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Published in: BMC Musculoskeletal Disorders 1/2013

Open Access 01-12-2013 | Research article

Response of human chondrocytes and mesenchymal stromal cells to a decellularized human dermis

Authors: Gianluca Giavaresi, Elena Bondioli, Davide Melandri, Roberto Giardino, Matilde Tschon, Paola Torricelli, Giovanna Cenacchi, Roberto Rotini, Alessandro Castagna, Francesca Veronesi, Stefania Pagani, Milena Fini

Published in: BMC Musculoskeletal Disorders | Issue 1/2013

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Abstract

Background

Although progress has been made in the treatment of articular cartilage lesions, they are still a major challenge because current techniques do not provide satisfactory long-term outcomes. Tissue engineering and the use of functional biomaterials might be an alternative regenerative strategy and fulfill clinical needs. Decellularized extracellular matrices have generated interest as functional biologic scaffolds, but there are few studies on cartilage regeneration. The aim of this study was to evaluate in vitro the biological influence of a newly developed decellularized human dermal extracellular matrix on two human primary cultures.

Methods

Normal human articular chondrocytes (NHAC-kn) and human mesenchymal stromal cells (hMSC) from healthy donors were seeded in polystyrene wells as controls (CTR), and on decellularized human dermis batches (HDM_derm) for 7 and 14 days. Cellular proliferation and differentiation, and anabolic and catabolic synthetic activity were quantified at each experimental time. Histology and scanning electron microscopy were used to evaluate morphology and ultrastructure.

Results

Both cell cultures had a similar proliferation rate that increased significantly (p < 0.0005) at 14 days. In comparison with CTR, at 14 days NHAC-kn enhanced procollagen type II (CPII, p < 0.05) and aggrecan synthesis (p < 0.0005), whereas hMSC significantly enhanced aggrecan synthesis (p < 0.0005) and transforming growth factor-beta1 release (TGF-β1, p < 0.0005) at both experimental times. Neither inflammatory stimulus nor catabolic activity induction was observed. By comparing data of the two primary cells, NHAC-kn synthesized significantly more CPII than did hMSC at both experimental times (p < 0.005), whereas hMSC synthesized more aggrecan at 7 days (p < 0.005) and TGF-β1 at both experimental times than did NHAC-kn (p < 0.005).

Conclusions

The results obtained showed that in in vitro conditions HDM_derm behaves as a suitable scaffold for the growth of both well-differentiated chondrocytes and undifferentiated mesenchymal cells, thus ensuring a biocompatible and bioactive substrate. Further studies are mandatory to test the use of HDM_derm with tissue engineering to assess its therapeutic and functional effectiveness in cartilage regeneration.
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Literature
1.
go back to reference Ahmed TA, Hincke MT: Strategies for articular cartilage lesion repair and functional restoration. Tissue Engineering. 2010, 16B: 305-329.CrossRef Ahmed TA, Hincke MT: Strategies for articular cartilage lesion repair and functional restoration. Tissue Engineering. 2010, 16B: 305-329.CrossRef
2.
go back to reference Jiang Y, Chen LK, Zhu DC, Zhang GR, Guo C, Qi YY, Ouyang HW: The inductive effect of bone morphogenetic protein-4 on chondral-lineage differentiation and in situ cartilage repair. Tissue Eng Part A. 2010, 16: 1621-1632.CrossRefPubMed Jiang Y, Chen LK, Zhu DC, Zhang GR, Guo C, Qi YY, Ouyang HW: The inductive effect of bone morphogenetic protein-4 on chondral-lineage differentiation and in situ cartilage repair. Tissue Eng Part A. 2010, 16: 1621-1632.CrossRefPubMed
3.
go back to reference Ge Z, Li C, Heng BC, Cao G, Yang Z: Functional biomaterials for cartilage regeneration. J Biomed Mater Res A. 2012, 100: 2526-2536.PubMed Ge Z, Li C, Heng BC, Cao G, Yang Z: Functional biomaterials for cartilage regeneration. J Biomed Mater Res A. 2012, 100: 2526-2536.PubMed
4.
go back to reference Little CJ, Bawolin NK, Chen X: Mechanical properties of natural cartilage and tissue-engineered constructs. Tissue Eng Part B Rev. 2011, 17: 213-227.CrossRefPubMed Little CJ, Bawolin NK, Chen X: Mechanical properties of natural cartilage and tissue-engineered constructs. Tissue Eng Part B Rev. 2011, 17: 213-227.CrossRefPubMed
5.
go back to reference Wolf MT, Daly KA, Reing JE, Badylak SF: Biologic scaffold composed of skeletal muscle extracellular matrix. Biomaterials. 2012, 33: 2916-2925. 10.1016/j.biomaterials.2011.12.055.CrossRefPubMed Wolf MT, Daly KA, Reing JE, Badylak SF: Biologic scaffold composed of skeletal muscle extracellular matrix. Biomaterials. 2012, 33: 2916-2925. 10.1016/j.biomaterials.2011.12.055.CrossRefPubMed
6.
go back to reference Bondioli E, Fini M, Veronesi F, Giavaresi G, Tschon M, Cenacchi G, Cerasoli S, Giardino R, Melandri D: Development and evaluation of a decellularized membrane from human dermis. J Tissue Eng Regen Med. 2012, 10.1002/term.1530 [Epub ahead of print]. Bondioli E, Fini M, Veronesi F, Giavaresi G, Tschon M, Cenacchi G, Cerasoli S, Giardino R, Melandri D: Development and evaluation of a decellularized membrane from human dermis. J Tissue Eng Regen Med. 2012, 10.1002/term.1530 [Epub ahead of print].
7.
go back to reference Rotini R, Marinelli A, Guerra E, Bettelli G, Castagna A, Fini M, Bondioli E, Busacca M: Human dermal matrix scaffold augmentation for large and massive rotator cuff repairs: preliminary clinical and MRI results at 1-year follow-up. Musculoskelet Surg. 2011, 95 (Suppl 1): S13-23.CrossRefPubMed Rotini R, Marinelli A, Guerra E, Bettelli G, Castagna A, Fini M, Bondioli E, Busacca M: Human dermal matrix scaffold augmentation for large and massive rotator cuff repairs: preliminary clinical and MRI results at 1-year follow-up. Musculoskelet Surg. 2011, 95 (Suppl 1): S13-23.CrossRefPubMed
8.
go back to reference Choi YC, Choi JS, Kim BS, Kim JD, Yoon HI, Cho YW: Decellularized extracellular matrix derived from porcine adipose tissue as a xenogeneic biomaterial for tissue engineering. Tissue Eng Part C Methods. 2012, Epub ahead of print Choi YC, Choi JS, Kim BS, Kim JD, Yoon HI, Cho YW: Decellularized extracellular matrix derived from porcine adipose tissue as a xenogeneic biomaterial for tissue engineering. Tissue Eng Part C Methods. 2012, Epub ahead of print
9.
go back to reference Yang Q, Peng J, Guo Q, Huang J, Zhang L, Yao J, Yang F, Wang S, Xu W, Wang A, Lu S: A cartilage ECM-derived 3-D porous acellular matrix scaffold for in vivo cartilage tissue engineering with PKH26-labeled chondrogenic bone marrow-derived mesenchymal stem cells. Biomaterials. 2008, 29: 2378-87. 10.1016/j.biomaterials.2008.01.037.CrossRefPubMed Yang Q, Peng J, Guo Q, Huang J, Zhang L, Yao J, Yang F, Wang S, Xu W, Wang A, Lu S: A cartilage ECM-derived 3-D porous acellular matrix scaffold for in vivo cartilage tissue engineering with PKH26-labeled chondrogenic bone marrow-derived mesenchymal stem cells. Biomaterials. 2008, 29: 2378-87. 10.1016/j.biomaterials.2008.01.037.CrossRefPubMed
10.
go back to reference Yang Z, Shi Y, Wei X, He J, Yang S, Dickson G, Tang J, Xiang J, Song C, Li G: Fabrication and repair of cartilage defects with a novel acellular cartilage matrix scaffold. Tissue Eng Part C Methods. 2010, 16: 865-76. 10.1089/ten.tec.2009.0444.CrossRefPubMed Yang Z, Shi Y, Wei X, He J, Yang S, Dickson G, Tang J, Xiang J, Song C, Li G: Fabrication and repair of cartilage defects with a novel acellular cartilage matrix scaffold. Tissue Eng Part C Methods. 2010, 16: 865-76. 10.1089/ten.tec.2009.0444.CrossRefPubMed
11.
go back to reference Gong YY, Xue JX, Zhang WJ, Zhou GD, Liu W, Cao Y: A sandwich model for engineering cartilage with acellular cartilage sheets and chondrocytes. Biomaterials. 2011, 32: 2265-73. 10.1016/j.biomaterials.2010.11.078.CrossRefPubMed Gong YY, Xue JX, Zhang WJ, Zhou GD, Liu W, Cao Y: A sandwich model for engineering cartilage with acellular cartilage sheets and chondrocytes. Biomaterials. 2011, 32: 2265-73. 10.1016/j.biomaterials.2010.11.078.CrossRefPubMed
12.
go back to reference Kim BS, Choi JS, Kim JD, Choi YC, Cho YW: Recellularization of decellularized human adipose-tissue-derived extracellular matrix sheets with other human cell types. Cell Tissue Res. 2012, 348: 559-67. 10.1007/s00441-012-1391-y.CrossRefPubMed Kim BS, Choi JS, Kim JD, Choi YC, Cho YW: Recellularization of decellularized human adipose-tissue-derived extracellular matrix sheets with other human cell types. Cell Tissue Res. 2012, 348: 559-67. 10.1007/s00441-012-1391-y.CrossRefPubMed
13.
go back to reference Schwarz S, Koerber L, Elsaesser AF, Goldberg-Bockhorn E, Seitz AM, Dürselen L, Ignatius A, Walther P, Breiter R, Rotter N: Decellularized cartilage matrix as a novel biomatrix for cartilage tissue-engineering applications. Tissue Eng Part A. 2012, Epub ahead of print Schwarz S, Koerber L, Elsaesser AF, Goldberg-Bockhorn E, Seitz AM, Dürselen L, Ignatius A, Walther P, Breiter R, Rotter N: Decellularized cartilage matrix as a novel biomatrix for cartilage tissue-engineering applications. Tissue Eng Part A. 2012, Epub ahead of print
14.
go back to reference Fini M, Bondioli E, Castagna A, Torricelli P, Giavaresi G, Rotini R, Marinelli A, Guerra E, Orlandi C, Carboni A, Aiti A, Benedettini E, Giardino R, Melandri D: Decellularized human dermis to treat massive rotator cuff tears: in vitro evaluations. Connect Tissue Res. 2012, 53: 298-306. 10.3109/03008207.2011.649929.CrossRefPubMed Fini M, Bondioli E, Castagna A, Torricelli P, Giavaresi G, Rotini R, Marinelli A, Guerra E, Orlandi C, Carboni A, Aiti A, Benedettini E, Giardino R, Melandri D: Decellularized human dermis to treat massive rotator cuff tears: in vitro evaluations. Connect Tissue Res. 2012, 53: 298-306. 10.3109/03008207.2011.649929.CrossRefPubMed
15.
go back to reference Kutsuna T, Inoue H, Takeda H, Takahashi T, Yamamoto H, Miura H, Higashiyama S: Fibronectin regulates proteoglycan production balance in transforming growth factor-β1-induced chondrogenesis. Int J Mol Med. 2011, 28: 829-34.PubMed Kutsuna T, Inoue H, Takeda H, Takahashi T, Yamamoto H, Miura H, Higashiyama S: Fibronectin regulates proteoglycan production balance in transforming growth factor-β1-induced chondrogenesis. Int J Mol Med. 2011, 28: 829-34.PubMed
16.
go back to reference Fortier LA, Barker JU, Strauss EJ, McCarrel TM, Cole BJ: The role of growth factors in cartilage repair. Clin Orthop Relat Res. 2011, 469: 2706-15. 10.1007/s11999-011-1857-3.CrossRefPubMedPubMedCentral Fortier LA, Barker JU, Strauss EJ, McCarrel TM, Cole BJ: The role of growth factors in cartilage repair. Clin Orthop Relat Res. 2011, 469: 2706-15. 10.1007/s11999-011-1857-3.CrossRefPubMedPubMedCentral
17.
go back to reference Pei M, Li JT, Shoukry M, Zhang Y: A review of decellularized stem cell matrix: a novel cell expansion system for cartilage tissue engineering. Eur Cell Mater. 2011, 22: 333-43.PubMed Pei M, Li JT, Shoukry M, Zhang Y: A review of decellularized stem cell matrix: a novel cell expansion system for cartilage tissue engineering. Eur Cell Mater. 2011, 22: 333-43.PubMed
18.
go back to reference Hoganson DM, O’Doherty EM, Owens GE, Harilal DO, Goldman SM, Bowley CM, Neville CM, Kronengold RT, Vacanti JP: The retention of extracellular matrix proteins and angiogenic and mitogenic cytokines in a decellularized porcine dermis. Biomaterials. 2010, 31: 6730-7. 10.1016/j.biomaterials.2010.05.019.CrossRefPubMed Hoganson DM, O’Doherty EM, Owens GE, Harilal DO, Goldman SM, Bowley CM, Neville CM, Kronengold RT, Vacanti JP: The retention of extracellular matrix proteins and angiogenic and mitogenic cytokines in a decellularized porcine dermis. Biomaterials. 2010, 31: 6730-7. 10.1016/j.biomaterials.2010.05.019.CrossRefPubMed
19.
go back to reference Hoganson DM, Owens GE, O’Doherty EM, Bowley CM, Goldman SM, Harilal DO, Neville CM, Kronengold RT, Vacanti JP: Preserved extracellular matrix components and retained biological activity in decellularized porcine mesothelium. Biomaterials. 2010, 31: 6934-40. 10.1016/j.biomaterials.2010.05.026.CrossRefPubMed Hoganson DM, Owens GE, O’Doherty EM, Bowley CM, Goldman SM, Harilal DO, Neville CM, Kronengold RT, Vacanti JP: Preserved extracellular matrix components and retained biological activity in decellularized porcine mesothelium. Biomaterials. 2010, 31: 6934-40. 10.1016/j.biomaterials.2010.05.026.CrossRefPubMed
20.
go back to reference Yang B, Zhang Y, Zhou L, Sun Z, Zheng J, Chen Y, Dai Y: Development of a porcine bladder acellular matrix with well-preserved extracellular bioactive factors for tissue engineering. Tissue Eng Part C Methods. 2010, 16: 1201-11.CrossRefPubMed Yang B, Zhang Y, Zhou L, Sun Z, Zheng J, Chen Y, Dai Y: Development of a porcine bladder acellular matrix with well-preserved extracellular bioactive factors for tissue engineering. Tissue Eng Part C Methods. 2010, 16: 1201-11.CrossRefPubMed
21.
go back to reference Mahmoudifar N, Doran PM: Chondrogenesis and cartilage tissue engineering: the longer road to technology development. Trends Biotechnol. 2012, 30: 166-76. 10.1016/j.tibtech.2011.09.002.CrossRefPubMed Mahmoudifar N, Doran PM: Chondrogenesis and cartilage tissue engineering: the longer road to technology development. Trends Biotechnol. 2012, 30: 166-76. 10.1016/j.tibtech.2011.09.002.CrossRefPubMed
22.
go back to reference Zhang L, Yuan T, Guo L, Zhang X: An in vitro study of collagen hydrogel to induce the chondrogenic differentiation of mesenchymal stem cells. J Biomed Mater Res A. 2012, 100: 2717-25.CrossRefPubMed Zhang L, Yuan T, Guo L, Zhang X: An in vitro study of collagen hydrogel to induce the chondrogenic differentiation of mesenchymal stem cells. J Biomed Mater Res A. 2012, 100: 2717-25.CrossRefPubMed
23.
go back to reference Abarrategi A, Lópiz-Morales Y, Ramos V, Civantos A, López-Durán L, Marco F, López-Lacomba JL: Chitosan scaffolds for osteochondral tissue regeneration. J Biomed Mater Res A. 2010, 95: 1132-41.CrossRefPubMed Abarrategi A, Lópiz-Morales Y, Ramos V, Civantos A, López-Durán L, Marco F, López-Lacomba JL: Chitosan scaffolds for osteochondral tissue regeneration. J Biomed Mater Res A. 2010, 95: 1132-41.CrossRefPubMed
24.
go back to reference Herlofsen SR, Küchler AM, Melvik JE, Brinchmann JE: Chondrogenic differentiation of human bone marrow-derived mesenchymal stem cells in self-gelling alginate discs reveals novel chondrogenic signature gene clusters. Tissue Eng Part A. 2011, 17: 1003-13. 10.1089/ten.tea.2010.0499.CrossRefPubMed Herlofsen SR, Küchler AM, Melvik JE, Brinchmann JE: Chondrogenic differentiation of human bone marrow-derived mesenchymal stem cells in self-gelling alginate discs reveals novel chondrogenic signature gene clusters. Tissue Eng Part A. 2011, 17: 1003-13. 10.1089/ten.tea.2010.0499.CrossRefPubMed
25.
go back to reference Chen WC, Wei YH, Chu IM, Yao CL: Effect of chondroitin sulphate C on the in vitro and in vivo chondrogenesis of mesenchymal stem cells in crosslinked type II collagen scaffolds. J Tissue Eng Regen Med. 2012, 10.1002/term.1463 [Epub ahead of print]. Chen WC, Wei YH, Chu IM, Yao CL: Effect of chondroitin sulphate C on the in vitro and in vivo chondrogenesis of mesenchymal stem cells in crosslinked type II collagen scaffolds. J Tissue Eng Regen Med. 2012, 10.1002/term.1463 [Epub ahead of print].
26.
go back to reference Unterman SA, Gibson M, Lee JH, Crist J, Chansakul T, Yang EC, Elisseeff JH: Hyaluronic acid-binding scaffold for articular cartilage repair. Tissue Eng Part A. 2012, Epub ahead of print Unterman SA, Gibson M, Lee JH, Crist J, Chansakul T, Yang EC, Elisseeff JH: Hyaluronic acid-binding scaffold for articular cartilage repair. Tissue Eng Part A. 2012, Epub ahead of print
27.
go back to reference Chen J, Chen H, Li P, Diao H, Zhu S, Dong L, Wang R, Guo T, Zhao J, Zhang J: Simultaneous regeneration of articular cartilage and subchondral bone in vivo using MSCs induced by a spatially controlled gene delivery system in bilayered integrated scaffolds. Biomaterials. 2011, 32: 4793-805. 10.1016/j.biomaterials.2011.03.041.CrossRefPubMed Chen J, Chen H, Li P, Diao H, Zhu S, Dong L, Wang R, Guo T, Zhao J, Zhang J: Simultaneous regeneration of articular cartilage and subchondral bone in vivo using MSCs induced by a spatially controlled gene delivery system in bilayered integrated scaffolds. Biomaterials. 2011, 32: 4793-805. 10.1016/j.biomaterials.2011.03.041.CrossRefPubMed
28.
go back to reference Bhardwaj N, Kundu SC: Chondrogenic differentiation of rat MSCs on porous scaffolds of silk fibroin/chitosan blends. Biomaterials. 2012, 33: 2848-57. 10.1016/j.biomaterials.2011.12.028.CrossRefPubMed Bhardwaj N, Kundu SC: Chondrogenic differentiation of rat MSCs on porous scaffolds of silk fibroin/chitosan blends. Biomaterials. 2012, 33: 2848-57. 10.1016/j.biomaterials.2011.12.028.CrossRefPubMed
29.
go back to reference Ahmed TA, Giulivi A, Griffith M, Hincke M: Fibrin glues in combination with mesenchymal stem cells to develop a tissue-engineered cartilage substitute. Tissue Eng Part A. 2011, 17: 323-35. 10.1089/ten.tea.2009.0773.CrossRefPubMed Ahmed TA, Giulivi A, Griffith M, Hincke M: Fibrin glues in combination with mesenchymal stem cells to develop a tissue-engineered cartilage substitute. Tissue Eng Part A. 2011, 17: 323-35. 10.1089/ten.tea.2009.0773.CrossRefPubMed
30.
go back to reference Lu H, Hoshiba T, Kawazoe N, Koda I, Song M, Chen G: Cultured cell-derived extracellular matrix scaffolds for tissue engineering. Biomaterials. 2011, 32: 9658-66. 10.1016/j.biomaterials.2011.08.091.CrossRefPubMed Lu H, Hoshiba T, Kawazoe N, Koda I, Song M, Chen G: Cultured cell-derived extracellular matrix scaffolds for tissue engineering. Biomaterials. 2011, 32: 9658-66. 10.1016/j.biomaterials.2011.08.091.CrossRefPubMed
31.
go back to reference Izal I, Aranda P, Sanz-Ramos P, Ripalda P, Mora G, Granero-Moltó F, Deplaine H, Gómez-Ribelles JL, Ferrer GG, Acosta V, Ochoa I, García-Aznar JM, Andreu EJ, Monleón-Pradas M, Doblaré M, Prósper F: Culture of human bone marrow-derived mesenchymal stem cells on of poly(L: -lactic acid) scaffolds: potential application for the tissue engineering of cartilage. Knee Surg Sports Traumatol Arthrosc. 2012, Epub ahead of print Izal I, Aranda P, Sanz-Ramos P, Ripalda P, Mora G, Granero-Moltó F, Deplaine H, Gómez-Ribelles JL, Ferrer GG, Acosta V, Ochoa I, García-Aznar JM, Andreu EJ, Monleón-Pradas M, Doblaré M, Prósper F: Culture of human bone marrow-derived mesenchymal stem cells on of poly(L: -lactic acid) scaffolds: potential application for the tissue engineering of cartilage. Knee Surg Sports Traumatol Arthrosc. 2012, Epub ahead of print
32.
go back to reference Mahmoudifar N, Doran PM: Chondrogenic differentiation of human adipose-derived stem cells in polyglycolic acid mesh scaffolds under dynamic culture conditions. Biomaterials. 2010, 31: 3858-67. 10.1016/j.biomaterials.2010.01.090.CrossRefPubMed Mahmoudifar N, Doran PM: Chondrogenic differentiation of human adipose-derived stem cells in polyglycolic acid mesh scaffolds under dynamic culture conditions. Biomaterials. 2010, 31: 3858-67. 10.1016/j.biomaterials.2010.01.090.CrossRefPubMed
33.
go back to reference Fan H, Tao H, Wu Y, Hu Y, Yan Y, Luo Z: TGF-β3 immobilized PLGA-gelatin/chondroitin sulfate/hyaluronic acid hybrid scaffold for cartilage regeneration. J Biomed Mater Res A. 2010, 95: 982-92.CrossRefPubMed Fan H, Tao H, Wu Y, Hu Y, Yan Y, Luo Z: TGF-β3 immobilized PLGA-gelatin/chondroitin sulfate/hyaluronic acid hybrid scaffold for cartilage regeneration. J Biomed Mater Res A. 2010, 95: 982-92.CrossRefPubMed
34.
go back to reference Lin PB, Ning LJ, Lian QZ, Xia Z, Xin Y, Sen BH, Fei NF: A study on repair of porcine articular cartilage defects with tissue-engineered cartilage constructed in vivo by composite scaffold materials. Ann Plast Surg. 2010, 65: 430-6. 10.1097/SAP.0b013e3181d6e38b.CrossRefPubMed Lin PB, Ning LJ, Lian QZ, Xia Z, Xin Y, Sen BH, Fei NF: A study on repair of porcine articular cartilage defects with tissue-engineered cartilage constructed in vivo by composite scaffold materials. Ann Plast Surg. 2010, 65: 430-6. 10.1097/SAP.0b013e3181d6e38b.CrossRefPubMed
35.
go back to reference Liu J, Song H, Zhang L, Xu H, Zhao X: Self-assembly-peptide hydrogels as tissue-engineering scaffolds for three-dimensional culture of chondrocytes in vitro. Macromol Biosci. 2010, 10: 1164-70. 10.1002/mabi.200900450.CrossRefPubMed Liu J, Song H, Zhang L, Xu H, Zhao X: Self-assembly-peptide hydrogels as tissue-engineering scaffolds for three-dimensional culture of chondrocytes in vitro. Macromol Biosci. 2010, 10: 1164-70. 10.1002/mabi.200900450.CrossRefPubMed
36.
go back to reference Yoon IS, Chung CW, Sung JH, Cho HJ, Kim JS, Shim WS, Shim CK, Chung SJ, Kim DD: Proliferation and chondrogenic differentiation of human adipose-derived mesenchymal stem cells in porous hyaluronic acid scaffold. J Biosci Bioeng. 2011, 112: 402-8. 10.1016/j.jbiosc.2011.06.018.CrossRefPubMed Yoon IS, Chung CW, Sung JH, Cho HJ, Kim JS, Shim WS, Shim CK, Chung SJ, Kim DD: Proliferation and chondrogenic differentiation of human adipose-derived mesenchymal stem cells in porous hyaluronic acid scaffold. J Biosci Bioeng. 2011, 112: 402-8. 10.1016/j.jbiosc.2011.06.018.CrossRefPubMed
37.
go back to reference Brennan EP, Reing J, Chev D, Myers-Irvin JM, Young EG, Badylak SF: Antibacterial activity within degradation products of biological scaffolds composed of extracellular matrix. Tissue Eng. 2006, 12: 2944-2955.CrossRef Brennan EP, Reing J, Chev D, Myers-Irvin JM, Young EG, Badylak SF: Antibacterial activity within degradation products of biological scaffolds composed of extracellular matrix. Tissue Eng. 2006, 12: 2944-2955.CrossRef
Metadata
Title
Response of human chondrocytes and mesenchymal stromal cells to a decellularized human dermis
Authors
Gianluca Giavaresi
Elena Bondioli
Davide Melandri
Roberto Giardino
Matilde Tschon
Paola Torricelli
Giovanna Cenacchi
Roberto Rotini
Alessandro Castagna
Francesca Veronesi
Stefania Pagani
Milena Fini
Publication date
01-12-2013
Publisher
BioMed Central
Published in
BMC Musculoskeletal Disorders / Issue 1/2013
Electronic ISSN: 1471-2474
DOI
https://doi.org/10.1186/1471-2474-14-12

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