Cannabinoid receptor-2 agonist inhibits macrophage induced EMT in non-small cell lung cancer by downregulation of EGFR pathway

Molecular Carcinogenesis

Volumn 55, Issue 12, 2016, Pages 2063-2076

  Ravi, Janani ^a   Elbaz, Mohamad ^a   Wani, Nissar A ^a   Nasser, Mohd W ^a   Ganju, Ramesh K ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

EGFR; EMT; JWH 015; NSCLC; TAM

Indexed keywords

2 METHYL 3 (1 NAPHTHOYL) 1 PROPYLINDOLE; 5 (4 CHLORO 3 METHYLPHENYL) 1 (4 METHYLBENZYL) N (1,3,3 TRIMETHYLBICYCLO[2.2.1]HEPTAN 2 YL) 3 PYRAZOLECARBOXAMIDE; ARGINASE 1; CANNABINOID 2 RECEPTOR; CD31 ANTIGEN; EPIDERMAL GROWTH FACTOR RECEPTOR; FOCAL ADHESION KINASE; GAMMA INTERFERON; GELATINASE A; INTERLEUKIN 10; INTERLEUKIN 4; KI 67 ANTIGEN; MESSENGER RNA; NERVE CELL ADHESION MOLECULE; TRANSCRIPTION FACTOR SLUG; TRANSCRIPTION FACTOR SNAIL; UVOMORULIN; VASCULAR CELL ADHESION MOLECULE 1; ANTINEOPLASTIC AGENT; INDOLE DERIVATIVE; JHW 015;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIPROLIFERATIVE ACTIVITY; ARTICLE; CANCER INHIBITION; CELL INFILTRATION; CONTROLLED STUDY; DOWN REGULATION; EPITHELIAL MESENCHYMAL TRANSITION; HUMAN; HUMAN CELL; MACROPHAGE; MALE; MESENCHYME CELL; MOUSE; NON SMALL CELL LUNG CANCER; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TUMOR ASSOCIATED LEUKOCYTE; A-549 CELL LINE; AGONISTS; ANIMAL; DRUG EFFECTS; LUNG; LUNG TUMOR; METABOLISM; PATHOLOGY; SIGNAL TRANSDUCTION;

A549 CELLS; ANIMALS; ANTINEOPLASTIC AGENTS; CARCINOMA, NON-SMALL-CELL LUNG; DOWN-REGULATION; EPITHELIAL-MESENCHYMAL TRANSITION; HUMANS; INDOLES; LUNG; LUNG NEOPLASMS; MACROPHAGES; MICE; RECEPTOR, CANNABINOID, CB2; RECEPTOR, EPIDERMAL GROWTH FACTOR; SIGNAL TRANSDUCTION;

EID: 84953791121     PISSN: 08991987     EISSN: 10982744     Source Type: Journal    
DOI: 10.1002/mc.22451     Document Type: Article

References (46)

1. Dearing KR, Sangal A, Weiss GJ. Maintaining clarity: Review of maintenance therapy in non-small cell lung cancer. World J Clin Oncol 2014; 5:103–113.
2. Cooper WA, Lam DC, O'Toole SA, Minna JD. Molecular biology of lung cancer. J Thorac Dis 2013; 5:S479–S490.
3. Seshacharyulu P, Ponnusamy MP, Haridas D, Jain M, Ganti AK, Batra SK. Targeting the EGFR signaling pathway in cancer therapy. Expert Opin Ther Targets 2012; 16:15–31.
4. Mitsudomi T, Yatabe Y. Mutations of the epidermal growth factor receptor gene and related genes as determinants of epidermal growth factor receptor tyrosine kinase inhibitors sensitivity in lung cancer. Cancer Sci 2007; 98:1817–1824.
5. Sato M, Shames DS, Hasegawa Y. Emerging evidence of epithelial-to-mesenchymal transition in lung carcinogenesis. Respirology 2012; 17:1048–1059.
6. Barr S, Thomson S, Buck E, et al. Bypassing cellular EGF receptor dependence through epithelial-to-mesenchymal-like transitions. Clin Exp Metastasis 2008; 25:685–693.
7. Tsai JH, Yang J. Epithelial-mesenchymal plasticity in carcinoma metastasis. Genes Dev 2013; 27:2192–2206.
8. Fang H, Declerck YA. Targeting the tumor microenvironment: From understanding pathways to effective clinical trials. Cancer Res 2013; 73:4965–4977.
9. Sounni NE, Noel A. Targeting the tumor microenvironment for cancer therapy. Clin Chem 2013; 59:85–93.
10. Ruffell B, Affara NI, Coussens LM. Differential macrophage programming in the tumor microenvironment. Trends Immunol 2012; 33:119–126.
11. Liu CY, Xu JY, Shi XY, et al. M2-polarized tumor-associated macrophages promoted epithelial-mesenchymal transition in pancreatic cancer cells, partially through TLR4/IL-10 signaling pathway. Lab Invest 2013; 93:844–854.
12. Lin CY, Lin CJ, Chen KH, Wu JC, Huang SH, Wang SM. Macrophage activation increases the invasive properties of hepatoma cells by destabilization of the adherens junction. FEBS Lett 2006; 580:3042–3050.
13. Vlaicu P, Mertins P, Mayr T, et al. Monocytes/macrophages support mammary tumor invasivity by co-secreting lineage-specific EGFR ligands and a STAT3 activator. BMC Cancer 2013; 13:197.
14. Alexander A, Smith PF, Rosengren RJ. Cannabinoids in the treatment of cancer. Cancer Lett 2009; 285:6–12.
15. Nasser MW, Qamri Z, Deol YS, et al. Crosstalk between chemokine receptor CXCR4 and cannabinoid receptor CB2 in modulating breast cancer growth and invasion. PLoS ONE 2011; 6:e23901.
16. Olea-Herrero N, Vara D, Malagarie-Cazenave S, Diaz-Laviada I. Inhibition of human tumour prostate PC-3 cell growth by cannabinoids R(+)-Methanandamide and JWH-015: Involvement of CB2. Br J Cancer 2009; 101:940–950.
17. Preet A, Qamri Z, Nasser MW, et al. Cannabinoid receptors, CB1 and CB2, as novel targets for inhibition of non-small cell lung cancer growth and metastasis. Cancer Prev Res (Phila) 2011; 4:65–75.
18. Elbaz M, Nasser MW, Ravi J, et al. Modulation of the tumor microenvironment and inhibition of EGF/EGFR pathway; novel anti-tumor mechanisms of Cannabidiol in breast cancer. Mol Oncol 2015; 9:906–919.
19. Nasser MW, Qamri Z, Deol YS, et al. S100A7 enhances mammary tumorigenesis through upregulation of inflammatory pathways. Cancer Res 2012; 72:604–615.
20. Qamri Z, Preet A, Nasser MW, et al. Synthetic cannabinoid receptor agonists inhibit tumor growth and metastasis of breast cancer. Mol Cancer Ther 2009; 8:3117–3129.
21. Deol YS, Nasser MW, Yu L, Zou X, Ganju RK. Tumor-suppressive effects of psoriasin (S100A7) are mediated through the beta-catenin/T cell factor 4 protein pathway in estrogen receptor-positive breast cancer cells. J Biol Chem 2011; 286:44845–44854.
22. Sneh A, Deol YS, Ganju A, et al. Differential role of psoriasin (S100A7) in estrogen receptor alpha positive and negative breast cancer cells occur through actin remodeling. Breast Cancer Res Treat 2013; 138:727–739.
23. Ravi J, Sneh A, Shilo K, Nasser MW, Ganju RK. FAAH inhibition enhances anandamide mediated anti-tumorigenic effects in non-small cell lung cancer by downregulating the EGF/EGFR pathway. Oncotarget 2014; 5:2475–2486.
24. Wani N, Nasser MW, Ahirwar DK, et al. C-X-C motif chemokine 12/C-X-C chemokine receptor type 7 signaling regulates breast cancer growth and metastasis by modulating the tumor microenvironment. Breast Cancer Res 2014; 16:R54.
25. Yamaguchi H, Wyckoff J, Condeelis J. Cell migration in tumors. Curr Opin Cell Biol 2005; 17:559–564.
26. Perlikos F, Harrington KJ, Syrigos KN. Key molecular mechanisms in lung cancer invasion and metastasis: A comprehensive review. Crit Rev Oncol Hematol 2013; 87:1–11.
27. Zhao J, Guan JL. Signal transduction by focal adhesion kinase in cancer. Cancer Metastasis Rev 2009; 28:35–49.
28. Ding YB, Chen GY, Xia JG, Zang XW, Yang HY, Yang L. Association of VCAM-1 overexpression with oncogenesis, tumor angiogenesis and metastasis of gastric carcinoma. World J Gastroenterol 2003; 9:1409–1414.
29. Shintani Y, Maeda M, Chaika N, Johnson KR, Wheelock MJ. Collagen I promotes epithelial-to-mesenchymal transition in lung cancer cells via transforming growth factor-beta signaling. Am J Respir Cell Mol Biol 2008; 38:95–104.
30. Garofalo M, Romano G, Di Leva G, et al. EGFR and MET receptor tyrosine kinase-altered microRNA expression induces tumorigenesis and gefitinib resistance in lung cancers. Nat Med 2012; 18:74–82.
31. Shou Y, Hirano T, Gong Y, et al. Influence of angiogenetic factors and matrix metalloproteinases upon tumour progression in non-small-cell lung cancer. Br J Cancer 2001; 85:1706–1712.
32. da Cunha Santos G, Shepherd FA, Tsao MS. EGFR mutations and lung cancer. Annu Rev Pathol 2011; 6:49–69.
33. Dehai C, Bo P, Qiang T, et al. Enhanced invasion of lung adenocarcinoma cells after co-culture with THP-1-derived macrophages via the induction of EMT by IL-6. Immunol Lett 2014; 160:1–10.
34. Goncalves BF, Campos SG, Costa CF, Scarano WR, Goes RM, Taboga SR. Key participants of the tumor microenvironment of the prostate: An approach of the structural dynamic of cellular elements and extracellular matrix components during epithelial-stromal transition. Acta Histochem 2015; 117:4–13.
35. Cridge BJ, Rosengren RJ. Critical appraisal of the potential use of cannabinoids in cancer management. Cancer Manag Res 2013; 5:301–313.
36. Freimuth N, Ramer R, Hinz B. Antitumorigenic effects of cannabinoids beyond apoptosis. J Pharmacol Exp Ther 2010; 332:336–344.
37. Chakravarti B, Ravi J, Ganju RK. Cannabinoids as therapeutic agents in cancer: Current status and future implications. Oncotarget 2014; 5:5852–5872.
38. Sarfaraz S, Adhami VM, Syed DN, Afaq F, Mukhtar H. Cannabinoids for cancer treatment: Progress and promise. Cancer Res 2008; 68:339–342.
39. Vara D, Salazar M, Olea-Herrero N, Guzman M, Velasco G, Diaz-Laviada I. Anti-tumoral action of cannabinoids on hepatocellular carcinoma: Role of AMPK-dependent activation of autophagy. Cell Death Differ 2011; 18:1099–1111.
40. Vara D, Morell C, Rodriguez-Henche N, Diaz-Laviada I. Involvement of PPARgamma in the antitumoral action of cannabinoids on hepatocellular carcinoma. Cell Death Dis 2013; 4:e618.
41. Emery SM, Alotaibi MR, Tao Q, Selley DE, Lichtman AH, Gewirtz DA. Combined antiproliferative effects of the aminoalkylindole WIN55, 212–2 and radiation in breast cancer cells. J Pharmacol Exp Ther 2014; 348:293–302.
42. McKallip RJ, Lombard C, Fisher M, et al. Targeting CB2 cannabinoid receptors as a novel therapy to treat malignant lymphoblastic disease. Blood 2002; 100:627–634.
43. Shih JY, Yang PC. The EMT regulator slug and lung carcinogenesis. Carcinogenesis 2011; 32:1299–1304.
44. Roberts PJ, Der CJ. Targeting the Raf-MEK-ERK mitogen-activated protein kinase cascade for the treatment of cancer. Oncogene 2007; 26:3291–3310.
45. Goubran HA, Kotb RR, Stakiw J, Emara ME, Burnouf T. Regulation of tumor growth and metastasis: the role of tumor microenvironment. Cancer Growth Metastasis 2014; 7:9–18.
46. Xu K, Ling J, Dong Z, Yu FX. Wound induced HB-EGF ectodomain shedding and EGFR activation in corneal epithelial cells. Invest Ophthalmol Vis Sci 2004; 45:813–820.