Ferritin blocks inhibitory effects of two-chain high molecular weight kininogen (HKa) on adhesion and survival signaling in endothelial cells

PLoS ONE

Volumn 7, Issue 7, 2012, Pages

  Tesfay, Lia ^a,b   Huhn, Annissa J ^a   Hatcher, Heather ^a   Torti, Frank M ^a,b   Torti, Suzy V ^a,b  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FERRITIN; FERRITIN H; FERRITIN L; FOCAL ADHESION KINASE; HIGH MOLECULAR WEIGHT KININOGEN; IRON BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; PAXILLIN; PROTEIN KINASE B; UNCLASSIFIED DRUG; UROKINASE RECEPTOR; VERY LATE ACTIVATION ANTIGEN 5; FOCAL ADHESION KINASE 1; PTK2 PROTEIN, HUMAN;

ANIMAL TISSUE; ANTIANGIOGENIC ACTIVITY; APOPTOSIS; ARTICLE; CELL ADHESION; CELL PROLIFERATION; CELL PROTECTION; CELL SPREADING; CELL SURVIVAL; CELL VIABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME ACTIVATION; HUMAN; HUMAN CELL; IN VIVO STUDY; INTRACELLULAR SIGNALING; MOUSE; NONHUMAN; PROTEIN DOMAIN; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; METABOLISM; PHYSIOLOGY; PROTEIN DEGRADATION; SIGNAL TRANSDUCTION; UMBILICAL VEIN ENDOTHELIAL CELL;

AMINO ACID MOTIFS; CELL ADHESION; CELL SURVIVAL; FERRITINS; FOCAL ADHESION KINASE 1; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; INTEGRIN ALPHA5BETA1; KININOGEN, HIGH-MOLECULAR-WEIGHT; MAP KINASE SIGNALING SYSTEM; PAXILLIN; PROTEOLYSIS; PROTO-ONCOGENE PROTEINS C-AKT;

EID: 84863628119     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0040030     Document Type: Article

References (44)

1. Folkman J, (2003) Fundamental concepts of the angiogenic process. Curr Mol Med 3: 643-651.
2. Rajappa M, Saxena P, Kaur J, (2010) Ocular angiogenesis: mechanisms and recent advances in therapy. Adv Clin Chem 50: 103-121.
3. Kelly RJ, Darnell C, Rixe O, (2010) Target inhibition in antiangiogenic therapy a wide spectrum of selectivity and specificity. Cancer J 16: 635-642.
4. Zins SR, Amare MF, Tadaki DK, Elster EA, Davis TA, (2010) Comparative analysis of angiogenic gene expression in normal and impaired wound healing in diabetic mice: effects of extracorporeal shock wave therapy. Angiogenesis 13: 293-304.
5. Lalmanach G, Naudin C, Lecaille F, Fritz H, (2010) Kininogens: More than cysteine protease inhibitors and kinin precursors. Biochimie 92: 1568-1579.
6. Cyr M, Lepage Y, Blais C Jr, Gervais N, Cugno M, et al. (2001) Bradykinin and des-Arg(9)-bradykinin metabolic pathways and kinetics of activation of human plasma. Am J Physiol Heart Circ Physiol 281: H275-283.
7. Schmaier AH, Wahl R, Fisher SJ, Brenner D, (1998) The pharmacokinetics of the kininogens. Thromb Res 92: 293-297.
8. Guo YL, Colman RW, (2005) Two faces of high-molecular-weight kininogen (HK) in angiogenesis: bradykinin turns it on and cleaved HK (HKa) turns it off. J Thromb Haemost 3: 670-676.
9. Torti FM, Torti SV, (2002) Regulation of ferritin genes and protein. Blood 99: 3505-3516.
10. Leimberg MJ, Prus E, Konijn AM, Fibach E, (2008) Macrophages function as a ferritin iron source for cultured human erythroid precursors. J Cell Biochem 103: 1211-1218.
11. Sibille JC, Kondo H, Aisen P, (1988) Interactions between isolated hepatocytes and Kupffer cells in iron metabolism: a possible role for ferritin as an iron carrier protein. Hepatology 8: 296-301.
12. Gray CP, Franco AV, Arosio P, Hersey P, (2001) Immunosuppressive effects of melanoma-derived heavy-chain ferritin are dependent on stimulation of IL-10 production. Int J Cancer 92: 843-850.
13. Fargion S, Fracanzani AL, Cislaghi V, Levi S, Cappellini MD, et al. (1991) Characteristics of the membrane receptor for human H-ferritin. Curr Stud Hematol Blood Transfus pp. 164-170.
14. Matzner Y, Hershko C, Polliack A, Konijn AM, Izak G, (1979) Suppressive effect of ferritin on in vitro lymphocyte function. Br J Haematol 42: 345-353.
15. Cohen LA, Gutierrez L, Weiss A, Leichtmann-Bardoogo Y, Zhang DL, et al. (2010) Serum ferritin is derived primarily from macrophages through a nonclassical secretory pathway. Blood 116: 1574-1584.
16. Chen TT, Li L, Chung DH, Allen CD, Torti SV, et al. (2005) TIM-2 is expressed on B cells and in liver and kidney and is a receptor for H-ferritin endocytosis. J Exp Med 202: 955-965.
17. Li L, Fang CJ, Ryan JC, Niemi EC, Lebron JA, et al. (2010) Binding and uptake of H-ferritin are mediated by human transferrin receptor-1. Proc Natl Acad Sci U S A 107: 3505-3510.
18. Ruddell RG, Hoang-Le D, Barwood JM, Rutherford PS, Piva TJ, et al. (2009) Ferritin functions as a proinflammatory cytokine via iron-independent protein kinase C zeta/nuclear factor kappaB-regulated signaling in rat hepatic stellate cells. Hepatology 49: 887-900.
19. Coffman LG, Brown JC, Johnson DA, Parthasarathy N, D'Agostino RB Jr, et al. (2008) Cleavage of high-molecular-weight kininogen by elastase and tryptase is inhibited by ferritin. Am J Physiol Lung Cell Mol Physiol 294: L505-515.
20. Coffman LG, Parsonage D, D'Agostino R Jr, Torti FM, Torti SV, (2009) Regulatory effects of ferritin on angiogenesis. Proc Natl Acad Sci U S A 106: 570-575.
21. Parthasarathy N, Torti SV, Torti FM, (2002) Ferritin binds to light chain of human H-kininogen and inhibits kallikrein-mediated bradykinin release. Biochem J 365: 279-286.
22. Guo YL, Wang S, Colman RW, (2001) Kininostatin, an angiogenic inhibitor, inhibits proliferation and induces apoptosis of human endothelial cells. Arterioscler Thromb Vasc Biol 21: 1427-1433.
23. Colman RW, Jameson BA, Lin Y, Johnson D, Mousa SA, (2000) Domain 5 of high molecular weight kininogen (kininostatin) down-regulates endothelial cell proliferation and migration and inhibits angiogenesis. Blood 95: 543-550.
24. Guo YL, Wang S, Cao DJ, Colman RW, (2003) Apoptotic effect of cleaved high molecular weight kininogen is regulated by extracellular matrix proteins. J Cell Biochem 89: 622-632.
25. Baker M, Robinson SD, Lechertier T, Barber PR, Tavora B, et al. (2012) Use of the mouse aortic ring assay to study angiogenesis. Nat Protoc 7: 89-104.
26. Hood JD, Frausto R, Kiosses WB, Schwartz MA, Cheresh DA, (2003) Differential alphav integrin-mediated Ras-ERK signaling during two pathways of angiogenesis. J Cell Biol 162: 933-943.
27. Mavria G, Vercoulen Y, Yeo M, Paterson H, Karasarides M, et al. (2006) ERK-MAPK signaling opposes Rho-kinase to promote endothelial cell survival and sprouting during angiogenesis. Cancer Cell 9: 33-44.
28. Somanath PR, Razorenova OV, Chen J, Byzova TV, (2006) Akt1 in endothelial cell and angiogenesis. Cell Cycle 5: 512-518.
29. Srinivasan R, Zabuawala T, Huang H, Zhang J, Gulati P, et al. (2009) Erk1 and Erk2 regulate endothelial cell proliferation and migration during mouse embryonic angiogenesis. PLoS One 4: e8283.
30. Colman RW, (2006) Regulation of angiogenesis by the kallikrein-kinin system. Curr Pharm Des 12: 2599-2607.
31. LaRusch GA, Mahdi F, Shariat-Madar Z, Adams G, Sitrin RG, et al. (2010) Factor XII stimulates ERK1/2 and Akt through uPAR, integrins, and the EGFR to initiate angiogenesis. Blood 115: 5111-5120.
32. Deakin NO, Turner CE, (2008) Paxillin comes of age. J Cell Sci 121: 2435-2444.
33. DeLa Cadena RA, Colman RW, (1991) Structure and functions of human kininogens. Trends Pharmacol Sci 12: 272-275.
34. Hasan AA, Cines DB, Herwald H, Schmaier AH, Muller-Esterl W, (1995) Mapping the cell binding site on high molecular weight kininogen domain 5. J Biol Chem 270: 19256-19261.
35. Kawasaki M, Maeda T, Hanasawa K, Ohkubo I, Tani T, (2003) Effect of His-Gly-Lys motif derived from domain 5 of high molecular weight kininogen on suppression of cancer metastasis both in vitro and in vivo. J Biol Chem 278: 49301-49307.
36. Li JY, Paragas N, Ned RM, Qiu A, Viltard M, et al. (2009) Scara5 is a ferritin receptor mediating non-transferrin iron delivery. Dev Cell 16: 35-46.
37. Rucker P, Torti FM, Torti SV, (1997) Recombinant ferritin: modulation of subunit stoichiometry in bacterial expression systems. Protein Eng 10: 967-973.
38. Cao DJ, Guo YL, Colman RW, (2004) Urokinase-type plasminogen activator receptor is involved in mediating the apoptotic effect of cleaved high molecular weight kininogen in human endothelial cells. Circ Res 94: 1227-1234.
39. McCrae KR, Donate F, Merkulov S, Sun D, Qi X, et al. (2005) Inhibition of angiogenesis by cleaved high molecular weight kininogen (HKa) and HKa domain 5. Curr Cancer Drug Targets 5: 519-528.
40. Peerschke EI, Ghebrehiwet B, (2007) The contribution of gC1qR/p33 in infection and inflammation. Immunobiology 212: 333-342.
41. Smith HW, Marshall CJ, (2010) Regulation of cell signalling by uPAR. Nat Rev Mol Cell Biol 11: 23-36.
42. Liu Y, Cao DJ, Sainz IM, Guo YL, Colman RW, (2008) The inhibitory effect of HKa in endothelial cell tube formation is mediated by disrupting the uPA-uPAR complex and inhibiting its signaling and internalization. Am J Physiol Cell Physiol 295: C257-267.
43. Lawson DM, Artymiuk PJ, Yewdall SJ, Smith JM, Livingstone JC, et al. (1991) Solving the structure of human H ferritin by genetically engineering intermolecular crystal contacts. Nature 349: 541-544.
44. Wang Z, Li C, Ellenburg M, Soistman E, Ruble J, et al. (2006) Structure of human ferritin L chain. Acta Crystallogr D Biol Crystallogr 62: 800-806.