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Arabidopsis AtSerpin1, crystal structure and in vivo interaction with its target protease RESPONSIVE TO DESICCATION-21 (RD21).

Lampl N, Budai-Hadrian O, Davydov O, Joss TV, Harrop SJ, Curmi PM, Roberts TH, Fluhr R
J Biol Chem 285 13550-60 (2010)
Cited: 55 times
EuropePMC logo PMID: 20181955

Abstract

In animals, protease inhibitors of the serpin family are associated with many physiological processes, including blood coagulation and innate immunity. Serpins feature a reactive center loop (RCL), which displays a protease target sequence as a bait. RCL cleavage results in an irreversible, covalent serpin-protease complex. AtSerpin1 is an Arabidopsis protease inhibitor that is expressed ubiquitously throughout the plant. The x-ray crystal structure of recombinant AtSerpin1 in its native stressed conformation was determined at 2.2 A. The electrostatic surface potential below the RCL was found to be highly positive, whereas the breach region critical for RCL insertion is an unusually open structure. AtSerpin1 accumulates in plants as a full-length and a cleaved form. Fractionation of seedling extracts by nonreducing SDS-PAGE revealed the presence of an additional slower migrating complex that was absent when leaves were treated with the specific cysteine protease inhibitor L-trans-epoxysuccinyl-L-leucylamido (4-guanidino)butane. Significantly, RESPONSIVE TO DESICCATION-21 (RD21) was the major protease labeled with the L-trans-epoxysuccinyl-L-leucylamido (4-guanidino)butane derivative DCG-04 in wild type extracts but not in extracts of mutant plants constitutively overexpressing AtSerpin1, indicating competition. Fractionation by nonreducing SDS-PAGE followed by immunoblotting with RD21-specific antibody revealed that the protease accumulated both as a free enzyme and in a complex with AtSerpin1. Importantly, both RD21 and AtSerpin1 knock-out mutants lacked the serpin-protease complex. The results establish that the major Arabidopsis plant serpin interacts with RD21. This is the first report of the structure and in vivo interaction of a plant serpin with its target protease.

Reviews - 3le2 mentioned but not cited (1)

  1. Peptide-based protease inhibitors from plants. Hellinger R, Gruber CW. Drug Discov Today 24 1877-1889 (2019)

Articles - 3le2 mentioned but not cited (7)

  1. Arabidopsis AtSerpin1, crystal structure and in vivo interaction with its target protease RESPONSIVE TO DESICCATION-21 (RD21). Lampl N, Budai-Hadrian O, Davydov O, Joss TV, Harrop SJ, Curmi PM, Roberts TH, Fluhr R. J Biol Chem 285 13550-13560 (2010)
  2. A Comprehensive Phylogenetic Analysis of the Serpin Superfamily. Spence MA, Mortimer MD, Buckle AM, Minh BQ, Jackson CJ. Mol Biol Evol 38 2915-2929 (2021)
  3. Plant protein peptidase inhibitors: an evolutionary overview based on comparative genomics. Santamaría ME, Diaz-Mendoza M, Diaz I, Martinez M. BMC Genomics 15 812 (2014)
  4. Serpins in rice: protein sequence analysis, phylogeny and gene expression during development. Francis SE, Ersoy RA, Ahn JW, Atwell BJ, Roberts TH. BMC Genomics 13 449 (2012)
  5. 1.45 Å resolution structure of SRPN18 from the malaria vector Anopheles gambiae. Meekins DA, Zhang X, Battaile KP, Lovell S, Michel K. Acta Crystallogr F Struct Biol Commun 72 853-862 (2016)
  6. The Importance of N186 in the Alpha-1-Antitrypsin Shutter Region Is Revealed by the Novel Bologna Deficiency Variant. Ronzoni R, Ferrarotti I, D'Acunto E, Balderacchi AM, Ottaviani S, Lomas DA, Irving JA, Miranda E, Fra A. Int J Mol Sci 22 5668 (2021)
  7. TcSERPIN, an inhibitor that interacts with cocoa defense proteins and has biotechnological potential against human pathogens. Ferreira MM, Farias KS, Zugaib M, Alves AMM, Amaral GV, Santos MLDC, Freitas ADS, Santana BCG, Dos Santos Júnior SL, Mora-Ocampo IY, Santos AS, da Silva MF, Andrade BS, Pirovani CP. Front Plant Sci 15 1337750 (2024)


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  1. Serpins flex their muscle: I. Putting the clamps on proteolysis in diverse biological systems. Silverman GA, Whisstock JC, Bottomley SP, Huntington JA, Kaiserman D, Luke CJ, Pak SC, Reichhart JM, Bird PI. J Biol Chem 285 24299-24305 (2010)
  2. Centrality of host cell death in plant-microbe interactions. Dickman MB, Fluhr R. Annu Rev Phytopathol 51 543-570 (2013)
  3. Reassessing apoptosis in plants. Dickman M, Williams B, Li Y, de Figueiredo P, Wolpert T. Nat Plants 3 773-779 (2017)
  4. Juggling jobs: roles and mechanisms of multifunctional protease inhibitors in plants. Grosse-Holz FM, van der Hoorn RA. New Phytol 210 794-807 (2016)
  5. The Increasing Impact of Activity-Based Protein Profiling in Plant Science. Morimoto K, van der Hoorn RA. Plant Cell Physiol 57 446-461 (2016)
  6. The complex world of plant protease inhibitors: Insights into a Kunitz-type cysteine protease inhibitor of Arabidopsis thaliana. Rustgi S, Boex-Fontvieille E, Reinbothe C, von Wettstein D, Reinbothe S. Commun Integr Biol 11 e1368599 (2018)
  7. Serpin protease inhibitors in plant biology. Fluhr R, Lampl N, Roberts TH. Physiol Plant 145 95-102 (2012)
  8. Chloroplast Protein Degradation in Senescing Leaves: Proteases and Lytic Compartments. Buet A, Costa ML, Martínez DE, Guiamet JJ. Front Plant Sci 10 747 (2019)
  9. Plant serpin protease inhibitors: specificity and duality of function. Cohen M, Davydov O, Fluhr R. J Exp Bot 70 2077-2085 (2019)
  10. Natural substrates of plant proteases: how can protease degradomics extend our knowledge? Tsiatsiani L, Gevaert K, Van Breusegem F. Physiol Plant 145 28-40 (2012)
  11. Probes for activity-based profiling of plant proteases. van der Hoorn RA, Kaiser M. Physiol Plant 145 18-27 (2012)
  12. Plant Serpins: Potential Inhibitors of Serine and Cysteine Proteases with Multiple Functions. Ferreira MM, Santos AS, Santos AS, Zugaib M, Pirovani CP. Plants (Basel) 12 3619 (2023)

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  2. Arabidopsis metacaspase 2d is a positive mediator of cell death induced during biotic and abiotic stresses. Watanabe N, Lam E. Plant J 66 969-982 (2011)
  3. Set-point control of RD21 protease activity by AtSerpin1 controls cell death in Arabidopsis. Lampl N, Alkan N, Davydov O, Fluhr R. Plant J 74 498-510 (2013)
  4. Post-translational regulation and trafficking of the granulin-containing protease RD21 of Arabidopsis thaliana. Gu C, Shabab M, Strasser R, Wolters PJ, Shindo T, Niemer M, Kaschani F, Mach L, van der Hoorn RA. PLoS One 7 e32422 (2012)
  5. Calcium-dependent activation and autolysis of Arabidopsis metacaspase 2d. Watanabe N, Lam E. J Biol Chem 286 10027-10040 (2011)
  6. Identification of host genes involved in geminivirus infection using a reverse genetics approach. Lozano-Durán R, Rosas-Díaz T, Luna AP, Bejarano ER. PLoS One 6 e22383 (2011)
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  10. Serpin1 and WSCP differentially regulate the activity of the cysteine protease RD21 during plant development in Arabidopsis thaliana. Rustgi S, Boex-Fontvieille E, Reinbothe C, von Wettstein D, Reinbothe S. Proc Natl Acad Sci U S A 114 2212-2217 (2017)
  11. Singlet Oxygen-Induced Membrane Disruption and Serpin-Protease Balance in Vacuolar-Driven Cell Death. Koh E, Carmieli R, Mor A, Fluhr R. Plant Physiol 171 1616-1625 (2016)
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  13. The tomato yellow leaf curl virus (TYLCV) V2 protein interacts with the host papain-like cysteine protease CYP1. Bar-Ziv A, Levy Y, Hak H, Mett A, Belausov E, Citovsky V, Gafni Y. Plant Signal Behav 7 983-989 (2012)
  14. A Kunitz-type protease inhibitor regulates programmed cell death during flower development in Arabidopsis thaliana. Boex-Fontvieille E, Rustgi S, Reinbothe S, Reinbothe C. J Exp Bot 66 6119-6135 (2015)
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  16. AtSERPIN1 is an inhibitor of the metacaspase AtMC1-mediated cell death and autocatalytic processing in planta. Lema Asqui S, Vercammen D, Serrano I, Valls M, Rivas S, Van Breusegem F, Conlon FL, Dangl JL, Coll NS. New Phytol 218 1156-1166 (2018)
  17. Potential use of a serpin from Arabidopsis for pest control. Alvarez-Alfageme F, Maharramov J, Carrillo L, Vandenabeele S, Vercammen D, Van Breusegem F, Smagghe G. PLoS One 6 e20278 (2011)
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  20. The Tomato yellow leaf curl virus (TYLCV) V2 protein inhibits enzymatic activity of the host papain-like cysteine protease CYP1. Bar-Ziv A, Levy Y, Citovsky V, Gafni Y. Biochem Biophys Res Commun 460 525-529 (2015)
  21. Comparative proteomic analysis of melon phloem exudates in response to viral infection. Serra-Soriano M, Navarro JA, Genoves A, Pallás V. J Proteomics 124 11-24 (2015)
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  24. Molecular and immunological characterization of wheat Serpin (Tri a 33). Mameri H, Denery-Papini S, Pietri M, Tranquet O, Larré C, Drouet M, Paty E, Jonathan AM, Beaudouin E, Moneret-Vautrin DA, Moreau T, Briozzo P, Gaudin JC. Mol Nutr Food Res 56 1874-1883 (2012)
  25. Mining the Active Proteome of Arabidopsis thaliana. van der Hoorn RA, Colby T, Nickel S, Richau KH, Schmidt J, Kaiser M. Front Plant Sci 2 89 (2011)
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  30. EMS Derived Wheat Mutant BIG8-1 (Triticum aestivum L.)-A New Drought Tolerant Mutant Wheat Line. le Roux ML, Burger NFV, Vlok M, Kunert KJ, Cullis CA, Botha AM. Int J Mol Sci 22 5314 (2021)
  31. Genome Wide Identification and Comparative Analysis of the Serpin Gene Family in Brachypodium and Barley. Rehman S, Jørgensen B, Aziz E, Batool R, Naseer S, Rasmussen SK. Plants (Basel) 9 E1439 (2020)
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