Volume 35 Issue 5
Sep.  2014
Turn off MathJax
Article Contents

Li-Li QING, Hui ZHAO, Lin-Lin LIU. Progress on low susceptibility mechanisms of transmissible spongiform encephalopathies. Zoological Research, 2014, 35(5): 436-445. doi: 10.13918/j.issn.2095-8137.2014.5.436
Citation: Li-Li QING, Hui ZHAO, Lin-Lin LIU. Progress on low susceptibility mechanisms of transmissible spongiform encephalopathies. Zoological Research, 2014, 35(5): 436-445. doi: 10.13918/j.issn.2095-8137.2014.5.436

Progress on low susceptibility mechanisms of transmissible spongiform encephalopathies

doi: 10.13918/j.issn.2095-8137.2014.5.436
Funds:  This item was supported by the National Natural Science Foundation of China (31060302 and 31260032), the Transgene Special Project of the Ministry of Agriculture of China (2011ZX08009-003-006) and the Natural Science Foundation of Yunnan Province (2010CD010).
More Information
  • Corresponding author: Hui ZHAO
  • Received Date: 2014-05-04
  • Rev Recd Date: 2014-06-20
  • Publish Date: 2014-09-08
  • Transmissible spongiform encephalopathies (TSEs), also known as prion diseases, are a group of fatal neurodegenerative diseases detected in a wide range of mammalian species. The "protein-only" hypothesis of TSE suggests that prions are transmissible particles devoid of nucleic acid and the primary pathogenic event is thought to be the conversion of cellular prion protein (PrPC) into the disease-associated isoform (PrPSc). According to susceptibility to TSEs, animals can be classified into susceptible species and low susceptibility species. In this review we focus on several species with low susceptibility to TSEs: dogs, rabbits, horses and buffaloes. We summarize recent studies into the characteristics of low susceptibility regarding protein structure, and biochemical and genetic properties.
  • 加载中
  • [1]
    Aguzzi A, Sigurdson C, Heikenwaelder M. 2008. Molecular mechanisms of prion pathogenesis. Annual Review of Pathology: Mechanisms Of Disease, 3(1): 11-40.
    [2]
    Aldhous P. 1990. BSE: Spongiform encephalopathy found in cat. Nature, 345(6272): 194.
    [3]
    Barlow RM, Rennie JC. 1976.The fate of ME7 scrapie infection in rats, guinea-pigs and rabbits. Research in Veterinary Science, 21(1): 110-111.
    [4]
    Barron RM, Campbell SL, King D, Bellon A, Chapman KE, Williamson RA, Manson JC. 2007. High titers of transmissible spongiform encephalopathy infectivity associated with extremely low levels of PrPSc in vivo. Journal of Biological Chemistry, 282(49): 35878-35886.
    [5]
    Beck JA, Campbell TA, Adamson G, Poulter M, Uphill JB, Molou E, Mead S. 2008. Association of a null allele of SPRN with variant Creutzfeldt-Jakob disease. Journal of Medical Genetics, 45(12): 813-817.
    [6]
    Bellotti V, Chiti F. 2008. Amyloidogenesis in its biological environment: challenging a fundamental issue in protein misfolding diseases. Current Opinion in Structural Biology, 18(6):771-779.
    [7]
    Bessen RA, Marsh RF. 1992. Identification of two biologically distinct strains of transmissible mink encephalopathy in hamsters. Journal of General Virology, 73(2): 329-334.
    [8]
    Brandner S, Raeber A, Sailer A, Blättler T, Fischer M, Weissmann C, Aguzzi A. 1996. Normal host prion protein (PrPC) is required for scrapie spread within the central nervous system. Proceedings of the National Academy of Sciences of the United States of America, 93(23): 13148-13151.
    [9]
    Büeler H, Aguzzi A, Sailer A, Greiner, RA, Autenried P, Aguet M, Weissmann C. 1993. Mice devoid of PrP are resistant to scrapie. Cell, 73(7): 1339-1347.
    [10]
    Caughey B, Baron GS, Chesebro B, Jeffrey M. 2009. Getting a grip on prions: oligomers, amyloids and pathological membrane interactions. Annual Review of Biochemistry, 78(1): 177-204.
    [11]
    Chandler RL.1961. Encephalopathy in mice produced by inoculation with scrapie brain material. The Lancet, 277(7191): 1378-1379.
    [12]
    Chianini F, Fernández-Borges N, Vidal E, Gibbard L, Pintado B, Castro JD, Priola SA, Hamilton S, Eaton SL, Finlayson J, Pang Y, Steele P, Reid HW, Dagleish MP, Castilla J. 2012. Rabbits are not resistant to prion infection. Proceedings of the National Academy of Sciences of the United States of America, 109(13): 5080-5085.
    [13]
    Collinge J, Clarke AR. 2007. A general model of prion strains and their pathogenicity. Science, 318(5852): 930-936.
    [14]
    Collinge J, Sidle KCL, Meads J, Ironside J, Hill AF. 1996. Molecular analysis of prion strain variation and the aetiology of‘new variant’ CJD. Nature, 383(6602): 685-690.
    [15]
    Collins SJ, Lawson VA, Masters CL. 2004. Transmissible spongiform encephalopathies. The Lancet, 363(9402): 51-62.
    [16]
    Courageot MP, Daude N, Nonno R, Paquet S, Di Bari MA, Le Dur A, Chapuis J, Hill AF, Agrimi U, Laude H, Vilette D. 2008. A cell line infectible by prion strains from different species. Journal of General Virology, 89(1): 341-347.
    [17]
    Daude N, Westaway D. 2011. Biological properties of the PrP-like Shadoo protein. Frontiers in Bioscience, 16: 1505-1516.
    [18]
    Fernández-Borges N, Chianini F, Eraña H, Vidal E, Eaton SL, Pintado B, Finlayson J, Dagleish MP, Castilla J. 2012. Naturally prion resistant mammals: A utopia? Prion, 6(5): 425-429.
    [19]
    Fernandez-Funez P, Zhang Y, Casas-Tinto S, Xiao X, Zou WQ, Rincon-Limas DE. 2010. Sequence-dependent prion protein misfolding and neurotoxicity. Journal of Biological Chemistry, 285(47): 36897-36908.
    [20]
    Fernandez-Funez P, Zhang Y, Sanchez-Garcia J, Jensen K, Zou WQ, Rincon-Limas DE. 2011. Pulling rabbits to reveal the secrets of the prion protein. Communicative & Integrative Biology, 4(3): 262-266.
    [21]
    Gibbs CJ, Gajdusek DC. 1973. Experimental subacute spongiform virus encephalopathies in primates and other laboratory animals. Science, 182(4107): 67-68.
    [22]
    Haase B, Doherr MG, Seuberlich T, Drögemüller C, Dolf G, Nicken P, Schiebel K, Ziegler U, Groschup MH, Zurbriggen A, Leeb T. 2007. PRNP promoter polymorphisms are associated with BSE susceptibility in Swiss and German cattle. BMC Genet, 8(1): 15.
    [23]
    Harman JL, Silva CJ. 2009. Bovine spongiform encephalopathy. Journal of the American Veterinary Medical Association, 234(1): 59-72.
    [24]
    Hill AF, Desbruslais M, Joiner S, Sidle KC, Gowland I, Collinge J, Doey LJ, Lantos P. 1997. The same prion strain causes vCJD and BSE. Nature, 389(6650): 448-450.
    [25]
    Hill AF, Joiner S, Linehan J, Desbruslais M, Lantos PL, Collinge J. 2000. Species-barrier-independent prion replication in apparently resistant species. Proceedings of the National Academy of Sciences of the United States of America, 97(18): 10248-10253.
    [26]
    Hornemann S, Glockshuber R. 1998. A scrapie-like unfolding intermediate of the prion protein domain PrP (121-231) induced by acidic pH. Proceedings of the National Academy of Sciences of the United States of America, 95(11): 6010-6014.
    [27]
    Imran M, Mahmood S, Babar ME, Hussain R, Yousaf MZ, Abid NB, Lone KP. 2012. PRNP gene variation in Pakistani cattle and buffaloes. Gene, 505(1): 180-185.
    [28]
    Imran M, Mahmood S. 2011. An overview of animal prion diseases. Virology Journal, 8(1): 493.
    [29]
    Juling K, Schwarzenbacher H, Williams JL, Fries R. 2006. A major genetic component of BSE susceptibility. BMC Biology, 4(1): 33.
    [30]
    Kaneko K, Zulianello L, Scott M, Cooper CM, Wallace AC, James TL, Cohen FE, Prusiner SB. 1997. Evidence for protein X binding to a discontinuous epitope on the cellular prion protein during scrapie prion propagation. Proceedings of the National Academy of Sciences of the United States of America, 94(19): 10069-10074.
    [31]
    Khan MQ, Sweeting B, Mulligan VK, Arslan PE, Cashman NR, Pai EF, Chakrabartty A. 2010. Prion disease susceptibility is affected by β-structure folding propensity and local side-chain interactions in PrP. Proceedings of the National Academy of Sciences of the United States of America, 107(46): 19808-19813.
    [32]
    Kimberlin RH, Walker CA. 1977. Characteristics of a short incubation model of scrapie in the golden hamster. Journal of General Virology, 34(2): 295-304.
    [33]
    Kirkwood JK, Cunningham AA. 1994. Epidemiological observations on spongiform encephalopathies in captive wild animals in the British Isles. Veterinary Record, 135(13): 296-303.
    [34]
    Lasmézas CI, Deslys JP, Robain O, Jaegly A, Beringue V, Peyrin JM, Fournier JG, Hauw JJ, Rossier J, Dormont D. 1997. Transmission of the BSE agent to mice in the absence of detectable abnormal prion protein. Science, 275(5298): 402-404.
    [35]
    Lin DH, Wen W. 2011. Progresses on prion proteins. Scientia China: Chimica, 41(4): 683-698.
    [36]
    Lloyd S, Mead S, Collinge J. 2011. Genetics of prion disease. Topics in Current Chemistr, 305: 1-22.
    [37]
    Lysek DA, Schorn C, Nivon LG, Esteve-Moya V, Christen B, Calzolai L, Schroetter CV, Fiorito F, Herrmann T, Guntert P, Wüthrich K. 2005. Prion protein NMR structures of cats, dogs, pigs, and sheep. Proceedings of the National Academy of Sciences of the United States of America, 102(3): 640-645.
    [38]
    Manson JC, Clarke AR, McBride PA, McConnell I, Hope J. 1994. PrP gene dosage determines the timing but not the final intensity or distribution of lesions in scrapie pathology. Neurodegeneration, 3(4): 331-340.
    [39]
    McKinley MP, Bolton DC, Prusiner SB. 1983. A protease-resistant protein is a structural component of the scrapie prion. Cell, 35(1): 57-62.
    [40]
    Msalya G, Shimogiri T, Ohno S, Okamoto S, Kawabe K, Minezawa M, Maeda Y. 2011. Evaluation of PRNP expression based on genotypes and alleles of two indel loci in the medulla oblongata of Japanese Black and Japanese Brown cattle. PLoS One, 6(5): e18787.
    [41]
    Nicholson EM, Brunelle BW, Richt JA, Kehrli Jr ME, Greenlee, JJ. 2008. Identification of a heritable polymorphism in bovine PRNP associated with genetic transmissible spongiform encephalopathy: evidence of heritable BSE. PLoS One, 3(8): e2912.
    [42]
    Nisbet RM, Harrison CF, Lawson VA, Masters CL, Cappai R, Hill AF. 2010. Residues surrounding the glycosylphosphatidylinositol anchor attachment site of PrP modulate prion infection: insight from the resistance of rabbits to prion disease. Journal of Virology, 84(13): 6678-6686.
    [43]
    Novakofski J, Brewer MS, Mateus-Pinilla N, Killefer J, McCusker RH. 2005. Prion biology relevant to bovine spongiform encephalopathy. Journal of Animal Science, 83(6):1455-1476.
    [44]
    Oztabak K, Ozkan E, Soysal I, Paya I, ün C. 2009. Detection of prion gene promoter and intron1 indel polymorphisms in Anatolian water buffalo (Bubalus bubalis). Journal of Animal Breeding and Genetics, 126(6): 463-467.
    [45]
    Pan KM, Baldwin M, Nguyen J, Gasset M, Serban A, Groth D, Mehlhorm I, Huang Z, Fletterick RJ, Cohen FE. 1993. Conversion of alpha-helices into beta-sheets features in the formation of the scrapie prion proteins. Proceedings of the National Academy of Sciences of the United States of America, 90(23): 10962-10966.
    [46]
    Pérez DR, Damberger FF, Wüthrich K. 2010. Horse prion protein NMR structure and comparisons with related variants of the mouse prion protein. Journal of Molecular Biology, 400(2): 121-128.
    [47]
    Polymenidou M, Trusheim H, Stallmach L, Moos R, Julius C, Miele G, Lenz-Bauer C, Aguzzi A. 2008. Canine MDCK cell lines are refractory to infection with human and mouse prions. Vaccine, 26(21): 2601-2614.
    [48]
    Premzl M, Sangiorgio L, Strumbo B, Marshall Graves JA, Simonic T, Gready JE. 2003. Shadoo, a new protein highly conserved from fish to mammals and with similarity to prion protein. Gene, 314: 89-102.
    [49]
    Prusiner SB. 1982. Novel proteinaceous infectious particles cause scrapie. Science, 216(4542): 136-144.
    [50]
    Prusiner SB. 1998. Nobel lecture: Prions. Proceedings of the National Academy of Sciences of the United States of America, 95(23): 13363-13383.
    [51]
    Sander P, Hamann H, Drögemüller C, Kashkevich K, Schiebel K, Leeb T. 2005. Bovine Prion protein gene (PRNP) promoter polymorphisms modulate PRNP expression and may be responsible for differences in bovine spongiform encephalopathy susceptibility. Journal of Biology Chemistry, 280(45): 37408-37414.
    [52]
    Sander P, Hamann H, Pfeiffer I, Wemheuer W, Brenig B, Groschup MH, Ziegler U, Distl O, Leeb T. 2004. Analysis of sequence variability of the bovine prion protein gene (PRNP) in German cattle breeds. Neurogenetics, 5(1): 19-25.
    [53]
    Seuberlich T, Botteron C, Wenker C, Café-Marçal V, Oevermann A, Haase B, Leeb T, Heim D, Zurbriggen A. 2006. Spongiform encephalopathy in a miniature zebu. Emerging Infectious Diseases, 12(12): 1950-1953.
    [54]
    Sigurdson CJ, Joshi-Barr S, Bett C, Winson O, Manco G, Schwarz P, Rulicke T, Nilsson KPR, Margalith I, Raeber A, Peretz D, Hornemann S, Wuthrich K, Aguzzi A. 2011. Spongiform encephalopathy in transgenic mice expressing a point mutation in the β2-α2 loop of the prion protein. Journal of Neuroscience, 31(39): 13840-13847.
    [55]
    Stewart P, Campbell L, Skogtvedt S, Griffin KA, Arnemo JM, Tryland M, Girling S, Miller MW, Tranulis MA, Goldmann W. 2012. Genetic predictions of prion disease susceptibility in carnivore species based on variability of the prion gene coding region. PloS One, 7(12): e50623.
    [56]
    Thomzig A, Cardone F, Krüger D, Pocchiari M, Brown P, Beekes M. 2006. Pathological prion protein in muscles of hamsters and mice infected with rodent-adapted BSE or vCJD. Journal of Neuroscience, 87(1): 251-254.
    [57]
    Uchida L, Heriyanto A, Thongchai C, Hanh TT, Horiuchi M, Ishihara K, Tamura Y, Muramatsu Y. 2014. Genetic diversity in the prion protein gene (PRNP) of domestic cattle and water buffaloes in Vietnam, Indonesia and Thailand. Journal of Veterinary Medical Science, in press.
    [58]
    Vidal E, Fernández-Borges N, Pintado B, Ordóñez M., Márquez M, Fondevila D, Torres JM, Pumarola M, Castilla J. 2013. Bovine spongiform encephalopathy induces misfolding of alleged prion-resistant species cellular prion protein without altering its pathobiological features. Journal of Neuroscience, 33(18): 7778-7786.
    [59]
    Vilette D, Andreoletti O, Archer F, Madelaine MF, Vilotte JL, Lehmann S, Laude H. 2001. Ex vivo propagation of infectious sheep scrapie agent in heterologous epithelial cells expressing ovine prion protein. Proceedings of the National Academy of Sciences of the United States of America, 98(7): 4055-4059.
    [60]
    Vorberg I, Groschup MH, Pfaff E, Priola SA. 2003. Multiple amino acid residues within the rabbit prion protein inhibit formation of its abnormal isoform. Journal of Virology, 77(3): 2003-2009.
    [61]
    Wang JY , Hao Z, Xu M, Wang X, Wu SB, Song BC, Liu WS, Li JP, Meng KY, Li ZY, Gao HW. 2010. Mapping the interaction site of prion protein and Sho. Molecular Biology Reports, 37(5): 2295-2300.
    [62]
    Wang SQ, Zhao H, Zhang YP. 2014. Advances in research on Shadoo, Shadow of prion protein. Chinese Science Bulletin, 59(9): 821-827.
    [63]
    Watts JC, Drisaldi B, Ng V, Yang J, Strome B, Horne P, Sy M, Young R, Mastrangelo P, Bergeron C, Fraser PE, Carlson GA, Mount HTJ, Schmitt-Ulms G, Westaway D. 2007. The CNS glycoprotein Shadoo has PrPC-like protective properties and displays reduced levels in prion infections. The EMBO Journal, 26(17): 4038-4050.
    [64]
    Watts JC, Stöhr J, Bhardwaj S, Wille H, Oehler A, DeArmond SJ, Giles K, Prusiner SB. 2011. Protease-resistant prions selectively decrease Shadoo protein. PLoS Pathogens, 7(11): e1002382.
    [65]
    Wells GA, Scott AC, Johnson CT, Gunning RF, Hancock RD, Jeffrey M, Dawson M, Bradley R. 1987. A novel progressive spongiform encephalopathy in cattle. Veterinary Record, 121(18): 419-420.
    [66]
    Wen Y, Li J, Yao WM, Xiong MQ, Hong J, Peng Y, Xiao GF, Lin DH. 2010a. Unique structural characteristics of the rabbit prion protein. Journal of Biological Chemistry, 285(41): 31682-31693.
    [67]
    Wen Y, Li J, Xiong M, Peng Y, Yao WM, Hong J, Lin DH. 2010b. Solution structure and dynamics of the I214V mutant of the rabbit prion protein. PLoS One, 5(10): e13273.
    [68]
    Westaway D, Genovesi S, Daude N, Brown R, Lau A, Lee I, Mays CE, Coomaraswamy J, Canine B, Pitstick R, Herbst A, Yang J, Ko KWS, Schmitt-Ulms G, Dearmond SJ, Mckenzie D, Hood L, Carlson GA. 2011. Down-regulation of Shadoo in prion infections traces a pre-clinical event inversely related to PrPSc accumulation. PLoS Pathogens, 7(11): e1002391.
    [69]
    Westaway D, Mirenda C A, Foster D, Zebarjadian Y, Scott M, Torchia M, Yang S, Serban H, Dearmond SJ, Ebeling C, Prusiner SB, Carlson GA. 1991. Paradoxical shortening of scrapie incubation times by expression of prion protein transgenes derived from long incubation period mice. Neuron, 7(1): 59-68.
    [70]
    Westaway D, Zuliani V, Cooper C M, Costa MD, Neuman S, Jenny AL, Detwiler L, Prusiner SB. 1994. Homozygosity for prion protein alleles encoding glutamine-171 renders sheep susceptible to natural scrapie. Genes and Development, 8(8): 959-969.
    [71]
    Wopfner F, Weidenhöfer G, Schneider R, Brunn AV, Gilch S, Schwarz TF, Werner T, Schätzl HM. 1999. Analysis of 27 mammalian and 9 avian PrPs reveals high conservation of flexible regions of the prion protein. Journal of Molecular Biology, 289(5): 1163-1178.
    [72]
    Yuan Z, Zhao D, Yang L. 2013. Decipher the mechanisms of rabbit's low susceptibility to prion infection. Acta Biochimica et Biophysica Sinica, 45(11): 899-903.
    [73]
    Zhang JP. 2009. Studies on the structural stability of rabbit prion probed by molecular dynamics simulations. Journal of Biomolecular Structure and Dynamics, 27(2): 159-162.
    [74]
    Zhang JP. 2010. Studies on the structural stability of rabbit prion probed by molecular dynamics simulations of its wild-type and mutants. Journal of Theoretical Biology, 264(1): 119-122.
    [75]
    Zhang JP. 2011a. The nature of the infectious agents: PrP models of resistant species to prion diseases (dog, rabbit and horses). In: Verdier JM. Prions and prion diseases: New developments. Chapter 2. New York: NOVA Science Publishers, 41-48.
    [76]
    Zhang JP, Liu DDW. 2011. Molecular dynamics studies on the structural stability of wild-type dog prion protein. Journal of Biomolecular Structure and Dynamics, 28(6): 861-869.
    [77]
    Zhang JP. 2011b. The structural stability of wild-type horse prion protein. Journal of Biomolecular Structure and Dynamics, 29(2): 369-377.
    [78]
    Zhao H, Liu LL, Du SH, Wang SQ, Zhang YP, Forloni G. 2012. Comparative analysis of the Shadoo gene between cattle and buffalo reveals significant differences. PloS One, 7(10): e46601.
    [79]
    Zhou Z, Yan X, Pan K, Chen J, Xie ZS, Xiao GF, Yang FQ, Liang Y. 2011. Fibril formation of the rabbit/human/bovine prion proteins. Biophysical Journal, 101(6): 1483-1492.
  • 加载中
通讯作者: 陈斌, bchen63@163.com
  • 1. 

    沈阳化工大学材料科学与工程学院 沈阳 110142

  1. 本站搜索
  2. 百度学术搜索
  3. 万方数据库搜索
  4. CNKI搜索

Article Metrics

Article views(598) PDF downloads(1624) Cited by()

Related
Proportional views

Progress on low susceptibility mechanisms of transmissible spongiform encephalopathies

doi: 10.13918/j.issn.2095-8137.2014.5.436
Funds:  This item was supported by the National Natural Science Foundation of China (31060302 and 31260032), the Transgene Special Project of the Ministry of Agriculture of China (2011ZX08009-003-006) and the Natural Science Foundation of Yunnan Province (2010CD010).
    Corresponding author: Hui ZHAO

Abstract: Transmissible spongiform encephalopathies (TSEs), also known as prion diseases, are a group of fatal neurodegenerative diseases detected in a wide range of mammalian species. The "protein-only" hypothesis of TSE suggests that prions are transmissible particles devoid of nucleic acid and the primary pathogenic event is thought to be the conversion of cellular prion protein (PrPC) into the disease-associated isoform (PrPSc). According to susceptibility to TSEs, animals can be classified into susceptible species and low susceptibility species. In this review we focus on several species with low susceptibility to TSEs: dogs, rabbits, horses and buffaloes. We summarize recent studies into the characteristics of low susceptibility regarding protein structure, and biochemical and genetic properties.

Li-Li QING, Hui ZHAO, Lin-Lin LIU. Progress on low susceptibility mechanisms of transmissible spongiform encephalopathies. Zoological Research, 2014, 35(5): 436-445. doi: 10.13918/j.issn.2095-8137.2014.5.436
Citation: Li-Li QING, Hui ZHAO, Lin-Lin LIU. Progress on low susceptibility mechanisms of transmissible spongiform encephalopathies. Zoological Research, 2014, 35(5): 436-445. doi: 10.13918/j.issn.2095-8137.2014.5.436
Reference (79)

Catalog

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return