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Regulation of programmed-death ligand in the human head and neck squamous cell carcinoma microenvironment is mediated through matrix metalloproteinase-mediated proteolytic cleavage

  • Authors:
    • Mayuko Hira-Miyazawa
    • Hiroyuki Nakamura
    • Mariko Hirai
    • Yutaka Kobayashi
    • Hiroko Kitahara
    • George Bou-Gharios
    • Shuichi Kawashiri
  • View Affiliations / Copyright

    Affiliations: Department of Oral and Maxillofacial Surgery, Division of Cancer Medicine, Kanazawa University Graduate School of Medical Science, Kanazawa, Ishikawa 920-8640, Japan, Institute of Ageing and Chronic Disease, University of Liverpool, Liverpool L7 8TX, UK
    Copyright: © Hira-Miyazawa et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
  • Pages: 379-388
    |
    Published online on: December 11, 2017
       https://doi.org/10.3892/ijo.2017.4221
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Abstract

Recurrent and/or metastatic head and neck squamous cell carcinoma (R/M HNSCC) is a devastating malignancy with a poor prognosis. According to recent clinical studies, tumour growth can be effectively reduced and survival can be improved by blocking the programmed death receptor-1 (PD-1)/programmed death-ligand 1 (PD‑L1) pathway. PD-L1 expression has been proposed as a potential causative mechanism, as HNSCC is highly immunosuppressive. However, anti-PD-1 treatment is beneficial only for certain patients. Therefore, the mechanisms controlling PD-L1 expression warrant further investigation in order to provide a better understanding of the predicting efficacy of and optimising anti-PD-1 therapy, alone or in combination. In this study, PD-L1 protein extracted from the cell membrane was found to be downregulated in OSC-20 cells compared with OSC-19 cells, despite a higher PD-L1 expression in the total cell lysate of the OSC-20 compared with the OSC-19 cells. Several matrix metalloproteinases (MMPs) were found to be upregulated in HNSCC; in particular, MMP-7 and -13 were upregulated in the OSC-20 compared with the OSC-19 cells. Purified PD-L1 was degraded by recombinant MMP-13 and -7. The expression of PD-L1 was significantly restored by a specific inhibitor of MMP-13 (CL82198), which suggested the involvement of MMP-13 in the shedding/cleavage of PD-L1 in the OSC-20 cells. Among the anticancer drugs conventionally used in the treatment of patients with HNSCC, paclitaxel increased MMP-13 expression in R/M HNSCC cells (HOC313 cells) co-cultured without/with dendritic cells (DCs). These results suggest that the shedding/cleavage of PD-L1 by MMP-13 is one of the mechanisms behind the protective effect against invasion and metastasis. Thus, MMP-13 has potential value as a marker predictive of the decreased efficacy of anti-PD-1 therapy. In addition, paclitaxel is a particularly promising candidate for combination therapy in R/M HNSCC with anti-PD-1 therapy.
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View References

1 

Topalian SL, Hodi FS, Brahmer JR, Gettinger SN, Smith DC, McDermott DF, Powderly JD, Carvajal RD, Sosman JA, Atkins MB, et al: Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med. 366:2443–2454. 2012. View Article : Google Scholar : PubMed/NCBI

2 

Brahmer JR, Tykodi SS, Chow LQ, Hwu WJ, Topalian SL, Hwu P, Drake CG, Camacho LH, Kauh J, Odunsi K, et al: Safety and activity of anti-PD-L1 antibody in patients with advanced cancer. N Engl J Med. 366:2455–2465. 2012. View Article : Google Scholar : PubMed/NCBI

3 

Topalian SL, Drake CG and Pardoll DM: Targeting the PD-1/B7-H1(PD-L1) pathway to activate anti-tumor immunity. Curr Opin Immunol. 24:207–212. 2012. View Article : Google Scholar : PubMed/NCBI

4 

Freeman GJ, Long AJ, Iwai Y, Bourque K, Chernova T, Nishimura H, Fitz LJ, Malenkovich N, Okazaki T, Byrne MC, et al: Engagement of the PD-1 immunoinhibitory receptor by a novel B7 family member leads to negative regulation of lymphocyte activation. J Exp Med. 192:1027–1034. 2000. View Article : Google Scholar : PubMed/NCBI

5 

Oliveira-Neto HH, Gleber-Netto FO, de Sousa SF, França CM, Aguiar MC, Silva TA and Batista AC: A comparative study of microvessel density in squamous cell carcinoma of the oral cavity and lip. Oral Surg Oral Med Oral Pathol Oral Radiol. 113:391–398. 2012. View Article : Google Scholar : PubMed/NCBI

6 

Liang X, Zhou H, Liu X, He Y, Tang Y, Zhu G, Zheng M and Yang J: Effect of local hyperthermia on lymphangiogenic factors VEGF-C and -D in a nude mouse xenograft model of tongue squamous cell carcinoma. Oral Oncol. 46:111–115. 2010. View Article : Google Scholar

7 

Strome SE, Dong H, Tamura H, Voss SG, Flies DB, Tamada K, Salomao D, Cheville J, Hirano F, Lin W, et al: B7-H1 blockade augments adoptive T-cell immunotherapy for squamous cell carcinoma. Cancer Res. 63:6501–6505. 2003.PubMed/NCBI

8 

Lyford-Pike S, Peng S, Young GD, Taube JM, Westra WH, Akpeng B, Bruno TC, Richmon JD, Wang H, Bishop JA, et al: Evidence for a role of the PD-1:PD-L1 pathway in immune resistance of HPV-associated head and neck squamous cell carcinoma. Cancer Res. 73:1733–1741. 2013. View Article : Google Scholar : PubMed/NCBI

9 

Zandberg DP and Strome SE: The role of the PD-L1:PD-1 pathway in squamous cell carcinoma of the head and neck. Oral Oncol. 50:627–632. 2014. View Article : Google Scholar : PubMed/NCBI

10 

Butte MJ, Keir ME, Phamduy TB, Sharpe AH and Freeman GJ: Programmed death-1 ligand 1 interacts specifically with the B7-1 costimulatory molecule to inhibit T cell responses. Immunity. 27:111–122. 2007. View Article : Google Scholar : PubMed/NCBI

11 

Keir ME, Butte MJ, Freeman GJ and Sharpe AH: PD-1 and its ligands in tolerance and immunity. Annu Rev Immunol. 26:677–704. 2008. View Article : Google Scholar : PubMed/NCBI

12 

Dong H, Strome SE, Salomao DR, Tamura H, Hirano F, Flies DB, Roche PC, Lu J, Zhu G, Tamada K, et al: Tumor-associated B7-H1 promotes T-cell apoptosis: A potential mechanism of immune evasion. Nat Med. 8:793–800. 2002. View Article : Google Scholar : PubMed/NCBI

13 

Tsushima F, Tanaka K, Otsuki N, Youngnak P, Iwai H, Omura K and Azuma M: Predominant expression of B7-H1 and its immunoregulatory roles in oral squamous cell carcinoma. Oral Oncol. 42:268–274. 2006. View Article : Google Scholar

14 

Iwai Y, Terawaki S and Honjo T: PD-1 blockade inhibits hema-togenous spread of poorly immunogenic tumor cells by enhanced recruitment of effector T cells. Int Immunol. 17:133–144. 2005. View Article : Google Scholar

15 

Hirano F, Kaneko K, Tamura H, Dong H, Wang S, Ichikawa M, Rietz C, Flies DB, Lau JS, Zhu G, et al: Blockade of B7-H1 and PD-1 by monoclonal antibodies potentiates cancer therapeutic immunity. Cancer Res. 65:1089–1096. 2005.PubMed/NCBI

16 

Hirai M, Kitahara H, Kobayashi Y, Kato K, Bou-Gharios G, Nakamura H and Kawashiri S: Regulation of PD-L1 expression in a high-grade invasive human oral squamous cell carcinoma microenvironment. Int J Oncol. 50:41–48. 2017. View Article : Google Scholar

17 

Dezutter-Dambuyant C, Durand I, Alberti L, Bendriss-Vermare N, Valladeau-Guilemond J, Duc A, Magron A, Morel AP, Sisirak V, Rodriguez C, et al: A novel regulation of PD-1 ligands on mesenchymal stromal cells through MMP-mediated proteolytic cleavage. Oncoimmunology. 5:e10911462015. View Article : Google Scholar

18 

Egeblad M and Werb Z: New functions for the matrix metal-loproteinases in cancer progression. Nat Rev Cancer. 2:161–174. 2002. View Article : Google Scholar : PubMed/NCBI

19 

Overall CM and López-Otín C: Strategies for MMP inhibition in cancer: Innovations for the post-trial era. Nat Rev Cancer. 2:657–672. 2002. View Article : Google Scholar : PubMed/NCBI

20 

Milner JM and Cawston TE: Matrix metalloproteinase knockout studies and the potential use of matrix metalloproteinase inhibitors in the rheumatic diseases. Curr Drug Targets Inflamm Allergy. 4:363–375. 2005. View Article : Google Scholar : PubMed/NCBI

21 

Le NT, Xue M, Castelnoble LA and Jackson CJ: The dual personalities of matrix metalloproteinases in inflammation. Front Biosci. 12:1475–1487. 2007. View Article : Google Scholar

22 

Yokoi T, Hirata S, Nishimura F, Miyakawa A, Odajima T and Kohama G: Some properties of a newly established human cell line derived from an oral squamous carcinoma. Tumor Res. 25:93-91–93. 1990.

23 

Yokoi T, Homma H and Odajima T: Establishment and characterization of OSC-19 cell line in serum and protein free culture. Tumor Res. 24:1–17. 1988.

24 

Ishisaki A, Oida S, Momose F, Amagasa T, Rikimaru K, Ichijo H and Sasaki S: Identification and characterization of autocrine-motility-factor-like activity in oral squamous-cell-carcinoma cells. Int J Cancer. 59:783–788. 1994. View Article : Google Scholar : PubMed/NCBI

25 

Arrighi JF, Hauser C, Chapuis B, Zubler RH and Kindler V: Long-term culture of human CD34(+) progenitors with FLT3-ligand, thrombopoietin, and stem cell factor induces extensive amplification of a CD34(−)CD14(−) and a CD34(−) CD14(+) dendritic cell precursor. Blood. 93:2244–2252. 1999.PubMed/NCBI

26 

Yang D, Chen Q, Le Y, Wang JM and Oppenheim JJ: Differential regulation of formyl peptide receptor-like 1 expression during the differentiation of monocytes to dendritic cells and macrophages. J Immunol. 166:4092–4098. 2001. View Article : Google Scholar : PubMed/NCBI

27 

Livak KJ and Schmittgen TD: Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) Method. Methods. 25:402–408. 2001. View Article : Google Scholar

28 

Nakamura H, Fujii Y, Ohuchi E, Yamamoto E and Okada Y: Activation of the precursor of human stromelysin 2 and its interactions with other matrix metalloproteinases. Eur J Biochem. 253:67–75. 1998. View Article : Google Scholar : PubMed/NCBI

29 

Nakamura H, Fujii Y, Inoki I, Sugimoto K, Tanzawa K, Matsuki H, Miura R, Yamaguchi Y and Okada Y: Brevican is degraded by matrix metalloproteinases and aggrecanase-1 (ADAMTS4) at different sites. J Biol Chem. 275:38885–38890. 2000. View Article : Google Scholar : PubMed/NCBI

30 

Zou W and Chen L: Inhibitory B7-family molecules in the tumour microenvironment. Nat Rev Immunol. 8:467–477. 2008. View Article : Google Scholar : PubMed/NCBI

31 

Wintterle S, Schreiner B, Mitsdoerffer M, Schneider D, Chen L, Meyermann R, Weller M and Wiendl H: Expression of the B7-related molecule B7-H1 by glioma cells: A potential mechanism of immune paralysis. Cancer Res. 63:7462–7467. 2003.PubMed/NCBI

32 

Konishi J, Yamazaki K, Azuma M, Kinoshita I, Dosaka-Akita H and Nishimura M: B7-H1 expression on non-small cell lung cancer cells and its relationship with tumor-infiltrating lymphocytes and their PD-1 expression. Clin Cancer Res. 10:5094–5100. 2004. View Article : Google Scholar : PubMed/NCBI

33 

Ohigashi Y, Sho M, Yamada Y, Tsurui Y, Hamada K, Ikeda N, Mizuno T, Yoriki R, Kashizuka H, Yane K, et al: Clinical significance of programmed death-1 ligand-1 and programmed death-1 ligand-2 expression in human esophageal cancer. Clin Cancer Res. 11:2947–2953. 2005. View Article : Google Scholar : PubMed/NCBI

34 

Thompson RH and Kwon ED: Significance of B7-H1 overexpression in kidney cancer. Clin Genitourin Cancer. 5:206–211. 2006. View Article : Google Scholar

35 

Hamanishi J, Mandai M, Iwasaki M, Okazaki T, Tanaka Y, Yamaguchi K, Higuchi T, Yagi H, Takakura K, Minato N, et al: Programmed cell death 1 ligand 1 and tumor-infiltrating CD8+ T lymphocytes are prognostic factors of human ovarian cancer. Proc Natl Acad Sci USA. 104:3360–3365. 2007. View Article : Google Scholar

36 

Nomi T, Sho M, Akahori T, Hamada K, Kubo A, Kanehiro H, Nakamura S, Enomoto K, Yagita H, Azuma M, et al: Clinical significance and therapeutic potential of the programmed death-1 ligand/programmed death-1 pathway in human pancreatic cancer. Clin Cancer Res. 13:2151–2157. 2007. View Article : Google Scholar : PubMed/NCBI

37 

Ghebeh H, Tulbah A, Mohammed S, Elkum N, Bin Amer SM, Al-Tweigeri T and Dermime S: Expression of B7-H1 in breast cancer patients is strongly associated with high proliferative Ki-67-expressing tumor cells. Int J Cancer. 121:751–758. 2007. View Article : Google Scholar : PubMed/NCBI

38 

Yao Y, Tao R, Wang X, Wang Y, Mao Y and Zhou LF: B7-H1 is correlated with malignancy-grade gliomas but is not expressed exclusively on tumor stem-like cells. Neuro Oncol. 11:757–766. 2009. View Article : Google Scholar : PubMed/NCBI

39 

Liotta LA and Kohn EC: The microenvironment of the tumour-host interface. Nature. 411:375–379. 2001. View Article : Google Scholar : PubMed/NCBI

40 

Shiomi T and Okada Y: MT1-MMP and MMP-7 in invasion and metastasis of human cancers. Cancer Metastasis Rev. 22:145–152. 2003. View Article : Google Scholar : PubMed/NCBI

41 

Deryugina EI and Quigley JP: Matrix metalloproteinases and tumor metastasis. Cancer Metastasis Rev. 25:9–34. 2006. View Article : Google Scholar : PubMed/NCBI

42 

Cornelius LA, Nehring LC, Harding E, Bolanowski M, Welgus HG, Kobayashi DK, Pierce RA and Shapiro SD: Matrix metalloproteinases generate angiostatin: Effects on neovascularization. J Immunol. 161:6845–6852. 1998.PubMed/NCBI

43 

Hamano Y, Zeisberg M, Sugimoto H, Lively JC, Maeshima Y, Yang C, Hynes RO, Werb Z, Sudhakar A and Kalluri R: Physiological levels of tumstatin, a fragment of collagen IV alpha3 chain, are generated by MMP-9 proteolysis and suppress angiogenesis via alphaV beta3 integrin. Cancer Cell. 3:589–601. 2003. View Article : Google Scholar : PubMed/NCBI

44 

Fukuda H, Mochizuki S, Abe H, Okano HJ, Hara-Miyauchi C, Okano H, Yamaguchi N, Nakayama M, D'Armiento J and Okada Y: Host-derived MMP-13 exhibits a protective role in lung metastasis of melanoma cells by local endostatin production. Br J Cancer. 105:1615–1624. 2011. View Article : Google Scholar : PubMed/NCBI

45 

Itoh T, Tanioka M, Yoshida H, Yoshioka T, Nishimoto H and Itohara S: Reduced angiogenesis and tumor progression in gela-tinase A-deficient mice. Cancer Res. 58:1048–1051. 1998.PubMed/NCBI

46 

Wilson CL, Heppner KJ, Labosky PA, Hogan BL and Matrisian LM: Intestinal tumorigenesis is suppressed in mice lacking the metalloproteinase matrilysin. Proc Natl Acad Sci USA. 94:1402–1407. 1997. View Article : Google Scholar : PubMed/NCBI

47 

Itoh T, Tanioka M, Matsuda H, Nishimoto H, Yoshioka T, Suzuki R and Uehira M: Experimental metastasis is suppressed in MMP-9-deficient mice. Clin Exp Metastasis. 17:177–181. 1999. View Article : Google Scholar : PubMed/NCBI

48 

Acuff HB, Carter KJ, Fingleton B, Gorden DL and Matrisian LM: Matrix metalloproteinase-9 from bone marrow-derived cells contributes to survival but not growth of tumor cells in the lung microenvironment. Cancer Res. 66:259–266. 2006. View Article : Google Scholar : PubMed/NCBI

49 

McCawley LJ, Crawford HC, King LE Jr, Mudgett J and Matrisian LM: A protective role for matrix metalloproteinase-3 in squamous cell carcinoma. Cancer Res. 64:6965–6972. 2004. View Article : Google Scholar : PubMed/NCBI

50 

Acuff HB, Sinnamon M, Fingleton B, Boone B, Levy SE, Chen X, Pozzi A, Carbone DP, Schwartz DR, Moin K, et al: Analysis of host- and tumor-derived proteinases using a custom dual species microarray reveals a protective role for stromal matrix metal-loproteinase-12 in non-small cell lung cancer. Cancer Res. 66:7968–7975. 2006. View Article : Google Scholar : PubMed/NCBI

51 

Balbín M, Fueyo A, Tester AM, Pendás AM, Pitiot AS, Astudillo A, Overall CM, Shapiro SD and López-Otín C: Loss of collagenase-2 confers increased skin tumor susceptibility to male mice. Nat Genet. 35:252–257. 2003. View Article : Google Scholar : PubMed/NCBI

52 

Kitahara H, Hirai M, Kato K, Bou-Gharios G, Nakamura H and Kawashiri S: Eribulin sensitizes oral squamous cell carcinoma cells to cetuximab via induction of mesenchymal-to-epithelial transition. Oncol Rep. 36:3139–3144. 2016. View Article : Google Scholar : PubMed/NCBI

53 

Dezső Z, Oestreicher J, Weaver A, Santiago S, Agoulnik S, Chow J, Oda Y and Funahashi Y: Gene expression profiling reveals epithelial mesenchymal transition (EMT) genes can selectively differentiate eribulin sensitive breast cancer cells. PLoS One. 9:e1061312014. View Article : Google Scholar

54 

Kavallaris M: Microtubules and resistance to tubulin-binding agents. Nat Rev Cancer. 10:194–204. 2010. View Article : Google Scholar : PubMed/NCBI

55 

Dong C, Li Z, Alvarez R Jr, Feng XH and Goldschmidt-Clermont PJ: Microtubule binding to Smads may regulate TGF-beta activity. Mol Cell. 5:27–34. 2000. View Article : Google Scholar : PubMed/NCBI

56 

Leivonen SK, Ala-Aho R, Koli K, Grénman R, Peltonen J and Kähäri VM: Activation of Smad signaling enhances collagenase-3 (MMP-13) expression and invasion of head and neck squamous carcinoma cells. Oncogene. 25:2588–2600. 2006. View Article : Google Scholar : PubMed/NCBI

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Copy and paste a formatted citation
Spandidos Publications style
Hira-Miyazawa M, Nakamura H, Hirai M, Kobayashi Y, Kitahara H, Bou-Gharios G and Kawashiri S: Regulation of programmed-death ligand in the human head and neck squamous cell carcinoma microenvironment is mediated through matrix metalloproteinase-mediated proteolytic cleavage. Int J Oncol 52: 379-388, 2018.
APA
Hira-Miyazawa, M., Nakamura, H., Hirai, M., Kobayashi, Y., Kitahara, H., Bou-Gharios, G., & Kawashiri, S. (2018). Regulation of programmed-death ligand in the human head and neck squamous cell carcinoma microenvironment is mediated through matrix metalloproteinase-mediated proteolytic cleavage. International Journal of Oncology, 52, 379-388. https://doi.org/10.3892/ijo.2017.4221
MLA
Hira-Miyazawa, M., Nakamura, H., Hirai, M., Kobayashi, Y., Kitahara, H., Bou-Gharios, G., Kawashiri, S."Regulation of programmed-death ligand in the human head and neck squamous cell carcinoma microenvironment is mediated through matrix metalloproteinase-mediated proteolytic cleavage". International Journal of Oncology 52.2 (2018): 379-388.
Chicago
Hira-Miyazawa, M., Nakamura, H., Hirai, M., Kobayashi, Y., Kitahara, H., Bou-Gharios, G., Kawashiri, S."Regulation of programmed-death ligand in the human head and neck squamous cell carcinoma microenvironment is mediated through matrix metalloproteinase-mediated proteolytic cleavage". International Journal of Oncology 52, no. 2 (2018): 379-388. https://doi.org/10.3892/ijo.2017.4221
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Spandidos Publications style
Hira-Miyazawa M, Nakamura H, Hirai M, Kobayashi Y, Kitahara H, Bou-Gharios G and Kawashiri S: Regulation of programmed-death ligand in the human head and neck squamous cell carcinoma microenvironment is mediated through matrix metalloproteinase-mediated proteolytic cleavage. Int J Oncol 52: 379-388, 2018.
APA
Hira-Miyazawa, M., Nakamura, H., Hirai, M., Kobayashi, Y., Kitahara, H., Bou-Gharios, G., & Kawashiri, S. (2018). Regulation of programmed-death ligand in the human head and neck squamous cell carcinoma microenvironment is mediated through matrix metalloproteinase-mediated proteolytic cleavage. International Journal of Oncology, 52, 379-388. https://doi.org/10.3892/ijo.2017.4221
MLA
Hira-Miyazawa, M., Nakamura, H., Hirai, M., Kobayashi, Y., Kitahara, H., Bou-Gharios, G., Kawashiri, S."Regulation of programmed-death ligand in the human head and neck squamous cell carcinoma microenvironment is mediated through matrix metalloproteinase-mediated proteolytic cleavage". International Journal of Oncology 52.2 (2018): 379-388.
Chicago
Hira-Miyazawa, M., Nakamura, H., Hirai, M., Kobayashi, Y., Kitahara, H., Bou-Gharios, G., Kawashiri, S."Regulation of programmed-death ligand in the human head and neck squamous cell carcinoma microenvironment is mediated through matrix metalloproteinase-mediated proteolytic cleavage". International Journal of Oncology 52, no. 2 (2018): 379-388. https://doi.org/10.3892/ijo.2017.4221
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