Imaging and spatial analysis of hematopoietic stem cell niches.


Journal

Annals of the New York Academy of Sciences
ISSN: 1749-6632
Titre abrégé: Ann N Y Acad Sci
Pays: United States
ID NLM: 7506858

Informations de publication

Date de publication:
04 2020
Historique:
received: 30 03 2019
revised: 30 05 2019
accepted: 06 06 2019
pubmed: 2 8 2019
medline: 2 10 2020
entrez: 2 8 2019
Statut: ppublish

Résumé

Hematopoietic stem cells (HSCs) have been long proposed to reside in defined anatomical locations within bone marrow (BM) tissues in direct contact or close proximity to nurturing cell types. Imaging techniques that allow the simultaneous mapping of HSCs and interacting cell types have been central to the discovery of basic principles of these so-called HSC niches. Despite major progress in the field, a quantitative and comprehensive model of the cellular and molecular components that define these specialized microenvironments is lacking to date, and uncertainties remain on the preferential localization of HSCs in the context of complex BM tissue landscapes. Recent technological breakthroughs currently allow for the quantitative spatial analysis of BM cellular components with extraordinary precision. Here, we critically discuss essential technical aspects related to imaging approaches, image processing tools, and spatial statistics, which constitute the three basic elements of rigorous quantitative spatial analyses of HSC niches in the BM microenvironment.

Identifiants

pubmed: 31368140
doi: 10.1111/nyas.14184
doi:

Types de publication

Journal Article Review

Langues

eng

Sous-ensembles de citation

IM

Pagination

5-16

Informations de copyright

© 2019 New York Academy of Sciences.

Références

Miller, H.J. 2004. Tobler's first law and spatial analysis. Ann. Assoc. Am. Geogr. 94: 284-289.
Bissell, M.J. & W.C. Hines. 2011. Why don't we get more cancer? A proposed role of the microenvironment in restraining cancer progression. Nat. Med. 17: 320-329.
Decker, M., J. Leslie, Q. Liu, et al. 2018. Hepatic thrombopoietin is required for bone marrow hematopoietic stem cell maintenance. Science 360: 106-110.
Morrison, S.J. & A.C. Spradling. 2008. Stem cells and niches: mechanisms that promote stem cell maintenance throughout life. Cell 132: 598-611.
Scadden, D.T. 2014. Nice neighborhood: emerging concepts of the stem cell niche. Cell 157: 41-50.
Cheung, T.H. & T.A. Rando. 2013. Molecular regulation of stem cell quiescence. Nat. Rev. Mol. Cell Biol. 14: 329-340.
Nombela-Arrieta, C. & M.G. Manz. 2017. Quantification and three-dimensional microanatomical organization of the bone marrow. Blood Adv. 1: 407-416.
Mendelson, A. & P.S. Frenette. 2014. Hematopoietic stem cell niche maintenance during homeostasis and regeneration. Nat. Med. 20: 833-846.
Hoggatt, J., Y. Kfoury & D.T. Scadden. 2016. Hematopoietic stem cell niche in health and disease. Annu. Rev. Pathol. Mech. Dis. 11: 555-581.
Crane, G.M., E. Jeffery & S.J. Morrison. 2017. Adult haematopoietic stem cell niches. Nat. Rev. Immunol. 4: 573-590.
Morrison, S.J. & D.T. Scadden. 2014. The bone marrow niche for haematopoietic stem cells. Nature 505: 327-334.
Orkin, S.H. & L.I. Zon. 2008. Hematopoiesis: an evolving paradigm for stem cell biology. Cell 132: 631-644.
Eaves, C.J. 2015. Hematopoietic stem cells: concepts, definitions, and the new reality. Blood 125: 2605-2613.
Schofield, R. 1978. The relationship between the spleen colony-forming cell and the haemopoietic stem cell. Blood Cells 4: 7-25.
Kiel, M.J., Ö.H. Yilmaz, T. Iwashita, et al. 2005. SLAM family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells. Cell 121: 1109-1121.
Acar, M., K.S. Kocherlakota, M.M. Murphy, et al. 2015. Deep imaging of bone marrow shows non-dividing stem cells are mainly perisinusoidal. Nature 526: 126-130.
Gazit, R., P.K. Mandal, W. Ebina, et al. 2014. Fgd5 identifies hematopoietic stem cells in the murine bone marrow. J. Exp. Med. 107: 1315-1331.
Sawai, C.M., S. Babovic, S. Upadhaya, et al. 2016. Hematopoietic stem cells are the major source of multilineage hematopoiesis in adult animals. Immunity 45: 597-609.
Chen, J.Y., S.K. Wang, S. Yamazaki, et al. 2016. Hoxb5 marks long-term haematopoietic stem cells and reveals a homogenous perivascular niche. Nature 530: 223-227.
Baryawno, N., D. Przybylski, M.S. Kowalczyk, et al. 2019. A cellular taxonomy of the bone marrow stroma in homeostasis and leukemia. Cell. https://doi.org/10.1016/j.cell.2019.04.040.
Tikhonova, A.N., I. Dolgalev, H. Hu, et al. 2019. The bone marrow microenvironment at single-cell resolution. Nature 505: 1-28.
Kfoury, Y. & D.T. Scadden. 2015. Mesenchymal cell contributions to the stem cell niche. Cell Stem Cell 16: 239-253.
Wilson, A., E. Laurenti, G. Oser, et al. 2008. Hematopoietic stem cells reversibly switch from dormancy to self-renewal during homeostasis and repair. Cell 135: 1118-1129.
Arai, F., A. Hirao, M. Ohmura, et al. 2004. Tie2/angiopoietin-1 signaling regulates hematopoietic stem cell quiescence in the bone marrow niche. Cell 118: 149-161.
Xie, Y., T. Yin, W. Wiegraebe, et al. 2008. Detection of functional haematopoietic stem cell niche using real-time imaging. Nature 457: 97-102.
Zhang, J., C. Niu, L. Ye, et al. 2003. Identification of the haematopoietic stem cell niche and control of the niche size. Nature 425: 836-841.
Zhao, M., F. Tao, A. Venkatraman, et al. 2019. N-cadherin-expressing bone and marrow stromal progenitor cells maintain reserve hematopoietic stem cells. Cell Rep. 26: 652-669.e6.
Cordeiro Gomes, A., T. Hara, V.Y. Lim, et al. 2016. Hematopoietic stem cell niches produce lineage-instructive signals to control multipotent progenitor differentiation. Immunity 45: 1219-1231.
Zhao, M., J.M. Perry, H. Marshall, et al. 2014. Megakaryocytes maintain homeostatic quiescence and promote post-injury regeneration of hematopoietic stem cells. Nat. Med. 20: 1321-1326.
Nombela Arrieta, C., G. Pivarnik, B. Winkel, et al. 2013. Quantitative imaging of haematopoietic stem and progenitor cell localization and hypoxic status in the bone marrow microenvironment. Nat. Cell Biol. 15: 533-543.
Yamazaki, S., H. Ema, G. Karlsson, et al. 2011. Nonmyelinating Schwann cells maintain hematopoietic stem cell hibernation in the bone marrow niche. Cell 147: 1146-1158.
Ntziachristos, V. 2010. Going deeper than microscopy: the optical imaging frontier in biology. Nat. Method 7: 603-614.
Richardson, D.S. & J.W. Lichtman. 2015. Clarifying tissue clearing. Cell 162: 246-257.
Susaki, E.A. & H.R. Ueda. 2016. Whole-body and whole-organ clearing and imaging techniques with single-cell resolution: toward organism-level systems biology in mammals. Cell Chem. Biol. 23: 137-157.
Gomariz, A., P.M. Helbling, S. Isringhausen, et al. 2018. Quantitative spatial analysis of haematopoiesis-regulating stromal cells in the bone marrow microenvironment by 3D microscopy. Nat. Commun. 9: 407-415.
Grüneboom, A., I. Hawwari, D. Weidner, et al. 2019. A network of trans-cortical capillaries as mainstay for blood circulation in long bones. Nat. Metab. 1: 236-250.
Coutu, D.L., K.D. Kokkaliaris, L. Kunz, et al. 2017. Multicolor quantitative confocal imaging cytometry. Nat. Method 15: 39-46.
Stegner, D., J.M.M. vanEeuwijk, O. Angay, et al. 2017. Thrombopoiesis is spatially regulated by the bone marrow vasculature. Nat. Commun. 8: 127.
Greenbaum, A., K.Y. Chan, T. Dobreva, et al. 2017. Bone CLARITY: clearing, imaging, and computational analysis of osteoprogenitors within intact bone marrow. Sci. Transl. Med. 9: eaah6518.
Celso, C.L., H.E. Fleming, J.W. Wu, et al. 2008. Live-animal tracking of individual haematopoietic stem/progenitor cells in their niche. Nature 457: 92-97.
Foster, K., F. Lassailly, F. Anjos-Afonso, et al. 2015. Different motile behaviors of human hematopoietic stem versus progenitor cells at the osteoblastic niche. Stem Cell Rep. 5: 690-701.
Celso, C.L., J.W. Wu & C.P. Lin. 2009. In vivo imaging of hematopoietic stem cells and their microenvironment. J. Biophoton. 2: 619-631.
Joseph, C., J.M. Quach, C.R. Walkley, et al. 2013. Deciphering hematopoietic stem cells in their niches: a critical appraisal of genetic models, lineage tracing, and imaging strategies. Cell Stem Cell 13: 520-533.
Ding, L., T.L. Saunders, G. Enikolopov, et al. 2012. Endothelial and perivascular cells maintain haematopoietic stem cells. Nature 481: 457-462.
Sugiyama, T., H. Kohara, M. Noda, et al. 2006. Maintenance of the hematopoietic stem cell pool by CXCL12-CXCR4 chemokine signaling in bone marrow stromal cell niches. Immunity 25: 977-988.
Méndez-Ferrer, S., T. von Michurina, F. Ferraro, et al. 2010. Mesenchymal and haematopoietic stem cells form a unique bone marrow niche. Nature 466: 829-834.
Asada, N., Y. Kunisaki, H. Pierce, et al. 2017. Differential cytokine contributions of perivascular haematopoietic stem cell niches. Nat. Cell Biol. 19: 214-223.
Bruns, I., D. Lucas, S. Pinho, et al. 2014. Megakaryocytes regulate hematopoietic stem cell quiescence through CXCL4 secretion. Nat. Med. 20: 1315-1320.
Sbalzarini, I.F. 2016. Seeing is believing: quantifying is convincing: computational image analysis in biology. Adv. Anat. Embryol. Cell Biol. 219: 1-39.
Sommer, C., C. Straehle, U. Kothe, et al. 2011. Ilastik: interactive learning and segmentation toolkit. In 2011 IEEE International Symposium on Biomedical Imaging: From Nano to Macro, 230-233.
Jones, T.R., I. Kang, D.B. Wheeler, et al. 2008. CellProfiler analyst: data exploration and analysis software for complex image-based screens. BMC Bioinformatics 9: 482-16.
Schindelin, J., I. Arganda-Carreras, E. Frise, et al. 2012. Fiji: an open-source platform for biological-image analysis. Nat. Method 9: 676-682.
Meijering, E., A.E. Carpenter, H. Peng, et al. 2016. Imagining the future of bioimage analysis. Nat. Biotechnol. 34: 1250-1255.
Myers, G. 2012. Why bioimage informatics matters. Nat. Method 9: 659-660.
Eliceiri, K.W., M.R. Berthold, I.G. Goldberg, et al. 2012. Biological imaging software tools. Nat. Method 9: 697-710.
Ljosa, V., K.L. Sokolnicki & A.E. Carpenter. 2012. Annotated high-throughput microscopy image sets for validation. Nat. Method 9: 637-637.
Maška, M., V. Ulman, D. Svoboda, et al. 2014. A benchmark for comparison of cell tracking algorithms. Bioinformatics 30: 1609-1617.
Caicedo, J.C., J. Roth, A. Goodman, et al. 2018. Evaluation of deep learning strategies for nucleus segmentation in fluorescence images. bioRxiv. https://doi.org/10.1101/335216.
Hollandi, R., A. Szkalisity, T. Toth, et al. 2019. A deep learning framework for nucleus segmentation using image style transfer. bioRxiv. https://doi.org/10.1101/580605.
Helmuth, J.A., G. Paul & I.F. Sbalzarini. 2010. Beyond co-localization: inferring spatial interactions between sub-cellular structures from microscopy images. BMC Bioinformatics 11: 372.
Kunisaki, Y., I. Bruns, C. Scheiermann, et al. 2013. Arteriolar niches maintain haematopoietic stem cell quiescence. Nature 502: 637-643.
Pinho, S., T. Marchand, E. Yang, et al. 2018. Lineage-biased hematopoietic stem cells are regulated by distinct niches. Dev. Cell 44: 634-641.e4.
Chen, X., H. Deng, M.J. Churchill, et al. 2017. Bone marrow myeloid cells regulate myeloid-biased hematopoietic stem cells via a histamine-dependent feedback loop. Cell Stem Cell 21: 747-760.e7.
Mokhtari, Z., F. Mech, S. Zehentmeier, et al. 2015. Quantitative image analysis of cell colocalization in murine bone marrow. Cytometry 87: 503-512.
Li, Y., T.D. Majarian, A.W. Naik, et al. 2016. Point process models for localization and interdependence of punctate cellular structures. Cytometry 89: 633-643.
Jammalamadaka, A., P. Suwannatat, S.K. Fisher, et al. 2015. Characterizing spatial distributions of astrocytes in the mammalian retina. Bioinformatics 31: 2024-2031.
Baddeley, A., E. Rubak & R. Turner. 2015. Spatial Point Patterns. CRC Press.

Auteurs

Alvaro Gomariz (A)

Department of Medical Oncology and Hematology, University Hospital, University of Zurich, Zurich, Switzerland.

Stephan Isringhausen (S)

Department of Medical Oncology and Hematology, University Hospital, University of Zurich, Zurich, Switzerland.

Patrick M Helbling (PM)

Department of Medical Oncology and Hematology, University Hospital, University of Zurich, Zurich, Switzerland.

César Nombela-Arrieta (C)

Department of Medical Oncology and Hematology, University Hospital, University of Zurich, Zurich, Switzerland.

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