CCRK depletion inhibits glioblastoma cell proliferation in a cilium-dependent manner

EMBO Reports

Volumn 14, Issue 8, 2013, Pages 741-747

  Yang, Ying ^a   Roine, Niina ^a   Mäkelä, Tomi P ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

Author keywords

CCRK; cilia; glioblastoma; ICK; MAK

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; CELL CYCLE RELATED KINASE; DNA; INTESTINAL CELL KINASE; MESSENGER RNA; PHOSPHATIDYLINOSITOL 3 KINASE INHIBITOR; PROTEIN KINASE; SHORT HAIRPIN RNA; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CANCER CELL; CELL CYCLE; CELL PROLIFERATION; CELL STRAIN 3T3; ENZYME ACTIVITY; ENZYME SUBSTRATE; EUKARYOTIC FLAGELLUM; FIBROBLAST; GENETIC TRANSDUCTION; GLIOBLASTOMA; GLIOMA CELL; GROWTH INHIBITION; LENTIVIRINAE; NONHUMAN; PRIORITY JOURNAL; TUMOR GROWTH;

ANIMALS; BRAIN NEOPLASMS; CELL CYCLE; CELL LINE, TUMOR; CELL PROLIFERATION; CILIA; CYCLIN-DEPENDENT KINASES; GENE EXPRESSION REGULATION, NEOPLASTIC; GLIOBLASTOMA; HUMANS; MICE; NIH 3T3 CELLS; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; RNA, SMALL INTERFERING;

EID: 84881475435     PISSN: 1469221X     EISSN: 14693178     Source Type: Journal    
DOI: 10.1038/embor.2013.80     Document Type: Article

References (36)

1. Ishikawa H, Marshall WF (2011) Ciliogenesis: building the cell's antenna. Nat Rev Mol Cell Biol 12: 222-234
2. Berbari NF, O'Connor AK, Haycraft CJ, Yoder BK (2009) The primary cilium as a complex signaling center. Curr Biol 19: R526-R535
3. Moser JJ, Fritzler MJ, Rattner JB (2009) Primary ciliogenesis defects are associated with human astrocytoma/glioblastoma cells. BMC Cancer 9: 448
4. Kim S, Zaghloul NA, Bubenshchikova E, Oh EC, Rankin S, Katsanis N, Obara T, Tsiokas L (2011) Nde1-mediated inhibition of ciliogenesis affects cell cycle re-entry. Nat Cell Biol 13: 351-360
5. Li A, Saito M, Chuang JZ, Tseng YY, Dedesma C, Tomizawa K, Kaitsuka T, Sung CH (2011) Ciliary transition zone activation of phosphorylated Tctex-1 controls ciliary resorption, S-phase entry and fate of neural progenitors. Nat Cell Biol 13: 402-411
6. Liu Y, Wu C, Galaktionov K (2004) p42, a novel cyclin-dependent kinase-activating kinase in mammalian cells. J Biol Chem 279: 4507-4514 (Pubitemid 38199041)
7. Ng SS et al (2007) Cell cycle-related kinase: a novel candidate oncogene in human glioblastoma. J Natl Cancer Inst 99: 936-948 (Pubitemid 47073500)
8. Wohlbold L, Larochelle S, Liao JC, Livshits G, Singer J, Shokat KM, Fisher RP (2006) The cyclin-dependent kinase (CDK) family member PNQALRE/CCRK supports cell proliferation but has no intrinsic CDK-activating kinase (CAK) activity. Cell Cycle 5: 546-554 (Pubitemid 43340534)
9. An X et al (2010) Functional characterisation of cell cycle-related kinase (CCRK) in colorectal cancer carcinogenesis. Eur J Cancer 46: 1752-1761
10. Feng H et al (2011) Cell cycle-related kinase is a direct androgen receptor-regulated gene that drives beta-catenin/T cell factor-dependent hepatocarcinogenesis. J Clin Invest 121: 3159-3175
11. Tam LW, Wilson NF, Lefebvre PA (2007) A CDK-related kinase regulates the length and assembly of flagella in Chlamydomonas. J Cell Biol 176: 819-829 (Pubitemid 46425542)
12. Ko HW, Norman RX, Tran J, Fuller KP, Fukuda M, Eggenschwiler JT (2010) Broad-minded links cell cycle-related kinase to cilia assembly and hedgehog signal transduction. Dev Cell 18: 237-247
13. Tukachinsky H, Lopez LV, Salic A (2010) A mechanism for vertebrate Hedgehog signaling: recruitment to cilia and dissociation of SuFu-Gli protein complexes. J Cell Biol 191: 415-428
14. Fu Z et al (2006) Identification of yin-yang regulators and a phosphorylation consensus for male germ cell-associated kinase (MAK)-related kinase. Mol Cell Biol 26: 8639-8654 (Pubitemid 44748594)
15. Wang LY, Kung HJ (2011) Male germ cell-associated kinase is overexpressed in prostate cancer cells and causes mitotic defects via deregulation of APC/C(CDH1). Oncogene 31: 2907-2918
16. Asleson CM, Lefebvre PA (1998) Genetic analysis of flagellar length control in Chlamydomonas reinhardtii: a new long-flagella locus and extragenic suppressor mutations. Genetics 148: 693-702 (Pubitemid 28087619)
17. Berman SA, Wilson NF, Haas NA, Lefebvre PA (2003) A novel MAP kinase regulates flagellar length in Chlamydomonas. Curr Biol 13: 1145-1149 (Pubitemid 36815264)
18. Bengs F, Scholz A, Kuhn D, Wiese M (2005) LmxMPK9, a mitogen-activated protein kinase homologue affects flagellar length in Leishmania mexicana. Mol Microbiol 55: 1606-1615 (Pubitemid 40342083)
19. Burghoorn J, Dekkers MP, Rademakers S, de Jong T, Willemsen R, Jansen G (2007) Mutation of the MAP kinase DYF-5 affects docking and undocking of kinesin-2 motors and reduces their speed in the cilia of Caenorhabditis elegans. Proc Natl Acad Sci USA 104: 7157-7162 (Pubitemid 47186025)
20. Omori Y et al (2010) Negative regulation of ciliary length by ciliary male germ cell-associated kinase (Mak) is required for retinal photoreceptor survival. Proc Natl Acad Sci USA 107: 22671-22676
21. Togawa K, Yan YX, Inomoto T, Slaugenhaupt S, Rustgi AK (2000) Intestinal cell kinase (ICK) localizes to the crypt region and requires a dual phosphorylation site found in map kinases. J Cell Physiol 183: 129-139 (Pubitemid 30130233)
22. Fu Z, Kim J, Vidrich A, Sturgill TW, Cohn SM (2009) Intestinal cell kinase, a MAP kinase-related kinase, regulates proliferation and G1 cell cycle progression of intestinal epithelial cells. Am J Physiol Gastrointest Liver Physiol 297: G632-G640
23. Marszalek JR, Ruiz-Lozano P, Roberts E, Chien KR, Goldstein LS (1999) Situs inversus and embryonic ciliary morphogenesis defects in mouse mutants lacking the KIF3A subunit of kinesin-II. Proc Natl Acad Sci USA 96: 5043-5048 (Pubitemid 29214532)
24. Ezratty EJ, Stokes N, Chai S, Shah AS, Williams SE, Fuchs E (2011) A role for the primary cilium in Notch signaling and epidermal differentiation during skin development. Cell 145: 1129-1141
25. Han YG, Kim HJ, Dlugosz AA, Ellison DW, Gilbertson RJ, Alvarez-Buylla A (2009) Dual and opposing roles of primary cilia in medulloblastoma development. Nat Med 15: 1062-1065
26. Wong SY, Seol AD, So PL, Ermilov AN, Bichakjian CK, Epstein EH Jr., Dlugosz AA, Reiter JF (2009) Primary cilia can both mediate and suppress Hedgehog pathway-dependent tumorigenesis. Nat Med 15: 1055-1061
27. Chakravarti A, Zhai G, Suzuki Y, Sarkesh S, Black PM, Muzikansky A, Loeffler JS (2004) The prognostic significance of phosphatidylinositol 3-kinase pathway activation in human gliomas. J Clin Oncol 22: 1926-1933 (Pubitemid 41095185)
28. Wang J, Hu L, Gupta N, Shamseldin T, Ozawa T, Klem J, Cardell M, Deen DF (1999) Induction and characterization of human glioma clones with different radiosensitivities. Neoplasia 1: 138-144
29. Yamashita T et al (2009) Essential and synergistic roles of RP1 and RP1L1 in rod photoreceptor axoneme and retinitis pigmentosa. J Neurosci 29: 9748-9760
30. Phirke P et al (2011) Transcriptional profiling of C. elegans DAF-19 uncovers a ciliary base-associated protein and a CDK/CCRK/LF2p-related kinase required for intraflagellar transport. Dev Biol 357: 235-247
31. Tam LW, Ranum PT, Lefebvre PA (2013) CDKL5 regulates flagellar length and localizes to the base of the flagella in Chlamydomonas. Mol Biol Cell 24: 588-600
32. Pugacheva EN, Jablonski SA, Hartman TR, Henske EP, Golemis EA (2007) HEF1-dependent Aurora A activation induces disassembly of the primary cilium. Cell 129: 1351-1363 (Pubitemid 46962087)
33. Xu J et al (2010) VHL inactivation induces HEF1 and Aurora kinase A. J Am Soc Nephrol 21: 2041-2046
34. Egeberg DL, Lethan M, Manguso R, Schneider L, Awan A, Jorgensen TS, Byskov AG, Pedersen LB, Christensen ST (2012) Primary cilia and aberrant cell signaling in epithelial ovarian cancer. Cilia 1: 15
35. Lutz MS, Burk RD (2006) Primary cilium formation requires von hippel-lindau gene function in renal-derived cells. Cancer Res 66: 6903-6907 (Pubitemid 44197663)
36. Seeley ES, Carriere C, Goetze T, Longnecker DS, Korc M (2009) Pancreatic cancer and precursor pancreatic intraepithelial neoplasia lesions are devoid of primary cilia. Cancer Res 69: 422-430