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Polycaprolactone/poly l-lactic acid nanofibrous scaffold improves osteogenic differentiation of the amniotic fluid-derived stem cells

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Abstract

Using stem cells is one of the most important determining factors in repairing lesions using regenerative medicine. Obtaining adult stem cells from patients is a perfect choice, but it is worth noting that their differentiation and proliferation potential decreases as the patient ages. For this reason, the use of amniotic fluid stem cells can be one of the excellent alternatives. This research aimed to investigate the osteogenic differentiation potential of the amniotic fluid stem cells while cultured on the polycaprolactone/poly l-lactic acid nanofibrous scaffold. Scaffolds were qualitatively evaluated by a scanning electron microscope, and their hydrophilicity and mechanical properties were studied using contact angle and tensile test, respectively. The biocompatibility and non-toxicity of the nanofibers were also evaluated using viability assay. The osteo-supportive capacity of the nanofibers was examined using alizarin red staining, alkaline phosphatase activity, and calcium release measurement. Finally, the expression level of four important bone-related genes was determined quantitatively. The results demonstrated that the mineralization rate, alkaline phosphatase activity, intracellular calcium, and bone-related genes increased significantly in the cells cultured on the polycaprolactone/poly l-lactic acid scaffold compared to the cells cultured on the tissue culture plate as a control. According to the results, it can be concluded that the polycaprolactone/poly l-lactic acid nanofibrous scaffold surprisingly improved the osteogenic differentiation potential of the amniotic fluid stem cells and, in combination with polycaprolactone/poly l-lactic acid nanofibers could be a promising candidate as bone implants.

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Data availability

The data supporting this study’s findings are available from the corresponding author upon reasonable request.

References 

  • Abazari R, Mahjoub AR, Ataei F, Morsali A, Carpenter-Warren CL, Mehdizadeh K, Slawin AM (2018) Chitosan immobilization on bio-MOF nanostructures: a biocompatible pH-responsive nanocarrier for doxorubicin release on MCF-7 cell lines of human breast cancer. Inorg Chem 57:13364–13379

    Article  CAS  PubMed  Google Scholar 

  • Antonucci I, Pantalone A, Tete S, SaliniBorlongan VCV, Hess D, Stuppia L (2012) Amniotic fluid stem cells: a promising therapeutic resource for cell-based regenerative therapy. Curr Pharm Des 18:1846–1863

    Article  CAS  PubMed  Google Scholar 

  • Ardeshirylajimi A, Delgoshaie M, Mirzaei S, Khojasteh A (2018) Different porosities of chitosan can influence the osteogenic differentiation potential of stem cells. J Cell Biochem 119:625–633

    Article  CAS  PubMed  Google Scholar 

  • Arjmand M, Ardeshirylajimi A, Maghsoudi H, Azadian E (2018) Osteogenic differentiation potential of mesenchymal stem cells cultured on nanofibrous scaffold improved in the presence of pulsed electromagnetic field. J Cell Physiol 233:1061–1070

    Article  CAS  PubMed  Google Scholar 

  • Azari A, Golchin A, Maymand MM, Mansouri F, Ardeshirylajimi A (2021) Electrospun polycaprolactone nanofibers: current research and applications in biomedical application. Adv Pharm Bulletin 12:658–672

    Google Scholar 

  • Burge R, Dawson-Hughes B, Solomon DH, Wong JB, King A, Tosteson A (2007) Incidence and economic burden of osteoporosis-related fractures in the United States, 2005–2025. J Bone Miner Res 22:465–475

    Article  PubMed  Google Scholar 

  • Cao Y, Mitchell G, Messina A, Price L, Thompson E, Penington A, Morrison W, O’Connor A, Stevens G, Cooper-White J (2006) The influence of architecture on degradation and tissue ingrowth into three-dimensional poly (lactic-co-glycolic acid) scaffolds in vitro and in vivo. Biomaterials 27:2854–2864

    Article  CAS  PubMed  Google Scholar 

  • Carraro G, Perin L, Sedrakyan S, Giuliani S, Tiozzo C, Lee J, Turcatel G, De Langhe SP, Driscoll B, Bellusci S (2008) Human amniotic fluid stem cells can integrate and differentiate into epithelial lung lineages. Stem Cells 26:2902–2911

    Article  CAS  PubMed  Google Scholar 

  • Chatterjee K, Lin-Gibson S, Wallace WE, Parekh SH, Lee YJ, Cicerone MT, Young MF, Simon CG Jr (2010) The effect of 3D hydrogel scaffold modulus on osteoblast differentiation and mineralization revealed by combinatorial screening. Biomaterials 31:5051–5062

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Christenson EM, Anseth KS, van den Beucken JJ, Chan CK, Ercan B, Jansen JA, Laurencin CT, Li WJ, Murugan R, Nair LS (2007) Nanobiomaterial applications in orthopedics. J Orthop Res 25:11–22

    Article  CAS  PubMed  Google Scholar 

  • Cipriani S, Bonini D, Marchina E, Balgkouranidou I, Caimi L, Zucconi GG, Barlati S (2007) Mesenchymal cells from human amniotic fluid survive and migrate after transplantation into adult rat brain. Cell Biol Int 31:845–850

    Article  CAS  PubMed  Google Scholar 

  • Correia C, Bhumiratana S, Yan L-P, Oliveira AL, Gimble JM, Rockwood D, Kaplan DL, Sousa RA, Reis RL, Vunjak-Novakovic G (2012) Development of silk-based scaffolds for tissue engineering of bone from human adipose-derived stem cells. Acta Biomater 8:2483–2492

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • De Coppi P, Bartsch G Jr, Siddiqui MM, Xu T, Santos CC, Perin L, Mostoslavsky G, Serre AC, Snyder EY, Yoo JJ (2007) Isolation of amniotic stem cell lines with potential for therapy. Nat Biotechnol 25:100–106

    Article  PubMed  Google Scholar 

  • De Coppi P, Callegari A, Chiavegato A, Gasparotto L, Piccoli M, Taiani J, Pozzobon M, Boldrin L, Okabe M, Cozzi E (2007) Amniotic fluid and bone marrow derived mesenchymal stem cells can be converted to smooth muscle cells in the cryo-injured rat bladder and prevent compensatory hypertrophy of surviving smooth muscle cells. J Urol 177:369–376

    Article  PubMed  Google Scholar 

  • Delo DM, De Coppi P, Bartsch G Jr, Atala A (2006) Amniotic fluid and placental stem cells. Methods Enzymol 419:426–438

    Article  CAS  PubMed  Google Scholar 

  • Deng C, Chang J, Wu C (2019) Bioactive scaffolds for osteochondral regeneration. J Orthop Transl 17:15–25

    Google Scholar 

  • Gholizadeh-Ghalehaziz S, Farahzadi R, Fathi E, Pashaiasl M (2015) A mini overview of isolation, characterization and application of amniotic fluid stem cells. Int J Stem Cells 8:115–120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guarino V, Causa F, Taddei P, Di Foggia M, Ciapetti G, Martini D, Fagnano C, Baldini N, Ambrosio L (2008) Polylactic acid fibre-reinforced polycaprolactone scaffolds for bone tissue engineering. Biomaterials 29:3662–3670

    Article  CAS  PubMed  Google Scholar 

  • Hasan MS, Ahmed I, Parsons A, Walker G, Scotchford C (2012) Cytocompatibility and mechanical properties of short phosphate glass fibre reinforced polylactic acid (PLA) composites: effect of coupling agent mediated interface. J Funct Biomater 3:706–725

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hipp J, Atala A (2008) Sources of stem cells for regenerative medicine. Stem Cell Reviews 4:3–11

    Article  PubMed  Google Scholar 

  • Hosseini FS, Enderami SE, Hadian A, Abazari MF, Ardeshirylajimi A, Saburi E, Soleimanifar F, Nazemisalman B (2019) Efficient osteogenic differentiation of the dental pulp stem cells on β-glycerophosphate loaded polycaprolactone/polyethylene oxide blend nanofibers. J Cell Physiol 234:13951–13958

    Article  CAS  PubMed  Google Scholar 

  • Jäger M, Degistirici Ö, Knipper A, Fischer J, Sager M, Krauspe R (2007) Bone healing and migration of cord blood—derived stem cells into a critical size femoral defect after xenotransplantation. J Bone Miner Res 22:1224–1233

    Article  PubMed  Google Scholar 

  • Janeczek AA, Tare RS, Scarpa E, Moreno-Jimenez I, Rowland CA, Jenner D, Newman TA, Oreffo RO, Evans ND (2016) Transient canonical Wnt stimulation enriches human bone marrow mononuclear cell isolates for osteoprogenitors. Stem Cells 34:418–430

    Article  CAS  PubMed  Google Scholar 

  • Kaviani A, Perry TE, Dzakovic A, Jennings RW, Ziegler MM, Fauza DO (2001) The amniotic fluid as a source of cells for fetal tissue engineering. J Pediatr Surg 36:1662–1665

    Article  CAS  PubMed  Google Scholar 

  • Kim J, Lee Y, Kim H, Hwang K, Kwon H, Kim S, Cho D, Kang S, You J (2007) Human amniotic fluid-derived stem cells have characteristics of multipotent stem cells. Cell Prolif 40:75–90

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kunisaki SM, Jennings RW, Fauza DO (2006) Fetal cartilage engineering from amniotic mesenchymal progenitor cells. Stem Cells Development 15:245–253

    Article  CAS  PubMed  Google Scholar 

  • Laowanitwattana T, Aungsuchawan S, Narakornsak S, Markmee R, Tancharoen W, Keawdee J, Boonma N, Tasuya W, Peerapapong L, Pangjaidee N (2018) Osteoblastic differentiation potential of human amniotic fluid-derived mesenchymal stem cells in different culture conditions. Acta Histochem 120:701–712

    Article  CAS  PubMed  Google Scholar 

  • Liao GY, Chen L, Zeng XY, Zhou XP, Xie XL, Peng EJ, Ye ZQ, Mai YW (2011) Electrospun poly (L-lactide)/poly (ε-caprolactone) blend fibers and their cellular response to adipose-derived stem cells. J Appl Polym Sci 120:2154–2165

    Article  CAS  Google Scholar 

  • Liu X, Ma PX (2004) Polymeric scaffolds for bone tissue engineering. Ann Biomed Eng 32:477–486

    Article  PubMed  Google Scholar 

  • Ma PX (2008) Biomimetic materials for tissue engineering. Adv Drug Deliv Rev 60:184–198

    Article  CAS  PubMed  Google Scholar 

  • Mahmoudinia Meymand M, Noruzinia M (2017) Osteoblastic differentiation of amniotic pluripotent stem cell. Sarem J Med Res 1:9–13

    Google Scholar 

  • Maraldi T, Riccio M, Resca E, Pisciotta A, La Sala GB, Ferrari A, Bruzzesi G, Motta A, Migliaresi C, Marzona L (2011) Human amniotic fluid stem cells seeded in fibroin scaffold produce in vivo mineralized matrix. Tissue Eng Part A 17:2833–2843

    Article  CAS  PubMed  Google Scholar 

  • Meng C, Tang D, Liu X, Meng J, Wei W, Gong RH, Li J (2023) Heterogeneous porous PLLA/PCL fibrous scaffold for bone tissue regeneration. Int J Biol Macromol 235:123781

    Article  CAS  PubMed  Google Scholar 

  • Messner J, Johnson L, Taylor D, Harwood P, Britten S, Foster P (2018) Treatment and functional outcomes of complex tibial fractures in children and adolescents using the Ilizarov method. Bone Joint J 100:396–403

    Article  PubMed  Google Scholar 

  • Mikos AG, Thorsen AJ, Czerwonka LA, Bao Y, Langer R, Winslow DN, Vacanti JP (1994) Preparation and characterization of poly (L-lactic acid) foams. Polymer 35:1068–1077

    Article  CAS  Google Scholar 

  • Mirzaei A, Moghadam AS, Abazari MF, Nejati F, Torabinejad S, Kaabi M, Enderami SE, Ardeshirylajimi A, Darvish M, Soleimanifar F (2019) Comparison of osteogenic differentiation potential of induced pluripotent stem cells on 2D and 3D polyvinylidene fluoride scaffolds. J Cell Physiol 234:17854–17862

    Article  CAS  PubMed  Google Scholar 

  • Mondal S, Nguyen TP, Hoang G, Manivasagan P, Kim MH, Nam SY, Oh J (2020) Hydroxyapatite nano bioceramics optimized 3D printed poly lactic acid scaffold for bone tissue engineering application. Ceram Int 46:3443–3455

    Article  CAS  Google Scholar 

  • Pan H-C, Cheng F-C, Chen C-J, Lai S-Z, Lee C-W, Yang D-Y, Chang M-H, Ho S-P (2007) Post-injury regeneration in rat sciatic nerve facilitated by neurotrophic factors secreted by amniotic fluid mesenchymal stem cells. J Clin Neurosci 14:1089–1098

    Article  CAS  PubMed  Google Scholar 

  • Patel U, Macri-Pellizzeri L, Zakir Hossain KM, Scammell BE, Grant DM, Scotchford CA, Hannon AC, Kennedy AR, Barney ER, Ahmed I (2019) In vitro cellular testing of strontium/calcium substituted phosphate glass discs and microspheres shows potential for bone regeneration. J Tissue Eng Regen Med 13:396–405

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Perin L, Sedrakyan S, Giuliani S, Da Sacco S, Carraro G, Shiri L, Lemley KV, Rosol M, Wu S, Atala A (2010) Protective effect of human amniotic fluid stem cells in an immunodeficient mouse model of acute tubular necrosis. PLoS ONE 5:e9357

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  • Place ES, Evans ND, Stevens MM (2009) Complexity in biomaterials for tissue engineering. Nat Mater 8:457–470

    Article  ADS  CAS  PubMed  Google Scholar 

  • Prusa A-R, Hengstschlager M (2002) Amniotic fluid cells and human stem cell research-a new connection. Med Sci Monit 8:RA253-257

    PubMed  Google Scholar 

  • Rodrigues MT, Lee B-K, Lee SJ, Gomes ME, Reis RL, Atala A, Yoo JJ (2012) The effect of differentiation stage of amniotic fluid stem cells on bone regeneration. Biomaterials 33:6069–6078

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez-Merchan EC, Forriol F (2004) Nonunion: general principles and experimental data. Clin Orthop Relat Res 1976–2007(419):4–12

    Article  Google Scholar 

  • Roubelakis MG, Trohatou O, Anagnou NP (2012) Amniotic fluid and amniotic membrane stem cells: marker discovery. Stem Cells Int 2012; https://doi.org/10.1155/2012/107836

  • Salamanca E, Tsao T-C, Hseuh H-W, Wu Y-F, Choy C-S, Lin C-K, Pan Y-H, Teng N-C, Huang M-C, Lin S-M (2021) Fabrication of polylactic acid/β-tricalcium phosphate FDM 3D printing fiber to enhance osteoblastic-like cell performance. Frontiers in Materials 8:683706

    Article  Google Scholar 

  • Salerno A, Zeppetelli S, Oliviero M, Battista E, Di Maio E, Iannace S, Netti PA (2012) Microstructure, degradation and in vitro MG63 cells interactions of a new poly (ε-caprolactone), zein, and hydroxyapatite composite for bone tissue engineering. J Bioact Compat Polym 27:210–226

    Article  CAS  Google Scholar 

  • Seong JM, Kim B-C, Park J-H, Kwon IK, Mantalaris A, Hwang Y-S (2010) Stem cells in bone tissue engineering. Biomed Mater 5:062001

    Article  ADS  PubMed  Google Scholar 

  • Shuai C, Yang W, Feng P, Peng S, Pan H (2021) Accelerated degradation of HAP/PLLA bone scaffold by PGA blending facilitates bioactivity and osteoconductivity. Bioactive Materials 6:490–502

    Article  CAS  PubMed  Google Scholar 

  • Sun H, Feng K, Hu J, Soker S, Atala A, Ma PX (2010) Osteogenic differentiation of human amniotic fluid-derived stem cells induced by bone morphogenetic protein-7 and enhanced by nanofibrous scaffolds. Biomaterials 31:1133–1139

    Article  CAS  PubMed  Google Scholar 

  • Yeh Y-C, Wei H-J, Lee W-Y, Yu C-L, Chang Y, Hsu L-W, Chung M-F, Tsai M-S, Hwang S-M, Sung H-W (2010) Cellular cardiomyoplasty with human amniotic fluid stem cells: in vitro and in vivo studies. Tissue Eng Part A 16:1925–1936

    Article  CAS  PubMed  Google Scholar 

  • Zhang S, Geng H, Xie H, Wu Q, Ma X, Zhou J, Chen F (2010) The heterogeneity of cell subtypes from a primary culture of human amniotic fluid. Cell Mol Biol Lett 15:424–439

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang L-T, Liu R-M, Luo Y, Zhao Y-J, Chen D-X, Yu C-Y, Xiao J-H (2019) Hyaluronic acid promotes osteogenic differentiation of human amniotic mesenchymal stem cells via the TGF-β/Smad signalling pathway. Life Sci 232:116669

    Article  CAS  PubMed  Google Scholar 

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S.M.P.: literature, accomplish experiments, data analysis, and manuscript draft preparation; A.A., S.I., and S.M.H.G.: experiments’ design, data analysis, and data and manuscript approval.

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Correspondence to Sayyed Mohammad Hossein Ghaderian.

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This study was approved by the research committee of the Biology Department of Islamic Azad University, Science and Research Unit, Tehran, Iran.

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Editor: John W. Harbell.

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Pishnamazi, S.M., Ghaderian, S.M.H., Irani, S. et al. Polycaprolactone/poly l-lactic acid nanofibrous scaffold improves osteogenic differentiation of the amniotic fluid-derived stem cells. In Vitro Cell.Dev.Biol.-Animal 60, 106–114 (2024). https://doi.org/10.1007/s11626-023-00838-3

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