DOI: 10.1002/pmic.200600883. Genome‐wide transcriptomic and proteomic analysis of the primary response to phosphate limitation in Streptomyces coelicolor M145 and in a ΔphoP mutant

Genome‐wide transcriptomic and proteomic analysis of the primary response to phosphate limitation in Streptomyces coelicolor M145 and in a ΔphoP mutant

10.1002/pmic.200600883

Crossref journal-article

Wiley

PROTEOMICS (311)

Abstract

AbstractPhosphate limitation in Streptomyces and in other bacteria triggers expression changes of a large number of genes. This response is mediated by the two‐component PhoR–PhoP system. A Streptomyces coelicolor ΔphoP mutant (lacking phoP) has been obtained by gene replacement. A genome‐wide analysis of the primary response to phosphate limitation using transcriptomic and proteomic studies has been made in the parental S. coelicolor M145 and in the ΔphoP mutant strains. Statistical analysis of the contrasts between the four sets of data generated (two strains under two phosphate conditions) allowed the classification of all genes into 12 types of profiles. The primary response to phosphate limitation involves upregulation of genes encoding scavenging enzymes needed to obtain phosphate from different phosphorylated organic compounds and overexpression of the high‐affinity phosphate transport system pstSCAB. Clear interactions have been found between phosphate metabolism and expression of nitrogen‐regulated genes and between phosphate and nitrate respiration genes. PhoP‐dependent repressions of antibiotic biosynthesis and of the morphological differentiation genes correlated with the observed ΔphoP mutant phenotype. Bioinformatic analysis of the presence of PHO boxes (PhoP‐binding sequences) in the upstream regions of PhoP‐controlled genes were validated by binding of PhoP, as shown by electrophoretic mobility shift assays.

Bibliography

RodrÃguezâGarcÃa, A., Barreiro, C., SantosâBeneit, F., SolaâLanda, A., & MartÃn, J. F. (2007). Genomeâwide transcriptomic and proteomic analysis of the primary response to phosphate limitation in Streptomyces coelicolor M145 and in a ÎphoP mutant. PROTEOMICS, 7(14), 2410â2429. Portico.

Authors 5

Antonio Rodríguez‐García (first)
Carlos Barreiro (additional)
Fernando Santos‐Beneit (additional)
Alberto Sola‐Landa (additional)
Juan F. Martín (additional)

References 82 Referenced 110

10.1002/bies.950120804
{'key': 'e_1_2_1_3_2', 'first-page': '1374', 'article-title': 'The signal‐transduction network for Pho regulation in Bacillus subtilis', 'volume': '178', 'author': 'Hulett F. M.', 'year': '1996', 'journal-title': 'J. Bacteriol.'} / J. Bacteriol. / The signal‐transduction network for Pho regulation in Bacillus subtilis by Hulett F. M. (1996)
10.1128/JB.178.15.4344-4366.1996
10.1128/JB.182.16.4478-4490.2000
{'key': 'e_1_2_1_6_2', 'first-page': '1', 'volume-title': 'Phosphate in Microorganisms: Cellular and Molecular Biology', 'author': 'Torriani‐Gorini A.', 'year': '1994'} / Phosphate in Microorganisms: Cellular and Molecular Biology by Torriani‐Gorini A. (1994)
{'key': 'e_1_2_1_7_2', 'first-page': '140', 'volume-title': 'Phosphate in Microorganisms: Cellular and Molecular Biology', 'author': 'Martín J. F.', 'year': '1994'} / Phosphate in Microorganisms: Cellular and Molecular Biology by Martín J. F. (1994)
10.1139/m85-053
10.1007/BF00903781
10.1099/00221287-136-11-2291
10.1128/jb.174.5.1487-1494.1992
10.1007/s002530050671
10.1073/pnas.1934677100
10.1046/j.1365-2958.2003.03529.x
10.1016/0378-1119(90)90139-I
10.1073/pnas.0931429100
10.1128/JB.188.2.677-686.2006
10.1111/j.1365-2958.2005.04631.x
10.1046/j.1365-2958.1998.01122.x
10.1128/JB.185.15.4519-4529.2003
10.1007/s00438-004-1030-8
10.1046/j.1365-2958.2002.03219.x
10.1002/pmic.200500842
{'key': 'e_1_2_1_24_2', 'volume-title': 'Practical Streptomyces genetics', 'author': 'Kieser T.', 'year': '2000'} / Practical Streptomyces genetics by Kieser T. (2000)
10.7164/antibiotics.27.298
10.1093/nar/gni086
10.1073/pnas.0337542100
10.1046/j.1365-2958.1996.6191336.x
10.1111/j.1574-6968.1989.tb03671.x
10.1042/bj0620315
10.1016/0003-2697(79)90115-5
10.1111/j.1742-4658.2004.04509.x
10.1002/(SICI)1522-2683(19991201)20:18<3551::AID-ELPS3551>3.0.CO;2-2
10.1007/s10295-005-0034-7
10.1093/nar/gkh870
{'key': 'e_1_2_1_36_2', 'volume-title': 'R: A language and environment for statistical computing', 'author': 'R Development Core Team', 'year': '2006'} / R: A language and environment for statistical computing by R Development Core Team (2006)
10.2202/1544-6115.1027
10.1016/S1046-2023(03)00155-5
10.1093/bioinformatics/bti270
10.1186/1471-2105-7-261
10.1016/j.febslet.2004.07.055
10.1186/1471-2105-6-181
10.1016/S0076-6879(96)74036-3
10.1006/jtbi.1997.0540
10.1093/nar/gkg567
10.1099/mic.0.27983-0
10.1146/annurev.mi.43.100189.001453
10.1093/nar/gnf103
10.1042/BST0330210
10.1099/mic.0.28383-0
10.1128/AEM.71.5.2391-2402.2005
10.1046/j.1365-2958.1998.00700.x
10.1128/JB.180.3.753-758.1998 / J. Bacteriol. / Analysis of Bacillus subtilis tagAB and tagDEF expression during phosphate starvation identifies a repressor role for PhoP˜P by Liu W. (1998)
10.1099/00221287-147-9-2447
10.1128/JB.187.18.6253-6254.2005
10.1007/s002030100321
10.1046/j.1365-2958.2001.02303.x
10.1128/JB.186.21.7364-7368.2004
10.1111/j.1365-2958.2005.04874.x
10.1074/jbc.M006079200
10.1093/emboj/cdg215
10.1046/j.1365-2958.2002.03150.x
10.1128/jb.173.22.7351-7360.1991
10.1016/0378-1119(93)90359-B
10.1038/417141a
10.1128/JB.183.20.5991-5996.2001
10.1101/gad.264403
10.1021/ja065247w
10.1007/s00203-006-0176-7
10.1002/1522-2683(200112)22:20<4404::AID-ELPS4404>3.0.CO;2-2
10.1007/s10295-003-0067-8
10.1016/S0022-2836(02)01280-9
10.1128/AAC.30.1.127
10.1128/JB.185.18.5442-5451.2003
10.1002/pmic.200300412
10.1093/nar/gkj149
10.1186/1471-2180-3-3
10.1002/9783527620890.ch2
10.1016/0167-7799(90)90170-3
10.1128/JB.00202-06
10.1128/JB.186.24.8424-8432.2004
10.1101/gad.943401
10.1128/JB.186.16.5197-5201.2004

Dates

Type	When
Created	18 years, 1 month ago (July 10, 2007, 9:54 a.m.)
Deposited	1 year, 9 months ago (Nov. 15, 2023, 6:46 a.m.)
Indexed	1 year ago (Aug. 15, 2024, 11:49 a.m.)
Issued	18 years, 2 months ago (July 1, 2007)
Published	18 years, 2 months ago (July 1, 2007)
Published Online	18 years, 1 month ago (July 10, 2007)
Published Print	18 years, 2 months ago (July 1, 2007)

Funders 0

None

BibTeX

@article{Rodr_guez_Garc_a_2007, title={Genome‐wide transcriptomic and proteomic analysis of the primary response to phosphate limitation in Streptomyces coelicolor M145 and in a ΔphoP mutant}, volume={7}, ISSN={1615-9861}, url={http://dx.doi.org/10.1002/pmic.200600883}, DOI={10.1002/pmic.200600883}, number={14}, journal={PROTEOMICS}, publisher={Wiley}, author={Rodríguez‐García, Antonio and Barreiro, Carlos and Santos‐Beneit, Fernando and Sola‐Landa, Alberto and Martín, Juan F.}, year={2007}, month=jul, pages={2410–2429} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2024,
        8,
        15
      ]
    ],
    "date-time": "2024-08-15T15:49:17Z",
    "timestamp": 1723736957551
  },
  "reference-count": 82,
  "publisher": "Wiley",
  "issue": "14",
  "license": [
    {
      "start": {
        "date-parts": [
          [
            2007,
            7,
            10
          ]
        ],
        "date-time": "2007-07-10T00:00:00Z",
        "timestamp": 1184025600000
      },
      "content-version": "vor",
      "delay-in-days": 9,
      "URL": "http://onlinelibrary.wiley.com/termsAndConditions#vor"
    }
  ],
  "content-domain": {
    "domain": [
      "analyticalsciencejournals.onlinelibrary.wiley.com"
    ],
    "crossmark-restriction": true
  },
  "published-print": {
    "date-parts": [
      [
        2007,
        7
      ]
    ]
  },
  "abstract": "<jats:title>Abstract</jats:title><jats:p>Phosphate limitation in <jats:italic>Streptomyces</jats:italic> and in other bacteria triggers expression changes of a large number of genes. This response is mediated by the two\u2010component PhoR\u2013PhoP system. A <jats:italic>Streptomyces coelicolor \u0394phoP</jats:italic> mutant (lacking <jats:italic>phoP</jats:italic>) has been obtained by gene replacement. A genome\u2010wide analysis of the primary response to phosphate limitation using transcriptomic and proteomic studies has been made in the parental <jats:italic>S. coelicolor</jats:italic> M145 and in the \u0394<jats:italic>phoP</jats:italic> mutant strains. Statistical analysis of the contrasts between the four sets of data generated (two strains under two phosphate conditions) allowed the classification of all genes into 12 types of profiles. The primary response to phosphate limitation involves upregulation of genes encoding scavenging enzymes needed to obtain phosphate from different phosphorylated organic compounds and overexpression of the high\u2010affinity phosphate transport system <jats:italic>pstSCAB</jats:italic>. Clear interactions have been found between phosphate metabolism and expression of nitrogen\u2010regulated genes and between phosphate and nitrate respiration genes. PhoP\u2010dependent repressions of antibiotic biosynthesis and of the morphological differentiation genes correlated with the observed \u0394<jats:italic>phoP</jats:italic> mutant phenotype. Bioinformatic analysis of the presence of PHO boxes (PhoP\u2010binding sequences) in the upstream regions of PhoP\u2010controlled genes were validated by binding of PhoP, as shown by electrophoretic mobility shift assays.</jats:p>",
  "DOI": "10.1002/pmic.200600883",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2007,
        7,
        10
      ]
    ],
    "date-time": "2007-07-10T13:54:26Z",
    "timestamp": 1184075666000
  },
  "page": "2410-2429",
  "update-policy": "http://dx.doi.org/10.1002/crossmark_policy",
  "source": "Crossref",
  "is-referenced-by-count": 110,
  "title": "Genome\u2010wide transcriptomic and proteomic analysis of the primary response to phosphate limitation in <b><i>Streptomyces coelicolor</i></b> M145 and in a \u0394<b><i>phoP</i></b> mutant",
  "prefix": "10.1002",
  "volume": "7",
  "author": [
    {
      "given": "Antonio",
      "family": "Rodr\u00edguez\u2010Garc\u00eda",
      "sequence": "first",
      "affiliation": []
    },
    {
      "given": "Carlos",
      "family": "Barreiro",
      "sequence": "additional",
      "affiliation": []
    },
    {
      "given": "Fernando",
      "family": "Santos\u2010Beneit",
      "sequence": "additional",
      "affiliation": []
    },
    {
      "given": "Alberto",
      "family": "Sola\u2010Landa",
      "sequence": "additional",
      "affiliation": []
    },
    {
      "given": "Juan F.",
      "family": "Mart\u00edn",
      "sequence": "additional",
      "affiliation": []
    }
  ],
  "member": "311",
  "published-online": {
    "date-parts": [
      [
        2007,
        7,
        10
      ]
    ]
  },
  "reference": [
    {
      "key": "e_1_2_1_2_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/bies.950120804"
    },
    {
      "key": "e_1_2_1_3_2",
      "first-page": "1374",
      "article-title": "The signal\u2010transduction network for Pho regulation in Bacillus subtilis",
      "volume": "178",
      "author": "Hulett F. M.",
      "year": "1996",
      "journal-title": "J. Bacteriol."
    },
    {
      "key": "e_1_2_1_4_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/JB.178.15.4344-4366.1996"
    },
    {
      "key": "e_1_2_1_5_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/JB.182.16.4478-4490.2000"
    },
    {
      "key": "e_1_2_1_6_2",
      "first-page": "1",
      "volume-title": "Phosphate in Microorganisms: Cellular and Molecular Biology",
      "author": "Torriani\u2010Gorini A.",
      "year": "1994"
    },
    {
      "key": "e_1_2_1_7_2",
      "first-page": "140",
      "volume-title": "Phosphate in Microorganisms: Cellular and Molecular Biology",
      "author": "Mart\u00edn J. F.",
      "year": "1994"
    },
    {
      "key": "e_1_2_1_8_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1139/m85-053"
    },
    {
      "key": "e_1_2_1_9_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/BF00903781"
    },
    {
      "key": "e_1_2_1_10_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1099/00221287-136-11-2291"
    },
    {
      "key": "e_1_2_1_11_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jb.174.5.1487-1494.1992"
    },
    {
      "key": "e_1_2_1_12_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/s002530050671"
    },
    {
      "key": "e_1_2_1_13_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.1934677100"
    },
    {
      "key": "e_1_2_1_14_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1046/j.1365-2958.2003.03529.x"
    },
    {
      "key": "e_1_2_1_15_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0378-1119(90)90139-I"
    },
    {
      "key": "e_1_2_1_16_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.0931429100"
    },
    {
      "key": "e_1_2_1_17_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/JB.188.2.677-686.2006"
    },
    {
      "key": "e_1_2_1_18_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1365-2958.2005.04631.x"
    },
    {
      "key": "e_1_2_1_19_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1046/j.1365-2958.1998.01122.x"
    },
    {
      "key": "e_1_2_1_20_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/JB.185.15.4519-4529.2003"
    },
    {
      "key": "e_1_2_1_21_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/s00438-004-1030-8"
    },
    {
      "key": "e_1_2_1_22_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1046/j.1365-2958.2002.03219.x"
    },
    {
      "key": "e_1_2_1_23_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/pmic.200500842"
    },
    {
      "key": "e_1_2_1_24_2",
      "volume-title": "Practical Streptomyces genetics",
      "author": "Kieser T.",
      "year": "2000"
    },
    {
      "key": "e_1_2_1_25_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.7164/antibiotics.27.298"
    },
    {
      "key": "e_1_2_1_26_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/nar/gni086"
    },
    {
      "key": "e_1_2_1_27_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.0337542100"
    },
    {
      "key": "e_1_2_1_28_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1046/j.1365-2958.1996.6191336.x"
    },
    {
      "key": "e_1_2_1_29_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1574-6968.1989.tb03671.x"
    },
    {
      "key": "e_1_2_1_30_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1042/bj0620315"
    },
    {
      "key": "e_1_2_1_31_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0003-2697(79)90115-5"
    },
    {
      "key": "e_1_2_1_32_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1742-4658.2004.04509.x"
    },
    {
      "key": "e_1_2_1_33_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/(SICI)1522-2683(19991201)20:18<3551::AID-ELPS3551>3.0.CO;2-2"
    },
    {
      "key": "e_1_2_1_34_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/s10295-005-0034-7"
    },
    {
      "key": "e_1_2_1_35_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/nar/gkh870"
    },
    {
      "key": "e_1_2_1_36_2",
      "volume-title": "R: A language and environment for statistical computing",
      "author": "R Development Core Team",
      "year": "2006"
    },
    {
      "key": "e_1_2_1_37_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.2202/1544-6115.1027"
    },
    {
      "key": "e_1_2_1_38_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S1046-2023(03)00155-5"
    },
    {
      "key": "e_1_2_1_39_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/bioinformatics/bti270"
    },
    {
      "key": "e_1_2_1_40_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1186/1471-2105-7-261"
    },
    {
      "key": "e_1_2_1_41_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/j.febslet.2004.07.055"
    },
    {
      "key": "e_1_2_1_42_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1186/1471-2105-6-181"
    },
    {
      "key": "e_1_2_1_43_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0076-6879(96)74036-3"
    },
    {
      "key": "e_1_2_1_44_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1006/jtbi.1997.0540"
    },
    {
      "key": "e_1_2_1_45_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/nar/gkg567"
    },
    {
      "key": "e_1_2_1_46_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1099/mic.0.27983-0"
    },
    {
      "key": "e_1_2_1_47_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1146/annurev.mi.43.100189.001453"
    },
    {
      "key": "e_1_2_1_48_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/nar/gnf103"
    },
    {
      "key": "e_1_2_1_49_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1042/BST0330210"
    },
    {
      "key": "e_1_2_1_50_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1099/mic.0.28383-0"
    },
    {
      "key": "e_1_2_1_51_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/AEM.71.5.2391-2402.2005"
    },
    {
      "key": "e_1_2_1_52_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1046/j.1365-2958.1998.00700.x"
    },
    {
      "key": "e_1_2_1_53_2",
      "doi-asserted-by": "crossref",
      "first-page": "753",
      "DOI": "10.1128/JB.180.3.753-758.1998",
      "article-title": "Analysis of Bacillus subtilis tagAB and tagDEF expression during phosphate starvation identifies a repressor role for PhoP\u02dcP",
      "volume": "180",
      "author": "Liu W.",
      "year": "1998",
      "journal-title": "J. Bacteriol."
    },
    {
      "key": "e_1_2_1_54_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1099/00221287-147-9-2447"
    },
    {
      "key": "e_1_2_1_55_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/JB.187.18.6253-6254.2005"
    },
    {
      "key": "e_1_2_1_56_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/s002030100321"
    },
    {
      "key": "e_1_2_1_57_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1046/j.1365-2958.2001.02303.x"
    },
    {
      "key": "e_1_2_1_58_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/JB.186.21.7364-7368.2004"
    },
    {
      "key": "e_1_2_1_59_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1365-2958.2005.04874.x"
    },
    {
      "key": "e_1_2_1_60_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1074/jbc.M006079200"
    },
    {
      "key": "e_1_2_1_61_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/emboj/cdg215"
    },
    {
      "key": "e_1_2_1_62_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1046/j.1365-2958.2002.03150.x"
    },
    {
      "key": "e_1_2_1_63_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jb.173.22.7351-7360.1991"
    },
    {
      "key": "e_1_2_1_64_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0378-1119(93)90359-B"
    },
    {
      "key": "e_1_2_1_65_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/417141a"
    },
    {
      "key": "e_1_2_1_66_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/JB.183.20.5991-5996.2001"
    },
    {
      "key": "e_1_2_1_67_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1101/gad.264403"
    },
    {
      "key": "e_1_2_1_68_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1021/ja065247w"
    },
    {
      "key": "e_1_2_1_69_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/s00203-006-0176-7"
    },
    {
      "key": "e_1_2_1_70_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/1522-2683(200112)22:20<4404::AID-ELPS4404>3.0.CO;2-2"
    },
    {
      "key": "e_1_2_1_71_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/s10295-003-0067-8"
    },
    {
      "key": "e_1_2_1_72_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0022-2836(02)01280-9"
    },
    {
      "key": "e_1_2_1_73_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/AAC.30.1.127"
    },
    {
      "key": "e_1_2_1_74_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/JB.185.18.5442-5451.2003"
    },
    {
      "key": "e_1_2_1_75_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/pmic.200300412"
    },
    {
      "key": "e_1_2_1_76_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/nar/gkj149"
    },
    {
      "key": "e_1_2_1_77_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1186/1471-2180-3-3"
    },
    {
      "key": "e_1_2_1_78_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/9783527620890.ch2"
    },
    {
      "key": "e_1_2_1_79_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0167-7799(90)90170-3"
    },
    {
      "key": "e_1_2_1_80_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/JB.00202-06"
    },
    {
      "key": "e_1_2_1_81_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/JB.186.24.8424-8432.2004"
    },
    {
      "key": "e_1_2_1_82_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1101/gad.943401"
    },
    {
      "key": "e_1_2_1_83_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/JB.186.16.5197-5201.2004"
    }
  ],
  "container-title": "PROTEOMICS",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://api.wiley.com/onlinelibrary/tdm/v1/articles/10.1002%2Fpmic.200600883",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "text-mining"
    },
    {
      "URL": "https://onlinelibrary.wiley.com/doi/full/10.1002/pmic.200600883",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2023,
        11,
        15
      ]
    ],
    "date-time": "2023-11-15T11:46:13Z",
    "timestamp": 1700048773000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://analyticalsciencejournals.onlinelibrary.wiley.com/doi/10.1002/pmic.200600883"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        2007,
        7
      ]
    ]
  },
  "references-count": 82,
  "journal-issue": {
    "issue": "14",
    "published-print": {
      "date-parts": [
        [
          2007,
          7
        ]
      ]
    }
  },
  "alternative-id": [
    "10.1002/pmic.200600883"
  ],
  "URL": "http://dx.doi.org/10.1002/pmic.200600883",
  "relation": {},
  "ISSN": [
    "1615-9853",
    "1615-9861"
  ],
  "subject": [],
  "container-title-short": "Proteomics",
  "published": {
    "date-parts": [
      [
        2007,
        7
      ]
    ]
  },
  "assertion": [
    {
      "value": "2006-11-08",
      "order": 0,
      "name": "received",
      "label": "Received",
      "group": {
        "name": "publication_history",
        "label": "Publication History"
      }
    },
    {
      "value": "2007-07-10",
      "order": 2,
      "name": "published",
      "label": "Published",
      "group": {
        "name": "publication_history",
        "label": "Publication History"
      }
    }
  ]
}