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 Reports
Join Editorial Board Propose a Special Issue
Print ISSN: 1021-335X Online ISSN: 1791-2431
Journal Cover
December-2019 Volume 42 Issue 6

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
December-2019 Volume 42 Issue 6

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

The prednisolone phosphate‑induced suppression of the angiogenic function of tumor‑associated macrophages enhances the antitumor effects of doxorubicin on B16.F10 murine melanoma cells in vitro

  • Authors:
    • Emilia Licarete
    • Valentin Florian Rauca
    • Lavinia Luput
    • Laura Patras
    • Alina Sesarman
    • Manuela Banciu
  • View Affiliations / Copyright

    Affiliations: Department of Molecular Biology and Biotechnology, Faculty of Biology and Geology, Babes‑Bolyai University, 400006 Cluj‑Napoca, Romania
  • Pages: 2694-2705
    |
    Published online on: October 1, 2019
       https://doi.org/10.3892/or.2019.7346
  • 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

Several lines of evidence have clearly demonstrated the role of the tumor microenvironment in favoring the drug resistance of melanoma cells, as well as the progression of this cancer type. Since our previous studies proved that the accumulation of prednisolone disodium phosphate (PLP) in melanoma tissue inhibited tumor growth by exerting anti‑angiogenic effects on the most abundant cells of the tumor microenvironment, tumor‑associated macrophages (TAMs), the present study investigated whether PLP could enhance the cytotoxic effects of doxorubicin (DOX) on B16.F10 murine melanoma cells. To assess the antitumor efficacy of the combined therapeutic approach based on PLP and DOX, we used a co‑culture system composed of bone marrow‑derived macrophages (BMDMs) and B16.F10 murine melanoma cells at a cell density ratio that approximates the melanoma microenvironment in vivo, ensuring the polarization of the BMDMs into TAMs. Thus, we assessed the combined therapeutic effects of PLP and DOX on melanoma cell proliferation and apoptosis, as well as on supportive processes for tumor growth, such as oxidative stress as well as the angiogenic and inflammatory capacity of the cell co‑culture. Our data demonstrated that the cytotoxicity of DOX was potentiated mainly via the anti‑angiogenic activity of PLP in the melanoma microenvironment in vitro. Moreover, the amplitude of the cytotoxicity of the combined treatments may be linked to the degree of the suppression of the pro‑angiogenic function of TAMs. Thus, the potent decrease in the expression of the majority of the angiogenic and inflammatory proteins in TAMs following the concomitant administration of PLP and DOX may be associated with their anti‑proliferative, as well as pro‑apoptotic effects on B16.F10 melanoma cells. However, the combination therapy tested did not affect the immunosuppressive phenotype of the TAMs, as the levels of two important markers of the M2‑like phenotype of macrophages (IL‑10 and Arg‑1) were not reduced or even increased following these treatments. On the whole, the findings of this study indicated that PLP improved the therapeutic outcome of DOX in the melanoma microenvironment via the inhibition of the pro‑angiogenic function of TAMs.
View Figures

Figure 1

Figure 2

Figure 3

Figure 4

Figure 5

View References

1 

Hsueh EC and Gorantla KC: Novel melanoma therapy. Exp Hematol Oncol. 5:232016. View Article : Google Scholar : PubMed/NCBI

2 

La Porta CA: Mechanism of drug sensitivity and resistance in melanoma. Curr Cancer Drug Targets. 9:391–397. 2009. View Article : Google Scholar : PubMed/NCBI

3 

Kuphal S and Bosserhoff A: Recent progress in understanding the pathology of malignant melanoma. J Pathol. 219:400–409. 2009. View Article : Google Scholar : PubMed/NCBI

4 

Nazarian R, Shi H, Wang Q, Kong X, Koya RC, Lee H, Chen Z, Lee MK, Attar N, Sazegar H, et al: Melanomas acquire resistance to B-RAF(V600E) inhibition by RTK or N-RAS upregulation. Nature. 468:973–977. 2010. View Article : Google Scholar : PubMed/NCBI

5 

Zaretsky JM, Garcia-Diaz A, Shin DS, Escuin-Ordinas H, Hugo W, Hu-Lieskovan S, Torrejon DY, Abril-Rodriguez G, Sandoval S, Barthly L, et al: Mutations associated with acquired resistance to PD-1 blockade in melanoma. N Engl J Med. 375:819–829. 2016. View Article : Google Scholar : PubMed/NCBI

6 

Larkin J, Chmielowski B, Lao CD, Hodi FS, Sharfman W, Weber J, Suijkerbuijk KPM, Azevedo S, Li H, Reshef D, et al: Neurologic serious adverse events associated with nivolumab plus ipilimumab or nivolumab alone in advanced melanoma, including a case series of encephalitis. Oncologist. 22:709–718. 2017. View Article : Google Scholar : PubMed/NCBI

7 

Long GV, Atkinson V, Cebon JS, Jameson MB, Fitzharris BM, McNeil CM, Hill AG, Ribas A, Atkins MB, Thompson JA, et al: Standard-dose pembrolizumab in combination with reduced-dose ipilimumab for patients with advanced melanoma (KEYNOTE-029): An open-label, phase 1b trial. Lancet Oncol. 18:1202–1210. 2017. View Article : Google Scholar : PubMed/NCBI

8 

Wolchok JD, Kluger H, Callahan MK, Postow MA, Rizvi NA, Lesokhin AM, Segal NH, Ariyan CE, Gordon RA, Reed K, et al: Nivolumab plus ipilimumab in advanced melanoma. N Engl J Med. 369:122–133. 2013. View Article : Google Scholar : PubMed/NCBI

9 

Melis C, Rogiers A, Bechter O and van den Oord JJ: Molecular genetic and immunotherapeutic targets in metastatic melanoma. Virchows Arch. 471:281–293. 2017. View Article : Google Scholar : PubMed/NCBI

10 

Son B, Lee S, Youn H, Kim E, Kim W and Youn B: The role of tumor microenvironment in therapeutic resistance. Oncotarget. 8:3933–3945. 2017. View Article : Google Scholar : PubMed/NCBI

11 

Wang T, Xiao M, Ge Y, Krepler C, Belser E, Lopez-Coral A, Xu X, Zhang G, Azuma R, Liu Q, et al: BRAF inhibition stimulates melanoma-associated macrophages to drive tumor growth. Clin Cancer Res. 21:1652–1664. 2015. View Article : Google Scholar : PubMed/NCBI

12 

Smith BD, Kaufman MD, Leary CB, Turner BA, Wise SC, Ahn YM, Booth RJ, Caldwell TM, Ensinger CL, Hood MM, et al: Altiratinib inhibits tumor growth, invasion, angiogenesis, and microenvironment-mediated drug resistance via balanced inhibition of MET, TIE2, and VEGFR2. Mol Cancer Ther. 14:2023–2034. 2015. View Article : Google Scholar : PubMed/NCBI

13 

Castells M, Thibault B, Delord JP and Couderc B: Implication of tumor microenvironment in chemoresistance: Tumor-associated stromal cells protect tumor cells from cell death. Int J Mol Sci. 13:9545–9571. 2012. View Article : Google Scholar : PubMed/NCBI

14 

Affara NI, Ruffell B, Medler TR, Gunderson AJ, Johansson M, Bornstein S, Bergsland E, Steinhoff M, Li Y, Gong Q, et al: B cells regulate macrophage phenotype and response to chemotherapy in squamous carcinomas. Cancer Cell. 25:809–821. 2014. View Article : Google Scholar : PubMed/NCBI

15 

Ries CH, Cannarile MA, Hoves S, Benz J, Wartha K, Runza V, Rey-Giraud F, Pradel LP, Feuerhake F, Klaman I, et al: Targeting tumor-associated macrophages with anti-CSF-1R antibody reveals a strategy for cancer therapy. Cancer Cell. 25:846–859. 2014. View Article : Google Scholar : PubMed/NCBI

16 

Solinas G, Germano G, Mantovani A and Allavena P: Tumor-associated macrophages (TAM) as major players of the cancer-related inflammation. J Leukoc Biol. 86:1065–1073. 2009. View Article : Google Scholar : PubMed/NCBI

17 

Mantovani A, Sozzani S, Locati M, Allavena P and Sica A: Macrophage polarization: Tumor-associated macrophages as a paradigm for polarized M2 mononuclear phagocytes. Trends Immunol. 23:549–555. 2002. View Article : Google Scholar : PubMed/NCBI

18 

Tham M, Tan KW, Keeble J, Wang X, Hubert S, Barron L, Tan NS, Kato M, Prevost-Blondel A, Angeli V and Abastado JP: Melanoma-initiating cells exploit M2 macrophage TGFbeta and arginase pathway for survival and proliferation. Oncotarget. 5:12027–12042. 2014. View Article : Google Scholar : PubMed/NCBI

19 

Yaddanapudi K, Putty K, Rendon BE, Lamont GJ, Faughn JD, Satoskar A, Lasnik A, Eaton JW and Mitchell RA: Control of tumor-associated macrophage alternative activation by macrophage migration inhibitory factor. J Immunol. 190:2984–2993. 2013. View Article : Google Scholar : PubMed/NCBI

20 

Clear AJ, Lee AM, Calaminici M, Ramsay AG, Morris KJ, Hallam S, Kelly G, Macdougall F, Lister TA and Gribben JG: Increased angiogenic sprouting in poor prognosis FL is associated with elevated numbers of CD163+ macrophages within the immediate sprouting microenvironment. Blood. 115:5053–5056. 2010. View Article : Google Scholar : PubMed/NCBI

21 

Leek RD, Lewis CE, Whitehouse R, Greenall M, Clarke J and Harris AL: Association of macrophage infiltration with angiogenesis and prognosis in invasive breast carcinoma. Cancer Res. 56:4625–4629. 1996.PubMed/NCBI

22 

Liu T, Larionova I, Litviakov N, Riabov V, Zavyalova M, Tsyganov M, Buldakov M, Song B, Moganti K, Kazantseva P, et al: Tumor-associated macrophages in human breast cancer produce new monocyte attracting and pro-angiogenic factor YKL-39 indicative for increased metastasis after neoadjuvant chemotherapy. Oncoimmunology. 7:e14369222018. View Article : Google Scholar : PubMed/NCBI

23 

Shieh YS, Hung YJ, Hsieh CB, Chen JS, Chou KC and Liu SY: Tumor-associated macrophage correlated with angiogenesis and progression of mucoepidermoid carcinoma of salivary glands. Ann Surg Oncol. 16:751–760. 2009. View Article : Google Scholar : PubMed/NCBI

24 

Marech I, Ammendola M, Sacco R, Sammarco G, Zuccalà V, Zizzo N, Leporini C, Luposella M, Patruno R, Filippelli G, et al: Tumour-associated macrophages correlate with microvascular bed extension in colorectal cancer patients. J Cell Mol Med. 20:1373–1380. 2016. View Article : Google Scholar : PubMed/NCBI

25 

Alupei MC, Licarete E, Patras L and Banciu M: Liposomal simvastatin inhibits tumor growth via targeting tumor-associated macrophages-mediated oxidative stress. Cancer Lett. 356:946–952. 2015. View Article : Google Scholar : PubMed/NCBI

26 

Banciu M, Metselaar JM, Schiffelers RM and Storm G: Antitumor activity of liposomal prednisolone phosphate depends on the presence of functional tumor-associated macrophages in tumor tissue. Neoplasia. 10:108–117. 2008. View Article : Google Scholar : PubMed/NCBI

27 

Banciu M, Schiffelers RM and Storm G: Investigation into the role of tumor-associated macrophages in the antitumor activity of Doxil. Pharm Res. 25:1948–1955. 2008. View Article : Google Scholar : PubMed/NCBI

28 

Sylvester B, Porfire A, Muntean DM, Vlase L, Lupuţ L, Licarete E, Sesarman A, Alupei MC, Banciu M, Achim M and Tomuţă I: Optimization of prednisolone-loaded long-circulating liposomes via application of quality by design (QbD) approach. J Liposome Res. 28:49–61. 2018. View Article : Google Scholar : PubMed/NCBI

29 

De Palma M and Lewis CE: Macrophage regulation of tumor responses to anticancer therapies. Cancer Cell. 23:277–286. 2013. View Article : Google Scholar : PubMed/NCBI

30 

Cortes-Funes H and Coronado C: Role of anthracyclines in the era of targeted therapy. Cardiovasc Toxicol. 7:56–60. 2007. View Article : Google Scholar : PubMed/NCBI

31 

Fink W, Zimpfer-Rechner C, Thoelke A, Figl R, Kaatz M, Ugurel S and Schadendorf D: Clinical phase II study of pegylated liposomal doxorubicin as second-line treatment in disseminated melanoma. Onkologie. 27:540–544. 2004.PubMed/NCBI

32 

Schadendorf D, Worm M, Algermissen B, Kohlmus CM and Czarnetzki BM: Chemosensitivity testing of human malignant melanoma. A retrospective analysis of clinical response and in vitro drug sensitivity. Cancer. 73:103–108. 1994. View Article : Google Scholar : PubMed/NCBI

33 

Vorobiof DA, Rapoport BL, Mahomed R and Karime M: Phase II study of pegylated liposomal doxorubicin in patients with metastatic malignant melanoma failing standard chemotherapy treatment. Melanoma Res. 13:201–203. 2003. View Article : Google Scholar : PubMed/NCBI

34 

Haase-Kohn C, Wolf S, Herwig N, Mosch B and Pietzsch J: Metastatic potential of B16-F10 melanoma cells is enhanced by extracellular S100A4 derived from RAW264.7 macrophages. Biochem Biophys Res Commun. 446:143–148. 2014. View Article : Google Scholar : PubMed/NCBI

35 

Zhang X, Goncalves R and Mosser DM: The isolation and characterization of murine macrophages. Curr Protoc Immunol. 14:Unit 14 11. 2008. View Article : Google Scholar

36 

Rauca VF, Licarete E, Luput L, Sesarman A, Patras L, Bulzu P, Rakosy-Tican E and Banciu M: Combination therapy of simvastatin and 5,6-dimethylxanthenone-4-acetic acid synergistically suppresses the aggressiveness of B16.F10 melanoma cells. PLoS One. 13:e02028272018. View Article : Google Scholar : PubMed/NCBI

37 

Banciu M, Fens MH, Storm G and Schiffelers RM: Antitumor activity and tumor localization of liposomal glucocorticoids in B16 melanoma-bearing mice. J Control Release. 127:131–136. 2008. View Article : Google Scholar : PubMed/NCBI

38 

Licarete E, Sesarman A, Rauca VF, Luput L, Patras L and Banciu M: HIF-1α acts as a molecular target for simvastatin cytotoxicity in B16.F10 melanoma cells cultured under chemically induced hypoxia. Oncol Lett. 13:3942–3950. 2017. View Article : Google Scholar : PubMed/NCBI

39 

Alupei MC, Licarete E, Cristian FB and Banciu M: Cytotoxicity of lipophilic statins depends on their combined actions on HIF-1α expression and redox status in B16.F10 melanoma cells. Anticancer Drugs. 25:393–405. 2014. View Article : Google Scholar : PubMed/NCBI

40 

Karatas F, Karatepe M and Baysar A: Determination of free malondialdehyde in human serum by high-performance liquid chromatography. Anal Biochem. 311:76–79. 2002. View Article : Google Scholar : PubMed/NCBI

41 

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 : PubMed/NCBI

42 

Chou TC and Talalay P: Quantitative analysis of dose-effect relationships: The combined effects of multiple drugs or enzyme inhibitors. Adv Enzyme Regul. 22:27–55. 1984. View Article : Google Scholar : PubMed/NCBI

43 

Chou TC: Theoretical basis, experimental design, and computerized simulation of synergism and antagonism in drug combination studies. Pharmacol Rev. 58:621–681. 2006. View Article : Google Scholar : PubMed/NCBI

44 

Venza M, Visalli M, Beninati C, De Gaetano GV, Teti D and Venza I: Cellular mechanisms of oxidative stress and action in melanoma. Oxid Med Cell Longev. 2015:4817822015. View Article : Google Scholar : PubMed/NCBI

45 

Rőszer T: Understanding the mysterious M2 macrophage through activation markers and effector mechanisms. Mediators Inflamm. 2015:8164602015. View Article : Google Scholar : PubMed/NCBI

46 

Larionova I, Cherdyntseva N, Liu T, Patysheva M, Rakina M and Kzhyshkowska J: Interaction of tumor-associated macrophages and cancer chemotherapy. Oncoimmunology. 8:15960042019. View Article : Google Scholar : PubMed/NCBI

47 

Manzano JL, Layos L, Bugés C, de Los Llanos Gil M, Vila L, Martínez-Balibrea E and Martínez-Cardús A: Resistant mechanisms to BRAF inhibitors in melanoma. Ann Transl Med. 4:2372016. View Article : Google Scholar : PubMed/NCBI

48 

Winder M and Viros A: Mechanisms of drug resistance in melanoma. Handb Exp Pharmacol. 249:91–108. 2018. View Article : Google Scholar : PubMed/NCBI

49 

Vera RE, Lamberti MJ, Rivarola VA and Rumie Vittar NB: Developing strategies to predict photodynamic therapy outcome: The role of melanoma microenvironment. Tumour Biol. 36:9127–9136. 2015. View Article : Google Scholar : PubMed/NCBI

50 

Klemm F and Joyce JA: Microenvironmental regulation of therapeutic response in cancer. Trends Cell Biol. 25:198–213. 2015. View Article : Google Scholar : PubMed/NCBI

51 

Szebeni GJ, Vizler C, Kitajka K and Puskas LG: Inflammation and cancer: Extra- and intracellular determinants of tumor-associated macrophages as tumor promoters. Mediators Inflamm. 2017:92940182017. View Article : Google Scholar : PubMed/NCBI

52 

Gajewski TF: Identifying and overcoming immune resistance mechanisms in the melanoma tumor microenvironment. Clin Cancer Res. 12:2326s–2330s. 2006. View Article : Google Scholar : PubMed/NCBI

53 

Varney ML, Olsen KJ, Mosley RL and Singh RK: Paracrine regulation of vascular endothelial growth factor-a expression during macrophage-melanoma cell interaction: Role of monocyte chemotactic protein-1 and macrophage colony-stimulating factor. J Interferon Cytokine Res. 25:674–683. 2005. View Article : Google Scholar : PubMed/NCBI

54 

Wang T, Ge Y, Xiao M, Lopez-Coral A, Azuma R, Somasundaram R, Zhang G, Wei Z, Xu X, Rauscher FJ III, et al: Melanoma-derived conditioned media efficiently induce the differentiation of monocytes to macrophages that display a highly invasive gene signature. Pigment Cell Melanoma Res. 25:493–505. 2012. View Article : Google Scholar : PubMed/NCBI

55 

Ruffell B and Coussens LM: Macrophages and therapeutic resistance in cancer. Cancer Cell. 27:462–472. 2015. View Article : Google Scholar : PubMed/NCBI

56 

Banciu M, Metselaar JM, Schiffelers RM and Storm G: Liposomal glucocorticoids as tumor-targeted anti-angiogenic nanomedicine in B16 melanoma-bearing mice. J Steroid Biochem Mol Biol. 111:101–110. 2008. View Article : Google Scholar : PubMed/NCBI

57 

Gouaze V, Mirault ME, Carpentier S, Salvayre R, Levade T and Andrieu-Abadie N: Glutathione peroxidase-1 overexpression prevents ceramide production and partially inhibits apoptosis in doxorubicin-treated human breast carcinoma cells. Mol Pharmacol. 60:488–496. 2001.PubMed/NCBI

58 

Ubezio P and Civoli F: Flow cytometric detection of hydrogen peroxide production induced by doxorubicin in cancer cells. Free Radic Biol Med. 16:509–516. 1994. View Article : Google Scholar : PubMed/NCBI

59 

Berthiaume JM and Wallace KB: Adriamycin-induced oxidative mitochondrial cardiotoxicity. Cell Biol Toxicol. 23:15–25. 2007. View Article : Google Scholar : PubMed/NCBI

60 

Wang S, Konorev EA, Kotamraju S, Joseph J, Kalivendi S and Kalyanaraman B: Doxorubicin induces apoptosis in normal and tumor cells via distinctly different mechanisms. Intermediacy of H(2)O(2)- and p53-dependent pathways. J Biol Chem. 279:25535–25543. 2004. View Article : Google Scholar : PubMed/NCBI

61 

Verma N and Vinayak M: A low dose of doxorubicin improves antioxidant defence system and modulates anaerobic metabolism during the development of lymphoma. Indian J Pharmacol. 44:308–313. 2012. View Article : Google Scholar : PubMed/NCBI

62 

Pritsos CA and Ma J: Basal and drug-induced antioxidant enzyme activities correlate with age-dependent doxorubicin oxidative toxicity. Chem Biol Interact. 127:1–11. 2000. View Article : Google Scholar : PubMed/NCBI

63 

Dong QM, Ling C, Chen X and Zhao LI: Inhibition of tumor necrosis factor-α enhances apoptosis induced by nuclear factor-kB inhibition in leukemia cells. Oncol Lett. 10:3793–3798. 2015. View Article : Google Scholar : PubMed/NCBI

64 

Kirito K, Watanabe T, Sawada K, Endo H, Ozawa K and Komatsu N: Thrombopoietin regulates Bcl-xL gene expression through Stat5 and phosphatidylinositol 3-kinase activation pathways. J Biol Chem. 277:8329–8337. 2002. View Article : Google Scholar : PubMed/NCBI

65 

Nalluri S, Ghoshal-Gupta S, Kutiyanawalla A, Gayatri S, Lee BR, Jiwani S, Rojiani AM and Rojiani MV: TIMP-1 inhibits apoptosis in lung adenocarcinoma cells via interaction with Bcl-2. PLoS One. 10:e01376732015. View Article : Google Scholar : PubMed/NCBI

66 

Valacca C, Tassone E and Mignatti P: TIMP-2 interaction with MT1-MMP activates the AKT pathway and protects tumor cells from apoptosis. PLoS One. 10:e01367972015. View Article : Google Scholar : PubMed/NCBI

67 

Valente P, Fassina G, Melchiori A, Masiello L, Cilli M, Vacca A, Onisto M, Santi L, Stetler-Stevenson WG and Albini A: TIMP-2 over-expression reduces invasion and angiogenesis and protects B16F10 melanoma cells from apoptosis. Int J Cancer. 75:246–253. 1998. View Article : Google Scholar : PubMed/NCBI

68 

Georgoudaki AM, Prokopec KE, Boura VF, Hellqvist E, Sohn S, Östling J, Dahan R, Harris RA, Rantalainen M, Klevebring D, et al: Reprogramming tumor-associated macrophages by antibody targeting inhibits cancer progression and metastasis. Cell Rep. 15:2000–2011. 2016. View Article : Google Scholar : PubMed/NCBI

69 

Sica A and Mantovani A: Macrophage plasticity and polarization: In vivo veritas. J Clin Invest. 122:787–795. 2012. View Article : Google Scholar : PubMed/NCBI

70 

Zheng X, Turkowski K, Mora J, Brüne B, Seeger W, Weigert A and Savai R: Redirecting tumor-associated macrophages to become tumoricidal effectors as a novel strategy for cancer therapy. Oncotarget. 8:48436–48452. 2017.PubMed/NCBI

Related Articles

  • Abstract
  • View
  • Download
  • Twitter
Copy and paste a formatted citation
Spandidos Publications style
Licarete E, Rauca VF, Luput L, Patras L, Sesarman A and Banciu M: The prednisolone phosphate‑induced suppression of the angiogenic function of tumor‑associated macrophages enhances the antitumor effects of doxorubicin on B16.F10 murine melanoma cells in vitro. Oncol Rep 42: 2694-2705, 2019.
APA
Licarete, E., Rauca, V.F., Luput, L., Patras, L., Sesarman, A., & Banciu, M. (2019). The prednisolone phosphate‑induced suppression of the angiogenic function of tumor‑associated macrophages enhances the antitumor effects of doxorubicin on B16.F10 murine melanoma cells in vitro. Oncology Reports, 42, 2694-2705. https://doi.org/10.3892/or.2019.7346
MLA
Licarete, E., Rauca, V. F., Luput, L., Patras, L., Sesarman, A., Banciu, M."The prednisolone phosphate‑induced suppression of the angiogenic function of tumor‑associated macrophages enhances the antitumor effects of doxorubicin on B16.F10 murine melanoma cells in vitro". Oncology Reports 42.6 (2019): 2694-2705.
Chicago
Licarete, E., Rauca, V. F., Luput, L., Patras, L., Sesarman, A., Banciu, M."The prednisolone phosphate‑induced suppression of the angiogenic function of tumor‑associated macrophages enhances the antitumor effects of doxorubicin on B16.F10 murine melanoma cells in vitro". Oncology Reports 42, no. 6 (2019): 2694-2705. https://doi.org/10.3892/or.2019.7346
Copy and paste a formatted citation
x
Spandidos Publications style
Licarete E, Rauca VF, Luput L, Patras L, Sesarman A and Banciu M: The prednisolone phosphate‑induced suppression of the angiogenic function of tumor‑associated macrophages enhances the antitumor effects of doxorubicin on B16.F10 murine melanoma cells in vitro. Oncol Rep 42: 2694-2705, 2019.
APA
Licarete, E., Rauca, V.F., Luput, L., Patras, L., Sesarman, A., & Banciu, M. (2019). The prednisolone phosphate‑induced suppression of the angiogenic function of tumor‑associated macrophages enhances the antitumor effects of doxorubicin on B16.F10 murine melanoma cells in vitro. Oncology Reports, 42, 2694-2705. https://doi.org/10.3892/or.2019.7346
MLA
Licarete, E., Rauca, V. F., Luput, L., Patras, L., Sesarman, A., Banciu, M."The prednisolone phosphate‑induced suppression of the angiogenic function of tumor‑associated macrophages enhances the antitumor effects of doxorubicin on B16.F10 murine melanoma cells in vitro". Oncology Reports 42.6 (2019): 2694-2705.
Chicago
Licarete, E., Rauca, V. F., Luput, L., Patras, L., Sesarman, A., Banciu, M."The prednisolone phosphate‑induced suppression of the angiogenic function of tumor‑associated macrophages enhances the antitumor effects of doxorubicin on B16.F10 murine melanoma cells in vitro". Oncology Reports 42, no. 6 (2019): 2694-2705. https://doi.org/10.3892/or.2019.7346
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