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The angiogenins: An emerging family of ribonuclease related proteins with diverse cellular functions

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Abstract

Angiogenin is a member of the ribonuclease superfamily, which shows an ever expanding collection of molecules being identified and cloned. It was initially isolated from the conditioned medium of cultured tumour cells. Its angiogenic activity appears to be critical for the maintenance and support of tumour growth. Angiogenin also plays a role in a number of non-malignant vasculoproliferative pathological conditions. Along with other related molecules, it has been identified in a wide variety of somatic tissues in adult and embryonic stages of vertebrate development. This suggests that angiogenin and related molecules are likely to play a vital role in normal physiology. Angiogenin is detectable in serum and to date has been implicated as a mitogen for vascular endothelial cells, an immune modulator with suppressive effects on polymorphonuclear leukocytes, an activator of certain protease cascades such as matrix metalloproteases and plasminogen-activated plasmin pathways, as well as an adhesion molecule. However, the role of the angiogenin family in both normal and abnormal physiology and in development will only fully be realised by genetic approaches involving gene deletion.

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References

  1. Polverini PJ. The pathophysiology of angiogenesis. Crit Rev Oral Biol 1995; 6: 230–47.

    CAS  Google Scholar 

  2. Folkman J, Klagsbrun M. Angiogenic factors. Science 1987; 235: 442–7.

    PubMed  CAS  Google Scholar 

  3. Folkman J, Cotran RS. Relation of vascular proliferation to tumour growth. Int Rev Exp Path 1976; 16: 207–48.

    PubMed  CAS  Google Scholar 

  4. Folkman J. Tumour angiogenesis: Therapeutic implications. N Engl J Med 1971; 285: 1185–6.

    Article  Google Scholar 

  5. Blood CH, Zetter BR. Tumour interaction with the vasculature: Angiogenesis and tumour metastasis. Biochim Biophys Acta 1990; 1032: 89–118.

    PubMed  CAS  Google Scholar 

  6. Pepper MS, Vassalli JD, Montesano R, Orci L. Urokinase-type plasminogen activator is induced in migrating capillary endothelial cells. J Cell Biol 1987; 105: 2535–41.

    PubMed  CAS  Google Scholar 

  7. Moscatelli D, Rifkin DB. Membrane and matrix localisation of proteinases — a common theme in tumour cell invasion and angiogenesis. Biochim Biophys Acta 1988; 948: 67–85.

    PubMed  CAS  Google Scholar 

  8. Odekon LE, Sato Y, Rifkin DB. Urokinase-type plasminogen activator mediates basic fibroblast growth factor induced bovine endothelial cell migration independent of its proteolytic activity. J Cell Physiol 1992; 150: 258–63.

    PubMed  CAS  Google Scholar 

  9. Thomas KA, Gimeneg-Gallego G. Fibroblast growth factors: Broad spectrum mitogens with potent angiogenic activity. Trends Biochem Sci USA 1986; 11: 81–4.

    CAS  Google Scholar 

  10. Leung DW, Cachiones G, Kuangiogenin WJ et al. Vascular endothelial growth factor is a secreted angiogenic mitogen. Science 1989; 246: 1306–12.

    PubMed  CAS  Google Scholar 

  11. Klagsbrun N, D'Amore PA. Regulators of angiogenesis. Annu Rev Physiol 1991; 53: 217–39.

    PubMed  CAS  Google Scholar 

  12. Haraguchi M, Miyadera K, Uemura K et al. Angiogenic activity of enzymes. Nature 1994; 368: 198.

    PubMed  CAS  Google Scholar 

  13. Fett JW, Strydom DJ, Lobb RR et al. Isolation and characterization of Angiogenin, an angiogenic protein from human carcinoma cells. Biochemistry 1985; 24: 5480–6.

    PubMed  CAS  Google Scholar 

  14. Strydom DJ, Fett JW, Lobb RR, et al. Amino acid sequence of tumour derived Angiogenin. Biochemistry 1985; 24: 5486–94.

    PubMed  CAS  Google Scholar 

  15. Kurachi K, Davie EW, Strydom DJ, Vallee BL. Sequence of the cDNA and gene for Angiogenin, a human angiogenesis factor. Biochemistry 1985; 24: 5494–9.

    PubMed  CAS  Google Scholar 

  16. Knighton D, Ausprunk D, Tapper D et al. Avascular and vascular phases of tumour growth in the chick embryo. Br J Cancer 1977; 35: 347–56.

    PubMed  CAS  Google Scholar 

  17. Langer R, Folkman J. Polymers for the sustained release of proteins and other macromolecules. Nature 1976; 263: 797–800.

    PubMed  CAS  Google Scholar 

  18. Shapiro R, Strydom DJ, Olson KA et al. Isolation of Angiogenin from natural human plasma. Biochemistry 1987; 26: 5141–6.

    PubMed  CAS  Google Scholar 

  19. D'Alessio G, Riordan JF. In D'Alessio G, Riordan JF (eds): Ribonucleases: Structure and Function. New York: Academic Press 1997.

    Google Scholar 

  20. Sorrentino S, Libonati M. Structure function relationships in human ribonucleases: Main distinctive features of the major RNase types. FEBS Lett 1997; 404: 1–5.

    PubMed  CAS  Google Scholar 

  21. Beintema JJ, Schuller C, Irie M et al. Molecular evolution of the ribonuclease superfamily. Prog Biophys Mol Biol 1988; 51: 165–92.

    PubMed  CAS  Google Scholar 

  22. Ackerman SJ. In Makino S, Fukada T (eds): Eosinophils: Biological and Clinical Aspects. Boca Raton, Florida: CRC Press 1993.

    Google Scholar 

  23. Seno M, Futami J, Tsushuma Y et al. Molecular cloning and expression of human ribonuclease-4 cDNA. Biochem Biophys Acta 1995; 1261: 424–6.

    PubMed  Google Scholar 

  24. Rosenberg HF, Dyer KD. Human ribonuclease-4 (Rnase-4)-coding sequence, chromosomal localization and identification of 2 distinct transcripts in human somatic tissues. Nucleic Acids Res 1995; 23: 4240–95.

    Google Scholar 

  25. Rosenberg HF, Dyer KD. Molecular cloning and characterization of a novel human ribonuclease (Rnase k6): Increasing diversity in the enlarging ribonuclease gene family. Nucleic Acids Res 1996; 24: 3507–13.

    PubMed  CAS  Google Scholar 

  26. Batten D, Dyer KD, Damachowske JB, Rosenberg HF. Molecular cloning of four novel murine ribonuclease genes: Unusual expansion within the ribonuclease A gene family. Nucleic Acids Res 1997; 25: 4235–9.

    PubMed  CAS  Google Scholar 

  27. Larson KA, Olson EV, Madden BJ et al. Two highly homologous ribonuclease genes expressed in mouse eosinophils identify a larger subgroup of the mammalian ribonuclease superfamily. Proc Natl Acad Sci USA 1996; 93: 12370–5.

    PubMed  CAS  Google Scholar 

  28. Bond MD, Strydom DJ, Vallee BL. Characterization and sequencing of rabbit, pig and mouse Angiogenin. Discernment of functionally important residues and regions. Biochim Biophys Acta 1993; 1162: 177–86.

    PubMed  CAS  Google Scholar 

  29. Vallee BL, Riordan JF. Organogenesis and Angiogenin. Cell Mol Life Sci 1997; 53: 803–15.

    PubMed  CAS  Google Scholar 

  30. Harper JW, Vallee BL. A covalent Angiogenin ribonuclease hybrid with a fourth disulfide bond generated by regional mutagenesis. Biochemistry 1989; 28: 1875–84.

    PubMed  CAS  Google Scholar 

  31. Acharya KR, Subramanian V, Shapiro R et al. Crystallization and preliminary X-ray analysis of human Angiogenin. J Mol Biol 1992; 228: 1269–70.

    PubMed  CAS  Google Scholar 

  32. Acharya KR, Shapiro R, Allen SC et al. Crystal structure of human Angiogenin reveals the structural basis for its functional divergence from ribonuclease. Proc Natl Acad Sci USA 1994; 91: 2915–9.

    PubMed  CAS  Google Scholar 

  33. Acharya KR, Leonidas DD, Papageorgiou AC et al. Structural studies on Angiogenin, a protein implicated in neovascularization during tumour growth. In Maragoudakis ME (ed): Angiogenesis: Models, Modulators and Clinical Applications. New York: Plenum Press 1998; 165–78.

    Google Scholar 

  34. Russo N, Shapiro R, Acharya KR. Role of glutamine in the ribonucleolytic activity of human Angiogenin. Proc Natl Acad Sci USA 1994; 91: 2920–4.

    PubMed  CAS  Google Scholar 

  35. Hallahan TW, Shapiro R, Vallee BL. Dual site mode for the angiogenic activity of Angiogenin. Proc Natl Acad Sci USA 1991; 88: 2222–6.

    PubMed  CAS  Google Scholar 

  36. Hallahan TW, Shapiro R, Strydom DJ, Vallee BL. Importance of Asparagine-61 and Asparagine-109 to the angiogenic activity of human Angiogenin. Biochemistry 1992; 31: 8022–9.

    PubMed  CAS  Google Scholar 

  37. Acharya KR, Shapiro R, Riordan JF, Vallee BL. Crystal structure of bovine angiogenin at 1.5 Å resolution. Proc Natl Acad Sci USA 1995; 92: 2949–53.

    PubMed  CAS  Google Scholar 

  38. Maes P, Damart D, Rommens C et al. The complete amino acid sequence of bovine milk Angiogenin. FEBS Lett 1988; 241: 41–5.

    PubMed  CAS  Google Scholar 

  39. Shapiro R, Riordan JF, Vallee BL. Characteristic ribonucleolytic activity of human Angiogenin. Biochemistry 1986; 25: 3527–32.

    PubMed  CAS  Google Scholar 

  40. St Clair DK, Rybak SM, Riordan JF, Vallee BL. Angiogenin abolishes cell-free protein synthesis by specific ribonucleolytic inactivation of 40S ribosomes. Biochemistry 1988; 27: 7263–8.

    PubMed  CAS  Google Scholar 

  41. Saxena SK, Rybak S, Davey RT et al. Angiogenin is a cytotoxic tRNA-specific ribonuclease in the RNase A superfamily. J Biol Chem 1992; 30: 21982–6.

    Google Scholar 

  42. Shapiro R, Vallee BL. Site directed mutagenesis of histidine-13 and histidine-114 of human Angiogenin. Alanine derivatives inhibit Angiogenin-induced angiogenesis. Biochemistry 1989; 28: 7401–8.

    PubMed  CAS  Google Scholar 

  43. Shapiro R, Fox EA, Riordan JF. Role of lysines in human Angiogenin: Chemical modification and site-directed mutagenesis. Biochemistry 1989; 28: 1726–32.

    PubMed  CAS  Google Scholar 

  44. Curran TP, Shapiro R, Riordan JF. Alteration of the enzymatic specificity of human Angiogenin by site-directed mutagenesis. Biochemistry 1993; 32: 2307–13.

    PubMed  CAS  Google Scholar 

  45. Rybak SM, Vallee BL. Base cleavage specificity of Angiogenin with Saccharomyces cerevisiae and Escherichia coli 5S RNAs. Biochemistry 1988; 27: 2288–94.

    PubMed  CAS  Google Scholar 

  46. Shapiro R, Weremowicz S, Riordan JF, Vallee BL. Ribonucleolytic activity of Angiogenin — essential histidine, lysine and arginine residues. Proc Natl Acad Sci USA 1987; 84: 8783–7.

    PubMed  CAS  Google Scholar 

  47. Hu GF, Riordan JF, Vallee BL. A putative Angiogenin receptor in Angiogenin-responsive human endothelial cells. Proc Natl Acad Sci USA 1997; 94: 2204–9.

    PubMed  CAS  Google Scholar 

  48. Hu GF, Strydom DJ, Fett JW et al. Actin is a binding protein for Angiogenin. Proc Natl Acad Sci USA 1993; 90: 1217–21.

    PubMed  CAS  Google Scholar 

  49. Olson KA, Fett JW, French TC et al. Angiogenin antagonists prevent tumour growth in vivo. Proc Natl Acad Sci USA 1995; 92: 442–6.

    PubMed  CAS  Google Scholar 

  50. Kinoshita N, Minshull J, Kirschner MW. The identification of two novel ligands of the FGF receptor by a yeast screening method and their activity in Xenopus development. Cell 1995; 83: 621–30.

    PubMed  CAS  Google Scholar 

  51. Badet J, Soncin G, Guitton JD et al. Specific binding of Angiogenin to calf pulmonary artery endothelial cells. Proc Natl Acad Sci USA 1989; 86: 8427–31.

    PubMed  CAS  Google Scholar 

  52. Soncin F, Guitton JD, Cartwright T, Badet J. Interaction of human Angiogenin with copper modulates Angiogenin binding to endothelial cells. Biochem and Biophys Res Commun 1997; 236: 604–10.

    CAS  Google Scholar 

  53. Chamoux M, Dehouck MP, Fruchart JC et al. Characterization of Angiogenin receptors on bovine brain endothelial cells. Biochem Biophys Res Commun 1991; 176: 833–9.

    PubMed  CAS  Google Scholar 

  54. Moroianu J, Riordan JF. Nuclear translocation of Angiogenin in proliferating endothelial cells is essential to its angiogenic activity. Proc Natl Acad Sci USA 1994; 91: 1677–81.

    PubMed  CAS  Google Scholar 

  55. Li R, Riordan JF, Hu GF. Nuclear translocation of human Angiogenin in cultured human umbilical artery endothelial cells is microtubule and lysosome independent. Biochem Biophys Res Commun 1997; 238: 305–12.

    PubMed  CAS  Google Scholar 

  56. Lobie PE, Mertani H, Morel G et al. Receptor mediated nuclear translocation of growth hormone. J Biol Chem 1994; 269: 21330–9.

    PubMed  CAS  Google Scholar 

  57. Moroianu J, Riordan JF. Identification of the nucleolar targeting signal of human Angiogenin. Biochem Biophys Res Commun 1994; 203: 1765–72.

    PubMed  CAS  Google Scholar 

  58. Lee WW, Galbraith RM. The extracellular actin-scavenger system and actin toxicity. N Engl J Med 1992; 326: 1335–41.

    Article  PubMed  CAS  Google Scholar 

  59. Bicknell R, Vallee BL. Angiogenin activates endothelial cell phospholipase C. Proc Natl Acad Sci USA 1988; 85: 5961–5.

    PubMed  CAS  Google Scholar 

  60. Bicknell R, Vallee BL. Angiogenin stimulates endothelial cell prostacyclin secretion by activation of phospholipase A2. Proc Natl Acad Sci USA 1989; 86: 1573–7.

    PubMed  CAS  Google Scholar 

  61. Shapiro R, Vallee BL. Human placental ribonuclease inhibitor abolishes both angiogenic and ribonucleolytic activities of Angiogenin. Proc Natl Acad Sci USA 1987; 24: 2238–41.

    Google Scholar 

  62. Shapiro R, Vallee BL. Interaction of human placental ribonuclease with placental ribonuclease I inhibitor. Biochemistry 1991; 30: 2246–55.

    PubMed  CAS  Google Scholar 

  63. Lee FS, Shapiro RS, Vallee BL. Tight-binding inhibition of Angiogenin and ribonuclease A by placental ribonuclease inhibitor. Biochemistry 1989; 28: 225–30.

    PubMed  CAS  Google Scholar 

  64. Lee FS, Fox EA, Zhou HM et al. Primary structure of human placental ribonuclease inhibitor. Biochemistry 1988; 27: 8545–53.

    PubMed  CAS  Google Scholar 

  65. Kobe B, Deisenhofer J. Crystal structure of porcine ribonuclease inhibitor, a protein with leucine-rich repeats. Nature 1993; 366: 751–6.

    PubMed  CAS  Google Scholar 

  66. Baumann H, Gauldie J. The acute phase response. Immunol Today 1994; 15: 74–80.

    PubMed  CAS  Google Scholar 

  67. Trey JE, Kusher I. The acute phase response and the haematopoeitic system: the role of cytokines. Crit Rev Oncol Hematol 1994; 15: 74–80.

    Google Scholar 

  68. Olson K, Verseilis SJ, Fett JW. Angiogenin is regulated in vivo as an acute phase protein. Biochem and Biophys Res Commun 1998; 242: 480–3.

    CAS  Google Scholar 

  69. Hu GF, Riordan JF. Angiogenin enhances actin acceleration of plasminogen activation. Biochem Biophys Res Commun 1993; 197: 682–7.

    PubMed  CAS  Google Scholar 

  70. Hu GF, Riordan JF, Vallee BL. Angiogenin promotes invasiveness of cultured endothelial cells by stimulation of cell-associated proteolytic activities. Proc Natl Acad Sci USA 1994; 91: 12096–100.

    PubMed  CAS  Google Scholar 

  71. Jimi S, Ito K, Kohno K et al. Modulation by bovine Angiogenin of tubular morphogenesis and expression of plasminogen activator in bovine endothelial cells. Biochem Biophys Res Commun 1995; 211: 476–83.

    PubMed  CAS  Google Scholar 

  72. Sillix DH, Francis J, Mahajan S, Briggs W. Impaired granulocyte phagocytosis and bacteriocidal activity in nephrotic syndrome. Kidney Int 1983; 23: 93–6.

    Google Scholar 

  73. Tolkoff-Rubin NE, Rubin RH. Uremia and host defenses. N Engl J Med 1990; 322: 770–2.

    Article  PubMed  CAS  Google Scholar 

  74. Haag-Weber M, Horl WH. Dysfunction of polymorphonuclear leukocytes in uremia. Semin Nephrol 1996; 16: 192–201.

    PubMed  CAS  Google Scholar 

  75. Ritchey EE, Wallin JD, Shah SV. Chemi-luminescence and superoxide anion production by leukocytes from chronic haemodialysis patients. Kidney Int 1981; 19: 349–58.

    PubMed  CAS  Google Scholar 

  76. Haag-Weber M, Horl WH. Are granulocyte inhibitory proteins contributing to enhanced susceptibility to infections in uraemia? Nephrol Dial Transplant 1996; 11: 98–100.

    PubMed  Google Scholar 

  77. Mansell MA, Grimes AJ, Jones NF. Leukocyte ATP and renal failiure. Clin Sci 1981; 61: 43–6.

    PubMed  CAS  Google Scholar 

  78. Tschesche H, Kopp C, Horl WH, Hempelmann U. Inhibition of degranulation of polymorphonuclear leukocytes by Angiogenin and its tryptic fragment. J Biol Chem 1994; 48: 30274–80.

    Google Scholar 

  79. Matousek J, Soucek J, Riha J et al. Immunosuppressive activity of Angiogenin in comparison with bovine seminal ribonuclease and pancreatic ribonuclease. Comp Biochem Physiol. Part 2 Biochem Mol Biol 1995; 63: 249–56.

    Google Scholar 

  80. Hu GF. Limited proteolysis of Angiogenin by elastase is regulated by plasminogen. J Protein Chem 1997; 16: 669–79.

    PubMed  CAS  Google Scholar 

  81. O'Reilly MS, Holmgren L, Shing Y et al. Angiostatin: A novel angiogenesis inhibitor that mediates the suppression of metastases by a Lewis lung carcinoma. Cell 1994; 79: 315–28.

    PubMed  Google Scholar 

  82. Weiner HL, Weiner LH, Swain JL. Tissue distribution and developmental expression of the messenger RNA encoding Angiogenin. Science 1987; 237: 280–2.

    PubMed  CAS  Google Scholar 

  83. Soncin F. Angiogenin supports endothelial and fibroblast cell adhesion. Proc Natl Acad Sci USA 1992; 89: 2232–6.

    PubMed  CAS  Google Scholar 

  84. Soncin F, Shapiro R, Fett JW. A cell-surface proteoglycan mediates human adenocarcinoma HT-29 cell adhesion to human Angiogenin. J Biol Chem 1994; 269: 8999–9005.

    PubMed  CAS  Google Scholar 

  85. Soncin F, Strydom D, Shapiro R. Interaction of heparin with human Angiogenin. J Biol Chem 1997; 15: 9818–24.

    Google Scholar 

  86. Li D, Bell J, Brown A et al. The observation of Angiogenin and basic fibroblast growth factor gene expression in human colonic adenocarcinomas and hepatocellular carcinomas. J Pathol 1994; 172: 171–5.

    PubMed  CAS  Google Scholar 

  87. Chopra V, Dinh TV, Hannigan EV. Serum levels of interleukins, growth factors and Angiogenin in patients with endometrial cancer. J Cancer Res Clin Oncol 1997; 123: 167–72.

    PubMed  CAS  Google Scholar 

  88. Chopra V, Dinh TV, Hannigan EV. Circulating serum levels of cytokines and Angiogenic factors in patients with cervical cancer. Cancer Invest 1998; 16: 152–9.

    PubMed  CAS  Google Scholar 

  89. Shimoyama S, Gansauge F, Gansauge S, Negri G, Oohara T, Beger HG. Increased Angiogenin expression in pancreatic cancer is related to cancer aggressiveness. Cancer Res 1996; 56: 2703–6.

    PubMed  CAS  Google Scholar 

  90. Hartmann A, Kunz M, Kostlin S, Gillitzer R, Toksoy A, Brocker EB, Klein CE. Hypoxia-induced up-regulation of Angiogenin in human malignant melanoma. Cancer Res 1999; 59: 1578–83.

    PubMed  CAS  Google Scholar 

  91. Olson KA, French TC, Vallee BL, Fett JW. A monoclonal antibody to human Angiogenin suppresses tumour growth in athymic mice. Cancer Res 1994; 54: 4576–9.

    PubMed  CAS  Google Scholar 

  92. Olson KA, Fett J. Prostatic carcinoma therapy with Angiogenin antagonists. Proc Ame Assoc Cancer Res 1996; 37: 57.

    Google Scholar 

  93. Olson KA, Fett JW. Inhibition of tumour growth and metastasis by Angiogenin antisense therapy. Proc Am Assoc Cancer Res 1998; 39: 98.

    Google Scholar 

  94. Burgmann H, Hollenstein U, Maca T et al. Increased serum laminin and Angiogenin concentrations in patients with peripheral arterial occlusive disease. J Clin Pathol 1996; 49: 508–10.

    PubMed  CAS  Google Scholar 

  95. Hosaka S, Shah MR, Barquin N et al. Expression of basic fibroblast growth factor and Angiogenin in arthritis. Pathobiol 1995; 63: 249–56.

    Article  CAS  Google Scholar 

  96. Ozaki H, Hayashi H, Oshima K. Angiogenin levels in the vitreous from patients with proliferative diabetic retinopathy. Opthalmic Res 1996; 28: 356–60.

    Article  CAS  Google Scholar 

  97. Gho YS, Chae CD. Anti angiogenic activity of the peptides complementary to the receptor binding site of Angiogenin. J Biol Chem 1997; 272: 24294–9.

    PubMed  CAS  Google Scholar 

  98. Kolben M, Blaser J, Ulm K et al. Angiogenin plasma levels during pregnancy. Am J Obstet Gynaecol 1997; 176: 37–41.

    CAS  Google Scholar 

  99. Malamitsi-Puchner A, Sarandakou A, Giannaki G et al. Changes of Angiogenin serum concentrations in the perinatal period. Pediatr Res 1997; 41: 909–11.

    PubMed  CAS  Google Scholar 

  100. Spong CY, Ghidini A, Walker CN et al. Elevated maternal serum midtrimester alpha-fetoprotein levels are associated with fetoplacental ischaemia. Am J Obstet Gynaecol 1997; 177: 1085–7.

    CAS  Google Scholar 

  101. Strydom DJ, Bond MD, Vallee BL. An angiogenic protein from bovine serum and milk-purification and primary structure of Angiogenin-2. Eur J Biochem 1997; 247: 535–44.

    PubMed  CAS  Google Scholar 

  102. Fu X, Kamps MP. E2a-Pbx1 induces aberrant expression of tissue specific and developmentally regulated genes when expressed in NIH 3T3 fibroblasts. Mol Cell Biol 1997; 17: 1503–12.

    PubMed  CAS  Google Scholar 

  103. Kamps MP, Baltimore DL. E2a-Pbx1, the t(1;19) translocation protein of human pre-B cell ALL, causes acute myeloblastic leukaemia in mice. Mol Cell Biol 1993; 13: 351–7.

    PubMed  CAS  Google Scholar 

  104. Dedera DA, Waller EK, Lebrum DP. Chimeric homeobox gene E2a-Pbx1 induces proliferation, apoptosis and malignant lymphomas in transgenic mice. Cell 1993; 74: 833–43.

    PubMed  CAS  Google Scholar 

  105. Brown WE, Nobile V, Subramanian V, Shapiro R. The mouse Angiogenin gene family: structures of an Angiogenin related protein gene and two pseudogenes. Genomics 1995; 29: 200–6.

    PubMed  CAS  Google Scholar 

  106. Nobile V, Vallee BL, Shapiro R. Characterization of mouse Angiogenin-related protein: implications for functional studies on Angiogenin. Proc Natl Acad Sci USA 1996; 93: 4331–5.

    PubMed  CAS  Google Scholar 

  107. Adams MD, Kierlavage AR, Fleischmann RD et al. Initial assessment of human gene diversity and expression patterns based upon 83 million nucleotides of cDNA sequence. Nature 1995; 377(6547 Suppl): 3–174.

    PubMed  CAS  Google Scholar 

  108. Rybak SM, Fett JW, Yao QZ, Vallee BL. Angiogenin mRNA in human tumour and normal cells. Biochem Biophys Res Com 1987; 146: 1240–3.

    PubMed  CAS  Google Scholar 

  109. Chang SI, Jeong GB, Park SH et al. Detection, quantitation, and localization of bovine Angiogenin by immunological assays. Biochem Biophys Res Com 1997; 232: 323–7.

    PubMed  CAS  Google Scholar 

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    Susan A. Adams & Vasanta Subramanian

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Adams, S.A., Subramanian, V. The angiogenins: An emerging family of ribonuclease related proteins with diverse cellular functions. Angiogenesis 3, 189–199 (1999). https://doi.org/10.1023/A:1009015512200

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