Postnatal developmental expression of regulator of G protein signaling 14 (RGS14) in the mouse brain

Journal of Comparative Neurology

Volumn 522, Issue 1, 2014, Pages 186-203

  Evans, Paul R ^a   Lee, Sarah E ^a   Smith, Yoland ^a,b   Hepler, John R ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b EMORY UNIVERSITY   (United States)

Author keywords

Hippocampal CA2; Hippocampus; RGS proteins; RGS14; Synaptic plasticity

Indexed keywords

GUANINE NUCLEOTIDE BINDING PROTEIN; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; PEROXIDASE; RGS 14 PROTEIN; RGS PROTEIN; SCAFFOLD PROTEIN; UNCLASSIFIED DRUG;

ADULT; ANIMAL EXPERIMENT; ANTIBODY SPECIFICITY; ARTICLE; BRAIN DEVELOPMENT; CONTROLLED STUDY; FEMALE; HIPPOCAMPAL CA2 REGION; HIPPOCAMPUS; IMMUNOREACTIVITY; LEARNING; MALE; MEMORY; MOUSE; NEOCORTEX; NERVE CELL PLASTICITY; NONHUMAN; OLFACTORY NUCLEUS; ORBITAL CORTEX; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PYRIFORM CORTEX; SPATIOTEMPORAL ANALYSIS; UPREGULATION;

HIPPOCAMPAL CA2; HIPPOCAMPUS; RGS PROTEINS; RGS14; SYNAPTIC PLASTICITY;

ANIMALS; ANTIBODIES, MONOCLONAL; BRAIN; CEREBRAL CORTEX; FEMALE; HIPPOCAMPUS; IMMUNOBLOTTING; IMMUNOENZYME TECHNIQUES; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; RATS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RGS PROTEINS; RNA, MESSENGER; UP-REGULATION;

EID: 84888268259     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.23395     Document Type: Article

References (39)

1. Benes FM, Kwok EW, Vincent SL, Todtenkopf MS. 1998. A reduction of nonpyramidal cells in sector CA2 of schizophrenics and manic depressives. Biol Psychiatry 44:88-97.
2. Bernstein LS, Ramineni S, Hague C, Cladman W, Chidiac P, Levey AI, Hepler JR. 2004. RGS2 binds directly and selectively to the M1 muscarinic acetylcholine receptor third intracellular loop to modulate Gq/11alpha signaling. J Biol Chem 279:21248-21256.
3. Braak H. 1980.Architectonics of the human telencephalic cortex Berlin: Springer.
4. Bruckner G, Grosche J, Hartlage-Rubsamen M, Schmidt S, Schachner M. 2003. Region and lamina-specific distribution of extracellular matrix proteoglycans, hyaluronan, and tenascin-R in the mouse hippocampal formation. J Chem Neuroanat 26:37-50.
5. Caruana DA, Alexander GM, Dudek SM. 2012. New insights into the regulation of synaptic plasticity from an unexpected place: hippocampal area CA2. Learn Mem 19:391-400.
6. Chevaleyre V, Siegelbaum SA. 2010. Strong CA2 pyramidal neuron synapses define a powerful disynaptic cortico-hippocampal loop. Neuron 66:560-572.
7. Cho H, Kozasa T, Takekoshi K, De Gunzburg J, Kehrl JH. 2000. RGS14, a GTPase-activating protein for Gi alpha, attenuates Gi alpha- and G13 alpha-mediated signaling pathways. Mol Pharmacol 58:569-576.
8. DeVito LM, Konigsberg R, Lykken C, Sauvage M, Young WS 3rd, Eichenbaum H. 2009. Vasopressin 1b receptor knock-out impairs memory for temporal order. J Neurosci 29:2676-2683.
9. Fiala JC, Feinberg M, Popov V, Harris KM. 1998. Synaptogenesis via dendritic filopodia in developing hippocampal area CA1. J Neurosci 18:8900-8911.
10. Grafstein-Dunn E, Young KH, Cockett MI, Khawaja XZ. 2001. Regional distribution of regulators of G-protein signaling (RGS) 1, 2, 13, 14, 16, and GAIP messenger ribonucleic acids by in situ hybridization in rat brain. Mol Brain Res 88:113-123.
11. Hollinger S, Hepler JR. 2002. Cellular regulation of RGS proteins: modulators and integrators of G protein signaling. Pharmacol Rev 54:527-559.
12. Hollinger S, Taylor JB, Goldman EH, Hepler JR. 2001. RGS14 is a bifunctional regulator of G alpha(i/o) activity that exists in multiple populations in brain. J Neurochem 79:941-949.
13. Holmseth S, Dehnes Y, Huang YH, Follin-Arbelet VV, Grutle NJ, Mylonakou MN, Plachez C, Zhou Y, Furness DN, Bergles DE, Lehre KP, Danbolt NC. 2012. The density of EAAC1 (EAAT3) glutamate transporters expressed by neurons in the mammalian CNS. J Neurosci 32:6000-6013.
14. Kiel C, Wohlgemuth S, Rousseau F, Schymkowitz J, Ferkinghoff-Borg J, Wittinghofer F, Serrano L. 2005. Recognizing and defining true Ras binding domains II: in silico prediction based on homology modelling and energy calculations. J Mol Biol 348:759-775.
15. Kimple RJ, De Vries L, Tronchere H, Behe CI, Morris RA, Farquhar MG, Siderovski DP. 2001. RGS12 and RGS14 GoLoco motifs are G alpha(i) interaction sites with guanine nucleotide dissociation inhibitor activity. J Biol Chem 276:29275-29281.
16. Kimple AJ, Bosch DE, Giguere PM, Siderovski DP. 2011. Regulators of G-protein signaling and their Galpha substrates: promises and challenges in their use as drug discovery targets. Pharmacol Rev 63:728-749.
17. Kirino T. 1982. Delayed neuronal death in the gerbil hippocampus following ischemia. Brain Res 239:57-69.
18. Larminie C, Murdock P, Walhin JP, Duckworth M, Blumer KJ, Scheideler MA, Garnier M. 2004. Selective expression of regulators of G-protein signaling (RGS) in the human central nervous system. Mol Brain Res 122:24-34.
19. Lee SE, Simons SB, Heldt SA, Zhao M, Schroeder JP, Vellano CP, Cowan DP, Ramineni S, Yates CK, Feng Y, Smith Y, Sweatt JD, Weinshenker D, Ressler KJ, Dudek SM, Hepler JR. 2010. RGS14 is a natural suppressor of both synaptic plasticity in CA2 neurons and hippocampal-based learning and memory. Proc Natl Acad Sci U S A 107:16994-16998.
20. Lein ES, Callaway EM, Albright TD, Gage FH. 2005. Redefining the boundaries of the hippocampal CA2 subfield in the mouse using gene expression and 3-dimensional reconstruction. J Comp Neurol 485:1-10.
21. Lein ES, Hawrylycz MJ, Ao N, Ayres M, Bensinger A, Bernard A, Boe AF, Boguski MS, Brockway KS, Byrnes EJ, Chen L, Chen L, Chen TM, Chin MC, Chong J, Crook BE, Czaplinska A, Dang CN, Datta S, Dee NR, Desaki AL, Desta T, Diep E, Dolbeare TA, Donelan MJ, Dong HW, Dougherty JG, Duncan BJ, Ebbert AJ, Eichele G, Estin LK, Faber C, Facer BA, Fields R, Fischer SR, Fliss TP, Frensley C, Gates SN, Glattfelder KJ, Halverson KR, Hart MR, Hohmann JG, Howell MP, Jeung DP, Johnson RA, Karr PT, Kawal R, Kidney JM, Knapik RH, Kuan CL, Lake JH, Laramee AR, Larsen KD, Lau C, Lemon TA, Liang AJ, Liu Y, Luong LT, Michaels J, Morgan JJ, Morgan RJ, Mortrud MT, Mosqueda NF, Ng LL, Ng R, Orta GJ, Overly CC, Pak TH, Parry SE, Pathak SD, Pearson OC, Puchalski RB, Riley ZL, Rockett HR, Rowland SA, Royall JJ, Ruiz MJ, Sarno NR, Schaffnit K, Shapovalova NV, Sivisay T, Slaughterbeck CR, Smith SC, Smith KA, Smith BI, Sodt AJ, Stewart NN, Stumpf KR, Sunkin SM, Sutram M, Tam A, Teemer CD, Thaller C, Thompson CL, Varnam LR, Visel A, Whitlock RM, Wohnoutka PE, Wolkey CK, Wong VY, Wood M, Yaylaoglu MB, Young RC, Youngstrom BL, Yuan XF, Zhang B, Zwingman TA, Jones AR. 2007. Genome-wide atlas of gene expression in the adult mouse brain. Nature 445:168-176.
22. Lopez-Aranda MF, Acevedo MJ, Carballo FJ, Gutierrez A, Khan ZU. 2006. Localization of the GoLoco motif carrier regulator of G-protein signalling 12 and 14 proteins in monkey and rat brain. Eur J Neurosci 23:2971-2982.
23. Manning CF, Bundros AM, Trimmer JS. 2012. Benefits and pitfalls of secondary antibodies: why choosing the right secondary is of primary importance. PloS one 7:e38313.
24. Mittal V, Linder ME. 2004. The RGS14 GoLoco domain discriminates among G alpha(i) isoforms. J Biol Chem 279:46772-46778.
25. Mural RJ, Adams MD, Myers EW, Smith HO, Miklos GL, Wides R, Halpern A, Li PW, Sutton GG, Nadeau J, Salzberg SL, Holt RA, Kodira CD, Lu F, Chen L, Deng Z, Evangelista CC, Gan W, Heiman TJ, Li J, Li Z, Merkulov GV, Milshina NV, Naik AK, Qi R, Shue BC, Wang A, Wang J, Wang X, Yan X, Ye J, Yooseph S, Zhao Q, Zheng L, Zhu SC, Biddick K, Bolanos R, Delcher AL, Dew IM, Fasulo D, Flanigan MJ, Huson DH, Kravitz SA, Miller JR, Mobarry CM, Reinert K, Remington KA, Zhang Q, Zheng XH, Nusskern DR, Lai Z, Lei Y, Zhong W, Yao A, Guan P, Ji RR, Gu Z, Wang ZY, Zhong F, Xiao C, Chiang CC, Yandell M, Wortman JR, Amanatides PG, Hladun SL, Pratts EC, Johnson JE, Dodson KL, Woodford KJ, Evans CA, Gropman B, Rusch DB, Venter E, Wang M, Smith TJ, Houck JT, Tompkins DE, Haynes C, Jacob D, Chin SH, Allen DR, Dahlke CE, Sanders R, Li K, Liu X, Levitsky AA, Majoros WH, Chen Q, Xia AC, Lopez JR, Donnelly MT, Newman MH, Glodek A, Kraft CL, Nodell M, Ali F, An HJ, Baldwin-Pitts D, Beeson KY, Cai S, Carnes M, Carver A, Caulk PM, Center A, Chen YH, Cheng ML, Coyne MD, Crowder M, Danaher S, Davenport LB, Desilets R, Dietz SM, Doup L, Dullaghan P, Ferriera S, Fosler CR, Gire HC, Gluecksmann A, Gocayne JD, Gray J, Hart B, Haynes J, Hoover J, Howland T, Ibegwam C, Jalali M, Johns D, Kline L, Ma DS, MacCawley S, Magoon A, Mann F, May D, McIntosh TC, Mehta S, Moy L, Moy MC, Murphy BJ, Murphy SD, Nelson KA, Nuri Z, Parker KA, Prudhomme AC, Puri VN, Qureshi H, Raley JC, Reardon MS, Regier MA, Rogers YH, Romblad DL, Schutz J, Scott JL, Scott R, Sitter CD, Smallwood M, Sprague AC, Stewart E, Strong RV, Suh E, Sylvester K, Thomas R, Tint NN, Tsonis C, Wang G, Wang G, Williams MS, Williams SM, Windsor SM, Wolfe K, Wu MM, Zaveri J, Chaturvedi K, Gabrielian AE, Ke Z, Sun J, Subramanian G, Venter JC, Pfannkoch CM, Barnstead M, Stephenson LD. 2002. A comparison of whole-genome shotgun-derived mouse chromosome 16 and the human genome. Science 296:1661-1671.
26. Oner SS, Maher EM, Breton B, Bouvier M, Blumer JB. 2010. Receptor-regulated interaction of activator of G-protein signaling-4 and Galphai. J Biol Chem 285:20588-20594.
27. Parker CC, Sokoloff G, Cheng R, Palmer AA. 2012. Genome-wide association for fear conditioning in an advanced intercross mouse line. Behav Genet 42:437-448.
28. Sadowski M, Wisniewski HM, Jakubowska-Sadowska K, Tarnawski M, Lazarewicz JW, Mossakowski MJ. 1999. Pattern of neuronal loss in the rat hippocampus following experimental cardiac arrest-induced ischemia. J Neurol Sci 168:13-20.
29. Scorza CA, Araujo BH, Leite LA, Torres LB, Otalora LF, Oliveira MS, Garrido-Sanabria ER, Cavalheiro EA. 2011. Morphological and electrophysiological properties of pyramidal-like neurons in the stratum oriens of Cornu ammonis 1 and Cornu ammonis 2 area of Proechimys. Neuroscience 177:252-268.
30. Shu FJ, Ramineni S, Amyot W, Hepler JR. 2007. Selective interactions between Gi alpha 1 and Gi alpha 3 and the GoLoco/GPR domain of RGS14 influence its dynamic subcellular localization. Cell Signal 19:163-176.
31. Shu FJ, Ramineni S, Hepler JR. 2010. RGS14 is a multifunctional scaffold that integrates G protein and Ras/Raf MAPkinase signalling pathways. Cell Signal 22:366-376.
32. Sloviter RS. 1991. Permanently altered hippocampal structure, excitability, and inhibition after experimental status epilepticus in the rat: the "dormant basket cell" hypothesis and its possible relevance to temporal lobe epilepsy. Hippocampus 1:41-66.
33. Snow BE, Antonio L, Suggs S, Gutstein HB, Siderovski DP. 1997. Molecular cloning and expression analysis of rat Rgs12 and Rgs14. Biochem Biophys Res Commun 233:770-777.
34. Traver S, Bidot C, Spassky N, Baltauss T, de Tand MF, Thomas JL, Zalc B, Janoueix-Lerosey I, de Gunzburg J. 2000. RGS14 is a novel Rap effector that preferentially regulates the GTPase activity of G alpha(o). Biochem J 350:19-29.
35. Vellano CP, Lee SE, Dudek SM, Hepler JR. 2011. RGS14 at the interface of hippocampal signaling and synaptic plasticity. Trends Pharmacol Sci 32:666-674.
36. Vellano CP, Brown NE, Blumer JB, Hepler JR. 2013. Assembly and function of the regulator of G protein signaling 14 (RGS14){middle dot}H-Ras signaling complex in live cells are regulated by Galphai1 and Galphai-linked G protein-coupled receptors. J Biol Chem 288:3620-3631.
37. Wilson DA, Rennaker RL. 2010. Cortical activity evoked by odors. In: Menini A, editor. The neurobiology of olfaction. Boca Raton, FL: CRC Press.
38. Wilson DA, Sullivan RM. 2011. Cortical processing of odor objects. Neuron 72:506-519.
39. Zhao M, Choi Y-S, Obrietan K, Dudek SM. 2007. Synaptic plasticity (and the lack thereof) in hippocampal CA2 neurons. J Neurosci 27:12025-12032.