Hypoxic conditioned medium from human amniotic fluid-derived mesenchymal stem cells accelerates skin wound healing through TGF-β/SMAD2 and PI3K/AKT pathways

International Journal of Molecular Sciences

Volumn 15, Issue 1, 2014, Pages 605-628

  Jun, Eun Kyoung ^a   Zhang, Qiankun ^a   Yoon, Byung Sun ^a   Moon, Jai Hee ^a   Lee, Gilju ^a   Park, Gyuman ^a   Kang, Phil Jun ^a   Lee, Jung Han ^a   Kim, Areee ^b   You, Seungkwon ^a  

^a Korea University   (South Korea)

^b Korea University College of Medicine   (South Korea)

Author keywords

Amniotic fluid derived mesenchymal stem cells(AF MASs); Hypoxia; PI3K AKT; TGF SMAD2; Wound healing

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; AMINOPEPTIDASE; COLLAGEN TYPE 3; ELASTIN; HYPOXIA INDUCIBLE FACTOR; OSTEOCALCIN; OSTEOPONTIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA 2; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOTRANSFERASE INHIBITOR; PROTEIN KINASE B; SB 505124; SMAD2 PROTEIN; STROMELYSIN; SYNDECAN 4; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; VITRONECTIN; 1,3 BENZODIOXOLE DERIVATIVE; 2-(4-MORPHOLINYL)-8-PHENYL-4H-1-BENZOPYRAN-4-ONE; 2-(5-BENZO(1,3)DIOXOL-5-YL-2-TERT-BUTYL-3H-IMIDAZOL-4-YL)-6-METHYLPYRIDINE HYDROCHLORIDE; CHROMONE DERIVATIVE; CULTURE MEDIUM; IMIDAZOLE DERIVATIVE; MORPHOLINE DERIVATIVE; PYRIDINE DERIVATIVE; SMAD2 PROTEIN, HUMAN;

AMNIOTIC FLUID CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; COLLAGEN SYNTHESIS; COLONY FORMING UNIT; CONTROLLED STUDY; CULTURE MEDIUM; ENZYME LINKED IMMUNOSORBENT ASSAY; FIBROBLAST; GENE EXPRESSION; HUMAN; HUMAN CELL; HYPOXIA; MESENCHYMAL STEM CELL; NONHUMAN; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TISSUE REGENERATION; WESTERN BLOTTING; WOUND HEALING; AMNION FLUID; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL CULTURE; CELL HYPOXIA; CELL MOTION; CYTOLOGY; DRUG EFFECTS; FEMALE; INSTITUTE FOR CANCER RESEARCH MOUSE; MESENCHYMAL STROMA CELL; METABOLISM; MOUSE; PATHOLOGY; PHARMACOLOGY; SIGNAL TRANSDUCTION; SKIN;

AMNIOTIC FLUID; ANIMALS; BENZODIOXOLES; CELL HYPOXIA; CELL MOVEMENT; CELL PROLIFERATION; CELLS, CULTURED; CHROMONES; CULTURE MEDIA, CONDITIONED; FEMALE; FIBROBLASTS; HUMANS; IMIDAZOLES; MESENCHYMAL STROMAL CELLS; MICE; MICE, INBRED ICR; MORPHOLINES; PYRIDINES; SIGNAL TRANSDUCTION; SKIN; SMAD2 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; WOUND HEALING;

EID: 84891795530     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms15010605     Document Type: Article

References (56)

1. Martin, P. Wound healing-aiming for perfect skin regeneration. Science 1997, 276, 75-81.
2. Falanga, V. Wound healing and its impairment in the diabetic foot. Lancet 2005, 366, 1736-1743.
3. Singer, A.J.; Clark, R.A.F. Cutaneous wound healing. N. Engl. J. Med. 1999, 341, 738-746.
4. Pillouer-Prost, A.L. Fibroblasts: What's new in cellular biology? J. Cosmet. Laser Ther. 2003, 5, 232-238.
5. Kim, S.; Park, S.; Sung, J-.; Yang, JM.; Park, SB.; Kwak, J.; Park, S. Wound healing effect of adipose-derived stem cells: A critical role of secretory factors on human dermal fibroblasts. J. Dermatol. Sci. 2007, 48, 15-24.
6. Tsai, M.S.; Lee, J.L.; Chang, Y.J.; Hwang, S.M. Isolation of human multipotent mesenchymal stem cells from second-trimester amniotic fluid using a novel two-stage culture protocol. Hum. Reprod. 2004, 19, 1450-1456.
7. Prusa, A.-R.; Hengstschlager, M. Amniotic fluid cells and human stem cell rese rA new connection. Med. Sci. Monit. 2002, 8, RA253-RA257.
8. Tsai, M.-S.; Hwang, S.-M.; Tsai, Y-L.; Cheng, F.-C.; Lee, J-L.; Chang, Y.-J. Clonal amniotic fluid-derived stem cells express characteristics of both mesenchymal and neural stem cells. Biol. Reprod. 2006, 74, 545-551.
9. De Coppi, P.; Bartsch, G.; Siddiqui, M.M.; Xu, T.; Santos, C.C.; Perin, L.; Mostoslavsky, G.; Serre, A.C.; Snyder, E.Y.; Yoo, J.J. Isolation of amniotic stem cell lines with potential for therapy. Nat. Biotechnol. 2007, 25, 100-106.
10. Scherjon, S.A.; Kleijburg-van Keur, C.; Noort, W.A.; Claas, F.H.; Willemze, R.; Fibbe, W.E.; Kanhai, H.H. Amniotic fluid as a novel source of mesenchymal stem cells for therapeutic transplantation. Blood 2003, 102, 1548-1549.
11. Horwitz, E.M.; Gordon, P.L.; Koo, W.K.; Marx, J.C.; Neel, M.D.; McNall, R.Y.; Lul, Hofmann T. Isolated allogeneic bone der ved mesenchymal cells engraft and stimulate growth in children with osteogenesis imperfecta: Implications for cell therapy of bone. Proc. Natl. Acad. Sci. USA 2002, 99, 8932-8937.
12. Bajada, S.; Harrison, P.; Ashton, B.; Cass-Pullicino, V.; Ashammakhi, N.; Richardson, J. Successful treatment of refractory tibial nonunion using calcium sulphate and bone marrow stromal cell implantation. J. Bone Joint Surg. Br. 2007, 89, 1382-1386.
13. Chen, S.-L.; Fang, W.-W.; Ye, F.; Liu, Y.H.; Qian, J.; Shan, S.J.; Zhang, J.-J.; Chunhua, R.Z.; Liao, L-M.; Lin, S. Effect on left ventricular function of intracoronary transplantation of autologous bone marrow mesenchymal stem cell in patients with acute myocardial infarction. Am. J. Cardiol. 2004, 94, 92-95.
14. Katritsis, D.G.; Sotiropoulou, P.A.; Karvouni, E.; Karabinos, I.; Korovesis, S.; Perez, S.A.; Voridis, E.M.; Papamichail, M. Transcoronary transplantation of autologous mesenchymal stem cells and endothelial progenitors into infarcted human myocardium. Catheter. Cardiovasc. Interv. 2005, 65, 321-329.
15. Chernykh, E.; Shevela, E.Y.; Leplina, O.Y.; Tikhonova, M.; Ostanin, A.; Kulagin, A.; Pronkina, N.; Muradov, Z.M.; Stupak, V.; Kozlov, V. Characteristics of bone marrow cells under conditions of impaired innervation in patients with spinal trauma. Bull. Exp. Biol. Med. 2006, 141, 117-120.
16. Fei, X.; Jiang, S.; Zhang, S.; Li, Y.; Ge, J.; He, B.; Goldstein, S.; Ruiz, G. Isolation, culture, and identification of amniotic fluid-derived mesenchymal stem cells. Cell Biochem. Biophys. 2013, 67, 689-694.
17. Chen, L.; Tredget, E.E.; Wu, P.Y.; Wu, Y. Paracrine facto o f mesenchymal stem cells recruit macrophages and endothelial lineage cells and enhance wound healing. PLoS One 2008, 3, e1886.
18. Walter, M.; Wright, K.T.; Fuller, H.; MacNeil, S.; Johnson, W.E.B. Mesenchymal stem cell-conditioned medium accelerates skinwound healing: Anin vitro study of fibroblast and keratinocyte scratch assays. Exp. Cell Res. 2010, 316, 1271-1281.
19. Yoon, B.S.; Moon, J.-H.; Jun, E.K.; Kim, J.; Maeng, I.; Kim, J.S.; Lee, J.H.; Baik, C.S.; Kim, A.; Cho, K.S. Secretory profiles and wound healing effects of human amniotdce rivfedi dmesenchymal stem cells. Stem Cells Dev. 2009, 19, 887-902.
20. Lee, E.Y.; Xia, Y.; Kim, W., Kim, M.H.; Kim, T.H.; Kim, K.J.; Park, B.S.; Sung, J.H. Hypoxia-enhanced wound-healing function of adipos-derived stem cells: Increase in stem cell proliferation and up-regulation of VEGF and bFGF. Wound Repair Regen. 2009, 17, 540-547.
21. Packer, L.; Fuehr, K. Low oxygen concentration extends the lifespan of cultured human diploid cells. Nature 1977, 267, 423-425.
22. Lash, G.E.; Fitzpatrick, T.E.; Graham, C.H. Effect of hypoxia on cellular adhesion to vitronectin and fibronectin. Biochem. Biophys. Res. Commun. 2001, 287, 622-629.
23. Carmeliet, P.; Dor, Y.; Herbert, MJ.; Fukumura, D.; Brusselmans, K.; Dewerchin, M.; Neeman, M.; Bono, F.; Abramovitch, R.; Maxwell, P. Role of-1α Iin hypoxia-mediated apoptosis, cell proliferation and tumour angiogenesis. Nature 1998, 394, 485-490.
24. Loike, J.; Cao, L.; Brett, J.; Ogawa, S.; Silverstein, S.; Stern, D. Hypoxia inducese glucose transporter expression in endothelial cells. Am. J. Physiol. Cell Physiol. 1992, 263, C326-C333.
25. Horino, Y.; Takahashi, S.; Miura, T.; Takahashi, Y. Prolonged hypoxia accelerates th posttranscriptional process of collagen synthesis in cultured fibr s.l Life Sc. 2002, 71, 3031-3045.
26. Minchenko, A.; Salceda, S.; Bauer, T.; Caro, J. Hypoxia regulatory elements of the human vascular endothelial growth factor gene. Cell. Mol. Biol. Res. 1994, 40, 35-39.
27. Lennon, D.P.; Edmison, J.M.; Caplan, A.I. Cultivation of rat de ived mesenchymal stem cells in reduced oxygen tension: Effects inn vitro and in vivo osteochondrogenesis. J. Cell. Physiol. 2001, 187, 345-355.
28. Crisostomo, P.R.; Wang, Y.; Markel, T.A.; Wang, M.; Lahm, T.; Meldrum, D.R. Human mesenchymal stem cells stimulated by TN-Fα, LPS, or hypoxia produce growth factors by an NFκB-but not JNK-dependent mechanism. Am. J. Physiol. Cell Physiol. 2008, 294, C675-C682.
29. Moon, J.-H.; Kwak, S.S.; Park, G.; Jung, HY-.; Yoon, B.S.; Park, J.; Ryu, K.S.; Choi, C.; Maeng, I.; Kim, B. Isolation and characterization of multipotent hu d erivkedl oid mesenchymal-like stem cells. Stem Cells Dev. 2008, 17, 713-724.
30. Colter, D.C.; Sekiya, I.; Prockop, D.J. Identification of a subpopulation of rapidly se-renewing and multipotential adult stem cells in colonies of human marrow stromal cells P roc. Natl. Acad. Sci. USA 2001, 98, 7841-7845.
31. Pittenger, M.F.; Mackay, A.M.; Beck, S.C.; Jaiswal, R.K.; Douglas, R.; Mosca, J. Moorman, M.A.; Simonetti, D.W.; Craig, S.; Marshak, D.R. Multilineage potential of adult human mesenchymal stem cells. Science 1999, 284, 143-147.
32. Young, H.E.; Steele, T.A.; Bray, R.A.; Hudson, J.; Floyd, J.A.; Hawkins, K.; Thomas, K.; Austin, T.; Edwards, C.; Cuzzourt, J. Human reserve pluripotent mesenchymal stem cells are present in the connective tissues of skeletal muscle and dermis derived from fetal, adult, and geriatric donors. Anat. Rec. 2001, 264, 51-62.
33. Kern, S.; Eichler, H.; Stoeve, J.; Külter, H.; Bieback, K. Comparative analysis of mesenchymal stem cells from bone marrow, umbilical cord blood, or adipose tis, Stem Cells 2006, 24, 1294-1301.
34. Park, G.; Yoon, B.S.; Moon, J.H.; Kim, B.; Jun, E.K.; Oh, S.; Kim, H.; Song, H.J.; Noh, J.Y.; Oh, C. Green tea polyphenol epigallocategaill-ate-suppresses collagen product ion and proliferation in keloid fibroblasts via inhibition of the S ing3-spa hway. J. Investig. Dermatol. 2008, 128, 2429-2441.
35. Rosch, R.; Junge, K.; Binnebösel, M.; Mirgartz, N.; Klinge, U.; Schumpelick, V. Improved abdominal wall wound healing by helium pneumoperitoneum. Surg. Endosc. 2006, 20, 1892-1896.
36. Jung, S.-A.; Lee, H.K.; Yoon, J.S.; Kim, S.-J.; Kim, C.Y.; Song, H.; Hwang, K.-C.; Lee, J.B.; Lee, J.H. Upregulation of TGF-β-induced tissue transglutaminase expression by PI3K-Akt pathway activation in human subconjunctival fibroblasts. Investig. Ophthalmol. Vis. Sci. 2007, 48, 1952-1958.
37. Galiano, R.D.; Michaels, V.; Dobryansky, M.; Levine, J.P.; Gurtner, G.C. Quantitative and reproducible murine model of excisional wound healing. Wound Repair Regen. 2004, 12, 485-492.
38. Yang, J.D.; Choi, D.S.; Cho, Y.K.; Kim, T.K.; Lee, J.W.; Choi, K.Y.; Chung, H.Y.; Cho, B.C.; Byun, J.S. Effect of amniotic fluid stem cells and amniotic fluid cells on the wound healing process in a white rat model. Arch. Plast. Surg. 2013, 40, 496-504.
39. Lord-Dufour, S.; Copland, I.B.; Levros, L.C.; Post, M.; Das, A.; Khosla, C.; Galipeau, J.; Rassart, E.; Annabi, B. Evidence for transcriptional regulation of the osphate transporter by HIF-1α: Targeting G6PT with mumbaistatin analogs in hypoxic mesenchymal stromal cells. Stem Cells 2009, 27, 489-497.
40. Tsai, C.-C.; Chen, Y.-J.; Yew, T.-L.; Chen, L.-L.; Wang, J.-Y.; Chiu, C.-H.; Hung, S.-C. Hypoxia inhibits senescence and maintains mesenchymal stem cell properties through down-regulation of E2A-p21 by HIF-TWIST. Blood 2011, 117, 459-469.
41. D'Ippolito, G.; Diabira, S.; Howard, G.A.; Roos, B.A.; Schiller, P.C. Low oxygen tension inhibits osteogenic differentiation and enhances stemness of human MIAMI cells. Bone 2006, 39, 513-522.
42. Rosova, I.; Dao, M.; Capoccia, B.; Link, D.; Nolta, J.A. Hypoxic preconditioning results in increased motility and improved therapeutic potential of human mesenchymal stem cells. Stem Cells 2008, 26, 2173-2182.
43. Kwon, D.S.; Kwon, C.H.; Kim, J.H.; Woo, J.S.; Jung, J.S.; Kim, Y.K. Signal transduction of MEK/ERK and PI3K/Akt ativation by hypoxia/reoxygenation in renal epithelial cellE ur. J. Cell Biol. 2006, 85, 1189-1199.
44. Liu, H.; Xue, W.; Ge, G.; Luo, X.; Li, Y.; Xiang, H.; Ding, X.; Tian, P.; Tia Hypoxic preconditioning advances CXCR4 and CXCR7 expression by activating HIF-1α in MSCs. Biochem. Biophys. Res. Commun. 2010, 401, 509-515.
45. Chen, J.; Crawford, R.; Chen, C.; Xiao, Y. The key regulatory roles of the PI3K/Akt signaling pathway in the functionalities of mesenchymal stem cells and applications in tissue regeneration. Tissue Eng. 2013, 19, 516-528.
46. Kinnaird, T.; Stabile, E.; Burnett, M.; Lee, C.; Barr, S.; Fuchs, S.; Epstein, S. Marerived stromal cells express genes encoding a broad spectrum of arteriogenic cytokines and promote in vitro and in vivo arteriogenesis through paracrine mechanisms. Circ. Res. 2004, 94, 678-685.
47. Lu, Y.; Azad, N.; Wang, L.; Iyer, A.K.; Castranova, V.; Jha G, R oja-nasakul, Y. Phosphatidylinositol-3-kinase/Akt regulates bleomycinduced fibroblast proliferation and collagen production. Am. J. Respir. Cell Mol. Biol. 2010, 42, 432-441.
48. Meckmongkol, T.T.; Harmon, R.; McKeown-Longo, P.; van de Water, L. The fibronectin synergy site modulates TGF-β-dependent fibroblast contraction. Biochem. Biophys. Res. Commun. 2007, 360, 709-714.
49. Hamada, K.; Sasaki, T.; Koni, P.A.; Natsui, M.; Kishimoto, H.; Sasaki, J.; Yajima, N.; Horie, Y.; Hasegawa, G.; Naito, M. The PTEN/PI3K pathway governs normal vascular development and tumor angiogenesis. Genes Dev. 2005, 19, 2054-2065.
50. Shih, N.R.; Jo, O.D.; Yanagawa, N. Effects of PHEX antisense in human osteoblast cells. J. Am. Soc. Nephrol. 2002, 13, 394-399.
51. Furstoss, O.; Dorey, K.; Simon, V.; Barilà, D.; Superti-Furga, G.; Roche, S. c-Abl is an effector of Src for growth factor-induced c-myc expression and DNA synthesis. EMBO J. 2002, 21, 514-524.
52. Mairet-Coello, G.; Tury, A.; DiCiccoBloom, E. Insulin-like growth factor-1 promotes G1/S cell cycle progression through bidirectional regulation of cyclins and cyclindependent kinase inhibitors via the phosphatidylinositol 3-kinase/Akt pathway in developing rat cerebral cortex. J. Neurosci. 2009, 29, 775-788.
53. Kho, Y.; Kim, S.; Yoon, B.S.; Moon, J.-H.; Kim, B.; Kwak, S.; Woo, J.; Oh, S.; Hong, K.; Kim, S. Induction of serum amyloid A genes is associated with growth and apoptosis of HC11 mammary epithelial cells. Biosci. Biotechnol. Biochem. 2008, 72, 70-81.
54. Miller, G.E.; Chen, E. Life stress and diminished expression of genes encoding glucocorticoid receptor and beta2-adrenergic receptor in children with asthma. Proc. Natl. Acad. Sci. USA 2006, 103, 5496-5501.
55. Neuhoff, S.; Moers, J.; Rieks, M.; Grunwald, T.; Jensen, A.; Dermietzel, R.; Meier, C Proliferation, differentiation, and cytokine secretion of human umbilical cord blood-derived mononuclear cells in vitro. Exp. Hematol. 2007, 35, 1119-1131.
56. Yoon, B.S.; Yoo, S.J.; Lee, J.E.; You, S.; Lee, H.T.; Yoon, H.S. Enhanced differentiation of human embryonic stem cells into cardiomyocytes by combining hanging drop culture and-5azacytidine treatment. Differentiation 2006, 74, 149-159.