Molecular cloning of the ribosomal P-proteins MgP1, MgP2, MgP0, and superoxide dismutase (SOD) in the mussel Mytilus galloprovincialis and analysis of MgP0 at stress conditions

Gene

Volumn 430, Issue 1-2, 2009, Pages 77-85

  Kolaiti, Regina Maria ^a   Lucas, Jared M ^b   Kouyanou Koutsoukou, Sophia ^a  

^a UNIVERSITY OF ATHENS   (Greece)

^b Fred Hutchinson Cancer Research Center   (United States)

Author keywords

Over expression; Phosphorylation; Purification; Ribosomal stalk; Stress

Indexed keywords

ALKALINE PHOSPHATASE; CADMIUM; COMPLEMENTARY DNA; PROTEIN MGP0; PROTEIN MGP1; PROTEIN MGP2; RIBOSOME PROTEIN; SORBITOL; SUPEROXIDE DISMUTASE; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; ESCHERICHIA COLI; EXPRESSION VECTOR; MOLECULAR CLONING; MYTILUS GALLOPROVINCIALIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; PROTEIN PURIFICATION; STRESS;

AMINO ACID SEQUENCE; ANIMALS; CADMIUM; CHROMATOGRAPHY, AFFINITY; CLONING, MOLECULAR; DNA, COMPLEMENTARY; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ESCHERICHIA COLI; IMMUNOBLOTTING; MOLECULAR SEQUENCE DATA; MYTILUS; RIBOSOMAL PROTEINS; RIBOSOMES; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID; SORBITOL; STRESS, PHYSIOLOGICAL; SUPEROXIDE DISMUTASE;

ESCHERICHIA COLI; MYTILUS GALLOPROVINCIALIS;

EID: 58049129569     PISSN: 03781119     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.gene.2008.10.024     Document Type: Article

References (54)

1. Abramczyk O., Zień P., Zieliński R., Pilecki M., Hellman U., and Szyszka R. The protein kinase 60S is a free catalytic CK2alpha' subunit and forms an inactive complex with superoxide dismutase SOD1. Biochem. Biophys. Res. Commun. 307 (2003) 31-40
2. Arslantas A. Development of functional models for a SOD. Met Based Drugs 9 (2002) 9-18
3. Ballesta J.P.G., and Remacha M. The large ribosomal subunit stalk as a regulatory element of the eukaryotic translational machinery. Prog. Nucleic Acid Res. Mol. Biol. 55 (1996) 157-193
4. Barnard G.F., et al. Gastric and hepatocellular carcinomas do not over express the same ribosomal protein messenger RNAs as colonic carcinoma. Cancer Res. 53 (1993) 4048-4052
5. Chang T.-W., Chen C.-C., Chen K.-Y., Su J.-H., Chang J.-H., and Chang M.-C. Ribosomal phosphoprotein P0 interacts with GCIP and over expression of P0 is associated with cellular proliferation in breast and liver carcinoma cells. Oncogene 27 (2008) 332-338
6. Diaconu M., et al. Structural basis for the function of the ribosomal L7/12 stalk in factor binding and GTPase activation. Cell. 121 (2005) 991-1004
7. Dondero F., Piacentini L., Banni M., Rebelo M., Burlando B., and Viarengo A. Quantitative PCR analysis of two molluscan metallothionein genes unveils differential expression and regulation. Gene 345 (2005) 259-270
8. Gagou M.E., Rodriguez-Gabriel M.A., Ballesta J.P.G., and Kouyanou S. The ribosomal P-proteins of the medfly Ceratitis capitata form a heterologous stalk structure interacting with the endogenous P-proteins, in conditional P0-null strains of the yeast Saccharomyces cerevisiae. Nucleic Acids Res. 28 (2000) 736-743
9. Galaris D., and Evangelou A. The role of oxidative stress in mechanisms of metal-induced carcinogenesis. Crit. Rev. Oncol. Hematol. 42 (2002) 93-103
10. Geret F., and Cosson R.P. Induction of specific isoforms of metallothionein in mussel tissues after exposure to cadmium or mercury. Arch. Environ. Contam. Toxicol. 42 (2002) 36-42
11. Geret F., Manduzio H., Company R., Leboulenger F., Bebianno M.J., and Danger J.M. Molecular cloning of superoxide dismutase (Cu/Zn-SOD) from aquatic molluscs. Mar. Environ. Res. 58 (2004) 619-623
12. Glover C.V. On the physiological role of casein kinase II in Saccharomyces cerevisiae. Prog. Nucleic Acid Res. Mol. Biol. 59 (1998) 95-133
13. Gonzalo P., and Reboud J.P. The puzzling lateral flexible stalk of the ribosome. Biol. Cell 95 (2003) 179-193
14. Grela P., Sawa-Makarska J., Gordiyenko Y., Robinson C.V., Grankowski N., and Tchorzewski M. Structural properties of the human acidic ribosomal P proteins forming the P1-P2 heterocomplex. J. Biochem. 143 (2008) 169-177
15. Guarinos E., Santos C., Sanchez A., Qiu D.-Y., Remacha M., and Ballesta J.P. Tag-mediated fractionation of yeast ribosome populations proves the monomeric organization of the eukaryotic ribosomal stalk structure. Mol. Microbiol. 50 (2003) 703-712
16. Hagiya A., et al. A mode of assembly of P0, P1, and P2 proteins at the GTPase-associated center in animal ribosome: in vitro analyses with P0 truncation mutants. J. Biol. Chem. 280 (2005) 39193-39199
17. Ilag L.L., et al. Heptameric (L12)6/L10 rather than canonical pentameric complexes are found by tandem MS of intact ribosomes from thermophilic bacteria. Proc. Natl. Acad. Sci. USA 102 (2005) 8192-8197
18. Kalpaxis D.L., Theos C., Xaplanteri M.A., Dinos G.P., Catsiki A.V., and Leotsinidis M. Biomonitoring of gulf of Patras, N. Peloponnesus, Greece. Application of a biomarker suite including evaluation of translation efficiency in Mytilus galloprovincialis cells. Environ. Res. 94 (2004) 211-222
19. Kondoh N., et al. Identification and characterization of genes associated with human hepatocellular carcinogenesis. Cancer Res. 59 (1999) 4990-4996
20. Koumarianou P., Marcos A.G., Ballesta J.P., and Kouyanou-Koutsoukou S. In vivo analysis of the acidic ribosomal proteins BmP1 and BmP2 of the silkworm Bombyx mori in the yeast Saccharomyces cerevisiae. Gene 388 (2007) 27-33
21. Kouyanou S., Gagou M.E., and Fragoulis E.G. Characterization of acidic ribosomal proteins from three developmental stages of the medfly Ceratitis capitata. Biochem. Mol. Biol. Int. 45 (1998) 623-633
22. Kouyanou S., Santos C., Koliaraki V., and Ballesta J.P. Protein BmP0 from the silkworm Bombyx mori can be assembled and is functional in the Saccharomyces cerevisiae ribosomal stalk in the absence of the acidic P1 and P2 proteins. Gene 18 314 (2003) 173-179
23. Krokowski D., Tchorzewski M., Boguszewska A., and Grankowski N. Acquisition of a stable structure by yeast ribosomal P0 protein requires binding of P1A-P2B complex: in vitro formation of the stalk structure. Biochim. Biophys. Acta 1724 (2005) 59-70
24. Krokowski D., Boguszewska A., Abramczyk D., Liljas A., Tchorzewski M., and Grankowski N. Yeast ribosomal P0 protein has two separate binding sites for P1/P2 proteins. Mol. Microbiol. 60 (2006) 386-400
25. Krokowski D., et al. Elevated copy number of L-A virus in yeast mutant strains defective in ribosomal stalk. Biochem. Biophys. Res. Commun. 355 (2007) 575-580
26. Kucuksezgin F., Kayatekin B.M., Uluturhan E., Uysal N., Acikgoz O., and Gonenc S. Preliminary investigation of sensitive biomarkers of trace metal pollution in mussel (Mytilus galloprovincialis) from Izmir Bay (Turkey). Environ. Monit. Assess. 141 (2008) 339-345
27. Lucas J.M., Vaccaro E., and Waite J.H. A molecular, morphometric and mechanical comparison of the structural elements of byssus from Mytilus edulis and Mytilus galloprovincialis. J. Exp. Biol. 205 (2002) 1807-1817
28. Meggio F., and Pinna L.A. One-thousand-and-one substrates of protein kinase CK2?. FASEB J. 17 (2003) 349-368
29. Montoya-García L., Muñoz-Ocotero V., Aguilar R., and Sánchez de Jiménez E. Regulation of acidic ribosomal protein expression and phosphorylation in maize. Biochemistry 41 (2002) 10166-10172
30. Nover L., Munsche D., Neumann D., Ohme K., and Scharf K.-D. Control of ribosome biosynthesis in plant cell cultures under heat shock conditions. Ribosomal proteins. Biochim. Biophys. Acta 160 (1986) 297-304
31. Pérez-Fernández J., Remacha M., and Ballesta J.P.G. The acidic protein binding site is partially hidden in the free S. cerevisiae ribosomal stalkprotein P0. Biochemistry 44 (2005) 5532-5540
32. Pytharopoulou S., Kouvela E.C., Sazakli E., Leotsinidis M., and Kalpaxis D.L. Evaluation of the global protein synthesis in Mytilus galloprovincialis in marine pollution monitoring: seasonal variability and correlations with other biomarkers. Aquat. Toxicol. 80 (2006) 33-41
33. Sambrook J., Fritsch E.F., and Maniatis T. Molecular Cloning: a Laboratory Manual (1989), Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
34. Sanchez-Madrid F., Reyes R., Conde P., and Ballesta J.P.G. Acidic ribosomal proteins from eukaryotic cells. Effect on ribosomal functions. Eur. J. Biochem. 98 (1979) 409-416
35. Santos C., and Ballesta J.P.G. Ribosomal phosphoprotein P0, contrary to phosphoproteins P1 and P2, is required for S. cerevisiae viability and ribosome assembly. J. Biol. Chem. 269 (1994) 15689-15696
36. Santos C., and Ballesta J.P.G. The highly conserved protein P0 carboxyl end is essential for ribosome activity only in the absence of proteins P1 and P2. J. Biol. Chem. 270 (1995) 20608-20614
37. Santos C., and Ballesta J.P. Characterization of the 26S rRNA-binding domain in Saccharomyces cerevisiae ribosomal stalk phosphoprotein P0. Mol. Microbiol. 58 (2005) 217-226
38. Schmitt J., Hess H., and Stunneberg H.G. Affinity purification of histidine-tagged proteins. Mol. Biol. Rep. 18 (1993) 223-230
39. Stohs S.J., and Bagchi D. Oxidative mechanisms in the toxicity of metal ions. Free Radic. Biol. Med. 18 (1995) 321-336
40. Storey K.B., and Storey J.M. Metabolic rate depression in animals: transcriptional and translational controls. Biol. Rev. Camb. Philos. Soc. 79 (2004) 207-233
41. Szick-Miranda K., and Bailey-Serres J. Regulated heterogeneity in 12-kDa P-protein phosphorylation and composition of ribosomes in maize (Zea mays L.). J. Biol. Chem. 276 (2001) 10921-10928
42. Szyszka R., Bou G., and Ballesta J.P.G. RAP kinase, a new enzyme phosphorylating the acidic P proteins from Saccharomyces cerevisiae. Biochim. Biophys. Acta 1293 (1995) 213-221
43. Torres M.A., et al. Oxidative stress in the mussel Mytella guyanensis from polluted mangroves on Santa Catarina Island, Brazil. Mar. Pollut. Bull. 44 (2002) 923-932
44. Tsurugi K., and Ogata K. Evidence for the exchangeability of acidic ribosomal proteins on cytoplasmic ribosomes in regenerating rat liver. J. Biochem. 98 (1985) 1427-1431
45. Vard C., Guillot D., Bargis P., Lavergne J.P., and Reboud J.P. A specific role for the phosphorylation of mammalian acidic ribosomal protein P2. J. Biol. Chem. 272 (1997) 20259-20262
46. Venier P., Pallavicini A., De Nardi B., and Lanfranchi G. Towards a catalogue of genes transcribed in multiple tissues of Mytilus galloprovincialis. Gene 314 (2003) 29-40
47. Viarengo A., Burlando B., Cavaletto M., Marchi B., Ponzano E., and Blasco J. Role of metallothionein against oxidative stress in the mussel Mytilus galloprovincialis. Am. J. Physiol. 277 (1999) R1612-R1619
48. Vilella M.D., Remacha M., Ortiz B.L., Mendez E., and Ballesta J.P.G. Characterization of the yeast acidic ribosomal phosphoproteins using monoclonal antibodies. Proteins L44/L45 and L44′ have different functional roles. Eur. J. Biochem. 196 (1991) 407-414
49. Wahl M.C., and Moller W. Structure and function of the acidic ribosomal stalk proteins. Curr. Protein Pept. Sci. 3 (2002) 93-106
50. Wool I.G., Chan Y.L., Gluck A., and Suzuki K. The primary structure of rat ribosomal proteins P0, P1 and P2 and a proposal for a uniform nomenclature for mammalian and yeast ribosomal proteins. Biochimie 73 (1991) 861-870
51. Wu S., and Storey K.B. Up-regulation of acidic ribosomal phosphoprotein P0 in response to freezing or anoxia in the freeze tolerant wood frog, Rana sylvatica. Cryobiology 50 (2005) 71-82
52. Zambrano R., Briones E., Remacha M., and Ballesta J.P.G. Phosphorylation of the acidic ribosomal P proteins in Saccharomyces cerevisiae: a reappraisal. Biochemistry 36 (1997) 14439-14446
53. Zielinski R., Pilecki M., Kubinski K., Zien P., Hellman U., and Szyszka R. Inhibition of yeast ribosomal stalk phosphorylation by Cu-Zn superoxide dismutase. Biochem. Biophys. Res. Commun. 296 (2002) 1310-1316
54. Zinker S., and Warner J.R. The ribosomal proteins of Saccharomyces cerevisiae. Phosphorylated and exchangeable proteins. J. Biol. Chem. 251 (1976) 1799-1807