Reversible S-nitrosylation limits over synthesis of fungal styrylpyrone upon nitric oxide burst
详细信息    查看全文
  • 作者:Yanxia Zhao ; Meihong He ; Qi Xi ; Jianing Ding…
  • 关键词:Inonotus obliquus ; Styrylpyrone biosynthesis ; S ; nitrosylation ; Denitrosylation
  • 刊名:Applied Microbiology and Biotechnology
  • 出版年:2016
  • 出版时间:May 2016
  • 年:2016
  • 卷:100
  • 期:9
  • 页码:4123-4134
  • 全文大小:850 KB
  • 参考文献:Beckert C, Horn C, Schnitzler JP, Lehning A, Hellert W, Veit M (1997) Styrylpyrone biosynthesis in Equisetum arvense. Phytochem 44:275–283CrossRef
    Benhar M (2015) Nitric oxide and thioredoxin system: a complex interplay in redox regulation. Biochim Biophys Acta 1850:2476–2484CrossRef PubMed
    Benhar M, Forrester M, Hess D, Stamler J (2008) Regulated protein denitrosylation by cytosolic and mitochondrial thioredoxins. Sci 320:1050–1054CrossRef
    Benhar M, Forrester MT, Stamler JS (2009) Protein denitrosylation: enzymatic mechanisms and cellular functions. Mol Cell Biol 10:721–733
    Ben-Lulu S, Ziv T, Admon A, Weisman-Shomer P, Benhar M (2014) A substrate trapping approach identifies proteins regulated by reversible S-nitrosylation. Mol Cell Proteom 13(10):2573–2583CrossRef
    Boller T, He SY (2009) Innate immunity in plants: an arms race between pattern recognition receptors in plants and effectors in microbial pathogen. Sci 324:742–744CrossRef
    Campos R, Nonogaki H, Suslow T, Saltveit ME (2004) Isolation and characterization of a wound inducible phenylalanine ammonia-lyase gene (LsPAL1) from Romaine lettuce leaves. Physiol Plant 121:429–438CrossRef
    Chen YJ, Ching WC, Lin YP, Chen YJ (2013) Methods for detection and characterization of protein S-nitrosylation. Methods 62:138–150CrossRef PubMed
    Cochrane FC, Davin LB, Lewis NG (2004) The Arabidopsis phenylalanine ammonia lyase gene family kinetic characterization of the four isoforms. Phytochem 65:1557–1564CrossRef
    Dempsey DA, Vlot AC, Wildermuth MC, Klessiq DF (2011) Salicylic acid biosynthesis and metabolism. Arabidopsis Book e0156. American Society of Plant Biologists, Washington DC. doi:10.1199/tab.0156
    Forrester MT, Thompson JW, Foster MW, Leonardo N, Moseley MA, Stamler JS (2009) Proteomic analysis of S-nitrosylation and denitrosylation by resin-assisted capture. Nat Biotechnol 27:557–559CrossRef PubMed PubMedCentral
    Grossi L, Montevecchi PC (2002) S-nitrosocysteine and cysteine from reaction of cysteine with nitrous acid. A Kinetic Investigation. J Org Chem 67:8625–8630CrossRef PubMed
    Hao G, Derakhshan B, Shi L, Campagne F, Gross SS (2006) SNOSID, a proteomic method for identification of cysteine S-nitrosylation sites in complex protein mixtures. PNAS 103:1012–1017CrossRef PubMed PubMedCentral
    Hess DT, Matsumoto A, Kim SO, Marshal HE, Stamler JS (2005) Protein S-nitrosylation: purview and parameters. Nat Rev Mol Cell Biol 6:150–156CrossRef PubMed
    Huang HY, Chieh SY, Tso TK, Chien Y, Lin HT, Tsai YC (2011) Orally administered mycelial culture of Phellinus linteus exhibits antitumor effects in hepatoma cell-bearing mice. J Ethnopharmacol 133:460–466CrossRef PubMed
    Keller NP (2015) Translating biosynthetic gene cluster into fungal armor and weaponry. Nat Chem Biol 11:671–677CrossRef PubMed PubMedCentral
    Kneeshaw S, Gelineau SR, Tada Y, Loake GJ, Spoel SH (2014) Selective protein denitrosylation activity of thioredoxin-h5 modulates plant immunity. Mol Cell 56:153–162CrossRef PubMed
    Kronenfeld G, Engelman R, Weisman-Shomer P, Atlas D, Benhar M (2014) Thioredoxin-mimetic peptides as catalysts of S-denitrosylation and anti-nitrosative stress agents. Free Rad Biol Med 79:138–146CrossRef PubMed
    Lee D, Meye K, Chapple C, Douglasa CJ (1997) Antisense suppression of 4-coumarate:coenzyme A ligase activity in Arabidopsis leads to altered lignin subunit composition. Plant Cell 9:1985–1998CrossRef PubMed PubMedCentral
    Lee I, Yun B (2008) Peroxidase-mediated formation of the fungal polyphenols 3,14-bishispidinyl. J Microbiol Biotechnol 18:107–109PubMed
    Lee IK, Yun BS (2011) Styrylpyrone-class compounds from medicinal fungi Phellinus and Inonotus spp, and their medicinal importance. J Antibiot 64:349–359CrossRef PubMed
    Lewin A, Mayer M, Chusainow J, Jacob D, Appel B (2005) Viral promoters can initiate expression of toxin genes introduced into Escherichia coli. BMC Biotechnol 5:19–28CrossRef PubMed PubMedCentral
    Malik SI, Hussain A, Yun BW, Spoel SH, Loake GJ (2011) GSNOR-mediated denitrosylation in the plant defence response. Plant Sci 181:540–544CrossRef PubMed
    Marinez-Ruiz A, Cadenas S, Lamas S (2011) Nitric oxide signaling: classical, less classical and nonclassical mechanisms. Free Rad Biol Medi 51:17–29CrossRef
    Nallamsetty S, Waugh DS (2007) A generic protocol for the expression and purification of recombinant proteins in Escherichia coli using a combinatorial His6-maltose binding protein fusion tag. Nat Protocol 2:383–391CrossRef
    Nikitovic D, Holmgren A (1996) S-nitrosoglutathione is cleaved by the thioredoxin system with liberation of glutathione and redox regulating nitric oxide. J Biol Chem 271:19180–19185CrossRef PubMed
    Raju K, Doulias PT, Tenopoulou M, Greene JL, Ischiropoulos H (2012) Strategies and tools to explore protein S-nitrosylation. Biochim Biophys Acta 1820:684–688CrossRef PubMed PubMedCentral
    Skelly M, Loake G (2013) Synthesis of redox-active molecules and their signaling functions during the expression of plant disease resistance. Antioxid Redox Signal 19:990–997CrossRef PubMed PubMedCentral
    Thompson JW, Forrester MT, Moseley MA, Foster MW (2013) Solid-phase capture for the detection and relative quantification of S-nitrosoproteins by mass spectrometry. Methods 62:130–137CrossRef PubMed PubMedCentral
    Uehara T, Nishiya T (2011) Screening systems for the identification of S-nitrosylated proteins. Nitric Oxide 25:108–111CrossRef PubMed
    Vitor S, Durate G, Saviani E, Vincentz M, HO HC, Salgado I (2013) Nitrate reductase is required for the transcriptional modulation and bactericidal activity of nitric oxide during the defense response of Arabidopsis thaliana against Pseudomonas syingae. Planta 238:475–486CrossRef PubMed
    Vogt T (2010) Phenylpropanoid biosynthesis. Mol Plant 3:2–20CrossRef PubMed
    Wu C, Parrott AM, Liu T, Jain MR, Yang Y, Sadoshima J, Li H (2011) Distinction of thioredoxin transnitrosylation and denitrosylation target proteins by the ICAT quantitative approach. J Proteom 74:2498–2509CrossRef
    Xin D, Zou X, Zou M, Liu C (2014) The expression and antibody preparation of S 100 A protein. Chin J Cell Mol Immunol 30:1166–1169
    Yu M, Lamattina L, Spoel SH, Loake GJ (2014) Nitric oxide function in plant biology: a redox cue in deconvolution. New Phytol 202:1142–1156CrossRef PubMed
    Yu M, Yun BW, Spoel SH, Loake GJ (2012) A sleigh ride through the SNO: regulation of plant immune function by protein S-nitrosylation. Curr Opin Plant Biol 15:424–430CrossRef PubMed
    Zhao Y, Miao K, Zhang M, Wei Z, Zheng W (2009) Effects of nitric oxide on production of antioxidant phenolic compounds in Phaeoporus obliquus. Mycosystema 28:750–754
    Zhao Y, Xi Q, Xu Q, He M, Ding J, Dai Y, Keller NP, Zheng W (2015) Correlation of nitric oxide produced by an inducible nitric oxide synthase-like protein with enhanced expression of the phenylpropanoid pathway in Inonotus obliquus cocultured with Phellinus morii. Appl Microbiol Biotechnol 99:4361–4372CrossRef PubMed
    Zheng NC, Huang BM, Xu J, Huang SS, Hu XC, Chen JZ, Yu XG (2006) Effect of amino acid site mutagenesis on the activity and heat stability of Clonorchis sinensis malate dehydrogenase. Chin J Zoon 22:575–579
    Zheng W, Liu Y, Pan S, Yuan W, Dai Y, Wei J (2011a) Involvements of S-nitrosylation and denitrosylation in the production of polyphenols by Inonotus obliquus. Appl Microbiol Biotechnol 90:1763–1772CrossRef PubMed
    Zheng W, Miao K, Liu Y, Zhao Y, Zhang M, Pan S, Dai Y (2010) Chemical diversity of biologically active metabolites in the sclerotia of Inonotus obliquus and submerged culture strategies for up-regulating their production. Appl Microbiol Biotechnol 87:1237–1254CrossRef PubMed
    Zheng W, Miao K, Zhao Y, Pan S, Zhang M, Jiang H (2009) Nitric oxide mediates the fungal-elicitor enhanced biosynthesis of antioxidant polyphenols in submerged cultures of Inonotus obliquus. Microbiol 155:3340–3348CrossRef
    Zheng W, Zhao Y, Zheng X, Liu Y, Pan S, Dai Y, Liu F (2011b) Production of antioxidant and antitumor metabolites by submerged cultures of Inonotus obliquus cocultured with Phellinus punctatus. Appl Microbiol Biotechnol 89:157–167CrossRef PubMed
    Zhou Z, Liu K (2010) Pigments of fungi (macromycetes). Nat Prod Rep 27:1531–1570CrossRef PubMed
  • 作者单位:Yanxia Zhao (1)
    Meihong He (1)
    Qi Xi (1)
    Jianing Ding (1)
    Baixia Hao (1)
    Nancy P Keller (2)
    Weifa Zheng (1)

    1. Laboratory of Biotechnology on Medicinal Plants, School of Life Sciences, Jiangsu Normal University, Xuzhou, 221116, China
    2. Department of Medical Microbiology and Immunology, University of Wisconsin-Madison, WI, 53706, USA
  • 刊物类别:Chemistry and Materials Science
  • 刊物主题:Chemistry
    Biotechnology
    Microbiology
    Microbial Genetics and Genomics
  • 出版者:Springer Berlin / Heidelberg
  • ISSN:1432-0614
文摘
Nitric oxide (NO) is known to be involved in modulating production of styrylpyrone polyphenols in the basidiomycete Inonotus obliquus. However, it remains unknown how NO orchestrates fungal styrylpyrone biosynthesis. Here, we show that a transient NO burst correlated with an enhanced expression of phenylalanine ammonia lyase (PAL), 4-coumarate CoA ligase (4CL), and styrylpyrone synthase (SPS), the key enzymes involved in styrylpyrone biosynthesis, and subsequently an increased production of styrylpyrone polyphenols. In parallel, the NO burst also resulted in S-nitrosylation of PAL, 4CL, and SPS, which compromised their enzymatic activities mediating a post-translational feedback mechanism that keeps NO-dependent transcriptional activation in check. Moreover, dysfunction of thioredoxin reductase (TrxR) further increased the formation of S-nitrosylated proteins, implicating the significance of the Trx system in maintaining a low level of protein-nitrosothiols. Three thioredoxin-like proteins (TrxLs) from I. obliquus show in vitro denitrosylation potential toward S-nitrosylated proteins via trans-denitrosylation or mixed disulfide intermediates. Thus, S-nitrosylation triggered by the NO burst limits over production of fungal styrylpyrone polyphenols, and denitrosylation by TrxLs that act in concert with TrxR play a key role in maintaining redox balance and orchestrating catalytic activities of the enzymes engaged in styrylpyrone synthetic metabolism.

© 2004-2018 中国地质图书馆版权所有 京ICP备05064691号 京公网安备11010802017129号

地址:北京市海淀区学院路29号 邮编:100083

电话:办公室:(+86 10)66554848;文献借阅、咨询服务、科技查新:66554700