Angiogenin interacts with the plasminogen activation system at the cell surface of breast cancer cells to regulate plasmin formation and cell migration

Molecular Oncology

Volumn 8, Issue 3, 2014, Pages 483-507

  Dutta, Sujoy ^a   Bandyopadhyay, Chirosree ^a   Bottero, Virginie ^a   Veettil, Mohanan V ^a   Wilson, Lydia ^a   Pins, Michael R ^b   Johnson, Karen E ^a   Warshall, Case ^a   Chandran, Bala ^a  

^a ROSALIND FRANKLIN UNIVERSITY OF MEDICINE AND SCIENCE   (United States)

^b ADVOCATE LUTHERAN GENERAL HOSPITAL   (United States)

Author keywords

Angiogenin; Breast cancer; Cell migration; Plasmin; Plasminogen activation system

Indexed keywords

ANGIOGENIN; LIPOCORTIN; LIPOCORTIN 2; MONOCLONAL ANTIBODY; PLASMIN; PROTEIN TYROSINE KINASE; UROKINASE RECEPTOR; PANCREATIC RIBONUCLEASE; PLASMINOGEN; UROKINASE;

ARTICLE; BREAST CANCER; BREAST METASTASIS; CANCER CELL; CELL MEMBRANE; CELL MIGRATION; CELL SURFACE; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; INTRADUCTAL CARCINOMA; LIPID RAFT; PLASMINOGEN ACTIVATION; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN PHOSPHORYLATION; TUMOR INVASION; BREAST; BREAST TUMOR; CELL MOTION; FEMALE; METABOLISM; PATHOLOGY; PROTEIN PROTEIN INTERACTION; TUMOR CELL LINE;

BREAST; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL MOVEMENT; FEMALE; HUMANS; NEOPLASM INVASIVENESS; PLASMINOGEN; PROTEIN INTERACTION MAPS; RECEPTORS, UROKINASE PLASMINOGEN ACTIVATOR; RIBONUCLEASE, PANCREATIC; UROKINASE-TYPE PLASMINOGEN ACTIVATOR;

EID: 84899491385     PISSN: 15747891     EISSN: 18780261     Source Type: Journal    
DOI: 10.1016/j.molonc.2013.12.017     Document Type: Article

References (69)

1. Akula S.M., Pramod N.P., Wang F.Z., Chandran B. Integrin alpha3beta1 (CD 49c/29) is a cellular receptor for Kaposi's sarcoma-associated herpesvirus (KSHV/HHV-8) entry into the target cells. Cell 2002, 108:407-419.
2. Andreasen P.A., Egelund R., Petersen H.H. The plasminogen activation system in tumor growth, invasion, and metastasis. Cell. Mol. Life Sci. 2000, 57:25-40.
3. Bharadwaj A., Bydoun M., Holloway R., Waisman D. Annexin A2 heterotetramer: structure and function. Int. J. Mol. Sci. 2013, 14:6259-6305.
4. Campo L., Turley H., Han C., Pezzella F., Gatter K.C., Harris A.L., Fox S.B. 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. 2005, 205:585-591.
5. Carriero M.V., Del Vecchio S., Capozzoli M., Franco P., Fontana L., Zannetti A., Botti G., D'Aiuto G., Salvatore M., Stoppelli M.P. Urokinase receptor interacts with alpha(v)beta5 vitronectin receptor, promoting urokinase-dependent cell migration in breast cancer. Cancer Res. 1999, 59:5307-5314.
6. Chakraborty S., ValiyaVeettil M., Sadagopan S., Paudel N., Chandran B. c-Cbl-mediated selective virus-receptor translocations into lipid rafts regulate productive Kaposi's sarcoma-associated herpesvirus infection in endothelial cells. J.Virol. 2011, 85:12410-12430.
7. Chakraborty S., Veettil M.V., Bottero V., Chandran B. Kaposi's sarcoma-associated herpesvirus interacts with EphrinA2 receptor to amplify signaling essential for productive infection. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:E1163-E1172.
8. Chandrasekaran E.V., Davidson E.A. Glycosaminoglycans of normal and malignant cultured human mammary cells. Cancer Res. 1979, 39:870-880.
9. Cho G.W., Kang B.Y., Kim S.H. Human angiogenin presents neuroprotective and migration effects in neuroblastoma cells. Mol. Cell. Biochem. 2010, 340:133-141.
10. Cunningham O., Andolfo A., Santovito M.L., Iuzzolino L., Blasi F., Sidenius N. Dimerization controls the lipid raft partitioning of uPAR/CD87 and regulates its biological functions. EMBO J. 2003, 22:5994-6003.
11. Deng S., Wang J., Hou L., Li J., Chen G., Jing B., Zhang X., Yang Z. Annexin A1, A2, A4 and A5 play important roles in breast cancer, pancreatic cancer and laryngeal carcinoma, alone and/or synergistically. Oncol. Lett. 2013, 5:107-112.
12. Du D., Xu F., Yu L., Zhang C., Lu X., Yuan H., Huang Q., Zhang F., Bao H., Jia L., Wu X., Zhu X., Zhang X., Zhang Z., Chen Z. The tight junction protein, occludin, regulates the directional migration of epithelial cells. Dev. Cell 2010, 18:52-63.
13. Estreicher A., Mühlhauser J., Carpentier J.L., Orci L., Vassalli J.D. The receptor for urokinase type plasminogen activator polarizes expression of the protease to the leading edge of migrating monocytes and promotes degradation of enzyme inhibitor complexes. J.Cell Biol. 1990, 111:783-792.
14. Fett J.W., Strydom D.J., Lobb R.R., Alderman E.M., Bethune J.L., Riordan J.F., Vallee B.L. Isolation and characterization of angiogenin, an angiogenic protein from human carcinoma cells. Biochemistry 1985, 24:5480-5486.
15. Forejtnikovà H., Vieillevoye M., Zermati Y., Lambert M., Pellegrino R.M., Guihard S., Gaudry M., Camaschella C., Lacombe C., Roetto A., Mayeux P., Verdier F. Transferrin receptor 2 is a component of the erythropoietin receptor complex and is required for efficient erythropoiesis. Blood 2010, 116:5357-5367.
16. Fu H., Feng J., Liu Q., Sun F., Tie Y., Zhu J., Xing R., Sun Z., Zheng X. Stress induces tRNA cleavage by angiogenin in mammalian cells. FEBS Lett. 2009, 583:437-442.
17. Gupta S.K., Haigh B.J., Griffin F.J., Wheeler T.T. The mammalian secreted RNases: mechanisms of action in host defence. Innate Immun. 2013, 19:86-97.
18. Hallahan T.W., Shapiro R., Vallee B.L. Dual site model for the organogenic activity of angiogenin. Proc. Natl. Acad. Sci. U. S. A. 1991, 88:2222-2226.
19. Hildenbrand R., Schaaf A. The urokinase-system in tumor tissue stroma of the breast and breast cancer cell invasion. Int. J. Oncol. 2009, 34:15-23.
20. Hu G.F. Limited proteolysis of angiogenin by elastase is regulated by plasminogen. J.Protein Chem. 1997, 16:669-679.
21. Hu G.F., Riordan J.F. Angiogenin enhances actin acceleration of plasminogen activation. Biochem. Biophys. Res. Commun. 1993, 197:682-687.
22. Hu G.F., Strydom D.J., Fett J.W., Riordan J.F., Vallee B.L. Actin is a binding protein for angiogenin. Proc. Natl. Acad. Sci. U. S. A. 1993, 90:1217-1221.
23. Hu G., Riordan J.F., Vallee B.L. Angiogenin promotes invasiveness of cultured endothelial cells by stimulation of cell-associated proteolytic activities. Proc. Natl. Acad. Sci. U. S. A. 1994, 91:12096-12100.
24. Hu G.F., Riordan J.F., Vallee B.L. A putative angiogenin receptor in angiogenin-responsive human endothelial cells. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:2204-2209.
25. Ito Y., Arai K., Nozawa R., Yoshida H., Higashiyama T., Takamura Y., Miya A., Kobayashi K., Kuma K., Miyauchi A. S100A10 expression in thyroid neoplasms originating from the follicular epithelium: contribution to the aggressive characteristic of anaplastic carcinoma. Anticancer Res. 2007, 27:2679-2683.
26. Ivanov P., Emara M.M., Villen J., Gygi S.P., Anderson P. Angiogenin-induced tRNA fragments inhibit translation initiation. Mol. Cell 2011, 43:613-623.
27. Jardine A.M., Leonidas D.D., Jenkins J.L., Park C., Raines R.T., Acharya K.R., Shapiro R. Cleavage of 3',5'-pyrophosphate-linked dinucleotides by ribonuclease A and angiogenin. Biochemistry 2001, 40:10262-10272.
28. Jones M.L., Ewing C.M., Isaacsa W.B., Getzenberg R.H. Prostate cancer-derived angiogenin stimulates the invasion of prostate fibroblasts. J.Cell. Mol. Med. 2012, 16:193-201.
29. Kwaan H.C., McMahon B. The role of plasminogen-plasmin system in cancer. Cancer Treat. Res. 2009, 148:43-66.
30. Kwon M., Yoon C.S., Jeong W., Rhee S.G., Waisman D.M. Annexin A2-S100A10 heterotetramer, a novel substrate of thioredoxin. J.Biol. Chem. 2005, 280:23584-23592.
31. Leuchowius K.,J., Weibrecht I., Söderberg O. In situ proximity ligation assay for microscopy and flow cytometry. Curr. Protoc. Cytom. 2011, 56. 9.36.1--9.36.15. (Chapter 9:Unit 9.36).
32. Li S., Hu G.F. Angiogenin-mediated rRNA transcription in cancer and neurodegeneration. Int. J. Biochem. Mol. Biol. 2010, 1:26-35.
33. Li S., Hu G.F. Emerging role of angiogenin in stress response and cell survival under adverse conditions. J.Cell. Physiol 2012, 227:2822-2826.
34. McCahill L.E., Single R., Ratliff J., Sheehey-Jones J., Gray A., James T. Local recurrence after partial mastectomy: relation to initial surgical margins. Am. J. Surg. 2011, 3:374-378.
35. McCahill L.E., Single R.M., Aiello Bowles E.J., Feigelson H.S., James T.A., Barney T., Engel J.M., Onitilo A.A. Variability in reexcision following breast conservation surgery. JAMA 2012, 5:467-475.
36. Montero S., Guzmán C., Cortés-Funes H., Colomer R. Angiogenin expression and prognosis in primary breast carcinoma. Clin. Cancer Res. 1998, 4:2161-2168.
37. Moroianu J., Riordan J.F. Identification of the nucleolar targeting signal of human angiogenin. Biochem. Biophys. Res. Commun. 1994, 203:1765-1772.
38. Murphy C.S., Pink J.J., Jordan V.C. Characterization of a receptor-negative, hormone-nonresponsive clone derived from a T47D human breast cancer cell line kept under estrogen-free conditions. Cancer Res. 1990, 50:7285-7292.
39. Nielsen L.S., Hansen J.G., Skriver L., Wilson E.L., Kaltoft K., Zeuthen J., Danø K. Purification of zymogen to plasminogen activator from human glioblastoma cells by affinity chromatography with monoclonal antibody. Biochemistry 1982, 21:6410-6415.
40. Nilsson U.W., Abrahamsson A., Dabrosin C. Angiogenin regulation by estradiol in breast tissue: tamoxifen inhibits angiogenin nuclear translocation and antiangiogenin therapy reduces breast cancer growth invivo. Clin. Cancer Res. 2010, 16:3659-3669.
41. Pan X., Xiong D., Yao X., Xin Y., Zhang L., Chen J. Up-regulating ribonuclease inhibitor inhibited epithelial-to-mesenchymal transition and metastasis in murine melanoma cells. Int. J. Biochem. Cell Biol. 2012, 44:998-1008.
42. Paudel N., Sadagopan S., Balasubramanian S., Chandran B. Kaposi's sarcoma-associated herpesvirus latency-associated nuclear antigen and angiogenin interact with common host proteins, including annexin A2, which is essential for survival of latently infected cells. J.Virol. 2012, 86:1589-1607.
43. Piccoli R., Olson K.A., Vallee B.L., Fett J.W. Chimeric anti-angiogenin antibody cAb 26-2F inhibits the formation of human breast cancer xenografts in athymic mice. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:4579-4583.
44. Pizzo E., Sarcinelli C., Sheng J., Fusco S., Formiggini F., Netti P., Yu W., D'Alessio G., Hu G.F. Ribonuclease/angiogenin inhibitor 1 regulates stress-induced subcellular localization of angiogenin and controls its growth and survival activities. J.Cell Sci. 2013, 126:4308-4319.
45. Pyatibratov M.G., Tolkatchev D., Plamondon J., Xu P., Ni F., Kostyukova A.S. Binding of human angiogenin inhibits actin polymerization. Arch. Biochem. Biophys. 2010, 495:74-81.
46. Rao J.S. Molecular mechanisms of glioma invasiveness: the role of proteases. Nat. Rev. Cancer 2003, 3:489-501.
47. Rescher U., Gerke V. S100A10/p11: family, friends and functions. Pflugers Arch. Eur. J. Physiol. 2008, 455:575-582.
48. Rose H.N., McGrath C.M. Alpha-lactalbumin production in human mammary carcinoma. Science 1975, 190:673-675.
49. Sadagopan S., Sharma-Walia N., Veettil M.V., Bottero V., Levine R., Vart R.J., Chandran B. Kaposi's sarcoma-associated herpesvirus upregulates angiogenin during infection of human dermal microvascular endothelial cells, which induces 45S rRNA synthesis, antiapoptosis, cell proliferation, migration, and angiogenesis. J.Virol. 2009, 83:3342-3364.
50. Sadagopan S., Valiya Veettil M., Paudel N., Bottero V., Chandran B. Kaposi's sarcoma-associated herpesvirus-induced angiogenin plays roles in latency via the phospholipase C gamma pathway: blocking angiogenin inhibits latent gene expression and induces the lytic cycle. J.Virol. 2011, 85:2666-2685.
51. Sadagopan S., Veettil M.V., Chakraborty S., Sharma-Walia N., Paudel N., Bottero V., Chandran B. Angiogenin functionally interacts with p53 and regulates p53-mediated apoptosis and cell survival. Oncogene 2012, 31:4835-4847.
52. Schroeck F., Arroyo de Prada N., Sperl S., Schmitt M., Viktor M. Interaction of plasminogen activator inhibitor type-1 (PAI-1) with vitronectin (Vn): mapping the binding sites on PAI-1 and Vn. Biol. Chem. 2002, 383:1143-1149.
53. Shapiro R., Vallee B.L. Site-directed mutagenesis of histidine-13 and histidine-114 of human angiogenin. Alanine derivatives inhibit angiogenin-induced angiogenesis. Biochemistry 1989, 28:7401-7408.
54. Shapiro R., Riordan J.F., Vallee B.L. Characteristic ribonucleolytic activity of human angiogenin. Biochemistry 1986, 25:3527-3532.
55. Smith H.W., Marshall C.J. Regulation of cell signalling by uPAR. Nat. Rev. Mol. Cell Biol. 2010, 11:23-36.
56. Söderberg O., Gullberg M., Jarvius M., Ridderstråle K., Leuchowius K.,J., Jarvius J., Wester K., Hydbring P., Bahram F., Larsson L.,G., Landegren U. Direct observation of individual endogenous protein complexes in situ by proximity ligation. Nat. Methods 2006, 3:995-1000.
57. Tello-Montoliu A., Patel J.V., Lip G.Y. Angiogenin: a review of the pathophysiology and potential clinical applications. J.Thromb. Haemost. 2006, 4:1864-1874.
58. Tsuji T., Sun Y., Kishimoto K., Olson K.A., Liu S., Hirukawa S., Hu G.F. Angiogenin is translocated to the nucleus of HeLa cells and is involved in ribosomal RNA transcription and cell proliferation. Cancer Res. 2005, 65:1352-1360.
59. Vergiliana J.F., Asokananthan N., Stewart G.A. Activation of the plasma kallikrein-kinin system on human lung epithelial cells. Biol. Chem. 2010, 391:1067-1077.
60. Vicente-Manzanares M., Choi C.K., Horwitz A.R. Integrins in cell migration-the actin connection. J.Cell Sci. 2009, 122:199-206.
61. Walen K.H., Stampfer M.R. Chromosome analyses of human mammary epithelial cells at stages of chemical-induced transformation progression to immortality. Cancer Genet. Cytogenet. 1989, 37:249-261.
62. Wei Y., Eble J.A., Wang Z., Kreidberg J.A., Chapman H.A. Urokinase receptors promote beta1 integrin function through interactions with integrin alpha3beta1. Mol. Biol. Cell 2001, 12:2975-2986.
63. Wei S., Gao X., Du J., Su J., Xu Z. Angiogenin enhances cell migration by regulating stress fiber assembly and focal adhesion dynamics. PLoS ONE 2011, 6:e28797.
64. Willmarth N.E., Albertson D.G., Ethier S.P. Chromosomal instability and lack of cyclin E regulation in hCdc4 mutant human breast cancer cells. Breast Cancer Res. 2004, 6:R531-R539.
65. Xu Z.P., Tsuji T., Riordan J.F., Hu G.F. The nuclear function of angiogenin in endothelial cells is related to rRNA production. Biochem. Biophys. Res. Commun. 2002, 294:287-292.
66. Yamasaki S., Ivanov P., Hu G.F., Anderson P. Angiogenin cleaves tRNA and promotes stress-induced translational repression. J.Cell Biol. 2009, 185:35-42.
67. Yang X., Popescu N.C., Zimonjic D.B. DLC1 interaction with S100A10 mediates inhibition of invitro cell invasionand tumorigenicity of lung cancer cells through a RhoGAP-independent mechanism. Cancer Res. 2011, 71:2916-2925.
68. Yang T., Peng H., Wang J., Yang J., Nice E.C., Xie K., Huang C. Prognostic and diagnostic significance of annexin A2 in colorectal cancer. Colorectal Dis. 2013, 15:e373-e381.
69. Yao X., Li D., Xiong D.M., Li L., Jiang R., Chen J.X. A novel role of ribonuclease inhibitor in regulation of epithelial-to-mesenchymal transition and ILK signaling pathway in bladder cancer cells. Cell Tissue Res. 2013, 353:409-423.