Peripheral nerve morphogenesis induced by scaffold micropatterning

Biomaterials

Volumn 35, Issue 13, 2014, Pages 4035-4045

  Cerri, Federica ^a   Salvatore, Luca ^b   Memon, Danish ^c   Martinelli Boneschi, Filippo ^a   Madaghiele, Marta ^b   Brambilla, Paola ^a   Del Carro, Ubaldo ^a   Taveggia, Carla ^a   Riva, Nilo ^a   Trimarco, Amelia ^a   Lopez, Ignazio D ^a   Comi, Giancarlo ^a   Pluchino, Stefano ^c   Martino, Gianvito ^a   Sannino, Alessandro ^b   Quattrini, Angelo ^a  

^a SAN RAFFAELE HOSPITAL   (Italy)

^b UNIVERSITY OF SALENTO   (Italy)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Biomaterials; Medical device; Nerve regeneration; Peripheral nervous system

Indexed keywords

BIOMATERIALS; COLLAGEN; GENE EXPRESSION; MICROSTRUCTURE; MOLECULAR BIOLOGY; NEURONS;

BIOLOGICAL PATHWAYS; GENE EXPRESSION ANALYSIS; GENOME WIDE ANALYSIS; MEDICAL DEVICES; MOLECULAR MECHANISM; NERVE REGENERATION; PERIPHERAL NERVOUS SYSTEM; SEQUENTIAL REGULATION;

SCAFFOLDS (BIOLOGY);

BETA1 INTEGRIN; COLLAGEN; GLIAL FIBRILLARY ACIDIC PROTEIN; LAMININ; LAMININ ALPHA2; LAMININ BETA1; NEU DIFFERENTIATION FACTOR; TISSUE SCAFFOLD; UNCLASSIFIED DRUG; BIOMATERIAL;

ADULT; ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BASEMENT MEMBRANE; CELL DIFFERENTIATION; CELL INTERACTION; CELL MIGRATION; CONTROLLED STUDY; DOWN REGULATION; FEMALE; GENE CONTROL; GENE EXPRESSION; HISTOPATHOLOGY; IN VIVO STUDY; MICROENVIRONMENT; MORPHOGENESIS; MOTOR PERFORMANCE; MYELINATED NERVE; MYELINATION; NERVE CONDUCTION; NERVE CRUSH; NERVE FIBER; NERVE REGENERATION; NERVE TRANSECTION; NEUROPHYSIOLOGY; NONHUMAN; PERIPHERAL NERVE; PERIPHERAL NERVE MORPHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; RAT; REAL TIME POLYMERASE CHAIN REACTION; RELATIVE DENSITY; RNA EXTRACTION; SCHWANN CELL; SCIATIC NERVE; ANIMAL; BIOENGINEERING; CHEMISTRY; CYTOLOGY; METABOLISM; PERIPHERAL NERVOUS SYSTEM; PHYSIOLOGY; PROCEDURES; SPRAGUE DAWLEY RAT; TISSUE SCAFFOLD;

RATTUS;

ANIMALS; BIOCOMPATIBLE MATERIALS; BIOENGINEERING; FEMALE; NERVE REGENERATION; PERIPHERAL NERVOUS SYSTEM; RATS; RATS, SPRAGUE-DAWLEY; TISSUE SCAFFOLDS;

EID: 84896738035     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2014.01.069     Document Type: Article

References (60)

1. Schröder J.M. Altered ratio between axon diameter and myelin sheath thickness in regenerated nerve fibers. Brain Res 1972, 45:49-65.
2. Place E.S., Evans N.D., Stevens M.M. Complexity in biomaterials for tissue engineering. Nat Mater 2009, 28:457-470.
3. Evans P.J. The peripheral nerve allograft: a decade of advancement. Atlas Hand Clin 2005, 10:187-197.
4. Yannas I.V. Emerging rules for inducing organ regeneration. Biomaterials 2013, 34:321-330.
5. Deumens R., Bozkurt A., Meek M.F., Marcus M.A., Joosten E.A., Weis J., et al. Repairing injured peripheral nerves: bridging the gap. Prog Neurobiol 2010, 92:245-276.
6. Chamberlain L.J., Yannas I.V., Hsu H.P., Spector M. Connective tissue response to tubular implants for peripheral nerve regeneration: the role of myofibroblasts. JComp Neurol 2000, 417:415-430.
7. Soller E.C., Tzeranis D.S., Miu K., So P.T.C., Yannas I.V. Common features of optimal collagen scaffolds that disrupt wound contraction and enhance regeneration both in peripheral nerves and in skin. Biomaterials 2012, 33:4738-4791.
8. Yannas I.V. Tissue and organ regeneration in adults 2001, Springer, New York.
9. Moore M.J., Friedman J.A., Lewellyn E.B., Mantila S.M., Krych A.J., Ameenuddin S., et al. Multiple-channel scaffolds to promote spinal cord axon regeneration. Biomaterials 2006, 27:419-429.
10. Stokols S., Tuszynski M.H. Freeze-dried agarose scaffolds with uniaxial channels stimulate and guide linear axonal growth following spinal cord injury. Biomaterials 2006, 27:443-451.
11. Harley B.A., Spilker M.H., Wu J.W., Asano K., Hsu H.-P., Spector M., et al. Optimal degradation rate for collagen chambers used for regeneration of peripheral nerves over long gaps. Cells Tissues Organs 2004, 176(1-3):153-165.
12. Oh S.H., Lee J.H. Fabrication and characterization of hydrophilized porous PLGA nerve guide conduits by a modified immersion precipitation method. JBiomed Mater Res 2007, 80:530-538.
13. Jeffries E.M., Wang Y. Biomimetic micropatterned multi-channel nerve guides by templated electrospinning. Biotechnol Bioeng 2012, 109:1571-1582.
14. Meek M.F., Den Dunnen W.F. Porosity of the wall of a Neurolac nerve conduit hampers nerve regeneration. Microsurgery 2009, 29:473-478.
15. Harley B.A., Hastings A.Z., Yannas I.V., Sannino A. Fabricating tubular scaffolds with a radial pore size gradient by a spinning technique. Biomaterials 2006, 27:866-874.
16. Quattrini A., Previtali S., Feltri M.L., Canal N., Nemni R., Wrabetz L. Beta 4 integrin and other Schwann cell markers in axonal neuropathy. Glia 1996, 17:294-306.
17. Stoll G., Muller H.W. Nerve injury, axonal de generation and neural regeneration: basic insights. Brain Pathol 1999, 9:313-325.
18. Triolo D., Dina G., Lorenzetti I., Malaguti M., Morana P., Del Carro U., et al. Loss of glial fibrillary acidic protein (GFAP) impairs Schwann cell proliferation and delays nerve regeneration after damage. JCell Sci 2006, 119:3981-3993.
19. La Marca R., Cerri F., Horiuchi K., Bachi A., Feltri M.L., Wrabetz L., et al. TACE (ADAM17) inhibits Schwann cell myelination. Nat Neurosci 2011, 14:857-865.
20. Du P., Kibbe W.A., Lin S.M. Lumi: a pipeline for processing Illumina microarray. Bioinformatics 2008, 24:1547-1548.
21. Wettenhall J.M., Smyth G.K. LimmaGUI: a graphical user interface for linear modeling of microarray data. Bioinformatics 2004, 20:3705-3706.
22. Dennis G., Sherman B.T., Hosack D.A., Yang J., Gao W., Lane H.C., et al. DAVID: database for annotation, visualization, and integrated discovery. Genome biol 2003, 4:P3.
23. Huang da W., Sherman B.T., Lempicki R.A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 2009, 4:44-57.
24. Ashburner M., Ball C.A., Blake J.A., Botstein D., Butler H., Cherry J.M., et al. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 2000, 25:25-29.
25. Prifti E., Zucker J.D., Clement K., Henegar C. FunNet: an integrative tool for exploring transcriptional interactions. Bioinformatics 2008, 24:2636-2638.
26. Piechota M., Korostynski M., Solecki W., Gieryk A., Slezak M., Bilecki W., et al. The dissection of transcriptional modules regulated by various drugs of abuse in the mouse striatum. Genome Biol 2010, 11:R48.
27. Sondell M., Lundborg G., Kanje M. Vascular endothelial growth factor has neurotrophic activity and stimulates axonal outgrowth, enhancing cell survival and Schwann cell proliferation in the peripheral nervous system. JNeurosci 1999, 19:5731-5740.
28. Parrinello S., Napoli I., Ribeiro S., Wingfield Digby P., Fedorova M., Parkinson D.B., et al. EphB signaling directs peripheral nerve regeneration through Sox2-dependent Schwann cell sorting. Cell 2010, 143:145-155.
29. Doyu M., Sobue G., Ken E., Kimata K., Shinomura T., Mitsuma T., et al. Laminin A, B1, and B2 chain gene expression in transected and regenerating nerves: regulation by axonal signals. JNeurochem 1993, 60:543-551.
30. Nodari A. Beta1 integrin activates Rac1 in Schwann cells to generate radial lamellae during axonal sorting and myelination. JCell Biol 2007, 177:1063-1075.
31. Feltri M.L., Scherer S.S., Nemni R., Kamholz J., Vogelbacker H., Scott M.O., et al. Beta 4 integrin expression in myelinating Schwann cells is polarized, developmentally regulated and axonally dependent. Development 1994, 120:1287-1301.
32. Parmantier E., Lynn B., Lowson D., Turmaine M., Namini S.S., Chakrabarti L., et al. Schwann cell-derived Desert hedgehog controls the development of peripheral nerve sheaths. Neuron 1999, 23:713-724.
33. Michailov G.V., Sereda M.W., Brinkmann B.G., Fischer T.M., Haug B., Birchmeir C., et al. Axonal neuregulin-1 regulates myelin sheath thickness. Science 2004, 304:700-703.
34. Taveggia C., Zanazzi G., Petrylak A., Yano H., Rosenbluth J., Einheber S., et al. Neuregulin-1 type III determines the ensheathment fate of axons. Neuron 2005, 47:681-694.
35. Greenfield S., Brostoff A., Eylar E.H., Morell P. Protein composition of myelin of the peripheral nervous system. JNeurochem 1973, 20:1207-1216.
36. LeBlanc A.C., Poduslo J.F. Axonal modulation of myelin gene expression in the peripheral nerve. JNeurosci Res 1990, 26:317-326.
37. Nishino J., Yamashita K., Hashiguchi H., Fujii H., Shimazaki T., Hamada H. Meteorin: a secreted protein that regulates glial cell differentiation and promotes axonal extension. EMBO J 2004, 23:1998-2008.
38. Eshed Y. Gliomedin mediates Schwann cell-axon interaction and the molecular assembly of the Nodes of Ranvier. Neuron 2005, 47:215-229.
39. Zhelyaznik N., Mey J. Regulation of retinoic acid receptors alpha, beta and retinoid X receptor alpha after sciatic nerve injury. Neuroscience 2006, 141:1761-1774.
40. Tawk M., Makoukji J., Belle M., Fonte C., Trousson A., Hawkins T., et al. Wnt/B-Catenin signaling is an essential and direct driver of myelin gene expression and myelinogenesis. JNeurosci 2011, 31:3729-3742.
41. Bosse F., Hasenpusch-Theil K., Kury P., Muller H.W. Gene expression profiling reveals that peripheral nerve regeneration is a consequence of both novel injury-dependent and reactivated developmental processes. JNeurochem 2006, 96:441-1457.
42. Einheber S., Hannocks M.J., Metz C.N., Rifkin D.B., Salzer J.L. Transforming growth factor-beta 1 regulates axon/Schwann cell interactions. JCell Biol 1995, 129:443-458.
43. Podratz J.L., Rodriguez E., Windebank A.J. Role of the extracellular matrix in myelination of peripheral nerve. Glia 2001, 35:35-40.
44. Scherer S.S. The biology and pathobiology of Schwann cells. Curr Opin Neurol 1997, 10:386-397.
45. Svaren J., Meijer D. The molecular machinery of myelin gene transcription in Schwann cells. Glia 2008, 56:1541-1551.
46. Fricker F.R., Lago N., Balarajah S., Tsantoulas C., Tanna S., Zhu N., et al. Axonally derived neuregulin-1 is required for remyelination and regeneration after nerve injury in adulthood. JNeurosci 2011, 31:3225-3233.
47. Atanasoski S., Scherer S.S., Sirkowski E., Leone D., Garratt A.N., Birchmeier C., et al. ErbB2 signaling in Schwann cells is mostly dispensable for maintenance of myelinated peripheral nerves and proliferation of adult Schwann cells after injury. JNeurosci 2006, 26:2124-2131.
48. Umehara F., Tate G., Itoh K., Osame M. Minifascicular neuropathy: a new concept of the human disease caused by desert hedgehog gene mutation. Cell Mol Biol 2002, 48:187-189.
49. Chen D., Zhao M., Mundy G.R. Bone morphogenetic proteins. Growth Factors 2004, 22:233-241.
50. Charon F., Tessier-Lavigne M. Novel brain wiring functions for classical morphogens: a role as graded positional cues in axon guidance. Development 2005, 132:2251-2262.
51. Feng X.H., Derynck R. Specificity and versatility in tgf-beta signaling through Smads. Annu Rev Cell Dev Biol 2005, 21:659-693.
52. Parkinson D.B., Dong Z., Bunting H., Whitfield J., Meier C., Marie H., et al. Transforming growth factor beta (TGFbeta ) mediates Schwann cell death invitro and invivo: examination of c-Jun activation, interactions with survival signals, and the relationship of TGF-beta mediated death to Schwann cell differentiation. JNeurosci 2001, 21:8572-8585.
53. D'Antonio M., Droggiti A., Feltri M.L., Roes J., Wrabetz L., Mirsky R., et al. TGFbeta type II receptor signaling controls Schwann cell death and proliferation in developing nerves. JNeurosci 2006, 26:8417-8427.
54. Goodrich L., Scott M. Hedgehog and patched in neural development and disease. Neuron 1998, 21:1243-1257.
55. Ciani L., Salinas P.C. WNTs in the vertebrate nervous system: from pattering to neuronal connectivity. Nat Rev Neurosci 2005, 6:351-362.
56. Cheyette B.N., Waxman J.S., Miller J.R., Takemaru K., Sheldahl L.C., Khlebtsova N., et al. Dapper, a Dishevelled-associated antagonist of beta-catenin and JNK signaling, is required for notochord formation. Dev Cell 2002, 2:449-461.
57. Lee H.J., Finkelstein D., Li X., Wu D., Shi D.L., Zheng J.J. Identification of transmembrane protein 88 (TMEM88) as a dishevelled-binding protein. JBiol Chem 2010, 285:41549-41556.
58. Bänziger C., Soldini D., Schütt C., Zipperlen P., Hausmann G., Basler K. Wntless, a conserved membrane protein dedicated to the secretion of Wnt proteins from signaling cells. Cell 2006, 125:509-522.
59. Bartscherer K., Pelte N., Ingelfinger D., Boutros M. Secretion of Wnt ligands requires Evi, a conserved transmembrane protein. cell 2006, 125:523-533.
60. Grigoryan T., Stein S., Qi J., Wende H., Garratt A.N., Nave K.A., et al. Wnt/Rspondin/β-catenin signals control axonal sorting and lineage progression in Schwann cell development. Proc Natl Acad Sci USA 2013, 110(45):18174-18179.