Cellular prion protein promotes regeneration of adult muscle tissue

Molecular and Cellular Biology

Volumn 30, Issue 20, 2010, Pages 4864-4876

  Stella, Roberto ^a   Massimino, Maria Lina ^a   Sandri, Marco ^a,b   Sorgato M Catia, M C ^a   Bertoli, Alessandro ^a  

^a UNIVERSITY OF PADOVA   (Italy)

^b VENETIAN INSTITUTE OF MOLECULAR MEDICINE   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE P38; PRION PROTEIN;

ANIMAL; ARTICLE; C57BL MOUSE; CELL CYCLE; CONGENIC STRAIN; CYTOLOGY; GENETICS; GROWTH, DEVELOPMENT AND AGING; INJURY; MALE; METABOLISM; MOUSE; MOUSE MUTANT; MUSCLE DEVELOPMENT; MYOBLAST; PHENOTYPE; PHYSIOLOGY; REGENERATION; SKELETAL MUSCLE; TRANSGENIC MOUSE;

ANIMALS; CELL CYCLE; MALE; MICE; MICE, CONGENIC; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MUSCLE DEVELOPMENT; MUSCLE, SKELETAL; MYOBLASTS, SKELETAL; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHENOTYPE; PRPC PROTEINS; REGENERATION;

EID: 78049403334     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.01040-09     Document Type: Article

References (74)

1. Aguzzi, A., F. Baumann, and J. Bremer. 2008. The prion's elusive reason for being. Annu. Rev. Neurosci. 31:439-477.
2. Sc accumulation in myocytes from sheep incubating natural scrapie. Nat. Med. 10:591-593.
3. Angers, R. C., S. R. Browning, T. S. Seward, C. J. Sigurdson, M. W. Miller, E. A. Hoover, and G. C. Telling. 2006. Prions in skeletal muscles of deer with chronic wasting disease. Science 311:1117.
4. Barton, E. R., L. Morris, A. Musarò, N. Rosenthal, and H. L. Sweeney. 2002. Muscle-specific expression of insulin-like growth factor I counters muscle decline in mdx mice. J. Cell Biol. 157:137-148.
5. Black, R. A. 2002. Tumor necrosis factor-alpha converting enzyme. Int. J. Biochem. Cell Biol. 34:1-5.
6. Bosque, P. J., C. Ryou, G. Telling, D. Peretz, G. Legname, S. J. DeArmond, and S. B. Prusiner. 2002. Prions in skeletal muscle. Proc. Natl. Acad. Sci. U. S. A. 99:3812-3817.
7. Buckingham, M., and D. Montarras. 2008. Skeletal muscle stem cells. Curr. Opin. Genet. Dev. 18:330-336.
8. Büeler, H., M. Fischer, Y. Lang, H. Bluethmann, H. P. Lipp, S. J. DeArmond, S. B. Prusiner, M. Aguet, and C. Weissmann. 1992. Normal development and behaviour of mice lacking the neuronal cell-surface PrP protein. Nature 356:577-582.
9. α pathway. Am. J. Physiol. Cell Physiol. 284:C658-C666.
10. Cantini, M., M. L. Massimino, A. Bruson, C. Catani, L. Dalla Libera, and U. Carraro. 1994. Macrophages regulate proliferation and differentiation of satellite cells. Biochem. Biophys. Res. Commun. 202:1688-1696.
11. Caughey, B., and G. S. Baron. 2006. Prions and their partners in crime. Nature 443:803-810.
12. Chargé, S. B., and M. A. Rudnicki. 2004. Cellular and molecular regulation of muscle regeneration. Physiol. Rev. 84:209-238.
13. Chen, S., A. Mange, L. Dong, S. Lehmann, and M. Schachner. 2003. Prion protein as trans-interacting partner for neurons is involved in neurite outgrowth and neuronal survival. Mol. Cell Neurosci. 22:227-233.
14. Chen, S. E., E. Gerken, Y. Zhang, M. Zhan, R. K Mohan, A. S. Li, M. B. Reid, and Y. P. Li. 2005. Role of TNF-alpha signaling in regeneration of cardiotoxin-injured muscle. Am. J. Physiol. Cell Physiol. 289:1179-1187.
15. Chen, S. E., B. Jin, and Y. P. Li. 2007. TNF-alpha regulates myogenesis and muscle regeneration by activating p38 MAPK. Am. J. Physiol. Cell Physiol. 292:1660-1671.
16. Sc-like molecules in peripheral tissues of transgenic mice expressing a prion protein insertional mutation. Neurobiol. Dis. 8:279-288.
17. Criado, J. R., M. Sanchez-Alavez, B. Conti, J. L. Giacchino, D. N. Wills, S. J. Henriksen, R. Race, J. C. Manson, B. Chesebro, and M. B. Oldstone. 2005. Mice devoid of prion protein have cognitive deficits that are rescued by reconstitution of PrP in neurons. Neurobiol. Dis. 19:255-265.
18. d'Albis, A., R. Couteaux, C. Janmot, A. Roulet, and J. C. Mira. 1988. Regeneration after cardiotoxin injury of innervated and denervated slow and fast muscles of mammals. Myosin isoform analysis. Eur. J. Biochem. 174: 103-110.
19. Dhawan, J., and T. A. Rando. 2005. Stem cells in postnatal myogenesis: molecular mechanisms of satellite cell quiescence, activation and replenishment. Trends Cell Biol. 15:666-673.
20. Donselaar, Y., O. Eerbeek, D. Kernell, and B. A. Verhey. 1987. Fibre sizes and histochemical staining characteristics in normal and chronically stimulated fast muscle of cat. J. Physiol. 382:237-354.
21. Glatzel, M., E. Abela, M. Maissen, and A. Aguzzi. 2003. Extraneural pathologic prion protein in sporadic Creutzfeldt-Jakob disease. N. Engl. J. Med. 349:1812-1820.
22. Graner, E., A. F. Mercadante, S. M. Zanata, O. V. Forlenza, A. L. Cabral, S. S. Veiga, M. A. Juliano, R. Roesler, R. Walz, A. Minetti, I. Izquierdo, V. R. Martins, and R. R. Brentani. 2000. Cellular prion protein binds laminin and mediates neuritogenesis. Brain Res. Mol. Brain Res. 76:85-92.
23. Hajj, G. N., M. H. Lopes, A. F. Mercadante, S. S. Veiga, R. B. da Silveira, T. G. Santos, K. C. Ribeiro, M. A. Juliano, S. G. Jacchieri, S. M. Zanata, and V. R. Martins. 2007. Cellular prion protein interaction with vitronectin supports axonal growth and is compensated by integrins. J. Cell Sci. 120: 1915-1926.
24. Harris, J. B. 2003. Myotoxic phospholipases A2 and the regeneration of skeletal muscles. Toxicon 42:933-945.
25. Huang, S., J. Liang, M. Zheng, X. Li, M. Wang, P. Wang, D. Vanegas, D. Wu, B. Chakraborty, A. P. Hays, K. Chen, S. G. Chen, S. Booth, M. Cohen, P. Gambetti, and Q. Kong. 2007. Inducible overexpression of wild-type prion protein in the muscles leads to a primary myopathy in transgenic mice. Proc. Natl. Acad. Sci. U. S. A. 104:6800-6805.
26. Isaacs, J. D., G. S. Jackson, and D. M. Altmann. 2006. The role of the cellular prion protein in the immune system. Clin. Exp. Immunol. 146:1-8.
27. Kanaani, J., S. B. Prusiner, J. Diacovo, S. Baekkeskov, and G. Legname. 2005. Recombinant prion protein induces rapid polarization and development of synapses in embryonic rat hippocampal neurons in vitro. J. Neurochem. 95:1373-1386.
28. Keren, A., Y. Tamir, and E. Bengal. 2006. The p38 MAPK signaling pathway: a major regulator of skeletal muscle development. Mol. Cell Endocrinol. 252:224-230.
29. Khosravani, H., Y. Zhang, S. Tsutsui, S. Hameed, C. Altier, J. Hamid, L. Chen, M. Villemaire, Z. Ali, F. R. Jirik, and G. W. Zamponi. 2008. Prion protein attenuates excitotoxicity by inhibiting NMDA receptors. J. Cell Biol. 181:551-565.
30. Klamt, F., F. Dal-Pizzol, M. J. Conte da Frota, R. Walz, M. E. Andrades, E. G. da Silva, R. R. Brentani, I. Izquierdo, and J. C. Fonseca Moreira. 2001. Imbalance of antioxidant defense in mice lacking cellular prion protein. Free Radic. Biol. Med. 30:1137-1144.
31. Kuang, S., M. A. Gillespie, and M. A. Rudnicki. 2008. Niche regulation of muscle satellite cell self-renewal and differentiation. Cell Stem Cell 2:22-31.
32. Lawlor, M. A., and P. Rotwein. 2000. Insulin-like growth factor-mediated muscle cell survival: central roles for Akt and cyclin-dependent kinase inhibitor p21. Mol. Cell Biol. 20:8983-8995.
33. Le Grand, F., and M. A. Rudnicki. 2007. Skeletal muscle satellite cells and adult myogenesis. Curr. Opin. Cell Biol. 19:628-633.
34. Li, Y. P., and R. J. Schwartz. 2001. TNF-alpha regulates early differentiation of C2C12 myoblasts in an autocrine fashion. FASEB J. 15:1413-1415.
35. Linden, R., V. R. Martins, M. A. Prado, M. Cammarota, I. Izquierdo, and R. R. Brentani. 2008. Physiology of the prion protein. Physiol. Rev. 88:673-728.
36. Lopes, M. H., G. N. Hajj, A. G. Muras, G. L. Mancini, R. M. Castro, K. C. Ribeiro, R. R. Brentani, R. Linden, and V. R. Martins. 2005. Interaction of cellular prion and stress-inducible protein 1 promotes neuritogenesis and neuroprotection by distinct signaling pathways. J. Neurosci. 25:11330-11339.
37. Lundberg, I. E., and M. Dastmalchi. 2002. Possible pathogenic mechanisms in inflammatory myopathies. Rheum. Dis. Clin. North Am. 28:799-822.
38. Malaga-Trillo, E., G. P. Solis, Y. Schrock, C. Geiss, L. Luncz, V. Thomanetz, and C. A. Stuermer. 2009. Regulation of embryonic cell adhesion by the prion protein. PLoS Biol. 7:e55.
39. Mallucci, G., A. Dickinson, J. Linehan, P. C. Klohn, S. Brandner, and J. Collinge. 2003. Depleting neuronal PrP in prion infection prevents disease and reverses spongiosis. Science 302:871-874.
40. Mallucci, G. R., S. Ratte, E. A. Asante, J. Linehan, I. Gowland, J. G. Jefferys, and J. Collinge. 2002. Post-natal knockout of prion protein alters hippocampal CA1 properties, but does not result in neurodegeneration. EMBO J. 21:202-210.
41. Manson, J., J. D. West, V. Thomson, P. McBride, M. H. Kaufman, and J. Hope. 1992. The prion protein gene: a role in mouse embryogenesis? Development 115:117-122.
42. Manson, J. C., A. R. Clarke, M. L. Hooper, L. Aitchison, I. McConnell, and J. Hope. 1994. 129/Ola mice carrying a null mutation in PrP that abolishes mRNA production are developmentally normal. Mol. Neurobiol. 8:121-127.
43. Massimino, M. L., J. Ferrari, M. C. Sorgato, and A. Bertoli. 2006. Heterogeneous PrPC metabolism in skeletal muscle cells. FEBS Lett. 580:878-884.
44. McKnight, A. J., A. J. Macfarlane, P. Dri, L. Turley, A. C. Willis, and S. Gordon. 1996. Molecular cloning of F4/80, a murine macrophage-restricted cell surface glycoprotein with homology to the G-protein-linked transmembrane 7 hormone receptor family. J. Biol. Chem. 271:486-489.
45. Merly, F., L. Lescaudron, T. Rouaud, F. Crossin, and M. F. Gardahaut. 1999. Macrophages enhance muscle satellite cell proliferation and delay their differentiation. Muscle Nerve 22:724-732.
46. Miele, G., A. R. Alejo Blanco, H. Baybutt, S. Horvat, J. Manson, and M. Clinton. 2003. Embryonic activation and developmental expression of the murine prion protein gene. Gene Expr. 11:1-12.
47. Musarò, A., K. J. McCullagh, F. J. Naya, E. N. Olson, and N. Rosenthal. 1999. IGF-1 induces skeletal myocyte hypertrophy through calcineurin in association with GATA-2 and NF-ATc1. Nature 400:581-585.
48. Musarò, A., K. McCullagh, A. Paul, L. Houghton, G. Dobrowolny, M. Molinaro, E. R. Barton, H. L. Sweeney, and N. Rosenthal. 2001. Localized Igf-1 transgene expression sustains hypertrophy and regeneration in senescent skeletal muscle. Nat. Genet. 27:195-200.
49. Nachlas, M. M., K. C. Tsou, E. De Souza, C. S. Cheng, and A. M. Seligman. 1957. Cytochemical demonstration of succinic dehydrogenase by the use of a new p-nitrophenyl substituted ditetrazole. J. Histochem. Cytochem. 5:420- 436.
50. Nazor, K. E., T. Seward, and G. C. Telling. 2007. Motor behavioral and neuropathological deficits in mice deficient for normal prion protein expression. Biochim. Biophys. Acta 1772:645-653.
51. Nico, P. B., B. Lobao-Soares, M. C. Landemberger, W. Marques, Jr., C. I. Tasca, C. F. de Mello, R. Walz, C. G. Carlotti, Jr., R. R. Brentani, A. C. Sakamoto, and M. M. Bianchin. 2005. Impaired exercise capacity, but unaltered mitochondrial respiration in skeletal or cardiac muscle of mice lacking cellular prion protein. Neurosci. Lett. 388:21-26.
52. Parkin, E. T., N. T. Watt, I. Hussain, E. A. Eckman, C. B. Eckman, J. C. Manson, H. N. Baybutt, A. J. Turner, and N. M. Hooper. 2007. Cellular prion protein regulates beta-secretase cleavage of the Alzheimer's amyloid precursor protein. Proc. Natl. Acad. Sci. U. S. A. 104:11062-11067.
53. Peden, A. H., D. L. Ritchie, M. W. Head, and J. W. Ironside. 2006. Detection and localization of PrPSc in the skeletal muscle of patients with variant, iatrogenic, and sporadic forms of Creutzfeldt-Jakob disease. Am. J. Pathol. 168:927-935.
54. Pradines, E., D. Loubet, S. Mouillet-Richard, P. Manivet, J. M. Launay, O. Kellermann, and B. Schneider. 2009. Cellular prion protein coupling to TACE-dependent TNF-alpha shedding controls neurotransmitter catabolism in neuronal cells. J. Neurochem. 110:912-923.
55. Prestori, F., P. Rossi, B. Bearzatto, J. Laine, D. Necchi, S. Diwakar, S. N. Schiffmann, H. Axelrad, and E. D'Angelo. 2008. Altered neuron excitability and synaptic plasticity in the cerebellar granular layer of juvenile prion protein knock-out mice with impaired motor control. J. Neurosci. 28:7091- 7103.
56. Prusiner, S. B. 1998. Prions. Proc. Natl. Acad. Sci. U. S. A. 95:13363-13383.
57. Reid, M. B., and Y. P. Li. 2001. Tumor necrosis factor-alpha and muscle wasting: a cellular perspective. Respir. Res. 2:269-272.
58. Rommel, C., S. C. Bodine, B. A. Clarke, R. Rossman, L. Nunez, T. N. Stitt, G. D. Yancopoulos, and D. J. Glass. 2001. Mediation of IGF-1-induced skeletal myotube hypertrophy by PI(3)K/Akt/mTOR and PI(3)K/Akt/GSK3 pathways. Nat. Cell Biol. 3:1009-1013.
59. Santuccione, A., V. Sytnyk, I. Leshchyns'ka, and M. Schachner. 2005. Prion protein recruits its neuronal receptor NCAM to lipid rafts to activate p59fyn and to enhance neurite outgrowth. J. Cell Biol. 169:341-354.
60. Schiaffino, S., M. Sandri, and M. Murgia. 2007. Activity-dependent signaling pathways controlling muscle diversity and plasticity. Physiology 22:269-278.
61. Serra, C., D. Palacios, C. Mozzetta, S. V. Forcales, I. Morantte, M. Ripani, D. R. Jones, K. Du, U. S. Jhala, C. Simone, and P. L. Puri. 2007. Functional interdependence at the chromatin level between the MKK6/p38 and IGF1/ PI3K/AKT pathways during muscle differentiation. Mol. Cell 28:200-213.
62. Simone, C., S. V. Forcales, D. A. Hill, A. N. Imbalzano, L. Latella, and P. L. Puri. 2004. p38 pathway targets SWI-SNF chromatin-remodeling complex to muscle-specific loci. Nat. Genet. 36:738-743.
63. Sorgato, M. C., C. Peggion, and A. Bertoli. 2009. Is, indeed, the prion protein a Harlequin servant of "many" masters?. Prion 3:202-205.
64. C) positively regulates neural precursor proliferation during developmental and adult mammalian neurogenesis. Proc. Natl. Acad. Sci. U. S. A. 103:3416-3421.
65. Steele, A. D., S. Lindquist, and A. Aguzzi. 2007. The prion protein knockout mouse: a phenotype under challenge. Prion 1:83-93.
66. Telling G. C., T. Haga, M. Torchia, P. Tremblay, S. J. DeArmond, and S. B. Prusiner. 1996. Interactions between wild-type and mutant prion proteins modulate neurodegeneration in transgenic mice. Genes Dev. 10:1736-1750.
67. Thomzig, A., W. Schulz-Schaeffer, C. Kratzel, J. Mai, and M. Beekes. 2004. Preclinical deposition of pathological prion protein PrPSc in muscles of hamsters orally exposed to scrapie. J. Clin. Invest. 113:1465-1472.
68. Westaway, D., S. J. DeArmond, J. Cayetano-Canlas, D. Groth, D. Foster, S. L. Yang, M. Torchia, G. A. Carlson, and S. B. Prusiner. 1994. Degeneration of skeletal muscle, peripheral nerves, and the central nervous system in transgenic mice overexpressing wild-type prion proteins. Cell 76:117-129.
69. Wu, Z., P. J. Woodring, K. S. Bhakta, K. Tamura, F. Wen, J. R. Feramisco, M. Karin, J. Y. Wang, and P. L. Puri. 2000. p38 and extracellular signalregulated kinases regulate the myogenic program at multiple steps. Mol. Cell. Biol. 20:3951-3964.
70. Zammit, P. S. 2008. All muscle satellite cells are equal, but are some more equal than others? J. Cell Sci. 121:2975-2982.
71. Zanusso, G., G. Vattemi, S. Ferrari, M. Tabaton, E. Pecini, T. Cavallaro, G. Tomelleri, M. Filosto, P. Tonin, E. Nardelli, N. Rizzuto, and S. Monaco. 2001. Increased expression of the normal cellular isoform of prion protein in inclusion-body myositis, inflammatory myopathies and denervation atrophy. Brain Pathol. 11:182-189.
72. Zetser, A., E. Gredinger, and E. Bengal. 1999. p38 mitogen-activated protein kinase pathway promotes skeletal muscle differentiation. Participation of the Mef2c transcription factor. J. Biol. Chem. 274:5193-5200.
73. Zhan, M., B. Jin, S. E. Chen, J. M. Reecy, and Y. P. Li. 2007. TACE release of TNF-alpha mediates mechanotransduction-induced activation of p38 MAPK and myogenesis. J. Cell Sci. 120:692-701.
74. Zhang, C. C., A. D. Steele, S. Lindquist, and H. F. Lodish. 2006. Prion protein is expressed on long-term repopulating hematopoietic stem cells and is important for their self-renewal. Proc. Natl. Acad. Sci. U. S. A. 103:2184- 2189.