Hypoxia promotes murine bone-marrow-derived stromal cell migration and tube formation

Stem Cells

Volumn 21, Issue 3, 2003, Pages 337-347

  Annabi, Borhane ^a   Lee, Ying Ta ^a   Turcotte, Sandra ^a   Naud, Emmanuelle ^a   Desrosiers, Richard R ^a   Champagne, Martin ^a   Eliopoulos, Nicoletta ^b   Galipeau, Jacques ^b   Béliveau, Richard ^a  

^a UNIVERSITY OF MONTREAL   (Canada)

^b MCGILL UNIVERSITY   (Canada)

Author keywords

Angiogenesis; Cell migration; Hypoxia; Matrix metalloproteinase; Murine marrow stromal cells

Indexed keywords

CYTOKINE; GELATINASE A; GROWTH FACTOR; MATRIGEL; MESSENGER RNA; VASCULOTROPIN;

ANGIOGENESIS; ANIMAL CELL; ARTICLE; AUTOCRINE EFFECT; BONE MARROW CELL; CELL MIGRATION; CONTROLLED STUDY; ENDOTHELIUM CELL; EXTRACELLULAR MATRIX; GENE EXPRESSION REGULATION; GENE INDUCTION; GLIOMA CELL; HUMAN; HUMAN CELL; HYPOXIA; MICROENVIRONMENT; MOUSE; NEOVASCULARIZATION (PATHOLOGY); NONHUMAN; PARACRINE SIGNALING; PROTEIN EXPRESSION; REGULATORY MECHANISM;

ANIMALIA; MURINAE;

EID: 0038323916     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1634/stemcells.21-3-337     Document Type: Article

References (50)

1. Prockop DJ. Marrow stromal cells as stem cells for nonhematopoietic tissues. Science 1997;276:71-74.
2. Dennis JE, Charbord P. Origin and differentiation of human and murine stroma. STEM CELLS 2002;20:205-214.
3. Huss R, Lange C, Weissinger EM et al. Evidence of peripheral blood-derived, plastic-adherent CD34(-/low) hematopoietic stem cell clones with mesenchymal stem cell characteristics. STEM CELLS 2000;18:252-260.
4. Tomanek RJ, Schatteman GC. Angiogenesis: new insights and therapeutic potential. Anat Rec 2000;261:126-135.
5. Reyes M, Lund T, Lenvik T et al. Purification and ex vivo expansion of postnatal human marrow mesodermal progenitor cells. Blood 2001;98:2615-2625.
6. Eliopoulos N, Al-Khaldi A, Beauséjour CM et al. Human cytidine deaminase as an ex vivo drug selectable marker in gene-modified primary bone marrow stromal cells. Gene Ther 2002;9:452-462.
7. Al-Khaldi A, Eliopoulos N, Martineau D et al. Postnatal bone marrow stromal cells elicit a potent VEGF-dependent neoangiogenic response in vivo. Gene Therapy 2003;8:621-629.
8. Reyes M, Dudek A, Jahagirdar B et al. Origin of endothelial progenitors in human postnatal bone marrow. J Clin Invest 2002;109:337-346.
9. Hombauer H, Minguell JJ. Selective interactions between epithelial tumour cells and bone marrow mesenchymal stem cells. Br J Cancer 2000;82:1290-1296.
10. Wallace SR, Oken MM, Lunetta KL et al. Abnormalities of bone marrow mesenchymal cells in multiple myeloma patients. Cancer 2001;91:1219-1230.
11. Birkedal-Hansen H. Proteolytic remodeling of extracellular matrix. Curr Opin Cell Biol 1995;7:728-735.
12. Forget MA, Desrosiers RR, Béliveau R. Physiological roles of matrix metalloproteinases: implications for tumor growth and metastasis. Can J Physiol Pharmacol 1999;77:465-480.
13. +) cells and their transmigration through reconstituted basement membrane. Blood 1999;93:3379-3390.
14. +) cells in response to chemokines. Exp Hematol 2000;28:1274-1285.
15. Coussens LM, Tinkle CL, Hanahan D et al. MMP-9 supplied by bone marrow-derived cells contributes to skin carcinogenesis. Cell 2000;103:481-490.
16. Holmbeck K, Bianco P,Caterina Jet al. MT1-MMP-deficient mice develop dwarfism, osteopenia, arthritis, and connective tissue disease due to inadequate collagen turnover. Cell 1999;99:81-92.
17. Malonne H, Langer I, Kiss R. Mechanisms of tumor angiogenesis and therapeutic implications: angiogenesis inhibitors. Clin Exp Metastasis 1999;17:1-14.
18. Lennon DP, Edmison JM, Caplan AI. Cultivation of rat marrow-derived mesenchymal stem cells in reduced oxygen tension: effects on in vitro and in vivo osteochondrogenesis. J Cell Physiol 2001;187:345-355.
19. Woodbury D, Schwarz EJ, Prockop DJ et al. Adult rat and human bone marrow stromal cells differentiate into neurons. J Neurosci Res 2000;61:364-370.
20. Javazon EH, Colter DC, Schwarz EJ et al. Rat marrow stromal cells are more sensitive to plating density and expand c more rapidly from single-cell-derived colonies than human marrow stromal cells. STEM CELLS 2001;19:219-225.
21. Zhao LR, Duan WM, Reyes M et al. Human bone marrow stem cells exhibit neural phenotypes and ameliorate neurological deficits after grafting into the ischemic brain of rats. Exp Neurol 2002;174:11-20.
22. Venetsanakos E, Mirza A, Fanton C et al. Induction of tubulogenesis in telomearse-immortalized human microvascular endothelial cells by glioblastoma cells. Exp Cell Res 2002;273:21-33.
23. Beaulieu E, Kachra Z, Mousseau N et al. Matrix metalloproteinases and their inhibitors in human pituitary tumors. Neurosurgery 1999;45:1432-1441.
24. Vukicevic S, Kleinman HK, Luyten FP et al. Identification of multiple active growth factors in basement membrane Matrigel suggests caution in interpretation of cellular activity related to extracellular matrix components. Exp Cell Res 1992;202:1-8.
25. Ben-Yosef Y, Lahat N, Shapiro S et al. Regulation of endothelial matrix metalloproteinase-2 by hypoxia/reoxygenation. Circ Res 2002;90:784-791.
26. Seiki M. Membrane-type matrix metalloproteinases. APMIS 1999;107:137-143.
27. Manske M, Bade EG. Growth factor-induced cell migration: biology and methods of analysis. Int Rev Cytol 1994;155:49-96.
28. Cross MJ, Claesson-Welsh L. FGF and VEGF function in angiogenesis: signalling pathways, biological responses and therapeutic inhibition. Trends Pharmacol Sci 2001;22:201-207.
29. Yanai N, Matsui N, Furusawa T et al. Sphingosine-1-phosphate and lysophosphatidic acid trigger invasion of primitive hematopoietic cells into stromal cell layers. Blood 2000;96:139-144.
30. Toth M, Bernardo MM, Gervasi DC et al. Tissue inhibitor of metalloproteinase (TIMP)-2 acts synergistically with synthetic matrix metalloproteinase (MMP) inhibitors but not with TIMP-4 to enhance the (Membrane type 1)-MMP-dependent activation of pro-MMP-2. J Biol Chem 2000;275:41415-41423.
31. Bernardo MM, Brown S, Li ZH et al. Design, synthesis, and characterization of potent, slow-binding inhibitors that are selective for gelatinases. J Biol Chem 2002;277:11201-11207.
32. Annabi B, Lachambre MP, Bousquet-Gagnon N et al. Green tea polyphenol (-)-epigallocatechin 3-gallate inhibits MMP-2 secretion and MT1-MMP-driven migration in glioblastoma cells. Biochim Biophys Acta 2002;1542:209-220.
33. Ramirez-Bergeron DL, Simon MC. Hypoxia-inducible factor and the development of stem cells of the cardiovascular system. STEM CELLS 2001;19:279-286.
34. Koong AC, Denko NC, Hudson KM et al. Candidate genes for the hypoxic tumor phenotype. Cancer Res 2000;60:883-887.
35. Yan SF, Lu J, Zou YS et al. Hypoxia-associated induction of early growth response-1 gene expression. J Biol Chem 1999;274:15030-15040.
36. Haas TL, Stitelman D, Davis SJ et al. Egr-1 mediates extra-cellular matrix-driven transcription of membrane type 1 matrix metalloproteinase in endothelium. J Biol Chem 1999;274:22679-22685.
37. Langer R, Conn H, Vacanti J et al. Control of tumor growth in animals by infusion of an angiogenesis inhibitor. Proc Natl Acad Sci USA 1980;77:4331-4335.
38. Ingber DE, Madri JA, Folkman JA. Possible mechanism for inhibition of angiogenesis by angiostatic steroids: induction of capillary basement membrane dissolution. Endocrinology 1986;119:1768-1775.
39. Annabi B, Lachambre MP, Bousquet-Gagnon N et al. Localization of membrane-type 1 matrix metalloproteinase in caveolae membrane domains. Biochem J 2001;353:547-553.
40. Galvez BG, Matias-Roman S, Albar JP et al. Membrane type 1-matrix metalloproteinase is activated during migration of human endothelial cells and modulates endothelial motility and matrix remodeling. J Biol Chem 2001;276:37491-37500.
41. Kajita M, Itoh Y, Chiba T et al. Membrane-type 1 matrix metalloproteinase cleaves CD44 and promotes cell migration. J Cell Biol 2001;153:893-904.
42. Hooper NM, Trew AJ, Parkin ET et al. The role of proteolysis in Alzheimer's disease. Adv Exp Med Biol 2000;477:379-390.
43. Dell'Aica I, Dona M, Sartor L et al. (-)Epigallocatechin-3-gallate directly inhibits MT1-MMP activity, leading to accumulation of nonactivated MMP-2 at the cell surface. Lab Invest 2002;82:1685-1693.
44. Lamy S, Gingras D, Béliveau R. Green tea catechins inhibit vascular endothelial growth factor receptor phosphorylation. Cancer Res 2002;62:381-385.
45. Deryugina E.I., Soroceanu L, Strongin AY. Up-regulation of vascular endothelial growth factor by membrane-type I matrix metalloproteinase stimulates human glioma xenograft growth and angiogenesis. Cancer Res 2002;62:580-588.
46. Sounni NE, Devy L, Hajitou A et al. MT1-MMP expression promotes tumor growth and angiogenesis through an up-regulation of vascular endothelial growth factor expression. FASEB J 2002;16:555-564.
47. Cipolleschi MG, Rovida E, Ivanovic Z et al. The expansion of murine bone marrow cells preincubated in hypoxia as an in vitro indicator of their marrow-repopulating ability. Leukemia 2000;14:735-739.
48. Ikeda E, Achen MG, Breier G et al. Hypoxia-induced transcriptional activation and increased mRNA stability of vascular endothelial growth factor in C6 glioma cells. J Biol Chem 1995;270:19761-19766.
49. Shima DT, Deutsch U, D'Amore PA. Hypoxic induction of vascular endothelial growth factor (VEGF) in human epithelial cells is mediated by increases in mRNA stability. FEBS Lett 1995;370:203-208.
50. Kourembanas S, Hannan RL, Faller DV. Oxygen tension regulates the expression of the platelet-derived growth factor-B chain gene in human endothelial cells. J Clin Invest 1990;86:670-674.