Abstract
The solute carrier (SLC) group of membrane transport proteins includes about 400 members organized into more than 50 families. The SLC family that comprises nucleoside-sugar transporters is referred to as SLC35. One of the members of this family is SLC35F1. The function of SLC35F1 is still unknown; however, recent studies demonstrated that SLC35F1 mRNA is highly expressed in the brain and in the kidney. Therefore, we examine the distribution of Slc35f1 protein in the murine forebrain using immunohistochemistry. We could demonstrate that Slc35f1 is highly expressed in the adult mouse brain in a variety of different brain structures, including the cortex, hippocampus, amygdala, thalamus, basal ganglia, and hypothalamus. To examine the possible roles of Slc35f1 and its subcellular localization, we used an in vitro glioblastoma cell line expressing Slc35f1. Co-labeling experiments were performed to reveal the subcellular localization of Slc35f1. Our results indicate that Slc35f1 neither co-localizes with markers for the Golgi apparatus nor with markers for the endoplasmic reticulum. Time-lapse microscopy of living cells revealed that Slc35f1-positive structures are highly dynamic and resemble vesicles. Using super-resolution microscopy, these Slc35f1-positive spots clearly co-localize with the recycling endosome marker Rab11.
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Atikuzzaman M, Alvarez-Rodriguez M, Vicente-Carrillo A, Johnsson M, Wright D, Rodriguez-Martinez H (2017) Conserved gene expression in sperm reservoirs between birds and mammals in response to mating. BMC Genomics 18:98
Avery CL, Wassel CL, Richard MA, Highland HM, Bien S, Zubair N, Soliman EZ, Fornage M, Bielinski SJ, Tao R, Seyerle AA, Shah SJ, Lloyd-Jones DM, Buyske S, Rotter JI, Post WS, Rich SS, Hindorff LA, Jeff JM, Shohet RV, Sotoodehnia N, Lin DY, Whitsel EA, Peters U, Haiman CA, Crawford DC, Kooperberg C, North KE (2017) Fine mapping of QT interval regions in global populations refines previously identified QT interval loci and identifies signals unique to African and Hispanic descent populations. Heart Rhythm 14:572–580
Blumenthal A, Giebel J, Warsow G, Li L, Ummanni R, Schordan S, Schordan E, Klemm P, Gretz N, Endlich K, Endlich N (2015) Mechanical stress enhances CD9 expression in cultured podocytes. Am J Physiol Ren Physiol 308:F602–F613
Brown TC, Correia SS, Petrok CN, Esteban JA (2007) Functional compartmentalization of endosomal trafficking for the synaptic delivery of AMPA receptors during long-term potentiation. J Neurosci 27:13311–13315
Busch R, Baldus M, Vogt M, Berger S, Bartsch D, Gass P, von Bohlen und Halbach O (2017) Effects of p75NTR-deficiency on cholinergic innervation of the amygdala and anxiety-like behavior. J Neurochem 141:461–471
Chen W, Feng Y, Chen D, Wandinger-Ness A (1998) Rab11 is required for trans-golgi network-to-plasma membrane transport and a preferential target for GDP dissociation inhibitor. Mol Biol Cell 9:3241–3257
Coe H, Michalak M (2010) ERp57, a multifunctional endoplasmic reticulum resident oxidoreductase. Int J Biochem Cell Biol 42:796–799
Creeley CE, Olney JW (2010) The young: neuroapoptosis induced by anesthetics and what to do about it. Anesth Analg 110:442–448
D'Adamo P, Masetti M, Bianchi V, More L, Mignogna ML, Giannandrea M, Gatti S (2014) RAB GTPases and RAB-interacting proteins and their role in the control of cognitive functions. Neurosci Biobehav Rev 46(Pt 2):302–314
Di Bonaventura C, Labate A, Maschio M, Meletti S, Russo E (2017) AMPA receptors and perampanel behind selected epilepsies: current evidence and future perspectives. Expert Opin Pharmacother 18:1751–1764
Dokter M, Busch R, Poser R, Vogt MA, von Bohlen und Halbach V, Gass P, Unsicker K, von Bohlen und Halbach O (2015) Implications of p75NTR for dentate gyrus morphology and hippocampus-related behavior revisited. Brain Struct Funct 220:1449–1462
Eijgelsheim M, Newton-Cheh C, Sotoodehnia N, de Bakker PI, Muller M, Morrison AC, Smith AV, Isaacs A, Sanna S, Dorr M, Navarro P, Fuchsberger C, Nolte IM, de Geus EJ, Estrada K, Hwang SJ, Bis JC, Ruckert IM, Alonso A, Launer LJ, Hottenga JJ, Rivadeneira F, Noseworthy PA, Rice KM, Perz S, Arking DE, Spector TD, Kors JA, Aulchenko YS, Tarasov KV, Homuth G, Wild SH, Marroni F, Gieger C, Licht CM, Prineas RJ, Hofman A, Rotter JI, Hicks AA, Ernst F, Najjar SS, Wright AF, Peters A, Fox ER, Oostra BA, Kroemer HK, Couper D, Volzke H, Campbell H, Meitinger T, Uda M, Witteman JC, Psaty BM, Wichmann HE, Harris TB, Kaab S, Siscovick DS, Jamshidi Y, Uitterlinden AG, Folsom AR, Larson MG, Wilson JF, Penninx BW, Snieder H, Pramstaller PP, van Duijn CM, Lakatta EG, Felix SB, Gudnason V, Pfeufer A, Heckbert SR, Stricker BH, Boerwinkle E, O'Donnell CJ (2010) Genome-wide association analysis identifies multiple loci related to resting heart rate. Hum Mol Genet 19:3885–3894
Franklin K, Paxinos G (2008) The mouse brain in stereotaxic coordinates, 3rd edn. Academic Press, Cambridge
Freund M, Walther T, von Bohlen und Halbach O (2012) Immunohistochemical localization of the angiotensin-(1-7) receptor Mas in the murine forebrain. Cell Tissue Res 348:29–35
Gebhardt C, von Bohlen und Halbach O, Hadler MD, Harteneck C, Albrecht D (2016) A novel form of capsaicin-modified amygdala LTD mediated by TRPM1. Neurobiol Learn Mem 136:1–12
Gu J, Firestein BL, Zheng JQ (2008) Microtubules in dendritic spine development. J Neurosci 28:12120–12124
Hamdan FF, Myers CT, Cossette P, Lemay P, Spiegelman D, Laporte AD, Nassif C, Diallo O, Monlong J, Cadieux-Dion M, Dobrzeniecka S, Meloche C, Retterer K, Cho MT, Rosenfeld JA, Bi W, Massicotte C, Miguet M, Brunga L, Regan BM, Mo K, Tam C, Schneider A, Hollingsworth G, Deciphering Developmental Disorders S, FitzPatrick DR, Donaldson A, Canham N, Blair E, Kerr B, Fry AE, Thomas RH, Shelagh J, Hurst JA, Brittain H, Blyth M, Lebel RR, Gerkes EH, Davis-Keppen L, Stein Q, Chung WK, Dorison SJ, Benke PJ, Fassi E, Corsten-Janssen N, Kamsteeg EJ, Mau-Them FT, Bruel AL, Verloes A, Ounap K, Wojcik MH, Albert DVF, Venkateswaran S, Ware T, Jones D, Liu YC, Mohammad SS, Bizargity P, Bacino CA, Leuzzi V, Martinelli S, Dallapiccola B, Tartaglia M, Blumkin L, Wierenga KJ, Purcarin G, O'Byrne JJ, Stockler S, Lehman A, Keren B, Nougues MC, Mignot C, Auvin S, Nava C, Hiatt SM, Bebin M, Shao Y, Scaglia F, Lalani SR, Frye RE, Jarjour IT, Jacques S, Boucher RM, Riou E, Srour M, Carmant L, Lortie A, Major P, Diadori P, Dubeau F, D'Anjou G, Bourque G, Berkovic SF, Sadleir LG, Campeau PM, Kibar Z, Lafreniere RG, Girard SL, Mercimek-Mahmutoglu S, Boelman C, Rouleau GA, Scheffer IE, Mefford HC, Andrade DM, Rossignol E, Minassian BA, Michaud JL (2017) High rate of recurrent de novo mutations in developmental and epileptic encephalopathies. Am J Hum Genet 101:664–685
Hediger MA, Clemencon B, Burrier RE, Bruford EA (2013) The ABCs of membrane transporters in health and disease (SLC series): introduction. Mol Asp Med 34:95–107
Ishida N, Kawakita M (2004) Molecular physiology and pathology of the nucleotide sugar transporter family (SLC35). Pflugers Arch 447:768–775
Kasukurthi R, Brenner MJ, Moore AM, Moradzadeh A, Ray WZ, Santosa KB, Mackinnon SE, Hunter DA (2009) Transcardial perfusion versus immersion fixation for assessment of peripheral nerve regeneration. J Neurosci Methods 184:303–309
Kokotos AC, Peltier J, Davenport EC, Trost M, Cousin MA (2018) Activity-dependent bulk endocytosis proteome reveals a key presynaptic role for the monomeric GTPase Rab11. Proc Natl Acad Sci U S A 115:E10177–E10186
Koschützke L, Bertram J, Hartmann B, Bartsch D, Lotze M, von Bohlen und Halbach O (2015) SrGAP3 knockout mice display enlarged lateral ventricles and specific cilia disturbances of ependymal cells in the third ventricle. Cell Tissue Res 361:645–650
Lazo OM, Gonzalez A, Ascano M, Kuruvilla R, Couve A, Bronfman FC (2013) BDNF regulates Rab11-mediated recycling endosome dynamics to induce dendritic branching. J Neurosci 33:6112–6122
Ng EL, Tang BL (2008) Rab GTPases and their roles in brain neurons and glia. Brain Res Rev 58:236–246
Nishimura M, Suzuki S, Satoh T, Naito S (2009) Tissue-specific mRNA expression profiles of human solute carrier 35 transporters. Drug Metab Pharmacokinet 24:91–99
Payne HL (2008) The role of transmembrane AMPA receptor regulatory proteins (TARPs) in neurotransmission and receptor trafficking (review). Mol Membr Biol 25:353–362
Sall JW, Stratmann G, Leong J, McKleroy W, Mason D, Shenoy S, Pleasure SJ, Bickler PE (2009) Isoflurane inhibits growth but does not cause cell death in hippocampal neural precursor cells grown in culture. Anesthesiology 110:826–833
Shirao T, Gonzalez-Billault C (2013) Actin filaments and microtubules in dendritic spines. J Neurochem 126:155–164
Siegerist F, Ribback S, Dombrowski F, Amann K, Zimmermann U, Endlich K, Endlich N (2017) Structured illumination microscopy and automatized image processing as a rapid diagnostic tool for podocyte effacement. Sci Rep 7:11473
Song Z (2013) Roles of the nucleotide sugar transporters (SLC35 family) in health and disease. Mol Asp Med 34:590–600
Stratmann G, Sall JW, May LD, Bell JS, Magnusson KR, Rau V, Visrodia KH, Alvi RS, Ku B, Lee MT, Dai R (2009) Isoflurane differentially affects neurogenesis and long-term neurocognitive function in 60-day-old and 7-day-old rats. Anesthesiology 110:834–848
Szafranski P, Von Allmen GK, Graham BH, Wilfong AA, Kang SH, Ferreira JA, Upton SJ, Moeschler JB, Bi W, Rosenfeld JA, Shaffer LG, Wai Cheung S, Stankiewicz P, Lalani SR (2015) 6q22.1 microdeletion and susceptibility to pediatric epilepsy. Eur J Hum Genet 23:173–179
Takahashi S, Kubo K, Waguri S, Yabashi A, Shin HW, Katoh Y, Nakayama K (2012) Rab11 regulates exocytosis of recycling vesicles at the plasma membrane. J Cell Sci 125:4049–4057
Vasan RS, Glazer NL, Felix JF, Lieb W, Wild PS, Felix SB, Watzinger N, Larson MG, Smith NL, Dehghan A, Grosshennig A, Schillert A, Teumer A, Schmidt R, Kathiresan S, Lumley T, Aulchenko YS, Konig IR, Zeller T, Homuth G, Struchalin M, Aragam J, Bis JC, Rivadeneira F, Erdmann J, Schnabel RB, Dorr M, Zweiker R, Lind L, Rodeheffer RJ, Greiser KH, Levy D, Haritunians T, Deckers JW, Stritzke J, Lackner KJ, Volker U, Ingelsson E, Kullo I, Haerting J, O'Donnell CJ, Heckbert SR, Stricker BH, Ziegler A, Reffelmann T, Redfield MM, Werdan K, Mitchell GF, Rice K, Arnett DK, Hofman A, Gottdiener JS, Uitterlinden AG, Meitinger T, Blettner M, Friedrich N, Wang TJ, Psaty BM, van Duijn CM, Wichmann HE, Munzel TF, Kroemer HK, Benjamin EJ, Rotter JI, Witteman JC, Schunkert H, Schmidt H, Volzke H, Blankenberg S (2009) Genetic variants associated with cardiac structure and function: a meta-analysis and replication of genome-wide association data. JAMA 302:168–178
von Bohlen und Halbach O (2009) Structure and function of dendritic spines within the hippocampus. Ann Anat 191:518–531
Zschenderlein C, Gebhardt C, von Bohlen und Halbach O, Kulisch C, Albrecht D (2011) Capsaicin-induced changes in LTP in the lateral amygdala are mediated by TRPV1. PLoS One 6:e16116
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We thank Sabine Hanisch and Sindy Schröder for excellent technical assistance.
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ESM 1
Time-lapse movie tracing of slc35f1 positive structures that move within the cell soma (one that moves towards the center of the cell is highlighted by a red arrow; 3 frames per second) (AVI 1174 kb)
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Farenholtz, J., Artelt, N., Blumenthal, A. et al. Expression of Slc35f1 in the murine brain. Cell Tissue Res 377, 167–176 (2019). https://doi.org/10.1007/s00441-019-03008-8
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DOI: https://doi.org/10.1007/s00441-019-03008-8