Angptl4 is upregulated under inflammatory conditions in the bone marrow of mice, expands myeloid progenitors, and accelerates reconstitution of platelets after myelosuppressive therapy

Journal of Hematology and Oncology

Volumn 8, Issue 1, 2015, Pages

  Schumacher, Anne ^a   Denecke, Bernd ^a   Braunschweig, Till ^a   Stahlschmidt, Jasmin ^a   Ziegler, Susanne ^a   Brandenburg, Lars Ove ^b   Stope, Matthias B ^c   Martincuks, Antons ^a   Vogt, Michael ^a   Görtz, Dieter ^a   Camporeale, Annalisa ^d   Poli, Valeria ^d   Müller Newen, Gerhard ^a   Brümmendorf, Tim H ^a   Ziegler, Patrick ^a  

^a UNIVERSITY HOSPITAL RWTH AACHEN   (Germany)

^b RWTH AACHEN UNIVERSITY   (Germany)

^c UNIVERSITY MEDICINE GREIFSWALD   (Germany)

^d UNIVERSITY OF TURIN   (Italy)

Author keywords

Angptl4; Inflammatory conditions; Myelosuppressive therapy; Platelet reconstitution; STAT3

Indexed keywords

BETA3 INTEGRIN; FIBRINOGEN RECEPTOR; GLYCOPROTEIN; PROTEIN ANGPTL4; STAT3 PROTEIN; UNCLASSIFIED DRUG; ANGIOPOIETIN; ANGPTL4 PROTEIN, MOUSE; STAT3 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BONE MARROW SUPPRESSION; CELL DIFFERENTIATION; CELL PROLIFERATION; COLONY FORMING UNIT; CONTROLLED STUDY; CYTOKINE PRODUCTION; FEMALE; GENE CLUSTER; GENE EXPRESSION; HEMATOPOIETIC STEM CELL; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; MEGAKARYOCYTE; MEGAKARYOPOIESIS; MICROARRAY ANALYSIS; MOUSE; MYELOID PROGENITOR CELL; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; STEM CELL EXPANSION; THROMBOCYTE COUNT; UPREGULATION; ANIMAL; BONE MARROW; BONE MARROW CELL; CYTOLOGY; HUMAN; METABOLISM; THROMBOCYTE;

ANGIOPOIETINS; ANIMALS; BLOOD PLATELETS; BONE MARROW; FEMALE; HUMANS; MICE; MYELOID CELLS; STAT3 TRANSCRIPTION FACTOR; UP-REGULATION;

EID: 85018143451     PISSN: None     EISSN: 17568722     Source Type: Journal    
DOI: 10.1186/s13045-015-0152-2     Document Type: Article

References (67)

1. Kondo M, Wagers AJ, Manz MG, Prohaska SS, Scherer DC, Beilhack GF, et al. Biology of hematopoietic stem cells and progenitors: implications for clinical application. Annu Rev Immunol. 2003;21:759-806.
2. Metcalf D. Hematopoietic cytokines. Blood. 2008;111:485-91.
3. Ihle JN, Witthuhn BA, Quelle FW, Yamamoto K, Silvennoinen O. Signaling through the hematopoietic cytokine receptors. Annu Rev Immunol. 1995;13:369-98.
4. Kaushansky K. Lineage-specific hematopoietic growth factors. N Engl J Med. 2006;354:2034-45.
5. Kumar H, Kawai T, Akira S. Toll-like receptors and innate immunity. Biochem Biophys Res Commun. 2009;388:621-5.
6. Hamilton JA. Colony-stimulating factors in inflammation and autoimmunity. Nat Rev Immunol. 2008;8:533-44.
7. Kawakami M, Tsutsumi H, Kumakawa T, Abe H, Hirai M, Kurosawa S, et al. Levels of serum granulocyte colony-stimulating factor in patients with infections. Blood. 1990;76:1962-4.
8. Selig C, Nothdurft W. Cytokines and progenitor cells of granulocytopoiesis in peripheral blood of patients with bacterial infections. Infect Immun. 1995;63:104-9.
9. Boettcher S, Ziegler P, Schmid MA, Takizawa H, van Rooijen N, Kopf M, et al. Cutting edge: LPS-induced emergency myelopoiesis depends on TLR4-expressing nonhematopoietic cells. J Immunol. 2012;188:5824-8.
10. Hibbs ML, Quilici C, Kountouri N, Seymour JF, Armes JE, Burgess AW, et al. Mice lacking three myeloid colony-stimulating factors (G-CSF, GM-CSF, and M-CSF) still produce macrophages and granulocytes and mount an inflammatory response in a sterile model of peritonitis. J Immunol. 2007;178:6435-43.
11. Lieschke GJ, Grail D, Hodgson G, Metcalf D, Stanley E, Cheers C, et al. Mice lacking granulocyte colony-stimulating factor have chronic neutropenia, granulocyte and macrophage progenitor cell deficiency, and impaired neutrophil mobilization. Blood. 1994;84:1737-46.
12. Seymour JF, Lieschke GJ, Grail D, Quilici C, Hodgson G, Dunn AR. Mice lacking both granulocyte colony-stimulating factor (CSF) and granulocyte-macrophage CSF have impaired reproductive capacity, perturbed neonatal granulopoiesis, lung disease, amyloidosis, and reduced long-term survival. Blood. 1997;90:3037-49.
13. Basu S, Hodgson G, Zhang HH, Katz M, Quilici C, Dunn AR. «Emergency» granulopoiesis in G-CSF-deficient mice in response to Candida albicans infection. Blood. 2000;95:3725-33.
14. Walker F, Zhang HH, Matthews V, Weinstock J, Nice EC, Ernst M, et al. IL6/sIL6R complex contributes to emergency granulopoietic responses in G-CSF- and GM-CSF-deficient mice. Blood. 2008;111:3978-85.
15. Zambon AC, Gaj S, Ho I, Hanspers K, Vranizan K, Evelo CT, et al. GO-Elite: a flexible solution for pathway and ontology over-representation. Bioinformatics (Oxford, England). 2012;28:2209-10.
16. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, et al. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium Nature Genetics. 2000;25:25-9.
17. Petersen TN, Brunak S, von Heijne G, Nielsen H. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods. 2011;8:785-6.
18. Kim I, Kim HG, Kim H, Kim HH, Park SK, Uhm CS, et al. Hepatic expression, synthesis and secretion of a novel fibrinogen/angiopoietin-related protein that prevents endothelial-cell apoptosis. Biochem J. 2000;346(Pt 3):603-10.
19. Kersten S, Mandard S, Tan NS, Escher P, Metzger D, Chambon P, et al. Characterization of the fasting-induced adipose factor FIAF, a novel peroxisome proliferator-activated receptor target gene. J Biol Chem. 2000;275:28488-93.
20. Yoon JC, Chickering TW, Rosen ED, Dussault B, Qin Y, Soukas A, et al. Peroxisome proliferator-activated receptor gamma target gene encoding a novel angiopoietin-related protein associated with adipose differentiation. Mol Cell Biol. 2000;20:5343-9.
21. Zhang CC, Kaba M, Iizuka S, Huynh H, Lodish HF. Angiopoietin-like proteins stimulate ex vivo expansion of hematopoietic stem cells. Nat Med. 2006;12:240-5.
22. Zhang CC, Kaba M, Ge G, Xie K, Tong W, Hug C, et al. Angiopoietin-like 5 and IGFBP2 stimulate ex vivo expansion of human cord blood hematopoietic stem cells as assayed by NOD/SCID transplantation. Blood. 2008;111:3415-23.
23. Quinton LJ, Nelson S, Boé DM, Zhang P, Zhong Q, Kolls JK, et al. The granulocyte colony-stimulating factor response after intrapulmonary and systemic bacterial challenges. J Infect Dis. 2002;185:1476-82.
24. Ueda Y, Kondo M, Kelsoe G. Inflammation and the reciprocal production of granulocytes and lymphocytes in bone marrow. J Exp Med. 2005;201:1771-80.
25. Gerber J, Raivich G, Wellmer A, Noeske C, Kunst T, Werner A, et al. A mouse model of Streptococcus pneumoniae meningitis mimicking several features of human disease. Acta Neuropathol. 2001;101:499-508.
26. Malley R, Henneke P, Morse SC, Cieslewicz MJ, Lipsitch M, Thompson CM, et al. Recognition of pneumolysin by Toll-like receptor 4 confers resistance to pneumococcal infection. Proc Natl Acad Sci U S A. 2003;100:1966-71.
27. Lee KS, Scanga CA, Bachelder EM, Chen Q, Snapper CM. TLR2 synergizes with both TLR4 and TLR9 for induction of the MyD88-dependent splenic cytokine and chemokine response to Streptococcus pneumoniae. Cell Immunol. 2007;245:103-10.
28. Albiger B, Dahlberg S, Sandgren A, Wartha F, Beiter K, Katsuragi H, et al. Toll-like receptor 9 acts at an early stage in host defence against pneumococcal infection. Cell Microbiol. 2007;9:633-44.
29. Lagasse E, Weissman IL. Flow cytometric identification of murine neutrophils and monocytes. J Immunol Methods. 1996;197:139-50.
30. Jaiswal S, Weissman IL. Hematopoietic stem and progenitor cells and the inflammatory response. Ann N Y Acad Sci. 2009;1174:118-21.
31. Zhang P, Welsh DA, Siggins 2nd RW, Bagby GJ, Raasch CE, Happel KI, et al. Acute alcohol intoxication inhibits the lineage- c-kit+ Sca-1+ cell response to Escherichia coli bacteremia. J Immunol. 2009;182:1568-76.
32. Yoshida K, Shimizugawa T, Ono M, Furukawa H. Angiopoietin-like protein 4 is a potent hyperlipidemia-inducing factor in mice and inhibitor of lipoprotein lipase. J Lipid Res. 2002;43:1770-2.
33. Matsumura-Takeda K, Sogo S, Isakari Y, Harada Y, Nishioka K, Kawakami T, et al. CD41+/CD45+ cells without acetylcholinesterase activity are immature and a major megakaryocytic population in murine bone marrow. Stem Cells (Dayton, Ohio). 2007;25:862-70.
34. Caen JP, Han ZC, Bellucci S, Alemany M. Regulation of megakaryocytopoiesis. Haemostasis. 1999;29:27-40.
35. Hofmann WK, Ottmann OG, Hoelzer D. Memorial lecture. Megakaryocytic growth factors: is there a new approach for management of thrombocytopenia in patients with malignancies? Leukemia. 1999;13(1):S14-8.
36. MacVittie TJ, Farese AM, Patchen ML, Myers LA. Therapeutic efficacy of recombinant interleukin-6 (IL-6) alone and combined with recombinant human IL-3 in a nonhuman primate model of high-dose, sublethal radiation-induced marrow aplasia. Blood. 1994;84:2515-22.
37. Saitoh M, Taguchi K, Yasuda S, Kikumori M, Nishimori T, Suda M, et al. Thrombopoietic activity of recombinant human interleukin-11 in nonhuman primates with ACNU-induced thrombocytopenia. Interferon Cytokine Res. 2000;20:539-45.
38. Wagemaker G, Neelis KJ, Hartong SCC, Wognum AW, Thomas GR, Fielder PJ, et al. The efficacy of recombinant TPO in murine And nonhuman primate models for myelosuppression and stem cell transplantation. Stem Cells (Dayton, Ohio). 1998;16 Suppl 2:127-41.
39. Slayton WB, Georgelas A, Pierce LJ, Elenitoba-Johnson KS, Perry SS, Marx M, et al. The spleen is a major site of megakaryopoiesis following transplantation of murine hematopoietic stem cells. Blood. 2002;100:3975-82.
40. Zeigler FC, de Sauvage F, Widmer HR, Keller GA, Donahue C, Schreiber RD, et al. In vitro megakaryocytopoietic and thrombopoietic activity of c-mpl ligand (TPO) on purified murine hematopoietic stem cells. Blood. 1994;84:4045-52.
41. Kostyak JC, Naik UP. Megakaryopoiesis: transcriptional insights into megakaryocyte maturation. Front Biosci. 2007;12:2050-62.
42. Goldfarb AN. Transcriptional control of megakaryocyte development. Oncogene. 2007;26:6795-802.
43. Athanasiou M, Clausen PA, Mavrothalassitis GJ, Zhang XK, Watson DK, Blair DG. Increased expression of the ETS-related transcription factor FLI-1/ERGB correlates with and can induce the megakaryocytic phenotype. Cell Growth Differ. 1996;7:1525-34.
44. Wang X, Crispino JD, Letting DL, Nakazawa M, Poncz M, Blobel GA. Control of megakaryocyte-specific gene expression by GATA-1 and FOG-1: role of Ets transcription factors. EMBO J. 2002;21:5225-34.
45. Bastian LS, Kwiatkowski BA, Breininger J, Danner S, Roth G. Regulation of the megakaryocytic glycoprotein IX promoter by the oncogenic Ets transcription factor Fli-1. Blood. 1999;93:2637-44.
46. Drachman JG, Sabath DF, Fox NE, Kaushansky K. Thrombopoietin signal transduction in purified murine megakaryocytes. Blood. 1997;89:483-92.
47. Kirito K, Osawa M, Morita H, Shimizu R, Yamamoto M, Oda A, et al. A functional role of Stat3 in in vivo megakaryopoiesis. Blood. 2002;99:3220-7.
48. Shivdasani RA, Rosenblatt MF, Zucker-Franklin D, Jackson CW, Hunt P, Saris CJ, et al. Transcription factor NF-E2 is required for platelet formation independent of the actions of thrombopoietin/MGDF in megakaryocyte development. Cell. 1995;81:695-704.
49. Shivdasani RA. The role of transcription factor NF-E2 in megakaryocyte maturation and platelet production. Stem Cells (Dayton, Ohio). 1996;14 Suppl 1:112-5.
50. Ezumi Y, Takayama H, Okuma M. Thrombopoietin, c-Mpl ligand, induces tyrosine phosphorylation of Tyk2, JAK2, and STAT3, and enhances agonists-induced aggregation in platelets in vitro. FEBS Lett. 1995;374:48-52.
51. Pang L, Xue HH, Szalai G, Wang X, Wang Y, Watson DK, et al. Maturation stage-specific regulation of megakaryopoiesis by pointed-domain Ets proteins. Blood. 2006;108:2198-206.
52. Ezoe S, Matsumura I, Gale K, Satoh Y, Ishikawa J, Mizuki M, et al. GATA transcription factors inhibit cytokine-dependent growth and survival of a hematopoietic cell line through the inhibition of STAT3 activity. J Biol Chem. 2005;280:13163-70.
53. Zhu P, Goh YY, Chin HF, Kersten S, Tan NS. Angiopoietin-like 4: a decade of research. Biosci Rep. 2012;32:211-9.
54. Mandard S, Zandbergen F, van Straten E, Wahli W, Kuipers F, Müller M, et al. The fasting-induced adipose factor/angiopoietin-like protein 4 is physically associated with lipoproteins and governs plasma lipid levels and adiposity. J Biol Chem. 2006;281:934-44.
55. Romeo S, Yin W, Kozlitina J, Pennacchio LA, Boerwinkle E, Hobbs HH, et al. Rare loss-of-function mutations in ANGPTL family members contribute to plasma triglyceride levels in humans. J Clin Invest. 2009;119:70-9.
56. Ge H, Yang G, Huang L, Motola DL, Pourbahrami T, Li C. Oligomerization and regulated proteolytic processing of angiopoietin-like protein 4. J Biol Chem. 2004;279:2038-45.
57. Lu B, Moser A, Shigenaga JK, Grunfeld C, Feingold KR. The acute phase response stimulates the expression of angiopoietin like protein 4. Biochem Biophys Res Commun. 2010;391:1737-41.
58. Ortega-Senovilla H, Schaefer-Graf U, Meitzner K, Graf K, Abou-Dakn M, Herrera E. Lack of relationship between cord serum angiopoietin-like protein 4 (ANGPTL4) and lipolytic activity in human neonates born by spontaneous delivery. PLoS One. 2013;8, e81201.
59. Zheng J, Umikawa M, Cui C, Li J, Chen X, Zhang C, et al. Inhibitory receptors bind ANGPTLs and support blood stem cells and leukaemia development. Nature. 2012;485:656-60.
60. Nakorn TN, Miyamoto T, Weissman IL. Characterization of mouse clonogenic megakaryocyte progenitors. Proc Natl Acad Sci U S A. 2003;100:205-10.
61. Na Nakorn T, Traver D, Weissman IL, Akashi K. Myeloerythroid-restricted progenitors are sufficient to confer radioprotection and provide the majority of day 8 CFU-S. J Clin Invest. 2002;109:1579-85.
62. Jayachandran M, Brunn GJ, Karnicki K, Miller RS, Owen WG, Miller VM. In vivo effects of lipopolysaccharide and TLR4 on platelet production and activity: implications for thrombotic risk. J Appl Physiol (Bethesda, Md: 1985). 2007;102:429-33.
63. Stahl CP, Zucker-Franklin D, Evatt BL, Winton EF. Effects of human interleukin-6 on megakaryocyte development and thrombocytopoiesis in primates. Blood. 1991;78:1467-75.
64. Hill RJ, Warren MK, Levin J. Stimulation of thrombopoiesis in mice by human recombinant interleukin 6. J Clin Invest. 1990;85:1242-7.
65. Ishibashi T, Kimura H, Uchida T, Kariyone S, Friese P, Burstein SA. Human interleukin 6 is a direct promoter of maturation of megakaryocytes in vitro. Proc Natl Acad Sci U S A. 1989;86:5953-7.
66. Wickenhauser C, Lorenzen J, Thiele J, Hillienhof A, Jungheim K, Schmitz B, et al. Secretion of cytokines (interleukins-1 alpha, -3, and -6 and granulocyte-macrophage colony-stimulating factor) by normal human bone marrow megakaryocytes. Blood. 1995;85:685-91.
67. Fan X, Shi P, Dai J, Lu Y, Chen X, Liu X, et al. Paired immunoglobulin-like receptor B regulates platelet activation. Blood. 2014;124:2421-30.