uni-leipzig-open-access/json/s00418-022-02156-3

{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2023,12,23]],"date-time":"2023-12-23T19:56:15Z","timestamp":1703361375381},"reference-count":32,"publisher":"Springer Science and Business Media LLC","issue":"3","license":[{"start":{"date-parts":[[2022,10,29]],"date-time":"2022-10-29T00:00:00Z","timestamp":1667001600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2022,10,29]],"date-time":"2022-10-29T00:00:00Z","timestamp":1667001600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"name":"DFG"},{"DOI":"10.13039\/501100001659","name":"Deutsche Forschungsgemeinschaft","doi-asserted-by":"publisher","award":["SCHU1979\/14-1"]},{"DOI":"10.13039\/501100011852","name":"Paracelsus Medical University","doi-asserted-by":"crossref"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Histochem Cell Biol"],"published-print":{"date-parts":[[2023,3]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Although autografts represent the gold standard for anterior cruciate ligament (ACL) reconstruction, tissue-engineered ACLs provide a prospect to minimize donor site morbidity and limited graft availability. This study characterizes the ligamentogenesis in embroidered poly(<jats:sc>L<\/jats:sc>-lactide-<jats:italic>co<\/jats:italic>-\u03b5-caprolactone) (P(LA-CL)) \/ polylactic acid (PLA) constructs using a dynamic nude mice xenograft model. (P(LA-CL))\/PLA scaffolds remained either untreated (co) or were functionalized by gas fluorination (F), collagen foam cross-linked with hexamethylene diisocyanate (HMDI) (coll), or F combined with the foam (F\u2009+\u2009coll). Cell-free constructs or those seeded for 1\u00a0week with lapine ACL ligamentocytes were implanted into nude mice for 12\u00a0weeks. Following explantation, cell vitality and content, histo(patho)logy of scaffolds (including organs: liver, kidney, spleen), sulphated glycosaminoglycan (sGAG) contents and biomechanical properties were assessed.<\/jats:p><jats:p>Scaffolds did not affect mice weight development and organs, indicating no organ toxicity. Moreover, scaffolds maintained their size and shape and reflected a high cell viability prior to and following implantation. Coll or F\u2009+\u2009coll scaffolds seeded with cells yielded superior macroscopic properties compared to the controls. Mild signs of inflammation (foreign-body giant cells\u00a0and hyperemia) were limited to scaffolds without collagen. Microscopical score values and sGAG content did not differ significantly. Although remaining stable after explantation, elastic modulus, maximum force, tensile strength and strain at F<jats:sub>max<\/jats:sub> were significantly lower in explanted scaffolds compared to those before implantation, with no significant differences between scaffold subtypes, except for a higher maximum force in F\u2009+\u2009coll compared with F samples (in vivo). Scaffold functionalization with fluorinated collagen foam provides a promising approach for ACL tissue engineering.<\/jats:p>\n                <jats:p><jats:bold>Graphical abstract<\/jats:bold><\/jats:p>\n                <jats:p><jats:bold>a<\/jats:bold> Lapine anterior cruciate ligament (LACL): red arrow, posterior cruciate ligament: yellow arrow. Medial anterior meniscotibial ligament: black arrow. <jats:bold>b<\/jats:bold> Explant culture to isolate LACL fibroblasts. <jats:bold>c<\/jats:bold> Scaffold variants: co: controls; F: functionalization by gas-phase fluorination; coll: collagen foam cross-linked with hexamethylene diisocyanate (HMDI). <jats:bold>c1-2<\/jats:bold> Embroidery pattern of the scaffolds. <jats:bold>d<\/jats:bold> Scaffolds were seeded with LACL fibroblasts using a dynamical culturing approach as depicted. <jats:bold>e<\/jats:bold> Scaffolds were implanted subnuchally into nude mice, fixed at the nuchal ligament and sacrospinal muscle tendons. <jats:bold>f<\/jats:bold> Two weeks after implantation. <jats:bold>g<\/jats:bold> Summary of analyses performed. Scale bars 1\u00a0cm (<jats:bold>b<\/jats:bold>,<jats:bold> d<\/jats:bold>), 0.5\u00a0cm (<jats:bold>c<\/jats:bold>).\u00a0(sketches drawn by G.S.-T. using Krita 4.1.7 [Krita foundation, The Netherlands]).<\/jats:p>","DOI":"10.1007\/s00418-022-02156-3","type":"journal-article","created":{"date-parts":[[2022,10,29]],"date-time":"2022-10-29T16:04:52Z","timestamp":1667059492000},"page":"275-292","update-policy":"http:\/\/dx.doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":6,"title":["In vivo ligamentogenesis in embroidered poly(lactic-co-\u03b5-caprolactone) \/ polylactic acid scaffolds functionalized by fluorination and hexamethylene diisocyanate cross-linked collagen foams"],"prefix":"10.1007","volume":"159","author":[{"given":"Maria","family":"Kokozidou","sequence":"first","affiliation":[]},{"given":"Clemens","family":"G\u00f6gele","sequence":"additional","affiliation":[]},{"given":"Felix","family":"Pirrung","sequence":"additional","affiliation":[]},{"given":"Niels","family":"Hammer","sequence":"additional","affiliation":[]},{"given":"Christian","family":"Werner","sequence":"additional","affiliation":[]},{"given":"Benjamin","family":"Kohl","sequence":"additional","affiliation":[]},{"given":"Judith","family":"Hahn","sequence":"additional","affiliation":[]},{"given":"Annette","family":"Breier","sequence":"additional","affiliation":[]},{"given":"Michaela","family":"Schr\u00f6pfer","sequence":"additional","affiliation":[]},{"given":"Michael","family":"Meyer","sequence":"additional","affiliation":[]},{"given":"Gundula","family":"Schulze-Tanzil","sequence":"additional","affiliation":[]}],"member":"297","published-online":{"date-parts":[[2022,10,29]]},"reference":[{"key":"2156_CR1","doi-asserted-by":"publisher","first-page":"691","DOI":"10.2174\/1574888X13666180809093343","volume":"13","author":"DE Archer","year":"2018","unstructured":"Archer DE, Mafi R, Mafi P, Khan WS (2018) Preclinical studies on biomaterial scaffold use in knee ligament regeneration: a systematic review. Curr Stem Cell Res Ther 13:691\u2013701","journal-title":"Curr Stem Cell Res Ther"},{"key":"2156_CR2","first-page":"23","volume-title":"Embroidery technology for hard-tissue scaffolds","author":"AC Breier","year":"2015","unstructured":"Breier AC (2015) Embroidery technology for hard-tissue scaffolds. Fundamentals, Applications and Tissue Engineering, Woodhead Publishing Series in Biomaterials, Biomedical Textiles for Orthopaedic and Surgical Applications, pp 23\u201343"},{"key":"2156_CR3","doi-asserted-by":"publisher","first-page":"4","DOI":"10.1016\/j.jocit.2018.09.002","volume":"4","author":"XL C\u00e9dric Laurent","year":"2018","unstructured":"C\u00e9dric Laurent XL, De Isla N, Wang X, Rahouadj R (2018) Defining a scaffold for ligament tissue engineering: What has been done, and what still needs to be done. J Cellular Immunotherapy 4:4\u20139","journal-title":"J Cellular Immunotherapy"},{"key":"2156_CR4","doi-asserted-by":"publisher","first-page":"102","DOI":"10.1089\/ten.tea.2019.0142","volume":"26","author":"CW Chang","year":"2020","unstructured":"Chang CW, Lee JH, Chao PG (2020) Chemical optimization for functional ligament tissue engineering. Tissue Eng Part A 26:102\u2013110","journal-title":"Tissue Eng Part A"},{"key":"2156_CR5","doi-asserted-by":"publisher","first-page":"200","DOI":"10.1186\/s12967-015-0560-7","volume":"13","author":"L Dai","year":"2015","unstructured":"Dai L, Hu X, Zhang X, Zhu J, Zhang J, Fu X, Duan X, Ao Y, Zhou C (2015) Different tenogenic differentiation capacities of different mesenchymal stem cells in the presence of BMP-12. J Transl Med 13:200","journal-title":"J Transl Med"},{"issue":"2","key":"2156_CR6","doi-asserted-by":"publisher","first-page":"42","DOI":"10.3390\/polym8020042","volume":"8","author":"C Dong","year":"2016","unstructured":"Dong C, Lv Y (2016) Application of collagen scaffold in tissue engineering: recent advances and new perspectives. Polymers 8(2):42","journal-title":"Polymers"},{"key":"2156_CR7","doi-asserted-by":"publisher","unstructured":"G\u00f6gele C, Hahn J, Elschner C, Breier A, Schr\u00f6pfer M, Prade I, Meyer M, Schulze-Tanzil G (2020a) Enhanced growth of lapine anterior cruciate ligament-derived fibroblasts on scaffolds embroidered from poly(l-lactide-co-$$\\varepsilon$$-caprolactone) and polylactic acid threads functionalized by fluorination and hexamethylene diisocyanate cross-linked collagen foams. Int J Mol Sci 21(3):1132. https:\/\/doi.org\/10.3390\/ijms21031132","DOI":"10.3390\/ijms21031132"},{"key":"2156_CR8","doi-asserted-by":"publisher","first-page":"572","DOI":"10.12968\/jowc.2020.29.10.572","volume":"29","author":"C G\u00f6gele","year":"2020","unstructured":"G\u00f6gele C, Schulze-Tanzil G, Kokozidou M, Gabel C, Billner M, Reichert B, Bodenschatz K (2020b) Growth characteristics of human juvenile, adult and murine fibroblasts: a comparison of polymer wound dressings. J Wound Care 29:572\u2013585","journal-title":"J Wound Care"},{"issue":"15","key":"2156_CR9","doi-asserted-by":"publisher","first-page":"8204","DOI":"10.3390\/ijms22158204","volume":"22","author":"C G\u00f6gele","year":"2021","unstructured":"G\u00f6gele C, Konrad J, Hahn J, Breier A, Schropfer M, Meyer M, Merkel R, Hoffmann B, Schulze-Tanzil G (2021) Maintenance of ligament homeostasis of spheroid-colonized embroidered and functionalized scaffolds after 3D stretch. Int J Mol Sci 22(15):8204","journal-title":"Int J Mol Sci"},{"key":"2156_CR10","doi-asserted-by":"publisher","unstructured":"Hahn J, Schulze-Tanzil G, Schr\u00f6pfer M, Meyer M, G\u00f6gele C, Hoyer M, Spickenheuer A, Heinrich G, Breier A (2019) Viscoelastic behavior of embroidered scaffolds for ACL tissue engineering made of PLA and P(LA-CL) after in vitro degradation. Int J Mol Sci 20(18):4655. https:\/\/doi.org\/10.3390\/ijms20184655","DOI":"10.3390\/ijms20184655"},{"key":"2156_CR11","doi-asserted-by":"publisher","first-page":"311","DOI":"10.1093\/abbs\/gmx005","volume":"49","author":"W Han","year":"2017","unstructured":"Han W, Chen L, Liu J, Guo A (2017) Enhanced tenogenic differentiation and tendon-like tissue formation by CHIP overexpression in tendon-derived stem cells. Acta Biochim Biophys Sin (Shanghai) 49:311\u2013317","journal-title":"Acta Biochim Biophys Sin (Shanghai)"},{"key":"2156_CR12","doi-asserted-by":"publisher","first-page":"290","DOI":"10.1016\/j.msec.2014.07.010","volume":"43","author":"M Hoyer","year":"2014","unstructured":"Hoyer M, Drechsel N, Meyer M, Meier C, Hinuber C, Breier A, Hahner J, Heinrich G, Rentsch C, Garbe LA, Ertel W, Schulze-Tanzil G, Lohan A (2014) Embroidered polymer-collagen hybrid scaffold variants for ligament tissue engineering. Mater Sci Eng C Mater Biol Appl 43:290\u2013299","journal-title":"Mater Sci Eng C Mater Biol Appl"},{"key":"2156_CR13","doi-asserted-by":"publisher","first-page":"226","DOI":"10.4161\/biom.22855","volume":"2","author":"J Kajahn","year":"2012","unstructured":"Kajahn J, Franz S, Rueckert E, Forstreuter I, Hintze V, Moeller S, Simon JC (2012) Artificial extracellular matrices composed of collagen I and high sulfated hyaluronan modulate monocyte to macrophage differentiation under conditions of sterile inflammation. Biomatter 2:226\u2013236","journal-title":"Biomatter"},{"key":"2156_CR14","doi-asserted-by":"publisher","first-page":"275","DOI":"10.1016\/j.actbio.2020.10.037","volume":"121","author":"Y Kawakami","year":"2021","unstructured":"Kawakami Y, Nonaka K, Fukase N, Amore A, Murata Y, Quinn P, Luketich S, Takayama K, Patel KG, Matsumoto T, Cummins JH, Kurosaka M, Kuroda R, Wagner WR, Fu FH, Huard J (2021) A cell-free biodegradable synthetic artificial ligament for the reconstruction of anterior cruciate ligament in a rat model. Acta Biomater 121:275\u2013287","journal-title":"Acta Biomater"},{"key":"2156_CR15","doi-asserted-by":"publisher","first-page":"168","DOI":"10.1016\/0003-2697(88)90532-5","volume":"174","author":"YJ Kim","year":"1988","unstructured":"Kim YJ, Sah RL, Doong JY, Grodzinsky AJ (1988) Fluorometric assay of DNA in cartilage explants using Hoechst 33258. Anal Biochem 174:168\u2013176","journal-title":"Anal Biochem"},{"key":"2156_CR16","doi-asserted-by":"publisher","first-page":"1579","DOI":"10.1039\/C6BM00958A","volume":"5","author":"S Liu","year":"2017","unstructured":"Liu S, Chen H, Wu T, Pan G, Fan C, Xu Y, Cui W (2017) Macrophage infiltration of electrospun polyester fibers. Biomater Sci 5:1579\u20131587","journal-title":"Biomater Sci"},{"issue":"7","key":"2156_CR17","doi-asserted-by":"publisher","first-page":"2059","DOI":"10.3390\/ijms19072059","volume":"19","author":"A Lohan","year":"2018","unstructured":"Lohan A, Kohl B, Meier C, Schulze-Tanzil G (2018) Tenogenesis of decellularized porcine Achilles tendon matrix reseeded with human tenocytes in the nude mice xenograft model. Int J Mol Sci 19(7):2059","journal-title":"Int J Mol Sci"},{"key":"2156_CR18","doi-asserted-by":"publisher","DOI":"10.1016\/j.jbiomech.2020.110011","volume":"112","author":"SJ Nelson","year":"2020","unstructured":"Nelson SJ, Creechley JJ, Wale ME, Lujan TJ (2020) Print-A-Punch: a 3D printed device to cut dumbbell-shaped specimens from soft tissue for tensile testing. J Biomech 112:110011","journal-title":"J Biomech"},{"key":"2156_CR19","doi-asserted-by":"publisher","first-page":"2024","DOI":"10.1016\/j.biomaterials.2012.11.046","volume":"34","author":"M Ni","year":"2013","unstructured":"Ni M, Rui YF, Tan Q, Liu Y, Xu LL, Chan KM, Wang Y, Li G (2013) Engineered scaffold-free tendon tissue produced by tendon-derived stem cells. Biomaterials 34:2024\u20132037","journal-title":"Biomaterials"},{"key":"2156_CR20","doi-asserted-by":"publisher","first-page":"1844","DOI":"10.1089\/scd.2014.0124","volume":"23","author":"S Noack","year":"2014","unstructured":"Noack S, Seiffart V, Willbold E, Laggies S, Winkel A, Shahab-Osterloh S, Florkemeier T, Hertwig F, Steinhoff C, Nuber UA, Gross G, Hoffmann A (2014) Periostin secreted by mesenchymal stem cells supports tendon formation in an ectopic mouse model. Stem Cells Dev 23:1844\u20131857","journal-title":"Stem Cells Dev"},{"key":"2156_CR21","doi-asserted-by":"publisher","first-page":"334","DOI":"10.1016\/S0268-0033(01)00007-9","volume":"16","author":"MM Panjabi","year":"2001","unstructured":"Panjabi MM, Courtney TW (2001) High-speed subfailure stretch of rabbit anterior cruciate ligament: changes in elastic, failure and viscoelastic characteristics. Clin Biomech (Bristol, Avon) 16:334\u2013340","journal-title":"Clin Biomech (Bristol, Avon)"},{"key":"2156_CR22","doi-asserted-by":"publisher","first-page":"4754","DOI":"10.1038\/s41598-020-61725-5","volume":"10","author":"M Rashid","year":"2020","unstructured":"Rashid M, Dudhia J, Dakin SG, Snelling SJB, De Godoy R, Mouthuy PA, Smith RKW, Morrey M, Carr AJ (2020) Histopathological and immunohistochemical evaluation of cellular response to a woven and electrospun polydioxanone (PDO) and polycaprolactone (PCL) patch for tendon repair. Sci Rep 10:4754","journal-title":"Sci Rep"},{"key":"2156_CR23","doi-asserted-by":"publisher","DOI":"10.1155\/2012\/303724","volume":"2012","author":"S Rathbone","year":"2012","unstructured":"Rathbone S, Maffulli N, Cartmell SH (2012) Most British surgeons would consider using a tissue-engineered anterior cruciate ligament: a questionnaire study. Stem Cells Int 2012:303724","journal-title":"Stem Cells Int"},{"key":"2156_CR24","doi-asserted-by":"crossref","unstructured":"Reifenrath J, Wellmann M, Kempfert M, Angrisani N, Welke B, Gniesmer S, Kampmann A, Menzel H, Willbold E (2020) TGF-beta3 Loaded Electrospun Polycaprolacton Fibre Scaffolds for Rotator Cuff Tear Repair: An in Vivo Study in Rats. Int J Mol Sci 21.","DOI":"10.3390\/ijms21031046"},{"key":"2156_CR25","doi-asserted-by":"publisher","first-page":"226","DOI":"10.2174\/1574888X12666170915120135","volume":"13","author":"TC Riley","year":"2018","unstructured":"Riley TC, Mafi R, Mafi P, Khan WS (2018) Knee ligament injury and the clinical application of tissue engineering techniques: a systematic review. Curr Stem Cell Res Ther 13:226\u2013234","journal-title":"Curr Stem Cell Res Ther"},{"key":"2156_CR26","doi-asserted-by":"publisher","first-page":"306","DOI":"10.1016\/j.actbio.2018.03.004","volume":"71","author":"AD Schoenenberger","year":"2018","unstructured":"Schoenenberger AD, Foolen J, Moor P, Silvan U, Snedeker JG (2018) Substrate fiber alignment mediates tendon cell response to inflammatory signaling. Acta Biomater 71:306\u2013317","journal-title":"Acta Biomater"},{"key":"2156_CR27","doi-asserted-by":"publisher","first-page":"11340","DOI":"10.1038\/s41598-018-29583-4","volume":"8","author":"M Scholze","year":"2018","unstructured":"Scholze M, Singh A, Lozano PF, Ondruschka B, Ramezani M, Werner M, Hammer N (2018) Utilization of 3D printing technology to facilitate and standardize soft tissue testing. Sci Rep 8:11340","journal-title":"Sci Rep"},{"key":"2156_CR28","doi-asserted-by":"publisher","first-page":"5498","DOI":"10.1021\/acsomega.0c00126","volume":"5","author":"M Schr\u00f6pfer","year":"2020","unstructured":"Schr\u00f6pfer M, Junghans F, Voigt D, Meyer M, Breier A, Schulze-Tanzil G, Prade I (2020) Gas-phase fluorination on PLA improves cell adhesion and spreading. ACS Omega 5:5498\u20135507","journal-title":"ACS Omega"},{"key":"2156_CR29","doi-asserted-by":"publisher","first-page":"561","DOI":"10.1302\/2046-3758.118.BJR-2021-0576.R1","volume":"11","author":"GG Schulze-Tanzil","year":"2022","unstructured":"Schulze-Tanzil GG, Delgado-Calcares M, Stange R, Wildemann B, Docheva D (2022) Tendon healing: a concise review on cellular and molecular mechanisms with a particular focus on the Achilles tendon. Bone Joint Res 11:561\u2013574","journal-title":"Bone Joint Res"},{"issue":"1","key":"2156_CR30","doi-asserted-by":"publisher","first-page":"6","DOI":"10.3390\/medicines9010006","volume":"9","author":"A Sivam","year":"2022","unstructured":"Sivam A, Enninghorst N (2022) The dilemma of reconstructive material choice for orbital floor fracture: a narrative review. Medicines 9(1):6","journal-title":"Medicines"},{"issue":"1\u20133","key":"2156_CR31","doi-asserted-by":"publisher","first-page":"13","DOI":"10.1016\/S0141-3910(97)00183-3","volume":"59","author":"K Tomihata","year":"1998","unstructured":"Tomihata K, Suzuki M, Oka T, Ikada Y (1998) A new resorbable monofilament suture. Polym Degrad Stab 59(1\u20133):13\u201318. https:\/\/doi.org\/10.1016\/S0141-3910(97)00183-3","journal-title":"Polym Degrad Stab"},{"key":"2156_CR32","doi-asserted-by":"publisher","first-page":"2760","DOI":"10.1016\/j.biomaterials.2013.12.042","volume":"35","author":"Y Xu","year":"2014","unstructured":"Xu Y, Dong S, Zhou Q, Mo X, Song L, Hou T, Wu J, Li S, Li Y, Li P, Gan Y, Xu J (2014) The effect of mechanical stimulation on the maturation of TDSCs-poly(L-lactide-co-e-caprolactone)\/collagen scaffold constructs for tendon tissue engineering. Biomaterials 35:2760\u20132772","journal-title":"Biomaterials"}],"container-title":["Histochemistry and Cell Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s00418-022-02156-3.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1007\/s00418-022-02156-3\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s00418-022-02156-3.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,3,10]],"date-time":"2023-03-10T17:04:54Z","timestamp":1678467894000},"score":1,"resource":{"primary":{"URL":"https:\/\/link.springer.com\/10.1007\/s00418-022-02156-3"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,10,29]]},"references-count":32,"journal-issue":{"issue":"3","published-print":{"date-parts":[[2023,3]]}},"alternative-id":["2156"],"URL":"http:\/\/dx.doi.org\/10.1007\/s00418-022-02156-3","relation":{},"ISSN":["0948-6143","1432-119X"],"issn-type":[{"value":"0948-6143","type":"print"},{"value":"1432-119X","type":"electronic"}],"subject":["Cell Biology","Medical Laboratory Technology","Molecular Biology","Histology"],"published":{"date-parts":[[2022,10,29]]},"assertion":[{"value":"16 September 2022","order":1,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"29 October 2022","order":2,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"The authors declare no competing interests.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}},{"value":"All authors declared that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Conflict of Interest"}}]}}