Role of notch signaling in the maintenance of human mesenchymal stem cells under hypoxic conditions

Stem Cells and Development

Volumn 23, Issue 18, 2014, Pages 2211-2224

  Moriyama, Hiroyuki ^a   Moriyama, Mariko ^a   Isshi, Haruki ^a   Ishihara, Shin ^a   Okura, Hanayuki ^b   Ichinose, Akihiro ^c   Ozawa, Toshiyuki ^d   Matsuyama, Akifumi ^b   Hayakawa, Takao ^a  

^a KINKI UNIVERSITY   (Japan)

^b NATIONAL INSTITUTE OF BIOMEDICAL INNOVATION   (Japan)

^c KOBE UNIVERSITY HOSPITAL   (Japan)

^d OSAKA CITY UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA SECRETASE INHIBITOR; GLUCOSE TRANSPORTER 3; HYPOXIA INDUCIBLE FACTOR; LACTIC ACID; NOTCH1 RECEPTOR; OXYGEN; TRANSCRIPTION FACTOR HES 1; HYPOXIA INDUCIBLE FACTOR 1ALPHA; NOTCH RECEPTOR;

ADULT; ARTICLE; CELL PROLIFERATION; CELL SURVIVAL; FEMALE; GENE EXPRESSION; GLUCOSE INTAKE; GLYCOLYSIS; HUMAN; HUMAN CELL; HUMAN TISSUE; HYPOXIA; MALE; MESENCHYMAL STEM CELL; SENESCENCE; UPREGULATION; CELL AGING; CELL CULTURE; CELL DIFFERENTIATION; CELL HYPOXIA; CELL LINEAGE; CYTOLOGY; DRUG EFFECTS; MESENCHYMAL STROMA CELL; METABOLISM; MIDDLE AGED; SIGNAL TRANSDUCTION; YOUNG ADULT;

ADULT; CELL AGING; CELL DIFFERENTIATION; CELL HYPOXIA; CELL LINEAGE; CELL PROLIFERATION; CELLS, CULTURED; FEMALE; GLYCOLYSIS; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MALE; MESENCHYMAL STROMAL CELLS; MIDDLE AGED; OXYGEN; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION; YOUNG ADULT;

EID: 84906993111     PISSN: 15473287     EISSN: 15578534     Source Type: Journal    
DOI: 10.1089/scd.2013.0642     Document Type: Article

References (57)

1. Okura H, H Komoda, A Saga, A Kakuta-Yamamoto, Y Hamada, Y Fumimoto, CM Lee, A Ichinose, Y Sawa and A Matsuyama. (2010). Properties of hepatocyte-like cell clusters from human adipose tissue-derived mesenchymal stem cells. Tissue Eng Part C Methods 16:761-770.
2. Okura H, A Matsuyama, CM Lee, A Saga, A Kakuta-Yamamoto, A Nagao, N Sougawa, N Sekiya, K Takekita, et al. (2010). Cardiomyoblast-like cells differentiated from human adipose tissue-derived mesenchymal stem cells improve left ventricular dysfunction and survival in a rat myocardial infarction model. Tissue Eng Part C Methods 16:417-425.
3. Okura H, H Komoda, Y Fumimoto, CM Lee, T Nishida, Y Sawa and A Matsuyama. (2009). Transdifferentiation of human adipose tissue-derived stromal cells into insulinproducing clusters. J Artif Organs 12:123-130.
4. Safford KM, SD Safford, JM Gimble, AK Shetty and HE Rice. (2004). Characterization of neuronal/glial differentiation of murine adipose-derived adult stromal cells. Exp Neurol 187:319-328.
5. Leu S, YC Lin, CM Yuen, CH Yen, YH Kao, CK Sun and HK Yip. (2010). Adipose-derived mesenchymal stem cells markedly attenuate brain infarct size and improve neurological function in rats. J Transl Med 8:63.
6. Ikegame Y, K Yamashita, S Hayashi, H Mizuno, M Tawada, F You, K Yamada, Y Tanaka, Y Egashira, et al. (2011). Comparison of mesenchymal stem cells from adipose tissue and bone marrow for ischemic stroke therapy. Cytotherapy 13:675-685.
7. Tan B, Z Luan, X Wei, Y He, G Wei, BH Johnstone, M Farlow and Y Du. (2011). AMP-activated kinase mediates adipose stem cell-stimulated neuritogenesis of PC12 cells. Neuroscience 181:40-47.
8. Reid AJ, M Sun, M Wiberg, S Downes, G Terenghi and PJ Kingham. (2011). Nerve repair with adipose-derived stem cells protects dorsal root ganglia neurons from apoptosis. Neuroscience 199:515-522.
9. Rehman J, D Traktuev, J Li, S Merfeld-Clauss, CJ Temm-Grove, JE Bovenkerk, CL Pell, BH Johnstone, RV Considine and KL March. (2004). Secretion of angiogenic and antiapoptotic factors by human adipose stromal cells. Circulation 109:1292-1298.
10. Lee EY, Y Xia, WS Kim, MH Kim, TH Kim, KJ Kim, BS Park and JH Sung. (2009). Hypoxia-enhanced woundhealing function of adipose-derived stem cells: increase in stem cell proliferation and up-regulation of VEGF and bFGF. Wound Repair Regen 17:540-547.
11. Moriyama M, H Moriyama, A Ueda, Y Nishibata, H Okura, A Ichinose, A Matsuyama and T Hayakawa. (2012). Human adipose tissue-derived multilineage progenitor cells exposed to oxidative stress induce neurite outgrowth in PC12 cells through p38 MAPK signaling. BMC Cell Biol 13:21.
12. Wu H, Z Ye and RI Mahato. (2011). Genetically modified mesenchymal stem cells for improved islet transplantation. Mol Pharm 8:1458-1470.
13. Wagner W, P Horn, M Castoldi, A Diehlmann, S Bork, R Saffrich, V Benes, J Blake, S Pfister, V Eckstein and AD Ho. (2008). Replicative senescence of mesenchymal stem cells: a continuous and organized process. PLoS One 3: e2213.
14. Kondoh H, ME Lleonart, Y Nakashima, M Yokode, M Tanaka, D Bernard, J Gil and D Beach. (2007). A high glycolytic flux supports the proliferative potential of murine embryonic stem cells. Antioxid Redox Signal 9:293-299.
15. Prigione A, B Fauler, R Lurz, H Lehrach and J Adjaye. (2010). The senescence-related mitochondrial/oxidative stress pathway is repressed in human induced pluripotent stem cells. Stem Cells 28:721-733.
16. Varum S, AS Rodrigues, MB Moura, O Momcilovic, C At Easley, J Ramalho-Santos, B Van Houten and G Schatten. (2011). Energy metabolism in human pluripotent stem cells and their differentiated counterparts. PLoS One 6:e20914.
17. Warburg O, F Wind and E Negelein. (1927). The Metabolism of tumors in the body. J Gen Physiol 8:519-530.
18. Kondoh H. (2008). Cellular life span and the Warburg effect. Exp Cell Res 314:1923-1928.
19. Kondoh H, ME Lleonart, J Gil, J Wang, P Degan, G Peters, D Martinez, A Carnero and D Beach. (2005). Glycolytic enzymes can modulate cellular life span. Cancer Res 65: 177-185.
20. Beckman KB and BN Ames. (1998). The free radical theory of aging matures. Physiol Rev 78:547-581.
21. Ezashi T, P Das and RM Roberts. (2005). Low O2 tensions and the prevention of differentiation of hES cells. Proc Natl Acad Sci U S A 102:4783-4788.
22. Forristal CE, KL Wright, NA Hanley, RO Oreffo and FD Houghton. (2010). Hypoxia inducible factors regulate pluripotency and proliferation in human embryonic stem cells cultured at reduced oxygen tensions. Reproduction 139:85-97.
23. Yoshida Y, K Takahashi, K Okita, T Ichisaka and S Yamanaka. (2009). Hypoxia enhances the generation of induced pluripotent stem cells. Cell Stem Cell 5:237-241.
24. Takubo K, N Goda, W Yamada, H Iriuchishima, E Ikeda, Y Kubota, H Shima, RS Johnson, A Hirao, M Suematsu and T Suda. (2010). Regulation of the HIF-1alpha level is essential for hematopoietic stem cells. Cell Stem Cell 7:391-402.
25. Santilli G, G Lamorte, L Carlessi, D Ferrari, L Rota Nodari, E Binda, D Delia, AL Vescovi and L De Filippis. (2010). Mild hypoxia enhances proliferation and multipotency of human neural stem cells. PLoS One 5:e8575.
26. Tsai CC, YJ Chen, TL Yew, LL Chen, JY Wang, CH Chiu and SC Hung. (2011). Hypoxia inhibits senescence and maintains mesenchymal stem cell properties through down-regulation of E2A-p21 by HIF-TWIST. Blood 117: 459-469.
27. Takubo K, G Nagamatsu, CI Kobayashi, A Nakamura-Ishizu, H Kobayashi, E Ikeda, N Goda, Y Rahimi, RS Johnson, et al. (2013). Regulation of glycolysis by pdk functions as a metabolic checkpoint for cell cycle quiescence in hematopoietic stem cells. Cell Stem Cell 12: 49-61.
28. Grayson WL, F Zhao, R Izadpanah, B Bunnell and T Ma. (2006). Effects of hypoxia on human mesenchymal stem cell expansion and plasticity in 3D constructs. J Cell Physiol 207:331-339.
29. Wang DW, B Fermor, JM Gimble, HA Awad and F Guilak. (2005). Influence of oxygen on the proliferation and metabolism of adipose derived adult stem cells. J Cell Physiol 204:184-191.
30. Moriyama M, M Osawa, SS Mak, T Ohtsuka, N Yamamoto, H Han, V Delmas, R Kageyama, F Beermann, L Larue and S Nishikawa. (2006). Notch signaling via Hes1 transcription factor maintains survival of melanoblasts and melanocyte stem cells. J Cell Biol 173:333-339.
31. Chiba S. (2006). Notch signaling in stem cell systems. Stem Cells 24:2437-2447.
32. Okura H, A Saga, Y Fumimoto, M Soeda, M Moriyama, H Moriyama, K Nagai, CM Lee, S Yamashita, et al. (2011). Transplantation of human adipose tissue-derived multilineage progenitor cells reduces serum cholesterol in hyperlipidemic Watanabe rabbits. Tissue Eng Part C Methods 17:145-154.
33. Saga A, H Okura, M Soeda, J Tani, Y Fumimoto, H Komoda, M Moriyama, H Moriyama, S Yamashita, et al. (2011). HMG-CoA reductase inhibitor augments the serum total cholesterol-lowering effect of human adipose tissuederived multilineage progenitor cells in hyperlipidemic homozygous Watanabe rabbits. Biochem Biophys Res Commun 412:50-54.
34. Moriyama H, M Moriyama, K Sawaragi, H Okura, A Ichinose, A Matsuyama and T Hayakawa. (2013). Tightly regulated and homogeneous transgene expression in human adipose-derived mesenchymal stem cells by lentivirus with tet-off system. PLoS One 8:e66274.
35. Sekiya I, BL Larson, JR Smith, R Pochampally, JG Cui and DJ Prockop. (2002). Expansion of human adult stem cells from bone marrow stroma: conditions that maximize the yields of early progenitors and evaluate their quality. Stem Cells 20:530-541.
36. Wagner W, F Wein, A Seckinger, M Frankhauser, U Wirkner, U Krause, J Blake, C Schwager, V Eckstein, W Ansorge and AD Ho. (2005). Comparative characteristics of mesenchymal stem cells from human bone marrow, adipose tissue, and umbilical cord blood. Exp Hematol 33:1402-1416.
37. Hass R, C Kasper, S Bohm and R Jacobs. (2011). Different populations and sources of human mesenchymal stem cells (MSC): A comparison of adult and neonatal tissue-derived MSC. Cell Commun Signal 9:12.
38. Gustafsson MV, X Zheng, T Pereira, K Gradin, S Jin, J Lundkvist, JL Ruas, L Poellinger, U Lendahl and M Bondesson. (2005). Hypoxia requires notch signaling to maintain the undifferentiated cell state. Dev Cell 9:617-628.
39. Zheng X, S Linke, JM Dias, X Zheng, K Gradin, TP Wallis, BR Hamilton, M Gustafsson, JL Ruas, et al. (2008). Interaction with factor inhibiting HIF-1 defines an additional mode of cross-coupling between the Notch and hypoxia signaling pathways. Proc Natl Acad Sci U S A 105:3368-3373.
40. Pietras A, K von Stedingk, D Lindgren, S Pahlman and H Axelson. (2011). JAG2 induction in hypoxic tumor cells alters Notch signaling and enhances endothelial cell tube formation. Mol Cancer Res 9:626-636.
41. Bedogni B, JA Warneke, BJ Nickoloff, AJ Giaccia and MB Powell. (2008). Notch1 is an effector of Akt and hypoxia in melanoma development. J Clin Invest 118:3660-3670.
42. Beitner-Johnson D, RT Rust, TC Hsieh and DE Millhorn. (2001). Hypoxia activates Akt and induces phosphorylation of GSK-3 in PC12 cells. Cell Signal 13:23-27.
43. Culver C, A Sundqvist, S Mudie, A Melvin, D Xirodimas and S Rocha. (2010). Mechanism of hypoxia-induced NFkappaB. Mol Cell Biol 30:4901-4921.
44. Rohwer N, C Dame, A Haugstetter, B Wiedenmann, K Detjen, CA Schmitt and T Cramer. (2010). Hypoxia-inducible factor 1alpha determines gastric cancer chemosensitivity via modulation of p53 and NF-kappaB. PLoS One 5:e12038.
45. Espinosa L, S Cathelin, T D'Altri, T Trimarchi, A Statnikov, J Guiu, V Rodilla, J Ingles-Esteve, J Nomdedeu, et al. (2010). The Notch/Hes1 pathway sustains NF-kappaB activation through CYLD repression in T cell leukemia. Cancer Cell 18:268-281.
46. Beverly LJ, DW Felsher and AJ Capobianco. (2005). Suppression of p53 by Notch in lymphomagenesis: implications for initiation and regression. Cancer Res 65:7159-7168.
47. Kim SB, GW Chae, J Lee, J Park, H Tak, JH Chung, TG Park, JK Ahn and CO Joe. (2007). Activated Notch1 interacts with p53 to inhibit its phosphorylation and transactivation. Cell Death Differ 14:982-991.
48. Landor SK, AP Mutvei, V Mamaeva, S Jin, M Busk, R Borra, TJ Gronroos, P Kronqvist, U Lendahl and CM Sahlgren. (2011). Hypo- and hyperactivated Notch signaling induce a glycolytic switch through distinct mechanisms. Proc Natl Acad Sci U S A 108:18814-18819.
49. Ciofani M and JC Zuniga-Pflucker. (2005). Notch promotes survival of pre-T cells at the beta-selection checkpoint by regulating cellular metabolism. Nat Immunol 6: 881-888.
50. Welford SM, B Bedogni, K Gradin, L Poellinger, M Broome Powell and AJ Giaccia. (2006). HIF1alpha delays premature senescence through the activation of MIF. Genes Dev 20:3366-3371.
51. Zhou D, J Xue, JC Lai, NJ Schork, KP White and GG Haddad. (2008). Mechanisms underlying hypoxia tolerance in Drosophila melanogaster: hairy as a metabolic switch. PLoS Genet 4:e1000221.
52. Funes JM, M Quintero, S Henderson, D Martinez, U Qureshi, C Westwood, MO Clements, D Bourboulia, RB Pedley, S Moncada and C Boshoff. (2007). Transformation of human mesenchymal stem cells increases their dependency on oxidative phosphorylation for energy production. Proc Natl Acad Sci U S A 104:6223-6228.
53. Kawauchi K, K Araki, K Tobiume and N Tanaka. (2008). p53 regulates glucose metabolism through an IKK-NFkappaB pathway and inhibits cell transformation. Nat Cell Biol 10:611-618.
54. Carter KL, E Cahir-McFarland and E Kieff. (2002). Epstein-barr virus-induced changes in B-lymphocyte gene expression. J Virol 76:10427-10436.
55. Ak P and AJ Levine. (2010). p53 and NF-kappaB: different strategies for responding to stress lead to a functional antagonism. FASEB J 24:3643-3652.
56. Prasad SM, M Czepiel, C Cetinkaya, K Smigielska, SC Weli, H Lysdahl, A Gabrielsen, K Petersen, N Ehlers, et al. (2009). Continuous hypoxic culturing maintains activation of Notch and allows long-term propagation of human embryonic stem cells without spontaneous differentiation. Cell Prolif 42:63-74.
57. Bash J, WX Zong, S Banga, A Rivera, DW Ballard, Y Ron and C Gelinas. (1999). Rel/NF-kappaB can trigger the Notch signaling pathway by inducing the expression of Jagged1, a ligand for Notch receptors. EMBO J 18:2803-2811.