Role of cellular prion proteins in the function of macrophages and dendritic cells

Protein and Peptide Letters

Volumn 16, Issue 3, 2009, Pages 239-246

  Nitta, Kayako ^a   Sakudo, Akikazu ^b   Masuyama, Jun ^a   Xue, Guangai ^a   Sugiura, Katsuaki ^c   Onodera, Takashi ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b OSAKA UNIVERSITY   (Japan)

^c FOOD AND AGRICULTURAL MATERIALS INSPECTION CENTER   (Japan)

Author keywords

Macrophage; Phagocytotic activity; PrPc; PrPSc; TSE

Indexed keywords

PRION PROTEIN;

ANIMAL; ARTICLE; DENDRITIC CELL; GENE EXPRESSION REGULATION; GENETICS; HUMAN; IMMUNOLOGY; MACROPHAGE; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PHAGOCYTOSIS; PRION DISEASE;

ANIMALS; DENDRITIC CELLS; GENE EXPRESSION REGULATION; HUMANS; MACROPHAGES; PHAGOCYTOSIS; PRION DISEASES; PRPC PROTEINS;

MUS;

EID: 63449117497     PISSN: 09298665     EISSN: None     Source Type: Journal    
DOI: 10.2174/092986609787601705     Document Type: Article

References (68)

1. Prusiner, S.B, Prions. Proc. Natl. Acad. Sci. U. S. A., 1998, 95, 13363-13383.
2. Sakudo, A.; Nakamura, I.: Ikuta, K.: Onodera, T. Recent developments in prion disease research: diagnostic tools and in vitro cell culture models. J. Vet. Med. Sci., 2007, 69, 329-337.
3. Will, R.G.; Zeidler, M.; Stewart, G.E.; Macleod, M.A.; Ironside, J.W.: Cousens, S.N.; Mackenzie, J.; Estibeiro, K.; Green, A.J.; Knight, R.S. Diagnosis of new variant Creutzfeldt-Jakob disease. Ann. Neurol., 2000, 47, 575-582.
4. Prusiner, S.B. Novel proteinaceous infectious particles cause scrapie. Science, 1982, 216, 136-144.
5. Manson, J.C.; Clarke, A.R.; McBride, P.A.; McConnell, I.; Hope, J. PrP gene dosage determines the timing but not the final intensity or distribution of lesions in scrapie pathology. Neurodegeneration, 1994, 3, 331-340.
6. Sakudo, A.; Lee, D.C.: Yoshimura, E.; Nagasaka, S.; Nitta, K.; Saeki, K.; Matsumoto, Y.; Lehmann, S.; Itohara, S.; Sakaguchi, S.; Onodera, T. Prion protein suppresses perturbation of cellular copper homeostasis under oxidative conditions. Biochem. Biophys. Res. Commun., 2004, 313, 850-855.
7. Kretzschmar, H.A.; Prusiner, S.B.; Stowring, L.E.; DeArmond, S.J. Scrapie prion proteins are synthesized in neurons. Am. J. Pathol., 1986, 122, 1-5.
8. Fournier, J.G. Nonneuronal cellular prion protein. Int. Rev. Cytol., 2001, 208, 121-160.
9. Bendheim, P.E.; Brown, H.R.; Rudelli, R.D.; Scala, L.J.; Goller, N.L.; Wen, G.Y.; Kascsak, R.J.; Cashman, N.R.; Bolton, D.C. Nearly ubiquitous tissue distribution of the scrapie agent precursor protein. Neurology, 1992, 42, 149-156.
10. Fournier, J.G.; Escaig-Haye, F.; Billette de Villemeur, T.; Robain, O.; Lasmezas, C.I.; Deslys, J.P.; Dormont, D.; Brown, P. Distribution and submicroscopic immunogold localization of cellular prion protein (PrPc) in extracerebral tissues. Cell Tissue Res., 1998, 292, 77-84.
11. Horiuchi, M.; Yamazaki, N.; Ikeda, T.; Ishiguro, N.; Shinagawa, M. A cellular form of prion protein (PrPC) exists in many nonneuronal tissues of sheep. J. Gen. Virol., 1995, 76, 2583-2587.
12. Moudjou, M.; Frobert, Y.; Grassi, J.; La Bonnardiere, C. Cellular prion protein status in sheep: tissue-specific biochemical signatures. J. Gen. Virol., 2001, 82, 2017-2024.
13. Bosque, P.J.; Ryou, C.; Telling, G.; Peretz, D.; Legname, G.; DeArmond, S.J.; Prusiner, S.B. Prions in skeletal muscle. Proc. Natl. Acad. Sci. USA, 2002, 99, 3812-3817.
14. Li, R.; Liu, D.; Zanusso, G.; Liu, T.; Fayen, J.D.; Huang, J.H.; Petersen, R.B.; Gambetti, P.; Sy, M.S. The expression and potential function of cellular prion protein in human lymphocytes. Cell Immunol., 2001, 207, 49-58.
15. Burthem, J.; Urban, B.; Pain, A.; Roberts, D.J. The normal cellular prion protein is strongly expressed by myeloid dendritic cells. Blood, 2001, 98, 3733-3738.
16. Dodelet, V.C.; Cashman, N.R. Prion protein expression in human leukocyte differentiation. Blood, 1998, 91, 1556-1561.
17. Durig, J.; Giese, A.; Schulz-Schaeffer, W.: Rosenthal, C.; Schmucker, U.; Bieschke, J.; Duhrsen, U.; Kretzschmar, H.A. Differential constitutive and activation-dependent expression of prion protein in human peripheral blood leucocytes. Br. J. Haematol., 2000, 108, 488-495.
18. Politopoulou, G.; Seebach, J.D.; Schmugge, M.; Schwarz, H.P.; Aguzzi, A. Age-related expression of the cellular prion protein in human peripheral blood leukocytes. Haematologica, 2000, 85, 580-587.
19. Cashman, N.R.; Loertscher, R.; Nalbantoglu, J.; Shaw, I.; Kascsak, R.J.; Bolton, D.C; Bendheim, P.E. Cellular isoform of the scrapie agent protein participates in lymphocyte activation. Cell, 1990, 61, 185-192.
20. Barclay, G.R.; Hope, J.; Birkett, C.R.; Turner, M.L. Distribution of cell-associated prion protein in normal adult blood determined by flow cytometry. Br. J. Haematol., 1999, 107, 804-814.
21. Antoine, N.: Cesbron, J.Y.; Coumans, B.: Jolois, O.; Zorzi, W.; Heinen, E. Differential expression of cellular prion protein on human blood and tonsil lymphocytes. Haematologica, 2000, 85, 475-480.
22. Holada, K.; Vostal, J.G. Different levels of prion protein (PrPc) expression on hamster, mouse and human blood cells. Br. J. Haematol, 2000, 110, 472-480.
23. Thielen, C: Antoine, N.; Melot, F.: Cesbron, J.Y.: Heinen, E.: Tsunoda, R. Human FDC express PrPc in vivo and in vitro. Dev. Immunol, 2001, 8, 259-266.
24. Brown, K.L.; Stewart, K.; Ritchie, D.L.; Mabbott, N.A.; Williams, A.; Fraser, H.; Morrison, W.I.; Bruce, M.E. Scrapie replication in lymphoid tissues depends on prion protein-expressing follicular dendritic cells. Nat. Med., 1999, 5, 1308-1312.
25. Montrasio, F.; Frigg, R.; Glatzel, M.; Klein, M.A.; Mackay, F.; Aguzzi, A.; Weissmann, C. Impaired prion replication in spleens of mice lacking functional follicular dendritic cells. Science, 2000, 288, 1257-1259.
26. Inoue, Y.; Yamakawa, Y.; Sakudo, A.; Kinumi, T.; Nakamura, Y.; Matsumoto, Y.: Saeki, K.; Kamiyama, T.: Onodera, T.; Nishijima, M. Infection route-independent accumulation of splenic abnormal prion protein. Jpn. J. Infect. Dis., 2005, 58, 78-82.
27. Martinez del Hoyo, G.; Lopez-Bravo, M.; Metharom, P.; Ardavin, C.; Aucouturier, P. Prion protein expression by mouse dendritic cells is restricted to the nonplasmacytoid subsets and correlates with the maturation state. J. Immunol., 2006, 177, 6137-6142.
28. Ballerini, C.; Gourdain, P.; Bachy, V.; Blanchard, N.; Levavasseur, E.; Gregoire, S.; Fontes, P.; Aucouturier, P.; Hivroz, C.; Carnaud, C Functional implication of cellular prion protein in antigen-driven interactions between T cells and dendritic cells. J. Immunol., 2006, 176, 7254-7262.
29. de Almeida, C.J.; Chiarini, L.B.; da Silva, J.P.; PM, E.S.: Martins, M.A.; Linden, R. The cellular prion protein modulates phagocytosis and inflammatory response. J. Leukoc. Biol., 2005, 77, 238-246.
30. Krebs, B.; Dorner-Ciossek, C.; Schmalzbauer, R.; Vassallo, N.; Herms, J.; Kretzschmar, H.A. Prion protein induced signaling cascades in monocytes. Biochem. Biophys. Res. Commun., 2006, 340, 13-22.
31. Aucouturier, P.; Carp, R.I.; Carnaud, C.; Wisniewski, T. Prion diseases and the immune system. Clin. Immunol., 2000, 96, 79-85.
32. Rezaie, P.; Lantos, P.L. Microglia and the pathogenesis of spongiform encephalopathies. Brain Res. Brain Res. Rev., 2001, 35, 55-72.
33. Prinz, M.; Montrasio, F.; Klein, M.A.; Schwarz, P.; Priller, J.; Odermatt, B.; Pfeffer, K.; Aguzzi, A. Lymph nodal prion replication and neuroinvasion in mice devoid of follicular dendritic cells. Proc. Natl. Acad. Sci. USA, 2002, 99, 919-924.
34. Beringue, V.; Adjou, K.T.; Lamoury, F.; Maignien, T.: Deslys, J.P.; Race, R.; Dormont, D. Opposite effects of dextran sulfate 500, the polyene antibiotic MS-8209, and Congo red on accumulation of the protease-resistant isoform of PrP in the spleens of mice inoculated intraperitoneally with the scrapie agent. J. Virol., 2000, 74, 5432-5440.
35. Beringue, V.; Demoy, M.; Lasmezas, C.I.; Gouritin, B.; Weingarten, C.; Deslys, J.P.; Andreux, J.P.; Couvreur, P.; Dormont, D. Role of spleen macrophages in the clearance of scrapie agent early in pathogenesis. J. Pathol., 2000, 190, 495-502.
36. Sakudo, A.; Onodera, T.; Suganuma, Y.; Kobayashi, T.; Saeki, K.; Ikuta, K. Recent advances in clarifying prion protein functions using knockout mice and derived cell lines. Mini Rev. Med. Chem., 2006, 6, 589-601.
37. Sakudo, A.; Lee, D.C.; Saeki, K.; Nakamura, Y.; Inoue, K.; Matsumoto, Y.; Itohara, S.; Onodera, T. Impairment of superoxide dismutase activation by N-terminally truncated prion protein (PrP) in PrP-deficient neuronal cell line. Biochem. Biophys. Res. Commun., 2003, 308, 660-667.
38. Sakudo, A.; Lee, D.C.; Nishimura, T.; Li, S.; Tsuji, S.; Nakamura, T.; Matsumoto, Y.; Saeki, K.; Itohara, S.; Ikuta, K.: Onodera, T. Octapeptide repeat region and N-terminal half of hydrophobic region of prion protein (PrP) mediate PrP-dependent activation of superoxide dismutase. Biochem. Biophys. Res. Commun., 2005, 326, 600-606.
39. Sakudo, A.; Lee, D.C.; Li, S.; Nakamura, T.: Matsumoto, Y.; Saeki, K.; Itohara, S.; Ikuta, K.; Onodera, T. PrP cooperates with STI1 to regulate SOD activity in PrP-deficient neuronal cell line. Biochem. Biophys. Res. Commun., 2005, 328, 14-19.
40. Brown, D.R.; Besinger, A. Prion protein expression and superoxide dismutase activity. Biochem. J., 1998, 334, 423-429.
41. Babior, B.M. Phagocytes and oxidative stress. Am. J. Med., 2000, 109, 33-44.
42. Brown, D.R. Microglia and prion disease. Microsc. Res. Tech., 2001, 54, 71-80.
43. Dheen, S.T.; Kaur, C.; Ling, E.A. Microglial activation and its implications in the brain diseases. Curr. Med. Chem., 2007, 14, 1189-1197.
44. Sakudo, A.; Nakamura, I.; Lee, D.C.; Saeki, K.; Ikuta, K.; Onodera, T. Neurotoxic prion protein (PrP) fragment 106-126 requires the N-terminal half of the hydrophobic region of PrP in the PrP-deficient neuronal cell line. Protein Pept. Lett., 2007, 14, 1-6.
45. Ciesielski-Treska, I.; Grant, N.I.; Ulrich, G.; Corrotte, M.; Bailly, Y.; Haeberle, A.M.; Chasserot-Golaz, S.; Bader, M.F. Fibrillar prion peptide (106-126) and scrapie prion protein hamper phagocytosis in microglia. Glia, 2004, 46, 101-115.
46. Kim, C.K.; Sakudo, A.; Taniuchi, Y.; Shigematsu, K.; Kang, C.B.; Saeki, K.; Matsumoto, Y.; Sakaguchi, S.; Itohara, S.; Onodera, T. Late-onset olfactory deficits and mitral cell loss in mice lacking prion protein with ectopic expression of Doppel. Int. J. Mol Med., 2007, 20, 169-176.
47. Kim, C.K.; Hirose, Y.; Sakudo, A.; Takeyama, N.; Kang, C.B.; Taniuchi, Y.; Matsumoto, Y.; Itohara, S.; Sakaguchi, S.; Onodera, T. Reduced response of splenocytes after mitogen-stimulation in the prion protein (PrP) gene-deficient mouse: PrPLP/Doppel production and cerebral degeneration. Biochem. Biophys. Res. Commun., 2007, 358, 469-474.
48. Kubosaki, A.; Yusa, S.; Nasu, Y.; Nishimura, T.; Nakamura, Y.; Saeki, K.; Matsumoto, Y.; Itohara, S.; Onodera, T. Distribution of cellular isoform of prion protein in T lymphocytes and bone marrow, analyzed by wild-type and prion protein gene-deficient mice. Biochem. Biophys. Res. Commun., 2001, 282, 103-107.
49. Seiler, P.; Aichele, P.; Odermatt, B.; Hengartner, H.; Zinkernagel, R.M.; Schwendener, R.A. Crucial role of marginal zone macrophages and marginal zone metallophils in the clearance of lymphocytic choriomeningitis virus infection. Eur. J. Immunol., 1997, 27, 2626-2633.
50. Bueler, H.; Fischer, M.; Lang, Y.; Bluethmann, H.; Lipp, H.P.; DeArmond, S.J.; Prusiner, S.B.; Aguet, M.; Weissmann, C. Normal development and behaviour of mice lacking the neuronal cellsurface PrP protein. Nature, 1992, 356, 577-582.
51. Rossi, D.; Cozzio, A.; Flechsig, E.; Klein, M.A.; Rulicke, T.; Aguzzi, A.; Weissmann, C. Onset of ataxia and Purkinje cell loss in PrP null mice inversely correlated with Dpl level in brain. EMBO J., 2001, 20, 694-702.
52. Manson, J.C.; Clarke, A.R.; Hooper, M.L.; Aitchison, L.; McConnell, I.; Hope, J. 129/Ola mice carrying a null mutation in PrP that abolishes mRNA production are developmentally normal. Mol. Neurobiol., 1994, 8, 121-127.
53. Sakaguchi, S.; Katamine, S.; Nishida, N.; Moriuchi, R.; Shigematsu, K.; Sugimoto, T.; Nakatani, A.; Kataoka, Y.; Houtani, T.; Shirabe, S.; Okada, H.; Hasegawa, S.; Miyamoto, T.; Noda, T. Loss of cerebellar Purkinje cells in aged mice homozygous for a disrupted PrP gene. Nature, 1996, 380, 528-531.
54. Moore, R.C.; Lee, I.Y.; Silverman, G.L.; Harrison, P.M.; Strome, R.; Heinrich, C; Karunaratne, A.; Pasternak, S.H.; Chishti, M.A.; Liang, Y.; Mastrangelo, P.; Wang, K.; Smit, A.F.; Katamine, S.; Carlson, G.A.; Cohen, F.E.; Prusiner, S.B.; Melton, D.W.; Tremblay, P.; Hood, L.E.; Westaway, D. Ataxia in prion protein (PrP)-deficient mice is associated with upregulation of the novel PrP-like protein doppel. J. Moi. Biol., 1999, 292, 797-817.
55. Perry, V.H.; Hume, D.A.; Gordon, S. Immunohistochemical localization of macrophages and microglia in the adult and developing mouse brain. Neuroscience, 1985, 15, 313-326.
56. Williams, A.; Van Dam, A.M.; Ritchie, D.; Eikelenboom, P.; Fraser, H. Immunocytochemical appearance of cytokines, prostaglandin E2 and lipocortin-1 in the CNS during the incubation period of murine scrapie correlates with progressive PrP accumulations. Brain Res., 1997, 754, 171-180.
57. Herrmann, L.M.; Davis, W.C.; Knowles, D.P.; Wardrop, K.J.; Sy, M.S.; Gambetti, P.; KI, O.R. Cellular prion protein is expressed on peripheral blood mononuclear cells but not platelets of normal and scrapie-infected sheep. Haematologica, 2001, 86, 146-153.
58. Schmitt-Ulms, G.; Legname, G.; Baldwin, M.A.; Ball, H.L.; Bradon, N.; Bosque, P.J.; Crossin, K.L.; Edelman, G.M.; DeArmond, S.J.; Cohen, F.E.; Prusiner, S.B. Binding of neural cell adhesion molecules (N-CAMs) to the cellular prion protein. J. Mol. Biol., 2001, 314, 1209-1225.
59. Rieger, R.; Edenhofer, F.; Lasmezas, C.I.; Weiss, S. The human 37-kDa laminin receptor precursor interacts with the prion protein in eukaryotic cells. Nat. Med., 1997, 3, 1383-1388.
60. Graner, E.; Mercadante, A.F.; Zanata, S.M.; Forlenza, O.V.; Cabrai, A.L.; Veiga, S.S.; Juliano, M.A.; Roesler, R.; Walz, R.; Minetti, A.; Izquierdo, I.; Martins, V.R.; Brentani, R.R. Cellular prion protein binds laminin and mediates neuritogenesis. Brain Res. Mol. Brain Res., 2000, 76, 85-92.
61. Gauczynski, S.; Peyrin, J.M.; Haik, S.; Leucht, C; Hundt, C; Rieger, R.; Krasemann, S.; Deslys, J.P.; Dormont, D.; Lasmezas, C.I.; Weiss, S. The 37-kDa/67-kDa laminin receptor acts as the cell-surface receptor for the cellular prion protein. EMBO J., 2001, 20, 5863-5875.
62. Kuwahara, C.; Takeuchi, A.M.; Nishimura, T.; Haraguchi, K.; Kubosaki, A.; Matsumoto, Y.; Saeki, K.; Yokoyama, T.; Itohara, S.; Onodera, T. Prions prevent neuronal cell-line death. Nature, 1999, 400, 225-226.
63. Yokoyama, T.; Kimura, K.M.; Ushiki, Y.; Yamada, S.; Morooka, A.; Nakashiba, T.; Sassa, T.; Itohara, S. In vivo conversion of cellular prion protein to pathogenic isoforms, as monitored by conformation-specific antibodies. J. Biol. Chem., 2001, 276, 11265-11271.
64. Fridovich, I. The biology of oxygen radicals. Science, 1978, 201, 875-880.
65. Wong, B.S.; Pan, T.; Liu, T.; Li, R.; Gambetti, P.; Sy, M.S. Differential contribution of superoxide dismutase activity by prion protein in vivo. Biochem. Biophys. Res. Commun., 2000, 273, 136-139.
66. Marikovsky, M.; Ziv, V.; Nevo, N.; Harris-Cerruti, C; Mahler, O. Cu/Zn superoxide dismutase plays important role in immune response. J. Immunol., 2003, 170, 2993-3001.
67. Tatarczuch, L.; Bischof, R.J.; Philip, C.J.; Lee, CS. Phagocytic capacity of leucocytes in sheep mammary secretions following weaning. J. Anal., 2002, 201, 351-361.
68. Gengelbach, G.P.; Ward, J.D.; Spears, J.W.; Brown, T.T., Jr. Effects of copper deficiency and copper deficiency coupled with high dietary iron or molybdenum on phagocytic cell function and response of calves to a respiratory disease challenge. J. Anim. Sci., 1997, 75, 1112-1118.