Transcriptional profiling of the injured sciatic nerve of mice carrying the Wld(S) mutant gene: Identification of genes involved in neuroprotection, neuroinflammation, and nerve regeneration

Brain, Behavior, and Immunity

Volumn 24, Issue 8, 2010, Pages 1254-1267

  Barrette, Benoit ^a   Calvo, Ezéquiel ^a   Vallières, Nicolas ^a   Lacroix, Steve ^a  

^a LAVAL UNIVERSITY   (Canada)

Author keywords

Axotomy; Growth factor; Immunity; Lymphocyte; Macrophage; Microarray; Nervous system; Peripheral nerve injury; Schwann cell; Wallerian degeneration

Indexed keywords

ALPHA SYNUCLEIN; BETACELLULIN; CD22 ANTIGEN; FIBROBLAST GROWTH FACTOR 5; SONIC HEDGEHOG PROTEIN; TRANSCRIPTOME;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL ADHESION; ENCEPHALITIS; GENE; GENE EXPRESSION; GENE IDENTIFICATION; GENETIC REGULATION; GENETIC TRANSCRIPTION; IMMUNE SYSTEM; MACROPHAGE; MICROARRAY ANALYSIS; MOUSE; NERVE DEGENERATION; NERVE REGENERATION; NEUROPROTECTION; NONHUMAN; PERIPHERAL NERVE INJURY; PRIORITY JOURNAL; SCIATIC NERVE; UPREGULATION; WLD GENE;

ANIMALS; AXONS; AXOTOMY; CELL ADHESION; CLUSTER ANALYSIS; CYTOKINES; DNA, COMPLEMENTARY; GENE EXPRESSION PROFILING; IN SITU HYBRIDIZATION; MICE; MICE, INBRED C57BL; NERVE GROWTH FACTORS; NERVE REGENERATION; NERVE TISSUE PROTEINS; NERVOUS SYSTEM PHYSIOLOGICAL PHENOMENA; NEURITIS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RNA; SCIATIC NERVE;

EID: 77957237015     PISSN: 08891591     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbi.2010.07.249     Document Type: Article

References (89)

1. Adalbert R., Gillingwater T.H., Haley J.E., Bridge K., Beirowski B., Berek L., Wagner D., Grumme D., Thomson D., Celik A., Addicks K., Ribchester R.R., Coleman M.P. A rat model of slow Wallerian degeneration (WldS) with improved preservation of neuromuscular synapses. Eur. J. Neurosci. 2005, 21:271-277.
2. Avery M.A., Sheehan A.E., Kerr K.S., Wang J., Freeman M.R. Wld S requires Nmnat1 enzymatic activity and N16-VCP interactions to suppress Wallerian degeneration. J. Cell Biol. 2009, 184:501-513.
3. Barrette B., Hebert M.A., Filali M., Lafortune K., Vallieres N., Gowing G., Julien J.P., Lacroix S. Requirement of myeloid cells for axon regeneration. J. Neurosci. 2008, 28:9363-9376.
4. Bedford L., Hay D., Paine S., Rezvani N., Mee M., Lowe J., Mayer R.J. Is malfunction of the ubiquitin proteasome system the primary cause of alpha-synucleinopathies and other chronic human neurodegenerative disease?. Biochim. Biophys. Acta 2008, 1782:683-690.
5. Beirowski B., Adalbert R., Wagner D., Grumme D.S., Addicks K., Ribchester R.R., Coleman M.P. The progressive nature of Wallerian degeneration in wild-type and slow Wallerian degeneration (WldS) nerves. BMC Neurosci. 2005, 6:6.
6. Beirowski B., Babetto E., Gilley J., Mazzola F., Conforti L., Janeckova L., Magni G., Ribchester R.R., Coleman M.P. Non-nuclear Wld(S) determines its neuroprotective efficacy for axons and synapses in vivo. J. Neurosci. 2009, 29:653-668.
7. Beirowski B., Berek L., Adalbert R., Wagner D., Grumme D.S., Addicks K., Ribchester R.R., Coleman M.P. Quantitative and qualitative analysis of Wallerian degeneration using restricted axonal labelling in YFP-H mice. J. Neurosci. Methods 2004, 134:23-35.
8. Benjamini Y., Drai D., Elmer G., Kafkafi N., Golani I. Controlling the false discovery rate in behavior genetics research. Behav. Brain Res. 2001, 125:279-284.
9. Bisby M.A., Chen S. Delayed wallerian degeneration in sciatic nerves of C57BL/Ola mice is associated with impaired regeneration of sensory axons. Brain Res. 1990, 530:117-120.
10. Bisby M.A., Tetzlaff W., Brown M.C. Cell body response to injury in motoneurons and primary sensory neurons of a mutant mouse, Ola (Wld), in which Wallerian degeneration is delayed. J. Comp. Neurol. 1995, 359:653-662.
11. Bloechlinger S., Karchewski L.A., Woolf C.J. Dynamic changes in glypican-1 expression in dorsal root ganglion neurons after peripheral and central axonal injury. Eur. J. Neurosci. 2004, 19:1119-1132.
12. Boivin A., Pineau I., Barrette B., Filali M., Vallieres N., Rivest S., Lacroix S. Toll-like receptor signaling is critical for Wallerian degeneration and functional recovery after peripheral nerve injury. J. Neurosci. 2007, 27:12565-12576.
13. Brown M.C., Perry V.H., Lunn E.R., Gordon S., Heumann R. Macrophage dependence of peripheral sensory nerve regeneration: possible involvement of nerve growth factor. Neuron 1991, 6:359-370.
14. Broxmeyer H.E., Lu L., Platzer E., Feit C., Juliano L., Rubin B.Y. Comparative analysis of the influences of human gamma, alpha and beta interferons on human multipotential (CFU-GEMM), erythroid (BFU-E) and granulocyte-macrophage (CFU-GM) progenitor cells. J. Immunol. 1983, 131:1300-1305.
15. Chandra S., Gallardo G., Fernandez-Chacon R., Schluter O.M., Sudhof T.C. Alpha-synuclein cooperates with CSPalpha in preventing neurodegeneration. Cell 2005, 123:383-396.
16. Chen S., Bisby M.A. Impaired motor axon regeneration in the C57BL/Ola mouse. J. Comp. Neurol. 1993, 333:449-454.
17. Coleman M. Axon degeneration mechanisms: commonality amid diversity. Nat. Rev. Neurosci. 2005, 6:889-898.
18. Coleman M.P., Freeman M.R. Wallerian degeneration, Wld(S), and Nmnat. Annu. Rev. Neurosci. 2010, 33:245-267.
19. Conforti L., Wilbrey A., Morreale G., Janeckova L., Beirowski B., Adalbert R., Mazzola F., Di Stefano M., Hartley R., Babetto E., Smith T., Gilley J., Billington R.A., Genazzani A.A., Ribchester R.R., Magni G., Coleman M. Wld S protein requires Nmnat activity and a short N-terminal sequence to protect axons in mice. J. Cell Biol. 2009, 184:491-500.
20. Dubyak G.R. Both sides now: multiple interactions of ATP with pannexin-1 hemichannels. Focus on " A permeant regulating its permeation pore: inhibition of pannexin 1 channels by ATP" Am. J. Physiol. Cell Physiol. 2009, 296:C235-C241.
21. Dufton N., Hannon R., Brancaleone V., Dalli J., Patel H.B., Gray M., D'Acquisto F., Buckingham J.C., Perretti M., Flower R.J. Anti-inflammatory role of the murine formyl-peptide receptor 2: ligand-specific effects on leukocyte responses and experimental inflammation. J. Immunol. 2010, 184:2611-2619.
22. Emmanouilidou E., Melachroinou K., Roumeliotis T., Garbis S.D., Ntzouni M., Margaritis L.H., Stefanis L., Vekrellis K. Cell-produced alpha-synuclein is secreted in a calcium-dependent manner by exosomes and impacts neuronal survival. J. Neurosci. 2010, 30:6838-6851.
23. Fridlender Z.G., Sun J., Kim S., Kapoor V., Cheng G., Ling L., Worthen G.S., Albelda S.M. Polarization of tumor-associated neutrophil phenotype by TGF-beta: " N1" versus " N2" TAN. Cancer Cell 2009, 16:183-194.
24. Fruttiger M., Schachner M., Martini R. Tenascin-C expression during wallerian degeneration in C57BL/Wlds mice: possible implications for axonal regeneration. J. Neurocytol. 1995, 24:1-14.
25. Fry E.J., Chagnon M.J., Lopez-Vales R., Tremblay M.L., David S. Corticospinal tract regeneration after spinal cord injury in receptor protein tyrosine phosphatase sigma deficient mice. Glia 2010, 58:423-433.
26. Fu S.Y., Gordon T. The cellular and molecular basis of peripheral nerve regeneration. Mol. Neurobiol. 1997, 14:67-116.
27. Fujino T., Wu Z., Lin W.C., Phillips M.A., Nedivi E. Cpg15 and cpg15-2 constitute a family of activity-regulated ligands expressed differentially in the nervous system to promote neurite growth and neuronal survival. J. Comp. Neurol. 2008, 507:1831-1845.
28. Gautier L., Cope L., Bolstad B.M., Irizarry R.A. Affy-analysis of Affymetrix GeneChip data at the probe level. Bioinformatics 2004, 20:307-315.
29. Gil O.D., Zanazzi G., Struyk A.F., Salzer J.L. Neurotrimin mediates bifunctional effects on neurite outgrowth via homophilic and heterophilic interactions. J. Neurosci. 1998, 18:9312-9325.
30. Gillingwater T.H., Wishart T.M., Chen P.E., Haley J.E., Robertson K., MacDonald S.H., Middleton S., Wawrowski K., Shipston M.J., Melmed S., Wyllie D.J., Skehel P.A., Coleman M.P., Ribchester R.R. The neuroprotective WldS gene regulates expression of PTTG1 and erythroid differentiation regulator 1-like gene in mice and human cells. Hum. Mol. Genet. 2006, 15:625-635.
31. Glass J.D., Brushart T.M., George E.B., Griffin J.W. Prolonged survival of transected nerve fibres in C57BL/Ola mice is an intrinsic characteristic of the axon. J. Neurocytol. 1993, 22:311-321.
32. Gold B.G., Austin D.R., Storm-Dickerson T. Multiple signals underlie the axotomy-induced up-regulation of c-JUN in adult sensory neurons. Neurosci. Lett. 1994, 176:123-127.
33. Guntinas-Lichius O., Angelov D.N., Morellini F., Lenzen M., Skouras E., Schachner M., Irintchev A. Opposite impacts of tenascin-C and tenascin-R deficiency in mice on the functional outcome of facial nerve repair. Eur. J. Neurosci. 2005, 22:2171-2179.
34. Hafler D.A. Multiple sclerosis. J. Clin. Invest. 2004, 113:788-794.
35. Hoopfer E.D., McLaughlin T., Watts R.J., Schuldiner O., O'Leary D.D., Luo L. Wlds protection distinguishes axon degeneration following injury from naturally occurring developmental pruning. Neuron 2006, 50:883-895.
36. Hossain M.A., Russell J.C., O'Brien R., Laterra J. Neuronal pentraxin 1: a novel mediator of hypoxic-ischemic injury in neonatal brain. J. Neurosci. 2004, 24:4187-4196.
37. Irizarry R.A., Hobbs B., Collin F., Beazer-Barclay Y.D., Antonellis K.J., Scherf U., Speed T.P. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 2003, 4:249-264.
38. Kawai H., Yasuda H., Terada M., Omatsu-Kanbe M., Kikkawa R. Axonal contact regulates expression of alpha2 and beta2 isoforms of Na+, K+-ATPase in Schwann cells: adhesion molecules and nerve regeneration. J. Neurochem. 1997, 69:330-339.
39. Kim H.G., Hwang Y.P., Han E.H., Choi C.Y., Yeo C.Y., Kim J.Y., Lee K.Y., Jeong H.G. Metallothionein-III provides neuronal protection through activation of nuclear factor-kappaB via the TrkA/phosphatidylinositol-3 kinase/Akt signaling pathway. Toxicol. Sci. 2009, 112:435-449.
40. Koumura A., Hamanaka J., Shimazawa M., Honda A., Tsuruma K., Uchida Y., Hozumi I., Satoh M., Inuzuka T., Hara H. Metallothionein-III knockout mice aggravates the neuronal damage after transient focal cerebral ischemia. Brain Res. 2009, 1292:148-154.
41. Larocque D., Fragoso G., Huang J., Mushynski W.E., Loignon M., Richard S., Almazan G. The QKI-6 and QKI-7 RNA binding proteins block proliferation and promote Schwann cell myelination. PLoS One 2009, 4:e5867.
42. Laser H., Conforti L., Morreale G., Mack T.G., Heyer M., Haley J.E., Wishart T.M., Beirowski B., Walker S.A., Haase G., Celik A., Adalbert R., Wagner D., Grumme D., Ribchester R.R., Plomann M., Coleman M.P. The slow Wallerian degeneration protein, WldS, binds directly to VCP/p97 and partially redistributes it within the nucleus. Mol. Biol. Cell 2006, 17:1075-1084.
43. Ligon K.L., Fancy S.P., Franklin R.J., Rowitch D.H. Olig gene function in CNS development and disease. Glia 2006, 54:1-10.
44. Lim S.H., Kwon S.K., Lee M.K., Moon J., Jeong D.G., Park E., Kim S.J., Park B.C., Lee S.C., Ryu S.E., Yu D.Y., Chung B.H., Kim E., Myung P.K., Lee J.R. Synapse formation regulated by protein tyrosine phosphatase receptor T through interaction with cell adhesion molecules and Fyn. EMBO J. 2009, 28:3564-3578.
45. Lin Q., Dong C., Cooper M.D. Impairment of T and B cell development by treatment with a type I interferon. J. Exp. Med. 1998, 187:79-87.
46. Liu B., Suyeoka G., Papa S., Franzoso G., Neufeld A.H. Growth arrest and DNA damage protein 45b (Gadd45b) protects retinal ganglion cells from injuries. Neurobiol. Dis. 2009, 33:104-110.
47. Lunn E.R., Perry V.H., Brown M.C., Rosen H., Gordon S. Absence of Wallerian degeneration does not hinder regeneration in peripheral nerve. Eur. J. Neurosci. 1989, 1:27-33.
48. MacDonald J.M., Beach M.G., Porpiglia E., Sheehan A.E., Watts R.J., Freeman M.R. The Drosophila cell corpse engulfment receptor Draper mediates glial clearance of severed axons. Neuron 2006, 50:869-881.
49. Mack T.G., Reiner M., Beirowski B., Mi W., Emanuelli M., Wagner D., Thomson D., Gillingwater T., Court F., Conforti L., Fernando F.S., Tarlton A., Andressen C., Addicks K., Magni G., Ribchester R.R., Perry V.H., Coleman M.P. Wallerian degeneration of injured axons and synapses is delayed by a Ube4b/Nmnat chimeric gene. Nat. Neurosci. 2001, 4:1199-1206.
50. Magyar J.P., Bartsch U., Wang Z.Q., Howells N., Aguzzi A., Wagner E.F., Schachner M. Degeneration of neural cells in the central nervous system of mice deficient in the gene for the adhesion molecule on Glia, the beta 2 subunit of murine Na, K-ATPase. J. Cell Biol. 1994, 127:835-845.
51. Maness P.F., Schachner M. Neural recognition molecules of the immunoglobulin superfamily: signaling transducers of axon guidance and neuronal migration. Nat. Neurosci. 2007, 10:19-26.
52. Martinez F.O., Gordon S., Locati M., Mantovani A. Transcriptional profiling of the human monocyte-to-macrophage differentiation and polarization: new molecules and patterns of gene expression. J. Immunol. 2006, 177:7303-7311.
53. Martinon F., Mayor A., Tschopp J. The inflammasomes: guardians of the body. Annu. Rev. Immunol. 2009, 27:229-265.
54. Mazzucchelli R., Durum S.K. Interleukin-7 receptor expression: intelligent design. Nat. Rev. Immunol. 2007, 7:144-154.
55. Mirsky R., Woodhoo A., Parkinson D.B., Arthur-Farraj P., Bhaskaran A., Jessen K.R. Novel signals controlling embryonic Schwann cell development, myelination and dedifferentiation. J. Peripher. Nerv. Syst. 2008, 13:122-135.
56. Monaco S., Gehrmann J., Raivich G., Kreutzberg G.W. MHC-positive, ramified macrophages in the normal and injured rat peripheral nervous system. J. Neurocytol. 1992, 21:623-634.
57. Monk K.R., Naylor S.G., Glenn T.D., Mercurio S., Perlin J.R., Dominguez C., Moens C.B., Talbot W.S. A G protein-coupled receptor is essential for Schwann cells to initiate myelination. Science 2009, 325:1402-1405.
58. Moore R.N., Larsen H.S., Horohov D.W., Rouse B.T. Endogenous regulation of macrophage proliferative expansion by colony-stimulating factor-induced interferon. Science 1984, 223:178-181.
59. Muley P.D., McNeill E.M., Marzinke M.A., Knobel K.M., Barr M.M., Clagett-Dame M. The atRA-responsive gene neuron navigator 2 functions in neurite outgrowth and axonal elongation. Dev. Neurobiol. 2008, 68:1441-1453.
60. Parkinson D.B., Bhaskaran A., Arthur-Farraj P., Noon L.A., Woodhoo A., Lloyd A.C., Feltri M.L., Wrabetz L., Behrens A., Mirsky R., Jessen K.R. C-Jun is a negative regulator of myelination. J. Cell Biol. 2008, 181:625-637.
61. Pelegrin P., Surprenant A. Pannexin-1 mediates large pore formation and interleukin-1beta release by the ATP-gated P2X7 receptor. EMBO J. 2006, 25:5071-5082.
62. Perry V.H., Brown M.C., Lunn E.R. Very slow retrograde and Wallerian degeneration in the CNS of C57BL/Ola mice. Eur. J. Neurosci. 1991, 3:102-105.
63. Perry V.H., Brown M.C., Lunn E.R., Tree P., Gordon S. Evidence that very slow Wallerian degeneration in C57BL/Ola mice is an intrinsic property of the peripheral nerve. Eur. J. Neurosci. 1990, 2:802-808.
64. Pineau I., Barrette B., Vallières N., Lacroix S. A novel method for multiple labeling combining in situ hybridization with immunofluorescence. J. Histochem. Cytochem. 2006, 54:1303-1313.
65. Pineau I., Lacroix S. Endogenous signals initiating inflammation in the injured nervous system. Glia 2009, 57:351-361.
66. Reeves R. Nuclear functions of the HMG proteins. Biochim. Biophys. Acta 2010, 1799:3-14.
67. Reichert F., Saada A., Rotshenker S. Peripheral nerve injury induces Schwann cells to express two macrophage phenotypes: phagocytosis and the galactose-specific lectin MAC-2. J. Neurosci. 1994, 14:3231-3245.
68. Resnitzky D., Yarden A., Zipori D., Kimchi A. Autocrine beta-related interferon controls c-myc suppression and growth arrest during hematopoietic cell differentiation. Cell 1986, 46:31-40.
69. Riethmacher D., Sonnenberg-Riethmacher E., Brinkmann V., Yamaai T., Lewin G.R., Birchmeier C. Severe neuropathies in mice with targeted mutations in the ErbB3 receptor. Nature 1997, 389:725-730.
70. Ritson G.P., Custer S.K., Freibaum B.D., Guinto J.B., Geffel D., Moore J., Tang W., Winton M.J., Neumann M., Trojanowski J.Q., Lee V.M., Forman M.S., Taylor J.P. TDP-43 mediates degeneration in a novel Drosophila model of disease caused by mutations in VCP/p97. J. Neurosci. 2010, 30:7729-7739.
71. Saijo K., Winner B., Carson C.T., Collier J.G., Boyer L., Rosenfeld M.G., Gage F.H., Glass C.K. A Nurr1/CoREST pathway in microglia and astrocytes protects dopaminergic neurons from inflammation-induced death. Cell 2009, 137:47-59.
72. Sasaki Y., Vohra B.P., Baloh R.H., Milbrandt J. Transgenic mice expressing the Nmnat1 protein manifest robust delay in axonal degeneration in vivo. J. Neurosci. 2009, 29:6526-6534.
73. Schmidt H., Raasch J., Merkler D., Klinker F., Krauss S., Bruck W., Prinz M. Type I interferon receptor signalling is induced during demyelination while its function for myelin damage and repair is redundant. Exp. Neurol. 2009, 216:306-311.
74. Shen Y., Tenney A.P., Busch S.A., Horn K.P., Cuascut F.X., Liu K., He Z., Silver J., Flanagan J.G. PTPsigma is a receptor for chondroitin sulfate proteoglycan, an inhibitor of neural regeneration. Science 2009, 326:592-596.
75. Silverman W.R., de Rivero Vaccari J.P., Locovei S., Qiu F., Carlsson S.K., Scemes E., Keane R.W., Dahl G. The pannexin 1 channel activates the inflammasome in neurons and astrocytes. J. Biol. Chem. 2009, 284:18143-18151.
76. Smyth G.K. Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol. 2004, 3. Article 3.
77. Taylor A.M., Berchtold N.C., Perreau V.M., Tu C.H., Li Jeon N., Cotman C.W. Axonal mRNA in uninjured and regenerating cortical mammalian axons. J. Neurosci. 2009, 29:4697-4707.
78. Teige I., Treschow A., Teige A., Mattsson R., Navikas V., Leanderson T., Holmdahl R., Issazadeh-Navikas S. IFN-beta gene deletion leads to augmented and chronic demyelinating experimental autoimmune encephalomyelitis. J. Immunol. 2003, 170:4776-4784.
79. Theofilopoulos A.N., Baccala R., Beutler B., Kono D.H. Type I interferons (alpha/beta) in immunity and autoimmunity. Annu. Rev. Immunol. 2005, 23:307-336.
80. Trebst C., Heine S., Lienenklaus S., Lindner M., Baumgartner W., Weiss S., Stangel M. Lack of interferon-beta leads to accelerated remyelination in a toxic model of central nervous system demyelination. Acta Neuropathol. 2007, 114:587-596.
81. Vargas M.E., Barres B.A. Why is Wallerian degeneration in the CNS so slow?. Annu. Rev. Neurosci. 2007, 30:153-179.
82. Wang J., Lin Q., Langston H., Cooper M.D. Resident bone marrow macrophages produce type 1 interferons that can selectively inhibit interleukin-7-driven growth of B lineage cells. Immunity 1995, 3:475-484.
83. Wang J., Zhai Q., Chen Y., Lin E., Gu W., McBurney M.W., He Z. A local mechanism mediates NAD-dependent protection of axon degeneration. J. Cell Biol. 2005, 170:349-355.
84. Wettenhall J.M., Simpson K.M., Satterley K., Smyth G.K. AffylmGUI: a graphical user interface for linear modeling of single channel microarray data. Bioinformatics 2006, 22:897-899.
85. Willis D., Li K.W., Zheng J.Q., Chang J.H., Smit A., Kelly T., Merianda T.T., Sylvester J., van Minnen J., Twiss J.L. Differential transport and local translation of cytoskeletal, injury-response, and neurodegeneration protein mRNAs in axons. J. Neurosci. 2005, 25:778-791.
86. Wu H.H., Bellmunt E., Scheib J.L., Venegas V., Burkert C., Reichardt L.F., Zhou Z., Farinas I., Carter B.D. Glial precursors clear sensory neuron corpses during development via Jedi-1, an engulfment receptor. Nat. Neurosci. 2009, 12:1534-1541.
87. Yahata N., Yuasa S., Araki T. Nicotinamide mononucleotide adenylyltransferase expression in mitochondrial matrix delays Wallerian degeneration. J. Neurosci. 2009, 29:6276-6284.
88. Yong V.W. Metalloproteinases: mediators of pathology and regeneration in the CNS. Nat. Rev. Neurosci. 2005, 6:931-944.
89. Zhang X., Chen Y., Wang C., Huang L.Y. Neuronal somatic ATP release triggers neuron-satellite glial cell communication in dorsal root ganglia. Proc. Natl. Acad. Sci. USA 2007, 104:9864-9869.