Cytosolic carboxypeptidase CCP6 is required for megakaryopoiesis by modulating Mad2 polyglutamylation

Journal of Experimental Medicine

Volumn 211, Issue 12, 2014, Pages 2439-2454

  Ye, Buqing ^a   Li, Chong ^a   Yang, Zhao ^a,b   Wang, Yanying ^a   Hao, Junfeng ^a   Wang, Li ^a   Li, Yi ^c   Du, Ying ^a   Hao, Lu ^a   Liu, Benyu ^a   Wang, Shuo ^a   Xia, Pengyan ^a   Huang, Guanling ^a   Sun, Lei ^a   Tian, Yong ^a   Fan, Zusen ^a  

^a INSTITUTE OF BIOPHYSICS   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c PEKING UNIVERSITY THIRD HOSPITAL   (China)

Author keywords

[No Author keywords available]

Indexed keywords

AURORA B KINASE; CARBOXYPEPTIDASE; CYTOSOLIC CARBOXYPEPTIDASE CCP6; LIGASE; PROTEIN CPP1; PROTEIN MAD2; PROTEIN TTLL4; PROTEIN TTLL6; UNCLASSIFIED DRUG; AGTPBP1 PROTEIN, MOUSE; CARBOXYPEPTIDASE TRANSPEPTIDASE; CCP6 PROTEIN, MOUSE; GUANINE NUCLEOTIDE BINDING PROTEIN; MAD2L1 PROTEIN, MOUSE; PEPTIDE SYNTHASE; POLYGLUTAMIC ACID; TTLL6 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BONE MARROW PROGENITOR CELL; CELL MATURATION; CONTROLLED STUDY; ENZYME ACTIVATION; HEMOSTASIS; HUMAN; HUMAN CELL; MEGAKARYOCYTE; MEGAKARYOPOIESIS; MOUSE; NONHUMAN; PHENOTYPE; POLYGLUTAMYLATION; PROTEIN EXPRESSION; PROTEIN PROCESSING; REGULATORY MECHANISM; SPLENOMEGALY; THROMBOCYTE COUNT; ANIMAL; BAGG ALBINO MOUSE; BONE MARROW CELL; CELL CULTURE; CELL DIFFERENTIATION; CYTOLOGY; CYTOSOL; ENZYMOLOGY; GENE EXPRESSION; GENETICS; HEK293 CELL LINE; K562 CELL LINE; KNOCKOUT MOUSE; METABOLISM; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; THROMBOCYTE; THROMBOCYTOPOIESIS; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE; WESTERN BLOTTING;

ANIMALS; BLOOD PLATELETS; BLOTTING, WESTERN; BONE MARROW CELLS; CARBOXYPEPTIDASES; CELL DIFFERENTIATION; CELLS, CULTURED; CYTOSOL; GENE EXPRESSION; GTP-BINDING PROTEINS; HEK293 CELLS; HUMANS; K562 CELLS; MAD2 PROTEINS; MEGAKARYOCYTES; MICE, INBRED BALB C; MICE, KNOCKOUT; MICROSCOPY, ELECTRON, TRANSMISSION; PEPTIDE SYNTHASES; POLYGLUTAMIC ACID; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SERINE-TYPE D-ALA-D-ALA CARBOXYPEPTIDASE; THROMBOPOIESIS;

EID: 84911903339     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20141123     Document Type: Article

References (56)

1. Bobinnec, Y., A. Khodjakov, L.M. Mir, C.L. Rieder, B. Eddé, and M. Bornens. 1998. Centriole disassembly in vivo and its effect on centrosome structure and function in vertebrate cells. J. Cell Biol. 143:1575-1589. http://dx.doi.org/10.1083/jcb.143.6.1575
2. Boitano, A.E., L. de Lichtervelde, J.L. Snead, M.P. Cooke, and P.G. Schultz. 2012. An image-based screen identifies a small molecule regulator of megakaryopoiesis. Proc. Natl. Acad. Sci. USA. 109:14019-14023. http://dx.doi.org/10.1073/pnas.1212545109
3. Bosch Grau, M., G. Gonzalez Curto, C. Rocha, M.M. Magiera, P. Marques Sousa, T. Giordano, N. Spassky, and C. Janke. 2013. Tubulin glycylases and glutamylases have distinct functions in stabilization and motility of ependymal cilia. J. Cell Biol. 202:441-451. http://dx.doi.org/10.1083/jcb.201305041
4. Campbell, C.S., and A. Desai. 2013. Tension sensing by Aurora B kinase is independent of survivin-based centromere localization. Nature. 497:118-121. http://dx.doi.org/10.1038/nature12057
5. Chakrabarti, L., J. Eng, R.A. Martinez, S. Jackson, J. Huang, D.E. Possin, B.L. Sopher, and A.R. La Spada. 2008. The zinc-binding domain of Nna1 is required to prevent retinal photoreceptor loss and cerebellar ataxia in Purkinje cell degeneration (pcd) mice. Vision Res. 48:1999-2005. http://dx.doi.org/10.1016/j.visres.2008.05.026
6. Chao, W.C., K. Kulkarni, Z. Zhang, E.H. Kong, and D. Barford. 2012. Structure of the mitotic checkpoint complex. Nature. 484:208-213. http://dx.doi.org/10.1038/nature10896
7. Ding, S., X. Wu, G. Li, M. Han, Y. Zhuang, and T. Xu. 2005. Efficient transposition of the piggyBac (PB) transposon in mammalian cells and mice. Cell. 122:473-483. http://dx.doi.org/10.1016/j.cell.2005.07.013
8. Eddé, B., J. Rossier, J.P. Le Caer, E. Desbruyères, F. Gros, and P. Denoulet. 1990. Posttranslational glutamylation of alpha-tubulin. Science. 247:83-85. http://dx.doi.org/10.1126/science.1967194
9. Fan, Z., P.J. Beresford, D.Y. Oh, D. Zhang, and J. Lieberman. 2003. Tumor suppressor NM23-H1 is a granzyme A-activated DNase during CTL-mediated apoptosis, and the nucleosome assembly protein SET is its inhibitor. Cell. 112:659-672. http://dx.doi.org/10.1016/S0092-8674(03)00150-8
10. Fernandez-Gonzalez, A., A.R. La Spada, J. Treadaway, J.C. Higdon, B.S. Harris, R.L. Sidman, J.I. Morgan, and J. Zuo. 2002. Purkinje cell degeneration (pcd) phenotypes caused by mutations in the axotomy-induced gene, Nna1. Science. 295:1904-1906. http://dx.doi.org/10.1126/science.1068912
11. Gagnon, C., D. White, J. Cosson, P. Huitorel, B. Eddé, E. Desbruyères, L. Paturle-Lafanechère, L. Multigner, D. Job, and C. Cibert. 1996. The polyglutamylated lateral chain of alpha-tubulin plays a key role in flagellar motility. J. Cell Sci. 109:1545-1553.
12. Gao, Y., E. Smith, E. Ker, P. Campbell, E.C. Cheng, S. Zou, S. Lin, L. Wang, S. Halene, and D.S. Krause. 2012. Role of RhoA-specific guanine exchange factors in regulation of endomitosis in megakaryocytes. Dev. Cell. 22:573-584. http://dx.doi.org/10.1016/j.devcel.2011.12.019
13. Geddis, A.E., and K. Kaushansky. 2004. Megakaryocytes express functional Aurora-B kinase in endomitosis. Blood. 104:1017-1024. http://dx.doi.org/10.1182/blood-2004-02-0419
14. Ichikawa, M., T. Asai, T. Saito, S. Seo, I. Yamazaki, T. Yamagata, K. Mitani, S. Chiba, S. Ogawa, M. Kurokawa, and H. Hirai. 2004. AML-1 is required for megakaryocytic maturation and lymphocytic differentiation, but not for maintenance of hematopoietic stem cells in adult hematopoiesis. Nat. Med. 10:299-304. http://dx.doi.org/10.1038/nm997
15. Ikegami, K., M. Mukai, J. Tsuchida, R.L. Heier, G.R. Macgregor, and M. Setou. 2006. TTLL7 is a mammalian beta-tubulin polyglutamylase required for growth of MAP2-positive neurites. J. Biol. Chem. 281:30707-30716. http://dx.doi.org/10.1074/jbc.M603984200
16. Janke, C., and J.C. Bulinski. 2011. Post-translational regulation of the microtubule cytoskeleton: mechanisms and functions. Nat. Rev. Mol. Cell Biol. 12:773-786. http://dx.doi.org/10.1038/nrm3227
17. Janke, C., K. Rogowski, D. Wloga, C. Regnard, A.V. Kajava, J.M. Strub, N. Temurak, J. van Dijk, D. Boucher, A. van Dorsselaer, et al. 2005. Tubulin polyglutamylase enzymes are members of the TTL domain protein family. Science. 308:1758-1762. http://dx.doi.org/10.1126/science.1113010
18. Kabeche, L., and D.A. Compton. 2012. Checkpoint-independent stabilization of kinetochore-microtubule attachments by Mad2 in human cells. Curr. Biol. 22:638-644. http://dx.doi.org/10.1016/j.cub.2012.02.030
19. Kalinina, E., R. Biswas, I. Berezniuk, A. Hermoso, F.X. Aviles, and L.D. Fricker. 2007. A novel subfamily of mouse cytosolic carboxypeptidases. FASEB J. 21:836-850. http://dx.doi.org/10.1096/fj.06-7329com
20. Kim, S., H. Sun, H.L. Ball, K. Wassmann, X. Luo, and H. Yu. 2010. Phosphorylation of the spindle checkpoint protein Mad2 regulates its conformational transition. Proc. Natl. Acad. Sci. USA. 107:19772-19777. http://dx.doi.org/10.1073/pnas.1009000107
21. Kubo, T., H.A. Yanagisawa, T. Yagi, M. Hirono, and R. Kamiya. 2010. Tubulin polyglutamylation regulates axonemal motility by modulating activities of inner-arm dyneins. Curr. Biol. 20:441-445. http://dx.doi.org/10.1016/j.cub.2009.12.058
22. Lordier, L., Y. Chang, A. Jalil, F. Aurade, L. Garçon, Y. Lécluse, F. Larbret, T. Kawashima, T. Kitamura, J. Larghero, et al. 2010. Aurora B is dispensable for megakaryocyte polyploidization, but contributes to the endomitotic process. Blood. 116:2345-2355. http://dx.doi.org/10.1182/blood-2010-01-265785
23. Machlus, K.R., and J.E. Italiano Jr. 2013. The incredible journey: From megakaryocyte development to platelet formation. J. Cell Biol. 201:785-796. http://dx.doi.org/10.1083/jcb.201304054
24. Mapelli, M., L. Massimiliano, S. Santaguida, and A. Musacchio. 2007. The Mad2 conformational dimer: structure and implications for the spindle assembly checkpoint. Cell. 131:730-743. http://dx.doi.org/10.1016/j.cell.2007.08.049
25. Mazharian, A., J. Mori, Y.J. Wang, S. Heising, B.G. Neel, S.P. Watson, and Y.A. Senis. 2013. Megakaryocyte-specific deletion of the protein-tyrosine phosphatases Shp1 and Shp2 causes abnormal megakaryocyte development, platelet production, and function. Blood. 121:4205-4220. http://dx.doi.org/10.1182/blood-2012-08-449272
26. Mercher, T., M.G. Cornejo, C. Sears, T. Kindler, S.A. Moore, I. Maillard, W.S. Pear, J.C. Aster, and D.G. Gilliland. 2008. Notch signaling specifies megakaryocyte development from hematopoietic stem cells. Cell Stem Cell. 3:314-326. http://dx.doi.org/10.1016/j.stem.2008.07.010
27. Michel, L.S., V. Liberal, A. Chatterjee, R. Kirchwegger, B. Pasche, W. Gerald, M. Dobles, P.K. Sorger, V.V. Murty, and R. Benezra. 2001. MAD2 haplo-insufficiency causes premature anaphase and chromosome instability in mammalian cells. Nature. 409:355-359. http://dx.doi.org/10.1038/35053094
28. Nakorn, T.N., T. Miyamoto, and I.L. Weissman. 2003. Characterization of mouse clonogenic megakaryocyte progenitors. Proc. Natl. Acad. Sci. USA. 100:205-210. http://dx.doi.org/10.1073/pnas.262655099
29. Papadantonakis, N., S. Matsuura, and K. Ravid. 2012. Megakaryocyte pathology and bone marrow fibrosis: the lysyl oxidase connection. Blood. 120:1774-1781. http://dx.doi.org/10.1182/blood-2012-02-402594
30. Poirault-Chassac, S., E. Six, C. Catelain, M. Lavergne, J.L. Villeval, W. Vainchenker, and E. Lauret. 2010. Notch/Delta4 signaling inhibits human megakaryocytic terminal differentiation. Blood. 116:5670-5678. http://dx.doi.org/10.1182/blood-2010-05-285957
31. Regnard, C., E. Desbruyères, J.C. Huet, C. Beauvallet, J.C. Pernollet, and B. Eddé. 2000. Polyglutamylation of nucleosome assembly proteins. J. Biol. Chem. 275:15969-15976. http://dx.doi.org/10.1074/jbc.M000045200
32. Rodriguez de la Vega, M., R.G. Sevilla, A. Hermoso, J. Lorenzo, S. Tanco, A. Diez, L.D. Fricker, J.M. Bautista, and F.X. Avilés. 2007. Nna1-like proteins are active metallocarboxypeptidases of a new and diverse M14 subfamily. FASEB J. 21:851-865. http://dx.doi.org/10.1096/fj.06-7330com
33. Rogowski, K., J. van Dijk, M.M. Magiera, C. Bosc, J.C. Deloulme, A. Bosson, L. Peris, N.D. Gold, B. Lacroix, M. Bosch Grau, et al. 2010. A family of protein-deglutamylating enzymes associated with neurodegeneration. Cell. 143:564-578. http://dx.doi.org/10.1016/j.cell.2010.10.014
34. Shah, J.V., and D.W. Cleveland. 2000. Waiting for anaphase: Mad2 and the spindle assembly checkpoint. Cell. 103:997-1000. http://dx.doi.org/10.1016/S0092-8674(00)00202-6
35. Sirajuddin, M., L.M. Rice, and R.D. Vale. 2014. Regulation of microtubule motors by tubulin isotypes and post-translational modifications. Nat. Cell Biol. 16:335-344. http://dx.doi.org/10.1038/ncb2920
36. Smith, E.C., J.N. Thon, M.T. Devine, S. Lin, V.P. Schulz, Y. Guo, S.A. Massaro, S. Halene, P. Gallagher, J.E. Italiano Jr., and D.S. Krause. 2012. MKL1 and MKL2 play redundant and crucial roles in megakaryocyte maturation and platelet formation. Blood. 120:2317-2329. http://dx.doi.org/10.1182/blood-2012-04-420828
37. Sun, L.V., K. Jin, Y. Liu, W. Yang, X. Xie, L. Ye, L. Wang, L. Zhu, S. Ding, Y. Su, et al. 2008. PBmice: an integrated database system of piggyBac (PB) insertional mutations and their characterizations in mice. Nucleic Acids Res. 36:D729-D734. http://dx.doi.org/10.1093/nar/gkm790
38. Suryavanshi, S., B. Eddé, L.A. Fox, S. Guerrero, R. Hard, T. Hennessey, A. Kabi, D. Malison, D. Pennock, W.S. Sale, et al. 2010. Tubulin glutamylation regulates ciliary motility by altering inner dynein arm activity. Curr. Biol. 20:435-440. http://dx.doi.org/10.1016/j.cub.2009.12.062
39. Tefferi, A. 2013. Polycythemia vera and essential thrombocythemia: 2013 update on diagnosis, risk-stratification, and management. Am. J. Hematol. 88:507-516. http://dx.doi.org/10.1002/ajh.23417
40. Thon, J.N., and J.E. Italiano. 2012. Platelets: production, morphology and ultrastructure. Handbook Exp. Pharmacol. 210:3-22. http://dx.doi.org/10.1007/978-3-642-29423-5_1
41. Tong, W., and H.F. Lodish. 2004. Lnk inhibits Tpo-mpl signaling and Tpomediated megakaryocytopoiesis. J. Exp. Med. 200:569-580. http://dx.doi.org/10.1084/jem.20040762
42. Tothova, Z., R. Kollipara, B.J. Huntly, B.H. Lee, D.H. Castrillon, D.E. Cullen, E.P. McDowell, S. Lazo-Kallanian, I.R. Williams, C. Sears, et al. 2007. FoxOs are critical mediators of hematopoietic stem cell resistance to physiologic oxidative stress. Cell. 128:325-339. http://dx.doi.org/10.1016/j.cell.2007.01.003
43. van Dijk, J., K. Rogowski, J. Miro, B. Lacroix, B. Eddé, and C. Janke. 2007. A targeted multienzyme mechanism for selective microtubule polyglutamylation. Mol. Cell. 26:437-448. http://dx.doi.org/10.1016/j.molcel.2007.04.012
44. van Dijk, J., J. Miro, J.M. Strub, B. Lacroix, A. van Dorsselaer, B. Edde, and C. Janke. 2008. Polyglutamylation is a post-translational modification with a broad range of substrates. J. Biol. Chem. 283:3915-3922. http://dx.doi.org/10.1074/jbc.M705813200
45. Wang, T., J. Parris, L. Li, and J.I. Morgan. 2006. The carboxypeptidase-like substrate-binding site in Nna1 is essential for the rescue of the Purkinje cell degeneration (pcd) phenotype. Mol. Cell. Neurosci. 33:200-213. http://dx.doi.org/10.1016/j.mcn.2006.07.009
46. Wang, S., P. Xia, B. Ye, G. Huang, J. Liu, and Z. Fan. 2013. Transient activation of autophagy via Sox2-mediated suppression of mTOR is an important early step in reprogramming to pluripotency. Cell Stem Cell. 13:617-625. http://dx.doi.org/10.1016/j.stem.2013.10.005
47. Wasylyk, C., A. Zambrano, C. Zhao, J. Brants, J. Abecassis, J.A. Schalken, H. Rogatsch, G. Schaefer, A. Pycha, H. Klocker, and B. Wasylyk. 2010. Tubulin tyrosine ligase like 12 links to prostate cancer through tubulin posttranslational modification and chromosome ploidy. Int. J. Cancer. 127:2542-2553. http://dx.doi.org/10.1002/ijc.25261
48. Wen, Q., B. Goldenson, and J.D. Crispino. 2011. Normal and malignant megakaryopoiesis. Expert Rev. Mol. Med. 13:e32. http://dx.doi.org/10.1017/S1462399411002043
49. Wen, Q., B. Goldenson, S.J. Silver, M. Schenone, V. Dancik, Z. Huang, L.Z. Wang, T.A. Lewis, W.F. An, X. Li, et al. 2012. Identification of regulators of polyploidization presents therapeutic targets for treatment of AMKL. Cell. 150:575-589. http://dx.doi.org/10.1016/j.cell.2012.06.032
50. Wolff, A., B. de Néchaud, D. Chillet, H. Mazarguil, E. Desbruyères, S. Audebert, B. Eddé, F. Gros, and P. Denoulet. 1992. Distribution of glutamylated alpha and beta-tubulin in mouse tissues using a specific monoclonal antibody, GT335. Eur. J. Cell Biol. 59:425-432.
51. Wong, C.H., C.N. Jenne, B. Petri, N.L. Chrobok, and P. Kubes. 2013. Nucleation of platelets with blood-borne pathogens on Kupffer cells precedes other innate immunity and contributes to bacterial clearance. Nat. Immunol. 14:785-792. http://dx.doi.org/10.1038/ni.2631
52. Woulfe, D., H. Jiang, A. Morgans, R. Monks, M. Birnbaum, and L.F. Brass. 2004. Defects in secretion, aggregation, and thrombus formation in platelets from mice lacking Akt2. J. Clin. Invest. 113:441-450. http://dx.doi.org/10.1172/JCI200420267
53. Xia, P., S. Wang, Y. Du, Z. Zhao, L. Shi, L. Sun, G. Huang, B. Ye, C. Li, Z. Dai, et al. 2013. WASH inhibits autophagy through suppression of Beclin 1 ubiquitination. EMBO J. 32:2685-2696. http://dx.doi.org/10.1038/emboj.2013.189
54. Yang, W., K. Jin, X. Xie, D. Li, J. Yang, L. Wang, N. Gu, Y. Zhong, and L.V. Sun. 2009. Development of a database system for mapping insertional mutations onto the mouse genome with large-scale experimental data. BMC Genomics. 10:S7. http://dx.doi.org/10.1186/1471-2164-10-S3-S7
55. Yin, F., A.M. Hoggatt, J. Zhou, and B.P. Herring. 2006. 130-kDa smooth muscle myosin light chain kinase is transcribed from a CArGdependent, internal promoter within the mouse mylk gene. Am. J. Physiol. Cell Physiol. 290:C1599-C1609. http://dx.doi.org/10.1152/ajpcell.00289.2005
56. Zhang, Y., Y. Nagata, G. Yu, H.G. Nguyen, M.R. Jones, P. Toselli, C.W. Jackson, M. Tatsuka, K. Todokoro, and K. Ravid. 2004. Aberrant quantity and localization of Aurora-B/AIM-1 and survivin during megakaryocyte polyploidization and the consequences of Aurora-B/AIM-1-deregulated expression. Blood. 103:3717-3726. http://dx.doi.org/10.1182/blood-2003-09-3365