Structural and functional analysis of the ovine laminin receptor gene (RPSA): Possible involvement of the LRP/LR protein in scrapie response

Mammalian Genome

Volumn 19, Issue 2, 2008, Pages 92-105

  Marcos Carcavilla, Ane ^a   Calvo, Jorge H ^b   González, Carmen ^a   Serrano, Carmen ^e   Moazami Goudarzi, Katayoun ^c   Laurent, Pascal ^c   Bertaud, Maud ^c   Hayes, Hélène ^c   Beattie, Anne E ^d   Lyahyai, Jaber ^e   Martín Burriel, Inmaculada ^e   Torres, Juan María ^f   Serrano, Magdalena ^a  

^a INIA   (Spain)

^b Unidad de Sanidad Vegetal   (Spain)

^c Institut National de la Recherche Agronomique   (France)

^d INVERMAY AGRICULTURAL CENTRE   (New Zealand)

^e UNIVERSIDAD DE ZARAGOZA   (Spain)

^f Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; LAMININ RECEPTOR; MESSENGER RNA;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN REGION; CEREBELLUM; CHROMOSOME MAP; CONTROLLED STUDY; DIENCEPHALON; FEMALE; GENE ISOLATION; GENE MAPPING; MAMMAL; MEDULLA OBLONGATA; NONHUMAN; NUCLEOTIDE SEQUENCE; OVINE LAMININ RECEPTOR GENE; PRION DISEASE; PSEUDOGENE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCRAPIE; SHEEP; STRUCTURE ANALYSIS;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; CHROMOSOME MAPPING; CHROMOSOMES, MAMMALIAN; GENE EXPRESSION REGULATION; GENOTYPE; MOLECULAR SEQUENCE DATA; POLYMORPHISM, GENETIC; RECEPTORS, LAMININ; SCRAPIE; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY, AMINO ACID; SHEEP, DOMESTIC;

CAPRA HIRCUS; MAMMALIA; OVIS; OVIS ARIES;

EID: 39149123474     PISSN: 09388990     EISSN: 14321777     Source Type: Journal    
DOI: 10.1007/s00335-007-9085-6     Document Type: Article

References (64)

1. Adjou KT, Simoneau S, Sales N, Lamoury F, Dormont D et al. (2003) A novel generation of heparan sulfate mimetics for the treatment of prion diseases. J Gen Virol 84:2595-2603
2. Asano Y, Takashima S, Asakura M, Shintani Y, Liao Y et al. (2004) Lamr1 functional retroposon causes right ventricular dysplasia in mice. Nat Genet 36:123-130
3. Auth D, Brawerman G (1992) A 33-kDa polypeptide with homology to the laminin receptor: component of translation machinery. Proc Natl Acad Sci USA 89:4368-4372
4. Balakirev ES, Ayala FJ (2003) Pseudogenes: are they "junk" or functional DNA? Annu Rev Genet 37:123-151
5. Baloui H, von Boxberg Y, Vinh J, Weiss S, Rossier J et al. (2004) Cellular prion protein/laminin receptor: distribution in adult central nervous system and characterization of an isoform associated with a subtype of cortical neurons. Eur J Neurosci 20:2605-2616
6. Baylis M, Chihota C, Stevenson E, Goldmann W, Smith A et al. (2004) Risk of scrapie in British sheep of different prion protein genotype. J Gen Virol 85:2735-2740
7. Ben-Zaken O, Tzaban S, Tal Y, Horonchik L, Esko JD et al. (2003) Cellular heparan sulfate participates in the metabolism of prions. J Biol Chem 278:40041-40049
8. Caplazi P, O'Rourke K, Wolf C, Shaw D, Baszler TV (2004) Biology of PrPsc accumulation in two natural scrapie-infected sheep flocks. J Vet Diagn Invest 16:489-496
9. Castilla J, Gutierrez-Adan A, Brun A, Doyle D, Pintado B et al. (2004) Subclinical bovine spongiform encephalopathy infection in transgenic mice expressing porcine prion protein. J Neurosci 24:5063-5069
10. Castronovo V, Claysmith AP, Barker KT, Cioce V, Krutzsch HC et al. (1991) Biosynthesis of the 67 kDa high affinity laminin receptor. Biochem Biophys Res Commun 177:177-183
11. Clausse N, Jackers P, Jares P, Joris B, Sobel ME et al. (1996) Identification of the active gene coding for the metastasis-associated 37LRP/p40 multifunctional protein. DNA Cell Biol 15:1009-1023
12. Crawford AM, Dodds KG, Ede AJ, Pierson CA, Montgomery GW, et al. (1995) An autosomal genetic linkage map of the sheep genome. Genetics 140:703-724
13. Creighton TE (1992) Protein folding pathways determined using disulphide bonds. Bioessays 14:195-199
14. Garcia-Crespo D, Juste R, Hurtado A (2005) Selection of ovine housekeeping genes for normalisation by real-time RT-PCR; analysis of PrP gene expression and genetic susceptibility to scrapie. BMC Vet Res 1:3
15. Gauczynski S, Peyrin JM, Haik S, Leucht C, Hundt C et al. (2001) The 37-kDa/67-kDa laminin receptor acts as the cell-surface receptor for the cellular prion protein. EMBO J 20:5863-5875
16. Gauczynski S, Nikles D, El-Gogo S, Papy-Garcia D, Rey C et al. (2006) The 37-kDa/67-kDa laminin receptor acts as a receptor for infectious prions and is inhibited by polysulfated glycanes. J Infect Dis 194:702-709
17. Goldmann W, Baylis M, Chihota C, Stevenson E, Hunter N (2005) Frequencies of PrP gene haplotypes in British sheep flocks and the implications for breeding programmes. J Appl Microbiol 98:1294-1302
18. Hayes H, Petit E, Dutrillaux B (1991) Comparison of RBG-banded karyotypes of cattle, sheep and goats. Cytogenet Cell Genet 57:51-55
19. Hirotsune S, Yoshida N, Chen A, Garrett L, Sugiyama F et al. (2003) An expressed pseudogene regulates the messenger-RNA stability of its homologous coding gene. Nature 423:91-96
20. Horonchik L, Tzaban S, Ben-Zaken O, Yedidia Y, Rouvinski A et al. (2005) Heparan sulfate is a cellular receptor for purified infectious prions. J Biol Chem 280:17062-17067
21. Hundt C, Peyrin JM, Haik S, Gauczynski S, Leucht C et al. (2001) Identification of interaction domains of the prion protein with its 37-kDa/67-kDa laminin receptor. EMBO J 20:5876-5886
22. Jackers P, Clausse N, Fernandez M, Berti A, Princen F et al. (1996) Seventeen copies of the human 37 kDa laminin receptor precursor/p40 ribosome-associated protein gene are processed pseudogenes arisen from retropositional events. Biochim Biophys Acta 1305:98-104
23. Karpatova M, Tagliabue E, Castronovo V, Magnifico A, Ardini E et al. (1996) Shedding of the 67-kD laminin receptor by human cancer cells. J Cell Biochem 60:226-234
24. Kim WH, Lee BL, Jun SH, Song SY, Kleinman HK (1998) Expression of 32/67-kDa laminin receptor in laminin adhesion-selected human colon cancer cell lines. Br J Cancer 77:15-20
25. Kinoshita K, Kaneda Y, Sato M, Saeki Y, Wataya-Kaneda M et al. (1998) LBP-p40 binds DNA tightly through associations with histones H2A, H2B, and H4. Biochem Biophys Res Commun 253:277-282
26. Kiss AM, Jady BE, Bertrand E, Kiss T (2004) Human box H/ACA pseudouridylation guide RNA machinery. Mol Cell Biol 24:5797-5807
27. Knorr C, Beuermann C, Beck J, Brenig B (2007) Characterization of the porcine multicopy ribosomal protein SA/37-kDa laminin receptor gene family. Gene 395:135-143
28. Kocisko DA, Priola SA, Raymond GJ, Chesebro B, Lansbury PT Jr et al. (1995) Species specificity in the cell-free conversion of prion protein to protease-resistant forms: a model for the scrapie species barrier. Proc Natl Acad Sci USA 92:3923-3927
29. Lander ES, Green P (1987) Construction of multilocus genetic linkage maps in humans. Proc Natl Acad Sci USA 84:2363-2367
30. Landowski TH, Dratz EA, Starkey JR (1995) Studies of the structure of the metastasis-associated 67 kDa laminin binding protein: fatty acid acylation and evidence supporting dimerization of the 32 kDa gene product to form the mature protein. Biochemistry 34:11276-11287
31. Leucht C, Simoneau S, Rey C, Vana K, Rieger R et al. (2003) The 37 kDa/67 kDa laminin receptor is required for PrP(Sc) propagation in scrapie-infected neuronal cells. EMBO Rep 4:290-295
32. Ligios C, Jeffrey M, Ryder SJ, Bellworthy SJ, Simmons MM (2002) Distinction of scrapie phenotypes in sheep by lesion profiling. J Comp Pathol 127:45-57
33. Lyahyai J, Bolea R, Serrano C, Monleón E, Moreno C et al. (2006) Correlation between Bax overexpression and prion deposition in medulla oblongata from natural scrapie without evidence of apoptosis. Acta Neuropathol (Berl) 112:451-460
34. Lysek DA, Schorn C, Nivon LG, Esteve-Moya V, Christen B et al. (2005) Prion protein NMR structures of cats, dogs, pigs, and sheep. Proc Natl Acad Sci USA 102:640-645
35. Lloyd SE, Onwuazor ON, Beck JA, Mallinson G, Farrall M et al. (2001) Identification of multiple quantitative trait loci linked to prion disease incubation period in mice. Proc Natl Acad Sci USA 98:6279-6283
36. Lloyd SE, Uphill JB, Targonski PV, Fisher EM, Collinge J (2002) Identification of genetic loci affecting mouse-adapted bovine spongiform encephalopathy incubation time in mice. Neurogenetics 4:77-81
37. Maddox JF, Davies KP, Crawford AM, Hulme DJ, Vaiman D et al. (2001) An enhanced linkage map of the sheep genome comprising more than 1000 loci. Genome Res 11:1275-1289
38. Manolakou K, Beaton J, McConnell I, Farquar C, Manson J et al. (2001) Genetic and environmental factors modify bovine spongiform encephalopathy incubation period in mice. Proc Natl Acad Sci USA 98:7402-7407
39. Mariottini P, Amaldi F (1990) The 5′ untranslated region of mRNA for ribosomal protein S19 is involved in its translational regulation during Xenopus development. Mol Cell Biol 10:816-822
40. Miller S, Dykes D, Polesky H (1988) A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Res 16:1215
41. Morel E, Andrieu T, Casagrande F, Gauczynski S, Weiss S et al. (2005) Bovine prion is endocytosed by human enterocytes via the 37 kDa/67 kDa laminin receptor. Am J Pathol 167:1033-1042
42. Moreno CR, Cosseddu GM, Andreoletti IO, Schibler L, Roig A et al (2003a) Identification of quantitative trait loci (QTL) modulating prion incubation period in sheep. Proceedings of the International Workshop on Major Genes and QTL in Sheep and Goat, Toulouse
43. Moreno CR, Lantier F, Lantier I, Sarradin P, Elsen JM (2003b) Detection of new quantitative trait loci for susceptibility to transmissible spongiform encephalopathies in mice. Genetics 165:2085-2091
44. Nag MK, Thai TT, Ruff EA, Selvamurugan N, Kunnimalaiyaan M et al. (1993) Genes for E1, E2, and E3 small nucleolar RNAs. Proc Natl Acad Sci USA 90:9001-9005
45. Priola SA, Caughey B, Race RE, Chesebro B (1994) Heterologous PrP molecules interfere with accumulation of protease-resistant PrP in scrapie-infected murine neuroblastoma cells. J Virol 68:4873-4878
46. Prusiner SB (1998) Prions. Proc Natl Acad Sci USA 95:13363-13383
47. Rabacchi SA, Neve RL, Drager UC (1990) A positional marker for the dorsal embryonic retina is homologous to the high-affinity laminin receptor. Development 109:521-531
48. Rao M, Manishen WJ, Maheshwari Y, Sykes DE, Siyanova EY et al. (1994) Laminin receptor expression in rat intestine and liver during development and differentiation. Gastroenterology 107:764-772
49. Rieger R, Edenhofer F, Lasmezas CI, Weiss S (1997) The human 37-kDa laminin receptor precursor interacts with the prion protein in eukaryotic cells. Nat Med 3:1383-1388
50. SAS Institute Inc. (1989) SAS/STAT® Users's Guide, version 6, 4th ed., vol. 1 (Cary, NC: SAS Institute, Inc.)
51. Scott M, Groth D, Foster D, Torchia M, Yang SL et al. (1993) Propagation of prions with artificial properties in transgenic mice expressing chimeric PrP genes. Cell 73:979-988
52. Selvamurugan N, Eliceiri GL (1995) The gene for human E2 small nucleolar RNA resides in an intron of a laminin-binding protein gene. Genomics 30:400-401
53. Shmakov AN, Bode J, Kilshaw PJ, Ghosh S (2000) Diverse patterns of expression of the 67-kD laminin receptor in human small intestinal mucosa: potential binding sites for prion proteins? J Pathol 191:318-322
54. Simoneau S, Haik S, Leucht C, Dormont D, Deslys JP et al. (2003) Different isoforms of the non-integrin laminin receptor are present in mouse brain and bind PrP. Biol Chem 384:243-246
55. Simons K, Toomre D (2000) Lipid rafts and signal transduction. Nat Rev Mol Cell Biol 1:31-39
56. Stephenson DA, Chiotti K, Ebeling C, Groth D, DeArmond SJ et al. (2000) Quantitative trait loci affecting prion incubation time in mice. Genomics 69:47-53
57. Vaiman D, Billault A, Tabet-Aoul K, Schibler L, Vilette D et al. (1999) Construction and characterization of a sheep BAC library of three genome equivalents. Mamm Genome 10:585-587
58. Vana K, Weiss S (2006) A trans-dominant negative 37 kDa/67 kDa laminin receptor mutant impairs PrP(Sc) propagation in scrapie-infected neuronal cells. J Mol Biol 358:57-66
59. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N et al. (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3:RESEARCH0034
60. Vidal E, Bolea R, Tortosa R, Costa C, Domènech A et al. (2006) Assessment of calcium-binding proteins (Parvalbumin and Calbindin D-28 K) and perineuronal nets in normal and scrapie-affected adult sheep brains. J Virol Meth 36:137-146
61. Vorberg I, Groschup MH, Pfaff E, Priola SA (2003) Multiple amino acid residues within the rabbit prion protein inhibit formation of its abnormal isoform. J Virol 77:2003-2009
62. Yenofsky R, Bergmann I, Brawerman G (1982) Messenger RNA species partially in a repressed state in mouse sarcoma ascites cells. Proc Natl Acad Sci USA 79:5876-5880
63. Yenofsky R, Cereghini S, Krowczynska A, Brawerman G (1983) Regulation of mRNA utilization in mouse erythroleukemia cells induced to differentiate by exposure to dimethyl sulfoxide. Mol Cell Biol 3:1197-1203
64. Yow H, Wong JM, Chen HS, Lee C, Steele GD et al. (1988) Increased mRNA expression of a laminin-binding protein in human colon carcinoma: complete sequence of a full-length cDNA encoding the protein. Proc Natl Acad Sci USA 85:6394-6398