Secreted protein Del-1 regulates myelopoiesis in the hematopoietic stem cell niche

Journal of Clinical Investigation

Volumn 127, Issue 10, 2017, Pages 3624-3639

  Mitroulis, Ioannis ^a,b   Chen, Lan Sun ^a   Singh, Rashim Pal ^a   Kourtzelis, Ioannis ^a   Economopoulou, Matina ^b   Kajikawa, Tetsuhiro ^c   Troullinaki, Maria ^a   Ziogas, Athanasios ^a   Ruppova, Klara ^a   Hosur, Kavita ^c   Maekawa, Tomoki ^c,i   Wang, Baomei ^c   Subramanian, Pallavi ^a   Tonn, Torsten ^d   Verginis, Panayotis ^a,e   Von Bonin, Malte ^b   Wobus, Manja ^b   Bornhäuser, Martin ^b,f   Grinenko, Tatyana ^a   Di Scala, Marianna ^g   Hidalgo, Andres ^g,h   Wielockx, Ben ^a,f   Hajishengallis, George ^c   Chavakis, Triantafyllos ^a,b,f   more..

^a DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^b UNIVERSITY HOSPITAL CARL GUSTAV CARUS   (Germany)

^c UNIVERSITY OF PENNSYLVANIA SCHOOL OF DENTAL MEDICINE   (United States)

^d Red Cross Donor Service Sachsen   (Germany)

^e BIOMEDICAL RESEARCH FOUNDATION   (Greece)

^f CENTER FOR REGENERATIVE THERAPIES DRESDEN   (Germany)

^g CENTRO NACIONAL DE INVESTIGACIONES CARDIOVASCULARES CNIC   (Spain)

^h LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

ⁱ NIIGATA UNIVERSITY GRADUATE SCHOOL OF MEDICAL AND DENTAL SCIENCES   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BETA3 INTEGRIN; DEVELOPMENTAL ENDOTHELIAL LOCUS 1; GLYCOPROTEIN; GRANULOCYTE COLONY STIMULATING FACTOR; SCLEROPROTEIN; STROMAL CELL DERIVED FACTOR 1; UNCLASSIFIED DRUG; CARRIER PROTEIN; CXCL12 PROTEIN, HUMAN; CXCL12 PROTEIN, MOUSE; EDIL3 PROTEIN, HUMAN; EDIL3 PROTEIN, MOUSE; ITGB3 PROTEIN, HUMAN;

ANIMAL CELL; ANIMAL EXPERIMENT; AORTIC ENDOTHELIAL CELL; CELL DIFFERENTIATION; CELL FUNCTION; CELL PROLIFERATION; CONFERENCE PAPER; CONTROLLED STUDY; HEMATOPOIETIC STEM CELL; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HEMATOPOIETIC SYSTEM; HUMAN; HUMAN CELL; MOUSE; MYELOPOIESIS; NONHUMAN; OSTEOBLAST CELL LINE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION; RETICULUM CELL; STEADY STATE; STEM CELL NICHE; STRESS; ANIMAL; ENDOTHELIUM CELL; GENETICS; KNOCKOUT MOUSE; METABOLISM; PHYSIOLOGICAL STRESS; SECRETION (PROCESS);

ANIMALS; CARRIER PROTEINS; CHEMOKINE CXCL12; ENDOTHELIAL CELLS; HEMATOPOIETIC STEM CELLS; HUMANS; INTEGRIN BETA3; MICE; MICE, KNOCKOUT; MYELOPOIESIS; STEM CELL NICHE; STRESS, PHYSIOLOGICAL;

EID: 85030535112     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI92571     Document Type: Conference Paper

References (77)

1. Trumpp A, Essers M, Wilson A. Awakening dormant haematopoietic stem cells. Nat Rev Immunol. 2010;10(3):201-209.
2. Sun J, et al. Clonal dynamics of native haematopoiesis. Nature. 2014;514(7522):322-327.
3. Morrison SJ, Scadden DT. The bone marrow niche for haematopoietic stem cells. Nature. 2014;505(7483):327-334.
4. Kiel MJ, Yilmaz OH, Iwashita T, Yilmaz OH, Terhorst C, Morrison SJ. SLAM family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells. Cell. 2005;121(7):1109-1121.
5. Winkler IG, et al. Vascular niche E-selectin regulates hematopoietic stem cell dormancy, self renewal and chemoresistance. Nat Med. 2012;18(11):1651-1657.
6. Itkin T, et al. Distinct bone marrow blood vessels differentially regulate haematopoiesis. Nature. 2016;532(7599):323-328.
7. Kunisaki Y, et al. Arteriolar niches maintain haematopoietic stem cell quiescence. Nature. 2013;502(7473):637-643.
8. Kusumbe AP, et al. Age-dependent modulation of vascular niches for haematopoietic stem cells. Nature. 2016;532(7599):380-384.
9. Ding L, Saunders TL, Enikolopov G, Morrison SJ. Endothelial and perivascular cells maintain haematopoietic stem cells. Nature. 2012;481(7382):457-462.
10. Acar M, et al. Deep imaging of bone marrow shows non-dividing stem cells are mainly perisinusoidal. Nature. 2015;526(7571):126-130.
11. Himburg HA, et al. Pleiotrophin regulates the retention and self-renewal of hematopoietic stem cells in the bone marrow vascular niche. Cell Rep. 2012;2(4):964-975.
12. Méndez-Ferrer S, et al. Mesenchymal and haematopoietic stem cells form a unique bone marrow niche. Nature. 2010;466(7308):829-834.
13. Mendelson A, Frenette PS. Hematopoietic stem cell niche maintenance during homeostasis and regeneration. Nat Med. 2014;20(8):833-846.
14. Kfoury Y, Scadden DT. Mesenchymal cell contributions to the stem cell niche. Cell Stem Cell. 2015;16(3):239-253.
15. Greenbaum A, et al. CXCL12 in early mesenchymal progenitors is required for haematopoietic stem-cell maintenance. Nature. 2013;495(7440):227-230.
16. Sugiyama T, Kohara H, Noda M, Nagasawa T. Maintenance of the hematopoietic stem cell pool by CXCL12-CXCR4 chemokine signaling in bone marrow stromal cell niches. Immunity. 2006;25(6):977-988.
17. Silberstein L, et al. Proximity-based differential single-cell analysis of the niche to identify stem/progenitor cell regulators. Cell Stem Cell. 2016;19(4):530-543.
18. Lo Celso C, et al. Live-animal tracking of individual haematopoietic stem/progenitor cells in their niche. Nature. 2009;457(7225):92-96.
19. Doan PL, et al. Epidermal growth factor regulates hematopoietic regeneration after radiation injury. Nat Med. 2013;19(3):295-304.
20. Himburg HA, et al. Pleiotrophin regulates the expansion and regeneration of hematopoietic stem cells. Nat Med. 2010;16(4):475-482.
21. To LB, Levesque JP, Herbert KE. How I treat patients who mobilize hematopoietic stem cells poorly. Blood. 2011;118(17):4530-4540.
22. Peffault de Latour R, et al. Recommendations on hematopoietic stem cell transplantation for inherited bone marrow failure syndromes. Bone Marrow Transplant. 2015;50(9):1168-1172.
23. Gertz MA. Current status of stem cell mobilization. Br J Haematol. 2010;150(6):647-662.
24. Morgan SJ, et al. Predictive factors for successful stem cell mobilization in patients with indolent lymphoproliferative disorders previously treated with fludarabine. Leukemia. 2004;18(5):1034-1038.
25. Bennett CL, Djulbegovic B, Norris LB, Armitage JO. Colony-stimulating factors for febrile neutropenia during cancer therapy. N Engl J Med. 2013;368(12):1131-1139.
26. Smith TJ et al. Recommendations for the use of WBC growth factors: American Society of Clinical Oncology Clinical Practice Guideline Update. J Clin Oncol. 2015;33(28):3199-3212.
27. Donini M, et al. G-CSF treatment of severe congenital neutropenia reverses neutropenia but does not correct the underlying functional deficiency of the neutrophil in defending against microorganisms. Blood. 2007;109(11):4716-4723.
28. Dale DC, et al. Severe chronic neutropenia: treatment and follow-up of patients in the Severe Chronic Neutropenia International Registry. Am J Hematol. 2003;72(2):82-93.
29. Choi EY, et al. Del-1, an endogenous leukocyteendothelial adhesion inhibitor, limits inflammatory cell recruitment. Science. 2008;322(5904):1101-1104.
30. Shin J, et al. DEL-1 restrains osteoclastogenesis and inhibits inflammatory bone loss in nonhuman primates. Sci Transl Med. 2015;7(307):307ra155.
31. Eskan MA, et al. The leukocyte integrin antagonist Del-1 inhibits IL-17-mediated inflammatory bone loss. Nat Immunol. 2012;13(5):465-473.
32. Hajishengallis G, Chavakis T. Endogenous modulators of inflammatory cell recruitment. Trends Immunol. 2013;34(1):1-6.
33. Casanova-Acebes M, et al. Rhythmic modulation of the hematopoietic niche through neutrophil clearance. Cell. 2013;153(5):1025-1035.
34. Leiva M, Quintana JA, Ligos JM, Hidalgo A. Haematopoietic ESL-1 enables stem cell proliferation in the bone marrow by limiting TGFβ availability. Nat Commun. 2016;7:10222.
35. Maekawa T, et al. Antagonistic effects of IL-17 and D-resolvins on endothelial Del-1 expression through a GSK-3β-C/EBPβ pathway. Nat Commun. 2015;6:8272.
36. Lai AY, Kondo M. Asymmetrical lymphoid and myeloid lineage commitment in multipotent hematopoietic progenitors. J Exp Med. 2006;203(8):1867-1873.
37. Pietras EM, et al. Functionally distinct subsets of lineage-biased multipotent progenitors control blood production in normal and regenerative conditions. Cell Stem Cell. 2015;17(1):35-46.
38. Yang L, et al. Identification of Lin(-)Sca1(+)kit(+) CD34(+)Flt3-short-term hematopoietic stem cells capable of rapidly reconstituting and rescuing myeloablated transplant recipients. Blood. 2005;105(7):2717-2723.
39. Xie Y, et al. Detection of functional haematopoietic stem cell niche using real-time imaging. Nature. 2009;457(7225):97-101.
40. Busch K, et al. Fundamental properties of unperturbed haematopoiesis from stem cells in vivo. Nature. 2015;518(7540):542-546.
41. Wilson A, et al. Hematopoietic stem cells reversibly switch from dormancy to selfrenewal during homeostasis and repair. Cell. 2008;135(6):1118-1129.
42. Passegué E, Wagers AJ, Giuriato S, Anderson WC, Weissman IL. Global analysis of proliferation and cell cycle gene expression in the regulation of hematopoietic stem and progenitor cell fates. J Exp Med. 2005;202(11):1599-1611.
43. Bowie MB, McKnight KD, Kent DG, McCaffrey L, Hoodless PA, Eaves CJ. Hematopoietic stem cells proliferate until after birth and show a reversible phase-specific engraftment defect. J Clin Invest. 2006;116(10):2808-2816.
44. Mettouchi A, et al. Integrin-specific activation of Rac controls progression through the G(1) phase of the cell cycle. Mol Cell. 2001;8(1):115-127.
45. Streuli CH. Integrins and cell-fate determination. J Cell Sci. 2009;122(Pt 2):171-177.
46. Umemoto T, et al. Integrin-αvβ3 regulates thrombopoietin-mediated maintenance of hematopoietic stem cells. Blood. 2012;119(1):83-94.
47. Umemoto T, et al. Expression of Integrin beta3 is correlated to the properties of quiescent hemopoietic stem cells possessing the side population phenotype. J Immunol. 2006;177(11):7733-7739.
48. Papayannopoulou T, Craddock C, Nakamoto B, Priestley GV, Wolf NS. The VLA4/VCAM-1 adhesion pathway defines contrasting mechanisms of lodgement of transplanted murine hemopoietic progenitors between bone marrow and spleen. Proc Natl Acad Sci USA. 1995;92(21):9647-9651.
49. Chen C, Liu Y, Liu Y, Zheng P. Mammalian target of rapamycin activation underlies HSC defects in autoimmune disease and inflammation in mice. J Clin Invest. 2010;120(11):4091-4101.
50. Nagai Y, et al. Toll-like receptors on hematopoietic progenitor cells stimulate innate immune system replenishment. Immunity. 2006;24(6):801-812.
51. Zhao JL, et al. Conversion of danger signals into cytokine signals by hematopoietic stem and progenitor cells for regulation of stress-induced hematopoiesis. Cell Stem Cell. 2014;14(4):445-459.
52. Boettcher S, et al. Endothelial cells translate pathogen signals into G-CSF-driven emergency granulopoiesis. Blood. 2014;124(9):1393-1403.
53. Boettcher S, et al. Cutting edge: LPS-induced emergency myelopoiesis depends on TLR4-expressing nonhematopoietic cells. J Immunol. 2012;188(12):5824-5828.
54. Manz MG, Boettcher S. Emergency granulopoiesis. Nat Rev Immunol. 2014;14(5):302-314.
55. Morrison SJ, Wright DE, Weissman IL. Cyclophosphamide/granulocyte colony-stimulating factor induces hematopoietic stem cells to proliferate prior to mobilization. Proc Natl Acad Sci USA. 1997;94(5):1908-1913.
56. Schuettpelz LG, et al. G-CSF regulates hematopoietic stem cell activity, in part, through activation of Toll-like receptor signaling. Leukemia. 2014;28(9):1851-1860.
57. Semerad CL, et al. G-CSF potently inhibits osteoblast activity and CXCL12 mRNA expression in the bone marrow. Blood. 2005;106(9):3020-3027.
58. Lévesque J-P, Hendy J, Takamatsu Y, Simmons PJ, Bendall LJ. Disruption of the CXCR4/CXCL12 chemotactic interaction during hematopoietic stem cell mobilization induced by GCSF or cyclophosphamide. J Clin Invest. 2003;111(2):187-196.
59. Nakamura-Ishizu A, et al. Extracellular matrix protein tenascin-C is required in the bone marrow microenvironment primed for hematopoietic regeneration. Blood. 2012;119(23):5429-5437.
60. Yu VWC et al. Epigenetic memory underlies cellautonomous heterogeneous behavior of hematopoietic stem cells. Cell. 2016;167(5):1310-1322.e17.
61. Yang J, et al. Single cell transcriptomics reveals unanticipated features of early hematopoietic precursors. Nucleic Acids Res. 2017;45(3):1281-1296.
62. Kozar K et al. Mouse development and cell proliferation in the absence of D-cyclins. Cell. 2004;118(4):477-491.
63. Zhu X, Ohtsubo M, Böhmer RM, Roberts JM, Assoian RK. Adhesion-dependent cell cycle progression linked to the expression of cyclin D1, activation of cyclin E-cdk2, and phosphorylation of the retinoblastoma protein. J Cell Biol. 1996;133(2):391-403.
64. Wang YH, et al. Cell-state-specific metabolic dependency in hematopoiesis and leukemogenesis. Cell. 2014;158(6):1309-1323.
65. Choi EY, et al. Developmental endothelial locus-1 is a homeostatic factor in the central nervous system limiting neuroinflammation and demyelination. Mol Psychiatry. 2015;20(7):880-888.
66. Miller PG, et al. In vivo RNAi screening identifies a leukemia-specific dependence on integrin beta 3 signaling. Cancer Cell. 2013;24(1):45-58.
67. Bruns I, et al. Megakaryocytes regulate hematopoietic stem cell quiescence through CXCL4 secretion. Nat Med. 2014;20(11):1315-1320.
68. Purton LE, Scadden DT. Limiting factors in murine hematopoietic stem cell assays. Cell Stem Cell. 2007;1(3):263-270.
69. Kim K-H, Chen C-C, Alpini G, Lau LF. CCN1 induces hepatic ductular reaction through integrin αvβ5-mediated activation of NF-κB. J Clin Invest. 2015;125(5):1886-1900.
70. Oswald J, et al. Mesenchymal stem cells can be differentiated into endothelial cells in vitro. Stem Cells Dayt. 2004;22(3):377-384.
71. von Dalowski F, et al. Mesenchymal stromal cells for treatment of acute steroid-refractory graft versus host disease: clinical responses and longterm outcome. Stem Cells. 2016;34(2):357-366.
72. Dhawan A, et al. Breast cancer cells compete with hematopoietic stem and progenitor cells for intercellular adhesion molecule 1-mediated binding to the bone marrow microenvironment. Carcinogenesis. 2016;37(8):759-767.
73. Duryagina R, et al. Overexpression of Jagged-1 and its intracellular domain in human mesenchymal stromal cells differentially affect the interaction with hematopoietic stem and progenitor cells. Stem Cells Dev. 2013;22(20):2736-2750.
74. Wobus M, et al. Breast carcinoma cells modulate the chemoattractive activity of human bone marrow-derived mesenchymal stromal cells by interfering with CXCL12. Int J Cancer. 2015;136(1):44-54.
75. Nombela-Arrieta C, et al. Quantitative imaging of haematopoietic stem and progenitor cell localization and hypoxic status in the bone marrow microenvironment. Nat Cell Biol. 2013;15(5):533-543.
76. Choi EY, et al. Regulation of LFA-1-dependent inflammatory cell recruitment by Cbl-b and 14-3-3 proteins. Blood. 2008;111(7):3607-3614.
77. Chung KJ, et al. A self-sustained loop of inflammation-driven inhibition of beige adipogenesis in obesity. Nat Immunol. 2017;18(6):654-664.