Galectin-1 stimulates motility of human umbilical cord blood-derived mesenchymal stem cells by downregulation of smad2/3-dependent collagen 3/5 and upregulation of NF-κB-dependent fibronectin/laminin 5 expression

Cell Death and Disease

Volumn 5, Issue 2, 2014, Pages

  Yun, S P ^a   Lee, S J ^a   Jung, Y H ^a   Han, H J ^a  

^a Seoul National University   (South Korea)

Author keywords

extracellular matrix proteins; galectin 1; motility; umbilical cord blood derived mesenchymal stem cells

Indexed keywords

CARBOHYDRATE; CAVEOLIN 1; CHOLESTEROL; COLLAGEN TYPE 3; COLLAGEN TYPE 5; FIBRONECTIN; FOCAL ADHESION KINASE; GALACTOSIDASE; GALECTIN 1; GELATINASE A; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTEGRIN; KALININ; LACTOSE; LECTIN; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE B; PROTEIN KINASE C; RNA; SMAD2 PROTEIN; SMAD3 PROTEIN; SMALL INTERFERING RNA;

ARTICLE; CALCIUM TRANSPORT; CELL CULTURE; CELL FRACTIONATION; CELL FUNCTION; CELL LYSATE; CELL MIGRATION; CELL MOTILITY; CHEMOTAXIS; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME LINKED IMMUNOSORBENT ASSAY; EXTRACELLULAR MATRIX; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE MICROSCOPY; MESENCHYMAL STEM CELL; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ISOLATION; UMBILICAL CORD BLOOD; WESTERN BLOTTING; WOUND HEALING;

CELL ADHESION MOLECULES; CELL MOVEMENT; CELLS, CULTURED; COLLAGEN TYPE III; COLLAGEN TYPE V; DOWN-REGULATION; FETAL BLOOD; FIBRONECTINS; GALECTIN 1; HUMANS; MESENCHYMAL STROMAL CELLS; NF-KAPPA B; SMAD2 PROTEIN; SMAD3 PROTEIN; UP-REGULATION;

EID: 84896744604     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2014.3     Document Type: Article

References (59)

1. Comte I, Kim Y, Young CC, van der Harg JM, Hockberger P, Bolam PJ et al. Galectin-3 maintains cell motility from the subventricular zone to the olfactory bulb. J Cell Sci 2011; 124: 2438-2447.
2. Barondes SH, Castronovo V, Cooper DN, Cummings RD, Drickamer K, Feizi T et al. Galectins: A family of animal beta-galactoside-binding lectins. Cell 1994; 76: 597-598.
3. Lee MY, Lee SH, Park JH, Han HJ. Interaction of galectin-1 with caveolae induces mouse embryonic stem cell proliferation through the Src, ERas, Akt and mTOR signaling pathways. Cell Mol Life Sci 2009; 66: 1467-1478.
4. Liu FT, Rabinovich GA. Galectins as modulators of tumour progression. Nat Rev Cancer 2005; 5: 29-41.
5. Chovanec M, Smetana Jr. K, Dvorankova B, Plzakova Z, Andre S, Gabius HJ. Decrease of nuclear reactivity to growth-regulatory galectin-1 in senescent human keratinocytes and detection of non-uniform staining profile alterations upon prolonged culture for galectin-1 and-3. Anat Histol Embryol 2004; 33: 348-354.
6. Silva Jr. WA, Covas DT, Panepucci RA, Proto-Siqueira R, Siufi JL, Zanette DL et al. The profile of gene expression of human marrow mesenchymal stem cells. Stem Cells 2003; 21: 661-669.
7. Szebeni GJ, Kriston-Pal E, Blazso P, Katona RL, Novak J, Szabo E et al. Identification of galectin-1 as a critical factor in function of mouse mesenchymal stromal cell-mediated tumor promotion. PLoS One 2012; 7: E41372.
8. Sakaguchi M, Shingo T, Shimazaki T, Okano HJ, Shiwa M, Ishibashi S et al. A carbohydrate-binding protein, Galectin-1, promotes proliferation of adult neural stem cells. Proc Natl Acad Sci USA 2006; 103: 7112-7117.
9. Panepucci RA, Siufi JL, Silva Jr. WA, Proto-Siquiera R, Neder L, Orellana M et al. Comparison of gene expression of umbilical cord vein and bone marrow-derived mesenchymal stem cells. Stem Cells 2004; 22: 1263-1278.
10. Dvorankova B, Szabo P, Lacina L, Gal P, Uhrova J, Zima T et al. Human galectins induce conversion of dermal fibroblasts into myofibroblasts and production of extracellular matrix: Potential application in tissue engineering and wound repair. Cells Tissues Organs 2011; 194: 469-480.
11. Park JH, Ryu JM, Yun SP, Kim MO, Han HJ. Fibronectin stimulates migration through lipid raft dependent NHE-1 activation in mouse embryonic stem cells: Involvement of RhoA, Ca2+/CaM, and ERK. Biochim Biophys Acta 2012; 1820: 1618-1627.
12. Suh HN, Han HJ. Collagen I regulates the self-renewal of mouse embryonic stem cells through alpha2beta1 integrin-And DDR1-dependent Bmi-1. J Cell Physiol 2011; 226: 3422-3432.
13. Suh HN, Kim MO, Han HJ. Laminin-111 stimulates proliferation of mouse embryonic stem cells through a reduction of gap junctional intercellular communication via RhoA-mediated Cx43 phosphorylation and dissociation of Cx43/ZO-1/drebrin complex. Stem Cells Dev 2012; 21: 2058-2070.
14. Veevers-Lowe J, Ball SG, Shuttleworth A, Kielty CM. Mesenchymal stem cell migration is regulated by fibronectin through a5b1-integrin-mediated activation of PDGFR-b and potentiation of growth factor signals. J Cell Sci 2011; 124: 1288-1300.
15. Gilles C, Polette M, Coraux C, Tournier JM, Meneguzzi G, Munaut C et al. Contribution of MT1-MMP and of human laminin-5 g2 chain degradation to mammary epithelial cell migration. J Cell Sci 2001; 114: 2967-2976.
16. Siwik DA, Chang DL, Colucci WS. Interleukin-1b and tumor necrosis factor-A decrease collagen synthesis and increase matrix metalloproteinase activity in cardiac fibroblasts in vitro. Circ Res 2000; 86: 1259-1265.
17. Ghosh AK, Yuan W, Mori Y, Varga J. Smad-dependent stimulation of type I collagen gene expression in human skin fibroblasts by TGF-b involves functional cooperation with p300/ CBP transcriptional coactivators. Oncogene 2000; 19: 3546-3555.
18. Lee BH, Park SY, Kang KB, Park RW, Kim IS. NF-kB activates fibronectin gene expression in rat hepatocytes. Biochem Biophys Res Commun 2002; 297: 1218-1224.
19. Zeddou M, Briquet A, Relic B, Josse C, Malaise MG, Gothot A et al. The umbilical cord matrix is a better source of mesenchymal stem cells (MSC) than the umbilical cord blood. Cell Biol Int 2010; 34: 693-701.
20. Sensebe L, Krampera M, Schrezenmeier H, Bourin P, Giordano R. Mesenchymal stem cells for clinical application. Vox Sang 2010; 98: 93-107.
21. Wakitani S, Nawata M, Tensho K, Okabe T, Machida H, Ohgushi H. Repair of articular cartilage defects in the patello-femoral joint with autologous bone marrow mesenchymal cell transplantation: Three case reports involving nine defects in five knees. J Tissue Eng Regen Med 2007; 1: 74-79.
22. Chai C, Leong KW. Biomaterials approach to expand and direct differentiation of stem cells. Mol Ther 2007; 15: 467-480.
23. Guan J, Zhu Z, Zhao RC, Xiao Z, Wu C, Han Q et al. Transplantation of human mesenchymal stem cells loaded on collagen scaffolds for the treatment of traumatic brain injury in rats. Biomaterials 2013; 34: 5937-5946.
24. Yamane J, Ishibashi S, Sakaguchi M, Kuroiwa T, Kanemura Y, Nakamura M et al. Transplantation of human neural stem/progenitor cells overexpressing galectin-1 improves functional recovery from focal brain ischemia in the Mongolian gerbil. Mol Brain 2011; 4: 35.
25. Tate CC, Shear DA, Tate MC, Archer DR, Stein DG, LaPlaca MC. Laminin and fibronectin scaffolds enhance neural stem cell transplantation into the injured brain. J Tissue Eng Regen Med 2009; 3: 208-217.
26. Lee MY, Han HJ. Galectin-1 upregulates glucose transporter-1 expression level via protein kinase C, phosphoinositol-3 kinase, and mammalian target of rapamycin pathways in mouse embryonic stem cells. Int J Biochem Cell Biol 2008; 40: 2421-2430.
27. Burns JS, Kristiansen M, Kristensen LP, Larsen KH, Nielsen MO, Christiansen H et al. Decellularized matrix from tumorigenic human mesenchymal stem cells promotes neovascularization with galectin-1 dependent endothelial interaction. PLoS One 2011; 6: E21888.
28. Camby I, Le Mercier M, Lefranc F, Kiss R. Galectin-1: A small protein with major functions. Glycobiology 2006; 16: 137R-157R.
29. Jung TY, Jung S, Ryu HH, Jeong YI, Jin YH, Jin SG et al. Role of galectin-1 in migration and invasion of human glioblastoma multiforme cell lines. J Neurosurg 2008; 109: 273-284.
30. Elola MT, Chiesa ME, Alberti AF, Mordoh J, Fink NE. Galectin-1 receptors in different cell types. J Biomed Sci 2005; 12: 13-29.
31. Meyer C, Liu Y, Kaul A, Peipe I, Dooley S. Caveolin-1 abrogates TGF-b mediated hepatocyte apoptosis. Cell Death Dis 2013; 4: E466.
32. Chen Z, Bakhshi FR, Shajahan AN, Sharma T, Mao M, Trane A et al. Nitric oxidedependent Src activation and resultant caveolin-1 phosphorylation promote eNOS/ caveolin-1 binding and eNOS inhibition. Mol Biol Cell 2012; 23: 1388-1398.
33. Lee H, Volonte D, Galbiati F, Iyengar P, Lublin DM, Bregman DB et al. Constitutive and growth factor-regulated phosphorylation of caveolin-1 occurs at the same site (Tyr-14) in vivo: Identification of a c-Src/Cav-1/Grb7 signaling cassette. Mol Endocrinol 2000; 14: 1750-1775.
34. Su B, Gao L, Meng F, Guo LW, Rothschild J, Gelman IH. Adhesion-mediated cytoskeletal remodeling is controlled by the direct scaffolding of Src from FAK complexes to lipid rafts by SSeCKS/AKAP12. Oncogene 2013; 32: 2016-2026.
35. Yun SP, Ryu JM, Kim MO, Park JH, Han HJ. Rapid actions of plasma membrane estrogen receptors regulate motility of mouse embryonic stem cells through a profilin-1/cofilin-1-directed kinase signaling pathway. Mol Endocrinol 2012; 26: 1291-1303.
36. Walzel H, Schulz U, Neels P, Brock J. Galectin-1, a natural ligand for the receptor-Type protein tyrosine phosphatase CD45. Immunol Lett 1999; 67: 193-202.
37. Vespa GN, Lewis LA, Kozak KR, Moran M, Nguyen JT, Baum LG et al. Galectin-1 specifically modulates TCR signals to enhance TCR apoptosis but inhibit IL-2 production and proliferation. J Immunol 1999; 162: 799-806.
38. Margadant C, van den Bout I, van Boxtel AL, Thijssen VL, Sonnenberg A. Epigenetic regulation of galectin-3 expression by beta1 integrins promotes cell adhesion and migration. J Biol Chem 2012; 287: 44684-44693.
39. Horiguchi N, Arimoto K, Mizutani A, Endo-Ichikawa Y, Nakada H, Taketani S. Galectin-1 induces cell adhesion to the extracellular matrix and apoptosis of non-Adherent human colon cancer Colo201 cells. J Biochem 2003; 134: 869-874.
40. Turpeenniemi-Hujanen T, Thorgeirsson UP, Hart IR, Grant SS, Liotta LA. Expression of collagenase IV (basement membrane collagenase) activity in murine tumor cell hybrids that differ in metastatic potential. J Natl Cancer Inst 1985; 75: 99-103.
41. Pasco S, Brassart B, Ramont L, Maquart FX, Monboisse JC. Control of melanoma cell invasion by type IV collagen. Cancer Detect Prev 2005; 29: 260-266.
42. D'Alessio S, Gerasi L, Blasi F. uPAR-deficient mouse keratinocytes fail to produce EGFR-dependent laminin-5, affecting migration in vivo and in vitro. J Cell Sci 2008; 121: 3922-3932.
43. Zou L, Cao S, Kang N, Huebert RC, Shah VH. Fibronectin induces endothelial cell migration through b-1 integrin and Src-dependent phosphorylation of fibroblast growth factor receptor-1 at tyrosines 653/654 and 766. J Biol Chem 2012; 287: 7190-7202.
44. Koshikawa N, Moriyama K, Takamura H, Mizushima H, Nagashima Y, Yanoma S et al. Overexpression of laminin g2 chain monomer in invading gastric carcinoma cells. Cancer Res 1999; 59: 5596-5601.
45. Carrero R, Cerrada I, Lledo E, Dopazo J, Garcia-Garcia F, Rubio MP et al. IL-1b induces mesenchymal stem cells migration and leucocyte chemotaxis through NF-kB. Stem Cell Rev 2012; 8: 905-916.
46. Huang K, Liu W, Lan T, Xie X, Peng J, Huang J et al. Berberine reduces fibronectin expression by suppressing the S1P-S1P2 receptor pathway in experimental diabetic nephropathy models. PLoS One 2012; 7: E43874.
47. Inai K, Norris RA, Hoffman S, Markwald RR, Sugi Y. BMP-2 induces cell migration and periostin expression during atrioventricular valvulogenesis. Dev Biol 2008; 315: 383-396.
48. Zhang GY, He B, Liao T, Luan Q, Tao C, Nie CL et al. Caveolin 1 inhibits transforming growth factor-beta1 activity via inhibition of Smad signaling by hypertrophic scar derived fibroblasts in vitro. J Dermatol Sci 2011; 62: 128-131.
49. Maity G, Sen T, Chatterjee A. Laminin induces matrix metalloproteinase-9 expression and activation in human cervical cancer cell line (SiHa). J Cancer Res Clin Oncol 2011; 137: 347-357.
50. Santamato A, Fransvea E, Dituri F, Caligiuri A, Quaranta M, Niimi T et al. Hepatic stellate cells stimulate HCC cell migration via laminin-5 production. Clin Sci (Lond) 2011; 121: 159-168.
51. Shi ZD, Wang H, Tarbell JM. Heparan sulfate proteoglycans mediate interstitial flow mechanotransduction regulating MMP-13 expression and cell motility via FAK-ERK in 3D collagen. PLoS One 2011; 6: E15956.
52. Suh HN, Han HJ. Laminin regulates mouse embryonic stem cell migration: Involvement of Epac1/Rap1 and Rac1/cdc42. Am J Physiol Cell Physiol 2010; 298: C1159-C1169.
53. Kollar S, Sandor N, Molvarec A, Stenczer B, Rigo Jr. J, Tulassay T et al. Prevalence of intracellular galectin-1-expressing lymphocytes in umbilical cord blood in comparison with adult peripheral blood. Biol Blood Marrow Transplant 2012; 18: 1608-1613.
54. Lamote I, Meyer E, Duchateau L, Burvenich C. Influence of 17b-estradiol, progesterone, and dexamethasone on diapedesis and viability of bovine blood polymorphonuclear leukocytes. J Dairy Sci 2004; 87: 3340-3349.
55. Chieng-Yane P, Bocquet A, Letienne R, Bourbon T, Sablayrolles S, Perez M et al. Protease-Activated receptor-1 antagonist F 16618 reduces arterial restenosis by downregulation of tumor necrosis factor a and matrix metalloproteinase 7 expression, migration, and proliferation of vascular smooth muscle cells. J Pharmacol Exp Ther 2011; 336: 643-651.
56. Park JH, Han HJ. Caveolin-1 plays important role in EGF-induced migration and proliferation of mouse embryonic stem cells: Involvement of PI3K/Akt and ERK. Am J Physiol Cell Physiol 2009; 297: C935-C944.
57. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976; 72: 248-254.
58. Song KS, Li S, Okamoto T, Quilliam LA, Sargiacomo M, Lisanti MP. Co-purification and direct interaction of Ras with caveolin, an integral membrane protein of caveolae microdomains. Detergent-free purification of caveolae microdomains. J Biol Chem 1996; 271: 9690-9697.
59. Lee SH, Lee YJ, Han HJ. Effect of arachidonic acid on hypoxia-induced IL-6 production in mouse ES cells: Involvement of MAPKs, NF-kB, and HIF-1a. J Cell Physiol 2010; 222: 574-585.