Matrix metalloproteinase and tissue inhibitors of metalloproteinase secretion by haematopoietic and stromal precursors and their production in normal and leukaemic long-term marrow cultures
L. A. Marquez-Curtis,
A. Dobrowsky, J. Montaño, A. R. Turner,
J. Ratajczak,
M. Z. Ratajczak,
A. Janowska-Wieczorek,
L. A. Marquez-Curtis
Canadian Blood Services, Edmonton, Alberta,
Search for more papers by this authorA. R. Turner
Department of Medicine, University of Alberta, Canada,
Search for more papers by this authorJ. Ratajczak
Department of Pathology and Laboratory Medicine, University of Pennsylvania, PA, USA, and
Search for more papers by this authorM. Z. Ratajczak
Department of Pathology and Laboratory Medicine, University of Pennsylvania, PA, USA, and
James Graham Brown Cancer Center, University of Louisville, Louisville, KY, USA
Search for more papers by this authorA. Janowska-Wieczorek
Canadian Blood Services, Edmonton, Alberta,
Department of Medicine, University of Alberta, Canada,
Search for more papers by this authorL. A. Marquez-Curtis,
A. Dobrowsky, J. Montaño, A. R. Turner,
J. Ratajczak,
M. Z. Ratajczak,
A. Janowska-Wieczorek,
L. A. Marquez-Curtis
Canadian Blood Services, Edmonton, Alberta,
Search for more papers by this authorA. R. Turner
Department of Medicine, University of Alberta, Canada,
Search for more papers by this authorJ. Ratajczak
Department of Pathology and Laboratory Medicine, University of Pennsylvania, PA, USA, and
Search for more papers by this authorM. Z. Ratajczak
Department of Pathology and Laboratory Medicine, University of Pennsylvania, PA, USA, and
James Graham Brown Cancer Center, University of Louisville, Louisville, KY, USA
Search for more papers by this authorA. Janowska-Wieczorek
Canadian Blood Services, Edmonton, Alberta,
Department of Medicine, University of Alberta, Canada,
Search for more papers by this author Dr Anna Janowska-Wieczorek, Department of Medicine, University of Alberta, CBS Building, 8249–114 Street, Edmonton, Alberta, Canada. E-mail: [email protected]
Abstract
Matrix metalloproteinases (MMPs) and tissue inhibitors of metalloproteinases (TIMPs) regulate the turnover of the extracellular matrix and may modulate the biology of haematopoietic cells. We investigated whether MMPs and TIMPs are produced in long-term marrow cultures (LTMCs) established from normal donors and acute myelogenous leukaemia (AML) patients, and by fibroblast- (F), granulocyte macrophage- (GM) and megakaryocyte- (Meg) colony-forming unit (CFU) and erythroid burst-forming unit (BFU-E)-derived precursor cells. ProMMP-9 levels were highest (> 400 ng/ml) at week 1 of normal LTMC, whereas proMMP-2, TIMP-1, TIMP-2 and TIMP-3 levels peaked (up to 1000 ng/ml) after the establishment of the adherent layer. In LTMC from AML patients, these patterns of secretion were reversed. Moreover, we found that after a 24 h incubation in serum-free media, normal CFU-GM-, BFU-E- and CFU-Meg-derived cells secreted proMMP-9 and CFU-F-derived cells proMMP-2, in contrast to cells from LTMC adherent layer which secreted both active and latent forms of MMP-2 and MMP-9 under serum-free conditions. However, when these adherent cells were incubated in 12·5% fetal calf or horse serum or complete LTMC growth media, active forms of MMP-2 and MMP-9 were no longer detectable, and TIMP levels increased. Hence, we concluded that (i) MMPs/TIMPs are secreted by normal human bone marrow haematopoietic and stromal cells and may play an important role in intercellular cross-talk in haematopoiesis; and (ii) only latent forms of MMPs are present under LTMC conditions, indicating that the specific media used for weekly re-feeding of LTMC can block activation of MMP-2 and MMP-9, maintaining the integrity of the stromal layer and supporting haematopoiesis in vitro.
References
- Alexander, C.M., Hansell, E.J., Behrendtsen, O., Flannery, M.L., Kishnani, N.S., Hawkes, S.P., Werb, Z. (1996) Expression and function of matrix metalloproteinases and their inhibitors at the maternal–embryonic boundary during mouse embryo implantation. Development, 122, 1723–1736.
- Baker, A.H., George, S.J., Zaltsman, A.B., Murphy, G., Newby, A.C. (1999) Inhibition of invasion and induction of apoptotic cell death of cancer cell lines by overexpression of TIMP-3. British Journal of Cancer, 79, 1347–1355.
- Bond, M., Murphy, G., Bennett, M.R., Amour, A., Knauper, V., Newby, A.C., Baker, A.H. (2000) Localization of the death domain of tissue inhibitor of metalloproteinase-3 to the N terminus. Journal of Biological Chemistry, 275, 41358–41363.
- Borland, G., Murphy, G., Ager, A. (1999) Tissue inhibitor of metalloproteinases-3 inhibits shedding of 1-selectin from leukocytes. Journal of Biological Chemistry, 274, 2810–2815.
- Brew, K., Dinakarpandian, D., Nagase, H. (2000) Tissue inhibitors of metalloproteinases: evolution, structure and function. Biochimica et Biophysica Acta, 1477, 267–283.
- Casey, T.M., Boecker, A., Chiu, J.F., Plaut, K. (2000) Glucocorticoids maintain the extracellular matrix of differentiated mammary tissue during explant and whole organ culture. Proceedings of the Society of Experimental Biology and Medicine, 224, 76–86.
- Chan, J.Y. & Watt, S.M. (2001) Adhesion receptors on haematopoietic progenitor cells. British Journal of Haematology, 112, 541–557.
- Coulombel, L., Eaves, A.C., Eaves, C.J. (1983) Enzymatic treatment of long-term marrow culture reveals the preferential location of primitive hemopoietic progenitors in the adherent layer. Blood, 62, 291–297.
- Dexter, T.M., Allen, T.D., Lajtha, L.G. (1977) Conditions controlling the proliferation of haemopoietic stem cells in vitro. Journal of Cell Physiology, 91, 335–344.
- Fassina, G., Ferrari, N., Brigati, C., Benelli, R., Santi, L., Noonan, D.M., Albini, A. (2000) Tissue inhibitors of metalloproteases: regulation and biological activities. Clinical and Experimental Metastasis, 18, 111–120.
- Forget, M.A., Desrosiers, R.R., Beliveau, R. (1999) Physiological roles of matrix metalloproteinases: implications for tumor growth and metastasis. Canadian Journal of Physiology and Pharmacology, 77, 465–480.DOI: 10.1139/cjpp-77-7-465
- George, S.J., Lloyd, C.T., Angelini, G.D., Newby, A.C., Baker, A.H. (2000) Inhibition of late vein graft neointima formation in human and porcine models by adenovirus-mediated overexpression of tissue inhibitor of metalloproteinase-3. Circulation, 101, 296–304.
- Gomez, D.E., Alonso, D.F., Yoshiji, H., Thorgeirsson, U.P. (1997) Tissue inhibitors of metalloproteinases: structure, regulation and biological functions. European Journal of Cell Biology, 74, 111–122.
-
Gomez-Morales, E.,
Martinez-Jaramillo, G.,
Sanchez-Valle, E.,
Valencia-Plata, I.,
Arana-Trejo, R.M.,
Castro, M.A.,
Pizzuto-Chavez, J.,
Mayani, H. (1998) Deficient proliferation of myeloid, erythroid, and multipotent progenitor cells in long-term marrow cultures from patients with aplastic anemia treated with immunosuppressive therapy.
American Journal of Hematology, 59, 149–155.
10.1002/(SICI)1096-8652(199810)59:2<149::AID-AJH8>3.0.CO;2-Y CAS PubMed Web of Science® Google Scholar
- Greenberger, J. (1991) The hemopoietic microenvironment. Critical Reviews in Oncology/Hematology, 8, 65–84.
- Greenberger, J.S. (1978) Sensitivity of corticosteroid-dependent insulin-resistant lipogenesis in marrow preadipocytes of obese-diabetic (db/db) mice. Nature, 275, 752–754.
- Guedez, L., Mansoor, A., Birkedal-Hansen, B., Lim, M.S., Fukushima, P., Venzon, D., Stetler-Stevenson, W.G., Stetler-Stevenson, M. (2001) Tissue inhibitor of metalloproteinases 1 regulation of interleukin-10 in B-cell differentiation and lymphomagenesis. Blood, 97, 1796–1802.
- Haas, T.L., Davis, S.J., Madri, J.A. (1998) Three-dimensional type I collagen lattices induce coordinate expression of matrix metalloproteinases MT1-MMP and MMP-2 in microvascular endothelial cells. Journal of Biological Chemistry, 273, 3604–3610.
- Janowska-Wieczorek, A., Mannoni, P., Turner, A.R., McGann, L.E., Shaw, A.R.E., Turc, J.M. (1984) Monoclonal antibody specific for granulocytic lineage cells and reactive with human pluripotent and committed haematopoietic progenitor cells. British Journal of Haematology, 58, 159–168.
- Janowska-Wieczorek, A., Mayani, H., Shen, S., Tupas, J., Belch, A.R., Morrish, D.W., Miller, G.G., Turner, A.R. (1991) Similarities in long-term cultures of blood and bone marrow from patients with acute myelogenous leukemia. International Journal of Cell Cloning, 9, 461–473.
- Janowska-Wieczorek, A., Marquez, L.A., Matsuzaki, A., Hashmi, H.R., Larratt, L.M., Boshkov, L.M., Turner, A.R., Zhang, M.C., Edwards, D.R., Kossakowska, A.E. (1999a) Expression of matrix metalloproteinases (MMP-2 and -9) and tissue inhibitors of metalloproteinases (TIMP-1 and -2) in acute myelogenous leukaemia blasts: comparison with normal bone marrow cells. British Journal of Haematology, 105, 402–411.
- Janowska-Wieczorek, A., Marquez, L.A., Nabholtz, J.-M., Cabuhat, M.L., Montaño, J., Chang, H., Rozmus, J., Russell, J.A., Edwards, D.R., Turner, A.R. (1999b) Growth factors and cytokines upregulate gelatinase expression in bone marrow CD34+ cells and their transmigration through reconstituted basement membrane. Blood, 93, 3379–3390.
- Janowska-Wieczorek, A., Matsuzaki, A., Marquez, L.A. (2000a) Matrix metalloproteinases in the hematopoietic microenvironment. Hematology, 4, 515–527.
- Janowska-Wieczorek, A., Marquez, L.A., Dobrowsky, A., Ratajczak, M.Z., Cabuhat, M.L. (2000b) Differential MMP and TIMP production by human marrow and peripheral blood CD34+ cells in response to chemokines. Experimental Hematology, 28, 1274–1285.DOI: 10.1016/s0301-472x(00)00532-4
- Klein, G. (1995) The extracellular matrix of the hematopoietic microenvironment. Experientia, 51, 914–922.
- Kossakowska, A.E., Edwards, D.R., Prusinkiewicz, C., Zhang, M.C., Guo, D., Urbanski, S.J., Grogan, T., Marquez, L.A., Janowska-Wieczorek, A. (1999) Interleukin-6 regulation of matrix metalloproteinases (MMP-2 and MMP-9) and tissue inhibitor of metalloproteinase (TIMP-1) expression in malignant non-Hodgkin's lymphomas. Blood, 94, 2080–2089.
- Lee, B., Ratajczak, J., Doms, R.W., Gewirtz, A.M., Ratajczak, M.Z. (1999) Coreceptor/chemokine receptor expression on human hematopoietic cells: biological implications for human immunodeficiency virus-type 1 infection. Blood, 93, 1145–1156.
- Lenz, O., Elliot, S.J., Stetler-Stevenson, W.G. (2000) Matrix metalloproteinases in renal development and disease. Journal of the American Society of Nephrology, 11, 1–15.
- Lim, M.S., Guedez, L., Stetler-Stevenson, W.G., Stetler-Stevenson, M. (1999) Tissue inhibitor of metalloproteinase-2 induces apoptosis in human T lymphocytes. Annals of the New York Academy of Science, 878, 522–523.
- Majka, M., Janowska-Wieczorek A., Ratajczak, J., Ehrenman, K., Pietrzkowski, Z., Kowalska, A., Gewirtz, A.M., Emerson, S.G., Ratajczak, M.Z. (2001) Numerous growth factors, cytokines, and chemokines are secreted by human CD34+ cells, myeloblasts, erythroblasts, and megakaryoblasts and regulate normal hematopoiesis in an autocrine/paracrine manner. Blood, 97, 3075–3085.
- Mayani, H., Guilbert, L.J., Clark, S.C., Janowska-Wieczorek, A. (1991) Inhibition of hematopoiesis in normal human long-term marrow cultures treated with recombinant human macrophage colony-stimulating factor. Blood, 78, 651–657.
- Mayani, H., Guilbert, L.J., Janowska-Wieczorek, A. (1990) Modulation of erythropoiesis and myelopoiesis by exogenous erythropoietin in human long-term marrow culture. Experimental Hematology, 18, 174–179.
- Mayani, H., Guilbert, L.J., Janowska-Wieczorek, A. (1992) Biology of the hemopoietic microenvironment. European Journal of Haematology, 49, 225–233.
- Metcalf, D. (1998) Regulatory mechanisms controlling hematopoiesis: principles and problems. Stem Cells, 16, 3–11.
- Morgunova, E., Tuuttila, A., Bergmann, U., Isupov, M., Lindqvist, Y., Schneider, G., Tryggvason, K. (1999) Structure of human pro-matrix metalloproteinase-2: activation mechanism revealed. Science, 284, 1667–1670.DOI: 10.1126/science.284.5420.1667
- Murphy, G., Stanton, H., Cowell, S., Butler, G., Knauper, V., Atkinson, S., Gavrilovic, J. (1999) Mechanisms for pro matrix metalloproteinase activation. APMIS, 107, 38–44.
- Nagase, H. & Woessner, Jr, J.F. (1999) Matrix metalloproteinases. Journal of Biological Chemistry, 274, 21491–21494.
- Oliver, G.W., Leferson, J.D., Stetler-Stevenson, W.G., Kleiner, D.E. (1997) Quantitative reverse zymography: analysis of picogram amounts of metalloproteinase inhibitors using gelatinase A and B reverse zymograms. Analytical Biochemistry, 244, 161–166.DOI: 10.1006/abio.1996.9895
- Park, M.T., Cha, H.J., Jeong, J.W., Kim, S.I., Chung, H.Y., Kim, N.D., Kim, O.H., Kim, K.W. (1999) Glucocorticoid receptor-induced down-regulation of MMP-9 by ginseng components, PD and PT contributes to inhibition of the invasive capacity of HT1080 human fibrosarcoma cells. Molecular Cells, 9, 476–483.
- Preiksaitis, J.K. & Janowska-Wieczorek, A. (1991) Persistence of cytomegalovirus in human long-term bone marrow culture: Relationship to hemopoiesis. Journal of Medical Virology, 35, 76–84.
-
Quesenberry, P.J. (1989) Stromal cells in long-term bone marrow cultures. In: Handbook of the Hemopoietic Microenvironment (ed. by M. Tavassoli), pp. 253–285. Humana Press, New Jersey.
10.1007/978-1-4612-4494-3_7 Google Scholar
- Seltzer, J.L., Horan, T.P., Eisen, A.Z. (1983) Regulation of gelatinase in human skin organ cultures by glucocorticoids. Journal of Investigative Dermatology, 80, 42s–43s.
- Seltzer, J.L., Lee, A.Y., Akers, K.T., Sudbeck, B., Southon, E.A., Wayner, E.A., Eisen, A.Z. (1994) Activation of 72-kDa type IV collagenase/gelatinase by normal fibroblasts in collagen lattices is mediated by integrin receptors but is not related to lattice contraction. Experimental Cell Research, 213, 365–374.DOI: 10.1006/excr.1994.1211
- Stetler-Stevenson, W.G., Bersch, N., Golde, D.W. (1992) Tissue inhibitor of metalloproteinase-2 (TIMP-2) has erythroid-potentiating activity. FEBS Letters, 296, 231–234.
- Streuli, C. (1999) Extracellular matrix remodelling and cellular differentiation. Current Opinion in Cell Biology, 11, 634–640.DOI: 10.1016/s0955-0674(99)00026-5
- Sugiura, Y., Shimada, H., Seeger, R.C., Laug, W.E., DeClerck, Y.A. (1998) Matrix metalloproteinase-2 and -9 are expressed in human neuroblastoma: contribution of stromal cells to their production and correlation with metastasis. Cancer Research, 58, 2209–2216.
-
Tavassoli, M. (1989) Handbook of the Hemopoietic Microenvironment. Humana Press, New Jersey.
10.1007/978-1-4612-4494-3_4 Google Scholar
- Tennant, G.B., Walsh, V., Truran, L.N., Edwards, P., Mills, K.I., Burnett, A.K. (2000) Abnormalities of adherent layers grown from bone marrow of patients with myelodysplasia. British Journal of Haematology, 111, 853–862.DOI: 10.1046/j.1365-2141.2000.02467.x
- Verfaillie, C., Hurley, R., Bhatia, R., McCarthy, J. (1994) Role of bone marrow matrix in normal and abnormal hematopoiesis. Critical Reviews in Oncology/Hematology, 16, 201–224.
- Werb, Z. (1997) ECM and cell surface proteolysis: Regulating cellular ecology. Cell, 91, 439–442.
- Westermarck, J. & Kahari, V.-M. (1999) Regulation of matrix metalloproteinase expression in tumor invasion. FASEB Journal, 13, 781–792.
- Wlodarski, K., Jakobisiak, M., Janowska-Wieczorek, A. (1980) Heterotopically induced bone marrow formation: morphology and transplantation. Experimental Hematology, 8, 1016–1023.
- Wong, H., Anderson, W.D., Cheng, T., Riabowol, K.Y. (1994) Monitoring mRNA expression by polymerase chain reaction: The ‘primer-dropping’ method. Analytical Biochemistry, 223, 251–258.DOI: 10.1006/abio.1994.1581
- Zhang, W., Knieling, G., Vohwinkel, G., Martinez, T., Kuse, R., Hossfeld, D.K., Duhrsen, U. (1999) Origin of stroma cells in long-term bone marrow cultures from patients with acute myeloid leukemia. Annals in Hematology, 78, 305–314.
- Zuckerman, K.S., Rhodes, R.K., Goodrum, D.D., Patel, V.R., Sparks, B., Wells, J., Wicha, M.S., Mayo, L.A. (1985) Inhibition of collagen deposition in the extracellular matrix prevents the establishment of a stroma supportive of hematopoiesis in long-term murine bone marrow cultures. Journal of Clinical Investigation, 75, 970–975.
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