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Relationship of angiogenin to pathophysiology of diseases

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Abstract

Angiogenin is a powerful stimulator of new blood vessel formation. It is a member of pancreatic ribonuclease (RNase) superfamily. It was originally isolated from conditioned medium of cultured tumor cells. Along with other associated molecules, it has been recognized in a variety of somatic tissues in embryonic stages and adult of vertebrate development. It binds to high-affinity endothelial cell surface receptors and, with lower affinity, to extracellular matrix. This suggests that angiogenin and related molecules are likely to play a vital role in normal physiology, even though the biological significance of angiogenin is uncertain due to weak catalytic activity of the protein. It has a significant critical role in angiogenesis. Angiogenin transported to the nucleus after being endocytosed by endothelial cell, where it was built up in the nucleolus and is a normal constituent of the circulation, rarely undergoes proliferation and promotes neovascularization. In blood angiogenin, levels increase in some physiological and pathological conditions, which may be of a prognostic significance. It also plays an important role in a number of nonmalignant vasculo-proliferative pathological conditions such as inflammatory bowel disease, proliferative diabetic retinopathy, cardiovascular diseases, and rheumatoid arthritis and in malignant diseases such as colorectal, gastric, pancreatic, melanoma, and urothelial cancer lesions. This review article aims to give an overview of the biochemical structure, receptor translocation, physiology, and types of angiogenin, in addition to its main role in pathological states and ultimately it's effect as a beneficial therapeutic approach.

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References

  • Abdel-Rahman AM, El-Sahrigy SA, Bakr SI (2006) A comparative study of two angiogenic factors: vascular endothelial growth factor and angiogenin in induced sputum from asthmatic children in acute attack. Chest 129:266–271

    Article  CAS  PubMed  Google Scholar 

  • Anagnostopoulos A, Eleftherakis-Papaiakovou V, Kastritis E, Tsionos K, Bamias A, Meletis J, Dimopoulos MA, Terpos E (2007) Serum concentrations of angiogenic cytokines in Waldenstrom macroglobulinaemia: the ratio of angiopoietin-1 to angiopoietin-2 and angiogenin correlate with disease severity. Br J Haematol 137:560–568

    Article  CAS  PubMed  Google Scholar 

  • Battegay F (1995) Angiogenesis: mechanistic in therapeutic prospects. J Mol Med 73:333–346

    Article  CAS  PubMed  Google Scholar 

  • Bicknell R, Vallee BL (1988) Angiogenin activates endothelial cell phospholipase C. Proc Natl Acad Sci U S A 85:5961–5965

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bodner-Adler B, Hefler L, Bodner K, Leodolter S, Frischmuth K, Kainz C, Mayerhofer K (2001) Serum levels of angiogenin (ANG) in invasive cervical cancer and in cervical intraepithelial neoplasia (CIN). Anticancer Res 21:809–812

    CAS  PubMed  Google Scholar 

  • Brieny E, Andrews D, Caccamo M, Chen Y, Clarke L, Coated G, Cox T, Cunningham F, Curwen V, Cutts T, Down T, Durbin R, Fernandez-Suarez XM, Flicek P, Graf S, Hammond M, Herrero J, Howe K, Iyer V, Jekosch K, Kahari A et al (2006) Ensembl Nucleic Acids Res 34:556–561

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Campo L, Turley H, Han C, Pezzella F, Gatter KC, Harris AL, Fox SB (2005) Angiogenin is up-regulated in the nucleus and cytoplasm in human primary breast carcinoma and is associated with markers of hypoxia but not survival. J Pathol 205:585–591

    Article  CAS  PubMed  Google Scholar 

  • Chiarelli F, Pomilio M, Mohn A, Tumini S, Verrotti A, Mezzetti A, Cipollone F, Wasniewska M, Morgese G, Spagnoli A (2002) Serum angiogenin concentrations in young patients with diabetes mellitus. Eur J Clin Invest 32:110–114

    Article  CAS  PubMed  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 85:208–220

    Article  CAS  PubMed  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 46:11810–11818

    Article  CAS  PubMed  Google Scholar 

  • Denekamp J (1992) Angiogenesis, neovascular proliferation and vascular pathophysiology as targets for cancer therapy. Br IRadiol 66:181–196

    Google Scholar 

  • Denekamp J, Hobson B (1982) Endothelial cell proliferation in experimental tumors. Br Cancer 46:711–720

    Article  CAS  Google Scholar 

  • Eberle K, Oberpichler A, Trantakis C, Krupp W, Knupfer M, Tschesche H, Seifert V (2000) The expression of angiogenin in tissue samples of different brain tumours and cultured glioma cells. Anticancer Res 20:1679–1684

    CAS  PubMed  Google Scholar 

  • Eppenberger U, Kueng W, Schlaeppi JM, Roesel JL, Benz C, Mueller H, Matter A, Zuber M, Luescher K, Litschgi M, Schmitt M, Foekens JA, Eppenberger-Castori S (1998) Markers of tumor angiogenesis and proteolysis independently define high- and low-risk subsets of node-negative breast cancer patients. J Clin Oncol 16:3129–3136

    CAS  PubMed  Google Scholar 

  • Etoh T, Shibuta, Barnard GF, Kitano S, Mori M (2000) Angiogenin expression in human colorectal cancer: the role of focal macrophage infiltration. Clin Cancer Res 6:3545–3551

    CAS  PubMed  Google Scholar 

  • Fett JW, Strydom DJ, Lobb RR, Aderman EM, Bethune JL, Riordan JF, Vallee BL (1985) Isolation and characterization of angiogenin, an angiogenic protein from human carcinoma cells. Biochemistry 24:5480–5486

    Article  CAS  PubMed  Google Scholar 

  • Forooghian F, Das B (2007) Anti-angiogenic effects of ribonucleic acid interference targeting vascular endothelial growth factor and hypoxia-inducible factor-1alpha. Am J Ophthalmol 144:61–68

    Article  Google Scholar 

  • Fu X, Kamps MP (1997) E2a-Pbx 1 induces aberrant expression of tissue-specific and developmentally regulated genes when expressed in NIH3T3 fibroblasts. Mol Cell Biol 17:1503–1512

    PubMed Central  CAS  PubMed  Google Scholar 

  • Fu X, Roberts WG, Nobile V, Shapiro R, Kamps MP (1999) mAngiogenin-3, a target gene of oncoprotein E2a-Pbx1, encodes anew angiogenic member of the angiogenin family. Growth Factors 17:125–137

    Article  CAS  PubMed  Google 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 1:33–40

    Article  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, Hardiman O (2006) ANG mutations segregate with familial and ‘sporadic’ amyotrophic lateral sclerosis. Nat Genet 38:411–413

    Article  CAS  PubMed  Google Scholar 

  • Hartmann A, Kunz M, Kostlin S, Gillitzer R, Toksoy A, Brocker EB, Klein C (1999) Hypoxia-induced up-regulation of angiogenin in human malignant melanoma. Cancer Res 59:1578–1583

    CAS  PubMed  Google Scholar 

  • Hayashi K, Yanagihara T, Hata T (2000) Serum angiogenin levels during menstrual cycle and pregnancy. Gynecol Obstet Invest 501:7–12

    Article  Google Scholar 

  • Heldin CH (1995) Dimerization of cell surface receptors in signal transduction. Cell 80:213–223

    Article  CAS  PubMed  Google Scholar 

  • Hisai H, Kato J, Kobune M, Murakami T, Miyanishi K, Takahashi M, Yoshizaki N, Takimoto R, Terui T, Niitsu Y (2003) Increased expression of angiogenin in hepatocellular carcinoma in correlation with tumor vascularity. Clin Cancer Res 9:4852–4859

    CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Hooper L, Stappenbeck TS, Hong CV, Gordon JI (2003) Angiogenins: a new class of microbial proteins involved in innate immunity. Nat Immunol 4:269–273

    Article  CAS  PubMed  Google Scholar 

  • Hu G-F (1997) Limited proteolysis of angiogenin by elastase is regulated by plasminogen. J Protein Chem 16:669–679

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hu G-F, Riordan JF (1993) Angiogenin enhances actin acceleration in plasminogen. Biochem Biophys Res Commun 197:682–687

    Article  CAS  PubMed  Google Scholar 

  • Hu G-F, Strydom DJ, Fett JW, Riordan J, Vallee BL (1993) Actin is binding protein for angiogenin. Proc Natl Acad Sci 90(4):1217–1221

    Google Scholar 

  • Hu GF, Riordan JF, Vallee BL (1994) Angiogenin promotes invasiveness of cultured endothelial cells by stimulation of cell associated proteolytic activities. Proc Natl Acad Sci U S A 61:12096–12100

    Article  Google Scholar 

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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hu GF, Gao X, Sun Y, Zhou J, Yang M, Xu Z (2005) Alpha-actinin-2, a cytoskeletal protein, binds to agiogenin. Bioch Biophys Res Commun 329:661–667

    Article  CAS  Google Scholar 

  • Jang SH, Kang DK, Chang SI, Scheraga HA, Shin HC (2004) High level production of bovine angiogenin in E. coli by an efficient refolding procedure. Biotechnol Lett 26(150):1–4

    Google Scholar 

  • Jimi S, Ito K, Kohno K, Ono M, Kuwano M, Itagaki Y, Ishikawa H (1995) Modulation by bovine angiogenin of tubular morphogenesis and expression of plasminogen activator in bovine endothelial cells. Biochem Biophys Res Commun 211:476–483

    Article  CAS  PubMed  Google Scholar 

  • Kao RY, 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 U S A 15:10066–10071

    Article  Google Scholar 

  • King TV, Vallee BL (1991a) Neovascularisation of the meniscus with angiogenin. An experimental study in rabbits. J Bone Joint Surg Br 4:587–590

    Google Scholar 

  • King TV, Vallee BL (1991b) Neovascularisation of the meniscus with angiogenin. An experimental study in rabbits. J Bone Joint Surg Br 73:587–590

    CAS  PubMed  Google Scholar 

  • Kolben M, Bläser J, Ulm K, Schmitt M, Schneider KT, Tschesche H, Graeff H (1997) Angiogenin plasma levels during pregnancy. Am J Obstet Gynecol 176:37–41

    Article  CAS  PubMed  Google Scholar 

  • Kurachi K, Davie EW, Strydom DJ, Riordran JF, Vallee BL (1985a) Sequence of the c DNA and gene for angiogenin a human angiogenesis factor. Biochemistry 24:5494–5499

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Lassus P, Teramo K, Nupponen I, Markkanen H, Cederqvist K, Andersson S (2003) Vascular endothelial growth factor and angiogenin levels during fetal development and in maternal diabetes. Biol Neonate 84:287–292

    Article  CAS  PubMed  Google Scholar 

  • Li D, Bell J, Brown A, Berry CL (1994) The observation of angiogenin and basic fibroblast growth factor gene expression in human colonic adenocarcinomas, gastric adenocarcinomas, and hepatocellular carcinomas. J Pathol 172:171–175

    Article  CAS  PubMed  Google Scholar 

  • Maes P, Damart D, Rommens C, Montreuil J, Spik G, Tartar A (1988) The complete amino acid sequence of bovine milk angiogenin. FEBS Lett 241:41–45

    Article  CAS  PubMed  Google Scholar 

  • Malamitsi-Puchner A, Sarandakou A, Dafogianni C, Tziotis J, Bartsocas CS (1998) Serum angiogenin levels in children and adolescents with insulin-dependent diabetes mellitus. Pediatr Res 43:798–800

    Article  CAS  PubMed  Google Scholar 

  • Martin A, Komada MR, Sane DC (2003) Abnormal angiogenesis in diabetes mellitus. Med Res Rev 23:117–145

    Article  CAS  PubMed  Google Scholar 

  • Mignatti P, Robbins E, Rifkin DB (1997) Tumour invasion through the human amniotic membrane: requirement for a proteinase cascade. Cell 47:487–498

    Article  Google Scholar 

  • Miyake H, Hara I, Yamanaka K, Gohji K, Arakawa S, Kamidono S (1999) Increased angiogenin expression in the tumor tissue and serum of urothelial carcinoma patients is related to disease progression and recurrence. Cancer 86:316–324

    Article  CAS  PubMed  Google Scholar 

  • Molica S, Vitelli G, Levato D, Giannarelli D, Vacca A, Cuneo A, Ribatti D, Digiesi G (2004) Serum angiogenin is not elevated in patients with early B-cell chronic lymphocytic leukemia but is prognostic factor for disease progression. Eur J Haematol 73(1):36–42

    Article  CAS  PubMed  Google Scholar 

  • Montero S, Guzman C, Cortes-Funes H, Colomer R (1998) Angiogenin expression and prognosis in primary breast carcinoma. Clin Cancer Res 4:2161–2168

    CAS  PubMed  Google Scholar 

  • Montesano R, Pepper MS, Vassalli J-D, Orci L (1987) Phorbol ester induces cultured endothelial cells to invade a fibrin matrix in the presence of fibrinolytic inhibitors. J Cell Physiol 132:509–516

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Musolino C, Calabrò L, Bellomo G, Cincotta M, Di Giacomo V, Pezzano C, Loteta B, Rizzo V, Guglielmo S, Alonci A (2002) Lipid profile in hematologic neoplasms. Recenti Prog Med 93:298–301

    PubMed  Google Scholar 

  • Musolino C, Alonci A, Bellomo G, Loteta B, Quartarone E, Gangemi D, Massara E, Calabro L (2004) Levels of soluble angiogenin in chronic myeloid malignancies: clinical implications. Eur J Haematol 72:416–419

    Article  CAS  PubMed  Google Scholar 

  • Nakamura M, Yamabe H, Osawa H, Nakamura N, Shimada M, Kumasaka R, Murakami R, Fujita T, Osanai T, Okumura K (2006) Hypoxic conditions stimulate the production of angiogenin and vascular endothelial growth factor by human renal proximal tubular epithelial cells in culture. Nephrol Dial Transplant 6:1489–1495

    Article  Google Scholar 

  • Nobile V, Vallee BL, Shapiro R (1996) Characterization of mouse angiogenin-related protein: implication for functional studies on angiogenin. Proc Natl Acad Sci U S A 93:4331–4335

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ozaki H, Hayashi H, Oshima K (1996) Angiogenin levels in the vitreous from patients with proliferative diabetic retinopathy. Ophthalmic Res 28:356–360

    Article  CAS  PubMed  Google Scholar 

  • Pantsulaia I, Trofimov S, Kobyliansky E, Livshits G (2006) Genetic and environmental determinants of circulating levels of angiogenin in community-based sample. Clin Endocrin 64:271–279

    Article  CAS  Google Scholar 

  • Passam FH, Alexandrakis MG, Moschandrea J, Sfiridaki A, Roussou PA, Siafakas NM (2006) Angiogenic molecules in Hodgkin's disease: results from sequential serum analysis. Int J Immunopathol Pharmacol 19:161–170

    CAS  PubMed  Google 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 6:317–330

    Article  PubMed Central  CAS  PubMed  Google 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 62:159–166

    Article  CAS  PubMed  Google Scholar 

  • Rajashekhar G, Loganath A, Roy AC, Chong SS, Wong YC (2005a) Extracellular matrix-dependent regulation of angiogenin expression in human placenta. J Cell Biochem 96:36–46

    Article  CAS  PubMed  Google Scholar 

  • Rajashekhar G, Loganath A, Roy AC, Chong SS, Wong Y (2005b) Hypoxia up-regulated angiogenin and down-regulated vascular cell adhesionmolecule-1 expression and secretion in human placental trophoblasts. J Soc Gynecol Investig 12:310–319

    Article  CAS  PubMed  Google Scholar 

  • Shaarawy M, Al-Sokkary F, Sheba M, Wahba O, Kandil HO, Abdel-Mohsen I (2005) Angiogenin and vascular endothelial growth factor in pregnancies complicated by preeclampsia. Int J Gynaecol Obstet 88:112–117

    Article  CAS  PubMed  Google Scholar 

  • Shapiro R, Strydom DJ, Olson KA, Vallee BL (1987) Isolation of angiogenin from normal human plasma. Biochemistry 26:5141–5146

    Article  CAS  PubMed  Google Scholar 

  • Sheen-Chen SM, Eng HL, Chen WJ, Chou FF, Chen HS (2000) Serum level of angiogenin in breast cancer. Anticancer Res 20:4769–4771

    CAS  PubMed  Google Scholar 

  • Shimoyama S, Gansauge F, Gansauge S, Negri G, Oohara T, Beger HG (1996) Increased angiogenin expression in pancreatic cancer is related to cancer aggressiveness. Cancer Res 56:2703–2706

    CAS  PubMed  Google Scholar 

  • Shimoyama S, Yamasaki K, Kawahara M, Kaminishi M (1999) Increased serum angiogenin concentration in colorectal cancer is correlated with cancer progression. Clin Cancer Res 5:1125–1130

    CAS  PubMed  Google Scholar 

  • Soncin F, Strydom DJ, Shapiro R (1997) Interaction of heparin with human angiogenin. J Biol Chem 272:9818–9824

    Article  CAS  PubMed  Google Scholar 

  • Stappenbeck TS, Hooper LV, Gordon JI (2002) Developmental regulation of intestinal angiogenesis by indigenous microbes via Paneth cells. Proc Natl Acad Sci 99(24):15451–15155

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Strydom DJ, Fett JW, Lobb RR, Alderman EM, Bethune JL, Riordan JF, Vallee BL (1985) Amino acid sequence of human tumor derived angiogenin. Biochemistry 24:5486–5494

    Article  CAS  PubMed  Google Scholar 

  • Subramanian V, Crabtree B, Acharya KR (2008) Human angiogenin is a neuroprotective factor and amyotrophic lateral sclerosis associated angiogenin variants affect neurite extension/pathfinding and survival of motor neurons. Hum Mol Genet 17:130–149

    Article  CAS  PubMed  Google Scholar 

  • Suzumori N, Zhao XX, Suzumori K (2004) Elevated angiogenin levels in the peritoneal fluid of women with endometriosis correlate with the extent of the disorder. Fertil Steril 82:93–96

    Article  CAS  PubMed  Google Scholar 

  • Tas F, Duranyildiz D, Oguz H, Camlica H, Yasasever V, Topuz E (2006) Circulating serum levels of angiogenic factors and vascular endothelial growth factor receptors 1 and 2 in melanoma patients. Melanoma Res 16:405–411

    Article  CAS  PubMed  Google Scholar 

  • Tello-Montoliu A, Patel JV, Lip GYH (2006) Angiogenin: a review of the pathophysiology and potential clinical applications. J Thromb Haemost 4(9):1864–1874

    Article  CAS  PubMed  Google Scholar 

  • Tello-Montoliu A, Marín F, Patel J, Roldán V, Mainar L, Vicente Vicente V, Sogorb F, Lip GYH (2007) Plasma angiogenin levels in acute coronary syndromes: implications for prognosis. Eur Heart J 28:2006–3011

    Article  Google Scholar 

  • Ugurel S, Rappl G, Tilgen W, Reinhold U (2001) Increased serum concentration of angiogenic factors in malignant melanoma patients correlates with tumor progression and survival. J Clin Oncol 19:577–583

    CAS  PubMed  Google Scholar 

  • Vallee BL, Riordan JF (1997) Organogenesis and angiogenin. Cell Mol Life Sci 53:803–815

    Article  CAS  PubMed  Google Scholar 

  • Verstovsek S, Kantarjian H, Aguayo A, Manshouri T, Freireich E, Keating M, Estey E, Albitar M (2001) Significance of angiogenin plasma concentrations in patients with acute myeloid leukaemia and advanced myelodysplastic syndrome. B J Haematol 114:290–295

    Article  CAS  Google Scholar 

  • Zhao XY, Hu SJ, Li J, Mou Y, Chan CF, Jin J, Sun J, Zhu ZH (2006) RAAV-mediated angiogenin gene transfer induces angiogenesis and modifies left ventricular remodeling in rats with myocardial infarction. J Mol Med 84:1033–1146

    Article  CAS  PubMed  Google Scholar 

  • Ziche M, Morbidelli L, Donnini S (1996) Angiogenesis. Exp Nephrol 4:1–14

    CAS  PubMed  Google Scholar 

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Idriss, N.K., Sayed, S., Zakhary, M.M. et al. Relationship of angiogenin to pathophysiology of diseases. Comp Clin Pathol 24, 229–239 (2015). https://doi.org/10.1007/s00580-013-1837-y

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