Histidine-rich glycoprotein: The Swiss Army knife of mammalian plasma

Blood

Volumn 117, Issue 7, 2011, Pages 2093-2101

  Poon, Ivan K H ^a,b   Patel, Kruti K ^b   Davis, David S ^a   Parish, Christopher R ^a   Hulett, Mark D ^a,b  

^a Biology and Environment   (Australia)

^b LA TROBE UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; C REACTIVE PROTEIN; COMPLEMENT COMPONENT C1Q; DNA; FIBRINOGEN; GLYCOPROTEIN; HEME; HEPARIN; HISTIDINE; HISTIDINE RICH GLYCOPROTEIN; IMMUNOGLOBULIN G; LIGAND; PHOSPHOLIPID; PLASMA PROTEIN; PLASMINOGEN; THROMBOSPONDIN 1; UNCLASSIFIED DRUG; ZINC ION;

ANGIOGENESIS; ANTIGEN ANTIBODY COMPLEX; BLOOD CLOTTING; CELL ADHESION; CELL DEATH; FIBRINOLYSIS; HUMAN; IMMUNOREGULATION; MAMMAL; NONHUMAN; PATHOGEN CLEARANCE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN PROCESSING; REVIEW; VASCULAR BIOLOGY;

EID: 79951846927     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2010-09-303842     Document Type: Review

References (99)

1. Heimburger N, Haupt H, Kranz T, Baudner S. Human serum proteins with high affinity to carboxymethylcellulose. II. Physicochemical and immunological characterization of a histidine-rich 3,8S- 2-glycoportein (CM-protein I) [in German]. Hoppe Seylers Z Physiol Chem. 1972;353(7):1133-1140.
2. Haupt H, Heimburger N. Human serum proteins with high affinity for carboxymethylcellulose. I. Isolation of lysozyme, C1q and 2 hitherto unknown -globulins [in German]. Hoppe Seylers Z Physiol Chem. 1972;353(7):1125-1132.
3. Jones AL, Hulett MD, Parish CR. Histidine-rich glycoprotein: a novel adaptor protein in plasma that modulates the immune, vascular and coagulation systems. Immunol Cell Biol. 2005;83(2):106-118. (Pubitemid 40469318)
4. Nair PS, Robinson WE. Purification and characterization of a histidine-rich glycoprotein that binds cadmium from the blood plasma of the bivalve Mytilus edulis. Arch Biochem Biophys. 1999;366(1):8-14. (Pubitemid 29394222)
5. Koide T, Foster D, Yoshitake S, Davie EW. Amino acid sequence of human histidine-rich glycoprotein derived from the nucleotide sequence of its cDNA. Biochemistry. 1986;25(8):2220-2225. (Pubitemid 16036040)
6. Sia DY, Rylatt DB, Parish CR. Anti-self receptors. V. Properties of a mouse serum factor that blocks autorosetting receptors on lymphocytes. Immunology. 1982;45(2):207-216. (Pubitemid 12214170)
7. Leung LL, Harpel PC, Nachman RL, Rabellino EM. Histidine-rich glycoprotein is present in human platelets and is released following thrombin stimulation. Blood. 1983;62(5):1016-1021. (Pubitemid 14237323)
8. van den Berg EA, le Clercq E, Kluft C, et al. Assignment of the human gene for histidine-rich glycoprotein to chromosome 3. Genomics. 1990;7(2):276-279.
9. Koide T, Odani S. Histidine-rich glycoprotein is evolutionarily related to the cystatin superfamily. Presence of two cystatin domains in the N-terminal region. FEBS Lett. 1987;216(1):17-21.
10. Sørensen CB, Krogh-Pedersen H, Petersen TE. Determination of the disulphide bridge arrangement of bovine histidine-rich glycoprotein. FEBS Lett. 1993;328(3):285-290. (Pubitemid 23238105)
11. Katagiri M, Tsutsui K, Yamano T, Shimonishi Y, Ishibashi F. Interaction of heme with a synthetic peptide mimicking the putative heme-binding site of histidine-rich glycoprotein. Biochem Biophys Res Commun. 1987;149(3):1070-1076.
12. Morgan WT. Interactions of the histidine-rich glycoprotein of serum with metals. Biochemistry. 1981;20(5):1054-1061.
13. Lijnen HR, Hoylaerts M, Collen D. Isolation and characterization of a human plasma protein with affinity for the lysine binding sites in plasminogen. Role in the regulation of fibrinolysis and identification as histidine-rich glycoprotein. J Biol Chem. 1980;255(21):10214-10222. (Pubitemid 11214600)
14. Poon IK, Yee DY, Jones AL, et al. Histidine-rich glycoprotein binds heparanase and regulates its enzymatic activity and cell surface interactions. Int J Biochem Cell Biol. 2010;42(9):1507-1516.
15. Leung LL. Interaction of histidine-rich glycoprotein with fibrinogen and fibrin. J Clin Invest. 1986;77(4):1305-1311. (Pubitemid 16047154)
16. Leung LL, Nachman RL, Harpel PC. Complex formation of platelet thrombospondin with histidine-rich glycoprotein. J Clin Invest. 1984;73(1):5-12. (Pubitemid 14222643)
17. Klenotic PA, Huang P, Palomo J, et al. Histidine-rich glycoprotein modulates the anti-angiogenic effects of vasculostatin. Am J Pathol. 2010;176(4):2039-2050.
18. Gorgani NN, Parish CR, Easterbrook Smith SB, Altin JG. Histidine-rich glycoprotein binds to human IgG and C1q and inhibits the formation of insoluble immune complexes. Biochemistry. 1997;36(22):6653-6662. (Pubitemid 27242323)
19. Manderson GA, Martin M, Onnerfjord P, et al. Interactions of histidine-rich glycoprotein with immunoglobulins and proteins of the complement system. Mol Immunol. 2009;46(16):3388-3398.
20. Gorgani NN, Altin JG, Parish CR. Histidine-rich glycoprotein regulates the binding of monomeric IgG and immune complexes to monocytes. Int Immunol. 1999;11(8):1275-1282. (Pubitemid 29355667)
21. Jones AL, Hulett MD, Parish CR. Histidine-rich glycoprotein binds to cell-surface heparan sulfate via its N-terminal domain following Zn2+ chelation. J Biol Chem. 2004;279(29):30114-30122. (Pubitemid 38937934)
22. Poon IK, Hulett MD, Parish CR. Histidine-rich glycoprotein is a novel plasma pattern recognition molecule that recruits IgG to facilitate necrotic cell clearance via Fc{gamma}RI on phagocytes. Blood. 2010;115(12):2473-2482.
23. Guan X, Juarez JC, Qi X, et al. Histidine-proline rich glycoprotein (HPRG) binds and transduces anti-angiogenic signals through cell surface tropomyosin on endothelial cells. Thromb Haemost. 2004;92(2):403-412. (Pubitemid 39172321)
24. Ohta T, Ikemoto Y, Usami A, Koide T, Wakabayashi S. High affinity interaction between histidine-rich glycoprotein and the cell surface type ATP synthase on T-cells. Biochim Biophys Acta. 2009;1788(5):1099-1107.
25. Gorgani NN, Smith BA, Kono DH, Theofilopoulos AN. Histidine-rich glycoprotein binds to DNA and Fc gamma RI and potentiates the ingestion of apoptotic cells by macrophages. J Immunol. 2002;169(9):4745-4751. (Pubitemid 35217136)
26. Jones AL, Poon IK, Hulett MD, Parish CR. Histidine-rich glycoprotein specifically binds to necrotic cells via its amino-terminal domain and facilitates necrotic cell phagocytosis. J Biol Chem. 2005;280(42):35733-35741. (Pubitemid 41532766)
27. Borza DB, Tatum FM, Morgan WT. Domain structure and conformation of histidine-proline-rich glycoprotein. Biochemistry. 1996;35(6):1925-1934.
28. Gorgani NN, Altin JG, Parish CR. Histidine-rich glycoprotein prevents the formation of insoluble immune complexes by rheumatoid factor. Immunology. 1999;98(3):456-463. (Pubitemid 29526971)
29. Gorgani NN, Parish CR, Altin JG. Differential binding of histidine-rich glycoprotein (HRG) to human IgG subclasses and IgG molecules containing kappa and lambda light chains. J Biol Chem. 1999;274(42):29633-29640.
30. Chang NS, Leu RW, Anderson JK, Mole JE. Role of N-terminal domain of histidine-rich glycoprotein in modulation of macrophage Fc gamma receptor-mediated phagocytosis. Immunology. 1994;81(2):296-302. (Pubitemid 24223209)
31. Chang NS, Leu RW, Rummage JA, Anderson JK, Mole JE. Regulation of macrophage Fc receptor expression and phagocytosis by histidine-rich glycoprotein. Immunology. 1992;77(4):532-538. (Pubitemid 23000473)
32. Poon IK, Hulett MD, Parish CR. Molecular mechanisms of late apoptotic/necrotic cell clearance. Cell Death Differ. 2010;17(3):381-397.
33. Poon IK, Parish CR, Hulett MD. Histidine-rich glycoprotein functions cooperatively with cell surface heparan sulfate on phagocytes to promote necrotic cell uptake. J Leukoc Biol. 2010;88(3):559-569.
34. Mevorach D, Mascarenhas JO, Gershov D, Elkon KB. Complement-dependent clearance of apoptotic cells by human macrophages. J Exp Med. 1998;188(12):2313-2320. (Pubitemid 29028503)
35. Silverstein RL, Leung LL, Harpel PC, Nachman RL. Platelet thrombospondin forms a trimolecular complex with plasminogen and histidine-rich glycoprotein. J Clin Invest. 1985;75(6):2065-2073. (Pubitemid 15233598)
36. Walz DA, Bacon-Baguley T, Kendra-Franczak S, DePoli P. Binding of thrombospondin to immobilized ligands: specific interaction with fibrinogen, plasminogen, histidine-rich glycoprotein, and fibronectin. Semin Thromb Hemost. 1987;13(3):317-325.
37. Rydengård V, Olsson AK, Morgelin M, Schmidtchen A. Histidine-rich glycoprotein exerts antibacterial activity. FEBS J. 2007;274(2):377-389. (Pubitemid 46046648)
38. Shannon O, Rydengård V, Schmidtchen A, et al. Histidine-rich glycoprotein promotes bacterial entrapment in clots and decreases mortality in a mouse model of sepsis. Blood. 2010;116(13):2365-2372.
39. Kacprzyk L, Rydengård V, Morgelin M, et al. Antimicrobial activity of histidine-rich peptides is dependent on acidic conditions. Biochim Biophys Acta. 2007;1768(11):2667-2680. (Pubitemid 350060862)
40. Rydengård V, Shannon O, Lundqvist K, et al. Histidine-rich glycoprotein protects from systemic Candida infection. PLoS Pathog. 2008;4(8):e1000116.
41. Nordahl EA, Rydengård V, Morgelin M, Schmidtchen A. Domain 5 of high molecular weight kininogen is antibacterial. J Biol Chem. 2005;280(41):34832-34839. (Pubitemid 41504617)
42. Bosshart H, Heinzelmann M. Endotoxin-neutralizing effects of histidine-rich peptides. FEBS Lett. 2003;553(1-2):135-140. (Pubitemid 37206339)
43. Lamb-Wharton RJ, Morgan WT. Induction of T-lymphocyte adhesion by histidine-proline-rich glycoprotein and concanavalin A. Cell Immunol. 1993;152(2):544-555. (Pubitemid 24040504)
44. Olsen HM, Parish CR, Altin JG. Histidine-rich glycoprotein binding to T-cell lines and its effect on T-cell substratum adhesion is strongly potentiated by zinc. Immunology. 1996;88(2):198-206.
45. Rylatt DB, Sia DY, Mundy JP, Parish CR. Autorosette inhibition factor: isolation and properties of the human plasma protein. Eur J Biochem. 1981;119(3):641-646.
46. Simantov R, Febbraio M, Crombie R, et al. Histidine-rich glycoprotein inhibits the antiangiogenic effect of thrombospondin-1. J Clin Invest. 2001;107(1):45-52. (Pubitemid 32047413)
47. Olsson AK, Larsson H, Dixelius J, et al. A fragment of histidine-rich glycoprotein is a potent inhibitor of tumor vascularization. Cancer Res. 2004;64(2):599-605. (Pubitemid 38120899)
48. Thulin A, Ringvall M, Dimberg A, et al. Activated platelets provide a functional microenvironment for the antiangiogenic fragment of histidine-rich glycoprotein. Mol Cancer Res. 2009;7(11):1792-1802.
49. Kärrlander M, Lindberg N, Olofsson T, et al. Histidine-rich glycoprotein can prevent development of mouse experimental glioblastoma. PLoS ONE. 2009;4(12):e8536.
50. Tsuchida-Straeten N, Ensslen S, Schafer C, et al. Enhanced blood coagulation and fibrinolysis in mice lacking histidine-rich glycoprotein (HRG). J Thromb Haemost. 2005;3(5):865-872. (Pubitemid 41632812)
51. Ohta T, Ikemoto Y, Saeki K, Koide T, Wakabayashi S. Histidine-rich glycoprotein and concanavalin A synergistically stimulate the phosphatidylinositol 3-kinase-independent signaling pathway in leukocytes leading to increased cell adhesion and changes in cell morphology. Cell Immunol. 2009;259(1):5-12.
52. Dixelius J, Olsson AK, Thulin A, et al. Minimal active domain and mechanism of action of the angiogenesis inhibitor histidine-rich glycoprotein. Cancer Res. 2006;66(4):2089-2097.
53. Lee C, Dixelius J, Thulin A, et al. Signal transduction in endothelial cells by the angiogenesis inhibitor histidine-rich glycoprotein targets focal adhesions. Exp Cell Res. 2006;312(13):2547-2556. (Pubitemid 44036805)
54. Doñate F, Juarez JC, Guan X, et al. Peptides derived from the histidine-proline domain of the histidine-proline-rich glycoprotein bind to tropomyosin and have antiangiogenic and antitumor activities. Cancer Res. 2004;64(16):5812-5817. (Pubitemid 39095581)
55. Juarez JC, Guan X, Shipulina NV, et al. Histidine-proline-rich glycoprotein has potent antiangiogenic activity mediated through the histidine-proline-rich domain. Cancer Res. 2002;62(18):5344-5350. (Pubitemid 35024611)
56. Simantov R, Febbraio M, Silverstein RL. The antiangiogenic effect of thrombospondin-2 is mediated by CD36 and modulated by histidine-rich glycoprotein. Matrix Biol. 2005;24(1):27-34. (Pubitemid 40320896)
57. Borza DB, Morgan WT. Acceleration of plasminogen activation by tissue plasminogen activator on surface-bound histidine-proline-rich glycoprotein. J Biol Chem. 1997;272(9):5718-5726. (Pubitemid 27102400)
58. Borza DB, Shipulina NV, Morgan WT. Effects of histidine-proline-rich glycoprotein on plasminogen activation in solution and on surfaces. Blood Coagul Fibrinolysis. 2004;15(8):663-672. (Pubitemid 39612972)
59. Jones AL, Hulett MD, Altin JG, Hogg P, Parish CR. Plasminogen is tethered with high affinity to the cell surface by the plasma protein, histidine-rich glycoprotein. J Biol Chem. 2004;279(37):38267-38276. (Pubitemid 39295974)
60. Saez CT, Jansen GJ, Smith A, Morgan WT. Interaction of histidine-proline-rich glycoprotein with plasminogen: effect of ligands, pH, ionic strength, and chemical modification. Biochemistry. 1995;34(8):2496-2503.
61. Freeman C, Parish CR. A rapid quantitative assay for the detection of mammalian heparanase activity. Biochem J. 1997;325(Pt 1):229-237.
62. Brown KJ, Parish CR. Histidine-rich glycoprotein and platelet factor 4 mask heparan sulfate proteoglycans recognized by acidic and basic fibroblast growth factor. Biochemistry. 1994;33(46):13918-13927. (Pubitemid 24381957)
63. Wake H, Mori S, Liu K, Takahashi HK, Nishibori M. Histidine-rich glycoprotein inhibited high mobility group box 1 in complex with heparin-induced angiogenesis in matrigel plug assay. Eur J Pharmacol. 2009;623(1-3):89-95.
64. Lijnen HR, Hoylaerts M, Collen D. Heparin binding properties of human histidine-rich glycoprotein. Mechanism and role in the neutralization of heparin in plasma. J Biol Chem. 1983;258(6):3803-3808. (Pubitemid 13052870)
65. Poon IK, Olsson AK, Hulett MD, Parish CR. Regulation of histidine-rich glycoprotein (HRG) function via plasmin-mediated proteolytic cleavage. Biochem J. 2009;424(1):27-37.
66. Lijnen HR, Van Hoef B, Collen D. Histidine-rich glycoprotein modulates the anticoagulant activity of heparin in human plasma. Thromb Haemost. 1984;51(2):266-268. (Pubitemid 14145109)
67. Lijnen HR, van Hoef B, Collen D. Interaction of heparin with histidine-rich glycoprotein and with antithrombin III. Thromb Haemost. 1983;50(2):560-562. (Pubitemid 13048235)
68. Lijnen HR, Hoylaerts M, Collen D. Neutralization of heparin activity by binding to human histidine-rich glycoprotein. Thromb Res. 1983;29(4):443-446. (Pubitemid 13162368)
69. Aktulga A, Ulutin ON. Normal human platelet zinc content and its release. In: Ulutin ON, Jones JV, eds. Recent Advances in Basic Research and Clinical Aspects. Amsterdam: Excerpta Medica; 1974:185-191.
70. Fu CL, Horn MK. III. Histidine-rich glycoprotein plus zinc to neutralize heparin. J Lab Clin Med. 2002;139(4):211-217.
71. Kluszynski BA, Kim C, Faulk WP. Zinc as a cofactor for heparin neutralization by histidine-rich glycoprotein. J Biol Chem. 1997;272(21):13541- 13547. (Pubitemid 27224783)
72. Horne MK, Goad JL, Merryman PK, Cullinane AM. Comparison of the effect of histidine-rich glycoprotein and 6- aminohexanoic acid on plasmin production and fibrinolysis in vitro. Thromb Res. 2000;99(2):179-186. (Pubitemid 30628491)
73. Sherman P, Soni R, Petric M, Karmali M. Surface properties of the Vero cytotoxin-producing Escherichia coli O157:H7. Infect Immun. 1987;55(8):1824- 1829.
74. Park SE, Chao M, Raj PA. Mechanical properties of surface-charged poly(methyl methacrylate) as denture resins. Int J Dent. 2009;2009:841431.
75. Huang RT. Adsorption of influenza virus to charged groups on natural and artificial surfaces. Med Microbiol Immunol. 1974;159(2):129-135.
76. Levine JS, Subang R, Koh JS, Rauch J. Induction of anti-phospholipid autoantibodies by beta2-glycoprotein I bound to apoptotic thymocytes. J Autoimmun. 1998;11(5):413-424. (Pubitemid 28520196)
77. Sugi T, McIntyre JA. Autoantibodies to phosphatidylethanolamine (PE) recognize a kininogen-PE complex. Blood. 1995;86(8):3083-3089.
78. Sjöwall C, Wettero J. Pathogenic implications for autoantibodies against C-reactive protein and other acute phase proteins. Clin Chim Acta. 2007;378(1-2):13-23. (Pubitemid 46241084)
79. Ball-Rosen C, Primak-Rubinovicz H, Korczyn AD, et al. Identification of histidine-rich glycoprotein, a potential autoantigen, in human and rat brain preparations. Ann N Y Acad Sci. 2007;1109:473-483. (Pubitemid 47511390)
80. Haseley LA, Wisnieski JJ, Denburg MR, et al. Antibodies to C1q in systemic lupus erythematosus: characteristics and relation to Fc gamma RIIA alleles. Kidney Int. 1997;52(5):1375-1380. (Pubitemid 27496068)
81. Arvieux J, Roussel B, Ponard D, Colomb MG. IgG2 subclass restriction of anti-beta 2 glycoprotein 1 antibodies in autoimmune patients. Clin Exp Immunol. 1994;95(2):310-315. (Pubitemid 24207145)
82. Buckley RH. Immunoglobulin G subclass deficiency: fact or fancy? Curr Allergy Asthma Rep. 2002;2(5):356-360.
83. Redegeld FA, Caldwell CC, Sitkovsky MV. Ectoprotein kinases: ecto-domain phosphorylation as a novel target for pharmacological manipulation? Trends Pharmacol Sci. 1999;20(11):453-459. (Pubitemid 29528217)
84. Culley FJ, Harris RA, Kaye PM, McAdam KP, Raynes JG. C-reactive protein binds to a novel ligand on Leishmania donovani and increases uptake into human macrophages. J Immunol. 1996;156(12):4691-4696. (Pubitemid 26174452)
85. Loveless RW, Floyd-O'Sullivan G, Raynes JG, Yuen CT, Feizi T. Human serum amyloid P is a multispecific adhesive protein whose ligands include 6-phosphorylated mannose and the 3-sulphated saccharides galactose, N-acetylgalactosamine and glucuronic acid. EMBO J. 1992;11(3):813-819.
86. Schmaier AH, McCrae KR. The plasma kallikreinkinin system: its evolution from contact activation. J Thromb Haemost. 2007;5(12):2323-2329. (Pubitemid 350154338)
87. Koide T. Human histidine-rich glycoprotein gene: evidence for evolutionary relatedness to cystatin supergene family. Thromb Res Suppl. 1988;8:91-97. (Pubitemid 18263680)
88. Smith A, Nuiry I, Morgan WT. Proteolysis of histidine-rich glycoprotein in plasma and in patients undergoing thrombolytic therapy. Thromb Res. 1985;40(5):653-661. (Pubitemid 16174602)
89. Kleniewski J, Blankenship DT, Cardin AD, Donaldson V. Mechanism of enhanced kinin release from high molecular weight kininogen by plasma kallikrein after its exposure to plasmin. J Lab Clin Med. 1992;120(1):129-139.
90. Campbell DJ. Towards understanding the kallikrein-kinin system: insights from measurement of kinin peptides. Braz J Med Biol Res. 2000;33(6):665-677.
91. Zhang JC, Claffey K, Sakthivel R, et al. Two-chain high molecular weight kininogen induces endothelial cell apoptosis and inhibits angiogenesis: partial activity within domain 5. FASEB J. 2000;14(15):2589-2600.
92. Sakai T, Balasubramanian K, Maiti S, Halder JB, Schroit AJ. Plasmin-cleaved beta-2-glycoprotein 1 is an inhibitor of angiogenesis. Am J Pathol. 2007;171(5):1659-1669.
93. Nilsson M, Wasylik S, Morgelin M, et al. The antibacterial activity of peptides derived from human beta-2 glycoprotein I is inhibited by protein H and M1 protein from Streptococcus pyogenes. Mol Microbiol. 2008;67(3):482-492.
94. Saigo K, Yoshida A, Ryo R, Yamaguchi N, Leung LL. Histidine-rich glycoprotein as a negative acute phase reactant. Am J Hematol. 1990;34(2):149-150. (Pubitemid 20180108)
95. Saigo K, Yoshida A, Sugano W, Ryo R, Yamaguchi N. Histidine-rich glycoprotein in blood during inflammation, surgical operation or hemodialysis [in Japanese]. Rinsho Ketsueki. 1990;31(12):1914-1919.
96. Castel M, Horellou MH, Conrad J, Samama M. Immunochemical determination of histidine-rich glycoprotein in healthy subjects and in a clinical population. In: Davisdon JF, Bachmann F, Bouvier CA, Kruithof EKO, eds. Progress in Fibrinolysis. Vol. 6. Churchill Livingstone: Edinburgh; 1988:370.
97. Souto JC, Gari M, Falkon L, Fontcuberta J. A new case of hereditary histidine-rich glycoprotein deficiency with familial thrombophilia. Thromb Haemost. 1996;75(2):374-375.
98. Angles-Cano E, Gris JC, Loyau S, Schved JF. Familial association of high levels of histidine-rich glycoprotein and plasminogen activator inhibitor-1 with venous thromboembolism. J Lab Clin Med. 1993;121(5):646-653. (Pubitemid 23148690)
99. Shigekiyo T, Kanazuka M, Azuma H, et al. Congenital deficiency of histidine-rich glycoprotein: failure to identify abnormalities in routine laboratory assays of hemostatic function, immunologic function, and trace elements. J Lab Clin Med. 1995;125(6):719-723.