Unusual cerebral vascular prion protein amyloid distribution in scrapie-infected transgenic mice expressing anchorless prion protein

Acta Neuropathologica Communications

Volumn 2, Issue 1, 2014, Pages

  Rangel, Alejandra ^a   Race, Brent ^a   Klingeborn, Mikael ^b   Striebel, James ^a   Chesebro, Bruce ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Basement membrane; Brain interstitial fluid; Cerebral amyloid angiopathy; Glycophosphatidylinositol anchor; Prion

Indexed keywords

EID: 85005877093     PISSN: None     EISSN: 20515960     Source Type: Journal    
DOI: 10.1186/2051-5960-1-25     Document Type: Article

References (43)

1. Aguzzi A, Polymenidou M: Mammalian prion biology: one century of evolving concepts. Cell 2004,116(2):313-327. 10.1016/S0092-8674(03)01031-6
2. Caughey B, Baron GS, Chesebro B, Jeffrey M: Getting a grip on prions: oligomers, amyloids, and pathological membrane interactions. Annu Rev Biochem 2009, 78: 177-204. 10.1146/annurev.biochem.78.082907.145410
3. Budka H, Aguzzi A, Brown P, Brucher JM, Bugiani O, Gullotta F, Haltia M, Hauw JJ, Ironside JW, Jellinger K, et al.: Neuropathological diagnostic criteria for Creutzfeldt-Jakob disease (CJD) and other human spongiform encephalopathies (prion diseases). Brain Pathol 1995,5(4):459-466. 10.1111/j.1750-3639.1995.tb00625.x
4. Gonzalez L, Martin S, Begara-McGorum I, Hunter N, Houston F, Simmons M, Jeffrey M: Effects of agent strain and host genotype on PrP accumulation in the brain of sheep naturally and experimentally affected with scrapie. J Comp Pathol 2002,126(1):17-29. 10.1053/jcpa.2001.0516
5. Jeffrey M, Goodsir CM, Bruce ME, McBride PA, Fraser JR: In vivo toxicity of prion protein in murine scrapie: ultrastructural and immunogold studies. Neuropathol Appl Neurobiol 1997,23(2):93-101. 10.1111/j.1365-2990.1997.tb01191.x
6. Parchi P, Giese A, Capellari S, Brown P, Schulz-Schaeffer W, Windl O, Zerr I, Budka H, Kopp N, Piccardo P, Poser S, Rojiani A, Streichemberger N, Julien J, Vital C, Ghetti B, Gambetti P, Kretzschmar H: Classification of sporadic Creutzfeldt-Jakob disease based on molecular and phenotypic analysis of 300 subjects. Ann Neurol 1999,46(2):224-233. 10.1002/1531-8249(199908)46:2<224::AID-ANA12>3.0.CO;2-W
7. Ghetti B, Piccardo P, Frangione B, Bugiani O, Giaccone G, Young K, Prelli F, Farlow MR, Dlouhy SR, Tagliavini F: Prion protein amyloidosis. Brain Pathol 1996,6(2):127-145. 10.1111/j.1750-3639.1996.tb00796.x
8. Jeffrey M, Goodsir CM, Bruce ME, McBride PA, Scott JR, Halliday WG: Infection specific prion protein (PrP) accumulates on neuronal plasmalemma in scrapie infected mice. Neurosci Lett 1992,147(1):106-109. 10.1016/0304-3940(92)90785-6
9. Piccardo P, Seiler C, Dlouhy SR, Young K, Farlow MR, Prelli F, Frangione B, Bugiani O, Tagliavini F, Ghetti B: Proteinase-K-resistant prion protein isoforms in Gerstmann-Straussler-Scheinker disease (Indiana kindred). J Neuropathol Exp Neurol 1996,55(11):1157-1163. 10.1097/00005072-199611000-00007
10. Chesebro B, Race B, Meade-White K, Lacasse R, Race R, Klingeborn M, Striebel J, Dorward D, McGovern G, Jeffrey M: Fatal transmissible amyloid encephalopathy: a new type of prion disease associated with lack of prion protein membrane anchoring. PLoS Pathog 2010,6(3):e1000800. 10.1371/journal.ppat.1000800
11. Race B, Meade-White K, Oldstone MB, Race R, Chesebro B: Detection of prion infectivity in fat tissues of scrapie-infected mice. PLoS Pathog 2008,4(12):e1000232. 10.1371/journal.ppat.1000232
12. Trifilo MJ, Yajima T, Gu Y, Dalton N, Peterson KL, Race RE, Meade-White K, Portis JL, Masliah E, Knowlton KU, Chesebro B, Oldstone MB: Prion-induced amyloid heart disease with high blood infectivity in transgenic mice. Science 2006,313(5783):94-97. 10.1126/science.1128635
13. Revesz T, Holton JL, Lashley T, Plant G, Frangione B, Rostagno A, Ghiso J: Genetics and molecular pathogenesis of sporadic and hereditary cerebral amyloid angiopathies. Acta Neuropathol 2009,118(1):115-130. 10.1007/s00401-009-0501-8
14. Ghetti B, Piccardo P, Spillantini MG, Ichimiya Y, Porro M, Perini F, Kitamoto T, Tateishi J, Seiler C, Frangione B, Bugiani O, Giaccone G, Prelli F, Goedert M, Dlouhy SR, Tagliavini F: Vascular variant of prion protein cerebral amyloidosis with tau-positive neurofibrillary tangles: the phenotype of the stop codon 145 mutation in PRNP. Proc Natl Acad Sci USA 1996,93(2):744-748. 10.1073/pnas.93.2.744
15. Jansen C, Parchi P, Capellari S, Vermeij AJ, Corrado P, Baas F, Strammiello R, van Gool WA, van Swieten JC, Rozemuller AJ: Prion protein amyloidosis with divergent phenotype associated with two novel nonsense mutations in PRNP. Acta Neuropathol 2010,119(2):189-197. 10.1007/s00401-009-0609-x
16. Jayadev S, Nochlin D, Poorkaj P, Steinbart EJ, Mastrianni JA, Montine TJ, Ghetti B, Schellenberg GD, Bird TD, Leverenz JB: Familial prion disease with Alzheimer disease-like tau pathology and clinical phenotype. Ann Neurol 2011,69(4):712-720. 10.1002/ana.22264
17. Mandybur TI: The incidence of cerebral amyloid angiopathy in Alzheimer's disease. Neurology 1975,25(2):120-126. 10.1212/WNL.25.2.120
18. Morimatsu M, Hirai S, Muramatsu A, Yoshikawa M: Senile degenerative brain lesions and dementia. J Am Geriatr Soc 1975,23(9):390-406.
19. Thal DR, Ghebremedhin E, Rub U, Yamaguchi H, Del Tredici K, Braak H: Two types of sporadic cerebral amyloid angiopathy. J Neuropathol Exp Neurol 2002,61(3):282-293.
20. Yamaguchi H, Yamazaki T, Lemere CA, Frosch MP, Selkoe DJ: Beta amyloid is focally deposited within the outer basement membrane in the amyloid angiopathy of Alzheimer's disease. An immunoelectron microscopic study. Am J Pathol 1992,141(1):249-259.
21. Weller RO, Massey A, Newman TA, Hutchings M, Kuo YM, Roher AE: Cerebral amyloid angiopathy: amyloid beta accumulates in putative interstitial fluid drainage pathways in Alzheimer's disease. Am J Pathol 1998,153(3):725-733. 10.1016/S0002-9440(10)65616-7
22. Carare RO, Bernardes-Silva M, Newman TA, Page AM, Nicoll JA, Perry VH, Weller RO: Solutes, but not cells, drain from the brain parenchyma along basement membranes of capillaries and arteries: significance for cerebral amyloid angiopathy and neuroimmunology. Neuropathol Appl Neurobiol 2008,34(2):131-144. 10.1111/j.1365-2990.2007.00926.x
23. Weller RO, Djuanda E, Yow HY, Carare RO: Lymphatic drainage of the brain and the pathophysiology of neurological disease. Acta Neuropathol 2009,117(1):1-14. 10.1007/s00401-008-0457-0
24. Weller RO, Boche D, Nicoll JA: Microvasculature changes and cerebral amyloid angiopathy in Alzheimer's disease and their potential impact on therapy. Acta Neuropathol 2009,118(1):87-102. 10.1007/s00401-009-0498-z
25. Chesebro B, Trifilo M, Race R, Meade-White K, Teng C, LaCasse R, Raymond L, Favara C, Baron G, Priola S, Caughey B, Masliah E, Oldstone M: Anchorless prion protein results in infectious amyloid disease without clinical scrapie. Science 2005,308(5727):1435-1439. 10.1126/science.1110837
26. Klingeborn M, Race B, Meade-White KD, Rosenke R, Striebel JF, Chesebro B: Crucial role for prion protein membrane anchoring in the neuroinvasion and neural spread of prion infection. J Virol 2011,85(4):1484-1494. 10.1128/JVI.02167-10
27. Rangel A, Race B, Striebel J, Chesebro B: Non-amyloid and amyloid prion protein deposits in prion-infected mice differ in blockage of interstitial brain fluid. Neuropathol Appl Neurobiol 2013,39(3):217-230. 10.1111/j.1365-2990.2012.01303.x
28. Tribouillard-Tanvier D, Race B, Striebel JF, Carroll JA, Phillips K, Chesebro B: Early cytokine elevation, PrPres deposition, and gliosis in mouse scrapie: no effect on disease by deletion of cytokine genes IL-12p40 and IL-12p35. J Virol 2012,86(19):10377-10383. 10.1128/JVI.01340-12
29. Matsunaga Y, Peretz D, Williamson A, Burton D, Mehlhorn I, Groth D, Cohen FE, Prusiner SB, Baldwin MA: Cryptic epitopes in N-terminally truncated prion protein are exposed in the full-length molecule: dependence of conformation on pH. Proteins 2001,44(2):110-118. 10.1002/prot.1077
30. Hawkes CA, Hartig W, Kacza J, Schliebs R, Weller RO, Nicoll JA, Carare RO: Perivascular drainage of solutes is impaired in the ageing mouse brain and in the presence of cerebral amyloid angiopathy. Acta Neuropathol 2011,121(4):431-443. 10.1007/s00401-011-0801-7
31. Misumi Y, Ando Y, Ueda M, Obayashi K, Jono H, Su Y, Yamashita T, Uchino M: Chain reaction of amyloid fibril formation with induction of basement membrane in familial amyloidotic polyneuropathy. J Pathol 2009,219(4):481-490. 10.1002/path.2618
32. Caughey B, Brown K, Raymond GJ, Katzenstein GE, Thresher W: Binding of the protease-sensitive form of PrP (prion protein) to sulfated glycosaminoglycan and congo red [corrected]. J Virol 1994,68(4):2135-2141.
33. Wong C, Xiong LW, Horiuchi M, Raymond L, Wehrly K, Chesebro B, Caughey B: Sulfated glycans and elevated temperature stimulate PrP(Sc)-dependent cell-free formation of protease-resistant prion protein. EMBO J 2001,20(3):377-386. 10.1093/emboj/20.3.377
34. Silveira JR, Raymond GJ, Hughson AG, Race RE, Sim VL, Hayes SF, Caughey B: The most infectious prion protein particles. Nature 2005,437(7056):257-261. 10.1038/nature03989
35. Mandybur TI: Cerebral amyloid angiopathy: the vascular pathology and complications. J Neuropathol Exp Neurol 1986,45(1):79-90. 10.1097/00005072-198601000-00007
36. Vinters HV, Gilbert JJ: Cerebral amyloid angiopathy: incidence and complications in the aging brain. II. The distribution of amyloid vascular changes. Stroke 1983,14(6):924-928. 10.1161/01.STR.14.6.924
37. Weller RO: Pathology of cerebrospinal fluid and interstitial fluid of the CNS: significance for Alzheimer disease, prion disorders and multiple sclerosis. J Neuropathol Exp Neurol 1998,57(10):885-894. 10.1097/00005072-199810000-00001
38. Weller RO, Subash M, Preston SD, Mazanti I, Carare RO: Perivascular drainage of amyloid-beta peptides from the brain and its failure in cerebral amyloid angiopathy and Alzheimer's disease. Brain Pathol 2008,18(2):253-266.
39. Eurelings LS, Richard E, Carrano A, Eikelenboom P, van Gool WA, Rozemuller AJ: Dyshoric capillary cerebral amyloid angiopathy mimicking Creutzfeldt-Jakob disease. J Neurol Sci 2010,295(1-2):131-134.
40. Richard E, Carrano A, Hoozemans JJ, van Horssen J, van Haastert ES, Eurelings LS, de Vries HE, Thal DR, Eikelenboom P, van Gool WA, Rozemuller AJ: Characteristics of dyshoric capillary cerebral amyloid angiopathy. J Neuropathol Exp Neurol 2010,69(11):1158-1167. 10.1097/NEN.0b013e3181fab558
41. Abbott NJ: Evidence for bulk flow of brain interstitial fluid: significance for physiology and pathology. Neurochem Int 2004,45(4):545-552. 10.1016/j.neuint.2003.11.006
42. Cserr HF, Patlak CS: Secretion and Bulk Flow of Interstital Fluid. In Physiology and Pharmacology of the Blood-brain Barrier. Edited by: Bradbury MWB. Berlin: Springer; 1992:245-261.
43. Schley D, Carare-Nnadi R, Please CP, Perry VH, Weller RO: Mechanisms to explain the reverse perivascular transport of solutes out of the brain. J Theor Biol 2006,238(4):962-974. 10.1016/j.jtbi.2005.07.005