Transcription factor sp4 regulates expression of nervous wreck 2 to control NMDAR1 levels and dendrite patterning

Developmental Neurobiology

Volumn 75, Issue 1, 2015, Pages 93-108

  Sun, Xinxin ^a   Pinacho, Raquel ^b   Saia, Gregory ^a   Punko, Diana ^a   Meana, J Javier ^c   Ramos, Belén ^b   Gill, Grace ^a  

^a TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF BARCELONA   (Spain)

^c UNIVERSITY OF THE BASQUE COUNTRY UPV EHU   (Spain)

Author keywords

Bipolar disorder; F BAR domain; NMDAR; Trafficking; Transcription factor

Indexed keywords

N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NERVOUS WRECK 2 PROTEIN; PROTEIN; TRANSCRIPTION FACTOR SP4; UNCLASSIFIED DRUG; CARRIER PROTEIN; FCHSD1 PROTEIN, HUMAN; MEMBRANE PROTEIN; NMDA RECEPTOR A1;

ADULT; AGED; ANIMAL EXPERIMENT; ARTICLE; BIPOLAR DISORDER; CELL SURFACE; CEREBELLUM; CLINICAL ARTICLE; CONTROLLED STUDY; DENDRITE; FEMALE; GENE CONTROL; GENE SILENCING; HUMAN; MALE; MIDDLE AGED; MORPHOGENESIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN DEPLETION; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; ANIMAL; CYTOLOGY; METABOLISM; PHYSIOLOGY;

ADULT; AGED; ANIMALS; BIPOLAR DISORDER; CARRIER PROTEINS; CEREBELLUM; DENDRITES; FEMALE; HUMANS; MALE; MEMBRANE PROTEINS; MICE; MIDDLE AGED; MORPHOGENESIS; RECEPTORS, N-METHYL-D-ASPARTATE; SIGNAL TRANSDUCTION; SP4 TRANSCRIPTION FACTOR;

EID: 84919345926     PISSN: 19328451     EISSN: 1932846X     Source Type: Journal    
DOI: 10.1002/dneu.22212     Document Type: Article

References (65)

1. Aspenstrom P, Fransson A, Richnau N. 2006. Pombe Cdc15 homology proteins: Regulators of membrane dynamics and the actin cytoskeleton. Trends Biochem Sci 31:670-679.
2. Balazs R, Jorgensen OS, Hack N. 1988. N-methyl-D-aspartate promotes the survival of cerebellar granule cells in culture. Neuroscience 27:437-451.
3. Becalska AN, Kelley CF, Berciu C, Stanishneva-Konovalova TB, Fu X, Wang S, Sokolova OS, et al. 2013. Formation of membrane ridges and scallops by the F-BAR protein Nervous Wreck. Mol Biol Cell 24:2406-2418.
4. Beneyto M, Kristiansen LV, Oni-Orisan A, McCullumsmith RE, Meador-Woodruff JH. 2007. Abnormal glutamate receptor expression in the medial temporal lobe in schizophrenia and mood disorders. Neuropsychopharmacology 32:1888-1902.
5. Bilimoria PM, Bonni A. 2008. Cultures of cerebellar granule neurons. CSH Protoc 2008:pdb prot5107.
6. Black AR, Black JD, Azizkhan-Clifford J. 2001. Sp1 and kruppel-like factor family of transcription factors in cell growth regulation and cancer. J Cell Physiol 188:143-160.
7. Bolbecker AR, Mehta C, Johannesen JK, Edwards CR, O'Donnell BF, Shekhar A, Nurnberger JI, et al. 2009. Eyeblink conditioning anomalies in bipolar disorder suggest cerebellar dysfunction. Bipolar Disorders 11:19-32.
8. Cao H, Yin X, Cao Y, Jin Y, Wang S, Kong Y, Chen Y, et al. 2013. FCHSD1 and FCHSD2 are expressed in hair cell stereocilia and cuticular plate and regulate actin polymerization in vitro. Plos One 8:e56516.
9. Carlson BR, Lloyd KE, Kruszewski A, Kim IH, Rodriguiz RM, Heindel C, Faytell M, et al. 2011. WRP/srGAP3 facilitates the initiation of spine development by an inverse F-BAR domain, and its loss impairs long-term memory. J Neurosci 31:2447-2460.
10. Carlson GC. 2012. Glutamate receptor dysfunction and drug targets across models of autism spectrum disorders. Pharmacol Biochem Behav 100:850-854.
11. Cline HT. 2001. Dendritic arbor development and synaptogenesis. Curr Opin Neurobiol 11:118-126.
12. Coyle IP, Koh YH, Lee WC, Slind J, Fergestad T, Littleton JT, Ganetzky B. 2004. Nervous wreck, an SH3 adaptor protein that interacts with Wsp, regulates synaptic growth in Drosophila. Neuron 41:521-534.
13. Datwani A, Iwasato T, Itohara S, Erzurumlu RS. 2002. NMDA receptor-dependent pattern transfer from afferents to postsynaptic cells and dendritic differentiation in the barrel cortex. Mol Cellular Neurosci 21:477-492.
14. Dharmalingam E, Haeckel A, Pinyol R, Schwintzer L, Koch D, Kessels MM, Qualmann B. 2009. F-BAR proteins of the syndapin family shape the plasma membrane and are crucial for neuromorphogenesis. J Neurosci 29:13315-13327.
15. Edgar R, Domrachev M, Lash AE. 2002. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 30:207-210.
16. Espinosa JS, Wheeler DG, Tsien RW, Luo L. 2009. Uncoupling dendrite growth and patterning: Single-cell knockout analysis of NMDA receptor 2B. Neuron 62:205-217.
17. Fountoulakis KN. 2012. The possible involvement of NMDA glutamate receptor in the etiopathogenesis of bipolar disorder. Curr Pharm Des 18:1605-1608.
18. Fuste M, Pinacho R, Melendez-Perez I, Villalmanzo N, Villalta-Gil V, Haro JM, Ramos B. 2013. Reduced expression of SP1 and SP4 transcription factors in peripheral blood mononuclear cells in first-episode psychosis. J Psychiatr Res 47:1608-1614.
19. Geddes AE, Huang XF, Newell KA. 2011. Reciprocal signalling between NR2 subunits of the NMDA receptor and neuregulin1 and their role in schizophrenia. Prog Neuropsychopharmacol Biol Psychiatry 35:896-904.
20. Ginsberg SD, Hemby SE, Smiley JF. 2012. Expression profiling in neuropsychiatric disorders: Emphasis on glutamate receptors in bipolar disorder. Pharmacol Biochem Behav 100:705-711.
21. Guerrier S, Coutinho-Budd J, Sassa T, Gresset A, Jordan NV, Chen K, Jin WL, et al. 2009. The F-BAR domain of srGAP2 induces membrane protrusions required for neuronal migration and morphogenesis. Cell 138:990-1004.
22. Itoh T, Erdmann KS, Roux A, Habermann B, Werner H, De Camilli P. 2005. Dynamin and the actin cytoskeleton cooperatively regulate plasma membrane invagination by BAR and F-BAR proteins. Dev Cell 9:791-804.
23. Jeans A, Malins R, Padamsey Z, Reinhart M, Emptage N. 2011. Increased expression of dysbindin-1A leads to a selective deficit in NMDA receptor signaling in the hippocampus. Neuropharmacology 61:1345-1353.
24. Ji B, Wang X, Pinto-Duarte A, Kim M, Caldwell S, Young JW, Behrens MM, et al. 2013. Prolonged ketamine effects in Sp4 hypomorphic mice: Mimicking phenotypes of schizophrenia. Plos One 8:(6)e66327.
25. Kelsoe J, Zhou XJ, Guo SZ, Shehktman T, He L, Geyer M. 2006. SP4 gene conveys susceptibility to bipolar disorder and schizophrenia. Am J Med Genet Part B: Neuropsychiatr Genet 141B:713-713.
26. Komuro H, Rakic P. 1993. Modulation of neuronal migration by NMDA receptors. Science 260:95-97.
27. Konarski JZ, McIntyre RS, Grupp LA, Kennedy SH. 2005. Is the cerebellum relevant in the circuitry of neuropsychiatric disorders? J Psychiatry Neurosci 30:178-186.
28. Krystal JH, Karper LP, Seibyl JP, Freeman GK, Delaney R, Bremner JD, Heninger GR, et al. 1994. Subanesthetic effects of the noncompetitive NMDA antagonist, ketamine, in humans-Psychotomimetic, perceptual, cognitive, and neuroendocrine responses. Arch Gen Psychiatry 51:199-214.
29. Lau CG, Zukin RS. 2007. NMDA receptor trafficking in synaptic plasticity and neuropsychiatric disorders. Nat Rev Neurosci 8:413-426.
30. Liu A, Hoffman PW, Lu W, Bai G. 2004. NF-kappaB site interacts with Sp factors and up-regulates the NR1 promoter during neuronal differentiation. J Biol Chem 279:17449-17458.
31. Liu A, Zhuang Z, Hoffman PW, Bai G. 2003. Functional analysis of the rat N-methyl-D-aspartate receptor 2A promoter: Multiple transcription starts points, positive regulation by Sp factors, and translational regulation. J Biol Chem 278:26423-26434.
32. Luscher C, Malenka RC. 2012. NMDA receptor-dependent long-term potentiation and long-term depression (LTP/LTD). Cold Spring Harb Perspect Biol 4:pii:a005710.
33. Mao X, Yang SH, Simpkins JW, Barger SW. 2007. Glutamate receptor activation evokes calpain-mediated degradation of Sp3 and Sp4, the prominent Sp-family transcription factors in neurons. J Neurochem 100:1300-1314.
34. Moghaddam B, Javitt D. 2012. From revolution to evolution: The glutamate hypothesis of schizophrenia and its implication for treatment. Neuropsychopharmacology 37:4-15.
35. Nudmamud-Thanoi S, Reynolds GP. 2004. The NR1 subunit of the glutamate/NMDA receptor in the superior temporal cortex in schizophrenia and affective disorders. Neurosci Lett 372:173-177.
36. O'Connor-Giles KM, Ho LL, Ganetzky B. 2008. Nervous wreck interacts with thickveins and the endocytic machinery to attenuate retrograde BMP signaling during synaptic growth. Neuron 58:507-518.
37. Okamoto S, Sherman K, Bai G, Lipton SA. 2002. Effect of the ubiquitous transcription factors, SP1 and MAZ, on NMDA receptor subunit type 1 (NR1) expression during neuronal differentiation. Brain Res Mol Brain Res 107:89-96.
38. Olney JW, Newcomer JW, Farber NB. 1999. NMDA receptor hypofunction model of schizophrenia. J Psychiatr Res 33:523-533.
39. Paoletti P, Bellone C, Zhou Q. 2013. NMDA receptor subunit diversity: Impact on receptor properties, synaptic plasticity and disease. Nat Rev Neurosci 14:383-400.
40. Pearce IA, Cambray-Deakin MA, Burgoyne RD. 1987. Glutamate acting on NMDA receptors stimulates neurite outgrowth from cerebellar granule cells. FEBS Lett 223:143-147.
41. Perez-Otano I, Ehlers MD. 2005. Homeostatic plasticity and NMDA receptor trafficking. Trends Neurosci 28:229-238.
42. Perez-Otano I, Lujan R, Tavalin SJ, Plomann M, Modregger J, Liu XB, Jones EG, et al. 2006. Endocytosis and synaptic removal of NR3A-containing NMDA receptors by PACSIN1/syndapin1. Nat Neurosci 9:611-621.
43. Pinacho R, Villalmanzo N, Lalonde J, Haro JM, Meana JJ, Gill G, Ramos B. 2011. The transcription factor SP4 is reduced in postmortem cerebellum of bipolar disorder subjects: Control by depolarization and lithium. Bipolar Disord 13:474-485.
44. Pinacho R, Villalmanzo N, Roca M, Iniesta R, Monje A, Haro JM, Meana JJ, et al. 2013. Analysis of Sp transcription factors in the postmortem brain of chronic schizophrenia: A pilot study of relationship to negative symptoms. J Psychiatr Res 47:926-934.
45. Priya A, Johar K, Wong-Riley MT. 2013. Specificity protein 4 functionally regulates the transcription of NMDA receptor subunits GluN1, GluN2A, and GluN2B. Biochim Biophys Acta 1833:2745-2756.
46. Rajan I, Cline HT. 1998. Glutamate receptor activity is required for normal development of tectal cell dendrites in vivo. J Neurosci 18:7836-7846.
47. Ramos B, Gaudilliere B, Bonni A, Gill G. 2007. Transcription factor Sp4 regulates dendritic patterning during cerebellar maturation. Proc Natl Acad Sci USA 104:9882-9887.
48. Ramos B, Valin A, Sun XX, Gill G. 2009. Sp4-dependent repression of neurotrophin-3 limits dendritic branching. Mol Cell Neurosci 42:152-159.
49. Rodal AA, Blunk AD, Akbergenova Y, Jorquera RA, Buhl LK, Littleton JT. 2011. A presynaptic endosomal trafficking pathway controls synaptic growth signaling. J Cell Biol 193:201-217.
50. Rodal AA, Motola-Barnes RN, Littleton JT. 2008. Nervous wreck and Cdc42 cooperate to regulate endocytic actin assembly during synaptic growth. J Neurosci 28:8316-8325.
51. Ryder PV, Faundez V. 2009. Schizophrenia: The "BLOC" may be in the endosomes. Sci Signal 2:pe66.
52. Saengsawang W, Mitok K, Viesselmann C, Pietila L, Lumbard DC, Corey SJ, Dent EW. 2012. The F-BAR protein CIP4 inhibits neurite formation by producing lamellipodial protrusions. Curr Biol 22:494-501.
53. Saia G, Lalonde J, Sun X, Ramos B, Gill G. 2014. Phosphorylation of the transcription factor Sp4 is reduced by NMDA receptor signaling. J Neurochem 129:743-752.
54. Schmahmann JD, Weilburg JB, Sherman JC. 2007. The neuropsychiatry of the cerebellum-Insights from the clinic. Cerebellum 6:254-267.
55. Schubert KO, Focking M, Prehn JH, Cotter DR. 2011. Hypothesis review: Are clathrin-mediated endocytosis and clathrin-dependent membrane and protein trafficking core pathophysiological processes in schizophrenia and bipolar disorder? Mol Psychiatry 17:669-681.
56. Sin WC, Haas K, Ruthazer ES, Cline HT. 2002. Dendrite growth increased by visual activity requires NMDA receptor and Rho GTPases. Nature 419:475-480.
57. St Amand TR, Lu JT, Zamora M, Gu Y, Stricker J, Hoshijima M, Epstein JA, et al. 2006. Distinct roles of HF-1b/Sp4 in ventricular and neural crest cells lineages affect cardiac conduction system development. Dev Biol 291:208-217.
58. Stewart SA, Dykxhoorn DM, Palliser D, Mizuno H, Yu EY, An DS, Sabatini DM, et al. 2003. Lentivirus-delivered stable gene silencing by RNAi in primary cells. RNA 9:493-501.
59. Tam GW, van de Lagemaat LN, Redon R, Strathdee KE, Croning MD, Malloy MP, Muir WJ, et al. 2010. Confirmed rare copy number variants implicate novel genes in schizophrenia. Biochem Soc Trans 38:445-451.
60. Wakita Y, Kakimoto T, Katoh H, Negishi M. 2011. The F-BAR protein Rapostlin regulates dendritic spine formation in hippocampal neurons. J Biol Chem 286:32672-32683.
61. Yeganeh-Doost P, Gruber O, Falkai P, Schmitt A. 2011. The role of the cerebellum in schizophrenia: From cognition to molecular pathways. Clinics (Sao Paulo) 66 Suppl 1:71-77.
62. Zhou X, Long JM, Geyer MA, Masliah E, Kelsoe JR, Wynshaw-Boris A, Chien KR. 2005. Reduced expression of the Sp4 gene in mice causes deficits in sensorimotor gating and memory associated with hippocampal vacuolization. Mol Psychiatry 10:393-406.
63. Zhou X, Nie ZG, Roberts A, Zhang DX, Sebat J, Malhotra D, Kelsoe JR, et al. 2010. Reduced NMDAR1 expression in the Sp4 hypomorphic mouse may contribute to endophenotypes of human psychiatric disorders. Hum Mol Genet 19:3797-3805.
64. Zhou X, Qyang Y, Kelsoe JR, Masliah E, Geyer MA. 2007. Impaired postnatal development of hippocampal dentate gyrus in Sp4 null mutant mice. Genes Brain Behav 6:269-276.
65. Zhou X, Tang W, Greenwood TA, Guo SZ, He L, Geyer MA, Kelsoe JR. 2009. Transcription factor SP4 is a susceptibility gene for bipolar disorder. Plos One 4:e5196.