Top

International Orthopaedics

Published in:

01-11-2017 | Original Paper

Tissue engineering-relevant characteristics of ex vivo and monolayer-expanded chondrocytes from the notch versus trochlea of human knee joints

Authors: Matthias Aurich, Gunther Olaf Hofmann, Bernd Rolauffs

Published in: International Orthopaedics | Issue 11/2017

Abstract

Purpose

The aim was to analyse the biological characteristics of chondrocytes from the two biopsy sites notch vs. trochlea of human knee joints. The question was whether tissue engineering-relevant characteristics such as viability and mRNA expression profile would be comparable ex vivo and after monolayer expansion, as these are parts of routine autologous chondrocyte implantation (ACI).

Methods

Biopsies from the intercondylar notch and the lateral aspect of the trochlea from 20 patients with ICRS grades 3 and 4 cartilage defects were harvested during arthroscopy. Collagen types 1, 2, and 10 mRNA were quantified by polymerase chain reaction.

Results

Compared with notch chondrocytes, ex vivo trochlea chondrocytes had comparable cell numbers, vitality and aggrecan, collagen types 1, −2 and −10 mRNA expression. After monolayer expansion both notch and trochlea chondrocyte characteristics were comparably altered, regardless of their biopsy origin, and no significant differences in viability and mRNA expression were noted.

Conclusions

Collectively, these findings suggest that tissue engineering-relevant characteristics of notch and trochlea chondrocytes are comparable ex vivo and after monolayer expansion. Thus, trochlea chondrocytes promise clinical potential and chondrocytes for ACI could potentially be generated from both notch and trochlea biopsy sites.

Heijink A, Gomoll AH, Madry H, Drobnic M, Filardo G, Espregueira-Mendes J, Van Dijk CN (2012) Biomechanical considerations in the pathogenesis of osteoarthritis of the knee. Knee Surg Sports Traumatol Arthrosc 20:423–435. https://doi.org/10.1007/s00167-011-1818-0 CrossRefPubMed

Johnstone B, Alini M, Cucchiarini M, Dodge GR, Eglin D, Guilak F, Madry H, Mata A, Mauck RL, Semino CE, Stoddart MJ (2013) Tissue engineering for articular cartilage repair--the state of the art. Eur Cells Mater 25:248–267CrossRef

Kon E, Filardo G, Di Matteo B, Perdisa F, Marcacci M (2013) Matrix assisted autologous chondrocyte transplantation for cartilage treatment: A systematic review. Bone Joint Res 2:18–25. https://doi.org/10.1302/2046-3758.22.2000092 CrossRefPubMedPubMedCentral

Niemeyer P, Albrecht D, Andereya S, Angele P, Ateschrang A, Aurich M, Baumann M, Bosch U, Erggelet C, Fickert S, Gebhard H, Gelse K, Gunther D, Hoburg A, Kasten P, Kolombe T, Madry H, Marlovits S, Meenen NM, Muller PE, Noth U, Petersen JP, Pietschmann M, Richter W, Rolauffs B, Rhunau K, Schewe B, Steinert A, Steinwachs MR, Welsch GH, Zinser W, Fritz J (2016) Autologous chondrocyte implantation (ACI) for cartilage defects of the knee: a guideline by the working group “Clinical tissue regeneration” of the German Society of Orthopaedics and Trauma (DGOU). Knee. https://doi.org/10.1016/j.knee.2016.02.001

Niemeyer P, Andereya S, Angele P, Ateschrang A, Aurich M, Baumann M, Behrens P, Bosch U, Erggelet C, Fickert S, Fritz J, Gebhard H, Gelse K, Gunther D, Hoburg A, Kasten P, Kolombe T, Madry H, Marlovits S, Meenen NM, Muller PE, Noth U, Petersen JP, Pietschmann M, Richter W, Rolauffs B, Rhunau K, Schewe B, Steinert A, Steinwachs MR, Welsch GH, Zinser W, Albrecht D (2013) Autologous chondrocyte implantation (ACI) for cartilage defects of the knee: a guideline by the working group “Tissue Regeneration” of the German Society of Orthopaedic Surgery and Traumatology (DGOU). Z Orthop Unfall 151:38–47. https://doi.org/10.1055/s-0032-1328207 PubMed

Aurich M, Bedi HS, Smith PJ, Rolauffs B, Muckley T, Clayton J, Blackney M (2011) Arthroscopic treatment of osteochondral lesions of the ankle with matrix-associated chondrocyte implantation: Early clinical and magnetic resonance imaging results. Am J Sports Med 39:311–319. https://doi.org/10.1177/0363546510381575 CrossRefPubMed

Ochs BG, Muller-Horvat C, Albrecht D, Schewe B, Weise K, Aicher WK, Rolauffs B (2011) Remodeling of articular cartilage and subchondral bone after bone grafting and matrix-associated autologous chondrocyte implantation for osteochondritis dissecans of the knee. Am J Sports Med 39:764–773. https://doi.org/10.1177/0363546510388896 CrossRefPubMed

Ochs BG, Muller-Horvat C, Rolauffs B, Fritz J, Weise K, Schewe B (2007) Treatment of osteochondritis dissecans of the knee: One-step procedure with bone grafting and matrix-supported autologous chondrocyte transplantation. Z Orthop Unfall 145:146–151. https://doi.org/10.1055/s-2007-965167 CrossRefPubMed

Lin Z, Fitzgerald JB, Xu J, Willers C, Wood D, Grodzinsky AJ, Zheng MH (2008) Gene expression profiles of human chondrocytes during passaged monolayer cultivation. J Orthop Res 26:1230–1237. https://doi.org/10.1002/jor.20523 CrossRefPubMed

10.

Brittberg M, Winalski CS (2003) Evaluation of cartilage injuries and repair. J Bone Joint Surg Am 85-A(Suppl 2):58–69CrossRef

11.

Marlovits S, Zeller P, Singer P, Resinger C, Vecsei V (2006) Cartilage repair: Generations of autologous chondrocyte transplantation. Eur J Radiol 57:24–31. https://doi.org/10.1016/j.ejrad.2005.08.009 CrossRefPubMed

12.

Aurich M, Eger W, Rolauffs B, Margulis A, Kuettner KE, Mollenhauer JA, Cole AA (2006) Ankle chondrocytes are more resistant to interleukin-1 than chondrocytes derived from the knee. Orthopade 35:784–790. https://doi.org/10.1007/s00132-006-0958-2 CrossRefPubMed

13.

Aurich M, Squires GR, Reiner A, Mollenhauer JA, Kuettner KE, Poole AR, Cole AA (2005) Differential matrix degradation and turnover in early cartilage lesions of human knee and ankle joints. Arthritis Rheum 52:112–119CrossRefPubMed

14.

Eger W, Aurich M, Schumacher BL, Mollenhauer J, Kuettner KE, Cole AA (2003) Differences in metabolism of chondrocytes of the knee and ankle joint. Z Orthop Grenzgeb 141:18–20

15.

Aicher WK, Rolauffs B (2014) The spatial organisation of joint surface chondrocytes: Review of its potential roles in tissue functioning, disease and early, preclinical diagnosis of osteoarthritis. Ann Rheum Dis 73:645–653. https://doi.org/10.1136/annrheumdis-2013-204308 CrossRefPubMed

16.

Rolauffs B, Williams JM, Grodzinsky AJ, Kuettner KE, Cole AA (2008) Distinct horizontal patterns in the spatial organization of superficial zone chondrocytes of human joints. J Struct Biol 162:335–344. https://doi.org/10.1016/j.jsb.2008.01.010 CrossRefPubMedPubMedCentral

17.

Jackson DW, Simon TM (1996) Chondrocyte transplantation. Arthroscopy 12:732–738CrossRefPubMed

18.

Matricali GA, Dereymaeker GP, Luyten FP (2010) Donor site morbidity after articular cartilage repair procedures: A review. Acta Orthop Belg 76:669–674PubMed

19.

Hsieh-Bonassera ND, Wu I, Lin JK, Schumacher BL, Chen AC, Masuda K, Bugbee WD, Sah RL (2009) Expansion and redifferentiation of chondrocytes from osteoarthritic cartilage: Cells for human cartilage tissue engineering. Tissue Eng A 15:3513–3523. https://doi.org/10.1089/ten.TEA.2008.0628 CrossRef

20.

Takahashi N, Knudson CB, Thankamony S, Ariyoshi W, Mellor L, Im HJ, Knudson W (2010) Induction of CD44 cleavage in articular chondrocytes. Arthritis Rheum 62:1338–1348. https://doi.org/10.1002/art.27410 CrossRefPubMedPubMedCentral

21.

Kurtis MS, Schmidt TA, Bugbee WD, Loeser RF, Sah RL (2003) Integrin-mediated adhesion of human articular chondrocytes to cartilage. Arthritis Rheum 48:110–118. https://doi.org/10.1002/art.10704 CrossRefPubMed

22.

Gigout A, Jolicoeur M, Buschmann MD (2005) Low calcium levels in serum-free media maintain chondrocyte phenotype in monolayer culture and reduce chondrocyte aggregation in suspension culture. Osteoarthr Cartil 13:1012–1024. https://doi.org/10.1016/j.joca.2005.06.003 CrossRefPubMed

23.

Foldager CB, Gomoll AH, Lind M, Spector M (2012) Cell seeding densities in autologous chondrocyte implantation techniques for cartilage repair. Cartilage 3:108–117. https://doi.org/10.1177/1947603511435522 CrossRefPubMedPubMedCentral

24.

Kuettner KE, Pauli BU, Gall G, Memoli VA, Schenk RK (1982) Synthesis of cartilage matrix by mammalian chondrocytes in vitro. I. Isolation, culture characteristics, and morphology. J Cell Biol 93:743–750CrossRefPubMed

25.

Kuettner KE, Memoli VA, Pauli BU, Wrobel NC, Thonar EJ, Daniel JC (1982) Synthesis of cartilage matrix by mammalian chondrocytes in vitro. II. Maintenance of collagen and proteoglycan phenotype. J Cell Biol 93:751–757CrossRefPubMed

26.

Daniel JC, Pauli BU, Kuettner KE (1984) Synthesis of cartilage matrix by mammalian chondrocytes in vitro. III. Effects of ascorbate. J Cell Biol 99:1960–1969CrossRefPubMed

27.

Mandl EW, van der Veen SW, Verhaar JA, van Osch GJ (2004) Multiplication of human chondrocytes with low seeding densities accelerates cell yield without losing redifferentiation capacity. Tissue Eng 10:109–118. https://doi.org/10.1089/107632704322791754 CrossRefPubMed

28.

Gigante A, Bevilacqua C, Ricevuto A, Mattioli-Belmonte M, Greco F (2007) Membrane-seeded autologous chondrocytes: Cell viability and characterization at surgery. Knee Surg Sports Traumatol Arthrosc 15:88–92. https://doi.org/10.1007/s00167-006-0115-9 CrossRefPubMed

29.

Steinert AF, Ghivizzani SC, Rethwilm A, Tuan RS, Evans CH, Noth U (2007) Major biological obstacles for persistent cell-based regeneration of articular cartilage. Arthritis Res Ther 9:213. https://doi.org/10.1186/ar2195 CrossRefPubMedPubMedCentral

30.

Imabuchi R, Ohmiya Y, Kwon HJ, Onodera S, Kitamura N, Kurokawa T, Gong JP, Yasuda K (2011) Gene expression profile of the cartilage tissue spontaneously regenerated in vivo by using a novel double-network gel: Comparisons with the normal articular cartilage. BMC Musculoskelet Disord 12:213. https://doi.org/10.1186/1471-2474-12-213 CrossRefPubMedPubMedCentral

31.

Benya PD, Shaffer JD (1982) Dedifferentiated chondrocytes reexpress the differentiated collagen phenotype when cultured in agarose gels. Cell 30:215–224CrossRefPubMed

32.

Caron MM, Emans PJ, Coolsen MM, Voss L, Surtel DA, Cremers A, van Rhijn LW, Welting TJ (2012) Redifferentiation of dedifferentiated human articular chondrocytes: Comparison of 2D and 3D cultures. Osteoarthr Cartil 20:1170–1178. https://doi.org/10.1016/j.joca.2012.06.016 CrossRefPubMed

33.

Babur BK, Ghanavi P, Levett P, Lott WB, Klein T, Cooper-White JJ, Crawford R, Doran MR (2013) The interplay between chondrocyte redifferentiation pellet size and oxygen concentration. PLoS One 8:e58865. https://doi.org/10.1371/journal.pone.0058865 CrossRefPubMedPubMedCentral

34.

Meretoja VV, Dahlin RL, Wright S, Kasper FK, Mikos AG (2014) Articular chondrocyte redifferentiation in 3D co-cultures with mesenchymal stem cells. Tissue Eng C Methods 20:514–523. https://doi.org/10.1089/ten.tec.2013.0532 CrossRef

35.

Schuh E, Hofmann S, Stok K, Notbohm H, Muller R, Rotter N (2012) Chondrocyte redifferentiation in 3D: The effect of adhesion site density and substrate elasticity. J Biomed Mater Res A 100:38–47. https://doi.org/10.1002/jbm.a.33226 CrossRefPubMed

36.

Levett PA, Melchels FP, Schrobback K, Hutmacher DW, Malda J, Klein TJ (2014) Chondrocyte redifferentiation and construct mechanical property development in single-component photocrosslinkable hydrogels. J Biomed Mater Res A 102:2544–2553. https://doi.org/10.1002/jbm.a.34924 CrossRefPubMed

37.

Jimenez G, Lopez-Ruiz E, Kwiatkowski W, Montanez E, Arrebola F, Carrillo E, Gray PC, Izpisua Belmonte JC, Choe S, Peran M, Marchal JA (2015) Activin a/BMP2 chimera AB235 drives efficient redifferentiation of long term cultured autologous chondrocytes. Sci Rep 5:16400. https://doi.org/10.1038/srep16400 CrossRefPubMedPubMedCentral

Title: Tissue engineering-relevant characteristics of ex vivo and monolayer-expanded chondrocytes from the notch versus trochlea of human knee joints
Authors: Matthias Aurich
Gunther Olaf Hofmann
Bernd Rolauffs
Publication date: 01-11-2017
Publisher: Springer Berlin Heidelberg
Published in: International Orthopaedics / Issue 11/2017
Print ISSN: 0341-2695
Electronic ISSN: 1432-5195
DOI: https://doi.org/10.1007/s00264-017-3615-y

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Tissue engineering-relevant characteristics of ex vivo and monolayer-expanded chondrocytes from the notch versus trochlea of human knee joints

Abstract

Purpose

Methods

Results

Conclusions

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

Purpose

Methods

Results

Conclusions

Please log in to get access to this content

Other articles of this Issue 11/2017

Subtypes of endothelial progenitor cells affect healing of segmental bone defects differently

Evaluation of thirty eight cemented pegged glenoid components with variable backside curvature: two-year minimum follow-up

Optimal post-operative radiation after soft-tissue sarcoma resection is achieved in less than two thirds of cases

Improved joint-line restitution in unicompartmental knee arthroplasty using a robotic-assisted surgical technique

Transitioning to the direct anterior approach in total hip arthroplasty. Is it a true muscle sparing approach when performed by a low volume hip replacement surgeon?

A study of normal foot abduction across various age groups in children