Platelet factor 4 regulates megakaryopoiesis through low-density lipoprotein receptor-related protein 1 (LRP1) on megakaryocytes

Blood

Volumn 114, Issue 11, 2009, Pages 2290-2298

  Lambert, Michele P ^a,b   Wang, Yuhuan ^a   Bdeir, Khalil H ^b   Nguyen, Yvonne ^a   Kowalska, M Anna ^a,c   Poncz, Mortimer ^a,b  

^a CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c INSTITUTE OF MEDICAL BIOLOGY   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN; PROTEIN ANTIBODY; RAP PROTEIN; SHORT HAIRPIN RNA; THROMBOCYTE FACTOR 4; ANTIBODY; LOW DENSITY LIPOPROTEIN RECEPTOR; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN ASSOCIATED PROTEIN; LRP1 PROTEIN, MOUSE; TUMOR SUPPRESSOR PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BONE MARROW; CELL ISOLATION; CONTROLLED STUDY; GROWTH INHIBITION; HUMAN; HUMAN CELL; IN VIVO STUDY; MALE; MEGAKARYOCYTE; MEGAKARYOPOIESIS; MOUSE; NONHUMAN; PARACRINE SIGNALING; POLYPLOIDY; PRIORITY JOURNAL; PROTEIN EXPRESSION; STEM CELL; THROMBOCYTE COUNT; ANIMAL; CYTOLOGY; DRUG ANTAGONISM; DRUG EFFECT; ENDOTHELIUM CELL; ERYTHROID MEGAKARYOCYTE PROGENITOR CELL; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOUSE MUTANT; PHYSIOLOGY; THROMBOCYTOPOIESIS;

ANIMALS; ANTIBODIES; ENDOTHELIAL CELLS; GENE EXPRESSION REGULATION; HUMANS; LDL-RECEPTOR RELATED PROTEIN-ASSOCIATED PROTEIN; MEGAKARYOCYTE-ERYTHROID PROGENITOR CELLS; MEGAKARYOCYTES; MICE; MICE, KNOCKOUT; PARACRINE COMMUNICATION; PLATELET FACTOR 4; RECEPTORS, LDL; THROMBOPOIESIS; TUMOR SUPPRESSOR PROTEINS;

EID: 70349576961     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2009-04-216473     Document Type: Article

References (47)

1. Kaser A, Brandacher G, Steurer W, et al. Interleukin-6 stimulates thrombopoiesis through thrombopoietin: role in inflammatory thrombocytosis. Blood. 2001;98(9):2720-2725.
2. Majka M, Janowska-Wieczorek A, Ratajczak J, et al. Stromal-derived factor 1 and thrombopoietin regulate distinct aspects of human megakaryopoiesis. Blood. 2000;96(13):4142-4151.
3. Weich NS, Fitzgerald M, Wang A, et al. Recombinant human interleukin-11 synergizes with steel factor and interleukin-3 to promote directly the early stages of murine megakaryocyte development in vitro. Blood. 2000;95(2):503-509. (Pubitemid 30041662)
4. Pillai MM, Iwata M, Awaya N, Graf L, Torok-Storb B. Monocyte-derived CXCL7 peptides in the marrow microenvironment. Blood. 2006;107(9):3520-3526.
5. Gewirtz AM, Zhang J, Ratajczak J, et al. Chemokine regulation of human megakaryocytopoiesis. Blood. 1995;86(7):2559-2567.
6. Majka M, Janowska-Wieczorek A, Ratajczak J, et al. Numerous growth factors, cytokines, and chemokines are secreted by human CD34(+) cells, myeloblasts, erythroblasts, and megakaryoblasts and regulate normal hematopoiesis in an autocrine/paracrine manner. Blood. 2001;97(10):3075-3085.
7. Lambert MP, Rauova L, Bailey M, Sola-Visner MC, Kowalska MA, Poncz M. Platelet factor 4 is a negative autocrine in vivo regulator of megakaryopoiesis: clinical and therapeutic implications. Blood. 2007;110(4):1153-1160. (Pubitemid 47281411)
8. Briquet-Laugier V, Lavenu-Bombled C, Schmitt A, et al. Probing platelet factor 4 alpha-granule targeting. J Thromb Haemost. 2004;2(12):2231-2240. (Pubitemid 40185786)
9. Luster AD, Greenberg SM, Leder P. The IP-10 chemokine binds to a specific cell surface heparan sulfate site shared with platelet factor 4 and inhibits endothelial cell proliferation. J Exp Med. 1995;182(1):219-231.
10. Sato Y, Waki M, Ohno M, Kuwano M, Sakata T. Carboxyl-terminal heparin-binding fragments of platelet factor 4 retain the blocking effect on the receptor binding of basic fibroblast growth factor. Jpn J Cancer Res. 1993;84(5):485-488. (Pubitemid 23193803)
11. Maurer AM, Han ZC, Dhermy D, Briere J. Inhibitory effect of platelet factor 4 on human erythroleukemic cells is dependent on cell surface heparan sulfate. J Lab Clin Med. 1996;127(4):382-390. (Pubitemid 126657320)
12. Yu G, Rux AH, Ma P, Bdeir K, Sachais BS. Endothelial expression of E-selectin is induced by the platelet-specific chemokine platelet factor 4 through LRP in an NF-kappaB-dependent manner. Blood. 2005;105(9):3545-3551. (Pubitemid 40628199)
13. Zhang C, Thornton MA, Kowalska MA, et al. Localization of distal regulatory domains in the megakaryocyte-specific platelet basic protein/platelet factor 4 gene locus. Blood. 2001;98(3):610-617.
14. Eslin DE, Zhang C, Samuels KJ, et al. Transgenic mice studies demonstrate a role for platelet factor 4 in thrombosis: dissociation between anticoagulant and antithrombotic effect of heparin. Blood. 2004;104(10):3173-3180. (Pubitemid 39507132)
15. Poncz M, Rauova L, Cines DB. The role of surface PF4: glycosaminoglycan complexes in the pathogenesis of heparin-induced thrombocytopenia (HIT). Pathophysiol Haemost Thromb. 2006;35(1-2):46-49. (Pubitemid 44350164)
16. Park KS, Rifat S, Eck H, Adachi K, Surrey S, Poncz M. Biologic and biochemic properties of recombinant platelet factor 4 demonstrate identity with the native protein. Blood. 1990;75(6):1290-1295. (Pubitemid 20107296)
17. Jackson CW, Brown LK, Somerville BC, Lyles SA, Look AT. Two-color flow cytometric measurement of DNA distributions of rat megakaryocytes in unfixed, unfractionated marrow cell suspensions. Blood. 1984;63(4):768-778.
18. Bouchard BA, Meisler NT, Nesheim ME, Liu CX, Strickland DK, Tracy PB. A unique function for LRP-1: a component of a two-receptor system mediating specific endocytosis of plasma-derived factor V by megakaryocytes. J Thromb Haemost. 2008;6(4):638-644.
19. National Center for Biotechnology Information. Primer-BLAST. http://www.ncbi.nlm.nih.gov/tools/primer-blast. Accessed December 19, 2005.
20. Zemskov EA, Mikhailenko I, Strickland DK, Belkin AM. Cell-surface transglutaminase undergoes internalization and lysosomal degradation: an essential role for LRP1. J Cell Sci. 2007;120(pt 18):3188-3199. (Pubitemid 350018410)
21. Nilsson SK, Christensen S, Raarup MK, Ryan RO, Nielsen MS, Olivecrona G. Endocytosis of apolipoprotein A-V by members of the low density lipoprotein receptor and the VPS10p domain receptor families. J Biol Chem. 2008;283(38):25920-25927.
22. Fuss IJ, Kanof ME, Smith PD, Zola H. Isolation of whole mononuclear cells from peripheral blood and cord blood. Curr Protoc Immunol. 2009; Chapter 7:Unit7.1.
23. Spangrude GJ, Heimfeld S, Weissman IL. Purification and characterization of mouse hematopoietic stem cells. Science. 1988;241(4861):58-62. (Pubitemid 18168116)
24. Long MW, WIlliams N. Immature megakaryocytes in the mouse: morphology and quantitation by acetylcholinesterase staining. Blood. 1981;58(5):1032-1039.
25. Naldini L, Blomer U, Gage FH, Trono D, Verma IM. Efficient transfer, integration, and sustained long-term expression of the transgene in adult rat brains injected with a lentiviral vector. Proc Natl Acad Sci U S A. 1996;93(21):11382-11388. (Pubitemid 26347130)
26. Terada H, Tsutsui J, Sanada J, Arima T, Ozawa M. Heparin binding protein-44 (HBP-44)/receptor-associated protein (RAP) mediates cell-substratum adhesion of mouse NIH/3T3 cells through its binding to low density lipoprotein (LDL) receptor-related protein (LRP). Mol Membr Biol. 1997;14(2):81-86. (Pubitemid 27356742)
27. Stachura DL, Chou ST, Weiss MJ. Early block to erythromegakaryocytic development conferred by loss of transcription factor GATA-1. Blood. 2006;107(1):87-97.
28. Chou ST, Opalinska JB, Yao Y, et al. Trisomy 21 enhances human fetal erythro-megakaryocytic development. Blood. 2008;112(12):4503-4506.
29. Doucette TA, Ryan CL, Tasker RA. Use of osmotic minipumps for sustained drug delivery in rat pups: effects on physical and neurobehavioural development. Physiol Behav. 2000;71(1-2):207-212.
30. Mayadas TN, Cullere X. Neutrophil beta2 integrins: moderators of life or death decisions. Trends Immunol. 2005;26(7):388-395. (Pubitemid 40835845)
31. Ceschin DG, Sanchez MC, Chiabrando GA. Insulin induces the low density lipoprotein receptor-related protein 1 (LRP1) degradation by the proteasomal system in J774 macrophage-derived cells. J Cell Biochem. 2009;106(3):372-380.
32. Gewirtz AM, Calabretta B, Rucinski B, Niewiarowski S, Xu WY. Inhibition of human megakaryocytopoiesis in vitro by platelet factor 4 (PF4) and a synthetic COOH-terminal PF4 peptide. J Clin Invest. 1989;83(5):1477-1486. (Pubitemid 19124100)
33. Lillis AP, Van Duyn LB, Murphy-Ullrich JE, Strickland DK. LDL receptor-related protein 1: unique tissue-specific functions revealed by selective gene knockout studies. Physiol Rev. 2008;88(3):887-918.
34. Suvarna S, Espinasse B, Qi R, et al. Determinants of PF4/heparin immunogenicity. Blood. 2007;110(13):4253-4260.
35. Greinacher A, Gopinadhan M, Gunther JU, et al. Close approximation of two platelet factor 4 tetramers by charge neutralization forms the antigens recognized by HIT antibodies. Arterioscler Thromb Vasc Biol. 2006;26(10):2386-2393. (Pubitemid 44465738)
36. Lasagni L, Francalanci M, Annunziato F, et al. An alternatively spliced variant of CXCR3 mediates the inhibition of endothelial cell growth induced by IP-10, Mig, and I-TAC, and acts as functional receptor for platelet factor 4. J Exp Med. 2003;197(11):1537-1549. (Pubitemid 36682550)
37. Kowalska MA, Mahmud SA, Lambert MP, Poncz M, Slungaard A. Endogenous platelet factor 4 stimulates activated protein C generation in vivo and improves survival after thrombin or lipopolysaccharide challenge. Blood. 2007;110(6):1903-1905. (Pubitemid 47443903)
38. May P, Woldt E, Matz RL, Boucher P. The LDL receptor-related protein (LRP) family: an old family of proteins with new physiological functions. Ann Med. 2007;39(3):219-228. (Pubitemid 46676481)
39. May P, Herz J, Bock HH. Molecular mechanisms of lipoprotein receptor signalling. Cell Mol Life Sci. 2005;62(19-20):2325-2338. (Pubitemid 41500548)
40. May P, Bock HH, Herz J. Integration of endocytosis and signal transduction by lipoprotein receptors. Sci STKE. 2003;2003(176):PE12.
41. Huang SS, Ling TY, Tseng WF, et al. Cellular growth inhibition by IGFBP-3 and TGF-beta1 requires LRP-1. FASEB J. 2003;17(14):2068-2081.
42. Houwerzijl EJ, Blom NR, van der Want JJ, et al. Ultrastructural study shows morphologic features of apoptosis and para-apoptosis in megakaryocytes from patients with idiopathic thrombocytopenic purpura. Blood. 2004;103(2):500-506.
43. Bussel JB, Cheng G, Saleh MN, et al. Eltrombopag for the treatment of chronic idiopathic thrombocytopenic purpura. N Engl J Med. 2007;357(22):2237- 2247. (Pubitemid 350190754)
44. Bussel JB, Kuter DJ, Pullarkat V, Lyons RM, Guo M, Nichol JL. Safety and efficacy of long-term treatment with romiplostim in thrombocytopenic patients with chronic ITP. Blood. 2009;113(10):2161-2171.
45. Kuter DJ, Bussel JB, Lyons RM, et al. Efficacy of romiplostim in patients with chronic immune thrombocytopenic purpura: a double-blind randomised controlled trial. Lancet. 2008;371(9610):395-403. (Pubitemid 351181334)
46. Kuter DJ. Thrombopoietin and thrombopoietin mimetics in the treatment of thrombocytopenia. Annu Rev Public Health. 2009;60:193-206.
47. Kuter DJ. New drugs for familiar therapeutic targets: thrombopoietin receptor agonists and immune thrombocytopenic purpura. Eur J Haematol Suppl. 2008;(69):9-18.