Histidine rich glycoprotein and cancer: A multi-faceted relationship

Anticancer Research

Volumn 34, Issue 2, 2014, Pages 593-604

  Johnson, Lisa D S ^a   Goubran, Hadi A ^b   Kotb, Rami R ^a,c  

^a BRITISH COLUMBIA CANCER AGENCY   (Canada)

^b UNIVERSITY OF SASKATCHEWAN   (Canada)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Hemostasis; Histidine rich glycoprotein; Innate immunity; Macrophage; Review.; Tumor microenvironment

Indexed keywords

ANGIOGENIC PROTEIN; ANTINEOPLASTIC AGENT; ANTITHROMBIN; BEVACIZUMAB; BLOOD CLOTTING FACTOR; CLODRONIC ACID; GLYCOPROTEIN; HEPARIN; HEPARIN BINDING PROTEIN; HISTIDINE RICH GLYCOPROTEIN; PIMONIDAZOLE; RECOMBINANT HISTIDINE RICH GLYCOPROTEIN; RECOMBINANT PROTEIN; THROMBOSPONDIN; TROPOMYOSIN; UNCLASSIFIED DRUG; HISTIDINE RICH PROTEINS; HISTIDINE-RICH PROTEINS; PLASMA PROTEIN; PROTEIN;

ANGIOGENESIS; ANTIANGIOGENIC ACTIVITY; CANCER ADJUVANT THERAPY; CANCER CHEMOTHERAPY; CANCER PROGNOSIS; CLINICAL TRIAL (TOPIC); FIBRINOLYSIS; FIBROSARCOMA; GENE EXPRESSION; HEMOSTASIS; HUMAN; HUMAN CHROMOSOME; IMMUNE RESPONSE; IMMUNOMODULATION; METASTASIS; MOLECULARLY TARGETED THERAPY; NEOPLASM; NONHUMAN; PLASMA; PROTEIN BINDING; PROTEIN BLOOD LEVEL; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN STRUCTURE; PROTEOMICS; REVIEW; THROMBOCYTE; THROMBOCYTE FUNCTION; TUMOR ASSOCIATED LEUKOCYTE; TUMOR IMMUNITY; TUMOR VASCULARIZATION; ANIMAL; BLOOD; HISTIDINE-RICH GLYCOPROTEIN; INNATE IMMUNITY; MACROPHAGE; METABOLISM; TUMOR MICROENVIRONMENT;

HEMOSTASIS; HISTIDINE-RICH GLYCOPROTEIN; INNATE IMMUNITY; MACROPHAGE; REVIEW; TUMOR MICROENVIRONMENT;

ANIMALS; BLOOD PROTEINS; HUMANS; NEOPLASMS; PROTEINS;

EID: 84897066298     PISSN: 02507005     EISSN: 17917530     Source Type: Journal    
DOI: None     Document Type: Review

References (77)

1. Borsig L: Antimetastatic activities of heparins and modified heparins. Experimental evidence. Thrombosis research 125(Suppl 2): S66-71, 2010.
2. Degen JL and Palumbo JS: Hemostatic factors, innate immunity and malignancy. Thrombosis research 129(Suppl 1): S1-5, 2012.
3. Palumbo JS, Talmage KE, Massari JV, La Jeunesse CM, Flick MJ, Kombrinck KW, Jirouskova M and Degen JL: Platelets and fibrin(ogen) increase metastatic potential by impeding natural killer cell-mediated elimination of tumor cells. Blood 105: 178-185, 2005.
4. van Sluis GL, Bruggemann LW, Esmon CT, Kamphuisen PW, Richel DJ, Buller HR, van Noorden CJ and Spek CA: Endogenous activated protein C is essential for immune-mediated cancer cell elimination from the circulation. Cancer letters 306: 106-110, 2011.
5. Lee C, Bongcam-Rudloff E, Sollner C, Jahnen-Dechent W and Claesson-Welsh L: Type 3 cystatins; fetuins, kininogen and histidine-rich glycoprotein. Frontiers in bioscience 14: 2911-2922, 2009.
6. Poon IK, Patel KK, Davis DS, Parish CR and Hulett MD: Histidine-rich glycoprotein: the Swiss Army knife of mammalian plasma. Blood 117: 2093-2101, 2011.
7. Engesser L, Kluft C, Briet E and Brommer EJ: Familial elevation of plasma histidine-rich glycoprotein in a family with thrombophilia. British J Haematology 67: 355-358, 1987.
8. Shannon O, Rydengard V, Schmidtchen A, Morgelin M, Alm P, Sorensen OE and Bjorck L: Histidine-rich glycoprotein promotes bacterial entrapment in clots and decreases mortality in a mouse model of sepsis. Blood 116: 2365-2372, 2010.
9. Rydengard V, Shannon O, Lundqvist K, Kacprzyk L, Chalupka A, Olsson AK, Morgelin M, Jahnen-Dechent W, Malmsten M and Schmidtchen A: Histidine-rich glycoprotein protects from systemic Candida infection. PLoS pathogens 4: e1000116, 2008.
10. Koide T, Foster D, Yoshitake S and Davie EW: Amino acid sequence of human histidine-rich glycoprotein derived from the nucleotide sequence of its cDNA. Biochemistry 25: 2220-2225, 1986.
11. Hennis BC, van Boheemen PA, Wakabayashi S, Koide T, Hoffmann JJ, Kievit P, Dooijewaard G, Jansen JG and Kluft C: Identification and genetic analysis of a common molecular variant of histidine-rich glycoprotein with a difference of 2kD in apparent molecular weight. Thrombosis and haemostasis 74: 1491-1496, 1995.
12. Jones AL, Hulett MD and Parish CR: Histidine-rich glycoprotein: A novel adaptor protein in plasma that modulates the immune, vascular and coagulation systems. Immunology and cell biology 83: 106-118, 2005.
13. Poon IK, Hulett MD, and Parish CR: Histidine-rich glycoprotein is a novel plasma pattern recognition molecule that recruits IgG to facilitate necrotic cell clearance via FcgammaRI on phagocytes. Blood 115: 2473-2482, 2010.
14. Wakabayashi S: New insights into the functions of histidine-rich glycoprotein. International review of cell and molecular biology 304: 467-493, 2013.
15. Dixelius J, Olsson AK, Thulin A, Lee C, Johansson I and Claesson-Welsh L: Minimal active domain and mechanism of action of the angiogenesis inhibitor histidine-rich glycoprotein. Cancer research 66: 2089-2097, 2006.
16. Patel KK, Poon IK, Talbo GH, Perugini MA, Taylor NL, Ralph TJ, Hoogenraad NJ and Hulett MD: New method for purifying histidine-rich glycoprotein from human plasma redefines its functional properties. IUBMB life 65: 550-563, 2013.
17. Juarez JC, Guan X, Shipulina NV, Plunkett ML, Parry GC, Shaw DE, Zhang JC, Rabbani SA, McCrae KR, Mazar AP, Morgan WT and Donate F: Histidine-proline-rich glycoprotein has potent antiangiogenic activity mediated through the histidine-prolinerich domain. Cancer research 62: 5344-5350, 2002.
18. Leung LL: Interaction of histidine-rich glycoprotein with fibrinogen and fibrin. The Journal of clinical investigation 77: 1305-1311, 1986.
19. Gorgani NN, Smith BA, Kono DH and Theofilopoulos AN: Histidine-rich glycoprotein binds to DNA and Fc gamma RI and potentiates the ingestion of apoptotic cells by macrophages. Journal of immunology 169: 4745-4751, 2002.
20. Hulett MD and Parish CR: Murine histidine-rich glycoprotein: cloning, characterization and cellular origin. Immunology and cell biology 78: 280-287, 2000.
21. 2+ chelation. The J Biological Chemistry 279: 30114-30122, 2004.
22. Wakabayashi S and Koide T: Histidine-rich glycoprotein: a possible modulator of coagulation and fibrinolysis. Seminars in thrombosis and hemostasis 37: 389-394, 2011.
23. Tsuchida-Straeten N, Ensslen S, Schafer C, Woltje M, Denecke B, Moser M, Graber S, Wakabayashi S, Koide T and Jahnen-Dechent W: Enhanced blood coagulation and fibrinolysis in mice lacking histidine-rich glycoprotein (HRG). J Thrombosis Haemostasis: JTH 3: 865-872, 2005.
24. Thulin A, Ringvall M, Dimberg A, Karehed K, Vaisanen T, Vaisanen MR, Hamad O, Wang J, Bjerkvig R, Nilsson B, Pihlajaniemi T, Akerud H, Pietras K, Jahnen-Dechent W, Siegbahn A and Olsson AK: Activated platelets provide a functional microenvironment for the antiangiogenic fragment of histidine-rich glycoprotein. Molecular Cancer Res: MCR 7: 1792-1802, 2009.
25. Ringvall M, Thulin A, Zhang L, Cedervall J, Tsuchida-Straeten N, Jahnen-Dechent W, Siegbahn A and Olsson AK: Enhanced platelet activation mediates the accelerated angiogenic switch in mice lacking histidine-rich glycoprotein. PloS one 6: e14526, 2011.
26. Shigekiyo T, Yoshida H, Kanagawa Y, Satoh K, Wakabayashi S, Matsumoto T and Koide T: Histidine-rich glycoprotein (HRG) Tokushima 2: novel HRG deficiency, molecular and cellular characterization. Thrombosis Haemostasis 84: 675-679, 2000.
27. Souto JC, Gari M, Falkon L and Fontcuberta J: A new case of hereditary histidine-rich glycoprotein deficiency with familial thrombophilia. Thrombosis and haemostasis 75: 374-375, 1996.
28. Shigekiyo T, Yoshida H, Matsumoto K, Azuma H, Wakabayashi S, Saito S, Fujikawa K and Koide T: HRG Tokushima: molecular and cellular characterization of histidine-rich glycoprotein (HRG) deficiency. Blood 91: 128-133, 1998.
29. Lijnen HR, Jacobs G and Collen D: Histidine-rich glycoprotein in a normal and a clinical population. Thrombosis Res 22: 519-523, 1981.
30. Saito H, Goodnough LT, Boyle JM and Heimburger N: Reduced histidine-rich glycoprotein levels in plasma of patients with advanced liver cirrhosis. Possible implications for enhanced fibrinolysis. The American J Med 73: 179-182, 1982.
31. Haukkamaa M, Morgan WT and Koskelo P: Serum histidine-rich glycoprotein during pregnancy and hormone treatment. Scandinavian journal of clinical and laboratory investigation 43: 591-595, 1983.
32. Karehed K, Wikstrom AK, Olsson AK, Larsson A, Olovsson M and Akerud H: Fibrinogen and histidine-rich glycoprotein in early-onset preeclampsia. Acta obstetricia et gynecologica Scandinavica 89: 131-139, 2010.
33. Wang F, Chmil C, Pierce F, Ganapathy K, Gump BB, MacKenzie JA, Metchref Y and Bendinskas K: Immobilized metal affinity chromatography and human serum proteomics. Journal of chromatography B, Analytical technologies in the biomedical and life sciences 934: 26-33, 2013.
34. Olsen HM, Parish CR and Altin JG: Histidine-rich glycoprotein binding to T-cell lines and its effect on T-cell substratum adhesion is strongly potentiated by zinc. Immunology 88: 198-206, 1996.
35. Fukamachi T, Chiba Y, Wang X, Saito H, Tagawa M and Kobayashi H: Tumor specific low pH environments enhance the cytotoxicity of lovastatin and cantharidin. Cancer letters 297: 182-189, 2010.
36. Leung LL, Harpel PC, Nachman RL and Rabellino EM: Histidinerich glycoprotein is present in human platelets and is released following thrombin stimulation. Blood 62: 1016-1021, 1983.
37. Borza DB and Morgan WT: Histidine-proline-rich glycoprotein as a plasma pH sensor. Modulation of its interaction with glycosaminoglycans by ph and metals. The Journal of biological chemistry 273: 5493-5499, 1998.
38. Vu TT, Stafford AR, Leslie BA, Kim PY, Fredenburgh JC and Weitz JI: Histidine-rich glycoprotein binds fibrin(ogen) with high affinity and competes with thrombin for binding to the gamma'-chain. The Journal of biological chemistry 286: 30314-30323, 2011.
39. MacQuarrie JL, Stafford AR, Yau JW, Leslie BA, Vu TT, Fredenburgh JC and Weitz JI: Histidine-rich glycoprotein binds factor XIIa with high affinity and inhibits contact-initiated coagulation. Blood 117: 4134-4141, 2011.
40. Xian X, Hakansson J, Stahlberg A, Lindblom P, Betsholtz C, Gerhardt H and Semb H: Pericytes limit tumor cell metastasis. The J Clinical Investigation 116: 642-651, 2006.
41. Olsson AK, Larsson H, Dixelius J, Johansson I, Lee C, Oellig C, Bjork I and Claesson-Welsh L: A fragment of histidine-rich glycoprotein is a potent inhibitor of tumor vascularization. Cancer Res 64: 599-605, 2004.
42. Simantov R, Febbraio M, Crombie R, Asch AS, Nachman RL and Silverstein RL: Histidine-rich glycoprotein inhibits the antiangiogenic effect of thrombospondin-1. The J Clinical Investigation 107: 45-52, 2001.
43. Hale JS, Li M, Sinyuk M, Jahnen-Dechent W, Lathia JD and Silverstein RL: Context dependent role of the CD36 - thrombospondin - histidine-rich glycoprotein axis in tumor angiogenesis and growth. PloS one 7: e40033, 2012.
44. Klenotic PA, Huang P, Palomo J, Kaur B, Van Meir EG, Vogelbaum MA, Febbraio M, Gladson CL and Silverstein RL: Histidine-rich glycoprotein modulates the anti-angiogenic effects of vasculostatin. The American journal of pathology 176: 2039-2050, 2010.
45. Tugues S, Honjo S, Konig C, Noguer O, Hedlund M, Botling J, Deschoemaeker S, Wenes M, Rolny C, Jahnen-Dechent W, Mazzone M and Claesson-Welsh L: Genetic deficiency in plasma protein HRG enhances tumor growth and metastasis by exacerbating immune escape and vessel abnormalization. Cancer research 72: 1953-1963, 2012.
46. Rolny C, Mazzone M, Tugues S, Laoui D, Johansson I, Coulon C, Squadrito ML, Segura I, Li X, Knevels E, Costa S, Vinckier S, Dresselaer T, Akerud P, De Mol M, Salomaki H, Phillipson M, Wyns S, Larsson E, Buysschaert I, Botling J, Himmelreich U, Van Ginderachter JA, De Palma M, Dewerchin M, Claesson-Welsh L and Carmeliet P: HRG inhibits tumor growth and metastasis by inducing macrophage polarization and vessel normalization through down-regulation of PlGF. Cancer Cell 19: 31-44, 2011.
47. Cooke VG, LeBleu VS, Keskin D, Khan Z, O'Connell JT, Teng Y, Duncan MB, Xie L, Maeda G, Vong S, Sugimoto H, Rocha RM, Damascena A, Brentani RR and Kalluri R: Pericyte depletion results in hypoxia-associated epithelial-to-mesenchymal transition and metastasis mediated by met signaling pathway. Cancer Cell 21: 66-81, 2012.
48. Cedervall J, Zhang Y, Ringvall M, Thulin A, Moustakas A, Jahnen-Dechent W, Siegbahn A and Olsson AK: HRG regulates tumor progression, epithelial to mesenchymal transition and metastasis via platelet-induced signaling in the pre-tumorigenic microenvironment. Angiogenesis 16: 889-902, 2013.
49. Karrlander M, Lindberg N, Olofsson T, Kastemar M, Olsson AK and Uhrbom L: Histidine-rich glycoprotein can prevent development of mouse experimental glioblastoma. PloS one 4: e8536, 2009.
50. Poon IK, Olsson AK, Hulett MD and Parish CR: Regulation of histidine-rich glycoprotein (HRG) function via plasmin-mediated proteolytic cleavage. The Biochemical Journal 424: 27-37, 2009.
51. Onder TT, Gupta PB, Mani SA, Yang J, Lander ES, and Weinberg RA: Loss of E-cadherin promotes metastasis via multiple downstream transcriptional pathways. Cancer research 68: 3645-3654, 2008.
52. Schumacher D, Strilic B, Sivaraj KK, Wettschureck N and Offermanns S: Platelet-derived nucleotides promote tumor-cell transendothelial migration and metastasis via P2Y2 receptor. Cancer cell 24: 130-137, 2013.
53. Blank M and Shoenfeld Y: Histidine-rich glycoprotein modulation of immune/autoimmune, vascular, and coagulation systems. Clinical reviews in allergy & immunology 34: 307-312, 2008.
54. Koide T, Odani S and Ono T: The N-terminal sequence of human plasma histidine-rich glycoprotein homologous to antithrombin with high affinity for heparin. FEBS letters 141: 222-224, 1982.
55. Bonde AK, Tischler V, Kumar S, Soltermann A and Schwendener RA: Intratumoral macrophages contribute to epithelial-mesenchymal transition in solid tumors. BMC Cancer 12: 35, 2012.
56. Qian BZ and Pollard JW: Macrophage diversity enhances tumor progression and metastasis. Cell 141: 39-51, 2010.
57. Ruffell B, Affara NI and Coussens LM: Differential macrophage programming in the tumor microenvironment. Trends in immunology 33: 119-126, 2012.
58. Lin EY, Li JF, Gnatovskiy L, Deng Y, Zhu L, Grzesik DA, Qian H, Xue XN and Pollard JW: Macrophages regulate the angiogenic switch in a mouse model of breast cancer. Cancer research 66: 11238-11246, 2006.
59. Allavena P and Mantovani A: Immunology in the clinic review series; focus on cancer: tumour-associated macrophages: undisputed stars of the inflammatory tumour microenvironment. Clinical and experimental immunology 167: 195-205, 2012.
60. Ino Y, Yamazaki-Itoh R, Shimada K, Iwasaki M, Kosuge T, Kanai Y and Hiraoka N: Immune cell infiltration as an indicator of the immune microenvironment of pancreatic cancer. British journal of cancer 108: 914-923, 2013.
61. Nonomura N, Takayama H, Nakayama M, Nakai Y, Kawashima A, Mukai M, Nagahara A, Aozasa K and Tsujimura A: Infiltration of tumour-associated macrophages in prostate biopsy specimens is predictive of disease progression after hormonal therapy for prostate cancer. BJU international 107: 1918-1922, 2011.
62. Wynn TA, Chawla A and Pollard JW: Macrophage biology in development, homeostasis and disease. Nature 496: 445-455, 2013.
63. Ong SM, Tan YC, Beretta O, Jiang D, Yeap WH, Tai JJ, Wong WC, Yang H, Schwarz H, Lim KH, Koh PK, Ling KL and Wong SC: Macrophages in human colorectal cancer are proinflammatory and prime T cells towards an anti-tumour type-1 inflammatory response. European J Immunology 42: 89-100, 2012.
64. Heusinkveld M, de Vos van Steenwijk PJ, Goedemans R, Ramwadhdoebe TH, Gorter A, Welters MJ, van Hall T and van der Burg SH: M2 macrophages induced by prostaglandin E2 and IL-6 from cervical carcinoma are switched to activated M1 macrophages by CD4+ Th1 cells. Journal of immunology 187: 1157-1165, 2011.
65. Saccani A, Schioppa T, Porta C, Biswas SK, Nebuloni M, Vago L, Bottazzi B, Colombo MP, Mantovani A and Sica A: p50 nuclear factor-kappaB overexpression in tumor-associated macrophages inhibits M1 inflammatory responses and antitumor resistance. Cancer research 66: 11432-11440, 2006.
66. Biswas SK and Mantovani A: Macrophage plasticity and interaction with lymphocyte subsets: cancer as a paradigm. Nature Immunology 11: 889-896, 2010.
67. Mitchem JB, Brennan DJ, Knolhoff BL, Belt BA, Zhu Y, Sanford DE, Belaygorod L, Carpenter D, Collins L, Piwnica-Worms D, Hewitt S, Udupi GM, Gallagher WM, Wegner C, West BL, Wang-Gillam A, Goedegebuure P, Linehan DC and DeNardo DG: Targeting tumor-infiltrating macrophages decreases tumor-initiating cells, relieves immunosuppression, and improves chemotherapeutic responses. Cancer Res 73: 1128-1141, 2013.
68. Shiao SL, Ganesan AP, Rugo HS, and Coussens LM: Immune microenvironments in solid tumors: new targets for therapy. Genes & development 25: 2559-2572, 2011.
69. Pyonteck SM, Akkari L, Schuhmacher AJ, Bowman RL, Sevenich L, Quail DF, Olson OC, Quick ML, Huse JT, Teijeiro V, Setty M, Leslie CS, Oei Y, Pedraza A, Zhang J, Brennan CW, Sutton JC, Holland EC, Daniel D and Joyce JA: CSF-1R inhibition alters macrophage polarization and blocks glioma progression. Nature medicine 19: 1264-1272, 2013.
70. Heusinkveld M and van der Burg SH: Identification and manipulation of tumor associated macrophages in human cancers. Journal of translational medicine 9: 216, 2011.
71. Shojaei F: Anti-angiogenesis therapy in cancer: current challenges and future perspectives. Cancer letters 320: 130-137, 2012.
72. Wu J, Xie X, Liu Y, He J, Benitez R, Buckanovich RJ and Lubman DM: Identification and confirmation of differentially expressed fucosylated glycoproteins in the serum of ovarian cancer patients using a lectin array and LC-MS/MS. J Proteome Res 11: 4541-4552, 2012.
73. Roberts AS, Campa MJ, Gottlin EB, Jiang C, Owzar K, Kindler HL, Venook AP, Goldberg RM, O'Reilly EM and Patz EF Jr.: Identification of potential prognostic biomarkers in patients with untreated, advanced pancreatic cancer from a phase 3 trial (Cancer and Leukemia Group B 80303). Cancer 118: 571-578, 2012.
74. Wang YS, Cao R, Jin H, Huang YP, Zhang XY, Cong Q, He YF and Xu CJ: Altered protein expression in serum from endometrial hyperplasia and carcinoma patients. J Hematology & Oncology 4: 15, 2011.
75. Schaub NP, Jones KJ, Nyalwidhe JO, Cazares LH, Karbassi ID, Semmes OJ, Feliberti EC, Perry RR and Drake RR: Serum proteomic biomarker discovery reflective of stage and obesity in breast cancer patients. Journal of the American College of Surgeons 208: 970-978; discussion 978-980, 2009.
76. Gabrilovich DI, Ostrand-Rosenberg S and Bronte V: Coordinated regulation of myeloid cells by tumours. Nature reviews Immunology 12: 253-268, 2012.
77. Huang Y, Goel S, Duda DG, Fukumura D and Jain RK: Vascular normalization as an emerging strategy to enhance cancer immunotherapy. Cancer research 73: 2943-2948, 2013.