Vascular smooth muscle differentiation of murine stroma: A sequential model

Experimental Hematology

Volumn 27, Issue 12, 1999, Pages 1782-1795

  Remy Martin, Jean Paul ^a   Marandin, Aliette ^a   Challier, Bruno ^a   Bernard, Gabrielle ^a   Deschaseaux, Marie ^a   Herve, Patrick ^a   Wei, Yanzhang ^b   Tsuji, Takashi ^c   Auerbach, Robert ^d   Dennis, James E ^e   Moore, Kateri A ^f   Greenberger, Joel S ^g   Charbord, Pierre ^a  

^a Institute Utinam   (France)

^b Dept of Microbiol and Molec Med ^*  (United States)

^c JT Inc   (Japan)

^d UNIVERSITY OF WISCONSIN MADISON   (United States)

^e CASE WESTERN RESERVE UNIVERSITY   (United States)

^f PRINCETON UNIVERSITY   (United States)

^g UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

Cytoskeleton; Extracellular matrix; Factor analysis; Marrow culture; Membrane antigens

Indexed keywords

ALPHA ACTIN; BETA ACTIN; CALDESMON; CD34 ANTIGEN; DESMIN; FIBRONECTIN; LAMININ; LY ANTIGEN; MEMBRANE ANTIGEN; MYOSIN; OSTEOPONTIN; THROMBOSPONDIN; THY 1 ANTIGEN; VASCULAR CELL ADHESION MOLECULE 1; VIMENTIN;

ANIMAL CELL; ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CELL LINE; EXTRACELLULAR MATRIX; IMMUNOFLUORESCENCE; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; STROMA CELL; WESTERN BLOTTING;

ANIMALS; BIOLOGICAL MARKERS; CELL DIFFERENTIATION; CELL LINE, TRANSFORMED; CYTOSKELETAL PROTEINS; EXTRACELLULAR MATRIX PROTEINS; HEMATOPOIESIS; HUMANS; MICE; MUSCLE, SMOOTH, VASCULAR; STROMAL CELLS;

MURINAE;

EID: 0032754348     PISSN: 0301472X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0301-472X(99)00122-8     Document Type: Article

References (77)

1. Dexter T.M., Allen T.D., Lajtha L.G. Conditions controlling the proliferation of haemopoietic stem cells in vitro. J Cell Physiol. 91:1976;335.
2. Gartner S., Kaplan H.S. Long-term culture of human bone marrow cells. Proc Natl Acad Sci U S A. 77:1980;4756.
3. Charbord P., Tamayo E., Saeland S., Duvert V., Poulet J., Gown A.M., Hervé P. Granulocyte-macrophage colony-stimulating factor (GM-CSF) in human long-term bone marrow cultures. endogeneous production in the adherent layer and effect of exogeneous GM-CSF on granulomonopoiesis Blood. 78:1991;1230.
4. Galmiche M.C., Koteliansky V.E., Hervé P., Charbord P. Stromal cells from human long-term marrow cultures are mesenchymal cells that differentiate following a vascular smooth muscle differentiation pathway. Blood. 82:1993;66.
5. Penn P.E., Jiang D.Z., Fei R.G., Sitnicka E., Wolf N.S. Dissecting the hematopoietic microenvironment. IX. Further characterization of murine bone marrow stromal cells. Blood. 81:1993;1205.
6. Moreau I., Duvert V., Caux C., Galmiche M.C., Charbord P., Banchereau J., Saeland S. Myofibroblastic stromal cells isolated from human bone marrow induce the proliferation of both early myeloid and B lymphoid cells. Blood. 82:1993;2396.
7. Li J., Sensebé L., Hervé P., Charbord P. Nontransformed colony-derived stromal cell lines from normal human marrows. III. The maintenance of hematopoiesis from CD. 34+(cell populations. Exp Hematol 25):1997;582.
8. Sitnicka E., Wang Q.R., Tsai S., Wolf N.S. Support versus inhibition of hematopoiesis by two characterized stromal cell types. Stem Cells. 13:1995;655.
9. Collins L.S., Dorshkind K. A stromal cell line from myeloid long-term bone marrow cultures can support myelopoiesis and B lymphopoiesis. J Immunol. 138:1987;1082.
10. Hunt P., Robertson D., Weiss D., Rennick D., Lee F., Witte O.N. A single bone marrow-derived stromal cell type supports the in vitro growth of early lymphoid and myeloid cells. Cell. 48:1987;997.
11. Friedrich C., Zausch E., Sugrue S.P., Gutierrez-Ramos J.C. Hematopoietic supportive functions of mouse bone marrow and fetal liver microenvironment. dissection of granulocyte, B-lymphocyte, and hematopoietic progenitor support at the stroma cell clone level Blood. 87:1996;4596.
12. Ohneda O., Yanai M., Obinata M. Microenvironment created by stromal cells is essential for a rapid expansion of erythroid cells in mouse fetal liver. Development. 110:1990;379.
13. Wineman J.P., Nishikawa S.I., Muller-Sieburg C.E. Maintenance of high levels of pluripotent hematopoietic stem cells in vitro. effect of stromal cells and c-kit Blood. 81:1993;365.
14. Wineman J.P., Moore K.A., Lemischka I.R., Muller-Sieburg C.E. Functional heterogeneity of the hematopoietic microenvironment. rare stromal elements maintain long-term repopulating stem cells Blood. 87:1996;4082.
15. Moore K.A., Ema H., Lemischka I.R. In vitro maintenance of highly purified, transplantable hematopoietic stem cells. Blood. 89:1997;4337.
16. Chiu C.P., Moulds C., Coffman R.L., Rennick D., Lee F. Multiple biological activities are expressed by a mouse interleukin 6 cDNA clone isolated from bone marrow stromal cells. Proc Natl Acad Sci U S A. 85:1988;7099.
17. Boswell H.S., Mochizuki D.Y., Burgess G.S., Gillis S., Walker E.B., Anderson D., Williams D.E. A novel mast cell growth factor (MCGF-3) produced by marrow-adherent cells that synergizes with interleukin 3 and interleukin 4. Exp Hematol. 18:1990;794.
18. Williams D.E., Eisenman J., Baird A., Rauch C., Van Bess K., March C.J., Park L.S., Martin U., Mochizucki D.Y., Boswell H.S., Burgess G.S., Cosman D., Lyman S.D. Identification of a ligand for the c-kit proto-oncogene. Cell. 63:1990;167.
19. Miyake K., Medina K.L., Hayashi S.I., Ono S., Hamaoka T., Kincade P.W. Monoclonal antibodies to Pgp-1/CD44 block lympho-hemopoiesis in long-term bone marrow cultures. J Exp Med. 171:1990;477.
20. Moore K.A., Pitowski B., Witte L., Hicklin D., Lemischka I.R. Hematopoietic activity of a stromal cell transmembrane protein containing epidermal growth factor-like repeat motifs. Proc Natl Acad Sci U S A. 94:1997;4011.
21. Baum C.M., Weissman I.L., Tsukamoto A.S., Buckle A.M., Peault B. Isolation of a candidate human hematopoietic stem-cell population. Proc Natl Acad Sci U S A. 89:1992;2804.
22. Isaad C., Croisille L., Katz A., Vainchenker W., Coulombel L. A murine stromal cell line allows the proliferation of very primitive human CD34++/CD38- progenitor cells in long-term cultures and semi-solid assays. Blood. 81:1993;2916.
23. Breems D.A., Blokland E.A.W., Neben S., Ploemacher R.E. Frequency analysis of human primitive haematopoietic stem cell subsets using a cobblestone area forming cell assay. Leukemia. 8:1994;1095.
24. Thiemann F.T., Moore K.A., Smogorzewska E.M., Lemischka I.R., Crooks G.M. The murine stromal cell lines AFT024 acts specifically on human CD34+CD38- progenitors to maintain primitive function and immunophenotype in vitro. Exp Hematol. 26:1998;612.
25. Miller J.S., McCullar V., Punzel M., Lemischka I.R., Moore K.A. Single adult human CD34+/lin-/CD38- progenitors give rise to natural killer cells, B-lineage cells, dendritic cells, and myeloid cells. Blood. 93:1999;96.
26. Anklesaria P., Kase K., Glowacki J., Holland C.A., Sakakeeny M.A., Wright J.A., Fitzgerald T.J., Lee C.Y., Greenberger J.S. Engraftment of a clonal bone marrow stromal cell line in vivo stimulates hematopoietic recovery from total body irradiation. Proc Natl Acad Sci U S A. 84:1987;7681.
27. Pietrangeli C.E., Hayashi S.I., Kincade P.W. Stromal cell lines which support lymphocyte growth. characterization, sensitivity to radiation and responsiveness to growth factors Eur J Immunol. 18:1988;863.
28. Peled A., Zipori D., Abramsky O., Ovadia H., Shezen E. Expression of alpha-smooth muscle actin in murine bone marrow stromal cells. Blood. 78:1991;304.
29. Montesano R., Pepper M.S., Möehle-Steinlein U., Risau W., Wagner E.F., Orci L. Increased proteolytic activity is responsible for the aberrant morphogenetic behavior of endothelial cells expressing the middle T oncogene. Cell. 62:1990;435.
30. Obeso J., Weber J., Auerbach R. A hemangioendothelioma-derived cell line. its use as a model for the study of endothelial cell biology Lab Invest. 63:1990;259.
31. Tsuji T., Ogasawara H., Aoki Y., Tsurumak Y., Kodama H. Characterization of murine stromal cell clones established from bone marrow and spleen. Leukemia. 10:1996;803.
32. Greenberger J.S., Sakakeeny M.A., Davis L.M., Moloney W.C., Reid D. Biologic properties of factor-independent non adherent hematopoietic and adherent preadipocyte cell lines derived from continuous bone marrow culture. Leuk Res. 8:1984;363.
33. Dorheim M.A., Sullivan M., Dandapani V., Wu X., Hudson J., Segarini P.R., Rosen D.M., Aulthouse A.L., Gimble J.M. Osteoblastic gene expression during adipogenesis in hematopoietic supporting murine bone marrow stromal cells. J Cell Physiol. 154:1993;317.
34. Smithson G., Medina K., Ponting I., Kincade P.W. Estrogen suppresses stromal cell-dependent lymphopoiesis in culture. J Immunol. 155:1995;3409.
35. Rennick D., Yang G., Gemmell L., Lee F. Control of hemopoiesis by a bone marrow stromal cell clone. lipopolysaccharide and interleukin-1 inducible production of colony-stimulating factors Blood. 69:1987;682.
36. Itoh K., Tezuka H., Sakoda H., Konno M., Nagata K., Uchiyama T., Uchino H., Mori K.J. Reproducible establishment of hemopoietic supportive stromal cell lines from murine bone marrow. Exp Hematol. 17:1989;145.
37. Lemoine F.M., Dedhar S., Lima G.M., Eaves C.J. Transformation-associated alterations in interactions between pre-B cells and fibronectin. Blood. 76:1990;2311.
38. Zipori D., Toledo J., von der Mark K. Phenotypic heterogeneity among stromal cell lines from mouse bone marrow disclosed in their extracellular matrix composition and interactions with normal and leukemic cells. Blood. 66:1985;447.
39. Benayahu D., Fried A., Zipori D., Wientroub S. Subpopulations of marrow stromal cells share a variety of osteoblastic markers. Calcif Tissue Int. 49:1991;202.
40. Pessina A., Neri M.G., Mineo E., Piccirillo M., Gribaldo L., Brambilla P., Zaleskis G., Ujhazy P. Expression of B cell markers on SR-4987 cells derived from murine bone marrow stroma. Exp Hematol. 25:1997;536.
41. Song Z.X., Shadduck R.K., Innes D.J., Waheed A. Jr., Quesenberry P.J. Hematopoietic factor production by a cell line (TC-1) derived from adherent murine marrow cells. Blood. 66:1985;273.
42. b-tsA58 transgenic mouse. Connect Tiss Res. 35:1996;93.
43. De Sauvage F., Carver-Moore K., Luoh S.M., Ryan A., Dowd M., Eaten D.L., Moore M.W. Physiological regulation of early and late stages of megakaryocytopoiesis by thrombopoietin. J Exp Med. 183:1996;651.
44. Toksoz D., Zsebo K.M., Smith K.A., Hu S., Brankow D., Suggs S.V., Martin F.H., Williams D.A. Support of human hematopoiesis in long-term bone marrow cultures by murine stromal cells selectively expressing the membrane-bound and secreted forms of the human homolog of the steel gene product, stem cell factor. Proc Natl Acad Sci U S A. 89:1992;7350.
45. Wei Y., Quertermous T., Wagner T.E. Directed endothelial differentiation of cultured embryonic yolk sac cells in vivo provides a novel cell-based system for gene therapy. Stem Cells. 13:1995;541.
46. Wang S.J., Greer P., Auerbach R. Isolation and propagation of yolk-sac-derived endothelial cells from a hypervascular transgenic mouse expressing a gain of function FPS/FES proto-oncogene. In Vitro Cell Dev Biol Animal. 32:1996;292.
47. Yoder M.C., Papaioannou V.E., Breitfeld P.P., Williams D.A. Murine yolk sac endoderm- and mesoderm-derived cell lines support in vitro growth and differentiation of hematopoietic cells. Blood. 83:1994;2436.
48. Hourdillé P., Hasitz M., Belloc F., Nurden A.T. Immunocytochemical study of the binding of fibrinogen and thrombospondin to ADP- and thrombin-stimulated human platelets. Blood. 65:1985;912.
49. Cavaillé F., Fournier T., Dallot E., Dhellemes C., Ferré F. Myosin heavy chain isoform expression in human myometrium. presence of an embyronic nonmuscle isoform in leiomyomas and in cultured cells Cell Motil Cytoskel. 30:1995;183.
50. Benzonana G., Skalli O., Gabbiani G. Correlation between the distribution of smooth muscle or non muscle myosins and α-smooth muscle actin in normal and pathological soft tissues. Cell Motil Cytoskeleton. 11:1988;260.
51. Hungerford J.E., Hoeffler J.P., Bowers C.W., Dahm L.M., Falchetto R., Shabanowitz J., Hunt D.F., Little C.D. Identification of a novel marker for primordial smooth muscle and its differential expression pattern in contractile vs noncontractile cells. J Cell Biol. 137:1997;925.
52. Sensebé L., Deschaseaux M., Li J., Hervé P., Charbord P. The broad spectrum of cytokine gene expression by myoid cells from the human marrow microenvironment. Stem Cells. 15:1996;133.
53. Solway J., Seltzer J., Samaha F.F., Kim S., Alger L.E., Niu Q., Morrisey E.E., Ip H.S., Parmacek M.S. Structure and expression of a smooth muscle cell-specific gene, SM22α J Biol Chem. 270:1995;13460.
54. Whitlock C.A., Tidmarsh G.F., Muller-Sieburg C., Weissman I.L. Bone marrow stromal cell lines with lymphopoietic activity express high levels of a pre-B neoplasia-associated molecule. Cell. 48:1987;1009.
55. Sappino A.P., Schurch W., Gabbiani G. Biology of disease. Differentiation repertoire of fibroblastic cells. expression of cytoskeletal proteins as marker of phenotypic modulations Lab Invest. 63:1990;144.
56. Cooper A.R., MacQueen H.A. Subunits of laminin are differentially synthesized in mouse eggs and early embryos. Dev Biol. 96:1983;467.
57. Thomas T., Dziadek M. Genes coding for basement membrane glycoproteins laminin, nidogen, and collagen IV are differentially expressed in the nervous system and by epithelial, endothelial, and mesenchymal cells of the mouse embryo. Exp Cell Res. 208:1993;54.
58. Hynes R (1989) Fibronectins. New York: Springer Verlag.
59. Schwartz S.M. Smooth muscle migration in atherosclerosis and restenosis. J Clin Invest. 99:1997;2814.
60. Gluckhova M., Koteliansky V. Integrins, cytoskeletal and extracellular matrix proteins in developing smooth muscle cells of human aorta. Schwarz S.M., Mecham R.P. The vascular smooth muscle cell. 1995;Academic Press, San Diego. 37p.
61. Li J., Sensebé L., Hervé P., Charbord P. Non-transformed colony-derived stromal cell lines from normal human marrows. II. Phenotypic characterization and differentiation pathway. Exp Hematol. 23:1995;133.
62. Raugi G.J., Mumby S.M., Abbott-Brown D., Bornstein P. Thrombospondin. synthesis and secretion by cells in culture J Cell Biol. 95:1982;351.
63. Miano J.M., Vlasic N., Tota R.R., Stemerman M.B. Smooth muscle cell immediate-early gene and growth factor activation follows vascular injury. A putative in vivo mechanism for autocrine growth. Arterioscler Thromb. 13:1993;211.
64. Majack R.A., Goodman L.V., Dixit V.M. Cell surface thrombospondin is functionally essential for vascular smooth muscle cell proliferation. J Cell Biol. 106:1988;415.
65. Yabkowitz R., Mansfield P.J., Ryan U.S., Suchard S.F. Thrombospondin mediates migration and potentiates platelet-derived growth factor-dependent migration of calf pulmonary artery smooth muscle cells. J Cell Physiol. 157:1993;24.
66. Owens G.K. Regulation of differentiation of vascular smooth muscle cells. Physiol Rev. 75:1995;487.
67. Izon D.J., Oritani K., Hamel M., Revilla Calvo C., Boyd R.L., Kincade P.W., Kruisbeek A.D. Identification and functional analysis of Ly-6A/E as a thymic and bone marrow stromal antigen. J Immunol. 156:1996;2391.
68. Satoh M., Mioh H., Shiotsu Y., Ogawa Y., Tamaoki T. Mouse bone marrow stromal cell line MC3T3-G2/PA6 with hematopoietic-supporting activity expresses high levels of stem cell antigen Sca-1. Exp Hematol. 25:1997;972.
69. Krause D.S., Ito T., Fackler M.J., Smith O.M., Collector M.I., Sharkis S.J., Stratford May W. Characterization of murine CD34, a marker for hematopoietic progenitor and stem cells. Blood. 84:1994;691.
70. Lin G., Finger E., Gutierrez-Ramos J.C. Expression of CD34 in endothelial cells, hematopoietic progenitors and nervous cells in fetal and adult mouse tissues. Eur J Immunol. 25:1995;1508.
71. Kinashi T., St. Pierre Y., Springer T.A. Expression of glycophosphatidylinositol-anchored and -non-anchored isoforms of vascular cell adhesion molecule 1 in murine stromal and endothelial cells. J Leukoc Biol. 37:1995;168.
72. Yanai T., Sekine C., Yagita H., Obinata M. Roles for integrin very late activation antigen-4 in stroma-dependent erythropoiesis. Blood. 10:1994;2844.
73. Van de Rijn M., Heimfeld S., Spangrude G.J., Weissman I.L. Mouse hematopoietic stem-cell antigen Sca-1 is a member of the Ly-6 antigen family. Proc Natl Acad Sci U S A. 86:1989;4634.
74. Maximow A.A. Relation of blood cells to connective tissues and endothelium. Physiol Rev. 4:1924;533.
75. Caplan A.I. Mesenchymal stem cells. J Orthop Res. 9:1991;641.
76. Gimble J.M., Robinson C.E., Wu X., Kelly K. The function of adipocytes in the bone marrow stroma. an update Bone. 19:1996;421.
77. Knospe W.H., Husseini S.G., Zipori D., Fried W. Hematopoiesis on cellulose ester membrane. XIII. A combination of cloned stromal cells is needed to establish a hematopoietic microenvironment supportive of trilineal hematopoiesis. Exp Hematol. 21:1993;257.