Emerging biological functions of ribonuclease 1 and angiogenin

References

• 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(8):2915–2919.
   PubMedGoogle Scholar
• Ackerman SJ, Gleich GJ, Loegering DA, Richardson BA, Butterworth AE. 1985. Comparative toxicity of purified human eosinophil granule cationic proteins for schistosomula of Schistosoma mansoni. Am J Trop Med Hyg. 34(4):735–745.
   PubMedGoogle Scholar
• Altman S. 2011. Ribonuclease P. Philos Trans R Soc Lond B Biol Sci. 366(1580):2936–2941.
   PubMed Web of Science ®Google Scholar
• Aluri KC, Salisbury JP, Prehn JHM, Agar JN. 2020. Loss of angiogenin function is related to earlier ALS onset and a paradoxical increase in ALS duration. Sci Rep. 10(1):3715.
   PubMedGoogle Scholar
• Anfinsen CB. 1973. Principles that govern the folding of protein chains. Science. 181(4096):223–230.
   PubMed Web of Science ®Google Scholar
• Anisimova M, Gascuel O. 2006. Approximate likelihood-ratio test for branches: a fast, accurate, and powerful alternative. Syst Biol. 55(4):539–552.
   PubMed Web of Science ®Google Scholar
• Attery A, Batra JK. 2017. Mouse eosinophil associated ribonucleases: Mechanism of cytotoxic, antibacterial and antiparasitic activities. Int J Biol Macromol. 94(Pt A):445–450.
   PubMedGoogle Scholar
• Avdeeva SV, Chernukha MU, Shaginyan IA, Tarantul VZ, Naroditsky BS. 2006. Human angiogenin lacks specific antimicrobial activity. Curr Microbiol. 53(6):477–478.
   PubMedGoogle Scholar
• Bárcena C, Stefanovic M, Tutusaus A, Martinez-Nieto GA, Martinez L, García-Ruiz C, de Mingo A, Caballeria J, Fernandez-Checa JC, Mari M, et al. 2015. Angiogenin secretion from hepatoma cells activates hepatic stellate cells to amplify a self-sustained cycle promoting liver cancer. Sci Rep. 5:7916.
   PubMedGoogle Scholar
• Barlow GB, Whitear SH, Wilkinson AW. 1979. The excretion of alkaline ribonuclease by children undergoing surgery. Br J Surg. 66(6):412–414.
   PubMedGoogle Scholar
• Barnard EA. 1969. Biological function of pancreatic ribonuclease. Nature. 221(5178):340–344.
   PubMedGoogle Scholar
• Barrabés S, Pagès-Pons L, Radcliffe CM, Tabarés G, Fort E, Royle L, Harvey DJ, Moenner M, Dwek RA, Rudd PM, et al. 2007. Glycosylation of serum ribonuclease 1 indicates a major endothelial origin and reveals an increase in core fucosylation in pancreatic cancer. Glycobiology. 17(4):388–400.
   PubMedGoogle Scholar
• Beintema JJ. 1986. Evolutionary role of posttranslational modifications of proteins, as illustrated by the glycosylation characteristics of the digestive enzyme pancreatic ribonuclease. J Mol Evol. 24(1–2):118–120.
   PubMedGoogle Scholar
• Beintema JJ, Kleineidam RG. 1998. The ribonuclease A superfamily: general discussion. Cell Mol Life Sci. 54(8):825–832.
   PubMedGoogle Scholar
• Beintema JJ, Schuller C, Irie M, Carsana A. 1988. Molecular evolution of the ribonuclease superfamily. Prog Biophys Mol Biol. 51(3):165–192.
   PubMedGoogle Scholar
• Benner SA. 1988. Extracellular ‘communicator RNA. FEBS Lett. 233:255–258.
   PubMedGoogle Scholar
• Benner SA, Allemann RK. 1989. The return of pancreatic ribonucleases. Trends Biochem Sci. 14(10):396–397.
   PubMedGoogle Scholar
• Bernstein E, Kim SY, Carmell MA, Murchison EP, Alcorn H, Li MZ, Mills AA, Elledge SJ, Anderson KV, Hannon GJ. 2003. Dicer is essential for mouse development. Nat Genet. 35(3):215–217.
   PubMed Web of Science ®Google Scholar
• Bicknell R, Vallee BL. 1988. Angiogenin activates endothelial cell phospholipase C. Proc Natl Acad Sci USA. 85(16):5961–5965.
   PubMedGoogle Scholar
• Blackburn P, Moore S. 1982. Pancreatic ribonuclease. Enzymes. 15:317–433.
   Google Scholar
• Boix E, Nogués MV. 2007. Mammalian antimicrobial proteins and peptides: overview on the RNase A superfamily members involved in innate host defence. Mol Biosyst. 3(5):317–335.
   PubMedGoogle Scholar
• Cabrera-Fuentes HA, Niemann B, Grieshaber P, Wollbrueck M, Gehron J, Preissner KT, Boning A. 2015. RNase1 as a potential mediator of remote ischaemic preconditioning for cardioprotectiondagger. Eur J Cardiothorac Surg. 48(5):732–737.
   PubMedGoogle Scholar
• Cabrera-Fuentes HA, Ruiz-Meana M, Simsekyilmaz S, Kostin S, Inserte J, Saffarzadeh M, Galuska SP, Vijayan V, Barba I, Barreto G, et al. 2014. RNase1 prevents the damaging interplay between extracellular RNA and tumour necrosis factor-α in cardiac ischaemia/reperfusion injury. Thromb Haemost. 112(6):1110–1119.
   PubMedGoogle Scholar
• Cafaro V, De Lorenzo C, Piccoli R, Bracale A, Mastronicola MR, Di Donato A, D'Alessio G. 1995. The antitumor action of seminal ribonuclease and its quaternary conformations. FEBS Lett. 359(1):31–34.
   PubMedGoogle Scholar
• Castresana J. 2000. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol. 17(4):540–552.
   PubMed Web of Science ®Google Scholar
• Castro J, Ribó M, Benito A, Vilanova M. 2013. Mini-review: nucleus-targeted ribonucleases as antitumor drugs . Curr Med Chem. 20(10):1225–1231.
   PubMed Web of Science ®Google Scholar
• Castro J, Ribó M, Vilanova M, Benito A. 2021. Strengths and challenges of secretory ribonucleases as antitumor agents. Pharmaceutics. 13(1):82.
   PubMedGoogle Scholar
• Chettri JK, Kuhn JA, Jaafar RM, Kania PW, Møller OS, Buchmann K. 2014. Epidermal response of rainbow trout to Ichthyobodo necator: Immunohistochemical and gene expression studies indicate a Th1-/Th2-like switch. J Fish Dis. 37(9):771–783.
   PubMedGoogle Scholar
• Chevenet F, Brun C, Banuls AL, Jacq B, Christen R. 2006. TreeDyn: towards dynamic graphics and annotations for analyses of trees. BMC Bioinformatics. 7:439.
   PubMed Web of Science ®Google Scholar
• Cho S, Beintema JJ, Zhang J. 2005. The ribonuclease A superfamily of mammals and birds: Identifying new members and tracing evolutionary histories. Genomics. 85(2):208–220.
   PubMed Web of Science ®Google Scholar
• Coombes E, Shakespeare P, Batstone G. 1977. Age and sex related reference values for serum ribonuclease. Clin Chim Acta. 79(1):271–275.
   PubMedGoogle Scholar
• Coombes EJ, Shakespeare PG, Batstone GF. 1978. Observations on serum and urine alkaline ribonuclease activity and urate after burn injury in man. Clin Chim Acta. 86(3):279–290.
   PubMedGoogle Scholar
• Cuchillo CM, Nogués MV, Raines RT. 2011. Bovine pancreatic ribonuclease: fifty years of the first enzymatic reaction mechanism. Biochemistry. 50(37):7835–7841.
   PubMedGoogle Scholar
• Cuchillo CM, Parés X, Guasch A, Barman T, Travers F, Nogués MV. 1993. The role of 2′,3′-cyclic phosphodiesters in the bovine pancreatic ribonuclease A catalysed cleavage of RNA: intermediates or products? FEBS Lett. 333(3):207–210.
   PubMedGoogle Scholar
• D'Alessio G. 1993. New and cryptic biological messages from RNases. Trends Cell Biol. 3:106–109.
   PubMedGoogle Scholar
• D'Alessio G, Di Donato A, Parente A, Piccoli R. 1991. Seminal ribonuclease: a unique member of the ribonuclease superfamily. Trends Biochem Sci. 16(3):104–106.
   PubMedGoogle Scholar
• D'Alessio G, Riordan JF, editors. 1997. Ribonucleases: structures and functions. New York, NY: Academic Press.
   Google Scholar
• Darzynkiewicz Z, Carter SP, Mikulski SM, Ardelt WJ, Shogen K. 1988. Cytostatic and cytotoxic effects of Pannon (P-30 Protein), a novel anticancer agent. Cell Tissue Kinet. 21(3):169–182.
   PubMedGoogle Scholar
• Dickson KA, Haigis MC, Raines RT. 2005. Ribonuclease inhibitor: structure and function. Prog Nucleic Acid Res Mol Biol. 80:349–374.
   PubMed Web of Science ®Google Scholar
• Domachowske JB, Dyer KD, Adams AG, Leto TL, Rosenberg HF. 1998b. Eosinophil cationic protein/RNase 3 is another RNase A-family ribonuclease with direct antiviral activity. Nucleic Acids Res. 26(14):3358–3363.
   PubMed Web of Science ®Google Scholar
• Domachowske JB, Dyer KD, Bonville CA, Rosenberg HF. 1998a. Recombinant human eosinophil-derived neurotoxin/RNase 2 functions as an effective antiviral agent against respiratory syncytial virus. J Infect Dis. 177(6):1458–1464.
   PubMed Web of Science ®Google Scholar
• Doolittle RF. 2009. Step-by-step evolution of vertebrate blood coagulation. Cold Spring Harb Symp Quant Biol. 74:35–40.
   PubMedGoogle Scholar
• Doolittle RF, Surgenor DM. 1962. Blood coagulation in fish. Am J Physiol. 203:964–970.
   PubMedGoogle Scholar
• Dostál J, Matoušek J. 1973. Isolation and some chemical properties of aspermatogenic substance from bull seminal vesicle fluid. J Reprod Fertil. 33(2):263–274.
   PubMedGoogle Scholar
• Dutta S, Bandyopadhyay C, Bottero V, Veettil MV, Wilson L, Pins MR, Johnson KE, Warshall C, Chandran B. 2014. Angiogenin interacts with the plasminogen activation system at the cell surface of breast cancer cells to regulate plasmin formation and cell migration. Mol Oncol. 8(3):483–507.
   PubMed Web of Science ®Google Scholar
• Edgar RC. 2004. MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32(5):1792–1797.
   PubMed Web of Science ®Google Scholar
• Eller CH, Chao TY, Singarapu KK, Ouerfelli O, Yang G, Markley JL, Danishefsky SJ, Raines RT. 2015. Human cancer antigen Globo H Is a cell-surface ligand for human Ribonuclease 1. ACS Cent Sci. 1(4):181–190.
   PubMedGoogle Scholar
• Eller CH, Lomax JE, Raines RT. 2014. Bovine brain ribonuclease is the functional homolog of human ribonuclease 1. J Biol Chem. 289(38):25996–26006.
   PubMedGoogle Scholar
• Eller CH, Raines RT. 2020. Antimicrobial synergy of a ribonuclease and a peptide secreted by human cells. ACS Infect Dis. 6(11):3083–3088.
   PubMedGoogle Scholar
• 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(20):5480–5486.
   PubMedGoogle Scholar
• Findlay D, Herries DG, Mathias AP, Rabin BR, Ross CA. 1961. The active site and mechanism of action of bovine pancreatic ribonuclease. Nature. 190:781–784.
   PubMed Web of Science ®Google Scholar
• Fischer S, Gerriets T, Wessels C, Walberer M, Kostin S, Stolz E, Zheleva K, Hocke A, Hippenstiel S, Preissner KT. 2007. Extracellular RNA mediates endothelial-cell permeability via vascular endothelial growth factor. Blood. 110(7):2457–2465.
   PubMed Web of Science ®Google Scholar
• Fischer S, Gesierich S, Griemert B, Schanzer A, Acker T, Augustin HG, Olsson AK, Preissner KT. 2013. Extracellular RNA liberates tumor necrosis factor-α to promote tumor cell trafficking and progression. Cancer Res. 73(16):5080–5089.
   PubMed Web of Science ®Google Scholar
• Fischer S, Grantzow T, Pagel JI, Tschernatsch M, Sperandio M, Preissner KT, Deindl E. 2012. Extracellular RNA promotes leukocyte recruitment in the vascular system by mobilising proinflammatory cytokines. Thromb Haemost. 108(4):730–741.
   PubMedGoogle Scholar
• Fischer S, Nishio M, Dadkhahi S, Gansler J, Saffarzadeh M, Shibamiyama A, Kral N, Baal N, Koyama T, Deindl E, et al. 2011. Expression and localisation of vascular ribonucleases in endothelial cells. Thromb Haemost. 105(2):345–355.
   PubMedGoogle Scholar
• 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(2):437–442.
   PubMed Web of Science ®Google Scholar
• Futami J, Tsushima Y, Murato Y, Tada H, Sasaki J, Seno M, Yamada H. 1997. Tissue-specific expression of pancreatic-type RNases and RNase inhibitor in humans. DNA Cell Biol. 16(4):413–419.
   PubMedGoogle Scholar
• Gajsiewicz JM, Smith SA, Morrissey JH. 2017. Polyphosphate and RNA differentially modulate the contact pathway of blood clotting. J Biol Chem. 292(5):1808–1814.
   PubMedGoogle Scholar
• Gansler J, Jaax M, Leiting S, Appel B, Greinacher A, Fischer S, Preissner KT. 2012. Structural requirements for the procoagulant activity of nucleic acids. PLoS One. 7(11):e50399.
   PubMedGoogle Scholar
• Garnett ER, Lomax JE, Mohammed BM, Gailani D, Sheehan JP, Raines RT. 2019. Phenotype of ribonuclease 1 deficiency in mice. RNA. 25(8):921–934.
   PubMedGoogle Scholar
• 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(1):33–40.
   PubMedGoogle Scholar
• Goncalves KA, Silberstein L, Li S, Severe N, Hu MG, Yang H, Scadden DT, Hu G-f. 2016. Angiogenin promotes hematopoietic regeneration by dichotomously regulating quiescence of stem and progenitor cells. Cell. 166(4):894–906.
   PubMedGoogle Scholar
• Goo SM, Cho S. 2013. The expansion and functional diversification of the mammalian ribonuclease A superfamily epitomizes the efficiency of multigene families at generating biological novelty. Genome Biol Evol. 5(11):2124–2140.
   PubMedGoogle Scholar
• Gotte G, Mahmoud Helmy A, Ercole C, Spadaccini R, Laurents DV, Donadelli M, Picone D. 2012. Double domain swapping in bovine seminal RNase: formation of distinct N- and C-swapped tetramers and multimers with increasing biological activities. PLoS One. 7(10):e46804.
   PubMedGoogle Scholar
• Green SA, Simoes-Costa M, Bronner ME. 2015. Evolution of vertebrates as viewed from the crest. Nature. 520(7548):474–482.
   PubMedGoogle Scholar
• 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(4):411–413.
   PubMed Web of Science ®Google Scholar
• Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O. 2010. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol. 59(3):307–321.
   PubMed Web of Science ®Google Scholar
• Hallahan TW, Shapiro R, Vallee BL. 1991. Dual site model for the organogenic activity of angiogenin. Proc Natl Acad Sci USA. 88(6):2222–2226.
   PubMedGoogle Scholar
• Han S, Han L, Yao Y, Sun H, Zan X, Liu Q. 2014. Activated hepatic stellate cells promote hepatocellular carcinoma cell migration and invasion via the activation of FAK-MMP9 signaling. Oncol Rep. 31(2):641–648.
   PubMed Web of Science ®Google Scholar
• Harder J, Schroder JM. 2002. RNase 7, a novel innate immune defense antimicrobial protein of healthy human skin. J Biol Chem. 277(48):46779–46784.
   PubMed Web of Science ®Google Scholar
• Hartmann A, Kunz M, Köstlin S, Gillitzer R, Toksoy A, Bröcker E-B, Klein CE. 1999. Hypoxia-induced up-regulation of angiogenin in human malignant melanoma. Cancer Res. 59(7):1578–1583.
   PubMed Web of Science ®Google Scholar
• Hasselmann DO, Rappl G, Tilgen W, Reinhold U. 2001. Extracellular tyrosinase mRNA within apoptotic bodies is protected from degradation in human serum. Clin Chem. 47(8):1488–1489.
   PubMed Web of Science ®Google Scholar
• He T, Qi F, Jia L, Wang S, Wang C, Song N, Fu Y, Li L, Luo Y. 2015. Tumor cell-secreted angiogenin induces angiogenic activity of endothelial cells by suppressing miR-542-3p. Cancer Lett. 368(1):115–125.
   PubMed Web of Science ®Google Scholar
• Hirs C, Moore S, Stein WH. 1960. The sequence of the amino acid residues in performic acid-oxidized ribonuclease. J Biol Chem. 235:633–647.
   PubMedGoogle Scholar
• Hoang TT, Johnson DA, Raines RT, Johnson JA. 2019. Angiogenin activates the astrocytic Nrf2/antioxidant-response element pathway and thereby protects murine neurons from oxidative stress. J Biol Chem. 294(41):15095–15103.
   PubMedGoogle Scholar
• Hoang TT, Raines RT. 2017. Molecular basis for the autonomous promotion of cell proliferation by angiogenin. Nucleic Acids Res. 45(2):818–831.
   PubMedGoogle Scholar
• Hoang TT, Smith TP, Raines RT. 2017. A boronic acid conjugate of angiogenin that shows ROS-responsive neuroprotective activity. Angew Chem Int Ed Engl. 56(10):2619–2622.
   PubMedGoogle Scholar
• Hofsteenge J, Kieffer B, Matthies R, Hemmings BA, Stone SR. 1988. Amino acid sequence of the ribonuclease inhibitor from porcine liver reveals the presence of leucine-rich repeats. Biochemistry. 27(23):8537–8544.
   PubMedGoogle Scholar
• Hooper LV, Stappenbeck TS, Hong CV, Gordon JI. 2003. Angiogenins: a new class of microbicidal proteins involved in innate immunity. Nat Immunol. 4(3):269–273.
   PubMed Web of Science ®Google Scholar
• Hu G-f, Xu C-j, 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(3):452–462.
   PubMedGoogle Scholar
• Huang X, Yuan T, Tschannen M, Sun Z, Jacob H, Du M, Liang M, Dittmar RL, Liu Y, Liang M, et al. 2013. Characterization of human plasma-derived exosomal RNAs by deep sequencing. BMC Genomics. 14:319.
   PubMed Web of Science ®Google Scholar
• Ilinskaya ON, Mahmud RS. 2014. Ribonucleases as antiviral agents. Mol Biol. 48(5):615–623.
   PubMed Web of Science ®Google Scholar
• International Human Genome Sequencing Consortium. 2001. Initial sequencing and analysis of the human genome. Nature. 409:860–921.
   PubMed Web of Science ®Google Scholar
• Irie M, Nitta K, Nonaka T. 1998. Biochemistry of frog ribonucleases. Cell Mol Life Sci. 54(8):775–784.
   PubMedGoogle Scholar
• Isaacs P. 1981. Non-specificity of elevated serum ribonuclease as a pancreatic tumour marker. Digestion. 22(2):101–107.
   PubMedGoogle Scholar
• Ivanov P, Emara MM, Villen J, Gygi SP, Anderson P. 2011. Angiogenin-induced tRNA fragments inhibit translation initiation. Mol Cell. 43(4):613–623.
   PubMed Web of Science ®Google Scholar
• Jiang Y, Doolittle RF. 2003. The evolution of vertebrate blood coagulation as viewed from a comparison of puffer fish and sea squirt genomes. Proc Natl Acad Sci USA. 100(13):7527–7532.
   PubMedGoogle Scholar
• Johnson RJ, McCoy JG, Bingman CA, Phillips GN, Jr., Raines RT. 2007. Inhibition of human pancreatic ribonuclease by the human ribonuclease inhibitor protein. J Mol Biol. 368(2):434–449.
   PubMed Web of Science ®Google Scholar
• Jones W. 1920. The action of boiled pancreas extract on yeast nucleic acid. J Am Physiol. 52(1):203–207.
   Google Scholar
• Kamm RC, Smith AG. 1972. Nucleic acid concentrations in normal human plasma. Clin Chem. 18(6):519–522.
   PubMed Web of Science ®Google Scholar
• Kannemeier C, Shibamiya A, Nakazawa F, Trusheim H, Ruppert C, Markart P, Song Y, Tzima E, Kennerknecht E, Niepmann M, et al. 2007. Extracellular RNA constitutes a natural procoagulant cofactor in blood coagulation. Proc Natl Acad Sci USA. 104(15):6388–6393.
   PubMed Web of Science ®Google Scholar
• Kao RYT, 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(15):10066–10071.
   PubMedGoogle Scholar
• Kartha G, Bello J, Harker D. 1967. Tertiary structure of ribonuclease. Nature. 213(5079):862–865.
   PubMed Web of Science ®Google Scholar
• 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(1):206–222.
   PubMedGoogle Scholar
• Kilgore HR, Latham AP, Ressler VT, Zhang B, Raines RT. 2020. Structure and dynamics of N-glycosylated human ribonuclease 1. Biochemistry. 59(34):3148–3156.
   PubMedGoogle Scholar
• Kim J-S, Souček J, Matoušek J, Raines RT. 1995a. Structural basis for the biological activities of bovine seminal ribonuclease. J Biol Chem. 270(18):10525–10530.
   PubMedGoogle Scholar
• Kim J-S, Souček J, Matoušek J, Raines RT. 1995b. Mechanism of ribonuclease cytotoxicity. J Biol Chem. 270(52):31097–31102.
   PubMedGoogle Scholar
• Kishimoto K, Yoshida S, Ibaragi S, Yoshioka N, Okui T, Hu GF, Sasaki A. 2012. Hypoxia-induced up-regulation of angiogenin, besides VEGF, is related to progression of oral cancer. Oral Oncol. 48(11):1120–1127.
   PubMedGoogle Scholar
• Kleinert E, Langenmayer MC, Reichart B, Kindermann J, Griemert B, Blutke A, Troidl K, Mayr T, Grantzow T, Noyan F, et al. 2016. Ribonuclease (RNase) prolongs survival of grafts in experimental heart transplantation. J Am Heart Assoc. 5:e003429.
   PubMedGoogle Scholar
• Klink TA, Woycechowsky KJ, Taylor KM, Raines RT. 2000. Contribution of disulfide bonds to the conformational stability and catalytic activity of ribonuclease A. Eur J Biochem. 267(2):566–572.
   PubMedGoogle Scholar
• Kobe B, Deisenhofer J. 1993. Crystal structure of porcine ribonuclease inhibitor, a protein with leucine-rich repeats. Nature. 366(6457):751–756.
   PubMed Web of Science ®Google Scholar
• Koga K, Osuga Y, Tsutsumi O, Momoeda M, Suenaga A, Kugu K, Fujiwara T, Takai Y, Yano T, Taketani Y. 2000. Evidence for the presence of angiogenin in human follicular fluid and the up-regulation of its production by human chorionic gonadotropin and hypoxia. J Clin Endocrinol Metab. 85(9):3352–3355.
   PubMed Web of Science ®Google Scholar
• Koga K, Osuga Y, Tsutsumi O, Yano T, Yoshino O, Takai Y, Matsumi H, Hiroi H, Kugu K, Momoeda M, et al. 2001. Demonstration of angiogenin in human endometrium and its enhanced expression in endometrial tissues in the secretory phase and the decidua. J Clin Endocrinol Metab. 86(11):5609–5614.
   PubMedGoogle Scholar
• Krutskikh A, Poliandri A, Cabrera-Sharp V, Dacheux JL, Poutanen M, Huhtaniemi I. 2012. Epididymal protein RNase10 is required for post-testicular sperm maturation and male fertility. . 26(10):4198–4209.
   Google Scholar
• Kutas V, Bertök L, Szabö L. 1969. Effect of endotoxin on the serum ribonuclease activity in rats. J Bacteriol. 100(1):550–551.
   PubMedGoogle Scholar
• Landre JB, Hewett PW, Olivot JM, Friedl P, Ko Y, Sachinidis A, Moenner M. 2002. Human endothelial cells selectively express large amounts of pancreatic-type ribonuclease (RNase 1). J Cell Biochem. 86(3):540–552.
   PubMedGoogle Scholar
• Lee FS, Shapiro R, Vallee BL. 1989. Tight-binding inhibition of angiogenin and ribonuclease A by placental ribonuclease inhibitor. Biochemistry. 28(1):225–230.
   PubMedGoogle Scholar
• Lee FS, Vallee BL. 1993. Structure and action of mammalian ribonuclease (angiogenin) inhibitor. Prog Nucleic Acid Res Mol Biol. 44:1–30.
   PubMedGoogle Scholar
• Lee H-H, Wang Y-N, Hung M-C. 2019. Functional roles of the human ribonuclease A superfamily in RNA metabolism and membrane receptor biology. Mol Aspects Med. 70:106–116.
   PubMedGoogle Scholar
• Lee H-H, Wang Y-N, Yang W-H, Xia W, Wei Y, Chan L-C, Wang Y-H, Jiang Z, Xu S, Yao J, et al. 2021. Human ribonuclease 1 serves as a secretory ligand of ephrin A4 receptor and induces breast tumor initiation. Nat Commun. 12(1):2788.
   PubMedGoogle Scholar
• Lee JE, Raines RT. 2005. Cytotoxicity of bovine seminal ribonuclease: monomer versus dimer. Biochemistry. 44(48):15760–15767.
   PubMedGoogle Scholar
• Lee JE, Raines RT. 2008. Ribonucleases as novel chemotherapeutics: the ranpirnase example. BioDrugs. 22(1):53–58.
   PubMed Web of Science ®Google Scholar
• Lee SH, Kim KW, Min K-M, Kim K-W, Chang S-I, Kim JC. 2014. Angiogenin reduces immune inflammation via inhibition of TANK-binding kinase 1 expression in human corneal fibroblast cells. Mediators Inflamm. 2014:861435.
   PubMedGoogle Scholar
• Lehrer RI, Szklarek D, Barton A, Ganz T, Hamann KJ, Gleich GJ. 1989. Antibacterial properties of eosinophil major basic protein and eosinophil cationic protein. J Immunol. 142(12):4428–4434.
   PubMedGoogle Scholar
• Leland PA, Staniszewski KE, Park C, Kelemen BR, Raines RT. 2002. The ribonucleolytic activity of angiogenin. Biochemistry. 41(4):1343–1350.
   PubMedGoogle Scholar
• Li J, Boix E. 2021. Host defence RNases as antiviral agents against enveloped single stranded RNA viruses. Virulence. 12(1):444–469.
   PubMed Web of Science ®Google Scholar
• Liu S, Yu D, Xu Z, Riordan JF, Hu G. 2001. Angiogenin activates Erk1/2 in human umbilical vein endothelial cells. Biochem Biophys Res Commun. 287(1):305–310.
   PubMedGoogle Scholar
• Lo KW, Lo YM, Leung SF, Tsang YS, Chan LY, Johnson PJ, Hjelm NM, Lee JC, Huang DP. 1999. Analysis of cell-free Epstein–Barr virus associated RNA in the plasma of patients with nasopharyngeal carcinoma. Clin Chem. 45(8 Pt 1):1292–1294.
   PubMedGoogle Scholar
• Lomax JE, Bianchetti CM, Chang A, Phillips GN Jr., Fox BG, Raines RT. 2014. Functional evolution of ribonuclease inhibitor: Insights from birds and reptiles. J Mol Biol. 426(17):3041–3056.
   PubMedGoogle Scholar
• Lomax JE, Eller CH, Raines RT. 2012. Rational design and evaluation of mammalian ribonuclease cytotoxins. Methods Enzymol. 502:273–290.
   PubMedGoogle Scholar
• Lomax JE, Eller CH, Raines RT. 2017. Comparative functional analysis of ribonuclease 1 homologs: molecular insights into evolving vertebrate physiology. Biochem J. 474(13):2219–2233.
   PubMedGoogle Scholar
• Lu L, Li J, Moussaoui M, Boix E. 2018. Immune modulation by human secreted RNases at the extracellular space. Front Immunol. 9:1012.
   PubMed Web of Science ®Google Scholar
• Lyons SM, Fay MM, Akiyama Y, Anderson PJ, Ivanov P. 2017. RNA biology of angiogenin: Current state and perspectives. RNA Biol. 14(2):171–178.
   PubMed Web of Science ®Google Scholar
• Maor D, Klein ME, Kenady DE, Chretien PB, Mardiney MR. 1978. Carcinoma of the lung and cigarette smoking. Effect on serum ribonuclease activity. JAMA. 239(26):2766–2768.
   PubMedGoogle Scholar
• Maor D, Mardiney MR Jr. 1978. Alteration of human serum ribonuclease activity in malignancy. Crit Rev Clin Lab Sci. 10(1):89–111.
   Google Scholar
• Marshall GR, Feng JA, Kuster DJ. 2008. Back to the future: ribonuclease A. Biopolymers. 90(3):259–277.
   PubMedGoogle Scholar
• Matoušek J. 1973. The effect of bovine seminal ribonuclease (AS RNase) on cells of Crocker tumour in mice. Experientia. 29(7):858–859.
   PubMedGoogle Scholar
• Mayer C, Neubert M, Grummt I. 2008. The structure of NoRC-associated RNA is crucial for targeting the chromatin remodelling complex NoRC to the nucleolus. EMBO Rep. 9(8):774–780.
   PubMedGoogle Scholar
• Mayer C, Schmitz KM, Li J, Grummt I, Santoro R. 2006. Intergenic transcripts regulate the epigenetic state of rRNA genes. Mol Cell. 22(3):351–361.
   PubMed Web of Science ®Google Scholar
• Merlino A, Ercole C, Picone D, Pizzo E, Mazzarella L, Sica F. 2008. The buried diversity of bovine seminal ribonuclease: shape and cytotoxicity of the swapped non-covalent form of the enzyme. J Mol Biol. 376(2):427–437.
   PubMedGoogle Scholar
• Merrifield RB. 1986. Solid phase synthesis. Science. 232(4748):341–348.
   PubMedGoogle Scholar
• Mittelbrunn M, Gutiérrez-Vázquez C, Villarroya-Beltri C, González S, Sánchez-Cabo F, González MÁ, Bernad A, Sánchez-Madrid F. 2011. Unidirectional transfer of microRNA-loaded exosomes from T cells to antigen-presenting cells. Nat Commun. 2:282.
   PubMed Web of Science ®Google Scholar
• Mizuta K, Awazu S, Yasuda T, Kishi K. 1990. Purification and characterization of three ribonucleases from human kidney: comparison with urine ribonucleases. Arch Biochem Biophys. 281(1):144–151.
   PubMedGoogle Scholar
• Molina HA, Kierszenbaum F, Hamann KJ, Gleich GJ. 1988. Toxic effects produced or mediated by human eosinophil granule components on Trypanosoma cruzi. Am J Trop Med Hyg. 38(2):327–334.
   PubMedGoogle Scholar
• Moore S, Stein WH. 1973. Chemical structures of pancreatic ribonuclease and deoxyribonuclease. Science. 180(4085):458–464.
   PubMedGoogle Scholar
• Moroianu J, Riordan JF. 1994. Identification of the nucleolar targeting signal of human angiogenin. Biochem Biophys Res Commun. 203(3):1765–1772.
   PubMedGoogle Scholar
• Muñoz-Chápuli R, Carmona R, Guadix JA, Macías D, Pérez-Pomares JM. 2005. The origin of the endothelial cells: an evo-devo approach for the invertebrate/vertebrate transition of the circulatory system. Evol Dev. 7(4):351–358.
   PubMed Web of Science ®Google Scholar
• Murthy BS, Sirdeshmukh R. 1992. Sensitivity of monomeric and dimeric forms of bovine seminal ribonuclease to human placental ribonuclease inhibitor. Biochem J. 281(2):343–348.
   PubMedGoogle Scholar
• Nakazawa F, Kannemeier C, Shibamiya A, Song Y, Tzima E, Schubert U, Koyama T, Niepmann M, Trusheim H, Engelmann B, et al. 2005. Extracellular RNA is a natural cofactor for the (auto-)activation of Factor VII-activating protease (FSAP). Biochem J. 385(Pt 3):831–838.
   PubMedGoogle Scholar
• Nicholson AW, editor. 2011. Ribonucleases. Berlin: Springer.
   Google Scholar
• Noschka R, Gerbl F, Löffler F, Kubis J, Rodríguez AA, Mayer D, Grieshober M, Holch A, Raasholm M, Forssmann W-G, et al. 2020. Unbiased identification of angiogenin as an endogenous antimicrobial protein with activity against virulent Mycobacterium tuberculosis. Front Microbiol. 11:618278.
   PubMedGoogle Scholar
• Olson KA, Verselis SJ, Fett JW. 1998. Angiogenin is regulated in vivo as an acute phase protein. Biochem Biophys Res Commun. 242(3):480–483.
   PubMedGoogle Scholar
• Oribe M. 1984. [Serum ribonuclease in rheumatic disease. I. Serum alkaline ribonuclease activities in rheumatic diseases, especially in malignant rheumatoid arthritis]. Fukuoka Igaku Zasshi. 75(9):524–533.
   PubMedGoogle Scholar
• Park C, Raines RT. 2001. Quantitative analysis of the effect of salt concentration on enzymatic catalysis. J Am Chem Soc. 123(46):11472–11479.
   PubMedGoogle Scholar
• Park J, Kim JT, Lee SJ, Kim JC. 2020. The anti-inflammatory effects of angiogenin in an endotoxin induced uveitis in rats. IJMS. 21(2):413.
   Google Scholar
• Pavlov N, Frendo JL, Guibourdenche J, Degrelle SA, Evain-Brion D, Badet J. 2014. Angiogenin expression during early human placental development; association with blood vessel formation. Biomed Res Int. 2014:781632.
   PubMedGoogle Scholar
• Pavlov N, Hatzi E, Bassaglia Y, Frendo JL, Evain Brion D, Badet J. 2003. Angiogenin distribution in human term placenta, and expression by cultured trophoblastic cells. Angiogenesis. 6(4):317–330.
   PubMedGoogle Scholar
• 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(37):27454–27460.
   PubMedGoogle Scholar
• Pizzo E, Varcamonti M, Di Maro A, D Maro A, Zanfardino A, Giancola C, D'Alessio G. 2008. Ribonucleases with angiogenic and bactericidal activities from the Atlantic salmon. FEBS J. 275(6):1283–1295.
   PubMedGoogle Scholar
• Raines RT. 1998. Ribonuclease A. Chem Rev. 98(3):1045–1065.
   PubMed Web of Science ®Google Scholar
• Raines RT, Toscano MP, Nierengarten DM, Ha JH, Auerbach R. 1995. Replacing a surface loop endows ribonuclease A with angiogenic activity. J Biol Chem. 270(29):17180–17184.
   PubMedGoogle Scholar
• Rajashekhar G, Loganath A, Roy AC, Wong YC. 2002. Expression and localization of angiogenin in placenta: enhanced levels at term over first trimester villi. Mol Reprod Dev. 62(2):159–166.
   PubMedGoogle Scholar
• Ramcharan SK, Lip GY, Stonelake PS, Blann AD. 2013. Angiogenin outperforms VEGF, EPCs and CECs in predicting Dukes’ and AJCC stage in colorectal cancer. Eur J Clin Invest. 43(8):801–808.
   PubMed Web of Science ®Google Scholar
• Reddi KK, Holland JF. 1976. Elevated serum ribonuclease in patients with pancreatic cancer. Proc Natl Acad Sci USA. 73(7):2308–2310.
   PubMedGoogle Scholar
• Reijns MA, Rabe B, Rigby RE, Mill P, Astell KR, Lettice LA, Boyle S, Leitch A, Keighren M, Kilanowski F, et al. 2012. Enzymatic removal of ribonucleotides from DNA is essential for mammalian genome integrity and development. Cell. 149(5):1008–1022.
   PubMed Web of Science ®Google Scholar
• Ressler VT, Raines RT. 2019. Consequences of the endogenous N-glycosylation of human ribonuclease 1. Biochemistry. 58(7):987–996.
   PubMedGoogle Scholar
• Reynolds LP, Grazul-Bilska AT, Redmer DA. 2002. Angiogenesis in the female reproductive organs: pathological implications. Int J Exp Pathol. 83(4):151–163.
   PubMedGoogle Scholar
• Ribó M, Beintema JJ, Osset M, Fernández E, Bravo J, de Llorens R, Cuchillo CM. 1994. Heterogeneity in the glycosylation pattern of human pancreatic ribonuclease. Biol Chem Hoppe Seyler. 375(5):357–363.
   PubMedGoogle Scholar
• Richards FM, Vithayathil PJ. 1959. The preparation of subtilisin-modified ribonuclease and the separation of the peptide and protein components. J Biol Chem. 234(6):1459–1465.
   PubMedGoogle Scholar
• Richards FM, Wyckoff HW. 1971. Bovine pancreatic ribonuclease. Enzymes. 4:647–806.
   Google Scholar
• Rosenberg HF. 2008. RNase A ribonucleases and host defense: an evolving story. J Leukoc Biol. 83(5):1079–1087.
   PubMed Web of Science ®Google Scholar
• Rosenberg HF, Dyer KD, Tiffany HL, Gonzalez M. 1995. Rapid evolution of a unique family of primate ribonuclease genes. Nat Genet. 10(2):219–223.
   PubMedGoogle Scholar
• Ruoppolo M, Vinci F, Klink TA, Raines RT, Marino G. 2000. Contribution of individual disulfide bonds to the oxidative folding of ribonuclease A. Biochemistry. 39(39):12033–12042.
   PubMedGoogle Scholar
• 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(8):2920–2924.
   PubMedGoogle Scholar
• Rutkoski TJ, Raines RT. 2008. Evasion of ribonuclease inhibitor as a determinant of ribonuclease cytotoxicity. Curr Pharm Biotechnol. 9(3):185–189.
   PubMed Web of Science ®Google Scholar
• Saikia M, Jobava R, Parisien M, Putnam A, Krokowski D, Gao X-H, Guan B-J, Yuan Y, Jankowsky E, Feng Z, et al. 2014. Angiogenin-cleaved tRNA halves interact with cytochrome c, protecting cells from apoptosis during osmotic stress. Mol Cell Biol. 34(13):2450–2463.
   PubMed Web of Science ®Google Scholar
• Sajdel-Sulkowska EM, Marotta CA. 1984. Alzheimer's disease brain: alterations in RNA levels and in a ribonuclease-inhibitor complex. Science. 225(4665):947–949.
   PubMed Web of Science ®Google Scholar
• Sarangdhar MA, Allam R. 2021. Angiogenin (ANG)—ribonuclease inhibitor (RNH1) system in protein synthesis and disease. IJMS. 22(3):1287.
   Google Scholar
• Savelyeva AV, Kuligina EV, Bariakin DN, Kozlov VV, Ryabchikova EI, Richter VA, Semenov DV. 2017. Variety of RNAs in peripheral blood cells, plasma, and plasma fractions. Biomed Res Int. 2017:7404912.
   PubMedGoogle Scholar
• Saxena SK, Rybak SM, Davey RT Jr., Youle RJ, Ackerman EJ. 1992. Angiogenin is a cytotoxic, tRNA-specific ribonuclease in the RNase A superfamily. J Biol Chem. 267(30):21982–21986.
   PubMedGoogle Scholar
• Schulenburg C, Weininger U, Neumann P, Meiselbach H, Stubbs MT, Sticht H, Balbach J, Ulbrich-Hofmann R, Arnold U. 2010. Impact of the C-terminal disulfide bond on the folding and stability of onconase. ChemBiChem. 11(7):978–986.
   PubMedGoogle Scholar
• Shapiro R, Riordan JF, Vallee BL. 1986. Characteristic ribonucleolytic activity of human angiogenin. Biochemistry. 25(12):3527–3532.
   PubMedGoogle Scholar
• Shu J, Huang M, Tian Q, Shui Q, Zhou Y, Chen J. 2015. Downregulation of angiogenin inhibits the growth and induces apoptosis in human bladder cancer cells through regulating AKT/mTOR signaling pathway. J Mol Histol. 46(2):157–171.
   PubMedGoogle Scholar
• Sigulem DM, Brasel JA, Velasco EG, Rosso P, Winick M. 1973. Plasma and urine ribonuclease as a measure of nutritional status in children. Am J Clin Nutr. 26(8):793–797.
   PubMedGoogle Scholar
• Simsekyilmaz S, Cabrera-Fuentes HA, Meiler S, Kostin S, Baumer Y, Liehn EA, Weber C, Boisvert WA, Preissner KT, Zernecke A. 2014. Role of extracellular RNA in atherosclerotic plaque formation in mice. Circulation. 129(5):598–606.
   PubMedGoogle Scholar
• Skorupa A, King MA, Aparicio IM, Dussmann H, Coughlan K, Breen B, Kieran D, Concannon CG, Marin P, Prehn JHM. 2012. Motoneurons secrete angiogenin to induce RNA cleavage in astroglia. J Neurosci. 32(15):5024–5038.
   PubMedGoogle Scholar
• Skorupa A, Urbach S, Vigy O, King MA, Chaumont-Dubel S, Prehn JH, Marin P. 2013. Angiogenin induces modifications in the astrocyte secretome: relevance to amyotrophic lateral sclerosis. J Proteomics. 91:274–285.
   PubMed Web of Science ®Google Scholar
• Smith SA, Travers RJ, Morrissey JH. 2015. How it all starts: initiation of the clotting cascade. Crit Rev Biochem Mol Biol. 50(4):326–336.
   PubMed Web of Science ®Google Scholar
• Sorrentino S. 2010. The eight human “canonical” ribonucleases: molecular diversity, catalytic properties, and special biological actions of the enzyme proteins. FEBS Lett. 584(11):2194–2200.
   PubMed Web of Science ®Google Scholar
• Sorrentino S, Libonati M. 1994. Human pancreatic-type and nonpancreatic-type ribonucleases: a direct side-by-side comparison of their catalytic properties. Arch Biochem Biophys. 312(2):340–348.
   PubMedGoogle Scholar
• Spencer JD, Schwaderer AL, Eichler T, Wang H, Kline J, Justice SS, Cohen DM, Hains DS. 2014. An endogenous ribonuclease inhibitor regulates the antimicrobial activity of ribonuclease 7 in the human urinary tract. Kidney Int. 85(5):1179–1191.
   PubMedGoogle Scholar
• Stieger P, Daniel JM, Tholen C, Dutzmann J, Knopp K, Gunduz D, Aslam M, Kampschulte M, Langheinrich A, Fischer S, et al. 2017. Targeting of extracellular RNA reduces edema formation and infarct size and improves survival after myocardial infarction in mice. J Am Heart Assoc. 6:e004541.
   PubMedGoogle Scholar
• Strong LE, Kink JA, Pensinger D, Mei B, Shahan M, Raines RT. 2012a. Efficacy of ribonuclease QBI-139 in combination with standard of care therapties. Cancer Res. 72(Suppl 1):1838.
   Google Scholar
• Strong LE, Kink JA, Mei B, Shahan MN, Raines RT. 2012b. First in human phase I clinical trial of QBI-139, a human ribonuclease variant, in solid tumors. J Clin Oncol. 30(Suppl):TPS3113.
   Google Scholar
• Stroun M, Anker P, Beljanski M, Henri J, Lederrey C, Ojha M, Maurice PA. 1978. Presence of RNA in the nucleoprotein complex spontaneously released by human lymphocytes and frog auricles in culture. Cancer Res. 38(10):3546–3554.
   PubMed Web of Science ®Google Scholar
• Strydom DJ. 1998. The angiogenins. Cell Mol Life Sci. 54(8):811–824.
   PubMedGoogle Scholar
• Su Z, Kuscu C, Malik A, Shibata E, Dutta A. 2019. Angiogenin generates specific stress-induced tRNA halves and is not involved in tRF-3-mediated gene silencing. J Biol Chem. 294(45):16930–16941.
   PubMed Web of Science ®Google Scholar
• Su Z, Wilson B, Kumar P, Dutta A. 2020. Noncanonical roles of tRNAs: tRNA fragments and beyond. Annu Rev Genet. 54:47–69.
   PubMedGoogle Scholar
• Subramanian V, Feng Y. 2007. A new role for angiogenin in neurite growth and pathfinding: Implications for amyotrophic lateral sclerosis. Hum Mol Genet. 16(12):1445–1453.
   PubMedGoogle Scholar
• Sun X, Wiedeman A, Agrawal N, Teal TH, Tanaka L, Hudkins KL, Alpers CE, Bolland S, Buechler MB, Hamerman JA, et al. 2013. Increased ribonuclease expression reduces inflammation and prolongs survival in TLR7 transgenic mice. J Immunol. 190(6):2536–2543.
   PubMed Web of Science ®Google Scholar
• Sznajd J, Magdoń M, Naskalski J, Uracz R, Wojcikiewicz O. 1981. Serum ribonuclease activity in acute myocardial infarction. Cor Vasa. 23(4):241–247.
   PubMedGoogle Scholar
• Thomas SP, Hoang TT, Ressler VT, Raines RT. 2018. Human angiogenin is a potent cytotoxin in the absence of ribonuclease inhibitor. RNA. 24(8):1018–1027.
   PubMedGoogle Scholar
• Thomas SP, Kim E, Kim J-S, Raines RT. 2016. Knockout of the ribonuclease inhibitor gene leaves human cells vulnerable to secretory ribonucleases. Biochemistry. 55(46):6359–6362.
   PubMedGoogle Scholar
• Thompson JE, Venegas FD, Raines RT. 1994. Energetics of catalysis by ribonucleases: fate of the 2′,3′-cyclic phosphodiester intermediate. Biochemistry. 33(23):7408–7414.
   PubMedGoogle Scholar
• Tsuji T, Sun Y, Kishimoto K, Olson KA, Liu S, Hirukawa S, Hu G-f. 2005. Angiogenin is translocated to the nucleus of HeLa cells and is involved in ribosomal RNA transcription and cell proliferation. Cancer Res. 65(4):1352–1360.
   PubMedGoogle Scholar
• Turchinovich A, Weiz L, Langheinz A, Burwinkel B. 2011. Characterization of extracellular circulating microRNA. Nucleic Acids Res. 39(16):7223–7233.
   PubMed Web of Science ®Google Scholar
• Urquidi V, Goodison S, Kim J, Chang M, Dai Y, Rosser CJ. 2012. Vascular endothelial growth factor, carbonic anhydrase 9, and angiogenin as urinary biomarkers for bladder cancer detection. Urology. 79(5):1185.e1–6.
   PubMed Web of Science ®Google Scholar
• Valadi H, Ekstrom K, Bossios A, Sjostrand M, Lee JJ, Lotvall JO. 2007. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol. 9(6):654–659.
   PubMed Web of Science ®Google Scholar
• Venge P, Byström J, Carlson M, Hâkansson L, Karawacjzyk M, Peterson C, Sevéus L, Trulson A. 1999. Eosinophil cationic protein (ECP): molecular and biological properties and the use of ECP as a marker of eosinophil activation in disease. Clin Exp Allergy. 29(9):1172–1186.
   PubMed Web of Science ®Google Scholar
• Vicentini AM, Kieffer B, Matthies R, Meyhack B, Hemmings BA, Stone SR, Hofsteenge J. 1990. Protein chemical and kinetic characterization of recombinant porcine ribonuclease inhibitor expressed in Saccharomyces cerevisiae. Biochemistry. 29(37):8827–8834.
   PubMedGoogle Scholar
• Vickers KC, Palmisano BT, Shoucri BM, Shamburek RD, Remaley AT. 2011. MicroRNAs are transported in plasma and delivered to recipient cells by high-density lipoproteins. Nat Cell Biol. 13(4):423–433.
   PubMed Web of Science ®Google Scholar
• Walberer M, Tschernatsch M, Fischer S, Ritschel N, Volk K, Friedrich C, Bachmann G, Mueller C, Kaps M, Nedelmann M, et al. 2009. RNase therapy assessed by magnetic resonance imaging reduces cerebral edema and infarction size in acute stroke. CNR. 6(1):12–19.
   Google Scholar
• Wang Y, Medvid R, Melton C, Jaenisch R, Blelloch R. 2007. DGCR8 is essential for microRNA biogenesis and silencing of embryonic stem cell self-renewal. Nat Genet. 39(3):380–385.
   PubMed Web of Science ®Google Scholar
• Wang Y-N, Lee H-H, Chou C-K, Yang W-H, Wei Y, Chen C-T, Yao J, Hsu JL, Zhu C, Ying H, et al. 2018b. Angiogenin/ribonuclease 5 is an EGFR ligand and a serum biomarker for erlotinib sensitivity in pancreatic cancer. Cancer Cell. 33(4):752–769.
   PubMedGoogle Scholar
• Wang Y-N, Lee H-H, Hung M-C. 2018a. A novel ligand-receptor relationship between families of ribonucleases and receptor tyrosine kinases. J Biomed Sci. 25(1):83.
   PubMedGoogle Scholar
• Weickmann JL, Olson EM, Glitz DG. 1984. Immunological assay of pancreatic ribonuclease in serum as an indicator of pancreatic cancer. Cancer Res. 44(4):1682–1687.
   PubMedGoogle Scholar
• Westmuckett AD, Nguyen EB, Herlea-Pana OM, Alvau A, Salicioni AM, Moore KL. 2014. Impaired sperm maturation in RNASE9 knockout mice. Biol Reprod. 90(6):120.
   PubMedGoogle Scholar
• Wieczorek AJ, Rhyner C, Block LH. 1985. Isolation and characterization of an RNA-proteolipid complex associated with the malignant state in humans. Proc Natl Acad Sci USA. 82(10):3455–3459.
   PubMedGoogle Scholar
• Windsor IW, Dudley DM, O'Connor DH, Raines RT. 2021. Ribonuclease zymogen induces cytotoxicity upon HIV-1 infection. AIDS Res Ther. 18(1):77.
   PubMedGoogle Scholar
• Windsor IW, Graff CJ, Raines RT. 2019. Circular zymogens of human ribonuclease 1. Protein Sci. 28(9):1713–1719.
   PubMedGoogle Scholar
• Wu Y, Mikulski SM, Ardelt W, Rybak SM, Youle RJ. 1993. A cytotoxic ribonuclease. Study of the mechanism of onconase cytotoxicity. J Biol Chem. 268(14):10686–10693.
   PubMed Web of Science ®Google Scholar
• Xu Z-p, Tsuji T, Riordan JF, Hu G-f. 2002. The nuclear function of angiogenin in endothelial cells is related to rRNA production. Biochem Biophys Res Commun. 294(2):287–292.
   PubMed Web of Science ®Google Scholar
• Yamasaki S, Ivanov P, Hu GF, Anderson P. 2009. Angiogenin cleaves tRNA and promotes stress-induced translational repression. J Cell Biol. 185(1):35–42.
   PubMed Web of Science ®Google Scholar
• Yáñez-Mó M, Siljander PR-M, Andreu Z, Bedina Zavec A, Borràs FE, Buzas EI, Buzas K, Casal E, Cappello F, Carvalho J, et al. 2015. Biological properties of extracellular vesicles and their physiological functions. J Extracell Vesicles. 4:27066.
   PubMed Web of Science ®Google Scholar
• Yasuda T, Nadano D, Takeshita H, Kishi K. 1993. Two distinct secretory ribonucleases from human cerebrum: purification, characterization and relationships to other ribonucleases. Biochem J. 296(3):617–625.
   PubMedGoogle Scholar
• Yoshioka N, Wang L, Kishimoto K, Tsuji T, Hu G-f. 2006. A therapeutic target for prostate cancer based on angiogenin-stimulated angiogenesis and cancer cell proliferation. Proc Natl Acad Sci USA. 103(39):14519–14524.
   PubMedGoogle Scholar
• Yu W, Goncalves KA, Li S, Kishikawa H, Sun G, Yang H, Vanli N, Wu Y, Jiang Y, Hu MG, et al. 2017. Plexin-B2 mediates physiologic and pathologic functions of angiogenin. Cell. 171(4):849–864.
   PubMedGoogle Scholar
• Yuan T, Huang X, Woodcock M, Du M, Dittmar R, Wang Y, Tsai S, Kohli M, Boardman L, Patel T, et al. 2016. Plasma extracellular RNA profiles in healthy and cancer patients. Sci Rep. 6(1):19413.
   PubMedGoogle Scholar
• Yue T, Zhan X, Zhang D, Jain R, Wang K-W, Choi JH, Misawa T, Su L, Quan J, Hildebrand S, Xu D, et al. 2021. SLFN2 protection of tRNAs from stress-induced cleavage is essential for T cell–mediated immunity. Science. 372(6543):eaba4220.
   PubMedGoogle Scholar
• Zendzian EN, Barnard EA. 1967. Distributions of pancreatic ribonuclease, chymotrypsin, and trypsin in vertebrates. Arch Biochem Biophys. 122(3):699–713.
   PubMedGoogle Scholar
• Zhang J, Dyer KD, Rosenberg HF. 2002. RNase 8, a novel RNase A superfamily ribonuclease expressed uniquely in placenta. Nucleic Acids Res. 30(5):1169–1175.
   PubMedGoogle Scholar
• Zhang Y, Xia X, Yan J, Yan L, Lu C, Zhu X, Wang T, Yin T, Li R, Chang HM, et al. 2017. Mesenchymal stem cell-derived angiogenin promotes primodial follicle survival and angiogenesis in transplanted human ovarian tissue. Reprod Biol Endocrinol. 15(1):18.
   PubMedGoogle Scholar
• Zhao W, Beintema JJ, Hofsteenge J. 1994. The amino acid sequence of iguana (Iguana iguana) pancreatic ribonuclease. Eur J Biochem. 219(1–2):641–646.
   PubMedGoogle Scholar
• Zhou H-M, Strydom DJ. 1993. The amino acid sequence of human ribonuclease 4, a highly conserved ribonuclease that cleaves specifically on the 3′ side of uridine. Eur J Biochem. 217(1):401–410.
   PubMedGoogle Scholar