Skip to main content

The Superfamily of Vertebrate-Secreted Ribonucleases

  • Chapter
  • First Online:
Book cover Ribonucleases

Part of the book series: Nucleic Acids and Molecular Biology ((NUCLEIC))

  • 1229 Accesses

Abstract

Recent investigations on vertebrate proteomes have revealed the presence of a single vertebrate-specific enzyme group: that of the RNases homologous to RNase A, the historical RNase archetype studied for more than a century. The genes encoding these RNases are all phylogenetically linked, and the gene products are all secreted proteins, thus forming an impressively large superfamily of vertebrate-secreted RNases, formerly called “RNase A superfamily.” The vertebrate-secreted RNases display surprisingly different physiological functions, other than that of ribonucleolytic enzymes, including angiogenesis, host defense, immunosuppression, biogenesis of ribosomes, and stress response. Some of the RNases have antitumor activity, as they are capable of selectively killing malignant cells, and have inspired an intensely pursued research line of translational value. A particular attention has been given in this chapter to the family of mammalian RNases, especially to RNase 5 (angiogenin) and microbicidal RNases 2 and 3, to the RNase inhibitor, and the recently investigated family of fish RNases.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Abtin A, Eckhart L, Mildner M, Ghannadan M, Harder J, Schroder JM, Tschachler E (2009) Degradation by stratum corneum proteases prevents endogenous RNase inhibitor from blocking antimicrobial activities of RNase 5 and RNase 7. J Investig Dermatol 129(9):2193–2201

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Antignani A, Naddeo M, Cubellis MV, Russo A, D’Alessio G (2001) Antitumor action of seminal ribonuclease, its dimeric structure, and its resistance to the cytosolic ribonuclease inhibitor. Biochemistry 40(12):3492–3496

    PubMed  CAS  Google Scholar 

  • Ardelt W, Shogen K, Darzynkiewicz Z (2008) Onconase and amphinase, the antitumor ribonucleases from rana pipiens oocytes. Curr Pharm Biotechnol 9(3):215–225

    PubMed  CAS  Google Scholar 

  • Arnold U, Ulbrich-Hofmann R (2006) Natural and engineered ribonucleases as potential cancer therapeutics. Biotechnol Lett 28(20):1615–1622

    PubMed  CAS  Google Scholar 

  • Bartholeyns J, Baudhuin P (1976) Inhibition of tumor cell proliferation by dimerized ribonuclease. Proc Natl Acad Sci USA 73(2):573–576

    PubMed  CAS  Google Scholar 

  • Beintema JJ, Gruber M (1965) La structure et l’activité de la ribonucléase pancréatique du rat. Bull Soc Chim Biol 47(12):2307–2310

    CAS  Google Scholar 

  • Beintema JJ, Wietzes P, Weickmann JL, Glitz DG (1984) The amino acid sequence of human pancreatic ribonuclease. Anal Biochem 136(1):48–64

    PubMed  CAS  Google Scholar 

  • Beintema JJ, Hofsteenge J, Iwama M, Morita T, Ohgi K, Irie M, Sugiyama RH, Schieven GL, Dekker CA, Glitz DG (1988) Amino acid sequence of the nonsecretory ribonuclease of human urine. Biochemistry 27(12):4530–4538

    PubMed  CAS  Google Scholar 

  • Beintema JJ, Breukelman HJ, Carsana A, Furia A (1997) Evolution of vertebrate ribonucleases: ribonuclease a superfamily. In: D’Alessio G, Riordan JF (eds) Ribonucleases: structures and functions. Academic Press, San Diego, pp 245–269

    Google Scholar 

  • Bennett MJ, Choe S, Eisenberg D (1994) Domain swapping: entangling alliances between proteins. Proc Natl Acad Sci USA 91(8):3127–3131

    PubMed  CAS  Google Scholar 

  • Bennett MJ, Schlunegger MP, Eisenberg D (1995) 3d domain swapping: a mechanism for oligomer assembly. Protein Sci 4(12):2455–2468

    PubMed  CAS  Google Scholar 

  • Berisio R, Lamzin VS, Sica F, Wilson KS, Zagari A, Mazzarella L (1999) Protein titration in the crystal state. J Mol Biol 292(4):845–854

    PubMed  CAS  Google Scholar 

  • Berisio R, Sica F, Lamzin VS, Wilson KS, Zagari A, Mazzarella L (2002) Atomic resolution structures of ribonuclease A at six pH values. Acta Crystallogr D Biol Crystallogr 58(Pt 3):441–450

    PubMed  CAS  Google Scholar 

  • Berisio R, Sica F, De Lorenzo C, Di Fiore A, Piccoli R, Zagari A, Mazzarella L (2003) Crystal structure of the dimeric unswapped form of bovine seminal ribonuclease. FEBS Lett 554(1–2):105–110

    PubMed  CAS  Google Scholar 

  • Blackburn P, Moore S (1982) Pancreatic ribonuclease. In: Boyer PD (ed) The enzymes, vol 15. Academic Press, New York, pp 317–433

    Google Scholar 

  • Blazquez M, Fominaya JM, Hofsteenge J (1996) Oxidation of sulfhydryl groups of ribonuclease inhibitor in epithelial cells is sufficient for its intracellular degradation. J Biol Chem 271(31):18638–18642

    PubMed  CAS  Google Scholar 

  • Boehm T, Folkman J, Browder T, O’Reilly MS (1997) Antiangiogenic therapy of experimental cancer does not induce acquired drug resistance. Nature 390(6658):404–407

    PubMed  CAS  Google Scholar 

  • Boix E, Nogues 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

    PubMed  CAS  Google Scholar 

  • Bond MD, Vallee BL (1990) Isolation and sequencing of mouse angiogenin DNA. Biochem Biophys Res Commun 171(3):988–995

    PubMed  CAS  Google Scholar 

  • Breukelman HJ, Beintema JJ, Confalone E, Costanzo C, Sasso MP, Carsana A, Palmieri M, Furia A (1993) Sequences related to the ox pancreatic ribonuclease coding region in the genomic DNA of mammalian species. J Mol Evol 37(1):29–35

    PubMed  CAS  Google Scholar 

  • Brown WE, Nobile V, Subramanian V, Shapiro R (1995) The mouse angiogenin gene family: structures of an angiogenin-related protein gene and two pseudogenes. Genomics 29(1):200–206

    PubMed  CAS  Google 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

    PubMed  CAS  Google Scholar 

  • Capasso S, Giordano F, Mattia CA, Mazzarella L, Zagari A (1983) Refinement of the structure of bovine seminal ribonuclease. Biopolymers 22(1):327–332

    PubMed  CAS  Google Scholar 

  • Carreras E, Boix E, Rosenberg HF, Cuchillo CM, Nogues MV (2003) Both aromatic and cationic residues contribute to the membrane-lytic and bactericidal activity of eosinophil cationic protein. Biochemistry 42(22):6636–6644

    PubMed  CAS  Google Scholar 

  • Castella S, Fouchecourt S, Teixeira-Gomes AP, Vinh J, Belghazi M, Dacheux F, Dacheux JL (2004) Identification of a member of a new RNase a family specifically secreted by epididymal caput epithelium. Biol Reprod 70(2):319–328

    PubMed  CAS  Google Scholar 

  • Chang CF, Chen C, Chen YC, Hom K, Huang RF, Huang TH (1998) The solution structure of a cytotoxic ribonuclease from the oocytes of Rana catesbeiana (bullfrog). J Mol Biol 283(1):231–244

    PubMed  CAS  Google Scholar 

  • Chen S, Le SY, Newton DL, Maizel JV Jr, Rybak SM (2000) A gender-specific mRNA encoding a cytotoxic ribonuclease contains a 3′ UTR of unusual length and structure. Nucleic Acids Res 28(12):2375–2382

    PubMed  CAS  Google Scholar 

  • Cho S, Zhang J (2007) Zebrafish ribonucleases are bactericidal: implications for the origin of the vertebrate RNase a superfamily. Mol Biol Evol 24(5):1259–1268

    PubMed  CAS  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  CAS  Google Scholar 

  • 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(42):11810–11818

    PubMed  CAS  Google Scholar 

  • Crestfield AM, Fruchter RG (1967) The homologous and hybrid dimers of ribonuclease A and its carboxymethylhistidine derivatives. J Biol Chem 242(14):3279–3284

    PubMed  CAS  Google Scholar 

  • Crestfield AM, Stein WH, Moore S (1962) On the aggregation of bovine pancreatic ribonuclease. Arch Biochem Biophys 1(Suppl):217–222

    PubMed  CAS  Google Scholar 

  • Cuchillo CM, Vilanova M, Nogués MV (1997) Pancreatic ribonuclease. In: D’Alessio G, Riordan JF (eds) Ribonucleases. Academic Press, San Diego, pp 271–304

    Google Scholar 

  • Cui XY, Fu PF, Pan DN, Zhao Y, Zhao J, Zhao BC (2003) The antioxidant effects of ribonuclease inhibitor. Free Radic Res 37(10):1079–1085

    PubMed  CAS  Google Scholar 

  • D’Alessio G (1963) The action of seminal enzymes on ribonucleic acid. Biochem J 89(1):7

    Google Scholar 

  • D’Alessio G (1993) New and cryptic biological messages from ribonucleases. Trends Cell Biol 3:106–109

    PubMed  Google Scholar 

  • D’Alessio G (1995) Oligomer evolution in action? [letter]. Nat Struct Biol 2(1):11–13

    PubMed  Google Scholar 

  • D’Alessio G (1999) Evolution of oligomeric proteins. The unusual case of a dimeric ribonuclease. Eur J Biochem 266:1–11

    Google Scholar 

  • D’Alessio G, Riordan JF (eds) (1997) Ribonucleases: structures and functions. Academic Press, New York

    Google Scholar 

  • D’Alessio G, Di Donato A, Parente A, Piccoli R (1991) Seminal RNase: a unique member of the ribonuclease superfamily. Trends Biochem Sci 16:104–106

    PubMed  Google Scholar 

  • D’Alessio G, Di Donato A, Mazzarella L, Piccoli R (1997) Seminal ribonuclease: the importance of diversity. In: D’Alessio G, Riordan G (eds) Ribonucleases: structures and functions. Academic Press, New York, pp 383–423

    Google Scholar 

  • Di Donato A, D’Alessio G (1973) Interchain disulfide bridges in ribonuclease BS-1. Biochem Biophys Res Commun 55(3):919–928

    PubMed  Google Scholar 

  • Di Donato A, Cafaro V, D’Alessio G (1994) Ribonuclease A can be transformed into a dimeric ribonuclease with antitumor activity. J Biol Chem 269(26):17394–17396

    PubMed  Google Scholar 

  • Domachowske JB, Dyer KD, Bonville CA, Rosenberg HF (1998) 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  CAS  Google Scholar 

  • Dubos R, Thompson R (1938) The decomposition of yeast nucleic acid by a heat-resistant enzyme. J Biol Chem 124:501–510

    Google Scholar 

  • During K, Porsch P, Mahn A, Brinkmann O, Gieffers W (1999) The non-enzymatic microbicidal activity of lysozymes. FEBS Lett 449(2–3):93–100

    PubMed  CAS  Google Scholar 

  • Dyer KD, Rosenberg HF, Zhang J (2004) Isolation, characterization, and evolutionary divergence of mouse RNase 6: evidence for unusual evolution in rodents. J Mol Evol 59(5):657–665

    PubMed  CAS  Google Scholar 

  • Emara MM, Ivanov P, Hickman T, Dawra N, Tisdale S, Kedersha N, Hu GF, Anderson P (2010) Angiogenin-induced tiRNAs promote stress-induced stress granule assembly. J Biol Chem 285:10959–10968

    PubMed  CAS  Google Scholar 

  • Ercole C, Spadaccini R, Alfano C, Tancredi T, Picone D (2007) A new mutant of bovine seminal ribonuclease with a reversed swapping propensity. Biochemistry 46(8):2227–2232

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Fruton JS, Simonds S (1958) General biochemistry. Wiley, New York

    Google 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  CAS  Google Scholar 

  • Futami J, Maeda T, Kitazoe M, Nukui E, Tada H, Seno M, Kosaka M, Yamada H (2001) Preparation of potent cytotoxic ribonucleases by cationization: enhanced cellular uptake and decreased interaction with ribonuclease inhibitor by chemical modification of carboxyl groups. Biochemistry 40(25):7518–7524

    PubMed  CAS  Google Scholar 

  • Gao X, Xu Z (2008) Mechanisms of action of angiogenin. Acta Biochim Biophys Sin 40(7):619–624

    PubMed  CAS  Google Scholar 

  • Garcia-Mayoral MF, Moussaoui M, de la Torre BG, Andreu D, Boix E, Nogues MV, Rico M, Laurents DV, Bruix M (2010) NMR structural determinants of eosinophil cationic protein binding to membrane and heparin mimetics. Biophys J 98(11):2702–2711

    PubMed  CAS  Google Scholar 

  • Gotte G, Libonati M (2004) Oligomerization of ribonuclease A: two novel three-dimensional domain-swapped tetramers. J Biol Chem 279(35):36670–36679

    PubMed  CAS  Google Scholar 

  • Gotte G, Bertoldi M, Libonati M (1999) Structural versatility of bovine ribonuclease A. Distinct conformers of trimeric and tetrameric aggregates of the enzyme. Eur J Biochem 265:680–687

    PubMed  CAS  Google Scholar 

  • 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(4):411–413

    PubMed  CAS  Google Scholar 

  • Griebenow K, Klibanov AM (1995) Lyophilization-induced reversible changes in the secondary structure of proteins. Proc Natl Acad Sci USA 92(24):10969–10976

    PubMed  CAS  Google Scholar 

  • Gupta V, Muyldermans S, Wyns L, Salunke DM (1999) The crystal structure of recombinant rat pancreatic RNase A. Proteins 35(1):1–12

    PubMed  CAS  Google Scholar 

  • Haigis MC, Kurten EL, Raines RT (2003) Ribonuclease inhibitor as an intracellular sentry. Nucleic Acids Res 31(3):1024–1032

    PubMed  CAS  Google Scholar 

  • Hamann KJ, Ten RM, Loegering DA, Jenkins RB, Heise MT, Schad CR, Pease LR, Gleich GJ, Barker RL (1990) Structure and chromosome localization of the human eosinophil-derived neurotoxin and eosinophil cationic protein genes: evidence for intronless coding sequences in the ribonuclease gene superfamily. Genomics 7(4):535–546

    PubMed  CAS  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  CAS  Google Scholar 

  • Hayano K, Iwama M, Sakamoto H, Watanabe H, Sanda A, Ohgi K, Irie M (1993) Characterization of poly C preferential ribonuclease from chicken liver. J Biochem 114(1):156–162

    PubMed  CAS  Google Scholar 

  • Hirukawa S, Olson KA, Tsuji T, Hu GF (2005) Neamine inhibits xenografic human tumor growth and angiogenesis in athymic mice. Clin Cancer Res 11(24 Pt 1):8745–8752

    PubMed  CAS  Google Scholar 

  • Hofsteenge J, Moldow C, Vicentini AM, Zelenko O, Jarai-Kote Z, Neumann U (1998) A single amino acid substitution changes ribonuclease 4 from a uridine-specific to a cytidine-specific enzyme. Biochemistry 37(26):9250–9257

    PubMed  CAS  Google Scholar 

  • Holloway DE, Chavali GB, Hares MC, Subramanian V, Acharya KR (2005) Structure of murine angiogenin: features of the substrate- and cell-binding regions and prospects for inhibitor-binding studies. Acta Crystallogr D Biol Crystallogr 61(Pt 12):1568–1578

    PubMed  Google 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  CAS  Google Scholar 

  • Hosokawa S, Irie M (1971) Purification and properties of seminal vesicle ribonucleases. J Biochem 69(4):683–697

    PubMed  CAS  Google Scholar 

  • Hu GF (1998) Neomycin inhibits angiogenin-induced angiogenesis. Proc Natl Acad Sci USA 95(17):9791–9795

    PubMed  CAS  Google Scholar 

  • Hu GF, Chang SI, Riordan JF, Vallee BL (1991) An angiogenin-binding protein from endothelial cells. Proc Natl Acad Sci USA 88(6):2227–2231

    PubMed  CAS  Google Scholar 

  • Hu GF, Strydom DJ, Fett JW, Riordan JF, Vallee BL (1993) Actin is a binding protein for angiogenin. Proc Natl Acad Sci USA 90(4):1217–1221

    PubMed  CAS  Google Scholar 

  • 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(3):452–462

    PubMed  CAS  Google Scholar 

  • Huang HC, Wang SC, Leu YJ, Lu SC, Liao YD (1998) The Rana catesbeiana rcr gene encoding a cytotoxic ribonuclease. Tissue distribution, cloning, purification, cytotoxicity, and active residues for RNase activity. J Biol Chem 273(11):6395–6401

    PubMed  CAS  Google Scholar 

  • 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(7):4626–4633

    PubMed  CAS  Google Scholar 

  • Ibrahim HR, Matsuzaki T, Aoki T (2001) Genetic evidence that antibacterial activity of lysozyme is independent of its catalytic function. FEBS Lett 506(1):27–32

    PubMed  CAS  Google Scholar 

  • Irie M, Nitta K, Nonaka T (1998) Biochemistry of frog ribonucleases. Cell Mol Life Sci 54(8):775–784

    PubMed  CAS  Google Scholar 

  • Jones W (1920) The action of boiled pancreas extract on yeast nucleic acid. Am J Physiol 52:203–207

    CAS  Google Scholar 

  • Kamiya Y, Oyama F, Oyama R, Sakakibara F, Nitta K, Kawauchi H, Takayanagi Y, Titani K (1990) Amino acid sequence of a lectin from japanese frog (Rana japonica) eggs. J Biochem 108(1):139–143

    PubMed  CAS  Google Scholar 

  • Katekaew S, Torikata T, Araki T (2006) The complete amino acid sequence of green turtle (Chelonia mydas) egg white ribonuclease. Protein J 25(5):316–327

    PubMed  CAS  Google Scholar 

  • Katekaew S, Torikata T, Hirakawa H, Kuhara S, Araki T (2007) Enzymatic properties of newly found green turtle egg white ribonuclease. Protein J 26(2):75–85

    PubMed  CAS  Google Scholar 

  • Katekaew S, Kuaprasert B, Torikata T, Kakuta Y, Kimura M, Yoneda K, Araki T (2010) Structure of the newly found green turtle egg-white ribonuclease. Acta Crystallogr 66(Pt 7):755–759

    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

    PubMed  CAS  Google Scholar 

  • 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(3):445–456

    PubMed  CAS  Google Scholar 

  • Kleinedam RG, Jekel PA, Beintema JJ, Situmorang P (1999) Seminal-type ribonuclease genes in ruminants. Sequence conservation without protein expression? Gene 231(1–2):147–153

    Google Scholar 

  • Klenova EM, Botezato I, Laudet V, Goodwin GH, Wallace JC, Lobanenkov VV (1992) Isolation of a cDNA clone encoding the RNase-superfamily-related gene highly expressed in chicken bone marrow cells. Biochem Biophys Res Commun 185(1):231–239

    PubMed  CAS  Google Scholar 

  • Kornguth SE, Stahmann MA, Anderson JW (1961) Effect of polylysine on the cytology of Ehrlich ascites tumor cells. Exp Cell Res 24:484–494

    PubMed  CAS  Google Scholar 

  • Kunitz M (1940) Crystalline ribonuclease. J Gen Physiol 24:15–32

    PubMed  CAS  Google Scholar 

  • Lander ES, Linton LM, Birren B, Nusbaum C et al (2001) Initial sequencing and analysis of the human genome. Nature 409(6822):860–921

    PubMed  CAS  Google 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

    PubMed  CAS  Google Scholar 

  • Ledoux L (1955) Action of ribonuclease on two solid tumours in vivo. Nature 176(4470):36–37

    PubMed  CAS  Google Scholar 

  • Lee JE, Raines RT (2005) Cytotoxicity of bovine seminal ribonuclease: monomer versus dimer. Biochemistry 44(48):15760–15767

    PubMed  CAS  Google Scholar 

  • Lee JE, Raines RT (2008) Ribonucleases as novel chemotherapeutics: the ranpirnase example. BioDrugs 22(1):53–58

    PubMed  CAS  Google 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

    PubMed  CAS  Google Scholar 

  • Leich F, Koditz J, Ulbrich-Hofman R, Arnold U (2006) Tandemization endows bovine pancreatic ribonuclease with cytotoxic activity. J Mol Biol 358(5):1305–1313

    PubMed  CAS  Google Scholar 

  • Leich F, Stohr N, Rietz A, Ulbrich-Hofmann R, Arnold U (2007) Endocytotic internalization as a crucial factor for the cytotoxicity of ribonucleases. J Biol Chem 282(38):27640–27646

    PubMed  CAS  Google Scholar 

  • Leland PA, Schultz LW, Kim BM, Raines RT (1998) Ribonuclease A variants with potent cytotoxic activity. Proc Natl Acad Sci USA 95(18):10407–10412

    PubMed  CAS  Google Scholar 

  • Leland PA, Staniszewski KE, Park C, Kelemen BR, Raines RT (2002) The ribonucleolytic activity of angiogenin. Biochemistry 41(4):1343–1350

    PubMed  CAS  Google Scholar 

  • Leu YJ, Chern SS, Wang SC, Hsiao YY, Amiraslanov I, Liaw YC, Liao YD (2003) Residues involved in the catalysis, base specificity, and cytotoxicity of ribonuclease from Rana catesbeiana based upon mutagenesis and x-ray crystallography. J Biol Chem 278(9):7300–7309

    PubMed  CAS  Google Scholar 

  • Levy CC, Karpetsky TP (1980) The purification and properties of chicken liver RNase: an enzyme which is useful in distinguishing between cytidylic and uridylic acid residues. J Biol Chem 255(5):2153–2159

    PubMed  CAS  Google Scholar 

  • Liao YD, Huang HC, Leu YJ, Wei CW, Tang PC, Wang SC (2000) Purification and cloning of cytotoxic ribonucleases from Rana catesbeiana (bullfrog). Nucleic Acids Res 28(21):4097–4104

    PubMed  CAS  Google Scholar 

  • Libonati M, Sorrentino S (2001) Degradation of double-stranded RNA by mammalian pancreatic-type ribonucleases. Meth Enzymol 341:234–248

    PubMed  CAS  Google Scholar 

  • Lin YM, Wu SJ, Chang TW, Wang CF, Suen CS, Hwang MJ, Chang MD, Chen YT, Liao YD (2010) Outer membrane protein I of Pseudomonas aeruginosa is a target of cationic antimicrobial peptide/protein. J Biol Chem 285(12):8985–8994

    PubMed  CAS  Google Scholar 

  • Liu Y, Hart PJ, Schlunegger MP, Eisenberg D (1998) The crystal structure of a 3D domain-swapped dimer of RNase A at 2.1 Å resolution. Proc Natl Acad Sci USA 95:3437–3442

    PubMed  CAS  Google Scholar 

  • Liu Y, Gotte G, Libonati M, Eisenberg D (2001) A domain-swapped RNase A dimer with implications for amyloid formation. Nat Struct Biol 8:211–214

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Lopez-Alonso JP, Bruix M, Font J, Ribo M, Vilanova M, Jimenez MA, Santoro J, Gonzalez C, Laurents DV (2010) NMR spectroscopy reveals that RNase A is chiefly denatured in 40% acetic acid: implications for oligomer formation by 3d domain swapping. J Am Chem Soc 132(5):1621–1630

    PubMed  CAS  Google Scholar 

  • Mastronicola MR, Piccoli R, D’Alessio G (1995) Key extracellular and intracellular steps in the antitumor action of seminal ribonuclease. Eur J Biochem 230(1):242–249

    PubMed  CAS  Google Scholar 

  • Matousek J, Gotte G, Pouckova P, Soucek J, Slavik T, Vottariello F, Libonati M (2003) Antitumor activity and other biological actions of oligomers of ribonuclease A. J Biol Chem 278(26):23817–23822

    PubMed  CAS  Google Scholar 

  • Mazzarella L, Capasso S, Demasi D, Di Lorenzo G, Mattia CA, Zagari A (1993) Bovine seminal ribonuclease. Structure at 1.9 Å resolution. Acta Crystallogr D49:389–402

    CAS  Google Scholar 

  • Mazzarella L, Vitagliano L, Zagari A (1995) Swapping structural determinants of ribonucleases: an energetic analysis of the hinge peptide 16–22. Proc Natl Acad Sci USA 92:3799–3803

    PubMed  CAS  Google Scholar 

  • Merlino A, Vitagliano L, Ceruso MA, Di Nola A, Mazzarella L (2002) Global and local motions in ribonuclease A: a molecular dynamics study. Biopolymers 65(4):274–283

    PubMed  CAS  Google Scholar 

  • Merlino A, Vitagliano L, Ceruso MA, Mazzarella L (2003) Subtle functional collective motions in pancreatic-like ribonucleases: from ribonuclease A to angiogenin. Proteins 53(1):101–110

    PubMed  CAS  Google Scholar 

  • Merlino A, Mazzarella L, Carannante A, Di Fiore A, Di Donato A, Notomista E, Sica F (2005) The importance of dynamic effects on the enzyme activity: x-ray structure and molecular dynamics of onconase mutants. J Biol Chem 280(18):17953–17960

    PubMed  CAS  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

    PubMed  CAS  Google Scholar 

  • Mikulski SM, Costanzi JJ, Vogelzang NJ, McCachren S, Taub RN, Chun H, Mittelman A, Panella T, Puccio C, Fine R, Shogen K (2002) Phase II trial of a single weekly intravenous dose of ranpirnase in patients with unresectable malignant mesothelioma. J Clin Oncol 20:274–281

    PubMed  CAS  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

    PubMed  CAS  Google Scholar 

  • Monti DM, D’Alessio G (2004) Cytosolic RNase inhibitor only affects RNases with intrinsic cytotoxicity. J Biol Chem 279(38):39195–39198

    PubMed  CAS  Google Scholar 

  • Monti DM, Montesano Gesualdi N, Matousek J, Esposito F, D’Alessio G (2007) The cytosolic ribonuclease inhibitor contributes to intracellular redox homeostasis. FEBS Lett 581(5):930–934

    PubMed  CAS  Google Scholar 

  • Monti DM, Yu W, Pizzo E, Shima K, Hu MG, Di Malta C, Piccoli R, D’Alessio G, Hu GF (2009) Characterization of the angiogenic activity of zebrafish ribonucleases. FEBS J 276(15):4077–4090

    PubMed  CAS  Google Scholar 

  • Moroianu J, Riordan JF (1994a) Identification of the nucleolar targeting signal of human angiogenin. Biochem Biophys Res Commun 203(3):1765–1772

    PubMed  CAS  Google Scholar 

  • Moroianu J, Riordan JF (1994b) Nuclear translocation of angiogenic proteins in endothelial cells: an essential step in angiogenesis. Biochemistry 33:12535–12539

    PubMed  CAS  Google Scholar 

  • Mosimann SC, Ardelt W, James MN (1994) Refined 1.7 Å x-ray crystallographic structure of p-30 protein, an amphibian ribonuclease with anti-tumor activity. J Mol Biol 236(4):1141–1153

    PubMed  CAS  Google Scholar 

  • Murthy BS, De Lorenzo C, Piccoli R, D’Alessio G, Sirdeshmukh R (1996) Effects of protein RNase inhibitor and substrate on the quaternary structures of bovine seminal RNase. Biochemistry 35:3880–3885

    PubMed  CAS  Google Scholar 

  • Naddeo M, Vitagliano L, Russo A, Gotte G, D’Alessio G, Sorrentino S (2005) Interactions of the cytotoxic RNase A dimers with the cytosolic ribonuclease inhibitor. FEBS Lett 579(12):2663–2668

    PubMed  CAS  Google Scholar 

  • Nakano T, Graf T (1992) Identification of genes differentially expressed in two types of v-myb-transformed avian myelomonocytic cells. Oncogene 7(3):527–534

    PubMed  CAS  Google Scholar 

  • Navarro S, Aleu J, Jimenez M, Boix E, Cuchillo CM, Nogues MV (2008) The cytotoxicity of eosinophil cationic protein/ribonuclease 3 on eukaryotic cell lines takes place through its aggregation on the cell membrane. Cell Mol Life Sci 65(2):324–337

    PubMed  CAS  Google Scholar 

  • Newton DL, Boque L, Wlodawer A, Huang CY, Rybak SM (1998) Single amino acid substitutions at the N-terminus of a recombinant cytotoxic ribonuclease markedly influence biochemical and biological properties. Biochemistry 37(15):5173–5183

    PubMed  CAS  Google Scholar 

  • Nitta R, Katayama N, Okabe Y, Iwama M, Watanabe H, Abe Y, Okazaki T, Ohgi K, Irie M (1989) Primary structure of a ribonuclease from bullfrog (Rana catesbeiana) liver. J Biochem 106(5):729–735

    PubMed  CAS  Google Scholar 

  • Nitto T, Lin C, Dyer KD, Wagner RA, Rosenberg HF (2005) Characterization of a ribonuclease gene and encoded protein from the reptile, Iguana iguana. Gene 352:36–44

    PubMed  CAS  Google Scholar 

  • 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(35):25622–25634

    PubMed  CAS  Google Scholar 

  • Notomista E, Catanzano F, Graziano G, Dal Piaz F, Barone G, D’Alessio G, Di Donato A (2000) Onconase: an unusually stable protein. Biochemistry 39(30):8711–8718

    PubMed  CAS  Google Scholar 

  • Notomista E, Catanzano F, Graziano G, Di Gaetano S, Barone G, Di Donato A (2001) Contribution of chain termini to the conformational stability and biological activity of onconase. Biochemistry 40(31):9097–9103

    PubMed  CAS  Google Scholar 

  • Notomista E, Mancheno JM, Crescenzi O, Di Donato A, Gavilanes J, D’Alessio G (2006) The role of electrostatic interactions in the antitumor activity of dimeric RNases. FEBS J 273(16):3687–3697

    PubMed  CAS  Google Scholar 

  • O’Reilly MS, Holmgren L, Chen C, Folkman J (1996) Angiostatin induces and sustains dormancy of human primary tumors in mice. Nat Med 2(6):689–692

    PubMed  Google Scholar 

  • Oppenheim JJ, Yang D (2005) Alarmins: chemotactic activators of immune responses. Curr Opin Immunol 17(4):359–365

    PubMed  CAS  Google Scholar 

  • Park C, Raines RT (2000) Dimer formation by a “monomeric” protein. Protein Sci 9(10):2026–2033

    PubMed  CAS  Google Scholar 

  • Penttinen J, Pujianto DA, Sipila P, Huhtaniemi I, Poutanen M (2003) Discovery in silico and characterization in vitro of novel genes exclusively expressed in the mouse epididymis. Mol Endocrinol 17(11):2138–2151

    PubMed  CAS  Google Scholar 

  • Piatigorsky J, Wistow G (1991) The recruitment of crystallins: new functions precede gene duplication. Science 252(5009):1078–1079

    CAS  Google Scholar 

  • Piccoli R, Tamburrini M, Piccialli G, Di Donato A, Parente A, D’Alessio G (1992) The dual-mode quaternary structure of seminal RNase. Proc Natl Acad Sci USA 89:1870–1874

    PubMed  CAS  Google Scholar 

  • Piccoli R, Di Gaetano S, De Lorenzo C, Grauso M, Monaco C, Spalletti-Cernia D, Laccetti P, Cinatl J, Matousek J, D’Alessio G (1999) A dimeric mutant of human pancreatic ribonuclease with selective cytotoxicity toward malignant cells. Proc Natl Acad Sci USA 96(14):7768–7773

    PubMed  CAS  Google Scholar 

  • Picone D, Di Fiore A, Ercole C, Franzese M, Sica F, Tomaselli S, Mazzarella L (2005) The role of the hinge loop in domain swapping. The special case of bovine seminal ribonuclease. J Biol Chem 280(14):13771–13778

    PubMed  CAS  Google Scholar 

  • Pizzo E, D’Alessio G (2007) The success of the RNase scaffold in the advance of biosciences and in evolution. Gene 406(1–2):8–12

    PubMed  CAS  Google 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

    PubMed  CAS  Google Scholar 

  • 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(6):1283–1295

    PubMed  CAS  Google Scholar 

  • Pizzo E, Merlino A, Turano M, Russo Krauss I, Coscia F, Zanfardino A, Varcamonti M, Furia A, Giancola C, Mazzarella L, Sica F, D’Alessio G (2010) A new RNase sheds light on the RNase/angiogenin subfamily from zebrafish. Biochem J 433(2):345–355

    Google Scholar 

  • Plummer TH Jr, Hirs CH (1964) On the structure of bovine pancreatic ribonuclease B. Isolation of a glycopeptide. J Biol Chem 239:2530–2538

    PubMed  CAS  Google Scholar 

  • Potenza N, Salvatore V, Migliozzi A, Martone V, Nobile V, Russo A (2006) Hybridase activity of human ribonuclease-1 revealed by a real-time fluorometric assay. Nucleic Acids Res 34(10):2906–2913

    PubMed  CAS  Google Scholar 

  • Quarto N, Pizzo E, D’Alessio G (2008) Temporal and spatial expression of RNases from zebrafish (Danio rerio). Gene 427(1–2):32–41

    PubMed  CAS  Google Scholar 

  • Raines RT (1998) Ribonuclease A. Chem Rev 98(3):1045–1066

    PubMed  CAS  Google Scholar 

  • Richards FM, Wyckoff HW (1971) Bovine pancreatic ribonuclease. In: Boyer P (ed) Enzymes, vol 4, 3rd edn. Academic Press, New York, pp 647–806

    Google Scholar 

  • Riordan JF (1997) Structure and function of angiogenin. In: D’Alessio G, Riordan JF (eds) Ribonucleases: structures and functions. Academic, New York, pp 446–466

    Google Scholar 

  • Rosenberg HF (1995) Recombinant human eosinophil cationic protein. Ribonuclease activity is not essential for cytotoxicity. J Biol Chem 270(14):7876–7881

    PubMed  CAS  Google Scholar 

  • Rosenberg HF, Domachowske JB (2001) Eosinophils, eosinophil ribonucleases, and their role in host defense against respiratory virus pathogens. J Leukoc Biol 70(5):691–698

    PubMed  CAS  Google Scholar 

  • Rosenberg HF, Dyer KD (1995) Human ribonuclease 4 (RNase 4): coding sequence, chromosomal localization and identification of two distinct transcripts in human somatic tissues. Nucleic Acids Res 23(21):4290–4295

    PubMed  CAS  Google Scholar 

  • Rosenberg HF, Dyer KD (1996) Molecular cloning and characterization of a novel human ribonuclease (RNase k6): increasing diversity in the enlarging ribonuclease gene family. Nucleic Acids Res 24(18):3507–3513

    PubMed  CAS  Google Scholar 

  • Rosenberg HF, Zhang J, Liao YD, Dyer KD (2001) Rapid diversification of RNase A superfamily ribonucleases from the bullfrog, Rana catesbeiana. J Mol Evol 53(1):31–38

    PubMed  CAS  Google Scholar 

  • Rubin J, Zagai U, Blom K, Trulson A, Engstrom A, Venge P (2009) The coding ECP 434(G>C) gene polymorphism determines the cytotoxicity of ECP but has minor effects on fibroblast-mediated gel contraction and no effect on RNase activity. J Immunol 183(1):445–451

    PubMed  CAS  Google Scholar 

  • Rudolph B, Podschun R, Sahly H, Schubert S, Schroder JM, Harder J (2006) Identification of RNase 8 as a novel human antimicrobial protein. Antimicrob Agents Chemother 50(9):3194–3196

    PubMed  CAS  Google 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

    PubMed  CAS  Google Scholar 

  • Rutkoski TJ, Raines RT (2008) Evasion of ribonuclease inhibitor as a determinant of ribonuclease cytotoxicity. Curr Pharm Biotechnol 9(3):185–189

    PubMed  CAS  Google Scholar 

  • Rutkoski TJ, Kink JA, Strong LE, Schilling CI, Raines RT (2010) Antitumor activity of ribonuclease multimers created by site-specific covalent tethering. Bioconjug Chem 21(9):1691–1702

    PubMed  CAS  Google Scholar 

  • Rybak SM (2008) Antibody-onconase conjugates: cytotoxicity and intracellular routing. Curr Pharm Biotechnol 9(3):226–230

    PubMed  CAS  Google Scholar 

  • Sassi SO, Braun EL, Benner SA (2007) The evolution of seminal ribonuclease: pseudogene reactivation or multiple gene inactivation events? Mol Biol Evol 24(4):1012–1024

    PubMed  CAS  Google Scholar 

  • Schulenburg C, Low C, Weininger U, Mrestani-Klaus C, Hofmann H, Balbach J, Ulbrich-Hofmann R, Arnold U (2009) The folding pathway of onconase is directed by a conserved intermediate. Biochemistry 48(35):8449–8457

    PubMed  CAS  Google 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. Chembiochem 11(7):978–986

    PubMed  CAS  Google Scholar 

  • 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(9):1238–1247

    PubMed  CAS  Google Scholar 

  • Seno M, Futami J, Kosaka M, Seno S, Yamada H (1994) Nucleotide sequence encoding human pancreatic ribonuclease. Biochim Biophys Acta 1218(3):466–468

    PubMed  CAS  Google Scholar 

  • Seno M, Futami J, Tsushima Y, Akutagawa K, Kosaka M, Tada H, Yamada H (1995) Molecular cloning and expression of human ribonuclease 4 cDNA. Biochim Biophys Acta 1261(3):424–426

    PubMed  Google Scholar 

  • Shapiro R, Fett JW, Strydom DJ, Vallee BL (1986) Isolation and characterization of a human colon carcinoma-secreted enzyme with pancreatic ribonuclease-like activity. Biochemistry 25(23):7255–7264

    PubMed  CAS  Google Scholar 

  • Sica F, Di Fiore A, Merlino A, Mazzarella L (2004) Structure and stability of the non-covalent swapped dimer of bovine seminal ribonuclease: an enzyme tailored to evade ribonuclease protein inhibitor. J Biol Chem 279(35):36753–36760

    PubMed  CAS  Google Scholar 

  • Simons BL, King MC, Cyr T, Hefford MA, Kaplan H (2002) Covalent cross-linking of proteins without chemical reagents. Protein Sci 11(6):1558–1564

    PubMed  CAS  Google Scholar 

  • Simons BL, Kaplan H, Fournier SM, Cyr T, Hefford MA (2007) A novel cross-linked RNase A dimer with enhanced enzymatic properties. Proteins 66(1):183–195

    PubMed  CAS  Google Scholar 

  • Sinatra F, Callari D, Viola M, Longombardo MT, Patania M, Litrico L, Emmanuele G, Lanteri E, D’Alessandro N, Travali S (2000) Bovine seminal RNase induces apoptosis in normal proliferating lymphocytes. Int J Clin Lab Res 30(4):191–196

    PubMed  CAS  Google Scholar 

  • Smith BD, Raines RT (2006) Genetic selection for critical residues in ribonucleases. J Mol Biol 362(3):459–478

    PubMed  CAS  Google Scholar 

  • Snyder M, Gleich G (1997) Eosinophil-associated ribonucleases. In: D’Alessio G, Riordan G (eds) Ribonucleases: structures and functions. Academic Press, San Diego, pp 426–444

    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  CAS  Google Scholar 

  • Sorrentino S, Libonati M (1994) Human pancreatic type and non-pancreatic type ribonucleases: a direct side-by-side comparison of their catalytic properties. Arch Biochem Biophys 312:340–348

    PubMed  CAS  Google Scholar 

  • Sorrentino S, Tucker GK, Glitz DG (1988) Purification and characterization of a ribonuclease from human liver. J Biol Chem 263(31):16125–16131

    PubMed  CAS  Google Scholar 

  • Sorrentino S, Glitz DG, Hamann KJ, Loegering DA, Checkel JL, Gleich GJ (1992) Eosinophil-derived neurotoxin and human liver ribonuclease. Identity of structure and linkage of neurotoxicity to nuclease activity. J Biol Chem 267(21):14859–14865

    PubMed  CAS  Google Scholar 

  • Soucek J, Hruba A, Paluska E, Chudomel V, Dostal J, Matousek J (1983) Immunosuppressive effects of bovine seminal fluid fractions with ribonuclease activity. Folia Biol 29(3):250–261

    CAS  Google Scholar 

  • Soucek J, Marinov I, Benes J, Hilgert I, Matousek J, Raines RT (1996) Immunosuppressive activity of bovine seminal ribonuclease and its mode of action. Immunobiology 195(3):271–285

    PubMed  CAS  Google Scholar 

  • Strydom DJ (1998) The angiogenins. Cell Mol Life Sci 54(8):811–824

    PubMed  CAS  Google 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

    PubMed  CAS  Google Scholar 

  • Suzuki M, Saxena SK, Boix E, Prill RJ, Vasandani VM, Ladner JE, Sung C, Youle RJ (1999) Engineering receptor-mediated cytotoxicity into human ribonucleases by steric blockade of inhibitor interaction. Nat Biotechnol 17(3):265–270

    PubMed  CAS  Google Scholar 

  • Tamburrini M, Scala G, Verde C, Ruocco MR, Parente A, Venuta S, D’Alessio G, Tamburrini M, Scala G, Verde C, Ruocco MR, Parente A, Venuta S, D’Alessio G (1990) Immunosuppressive activity of bovine seminal RNase on T-cell proliferation. Eur J Biochem 190:145–148

    PubMed  CAS  Google Scholar 

  • Titani K, Takio K, Kuwada M, Nitta K, Sakakibara F, Kawauchi H, Takayanagi G, Hakomori S (1987) Amino acid sequence of sialic acid binding lectin from frog (Rana catesbeiana) eggs. Biochemistry 26(8):2189–2194

    PubMed  CAS  Google Scholar 

  • Torrent M, Cuyas E, Carreras E, Navarro S, Lopez O, de la Maza A, Nogues MV, Reshetnyak YK, Boix E (2007) Topography studies on the membrane interaction mechanism of the eosinophil cationic protein. Biochemistry 46(3):720–733

    PubMed  CAS  Google Scholar 

  • Torrent M, Badia M, Moussaoui M, Sanchez D, Nogues MV, Boix E (2010) Comparison of human RNase 3 and RNase 7 bactericidal action at the gram-negative and gram-positive bacterial cell wall. FEBS J 277(7):1713–1725

    PubMed  CAS  Google Scholar 

  • Trabesinger Ruef N, Jermann T, Zankel T, Durrant B, Frank G, Benner SA (1996) Pseudogenes in ribonuclease evolution: a source of new biomacromolecular function? FEBS Lett 382(3):319–322

    PubMed  CAS  Google Scholar 

  • 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(4):1352–1360

    PubMed  CAS  Google Scholar 

  • Turcotte RF, Raines RT (2008) Interaction of onconase with the human ribonuclease inhibitor protein. Biochem Biophys Res Commun 377(2):512–514

    PubMed  CAS  Google Scholar 

  • Vescia S, Tramontano D, Augusti Tocco G, D’Alessio G (1980) In vitro studies on selective inhibition of tumor cell growth by seminal ribonuclease. Cancer Res 40(10):3740–3744

    PubMed  CAS  Google Scholar 

  • Vicentini AM, Hemmings BA, Hofsteenge J (1994) Residues 36–42 of liver RNase pl3 contribute to its uridine-preferring substrate specificity. Cloning of the cDNA and site-directed mutagenesis studies. Protein Sci 3(3):459–466

    PubMed  CAS  Google Scholar 

  • Vicentini AM, Kote-Jarai Z, Hofsteenge J (1996) Structural determinants of the uridine-preferring specificity of RNase pl3. Biochemistry 35(28):9128–9132

    PubMed  CAS  Google Scholar 

  • Viola M, Libra M, Callari D, Sinatra F, Spada D, Noto D, Emmanuele G, Romano F, Averna M, Pezzino FM, Stivala F, Travali S (2005) Bovine seminal ribonuclease is cytotoxic for both malignant and normal telomerase-positive cells. Int J Oncol 27(4):1071–1077

    PubMed  CAS  Google Scholar 

  • Vitagliano L, Merlino A, Zagari A, Mazzarella L (2000) Productive and nonproductive binding to ribonuclease A: x-ray structure of two complexes with uridylyl(2′,5′)guanosine. Protein Sci 9(6):1217–1225

    PubMed  CAS  Google Scholar 

  • Vitagliano L, Merlino A, Zagari A, Mazzarella L (2002) Reversible substrate-induced domain motions in ribonuclease A. Proteins 46(1):97–104

    PubMed  CAS  Google Scholar 

  • Vottariello F, Costanzo C, Gotte G, Libonati M (2010) “Zero-length” dimers of ribonuclease A: further characterization and no evidence of cytotoxicity. Bioconjug Chem 21(4):635–645

    PubMed  CAS  Google Scholar 

  • Wang S, Li H (2006) Radical scavenging activity of ribonuclease inhibitor from cow placenta. Biochemistry (Moscow) 71:520–524

    CAS  Google Scholar 

  • Wright PE, Dyson HJ (1999) Intrinsically unstructured proteins: re-assessing the protein structure-function paradigm. J Mol Biol 293(2):321–331

    PubMed  CAS  Google Scholar 

  • Wright PE, Dyson HJ (2009) Linking folding and binding. Curr Opin Struct Biol 19(1):31–38

    PubMed  CAS  Google 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  CAS  Google Scholar 

  • 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(6):609–617

    PubMed  CAS  Google Scholar 

  • 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(2):287–292

    PubMed  CAS  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  CAS  Google Scholar 

  • Yang D, Rosenberg HF, Chen Q, Dyer KD, Kurosaka K, Oppenheim JJ (2003) Eosinophil-derived neurotoxin (EDN), an antimicrobial protein with chemotactic activities for dendritic cells. Blood 102(9):3396–3403

    PubMed  CAS  Google Scholar 

  • Yang D, Chen Q, Rosenberg HF, Rybak SM, Newton DL, Wang ZY, Fu Q, Tchernev VT, Wang M, Schweitzer B, Kingsmore SF, Patel DD, Oppenheim JJ, Howard OM (2004) Human ribonuclease a superfamily members, eosinophil-derived neurotoxin and pancreatic ribonuclease, induce dendritic cell maturation and activation. J Immunol 173(10):6134–6142

    PubMed  CAS  Google Scholar 

  • Youle RJ, D’Alessio G (1997) Antitumor RNases. In: D’Alessio G, Riordan JF (eds) Ribonucleases: structures and function. Academic Press, San Diego, pp 491–514

    Google Scholar 

  • Zanfardino A, Pizzo E, Di Maro A, Varcamonti M, D’Alessio G (2010) The bactericidal action on Escherichia coli of zf-RNase-3 is triggered by the suicidal action of the bacterium OmpT protease. FEBS J 277(8):1921–1928

    PubMed  CAS  Google Scholar 

  • Zhang J, Dyer KD, Rosenberg HF (2000) Evolution of the rodent eosinophil-associated RNase gene family by rapid gene sorting and positive selection. Proc Natl Acad Sci USA 97(9):4701–4706

    PubMed  CAS  Google 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

    PubMed  CAS  Google Scholar 

  • Zhang J, Dyer KD, Rosenberg HF (2003) Human RNase 7: a new cationic ribonuclease of the RNase A superfamily. Nucleic Acids Res 31(2):602–607

    PubMed  CAS  Google 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

    PubMed  CAS  Google Scholar 

  • Zhao H, Ardelt B, Ardelt W, Shogen K, Darzynkiewicz Z (2008) The cytotoxic ribonuclease onconase targets RNA interference (siRNA). Cell Cycle 7(20):3258–3261

    PubMed  CAS  Google 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 217:401–409

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

I wish to thank my colleagues Tina Giancola, Guo-Fu Hu, Lelio Mazzarella, Antonello Merlino, Elio Pizzo, James F. Riordan, and Filomena Sica, who kindly contributed to improve the manuscript with their suggestions.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Giuseppe D’Alessio .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2011 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

D’Alessio, G. (2011). The Superfamily of Vertebrate-Secreted Ribonucleases. In: Nicholson, A. (eds) Ribonucleases. Nucleic Acids and Molecular Biology. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-21078-5_1

Download citation

Publish with us

Policies and ethics