Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.
ADVANCED SEARCH
Log in
Top
Calcified Tissue International
Published in: Calcified Tissue International 3/2013

01-09-2013 | Original Research

Interactions Between B Lymphocytes and the Osteoblast Lineage in Bone Marrow

Authors: Cristina Panaroni, Joy Y. Wu

Published in: Calcified Tissue International | Issue 3/2013

Login to get access

Abstract

The regulatory effects of the immune system on the skeleton during homeostasis and activation have been appreciated for years. In the past decade it has become evident that bone tissue can also regulate immune cell development. In the bone marrow, the differentiation of hematopoietic progenitors requires specific microenvironments, called “niches,” provided by various subsets of stromal cells, many of which are of mesenchymal origin. Among these stromal cell populations, cells of the osteoblast lineage serve a supportive function in the maintenance of normal hematopoiesis, and B lymphopoiesis in particular. Within the osteoblast lineage, distinct differentiation stages exert differential regulatory effects on hematopoietic development. In this review we will highlight the critical role of osteoblast progenitors in the perivascular B lymphocyte niche.
Literature
1.
2.
Tokoyoda K et al (2004) Cellular niches controlling B lymphocyte behavior within bone marrow during development. Immunity 20(6):707–718PubMedCrossRef
3.
Nagasawa T (2006) Microenvironmental niches in the bone marrow required for B-cell development. Nat Rev Immunol 6(2):107–116PubMedCrossRef
4.
Otero DC, Rickert RC (2003) CD19 function in early and late B cell development. II. CD19 facilitates the pro-B/pre-B transition. J Immunol 171(11):5921–5930PubMed
5.
Hardy RR et al (1991) Resolution and characterization of pro-B and pre-pro-B cell stages in normal mouse bone marrow. J Exp Med 173(5):1213–1225PubMedCrossRef
6.
Osmond DG, Rolink A, Melchers F (1998) Murine B lymphopoiesis: towards a unified model. Immunol Today 19(2):65–68PubMedCrossRef
7.
Li YS et al (1996) Identification of the earliest B lineage stage in mouse bone marrow. Immunity 5(6):527–535PubMedCrossRef
8.
Ogawa M, ten Boekel E, Melchers F (2000) Identification of CD19–B220+c-Kit+Flt3/Flk-2+ cells as early B lymphoid precursors before pre-B-I cells in juvenile mouse bone marrow. Int Immunol 12(3):313–324PubMedCrossRef
9.
Zou YR et al (1998) Function of the chemokine receptor CXCR4 in haematopoiesis and in cerebellar development. Nature 393(6685):595–599PubMedCrossRef
10.
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(6):2305–2309PubMedCrossRef
11.
Peled A et al (1999) Dependence of human stem cell engraftment and repopulation of NOD/SCID mice on CXCR4. Science 283(5403):845–848PubMedCrossRef
12.
Tachibana K et al (1998) The chemokine receptor CXCR4 is essential for vascularization of the gastrointestinal tract. Nature 393(6685):591–594PubMedCrossRef
13.
Nagasawa T et al (1996) Defects of B-cell lymphopoiesis and bone-marrow myelopoiesis in mice lacking the CXC chemokine PBSF/SDF-1. Nature 382(6592):635–638PubMedCrossRef
14.
Lee G et al (1988) Recombinant interleukin-7 supports the growth of normal B lymphocyte precursors. Curr Top Microbiol Immunol 141:16–18PubMedCrossRef
15.
Miller JP et al (2002) The earliest step in B lineage differentiation from common lymphoid progenitors is critically dependent upon interleukin 7. J Exp Med 196(5):705–711PubMedCrossRef
16.
von Freeden-Jeffry U et al (1995) Lymphopenia in interleukin (IL)-7 gene-deleted mice identifies IL-7 as a nonredundant cytokine. J Exp Med 181(4):1519–1526CrossRef
17.
Peschon JJ et al (1994) Early lymphocyte expansion is severely impaired in interleukin 7 receptor-deficient mice. J Exp Med 180(5):1955–1960PubMedCrossRef
18.
Sugiyama T et al (2006) Maintenance of the hematopoietic stem cell pool by CXCL12-CXCR4 chemokine signaling in bone marrow stromal cell niches. Immunity 25(6):977–988PubMedCrossRef
19.
Mourcin F et al (2011) Galectin-1-expressing stromal cells constitute a specific niche for pre-BII cell development in mouse bone marrow. Blood 117(24):6552–6561PubMedCrossRef
20.
Gauthier L et al (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(20):13014–13019PubMedCrossRef
21.
Espeli M et al (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(23):5878–5886PubMedCrossRef
22.
Sapoznikov A et al (2008) Perivascular clusters of dendritic cells provide critical survival signals to B cells in bone marrow niches. Nat Immunol 9(4):388–395PubMedCrossRef
23.
Link D, Calvi L. (submitted). Cellular complexity of the bone marrow hematopoietic stem cell niche. Calcif Tissue Int
24.
Taichman RS, Emerson SG (1994) Human osteoblasts support hematopoiesis through the production of granulocyte colony-stimulating factor. J Exp Med 179(5):1677–1682PubMedCrossRef
25.
Avecilla ST et al (2004) Chemokine-mediated interaction of hematopoietic progenitors with the bone marrow vascular niche is required for thrombopoiesis. Nat Med 10(1):64–71PubMedCrossRef
26.
Naveiras O et al (2009) Bone-marrow adipocytes as negative regulators of the haematopoietic microenvironment. Nature 460(7252):259–263PubMedCrossRef
27.
Omatsu Y et al (2010) The essential functions of adipo-osteogenic progenitors as the hematopoietic stem and progenitor cell niche. Immunity 33(3):387–399PubMedCrossRef
28.
Kiel MJ et al (2005) SLAM family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells. Cell 121(7):1109–1121PubMedCrossRef
29.
Ding L et al (2012) Endothelial and perivascular cells maintain haematopoietic stem cells. Nature 481(7382):457–462PubMedCrossRef
30.
Katayama Y et al (2006) Signals from the sympathetic nervous system regulate hematopoietic stem cell egress from bone marrow. Cell 124(2):407–421PubMedCrossRef
31.
Mendez-Ferrer S et al (2008) Haematopoietic stem cell release is regulated by circadian oscillations. Nature 452(7186):442–447PubMedCrossRef
32.
Yamazaki S et al (2011) Nonmyelinating Schwann cells maintain hematopoietic stem cell hibernation in the bone marrow niche. Cell 147(5):1146–1158PubMedCrossRef
33.
Winkler IG et al (2010) Bone marrow macrophages maintain hematopoietic stem cell (HSC) niches and their depletion mobilizes HSCs. Blood 116(23):4815–4828PubMedCrossRef
34.
Christopher MJ et al (2011) Expression of the G-CSF receptor in monocytic cells is sufficient to mediate hematopoietic progenitor mobilization by G-CSF in mice. J Exp Med 208(2):251–260PubMedCrossRef
35.
Chow A et al (2011) Bone marrow CD169+ macrophages promote the retention of hematopoietic stem and progenitor cells in the mesenchymal stem cell niche. J Exp Med 208(2):261–271PubMedCrossRef
36.
Porter RL, Calvi LM (2008) Communications between bone cells and hematopoietic stem cells. Arch Biochem Biophys 473(2):193–200PubMedCrossRef
37.
Wu JY, Scadden DT, Kronenberg HM (2009) Role of the osteoblast lineage in the bone marrow hematopoietic niches. J Bone Miner Res 24(5):759–764PubMedCrossRef
38.
Komori T et al (1997) Targeted disruption of Cbfa1 results in a complete lack of bone formation owing to maturational arrest of osteoblasts. Cell 89(5):755–764PubMedCrossRef
39.
Otto F et al (1997) Cbfa1, a candidate gene for cleidocranial dysplasia syndrome, is essential for osteoblast differentiation and bone development. Cell 89(5):765–771PubMedCrossRef
40.
Nakashima K et al (2002) The novel zinc finger-containing transcription factor osterix is required for osteoblast differentiation and bone formation. Cell 108(1):17–29PubMedCrossRef
41.
Zhou X et al (2010) Multiple functions of Osterix are required for bone growth and homeostasis in postnatal mice. Proc Natl Acad Sci USA 107(29):12919–12924PubMedCrossRef
42.
Deguchi K et al (1999) Excessive extramedullary hematopoiesis in Cbfa1-deficient mice with a congenital lack of bone marrow. Biochem Biophys Res Commun 255(2):352–359PubMedCrossRef
43.
Visnjic D et al (2004) Hematopoiesis is severely altered in mice with an induced osteoblast deficiency. Blood 103(9):3258–3264PubMedCrossRef
44.
Zhu J et al (2007) Osteoblasts support B-lymphocyte commitment and differentiation from hematopoietic stem cells. Blood 109(9):3706–3712PubMedCrossRef
45.
Ducy P et al (1997) Osf2/Cbfa1: a transcriptional activator of osteoblast differentiation. Cell 89(5):747–754PubMedCrossRef
46.
Aubin JE (2001) Regulation of osteoblast formation and function. Rev Endocr Metab Disord 2(1):81–94PubMedCrossRef
47.
Ducy P et al (1996) Increased bone formation in osteocalcin-deficient mice. Nature 382(6590):448–452PubMedCrossRef
48.
Cheng YH et al (2011) Impact of maturational status on the ability of osteoblasts to enhance the hematopoietic function of stem and progenitor cells. J Bone Miner Res 26(5):1111–1121PubMedCrossRef
49.
Chitteti BR et al (2013) Hierarchical organization of osteoblasts reveals the significant role of CD166 in hematopoietic stem cell maintenance and function. Bone 54(1):58–67PubMedCrossRef
50.
Chan CK et al (2009) Endochondral ossification is required for haematopoietic stem-cell niche formation. Nature 457(7228):490–494PubMedCrossRef
51.
Manolagas SC (2000) Birth and death of bone cells: basic regulatory mechanisms and implications for the pathogenesis and treatment of osteoporosis. Endocr Rev 21(2):115–137PubMedCrossRef
52.
Crisan M et al (2008) A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell 3(3):301–313PubMedCrossRef
53.
Armulik A, Genove G, Betsholtz C (2011) Pericytes: developmental, physiological, and pathological perspectives, problems, and promises. Dev Cell 21(2):193–215PubMedCrossRef
54.
Mendez-Ferrer S et al (2010) Mesenchymal and haematopoietic stem cells form a unique bone marrow niche. Nature 466(7308):829–834PubMedCrossRef
55.
Morikawa S et al (2009) Prospective identification, isolation, and systemic transplantation of multipotent mesenchymal stem cells in murine bone marrow. J Exp Med 206(11):2483–2496PubMedCrossRef
56.
Ding L, Morrison SJ (2013) Haematopoietic stem cells and early lymphoid progenitors occupy distinct bone marrow niches. Nature 495(7440):231–235PubMedCrossRef
57.
Greenbaum A et al (2013) CXCL12 in early mesenchymal progenitors is required for haematopoietic stem-cell maintenance. Nature 495(7440):227–230PubMedCrossRef
58.
Maes C et al (2010) Osteoblast precursors, but not mature osteoblasts, move into developing and fractured bones along with invading blood vessels. Dev Cell 19(2):329–344PubMedCrossRef
59.
Sacchetti B et al (2007) Self-renewing osteoprogenitors in bone marrow sinusoids can organize a hematopoietic microenvironment. Cell 131(2):324–336PubMedCrossRef
60.
Calvi LM et al (2003) Osteoblastic cells regulate the haematopoietic stem cell niche. Nature 425(6960):841–846PubMedCrossRef
61.
Jung Y et al (2006) Regulation of SDF-1 (CXCL12) production by osteoblasts; a possible mechanism for stem cell homing. Bone 38(4):497–508PubMedCrossRef
62.
Song L et al (2012) Loss of Wnt/beta-catenin signaling causes cell fate shift of preosteoblasts from osteoblasts to adipocytes. J Bone Miner Res 27(11):2344–2358PubMedCrossRef
63.
Corselli M et al (2013) Perivascular support of human hematopoietic stem/progenitor cells. Blood 121(15):2891–2901PubMedCrossRef
64.
Aguila HL et al (2012) Osteoblast-specific overexpression of human interleukin-7 rescues the bone mass phenotype of interleukin-7-deficient female mice. J Bone Miner Res 27(5):1030–1042PubMedCrossRef
65.
Juppner H et al (1991) A G protein-linked receptor for parathyroid hormone and parathyroid hormone-related peptide. Science 254(5034):1024–1026PubMedCrossRef
66.
Wu JY et al (2008) Osteoblastic regulation of B lymphopoiesis is mediated by Gsα-dependent signaling pathways. Proc Natl Acad Sci USA 105(44):16976–16981PubMedCrossRef
67.
Wu JY et al (2011) Gsalpha enhances commitment of mesenchymal progenitors to the osteoblast lineage but restrains osteoblast differentiation in mice. J Clin Invest 121(9):3492–3504PubMedCrossRef
68.
Fulzele K et al (2013) Myelopoiesis is regulated by osteocytes through Gsα-dependent signaling. Blood 121(6):930–939PubMedCrossRef
69.
Link A et al (2007) Fibroblastic reticular cells in lymph nodes regulate the homeostasis of naive T cells. Nat Immunol 8(11):1255–1265PubMedCrossRef
70.
Nagasawa T, Omatsu Y, Sugiyama T (2011) Control of hematopoietic stem cells by the bone marrow stromal niche: the role of reticular cells. Trends Immunol 32(7):315–320PubMedCrossRef
71.
Arroyo AG et al (1996) Differential requirements for alpha4 integrins during fetal and adult hematopoiesis. Cell 85(7):997–1008PubMedCrossRef
72.
Franzoso G et al (1997) Requirement for NF-kappaB in osteoclast and B-cell development. Genes Dev 11(24):3482–3496PubMedCrossRef
73.
Kong YY et al (1999) OPGL is a key regulator of osteoclastogenesis, lymphocyte development and lymph-node organogenesis. Nature 397(6717):315–323PubMedCrossRef
74.
Tagaya H et al (2013) Intramedullary and extramedullary B lymphopoiesis in osteopetrotic mice. Blood 95(11):3363–3370
75.
Blin-Wakkach C et al (2004) Hematological defects in the oc/oc mouse, a model of infantile malignant osteopetrosis. Leukemia 18(9):1505–1511PubMedCrossRef
76.
Scimeca JC et al (2000) The gene encoding the mouse homologue of the human osteoclast-specific 116-kDa V-ATPase subunit bears a deletion in osteosclerotic (oc/oc) mutants. Bone 26(3):207–213PubMedCrossRef
77.
Blin-Wakkach C et al (2004) Characterization of a novel bipotent hematopoietic progenitor population in normal and osteopetrotic mice. J Bone Miner Res 19(7):1137–1143PubMedCrossRef
78.
Blin-Wakkach C et al (2006) Interleukin-7 partially rescues B-lymphopoiesis in osteopetrotic oc/oc mice through the engagement of B220+ CD11b+ progenitors. Exp Hematol 34(7):851–859PubMedCrossRef
79.
Mansour A et al (2011) Osteoclast activity modulates B-cell development in the bone marrow. Cell Res 21(7):1102–1115PubMedCrossRef
80.
Tang Y et al (2009) TGF-beta1-induced migration of bone mesenchymal stem cells couples bone resorption with formation. Nat Med 15(7):757–765PubMedCrossRef
81.
Cain CJ et al (2012) Absence of sclerostin adversely affects B-cell survival. J Bone Miner Res 27(7):1451–1461PubMedCrossRef
82.
Semenov M, Tamai K, He X (2005) SOST is a ligand for LRP5/LRP6 and a Wnt signaling inhibitor. J Biol Chem 280(29):26770–26775PubMedCrossRef
83.
Choi HY et al (2009) Lrp4, a novel receptor for Dickkopf 1 and sclerostin, is expressed by osteoblasts and regulates bone growth and turnover in vivo. PLoS One 4(11):e7930PubMedCrossRef
84.
Li X et al (2008) Targeted deletion of the sclerostin gene in mice results in increased bone formation and bone strength. J Bone Miner Res 23(6):860–869PubMedCrossRef
85.
Tamura M, Sato MM, Nashimoto M (2011) Regulation of CXCL12 expression by canonical Wnt signaling in bone marrow stromal cells. Int J Biochem Cell Biol 43(5):760–767PubMedCrossRef
86.
Chang MK et al (2008) Osteal tissue macrophages are intercalated throughout human and mouse bone lining tissues and regulate osteoblast function in vitro and in vivo. J Immunol 181(2):1232–1244PubMed
87.
Winkler IG et al (2013) B-lymphopoiesis is stopped by mobilizing doses of G-CSF and is rescued by overexpression of the anti-apoptotic protein Bcl2. Haematologica 98(3):325–333PubMedCrossRef
Metadata
Title
Interactions Between B Lymphocytes and the Osteoblast Lineage in Bone Marrow
Authors
Cristina Panaroni
Joy Y. Wu
Publication date
01-09-2013
Publisher
Springer US
Published in
Calcified Tissue International / Issue 3/2013
Print ISSN: 0171-967X
Electronic ISSN: 1432-0827
DOI
https://doi.org/10.1007/s00223-013-9753-3

Other articles of this Issue 3/2013

Calcified Tissue International 3/2013 Go to the issue

Editorial

Treatment Thresholds for Osteoporosis and Reimbursability Criteria: Perspectives Associated with Fracture Risk-Assessment Tools

Original Research

The Effect of Endogenous Parathyroid Hormone in Iliac Bone Structure and Turnover in Healthy Postmenopausal Women

Original Research

Ninety-One Osteoporosis Patients Affected with Bisphosphonate-Related Osteonecrosis of the Jaw: A Case Series

Original Research

Acidosis Inhibits Mineralization in Human Osteoblasts

Original Research

Adaptation of Tibial Structure and Strength to Axial Compression Depends on Loading History in Both C57BL/6 and BALB/c Mice

Original Research

Citrate Occurs Widely in Healthy and Pathological Apatitic Biomineral: Mineralized Articular Cartilage, and Intimal Atherosclerotic Plaque and Apatitic Kidney Stones
Obesity Clinical Trial Summary

At a glance: The STEP trials

Read more

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Pediatric Cardiology Video

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

Cardiopulmonary Comorbidity Video

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Valvular Heart Disease Video

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Heart Failure Video

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Heart Failure Video

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.

Watch now

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

16-04-2024 Type 2 Diabetes News

Incentivised to exercise

11-04-2024 Lifestyle Modifications News

New intervention for STEMI-related cardiogenic shock

10-04-2024 Myocardial Infarction News

» View more highlights on the ACC 2024 congress hub page

Image Credits