Sorting protein VPS33B regulates exosomal autocrine signaling to mediate hematopoiesis and leukemogenesis

Journal of Clinical Investigation

Volumn 126, Issue 12, 2016, Pages 4537-4553

  Gu, Hao ^a,b   Chen, Chiqi ^b   Hao, Xiaoxin ^b   Wang, Conghui ^b   Zhang, Xiaocui ^b   Li, Zhen ^b   Shao, Hongfang ^c   Zeng, Hongxiang ^b   Yu, Zhuo ^b   Xie, Li ^b   Xia, Fangzhen ^b   Zhang, Feifei ^b   Liu, Xiaoye ^b   Zhang, Yaping ^b   Jiang, Haishan ^b   Zhu, Jun ^b   Wan, Jiangbo ^b   Wang, Chun ^b   Weng, Wei ^b   Xie, Jingjing ^d   Tao, Minfang ^c   Zhang, Cheng Cheng ^e   Liu, Junling ^b   Chen, Guo Qiang ^a,b   Zheng, Junke ^b   more..

^a UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^b SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^c SHANGHAI JIAO TONG UNIVERSITY AFFILIATED SIXTH PEOPLE S HOSPITAL   (China)

^d BINZHOU MEDICAL UNIVERSITY   (China)

^e UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

SECRETORY PROTEIN; UNCLASSIFIED DRUG; VPS33B PROTEIN; GDI2 PROTEIN, MOUSE; GUANINE NUCLEOTIDE DISSOCIATION INHIBITOR; RAB PROTEIN; RAB11 PROTEIN; RAB27A PROTEIN, MOUSE; VESICULAR TRANSPORT PROTEIN; VPS33B PROTEIN, MOUSE;

ANIMAL CELL; ARTICLE; AUTOCRINE EFFECT; BIOGENESIS; CELL MATURATION; CELL PROLIFERATION; EMBRYO; ENDOSOME; EXOSOME; EXTRACELLULAR SPACE; GENE OVEREXPRESSION; HEK293 CELL LINE; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; LEUKEMIA CELL; LEUKEMOGENESIS; LYSOSOME; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROCESSING; PROTEIN SECRETION; PROTEIN TARGETING; SIGNAL TRANSDUCTION; TRANSMISSION ELECTRON MICROSCOPY; ANIMAL; CELL TRANSFORMATION; GENETICS; KNOCKOUT MOUSE; LEUKEMIA; METABOLISM; PATHOLOGY; PROTEIN TRANSPORT;

ANIMALS; AUTOCRINE COMMUNICATION; CELL TRANSFORMATION, NEOPLASTIC; EXOSOMES; GUANINE NUCLEOTIDE DISSOCIATION INHIBITORS; HEK293 CELLS; HEMATOPOIESIS; HUMANS; LEUKEMIA; MICE; MICE, KNOCKOUT; PROTEIN TRANSPORT; RAB GTP-BINDING PROTEINS; SIGNAL TRANSDUCTION; VESICULAR TRANSPORT PROTEINS;

EID: 85002514611     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI87105     Document Type: Article

References (60)

1. Till JE, McCulloch EA. A direct measurement of the radiation sensitivity of normal mouse bone marrow cells. Radiat Res. 1961;14:213-222.
2. Bryder D, Rossi DJ, Weissman IL. Hematopoietic stem cells: the paradigmatic tissue-specific stem cell. Am J Pathol. 2006;169(2):338-346.
3. Abramson S, Miller RG, Phillips RA. The identification in adult bone marrow of pluripotent and restricted stem cells of the myeloid and lymphoid systems. J Exp Med. 1977;145(6):1567-1579.
4. Blank U, Karlsson G, Karlsson S. Signaling pathways governing stem-cell fate. Blood. 2008;111(2):492-503.
5. Zhang CC, Lodish HF. Cytokines regulating hematopoietic stem cell function. Curr Opin Hematol. 2008;15(4):307-311.
6. Zhao M, Li L. Regulation of hematopoietic stem cells in the niche. Sci China Life Sci. 2015;58(12):1209-1215.
7. Ding L, Saunders TL, Enikolopov G, Mor-rison SJ. Endothelial and perivascular cells maintain haematopoietic stem cells. Nature. 2012;481(7382):457-462.
8. Yoshihara H, et al. Thrombopoietin/MPL signaling regulates hematopoietic stem cell quiescence and interaction with the osteoblastic niche. Cell Stem Cell. 2007;1(6):685-697.
9. Sugimura R, et al. Noncanonical Wnt signaling maintains hematopoietic stem cells in the niche. Cell. 2012;150(2):351-365.
10. Reya T, et al. A role for Wnt signalling in self-renewal of haematopoietic stem cells. Nature. 2003;423(6938):409-414.
11. Fortunel NO, Hatzfeld JA, Monier MN, Hatzfeld A. Control of hematopoietic stem/progenitor cell fate by transforming growth factor-β. Oncol Res. 2003;13(6-10):445-453.
12. Arai F, et al. Tie2/angiopoietin-1 signaling regulates hematopoietic stem cell quiescence in the bone marrow niche. Cell. 2004;118(2):149-161.
13. Yeoh JS, et al. Fibroblast growth factor-1 and-2 preserve long-term repopulating ability of hema-topoietic stem cells in serum-free cultures. Stem Cells. 2006;24(6):1564-1572.
14. Zheng J, et al. Inhibitory receptors bind ANGPTLs and support blood stem cells and leukaemia development. Nature. 2012;485(7400):656-660.
15. Zheng J, Huynh H, Umikawa M, Silvany R, Zhang CC. Angiopoietin-like protein 3 supports the activity of hematopoietic stem cells in the bone marrow niche. Blood. 2011;117(2):470-479.
16. Ludwig AK, Giebel B. Exosomes: small vesicles participating in intercellular communication. Int J Biochem Cell Biol. 2012;44(1):11-15.
17. Simpson RJ, Jensen SS, Lim JW. Proteomic profiling of exosomes: current perspectives. Proteom-ics. 2008;8(19):4083-4099.
18. Thuma F, Zöller M. Outsmart tumor exosomes to steal the cancer initiating cell its niche. Semin Cancer Biol. 2014;28:39-50.
19. Bonifacino JS, Glick BS. The mechanisms of vesicle budding and fusion. Cell. 2004;116(2):153-166.
20. Bonifacino JS, Lippincott-Schwartz J. Coat proteins: shaping membrane transport. Nat Rev Mol Cell Biol. 2003;4(5):409-414.
21. McMahon HT, Mills IG. COP and clath-rin-coated vesicle budding: different pathways, common approaches. Curr Opin Cell Biol. 2004;16(4):379-391.
22. Bem D, et al. VPS33B regulates protein sorting into and maturation of a-granule progenitor organelles in mouse megakaryocytes. Blood. 2015;126(2):133-143.
23. Hanson PI, Cashikar A. Multivesicular body morphogenesis. Annu Rev Cell Dev Biol. 2012;28:337-362.
24. King SM, Reed GL. Development of platelet secretory granules. Semin Cell Dev Biol. 2002;13(4):293-302.
25. Heijnen HF, Debili N, Vainchencker W, Breton-Gorius J, Geuze HJ, Sixma JJ. Multivesicular bodies are an intermediate stage in the formation of platelet α-granules. Blood. 1998;91(7):2313-2325.
26. Wubbolts R, et al. Proteomic and biochemical analyses of human B cell-derived exosomes. Potential implications for their function and multivesicular body formation. J Biol Chem. 2003;278(13):10963-10972.
27. Gissen P, et al. Mutations in VPS33B, encoding a regulator of SNARE-dependent membrane fusion, cause arthrogryposis-renal dysfunc-tion-cholestasis (ARC) syndrome. Nat Genet. 2004;36(4):400-404.
28. Lo B, et al. Requirement of VPS33B, a member of the Sec1/Munc18 protein family, in megakaryo-cyte and platelet alpha-granule biogenesis. Blood. 2005;106(13):4159-4166.
29. Urban D, et al. The VPS33B-binding pro-tein VPS16B is required in megakaryocyte and platelet a-granule biogenesis. Blood. 2012;120(25):5032-5040.
30. Mane SM, et al. Purification and characterization of human lysosomal membrane glycoproteins. Arch Biochem Biophys. 1989;268(1):360-378.
31. Kobayashi T, et al. The tetraspanin CD63/lamp3 cycles between endocytic and secretory compartments in human endothelial cells. Mol Biol Cell. 2000;11(5):1829-1843.
32. Xu R, Greening DW, Zhu HJ, Takahashi N, Simpson RJ. Extracellular vesicle isolation and char-acterization: toward clinical application. J Clin Invest. 2016;126(4):1152-1162.
33. Tauro BJ, et al. Comparison of ultracentrifuga-tion, density gradient separation, and immuno-affinity capture methods for isolating human colon cancer cell line LIM1863-derived exo-somes. Methods. 2012;56(2):293-304.
34. Zhang CC, et al. Angiopoietin-like proteins stimulate ex vivo expansion of hematopoietic stem cells. Nat Med. 2006;12(2):240-245.
35. Wang YH, et al. Cell-state-specific metabolic dependency in hematopoiesis and leukemogene-sis. Cell. 2014;158(6):1309-1323.
36. Saito Y, Chapple RH, Lin A, Kitano A, Nakada D. AMPK protects leukemia-initiating cells in myeloid leukemias from metabolic stress in the bone marrow. Cell Stem Cell. 2015;17(5):585-596.
37. Chen X, Zheng J, Zou Y, Song C, Hu X, Zhang CC. IGF binding protein 2 is a cell-autonomous factor supporting survival and migration of acute leukemia cells. J Hematol Oncol. 2013;6(1):72.
38. Huynh H, et al. IGF binding protein 2 supports the survival and cycling of hematopoietic stem cells. Blood. 2011;118(12):3236-3243.
39. Wartosch L, Günesdogan U, Graham SC, Luzio JP. Recruitment of VPS33A to HOPS by VPS16 is required for lysosome fusion with endosomes and autophagosomes. Traffic. 2015;16(7):727-742.
40. Göthert JR, et al. In vivo fate-tracing studies using the Scl stem cell enhancer: embryonic hematopoietic stem cells significantly contribute to adult hematopoiesis. Blood. 2005;105(7):2724-2732.
41. Cheng T, et al. Hematopoietic stem cell quiescence maintained by p21cip1/waf1. Science. 2000;287(5459):1804-1808.
42. Baietti MF, et al. Syndecan-syntenin-ALIX regulates the biogenesis of exosomes. Nat Cell Biol. 2012;14(7):677-685.
43. Beckett K, et al. Drosophila S2 cells secrete wingless on exosome-like vesicles but the wingless gradient forms independently of exosomes. Traffic. 2013;14(1):82-96.
44. Urbé S, Huber LA, Zerial M, Tooze SA, Parton RG. Rab11, a small GTPase associated with both constitutive and regulated secretory pathways in PC12 cells. FEBS Lett. 1993;334(2):175-182.
45. Tolmachova T, Abrink M, Futter CE, Authi KS, Seabra MC. Rab27b regulates number and secretion of platelet dense granules. Proc Natl Acad Sci USA. 2007;104(14):5872-5877.
46. Ostrowski M, et al. Rab27a and Rab27b control different steps of the exosome secretion pathway. Nat Cell Biol. 2010;12(1):19-30.
47. Hsu C, et al. Regulation of exosome secretion by Rab35 and its GTPase-activating proteins TBC-1D10A-C. J Cell Biol. 2010;189(2):223-232.
48. Ullrich O, et al. Rab GDP dissociation inhibitor as a general regulator for the membrane association of rab proteins. J Biol Chem. 1993;268(24):18143-18150.
49. Paek I, et al. ERS-24, a mammalian v-SNARE implicated in vesicle traffic between the ER and the Golgi. J Cell Biol. 1997;137(5):1017-1028.
50. John BA, Meister M, Banning A, Tikkanen R. Flo-tillins bind to the dileucine sorting motif of ß-site amyloid precursor protein-cleaving enzyme 1 and influence its endosomal sorting. FEBS J. 2014;281(8):2074-2087.
51. Hou H, et al. Inhibitors of phosphatidylinositol 3'-kinases promote mitotic cell death in HeLa cells. PLoS One. 2012;7(4):e35665.
52. Miller S, Oleksy A, Perisic O, Williams RL. Finding a fitting shoe for Cinderella: search-ing for an autophagy inhibitor. Autophagy. 2010;6(6):805-807.
53. Oike Y, et al. Angiopoietin-related growth factor (AGF) promotes epidermal proliferation, remod-eling, and regeneration. Proc Natl Acad Sci USA. 2003;100(16):9494-9499.
54. Deng M, et al. A motif in LILRB2 critical for Angptl2 binding and activation. Blood. 2014;124(6):924-935.
55. Zhang FF, et al. Inhibitory leukocyte immuno-globulin-like receptors in cancer development. Sci China Life Sci. 2015;58(12):1216-1225.
56. Bhuin T, Roy JK. Rab proteins: the key regulators of intracellular vesicle transport. Exp Cell Res. 2014;328(1):1-19.
57. van Niel G, et al. The tetraspanin CD63 regulates ESCRT-independent and-dependent endo-somal sorting during melanogenesis. Dev Cell. 2011;21(4):708-721.
58. Carayon K, et al. Proteolipidic composition of exosomes changes during reticulocyte maturation. J Biol Chem. 2011;286(39):34426-34439.
59. Koles K, et al. Mechanism of evenness interrupted (Evi)-exosome release at synaptic boutons. J Biol Chem. 2012;287(20):16820-16834.
60. Zheng J, et al. Ex vivo expanded hematopoi-etic stem cells overcome the MHC barrier in allogeneic transplantation. Cell Stem Cell. 2011;9(2):119-130.