Spandidos Publications Logo
  • About
    • About Spandidos
    • Aims and Scopes
    • Abstracting and Indexing
    • Editorial Policies
    • Reprints and Permissions
    • Job Opportunities
    • Terms and Conditions
    • Contact
  • Journals
    • All Journals
    • Oncology Letters
      • Oncology Letters
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Oncology
      • International Journal of Oncology
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Molecular and Clinical Oncology
      • Molecular and Clinical Oncology
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Experimental and Therapeutic Medicine
      • Experimental and Therapeutic Medicine
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Molecular Medicine
      • International Journal of Molecular Medicine
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Biomedical Reports
      • Biomedical Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Oncology Reports
      • Oncology Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Molecular Medicine Reports
      • Molecular Medicine Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • World Academy of Sciences Journal
      • World Academy of Sciences Journal
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Functional Nutrition
      • International Journal of Functional Nutrition
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Epigenetics
      • International Journal of Epigenetics
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Medicine International
      • Medicine International
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
  • Articles
  • Information
    • Information for Authors
    • Information for Reviewers
    • Information for Librarians
    • Information for Advertisers
    • Conferences
  • Language Editing
Spandidos Publications Logo
  • About
    • About Spandidos
    • Aims and Scopes
    • Abstracting and Indexing
    • Editorial Policies
    • Reprints and Permissions
    • Job Opportunities
    • Terms and Conditions
    • Contact
  • Journals
    • All Journals
    • Biomedical Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Experimental and Therapeutic Medicine
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Epigenetics
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Functional Nutrition
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Molecular Medicine
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Oncology
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Medicine International
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Molecular and Clinical Oncology
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Molecular Medicine Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Oncology Letters
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Oncology Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • World Academy of Sciences Journal
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
  • Articles
  • Information
    • For Authors
    • For Reviewers
    • For Librarians
    • For Advertisers
    • Conferences
  • Language Editing
Login Register Submit
  • This site uses cookies
  • You can change your cookie settings at any time by following the instructions in our Cookie Policy. To find out more, you may read our Privacy Policy.

    I agree
Search articles by DOI, keyword, author or affiliation
Search
Advanced Search
presentation
Oncology Letters
Join Editorial Board Propose a Special Issue
Print ISSN: 1792-1074 Online ISSN: 1792-1082
Journal Cover
May-2021 Volume 21 Issue 5

Full Size Image

Sign up for eToc alerts
Recommend to Library

Journals

International Journal of Molecular Medicine

International Journal of Molecular Medicine

International Journal of Molecular Medicine is an international journal devoted to molecular mechanisms of human disease.

International Journal of Oncology

International Journal of Oncology

International Journal of Oncology is an international journal devoted to oncology research and cancer treatment.

Molecular Medicine Reports

Molecular Medicine Reports

Covers molecular medicine topics such as pharmacology, pathology, genetics, neuroscience, infectious diseases, molecular cardiology, and molecular surgery.

Oncology Reports

Oncology Reports

Oncology Reports is an international journal devoted to fundamental and applied research in Oncology.

Experimental and Therapeutic Medicine

Experimental and Therapeutic Medicine

Experimental and Therapeutic Medicine is an international journal devoted to laboratory and clinical medicine.

Oncology Letters

Oncology Letters

Oncology Letters is an international journal devoted to Experimental and Clinical Oncology.

Biomedical Reports

Biomedical Reports

Explores a wide range of biological and medical fields, including pharmacology, genetics, microbiology, neuroscience, and molecular cardiology.

Molecular and Clinical Oncology

Molecular and Clinical Oncology

International journal addressing all aspects of oncology research, from tumorigenesis and oncogenes to chemotherapy and metastasis.

World Academy of Sciences Journal

World Academy of Sciences Journal

Multidisciplinary open-access journal spanning biochemistry, genetics, neuroscience, environmental health, and synthetic biology.

International Journal of Functional Nutrition

International Journal of Functional Nutrition

Open-access journal combining biochemistry, pharmacology, immunology, and genetics to advance health through functional nutrition.

International Journal of Epigenetics

International Journal of Epigenetics

Publishes open-access research on using epigenetics to advance understanding and treatment of human disease.

Medicine International

Medicine International

An International Open Access Journal Devoted to General Medicine.

Journal Cover
May-2021 Volume 21 Issue 5

Full Size Image

Sign up for eToc alerts
Recommend to Library

  • Article
  • Citations
    • Cite This Article
    • Download Citation
    • Create Citation Alert
    • Remove Citation Alert
    • Cited By
  • Similar Articles
    • Related Articles (in Spandidos Publications)
    • Similar Articles (Google Scholar)
    • Similar Articles (PubMed)
  • Download PDF
  • Download XML
  • View XML
Article Open Access

Macrophage CCL22 expression promotes lymphangiogenesis in patients with tongue squamous cell carcinoma via IL-4/STAT6 in the tumor microenvironment

  • Authors:
    • Satoshi Kimura
    • Hirotsugu Noguchi
    • Uki Nanbu
    • Toshiyuki Nakayama
  • View Affiliations / Copyright

    Affiliations: Department of Clinical Pathology, Kitakyushu City Yahata Hospital, Kitakyushu, Fukuoka 805-8534, Japan, Department of Pathology, School of Medicine, University of Occupational and Environmental Health, Kitakyushu, Fukuoka 807-8555, Japan
    Copyright: © Kimura et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
  • Article Number: 383
    |
    Published online on: March 16, 2021
       https://doi.org/10.3892/ol.2021.12644
  • Expand metrics +
Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )
Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )
Cited By (CrossRef): 0 citations Loading Articles...

This article is mentioned in:



Abstract

The C‑C motif chemokine ligand 22 (CCL22) chemokine is produced by M2‑like tumor‑associated macrophages (TAMs) in the tumor microenvironment. Chemokine C‑C motif receptor 4 (CCR4), the CCL22 receptor, on T helper2 (Th2) cells leads to a Th2 cytokine‑dominant environment. In our previous study, lymph node metastasis was the main predictor of tongue squamous cell carcinoma (SCC) via CCL22. Therefore, the present study aimed to investigate the effects of CCL22 and a Th2 cytokine‑predominant tumor microenvironment on vascular endothelial growth factor (VEGF)‑C expression and lymphangiogenesis. The post‑operative courses of 110 patients with early‑stage tongue SCC with a histopathological diagnosis based on the 8th TNM classification were followed up (mean/median follow‑up time, 47.1/42.0 months) from surgery until death or the last follow‑up visit, and subsequent lymph node relapse was assessed. Lymphangiogenesis and the immunohistochemical expression of several markers (CCL22, CCR4 and VEGF‑C) were evaluated. The Kaplan‑Meier method was used to plot lymph node relapse‑free survival and overall survival curves, which were compared using the log‑rank test. In vitro, the association between CCL22 and VEGF‑C by interleukin (IL)‑4/signal transducer and activator of transcription 6 (STAT6) stimulation was examined. Lymphangiogenesis was significantly associated with lymph node relapse (P<0.001) and a CCL22+ macrophage ratio (P<0.001). CCL22+ TAMs were positive for VEGF‑C and surrounded by CCR4+ cells. Additionally, VEGF‑C expression was increased in IL‑4/STAT6‑stimulated macrophages. In addition, the STAT6 signaling pathway was activated in the SCC cells in the deeply invaded part of the tumor along with the aggregated macrophages. In conclusion, TAM CCL22 expression led to lymph node relapse via VEGF‑C expression within the tumor microenvironment and the IL‑4/STAT6 signaling pathway in early stage tongue SCC. Additionally, the worst pattern of invasion and depth of invasion were revealed to be useful parameters for lymph node relapse in patients with tongue SCC. The present study suggested that CCL22 contributed to the role of M2‑like differentiated TAMs in prognosis and lymph node relapse via IL‑4/STAT6 and VEGF. The IL‑4/STAT6 signaling pathway may be a new molecular target for tongue SCC.
View Figures

Figure 1

Figure 2

Figure 3

Figure 4

View References

1 

Siegel RL, Miller KD and Jemal A: Cancer statistics, 2015. CA Cancer J Clin. 65:5–29. 2015. View Article : Google Scholar : PubMed/NCBI

2 

Warnakulasuriya S: Global epidemiology of oral and oropharyngeal cancer. Oral Oncol. 45:309–316. 2009. View Article : Google Scholar : PubMed/NCBI

3 

Ariyoshi Y, Shimahara M, Omura K, Yamamoto E, Mizuki H, Chiba H, Imai Y, Fujita S, Shinohara M and Seto K; Japanese Society of Oral and Maxillofacial Surgeons, 2002, : Epidemiological study of malignant tumors in the oral and maxillofacial region: Survey of member institutions of the Japanese Society of Oral and Maxillofacial Surgeons, 2002. Int J Clin Oncol. 13:220–228. 2008. View Article : Google Scholar : PubMed/NCBI

4 

Dünne AA, Müller HH, Eisele DW, Kessel K, Moll R and Werner JA: Meta-analysis of the prognostic significance of perinodal spread in head and neck squamous cell carcinomas (HNSCC) patients. Eur J Cancer. 42:1863–1868. 2006. View Article : Google Scholar : PubMed/NCBI

5 

Afzali P and Ward BB: Management of the neck in oral squamous cell carcinoma: Background, classification, and current philosophy. Oral Maxillofac Surg Clin North Am. 31:69–84. 2019. View Article : Google Scholar : PubMed/NCBI

6 

Kimura S, Nanbu U, Noguchi H, Harada Y, Kumamoto K, Sasaguri Y and Nakayama T: Macrophage CCL22 expression in the tumor microenvironment and implications for survival in patients with squamous cell carcinoma of the tongue. J Oral Pathol Med. 48:677–685. 2019. View Article : Google Scholar : PubMed/NCBI

7 

Kaesler S, Wölbing F, Kempf WE, Skabytska Y, Köberle M, Volz T, Sinnberg T, Amaral T, Möckel S, Yazdi A, et al: Targeting tumor-resident mast cells for effective anti-melanoma immune responses. JCI Insight. 4:e1250572019. View Article : Google Scholar

8 

Messex JK, Byrd CJ and Liou GY: Signaling of macrophages that contours the tumor microenvironment for promoting cancer development. Cells. 9:e9192020. View Article : Google Scholar : PubMed/NCBI

9 

Godiska R, Chantry D, Raport CJ, Sozzani S, Allavena P, Leviten D, Mantovani A and Gray PW: Human macrophage-derived chemokine (MDC), a novel chemoattractant for monocytes, monocyte-derived dendritic cells, and natural killer cells. J Exp Med. 185:1595–1604. 1997. View Article : Google Scholar : PubMed/NCBI

10 

Imai T, Chantry D, Raport CJ, Wood CL, Nishimura M, Godiska R, Yoshie O and Gray PW: Macrophage-derived chemokine is a functional ligand for the CC chemokine receptor 4. J Biol Chem. 273:1764–1768. 1998. View Article : Google Scholar : PubMed/NCBI

11 

Curiel TJ, Coukos G, Zou L, Alvarez X, Cheng P, Mottram P, Evdemon-Hogan M, Conejo-Garcia JR, Zhang L, Burow M, et al: Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat Med. 10:942–949. 2004. View Article : Google Scholar : PubMed/NCBI

12 

Imai T, Nagira M, Takagi S, Kakizaki M, Nishimura M, Wang J, Gray PW, Matsushima K and Yoshie O: Selective recruitment of CCR4-bearing Th2 cells toward antigen-presenting cells by the CC chemokines thymus and activation-regulated chemokine and macrophage-derived chemokine. Int Immunol. 11:81–88. 1999. View Article : Google Scholar : PubMed/NCBI

13 

Biedermann T, Schwärzler C, Lametschwandtner G, Thoma G, Carballido-Perrig N, Kund J, de Vries JE, Rot A and Carballido JM: Targeting CLA/E-selectin interactions prevents CCR4-mediated recruitment of human Th2 memory cells to human skin in vivo. Eur J Immunol. 32:3171–3180. 2002. View Article : Google Scholar : PubMed/NCBI

14 

Franciszkiewicz K, Boissonnas A, Boutet M, Combadière C and Mami-Chouaib F: Role of chemokines and chemokine receptors in shaping the effector phase of the antitumor immune response. Cancer Res. 72:6325–6332. 2012. View Article : Google Scholar : PubMed/NCBI

15 

Zwaans BM and Bielenberg DR: Potential therapeutic strategies for lymphatic metastasis. Microvasc Res. 74:145–158. 2007. View Article : Google Scholar : PubMed/NCBI

16 

Moussai D, Mitsui H, Pettersen JS, Pierson KC, Shah KR, Suárez-Fariñas M, Cardinale IR, Bluth MJ, Krueger JG, Carucci JA, et al: The human cutaneous squamous cell carcinoma microenvironment is characterized by increased lymphatic density and enhanced expression of macrophage-derived VEGF-C. J Invest Dermato. 131:229–236. 2011. View Article : Google Scholar

17 

Nakagawa T, Ohnishi K, Kosaki Y, Saito Y, Horlad H, Fujiwara Y, Takeya M and Komohara Y: Optimum immunohistochemical procedures for analysis of macrophages in human and mouse formalin fixed paraffin-embedded tissue samples. J Clin Exp Hematop. 57:31–36. 2017. View Article : Google Scholar : PubMed/NCBI

18 

Yamagata Y, Tomioka H, Sakamoto K, Sato K, Harada H, Ikeda T and Kayamori K: CD163-positive macrophages within the tumor stroma are associated with lymphangiogenesis and lymph node metastasis in oral squamous cell carcinoma. J Oral Maxillofac Surg. 75:2144–2153. 2017. View Article : Google Scholar : PubMed/NCBI

19 

Kimura S, Noguchi H, Nanbu U, Wang KY, Sasaguri Y and Nakayama T: Relationship between CCL22 expression by vascular smooth muscle cells and macrophage histamine receptors in atherosclerosis. J Atheroscler Thromb. 25:1240–1254. 2018. View Article : Google Scholar : PubMed/NCBI

20 

Tsujikawa T, Yaguchi T, Ohmura G, Ohta S, Kobayashi A, Kawamura N, Fujita T, Nakano H, Shimada T, Takahashi T, et al: Autocrine and paracrine loops between cancer cells and macrophages promote lymph node metastasis via CCR4/CCL22 in head and neck squamous cell carcinoma. Int J Cancer. 132:2755–2766. 2013. View Article : Google Scholar : PubMed/NCBI

21 

Almangush A, Bello IO, Keski-Säntti H, Mäkinen LK, Kauppila JH, Pukkila M, Hagström J, Laranne J, Tommola S, Nieminen O, et al: Depth of invasion, tumor budding, and worst pattern of invasion: Prognostic indicators in early-stage oral tongue cancer. Head Neck. 36:811–818. 2014. View Article : Google Scholar : PubMed/NCBI

22 

Brandwein-Gensler M, Teixeira MS, Lewis CM, Lee B, Rolnitzky L, Hille JJ, Genden E, Urken ML and Wang BY: Oral squamous cell carcinoma: Histologic risk assessment, but not margin status, is strongly predictive of local disease-free and overall survival. Am J Surg Pathol. 29:167–178. 2005. View Article : Google Scholar : PubMed/NCBI

23 

Shimizu S, Miyazaki A, Sonoda T, Koike K, Ogi K, Kobayashi JI, Kaneko T, Igarashi T, Ueda M, Dehari H, et al: Tumor budding is an independent prognostic marker in early stage oral squamous cell carcinoma: With special reference to the mode of invasion and worst pattern of invasion. PLoS One. 13:e01954512018. View Article : Google Scholar : PubMed/NCBI

24 

Caldeira PC, Soto AML, de Aguiar MCF and Martins CC: Tumor depth of invasion and prognosis of early-stage oral squamous cell carcinoma: A meta-analysis. Oral Dis. 26:1357–1365. 2020. View Article : Google Scholar : PubMed/NCBI

25 

den Toom IJ, Janssen LM, van Es RJJ, Karagozoglu KH, de Keizer B, van Weert S, Willems SM, Bloemena E, Leemans CR and de Bree R: Depth of invasion in patients with early stage oral cancer staged by sentinel node biopsy. Head Neck. 41:2100–2106. 2019. View Article : Google Scholar : PubMed/NCBI

26 

Amin MB, Edge SB, Greene FL, Byrd DR, Brookland RK, Washington MK, Gershenwald JE, Compton CC, Hess KR, Sullivan DC, et al: AJCC Cancer Staging Manual. 8th edition. Springer; New York, NY: 2017, View Article : Google Scholar

27 

Lydiatt WM, Patel SG, O'Sullivan B, Brandwein MS, Ridge JA, Migliacci JC, Loomis AM and Shah JP: Head and Neck cancers-major changes in the American Joint Committee on cancer eighth edition cancer staging manual. CA Cancer J Clin. 67:122–137. 2017. View Article : Google Scholar : PubMed/NCBI

28 

Audet N, Beasley NJ, MacMillan C, Jackson DG, Gullane PJ and Kamel-Reid S: Lymphatic vessel density, nodal metastases, and prognosis in patients with head and neck cancer. Arch Otolaryngol Head Neck Surg. 131:1065–1070. 2005. View Article : Google Scholar : PubMed/NCBI

29 

Kimura S, Tanimoto A, Wang KY, Shimajiri S, Guo X, Tasaki T, Yamada S and Sasaguri Y: Expression of macrophage-derived chemokine (CCL22) in atherosclerosis and regulation by histamine via the H2 receptor. Pathol Int. 62:675–683. 2012. View Article : Google Scholar : PubMed/NCBI

30 

Kanda Y: Investigation of the freely available easy-to-use software ‘EZR’ for medical statistics. Bone Marrow Transplant. 48:452–458. 2013. View Article : Google Scholar : PubMed/NCBI

31 

D'Alessio S, Correale C, Tacconi C, Gandelli A, Pietrogrande G, Vetrano S, Genua M, Arena V, Spinelli A, Peyrin-Biroulet L, et al: VEGF-C-dependent stimulation of lymphatic function ameliorates experimental inflammatory bowel disease. J Clin Invest. 124:3863–3878. 2014. View Article : Google Scholar : PubMed/NCBI

32 

Komohara Y, Fujiwara Y, Ohnishi K and Takeya M: Tumor-associated macrophages: Potential therapeutic targets for anti-cancer therapy. Adv Drug Deliv Rev. 99:180–185. 2016. View Article : Google Scholar : PubMed/NCBI

33 

Miyasato Y, Takashima Y, Takeya H, Yano H, Hayano A, Nakagawa T, Makino K, Takeya M, Yamanaka R and Komohara Y: The expression of PD-1 ligands and IDO1 by macrophage/microglia in primary central nervous system lymphoma. J Clin Exp Hematop. 58:95–101. 2018. View Article : Google Scholar : PubMed/NCBI

34 

Komohara Y and Takeya M: CAFs and TAMs: Maestros of the tumour microenvironment. J Pathol. 241:313–315. 2017. View Article : Google Scholar : PubMed/NCBI

35 

Alitalo K, Tammela T and Petrova TV: Lymphangiogenesis in development and human disease. Nature. 438:946–953. 2005. View Article : Google Scholar : PubMed/NCBI

36 

Shi VY, Bao L and Chan LS: Inflammation-driven dermal lymphangiogenesis in atopic dermatitis is associated with CD11b+ macrophage recruitment and VEGF-C up-regulation in the IL-4-transgenic mouse model. Microcirculation. 19:567–579. 2012. View Article : Google Scholar : PubMed/NCBI

37 

Roca H, Varsos ZS, Sud S, Craig MJ, Ying C and Pienta KJ: CCL2 and interleukin-6 promote survival of human CD11b+ peripheral blood mononuclear cells and induce M2-type macrophage polarization. J Biol Chem. 284:34342–34354. 2009. View Article : Google Scholar : PubMed/NCBI

38 

Zhang B, Yao G, Zhang Y and Gao J, Yang B, Rao Z and Gao J and Gao J: M2-polarized tumor-associated macrophages are associated with poor prognoses resulting from accelerated lymphangiogenesis in lung adenocarcinoma. Clinics (São Paulo). 66:1879–1886. 2011. View Article : Google Scholar

39 

Savetsky IL, Ghanta S, Gardenier JC, Torrisi JS, García Nores GD, Hespe GE, Nitti MD, Kataru RP and Mehrara BJ: Th2 cytokines inhibit lymphangiogenesis. PLoS One. 10:e01269082015. View Article : Google Scholar : PubMed/NCBI

40 

Zhang B, Wang J, Gao J, Guo Y, Chen X, Wang B, Gao J, Rao Z and Chen Z: Alternatively activated RAW264.7 macrophages enhance tumor lymphangiogenesis in mouse lung adenocarcinoma. J Cell Biochem. 107:134–143. 2009. View Article : Google Scholar : PubMed/NCBI

41 

Hinshaw DC and Shevde LA: The tumor microenvironment innately modulates cancer progression. Cancer Res. 79:4557–4566. 2019. View Article : Google Scholar : PubMed/NCBI

42 

Fulkerson PC, Zimmermann N, Hassman LM, Finkelman FD and Rothenberg ME: Pulmonary chemokine expression is coordinately regulated by STAT1, STAT6, and IFN-gamma. J Immunol. 173:7565–7574. 2004. View Article : Google Scholar : PubMed/NCBI

43 

Hsu MC, Pan MR and Hung WC: Two birds, one stone: Double hits on tumor growth and lymphangiogenesis by targeting vascular endothelial growth factor receptor 3. Cells. 8:e2702019. View Article : Google Scholar : PubMed/NCBI

44 

Binnemars-Postma K, Bansal R, Storm G and Prakash J: Targeting the Stat6 pathway in tumor-associated macrophages reduces tumor growth and metastatic niche formation in breast cancer. FASEB J. 32:969–978. 2018. View Article : Google Scholar : PubMed/NCBI

Related Articles

  • Abstract
  • View
  • Download
  • Twitter
Copy and paste a formatted citation
Spandidos Publications style
Kimura S, Noguchi H, Nanbu U and Nakayama T: Macrophage CCL22 expression promotes lymphangiogenesis in patients with tongue squamous cell carcinoma via IL-4/STAT6 in the tumor microenvironment. Oncol Lett 21: 383, 2021.
APA
Kimura, S., Noguchi, H., Nanbu, U., & Nakayama, T. (2021). Macrophage CCL22 expression promotes lymphangiogenesis in patients with tongue squamous cell carcinoma via IL-4/STAT6 in the tumor microenvironment. Oncology Letters, 21, 383. https://doi.org/10.3892/ol.2021.12644
MLA
Kimura, S., Noguchi, H., Nanbu, U., Nakayama, T."Macrophage CCL22 expression promotes lymphangiogenesis in patients with tongue squamous cell carcinoma via IL-4/STAT6 in the tumor microenvironment". Oncology Letters 21.5 (2021): 383.
Chicago
Kimura, S., Noguchi, H., Nanbu, U., Nakayama, T."Macrophage CCL22 expression promotes lymphangiogenesis in patients with tongue squamous cell carcinoma via IL-4/STAT6 in the tumor microenvironment". Oncology Letters 21, no. 5 (2021): 383. https://doi.org/10.3892/ol.2021.12644
Copy and paste a formatted citation
x
Spandidos Publications style
Kimura S, Noguchi H, Nanbu U and Nakayama T: Macrophage CCL22 expression promotes lymphangiogenesis in patients with tongue squamous cell carcinoma via IL-4/STAT6 in the tumor microenvironment. Oncol Lett 21: 383, 2021.
APA
Kimura, S., Noguchi, H., Nanbu, U., & Nakayama, T. (2021). Macrophage CCL22 expression promotes lymphangiogenesis in patients with tongue squamous cell carcinoma via IL-4/STAT6 in the tumor microenvironment. Oncology Letters, 21, 383. https://doi.org/10.3892/ol.2021.12644
MLA
Kimura, S., Noguchi, H., Nanbu, U., Nakayama, T."Macrophage CCL22 expression promotes lymphangiogenesis in patients with tongue squamous cell carcinoma via IL-4/STAT6 in the tumor microenvironment". Oncology Letters 21.5 (2021): 383.
Chicago
Kimura, S., Noguchi, H., Nanbu, U., Nakayama, T."Macrophage CCL22 expression promotes lymphangiogenesis in patients with tongue squamous cell carcinoma via IL-4/STAT6 in the tumor microenvironment". Oncology Letters 21, no. 5 (2021): 383. https://doi.org/10.3892/ol.2021.12644
Follow us
  • Twitter
  • LinkedIn
  • Facebook
About
  • Spandidos Publications
  • Careers
  • Cookie Policy
  • Privacy Policy
How can we help?
  • Help
  • Live Chat
  • Contact
  • Email to our Support Team