Metastatic function of BMP-2 in gastric cancer cells: The role of PI3K/AKT, MAPK, the NF-ΚB pathway, and MMP-9 expression

Experimental Cell Research

Volumn 317, Issue 12, 2011, Pages 1746-1762

  Kang, Myoung Hee ^a   Oh, Sang Cheul ^a   Lee, Hyun Joo ^a   Kang, Han Na ^a   Kim, Jung Lim ^a   Kim, Jun Suk ^a   Yoo, Young A ^a  

^a Korea University College of Medicine   (South Korea)

Author keywords

Bone morphogenetic protein (BMP) 2; Gastric cancer; Invasion; Matrix metalloproteinase (MMP) 9; Metastasis; Migration; Mitogen activated protein kinase (MAPK); Nuclear factor (NF) B; Phosphatidylinositol 3 kinase (PI3K) Akt

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 2 MORPHOLINO 8 PHENYLCHROMONE; BONE MORPHOGENETIC PROTEIN 2; GELATINASE B; I KAPPA B; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B;

ADULT; ARTICLE; CANCER CELL; CELL INVASION; CELL MOTILITY; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; LYMPH NODE METASTASIS; MAJOR CLINICAL STUDY; MALE; METASTASIS; PRIORITY JOURNAL; PROGNOSIS; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; STIMULATION; STOMACH CANCER; TUMOR BIOPSY;

EID: 79958820992     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2011.04.006     Document Type: Article

References (68)

1. Hogan B.L. Bone morphogenetic proteins in development. Curr. Opin. Genet. Dev. 1996, 6:432-438.
2. von Bubnoff A., Cho K.W. Intracellular BMP signaling regulation in vertebrates: pathway or network?. Dev. Biol. 2001, 239:1-14.
3. Balemans W., Van Hul W. Extracellular regulation of BMP signaling in vertebrates: a cocktail of modulators. Dev. Biol. 2002, 250:231-250.
4. Chen D., Zhao M., Mundy G.R. Bone morphogenetic proteins. Growth factors 2004, 22:233-241.
5. Hardwick J.C., Van Den Brink G.R., Bleuming S.A., Ballester I., Van Den Brande J.M., Keller J.J., Offerhaus G.J., Van Deventer S.J., Peppelenbosch M.P. Bone morphogenetic protein 2 is expressed by, and acts upon, mature epithelial cells in the colon. Gastroenterology 2004, 126:111-121.
6. Narita T., Saitoh K., Kameda T., Kuroiwa A., Mizutani M., Koike C., Iba H., Yasugi S. BMPs are necessary for stomach gland formation in the chicken embryo: a study using virally induced BMP-2 and Noggin expression. Development 2000, 127:981-988.
7. Barros R., Pereira B., Duluc I., Azevedo M., Mendes N., Camilo V., Jacobs R.J., Paulo P., Santos-Silva F., van Seuningen I., van den Brink G.R., David L., Freund J.N., Almeida R. Key elements of the BMP/SMAD pathway co-localize with CDX2 in intestinal metaplasia and regulate CDX2 expression in human gastric cell lines. J. Pathol. 2008, 215:411-420.
8. Park Y., Kim J.W., Kim D.S., Kim E.B., Park S.J., Park J.Y., Choi W.S., Song J.G., Seo H.Y., Oh S.C., Kim B.S., Park J.J., Kim Y.H., Kim J.S. The bone morphogenesis protein-2 (BMP-2) is associated with progression to metastatic disease in gastric cancer. Cancer Res. Treat. 2008, 40:127-132.
9. Park Y., Kang M.H., Seo H.Y., Park J.M., Choi C.W., Kim Y.H., Kim I.S., Kim J.S., Oh S.C. Bone morphogenetic protein-2 levels are elevated in the patients with gastric cancer and correlate with disease progression. Med. Oncol. 2010, 27:1192-1199.
10. Kang M.H., Kim J.S., Seo J.E., Oh S.C., Yoo Y.A. BMP2 accelerates the motility and invasiveness of gastric cancer cells via activation of the phosphatidylinositol 3-kinase (PI3K)/Akt pathway. Exp. Cell Res. 2010, 316:24-37.
11. Beck S.E., Carethers J.M. BMP suppresses PTEN expression via RAS/ERK signaling. Cancer Biol. Ther. 2007, 6:1313-1317.
12. Sugimori K., Matsui K., Motomura H., Tokoro T., Wang J., Higa S., Kimura T., Kitajima I. BMP-2 prevents apoptosis of the N1511 chondrocytic cell line through PI3K/Akt-mediated NF-kappaB activation. J. Bone Miner. Metab. 2005, 23:411-419.
13. Graham T.R., Odero-Marah V.A., Chung L.W., Agrawal K.C., Davis R., Abdel-Mageed A.B. PI3K/Akt-dependent transcriptional regulation and activation of BMP-2-Smad signaling by NF-kappaB in metastatic prostate cancer cells. Prostate 2009, 69:168-180.
14. Fong Y.C., Li T.M., Wu C.M., Hsu S.F., Kao S.T., Chen R.J., Lin C.C., Liu S.C., Wu C.L., Tang C.H. BMP-2 increases migration of human chondrosarcoma cells via PI3K/Akt pathway. J. Cell. Physiol. 2008, 217:846-855.
15. Byun D.S., Cho K., Ryu B.K., Lee M.G., Park J.I., Chae K.S., Kim H.J., Chi S.G. Frequent monoallelic deletion of PTEN and its reciprocal association with PIK3CA amplification in gastric carcinoma. Int. J. Cancer 2003, 104:318-327.
16. Oki E., Baba H., Tokunaga E., Nakamura T., Ueda N., Futatsugi M., Mashino K., Yamamoto M., Ikebe M., Kakeji Y., Maehara Y. Akt phosphorylation associates with LOH of PTEN and leads to chemoresistance for gastric cancer. Int. J. Cancer 2005, 117:376-380.
17. Yang X., Fraser M., Moll U.M., Basak A., Tsang B.K. Akt-mediated cisplatin resistance in ovarian cancer: modulation of p53 action on caspase-dependent mitochondrial death pathway. Cancer Res. 2006, 66:3126-3136.
18. Verma A., Atten M.J., Attar B.M., Holian O. Selenomethionine stimulates MAPK (ERK) phosphorylation, protein oxidation, and DNA synthesis in gastric cancer cells. Nutr. Cancer 2004, 49:184-190.
19. Feng W., Brown R.E., Trung C.D., Li W., Wang L., Khoury T., Alrawi S., Yao J., Xia K., Tan D. Morphoproteomic profile of mTOR, Ras/Raf kinase/ERK, and NF-kappaB pathways in human gastric adenocarcinoma. Ann. Clin. Lab. Sci. 2008, 38:195-209.
20. Lee B.L., Lee H.S., Jung J., Cho S.J., Chung H.Y., Kim W.H., Jin Y.W., Kim C.S., Nam S.Y. Nuclear factor-kappaB activation correlates with better prognosis and Akt activation in human gastric cancer. Clin. Cancer Res. 2005, 11:2518-2525.
21. Karin M., Greten F.R. NF-kappaB: linking inflammation and immunity to cancer development and progression. Nat. Rev. 2005, 5:749-759.
22. Oya M., Takayanagi A., Horiguchi A., Mizuno R., Ohtsubo M., Marumo K., Shimizu N., Murai M. Increased nuclear factor-kappa B activation is related to the tumor development of renal cell carcinoma. Carcinogenesis 2003, 24:377-384.
23. Nair A., Venkatraman M., Maliekal T.T., Nair B., Karunagaran D. NF-kappaB is constitutively activated in high-grade squamous intraepithelial lesions and squamous cell carcinomas of the human uterine cervix. Oncogene 2003, 22:50-58.
24. Abdel-Latif M.M., O'Riordan J., Windle H.J., Carton E., Ravi N., Kelleher D., Reynolds J.V. NF-kappaB activation in esophageal adenocarcinoma: relationship to Barrett's metaplasia, survival, and response to neoadjuvant chemoradiotherapy. Ann. Surg. 2004, 239:491-500.
25. Katiyar S.K., Meeran S.M. Obesity increases the risk of UV radiation-induced oxidative stress and activation of MAPK and NF-kappaB signaling. Free Radic. Biol. Med. 2007, 42:299-310.
26. Levy Y., Ronen D., Bershadsky A.D., Zick Y. Sustained induction of ERK, protein kinase B, and p70 S6 kinase regulates cell spreading and formation of F-actin microspikes upon ligation of integrins by galectin-8, a mammalian lectin. J. Biol. Chem. 2003, 278:14533-14542.
27. Deryugina E.I., Quigley J.P. Matrix metalloproteinases and tumor metastasis. Cancer Metastasis Rev. 2006, 25:9-34.
28. St-Pierre Y., Van Themsche C., Esteve P.O. Emerging features in the regulation of MMP-9 gene expression for the development of novel molecular targets and therapeutic strategies. Curr. Drug Targets 2003, 2:206-215.
29. Van den Steen P.E., Dubois B., Nelissen I., Rudd P.M., Dwek R.A., Opdenakker G. Biochemistry and molecular biology of gelatinase B or matrix metalloproteinase-9 (MMP-9). Crit. Rev. Biochem. Mol. Biol. 2002, 37:375-536.
30. Egeblad M., Werb Z. New functions for the matrix metalloproteinases in cancer progression. Nat. Rev. Cancer 2002, 2:161-174.
31. Suzuki A., Lu J., Kusakai G., Kishimoto A., Ogura T., Esumi H. ARK5 is a tumor invasion-associated factor downstream of Akt signaling. Mol. Cell. Biol. 2004, 24:3526-3535.
32. Zi X., Guo Y., Simoneau A.R., Hope C., Xie J., Holcombe R.F., Hoang B.H. Expression of Frzb/secreted Frizzled-related protein 3, a secreted Wnt antagonist, in human androgen-independent prostate cancer PC-3 cells suppresses tumor growth and cellular invasiveness. Cancer Res. 2005, 65:9762-9770.
33. Yoo H.G., Shin B.A., Park J.S., Lee K.H., Chay K.O., Yang S.Y., Ahn B.W., Jung Y.D. IL-1beta induces MMP-9 via reactive oxygen species and NF-kappaB in murine macrophage RAW 264.7 cells. Biochem. Biophys. Res. Commun. 2002, 298:251-256.
34. Coussens L.M., Werb Z. Inflammation and cancer. Nature 2002, 420:860-867.
35. Ghosh S., May M.J., Kopp E.B. NF-kappa B and Rel proteins: evolutionarily conserved mediators of immune responses. Annu. Rev. Immunol. 1998, 16:225-260.
36. Wang C.Y., Mayo M.W., Korneluk R.G., Goeddel D.V., Baldwin A.S. NF-kappaB antiapoptosis: induction of TRAF1 and TRAF2 and c-IAP1 and c-IAP2 to suppress caspase-8 activation. Science (New York, N.Y.) 1998, 281:1680-1683.
37. Darnay B.G., Aggarwal B.B. Signal transduction by tumour necrosis factor and tumour necrosis factor related ligands and their receptors. Ann. Rheum. Dis. 1999, 58(Suppl. 1):I2-I13.
38. Wang C.Y., Cusack J.C., Liu R., Baldwin A.S. Control of inducible chemoresistance: enhanced anti-tumor therapy through increased apoptosis by inhibition of NF-kappaB. Nat. Med. 1999, 5:412-417.
39. Guttridge D.C., Mayo M.W., Madrid L.V., Wang C.Y., Baldwin A.S. NF-kappaB-induced loss of MyoD messenger RNA: possible role in muscle decay and cachexia. Science (New York, N.Y.) 2000, 289:2363-2366.
40. Ozes O.N., Mayo L.D., Gustin J.A., Pfeffer S.R., Pfeffer L.M., Donner D.B. NF-kappaB activation by tumour necrosis factor requires the Akt serine-threonine kinase. Nature 1999, 401:82-85.
41. Madrid L.V., Wang C.Y., Guttridge D.C., Schottelius A.J., Baldwin A.S., Mayo M.W. Akt suppresses apoptosis by stimulating the transactivation potential of the RelA/p65 subunit of NF-kappaB. Mol. Cell. Biol. 2000, 20:1626-1638.
42. Mansell A., Khelef N., Cossart P., O'Neill L.A. Internalin B activates nuclear factor-kappa B via Ras, phosphoinositide 3-kinase, and Akt. J. Biol. Chem. 2001, 276:43597-43603.
43. Yang C.H., Murti A., Pfeffer S.R., Kim J.G., Donner D.B., Pfeffer L.M. Interferon alpha/beta promotes cell survival by activating nuclear factor kappa B through phosphatidylinositol 3-kinase and Akt. J. Biol. Chem. 2001, 276:13756-13761.
44. Birkenkamp K.U., Geugien M., Schepers H., Westra J., Lemmink H.H., Vellenga E. Constitutive NF-kappaB DNA-binding activity in AML is frequently mediated by a Ras/PI3-K/PKB-dependent pathway. Leukemia 2004, 18:103-112.
45. Park Y., Kang M.H., Seo H.Y., Park J.M., Choi C.W., Kim Y.H., Kim I.S., Kim J.S., Oh S.C. Bone morphogenetic protein-2 levels are elevated in the patients with gastric cancer and correlate with disease progression. Med. Oncol. 2010, 27:1192-1199.
46. Deng H., Makizumi R., Ravikumar T.S., Dong H., Yang W., Yang W.L. Bone morphogenetic protein-4 is overexpressed in colonic adenocarcinomas and promotes migration and invasion of HCT116 cells. Exp. Cell Res. 2007, 313:1033-1044.
47. Gordon K.J., Kirkbride K.C., How T., Blobe G.C. Bone morphogenetic proteins induce pancreatic cancer cell invasiveness through a Smad1-dependent mechanism that involves matrix metalloproteinase-2. Carcinogenesis 2009, 30:238-248.
48. Rothhammer T., Poser I., Soncin F., Bataille F., Moser M., Bosserhoff A.K. Bone morphogenic proteins are overexpressed in malignant melanoma and promote cell invasion and migration. Cancer Res. 2005, 65:448-456.
49. Clement J.H., Raida M., Sanger J., Bicknell R., Liu J., Naumann A., Geyer A., Waldau A., Hortschansky P., Schmidt A., Hoffken K., Wolft S., Harris A.L. Bone morphogenetic protein 2 (BMP-2) induces in vitro invasion and in vivo hormone independent growth of breast carcinoma cells. Int. J. Oncol. 2005, 27:401-407.
50. Langenfeld E.M., Calvano S.E., Abou-Nukta F., Lowry S.F., Amenta P., Langenfeld J. The mature bone morphogenetic protein-2 is aberrantly expressed in non-small cell lung carcinomas and stimulates tumor growth of A549 cells. Carcinogenesis 2003, 24:1445-1454.
51. Hsu M.Y., Rovinsky S., Penmatcha S., Herlyn M., Muirhead D. Bone morphogenetic proteins in melanoma: angel or devil?. Cancer Metastasis Rev. 2005, 24:251-263.
52. Theriault B.L., Shepherd T.G., Mujoomdar M.L., Nachtigal M.W. BMP4 induces EMT and Rho GTPase activation in human ovarian cancer cells. Carcinogenesis 2007, 28:1153-1162.
53. Chin Y.R., Toker A. Function of Akt/PKB signaling to cell motility, invasion and the tumor stroma in cancer. Cell. Signal. 2009, 21:470-476.
54. Meng Q., Xia C., Fang J., Rojanasakul Y., Jiang B.H. Role of PI3K and AKT specific isoforms in ovarian cancer cell migration, invasion and proliferation through the p70S6K1 pathway. Cell. Signal. 2006, 18:2262-2271.
55. Amiri A., Noei F., Jeganathan S., Kulkarni G., Pinke D.E., Lee J.M. eEF1A2 activates Akt and stimulates Akt-dependent actin remodeling, invasion and migration. Oncogene 2007, 26:3027-3040.
56. Sivaraman V.S., Wang H., Nuovo G.J., Malbon C.C. Hyperexpression of mitogen-activated protein kinase in human breast cancer. J. Clin. Invest. 1997, 99:1478-1483.
57. Grotegut S., von Schweinitz D., Christofori G., Lehembre F. Hepatocyte growth factor induces cell scattering through MAPK/Egr-1-mediated upregulation of Snail. EMBO J. 2006, 25:3534-3545.
58. Janda E., Lehmann K., Killisch I., Jechlinger M., Herzig M., Downward J., Beug H., Grunert S. Ras and TGF[beta] cooperatively regulate epithelial cell plasticity and metastasis: dissection of Ras signaling pathways. J. Cell Biol. 2002, 156:299-313.
59. Lai T.H., Fong Y.C., Fu W.M., Yang R.S., Tang C.H. Osteoblasts-derived BMP-2 enhances the motility of prostate cancer cells via activation of integrins. Prostate 2008, 68:1341-1353.
60. Attisano L., Wrana J.L. Signal transduction by the TGF-beta superfamily. Science (New York, N.Y.) 2002, 296:1646-1647.
61. Ghosh-Choudhury N., Abboud S.L., Nishimura R., Celeste A., Mahimainathan L., Choudhury G.G. Requirement of BMP-2-induced phosphatidylinositol 3-kinase and Akt serine/threonine kinase in osteoblast differentiation and Smad-dependent BMP-2 gene transcription. J. Biol. Chem. 2002, 277:33361-33368.
62. Ghosh-Choudhury N., Mandal C.C., Choudhury G.G. Statin-induced Ras activation integrates the phosphatidylinositol 3-kinase signal to Akt and MAPK for bone morphogenetic protein-2 expression in osteoblast differentiation. J. Biol. Chem. 2007, 282:4983-4993.
63. Friess H., Guo X.Z., Nan B.C., Kleeff J., Buchler M.W. Growth factors and cytokines in pancreatic carcinogenesis. Ann. N. Y. Acad. Sci. 1999, 880:110-121.
64. Yeh Y.Y., Chiao C.C., Kuo W.Y., Hsiao Y.C., Chen Y.J., Wei Y.Y., Lai T.H., Fong Y.C., Tang C.H. TGF-beta1 increases motility and alphavbeta3 integrin up-regulation via PI3K, Akt and NF-kappaB-dependent pathway in human chondrosarcoma cells. Biochem. Pharmacol. 2008, 75:1292-1301.
65. Huang Y.C., Hsiao Y.C., Chen Y.J., Wei Y.Y., Lai T.H., Tang C.H. Stromal cell-derived factor-1 enhances motility and integrin up-regulation through CXCR4, ERK and NF-kappaB-dependent pathway in human lung cancer cells. Biochem. Pharmacol. 2007, 74:1702-1712.
66. Zhong H., SuYang H., Erdjument-Bromage H., Tempst P., Ghosh S. The transcriptional activity of NF-kappaB is regulated by the IkappaB-associated PKAc subunit through a cyclic AMP-independent mechanism. Cell 1997, 89:413-424.
67. Vermeulen L., De Wilde G., Van Damme P., Vanden Berghe W., Haegeman G. Transcriptional activation of the NF-kappaB p65 subunit by mitogen- and stress-activated protein kinase-1 (MSK1). EMBO J. 2003, 22:1313-1324.
68. Haque M., Francis J., Sehgal I. Aryl hydrocarbon exposure induces expression of MMP-9 in human prostate cancer cell lines. Cancer Lett. 2005, 225:159-166.