Functional complexity of the axonal growth cone: A proteomic analysis

PLoS ONE

Volumn 7, Issue 2, 2012, Pages

  Estrada Bernal, Adriana ^a,c   Sanford, Staci D ^a   Sosa, Lucas J ^a   Simon, Glenn C ^a   Hansen, Kirk C ^b   Pfenninger, Karl H ^a  

^a Children's Hospital Colorado   (United States)

^b UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^c OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BIOINFORMATICS; BRAIN CELL; BRAIN HOMOGENATE; CARBOHYDRATE METABOLISM; CATABOLISM; CHROMATIN ASSEMBLY AND DISASSEMBLY; CONTROLLED STUDY; CYTOSKELETON; ENRICHMENT CULTURE; FETUS (ANATOMY); GOLGI COMPLEX; GROWTH CONE; HIPPOCAMPUS; IMMUNOFLUORESCENCE TEST; NERVE CELL CULTURE; NERVE FIBER GROWTH; NONHUMAN; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN MICROARRAY; PROTEIN PROCESSING; PROTEIN SYNTHESIS; PROTEOMICS; RAT; RETICULAR FORMATION; RNA TRANSLATION; ROUGH ENDOPLASMIC RETICULUM; TRANSPORT VESICLE; UBIQUITINATION; WESTERN BLOTTING; ANIMAL; BIOLOGY; BRAIN; CHEMISTRY; CLUSTER ANALYSIS; FLUORESCENCE MICROSCOPY; METABOLISM; METHODOLOGY; NERVE FIBER; PHYSIOLOGY; PRENATAL DEVELOPMENT; SPRAGUE DAWLEY RAT;

RATTUS;

CARBOHYDRATE; PROTEOME;

ANIMALS; AXONS; BRAIN; CARBOHYDRATES; CLUSTER ANALYSIS; COMPUTATIONAL BIOLOGY; GROWTH CONES; HIPPOCAMPUS; MICROSCOPY, FLUORESCENCE; PROTEIN FOLDING; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEOME; PROTEOMICS; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84857584753     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0031858     Document Type: Article

References (56)

1. Letourneau PC, (1996) The cytoskeleton in nerve growth cone motility and axonal pathfinding. Perspect Dev Neurobiol 4: 111-123.
2. Pfenninger KH, (2009) Plasma membrane expansion: a neuron's Herculean task. Nat Rev Neurosci 10: 251-261.
3. Conde C, Caceres A, (2009) Microtubule assembly, organization and dynamics in axons and dendrites. Nat Rev Neurosci 10: 319-332.
4. Tessier-Lavigne M, Goodman CS, (1996) The molecular biology of axon guidance. Science 274: 1123-1133.
5. O'Donnell M, Chance RK, Bashaw GJ, (2009) Axon growth and guidance: receptor regulation and signal transduction. Annu Rev Neurosci 32: 383-412.
6. Lohse K, Helmke SM, Wood MR, Quiroga S, de la Houssaye BA, et al. (1996) Axonal origin and purity of growth cones isolated from fetal rat brain. Brain Res Dev Brain Res 96: 83-96.
7. 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: 573-584.
8. Meiri KF, Pfenninger KH, Willard MB, (1986) Growth-associated protein, GAP-43, a polypeptide that is induced when neurons extend axons, is a component of growth cones and corresponds to pp46, a major polypeptide of a subcellular fraction enriched in growth cones. Proc Natl Acad Sci U S A 83: 3537-3541.
9. Nozumi M, Togano T, Takahashi-Niki K, Lu J, Honda A, et al. (2009) Identification of functional marker proteins in the mammalian growth cone. Proc Natl Acad Sci U S A 106: 17211-17216.
10. Dennis G Jr, Sherman BT, Hosack DA, Yang J, Gao W, et al. (2003) DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome Biol 4: P3.
11. Huang da W, Sherman BT, Lempicki RA, (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4: 44-57.
12. Huang da W, Sherman BT, Lempicki RA, (2009) Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res 37: 1-13.
13. Dotti CG, Banker GA, Binder LI, (1987) The expression and distribution of the microtubule-associated proteins tau and microtubule-associated protein 2 in hippocampal neurons in the rat in situ and in cell culture. Neuroscience 23: 121-130.
14. Ferreira A, Busciglio J, Caceres A, (1987) An immunocytochemical analysis of the ontogeny of the microtubule-associated proteins MAP-2 and Tau in the nervous system of the rat. Brain Res 431: 9-31.
15. Kosik KS, Finch EA, (1987) MAP2 and tau segregate into dendritic and axonal domains after the elaboration of morphologically distinct neurites: an immunocytochemical study of cultured rat cerebrum. J Neurosci 7: 3142-3153.
16. Rothstein JD, Martin L, Levey AI, Dykes-Hoberg M, Jin L, et al. (1994) Localization of neuronal and glial glutamate transporters. Neuron 13: 713-725.
17. Schmidt EF, Strittmatter SM, (2007) The CRMP family of proteins and their role in Sema3A signaling. Adv Exp Med Biol 600: 1-11.
18. Nguyen VQ, Co C, Irie K, Li JJ, (2000) Clb/Cdc28 kinases promote nuclear export of the replication initiator proteins Mcm2-7. Curr Biol 10: 195-205.
19. Naryzhny SN, Lee H, (2004) The post-translational modifications of proliferating cell nuclear antigen: acetylation, not phosphorylation, plays an important role in the regulation of its function. J Biol Chem 279: 20194-20199.
20. Vriz S, Lemaitre JM, Leibovici M, Thierry N, Mechali M, (1992) Comparative analysis of the intracellular localization of c-Myc, c-Fos, and replicative proteins during cell cycle progression. Mol Cell Biol 12: 3548-3555.
21. Negre-Aminou P, Pfenninger KH, (1993) Arachidonic acid turnover and phospholipase A2 activity in neuronal growth cones. J Neurochem 60: 1126-1136.
22. Kornfeld R, Kornfeld S, (1985) Assembly of asparagine-linked oligosaccharides. Annu Rev Biochem 54: 631-664.
23. Dunphy WG, Rothman JE, (1983) Compartmentation of asparagine-linked oligosaccharide processing in the Golgi apparatus. J Cell Biol 97: 270-275.
24. Wu CC, Taylor RS, Lane DR, Ladinsky MS, Weisz JA, et al. (2000) GMx33: a novel family of trans-Golgi proteins identified by proteomics. Traffic 1: 963-975.
25. Jones SM, Crosby JR, Salamero J, Howell KE, (1993) A cytosolic complex of p62 and rab6 associates with TGN38/41 and is involved in budding of exocytic vesicles from the trans-Golgi network. J Cell Biol 122: 775-788.
26. Perry RB, Fainzilber M, (2009) Nuclear transport factors in neuronal function. Semin Cell Dev Biol 20: 600-606.
27. Otis KO, Thompson KR, Martin KC, (2006) Importin-mediated nuclear transport in neurons. Curr Opin Neurobiol 16: 329-335.
28. Harel A, Forbes DJ, (2004) Importin beta: conducting a much larger cellular symphony. Mol Cell 16: 319-330.
29. Pertz OC, Wang Y, Yang F, Wang W, Gay LJ, et al. (2008) Spatial mapping of the neurite and soma proteomes reveals a functional Cdc42/Rac regulatory network. Proc Natl Acad Sci U S A 105: 1931-1936.
30. Zivraj KH, Tung YC, Piper M, Gumy L, Fawcett JW, et al. (2010) Subcellular profiling reveals distinct and developmentally regulated repertoire of growth cone mRNAs. J Neurosci 30: 15464-15478.
31. Jeffery CJ, (2003) Moonlighting proteins: old proteins learning new tricks. Trends Genet 19: 415-417.
32. Giuditta A, Kaplan BB, van Minnen J, Alvarez J, Koenig E, (2002) Axonal and presynaptic protein synthesis: new insights into the biology of the neuron. Trends Neurosci 25: 400-404.
33. Campbell DS, Holt CE, (2001) Chemotropic responses of retinal growth cones mediated by rapid local protein synthesis and degradation. Neuron 32: 1013-1026.
34. Zheng JQ, Kelly TK, Chang B, Ryazantsev S, Rajasekaran AK, et al. (2001) A functional role for intra-axonal protein synthesis during axonal regeneration from adult sensory neurons. J Neurosci 21: 9291-9303.
35. Brittis PA, Lu Q, Flanagan JG, (2002) Axonal protein synthesis provides a mechanism for localized regulation at an intermediate target. Cell 110: 223-235.
36. Brunet I, Weinl C, Piper M, Trembleau A, Volovitch M, et al. (2005) The transcription factor Engrailed-2 guides retinal axons. Nature 438: 94-98.
37. Wu KY, Hengst U, Cox LJ, Macosko EZ, Jeromin A, et al. (2005) Local translation of RhoA regulates growth cone collapse. Nature 436: 1020-1024.
38. Willis D, Li KW, Zheng JQ, Chang JH, Smit A, et al. (2005) Differential transport and local translation of cytoskeletal, injury-response, and neurodegeneration protein mRNAs in axons. J Neurosci 25: 778-791.
39. Willis DE, Twiss JL, (2006) The evolving roles of axonally synthesized proteins in regeneration. Curr Opin Neurobiol 16: 111-118.
40. Hengst U, Jaffrey SR, (2007) Function and translational regulation of mRNA in developing axons. Semin Cell Dev Biol 18: 209-215.
41. Lin AC, Holt CE, (2008) Function and regulation of local axonal translation. Curr Opin Neurobiol 18: 60-68.
42. Bassell GJ, Zhang H, Byrd AL, Femino AM, Singer RH, et al. (1998) Sorting of beta-actin mRNA and protein to neurites and growth cones in culture. J Neurosci 18: 251-265.
43. Bi J, Tsai NP, Lin YP, Loh HH, Wei LN, (2006) Axonal mRNA transport and localized translational regulation of kappa-opioid receptor in primary neurons of dorsal root ganglia. Proc Natl Acad Sci U S A 103: 19919-19924.
44. Merianda TT, Lin AC, Lam JS, Vuppalanchi D, Willis DE, et al. (2009) A functional equivalent of endoplasmic reticulum and Golgi in axons for secretion of locally synthesized proteins. Mol Cell Neurosci 40: 128-142.
45. Mann F, Miranda E, Weinl C, Harmer E, Holt CE, (2003) B-type Eph receptors and ephrins induce growth cone collapse through distinct intracellular pathways. J Neurobiol 57: 323-336.
46. Verma P, Chierzi S, Codd AM, Campbell DS, Meyer RL, et al. (2005) Axonal protein synthesis and degradation are necessary for efficient growth cone regeneration. J Neurosci 25: 331-342.
47. Drinjakovic J, Jung H, Campbell DS, Strochlic L, Dwivedy A, et al. (2010) E3 ligase Nedd4 promotes axon branching by downregulating PTEN. Neuron 65: 341-357.
48. Mayer MP, Bukau B, (2005) Hsp70 chaperones: cellular functions and molecular mechanism. Cell Mol Life Sci 62: 670-684.
49. Doyle SM, Wickner S, (2009) Hsp104 and ClpB: protein disaggregating machines. Trends Biochem Sci 34: 40-48.
50. Koike M, Fukushi J, Ichinohe Y, Higashimae N, Fujishiro M, et al. (2010) Valosin-containing protein (VCP) in novel feedback machinery between abnormal protein accumulation and transcriptional suppression. J Biol Chem 285: 21736-21749.
51. Casey PJ, Solski PA, Der CJ, Buss JE, (1989) p21ras is modified by a farnesyl isoprenoid. Proc Natl Acad Sci U S A 86: 8323-8327.
52. Gumy LF, Yeo GS, Tung YC, Zivraj KH, Willis D, et al. (2011) Transcriptome analysis of embryonic and adult sensory axons reveals changes in mRNA repertoire localization. RNA 17: 85-98.
53. Fulga TA, Van Vactor D, (2008) Synapses and growth cones on two sides of a highwire. Neuron 57: 339-344.
54. Murphey RK, Godenschwege TA, (2002) New roles for ubiquitin in the assembly and function of neuronal circuits. Neuron 36: 5-8.
55. Wessel D, Flugge UI, (1984) A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids. Anal Biochem 138: 141-143.
56. Pfenninger KH, Maylie-Pfenninger MF, (1981) Lectin labeling of sprouting neurons. I. Regional distribution of surface glycoconjugates. J Cell Biol 89: 536-546.