Porous Se@SiO₂ nanocomposite promotes migration and osteogenic differentiation of rat bone marrow mesenchymal stem cell to accelerate bone fracture healing in a rat model

References

• Balogh ZJ, Reumann MK, Gruen RL, et al. Advances and future directions for management of trauma patients with musculoskeletal injuries. Lancet (London, England). 2012;380(9847):1109–1119. doi:10.1016/S0140-6736(12)60991-X
   PubMed Web of Science ®Google Scholar
• Nakamura A, Akahane M, Shigematsu H, et al. Cell sheet transplantation of cultured mesenchymal stem cells enhances bone formation in a rat nonunion model. Bone. 2010;46(2):418–424. doi:10.1016/j.bone.2009.08.04819716454
   PubMedGoogle Scholar
• Kallai I, van Lenthe GH, Ruffoni D, et al. Quantitative, structural, and image-based mechanical analysis of nonunion fracture repaired by genetically engineered mesenchymal stem cells. J Biomech. 2010;43(12):2315–2320. doi:10.1016/j.jbiomech.2010.04.03120471652
   PubMedGoogle Scholar
• Horwitz EM, Prockop DJ, Fitzpatrick LA, et al. Transplantability and therapeutic effects of bone marrow-derived mesenchymal cells in children with osteogenesis imperfecta. Nat Med. 1999;5(3):309–313. doi:10.1038/652910086387
   PubMed Web of Science ®Google Scholar
• Cancedda R, Bianchi G, Derubeis A, Quarto R. Cell therapy for bone disease: a review of current status. Stem Cells. 2003;21(5):610–619. doi:10.1634/stemcells.21-5-61012968115
   PubMedGoogle Scholar
• Atashi F, Modarressi A, Pepper MS. The role of reactive oxygen species in mesenchymal stem cell adipogenic and osteogenic differentiation: a review. Stem Cells Dev. 2015;24(10):1150–1163. doi:10.1089/scd.2014.048425603196
   PubMed Web of Science ®Google Scholar
• Marie PJ. Targeting integrins to promote bone formation and repair. Nat Rev Endocrinol. 2013;9(5):288–295. doi:10.1038/nrendo.2013.423358353
   PubMed Web of Science ®Google Scholar
• Guan M, Yao W, Liu R, et al. Directing mesenchymal stem cells to bone to augment bone formation and increase bone mass. Nat Med. 2012;18(3):456–462. doi:10.1038/nm.266522306732
   PubMed Web of Science ®Google Scholar
• Yao W, Lay YE, Kot A, et al. Improved mobilization of exogenous mesenchymal stem cells to bone for fracture healing and sex difference. Stem Cells. 2016;34(10):2587–2600. doi:10.1002/stem.243327334693
   PubMed Web of Science ®Google Scholar
• Takarada T, Nakazato R, Tsuchikane A, et al. Genetic analysis of Runx2 function during intramembranous ossification. Development. 2016;143(2):211–218. doi:10.1242/dev.12879326657773
   PubMedGoogle Scholar
• Schussler SD, Uske K, Marwah P, et al. Controlled release of vanadium from a composite scaffold stimulates mesenchymal stem cell osteochondrogenesis. Aaps J. 2017;19(4):1017–1028. doi:10.1208/s12248-017-0073-928332167
   PubMedGoogle Scholar
• Muinos-Lopez E, Ripalda-Cemborain P, Lopez-Martinez T, et al. Hypoxia and reactive oxygen species homeostasis in mesenchymal progenitor cells define a molecular mechanism for fracture nonunion. Stem Cells. 2016;34(9):2342–2353. doi:10.1002/stem.239927250101
   PubMedGoogle Scholar
• Wang H, Wei W, Zhang SY, et al. Melatonin-selenium nanoparticles inhibit oxidative stress and protect against hepatic injury induced by bacillus calmette-guerin/lipopolysaccharide in mice. J Pineal Res. 2005;39(2):156–163. doi:10.1111/j.1600-079X.2005.00231.x16098093
   PubMedGoogle Scholar
• Wang J, Liu Z, He X, et al. Selenium deficiency induces duodenal villi cell apoptosis via an oxidative stress-induced mitochondrial apoptosis pathway and an inflammatory signaling-induced death receptor pathway. Metallomics Integr Biometal Sci. 2018;10:1390.
   PubMed Web of Science ®Google Scholar
• Sheng Y, Liu G, Wang M, Lv Z, Du P. A selenium polysaccharide from Platycodon grandiflorum rescues PC12 cell death caused by H2O2 via inhibiting oxidative stress. Int J Biol Macromol. 2017;104:393–399. doi:10.1016/j.ijbiomac.2017.06.05228610929
   PubMed Web of Science ®Google Scholar
• Zeng H, Cao JJ, Combs GF Jr. Selenium in bone health: roles in antioxidant protection and cell proliferation. Nutrients. 2013;5(1):97–110. doi:10.3390/nu501009723306191
   PubMed Web of Science ®Google Scholar
• Cao JJ, Gregoire BR, Zeng H. Selenium deficiency decreases antioxidative capacity and is detrimental to bone microarchitecture in mice. J Nutr. 2012;142(8):1526–1531. doi:10.3945/jn.111.15704022739365
   PubMedGoogle Scholar
• Liu H, Bian W, Liu S, Huang K. Selenium protects bone marrow stromal cells against hydrogen peroxide-induced inhibition of osteoblastic differentiation by suppressing oxidative stress and ERK signaling pathway. Biol Trace Elem Res. 2012;150(1–3):441–450. doi:10.1007/s12011-012-9488-422890880
   PubMedGoogle Scholar
• Steinbeck MJ, Kim JK, Trudeau MJ, Hauschka PV, Karnovsky MJ. Involvement of hydrogen peroxide in the differentiation of clonal HD-11EM cells into osteoclast-like cells. J Cell Physiol. 1998;176(3):574–587. doi:10.1002/(SICI)1097-4652(199809)176:3<574::AID-JCP14>3.0.CO;2-#9699510
   PubMed Web of Science ®Google Scholar
• Lean JM, Jagger CJ, Kirstein B, Fuller K, Chambers TJ. Hydrogen peroxide is essential for estrogen-deficiency bone loss and osteoclast formation. Endocrinology. 2005;146(2):728–735. doi:10.1210/en.2004-102115528306
   PubMed Web of Science ®Google Scholar
• Srivastava N, Mukhopadhyay M. Green synthesis and structural characterization of selenium nanoparticles and assessment of their antimicrobial property. Bioprocess Biosyst Eng. 2015;38(9):1723–1730. doi:10.1007/s00449-015-1413-825972036
   PubMed Web of Science ®Google Scholar
• Estevez H, Garcia-Lidon JC, Luque-Garcia JL, Camara C. Effects of chitosan-stabilized selenium nanoparticles on cell proliferation, apoptosis and cell cycle pattern in HepG2 cells: comparison with other selenospecies. Colloids Surf B Biointerfaces. 2014;122:184–193. doi:10.1016/j.colsurfb.2014.06.06225038448
   PubMed Web of Science ®Google Scholar
• Zhu Y, Deng G, Ji A, et al. Porous Se@SiO2 nanospheres treated paraquat-induced acute lung injury by resisting oxidative stress. Int J Nanomedicine. 2017;12:7143–7152. doi:10.2147/IJN.S14319229026307
   PubMed Web of Science ®Google Scholar
• Komori T, Yagi H, Nomura S, et al. Targeted disruption of Cbfa1 results in a complete lack of bone formation owing to maturational arrest of osteoblasts. Cell. 1997;89(5):755–764.9182763
   PubMed Web of Science ®Google Scholar
• Wynn RF, Hart CA, Corradi-Perini C, et al. A small proportion of mesenchymal stem cells strongly expresses functionally active CXCR4 receptor capable of promoting migration to bone marrow. Blood. 2004;104(9):2643–2645. doi:10.1182/blood-2004-02-052615251986
   PubMedGoogle Scholar
• Shi M, Li J, Liao L, et al. Regulation of CXCR4 expression in human mesenchymal stem cells by cytokine treatment: role in homing efficiency in NOD/SCID mice. Haematologica. 2007;92(7):897–904.17606439
   PubMed Web of Science ®Google Scholar
• Deng G, Wang W, Yang C, Gao R, Yang X, Ye X. Shaking improves the whole bone marrow adherent method of purification. Mol Med Rep. 2016;13(4):3133–3138. doi:10.3892/mmr.2016.492026936221
   PubMedGoogle Scholar
• Deng GY, Chen CZ, Zhang JJ, et al. Se@SiO2 nanocomposites attenuate doxorubicin-induced cardiotoxicity through combatting oxidative damage. Artif Cell Nanomed Biotechnol 2018;46:112–121.
   Google Scholar
• Liu X, Deng G, Wang Y, et al. A novel and facile synthesis of porous SiO2-coated ultrasmall Se particles as a drug delivery nanoplatform for efficient synergistic treatment of cancer cells. Nanoscale. 2016;8(16):8536–8541. doi:10.1039/c6nr02298g27072410
   PubMedGoogle Scholar
• Xu L, Huang S, Hou Y, et al. Sox11-modified mesenchymal stem cells (MSCs) accelerate bone fracture healing: sox11 regulates differentiation and migration of MSCs. FASEB J. 2015;29(4):1143–1152. doi:10.1096/fj.14-25416925466891
   PubMed Web of Science ®Google Scholar
• Hankenson KD, Gagne K, Shaughnessy M. Extracellular signaling molecules to promote fracture healing and bone regeneration. Adv Drug Deliv Rev. 2015;94:3–12. doi:10.1016/j.addr.2015.09.00826428617
   PubMed Web of Science ®Google Scholar
• Kovach TK, Dighe AS, Lobo PI, Cui Q. Interactions between MSCs and immune cells: implications for bone healing. J Immunol Res. 2015;2015:752510. doi:10.1155/2015/75251026000315
   PubMed Web of Science ®Google Scholar
• Rharass T, Lucas S, IN ENDOCRINOLOGY: MECHANISMS. Bone marrow adiposity and bone, a bad romance? Eur J Endocrinol. 2018;179(4):R165–R182. doi:10.1530/EJE-18-018230299886
   PubMedGoogle Scholar
• Liu X, Duan B, Cheng Z, et al. SDF-1/CXCR4 axis modulates bone marrow mesenchymal stem cell apoptosis, migration and cytokine secretion. Protein Cell. 2011;2(10):845–854. doi:10.1007/s13238-011-1097-z22058039
   PubMed Web of Science ®Google Scholar
• Li M, Chen X, Yan J, et al. Inhibition of osteoclastogenesis by stem cell-derived extracellular matrix through modulation of intracellular reactive oxygen species. Acta Biomater. 2018;71:118–131. doi:10.1016/j.actbio.2018.03.00329526830
   PubMed Web of Science ®Google Scholar
• Tan J, Xu X, Tong Z, et al. Decreased osteogenesis of adult mesenchymal stem cells by reactive oxygen species under cyclic stretch: a possible mechanism of age related osteoporosis. Bone Res. 2015;3:15003. doi:10.1038/boneres.2015.326273536
   PubMed Web of Science ®Google Scholar
• Li Q, Gao Z, Chen Y, Guan MX. The role of mitochondria in osteogenic, adipogenic and chondrogenic differentiation of mesenchymal stem cells. Protein Cell. 2017;8(6):439–445. doi:10.1007/s13238-017-0385-728271444
   PubMedGoogle Scholar
• Li J, Zhang J, Chen Y, Kawazoe N, Chen G. TEMPO-conjugated gold nanoparticles for reactive oxygen species scavenging and regulation of stem cell differentiation. ACS Appl Mater Interfaces. 2017;9(41):35683–35692. doi:10.1021/acsami.7b1248628944661
   PubMedGoogle Scholar
• Sun W, Qiao W, Zhou B, et al. Overexpression of Sirt1 in mesenchymal stem cells protects against bone loss in mice by FOXO3a deacetylation and oxidative stress inhibition. Metabolism. 2018;88:61–71. doi:10.1016/j.metabol.2018.06.00630318050
   PubMed Web of Science ®Google Scholar
• Rayman MP. The importance of selenium to human health. Lancet (London, England). 2000;356(9225):233–241. doi:10.1016/S0140-6736(00)02490-9
   PubMed Web of Science ®Google Scholar
• Alehagen U, Aaseth J. Selenium and coenzyme Q10 interrelationship in cardiovascular diseases–A clinician‘s point of view. J Trace Elem Med Biol. 2015;31:157–162. doi:10.1016/j.jtemb.2014.11.00625511910
   PubMed Web of Science ®Google Scholar
• Zajnudinov ZM, Shabanov AK, Sorin SN, et al. Selenium metabolism in patients with severe multiple trauma. Anesteziologiya i Reanimatologiya. 2014(3):68–71.
   Google Scholar
• Moreno-Reyes R, Suetens C, Mathieu F, et al. Kashin-Beck osteoarthropathy in rural Tibet in relation to selenium and iodine status. N Engl J Med. 1998;339(16):1112–1120. doi:10.1056/NEJM1998101533916049770558
   PubMedGoogle Scholar
• Moreno-Reyes R, Egrise D, Boelaert M, Goldman S, Meuris S. Iodine deficiency mitigates growth retardation and osteopenia in selenium-deficient rats. J Nutr. 2006;136(3):595–600. doi:10.1093/jn/136.3.59516484530
   PubMedGoogle Scholar
• Zhang J, Wang X, Xu T. Elemental selenium at nano size (Nano-Se) as a potential chemopreventive agent with reduced risk of selenium toxicity: comparison with se-methylselenocysteine in mice. Toxicol Sci. 2008;101(1):22–31. doi:10.1093/toxsci/kfm22117728283
   PubMed Web of Science ®Google Scholar
• Deng G, Dai C, Chen J, et al. Porous Se@SiO2 nanocomposites protect the femoral head from methylprednisolone-induced osteonecrosis. Int J Nanomedicine. 2018;13:1809–1818.29606872
   PubMed Web of Science ®Google Scholar
• Wang H, Zhang J, Yu H. Elemental selenium at nano size possesses lower toxicity without compromising the fundamental effect on selenoenzymes: comparison with selenomethionine in mice. Free Radic Biol Med. 2007;42(10):1524–1533. doi:10.1016/j.freeradbiomed.2007.02.01317448899
   PubMed Web of Science ®Google Scholar
• He Y, Chen S, Liu Z, Cheng C, Li H, Wang M. Toxicity of selenium nanoparticles in male Sprague-Dawley rats at supranutritional and nonlethal levels. Life Sci. 2014;115(1–2):44–51. doi:10.1016/j.lfs.2014.08.02325219884
   PubMed Web of Science ®Google Scholar
• Liao L, Su X, Yang X, et al. TNF-alpha inhibits FoxO1 by upregulating miR-705 to aggravate oxidative damage in bone marrow-derived mesenchymal stem cells during osteoporosis. Stem Cells. 2016;34(4):1054–1067. doi:10.1002/stem.227426700816
   PubMedGoogle Scholar
• Chen CT, Shih YR, Kuo TK, Lee OK, Wei YH. Coordinated changes of mitochondrial biogenesis and antioxidant enzymes during osteogenic differentiation of human mesenchymal stem cells. Stem Cells. 2008;26(4):960–968. doi:10.1634/stemcells.2007-050918218821
   PubMed Web of Science ®Google Scholar
• Lin CH, Li NT, Cheng HS, Yen ML. Oxidative stress induces imbalance of adipogenic/osteoblastic lineage commitment in mesenchymal stem cells through decreasing SIRT1 functions. J Cell Mol Med. 2018;22(2):786–796. doi:10.1111/jcmm.1335628975701
   PubMedGoogle Scholar
• Watanabe J, Yamada M, Niibe K, et al. Preconditioning of bone marrow-derived mesenchymal stem cells with N-acetyl-L-cysteine enhances bone regeneration via reinforced resistance to oxidative stress. Biomaterials. 2018;185:25–38. doi:10.1016/j.biomaterials.2018.08.05530216807
   PubMedGoogle Scholar
• Kim JY, Shin KK, Lee AL, et al. MicroRNA-302 induces proliferation and inhibits oxidant-induced cell death in human adipose tissue-derived mesenchymal stem cells. Cell Death Dis. 2014;5:e1385. doi:10.1038/cddis.2014.34425144720
   PubMed Web of Science ®Google Scholar
• Wang X, Zhao T, Huang W, et al. Hsp20-engineered mesenchymal stem cells are resistant to oxidative stress via enhanced activation of Akt and increased secretion of growth factors. Stem Cells. 2009;27(12):3021–3031. doi:10.1002/stem.23019816949
   PubMed Web of Science ®Google Scholar
• Li K, Shen Q, Xie Y, You M, Huang L, Zheng X. Incorporation of cerium oxide into hydroxyapatite coating protects bone marrow stromal cells against H2O2-induced inhibition of osteogenic differentiation. Biol Trace Elem Res. 2018;182(1):91–104. doi:10.1007/s12011-017-1066-328624869
   PubMed Web of Science ®Google Scholar
• Kang Q, Song WX, Luo Q, et al. A comprehensive analysis of the dual roles of BMPs in regulating adipogenic and osteogenic differentiation of mesenchymal progenitor cells. Stem Cells Dev. 2009;18(4):545–559. doi:10.1089/scd.2008.013018616389
   PubMed Web of Science ®Google Scholar
• Chen D, Zhao M, Mundy GR. Bone morphogenetic proteins. Growth Factors. 2004;22(4):233–241. doi:10.1080/0897719041233127989015621726
   PubMed Web of Science ®Google Scholar
• Kugimiya F, Yano F, Ohba S, et al. Mechanism of osteogenic induction by FK506 via BMP/Smad pathways. Biochem Biophys Res Commun. 2005;338(2):872–879. doi:10.1016/j.bbrc.2005.10.02416246307
   PubMed Web of Science ®Google Scholar