Proteomic analysis of the palmitoyl protein thioesterase 1 interactome in SH-SY5Y human neuroblastoma cells

Journal of Proteomics

Volumn 123, Issue , 2015, Pages 42-53

  Scifo, Enzo ^a   Szwajda, Agnieszka ^a   Soliymani, Rabah ^a   Pezzini, Francesco ^b   Bianchi, Marzia ^b,c   Dapkunas, Arvydas ^a   Debski, Janusz ^d   Uusi Rauva, Kristiina ^e,f   Dadlez, Michał ^d   Gingras, Anne Claude ^g,h   Tyynelä, Jaana ^a   Simonati, Alessandro ^b   Jalanko, Anu ^a,f   Baumann, Marc H ^a   Lalowski, Maciej ^a,e  

^a UNIVERSITY OF HELSINKI   (Finland)

^b UNIVERSITY OF VERONA   (Italy)

^c BAMBINO GESÙ CHILDREN S HOSPITAL   (Italy)

^d INSTITUTE OF BIOCHEMISTRY AND BIOPHYSICS   (Poland)

^e FOLKHÄLSAN INSTITUTE OF GENETICS   (Finland)

^f NATIONAL PUBLIC HEALTH INSTITUTE   (Finland)

^g MOUNT SINAI HOSPITAL   (Canada)

^h UNIVERSITY OF TORONTO   (Canada)

Author keywords

Affinity purification; CLN1 disease; Interactome; Mass spectrometry; Neuronal ceroid lipofuscinoses; Palmitoyl protein thioesterase 1

Indexed keywords

COLLAPSIN RESPONSE MEDIATOR PROTEIN 1; DOPAMINE BETA MONOOXYGENASE; DOPAMINE RECEPTOR; MICROTUBULE ASSOCIATED PROTEIN 1; PALMITOYL PROTEIN THIOESTERASE; PALMITOYL PROTEIN THIOESTERASE 1; UNCLASSIFIED DRUG; MEMBRANE PROTEIN; PPT1 PROTEIN, HUMAN;

AFFINITY PURIFICATION; ARTICLE; CELL MIGRATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; HYBRID QUADRUPOLE ORBITRAP MASS SPECTROMETRY; IN VIVO STUDY; INTERACTOME; LIPID METABOLISM; MASS SPECTROMETRY; NERVE CELL; NERVE FIBER; NEUROBLASTOMA CELL LINE; NEURONAL CEROID LIPOFUSCINOSIS; PALMITOYLATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEOMICS; SIGNAL TRANSDUCTION; AXON; BRAIN; CELL MOTION; ENERGY METABOLISM; FLUORESCENCE MICROSCOPY; GENE EXPRESSION REGULATION; GENETICS; GLYCOSYLATION; HEK293 CELL LINE; LYSOSOME; METABOLISM; MITOCHONDRION; MUTATION; NEUROBLASTOMA; OPEN READING FRAME; PHYSIOLOGY; PROCEDURES; TUMOR CELL LINE;

AXONS; BRAIN; CELL LINE, TUMOR; CELL MOVEMENT; ENERGY METABOLISM; GENE EXPRESSION REGULATION, NEOPLASTIC; GLYCOSYLATION; HEK293 CELLS; HUMANS; LYSOSOMES; MASS SPECTROMETRY; MEMBRANE PROTEINS; MICROSCOPY, FLUORESCENCE; MITOCHONDRIA; MUTATION; NEUROBLASTOMA; NEURONAL CEROID-LIPOFUSCINOSES; NEURONS; OPEN READING FRAMES; PROTEOMICS; SIGNAL TRANSDUCTION;

EID: 84927932541     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2015.03.038     Document Type: Article

References (95)

1. Gavin A.C., Bosche M., Krause R., Grandi P., Marzioch M., Bauer A., et al. Functional organization of the yeast proteome by systematic analysis of protein complexes. Nature 2002, 415:141-147.
2. Krogan N.J., Cagney G., Yu H., Zhong G., Guo X., Ignatchenko A., et al. Global landscape of protein complexes in the yeast Saccharomyces cerevisiae. Nature 2006, 440:637-643.
3. Ewing R.M., Chu P., Elisma F., Li H., Taylor P., Climie S., et al. Large-scale mapping of human protein-protein interactions by mass spectrometry. Mol Syst Biol 2007, 3:89.
4. Alberts B. The cell as a collection of protein machines: preparing the next generation of molecular biologists. Cell 1998, 92:291-294.
5. Wisniewski J.R., Zougman A., Nagaraj N., Mann M. Universal sample preparation method for proteome analysis. Nat Methods 2009, 6:359-362.
6. Vesa J., Hellsten E., Verkruyse L.A., Camp L.A., Rapola J., Santavuori P., et al. Mutations in the palmitoyl protein thioesterase gene causing infantile neuronal ceroid lipofuscinosis. Nature 1995, 376:584-587.
7. Hofmann S.L., Das A.K., Lu J.Y., Soyombo A.A. Positional candidate gene cloning of CLN1. Adv Genet 2001, 45:69-92.
8. Kim S.J., Zhang Z., Sarkar C., Tsai P.C., Lee Y.C., Dye L., et al. Palmitoyl protein thioesterase-1 deficiency impairs synaptic vesicle recycling at nerve terminals, contributing to neuropathology in humans and mice. J Clin Invest 2008, 118:3075-3086.
9. Virmani T., Gupta P., Liu X., Kavalali E.T., Hofmann S.L. Progressively reduced synaptic vesicle pool size in cultured neurons derived from neuronal ceroid lipofuscinosis-1 knockout mice. Neurobiol Dis 2005, 20:314-323.
10. Verkruyse L.A., Hofmann S.L. Lysosomal targeting of palmitoyl-protein thioesterase. J Biol Chem 1996, 271:15831-15836.
11. Bellizzi J.J., Widom J., Kemp C., Lu J.Y., Das A.K., Hofmann S.L., et al. The crystal structure of palmitoyl protein thioesterase 1 and the molecular basis of infantile neuronal ceroid lipofuscinosis. Proc Natl Acad Sci U S A 2000, 97:4573-4578.
12. Lyly A., von Schantz C., Salonen T., Kopra O., Saarela J., Jauhiainen M., et al. Glycosylation, transport, and complex formation of palmitoyl protein thioesterase 1 (PPT1)-distinct characteristics in neurons. BMC Cell Biol 2007, 8:22.
13. Ahtiainen L., Van Diggelen O.P., Jalanko A., Kopra O. Palmitoyl protein thioesterase 1 is targeted to the axons in neurons. J Comp Neurol 2003, 455:368-377.
14. Lehtovirta M., Kyttala A., Eskelinen E.L., Hess M., Heinonen O., Jalanko A. Palmitoyl protein thioesterase (PPT) localizes into synaptosomes and synaptic vesicles in neurons: implications for infantile neuronal ceroid lipofuscinosis (INCL). Hum Mol Genet 2001, 10:69-75.
15. Cho S., Dawson P.E., Dawson G. Antisense palmitoyl protein thioesterase 1 (PPT1) treatment inhibits PPT1 activity and increases cell death in LA-N-5 neuroblastoma cells. J Neurosci Res 2000, 62:234-240.
16. Zhang Z., Lee Y.C., Kim S.J., Choi M.S., Tsai P.C., Xu Y., et al. Palmitoyl-protein thioesterase-1 deficiency mediates the activation of the unfolded protein response and neuronal apoptosis in INCL. Hum Mol Genet 2006, 15:337-346.
17. Holopainen J.M., Saarikoski J., Kinnunen P.K., Jarvela I. Elevated lysosomal pH in neuronal ceroid lipofuscinoses (NCLs). Eur J Biochem 2001, 268:5851-5856.
18. Ahtiainen L., Luiro K., Kauppi M., Tyynela J., Kopra O., Jalanko A. Palmitoyl protein thioesterase 1 (PPT1) deficiency causes endocytic defects connected to abnormal saposin processing. Exp Cell Res 2006, 312:1540-1553.
19. Aby E., Roth A., Gumps K., Sigmon S., Jenkins S.E., Kim J.J., et al. Mutations in palmitoyl-protein thioesterase 1 alter exocytosis and endocytosis at synapses in Drosophila larvae. Fly (Austin) 2013, 7.
20. Lyly A., Marjavaara S.K., Kyttala A., Uusi-Rauva K., Luiro K., Kopra O., et al. Deficiency of the INCL protein PPt1 results in changes in ectopic F1-ATP synthase and altered cholesterol metabolism. Hum Mol Genet 2008, 17:1406-1417.
21. Ahtiainen L., Kolikova J., Mutka A.L., Luiro K., Gentile M., Ikonen E., et al. Palmitoyl protein thioesterase 1 (PPt1)-deficient mouse neurons show alterations in cholesterol metabolism and calcium homeostasis prior to synaptic dysfunction. Neurobiol Dis 2007, 28:52-64.
22. Das A.K., Becerra C.H., Yi W., Lu J.Y., Siakotos A.N., Wisniewski K.E., et al. Molecular genetics of palmitoyl-protein thioesterase deficiency in the U.S. J Clin Invest 1998, 102:361-370.
23. Santorelli F.M., Garavaglia B., Cardona F., Nardocci N., Bernardina B.D., Sartori S., et al. Molecular epidemiology of childhood neuronal ceroid-lipofuscinosis in Italy. Orphanet J Rare Dis 2013, 8:19.
24. Santavuori P. Neuronal ceroid-lipofuscinoses in childhood. Brain Dev 1988, 10:80-83.
25. Tyynela J., Palmer D.N., Baumann M., Haltia M. Storage of saposins A and D in infantile neuronal ceroid-lipofuscinosis. FEBS Lett 1993, 330:8-12.
26. Gupta P., Soyombo A.A., Atashband A., Wisniewski K.E., Shelton J.M., Richardson J.A., et al. Disruption of PPT1 or PPT2 causes neuronal ceroid lipofuscinosis in knockout mice. Proc Natl Acad Sci U S A 2001, 98:13566-13571.
27. Jalanko A., Vesa J., Manninen T., von Schantz C., Minye H., Fabritius A.L., et al. Mice with PPt1Deltaex4 mutation replicate the INCL phenotype and show an inflammation-associated loss of interneurons. Neurobiol Dis 2005, 18:226-241.
28. Bible E., Gupta P., Hofmann S.L., Cooper J.D. Regional and cellular neuropathology in the palmitoyl protein thioesterase-1 null mutant mouse model of infantile neuronal ceroid lipofuscinosis. Neurobiol Dis 2004, 16:346-359.
29. Miller J.N., Kovacs A.D., Pearce D.A. The novel Cln1R151X mouse model of infantile neuronal ceroid lipofuscinosis (INCL) for testing nonsense suppression therapy. Hum Mol Genet 2015, 24:185-196.
30. Porter M.Y., Turmaine M., Mole S.E. Identification and characterization of Caenorhabditis elegans palmitoyl protein thioesterase1. J Neurosci Res 2005, 79:836-848.
31. Hickey A.J., Chotkowski H.L., Singh N., Ault J.G., Korey C.A., MacDonald M.E., et al. Palmitoyl-protein thioesterase 1 deficiency in Drosophila melanogaster causes accumulation of abnormal storage material and reduced life span. Genetics 2006, 172:2379-2390.
32. Koch H.B., Zhang R., Verdoodt B., Bailey A., Zhang C.D., Yates J.R., et al. Large-scale identification of c-MYC-associated proteins using a combined TAP/MudPIT approach. Cell Cycle 2007, 6:205-217.
33. Wagner S.A., Beli P., Weinert B.T., Nielsen M.L., Cox J., Mann M., et al. A proteome-wide, quantitative survey of in vivo ubiquitylation sites reveals widespread regulatory roles. Mol Cell Proteomics 2011, 10. [M111 013284].
34. Liu B., Zheng Y., Wang T.D., Xu H.Z., Xia L., Zhang J., et al. Proteomic identification of common SCF ubiquitin ligase FBXO6-interacting glycoproteins in three kinds of cells. J Proteome Res 2012, 11:1773-1781.
35. Havugimana P.C., Hart G.T., Nepusz T., Yang H., Turinsky A.L., Li Z., et al. A census of human soluble protein complexes. Cell 2012, 150:1068-1081.
36. Byron A., Humphries J.D., Craig S.E., Knight D., Humphries M.J. Proteomic analysis of alpha4beta1 integrin adhesion complexes reveals alpha-subunit-dependent protein recruitment. Proteomics 2012, 12:2107-2114.
37. Wang J., Huo K., Ma L., Tang L., Li D., Huang X., et al. Toward an understanding of the protein interaction network of the human liver. Mol Syst Biol 2011, 7:536.
38. Nicholson J., Scherl A., Way L., Blackburn E.A., Walkinshaw M.D., Ball K.L., et al. A systems wide mass spectrometric based linear motif screen to identify dominant in-vivo interacting proteins for the ubiquitin ligase MDM2. Cell Signal 2014, 26:1243-1257.
39. Chu-LaGraff Q., Blanchette C., O'Hern P., Denefrio C. The Batten disease palmitoyl protein thioesterase 1 gene regulates neural specification and axon connectivity during Drosophila embryonic development. PLoS One 2010, 5:e14402.
40. Scifo E., Szwajda A., Debski J., Uusi-Rauva K., Kesti T., Dadlez M., et al. Drafting the CLN3 protein interactome in SH-SY5Y human neuroblastoma cells: a label-free quantitative proteomics approach. J Proteome Res 2013, 12:2101-2115.
41. Scifo E., Szwajda A., Soliymani R., Pezzini F., Bianchi M., Dapkunas A., et al. Quantitative analysis of PPT1 interactome in human neuroblastoma cells. Data in brief 2015, [submitted for publication].
42. Hellsten E., Vesa J., Olkkonen V.M., Jalanko A., Peltonen L. Human palmitoyl protein thioesterase: evidence for lysosomal targeting of the enzyme and disturbed cellular routing in infantile neuronal ceroid lipofuscinosis. EMBO J 1996, 15:5240-5245.
43. Shannon P., Markiel A., Ozier O., Baliga N.S., Wang J.T., Ramage D., et al. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 2003, 13:2498-2504.
44. Bindea G., Mlecnik B., Hackl H., Charoentong P., Tosolini M., Kirilovsky A., et al. ClueGO: a cytoscape plug-in to decipher functionally grouped gene ontology and pathway annotation networks. Bioinformatics 2009, 25:1091-1093.
45. Chen R., Jiang X., Sun D., Han G., Wang F., Ye M., et al. Glycoproteomics analysis of human liver tissue by combination of multiple enzyme digestion and hydrazide chemistry. J Proteome Res 2009, 8:651-661.
46. Zhang H., Li X.J., Martin D.B., Aebersold R. Identification and quantification of N-linked glycoproteins using hydrazide chemistry, stable isotope labeling and mass spectrometry. Nat Biotechnol 2003, 21:660-666.
47. Cho S., Dawson G. Palmitoyl protein thioesterase 1 protects against apoptosis mediated by Ras-Akt-caspase pathway in neuroblastoma cells. J Neurochem 2000, 74:1478-1488.
48. Duncan J.A., Gilman A.G. A cytoplasmic acyl-protein thioesterase that removes palmitate from G protein alpha subunits and p21(RAS). J Biol Chem 1998, 273:15830-15837.
49. Burckstummer T., Bennett K.L., Preradovic A., Schutze G., Hantschel O., Superti-Furga G., et al. An efficient tandem affinity purification procedure for interaction proteomics in mammalian cells. Nat Methods 2006, 3:1013-1019.
50. Choi H., Larsen B., Lin Z.Y., Breitkreutz A., Mellacheruvu D., Fermin D., et al. SAINT: probabilistic scoring of affinity purification-mass spectrometry data. Nat Methods 2011, 8:70-73.
51. Choi H., Liu G., Mellacheruvu D., Tyers M., Gingras A.C., Nesvizhskii A.I. Analyzing protein-protein interactions from affinity purification-mass spectrometry data with SAINT. Curr Protoc Bioinformatics 2012, [Chapter 8:Unit8.15]. 10.1002/0471250953.bi0815s39.
52. Teo G., Liu G., Zhang J., Nesvizhskii A.I., Gingras A.C., Choi H. SAINTexpress: improvements and additional features in significance analysis of INTeractome software. J Proteomics 2014, 100:37-43.
53. Yoshida H., Watanabe A., Ihara Y. Collapsin response mediator protein-2 is associated with neurofibrillary tangles in Alzheimer's disease. J Biol Chem 1998, 273:9761-9768.
54. Barzilai A., Zilkha-Falb R., Daily D., Stern N., Offen D., Ziv I., et al. The molecular mechanism of dopamine-induced apoptosis: identification and characterization of genes that mediate dopamine toxicity. J Neural Transm Suppl 2000, 59-76.
55. Kim C.H., Zabetian C.P., Cubells J.F., Cho S., Biaggioni I., Cohen B.M., et al. Mutations in the dopamine beta-hydroxylase gene are associated with human norepinephrine deficiency. Am J Med Genet 2002, 108:140-147.
56. Ottis P., Koppe K., Onisko B., Dynin I., Arzberger T., Kretzschmar H., et al. Human and rat brain lipofuscin proteome. Proteomics 2012, 12:2445-2454.
57. Paganoni S., Ferreira A. Neurite extension in central neurons: a novel role for the receptor tyrosine kinases Ror1 and Ror2. J Cell Sci 2005, 118:433-446.
58. Del Rio J.A., Gonzalez-Billault C., Urena J.M., Jimenez E.M., Barallobre M.J., Pascual M., et al. MAP1B is required for Netrin 1 signaling in neuronal migration and axonal guidance. Curr Biol 2004, 14:840-850.
59. Tikka S., Monogioudi E., Gotsopoulos A., Soliymani R., Scifo E., Pezzini F., et al. Proteomic profiling in CLN1 disease brain: an imaging and label-free proteomics approach 2014, [submitted for publication].
60. Schmitt T., Ogris C., Sonnhammer E.L. FunCoup 3.0: database of genome-wide functional coupling networks. Nucleic Acids Res 2014, 42:D380-D388.
61. Skarra D.V., Goudreault M., Choi H., Mullin M., Nesvizhskii A.I., Gingras A.C., et al. Label-free quantitative proteomics and SAINT analysis enable interactome mapping for the human Ser/Thr protein phosphatase 5. Proteomics 2011, 11:1508-1516.
62. Moon S., Han D., Kim Y., Jin J., Ho W.K. Interactome analysis of AMP-activated protein kinase (AMPK)-alpha1 and -beta1 in INS-1 pancreatic beta-cells by affinity purification-mass spectrometry. Sci Rep 2014, 4:4376.
63. Vandamme J., Volkel P., Rosnoblet C., Le Faou P., Angrand P.O. Interaction proteomics analysis of polycomb proteins defines distinct PRC1 complexes in mammalian cells. Mol Cell Proteomics 2011, 0. [M110 002642].
64. Mellacheruvu D., Wright Z., Couzens A.L., Lambert J.P., St-Denis N.A., Li T., et al. The CRAPome: a contaminant repository for affinity purification-mass spectrometry data. Nat Methods 2013, 10:730-736.
65. Kitao Y., Matsuyama T., Takano K., Tabata Y., Yoshimoto T., Momoi T., et al. Does ORP150/HSP12A protect dopaminergic neurons against MPTP/MPP(+)-induced neurotoxicity?. Antioxid Redox Signal 2007, 9:589-595.
66. Uusi-Rauva K., Luiro K., Tanhuanpaa K., Kopra O., Martin-Vasallo P., Kyttala A., et al. Novel interactions of CLN3 protein link Batten disease to dysregulation of fodrin-Na+, K+ ATPase complex. Exp Cell Res 2008, 314:2895-2905.
67. Behrends C., Sowa M.E., Gygi S.P., Harper J.W. Network organization of the human autophagy system. Nature 2010, 466:68-76.
68. Oresic K., Mueller B., Tortorella D. Cln6 mutants associated with neuronal ceroid lipofuscinosis are degraded in a proteasome-dependent manner. Biosci Rep 2009, 29:173-181.
69. Tyynela J., Sohar I., Sleat D.E., Gin R.M., Donnelly R.J., Baumann M., et al. A mutation in the ovine cathepsin D gene causes a congenital lysosomal storage disease with profound neurodegeneration. EMBO J 2000, 19:2786-2792.
70. Fritchie K., Siintola E., Armao D., Lehesjoki A.E., Marino T., Powell C., et al. Novel mutation and the first prenatal screening of cathepsin D deficiency (CLN10). Acta Neuropathol 2009, 117:201-208.
71. Pezzini F., Gismondi F., Tessa A., Tonin P., Carrozzo R., Mole S.E., et al. Involvement of the mitochondrial compartment in human NCL fibroblasts. Biochem Biophys Res Commun 2011, 416:159-164.
72. Ren J., Wen L., Gao X., Jin C., Xue Y., Yao X. CSS-Palm 2.0: an updated software for palmitoylation sites prediction. Protein Eng Des Sel 2008, 21:639-644.
73. Wang X.B., Wu L.Y., Wang Y.C., Deng N.Y. Prediction of palmitoylation sites using the composition of k-spaced amino acid pairs. Protein Eng Des Sel 2009, 22:707-712.
74. Black M.M., Slaughter T., Fischer I. Microtubule-associated protein 1b (MAP1b) is concentrated in the distal region of growing axons. J Neurosci 1994, 14:857-870.
75. Gonzalez-Billault C., Jimenez-Mateos E.M., Caceres A., Diaz-Nido J., Wandosell F., Avila J. Microtubule-associated protein 1B function during normal development, regeneration, and pathological conditions in the nervous system. J Neurobiol 2004, 58:48-59.
76. DiTella M.C., Feiguin F., Carri N., Kosik K.S., Caceres A. MAP-1B/TAU functional redundancy during laminin-enhanced axonal growth. J Cell Sci 1996, 109(Pt 2):467-477.
77. Gonzalez-Billault C., Del Rio J.A., Urena J.M., Jimenez-Mateos E.M., Barallobre M.J., Pascual M., et al. A role of MAP1B in Reelin-dependent neuronal migration. Cereb Cortex 2005, 15:1134-1145.
78. Takei Y., Teng J., Harada A., Hirokawa N. Defects in axonal elongation and neuronal migration in mice with disrupted tau and map1b genes. J Cell Biol 2000, 150:989-1000.
79. Gonzalez-Billault C., Avila J., Caceres A. Evidence for the role of MAP1B in axon formation. Mol Biol Cell 2001, 12:2087-2098.
80. Charrier E., Reibel S., Rogemond V., Aguera M., Thomasset N., Honnorat J. Collapsin response mediator proteins (CRMPs): involvement in nervous system development and adult neurodegenerative disorders. Mol Neurobiol 2003, 28:51-64.
81. Shirvan A., Ziv I., Fleminger G., Shina R., He Z., Brudo I., et al. Semaphorins as mediators of neuronal apoptosis. J Neurochem 1999, 73:961-971.
82. Gu Y., Ihara Y. Evidence that collapsin response mediator protein-2 is involved in the dynamics of microtubules. J Biol Chem 2000, 275:17917-17920.
83. Fukata Y., Itoh T.J., Kimura T., Menager C., Nishimura T., Shiromizu T., et al. CRMP-2 binds to tubulin heterodimers to promote microtubule assembly. Nat Cell Biol 2002, 4:583-591.
84. Arimura N., Menager C., Fukata Y., Kaibuchi K. Role of CRMP-2 in neuronal polarity. J Neurobiol 2004, 58:34-47.
85. Inagaki N., Chihara K., Arimura N., Menager C., Kawano Y., Matsuo N., et al. CRMP-2 induces axons in cultured hippocampal neurons. Nat Neurosci 2001, 4:781-782.
86. Quach T.T., Duchemin A.M., Rogemond V., Aguera M., Honnorat J., Belin M.F., et al. Involvement of collapsin response mediator proteins in the neurite extension induced by neurotrophins in dorsal root ganglion neurons. Mol Cell Neurosci 2004, 25:433-443.
87. Ito T., Kagoshima M., Sasaki Y., Li C., Udaka N., Kitsukawa T., et al. Repulsive axon guidance molecule Sema3A inhibits branching morphogenesis of fetal mouse lung. Mech Dev 2000, 97:35-45.
88. Wang L.H., Strittmatter S.M. A family of rat CRMP genes is differentially expressed in the nervous system. J Neurosci 1996, 16:6197-6207.
89. Castegna A., Aksenov M., Thongboonkerd V., Klein J.B., Pierce W.M., Booze R., et al. Proteomic identification of oxidatively modified proteins in Alzheimer's disease brain. Part II: dihydropyrimidinase-related protein 2, alpha-enolase and heat shock cognate 71. J Neurochem 2002, 82:1524-1532.
90. Honnorat J., Byk T., Kusters I., Aguera M., Ricard D., Rogemond V., et al. Ulip/CRMP proteins are recognized by autoantibodies in paraneoplastic neurological syndromes. Eur J Neurosci 1999, 11:4226-4232.
91. Yuasa-Kawada J., Suzuki R., Kano F., Ohkawara T., Murata M., Noda M. Axonal morphogenesis controlled by antagonistic roles of two CRMP subtypes in microtubule organization. Eur J Neurosci 2003, 17:2329-2343.
92. Leung T., Ng Y., Cheong A., Ng C.H., Tan I., Hall C., et al. p80 ROKalpha binding protein is a novel splice variant of CRMP-1 which associates with CRMP-2 and modulates RhoA-induced neuronal morphology. FEBS Lett 2002, 532:445-449.
93. Timmers H.J., Deinum J., Wevers R.A., Lenders J.W. Congenital dopamine-beta-hydroxylase deficiency in humans. Ann N Y Acad Sci 2004, 1018:520-523.
94. Cross A.J., Crow T.J., Perry E.K., Perry R.H., Blessed G., Tomlinson B.E. Reduced dopamine-beta-hydroxylase activity in Alzheimer's disease. Br Med J (Clin Res Ed) 1981, 282:93-94.
95. Schindelin J., Arganda-Carreras I., Frise E., Kaynig V., Longair M., Pietzsch T., et al. Fiji: an open-source platform for biological-image analysis. Nat Methods 2012, 9:676-682.