Unique human CD133+ leukemia cell line and its modulation towards a mesenchymal phenotype by FGF2 and TGFβ1

Journal of Cellular Physiology

Volumn 206, Issue 3, 2006, Pages 682-692

  Bodo, Maria ^a   Baroni, Tiziano ^a   Bellucci, Catia ^a   Lilli, Cinzia ^a   De Ioanni, Maria ^a   Bonifacio, Elisabetta ^a   Moretti, Lorenzo ^a   Becchetti, Ennio ^a   Bellocchio, Silvia ^a   Delfini, Costante ^b   Lumare, Eleonora ^c   Tabilio, Antonio ^a  

^a UNIVERSITY OF PERUGIA   (Italy)

^b SAN SALVATORE HOSPITAL   (Italy)

^c UNIVERSITY OF FERRARA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

BETA GLYCAN PROTEOGLYCAN; BETA1 INTEGRIN; BIGLYCAN; CD133 ANTIGEN; CD14 ANTIGEN; CD34 ANTIGEN; CD36 ANTIGEN; CD38 ANTIGEN; CD45 ANTIGEN; CD71 ANTIGEN; CELL MARKER; COLLAGEN TYPE 1; COLLAGEN TYPE 3; COLLAGENASE; ENDOGLIN; FIBROBLAST GROWTH FACTOR 2; FIBRONECTIN; GLYCOSAMINOGLYCAN; GROWTH FACTOR RECEPTOR; HERMES ANTIGEN; HLA DR ANTIGEN; INTERCELLULAR ADHESION MOLECULE 1; MESSENGER RNA; OSTEOCALCIN; PROTEIN P75; PROTEIN P75 LNGFR; PROTEOGLYCAN; TRANSCRIPTION FACTOR RUNX2; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG;

ACUTE LYMPHOBLASTIC LEUKEMIA; ARTICLE; AUTOCRINE EFFECT; CANCER CELL CULTURE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL STRAIN GM 490; CONTROLLED STUDY; CULTURE MEDIUM; EXTRACELLULAR MATRIX; GENE EXPRESSION; HEMATOLOGIC DISEASE; HUMAN; HUMAN CELL; LEUKEMIA CELL LINE; MESENCHYME CELL; NUCLEOTIDE SEQUENCE; OSTEOBLAST; PHENOTYPE; PRIORITY JOURNAL; PROTEIN SYNTHESIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STEM CELL;

ANIMALS; ANTIGENS, CD; BONE MARROW CELLS; CELL DIFFERENTIATION; CELL LINE, TUMOR; CELL PROLIFERATION; COLLAGEN; COLLAGENASES; COLONY-FORMING UNITS ASSAY; CORE BINDING FACTOR ALPHA 1 SUBUNIT; FIBROBLAST GROWTH FACTOR 2; FIBRONECTINS; GLYCOPROTEINS; GLYCOSAMINOGLYCANS; HUMANS; LEUKEMIA, LYMPHOCYTIC, ACUTE; MESENCHYMAL STEM CELLS; OSTEOCALCIN; PEPTIDES; RECEPTOR, FIBROBLAST GROWTH FACTOR, TYPE 2; RECEPTOR, NERVE GROWTH FACTOR; RNA, MESSENGER; TRANSFORMING GROWTH FACTOR BETA;

EID: 31944448892     PISSN: 00219541     EISSN: None     Source Type: Journal    
DOI: 10.1002/jcp.20517     Document Type: Article

References (74)

1. Abkowitz JL, Robinson AE, Kale S, Long MW, Chen J. 2003. Mobilization of hematopoietic stem cells during homeostasis and after cytokine exposure. Blood 102:1249-1253.
2. Aral F, Hirao A, Suda T. 2005. Regulation of hematopoietic stem cells by the niche. Trends Cardiovasc Med 15:75-79.
3. Auffray I, Chevalier S, Froger J, Izac B, Vainchenker W, Gascan H, Coulombel L. 1996. Nerve growth factor is involved in the supportive effect by bone marrow-derived stromal cells of the factor-dependent human cell line UT-7. Blood 88: 1608-1618.
4. Bae SC, Lee KS, Zhang YW, Ito Y. 2001. Intimate relationship between TGF-beta/BMP signaling and runt domain transcription factor, PEBP2/CBF. J Bone Joint Surg Am 83-A(Suppl 1) (Pt 1):S48-S55.
5. Balduino A, Hurtado SP, Frazao P, Takiya CM, Alves LM, Nasciutti LE, El-Cheikh MC, Borojevic R. 2005. Bone marrow subendosteal microenvironment harbours functionally distinct haemosupportive stromal cell populations. Cell Tissue Res 319:255-266.
6. Bianchi G, Banfi A, Mastrogiacomo M, Notaro R, Luzzatto L, Cancedda R, Quarto R. 2003. Ex vivo enrichment of mesenchymal cell progenitors by fibroblast growth factor 2. Exp Cell Res 287:98-105.
7. Bikfalvi A, Klein S, Pintucci G, Rifkin DB. 1997. Biological roles of fibroblast growth factor-2. Endocr Rev 18:26-45.
8. Bjornson CR, Rietze RL, Reynolds BA, Magli MC, Vescovi AL. 1999. Turning brain into blood: A hematopoietic fate adopted by adult neural stem cells in vivo. Science 283:534-537.
9. Bodo M, Pezzetti F, Baroni T, Carinci F, Arena N, Nicoletti I, Becchetti E. 1993. Hyaluronic acid modulates growth, morphology and cytoskeleton in embryonic chick skin fibroblasts. Int J Dev Biol 37:349-352.
10. Carion A, Benboubker L, Herault O, Roingeard F, Degenne M, Senecal D, Desbois I, Colombat P, Charbord P, Binet C, Domenech J. 2003. Stromal-derived factor 1 and matrix metalloproteinase 9 levels in bone marrow and peripheral blood of patients mobilized by granulocyte colony-stimulating factor and chemotherapy. Relationship with mobilizing capacity of haematopoietic progenitor cells. Br J Heamatol 122:918-926.
11. Carlo-Stella C, Mangoni L, Piovani G, Garau D, Almici C, Rizzoli V. 1994. Identification of Philadelphia-negative granulocyte-macrophage colony-forming units generated by stroma-adherent cells from chronic myelogenous leukemia patients. Blood 83:1373-1380.
12. Cattoretti G, Schiro R, Orazi A, Soligo D, Colombo MP. 1993. Bone marrow stroma in humans: Anti-nerve growth factor receptor antibodies selectively stain reticular cells in vivo and in vitro. Blood 81:1726-1738.
13. Chikazu D, Katagiri M, Ogasawara T, Ogata N, Shimoaka T, Takato T, Nakamura K, Kawaguchi H. 2001. Regulation of osteoclast differentiation by fibroblast growth factor 2: Stimulation of receptor activator of nuclear factor KappaB ligand/osteoclast differentiation factor expression in osteoblasts and inhibition of macrophage colony-stimulating factor function in osteoclast precursors. J Bone Miner Res 16:2074-2081.
14. Chomczynski P, Sacchi N. 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162: 156-159.
15. Conrad GW, Hamilton C, Haynes E. 1977. Differences in glycosaminoglycans synthesized by fibroblast-like cells from chick cornea, heart, and skin. J Biol Chem 252:6861-6870.
16. Cornet F, Anselme K, Grard T, Rouahi M, Noel B, Hardouin P, Jeanfils J. 2002. The influence of culture conditions on extracellular matrix proteins synthesized by osteoblasts derived from rabbit bone marrow. J Biomed Mater Res 63: 400-407.
17. Delfini C, Tabilio A, Falzetti F, Centis F, Annibali M. 1995. A human non-hematopoietic cell line expressing thrombosponding receptor (CD36): Preliminary characterization. Exp Hematol 23:101.
18. Delfini C, Centis F, Falzetti F, Tabilio A. 2002. Expression of CD133 on a human cell line lacking CD34. Leukemia 16:2174-2175.
19. Dubois CM, Ruscetti FW, Stankova J, Keller JK. 1994. Transforming growth factor-beta regulates c-kit message stability and cell-surface protein expression in hematopoietic progenitors. Blood 83:3138-3145.
20. Engvall E, Ruoslahti E. 1977. Binding of soluble form of fibroblast surface protein, fibronectin, to collagen. Int J Cancer 20:1-5.
21. Erdman R, Stahl RC, Rothblum K, Chernousov MA, Carey DJ. 2002. Schwann cell adhesion to a novel heparan sulfate binding site in the N-terminal domain of alpha 4 type V collagen is mediated by syndecan-3. J Biol Chem 277:7619-7625.
22. Faham S, Hileman RE, Fromm JR, Rees DC. 1996. Heparin structure and interactions with basic fibroblast growth factor. Science 271:1116-1120.
23. Fannon M, Forsten KE, Nugent MA. 2000. Potentiation and inhibition of bFGF binding by heparin: A model for regulation of cellular response. Biochemistry 39:1434-1445.
24. Fried J, Perez AG, Clarkson BD. 1978. Rapid hypotonic method for flow cytofluorometry of monolayer cell culture. Some pitfalls in staining and data analysis. J Histoch Cytoch 26:921-933.
25. Gomez-Pinilla F, Miller S, Choi J, Cotman CW. 1997. Heparan sulfate potetiates the autocrine action of basic fibroblast growth factor in astrocytes: An in vivo and in vitro study. Neuroscience 76:137-145.
26. Goodell MA, Rosenzweig M, Kim H, Marks DF, DeMaria M, Paradis G, Grupp SA, Sieff CA, Mulligan RC, Johnson RP. 1997. Dye efflux studies suggest that hematopoietic stem cells expressing low or undetectable levels of CD34 antigen exist in multiple species. Nat Med 3:1337-1345.
27. Graeber TG, Eisenberg D. 2001. Bioinformatic identification of potential autocrine signaling loops in cancers from gene expression profiles. Nat Genet 29:295-300.
28. Gupta P, Oegema TR, Brazil JJ, Dudek AZ, Slungaard A, Verfaille CM. 1998. Structurally specific heparan sulfates support primitive human hematopoiesis by formation of a multimolecular stem cell niche. Blood 92:4641-4651.
29. Hankemeier S, Keus M, Zeichen J, Jagodzinski M, Barkhausen T, Bosch U, Krettek C, Van Griensven M. 2005. Modulation of proliferation and differentiation of human bone marrow stromal cells by fibroblast growth factor 2: Potential implications for tissue engineering of tendons and ligaments. Tissue Eng 11:41-49.
30. Inatani M, Haruta M, Honjo M, Oohira A, Kido N, Takahashi M, Honda Y, Tanihara H. 2001. Upregulated expression of N-syndecan, a transmembrane heparan sulfate proteoglycan, in differentiated neural stem cells. Brain Res 920:217-221.
31. Jackson KA, Mi T, Goodell MA. 1999. Hematopoietic potential of stem cells isolated from murine skeletal muscle. Proc Natl Acad Sci USA 96:14482-14486.
32. Johansson CB, Momma S, Clarke DL, Risling M, Lendhal U, Frisen J. 1999. Identification of a neural stem cell in the adult mammalian central nervous system. Cell 96:25-34.
33. Kannan Y, Usami K, Okada M, Shimizu S, Matsuda H. 1992. Nerve growth factor suppresses apoptosis of murine neutrophils. Bioch Biophys Res Commun 186:1050-1056.
34. Klein G. 1995. The extracellular matrix of the hematopoietic microenvironment. Experientia 51:914-926.
35. - stem cells that give rise to SCID-repopulating cells. Blood 101:869-876.
36. Kuznetsov SA, Friedenstein AJ, Gehron Robey P. 1997. Factors required for bone marrow stromal fibroblast colony formation in vitro. Br J Haematol 97:561-570.
37. La Barca C, Paigen KA. 1980. Simple, rapid, and sensitive DNA assay procedure. Anal Biochem 102:344-352.
38. Labouyrie E, Dubus P, Groppi A, Mahon FX, Ferrer J, Parrens M, Reiffers J, de Mascarel A, Merlio JP. 1999. Expression of neurotrophins and their receptors in human bone marrow. Am J Pathol 154:405-415.
39. Le Bousse-Kerdiles MC. 1999. Dual implication of fibrogenic citokines in the pathogenesis of fibrosis and myeloproliferation in myeloid metaplasia with myelofibrosis. Ann Hematol 78:437-444.
40. Lee KS, Kim HJ, Li QL, Chi XZ, Ueta C, Komori T, Wozney JM, Kim EG, Choi JY, Ryoo HM, Bae SC. 2000. Runx2 is a common target of trasforming growth factor beta1 and bone morphogenetic protein 2, and cooperation between Runx2 and Smad5 induces osteoblast-specific gene expression in the pluripotent mesenchymal precursor cell line C2C12. Mol Cell Biol 20:8783-8792.
41. Lieb E, Milz S, Vogel T, Hacker M, Dauner M, Schulz MB. 2004. Effects of transforming growth factor beta1 on bonelike tissue formation in three-dimensional cell culture. I. Culture conditions and tissue formation. Tissue Eng 10:1399-1413.
42. Luukko K, Moshnyakov M, Sainio K, Saarma M, Sariola H, Thesleff I. 1996. Expression of neurotrophin receptors during rat tooth development is developmentally regulated, independent of innervation, and suggests functions in the regulation of morphogenesis and innervation. Dev Dyn 206: 87-99.
43. Massaguè J. 1987. Identification of receptors for type-beta transforming growth factor. Methods Enzymol 146:174-195.
44. Massaguè J. 1990. The transforming growth factor-beta family. Ann Rev Cell Biol 6:597-641.
45. Minguell JJ, Hardy C, Tavassoli M. 1992. Membrane-associated chondroitin sulfate proteoglycan and fibronectin mediate the binding of hemopoietic progenitor cells to stromal cells. Exp Cell Res 20:200-207.
46. Mohle R, Bautz F, Rafii S, Moore MA, Brugger W, Kanz L. 1999. Regulation of transendothelial migration of hematopoietic progenitor cells. Ann N Y Acad Sci 872:176-185.
47. Moscatelli D. 1987. High and low affinity bindingsites for basic fibroblast growth factor on cultured cells: Absence of a role for low affinity binding in the stimulation of plasminogen activator production by bovine capillary endothelial cells. J Cell Physiol 131:123-130.
48. Munson PJ, Rodbard D. 1980. Ligand: A versatile computerized approach for characterization of ligand-binding system. Anal Biochem 107:220-239.
49. Netelenbos T, Zuijderduijn S, Van Den Born J, Kessler FL, Zweegman S, Huijgens PC, Drager AM. 2002. Proteoglycans guide SDF-1-induced migration of hematopoietic progenitor cells. J Leuoc Biol 72:353-362.
50. Novitzky N, Makgoka SJ, Mohamed R. 2001. Basic fibroblast growth factor corrects proliferative derangement of bone marow stroma amd CD34(+) population following allogeneic stem cell transplantation. Exp Hematol 29:1432-1438.
51. Ogawa M. 2002. Changing phenotypes of hematopoietic stem cells. Exp Hematol 30:3-6.
52. Pfeilschifter J, D'Souza SM, Mundy GR. 1987. Effects of transforming growth factor-beta on osteoblastic osteosarcoma cells. Endocrinology 121: 212-218.
53. Quirici N, Soligo D, Bossolasco P, Servida F, Lumini C, Deliliers GL. 2002. Isolation of bone marrow mesenchymal stem cells by anti-nerve growth factor receptor antibodies. Exp Hematol 30:783-791.
54. Roelen BA, Dijke P. 2003. Controlling mesenchymal stem cell differentiation by TGFBeta family members. J Orthop Sci 8:740-748.
55. Ruoslahti E. 1989. Proteoglycans in cell regulation. J Biol Chem 264:13369-13372.
56. Sasano Y, Zhu JX, Tsubota M, Takahashi I, Onodera K, Mizoguchi I, Kagayama M. 2002. Gene expression of MMP-8 and MMP-13 during embryonic development of bone and cartilage in the rat mandible and hind limb. J Histoch Cytochem 50:325-332.
57. Sato T, Laver JH, Ogawa M. 1999. Reversible expression of CD34 by murine hematopoietic stem cells. Blood 94:2548-2554.
58. Scatchard G. 1949. The attractions of proteins for small molecules and ions. Ann N Y Acad Sci 51:660-672.
59. Siczkowski M, Clarke D, Gordon MY. 1992a. Binding of primitive hematopoietic progenitor cells to marrow stromal cells involves heparan sulfate. Blood 80:912-919.
60. Siczkowski M, Robertson D, Gordon MY. 1992b. Synthesis and deposition of glycosaminoglycans in the murine hemopoietic stromal line S17: Modulators of the hemopoietic microenvironment. Exp Hematol 20:1285-1290.
61. Song QH, Klepeis VE, Nugent MA, Trinkaus-Randall V. 2002. TGF-beta 1 and FGF-2 mRNA expression during fibroblast wound healing. Mol Pathol 55:164-176.
62. Sugahara H, Kanakura Y, Furitsu T, Ishihara K, Oritani K, Ikeda H, Kitayama H, Ishikawa J, Hashimoto K, Kanayama Y, et al. 1994. Induction of programmed cell death in human hematopoietic cell lines by fibronectin via its interaction with very late antigen 5. J Exp Med 179:1757-1766.
63. Sweeney EA, Lortat-Jacob H, Priestley GV, Nakamoto B, Papayannopoulou T. 2002. Sulfated polysaccharides increase plasma levels of SDF-1 in monkeys and mice: Involvement in mobilization of stem/progenitor cells. Blood 99: 44-51.
64. Sykes B, Puddle B, Francis M, Smith R. 1976. The estimation of two collagens human dermis by interrupted gel electrophoresis. Biochem Biophys Res Commun 72:1472-1480.
65. Ta TV, Baraniak D, Julian J, Korostoff J, Carson DD, Farach-Carson MC. 2002. Heparan sulfate interacting protein (HIP/L29) negatively regulates growth responses to basic fibroblast growth factor in gingival fibroblasts. J Dent Res 81:247-252.
66. Tabilio A, Falzetti F, Giannoni C, Aversa F, Martelli MP, Rossetti M, Caputo P, Chionne F, Gambelunghe C, Martelli MF. 1997. Stem cell mobilization in normal donors. J Hematother 6:227-234.
67. Tanaka Y, Adams DH, Shaw S. 1993. Proteoglycans on endothelial cells present adhesion-inducing cytokines to leukocytes. Immunol Today 14:111-115.
68. Tufvesson E, Malmstrom J, Marko-Varga G, Westergren-Thorsson G. 2002. Biglycan isoforms with differences in polysaccharide substitution and core protein in human lung fibroblasts. Eur J Biochem 269:3688-3696.
69. Urashima M, Ogata A, Chauhan D, Hatziyanni M, Vidriales MB, Dedera DA, Schlossman RL, Anderson KC. 1996. Transforming growth factor-beta1: Differential effects on multiple myeloma versus normal B cells. Blood 87: 1928-1938.
70. Wagner C. 2000. Fibronectin synthesis by activated T limphocites: Up-regulation of a surface-associated isoform with signalling function. Immunology 99:532-539.
71. Webster DF, Harvey WA. 1979. A quantitative assay for collagen synthesis in microwell fibroblast cultures. Anal Bioch 96:220-224.
72. Woodbury D, Schwarz EJ, Prockop DJ, Black IB. 2000. Adult rat and human bone marrow stromal cells differentiate into neurons. J Neurosc Res 61:364-370.
73. Xiao G, Jiang D, Gopalakrishnan R, Franceschi RT. 2002. FGF-2 induction of the osteocalcin gene requires MAPK activity and phosphorylation of the osteoblast transcription factor, Cbfa1/Runx2. J Biol Chem 277:36181-36187.
74. Zuckerman KS. 1984. Composition and function of extracellular matrix in the stroma of long-terbiooom marrow cultures. In: Wright DG, Greenberger JS, editors. Long-term bone marrow culture. New York, NY: Liss. 157p.