Top

Published in:

01-06-2014 | Progress in Hematology

Regulation of hematopoiesis in endosteal microenvironments

Authors: Noboru Asada, Yoshio Katayama

Published in: International Journal of Hematology | Issue 6/2014

Abstract

After birth, the hematopoietic system develops along with bone formation in mammals. Osteolineage cells are derived from mesenchymal progenitor cells, and differentiate into several types of bone-forming cells. Of the various types of cell constituents in bone marrow, osteolineage cells have been shown to play important roles in hematopoiesis. Early studies have identified osteoblasts as a hematopoietic stem cell niche component. Since that time, the role of endosteal microenvironment as a critical regulator of hematopoietic stem/progenitor cell (HSC/HPC) behavior has been appreciated particularly under stress conditions, such as cytokine-induced HSC/HPC mobilization, homing/engraftment after bone marrow transplantation, and disease models of leukemia/myelodysplasia. Recent studies revealed that the most differentiated osteolineage cells, i.e., osteocytes, play important roles in the regulation of hematopoiesis. In this review, we provide an overview of recent advances in knowledge of regulatory hematopoietic mechanisms in the endosteal area.

Omatsu Y, Sugiyama T, Kohara H, et al. The essential functions of adipo-osteogenic progenitors as the hematopoietic stem and progenitor cell niche. Immunity. 2010;33(3):387–99.PubMedCrossRef

Mendez-Ferrer S, Michurina TV, Ferraro F, et al. Mesenchymal and haematopoietic stem cells form a unique bone marrow niche. Nature. 2010;466(7308):829–34.PubMedCentralPubMedCrossRef

Greenbaum A, Hsu YM, Day RB, et al. CXCL12 in early mesenchymal progenitors is required for haematopoietic stem-cell maintenance. Nature. 2013;495(7440):227–30.PubMedCentralPubMedCrossRef

Ding L, Morrison SJ. Haematopoietic stem cells and early lymphoid progenitors occupy distinct bone marrow niches. Nature. 2013;495(7440):231–5.PubMedCentralPubMedCrossRef

Kunisaki Y, Bruns I, Scheiermann C, et al. Arteriolar niches maintain haematopoietic stem cell quiescence. Nature. 2013;502(7473):637–43.PubMedCrossRef

Komori T, Yagi H, Nomura S, et al. Targeted disruption of Cbfa1 results in a complete lack of bone formation owing to maturational arrest of osteoblasts. Cell. 1997;89(5):755–64.PubMedCrossRef

Nakashima K, Zhou X, Kunkel G, et al. The novel zinc finger-containing transcription factor osterix is required for osteoblast differentiation and bone formation. Cell. 2002;108(1):17–29.PubMedCrossRef

Nakashima K, de Crombrugghe B. Transcriptional mechanisms in osteoblast differentiation and bone formation. Trends Genet. 2003;19(8):458–66.PubMedCrossRef

Manolagas SC. Birth and death of bone cells: basic regulatory mechanisms and implications for the pathogenesis and treatment of osteoporosis. Endocr Rev. 2000;21(2):115–37.PubMed

10.

Jilka RL, Weinstein RS, Bellido T, et al. Osteoblast programmed cell death (apoptosis): modulation by growth factors and cytokines. J Bone Miner Res. 1998;13(5):793–802.PubMedCrossRef

11.

Bonewald LF. The amazing osteocyte. J Bone Miner Res. 2011;26(2):229–38.PubMedCentralPubMedCrossRef

12.

Fulzele K, Krause DS, Panaroni C, et al. Myelopoiesis is regulated by osteocytes through Gsalpha-dependent signaling. Blood. 2013;121(6):930–9.PubMedCentralPubMedCrossRef

13.

Asada N, Katayama Y, Sato M, et al. Matrix-embedded osteocytes regulate mobilization of hematopoietic stem/progenitor cells. Cell Stem Cell. 2013;12(6):737–47.PubMedCrossRef

14.

Sato M, Asada N, Kawano Y, et al. Osteocytes regulate primary lymphoid organs and fat metabolism. Cell Metab. 2013;18(5):749–58.PubMedCrossRef

15.

Taichman RS, Emerson SG. Human osteoblasts support hematopoiesis through the production of granulocyte colony-stimulating factor. J Exp Med. 1994;179(5):1677–82.PubMedCrossRef

16.

Calvi LM, Adams GB, Weibrecht KW, et al. Osteoblastic cells regulate the haematopoietic stem cell niche. Nature. 2003;425(6960):841–6.PubMedCrossRef

17.

Zhang J, Niu C, Ye L, et al. Identification of the haematopoietic stem cell niche and control of the niche size. Nature. 2003;425(6960):836–41.PubMedCrossRef

18.

Lymperi S, Horwood N, Marley S, et al. Strontium can increase some osteoblasts without increasing hematopoietic stem cells. Blood. 2008;111(3):1173–81.PubMedCrossRef

19.

Nakamura Y, Arai F, Iwasaki H, et al. Isolation and characterization of endosteal niche cell populations that regulate hematopoietic stem cells. Blood. 2010;116(9):1422–32.PubMedCrossRef

20.

Arai F, Hirao A, Ohmura M, et al. Tie2/angiopoietin-1 signaling regulates hematopoietic stem cell quiescence in the bone marrow niche. Cell. 2004;118(2):149–61.PubMedCrossRef

21.

Yoshihara H, Arai F, Hosokawa K, et al. Thrombopoietin/MPL signaling regulates hematopoietic stem cell quiescence and interaction with the osteoblastic niche. Cell Stem Cell. 2007;1(6):685–97.PubMedCrossRef

22.

Qian H, Buza-Vidas N, Hyland CD, et al. Critical role of thrombopoietin in maintaining adult quiescent hematopoietic stem cells. Cell Stem Cell. 2007;1(6):671–84.PubMedCrossRef

23.

Sugimura R, He XC, Venkatraman A, et al. Noncanonical Wnt signaling maintains hematopoietic stem cells in the niche. Cell. 2012;150(2):351–65.PubMedCrossRef

24.

Adams GB, Chabner KT, Alley IR, et al. Stem cell engraftment at the endosteal niche is specified by the calcium-sensing receptor. Nature. 2006;439(7076):599–603.PubMedCrossRef

25.

Kollet O, Dar A, Shivtiel S, et al. Osteoclasts degrade endosteal components and promote mobilization of hematopoietic progenitor cells. Nat Med. 2006;12(6):657–64.PubMedCrossRef

26.

Mansour A, Abou-Ezzi G, Sitnicka E, et al. Osteoclasts promote the formation of hematopoietic stem cell niches in the bone marrow. J Exp Med. 2012;209(3):537–49.PubMedCentralPubMedCrossRef

27.

Miyamoto K, Yoshida S, Kawasumi M, et al. Osteoclasts are dispensable for hematopoietic stem cell maintenance and mobilization. J Exp Med. 2011;208(11):2175–81.PubMedCentralPubMedCrossRef

28.

Tatsumi S, Ishii K, Amizuka N, et al. Targeted ablation of osteocytes induces osteoporosis with defective mechanotransduction. Cell Metab. 2007;5(6):464–75.PubMedCrossRef

29.

Marotti G, Ferretti M, Muglia MA, et al. A quantitative evaluation of osteoblast-osteocyte relationships on growing endosteal surface of rabbit tibiae. Bone. 1992;13(5):363–8.PubMedCrossRef

30.

Yellowley CE, Li Z, Zhou Z, et al. Functional gap junctions between osteocytic and osteoblastic cells. J Bone Miner Res. 2000;15(2):209–17.PubMedCrossRef

31.

Crucian B, Sams C. Immune system dysregulation during spaceflight: clinical risk for exploration-class missions. J Leukoc Biol. 2009;86(5):1017–8.PubMedCrossRef

32.

Gueguinou N, Huin-Schohn C, Bascove M, et al. Could spaceflight-associated immune system weakening preclude the expansion of human presence beyond Earth’s orbit? J Leukoc Biol. 2009;86(5):1027–38.PubMedCrossRef

33.

Christopher MJ, Link DC. Granulocyte colony-stimulating factor induces osteoblast apoptosis and inhibits osteoblast differentiation. J Bone Miner Res. 2008;23(11):1765–74.PubMedCentralPubMedCrossRef

34.

Katayama Y, Battista M, Kao WM, et al. Signals from the sympathetic nervous system regulate hematopoietic stem cell egress from bone marrow. Cell. 2006;124(2):407–21.PubMedCrossRef

35.

Kawamori Y, Katayama Y, Asada N, et al. Role for vitamin D receptor in the neuronal control of the hematopoietic stem cell niche. Blood. 2010;116(25):5528–35.PubMedCrossRef

36.

Mendez-Ferrer S, Lucas D, Battista M, Frenette PS. Haematopoietic stem cell release is regulated by circadian oscillations. Nature. 2008;452(7186):442–7.PubMedCrossRef

37.

Chow A, Lucas D, Hidalgo A, et al. Bone marrow CD169+ macrophages promote the retention of hematopoietic stem and progenitor cells in the mesenchymal stem cell niche. J Exp Med. 2011;208(2):261–71.PubMedCentralPubMedCrossRef

38.

Christopher MJ, Rao M, Liu F, et al. Expression of the G-CSF receptor in monocytic cells is sufficient to mediate hematopoietic progenitor mobilization by G-CSF in mice. J Exp Med. 2011;208(2):251–60.PubMedCentralPubMedCrossRef

39.

Winkler IG, Sims NA, Pettit AR, et al. Bone marrow macrophages maintain hematopoietic stem cell (HSC) niches and their depletion mobilizes HSCs. Blood. 2010;116(23):4815–28.PubMedCrossRef

40.

Taylor AF, Saunders MM, Shingle DL, et al. Mechanically stimulated osteocytes regulate osteoblastic activity via gap junctions. Am J Physiol Cell Physiol. 2007;292(1):C545–52.PubMedCrossRef

41.

Chang MK, Raggatt LJ, Alexander KA, et al. Osteal tissue macrophages are intercalated throughout human and mouse bone lining tissues and regulate osteoblast function in vitro and in vivo. J Immunol. 2008;181(2):1232–44.PubMedCrossRef

42.

Kamioka H, Honjo T, Takano-Yamamoto T. A three-dimensional distribution of osteocyte processes revealed by the combination of confocal laser scanning microscopy and differential interference contrast microscopy. Bone. 2001;28(2):145–9.PubMedCrossRef

43.

Gonzalez-Nieto D, Li L, Kohler A, et al. Connexin-43 in the osteogenic BM niche regulates its cellular composition and the bidirectional traffic of hematopoietic stem cells and progenitors. Blood. 2012;119(22):5144–54.PubMedCentralPubMedCrossRef

44.

Ishikawa F, Yoshida S, Saito Y, et al. Chemotherapy-resistant human AML stem cells home to and engraft within the bone-marrow endosteal region. Nat Biotechnol. 2007;25(11):1315–21.PubMedCrossRef

45.

Ishikawa F. Modeling normal and malignant human hematopoiesis in vivo through newborn NSG xenotransplantation. Int J Hematol. 2013;98(6):634–40.PubMedCrossRef

46.

Schepers K, Pietras EM, Reynaud D, et al. Myeloproliferative neoplasia remodels the endosteal bone marrow niche into a self-reinforcing leukemic niche. Cell Stem Cell. 2013;13(3):285–99.PubMedCrossRef

47.

Raaijmakers MH, Mukherjee S, Guo S, et al. Bone progenitor dysfunction induces myelodysplasia and secondary leukaemia. Nature. 2010;464(7290):852–7.PubMedCentralPubMedCrossRef

48.

Raaijmakers MH. Myelodysplastic syndromes: revisiting the role of the bone marrow microenvironment in disease pathogenesis. Int J Hematol. 2012;95(1):17–25.PubMedCrossRef

49.

Kode A, Manavalan JS, Mosialou I, et al. Leukaemogenesis induced by an activating beta-catenin mutation in osteoblasts. Nature. 2014;506(7487):240–4.PubMedCrossRef

Title: Regulation of hematopoiesis in endosteal microenvironments
Authors: Noboru Asada
Yoshio Katayama
Publication date: 01-06-2014
Publisher: Springer Japan
Published in: International Journal of Hematology / Issue 6/2014
Print ISSN: 0925-5710
Electronic ISSN: 1865-3774
DOI: https://doi.org/10.1007/s12185-014-1583-1

Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Watch now

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras

Prof. Fabrice Barlesi

Developed by: Springer Medicine

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 6/2014

Bortezomib plus melphalan and prednisone (VMP regimen) as the initial treatment for IgE multiple myeloma: a case study

Primary B-lymphoblastic lymphoma of gallbladder involving mandibular bone

Transient abnormal myelopoiesis in a phenotypically normal newborn with polyclonal trisomy 21

Bone marrow Schwann cells induce hematopoietic stem cell hibernation

SCF/C-KIT signaling modulates tryptase expression in acute myeloid leukemia cells

Incidence and outcomes of Clostridium difficile-associated disease in hematopoietic cell transplant recipients

Keynote webinar | Spotlight on antibody–drug conjugates in cancer