Differences in cartilage-forming capacity of expanded human chondrocytes from ear and nose and their gene expression profiles

Cell Transplantation

Volumn 20, Issue 6, 2011, Pages 925-940

  Hellingman, Catharine A ^a   Verwiel, Eugène T P ^b   Slagt, Inez ^a   Koevoet, Wendy ^a   Poublon, René M L ^a   Nolst Trenité, Gilbert J ^c   de Jong, Robert J Baatenburg ^a   Jahr, Holger ^a   van Osch, Gerjo J V M ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

^b RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^c ACADEMIC MEDICAL CENTER   (Netherlands)

Author keywords

Cartilage; Chondrocytes; Chondrogenesis; Collagen X; Mineralization; Tissue engineering

Indexed keywords

ACTIVIN RECEPTOR LIKE KINASE 1; AGGRECANASE 2; BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN 5; COLLAGEN TYPE 10; COLLAGEN TYPE 2; COLLAGENASE 3; FIBROBLAST GROWTH FACTOR RECEPTOR 3;

ADOLESCENT; ADULT; AGED; ARTICLE; CARTILAGE CELL; CHILD; CONTROLLED STUDY; DNA MICROARRAY; EAR CARTILAGE; EXTRACELLULAR MATRIX; GENE EXPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; NOSE CARTILAGE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SCHOOL CHILD;

ADAM PROTEINS; ADOLESCENT; ADULT; AGED; BONE MORPHOGENETIC PROTEIN 5; CARTILAGE, ARTICULAR; CHILD; CHILD, PRESCHOOL; CHONDROCYTES; CHONDROGENESIS; COLLAGEN TYPE X; EAR CARTILAGE; GENE EXPRESSION PROFILING; HUMANS; INSULIN-LIKE GROWTH FACTOR I; MATRIX METALLOPROTEINASE 13; MIDDLE AGED; NASAL SEPTUM; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; TISSUE ENGINEERING;

EID: 80051779918     PISSN: 09636897     EISSN: None     Source Type: Journal    
DOI: 10.3727/096368910X539119     Document Type: Article

References (46)

1. Asawa Y.; Ogasawara T.; Takahashi T.; Yamaoka H.; Nishizawa S.; Matsudaira K.; Mori Y.; Takato T.; Hoshi K. Aptitude of auricular and nasoseptal chondrocytes cultured under a monolayer or three-dimensional condition for cartilage tissue engineering. Tissue Eng. Part A 15:1109-1118; 2009.
2. Brittberg M.; Lindahl A.; Nilsson A.; Ohlsson C.; Isaksson O.; Peterson L. Treatment of deep cartilage defects in the knee with autologous chondrocyte transplantation. N. Engl. J. Med. 331:889-895; 1994.
3. Byers B. A.; Mauck R. L.; Chiang I. E.; Tuan R. S. Transient exposure to transforming growth factor beta 3 under serum-free conditions enhances the biomechanical and biochemical maturation of tissue-engineered cartilage. Tissue Eng. Part A 14:1821-1834; 2008.
4. Chung C.; Erickson I. E.; Mauck R. L.; Burdick J. A. Differential behavior of auricular and articular chondrocytes in hyaluronic acid hydrogels. Tissue Eng. Part A 14:1121-1131; 2008.
5. Cui J. H.; Park S. R.; Park K.; Choi B. H.; Min B. H. Preconditioning of mesenchymal stem cells with low-intensity ultrasound for cartilage formation in vivo. Tissue Eng. 13:351-360; 2007.
6. Das R. H.; Jahr H.; Verhaar J. A.; van der Linden J. C.; van Osch G. J.; Weinans H. In vitro expansion affects the response of chondrocytes to mechanical stimulation. Osteoarthritis Cartilage 16:385-391; 2008.
7. De Chalain T.; Phillips J. H.; Hinek A. Bioengineering of elastic cartilage with aggregated porcine and human auricular chondrocytes and hydrogels containing alginate, collagen, and kappa-elastin. J. Biomed. Mater. Res. 44:280-288; 1999.
8. Dell'Accio F.; De Bari C.; Luyten F. P. Molecular markers predictive of the capacity of expanded human articular chondrocytes to form stable cartilage in vivo. Arthritis Rheum. 44:1608-1619; 2001.
9. Duynstee M. L.; Verwoerd-Verhoef H. L.; Verwoerd C. D.; Van Osch G. J. The dual role of perichondrium in cartilage wound healing. Plast. Reconstr. Surg. 110:1073-1079; 2002.
10. Farndale R. W.; Buttle D. J.; Barrett A. J. Improved quantitation and discrimination of sulphated glycosaminoglycans by use of dimethylmethylene blue. Biochem. Biophys. Acta 883:173-177; 1986.
11. Farrell E.; van der Jagt O. P.; Koevoet W.; Kops N.; van Maanen C. J.; Hellingman C. A.; Jahr H.; O'Brien F. J.; Verhaar J. A. N.; Weinans H.; van Osch G. J. V. M. Chondrogenic priming of human bone marrow stromal cells: A better route to bone repair? Tissue Eng. Part C Methods 15:285-295; 2009.
12. Grogan S. P.; Barbero A.; Diaz-Romero J.; Cleton- Jansen A. M.; Soeder S.; Whiteside R.; Hogendoorn P. C.; Farhadi J.; Aigner T.; Martin I.; Mainil-Varlet P. Identification of markers to characterize and sort human articular chondrocytes with enhanced in vitro chondrogenic capacity. Arthritis Rheum. 56:586-595; 2007.
13. Hellingman C. A.; Koevoet W.; Kops N.; Farrell E.; Jahr H.; Liu W.; Baatenburg de Jong R. J.; Frenz D.; van Osch G. J. Fibroblast Growth Factor Receptors in in-vitro and in-vivo chondrogenesis: Relating tissue engineering using adult mesenchymal stem cells to embryonic development. Tissue Eng. Part A 16:545-556; 2009.
14. Henderson J. H.; Welter J. F.; Mansour J. M.; Niyibizi C.; Caplan A. I.; Dennis J. E. Cartilage tissue engineering for laryngotracheal reconstruction: Comparison of chondrocytes from three anatomic locations in the rabbit. Tissue Eng. 13:843-853; 2007.
15. Hierck B. P.; Iperen L. V.; Gittenberger-de Groot A. C.; Poelmann R. E. Modified indirect immuno detection allows study of murine tissue with mouse monoclonal antibodies. J. Histochem. Cytochem. 42:1499-1502; 1994.
16. Huang D. W.; Sherman B. T.; Lempicki R. A. Systematic and integrative analysis of large gene lists using DAVID Bioinformatics Resources. Nat. Protoc. 4:44-57; 2009.
17. Ichinose S.; Yamagata K.; Sekiya I.; Muneta T.; Tagami M. Detailed examination of cartilage formation and endochondral ossification using human mesenchymal stem cells. Clin. Exp. Pharmacol. Physiol. 32:561-570; 2005.
18. Isogai N.; Kusuhara H.; Ikada Y.; Ohtani H.; Jacquet R.; Hillyer J.; Lowder E.; Landis W. J. Comparison of different chondrocytes for use in tissue engineering of cartilage model structures. Tissue Eng. 12:691-703, 2006.
19. Jakob M.; Démarteau O.; Schäfer D.; Hintermann B.; Dick W.; Heberer M.; Martin I. Specific growth factors during the expansion and redifferentiation of adult human articular chondrocytes enhance chondrogenesis and cartilaginous tissue formation in vitro. J. Cell. Biochem. 81:368-377; 2001.
20. Jenniskens Y. M.; Koevoet W.; de Bart A. C.; Weinans H.; Jahr H.; Verhaar J. A.; DeGroot J.; van Osch G. J. Biochemical and functional modulation of the cartilage collagen network by IGF1, TGFbeta2 and FGF2. Osteoarthritis Cartilage 14:1136-1146; 2006.
21. Lee K. A.; Pierce R. A.; Mecham R. P.; Parks W. C. Increased mesenchymal cell density accompanies induction of tropoelastin expression in developing elastic tissue. Dev. Dyn. 200:53-67; 1994.
22. Litvak K. J.; Schmittgen T. D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta c(T)) Method. Methods 25:402-408; 2001.
23. Macchiarini P.; Jungebluth P.; Go T.; Asnaghi M. A.; Rees L. E.; Cogan T. A.; Dodson A.; Martorell J.; Bellini S.; Parnigotto P. P.; Dickinson S. C.; Hollander A. P.; Mantero S.; Conconi M. T.; Birchall M. A. Clinical transplantation of a tissue-engineered airway. Lancet 372:2023-2030; 2008.
24. Mailhot G.; Yang M.; Mason-Savas A.; Mackay C. A.; Leav I.; Odgren P. R. BMP-5 expression increases during chondrocyte differentiation in vivo and in vitro and promotes proliferation and cartilage matrix synthesis in primary chondrocyte cultures. J. Cell. Physiol. 214:56-64; 2008.
25. Marijnissen W. J.; van Osch G. J.; Aigner J.; van der Veen S. W.; Hollander A. P.; Verwoerd-Verhoef H. L.; Verhaar J. A. Alginate as a chondrocyte-delivery substance in combination with a non-woven scaffold for cartilage tissue engineering. Biomaterials 23:1511-1517; 2002.
26. Markway B. D.; Tan G. K.; Brooke G.; Hudson J. E.; Cooper-White J. J.; Doran M. R. Enhanced chondrogenic differentiation of human bone marrow-derived mesenchymal stem cells in low oxygen environment micropellet cultures. Cell Transplant. 19:29-42; 2010.
27. Mueller M. B.; Tuan R. S. Functional characterization of hypertrophy in chondrogenesis of human mesenchymal stem cells. Arthritis Rheum. 58:1377-1388; 2008.
28. Murdoch A. D.; Grady L. M.; Ablett M. P.; Katopodi T.; Meadows R. S.; Hardingham T. E. Chondrogenic differentiation of human bone marrow stem cells in transwell cultures: Generation of scaffold-free cartilage. Stem Cells 25:2786-2796; 2007.
29. Naumann A.; Dennis J. E.; Aigner J.; Coticchia J.; Arnold J.; Berghaus A.; Kastenbauer E. R.; Caplan A. I. Tissue engineering of autologous cartilage grafts in three-dimensional in vitro macroaggregate culture system. Tissue Eng. 10:1695-1706; 2004.
30. Panossian A.; Ashiku S.; Kirchhoff C. H.; Randolph M. A.; Yaremchuk M. J. Effects of cell concentration and growth period on articular and ear chondrocyte transplants for tissue engineering. Plast. Reconstr. Surg. 108:392-402; 2001.
31. Park S. S.; Jin H. R.; Chi D. H.; Taylor R. S. Characteristics of tissue-engineered cartilage from human auricular chondrocytes. Biomaterials 25:2363-2369; 2004.
32. Pavlov M. I.; Sautier J. M.; Oboeuf M.; Asselin A.; Berdal A. Chondrogenic differentiation during midfacial development in the mouse: In vivo and in vitro studies. Biol. Cell 95:75-86; 2003.
33. Pelttari K.; Winter A.; Steck E.; Goetzke K.; Hennig T.; Ochs B. G.; Aigner T.; Richter W. Premature induction of hypertrophy during in vitro chondrogenesis of human mesenchymal stem cells correlates with calcification and vascular invasion after ectopic transplantation in SCID mice. Arthritis Rheum. 54:3254-3266; 2006.
34. Rotter N.; Haisch A.; Bücheler M. Cartilage and bone tissue engineering for reconstructive head and neck surgery. Eur. Arch. Otorhinolaryngol. 262:539-545; 2005.
35. Saris D. B.; Vanlauwe J.; Victor J.; Haspl M.; Bohnsack M.; Fortems Y.; Vandekerckhove B.; Almqvist K. F.; Claes T.; Handelberg F.; Lagae K.; van der Bauwhede J.; Vandenneucker H.; Yang K. G.; Jelic M.; Verdonk R.; Veulemans N.; Bellemans J.; Luyten F. P. Characterized chondrocyte implantation results in better structural repair when treating symptomatic cartilage defects of the knee in a randomized controlled trial versus microfracture. Am. J. Sports Med. 36:235-246; 2008.
36. Skoog T.; Ohlsén L.; Sohn S. A. Perichondrial potential for cartilagenous regeneration. Scand. J. Plast. Reconstr. Surg. 6:123-125; 1972.
37. Takahashi T.; Ogasawara T.; Kishimoto J.; Liu G.; Asato H.; Nakatsuka T.; Uchinuma E.; Nakamura K.; Kawaguchi H.; Chung U. I.; Takato T.; Hoshi K. Synergistic effects of FGF-2 with insulin or IGF-I on the proliferation of human auricular chondrocytes. Cell Transplant. 14:683-693; 2005.
38. Tay A. G.; Farhadi J.; Suetterlin R.; Pierer G.; Heberer M.; Martin I. Cell yield, proliferation, and postexpansion differentiation capacity of human ear, nasal, and rib chondrocytes. Tissue Eng. 10:762-770; 2004.
39. Togo T.; Utani A.; Naitoh M.; Ohta M.; Tsuji Y.; Morikawa N.; Nakamura M.; Suzuki S. Identification of cartilage progenitor cells in the adult ear perichondrium: Utilization for cartilage reconstruction. Lab. Invest. 86:445-457; 2006.
40. Van Osch G. J.; Brittberg M.; Dennis J. E.; Bastiaansen-Jenniskens Y. M.; Erben R. G.; Konttinen Y. T.; Luyten F. P. Cartilage repair: Past and future-lessons for regenerative medicine. J. Cell. Mol. Med. 13:792-810; 2009.
41. Van Osch G. J.; Mandl E. W.; Jahr H.; Koevoet W.; Nolst-Trenit G.; Verhaar J. A. Considerations on the use of ear chondrocytes as donor chondrocytes for cartilage tissue engineering. Biorheology 41:411-421; 2004.
42. Van Osch G. J.; Van Der Veen S. W.; Burger E. H.; Verwoerd-Verhoef H. L. Chondrogenic potential of in vitro multiplied rabbit perichondrium cells cultured in alginate beads in defined medium. Tissue Eng. 6:321-330; 2000.
43. Weidenbecher M.; Tucker H. M.; Awadallah A.; Dennis J. E. Fabrication of a neotrachea using engineered cartilage. Laryngoscope 118:593-598; 2008.
44. Xu J. W.; Zaporojan V.; Peretti G. M.; Roses R. E.; Morse K. B.; Roy A. K.; Mesa J. M.; Randolph M. A.; Bonassar L. J.; Yaremchuk M. J. Injectable tissue-engineered cartilage with different chondrocyte sources. Plast. Reconstr. Surg. 113:1361-1371; 2004.
45. Yanaga H.; Imai K.; Fujimoto T.; Yanaga K. Generating ears from cultured autologous auricular chondrocytes by using two-stage implantation in treatment of microtia. Plast. Reconstr. Surg. 124:817-825; 2009.
46. Yanaga H.; Yanaga K.; Imai K.; Koga M.; Soejima C.; Ohmori K. Clinical application of cultured autologous human auricular chondrocytes with autologous serum for craniofacial or nasal augmentation and repair. Plast. Reconstr. Surg. 117:2019-2030; 2006.