Bone marrow microenvironment and its role in the pathogenesis of leukaemia
Authors:
E. Létalová 1; M. Doubek 2; F. Folber 1; J. Verner 1; M. Mráz 2; Š. Pospíšilová 2; J. Mayer 2
Authors‘ workplace:
Interní hematoonkologická klinika, Fakultní nemocnice Brno a Lékařská fakulta Masarykovy univerzity, Brno
1; Středoevropský technologický institut, Masarykova univerzita, Brno
2
Published in:
Transfuze Hematol. dnes,17, 2011, No. 4, p. 171-176.
Category:
Comprehensive Reports, Original Papers, Case Reports
Overview
Bone marrow microenvironment plays a key role in the process of haematopoiesis. It has a supportive function for quiescent haematopoietic stem cells located in so called „niches“. It provides appropriate conditions for haematopoietic stem cell differentiation and for the proliferation of blood elements. Under certain conditions, the bone marrow microenvironment may be colonized by circulating peripheral haematopoietic stem cells (a fact used in the process of peripheral blood stem cell transplantation). It is probable that this mechanism is also used by malignant (leukemic) cells to infiltrate the microenvironment and thus take advantage of all the supportive functions provided to divide, proliferate and more or less differentiate into the leukemic population.
Key words:
haematopoiesis, bone marrow microenvironment, haematopoietic stem cell niche
Sources
1. Greer JP, Foerster J, Rodgers GM, Paraskevas F, Glader B, Arber DA, Means RT (Eds.). Wintrobeęs clinical hematology. 12th edition. Vol. 1. Wolters Kluwer/Lippincot Williams & Wilkins, Philadelphia 2009; 1329 s.
2. Yoder MC, Williams DA. Matrix molecule interactions with hematopoietic stem cells. Exp Hematol 1995; 23: 961-967.
3. Bentley SA. Collagen synthesis by bone marrow stromal cells: a quantitative study. Br J Haematol 1982; 50: 491-497.
4. Gay RE, Prince CW, Zuckerman KS, et al. The collagenous hemopoietic microenvironment. Humana Press, Clifton 1989; 369-398.
5. Williams DA, Rios M. Stephens C, et al. Fibronectin and VLA-4 in haematopoietic stem cell-microenvironment interactions. Nature 1991; 352: 438-441.
6. Russell ES. Hereditary anemias of the mouse: a review for geneticists. Adv Genet 1979; 20: 357-459.
7. Tavassoli M, Hardy CL. Molecular basis of homing of intravenously transplanted stem cells to the bone marrow. Blood 1990; 76: 1059-1070.
8. Bouvard D, Brakebusch C, Gustafsson E, et al. Functional consequences of integrin gene mutations in mice. Circ Res 2001;89:211-223.
9. Levesque JP, Simmons PJ. Cytoskeleton and integrin-mediated adhesion signaling in human CD 34+ hemopoietic progenitor cells. Exp Hematol 1999; 27: 579-586.
10. Scott LM, Priestley GV, Papayannopoulou T. Deletion of alpha4 integrins from adult hematopoietic cells reveals roles in homeostasis, regeneration, and homing. Mol Cell Biol 2003; 23: 9349-9360.
11. Papayannopoulou T, Nakamoto B, Peripheralization of hemopoietic progenitors in primates treated with anti-VLA4 integrin. Proc Natl Acad Sci USA 1993; 90: 9374-9378.
12. Papayannopoulou T, Priestley GV Nakamoto B, Anti-VLA4/VCAM-1-induced mobilization requires cooperative signaling through the kit/mkit ligandparhway. Blood 1998; 91: 2231-2239.
13. Papayannopoulou T, Craddock C, Nakamoto B, et al. 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 1995;92:9647-9651.
14. Zanjani EC, Flake AW, Almeida-Porada G, et al. Homing of human cells in the fetal sheep model: modulation by antibodies activating or inhibiting very late activation antigen-4-dependent function. Blood 1999;94:2515-2522.
15. Delforge M, Raets V, Van Duppen V, et al. CD34+ marrow progenitors from MDS patients with high levels of intramedullary apoptosis have reduced expression of alpha2beta1 and alpha5beta1 integrins. Leukemia 2005; 19: 57-63.
16. Koni PA, Joshi SK, Temann UA, et al. Conditional vascular cell adhesion molecule 1 deletion in mice: impaired lymphocyte migration to bone marrow. J Exp Med 2001; 193: 741-754.
17. Leuker CE, Labow M, Muller W, et al. 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 2001; 193: 755-768.
18. Fox NE, Kaushansky K. Engagement of integrin alpha 4beta1 enhances thrombopoietin-induced megakaryopoiesis. Exp Hematol 2005; 33: 94-99.
19. Etzioni A, Doerschuk CM, Harlan JM. Of man and mouse: leukocyte and endothelial adhesion molecule deficiencies. Blood 1999; 94: 3281-3288.
20. Greenberg AW, Kerr WG, Hammer DA. Relationship between selectin-mediated rolling of hematopoietic stem and progenitor cells and progression in hematopoietic development. Blood 2000; 95: 478-486.
21. Naiyer Aj, Jo DY, Ahm J, et al. Stromal derived factor-1-induced chemokinesis of cord blood CD34(+) cells (long-term culture-initiating cells) through endothelial cells is mediated by E-selectin. Blood 1999; 94: 4011-4019.
22. Aiuti A, Webb IJ, Bleul C, et al. The chemokine SDF-1 is a chemoattractant for human CD 34+ hematopoietic progenitor cells and provides a new mechanism to explain the mobilization of CD 34+ progenitors to peripheral blood. J Exp Med 1997; 185: 111-120.
23. Wright DE, Bowman EP, Wagers AJ, et al. Hematopoietic stem cells are uniquely selective in their migratory response to chemokines. J Exp Med 2002; 195: 1145-1154.
24. Nagasawa T, Hirota S, Tachibana K, et al. Defects of B-cell lymphopoiesis and bone-marrow myelopoiesis in mice lacking the CXC chemokine PBSF/SDF-1. Nature 1996; 382: 635-638.
25. Zou YR, Kottmann AH, Kuroda M, et al. Function of the chemokine receptor CXCR4 in haematopoiesis and in cerebellar development. Nature 1998; 393: 595-599.
26. Uhlman DL, Luikhart SD. The role of proteoglycans in the adhesion and differentiation of hematopoietic cells. In: Long MW, Wicha MS, eds. The hematopoietic microenvironment. Baltimore: The Johns Hopkins University Press, 1993: 232-245.
27. Wight TN, Kinsella MG, Keating A, et al. Proteoglycans in human long-term bone marrow cultures: biochemical and ultracstructural analyses. Blood 1986; 67: 1333-1343.
28. Siczkowski M, Clarke D, Gordon MY. Binding of primitive hematopoietic progenitor cells to marrow stromal cells involves heparan sulfate. Blood 1992;80:912-919.
29. Minguell JJ, Hard C, Tavassoli M. Membrane-associated chondroitin sulfate proteoglycan and fibronectin mediate the binding of hemopoietic progenitor cells to stromal cells. Exp Cell Res 1992; 201: 200-207.
30. Bruno E, Luikart SD, Long MW, et al. Marrow-derived heparan sulfate proteoglycan mediates the adhesion of hematopoietic progenitor cells to cytokines. Exp Hematol 1995; 23: 1212-1217.
31. Gordon MY, Riley GP, Watt SM, et al. Compartmentalization of a haematopoietic growth factor (GM-CSF) by glycosaminoglycans in the bone marrow microenvironment. Nature 1987; 326: 403-405.
32. Roberts R, Gallagher J, Spooncer E, et al. Heparan sulphate bound growth factors a mechanism for stromal cell mediated haemopoiesis. Nature 1988; 332: 376-378.
33. Schofield R. The relationship between the spleen colony-forming cell and the haemopoietic stem cell. Blood Cells 1978; 4: 7-25.
34. Yin T, Li L. The stem cell niches in bone. J Clin Invest 2006; 116: 1195-1201.
35. Taichman RS, Reálky MJ, Emerson SG. Human osteoblasts support human hematopoietic progenitor cells in vitro bone marrow cultures. Blood 1996; 87: 518-524.
36. Kopp HG, Avecilla ST, Hooper AT, et al. The bone marrow vascular niche: home of HSC differentiation and mobilization. Physiology (Bethesda) 2005; 20: 349-356.
37. Kiel MJ, Yilmaz OH, Iwashita T, et al. SLAM family receptors distinguish hematopoietic stem and progenitor cells and repeal endothelial niches for stem cells. Cell 2005; 121: 1109-1121.
38. Chute JP, Saini AA, Chute DJ, et al. Ex vivo culture with human brain endothelial cells increases the SCID-repopulating capacity of adult human bone marrow. Blood 2002; 100: 4433-4439.
39. Caligaris-Cappio F, Ghia P. Novel insights in chronic lymphocytic leukemia: are we getting closer to understanding the pathogenesis of the disease? J Clin Oncol 2008; 26: 4497-4503.
40. Burger JA, Kipps TJ. CXCR4: a key receptor in the crosstalk between tumor cells and their microenvironment. Blood 2006; 107: 1761-1767.
41. Burkle A, Niedermeier M, Schmitt-Graff A, Wierda WG, Keating MJ, Burger JA. Overexpression of the CXCR5 chemokine receptor, and its ligand, CXCL13 in B-cell chronic lymphocytic leukemia. Blood 2007; 110: 3316-3325.
42. Till KJ, Lin K, Zuzel M, Cawley JC. The chemokine receptor CCR7 and alpha4 integrin are important for migration of chronic lymphocytic leukemia cells into lymph nodes. Blood 2002; 99: 2977-2984.
43. Letilovic T, Vrhovac R, Verstovsek S, Jaksic B, Ferrajoli A. Role of angiogenesis in chronic lymphocytic leukemia. Cancer 2006; 107: 925-934.
44. von Bergwelt-Baildon M, Maecker B, Schultze J, Gribben JG. CD40 activation: potential for specific immunotherapy in B-CLL. Ann Oncol 2004; 15: 853-857.
45. Zucchetto A, Benedetti D, Tripodo C, et al. CD38/CD31, the CCL3 and CCL4 chemokines, and CD49d/VCAM-1 are interchained by sequential events sustaining chronic lymphocytic leukemia cell survival. Cancer Res 2009; 69: 4001-4009.
46. Smolej L. Význam mikroprostředí u chronické lymfocytární leukemie. Transfuze Hematol dnes 2010; 16(suppl. 1): 24-28.
47. Spangrude GJ, Heimfeld S, Weissman IL. Purification and characterization of mouse hematopoietic stem cells. Science 1988; 241: 58-62.
48. Bonnet D, Dick JE. Human acute myeloid leukemia is organized as a hierarchy that originates from primitive hematopoietic cells. Nat Med 1997; 3: 730-737.
49. Lapidot T, Sirard C, Vormoor J, et al. A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature 1994; 367: 645-648.
50. Cozzio A, Passegue E, Ayton PM, Karsunky H, Cleary ML, Weissman IL. Similar MLL-associated leukemias arising from self-renewing stem cells and short-lived myeloid progenitors. Genes Dev 2003; 17: 3029-3035.
51. Krivtsov AV, Twomey D, Feng Z, et al. Transformation from committed progenitor to leukaemia stem cell initiated by MLL-AF9. Nature 2006; 442: 818-822.
52. Huntly BJ, Shigematsu H, Deguchi K, et al. MOZ-TIF2, but not BCR-ABL, confers properties of leukemic stem cells to committed murine hematopoietic progenitors. Cancer Cell 2004; 6: 587-596.
53. Rombouts EJ, Pavic B, Lowenberg B, Ploemacher RE. Relation between CXCR-4 expression, Flt3 mutations, and unfavorable prognosis of adult acute myeloid leukemia. Blood 2004; 104: 550-557.
54. Spoo AC, Lubbert M, Wierda WG, Burger JA. CXCR4 is a prognostic marker in acute myelogenous leukemia. Blood 2007; 109: 786-791.
55. Somervaille TC, Cleary ML. Identification and characterization of leukemia stem cells in murine MLL-AF9 acute myeloid leukemia. Cancer Cell 2006; 10: 257-268.
56. Krause DS, Lazarides K, von Andrian UH, Van Etten RA. Requirement for CD44 in homing and engraftment of BCR-ABL-expressing leukemic stem cells. Nat Med 2006; 12: 1175-1180.
57. Florian S, Sonneck K, Hauswirth AW, et al. Detection of molecular targets on the surface of CD34+/CD38- stem cells in various myeloid malignancies. Leuk Lymphoma 2006; 47: 207-222.
58. Paget S. The distribution of secondary growths in cancer of the breast. 1889. Cancer Metastasis Rev 1989; 8: 98-101.
59. Bhatia R, McGlave PB, Dewald GW, Blazar BR, Verfaillie CM. Abnormal function of the bone marrow microenvironment in chronic myelogenous leukemia: role of malignant stromal macrophages. Blood 1995; 85: 3636-3645.
60. Colmone A, Amorim M, Pontier AL, Wang S, Jablonski E, Sipkins DA. Leukemic cells create bone marrow niches that disrupt the behavior of normal hematopoietic progenitor cells. Science 2008; 322: 1861-1865.
61. 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: 977-988.
62. Oberlin E, Amara A, Bachelerie F, et al. The CXC chemokine SDF-1 is the ligand for LESTR/fusin and prevents infection by T-cell-line-adapted HIV-1. Nature 1996; 382: 833-835.
63. Peled A, Petit I, Kollet O, et al. Dependence of human stem cell engraftment and repopulation of NOD/SCID mice on CXCR4. Science 1999; 283: 845-848.
64. Vianello F, Villanova F, Tisato V, et al. Bone marrow mesenchymal stromal cells non-selectively protect chronic myeloid leukemia cells from imatinib-induced apoptosis via the CXCR4/CXCL12 axis. Haematologica 2010; 95: 1081-1089.
65. Dillmann F, Veldwijk MR, Laufs S, et al. Plerixafor inhibits chemotaxis toward SDF-1 and CXCR4-mediated stroma contact in a dose-dependent manner resulting in increased susceptibility of BCR-ABL+ cell to Imatinib and Nilotinib. Leuk Lymphoma 2009; 50: 1676-1686.
66. Nair RR, Tolentino J, Hazlehurst LA. The bone marrow microenvironment as a sanctuary for minimal residual disease in CML. Biochem Pharmacol 2010; 80: 602-612.
Labels
Haematology Internal medicine Clinical oncologyArticle was published in
Transfusion and Haematology Today
2011 Issue 4
Most read in this issue
- Bone marrow microenvironment and its role in the pathogenesis of leukaemia
- Donor lymphocyte collections from unrelated donors of the Czech National Marrow Donors Registry (ČNMDR) between 1999 and 2010
- Serum levels of immunoglobulin free light chains in monoclonal gammopathy of undetermined significance and their contribution to stratification and monitoring
- Randomized, double-blind trial of fluconazole versus variconazole for prevention of invasive fungal infection after allogeneic hematopoietic cell transplantation