Quantitative spatial analysis of haematopoiesis-regulating stromal cells in the bone marrow microenvironment by 3D microscopy

被引:111
作者
Gomariz, Alvaro [1 ,2 ,3 ]
Helbling, Patrick M. [1 ,2 ]
Isringhausen, Stephan [1 ,2 ]
Suessbier, Ute [1 ,2 ]
Becker, Anton [4 ]
Boss, Andreas [4 ]
Nagasawa, Takashi [5 ]
Paul, Gregory [3 ]
Goksel, Orcun [3 ]
Szekely, Gabor [3 ]
Stoma, Szymon [6 ]
Norrelykke, Simon F. [6 ]
Manz, Markus G. [1 ,2 ]
Nombela-Arrieta, Cesar [1 ,2 ]
机构
[1] Univ Hosp, Hematol, CH-8091 Zurich, Switzerland
[2] Univ Zurich, CH-8091 Zurich, Switzerland
[3] Swiss Fed Inst Technol, Comp Vis Lab, CH-8092 Zurich, Switzerland
[4] Univ Hosp Zurich, Dept Diagnost & Intervent Radiol, CH-8091 Zurich, Switzerland
[5] Osaka Univ, Dept Microbiol & Immunol, Osaka 5650871, Japan
[6] Swiss Fed Inst Technol, Sci Ctr Opt & Electron Microscopy ScopeM, CH-8093 Zurich, Switzerland
基金
瑞士国家科学基金会;
关键词
STEM-CELLS; ENDOTHELIAL-CELLS; T-CELLS; NICHES; REGENERATION; PROGENITORS; MAINTENANCE; HOMEOSTASIS; BLOOD; THROMBOPOIESIS;
D O I
10.1038/s41467-018-04770-z
中图分类号
O [数理科学和化学]; P [天文学、地球科学]; Q [生物科学]; N [自然科学总论];
学科分类号
07 ; 0710 ; 09 ;
摘要
Sinusoidal endothelial cells and mesenchymal CXCL12-abundant reticular cells are principal bone marrow stromal components, which critically modulate haematopoiesis at various levels, including haematopoietic stem cell maintenance. These stromal subsets are thought to be scarce and function via highly specific interactions in anatomically confined niches. Yet, knowledge on their abundance, global distribution and spatial associations remains limited. Using three-dimensional quantitative microscopy we show that sinusoidal endothelial and mesenchymal reticular subsets are remarkably more abundant than estimated by conventional flow cytometry. Moreover, both cell types assemble in topologically complex networks, associate to extracellular matrix and pervade marrow tissues. Through spatial statistical methods we challenge previous models and demonstrate that even in the absence of major specific interaction forces, virtually all tissue-resident cells are invariably in physical contact with, or close proximity to, mesenchymal reticular and sinusoidal endothelial cells. We further show that basic structural features of these stromal components are preserved during ageing.
引用
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页数:15
相关论文
共 74 条
[1]   Deep imaging of bone marrow shows non-dividing stem cells are mainly perisinusoidal [J].
Acar, Melih ;
Kocherlakota, Kiranmai S. ;
Murphy, Malea M. ;
Peyer, James G. ;
Oguro, Hideyuki ;
Inra, Christopher N. ;
Jaiyeola, Christabel ;
Zhao, Zhiyu ;
Luby-Phelps, Katherine ;
Morrison, Sean J. .
NATURE, 2015, 526 (7571) :126-+
[2]   Adipocyte Accumulation in the Bone Marrow during Obesity and Aging Impairs Stem Cell-Based Hematopoietic and Bone Regeneration [J].
Ambrosi, Thomas H. ;
Scialdone, Antonio ;
Graja, Antonia ;
Gohlke, Sabrina ;
Jank, Anne-Marie ;
Bocian, Carla ;
Woelk, Lena ;
Fan, Hua ;
Logan, Darren W. ;
Schuermann, Annette ;
Saraiva, Luis R. ;
Schulz, Tim J. .
CELL STEM CELL, 2017, 20 (06) :771-+
[3]  
[Anonymous], 2016, CHAP HALL CRC INTERD
[4]   Long-term hematopoietic stem cells require stromal cell-derived factor-1 for colonizing bone marrow during ontogeny [J].
Ara, T ;
Tokoyoda, K ;
Sugiyama, T ;
Egawa, T ;
Kawabata, K ;
Nagasawa, T .
IMMUNITY, 2003, 19 (02) :257-267
[5]   Differential cytokine contributions of perivascular haematopoietic stern cell niches [J].
Asada, Noboru ;
Kunisaki, Yuya ;
Pierce, Halley ;
Wang, Zichen ;
Fernandez, Nicolas F. ;
Birbrair, Alexander ;
Ma'ayan, Avi ;
Frenette, Paul S. .
NATURE CELL BIOLOGY, 2017, 19 (03) :214-223
[6]   Chemokine-mediated interaction of hematopoietic progenitors with the bone marrow vascular niche is required for thrombopoiesis [J].
Avecilla, ST ;
Hattori, K ;
Heissig, B ;
Tejada, R ;
Liao, F ;
Shido, K ;
Jin, DK ;
Dias, S ;
Zhang, F ;
Hartman, TE ;
Hackett, NR ;
Crystal, RG ;
Witte, L ;
Hicklin, DJ ;
Bohlen, P ;
Eaton, D ;
Lyden, D ;
de Sauvage, F ;
Rafii, S .
NATURE MEDICINE, 2004, 10 (01) :64-71
[7]   Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells [J].
Bettelli, E ;
Carrier, YJ ;
Gao, WD ;
Korn, T ;
Strom, TB ;
Oukka, M ;
Weiner, HL ;
Kuchroo, VK .
NATURE, 2006, 441 (7090) :235-238
[8]   Flow Dynamics and HSPC Homing in Bone Marrow Microvessels [J].
Bixel, M. Gabriele ;
Kusumbe, Anjali P. ;
Ramasamy, Saravana K. ;
Sivaraj, Kishor K. ;
Butz, Stefan ;
Vestweber, Dietmar ;
Adams, Ralf H. .
CELL REPORTS, 2017, 18 (07) :1804-1816
[9]   Endothelial cells translate pathogen signals into G-CSF-driven emergency granulopoiesis [J].
Boettcher, Steffen ;
Gerosa, Rahel C. ;
Radpour, Ramin ;
Bauer, Judith ;
Ampenberger, Franziska ;
Heikenwalder, Mathias ;
Kopf, Manfred ;
Manz, Markus G. .
BLOOD, 2014, 124 (09) :1393-1403
[10]   In Vivo Labeling by CD73 Marks Multipotent Stromal Cells and Highlights Endothelial Heterogeneity in the Bone Marrow Niche [J].
Breitbach, Martin ;
Kimura, Kenichi ;
Luis, Tiago C. ;
Fuegemann, Christopher J. ;
Woll, Petter S. ;
Hesse, Michael ;
Facchini, Raffaella ;
Rieck, Sarah ;
Jobin, Katarzyna ;
Reinhardt, Julia ;
Ohneda, Osamu ;
Wenzel, Daniela ;
Geisen, Caroline ;
Kurts, Christian ;
Kastenmueller, Wolfgang ;
Hoelzel, Michael ;
Jacobsen, Sten E. W. ;
Fleischmann, Bernd K. .
CELL STEM CELL, 2018, 22 (02) :262-+