ShyA, a membrane protein for proper septation of hyphae in Streptomyces

Shun-Fu Tseng, Tzu-Wen Huang, Hsiuh-Wei Chen, Ming-Kai Chern, Ming-F. Tam, Shu-Chun Teng

Research output: Contribution to journalArticle

1 Citation (Scopus)

Abstract

The life cycle of Streptomyces involves the formation of filamentous substrate and aerial hyphae. Following cessation of growth of an aerial hypha, multiple septation occurs at the tip to produce a chain of unigenomic spores. A gene, shyA, which influences several aspects of this growth, was isolated and partially characterized in Streptomyces coelicolor. The gene product is a representative of a well-conserved family of small actinomycete proteins. The shyA mutant sporulates normally but displays hyper septum formation and altered spore-chain morphology. Biochemical separation experiments and immunofluorescence staining demonstrated that the shyA gene product locates at cell membranes. Moreover, yeast two-hybrid screen and GST-pull-down assay showed that ShyA can interact with itself. Altogether, ShyA belongs to a new family of membrane-associated proteins which plays a role in morphological differentiation in actinomycetes. © 2006 Elsevier Inc. All rights reserved.
Original languageEnglish
Pages (from-to)369-377
Number of pages9
JournalBiochemical and Biophysical Research Communications
Volume343
Issue number2
DOIs
Publication statusPublished - 2006
Externally publishedYes

Fingerprint

Hyphae
Streptomyces
Membrane Proteins
Actinobacteria
Genes
Spores
Antennas
Streptomyces coelicolor
Cell membranes
Growth
Life Cycle Stages
Yeast
Fluorescent Antibody Technique
Life cycle
Assays
Yeasts
Cell Membrane
Staining and Labeling
Substrates
Proteins

Keywords

  • Actinomycetes
  • Hyphae
  • Membrane protein
  • Spore
  • Streptomyces
  • gene product
  • glutathione transferase
  • membrane protein
  • protein shyA
  • unclassified drug
  • animal cell
  • article
  • cell division
  • cell membrane
  • cell structure
  • chemical analysis
  • enzyme isolation
  • immunofluorescence test
  • nonhuman
  • priority journal
  • protein interaction
  • separation technique
  • Streptomyces coelicolor
  • Amino Acid Sequence
  • Cell Proliferation
  • Cell Size
  • Membrane Proteins
  • Molecular Sequence Data
  • Sequence Homology, Amino Acid
  • Actinobacteria (class)
  • Animalia

Cite this

ShyA, a membrane protein for proper septation of hyphae in Streptomyces. / Tseng, Shun-Fu; Huang, Tzu-Wen; Chen, Hsiuh-Wei; Chern, Ming-Kai; Tam, Ming-F.; Teng, Shu-Chun.

In: Biochemical and Biophysical Research Communications, Vol. 343, No. 2, 2006, p. 369-377.

Research output: Contribution to journalArticle

Tseng, Shun-Fu ; Huang, Tzu-Wen ; Chen, Hsiuh-Wei ; Chern, Ming-Kai ; Tam, Ming-F. ; Teng, Shu-Chun. / ShyA, a membrane protein for proper septation of hyphae in Streptomyces. In: Biochemical and Biophysical Research Communications. 2006 ; Vol. 343, No. 2. pp. 369-377.
@article{6443faacdede4abeb7811dc9ca0a2d4f,
title = "ShyA, a membrane protein for proper septation of hyphae in Streptomyces",
abstract = "The life cycle of Streptomyces involves the formation of filamentous substrate and aerial hyphae. Following cessation of growth of an aerial hypha, multiple septation occurs at the tip to produce a chain of unigenomic spores. A gene, shyA, which influences several aspects of this growth, was isolated and partially characterized in Streptomyces coelicolor. The gene product is a representative of a well-conserved family of small actinomycete proteins. The shyA mutant sporulates normally but displays hyper septum formation and altered spore-chain morphology. Biochemical separation experiments and immunofluorescence staining demonstrated that the shyA gene product locates at cell membranes. Moreover, yeast two-hybrid screen and GST-pull-down assay showed that ShyA can interact with itself. Altogether, ShyA belongs to a new family of membrane-associated proteins which plays a role in morphological differentiation in actinomycetes. {\circledC} 2006 Elsevier Inc. All rights reserved.",
keywords = "Actinomycetes, Hyphae, Membrane protein, Spore, Streptomyces, gene product, glutathione transferase, membrane protein, protein shyA, unclassified drug, animal cell, article, cell division, cell membrane, cell structure, chemical analysis, enzyme isolation, immunofluorescence test, nonhuman, priority journal, protein interaction, separation technique, Streptomyces coelicolor, Amino Acid Sequence, Cell Proliferation, Cell Size, Membrane Proteins, Molecular Sequence Data, Sequence Homology, Amino Acid, Actinobacteria (class), Animalia",
author = "Shun-Fu Tseng and Tzu-Wen Huang and Hsiuh-Wei Chen and Ming-Kai Chern and Ming-F. Tam and Shu-Chun Teng",
note = "Export Date: 13 April 2016 CODEN: BBRCA 通訊地址: Teng, S.-C.; Department of Microbiology, College of Medicine, National Taiwan University, Taipei 10063, Taiwan; 電子郵件: scteng@ha.mc.ntu.edu.tw 化學物質/CAS: glutathione transferase, 50812-37-8; Membrane Proteins 參考文獻: Champness, W., (2000) Actinomycete Development, Antibiotic Production, and Phylogeny: Questions and Challenges, Prokaryotic Development, , American Society for Microbiology Washington, D.C; Chater, K.F., Taking a genetic scalpel to the Streptomyces colony (1998) Microbiology, 144, pp. 1465-1478; Kelemen, G.H., Buttner, M.J., Initiation of aerial mycelium formation in Streptomyces (1998) Curr. Opin. Microbiol., 1, pp. 656-662; Grantcharova, N., Lustig, U., Flardh, K., Dynamics of FtsZ assembly during sporulation in Streptomyces coelicolor A3(2) (2005) J. Bacteriol., 187, pp. 3227-3237; Schwedock, J., McCormick, J.R., Angert, E.R., Nodwell, J.R., Losick, R., Assembly of the cell division protein FtsZ into ladder-like structures in the aerial hyphae of Streptomyces coelicolor (1997) Mol. Microbiol., 25, pp. 847-858; McCormick, J.R., Su, E.P., Driks, A., Losick, R., Growth and viability of Streptomyces coelicolor mutant for the cell division gene ftsZ (1994) Mol. Microbiol., 14, pp. 243-254; Flardh, K., Leibovitz, E., Buttner, M.J., Chater, K.F., Generation of a non-sporulating strain of Streptomyces coelicolor A3(2) by the manipulation of a developmentally controlled ftsZ promoter (2000) Mol. Microbiol., 38, pp. 737-749; Grantcharova, N., Ubhayasekera, W., Mowbray, S.L., McCormick, J.R., Flardh, K., A missense mutation in ftsZ differentially affects vegetative and developmentally controlled cell division in Streptomyces coelicolor A3(2) (2003) Mol. Microbiol., 47, pp. 645-656; Chater, K.F., Regulation of sporulation in Streptomyces coelicolor A3(2): A checkpoint multiplex? (2001) Curr. Opin. Microbiol., 4, pp. 667-673; Wosten, H.A., Willey, J.M., Surface-active proteins enable microbial aerial hyphae to grow into the air (2000) Microbiology, 146, pp. 767-773; Keiser, T., Bibb, M.J., Buttner, M.J., Chater, K.F., Hopwood, D.A., (2000) Practical Streptomyces Genetics, , John Innes Foundation Norwich, United Kingdom; Ausubel, F.M., Brent, R., Kingston, R.E., Moore, D.D., Seidman, J.G., Smith, J.A., Struhl, K., (1998) Current Protocols in Molecular Biology, , John Wiley New Jersey, USA; James, P., Halladay, J., Craig, E.A., Genomic libraries and a host strain designed for highly efficient two-hybrid selection in yeast (1996) Genetics, 144, pp. 1425-1436; Vieira, J., Messing, J., The pUC plasmids, an M13mp7-derived system for insertion mutagenesis and sequencing with synthetic universal primers (1982) Gene, 19, pp. 259-268; Bierman, M., Logan, R., O'Brien, K., Seno, E.T., Rao, R.N., Schoner, B.E., Plasmid cloning vectors for the conjugal transfer of DNA from Escherichia coli to Streptomyces spp (1992) Gene, 116, pp. 43-49; Yeh, H.I., Hsieh, C.H., Wang, L.Y., Tsai, S.P., Hsu, H.Y., Tam, M.F., Mass spectrometric analysis of rat liver cytosolic glutathione S-transferases: Modifications are limited to N-terminal processing (1995) Biochem. J., 308, pp. 69-75; Meijer, W.J., Serna-Rico, A., Salas, M., Characterization of the bacteriophage phi29-encoded protein p16.7: A membrane protein involved in phage DNA replication (2001) Mol. Microbiol., 39, pp. 731-746; Lin, Y.S., Kieser, H.M., Hopwood, D.A., Chen, C.W., The chromosomal DNA of Streptomyces lividans 66 is linear (1993) Mol. Microbiol., 10, pp. 923-933; Huang, C.H., Lin, Y.S., Yang, Y.L., Huang, S.W., Chen, C.W., The telomeres of Streptomyces chromosomes contain conserved palindromic sequences with potential to form complex secondary structures (1998) Mol. Microbiol., 28, pp. 905-916; Bao, K., Cohen, S.N., Terminal proteins essential for the replication of linear plasmids and chromosomes in Streptomyces (2001) Genes. Dev., 15, pp. 1518-1527; Yang, C.C., Huang, C.H., Li, C.Y., Tsay, Y.G., Lee, S.C., Chen, C.W., The terminal proteins of linear Streptomyces chromosomes and plasmids: A novel class of replication priming proteins (2002) Mol. Microbiol., 43, pp. 297-305; Bentley, S.D., Chater, K.F., Cerdeno-Tarraga, A.M., Challis, G.L., Thomson, N.R., James, K.D., Harris, D.E., Hopwood, D.A., Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2) (2002) Nature, 417, pp. 141-147; Hesketh, A.R., Chandra, G., Shaw, A.D., Rowland, J.J., Kell, D.B., Bibb, M.J., Chater, K.F., Primary and secondary metabolism, and post-translational protein modifications, as portrayed by proteomic analysis of Streptomyces coelicolor (2002) Mol. Microbiol., 46, pp. 917-932; Flardh, K., Growth polarity and cell division in Streptomyces (2003) Curr. Opin. Microbiol., 6, pp. 564-571",
year = "2006",
doi = "10.1016/j.bbrc.2006.02.178",
language = "English",
volume = "343",
pages = "369--377",
journal = "Biochemical and Biophysical Research Communications",
issn = "0006-291X",
publisher = "Elsevier B.V.",
number = "2",

}

TY - JOUR

T1 - ShyA, a membrane protein for proper septation of hyphae in Streptomyces

AU - Tseng, Shun-Fu

AU - Huang, Tzu-Wen

AU - Chen, Hsiuh-Wei

AU - Chern, Ming-Kai

AU - Tam, Ming-F.

AU - Teng, Shu-Chun

N1 - Export Date: 13 April 2016 CODEN: BBRCA 通訊地址: Teng, S.-C.; Department of Microbiology, College of Medicine, National Taiwan University, Taipei 10063, Taiwan; 電子郵件: scteng@ha.mc.ntu.edu.tw 化學物質/CAS: glutathione transferase, 50812-37-8; Membrane Proteins 參考文獻: Champness, W., (2000) Actinomycete Development, Antibiotic Production, and Phylogeny: Questions and Challenges, Prokaryotic Development, , American Society for Microbiology Washington, D.C; Chater, K.F., Taking a genetic scalpel to the Streptomyces colony (1998) Microbiology, 144, pp. 1465-1478; Kelemen, G.H., Buttner, M.J., Initiation of aerial mycelium formation in Streptomyces (1998) Curr. Opin. Microbiol., 1, pp. 656-662; Grantcharova, N., Lustig, U., Flardh, K., Dynamics of FtsZ assembly during sporulation in Streptomyces coelicolor A3(2) (2005) J. Bacteriol., 187, pp. 3227-3237; Schwedock, J., McCormick, J.R., Angert, E.R., Nodwell, J.R., Losick, R., Assembly of the cell division protein FtsZ into ladder-like structures in the aerial hyphae of Streptomyces coelicolor (1997) Mol. Microbiol., 25, pp. 847-858; McCormick, J.R., Su, E.P., Driks, A., Losick, R., Growth and viability of Streptomyces coelicolor mutant for the cell division gene ftsZ (1994) Mol. Microbiol., 14, pp. 243-254; Flardh, K., Leibovitz, E., Buttner, M.J., Chater, K.F., Generation of a non-sporulating strain of Streptomyces coelicolor A3(2) by the manipulation of a developmentally controlled ftsZ promoter (2000) Mol. Microbiol., 38, pp. 737-749; Grantcharova, N., Ubhayasekera, W., Mowbray, S.L., McCormick, J.R., Flardh, K., A missense mutation in ftsZ differentially affects vegetative and developmentally controlled cell division in Streptomyces coelicolor A3(2) (2003) Mol. Microbiol., 47, pp. 645-656; Chater, K.F., Regulation of sporulation in Streptomyces coelicolor A3(2): A checkpoint multiplex? (2001) Curr. Opin. Microbiol., 4, pp. 667-673; Wosten, H.A., Willey, J.M., Surface-active proteins enable microbial aerial hyphae to grow into the air (2000) Microbiology, 146, pp. 767-773; Keiser, T., Bibb, M.J., Buttner, M.J., Chater, K.F., Hopwood, D.A., (2000) Practical Streptomyces Genetics, , John Innes Foundation Norwich, United Kingdom; Ausubel, F.M., Brent, R., Kingston, R.E., Moore, D.D., Seidman, J.G., Smith, J.A., Struhl, K., (1998) Current Protocols in Molecular Biology, , John Wiley New Jersey, USA; James, P., Halladay, J., Craig, E.A., Genomic libraries and a host strain designed for highly efficient two-hybrid selection in yeast (1996) Genetics, 144, pp. 1425-1436; Vieira, J., Messing, J., The pUC plasmids, an M13mp7-derived system for insertion mutagenesis and sequencing with synthetic universal primers (1982) Gene, 19, pp. 259-268; Bierman, M., Logan, R., O'Brien, K., Seno, E.T., Rao, R.N., Schoner, B.E., Plasmid cloning vectors for the conjugal transfer of DNA from Escherichia coli to Streptomyces spp (1992) Gene, 116, pp. 43-49; Yeh, H.I., Hsieh, C.H., Wang, L.Y., Tsai, S.P., Hsu, H.Y., Tam, M.F., Mass spectrometric analysis of rat liver cytosolic glutathione S-transferases: Modifications are limited to N-terminal processing (1995) Biochem. J., 308, pp. 69-75; Meijer, W.J., Serna-Rico, A., Salas, M., Characterization of the bacteriophage phi29-encoded protein p16.7: A membrane protein involved in phage DNA replication (2001) Mol. Microbiol., 39, pp. 731-746; Lin, Y.S., Kieser, H.M., Hopwood, D.A., Chen, C.W., The chromosomal DNA of Streptomyces lividans 66 is linear (1993) Mol. Microbiol., 10, pp. 923-933; Huang, C.H., Lin, Y.S., Yang, Y.L., Huang, S.W., Chen, C.W., The telomeres of Streptomyces chromosomes contain conserved palindromic sequences with potential to form complex secondary structures (1998) Mol. Microbiol., 28, pp. 905-916; Bao, K., Cohen, S.N., Terminal proteins essential for the replication of linear plasmids and chromosomes in Streptomyces (2001) Genes. Dev., 15, pp. 1518-1527; Yang, C.C., Huang, C.H., Li, C.Y., Tsay, Y.G., Lee, S.C., Chen, C.W., The terminal proteins of linear Streptomyces chromosomes and plasmids: A novel class of replication priming proteins (2002) Mol. Microbiol., 43, pp. 297-305; Bentley, S.D., Chater, K.F., Cerdeno-Tarraga, A.M., Challis, G.L., Thomson, N.R., James, K.D., Harris, D.E., Hopwood, D.A., Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2) (2002) Nature, 417, pp. 141-147; Hesketh, A.R., Chandra, G., Shaw, A.D., Rowland, J.J., Kell, D.B., Bibb, M.J., Chater, K.F., Primary and secondary metabolism, and post-translational protein modifications, as portrayed by proteomic analysis of Streptomyces coelicolor (2002) Mol. Microbiol., 46, pp. 917-932; Flardh, K., Growth polarity and cell division in Streptomyces (2003) Curr. Opin. Microbiol., 6, pp. 564-571

PY - 2006

Y1 - 2006

N2 - The life cycle of Streptomyces involves the formation of filamentous substrate and aerial hyphae. Following cessation of growth of an aerial hypha, multiple septation occurs at the tip to produce a chain of unigenomic spores. A gene, shyA, which influences several aspects of this growth, was isolated and partially characterized in Streptomyces coelicolor. The gene product is a representative of a well-conserved family of small actinomycete proteins. The shyA mutant sporulates normally but displays hyper septum formation and altered spore-chain morphology. Biochemical separation experiments and immunofluorescence staining demonstrated that the shyA gene product locates at cell membranes. Moreover, yeast two-hybrid screen and GST-pull-down assay showed that ShyA can interact with itself. Altogether, ShyA belongs to a new family of membrane-associated proteins which plays a role in morphological differentiation in actinomycetes. © 2006 Elsevier Inc. All rights reserved.

AB - The life cycle of Streptomyces involves the formation of filamentous substrate and aerial hyphae. Following cessation of growth of an aerial hypha, multiple septation occurs at the tip to produce a chain of unigenomic spores. A gene, shyA, which influences several aspects of this growth, was isolated and partially characterized in Streptomyces coelicolor. The gene product is a representative of a well-conserved family of small actinomycete proteins. The shyA mutant sporulates normally but displays hyper septum formation and altered spore-chain morphology. Biochemical separation experiments and immunofluorescence staining demonstrated that the shyA gene product locates at cell membranes. Moreover, yeast two-hybrid screen and GST-pull-down assay showed that ShyA can interact with itself. Altogether, ShyA belongs to a new family of membrane-associated proteins which plays a role in morphological differentiation in actinomycetes. © 2006 Elsevier Inc. All rights reserved.

KW - Actinomycetes

KW - Hyphae

KW - Membrane protein

KW - Spore

KW - Streptomyces

KW - gene product

KW - glutathione transferase

KW - membrane protein

KW - protein shyA

KW - unclassified drug

KW - animal cell

KW - article

KW - cell division

KW - cell membrane

KW - cell structure

KW - chemical analysis

KW - enzyme isolation

KW - immunofluorescence test

KW - nonhuman

KW - priority journal

KW - protein interaction

KW - separation technique

KW - Streptomyces coelicolor

KW - Amino Acid Sequence

KW - Cell Proliferation

KW - Cell Size

KW - Membrane Proteins

KW - Molecular Sequence Data

KW - Sequence Homology, Amino Acid

KW - Actinobacteria (class)

KW - Animalia

U2 - 10.1016/j.bbrc.2006.02.178

DO - 10.1016/j.bbrc.2006.02.178

M3 - Article

VL - 343

SP - 369

EP - 377

JO - Biochemical and Biophysical Research Communications

JF - Biochemical and Biophysical Research Communications

SN - 0006-291X

IS - 2

ER -