Anisomycin is a multifunctional drug: More than just a tool to inhibit protein synthesis

Current Chemical Biology

Volumn 4, Issue 2, 2010, Pages 124-132

  Macías Silva, Marina ^a   Vázquez Victorio, Genaro ^a   Hernández Damián, Jacqueline ^a  

^a UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

Author keywords

Anisomycin; Apoptosis; Cancer; MAPKs; Protein synthesis inhibition; Ribotoxic stress; Signaling

Indexed keywords

ANISOMYCIN; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; PEPTIDYLTRANSFERASE; STRESS ACTIVATED PROTEIN KINASE;

AMNESIA; ENZYME ACTIVITY; GENE EXPRESSION; HUMAN; IMMUNE SYSTEM; MAMMAL CELL; MEMORY CONSOLIDATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN SYNTHESIS; REVIEW; RIBOSOME; SIGNAL TRANSDUCTION; T LYMPHOCYTE;

ANIMALIA; BACTERIA (MICROORGANISMS); EUKARYOTA; MAMMALIA; MUS; STREPTOMYCES GRISEOLUS;

EID: 77951527511     PISSN: 18723136     EISSN: None     Source Type: Journal    
DOI: 10.2174/187231310791170793     Document Type: Review

References (83)

1. Sobin BA, Tanner FW. Anisomycin, a new anti-protozoan antibiotic. J Am Chem Soc 1954; 76: 4053.
2. Grollman AP. Inhibitors of protein biosynthesis. II. Mode of action of anisomycin. J Biol Chem 1967; 242: 3226-3233
3. Greenberg ME, Hermanowski AL, Ziff EB. Effect of protein synthesis inhibitors on growth factor activation of c-fos, c-myc, and actin gene transcription. Mol Cell Biol 1986; 6: 1050-1057
4. Cano E, Mahadevan LC. Parallel signal processing among mammalian MAPKs. TIBS 1995; 20: 117-122
5. Laskin JD, Heck DE, Laskin DL. The ribotoxic stress response as a potential mechanism for map kinase activation in xenobiotic toxicity. Toxicol Sci 2002; 69: 289-291
6. Radulovic J, Tronson NC. Protein synthesis inhibitors, gene super-induction and memory: too little or too much protein? Neurobiol Learn Mem 2008; 89: 212-218
7. Barbacid M, Vazquez D. [3H]anisomycin binding to eukaryotic ribosomes. J Mol Biol 1973; 84: 603-23.
8. Ioannou M, Coutsogeorgopoulos C, Synetos D. Kinetics of inhibition of rabbit reticulocyte peptidyltransferase by anisomycin and sparsomycin. Mol Pharm 1998; 53: 1089-1096
9. Shifrin VI, Anderson P. Trichothecene mycotoxins trigger a ribotoxic stress response that activates c-Jun N-terminal kinase and p38 mitogen-activated protein kinase and induces apoptosis. J Biol Chem 1999; 274: 13985-13992 (Pubitemid 129518701)
10. Kirillov S, Porsea BT, Vestera B, Woolleyc P, Garrett RA. Movement of the 3'-end of tRNA through the peptidyl transferase centre and its inhibition by antibiotics. FEBS Lett 1997; 406: 223-233 (Pubitemid 27166301)
11. Hansen JL, Moore PB, Steitz TA. Structures of five antibiotics bound at the peptidyl transferase center of the large ribosomal subunit. J Mol Biol 2003; 330: 1061-1075
12. Jimenez A, Vazquez D. Quantitative binding of antibiotics to ribosomes from yeast mutant altered on the peptidyl-transferase center. Eur J Biochem 1975; 54: 483-492
13. Shaw AR, Ziff EB. Selective inhibition of adenovirus type 2 early region II and III transcription by anisomycin block of protein synthesis. Mol Cell Biol 1982; 2: 789-799
14. Eggerding FA. Alterations in early adenovirus transcription and mRNA abundante induced by translational inhibitors. J Biol Chem 1985; 260: 8354-8359
15. Barton DJ, Morasco BJ, Flanegan JB. Translating ribosomes inhibit poliovirus negative-strand RNA synthesis. J Virol 1999; 73: 10104-10112
16. Uptain SM, Kane CM, Chamberlin MJ. Basic mechanisms of transcript elongation and its regulation. Annu Rev Biochem 1997; 66: 117-172
17. Iordanov MS, Pribnow D, Magun JL, et al. 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 1997; 17: 3373-3381 (Pubitemid 27215052)
18. Iordanov MS, Pribnow D, Magun JL, Dinh TH, Pearson JA, Magun BE. Ultraviolet radiation triggers the ribotoxic stress response in mammalian cells. J Biol Chem 1998; 273: 15794-15803 (Pubitemid 28298201)
19. Iordanov MS, Magun BE. Different mechanisms of c-Jun NH(2)- terminal kinase-1 (JNK1) activation by ultraviolet-B radiation and oxidative stressors. J Biol Chem 1999; 274: 25801-25806
20. Ouyang D-Y, Wang Y-Y, Zheng Y-T. Activation of c-jun N-terminal kinases by ribotoxic stresses. Cell Mol Immunol 2005; 2: 419-425.
21. Dent P, Yacoub A, Contessa J, et al. Stress and radiation-induced activation of multiple intracellular signaling pathways. Radiation Res 2003; 159: 283-300. (Pubitemid 36314943)
22. Swantek JL, Cobb MH, Geppert TD. Jun N-terminal kinase/stress-activated protein kinase (JNK/SAPK) is required for lipopolysaccharide stimulation of tumor necrosis factor alpha (TNF-α) translation: Glucocorticoids inhibit TNF-α translation by blocking JNK/SAPK. Mol Cel Biol 1997; 17: 6274-6282
23. Stein B, Brady H, Yang MX, Young DB, Barbosa MS. Cloning and characterization of MEK6, a novel member of the mitogen-activated protein kinase kinase cascade. J Biol Chem 1996; 271: 11427-11433 (Pubitemid 26155983)
24. Coso OA, Chiariello M, Yu J-C, et al. The small GTP-binding protein Rac1 and Cdc42 regulate the activity of the JNK/SAPK signaling pathway. Cell 1995; 81: 1137-1146
25. Bodmer D, Brors D, Pak K, Gloddek B, Ryan AF. Rescue of auditory hair cells from aminoglycoside toxicity by Clostridium difficile toxin B, an inhibitor of the small GTPases Rho/Rac/Cdc42. Hearing Res 2002; 172: 81-86.
26. Ward DT, Maldonado-Pérez D, Hollins L, Riccardi D. Aminoglycosides induce acute cell signaling and chronic cell death in renal cells that express the calcium-sensing receptor. J Am Soc Nephrol 2005; 16: 1236-1244 (Pubitemid 41716508)
27. Inoue T, Hammaker D, Boyle DL, Firestein GS. Regulation of JNK by MKK-7 in fibroblast-like synoviocytes. Arthritis Rheum 2006; 54: 2127-2135 (Pubitemid 44051068)
28. Cano E, Hazzalin CA, Mahadevan LC. Anisomycin-activated protein kinases p45 and p55 but not mitogen-activated protein kinases ERK-1 and -2 are implicated in the induction of c-fos and c-jun. Mol Cell Biol 1994; 14: 7352-7362 (Pubitemid 24326400)
29. Shafer LM, Slice LW. Anisomycin induces COX-2 mRNA expression through p38(MAPK) and CREB independent of small GTPases in intestinal epithelial cells. Biochim Biophys Acta 2005; 1745: 393-400.
30. Yujiri T, Sather S, Fanger GR, Johnson GL. Role of MEKK1 in cell survival and activation of JNK and ERK pathways defined by targeted gene disruption. Science 1998; 282:1911-1914 (Pubitemid 28555274)
31. Hazzalin CA, Le Panse R, Cano E, Mahadevan LC. Anisomycin selectively desensitizes signalling components involved in stress kinase activation and fos and jun induction. Mol Cell Biol 1998; 18: 1844-1854 (Pubitemid 28152633)
32. Barros LF, Young M, Saklatvala J, Baldwin SA. Evidence of two mechanisms for the activation of the glucose transporter GLUT1 by anisomycin: p38(MAP kinase) activation and protein synthesis inhibition in mammalian cells. J Physiol 1997; 504: 517-525
33. Edwards DR, Mahadevan LC. Protein synthesis inhibitors differentially superinduce c-fos and c-jun by three distinct mechanisms: lack of evidence for labile repressors. EMBO J 1992; 1: 2415-2424
34. Bébien M, Salinas S, Becamel C, Richard V, Linares L, Hipskind RA. Immediate-early gene induction by the stresses anisomycin and arsenite in human osteosarcoma cells involves MAPK cascade signaling to Elk-1, CREB and SRF. Oncogene. 2003; 22: 1836-1847
35. Ogawa T, Hayashi T, Kyoizumi S, et al. Anisomycin downregulates gap-junctional intercellular communication via the p38 MAP-kinase pathway. J Cell Sci 2004; 117: 2087-2096 (Pubitemid 38745141)
36. Theodosiou A, Ashworth A. Differential effects of stress stimuli on a JNK-inactivating phosphatase. Oncogene 2002; 21: 2387-2397 (Pubitemid 34407297)
37. Joiakim A, Mathieu PA, Elliott AA, Reiners JJ Jr. Superinduction of CYP1A1 in MCF10A cultures by cycloheximide, anisomycin, and puromycin: a process independent of effects on protein translation and unrelated to suppression of aryl hydrocarbon receptor proteolysis by the proteasome. Mol Pharmacol 2004; 66: 936-947 (Pubitemid 39319466)
38. Vázquez-Macías A, Ruíz-Mendoza AB, Fonseca-Sánchez MA, Briones-Orta MA, Macías-Silva M. Downregulation of Ski and SnoN co-repressors by anisomycin. FEBS Lett 2005; 579: 3701-3706 (Pubitemid 40897712)
39. Hernández-Damián J, Tecalco-Cruz AC, Vázquez- Macías A, Sosa-Garrocho M, Caligaris C, Macías-Silva M. Anisomycin requires TGF-β type I receptor ALK5 to induce the downregulation of SnoN and Ski corepressors. 2010; manuscript in preparation.
40. Törocsik B, Szeberényi J. Anisomycin uses multiple mechanisms to stimulate mitogen-activated protein kinases and gene expression and to inhibit neuronal differentiation in PC12 phaeochromocytoma cells. Eur J Neurosci 2000; 12: 527-532 (Pubitemid 30142753)
41. Polverino AJ, Patterson SD. Selective activation of caspase during apoptotic induction in HL-60 cells. Effects of a tetrapeptide inhibitor. J Biol Chem. 1997; 272: 7013-7021
42. Watanabe N, Iwamoto T, Dickinson DA, Iles KE, Forman HJ. Activation of the mitochondrial caspase cascade in the absence of protein synthesis does not require c-Jun N-terminal kinase. Arch Biochem Biophys 2002; 405: 231-240 (Pubitemid 35191737)
43. Hoppe J, Kilic M, Hoppe V, Sachinidis A, Kagerhuber U. Formation of caspase-3 complexes and fragmentation of caspase-12 during anisomycin-induced apoptosis in AKR-2B cells without aggregation of Apaf-1. Eur J Cell Biol 2002; 81: 567-576 (Pubitemid 35256385)
44. Curtin JF, Cotter TG. Anisomycin activates JNK and sensitises DU 145 prostate carcinoma cells to Fas mediated apoptosis. Br J Cancer 2002; 87: 1188-1194
45. Santibañez JF, Hurtado C. Ha-Ras sensitizes transformed mouse skin cells to anisomycin-induced apoptosis. FEBS Lett 2005; 579: 6459-6464 (Pubitemid 41612168)
46. Lee KH, Nishimura S, Matsunaga S, Fusetani N, Horinouchi S, Yoshida M. Inhibition of protein synthesis and activation of stress-activated protein kinases by onnamide A and theopederin B, antitumor marine natural products. Cancer Sci 2005; 96: 357-364 (Pubitemid 41007471)
47. Abayasiriwardana KS, Barbone D, Kim KU, et al. Malignant mesothelioma cells are rapidly sensitized to TRAIL-induced apoptosis by low-dose anisomycin via Bim. Mol Cancer Ther 2007; 6: 2766-2776 (Pubitemid 350058156)
48. Xia S, Li Y, Rosen EM, Laterra J. Ribotoxic stress sensitizes glioblastoma cells to death receptor-induced apoptosis: Requirements for c-Jun NH2-terminal kinase and Bim. Mol Cancer Res 2007; 5: 783-792 (Pubitemid 47294806)
49. Hori T, Kondo T, Tabuchi Y, et al. Molecular mechanism of apoptosis and gene expressions in human lymphoma U937 cells treated with anisomycin. Chem Biol Interact 2008; 172: 125-140
50. Croons V, Martinet W, Herman AG, Timmermans J-P, De Meyer GRY. Protein synthesis inhibitor anisomycin induces macrophage apoptosis in rabbit atherosclerotic plaques through p38 mitogen-activated protein kinase. J Pharmacol Exp Therap 2009; 329: 856-864
51. Daubriac J, Fleury-Feith J, Kheuang L, et al. Malignant pleural mesothelioma cells resist anoikis as quiescent pluricellular aggregates. Cell Death Differ 2009; 16: 1146-1155
52. Mawji IA, Simpson CD, Gronda M, et al. A chemical screen identifies anisomycin as an anoikis sensitizer that functions by decreasing FLIP protein synthesis. Cancer Res 2007; 67: 8307-8315 (Pubitemid 47395169)
53. Rüller S, Stahl C, Köhler G, et al. Sensitization of tumor cells to ribotoxic stress-induced apoptotic cell death: A new therapeutic strategy. Clin Cancer Res 1999; 5: 2714-2725 (Pubitemid 29493944)
54. Xing F, Yu Z, Liu J, et al. Anisomycin inhibits the behaviors of T cells and the allogeneic skin transplantation in mice. J Immunother 2008; 31: 858-870
55. Bunyard P, Handley M, Pollara G, et al. Ribotoxic stress activates p38 and JNK kinases and modulates the antigen-presenting activity of dendritic cells. Mol Immunol 2003; 39: 815-827 (Pubitemid 36263133)
56. Nader K, Schafe GE, Le Doux JE. Fear memories require protein synthesis in the amygdala for reconsolidation after retrieval. Nature 2000; 406: 722-726
57. Debiec J, LeDoux JE, Nader K. Cellular and systems reconsolidation in the hippocampus. Neuron 2002; 36: 527-538
58. Rudy JW. Is there a baby in the bathwater? Maybe: some methodological issues for the de novo protein synthesis hypothesis. Neurobiol Learn Mem 2008; 89: 219-224
59. Flood JF, Vidal D, Bennett EL, Orme AE, Vasquez S, Jarvik ME. Memory facilitating and anti-amnesic effects of corticosteroids. Pharmacol Biochem Behav 1978; 8: 81-87 (Pubitemid 8287113)
60. Flood JF, Bennett EL, Orme AE, Rosenzweig MR, Jarvik ME. Memory: modifications of anisomycin-induced amnesia by stimulants and depressants. Science 1978; 199: 324-326
61. Judge ME, Quartermain D. Alleviation of anisomycin-induced amnesia by pre-test treatment with lysine-vasopressin. Pharm Biochem Behav 1982; 16: 463-466 (Pubitemid 12147020)
62. Rudy JW, Biedenkapp JC, Moineau J, Bolding K. Anisomycin and the reconsolidation hypothesis. Learn Mem 2006; 13: 1-3.
63. Routtenberg A. The substrate for long-lasting memory: if not protein synthesis, then what? Neurobiol Learn Mem 2008; 89: 225-233
64. Wanisch K, Wotjak CT. Time course and efficiency of protein synthesis inhibition following intracerebral and systemic anisomycin treatment. Neurobiol Learn Mem 2008; 90: 485-494
65. Tronson NC, Taylor JR. Molecular mechanism of memory reconsolidation. Nature Rev Neurosci 2007; 8: 262-275.
66. Goard M, Aakalu G, Fedoryak OD, et al. Light-mediated inhibition of protein synthesis. Chem Biol 2005; 12: 685-693
67. Hanna J, Leggett DS, Finley D. Ubiquitin depletion as a key mediator of toxicity by translational inhibitors. Mol Cell Biol 2003; 23: 9251-9261 (Pubitemid 37499812)
68. Mahadevan LC, Edwards DR. Signalling and superinduction. Nature 1991; 349: 747-748
69. Zinck R, Cahill MA, Kracht M, Sachsenmaier C, Hipskind RA, Nordheim Protein synthesis inhibitors reveal differential regulation of mitogen-activated protein kinase and stress-activated protein kinase pathways that converge on Elk-1. Mol Cell Biol 1995; 15: 4930-4938
70. Dhawan P, Bell A, Kumar A, Golden C, Mehta KD. Critical role of p42/44 MAPK activation in anisomycin and hepatocyte growth factor-induced LDL receptor expression: activation of Raf-1/MEK-1/p42/44 MAPK cascade alone is sufficient to induce LDL receptor expression. J Lipid Res 1999; 40: 1911-1919 (Pubitemid 29477262)
71. Konishi Y, Sato H, Tanaka T. Anisomycin superinduces annexin V mRNA expression through the ERK1/2 but not the p38 MAP kinase pathway. Biochem Biophys Res Comm 2004; 313: 977-983 (Pubitemid 38050088)
72. Shin SY, Lee JH, Min B, Lee YH. The translation inhibitor anisomycin induces Elk-1-mediated transcriptional activation of egr-1 through multiple mitogen-activated protein kinase pathways. Exp Mol Med 2006; 38: 677-685
73. Faggioli L, Costanzo C, Merola M, Furia A, Palmieri M. Protein synthesis inhibitors cycloheximide and anisomycin induce interleukin-6 gene expression and activate transcription factor NF-kappaB. Biochem Biophys Res Commun 1997; 233: 507-513 (Pubitemid 27226658)
74. Park J, Liu AYC. JNK Phosphorylates the HSF1 transcriptional activation domain: Role of JNK in the regulation of the heat shock response. J Cell Biochem 2001; 82: 326-338 (Pubitemid 32606294)
75. Hemi R, Paz K, Wertheim N, Karasik A, Zick Y, Kanety H. Transactivation of ErbB2 and ErbB3 by tumor necrosis factor-alpha and anisomycin leads to impaired insulin signaling through serine/threonine phosphorylation of IRS proteins. J Biol Chem 2002; 277: 8961-8969 (Pubitemid 34952968)
76. Diradourian C, Le May C, Caüzac M, Girard J, Burnol AF, Pégorier JP. Involvement of ZIP/p62 in the regulation of PPARalpha transcriptional activity by p38-MAPK. Biochim Biophys Acta 2008; 1781: 239-244
77. Knebel A, Morrice N, Cohen P. A novel method to identify protein kinase substrates: eEF2 kinase is phosphorylated and inhibited by SAPK4/p38delta. EMBO J 2001; 20: 4360-4369 (Pubitemid 32772030)
78. Qun W, Jia-Yu Z, Shi-Jie L, Hong-Lian L. Overactivated mitogen-activated protein kinase by anisomycin induces tau hyperphosphorylation. Acta Physiologica Sinica 2008; 60: 485-491
79. Wang X, Mader MM, Toth JE, et al. Complete inhibition of anisomycin and UV radiation but not cytokine induced JNK and p38 activation by an aryl-substituted dihydropyrrolopyrazole quinoline and mixed lineage kinase 7 small interfering RNA. J Biol Chem 2005; 280: 19298-19305 (Pubitemid 41379637)
80. Hauser C, Schuettengruber B, Bartl S, Lagger G, Seiser C. Activation of the mouse histone deacetylase 1 gene by cooperative histone phosphorylation and acetylation. Mol Cell Biol 2002; 22: 7820-7830 (Pubitemid 35217293)
81. Kardalinou E, Zhelev N, Hazzalin CA, Mahadevan LC. Anisomycin and rapamycin define an area upstream of p70/85S6k containing a bifurcation to Histone H3-HMG-like protein phosphorylation and c-fos-c-jun induction. Mol Cell Biol 1994; 14: 1066-1074 (Pubitemid 24984254)
82. Adachi S, Natsume H, Yamauchi J, Matsushima-Nishiwaki R, Joe AK, Moriwaki H, Kozawa O. p38 MAP kinase controls EGF receptor downregulation via phosphorylation at Ser1046/1047. Cancer Lett 2009; 277: 108-113
83. Törocsik B, Szeberényi J. Anisomycin affects both pro- and antiapoptotic mechanisms in PC12 cells. Biochem Biophys Res Commun 2000; 278: 550-556