The polyamine transporter Slc18b1(VPAT) is important for both short and long time memory and for regulation of polyamine content in the brain
Autoři:
Robert Fredriksson aff001; Smitha Sreedharan aff002; Karin Nordenankar aff001; Johan Alsiö aff002; Frida A. Lindberg aff001; Ashley Hutchinson aff002; Anders Eriksson aff002; Sahar Roshanbin aff001; Diana M. Ciuculete aff002; Anica Klockars aff002; Aniruddha Todkar aff002; Maria G. Hägglund aff002; Sofie V. Hellsten aff001; Viktoria Hindlycke aff002; Åke Västermark aff002; Ganna Shevchenko aff003; Gaia Olivo aff002; Cheng K aff004; Klas Kullander aff002; Ali Moazzami aff004; Jonas Bergquist aff003; Pawel K. Olszewski aff002; Helgi B. Schiöth aff002
Působiště autorů:
Department of Pharmaceutical Biosciences, Uppsala University, Uppsala, Sweden
aff001; Department of Neuroscience, Functional Pharmacology, Uppsala University, Uppsala, Sweden
aff002; Department of Chemistry, Uppsala University, Uppsala, Sweden
aff003; Department of Molecular Sciences, Swedish University of Agricultural Sciences, Uppsala, Sweden
aff004; Institute for Translational Medicine and Biotechnology, Sechenov First Moscow State Medical University, Moscow, Russia
aff005
Vyšlo v časopise:
The polyamine transporter Slc18b1(VPAT) is important for both short and long time memory and for regulation of polyamine content in the brain. PLoS Genet 15(12): e32767. doi:10.1371/journal.pgen.1008455
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pgen.1008455
Souhrn
SLC18B1 is a sister gene to the vesicular monoamine and acetylcholine transporters, and the only known polyamine transporter, with unknown physiological role. We reveal that Slc18b1 knock out mice has significantly reduced polyamine content in the brain providing the first evidence that Slc18b1 is functionally required for regulating polyamine levels. We found that this mouse has impaired short and long term memory in novel object recognition, radial arm maze and self-administration paradigms. We also show that Slc18b1 KO mice have altered expression of genes involved in Long Term Potentiation, plasticity, calcium signalling and synaptic functions and that expression of components of GABA and glutamate signalling are changed. We further observe a partial resistance to diazepam, manifested as significantly lowered reduction in locomotion after diazepam treatment. We suggest that removal of Slc18b1 leads to reduction of polyamine contents in neurons, resulting in reduced GABA signalling due to long-term reduction in glutamatergic signalling.
Klíčová slova:
Animal behavior – Cognitive impairment – Gamma-aminobutyric acid – Glutamate – Memory – Mice – Nose – Diazepam
Zdroje
1. Pegg AE. Functions of Polyamines in Mammals. J Biol Chem. 2016;291(29):14904–12. doi: 10.1074/jbc.R116.731661 27268251.
2. Pegg AE. Mammalian polyamine metabolism and function. IUBMB Life. 2009;61(9):880–94. doi: 10.1002/iub.230 19603518.
3. Miller-Fleming L, Olin-Sandoval V, Campbell K, Ralser M. Remaining Mysteries of Molecular Biology: The Role of Polyamines in the Cell. J Mol Biol. 2015;427(21):3389–406. doi: 10.1016/j.jmb.2015.06.020 26156863.
4. Pendeville H, Carpino N, Marine JC, Takahashi Y, Muller M, Martial JA, et al. The ornithine decarboxylase gene is essential for cell survival during early murine development. Mol Cell Biol. 2001;21(19):6549–58. doi: 10.1128/MCB.21.19.6549-6558.2001 11533243.
5. McGurk JF, Bennett MV, Zukin RS. Polyamines potentiate responses of N-methyl-D-aspartate receptors expressed in xenopus oocytes. Proc Natl Acad Sci U S A. 1990;87(24):9971–4. doi: 10.1073/pnas.87.24.9971 1702227.
6. Williams K, Romano C, Dichter MA, Molinoff PB. Modulation of the NMDA receptor by polyamines. Life Sci. 1991;48(6):469–98. doi: 10.1016/0024-3205(91)90463-l 1825128.
7. Meyer RC, Knox J, Purwin DA, Spangler EL, Ingram DK. Combined stimulation of the glycine and polyamine sites of the NMDA receptor attenuates NMDA blockade-induced learning deficits of rats in a 14-unit T-maze. Psychopharmacology (Berl). 1998;135(3):290–5. doi: 10.1007/s002130050512 9498733.
8. Benveniste M, Mayer ML. Multiple effects of spermine on N-methyl-D-aspartic acid receptor responses of rat cultured hippocampal neurones. J Physiol. 1993;464:131–63. doi: 10.1113/jphysiol.1993.sp019627 8229795.
9. Mott DD, Washburn MS, Zhang S, Dingledine RJ. Subunit-dependent modulation of kainate receptors by extracellular protons and polyamines. J Neurosci. 2003;23(4):1179–88. doi: 10.1523/JNEUROSCI.23-04-01179.2003 12598606.
10. Hiasa M, Miyaji T, Haruna Y, Takeuchi T, Harada Y, Moriyama S, et al. Identification of a mammalian vesicular polyamine transporter. Scientific reports. 2014;4:6836. doi: 10.1038/srep06836 25355561.
11. Anne C, Gasnier B. Vesicular neurotransmitter transporters: mechanistic aspects. Current topics in membranes. 2014;73:149–74. doi: 10.1016/B978-0-12-800223-0.00003-7 24745982.
12. de Castro BM, De Jaeger X, Martins-Silva C, Lima RD, Amaral E, Menezes C, et al. The vesicular acetylcholine transporter is required for neuromuscular development and function. Mol Cell Biol. 2009;29(19):5238–50. doi: 10.1128/MCB.00245-09 19635813.
13. Jacobsson JA, Stephansson O, Fredriksson R. C6ORF192 forms a unique evolutionary branch among solute carriers (SLC16, SLC17, and SLC18) and is abundantly expressed in several brain regions. Journal of molecular neuroscience: MN. 2010;41(2):230–42. doi: 10.1007/s12031-009-9222-7 19697161.
14. Sreedharan S, Shaik JH, Olszewski PK, Levine AS, Schioth HB, Fredriksson R. Glutamate, aspartate and nucleotide transporters in the SLC17 family form four main phylogenetic clusters: evolution and tissue expression. BMC Genomics. 11(1):17. Epub 2010/01/12. doi: 10.1186/1471-2164-11-17 20059771.
15. Rodriguez CI, Buchholz F, Galloway J, Sequerra R, Kasper J, Ayala R, et al. High-efficiency deleter mice show that FLPe is an alternative to Cre-loxP. Nat Genet. 2000;25(2):139–40. doi: 10.1038/75973 10835623.
16. Lallemand Y, Luria V, Haffner-Krausz R, Lonai P. Maternally expressed PGK-Cre transgene as a tool for early and uniform activation of the Cre site-specific recombinase. Transgenic Res. 1998;7(2):105–12. doi: 10.1023/a:1008868325009 9608738.
17. Jarrard LE, Okaichi H, Steward O, Goldschmidt RB. On the role of hippocampal connections in the performance of place and cue tasks: comparisons with damage to hippocampus. Behav Neurosci. 1984;98(6):946–54. doi: 10.1037//0735-7044.98.6.946 6439229.
18. Sanchis-Segura C, Spanagel R. Behavioural assessment of drug reinforcement and addictive features in rodents: an overview. Addict Biol. 2006;11(1):2–38. doi: 10.1111/j.1369-1600.2006.00012.x 16759333.
19. Reiner A, Yekutieli D, Benjamini Y. Identifying differentially expressed genes using false discovery rate controlling procedures. Bioinformatics. 2003;19(3):368–75. doi: 10.1093/bioinformatics/btf877 12584122.
20. Benjamini Y, Hochberg Y. Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing J R Stat Soc Series B Stat Methodol. 1995;57(1):289–300.
21. Mootha VK, Lindgren CM, Eriksson KF, Subramanian A, Sihag S, Lehar J, et al. PGC-1alpha-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat Genet. 2003;34(3):267–73. doi: 10.1038/ng1180 12808457.
22. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci U S A. 2005;102(43):15545–50. doi: 10.1073/pnas.0506580102 16199517.
23. Kanehisa M, Furumichi M, Tanabe M, Sato Y, Morishima K. KEGG: new perspectives on genomes, pathways, diseases and drugs. Nucleic Acids Res. 2017;45(D1):D353–D61. doi: 10.1093/nar/gkw1092 27899662.
24. Caruso V, Lagerstrom MC, Olszewski PK, Fredriksson R, Schioth HB. Synaptic changes induced by melanocortin signalling. Nature reviews Neuroscience. 2014;15(2):98–110. doi: 10.1038/nrn3657 24588018.
25. Bach ME, Hawkins RD, Osman M, Kandel ER, Mayford M. Impairment of spatial but not contextual memory in CaMKII mutant mice with a selective loss of hippocampal LTP in the range of the theta frequency. Cell. 1995;81(6):905–15. doi: 10.1016/0092-8674(95)90010-1 7781067.
26. Matsuo N, Yamasaki N, Ohira K, Takao K, Toyama K, Eguchi M, et al. Neural activity changes underlying the working memory deficit in alpha-CaMKII heterozygous knockout mice. Frontiers in behavioral neuroscience. 2009;3:20. doi: 10.3389/neuro.08.020.2009 19750198.
27. Kelleher RJ 3rd, Govindarajan A, Jung HY, Kang H, Tonegawa S. Translational control by MAPK signaling in long-term synaptic plasticity and memory. Cell. 2004;116(3):467–79. doi: 10.1016/s0092-8674(04)00115-1 15016380.
28. Chen X, Garelick MG, Wang H, Lil V, Athos J, Storm DR. PI3 kinase signaling is required for retrieval and extinction of contextual memory. Nature neuroscience. 2005;8(7):925–31. doi: 10.1038/nn1482 15937483.
29. Antunes M, Biala G. The novel object recognition memory: neurobiology, test procedure, and its modifications. Cognitive processing. 2012;13(2):93–110. doi: 10.1007/s10339-011-0430-z 22160349.
30. Skinner BF. The phylogeny and ontogeny of behavior. Contingencies of reinforcement throw light on contingencies of survival in the evolution of behavior. Science. 1966;153(3741):1205–13. doi: 10.1126/science.153.3741.1205 5918710.
31. Chun MM, Phelps EA. Memory deficits for implicit contextual information in amnesic subjects with hippocampal damage. Nature neuroscience. 1999;2(9):844–7. doi: 10.1038/12222 10461225.
32. Bjarnadottir TK, Fredriksson R, Schioth HB. The gene repertoire and the common evolutionary history of glutamate, pheromone (V2R), taste(1) and other related G protein-coupled receptors. Gene. 2005;362:70–84. doi: 10.1016/j.gene.2005.07.029 16229975.
33. Niswender CM, Conn PJ. Metabotropic glutamate receptors: physiology, pharmacology, and disease. Annual review of pharmacology and toxicology. 2010;50:295–322. doi: 10.1146/annurev.pharmtox.011008.145533 20055706.
34. Ramani D, De Bandt JP, Cynober L. Aliphatic polyamines in physiology and diseases. Clin Nutr. 2014;33(1):14–22. doi: 10.1016/j.clnu.2013.09.019 24144912.
35. Takeuchi T, Harada Y, Moriyama S, Furuta K, Tanaka S, Miyaji T, et al. Vesicular Polyamine Transporter Mediates Vesicular Storage and Release of Polyamine from Mast Cells. J Biol Chem. 2017;292(9):3909–18. doi: 10.1074/jbc.M116.756197 28082679.
36. Luscher C, Malenka RC. NMDA receptor-dependent long-term potentiation and long-term depression (LTP/LTD). Cold Spring Harb Perspect Biol. 2012;4(6). doi: 10.1101/cshperspect.a005710 22510460.
37. Hagglund MG, Hellsten SV, Bagchi S, Ljungdahl A, Nilsson VC, Winnergren S, et al. Characterization of the transporterB0AT3 (Slc6a17) in the rodent central nervous system. BMC Neurosci. 2013;14:54. doi: 10.1186/1471-2202-14-54 23672601.
38. Linford A, Yoshimura S, Nunes Bastos R, Langemeyer L, Gerondopoulos A, Rigden DJ, et al. Rab14 and its exchange factor FAM116 link endocytic recycling and adherens junction stability in migrating cells. Dev Cell. 2012;22(5):952–66. doi: 10.1016/j.devcel.2012.04.010 22595670.
39. Saluja R, Kumar A, Jain M, Goel SK, Jain A. Role of Sphingosine-1-Phosphate in Mast Cell Functions and Asthma and Its Regulation by Non-Coding RNA. Front Immunol. 2017;8:587. doi: 10.3389/fimmu.2017.00587 28588581.
40. Hammond JW, Cai D, Verhey KJ. Tubulin modifications and their cellular functions. Curr Opin Cell Biol. 2008;20(1):71–6. doi: 10.1016/j.ceb.2007.11.010 18226514.
41. Bormann J. Electrophysiological characterization of diazepam binding inhibitor (DBI) on GABAA receptors. Neuropharmacology. 1991;30(12B):1387–9. doi: 10.1016/s0028-3908(11)80006-7 1723508.
42. Underhill SM, Wheeler DS, Li M, Watts SD, Ingram SL, Amara SG. Amphetamine modulates excitatory neurotransmission through endocytosis of the glutamate transporter EAAT3 in dopamine neurons. Neuron. 2014;83(2):404–16. doi: 10.1016/j.neuron.2014.05.043 25033183.
43. Paladini CA, Fiorillo CD, Morikawa H, Williams JT. Amphetamine selectively blocks inhibitory glutamate transmission in dopamine neurons. Nature neuroscience. 2001;4(3):275–81. doi: 10.1038/85124 11224544.
44. Adams MM, Smith TD, Moga D, Gallagher M, Wang Y, Wolfe BB, et al. Hippocampal dependent learning ability correlates with N-methyl-D-aspartate (NMDA) receptor levels in CA3 neurons of young and aged rats. J Comp Neurol. 2001;432(2):230–43. doi: 10.1002/cne.1099 11241388.
45. Rao TS, Cler JA, Oei EJ, Emmett MR, Mick SJ, Iyengar S, et al. The polyamines, spermine and spermidine, negatively modulate N-methyl-d-aspartate (NMDA) and quisqualate receptor mediated responses in vivo: Cerebellar cyclic GMP measurements. Neurochem Int. 1990;16(2):199–206. doi: 10.1016/0197-0186(90)90088-b 20504558.
46. Chapouthier G, Venault P. GABA-A receptor complex and memory processes. Curr Top Med Chem. 2002;2(8):841–51 12171575.
47. Thanapreedawat P, Kobayashi H, Inui N, Sakamoto K, Kim M, Yoto A, et al. GABA affects novel object recognition memory and working memory in rats. J Nutr Sci Vitaminol (Tokyo). 2013;59(2):152–7. doi: 10.3177/jnsv.59.152 23727647.
48. Cheng K, Mullner E, Moazzami AA, Carlberg H, Brannas E, Pickova J. Metabolomics Approach To Evaluate a Baltic Sea Sourced Diet for Cultured Arctic Char (Salvelinus alpinus L.). Journal of agricultural and food chemistry. 2017;65(24):5083–90. doi: 10.1021/acs.jafc.7b00994 28557427.
49. Wishart DS, Tzur D, Knox C, Eisner R, Guo AC, Young N, et al. HMDB: the Human Metabolome Database. Nucleic Acids Res. 2007;35(Database issue):D521–6. doi: 10.1093/nar/gkl923 17202168.
50. Rohnisch HE, Eriksson J, Mullner E, Agback P, Sandstrom C, Moazzami AA. AQuA: An Automated Quantification Algorithm for High-Throughput NMR-Based Metabolomics and Its Application in Human Plasma. Analytical chemistry. 2018;90(3):2095–102. doi: 10.1021/acs.analchem.7b04324 29260864.
51. Li C, Wong WH. Model-based analysis of oligonucleotide arrays: expression index computation and outlier detection. Proc Natl Acad Sci U S A. 2001;98(1):31–6. doi: 10.1073/pnas.011404098 11134512.
52. Smyth GK. Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol. 2004;3:Article3. doi: 10.2202/1544-6115.1027 16646809.
53. Smyth GK. limma: Linear Models for Microarray Data. In: Gentleman R, Carey V, Dudoit S, Irizarry R, Huber W, editors. Bioinformatics and Computational Biology Solutions using R and Bioconductor: Sringer; 2015. p. 397–420.
54. Bordier C. Phase-Separation of Integral Membrane-Proteins in Triton X-114 Solution. J Biol Chem. 1981;256(4):1604–7. 6257680
55. Mastro R, Hall M. Protein delipidation and precipitation by tri-n-butylphosphate, acetone, and methanol treatment for isoelectric focusing and two-dimensional gel electrophoresis. Analytical biochemistry. 1999;273(2):313–5. doi: 10.1006/abio.1999.4224 10469505.
56. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951;193(1):265–75. 14907713.
57. Wisniewski JR, Zougman A, Nagaraj N, Mann M. Universal sample preparation method for proteome analysis. Nat Methods. 2009;6(5):359–U60. doi: 10.1038/nmeth.1322 19377485
58. Boersema PJ, Raijmakers R, Lemeer S, Mohammed S, Heck AJ. Multiplex peptide stable isotope dimethyl labeling for quantitative proteomics. Nature protocols. 2009;4(4):484–94. doi: 10.1038/nprot.2009.21 19300442.
59. Walf AA, Frye CA. The use of the elevated plus maze as an assay of anxiety-related behavior in rodents. Nature protocols. 2007;2(2):322–8. doi: 10.1038/nprot.2007.44 17406592.
60. Deacon RM. Measuring motor coordination in mice. J Vis Exp. 2013;(75):e2609. doi: 10.3791/2609 23748408.
61. Sharma S, Rakoczy S, Brown-Borg H. Assessment of spatial memory in mice. Life Sci. 2010;87(17–18):521–36. doi: 10.1016/j.lfs.2010.09.004 20837032.
62. Richardson NR, Roberts DC. Progressive ratio schedules in drug self-administration studies in rats: a method to evaluate reinforcing efficacy. Journal of neuroscience methods. 1996;66(1):1–11. doi: 10.1016/0165-0270(95)00153-0 8794935.
63. Davies G, Marioni RE, Liewald DC, Hill WD, Hagenaars SP, Harris SE, et al. Genome-wide association study of cognitive functions and educational attainment in UK Biobank (N = 112 151). Molecular psychiatry. 2016;21(6):758–67. doi: 10.1038/mp.2016.45 27046643.
64. Shimoyama I, Ninchoji T, Uemura K. The finger-tapping test. A quantitative analysis. Archives of neurology. 1990;47(6):681–4. doi: 10.1001/archneur.1990.00530060095025 2346396.
65. Hagenaars SP, Cox SR, Hill WD, Davies G, Liewald DCM, Group CcCW, et al. Genetic contributions to Trail Making Test performance in UK Biobank. Molecular psychiatry. 2017. doi: 10.1038/mp.2017.189 28924184.
66. Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MA, Bender D, et al. PLINK: a tool set for whole-genome association and population-based linkage analyses. American journal of human genetics. 2007;81(3):559–75. doi: 10.1086/519795 17701901.
Štítky
Genetika Reprodukční medicínaČlánek vyšel v časopise
PLOS Genetics
2019 Číslo 12
- Primární hyperoxalurie – aktuální možnosti diagnostiky a léčby
- Srdeční frekvence embrya může být faktorem užitečným v předpovídání výsledku IVF
- Akutní intermitentní porfyrie
- Vztah užívání alkoholu a mužské fertility
- Šanci na úspěšný průběh těhotenství snižují nevhodné hladiny progesteronu vznikající při umělém oplodnění
Nejčtenější v tomto čísle
- Aspergillus fumigatus calcium-responsive transcription factors regulate cell wall architecture promoting stress tolerance, virulence and caspofungin resistance
- Architecture of the Escherichia coli nucleoid
- Common gardens in teosintes reveal the establishment of a syndrome of adaptation to altitude
- Restricted and non-essential redundancy of RNAi and piRNA pathways in mouse oocytes