Monocyte-Induced Prostate Cancer Cell Invasion is Mediated by Chemokine Ligand 2 and Nuclear Factor-κB Activity

Overview

Journal J Clin Cell Immunol

Publisher Omics Publishing Group

Date 2015 Aug 29

PMID 26317041

Citations 18

Authors

Paul F Lindholm

Neela Sivapurapu

Borko Jovanovic

Andre Kajdacsy-Balla

Affiliations

Soon will be listed here.

Abstract

Study Background: The tumor microenvironment contains inflammatory cells which can influence cancer growth and progression; however the mediators of these effects vary with different cancer types. The mechanisms by which prostate cancer cells communicate with monocytes to promote cancer progression are incompletely understood. This study tested prostate cancer cell and monocyte interactions that lead to increased prostate cancer cell invasion.

Methods: We analyzed the prostate cancer cell invasion and NF-κB activity and cytokine expression during interaction with monocyte-lineage cells in co-cultures. The roles of monocyte chemotactic factor (MCP-1/CCL2) and NF-κB activity for co-culture induced prostate cancer invasion were tested. Clinical prostate cancer NF-κB expression was analyzed by immunohistochemistry.

Results: In co-cultures of prostate cancer cell lines with monocyte-lineage cells, (C-C motif) ligand 2 (CCL2) levels were significantly increased when compared with monocytes or cancer cells cultured alone. Prostate cancer cell invasion was induced by recombinant CCL2 in a dose dependent manner, similar to co-cultures with monocytes. The monocyte-induced prostate cancer cell invasion was inhibited by CCL2 neutralizing antibodies and by the CCR2 inhibitor, RS102895. Prostate cancer cell invasion and CCL2 expression induced in the co-cultures was inhibited by Lactacystin and Bay11-7082 NF-κB inhibitors. Prostate cancer cell NF-κB DNA binding activity depended on CCL2 dose and was inhibited by CCL2 neutralizing antibodies. Clinical prostate cancer NF-κB expression correlated with tumor grade.

Conclusions: Co-cultures with monocyte-lineage cell lines stimulated increased prostate cancer cell invasion through increased CCL2 expression and increased prostate cancer cell NF-κB activity. CCL2 and NF-κB may be useful therapeutic targets to interfere with inflammation-induced prostate cancer invasion.

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References

Quail D, Joyce J . Microenvironmental regulation of tumor progression and metastasis. Nat Med. 2013; 19(11):1423-37. PMC: 3954707. DOI: 10.1038/nm.3394. View

Ellis C, Dyson M, Stephenson T, Maltby E . HER2 amplification status in breast cancer: a comparison between immunohistochemical staining and fluorescence in situ hybridisation using manual and automated quantitative image analysis scoring techniques. J Clin Pathol. 2005; 58(7):710-4. PMC: 1770709. DOI: 10.1136/jcp.2004.023424. View

Zhang J, Patel L, Pienta K . CC chemokine ligand 2 (CCL2) promotes prostate cancer tumorigenesis and metastasis. Cytokine Growth Factor Rev. 2009; 21(1):41-8. PMC: 2857769. DOI: 10.1016/j.cytogfr.2009.11.009. View

Hodge J, Bub J, Kaul S, Kajdacsy-Balla A, Lindholm P . Requirement of RhoA activity for increased nuclear factor kappaB activity and PC-3 human prostate cancer cell invasion. Cancer Res. 2003; 63(6):1359-64. View

Hernandez L, Smirnova T, Kedrin D, Wyckoff J, Zhu L, Stanley E . The EGF/CSF-1 paracrine invasion loop can be triggered by heregulin beta1 and CXCL12. Cancer Res. 2009; 69(7):3221-7. PMC: 2820720. DOI: 10.1158/0008-5472.CAN-08-2871. View

Zhang J, Lu Y, Pienta K . Multiple roles of chemokine (C-C motif) ligand 2 in promoting prostate cancer growth. J Natl Cancer Inst. 2010; 102(8):522-8. PMC: 2857800. DOI: 10.1093/jnci/djq044. View

Varney M, Olsen K, Mosley R, Singh R . 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. 2005; 25(11):674-83. DOI: 10.1089/jir.2005.25.674. View

Ramudo L, Yubero S, Manso M, Vicente S, De Dios I . Signal transduction of MCP-1 expression induced by pancreatitis-associated ascitic fluid in pancreatic acinar cells. J Cell Mol Med. 2009; 13(7):1314-20. PMC: 4496145. DOI: 10.1111/j.1582-4934.2008.00529.x. View

Repesh L . A new in vitro assay for quantitating tumor cell invasion. Invasion Metastasis. 1989; 9(3):192-208. View

10.

Cai K, Qi D, Hou X, Wang O, Chen J, Deng B . MCP-1 upregulates amylin expression in murine pancreatic β cells through ERK/JNK-AP1 and NF-κB related signaling pathways independent of CCR2. PLoS One. 2011; 6(5):e19559. PMC: 3092759. DOI: 10.1371/journal.pone.0019559. View

11.

Sutcliffe A, Clarke D, Bradbury D, Corbett L, Patel J, Knox A . Transcriptional regulation of monocyte chemotactic protein-1 release by endothelin-1 in human airway smooth muscle cells involves NF-kappaB and AP-1. Br J Pharmacol. 2009; 157(3):436-50. PMC: 2707990. DOI: 10.1111/j.1476-5381.2009.00143.x. View

12.

Karin M . Nuclear factor-kappaB in cancer development and progression. Nature. 2006; 441(7092):431-6. DOI: 10.1038/nature04870. View

13.

Grivennikov S, Greten F, Karin M . Immunity, inflammation, and cancer. Cell. 2010; 140(6):883-99. PMC: 2866629. DOI: 10.1016/j.cell.2010.01.025. View

14.

Harkonen P, Vaananen H . Monocyte-macrophage system as a target for estrogen and selective estrogen receptor modulators. Ann N Y Acad Sci. 2007; 1089:218-27. DOI: 10.1196/annals.1386.045. View

15.

Yamasaki A, Kameda C, Xu R, Tanaka H, Tasaka T, Chikazawa N . Nuclear factor kappaB-activated monocytes contribute to pancreatic cancer progression through the production of Shh. Cancer Immunol Immunother. 2009; 59(5):675-86. PMC: 11030800. DOI: 10.1007/s00262-009-0783-7. View

16.

Mohamed M, Cavallo-Medved D, Rudy D, Anbalagan A, Moin K, Sloane B . Interleukin-6 increases expression and secretion of cathepsin B by breast tumor-associated monocytes. Cell Physiol Biochem. 2010; 25(2-3):315-24. PMC: 3030463. DOI: 10.1159/000276564. View

17.

Lu T, Stark G . Cytokine overexpression and constitutive NFkappaB in cancer. Cell Cycle. 2004; 3(9):1114-7. View

18.

Kuo P, Shen K, Hung S, Hsu Y . CXCL1/GROα increases cell migration and invasion of prostate cancer by decreasing fibulin-1 expression through NF-κB/HDAC1 epigenetic regulation. Carcinogenesis. 2012; 33(12):2477-87. DOI: 10.1093/carcin/bgs299. View

19.

Lu Y, Cai Z, Galson D, Xiao G, Liu Y, George D . Monocyte chemotactic protein-1 (MCP-1) acts as a paracrine and autocrine factor for prostate cancer growth and invasion. Prostate. 2006; 66(12):1311-8. DOI: 10.1002/pros.20464. View

20.

Pyonteck S, Akkari L, Schuhmacher A, Bowman R, Sevenich L, Quail D . CSF-1R inhibition alters macrophage polarization and blocks glioma progression. Nat Med. 2013; 19(10):1264-72. PMC: 3840724. DOI: 10.1038/nm.3337. View