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AtCYS1, A Cystatin From Arabidopsis Thaliana, Suppresses Hypersensitive Cell Death.

B. Belenghi, F. Acconcia, M. Trovato, M. Perazzolli, A. Bocedi, F. Polticelli, P. Ascenzi, M. Delledonne
Published 2003 · Biology, Medicine

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In plants, cysteine protease inhibitors are involved in the regulation of protein turnover and play an important role in resistance against insects and pathogens. AtCYS1 from Arabidopsis thaliana encodes a protein of 102 amino acids that contains the conserved motif of cysteine protease inhibitors belonging to the cystatin superfamily (Gln-Val-Val-Ala-Gly). Recombinant A. thaliana cystatin-1 (AtCYS1) was expressed in Escherichia coli and purified. AtCYS1 inhibits the catalytic activity of papain (Kd = 4.0 x 10-2 micro m, at pH 7.0 and 25 degrees C), generally taken as a molecular model of cysteine proteases. The molecular bases for papain inhibition by AtCYS1 have been analysed taking into account the three-dimensional structure of the papain-stefin B complex. AtCYS1 is constitutively expressed in roots and in developing siliques of A. thaliana. In leaves, AtCYS1 is strongly induced by wounding, by challenge with avirulent pathogens and by nitric oxide (NO). The overexpression of AtCYS1 blocks cell death activated by either avirulent pathogens or by oxidative and nitrosative stress in both A. thaliana suspension cultured cells and in transgenic tobacco plants. The suppression of the NO-mediated cell death in plants overexpressing AtCYS1 provides the evidence that NO is not cytotoxic for the plant, indicating that NO functions as cell death trigger through the stimulation of an active process, in which cysteine proteases and theirs proteinaceous inhibitors appear to play a crucial role.
This paper references
Cleavage of structural proteins during
U. K. Laemmli (1970)
Molecular cloning and gibberellin-induced expression of multiple cysteine proteinases of rice seeds (oryzains).
H. Watanabe (1991)
10.1021/BI990488K
Importance of the second binding loop and the C-terminal end of cystatin B (stefin B) for inhibition of cysteine proteinases.
E. Pol (1999)
10.1046/J.1365-313X.1997.11061187.X
Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley—powdery mildew interaction
H. Thordal-Christensen (1997)
10.1093/NAR/17.20.8385
Efficient transformation of Agrobacterium spp. by high voltage electroporation.
W. Shen (1989)
10.1104/pp.103.4.1347
Methyl Jasmonate Induces Papain Inhibitor(s) in Tomato Leaves
C. Bolter (1993)
10.1104/pp.111.4.1299
Two Wound-Inducible Soybean Cysteine Proteinase Inhibitors Have Greater Insect Digestive Proteinase Inhibitory Activities than a Constitutive Homolog
Y. Zhao (1996)
10.1007/BF01977351
NewAgrobacterium helper plasmids for gene transfer to plants
E. Hood (2005)
10.1016/0003-2697(76)90527-3
A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.
M. M. Bradford (1976)
10.1104/pp.112.3.1201
Differential Expression of Soybean Cysteine Proteinase Inhibitor Genes during Development and in Response to Wounding and Methyl Jasmonate
M. A. Botella (1996)
10.1089/152308603321223522
The functions of nitric oxide-mediated signaling and changes in gene expression during the hypersensitive response.
M. Delledonne (2003)
10.1038/29087
Nitric oxide functions as a signal in plant disease resistance
M. Delledonne (1998)
10.1128/JB.168.2.512-522.1986
Gene cluster of Pseudomonas syringae pv. "phaseolicola" controls pathogenicity of bean plants and hypersensitivity of nonhost plants.
P. B. Lindgren (1986)
10.1093/nar/28.1.235
The Protein Data Bank
H. Berman (2000)
10.1016/S1369-5266(00)00086-8
Trade-offs between pathogen and herbivore resistance.
G. Felton (2000)
10.1016/0014-5793(93)80621-Z
Reaction of nitric oxide with hydrogen peroxide to produce potentially cytotoxic singlet oxygen as a model for nitric oxide‐mediated killing
A. Noronha-Dutra (1993)
10.1016/S0014-5793(99)01611-7
Translocation of cytochrome c from the mitochondria to the cytosol occurs during heat‐induced programmed cell death in cucumber plants
J. Balk (1999)
10.1016/0167-4838(85)90057-3
The proteolytic activities of chymopapain, papain, and papaya proteinase III.
S. Zucker (1985)
10.1016/S0014-5793(01)03230-6
Participation of the mitochondrial permeability transition pore in nitric oxide‐induced plant cell death
E. E. Saviani (2002)
10.1016/S0960-9822(02)00510-9
Calcium-mediated apoptosis in a plant hypersensitive disease resistance response
A. Levine (1996)
10.1046/J.1432-1327.1998.2520001.X
Mitochondria and apoptosis.
B. Mignotte (1998)
Three - dimensional structure of oryzacystatinI , a cysteine proteinase inhibitor of the rice , Oryza sativa L . japonica
K. Nagata (2000)
10.1002/ELPS.1150181505
SWISS‐MODEL and the Swiss‐Pdb Viewer: An environment for comparative protein modeling
N. Guex (1997)
10.1126/SCIENCE.227.4691.1229
A simple and general method for transferring genes into plants.
R. Horsch (1985)
10.1007/BF00020124
Characterization of a cDNA encoding cysteine proteinase inhibitor from Chinese cabbage (Brassica campestris L. ssp. pekinensis) flower buds
C. O. Lim (2004)
Comparative modelling by statisfaction of spatial restraints
A. Šali (1993)
10.1007/BF01248409
Toxicity toChrysomela tremulae (Coleoptera: Chrysomelidae) of transgenic poplars expressing a cysteine proteinase inhibitor
J. C. Leplé (2005)
10.1002/PROT.340110407
Protein folding and association: Insights from the interfacial and thermodynamic properties of hydrocarbons
A. Nicholls (1991)
10.1007/s004250050409
Early events in the elicitation of plant defence
J. Ebel (1998)
10.1016/S0022-1910(97)00040-1
The adaptation of insects to plant protease inhibitors.
C. Bolter (1997)
10.1021/BI00430A022
Kinetics of binding of chicken cystatin to papain.
I. Björk (1989)
10.1016/S1369-5266(99)00026-6
Die and let live - programmed cell death in plants.
E. Lam (1999)
Molecular cloning of a cysteine proteinase inhibitor of rice (oryzacystatin). Homology with animal cystatins and transient expression in the ripening process of rice seeds.
K. Abe (1987)
10.1002/JMR.300050306
Binding of the kunitz‐type trypsin inhibitor DE‐3 from Erythrina caffra seeds to serine proteinases: a comparative study
S. Onesti (1992)
Gapped BLAST and PSI-BLAST: A new
D. Lipman (1997)
10.1105/tpc.11.3.431
The Involvement of Cysteine Proteases and Protease Inhibitor Genes in the Regulation of Programmed Cell Death in Plants
M. Solomon (1999)
10.1002/j.1460-2075.1988.tb03109.x
The 2.0 A X‐ray crystal structure of chicken egg white cystatin and its possible mode of interaction with cysteine proteinases.
W. Bode (1988)
10.1016/S0960-9822(99)80140-7
Inverse relationship between systemic resistance of plants to microorganisms and to insect herbivory
G. Felton (1999)
10.1105/tpc.2.5.437
Arabidopsis is susceptible to infection by a downy mildew fungus.
E. Koch (1990)
10.1006/JMBI.1994.0088
The three-dimensional solution structure of human stefin A.
J. Martin (1995)
10.1021/JF00008A030
Isolation and partial characterization of a soybean cystatin cysteine proteinase inhibitor of coleopteran digestive proteolytic activity
M. Hines (1991)
10.1105/tpc.11.2.237
Victorin Induction of an Apoptotic/Senescence–like Response in Oats
D. Navarre (1999)
10.1007/BF00019555
Induction of cysteine and serine proteases during xylogenesis in Zinnia elegans
Z. Ye (2004)
10.1016/0168-9452(91)90044-9
The expression of papain inhibitors during development of cowpea seeds
K. Fernandes (1991)
10.1042/BJ2010189
L-trans-Epoxysuccinyl-leucylamido(4-guanidino)butane (E-64) and its analogues as inhibitors of cysteine proteinases including cathepsins B, H and L.
A. Barrett (1982)
Gapped BLAST and PSIBLAST: a new generation of protein database search programs
S. F. Altschul (1997)
10.1002/j.1460-2075.1990.tb08321.x
The refined 2.4 A X‐ray crystal structure of recombinant human stefin B in complex with the cysteine proteinase papain: a novel type of proteinase inhibitor interaction.
M. Stubbs (1990)
10.1023/A:1006133311402
Markers for hypersensitive response and senescence show distinct patterns of expression
D. Pontier (2004)
10.1073/pnas.231178298
Signal interactions between nitric oxide and reactive oxygen intermediates in the plant hypersensitive disease resistance response
M. Delledonne (2001)
10.1074/JBC.271.11.6144
The Chemistry and Tumoricidal Activity of Nitric Oxide/Hydrogen Peroxide and the Implications to Cell Resistance/Susceptibility (*)
R. Farias-Eisner (1996)
Toxicity to Chrysomela tremulae (Coleoptera: Chrysomelidae) of transgenic poplars expressing a cysteine proteinase inhibitor.Mol
J. C. Leplé (1995)
Molecular Cloning: A Laboratory Manual
J. Sambrook (1983)
10.1007/BF00021535
Characterization of a genomic sequence coding for potato multicystatin, an eight-domain cysteine proteinase inhibitor
C. Waldron (2004)
10.1038/70781
The use of cysteine proteinase inhibitors to engineer resistance against potyviruses in transgenic tobacco plants
R. Gutiérrez-Campos (1999)
10.1146/ANNUREV.PY.28.090190.002233
Protease Inhibitors in Plants: Genes for Improving Defenses Against Insects and Pathogens
C. Ryan (1990)
10.1110/ps.11901
Role of the single cysteine residue, Cys 3, of human and bovine cystatin B (stefin B) in the inhibition of cysteine proteinases
E. Pol (2001)
10.1107/S0021889892009944
PROCHECK: a program to check the stereochemical quality of protein structures
R. Laskowski (1993)
1-Trans-epoxysuccinyl-leucylamido(4-guanidino)butane (E-64) and its analogues as inhibitors of cysteine proteinases including cathepsins
A. J. Barrett (1982)
Handbook of proteolytic enzymes
A. Barrett (1998)
10.1093/NAR/22.22.4673
CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice.
J. Thompson (1994)
10.1104/pp.010999
Oxidative Stress Increased Respiration and Generation of Reactive Oxygen Species, Resulting in ATP Depletion, Opening of Mitochondrial Permeability Transition, and Programmed Cell Death1
B. Tiwari (2002)
10.1074/jbc.M001054200
Inhibition of Papain by S-Nitrosothiols
M. Xian (2000)
10.1023/A:1006154829118
A chestnut seed cystatin differentially effective against cysteine proteinases from closely related pests
M. Pernas (2004)
10.1046/j.1365-313X.1991.t01-7-00999.x
Identification and molecular mapping of a single Arabidopsis thaliana locus determining resistance to a phytopathogenic Pseudomonas syringae isolate.
T. Debener (1991)
Two distinct cystatin species in rice seeds with different specificities against cysteine proteinases. Molecular cloning, expression, and biochemical studies on oryzacystatin-II.
H. Kondo (1990)
10.1006/JMBI.1993.1658
The structures of native phosphorylated chicken cystatin and of a recombinant unphosphorylated variant in solution.
T. Dieckmann (1993)
10.1111/J.1365-313X.1994.00715.X
Biologically induced systemic acquired resistance in Arabidopsis thaliana
R. Cameron (1994)
10.1016/0092-8674(94)90577-0
DET1, a negative regulator of light-mediated development and gene expression in arabidopsis, encodes a novel nuclear-localized protein
A. Pepper (1994)
10.1023/A:1009605001253
Transformation of white poplar (Populus alba L.) with a novel Arabidopsis thaliana cysteine proteinase inhibitor and analysis of insect pest resistance
M. Delledonne (2004)
10.2210/pdb1eqk/pdb
Three-dimensional solution structure of oryzacystatin-I, a cysteine proteinase inhibitor of the rice, Oryza sativa L. japonica.
K. Nagata (2000)
Jasmonate is essential for insect defense in Arabidopsis
Texa Biophysics (1997)
10.1002/PRO.5560060102
Friends and relations of the cystatin superfamily—new members and their evolution
W. M. Brown (1997)
10.1104/PP.121.1.71
Mannose induces an endonuclease responsible for DNA laddering in plant cells.
J. C. Stein (1999)
10.1021/BI980026R
The role of Gly-4 of human cystatin A (stefin A) in the binding of target proteinases. Characterization by kinetic and equilibrium methods of the interactions of cystatin A Gly-4 mutants with papain, cathepsin B, and cathepsin L.
S. Estrada (1998)
10.1016/0092-8674(94)90544-4
H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response
Alex Levine (1994)
10.1111/J.1432-1033.1992.TB17365.X
Corn kernel cysteine proteinase inhibitor as a novel cystatin superfamily member of plant origin. Molecular cloning and expression studies.
M. Abe (1992)



This paper is referenced by
Function and Regulation of Xylem Cysteine Protease 1 and Xylem Cysteine Protease 2 in Arabidopsis
I. Ismail (2003)
10.1016/j.ijbiomac.2016.11.107
Insight into the biochemical, kinetic and spectroscopic characterization of garlic (Allium sativum) phytocystatin: Implication for cardiovascular disease.
Mohd Faizan Siddiqui (2017)
10.3389/fpls.2017.00743
Molecular Characterization and Expression Profiling of Brachypodium distachyon L. Cystatin Genes Reveal High Evolutionary Conservation and Functional Divergence in Response to Abiotic Stress
Saminathan Subburaj (2017)
10.1093/JXB/ERI295
Stress responses to polycyclic aromatic hydrocarbons in Arabidopsis include growth inhibition and hypersensitive response-like symptoms.
Merianne Alkio (2005)
10.1080/09540100903427314
Investigating the role of cystatin in conferring stage dependent resistance against Karnal bunt of wheat
V. Gupta (2010)
10.3389/fpls.2019.00473
Proteases Underground: Analysis of the Maize Root Apoplast Identifies Organ Specific Papain-Like Cysteine Protease Activity
Jan Schulze Hüynck (2019)
Caracterização de genes de cafe (coffea sp.) induzidos durante a infestação do bicho mineiro (leucoptera coffeella)
Jorge Maurício Costa Mondego (2005)
Identification and characterization of copper-responsive proteins in arabidopsis
Courtney Solheim (2008)
Protection of recombinant glutathione reductase by Oryzacystatin-I in transgenic tobacco
Tsholofelo Reineth Kibido (2013)
10.2306/SCIENCEASIA1513-1874.2013.39.596
Characterization of a cDNA encoding cystatin with antifungal activity from Siam tulip Curcuma alismatifolia
Ruangwit Porruan (2013)
10.1007/s12104-011-9334-1
Resonance assignments and secondary structure of a phytocystatin from Ananas comosus
D. Irene (2012)
10.3390/ijms140611125
Short-Term Chromium-Stress-Induced Alterations in the Maize Leaf Proteome
R. Wang (2013)
10.1007/s10059-009-0081-4
The calmodulin-binding transcription factor OsCBT suppresses defense responses to pathogens in rice
S. C. Koo (2009)
10.1016/j.biochi.2019.06.006
Recombinant cystatins in plants.
J. Tremblay (2019)
10.1016/j.pep.2018.04.014
Cloning and characterization of ApCystatin, a plant cystatin gene from Agapanthus praecox ssp. orientalis responds to abiotic stress.
Guan-qun Chen (2018)
10.1080/23312025.2016.1262489
Isolation and purification of phytocystatin from almond: Biochemical, biophysical, and immunological characterization
A. A. Siddiqui (2016)
10.1080/15216540310001639274
Nitric Oxide Signaling in Plant‐Pathogen Interactions
M. C. Romero-Puertas (2003)
10.1371/journal.pone.0067377
Secretome Analysis of the Pine Wood Nematode Bursaphelenchus xylophilus Reveals the Tangled Roots of Parasitism and Its Potential for Molecular Mimicry
Ryoji Shinya (2013)
10.1111/j.1365-3040.2009.02073.x
Regulation of growth response to water stress in the soybean primary root. I. Proteomic analysis reveals region-specific regulation of phenylpropanoid metabolism and control of free iron in the elongation zone.
M. Yamaguchi (2010)
10.1016/J.BBRC.2006.10.071
Functional study of hot pepper 26S proteasome subunit RPN7 induced by Tobacco mosaic virus from nuclear proteome analysis.
Boo-Ja Lee (2006)
10.1105/tpc.111.093732
A Maize Cystatin Suppresses Host Immunity by Inhibiting Apoplastic Cysteine Proteases[C][W]
Karina van der Linde (2012)
10.1093/JXB/ERJ052
NO way to live; the various roles of nitric oxide in plant-pathogen interactions.
L. Mur (2006)
10.1007/s10495-006-6601-1
A cellular suicide strategy of plants: vacuole-mediated cell death
N. Hatsugai (2006)
10.1016/S1672-0229(10)60005-8
In silico Analysis of Sequential, Structural and Functional Diversity of Wheat Cystatins and Its Implication in Plant Defense
S. Dutt (2010)
10.1002/9781444328547.CH3
Sounding the Alarm: Signaling and Communication in Plant Defense
Dale R. Walters (2010)
10.1007/s00299-015-1810-0
Genome-wide identification and characterization of cystatin family genes in rice (Oryza sativa L.)
Wei Wang (2015)
10.1016/j.niox.2014.06.008
Detection and function of nitric oxide during the hypersensitive response in Arabidopsis thaliana: where there's a will there's a way.
J. Chen (2014)
10.4161/psb.18967
Caspase-like enzymatic activity and the ascorbate-glutathione cycle participate in salt stress tolerance of maize conferred by exogenously applied nitric oxide
M. Keyster (2012)
10.1111/j.1462-5822.2004.00361.x
The role and regulation of programmed cell death in plant–pathogen interactions
J. Greenberg (2004)
10.1093/JXB/ERM244
Nitric oxide function and signalling in plant disease resistance.
J. Hong (2008)
10.1271/bbb.68.1681
Molecular Cloning, Expression, and Functional Characterization of a Cystatin from Pineapple Stem
D. J. Shyu (2004)
10.1038/cdd.2016.34
Inhibition of cathepsin B by caspase-3 inhibitors blocks programmed cell death in Arabidopsis
Y. Ge (2016)
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