Calcium/calmodulin-dependent protein kinase type IV Is a target gene of the Wnt/β-catenin signaling pathway

Journal of Cellular Physiology

Volumn 221, Issue 3, 2009, Pages 658-667

  Arrázola, Macarena S ^a   Varela Nallar, Lorena ^a   Colombres, Marcela ^a   Toledo, Enrique M ^a   Cruzat, Fernando ^b   Pavez, Leonardo ^c   Assar, Rodrigo ^d   Aravena, Andrés ^d   González, Mauricio ^c   Montecino, Martín ^b   Maass, Alejandro ^d   Martínez, Servet ^d   Inestrosa, Nibaldo C ^a  

^a PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

^b UNIVERSITY OF CONCEPCIÓN   (Chile)

^c UNIVERSITY OF CHILE   (Chile)

^d DEPARTAMENTO DE FÍSICA   (Chile)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE IV; LITHIUM; LYMPHOID ENHANCER FACTOR 1; MESSENGER RNA; TRANSCRIPTION FACTOR; WNT PROTEIN; WNT3A PROTEIN; LITHIUM CHLORIDE; T CELL FACTOR PROTEIN; WNT3 PROTEIN;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIOINFORMATICS; CONTROLLED STUDY; EMBRYO; GENE TARGETING; GENOME; HIPPOCAMPUS; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IN VIVO STUDY; MEMORY DISORDER; MOUSE; NERVE CELL; NONHUMAN; PREDICTION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; SPATIAL MEMORY; ANIMAL; ANIMAL BEHAVIOR; BIOLOGY; CELL LINE; CYTOLOGY; DISEASE MODEL; DRUG EFFECT; ENHANCER REGION; GENE EXPRESSION; GENETIC TRANSFECTION; GENETICS; METABOLISM; MOUSE STRAIN; NEUROPSYCHOLOGICAL TEST; PATHOLOGY; PHYSIOLOGY; PROMOTER REGION; RAT STRAIN; TRANSGENIC MOUSE;

MUS; RATTUS;

ALZHEIMER DISEASE; ANIMALS; BEHAVIOR, ANIMAL; BETA CATENIN; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 4; CELL LINE; COMPUTATIONAL BIOLOGY; DISEASE MODELS, ANIMAL; ENHANCER ELEMENTS, GENETIC; GENE EXPRESSION; HIPPOCAMPUS; HUMANS; LITHIUM CHLORIDE; MICE; MICE, INBRED STRAINS; MICE, TRANSGENIC; NEURONS; NEUROPSYCHOLOGICAL TESTS; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; RATS; RATS, INBRED STRAINS; SIGNAL TRANSDUCTION; TCF TRANSCRIPTION FACTORS; TRANSFECTION; WNT PROTEINS;

EID: 70449699789     PISSN: 00219541     EISSN: None     Source Type: Journal    
DOI: 10.1002/jcp.21902     Document Type: Article

References (75)

1. Alvarez AR, Godoy JA, Mullendorff K, Olivares GH, Bronfman M, Inestrosa NC. 2004. Wnt- 3a overcomes β-amyloid toxicity in rat hippocampal neurons. Exp Cell Res 297:186-196. (Pubitemid 38759572)
2. 2+-and stimulus duration-dependent switch for hippocampal gene expression. Cell 87:1203-1214.
3. Bok J, Wang Q, Huang J, Green S. 2007. CaMKII and CaMKIV mediate distinct prosurvival signaling pathways in response to depolarization in neurons. Mol Cell Neurosci 36:13-26. (Pubitemid 47379552)
4. Brabletz T, Jung A, Dag S, Hlubek F, Kirchner T. 1999. β-catenin regulates the expression of the matrix metalloproteinase-7 in human colorectal cancer. Am J Pathol 155:1033-1038. (Pubitemid 29488909)
5. Cadigan KM, Fish MP, Rulifson EJ, Nusse R. 1998. Wingless repression of Drosophila frizzled 2 expression shapes the Wingless morphogen gradient in the wing. Cell 93:767-777. (Pubitemid 28257583)
6. Caricasole A, Copani A, Caraci F, Aronica E, Rosenmuller AJ, Caruso A, Storto M, Gaviraghi G, Terstappen GC, Nicoletti F. 2004. Induction of Dickkopf-1, a negative modulator of the Wnt pathway, is associated with neuronal degeneration in Alzheimer's brain. J Neurosci 24:6021-6027. (Pubitemid 38859398)
7. Cerpa W, Godoy JA, Alfaro I, Farías GG, Metcalfe MJ, Fuentealba R, Bonansco C, Inestrosa NC. 2008. Wnt-7a modulates the synaptic vesicle cycle and synaptic transmission in hippocampal neurons. J Biol Chem 283:5918-5927.
8. Chacón MA, Varela-Nallar L, Inestrosa NC. 2008. Frizzled-1 is involved in the neuroprotective effect of Wnt3a against Aβ oligomers. J Cell Physiol 217:215-227.
9. Chamorro MN, Schwartz DR, Vonica A, Brivanlou AH, Cho KR, Varmus HE. 2005. FGF-20 and DKK1 are transcriptional targets of β-catenin and FGF-20 is implicated in cancer and development. EMBO J 24:73-84. (Pubitemid 40188465)
10. Chen G, Chen KS, Knox J, Inglis J, Bernard A, Martin SJ, Justice A, McConlogue L, Games D, Freedman SB, Morris RG. 2000. A learning deficit related to age and β-amyloid plaques in a mouse model of Alzheimer's disease. Nature 408:975-979. (Pubitemid 32101643)
11. Clevers H. 2006. Wnt/β-catenin signaling in development and disease. Cell 127:469-480.
12. Cohen S, Greenberg ME. 2008. Communication between the synapse and the nucleus in neuronal development, plasticity and disease. Annu Rev Cell Dev Biol 24:183-209.
13. Colombres M, Henríquez JP, Reig GF, Scheu J, Calderón R, Alvarez A, Brandan E, Inestrosa NC. 2008. Heparin activates Wnt signaling for neuronal morphogenesis. J Cell Physiol 216:805-815.
14. Crawford HC, Fingleton BM, Rudolph-Owen LA, Goss KJ, Rubinfeld B, Polakis P, Matrisian LM. 1999. The metalloproteinase matrilysin is a target of β-catenin transactivation in intestinal tumors. Oncogene 18:2883-2891. (Pubitemid 29250878)
15. Davuluri RV, Sumio YS, Zhang MQ. 2000. CART Classification of human 5′ UTR sequences. Genome Res 10:1807-1816.
16. De Ferrari GV, Chacon MA, Barria MI, Garrido JL, Godoy JA, Olivares G, Reyes AE, Alvarez A, Bronfman M, Inestrosa NC. 2003. Activation of Wnt signaling rescues neurodegeneration and behavioral impairments induced by β-amyloid fibrils. Mol Psychiatry 8:195-208. (Pubitemid 36315228)
17. Dorsky RI, Raible DW, Moon RT. 2000. Direct regulation of nacre, a zebrafish MITF homolog required for pigment cell formation, by the Wnt pathway. Genes Dev 14:158-162.
18. Finkbeiner S, Tavazoie SF, Maloratsky A, Jacobs KM, Harris KM, Greenberg ME. 1997. CREB: A major mediator of neuronal neurotrophin responses. Neuron 19:1031-1047. (Pubitemid 27512364)
19. Fuentealba RA. 2005. Role of the Wnt signaling pathway in the toxicity of the β-amyloid peptide in cellular models of Alzheimer's disease. PhD Thesis, Program in Biological Sciences, P. Catholic University of Chile.
20. Fukushima H, Maeda R, Suzuki R, Suzuki A, Nomoto M, Toyoda H, Wu LJ, Xu H, Zhao MG, Ueda K, Kitamoto A, Mamiya N, Yoshida T, Homma S, Masushige S, Zhuo M, Kida S. 2008. Upregulation of calcium/calmodulin-dependent protein kinase IV improves memory formation and rescues memory loss with aging. J Neurosci 28:9910-9919.
21. Galceran J, Sustmann C, Hsu SC, Folberth S, Grosschedl R. 2004. LEF1-mediated regulation of Delta-like1 links Wnt and Notch signaling in somitogenesis. Genes Dev 18:2718-2723. (Pubitemid 39507764)
22. Gallin WJ, Greenberg ME. 1995. Calcium regulation of gene expression in neurons: The mode of entry matters. Curr Opin Neurobiol 5:367-374.
23. Garcia-Alloza M, Robbins EM, Zhang-Nunes SX, Purcell SM, Betensky RA, Raju S, Prada C, Greenberg SM, Bacskai BJ, Frosch MP. 2006. Characterization of amyloid deposition in the APPswe/PS1dE9 mouse model of Alzheimer disease. Neurobiol Dis 24:516-524. (Pubitemid 44716680)
24. González-Sancho JM, Aguilera O, Garcîa JM, Pendás-Franco N, Peña C, Cal S, García de Herreros A, Bonilla F, Muñoz A. 2005. The Wnt antagonist DICKKOPF-1 gene is a downstream target of β-catenin/TCF and is downregulated in human colon cancer. Oncogene 24:1098-1103.
25. Gordon MD, Nusse R. 2006. Wnt signaling: Multiple pathways, multiple receptors, and multiple transcription factors. J Biol Chem 281:22429-22433.
26. Hardy J, Selkoe DJ. 2002. The amyloid hypothesis of Alzheimer's disease: Progress and problems on the road to therapeutics. Science 297:353-356. (Pubitemid 34790756)
27. Hofmann M, Schuster-Gossler K, Watabe-Rudolph M, Aulehla A, Herrmann BG, Gossler A. 2004. WNT signaling, in synergy with T/TBX6, controls Notch signaling by regulating Dll1 expression in the presomitic mesoderm of mouse embryos. Genes Dev 18:2712-2717. (Pubitemid 39507763)
28. Hu SC, Chrivia J, Ghosh A. 1999. Regulation of CBP-mediated transcription by neuronal calcium signaling. Neuron 22:799-808. (Pubitemid 29203502)
29. Impey S, Mark M, Villacres EC, Poser S, Chavkin C, Storm DR. 1996. Induction of CRE-mediated gene expression by stimuli that generate long-lasting LTP in area CA1 of the hippocampus. Neuron 16:973-982. (Pubitemid 126335761)
30. Impey S, Fong AL, Wang Y, Cardinaux JR, Fass DM, Obrietan K, Wayman GA, Storm DR, Soderling TR, Goodman RH. 2002. Phosphorylation of CBP mediates transcriptional activation by neural activity and CaM kinase IV. Neuron 34:235-244. (Pubitemid 34442566)
31. Inestrosa NC, Toledo EM. 2008. The role of Wnt signaling in neuronal dysfunction in Alzheimer's disease. Mol Neurodegener 3:9.
32. Inestrosa N, De Ferrari GV, Garrido JL, Alvarez A, Olivares GH, Barría MI, Bronfman M, Chacón MA. 2002. Wnt signaling involvement in β-amyloid-dependent neurodegeneration. Neurochem Int 41:341-344. (Pubitemid 34899423)
33. Inestrosa N, Varela-Nallar L, Grabowski CP, Colombres M. 2007. Synaptotoxicity in Alzheimer's disease:The Wnt signaling pathway as a molecular target. IUBMB Life 59:316-321. (Pubitemid 46763756)
34. 2+/calmodulin-dependent protein kinase during neuronal differentiation. Proc Natl Acad Sci USA 88:4050-4053.
35. Jho EH, Zhang T, Domon C, Joo CK, Freund JN, Costantini F. 2002. Wnt/β-catenin/Tcf signaling induces the transcription of Axin2, a negative regulator of the signaling pathway. Mol Cell Biol 22:1172-1183. (Pubitemid 34094853)
36. Jung HC, Kim K. 2005. Identification of MYCBP as a β-catenin/LEF-1 target using DNA microarray analysis. Life Sci 77:1249-1262. (Pubitemid 40898323)
37. Kim TH, Xiong H, Zhang Z, Ren B. 2005. β-Catenin activates the growth factor endothelin-1 in colon cancer cells. Oncogene 24:597-604. (Pubitemid 40188564)
38. Kioussi C, Briata P, Baek SH, Rose DW, Hamblet NS, Herman T, Ohgi KA, Lin C, Gleiberman A, Wang J, Brault V, Ruiz-Lozano P, Nguyen HD, Kemler R, Glass CK, Wynshaw-Boris A, Rosenfeld MG. 2002. Identification of a Wnt/Dvl/β-Catenin → Pitx2 pathway mediating cell-type-specific proliferation during development. Cell 111:673-685. (Pubitemid 35441249)
39. Klein PS, Melton DA. 1996. A molecular mechanism for the effect of lithium on development. Proc Natl Acad Sci USA 93:8455-8459.
40. Lee SM, Tole S, Grove E, McMahon AP. 2000. A local Wnt-3a signal is required for development of the mammalian hippocampus. Development 127:457-467. (Pubitemid 30093394)
41. Lei Q, Jeong Y, Misra K, Li S, Zelman AK, Epstein DJ, Matise MP. 2006. Wnt signaling inhibitors regulate the transcriptional response to morphogenetic Shh-Gli signaling in the neural tube. Dev Cell 11:325-337. (Pubitemid 44283939)
42. Leow CC, Romero MS, Ross S, Polakis P, Gao WQ. 2004. Hath1, down-regulated in colon adenocarcinomas, inhibits proliferation and tumorigenesis of colon cancer cells. Cancer Res 64:6050-6057. (Pubitemid 39129403)
43. Logan CY, Nusse R. 2006. The Wnt signaling pathway to development and disease. Annu Rev Cell Dev Biol 20:781-810.
44. Lustig B, Jerchow B, Sachs M, Weiler S, Pietsch T, Karsten U, van de Wetering M, Clevers H, Schlag PM, Birchmeier W, Behrens J. 2002. Negative feedback loop of Wnt signaling through upregulation of conductin/axin2 in colorectal and liver tumors. Mol Cell Biol 22:1184-1193. (Pubitemid 34094854)
45. Magdesian MH, Carvalho MM, Mendes FA, Saraiva LM, Juliano MA, Juliano L, Garcia-Abreu J, Ferreira ST. 2008. Amyloid-β binds to the extracellular cysteine-rich domain of Frizzled and inhibits Wnt/β-catenin signaling. J Biol Chem 283:9359-9368.
46. Mann B, Gelos M, Siedow A, Hanski ML, Gratchev A, Ilyas M, Bodmer WF, Moyer MP, Riecken EO, Buhr HJ, Hanski C. 1999. Target genes of β-catenin-T cell-factor/lymphoid-enhancer-factor signaling in human colorectal carcinomas. Proc Natl Acad Sci USA 96:1603-1608. (Pubitemid 29098498)
47. Marie H, Morishita W, Yu X, Calakos N, Malenka RC. 2005. Generation of silent synapses by acute in vivo expression of CaMKIV and CREB. Neuron 45:741-752. (Pubitemid 40320708)
48. Masckauchán TN, Shawber CJ, Funahashi Y, Li CM, Kitajewski J. 2005. Wnt/β-catenin signaling induces proliferation, survival and interleukin-8 in human endothelial cells. Angiogenesis 8:43-51. (Pubitemid 41223838)
49. Mbebi C, Sée V, Mercken L, Pradier L, Müller U, Loeffler JP. 2002. Amyloid precursor protein family-induced neuronal death is mediated by impairment of the neuroprotective calcium/ calmodulin protein kinase IV-dependent signaling pathway. J Biol Chem 277:20979-20990. (Pubitemid 34967409)
50. McGrew LL, Takemaru K, Bates R, Moon RT. 1999. Direct regulation of the Xenopus engrailed-2 promoter by the Wnt signaling pathway, and a molecular screen for Wntresponsive genes, confirm a role for Wnt signaling during neural patterning in Xenopus. Mech Dev 87:21-32. (Pubitemid 29428083)
51. Niida A, Hiroko T, Kasai M, Furukawa Y, Nakamura Y, Suzuki Y, Sugano S, Akiyama T. 2004. DKK1, a negative regulator of Wnt signaling, is a target of the β-catenin/TCF pathway. Oncogene 23:8520-8526. (Pubitemid 39540802)
52. Pereira L, Yi F, Merrill BJ. 2006. Repression of Nanog gene transcription by Tcf3 limits embryonic stem cell self-renewal. Mol Cell Biol 26:7479-7491. (Pubitemid 44547699)
53. Pfaffl MW. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:2002-2007.
54. Pilon N, Oh K, Sylvestre JR, Bouchard N, Savory J, Lohnes D. 2006. Cdx4 is a direct target of the canonical Wnt pathway. Dev Biol 289:55-63. (Pubitemid 41804088)
55. Quintanilla RA, Munoz FJ, Metcalfe MJ, Hitschfeld M, Olivares G, Godoy JA, Inestrosa NC. 2005. Trolox and 17β-estradiol protect against amyloid β-peptide neurotoxicity by a mechanism that involves modulation of the Wnt signaling pathway. J Biol Chem 280:11615-11625. (Pubitemid 40418475)
56. Rahmani M, Read JT, Carthy JM, McDonald PC, Wong BW, Esfandiarei M, Si X, Luo Z, Luo H, Rennie PS, McManus BM., 2005. Regulation of the versican promoter by the β-catenin-Tcell factor complex in vascular smooth muscle cells. J Biol Chem 280:13019-13028.
57. Rockman SP, Currie SA, Ciavarella M, Vincan E, Dow C, Thomas RJ, Phillips WA. 2001. Id2 is a target of the β-catenin/T cell factor pathway in colon carcinoma. J Biol Chem 276:45113-45119.
58. Roose J, Huls G, van Beest M, Moerer P, van der Horn K, Goldschmeding R, Logtenberg T, Clevers H. 1999. Synergy between tumor suppressor APC and the β-catenin-Tcf4 target Tcf1. Science 285:1923-1926.
59. Saito H, Yasumoto K, Takeda K, Takahashi K, Fukuzaki A, Orikasa S, Shibahara S. 2002. Melanocyte-specific microphthalmia-associated transcription factor isoform activates its own gene promoter through physical interaction with lymphoid-enhancing factor 1. J Biol Chem 277:28787-122879
60. Sansom OJ, Reed KR, van de Wetering M, Muncan V, Winton DJ, Clevers H, Clarke AR. 2005. Cyclin D1 is not an immediate target of β-catenin following Apc loss in the intestine. J Biol Chem 280:28463-28467.
61. Sée V, Boutillier AL, Bito H, Loeffler JP. 2001. Calcium/calmodulin-dependent protein kinase type IV (CaMKIV) inhibits apoptosis induced by potassium deprivation in cerebellar granule neurons. FASEB J 15:134-144.
62. Shtutman M, Zhurinsky J, Simcha I, Albanese C, D'Amico M, Pestell R, Ben-Ze'ev A. 1999. The cyclin D1 gene is a target of the β-catenin/LEF-1 pathway. Proc Natl Acad Sci USA 96:5522-5527.
63. Si W, Kang Q, Luu HH, Park JK, Luo Q, Song WX, Jiang W, Luo X, Li X, Yin H, Montag AG, Haydon RC, He TC. 2006. CCN1/Cyr61 is regulated by the canonical Wnt signal and plays an important role in Wnt3A-induced osteoblast differentiation of mesenchymal stem cells. Mol Cell Biol 26:2955-2964.
64. Silva AJ, Kogan JH, Frankland PW, Kida S. 1998. CREB and memory. Annu Rev Neurosci 21:127-148.
65. Soderling TR, Stull JT. 2001. Structure and regulation of calcium/calmodulin-dependent protein kinases. Chem Rev 101:2341-2351.
66. Soutoglou E, Talianidis L. 2002. Coordination of PIC assembly and chromatin remodeling during differentiation-induced gene activation. Science 295:1901-1904.
67. Tetsu O, McCormick F. 1999. β-catenin regulates expression of cyclin D1 in colon carcinoma cells. Nature 398:422-426.
68. Toledo EM, Inestrosa NC. 2009. Activation of Wnt signaling by Lithium and Rosiglitazone reduced spatial memory impairment and neurodegeneration in brains of APPswe/ PSEN1ΔE9 mouse model of Alzheimer's disease. Mol Psychiatry Epub ahead of print, DOI: 10.1038/mp.2009.72.
69. Toledo EM, Colombres M, Inestrosa NC. 2008. Wnt signaling in neuroprotection and stem cell differentiation. Prog Neurobiol 86:281-296.
70. van der Heyden MA, Rook MB, Hermans MM, Rijksen G, Boonstra J, Defize LH, Destree OH. 1998. Identification of connexin43 as a functional target for Wnt signaling. J Cell Sci 111:1741-1749.
71. Villagra A, Cruzat F, Carvallo L, Paredes R, Olate J, van Wijnen AJ, Stein GS, Lian J, Stein J, Imbalzano AN, Montecino M. 2006. Chromatin remodeling and transcriptional activity of the bone-specific osteocalcin gene require CCAAT/enhancer-binding protein β-dependent recruitment of SWI/SNF activity. J Biol Chem 281:22695-22706.
72. Willert J, Epping M, Pollack JR, Brown PO, Nusse R. 2002. A transcriptional response to Wnt protein in human embryonic carcinoma cells. BMC Dev Biol 2:8.
73. Wu GY, Deisseroth K, Tsein RW. 2001. Activity-dependent CREB phosphorylation: Convergence of a fast, sensitive calmodulin kinase pathway and slow, less sensitive mitogen-activated protein kinase pathway. Proc Natl Acad Sci USA 98:2808-2813.
74. Zhang Z, Hartmann H, Do VM, Abramowski D, Sturchler-Pierrat C, Staufenbiel M, Sommer B, van de Wetering M, Clevers H, Saftig P, De Strooper B, He X, Yankner BA. 1998. Destabilization of β-catenin by mutations in presenilin-1 potentiates neuronal apoptosis. Nature 395:698-702. (Pubitemid 28475966)
75. Zhou C, Liu S, Zhou X, Xue L, Quan L, Lu N, Zhang G, Bai J, Wang Y, Liu Z, Zhan Q, Zhu H, Xu N. 2005. Overexpression of human pituitary tumor transforming gene (hPTTG), is regulated by β-catenin/TCF pathway in human esophageal squamous cell carcinoma. Int J Cancer 113:891-898. (Pubitemid 40096868)