Maternal embryonic leucine zipper kinase is a key regulator of the proliferation of malignant brain tumors, including brain tumor stem cells

Journal of Neuroscience Research

Volumn 86, Issue 1, 2008, Pages 48-60

  Nakano, Ichiro ^a   Masterman Smith, Michael ^a   Saigusa, Kuniyasu ^a   Paucar, Andres A ^a   Horvath, Steve ^b   Shoemaker, Lorelei ^a   Watanabe, Momoko ^a   Negro, Alejandra ^c   Bajpai, Ruchi ^c   Howes, Amy ^c   Lelievre, Vincent ^a   Waschek, James A ^a,d   Lazareff, Jorge A ^a   Freije, William A ^a   Liau, Linda M ^a   Gilbertson, Richard J ^e   Cloughesy, Timothy F ^a   Geschwind, Daniel H ^a,d   Nelson, Stanley F ^a   Mischel, Paul S ^a   Terskikh, Alexey V ^c   Kornblum, Harley I ^a,f   more..

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c BURNHAM INSTITUTE   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^f CIMI   (United States)

Author keywords

Brain tumor; Brain tumor stem cell; Maternal embryonic leucine zipper kinase; Proliferation

Indexed keywords

LEUCINE ZIPPER PROTEIN; PROTEIN KINASE B; RAS PROTEIN; SMALL INTERFERING RNA;

ADULT; AGED; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN TUMOR; CANCER GRADING; CANCER GROWTH; CANCER STEM CELL; CANCER SURVIVAL; CELL CULTURE; CELL PROLIFERATION; CELL TRANSFORMATION; CLINICAL ARTICLE; CONTROLLED STUDY; ENZYME INHIBITION; ENZYME REGULATION; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; UPREGULATION;

ADULT; AGED; ANIMALS; BRAIN NEOPLASMS; CELL PROLIFERATION; CELLS, CULTURED; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION REGULATION, NEOPLASTIC; GLIOBLASTOMA; HUMANS; MALE; MASS SPECTROMETRY; MICE; MICE, KNOCKOUT; MIDDLE AGED; NEOPLASTIC STEM CELLS; PITUITARY ADENYLATE CYCLASE-ACTIVATING POLYPEPTIDE; PROTEIN-SERINE-THREONINE KINASES; RECEPTORS, CELL SURFACE; RNA, SMALL INTERFERING; TRANSFECTION;

EID: 38049090322     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.21471     Document Type: Article

References (51)

1. Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, Hjelmeland AB, Dewhirst MW, Bigner DD, Rich JN. 2006. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 444:756-760.
2. Beullens M, Vancauwenbergh S, Morrice N, Derua R, Ceulemans H, Waelkens E, Bollen M. 2005. Substrate specificity and activity regulation of protein kinase MELK. J Biol Chem 280:40003-40011.
3. Cheng JC, Sakamoto KM, Horwitz EM, Karsten SL, Shoemaker L, Kornblum HI, Mali P. 2007. A meeting report: new technologies in stem cell research. Stem Cells (in press).
4. Clement V, Sanchez P, de Tribolet N, Radovanovic I, Ruiz i Altaba A. 2007. HEDGEHOG-GLI1 signaling regulates human glioma growth, cancer stem cell self-renewal, and tumorigenicity. Curr Biol 17:165-172.
5. Colwell CS, Michel S, Itri J, Rodriguez W, Tam J, Lelievre V, Hu Z, Waschek JA. 2004. Selective deficits in the circadian light response in mice lacking PACAP. Am J Physiol Regul Integr Comp Physiol 287:R1194-R1201.
6. Cox DR, Oakes D. 1990. Analysis of survival data. New York: Chapman and Hall.
7. Davezac N, Baldin V, Blot J, Ducommun B, Tassan JP. 2002. Human pEg3 kinase associates with and phosphorylates CDC25B phosphatase: a potential role for pEg3 in cell cycle regulation. Oncogene 21:7630-7641.
8. Easterday MC, Dougherty JD, Jackson RL, Ou J, Nakano I, Paucar AA, Roobini B, Dianati M, Irvin DK, Weissman IL, Terskikh AV, Geschwind DH, Kornblum HI. 2003. Neural progenitor genes. Germinal zone expression and analysis of genetic overlap in stem cell populations. Dev Biol 264:309-922.
9. Freije WA, Castro-Vargas FE, Fang Z, Horvath S, Cloughesy T, Liau LM, Mischel PS, Nelson SF. 2004. Gene expression profiling of gliomas strongly predicts survival. Cancer Res 64:6503-6510.
10. Gage FH. 2000. Mammalian neural stem cells. Science 287:1433-1438.
11. Galli R, Binda E, Orfanelli U, Cipelletti B, Gritti A, De Vitis SF, Fiocco R, Foroni C, Dimeco F, Vescovi A. 2004. Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma. Cancer Res 64:7011-7021.
12. Geschwind DH, Ou J, Easterday MC, Dougherty JD, Jackson RL, Chen Z, Antoine H, Terskikh A, Weissman IL, Nelson SF, Kornblum HI. 2001a. A genetic analysis of neural progenitor differentiation. Neuron 29:325-339.
13. Geschwind DH, Ou J, Easterday MC, Dougherty JD, Jackson RL, Chen Z, Antoine H, Terskikh A, Weissman IL, Nelson SF, Kornblum HI. 2001b. A genetic analysis of neural progenitor differentiation. Neuron 29(2):325-339.
14. Goodrich LV, Milenkovic L, Higgins KM, Scott MP. 1997. Altered neural cell fates and medulloblastoma in mouse patched mutants. Science 277:1109-1113.
15. 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. 2005. Maternal embryonic leucine zipper kinase/murine protein serine-threonine kinase 38 is a promising therapeutic target for multiple cancers. Cancer Res 65:9751-9761.
16. Groszer M, Erickson R, Scripture-Adams DD, Lesche R, Trumpp A, Zack JA, Kornblum HI, Liu X, Wu H. 2001. Negative regulation of neural stem/progenitor cell proliferation by the Pten tumor supporessor gene in vivo. Science 294:2186-2189.
17. Hemmati HD, Nakano I, Lazareff JA, Masterman-Smith M, Geschwind DH, Bronner-Fraser M, Kornblum HI. 2003a. Cancerous stem cells can arise from pediatric brain tumors. Proc Natl Acad Sci U S A 100: 15178-15183.
18. Hemmati HD, Nakano I, Lazareff JA, Masterman-Smith M, Geschwind DH, Bronner-Fraser M, Kornblum HI. 2003b. Cancerous stem cells can arise from pediatric brain tumors. Proc Natl Acad Sci U S A 100(25):15178-15183. Epub 12003 Nov 15126.
19. Kaplan E, Meier P. 1958. Nonparametric estimation from incomplete observations. J Am Stat Assoc 53:457.
20. Kato K, Ogura T, Kishimoto A, Minegishi Y, Nakajima N, Miyazaki M, Esumi H. 2002. Critical roles of AMP-activated protein kinase in constitutive tolerance of cancer cells to nutrient deprivation and tumor formation. Oncogene 21:6082-6090.
21. Kesari S, Ramakrishna N, Sauvageot C, Stiles CD, Wen PY. 2005. Targeted molecular therapy of malignant gliomas. Curr Neurol Neurosci Rep 5:186-197.
22. Kim M, Morshead CM. 2003. Distinct populations of forebrain neural stem and progenitor cells can be isolated using side-population analysis. J Neurosci 23(33):10703-10709.
23. Kornblum HI, Geschwind DH. 2001. Molecular markers in CNS stem cell research: hitting a moving target. Nat Rev Neurosci 2:843-846.
24. Kornblum HI, Chugani HT, Tatsukawa K, Gall CM. 1994. Cerebral hemidecortication alters expression of transforming growth factor alpha mRNA in the neostriatum of developing rats. Brain Res Mol Brain Res 21:107-114.
25. Kornblum HI, Hussain R, Wiesen J, Miettinen P, Zurcher SD, Chow K, Derynck R, Werb Z. 1998. Abnormal astrocyte development and neuronal death in mice lacking the epidermal growth factor receptor. J Neurosci Res 53:697-717.
26. Lee J, Kotliarova S, Kotliarov Y, Li A, Su Q, Donin NM, Pastorino S, Purow BW, Christopher N, Zhang W, Park JK, Fine HA. 2006. 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 9:391-403.
27. Li C, Wong WH. 2001. Model-based analysis of oligonucleotide arrays: expression index computation and outlier detection. Proc Natl Acad Sci U S A 98:31-36.
28. Liu G, Yuan X, Zeng Z, Tunici P, Ng H, Abdulkadir IR. 2006. Analysis of gene expression and chemoresistance of CD133+ cancer stem cells in glioblastoma. Mol Cancer 5:67.
29. Liu J, Guo L, Luo Y, Li JW, Li H. 2000. All trans-retinoic acid suppresses in vitro growth and down-regulates LIF gene expression as well as telomerase activity of human medulloblastoma cells. Anticancer Res 20:2659-2664.
30. Lizcano JM, Goransson O, Toth R, Deak M, Morrice NA, Boudeau J, Hawley SA, Udd L, Makela TP, Hardie DG, Alessi DR. 2004. LKB1 is a master kinase that activates 13 kinases of the AMPK subfamily, including MARK/PAR-1. Embo J 23:833-843.
31. 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. 2005. Maternal embryonic leucine zipper kinase (MELK) regulates multipotent neural progenitor proliferation. J Cell Biol 170:413-427.
32. Naldini L, Blomer U, Gallay P, Ory D, Mulligan R, Gage FH, Verma IM, Trono D. 1996. In vivo gene delivery and stable transduction of nondividing cells by a lentiviral vector. Science 272:263-267.
33. Newton HBERAT. 2004. Molecular neuro-oncology and development of targeted therapeutic strategies for brain tumors. Part 2: PI3K/Akt/PTEN, mTOR, SHH/PTCH and angiogenesis. Expert Rev Anticancer Ther 4:105-128.
34. Nicot A, Lelievre V, Tam J, Waschek JA, DiCicco-Bloom E. 2002. Pituitary adenylate cyclase-activating polypeptide and sonic hedgehog interact to control cerebellar granule precursor cell proliferation. J Neurosci 22:9244-9254.
35. Palmer TD, Ray J, Gage FH. 1995. FGF-2-responsive neuronal progenitors reside in proliferative and quiescent regions of the adult rodent brain. Mol Cell Neurosci 6:474-486.
36. Phillips HS, Kharbanda S, Chen R, Forrest WF, Soriano RH, Wu TD, Misra A, Nigro JM, Colman H, Soroceanu L, Williams PM, Modrusan Z, Feuerstein BG, Aldape K. 2006. Molecular subclasses of high-grade glioma predict prognosis, delineate a pattern of disease progression, and resemble stages in neurogenesis. Cancer Cell 9:157-173.
37. Pomeroy SL, Tamayo P, Gaasenbeek M, Sturla LM, Angelo M, McLaughlin ME, Kim JY, Goumnerova LC, Black PM, Lau C, Allen JC, Zagzag D, Olson JM, Curran T, Wetmore C, Biegel JA, Poggio T, Mukherjee S, Rifkin R, Califano A, Stolovitzky G, Louis DN, Mesirov JP, Lander ES, Golub TR. 2002. Prediction of central nervous system embryonal tumour outcome based on gene expression. Nature 415:436-442.
38. Reynolds BA, Weiss S. 1992. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 255:1707-1710.
39. Shevchenko A, Wilm M, Vorm O, Jensen ON, Podtelejnikov AV, Neubauer G, Mortensen P, Mann M. 1996. A strategy for identifying gel-separated proteins in sequence databases by MS alone. Biochem Soc Trans 24:893-896.
40. Singh SK, Clarke ID, Terasaki M, Bonn VE, Hawkins C, Squire J, Dirks PB. 2003. Identification of a cancer stem cell in human brain tumors. Cancer Res 63:5821-5828.
41. Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J, Hide T, Henkelman RM, Cusimano MD, Dirks PB. 2004. Identification of human brain tumour initiating cells. Nature 432: 396-401.
42. Sonoda Y, Ozawa T, Hirose Y, Aldape KD, McMahon M, Berger MS, Pieper RO. 2001. Formation of intracranial tumors by genetically modified human astrocytes defines four pathways critical in the development of human anaplastic astrocytoma. Cancer Res 61:4956-4960.
43. Stapleton D, Mitchelhill KI, Gao G, Widmer J, Michell BJ, Teh T, House CM, Fernandez CS, Cox T, Witters LA, Kemp BE. 1996. Mammalian AMP-activated protein kinase subfamily. J Biol Chem 271:611-614.
44. Suzuki A, Kusakai G, Kishimoto A, Lu J, Ogura T, Esumi H. 2003a. ARK5 suppresses the cell death induced by nutrient starvation and death receptors via inhibition of caspase 8 activation, but not by chemotherapeutic agents or UV irradiation. Oncogene 22:6177-6182.
45. Suzuki A, Kusakai G, Kishimoto A, Lu J, Ogura T, Lavin MF, Esumi H. 2003b. Identification of a novel protein kinase mediating Akt survival signaling to the ATM protein. J Biol Chem 278:48-53.
46. Taylor MD, Poppleton H, Fuller C, Su X, Liu Y, Jensen P, Magdaleno S, Dalton J, Calabrese C, Board J, Macdonald T, Rutka J, Guha A, Gajjar A, Curran T, Gilbertson RJ. 2005. Radial glia cells are candidate stem cells of ependymoma. Cancer Cell 8:323-335.
47. Thompson MC, Fuller C, Hogg TL, Dalton J, Finkelstein D, Lau CC, Chintagumpala M, Adesina A, Ashley DM, Kellie SJ, Taylor MD, Curran T, Gajjar A, Gilbertson RJ. 2006. Genomics identifies medulloblastoma subgroups that are enriched for specific genetic alterations. J Clin Oncol 24:1924-1931.
48. Tso CL, Freije WA, Day A, Chen Z, Merriman B, Perlina A, Lee Y, Dia EQ, Yoshimoto K, Mischel PS, Liau LM, Cloughesy TF, Nelson SF. 2006. Distinct transcription profiles of primary and secondary glioblastoma subgroups. Cancer Res 66:159-167.
49. Vulsteke V, Beullens M, Boudrez A, Keppens S, Van Eynde A, Rider MH, Stalmans W, Bollen M. 2003. Inhibition of spliceosome assembly by the cell cycle-regulated protein kinase MELK and involvement of splicing factor NIPP1. J Biol Chem 279:8642-8647.
50. Zhu W, Giangrande PH, Nevins JR. 2004. E2Fs link the control of G1/S and G2/M transcription. Embo J 23:4615-4626.
51. Zufferey R, Dull T, Mandel RJ, Bukovsky A, Quiroz D, Naldini L, Trono D. 1998. Self-inactivating lentivirus vector for safe and efficient in vivo gene delivery. J Virol 72:9873-9880.