Platelets from mice lacking the aryl hydrocarbon receptor exhibit defective collagen-dependent signaling

Journal of Thrombosis and Haemostasis

Volumn 12, Issue 3, 2014, Pages 383-394

  Lindsey, S ^a   Jiang, J ^a   Woulfe, D ^a   Papoutsakis, E T ^a  

^a UNIVERSITY OF DELAWARE   (United States)

Author keywords

Aryl hydrocarbon receptor; Blood platelets; Cell adhesion; Collagen; Platelet activation; Platelet aggregation

Indexed keywords

ADENOSINE DIPHOSPHATE; ANTITHROMBOCYTIC AGENT; AROMATIC HYDROCARBON RECEPTOR; ARYL HYDROCARBON RECEPTOR INHIBITOR; COLLAGEN; FIBRINOGEN; PHOSPHOLIPASE C GAMMA2; PROTEINASE ACTIVATED RECEPTOR; PROTEINASE ACTIVATED RECEPTOR 4; RAC PROTEIN; RAC1 PROTEIN; THROMBIN; THROMBOPOIETIN; UNCLASSIFIED DRUG; VAV PROTEIN; VAV1 PROTEIN; VAV3 PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BLEEDING; BONE MARROW; CELL DIFFERENTIATION; CELL SPREADING; CONTROLLED STUDY; EX VIVO STUDY; FEMALE; MALE; MEGAKARYOCYTE; MEGAKARYOPOIESIS; MOUSE; NONHUMAN; PHENOTYPE; POLYPLOIDY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; RECEPTOR DOWN REGULATION; SIGNAL TRANSDUCTION; STEM CELL; THROMBOCYTE; THROMBOCYTE ACTIVATION; THROMBOCYTE AGGREGATION; THROMBOCYTE FUNCTION; WESTERN BLOTTING; WILD TYPE;

ARYL HYDROCARBON RECEPTOR; BLOOD PLATELETS; CELL ADHESION; COLLAGEN; PLATELET ACTIVATION; PLATELET AGGREGATION;

ANIMALS; BLOOD PLATELETS; BONE MARROW CELLS; CELL DIFFERENTIATION; COLLAGEN; FEMALE; HEMORRHAGE; HEMOSTASIS; LIGANDS; MALE; MEGAKARYOCYTES; MICE; MICE, KNOCKOUT; PHENOTYPE; PLATELET ACTIVATION; PLATELET AGGREGATION; PLOIDIES; RECEPTORS, ARYL HYDROCARBON; SIGNAL TRANSDUCTION; STEM CELLS; THROMBOPOIETIN;

EID: 84896782441     PISSN: 15387933     EISSN: 15387836     Source Type: Journal    
DOI: 10.1111/jth.12490     Document Type: Article

References (32)

1. Nieswandt B, Watson SP. Platelet-collagen interaction: is GPVI the central receptor? Blood 2003; 102: 449-61.
2. Watson SP, Gibbins J. Collagen receptor signalling in platelets: extending the role of the ITAM. Immunol Today 1998; 19: 260-4.
3. Nieswandt B, Brakebusch C, Bergmeier W, Schulte V, Bouvard D, Mokhtari-Nejad R, Lindhout T, Heemskerk JW, Zirngibl H, Fassler R. Glycoprotein VI but not alpha2beta1 integrin is essential for platelet interaction with collagen. EMBO J 2001; 20: 2120-30.
4. Jung SM, Moroi M. Platelets interact with soluble and insoluble collagens through characteristically different reactions. J Biol Chem 1998; 273: 14827-37.
5. Jung SM, Moroi M. Signal-transducing mechanisms involved in activation of the platelet collagen receptor integrin alpha(2)beta(1). J Biol Chem 2000; 275: 8016-26.
6. Goto S, Tamura N, Handa S, Arai M, Kodama K, Takayama H. Involvement of glycoprotein VI in platelet thrombus formation on both collagen and von Willebrand factor surfaces under flow conditions. Circulation 2002; 106: 266-72.
7. Holtkotter O, Nieswandt B, Smyth N, Muller W, Hafner M, Schulte V, Krieg T, Eckes B. Integrin alpha 2-deficient mice develop normally, are fertile, but display partially defective platelet interaction with collagen. J Biol Chem 2002; 277: 10789-94.
8. Kuijpers MJ, Schulte V, Bergmeier W, Lindhout T, Brakebusch C, Offermanns S, Fassler R, Heemskerk JW, Nieswandt B. Complementary roles of glycoprotein VI and alpha2beta1 integrin in collagen-induced thrombus formation in flowing whole blood ex vivo. FASEB J 2003; 17: 685-7.
9. Lindsey S, Papoutsakis ET. The evolving role of the aryl hydrocarbon receptor (AHR) in the normophysiology of hematopoiesis. Stem Cell Rev 2012; 8: 1223-35.
10. Lindsey S, Papoutsakis ET. The aryl hydrocarbon receptor (AHR) transcription factor regulates megakaryocytic polyploidization. Br J Haematol 2011; 152: 469-84.
11. Schmidt JV, Su GH, Reddy JK, Simon MC, Bradfield CA. Characterization of a murine Ahr null allele: involvement of the Ah receptor in hepatic growth and development. Proc Natl Acad Sci USA 1996; 93: 6731-6.
12. Konieczna I, Horvath E, Wang H, Lindsey S, Saberwal G, Bei L, Huang W, Platanias L, Eklund EA. Constitutive activation of SHP2 in mice cooperates with ICSBP deficiency to accelerate progression to acute myeloid leukemia. J Clin Invest 2008; 118: 853-67.
13. Lindsey S, Huang W, Wang H, Horvath E, Zhu C, Eklund EA. Activation of SHP2 protein-tyrosine phosphatase increases HoxA10-induced repression of the genes encoding gp91(PHOX) and p67(PHOX). J Biol Chem 2007; 282: 2237-49.
14. Apostolidis PA, Lindsey S, Miller WM, Papoutsakis ET. Proposed megakaryocytic regulon of p53: the genes engaged to control cell cycle and apoptosis during megakaryocytic differentiation. Physiol Genomics 2012; 44: 638-50.
15. Goodman SL. Sheep, pig, and human platelet-material interactions with model cardiovascular biomaterials. J Biomed Mater Res 1999; 45: 240-50.
16. Lindsey S, Zhu C, Lu YF, Eklund EA. HoxA10 represses transcription of the gene encoding p67phox in phagocytic cells. J Immunol 2005; 175: 5269-79.
17. Chetty S, Pagliuca FW, Honore C, Kweudjeu A, Rezania A, Melton DA. A simple tool to improve pluripotent stem cell differentiation. Nat Methods 2013; 10: 553-6.
18. Pal R, Mamidi MK, Das AK, Bhonde R. Diverse effects of dimethyl sulfoxide (DMSO) on the differentiation potential of human embryonic stem cells. Arch Toxicol 2012; 86: 651-61.
19. Preisler HD, Giladi M. Differentiation of erythroleukemic cells in vitro: irreversible induction by dimethyl sulfoxide (DMSO). J Cell Physiol 1975; 85: 537-46.
20. van Roozendaal KE, Darling D, Farzaneh F. DMSO and retinoic acid induce HL-60 differentiation by different but converging pathways. Exp Cell Res 1990; 190: 137-40.
21. Hirabayashi Y, Inoue T. Aryl hydrocarbon receptor biology and xenobiotic responses in hematopoietic progenitor cells. Biochem Pharmacol 2009; 77: 521-35.
22. Teske S, Bohn AA, Hogaboam JP, Lawrence BP. Aryl hydrocarbon receptor targets pathways extrinsic to bone marrow cells to enhance neutrophil recruitment during influenza virus infection. Toxicol Sci 2008; 102: 89-99.
23. Carvajal-Gonzalez JM, Mulero-Navarro S, Roman AC, Sauzeau V, Merino JM, Bustelo XR, Fernandez-Salguero PM. The dioxin receptor regulates the constitutive expression of the vav3 proto-oncogene and modulates cell shape and adhesion. Mol Biol Cell 2009; 20: 1715-27.
24. Sauzeau V, Carvajal-Gonzalez JM, Riolobos AS, Sevilla MA, Menacho-Marquez M, Roman AC, Abad A, Montero MJ, Fernandez-Salguero P, Bustelo XR. Transcriptional factor aryl hydrocarbon receptor (Ahr) controls cardiovascular and respiratory functions by regulating the expression of the Vav3 proto-oncogene. J Biol Chem 2011; 286: 2896-909.
25. Pearce AC, Senis YA, Billadeau DD, Turner M, Watson SP, Vigorito E. Vav1 and vav3 have critical but redundant roles in mediating platelet activation by collagen. J Biol Chem 2004; 279: 53955-62.
26. Kreutz RP, Breall JA, Kreutz Y, Owens J, Lu D, Bolad I, von der Lohe E, Sinha A, Flockhart DA. Protease activated receptor-1 (PAR-1) mediated platelet aggregation is dependent on clopidogrel response. Thromb Res 2012; 130: 198-202.
27. Ou X, Ramos KS. Regulation of cytochrome P4501A1 gene expression in vascular smooth muscle cells through aryl hydrocarbon receptor-mediated signal transduction requires a protein synthesis inhibitor. Arch Biochem Biophys 1995; 316: 116-22.
28. Brake PB, Zhang L, Jefcoate CR. Aryl hydrocarbon receptor regulation of cytochrome P4501B1 in rat mammary fibroblasts: evidence for transcriptional repression by glucocorticoids. Mol Pharmacol 1998; 54: 825-33.
29. Smith BW, Rozelle SS, Leung A, Ubellacker J, Parks A, Nah SK, French D, Gadue P, Monti S, Chui DH, Steinberg MH, Frelinger AL, Michelson AD, Theberge R, McComb ME, Costello CE, Kotton DN, Mostoslavsky G, Sherr DH, Murphy GJ. The aryl hydrocarbon receptor directs hematopoietic progenitor cell expansion and differentiation. Blood 2013; 122: 376-85.
30. Sauvageau G, Humphries RK. Medicine. The blood stem cell Holy Grail? Science 2010; 329: 1291-2.
31. Miyakawa Y, Oda A, Druker BJ, Ozaki K, Handa M, Ohashi H, Ikeda Y. Thrombopoietin and thrombin induce tyrosine phosphorylation of Vav in human blood platelets. Blood 1997; 89: 2789-98.
32. Pearce AC, Wilde JI, Doody GM, Best D, Inoue O, Vigorito E, Tybulewicz VL, Turner M, Watson SP. Vav1, but not Vav2, contributes to platelet aggregation by CRP and thrombin, but neither is required for regulation of phospholipase C. Blood 2002; 100: 3561-9.