Prion protein expression and functional importance in skeletal muscle

Antioxidants and Redox Signaling

Volumn 15, Issue 9, 2011, Pages 2465-2475

  Smith, Jeffrey D ^a,b   Moylan, Jennifer S ^a,b   Hardin, Brian J ^a,b   Chambers, Melissa A ^a,b   Estus, Steven ^a   Telling, Glenn C ^a   Reid, Michael B ^a,b  

^a UNIVERSITY OF KENTUCKY   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DICHLOROFLUORESCIN; FLUORESCENT DYE; GLUCOSE; INSULIN; MESSENGER RNA; NITRIC OXIDE; PRION PROTEIN; UNCLASSIFIED DRUG;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; DIAPHRAGM; EXTENSOR DIGITORUM LONGUS; GASTROCNEMIUS MUSCLE; GLUCOSE TRANSPORT; GLYCOSYLATION; HOMEOSTASIS; HUMAN; HUMAN TISSUE; MALE; MOUSE; MUSCLE CELL; MUSCLE CONTRACTION; MUSCLE FORCE; MYOTUBE; NONHUMAN; OXIDATION; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REAL TIME POLYMERASE CHAIN REACTION; SKELETAL MUSCLE; SOLEUS MUSCLE; TIBIALIS ANTERIOR MUSCLE;

ANIMALS; BLOTTING, WESTERN; CELL LINE; DIAPHRAGM; HUMANS; MICE; MICE, TRANSGENIC; MUSCLE, SKELETAL; OXIDATION-REDUCTION; PRIONS;

ANIMALIA; MURINAE; MUS;

EID: 80052995726     PISSN: 15230864     EISSN: 15577716     Source Type: Journal    
DOI: 10.1089/ars.2011.3945     Document Type: Article

References (50)

1. Angers RC, Browning SR, Seward TS, Sigurdson CJ, Miller MW, Hoover EA, and Telling GC. Prions in skeletal muscles of deer with chronic wasting disease. Science 311: 1117, 2006.
2. Arata H, Takashima H, Hirano R, Tomimitsu H, Machigashira K, Izumi K, Kikuno M, Ng AR, Umehara F, Arisato T, Ohkubo R, Nakabeppu Y, Nakajo M, Osame M, and Arimura K. Early clinical signs and imaging findings in Gerstmann-Straussler-Scheinker syndrome (Pro102Leu). Neurology 66: 1672-1678, 2006. (Pubitemid 43964621)
3. Braga M, Sinha Hikim AP, Datta S, Ferrini MG, Brown D, Kovacheva EL, Gonzalez-Cadavid NF, and Sinha-Hikim I. Involvement of oxidative stress and caspase 2-mediated intrinsic pathway signaling in age-related increase in muscle cell apoptosis in mice. Apoptosis 13: 822-832, 2008.
4. Brown DR, Nicholas RS, and Canevari L. Lack of prion protein expression results in a neuronal phenotype sensitive to stress. J Neurosci Res 67: 211-224, 2002. (Pubitemid 34052040)
5. Brown DR, Schulz-Schaeffer WJ, Schmidt B, and Kretzschmar HA. Prion protein-deficient cells show altered response to oxidative stress due to decreased SOD-1 activity. Exp Neurol 146: 104-112, 1997. (Pubitemid 27319724)
6. Capellari S, Zaidi SI, Urig CB, Perry G, Smith MA, and Petersen RB. Prion protein glycosylation is sensitive to redox change. J Biol Chem 274: 34846-34850, 1999. (Pubitemid 129509530)
7. Chambers MA, Moylan JS, Smith JD, Goodyear LJ, and Reid MB. Stretch-stimulated glucose uptake in skeletal muscle is mediated by reactive oxygen species and p38 MAP-kinase. J Physiol 587: 3363-3373, 2009.
8. Choi CJ, Anantharam V, Saetveit NJ, Houk RS, Kanthasamy A, and Kanthasamy AG. Normal cellular prion protein protects against manganese-induced oxidative stress and apoptotic cell death. Toxicol Sci 98: 495-509, 2007. (Pubitemid 47244819)
9. Close RI. The relations between sarcomere length and characteristics of isometric twitch contractions of frog sartorius muscle. J Physiol 220: 745-762, 1972.
10. Ferreira LF, Moylan JS, Gilliam LA, Smith JD, Nikolova-Karakashian M, and Reid MB. Sphingomyelinase stimulates oxidant signaling to weaken skeletal muscle and promote fatigue. Am J Physiol Cell Physiol 299: C552-560, 2010.
11. Goh AX, Li C, Sy MS, and Wong BS. Altered prion protein glycosylation in the aging mouse brain. J Neurochem 100: 841-854, 2007. (Pubitemid 46095632)
12. Gomes MD, Lecker SH, Jagoe RT, Navon A, and Goldberg AL. Atrogin-1, a muscle-specific F-box protein highly expressed during muscle atrophy. Proc Natl Acad Sci USA 98: 14440-14445, 2001. (Pubitemid 33121410)
13. Graner E, Mercadante AF, Zanata SM, Martins VR, Jay DG, and Brentani RR. Laminin-induced PC-12 cell differentiation is inhibited following laser inactivation of cellular prion protein. FEBS Lett 482: 257-260, 2000.
14. Guillot-Sestier MV, Sunyach C, Druon C, Scarzello S, and Checler F. The alpha-secretase-derived N-terminal product of cellular prion, N1, displays neuroprotective function in vitro and in vivo. J Biol Chem 284: 35973-35986, 2009.
15. Haigh CL and Brown DR. Prion protein reduces both oxidative and non-oxidative copper toxicity. J Neurochem 98: 677-689, 2006. (Pubitemid 44051270)
16. Haigh CL, Lewis VA, Vella LJ, Masters CL, Hill AF, Lawson VA, and Collins SJ. PrPC-related signal transduction is influenced by copper, membrane integrity and the alpha cleavage site. Cell Res 19: 1062-1078, 2009.
17. Hardin BJ, Campbell KS, Smith JD, Arbogast S, Smith J, Moylan JS, and Reid MB. TNF-alpha acts via TNFR1 and muscle-derived oxidants to depress myofibrillar force in murine skeletal muscle. J Appl Physiol 104: 694-699, 2008. (Pubitemid 351468797)
18. Horiuchi M, Yamazaki N, Ikeda T, Ishiguro N, and Shinagawa M. A cellular form of prion protein (PrPC) exists in many non-neuronal tissues of sheep. J Gen Virol 76 ( Pt 10): 2583-2587, 1995.
19. Kanaani J, Prusiner SB, Diacovo J, Baekkeskov S, and Legname G. Recombinant prion protein induces rapid polarization and development of synapses in embryonic rat hippocampal neurons in vitro. J Neurochem 95: 1373-1386, 2005. (Pubitemid 41779262)
20. Klamt F, Dal-Pizzol F, Conte da Frota ML, Jr., Walz R, Andrades ME, da Silva EG, Brentani RR, Izquierdo I, and Fonseca Moreira JC. Imbalance of antioxidant defense in mice lacking cellular prion protein. Free Radic Biol Med 30: 1137-1144, 2001. (Pubitemid 32441839)
21. Lawler JM and Powers SK. Oxidative stress, antioxidant status, and the contracting diaphragm. Can J Appl Physiol 23: 23-55, 1998. (Pubitemid 128446881)
22. Li YP, Chen Y, Li AS, and Reid MB. Hydrogen peroxide stimulates ubiquitin-conjugating activity and expression of genes for specific E2 and E3 proteins in skeletal muscle myotubes. Am J Physiol Cell Physiol 285: C806-812, 2003. (Pubitemid 37158805)
23. Lledo PM, Tremblay P, DeArmond SJ, Prusiner SB, and Nicoll RA. Mice deficient for prion protein exhibit normal neuronal excitability and synaptic transmission in the hippocampus. Proc Natl Acad Sci USA 93: 2403-2407, 1996. (Pubitemid 26104362)
24. Massimino ML, Ferrari J, Sorgato MC, and Bertoli A. Heterogeneous PrPC metabolism in skeletal muscle cells. FEBS Letters 580: 878-884, 2006. (Pubitemid 43152308)
25. Matuszczak Y, Arbogast S, and Reid MB. Allopurinol mitigates muscle contractile dysfunction caused by hindlimb unloading in mice. Aviat Space Environ Med 75: 581-588, 2004. (Pubitemid 38857377)
26. Mays CE, Titlow W, Seward T, Telling GC, and Ryou C. Enhancement of protein misfolding cyclic amplification by using concentrated cellular prion protein source. Biochem Biophys Res Commun 388: 306-310, 2009.
27. Moylan JS and Reid MB. Oxidative stress, chronic disease, and muscle wasting. Muscle Nerve 35: 411-429, 2007. (Pubitemid 46542961)
28. Murrant CL, Andrade FH, and Reid MB. Exogenous reactive oxygen and nitric oxide alter intracellular oxidant status of skeletal muscle fibres. Acta Physiol Scand 166: 111-121, 1999. (Pubitemid 29304170)
29. Nazor KE, Seward T, and Telling GC. Motor behavioral and neuropathological deficits in mice deficient for normal prion protein expression. Biochim Biophys Acta 1772: 645-653, 2007. (Pubitemid 46880209)
30. Nico PB, de-Paris F, Vinade ER, Amaral OB, Rockenbach I, Soares BL, Guarnieri R, Wichert-Ana L, Calvo F, Walz R, Izquierdo I, Sakamoto AC, Brentani R, Martins VR, and Bianchin MM. Altered behavioural response to acute stress in mice lacking cellular prion protein. Behav Brain Res 162: 173-181, 2005. (Pubitemid 40828529)
31. Nico PB, Lobao-Soares B, Landemberger MC, Marques W, Jr., Tasca CI, de Mello CF, Walz R, Carlotti CG, Jr., Brentani RR, Sakamoto AC, and Bianchin MM. Impaired exercise capacity, but unaltered mitochondrial respiration in skeletal or cardiac muscle of mice lacking cellular prion protein. Neurosci Lett 388: 21-26, 2005. (Pubitemid 41569364)
32. Nishimura T, Sakudo A, Nakamura I, Lee DC, Taniuchi Y, Saeki K, Matsumoto Y, Ogawa M, Sakaguchi S, Itohara S, and Onodera T. Cellular prion protein regulates intracellular hydrogen peroxide level and prevents copper-induced apoptosis. Biochem Biophys Res Commun 323: 218-222, 2004. (Pubitemid 39200671)
33. Ostlund P, Lindegren H, Pettersson C, and Bedecs K. Altered insulin receptor processing and function in scrapieinfected neuroblastoma cell lines. Brain Res Mol Brain Res 97: 161-170, 2001. (Pubitemid 34025095)
34. Pamplona R, Naudi A, Gavin R, Pastrana MA, Sajnani G, Ilieva EV, Del Rio JA, Portero-Otin M, Ferrer I, and Requena JR. Increased oxidation, glycoxidation, and lipoxidation of brain proteins in prion disease. Free Radic Biol Med 45: 1159-1166, 2008.
35. Pankiewicz J, Prelli F, Sy MS, Kascsak RJ, Kascsak RB, Spinner DS, Carp RI, Meeker HC, Sadowski M, and Wisniewski T. Clearance and prevention of prion infection in cell culture by anti-PrP antibodies. Eur J Neurosci 23: 2635-2647, 2006. (Pubitemid 43801455)
36. Powers SK and Jackson MJ. Exercise-induced oxidative stress: Cellular mechanisms and impact on muscle force production. Physiol Rev 88: 1243-1276, 2008.
37. Reid MB. Nitric oxide, reactive oxygen species, and skeletal muscle contraction. Med Sci Sports Exerc 33: 371-376, 2001. (Pubitemid 32209654)
38. Reid MB, Haack KE, Franchek KM, Valberg PA, Kobzik L, and West MS. Reactive oxygen in skeletal muscle. I. Intracellular oxidant kinetics and fatigue in vitro. J Appl Physiol 73: 1797-1804, 1992.
39. Rudd PM, Wormald MR, Wing DR, Prusiner SB, and Dwek RA. Prion glycoprotein: structure, dynamics, and roles for the sugars. Biochemistry 40: 3759-3766, 2001. (Pubitemid 32280412)
40. Sandstrom ME, Zhang SJ, Bruton J, Silva JP, Reid MB, Westerblad H, and Katz A. Role of reactive oxygen species in contraction-mediated glucose transport in mouse skeletal muscle. J Physiol 575: 251-262, 2006. (Pubitemid 44178142)
41. Schneider B, Mutel V, Pietri M, Ermonval M, Mouillet-Richard S, and Kellermann O. NADPH oxidase and extracellular regulated kinases 1/2 are targets of prion protein signaling in neuronal and nonneuronal cells. Proc Natl Acad Sci USA 100: 13326-13331, 2003. (Pubitemid 37444741)
42. Silberstein L, Webster SG, Travis M, and Blau HM. Developmental progression of myosin gene expression in cultured muscle cells. Cell 46: 1075-1081, 1986. (Pubitemid 17182731)
43. Singh A, Kong Q, Luo X, Petersen RB, Meyerson H, and Singh N. Prion protein (PrP) knock-out mice show altered iron metabolism: A functional role for PrP in iron uptake and transport. PLoS One 4: e6115, 2009.
44. Steele AD, Emsley JG, Ozdinler PH, Lindquist S, and Macklis JD. Prion protein (PrPc) positively regulates neural precursor proliferation during developmental and adult mammalian neurogenesis. Proc Natl Acad Sci USA 103: 3416-3421, 2006. (Pubitemid 43346483)
45. Stella R, Massimino ML, Sandri M, Sorgato MC, and Bertoli A. Cellular prion protein promotes regeneration of adult muscle tissue. Mol Cell Biol 30: 4864-4876, 2010.
46. Supinski G, Stofan D, Callahan LA, Nethery D, Nosek TM, and DiMarco A. Peroxynitrite induces contractile dysfunction and lipid peroxidation in the diaphragm. J Appl Physiol 87: 783-791, 1999. (Pubitemid 29375017)
47. Telling GC, Haga T, Torchia M, Tremblay P, DeArmond SJ, and Prusiner SB. Interactions between wild-type and mutant prion proteins modulate neurodegeneration in transgenic mice. Genes Dev 10: 1736-1750, 1996. (Pubitemid 26272380)
48. Westaway D, Cooper C, Turner S, Da Costa M, Carlson GA, and Prusiner SB. Structure and polymorphism of the mouse prion protein gene. Proc Natl Acad Sci USA 91: 6418-6422, 1994. (Pubitemid 24200672)
49. Wong BS, Liu T, Li R, Pan T, Petersen RB, Smith MA, Gambetti P, Perry G, Manson JC, Brown DR, and Sy MS. Increased levels of oxidative stress markers detected in the brains of mice devoid of prion protein. J Neurochem 76: 565-572, 2001. (Pubitemid 32097032)
50. Zhu H, Tucker HM, Grear KE, Simpson JF, Manning AK, Cupples LA, and Estus S. A common polymorphism decreases low-density lipoprotein receptor exon 12 splicing efficiency and associates with increased cholesterol. Hum Mol Genet 16: 1765-1772, 2007. (Pubitemid 47241835)