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Review

The location and cellular composition of the hemopoietic stem cell niche

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Pages 135-143 | Received 15 Sep 2011, Accepted 05 Oct 2011, Published online: 23 Nov 2011

References

  • Trentin JJ. Determination of bone marrow stem cell differentiation by stromal hemopoietic inductive microenvironments (HIM). Am J Pathol. 1971;65:621–8.
  • Schofield R. The relationship between the spleen colony-forming cell and the haemopoietic stem cell. Blood Cells. 1978;4:7–25.
  • Lord BI, Hendry JH. The distribution of haemopoietic colony-forming units in the mouse femur, and its modification by x rays. Br J Radiol. 1972;45:110–5.
  • Lord BI, Testa NG, Hendry JH. The relative spatial distributions of CFU-S and CFU-C in the normal mouse femur. Blood. 1975;46:65–72.
  • Gong JK. Endosteal marrow: a rich source of hematopoietic stem cells. Science. 1978;199:1443–5.
  • Maloney MA, Lamela RA, Dorie MJ, Patt HM. Concentration gradient of blood stem cells in mouse bone marrow: an open question. Blood. 1978;51:521–5.
  • Mason TM, Lord BI, Hendry JH. The development of spatial distributions of CFU-S and in-vitro CFC in femora of mice of different ages. Br J Haemat. 1989;73:455–61.
  • Schoeters GER, Vanderborght OLJ. Haemopoietic stem cell concentration and CFUs in DNA synthesis in bone marrow from different bone regions. Experientia. 1980;36:459–61.
  • Svoboda V. Distribution of colony-forming cells in mouse bone marrow. Acta Haematol. 1974;51:113–20.
  • Lambertsen RH, Weiss L. A model of intramedullary hematopoietic microenvironments based on stereologic study of the distribution of endocloned marrow colonies. Blood. 1984;63:287–97.
  • Nilsson SK, Dooner MS, Tiarks CY, Weier H-UG, Quesenberry PJ. Potential and distribution of transplanted hematopoietic stem cells in a nonablated mouse model. Blood. 1997;89:4013–20.
  • Nilsson SK, Hulspas R, Weier H-UG, Quesenberry PJ. In situ detection of individual transplanted bone marrow cells using FISH on sections of paraffin-embedded whole murine femurs. J Histochem Cytochem. 1996;44:1069–74.
  • Nilsson SK, Johnston HM, Coverdale JA. Spatial localization of transplanted hemopoietic stem cells: inferences for the localization of stem cell niches. Blood. 2001;97:2293–9.
  • Nilsson SK, Dooner MS, Quesenberry PJ. Synchronized cell-cycle induction of engrafting long-term repopulating stem cells. Blood. 1997;90:4646–50.
  • Yoshimoto M, Shinohara T, Heike T, Shiota M, Kanatsu-Shinohara M, Nakahata T. Direct visualization of transplanted hematopoietic cell reconstitution in intact mouse organs indicates the presence of a niche. Exp Hematol. 2003;31:733–40.
  • Kohler A, Schmithorst V, Filippi MD, Ryan MA, Daria D, Gunzer M, . Altered cellular dynamics and endosteal location of aged early hematopoietic progenitor cells revealed by time-lapse intravital imaging in long bones. Blood. 2009;114:290–298.
  • Lewandowski D, Barroca V, Duconge F, Bayer J, Van Nhieu JT, Pestourie C, . In vivo cellular imaging pinpoints the role of reactive oxygen species in the early steps of adult hematopoietic reconstitution. Blood. 2010;115:443–52.
  • Lo Celso C, Fleming HE, Wu JW, Zhao CX, Miake-Lye S, Fujisaki J, . Live-animal tracking of individual haematopoietic stem/progenitor cells in their niche. Nature. 2009;457:92–6.
  • Suzuki N, Ohneda O, Minegishi N, Nishikawa M, Ohta T, Takahashi S, . Combinatorial Gata2 and Sca1 expression defines hematopoietic stem cells in the bone marrow niche. Proc Natl Acad Sci USA. 2006;103:2202–7.
  • Xie Y, Yin T, Wiegraebe W, He XC, Miller D, Stark D, . Detection of functional haematopoietic stem cell niche using real-time imaging. Nature. 2009;457:97–101.
  • Askenasy N, Zorina T, Farkas DL, Shalit I. Transplanted hematopoietic cells seed in clusters in recipient bone marrow in vivo. Stem Cells. 2002;20:301–10.
  • Askenasy N, Farkas DL. Optical imaging of PKH-labeled hematopoietic cells in recipient bone marrow in vivo. Stem Cells. 2002;20:501–13.
  • Suzuki T, Yokoyama Y, Kumano K, Takanashi M, Kozuma S, Takato T, . Highly efficient ex vivo expansion of human hematopoietic stem cells using Delta1-Fc chimeric protein. Stem Cells. 2006;24:2456–65.
  • Lichtman MA. The ultrastructure of the hemopoietic environment of the marrow: a review. Exp Hematol. 1981;9: 391–410.
  • Yahata T, Muguruma Y, Yumino S, Sheng Y, Uno T, Matsuzawa H, . Quiescent human hematopoietic stem cells in the bone marrow niches organize the hierarchical structure of hematopoiesis. Stem Cells. 2008;26:3228–36.
  • Daldrup-Link HE, Link TM, Rummeny EJ, August C, Konemann S, Jurgens H, . Assessing permeability alterations of the blood–bone marrow barrier due to total body irradiation: in vivo quantification with contrast enhanced magnetic resonance imaging. Bone Marrow Transplant. 2000;25:71–8.
  • Chamberlin W, Barone J, Kedo A, Fried W. Lack of recovery of murine hematopoietic stromal cells after irradiation-induced damage. Blood. 1974;44:385–92.
  • Li XM, Hu Z, Jorgenson ML, Wingard JR, Slayton WB. Bone marrow sinusoidal endothelial cells undergo nonapoptotic cell death and are replaced by proliferating sinusoidal cells in situ to maintain the vascular niche following lethal irradiation. Exp Hematol. 2008;36:1143–56.
  • Plett PA, Frankovitz SM, Orschell-Traycoff CM. In vivo trafficking, cell cycle activity, and engraftment potential of phenotypically defined primitive hematopoietic cells after transplantation into irradiated or nonirradiated recipients. Blood. 2002;100:3545–52.
  • Wang Y, Liu L, Pazhanisamy SK, Li H, Meng A, Zhou D. Total body irradiation causes residual bone marrow injury by induction of persistent oxidative stress in murine hematopoietic stem cells. Free Radic Biol Med. 2010;48:348–56.
  • Narayan K, Juneja S, Garcia C. Effects of 5-fluorouracil or total-body irradiation on murine bone marrow microvasculature. Exp Hematol. 1994;22:142–8.
  • Narayan K, Cliff WJ. Morphology of irradiated microvasculature: a combined in vivo and electron-microscopic study. Am J Pathol. 1982;106:47–62.
  • Kollet O, Shivtiel S, Chen YQ, Suriawinata J, Thung SN, Dabeva MD, . HGF, SDF-1, and MMP-9 are involved in stress-induced human CD34 + stem cell recruitment to the liver. J Clin Invest. 2003;112:160–9.
  • Mazo IB, Quackenbush EJ, Lowe JB, von Andrian UH. Total body irradiation causes profound changes in endothelial traffic molecules for hematopoietic progenitor cell recruitment to bone marrow. Blood. 2002;99:4182–91.
  • Ponomaryov T, Peled A, Petit I, Taichman RS, Habler L, Sandbank J, . Induction of the chemokine stromal-derived factor-1 following DNA damage improves human stem cell function. J Clin Invest. 2000;106:1331–9.
  • Calvi LM, Adams GB, Weibrecht KW, Weber JM, Olson DP, Knight MC, . Osteoblastic cells regulate the haematopoietic stem cell niche. Nature. 2003;425:841–6.
  • Zhang J, Niu C, Ye L, Huang H, He X, Tong WG, . Identification of the haematopoietic stem cell niche and control of the niche size. Nature. 2003;425:836–41.
  • Kiel MJ, Iwashita T, Yilmaz OH, Morrison SJ. Spatial differences in hematopoiesis but not in stem cells indicate a lack of regional patterning in definitive hematopoietic stem cells. Dev Biol. 2005;283:29–39.
  • Sacchetti B, Funari A, Michienzi S, Di Cesare S, Piersanti S, Saggio I, . Self-renewing osteoprogenitors in bone marrow sinusoids can organize a hematopoietic microenvironment. Cell. 2007;131:324–36.
  • Sorrentino A, Ferracin M, Castelli G, Biffoni M, Tomaselli G, Baiocchi M, . Isolation and characterization of CD146 + multipotent mesenchymal stromal cells. Exp Hematol. 2008;36:1035–46.
  • 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;25:977–88.
  • Weiss L. The hematopoietic microenvironment of the bone marrow: an ultrastructural study of the stroma in rats. Anat Rec. 1976;186:161–84.
  • Weiss L, Geduldig U. Barrier cells: stromal regulation of hematopoiesis and blood cell release in normal and stressed murine bone marrow. Blood. 1991;78:975–90.
  • Oh IH, Kwon KR. Concise review: multiple niches for hematopoietic stem cell regulations. Stem Cells. 2010;28: 1243–9.
  • Ehninger A, Trumpp A. The bone marrow stem cell niche grows up: mesenchymal stem cells and macrophages move in. J Exp Med. 2011;208:421–8.
  • Taichman RS, Emerson SG. Human osteoblasts support hematopoiesis through the production of granulocyte colony-stimulating factor. J Exp Med. 1994;179:1677–82.
  • Taichman RS, Reilly MJ, Emerson SG. Human osteoblasts support human hematopoietic progenitor cells in vitro bone marrow cultures. Blood. 1996;87:518–24.
  • Pereira RM, Delany AM, Durant D, Canalis E. Cortisol regulates the expression of Notch in osteoblasts. J Cell Biochem. 2002;85:252–8.
  • Karanu FN, Murdoch B, Gallacher L, Wu DM, Koremoto M, Sakano S, . The notch ligand jagged-1 represents a novel growth factor of human hematopoietic stem cells. J Exp Med. 2000;192:1365–72.
  • Milner LA, Bigas A. Notch as a mediator of cell fate determination in hematopoiesis: evidence and speculation. Blood. 1999;93:2431–48.
  • Hosokawa K, Arai F, Yoshihara H, Nakamura Y, Gomei Y, Iwasaki H, . Function of oxidative stress in the regulation of hematopoietic stem cell-niche interaction. Biochem Biophys Res Commun. 2007;363:578–83.
  • Wilson A, Murphy MJ, Oskarsson T, Kaloulis K, Bettess MD, Oser GM, . c-Myc controls the balance between hematopoietic stem cell self-renewal and differentiation. Genes Dev. 2004;18:2747–63.
  • Visnjic D, Kalajzic Z, Rowe DW, Katavic V, Lorenzo J, Aguila HL. Hematopoiesis is severely altered in mice with an induced osteoblast deficiency. Blood. 2004;103:3258–64.
  • Zhu J, Garrett R, Jung Y, Zhang Y, Kim N, Wang J, . Osteoblasts support B-lymphocyte commitment and differentiation from hematopoietic stem cells. Blood. 2007;109: 3706–12.
  • Visnjic D, Kalajzic I, Gronowicz G, Aguila HL, Clark SH, Lichtler AC, . Conditional ablation of the osteoblast lineage in Col2.3deltatk transgenic mice. J Bone Miner Res. 2001;16:2222–31.
  • Kiel MJ, Radice GL, Morrison SJ. Lack of evidence that hematopoietic stem cells depend on N-cadherin-mediated adhesion to osteoblasts for their maintenance. Cell Stem Cell. 2007;1:204–17.
  • Chen XD, Shi S, Xu T, Robey PG, Young MF. Age-related osteoporosis in biglycan-deficient mice is related to defects in bone marrow stromal cells. J Bone Miner Res. 2002;17: 331–40.
  • Qian H, Buza-Vidas N, Hyland CD, Jensen CT, Antonchuk J, Mansson R, . Critical role of thrombopoietin in maintaining adult quiescent hematopoietic stem cells. Cell Stem Cell. 2007;1:671–84.
  • Yoshihara H, Arai F, Hosokawa K, Hagiwara T, Takubo K, Nakamura Y, . Thrombopoietin/MPL signaling regulates hematopoietic stem cell quiescence and interaction with the osteoblastic niche. Cell Stem Cell. 2007;1:685–97.
  • Arai F, Yoshihara H, Hosokawa K, Nakamura Y, Gomei Y, Iwasaki H, . Niche regulation of hematopoietic stem cells in the endosteum. Ann NY Acad Sci. 2009;1176:36–46.
  • Nilsson SK, Johnston HM, Whitty GA, Williams B, Webb RJ, Denhardt DT, . Osteopontin, a key component of the hematopoietic stem cell niche and regulator of primitive hematopoietic progenitor cells. Blood. 2005;106:1232–9.
  • Stier S, Ko Y, Forkert R, Lutz C, Neuhaus T, Grunewald E, . Osteopontin is a hematopoietic stem cell niche component that negatively regulates stem cell pool size. J Exp Med. 2005;201:1781–91.
  • Grassinger J, Haylock DN, Storan MJ, Haines GO, Williams B, Whitty GA, . Thrombin-cleaved osteopontin regulates hemopoietic stem and progenitor cell functions through interactions with alpha9beta1 and alpha4beta1 integrins. Blood. 2009;114:49–59.
  • Arai F, Hirao A, Ohmura M, Sato H, Matsuoka S, Takubo K, . Tie2/angiopoietin-1 signaling regulates hematopoietic stem cell quiescence in the bone marrow niche. Cell. 2004;118:149–61.
  • Jung Y, Wang J, Schneider A, Sun YX, Koh-Paige AJ, Osman NI, . Regulation of SDF-1 (CXCL12) production by osteoblasts; a possible mechanism for stem cell homing. Bone. 2006;38:497–508.
  • Hosokawa K, Arai F, Yoshihara H, Iwasaki H, Nakamura Y, Gomei Y, . Knockdown of N-cadherin suppresses the long-term engraftment of hematopoietic stem cells. Blood. 2010;116:554–63.
  • Gillette JM, Larochelle A, Dunbar CE, Lippincott-Schwartz J. Intercellular transfer to signalling endosomes regulates an ex vivo bone marrow niche. Nat Cell Biol. 2009;11:303–11.
  • Mancini SJ, Mantei N, Dumortier A, Suter U, MacDonald HR, Radtke F. Jagged1-dependent Notch signaling is dispensable for hematopoietic stem cell self-renewal and differentiation. Blood. 2005;105:2340–2.
  • Li P, Zon LI. Resolving the controversy about N-cadherin and hematopoietic stem cells. Cell Stem Cell. 2010;6:199–202.
  • Kiel MJ, Acar M, Radice GL, Morrison SJ. Hematopoietic stem cells do not depend on N-cadherin to regulate their maintenance. Cell Stem Cell. 2009;4:170–9.
  • Jung Y, Wang J, Havens A, Sun Y, Jin T, Taichman RS. Cell-to-cell contact is critical for the survival of hematopoietic progenitor cells on osteoblasts. Cytokine. 2005;32:155–62.
  • Mendez-Ferrer S, Michurina TV, Ferraro F, Mazloom AR, Macarthur BD, Lira SA, . Mesenchymal and haematopoietic stem cells form a unique bone marrow niche. Nature. 2010;466:829–34.
  • Omatsu Y, Sugiyama T, Kohara H, Kondoh G, Fujii N, Kohno K, . The essential functions of adipo-osteogenic progenitors as the hematopoietic stem and progenitor cell niche. Immunity. 2010;33:387–99.
  • Goodman JW, Hodgson GS. Evidence for stem cells in the peripheral blood of mice. Blood. 1962;19:702–14.
  • Fleming WH, Alpern EJ, Uchida N, Ikuta K, Weissman IL. Steel factor influences the distribution and activity of murine hematopoietic stem cells in vivo. Proc Natl Acad Sci USA. 1993;90:3760–4.
  • Wright DE, Wagers AJ, Gulati AP, Johnson FL, Weissman IL. Physiological migration of hematopoietic stem and progenitor cells. Science. 2001;294:1933–6.
  • Massberg S, Schaerli P, Knezevic-Maramica I, Kollnberger M, Tubo N, Moseman EA, . Immunosurveillance by hematopoietic progenitor cells trafficking through blood, lymph, and peripheral tissues. Cell. 2007;131:994–1008.
  • Abkowitz JL, Robinson AE, Kale S, Long MW, Chen J. Mobilization of hematopoietic stem cells during homeostasis and after cytokine exposure. Blood. 2003;102:1249–53.
  • Mendez-Ferrer S, Lucas D, Battista M, Frenette PS. Haematopoietic stem cell release is regulated by circadian oscillations. Nature. 2008;452:442–7.
  • McKinney-Freeman S, Goodell MA. Circulating hematopoietic stem cells do not efficiently home to bone marrow during homeostasis. Exp Hematol. 2004;32:868–76.
  • Bhattacharya D, Czechowicz A, Ooi AG, Rossi DJ, Bryder D, Weissman IL. Niche recycling through division-independent egress of hematopoietic stem cells. J Exp Med. 2009;206: 2837–50.
  • Sipkins DA, Wei X, Wu JW, Runnels JM, Cote D, Means TK, . In vivo imaging of specialized bone marrow endothelial microdomains for tumour engraftment. Nature. 2005;435:969–73.
  • Winkler IG, Levesque JP. Mechanisms of hematopoietic stem cell mobilization: when innate immunity assails the cells that make blood and bone. Exp Hematol. 2006;34: 996–1009.
  • Kiel MJ, Yilmaz OH, Iwashita T, Terhorst C, Morrison SJ. SLAM family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells. Cell. 2005;121:1109–21.
  • Ellis SL, Grassinger J, Jones A, Borg J, Camenisch T, Haylock D, . The relationship between bone, hemopoietic stem cells, and vasculature. Blood. 2011;118:1516–24.
  • 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;121:1109–21.
  • Rafii S, Shapiro F, Pettengell R, Ferris B, Nachman RL, Moore MA, . Human bone marrow microvascular endothelial cells support long-term proliferation and differentiation of myeloid and megakaryocytic progenitors. Blood. 1995;86:3353–63.
  • Avecilla ST, Hattori K, Heissig B, Tejada R, Liao F, Shido K, . Chemokine-mediated interaction of hematopoietic progenitors with the bone marrow vascular niche is required for thrombopoiesis. Nat Med. 2004;10:64–71.
  • Kopp HG, Avecilla ST, Hooper AT, Rafii S. The bone marrow vascular niche: home of HSC differentiation and mobilization. Physiology (Bethesda). 2005;20:349–56.
  • Haylock DN, Williams B, Johnston HM, Liu MC, Rutherford KE, Whitty GA, . Hemopoietic stem cells with higher hemopoietic potential reside at the bone marrow endosteum. Stem Cells. 2007;25:1062–9.
  • Li Z, Li L. Understanding hematopoietic stem-cell microenvironments. Trends Biochem Sci. 2006;31:589–95.
  • Wilson A, Trumpp A. Bone-marrow haematopoietic-stem-cell niches. Nat Rev Immunol. 2006;6:93–106.
  • Weiss L, Chen L-T. The organization of hematopoietic cords and vascular sinuses in bone marrow. Blood Cells. 1975;1: 617–38.
  • Yamazaki K, Allen TD. Ultrastructural and morphometric alterations in bone marrow stromal tissue after 7 Gy irradiation. Blood Cells. 1991;17:527–49.
  • Katayama Y, Battista M, Kao WM, Hidalgo A, Peired AJ, Thomas SA, . Signals from the sympathetic nervous system regulate hematopoietic stem cell egress from bone marrow. Cell. 2006;124:407–21.
  • McKee MD, Nanci A. Osteopontin: an interfacial extracellular matrix protein in mineralized tissues. Connect Tissue Res. 1996;35:197–205.
  • Kollet O, Dar A, Shivtiel S, Kalinkovich A, Lapid K, Sztainberg Y, . Osteoclasts degrade endosteal components and promote mobilization of hematopoietic progenitor cells. Nat Med. 2006;12:657–64.
  • Silver IA, Murrills RJ, Etherington DJ. Microelectrode studies on the acid microenvironment beneath adherent macrophages and osteoclasts. Exp Cell Res. 1988;175:266–76.
  • Adams GB, Chabner KT, Alley IR, Olson DP, Szczepiorkowski ZM, Poznansky MC, . Stem cell engraftment at the endosteal niche is specified by the calcium-sensing receptor. Nature. 2006;439:599–603.
  • DiMascio L, Voermans C, Uqoezwa M, Duncan A, Lu D, Wu J, . Identification of adiponectin as a novel hemopoietic stem cell growth factor. J Immunol. 2007;178:3511–20.
  • Naveiras O, Nardi V, Wenzel PL, Hauschka PV, Fahey F, Daley GQ. Bone-marrow adipocytes as negative regulators of the haematopoietic microenvironment. Nature. 2009;460:259–63.
  • Lei Z, Xiaoying Z, Xingguo L. Ovariectomy-associated changes in bone mineral density and bone marrow haematopoiesis in rats. Int J Exp Pathol. 2009;90:512–9.
  • Beeton CA, Bord S, Ireland D, Compston JE. Osteoclast formation and bone resorption are inhibited by megakaryocytes. Bone. 2006;39:985–90.
  • Kacena MA, Gundberg CM, Horowitz MC. A reciprocal regulatory interaction between megakaryocytes, bone cells, and hematopoietic stem cells. Bone. 2006;39:978–84.
  • Kacena MA, Shivdasani RA, Wilson K, Xi Y, Troiano N, Nazarian A, . Megakaryocyte-osteoblast interaction revealed in mice deficient in transcription factors GATA-1 and NF-E2. J Bone Miner Res. 2004;19:652–60.
  • Bord S, Frith E, Ireland DC, Scott MA, Craig JI, Compston JE. Megakaryocytes modulate osteoblast synthesis of type-l collagen, osteoprotegerin, and RANKL. Bone. 2005;36: 812–9.
  • Dominici M, Rasini V, Bussolari R, Chen X, Hofmann TJ, Spano C, . Restoration and reversible expansion of the osteoblastic hematopoietic stem cell niche after marrow radioablation. Blood. 2009;114:2333–2243.

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