Structural and functional implications of positive selection at the primate angiogenin gene

Springer Science and Business Media LLC - Tập 7 Số 1 - 2007
Daniel S. Osório1, Agostinho Antunes1, María J. Ramos1
1REQUIMTE, Departamento de Química, Faculdade de Ciências, Universidade do Porto, Rua do Campo Alegre, 687, 4169-007 Porto, Portugal

Tóm tắt

Abstract Background Angiogenesis, the formation of new blood vessels, is a primordial process in development and its dysregulation has a central role in the pathogenesis of many diseases. Angiogenin (ANG), a peculiar member of the RNase A superfamily, is a potent inducer of angiogenesis involved in many different types of cancer, amyotrophic lateral sclerosis and also with a possible role in the innate immune defense. The evolutionary path of this family has been a highly dynamic one, where positive selection has played a strong role. In this work we used a combined gene and protein level approach to determine the main sites under diversifying selection on the primate ANG gene and analyze its structural and functional implications. Results We obtained evidence for positive selection in the primate ANG gene. Site specific analysis pointed out 15 sites under positive selection, most of which also exhibited drastic changes in amino acid properties. The mapping of these sites in the ANG 3D-structure described five clusters, four of which were located in functional regions: two in the active site region, one in the nucleolar location signal and one in the cell-binding site. Eight of the 15 sites under selection in the primate ANG gene were highly or moderately conserved in the RNase A family, suggesting a directed event and not a simple consequence of local structural or functional permissiveness. Moreover, 11 sites were exposed to the surface of the protein indicating that they may influence the interactions performed by ANG. Conclusion Using a maximum likelihood gene level analysis we identified 15 sites under positive selection in the primate ANG genes, that were further corroborated through a protein level analysis of radical changes in amino acid properties. These sites mapped onto the main functional regions of the ANG protein. The fact that evidence for positive selection is present in all ANG regions required for angiogenesis may be a good indication that angiogenesis is the process under selection. However, other possibilities to be considered arise from the possible involvement of ANG in innate immunity and the potential influence or co-evolution with its interacting proteins and ligands.

Từ khóa


Tài liệu tham khảo

Carmeliet P: Angiogenesis in life, disease and medicine. Nature. 2005, 438 (7070): 932-936. 10.1038/nature04478.

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 (20): 5480-5486. 10.1021/bi00341a030.

Tello-Montoliu A, Patel JV, Lip GY: Angiogenin: a review of the pathophysiology and potential clinical applications. J Thromb Haemost. 2006, 4 (9): 1864-1874. 10.1111/j.1538-7836.2006.01995.x.

Fett JW, Olson KA, Rybak SM: A monoclonal antibody to human angiogenin. Inhibition of ribonucleolytic and angiogenic activities and localization of the antigenic epitope. Biochemistry. 1994, 33 (18): 5421-5427. 10.1021/bi00184a010.

Olson KA, French TC, Vallee BL, Fett JW: A monoclonal antibody to human angiogenin suppresses tumor growth in athymic mice. Cancer Res. 1994, 54 (17): 4576-4579.

Olson KA, Byers HR, Key ME, Fett JW: Inhibition of prostate carcinoma establishment and metastatic growth in mice by an antiangiogenin monoclonal antibody. Int J Cancer. 2002, 98 (6): 923-929. 10.1002/ijc.10282.

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 U S A. 1998, 95 (8): 4579-4583. 10.1073/pnas.95.8.4579.

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 (11): 3598-3605.

Olson KA, Fett JW, French TC, Key ME, Vallee BL: Angiogenin antagonists prevent tumor growth in vivo. Proc Natl Acad Sci U S A. 1995, 92 (2): 442-446. 10.1073/pnas.92.2.442.

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 U S A. 2002, 99 (15): 10066-10071. 10.1073/pnas.152342999.

Hooper LV, Stappenbeck TS, Hong CV, Gordon JI: Angiogenins: a new class of microbicidal proteins involved in innate immunity. Nat Immunol. 2003, 4 (3): 269-273. 10.1038/ni888.

Bedoya VI, Boasso A, Hardy AW, Rybak S, Shearer GM, Rugeles MT: Ribonucleases in HIV Type 1 Inhibition: Effect of Recombinant RNases on Infection of Primary T Cells and Immune Activation-Induced RNase Gene and Protein Expression. AIDS Res Hum Retroviruses. 2006, 22 (9): 897-907. 10.1089/aid.2006.22.897.

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, Hardiman O: ANG mutations segregate with familial and 'sporadic' amyotrophic lateral sclerosis. Nat Genet. 2006, 38 (4): 411-413. 10.1038/ng1742.

Lambrechts D, Lafuste P, Carmeliet P, Conway EM: Another angiogenic gene linked to amyotrophic lateral sclerosis. Trends Mol Med. 2006, 12 (8): 345-347. 10.1016/j.molmed.2006.06.008.

Kurachi K, Davie EW, Strydom DJ, Riordan JF, Vallee BL: Sequence of the cDNA and gene for angiogenin, a human angiogenesis factor. Biochemistry. 1985, 24 (20): 5494-5499. 10.1021/bi00341a032.

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 (20): 5486-5494. 10.1021/bi00341a031.

Shapiro R, Riordan JF, Vallee BL: Characteristic ribonucleolytic activity of human angiogenin. Biochemistry. 1986, 25 (12): 3527-3532. 10.1021/bi00360a008.

Hallahan TW, Shapiro R, Vallee BL: Dual site model for the organogenic activity of angiogenin. Proc Natl Acad Sci U S A. 1991, 88 (6): 2222-2226. 10.1073/pnas.88.6.2222.

Hallahan TW, Shapiro R, Strydom DJ, Vallee BL: Importance of asparagine-61 and asparagine-109 to the angiogenic activity of human angiogenin. Biochemistry. 1992, 31 (34): 8022-8029. 10.1021/bi00149a036.

Moroianu J, Riordan JF: Identification of the nucleolar targeting signal of human angiogenin. Biochem Biophys Res Commun. 1994, 203 (3): 1765-1772. 10.1006/bbrc.1994.2391.

Harper JW, Vallee BL: A covalent angiogenin/ribonuclease hybrid with a fourth disulfide bond generated by regional mutagenesis. Biochemistry. 1989, 28 (4): 1875-1884. 10.1021/bi00430a067.

Moroianu J, Riordan JF: Nuclear translocation of angiogenin in proliferating endothelial cells is essential to its angiogenic activity. Proc Natl Acad Sci U S A. 1994, 91 (5): 1677-1681. 10.1073/pnas.91.5.1677.

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 (18): 7401-7408. 10.1021/bi00444a038.

Cho S, Beintema JJ, Zhang J: The ribonuclease A superfamily of mammals and birds: identifying new members and tracing evolutionary histories. Genomics. 2005, 85 (2): 208-220. 10.1016/j.ygeno.2004.10.008.

Cho S, Zhang J: Ancient expansion of the ribonuclease A superfamily revealed by genomic analysis of placental and marsupial mammals. Gene. 2006, 373: 116-125. 10.1016/j.gene.2006.01.018.

Rosenberg HF, Dyer KD: Eosinophil cationic protein and eosinophil-derived neurotoxin. Evolution of novel function in a primate ribonuclease gene family. J Biol Chem. 1995, 270 (37): 21539-21544. 10.1074/jbc.270.37.21539.

Zhang J, Dyer KD, Rosenberg HF: Evolution of the rodent eosinophil-associated RNase gene family by rapid gene sorting and positive selection. Proc Natl Acad Sci U S A. 2000, 97 (9): 4701-4706. 10.1073/pnas.080071397.

Singhania NA, Dyer KD, Zhang J, Deming MS, Bonville CA, Domachowske JB, Rosenberg HF: Rapid evolution of the ribonuclease A superfamily: adaptive expansion of independent gene clusters in rats and mice. J Mol Evol. 1999, 49 (6): 721-728. 10.1007/PL00006594.

Zhang J, Rosenberg HF: Diversifying selection of the tumor-growth promoter angiogenin in primate evolution. Mol Biol Evol. 2002, 19 (4): 438-445.

Wildman DE, Uddin M, Liu G, Grossman LI, Goodman M: Implications of natural selection in shaping 99.4% nonsynonymous DNA identity between humans and chimpanzees: enlarging genus Homo. Proc Natl Acad Sci U S A. 2003, 100 (12): 7181-7188. 10.1073/pnas.1232172100.

Zhang J, Zhang YP: Pseudogenization of the tumor-growth promoter angiogenin in a leaf-eating monkey. Gene. 2003, 308: 95-101. 10.1016/S0378-1119(03)00470-0.

Rosenberg NA: The probability of topological concordance of gene trees and species trees. Theor Popul Biol. 2002, 61 (2): 225-247. 10.1006/tpbi.2001.1568.

Yang Z: PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci. 1997, 13 (5): 555-556.

Yang Z, Wong WS, Nielsen R: Bayes empirical bayes inference of amino acid sites under positive selection. Mol Biol Evol. 2005, 22 (4): 1107-1118. 10.1093/molbev/msi097.

Berlin S, Smith NG: Testing for adaptive evolution of the female reproductive protein ZPC in mammals, birds and fishes reveals problems with the M7-M8 likelihood ratio test. BMC Evol Biol. 2005, 5: 65-10.1186/1471-2148-5-65.

Suzuki Y, Nei M: False-positive selection identified by ML-based methods: examples from the Sig1 gene of the diatom Thalassiosira weissflogii and the tax gene of a human T-cell lymphotropic virus. Mol Biol Evol. 2004, 21 (5): 914-921. 10.1093/molbev/msh098.

Woolley S, Johnson J, Smith MJ, Crandall KA, McClellan DA: TreeSAAP: selection on amino acid properties using phylogenetic trees. Bioinformatics. 2003, 19 (5): 671-672. 10.1093/bioinformatics/btg043.

Landau M, Mayrose I, Rosenberg Y, Glaser F, Martz E, Pupko T, Ben-Tal N: ConSurf 2005: the projection of evolutionary conservation scores of residues on protein structures. Nucleic Acids Res. 2005, 33 (Web Server issue): W299-302. 10.1093/nar/gki370.

Guex N, Peitsch MC: SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis. 1997, 18 (15): 2714-2723. 10.1002/elps.1150181505.

Chatani E, Hayashi R: Functional and structural roles of constituent amino acid residues of bovine pancreatic ribonuclease A. J Biosci Bioeng. 2001, 92 (2): 98-107. 10.1263/jbb.92.98.

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 U S A. 1994, 91 (8): 2915-2919. 10.1073/pnas.91.8.2915.

Leonidas DD, Shapiro R, Allen SC, Subbarao GV, Veluraja K, Acharya KR: Refined crystal structures of native human angiogenin and two active site variants: implications for the unique functional properties of an enzyme involved in neovascularisation during tumour growth. J Mol Biol. 1999, 285 (3): 1209-1233. 10.1006/jmbi.1998.2378.

Reiersen H, Rees AR: The hunchback and its neighbours: proline as an environmental modulator. Trends Biochem Sci. 2001, 26 (11): 679-684. 10.1016/S0968-0004(01)01957-0.

Lixin R, Efthymiadis A, Henderson B, Jans DA: Novel properties of the nucleolar targeting signal of human angiogenin. Biochem Biophys Res Commun. 2001, 284 (1): 185-193. 10.1006/bbrc.2001.4953.

Shapiro R, Vallee BL: Identification of functional arginines in human angiogenin by site-directed mutagenesis. Biochemistry. 1992, 31 (49): 12477-12485. 10.1021/bi00164a026.

Hu GF, Chang SI, Riordan JF, Vallee BL: An angiogenin-binding protein from endothelial cells. Proc Natl Acad Sci U S A. 1991, 88 (6): 2227-2231. 10.1073/pnas.88.6.2227.

Hu GF, Strydom DJ, Fett JW, Riordan JF, Vallee BL: Actin is a binding protein for angiogenin. Proc Natl Acad Sci U S A. 1993, 90 (4): 1217-1221. 10.1073/pnas.90.4.1217.

Strydom DJ: The angiogenins. Cell Mol Life Sci. 1998, 54 (8): 811-824. 10.1007/s000180050210.

Hu GF, Riordan JF, Vallee BL: A putative angiogenin receptor in angiogenin-responsive human endothelial cells. Proc Natl Acad Sci U S A. 1997, 94 (6): 2204-2209. 10.1073/pnas.94.6.2204.

Hu H, Gao X, Sun Y, Zhou J, Yang M, Xu Z: Alpha-actinin-2, a cytoskeletal protein, binds to angiogenin. Biochem Biophys Res Commun. 2005, 329 (2): 661-667. 10.1016/j.bbrc.2005.01.158.

Rajashekhar G, Loganath A, Roy AC, Wong YC: Expression and localization of angiogenin in placenta: enhanced levels at term over first trimester villi. Mol Reprod Dev. 2002, 62 (2): 159-166. 10.1002/mrd.10116.

Wildman DE, Chen C, Erez O, Grossman LI, Goodman M, Romero R: Evolution of the mammalian placenta revealed by phylogenetic analysis. Proc Natl Acad Sci U S A. 2006, 103 (9): 3203-3208. 10.1073/pnas.0511344103.

Vogel P: The current molecular phylogeny of Eutherian mammals challenges previous interpretations of placental evolution. Placenta. 2005, 26 (8-9): 591-596. 10.1016/j.placenta.2004.11.005.

Huttley GA, Easteal S, Southey MC, Tesoriero A, Giles GG, McCredie MR, Hopper JL, Venter DJ: Adaptive evolution of the tumour suppressor BRCA1 in humans and chimpanzees. Australian Breast Cancer Family Study. Nat Genet. 2000, 25 (4): 410-413. 10.1038/78092.

Crespi BJ, Summers K: Positive selection in the evolution of cancer. Biol Rev Camb Philos Soc. 2006, 81 (3): 407-424. 10.1017/S1464793106007056. 2006/06/10

Del Bo R, Scarlato M, Ghezzi S, Martinelli-Boneschi F, Corti S, Locatelli F, Santoro D, Prelle A, Briani C, Nardini M, Siciliano G, Mancuso M, Murri L, Bresolin N, Comi GP: Absence of angiogenic genes modification in Italian ALS patients. Neurobiol Aging. 2006

Cronin S, Greenway MJ, Ennis S, Kieran D, Green A, Prehn JH, Hardiman O: Elevated serum angiogenin levels in ALS. Neurology. 2006, 67 (10): 1833-1836. 10.1212/01.wnl.0000244466.46020.47.

Weiner HL, Weiner LH, Swain JL: Tissue distribution and developmental expression of the messenger RNA encoding angiogenin. Science. 1987, 237 (4812): 280-282. 10.1126/science.2440105.

Moenner M, Gusse M, Hatzi E, Badet J: The widespread expression of angiogenin in different human cells suggests a biological function not only related to angiogenesis. European journal of biochemistry / FEBS. 1994, 226 (2): 483-490. 10.1111/j.1432-1033.1994.tb20073.x.

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 (2): 287-292. 10.1016/S0006-291X(02)00479-5.

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 (1): 121-128. 10.1021/bi020465x.

Thompson JD, Higgins DG, Gibson TJ: CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994, 22 (22): 4673-4680. 10.1093/nar/22.22.4673.

Kumar S, Tamura K, Nei M: MEGA3: Integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment. Brief Bioinform. 2004, 5 (2): 150-163. 10.1093/bib/5.2.150.

Saitou N, Nei M: The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987, 4 (4): 406-425.

Felsenstein J: Confidence limits on phylogenies: An approach using the bootstrap. Evolution :. 1985, 39: 783-791. 10.2307/2408678.

Swofford DL: PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4. 2000, Sunderland, Massachusetts , Sinauer Associates

Calendini F, Martin JF: PaupUP v1.0.2032.22590 Beta. A free graphical frontend for Paup* Dos software. 2005, Program distributed by the authors

Ronquist F, Huelsenbeck JP: MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics. 2003, 19 (12): 1572-1574. 10.1093/bioinformatics/btg180.

Posada D, Crandall KA: MODELTEST: testing the model of DNA substitution. Bioinformatics. 1998, 14 (9): 817-818. 10.1093/bioinformatics/14.9.817.

Nylander JAA: MrModeltest v2.2. 2004, Program distributed by the author. Evolutionary Biology Centre, Uppsala University, [http://www.ebc.uu.se/systzoo/staff/nylander.html]

Marques AT, Antunes A, Fernandes PA, Ramos MJ: Comparative evolutionary genomics of the HADH2 gene encoding Abeta-binding alcohol dehydrogenase/17beta-hydroxysteroid dehydrogenase type 10 (ABAD/HSD10). BMC genomics. 2006, 7: 202-10.1186/1471-2164-7-202.

da Fonseca RR, Antunes A, Melo A, Ramos MJ: Structural divergence and adaptive evolution in mammalian cytochromes P450 2C. Gene. 2007, 387 (1-2): 58-66. 10.1016/j.gene.2006.08.017.

Hooft RW, Vriend G, Sander C, Abola EE: Errors in protein structures. Nature. 1996, 381 (6580): 272-10.1038/381272a0.

Marti-Renom MA, Stuart AC, Fiser A, Sanchez R, Melo F, Sali A: Comparative protein structure modeling of genes and genomes. Annu Rev Biophys Biomol Struct. 2000, 29: 291-325. 10.1146/annurev.biophys.29.1.291.

Robert Fraczkiewicz WB: Exact and efficient analytical calculation of the accessible surface areas and their gradients for macromolecules. Journal of Computational Chemistry. 1998, 19 (3): 319-333. 10.1002/(SICI)1096-987X(199802)19:3<319::AID-JCC6>3.0.CO;2-W.

Russo N, Acharya KR, Vallee BL, Shapiro R: A combined kinetic and modeling study of the catalytic center subsites of human angiogenin. Proc Natl Acad Sci U S A. 1996, 93 (2): 804-808. 10.1073/pnas.93.2.804.

Papageorgiou AC, Shapiro R, Acharya KR: Molecular recognition of human angiogenin by placental ribonuclease inhibitor--an X-ray crystallographic study at 2.0 A resolution. Embo J. 1997, 16 (17): 5162-5177. 10.1093/emboj/16.17.5162.

Smith BD, Raines RT: Genetic selection for critical residues in ribonucleases. J Mol Biol. 2006, 362 (3): 459-478. 10.1016/j.jmb.2006.07.020.

Shapiro R, Fox EA, Riordan JF: Role of lysines in human angiogenin: chemical modification and site-directed mutagenesis. Biochemistry. 1989, 28 (4): 1726-1732. 10.1021/bi00430a045.

Thông tin
Thông tin xuất bản

Springer Science and Business Media LLC

Tập 7 Số 1

Thông tin tác giả