Feed-forward reciprocal activation of PAFR and STAT3 regulates epithelial-mesenchymal transition in non-small cell lung cancer

Cancer Research

Volumn 75, Issue 19, 2015, Pages 4198-4210

  Chen, Jie ^a   Lan, Tian ^a,b   Zhang, Weimin ^a   Dong, Lijia ^a   Kang, Nan ^a   Zhang, Shumin ^a   Fu, Ming ^a   Liu, Bing ^c   Liu, Kangtai ^d   Zhan, Qimin ^a  

^a CANCER HOSPITAL   (China)

^b CAPITAL MEDICAL UNIVERSITY   (China)

^c GUANGDONG PHARMACEUTICAL UNIVERSITY   (China)

^d TSINGHUA UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 6; JANUS KINASE 2; NERVE CELL ADHESION MOLECULE; PROTEIN TYROSINE KINASE; STAT3 PROTEIN; THROMBOCYTE ACTIVATING FACTOR RECEPTOR; TRANSCRIPTION FACTOR SNAIL; TRANSCRIPTION FACTOR ZEB1; UVOMORULIN; VIMENTIN; FIBRINOGEN RECEPTOR; G PROTEIN COUPLED RECEPTOR; GUANINE NUCLEOTIDE BINDING PROTEIN; IL6 PROTEIN, HUMAN; PROTEIN KINASE; SMALL INTERFERING RNA; STAT3 PROTEIN, HUMAN; TUMOR PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; CANCER GROWTH; CANCER PROGNOSIS; CARCINOGENICITY; CELL INVASION; CELL PROLIFERATION; CELL VIABILITY; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NON SMALL CELL LUNG CANCER; NONHUMAN; OVERALL SURVIVAL; POSITIVE FEEDBACK; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; RECEPTOR DOWN REGULATION; SIGNAL TRANSDUCTION; UPREGULATION; ADULT; AGED; ANIMAL; BIOSYNTHESIS; BREAST TUMOR; CANCER TRANSPLANTATION; CARCINOMA; COLORECTAL TUMOR; DISEASE COURSE; FEEDBACK SYSTEM; GENETICS; LUNG TUMOR; MALE; METABOLISM; MIDDLE AGED; NUDE MOUSE; PATHOLOGY; PHYSIOLOGY; STOMACH TUMOR; TUMOR CELL LINE; TUMOR INVASION; XENOGRAFT;

ADULT; AGED; ANIMALS; BREAST NEOPLASMS; CARCINOMA; CARCINOMA, NON-SMALL-CELL LUNG; CELL LINE, TUMOR; COLORECTAL NEOPLASMS; DISEASE PROGRESSION; ENZYME ACTIVATION; EPITHELIAL-MESENCHYMAL TRANSITION; FEEDBACK, PHYSIOLOGICAL; FEMALE; GTP-BINDING PROTEINS; HETEROGRAFTS; HUMANS; INTERLEUKIN-6; LUNG NEOPLASMS; MALE; MICE; MICE, NUDE; MIDDLE AGED; NEOPLASM INVASIVENESS; NEOPLASM PROTEINS; NEOPLASM TRANSPLANTATION; PLATELET MEMBRANE GLYCOPROTEINS; PROTEIN KINASES; RECEPTORS, G-PROTEIN-COUPLED; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; STOMACH NEOPLASMS; UP-REGULATION;

EID: 84945541320     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-15-1062     Document Type: Article

References (50)

1. Muller-Tidow C, Diederichs S, Bulk E, Pohle T, Steffen B, Schwable J, et al. Identification of metastasis-associated receptor tyrosine kinases in nonsmall cell lung cancer. Cancer Res 2005;65:1778-82.
2. Herbst RS, Heymach JV, Lippman SM. Lung cancer. N Engl J Med 2008; 359:1367-80.
3. Dorsam RT, Gutkind JS. G-protein-coupled receptors and cancer. Nat Rev Cancer 2007;7:79-94.
4. Nikitenko LL, Leek R, Henderson S, Pillay N, Turley H, Generali D, et al. The G-protein-coupled receptor CLR is upregulated in an autocrine loop with adrenomedullin in clear cell renal cell carcinoma and associated with poor prognosis. Clin Cancer Res 2013;19:5740-8.
5. Mills GB, Moolenaar WH. The emerging role of lysophosphatidic acid in cancer. Nat Rev Cancer 2003;3:582-91.
6. Cundell DR, Gerard NP, Gerard C, Idanpaan-Heikkila I, Tuomanen EI. Streptococcus pneumoniae anchor to activated human cells by the receptor for platelet-activating factor. Nature 1995;377:435-8.
7. Melnikova VO, Villares GJ, Bar-Eli M. Emerging roles of PAR-1 and PAFR in melanoma metastasis. Cancer Microenviron 2008;1:103-11.
8. Cellai C, Laurenzana A, Vannucchi AM, Caporale R, Paglierani M, Di Lollo S, et al. Growth inhibition and differentiation of human breast cancer cells by the PAFR antagonist WEB-2086. Br J Cancer 2006;94: 1637-42.
9. Aponte M, Jiang W, Lakkis M, Li MJ, Edwards D, Albitar L, et al. Activation of platelet-activating factor receptor and pleiotropic effects on tyrosine phospho-EGFR/Src/FAK/paxillin in ovarian cancer. Cancer Res 2008;68:5839-48.
10. Radisky DC, Levy DD, Littlepage LE, Liu H, Nelson CM, Fata JE, et al. Rac1b and reactive oxygen species mediate MMP-3-induced EMT and genomic instability. Nature 2005;436:123-7.
11. Thiery JP. Epithelial-mesenchymal transitions in cancer onset and progression. Bull Acad Natl Med 2009;193:1969-78
12. Voulgari A, Pintzas A. Epithelial-mesenchymal transition in cancer metastasis: mechanisms, markers and strategies to overcome drug resistance in the clinic. Biochim Biophys Acta 2009;1796:75-90.
13. Kim WH, Chon CY, Moon YM, Kang JK, Park IS, Choi HJ. Effect of anticancer drugs and desferrioxamine in combination with radiation on hepatoma cell lines. Yonsei Med J 1993;34:45-56.
14. Epling-Burnette PK, Liu JH, Catlett-Falcone R, Turkson J, Oshiro M, Kothapalli R, et al. Inhibition of STAT3 signaling leads to apoptosis of leukemic large granular lymphocytes and decreased Mcl-1 expression. J Clin Invest 2001;107:351-62.
15. Shinozaki K, Kawasaki T, Kambayashi J, Sakon M, Shiba E, Uemura Y, et al. A new method of purification and sensitive bioassay of plateletactivating factor (PAF) in human whole blood. Life Sci 1994;54: 429-37.
16. Denizot Y, Desplat V, Drouet M, Bertin F, Melloni B. Is there a role of platelet-activating factor in human lung cancer? Lung Cancer 2001;33: 195-202.
17. Huang C, Yang G, Jiang T, Zhu G, Li H, Qiu Z. The effects and mechanisms of blockage of STAT3 signaling pathway on IL-6 inducing EMT in human pancreatic cancer cells in vitro. Neoplasma 2011;58:396-405.
18. Xiong H, Hong J, Du W, Lin YW, Ren LL, Wang YC, et al. Roles of STAT3 and ZEB1 proteins in E-cadherin down-regulation and human colorectal cancer epithelial-mesenchymal transition. J Biol Chem 2012;287: 5819-32.
19. Wendt MK, Balanis N, Carlin CR, Schiemann WP. STAT3 and epithelial-mesenchymal transitions in carcinomas. JAKSTAT 2014;3:e28975.
20. Ishii S, Shimizu T. Platelet-activating factor (PAF) receptor and genetically engineered PAF receptor mutant mice. Prog Lipid Res 2000;39:41-82.
21. Yu H, Pardoll D, Jove R. STATs in cancer inflammation and immunity: a leading role for STAT3. Nat Rev Cancer 2009;9:798-809.
22. Sumimoto H, Imabayashi F, Iwata T, Kawakami Y. The BRAF-MAPK signaling pathway is essential for cancer-immune evasion in human melanoma cells. J Exp Med 2006;203:1651-6.
23. Heinrich PC, Behrmann I, Muller-Newen G, Schaper F, Graeve L. Interleukin- 6-type cytokine signalling through the gp130/Jak/STAT pathway. Biochem J 1998;334:297-314.
24. Zhong Z, Wen Z, Darnell JE Jr. Stat3: a STAT family member activated by tyrosine phosphorylation in response to epidermal growth factor and interleukin-6. Science 1994;264:95-8.
25. Denizot Y, Descottes B, Truffinet V, Valleix D, Labrousse F, Mathonnet M. Platelet-activating factor and liver metastasis of colorectal cancer. Int J Cancer 2005;113:503-5.
26. Im SY, Ko HM, Kim JW, Lee HK, Ha TY, Lee HB, et al. Augmentation of tumormetastasis by platelet-activating factor. Cancer Res 1996;56:2662-5.
27. Kang YH, Kim WH, Park MK, Han BH. Antimetastatic and antitumor effects of benzoquinonoid AC7-1 from Ardisia crispa. Int J Cancer 2001; 93:736-40.
28. Xu B, Gao L, Wang L, Tang G, He M, Yu Y, et al. Effects of platelet-activating factor and its differential regulation by androgens and steroid hormones in prostate cancers. Br J Cancer 2013;109:1279-86.
29. Kamran MZ, Patil P, Gude RP. Role of STAT3 in cancer metastasis and translational advances. Biomed Res Int 2013;2013:421821.
30. Masciocchi D, Gelain A, Villa S, Meneghetti F, Barlocco D. Signal transducer and activator of transcription 3 (STAT3): a promising target for anticancer therapy. Future Med Chem 2011;3:567-97.
31. Devarajan E, Huang S. STAT3 as a central regulator of tumor metastases. Curr Mol Med 2009;9:626-33.
32. Al Zaid Siddiquee K, Turkson J. STAT3 as a target for inducing apoptosis in solid and hematological tumors. Cell Res 2008;18:254-67.
33. Chang Q, Daly L, Bromberg J. The IL-6 feed-forward loop: a driver of tumorigenesis. Semin Immunol 2014;26:48-53.
34. Hodge DR, Hurt EM, Farrar WL. The role of IL-6 and STAT3 in inflammation and cancer. Eur J Cancer 2005;41:2502-12.
35. Bayliss TJ, Smith JT, Schuster M, Dragnev KH, Rigas JR. A humanized anti-IL-6 antibody (ALD518) in non-small cell lung cancer. Expert Opin Biol Ther 2011;11:1663-8.
36. Ancrile B, Lim KH, Counter CM. Oncogenic Ras-induced secretion of IL6 is required for tumorigenesis. Genes Dev 2007;21:1714-9.
37. Lacasse C, Turcotte S, Gingras D, Stankova J, Rola-Pleszczynski M. Plateletactivating factor stimulates interleukin-6 production by human endothelial cells and synergizes with tumor necrosis factor for enhanced production of granulocyte-macrophage colony stimulating factor. Inflammation 1997;21:145-58.
38. Sattayaprasert P, Choi HB, Chongthammakun S, McLarnon JG. Plateletactivating factor enhancement of calcium influx and interleukin-6 expression, but not production, in human microglia. J Neuroinflammation 2005;2:11.
39. Ichinowatari G, Yamada M, Yaginuma H, Tsuyuki K, Tanimoto A, Ohuchi K. Participation of prostaglandin E2 and platelet-activating factor in thapsigargin-induced production of interleukin-6. Eur J Pharmacol 2002;434:187-96.
40. Gaumond F, Fortin D, Stankova J, Rola-Pleszczynski M. Differential signaling pathways in platelet-activating factor-induced proliferation and interleukin-6 production by rat vascular smooth muscle cells. J Cardiovasc Pharmacol 1997;30:169-75.
41. Coussens LM, Werb Z. Inflammation and cancer. Nature 2002;420:860-7.
42. Mantovani A, Allavena P, Sica A, Balkwill F. Cancer-related inflammation. Nature 2008;454:436-44.
43. Stafforini DM, McIntyre TM, Zimmerman GA, Prescott SM. Platelet-activating factor, a pleiotrophic mediator of physiological and pathological processes. Crit Rev Clin Lab Sci 2003;40:643-72.
44. Braquet P, Rola-Pleszczynski M. The role of PAF in immunological responses: a review. Prostaglandins 1987;34:143-8.
45. Camussi G, Tetta C, Baglioni C. The role of platelet-activating factor in inflammation. Clin Immunol Immunopathol 1990;57:331-8.
46. Lin WW, Karin M. A cytokine-mediated link between innate immunity, inflammation, and cancer. J Clin Invest 2007;117:1175-83.
47. Fillon S, Soulis K, Rajasekaran S, Benedict-Hamilton H, Radin JN, Orihuela CJ, et al. Platelet-activating factor receptor and innate immunity: uptake of gram-positive bacterial cell wall into host cells and cell-specific pathophysiology. J Immunol 2006;177: 6182-91.
48. Rios FJ, Ferracini M, Pecenin M, Koga MM, Wang Y, Ketelhuth DF, et al. Uptake of oxLDL and IL-10 production by macrophages requires PAFR and CD36 recruitment into the same lipid rafts. PLoS One 2013;8: e76893.
49. Holzel M, Bovier A, Tuting T. Plasticity of tumour and immune cells: a source of heterogeneity and a cause for therapy resistance? Nat Rev Cancer 2013;13:365-76.
50. Balkwill F. Cancer and the chemokine network. Nat Rev Cancer 2004;4:540-50.