W and Zheng J: Sonodynamic therapy improves anti‑tumor immune effect by increasing the infiltration of CD8+ T cells and altering tumor blood vessels in murine B16F10 melanoma xenograft. Oncol Rep 40: 2163-2170, 2018.
APA
Peng, Y., Jia, L., Wang, S., Cao, W., & Zheng, J. (2018). Sonodynamic therapy improves anti‑tumor immune effect by increasing the infiltration of CD8+ T cells and altering tumor blood vessels in murine B16F10 melanoma xenograft. Oncology Reports, 40, 2163-2170. https://doi.org/10.3892/or.2018.6612
MLA
Peng, Y., Jia, L., Wang, S., Cao, W., Zheng, J."Sonodynamic therapy improves anti‑tumor immune effect by increasing the infiltration of CD8+ T cells and altering tumor blood vessels in murine B16F10 melanoma xenograft". Oncology Reports 40.4 (2018): 2163-2170.
Chicago
Peng, Y., Jia, L., Wang, S., Cao, W., Zheng, J."Sonodynamic therapy improves anti‑tumor immune effect by increasing the infiltration of CD8+ T cells and altering tumor blood vessels in murine B16F10 melanoma xenograft". Oncology Reports 40, no. 4 (2018): 2163-2170. https://doi.org/10.3892/or.2018.6612
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