HRG regulates tumor progression, epithelial to mesenchymal transition and metastasis via platelet-induced signaling in the pre-tumorigenic microenvironment

Angiogenesis

Volumn 16, Issue 4, 2013, Pages 889-902

  Cedervall, Jessica ^a   Zhang, Yanyu ^a   Ringvall, Maria ^a   Thulin, Åsa ^b   Moustakas, Aristidis ^a,c   Jahnen Dechent, Willi ^d   Siegbahn, Agneta ^b   Olsson, Anna Karin ^a  

^a UPPSALA UNIVERSITY   (Sweden)

^b UPPSALA UNIVERSITY   (Sweden)

^c LUDWIG INSTITUTE FOR CANCER RESEARCH   (Sweden)

^d RWTH AACHEN UNIVERSITY   (Germany)

Author keywords

Angiogenesis; EMT; HRG; Metastasis; Platelets

Indexed keywords

GLYCOPROTEIN; HISTIDINE RICH GLYCOPROTEIN; PLATELET DERIVED GROWTH FACTOR BETA RECEPTOR; PROTEIN KINASE; PROTEIN KINASE B BETA; TANK BINDING KINASE 1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; LIVER METASTASIS; METASTASIS; MOUSE; NONHUMAN; PANCREAS ISLET; PERICYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; THROMBOCYTE; TUMOR GROWTH; TUMOR MICROENVIRONMENT; TUMOR VASCULARIZATION; TUMOR VOLUME;

MUS;

ANIMALS; BLOOD PLATELETS; CARCINOMA; CELL TRANSFORMATION, NEOPLASTIC; CELLULAR MICROENVIRONMENT; DISEASE PROGRESSION; EPITHELIAL-MESENCHYMAL TRANSITION; INSULINOMA; ISLETS OF LANGERHANS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; NEOPLASM METASTASIS; NEOVASCULARIZATION, PATHOLOGIC; PANCREATIC NEOPLASMS; PROTEIN-SERINE-THREONINE KINASES; PROTEINS; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTOR, PLATELET-DERIVED GROWTH FACTOR BETA; SIGNAL TRANSDUCTION; TUMOR BURDEN; TUMOR SUPPRESSOR PROTEINS;

EID: 84884819218     PISSN: 09696970     EISSN: 15737209     Source Type: Journal    
DOI: 10.1007/s10456-013-9363-8     Document Type: Article

References (52)

1. Felding-Habermann B, Habermann R, Saldivar E, Ruggeri ZM (1996) Role of beta3 integrins in melanoma cell adhesion to activated platelets under flow. J Biol Chem 271(10):5892-5900
2. Jurk K, Kehrel BE (2005) Platelets: physiology and biochemistry. Semin Thromb Hemost 31(4):381-392
3. Gay LJ, Felding-Habermann B (2011) Contribution of platelets to tumour metastasis. Nat Rev Cancer 11(2):123-134
4. Lip GY, Chin BS, Blann AD (2002) Cancer and the prothrombotic state. Lancet Oncol 3(1):27-34
5. Pinedo HM, Verheul HM, D'Amato RJ, Folkman J (1998) Involvement of platelets in tumour angiogenesis? Lancet 352(9142):1775-1777
6. Pipili-Synetos E, Papadimitriou E, Maragoudakis ME (1998) Evidence that platelets promote tube formation by endothelial cells on matrigel. Br J Pharmacol 125(6):1252-1257
7. Verheul HM, Jorna AS, Hoekman K, Broxterman HJ, Gebbink MF, Pinedo HM (2000) Vascular endothelial growth factor-stimulated endothelial cells promote adhesion and activation of platelets. Blood 96(13):4216-4221
8. Brill A, Elinav H, Varon D (2004) Differential role of platelet granular mediators in angiogenesis. Cardiovasc Res 63(2):226-235
9. Rhee JS, Black M, Schubert U, Fischer S, Morgenstern E, Hammes HP, Preissner KT (2004) The functional role of blood platelet components in angiogenesis. Thromb Haemost 92(2):394-402
10. Chiodoni C, Iezzi M, Guiducci C, Sangaletti S, Alessandrini I, Ratti C, Tiboni F, Musiani P, Granger DN, Colombo MP (2006) Triggering CD40 on endothelial cells contributes to tumor growth. J Exp Med 203(11):2441-2450
11. Kisucka J, Butterfield CE, Duda DG, Eichenberger SC, Saffaripour S, Ware J, Ruggeri ZM, Jain RK, Folkman J, Wagner DD (2006) Platelets and platelet adhesion support angiogenesis while preventing excessive hemorrhage. Proc Natl Acad Sci USA 103(4):855-860
12. Ringvall M, Thulin A, Zhang L, Cedervall J, Tsuchida-Straeten N, Jahnen-Dechent W, Siegbahn A, Olsson AK (2011) Enhanced platelet activation mediates the accelerated angiogenic switch in mice lacking histidine-rich glycoprotein. PLoS ONE 6(1):e14526
13. Verheul HM, Hoekman K, Luykx-de Bakker S, Eekman CA, Folman CC, Broxterman HJ, Pinedo HM (1997) Platelet: transporter of vascular endothelial growth factor. Clin Cancer Res 3(12 Pt 1):2187-2190
14. Italiano JE Jr, Richardson JL, Patel-Hett S, Battinelli E, Zaslavsky A, Short S, Ryeom S, Folkman J, Klement GL (2008) Angiogenesis is regulated by a novel mechanism: pro- and antiangiogenic proteins are organized into separate platelet alpha granules and differentially released. Blood 111(3):1227-1233
15. Cedervall J, Olsson A-K (2012) Platelet regulation of angiogenesis, tumor growth and metastasis. In: Ran S (ed) Tumor angiogenesis. In Tech, ISBN 978-953-307-878-6, pp 115-134
16. Labelle M, Begum S, Hynes RO (2011) Direct signaling between platelets and cancer cells induces an epithelial-mesenchymal-like transition and promotes metastasis. Cancer Cell 20(5):576-590
17. Browder T, Folkman J, Pirie-Shepherd S (2000) The hemostatic system as a regulator of angiogenesis. J Biol Chem 275(3):1521-1524
18. Staton CA, Lewis CE (2005) Angiogenesis inhibitors found within the haemostasis pathway. J Cell Mol Med 9(2):286-302
19. Poon IK, Patel KK, Davis DS, Parish CR, Hulett MD (2011) Histidine-rich glycoprotein: the Swiss Army knife of mammalian plasma. Blood 117(7):2093-2101
20. Hulett MD, Parish CR (2000) Murine histidine-rich glycoprotein: cloning, characterization and cellular origin. Immunol Cell Biol 78(3):280-287
21. Lerch PG, Nydegger UE, Kuyas C, Haeberli A (1988) Histidine-rich glycoprotein binding to activated human platelets. Br J Haematol 70(2):219-224
22. Horne MK 3rd, Merryman PK, Cullinane AM (2001) Histidine-proline-rich glycoprotein binding to platelets mediated by transition metals. Thromb Haemost 85(5):890-895
23. Tsuchida-Straeten N, Ensslen S, Schafer C, Woltje M, Denecke B, Moser M, Graber S, Wakabayashi S, Koide T, Jahnen-Dechent W (2005) Enhanced blood coagulation and fibrinolysis in mice lacking histidine-rich glycoprotein (HRG). J Thromb Haemost 3(5):865-872
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, Olsson AK (2009) Activated platelets provide a functional microenvironment for the antiangiogenic fragment of histidine-rich glycoprotein. Mol Cancer Res 7(11):1792-1802
25. Workman P, Balmain A, Hickman JA, McNally NJ, Rohas AM, Mitchison NA, Pierrepoint CG, Raymond R, Rowlatt C, Stephens TC, et al. (1988) UKCCCR guidelines for the welfare of animals in experimental neoplasia. Lab Anim 22(3):195-201
26. Persson C, Savenhed C, Bourdeau A, Tremblay ML, Markova B, Bohmer FD, Haj FG, Neel BG, Elson A, Heldin CH, Ronnstrand L, Ostman A, Hellberg C (2004) Site-selective regulation of platelet-derived growth factor beta receptor tyrosine phosphorylation by T-cell protein tyrosine phosphatase. Mol Cell Biol 24(5):2190-2201
27. Korherr C, Gille H, Schafer R, Koenig-Hoffmann K, Dixelius J, Egland KA, Pastan I, Brinkmann U (2006) Identification of proangiogenic genes and pathways by high-throughput functional genomics: TBK1 and the IRF3 pathway. Proc Natl Acad Sci USA 103(11):4240-4245
28. Czabanka M, Korherr C, Brinkmann U, Vajkoczy P (2008) Influence of TBK-1 on tumor angiogenesis and microvascular inflammation. Front Biosci 13:7243-7249
29. Ou YH, Torres M, Ram R, Formstecher E, Roland C, Cheng T, Brekken R, Wurz R, Tasker A, Polverino T, Tan SL, White MA (2011) TBK1 directly engages Akt/PKB survival signaling to support oncogenic transformation. Mol Cell 41(4):458-470
30. Barbie DA, Tamayo P, Boehm JS, Kim SY, Moody SE, Dunn IF, Schinzel AC, Sandy P, Meylan E, Scholl C, Frohling S, Chan EM, Sos ML, Michel K, Mermel C, Silver SJ, Weir BA, Reiling JH, Sheng Q, Gupta PB, Wadlow RC, Le H, Hoersch S, Wittner BS, Ramaswamy S, Livingston DM, Sabatini DM, Meyerson M, Thomas RK, Lander ES, Mesirov JP, Root DE, Gilliland DG, Jacks T, Hahn WC (2009) Systematic RNA interference reveals that oncogenic KRAS-driven cancers require TBK1. Nature 462(7269):108-112
31. Villagrasa P, Diaz VM, Vinas-Castells R, Peiro S, Del Valle-Perez B, Dave N, Rodriguez-Asiain A, Casal JI, Lizcano JM, Dunach M, Garcia de Herreros A (2012) Akt2 interacts with Snail1 in the E-cadherin promoter. Oncogene 31(36):4022-4033
32. Cheng GZ, Chan J, Wang Q, Zhang W, Sun CD, Wang LH (2007) Twist transcriptionally up-regulates AKT2 in breast cancer cells leading to increased migration, invasion, and resistance to paclitaxel. Cancer Res 67(5):1979-1987
33. Chau NM, Ashcroft M (2004) Akt2: a role in breast cancer metastasis. Breast Cancer Res 6(1):55-57
34. Arboleda MJ, Lyons JF, Kabbinavar FF, Bray MR, Snow BE, Ayala R, Danino M, Karlan BY, Slamon DJ (2003) Overexpression of AKT2/protein kinase Bbeta leads to up-regulation of beta1 integrins, increased invasion, and metastasis of human breast and ovarian cancer cells. Cancer Res 63(1):196-206
35. Pietras K, Sjoblom T, Rubin K, Heldin CH, Ostman A (2003) PDGF receptors as cancer drug targets. Cancer Cell 3(5):439-443
36. Lindahl P, Johansson BR, Leveen P, Betsholtz C (1997) Pericyte loss and microaneurysm formation in PDGF-B-deficient mice. Science 277(5323):242-245
37. Lindblom P, Gerhardt H, Liebner S, Abramsson A, Enge M, Hellstrom M, Backstrom G, Fredriksson S, Landegren U, Nystrom HC, Bergstrom G, Dejana E, Ostman A, Lindahl P, Betsholtz C (2003) Endothelial PDGF-B retention is required for proper investment of pericytes in the microvessel wall. Genes Dev 17(15):1835-1840
38. Olsson AK, Dimberg A, Kreuger J, Claesson-Welsh L (2006) VEGF receptor signalling - in control of vascular function. Nat Rev Mol Cell Biol 7(5):359-371
39. Gotzmann J, Mikula M, Eger A, Schulte-Hermann R, Foisner R, Beug H, Mikulits W (2004) Molecular aspects of epithelial cell plasticity: implications for local tumor invasion and metastasis. Mutat Res 566(1):9-20
40. Jechlinger M, Sommer A, Moriggl R, Seither P, Kraut N, Capodiecci P, Donovan M, Cordon-Cardo C, Beug H, Grunert S (2006) Autocrine PDGFR signaling promotes mammary cancer metastasis. J Clin Invest 116(6):1561-1570
41. Gotzmann J, Fischer AN, Zojer M, Mikula M, Proell V, Huber H, Jechlinger M, Waerner T, Weith A, Beug H, Mikulits W (2006) A crucial function of PDGF in TGF-beta-mediated cancer progression of hepatocytes. Oncogene 25(22):3170-3185
42. Perl AK, Wilgenbus P, Dahl U, Semb H, Christofori G (1998) A causal role for E-cadherin in the transition from adenoma to carcinoma. Nature 392(6672):190-193
43. Pomerantz JL, Baltimore D (1999) NF-kappaB activation by a signaling complex containing TRAF2, TANK and TBK1, a novel IKK-related kinase. EMBO J 18(23):6694-6704
44. Smith CL, Baek ST, Sung CY, Tallquist MD (2011) Epicardial-derived cell epithelial-to-mesenchymal transition and fate specification require PDGF receptor signaling. Circ Res 108(12):e15-e26
45. Chen H, Gu X, Liu Y, Wang J, Wirt SE, Bottino R, Schorle H, Sage J, Kim SK (2011) PDGF signalling controls age-dependent proliferation in pancreatic beta-cells. Nature 478(7369):349-355
46. Tugues S, Honjo S, Konig C, Noguer O, Hedlund M, Botling J, Deschoemaeker S, Wenes M, Rolny C, Jahnen-Dechent W, Mazzone M, Claesson-Welsh L (2012) Genetic deficiency in plasma protein HRG enhances tumor growth and metastasis by exacerbating immune escape and vessel abnormalization. Cancer Res 72(8):1953-1963
47. 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, Carmeliet P (2011) HRG inhibits tumor growth and metastasis by inducing macrophage polarization and vessel normalization through downregulation of PlGF. Cancer Cell 19(1):31-44
48. Scull CM, Hays WD, Fischer TH (2010) Macrophage pro-inflammatory cytokine secretion is enhanced following interaction with autologous platelets. J Inflamm (Lond) 7:53
49. Ho-Tin-Noe B, Goerge T, Wagner DD (2009) Platelets: guardians of tumor vasculature. Cancer Res 69(14):5623-5626
50. Macquarrie JL, Stafford AR, Yau JW, Leslie BA, Vu TT, Fredenburgh JC, Weitz JI (2011) Histidine-rich glycoprotein binds factor XIIa with high affinity and inhibits contact-initiated coagulation. Blood 117(15):4134-4141
51. Vu TT, Stafford AR, Leslie BA, Kim PY, Fredenburgh JC, Weitz JI (2011) Histidine-rich glycoprotein binds fibrin(ogen) with high affinity and competes with thrombin for binding to the gamma'-chain. J Biol Chem 286(35):30314-30323
52. Bergers G, Javaherian K, Lo KM, Folkman J, Hanahan D (1999) Effects of angiogenesis inhibitors on multistage carcinogenesis in mice. Science 284(5415):808-812