Activation of endoplasmic reticulum stress signaling pathway is associated with neuronal degeneration in MoMuLV-ts1-induced spongiform encephalomyelopathy

Laboratory Investigation

Volumn 84, Issue 7, 2004, Pages 816-827

  Kim, Hun Taek ^a   Waters, Kara ^a   Stoica, George ^a   Qiang, Wenan ^b   Liu, Na ^b   Scofield, Virginia L ^b   Wong, Paul K Y ^b  

^a TEXAS A AND M UNIVERSITY   (United States)

^b UNIVERSITY OF TEXAS   (United States)

Author keywords

Calcium; CaMKII ; ER stress; GADD153; MoMuLV ts1; Neuronal death; Spongiform encephalomyelopathy

Indexed keywords

CALCIUM ION; CASPASE 12; CASPASE 3; CYTOKINE; DOUBLE STRANDED RNA DEPENDENT PROTEIN KINASE LIKE ENDOPLASMIC RETICULUM KINASE; GLUCOSE REGULATED PROTEIN 78; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; INITIATION FACTOR 2; INITIATION FACTOR 2ALPHA; NEUROTOXIN; PROTEIN KINASE; PROTEIN KINASE (CALCIUM,CALMODULIN) II; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN SPONGIOSIS; BRAIN STEM; CALCIUM HOMEOSTASIS; CONTROLLED STUDY; CYTOKINE RELEASE; DEGENERATIVE DISEASE; ENDOPLASMIC RETICULUM; ENZYME PHOSPHORYLATION; GLIA CELL; MOLONEY LEUKEMIA ONCOVIRUS; MOUSE; NERVE CELL NECROSIS; NERVE DEGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROCESSING; SIGNAL TRANSDUCTION; STRESS;

ANIMALS; BRAIN STEM; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; CALCIUM; CASPASE 3; CASPASES; CCAAT-ENHANCER-BINDING PROTEINS; CENTRAL NERVOUS SYSTEM DISEASES; ENDOPLASMIC RETICULUM; GENE EXPRESSION REGULATION; MICE; MOLONEY MURINE LEUKEMIA VIRUS; NERVE DEGENERATION; PHOSPHORYLATION; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTOR CHOP; TRANSCRIPTION FACTORS;

EID: 3042638296     PISSN: 00236837     EISSN: None     Source Type: Journal    
DOI: 10.1038/labinvest.3700104     Document Type: Article

References (56)

1. Yuen PH, Szurek PF. The reduced virulence of the thymotropic Moloney murine leukemia virus derivative MoMuLV-TB is mapped to 11 mutations within the U3 region of the long terminal repeat. J Virol 1989;63:471-480.
2. Wong PKY, Prasad G, Hansen J, et al. ts1, a mutant of Moloney murine leukemia virus-TB, causes both immunodeficiency and neurologic disorders in BALB/c mice. Virology 1989;170:450-459.
3. Szurek PF, Yuen PH, Ball JK, et al. A Val-25-to-Ile substitution in the envelope precursor polyprotein, gPr80env, is responsible for the temperature sensitivity, inefficient processing of gPr80env, and neurovirulence of ts1, a mutant of Moloney murine leukemia virus TB. J Virol 1990;64:467-475.
4. Wong PKY, Floyd E, Szurek PF. High susceptibility of FVB/N mice to the paralytic disease induced by ts1, a mutant of Moloney murine leukemia virus TB. Virology 1991;180:365-371.
5. Stoica G, Illanes O, Tasca SI, et al. Temporal central and peripheral nervous system changes induced by a paralytogenic mutant of Moloney murine leukemia virus TB. Lab Invest 1993;69:724-735.
6. Choe W, Stoica G, Lynn W, et al. Neurodegeneration induced by MoMuLV-ts1 and increased expression of Fas and TNF-α in the central nervous system. Brain Res 1998;779:1-8.
7. Kim HT, Qiang W, Wong PKY, et al. Enhanced proteolysis of IκBα and IκBβ proteins in astrocytes by Moloney murine leukemia virus (MoMuLV)-ts1 infection: A potential mechanism of NF-κB activation. J Neurovirol 2001;7:466-475.
8. Stoica G, Tasca SI, Wong PKY. Motor neuronal loss and nearofilament-ubiquitin alteration in MoMuLV-ts1 encephalopathy. Acta Neuropathol (Berl) 2000;99:238-244.
9. Tyor WR, Wesselingh SL, Griffin JW, et al. Unifying hypothesis for the pathogenesis of HIV-associated dementia complex, vacuolar myelopathy, and sensory neuropathy. J Acquir Immune Defic Syndr Hum Retrovirol. 1995;9:379-388.
10. Forno LS. Neuropathology of Parkinson's disease. J Neuropathol Exp Neurol 1996;55:259-272.
11. Tu PH, Raju P, Robinson KA, et al. Transgenic mice carrying a human mutant superoxide dismutase transgene develop neuronal cytoskeletal pathology resembling human amyotrophic lateral sclerosis lesions. Proc Natl Acad Sci USA 1996;93:3155-3160.
12. Sagot Y, Dubois-Dauphin M, Tan SA, et al. Bcl-2 overexpression prevents motoneuron cell body loss but not axonal degeneration in a mouse model of a neurodegenerative disease. J Neurosci 1995;15:7727-7733.
13. Prusiner SB. Prions. Proc Natl Acad Sci USA 1998;95:13363-13383.
14. Harding HP, Zhang Y, Ron D. Protein translation and folding are coupled by an endoplasmic reticulumresident kinase. Nature 1999;397:271-274.
15. Kaufman RJ. Stress signaling from the lumen of the endoplasmic reticulum: coordination of gene transcriptional and translational controls. Genes Dev 1999;13:1211-1233.
16. Paschen W. Dependence of vital cell function on endoplasmic reticulum calcium levels: implications for the mechanisms underlying neuronal cell injury in different pathological states. Cell Calcium 2001;29:1-11.
17. Ron D, Habener JF. CHOP, a novel developmentally regulated nuclear protein that dimerizes with transcription factors C/EBP and LAP and functions as a dominant-negative inhibitor of gene transcription. Genes Dev 1992;6:439-453.
18. Barone MV, Crozat A, Tabaee A, et al. CHOP (GADD153) and its oncogenic variant, TLS-CHOP, have opposing effects on the induction of G1/S arrest. Genes Dev 1994;8:453-464.
19. Fawcett TW, Eastman HB, Martindale JL, et al. Physical and functional association between GADD153 and CCAAT/enhancer-binding protein β during cellular stress. J Biol Chem 1996;271:14285-14289.
20. Nakagawa T, Zhu H, Morishima N, et al. Caspase-12 mediates endoplasmic-reticulum-specific apoptosis and cytotoxicity by amyloid-beta. Nature 2000;403:98-103.
21. Sherman MY, Goldberg AL. Cellular defenses against unfolded proteins: a cell biologist thinks about neurodegenerative diseases. Neuron 2001;29:15-32.
22. Oyadomari S, Takeda K, Takiguchi M, et al. Nitric oxide-induced apoptosis in pancreatic beta cells is mediated by the endoplasmic reticulum stress pathway. Proc Natl Acad Sci USA 2001;98:10845-10850.
23. Gotoh T, Oyadomari S, Mori K, et al. Nitric oxide-induced apoptosis in RAW 264.7 macrophages is mediated by endoplasmic reticulum stress pathway involving ATF6 and CHOP. J Biol Chem 2002;277:12343-12350.
24. Kim BC, Kim HT, Mamura M, et al. Tumor necrosis factor induces apoptosis in hepatoma cells by increasing Ca(2+) release from the endoplasmic reticulum and suppressing Bcl-2 expression. J Biol Chem 2002;277:31381-31389.
25. Hacki J, Egger L, Monney L, et al. Apoptotic crosstalk between the endoplasmic reticulum and mitochondria controlled by Bcl-2. Oncogene 2000;19:2286-2295.
26. Wei MC, Zong WX, Cheng EH, et al. Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death. Science 2001;292:727-730.
27. Desagher S, Martinou JC. Mitochondria as the central control point of apoptosis. Trends Cell Biol 2000;10:369-377.
28. Kim HT, Tasca S, Qiang W, et al. Induction of p53 accumulation by Moloney murine leukemia virus-ts1 infection in astrocytes via activation of extracellular signal-regulated kinases 1/2. Lab Invest 2002;82:693-702.
29. Wong PKY, Soong MM, Yuen PH. Replication of murine leukemia virus in heterologous cells: interaction between ecotropic and xenotropic viruses. Virology 1981;109:366-378.
30. Kim HT, Stoica G, Bazer FW, et al. Interferon tau-induced hepatocyte apoptosis in sheep. Hepatology 2000;31:1275-1284.
31. Siklos L, Engelhardt JI, Reaume AG, et al. Altered calcium homeostasis in spinal motoneurons but not in oculomotor neurons of SOD-1 knockout mice. Acta Neuropathol 2000;99:517-524.
32. Gonzales-Scarano F, Nathanson N, Wong PKY. Retroviruses and the nervous system. In: Levy JA (ed). The Retroviridae. Plenum Press: New York, 1995, pp 127-136.
33. Earnshaw WC, Martins LM, Kaufmann SH. Mammalian caspases: structure, activation, substrates, and functions during apoptosis. Annu Rev Biochem 1999;68:383-424.
34. Rao RV, Castro-Obregon S, Frankowski H, et al. Coupling endoplasmic reticulum stress to the cell death program. An Apaf-1-independent intrinsic pathway. J Biol Chem 2002;277:21836-21842.
35. 2+ increases transcriptional activity and mRNA stability. J Biol Chem 1992;267:20465-20470.
36. Lipton SA, Nicotera P. Calcium, free radicals and excitotoxins in neuronal apoptosis. Cell Calcium 1997;23:165-171.
37. Orrenius S, Zhivotovsky B, Nicotera P. Regulation of cell death: the calcium-apoptosis link. Nat Rev Mol Cell Biol 2003;4:552-565.
38. Braun AP, Schulman H. The multifunctional calcium/calmodulin-dependent protein kinase: from form to function. Annu Rev Physiol 1995;57:417-445.
39. Soderling TR. The Ca-calmodulin-dependent protein kinase cascade. Trends Biochem Sci 1999;24:232-236.
40. Hetz C, Russelakis-Carneiro M, Maundrell K, et al. Caspase-12 and endoplasmic reticulum stress mediate neurotoxicity of pathological prion protein. EMBO J 2003;22:5435-5445.
41. Dimcheff DE, Askovic S, Baker AH, et al. Endoplasmic reticulum stress is a determinant of retrovirus-induced spongiform neurodegeneration. J Virol 2003;77:12617-12629.
42. Spear E, Ng DT. The unfolded protein response: no longer just a special teams player. Traffic 2001;2:515-523.
43. McCullough KD, Martindale JL, Klotz LO, et al. Gadd153 sensitizes cells to endoplasmic reticulum stress by down-regulating Bcl2 and perturbing the cellular redox state. Mol Cell Biol 2001;21:1249-1259.
44. Boya P, Cohen I, Zamzami N, et al. Endoplasmic reticulum stress-induced cell death requires mitochondrial membrane permeabilization. Cell Death Differ 2002;9:465-467.
45. Zong WX, Li C, Hatzivassiliou G, et al. Bax and Bak can localize to the endoplasmic reticulum to initiate apoptosis. J Cell Biol 2003;162:59-69.
46. 2+ disturbances, and cell death in renal epithelial cells. J Biol Chem 1997;272:21751-21759.
47. Morris JA, Dorner AJ, Edwards CA, et al. Immunoglobulin binding protein (BiP) function is required to protect cells from endoplasmic reticulum stress but is not required for the secretion of selective proteins. J Biol Chem 1997;272:4327-4334.
48. Yu Z, Luo H, Fu W, et al. The endoplasmic reticulum stress-responsive protein GRP78 protects neurons against excitotoxicity and apoptosis: suppression of oxidative stress and stabilization of calcium homeostasis. Exp Neurol 1999;155:302-314.
49. Kalai M, Lamkanfi M, Denecker G, et al. Regulation of the expression and processing of caspase-12. J Cell Biol 2003;162:457-467.
50. Watanabe Y, Suzuki O, Haruyama T, et al. Interferon-gamma induces reactive oxygen species and endoplasmic reticulum stress at the hepatic apoptosis. J Cell Biochem 2003;89:244-253.
51. Thastrup O, Cullen PJ, Drobak BK, et al. Thapsigargin, a tumor promoter, discharges intracellular Ca2+ stores by specific inhibition of the endoplasmic reticulum Ca2(+)-ATPase. Proc Natl Acad Sci USA 1990;87:2466-2470.
52. Fine S M, Angel RA, Perry SW, et al. Tumor necrosis factor-α inhibits glutamate uptake by primary human astrocytes: implications for pathogenesis of HIV-1 dementia. J Biol Chem 1996;271:15303-15306.
53. Bezzi P, Domercq M, Brambilla L, et al. CXCR4-activated astrocytes glutamate release via TNFα: amplification by microglia triggers neurotoxicity. Nat Neurosci 2001;4:702-710.
54. Laabich A, Li G, Cooper NG. Characterization of apoptosis-genes associated with NMDA mediated cell death in the adult rat retina. Brain Res Mol Brain Res 2001;91:34-42.
55. Foos TM, Wu JY. The role of taurine in the central nervous system and the modulation of intracellular calcium homeostasis. Neurochem Res 2002;27:21-26.
56. Takano H, Fukushi H, Morishima Y, et al. Calmodulin and calmodulin-dependent kinase II mediate neuronal cell death induced by depolarization. Brain Res 2003;962:41-47.