Analysis of Cdk5-related phosphoproteomics in growth cones

Journal of Molecular Neuroscience

Volumn 52, Issue 3, 2014, Pages 384-391

  Wen, Zheng ^a,b   Gao, Caiyun ^a,b   Wang, Xuemin ^c   Shi, Jing ^a,b   Tian, Bo ^a,b  

^a HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^b BEIJING UNIVERSITY OF POSTS AND TELECOMMUNICATIONS   (China)

^c SOUTHERN MEDICAL UNIVERSITY   (China)

Author keywords

Bioinformatics; Cyclin dependent kinase 5; Gene ontology; Mass spectrometry; Neuron axonal growth cone; Phosphoproteome

Indexed keywords

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANIMALS; CYCLIN-DEPENDENT KINASE 5; GROWTH CONES; MICE; MICE, INBRED C57BL; MOLECULAR SEQUENCE DATA; PHOSPHORYLATION; PROTEOME;

EID: 84894302619     PISSN: 08958696     EISSN: 15591166     Source Type: Journal    
DOI: 10.1007/s12031-013-0162-x     Document Type: Article

References (47)

1. Bian F, Nath R, Sobocinski G, Booher RN, Lipinski WJ, Callahan MJ et al (2002) Axonopathy, tau abnormalities, and dyskinesia, but no neurofibrillary tangles in p25-transgenic mice. J Comp Neurol 446(3):257-266
2. Burden-Gulley SM, Pendergast M, Lemmon V (1997) The role of cell adhesion molecule L1 in axonal extension, growth cone motility, and signal transduction. Cell Tissue Res 290(2):415-422
3. Calkins DJ, Horner PJ (2012) The cell and molecular biology of glaucoma: axonopathy and the brain. Investig Ophthalmol Vis Sci 53(5):2482-2484
4. Chi Y, Welcker M, Hizli AA, Posakony JJ, Aebersold R, Clurman BE (2008) Identification of CDK2 substrates in human cell lysates. Genome Biol 9(10):R149
5. Dent EW, Gertler FB (2003) Cytoskeletal dynamics and transport in growth cone motility and axon guidance. Neuron 40(2):209-227
6. Dent, E W, Gupton S L, Gertler,F B (2011) The growth cone cytoskeleton in axon outgrowth and guidance. Cold Spring Harb Perspect Biol. 3(3).
7. Dhavan R, Tsai LH (2001) A decade of CDK5. Nat Rev Mol Cell Biol 2(10):749-759
8. Engelhardt M, Vorwald S., Sobotzik J. M, Bennett V and Schultz C (2012) Ankyrin-B structurally defines terminal microdomains of peripheral somatosensory axons. Brain Struct Funct.
9. Estrada-Bernal A, Sanford SD, Sosa LJ, Simon GC, Hansen KC, Pfenninger KH (2012) Functional complexity of the axonal growth cone: a proteomic analysis. PLoS One 7(2):e31858
10. Gallo G, Letourneau PC (2004) Regulation of growth cone actin filaments by guidance cues. J Neurobiol 58(1):92-102
11. Garbe DS, Das A, Dubreuil RR, Bashaw GJ (2007) Beta-spectrin functions independently of ankyrin to regulate the establishment and maintenance of axon connections in the drosophila embryonic CNS. Development 134(2):273-284
12. Gorg A, Weiss W, Dunn MJ (2004) Current two-dimensional electrophoresis technology for proteomics. Proteomics 4(12):3665-3685
13. Hahn CM, Kleinholz H, Koester MP, Grieser S, Thelen K, Pollerberg GE (2005) Role of cyclin-dependent kinase 5 and its activator P35 in local axon and growth cone stabilization. Neuroscience 134(2):449-465
14. Hasan N, Wu HF, Li YH, Nawaz M (2010) Two-step on-particle ionization/enrichment via a washing- and separation-free approach: multifunctional TiO2 nanoparticles as desalting, accelerating, and affinity probes for microwave-assisted tryptic digestion of phosphoproteins in ESI-MS and MALDI-MS: comparison with microscale TiO2. Anal Bioanal Chem 396(8):2909-2919
15. Hayashi K, Pan Y, Shu H, Ohshima T, Kansy JW, White CL 3rd et al (2006) Phosphorylation of the tubulin-binding protein, stathmin, by Cdk5 and MAP kinases in the brain. J Neurochem 99(1):237-250
16. Hornbeck PV, Chabra I, Kornhauser JM, Skrzypek E, Zhang B (2004) PhosphoSite: a bioinformatics resource dedicated to physiological protein phosphorylation. Proteomics 4(6):1551-1561
17. Iwadate Y (2008) Clinical proteomics in cancer research-promises and limitations of current two-dimensional gel electrophoresis. Curr Med Chem 15(23):2393-2400
18. Kawauchi T, Chihama K, Nishimura YV, Nabeshima Y, Hoshino M (2005) MAP1B phosphorylation is differentially regulated by Cdk5/p35, Cdk5/p25, and JNK. Biochem Biophys Res Commun 331(1):50-55
19. Koch I, Schwarz H, Beuchle D, Goellner B, Langegger M, Aberle H (2008) Drosophila ankyrin 2 is required for synaptic stability. Neuron 58(2):210-222
20. Lanier LM, Gertler FB (2000) From Abl to actin: Abl tyrosine kinase and associated proteins in growth cone motility. Curr Opin Neurobiol 10(1):80-87
21. Lemeer S, Kunold E, Klaeger S, Raabe M, Towers MW, Claudes E et al (2012) Phosphorylation site localization in peptides by MALDI MS/MS and the Mascot Delta Score. Anal Bioanal Chem 402(1):249-260
22. Li, J. Y. and Conforti, L (2012) Axonopathy in Huntington's disease. Exp Neurol.
23. Li QR, Ning ZB, Tang JS, Nie S, Zeng R (2009) Effect of peptide-to-TiO2 beads ratio on phosphopeptide enrichment selectivity. J Proteome Res 8(11):5375-5381
24. Lin YC, Yeckel MF, Koleske AJ (2013) Abl2/Arg controls dendritic spine and dendrite arbor stability via distinct cytoskeletal control pathways. J Neurosci 33(5):1846-1857
25. Lowery LA, Van Vactor D (2009) The trip of the tip: understanding the growth cone machinery. Nat Rev Mol Cell Biol 10(5):332-343
26. Loyet KM, Stults JT, Arnott D (2005) Mass spectrometric contributions to the practice of phosphorylation site mapping through 2003: a literature review. Mol Cell Proteomics 4(3):235-245
27. Macek B, Mijakovic I, Olsen JV, Gnad F, Kumar C, Jensen PR et al (2007) The serine/threonine/tyrosine phosphoproteome of the model bacterium Bacillus subtilis. Mol Cell Proteomics 6(4):697-707
28. Meijer L, Borgne A, Mulner O, Chong JP, Blow JJ, Inagaki N et al (1997) Biochemical and cellular effects of roscovitine, a potent and selective inhibitor of the cyclin-dependent kinases cdc2, cdk2 and cdk5. Eur J Biochem 243(1-2):527-536
29. Nikolic M, Chou MM, Lu W, Mayer BJ, Tsai LH (1998) The p35/Cdk5 kinase is a neuron-specific Rac effector that inhibits Pak1 activity. Nature 395(6698):194-198
30. O'Malley KL (2010) The role of axonopathy in Parkinson's disease. Exp Neurobiol 19(3):115-119
31. Obenauer JC (2003) Scansite 2.0: proteome-wide prediction of cell signaling interactions using short sequence motifs. Nucleic Acids Res 31(13):3635-3641
32. Ooashi N, Kamiguchi H (2009) The cell adhesion molecule L1 controls growth cone navigation via ankyrin(B)-dependent modulation of cyclic AMP. Neurosci Res 63(3):224-226
33. Ookata K, Hisanaga S, Sugita M, Okuyama A, Murofushi H, Kitazawa H et al (1997) MAP4 is the in vivo substrate for CDC2 kinase in HeLa cells: identification of an M-phase specific and a cell cycle-independent phosphorylation site in MAP4. Biochemistry 36(50):15873-15883
34. Paglini G, Pigino G, Kunda P, Morfini G, Maccioni R, Quiroga S et al (1998) Evidence for the participation of the neuron-specific CDK5 activator P35 during laminin-enhanced axonal growth. J Neurosci 18(23):9858-9869
35. Pfenninger KH, Ellis L, Johnson MP, Friedman LB, Somlo S (1983) Nerve growth cones isolated from fetal rat brain: subcellular fractionation and characterization. Cell 35(2 Pt 1):573-584
36. Rashid T, Banerjee M, Nikolic M (2001) Phosphorylation of Pak1 by the p35/Cdk5 kinase affects neuronal morphology. J Biol Chem 276(52):49043-49052
37. Sahin B, Hawasli AH, Greene RW, Molkentin JD, Bibb JA (2008) Negative regulation of cyclin-dependent kinase 5 targets by protein kinase C. Eur J Pharmacol 581(3):270-275
38. Saito S, Fujita T, Komiya Y, Igarashi M (1992) Biochemical characterization of nerve growth cones isolated from both fetal and neonatal rat forebrains: the growth cone particle fraction mainly consists of axonal growth cones in both stages. Brain Res Dev Brain Res 65(2):179-184
39. Su SC, Tsai LH (2011) Cyclin-dependent kinases in brain development and disease. Annu Rev Cell Dev Biol 27:465-491
40. Surti TS, Huang L, Jan YN, Jan LY, Cooper EC (2005) Identification by mass spectrometry and functional characterization of two phosphorylation sites of KCNQ2/KCNQ3 channels. Proc Natl Acad Sci U S A 102(49):17828-17833
41. Takano M, Koyama Y, Ito H, Hoshino S, Onogi H, Hagiwara M et al (2004) Regulation of binding of lamin B receptor to chromatin by SR protein kinase and cdc2 kinase in Xenopus egg extracts. J Biol Chem 279(13):13265-13271
42. UniProt C (2010) The Universal Protein Resource (UniProt) in 2010. Nucleic Acids Res 38(Database issue):D142-D148
43. Wills Z, Marr L, Zinn K, Goodman CS, Van Vactor D (1999) Profilin and the Abl tyrosine kinase are required for motor axon outgrowth in the Drosophila embryo. Neuron 22(2):291-299
44. Wisniewski JR, Nagaraj N, Zougman A, Gnad F, Mann M (2010) Brain phosphoproteome obtained by a FASP-based method reveals plasma membrane protein topology. J Proteome Res 9(6):3280-3289
45. Xin X, Wang Y, Ma XM, Rompolas P, Keutmann HT, Mains RE et al (2008) Regulation of kalirin by Cdk5. J Cell Sci 121(Pt 15):2601-2611
46. Xue Y, Liu Z, Cao J, Ma Q, Gao X, Wang Q et al (2011) GPS 2.1: enhanced prediction of kinase-specific phosphorylation sites with an algorithm of motif length selection. Protein Eng Des Sel 24(3):255-260
47. Zukerberg LR, Patrick GN, Nikolic M, Humbert S, Wu CL, Lanier LM et al (2000) Cables links Cdk5 and c-Abl and facilitates Cdk5 tyrosine phosphorylation, kinase upregulation, and neurite outgrowth. Neuron 26(3):633-646