SLAM Family Receptors Distinguish Hematopoietic Stem and Progenitor Cells and Reveal Endothelial Niches for Stem Cells

doi:10.1016/J.CELL.2005.05.026

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SLAM Family Receptors Distinguish Hematopoietic Stem and Progenitor Cells and Reveal Endothelial Niches for Stem Cells

Journal Article•DOI•

SLAM Family Receptors Distinguish Hematopoietic Stem and Progenitor Cells and Reveal Endothelial Niches for Stem Cells

Mark J. Kiel¹, Ömer H. Yilmaz¹, Toshihide Iwashita¹, Osman H. Yilmaz¹, Cox Terhorst², Sean J. Morrison¹ - Show less +2 more•Institutions (2)

University of Michigan¹, Beth Israel Deaconess Medical Center²

01 Jul 2005-Cell (Cell Press)-Vol. 121, Iss: 7, pp 1109-1121

TL;DR: This work compared the gene expression profiles of highly purified HSCs and non-self-renewing multipotent hematopoietic progenitors and found that both groups occupied multiple niches, including sinusoidal endothelium in diverse tissues.

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About: This article is published in Cell.The article was published on 2005-07-01 and is currently open access. It has received 3091 citations till now. The article focuses on the topics: Hematopoietic stem cell niche & Stem cell.

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Journal Article•DOI•

Mesenchymal and haematopoietic stem cells form a unique bone marrow niche

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Simón Méndez-Ferrer¹, Tatyana V. Michurina², Francesca Ferraro³, Amin R. Mazloom¹, Ben D. MacArthur⁴, Ben D. MacArthur¹, Sergio A. Lira¹, David T. Scadden³, Avi Ma'ayan¹, Grigori Enikolopov², Paul S. Frenette¹, Paul S. Frenette⁵ - Show less +8 more•Institutions (5)

Icahn School of Medicine at Mount Sinai¹, Cold Spring Harbor Laboratory², Harvard University³, Centro Nacional de Investigaciones Cardiovasculares⁴, Albert Einstein College of Medicine⁵

12 Aug 2010-Nature

TL;DR: It is demonstrated that mesenchymal stem cells (MSCs), identified using nestin expression, constitute an essential HSC niche component and are indicative of a unique niche in the bone marrow made of heterotypic stem-cell pairs.

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Abstract: The cellular constituents forming the haematopoietic stem cell (HSC) niche in the bone marrow are unclear, with studies implicating osteoblasts, endothelial and perivascular cells. Here we demonstrate that mesenchymal stem cells (MSCs), identified using nestin expression, constitute an essential HSC niche component. Nestin(+) MSCs contain all the bone-marrow colony-forming-unit fibroblastic activity and can be propagated as non-adherent 'mesenspheres' that can self-renew and expand in serial transplantations. Nestin(+) MSCs are spatially associated with HSCs and adrenergic nerve fibres, and highly express HSC maintenance genes. These genes, and others triggering osteoblastic differentiation, are selectively downregulated during enforced HSC mobilization or beta3 adrenoreceptor activation. Whereas parathormone administration doubles the number of bone marrow nestin(+) cells and favours their osteoblastic differentiation, in vivo nestin(+) cell depletion rapidly reduces HSC content in the bone marrow. Purified HSCs home near nestin(+) MSCs in the bone marrow of lethally irradiated mice, whereas in vivo nestin(+) cell depletion significantly reduces bone marrow homing of haematopoietic progenitors. These results uncover an unprecedented partnership between two distinct somatic stem-cell types and are indicative of a unique niche in the bone marrow made of heterotypic stem-cell pairs.

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3,012 citations

Journal Article•DOI•

Self-Renewing Osteoprogenitors in Bone Marrow Sinusoids Can Organize a Hematopoietic Microenvironment

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Benedetto Sacchetti¹, Alessia Funari², Stefano Michienzi¹, Silvia Di Cesare, Stefania Piersanti, Isabella Saggio³, Isabella Saggio¹, Enrico Tagliafico, Stefano Ferrari, Pamela Gehron Robey⁴, Mara Riminucci², Paolo Bianco¹ - Show less +8 more•Institutions (4)

Sapienza University of Rome¹, University of L'Aquila², National Research Council³, National Institutes of Health⁴

19 Oct 2007-Cell

TL;DR: It is shown that MCAM/CD146-expressing, subendothelial cells in human BM stroma are capable of transferring, upon transplantation, the HME to heterotopic sites, coincident with the establishment of identical subendOThelial cells within a miniature bone organ.

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2,093 citations

Cites background from "SLAM Family Receptors Distinguish H..."

..., 2003), as well as to endothelial cells lining sinusoids (Kiel et al., 2005), suggesting a potential multiplicity of physiologically important...
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...and sinusoidal surfaces (Kiel et al., 2005), but also CXCL12-expressing ‘‘reticular’’ cells within the hematopoietic space (Sugiyama et al....
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...As (self-renewing) progenitors of sinusoidal adventitial reticular cells, CD146+ stromal cells contribute to the organization, and become an integral part, of the structure of sinusoidal walls, in the vicinities of which HSCs have been directly localized (Kiel et al., 2005)....
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...A body of evidence also suggests that endosteal (Calvi et al., 2003; Zhang et al., 2003) and sinusoidal surfaces (Kiel et al., 2005), but also CXCL12-expressing ‘‘reticular’’ cells within the hematopoietic space (Sugiyama et al., 2006), may represent specific sites of HSC regulation (‘‘niches’’)....
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...of sinusoidal walls, in the vicinities of which HSCs have been directly localized (Kiel et al., 2005)....
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Journal Article•DOI•

A Perivascular Niche for Brain Tumor Stem Cells

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Christopher Calabrese¹, Helen Poppleton¹, Mehmet Kocak¹, Twala L. Hogg¹, Christine E. Fuller¹, Blair Hamner¹, Eun Young Oh¹, M. Waleed Gaber¹, David Finklestein¹, Meredith Allen¹, Adrian J. Frank¹, Ildar T. Bayazitov¹, Stanislav S. Zakharenko¹, Amar Gajjar¹, Andrew M. Davidoff¹, Richard J. Gilbertson¹ - Show less +12 more•Institutions (1)

St. Jude Children's Research Hospital¹

01 Jan 2007-Cancer Cell

TL;DR: This work shows that endothelial cells interact closely with self-renewing brain tumor cells and secrete factors that maintain these cells in a stem cell-like state, and proposes that brain CSCs are maintained within vascular niches that are important targets for therapeutic approaches.

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2,065 citations

Cites background from "SLAM Family Receptors Distinguish H..."

...CSCs have been identified in established brain tumor cell lines and are responsible for the in vivo malignancy of these cells (Kondo et al., 2004)....
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Journal Article•DOI•

Maintenance of the Hematopoietic Stem Cell Pool by CXCL12-CXCR4 Chemokine Signaling in Bone Marrow Stromal Cell Niches

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Tatsuki Sugiyama¹, Hiroshi Kohara¹, Mamiko Noda¹, Takashi Nagasawa¹•Institutions (1)

Kyoto University¹

01 Dec 2006-Immunity

TL;DR: It is shown that the induced deletion of CXCR4, a receptor for CXC chemokine ligand (CXCL) 12 in adult mice, resulted in severe reduction of HSC numbers and increased sensitivity to myelotoxic injury, although it did not impair expansion of the more mature progenitors.

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2,046 citations

Cites background or result from "SLAM Family Receptors Distinguish H..."

...jp with sinusoidal endothelium although only some HSCs adjoin the endosteum (Kiel et al., 2005)....
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...Many CD150CD48(2)CD41(2) cells are associated with the sinusoidal endothelium in the bone marrow (Kiel et al., 2005)....
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...Consistent with previous studies (Kiel et al., 2005; Tokoyoda et al., 2004), many c-kit+Sca-1+ and CD150+CD482 CD412 cells were found scattered throughout the marrow, and the remaining cells resided near the bone surface (data not shown)....
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...Consistent with previous studies (Kiel et al., 2005; Tokoyoda et al., 2004), many c-kitSca-1 and CD150CD48(2) CD41(2) cells were found scattered throughout the marrow, and the remaining cells resided near the bone surface (data not shown)....
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...Considering that many HSCs are associated with sinusoidal endothelium (Kiel et al., 2005), our findings that almost all c-kitSca-1 and CD150CD48(2) CD41(2) cells near the sinusoidal endothelium were in contact with CAR cells surrounding endothelial cells in the extravascular space suggest that HSCs in vascular niches are in contact with CAR cells, raising the possibility that CAR cells are a critical cellular component of vascular niches (Ara et al....
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Journal Article•DOI•

The bone marrow niche for haematopoietic stem cells

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Sean J. Morrison¹, David T. Scadden²•Institutions (2)

University of Texas Southwestern Medical Center¹, Harvard University²

16 Jan 2014-Nature

TL;DR: The haematopoietic stem cell niche remains incompletely defined and beset by competing models, and outstanding questions concern the cellular complexity of the niche, the role of the endosteum and functional heterogeneity among perivascular microenvironments.

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Abstract: Niches are local tissue microenvironments that maintain and regulate stem cells. Haematopoiesis provides a model for understanding mammalian stem cells and their niches, but the haematopoietic stem cell (HSC) niche remains incompletely defined and beset by competing models. Recent progress has been made in elucidating the location and cellular components of the HSC niche in the bone marrow. The niche is perivascular, created partly by mesenchymal stromal cells and endothelial cells and often, but not always, located near trabecular bone. Outstanding questions concern the cellular complexity of the niche, the role of the endosteum and functional heterogeneity among perivascular microenvironments.

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1,899 citations

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References

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Open Access

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Journal Article•DOI•

A novel multigene family may encode odorant receptors: A molecular basis for odor recognition

[...]

Linda B. Buck¹, Richard Axel²•Institutions (2)

Columbia University¹, Howard Hughes Medical Institute²

05 Apr 1991-Cell

TL;DR: This work has cloned and characterized 18 different members of an extremely large multigene family that encodes seven transmembrane domain proteins whose expression is restricted to the olfactory epithelium and is likely to encode a diverse family of odorant receptors.

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4,537 citations

"SLAM Family Receptors Distinguish H..." refers background in this paper

...The locations and identities of olfactory sensory neurons and chemosensory neurons are distinguished by their differential expression of olfactory receptors (Buck and Axel, 1991) and Mrg family receptors (Dong et al., 2001), respectively....
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Journal Article•DOI•

Osteoblastic cells regulate the haematopoietic stem cell niche

[...]

Laura M. Calvi¹, Gregor B. Adams², Kathryn W. Weibrecht², Jonathan M. Weber¹, David P. Olson², M. C. Knight², Roderick P. Martin², Ernestina Schipani², P. Divieti², F. R. Bringhurst², Laurie A. Milner¹, Henry M. Kronenberg², David T. Scadden² - Show less +9 more•Institutions (2)

University of Rochester¹, Harvard University²

23 Oct 2003-Nature

TL;DR: Osteoblastic cells are a regulatory component of the haematopoietic stem cell niche in vivo that influences stem cell function through Notch activation.

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Abstract: Stem cell fate is influenced by specialized microenvironments that remain poorly defined in mammals. To explore the possibility that haematopoietic stem cells derive regulatory information from bone, accounting for the localization of haematopoiesis in bone marrow, we assessed mice that were genetically altered to produce osteoblast-specific, activated PTH/PTHrP receptors (PPRs). Here we show that PPR-stimulated osteoblastic cells that are increased in number produce high levels of the Notch ligand jagged 1 and support an increase in the number of haematopoietic stem cells with evidence of Notch1 activation in vivo. Furthermore, ligand-dependent activation of PPR with parathyroid hormone (PTH) increased the number of osteoblasts in stromal cultures, and augmented ex vivo primitive haematopoietic cell growth that was abrogated by gamma-secretase inhibition of Notch activation. An increase in the number of stem cells was observed in wild-type animals after PTH injection, and survival after bone marrow transplantation was markedly improved. Therefore, osteoblastic cells are a regulatory component of the haematopoietic stem cell niche in vivo that influences stem cell function through Notch activation. Niche constituent cells or signalling pathways provide pharmacological targets with therapeutic potential for stem-cell-based therapies.

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3,434 citations

"SLAM Family Receptors Distinguish H..." refers background or result in this paper

...HSCs that localized to endosteum were presumably associated with osteoblasts, consistent with prior studies (Calvi et al., 2003; Zhang et al., 2003; Arai et al., 2004; Visnjic et al., 2004)....
[...]
...Studies of various transgenic mice have demonstrated the functional importance of osteoblasts in regulating bone marrow HSCs (Calvi et al., 2003; Zhang et al., 2003; Visnjic et al., 2004)....
[...]

Journal Article•DOI•

Identification of the haematopoietic stem cell niche and control of the niche size

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Jiwang Zhang¹, Chao Niu¹, Ling Ye², Haiyang Huang², Xi C. He¹, Wei Gang Tong¹, Jason Ross¹, Jeffrey S. Haug¹, Teri Johnson¹, Jian Q. Feng², Stephen E. Harris², Leanne M. Wiedemann³, Leanne M. Wiedemann¹, Yuji Mishina⁴, Linheng Li³, Linheng Li¹ - Show less +12 more•Institutions (4)

Stowers Institute for Medical Research¹, University of Missouri–Kansas City², University of Kansas³, National Institutes of Health⁴

23 Oct 2003-Nature

TL;DR: It is concluded that SNO cells lining the bone surface function as a key component of the niche to support HSCs, and that BMP signalling through BMPRIA controls the number of H SCs by regulating niche size.

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Abstract: Haematopoietic stem cells (HSCs) are a subset of bone marrow cells that are capable of self-renewal and of forming all types of blood cells (multi-potential). However, the HSC 'niche'--the in vivo regulatory microenvironment where HSCs reside--and the mechanisms involved in controlling the number of adult HSCs remain largely unknown. The bone morphogenetic protein (BMP) signal has an essential role in inducing haematopoietic tissue during embryogenesis. We investigated the roles of the BMP signalling pathway in regulating adult HSC development in vivo by analysing mutant mice with conditional inactivation of BMP receptor type IA (BMPRIA). Here we show that an increase in the number of spindle-shaped N-cadherin+CD45- osteoblastic (SNO) cells correlates with an increase in the number of HSCs. The long-term HSCs are found attached to SNO cells. Two adherens junction molecules, N-cadherin and beta-catenin, are asymmetrically localized between the SNO cells and the long-term HSCs. We conclude that SNO cells lining the bone surface function as a key component of the niche to support HSCs, and that BMP signalling through BMPRIA controls the number of HSCs by regulating niche size.

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2,949 citations

"SLAM Family Receptors Distinguish H..." refers background or result in this paper

...Immunofluorescence studies with markers of primitive hematopoietic progenitors have suggested that HSCs interact with osteoblasts at the endosteum of bone marrow (Zhang et al., 2003; Arai et al., 2004; Wilson et al., 2004)....
[...]
...%) were associated with endosteum, consistent with prior studies (Zhang et al., 2003; Arai et al., 2004; Wilson et al., 2004), and another nine cells were not associated with recognizable cell types....
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...…Endothelium rior studies have imaged the interaction of primitive ematopoietic progenitors with osteoblasts in the endsteum of bone marrow (Zhang et al., 2003; Arai et al., 004; Wilson et al., 2004) (see Figures S2D and S2E for chematic of bone marrow and spleen), but HSCs have ot been…...
[...]
...HSCs that localized to endosteum were presumably associated with osteoblasts, consistent with prior studies (Calvi et al., 2003; Zhang et al., 2003; Arai et al., 2004; Visnjic et al., 2004)....
[...]
...Studies of various transgenic mice have demonstrated the functional importance of osteoblasts in regulating bone marrow HSCs (Calvi et al., 2003; Zhang et al., 2003; Visnjic et al., 2004)....
[...]

Journal Article•DOI•

Purification and Characterization of Mouse Hematopoietic Stem Cells

[...]

Gerald J. Spangrude¹, Shelly Heimfeld¹, Irving L. Weissman¹•Institutions (1)

Stanford University¹

01 Jul 1988-Science

TL;DR: Mouse bone marrow hematopoietic stem cells were isolated with the use of a variety of phenotypic markers and thirty of these cells are sufficient to save 50 percent of lethally irradiated mice, and to reconstitute all blood cell types in the survivors.

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Abstract: Mouse bone marrow hematopoietic stem cells were isolated with the use of a variety of phenotypic markers. These cells can proliferate and differentiate with approximately unit efficiency into myelomonocytic cells, B cells, or T cells. Thirty of these cells are sufficient to save 50 percent of lethally irradiated mice, and to reconstitute all blood cell types in the survivors.

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2,893 citations

Journal Article•DOI•

Long-Term Lymphohematopoietic Reconstitution by a Single CD34-Low/Negative Hematopoietic Stem Cell

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Masatake Osawa¹, Ken-ichi Hanada², Hirofumi Hamada², Hiromitsu Nakauchi¹•Institutions (2)

University of Tsukuba¹, Japanese Foundation for Cancer Research²

12 Jul 1996-Science

TL;DR: A monoclonal antibody raised to the mouse homolog of CD34 (mCD34) was used to purify mouse HSCs to near homogeneity to enable analysis of the self-renewal and multilineage differentiation of individual HSCS.

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Abstract: Hematopoietic stem cells (HSCs) supply all blood cells throughout life by making use of their self-renewal and multilineage differentiation capabilities. A monoclonal antibody raised to the mouse homolog of CD34 (mCD34) was used to purify mouse HSCs to near homogeneity. Unlike in humans, primitive adult mouse bone marrow HSCs were detected in the mCD34 low to negative fraction. Injection of a single mCD34(lo/-), c-Kit+, Sca-1(+), lineage markers negative (Lin-) cell resulted in long-term reconstitution of the lymphohematopoietic system in 21 percent of recipients. Thus, the purified HSC population should enable analysis of the self-renewal and multilineage differentiation of individual HSCs.

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2,134 citations