Proteomic assessment of sympathetic ganglia from adult mice that possess null mutations of ExonIII or ExonIV in the p75 neurotrophin receptor gene

Brain Research

Volumn 1253, Issue , 2009, Pages 1-14

  McDonald, Todd G ^a   Scott, Samuel A ^c   Kane, Kevin M ^c   Kawaja, Michael D ^a,b  

^a QUEEN S UNIVERSITY   (Canada)

^b QUEEN S UNIVERSITY   (Canada)

^c OHIO UNIVERSITY   (United States)

Author keywords

Annexin V; Autonomic; p75NTR; Phenotype; Proteomics; Stereology

Indexed keywords

ISOPROTEIN; LAMIN A; LIPOCORTIN 5; NERVE GROWTH FACTOR; NEUROTROPHIN RECEPTOR P75; PROTEOME; TYROSINE 3 MONOOXYGENASE;

ALLELE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EXON; GENE EXPRESSION; GENE MUTATION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; P75 NEUROTROPHIN RECEPTOR GENE; PRIORITY JOURNAL; PROTEOMICS; RECEPTOR GENE; SIGNAL TRANSDUCTION; STEREOLOGY; SYMPATHETIC GANGLION; SYMPATHETIC NERVE CELL; VALIDATION STUDY; WILD TYPE;

ANIMALS; ANNEXIN A5; DOWN-REGULATION; ENDOPEPTIDASES; GANGLIA, SYMPATHETIC; HEAT-SHOCK PROTEINS; ISOENZYMES; LAMIN TYPE A; MICE; MICE, KNOCKOUT; MITOCHONDRIAL PROTEINS; MUSCLE PROTEINS; MUTATION; NEURONS; PHENOTYPE; PROTEOME; PROTEOMICS; RECEPTORS, NERVE GROWTH FACTOR; REPRODUCIBILITY OF RESULTS; TYROSINE 3-MONOOXYGENASE;

MUS;

EID: 58249138598     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2008.11.017     Document Type: Article

References (61)

1. Allen R.T., Hunter W.J., and Agrawal D.K. Morphological and biochemical characterization and analysis of apoptosis. J. Pharmacol. Toxicol.Methods 37 (1997) 215-228
2. Bamji S.X., Majdan M., Pozniak C.D., Belliveau D.J., Aloyz R., Kohn J., Causing C.G., and Miller F.D. The p75 neurotrophin receptor mediates neuronal apoptosis and is essential for naturally occurring sympathetic neuron death. J. Cell Biol. 140 (1998) 911-923
3. Barker P.A. p75NTR: a study in contrasts. Cell Death Differ. 5 (1998) 346-356
4. Barker P.A. p75NTR is positively promiscuous: novel partners and new insights. Neuron 42 (2004) 529-533
5. Barker P.A., and Shooter E.M. Disruption of NGF binding to the low affinity neurotrophin receptor p75LNTR reduces NGF binding to TrkA on PC12 cells. Neuron 13 (1994) 203-215
6. Battleman D.S., Geller A.I., and Chao M.V. HSV-1 vector-mediated gene transfer of the human nerve growth factor receptor p75hNGFR defines high-affinity NGF binding. J. Neurosci. 13 (1993) 941-951
7. Brennan C., Rivas-Plata K., and Landis S.C. The p75 neurotrophin receptor influences NT-3 responsiveness of sympathetic neurons in vivo. Nat. Neurosci. 2 (1999) 699-705
8. Chao M.V. The p75 neurotrophin receptor. J. Neurobiol. 25 (1994) 1373-1385
9. Chapman B.S., and Kuntz I.D. Modeled structure of the 75-kDa neurotrophin receptor. Protein Sci. 4 (1995) 1696-1707
10. Coome G.E., and Kawaja M.D. Prolonged exposure to elevated levels of endogenous nerve growth factor affects the morphological and neurochemical features of sympathetic neurons of postnatal and adult mice. Neuroscience 90 (1999) 941-955
11. Coome G.E., Elliott J., and Kawaja M.D. Sympathetic and sensory axons invade the brains of nerve growth factor transgenic mice in the absence of p75NTR expression. Exp. Neurol. 149 (1998) 284-294
12. Cowen T., Woodhoo A., Sullivan C.D., Jolly R., Crutcher K.A., Wyatt S., Michael G.J., Orike N., Gatzinsky K., and Thrasivoulou C. Reduced age-related plasticity of neurotrophin receptor expression in selected sympathetic neurons of the rat. Aging Cell 2 (2003) 59-69
13. Curtis R., Adryan K.M., Stark J.L., Park J.S., Compton D.L., Weskamp G., Huber L.J., Chao M.V., Jaenisch R., Lee K.F., et al. Differential role of the low affinity neurotrophin receptor (p75) in retrograde axonal transport of the neurotrophins. Neuron 14 (1995) 1201-1211
14. Dale E.C., Yang X., Moore S.K., and Shyamala G. Cloning and characterization of the promoter for murine 84-kDa heat-shock protein. Gene 172 (1996) 279-284
15. Dechant G., and Barde Y.A. Signalling through the neurotrophin receptor p75NTR. Curr. Opin. Neurobiol. 7 (1997) 413-418
16. Gidon-Jeangirard C., Hugel B., Holl V., Toti F., Laplanche J.L., Meyer D., and Freyssinet J.M. Annexin V delays apoptosis while exerting an external constraint preventing the release of CD4+ and PrPc+ membrane particles in a human T lymphocyte model. J. Immunol. 162 (1999) 5712-5718
17. Gidon-Jeangirard C., Solito E., Hofmann A., Russo-Marie F., Freyssinet J.M., and Martínez M.C. Annexin V counteracts apoptosis while inducing Ca(2+) influx in human lymphocytic T cells. Biochem. Biophys. Res. Commun. 265 (1999) 709-715
18. Gieffers C., Korioth F., Heimann P., Ungermann C., and Frey J. Mitofilin is a transmembrane protein of the inner mitochondrial membrane expressed as two isoforms. Exp. Cell Res. 232 (1997) 395-399
19. Graham D.R., Garnham C.P., Fu Q., Robbins J., and Van Eyk J.E. Improvements in two-dimensional gel electrophoresis by utilizing a low cost "in-house" neutral pH sodium dodecyl sulfate-polyacrylamide electrophoresis system. Proteomics 5 (2005) 2309-2314
20. Grimes M.L., Zhou J., Beattie E.C., Yuen E.C., Hall D.E., Valletta J.S., Topp K.S., LaVail J.H., Bunnett N.W., and Mobley W.C. Endocytosis of activated trkA: evidence that nerve growth factor induces formation of signaling endosomes. J. Neurosci. 16 (1996) 7950-7964
21. Gotzmann J., and Foisner R. A-type lamin complexes and regenerative potential: a step towards understanding laminopathic diseases? Histochem. Cell Biol. 125 (2006) 33-41
22. Hagg T., Fass-Holmes B., Vahlsing H.L., Manthorpe M., Conner J.M., and Varon S. Nerve growth factor (NGF) reverses axotomy-induced decreases in choline acetyltransferase, NGF receptor and size of medial septum cholinergic neurons. Brain Res. 505 (1989) 29-38
23. Hannila S.S., and Kawaja M.D. Nerve growth factor-induced growth of sympathetic axons into the optic tract of mature mice is enhanced by an absence of p75NTR expression. J. Neurobiol. 39 (1999) 51-66
24. Hannila S.S., Lawrance G.M., Ross G.M., and Kawaja M.D. TrkA and mitogen-activated protein kinase phosphorylation are enhanced in sympathetic neurons lacking functional p75 neurotrophin receptor expression. Eur. J. Neurosci. 19 (2004) 2903-2908
25. Hantzopoulos P.A., Suri C., Glass D.J., Goldfarb M.P., and Yancopoulos G.D. The low affinity NGF receptor, p75, can collaborate with each of the Trks to potentiate functional responses to the neurotrophins. Neuron 13 (1994) 187-201
26. Hefti F., Hartikka J., Salvatierra A., Weiner W.J., and Mash D.C. Localization of nerve growth factor receptors in cholinergic neurons of the human basal forebrain. Neurosci. Lett. 69 (1986) 37-41
27. Hempstead B.L., Patil N., Thiel B., and Chao M.V. Deletion of cytoplasmic sequences of the nerve growth factor receptor leads to loss of high affinity ligand binding. J. Biol. Chem. 265 (1990) 9595-9598
28. Hempstead B.L., Martin-Zanca D., Kaplan D.R., Parada L.F., and Chao M.V. High-affinity NGF binding requires coexpression of the trk proto-oncogene and the low-affinity NGF receptor. Nature 350 (1991) 678-683
29. Jahed A., and Kawaja M.D. The influences of p75 neurotrophin receptor and brain-derived neurotrophic factor in the sympathetic innervation of target tissues during murine postnatal development. Auton Neurosci. 118 (2005) 32-42
30. John G.B., Shang Y., Li L., Renken C., Mannella C.A., Selker J.M., Rangell L., Bennett M.J., and Zha J. The mitochondrial inner membrane protein mitofilin controls cristae morphology. Mol. Biol. Cell 16 (2005) 1543-1554
31. Johnson Jr. E.M., Osborne P.A., and Taniuchi M. Destruction of sympathetic and sensory neurons in the developing rat by a monoclonal antibody against the nerve growth factor (NGF) receptor. Brain Res. 478 (1989) 166-170
32. Kawaja M.D. Sympathetic and sensory innervation of the extracerebral vasculature: roles for p75NTR neuronal expression and nerve growth factor. J. Neurosci. Res. 52 (1998) 295-306
33. Kawaja M.D., Rosenberg M.B., Yoshida K., and Gage F.H. Somatic gene transfer of nerve growth factor promotes the survival of axotomized septal neurons and the regeneration of their axons in adult rats. J. Neurosci. 12 (1992) 2849-2864
34. Kohn J., Aloyz R.S., Toma J.G., Haak-Frenscho M., and Miller F.D. Functionally antagonistic interactions between the trkA and p75 neurotrophins receptors regulate sympathetic neuron growth and target innervation. J. Neurosci. 19 (1999) 5393-5408
35. Krol K.M., Crutcher K.A., Kalisch B.E., Rylett R.J., and Kawaja M.D. Absence of p75(NTR) expression reduces nerve growth factor immunolocalization in cholinergic septal neurons. J. Comp. Neurol. 427 (2000) 54-66
36. Lee K.F., Li E., Huber L.J., Landis S.C., Sharpe A.H., Chao M.V., and Jaenisch R. Targeted mutation of the gene encoding the low affinity NGF receptor p75 leads to deficits in the peripheral sensory nervous system. Cell 69 (1992) 737-749
37. Lee K.F., Bachman K., Landis S.C., and Jaenisch R. Dependence on p75 for innervation of some sympathetic targets. Science 263 (1994) 1447-1449
38. Lopez M.F., Berggren K., Chernokalskaya E., Lazarev A., Robinson M., and Patton W.F. A comparison of silver stain and SYPRO Ruby Protein Gel Stain with respect to protein detection in two-dimensional gels and identification by peptide mass profiling. Electrophoresis 21 (2000) 3673-3683
39. Majdan M., Walsh G.S., Aloyz R., and Miller F.D. TrkA mediates developmental sympathetic neuron survival in vivo by silencing an ongoing p75NTR-mediated death signal. J. Cell Biol. 155 (2001) 1275-1285
40. Max S.R., Rohrer H., Otten U., and Thoenen H. Nerve growth factor-mediated induction of tyrosine hydroxylase in rat superior cervical ganglia in vitro. J. Biol. Chem. 253 (1978) 8013-8015
41. Miller F.D., Mathew T.C., and Toma J.G. Regulation of nerve growth factor receptor gene expression by nerve growth factor in the developing peripheral nervous system. J. Cell Biol. 112 (1991) 303-312
42. Miller F.D., Speelman A., Mathew T.C., Fabian J., Chang E., Pozniak C., and Toma J.G. Nerve growth factor derived from terminals selectively increases the ratio of p75 to trkA NGF receptors on mature sympathetic neurons. Dev. Biol. 161 (1994) 206-217
43. Otten U., Schwab M., Gagnon C., and Thoenen H. Selective induction of tyrosine hydroxylase and dopamine beta-hydroxylase by nerve growth factor: comparison between adrenal medulla and sympathetic ganglia of adult and newborn rats. Brain Res. 133 (1977) 291-303
44. Paul C.E., Vereker E., Dickson K.M., and Barker P.A. A pro-apoptotic fragment of the p75 neurotrophin receptor is expressed in p75NTRExonIV null mice. J. Neurosci. 24 (2004) 1917-1923
45. Ramon-Cueto A., Perez J., and Nieto-Sampedro M. In vitro enfolding of olfactory neurites by p75 NGF receptor positive ensheathing cells from adult rat olfactory bulb. Eur. J. Neurosci. 5 (1993) 1172-1180
46. Reutelingsperger C.P., and van Heerde W.L. Annexin V, the regulator of phosphatidylserine-catalyzed inflammation and coagulation during apoptosis. Cell. Mol. Life Sci. 53 (1997) 527-532
47. Shevchenko A., Wilm M., Vorm O., and Mann M. Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 68 (1996) 850-858
48. Taniuchi M., Clark H.B., and Johnson Jr. E.M. Induction of nerve growth factor receptor in Schwann cells after axotomy. Proc. Natl. Acad. Sci. U. S. A. 83 (1986) 4094-4098
49. Toma J.G., Rogers D., Senger D.L., Campenot R.B., and Miller F.D. Spatial regulation of neuronal gene expression in response to nerve growth factor. Dev. Biol. 184 (1997) 1-9
50. Verge V.M., Merlio J.P., Grondin J., Ernfors P., Persson H., Riopelle R.J., Hokfelt T., and Richardson P.M. Colocalization of NGF binding sites, trk mRNA, and low-affinity NGF receptor mRNA in primary sensory neurons: responses to injury and infusion of NGF. J. Neurosci. 12 (1992) 4011-4022
51. von Schack D., Casademunt E., Schweigreiter R., Meyer M., Bibel M., and Dechant G. Complete ablation of the neurotrophin receptor p75NTR causes defects both in the nervous and the vascular system. Nat. Neurosci. 4 (2001) 977-978
52. Walsh G.S., Krol K.M., Crutcher K.A., and Kawaja M.D. Enhanced neurotrophin-induced axon growth in myelinated portions of the CNS in mice lacking the p75 neurotrophin receptor. J. Neurosci. 19 (1999) 4155-4168
53. Walsh G.S., Krol K.M., and Kawaja M.D. Absence of the p75 neurotrophin receptor alters the pattern of sympathosensory sprouting in the trigeminal ganglia of mice overexpressing nerve growth factor. J. Neurosci. 19 (1999) 258-273
54. Welcher A.A., Bitler C.M., Radeke M.J., and Shooter E.M. Nerve growth factor binding domain of the nerve growth factor receptor. Proc. Natl. Acad. Sci. U. S. A. 88 (1991) 159-163
55. Wilson K.L. The nuclear envelope, muscular dystrophy and gene expression. Trends Cell. Biol. 10 (2000) 125-129
56. Wilson S.M., Bhattacharyya B., Rachel R.A., Coppola V., Tessarollo L., Householder D.B., Fletcher C.F., Miller R.J., Copeland N.G., and Jenkins N.A. Synaptic defects in ataxia mice result from a mutation in Usp14, encoding a ubiquitin-specific protease. Nat. Genet. 32 (2002) 420-425
57. Wishart T.M., Paterson J.M., Short D.M., Meredith S., Robertson K.A., Sutherland C., Cousin M.A., Dutia M.B., and Gillingwater T.H. Differential proteomic analysis of synaptic proteins identifies potential cellular targets and protein mediators of synaptic neuroprotection conferred by the slow Wallerian degeneration (Wlds) gene. Mol. Cell. Proteomics 8 (2007) 1318-1330
58. Yan H., and Chao M.V. Disruption of cysteine-rich repeats of the p75 nerve growth factor receptor leads to loss of ligand binding. J. Biol. Chem. 266 (1991) 12099-12104
59. Ye H., Kuruvilla R., Zweifel L.S., and Ginty D.D. Evidence in support of signaling endosome-based retrograde survival of sympathetic neurons. Neuron 39 (2003) 57-68
60. Zapf-Colby A., and Olefsky J.M. Nerve growth factor processing and trafficking events following TrkA-mediated endocytosis. Endocrinology 139 (1998) 3232-3240
61. Zhou X.F., Rush R.A., and McLachlan E.M. Differential expression of the p75 nerve growth factor receptor in glia and neurons of the rat dorsal root ganglia after peripheral nerve transection. J. Neurosci. 16 (1996) 2901-2911