Expression and function of adhesion receptors in acute myelogenous leukemia: Parallels with normal erythroid and myeloid progenitors

Acta Haematologica

Volumn 97, Issue 1-2, 1997, Pages 53-62

  Liesveld, Jane L ^a  

^a UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

Author keywords

Acute myelogenous leukemia; Adhesion; Receptor function; Surface phenotype

Indexed keywords

CELL ADHESION MOLECULE; CELL SURFACE RECEPTOR; IMMUNOGLOBULIN; INTEGRIN; PROTEOGLYCAN; SELECTIN; SIALOADHESIN;

ACUTE GRANULOCYTIC LEUKEMIA; ANTIGEN EXPRESSION; BLAST CELL; BONE MARROW CELL; CANCER CLASSIFICATION; CELL ADHESION; CELL INTERACTION; ERYTHROID CELL; EXTRACELLULAR MATRIX; HEMATOPOIETIC STEM CELL; PRIORITY JOURNAL; REVIEW;

ACUTE DISEASE; ANTIGENS, CD; BONE MARROW; CELL ADHESION; CONNECTIVE TISSUE; EXTRACELLULAR MATRIX PROTEINS; GENE EXPRESSION REGULATION, LEUKEMIC; HEMATOPOIESIS; HUMANS; INTEGRINS; L-SELECTIN; LEUKEMIA, MYELOID; NEOPLASM PROTEINS; PHENOTYPE; PROTEOGLYCANS; TUMOR STEM CELLS;

EID: 14444285265     PISSN: 00015792     EISSN: 14219662     Source Type: Journal    
DOI: 10.1159/000203659     Document Type: Article

References (103)

1. Miller KB: Clinical manifestations of acute myeloid leukemia; in Hoffman R, Benz EJ, Shattil SJ, Furie B, Cohen HJ, Sibcrstcin LE (eds): Hematology, Basic Principles and Practice. New York, Churchill Livingstone, 1995, pp 993-1004.
2. Lichtman MA: The ultrastructure of the hemopoietic environment of the marrow: A review. Exp Hcmatol 1981;9:391-401.
3. Reuss-Borst MA, Burgring HJ, Klein G, Muller CA: Adhesion molecules on CD34+ hematopoietic cells in normal human bone marrow and leukemia. Ann Hematol 1992;65; 169- 174.
4. Long MW: Blood cell cytoadhesion molecules. Exp Hematol 1992;20:288-301.
5. Hcmlcr ME, Lobb RR: The leukocyte ßi inte-grins. CurrSci 1995;2:61-67.
6. Sanchez-Aparicio P, Domingucz-Jimcncz C, Garcia-Pardo A: Activation of the a4l inte-grin through the ßi subunit induces recognition of the RGDS sequence in fibronectin. J Cell Biol 1994;126:271-279.
7. Stamenkovic I: The L-selectin adhesion system. CurrSci 1995;2:68-75.
8. Norman KE, Moore KL, McEver RP, Ley K: Leukocyte rolling in vivo is mediated by P-sclcctin glycoprotein ligand-1. Blood 1995;86: 4417-4421.
9. Buzby JS, Knoppel EM, Cairo MS: Coordinate regulation of Steel factor, its receptor (Kit), and cytoadhesion molecule (ICAM-1 and ELAM-1) mRNA expression in human vascular endothelial cells of differing origins. Exp Hematol 1994;22:122-129.
10. Liesveld JL. DiPcrsio JF, Abboud CN: Intc-grins and adhesive receptors in normal and leukemic CD34+ progenitor cells: Potential regulatory checkpoints for cellular traffic. Leuk Lymphoma 1994;14:19-28.
11. Liesveld J, Winslow JM, Frediaini KE, Ryan DH. Abboud CN: Expression of integrins and examination of their adhesive function in normal and leukemic hematopoietic cells. Blood 1993;81:112-121.
12. Sealand S, Durvet V, Caux C, Pandrau D. Favre C, Valle A, Durand I, Charbord P, deVries J, Banchereau J: Distribution of surface membrane molecules on bone marrow and cord blood CD34+ hematopoietic cells. Exp Hematol 1992;20:24-33.
13. Coustan-Smith E, Behm FG, Hurwitz CA, Rivera GK, Campana D: N-CAM (CD56) expression by CD34+ malignant myeloblasts has implications for minimal residual disease detection in acute myeloid leukemia. Leukemia 1993;7:853-858.
14. Soligo D, Schiro R. Luksch R, Manara G, Qui-riei N, Parravicini C, Deliliers G: Expression of integrins in human bone marrow. Br J Haematol 1990;76:323-332.
15. Archimbaud E, Thomas X, Campos L, Maguad JP, Dorc JF, Ficrc D: Expression of surface adhesion molecules CD54 (ICAM-1) and CD58 (LFA-3) in adult acute leukemia: Relationship within initial characteristics and prognosis. Leukemia 1992;6:265-271.
16. Lukashev ME. Sheppard D, Pytela R: Disruption of integrin function and induction of tyrosine phosphorylation by the autonomously expressed Pi integrin cytoplasmic domain. J Biol Chem 1994:269:18311-18314.
17. Yoder MC, Williams DA: Matrix molecule interactions with hematopoietic stem cells. Exp Hematol 1995;23:961-967.
18. Verfaille CM, McCarthy JB. McGlavc PB: Differentiation of primitive human multipotent liematopoictic progenitors into single lineage donogenic progenitors is accompanied by alteration in their interactions with fibronectin. J Exp Med 1991;174:693-703.
19. Verfaillie C, Benis A, Iida J, McGlavc P, McCarthy J: Adhesion of committed human hematopoietic progenitors to synthetic peptides from the C-terminal heparin-binding domain of fibronectin: Cooperation between the integrin ajpi and the CD44 adhesion receptor. Blood 1994:84:1802-1811.
20. Coulombel L, Vuillet M, Leroy C, Tchcrnia G: Lineage and stage-specific adhesion of human hematopoietic progenitor cells to extracellular matrices from marrow fibroblasts. Blood 1988; 71:329-334.
21. Tsai S, Patel V, Beaumont E, Lodish H, Nathan D, Sieff C: Differential binding of cry-throid and myeloid progenitors to fibroblasts and fibronectin. Blood 1987;69:1587-1594.
22. Weinstein R, Riordan M, Wenc K, Kreczko S, Zhou M,: Dual role of fibronectin in hematopoietic differentiation. Blood 1989;73: 111-116.
23. Vuillet-Gaugler M, Breton-Gorius J, Vain-chenker W, Guichard J, Leroy C, Tchcrnia G, Coulombel L: Loss of attachment to fibronectin with terminal erythroid differentiation. Blood 1990;75:865-873.
24. Patel V, Ciechanover A, Platt O, Lodish HF: Mammalian reticulocytes lose adhesion to fibronectin during maturation to erythrocytes. ProcNatl Acad Sci USA 1985;82:440-444.
25. Patel V, Lodish H: The fibronectin receptor on mammalian erythroid precursor cells: Characterization and developmental regulation. J Cell Biol 1986;102:449-456.
26. Zannettino ACW, Berndt MC, Butcher C, Butcher EC, Vadas MA, Simmons PJ: Primitive human hematopoietic progenitors adhere to P-selectin (CD62P). Blood 1995:86:3466-3477.
27. Bevilacqua MP, Stengclin S, Gimbrone MA, Seed B: Endothelial leukocyte adhesion molecule-1: An inducible receptor for neutrophils related to complement regulatory proteins and lectins. Science 1989;243:1160-1165.
28. Foxall C, Watson SR. Dowbenko D, Fennie C, Lasky LA, Kiso M, Hasagawa A, Asa D. Brand-Icy BK: The three members of the selectin receptor family recognize a common carbohydrate epitope, the sialyl Lewis-x oligosaccharide. J Cell Biol 1992; 117:895-902.
29. Freeman SD, Kelm S, Barber EK, Crocker PR: Characterization of CD33 as a new member of the sialadhesin family of cellular interaction molecules. Blood 1995;85:2005-2012.
30. Remold-O'Donnell E, Kenney DM, Parkman R, Cairns L, Savage B. Rosen FS: Characterization of a human lymphocyte surface sialoglyco-protein that is defective in Wiskott-Aldrich syndrome. J Exp Med 1984; 159:1705-1723.
31. Bazil V, Brandt J, Tsukamoto A, Hoffman R: Apoptosis of human hematopoietic progenitor cells induced by crosslinking of surface CD43, the major sialoglycoprotcin of leukocytes. Blood 1995:86:502-511.
32. Traore Y, Him J: Certain anti-CD34 monoclonal antibodies induce homotypic adhesion of leukemic cell lines in a CD18-dcpendcnt and a CD 18-independent way. Eur J Immunol 1994;24:2304-2311.
33. Kortlcpcl K, Bcndall U, Gottlieb DJ: Human acute myeloid leukemia cells express adhesion proteins and bind to bone marrow fibroblast monolayers and extracellular matrix proteins. Leukemia 1993;7:1174-1179.
34. Ross L, Davis CM, Molony L: A truncated recombinant intercellular adhesion molecule-1 inhibits adhesion of leukemic cell lines to upregulated endothelial cells. In Vitro Cell Dev Biol 1994;30A:875-880.
35. Bradstock KF. Gottlieb DJ: Interaction of acute leukemia cells with the bone marrow microenvironment: Implications for control of minimal residual disease. Lcuk Lymphoma 1995;18:1-16.
36. Ghaffari S, Dougherty GJ, Lansdorp PM, Eaves AC. Eaves CJ: Differentiation-associated changes in CD44 isoform expression during normal hematopoiesis and their alteration in chronic myeloid leukemia. Blood 1995:86: 2976-2985.
37. Lcwinsohn DM, Naglcr A, Ginzton N, Greenberg P. Butcher EC: Hematopoietic progenitor cell expression of the H-CAM (CD44) homing-associated adhesion moelcule. Blood 1990;75: 589-595.
38. Thomas X. Vila L, Campos L. Sabido O, Ar-chimbaud E: Expression of N-CAM (CD56) on acute leukemia cells: Relationship with disease characteristics and outcome. Lcuk Lymphoma 1995:19:295-300.
39. Bennett JM. Catovsky D, Daniel MT, Flandrin G, Galton DAG. Gralnick HR, Sultan C: Proposed revised cirteria for the classification of acute myeloid leukemia: A report of the French-American-British Cooperative Group. Ann Intern Med 1985;103:620-625.
40. Papayannopoulou T, Brice M: Integrin expression profiles during erythroid differentiation. Blood 1992;78:1686-1694.
41. van Schravendijk MR, Handunnitti SM. Barnwell JW, Howard RJ: Normal human erythrocytes express CD36, an adhesion molecule of monocytes, platelets, and endothelial cells. Blood 1992;80:2105-2114.
42. Rosemblatt M, Vuillet-Gaugler M, Leroy C, Coulombcl L: Cocxprcssion of two fibronectin receptors, VLA-4 and VLA-5, by immature human erythroblastic precursor cells. J Clin Invest 1991;87:6-11.
43. Okumura N, Tsuji K, Nakahata T: Changes in cell surface antigen expression during proliferation and differentiation of human erythroid progenitors. Blood 1992;80:642-650.
44. Sugimoto K, Tsurumaki Y, Hoshi H, Kadowa-ki S, LeBousse-Kerdiles MC, Smadja-Joffe F, Mori KJ: Effects of anti-CD44 monoclonal antibody on adhesion of erythroid leukemic cells (ELM-1-1) to hematopoietic supportive cells (MS-5): CD44. but not hyaluronate-mediated, cell-cell adhesion. Exp Hcmatol 1994,22:488-494.
45. Banu N, Wang JF, Deng B, Groopman JE, Avraham H: Modulation of megakaryocyto-poiesis by thrombopoietin: the c-mpl ligand. Blood 1995;86:1331-1338.
46. Clark BR, Gallagher JT, Dexter TM: Cell adhesion in the stromal regulation of haemopoiesis. Bailliéres Clin Haematol 1992;5:619-652.
47. Tavassoli M, Mingucll JJ: Homing of hemopoietic progenitor cells to the marrow. Proc Soc Exp Biol Med 1991;196:367-373.
48. Simmons PJ, Masinovsky B, Longenccker BM. Berenson R, Torok-Storb B. Gallatin W: Vascular cell adhesion molecule-1 expressed by bone marrow stroma cells mediates the binding of hematopoietic progenitor cells. Blood 1992; 80:388-395.
49. Kortlepel K, Bendall LJ, Gottlieb DJ: Human acute myeloid leukemia cells express adhesion proteins and bind to bone marrow fibroblasts monolayers and extracellular matrix proteins. Leukemia 1993;7:1174-1179.
50. Long WM, Briddell R, Walter AW, Bruno E, Hoffman R: Human hematopoietic stem cell adherence to cytokines and matrix molecules. J Clin Invest 1992;90:251-255.
51. hi stem cells to bone marrow stroma. J Clin Invest 1992;90:358-367.
52. Dcnkcrs IAM, Beelen RHJ, Ossenkoppele GJ, Nauta JJP. Langen-huijscn MMAC: Adhesive capacity of human long-term bone marrow cultures from normals and patients with acute myeloid leukaemia: The influence of adhesion molecules. Lcuk Res 1993;17:255-261.
53. Bendall LJ. Kortlepel K, Gottlieb DJ: Human acute myeloid leukemia cells bind to bone marrow stroma via a combination of beta-1 and beta-2 integrin mechanisms. Blood 1993:82: 3125-3132.
54. Butcher EC: Leukocyte-endothelial cell recognition: Three (or more) steps to specificity and diversity. Cell 1991;67:1033-1036.
55. Liesveld JL, Frediani KE, Harbol AW. DiPcr-sio JF, Abboud CN: Characterization of the adherence of normal and leukemic CD34+ cells to endothelial monolayers. Leukemia 1994:8: 2111-2117.
56. Cavcnaugh JD, Gordon-Smith EC, Gibson FM, Gordon MY: Acute myeloid leukaemia blast cells bind to human endothelium in vitro utilizing E-selectin and vascular cell adhesion moleculc-1 (VCAM-1). Br J Haematol 1993: 85:285-291.
57. Muori K, Suda T, Nojiri H, Amcmiya Y, Miu-ra Y, Singhal H, Hakomori S: Expression of sia-lyl-Lewis* in CD34-positivc leukemic blasts. Leukemia 1993;7:336.
58. Simmons PJ, Zannettion A, Gronthos S, Lcav-esley D: Potenital adhesion mechanisms for localisation of haemopoietic progenitors to bone marrow stroma. Lcuk Lymphoma 1994; 12:353-363.
59. Schweitzer CM, van der Schoot CE. Drager AM, van der Valk P, Zevenbergen A, Hooi-brind B, Westra AH, Langenhuijsen MMAC: Isolation and culture of human bone marrow endothelial cells. Exp Hematol 1995;23:41-48.
60. Rafti S, Shapiro F, Pettengcll R. Ferris B, Nachman RL, Moore MAS, Asch AS: Human bone marrow microvascular endothelial cells support long-term proliferation and differentiation of myeloid and megakaryocytic progenitors. Blood 1995;86:3353-3363.
61. Schweitzer CM, van der Schoot CE, Drager AM, van der Valk P, Zevenbergen A, Hooi-brink B, Westra AH: Isolation and culture of human bone marrow endothelial cells. Exp Hematol 1995;23:41-48.
62. Koenigsmann M. Griffin JD. DiCarlo J, Can-nistra SA: Myeloid and erythroid progenitor cells from normal bone marrow adhere to collagen type I. Blood 1992;79:657-665.
63. Klein G. Muller CA. Tillet E, Chu ML, Timpl R: Collagen type VI in the human bone marrow microenvironment: A strong cytoadhesive component. Blood 1995;86:1740-1748.
64. Takada Y. Huang C, Hemler ME: Fibronectin receptor structure in the VLA family of heterodimers. Nature 1987,326:607-609.
65. Long MW, Dixit VM: Thrombospondin functions as a cytoadhesion molecule for human hematopoietic progenitor cells. Blood 1990;75: 2311-2318.
66. Kerst JM, Sanders JB, Slapcr-Cortenbach IC. Doorakkers MC, Hooibrink B, van Oers RH. van dem Borne AE, van der Schoot CE: Alpha 4 and alpha 5 beta-1 are differentially expressed during myelopoiesis and mediate the adherence of CD34+ cells to fibronectin in an activation-dcpcndcnt way. Blood 1993:81: 244-351.
67. Gordon MY, Riley GP, Clarke D: Heparan sulfate is necessary for adhesive interactions between human early hemopoietic progenitor cells and the extracellular matrix of the marrow microenvironment. Leukemia 1988,2:804-809.
68. Siczkowski M, Clarke D, Gordon MY: Binding of primitive hematopoietic progenitor cells to marrow stromal cells involves heparan sulfate. Blood 1992:80:912-919.
69. Miyake K, Underhill CB, Lesley J, Kincade PW: Hyaluronate can function as a cell adhesion molecule and CD44 participates in hyaluronate recognition. J Exp Med 1990; 171:477-488.
70. Minguell JJ, Hardy 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.
71. Siczkowski M, Andrw T. Amos S. Gordon MY: Hyaluronic acid regulates the function and distribution of sulfated glycosaminoglycans in bone marrow stromal cultures. Exp Hematol 1993;21:126-130.
72. Timar J, Bartha DC, Ladanyi A, Tarcsafalvi A, Lapis K: PMA induces shift from chondroitin to heparan sulphate on proteoglycans correlating with fibronectin adhesion of MDS human leukemia cells. Anticancer Res 1994; 14:1227- 1231.
73. Gordon MY, Clarke D, Atkinson J, Greaves MF: Hemopoietic progenitor cell binding to stroma microenvironment in vitro. Exp Hematol 1990;18:837-842.
74. Kanakura Y, Ikeda H. Kitayman H, Sugahara H, Furitsu T: Expression, function and activation of the proto-oncogene c-kit product in human leukemia cells. Leuk Lymphoma 1993; 10:35-41.
75. McKenna HJ. de Vries P, Brascl K, Lyman SD, Williams DE: Effect of flt3 ligand on the ex vivo expansion of human CD34+ hematopoietic progenitor cells. Blood 1995;86:3413-3420.
76. Azzarelli B, Easterling K, Norton JA: Leukemic cell-endothelial cell interactions in leukemic cell dissemination. Lab Invest 1989:60: 45-64.
77. Papayannopoulou T, Nakamoto B: Peripheral-ization of hematopoietic progenitors in primates treated with anti-VLA4 integrin. Proc Natl Acad Sci USA 1993;90:9374-9378.
78. Mohle R. Murea S, Kirsch M, Haas R: Differential expression of L-selectin, VLA-4 and LFA-1 on CD34+ progenitor cells from bone marrow and peripheral blood during G-CSF-enhanced recovery. Exp Hematol 1995;23: 1535-1542.
79. Dercksen MW, Gerritsen WR, Rodenhuis S, Dirkson MK, Slaper-Cortenbach IC, Schaas-berg WP, Pinedo HM, von dem Borne AE, van-dcr Schoot CE: Expression of adhesion molecules on CD34+ cells: CD34+L-sclcctin+ predicts a rapid platelet recovery after peripheral blood stem cell transplantation. Blood 1995; 85:3313-3319.
80. Springer TA: Traffic signals for lymphocyte recirculation and leukocyte emigration: The multistep paradigm. Cell 1994;76:301-314.
81. Varki A: Selectin ligands. Proc Natl Acad Sci USA 1994;91:7390-7397.
82. Denkers IAM. De Jong-De BoerTJM, Beeline RHJ, Ossenkoppele GJ, Langenhuijsen MMAC: VLA molecule expression may be involved in the release of acute myeloid leu-kaemic cells from the bone marrow. Leuk Res 1992;16:469-474.
83. Folkman J, Shiy Y: Angiogcncsis. J Biol Chem 1992;267:10931-10934.
84. Iizuka Y, Aiso M, Oshimi K, Kanemaru M, Kawamura M, Takeuchi J, Horikoshi A, Oh-shima T, Mizoguchi H, Horic T: Myeloblastoma formation in acute myeloid leukemia. Leuk Res 1993;16:665-671.
85. Di Noto R, Schiavone EM, Ferrara F, Manzo C. Lo Pardo C, Del Vecchio L: Expression and ATRA-driven modulation of adhesion molecules in acute promyelocytic leukemia. Leukemia 1994:8:1900.
86. Stucki A, Cordey A-S. Monai N, Schapira M, Spcrtini O: Activation of vascular endothelial cells by leukemic blasts cells: A mechanism of leukostasis (abstract). Blood 1995,86:435. Torok-Storb B: Cellular interactions. Blood 1988;73:373-385.
87. Gordon MY, Dowding CR, Riley GR, Goldman JM. Greaves MF: Altered adhesive interactions with marrow stroma of hematopoietic progenitor cells in chronic myeloid leukemia. Nature 1987;328:342-344.
88. Bhatia R, Wayner EA, McGlave PB. Verfaillie CM: Interferon-alpha restores normal adhesion of chronic myelogenous leukemia hematopoietic progenitors to bone marrow stroma by correcting impaired (51 integrin receptor function. J Clin Invest 1994;94:384-394.
89. Renshaw MW, McWhirter FJ, Wang JY: The human leukemia oncogene bcr-abl abrogates the anchorage requirement but not the growth factor requirement for proliferation. Mol Cell Biol 1995;15:1286-1293.
90. Coulombel L, Eaves CJ, Kalousek KD, Gupta C, Eaves AC: Long term marrow culture of cells from patients with acute myelogenous leukemia (AML): Selection in favour of normal phenotypes in some but not all cases. J Clin Invest 1985;75:961-969.
91. Ways DK, Posekany K, deVente J, Garriw T, Chen J, Hooder J. Qin W, Cook P, Fletcher D, Parker P: Overexpression of protein kinase C-zcta stimulates leukemic cell differentiation. Cell Growth Differ 1994;5:1195-1203.
92. Haimovich B. Lipfert L, Brugge JS. Shattil SJ: Tyrosine phosphorylation and cytoskeletal reorganization in platelets are triggered by interaction of integrin receptors with their immobilized ligands. J Biol Chem 1993; 152: 3760-3767.
93. Kinashi T. Springer TA: Regulation of cell-matrix adhesion by receptor tyrosine kinases. Leuk Lymphoma 1995;18:203-308.
94. FAK in human hematopoietic cells, possibly through ‘inside-out’ signaling (abstract). Blood 1995; 86:253.
95. Bendall LJ, Daniel A, Kortlepel K, Gotlieb DJ: Bone marrow adherent layers inhibit apoptosis of acute myeloid leukemia cells. Exp Hematol 1994;22:1252-1260.
96. Watanabe H, Nakanishi I, Yamashita K. Hayakawa T, Okada Y: Matrix metallopro-teinase-9 (92 kDa gelatinase/type IV collage-nase) from U937 monoblastoid cells: Correlation with cellular invasion. J Cell Sci 1993; 104:991-999.
97. Janiak M, Hashmi HR, Janowska-Wieczorek A: Use of the matrigel-based assay to measure the invasivenesss of leukemic cells. Exp Hematol 1994;22:559-565.
98. Olive D, Lopez M, Blaise D. Viens P, Stoppa AM, Brandely M, Mawas C, Mannoni P, Ma-raninchi D: Cell surface expression of ICAM-1 (CD54) and LFA-3 (CD58), two adhesion molecules, is up-regulated on marrow leukemic blasts after in vivo administration of high-dose recombinant interleukin-2. J Im-munother 1991;10:412-417.
99. Bendall LJ, Kortlepel K, Gottlieb DJ: GM-CSF enhances IL-2-activatcd natural killer cell lysis of clonogenic AML cells by upregu-lating target cell expression of ICAM-1. Leukemia 1995;9:677-684.
100. Bendall LJ. Kortlepel K, Bradstock KF, Gottlieb DJ: Natural killer cells adhere to bone marrow fibroblasts and inhibit adhesion of acute myeloid leukemia cells. Leukemia 1995;9:999-1005.
101. Aoyagi M, Furusawa S, Waga K, Tsunogakc S, Shishido H: Suppression of normal hema-topoiesis in acute leukemia: Effect of leukemic cells on bone marrow stromal cells and hematopoietic progenitor cells. Intern Med 199;88:288-295.
102. Wetzler M, Estrov Z, Talpaz M, Kim KJ, Alphonso M, Srinivasan R, Kurzrock R: Leukemia inhibitory factor in long-term adherent layer culture: Increased levels of bioactive protein in leukemia and modulation by IL-4, IL-1 beta, and TNF-alpha. Cancer Res 1994; 54:1837-1842.
103. Kubota A, Okamura S, Shimoda K, Niho Y: Augmented production of interleukin 6 by co-culture of human bone marrow adherent cells and human leukemic cells. Biomed Pharma-cother 1993;47:379-384