Differential signature of the centrosomal MARK4 isoforms in glioma

Analytical Cellular Pathology

Volumn 34, Issue 6, 2011, Pages 319-338

  Magnani, Ivana ^a   Novielli, Chiara ^a   Fontana, Laura ^a   Tabano, Silvia ^a   Rovina, Davide ^a   Moroni, Ramona F ^b   Bauer, Dario ^a,c   Mazzoleni, Stefania ^d   Colombo, Elisa A ^a   Tedeschi, Gabriella ^a   Monti, Laura ^a   Porta, Giovanni ^e   Bosari, Silvano ^c   Frassoni, Carolina ^b   Galli, Rossella ^d   Bello, Lorenzo ^a   Larizza, Lidia ^a  

^a UNIVERSITY OF MILAN   (Italy)

^b DEPARTMENT OF NEUROSURGERY   (Italy)

^c FONDAZIONE IRCCS CA GRANDA OSPEDALE MAGGIORE POLICLINICO   (Italy)

^d SAN RAFFAELE HOSPITAL   (Italy)

^e UNIVERSITY OF INSUBRIA   (Italy)

Author keywords

alternative splicing; glioma; MARK4 kinase; neural cancer stem cells; nucleolus

Indexed keywords

MICROTUBULE AFFINITY REGULATING KINASE 4; MICROTUBULE ASSOCIATED PROTEIN; PROTEIN SERINE THREONINE KINASE; UNCLASSIFIED DRUG; ISOENZYME; MARK4 PROTEIN, HUMAN; MARK4 PROTEIN, MOUSE; MESSENGER RNA; TUMOR MARKER;

ADULT; AGED; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN REGION; BRAIN VENTRICLE; CANCER GRADING; CANCER STEM CELL; CELLULAR DISTRIBUTION; CENTROSOME; CHILD; CONTROLLED STUDY; FEMALE; GLIOBLASTOMA; GLIOMA CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNODETECTION; MALE; MUTATIONAL ANALYSIS; NEURAL STEM CELL; NONHUMAN; NUCLEOLAR LOCALIZATION SIGNAL; PHENOTYPE; PRESCHOOL CHILD; PREVALENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SCHOOL CHILD; SEQUENCE ANALYSIS; TUMOR CELL; ANIMAL; BIOPSY; ENZYMOLOGY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GLIOMA; HUMAN GENOME; METABOLISM; MIDDLE AGED; MOUSE; NUCLEOLUS; NUCLEOTIDE SEQUENCE; PATHOLOGY; TUMOR CELL LINE;

ADULT; AGED; ANIMALS; BASE SEQUENCE; BIOPSY; CELL LINE, TUMOR; CELL NUCLEOLUS; CENTROSOME; CHILD; CHILD, PRESCHOOL; DNA MUTATIONAL ANALYSIS; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; GENOME, HUMAN; GLIOMA; HUMANS; ISOENZYMES; MALE; MICE; MIDDLE AGED; NEOPLASTIC STEM CELLS; NEURAL STEM CELLS; PHENOTYPE; PROTEIN-SERINE-THREONINE KINASES; RNA, MESSENGER; TUMOR MARKERS, BIOLOGICAL;

EID: 84864591281     PISSN: 22107177     EISSN: 22107185     Source Type: Journal    
DOI: 10.3233/ACP-2011-0031     Document Type: Article

References (49)

1. S. Guo and K.J. Kemphues, Par-1, a gene required for establishing polarity in C. elegans embryos, encodes a putative Ser/Thr kinase that is asymmetrically distributed, Cell 81 (1995), 611-620.
2. J.M. Shulman, R. Benton and D. St Johnston, The Drosophila homolog of C. elegans PAR-1 organizes the oocyte cytoskele-ton and directs oskar mRNA localization to the posterior pole, Cell 101 (2000), 377-388.
3. G. Drewes, A. Ebneth, U. Preuss, E.M. Mandelkow and E. Mandelkow, MARK, a novel family of protein kinases that phosphorylate microtubule-associated proteins and trigger microtubule disruption, Cell 89 (1997), 297-308. (Pubitemid 27199901)
4. B. Trinczek, M. Brajenovic, A. Ebneth and G. Drewes, MARK4 is a novel Microtubule-associated Proteins/Micro-tubule Affinity-regulating Kinase that binds to the cellular microtubule network and to centrosomes, J Biol Chem 279 (2004), 5915-5923. (Pubitemid 38220624)
5. W. Biernat, Y. Tohma, Y. Yonekawa, P. Kleihuesand H. Ohgaki, Alterations of cell cycle regulatory genes in primary (de novo) and secondary glioblastomas, Acta Neuropathol 94 (1997), 303-309. (Pubitemid 27450108)
6. J.P. Tassan and X. Le Goff, An overview of the KIN1/PAR-1/MARK kinase family, Biol Cell 96 (2004), 193-199. (Pubitemid 38461444)
7. M. Elbert, G. Rossi and P. Brennwald, The yeast Par-1 homologs Kin1 and Kin2 show genetic and physical interactions with components of the exocytic machinery, Mol Biol Cell 16 (2005), 532-549. (Pubitemid 40165553)
8. O. Göransson, M. Deak, S. Wullschleger, N.A. Morrice, A.R. Prescott and D.R. Alessi, Regulation of the polarity kinases PAR-1/MARK by 14-3-3 interaction and phosphorylation, J Cell Sc 119 (2006), 4059-4070. (Pubitemid 44650878)
9. G. Manning, D.B. Whyte, R. Martinez, T. Hunter and S. Sudarsanam, The protein kinase complement of the human genome, Science 298 (2002), 1912-1934. (Pubitemid 35425239)
10. A. Marx, C. Nugoor, S. Panneerselvam and E. Mandelkow, Structure and function of polarity-inducing kinase family MARK/Par-1 within the branch of AMPK/Snf1-related kinases, FASEB J 24 (2010), 1637-1648.
11. T. Kato, S. Satoh, H. Okabe, O. Kitahara, K. Ono, C. Kihara, T. Tanaka, T. Tsunoda, Y. Yamaoka, Y. Nakamura and Y. Furukawa, Isolation of a novel human gene, MARKL1, homologous to MARK3 and its involvement in hepatocellular carcinogenesis, Neoplasia 3 (2001), 4-9. (Pubitemid 32201604)
12. R.F. Moroni, S. De Biasi, P. Colapietro, L. Larizza and A. Beghini, Distinct expression pattern of microtubule-associated protein/microtubule affinity-regulating kinase 4 in differentiated neurons, Neuroscience 143 (2006), 83-94. (Pubitemid 44667314)
13. A. Schneider, A. Laage, O. von Ahsen, A. Fischer, M. Rossner, S. Scheek, S. Grünewald, R. Kuner, D. Weber, C. Krüger, B. Klaussner, B. Götz, H. Hiemisch, D. Newrzella, A. Martin-Villalba, A. Bach and M. Schwaninger, Identification of regulated genes during permanent focal cerebral ischemia: characterization of the protein kinase 9b5/MARKL1/MARK4, J Neurochem 88 (2004), 1114-1126. (Pubitemid 38280679)
14. A. Beghini, I. Magnani, G. Roversi, T. Piepoli, S. Di Terlizzi, R.F. Moroni, B. Pollo, A.M. Fuhrman Conti, J.K. Cowell, G. Finocchiaro and L. Larizza, The neural progenitor-restricted isoform of the MARK4 gene in 19q13.2 is upregulated in human gliomas and overexpressed in a subset of glioblastoma cell lines, Oncogene 22 (2003), 2581-2591. (Pubitemid 36605606)
15. D.W. Parsons, T.L. Wang, Y. Samuels, A. Bardelli, J.M. Cummins, L. DeLong, N. Silliman, J. Ptak, S. Szabo, J.K. Willson, S. Markowitz, K.W. Kinzler, B. Vogelstein, C. Lengauer and V.E. Velculescu, Colorectal cancer: Mutations in a signalling pathway, Nature 436 (2005), 792. (Pubitemid 41160630)
16. S. Yamashita, Y. Tsujino, K. Moriguchi, M. Tatematsu and T. Ushijima, Chemical genomic screening for methylation-silenced genes in gastric cancer cell lines using 5-aza-2'deoxycytidine treatment and oligonucleotide microarray, Cancer Sci 97 (2006), 64-71. (Pubitemid 43257029)
17. W Sun, K. Zhang, X. Zhang, W Lei, T. Xiao, J. Ma, S. Guo, S. Shao, H. Zhang, Y Liu, J. Yuan and Z. Hu, Identification of differentially expressed genes in human lung squamous cell carcinoma using suppression subtractive hybridization, Cancer lett 212 (2004), 83-93. (Pubitemid 38887723)
18. G. Roversi, R. Pfundt, R.F. Moroni, I. Magnani, S. van Reijmersdal, B. Pollo, H. Straatman, L. Larizza and E.F. Schoenmakers, Identification of novel genomic markers related to progression to glioblastoma through genomic profiling of 25 primary glioma cell lines, Oncogene 25 (2006), 1571-1583. (Pubitemid 43361942)
19. I. Magnani, C. Novielli, M. Bellini, G. Roversi, L. Bello and L. Larizza, Multiple localization of endogenous MARK4L protein in human glioma, Cell oncol 31 (2009), 357-370.
20. I. Magnani, S. Guerneri, B. Pollo, N. Cirenei, B.M. Colombo, G. Broggi, C. Galli, O. Bugiani, S. DiDonato, G. Finocchiaro and A.M. Fuhrman Conti, Increasing complexity of the karyotype in 50 human gliomas, Cancer Genet Cytogenet 75 (1994), 77-89.
21. P. Perego, A. Boiardi, N. Carenini, M. De Cesare, E. Dolfini, R. Giardini, I. Magnani, S. Martignone, A. Silvani, C. Soranzo and F. Zunino, Characterization of an established human, malignant, glioblastoma cell line (GBM) and its response to conventional drugs, J Cancer Res Clin Oncol 120 (1994), 585-592. (Pubitemid 24281406)
22. R. Galli, E. Binda, U. Orfanelli, B. Cipelletti, A. Gritti, S. De Vitis, R. Fiocco, C. Foroni, F. Dimeco and A. Vescovi, Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma, Cancer Res 64 (2004), 7011-7021. (Pubitemid 39331011)
23. C. Foroni, R. Galli, B. Cipelletti, A. Caumo, S. Alberti, R. Fiocco and A. Vescovi, Resilience to transformation and inherent genetic and functional stability of adult neural stem cells ex vivo, Cancer Res 67 (2007), 3725-3733. (Pubitemid 46762158)
24. K.J. Livak and T.D. Schmittgen, Analysis of relative gene expression data using real-time quantitative PCR and the 2-AACT method, Methods 25 (2001), 402-408. (Pubitemid 34164012)
25. J. Vandesompele, K. De Preter, F. Pattyn, B. Poppe, N. Van Roy, A. De Paepe and F. Speleman, Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes, Genome Biol 3 (2002), 0034.1-0034.11.
26. D.N. Louis, H. Ohgaki, O.D. Wiestler, W.K. Cavenee, P.C. Burger, A. Jouvet, B.W. Scheithauer and P. Kleihues, The 2007 WHO classification of tumours of the central nervous system, Acta Neuropathol 114 (2007), 97-109. (Pubitemid 47103521)
27. Cancer Genome Atlas Research Network, Comprehensive genomic characterization defines human glioblastoma genes and core pathways, Nature 455 (2008), 1061-1068.
28. S.C. Chauhan, N. Vinayek, D.M. Maher, M.C. Bell, K.A. Dunham, M.D. Koch, Y. Lio and M. Jaggi, Combined staining of TAG-72, MUC1 and CA125 improves labelling sensitivity in ovarian cancer: Antigens for multi-targeted antibody-guided therapy, J Histochem Cytochem 55 (2007), 867-875. (Pubitemid 47068277)
29. J. Lee, S. Kotliarova, Y. Kotliarov, A. Li, Q. Su, N.M. Donin, S. Pastorino, B.W. Purow, N. Christopher, W. Zhang, J.K. Park and H.A. Fine, Tumor stem cells derived from glioblastomas cultured in bFGF and EGF more closely mirror the phenotype and genotype of primary tumors than do serum-cultured cell lines, Cancer Cell 9 (2006), 391-403. (Pubitemid 43668737)
30. C. Greenman, P. Stephens, R. Smith, G.L. Dalgliesh, C. Hunter, G. Bignell, H. Davies, J. Teague, A. Butler, C. Stevens, S. Edkins, S. O'Meara, I. Vastrik, E.E. Schmidt, T. Avis, S. Barthorpe, G. Bhamra, G. Buck, B. Choudhury, J. Clements, J. Cole, E. Dicks, S. Forbes, K. Gray, K. Halliday, R. Harrison, K. Hills, J. Hinton, A. Jenkinson, D. Jones, et al., Patterns of somatic mutation in human cancer genomes, Nature 446 (2007), 153-158. (Pubitemid 46398669)
31. M. Noble andJ. Dietrich, The complex identityofbrain tumors: Emerging concerns regarding origin, diversity and plasticity, Trends Neurosci 27 (2004), 148-154. (Pubitemid 38251515)
32. A.L. Vescovi, R. Galli and B.A. Reynolds, Brain tumour stem cells, Nat Rev Cancer 6 (2006), 425-436.
33. J.P. Venables, Unbalanced alternative splicing and its significance in cancer, Bioessays 28 (2006), 378-386.
34. P.J. Grabowski and D.L. Black, Alternative RNA splicing in the nervous system, Prog Neurobiol 65 (2001), 289-308. (Pubitemid 32709987)
35. F. Liu and C.X. Gong, Tau exon 10 alternative splicing and tauopathies, Mol Neurodegener 3 (2008), 8.
36. H. Harris, Alongviewoffashionsincancer research, Bioessays 27 (2005), 833-888.
37. A. Tacconelli, A.R. Farina, L. Cappabianca, A. Gulino and A.R. Mackay, TrkAIII. A novel hypoxia-regulated alternative TrkA splice variant of potential physiological and pathological importance, Cell Cycle 4 (2005), 8-9. (Pubitemid 41038914)
38. A. Mohr, R.M. Zwacka, G. Jarmy, C. Büneker, H. Schrezen-meier, K. Döhner, C. Beltinger, M. Wiesneth, K.M. Debatin and K. Stahnke, Caspase-8L expression protects CD34+ hematopoietic progenitor cells and leukemic cells from CD95-mediated apoptosis, Oncogene 24 (2005), 2421-2429. (Pubitemid 40546700)
39. H. Mochizuki, T. Nishi, J.M. Bruner, P.S. Lee, V.A. Levin and H. Saya, Alternative splicing of neurofibromatosis type 1 gene transcript in malignant brain tumors: PCR analysis of frozen-section mRNA, Mol Carcinog 6 (1992), 83-87.
40. V. Vella, G. Pandini, L. Sciacca, R. Mineo, R. Vigneri, V. Pezzino and A. Belfiore, A novel autocrine loop involving IGF-II and the insulin receptor isoform-A stimulates growth of thyroid cancer, J Clin Endocrinol Metab 87 (2002), 245-254. (Pubitemid 34084698)
41. S.K. Singh, I.D. Clarke, M. Terasaki, V.E. Bonn, C. Hawkins, J. Squire and P.B. Dirks, Identification of a cancer stem cell in human brain tumors, Cancer Res 63 (2003), 5821-5828. (Pubitemid 37187480)
42. Q.B. Zhang, X.Y. Ji, Q. Huang, J. Dong, Y.D. Zhu and Q. Lan, Differentiation profile ofbrain tumor stem cells:Acomparative study with neural stem cells, Cell Res 16 (2006), 909-915. (Pubitemid 44973578)
43. L. López-Saavedra and L.A. Herrera, The role of alternative mRNA splicing in chromosome instability, Mutat Res 705 (2010), 246-225.
44. K.M. Sze, Y.P. Ching, D.Y. Jin and I.O. Ng, Role of a novel splice variantofmitotic arrest deficient1 (MAD1), MAD1beta, in mitotic checkpoint control in liver cancer, Cancer Res 68 (2008), 9194-9201.
45. M. Yasen, H. Mizushima, K. Mogushi, G. Obulhasim, K. Miyaguchi, K. Inoue, I. Nakahara, T. Ohta, A. Aihara, S. Tanaka, S. Arii and H. Tanaka, Expression of Aurora B and alternative variant forms in hepatocellular carcinoma and adjacent tissue, Cancer Sci 100 (2009), 472-480.
46. A.R. Farina, A. Tacconelli, L. Cappabianca, G. Cea, S. Panella, A. Chioda, A. Romanelli, C. Pedone, A. Gulino and A.R. Mackay, The alternative TrkAIII splice variant targets the centrosome and promotes genetic instability, Mol Cell Biol 29 (2009), 4812-4830.
47. R.S. Hames and A.M. Fry, Alternative splice variants of the human centrosome kinase Nek2 exhibit distinct patterns of expression in mitosis, Biochem J 361 (2002), 77-85. (Pubitemid 34171411)
48. G. Drewes, A. Ebneth and E.M. Mandelkow, MAPs, MARKs and microtubule dynamics, Trends Biochem Sci 23 (1998), 307-311.
49. M. Carmo-Fonseca, L. Mendes-Soares and I. Campos, To beor not to be in the nucleolus, Nat Cell Biol 2 (2000), E107-E112.