リケラボ論文検索は、全国の大学リポジトリにある学位論文・教授論文を一括検索できる論文検索サービスです。

リケラボ 全国の大学リポジトリにある学位論文・教授論文を一括検索するならリケラボ論文検索大学・研究所にある論文を検索できる

リケラボ 全国の大学リポジトリにある学位論文・教授論文を一括検索するならリケラボ論文検索大学・研究所にある論文を検索できる

大学・研究所にある論文を検索できる 「Matrix Metalloproteinase 9 Induced in Esophageal Squamous Cell Carcinoma Cells via Close Contact with Tumor-Associated Macrophages Contributes to Cancer Progression and Poor Prognosis」の論文概要。リケラボ論文検索は、全国の大学リポジトリにある学位論文・教授論文を一括検索できる論文検索サービスです。

コピーが完了しました

URLをコピーしました

論文の公開元へ論文の公開元へ
書き出し

Matrix Metalloproteinase 9 Induced in Esophageal Squamous Cell Carcinoma Cells via Close Contact with Tumor-Associated Macrophages Contributes to Cancer Progression and Poor Prognosis

Tsukamoto, Shuichi Koma, Yu-ichiro Kitamura, Yu Tanigawa, Kohei Azumi, Yuki Miyako, Shoji Urakami, Satoshi Hosono, Masayoshi Kodama, Takayuki Nishio, Mari Shigeoka, Manabu Yokozaki, Hiroshi 神戸大学

2023.06

概要

Tumor-associated macrophages (TAMs) contribute to disease progression in various cancers, including esophageal squamous cell carcinoma (ESCC). We have previously used an indirect co-culture system between ESCC cell lines and macrophages to analyze their interactions. Recently, we established a direct co-culture system to closely simulate actual ESCC cell-TAM contact. We found that matrix metalloproteinase 9 (MMP9) was induced in ESCC cells by direct co-culture with TAMs, not by indirect co-culture. MMP9 was associated with ESCC cell migration and invasion, and its expression was controlled by the Stat3 signaling pathway in vitro. Immunohistochemical analyses revealed that MMP9 expression in cancer cells at the invasive front (“cancer cell MMP9”) was related to high infiltration of CD204 positive M2-like TAMs (p < 0.001) and was associated with worse overall and disease-free survival of patients (p = 0.036 and p = 0.038, respectively). Furthermore, cancer cell MMP9 was an independent prognostic factor for disease-free survival. Notably, MMP9 expression in cancer stroma was not associated with any clinicopathological factors or patient prognoses. Our results suggest that close interaction with TAMs infiltrating in cancer stroma or cancer nests induces MMP9 expression in ESCC cells, equipping them with more malignant features.

この論文で使われている画像

関連論文

参考文献

1.

2.

3.

Sheikh, M.; Roshandel, G.; McCormack, V.; Malekzadeh, R. Current Status and Future Prospects for Esophageal Cancer. Cancers

2023, 15, 765. [CrossRef] [PubMed]

Cancer Statistics. Cancer Information Service, National Cancer Center, Japan (National Cancer Registry, Ministry of Health, Labour

and Welfare). Available online: https://ganjoho.jp/reg_stat/statistics/data/dl/index.html#a14 (accessed on 24 February 2023).

Watanabe, M.; Toh, Y.; Ishihara, R.; Kono, K.; Matsubara, H.; Miyazaki, T.; Morita, M.; Murakami, K.; Muro, K.; Numasaki, H.;

et al. Comprehensive registry of esophageal cancer in Japan, 2015. Esophagus Off. J. Jpn. Esophageal Soc. 2023, 20, 1–28. [CrossRef]

[PubMed]

Cancers 2023, 15, 2987

4.

5.

6.

7.

8.

9.

10.

11.

12.

13.

14.

15.

16.

17.

18.

19.

20.

21.

22.

23.

24.

25.

26.

21 of 23

Shimada, H.; Nabeya, Y.; Okazumi, S.-I.; Matsubara, H.; Shiratori, T.; Gunji, Y.; Kobayashi, S.; Hayashi, H.; Ochiai, T. Prediction of

survival with squamous cell carcinoma antigen in patients with resectable esophageal squamous cell carcinoma. Surgery 2003,

133, 486–494. [CrossRef] [PubMed]

Komohara, Y.; Fujiwara, Y.; Ohnishi, K.; Takeya, M. Tumor-associated macrophages: Potential therapeutic targets for anti-cancer

therapy. Adv. Drug Deliv. Rev. 2016, 99, 180–185. [CrossRef]

Shigeoka, M.; Urakawa, N.; Nakamura, T.; Nishio, M.; Watajima, T.; Kuroda, D.; Komori, T.; Kakeji, Y.; Semba, S.; Yokozaki, H.

Tumor associated macrophage expressing CD204 is associated with tumor aggressiveness of esophageal squamous cell carcinoma.

Cancer Sci. 2013, 104, 1112–1119. [CrossRef]

Urakawa, N.; Utsunomiya, S.; Nishio, M.; Shigeoka, M.; Takase, N.; Arai, N.; Kakeji, Y.; Koma, Y.-I.; Yokozaki, H. GDF15 derived

from both tumor-associated macrophages and esophageal squamous cell carcinomas contributes to tumor progression via Akt

and Erk pathways. Lab. Investig. 2015, 95, 491–503. [CrossRef]

Hosono, M.; Koma, Y.-I.; Takase, N.; Urakawa, N.; Higashino, N.; Suemune, K.; Kodaira, H.; Nishio, M.; Shigeoka, M.; Kakeji,

Y.; et al. CXCL8 derived from tumor-associated macrophages and esophageal squamous cell carcinomas contributes to tumor

progression by promoting migration and invasion of cancer cells. Oncotarget 2017, 8, 106071–106088. [CrossRef]

Fujikawa, M.; Koma, Y.-I.; Hosono, M.; Urakawa, N.; Tanigawa, K.; Shimizu, M.; Kodama, T.; Sakamoto, H.; Nishio, M.; Shigeoka,

M.; et al. Chemokine (C-C Motif) Ligand 1 Derived from Tumor-Associated Macrophages Contributes to Esophageal Squamous

Cell Carcinoma Progression via CCR8-Mediated Akt/Proline-Rich Akt Substrate of 40 kDa/Mammalian Target of Rapamycin

Pathway. Am. J. Pathol. 2021, 191, 686–703. [CrossRef]

Kodama, T.; Koma, Y.-I.; Arai, N.; Kido, A.; Urakawa, N.; Nishio, M.; Shigeoka, M.; Yokozaki, H. CCL3–CCR5 axis contributes to

progression of esophageal squamous cell carcinoma by promoting cell migration and invasion via Akt and ERK pathways. Lab.

Investig. 2020, 100, 1140–1157. [CrossRef]

Tanigawa, K.; Tsukamoto, S.; Koma, Y.-I.; Kitamura, Y.; Urakami, S.; Shimizu, M.; Fujikawa, M.; Kodama, T.; Nishio, M.; Shigeoka,

M.; et al. S100A8/A9 Induced by Interaction with Macrophages in Esophageal Squamous Cell Carcinoma Promotes the Migration

and Invasion of Cancer Cells via Akt and p38 MAPK Pathways. Am. J. Pathol. 2022, 192, 536–552. [CrossRef]

Kodaira, H.; Koma, Y.; Hosono, M.; Higashino, N.; Suemune, K.; Nishio, M.; Shigeoka, M.; Yokozaki, H. ANXA10 induction by

interaction with tumor-associated macrophages promotes the growth of esophageal squamous cell carcinoma. Pathol. Int. 2019,

69, 135–147. [CrossRef] [PubMed]

Kitamura, Y.; Koma, Y.-I.; Tanigawa, K.; Tsukamoto, S.; Azumi, Y.; Miyako, S.; Urakami, S.; Kodama, T.; Nishio, M.; Shigeoka, M.;

et al. Roles of IL-7R Induced by Interactions between Cancer Cells and Macrophages in the Progression of Esophageal Squamous

Cell Carcinoma. Cancers 2023, 15, 394. [CrossRef] [PubMed]

Nishihira, T.; Hashimoto, Y.; Katayama, M.; Mori, S.; Kuroki, T. Molecular and cellular features of esophageal cancer cells. J.

Cancer Res. Clin. Oncol. 1993, 119, 441–449. [CrossRef] [PubMed]

Martens, M.; Ammar, A.; Riutta, A.; Waagmeester, A.; Slenter, D.N.; Hanspers, K.; Miller, R.A.; Digles, D.; Lopes, E.N.; Ehrhart, F.;

et al. WikiPathways: Connecting communities. Nucleic Acids Res. 2020, 49, D613–D621. [CrossRef] [PubMed]

Japanese Esophageal Society. Japanese Classification of Esophageal Cancer, 11th Edition: Part I. Esophagus 2016, 14, 1–36.

[CrossRef]

Japanese Esophageal Society. Japanese Classification of Esophageal Cancer, 11th Edition: Part II and III. Esophagus 2017, 14, 37–65.

[CrossRef]

Brierley, J.D.; Gospodarowicz, M.K.; Wittekind, C. TNM Classification of Malignant Tumours, 8th ed.; Wiley-Blackwell: Hoboken,

NJ, USA, 2016.

Kessenbrock, K.; Plaks, V.; Werb, Z. Matrix Metalloproteinases: Regulators of the Tumor Microenvironment. Cell 2010, 141, 52–67.

[CrossRef]

Farina, A.R.; Mackay, A.R. Gelatinase B/MMP-9 in Tumour Pathogenesis and Progression. Cancers 2014, 6, 240–296. [CrossRef]

Mondal, S.; Adhikari, N.; Banerjee, S.; Amin, S.A.; Jha, T. Matrix metalloproteinase-9 (MMP-9) and its inhibitors in cancer: A

minireview. Eur. J. Med. Chem. 2020, 194, 112260. [CrossRef]

Yu, X.-Y.; Lin, S.-C.; Zhang, M.-Q.; Guo, X.-T.; Ma, K.; Wang, L.-X.; Huang, W.-T.; Wang, Z.; Yu, X.; Wang, C.-G.; et al. Association

and prognostic significance of alpha-L-fucosidase-1 and matrix metalloproteinase 9 expression in esophageal squamous cell

carcinoma. World J. Gastrointest. Oncol. 2022, 14, 498–510. [CrossRef]

Ohashi, K.; Nemoto, T.; Nakamura, K.; Nemori, R. Increased expression of matrix metalloproteinase 7 and 9 and membrane type

1-matrix metalloproteinase in esophageal squamous cell carcinomas. Cancer 2000, 88, 2201–2209. [CrossRef]

Mukherjee, S.; Roth, M.J.; Dawsey, S.M.; Yan, W.; Rodriguez-Canales, J.; Erickson, H.S.; Hu, N.; Goldstein, A.M.; Taylor, P.R.;

Richardson, A.M.; et al. Increased matrix metalloproteinase activation in esophageal squamous cell carcinoma. J. Transl. Med.

2010, 8, 91. [CrossRef] [PubMed]

Tanioka, Y.; Yoshida, T.; Yagawa, T.; Saiki, Y.; Takeo, S.; Harada, T.; Okazawa, T.; Yanai, H.; Okita, K. Matrix metalloproteinase-7

and matrix metalloproteinase-9 are associated with unfavourable prognosis in superficial oesophageal cancer. Br. J. Cancer 2003,

89, 2116–2121. [CrossRef] [PubMed]

Liu, M.; Hu, Y.; Zhang, M.-F.; Luo, K.-J.; Xie, X.-Y.; Wen, J.; Fu, J.-H.; Yang, H. MMP1 promotes tumor growth and metastasis in

esophageal squamous cell carcinoma. Cancer Lett. 2016, 377, 97–104. [CrossRef] [PubMed]

Cancers 2023, 15, 2987

27.

28.

29.

30.

31.

32.

33.

34.

35.

36.

37.

38.

39.

40.

41.

42.

43.

44.

45.

46.

47.

48.

49.

22 of 23

Fogg, K.C.; Olson, W.R.; Miller, J.N.; Khan, A.; Renner, C.; Hale, I.; Weisman, P.S.; Kreeger, P.K. Alternatively activated macrophagederived secretome stimulates ovarian cancer spheroid spreading through a JAK2/STAT3 pathway. Cancer Lett. 2019, 458, 92–101.

[CrossRef]

Carroll, M.J.; Kapur, A.; Felder, M.; Patankar, M.S.; Kreeger, P.K. M2 macrophages induce ovarian cancer cell proliferation via a

heparin binding epidermal growth factor/matrix metalloproteinase 9 intercellular feedback loop. Oncotarget 2016, 7, 86608–86620.

[CrossRef]

Xu, Q.; Ma, H.; Chang, H.; Feng, Z.; Zhang, C.; Yang, X. The interaction of interleukin-8 and PTEN inactivation promotes the

malignant progression of head and neck squamous cell carcinoma via the STAT3 pathway. Cell Death Dis. 2020, 11, 405. [CrossRef]

Yuan, X.; Li, Y.; Zhang, A.Z.; Jiang, C.H.; Li, F.P.; Xie, Y.F.; Li, J.F.; Liang, W.H.; Zhang, H.J.; Liu, C.X.; et al. Tumor-associated

macrophage polarization promotes the progression of esophageal carcinoma. Aging 2020, 13, 2049–2072. [CrossRef]

Kamoshida, G.; Matsuda, A.; Miura, R.; Takashima, Y.; Katsura, A.; Tsuji, T. Potentiation of tumor cell invasion by co-culture

with monocytes accompanying enhanced production of matrix metalloproteinase and fibronectin. Clin. Exp. Metastasis 2013, 30,

289–297. [CrossRef]

Komohara, Y.; Horlad, H.; Ohnishi, K.; Fujiwara, Y.; Bai, B.; Nakagawa, T.; Suzu, S.; Nakamura, H.; Kuratsu, J.-I.; Takeya, M.

Importance of direct macrophage—Tumor cell interaction on progression of human glioma. Cancer Sci. 2012, 103, 2165–2172.

[CrossRef]

Umakoshi, M.; Takahashi, S.; Itoh, G.; Kuriyama, S.; Sasaki, Y.; Yanagihara, K.; Yashiro, M.; Maeda, D.; Goto, A.; Tanaka,

M. Macrophage-mediated transfer of cancer-derived components to stromal cells contributes to establishment of a pro-tumor

microenvironment. Oncogene 2019, 38, 2162–2176. [CrossRef] [PubMed]

Wang, J.; Levenson, A.S.; Satcher, R.L. Identification of a unique set of genes altered during cell-cell contact in an in vitro model

of prostate cancer bone metastasis. Int. J. Mol. Med. 2006, 17, 849–856. [CrossRef] [PubMed]

Waltera, A.; Schulz, D.; Schaefer, N.; Stoeckl, S.; Pion, E.; Haerteis, S.; Reichert, T.E.; Ettl, T.; Bauer, R.J. Opposing MMP-9

Expression in Mesenchymal Stromal Cells and Head and Neck Tumor Cells after Direct 2D and 3D Co-Culture. Int. J. Mol. Sci.

2023, 24, 1293. [CrossRef] [PubMed]

Takaishi, K.; Komohara, Y.; Tashiro, H.; Ohtake, H.; Nakagawa, T.; Katabuchi, H.; Takeya, M. Involvement of M2-polarized

macrophages in the ascites from advanced epithelial ovarian carcinoma in tumor progression via Stat3 activation. Cancer Sci.

2010, 101, 2128–2136. [CrossRef]

Ning, Y.; Cui, Y.; Li, X.; Cao, X.; Chen, A.; Xu, C.; Cao, J.; Luo, X. Co-culture of ovarian cancer stem-like cells with macrophages

induced SKOV3 cells stemness via IL-8/STAT3 signaling. Biomed. Pharmacother. 2018, 103, 262–271. [CrossRef]

Jia, Z.-H.; Jia, Y.; Guo, F.-J.; Chen, J.; Zhang, X.-W.; Cui, M.-H. Phosphorylation of STAT3 at Tyr705 regulates MMP-9 production

in epithelial ovarian cancer. PLoS ONE 2017, 12, e0183622. [CrossRef]

Suzuki, T.; Kuwabara, Y.; Iwata, H.; Mitani, M.; Shinoda, N.; Sato, A.; Mitsui, A.; Sugiura, M.; Kato, J.; Fujii, Y. Role of matrix

metalloproteinase-9 in in vitro invasion of esophageal carcinoma cells. J. Surg. Oncol. 2002, 81, 80–86. [CrossRef]

Dufour, A.; Sampson, N.S.; Zucker, S.; Cao, J. Role of the hemopexin domain of matrix metalloproteinases in cell migration. J. Cell.

Physiol. 2008, 217, 643–651. [CrossRef]

Wang, X.-Q.; Sun, P.; Paller, A.S. Ganglioside GM3 Inhibits Matrix Metalloproteinase-9 Activation and Disrupts Its Association

with Integrin. J. Biol. Chem. 2003, 278, 25591–25599. [CrossRef]

Yu, Q.; Stamenkovic, I. Localization of matrix metalloproteinase 9 to the cell surface provides a mechanism for CD44-mediated

tumor invasion. Genes Dev. 1999, 13, 35–48. [CrossRef]

Bannikov, G.A.; Karelina, T.V.; Collier, I.E.; Marmer, B.L.; Goldberg, G.I. Substrate Binding of Gelatinase B Induces Its Enzymatic

Activity in the Presence of Intact Propeptide. J. Biol. Chem. 2002, 277, 16022–16027. [CrossRef] [PubMed]

Tadbir, A.A.; Mardani, M.; Pourshahidi, S.; Nezarati, K.; Bahadori, P. Prognostic value of matrix metalloproteinase-9 expression in

oral squamous cell carcinoma and its association with angiogenesis. J. Clin. Exp. Dent. 2016, 8, e130–e135. [CrossRef]

Kabashima, A.; Maehara, Y.; Kakeji, Y.; Baba, H.; Koga, T.; Sugimachi, K. Clinicopathological features and overexpression of

matrix metalloproteinases in intramucosal gastric carcinoma with lymph node metastasis. Clin. Cancer Res. 2000, 6, 3581–3584.

Joseph, C.; Alsaleem, M.; Orah, N.; Narasimha, P.L.; Miligy, I.M.; Kurozumi, S.; Ellis, I.O.; Mongan, N.; Green, A.R.; Rakha, E.A.

Elevated MMP9 expression in breast cancer is a predictor of shorter patient survival. Breast Cancer Res. Treat. 2020, 182, 267–282.

[CrossRef] [PubMed]

Reis, S.T.; Leite, K.R.M.; Piovesan, L.F.; Pontes-Junior, J.; Viana, N.I.; Abe, D.K.; Crippa, A.; Moura, C.M.; Adonias, S.P.; Srougi, M.;

et al. Increased expression of MMP-9 and IL-8 are correlated with poor prognosis of Bladder Cancer. BMC Urol. 2012, 12, 18.

[CrossRef]

Martins, J.M.A.; Rabelo-Santos, S.H.; Westin, M.C.D.A.; Zeferino, L.C. Tumoral and stromal expression of MMP-2, MMP-9,

MMP-14, TIMP-1, TIMP-2, and VEGF-A in cervical cancer patient survival: A competing risk analysis. BMC Cancer 2020, 20, 660.

[CrossRef]

Sillanpää, S.; Anttila, M.; Voutilainen, K.; Ropponen, K.; Turpeenniemi-Hujanen, T.; Puistola, U.; Tammi, R.; Tammi, M.; Sironen,

R.; Saarikoski, S.; et al. Prognostic significance of matrix metalloproteinase-9 (MMP-9) in epithelial ovarian cancer. Gynecol. Oncol.

2007, 104, 296–303. [CrossRef]

Cancers 2023, 15, 2987

50.

51.

52.

53.

23 of 23

Hu, J.M.; Liu, K.; Liu, J.H.; Jiang, X.L.; Wang, X.L.; Chen, Y.Z.; Li, S.G.; Zou, H.; Pang, L.J.; Liu, C.X.; et al. CD163 as a marker of

M2 macrophage, contribute to predicte aggressiveness and prognosis of Kazakh esophageal squamous cell carcinoma. Oncotarget

2017, 8, 21526–21538. [CrossRef]

Chakrabarti, S.; Patel, K.D. Regulation of matrix metalloproteinase-9 release from IL-8-stimulated human neutrophils. J. Leukoc.

Biol. 2005, 78, 279–288. [CrossRef]

Van den Steen, P.E.; Proost, P.; Wuyts, A.; Van Damme, J.; Opdenakker, G. Neutrophil gelatinase B potentiates interleukin-8

tenfold by aminoterminal processing, whereas it degrades CTAP-III, PF-4, and GRO-alpha and leaves RANTES and MCP-2 intact.

Blood 2000, 96, 2673–2681. [CrossRef]

Blanchette-Farra, N.; Kita, D.; Konstorum, A.; Tesfay, L.; Lemler, D.; Hegde, P.; Claffey, K.P.; Torti, F.M.; Torti, S.V. Contribution

of three-dimensional architecture and tumor-associated fibroblasts to hepcidin regulation in breast cancer. Oncogene 2018, 37,

4013–4032. [CrossRef] [PubMed]

Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual

author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to

people or property resulting from any ideas, methods, instructions or products referred to in the content.

...

参考文献をもっと見る

全国の大学の
卒論・修論・学位論文

一発検索!

この論文の関連論文を見る