Attenuating the endoplasmic reticulum stress response improves functional recovery after spinal cord injury

GLIA

Volumn 59, Issue 10, 2011, Pages 1489-1502

  Ohri, Sujata Saraswat ^a   Maddie, Melissa A ^a   Zhao, Yongmei ^a,b   Qiu, Mengsheng S ^a   Hetman, Michal ^a   Whittemore, Scott R ^a  

^a University of Louisville School of Medicine   (United States)

^b CAPITAL MEDICAL UNIVERSITY   (China)

Author keywords

Contusion; ER stress; Locomoter activity; Oligodendrocyte; Spinal cord injury; White matter sparing

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 4; BIOLOGICAL MARKER; CLAUDIN 11; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; MESSENGER RNA; MYELIN BASIC PROTEIN; X BOX BINDING PROTEIN 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; CONVALESCENCE; ENDOPLASMIC RETICULUM STRESS; FEMALE; IMMUNOHISTOCHEMISTRY; MACROGLIA; MOUSE; NERVE CELL; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SPINAL CORD INJURY; UNFOLDED PROTEIN RESPONSE; UPREGULATION; WHITE MATTER;

ACTIVATING TRANSCRIPTION FACTOR 4; ANALYSIS OF VARIANCE; ANIMALS; APOPTOSIS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CASPASE 3; DISEASE MODELS, ANIMAL; DNA-BINDING PROTEINS; ENDOPLASMIC RETICULUM STRESS; EUKARYOTIC INITIATION FACTOR-2; FEMALE; LOCOMOTION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYELIN BASIC PROTEINS; NERVE FIBERS, MYELINATED; NERVE TISSUE PROTEINS; OLIGODENDROGLIA; RECOVERY OF FUNCTION; RNA, MESSENGER; SPINAL CORD INJURIES; TIME FACTORS; TRANSCRIPTION FACTOR CHOP; TRANSCRIPTION FACTORS; UNFOLDED PROTEIN RESPONSE; UP-REGULATION;

EID: 79960704499     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.21191     Document Type: Article

References (56)

1. Aksenova M, Butterfield DA, Zhang SX, Underwood M, Geddes JW. 2002. Increased protein oxidation and decreased creatine kinase BB expression and activity after spinal cord contusion injury. J Neurotrauma 19: 491-502.
2. Aufenberg C, Wenkel S, Mautes A, Paschen W. 2005. Spinal cord trauma activates processing of XBP1 mRNA indicative of endoplasmic reticulum dysfunction. J Neurotrauma 22: 1018-1024.
3. Basso DM, Fisher LC, Anderson AJ, Jakeman LB, McTigue DM, Popovich PG. 2006. Basso mouse scale for locomotion detects differences in recovery after spinal cord injury in five common mouse strains. J Neurotrauma 23: 635-659.
4. Benton RL, Maddie MA, Minnillo DR, Hagg T, Whittemore SR. 2008. Griffonia simplicifolia isolectin B4 identifies a specific subpopulation of angiogenic blood vessels following contusive spinal cord injury in the adult mouse. J Comp Neurol 507: 1031-1052.
5. Cao Q, He Q, Wang Y, Cheng X, Howard RM, Zhang Y, DeVries WH, Shields CB, Magnuson DS, Xu XM, Kim DH, Whittemore SR. 2010. Transplantation of ciliary neurotrophic factor-expressing adult oligodendrocyte precursor cells promotes remyelination and functional recovery after spinal cord injury. J Neurosci 30: 2989-3001.
6. Casha S, Yu WR, Fehlings MG. 2001. Oligodendroglial apoptosis occurs along degenerating axons and is associated with FAS, p75 expression following spinal cord injury in the rat. Neuroscience 103: 203-218.
7. Coggeshall RE, Lekan HA. 1996. Methods for determining numbers of cells and synapses: A case for more uniform standards of review. J Comp Neurol 364: 6-15.
8. Fassbender JM, Myers SA, Whittemore SR. 2011. Activating Notch signaling post-SCI modulates angiogenesis in penumbral vascular beds but does not improve hindlimb locomoter recovery. Exp Neurol 227: 302-313.
9. Faulkner JR, Hermann JE, Woo MJ, Tansey KE. 2004. Reactive astrocytes protect tissue and preserve function after spinal cord injury. J Neurosci 24: 2143-2155.
10. Fu H, Qi Y, Tan m, Cai J, Takebayashi H, Nakafuku M, Richardson W, Qiu M. 2002. Dual origin of spinal oligodendrocyte progenitors and evidence for the cooperative role of Olig2 and NKx2.2 in the control of oligodendrocyte differentiation. Development 129: 681-693.
11. Gargalovic PS, Gharavi NM, Clark MJ, Pagnon J, Yang WP, He A, Truong A, Baruch-Oren T, Berliner JA, Kirchgessner TG, Lusis AJ. 2006. The unfolded protein response is an important regulator of inflammatory genes in endothelial cells. Arterioscler Thromb Vasc Biol 26: 2490-2496.
12. Hagg T, Oudega M. 2006. Degenerative and spontaneous regenerative processes after spinal cord injury. J Neurotrauma 23: 264-280.
13. Harding HP, Calfon M, Urano F, Novoa I, Ron D. 2002. Transcriptional and translational control in the mammalian unfolded protein response. Annu Rev Cell Dev Biol 18: 575-599.
14. Harding HP, Novo II, Zhang Y, Zeng H, Wek R, Schapira M, Ron D. 2000. Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol Cell 6: 1099-1108.
15. Hayashi T, Saito A, Okuno S, Ferrand-Drake M, Chan PH. 2003. Induction of GRP78 by ischemic preconditioning reduces endoplasmic reticulum stress and prevents delayed neuronal cell death. J Cereb Blood Flow Metab 23: 949-961.
16. Haze K, Yoshida H, Yanagi H, Yura T, Mori K. 1999. Mammalian transcription factor ATF6 is synthesized as a transmembrane protein and activated by proteolysis in response to endoplasmic reticulum stress. Mol Biol Cell 10: 3787-3799.
17. Holtz WA, O'Malley KL. 2003. Parkinsonian mimetics induce aspects of unfolded protein response in death of dopaminergic neurons. J Biol Chem 23: 19367-19377.
18. Hinnebusch AG. 1997. Translational regulation of yeast GCN4. A window on factors that control initiator-trna binding to the ribosome. J Biol Chem 272: 21661-21664.
19. Hirota M, Kitagaki M, Itagaki H, Aiba S. 2006. Quantitative measurement of spliced XBP1 mRNA as an indicator of ER stress. J Toxicol Sci 31: 149-156.
20. Kohno K, Higuchi T, Ohta S, Kumon Y, Sakaki S. 1997. Neuroprotective nitric oxide synthase inhibitor reduces intracellular calcium accumulation following transient global ischemia in the gerbil. Neurosci Lett 224: 17-20.
21. Kollenburg van B, Dijk van J, Garbern J, Thomas AAM, Scheper GC, Powers JM, Knaap van der MS. 2006. Glia-specific activation of all pathways of the unfolded protein response in vanishing white matter disease. J Neuropathol Exp Neurol 65: 707-715.
22. Lange PS, Chavez JC, Pinto JT, Coppola G, Sun CW, Townes TM, Geschwind DH, Ratan RR. 2008. ATF4 is an oxidative stress-inducible, prodeath transcription factor in neurons in vitro and in vivo. J Exp Med 205: 1227-1242.
23. Lasiene J, Shupe L, Perlmutters, Horner P. 2008. No evidence for chronic demyelination in spared axons after spinal cord injury in a mouse. J Neurosci 28: 3887-3896.
24. Li GL, Brodin G, Farooque M, Funa K, Holtz A, Wang WL, Olsson Y. 1996. Apoptosis and expression of Bcl-2 after compression trauma to rat spinal cord. J Neuropathol Exp Neurol 55: 280-289.
25. Lin W, Bailey SL, Ho H, Harding HP, Ron D, Miller SD, Popko B. 2007. The integrated stress response prevents demyelination by protecting oligodendrocytes against immune-mediated damage. J Clin Invest 117: 448-456.
26. Lin W, Harding HP, Ron D, Popko B. 2005. Endoplasmic reticulum stress modulates the response of myelinating oligodendrocytes to the immune cytokine interferon-γ. J Cell Biol 169: 603-612.
27. Lin W, Kemper A, Dupree JL, Harding HP, Ron D, Popko B. 2006. Interferon-γ inhibits central nervous system remyelination through a process modulated by endoplasmic reticulum stress. Brain 129: 1306-1318.
28. Lin W, Kunkler PE, Harding HP, Ron D, Kraig RP, Popko B. 2008. Enhanced integrated stress response promotes myelinating oligodendrocyte survival in response to interferon-gamma. Am J Pathology 173: 1508-1517.
29. Magnuson DS, Lovett R, Coffee C, Gray R, Han Y, Zhang YP, Burke DA. 2005. Functional consequences of lumbar spinal cord contusion injuries in the adult rat. J Neurotrauma 22: 529-543.
30. Maytin EV, Habener JF. 1998. Transcription factors C/EBP α, C/EBP β, and CHOP(Gadd153) expressed during the differentiation program of keratinocytes in vitro and in vivo. J Invest Dermatol 110: 238-246.
31. McCullough KD, Martindale JL, Klotz LO, AW TY, Holbrook NJ. 2001. Gadd153 sensitizes cells to endoplasmic reticulum stress by down-regulating Bcl2 and perturbing the cellular redox state. Mol Cell Biol 21: 1249-1259.
32. McTigue DM, Horner PJ, Stokes BT, Gage FH. 1998. Neurotrophin-3 and brain-derived neurotrophic factor induce oligodendrocyte proliferation and myelination of regenerating axons in the contused adult rat spinal cord. J Neurosci 18: 5354-5365.
33. Milhavet O, Marindale JL, Camandola S, Chan SL, Gary DS, Cheng A, Holbrook NJ, Mattson MP. 2002. Involvement of Gadd153 in the pathogenic action of presenilin-1 mutations. J Neurochem 83: 673-681.
34. Mungrue IN, Pagnon J, Kohannim O, Gargalovic PS, Lusis AJ. 2009. CHAC1/MGC4504 is a novel proapoptotic component of the unfolded protein response, downstream of the ATF4-ATF3-CHOP cascade. J Immunol 182: 466-476.
35. Ohoka N, Yoshii S, Hattori Ti, Onozaki K, Hayashi H. 2005. TRB3, a novel ER stress-inducible gene, is induced via ATF4-CHOP pathway and is involved in cell death. EMBO J 24: 1243-1255.
36. Oyadomari S, Takeda K, Takiguchi M, Gotoh T, Matsumoto M, Wada I, Akira S, Araki E, Mori M. 2001. Nitric oxide-induced apoptosis in pancreatic beta cells is mediated by the endoplasmic reticulum stress pathway. Proc Natl Acad Sci 98: 10845-10850.
37. Ozcan U, Yilmaz E, Ozcan L, Furuhashi M, Vaillancourt E, Smith RO, Gorgun CZ, Hotamisligil GS. 2006. Chemical chaperones reduce ER stress and restore glucose homeostasis in a mouse model of type 2 diabetes. Science 313: 1137-1140.
38. Penas C, Guzmán MS, Verdú E, Forés J, Navarro X, Casas C. 2007. Spinal cord injury induces endoplasmic reticulum stress with different cell-type dependent response. J Neurochem 102: 1242-1255.
39. Pennuto M, Tinelli E, Malaguti M, Del Carro U, D'Antonio M, Ron D, Quattrini A, Feltri ML, Wrabetz L. 2008. Ablation of the UPR-mediator CHOP restores motor function and reduces demyelination in Charcot-Marie-Tooth 1B mice. Neuron 57: 393-405.
40. Prostko CR, Brostrom MA, Brostrom CO. 1993. Reversible phosphorylation of eurkaryotic initiation factor 2 alpha in response to endoplasmic reticular signaling. Mol Cell Biochem 127-128: 255-265.
41. Puthalakath H. 2007. ER stress triggers apoptosis by activating BH3-only protein Bim. Cell 129: 1337-1349.
42. Ron D, Habener JF. 1992. CHOP, a novel developmentally regulated nuclear protein that dimerizes with transcription factors C/EBP and LAP, functions as a dominant-negative inhibitor of gene transcription. Genes Dev 6: 439-453.
43. Ron D, Walter P. 2007. Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 8: 519-529.
44. Rowland JW, Hawryluk GW, Kwon B, Fehlings MG. 2008. Current status of acute spinal cord injury pathophysiology and emerging therapies: promise on the horizon. Neurosurg Focus 25: E2.
45. Scheff SW, Rabchevsky AG, Fugaccia I, Main JA, Lumpp JEJr. 2003. Experimental modeling of spinal cord injury characterization of a force-defined injury device. J Neurotrauma 20: 179-193.
46. Schröder M. 2008. Endoplasmic reticulum stress responses. Cell Mol Life Sci 65: 862-894.
47. Schröder M, Kaufman RJ. 2005. The mammalian unfolded protein response. Annu Rev Biochem 74: 739-89.
48. Silver J, Miller JH. 2004. Regeneration beyond glial scar. Nat Rev Neurosci 5: 146-156.
49. Sok J, Wang XZ, Batchvarova N, Kuroda M, Harding H, Ron D. 1999. CHOP-dependent stress-inducible expression of a novel form of carbonic anhydrase VI. Mol Cell Biol 19: 495-504.
50. Sokka AL, Putkonen N, Mudo G, Pryazhnikov E, Reijonen S, Khiroug L, Belluardo N, Lindholm D, Korhonen L. 2007. Endoplasmic reticulum stress inhibition protects against excitotoxic neuronal injury in the rat brain. J Neurosci 27: 901-908.
51. Southwood CM, Garbern J, Jiang W, Gow A. 2002. The unfolded protein response modulates disease severity in Pelizaeus-Merzbacher disease. Neuron 36: 585-596.
52. 2 up-regulates death receptor 5 gene expression in HCT116 cells: Involvement of reactive oxygen species and C/EBP homologous transcription factor gene transcription. Mol Cancer Ther 7: 3429-3440.
53. Yamaguchi H, Wang HG. 2004. CHOP is involved in endoplasmic reticulum stress-induced apoptosis by enhancing DR5 expression in human carcinoma cells. J Biol Chem 279: 45495-45502.
54. Yoshida H, Matsui T, Yamamota A, Okada T, Kazatoshi M. 2001. XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell 107: 881-891.
55. Zhang K, Kaufman RJ. 2008. From endoplasmic-reticulum stress to the inflammatory response. Nature 454: 455-462.
56. Zinsner H, Kuroda M, Wang X, Batchvarova N, Lightfoot RT, Remotti H, Stevene JL, Ron D. 1998. CHOP is implicated in programmed cell death in response to impaired function of the endoplasmic reticulum. Genes Dev 12: 982-995.