NNK promotes migration and invasion of lung cancer cells through activation of c-Src/PKCι/FAK loop

Cancer Letters

Volumn 318, Issue 1, 2012, Pages 106-113

  Shen, Jie ^a,c   Xu, Lijun ^b   Owonikoko, Taofeek K ^a   Sun, Shi Yong ^a   Khuri, Fadlo R ^a   Curran, Walter J ^a   Deng, Xingming ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

^c SHANGHAI JIAO TONG UNIVERSITY   (China)

Author keywords

C Src; FAK; Invasion; Lung cancer; Migration; PKC iota

Indexed keywords

BUNGAROTOXIN RECEPTOR; CARCINOGEN; FOCAL ADHESION KINASE; NITROSAMINE 4 (METHYLNITROSAMINO) 1 (3 PYRIDYL) 1 BUTANONE; PROTEIN KINASE C IOTA; PROTEIN TYROSINE KINASE; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; CANCER CELL; CELL INVASION; CELL MIGRATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME BINDING; ENZYME LOCALIZATION; HUMAN; HUMAN CELL; LUNG CANCER; PRIORITY JOURNAL; PROTEIN FUNCTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION;

BLOTTING, WESTERN; BUNGAROTOXINS; CARCINOGENS; CELL ADHESION; CELL MOVEMENT; FLUORESCENT ANTIBODY TECHNIQUE; FOCAL ADHESION KINASE 1; HUMANS; ISOENZYMES; LUNG NEOPLASMS; NEOPLASM INVASIVENESS; NITROSAMINES; PROTEIN KINASE C; PROTO-ONCOGENE PROTEINS PP60(C-SRC); RECEPTORS, NICOTINIC; RNA, SMALL INTERFERING; TUMOR CELLS, CULTURED; WOUND HEALING;

EID: 84857138655     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2011.12.008     Document Type: Article

References (48)

1. Fidler I.J. Cancer metastasis. Br. Med. Bull. 1991, 47:157-177.
2. Gomez D.E., Skilton G., Alonso D.F., Kazanietz M.G. The role of protein kinase C and novel phorbol ester receptors in tumor cell invasion and metastasis (Review). Oncol. Rep. 1999, 6:1363-1370.
3. Liotta L.A. Tumor invasion and metastases-role of the extracellular matrix: Rhoads Memorial Award lecture. Cancer Res. 1986, 46:1-7.
4. Lauffenburger D.A., Horwitz A.F. Cell migration: a physically integrated molecular process. Cell 1996, 84:359-369.
5. Bredin C.G., Liu Z., Hauzenberger D., Klominek J. Growth-factor-dependent migration of human lung-cancer cells. Int. J. Cancer 1999, 82:338-345.
6. Gopalakrishna R., Chen Z.H., Gundimeda U. Tobacco smoke tumor promoters Catechol and hydroquinone, induce oxidative regulation of protein kinase C and influence invasion and metastasis of lung carcinoma cells. Proc. Natl. Acad. Sci. USA 1994, 91:12233-12237.
7. Murin S., Inciardi J. Cigarette smoking and the risk of pulmonary metastasis from breast cancer. Chest 2001, 119:1635-1640.
8. Schuller H.M., Plummer H.K., Jull B.A. Receptor-mediated effects of nicotine and its nitrosated derivative NNK on pulmonary neuroendocrine cells. Anat. Rec. A Discov. Mol. Cell Evol. Biol. 2003, 270:51-58.
9. Dumont J.A., Bitonti A.J. Modulation of human melanoma cell metastasis and adhesion may involve integrin phosphorylation mediated through protein kinase C. Biochem. Biophys. Res. Commun. 1994, 204:264-272.
10. Herbert J.M., Maffrand J.P. Tumor cell adherence to cultured capillary endothelial cells is promoted by activators of protein kinase C. Biochem. Pharmacol. 1991, 42:163-170.
11. Quigley R.L., Shafer S.H., Williams C.L. Regulation of integrin-mediated adhesion by muscarinic acetylcholine receptors and protein kinase C in small cell lung carcinoma. Chest 1998, 114:839-846.
12. Lewis J.M., Cheresh D.A., Schwartz M.A. Protein kinase C regulates alpha v beta 5-dependent cytoskeletal associations and focal adhesion kinase phosphorylation. J. Cell. Biol. 1996, 134:1323-1332.
13. Newton A.C. Protein kinase C: structure function, and regulation. J. Biol. Chem. 1995, 270:28495-28498.
14. Mellor H., Parker P.J. The extended protein kinase C superfamily. Biochem. J. 1998, 332:281-292.
15. Spitaler M., Villunger A., Grunicke H., Uberall F. Unique structural and functional properties of the ATP-binding domain of atypical protein kinase C-iota. J. Biol. Chem. 2000, 275:33289-33296.
16. Selbie L.A., Schmitz-Peiffer C., Sheng Y., Biden T.J. Molecular cloning and characterization of PKC iota, an atypical isoform of protein kinase C derived from insulin-secreting cells. J. Biol. Chem. 1993, 268:24296-24302.
17. Murray N.R., Fields A.P. Atypical protein kinase C iota protects human leukemia cells against drug-induced apoptosis. J. Biol. Chem. 1997, 272:27521-27524.
18. Wooten M.W., Vandenplas M.L., Seibenhener M.L., Geetha T., Diaz-Meco M.T. Nerve growth factor stimulates multisite tyrosine phosphorylation and activation of the atypical protein kinase C's via a src kinase pathway. Mol. Cell. Biol. 2001, 21:8414-8427.
19. Lallena M.J., Diaz-Meco M.T., Bren G., Paya C.V., Moscat J. Activation of IkappaB kinase beta by protein kinase C isoforms. Mol. Cell. Biol. 1999, 19:2180-2188.
20. Murray N.R., Jamieson L., Yu W., Zhang J., Gokmen-Polar Y., Sier D., Anastasiadis P., Gatalica Z., Thompson E.A., Fields A.P. Protein kinase Ciota is required for Ras transformation and colon carcinogenesis in vivo. J. Cell. Biol. 2004, 164:797-802.
21. Selzer E., Okamoto I., Lucas T., Kodym R., Pehamberger H., Jansen B. Protein kinase C isoforms in normal and transformed cells of the melanocytic lineage. Melanoma. Res. 2002, 12:201-209.
22. Hanks S.K., Ryzhova L., Shin N.Y., Brabek J. Focal adhesion kinase signaling activities and their implications in the control of cell survival and motility. Front Biosci. 2003, 8:d982-996.
23. Gabarra-Niecko V., Schaller M.D., Dunty J.M. FAK regulates biological processes important for the pathogenesis of cancer. Cancer Metastasis. Rev. 2003, 22:359-374.
24. Thomas S.M., Brugge J.S. Cellular functions regulated by Src family kinases. Annu. Rev. Cell. Dev. Biol. 1997, 13:513-609.
25. Nakamoto T., Sakai R., Ozawa K., Yazaki Y., Hirai H. Direct binding of C-terminal region of p130Cas to SH2 and SH3 domains of Src kinase. J. Biol. Chem. 1996, 271:8959-8965.
26. Turner C.E. Paxillin and focal adhesion signalling. Nat. Cell. Biol. 2000, 2:E231-236.
27. Lin E.H., Hui A.Y., Meens J.A., Tremblay E.A., Schaefer E., Elliott B.E. Disruption of Ca2+-dependent cell-matrix adhesion enhances c-Src kinase activity, but causes dissociation of the c-Src/FAK complex and dephosphorylation of tyrosine-577 of FAK in carcinoma cells. Exp. Cell. Res. 2004, 293:1-13.
28. Jones R.J., Brunton V.G., Frame M.C. Adhesion-linked kinases in cancer; emphasis on src, focal adhesion kinase and PI 3-kinase. Eur. J. Cancer 2000, 36:1595-1606.
29. Calalb M.B., Polte T.R., Hanks S.K. Tyrosine phosphorylation of focal adhesion kinase at sites in the catalytic domain regulates kinase activity: a role for Src family kinases. Mol. Cell. Biol. 1995, 15:954-963.
30. Calalb M.B., Zhang X., Polte T.R., Hanks S.K. Focal adhesion kinase tyrosine-861 is a major site of phosphorylation by Src. Biochem. Biophys. Res. Commun. 1996, 228:662-668.
31. Verbeek B.S., Vroom T.M., Rijksen G. Overexpression of c-Src enhances cell-matrix adhesion and cell migration in PDGF-stimulated NIH3T3 fibroblasts. Exp. Cell. Res. 1999, 248:531-537.
32. Kaplan K.B., Swedlow J.R., Morgan D.O., Varmus H.E. C-Src enhances the spreading of src-/- fibroblasts on fibronectin by a kinase-independent mechanism. Genes Dev. 1995, 9:1505-1517.
33. Jamieson L., Carpenter L., Biden T.J., Fields A.P. Protein kinase Ciota activity is necessary for Bcr-Abl-mediated resistance to drug-induced apoptosis. J. Biol. Chem. 1999, 274:3927-3930.
34. Xu L., Deng X. Suppression of cancer cell migration and invasion by protein phosphatase 2A through dephosphorylation of mu- and m-calpains. J. Biol. Chem. 2006, 281:35567-35575.
35. Seibenhener M.L., Roehm J., White W.O., Neidigh K.B., Vandenplas M.L., Wooten M.W. Identification of Src as a novel atypical protein kinase C-interacting protein. Mol. Cell. Biol. Res. Commun. 1999, 2:28-31.
36. Hanke J.H., Gardner J.P., Dow R.L., Changelian P.S., Brissette W.H., Weringer E.J., Pollok B.A., Connelly P.A. Discovery of a novel potent, and Src family-selective tyrosine kinase inhibitor. Study of Lck- and FynT-dependent T cell activation. J. Biol. Chem. 1996, 271:695-701.
37. Jull B.A., Plummer H.K., Schuller H.M. Nicotinic receptor-mediated activation by the tobacco-specific nitrosamine NNK of a Raf-1/MAP kinase pathway Resulting in phosphorylation of c-myc in human small cell lung carcinoma cells and pulmonary neuroendocrine cells. J. Cancer Res. Clin. Oncol. 2001, 127:707-717.
38. Jin Z., Gao F., Flagg T., Deng X. Tobacco-specific nitrosamine 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone promotes functional cooperation of Bcl2 and c-Myc through phosphorylation in regulating cell survival and proliferation. J. Biol. Chem. 2004, 279:40209-40219.
39. Semizarov D., Frost L., Sarthy A., Kroeger P., Halbert D.N., Fesik S.W. Specificity of short interfering RNA determined through gene expression signatures. Proc. Natl. Acad. Sci. USA 2003, 100:6347-6352.
40. Maser E., Stinner B., Atalla A. Carbonyl reduction of 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone (NNK) by cytosolic enzymes in human liver and lung. Cancer Lett. 2000, 148:135-144.
41. Schuller H.M. Mechanisms of smoking-related lung and pancreatic adenocarcinoma development. Nat. Rev. Cancer 2002, 2:455-463.
42. Brunnemann K.D., Mitacek E.J., Liu Y., Limsila T., Suttajit M. Assessment of major carcinogenic tobacco-specific N-nitrosamines in Thai cigarettes. Cancer Detect. Prev. 1996, 20:114-121.
43. Maser E., Friebertshauser J., Volker B. Purification, characterization and NNK carbonyl reductase activities of 11beta-hydroxysteroid dehydrogenase type 1 from human liver: enzyme cooperativity and significance in the detoxification of a tobacco-derived carcinogen. Chem. Biol. Interact. 2003, 143-144:435-448.
44. Hauck C.R., Hsia D.A., Schlaepfer D.D. The focal adhesion kinase-a regulator of cell migration and invasion. IUBMB Life 2002, 53:115-119.
45. Jin Z., Xin M., Deng X. Survival function of protein kinase C{iota} as a novel nitrosamine 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone-activated bad kinase. J. Biol. Chem. 2005, 280:16045-16052.
46. Lopez M.G., Montiel C., Herrero C.J., Garcia-Palomero E., Mayorgas I., Hernandez-Guijo J.M., Villarroya M., Olivares R., Gandia L., McIntosh J.M., Olivera B.M., Garcia A.G. Unmasking the functions of the chromaffin cell alpha7 nicotinic receptor by using short pulses of acetylcholine and selective blockers. Proc. Natl. Acad. Sci. USA 1998, 95:14184-14189.
47. Salvaterra P.M., Mahler H.R. Nicotinic acetylcholine receptor from rat brain Solubilization, partial purification, and characterization. J. Biol. Chem. 1976, 251:6327-6334.
48. Hung Y.H., Hung W.C. 4-(Methylnitrosamino)-1-(3-pyridyl)-1-butanone (NNK) enhances invasiveness of lung cancer cells by up-regulating contactin-1 via the alpha7 nicotinic acetylcholine receptor/ERK signaling pathway. Chem. Biol. Interact. 2009, 179:154-159.