Global Analysis of Neuronal Phosphoproteome Regulation by Chondroitin Sulfate Proteoglycans

PLoS ONE

Volumn 8, Issue 3, 2013, Pages

  Yu, Panpan ^a   Pisitkun, Trairak ^a   Wang, Guanghui ^a   Wang, Rong ^b   Katagiri, Yasuhiro ^a   Gucek, Marjan ^a   Knepper, Mark A ^a   Geller, Herbert M ^a  

^a NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

^b CENTER FOR BIOLOGICS EVALUATION AND RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COFILIN; GLYCOGEN SYNTHASE KINASE 3BETA; NUCLEIC ACID BINDING PROTEIN; PHOSPHOPEPTIDE; PROTEOCHONDROITIN SULFATE; SEMAPHORIN;

ANIMAL CELL; ARTICLE; AXON GUIDANCE; CADHERIN SIGNALING PATHWAY; CHEMICAL LABELING; CONTROLLED STUDY; EPIDERMAL GROWTH FACTOR RECEPTOR SIGNALING PATHWAY; FRACTIONATION; GRANULE CELL; IMMOBILIZED METAL AFFINITY CHROMATOGRAPHY; INTEGRIN SIGNALING PATHWAY; ISOBARIC TAGS FOR RELATIVE AND ABSOLUTE QUANTITATION LABELING; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; MOUSE; NERVE CELL; NERVE FIBER GROWTH; NERVOUS SYSTEM FUNCTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHOSPHOPROTEOMICS; POSTTRANSCRIPTIONAL CONTROL; PROTEIN PHOSPHORYLATION; PROTEOMICS; SIGNAL TRANSDUCTION; STRONG CATION EXCHANGE CHROMATOGRAPHY FRACTIONATION; SYNAPSE VESICLE TRAFFICKING; TRANSCRIPTION REGULATION;

ACTIN DEPOLYMERIZING FACTORS; ANIMALS; BLOTTING, WESTERN; CHONDROITIN SULFATE PROTEOGLYCANS; CHROMATOGRAPHY, AFFINITY; CHROMATOGRAPHY, ION EXCHANGE; CHROMATOGRAPHY, LIQUID; COMPUTATIONAL BIOLOGY; EXTRACELLULAR MATRIX; MICE; NEURONS; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEOMICS; SIGNAL TRANSDUCTION; TANDEM MASS SPECTROMETRY;

EID: 84875058793     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0059285     Document Type: Article

References (45)

1. Silver J, Miller JH, (2004) Regeneration beyond the glial scar. Nat Rev Neurosci 5: 146-156.
2. Snow DM, Brown EM, Letourneau PC, (1996) Growth cone behavior in the presence of soluble chondroitin sulfate proteoglycan (CSPG), compared to behavior on CSPG bound to laminin or fibronectin. Int J Dev Neurosci 14: 331-349.
3. Yu P, Santiago LY, Katagiri Y, Geller HM, (2012) Myosin II activity regulates neurite outgrowth and guidance in response to chondroitin sulfate proteoglycans. J Neurochem 120: 1117-1128.
4. Inatani M, Honjo M, Otori Y, Oohira A, Kido N, et al. (2001) Inhibitory effects of neurocan and phosphacan on neurite outgrowth from retinal ganglion cells in culture. Invest Ophthalmol Vis Sci 42: 1930-1938.
5. Bradbury EJ, Moon LD, Popat RJ, King VR, Bennett GS, et al. (2002) Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature 416: 636-640.
6. Garcia-Alias G, Barkhuysen S, Buckle M, Fawcett JW, (2009) Chondroitinase ABC treatment opens a window of opportunity for task-specific rehabilitation. Nat Neurosci 12: 1145-1151.
7. Massey JM, Hubscher CH, Wagoner MR, Decker JA, Amps J, et al. (2006) Chondroitinase ABC digestion of the perineuronal net promotes functional collateral sprouting in the cuneate nucleus after cervical spinal cord injury. J Neurosci 26: 4406-4414.
8. Wang H, Katagiri Y, McCann TE, Unsworth E, Goldsmith P, et al. (2008) Chondroitin-4-sulfation negatively regulates axonal guidance and growth. J Cell Sci 121: 3083-3091.
9. Laabs TL, Wang H, Katagiri Y, McCann T, Fawcett JW, et al. (2007) Inhibiting glycosaminoglycan chain polymerization decreases the inhibitory activity of astrocyte-derived chondroitin sulfate proteoglycans. J Neurosci 27: 14494-14501.
10. Ughrin YM, Chen ZJ, Levine JM, (2003) Multiple regions of the NG2 proteoglycan inhibit neurite growth and induce growth cone collapse. J Neurosci 23: 175-186.
11. Shen Y, Tenney AP, Busch SA, Horn KP, Cuascut FX, et al. (2009) PTPsigma is a receptor for chondroitin sulfate proteoglycan, an inhibitor of neural regeneration. Science 326: 592-596.
12. Fry EJ, Chagnon MJ, Lopez-Vales R, Tremblay ML, David S, (2010) Corticospinal tract regeneration after spinal cord injury in receptor protein tyrosine phosphatase sigma deficient mice. Glia 58: 423-433.
13. Fisher D, Xing B, Dill J, Li H, Hoang HH, et al. (2011) Leukocyte common antigen-related phosphatase is a functional receptor for chondroitin sulfate proteoglycan axon growth inhibitors. J Neurosci 31: 14051-14066.
14. Dickendesher TL, Baldwin KT, Mironova YA, Koriyama Y, Raiker SJ, et al. (2012) NgR1 and NgR3 are receptors for chondroitin sulfate proteoglycans. Nat Neurosci 15: 703-712.
15. Sivasankaran R, Pei J, Wang KC, Zhang YP, Shields CB, et al. (2004) PKC mediates inhibitory effects of myelin and chondroitin sulfate proteoglycans on axonal regeneration. Nat Neurosci 7: 261-268.
16. Monnier PP, Sierra A, Schwab JM, Henke-Fahle S, Mueller BK, (2003) The Rho/ROCK pathway mediates neurite growth-inhibitory activity associated with the chondroitin sulfate proteoglycans of the CNS glial scar. Mol Cell Neurosci 22: 319-330.
17. Fu Q, Hue J, Li S, (2007) Nonsteroidal anti-inflammatory drugs promote axon regeneration via RhoA inhibition. J Neurosci 27: 4154-4164.
18. Dill J, Wang H, Zhou F, Li S, (2008) Inactivation of glycogen synthase kinase 3 promotes axonal growth and recovery in the CNS. J Neurosci 28: 8914-8928.
19. Ross PL, Huang YN, Marchese JN, Williamson B, Parker K, et al. (2004) Multiplexed protein quantitation in Saccharomyces cerevisiae using amine-reactive isobaric tagging reagents. Mol Cell Proteomics 3: 1154-1169.
20. Phanstiel D, Unwin R, McAlister GC, Coon JJ, (2009) Peptide quantification using 8-plex isobaric tags and electron transfer dissociation tandem mass spectrometry. Anal Chem 81: 1693-1698.
21. Schwartz D, Gygi SP, (2005) An iterative statistical approach to the identification of protein phosphorylation motifs from large-scale data sets. Nat Biotechnol 23: 1391-1398.
22. Malik R, Nigg EA, Korner R, (2008) Comparative conservation analysis of the human mitotic phosphoproteome. Bioinformatics 24: 1426-1432.
23. Zhao B, Pisitkun T, Hoffert JD, Knepper MA, Saeed F (2012) CPhos: A Program to Calculate and Visualize Evolutionarily Conserved Functional Phosphorylation Sites. Proteomics.
24. Tan CL, Kwok JC, Patani R, Ffrench-Constant C, Chandran S, et al. (2011) Integrin activation promotes axon growth on inhibitory chondroitin sulfate proteoglycans by enhancing integrin signaling. J Neurosci 31: 6289-6295.
25. Hsieh SH, Ferraro GB, Fournier AE, (2006) Myelin-associated inhibitors regulate cofilin phosphorylation and neuronal inhibition through LIM kinase and Slingshot phosphatase. J Neurosci 26: 1006-1015.
26. Kelly TA, Katagiri Y, Vartanian KB, Kumar P, Chen, II, et al, (2010) Localized alteration of microtubule polymerization in response to guidance cues. J Neurosci Res 88: 3024-3033.
27. Hlavanda E, Klement E, Kokai E, Kovacs J, Vincze O, et al. (2007) Phosphorylation blocks the activity of tubulin polymerization-promoting protein (TPPP): identification of sites targeted by different kinases. J Biol Chem 282: 29531-29539.
28. Fourest-Lieuvin A, Peris L, Gache V, Garcia-Saez I, Juillan-Binard C, et al. (2006) Microtubule regulation in mitosis: tubulin phosphorylation by the cyclin-dependent kinase Cdk1. Mol Biol Cell 17: 1041-1050.
29. Calamia V, Fernandez-Puente P, Mateos J, Lourido L, Rocha B, et al. (2012) Pharmacoproteomic study of three different chondroitin sulfate compounds on intracellular and extracellular human chondrocyte proteomes. Mol Cell Proteomics 11: M111 013417.
30. Kantor DB, Chivatakarn O, Peer KL, Oster SF, Inatani M, et al. (2004) Semaphorin 5A is a bifunctional axon guidance cue regulated by heparan and chondroitin sulfate proteoglycans. Neuron 44: 961-975.
31. Snow DM, Letourneau PC, (1992) Neurite outgrowth on a step gradient of chondroitin sulfate proteoglycan (CS-PG). J Neurobiol 23: 322-336.
32. Letourneau PC, Condic ML, Snow DM, (1994) Interactions of developing neurons with the extracellular matrix. J Neurosci 14: 915-928.
33. Kwok JC, Dick G, Wang D, Fawcett JW, (2011) Extracellular matrix and perineuronal nets in CNS repair. Dev Neurobiol 71: 1073-1089.
34. Sharma K, Selzer ME, Li S (2012) Scar-mediated inhibition and CSPG receptors in the CNS. Exp Neurol.
35. Balsamo J, Ernst H, Zanin MK, Hoffman S, Lilien J, (1995) The interaction of the retina cell surface N-acetylgalactosaminylphosphotransferase with an endogenous proteoglycan ligand results in inhibition of cadherin-mediated adhesion. J Cell Biol 129: 1391-1401.
36. Li H, Leung TC, Hoffman S, Balsamo J, Lilien J, (2000) Coordinate regulation of cadherin and integrin function by the chondroitin sulfate proteoglycan neurocan. J Cell Biol 149: 1275-1288.
37. Rush J, Moritz A, Lee KA, Guo A, Goss VL, et al. (2005) Immunoaffinity profiling of tyrosine phosphorylation in cancer cells. Nat Biotechnol 23: 94-101.
38. De Wit J, De Winter F, Klooster J, Verhaagen J, (2005) Semaphorin 3A displays a punctate distribution on the surface of neuronal cells and interacts with proteoglycans in the extracellular matrix. Mol Cell Neurosci 29: 40-55.
39. Ow SY, Salim M, Noirel J, Evans C, Rehman I, et al. (2009) iTRAQ underestimation in simple and complex mixtures: "the good, the bad and the ugly". J Proteome Res 8: 5347-5355.
40. Karp NA, Huber W, Sadowski PG, Charles PD, Hester SV, et al. (2010) Addressing accuracy and precision issues in iTRAQ quantitation. Mol Cell Proteomics 9: 1885-1897.
41. Keshamouni VG, Michailidis G, Grasso CS, Anthwal S, Strahler JR, et al. (2006) Differential protein expression profiling by iTRAQ-2DLC-MS/MS of lung cancer cells undergoing epithelial-mesenchymal transition reveals a migratory/invasive phenotype. J Proteome Res 5: 1143-1154.
42. Hoffert JD, Pisitkun T, Saeed F, Song JH, Chou CL, et al. (2012) Dynamics of the G protein-coupled vasopressin V2 receptor signaling network revealed by quantitative phosphoproteomics. Mol Cell Proteomics 11: M111 014613.
43. Boekhorst J, Boersema PJ, Tops BB, van Breukelen B, Heck AJ, et al. (2011) Evaluating experimental bias and completeness in comparative phosphoproteomics analysis. PLoS One 6: e23276.
44. Saeed F, Pisitkun T, Hoffert JD, Wang G, Gucek M, et al. (2012) An Efficient Dynamic Programming Algorithm for Phosphorylation Site Assignment of Large-Scale Mass Spectrometry Data. International Workshop on Computational Proteomics, proceedings of IEEE International Conference on Bioinformatics and Biomedicine (BIBM).
45. Villen J, Beausoleil SA, Gerber SA, Gygi SP, (2007) Large-scale phosphorylation analysis of mouse liver. Proc Natl Acad Sci U S A 104: 1488-1493.