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The 2.0 A crystal structure and substrate specificity of the KDEL-tailed cysteine endopeptidase functioning in programmed cell death of Ricinus communis endosperm.

Than ME, Helm M, Simpson DJ, Lottspeich F, Huber R, Gietl C
J Mol Biol 336 1103-16 (2004)
Cited: 35 times
EuropePMC logo PMID: 15037072

Abstract

In the senescing endosperm of germinating castor bean (Ricinus communis) a special organelle (the ricinosome) releases a papain-type cysteine endopeptidase (CysEP) during the final stages of cellular disintegration. Protein cleavage sites for the Ricinus CysEP were determined with fluorogenic peptides (Abz-Xaa-Arg-/-Gln-Gln-Tyr(NO2)-Asp). The highest kcat/Km values were obtained with neutral amino acid residues with large aliphatic and non-polar (Leu, Val, Ile, Met) or aromatic (Phe, Tyr, Trp) side-chains. A second series (Abz-Leu-Xaa-/Gln-Pro-Tyr(NO2)-Asp) was evaluated. Based on these results, the covalent binding inhibitor H-D-Val-Leu-Lys-chloromethylketone (CMK) was chosen as substrate analogue for replacement in the catalytic site. Unusually, CysEP cleaved beta-casein N and C-terminal to the amino acid proline. CysEP was crystallized, its structure was solved by molecular replacement at 2.0 A resolution and refined to a R-factor of 18.1% (Rfree=22.6%). The polypeptide chain folds as in papain into two domains divided by the active site cleft, an elongated surface depression harboring the active site. The non-primed specificity subsites of the proteinase are clearly defined by the H-D-Val-Leu-Lys-CMK-inhibitor covalently bound to the active site. The absence of the occluding loop, which blocks the active site of exopeptidases at the C-terminal side of the scissile bond, identifies CysEP as an endopeptidase. The more open pocket of the Ricinus CysEP correlates with the extended variety of substrate amino acid residues accommodated by this enzyme, including even proline at the P1 and P1' positions. This may allow the enzyme to attack a greater variety of proteins during programmed cell death.

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  2. C1A cysteine-proteases and their inhibitors in plants. Martínez M, Cambra I, González-Melendi P, Santamaría ME, Díaz I. Physiol Plant 145 85-94 (2012)
  3. The structural basis of specific protease-inhibitor interactions at the plant-pathogen interface. Hörger AC, van der Hoorn RA. Curr Opin Struct Biol 23 842-850 (2013)
  4. Programmed cell death in Ricinus and Arabidopsis: the function of KDEL cysteine peptidases in development. Hierl G, Vothknecht U, Gietl C. Physiol Plant 145 103-113 (2012)
  5. 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)

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  2. Subclassification and biochemical analysis of plant papain-like cysteine proteases displays subfamily-specific characteristics. Richau KH, Kaschani F, Verdoes M, Pansuriya TC, Niessen S, Stüber K, Colby T, Overkleeft HS, Bogyo M, Van der Hoorn RA. Plant Physiol 158 1583-1599 (2012)
  3. Heterologous expression, purification, refolding, and structural-functional characterization of EP-B2, a self-activating barley cysteine endoprotease. Bethune MT, Strop P, Tang Y, Sollid LM, Khosla C. Chem Biol 13 637-647 (2006)
  4. Structural and functional characterization of Falcipain-2, a hemoglobinase from the malarial parasite Plasmodium falciparum. Hogg T, Nagarajan K, Herzberg S, Chen L, Shen X, Jiang H, Wecke M, Blohmke C, Hilgenfeld R, Schmidt CL. J Biol Chem 281 25425-25437 (2006)
  5. Ricinosomes and endosperm transfer cell structure in programmed cell death of the nucellus during Ricinus seed development. Greenwood JS, Helm M, Gietl C. Proc Natl Acad Sci U S A 102 2238-2243 (2005)
  6. Ricinosomes predict programmed cell death leading to anther dehiscence in tomato. Senatore A, Trobacher CP, Greenwood JS. Plant Physiol 149 775-790 (2009)
  7. Endoplasmic reticulum KDEL-tailed cysteine endopeptidase 1 of Arabidopsis (AtCEP1) is involved in pathogen defense. Höwing T, Huesmann C, Hoefle C, Nagel MK, Isono E, Hückelhoven R, Gietl C. Front Plant Sci 5 58 (2014)
  8. Identification of the cysteine protease Amb a 11 as a novel major allergen from short ragweed. Bouley J, Groeme R, Le Mignon M, Jain K, Chabre H, Bordas-Le Floch V, Couret MN, Bussières L, Lautrette A, Naveau M, Baron-Bodo V, Lombardi V, Mascarell L, Batard T, Nony E, Moingeon P. J Allergy Clin Immunol 136 1055-1064 (2015)
  9. Evolution of a guarded decoy protease and its receptor in solanaceous plants. Kourelis J, Malik S, Mattinson O, Krauter S, Kahlon PS, Paulus JK, van der Hoorn RAL. Nat Commun 11 4393 (2020)
  10. Ex vivo processing for maturation of Arabidopsis KDEL-tailed cysteine endopeptidase 2 (AtCEP2) pro-enzyme and its storage in endoplasmic reticulum derived organelles. Hierl G, Höwing T, Isono E, Lottspeich F, Gietl C. Plant Mol Biol 84 605-620 (2014)
  11. Expression analysis of KDEL-CysEPs programmed cell death markers during reproduction in Arabidopsis. Zhou LZ, Höwing T, Müller B, Hammes UZ, Gietl C, Dresselhaus T. Plant Reprod 29 265-272 (2016)
  12. Genome-wide comparative analysis of papain-like cysteine protease family genes in castor bean and physic nut. Zou Z, Huang Q, Xie G, Yang L. Sci Rep 8 331 (2018)
  13. Papain-Like Cysteine Protease Gene Family in Fig (Ficus carica L.): Genome-Wide Analysis and Expression Patterns. Zhai Y, Cui Y, Song M, Vainstein A, Chen S, Ma H. Front Plant Sci 12 681801 (2021)
  14. Sequence comparison, molecular modeling, and network analysis predict structural diversity in cysteine proteases from the Cape sundew, Drosera capensis. Butts CT, Zhang X, Kelly JE, Roskamp KW, Unhelkar MH, Freites JA, Tahir S, Martin RW. Comput Struct Biotechnol J 14 271-282 (2016)
  15. Involvement of Arabidopsis thaliana endoplasmic reticulum KDEL-tailed cysteine endopeptidase 1 (AtCEP1) in powdery mildew-induced and AtCPR5-controlled cell death. Höwing T, Dann M, Hoefle C, Hückelhoven R, Gietl C. PLoS One 12 e0183870 (2017)
  16. Structural insights into the substrate specificity and activity of ervatamins, the papain-like cysteine proteases from a tropical plant, Ervatamia coronaria. Ghosh R, Chakraborty S, Chakrabarti C, Dattagupta JK, Biswas S. FEBS J 275 421-434 (2008)
  17. Survey of the rubber tree genome reveals a high number of cysteine protease-encoding genes homologous to Arabidopsis SAG12. Zou Z, Liu J, Yang L, Xie G. PLoS One 12 e0171725 (2017)
  18. The role of KDEL-tailed cysteine endopeptidases of Arabidopsis (AtCEP2 and AtCEP1) in root development. Höwing T, Dann M, Müller B, Helm M, Scholz S, Schneitz K, Hammes UZ, Gietl C. PLoS One 13 e0209407 (2018)
  19. Morphological and Structural Details of Tomato Seed Coat Formation: A Different Functional Role of the Inner and Outer Epidermises in Unitegmic Ovule. Chaban IA, Gulevich AA, Kononenko NV, Khaliluev MR, Baranova EN. Plants (Basel) 11 1101 (2022)
  20. POLLEN STERILITY, a novel suppressor of cell division, is required for timely tapetal programmed cell death in rice. Che R, Hu B, Wang W, Xiao Y, Liu D, Yin W, Tong H, Chu C. Sci China Life Sci 65 1235-1247 (2022)
  21. A Novel Senescence-Specific Gene (ZmSAG39) Negatively Regulates Darkness and Drought Responses in Maize. Wang C, Gao B, Chen N, Jiao P, Jiang Z, Zhao C, Ma Y, Guan S, Liu S. Int J Mol Sci 23 15984 (2022)


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