Ablation of the cellular prion protein, PrPC, specifically on follicular dendritic cells has no effect on their maturation or function

Immunology

Volumn 138, Issue 3, 2013, Pages 246-257

  McCulloch, Laura ^a   Brown, Karen L ^a   Mabbott, Neil A ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Antibody response; Follicular dendritic cell; Germinal centre; Prion protein; Spleen

Indexed keywords

IMMUNOGLOBULIN G; IMMUNOGLOBULIN G2A; IMMUNOGLOBULIN G2B; IMMUNOGLOBULIN G3; IMMUNOGLOBULIN M; PRION PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY AFFINITY; ANTIBODY PRODUCTION; ANTIBODY RESPONSE; ANTIGEN ANTIBODY COMPLEX; ANTIGEN SPECIFICITY; ARTICLE; B LYMPHOCYTE; CELL FUNCTION; CELL MATURATION; CELL STRUCTURE; CONTROLLED STUDY; FOLLICULAR DENDRITIC CELL; LYMPHOID TISSUE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION;

ANIMALS; ANTIBODY AFFINITY; ANTIBODY FORMATION; ANTIGEN-ANTIBODY COMPLEX; ANTIGENS; CELL DIFFERENTIATION; DENDRITIC CELLS, FOLLICULAR; GERMINAL CENTER; MICE; MICE, TRANSGENIC; PRPC PROTEINS;

EID: 84873315035     PISSN: 00192805     EISSN: 13652567     Source Type: Journal    
DOI: 10.1111/imm.12031     Document Type: Article

References (70)

1. Heinen E, Bosseloir A, Bouzahzah F. Follicular dendritic cells: origin and function. Curr Top Microbiol Immunol 1995; 201:15-47.
2. Wang X, Cho B, Suzuki K, Xu Y, Green JA, An J, Cyster JG. Follicular dendritic cells help establish follicle identity and promote B cell retention in germinal centers. J Exp Med 2011; 208:2497-510.
3. Kapasi ZF, Burton GF, Shultz LD, Tew JG, Szakal AK. Induction of functional follicular dendritic cell development in severe combined immunodeficiency mice. Influence of B and T cells. J Immunol 1993; 150:2648-58.
4. Kapasi ZF, Qin D, Kerr WG, Kosco-Vilbois MH, Shultz LD, Tew JG, Szakal AK. Follicular dendritic cell (FDC) precursors in primary lymphoid tissues. J Immunol 1998; 160:1078-84.
5. Balogh P, Aydar Y, Tew JG, Szakal AK. Ontogeny of the follicular dendritic cell phenotype and function in the postnatal murine spleen. Cell Immunol 2001; 214:45-53.
6. Chaplin DD, Fu YX. Cytokine regulation of secondary lymphoid organ development. Curr Opin Immunol 1998; 10:289-97.
7. Victoratos P, Lagnel J, Tzima S, Alimzhanov MB, Rajewsky K, Pasparakis M, Kollias G. FDC-specific functions of p55TNFR and IKK2 in the development of FDC networks and of antibody responses. Immunity 2006; 24:65-77.
8. Krautler NJ, Kana V, Kranich J, et al. Follicular dendritic cells emerge from ubiquitous perivascular precursors. Cell 2012; 150:194-206.
9. Qin D, Wu J, Vora KA, Ravetch JV, Szakal AK, Manser T, Tew JG. Fcγ receptor IIB on follicular dendritic cells regulates the B cell recall response. J Immunol 2000; 164:6268-75.
10. Gray D, Skarvall H. B-cell memory is short-lived in the absence of antigen. Nature 1988; 336:70-3.
11. Gray D, Kosco MH, Stockinger B. Novel pathways of antigen presentation for the maintenance of memory. Int Immunol 1991; 3:141-8.
12. Kosco MH, Pflugfelder E, Gray D. Follicular dendritic cell-dependent adhesion and proliferation of B cells in vitro. J Immunol 1992; 148:2331-9.
13. Suzuki K, Grigorova I, Phan TG, Kelly LM, Cyster JG. Visualizing B cell capture of cognate antigen from follicular dendritic cells. J Exp Med 2009; 206:1485-93.
14. Roozendaal R, Carroll MC. Complement receptors CD21 and CD35 in humoral immunity. Immunol Rev 2007; 219:157-66.
15. Nielsen CH, Fischer EM, Leslie RGQ. The role of complement in the acquired immune response. Immunology 2000; 100:4-12.
16. Videm V, Albrigtsen M. Soluble ICAM-1 and VCAM-1 as markers of endothelial activation. Scand J Immunol 2008; 67:523-31.
17. Kosco-Vilbois MH, Bonnefoy JY, Chvatchko Y. The physiology of murine germinal center reactions. Immunol Rev 1997; 156:127-36.
18. Kopf M, Herren S, Wiles MV, Pepys MB, Kosco-Vilbois MH. Interleukin 6 influences germinal center development and antibody production via a contribution of C3 complement component. J Exp Med 1998; 188:1895-906.
19. Hase H, Kanno Y, Kojima M, et al. BAFF/BLys can potentiate B-cell selection with the B-cel coreceptor complex. Blood 2004; 103:2257-65.
20. Suzuki K, Maruya M, Kawamoto S, Sitnik K, Kitamura H, Agace WW, Fagarasan S. The sensing of environmental stimuli by follicular dendritic cells promotes immunoglobulin A generation in the gut. Immunity 2010; 33:71-83.
21. Kranich J, Krautler NJ, Heinen E, et al. Follicular dendritic cells control engulfment of apoptotic bodies by secreting Mfge8. J Exp Med 2008; 205:1293-302.
22. Ho J, Moir S, Kulik L, et al. Role for CD21 in the establishment of an extracellular HIV reservoir in lymphoid tissues. J Immunol 2007; 178:6968-74.
23. Manson JC, Clarke AR, Hooper ML, 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; 8:121-7.
24. Brown KL, Stewart K, Ritchie DL, Mabbott NA, Williams A, Fraser H, Morrison WI, Bruce ME. Scrapie replication in lymphoid tissues depends on prion protein-expressing follicular dendritic cells. Nat Med 1999; 5:1308-12.
25. C) expression alone is sufficient to sustain prion infection in the spleen. PLoS Pathog 2011; 7:e1002402.
26. Caughey B, Race RE, Chesebro B. Detection of prion protein mRNA in normal and scrapie-infected tissues and cell lines. J Gen Virol 1988; 69:711-6.
27. Kretzschmar HA, Prusiner SB, Stowring LE, deArmond SJ. Scrapie prion proteins are synthesised in neurones. Am J Pathol 1986; 122:1-5.
28. Brown HR, Goller NL, Rudelli RD, Mertz GS, Wolfe GC, Wisniewski HM, Robakis NK. The mRNA encoding the scrapie agent protein is present in a variety of non-neuronal cells. Acta Neuropathol 1990; 80:1-6.
29. Ford MJ, Burton LJ, Morris RJ, Hall SM. Selective expression of prion protein in peripheral tissues of the adult mouse. Neuroscience 2002; 113:177-92.
30. Prusiner SB, Groth D, Serban A, et al. Ablation of the prion protein (PrP) gene in mice prevents scrapie and facilitates production of anti-PrP antibodies. Proc Natl Acad Sci USA 1993; 90:10608-12.
31. c. Br Med Bull 2003; 66:61-70.
32. Prusiner SB, Scott MR, DeArmond SJ, Cohen FE. Prion protein biology. Cell 1998; 93:337-48.
33. Tobler I, Gaus SE, Deboer T, et al. Altered circadian activity rhythms and sleep in mice devoid of prion protein. Nature 1996; 380:639-42.
34. Collinge J, Whittington MA, Sidle KCL, Smith CJ, Palmer MS, Clarke AR, Jefferys JGR. Prion protein is necessary for normal synaptic function. Nature 1994; 370:295-7.
35. Nico PBC, de-Paris F, Vinade ER, et al. Altered behavioural response to acute stress in mice lacking cellular prion protein. Behav Brain Res 2005; 162:173-81.
36. Coitinho AS, Roesler R, Martins VR, Brentani RR, Izquierdo I. Cellular prion protein ablation impairs behavior as a function of age. NeuroReport 2003; 14:1375-9.
37. Walz R, Amaral OB, Rockenbach IC, Roesler R, Izquierdo I, Cavalheiro EA, Martins VR, Brentani RR. Increased sensitivity to seizures in mice lacking cellular prion protein. Epilepsia 1999; 40:1679-82.
38. Mouillet-Richard S, Ermonval M, Chebassier C, Laplanche JL, Lehmann S, Launay JM, Kellermann O. Signal transduction through prion protein. Science 2000; 289:1925-8.
39. C directly interacts with proteins involved in signaling pathways. J Biol Chem 2001; 276:44604-12.
40. Paitel E, Alves da Costa C, Vilette D, Grassi J, Checler F. Overexpression of PrPc triggers caspase 3 activation: potentiation by proteasome inhibitors and blockade by anti-PrP antibodies. J Neurochem 2002; 83:1208-14.
41. Kurschner C, Morgan JI. The cellular prion protein (PrP) selectively binds to Bcl-2 in the yeast two-hybrid system. Mol Brain Res 1995; 30:165-8.
42. Bounhar Y, Zhang Y, Goodyer CG, LeBlanc A. Prion protein protects human neurons against Bax-mediated apoptosis. J Biol Chem 2001; 276:39145-9.
43. Mitteregger G, Vosko M, Krebs B, Xiang W, Kohlmannsperger V, Nolting S, Hamann GF, Kretzschmar HA. The role of the octarepeat region in neuroprotective function of the cellular prion protein. Brain Pathol 2007; 17:174-83.
44. Aude-Garcia C, Villiers C, Candéias S, Garrel C, Bertrand C, Collin V, Marche P, Jouvin-Marche E. Enhanced susceptibility of T lymphocytes to oxidative stress in the absence of the cellular prion protein. Cell Mol Life Sci 2011; 68:687-96.
45. Kraus M, Alimzhanov MB, Rajewsky N, Rajewsky K. Survival of resting mature B lymphocytes depends on BCR signaling via the Igα/β heterodimer. Cell 2004; 117:787-800.
46. Tuzi NL, Clarke AR, Bradford B, Aitchison L, Thomson V, Manson JC. Cre-loxP mediated control of PrP to study transmissible spongiform encephalopathy diseases. Genesis 2004; 40:1-6.
47. Manson JC, Clarke AR, McBride PA, McConnell I, Hope J. PrP gene dosage determines the timing but not the final intensity or distribution of lesions in scrapie pathology. Neurodegeneration 1994; 3:331-40.
48. Farquhar CF, Somerville RA, Ritchie LA. Post-mortem immunodiagnosis of scrapie and bovine spongiform encephalopathy. J Virol Methods 1989; 24:215-21.
49. Inman CF, Rees LEN, Barker E, Haverson K, Stokes CR, Bailey M. Validation of computer-assisted, pixel-based analysis of multiple-colour immunofluorescence histology. J Immunol Methods 2005; 302:156-67.
50. Liu Y-J, Xu J, de Bouteiller O, et al. Follicular dendritic cells specifically express the long CR2/CD21 isoform. J Exp Med 1997; 185:165-70.
51. Takahashi K, Kozono Y, Waldschmidt TJ, Berthiaume D, Quigg RJ, Baron A, Holers VM. Mouse complement receptors type 1 (CR1;CD35) and type 2 (CR2;CD21): expression on normal B cell subpopulations and decreased levels during the development of autoimmunity in MRL/lpr mice. J Immunol 1997; 159:1557-69.
52. Tsoukas CD, Lambris JD. Expression of CR2/EBV receptors on human thymocytes detected by monoclonal antibodies. Eur J Immunol 1988; 18:1299-302.
53. + cells in HIV-infected persons. Immunology 1992; 75:59-65.
54. Sixbey J, Lemon S, Pagano J. A second site for Epstein-Barr virus shedding: the uterine cervix. Lancet 1986; 328:1122-4.
55. Andrasfalvy M, Prechl J, Hardy T, Erdei A, Bajtay Z. Mucosal type mast cells express complement receptor type 2 (CD21). Immunol Lett 2002; 82:29-34.
56. Kosco-Vilbois MH. Are follicular dendritic cells really good for nothing? Nat Rev Immunol 2003; 3:764-9.
57. Oda M, Uchiyama S, Noda M, et al. Effects of antibody affinity and antigen valence on molecular forms of immune complexes. Mol Immunol 2009; 47:357-64.
58. Keşmir C, De Boer RJ. A spatial model of germinal center reactions: cellular adhesion based sorting of B cells results in efficient affinity maturation. J Theor Biol 2003; 222:9-22.
59. Vora KA, Ravetch JV, Manser T. Amplified follicular immune complex deposition in mice lacking the Fc receptor γ-chain does not alter maturation of the B cell response. J Immunol 1997; 159:2116-24.
60. Genoud N, Behrens A, Miele G, Robay D, Heppner FL, Freigang S, Aguzzi A. Disruption of Doppel prevents neurodegeneration in mice with extensive Prnp deletions. Proc Natl Acad Sci USA 2004; 101:4198-203.
61. Bueler H, Fischer M, Lang Y, et al. Normal development and behaviour of mice lacking the neuronal cell-surface PrP protein. Nature 1992; 356:577-82.
62. Ballerini C, Gourdain P, Bachy V, et al. Functional implication of cellular prion protein in antigen-driven interactions between T cells and dendritic cells. J Immunol 2006; 176:7254-62.
63. Kubosaki A, Yusa S, Nasu Y, et al. 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; 282:103-7.
64. Williamson RA, Peretz D, Smorodinsky N, et al. Circumventing tolerance to generate autologous monoclonal antibodies to the prion protein. Proc Natl Acad Sci USA 1996; 93:7279-82.
65. Khalili-Shirazi A, Quaratino S, Londei M, et al. Protein conformation significantly influences immune responses to prion protein. J Immunol 2005; 174:3256-63.
66. Petit CSV, Barreau F, Besnier L, et al. Requirement of cellular prion protein for intestinal barrier function and mislocalization in patients with inflammatory bowel disease. Gastroenterology 2012; 143:122-32.
67. Krenacs T, van Dartel M, Lindhout E, Rosendaal M. Direct cell/cell communication in the lymphoid germinal center: connexin43 gap junctions functionally couple follicular dendritic cells to each other and to B lymphocytes. Eur J Immunol 1997; 27:1489-97.
68. Stuermer CAO, Langhorst MF, Wiechers MF, Legler DF, Von Hanwehr SH, Guse AH, Plattner H. PrPc capping in T cells promotes its association with the lipid raft proteins reggie-1 and reggie-2 and leads to signal transduction. FASEB J 2004; 18:1731-3.
69. Cashman NR, Loertscher R, Nalbantoglu J, Shaw I, Kascsak RJ, Bolton DC, Bendheim PE. Cellular isoform of the scrapie agent protein participates in lymphocyte activation. Cell 1990; 61:185-92.
70. Li R, Liu D, Zanusso G, et al. The expression and potential function of cellular prion protein in human lymphocytes. Cell Immunol 2001; 207:49-58.