Infection of prions and treatment of PrP106-126 alter the endogenous status of protein 14-3-3 and trigger the mitochondrial apoptosis possibly via activating Bax pathway

Molecular Neurobiology

Volumn 49, Issue 2, 2014, Pages 840-851

  Shi, Qi ^a   Song, Qin Qin ^a   Sun, Peng ^a   Zhang, Jin ^a   Song, Juan ^a   Chen, Li Na ^a   Xiao, Kang ^a   Wang, Shao Bin ^a   Zhang, Ya Zhou ^a   Li, Gong Qi ^a   Sheng, Lin Jun ^a   Wang, Bao Dong ^a   Lu, Ming Zhi ^a   Han, Jun ^a   Dong, Xiao Ping ^a,b  

^a CHINESE CENTER FOR DISEASE CONTROL AND PREVENTION   (China)

^b INSTITUTE OF MICROBIOLOGY   (China)

Author keywords

14 3 3; Apoptosis; Bax; Prion; S nitrosylation; Scrapie

Indexed keywords

CASPASE 3; PRION PROTEIN; PRION PROTEIN[106-126]; PROTEIN 14 3 3; PROTEIN BAX; PROTEIN BCL 2; UNCLASSIFIED DRUG; BAX PROTEIN, HUMAN; PEPTIDE FRAGMENT; PRION; PRION PROTEIN (106-126);

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; GENE SILENCING; HAMSTER; HUMAN; HUMAN CELL; INCUBATION TIME; MITOCHONDRION; NITROSYLATION; NONHUMAN; PRION; PRION DISEASE; PROTEIN CLEAVAGE; SCRAPIE; SIGNAL TRANSDUCTION; UPREGULATION; WESTERN BLOTTING; ANIMAL; BIOSYNTHESIS; CRICETULUS; DRUG EFFECTS; HELA CELL LINE; METABOLISM; PATHOLOGY; PHYSIOLOGY; TOXICITY;

14-3-3 PROTEINS; ANIMALS; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; CRICETINAE; CRICETULUS; HELA CELLS; HUMANS; MITOCHONDRIA; PEPTIDE FRAGMENTS; PRION DISEASES; PRIONS;

EID: 84896513310     PISSN: 08937648     EISSN: 15591182     Source Type: Journal    
DOI: 10.1007/s12035-013-8560-1     Document Type: Article

References (46)

1. Venneti S (2010) Prion diseases. Clin Lab Med 30:293-309
2. Henriques ST, Pattenden LK, Aguilar MI, Castanho MA (2009) The toxicity of prion protein fragment PrP(106-126) is not mediated by membrane permeabilization as shown by a M112W substitution. Biochemistry 48:4198-4208
3. Vassallo N (2009) Properties and pathogenicity of prion-derived peptides. Protein Pept Lett 16:230-238
4. Walsh P, Yau J, Simonetti K, Sharpe S (2009) Morphology and secondary structure of stable beta-oligomers formed by amyloid peptide PrP(106-126). Biochemistry 48:5779-5781
5. Bounhar Y, Zhang Y, Goodyer CG, LeBlanc A (2001) Prion protein protects human neurons against Bax-mediated apoptosis. J Biol Chem 276:39145-39149
6. Kuwahara C, Takeuchi AM, Nishimura T, Haraguchi K, Kubosaki A et al (1999) Prions prevent neuronal cell-line death. Nature 400:225-226 (Pubitemid 29334128)
7. Roucou X, Guo Q, Zhang Y, Goodyer CG, LeBlanc AC (2003) Cytosolic prion protein is not toxic and protects against Bax-mediated cell death in human primary neurons. J Biol Chem 278:40877-40881 (Pubitemid 37280906)
8. Li A, Harris DA (2005) Mammalian prion protein suppresses Bax-induced cell death in yeast. J Biol Chem 280:17430-17434 (Pubitemid 41389214)
9. Hoshino S, Inoue K, Yokoyama T, Kobayashi S, Asakura T et al (2003) Prions prevent brain damage after experimental brain injury: A preliminary report. Acta Neurochir Suppl 86:297-299
10. Brown DR, Nicholas RS, Canevari L (2002) Lack of prion protein expression results in a neuronal phenotype sensitive to stress. J Neurosci Res 67:211-224 (Pubitemid 34052040)
11. Shmerling D, Hegyi I, Fischer M, Blattler T, Brandner S et al (1998) Expression of amino-terminally truncated PrP in themouse leading to ataxia and specific cerebellar lesions. Cell 93:203-214 (Pubitemid 28180854)
12. Rossi D, Cozzio A, Flechsig E, Klein MA, Rulicke T et al (2001) Onset of ataxia and Purkinje cell loss in PrP null mice inversely correlated with Dpl level in brain. EMBO J 20:694-702 (Pubitemid 32167634)
13. Porter GW, Khuri FR, Fu H (2006) Dynamic 14-3-3/client protein interactions integrate survival and apoptotic pathways. Semin Cancer Biol 16:193-202 (Pubitemid 43796125)
14. Dougherty MK, Morrison DK (2004) Unlocking the code of 14-3-3. J Cell Sci 117:1875-1884 (Pubitemid 38745122)
15. Mackintosh C (2004) Dynamic interactions between 14-3-3 proteins and phosphoproteins regulate diverse cellular processes. Biochem J 381:329-342
16. Fountoulakis M, Cairns N, Lubec G (1999) Increased levels of 14-3-3 gamma and epsilon proteins in brain of patients with Alzheimer 's disease and Down syndrome. J Neural Transm Suppl 57:323-335
17. Kawamoto Y, Akiguchi I, Nakamura S, Honjyo Y, Shibasaki H et al (2002) 14-3-3 proteins in Lewy bodies in Parkinson disease and diffuse Lewy body disease brains. J Neuropathol Exp Neurol 61:245-253 (Pubitemid 34212599)
18. Peyrl A, Weitzdoerfer R, Gulesserian T, Fountoulakis M, Lubec G (2002) Aberrant expression of signaling-related proteins 14-3-3 gamma and RACK1 in fetal Down syndrome brain (trisomy 21). Electrophoresis 23:152-157
19. Chen HK, Fernandez-Funez P, Acevedo SF, Lam YC, Kaytor MD et al (2003) Interaction of Akt-phosphorylated ataxin-1 with 14-3-3 mediates neurodegeneration in spinocerebellar ataxia type 1. Cell 113:457-468 (Pubitemid 36588749)
20. Kretzschmar HA, Ironside JW, DeArmond SJ, Tateishi J (1996) Diagnostic criteria for sporadic Creutzfeldt-Jakob disease. Arch Neurol 53:913-920 (Pubitemid 26301703)
21. Zerr I, Kallenberg K, Summers DM, Romero C, Taratuto A et al (2009) Updated clinical diagnostic criteria for sporadic Creutzfeldt-Jakob disease. Brain 132:2659-2668
22. Gao JM, Gao C, Han J, Zhou XB, Xiao XL et al (2004) Dynamic analyses of PrP and PrP(Sc) in brain tissues of golden hamsters infected with scrapie strain 263K revealed various PrP forms. Biomed Environ Sci 17:8-20 (Pubitemid 38638965)
23. Shi Q, Zhang BY, Gao C, Han J, Wang GR et al (2012) The diversities of PrP(Sc) distributions and pathologic changes in various brain regions from a Chinese patient with G114V genetic CJD. Neuropathology 32:51-59
24. Wang SB, Shi Q, Xu Y, Xie WL, Zhang J et al (2012) Protein disulfide isomerase regulates endoplasmic reticulum stress and the apoptotic process during prion infection and PrP mutant-induced cytotoxicity. PLoS One 7:e38221
25. Kazi A, Sun J, Doi K, Sung SS, Takahashi Y et al (2011) The BH3 alpha-helical mimic BH3-M6 disrupts Bcl-X(L), Bcl-2, and MCL-1 protein-protein interactions with Bax, Bak, Bad, or Bim and induces apoptosis in a Bax- and Bim-dependent manner. J Biol Chem 286: 9382-9392
26. Sluchanko NN, Gusev NB (2010) 14-3-3 proteins and regulation of cytoskeleton. Biochemistry (Mosc) 75:1528-1546
27. Pellegrini G, Dellambra E, Golisano O, Martinelli E, Fantozzi I et al (2001) p63 identifies keratinocyte stem cells. Proc Natl Acad Sci U S A 98:3156-3161 (Pubitemid 32220815)
28. Stamler JS, Simon DI, Osborne JA, Mullins ME, Jaraki O et al (1992) S -nitrosylation of proteins with nitric oxide: synthesis and characterization of biologically active compounds. Proc Natl Acad Sci U S A 89:444-448
29. Nakamura T, Lipton SA (2011) Redox modulation by S -nitrosylation contributes to protein misfolding, mitochondrial dynamics, and neuronal synaptic damage in neurodegenerative diseases. Cell Death Differ 18:1478-1486
30. Uehara T, Nakamura T, Yao D, Shi ZQ, Gu Z et al (2006) S-nitrosylated protein-disulphide isomerase links protein misfolding to neurodegeneration. Nature 441:513-517 (Pubitemid 44050153)
31. An R, Dong C, Lei Y, Han L, Li P et al (2008) PrP mutants with different numbers of octarepeat sequences are more susceptible to the oxidative stress. Sci China C Life Sci 51:630-639 (Pubitemid 351999740)
32. McMahon HE (2012) Prion processing: A double-edged sword? Biochem Soc Trans 40:735-738
33. Stefani IC, Wright D, Polizzi KM, Kontoravdi C (2012) The role of ER stress-induced apoptosis in neurodegeneration. Curr Alzheimer Res 9:373-387
34. Ferreiro E, Oliveira CR, Pereira CM (2008) The release of calcium from the endoplasmic reticulum induced by amyloid-beta and prion peptides activates the mitochondrial apoptotic pathway. Neurobiol Dis 30:331-342
35. Didonna A, Sussman J, Benetti F, Legname G (2012) The role of Bax and caspase-3 in doppel-induced apoptosis of cerebellar granule cells. Prion 6:309-316
36. Li A, Barmada SJ, Roth KA, Harris DA (2007) N-terminally deleted forms of the prion protein activate both Bax-dependent and Bax-independent neurotoxic pathways. J Neurosci 27:852-859 (Pubitemid 46174505)
37. Park YG, Jeong JK, Moon MH, Lee JH, Lee YJ et al (2012) Insulin-like growth factor-1 protects against prion peptide-induced cell death in neuronal cells via inhibition of Bax translocation. Int J Mol Med 30:1069-1074
38. Tsuruta F, Sunayama J, Mori Y, Hattori S, Shimizu S et al (2004) JNK promotes Bax translocation to mitochondria through phosphorylation of 14-3-3 proteins. EMBO J 23:1889-1899 (Pubitemid 38649651)
39. Nomura M, Shimizu S, Sugiyama T, Narita M, Ito T et al (2003) 14-3-3 Interacts directly with and negatively regulates pro-apoptotic Bax. J Biol Chem 278:2058-2065 (Pubitemid 36801450)
40. Datta SR, Katsov A, Hu L, Petros A, Fesik SWet al (2000) 14-3-3 proteins and survival kinases cooperate to inactivate BAD by BH3 domain phosphorylation. Mol Cell 6:41-51
41. Guo Y, Gong HS, Zhang J, XieWL, Tian C et al (2012) Remarkable reduction of MAP2 in the brains of scrapie-infected rodents and human prion disease possibly correlated with the increase of calpain. PLoS One 7:e30163
42. Zhang J, Dong XP (2012) Dysfunction of microtubule-associated proteins of MAP2/tau family in Prion disease. Prion 6:334-338
43. Zhou RM, Jing YY, Guo Y, Gao C, Zhang BYet al (2011) Molecular interaction of TPPP with PrP antagonized the CytoPrP-induced disruption of microtubule structures and cytotoxicity. PLoS One 6:e23079
44. Gong HS, Guo Y, Tian C, Xie WL, Shi Q et al (2012) Reduction of protein kinase MARK4 in the brains of experimental scrapie rodents and human prion disease correlates with deposits of PrP(Sc). Int J Mol Med 30:569-578
45. Bai Y, Li Q, Yang J, Zhou X, Yin X et al (2008) p75(NTR) activation of NF-kappaB is involved in PrP106-126-induced apoptosis in mouse neuroblastoma cells. Neurosci Res 62:9-14
46. Wang H, Tian C, Xu Y, Xie WL, Zhang J et al (2013) Abortive cell cycle events in the brains of scrapie-infected hamsters with remarkable decreases of PLK3/Cdc25C and increases of PLK1/cyclin B1. Mol Neurobiol. doi:10.1007/s12035- 013-8455-1