IL-1α induces thrombopoiesis through megakaryocyte rupture in response to acute platelet needs

Journal of Cell Biology

Volumn 209, Issue 3, 2015, Pages 453-466

  Nishimura, Satoshi ^a,b,c   Nagasaki, Mika ^a   Kunishima, Shinji ^d   Sawaguchi, Akira ^e   Sakata, Asuka ^b   Sakaguchi, Hiroyasu ^f   Ohmori, Tsukasa ^b   Manabe, Ichiro ^a   Italiano, Joseph E ^g   Ryu, Tomiko ^h   Takayama, Naoya ⁱ   Komuro, Issei ^a   Kadowaki, Takashi ^a   Eto, Koji ⁱ   Nagai, Ryozo ^b  

^a UNIVERSITY OF TOKYO   (Japan)

^b JICHI MEDICAL UNIVERSITY   (Japan)

^c JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^d NATIONAL HOSPITAL ORGANIZATION NAGOYA MEDICAL CENTER   (Japan)

^e UNIVERSITY OF MIYAZAKI   (Japan)

^f Web Solution Group   (Japan)

^g BOSTON CHILDREN S HOSPITAL   (United States)

^h Social Insurance Central General Hospital   (Japan)

ⁱ KYOTO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; FAS LIGAND; INTERLEUKIN 1 RECEPTOR TYPE I; INTERLEUKIN 1ALPHA; THROMBOPOIETIN; TUBULIN; CASP3 PROTEIN, MOUSE; FASL PROTEIN, MOUSE; IL1R1 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; BIOGENESIS; CELL DIFFERENTIATION; CELL LOSS; CELL MATURATION; CELL MEMBRANE; CONTROLLED STUDY; ENZYME ACTIVATION; FETUS; MEGAKARYOCYTE; MEMBRANE STRUCTURE; MICROTUBULE ASSEMBLY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; THROMBOCYTE; THROMBOCYTE COUNT; THROMBOCYTE RELEASE REACTION; THROMBOCYTOPOIESIS; ANIMAL; CYTOLOGY; GENETICS; METABOLISM; PHYSIOLOGY; TRANSGENIC MOUSE;

ANIMALS; APOPTOSIS; BLOOD PLATELETS; CASPASE 3; FAS LIGAND PROTEIN; INTERLEUKIN-1ALPHA; MEGAKARYOCYTES; MICE; MICE, TRANSGENIC; RECEPTORS, INTERLEUKIN-1 TYPE I; THROMBOPOIESIS; THROMBOPOIETIN;

EID: 84938326619     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201410052     Document Type: Article

References (39)

1. Ahn, H.J., I.P. Sohn, H.C. Kwon, D.H. Jo, Y.D. Park, and C.K. Min. 2002. Characteristics of the cell membrane fluidity, actin fibers, and mitochondrial dysfunctions of frozen-thawed two-cell mouse embryos. Mol. Reprod. Dev. 61:466-476. http://dx.doi.org/10.1002/mrd.10040.
2. Avanzi, M.P., and W.B. Mitchell. 2014. Ex vivo production of platelets from stem cells. Br. J. Haematol. 165:237-247. http://dx.doi.org/10.1111/bjh.12764.
3. Beaulieu, L.M., E. Lin, E. Mick, M. Koupenova, E.O. Weinberg, C.D. Kramer, C.A. Genco, K. Tanriverdi, M.G. Larson, E.J. Benjamin, and J.E. Freedman. 2014. Interleukin 1 receptor 1 and interleukin 1β regulate megakaryocyte maturation, platelet activation, and transcript profile during inflammation in mice and humans. Arterioscler. Thromb. Vasc. Biol. 34:552-564. http://dx.doi.org/10.1161/ATVBAHA.113.302700.
4. Bosch, M., and V.E. Franklin-Tong. 2007. Temporal and spatial activation of caspase-like enzymes induced by self-incompatibility in Papaver pollen. Proc. Natl. Acad. Sci. USA. 104:18327-18332. http://dx.doi.org/10.1073/pnas.0705826104.
5. Clarke, M.C., J. Savill, D.B. Jones, B.S. Noble, and S.B. Brown. 2003. Compartmentalized megakaryocyte death generates functional platelets committed to caspase-independent death. J. Cell Biol. 160:577-587. http://dx.doi.org/10.1083/jcb.200210111.
6. De Botton, S., S. Sabri, E. Daugas, Y. Zermati, J.E. Guidotti, O. Hermine, G. Kroemer, W. Vainchenker, and N. Debili. 2002. Platelet formation is the consequence of caspase activation within megakaryocytes. Blood. 100:1310-1317. http://dx.doi.org/10.1182/blood-2002-03-0686.
7. De Cuyper, I.M., M. Meinders, E. van de Vijver, D. de Korte, L. Porcelijn, M. de Haas, J.A. Eble, K. Seeger, S. Rutella, D. Pagliara, et al. 2013. A novel flow cytometry-based platelet aggregation assay. Blood. 121:e70-e80. http://dx.doi.org/10.1182/blood-2012-06-437723.
8. de Sauvage, F.J., P.E. Hass, S.D. Spencer, B.E. Malloy, A.L. Gurney, S.A. Spencer, W.C. Darbonne, W.J. Henzel, S.C. Wong, W.J. Kuang, et al. 1994. Stimulation of megakaryocytopoiesis and thrombopoiesis by the c-Mpl ligand. Nature. 369:533-538. http://dx.doi.org/10.1038/369533a0.
9. de Sauvage, F.J., K. Carver-Moore, S.M. Luoh, A. Ryan, M. Dowd, D.L. Eaton, and M.W. Moore. 1996. Physiological regulation of early and late stages of megakaryocytopoiesis by thrombopoietin. J. Exp. Med. 183:651-656. http://dx.doi.org/10.1084/jem.183.2.651.
10. Denis, M.M., N.D. Tolley, M. Bunting, H. Schwertz, H. Jiang, S. Lindemann, C.C. Yost, F.J. Rubner, K.H. Albertine, K.J. Swoboda, et al. 2005. Escaping the nuclear confines: signal-dependent pre-mRNA splicing in anucleate platelets. Cell. 122:379-391. http://dx.doi.org/10.1016/j.cell.2005.06.015.
11. Eto, K., H. Nishikii, T. Ogaeri, S. Suetsugu, A. Kamiya, T. Kobayashi, D. Yamazaki, A. Oda, T. Takenawa, and H. Nakauchi. 2007. The WAVE2/Abi1 complex differentially regulates megakaryocyte development and spreading: implications for platelet biogenesis and spreading machinery. Blood. 110:3637-3647. http://dx.doi.org/10.1182/blood-2007-04-085860.
12. Horai, R., M. Asano, K. Sudo, H. Kanuka, M. Suzuki, M. Nishihara, M. Takahashi, and Y. Iwakura. 1998. Production of mice deficient in genes for interleukin (IL)-1α, IL-1β, IL-1α/γ, and IL-1 receptor antagonist shows that IL-1β is crucial in turpentine-induced fever development and glucocorticoid secretion. J. Exp. Med. 187:1463-1475. http://dx.doi.org/10.1084/jem.187.9.1463.
13. Italiano, J.E., Jr., P. Lecine, R.A. Shivdasani, and J.H. Hartwig. 1999. Blood platelets are assembled principally at the ends of proplatelet processes produced by differentiated megakaryocytes. J. Cell Biol. 147:1299-1312. http://dx.doi.org/10.1083/jcb.147.6.1299.
14. Jiang, J., D.S. Woulfe, and E.T. Papoutsakis. 2014. Shear enhances thrombopoiesis and formation of microparticles that induce megakaryocytic differentiation of stem cells. Blood. 124:2094-2103. http://dx.doi.org/10.1182/blood-2014-01-547927.
15. Josefsson, E.C., D.L. Burnett, M. Lebois, M.A. Debrincat, M.J. White, K.J. Henley, R.M. Lane, D. Moujalled, S.P. Preston, L.A. O'Reilly, et al. 2014. Platelet production proceeds independently of the intrinsic and extrinsic apoptosis pathways. Nat. Commun. 5:3455. http://dx.doi.org/10.1038/ncomms4455.
16. Junt, T., H. Schulze, Z. Chen, S. Massberg, T. Goerge, A. Krueger, D.D. Wagner, T. Graf, J.E. Italiano Jr., R.A. Shivdasani, and U.H. von Andrian. 2007. Dynamic visualization of thrombopoiesis within bone marrow. Science. 317:1767-1770. http://dx.doi.org/10.1126/science.1146304.
17. Kaushansky, K. 2003. Thrombopoietin: a tool for understanding thrombopoiesis. J. Thromb. Haemost. 1:1587-1592. http://dx.doi.org/10.1046/j.1538-7836.2003.00273.x.
18. Kowata, S., S. Isogai, K. Murai, S. Ito, K. Tohyama, M. Ema, J. Hitomi, and Y. Ishida. 2014. Platelet demand modulates the type of intravascular protrusion of megakaryocytes in bone marrow. Thromb. Haemost. 112:743-756. http://dx.doi.org/10.1160/TH14-02-0123.
19. Kunishima, S., S. Nishimura, H. Suzuki, M. Imaizumi, and H. Saito. 2014. TUBB1 mutation disrupting microtubule assembly impairs proplatelet 20121090 formation and results in congenital macrothrombocytopenia. Eur. J. Haematol. 92:276-282. http://dx.doi.org/10.1111/ejh.12252.
20. Kuter, D.J. 2007. New thrombopoietic growth factors. Blood. 109:4607-4616. http://dx.doi.org/10.1182/blood-2006-10-019315.
21. Machlus, K.R., J.N. Thon, and J.E. Italiano Jr. 2014. Interpreting the developmental dance of the megakaryocyte: a review of the cellular and molecular processes mediating platelet formation. Br. J. Haematol. 165:227-236. http://dx.doi.org/10.1111/bjh.12758.
22. Matsumura, H., H. Hasuwa, N. Inoue, M. Ikawa, and M. Okabe. 2004. Lineagespecific cell disruption in living mice by Cre-mediated expression of diphtheria toxin A chain. Biochem. Biophys. Res. Commun. 321:275-279. http://dx.doi.org/10.1016/j.bbrc.2004.06.139.
23. Nakamura-Ishizu, A., K. Takubo, M. Fujioka, and T. Suda. 2014. Megakaryocytes are essential for HSC quiescence through the production of thrombopoietin. Biochem. Biophys. Res. Commun. 454:353-357. http://dx.doi.org/10.1016/j.bbrc.2014.10.095.
24. Nambu, A., S. Nakae, and Y. Iwakura. 2006. IL-1beta, but not IL-1alpha, is required for antigen-specific T cell activation and the induction of local inflammation in the delayed-type hypersensitivity responses. Int. Immunol. 18:701-712. http://dx.doi.org/10.1093/intimm/dxl007.
25. Ng, A.P., M. Kauppi, D. Metcalf, C.D. Hyland, E.C. Josefsson, M. Lebois, J.G. Zhang, T.M. Baldwin, L. Di Rago, D.J. Hilton, and W.S. Alexander. 2014. Mpl expression on megakaryocytes and platelets is dispensable for thrombopoiesis but essential to prevent myeloproliferation. Proc. Natl. Acad. Sci. USA. 111:5884-5889. http://dx.doi.org/10.1073/pnas.1404354111.
26. Nishimura, S., I. Manabe, M. Nagasaki, K. Seo, H. Yamashita, Y. Hosoya, M. Ohsugi, K. Tobe, T. Kadowaki, R. Nagai, and S. Sugiura. 2008. In vivo imaging in mice reveals local cell dynamics and inflammation in obese adipose tissue. J. Clin. Invest. 118:710-721.
27. Nishimura, S., I. Manabe, M. Nagasaki, K. Eto, H. Yamashita, M. Ohsugi, M. Otsu, K. Hara, K. Ueki, S. Sugiura, et al. 2009. CD8+ effector T cells contribute to macrophage recruitment and adipose tissue inflammation in obesity. Nat. Med. 15:914-920. http://dx.doi.org/10.1038/nm.1964.
28. Patel, S.R., J.H. Hartwig, and J.E. Italiano Jr. 2005. The biogenesis of platelets from megakaryocyte proplatelets. J. Clin. Invest. 115:3348-3354. http://dx.doi.org/10.1172/JCI26891.
29. Patel-Hett, S., J.L. Richardson, H. Schulze, K. Drabek, N.A. Isaac, K. Hoffmeister, R.A. Shivdasani, J.C. Bulinski, N. Galjart, J.H. Hartwig, and J.E. Italiano Jr. 2008. Visualization of microtubule growth in living platelets reveals a dynamic marginal band with multiple microtubules. Blood. 111:4605-4616. http://dx.doi.org/10.1182/blood-2007-10-118844.
30. Rider, P., Y. Carmi, O. Guttman, A. Braiman, I. Cohen, E. Voronov, M.R. White, C.A. Dinarello, and R.N. Apte. 2011. IL-1α and IL-1β recruit different myeloid cells and promote different stages of sterile inflammation. J. Immunol. 187:4835-4843. http://dx.doi.org/10.4049/jimmunol.1102048.
31. Sanjuan-Pla, A., I.C. Macaulay, C.T. Jensen, P.S. Woll, T.C. Luis, A. Mead, S. Moore, C. Carella, S. Matsuoka, T. Bouriez Jones, et al. 2013. Plateletbiased stem cells reside at the apex of the haematopoietic stem-cell hierarchy. Nature. 502:232-236. http://dx.doi.org/10.1038/nature12495.
32. Takayama, N., S. Nishimura, S. Nakamura, T. Shimizu, R. Ohnishi, H. Endo, T. Yamaguchi, M. Otsu, K. Nishimura, M. Nakanishi, et al. 2010. Transient activation of c-MYC expression is critical for efficient platelet generation from human induced pluripotent stem cells. J. Exp. Med. 207:2817-2830. http://dx.doi.org/10.1084/jem.20100844.
33. Takizawa, H., S. Nishimura, N. Takayama, A. Oda, H. Nishikii, Y. Morita, S. Kakinuma, S. Yamazaki, S. Okamura, N. Tamura, et al. 2010. Lnk regulates integrin alphaIIbbeta3 outside-in signaling in mouse platelets, leading to stabilization of thrombus development in vivo. J. Clin. Invest. 120:179-190. http://dx.doi.org/10.1172/JCI39503.
34. Thon, J.N., and J.E. Italiano. 2010. Platelet formation. Semin. Hematol. 47:220-226. http://dx.doi.org/10.1053/j.seminhematol.2010.03.005.
35. Thon, J.N., A. Montalvo, S. Patel-Hett, M.T. Devine, J.L. Richardson, A. Ehrlicher, M.K. Larson, K. Hoffmeister, J.H. Hartwig, and J.E. Italiano Jr. 2010. Cytoskeletal mechanics of proplatelet maturation and platelet release. J. Cell Biol. 191:861-874. http://dx.doi.org/10.1083/jcb.201006102.
36. Thon, J.N., H. Macleod, A.J. Begonja, J. Zhu, K.C. Lee, A. Mogilner, J.H. Hartwig, and J.E. Italiano Jr. 2012. Microtubule and cortical forces determine platelet size during vascular platelet production. Nat. Commun. 3:852. http://dx.doi.org/10.1038/ncomms1838.
37. Yamamoto, R., Y. Morita, J. Ooehara, S. Hamanaka, M. Onodera, K.L. Rudolph, H. Ema, and H. Nakauchi. 2013. Clonal analysis unveils self-renewing lineage-restricted progenitors generated directly from hematopoietic stem cells. Cell. 154:1112-1126. http://dx.doi.org/10.1016/j.cell.2013.08.007.
38. Yang, M., K. Li, C.M. Chui, P.M. Yuen, P.K. Chan, C.K. Chuen, C.K. Li, and T.F. Fok. 2000. Expression of interleukin (IL) 1 type I and type II receptors in megakaryocytic cells and enhancing effects of IL-1beta on megakaryocytopoiesis and NF-E2 expression. Br. J. Haematol. 111:371-380. http://dx.doi.org/10.1046/j.1365-2141.2000.02340.x.
39. Zhang, L., M. Orban, M. Lorenz, V. Barocke, D. Braun, N. Urtz, C. Schulz, M.L. von Brühl, A. Tirniceriu, F. Gaertner, et al. 2012. A novel role of sphingosine 1-phosphate receptor S1pr1 in mouse thrombopoiesis. J. Exp. Med. 209:2165-2181. http://dx.doi.org/10.1084/jem.20121090.