In vivo localization and identification of SUMOylated proteins in the brain of His6-HA-SUMO1 knock-in mice

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 51, 2012, Pages 21122-21127

  Tirard, Marilyn ^a   Hsiao, He Hsuan ^b,c   Nikolov, Miroslav ^b,c   Urlaub, Henning ^b,c   Melchior, Frauke ^d   Brose, Nils ^a  

^a MAX PLANCK INSTITUTE OF EXPERIMENTAL MEDICINE   (Germany)

^b MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

^c UNIVERSITY MEDICAL CENTER GÖTTINGEN   (Germany)

^d GERMAN CANCER RESEARCH CENTER   (Germany)

Author keywords

Affinity purification; Synapse

Indexed keywords

HISTIDINE; NUCLEAR RECEPTOR COACTIVATOR; PROTEIN CTIP2; PROTEIN SMCHD1; PROTEIN ZBTB20; SUMO 1 PROTEIN; TRANSCRIPTION INTERMEDIATE FACTOR 1 GAMMA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; BRAIN TISSUE; CONTROLLED STUDY; EXPERIMENTAL MOUSE; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; LAMELLAR BODY; MAMMAL; MOUSE; NEUROCHEMISTRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PURIFICATION; SUMOYLATION; VALIDATION PROCESS;

ANIMALS; BRAIN; CELL NUCLEUS; CELLS, CULTURED; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MASS SPECTROMETRY; MICE; MICE, TRANSGENIC; MODELS, BIOLOGICAL; NEURONS; PROTEIN BINDING; SMALL UBIQUITIN-RELATED MODIFIER PROTEINS; SUMO-1 PROTEIN;

EUKARYOTA; MAMMALIA; MUS;

EID: 84871371484     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1215366110     Document Type: Article

References (36)

1. Geiss-Friedlander R, Melchior F (2007) Concepts in sumoylation: A decade on. Nat Rev Mol Cell Biol 8(12):947-956.
2. Gareau JR, Lima CD (2010) The SUMO pathway: Emerging mechanisms that shape specificity, conjugation and recognition. Nat Rev Mol Cell Biol 11(12):861-871.
3. Sarge KD, Park-Sarge OK (2011) SUMO and its role in human diseases. Int Rev Cell Mol Biol 288:167-183.
4. Wilkinson KA, Nakamura Y, Henley JM (2010) Targets and consequences of protein SUMOylation in neurons. Brain Res Brain Res Rev 64(1):195-212.
5. Kantamneni S, et al. (2011) Activity-dependent SUMOylation of the brain-specific scaffolding protein GISP. Biochem Biophys Res Commun 409(4):657-662.
6. Craig TJ, et al. (2012) Homeostatic synaptic scaling is regulated by protein SUMOylation. J Biol Chem 287(27):22781-22788.
7. Hay RT (2005) SUMO: A history of modification. Mol Cell 18(1):1-12.
8. Seeler JS, Dejean A (2003) Nuclear and unclear functions of SUMO. Nat Rev Mol Cell Biol 4(9):690-699.
9. Owerbach D, McKay EM, Yeh ET, Gabbay KH, Bohren KM (2005) A proline-90 residue unique to SUMO-4 prevents maturation and sumoylation. Biochem Biophys Res Commun 337(2):517-520.
10. Bayer P, et al. (1998) Structure determination of the small ubiquitin-related modifier SUMO-1. J Mol Biol 280(2):275-286.
11. Bayona JC, et al. (2011) SUMOylation pathway in Trypanosoma cruzi : Functional characterization and proteomic analysis of target proteins. Mol Cell Proteomics, 10.1074/mcp.M110.007369.
12. Braun L, et al. (2009) The small ubiquitin-like modifier (SUMO)-conjugating system of Toxoplasma gondii. Int J Parasitol 39(1):81-90.
13. Park HC, et al. (2011) Identification and molecular properties of SUMO-binding proteins in Arabidopsis. Mol Cells 32(2):143-151.
14. Rosas-Acosta G, Russell WK, Deyrieux A, Russell DH, Wilson VG (2005) A universal strategy for proteomic studies of SUMO and other ubiquitin-like modifiers. Mol Cell Proteomics 4(1):56-72.
15. Vertegaal AC, et al. (2006) Distinct and overlapping sets of SUMO-1 and SUMO-2 target proteins revealed by quantitative proteomics. Mol Cell Proteomics 5(12):2298-2310.
16. Nie M, Xie Y, Loo JA, Courey AJ (2009) Genetic and proteomic evidence for roles of Drosophila SUMO in cell cycle control, Ras signaling, and early pattern formation. PLoS ONE 4(6):e5905.
17. Tatham MH, Matic I, Mann M, Hay RT (2011) Comparative proteomic analysis identifies a role for SUMO in protein quality control. Sci Signal 4(178):rs4.
18. Panse VG, Hardeland U, Werner T, Kuster B, Hurt E (2004) A proteome-wide approach identifies sumoylated substrate proteins in yeast. J Biol Chem 279(40):41346-41351.
19. Miller MJ, Barrett-Wilt GA, Hua Z, Vierstra RD (2010) Proteomic analyses identify a diverse array of nuclear processes affected by small ubiquitin-like modifier conjugation in Arabidopsis. Proc Natl Acad Sci USA 107(38):16512-16517.
20. Leach MD, Stead DA, Argo E, Brown AJ (2011) Identification of sumoylation targets, combined with inactivation of SMT3, reveals the impact of sumoylation upon growth, morphology, and stress resistance in the pathogen Candida albicans. Mol Biol Cell 22 (5):687-702.
21. Kaminsky R, et al. (2009) SUMO regulates the assembly and function of a cytoplasmic intermediate filament protein in C. elegans. Dev Cell 17(5):724-735.
22. Denison C, et al. (2005) A proteomic strategy for gaining insights into protein sumoylation in yeast. Mol Cell Proteomics 4(3):246-254.
23. Hannich JT, et al. (2005) Defining the SUMO-modified proteome by multiple approaches in Saccharomyces cerevisiae. J Biol Chem 280(6):4102-4110.
24. Zhang FP, et al. (2008) Sumo-1 function is dispensable in normal mouse development. Mol Cell Biol 28(17):5381-5390.
25. Hetzer M, Gruss OJ, Mattaj IW (2002) The Ran GTPase as a marker of chromosome position in spindle formation and nuclear envelope assembly. Nat Cell Biol 4(7):E177-E184.
26. Krumova P, et al. (2011) Sumoylation inhibits alpha-synuclein aggregation and toxicity. J Cell Biol 194(1):49-60.
27. Hsiao HH, Meulmeester E, Frank BT, Melchior F, Urlaub H (2009) "ChopNSpice," a mass spectrometric approach that allows identification of endogenous small ubiquitin-like modifier-conjugated peptides. Mol Cell Proteomics 8(12):2664-2675.
28. Mahajan R, Delphin C, Guan T, Gerace L, Melchior F (1997) A small ubiquitin-related polypeptide involved in targeting RanGAP1 to nuclear pore complex protein RanBP2. Cell 88(1):97-107.
29. Riquelme C, Barthel KK, Liu X (2006) SUMO-1 modification of MEF2A regulates its transcriptional activity. J Cell Mol Med 10(1):132-144.
30. Li X, et al. (2007) Role for KAP1 serine 824 phosphorylation and sumoylation/desumoylation switch in regulating KAP1-mediated transcriptional repression. J Biol Chem 282(50):36177-36189.
31. Galisson F, et al. (2011) A novel proteomics approach to identify SUMOylated proteins and their modification sites in human cells. Mol Cell Proteomics, 10.1074/mcp. M110.004796.
32. Long J, Zuo D, Park M(2005) Pc2-mediated sumoylation of Smad-interacting protein 1 attenuates transcriptional repression of E-cadherin. J Biol Chem 280(42):35477-35489.
33. Kuwata T, Nakamura T (2008) BCL11A is a SUMOylated protein and recruits SUMOconjugation enzymes in its nuclear body. Genes Cells 13(9):931-940.
34. Johnson ES, Blobel G (1999) Cell cycle-regulated attachment of the ubiquitin-related protein SUMO to the yeast septins. J Cell Biol 147(5):981-994.
35. Martin SF, Tatham MH, Hay RT, Samuel ID (2008) Quantitative analysis of multi-protein interactions using FRET: Application to the SUMO pathway. Protein Sci 17(4):777-784.
36. Matic I, et al. (2010) Site-specific identification of SUMO-2 targets in cells reveals an inverted SUMOylation motif and a hydrophobic cluster SUMOylation motif. Mol Cell 39(4):641-652.