VPS33B regulates protein sorting into and maturation of a-granule progenitor organelles in mouse megakaryocytes

Blood

Volumn 126, Issue 2, 2015, Pages 133-143

  Bem, Danai ^a   Smith, Holly ^a,b   Banushi, Blerida ^b   Burden, Jemima J ^b   White, Ian J ^b   Hanley, Joanna ^b,c   Jeremiah, Nadia ^d   Rieux Laucat, Frédéric ^d   Bettels, Ruth ^e   Ariceta, Gema ^f   Mumford, Andrew D ^g   Thomas, Steven G ^a   Watson, Steve P ^a   Gissen, Paul ^b,h  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

^d Laboratory of Immunogenetics of Pediatric Autoimmune Diseases   (France)

^e UNIVERSITY HOSPITAL MÜNSTER   (Germany)

^f HOSPITAL UNIVERSITARI VALL D HEBRON   (Spain)

^g UNIVERSITY OF BRISTOL   (United Kingdom)

^h GREAT ORMOND STREET HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

PADGEM PROTEIN; REGULATOR PROTEIN; THROMBIN; UNCLASSIFIED DRUG; VON WILLEBRAND FACTOR; VPS33B PROTEIN; VESICULAR TRANSPORT PROTEIN; VPS33B PROTEIN, HUMAN; VPS33B PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BLEEDING TENDENCY; CASE REPORT; CELL MATURATION; CELL ORGANELLE; CELL SIZE; CELL STRUCTURE; CELL VACUOLE; CONTROLLED STUDY; DENDRITIC CELL; ERYTHROCYTE; EXTRAMEDULLARY HEMATOPOIESIS; HEMATOCRIT; HUMAN; IMMUNOELECTRON MICROSCOPY; IN VITRO STUDY; LEUKOCYTE; LYMPHOCYTE; MACROPHAGE; MEGAKARYOBLAST; MEGAKARYOCYTE; MEGAKARYOPOIESIS; MONOCYTE; MOUSE; MULTIVESICULAR BODY; NEUTROPHIL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN TARGETING; SPLEEN CELL; THROMBOCYTE AGGREGATION; THROMBOCYTE COUNT; THROMBOCYTE FUNCTION; THROMBOCYTE VOLUME; ANIMAL; ARTHROGRYPOSIS; C57BL MOUSE; CELL CULTURE; CELL GRANULE; CHOLESTASIS; CYTOLOGY; GENETICS; GRAY PLATELET SYNDROME; KIDNEY FAILURE; METABOLISM; PHYSIOLOGY; PROTEIN TRANSPORT; SINGLE NUCLEOTIDE POLYMORPHISM; TRANSGENIC MOUSE;

ANIMALS; ARTHROGRYPOSIS; CELLS, CULTURED; CHOLESTASIS; CYTOPLASMIC GRANULES; GRAY PLATELET SYNDROME; HUMANS; MEGAKARYOCYTES; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; ORGANELLES; PLATELET COUNT; POLYMORPHISM, SINGLE NUCLEOTIDE; PROTEIN TRANSPORT; RENAL INSUFFICIENCY; VESICULAR TRANSPORT PROTEINS;

EID: 84937778865     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2014-12-614677     Document Type: Article

References (42)

1. Maynard DM, Heijnen HF, Horne MK, White JG, Gahl WA. Proteomic analysis of platelet alphagranules using mass spectrometry. J Thromb Haemost. 2007;5(9):1945-1955.
2. Maynard DM, Heijnen HF, Gahl WA, Gunay-Aygun M. The a-granule proteome: novel proteins in normal and ghost granules in gray platelet syndrome. J Thromb Haemost. 2010;8(8): 1786-1796.
3. Blair P, Flaumenhaft R. Platelet alpha-granules: basic biology and clinical correlates. Blood Rev. 2009;23(4):177-189.
4. Zucker-Franklin D. Endocytosis by human platelets: metabolic and freeze-fracture studies. J Cell Biol. 1981;91(3 pt 1):706-715.
5. Handagama PJ, George JN, Shuman MA, McEver RP, Bainton DF. Incorporation of a circulating protein into megakaryocyte and platelet granules. Proc Natl Acad Sci USA. 1987;84(3):861-865.
6. Behnke O. Coated pits and vesicles transfer plasma components to platelet granules. Thromb Haemost. 1989;62(2):718-722.
7. King SM, Reed GL. Development of platelet secretory granules. Semin Cell Dev Biol. 2002; 13(4):293-302.
8. Heijnen HF, Debili N, Vainchencker W, Breton-Gorius J, Geuze HJ, Sixma JJ. Multivesicular bodies are an intermediate stage in the formation of platelet alpha-granules. Blood. 1998;91(7): 2313-2325.
9. Albers CA, Cvejic A, Favier R, et al. Exome sequencing identifies NBEAL2 as the causative gene for gray platelet syndrome. Nat Genet. 2011; 43(8):735-737.
10. Gunay-Aygun M, Falik-Zaccai TC, Vilboux T, et al. NBEAL2 is mutated in gray platelet syndrome and is required for biogenesis of platelet a-granules. Nat Genet. 2011;43(8):732-734.
11. Kahr WH, Hinckley J, Li L, et al. Mutations in NBEAL2, encoding a BEACH protein, cause gray platelet syndrome. Nat Genet. 2011;43(8): 738-740.
12. Aminkeng F. GFI1B mutation causes autosomal dominant gray platelet syndrome. Clin Genet. 2014;85(6):534-535.
13. Monteferrario D, Bolar NA, Marneth AE, et al. A dominant-negative GFI1B mutation in the gray platelet syndrome. N Engl J Med. 2014;370(3): 245-253.
14. Deppermann C, Cherpokova D, Nurden P, et al. Gray platelet syndrome and defective thrombo-inflammation in Nbeal2-deficient mice. JClinInvest.2013;123(8):3331-3342.
15. Deppermann C, Nurden P, Nurden AT, Nieswandt B, Stegner D. The Nbeal2(-/-) mouse as a model for the gray platelet syndrome. Rare Dis. 2013;1: e26561.
16. Kahr WH, Lo RW, Li L, et al. Abnormal megakaryocyte development and platelet function in Nbeal2(-/-) mice. Blood. 2013;122(19): 3349-3358.
17. Guerrero JA, Bennett C, van der Weyden L, et al. Gray platelet syndrome: proinflammatory megakaryocytes and a-granule loss cause myelofibrosis and confer metastasis resistance in mice. Blood. 2014;124(24): 3624-3635.
18. Gissen P, Tee L, Johnson CA, et al. Clinical and molecular genetic features of ARC syndrome. Hum Genet. 2006;120(3):396-409.
19. Gissen P, Johnson CA, Morgan NV, et al. Mutations in VPS33B, encoding a regulator of SNARE-dependent membrane fusion, cause arthrogryposis-renal dysfunction-cholestasis (ARC) syndrome. Nat Genet. 2004;36(4): 400-404.
20. Cullinane AR, Straatman-Iwanowska A, Zaucker A, et al. Mutations in VIPAR cause an arthrogryposis, renal dysfunction and cholestasis syndrome phenotype with defects in epithelial polarization. Nat Genet. 2010;42(4):303-312.
21. Smith H, Galmes R, Gogolina E, et al. Associations among genotype, clinical phenotype, and intracellular localization of trafficking proteins in ARC syndrome. Hum Mutat. 2012;33(12): 1656-1664.
22. Deal JE, Barratt TM, Dillon MJ. Fanconi syndrome, ichthyosis, dysmorphism, jaundice and diarrhoea-a new syndrome. Pediatr Nephrol. 1990;4(4):308-313.
23. Kim SM, Chang HK, Song JW, Koh H, Han SJ; Severance Pediatric Liver Disease Research Group. Agranular platelets as a cardinal feature of ARC syndrome. J Pediatr Hematol Oncol. 2010; 32(4):253-258.
24. Lo B, Li L, Gissen P, et al. Requirement of VPS33B, a member of the Sec1/Munc18 protein family, in megakaryocyte and platelet alphagranule biogenesis. Blood. 2005;106(13): 4159-4166.
25. Urban D, Li L, Christensen H, et al. The VPS33B-binding protein VPS16B is required in megakaryocyte and platelet a-granule biogenesis. Blood. 2012;120(25):5032-5040.
26. Eckly A, Strassel C, Cazenave JP, Lanza F, Léon C, Gachet C. Characterization of megakaryocyte development in the native bone marrow environment. Methods Mol Biol. 2012;788: 175-192.
27. Breton-Gorius J, Vainchenker W, Nurden A, Levy-Toledano S, Caen J. Defective alpha-granule production in megakaryocytes from gray platelet syndrome: ultrastructural studies of bone marrow cells and megakaryocytes growing in culture from blood precursors. Am J Pathol. 1981;102(1): 10-19.
28. White JG. Ultrastructural studies of the gray platelet syndrome. Am J Pathol. 1979;95(2): 445-462.
29. Seibler J, Zevnik B, Küter-Luks B, et al. Rapid generation of inducible mouse mutants. Nucleic Acids Res. 2003;31(4):e12.
30. Drouin A, Favier R, Massé JM, et al. Newly recognized cellular abnormalities in the gray platelet syndrome. Blood. 2001;98(5):1382-1391.
31. Schmitz G, Müller G. Structure and function of lamellar bodies, lipid-protein complexes involved in storage and secretion of cellular lipids. J Lipid Res. 1991;32(10):1539-1570.
32. Lajoie P, Guay G, Dennis JW, Nabi IR. The lipid composition of autophagic vacuoles regulates expression of multilamellar bodies. J Cell Sci. 2005;118(pt 9):1991-2003.
33. Hariri M, Millane G, Guimond MP, Guay G, Dennis JW, Nabi IR. Biogenesis of multilamellar bodies via autophagy. Mol Biol Cell. 2000;11(1): 255-268.
34. Hershkovitz D, Mandel H, Ishida-Yamamoto A, et al. Defective lamellar granule secretion in arthrogryposis, renal dysfunction, and cholestasis syndrome caused by a mutation in VPS33B. Arch Dermatol. 2008;144(3):334-340.
35. Cullinane AR, Straatman-Iwanowska A, Seo JK, et al. Molecular investigations to improve diagnostic accuracy in patients with ARC syndrome. Hum Mutat. 2009;30(2):E330-E337.
36. Akbar MA, Tracy C, Kahr WH, Krämer H. The fullof-bacteria gene is required for phagosome maturation during immune defense in Drosophila. J Cell Biol. 2011;192(3):383-390.
37. Perini ED, Schaefer R, Stöter M, Kalaidzidis Y, Zerial M. Mammalian CORVET is required for fusion and conversion of distinct early endosome subpopulations. Traffic. 2014;15(12):1366-1389.
38. Pols MS, van Meel E, Oorschot V, et al. hVps41 and VAMP7 function in direct TGN to late endosome transport of lysosomal membrane proteins. Nat Commun. 2013;4:1361.
39. Graham SC, Wartosch L, Gray SR, et al. Structural basis of Vps33A recruitment to the human HOPS complex by Vps16. Proc Natl Acad Sci USA. 2013;110(33):13345-13350.
40. Suzuki T, Oiso N, Gautam R, et al. The mouse organellar biogenesis mutant buff results from a mutation in Vps33a, a homologue of yeast vps33 and Drosophila carnation. Proc Natl Acad Sci USA. 2003;100(3):1146-1150.
41. Youssefian T, Cramer EM. Megakaryocyte dense granule components are sorted in multivesicular bodies. Blood. 2000;95(12):4004-4007.
42. Ambrosio AL, Boyle JA, Di Pietro SM. Mechanism of platelet dense granule biogenesis: study of cargo transport and function of Rab32 and Rab38 in a model system. Blood. 2012;120(19): 4072-4081.