Emerging role of angiogenin in stress response and cell survival under adverse conditions

Journal of Cellular Physiology

Volumn 227, Issue 7, 2012, Pages 2822-2826

  Li, Shuping ^a,b   Hu, Guo Fu ^a,c  

^a TUFTS MEDICAL CENTER   (United States)

^b ZHEJIANG UNIVERSITY   (China)

^c TUFTS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOGENIN; ANGIOPOIETIN RECEPTOR; BAG 1 PROTEIN; EPIDERMAL GROWTH FACTOR; FIBROBLAST GROWTH FACTOR; FIBROBLAST GROWTH FACTOR 2; PROTEIN BCL 2; RIBONUCLEASE; RIBOSOME RNA; VASCULOTROPIN;

ANGIOGENESIS; BIOGENESIS; BIOSYNTHESIS; CANCER GROWTH; CELL GROWTH; CELL PROLIFERATION; CELL SURVIVAL; CELLULAR STRESS RESPONSE; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA CLEAVAGE; RNA TRANSCRIPTION; SHORT SURVEY;

ANIMALS; CELL GROWTH PROCESSES; CELL SURVIVAL; HUMANS; PROTEIN BIOSYNTHESIS; RIBONUCLEASE, PANCREATIC; RNA, TRANSFER; STRESS, PHYSIOLOGICAL;

VERTEBRATA;

EID: 84863350770     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.23051     Document Type: Short Survey

References (63)

1. Bonnal S, Schaeffer C, Creancier L, Clamens S, Moine H, Prats AC, Vagner S. 2003. A single internal ribosome entry site containing a G quartet RNA structure drives fibroblast growth factor 2 gene expression at four alternative translation initiation codons. J Biol Chem 278: 39330-39336.
2. Cho S, Zhang J. 2006. Ancient expansion of the ribonuclease A superfamily revealed by genomic analysis of placental and marsupial mammals. Gene 373: 116-125.
3. Coldwell MJ, deSchoolmeester ML, Fraser GA, Pickering BM, Packham G, Willis AE. 2001. The p36 isoform of BAG-1 is translated by internal ribosome entry following heat shock. Oncogene 20: 4095-4100.
4. Emara MM, Ivanov P, Hickman T, Dawra N, Tisdale S, Kedersha N, Hu GF, Anderson P. 2010. Angiogenin-induced tRNA-derived stress-induced RNAs promote stress-induced stress granule assembly. J Biol Chem 285: 10959-10968.
5. Fett JW, Strydom DJ, Lobb RR, Alderman EM, Bethune JL, Riordan JF, Vallee BL. 1985. Isolation and characterization of angiogenin, an angiogenic protein from human carcinoma cells. Biochemistry 24: 5480-5486.
6. Fu H, Feng J, Liu Q, Sun F, Tie Y, Zhu J, Xing R, Sun Z, Zheng X. 2009. Stress induces tRNA cleavage by angiogenin in mammalian cells. FEBS Lett 583: 437-442.
7. Fu H, Tie Y, Xu C, Zhang Z, Zhu J, Shi Y, Jiang H, Sun Z, Zheng X. 2005. Identification of human fetal liver miRNAs by a novel method. FEBS Lett 579: 3849-3854.
8. Giraud S, Greco A, Brink M, Diaz JJ, Delafontaine P. 2001. Translation initiation of the insulin-like growth factor I receptor mRNA is mediated by an internal ribosome entry site. J Biol Chem 276: 5668-5675.
9. Greenway MJ, Andersen PM, Russ C, Ennis S, Cashman S, Donaghy C, Patterson V, Swingler R, Kieran D, Prehn J, Morrison KE, Green A, Acharya KR, Brown RH Jr, Hardiman O. 2006. ANG mutations segregate with familial and 'sporadic' amyotrophic lateral sclerosis. Nat Genet 38: 411-413.
10. Haiser HJ, Karginov FV, Hannon GJ, Elliot MA. 2008. Developmentally regulated cleavage of tRNAs in the bacterium Streptomyces coelicolor. Nucleic Acids Res 36: 732-741.
11. Hallahan TW, Shapiro R, Vallee BL. 1991. Dual site model for the organogenic activity of angiogenin. Proc Natl Acad Sci USA 88: 2222-2226.
12. Hanahan D, Weinberg RA. 2000. The hallmarks of cancer. Cell 100: 57-70.
13. Hartmann A, Kunz M, Kostlin S, Gillitzer R, Toksoy A, Brocker EB, Klein CE. 1999. Hypoxia-induced up-regulation of angiogenin in human malignant melanoma. Cancer Res 59: 1578-1583.
14. Hirukawa S, Olson KA, Tsuji T, Hu GF. 2005. Neamine inhibits xenografic human tumor growth and angiogenesis in athymic mice. Clin Cancer Res 11: 8745-8752.
15. Holcik M, Lefebvre C, Yeh C, Chow T, Korneluk RG. 1999. A new internal-ribosome-entry-site motif potentiates XIAP-mediated cytoprotection. Nat Cell Biol 1: 190-192.
16. Hu GF, Riordan JF, Vallee BL. 1997. A putative angiogenin receptor in angiogenin-responsive human endothelial cells. Proc Natl Acad Sci USA 94: 2204-2209.
17. Ibaragi S, Yoshioka N, Kishikawa H, Hu JK, Sadow PM. Li M, Hu G-f 2009a. Angiogenin-stimulated ribosomal RNA transcription is essential for initiation and survival of AKT-induced prostate intraepithelial neoplasia. Mol Cancer Res 7: 415-424.
18. Ibaragi S, Yoshioka N, Li S, Hu MG, Hirukawa S, Sadow PM, Hu G-f. 2009b. Neamine inhibits prostate cancer growth by suppressing angiogenin-mediated ribosomal RNA transcription. Clin Cancer Res 15: 1981-1988
19. Ivanov P, Emara MM, Villen J, Gygi SP, Anderson P. 2011. Angiogenin-induced tRNA fragments inhibit translation initiation. Mol Cell 43: 613-623.
20. Jochl C, Rederstorff M, Hertel J, Stadler PF, Hofacker IL, Schrettl M, Haas H, Huttenhofer A. 2008. Small ncRNA transcriptome analysis from Aspergillus fumigatus suggests a novel mechanism for regulation of protein synthesis. Nucleic Acids Res 36: 2677-2689.
21. Kao RY, Jenkins JL, Olson KA, Key ME, Fett JW, Shapiro R. 2002. A small-molecule inhibitor of the ribonucleolytic activity of human angiogenin that possesses antitumor activity. Proc Natl Acad Sci USA 99: 10066-10071.
22. Katona TM, Neubauer BL, Iversen PW, Zhang S, Baldridge LA, Cheng L. 2005. Elevated expression of angiogenin in prostate cancer and its precursors. Clin Cancer Res 11: 8358-8363.
23. Kieran D, Sebastia J, Greenway MJ, King MA, Connaughton D, Concannon CG, Fenner B, Hardiman O, Prehn JH. 2008. Control of motoneuron survival by angiogenin. J Neurosci 28: 14056-14061.
24. Kishimoto K, Liu S, Tsuji T, Olson KA, Hu GF. 2005. Endogenous angiogenin in endothelial cells is a general requirement for cell proliferation and angiogenesis. Oncogene 24: 445-456.
25. Lang KJ, Kappel A, Goodall GJ. 2002. Hypoxia-inducible factor-1alpha mRNA contains an internal ribosome entry site that allows efficient translation during normoxia and hypoxia. Mol Biol Cell 13: 1792-1801.
26. Lee SR, Collins K. 2005. Starvation-induced cleavage of the tRNA anticodon loop in Tetrahymena thermophila. J Biol Chem 280: 42744-42749.
27. Li S, Hu GF. 2010. Angiogenin-mediated rRNA transcription in cancer and neurodegeneration. Int J Biochem Mol Biol 1: 26-35.
28. Li S, Ibaragi S, Hu GF. 2011. Angiogenin as a molecular target for the treatment of prostate cancer. Curr Cancer Ther Rev 7: 83-90.
29. Li S, Yu W, Kishikawa H, Hu GF. 2010. Angiogenin prevents serum withdrawal-induced apoptosis of P19 embryonal carcinoma cells. FEBS J 277: 3575-3587.
30. Majumder PK, Yeh JJ, George DJ, Febbo PG, Kum J, Xue Q, Bikoff R, Ma H, Kantoff PW, Golub TR, Loda M, Sellers WR. 2003. Prostate intraepithelial neoplasia induced by prostate restricted Akt activation: The MPAKT model. Proc Natl Acad Sci USA 100: 7841-7846.
31. Martineau Y, Le Bec C, Monbrun L, Allo V, Chiu IM, Danos O, Moine H, Prats H, Prats AC. 2004. Internal ribosome entry site structural motifs conserved among mammalian fibroblast growth factor 1 alternatively spliced mRNAs. Mol Cell Biol 24: 7622-7635.
32. McEwen E, Kedersha N, Song B, Scheuner D, Gilks N, Han A, Chen JJ, Anderson P, Kaufman RJ. 2005. Heme-regulated inhibitor kinase-mediated phosphorylation of eukaryotic translation initiation factor 2 inhibits translation, induces stress granule formation, and mediates survival upon arsenite exposure. J Biol Chem 280: 16925-16933.
33. Mitchell SA, Spriggs KA, Bushell M, Evans JR, Stoneley M, Le Quesne JP, Spriggs RV, Willis AE. 2005. Identification of a motif that mediates polypyrimidine tract-binding protein-dependent internal ribosome entry. Genes Dev 19: 1556-1571.
34. Moroianu J, Riordan JF. 1994a. Identification of the nucleolar targeting signal of human angiogenin. Biochem Biophys Res Commun 203: 1765-1772.
35. Moroianu J, Riordan JF. 1994b. Nuclear translocation of angiogenin in proliferating endothelial cells is essential to its angiogenic activity. Proc Natl Acad Sci USA 91: 1677-1681.
36. Moss T. 2004. At the crossroads of growth control; making ribosomal RNA. Curr Opin Genet Dev 14: 210-217.
37. Nakamura M, Yamabe H, Osawa H, Nakamura N, Shimada M, Kumasaka R, Murakami R, Fujita T, Osanai T, Okumura K. 2006. Hypoxic conditions stimulate the production of angiogenin and vascular endothelial growth factor by human renal proximal tubular epithelial cells in culture. Nephrol Dial Transplant 21: 1489-1495.
38. Nazar RN. 2004. Ribosomal RNA processing and ribosome biogenesis in eukaryotes. IUBMB Life 56: 457-465.
39. Olson KA, Byers HR, Key ME, Fett JW. 2001. Prevention of human prostate tumor metastasis in athymic mice by antisense targeting of human angiogenin. Clin Cancer Res 7: 3598-3605.
40. Olson KA, Byers HR, Key ME, Fett JW. 2002. Inhibition of prostate carcinoma establishment and metastatic growth in mice by an antiangiogenin monoclonal antibody. Int J Cancer 98: 923-929.
41. Olson KA, Fett JW, French TC, Key ME, Vallee BL. 1995. Angiogenin antagonists prevent tumor growth in vivo. Proc Natl Acad Sci USA 92: 442-446.
42. Park EH, Lee JM, Blais JD, Bell JC, Pelletier J. 2005. Internal translation initiation mediated by the angiogenic factor Tie2. J Biol Chem 280: 20945-20953.
43. Pozner A, Goldenberg D, Negreanu V, Le SY, Elroy-Stein O, Levanon D, Groner Y. 2000. Transcription-coupled translation control of AML1/RUNX1 is mediated by cap- and internal ribosome entry site-dependent mechanisms. Mol Cell Biol 20: 2297-2307.
44. Ruggero D, Pandolfi PP. 2003. Does the ribosome translate cancer? Nat Rev Cancer 3: 179-192.
45. Sebastia J, Kieran D, Breen B, King MA, Netteland DF, Joyce D, Fitzpatrick SF, Taylor CT, Prehn JH. 2009. Angiogenin protects motoneurons against hypoxic injury. Cell Death Differ 16: 1238-1247.
46. Shapiro R, Vallee BL. 1989. Site-directed mutagenesis of histidine-13 and histidine-114 of human angiogenin. Alanine derivatives inhibit angiogenin-induced angiogenesis Biochemistry 28: 7401-7408.
47. Sherrill KW, Byrd MP, Van Eden ME, Lloyd RE. 2004. BCL-2 translation is mediated via internal ribosome entry during cell stress. J Biol Chem 279: 29066-29074.
48. Stein I, Itin A, Einat P, Skaliter R, Grossman Z, Keshet E. 1998. Translation of vascular endothelial growth factor mRNA by internal ribosome entry: Implications for translation under hypoxia. Mol Cell Biol 18: 3112-3119.
49. Stoneley M, Paulin FE, Le Quesne JP, Chappell SA, Willis AE. 1998. C-Myc 5′ untranslated region contains an internal ribosome entry segment. Oncogene 16: 423-428.
50. Strydom DJ, Fett JW, Lobb RR, Alderman EM, Bethune JL, Riordan JF, Vallee BL. 1985. Amino acid sequence of human tumor derived angiogenin. Biochemistry 24: 5486-5494.
51. Subramanian V, Crabtree B, Acharya KR. 2008. Human angiogenin is a neuroprotective factor and amyotrophic lateral sclerosis associated angiogenin variants affect neurite extension/pathfinding and survival of motor neurons. Hum Mol Genet 17: 130-149.
52. Thompson DM, Lu C, Green PJ, Parker R. 2008. tRNA cleavage is a conserved response to oxidative stress in eukaryotes. RNA 14: 2095-2103.
53. Trouillon R, Kang DK, Park H, Chang SI, O'Hare D. 2010. Angiogenin induces nitric oxide synthesis in endothelial cells through PI-3 and Akt kinases. Biochemistry 49: 3282-3288.
54. Tsuji T, Sun Y, Kishimoto K, Olson KA, Liu S, Hirukawa S, Hu GF. 2005. Angiogenin is translocated to the nucleus of HeLa cells and is involved in ribosomal RNA transcription and cell proliferation. Cancer Res 65: 1352-1360.
55. Verselis SJ, Olson KA, Fett JW. 1999. Regulation of angiogenin expression in human HepG2 hepatoma cells by mediators of the acute-phase response. Biochem Biophys Res Commun 259: 178-184.
56. Warnakulasuriyarachchi D, Cerquozzi S, Cheung HH, Holcik M. 2004. Translational induction of the inhibitor of apoptosis protein HIAP2 during endoplasmic reticulum stress attenuates cell death and is mediated via an inducible internal ribosome entry site element. J Biol Chem 279: 17148-17157.
57. Weiner HL, Weiner LH, Swain JL. 1987. Tissue distribution and developmental expression of the messenger RNA encoding angiogenin. Science 237: 280-282.
58. Wu D, Yu W, Kishikawa H, Folkerth RD, Iafrate AJ, Shen Y, Xin W, Sims K, Hu GF. 2007. Angiogenin loss-of-function mutations in amyotrophic lateral sclerosis. Ann Neurol 62: 609-617.
59. Xu ZP, Tsuji T, Riordan JF, Hu GF. 2002. The nuclear function of angiogenin in endothelial cells is related to rRNA production. Biochem Biophys Res Commun 294: 287-292.
60. Xu ZP, Tsuji T, Riordan JF, Hu GF. 2003. Identification and characterization of an angiogenin-binding DNA sequence that stimulates luciferase reporter gene expression. Biochemistry 42: 121-128.
61. Yamasaki S, Anderson P. 2008. Reprogramming mRNA translation during stress. Curr Opin Cell Biol 20: 222-226.
62. Yamasaki S, Ivanov P, Hu GF, Anderson P. 2009. Angiogenin cleaves tRNA and promotes stress-induced translational repression. J Cell Biol 185: 35-42.
63. Yoshioka N, Wang L, Kishimoto K, Tsuji T, Hu GF. 2006. A therapeutic target for prostate cancer based on angiogenin-stimulated angiogenesis and cancer cell proliferation. Proc Natl Acad Sci USA 103: 14519-14524.