Maternal embryonic leucine zipper kinase enhances gastric cancer progression via the FAK/Paxillin pathway

Molecular Cancer

Volumn 13, Issue 1, 2014, Pages

  Du, Tao ^a   Qu, Ying ^a   Li, Jianfang ^a   Li, Hao ^a   Su, Liping ^a   Zhou, Quan ^a   Yan, Min ^a   Li, Chen ^a   Zhu, Zhenggang ^a   Liu, Bingya ^a  

^a SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

FAK; Gastric cancer; MELK; Paxillin; Tumor invasion; Tumor migration

Indexed keywords

ACTIN; CHOLECYSTOKININ OCTAPEPTIDE; FLUOROURACIL; FOCAL ADHESION KINASE; GASTRIN; KI 67 ANTIGEN; MATERNAL EMBRYONIC LEUCINE ZIPPER KINASE; MESSENGER RNA; PAXILLIN; PROTEIN KINASE; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; FOCAL ADHESION KINASE 1; MELK PROTEIN, MOUSE; PROTEIN SERINE THREONINE KINASE; PTK2 PROTEIN, MOUSE; PXN PROTEIN, MOUSE; SMALL INTERFERING RNA;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CANCER CELL LINE; CANCER GROWTH; CARCINOGENICITY; CELL ACTIVITY; CELL GROWTH; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; CELL STRUCTURE; CLINICAL ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; FILTERS AND MEMBRANES; FLOW CYTOMETRY; G1 PHASE CELL CYCLE CHECKPOINT; G2 PHASE CELL CYCLE CHECKPOINT; HUMAN; IMMUNOFLUORESCENCE TEST; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; LYMPH NODE METASTASIS; M PHASE CELL CYCLE CHECKPOINT; MALE; MOLECULAR MECHANICS; MOUSE; NONHUMAN; PERITONEUM METASTASIS; POLYMERASE CHAIN REACTION; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; QUANTITATIVE STUDY; S PHASE CELL CYCLE CHECKPOINT; SIGNAL TRANSDUCTION; STOMACH CANCER; STRESS FIBER; TUMOR ENGRAFTMENT; WESTERN BLOTTING; ACTIN FILAMENT; AGED; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL CYCLE; CELL SURVIVAL; DRUG EFFECTS; DRUG SCREENING; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MIDDLE AGED; NUDE MOUSE; PATHOLOGY; PHOSPHORYLATION; STOMACH NEOPLASMS; TUMOR CELL LINE; TUMOR INVASION;

ACTIN CYTOSKELETON; AGED; ANIMALS; ANTINEOPLASTIC AGENTS; CELL CYCLE; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; FEMALE; FLUOROURACIL; FOCAL ADHESION KINASE 1; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MALE; MICE; MICE, NUDE; MIDDLE AGED; NEOPLASM INVASIVENESS; PAXILLIN; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; STOMACH NEOPLASMS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84900019839     PISSN: None     EISSN: 14764598     Source Type: Journal    
DOI: 10.1186/1476-4598-13-100     Document Type: Article

References (46)

1. Moore MA, Manan AA, Chow KY, Cornain SF, Devi CR, Triningsih FX, Laudico A, Mapua CA, Mirasol-Lumague MR, Noorwati S, Nyunt K, Othman NH, Shah SA, Sinuraya ES, Yip CH, Sobue T. Cancer epidemiology and control in peninsular and island South-East Asia - past, present and future. Asian Pac J Cancer Prev 2010, 11(Suppl 2):81-98.
2. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin 2011, 61:69-90. 10.3322/caac.20107, 21296855.
3. Kato M, Asaka M. Recent development of gastric cancer prevention. Jpn J Clin Oncol 2012, 42:987-994. 10.1093/jjco/hys151, 23018579.
4. Kanat O, O'Neil BH. Metastatic gastric cancer treatment: a little slow but worthy progress. Med Oncol 2013, 30:464.
5. Steeg PS. Tumor metastasis: mechanistic insights and clinical challenges. Nat Med 2006, 12:895-904. 10.1038/nm1469, 16892035.
6. Felding-Habermann B. Integrin adhesion receptors in tumor metastasis. Clin Exp Metastasis 2003, 20:203-213. 10.1023/A:1022983000355, 12741679.
7. Heyer BS, Warsowe J, Solter D, Knowles BB, Ackerman SL. New member of the Snf1/AMPK kinase family, Melk, is expressed in the mouse egg and preimplantation embryo. Mol Reprod Dev 1997, 47:148-156. 10.1002/(SICI)1098-2795(199706)47:2<148::AID-MRD4>3.0.CO;2-M, 9136115.
8. Davezac N, Baldin V, Blot J, Ducommun B, Tassan JP. Human pEg3 kinase associates with and phosphorylates CDC25B phosphatase: a potential role for pEg3 in cell cycle regulation. Oncogene 2002, 21:7630-7641. 10.1038/sj.onc.1205870, 12400006.
9. Blot J, Chartrain I, Roghi C, Philippe M, Tassan JP. Cell cycle regulation of pEg3, a new Xenopus protein kinase of the KIN1/PAR-1/MARK family. Dev Biol 2002, 241:327-338. 10.1006/dbio.2001.0525, 11784115.
10. Nagase T, Seki N, Ishikawa K, Tanaka A, Nomura N. Prediction of the coding sequences of unidentified human genes. V. The coding sequences of 40 new genes (KIAA0161-KIAA0200) deduced by analysis of cDNA clones from human cell line KG-1. DNA Res 1996, 3:17-24. 10.1093/dnares/3.1.17, 8724849.
11. Nakano I, Paucar AA, Bajpai R, Dougherty JD, Zewail A, Kelly TK, Kim KJ, Ou J, Groszer M, Imura T, Freije WA, Nelson SF, Sofroniew MV, Wu H, Liu X, Terskikh AV, Geschwind DH, Kornblum HI. Maternal embryonic leucine zipper kinase (MELK) regulates multipotent neural progenitor proliferation. J Cell Biol 2005, 170:413-427. 10.1083/jcb.200412115, 2171475, 16061694.
12. Badouel C, Chartrain I, Blot J, Tassan JP. Maternal embryonic leucine zipper kinase is stabilized in mitosis by phosphorylation and is partially degraded upon mitotic exit. Exp Cell Res 2010, 316:2166-2173. 10.1016/j.yexcr.2010.04.019, 20420823.
13. Vulsteke V, Beullens M, Boudrez A, Keppens S, Van Eynde A, Rider MH, Stalmans W, Bollen M. Inhibition of spliceosome assembly by the cell cycle-regulated protein kinase MELK and involvement of splicing factor NIPP1. J Biol Chem 2004, 279:8642-8647. 10.1074/jbc.M311466200, 14699119.
14. Beullens M, Vancauwenbergh S, Morrice N, Derua R, Ceulemans H, Waelkens E, Bollen M. Substrate specificity and activity regulation of protein kinase MELK. J Biol Chem 2005, 280:40003-40011. 10.1074/jbc.M507274200, 16216881.
15. Kig C, Beullens M, Beke L, Van Eynde A, Linders JT, Brehmer D, Bollen M. Maternal embryonic leucine zipper kinase (MELK) reduces replication stress in glioblastoma cells. J Biol Chem 2013, 288:24200-24212. 10.1074/jbc.M113.471433, 23836907.
16. Seong HA, Gil M, Kim KT, Kim SJ, Ha H. Phosphorylation of a novel zinc-finger-like protein, ZPR9, by murine protein serine/threonine kinase 38 (MPK38). Biochem J 2002, 361:597-604. 10.1042/0264-6021:3610597, 1222342, 11802789.
17. Kuner R, Falth M, Pressinotti NC, Brase JC, Puig SB, Metzger J, Gade S, Schafer G, Bartsch G, Steiner E, Klocker H, Sultmann H. The maternal embryonic leucine zipper kinase (MELK) is upregulated in high-grade prostate cancer. J Mol Med (Berl) 2013, 91:237-248. 10.1007/s00109-012-0949-1, 22945237.
18. Lin ML, Park JH, Nishidate T, Nakamura Y, Katagiri T. Involvement of maternal embryonic leucine zipper kinase (MELK) in mammary carcinogenesis through interaction with Bcl-G, a pro-apoptotic member of the Bcl-2 family. Breast Cancer Res 2007, 9:R17. 10.1186/bcr1650, 1851384, 17280616.
19. Marie SK, Okamoto OK, Uno M, Hasegawa AP, Oba-Shinjo SM, Cohen T, Camargo AA, Kosoy A, Carlotti CG, Toledo S, Moreira-Filho CA, Zago MA, Simpson AJ, Caballero OL. Maternal embryonic leucine zipper kinase transcript abundance correlates with malignancy grade in human astrocytomas. Int J Cancer 2008, 122:807-815. 10.1002/ijc.23189, 17960622.
20. Nakano I, Masterman-Smith M, Saigusa K, Paucar AA, Horvath S, Shoemaker L, Watanabe M, Negro A, Bajpai R, Howes A, Lelievre V, Waschek JA, Lazareff JA, Freije WA, Liau LM, Gilbertson RJ, Cloughesy TF, Geschwind DH, Nelson SF, Mischel PS, Terskikh AV, Kornblum HI. Maternal embryonic leucine zipper kinase is a key regulator of the proliferation of malignant brain tumors, including brain tumor stem cells. J Neurosci Res 2008, 86:48-60. 10.1002/jnr.21471, 17722061.
21. Pickard MR, Green AR, Ellis IO, Caldas C, Hedge VL, Mourtada-Maarabouni M, Williams GT. Dysregulated expression of Fau and MELK is associated with poor prognosis in breast cancer. Breast Cancer Res 2009, 11:R60. 10.1186/bcr2350, 2750122, 19671159.
22. Yoshimoto K, Ma X, Guan Y, Mizoguchi M, Nakamizo A, Amano T, Hata N, Kuga D, Sasaki T. Expression of stem cell marker and receptor kinase genes in glioblastoma tissue quantified by real-time RT-PCR. Brain Tumor Pathol 2011, 28:291-296. 10.1007/s10014-011-0046-0, 3196642, 21691733.
23. Hebbard LW, Maurer J, Miller A, Lesperance J, Hassell J, Oshima RG, Terskikh AV. Maternal embryonic leucine zipper kinase is upregulated and required in mammary tumor-initiating cells in vivo. Cancer Res 2010, 70:8863-8873. 10.1158/0008-5472.CAN-10-1295, 3990264, 20861186.
24. Gray D, Jubb AM, Hogue D, Dowd P, Kljavin N, Yi S, Bai W, Frantz G, Zhang Z, Koeppen H, de Sauvage FJ, Davis DP. Maternal embryonic leucine zipper kinase/murine protein serine-threonine kinase 38 is a promising therapeutic target for multiple cancers. Cancer Res 2005, 65:9751-9761. 10.1158/0008-5472.CAN-04-4531, 16266996.
25. Chung S, Nakamura Y. MELK inhibitor, novel molecular targeted therapeutics for human cancer stem cells. Cell Cycle 2013, 12:1655-1656. 10.4161/cc.24988, 23673321.
26. Nakano I, Joshi K, Visnyei K, Hu B, Watanabe M, Lam D, Wexler E, Saigusa K, Nakamura Y, Laks DR, Mischel PS, Viapiano M, Kornblum HI. Siomycin A targets brain tumor stem cells partially through a MELK-mediated pathway. Neuro Oncol 2011, 13:622-634. 10.1093/neuonc/nor023, 3107094, 21558073.
27. Choi S, Ku JL. Resistance of colorectal cancer cells to radiation and 5-FU is associated with MELK expression. Biochem Biophys Res Commun 2011, 412:207-213. 10.1016/j.bbrc.2011.07.060, 21806965.
28. Deakin NO, Turner CE. Paxillin comes of age. J Cell Sci 2008, 121:2435-2444. 10.1242/jcs.018044, 2522309, 18650496.
29. Lietha D, Cai X, Ceccarelli DF, Li Y, Schaller MD, Eck MJ. Structural basis for the autoinhibition of focal adhesion kinase. Cell 2007, 129:1177-1187. 10.1016/j.cell.2007.05.041, 2077847, 17574028.
30. Mitra SK, Schlaepfer DD. Integrin-regulated FAK-Src signaling in normal and cancer cells. Curr Opin Cell Biol 2006, 18:516-523. 10.1016/j.ceb.2006.08.011, 16919435.
31. Schaller MD, Parsons JT. pp125FAK-dependent tyrosine phosphorylation of paxillin creates a high-affinity binding site for Crk. Mol Cell Biol 1995, 15:2635-2645. 230493, 7537852.
32. Grimsley CM, Kinchen JM, Tosello-Trampont AC, Brugnera E, Haney LB, Lu M, Chen Q, Klingele D, Hengartner MO, Ravichandran KS. Dock180 and ELMO1 proteins cooperate to promote evolutionarily conserved Rac-dependent cell migration. J Biol Chem 2004, 279:6087-6097.
33. Siesser PM, Hanks SK. The signaling and biological implications of FAK overexpression in cancer. Clin Cancer Res 2006, 12:3233-3237. 10.1158/1078-0432.CCR-06-0456, 16740741.
34. Raftopoulou M, Hall A. Cell migration: Rho GTPases lead the way. Dev Biol 2004, 265:23-32. 10.1016/j.ydbio.2003.06.003, 14697350.
35. Valles AM, Beuvin M, Boyer B. Activation of Rac1 by paxillin-Crk-DOCK180 signaling complex is antagonized by Rap1 in migrating NBT-II cells. J Biol Chem 2004, 279:44490-44496. 10.1074/jbc.M405144200, 15308668.
36. Tsubouchi A, Sakakura J, Yagi R, Mazaki Y, Schaefer E, Yano H, Sabe H. Localized suppression of RhoA activity by Tyr31/118-phosphorylated paxillin in cell adhesion and migration. J Cell Biol 2002, 159:673-683. 10.1083/jcb.200202117, 2173105, 12446743.
37. Hsia DA, Mitra SK, Hauck CR, Streblow DN, Nelson JA, Ilic D, Huang S, Li E, Nemerow GR, Leng J, Spencer KS, Cheresh DA, Schlaepfer DD. Differential regulation of cell motility and invasion by FAK. J Cell Biol 2003, 160:753-767. 10.1083/jcb.200212114, 2173366, 12615911.
38. Yu HG, Nam JO, Miller NL, Tanjoni I, Walsh C, Shi L, Kim L, Chen XL, Tomar A, Lim ST, Schlaepfer DD. p190RhoGEF (Rgnef) promotes colon carcinoma tumor progression via interaction with focal adhesion kinase. Cancer Res 2011, 71:360-370. 10.1158/0008-5472.CAN-10-2894, 3064514, 21224360.
39. Joshi K, Banasavadi-Siddegowda Y, Mo X, Kim SH, Mao P, Kig C, Nardini D, Sobol RW, Chow LM, Kornblum HI, Waclaw R, Beullens M, Nakano I. MELK-dependent FOXM1 phosphorylation is essential for proliferation of glioma stem cells. Stem Cells 2013, 31:1051-1063. 10.1002/stem.1358, 3744761, 23404835.
40. Saito R, Nakauchi H, Watanabe S. Serine/threonine kinase, Melk, regulates proliferation and glial differentiation of retinal progenitor cells. Cancer Sci 2012, 103:42-49. 10.1111/j.1349-7006.2011.02104.x, 21923749.
41. Badouel C, Korner R, Frank-Vaillant M, Couturier A, Nigg EA, Tassan JP. M-phase MELK activity is regulated by MPF and MAPK. Cell Cycle 2006, 5:883-889. 10.4161/cc.5.8.2683, 16628004.
42. Yilmaz M, Christofori G, Lehembre F. Distinct mechanisms of tumor invasion and metastasis. Trends Mol Med 2007, 13:535-541. 10.1016/j.molmed.2007.10.004, 17981506.
43. Chodniewicz D, Klemke RL. Regulation of integrin-mediated cellular responses through assembly of a CAS/Crk scaffold. Biochim Biophys Acta 2004, 1692:63-76. 10.1016/j.bbamcr.2004.03.006, 15246680.
44. Zhai J, Lin H, Nie Z, Wu J, Canete-Soler R, Schlaepfer WW, Schlaepfer DD. Direct interaction of focal adhesion kinase with p190RhoGEF. J Biol Chem 2003, 278:24865-24873. 10.1074/jbc.M302381200, 12702722.
45. Qu Y, Li J, Cai Q, Liu B. Hec1/Ndc80 is overexpressed in human gastric cancer and regulates cell growth. J Gastroenterol 2014, 49:408-418. 10.1007/s00535-013-0809-y, 23591767.
46. Bandyopadhyay S, Zhan R, Chaudhuri A, Watabe M, Pai SK, Hirota S, Hosobe S, Tsukada T, Miura K, Takano Y, Saito K, Pauza ME, Hayashi S, Wang Y, Mohinta S, Mashimo T, Iiizumi M, Furuta E, Watabe K. Interaction of KAI1 on tumor cells with DARC on vascular endothelium leads to metastasis suppression. Nat Med 2006, 12:933-938. 10.1038/nm1444, 16862154.