Molecular and General Genetics MGG

, Volume 237, Issue 1–2, pp 193–205 | Cite as

The prosomal RNA-binding protein p27K is a member of the α-type human prosomal gene family

  • F. Bey
  • I. Silva Pereira
  • O. Coux
  • E. Viegas-Péquignot
  • F. Recillas Targa
  • H. G. Nothwang
  • B. Dutrillaux
  • K. Scherrer
Article

Summary

Monoclonal antibodies demonstrated high conservation during evolution of a prosomal protein of Mr 27 000 and differentiation - specific expression of the epitope. More than 90% of the reacting antigen was found as a p27K protein in the free messenger ribonucleoprotein (mRNP) fraction but another protein of Mr 38000, which shared protease fingerprint patterns with the p27K polypeptide, was also labelled in the nuclear and polyribosomal fractions. Sequencing of cDNA recombinant clones encoding the p27/38K protein and comparison with another prosomal protein, p30-33K, demonstrated the existence of a common characteristic sequence pattern containing three highly conserved segments. The genes Hs PROS-27 and Hs PROS-30 were mapped to chromosomes 14 (14g13) and 11 (11p15.1), respectively. The structure of the p27K protein shows multiple potential phosphorylation sites, an NTP-binding fold and an RNA-binding consensus sequence. The Hs PROS-27/β-galactosidase fusion protein binds a single RNA of about 120 nucleotides from total HeLa cell RNA. Sequence comparisons show that the Hs PROS-27 and Hs PROS-30 genes belong to the gene family that encodes the prosome — MCP (multicatalytic proteinase) — proteasome proteins. Comparison with other members of the family from various species allowed us to show that the tripartite consensus sequence characteristic of the α-type sub-family is conserved from archeobacteria to man. The members of this gene family are characterised by very high evolutionary conservation of amino acid sequences of homologous genes and 20%–35 sequence similarity, between different family member within the same species and are clearly distinct from the β-type family.

Key words

Gene family Prosomes Multicatalytic Proteinase (MCP) Proteasomes RNA-binding protein mRNP 

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References

  1. Adam SA, Nakagawa T, Swanson MS, Woodruff TK, Dreyfuss G (1986) mRNA polyadenylate-binding protein: gene isolation and sequencing and identification of a ribonucleoprotein consensus sequence. Mol Cell Biol 6:2932–2943Google Scholar
  2. Akhayat O, Grossi de Sa MF, Infante AA (1987) Sea urchin prosome: characterization and changes during development. Proc Natl Acad Sci USA 84:1595–1599Google Scholar
  3. Aki M, Tamura T, Tokunaga F, Iwanaga S, Kawamura Y, Shimbara N, Kagawa S, Tanaka K, Ichihara A (1992) cDNA cloning of rat proteasome subunit RC1, a homologue of RING10 located in the human MHC class II region. FEBS Lett 301:65–68Google Scholar
  4. Arcangeletti C, Olink-Coux M, Minisini R, Hueca M, Chezzi C, Scherrer K (1992) Patterns of cytodistribution of prosomal antigens on the vimentin and cytokeratin networks of monkey kidney cells. Eur J Cell Biol, in pressGoogle Scholar
  5. Arrigo AP, Tanaka K, Goldberg AL, Welch WJ (1988) Identity of the 19S “prosome” particle with the large multifunctional protease complex of mammalian cells (the proteasome). Nature 331:192–194Google Scholar
  6. Aviv H, Leder P (1972) Purification of biologically active globin messenger RNA by chromatography on oligothymidylic acid-cellulose. Proc Natl Acad Sci USA 69:1408–1412Google Scholar
  7. Banzdiulis RJ, Swanson M, Dreyfuss G (1989) RNA-binding proteins as developmental regulators. Genes Dev 3:431–437Google Scholar
  8. Briane D, Olink-Coux M, Vassy J, Oudar O, Huesca M, Scherrer K, Foucrier J (1992) Immunolocalization of a specific type of prosome close to the bile canaliculi in fetal and adult rat liver. Eur J Cell Biol 57:30–39Google Scholar
  9. Brown MC, Driscoll J, Monaco JJ (1991) Structural and serological similarity of MHC-linked LMP and proteasome (multicatalytic proteinase) complexes. Nature 353:355–357Google Scholar
  10. Bureau JP, Garrelly L, Vago P, Bayle S, Olink-Coux M, Aguilar V, Scherrer K (1989) Identification of prosomes proteins in human T lymphocyte populations by flow cytometry. Biol Cell 67:22aGoogle Scholar
  11. Castano JG, Ornberg R, Koster JG, Tobian JA, Zasloff M (1986) Eukaryotic pre-tRNA 5′ processing nuclease: copurification with a complex cylindrical particle. Cell 46:377–387Google Scholar
  12. Chambers JC, Kenan D, Martin BJ, Keene JD (1988) Genomic structure and amino acid sequence domains of the human La autoantigen. J Biol Chem 263:18043–18051Google Scholar
  13. Chomczynski P, Sacchi N (1987) Single-step method of RNA isolation by acid guanidium thiocyanate phenol chloroform extraction. Anal Biochem 162:156–159Google Scholar
  14. Cobianchi F, Sengupta DN, Zmuddzka BZ, Wilson SH (1986) Structure of rodent helix-destabilizing protein revealed by cDNA cloning. J Biol Chem 261:3536–3543Google Scholar
  15. Coux O, Nothwang H-G, Scherrer K, Bergsma-Schutter W, Arnberg A, Timmins P, Langowski J, Cohen-Addad C (1992) Structure and RNA content of the prosomes. FEBS Lett 300:49–55Google Scholar
  16. Dahlmann B, Kuehn L, Ishiura S, Tsukahara T, Sugita H, Tanaka K, Rivett J, Hough RF, Rechsteiner M, Mykles DL, Fagan JM, Waxman L, Ishii S, Sasaki M, Kloetzel PM, Harris H, Ray K, Behal FJ, Demartino GN, McGuire MJ (1988) The multicatalytic proteinase: a high-M(r) endopeptidase. Biochem J 255:750–751Google Scholar
  17. De Martino GN, Orth K, McCullough ML, Lee LW, Munn TZ, Moomaw CR, Dawson PA, Slaughter CA (1991) The primary structures of four subunits of the human, high-molecular-weight proteinase, macropain (proteasome), are distinct but homologous. Biochim Biophys Acta 1079:29–38Google Scholar
  18. Emori Y, Tsukahara T, Kawasaki H, Ishiura S, Sugita H, Suzuki K (1991) Molecular cloning and functional analysis of three subunits of yeast proteasome. Mol Cell Biol 11:344–353Google Scholar
  19. Falkenburg PE, Haass C, Kloetzel PM, Niedel B, Kopp F, Kuehn L, Dahlmann B (1988) Drosophila small cytoplasmic 19S ribonucleoprotein is homologous to the rat multicatalytic proteinase. Nature 331:190–192Google Scholar
  20. Feinberg AP, Vogelstein B (1983) A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem 132:6–13Google Scholar
  21. Fujii G, Tashiro K, Emori Y, Saigo K, Tanaka K, Shiokawa K, (1991) Deduced primary structure of a Xenopus proteasome subunit XC3 and expression of its mRNA during early development. Biochem Biophys Res Commun 178:1233–1239Google Scholar
  22. Fujiwara T, Tanaka K, Kumatori A, Shin S, Yoshimura T, Ichihara A, Iokunaga F, Aruga R, Wanaga S, Kakizuka A, Nakanishi S (1989) Molecular cloning of cDNA for proteasome (multicatalytic proteinase complexes) from rat liver: primary structure of the largest component (C2). Biochemistry 28:7332–7340Google Scholar
  23. Fujiwara T, Tanaka K, Orino E, Yoshimura T, Kumatori A, Tamura T, Chungi CH, Nakai T, Yamaguchi K, Shin S, Kakizuka A, Nakanishi S, Ichihara A (1990) Proteasomes are essential for yeast proliferation — cDNA cloning and gene disruption of 2 major subunits. J Biol Chem 265:16604–16613Google Scholar
  24. Glover DM (1985) DNA cloning: a practical approach. IRL Press, OxfordGoogle Scholar
  25. Glynne R, Powis SH, Beck S, Kelly A, Kerr LA, Trowsdale J (1991) A proteasome-related gene between the 2 ABC transporter loci in the class-II Region of the human MHC. Nature 353:357–360Google Scholar
  26. Grainger JL, Winkler MM (1987) Fertilization triggers unmasking of maternal mRNAs in Sea Urchin eggs. Mol Cell Biol 7:3947–3954Google Scholar
  27. Grainger JL, Winkler MM (1989) The sea urchin multicatalytic protease: purification, biochemical analysis, subcellular distribution, and relationship to snRNPs. J Cell Biol 109:675–683Google Scholar
  28. Grossi de Sa MF, Martins de Sa C, Harper F, Coux O, Akhayat O, Florentin Y, Pal JK, Scherrer K (1988a) Cytolocalization of prosomes as a function of differentiation. J Cell Sci 89:151–165Google Scholar
  29. Grossi de Sa MF, Martins de Sa C, Harper F, Olink-Coux M, Huesca M, Scherrer K (1988b) The association of prosomes with some of the intermediate filament networks on the animal cell. J Cell Biol 107:1517–1530Google Scholar
  30. Haass C, Pesold-Hurt B, Multhaup G, Beyreuther K, Kloetzel PM (1989) The PROS-35 gene encodes the 35 Kd protein subunit of Drosophila melanogaster proteasome. EMBO J 8:2372–2379Google Scholar
  31. Haass C, Pesoldhurt B, Kloetzel PM (1990a) The Drosophila PROS-29 gene is a new member of the PROS-gene-family. Nucleic Acids Res 18:4018Google Scholar
  32. Haass C, Pesold-Hurt B, Multhaup G, Beyreuther K, Kloetzel PM (1990b) The Drosophila PROS-28.1 gene is a member of the proteasome gene family. Gene 90:235–241Google Scholar
  33. Haffter P, Fox TD (1991) Nucleotide sequence of PUP1 encoding a putative proteasome subunit in Saccharomyces cerevisiae. Nucleic Acids Res 19:5075–5075Google Scholar
  34. Heinemeyer W, Kleinschmidt JA, Saidowsky J, Escher C, Wolf DH (1991) Proteinase yscE, the yeast proteasome/multicatalytic-multifunctional proteinase — mutants unravel its function in stress induced proteolysis and uncover its necessity for cell survival. EMBO J 10:555–562Google Scholar
  35. Horsch A, Martins de Sa C, Dineva B, Spindler E, Schmid HP (1989) Prosomes discriminate between mRNA of adenovirus infected and uninfected HeLa cells. FEBS Lett 246:131–136Google Scholar
  36. Kelly A, Powis SH, Glynner R, Radley E, Beck S, Trowsdale J (1991) Second proteasome-related gene in the human MHC class II region. Nature 353:667–668Google Scholar
  37. Kreutzer-Schmid C, Schmid HP (1990) The prosomal protein of 27 kDa and a nuclear 38 kDa protein are immunologically related. FEBS Lett 267:142–146Google Scholar
  38. Krohne G, Wolin SL, McKeon FD, Franke WW, Kirschner MW (1987) Nuclear lamin LI of Xenopus laevis: cDNA cloning, amino acid sequence and binding specificity of a member of the lamin B sub-family. EMBO J 6:3801–3808Google Scholar
  39. Kumatori A, Tanaka K, Tamura T, Fujiwara T, Ichihara A, Tokunaga F, Onikura A, Iwanaga S (1990) cDNA cloning and sequencing of component C9 of proteasomes from rat hepatoma cells. FEBS Lett 264:279–282Google Scholar
  40. Kyte J, Doolittle (1982) A simple method for displaying the hydrophobic character of a protein J Mol Biol 157:105–132Google Scholar
  41. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685Google Scholar
  42. Lee DH, Tanaka K, Tamuea T, Chung C, Ichihara A (1992) PRS3 encoding an essential subunit of Yeast proteasomes homologous to mammalian proteasome subunit C5. Biochem Biophys Res Commun 182:452–460Google Scholar
  43. Lerner MR, Steitz JA (1979) Antibodies to small nuclear RNAs complexed with proteins are produced by patients with systemic lupus erythematosus. Proc Natl Acad Sci USA 76:5495–5499Google Scholar
  44. Maniatis T, Fritsch EF, Sambrook J (1982) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, NYGoogle Scholar
  45. Martinez CK, Monaco JJ (1991) Homology of proteasome subunits to a major histocompatibility complex-linked LMP gene. Nature 353:664–667Google Scholar
  46. Martins de Sa C, Grossi de Sa ME, Akhayat O, Broders F, Scherrer K, Horsch A, Schmid HP (1986) Prosomes: Ubiquity and inter species structural variation. J Mol Biol 187:479–493Google Scholar
  47. Martins de Sa C, Rollet E, Grossi de Sa M-F, Tanguay RM, Best-Belpomme M, Scherrer K (1989) Prosomes and the heatshock complexes in Drosophila melanogaster cells. Mol Cell Biol 9:2672–2681Google Scholar
  48. Monaco JJ, McDevitt HO (1982) Identification of a forth class of proteins linked to the murine major histocompatibility complex. Proc Nat Acad Sci USA 79:3001–3005Google Scholar
  49. Nothwang H-G, Coux O, Bey F, Scherrer K (1992a) Prosomes and their multicatalytic (MCP) proteinase activity. Eur J Biochem 207:621–630Google Scholar
  50. Nothwang H-G, Coux O, Keith G, Silva Pereira I, Scherrer K (1992b) The major RNA in prosomes of HeLa cells and duck erythroblasts in tRNALys,3. Nucleic Acids Res 20:1959–1965Google Scholar
  51. Olink-Coux M, Huesca M, Scherrer K (1992) Specific types of prosomes are associated to subnetworks of the intermediate filaments in PtK 1 cells. Eur J Cell Biol, in pressGoogle Scholar
  52. Orlowski M (1990) The Multicatalytic-Proteinase Complex, a major extralysosomal proteolytic system. Biochemistry 29:10289–10297Google Scholar
  53. Orlowski M, Wilk S (1988) “Multicatalytic proteinase complex” or “multicatalytic proteinase: a high-M(r) endopeptidase”. Biochem J 255:751Google Scholar
  54. Ortiznavarrete V, Seelig A, Gernold M, Frentzel S, Kloetzel PM, Hammerling GJ (1991) Subunit of the 20s proteasome (Multicatalytic proteinase) encoded by the major histocompatibility complex. Nature 353:662–664Google Scholar
  55. Pal JK, Gounon P, Grossi de Sa M-F, Scherrer K (1988) Distribution of prosome antigens changes as a function of embryonic development and tissue-type differentiation in Pleurodeles walti. J Cell Sci 90:555–567Google Scholar
  56. Peters JM, Walsh J, Franke WW (1990) An abundant and ubiquitous homo-oligomeric ring-shaped ATPase particle related to the putative vesicle fusion proteins Sec 18p and NSF. EMBO J 9:1757–1767Google Scholar
  57. Pühler G, Weinkauf S, Bachmann L, Muller S, Engel A, Hegerl R, Baumeister W (1992) Subunit stoichiometry and three-dimensional arrangement in proteasomes from Thermoplasma acidophilum. EMBO J 11:1607–1616Google Scholar
  58. Query CC, Bentley RC, Keene JD (1989) A common RNA recognition motif identified within a defined U1 RNA binding domain of the 70K Ul snRNP protein. Cell 57:89–101Google Scholar
  59. Riva S, Morandi C, Tsoulfas P, Pandolfo MN, Biamonti G, Merill B, Williams KR, Multhaup G, Beyreuther K, Werr H, Heinrich B, Schafer KP (1986) Mammalian single-stranded DNA binding protein UP1 is derived from the hnRNP core protein A1. EMBO J 5:2267–2273Google Scholar
  60. Rivett AJ (1989) The multicatalytic proteinase complex. RBC Cell Biol Rev 20:113–123Google Scholar
  61. Roberts B (1989) Nuclear location signal-mediated protein transport. Biochim Biophys Acta 1008:263–280Google Scholar
  62. Sachs AB, Bond WM, Kornberg RD (1986) A single gene from yeast for both nuclear and cytoplasmic polyadenylate-binding proteins: domain structure and expression. Cell 45:827–835Google Scholar
  63. Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74:5463–5467Google Scholar
  64. Scherrer K (1990) Prosomes, subcomplexes of untranslated messenger RNP. Mol Biol Rep 14:1–9Google Scholar
  65. Schmid HP, Akhayat O, Martins de Sa C, Puvion F, Koehler K, Scherrer K (1984) The Prosome: An ubiquitous morphologically distinct RNP particle associated with repressed mRNPs and containing specific ScRNA and a characteristic set of proteins. EMBO J 3:29–34Google Scholar
  66. Shelton E, Kuff EL, Maxwell ES, Harrington JT (1970) Cytoplasmic particles and aminoacyl transferase I activity. J Cell Biol 45:1–8Google Scholar
  67. Silva Pereira I, Bey F, Coux O, Scherrer K (1992) Two mRNAs exist for the Hs PROS-30 gene encoding a component of human prosomes. Gene 120:235–242Google Scholar
  68. Skilton HE, Eperon IC, Rivett AJ (1991) Co-purification of a small RNA species with multicatalytic proteinase (proteasome) from rat liver. FEBS Lett 279:351–355Google Scholar
  69. Spohr G, Granboulan N, Morel C, Scherrer K (1970) Messenger RNA in HeLa cells: an investigation of free and polyribosome — bound cytoplasmic messenger ribonucleoprotein particles by kinetic labelling and electron microscopy. Eur J Biochem 17:296–318Google Scholar
  70. Staden R (1982) An interactive graphics program for comparing and aligning nucleic acid and amino acid sequences. Nucleic Acids Res 10:2951–2901Google Scholar
  71. Swanson MS, Nakagawa TY, LeVan K, Dreyfuss G (1987) Primary structure of human nuclear ribonucleoprotein particle C proteins: conservation of sequence and domain structures in heterogeneous nuclear RNA, mRNA, and pre-rRNA-binding proteins. Mol Cell Biol 7:1731–1739Google Scholar
  72. Tamura T, Tanaka K, Kumatori A, Yamada F, Tsurumi C, Fujiwara T, Ichihara A, Tokunaga F, Aruga R, Iwanaga S (1990) cDNA cloning and sequencing of component C5 of proteasomes from rat hepatoma-cells. FEBS Lett 264:91–94Google Scholar
  73. Tamura T, Lee DH, Osaka F, Fujiwara T, Shin S, Chung CH, Tanaka K, Ichihara A (1991) Molecular cloning and sequence analysis of cDNAs for five major subunits of human proteasomes (multi-catalytic proteinase complexes). Biochim Biophys Acta 1089:95–102Google Scholar
  74. Tanaka K, Fujiwara T, Kumatori A, Shin S, Yoshimura T, Ichihara A, Tokunaga F, Aruga R, Iwanaga S, Kakizuka A, Nakanishi S (1990a) Molecular cloning of cDNA for proteasomes from rat-liver — primary structure of component-C3 with a possible tyrosine phosphorylation site. Biochemistry 29:3777–3785Google Scholar
  75. Tanaka K, Yoshimura T, Tamura T, Fujiwara T, Kumatori A, Ichihara A (1990b) Possible mechanism of nuclear translocation of proteasomes. FEBS Lett 271:41–46Google Scholar
  76. Tanaka K, Kanayama H, Tamura T, Lee DH, Kumatori A, Fujiwara T, Ichihara A, Tokunaga F, Aruga R, Iwanaga S (1990c) cDNA cloning and sequencing of component C8 of proteasomes from rat hepatoma cells. Biochem Biophys Res Commun 171:676–683Google Scholar
  77. Tomek W, Adam G, Schmid HP (1988) Prosomes, small cytoplasmic RNP particles, contain glycoproteins. FEBS Lett 239:155–158Google Scholar
  78. Van Riel M, Martens G (1991) Cloning and sequence analysis of pituitary cDNA encoding the beta-subunit of Xenopus proteasome. FEBS Lett 291:37–40Google Scholar
  79. Viegas-Pequignot E, Dutrillaux B (1978) Une méthode simple pour l'obtention de mitoses en prophase et en métaphase. Ann Génét 21:122–125Google Scholar
  80. Viegas-Pequignot E, Dutrillaux B, Magdelenat H, Coppey-Moisan M (1989) Mapping of single-copy DNA sequences on human chromosomes by in situ hybridization with biotinylated probes: Enhancement of detection sensitivity by intensified-fluorescence digital-imaging microscopy. Proc Natl Acad Sci USA 86:582–586Google Scholar
  81. Walker JE, Saraste M, Runswick MJ, Gay NJ (1982) Distantly related sequences in the a and b subunits of ATP synthetase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide fold. EMBO J 1:945–951Google Scholar
  82. Walter P, Blobel G (1983) Signal recognition particle, a ribonucleoprotein required for cotranslational translocation of proteins: isolation and properties. Methods Enzymol 96:84–93Google Scholar
  83. Wolin SL, Krohne G, Kirschner MW (1987) A new lamin in Xenopus somatic tissues displays strong homology to human lamin. EMBO J 6:3809–3818Google Scholar
  84. Zwickl P, Lottspeich F, Dahlmann B, Baumeister W (1991) Cloning and sequencing of the gene encoding the large (alpha-) subunit of the proteasome from Thermoplasma acidophilum FEBS Lett 278:217–221Google Scholar
  85. Zwickl P, Grizwa A, Puehler G, Dahlmann B, Lottspeich F, Baumeister W (1992) The primary structure of the Thermoplasma proteasome and its implication for the structure, function and evolution of the multicatalytic proteinase. Biochemistry 31:964–971Google Scholar

Copyright information

© Springer-Verlag 1993

Authors and Affiliations

  • F. Bey
    • 1
  • I. Silva Pereira
    • 1
  • O. Coux
    • 1
  • E. Viegas-Péquignot
    • 2
  • F. Recillas Targa
    • 1
  • H. G. Nothwang
    • 1
  • B. Dutrillaux
    • 2
  • K. Scherrer
    • 1
  1. 1.Institut Jacques Monod du CNRSUniversité Paris 7Paris Cedex 05France
  2. 2.Institut CurieParisFrance

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