Mechanisms of action of angiogenin
Xiangwei Gao,
Zhengping Xu,
Xiangwei Gao
Research Center for Environmental Genomics, and Bioelectromagnetics Laboratory, Zhejiang University School of Medicine, Hangzhou 310058, China
Search for more papers by this authorCorresponding Author
Zhengping Xu
Research Center for Environmental Genomics, and Bioelectromagnetics Laboratory, Zhejiang University School of Medicine, Hangzhou 310058, China
*Corresponding author: Tel, 86-571-88208164; Fax, 86-571-88208163; E-mail, [email protected]Search for more papers by this authorXiangwei Gao,
Zhengping Xu,
Xiangwei Gao
Research Center for Environmental Genomics, and Bioelectromagnetics Laboratory, Zhejiang University School of Medicine, Hangzhou 310058, China
Search for more papers by this authorCorresponding Author
Zhengping Xu
Research Center for Environmental Genomics, and Bioelectromagnetics Laboratory, Zhejiang University School of Medicine, Hangzhou 310058, China
*Corresponding author: Tel, 86-571-88208164; Fax, 86-571-88208163; E-mail, [email protected]Search for more papers by this authorThis work was supported by grants from the National Natural Science Foundation of China (30171035, 30470670 and 30770470), the Program for New Century Excellent Talents in University (No. NCET-05-0521) and the Zhejiang Provincial Program for the Cultivation of High-level Innovative Health Talents (2007-191)
Abstract
Angiogenin induces angiogenesis by activating vessel endothelial and smooth muscle cells and triggering a number of biological processes, including cell migration, invasion, proliferation, and formation of tubular structures. It has been reported that angiogenin plays its functions mainly through four pathways: (1) exerting its ribonucleolytic activity; (2) binding to membrane actin and then inducing basement membrane degradation; (3) binding to a putative 170-kDa protein and subsequently transducing signal into cytoplasm; and (4) translocating into the nucleus of target cells directly and then enhancing ribosomal RNA transcription. Angiogenin can also translocate into the nucleus of cancer cells and induces the corresponding cell proliferation. Furthermore, angiogenin has neuroprotective activities in the central nervous system and the loss of its function may be related to amyotrophic lateral sclerosis. This review intends to conclude the mechanisms underlying these actions of angiogenin and give a perspective on future research.
References
- 1 Fett JW, Strydom DJ, Lobb RR, Alderman EM, Bethune JL, Riordan JF, Vallee BL. Isolation and characterization of angiogenin, an angiogenic protein from human carcinoma cells. Biochemistry 1985, 24: 5480–5486.
- 2 Weremowicz S, Fox EA, Morton CC, Vallee BL. Localization of the human angiogenin gene to chromosome band 14q11, proximal to the T cell receptor α/Δ locus. Am J Hum Genet 1990, 47: 973–981.
- 3 Folkman J. Angiogenesis: an organizing principle for drug discovery? Nat Rev Drug Discov 2007, 6: 273–286.
- 4 Strydom DJ, Fett JW, Lobb RR, Alderman EM, Bethune JL, Riordan JF, Vallee BL. Amino acid sequence of human tumor derived angiogenin. Biochemistry 1985, 24: 5486–5494.
- 5 Acharya KR, Shapiro R, Allen SC, Riordan JF, Vallee BL. Crystal structure of human angiogenin reveals the structural basis for its functional divergence from ribonuclease. Proc Natl Acad Sci USA 1994, 91: 2915–2919.
- 6 Russo N, Shapiro R, Acharya KR, Riordan JF, Vallee BL. Role of glutamine-117 in the ribonucleolytic activity of human angiogenin. Proc Natl Acad Sci USA 1994, 91: 2920–2924.
- 7 Shapiro R, Vallee BL. Site-directed mutagenesis of histidine-13 and histidine-114 of human angiogenin. Alanine derivatives inhibit angiogenin-induced angiogenesis. Biochemistry 1989, 28: 7401–7408.
- 8 Shapiro R, Fox EA, Riordan JF. Role of lysines in human angiogenin: chemical modification and site-directed mutagenesis. Biochemistry 1989, 28: 1726–1732.
- 9 Shapiro R, Vallee BL. Human placental ribonuclease inhibitor abolishes both angiogenic and ribonucleolytic activities of angiogenin. Proc Natl Acad Sci USA 1987, 84: 2238–2241.
- 10 Kao RY, Jenkins JL, Olson KA, Key ME, Fett JW, Shapiro R. A small-molecule inhibitor of the ribonucleolytic activity of human angiogenin that possesses antitumor activity. Proc Natl Acad Sci USA 2002, 99: 10066–10071.
- 11 Hallahan TW, Shapiro R, Vallee BL. Dual site model for the organogenic activity of angiogenin. Proc Natl Acad Sci USA 1991, 88: 2222–2226.
- 12 Hu GF, Chang SI, Riordan JF, Vallee BL. An angiogenin-binding protein from endothelial cells. Proc Natl Acad Sci USA 1991, 88: 2227–2231.
- 13 Hu GF, Strydom DJ, Fett JW, Riordan JF, Vallee BL. Actin is a binding protein for angiogenin. Proc Natl Acad Sci USA 1993, 90: 1217–1221.
- 14 Hu G, Riordan JF, Vallee BL. Angiogenin promotes invasiveness of cultured endothelial cells by stimulation of cell-associated proteolytic activities. Proc Natl Acad Sci USA 1994, 91: 12096–12100.
- 15 Soncin F. Angiogenin supports endothelial and fibroblast cell adhesion. Proc Natl Acad Sci USA 1992, 89: 2232–2236.
- 16 Hu GF, Riordan JF, Vallee BL. A putative angiogenin receptor in angiogenin-responsive human endothelial cells. Proc Natl Acad Sci USA 1997, 94: 2204–2209.
- 17 Liu S, Yu D, Xu ZP, Riordan JF, Hu GF. Angiogenin activates ERK1/2 in human umbilical vein endothelial cells. Biochem Biophys Res Commun 2001, 287: 305–310.
- 18 Kim HM, Kang DK, Kim HY, Kang SS, Chang SI. 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 2007, 352: 509–513.
- 19 Xu Z, Monti DM, Hu G. Angiogenin activates human umbilical artery smooth muscle cells. Biochem Biophys Res Commun 2001, 285: 909–914.
- 20 Hu GF. Neomycin inhibits angiogenin-induced angiogenesis. Proc Natl Acad Sci USA 1998, 95: 9791–9795.
- 21 Moroianu J, Riordan JF. Nuclear translocation of angiogenin in proliferating endothelial cells is essential to its angiogenic activity. Proc Natl Acad Sci USA 1994, 91: 1677–1681.
- 22
Hu G,
Xu C,
Riordan JF.
Human angiogenin is rapidly translocated to the nucleus of human umbilical vein endothelial cells and binds to DNA.
J Cell Biochem
2000, 76: 452–462.
10.1002/(SICI)1097-4644(20000301)76:3<452::AID-JCB12>3.0.CO;2-Z CAS PubMed Web of Science® Google Scholar
- 23 Xu ZP, Tsuji T, Riordan JF, Hu GF. The nuclear function of angiogenin in endothelial cells is related to rRNA production. Biochem Biophys Res Commun 2002, 294: 287–292.
- 24 Xu ZP, Tsuji T, Riordan JF, Hu GF. Identification and characterization of an angiogenin-binding DNA sequence that stimulates luciferase reporter gene expression. Biochemistry 2003, 42: 121–128.
- 25 Kishimoto K, Liu S, Tsuji T, Olson KA, Hu GF. Endogenous angiogenin in endothelial cells is a general requirement for cell proliferation and angiogenesis. Oncogene 2005, 24: 445–456.
- 26 Moroianu J, Riordan JF. Identification of the nucleolar targeting signal of human angiogenin. Biochem Biophys Res Commun 1994, 203: 1765–1772.
- 27 Lixin R, Efthymiadis A, Henderson B, Jans DA. Novel properties of the nucleolar targeting signal of human angiogenin. Biochem Biophys Res Commun 2001, 284: 185–193.
- 28 Li R, Riordan JF, Hu G. Nuclear translocation of human angiogenin in cultured human umbilical artery endothelial cells is microtubule and lysosome independent. Biochem Biophys Res Commun 1997, 238: 305–312.
- 29 Yoshioka N, Wang L, Kishimoto K, Tsuji T, Hu GF. A therapeutic target for prostate cancer based on angiogenin-stimulated angiogenesis and cancer cell proliferation. Proc Natl Acad Sci USA 2006, 103: 14519–14524.
- 30 Tsuji T, Sun Y, Kishimoto K, Olson KA, Liu S, Hirukawa S, Hu GF. Angiogenin is translocated to the nucleus of HeLa cells and is involved in ribosomal RNA transcription and cell proliferation. Cancer Res 2005, 65: 1352–1360.
- 31 Soncin F, Shapiro R, Fett JW. A cell-surface proteoglycan mediates human adenocarcinoma HT-29 cell adhesion to human angiogenin. J Biol Chem 1994, 269: 8999–9005.
- 32 Oosthuyse B, Moons L, Storkebaum E, Beck H, Nuyens D, Brusselmans K, Van Dorpe J et al. Deletion of the hypoxia-response element in the vascular endothelial growth factor promoter causes motor neuron degeneration. Nat Genet 2001, 28: 131–138.
- 33 Greenway MJ, Alexander MD, Ennis S, Traynor BJ, Corr B, Frost E, Green A et al. A novel candidate region for ALS on chromosome 14q11.2. Neurology 2004, 63: 1936–1938.
- 34 Greenway MJ, Andersen PM, Russ C, Ennis S, Cashman S, Donaghy C, Patterson V et al. ANG mutations segregate with familial and “sporadic” amyotrophic lateral sclerosis. Nat Genet 2006, 38: 411–413.
- 35 Wu D, Yu W, Kishikawa H, Folkerth RD, Iafrate AJ, Shen Y, Xin W et al. Angiogenin loss-of-function mutations in amyotrophic lateral sclerosis. Ann Neurol 2007, 62: 609–617.
- 36 Crabtree B, Thiyagarajan N, Prior SH, Wilson P, Iyer S, Ferns T, Shapiro R et al. Characterization of human angiogenin variants implicated in amyotrophic lateral sclerosis. Biochemistry 2007, 46: 11810–11818.
- 37 Corrado L, Battistini S, Penco S, Bergamaschi L, Testa L, Ricci C, Giannini F et al. Variations in the coding and regulatory sequences of the angiogenin (ANG) gene are not associated to ALS (amyotrophic lateral sclerosis) in the Italian population. J Neurol Sci 2007, 258: 123–127.
- 38 Conforti FL, Sprovieri T, Mazzei R, Ungaro C, La Bella V, Tessitore A, Patitucci A et al. A novel Angiogenin gene mutation in a sporadic patient with amyotrophic lateral sclerosis from southern Italy. Neuromuscul Disord 2008, 18: 68–70.
- 39 Gellera C, Colombrita C, Ticozzi N, Castellotti B, Bragato C, Ratti A, Taroni F et al. Identification of new ANG gene mutations in a large cohort of Italian patients with amyotrophic lateral sclerosis. Neurogenetics 2008, 9: 33–40.
- 40 Subramanian V, Feng Y. A new role for angiogenin in neurite growth and pathfinding: implications for amyotrophic lateral sclerosis. Hum Mol Genet 2007, 16: 1445–1453.
- 41 Subramanian V, Crabtree B, Acharya KR. Human angiogenin is a neuroprotective factor and amyotrophic lateral sclerosis associated angiogenin variants affect neurite extension/pathfinding and survival of motor neurons. Hum Mol enet 2008, 17: 130–149.
- 42 Suzumori N, Zhao XX, Suzumori K. Elevated angiogenin levels in the peritoneal fluid of women with endometriosis correlate with the extent of the disorder. Fertil Steril 2004, 82: 93–96.
- 43 Burgmann H, Hollenstein U, Maca T, Zedwitz-Liebenstein K, Thalhammer F, Koppensteiner R, Ehringer H et al. Increased serum laminin and angiogenin concentrations in patients with peripheral arterial occlusive disease. J Clin Pathol 1996, 49: 508–510.
- 44 Koutroubakis IE, Xidakis C, Karmiris K, Sfiridaki A, Kandidaki E, Kouroumalis EA. Serum angiogenin in inflammatory bowel disease. Dig Dis Sci 2004, 49: 1758–1762.
- 45 Hosaka S, Shah MR, Barquin N, Haines GK, Koch AE. Expression of basic fibroblast growth factor and angiogenin in arthritis. Pathobiology 1995, 63: 249–256.
- 46 Chiarelli F, Pomilio M, Mohn A, Tumini S, Verrotti A, Mezzetti A, Cipollone F et al. Serum angiogenin concentrations in young patients with diabetes mellitus. Eur J Clin Invest 2002, 32: 110–114.
- 47 Shapiro R, Riordan JF, Vallee BL. Characteristic ribonucleolytic activity of human angiogenin. Biochemistry 1986, 25: 3527–3532.
- 48 Saxena SK, Rybak SM, Davey RT Jr, Youle RJ, Ackerman EJ. Angiogenin is a cytotoxic, tRNA-specific ribonuclease in the RNase A superfamily. J Biol Chem 1992, 267: 21982–21986.
- 49 Rybak SM, Vallee BL. Base cleavage specificity of angiogenin with Saccharomyces cerevisiae and Escherichia coli 5S RNAs. Biochemistry 1988, 27: 2288–2294.
- 50 Leland PA, Staniszewski KE, Park C, Kelemen BR, Raines RT. The ribonucleolytic activity of angiogenin. Biochemistry 2002, 41: 1343–1350.
- 51 Hu H, Gao X, Sun Y, Zhou J, Yang M, Xu Z. α-actinin-2, a cytoskeletal protein, binds to angiogenin. Biochem Biophys Res Commun 2005, 329: 661–667.
- 52 Gao X, Hu H, Zhu J, Xu Z. Identification and characterization of follistatin as a novel angiogenin-binding protein. FEBS Lett 2007, 581: 5505–5510.
- 53 Zhang H, Gao X, Weng C and Xu Z. Interaction between angiogenin and fibulin 1: evidence and implication. Acta Biochim Biophys Sin 2008, 40: 375–380.
- 54 Piccoli R, Olson KA, Vallee BL, Fett JW. Chimeric anti-angiogenin antibody cAb 26-2F inhibits the formation of human breast cancer xenografts in athymic mice. Proc Natl Acad Sci USA 1998, 95: 4579–4583.
- 55 Gho YS, Chae CB. Anti-angiogenin activity of the peptides complementary to the receptor-binding site of angiogenin. J Biol Chem 1997, 272: 24294–24299.
- 56 Olson KA, Byers HR, Key ME, Fett JW. Prevention of human prostate tumor metastasis in athymic mice by antisense targeting of human angiogenin. Clin Cancer Res 2001, 7: 3598–3605.
