Characterization of the angiogenic activity of zebrafish ribonucleases

FEBS Journal

Volumn 276, Issue 15, 2009, Pages 4077-4090

  Monti, Daria M ^a   Yu, Wenhao ^b   Pizzo, Elio ^a   Shima, Kaori ^b   Hu, Miaofen G ^c   Di Malta, Chiara ^a   Piccoli, Renata ^a   D'Alessio, Giuseppe ^a   Hu, Guo Fu ^b  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^b HARVARD MEDICAL SCHOOL   (United States)

^c TUFTS MEDICAL CENTER   (United States)

Author keywords

Amyotrophic lateral sclerosis; Angiogenesis; Angiogenin; Ribonuclease; Zebrafish

Indexed keywords

ANGIOGENIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PANCREATIC RIBONUCLEASE; RIBONUCLEASE; RIBONUCLEASE III; RIBOSOME RNA; UNCLASSIFIED DRUG; ZEBRAFISH RIBONUCLEASE;

ANGIOGENESIS; ARTICLE; CELL SURFACE; CONCENTRATION RESPONSE; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME ACTIVITY; ENZYME BINDING; GENE TRANSLOCATION; HELA CELL; HUMAN; HUMAN CELL; HUMAN UMBILICAL VEIN ENDOTHELIAL CELL; NUCLEOLUS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RNA TRANSCRIPTION; SEQUENCE HOMOLOGY; UMBILICAL VEIN; ZEBRA FISH;

ANIMALS; DISULFIDES; ENDOTHELIUM, VASCULAR; EOSINOPHIL CATIONIC PROTEIN; HELA CELLS; HUMANS; NEOVASCULARIZATION, PHYSIOLOGIC; RIBONUCLEASE, PANCREATIC; RIBONUCLEASES; UMBILICAL VEINS; ZEBRAFISH;

DANIO RERIO;

EID: 68149178338     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2009.07115.x     Document Type: Article

References (68)

1. Beintema JJ, Breukelman HJ, Carsana A Furia A (1997) Evolution of vertebrate ribonucleases: ribonuclease A superfamily. In Ribonucleases: Structures and Functions (D'Alessio G Riordan JF, eds pp 245 269. Academic Press, San Diego, CA.
2. Riordan JF (1997) Structure and function of angiogenin. In Ribonucleases: Structures and Functions (D'Alessio G Riordan JF, eds pp 446 466. Academic Press, New York, NY.
3. Matousek J (1994) Aspermatogenic effect of the bull seminal ribonuclease (BS RNase) in the presence of anti-BS RNase antibodies in mice. Anim Genet 25 (Suppl 1 45 50.
4. Harder J Schroder JM (2002) RNase 7, a novel innate immune defense antimicrobial protein of healthy human skin. J Biol Chem 277, 46779 46784.
5. Youle RJ D'Alessio G (1997) Antitumor RNases. In Ribonucleases Structures and Function (D'Alessio G Riordan JF, eds pp 491 514. Academic Press, San Diego, CA.
6. Tamburrini M, Scala G, Verde C, Ruocco M.R, Parente A, Venuta S., D'Alessio G, Tamburrini M, Scala G, Verde C et al. (1990) Immunosuppressive activity of bovine seminal RNase on T-cell proliferation. Eur J Biochem 190, 145 148.
7. Rosenberg HF (1995) Recombinant human eosinophil cationic protein. Ribonuclease activity is not essential for cytotoxicity. J Biol Chem 270, 7876 7881.
8. Huang YC, Lin YM, Chang TW, Wu SJ, Lee YS, Chang MD, Chen C, Wu SH Liao YD (2007) The flexible and clustered lysine residues of human ribonuclease 7 are critical for membrane permeability and antimicrobial activity. J Biol Chem 282, 4626 4633.
9. Fett JW, Strydom DJ, Lobb RR, Alederman EM, Bethune JL, Riordan JF Vallee B (1985) Isolation and characterization of angiogenin, an angiogenic protein from human carcinoma cells. Biochemistry 24, 5480 5486.
10. Strydom DJ (1998) The angiogenins. Cell Mol Life Sci 54, 811 824.
11. Nitto T, Dyer KD, Czapiga M Rosenberg HF (2006) Evolution and function of leukocyte RNase A ribonucleases of the avian species, Gallus gallus. J Biol Chem 281, 25622 25634.
12. Cho S Zhang J (2007) Zebrafish ribonucleases are bactericidal: implications for the origin of the vertebrate RNase A superfamily. Mol Biol Evol 24, 1259 1268.
13. Kazakou K, Holloway DE, Prior SH, Subramanian V Acharya KR (2008) Ribonuclease A homologues of the zebrafish: polymorphism, crystal structures of two representatives and their evolutionary implications. J Mol Biol 380, 206 222.
14. Pizzo E, Buonanno P, Di Maro A, Ponticelli S, De Falco S, Quarto N, Cubellis MV D'Alessio G (2006) Ribonucleases and angiogenins from fish. J Biol Chem 281, 27454 27460.
15. Pizzo E, Varcamonti M, Di Maro A, Zanfardino A, Giancola C D'Alessio G (2008) Ribonucleases with angiogenic and bactericidal activities from the Atlantic salmon. Febs J 275, 1283 1295.
16. Hooper LV, Stappenbeck TS, Hong CV Gordon JI (2003) Angiogenins: a new class of microbicidal proteins involved in innate immunity. Nat Immunol 4, 269 273.
17. Shapiro R, Riordan JF Vallee BL (1986) Characteristic ribonucleolytic activity of human angiogenin. Biochemistry 25, 3527 3532.
18. Hu G, Riordan JF Vallee BL (1994) Angiogenin promotes invasiveness of cultured endothelial cells by stimulation of cell-associated proteolytic activities. Proc Natl Acad Sci USA 91, 12096 12100.
19. 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.
20. Jimi S, Ito K, Kohno K, Ono M, Kuwano M, Itagaki Y Ishikawa H (1995) Modulation by bovine angiogenin of tubular morphogenesis and expression of plasminogen activator in bovine endothelial cells. Biochem Biophys Res Commun 211, 476 483.
21. 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.
22. Li R, Riordan JF Hu G (1997) Nuclear translocation of human angiogenin in cultured human umbilical artery endothelial cells is microtubule and lysosome independent. Biochem Biophys Res Commun 238, 305 312.
23. Hu G, Xu C Riordan JF (2000) Human angiogenin is rapidly translocated to the nucleus of human umbilical vein endothelial cells and binds to DNA. J Cell Biochem 76, 452 462.
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. 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.
26. 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.
27. Greenway MJ, Alexander MD, Ennis S, Traynor BJ, Corr B, Frost E, Green A Hardiman O (2004) A novel candidate region for ALS on chromosome 14q11.2. Neurology 63, 1936 1938.
28. Conforti FL, Sprovieri T, Mazzei R, Ungaro C, La Bella V, Tessitore A, Patitucci A, Magariello A, Gabriele AL, Tedeschi G et al. (2007) A novel Angiogenin gene mutation in a sporadic patient with amyotrophic lateral sclerosis from southern Italy. Neuromuscul Disord 18, 68 70.
29. Gellera C, Colombrita C, Ticozzi N, Castellotti B, Bragato C, Ratti A, Taroni F Silani V (2008) Identification of new ANG gene mutations in a large cohort of Italian patients with amyotrophic lateral sclerosis. Neurogenetics 9, 33 40.
30. Greenway MJ, Andersen PM, Russ C, Ennis S, Cashman S, Donaghy C, Patterson V, Swingler R, Kieran D, Prehn J et al. (2006) ANG mutations segregate with familial and 'sporadic' amyotrophic lateral sclerosis. Nat Genet 38, 411 413.
31. Crabtree B, Thiyagarajan N, Prior SH, Wilson P, Iyer S, Ferns T, Shapiro R, Brew K, Subramanian V Acharya KR (2007) Characterization of human angiogenin variants implicated in amyotrophic lateral sclerosis. Biochemistry 46, 11810 11818. (Pubitemid 47623749)
32. Subramanian V Feng Y (2007) A new role for angiogenin in neurite growth and pathfinding: implications for amyotrophic lateral sclerosis. Hum Mol Genet 16, 1445 1453.
33. 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.
34. 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.
35. Childs S, Chen JN, Garrity DM Fishman MC (2002) Patterning of angiogenesis in the zebrafish embryo. Development 129, 973 982.
36. Lemmens R, Van Hoecke A, Hersmus N, Geelen V, D'Hollander I, Thijs V, Van Den Bosch L, Carmeliet P Robberecht W (2007) Overexpression of mutant superoxide dismutase 1 causes a motor axonopathy in the zebrafish. Hum Mol Genet 16, 2359 2365.
37. Winkler C, Eggert C, Gradl D, Meister G, Giegerich M, Wedlich D, Laggerbauer B Fischer U (2005) Reduced U snRNP assembly causes motor axon degeneration in an animal model for spinal muscular atrophy. Genes Dev 19, 2320 2330.
38. Acharya KR, Shapiro R, Allen SC, Riordan JF Vallee BL (1994) Crystal structure of human angiogenin reveals the structural basis for its functional divergence from ribonuclease. Proc Natl Acad Sci USA 91, 2915 2919.
39. 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.
40. Adams SA Subramanian V (1999) The angiogenins: an emerging family of ribonuclease related proteins with diverse cellular functions. Angiogenesis 3, 189 199.
41. 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.
42. Badet J, Soncin F, Guitton JD, Lamare O, Cartwright T Barritault D (1989) Specific binding of angiogenin to calf pulmonary artery endothelial cells. Proc Natl Acad Sci USA 86, 8427 8431.
43. Liu S, Yu D, Xu ZP, Riordan JF Hu GF (2001) Angiogenin activates Erk1/2 in human umbilical vein endothelial cells. Biochem Biophys Res Commun 287, 305 310.
44. Kim HM, Kang DK, Kim HY, Kang SS Chang SI (2007) Angiogenin-induced protein kinase B/Akt activation is necessary for angiogenesis but is independent of nuclear translocation of angiogenin in HUVE cells. Biochem Biophys Res Commun 352, 509 513.
45. Moroianu J Riordan JF (1994) Nuclear translocation of angiogenin in proliferating endothelial cells is essential to its angiogenic activity. Proc Natl Acad Sci USA 91, 1677 1681. (Pubitemid 24080268)
46. 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.
47. Eichler DC Craig N (1994) Processing of eukaryotic ribosomal RNA. Prog Nucleic Acid Res Mol Biol 49, 197 239.
48. Maden BE (1990) The numerous modified nucleotides in eukaryotic ribosomal RNA. Prog Nucleic Acid Res Mol Biol 39, 241 303.
49. Kass S, Craig N Sollner-Webb B (1987) Primary processing of mammalian rRNA involves two adjacent cleavages and is not species specific. Mol Cell Biol 7, 2891 2898.
50. Miller KG Sollner-Webb B (1981) Transcription of mouse rRNA genes by RNA polymerase I: in vitro and in vivo initiation and processing sites. Cell 27, 165 174.
51. Mougey EB, Pape LK Sollner-Webb B (1993) A U3 small nuclear ribonucleoprotein-requiring processing event in the 5′ external transcribed spacer of Xenopus precursor rRNA. Mol Cell Biol 13, 5990 5998.
52. Craig N, Kass S Sollner-Webb B (1987) Nucleotide sequence determining the first cleavage site in the processing of mouse precursor rRNA. Proc Natl Acad Sci USA 84, 629 633.
53. Tello-Montoliu A, Patel JV Lip GY (2006) Angiogenin: a review of the pathophysiology and potential clinical applications. J Thromb Haemost 4, 1864 1874.
54. Acharya KR, Shapiro R, Riordan JF Vallee BL (1995) Crystal structure of bovine angiogenin at 1.5-A resolution. Proc Natl Acad Sci USA 92, 2949 2953.
55. Chavali GB, Papageorgiou AC, Olson KA, Fett JW, Hu G, Shapiro R Acharya KR (2003) The crystal structure of human angiogenin in complex with an antitumor neutralizing antibody. Structure 11, 875 885.
56. Shapiro R Vallee BL (1992) Identification of functional arginines in human angiogenin by site-directed mutagenesis. Biochemistry 31, 12477 12485.
57. 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.
58. 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.
59. 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.
60. Kishikawa H, Wu D Hu GF (2008) Targeting angiogenin in therapy of amyotropic lateral sclerosis. Expert Opin Ther Targets 12, 1229 1242.
61. Moroianu J Riordan JF (1994) Identification of the nucleolar targeting signal of human angiogenin. Biochem Biophys Res Commun 203, 1765 1772.
62. Comai L (1999) The nucleolus: a paradigm for cell proliferation and aging. Braz J Med Biol Res 32, 1473 1478.
63. Melese T Xue Z (1995) The nucleolus: an organelle formed by the act of building a ribosome. Curr Opin Cell Biol 7, 319 324.
64. Stoykova AS, Dabeva MD, Dimova RN Hadjiolov AA (1985) Ribosome biogenesis and nucleolar ultrastructure in neuronal and oligodendroglial rat brain cells. J Neurochem 45, 1667 1676.
65. Russo N, Shapiro R, Acharya KR, Riordan JF Vallee BL (1994) Role of glutamine-117 in the ribonucleolytic activity of human angiogenin. Proc Natl Acad Sci USA 91, 2920 2924.
66. Shapiro R, Harper JW, Fox EA, Jansen HW, Hein F Uhlmann E (1988) Expression of Met-(-1) angiogenin in Escherichia coli: conversion to the authentic less than Glu-1 protein. Anal Biochem 175, 450 461.
67. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A Speleman F (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3, RESEARCH0034.
68. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29, e45.