Accumulation profiles of PrPScin hemal nodes of naturally and experimentally scrapie-infected sheep

Springer Science and Business Media LLC - Tập 9 - Trang 1-12 - 2013
Rohana P Dassanayake1, Thomas C Truscott2, M Özgür Özyiğit3, Dongyue Zhuang2, David A Schneider2, Katherine I O’Rourke1
1Department of Veterinary Microbiology and Pathology, College of Veterinary Medicine, Washington State University, Pullman, USA
2U.S. Department of Agriculture, Animal Disease Research Unit, Agricultural Research Service, Pullman, USA
3Department of Pathology, Faculty of Veterinary Medicine, Uludağ University, Görükle, Turkey

Tóm tắt

In classical scrapie, the disease-associated abnormal isoform (PrPSc) of normal prion protein accumulates principally in the nervous system and lymphoid tissues of small ruminants. Lymph nodes traffic leukocytes via lymphatic and blood vasculatures but hemal nodes lack lymphatic vessels and thus traffic leukocytes only via the blood. Although PrPSc accumulation profiles are well-characterized in ovine lymphoid tissues, there is limited information on such profiles in hemal nodes. Therefore, the objective of this study was to compare the follicular accumulation of PrPSc within hemal nodes and lymph nodes by prion epitope mapping and western blot studies. Our studies found that PrPSc accumulation in 82% of animals’ abdominal hemal nodes when PrPSc is detected in both mesenteric and retropharyngeal lymph nodes collected from preclinical and clinical, naturally and experimentally (blood transfusion) scrapie-infected sheep representing all three major scrapie-susceptible Prnp genotypes. Abdominal hemal nodes and retropharyngeal lymph nodes were then used to analyze immune cell phenotypes and PrPSc epitope mapping by immunohistochemistry and PrPSc banding patterns by western blot. Similar patterns of PrPSc accumulation were detected within the secondary follicles of hemal nodes and retropharyngeal lymph nodes, where cellular labeling was mostly associated with macrophages and follicular dendritic cells. The pattern of PrPSc accumulation within hemal nodes and retropharyngeal lymph nodes also did not differ with respect to epitope mapping with seven mAbs (N-terminus, n = 4; globular domain, n = 2; C-terminus, n = 1) in all three Prnp genotypes. Western blot analysis of hemal node and retropharyngeal lymph node homogenates revealed identical three banding patterns of proteinase K resistant PrPSc. Despite the anatomical difference in leukocyte trafficking between lymph nodes and hemal nodes, the follicles of hemal nodes appear to process PrPSc similarly to lymph nodes.

Tài liệu tham khảo

Bolton DC, McKinley MP, Prusiner SB: Identification of a protein that purifies with the scrapie prion. Science. 1982, 218 (4579): 1309-1311. 10.1126/science.6815801. Prusiner SB: Novel proteinaceous infectious particles cause scrapie. Science. 1982, 216 (4542): 136-144. 10.1126/science.6801762. Andreoletti O, Berthon P, Marc D, Sarradin P, Grosclaude J, van Keulen L, Schelcher F, Elsen JM, Lantier F: Early accumulation of PrP(Sc) in gut-associated lymphoid and nervous tissues of susceptible sheep from a Romanov flock with natural scrapie. J Gen Virol. 2000, 81 (Pt 12): 3115-3126. van Keulen LJ, Schreuder BE, Meloen RH, Mooij-Harkes G, Vromans ME, Langeveld JP: Immunohistochemical detection of prion protein in lymphoid tissues of sheep with natural scrapie. J Clin Microbiol. 1996, 34 (5): 1228-1231. O'Rourke KI, Baszler TV, Parish SM, Knowles DP: Preclinical detection of PrPSc in nictitating membrane lymphoid tissue of sheep. Vet Rec. 1998, 142 (18): 489-491. 10.1136/vr.142.18.489. O'Rourke KI, Baszler TV, Besser TE, Miller JM, Cutlip RC, Wells GA, Ryder SJ, Parish SM, Hamir AN, Cockett NE: Preclinical diagnosis of scrapie by immunohistochemistry of third eyelid lymphoid tissue. J Clin Microbiol. 2000, 38 (9): 3254-3259. Schreuder BE, van Keulen LJ, Vromans ME, Langeveld JP, Smits MA: Tonsillar biopsy and PrPSc detection in the preclinical diagnosis of scrapie. Vet Rec. 1998, 142 (21): 564-568. 10.1136/vr.142.21.564. Espenes A, Press CM, Landsverk T, Tranulis MA, Aleksandersen M, Gunnes G, Benestad SL, Fuglestveit R, Ulvund MJ: Detection of PrP(Sc) in rectal biopsy and necropsy samples from sheep with experimental scrapie. J Comp Pathol. 2006, 134 (2–3): 115-125. Gonzalez L, Dagleish MP, Martin S, Dexter G, Steele P, Finlayson J, Jeffrey M: Diagnosis of preclinical scrapie in live sheep by the immunohistochemical examination of rectal biopsies. Vet Rec. 2008, 162 (13): 397-403. 10.1136/vr.162.13.397. van Keulen LJ, Vromans ME, van Zijderveld FG: Early and late pathogenesis of natural scrapie infection in sheep. APMIS. 2002, 110 (1): 23-32. 10.1034/j.1600-0463.2002.100104.x. Houston F, McCutcheon S, Goldmann W, Chong A, Foster J, Siso S, Gonzalez L, Jeffrey M, Hunter N: Prion diseases are efficiently transmitted by blood transfusion in sheep. Blood. 2008, 112 (12): 4739-4745. 10.1182/blood-2008-04-152520. McCutcheon S, Alejo Blanco AR, Houston EF, de Wolf C, Tan BC, Smith A, Groschup MH, Hunter N, Hornsey VS, MacGregor IR: All clinically-relevant blood components transmit prion disease following a single blood transfusion: a sheep model of vCJD. PLoS One. 2011, 6 (8): e23169-10.1371/journal.pone.0023169. Dassanayake RP, Schneider DA, Truscott TC, Young AJ, Zhuang D, O'Rourke KI: Classical scrapie prions in ovine blood are associated with B lymphocytes and platelet-rich plasma. BMC Vet Res. 2011, 7: 75-10.1186/1746-6148-7-75. Andreoletti O, Litaise C, Simmons H, Corbiere F, Lugan S, Costes P, Schelcher F, Vilette D, Grassi J, Lacroux C: Highly efficient prion transmission by blood transfusion. PLoS Pathog. 2012, 8 (6): e1002782-10.1371/journal.ppat.1002782. Hadlow WJ, Kennedy RC, Race RE, Eklund CM: Virologic and neurohistologic findings in dairy goats affected with natural scrapie. Vet Pathol. 1980, 17 (2): 187-199. Hadlow WJ, Kennedy RC, Race RE: Natural infection of Suffolk sheep with scrapie virus. J Infect Dis. 1982, 146 (5): 657-664. 10.1093/infdis/146.5.657. Race R, Jenny A, Sutton D: Scrapie infectivity and proteinase K-resistant prion protein in sheep placenta, brain, spleen, and lymph node: implications for transmission and antemortem diagnosis. J Infect Dis. 1998, 178 (4): 949-953. 10.1086/515669. Terry LA, Howells L, Hawthorn J, Edwards JC, Moore SJ, Bellworthy SJ, Simmons H, Lizano S, Estey L, Leathers V: Detection of PrPsc in blood from sheep infected with the scrapie and bovine spongiform encephalopathy agents. J Virol. 2009, 83 (23): 12552-12558. 10.1128/JVI.00311-09. Edwards JC, Moore SJ, Hawthorn JA, Neale MH, Terry LA: PrP(Sc) is associated with B cells in the blood of scrapie-infected sheep. Virology. 2010, 405 (1): 110-119. 10.1016/j.virol.2010.05.023. Thorne L, Terry LA: In vitro amplification of PrPSc derived from the brain and blood of sheep infected with scrapie. J Gen Virol. 2008, 89 (Pt 12): 3177-3184. Lacroux C, Vilette D, Fernandez-Borges N, Litaise C, Lugan S, Morel N, Corbiere F, Simon S, Simmons H, Costes P: Prionemia and leukocyte-platelet-associated infectivity in sheep transmissible spongiform encephalopathy models. J Virol. 2012, 86 (4): 2056-2066. 10.1128/JVI.06532-11. Casteleyn CR, Breugelmans S, Simoens P, Van den Broeck W: Morphological and immunological characteristics of the bovine temporal lymph node and hemal node. Vet Immunol Immunopathol. 2008, 126 (3–4): 339-350. Turner DR: The reticulo-endothelial components of the haemal node. A light and electron microscopic study. J Anat. 1971, 108 (Pt 1): 13-22. Ceccarelli P, Gargiulo AM, Fagioli O, Pedini V: Cytochemical identification of lymphocytes and other mononuclear cells in ovine and bovine hemal nodes. Comp Immunol Microbiol Infect Dis. 1986, 9 (4): 297-302. 10.1016/0147-9571(86)90042-1. McGovern G, Jeffrey M: Scrapie-specific pathology of sheep lymphoid tissues. PLoS One. 2007, 2 (12): e1304-10.1371/journal.pone.0001304. Jeffrey M, Martin S, Gonzalez L: Cell-associated variants of disease-specific prion protein immunolabelling are found in different sources of sheep transmissible spongiform encephalopathy. J Gen Virol. 2003, 84 (Pt 4): 1033-1045. Andreoletti O, Berthon P, Levavasseur E, Marc D, Lantier F, Monks E, Elsen JM, Schelcher F: Phenotyping of protein-prion (PrPsc)-accumulating cells in lymphoid and neural tissues of naturally scrapie-affected sheep by double-labeling immunohistochemistry. J Histochem Cytochem. 2002, 50 (10): 1357-1370. 10.1177/002215540205001009. Mok SW, Proia RL, Brinkmann V, Mabbott NA: B cell-specific S1PR1 deficiency blocks prion dissemination between secondary lymphoid organs. J Immunol. 2012, 188 (10): 5032-5040. 10.4049/jimmunol.1200349. Zhang W, Nasu T, Hosaka YZ, Yasuda M: Comparative studies on the distribution and population of immunocompetent cells in bovine hemal node, lymph node and spleen. J Vet Med Sci. 2012, 74 (4): 405-411. 10.1292/jvms.11-0405. Young AJ, Dudler L, Yamaguchi K, Marston W, Hein WR: Structure and expression of ovine complement receptor type 2. Vet Immunol Immunopathol. 1999, 72 (1–2): 67-72. Young AJ, Marston WL, Dudler L: Subset-specific regulation of the lymphatic exit of recirculating lymphocytes in vivo. J Immunol. 2000, 165 (6): 3168-3174. Houston F, Foster JD, Chong A, Hunter N, Bostock CJ: Transmission of BSE by blood transfusion in sheep. Lancet. 2000, 356 (9234): 999-1000. 10.1016/S0140-6736(00)02719-7. Hunter N, Foster J, Chong A, McCutcheon S, Parnham D, Eaton S, MacKenzie C, Houston F: Transmission of prion diseases by blood transfusion. J Gen Virol. 2002, 83 (Pt 11): 2897-2905. Bannach O, Birkmann E, Reinartz E, Jaeger KE, Langeveld JP, Rohwer RG, Gregori L, Terry LA, Willbold D, Riesner D: Detection of prion protein particles in blood plasma of scrapie infected sheep. PLoS One. 2012, 7 (5): e36620-10.1371/journal.pone.0036620. Huang H, Rendulich J, Stevenson D, O'Rourke K, Balachandran A: Evaluation of Western blotting methods using samples with or without sodium phosphotungstic acid precipitation for diagnosis of scrapie and chronic wasting disease. Can J Vet Res. 2005, 69 (3): 193-199. Baylis M, Goldmann W, Houston F, Cairns D, Chong A, Ross A, Smith A, Hunter N, McLean AR: Scrapie epidemic in a fully PrP-genotyped sheep flock. J Gen Virol. 2002, 83 (Pt 11): 2907-2914. O'Rourke KI, Schneider DA, Spraker TR, Dassanayake RP, Highland MA, Zhuang D, Truscott TC: Transmissibility of caprine scrapie in ovine transgenic mice. BMC Vet Res. 2012, 8: 42-10.1186/1746-6148-8-42.