Placenta
Volume 29, Issue 5 , Pages 422-428 , May 2008

Effects of Nutrition and Genotype on Prion Protein (PrPC) Gene Expression in the Fetal and Maternal Sheep Placenta

  • J.M. Evoniuk

      Affiliations

    • Department of Animal and Range Sciences, North Dakota State University, 1300 Albrecht Boulevard, Fargo, ND 58105, USA
    • ,
  • M.L. Johnson

      Affiliations

    • Department of Animal and Range Sciences, North Dakota State University, 1300 Albrecht Boulevard, Fargo, ND 58105, USA
    • ,
  • P.P. Borowicz

      Affiliations

    • Department of Animal and Range Sciences, North Dakota State University, 1300 Albrecht Boulevard, Fargo, ND 58105, USA
    • ,
  • J.S. Caton

      Affiliations

    • Department of Animal and Range Sciences, North Dakota State University, 1300 Albrecht Boulevard, Fargo, ND 58105, USA
    • ,
  • K.A. Vonnahme

      Affiliations

    • Department of Animal and Range Sciences, North Dakota State University, 1300 Albrecht Boulevard, Fargo, ND 58105, USA
    • ,
  • L.P. Reynolds

      Affiliations

    • Department of Animal and Range Sciences, North Dakota State University, 1300 Albrecht Boulevard, Fargo, ND 58105, USA
    • ,
  • J.B. Taylor

      Affiliations

    • USDA, ARS, USSES, Dubois, ID, USA
    • ,
  • C.L. Stoltenow

      Affiliations

    • Department of Animal and Range Sciences, North Dakota State University, 1300 Albrecht Boulevard, Fargo, ND 58105, USA
    • ,
  • K.I. O'Rourke

      Affiliations

    • USDA, ARS, ADRU, Pullman, WA, USA
    • ,
  • D.A. Redmer

      Affiliations

    • Department of Animal and Range Sciences, North Dakota State University, 1300 Albrecht Boulevard, Fargo, ND 58105, USA
    • Corresponding Author InformationCorresponding author. Tel.: +1 701 231 7991; fax: +1 701 231 7590.

,Accepted 9 February 2008.

References 

  1. Prusiner SB. Prions. Proc Natl Acad Sci USA. 1998;95:13363–13383
  2. DeArmond SJ, Mobley WC, DeMott DL. Changes in the localization of brain prion proteins during scrapie infection. Neurology. 1987;37:1271–1280
  3. Brown DR, Besinger A, Herms JW, Kretzschmar HA. Microglial expression of the prion protein. NeuroReport. 1998;9:1425–1429
  4. Glatzel M, Aguzzi A. PrP(C) expression in the peripheral nervous system is a determinant of prion neuroinvasion. J Gen Virol. 2000;81:2813–2821
  5. Herrmann LM, Baszler TV, Knowles DP, Cheevers WP. PrPSc is not detected in peripheral blood leukocytes of scrapie-infected sheep: Determining the limit of sensitivity by immunohistochemistry. Clin Diagn Lab Immunol. 2002;9:499–502
  6. Hallidays S, Houston F, Hunter N. Expression of PrPC on cellular components of sheep blood. J Gen Virol. 2005;86:1571–1579
  7. 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
  8. Ning ZY, Zhao DM, Yang JM, Cui YL, Meng LP, Wu CD, et al. Quantification of prion gene expression in brain and peripheral organs of golden hamster by real-time RT-PCR. Anim Biotechnol. 2005;16:55–65
  9. Donadio S, Alfaidy N, De Keukeleire B, Micoud J, Feige JJ, Challis JR, et al. Expression and localization of cellular prion and COMMD1 proteins in human placenta throughout pregnancy. Placenta. 2007;28:907–911
  10. Thumdee P, Ponsuksili S, Murani E, Nganvongpanit K, Gehrig B, Tesfaye D, et al. Expression of the prion protein gene (PRNP) and cellular prion protein (PrPc) in cattle and sheep fetuses and maternal tissues during pregnancy. Gene Expr. 2007;13:283–297
  11. Pattison IH, Hoare MN, Jebbett JN. Spread of scrapie to sheep and goats by oral dosing with foetal membranes from scrapie-affected sheep. Vet Rec. 1972;90:465–468
  12. Hoinville LJ. A review of the epidemiology of scrapie in sheep. Rev Sci Technol. 1996;15:827–852
  13. Bueler H, Aguzzi A, Sailer A, Greiner RA, Autenried P, Aguet M, et al. Mice devoid of PrP are resistant to scrapie. Cell. 1993;73:1339–1347
  14. Hunter N. Scrapie—Uncertainties, biology and molecular approaches. Biochim Biophys Acta. 2007;1772:619–628
  15. Goldmann W, Hunter N, Smith G, Foster J, Hope J. PrP genotypes and the Sip gene in Cheviot sheep form the basis for scrapie strain typing in sheep. Ann N Y Acad Sci. 1994;724:296–299
  16. Belt PB, Muileman IH, Schreuder BE, de Bos RJ, Gielkens AL, Smits MA. Identification of five allelic variants of the sheep PrP gene and their association with natural scrapie. J Gen Virol. 1995;76(Pt 3):509–517
  17. Hunter N, Foster JD, Goldmann W, Stear MJ, Hope J, Bostock C. Natural scrapie in a closed flock of Cheviot sheep occurs only in specific PrP genotypes. Arch Virol. 1996;141:809–824
  18. Parry HB. Scrapie: A transmissible and hereditary disease of sheep. Heredity. 1962;17:75–105
  19. Parry HB. Scrapie disease in sheep. New York: Academic Press; 1983;p. 69
  20. Vonnahme KA, Hess BW, Hansen TR, McCormick RJ, Rule DC, Moss GE, et al. Maternal undernutrition from early- to mid-gestation leads to growth retardation, cardiac ventricular hypertrophy, and increased liver weight in the fetal sheep. Biol Reprod. 2003;69:133–140
  21. Wallace JM, Luther JS, Milne JS, Aitken RP, Redmer DA, Reynolds LP, et al. Nutritional modulation of adolescent pregnancy outcome—a review. Placenta. 2006;27(suppl A):S61–S68
  22. Borowicz PP, Arnold DR, Johnson ML, Grazul-Bilska AT, Redmer DA, Reynolds LP. Placental growth throughout the last two thirds of pregnancy in sheep: vascular development and angiogenic factor expression. Biol Reprod. 2007;76:259–267
  23. Redmer DA, Doraiswamy V, Bortnem BJ, Fisher K, Jablonka-Shariff A, Grazul-Bilska AT, et al. Evidence for a role of capillary pericytes in vascular growth of the developing ovine corpus luteum. Biol Reprod. 2001;65:879–889
  24. Redmer DA, Aitken RP, Milne JS, Reynolds LP, Wallace JM. Influence of maternal nutrition on messenger RNA expression of placental angiogenic factors and their receptors at midgestation in adolescent sheep. Biol Reprod. 2005;72:1004–1009
  25. Chomczynski P. A reagent for the single-step simultaneous isolation of RNA, DNA and proteins from cell and tissue samples. BioTechniques. 1993;15:532–537
  26. Johnson ML, Evoniuk JM, Stoltenow CL, O'Rourke KI, Redmer DA. Development of an assay to determine single nucleotide polymorphisms (SNP) in the prion gene for the diagnosis of genetic susceptibility to scrapie in sheep. J Vet Diagn Invest. 2007;19:73–77
  27. Reynolds LP, Redmer DA. Growth and microvascular development of the uterus during early pregnancy in ewes. Biol Reprod. 1992;47:698–708
  28. Kirk RE. Experimental design: procedures for the behavioral sciences. Pacific Grove, CA: Brooks/Cole; 1982;
  29. Weissmann C, Bueler H, Fischer M, Sauer A, Aguet M. Susceptibility to scrapie in mice is dependent on PrPC. Phil Trans R Soc Lond B Biol Sci. 1994;343:431–433
  30. Kubosaki A, Nishimura-Nasu Y, Nishimura T, Yusa S, Sakudo A, Saeki K, et al. Expression of normal cellular prion protein (PrPc) on T lymphocytes and the effect of copper ion: analysis by wild-type and prion protein gene-deficient mice. Biochem Biophys Res Commun. 2003;307:810–813
  31. Tuo W, Zhuang D, Knowles DP, Cheevers WP, Sy MS, O'Rourke KI. PrP-C and PrP-Sc at the Fetal-Maternal Interface. J Biol Chem. 2001;276:18229–18234
  32. Herms J, Tings T, Gall S, Madlung A, Giese A, Siebert H, et al. Evidence of presynaptic location and function of the prion protein. J Neurosci. 1999;19:8866–8875
  33. Collinge J, Whittington MA, Sidle KCL, Smith CJ, Palmer MS, Clarke AR, et al. Prion protein is necessary for normal synaptic function. Nature. 1994;370:295–297
  34. Caughey B, Race RE, Ernst D, Buchmeier MJ, Chesebro B. Prion protein biosynthesis in scrapie-infected and uninfected neuroblastoma cells. J Virol. 1989;63:175–181
  35. Brown DR, Qin K, Herms JW, Madlung A, Manson J, Strome R, et al. The cellular prion protein binds copper in vivo. Nature. 1997;390:684–687
  36. Kim BH, Lee HG, Choi JK, Kim JI, Choi EK, Carp RI, et al. The cellular prion protein (PrPC) prevents apoptotic neuronal cell death and mitochondrial dysfunction induced by serum deprivation. Mol Brain Res. 2004;124:40–50
  37. McLennan NF, Brennan PM, McNeill A, Davies I, Fotheringham A, Rennison KA, et al. Prion protein accumulation and neuroprotection in hypoxic brain damage. Am J Pathol. 2004;65(1):227–235
  38. Manson J, West JD, Thomson V, McBride P, Kaufman MH, Hope J. The prion protein gene: A role in mouse embryogenesis?. Development. 1992;115:117–122
  39. Andreoletti O, Lacroux C, Chabert A, Monnereau L, Tabouret G, Lantier F, et al. PrPSc accumulation in placentas of ewes exposed to natural scrapie: influence of foetal PrP genotype and effect on ewe-to-lamb transmission. J Gen Virol. 2002;83:2607–2616
  40. Tuo W, O'Rourke KI, Zhuang D, Cheevers WP, Spraker TR, Knowles DP. Pregnancy status and fetal prion genetics determine PrPSc accumulation in placentomes of scrapie-infected sheep. Proc Natl Acad Sci USA. 2002;99:6310–6315
  41. Lacroux C, Corbiere F, Tabouret G, Lugan S, Costes P, Mathey J, et al. Dynamics and genetics of PrPSc placental accumulation in sheep. J Gen Virol. 2007;88:1056–1061
  42. Ryder S, Dexter G, Bellworthy S, Tongue S. Demonstration of lateral transmission of scrapie between sheep kept under natural conditions using lymphoid tissue biopsy. Res Vet Sci. 2004;76:211–217
  43. Herrmann LM, Baszler TV, O'Rourke KI, Suarez CE, Bakko M, Alverson J, et al. Fewer PrPc myeloid-based cells in sheep with the prion-resistant genotype. NeuroReport. 2006;17:125–129
  44. Alverson J, O'Rourke KI, Baszler TV. PrPSc accumulation in fetal cotyledons of scrapie-resistant lambs is influenced by fetus location in the uterus. J Gen Virol. 2006;87:1035–1041
  45. Wooding FBP. Frequency and localization of binucleate cells in the placentomes of ruminants. Placenta. 1983;4:527–539
  46. Wooding FBP. Role of binucleate cells in fetomaternal cell fusion at implantation in the sheep. Am J Anat. 1984;170:233–250
  47. Myagkaya G, Schellens JPM. Final stages of erythrophagocytosis in the sheep placenta. Cell Tissue Res. 1981;214:501–518

PII: S0143-4004(08)00047-7

doi: 10.1016/j.placenta.2008.02.003

Placenta
Volume 29, Issue 5 , Pages 422-428 , May 2008

Article Tools

* Image Usage & Resolution