Neuroprotective function of cellular prion protein in a mouse model of amyotrophic lateral sclerosis

American Journal of Pathology

Volumn 176, Issue 3, 2010, Pages 1409-1420

  Steinacker, Petra ^a   Hawlik, Andreas ^a   Lehnert, Stefan ^a   Jahn, Olaf ^b,c   Meier, Stephen ^a   Görz, Evamaria ^a   Braunstein, Kerstin E ^a   Krzovska, Marija ^a   Schwalenstöcker, Birgit ^a   Jesse, Sarah ^a   Pröpper, Christian ^a   Böckers, Tobias ^a   Ludolph, Albert ^a   Otto, Markus ^a  

^a UNIVERSITY OF ULM   (Germany)

^b MAX PLANCK INSTITUTE OF EXPERIMENTAL MEDICINE   (Germany)

^c Deutsche Forschungsgemeinschaft   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

COPPER ZINC SUPEROXIDE DISMUTASE; CREATINE KINASE; GLIAL FIBRILLARY ACIDIC PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PRION PROTEIN; PROTEIN BCL 2; PROTEIN KINASE B;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL VACUOLE; CONTROLLED STUDY; DISEASE COURSE; FEMALE; MALE; MOTONEURON; MOUSE; MUSCLE WEAKNESS; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; ROTAROD TEST; WEIGHT REDUCTION;

EID: 77749242612     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.2353/ajpath.2010.090355     Document Type: Article

References (64)

1. Leigh PN, Swash M, Iwasaki Y, Ludolph A, Meininger V, Miller RG, Mitsumoto H, Shaw P, Tashiro K, Van Den Berg L: Amyotrophic lateral sclerosis: a consensus viewpoint on designing and implementing a clinical trial. Amyotroph Lateral Scler Other Motor Neuron Disord 2004, 5:84-98
2. Kabashi E, Valdmanis PN, Dion P, Rouleau GA: Oxidized/misfolded superoxide dismutase-1: the cause of all amyotrophic lateral sclerosis? Ann Neurol 2007, 62:553-559
3. Urushitani M, Sik A, Sakurai T, Nukina N, Takahashi R, Julien JP: Chromogranin-mediated secretion of mutant superoxide dismutase proteins linked to amyotrophic lateral sclerosis. Nat Neurosci 2006, 9:108-118
4. Pasinelli P, Houseweart MK, Brown RH Jr, Cleveland DW: Caspase-1 and -3 are sequentially activated in motor neuron death in Cu,Zn superoxide dismutase-mediated familial amyotrophic lateral sclerosis. Proc Natl Acad Sci USA: 2000, 97:13901-13906
5. Kostic V, Jackson-Lewis V, de Bilbao F, Dubois-Dauphin M, Przedborski S: Bcl-2: prolonging life in a transgenic mouse model of familial amyotrophic lateral sclerosis. Science 1997, 277:559-562
6. Li M, Ona VO, Guegan C, Chen M, Jackson-Lewis V, Andrews LJ, Olszewski AJ, Stieg PE, Lee JP, Przedborski S, Friedlander RM: Functional role of caspase-1 and caspase-3 in an ALS transgenic mouse model. Science 2000, 288:335-339
7. Boillee S, Vande Velde C, Cleveland DW: ALS: a disease of motor neurons and their nonneuronal neighbors. Neuron 2006, 52:39-59
8. Pramatarova A, Laganiere J, Roussel J, Brisebois K, Rouleau GA: Neuron-specific expression of mutant superoxide dismutase 1 in transgenic mice does not lead to motor impairment. J Neurosci 2001, 21:3369-3374
9. Van Damme P, Bogaert E, Dewil M, Hersmus N, Kiraly D, Scheveneels W, Bockx I, Braeken D, Verpoorten N, Verhoeven K, Timmerman V, Herijgers P, Callewaert G, Carmeliet P, Van Den Bosch L, Robberecht W: Astrocytes regulate GluR2 expression in motor neurons and their vulnerability to excitotoxicity. Proc Natl Acad Sci USA: 2007, 104:14825-14830
10. Yamanaka K, Chun SJ, Boillee S, Fujimori-Tonou N, Yamashita H, Gutmann DH, Takahashi R, Misawa H, Cleveland DW: Astrocytes as determinants of disease progression in inherited amyotrophic lateral sclerosis. Nat Neurosci 2008, 11:251-253
11. Clement AM, Nguyen MD, Roberts EA, Garcia ML, Boillee S, Rule M, McMahon AP, Doucette W, Siwek D, Ferrante RJ, Brown RH Jr, Julien JP, Goldstein LS, Cleveland DW: Wild-type nonneuronal cells extend survival of SOD1 mutant motor neurons in ALS mice. Science 2003, 302:113-117
12. Bilsland LG, Nirmalananthan N, Yip J, Greensmith L, Duchen MR: Expression of mutant SOD1 in astrocytes induces functional deficits in motoneuron mitochondria. J Neurochem 2008, 107:1271-1283
13. Dupuis L, Mbebi C, Gonzalez de Aguilar JL, Rene F, Muller A, de Tapia M, Loeffler JP: Loss of prion protein in a transgenic model of amyotrophic lateral sclerosis. Mol Cell Neurosci 2002, 19:216-224
14. Westergard L, Christensen HM, Harris DA: The cellular prion protein (PrP[C]): its physiological function and role in disease. Biochim Biophys Acta 2007, 1772:629-644
15. Lima FR, Arantes CP, Muras AG, Nomizo R, Brentani RR, Martins VR: Cellular prion protein expression in astrocytes modulates neuronal survival and differentiation. J Neurochem 2007, 103:2164-2176
16. Arantes C, Nomizo R, Lopes MH, Hajj GN, Lima FR, Martins VR: Prion protein and its ligand stress inducible protein 1 regulate astrocyte development. Glia 2009, 57:1439-1449
17. Hosokawa-Muto J, Kamatari YO, Nakamura HK, Kuwata K: Variety of anti-prion compounds discovered through an in silico screen based on PrPC structure: A correlation between anti-prion activity and binding affinity. Antimicrob Agents Chemother 2009, 53:765-771
18. Steinacker P, Schwarz P, Reim K, Brechlin P, Jahn O, Kratzin H, Aitken A, Wiltfang J, Aguzzi A, Bahn E, Baxter HC, Brose N, Otto M: Unchanged survival rates of 14-3-3gamma knockout mice after inoculation with pathological prion protein. Mol Cell Biol 2005, 25:1339-1346
19. Habisch HJ, Janowski M, Binder D, Kuzma-Kozakiewicz M, Widmann A, Habich A, Schwalenstocker B, Hermann A, Brenner R, Lukomska B, Domanska-Janik K, Ludolph AC, Storch A: Intrathecal application of neuroectodermally converted stem cells into a mouse model of ALS: limited intraparenchymal migration and survival narrows therapeutic effects. J Neural Transm 2007, 114:1395-1406
20. Ludolph AC, Bendotti C, Blaugrund E, Hengerer B, Loffler JP, Martin J, Meininger V, Meyer T, Moussaoui S, Robberecht W, Scott S, Silani V, Van Den Berg LH: Guidelines for the preclinical in vivo evaluation of pharmacological active drugs for ALS/MND: report on the 142nd ENMC international workshop. Amyotroph Lateral Scler 2007, 8: 217-223
21. Boillee S, Yamanaka K, Lobsiger CS, Copeland NG, Jenkins NA, Kassiotis G, Kollias G, Cleveland DW: Onset and progression in inherited ALS determined by motor neurons and microglia. Science 2006, 312:1389-1392
22. Teuchert M, Fischer D, Schwalenstoecker B, Habisch HJ, Bockers TM, Ludolph AC: A dynein mutation attenuates motor neuron degeneration in SOD1(G93A) mice. Exp Neurol 2006, 198:271-274
23. Wiltfang J, Smirnov A, Schnierstein B, Kelemen G, Matthies U, Klafki HW, Staufenbiel M, Huther G, Ruther E, Kornhuber J: Improved electrophoretic separation and immunoblotting of beta-amyloid (A beta) peptides 1-40, 1-42, and 1-43. Electrophoresis 1997, 18: 527-532
24. Liu NK, Xu XM: beta-tubulin is a more suitable internal control than beta-actin in western blot analysis of spinal cord tissues after traumatic injury. J Neurotrauma 2006, 23:1794-1801
25. Brechlin P, Jahn O, Steinacker P, Cepek L, Kratzin H, Lehnert S, Jesse S, Mollenhauer B, Kretzschmar HA, Wiltfang J, Otto M: Cerebrospinal fluid-optimized two-dimensional difference gel electrophoresis (2-D DIGE) facilitates the differential diagnosis of Creutzfeldt-Jakob disease. Proteomics 2008, 8:4357-4366
26. Jahn O, Hesse D, Reinelt M, Kratzin HD: Technical innovations for the automated identification of gel-separated proteins by MALDI-TOF mass spectrometry. Anal Bioanal Chem 2006, 386:92-103
27. Wong PC, Borchelt DR: Motor neuron disease caused by mutations in superoxide dismutase 1. Curr Opin Neurol 1995, 8:294-301
28. Chiarini LB, Freitas AR, Zanata SM, Brentani RR, Martins VR, Linden R: Cellular prion protein transduces neuroprotective signals. EMBO J 2002, 21:3317-3326
29. Spudich A, Frigg R, Kilic E, Kilic U, Oesch B, Raeber A, Bassetti CL, Hermann DM: Aggravation of ischemic brain injury by prion protein deficiency: role of ERK-1/-2 and STAT-1. Neurobiol Dis 2005, 20:442-449
30. Lagier-Tourenne C, Cleveland DW: Rethinking ALS: the FUS about TDP-43. Cell 2009, 136:1001-1004
31. Brown DR, Schulz-Schaeffer WJ, Schmidt B, Kretzschmar HA: Prion protein-deficient cells show altered response to oxidative stress due to decreased SOD-1 activity. Exp Neurol 1997, 146:104-112
32. Jones S, Batchelor M, Bhelt D, Clarke AR, Collinge J, Jackson GS: Recombinant prion protein does not possess SOD-1 activity. Biochem J 2005, 392:309-312
33. Dal Canto MC, Gurney ME: Development of central nervous system pathology in a murine transgenic model of human amyotrophic lateral sclerosis. Am J Pathol 1994, 145:1271-1279
34. Dal Canto MC, Gurney ME: A low expressor line of transgenic mice carrying a mutant human Cu,Zn superoxide dismutase (SOD1) gene develops pathological changes that most closely resemble those in human amyotrophic lateral sclerosis. Acta Neuropathol 1997, 93:537-550
35. Shibata N: Transgenic mouse model for familial amyotrophic lateral sclerosis with superoxide dismutase-1 mutation. Neuropathology 2001, 21:82-92
36. Jiang YM, 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, 57:236-251
37. Casciati A, Ferri A, Cozzolino M, Celsi F, Nencini M, Rotilio G, Carri MT: Oxidative modulation of nuclear factor-kappaB in human cells expressing mutant fALS-typical superoxide dismutases. J Neurochem 2002, 83:1019-1029
38. Ferlazzo N, Condello S, Curro M, Parisi G, Ientile R, Caccamo D: NF-kappaB activation is associated with homocysteine-induced injury in Neuro2a cells. BMC Neurosci 2008, 9:62
39. Jang MH, Jung SB, Lee MH, Kim CJ, Oh YT, Kang I, Kim J, Kim EH: Melatonin attenuates amyloid beta25-35-induced apoptosis in mouse microglial BV2 cells. Neurosci Lett 2005, 380:26-31
40. Vukosavic S, Stefanis L, Jackson-Lewis V, Guegan C, Romero N, Chen C, Dubois-Dauphin M, Przedborski S: Delaying caspase activation by Bcl-2: a clue to disease retardation in a transgenic mouse model of amyotrophic lateral sclerosis. J Neurosci 2000, 20:9119-9125
41. Brown DR, Nicholas RS, Canevari L: Lack of prion protein expression results in a neuronal phenotype sensitive to stress. J Neurosci Res 2002, 67:211-224
42. Petrakis S, Sklaviadis T: Identification of proteins with high affinity for refolded and native PrPC. Proteomics 2006, 6:6476-6484
43. Adhihetty PJ, Beal MF: Creatine and its potential therapeutic value for targeting cellular energy impairment in neurodegenerative diseases. Neuromolecular Med 2008, 10:275-290
44. Chung MA, Lee JE, Lee JY, Ko MJ, Lee ST, Kim HJ: Alteration of collapsin response mediator protein-2 expression in focal ischemic rat brain. Neuroreport 2005, 16:1647-1653
45. Yoshida H, Watanabe A, Ihara Y: Collapsin response mediator protein-2 is associated with neurofibrillary tangles in Alzheimer's disease. J Biol Chem 1998, 273:9761-9768
46. Zhang Z, Ottens AK, Sadasivan S, Kobeissy FH, Fang T, Hayes RL, Wang KK: Calpain-mediated collapsin response mediator protein-1, -2, and -4 proteolysis after neurotoxic and traumatic brain injury. J Neurotrauma 2007, 24:460-472
47. Cole AR, Noble W, van Aalten L, Plattner F, Meimaridou R, Hogan D, Taylor M, LaFrancois J, Gunn-Moore F, Verkhratsky A, Oddo S, LaFerla F, Giese KP, Dineley KT, Duff K, Richardson JC, Yan SD, Hanger DP, Allan SM, Sutherland C: Collapsin response mediator protein-2 hyperphosphorylation is an early event in Alzheimer's disease progression. J Neurochem 2007, 103:1132-1144
48. Ilzecka J, Stelmasiak Z: Creatine kinase activity in amyotrophic lateral sclerosis patients. Neurol Sci 2003, 24:286-287
49. Levine JB, Kong J, Nadler M, Xu Z: Astrocytes interact intimately with degenerating motor neurons in mouse amyotrophic lateral sclerosis (ALS). Glia 1999, 28:215-224
50. Hall ED, Oostveen JA, Gurney ME: Relationship of microglial and astrocytic activation to disease onset and progression in a transgenic model of familial ALS. Glia 1998, 23:249-256
51. Nagai M, Re DB, Nagata T, Chalazonitis A, Jessell TM, Wichterle H, Przedborski S: Astrocytes expressing ALS-linked mutated SOD1 release factors selectively toxic to motor neurons. Nat Neurosci 2007, 10:615-622
52. Beers DR, Henkel JS, Xiao Q, Zhao W, Wang J, Yen AA, Siklos L, McKercher SR, Appel SH: Wild-type microglia extend survival in PU. 1 knockout mice with familial amyotrophic lateral sclerosis. Proc Natl Acad Sci USA: 2006, 103:16021-16026
53. Peviani M, Cheroni C, Troglio F, Quarto M, Pelicci G, Bendotti C: Lack of changes in the PI3K/AKT survival pathway in the spinal cord motor neurons of a mouse model of familial amyotrophic lateral sclerosis. Mol Cell Neurosci 2007, 34:592-602
54. Freire E, Gomes FC, Linden R, Neto VM, Coelho-Sampaio T: Structure of laminin substrate modulates cellular signaling for neuritogenesis. J Cell Sci 2002, 115:4867-4876
55. Wiksten M, Vaananen A, Liesi P: Selective overexpression of gamma1 laminin in astrocytes in amyotrophic lateral sclerosis indicates an involvement in ALS pathology. J Neurosci Res 2007, 85:2045-2058
56. Dewil M, Lambrechts D, Sciot R, Shaw PJ, Ince PG, Robberecht W, Van den Bosch L: Vascular endothelial growth factor counteracts the loss of phospho-Akt preceding motor neurone degeneration in amyotrophic lateral sclerosis. Neuropathol Appl Neurobiol 2007, 33:499-509
57. Kieran D, Sebastia J, Greenway MJ, King MA, Connaughton D, Concannon CG, Fenner B, Hardiman O, Prehn JH: Control of motoneuron survival by angiogenin. J Neurosci 2008, 28:14056-14061
58. Lee ES, Yin Z, Milatovic D, Jiang H, Aschner M: Estrogen and tamoxifen protect against Mn-induced toxicity in rat cortical primary cultures of neurons and astrocytes. Toxicol Sci 2009, 110:156-167
59. Chung YH, Joo KM, Lim HC, Cho MH, Kim D, Lee WB, Cha CI: 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: 203-209
60. Vassallo N, Herms J, Behrens C, Krebs B, Saeki K, Onodera T, Windl O, Kretzschmar HA: Activation of phosphatidylinositol 3-kinase by cellular prion protein and its role in cell survival. Biochem Biophys Res Commun 2005, 332:75-82
61. Weise J, Doeppner TR, Muller T, Wrede A, Schulz-Schaeffer W, Zerr I, Witte OW, Bahr M: Overexpression of cellular prion protein alters postischemic Erk1/2 phosphorylation but not Akt phosphorylation and protects against focal cerebral ischemia. Restor Neurol Neurosci 2008, 26:57-64
62. Stanciu M, Wang Y, Kentor R, Burke N, Watkins S, Kress G, Reynolds I, Klann E, Angiolieri MR, Johnson JW, DeFranco DB: Persistent activation of ERK contributes to glutamate-induced oxidative toxicity in a neuronal cell line and primary cortical neuron cultures. J Biol Chem 2000, 275:12200-12206
63. Perry G, Roder H, Nunomura A, Takeda A, Friedlich AL, Zhu X, Raina AK, Holbrook N, Siedlak SL, Harris PL, Smith MA: Activation of neuronal extracellular receptor kinase (ERK) in Alzheimer disease links oxidative stress to abnormal phosphorylation. Neuroreport 1999, 10:2411-2415
64. Chu CT, Levinthal DJ, Kulich SM, Chalovich EM, DeFranco DB: Oxidative neuronal injury. The dark side of ERK1/2. Eur J Biochem 2004, 271:2060-2066