Endoplasmic reticulum stress is accompanied by activation of NF-κB in amyotrophic lateral sclerosis

Journal of Neuroimmunology

Volumn 270, Issue 1-2, 2014, Pages 29-36

  Prell, T ^a   Lautenschlager J ^a   Weidemann, L ^a   Ruhmer, J ^a   Witte, O W ^a   Grosskreutz, J ^a  

^a JENA UNIVERSITY HOSPITAL   (Germany)

Author keywords

Endoplasmic reticulum stress; Motor neuron; NFkB; Superoxide dismutase; Unfolded protein response

Indexed keywords

ENDOPLASMIC RETICULUM STRESS; MOTOR NEURON; NFKB; SUPEROXIDE DISMUTASE; UNFOLDED PROTEIN RESPONSE;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; BLOTTING, WESTERN; DISEASE MODELS, ANIMAL; ENDOPLASMIC RETICULUM STRESS; HUMANS; IMMUNOHISTOCHEMISTRY; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MOTOR NEURONS; MUTATION; NF-KAPPA B; SUPEROXIDE DISMUTASE; UNFOLDED PROTEIN RESPONSE;

EID: 84898773604     PISSN: 01655728     EISSN: 18728421     Source Type: Journal    
DOI: 10.1016/j.jneuroim.2014.03.005     Document Type: Article

References (59)

1. Al Chalabi A., Jones A., Troakes C., King A., Al Sarraj S., van den Berg L.H. The genetics and neuropathology of amyotrophic lateral sclerosis. Acta Neuropathol. 2012, 124(3):339-352.
2. Atkin J.D., Farg M.A., Walker A.K., McLean C., Tomas D., Horne M.K. Endoplasmic reticulum stress and induction of the unfolded protein response in human sporadic amyotrophic lateral sclerosis. Neurobiol. Dis. 2008, 30(3):400-407.
3. Carri M.T., Cozzolino M. SOD1 and mitochondria in ALS: a dangerous liaison. J. Bioenerg. Biomembr. 2011, 43(6):593-599.
4. Casciati A., Ferri A., Cozzolino M., Celsi F., Nencini M., Rotilio G., Carri M.T. Oxidative modulation of nuclear factor-kappaB in human cells expressing mutant fALS-typical superoxide dismutases. J. Neurochem. 2002, 83(5):1019-1029.
5. Cashman N.R., Durham H.D., Blusztajn J.K., Oda K., Tabira T., Shaw I.T., Dahrouge S., Antel J.P. Neuroblastoma x spinal cord (NSC) hybrid cell lines resemble developing motor neurons. Dev. Dyn. 1992, 194(3):209-221.
6. Chung Y.H., Joo K.M., Lim H.C., Cho M.H., Kim D., Lee W.B., Cha C.I. Immunohistochemical study on the distribution of phosphorylated extracellular signal-regulated kinase (ERK) in the central nervous system of SOD1G93A transgenic mice. Brain Res. 2005, 1050(1-2):203-209.
7. Cozzolino M., Carri M.T. Mitochondrial dysfunction in ALS. Prog. Neurobiol. 2012, 97(2):54-66.
8. Deng J., Lu P.D., Zhang Y., Scheuner D., Kaufman R.J., Sonenberg N., Harding H.P., Ron D. Translational repression mediates activation of nuclear factor kappa B by phosphorylated translation initiation factor 2. Mol. Cell. Biol. 2004, 24(23):10161-10168.
9. Dudek J., Benedix J., Cappel S., Greiner M., Jalal C., Muller L., Zimmermann R. Functions and pathologies of BiP and its interaction partners. Cell. Mol. Life Sci. 2009, 66(9):1556-1569.
10. Ferri A., Cozzolino M., Crosio C., Nencini M., Casciati A., Gralla E.B., Rotilio G., Valentine J.S., Carri M.T. Familial ALS-superoxide dismutases associate with mitochondria and shift their redox potentials. Proc. Natl. Acad. Sci. U. S. A. 2006, 103(37):13860-13865.
11. Ghosh G., Wang V.Y., Huang D.B., Fusco A. NF-kappaB regulation: lessons from structures. Immunol. Rev. 2012, 246(1):36-58.
12. Grosskreutz J., Van Den B.L., Keller B.U. Calcium dysregulation in amyotrophic lateral sclerosis. Cell Calcium 2010, 47(2):165-174.
13. Gurney M.E., Pu H., Chiu A.Y., Dal Canto M.C., Polchow C.Y., Alexander D.D., Caliendo J., Hentati A., Kwon Y.W., Deng H.X., et al. Motor neuron degeneration in mice that express a human Cu,Zn superoxide dismutase mutation. Science 1994, 264(5166):1772-1775.
14. Gutierrez H., Davies A.M. Regulation of neural process growth, elaboration and structural plasticity by NF-kappaB. Trends Neurosci. 2011, 34(6):316-325.
15. Haddad J.J. Antioxidant and prooxidant mechanisms in the regulation of redox(y)-sensitive transcription factors. Cell. Signal. 2002, 14(11):879-897.
16. Hayden M.S., Ghosh S. Signaling to NF-kappaB. Genes Dev. 2004, 18(18):2195-2224.
17. Hsiung G.Y., DeJesus-Hernandez M., Feldman H.H., Sengdy P., Bouchard-Kerr P., Dwosh E., Butler R., Leung B., Fok A., Rutherford N.J., Baker M., Rademakers R., Mackenzie I.R. Clinical and pathological features of familial frontotemporal dementia caused by C9ORF72 mutation on chromosome 9p. Brain 2012, 135(Pt 3):709-722.
18. Hu P., Han Z., Couvillon A.D., Kaufman R.J., Exton J.H. Autocrine tumor necrosis factor alpha links endoplasmic reticulum stress to the membrane death receptor pathway through IRE1alpha-mediated NF-kappaB activation and down-regulation of TRAF2 expression. Mol. Cell. Biol. 2006, 26(8):3071-3084.
19. Jiang H.Y., Wek S.A., McGrath B.C., Scheuner D., Kaufman R.J., Cavener D.R., Wek R.C. Phosphorylation of the alpha subunit of eukaryotic initiation factor 2 is required for activation of NF-kappaB in response to diverse cellular stresses. Mol. Cell. Biol. 2003, 23(16):5651-5663.
20. Jiang Y.M., Yamamoto M., Kobayashi Y., Yoshihara T., Liang Y., Terao S., Takeuchi H., Ishigaki S., Katsuno M., Adachi H., Niwa J., Tanaka F., Doyu M., Yoshida M., Hashizume Y., Sobue G. Gene expression profile of spinal motor neurons in sporadic amyotrophic lateral sclerosis. Ann. Neurol. 2005, 57(2):236-251.
21. Kaltschmidt B., Kaltschmidt C., Salminen A., Kauppinen A., Suuronen T., Kaarniranta K., Ojala J. NF-kappaB in the nervous system ER stress in Alzheimer's disease: a novel neuronal trigger for inflammation and Alzheimer's pathology. Cold Spring Harb. Perspect. Biol. 2009, 1(3):a001271.
22. Kato Y., Matsumura K., Kinosada Y., Narita Y., Kuzuhara S., Nakagawa T. Detection of pyramidal tract lesions in amyotrophic lateral sclerosis with magnetization-transfer measurements. AJNR Am. J. Neuroradiol. 1997, 18(8):1541-1547.
23. Kikuchi H., Almer G., Yamashita S., Guegan C., Nagai M., Xu Z., Sosunov A.A., McKhann G.M., Przedborski S. Spinal cord endoplasmic reticulum stress associated with a microsomal accumulation of mutant superoxide dismutase-1 in an ALS model. Proc. Natl. Acad. Sci. U. S. A. 2006, 103(15):6025-6030.
24. Kitamura M. Control of NF-kappaB and inflammation by the unfolded protein response. Int. Rev. Immunol. 2011, 30(1):4-15.
25. Kozutsumi Y., Segal M., Normington K., Gething M.J., Sambrook J. The presence of malfolded proteins in the endoplasmic reticulum signals the induction of glucose-regulated proteins. Nature 1988, 332(6163):462-464.
26. Lautenschlaeger J., Prell T., Grosskreutz J. Endoplasmic reticulum stress and the ER mitochondrial calcium cycle in amyotrophic lateral sclerosis. Amyotroph. Lateral Scler. 2012, 13(2):166-177.
27. Lautenschlager J., Prell T., Ruhmer J., Weidemann L., Witte O.W., Grosskreutz J. Overexpression of human mutated G93A SOD1 changes dynamics of the ER mitochondria calcium cycle specifically in mouse embryonic motor neurons. Exp. Neurol. 2013, 247C:91-100.
28. Lehnardt S., Massillon L., Follett P., Jensen F.E., Ratan R., Rosenberg P.A., Volpe J.J., Vartanian T. Activation of innate immunity in the CNS triggers neurodegeneration through a Toll-like receptor 4-dependent pathway. Proc. Natl. Acad. Sci. U. S. A. 2003, 100(14):8514-8519.
29. Listwak S.J., Rathore P., Herkenham M. Minimal NF-kappaB activity in neurons. Neuroscience 2013, 250:282-299.
30. Malhotra J.D., Kaufman R.J. Endoplasmic reticulum stress and oxidative stress: a vicious cycle or a double-edged sword?. Antioxid. Redox Signal. 2007, 9(12):2277-2293.
31. Mattson M.P. NF-kappaB in the survival and plasticity of neurons. Neurochem. Res. 2005, 30(6-7):883-893.
32. Meyer M., Caselmann W.H., Schluter V., Schreck R., Hofschneider P.H., Baeuerle P.A. Hepatitis B virus transactivator MHBst: activation of NF-kappa B, selective inhibition by antioxidants and integral membrane localization. EMBO J. 1992, 11(8):2991-3001.
33. Migheli A., Piva R., Atzori C., Troost D., Schiffer D. c-Jun, JNK/SAPK kinases and transcription factor NF-kappa B are selectively activated in astrocytes, but not motor neurons, in amyotrophic lateral sclerosis. J. Neuropathol. Exp. Neurol. 1997, 56(12):1314-1322.
34. Mincheva-Tasheva S., Soler R.M. NF-kappaB signaling pathways: role in nervous system physiology and pathology. Neuroscientist 2013, 19(2):175-194.
35. Nagata T., Ilieva H., Murakami T., Shiote M., Narai H., Ohta Y., Hayashi T., Shoji M., Abe K. Increased ER stress during motor neuron degeneration in a transgenic mouse model of amyotrophic lateral sclerosis. Neurol. Res. 2007, 29(8):767-771.
36. Nakagawa T., Zhu H., Morishima N., Li E., Xu J., Yankner B.A., Yuan J. Caspase-12 mediates endoplasmic-reticulum-specific apoptosis and cytotoxicity by amyloid-beta. Nature 2000, 403(6765):98-103.
37. Nishitoh H., Kadowaki H., Nagai A., Maruyama T., Yokota T., Fukutomi H., Noguchi T., Matsuzawa A., Takeda K., Ichijo H. ALS-linked mutant SOD1 induces ER stress- and ASK1-dependent motor neuron death by targeting Derlin-1. Genes Dev. 2008, 22(11):1451-1464.
38. Pahl H.L., Baeuerle P.A. Expression of influenza virus hemagglutinin activates transcription factor NF-kappa B. J. Virol. 1995, 69(3):1480-1484.
39. Parakh S., Spencer D.M., Halloran M.A., Soo K.Y., Atkin J.D. Redox regulation in amyotrophic lateral sclerosis. Oxidative Med. Cell. Longev. 2013, 2013:408681.
40. Philips T., Robberecht W. Neuroinflammation in amyotrophic lateral sclerosis: role of glial activation in motor neuron disease. Lancet Neurol. 2011, 10(3):253-263.
41. Prell T., Lautenschlager J., Witte O.W., Carri M.T., Grosskreutz J. The unfolded protein response in models of human mutant G93A amyotrophic lateral sclerosis. Eur. J. Neurosci. 2012, 35(5):652-660.
42. Pyo J.S., Ko Y.S., Kim W.H., Kim M., Lee K.W., Nam S.Y., Chung H.Y., Cho S.J., Baik T.K., Lee B.L. Impairment of nuclear factor-kappaB activation increased glutamate excitotoxicity in a motoneuron-neuroblastoma hybrid cell line expressing mutant (G93A) Cu/Zn-superoxide dismutase. J. Neurosci. Res. 2010, 88(11):2494-2503.
43. Renton A.E., Majounie E., Waite A., Simon-Sanchez J., Rollinson S., Gibbs J.R., Schymick J.C., Laaksovirta H., van Swieten J.C., Myllykangas L., Kalimo H., Paetau A., Abramzon Y., Remes A.M., Kaganovich A., Scholz S.W., Duckworth J., Ding J., Harmer D.W., Hernandez D.G., Johnson J.O., Mok K., Ryten M., Trabzuni D., Guerreiro R.J., Orrell R.W., Neal J., Murray A., Pearson J., Jansen I.E., Sondervan D., Seelaar H., Blake D., Young K., Halliwell N., Callister J.B., Toulson G., Richardson A., Gerhard A., Snowden J., Mann D., Neary D., Nalls M.A., Peuralinna T., Jansson L., Isoviita V.M., Kaivorinne A.L., Holtta-Vuori M., Ikonen E., Sulkava R., Benatar M., Wuu J., Chio A., Restagno G., Borghero G., Sabatelli M., Heckerman D., Rogaeva E., Zinman L., Rothstein J.D., Sendtner M., Drepper C., Eichler E.E., Alkan C., Abdullaev Z., Pack S.D., Dutra A., Pak E., Hardy J., Singleton A., Williams N.M., Heutink P., Pickering-Brown S., Morris H.R., Tienari P.J., Traynor B.J. A hexanucleotide repeat expansion in C9ORF72 is the cause of chromosome 9p21-linked ALS-FTD. Neuron 2011, 72(2):257-268.
44. Rosen D.R., Siddique T., Patterson D., Figlewicz D.A., Sapp P., Hentati A., Donaldson D., Goto J., O'Regan J.P., Deng H.X., et al. Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 1993, 362(6415):59-62.
45. Rothstein J.D. Current hypotheses for the underlying biology of amyotrophic lateral sclerosis. Ann. Neurol. 2009, 65(Suppl. 1):S3-S9.
46. Saccon R.A., Bunton-Stasyshyn R.K., Fisher E.M., Fratta P. Is SOD1 loss of function involved in amyotrophic lateral sclerosis?. Brain 2013, 136(Pt 8):2342-2358.
47. Salminen A., Kauppinen A., Suuronen T., Kaarniranta K., Ojala J. ER stress in Alzheimer's disease: a novel neuronal trigger for inflammation and Alzheimer's pathology. J. Neuroinflammation 2009, 6:41.
48. Shaw B.F., Valentine J.S. How do ALS-associated mutations in superoxide dismutase 1 promote aggregation of the protein?. Trends Biochem. Sci. 2007, 32(2):78-85.
49. Tam A.B., Mercado E.L., Hoffmann A., Niwa M. ER stress activates NF-kappaB by integrating functions of basal IKK activity, IRE1 and PERK. PLoS One 2012, 7(10):e45078.
50. Urano F., Wang X., Bertolotti A., Zhang Y., Chung P., Harding H.P., Ron D. Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 2000, 287(5453):664-666.
51. Van Damme P., Callewaert G., Eggermont J., Robberecht W., Van Den Bosch L. Chloride influx aggravates Ca2+-dependent AMPA receptor-mediated motoneuron death. J. Neurosci. 2003, 23(12):4942-4950.
52. Van Den Bosch L., Vandenberghe W., Klaassen H., Van Houtte E., Robberecht W. Ca(2+)-permeable AMPA receptors and selective vulnerability of motor neurons. J. Neurol. Sci. 2000, 180(1-2):29-34.
53. Verkhratsky A. Physiology and pathophysiology of the calcium store in the endoplasmic reticulum of neurons. Physiol. Rev. 2005, 85(1):201-279.
54. Vijayalakshmi K., Alladi P.A., Ghosh S., Prasanna V.K., Sagar B.C., Nalini A., Sathyaprabha T.N., Raju T.R. Evidence of endoplasmic reticular stress in the spinal motor neurons exposed to CSF from sporadic amyotrophic lateral sclerosis patients. Neurobiol. Dis. 2011, 41(3):695-705.
55. Walker A.K. Protein disulfide isomerase and the endoplasmic reticulum in amyotrophic lateral sclerosis. J. Neurosci. 2010, 30(11):3865-3867.
56. Wang L., Popko B., Roos R.P. The unfolded protein response in familial amyotrophic lateral sclerosis. Hum. Mol. Genet. 2011, 20(5):1008-1015.
57. Yoshida H., Matsui T., Yamamoto A., Okada T., Mori K. XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell 2001, 107(7):881-891.
58. Zhang K. Integration of ER stress, oxidative stress and the inflammatory response in health and disease. Int. J. Clin. Exp. Med. 2010, 3(1):33-40.
59. Zhang K., Kaufman R.J. From endoplasmic-reticulum stress to the inflammatory response. Nature 2008, 454(7203):455-462.