Programmed cell death in plants resembles apoptosis of animals

Biotecnologia Aplicada

Volumn 23, Issue 1, 2006, Pages 1-10

  Collazo, Cyrelys ^a   Chacón, Osmani ^b   Borrás, Orlando ^a  

^a CENTER FOR GENETIC ENGINEERING AND BIOTECHNOLOGY   (Cuba)

^b Tobacco Research Institute   (Cuba)

Author keywords

Apoptosis; Caspases; Ion fluxes; Mitochondria; Mitogen activated protein kinases; Programmed cell death; Reactive oxygen species

Indexed keywords

HYDROLASE; TOXIN;

APOPTOSIS; CELL DEATH; CELL VACUOLE; CELL WALL; CONTROLLED STUDY; GENE EXPRESSION; HYDROLYSIS; NONHUMAN; PHAGOCYTOSIS; PLANT CELL; PLANT GENETICS; REVIEW;

ANIMALIA;

EID: 34548528580     PISSN: 08644551     EISSN: 10272852     Source Type: Journal    
DOI: None     Document Type: Review

References (110)

1. Gilchrist DG. Programmed cell death in plant disease: the purpose and promise of cellular suicide. Annu Rev Phytopathol 1998;36:393-414.
2. Okada H, Mak TW. Pathways of apoptotic and non-apoptotic death in tumour cells. Nature reviews 2004;4:592-603.
3. Kerr JFR, Willie AH, Currie AR. Apoptosis: a basical phenomenon with wide ranging implications in tissue kinetics. Br J Cancer 1972;26:239-57.
4. Pennel RI, Lamb C. Programmed cell death in plants. Plant Cell 1997;9:1157-68.
5. Kurana SMP, Pandey SK, Sarkas D, Chanemougasoundharam A. Apoptosis in plant disease response:a close encounter of the pathogen kind. Curr Sci 2005;88:740-52.
6. Goodman RN, Novacky AJ. The hypersensitive reaction in plants to pathogens: a resistance phenomenon. Amer Phyto - pathol Soc Press, St. Paul 1996.
7. Drew MC, He CJ, Morgan PW. Programmed cell death and aerenchyma formation in roots. Trends in Plant Science 2000;5:123-7.
8. McCabe PF, Leaver CL. Programmed cell death in cell cultures. Plant Molecular Biology 2000;44:359-68.
9. Darzynkiewiks Z, Bruno S, Bino G, Gorezca W, Hotz MA, Lassota P, Trganos F. Features of apoptotic cells measured by flow cytometry. Cytometry 1992;13:795-808.
10. Cutler SR, Sommerville CR. Imaging cell death: GFP-Nit1 aggregation marks an early step of wound and herbicide induced cell death. BMC Plant Biol 2005;5:1-15.
11. Cohen GM, Sun X, Fearnhead H, Macfarlane M, Brown DJ, Snowden RT, Dinsdale D. Formation of large molecular weight fragments of DNA is a key committed step of apoptosis in thymocites. J Inmunol 1994;153:507-16.
12. Gavireli Y, Sherman Y, Ben- Sasson SA. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J Cell Biol 1992;119:493-501.
13. Mitler R, Lam E. Pathogen-induced programmed cell death in tobacco. Plant Mol Biol 1997;34:209-21.
14. Ryerson DE, Heath Mc. Cleavage of nuclear DNA into oligonucleosomal fragments during cell death induced by fungal infection or by abiotic treatments. Plant Cell 1996;8:393-402.
15. Wang H, Bostock RM, Gilchrist DG. Apoptosis: A functional paradigm for programmed cell death induced by a host-selective phytotoxin and invoked during development. Plant Cell 1996;8:375-91.
16. O'Brien IE, Baguley BC, Murray BG, Morris BA, Ferguson IB. Early stages in the apoptotic pathway in plant cells are reversible. Plant J 1998;13:803-14.
17. Mitler R, Lam E. Identification, characterization and purification of a tobacco endonuclease activity upon hypersensitive response cell death. Plant Cell 1995;7:1951-62.
18. Gunawardena A, Greenwood JS, Dengler N. Programmed cell death remodels lace plant leaf shape during development. Plant Cell 2004;16:70-3.
19. Tyurina YY, Tyurina VA, Zhaoa O, Djukica M, Quinnd PJ, Pitta BJ, Kagan VE. Oxidation of phosphatidylserine: a mechanism for plasma membrane phospholipid scrambling during apoptosis Biochem Biophys Res Com 2004;324:1059-64.
20. Kagan VE, Fabisiak JP, Shvedova AA, Tyurina YY, Tyurin VA, Schor NF, Kawai K. Oxidative signalling pathway for externalization of plasma membrane phosphatidylserine during apoptosis. FEBS Lett. 2000;477:1-7.
21. Ferraro-Peyret C, Quemeneur L, Flacher M, Revillard JP, Genestier L. Caspase-independent phosphatidyl - serine exposure during apoptosis of primary T- lymphocytes. J Immunol 2002;169:4805-10.
22. Xu CJ, Chen KS, Ferguson IB. Programmed cell death feature in apple suspension cells under low oxygen culture. J Zhejiang Univ Sci 2004;5:137-43.
23. Wang M, Oppedijk BJ, Lu X, Van Duijn B, Schilperoort RA. Apoptosis in barley aleurone during germination and its inhibition by abscisic acid. Plant Mol Biol 1996;32:1125-34.
24. McCabe PF, Pennell R I. In Techniques in Apoptosis (eds Kotter TG, Martin SJ), Portland Press, London, 1996:301-26.
25. Lai V, Srivastava LM. Nuclear changes during differentiation of xylem vessel elements. Cytobiol 1976;12:220-43.
26. Greenberg JT, Yao N. The role and regulation of programmed cell death in plant-pathogen interactions. Cell Microbiol 2004;6:201-11.
27. Groover A, Jones AM. Tracheary element differentiation uses a novel mechanism coordinating programmed cell death and secondary cell wall synthesis. Plant Physiol 1999;119:375-84.
28. Kam PCA. Apoptosis: mechanisms and clinical implications. Anaesthesia 2000;55:1081-93.
29. Jones AM. Programmed cell death in development and defense. Plant Physiol 2001;125:94-7.
30. Jones A. Does the plant mitochondrion integrate cellular stress and regulate programmed cell death Trends in Plant Sci 2000;5:1360-85.
31. Schussler EE, Longstreth DJ. Changes in cell structure during the formation of root aerenchyma in Sagittaria lancifolia (Alismataceae) Am J Bot 2000;87:12-9.
32. Beers EP, McDowell. Regulation and execution of programmed cell death in response to pathogens, stress and developmental cues. Curr Op Plant Biol 2001;4:561-7.
33. Filonova LH, Bozhkov PV, Brukhin VB, Daniel G, Zhivotovsky B, von Arnold S. Two waves of programmed cell death occur during formation and development of somatic embryos in the gymnosperm, Norway spruce. J Cell Sci 2000;113:4399-411.
34. Kim J, Kilonsky DJ. Autophagy, cytoplasm-to-vacuole targeting pathway, and pexophagy in yeast and mammalian cells. Annu Rev Biochem 2000;69:303-42.
35. Regiori F, Kilonski DJ. Autophagy in the eukaryotic cell. Eukaryot Cell 2002;1:11-21.
36. Nakashima J, Takabe M, Fukuda H. Autolysis during in vitro tracheary element differentiation: Formation and location of the perforation. Plant Cell Physiol 2000;4:1267-71.
37. He X, Kermode AR. Nuclease activities and DNA fragmentation during programmed cell death of megaga-metophyte cells of white spruce (Picea glauca) seeds. Plant Mol Biol 2003;51:509-21.
38. Kozela C, Regan S. How plants make tubes. Trends in Plant Sci 2003;8:159-64.
39. Meitzstein MM, Stanfield GM, Horvittz HR. Genetics of programmed cell death in C. elegans: past, present and future. Trends Genetic 1998;14:410-6.
40. Green DR, Reed JC. Mitochondria and apoptosis. Science 1998;281:1309-12.
41. Thornberry NA, Rosen A, Nicholson DW. Control of apoptosis by proteases. Adv in Pharmacol 1997;41:155-77.
42. Grutter MG. Caspases: key players in programmed cell death. Curr Opin Struct Biol 2000;10:649-55.
43. Koonin EV, Aravind L. Classification of the caspase-hemoglobinase fold: detection of new families and implications for the origin of the eukaryotic separins. Proteins 2002;46:355-67.
44. Woltering EJ, Van der Bent A, Hoeberichts A. Do plant caspases exist Plant Physiol 2002;130:1764-9.
45. Krishnamurthy KV, Krishnaraj R, Chozhavendan R, Samuel Christopher F. The programme of cell death in plants and animals. A comparison. Current Science 2000;79(9):1169-81.
46. Lam E, del Pozo O. Caspase-like protease involvement in the control of plant cell death. Plant Mol Biol 2000;44:417-28.
47. Bozhkov PV, Filonova LH, Suarez MF, Helmersson A, Smertenko AP, Zhivotovsky B, Von Arnold S. VEIDase is a principal caspase-like activity involved in plant programmed cell death and essential for embryonic pattern formation. Cell Death Differ 2004;11:175-82.
48. Madeo F, Herker E, Maldener C, Wissing S, Lachelt S, Herlan M, Fehr M, Lauber K, Sigrist SJ, Wesselborg S, Frohlich KU. A caspase-related protease regulates apoptosis in yeast. Mol Cell 2002;9:911-7.
49. Hoeberichts FA, Ten Have A, Woltering EJ. A tomato metacaspase gene is upregulated during programmed cell death in Botrytis cinerea infected leaves. Planta 2003;217:517-22.
50. Mlejnek P, Prochazka, S. Activation of caspase-like proteases and induction of apoptosis by isopentenyladenosine in tobacco BY-2 cells. Planta 2002;215:158-66.
51. Lincoln JE, Richael C, Overduin B, Smith K, Bostock R, Gilchrist DG. Expression of the antiapoptotic baculovirus p35 gene in tomato blocks programmed cell death and provides broad-spectrum resistance to disease. Proc Natl Acad Sci USA 2002;99:15217-21.
52. Chichkova NV, Kim SH, Titova ES, Kalkum M, Morozov VS, RubtsovYP, Kalinina NO, Taliansky ME, Vartapetian AB. A plant caspase-like protease activated during the hypersensitive response. Plant Cell 2004;16:157-71.
53. D'Silva I, Poirier GG, Heath M. Activation of cysteine proteases in cowpea plants during the hypersensitive response-a form of programmed cell death. Exp Cell Res 1998;245:389-99.
54. Rotari VI, Dando PM, Barrett AJ. Legumain forms from plants and animals differ in their specificity. Biol Chem 200 1;382:953-9.
55. Hatsugai N, Kuroyanagi M, Yamada K, Meshi T, Tsuda S, Kondo M, Nishimura M, Hara-Nishimura I. A plant vacuolar protease, VPE, mediates virus-induced hypersensitive cell death. Science 2004;305:855-8.
56. Krishnamurthy KV, Krishnaraj R, Chozhavendan R, Christopher FS. The programme of cell death in plants and animals- A comparison. Curr Sci 2000;79:1169-81.
57. Aron JL, Parthun MR, Marcucci G, Kitada S, Mone AP, Davis ME, Shen T, Murphy T, Wickham J, Kanakry C, Lucas DM, Reed JC, Grever MR, Byrd JC. Depsipeptide (FR901228) induces histone acetylation and inhibition of histone deacetylase in chronic lymphocytic leukemia cells concurrent with activation of caspase 8-mediated apoptosis and down-regulation of c- FLIP protein. Blood 2003;102:652-8.
58. Cain K, Bratton SB, Cohen GM. The Apaf-1apoptosome: a large caspaseactivating complex. Biochimie 2002;84:203-14.
59. Stein JC, Hansen G. Mannose induces an endonuclease responsible for DNA laddering in plant cells. Plant Physiol 1999;121:71-9.
60. Perl A, Gergely P, Nagy G, Koncz A, Banki K. Mitochondrial hyperpola - rization: a checkpoint of T-cell life, death and autoimmunity. Trend in Plant Sci 2004;25:360-7.
61. Wei M, Zong WZ, Cheng EH, Lindten T, Panoutsakopoulou V, Ross A, Roth KA, MacGregor GR, Thompson CB, Korsmeyer SJ. Proapoptotic BAK and BAX: A requisite gateway to mitochondrial dysfunction and death. Science 2001;292:727-30.
62. Dion M, Chamberlain H, St-Michel C, Plante M, Darveau A, Lafontaine JG. Detection of a homologue to Bcl-2 in plant cells. Biochem Cell Biol 1997; 75:457-61.
63. Dickman MB, Oltersdorf T, Li W, Clemente T, French R. Abrogation of disease development in plants expressing animal antiapoptotic genes. Proc Natl Acad Sci USA 2001;98:6957-62.
64. Lancomme C, Roby D. Identification of new early markers of the hypersensitive response in Arabidopsis thaliana. FEBS Lett 1999;459:149-53.
65. Sanchez P, Zabala MD, Grant M. AtBI-1, plant homolog of Bax Inhibitor-1, supress Bax induced cell death in yeast and is rapidly upregulated during wounding and pathogen challenge. Plant J 2000;21:393-9.
66. Ordog SH, Higgins VJ, Vanlerberghe GC. Mitochondrial alternative oxidase is not a critical component of plant viral resistance but may play a role in the hypersensitive response. Plant Physiol 2002;129:1858-65.
67. Vanlerberghe GC, Robson CA, Yip, JYH. Induction of mitochondrial alternative oxidase in response to a cell signal pathway down-regulating the cytochrome c path - way prevents programmed cell death. Plant Physiol 2002;129:1829-42.
68. Maxwell DP, Wang Y, McIntosh L. The alternative oxidase lowers mitochondrial reactive oxygen production in plant cells. Proc Natl Acad Sci USA 1999; 96: 8271-6.
69. Deveraux QL, Reed JC. IAP family proteins-suppressors of apoptosis. Genes Dev 1999;13:239-52.
70. Verhagen AM, Coulson EJ, Vaux DL. Inhibitor of apoptosis proteins and their relatives: IAPs and other BIRPs. Genome Biol 2001;2:3009.
71. Du C, Fang M, Li Y, Li L, Wang X. Smac, a mitochondrial protein that promotes cytochrome c-dependent caspase activation by eliminating IAP inhibition. Cell 2000;102:33-42.
72. Verhagen AM, Ekert PG, Pakusch M, Silke J, Connolly LM, Reid GE, Moritz RL, Simpson RJ, Vaux DL. Identification of DIABLO, a mammalian protein that promotes apoptosis by binding to and antagonizing IAP proteins. Cell 2000;102:43-53.
73. Rudin CM, Thompson CB. Apoptosis and disease:regulation and clinical relevance of programmed cell death. Annual Review of Medicine 1997;48:267-81.
74. Van der Biezen EA, Jones JD. The NBARC domain: a novel signalling motif shared by plant resistance gene products and regulators of cell death in animals. Curr Biol 1998;8:226-67.
75. Inohara N, Koseki T, del Paso L, Hu Y, Yee C, Chen S, Cario R, Merino J, Liu D, Ni J, Nuñez G. Nod 1, an Apaf-1-like activator of caspase 9 and nuclear factor-kappa B. J Biol Chem 1999;274:14560-7.
76. Heath M. Hypersensitive response-related cell death. Plant Mol Biol 2000;44:321-34.
77. Jin HL, Liu YD, Yang KY, Kim CY, Baker B, Zhang SQ. Function of mitogen-activated protein kinase pathway in N gene-mediated resistance in tobacco. Plant J, 2003;33:719-31.
78. Ren D, Yang H, Zhang S. Cell death mediated by MAPK is associated with hydrogen peroxide production in Arabidopsis. J Chem Biol 2002;4:559-65.
79. Yamakawa H, Katou S, Seo S, Mitsuhara I, Kamada H, Ohashi Y. Plant mitogen-activated protein kinase phosphatase interacts with calmodulins. J Biol Chem 2004;279:928-36.
80. Gaitanaki C, Konstantina S, Chrysa S, Beis I. Oxidative stress stimulates multiple MAPK signalling pathways and the phosphorylation of the small HSP27 in the perfused amphibian heart. J Exp Biol 2003;206:2759-69.
81. Grethe S, Ares MP, Andersson T, Porn-Ares MI. p38 MAPK mediates TNF-induced apoptosis in endothelial cells via phosphorylation and downregulation of Bcl-x(L). Exp Cell Res 2004;298:632-42.
82. Larbi A, Douziech N, Fortin C, Linteau A, Dupuis G, Fulop T Jr. The role of the MAPK pathway alterations in GM-CSF modulated human neutrophil apoptosis with aging. Immun Ageing 2005;2:6.
83. Scheid MP, Schubert KM, Duronio V: Regulation of Bad phosphorylation and association with Bcl-xL by the MAPK/Erk kinase. J Biol Chem 1999;274:31108-13.
84. Holmström TH, Schmitz I, Söderström TS, Poukkula M, Johnson VL, Chow SC, Krammer PH, Eriksson JE. MAPK/ERK signalling in activated T cells inhibits CD95/Fas-mediated apoptosis downstream of DISC assembly. EMBO J 2000;19:5418-28.
85. Hannun YA, Obeid LM. The ceramide-centric universe of lipid-mediating cell regulation: Stress encounters of the lipid kind. J Biol Chem 2002;277:25847-50.
86. Liang H, Yao N, Song JT, Luo S, Lu H, Greenberg JT. Ceramides modulate programmed cell death in plants. Genes Dev 2003;17:2636-41.
87. Sugiura M, Kono K, Liu H, Shimizugawa T, Minekura H, Spiegel S, Kohama T. Ceramide kinase, a novel lipid kinase. J Biol Chem 2002;277:23294-300.
88. Lynch DV. Enzymes of sphingolipid metabolism in plants. In Sphingolipid Metabolism (eds Merrill AH, Hannun YA), Academic Press, (San Diego) 2000:130-49.
89. Imai H, Nishiura H. Phosphorylation of sphingoid long-chain bases in Arabidopsis: functional characterization and expression of the first sphingoid longchain base kinase gene in plants. Plant Cell Physiol 2005;46:375-80.
90. Spassieva SD, Markham JE, Hille J. The plant disease resistance gene Asc-1 prevents disruption of sphingolipid metabolism during AAL-toxin-induced programmed cell death. Plant J 2002;32:561-2.
91. Brandwagt BF, Mesbah LA, Takken FL, Laurent PL, Kneppers TJ, Hille J, Nijkamp HJ. A longevity assurance gene homolog of tomato mediates resistance to Alternaria alternata f.sp. lycopersici toxins and fumonisin B1. Proc Natl Acad Sci USA 2000;97:4961-6.
92. Brandwagt BF, Kneppers TJ,. Van der Weerden GM, John J. Nijkamp HJ, Hille J Most AAL toxin-sensitive Nicotiana species are resistant to the tomato fungal pathogen MPMI 2001;14:460-70.
93. Delledonne M, Zeier J, Marocco A, Lamb C. Signal interactions between nitric oxide and reactive oxygen intermediates in the plant hypersensitive disease resistance response. Proc Natl Acad Sci (USA) 2001;98:13454-9.
94. Wendehenne D, Lamotte O, Frachisse J-M, Barbier-Brygoo H, Pugin A. Nitrate efflux is an essential component of the cryptogein signalling pathway leading to defense responses and hypersensitive cell death in tobacco. Plant Cell 2002; 14:1937-51.
95. Hancock JT, Desikan R, Clarke A, Hurst RD, Neill SJ. Cell signalling following plant/pathogen interactions involves the generation of reactive oxygen and reactive nitrogen species. Plant Physiol Biochem 2002;40:611-7.
96. Nakagami H, Kiegerl S, Hirt H. OMTK1, a novel MAPKKK, channels oxidative stress signalling through direct MAPK interaction. J Biol Chem 2004;279:26959-66.
97. Gechev TS, Hille J. Hydrogen peroxide as a signal controlling plant programmed cell death. J Cell Biol 2005;168:17-20.
98. Alamillo JM, Garcia-Olmedo F. Effects of urate, a natural inhibitor of peroxynitrite-mediated toxicity, in the response of Arabidopsis thaliana to the bacterial pathogen Pseudomonas syringae. Plant J 2001;25:529-40.
99. Tada Y, Mori T, Shinogi T, Yao N, Takahashi S, Betsuyaku S, Sakamoto M, Park P, Nakayashiki H, Tosa Y. Nitric oxide and reactive oxygen species do not elicit hypersensitive cell death but induce apoptosis in the adjacent cells during the defense response of oat. Mol Plant Microbe Interact 2004;17: 245-53.
100. Zhang C, Czymmek KJ, Shapiro AD. Nitric oxide does not trigger early programmed cell death events but may contribute to cell-to-cell signalling governing progression of the Arabi-dopsis hypersensitive response. Mol Plant-Microb Interact 2003;16:962-72.
101. Delledone M. NO news is good news for plants. Curr Opin Plant Biol 2005; 8:390-6.
102. Daiber A, Frein D, Namgaladze D, Ullrich V. Oxidation and nitrosation in the nitrogen monoxide/superoxide system. J Biol Chem 2002;14:11882-8.
103. Kurusu T, Yagala T, Miyao A, Hirochika H, Kuchitsu K. Identification of a putative voltage-gated Ca2+ channel as a key regulator of elicitor-induced hypersensitive cell death and mitogen-activated protein kinase activation in rice. Plant J 2005;42:798.
104. Fernán dez-Fernandez JM, Nobles M, Currid A, Vazquez E, Valcerde MA. Maxi K+ channel mediates regulatory volume decrease response in a human bronchial epithelial cell line. Am J Physiol Lung Cell Moll Physiol 2002;283:L1705-14.
105. Remillard CV, Yuan JXJ. Activation of K+ channels: an essential pathway in programmed cell death. Am J Physiol Lung Mol Physiol 2004;286:L49-67.
106. Bossy-Wetzel, Schwarzenbacher R, Lipton S. Molecular pathways to neurodeneration. Nature Med 2004;10:S2-9.
107. Vailleau F, Daniel X, Tronchet M, Montillet JL, Triantaphylides C, Roby D. A R2R3-MYB gene, AtMYB30, acts as a positive regulator of the hypersensitive cell death program in plants in response to pathogen attack. Proc Natl Acad Sci USA 2002;99:10179-84.
108. Keller H, Pamboukdjian N, Ponchet M, Poupet A, Delon R, Verrier JL, Roby D, Ricci P. Pathogen-induced elicitin production in transgenic tobacco generates a hyper -sensitive response in nonspecific disease resistance. Plant Cell 1999;11:223-35.
109. Hammond-Kosack KE, Tang S, Harrison K, Jones JDG. The tomato cf-9 disease resistance gene functions in tobacco and potato to confer responsive-ness to the fungal avirulence gene product Avr9. Plant Cell 1996;10:1251-66.
110. 2+ concentrations and pHs. Plant Cell Physiol 2004;45:1371-9.