In vivo imaging of hematopoietic stem cells and their microenvironment

In this review we provide a description of the basic concepts and paradigms currently constituting the foundations of adult stem cell biology, and discuss the role that live imaging techniques have in the development of the field. We focus on live imaging of hematopoietic stem cells (HSCs) as the basic biology and clinical applications of HSCs have historically been at the forefront of the stem cell field, and HSC are the first mammalian tissue stem cells to be visualized in vivo using advanced light microscopy techniques. We outline the current technical challenges that remain to be overcome before stem cells and their niche can be more fully characterized using the live imaging technology.

[1]  Timm Schroeder,et al.  Imaging stem-cell-driven regeneration in mammals , 2008, Nature.

[2]  F. Watt,et al.  Contribution of stem cells and differentiated cells to epidermal tumours , 2003, Nature Reviews Cancer.

[3]  M. Raaijmakers,et al.  ATP-binding-cassette transporters in hematopoietic stem cells and their utility as therapeutical targets in acute and chronic myeloid leukemia , 2007, Leukemia.

[4]  S. Rafii,et al.  The bone marrow vascular niche: home of HSC differentiation and mobilization. , 2005, Physiology.

[5]  Hiromitsu Nakauchi,et al.  Long-Term Lymphohematopoietic Reconstitution by a Single CD34-Low/Negative Hematopoietic Stem Cell , 1996, Science.

[6]  Haiyang Huang,et al.  Identification of the haematopoietic stem cell niche and control of the niche size , 2003, Nature.

[7]  D. Farkas,et al.  Optical Imaging of PKH‐Labeled Hematopoietic Cells in Recipient Bone Marrow In Vivo , 2002, Stem cells.

[8]  David Bryder,et al.  Hematopoietic stem cells: the paradigmatic tissue-specific stem cell. , 2006, The American journal of pathology.

[9]  G. Spangrude,et al.  Resting and activated subsets of mouse multipotent hematopoietic stem cells. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[10]  J. Till,et al.  A direct measurement of the radiation sensitivity of normal mouse bone marrow cells. , 1961, Radiation research.

[11]  M. Starnbach,et al.  Activation of bone marrow–resident memory T cells by circulating, antigen-bearing dendritic cells , 2005, Nature Immunology.

[12]  Katta G. Murty,et al.  On KΔ , 1986, Discret. Appl. Math..

[13]  D. Scadden,et al.  Evolving concepts on the microenvironmental niche for hematopoietic stem cells , 2008, Current opinion in hematology.

[14]  D. Scadden,et al.  The leukemic stem cell niche: current concepts and therapeutic opportunities. , 2009, Blood.

[15]  E. Fuchs,et al.  Socializing with the Neighbors Stem Cells and Their Niche , 2004, Cell.

[16]  Lihong V. Wang,et al.  Noninvasive laser-induced photoacoustic tomography for structural and functional in vivo imaging of the brain , 2003, Nature Biotechnology.

[17]  Yousef Al-Kofahi,et al.  Associative image analysis: A method for automated quantification of 3D multi-parameter images of brain tissue , 2008, Journal of Neuroscience Methods.

[18]  A. S. Conner,et al.  Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo , 1996, The Journal of experimental medicine.

[19]  Daniel Lucas,et al.  Haematopoietic stem cell release is regulated by circadian oscillations , 2008, Nature.

[20]  D. Scadden,et al.  Limiting factors in murine hematopoietic stem cell assays. , 2007, Cell stem cell.

[21]  T. A. Hewett,et al.  The relative quiescence of hematopoietic stem cells in nonhuman primates. , 2001, Blood.

[22]  I. Weissman,et al.  In vivo proliferation and cell cycle kinetics of long-term self-renewing hematopoietic stem cells. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[23]  I. Weissman,et al.  The long-term repopulating subset of hematopoietic stem cells is deterministic and isolatable by phenotype. , 1994, Immunity.

[24]  D. Kaufman,et al.  Donor cell leukemia: insight into cancer stem cells and the stem cell niche. , 2007, Blood.

[25]  U. V. von Andrian,et al.  Perisinusoidal B cells in the bone marrow participate in T-independent responses to blood-borne microbes. , 2005, Immunity.

[26]  Ulo Langel,et al.  Cell-penetrating peptides: mechanism and kinetics of cargo delivery. , 2005, Advanced drug delivery reviews.

[27]  D. Rowe,et al.  Hematopoiesis is severely altered in mice with an induced osteoblast deficiency. , 2004, Blood.

[28]  D. Farkas,et al.  The tale of early hematopoietic cell seeding in the bone marrow niche. , 2006, Stem cells and development.

[29]  Nobuko Uchida,et al.  Long-term monitoring of transplanted human neural stem cells in developmental and pathological contexts with MRI , 2007, Proceedings of the National Academy of Sciences.

[30]  J. Dick,et al.  Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell , 1997, Nature Medicine.

[31]  S. Gronthos,et al.  Concise Review: Mesenchymal Stromal Cells: Potential for Cardiovascular Repair , 2008, Stem cells.

[32]  Irving L. Weissman,et al.  Shifting foci of hematopoiesis during reconstitution from single stem cells , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[33]  J. Dick,et al.  Cancer stem cells: lessons from leukemia. , 2005, Trends in cell biology.

[34]  David W. Rowe,et al.  Live-animal tracking of individual haematopoietic stem/progenitor cells in their niche , 2009, Nature.

[35]  Darwin J. Prockop,et al.  Transplantability and therapeutic effects of bone marrow-derived mesenchymal cells in children with osteogenesis imperfecta , 1999, Nature Medicine.

[36]  Angela C. Colmone,et al.  Leukemic Cells Create Bone Marrow Niches That Disrupt the Behavior of Normal Hematopoietic Progenitor Cells , 2008, Science.

[37]  Steffen Jung,et al.  Perivascular clusters of dendritic cells provide critical survival signals to B cells in bone marrow niches , 2008, Nature Immunology.

[38]  Pieter C Dorrestein,et al.  A monovalent streptavidin with a single femtomolar biotin binding site , 2006, Nature Methods.

[39]  S. Gerson,et al.  DNA repair defects in stem cell function and aging. , 2005, Annual review of medicine.

[40]  W. Denk,et al.  Adaptive wavefront correction in two-photon microscopy using coherence-gated wavefront sensing , 2006, Proceedings of the National Academy of Sciences.

[41]  R. Weinberg,et al.  Transitions between epithelial and mesenchymal states: acquisition of malignant and stem cell traits , 2009, Nature Reviews Cancer.

[42]  M. Little,et al.  A Side Order of Stem Cells: The SP Phenotype , 2006, Stem cells.

[43]  David L Kaplan,et al.  Stem cell- and scaffold-based tissue engineering approaches to osteochondral regenerative medicine. , 2009, Seminars in cell & developmental biology.

[44]  Mary Anne Wheeler,et al.  Stem , 1985 .

[45]  I. Weissman,et al.  Establishment of a normal hematopoietic and leukemia stem cell hierarchy. , 2008, Cold Spring Harbor symposia on quantitative biology.

[46]  J. Hendry,et al.  Clonogenic Cells and Stem Cells in Epidermis , 1973 .

[47]  Keisuke Ito,et al.  Tie2/Angiopoietin-1 Signaling Regulates Hematopoietic Stem Cell Quiescence in the Bone Marrow Niche , 2004, Cell.

[48]  Charles P. Lin,et al.  CXCR4 inhibitor AMD3100 disrupts the interaction of multiple myeloma cells with the bone marrow microenvironment and enhances their sensitivity to therapy. , 2009, Blood.

[49]  B. Williams,et al.  Quiescence, cycling, and turnover in the primitive hematopoietic stem cell compartment. , 1997, Experimental hematology.

[50]  D. Brömme,et al.  Differences in matrix composition between calvaria and long bone in mice suggest differences in biomechanical properties and resorption: Special emphasis on collagen. , 2008, Bone.

[51]  D. Scadden,et al.  The stem-cell niche as an entity of action , 2006, Nature.

[52]  Richard O. Hynes,et al.  Hematopoietic Progenitor Cell Rolling in Bone Marrow Microvessels: Parallel Contributions by Endothelial Selectins and Vascular Cell Adhesion Molecule 1 , 1998, The Journal of experimental medicine.

[53]  Laurie E Ailles,et al.  Granulocyte-macrophage progenitors as candidate leukemic stem cells in blast-crisis CML. , 2004, The New England journal of medicine.

[54]  A. Uccelli,et al.  Mesenchymal stem cells in health and disease , 2008, Nature Reviews Immunology.

[55]  Joseph E Italiano,et al.  Dynamic Visualization of Thrombopoiesis Within Bone Marrow , 2007, Science.

[56]  D. Scadden,et al.  Osteoblastic cells regulate the haematopoietic stem cell niche , 2003, Nature.

[57]  H. Nakauchi,et al.  The ABC transporter Bcrp1/ABCG2 is expressed in a wide variety of stem cells and is a molecular determinant of the side-population phenotype , 2001, Nature Medicine.

[58]  J. Audet,et al.  Flow cytometric screening of cell-penetrating peptides for their uptake into embryonic and adult stem cells. , 2007, Analytical biochemistry.

[59]  G. G. Stokes.  "J." , 1890, The New Yale Book of Quotations.

[60]  E. Thomas,et al.  Intravenous infusion of bone marrow in patients receiving radiation and chemotherapy. , 1957, The New England journal of medicine.

[61]  S. Morrison,et al.  Supplemental Experimental Procedures , 2022 .

[62]  J. Schuetz,et al.  Bcrp1 gene expression is required for normal numbers of side population stem cells in mice, and confers relative protection to mitoxantrone in hematopoietic cells in vivo , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[63]  A. Cope,et al.  Strontium can increase some osteoblasts without increasing hematopoietic stem cells. , 2008, Blood.

[64]  R. Schofield.  The relationship between the spleen colony-forming cell and the haemopoietic stem cell. , 1978, Blood cells.

[65]  Xunbin Wei,et al.  In vivo imaging of specialized bone marrow endothelial microdomains for tumour engraftment , 2005, Nature.

[66]  Lihong V. Wang,et al.  Functional photoacoustic microscopy for high-resolution and noninvasive in vivo imaging , 2006, Nature Biotechnology.

[67]  E. Fuchs,et al.  Defining the Epithelial Stem Cell Niche in Skin , 2004, Science.

[68]  Luke E. K. Achenie,et al.  Expression Profile of Osteoblast Lineage at Defined Stages of Differentiation* , 2005, Journal of Biological Chemistry.

[69]  E. Rummeny,et al.  Migration of iron oxide-labeled human hematopoietic progenitor cells in a mouse model: in vivo monitoring with 1.5-T MR imaging equipment. , 2005, Radiology.

[70]  S. Morrison,et al.  Lack of evidence that hematopoietic stem cells depend on N-cadherin-mediated adhesion to osteoblasts for their maintenance. , 2007, Cell stem cell.

[71]  Robert S Negrin,et al.  Hematopoietic stem and progenitor cells: clinical and preclinical regeneration of the hematolymphoid system. , 2005, Annual review of medicine.

[72]  Robert Lanza,et al.  Essentials of stem cell biology , 2009 .