Divergent patterns of cytosolic TDP-43 and neuronal progranulin expression following axotomy: Implications for TDP-43 in the physiological response to neuronal injury

Brain Research

Volumn 1249, Issue , 2009, Pages 202-211

  Moisse, Katie ^a,b   Volkening, Kathryn ^a   Leystra Lantz, Cheryl ^a   Welch, Ian ^a,b   Hill, Tracy ^b   Strong, Michael J ^a,b  

^a ROBARTS RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

Amyotrophic lateral sclerosis; Axotomy; Microglia; Progranulin; RNA granule; TDP 43

Indexed keywords

CASPASE 3; PROGRANULIN; TAR DNA BINDING PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; C57BL 6 MOUSE; COGNITION; CONFOCAL MICROSCOPY; CYTOSOL; IMMUNOCOMPETENT CELL; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; INFLAMMATION; MICROGLIA; MOUSE; NERVE CELL LESION; NERVE FIBER TRANSECTION; NONHUMAN; PHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; UPREGULATION; WESTERN BLOTTING;

ANALYSIS OF VARIANCE; ANIMALS; AXOTOMY; CASPASE 3; CYTOSOL; DNA-BINDING PROTEINS; FEMALE; IMMUNOHISTOCHEMISTRY; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; MICE, INBRED C57BL; MICROGLIA; MICROSCOPY, CONFOCAL; MOTOR NEURONS; RNA, MESSENGER; RNA-BINDING PROTEINS; SCIATIC NERVE; SPINAL CORD; UP-REGULATION;

MUS;

EID: 58049221032     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2008.10.021     Document Type: Article

References (42)

1. Ahmed Z., Mackenzie I.R., Hutton M.L., and Dickson D.W. Progranulin in frontotemporal lobar degeneration and neuroinflammation. J. Neuroinflammation. 4 (2007) 7
2. Arai T., Hasegawa M., Akiyama H., Ikeda K., Nonaka T., Mori H., Mann D., Tsuchiya K., Yoshida M., Hashizume Y., and Oda T. TDP-43 is a component of ubiquitin-positive tau-negative inclusions in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Biochem. Biophys. Res. Commun. 351 (2006) 602-611
3. Baker M., Mackenzie I.R., Pickering-Brown S.M., Gass J., Rademakers R., Lindholm C., Snowden J., Adamson J., Sadovnick A.D., Rollinson S., Cannon A., Dwosh E., Neary D., Melquist S., Richardson A., Dickson D., Berger Z., Eriksen J., Robinson T., Zehr C., Dickey C.A., Crook R., McGowan E., Mann D., Boeve B., Feldman H., and Hutton M. Mutations in progranulin cause tau-negative frontotemporal dementia linked to chromosome 17. Nature 442 (2006) 916-919
4. Bergeron C., Beric-Maskarel K., Muntasser S., Weyer L., Somerville M., and Percy M.E. Neurofilament light and polyadenylated mRNA levels are decreased in amyotrophic lateral sclerosis motor neurons. J. Neuropathol. Exp. Neurol. 53 (1994) 221-230
5. Buratti E., and Baralle F.E. Multiple roles of TDP-43 in gene expression, splicing regulation, and human disease. Front Biosci. 13 (2008) 867-878
6. Cruts M., and Van B.C. Loss of progranulin function in frontotemporal lobar degeneration. Trends Genet. 24 (2008) 186-194
7. Cruts M., Gijselinck I., van der Z.J., Engelborghs S., Wils H., Pirici D., Rademakers R., Vandenberghe R., Dermaut B., Martin J.J., van D.C., Peeters K., Sciot R., Santens P., De P.T., Mattheijssens M., Van den B.M., Cuijt I., Vennekens K., De Deyn P.P., Kumar-Singh S., and Van B.C. Null mutations in progranulin cause ubiquitin-positive frontotemporal dementia linked to chromosome 17q21. Nature 442 (2006) 920-924
8. Cruts M., Kumar-Singh S., and Van B.C. Progranulin mutations in ubiquitin-positive frontotemporal dementia linked to chromosome 17q21. Curr. Alzheimer Res. 3 (2006) 485-491
9. Elvira G., Wasiak S., Blandford V., Tong X.-K., Serrano A., Fan X., del Rayo Sánchez-Carbente M., Servant F., Bell A.W., Boismenu D., Lacaille J.-C., McPherson P.S., DesGroseillers L., and Sossing W.S. Characterization of an RNA granule from developing brain. Mol. Cell. Proteomics 5 (2006) 635-651
10. Eriksen J.L., and Mackenzie I.R. Progranulin: normal function and role in neurodegeneration. J. Neurochem. 104 (2008) 287-297
11. Ge W.W., Volkening K., Leystra-Lantz C., Jaffe H., and Strong M.J. 14-3-3 protein binds to the low molecular weight neurofilament (NFL) mRNA 3′ UTR. Mol. Cell Neurosci. 34 (2007) 80-87
12. Geser F., Brandmeir N.J., Kwong L.K., Martinez-Lage M., Elman L., McCluskey L., Xie S.X., Lee V.M., and Trojanowski J.Q. Evidence of multisystem disorder in whole-brain map of pathological TDP-43 in amyotrophic lateral sclerosis. Arch. Neurol. 65 (2008) 636-641
13. Goldstein M.E., Weiss S.R., Lazzarini R.A., Shneidman P.S., Lees J.F., and Schlaepfer W.W. mRNA levels of all three neurofilament proteins decline following nerve transection. Brain Res. 427 (1988) 287-291
14. Hoffman P.N., Pollock S.C., and Striph G.G. Altered gene expression after optic nerve transection: reduced neurofilament expression as a general response to axonal injury. Exp. Neurol. 119 (1993) 32-36
15. Inukai Y., Nonaka T., Arai T., Yoshida M., Hashizume Y., Beach T.G., Buratti E., Baralle F.E., Akiyama H., Hisanaga S.I., and Hasegawa M. Abnormal phosphorylation of Ser409/410 of TDP-43 in FTLD-U and ALS. FEBS Lett. 582 (2008) 2899-2904
16. Kabashi E., Valdmanis P.N., Dion P., Spiegelman D., McConkey B.J., Vande V.C., Bouchard J.P., Lacomblez L., Pochigaeva K., Salachas F., Pradat P.F., Camu W., Meininger V., Dupre N., and Rouleau G.A. TARDBP mutations in individuals with sporadic and familial amyotrophic lateral sclerosis. Nat. Genet. 40 (2008) 572-574
17. Lariviere R.C., and Julien J.P. Functions of intermediate filaments in neuronal development and disease. J. Neurobiol. 58 (2004) 131-148
18. Lieberman A.R. The axon reaction: a review of the principal features of perikaryal responses to axon injury. Int. Rev. Neurobiol. 14 (1971) 49-124
19. Mackenzie I.R., Baker M., Pickering-Brown S., Hsiung G.Y., Lindholm C., Dwosh E., Gass J., Cannon A., Rademakers R., Hutton M., and Feldman H.H. The neuropathology of frontotemporal lobar degeneration caused by mutations in the progranulin gene. Brain 129 (2006) 3081-3090
20. Marsala M., and Yaksh T.L. Transient spinal ischemia in the rat: characterization of behavioral and histopathological consequences as a function of the duration of aortic occlusion. J. Cereb. Blood Flow Metab. 14 (1994) 526-535
21. Menzies F.M., Grierson A.J., Cookson M.R., Heath P.R., Tomkins J., Figlewicz D.A., Ince P.G., and Shaw P.J. Selective loss of neurofilament expression in Cu/Zn superoxide dismutase (SOD1) linked amyotrophic lateral sclerosis. J. Neurochem. 82 (2002) 1118-1128
22. Mishra M., Paunesku T., Woloschak G.E., Siddique T., Zhu L., Lin S., Greco K., and Bigio E.H. Gene expression analysis of frontotemporal lobar degeneration of the motor neuron disease type with ubiquitinated inclusions. Acta Neuropathol. 114 (2007) 81-94
23. Moisse K., and Strong M.J. Innate immunity in amyotrophic lateral sclerosis. Biochim. Biophys. Acta 1762 (2006) 1083-1093
24. Mukherjee O., Pastor P., Cairns N.J., Chakraverty S., Kauwe J.S., Shears S., Behrens M.I., Budde J., Hinrichs A.L., Norton J., Levitch D., Taylor-Reinwald L., Gitcho M., Tu P.H., Tenenholz G.L., Liscic R.M., Armendariz J., Morris J.C., and Goate A.M. HDDD2 is a familial frontotemporal lobar degeneration with ubiquitin-positive, tau-negative inclusions caused by a missense mutation in the signal peptide of progranulin. Ann. Neurol. 60 (2006) 314-322
25. Muma N.A., Hoffman P.N., Slunt H.H., Applegate M.D., Lieberburg I., and Price D.L. Alterations in levels of mRNAs coding for neurofilament protein subunits during regeneration. Exp. Neurol. 107 (1990) 230-235
26. Neumann M., Sampathu D.M., Kwong L.K., Truax A.C., Micsenyi M.C., Chou T.T., Bruce J., Schuck T., Grossman M., Clark C.M., McCluskey L.F., Miller B.L., Masliah E., Mackenzie I.R., Feldman H., Feiden W., Kretzschmar H.A., Trojanowski J.Q., and Lee V.M. Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science 314 (2006) 130-133
27. Price D.L., and Porter K.R. The response of ventral horn neurons to axonal transection. J. Cell Biol. 53 (1972) 24-37
28. Rosen D.R., Siddique T., Patterson D., Figlewicz D.A., Sapp P., Hentati A., Donaldson D., Goto J., O'Regan J.P., and Deng H.X. Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 362 (1993) 59-62
29. Schymick J.C., Yang Y., Andersen P.M., Vonsattel J.P., Greenway M., Momeni P., Elder J., Chio A., Restagno G., Robberecht W., Dahlberg C., Mukherjee O., Goate A., Graff-Radford N., Caselli R.J., Hutton M., Gass J., Cannon A., Rademakers R., Singleton A.B., Hardiman O., Rothstein J., Hardy J., and Traynor B.J. Progranulin mutations and amyotrophic lateral sclerosis or amyotrophic lateral sclerosis-frontotemporal dementia phenotypes. J. Neurol. Neurosurg. Psychiatry 78 (2007) 754-756
30. Shankaran S.S., Capell A., Hruscha A.T., Fellerer K., Neumann M., Schmid B., and Haass C. Missense mutations in the progranulin gene linked to frontotemporal lobar degeneration with ubiquitin-immunoreactive inclusions reduce progranulin production and secretion. J. Biol. Chem. 283 (2008) 1744-1753
31. Sreedharan J., Blair I.P., Tripathi V.B., Hu X., Vance C., Rogelj B., Ackerley S., Durnall J.C., Williams K.L., Buratti E., Baralle F., de B.J., Mitchell J.D., Leigh P.N., Al-Chalabi A., Miller C.C., Nicholson G., and Shaw C.E. TDP-43 mutations in familial and sporadic amyotrophic lateral sclerosis. Science 319 (2008) 1668-1672
32. Strong M.J. Neurofilament metabolism in sporadic amyotrophic lateral sclerosis. J. Neurol. Sci. 169 (1999) 170-177
33. Strong M.J. The evidence for ALS as a multisystems disorder of limited phenotypic expression. Can. J. Neurol. Sci. 28 (2001) 283-298
34. Strong M.J., Kesavapany S., and Pant H.C. The pathobiology of amyotrophic lateral sclerosis: a proteinopathy?. J. Neuropathol. Exp. Neurol. 64 (2005) 649-664
35. Strong M.J., Volkening K., Hammond R., Yang W., Strong W., Leystra-Lantz C., and Shoesmith C. TDP43 is a human low molecular weight neurofilament (hNFL) mRNA-binding protein. Mol. Cell Neurosci. 35 (2007) 320-327
36. Tetzlaff W., Bisby M.A., and Kreutzberg G.W. Changes in cytoskeletal proteins in the rat facial nucleus following axotomy. J. Neurosci. 8 (1988) 3181-3189
37. Wang J., Xu G., Slunt H.H., Gonzales V., Coonfield M., Fromholt D., Copeland N.G., Jenkins N.A., and Borchelt D.R. Coincident thresholds of mutant protein for paralytic disease and protein aggregation caused by restrictively expressed superoxide dismutase cDNA. Neurobiol. Dis. 20 (2005) 943-952
38. Wang I.F., Wu L.S., Chang H.Y., and Shen C.K. TDP-43, the signature protein of FTLD-U, is a neuronal activity-responsive factor. J. Neurochem. 105 (2008) 797-806
39. Watson W.E. Cellular responses to axotomy and to related procedures. Br. Med. Bull. 30 (1974) 112-115
40. Winton M.J., Igaz L.M., Wong M.M., Kwong L.K., Trojanowski J.Q., and Lee V.M.Y. Disturbance of nuclear and cytoplasmic TAR DNA binding protein (TDP-43) induces disease-like redistribution, sequestration and aggregate formation. J. Biol. Chem 283 (2008) 13302-13309
41. Wong N.K., He B.P., and Strong M.J. Characterization of neuronal intermediate filament protein expression in cervical spinal motor neurons in sporadic amyotrophic lateral sclerosis (ALS). J. Neuropathol. Exp. Neurol. 59 (2000) 972-982
42. Zhang Y.J., Xu Y.F., Dickey C.A., Buratti E., Baralle F., Bailey R., Pickering-Brown S., Dickson D., and Petrucelli L. Progranulin mediates caspase-dependent cleavage of TAR DNA binding protein-43. J. Neurosci. 27 (2007) 10530-10534