Activity-dependent SUMOylation of the Brain-specific Scaffolding Protein GISP

Overview

Journal Biochem Biophys Res Commun

Publisher Elsevier

Specialty Biochemistry

Date 2011 May 28

PMID 21616059

Citations 13

Authors

Sriharsha Kantamneni

Kevin A Wilkinson

Nadia Jaafari

Emi Ashikaga

Daniel Rocca

Philip Rubin

Susan C Jacobs

Atsushi Nishimune

Jeremy M Henley

Affiliations

Soon will be listed here.

Abstract

G-protein coupled receptor interacting scaffold protein (GISP) is a multi-domain, brain-specific protein derived from the A-kinase anchoring protein (AKAP)-9 gene. Using yeast two-hybrid screens to identify GISP interacting proteins we isolated the SUMO conjugating enzyme Ubc9. GISP interacts with Ubc9 in vitro, in heterologous cells and in neurons. SUMOylation is a post-translational modification in which the small protein SUMO is covalently conjugated to target proteins, modulating their function. Consistent with its interaction with Ubc9, we show that GISP is SUMOylated by both SUMO-1 and SUMO-2 in both in vitro SUMOylation assays and in mammalian cells. Intriguingly, SUMOylation of GISP in neurons occurs in an activity-dependent manner in response to chemical LTP. These data suggest that GISP is a novel neuronal SUMO substrate whose SUMOylation status is modulated by neuronal activity.

Citing Articles

UBC-9 Acts in GABA Neurons to Control Neuromuscular Signaling in .

Kreyden V, Mawi E, Rush K, Kowalski J Neurosci Insights. 2020; 15:2633105520962792.

PMID: 33089216 PMC: 7543134. DOI: 10.1177/2633105520962792.

Response: Commentary: Analysis of SUMO1-conjugation at synapses.

Daniel J, Cooper B, Palvimo J, Zhang F, Brose N, Tirard M Front Cell Neurosci. 2018; 12:117.

PMID: 29766991 PMC: 5938361. DOI: 10.3389/fncel.2018.00117.

Analysis of SUMO1-conjugation at synapses.

Daniel J, Cooper B, Palvimo J, Zhang F, Brose N, Tirard M Elife. 2017; 6.

PMID: 28598330 PMC: 5493437. DOI: 10.7554/eLife.26338.

Dynamic Arc SUMOylation and Selective Interaction with F-Actin-Binding Protein Drebrin A in LTP Consolidation .

Nair R, Patil S, Tiron A, Kanhema T, Panja D, Schiro L Front Synaptic Neurosci. 2017; 9:8.

PMID: 28553222 PMC: 5426369. DOI: 10.3389/fnsyn.2017.00008.

SUMOylation of Argonaute-2 regulates RNA interference activity.

Josa-Prado F, Henley J, Wilkinson K Biochem Biophys Res Commun. 2015; 464(4):1066-1071.

PMID: 26188511 PMC: 4624959. DOI: 10.1016/j.bbrc.2015.07.073.

References

Lu W, Man H, Ju W, Trimble W, MacDonald J, Wang Y . Activation of synaptic NMDA receptors induces membrane insertion of new AMPA receptors and LTP in cultured hippocampal neurons. Neuron. 2001; 29(1):243-54. DOI: 10.1016/s0896-6273(01)00194-5. View

Xu J, He Y, Qiang B, Yuan J, Peng X, Pan X . A novel method for high accuracy sumoylation site prediction from protein sequences. BMC Bioinformatics. 2008; 9:8. PMC: 2245905. DOI: 10.1186/1471-2105-9-8. View

Martin S, Nishimune A, Mellor J, Henley J . SUMOylation regulates kainate-receptor-mediated synaptic transmission. Nature. 2007; 447(7142):321-5. PMC: 3310901. DOI: 10.1038/nature05736. View

Wilkinson K, Henley J . Analysis of metabotropic glutamate receptor 7 as a potential substrate for SUMOylation. Neurosci Lett. 2011; 491(3):181-6. PMC: 3122152. DOI: 10.1016/j.neulet.2011.01.032. View

Kantamneni S, Holman D, Wilkinson K, Nishimune A, Henley J . GISP increases neurotransmitter receptor stability by down-regulating ESCRT-mediated lysosomal degradation. Neurosci Lett. 2009; 452(2):106-10. PMC: 3310152. DOI: 10.1016/j.neulet.2009.01.011. View

Nishimune A, Isaac J, Molnar E, Noel J, Nash S, Tagaya M . NSF binding to GluR2 regulates synaptic transmission. Neuron. 1998; 21(1):87-97. DOI: 10.1016/s0896-6273(00)80517-6. View

Bouschet T, Martin S, Kanamarlapudi V, Mundell S, Henley J . The calcium-sensing receptor changes cell shape via a beta-arrestin-1 ARNO ARF6 ELMO protein network. J Cell Sci. 2007; 120(Pt 15):2489-97. PMC: 3324777. DOI: 10.1242/jcs.03469. View

Kantamneni S, Correa S, Hodgkinson G, Meyer G, Vinh N, Henley J . GISP: a novel brain-specific protein that promotes surface expression and function of GABA(B) receptors. J Neurochem. 2007; 100(4):1003-17. PMC: 3315443. DOI: 10.1111/j.1471-4159.2006.04271.x. View

Babst M . A protein's final ESCRT. Traffic. 2004; 6(1):2-9. DOI: 10.1111/j.1600-0854.2004.00246.x. View

10.

Williams R, Urbe S . The emerging shape of the ESCRT machinery. Nat Rev Mol Cell Biol. 2007; 8(5):355-68. DOI: 10.1038/nrm2162. View

11.

Park M, Penick E, Edwards J, Kauer J, Ehlers M . Recycling endosomes supply AMPA receptors for LTP. Science. 2004; 305(5692):1972-5. DOI: 10.1126/science.1102026. View

12.

Anderson D, Wilkinson K, Henley J . Protein SUMOylation in neuropathological conditions. Drug News Perspect. 2009; 22(5):255-65. PMC: 3309023. DOI: 10.1358/dnp.2009.22.5.1378636. View

13.

Wilkinson K, Henley J . Mechanisms, regulation and consequences of protein SUMOylation. Biochem J. 2010; 428(2):133-45. PMC: 3310159. DOI: 10.1042/BJ20100158. View

14.

Feligioni M, Nishimune A, Henley J . Protein SUMOylation modulates calcium influx and glutamate release from presynaptic terminals. Eur J Neurosci. 2009; 29(7):1348-56. PMC: 3309032. DOI: 10.1111/j.1460-9568.2009.06692.x. View

15.

Kantamneni S, Holman D, Wilkinson K, Correa S, Feligioni M, Ogden S . GISP binding to TSG101 increases GABA receptor stability by down-regulating ESCRT-mediated lysosomal degradation. J Neurochem. 2008; 107(1):86-95. PMC: 3314514. DOI: 10.1111/j.1471-4159.2008.05580.x. View

16.

Lu H, Liu B, You S, Xue Q, Zhang F, Cheng J . The activity-dependent stimuli increase SUMO modification in SHSY5Y cells. Biochem Biophys Res Commun. 2009; 390(3):872-6. DOI: 10.1016/j.bbrc.2009.10.065. View

17.

Rodriguez M, Dargemont C, Hay R . SUMO-1 conjugation in vivo requires both a consensus modification motif and nuclear targeting. J Biol Chem. 2001; 276(16):12654-9. DOI: 10.1074/jbc.M009476200. View

18.

Wilkinson K, Nishimune A, Henley J . Analysis of SUMO-1 modification of neuronal proteins containing consensus SUMOylation motifs. Neurosci Lett. 2008; 436(2):239-44. PMC: 3310158. DOI: 10.1016/j.neulet.2008.03.029. View

19.

Sampson D, Wang M, Matunis M . The small ubiquitin-like modifier-1 (SUMO-1) consensus sequence mediates Ubc9 binding and is essential for SUMO-1 modification. J Biol Chem. 2001; 276(24):21664-9. DOI: 10.1074/jbc.M100006200. View

20.

Uchimura Y, Nakamura M, Sugasawa K, Nakao M, Saitoh H . Overproduction of eukaryotic SUMO-1- and SUMO-2-conjugated proteins in Escherichia coli. Anal Biochem. 2004; 331(1):204-6. DOI: 10.1016/j.ab.2004.04.034. View