The promotion of osteochondral repair by combined intra-articular injection of parathyroid hormone-related protein and implantation of a bi-layer collagen-silk scaffold

Biomaterials

Volumn 34, Issue 25, 2013, Pages 6046-6057

  Zhang, Wei ^a,b   Chen, Jialin ^a,b   Tao, Jiadong ^a,b   Hu, Changchang ^a,b   Chen, Longkun ^c   Zhao, Hongshi ^a,b   Xu, Guowei ^a,b   Heng, Boon C ^d   Ouyang, Hong Wei ^a,b  

^a ZHEJIANG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b Zhejiang Provincial Key Laboratory of Tissue Engineering and Regenerative Medicine   (China)

^c Zhejiang Xingyue Biotechnology Co Ltd   (China)

^d ETH ZURICH   (Switzerland)

Author keywords

Cartilage tissue engineering; Chondrocyte terminal differentiation; Chondrogenesis; Collagen silk scaffold; Osteochondral defects; PTHrP

Indexed keywords

CARTILAGE TISSUE ENGINEERING; CHONDROGENESIS; OSTEOCHONDRAL DEFECTS; PTHRP; TERMINAL DIFFERENTIATION;

CARTILAGE; COLLAGEN; DEFECTS; JOINTS (ANATOMY); REPAIR; SCAFFOLDS (BIOLOGY); STEM CELLS; VEHICLE ROUTING;

TISSUE;

AGGRECANASE 2; BETA CATENIN; COLLAGEN; COLLAGEN SILK SCAFFOLD; COLLAGENASE 3; FRIZZLED PROTEIN; LYMPHOID ENHANCER FACTOR 1; PARATHYROID HORMONE RELATED PROTEIN; PROTEIN C JUN; TISSUE SCAFFOLD; TRANSCRIPTION FACTOR 7; UNCLASSIFIED DRUG; WNT PROTEIN;

ADULT; AGED; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ARTICULAR CARTILAGE; BIOCOMPATIBILITY; BONE REMODELING; CARTILAGE CELL; CELL SHAPE; CHONDROGENESIS; COMPARATIVE STUDY; CONTROLLED STUDY; HUMAN; HUMAN TISSUE; HYALINE CARTILAGE; HYPERTROPHY; IMMUNOBLOTTING; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; IMPLANTATION; IN VITRO STUDY; INTRACELLULAR SIGNALING; KNEE; NONHUMAN; OSSIFICATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RABBIT; REAL TIME POLYMERASE CHAIN REACTION; TISSUE ENGINEERING; TISSUE REGENERATION; TISSUE REPAIR; TREATMENT OUTCOME; WESTERN BLOTTING;

AGED; ANIMALS; CARTILAGE, ARTICULAR; CELLS, CULTURED; CHONDROCYTES; CHONDROGENESIS; COLLAGEN; HUMANS; MIDDLE AGED; PARATHYROID HORMONE-RELATED PROTEIN; RABBITS; SILK; TISSUE ENGINEERING; TISSUE SCAFFOLDS;

ORYCTOLAGUS CUNICULUS;

EID: 84878612658     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2013.04.055     Document Type: Article

References (49)

1. McNickle A.G., Provencher M.T., Cole B.J. Overview of existing cartilage repair technology. Sports Med Arthrosc 2008, 16:196-201.
2. Temenoff J.S., Mikos A.G. Review: tissue engineering for regeneration of articular cartilage. Biomaterials 2000, 21:431-440.
3. Ahmed T.A., Hincke M.T. Strategies for articular cartilage lesion repair and functional restoration. Tissue Eng Part B Rev 2010, 16:305-329.
4. Nukavarapu S.P., Dorcemus D.L. Osteochondral tissue engineering: current strategies and challenges. Biotechnol Adv 2012, Available from URL:. http://www.ncbi.nlm.nih.gov/pubmed/23174560, 10.1016/j.biotechadv.2012.11.004.
5. Gelse K., Klinger P., Koch M., Surmann-Schmitt C., von der Mark K., Swoboda B., et al. Thrombospondin-1 prevents excessive ossification in cartilage repair tissue induced by osteogenic protein-1. Tissue Eng Part A 2011, 17:2101-2112.
6. Ochi M., Uchio Y., Kawasaki K., Wakitani S., Iwasa J. Transplantation of cartilage-like tissue made by tissue engineering in the treatment of cartilage defects of the knee. JBone Jt Surg Br 2002, 84:571-578.
7. Henderson I.J., La Valette D.P. Subchondral bone overgrowth in the presence of full-thickness cartilage defects in the knee. Knee 2005, 12:435-440.
8. Shapiro F., Koide S., Glimcher M.J. Cell origin and differentiation in the repair of full-thickness defects of articular cartilage. JBone Jt Surg Am 1993, 75:532-553.
9. Hunziker E.B. Articular cartilage repair: basic science and clinical progress. A review of the current status and prospects. Osteoarthritis Cartilage 2002, 10:432-463.
10. Csaki C., Schneider P.R., Shakibaei M. Mesenchymal stem cells as a potential pool for cartilage tissue engineering. Ann Anat 2008, 190:395-412.
11. Gelse K., Beyer C., Welsch G., Blanke M. Endochondral ossification in cartilage repair tissue hampers bone marrow stimulating techniques. Rheumatology 2012, S3:002.
12. Zhang W., Chen J., Zhang S., Ouyang H.W. Inhibitory function of parathyroid hormone-related protein on chondrocyte hypertrophy: the implication for articular cartilage repair. Arthritis Res Ther 2012, 14:221.
13. Gelse K., Ekici A.B., Cipa F., Swoboda B., Carl H.D., Olk A., et al. Molecular differentiation between osteophytic and articular cartilage-clues for a transient and permanent chondrocyte phenotype. Osteoarthritis Cartilage 2012, 20:162-171.
14. Bhumiratana S., Grayson W.L., Castaneda A., Rockwood D.N., Gil E.S., Kaplan D.L., et al. Nucleation and growth of mineralized bone matrix on silk-hydroxyapatite composite scaffolds. Biomaterials 2011, 32:2812-2820.
15. Hutmacher D.W. Scaffolds in tissue engineering bone and cartilage. Biomaterials 2000, 21:2529-2543.
16. Li C., Vepari C., Jin H.J., Kim H.J., Kaplan D.L. Electrospun silk-BMP-2 scaffolds for bone tissue engineering. Biomaterials 2006, 27:3115-3124.
17. Qi Y.Y., Chen X., Jiang Y.Z., Cai H.X., Wang L.L., Song X.H., et al. Local delivery of autologous platelet in collagen matrix simulated in situ articular cartilage repair. Cell Transplant 2009, 18:1161-1169.
18. Mithoefer K., Williams R.R., Warren R.F., Potter H.G., Spock C.R., Jones E.C., et al. The microfracture technique for the treatment of articular cartilage lesions in the knee. A prospective cohort study. JBone Jt Surg Am 2005, 87:1911-1920.
19. Brown W.E., Potter H.G., Marx R.G., Wickiewicz T.L., Warren R.F. Magnetic resonance imaging appearance of cartilage repair in the knee. Clin Orthop Relat Res 2004, 422:214-223.
20. Cole B.J., Farr J., Winalski C.S., Hosea T., Richmond J., Mandelbaum B., et al. Outcomes after a single-stage procedure for cell-based cartilage repair: a prospective clinical safety trial with 2-year follow-up. Am J Sports Med 2011, 39:1170-1179.
21. Weir E.C., Philbrick W.M., Amling M., Neff L.A., Baron R., Broadus A.E. Targeted overexpression of parathyroid hormone-related peptide in chondrocytes causes chondrodysplasia and delayed endochondral bone formation. Proc Natl Acad Sci U S A 1996, 93:10240-10245.
22. Schipani E., Lanske B., Hunzelman J., Luz A., Kovacs C.S., Lee K., et al. Targeted expression of constitutively active receptors for parathyroid hormone and parathyroid hormone-related peptide delays endochondral bone formation and rescues mice that lack parathyroid hormone-related peptide. Proc Natl Acad Sci U S A 1997, 94:13689-13694.
23. Karaplis A.C., Luz A., Glowacki J., Bronson R.T., Tybulewicz V.L., Kronenberg H.M., et al. Lethal skeletal dysplasia from targeted disruption of the parathyroid hormone-related peptide gene. Genes Dev 1994, 8:277-289.
24. Amizuka N., Warshawsky H., Henderson J.E., Goltzman D., Karaplis A.C. Parathyroid hormone-related peptide-depleted mice show abnormal epiphyseal cartilage development and altered endochondral bone formation. JCell Biol 1994, 126:1611-1623.
25. Vortkamp A., Lee K., Lanske B., Segre G.V., Kronenberg H.M., Tabin C.J. Regulation of rate of cartilage differentiation by Indian hedgehog and PTH-related protein. Science 1996, 273:613-622.
26. Chen X., Macica C.M., Nasiri A., Broadus A.E. Regulation of articular chondrocyte proliferation and differentiation by Indian hedgehog and parathyroid hormone-related protein in mice. Arthritis Rheum 2008, 58:3788-3797.
27. Macica C, Liang G, Nasiri A, Broadus AE. Genetic evidence of the regulatory role of parathyroid hormone-related protein in articular chondrocyte maintenance in an experimental mouse model. Arthritis Rheum 63: 3333-43.
28. Sampson E.R., Hilton M.J., Tian Y., Chen D., Schwarz E.M., Mooney R.A., et al. Teriparatide as a chondroregenerative therapy for injury-induced osteoarthritis. Sci Transl Med 2011, 3:101ra93.
29. Fischer J., Dickhut A., Rickert M., Richter W. Human articular chondrocytes secrete parathyroid hormone-related protein and inhibit hypertrophy of mesenchymal stem cells in coculture during chondrogenesis. Arthritis Rheum 2010, 62:2696-2706.
30. Weiss S., Hennig T., Bock R., Steck E., Richter W. Impact of growth factors and PTHrP on early and late chondrogenic differentiation of human mesenchymal stem cells. JCell Physiol 2010, 223:84-93.
31. Jiang J., Leong N.L., Mung J.C., Hidaka C., Lu H.H. Interaction between zonalpopulations of articular chondrocytes suppresses chondrocyte mineralization and this process is mediated by PTHrP. Osteoarthritis Cartilage 2008, 16:70-82.
32. Chang J.K., Chang L.H., Hung S.H., Wu S.C., Lee H.Y., Lin Y.S., et al. Parathyroid hormone 1-34 inhibits terminal differentiation of human articular chondrocytes and osteoarthritis progression in rats. Arthritis Rheum 2009, 60:3049-3060.
33. Mizuta H., Kudo S., Nakamura E., Takagi K., Hiraki Y. Expression of the PTH/PTHrP receptor in chondrogenic cells during the repair of full-thickness defects of articular cartilage. Osteoarthritis Cartilage 2006, 14:944-952.
34. Kudo S., Mizuta H., Otsuka Y., Takagi K., Hiraki Y. Inhibition of chondrogenesis by parathyroid hormone invivo during repair of full-thickness defects of articular cartilage. JBone Miner Res 2000, 15:253-260.
35. Yin Z., Chen X., Chen J.L., Shen W.L., Hieu N.T., Gao L., et al. The regulation of tendon stem cell differentiation by the alignment of nanofibers. Biomaterials 2010, 31:2163-2175.
36. Chen J.L., Yin Z., Shen W.L., Chen X., Heng B.C., Zou X.H., et al. Efficacy of hESC-MSCs in knitted silk-collagen scaffold for tendon tissue engineering and their roles. Biomaterials 2010, 31:9438-9451.
37. Eastwood S.L., Harrison P.J. Synaptic pathology in the anterior cingulate cortex in schizophrenia and mood disorders. A review and a Western blot study of synaptophysin, GAP-43 and the complexins. Brain Res Bull 2001, 55:569-578.
38. Pieper J.S., Oosterhof A., Dijkstra P.J., Veerkamp J.H., van Kuppevelt T.H. Preparation and characterization of porous crosslinked collagenous matrices containing bioavailable chondroitin sulphate. Biomaterials 1999, 20:847-858.
39. van den Borne M.P., Raijmakers N.J., Vanlauwe J., Victor J., de Jong S.N., Bellemans J., et al. International Cartilage Repair Society (ICRS) and Oswestry macroscopic cartilage evaluation scores validated for use in Autologous Chondrocyte Implantation (ACI) and microfracture. Osteoarthritis Cartilage 2007, 15:1397-1402.
40. Guo X., Park H., Young S., Kretlow J.D., van den Beucken J.J., Baggett L.S., et al. Repair of osteochondral defects with biodegradable hydrogel composites encapsulating marrow mesenchymal stem cells in a rabbit model. Acta Biomater 2010, 6:39-47.
41. O'Driscoll S.W., Keeley F.W., Salter R.B. Durability of regenerated articular cartilage produced by free autogenous periosteal grafts in major full-thickness defects in joint surfaces under the influence of continuous passive motion. A follow-up report at one year. JBone Jt Surg Am 1988, 70:595-606.
42. Lanske B., Karaplis A.C., Lee K., Luz A., Vortkamp A., Pirro A., et al. PTH/PTHrP receptor in early development and Indian hedgehog-regulated bone growth. Science 1996, 273:663-666.
43. Pioszak A.A., Parker N.R., Gardella T.J., Xu H.E. Structural basis for parathyroid hormone-related protein binding to the parathyroid hormone receptor and design of conformation-selective peptides. JBiol Chem 2009, 284:28382-28391.
44. Dong Y.F., Soung D.Y., Schwarz E.M., O'Keefe R.J., Drissi H. Wnt induction of chondrocyte hypertrophy through the Runx2 transcription factor. JCell Physiol 2006, 208:77-86.
45. Zhu M., Tang D., Wu Q., Hao S., Chen M., Xie C., et al. Activation of beta-catenin signaling in articular chondrocytes leads to osteoarthritis-like phenotype inadult beta-catenin conditional activation mice. JBone Miner Res 2009, 24:12-21.
46. Kulkarni N.H., Halladay D.L., Miles R.R., Gilbert L.M., Frolik C.A., Galvin R.J., et al. Effects of parathyroid hormone on Wnt signaling pathway in bone. JCell Biochem 2005, 95:1178-1190.
47. Kakar S., Einhorn T.A., Vora S., Miara L.J., Hon G., Wigner N.A., et al. Enhanced chondrogenesis and Wnt signaling in PTH-treated fractures. JBone Miner Res 2007, 22:1903-1912.
48. Lietman S.A., Miyamoto S., Brown P.R., Inoue N., Reddi A.H. The temporal sequence of spontaneous repair of osteochondral defects in the knees of rabbits is dependent on the geometry of the defect. JBone Jt Surg Br 2002, 84:600-606.
49. Kudo S., Mizuta H., Takagi K., Hiraki Y. Cartilaginous repair of full-thickness articular cartilage defects is induced by the intermittent activation of PTH/PTHrP signaling. Osteoarthritis Cartilage 2011, 19:886-894.