Cellular and Molecular Life Sciences

, Volume 73, Issue 4, pp 687–703 | Cite as

Adhesion receptors involved in HSC and early-B cell interactions with bone marrow microenvironment

  • Maria De Grandis
  • Anne-Catherine Lhoumeau
  • Stéphane J. C. Mancini
  • Michel Aurrand-Lions


Hematopoiesis takes place in the bone marrow of adult mammals and is the process by which blood cells are replenished every day throughout life. Differentiation of hematopoietic cells occurs in a stepwise manner through intermediates of differentiation that could be phenotypically identified. This has allowed establishing hematopoietic cell classification with hematopoietic stem cells (HSCs) at the top of the hierarchy. HSCs are mostly quiescent and serve as a reservoir for maintenance of lifelong hematopoiesis. Over recent years, it has become increasingly clear that HSC quiescence is not only due to intrinsic properties, but is also mediated by cognate interactions between HSCs and surrounding cells within micro-anatomical sites called “niches”. This hematopoietic/stromal crosstalk model also applies to more mature progenitors such as B cell progenitors, which are thought to reside in distinct “niches”. This prompted many research teams to search for specific molecular mechanisms supporting leuko-stromal crosstalk in the bone marrow and acting at specific stage of differentiation to regulate hematopoietic homeostasis. Here, we review recent data on adhesion mechanisms involved in HSCs and B cell progenitors interactions with surrounding bone marrow stromal cells.


Adhesion Niche Hematopoietic stem cell B cell 



The authors apologize to those whose work has not been cited due to space limitation. MDG is supported by a grant from “Fondation de France”. Our laboratory is supported by Inca (# 5940), ARC Foundation (PJA# 20141201990 to MAL; PJA# 20131200298 to SM), SIRIC (# INCa-DGOS-Inserm 6038), PACA Cancéropôle and PACA Region.


  1. 1.
    Discher DE, Mooney DJ, Zandstra PW (2009) Growth factors, matrices, and forces combine and control stem cells. Science 324:1673–1677PubMedCentralPubMedCrossRefGoogle Scholar
  2. 2.
    Gattazzo F, Urciuolo A, Bonaldo P (2014) Extracellular matrix: a dynamic microenvironment for stem cell niche. Biochim Biophys Acta 1840:2506–2519PubMedCentralPubMedCrossRefGoogle Scholar
  3. 3.
    Nilsson SK, Debatis ME, Dooner MS, Madri JA, Quesenberry PJ, Becker PS (1998) Immunofluorescence characterization of key extracellular matrix proteins in murine bone marrow in situ. J Histochem Cytochem 46:371–377PubMedCrossRefGoogle Scholar
  4. 4.
    Nilsson SK, Johnston HM, Whitty GA, Williams B, Webb RJ, Denhardt DT, Bertoncello I, Bendall LJ, Simmons PJ, Haylock DN (2005) Osteopontin, a key component of the hematopoietic stem cell niche and regulator of primitive hematopoietic progenitor cells. Blood 106:1232–1239PubMedCrossRefGoogle Scholar
  5. 5.
    Klamer S, Voermans C (2014) The role of novel and known extracellular matrix and adhesion molecules in the homeostatic and regenerative bone marrow microenvironment. Cell Adh Migr 8:563–577PubMedPubMedCentralCrossRefGoogle Scholar
  6. 6.
    Calvi LM, Adams GB, Weibrecht KW, Weber JM, Olson DP, Knight MC, Martin RP, Schipani E, Divieti P, Bringhurst FR, Milner LA, Kronenberg HM, Scadden DT (2003) Osteoblastic cells regulate the haematopoietic stem cell niche. Nature 425:841–846PubMedCrossRefGoogle Scholar
  7. 7.
    Chan CK, Chen CC, Luppen CA, Kim JB, DeBoer AT, Wei K, Helms JA, Kuo CJ, Kraft DL, Weissman IL (2009) Endochondral ossification is required for haematopoietic stem-cell niche formation. Nature 457:490–494PubMedCentralPubMedCrossRefGoogle Scholar
  8. 8.
    Grassinger J, Haylock DN, Williams B, Olsen GH, Nilsson SK (2010) Phenotypically identical hemopoietic stem cells isolated from different regions of bone marrow have different biologic potential. Blood 116:3185–3196PubMedCrossRefGoogle Scholar
  9. 9.
    Shiozawa Y, Taichman RS (2012) Getting blood from bone: an emerging understanding of the role that osteoblasts play in regulating hematopoietic stem cells within their niche. Exp Hematol 40:685–694PubMedCentralPubMedCrossRefGoogle Scholar
  10. 10.
    Arai F, Hirao A, Ohmura M, Sato H, Matsuoka S, Takubo K, Ito K, Koh GY, Suda T (2004) Tie2/angiopoietin-1 signaling regulates hematopoietic stem cell quiescence in the bone marrow niche. Cell 118:149–161PubMedCrossRefGoogle Scholar
  11. 11.
    Yoshihara H, Arai F, Hosokawa K, Hagiwara T, Takubo K, Nakamura Y, Gomei Y, Iwasaki H, Matsuoka S, Miyamoto K, Miyazaki H, Takahashi T, Suda T (2007) Thrombopoietin/MPL signaling regulates hematopoietic stem cell quiescence and interaction with the osteoblastic niche. Cell Stem Cell 1:685–697PubMedCrossRefGoogle Scholar
  12. 12.
    Thoren LA, Liuba K, Bryder D, Nygren JM, Jensen CT, Qian H, Antonchuk J, Jacobsen SE (2008) Kit regulates maintenance of quiescent hematopoietic stem cells. J Immunol 180:2045–2053PubMedCrossRefGoogle Scholar
  13. 13.
    Zhang J, Niu C, Ye L, Huang H, He X, Tong WG, Ross J, Haug J, Johnson T, Feng JQ, Harris S, Wiedemann LM, Mishina Y, Li L (2003) Identification of the haematopoietic stem cell niche and control of the niche size. Nature 425:836–841PubMedCrossRefGoogle Scholar
  14. 14.
    El-Badri NS, Wang BY, Cherry, Good RA (1998) Osteoblasts promote engraftment of allogeneic hematopoietic stem cells. Exp Hematol 26:110–116PubMedGoogle Scholar
  15. 15.
    Greenbaum A, Hsu YM, Day RB, Schuettpelz LG, Christopher MJ, Borgerding JN, Nagasawa T, Link DC (2013) CXCL12 in early mesenchymal progenitors is required for haematopoietic stem-cell maintenance. Nature 495:227–230PubMedCentralPubMedCrossRefGoogle Scholar
  16. 16.
    Ding L, Saunders TL, Enikolopov G, Morrison SJ (2012) Endothelial and perivascular cells maintain haematopoietic stem cells. Nature 481:457–462PubMedCentralPubMedCrossRefGoogle Scholar
  17. 17.
    Takubo K, Goda N, Yamada W, Iriuchishima H, Ikeda E, Kubota Y, Shima H, Johnson RS, Hirao A, Suematsu M, Suda T (2010) Regulation of the HIF-1alpha level is essential for hematopoietic stem cells. Cell Stem Cell 7:391–402PubMedCrossRefGoogle Scholar
  18. 18.
    Adams GB, Chabner KT, Alley IR, Olson DP, Szczepiorkowski ZM, Poznansky MC, Kos CH, Pollak MR, Brown EM, Scadden DT (2006) Stem cell engraftment at the endosteal niche is specified by the calcium-sensing receptor. Nature 439:599–603PubMedCrossRefGoogle Scholar
  19. 19.
    Kiel MJ, Yilmaz OH, Iwashita T, Terhorst C, Morrison SJ (2005) SLAM family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells. Cell 121:1109–1121PubMedCrossRefGoogle Scholar
  20. 20.
    Wilson A, Trumpp A (2006) Bone-marrow haematopoietic-stem-cell niches. Nat Rev Immunol 6:93–106PubMedCrossRefGoogle Scholar
  21. 21.
    Kopp HG, Avecilla ST, Hooper AT, Rafii S (2005) The bone marrow vascular niche: home of HSC differentiation and mobilization. Physiology (Bethesda) 20:349–356CrossRefGoogle Scholar
  22. 22.
    Rafii S, Shapiro F, Rimarachin J, Nachman RL, Ferris B, Weksler B, Moore MA, Asch AS (1994) Isolation and characterization of human bone marrow microvascular endothelial cells: hematopoietic progenitor cell adhesion. Blood 84:10–19PubMedGoogle Scholar
  23. 23.
    Schweitzer KM, Vicart P, Delouis C, Paulin D, Drager AM, Langenhuijsen MM, Weksler BB (1997) Characterization of a newly established human bone marrow endothelial cell line: distinct adhesive properties for hematopoietic progenitors compared with human umbilical vein endothelial cells. Lab Invest 76:25–36PubMedGoogle Scholar
  24. 24.
    Wang L, Benedito R, Bixel MG, Zeuschner D, Stehling M, Savendahl L, Haigh JJ, Snippert H, Clevers H, Breier G, Kiefer F, Adams RH (2013) Identification of a clonally expanding haematopoietic compartment in bone marrow. EMBO J 32:219–230PubMedCentralPubMedCrossRefGoogle Scholar
  25. 25.
    Rafii S, Mohle R, Shapiro F, Frey BM, Moore MA (1997) Regulation of hematopoiesis by microvascular endothelium. Leuk Lymphoma 27:375–386PubMedGoogle Scholar
  26. 26.
    Yao L, Yokota T, Xia L, Kincade PW, McEver RP (2005) Bone marrow dysfunction in mice lacking the cytokine receptor gp130 in endothelial cells. Blood 106:4093–4101PubMedCentralPubMedCrossRefGoogle Scholar
  27. 27.
    Hooper AT, Butler JM, Nolan DJ, Kranz A, Iida K, Kobayashi M, Kopp HG, Shido K, Petit I, Yanger K, James D, Witte L, Zhu Z, Wu Y, Pytowski B, Rosenwaks Z, Mittal V, Sato TN, Rafii S (2009) Engraftment and reconstitution of hematopoiesis is dependent on VEGFR2-mediated regeneration of sinusoidal endothelial cells. Cell Stem Cell 4:263–274PubMedCentralPubMedCrossRefGoogle Scholar
  28. 28.
    Butler JM, Nolan DJ, Vertes EL, Varnum-Finney B, Kobayashi H, Hooper AT, Seandel M, Shido K, White IA, Kobayashi M, Witte L, May C, Shawber C, Kimura Y, Kitajewski J, Rosenwaks Z, Bernstein ID, Rafii S (2010) Endothelial cells are essential for the self-renewal and repopulation of Notch-dependent hematopoietic stem cells. Cell Stem Cell 6:251–264PubMedCentralPubMedCrossRefGoogle Scholar
  29. 29.
    Kobayashi H, Butler JM, O’Donnell R, Kobayashi M, Ding BS, Bonner B, Chiu VK, Nolan DJ, Shido K, Benjamin L, Rafii S (2010) Angiocrine factors from Akt-activated endothelial cells balance self-renewal and differentiation of haematopoietic stem cells. Nat Cell Biol 12:1046–1056PubMedCentralPubMedCrossRefGoogle Scholar
  30. 30.
    Poulos MG, Guo P, Kofler NM, Pinho S, Gutkin MC, Tikhonova A, Aifantis I, Frenette PS, Kitajewski J, Rafii S, Butler JM (2013) Endothelial Jagged-1 is necessary for homeostatic and regenerative hematopoiesis. Cell Rep 4:1022–1034PubMedCentralPubMedCrossRefGoogle Scholar
  31. 31.
    Salter AB, Meadows SK, Muramoto GG, Himburg H, Doan P, Daher P, Russell L, Chen B, Chao NJ, Chute JP (2009) Endothelial progenitor cell infusion induces hematopoietic stem cell reconstitution in vivo. Blood 113:2104–2107PubMedCentralPubMedCrossRefGoogle Scholar
  32. 32.
    Isern J, Garcia-Garcia A, Martin AM, Arranz L, Martin-Perez D, Torroja C, Sanchez-Cabo F, Mendez-Ferrer S (2014) The neural crest is a source of mesenchymal stem cells with specialized hematopoietic stem cell niche function. Elife 3:e03696PubMedCentralPubMedCrossRefGoogle Scholar
  33. 33.
    Mendez-Ferrer S, Michurina TV, Ferraro F, Mazloom AR, Macarthur BD, Lira SA, Scadden DT, Ma’ayan A, Enikolopov GN, Frenette PS (2010) Mesenchymal and haematopoietic stem cells form a unique bone marrow niche. Nature 466:829–834PubMedCentralPubMedCrossRefGoogle Scholar
  34. 34.
    Sugiyama T, Kohara H, Noda M, Nagasawa T (2006) Maintenance of the hematopoietic stem cell pool by CXCL12-CXCR4 chemokine signaling in bone marrow stromal cell niches. Immunity 25:977–988PubMedCrossRefGoogle Scholar
  35. 35.
    Omatsu Y, Sugiyama T, Kohara H, Kondoh G, Fujii N, Kohno K, Nagasawa T (2010) The essential functions of adipo-osteogenic progenitors as the hematopoietic stem and progenitor cell niche. Immunity 33:387–399PubMedCrossRefGoogle Scholar
  36. 36.
    Isern J, Mendez-Ferrer S (2011) Stem cell interactions in a bone marrow niche. Curr Osteoporos Rep 9:210–218PubMedCrossRefGoogle Scholar
  37. 37.
    Dexter TM, Allen TD, Lajtha LG (1977) Conditions controlling the proliferation of haemopoietic stem cells in vitro. J Cell Physiol 91:335–344PubMedCrossRefGoogle Scholar
  38. 38.
    Whitlock CA, Witte ON (1982) Long-term culture of B lymphocytes and their precursors from murine bone marrow. Proc Natl Acad Sci USA 79:3608–3612PubMedCentralPubMedCrossRefGoogle Scholar
  39. 39.
    Dorshkind K, Schouest L, Fletcher WH (1985) Morphologic analysis of long-term bone marrow cultures that support B-lymphopoiesis or myelopoiesis. Cell Tissue Res 239:375–382PubMedCrossRefGoogle Scholar
  40. 40.
    Jacobsen K, Osmond DG (1990) Microenvironmental organization and stromal cell associations of B lymphocyte precursor cells in mouse bone marrow. Eur J Immunol 20:2395–2404PubMedCrossRefGoogle Scholar
  41. 41.
    Nagasawa T, Kikutani H, Kishimoto T (1994) Molecular cloning and structure of a pre-B-cell growth-stimulating factor. Proc Natl Acad Sci USA 91:2305–2309PubMedCentralPubMedCrossRefGoogle Scholar
  42. 42.
    Egawa T, Kawabata K, Kawamoto H, Amada K, Okamoto R, Fujii N, Kishimoto T, Katsura Y, Nagasawa T (2001) The earliest stages of B cell development require a chemokine stromal cell-derived factor/pre-B cell growth-stimulating factor. Immunity 15:323–334PubMedCrossRefGoogle Scholar
  43. 43.
    Ma Q, Jones D, Springer TA (1999) The chemokine receptor CXCR4 is required for the retention of B lineage and granulocytic precursors within the bone marrow microenvironment. Immunity 10:463–471PubMedCrossRefGoogle Scholar
  44. 44.
    Hargreaves DC, Hyman PL, Lu TT, Ngo VN, Bidgol A, Suzuki G, Zou YR, Littman DR, Cyster JG (2001) A coordinated change in chemokine responsiveness guides plasma cell movements. J Exp Med 194:45–56PubMedCentralPubMedCrossRefGoogle Scholar
  45. 45.
    Ma Q, Jones D, Borghesani PR, Segal RA, Nagasawa T, Kishimoto T, Bronson RT, Springer TA (1998) Impaired B-lymphopoiesis, myelopoiesis, and derailed cerebellar neuron migration in CXCR4- and SDF-1-deficient mice. Proc Natl Acad Sci USA 95:9448–9453PubMedCentralPubMedCrossRefGoogle Scholar
  46. 46.
    Namen AE, Lupton S, Hjerrild K, Wignall J, Mochizuki DY, Schmierer A, Mosley B, March CJ, Urdal D, Gillis S (1988) Stimulation of B-cell progenitors by cloned murine interleukin-7. Nature 333:571–573PubMedCrossRefGoogle Scholar
  47. 47.
    Li YS, Hayakawa K, Hardy RR (1993) The regulated expression of B lineage associated genes during B cell differentiation in bone marrow and fetal liver. J Exp Med 178:951–960PubMedCrossRefGoogle Scholar
  48. 48.
    Dias S, Silva H Jr, Cumano A, Vieira P (2005) Interleukin-7 is necessary to maintain the B cell potential in common lymphoid progenitors. J Exp Med 201:971–979PubMedCentralPubMedCrossRefGoogle Scholar
  49. 49.
    Peschon JJ, Morrissey PJ, Grabstein KH, Ramsdell FJ, Maraskovsky E, Gliniak BC, Park LS, Ziegler SF, Williams DE, Ware CB, Meyer JD, Davison BL (1994) Early lymphocyte expansion is severely impaired in interleukin 7 receptor-deficient mice. J Exp Med 180:1955–1960PubMedCrossRefGoogle Scholar
  50. 50.
    von Freeden-Jeffry U, Vieira P, Lucian LA, McNeil T, Burdach SE, Murray R (1995) Lymphopenia in interleukin (IL)-7 gene-deleted mice identifies IL-7 as a nonredundant cytokine. J Exp Med 181:1519–1526CrossRefGoogle Scholar
  51. 51.
    Corfe SA, Paige CJ (2012) The many roles of IL-7 in B cell development; mediator of survival, proliferation and differentiation. Semin Immunol 24:198–208PubMedCrossRefGoogle Scholar
  52. 52.
    Tokoyoda K, Egawa T, Sugiyama T, Choi BI, Nagasawa T (2004) Cellular niches controlling B lymphocyte behavior within bone marrow during development. Immunity 20:707–718PubMedCrossRefGoogle Scholar
  53. 53.
    Marshall AJ, Fleming HE, Wu GE, Paige CJ (1998) Modulation of the IL-7 dose-response threshold during pro-B cell differentiation is dependent on pre-B cell receptor expression. J Immunol 161:6038–6045PubMedGoogle Scholar
  54. 54.
    Fleming HE, Paige CJ (2001) Pre-B cell receptor signaling mediates selective response to IL-7 at the pro-B to pre-B cell transition via an ERK/MAP kinase-dependent pathway. Immunity 15:521–531PubMedCrossRefGoogle Scholar
  55. 55.
    Mourcin F, Breton C, Tellier J, Narang P, Chasson L, Jorquera A, Coles M, Schiff C, Mancini SJ (2011) Galectin-1-expressing stromal cells constitute a specific niche for pre-BII cell development in mouse bone marrow. Blood 117:6552–6561PubMedCrossRefGoogle Scholar
  56. 56.
    Pelanda R, Torres RM (2006) Receptor editing for better or for worse. Curr Opin Immunol 18:184–190PubMedCrossRefGoogle Scholar
  57. 57.
    Sandel PC, Gendelman M, Kelsoe G, Monroe JG (2001) Definition of a novel cellular constituent of the bone marrow that regulates the response of immature B cells to B cell antigen receptor engagement. J Immunol 166:5935–5944PubMedCrossRefGoogle Scholar
  58. 58.
    Sandel PC, Monroe JG (1999) Negative selection of immature B cells by receptor editing or deletion is determined by site of antigen encounter. Immunity 10:289–299PubMedCrossRefGoogle Scholar
  59. 59.
    Hyafil F, Babinet C, Jacob F (1981) Cell–cell interactions in early embryogenesis: a molecular approach to the role of calcium. Cell 26:447–454PubMedCrossRefGoogle Scholar
  60. 60.
    Carmeliet P, Lampugnani MG, Moons L, Breviario F, Compernolle V, Bono F, Balconi G, Spagnuolo R, Oosthuyse B, Dewerchin M, Zanetti A, Angellilo A, Mattot V, Nuyens D, Lutgens E, Clotman F, de Ruiter MC, Gittenberger-de Groot A, Poelmann R, Lupu F, Herbert JM, Collen D, Dejana E (1999) Targeted deficiency or cytosolic truncation of the VE-cadherin gene in mice impairs VEGF-mediated endothelial survival and angiogenesis. Cell 98:147–157PubMedCrossRefGoogle Scholar
  61. 61.
    Giampietro C, Taddei A, Corada M, Sarra-Ferraris GM, Alcalay M, Cavallaro U, Orsenigo F, Lampugnani MG, Dejana E (2012) Overlapping and divergent signaling pathways of N-cadherin and VE-cadherin in endothelial cells. Blood 119:2159–2170PubMedCrossRefGoogle Scholar
  62. 62.
    Zarbock A, Ley K, McEver RP, Hidalgo A (2011) Leukocyte ligands for endothelial selectins: specialized glycoconjugates that mediate rolling and signaling under flow. Blood 118:6743–6751PubMedCentralPubMedCrossRefGoogle Scholar
  63. 63.
    McEver RP (2015) Selectins: initiators of leucocyte adhesion and signalling at the vascular wall. Cardiovasc Res 107:331–339PubMedCrossRefGoogle Scholar
  64. 64.
    van Buul JD, Kanters E, Hordijk PL (2007) Endothelial signaling by Ig-like cell adhesion molecules. Arterioscler Thromb Vasc Biol 27:1870–1876PubMedCrossRefGoogle Scholar
  65. 65.
    Furness SG, McNagny K (2006) Beyond mere markers: functions for CD34 family of sialomucins in hematopoiesis. Immunol Res 34:13–32PubMedCrossRefGoogle Scholar
  66. 66.
    Civin CI, Strauss LC, Brovall C, Fackler MJ, Schwartz JF, Shaper JH (1984) Antigenic analysis of hematopoiesis. III. A hematopoietic progenitor cell surface antigen defined by a monoclonal antibody raised against KG-1a cells. J Immunol 133:157–165PubMedGoogle Scholar
  67. 67.
    Watt SM, Chan JY (2000) CD164–a novel sialomucin on CD34+ cells. Leuk Lymphoma 37:1–25PubMedCrossRefGoogle Scholar
  68. 68.
    Hertweck MK, Erdfelder F, Kreuzer KA (2011) CD44 in hematological neoplasias. Ann Hematol 90:493–508PubMedCrossRefGoogle Scholar
  69. 69.
    Ghaffari S, Smadja-Joffe F, Oostendorp R, Levesque JP, Dougherty G, Eaves A, Eaves C (1999) CD44 isoforms in normal and leukemic hematopoiesis. Exp Hematol 27:978–993PubMedCrossRefGoogle Scholar
  70. 70.
    Lesley J, Hyman R, Schulte R (1985) Evidence that the Pgp-1 glycoprotein is expressed on thymus-homing progenitor cells of the thymus. Cell Immunol 91:397–403PubMedCrossRefGoogle Scholar
  71. 71.
    Humphries JD, Byron A, Humphries MJ (2006) Integrin ligands at a glance. J Cell Sci 119:3901–3903PubMedCentralPubMedCrossRefGoogle Scholar
  72. 72.
    Elices MJ, Osborn L, Takada Y, Crouse C, Luhowskyj S, Hemler ME, Lobb RR (1990) VCAM-1 on activated endothelium interacts with the leukocyte integrin VLA-4 at a site distinct from the VLA-4/fibronectin binding site. Cell 60:577–584PubMedCrossRefGoogle Scholar
  73. 73.
    Guan JL, Hynes RO (1990) Lymphoid cells recognize an alternatively spliced segment of fibronectin via the integrin receptor alpha 4 beta 1. Cell 60:53–61PubMedCrossRefGoogle Scholar
  74. 74.
    Bayless KJ, Meininger GA, Scholtz JM, Davis GE (1998) Osteopontin is a ligand for the alpha4beta1 integrin. J Cell Sci 111(Pt 9):1165–1174PubMedGoogle Scholar
  75. 75.
    Brittain JE, Han J, Ataga KI, Orringer EP, Parise LV (2004) Mechanism of CD47-induced alpha4beta1 integrin activation and adhesion in sickle reticulocytes. J Biol Chem 279:42393–42402PubMedCrossRefGoogle Scholar
  76. 76.
    Cunningham SA, Rodriguez JM, Arrate MP, Tran TM, Brock TA (2002) JAM2 interacts with alpha4beta1. Facilitation by JAM3. J Biol Chem 277:27589–27592PubMedCrossRefGoogle Scholar
  77. 77.
    Ludwig RJ, Hardt K, Hatting M, Bistrian R, Diehl S, Radeke HH, Podda M, Schon MP, Kaufmann R, Henschler R, Pfeilschifter JM, Santoso S, Boehncke WH (2009) Junctional adhesion molecule (JAM)-B supports lymphocyte rolling and adhesion through interaction with alpha4beta1 integrin. Immunology 128:196–205PubMedCentralPubMedCrossRefGoogle Scholar
  78. 78.
    Mould AP, Humphries MJ (2004) Regulation of integrin function through conformational complexity: not simply a knee-jerk reaction? Curr Opin Cell Biol 16:544–551PubMedCrossRefGoogle Scholar
  79. 79.
    Huveneers S, Danen EH (2009) Adhesion signaling—crosstalk between integrins, Src and Rho. J Cell Sci 122:1059–1069PubMedCrossRefGoogle Scholar
  80. 80.
    Kinashi T (2005) Intracellular signalling controlling integrin activation in lymphocytes. Nat Rev Immunol 5:546–559PubMedCrossRefGoogle Scholar
  81. 81.
    Wehrle-Haller B (2012) Structure and function of focal adhesions. Curr Opin Cell Biol 24:116–124PubMedCrossRefGoogle Scholar
  82. 82.
    Osmani N, Labouesse M (2015) Remodeling of keratin-coupled cell adhesion complexes. Curr Opin Cell Biol 32C:30–38CrossRefGoogle Scholar
  83. 83.
    Prosper F, Verfaillie CM (2001) Regulation of hematopoiesis through adhesion receptors. J Leukoc Biol 69:307–316PubMedGoogle Scholar
  84. 84.
    Katayama Y, Hidalgo A, Peired A, Frenette PS (2004) Integrin alpha4beta7 and its counterreceptor MAdCAM-1 contribute to hematopoietic progenitor recruitment into bone marrow following transplantation. Blood 104:2020–2026PubMedCrossRefGoogle Scholar
  85. 85.
    Wagers AJ, Allsopp RC, Weissman IL (2002) Changes in integrin expression are associated with altered homing properties of Lin(−/lo)Thy1.1(lo)Sca-1(+)c-kit(+) hematopoietic stem cells following mobilization by cyclophosphamide/granulocyte colony-stimulating factor. Exp Hematol 30:176–185PubMedCrossRefGoogle Scholar
  86. 86.
    Umemoto T, Yamato M, Ishihara J, Shiratsuchi Y, Utsumi M, Morita Y, Tsukui H, Terasawa M, Shibata T, Nishida K, Kobayashi Y, Petrich BG, Nakauchi H, Eto K, Okano T (2012) Integrin-alphavbeta3 regulates thrombopoietin-mediated maintenance of hematopoietic stem cells. Blood 119:83–94PubMedCentralPubMedCrossRefGoogle Scholar
  87. 87.
    Jeannet R, Cai Q, Liu H, Vu H, Kuo YH (2013) Alcam regulates long-term hematopoietic stem cell engraftment and self-renewal. Stem Cells 31:560–571PubMedCrossRefGoogle Scholar
  88. 88.
    Chitteti BR, Kobayashi M, Cheng Y, Zhang H, Poteat BA, Broxmeyer HE, Pelus LM, Hanenberg H, Zollman A, Kamocka MM, Carlesso N, Cardoso AA, Kacena MA, Srour EF (2014) CD166 regulates human and murine hematopoietic stem cells and the hematopoietic niche. Blood 124:519–529PubMedCentralPubMedCrossRefGoogle Scholar
  89. 89.
    Ooi AG, Karsunky H, Majeti R, Butz S, Vestweber D, Ishida T, Quertermous T, Weissman IL, Forsberg EC (2009) The adhesion molecule esam1 is a novel hematopoietic stem cell marker. Stem Cells 27:653–661PubMedCrossRefGoogle Scholar
  90. 90.
    Yokota T, Oritani K, Butz S, Kokame K, Kincade PW, Miyata T, Vestweber D, Kanakura Y (2009) The endothelial antigen ESAM marks primitive hematopoietic progenitors throughout life in mice. Blood 113:2914–2923PubMedCentralPubMedCrossRefGoogle Scholar
  91. 91.
    Sugano Y, Takeuchi M, Hirata A, Matsushita H, Kitamura T, Tanaka M, Miyajima A (2008) Junctional adhesion molecule-A, JAM-A, is a novel cell-surface marker for long-term repopulating hematopoietic stem cells. Blood 111:1167–1172PubMedCrossRefGoogle Scholar
  92. 92.
    Forsberg EC, Prohaska SS, Katzman S, Heffner GC, Stuart JM, Weissman IL (2005) Differential expression of novel potential regulators in hematopoietic stem cells. PLoS Genet 1:e28PubMedCentralPubMedCrossRefGoogle Scholar
  93. 93.
    Praetor A, McBride JM, Chiu H, Rangell L, Cabote L, Lee WP, Cupp J, Danilenko DM, Fong S (2009) Genetic deletion of JAM-C reveals a role in myeloid progenitor generation. Blood 113:1919–1928PubMedCentralPubMedCrossRefGoogle Scholar
  94. 94.
    Arcangeli ML, Frontera V, Bardin F, Obrados E, Adams S, Chabannon C, Schiff C, Mancini SJ, Adams RH, Aurrand-Lions M (2011) JAM-B regulates maintenance of hematopoietic stem cells in the bone marrow. Blood 118:4609–4619PubMedCrossRefGoogle Scholar
  95. 95.
    Mazo IB, Massberg S, von Andrian UH (2011) Hematopoietic stem and progenitor cell trafficking. Trends Immunol 32:493–503PubMedCentralPubMedCrossRefGoogle Scholar
  96. 96.
    Papayannopoulou T, Craddock C, Nakamoto B, Priestley GV, Wolf NS (1995) The VLA4/VCAM-1 adhesion pathway defines contrasting mechanisms of lodgement of transplanted murine hemopoietic progenitors between bone marrow and spleen. Proc Natl Acad Sci USA 92:9647–9651PubMedCentralPubMedCrossRefGoogle Scholar
  97. 97.
    Frenette PS, Subbarao S, Mazo IB, von Andrian UH, Wagner DD (1998) Endothelial selectins and vascular cell adhesion molecule-1 promote hematopoietic progenitor homing to bone marrow. Proc Natl Acad Sci USA 95:14423–14428PubMedCentralPubMedCrossRefGoogle Scholar
  98. 98.
    Mazo IB, Gutierrez-Ramos JC, Frenette PS, Hynes RO, Wagner DD, von Andrian UH (1998) Hematopoietic progenitor cell rolling in bone marrow microvessels: parallel contributions by endothelial selectins and vascular cell adhesion molecule 1. J Exp Med 188:465–474PubMedCentralPubMedCrossRefGoogle Scholar
  99. 99.
    Katayama Y, Hidalgo A, Furie BC, Vestweber D, Furie B, Frenette PS (2003) PSGL-1 participates in E-selectin-mediated progenitor homing to bone marrow: evidence for cooperation between E-selectin ligands and alpha4 integrin. Blood 102:2060–2067PubMedCrossRefGoogle Scholar
  100. 100.
    Hidalgo A, Weiss LA, Frenette PS (2002) Functional selectin ligands mediating human CD34(+) cell interactions with bone marrow endothelium are enhanced postnatally. J Clin Invest 110:559–569PubMedCentralPubMedCrossRefGoogle Scholar
  101. 101.
    Sackstein R, Merzaban JS, Cain DW, Dagia NM, Spencer JA, Lin CP, Wohlgemuth R (2008) Ex vivo glycan engineering of CD44 programs human multipotent mesenchymal stromal cell trafficking to bone. Nat Med 14:181–187PubMedCrossRefGoogle Scholar
  102. 102.
    Dimitroff CJ, Lee JY, Rafii S, Fuhlbrigge RC, Sackstein R (2001) CD44 is a major E-selectin ligand on human hematopoietic progenitor cells. J Cell Biol 153:1277–1286PubMedCentralPubMedCrossRefGoogle Scholar
  103. 103.
    Avigdor A, Goichberg P, Shivtiel S, Dar A, Peled A, Samira S, Kollet O, Hershkoviz R, Alon R, Hardan I, Ben-Hur H, Naor D, Nagler A, Lapidot T (2004) CD44 and hyaluronic acid cooperate with SDF-1 in the trafficking of human CD34+ stem/progenitor cells to bone marrow. Blood 103:2981–2989PubMedCrossRefGoogle Scholar
  104. 104.
    Papayannopoulou T, Priestley GV, Nakamoto B, Zafiropoulos V, Scott LM, Harlan JM (2001) Synergistic mobilization of hemopoietic progenitor cells using concurrent beta1 and beta2 integrin blockade or beta2-deficient mice. Blood 97:1282–1288PubMedCrossRefGoogle Scholar
  105. 105.
    Qian H, Tryggvason K, Jacobsen SE, Ekblom M (2006) Contribution of alpha6 integrins to hematopoietic stem and progenitor cell homing to bone marrow and collaboration with alpha4 integrins. Blood 107:3503–3510PubMedCrossRefGoogle Scholar
  106. 106.
    Bonig H, Priestley GV, Wohlfahrt M, Kiem HP, Papayannopoulou T (2009) Blockade of alpha6-integrin reveals diversity in homing patterns among human, baboon, and murine cells. Stem Cells Dev 18:839–844PubMedCentralPubMedCrossRefGoogle Scholar
  107. 107.
    Nagasawa T, Hirota S, Tachibana K, Takakura N, Nishikawa S, Kitamura Y, Yoshida N, Kikutani H, Kishimoto T (1996) Defects of B-cell lymphopoiesis and bone-marrow myelopoiesis in mice lacking the CXC chemokine PBSF/SDF-1. Nature 382:635–638PubMedCrossRefGoogle Scholar
  108. 108.
    Nagasawa T (2000) A chemokine, SDF-1/PBSF, and its receptor, CXC chemokine receptor 4, as mediators of hematopoiesis. Int J Hematol 72:408–411PubMedGoogle Scholar
  109. 109.
    Peled A, Petit I, Kollet O, Magid M, Ponomaryov T, Byk T, Nagler A, Ben-Hur H, Many A, Shultz L, Lider O, Alon R, Zipori D, Lapidot T (1999) Dependence of human stem cell engraftment and repopulation of NOD/SCID mice on CXCR4. Science 283:845–848PubMedCrossRefGoogle Scholar
  110. 110.
    Kahn J, Byk T, Jansson-Sjostrand L, Petit I, Shivtiel S, Nagler A, Hardan I, Deutsch V, Gazit Z, Gazit D, Karlsson S, Lapidot T (2004) Overexpression of CXCR4 on human CD34+ progenitors increases their proliferation, migration, and NOD/SCID repopulation. Blood 103:2942–2949PubMedCrossRefGoogle Scholar
  111. 111.
    Peled A, Kollet O, Ponomaryov T, Petit I, Franitza S, Grabovsky V, Slav MM, Nagler A, Lider O, Alon R, Zipori D, Lapidot T (2000) The chemokine SDF-1 activates the integrins LFA-1, VLA-4, and VLA-5 on immature human CD34(+) cells: role in transendothelial/stromal migration and engraftment of NOD/SCID mice. Blood 95:3289–3296PubMedGoogle Scholar
  112. 112.
    Foudi A, Jarrier P, Zhang Y, Wittner M, Geay JF, Lecluse Y, Nagasawa T, Vainchenker W, Louache F (2006) Reduced retention of radioprotective hematopoietic cells within the bone marrow microenvironment in CXCR4−/− chimeric mice. Blood 107:2243–2251PubMedCrossRefGoogle Scholar
  113. 113.
    Bonig H, Priestley GV, Nilsson LM, Jiang Y, Papayannopoulou T (2004) PTX-sensitive signals in bone marrow homing of fetal and adult hematopoietic progenitor cells. Blood 104:2299–2306PubMedCrossRefGoogle Scholar
  114. 114.
    Petit I, Goichberg P, Spiegel A, Peled A, Brodie C, Seger R, Nagler A, Alon R, Lapidot T (2005) Atypical PKC-zeta regulates SDF-1-mediated migration and development of human CD34+ progenitor cells. J Clin Invest 115:168–176PubMedCentralPubMedCrossRefGoogle Scholar
  115. 115.
    Sengupta A, Duran A, Ishikawa E, Florian MC, Dunn SK, Ficker AM, Leitges M, Geiger H, Diaz-Meco M, Moscat J, Cancelas JA (2011) Atypical protein kinase C (aPKCzeta and aPKClambda) is dispensable for mammalian hematopoietic stem cell activity and blood formation. Proc Natl Acad Sci USA 108:9957–9962PubMedCentralPubMedCrossRefGoogle Scholar
  116. 116.
    Fukuda S, Broxmeyer HE, Pelus LM (2005) Flt3 ligand and the Flt3 receptor regulate hematopoietic cell migration by modulating the SDF-1alpha(CXCL12)/CXCR4 axis. Blood 105:3117–3126PubMedCrossRefGoogle Scholar
  117. 117.
    Leung KT, Chan KY, Ng PC, Lau TK, Chiu WM, Tsang KS, Li CK, Kong CK, Li K (2011) The tetraspanin CD9 regulates migration, adhesion, and homing of human cord blood CD34+ hematopoietic stem and progenitor cells. Blood 117:1840–1850PubMedCrossRefGoogle Scholar
  118. 118.
    Imbert AM, Belaaloui G, Bardin F, Tonnelle C, Lopez M, Chabannon C (2006) CD99 expressed on human mobilized peripheral blood CD34+ cells is involved in transendothelial migration. Blood 108:2578–2586PubMedCrossRefGoogle Scholar
  119. 119.
    Ross EA, Freeman S, Zhao Y, Dhanjal TS, Ross EJ, Lax S, Ahmed Z, Hou TZ, Kalia N, Egginton S, Nash G, Watson SP, Frampton J, Buckley CD (2008) A novel role for PECAM-1 (CD31) in regulating haematopoietic progenitor cell compartmentalization between the peripheral blood and bone marrow. PLoS ONE 3:e2338PubMedCentralPubMedCrossRefGoogle Scholar
  120. 120.
    Yahata T, Ando K, Sato T, Miyatake H, Nakamura Y, Muguruma Y, Kato S, Hotta T (2003) A highly sensitive strategy for SCID-repopulating cell assay by direct injection of primitive human hematopoietic cells into NOD/SCID mice bone marrow. Blood 101:2905–2913PubMedCrossRefGoogle Scholar
  121. 121.
    Kiel MJ, Radice GL, Morrison SJ (2007) Lack of evidence that hematopoietic stem cells depend on N-cadherin-mediated adhesion to osteoblasts for their maintenance. Cell Stem Cell 1:204–217PubMedCrossRefGoogle Scholar
  122. 122.
    Haug JS, He XC, Grindley JC, Wunderlich JP, Gaudenz K, Ross JT, Paulson A, Wagner KP, Xie Y, Zhu R, Yin T, Perry JM, Hembree MJ, Redenbaugh EP, Radice GL, Seidel C, Li L (2008) N-cadherin expression level distinguishes reserved versus primed states of hematopoietic stem cells. Cell Stem Cell 2:367–379PubMedCrossRefGoogle Scholar
  123. 123.
    Jung Y, Wang J, Schneider A, Sun YX, Koh-Paige AJ, Osman NI, McCauley LK, Taichman RS (2006) Regulation of SDF-1 (CXCL12) production by osteoblasts; a possible mechanism for stem cell homing. Bone 38:497–508PubMedCrossRefGoogle Scholar
  124. 124.
    Driessen RL, Johnston HM, Nilsson SK (2003) Membrane-bound stem cell factor is a key regulator in the initial lodgment of stem cells within the endosteal marrow region. Exp Hematol 31:1284–1291PubMedCrossRefGoogle Scholar
  125. 125.
    Li WM, Huang WQ, Huang YH, Jiang DZ, Wang QR (2000) Positive and negative hematopoietic cytokines produced by bone marrow endothelial cells. Cytokine 12:1017–1023PubMedCrossRefGoogle Scholar
  126. 126.
    Itkin T, Kaufmann KB, Gur-Cohen S, Ludin A, Lapidot T (2013) Fibroblast growth factor signaling promotes physiological bone remodeling and stem cell self-renewal. Curr Opin Hematol 20:237–244PubMedGoogle Scholar
  127. 127.
    Winkler IG, Barbier V, Nowlan B, Jacobsen RN, Forristal CE, Patton JT, Magnani JL, Levesque JP (2012) Vascular niche E-selectin regulates hematopoietic stem cell dormancy, self renewal and chemoresistance. Nat Med 18:1651–1657PubMedCrossRefGoogle Scholar
  128. 128.
    Wilson A, Laurenti E, Oser G, van der Wath RC, Blanco-Bose W, Jaworski M, Offner S, Dunant CF, Eshkind L, Bockamp E, Lio P, Macdonald HR, Trumpp A (2008) Hematopoietic stem cells reversibly switch from dormancy to self-renewal during homeostasis and repair. Cell 135:1118–1129PubMedCrossRefGoogle Scholar
  129. 129.
    Kinashi T, Springer TA (1994) Steel factor and c-kit regulate cell–matrix adhesion. Blood 83:1033–1038PubMedGoogle Scholar
  130. 130.
    Kodama H, Nose M, Niida S, Nishikawa S (1994) Involvement of the c-kit receptor in the adhesion of hematopoietic stem cells to stromal cells. Exp Hematol 22:979–984PubMedGoogle Scholar
  131. 131.
    Kovach NL, Lin N, Yednock T, Harlan JM, Broudy VC (1995) Stem cell factor modulates avidity of alpha 4 beta 1 and alpha 5 beta 1 integrins expressed on hematopoietic cell lines. Blood 85:159–167PubMedGoogle Scholar
  132. 132.
    Qian H, Buza-Vidas N, Hyland CD, Jensen CT, Antonchuk J, Mansson R, Thoren LA, Ekblom M, Alexander WS, Jacobsen SE (2007) Critical role of thrombopoietin in maintaining adult quiescent hematopoietic stem cells. Cell Stem Cell 1:671–684PubMedCrossRefGoogle Scholar
  133. 133.
    Scott LM, Priestley GV, Papayannopoulou T (2003) Deletion of alpha4 integrins from adult hematopoietic cells reveals roles in homeostasis, regeneration, and homing. Mol Cell Biol 23:9349–9360PubMedCentralPubMedCrossRefGoogle Scholar
  134. 134.
    Hidalgo A, Peired AJ, Weiss LA, Katayama Y, Frenette PS (2004) The integrin alphaMbeta2 anchors hematopoietic progenitors in the bone marrow during enforced mobilization. Blood 104:993–1001PubMedCrossRefGoogle Scholar
  135. 135.
    Schreiber TD, Steinl C, Essl M, Abele H, Geiger K, Muller CA, Aicher WK, Klein G (2009) The integrin alpha9beta1 on hematopoietic stem and progenitor cells: involvement in cell adhesion, proliferation and differentiation. Haematologica 94:1493–1501PubMedCentralPubMedCrossRefGoogle Scholar
  136. 136.
    Levesque JP, Leavesley DI, Niutta S, Vadas M, Simmons PJ (1995) Cytokines increase human hemopoietic cell adhesiveness by activation of very late antigen (VLA)-4 and VLA-5 integrins. J Exp Med 181:1805–1815PubMedCrossRefGoogle Scholar
  137. 137.
    Nie Y, Han YC, Zou YR (2008) CXCR4 is required for the quiescence of primitive hematopoietic cells. J Exp Med 205:777–783PubMedCentralPubMedCrossRefGoogle Scholar
  138. 138.
    Cancelas JA, Lee AW, Prabhakar R, Stringer KF, Zheng Y, Williams DA (2005) Rac GTPases differentially integrate signals regulating hematopoietic stem cell localization. Nat Med 11:886–891PubMedCrossRefGoogle Scholar
  139. 139.
    Zoughlami Y, Voermans C, Brussen K, van Dort KA, Kootstra NA, Maussang D, Smit MJ, Hordijk PL, van Hennik PB (2012) Regulation of CXCR4 conformation by the small GTPase Rac1: implications for HIV infection. Blood 119:2024–2032PubMedCrossRefGoogle Scholar
  140. 140.
    Arcangeli ML, Bardin F, Frontera V, Bidaut G, Obrados E, Adams RH, Chabannon C, Aurrand-Lions M (2014) Function of Jam-B/Jam-C interaction in homing and mobilization of human and mouse hematopoietic stem and progenitor cells. Stem Cells 32:1043–1054PubMedCrossRefGoogle Scholar
  141. 141.
    Sudo T, Yokota T, Oritani K, Satoh Y, Sugiyama T, Ishida T, Shibayama H, Ezoe S, Fujita N, Tanaka H, Maeda T, Nagasawa T, Kanakura Y (2012) The endothelial antigen ESAM monitors hematopoietic stem cell status between quiescence and self-renewal. J Immunol 189:200–210PubMedCrossRefGoogle Scholar
  142. 142.
    Busch K, Klapproth K, Barile M, Flossdorf M, Holland-Letz T, Schlenner SM, Reth M, Hofer T, Rodewald HR (2015) Fundamental properties of unperturbed haematopoiesis from stem cells in vivo. Nature 518:542–546PubMedCrossRefGoogle Scholar
  143. 143.
    Mendez-Ferrer S, Lucas D, Battista M, Frenette PS (2008) Haematopoietic stem cell release is regulated by circadian oscillations. Nature 452:442–447PubMedCrossRefGoogle Scholar
  144. 144.
    Scheiermann C, Kunisaki Y, Lucas D, Chow A, Jang JE, Zhang D, Hashimoto D, Merad M, Frenette PS (2012) Adrenergic nerves govern circadian leukocyte recruitment to tissues. Immunity 37:290–301PubMedCentralPubMedCrossRefGoogle Scholar
  145. 145.
    Massberg S, Schaerli P, Knezevic-Maramica I, Kollnberger M, Tubo N, Moseman EA, Huff IV, Junt T, Wagers AJ, Mazo IB, von Andrian UH (2007) Immunosurveillance by hematopoietic progenitor cells trafficking through blood, lymph, and peripheral tissues. Cell 131:994–1008PubMedCentralPubMedCrossRefGoogle Scholar
  146. 146.
    Wagers AJ, Sherwood RI, Christensen JL, Weissman IL (2002) Little evidence for developmental plasticity of adult hematopoietic stem cells. Science 297:2256–2259PubMedCrossRefGoogle Scholar
  147. 147.
    Petit I, Szyper-Kravitz M, Nagler A, Lahav M, Peled A, Habler L, Ponomaryov T, Taichman RS, Arenzana-Seisdedos F, Fujii N, Sandbank J, Zipori D, Lapidot T (2002) G-CSF induces stem cell mobilization by decreasing bone marrow SDF-1 and up-regulating CXCR4. Nat Immunol 3:687–694PubMedCrossRefGoogle Scholar
  148. 148.
    Levesque JP, Helwani FM, Winkler IG (2010) The endosteal ‘osteoblastic’ niche and its role in hematopoietic stem cell homing and mobilization. Leukemia 24:1979–1992PubMedCrossRefGoogle Scholar
  149. 149.
    Liu F, Poursine-Laurent J, Link DC (2000) Expression of the G-CSF receptor on hematopoietic progenitor cells is not required for their mobilization by G-CSF. Blood 95:3025–3031PubMedGoogle Scholar
  150. 150.
    Levesque JP, Hendy J, Takamatsu Y, Simmons PJ, Bendall LJ (2003) Disruption of the CXCR4/CXCL12 chemotactic interaction during hematopoietic stem cell mobilization induced by GCSF or cyclophosphamide. J Clin Invest 111:187–196PubMedCentralPubMedCrossRefGoogle Scholar
  151. 151.
    Levesque JP, Takamatsu Y, Nilsson SK, Haylock DN, Simmons PJ (2001) Vascular cell adhesion molecule-1 (CD106) is cleaved by neutrophil proteases in the bone marrow following hematopoietic progenitor cell mobilization by granulocyte colony-stimulating factor. Blood 98:1289–1297PubMedCrossRefGoogle Scholar
  152. 152.
    Heissig B, Hattori K, Dias S, Friedrich M, Ferris B, Hackett NR, Crystal RG, Besmer P, Lyden D, Moore MA, Werb Z, Rafii S (2002) Recruitment of stem and progenitor cells from the bone marrow niche requires MMP-9 mediated release of kit-ligand. Cell 109:625–637PubMedCentralPubMedCrossRefGoogle Scholar
  153. 153.
    Levesque JP, Liu F, Simmons PJ, Betsuyaku T, Senior RM, Pham C, Link DC (2004) Characterization of hematopoietic progenitor mobilization in protease-deficient mice. Blood 104:65–72PubMedCrossRefGoogle Scholar
  154. 154.
    Christopherson KW 2nd, Cooper S, Broxmeyer HE (2003) Cell surface peptidase CD26/DPPIV mediates G-CSF mobilization of mouse progenitor cells. Blood 101:4680–4686PubMedCrossRefGoogle Scholar
  155. 155.
    Winkler IG, Hendy J, Coughlin P, Horvath A, Levesque JP (2005) Serine protease inhibitors serpina1 and serpina3 are down-regulated in bone marrow during hematopoietic progenitor mobilization. J Exp Med 201:1077–1088PubMedCentralPubMedCrossRefGoogle Scholar
  156. 156.
    Takamatsu Y, Simmons PJ, Moore RJ, Morris HA, To LB, Levesque JP (1998) Osteoclast-mediated bone resorption is stimulated during short-term administration of granulocyte colony-stimulating factor but is not responsible for hematopoietic progenitor cell mobilization. Blood 92:3465–3473PubMedGoogle Scholar
  157. 157.
    Miyamoto K, Yoshida S, Kawasumi M, Hashimoto K, Kimura T, Sato Y, Kobayashi T, Miyauchi Y, Hoshi H, Iwasaki R, Miyamoto H, Hao W, Morioka H, Chiba K, Yasuda H, Penninger JM, Toyama Y, Suda T, Miyamoto T (2011) Osteoclasts are dispensable for hematopoietic stem cell maintenance and mobilization. J Exp Med 208:2175–2181PubMedCentralPubMedCrossRefGoogle Scholar
  158. 158.
    Broxmeyer HE, Orschell CM, Clapp DW, Hangoc G, Cooper S, Plett PA, Liles WC, Li X, Graham-Evans B, Campbell TB, Calandra G, Bridger G, Dale DC, Srour EF (2005) Rapid mobilization of murine and human hematopoietic stem and progenitor cells with AMD3100, a CXCR4 antagonist. J Exp Med 201:1307–1318PubMedCentralPubMedCrossRefGoogle Scholar
  159. 159.
    Bonig H, Wundes A, Chang KH, Lucas S, Papayannopoulou T (2008) Increased numbers of circulating hematopoietic stem/progenitor cells are chronically maintained in patients treated with the CD49d blocking antibody natalizumab. Blood 111:3439–3441PubMedCentralPubMedCrossRefGoogle Scholar
  160. 160.
    Vermeulen M, Le Pesteur F, Gagnerault MC, Mary JY, Sainteny F, Lepault F (1998) Role of adhesion molecules in the homing and mobilization of murine hematopoietic stem and progenitor cells. Blood 92:894–900PubMedGoogle Scholar
  161. 161.
    Lee S, Im SA, Yoo ES, Nam EM, Lee MA, Ahn JY, Huh JW, Kim DY, Lee SN, Kim MJ, Lee SJ, Chung WS, Seong CM (2000) Mobilization kinetics of CD34(+) cells in association with modulation of CD44 and CD31 expression during continuous intravenous administration of G-CSF in normal donors. Stem Cells 18:281–286PubMedCrossRefGoogle Scholar
  162. 162.
    Tesio M, Golan K, Corso S, Giordano S, Schajnovitz A, Vagima Y, Shivtiel S, Kalinkovich A, Caione L, Gammaitoni L, Laurenti E, Buss EC, Shezen E, Itkin T, Kollet O, Petit I, Trumpp A, Christensen J, Aglietta M, Piacibello W, Lapidot T (2011) Enhanced c-Met activity promotes G-CSF-induced mobilization of hematopoietic progenitor cells via ROS signaling. Blood 117:419–428PubMedCrossRefGoogle Scholar
  163. 163.
    Mayack SR, Wagers AJ (2008) Osteolineage niche cells initiate hematopoietic stem cell mobilization. Blood 112:519–531PubMedCentralPubMedCrossRefGoogle Scholar
  164. 164.
    Winkler IG, Sims NA, Pettit AR, Barbier V, Nowlan B, Helwani F, Poulton IJ, van Rooijen N, Alexander KA, Raggatt LJ, Levesque JP (2010) Bone marrow macrophages maintain hematopoietic stem cell (HSC) niches and their depletion mobilizes HSCs. Blood 116:4815–4828PubMedCrossRefGoogle Scholar
  165. 165.
    Greenbaum AM, Link DC (2011) Mechanisms of G-CSF-mediated hematopoietic stem and progenitor mobilization. Leukemia 25:211–217PubMedCrossRefGoogle Scholar
  166. 166.
    Miyake K, Weissman IL, Greenberger JS, Kincade PW (1991) Evidence for a role of the integrin VLA-4 in lympho-hemopoiesis. J Exp Med 173:599–607PubMedCrossRefGoogle Scholar
  167. 167.
    Dittel BN, LeBien TW (1995) Reduced expression of vascular cell adhesion molecule-1 on bone marrow stromal cells isolated from marrow transplant recipients correlates with a reduced capacity to support human B lymphopoiesis in vitro. Blood 86:2833–2841PubMedGoogle Scholar
  168. 168.
    Arroyo AG, Yang JT, Rayburn H, Hynes RO (1996) Differential requirements for alpha4 integrins during fetal and adult hematopoiesis. Cell 85:997–1008PubMedCrossRefGoogle Scholar
  169. 169.
    Glodek AM, Honczarenko M, Le Y, Campbell JJ, Silberstein LE (2003) Sustained activation of cell adhesion is a differentially regulated process in B lymphopoiesis. J Exp Med 197:461–473PubMedCentralPubMedCrossRefGoogle Scholar
  170. 170.
    Park SY, Wolfram P, Canty K, Harley B, Nombela-Arrieta C, Pivarnik G, Manis J, Beggs HE, Silberstein LE (2013) Focal adhesion kinase regulates the localization and retention of pro-B cells in bone marrow microenvironments. J Immunol 190:1094–1102PubMedCentralPubMedCrossRefGoogle Scholar
  171. 171.
    Guo B, Kato RM, Garcia-Lloret M, Wahl MI, Rawlings DJ (2000) Engagement of the human pre-B cell receptor generates a lipid raft-dependent calcium signaling complex. Immunity 13:243–253PubMedCrossRefGoogle Scholar
  172. 172.
    Ohnishi K, Melchers F (2003) The nonimmunoglobulin portion of lambda5 mediates cell-autonomous pre-B cell receptor signaling. Nat Immunol 4:849–856PubMedCrossRefGoogle Scholar
  173. 173.
    Ubelhart R, Bach MP, Eschbach C, Wossning T, Reth M, Jumaa H (2010) N-linked glycosylation selectively regulates autonomous precursor BCR function. Nat Immunol 11:759–765PubMedCrossRefGoogle Scholar
  174. 174.
    Bradl H, Wittmann J, Milius D, Vettermann C, Jack HM (2003) Interaction of murine precursor B cell receptor with stroma cells is controlled by the unique tail of lambda 5 and stroma cell-associated heparan sulfate. J Immunol 171:2338–2348PubMedCrossRefGoogle Scholar
  175. 175.
    Gauthier L, Rossi B, Roux F, Termine E, Schiff C (2002) Galectin-1 is a stromal cell ligand of the pre-B cell receptor (BCR) implicated in synapse formation between pre-B and stromal cells and in pre-BCR triggering. Proc Natl Acad Sci USA 99:13014–13019PubMedCentralPubMedCrossRefGoogle Scholar
  176. 176.
    Elantak L, Espeli M, Boned A, Bornet O, Bonzi J, Gauthier L, Feracci M, Roche P, Guerlesquin F, Schiff C (2012) Structural basis for galectin-1-dependent pre-B cell receptor (pre-BCR) activation. J Biol Chem 287:44703–44713PubMedCentralPubMedCrossRefGoogle Scholar
  177. 177.
    Espeli M, Mancini SJ, Breton C, Poirier F, Schiff C (2009) Impaired B-cell development at the pre-BII-cell stage in galectin-1-deficient mice due to inefficient pre-BII/stromal cell interactions. Blood 113:5878–5886PubMedCrossRefGoogle Scholar
  178. 178.
    Rossi B, Espeli M, Schiff C, Gauthier L (2006) Clustering of pre-B cell integrins induces galectin-1-dependent pre-B cell receptor relocalization and activation. J Immunol 177:796–803PubMedCrossRefGoogle Scholar
  179. 179.
    Li W, Ishihara K, Yokota T, Nakagawa T, Koyama N, Jin J, Mizuno-Horikawa Y, Wang X, Miyoshi E, Taniguchi N, Kondo A (2008) Reduced alpha4beta1 integrin/VCAM-1 interactions lead to impaired pre-B cell repopulation in alpha 1,6-fucosyltransferase deficient mice. Glycobiology 18:114–124PubMedCrossRefGoogle Scholar
  180. 180.
    Koni PA, Joshi SK, Temann UA, Olson D, Burkly L, Flavell RA (2001) Conditional vascular cell adhesion molecule 1 deletion in mice: impaired lymphocyte migration to bone marrow. J Exp Med 193:741–754PubMedCentralPubMedCrossRefGoogle Scholar
  181. 181.
    Leuker CE, Labow M, Muller W, Wagner N (2001) Neonatally induced inactivation of the vascular cell adhesion molecule 1 gene impairs B cell localization and T cell-dependent humoral immune response. J Exp Med 193:755–768PubMedCentralPubMedCrossRefGoogle Scholar
  182. 182.
    Pereira JP, An J, Xu Y, Huang Y, Cyster JG (2009) Cannabinoid receptor 2 mediates the retention of immature B cells in bone marrow sinusoids. Nat Immunol 10:403–411PubMedCentralPubMedCrossRefGoogle Scholar
  183. 183.
    Beck TC, Gomes AC, Cyster JG, Pereira JP (2014) CXCR4 and a cell-extrinsic mechanism control immature B lymphocyte egress from bone marrow. J Exp Med 211:2567–2581PubMedCentralPubMedCrossRefGoogle Scholar
  184. 184.
    Allende ML, Tuymetova G, Lee BG, Bonifacino E, Wu YP, Proia RL (2010) S1P1 receptor directs the release of immature B cells from bone marrow into blood. J Exp Med 207:1113–1124PubMedCentralPubMedCrossRefGoogle Scholar

Copyright information

© Springer Basel 2015

Authors and Affiliations

  • Maria De Grandis
    • 1
  • Anne-Catherine Lhoumeau
    • 1
  • Stéphane J. C. Mancini
    • 1
  • Michel Aurrand-Lions
    • 1
  1. 1.Centre de Recherche en Cancérologie de Marseille, Institut Paoli-Calmettes, Inserm U1068, CNRS UMR7258Aix-Marseille Université UM105MarseilleFrance

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