Injectable laminin-functionalized hydrogel for nucleus pulposus regeneration

Biomaterials

Volumn 34, Issue 30, 2013, Pages 7381-7388

  Francisco, Aubrey T ^a   Mancino, Robert J ^a   Bowles, Robby D ^a   Brunger, Jonathan M ^a,b   Tainter, David M ^c   Chen, Yi Te ^b,d,e,f   Richardson, William J ^b   Guilak, Farshid ^a,b   Setton, Lori A ^a,b  

^a USA   (United States)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

^c DUKE NUS MEDICAL SCHOOL   (Singapore)

^d SHIN KONG WU HO SU MEMORIAL HOSPITAL   (Taiwan)

^e FU JEN CATHOLIC UNIVERSITY   (Taiwan)

^f NATIONAL YANG MING UNIVERSITY   (Taiwan)

Author keywords

Injectable; Intervertebral disc; Laminin; Nucleus pulposus; Organ culture; Polyethylene glycol

Indexed keywords

INJECTABLE; INTERVERTEBRAL DISCS; LAMININ; NUCLEUS PULPOSUS; ORGAN CULTURE;

BIOCHEMISTRY; BIOMATERIALS; CELLS; CYTOLOGY; GELATION; HYDROGELS; MECHANICAL PROPERTIES; POLYETHYLENE GLYCOLS;

BIOMECHANICS;

BIOMATERIAL; LAMININ 111; MACROGOL; RECOMBINANT PROTEIN; TREVIGEN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL ADHESION; CELL SURVIVAL; CONTROLLED STUDY; DRUG DELIVERY SYSTEM; GELATION; HYDROGEL; IN VITRO STUDY; IN VIVO STUDY; INTERVERTEBRAL DISK; LIQUID; MOLECULAR DYNAMICS; NERVE REGENERATION; NONHUMAN; NUCLEUS PULPOSUS; PHENOTYPE; PRIORITY JOURNAL; SHEAR STRENGTH; SUSPENSION;

INJECTABLE; INTERVERTEBRAL DISC; LAMININ; NUCLEUS PULPOSUS; ORGAN CULTURE; POLYETHYLENE GLYCOL;

ANIMALS; BIOCOMPATIBLE MATERIALS; CELLS, CULTURED; HUMANS; HYDROGEL; INJECTIONS; INTERVERTEBRAL DISC; LAMININ; LUCIFERASES; MECHANICAL PHENOMENA; POLYETHYLENE GLYCOLS; RATS; RATS, SPRAGUE-DAWLEY; REGENERATION; RHEOLOGY; SUS SCROFA;

EID: 84880508995     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2013.06.038     Document Type: Article

References (60)

1. Owens P.L., Woeltje M., Mutter R. Emergency department visits and inpatient stays related to back problems, 2008: statistical brief #105. Healthcare Cost and Utilization Project (HCUP) statistical briefs 2006, Rockville (MD).
2. Lyons G., Eisenstein S.M., Sweet M.B.E. Biochemical-changes in intervertebral-disk degeneration. Biochim Biophys Acta 1981, 673:443-453.
3. Walmsley R. The development and growth of the intervertebral disc. Edinb Med J 1953, 60:341-364.
4. Wolfe H.J., Putschar W.G., Vickery A.L. Role of the notochord in human intervetebral disk. I. Fetus and infant. Clin Orthop Relat Res 1965, 39:205-212.
5. Oegema T.R. The role of disc cell heterogeneity in determining disc biochemistry: a speculation. Biochem Soc Trans 2002, 30:839-844.
6. Hunter C.J., Matyas J.R., Duncan N.A. The notochordal cell in the nucleus pulposus: a review in the context of tissue engineering. Tissue Eng 2003, 9:667-677.
7. Risbud M.V., Schaer T.P., Shapiro I.M. Toward an understanding of the role of notochordal cells in the adult intervertebral disc: from discord to accord. Dev Dyn 2010, 239:2141-2148.
8. Sakai D. Future perspectives of cell-based therapy for intervertebral disc disease. Eur Spine J 2008, 17(Suppl.4):452-458.
9. Phillips F.M., Reuben J., Wetzel F.T. Intervertebral disc degeneration adjacent to a lumbar fusion. An experimental rabbit model. JBone Jt Surg Br 2002, 84:289-294.
10. Meisel H.J., Siodla V., Ganey T., Minkus Y., Hutton W.C., Alasevic O.J. Clinical experience in cell-based therapeutics: disc chondrocyte transplantation a treatment for degenerated or damaged intervertebral disc. Biomol Eng 2007, 24:5-21.
11. Crevensten G., Walsh A.J., Ananthakrishnan D., Page P., Wahba G.M., Lotz J.C., et al. Intervertebral disc cell therapy for regeneration: mesenchymal stem cell implantation in rat intervertebral discs. Ann Biomed Eng 2004, 32:430-434.
12. Sakai D., Mochida J., Yamamoto Y., Nomura T., Okuma M., Nishimura K., et al. Transplantation of mesenchymal stem cells embedded in atelocollagen gel to the intervertebral disc: a potential therapeutic model for disc degeneration. Biomaterials 2003, 24:3531-3541.
13. Gruber H.E., Johnson T.L., Leslie K., Ingram J.A., Martin D., Hoelscher G., et al. Autologous intervertebral disc cell implantation: a model using Psammomys obesus, the sand rat. Spine 2002, 27:1626-1633.
14. Ganey T., Libera J., Moos V., Alasevic O., Fritsch K.G., Meisel H.J., et al. Disc chondrocyte transplantation in a canine model: a treatment for degenerated or damaged intervertebral disc. Spine 2003, 28:2609-2620.
15. Sakai D., Mochida J., Iwashina T., Watanabe T., Nakai T., Ando K., et al. Differentiation of mesenchymal stem cells transplanted to a rabbit degenerative disc model: potential and limitations for stem cell therapy in disc regeneration. Spine 2005, 30:2379-2387.
16. Leckie S.K., Sowa G.A., Bechara B.P., Hartman R.A., Coelho J.P., Witt W.T., et al. Injection of human umbilical tissue-derived cells into the nucleus pulposus alters the course of intervertebral disc degeneration invivo. Spine J 2013, 13:263-272.
17. Bertram H., Kroeber M., Wang H., Unglaub F., Guehring T., Carstens C., et al. Matrix-assisted cell transfer for intervertebral disc cell therapy. Biochem Biophys Res Commun 2005, 331:1185-1192.
18. Omlor G.W., Bertram H., Kleinschmidt K., Fischer J., Brohm K., Guehring T., et al. Methods to monitor distribution and metabolic activity of mesenchymal stem cells following invivo injection into nucleotomized porcine intervertebral discs. Eur Spine J 2010, 19:601-612.
19. Saldanha K.J., Piper S.L., Ainslie K.M., Kim H.T., Majumdar S. Magnetic resonance imaging of iron oxide labelled stem cells: applications to tissue engineering based regeneration of the intervertebral disc. Eur Cell Mater 2008, 16:17-25.
20. Peroglio M., Grad S., Mortisen D., Sprecher C.M., Illien-Junger S., Alini M., et al. Injectable thermoreversible hyaluronan-based hydrogels for nucleus pulposus cell encapsulation. Eur Spine J 2012, 21(Suppl.6):S839-S849.
21. Revell P.A., Damien E., Di Silvio L., Gurav N., Longinotti C., Ambrosio L. Tissue engineered intervertebral disc repair in the pig using injectable polymers. JMater Sci Mater Med 2007, 18:303-308.
22. Sakai D., Mochida J., Iwashina T., Hiyama A., Omi H., Imai M., et al. Regenerative effects of transplanting mesenchymal stem cells embedded in atelocollagen to the degenerated intervertebral disc. Biomaterials 2006, 27:335-345.
23. Collin E.C., Grad S., Zeugolis D.I., Vinatier C.S., Clouet J.R., Guicheux J.J., et al. An injectable vehicle for nucleus pulposus cell-based therapy. Biomaterials 2011, 32:2862-2870.
24. Cheng Y.H., Yang S.H., Su W.Y., Chen Y.C., Yang K.C., Cheng W.T., et al. Thermosensitive chitosan-gelatin-glycerol phosphate hydrogels as a cell carrier for nucleus pulposus regeneration: an invitro study. Tissue Eng Part A 2010, 16:695-703.
25. Dang J.M., Sun D.D., Shin-Ya Y., Sieber A.N., Kostuik J.P., Leong K.W. Temperature-responsive hydroxybutyl chitosan for the culture of mesenchymal stem cells and intervertebral disk cells. Biomaterials 2006, 27:406-418.
26. Roughley P., Hoemann C., DesRosiers E., Mwale F., Antoniou J., Alini M. The potential of chitosan-based gels containing intervertebral disc cells for nucleus pulposus supplementation. Biomaterials 2006, 27:388-396.
27. Miner J.H., Yurchenco P.D. Laminin functions in tissue morphogenesis. Annu Rev Cell Dev Biol 2004, 20:255-284.
28. Ekblom P., Lonai P., Talts J.F. Expression and biological role of laminin-1. Matrix Biol 2003, 22:35-47.
29. Gilchrist C.L., Chen J., Richardson W.J., Loeser R.F., Setton L.A. Functional integrin subunits regulating cell-matrix interactions in the intervertebral disc. JOrthop Res 2007, 25:829-840.
30. Chen J., Jing L., Gilchrist C.L., Richardson W.J., Fitch R.D., Setton L.A. Expression of laminin isoforms, receptors, and binding proteins unique to nucleus pulposus cells of immature intervertebral disc. Connect Tissue Res 2009, 50:294-306.
31. Nettles D.L., Richardson W.J., Setton L.A. Integrin expression in cells of the intervertebral disc. JAnat 2004, 204:515-520.
32. Gilchrist C.L., Darling E.M., Chen J., Setton L.A. Extracellular matrix ligand and stiffness modulate immature nucleus pulposus cell-cell interactions. PloS One 2011, 6:e27170.
33. Gilchrist C.L., Francisco A.T., Plopper G.E., Chen J., Setton L.A. Nucleus pulposus cell-matrix interactions with laminins. Eur Cell Mater 2011, 21:523-532.
34. Drury J.L., Mooney D.J. Hydrogels for tissue engineering: scaffold design variables and applications. Biomaterials 2003, 24:4337-4351.
35. Zhu J. Bioactive modification of poly(ethylene glycol) hydrogels for tissue engineering. Biomaterials 2010, 31:4639-4656.
36. Dikovsky D., Bianco-Peled H., Seliktar D. Defining the role of matrix compliance and proteolysis in three-dimensional cell spreading and remodeling. Biophys J 2008, 94:2914-2925.
37. Peyton S.R., Kim P.D., Ghajar C.M., Seliktar D., Putnam A.J. The effects of matrix stiffness and RhoA on the phenotypic plasticity of smooth muscle cells in a 3-D biosynthetic hydrogel system. Biomaterials 2008, 29:2597-2607.
38. Marquardt L., Willits R.K. Neurite growth in PEG gels: effect of mechanical stiffness and laminin concentration. JBiomed Mater Res A 2011, 98:1-6.
39. Elbert D.L., Pratt A.B., Lutolf M.P., Halstenberg S., Hubbell J.A. Protein delivery from materials formed by self-selective conjugate addition reactions. JControl Release 2001, 76:11-25.
40. Pratt A.B., Weber F.E., Schmoekel H.G., Muller R., Hubbell J.A. Synthetic extracellular matrices for in situ tissue engineering. Biotechnol Bioeng 2004, 86:27-36.
41. Habeeb A.F. Chemical evaluation of conformational differences in native and chemically modified proteins. Biochim Biophys Acta 1966, 115:440-454.
42. Chen J., Baer A.E., Paik P.Y., Yan W., Setton L.A. Matrix protein gene expression in intervertebral disc cells subjected to altered osmolarity. Biochem Biophys Res Commun 2002, 293:932-938.
43. Salmon P., Trono D. Production and titration of lentiviral vectors. Curr Protoc Neurosci. 2006, Chapter 4:Unit 4.21.
44. Ferletta M., Kikkawa Y., Yu H., Talts J.F., Durbeej M., Sonnenberg A., et al. Opposing roles of integrin alpha6Abeta1 and dystroglycan in laminin-mediated extracellularsignal-regulated kinase activation. Mol Biol Cell 2003, 14:2088-2103.
45. Veronese F.M., Mero A. The impact of PEGylation on biological therapies. BioDrugs: Clin Immuno Biopharm Gene Ther 2008, 22:315-329.
46. Boyd L.M., Carter A.J. Injectable biomaterials and vertebral endplate treatment for repair and regeneration of the intervertebral disc. Eur Spine J 2006, 15(Suppl.3):S414-S421.
47. Iatridis J.C., Setton L.A., Weidenbaum M., Mow V.C. The viscoelastic behavior of the non-degenerate human lumbar nucleus pulposus in shear. JBiomech 1997, 30:1005-1013.
48. Iatridis J.C., Weidenbaum M., Setton L.A., Mow V.C. Is the nucleus pulposus a solid or a fluid? Mechanical behaviors of the nucleus pulposus of the human intervertebral disc. Spine 1996, 21:1174-1184.
49. Metters A., Hubbell J. Network formation and degradation behavior of hydrogels formed by Michael-type addition reactions. Biomacromolecules 2005, 6:290-301.
50. Nettles D.L., Haider M.A., Chilkoti A., Setton L.A. Neural network analysis identifies scaffold properties necessary for invitro chondrogenesis in elastin-like polypeptide biopolymer scaffolds. Tissue Eng Part A 2010, 16:11-20.
51. O'Halloran D.M., Pandit A.S. Tissue-engineering approach to regenerating the intervertebral disc. Tissue Eng 2007, 13:1927-1954.
52. Bowles R.D., Gebhard H.H., Hartl R., Bonassar L.J. Tissue-engineered intervertebral discs produce new matrix, maintain disc height, and restore biomechanical function to the rodent spine. Proc Natl Acad Sci U S A 2011, 108:13106-13111.
53. Nerurkar N.L., Elliott D.M., Mauck R.L. Mechanics of oriented electrospun nanofibrous scaffolds for annulus fibrosus tissue engineering. JOrthop Res 2007, 25:1018-1028.
54. Lutolf M., Hubbell J. Synthetic biomaterials as instructive extracellular microenvironments for morphogenesis in tissue engineering. Nat Biotechnol 2005, 23:47-55.
55. Chiba K., Andersson G.B., Masuda K., Thonar E.J. Metabolism of the extracellular matrix formed by intervertebral disc cells cultured in alginate. Spine 1997, 22:2885-2893.
56. Chou A.I., Nicoll S.B. Characterization of photocrosslinked alginate hydrogels for nucleus pulposus cell encapsulation. JBiomed Mater Res A 2009, 91:187-194.
57. Wang B., Wu Y., Shao Z., Yang S., Che B., Sun C., et al. Functionalized self-assembling peptide nanofiber hydrogel as a scaffold for rabbit nucleus pulposus cells. JBiomed Mater Res A 2012, 100:646-653.
58. Bron J.L., Helder M.N., Meisel H.J., Van Royen B.J., Smit T.H. Repair, regenerative and supportive therapies of the annulus fibrosus: achievements and challenges. Eur Spine J 2009, 18:301-313.
59. Leo B.M., Li X., Balian G., Anderson D.G. Invivo bioluminescent imaging of virus-mediated gene transfer and transduced cell transplantation in the intervertebral disc. Spine 2004, 29:838-844.
60. Troy T., Jekic-McMullen D., Sambucetti L., Rice B. Quantitative comparison of the sensitivity of detection of fluorescent and bioluminescent reporters in animal models. Mol Imaging 2004, 3:9-23.