Altered regulation of the Spry2/Dyrk1A/PP2A triad by homocysteine impairs neural progenitor cell proliferation

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1863, Issue 12, 2016, Pages 3015-3026

  Rabaneda, Luis G ^a,b   Geribaldi Doldán, Noelia ^a   Murillo Carretero, Maribel ^a   Carrasco, Manuel ^a   Martínez Salas, José M ^a   Verástegui, Cristina ^a   Castro, Carmen ^a  

^a UNIVERSITY OF CÁDIZ   (Spain)

^b UNIVERSITY OF NAVARRA   (Spain)

Author keywords

Dyrk1A; homocysteine; neural progenitor cells; neurogenesis; PP2A; Spry2

Indexed keywords

DYRK1A PROTEIN; FIBROBLAST GROWTH FACTOR RECEPTOR; HOMOCYSTEINE; MESSENGER RNA; METHYLTRANSFERASE; PHOSPHOPROTEIN PHOSPHATASE 2A; PROTEIN KINASE; SPROUTY PROTEIN; SPRY2 PROTEIN; UNCLASSIFIED DRUG; CYCLIN E; DYRK KINASE; MAPK1 PROTEIN, MOUSE; MEMBRANE PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PHOSPHOPROTEIN PHOSPHATASE 2; PROTEIN SERINE THREONINE KINASE; PROTEIN TYROSINE KINASE; SIGNAL PEPTIDE; SPRY2 PROTEIN, MOUSE;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIPROLIFERATIVE ACTIVITY; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; DEMETHYLATION; DNA METHYLATION; DOWN REGULATION; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INACTIVATION; ENZYME PHOSPHORYLATION; GENE EXPRESSION; HYPERHOMOCYSTEINEMIA; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NEURAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN STABILITY; UPREGULATION; ANIMAL; CYTOLOGY; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MULTICELLULAR SPHEROID; NERVOUS SYSTEM DEVELOPMENT; PHOSPHORYLATION; SIGNAL TRANSDUCTION;

ANIMALS; CELL PROLIFERATION; CYCLIN E; DNA METHYLATION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOMOCYSTEINE; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE PROTEINS; MICE; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; NEURAL STEM CELLS; NEUROGENESIS; PHOSPHORYLATION; PROMOTER REGIONS, GENETIC; PROTEIN PHOSPHATASE 2; PROTEIN STABILITY; PROTEIN-SERINE-THREONINE KINASES; PROTEIN-TYROSINE KINASES; RECEPTORS, FIBROBLAST GROWTH FACTOR; RNA, MESSENGER; SIGNAL TRANSDUCTION; SPHEROIDS, CELLULAR;

EID: 84989237146     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2016.09.018     Document Type: Article

References (50)

1. [1] Refsum, H., Ueland, P.M., Nygard, O., Vollset, S.E., Homocysteine and cardiovascular disease. Annu. Rev. Med. 49 (1998), 31–62.
2. [2] Seshadri, S., Beiser, A., Selhub, J., Jacques, P.F., Rosenberg, I.H., D'Agostino, R.B., Wilson, P.W., Wolf, P.A., Plasma homocysteine as a risk factor for dementia and Alzheimer's disease. N. Engl. J. Med. 346 (2002), 476–483.
3. [3] Ravaglia, G., Forti, P., Maioli, F., Chiappelli, M., Montesi, F., Tumini, E., Mariani, E., Licastro, F., Patterson, C., Blood inflammatory markers and risk of dementia: The Conselice Study of Brain Aging. Neurobiol. Aging, 2006.
4. [4] Haan, M.N., Miller, J.W., Aiello, A.E., Whitmer, R.A., Jagust, W.J., Mungas, D.M., Allen, L.H., Green, R., Homocysteine, B vitamins, and the incidence of dementia and cognitive impairment: results from the Sacramento Area Latino Study on Aging. Am. J. Clin. Nutr. 85 (2007), 511–517.
5. [5] Lerner, V., Miodownik, C., Kaptsan, A., Vishne, T., Sela, B.A., Levine, J., High serum homocysteine levels in young male schizophrenic and schizoaffective patients with tardive parkinsonism and/or tardive dyskinesia. J. Clin. Psychiatry 66 (2005), 1558–1563.
6. [6] Rabaneda, L.G., Carrasco, M., Lopez-Toledano, M.A., Murillo-Carretero, M., Ruiz, F.A., Estrada, C., Castro, C., Homocysteine inhibits proliferation of neuronal precursors in the mouse adult brain by impairing the basic fibroblast growth factor signaling cascade and reducing extracellular regulated kinase 1/2-dependent cyclin E expression. FASEB J. 22 (2008), 3823–3835.
7. [7] Lugert, S., Basak, O., Knuckles, P., Haussler, U., Fabel, K., Gotz, M., Haas, C.A., Kempermann, G., Taylor, V., Giachino, C., Quiescent and active hippocampal neural stem cells with distinct morphologies respond selectively to physiological and pathological stimuli and aging. Cell Stem Cell 6 (2010), 445–456.
8. [8] Fuentealba, L.C., Obernier, K., Alvarez-Buylla, A., Adult neural stem cells bridge their niche. Cell Stem Cell 10 (2012), 698–708.
9. [9] Ming, G.L., Song, H., Adult neurogenesis in the mammalian brain: significant answers and significant questions. Neuron 70 (2011), 687–702.
10. [10] Goldman, S., Glia as neural progenitor cells. Trends Neurosci. 26 (2003), 590–596.
11. [11] Alvarez-Buylla, A., Garcia-Verdugo, J.M., Neurogenesis in adult subventricular zone. J. Neurosci. 22 (2002), 629–634.
12. [12] Palmer, T.D., Ray, J., Gage, F.H., FGF-2-responsive neuronal progenitors reside in proliferative and quiescent regions of the adult rodent brain. Mol. Cell. Neurosci. 6 (1995), 474–486.
13. [13] Jin, K., Sun, Y., Xie, L., Batteur, S., Mao, X.O., Smelick, C., Logvinova, A., Greenberg, D.A., Neurogenesis and aging: FGF-2 and HB-EGF restore neurogenesis in hippocampus and subventricular zone of aged mice. Aging Cell 2 (2003), 175–183.
14. [14] Bull, N.D., Bartlett, P.F., The adult mouse hippocampal progenitor is neurogenic but not a stem cell. J. Neurosci. 25 (2005), 10815–10821.
15. [15] Carrasco, M., Rabaneda, L.G., Murillo-Carretero, M., Ortega-Martinez, S., Martinez-Chantar, M.L., Woodhoo, A., Luka, Z., Wagner, C., Lu, S.C., Mato, J.M., Mico, J.A., Castro, C., Glycine N-methyltransferase expression in the hippocampus and its role in neurogenesis and cognitive performance. Hippocampus 24 (2014), 840–852.
16. [16] Hanafusa, H., Torii, S., Yasunaga, T., Nishida, E., Sprouty1 and Sprouty2 provide a control mechanism for the Ras/MAPK signalling pathway. Nat. Cell Biol. 4 (2002), 850–858.
17. [17] Yim, D.G., Ghosh, S., Guy, G.R., Virshup, D.M., Casein kinase 1 regulates Sprouty2 in FGF-ERK signaling. Oncogene 34 (2015), 474–484.
18. [18] DaSilva, J., Xu, L., Kim, H.J., Miller, W.T., Bar-Sagi, D., Regulation of sprouty stability by Mnk1-dependent phosphorylation. Mol. Cell. Biol. 26 (2006), 1898–1907.
19. [19] Chandramouli, S., Yu, C.Y., Yusoff, P., Lao, D.H., Leong, H.F., Mizuno, K., Guy, G.R., Tesk1 interacts with Spry2 to abrogate its inhibition of ERK phosphorylation downstream of receptor tyrosine kinase signaling. J. Biol. Chem. 283 (2008), 1679–1691.
20. [20] Aranda, S., Alvarez, M., Turro, S., Laguna, A., de la Luna, S., Sprouty2-mediated inhibition of fibroblast growth factor signaling is modulated by the protein kinase DYRK1A. Mol. Cell. Biol. 28 (2008), 5899–5911.
21. [21] Lao, D.H., Yusoff, P., Chandramouli, S., Philp, R.J., Fong, C.W., Jackson, R.A., Saw, T.Y., Yu, C.Y., Guy, G.R., Direct binding of PP2A to Sprouty2 and phosphorylation changes are a prerequisite for ERK inhibition downstream of fibroblast growth factor receptor stimulation. J. Biol. Chem. 282 (2007), 9117–9126.
22. [22] Mason, J.M., Morrison, D.J., Basson, M.A., Licht, J.D., Sprouty proteins: multifaceted negative-feedback regulators of receptor tyrosine kinase signaling. Trends Cell Biol. 16 (2006), 45–54.
23. [23] Mayer, C.E., Haigl, B., Jantscher, F., Siegwart, G., Grusch, M., Berger, W., Sutterluty, H., Bimodal expression of Sprouty2 during the cell cycle is mediated by phase-specific Ras/MAPK and c-Cbl activities. Cell. Mol. Life Sci. 67 (2010), 3299–3311.
24. [24] McKie, A.B., Douglas, D.A., Olijslagers, S., Graham, J., Omar, M.M., Heer, R., Gnanapragasam, V.J., Robson, C.N., Leung, H.Y., Epigenetic inactivation of the human sprouty2 (hSPRY2) homologue in prostate cancer. Oncogene 24 (2005), 2166–2174.
25. [25] Lo, T.L., Yusoff, P., Fong, C.W., Guo, K., McCaw, B.J., Phillips, W.A., Yang, H., Wong, E.S., Leong, H.F., Zeng, Q., Putti, T.C., Guy, G.R., The ras/mitogen-activated protein kinase pathway inhibitor and likely tumor suppressor proteins, sprouty 1 and sprouty 2 are deregulated in breast cancer. Cancer Res. 64 (2004), 6127–6136.
26. [26] Fong, C.W., Chua, M.S., McKie, A.B., Ling, S.H., Mason, V., Li, R., Yusoff, P., Lo, T.L., Leung, H.Y., So, S.K., Guy, G.R., Sprouty 2, an inhibitor of mitogen-activated protein kinase signaling, is down-regulated in hepatocellular carcinoma. Cancer Res. 66 (2006), 2048–2058.
27. [27] Hattori, M., Fujiyama, A., Taylor, T.D., Watanabe, H., Yada, T., Park, H.S., Toyoda, A., Ishii, K., Totoki, Y., Choi, D.K., Groner, Y., Soeda, E., Ohki, M., Takagi, T., Sakaki, Y., Taudien, S., Blechschmidt, K., Polley, A., Menzel, U., Delabar, J., Kumpf, K., Lehmann, R., Patterson, D., Reichwald, K., Rump, A., Schillhabel, M., Schudy, A., Zimmermann, W., Rosenthal, A., Kudoh, J., Schibuya, K., Kawasaki, K., Asakawa, S., Shintani, A., Sasaki, T., Nagamine, K., Mitsuyama, S., Antonarakis, S.E., Minoshima, S., Shimizu, N., Nordsiek, G., Hornischer, K., Brant, P., Scharfe, M., Schon, O., Desario, A., Reichelt, J., Kauer, G., Blocker, H., Ramser, J., Beck, A., Klages, S., Hennig, S., Riesselmann, L., Dagand, E., Haaf, T., Wehrmeyer, S., Borzym, K., Gardiner, K., Nizetic, D., Francis, F., Lehrach, H., Reinhardt, R., Yaspo, M.L., m. Chromosome, c. sequencing, The DNA sequence of human chromosome 21. Nature 405 (2000), 311–319.
28. [28] Guedj, F., Pereira, P.L., Najas, S., Barallobre, M.J., Chabert, C., Souchet, B., Sebrie, C., Verney, C., Herault, Y., Arbones, M., Delabar, J.M., DYRK1A: a master regulatory protein controlling brain growth. Neurobiol. Dis. 46 (2012), 190–203.
29. [29] Souchet, B., Guedj, F., Sahun, I., Duchon, A., Daubigney, F., Badel, A., Yanagawa, Y., Barallobre, M.J., Dierssen, M., Yu, E., Herault, Y., Arbones, M., Janel, N., Creau, N., Delabar, J.M., Excitation/inhibition balance and learning are modified by Dyrk1a gene dosage. Neurobiol. Dis. 69 (2014), 65–75.
30. [30] Thomazeau, A., Lassalle, O., Iafrati, J., Souchet, B., Guedj, F., Janel, N., Chavis, P., Delabar, J., Manzoni, O.J., Prefrontal deficits in a murine model overexpressing the down syndrome candidate gene dyrk1a. J. Neurosci. 34 (2014), 1138–1147.
31. [31] Najas, S., Arranz, J., Lochhead, P.A., Ashford, A.L., Oxley, D., Delabar, J.M., Cook, S.J., Barallobre, M.J., Arbones, M.L., DYRK1A-mediated Cyclin D1 Degradation in Neural Stem Cells Contributes to the Neurogenic Cortical Defects in Down Syndrome. EBioMedicine 2 (2015), 120–134.
32. [32] Abekhoukh, S., Planque, C., Ripoll, C., Urbaniak, P., Paul, J.L., Delabar, J.M., Janel, N., Dyrk1A, a serine/threonine kinase, is involved in ERK and Akt activation in the brain of hyperhomocysteinemic mice. Mol. Neurobiol. 47 (2013), 105–116.
33. [33] Finkelstein, J.D., Kyle, W.E., Harris, B.J., Methionine metabolism in mammals: regulatory effects of S-adenosylhomocysteine. Arch. Biochem. Biophys. 165 (1974), 774–779.
34. [34] Garrow, T.A., Purification, kinetic properties, and cDNA cloning of mammalian betaine-homocysteine methyltransferase. J. Biol. Chem. 271 (1996), 22831–22838.
35. [35] Torroglosa, A., Murillo-Carretero, M., Romero-Grimaldi, C., Matarredona, E.R., Campos-Caro, A., Estrada, C., Nitric oxide decreases subventricular zone stem cell proliferation by inhibition of epidermal growth factor receptor and phosphoinositide-3-kinase/Akt pathway. Stem Cells 25 (2007), 88–97.
36. [36] Winer, J., Jung, C.K., Shackel, I., Williams, P.M., Development and validation of real-time quantitative reverse transcriptase-polymerase chain reaction for monitoring gene expression in cardiac myocytes in vitro. Anal. Biochem. 270 (1999), 41–49.
37. [37] Guy, G.R., Jackson, R.A., Yusoff, P., Chow, S.Y., Sprouty proteins: modified modulators, matchmakers or missing links?. J. Endocrinol. 203 (2009), 191–202.
38. [38] Gockler, N., Jofre, G., Papadopoulos, C., Soppa, U., Tejedor, F.J., Becker, W., Harmine specifically inhibits protein kinase DYRK1A and interferes with neurite formation. FEBS J. 276 (2009), 6324–6337.
39. [39] Casci, T., Vinos, J., Freeman, M., Sprouty, an intracellular inhibitor of Ras signaling. Cell 96 (1999), 655–665.
40. [40] Pilz, R.B., Van den Berghe, G., Boss, G.R., Adenosine dialdehyde and nitrous oxide induce HL-60 differentiation. Blood 70 (1987), 1161–1164.
41. [41] Johnson, B.A., Najbauer, J., Aswad, D.W., Accumulation of substrates for protein L-isoaspartyl methyltransferase in adenosine dialdehyde-treated PC12 cells. J. Biol. Chem. 268 (1993), 6174–6181.
42. [42] Cantoni, G.L., Biological methylation: selected aspects. Annu. Rev. Biochem. 44 (1975), 435–451.
43. [43] Hamelet, J., Noll, C., Ripoll, C., Paul, J.L., Janel, N., Delabar, J.M., Effect of hyperhomocysteinemia on the protein kinase DYRK1A in liver of mice. Biochem. Biophys. Res. Commun. 378 (2009), 673–677.
44. [44] Sutterluty, H., Mayer, C.E., Setinek, U., Attems, J., Ovtcharov, S., Mikula, M., Mikulits, W., Micksche, M., Berger, W., Down-regulation of Sprouty2 in non-small cell lung cancer contributes to tumor malignancy via extracellular signal-regulated kinase pathway-dependent and -independent mechanisms. Mol. Cancer Res. 5 (2007), 509–520.
45. [45] Sanui, T., Tanaka, U., Fukuda, T., Toyoda, K., Taketomi, T., Atomura, R., Yamamichi, K., Nishimura, F., Mutation of Spry2 induces proliferation and differentiation of osteoblasts but inhibits proliferation of gingival epithelial cells. J. Cell. Biochem. 116 (2015), 628–639.
46. [46] Ferron, S.R., Pozo, N., Laguna, A., Aranda, S., Porlan, E., Moreno, M., Fillat, C., de la Luna, S., Sanchez, P., Arbones, M.L., Farinas, I., Regulated segregation of kinase Dyrk1A during asymmetric neural stem cell division is critical for EGFR-mediated biased signaling. Cell Stem Cell 7 (2010), 367–379.
47. [47] Zhao, X., Ueba, T., Christie, B.R., Barkho, B., McConnell, M.J., Nakashima, K., Lein, E.S., Eadie, B.D., Willhoite, A.R., Muotri, A.R., Summers, R.G., Chun, J., Lee, K.F., Gage, F.H., Mice lacking methyl-CpG binding protein 1 have deficits in adult neurogenesis and hippocampal function. Proc. Natl. Acad. Sci. U. S. A. 100 (2003), 6777–6782.
48. [48] Ma, D.K., Jang, M.H., Guo, J.U., Kitabatake, Y., Chang, M.L., Pow-Anpongkul, N., Flavell, R.A., Lu, B., Ming, G.L., Song, H., Neuronal activity-induced Gadd45b promotes epigenetic DNA demethylation and adult neurogenesis. Science 323 (2009), 1074–1077.
49. [49] Fernandez-Sanchez, M.E., Gonatopoulos-Pournatzis, T., Preston, G., Lawlor, M.A., Cowling, V.H., S-adenosyl homocysteine hydrolase is required for Myc-induced mRNA cap methylation, protein synthesis, and cell proliferation. Mol. Cell. Biol. 29 (2009), 6182–6191.
50. [50] Wolf, J.J., Dowell, R.D., Mahony, S., Rabani, M., Gifford, D.K., Fink, G.R., Feed-forward regulation of a cell fate determinant by an RNA-binding protein generates asymmetry in yeast. Genetics 185 (2010), 513–522.