A plant alternative to animal caspases: Subtilisin-like proteases

Cell Death and Differentiation

Volumn 18, Issue 8, 2011, Pages 1289-1297

  Vartapetian, A B ^a   Tuzhikov, A I ^a   Chichkova, N V ^a   Taliansky, M ^b   Wolpert, T J ^c  

^a MOSCOW STATE UNIVERSITY   (Russian Federation)

^b SCOTTISH CROP RESEARCH INSTITUTE   (United Kingdom)

^c OREGON STATE UNIVERSITY   (United States)

Author keywords

caspases; phytaspase; saspases; subtilisin like protein

Indexed keywords

ASPARTIC ACID; CASPASE; CASPASE 3; CASPASE 3 INHIBITOR; CASPASE INHIBITOR; ENZYME; ENZYME PRECURSOR; PENTAPEPTIDE; PHYTASPASE; PROTEINASE; RIBULOSEBISPHOSPHATE CARBOXYLASE; SASPASE; SUBTILISIN; SUBTILISIN LIKE PROTEASE; UNCLASSIFIED DRUG; VICTORIN;

ABIOTIC STRESS; APOPLAST; APOPTOSIS; ARABIDOPSIS; BIOTIC STRESS; CATALYSIS; CELLULAR DISTRIBUTION; DRUG INHIBITION; ENZYME ACTIVITY; ENZYME SPECIFICITY; ENZYME STRUCTURE; ENZYME SUBSTRATE; ENZYME SYNTHESIS; FUNGUS; INTERCELLULAR SPACE; OAT; OSMOTIC STRESS; OXIDATIVE STRESS; PLANT; PLANT CELL; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN HYDROLYSIS; PROTEIN PROCESSING; PROTEIN SECRETION; REGULATORY MECHANISM; REVIEW; RIBOSOME; RICE; TOBACCO; VIRUS INFECTION;

ANIMALS; APOPTOSIS; CASPASES; CATALYTIC DOMAIN; CYSTEINE PROTEINASE INHIBITORS; ISOENZYMES; MODELS, MOLECULAR; PHYLOGENY; PLANT PROTEINS; PLANTS; PROTEIN CONFORMATION; SUBTILISIN;

ANIMALIA;

EID: 79960260879     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/cdd.2011.49     Document Type: Review

References (58)

1. Williams B, Dickman M. Plant programmed cell death: can't live with it; can't live without it. Mol Plant Pathol 2008; 9: 531-544. (Pubitemid 351832399)
2. Reape TJ, Molony EM, McCabe PF. Programmed cell death in plants: distinguishing between different modes. J Exp Bot 2008; 59: 435-444. (Pubitemid 351640731)
3. Reape TJ, McCabe PF. Apoptotic-like regulation of programmed cell death in plants. Apoptosis 2010; 15: 249-256.
4. del Pozo O, Lam E. Caspases and programmed cell death in the hypersensitive response of plants to pathogens. Curr Biol 1998; 8: 1129-1132. (Pubitemid 28501377)
5. Bonneau L, Ge Y, Drury GE, Gallois P. What happened to plant caspases? J Exp Bot 2008; 59: 491-499. (Pubitemid 351640745)
6. del Pozo O, Lam E. Expression of the baculovirus p35 protein in tobacco affects cell death progression and compromises N gene-mediated disease resistance response to tobacco mosaic virus. Mol Plant Microbe Interact 2003; 16: 485-494. (Pubitemid 36610721)
7. Hatsugai N, Kuroyanagi M, Yamada K, Meshi T, Tsuda S, Kondo M et al. A plant vacuolar protease, VPE, mediates virus-induced hypersensitive cell death. Science 2004; 305: 855-858. (Pubitemid 39038418)
8. Rojo E, Martín R, Carter C, Zouhar J, Pan S, Plotnikova J et al. VPEgamma exhibits a caspase-like activity that contributes to defense against pathogens. Curr Biol 2004; 14: 1897-1906. (Pubitemid 39464812)
9. Hatsugai N, Iwasaki S, Tamura K, Kondo M, Fuji K, Ogasawara K et al. A novel membrane fusion-mediated plant immunity against bacterial pathogens. Genes Dev 2009; 23: 2496-2506.
10. Dodson G, Wlodawer A. Catalytic triads and their relatives. Trends Biochem Sci 1998; 23: 347-352. (Pubitemid 28461867)
11. Rawlings ND, Barrett AJ, Bateman A. MEROPS: the peptidase database. Nucleic Acids Res 2010; 38: D227-D233.
12. Tripathi LP, Sowdhamini R. Cross genome comparisons of serine proteases in Arabidopsis and rice. BMC Genomics 2006; 7: 200-231.
13. Rautengarten C, Steinhauser D, Bü ssis D, Stintzi A, Schaller A, Kopka J et al. Inferring hypotheses on functional relationships of genes: analysis of the Arabidopsis thaliana subtilase gene family. PLoS Comput Biol 2005; 1: e40.
14. Baker D, Sohl JL, Agard DA. A protein-folding reaction under kinetic control. Nature 1992; 356: 263-265.
15. Ottmann C, Rose R, Huttenlocher F, Cedzich A, Hauske P, Kaiser M et al. Structural basis for Ca2+-independence and activation by homodimerization of tomato subtilase 3. Proc Natl Acad Sci USA 2009; 106: 17223-17228.
16. Yamagata H, Masuzawa T, Nagaoka Y, Ohnishi T, Iwasaki T. Cucumisin, a serine protease from melon fruits, shares structural homology with subtilisin and is generated from a large precursor. J Biol Chem 1994; 269: 32725-32731.
17. Schaller A. A cut above the rest: the regulatory function of plant proteases. Planta 2004; 220: 183-197. (Pubitemid 40084177)
18. Von Groll U, Berger D, Altman T. The Subtilisin-like serine protease SDD1 mediates cell-to-cell signaling during Arabidopsis stomatal development. Plant Cell 2002; 14: 1527-1539. (Pubitemid 34817141)
19. Tanaka H, Onouchi H, Kondo M, Hara-Nishimura I, Nishimura M, Machida C et al. A subtilisin-like serine protease is required for epidermal surface formation in Arabidopsis embryos and juvenile plants. Development 2001; 128: 4681-4689. (Pubitemid 33138579)
20. Rautengarten C, Usadel B, Neumetzler L, Hartmann J, Bü ssis D, Altmann T. A subtilisinlike serine protease essential for mucilage release from Arabidopsis seed coats. Plant J 2008; 54: 466-480. (Pubitemid 351585493)
21. Tan-Wilson AL, Liu X, Chen R, Qi X, Wilson KA. An acidic amino acid-specific protease from germinating soybeans. Phytochemistry 1996; 42: 313-319. (Pubitemid 126655023)
22. Boyd PM, Barnaby N, Tan-Wilson A, Wilson KA. Cleavage specificity of the subtilisin-like protease C1 from soybean. Biochim Biophys Acta 2002; 1596: 269-282. (Pubitemid 34455052)
23. Liu JX, Srivastava R, Che P, Howell SH. Salt stress responses in Arabidopsis utilize a signal transduction pathway related to endoplasmic reticulum stress signaling. Plant J 2007; 51: 897-909. (Pubitemid 47301665)
24. Wolf S, Rausch T, Greiner S. The N-terminal pro region mediates retention of unprocessed type-I PME in the Golgi apparatus. Plant J 2009; 58: 361-375.
25. Srivastava R, Liu JX, Guo H, Yin Y, Howell SH. Regulation and processing of a plant peptide hormone, AtRALF23, in Arabidopsis. Plant J 2009; 59: 930-939.
26. Srivastava R, Liu JX, Howell SH. Proteolytic processing of a precursor protein for a growth-promoting peptide by a subtilisin serine protease in Arabidopsis. Plant J 2008; 56: 219-227.
27. Jordá L, Coego A, Conejero V, Vera P. A genomic cluster containing four differentially regulated subtilisin-like processing protease genes is in tomato plants. J Biol Chem 1999; 274: 2360-2365.
28. Tornero P, Conejero V, Vera P. Primary structure and expression of a pathogen-induced protease (PR-P69) in tomato plants: similarity of functional domains to subtilisin-like endoproteases. Proc Natl Acad Sci USA 1996; 93: 6332-6337.
29. Wolpert TJ, Macko V, Acklin W, Jaun B, Seibl J, Meili J et al. Structure of victorin C, the major host-selective toxin from Cochliobolus victoriae. Experientia 1985; 41: 1524-1529. (Pubitemid 16212485)
30. Wolpert TJ, Macko V, Acklin W, Jaun B, Arigoni D. Structure of minor host-selective toxins from Cochliobolus victoriae. Experientia 1986; 42: 1296-1299.
31. Wolpert TJ, Dunkle LD, Ciuffetti LM. Host-selective toxins and avirulence determinants: What's in a name? Ann Rev Phytopathol 2002; 40: 251-285. (Pubitemid 35235582)
32. Welsh JN, Peturson B, Machacek JE. Associated inheritance of reaction to races of crown rust, Puccinia coronata avenae Erikss., and to Victoria blight, Helminthosporium victoriae Mand M., in oats. Can J Bot 1954; 32: 55-68.
33. Mayama S, Bordin APA, Morikawa T, Tanpo H, Kato H. Association of avenalumin accumulation with co-segregation of victorin sensitivity and crown rust resistance in oat lines carrying the Pc-2 gene. Physiol Mol Plant Pathol 1995; 46: 263-274.
34. Lorang JM, Carkaci-Salli N, Wolpert TJ. Identification and characterization of victorin sensitivity in Arabidopsis thaliana. Mol Plant Microb Interact 2004; 17: 577-582. (Pubitemid 38642201)
35. Lorang JM, Sweat TA, Wolpert TJ. Plant disease susceptibility conferred by a 'resistance' gene. Proc Natl Acad Sci USA 2007; 37: 14861-14866. (Pubitemid 350003233)
36. Sweat TA, Lorang JM, Bakker EG, Wolpert TJ. Characterization of natural and induced variation in the LOV1 gene, a CC-NB-LRR gene conferring victorin sensitivity and disease susceptibility in Arabidopsis. Mol Plant Microbe Interact 2008; 21: 7-19. (Pubitemid 350262357)
37. Yao N, Tada Y, Park P, Nakayashiki H, Tosa Y, Mayama S. Novel evidence for apoptotic cell response and differential signals in chromatin condensation and DNA cleavage in victorin-treated oats. Plant J 2001; 28: 13-26. (Pubitemid 33011506)
38. Curtis MJ, Wolpert TJ. The victorin induced mitochondrial permeability transition precedes cell shrinkage and biochemical markers of cell death and shrinkage occurs without loss of membrane integrity. Plant J 2004; 38: 244-259. (Pubitemid 38503726)
39. Navarre DA, Wolpert TJ. Victorin induction of an apoptotic/senescence- like response in oats. Plant Cell 1999; 11: 237-249.
40. Tada Y, Hata S, Takata Y, Nakayashiki H, Tosa Y, Mayama S. Induction and signaling of an apoptotic response typified by DNA laddering in the defense response of oats to infection and elicitors. Mol Plant Microbe Interact 2001; 14: 477-486. (Pubitemid 32235581)
41. Curtis MJ, Wolpert TJ. The oat mitochondrial permeability transition and its implication in victorin binding and induced cell death. Plant J 2002; 29: 295-312. (Pubitemid 34179489)
42. Coffeen WC, Wolpert TJ. Purification and characterization of serine proteases that exhibit caspase-like activity and are associated with programmed cell death in oats. Plant Cell 2004; 16: 857-873. (Pubitemid 38459207)
43. Powers JC, Asgian JL, Ekici OD, James KB. Irreversible inhibitors of serine cysteine and threonine proteases. Chem Rev 2002; 102: 4639-4750.
44. Bernard D, Mé hul B, Thomas-Collignon A, Delattre C, Donovan M, Schmidt R. Identification and characterization of a novel retroviral-like aspartic protease specifically expressed in human epidermis. J Invest Dermatol 2005; 125: 278-287. (Pubitemid 41648161)
45. Balk J, Leaver CJ, McCabe PF. Translocation of cytochrome c from the mitochondria to the cytosol occurs during heat-induced programmed cell death in cucumber plants. FEBS Lett 1999; 463: 151-154. (Pubitemid 30001737)
46. Tian R-H, Zhang G-Y, Yan C-H, Dai Y-R. Involvement of poly(ADP-ribose) polymerase and activation of caspase-3-like protease in heat shock-induced apoptosis in tobacco suspension cells. FEBS Lett 2000; 474: 11-15. (Pubitemid 30320823)
47. Chichkova NV, Kim SH, Titova ES, Kalkum M, Morozov VS, Rubtsov YP et al. A plant caspase-like protease activated during the hypersensitive response. Plant Cell 2004; 16: 157-171. (Pubitemid 38162360)
48. Chichkova NV, Galiullina RA, Taliansky ME, Vartapetian AB. Tissue disruption activates a plant caspase-like protease with TATD cleavage specificity. Plant Stress 2008; 2: 89-95.
49. Chichkova NV, Shaw J, Galiullina RA, Drury GE, Tuzhikov AI, Kim SH et al. Phytaspase, a relocalisable cell death promoting plant protease with caspase specificity. EMBO J 2010; 29: 1149-1161.
50. Fuentes-Prior P, Salvesen GS. The protein structures that shape caspase activity, specificity, activation and inhibition. Biochem J 2004; 384: 201-232. (Pubitemid 39656233)
51. Cedzich A, Huttenlocher F, Kuhn BM, Pfannstiel J, Gabler L, Stintzi A et al. The proteaseassociated domain and C-terminal extension are required for zymogen processing, sorting within the secretory pathway, and activity of tomato subtilase 3 (SlSBT3). J Biol Chem 2009; 284: 14068-14078.
52. Fontanini D, Jones BL. SEP-1 - a subtilisin-like serine endopeptidase from germinated seeds of Hordeum vulgare L.cv. Morex. Planta 2002; 215: 885-893. (Pubitemid 36080246)
53. Steiner DF. The proprotein convertases. Curr Opin Chem Biol 1998; 2: 31-39. (Pubitemid 128419196)
54. Howard EA, Zupan JR, Citovsky V, Zambryski PC. The VirD2 protein of A. tumefaciens contains a C-terminal bipartite nuclear localization signal: implications for nuclear uptake of DNA in plant cells. Cell 1992; 68: 109-118.
55. Reavy B, Bagirova S, Chichkova NV, Fedoseeva SV, Kim SH, Vartapetian AB et al. Caspase-resistant VirD2 protein provides enhanced gene delivery and expression in plants. Plant Cell Rep 2007; 26: 1215-1219. (Pubitemid 47124991)
56. Eswar N, Webb B, Marti-Renom MA, Madhusudhan MS, Eramian D, Shen MY et al. Comparative protein structure modeling using Modeller. Curr Protoc Bioinform 2006; Chapter 5, Unit 5.6.
57. Bikadi Z, Hazai E. Application of the PM6 semi-empirical method to modeling proteins enhances docking accuracy of AutoDock. J Cheminform 2009; 1: 15.
58. Ordog R. PyDeT, a PyMOL plug-in for visualizing geometric concepts around proteins. Bioinformation 2008; 2: 346-347.