394
Views
20
CrossRef citations to date
0
Altmetric
Original Articles

Hypoxia reduces the osteogenic differentiation of peripheral blood mesenchymal stem cells by upregulating Notch-1 expression

ORCID Icon, ORCID Icon, , , , , , & show all
Pages 583-596 | Received 08 Aug 2018, Accepted 02 Apr 2019, Published online: 28 May 2019

References

  • Wu G, Pan M, Wang X, Wen J, Cao S, Li Z, Li Y, Qian C, Liu Z, Wu W, Zhu L, Guo J. Osteogenesis of peripheral blood mesenchymal stem cells in self assembling peptide nanofiber for healing critical size calvarial bony defect. Sci Rep. 2015;5:16681. doi:10.1038/srep16681.
  • Yang L, Zhu L, Dong W, Cao Y, Rong Z. Oxygen-generating scaffolds: a new strategy for bone tissue engineering. Bone. 2013;57:322–323. doi:10.1016/j.bone.2013.07.034.
  • Brighton CT, Krebs AG. Oxygen tension of healing fractures in the rabbit. J Bone Joint Surg Am. 1972;54:323–332. doi:10.2106/00004623-197254020-00010.
  • Kofoed H, Sjøntoft E, Siemssen SO, Olesen HP. Bone marrow circulation after osteotomy. Blood flow, pO2, pCO2, and pressure studied in dogs. Acta Orthop Scand. 1985;56:400–403. doi:10.3109/17453678508994357.
  • Harrison JS, Rameshwar P, Chang V, Bandari P. Oxygen saturation in the bone marrow of healthy volunteers. Blood. 2002;99:394. doi:10.1182/blood.V99.1.394.
  • Buizer AT, Bulstra SK, Veldhuizen AG, Kuijer R. The balance between proliferation and transcription of angiogenic factors of mesenchymal stem cells in hypoxia. Connect Tissue Res. 2018;59:12–20. doi:10.1080/03008207.2017.1412432.
  • Fotia C, Massa A, Boriani F, Baldini N, Granchi D. Hypoxia enhances proliferation and stemness of human adipose-derived mesenchymal stem cells. Cytotechnology. 2015;67:1073–1084. doi:10.1007/s10616-014-9731-2.
  • Burian E, Probst F, Palla B, Riedel C, Mm S, Cornelsen M, König F, Schieker M, Otto S. Effect of hypoxia on the proliferation of porcine bone marrow-derived mesenchymal stem cells and adipose-derived mesenchymal stem cells in 2- and 3-dimensional culture. J Craniomaxillofac Surg. 2017;45:414–419.
  • Yu Y, Yin Y, Wu RX, He XT, Zhang XY, Chen FM. Hypoxia and low-dose inflammatory stimulus synergistically enhance bone marrow mesenchymal stem cell migration. Cell Prolif. 2017;50. doi:10.1111/cpr.12368.
  • Ciapetti G, Granchi D, Fotia C, Savarino L, Dallari D, Del Piccolo N, Donati DM, Baldini N. Effects of hypoxia on osteogenic differentiation of mesenchymal stromal cells used as a cell therapy for avascular necrosis of the femoral head. Cytotherapy. 2016;18:1087–1099. doi:10.1016/j.jcyt.2016.06.005.
  • Chung DJ, Hayashi K, Toupadakis CA, Wong A, Yellowley CE. Osteogenic proliferation and differentiation of canine bone marrow and adipose tissue derived mesenchymal stromal cells and the influence of hypoxia. Res Vet Sci. 2012;92:66–75. doi:10.1016/j.rvsc.2010.10.012.
  • Hoch AI, Leach JK. Concise review: optimizing expansion of bone marrow mesenchymal stem/stromal cells for clinical applications. Stem Cells Transl Med. 2014;3:643–652. doi:10.5966/sctm.2013-0196.
  • Ma T, Grayson WL, Fröhlich M, Vunjak-Novakovic G. Hypoxia and stem cell-based engineering of mesenchymal tissues. Biotechnol Prog. 2009;25:32–42. doi:10.1002/btpr.128.
  • Mazumdar J, Dondeti V, Simon MC. Hypoxia-inducible factors in stem cells and cancer. J Cell Mol Med. 2009;13:4319–4328. doi:10.1111/j.1582-4934.2009.00963.x.
  • Salim A, Nacamuli RP, Morgan EF, Giaccia AJ, Longaker MT. Transient changes in oxygen tension inhibit osteogenic differentiation and Runx2 expression in osteoblasts. J Biol Chem. 2004;279:40007–40016. doi:10.1074/jbc.M403715200.
  • Potier E, Ferreira E, Andriamanalijaona R, Pujol JP, Oudina K, Logeart-Avramoglou D, Petite H. Hypoxia affects mesenchymal stromal cell osteogenic differentiation and angiogenic factor expression. Bone. 2007;40:1078–1087. doi:10.1016/j.bone.2006.11.024.
  • Xu N, Liu H, Qu F, Fan J, Mao K, Yin Y, Liu J, Geng Z, Wang Y. Hypoxia inhibits the differentiation of mesenchymal stem cells into osteoblasts by activation of Notch signaling. Exp Mol Pathol. 2013;94:33–39. doi:10.1016/j.yexmp.2012.08.003.
  • Artavanis-Tsakonas S, Rand MD, Lake RJ. Notch signaling: cell fate control and signal integration in development. Science. 1999;284:770–776. doi:10.1126/science.284.5415.770.
  • Lai EC. Notch signaling: control of cell communication and cell fate. Development. 2004;131:965–973. doi:10.1242/dev.01074.
  • Chiba S. Notch signaling in stem cell systems. Stem Cells. 2006;24:2437–2447. doi:10.1634/stemcells.2005-0661.
  • Hilton MJ, Tu X, Wu X, Bai S, Zhao H, Kobayashi T, Kronenberg HM, Teitelbaum SL, Ross FP, Kopan R, Long F. Notch signaling maintains bone marrow mesenchymal progenitors by suppressing osteoblast differentiation. Nat Med. 2008;14:306–314. doi:10.1038/nm1716.
  • Deregowski V, Gazzerro E, Priest L, Rydziel S, Notch CE. 1 overexpression inhibits osteoblastogenesis by suppressing Wnt/beta-catenin but not bone morphogenetic protein signaling. J Biol Chem. 2006;281:6203–6210. doi:10.1074/jbc.M508370200.
  • Zanotti S, Smerdel-Ramoya A, Stadmeyer L, Durant D, Radtke F, Canalis E. Notch inhibits osteoblast differentiation and causes osteopenia. Endocrinology. 2008;149:3890–3899. doi:10.1210/en.2008-0140.
  • Chong PP, Selvaratnam L, Abbas AA, Kamarul T. Human peripheral blood derived mesenchymal stem cells demonstrate similar characteristics and chondrogenic differentiation potential to bone marrow derived mesenchymal stem cells. J Orthop Res. 2012;30:634–642. doi:10.1002/jor.21558.
  • Kwon JS, Kim SW, Kwon DY, Park SH, Son AR, Kim JH, Kim MS. In vivo osteogenic differentiation of human turbinate mesenchymal stem cells in an injectable in situ-forming hydrogel. Biomaterials. 2014;35:5337–5346. doi:10.1016/j.biomaterials.2014.01.026.
  • Liu Y, Ming L, Luo H, Liu W, Zhang Y, Liu H, Jin Y. Integration of a calcined bovine bone and BMSC-sheet 3D scaffold and the promotion of bone regeneration in large defects. Biomaterials. 2013;34:9998–10006. doi:10.1016/j.biomaterials.2013.09.040.
  • Köhler C, Bell AW, Bowen WC, Monga SP, Fleig W, Michalopoulos GK. Expression of Notch-1 and its ligand Jagged-1 in rat liver during liver regeneration. Hepatology. 2004;39:1056–1065. doi:10.1002/hep.20156.
  • Jaiswal S, Weissman IL. Hematopoietic stem and progenitor cells and the inflammatory response. Ann N Y Acad Sci. 2009;1174:118–121. doi:10.1111/j.1749-6632.2009.04930.x.
  • Roufosse CA, Direkze NC, Otto WR, Wright NA. Circulating mesenchymal stem cells. Int J Biochem Cell Biol. 2004;36:585–597. doi:10.1016/j.biocel.2003.10.007.
  • Ezashi T, Das P, Roberts RM. Low O2 tensions and the prevention of differentiation of hES cells. Proc Natl Acad Sci USA. 2005;102:4783–4788. doi:10.1073/pnas.0501283102.
  • Cipolleschi MG, Dello Sbarba P, Olivotto M. The role of hypoxia in the maintenance of hematopoietic stem cells. Blood. 1993;82:2031–2037.
  • Grayson WL, Zhao F, Bunnell B, Ma T. Hypoxia enhances proliferation and tissue formation of human mesenchymal stem cells. Biochem Biophys Res Commun. 2007;358:948–953. doi:10.1016/j.bbrc.2007.05.054.
  • Krinner A, Zscharnack M, Bader A, Drasdo D, Galle J. Impact of oxygen environment on mesenchymal stem cell expansion and chondrogenic differentiation. Cell Prolif. 2009;42:471–484. doi:10.1111/j.1365-2184.2009.00621.x.
  • Hao Y, Cheng D, Ma Y, Zhou W, Wang Y. The relationship between oxygen concentration, reactive oxygen species and the biological characteristics of human bone marrow hematopoietic stem cells. Transplant Proc. 2011;43:2755–2761. doi:10.1016/j.transproceed.2011.09.059.
  • Deschepper M, Oudina K, David B, Myrtil V, Collet C, Bensidhoum M, Logeart-Avramoglou D, Petite H. Survival and function of mesenchymal stem cells (MSCs) depend on glucose to overcome exposure to long-term, severe and continuous hypoxia. J Cell Mol Med. 2011;15:1505–1514. doi:10.1111/j.1582-4934.2010.01138.x.
  • Benjamin S, Sheyn D, Ben-David S, Oh A, Kallai I, Li N, Gazit D, Gazit Z. Oxygenated environment enhances both stem cell survival and osteogenic differentiation. Tissue Eng Part A. 2013;19:748–758. doi:10.1089/ten.tea.2012.0298.
  • Annabi B, Lee YT, Turcotte S, Naud E, Desrosiers RR, Champagne M, Eliopoulos N, Galipeau J, Béliveau R. Hypoxia promotes murine bone-marrow-derived stromal cell migration and tube formation. Stem Cells. 2003;21:337–347. doi:10.1634/stemcells.21-3-337.
  • Rosová I, Dao M, Capoccia B, Link D, Nolta JA. Hypoxic preconditioning results in increased motility and improved therapeutic potential of human mesenchymal stem cells. Stem Cells. 2008;26:2173–2182. doi:10.1634/stemcells.2007-1104.
  • Choi JH, Lim SM, Yoo YI, Jung J, Park JW, Kim GJ. Microenvironmental interaction between hypoxia and endothelial cells controls the migration ability of placenta-derived mesenchymal stem cells via alpha4 integrin and Rho signaling. J Cell Biochem. 2016;117:1145–1157. doi:10.1002/jcb.25508.
  • HKh H, Jiang S, Idris NM, Ashraf M. IGF-1-overexpressing mesenchymal stem cells accelerate bone marrow stem cell mobilization via paracrine activation of SDF-1alpha/CXCR4 signaling to promote myocardial repair. Circ Res. 2008;103:1300–1308. doi:10.1161/CIRCRESAHA.108.186742.
  • Liu H, Yang M, Wu G, Yang L, Cao Y, Liu C, Tan Z, Jin Y, Guo J, Zhu L. Effects of different oxygen concentrations on the proliferation, survival, migration, and osteogenic differentiation of MC3T3-E1 cells. Connect Tissue Res. 2019;60:240–253. doi:10.1080/03008207.2018.1487413.
  • Hawkins KE, Sharp TV, McKay TR. The role of hypoxia in stem cell potency and differentiation. Regen Med. 2013;8:771–782. doi:10.2217/rme.13.71.
  • Wagegg M, Gaber T, Lohanatha FL, Hahne M, Strehl C, Fangradt M, Tran CL, Schönbeck K, Hoff P, Ode A, Perka C, Duda GN, Buttgereit F, Covas DT. Hypoxia promotes osteogenesis but suppresses adipogenesis of human mesenchymal stromal cells in a hypoxia-inducible factor-1 dependent manner. PLoS One. 2012;7:e46483. doi:10.1371/journal.pone.0046483.
  • Binder BY, Sagun JE, Leach JK. Reduced serum and hypoxic culture conditions enhance the osteogenic potential of human mesenchymal stem cells. Stem Cell Rev. 2015;11:387–393. doi:10.1007/s12015-014-9555-7.
  • Wang Y, Li J, Wang Y, Lei L, Jiang C, An S, Zhan Y, Cheng Q, Zhao Z, Wang J, Jiang L. Effects of hypoxia on osteogenic differentiation of rat bone marrow mesenchymal stem cells. Mol Cell Biochem. 2012;362:25–33. doi:10.1007/s11010-011-1131-8.
  • Bolos V, Grego-Bessa J, de la Pompa JL. Notch signaling in development and cancer. Endocr Rev. 2007;28:339–363. doi:10.1210/er.2006-0046.
  • Watt FM, Estrach S, Ambler CA. Epidermal Notch signalling: differentiation, cancer and adhesion. Curr Opin Cell Biol. 2008;20:171–179. doi:10.1016/j.ceb.2008.01.010.
  • Zamurovic N, Cappellen D, Rohner D, Susa M. Coordinated activation of notch, Wnt, and transforming growth factor-beta signaling pathways in bone morphogenic protein 2-induced osteogenesis. Notch target gene Hey1 inhibits mineralization and Runx2 transcriptional activity. J Biol Chem. 2004;279:37704–37715. doi:10.1074/jbc.M403813200.
  • Amir LR, Li G, Schoenmaker T, Everts V, Bronckers AL. Effect of thrombin peptide 508 (TP508) on bone healing during distraction osteogenesis in rabbit tibia. Cell Tissue Res. 2007;330:35–44. doi:10.1007/s00441-007-0475-6.
  • Nakashima K, Zhou X, Kunkel G, Zhang Z, Deng JM, Behringer RR, de Crombrugghe B. The novel zinc finger-containing transcription factor osterix is required for osteoblast differentiation and bone formation. Cell. 2002;108:17–29. doi:10.1016/S0092-8674(01)00622-5.
  • Lin GL, Hankenson KD. Integration of BMP, Wnt, and notch signaling pathways in osteoblast differentiation. J Cell Biochem. 2011;112:3491–3501. doi:10.1002/jcb.v112.12.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.