Skip to main content
SpringerLink
Log in

Ribosome Inactivating Proteins and Apoptosis

  • Chapter
  • First Online:
Toxic Plant Proteins

Part of the book series: Plant Cell Monographs ((CELLMONO,volume 18))

Abstract

Ribosome inactivating proteins (RIPs) are RNA N-glycosidases which potently inhibit translation by inactivating ribosomes. RIPs have also been shown to possess the ability to induce apoptosis. A number of RIPs from different sources have been used to study the mechanism of apoptosis induction. However, it is being observed that these toxins trigger apoptosis in different cell types via different mechanisms; although in most cases mitochondria have been involved, no single common pathway that is followed by the RIPs for apoptosis induction has emerged. There appears to be a consensus that the protein synthesis inhibition and induction of apoptosis by RIPs are independent of each other. In this chapter, we bring together the available studies on apoptosis induction by RIPs.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Adams JM, Cory S (2001) Life-or-death decisions by the Bcl-2 protein family. Trends Biochem Sci 26:61–66

    Article  PubMed  CAS  Google Scholar 

  • Allam M, Bertrand R, Zhang-Sun G, Pappas J, Viallet J (1997) Cholera toxin triggers apoptosis in human lung cancer cell lines. Cancer Res 57:2615–2618

    PubMed  CAS  Google Scholar 

  • Bagga S, Seth D, Batra JK (2003) The cytotoxic activity of ribosome-inactivating protein saporin-6 is attributed to its rRNA N-glycosidase and internucleosomal DNA fragmentation activities. J Biol Chem 278:4813–4820

    Article  PubMed  CAS  Google Scholar 

  • Bantel H, Engels IH, Voelter W, Schulze-Osthoff K, Wesselborg S (1999) Mistletoe lectin activates caspase-8/FLICE independently of death receptor signaling and enhances anticancer drug-induced apoptosis. Cancer Res 59:2083–2090

    PubMed  CAS  Google Scholar 

  • Barbieri L, Battelli MG, Stirpe F (1993) Ribosome-inactivating proteins from plants. Biochim Biophys Acta 1154:237–282

    Article  PubMed  CAS  Google Scholar 

  • Barbieri L, Brigotti M, Perocco P, Carnicelli D, Ciani M, Mercatali L, Stirpe F (2003) Ribosome-inactivating proteins depurinate poly(ADP-ribosyl)ated poly(ADP-ribose) polymerase and have transforming activity for 3T3 fibroblasts. FEBS Lett 538:178–182

    Article  PubMed  CAS  Google Scholar 

  • Barbieri L, Polito L, Bolognesi A, Ciani M, Pelosi E, Farini V, Jha AK, Sharma N, Vivanco JM, Chambery A, Parente A, Stirpe F (2006) Ribosome-inactivating proteins in edible plants and purification and characterization of a new ribosome-inactivating protein from Cucurbita moschata. Biochim Biophys Acta 1760:783–792

    Article  PubMed  CAS  Google Scholar 

  • Barbieri L, Valbonesi P, Bonora E, Gorini P, Bolognesi A, Stirpe F (1997) Polynucleotide:adenosine glycosidase activity of ribosome-inactivating proteins: effect on DNA, RNA and poly(A). Nucleic Acids Res 25:518–522

    Article  PubMed  CAS  Google Scholar 

  • Barbieri L, Valbonesi P, Govoni M, Pession A, Stirpe F (2000) Polynucleotide:adenosine glycosidase activity of saporin-L1: effect on various forms of mammalian DNA. Biochim Biophys Acta 1480:258–266

    Article  PubMed  CAS  Google Scholar 

  • Bass HW, Webster C, GR OB, Roberts JK, Boston RS (1992) A maize ribosome-inactivating protein is controlled by the transcriptional activator opaque-2. Plant Cell 4:225–234

    PubMed  CAS  Google Scholar 

  • Battelli MG (2004) Cytotoxicity and toxicity to animals and humans of ribosome-inactivating proteins. Mini Rev Med Chem 4:513–521

    Article  PubMed  CAS  Google Scholar 

  • Beaumelle B, Alami M, Hopkins CR (1993) ATP-dependent translocation of ricin across the membrane of purified endosomes. J Biol Chem 268:23661–23669

    PubMed  CAS  Google Scholar 

  • Bergamaschi G, Perfetti V, Tonon L, Novella A, Lucotti C, Danova M, Glennie MJ, Merlini G, Cazzola M (1996) Saporin, a ribosome-inactivating protein used to prepare immunotoxins, induces cell death via apoptosis. Br J Haematol 93:789–794

    Article  PubMed  CAS  Google Scholar 

  • Bhutia SK, Mallick SK, Maiti S, Maiti TK (2009) Inhibitory effect of Abrus abrin-derived peptide fraction against Dalton's lymphoma ascites model. Phytomedicine 16:377–385

    Article  PubMed  CAS  Google Scholar 

  • Bolognesi A, Tazzari PL, Olivieri F, Polito L, Falini B, Stirpe F (1996) Induction of apoptosis by ribosome-inactivating proteins and related immunotoxins. Int J Cancer 68:349–355

    Article  PubMed  CAS  Google Scholar 

  • Brigotti M, Accorsi P, Carnicelli D, Rizzi S, Gonzalez Vara A, Montanaro L, Sperti S (2001) Shiga toxin 1: damage to DNA in vitro. Toxicon 39:341–348

    Article  PubMed  CAS  Google Scholar 

  • Brigotti M, Alfieri R, Sestili P, Bonelli M, Petronini PG, Guidarelli A, Barbieri L, Stirpe F, Sperti S (2002) Damage to nuclear DNA induced by Shiga toxin 1 and ricin in human endothelial cells. FASEB J 16:365–372

    Article  PubMed  CAS  Google Scholar 

  • Brigotti M, Rizzi S, Carnicelli D, Montanaro L, Sperti S (2000) A survey of adenine and 4-aminopyrazolo[3,4-d]pyrimidine (4-APP) as inhibitors of ribosome-inactivating proteins (RIPs). Life Sci 68:331–336

    Article  PubMed  CAS  Google Scholar 

  • Brinkmann U, Mansfield E, Pastan I (1997) Effects of BCL-2 overexpression on the sensitivity of MCF-7 breast cancer cells to ricin, diphtheria and Pseudomonas toxin and immunotoxins. Apoptosis 2:192–198

    Article  PubMed  CAS  Google Scholar 

  • Bussing A, Multani AS, Pathak S, Pfuller U, Schietzel M (1998) Induction of apoptosis by the N-acetyl-galactosamine-specific toxic lectin from Viscum album L. is associated with a decrease of nuclear p53 and Bcl-2 proteins and induction of telomeric associations. Cancer Lett 130:57–68

    Article  PubMed  CAS  Google Scholar 

  • Büssing A, Stein GM, Pfüller U, Schietzel M (1999) Induction of Fas ligand (CD95L) by the toxic mistletoe lectins in human lymphocytes. Anticancer Res 19:1785–1790

    PubMed  Google Scholar 

  • Cameron P, Smith SJ, Giembycz MA, Rotondo D, Plevin R (2003) Verotoxin activates mitogen-activated protein kinase in human peripheral blood monocytes: role in apoptosis and proinflammatory cytokine release. Br J Pharmacol 140:1320–1330

    Article  PubMed  CAS  Google Scholar 

  • Carnicelli D, Brigotti M, Montanaro L, Sperti S (1992) Differential requirement of ATP and extra-ribosomal proteins for ribosome inactivation by eight RNA N-glycosidases. Biochem Biophys Res Commun 182:579–582

    Article  PubMed  CAS  Google Scholar 

  • Chan Tung KW, Mansouri S, Hudak KA (2008) Expression of pokeweed antiviral protein in mammalian cells activates c-Jun NH2-terminal kinase without causing apoptosis. Int J Biochem Cell Biol 40:2452–2461

    Article  PubMed  CAS  Google Scholar 

  • Chang MP, Bramhall J, Graves S, Bonavida B, Wisnieski BJ (1989) Internucleosomal DNA cleavage precedes diphtheria toxin-induced cytolysis. Evidence that cell lysis is not a simple consequence of translation inhibition. J Biol Chem 264:15261–15267

    PubMed  CAS  Google Scholar 

  • Cherney BW, McBride OW, Chen DF, Alkhatib H, Bhatia K, Hensley P, Smulson ME (1987) cDNA sequence, protein structure, and chromosomal location of the human gene for poly(ADP-ribose) polymerase. Proc Natl Acad Sci USA 84:8370–8374

    Article  PubMed  CAS  Google Scholar 

  • Chiarugi A, Moskowitz MA (2002) Cell biology. PARP-1-a perpetrator of apoptotic cell death? Science 297:200–201

    Article  PubMed  CAS  Google Scholar 

  • Ching JC, Jones NL, Ceponis PJ, Karmali MA, Sherman PM (2002) Escherichia coli Shiga-like toxins induce apoptosis and cleavage of poly(ADP-ribose) polymerase via in vitro activation of caspases. Infect Immun 70:4669–4677

    Article  PubMed  CAS  Google Scholar 

  • Chinnaiyan AM (1999) The apoptosome: heart and soul of the cell death machine. Neoplasia 1:5–15

    Article  PubMed  CAS  Google Scholar 

  • Chiu LC, Ooi VE, Sun SS (2001) Induction of apoptosis by a ribosome-inactivating protein from Agrostemma githago is associated with down-regulation of anti-apoptotic bcl-2 protein expression. Int J Oncol 19:137–141

    PubMed  CAS  Google Scholar 

  • Choi SH, Lyu SY, Park WB (2004) Mistletoe lectin induces apoptosis and telomerase inhibition in human A253 cancer cells through dephosphorylation of Akt. Arch Pharm Res 27:68–76

    Article  PubMed  CAS  Google Scholar 

  • Du C, Fang M, Li Y, Li L, Wang X (2000) Smac, a mitochondrial protein that promotes cytochrome c-dependent caspase activation by eliminating IAP inhibition. Cell 102:33–42

    Article  PubMed  CAS  Google Scholar 

  • Endo Y, Mitsui K, Motizuki M, Tsurugi K (1987) The mechanism of action of ricin and related toxic lectins on eukaryotic ribosomes. The site and the characteristics of the modification in 28S ribosomal RNA caused by the toxins. J Biol Chem 262:5908–5912

    PubMed  CAS  Google Scholar 

  • Endo Y, Tsurugi K (1988) The RNA N-glycosidase activity of ricin A-chain. The characteristics of the enzymatic activity of ricin A-chain with ribosomes and with rRNA. J Biol Chem 263:8735–8739

    PubMed  CAS  Google Scholar 

  • Erwert RD, Eiting KT, Tupper JC, Winn RK, Harlan JM, Bannerman DD (2003) Shiga toxin induces decreased expression of the anti-apoptotic protein Mcl-1 concomitant with the onset of endothelial apoptosis. Microb Pathog 35:87–93

    Article  PubMed  CAS  Google Scholar 

  • Fong WP, Mock WY, Ng TB (2000) Intrinsic ribonuclease activities in ribonuclease and ribosome-inactivating proteins from the seeds of bitter gourd. Int J Biochem Cell Biol 32:571–577

    Article  PubMed  CAS  Google Scholar 

  • Fujii J, Matsui T, Heatherly DP, Schlegel KH, Lobo PI, Yutsudo T, Ciraolo GM, Morris RE, Obrig T (2003) Rapid apoptosis induced by Shiga toxin in HeLa cells. Infect Immun 71:2724–2735

    Article  PubMed  CAS  Google Scholar 

  • Fujii J, Wood K, Matsuda F, Carneiro-Filho BA, Schlegel KH, Yutsudo T, Binnington-Boyd B, Lingwood CA, Obata F, Kim KS, Yoshida S, Obrig T (2008) Shiga toxin 2 causes apoptosis in human brain microvascular endothelial cells via C/EBP homologous protein. Infect Immun 76:3679–3689

    Article  PubMed  CAS  Google Scholar 

  • Garrido C, Galluzzi L, Brunet M, Puig PE, Didelot C, Kroemer G (2006) Mechanisms of cytochrome c release from mitochondria. Cell Death Differ 13:1423–1433

    Article  PubMed  CAS  Google Scholar 

  • Geier A, Bar-Shalom I, Beery R, Haimsohn M, Hemi R, Malik Z, Lunenfeld B, Karasik A (1996) Induction of apoptosis in MDA-231 cells by protein synthesis inhibitors is suppressed by multiple agents. Cancer Invest 14:435–444

    Article  PubMed  CAS  Google Scholar 

  • Girbes T, Ferreras JM, Arias FJ, Stirpe F (2004) Description, distribution, activity and phylogenetic relationship of ribosome-inactivating proteins in plants, fungi and bacteria. Mini Rev Med Chem 4:461–476

    Article  PubMed  CAS  Google Scholar 

  • Griffiths GD, Leek MD, Gee DJ (1987) The toxic plant proteins ricin and abrin induce apoptotic changes in mammalian lymphoid tissues and intestine. J Pathol 151:221–229

    Article  PubMed  CAS  Google Scholar 

  • Hajnoczky G, Davies E, Madesh M (2003) Calcium signaling and apoptosis. Biochem Biophys Res Commun 304:445–454

    Article  PubMed  CAS  Google Scholar 

  • Helmy M, Lombard S, Pieroni G (1999) Ricin RCA60: evidence of its phospholipase activity. Biochem Biophys Res Commun 258:252–255

    Article  PubMed  CAS  Google Scholar 

  • Higuchi S, Tamura T, Oda T (2003) Cross-talk between the pathways leading to the induction of apoptosis and the secretion of tumor necrosis factor-alpha in ricin-treated RAW 264.7 cells. J Biochem 134:927–933

    Article  PubMed  CAS  Google Scholar 

  • Hill MM, Adrain C, Duriez PJ, Creagh EM, Martin SJ (2004) Analysis of the composition, assembly kinetics and activity of native Apaf-1 apoptosomes. EMBO J 23:2134–2145

    Article  PubMed  CAS  Google Scholar 

  • Hsu H, Xiong J, Goeddel DV (1995) The TNF receptor 1-associated protein TRADD signals cell death and NF-kappa B activation. Cell 81:495–504

    Article  PubMed  CAS  Google Scholar 

  • Hu R, Zhai Q, Liu W, Liu X (2001) An insight into the mechanism of cytotoxicity of ricin to hepatoma cell: roles of Bcl-2 family proteins, caspases, Ca(2+)-dependent proteases and protein kinase C. J Cell Biochem 81:583–593

    Article  PubMed  CAS  Google Scholar 

  • Hudak KA, Wang P, Tumer NE (2000) A novel mechanism for inhibition of translation by pokeweed antiviral protein: depurination of the capped RNA template. RNA 6:369–380

    Article  PubMed  CAS  Google Scholar 

  • Hughes JN, Lindsay CD, Griffiths GD (1996) Morphology of ricin and abrin exposed endothelial cells is consistent with apoptotic cell death. Hum Exp Toxicol 15:443–451

    Article  PubMed  CAS  Google Scholar 

  • Husain J, Tickle IJ, Wood SP (1994) Crystal structure of momordin, a type I ribosome inactivating protein from the seeds of Momordica charantia. FEBS Lett 342:154–158

    Article  PubMed  CAS  Google Scholar 

  • Igney FH, Krammer PH (2002) Death and anti-death: tumour resistance to apoptosis. Nat Rev Cancer 2:277–288

    Article  PubMed  CAS  Google Scholar 

  • Iordanov MS, Choi RJ, Ryabinina OP, Dinh TH, Bright RK, Magun BE (2002) The UV (Ribotoxic) stress response of human keratinocytes involves the unexpected uncoupling of the Ras-extracellular signal-regulated kinase signaling cascade from the activated epidermal growth factor receptor. Mol Cell Biol 22:5380–5394

    Article  PubMed  CAS  Google Scholar 

  • Iordanov MS, Magun BE (1998) Loss of cellular K+ mimics ribotoxic stress. Inhibition of protein synthesis and activation of the stress kinases SEK1/MKK4, stress-activated protein kinase/c-Jun NH2-terminal kinase 1, and p38/HOG1 by palytoxin. J Biol Chem 273:3528–3534

    Article  PubMed  CAS  Google Scholar 

  • Iordanov MS, Pribnow D, Magun JL, Dinh TH, Pearson JA, Chen SL, Magun BE (1997) Ribotoxic stress response: activation of the stress-activated protein kinase JNK1 by inhibitors of the peptidyl transferase reaction and by sequence-specific RNA damage to the alpha-sarcin/ricin loop in the 28S rRNA. Mol Cell Biol 17:3373–3381

    PubMed  CAS  Google Scholar 

  • Ishizaki T, Megumi C, Komai F, Masuda K, Oosawa K (2002) Accumulation of a 31-kDa glycoprotein in association with the expression of embryogenic potential by spinach callus in culture. Physiol Plant 114:109–115

    Article  PubMed  CAS  Google Scholar 

  • Jones NL, Islur A, Haq R, Mascarenhas M, Karmali MA, Perdue MH, Zanke BW, Sherman PM (2000) Escherichia coli Shiga toxins induce apoptosis in epithelial cells that is regulated by the Bcl-2 family. Am J Physiol Gastrointest Liver Physiol 278:G811–G819

    PubMed  CAS  Google Scholar 

  • Kataoka T, Schroter M, Hahne M, Schneider P, Irmler M, Thome M, Froelich CJ, Tschopp J (1998) FLIP prevents apoptosis induced by death receptors but not by perforin/granzyme B, chemotherapeutic drugs, and gamma irradiation. J Immunol 161:3936–3942

    PubMed  CAS  Google Scholar 

  • Kelliher MA, Grimm S, Ishida Y, Kuo F, Stanger BZ, Leder P (1998) The death domain kinase RIP mediates the TNF-induced NF-kappaB signal. Immunity 8:297–303

    Article  PubMed  CAS  Google Scholar 

  • Kerr JF, Wyllie AH, Currie AR (1972) Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 26:239–257

    Article  PubMed  CAS  Google Scholar 

  • Khan T, Waring P (1993) Macrophage adherence prevents apoptosis induced by ricin. Eur J Cell Biol 62:406–414

    PubMed  CAS  Google Scholar 

  • Khil LY, Kim W, Lyu S, Park WB, Yoon JW, Jun HS (2007) Mechanisms involved in Korean mistletoe lectin-induced apoptosis of cancer cells. World J Gastroenterol 13:2811–2818

    PubMed  CAS  Google Scholar 

  • Khwaja TA, Wajahat T, Ahmad I, Hoessli DC, Walker-Nasir E, Kaleem A, Qazi WM, Shakoori AR, Din NU (2008) In silico modulation of apoptotic Bcl-2 proteins by mistletoe lectin-1: functional consequences of protein modifications. J Cell Biochem 103:479–491

    Article  PubMed  CAS  Google Scholar 

  • Kim MS, So HS, Lee KM, Park JS, Lee JH, Moon SK, Ryu DG, Chung SY, Jung BH, Kim YK, Moon G, Park R (2000) Activation of caspase cascades in Korean mistletoe (Viscum album var. coloratum) lectin-II-induced apoptosis of human myeloleukemic U937 cells. Gen Pharmacol 34:349–355

    Article  PubMed  CAS  Google Scholar 

  • Kim WH, Park WB, Gao B, Jung MH (2004) Critical role of reactive oxygen species and mitochondrial membrane potential in Korean mistletoe lectin-induced apoptosis in human hepatocarcinoma cells. Mol Pharmacol 66:1383–1396

    Article  PubMed  CAS  Google Scholar 

  • Kischkel FC, Hellbardt S, Behrmann I, Germer M, Pawlita M, Krammer PH, Peter ME (1995) Cytotoxicity-dependent APO-1 (Fas/CD95)-associated proteins form a death-inducing signaling complex (DISC) with the receptor. EMBO J 14:5579–5588

    PubMed  CAS  Google Scholar 

  • Kiyokawa N, Mori T, Taguchi T, Saito M, Mimori K, Suzuki T, Sekino T, Sato N, Nakajima H, Katagiri YU, Takeda T, Fujimoto J (2001) Activation of the caspase cascade during Stx1-induced apoptosis in Burkitt's lymphoma cells. J Cell Biochem 81:128–142

    Article  PubMed  CAS  Google Scholar 

  • Kochi SK, Collier RJ (1993) DNA fragmentation and cytolysis in U937 cells treated with diphtheria toxin or other inhibitors of protein synthesis. Exp Cell Res 208:296–302

    Article  PubMed  CAS  Google Scholar 

  • Kojio S, Zhang H, Ohmura M, Gondaira F, Kobayashi N, Yamamoto T (2000) Caspase-3 activation and apoptosis induction coupled with the retrograde transport of Shiga toxin: inhibition by brefeldin A. FEMS Immunol Med Microbiol 29:275–281

    Article  PubMed  CAS  Google Scholar 

  • Komatsu N, Nakagawa M, Oda T, Muramatsu T (2000) Depletion of intracellular NAD(+) and ATP levels during ricin-induced apoptosis through the specific ribosomal inactivation results in the cytolysis of U937 cells. J Biochem 128:463–470

    Article  PubMed  CAS  Google Scholar 

  • Korcheva V, Wong J, Lindauer M, Jacoby DB, Iordanov MS, Magun B (2007) Role of apoptotic signaling pathways in regulation of inflammatory responses to ricin in primary murine macrophages. Mol Immunol 44:2761–2771

    Article  PubMed  CAS  Google Scholar 

  • Lavastre V, Chiasson S, Cavalli H, Girard D (2005) Viscum album agglutinin-I induces apoptosis and degradation of cytoskeletal proteins via caspases in human leukaemia eosinophil AML14.3D10 cells: differences with purified human eosinophils. Br J Haematol 130:527–535

    Article  PubMed  CAS  Google Scholar 

  • Lavastre V, Pelletier M, Saller R, Hostanska K, Girard D (2002) Mechanisms involved in spontaneous and Viscum album agglutinin-I-induced human neutrophil apoptosis: Viscum album agglutinin-I accelerates the loss of antiapoptotic Mcl-1 expression and the degradation of cytoskeletal paxillin and vimentin proteins via caspases. J Immunol 168:1419–1427

    PubMed  CAS  Google Scholar 

  • Lee KH, Rudolph KL, Ju YJ, Greenberg RA, Cannizzaro L, Chin L, Weiler SR, DePinho RA (2001) Telomere dysfunction alters the chemotherapeutic profile of transformed cells. Proc Natl Acad Sci USA 98:3381–3386

    Article  PubMed  CAS  Google Scholar 

  • Lee SY, Cherla RP, Tesh VL (2007) Simultaneous induction of apoptotic and survival signaling pathways in macrophage-like THP-1 cells by Shiga toxin 1. Infect Immun 75:1291–1302

    Article  PubMed  CAS  Google Scholar 

  • Lee SY, Lee MS, Cherla RP, Tesh VL (2008) Shiga toxin 1 induces apoptosis through the endoplasmic reticulum stress response in human monocytic cells. Cell Microbiol 10:770–780

    Article  PubMed  CAS  Google Scholar 

  • Lehar SM, Pedersen JT, Kamath RS, Swimmer C, Goldmacher VS, Lambert JM, Blattler WA, Guild BC (1994) Mutational and structural analysis of the lectin activity in binding domain 2 of ricin B chain. Protein Eng 7:1261–1266

    Article  PubMed  CAS  Google Scholar 

  • Li F, Mei Y, Wang Y, Chen C, Tu J, Xiao B, Xu L (2005) Trichosanthin inhibits antigen-specific T cell expansion through nitric oxide-mediated apoptosis pathway. Cell Immunol 234:23–30

    Article  PubMed  CAS  Google Scholar 

  • Li J, Xia X, Nie H, Smith MA, Zhu X (2007a) PKC inhibition is involved in trichosanthin-induced apoptosis in human chronic myeloid leukemia cell line K562. Biochim Biophys Acta 1770:63–70

    Article  PubMed  CAS  Google Scholar 

  • Li J, Xia X, Ke Y, Nie H, Smith MA, Zhu X (2007b) Trichosanthin induced apoptosis in HL-60 cells via mitochondrial and endoplasmic reticulum stress signaling pathways. Biochim Biophys Acta 1770:1169–1180

    Article  PubMed  CAS  Google Scholar 

  • Li MX, Yeung HW, Pan LP, Chan SI (1991) Trichosanthin, a potent HIV-1 inhibitor, can cleave supercoiled DNA in vitro. Nucleic Acids Res 19:6309–6312

    Article  PubMed  CAS  Google Scholar 

  • Li XD, Chen WF, Liu WY, Wang GH (1997) Large-scale preparation of two new ribosome-inactivating proteins – Cinnamomum and Camphorin from the seeds of Cinnamomum camphora. Protein Expr Purif 10:27–31

    Article  PubMed  CAS  Google Scholar 

  • Lindahl T, Satoh MS, Poirier GG, Klungland A (1995) Post-translational modification of poly(ADP-ribose) polymerase induced by DNA strand breaks. Trends Biochem Sci 20:405–411

    Article  PubMed  CAS  Google Scholar 

  • Liu JP (1999) Studies of the molecular mechanisms in the regulation of telomerase activity. FASEB J 13:2091–2104

    PubMed  CAS  Google Scholar 

  • Liu RS, Yang JH, Liu WY (2002) Isolation and enzymatic characterization of lamjapin, the first ribosome-inactivating protein from cryptogamic algal plant (Laminaria japonica A). Eur J Biochem 269:4746–4752

    Article  PubMed  CAS  Google Scholar 

  • Lyu SY, Choi SH, Park WB (2002) Korean mistletoe lectin-induced apoptosis in hepatocarcinoma cells is associated with inhibition of telomerase via mitochondrial controlled pathway independent of p53. Arch Pharm Res 25:93–101

    Article  PubMed  CAS  Google Scholar 

  • Marchant A, Hartley MR (1995) The action of pokeweed antiviral protein and ricin A-chain on mutants in the alpha-sarcin loop of Escherichia coli 23S ribosomal RNA. J Mol Biol 254:848–855

    Article  PubMed  CAS  Google Scholar 

  • Mlsna D, Monzingo AF, Katzin BJ, Ernst S, Robertus JD (1993) Structure of recombinant ricin A chain at 2.3 A. Protein Sci 2:429–435

    Article  PubMed  CAS  Google Scholar 

  • Mock JW, Ng TB, Wong RN, Yao QZ, Yeung HW, Fong WP (1996) Demonstration of ribonuclease activity in the plant ribosome-inactivating proteins alpha- and beta-momorcharins. Life Sci 59:1853–1859

    Article  PubMed  CAS  Google Scholar 

  • Monzingo AF, Robertus JD (1992) X-ray analysis of substrate analogs in the ricin A-chain active site. J Mol Biol 227:1136–1145

    Article  PubMed  CAS  Google Scholar 

  • Morimoto H, Bonavida B (1992) Diphtheria toxin- and Pseudomonas A toxin-mediated apoptosis. ADP ribosylation of elongation factor-2 is required for DNA fragmentation and cell lysis and synergy with tumor necrosis factor-alpha. J Immunol 149:2089–2094

    PubMed  CAS  Google Scholar 

  • Narayanan S, Surolia A, Karande AA (2004) Ribosome-inactivating protein and apoptosis: abrin causes cell death via mitochondrial pathway in Jurkat cells. Biochem J 377:233–240

    Article  PubMed  CAS  Google Scholar 

  • Ng TB, Parkash A (2002) Hispin, a novel ribosome inactivating protein with antifungal activity from hairy melon seeds. Protein Expr Purif 26:211–217

    Article  PubMed  CAS  Google Scholar 

  • Ng TB, Parkash A, Tso WW (2002) Purification and characterization of moschins, arginine-glutamate-rich proteins with translation-inhibiting activity from brown pumpkin (Cucurbita moschata) seeds. Protein Expr Purif 26:9–13

    Article  PubMed  CAS  Google Scholar 

  • Ng TB, Parkash A, Tso WW (2003) Purification and characterization of alpha- and beta-benincasins, arginine/glutamate-rich peptides with translation-inhibiting activity from wax gourd seeds. Peptides 24:11–16

    Article  PubMed  CAS  Google Scholar 

  • Nicolas E, Beggs JM, Haltiwanger BM, Taraschi TF (1997) Direct evidence for the deoxyribonuclease activity of the plant ribosome inactivating protein gelonin. FEBS Lett 406:162–164

    Article  PubMed  CAS  Google Scholar 

  • Nicolas E, Beggs JM, Haltiwanger BM, Taraschi TF (1998) A new class of DNA glycosylase/apurinic/apyrimidinic lyases that act on specific adenines in single-stranded DNA. J Biol Chem 273:17216–17220

    Article  PubMed  CAS  Google Scholar 

  • Nicolas E, Beggs JM, Taraschi TF (2000) Gelonin is an unusual DNA glycosylase that removes adenine from single-stranded DNA, normal base pairs and mismatches. J Biol Chem 275:31399–31406

    Article  PubMed  CAS  Google Scholar 

  • Oda T, Komatsu N, Muramatsu T (1997) Inhibitory effect of dideoxyforskolin on cell death induced by ricin, modeccin, diphtheria toxin, and Pseudomonas toxin in MDCK cells. Cell Struct Funct 22:545–554

    Article  PubMed  CAS  Google Scholar 

  • Olsnes S, Pihl A (1973) Isolation and properties of abrin: a toxic protein inhibiting protein synthesis. Evidence for different biological functions of its two constituent-peptide chains. Eur J Biochem 35:179–185

    Article  PubMed  CAS  Google Scholar 

  • Olsnes S, Pihl A (1981) Chimeric toxins. Pharmacol Ther 15:355–381

    Article  PubMed  CAS  Google Scholar 

  • Olsnes S, Sandvig K (1988) How protein toxins enter and kill cells. Cancer Treat Res 37:39–73

    Article  PubMed  CAS  Google Scholar 

  • Pae HO, Oh GS, Kim NY, Shin MK, Lee HS, Yun YG, Oh H, Kim YM, Chung HT (2001) Roles of extracellular signal-regulated kinase and p38 mitogen-activated protein kinase in apoptosis of human monoblastic leukemia U937 cells by lectin-II isolated from Korean mistletoe. In Vitro Mol Toxicol 14:99–106

    Article  CAS  Google Scholar 

  • Pae HO, Seo WG, Shin M, Lee HS, Kim SB, Chung HT (2000) Protein kinase A or C modulates the apoptosis induced by lectin II isolated from Korean mistletoe, Viscum album var. Coloratum, in the human leukemic HL-60 cells. Immunopharmacol Immunotoxicol 22:279–295

    Article  PubMed  CAS  Google Scholar 

  • Park R, Kim MS, So HS, Jung BH, Moon SR, Chung SY, Ko CB, Kim BR, Chung HT (2000) Activation of c-Jun N-terminal kinase 1 (JNK1) in mistletoe lectin II-induced apoptosis of human myeloleukemic U937 cells. Biochem Pharmacol 60:1685–1691

    Article  PubMed  CAS  Google Scholar 

  • Parkash A, Ng TB, Tso WW (2002a) Isolation and characterization of luffacylin, a ribosome inactivating peptide with anti-fungal activity from sponge gourd (Luffa cylindrica) seeds. Peptides 23:1019–1024

    Article  PubMed  CAS  Google Scholar 

  • Parkash A, Ng TB, Tso WW (2002b) Purification and characterization of charantin, a napin-like ribosome-inactivating peptide from bitter gourd (Momordica charantia) seeds. J Pept Res 59:197–202

    Article  PubMed  CAS  Google Scholar 

  • Polito L, Bortolotti M, Farini V, Battelli MG, Barbieri L, Bolognesi A (2009) Saporin induces multiple death pathways in lymphoma cells with different intensity and timing as compared to ricin. Int J Biochem Cell Biol 41:1055–1061

    Article  PubMed  CAS  Google Scholar 

  • Prestle J, Schonfelder M, Adam G, Mundry KW (1992) Type 1 ribosome-inactivating proteins depurinate plant 25S rRNA without species specificity. Nucleic Acids Res 20:3179–3182

    Article  PubMed  CAS  Google Scholar 

  • Qu X, Qing L (2004) Abrin induces HeLa cell apoptosis by cytochrome c release and caspase activation. J Biochem Mol Biol 37:445–453

    Article  PubMed  CAS  Google Scholar 

  • Rao PV, Jayaraj R, Bhaskar AS, Kumar O, Bhattacharya R, Saxena P, Dash PK, Vijayaraghavan R (2005) Mechanism of ricin-induced apoptosis in human cervical cancer cells. Biochem Pharmacol 69:855–865

    Article  PubMed  CAS  Google Scholar 

  • Rappuoli R (1997) Guidebook to protein toxins and their use in cell biology. Oxford University Press, New York, pp 57–58

    Google Scholar 

  • Reinbothe S, Reinbothe C, Lehmann J, Becker W, Apel K, Parthier B (1994) JIP60, a methyl jasmonate-induced ribosome-inactivating protein involved in plant stress reactions. Proc Natl Acad Sci USA 91:7012–7016

    Article  PubMed  CAS  Google Scholar 

  • Robertus JD (1996) The structure of ribosome inactivating proteins from plants. In: Parker MW (ed) Protein toxin structure. Landes, Austin, pp 253–270

    Google Scholar 

  • Roncuzzi L, Gasperi-Campani A (1996) DNA-nuclease activity of the single-chain ribosome-inactivating proteins dianthin 30, saporin 6 and gelonin. FEBS Lett 392:16–20

    Article  PubMed  CAS  Google Scholar 

  • Roudkenar MH, Bouzari S, Kuwahara Y, Roushandeh AM, Baba T, Oloomi M, Fukumoto M (2008) Induction of apoptosis on K562 cell line and double strand breaks on colon cancer cell line expressing high affinity receptor for granulocyte macrophage-colony stimulating factor (GM-CSF). Iran Biomed J 12:1–6

    PubMed  CAS  Google Scholar 

  • Saelens X, Festjens N, Vande Walle L, van Gurp M, van Loo G, Vandenabeele P (2004) Toxic proteins released from mitochondria in cell death. Oncogene 23:2861–2874

    Article  PubMed  CAS  Google Scholar 

  • Sakahira H, Enari M, Nagata S (1998) Cleavage of CAD inhibitor in CAD activation and DNA degradation during apoptosis. Nature 391:96–99

    Article  PubMed  CAS  Google Scholar 

  • Sandvig K, Olsnes S, Pihl A (1976) Kinetics of binding of the toxic lectins abrin and ricin to surface receptors of human cells. J Biol Chem 251:3977–3984

    PubMed  CAS  Google Scholar 

  • Sandvig K, van Deurs B (1996) Endocytosis, intracellular transport, and cytotoxic action of Shiga toxin and ricin. Physiol Rev 76:949–966

    PubMed  CAS  Google Scholar 

  • Satyamoorthy K, Soballe PW, Soans F, Herlyn M (1997) Adenovirus infection enhances killing of melanoma cells by a mitotoxin. Cancer Res 57:1873–1876

    PubMed  CAS  Google Scholar 

  • Scaffidi C, Schmitz I, Krammer PH, Peter ME (1999) The role of c-FLIP in modulation of CD95-induced apoptosis. J Biol Chem 274:1541–1548

    Article  PubMed  CAS  Google Scholar 

  • Schimmer AD (2004) Inhibitor of apoptosis proteins: translating basic knowledge into clinical practice. Cancer Res 64:7183–7190

    Article  PubMed  CAS  Google Scholar 

  • Sharma N, Park SW, Vepachedu R, Barbieri L, Ciani M, Stirpe F, Savary BJ, Vivanco JM (2004) Isolation and characterization of an RIP (ribosome-inactivating protein)-like protein from tobacco with dual enzymatic activity. Plant Physiol 134:171–181

    Article  PubMed  CAS  Google Scholar 

  • Shih SF, Wu YH, Hung CH, Yang HY, Lin JY (2001) Abrin triggers cell death by inactivating a thiol-specific antioxidant protein. J Biol Chem 276:21870–21877

    Article  PubMed  CAS  Google Scholar 

  • Sikriwal D, Ghosh P, Batra JK (2008) Ribosome inactivating protein saporin induces apoptosis through mitochondrial cascade, independent of translation inhibition. Int J Biochem Cell Biol 40:2880–2888

    Article  PubMed  CAS  Google Scholar 

  • Sims JL, Berger SJ, Berger NA (1983) Poly(ADP-ribose) polymerase inhibitors preserve nicotinamide adenine dinucleotide and adenosine 5′-triphosphate pools in DNA-damaged cells: mechanism of stimulation of unscheduled DNA synthesis. Biochemistry 22:5188–5194

    Article  PubMed  CAS  Google Scholar 

  • Slee EA, Adrain C, Martin SJ (2001) Executioner caspase-3, -6, and -7 perform distinct, non-redundant roles during the demolition phase of apoptosis. J Biol Chem 276:7320–7326

    Article  PubMed  CAS  Google Scholar 

  • Smith WE, Kane AV, Campbell ST, Acheson DW, Cochran BH, Thorpe CM (2003) Shiga toxin 1 triggers a ribotoxic stress response leading to p38 and JNK activation and induction of apoptosis in intestinal epithelial cells. Infect Immun 71:1497–1504

    Article  PubMed  CAS  Google Scholar 

  • Steeves RM, Denton ME, Barnard FC, Henry A, Lambert JM (1999) Identification of three oligosaccharide binding sites in ricin. Biochemistry 38:11677–11685

    Article  PubMed  CAS  Google Scholar 

  • Stirpe F (2004) Ribosome-inactivating proteins. Toxicon 44:371–383

    Article  PubMed  CAS  Google Scholar 

  • Stirpe F, Bailey S, Miller SP, Bodley JW (1988) Modification of ribosomal RNA by ribosome-inactivating proteins from plants. Nucleic Acids Res 16:1349–1357

    Article  PubMed  CAS  Google Scholar 

  • Stirpe F, Battelli MG (2006) Ribosome-inactivating proteins: progress and problems. Cell Mol Life Sci 63:1850–1866

    Article  PubMed  CAS  Google Scholar 

  • Stirpe F, Gasperi-Campani A, Barbieri L, Lorenzoni E, Montanaro L, Sperti S, Bonetti E (1977) Inhibition of protein synthesis by modeccin, the toxin of Modecca digitata. FEBS Lett 85:65–67

    Article  PubMed  CAS  Google Scholar 

  • Swimmer C, Lehar SM, McCafferty J, Chiswell DJ, Blattler WA, Guild BC (1992) Phage display of ricin B chain and its single binding domains: system for screening galactose-binding mutants. Proc Natl Acad Sci USA 89:3756–3760

    Article  PubMed  CAS  Google Scholar 

  • Tamura T, Tsuruta N, Hirano K, Yamaguchi K, Oda T (2003) Butyric acid sensitizes Vero cells to ricin-induced apoptosis via accelerated activation of multiple signal transduction pathways. Cell Struct Funct 28:475–485

    Article  PubMed  CAS  Google Scholar 

  • Tournier C, Hess P, Yang DD, Xu J, Turner TK, Nimnual A, Bar-Sagi D, Jones SN, Flavell RA, Davis RJ (2000) Requirement of JNK for stress-induced activation of the cytochrome c-mediated death pathway. Science 288:870–874

    Article  PubMed  CAS  Google Scholar 

  • Uptain SM, Kane CM, Chamberlin MJ (1997) Basic mechanisms of transcript elongation and its regulation. Annu Rev Biochem 66:117–172

    Article  PubMed  CAS  Google Scholar 

  • van Deurs B, Tonnessen TI, Petersen OW, Sandvig K, Olsnes S (1986) Routing of internalized ricin and ricin conjugates to the Golgi complex. J Cell Biol 102:37–47

    Article  PubMed  Google Scholar 

  • van Loo G, van Gurp M, Depuydt B, Srinivasula SM, Rodriguez I, Alnemri ES, Gevaert K, Vandekerckhove J, Declercq W, Vandenabeele P (2002a) The serine protease Omi/HtrA2 is released from mitochondria during apoptosis. Omi interacts with caspase-inhibitor XIAP and induces enhanced caspase activity. Cell Death Differ 9:20–26

    Article  PubMed  Google Scholar 

  • van Loo G, Saelens X, van Gurp M, MacFarlane M, Martin SJ, Vandenabeele P (2002b) The role of mitochondrial factors in apoptosis: a Russian roulette with more than one bullet. Cell Death Differ 9:1031–1042

    Article  PubMed  CAS  Google Scholar 

  • Verma S, Zhao LJ, Chinnadurai G (2001) Phosphorylation of the pro-apoptotic protein BIK: mapping of phosphorylation sites and effect on apoptosis. J Biol Chem 276:4671–4676

    Article  PubMed  CAS  Google Scholar 

  • Vervecken W, Kleff S, Pfuller U, Bussing A (2000) Induction of apoptosis by mistletoe lectin I and its subunits. No evidence for cytotoxic effects caused by isolated A- and B-chains. Int J Biochem Cell Biol 32:317–326

    Article  PubMed  CAS  Google Scholar 

  • Wajant H (2002) The Fas signaling pathway: more than a paradigm. Science 296:1635–1636

    Article  PubMed  CAS  Google Scholar 

  • Walsh TA, Morgan AE, Hey TD (1991) Characterization and molecular cloning of a proenzyme form of a ribosome-inactivating protein from maize. Novel mechanism of proenzyme activation by proteolytic removal of a 2.8-kiloDalton internal peptide segment. J Biol Chem 266:23422–23427

    PubMed  CAS  Google Scholar 

  • Wang P, Tumer NE (1999) Pokeweed antiviral protein cleaves double-stranded supercoiled DNA using the same active site required to depurinate rRNA. Nucleic Acids Res 27:1900–1905

    Article  PubMed  CAS  Google Scholar 

  • Wang P, Yan H, Li JC (2007) CREB-mediated Bcl-2 expression in trichosanthin-induced Hela cell apoptosis. Biochem Biophys Res Commun 363:101–105

    Article  PubMed  CAS  Google Scholar 

  • Wang YY, Ouyang DY, Huang H, Chan H, Tam SC, Zheng YT (2005) Enhanced apoptotic action of trichosanthin in HIV-1 infected cells. Biochem Biophys Res Commun 331:1075–1080

    Article  PubMed  CAS  Google Scholar 

  • Weng A, Melzig MF, Bachran C, Fuchs H (2008) Enhancement of saporin toxicity against U937 cells by Gypsophila saponins. J Immunotoxicol 5:287–292

    Article  PubMed  CAS  Google Scholar 

  • Wilson C, Foster GH, Bitzan M (2005) Silencing of Bak ameliorates apoptosis of human proximal tubular epithelial cells by Escherichia coli-derived Shiga toxin 2. Infection 33:362–367

    Article  PubMed  CAS  Google Scholar 

  • Xiong SD, Yu K, Liu XH, Yin LH, Kirschenbaum A, Yao S, Narla G, DiFeo A, Wu JB, Yuan Y, Ho SM, Lam YW, Levine AC (2009) Ribosome-inactivating proteins isolated from dietary bitter melon induce apoptosis and inhibit histone deacetylase-1 selectively in premalignant and malignant prostate cancer cells. Int J Cancer 125:774–782

    Article  PubMed  CAS  Google Scholar 

  • Xu L, Wang Y, Wang L, Gao Y, An C (2008) TYchi, a novel chitinase with RNA N-glycosidase and anti-tumor activities. Front Biosci 13:3127–3135

    Article  PubMed  CAS  Google Scholar 

  • Yu SW, Wang H, Poitras MF, Coombs C, Bowers WJ, Federoff HJ, Poirier GG, Dawson TM, Dawson VL (2002) Mediation of poly(ADP-ribose) polymerase-1-dependent cell death by apoptosis-inducing factor. Science 297:259–263

    Article  PubMed  CAS  Google Scholar 

  • Zhang C, Gong Y, Ma H, An C, Chen D, Chen ZL (2001) Reactive oxygen species involved in trichosanthin-induced apoptosis of human choriocarcinoma cells. Biochem J 355:653–661

    PubMed  CAS  Google Scholar 

  • Zhang CY, Gong YX, Ma H, An CC, Chen DY (2000) Trichosanthin induced calcium-dependent generation of reactive oxygen species in human choriocarcinoma cells. Analyst 125:1539–1542

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Immunochemistry Laboratory, National Institute of Immunology, Aruna Asaf Ali Marg, New Delhi, 110067, India

    Deepa Sikriwal & Janendra K. Batra

Authors
  1. Deepa Sikriwal
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Janendra K. Batra
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Janendra K. Batra .

Editor information

Editors and Affiliations

  1. Dept. Biological Sciences, University of Warwick, Coventry, CV47AL, United Kingdom

    J. Michael Lord

  2. Dept. Biological Sciences, University of Warwick, Coventry, CV47AL, United Kingdom

    Martin R. Hartley

Rights and permissions

Reprints and permissions

Copyright information

© 2010 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Sikriwal, D., Batra, J.K. (2010). Ribosome Inactivating Proteins and Apoptosis. In: Lord, J., Hartley, M. (eds) Toxic Plant Proteins. Plant Cell Monographs, vol 18. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-12176-0_9

Download citation

Publish with us

Policies and ethics

Search

Navigation