Early growth response protein 1 regulates promoter activity of α-plasma membrane calcium ATPase 2, a major calcium pump in the brain and auditory system
Tóm tắt
Along with sodium/calcium (Ca2+) exchangers, plasma membrane Ca2+ ATPases (ATP2Bs) are main regulators of intracellular Ca2+ levels. There are four ATP2B paralogs encoded by four different genes. Atp2b2 encodes the protein pump with the fastest activation, ATP2B2. In mice, the Atp2b2 transcript has several alternate transcriptional start site variants: α, β, µ and δ. These variants are expressed in developmental and tissue specific manners. The α and β Atp2b2 transcripts are equally expressed in the brain. αAtp2b2 is the only transcript found in the outer hair cells of young mice (Silverstein RS, Tempel BL. in Neuroscience 141:245–257, 2006). Mutations in the coding region of the mouse Atp2b2 gene indicate a narrow window for tolerated dysfunction of the ATP2B2 protein, specifically in the auditory system. This highlights the necessity of tight regulation of this gene for normal cell physiology. Although ATP2Bs are important regulators of Ca2+ in many cell types, little is known about their transcriptional regulation. This study identifies the proximal promoter of the αAtp2b2 transcript. Further investigations indicate that ATOH1 and EGR1 modulate promoter activity. Additionally, we report that EGR1 increases endogenous expression of Atp2b2 transcript in two cell lines. Electrophoretic mobility shift assays (EMSA) indicate that EGR1 binds to a specific site in the CpG island of the αAtp2b2 promoter. This study furthers our understanding of Atp2b2 regulation by: (I) elucidating transcriptional regulatory mechanisms for Atp2b2, and (II) identifying transcription factors that modulate expression of Atp2b2 in the brain and peripheral auditory system and (III) allows for future studies modulating gene expression of Atp2b2.
Tài liệu tham khảo
citation_journal_title=Subcell Biochem; citation_title=The plasma membrane calcium ATPase and disease; citation_author=BL Tempel, DJ Shilling; citation_volume=45; citation_publication_date=2007; citation_pages=365-383; citation_doi=10.1007/978-1-4020-6191-2_13; citation_id=CR1
citation_journal_title=Biochem Biophys Res Commun; citation_title=Plasma membrane calcium ATPases: from generic Ca2+ sump pumps to versatile systems for fine-tuning cellular Ca2+
; citation_author=EE Strehler; citation_volume=460; citation_publication_date=2015; citation_pages=26-33; citation_doi=10.1016/j.bbrc.2015.01.121; citation_id=CR2
citation_journal_title=Biochem Biophys Res Commun; citation_title=Phenotypes of SERCA and PMCA knockout mice; citation_author=V Prasad, GW Okunade, ML Miller, GE Shull; citation_volume=322; citation_publication_date=2004; citation_pages=1192-1203; citation_doi=10.1016/j.bbrc.2004.07.156; citation_id=CR3
citation_journal_title=Curr Opin Nephrol Hypertens; citation_title=ATP2B1 and blood pressure: from associations to pathophysiology; citation_author=N Hirawa, A Fujiwara, S Umemura; citation_volume=22; citation_publication_date=2013; citation_pages=177-184; citation_doi=10.1097/MNH.0b013e32835da4ca; citation_id=CR4
citation_journal_title=Brain Behav; citation_title=PMCA4 (ATP2B4) mutation in familial spastic paraplegia causes delay in intracellular calcium extrusion; citation_author=PW-L Ho, SY-Y Pang, M Li, ZH-M Tse, MH-W Kung, P-C Sham, S-L Ho; citation_volume=5; citation_publication_date=2015; citation_pages=1-2; citation_doi=10.1002/brb3.321; citation_id=CR5
citation_journal_title=Nat Genet; citation_title=Mutations in a plasma membrane Ca2+-ATPase gene cause deafness in deafwaddler mice; citation_author=VA Street, JW McKee-Johnson, RC Fonseca, BL Tempel, K Noben-Trauth; citation_volume=19; citation_publication_date=1998; citation_pages=390-394; citation_doi=10.1038/1284; citation_id=CR6
citation_journal_title=Hear Res; citation_title=Effects of PMCA2 mutation on DPOAE amplitudes and latencies in deafwaddler mice; citation_author=D Konrad-Martin, JS Norton, KE Mascher, BL Tempel; citation_volume=151; citation_publication_date=2001; citation_pages=205-220; citation_doi=10.1016/S0378-5955(00)00228-8; citation_id=CR7
citation_journal_title=N Engl J Med; citation_title=Modification of human hearing loss by plasma-membrane calcium pump PMCA2; citation_author=JM Schultz, Y Yang, AJ Caride, AG Filoteo, AR Penheiter, A Lagziel, RJ Morell, SA Mohiddin, L Fananapazir, AC Madeo; citation_volume=352; citation_publication_date=2005; citation_pages=1557-1564; citation_doi=10.1056/NEJMoa043899; citation_id=CR8
citation_journal_title=Proc Natl Acad Sci USA; citation_title=A functional study of plasma-membrane calcium-pump isoform 2 mutants causing digenic deafness; citation_author=R Ficarella, F Leva, M Bortolozzi, S Ortolano, F Donaudy, M Petrillo, S Melchionda, A Lelli, T Domi, L Fedrizzi, D Lim, GE Shull, P Gasparini, M Brini, F Mammano, E Carafoli; citation_volume=104; citation_publication_date=2007; citation_pages=1516-1521; citation_doi=10.1073/pnas.0609775104; citation_id=CR9
citation_journal_title=World J Biol Chem; citation_title=Plasma membrane calcium pumps and their emerging roles in cancer; citation_author=SJ Roberts-Thomson; citation_volume=1; citation_publication_date=2010; citation_pages=248; citation_doi=10.4331/wjbc.v1.i8.248; citation_id=CR10
citation_journal_title=PLoS ONE; citation_title=The evidence for association of ATP2B2 polymorphisms with autism in Chinese Han population; citation_author=W Yang, J Liu, F Zheng, M Jia, L Zhao, T Lu, Y Ruan, J Zhang, W Yue, D Zhang, L Wang; citation_volume=8; citation_publication_date=2013; citation_pages=e61021; citation_doi=10.1371/journal.pone.0061021; citation_id=CR11
citation_journal_title=Hear Res; citation_title=A new Atp2b2 deafwaddler allele, dfwi5, interacts strongly with Cdh23 and other auditory modifiers; citation_author=CJ Watson, BL Tempel; citation_volume=304; citation_publication_date=2013; citation_pages=41-48; citation_doi=10.1016/j.heares.2013.06.003; citation_id=CR12
citation_journal_title=Hear Res; citation_title=Characterization of the deafwaddler mutant of the rat plasma membrane calcium-ATPase 2; citation_author=AR Penheiter, AG Filoteo, CL Croy, JT Penniston; citation_volume=162; citation_publication_date=2001; citation_pages=19-28; citation_doi=10.1016/S0378-5955(01)00356-2; citation_id=CR13
citation_journal_title=Hear Res; citation_title=Haplo-insufficiency revealed in deafwaddler mice when tested for hearing loss and ataxia; citation_author=BJ McCullough, BL Tempel; citation_volume=195; citation_publication_date=2004; citation_pages=90-102; citation_doi=10.1016/j.heares.2004.05.003; citation_id=CR14
citation_journal_title=Arch Biochem Biophys; citation_title=The mouse plasma membrane Ca2+ pump isoform 1 promoter: cloning and characterization; citation_author=Y Du, L Carlock, TH Kuo; citation_volume=316; citation_publication_date=1995; citation_pages=302-310; citation_doi=10.1006/abbi.1995.1041; citation_id=CR15
citation_journal_title=Proc R Soc Lond B Biol Sci; citation_title=Auditory hair cell precursors immortalized from the mammalian inner ear; citation_author=MN Rivolta, N Grix, P Lawlor, JF Ashmore, DJ Jagger, MC Holley; citation_volume=265; citation_publication_date=1998; citation_pages=1595-1603; citation_doi=10.1098/rspb.1998.0477; citation_id=CR16
citation_journal_title=BMC Bioinform; citation_title=MotifMap: integrative genome-wide maps of regulatory motif sites for model species; citation_author=K Daily, VR Patel, P Rigor, X Xie, P Baldi; citation_volume=12; citation_publication_date=2011; citation_pages=495; citation_doi=10.1186/1471-2105-12-495; citation_id=CR17
citation_journal_title=J Biol Chem; citation_title=Detection and characterization of cellular EGR-1 binding to its recognition site; citation_author=X Cao, R Mahendran, GR Guy, YH Tan; citation_volume=268; citation_publication_date=1993; citation_pages=16949-16957; citation_id=CR18
citation_journal_title=Neuroscience; citation_title=Atp2b2, encoding plasma membrane Ca2+-ATPase type 2, (PMCA2) exhibits tissue-specific first exon usage in hair cells, neurons, and mammary glands of mice; citation_author=RS Silverstein, BL Tempel; citation_volume=141; citation_publication_date=2006; citation_pages=245-257; citation_doi=10.1016/j.neuroscience.2006.03.036; citation_id=CR19
citation_journal_title=Nature; citation_title=The accessible chromatin landscape of the human genome; citation_author=RE Thurman, E Rynes, R Humbert, J Vierstra, MT Maurano, E Haugen, NC Sheffield, AB Stergachis, H Wang, B Vernot, K Garg, S John, R Sandstrom, D Bates, L Boatman, TK Canfield, M Diegel, D Dunn, AK Ebersol, T Frum, E Giste, AK Johnson, EM Johnson, T Kutyavin, B Lajoie, B-K Lee, K Lee, D London, D Lotakis, S Neph; citation_volume=489; citation_publication_date=2012; citation_pages=75-82; citation_doi=10.1038/nature11232; citation_id=CR20
citation_journal_title=Nat Rev Genet; citation_title=Metazoan promoters: emerging characteristics and insights into transcriptional regulation; citation_author=B Lenhard, A Sandelin, P Carninci; citation_volume=13; citation_issue=4; citation_publication_date=2012; citation_pages=233-245; citation_id=CR21
citation_journal_title=PLoS Biol; citation_title=A user’s guide to the encyclopedia of DNA elements (ENCODE); citation_author=; citation_volume=9; citation_publication_date=2011; citation_pages=e1001046; citation_doi=10.1371/journal.pbio.1001046; citation_id=CR22
citation_journal_title=Nature; citation_title=An integrated encyclopedia of DNA elements in the human genome; citation_author=; citation_volume=489; citation_publication_date=2012; citation_pages=57-74; citation_doi=10.1038/nature11247; citation_id=CR23
citation_journal_title=J Neurobiol; citation_title=Cell lines in inner ear research; citation_author=MN Rivolta, MC Holley; citation_volume=53; citation_publication_date=2002; citation_pages=306-318; citation_doi=10.1002/neu.10111; citation_id=CR24
citation_journal_title=Bioinform Oxf Engl; citation_title=MatInspector and beyond: promoter analysis based on transcription factor binding sites; citation_author=K Cartharius, K Frech, K Grote, B Klocke, M Haltmeier, A Klingenhoff, M Frisch, M Bayerlein, T Werner; citation_volume=21; citation_publication_date=2005; citation_pages=2933-2942; citation_doi=10.1093/bioinformatics/bti473; citation_id=CR25
citation_journal_title=Bioinform Oxf Engl; citation_title=Estimating transcription factor bindability on DNA; citation_author=T Tsunoda, T Takagi; citation_volume=15; citation_publication_date=1999; citation_pages=622-630; citation_doi=10.1093/bioinformatics/15.7.622; citation_id=CR26
citation_journal_title=Database J Biol Databases Curation; citation_title=SHIELD: an integrative gene expression database for inner ear research; citation_author=J Shen, DI Scheffer, KY Kwan, DP Corey; citation_volume=2015; citation_publication_date=2015; citation_pages=bav071; citation_id=CR27
citation_journal_title=PLoS ONE; citation_title=A novel Atoh1 “self-terminating” mouse model reveals the necessity of proper Atoh1 level and duration for hair cell differentiation and viability; citation_author=N Pan, I Jahan, J Kersigo, JS Duncan, B Kopecky, B Fritzsch; citation_volume=7; citation_publication_date=2012; citation_pages=e30358; citation_doi=10.1371/journal.pone.0030358; citation_id=CR28
citation_journal_title=Dev Dyn; citation_title=Downstream targets of GATA3 in the vestibular sensory organs of the inner ear; citation_author=DM Alvarado, R Veile, J Speck, M Warchol, M Lovett; citation_volume=238; citation_publication_date=2009; citation_pages=3093-3102; citation_doi=10.1002/dvdy.22149; citation_id=CR29
citation_journal_title=Neurobiol Dis; citation_title=Hearing loss following Gata3 haploinsufficiency is caused by cochlear disorder; citation_author=J Wees, MA Looij, MM Ruiter, H Elias, H Burg, S-S Liem, D Kurek, JD Engel, A Karis, BG Zanten, CI Zeeuw, FG Grosveld, JH Doorninck; citation_volume=16; citation_publication_date=2004; citation_pages=169-178; citation_doi=10.1016/j.nbd.2004.02.004; citation_id=CR30
citation_journal_title=Hum Mol Genet; citation_title=Transcription profiling of inner ears from Pou4f3ddl/ddl identifies Gfi1 as a target of the Pou4f3 deafness gene; citation_author=R Hertzano; citation_volume=13; citation_publication_date=2004; citation_pages=2143-2153; citation_doi=10.1093/hmg/ddh218; citation_id=CR31
citation_journal_title=Front Pharmacol; citation_title=Protein kinases as switches for the function of upstream stimulatory factors: implications for tissue injury and cancer; citation_author=T Horbach, C Götz, T Kietzmann, EY Dimova; citation_volume=6; citation_publication_date=2015; citation_pages=3; citation_doi=10.3389/fphar.2015.00003; citation_id=CR32
citation_journal_title=Noise Health; citation_title=Differential gene expression following noise trauma in birds and mammals; citation_author=MI Lomax, T-W Gong, Y Cho, L Huang, S-H Oh, HJ Adler, Y Raphael, RA Altschuler; citation_volume=3; citation_publication_date=2001; citation_pages=19-35; citation_id=CR33
citation_journal_title=Mol Vis; citation_title=Microarray analysis of retinal gene expression in Egr-1 knockout mice; citation_author=R Schippert, F Schaeffel, MP Feldkaemper; citation_volume=15; citation_publication_date=2009; citation_pages=2720-2739; citation_id=CR34
citation_journal_title=J Cell Biol; citation_title=Role of Egr1 in hippocampal synaptic enhancement induced by tetanic stimulation and amputation; citation_author=F Wei, ZC Xu, Z Qu, J Milbrandt, M Zhuo; citation_volume=149; citation_publication_date=2000; citation_pages=1325-1334; citation_doi=10.1083/jcb.149.7.1325; citation_id=CR35
citation_journal_title=Eur J Histochem EJH; citation_title=Expression of immediate-early genes in the inferior colliculus and auditory cortex in salicylate-induced tinnitus in rat; citation_author=SS Hu, L Mei, JY Chen, ZW Huang, H Wu; citation_volume=58; citation_publication_date=2014; citation_pages=2294; citation_id=CR36
citation_journal_title=PLoS ONE; citation_title=Large scale gene expression profiles of regenerating inner ear sensory epithelia; citation_author=RD Hawkins, S Bashiardes, KE Powder, SA Sajan, V Bhonagiri, DM Alvarado, J Speck, ME Warchol, M Lovett; citation_volume=2; citation_publication_date=2007; citation_pages=e525; citation_doi=10.1371/journal.pone.0000525; citation_id=CR37
citation_journal_title=Microarrays Basel Switz; citation_title=The transcriptomics to proteomics of hair cell regeneration: looking for a hair cell in a haystack; citation_author=ME Smith, G Rajadinakaran; citation_volume=2; citation_publication_date=2013; citation_pages=186-207; citation_doi=10.3390/microarrays2030186; citation_id=CR38
citation_journal_title=J Neurosci; citation_title=Gene expression by mouse inner ear hair cells during development; citation_author=DI Scheffer, J Shen, DP Corey, Z-Y Chen; citation_volume=35; citation_publication_date=2015; citation_pages=6366-6380; citation_doi=10.1523/JNEUROSCI.5126-14.2015; citation_id=CR39
citation_journal_title=Genome Res; citation_title=Transcript profiling of functionally related groups of genes during conditional differentiation of a mammalian cochlear hair cell line; citation_author=MN Rivolta; citation_volume=12; citation_publication_date=2002; citation_pages=1091-1099; citation_doi=10.1101/gr.225602; citation_id=CR40
citation_journal_title=Nucleic Acids Res; citation_title=Localised sequence regions possessing high melting temperatures prevent the amplification of a DNA mimic in competitive PCR; citation_author=DG McDowell, NA Burns, HC Parkes; citation_volume=26; citation_publication_date=1998; citation_pages=3340-3347; citation_doi=10.1093/nar/26.14.3340; citation_id=CR41
citation_journal_title=Mol Biosyst; citation_title=Identification of DNA–protein complexes using an improved, combined western blotting-electrophoretic mobility shift assay (WEMSA) with a fluorescence imaging system; citation_author=K Deckmann, F Rörsch, G Geisslinger, S Grösch; citation_volume=8; citation_publication_date=2012; citation_pages=1389; citation_doi=10.1039/c2mb05500g; citation_id=CR42
citation_journal_title=J Biol Chem; citation_title=The novel PMCA2 pump mutation Tommy impairs cytosolic calcium clearance in hair cells and links to deafness in mice; citation_author=M Bortolozzi, M Brini, N Parkinson, G Crispino, P Scimemi, RD Siati, F Leva, A Parker, S Ortolano, E Arslan, SD Brown, E Carafoli, F Mammano; citation_volume=285; citation_publication_date=2010; citation_pages=37693-37703; citation_doi=10.1074/jbc.M110.170092; citation_id=CR43
citation_journal_title=J Assoc Res Otolaryngol; citation_title=Low endolymph calcium concentrations in deafwaddler2J mice suggest that PMCA2 contributes to endolymph calcium maintenance; citation_author=JD Wood, S Muchinsky, A Filoteo, J Penniston, B Tempel; citation_volume=5; citation_publication_date=2004; citation_pages=99-110; citation_doi=10.1007/s10162-003-4022-1; citation_id=CR44
citation_journal_title=Hear Res; citation_title=Evidence for differential regulation of calcium by outer versus inner hair cells: plasma membrane Ca-ATPase gene expression; citation_author=H Furuta, L Luo, K Hepler, AF Ryan; citation_volume=123; citation_publication_date=1998; citation_pages=10-26; citation_doi=10.1016/S0378-5955(98)00091-4; citation_id=CR45