Cold‐shock induction of a family of TIP1‐related proteins associated with the membrane in Saccharomyces cerevisiae

TIP1 is the first known cold‐shock‐and heat‐shock‐induced gene in Saccharomyces cerevisiae. Here it is demonstrated that a TIP1 homologue, TIR1, which had been previously cloned as SRP1 (serine‐rich protein), is strongly induced by a downshift in growth temperature from 30 to 10°C. We further cloned TIR2, which is transcribed at a low basal level but is increased strongly by cold shock and, to a lesser extent, by heat shock. The predicted protein sequence of TIR2 demonstrates remarkable homology to T1R1 (72.2%) and is also homologous with TIP1 (49%). TIP1, TIR1 and TIR2 are rich in both serine and alanine residues and each contains serine‐rich tandem repeats. The proteins contain putative N‐terminal signal peptides as well as hydro‐phobic C‐terminal sequences, indicating that the proteins may be membrane bound. The predicted protein sequences are also consistent with extensive O‐mannosylation as well as glycosyl‐phosphatidyl inositol (GPI) membrane anchoring. Cell fractionation analysis as well as studies using a yeast strain that is conditionally deficient in glycosylation demonstrate that TIP1 is a heavily modified membrane‐associated protein. Single, double combinations and triple mutants were created and none demonstrated any obvious phenotype, indicating that this family of genes is not essential for normal growth.

[1]  D. Baltimore,et al.  RAG-1 interacts with the repeated amino acid motif of the human homologue of the yeast protein SRP1. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[2]  M. Inouye,et al.  The cold‐shock response — a hot topic , 1994, Molecular microbiology.

[3]  M. Inouye,et al.  Family of the major cold‐shock protein, CspA (CS7.4), of Escherichia coli, whose members show a high sequence similarity with the eukaryotic Y‐box binding proteins , 1994, Molecular microbiology.

[4]  M. Inouye,et al.  Chloramphenicol induces the transcription of the major cold shock gene of Escherichia coli, cspA , 1993, Journal of bacteriology.

[5]  M. Czisch,et al.  Structure in solution of the major cold-shock protein from Bacillus subtilis , 1993, Nature.

[6]  Hermann Schindelin,et al.  Universal nucleic acid-binding domain revealed by crystal structure of the B. subtilis major cold-shock protein , 1993, Nature.

[7]  Y. Matsui,et al.  Three yeast genes, PIR1, PIR2 and PIR3, containing internal tandem repeats, are related to each other, and PIR1 and PIR2 are required for tolerance to heat shock , 1993, Yeast.

[8]  M. Nomura,et al.  Cloning and characterization of SRP1, a suppressor of temperature-sensitive RNA polymerase I mutations, in Saccharomyces cerevisiae , 1992, Molecular and cellular biology.

[9]  M. Marahiel,et al.  Characterization of cspB, a Bacillus subtilis inducible cold shock gene affecting cell viability at low temperatures , 1992, Journal of bacteriology.

[10]  N. Kalkkinen,et al.  A heat shock gene from Saccharomyces cerevisiae encoding a secretory glycoprotein. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[11]  T. Mélèse,et al.  NSR1 is required for pre-rRNA processing and for the proper maintenance of steady-state levels of ribosomal subunits , 1992, Molecular and cellular biology.

[12]  H. Antoun,et al.  Heat and cold shock protein synthesis in arctic and temperate strains of rhizobia , 1992, Applied and environmental microbiology.

[13]  M. Inouye,et al.  Cold shock induction of yeast NSR1 protein and its role in pre-rRNA processing. , 1992, The Journal of biological chemistry.

[14]  M. Inouye,et al.  Yeast NSR1 protein that has structural similarity to mammalian nucleolin is involved in pre-rRNA processing. , 1992, The Journal of biological chemistry.

[15]  S. Kaul,et al.  Cold shock response of yeast cells: induction of a 33 kDa protein and protection against freezing injury. , 1992, Cellular and molecular biology.

[16]  S Udenfriend,et al.  Phosphatidylinositol glycan (PI-G) anchored membrane proteins. Amino acid requirements adjacent to the site of cleavage and PI-G attachment in the COOH-terminal signal peptide. , 1992, The Journal of biological chemistry.

[17]  M. Inouye,et al.  Identification of the promoter region of the Escherichia coli major cold shock gene, cspA , 1992, Journal of bacteriology.

[18]  E. Breierová,et al.  Cryoprotective effects of yeast extracellular polysaccharides and glycoproteins. , 1992, Cryobiology.

[19]  N. Kalkkinen,et al.  A heat shock gene from Saccharomyces cerevisiae encoding a secretory glycoprotein. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[20]  S. Kaul,et al.  Cryoprotection provided by heat shock treatment in Saccharomyces cerevisiae. , 1992, Cellular and molecular biology.

[21]  P. Robbins,et al.  Chitinase is required for cell separation during growth of Saccharomyces cerevisiae. , 1991, The Journal of biological chemistry.

[22]  M. Inouye,et al.  TIP 1, a cold shock-inducible gene of Saccharomyces cerevisiae. , 1991, The Journal of biological chemistry.

[23]  Gene expression during cold and heat shock in wheat. , 1991, Biochemistry and cell biology = Biochimie et biologie cellulaire.

[24]  Z. Xue,et al.  The NSR1 gene encodes a protein that specifically binds nuclear localization sequences and has two RNA recognition motifs , 1991, The Journal of cell biology.

[25]  F. Sherman Getting started with yeast. , 1991, Methods in enzymology.

[26]  P. Orlean Dolichol phosphate mannose synthase is required in vivo for glycosyl phosphatidylinositol membrane anchoring, O mannosylation, and N glycosylation of protein in Saccharomyces cerevisiae , 1990, Molecular and cellular biology.

[27]  W. E. Inniss,et al.  Induction of protein synthesis in response to cold shock in the psychrotrophic yeast Trichosporon pullulans , 1990 .

[28]  G. Vonheijne The signal peptide. , 1990 .

[29]  M. Inouye,et al.  Major cold shock protein of Escherichia coli. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[30]  M. G. Low The glycosyl-phosphatidylinositol anchor of membrane proteins. , 1989, Biochimica et biophysica acta.

[31]  K. Hauser,et al.  Purification of the inducible α‐agglutinin of S. cerevisiae and molecular cloning of the gene , 1989 .

[32]  R. Sikorski,et al.  A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. , 1989, Genetics.

[33]  B. Dobberstein,et al.  A tripartite structure of the signals that determine protein insertion into the endoplasmic reticulum membrane , 1989, The Journal of cell biology.

[34]  G. Salerno,et al.  Raffinose Synthesis in Chlorella vulgaris Cultures after a Cold Shock. , 1989, Plant physiology.

[35]  D. Marguet,et al.  Yeast gene SRP1 (serine-rich protein). Intragenic repeat structure and identification of a family of SRP1-related DNA sequences. , 1988, Journal of molecular biology.

[36]  D. Marguet,et al.  Gene cloning from yeast chromosome‐specific mini‐library Isolation of the SRP1 ‐related DNA sequence located on chromosome XV , 1988, FEBS letters.

[37]  R. Schekman,et al.  The yeast SEC53 gene encodes phosphomannomutase. , 1988, The Journal of biological chemistry.

[38]  M. Maniak,et al.  A developmentally regulated membrane protein gene in Dictyostelium discoideum is also induced by heat shock and cold shock , 1988, Molecular and cellular biology.

[39]  M. Ferguson,et al.  Cell-surface anchoring of proteins via glycosyl-phosphatidylinositol structures. , 1988, Annual review of biochemistry.

[40]  F. Neidhardt,et al.  Induction of proteins in response to low temperature in Escherichia coli , 1987, Journal of bacteriology.

[41]  C. Watanabe,et al.  Compilation and comparison of the sequence context around the AUG startcodons in Saccharomyces cerevisiae mRNAs. , 1987, Nucleic acids research.

[42]  A. Müller-Taubenberger,et al.  Transcript regulation and carboxyterminal extension of ubiquitin in Dictyostelium discoideum , 1986 .

[43]  K. Murata,et al.  Transformation of intact yeast cells treated with alkali cations , 1983 .

[44]  J. Vieira,et al.  The pUC plasmids, an M13mp7-derived system for insertion mutagenesis and sequencing with synthetic universal primers. , 1982, Gene.

[45]  F. Sherman,et al.  DNA sequence required for efficient transcription termination in yeast , 1982, Cell.

[46]  F. Sanger,et al.  DNA sequencing with chain-terminating inhibitors. , 1977, Proceedings of the National Academy of Sciences of the United States of America.