The effect of long-term release of Shh from implanted biodegradable microspheres on recovery from spinal cord injury in mice

Biomaterials

Volumn 33, Issue 10, 2012, Pages 2892-2901

  Lowry, Natalia ^a,b   Goderie, Susan K ^a   Lederman, Patricia ^a   Charniga, Carol ^a   Gooch, Michael R ^b   Gracey, Kristina D ^b   Banerjee, Akhilesh ^c   Punyani, Supriya ^c   Silver, Jerry ^d   Kane, Ravi S ^c   Stern, Jeffrey H ^a   Temple, Sally ^a,b  

^a Neural Stem Cell Institute   (United States)

^b ALBANY MEDICAL COLLEGE   (United States)

^c RENSSELAER POLYTECHNIC INSTITUTE   (United States)

^d CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Biodegradable microspheres; Mouse; Shh; Spinal cord injury

Indexed keywords

AXON GUIDANCES; CELL ACTIVATION; CONTROLLED DELIVERY; CORTICOSPINAL; ENVIRONMENTAL FACTORS; MOTOR NEURONS; MOUSE; MOUSE MODELS; MULTIPLE PROCESS; OLIGODENDROCYTES; PROGENITOR CELL; SCAR FORMATION; SHH; SPINAL CORD INJURY; SPINAL CORDS; THERAPEUTIC INTERVENTION;

DOSIMETRY; MAMMALS; MICROSPHERES; MOLECULAR BIOLOGY; NEURONS; PATIENT REHABILITATION; TISSUE;

STEM CELLS;

MICROSPHERE; SONIC HEDGEHOG PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BIODEGRADABLE IMPLANT; CELL PROLIFERATION; CONTROLLED STUDY; CONTUSION; FEMALE; MOTOR PERFORMANCE; MOUSE; NERVE SPROUTING; NONHUMAN; OLIGODENDROGLIA; OUTCOME ASSESSMENT; PRIORITY JOURNAL; PYRAMIDAL TRACT; SCAR FORMATION; SPINAL CORD INJURY; TREATMENT RESPONSE;

ANIMALS; ASTROCYTES; BIODEGRADATION, ENVIRONMENTAL; CELL PROLIFERATION; DELAYED-ACTION PREPARATIONS; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION; HEDGEHOG PROTEINS; IMPLANTS, EXPERIMENTAL; LACTIC ACID; MICE; MICE, INBRED C57BL; MICROSPHERES; POLYGLYCOLIC ACID; RECOVERY OF FUNCTION; SPINAL CORD INJURIES; STEM CELLS;

MUS;

EID: 84856239336     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2011.12.048     Document Type: Article

References (47)

1. Park E., Velumian A.A., Fehlings M.G. The role of excitotoxicity in secondary mechanisms of spinal cord injury: a review with an emphasis on the implications for white matter degeneration. JNeurotrauma 2004, 21:754-774.
2. Busch S.A., Silver J. The role of extracellular matrix in CNS regeneration. Curr Opin Neurobiol 2007, 17:120-127.
3. Harel N.Y., Strittmatter S.M. Can regenerating axons recapitulate developmental guidance during recovery from spinal cord injury?. Nat Rev Neurosci 2006, 7:603-616.
4. Lu P., Tuszynski M.H. Growth factors and combinatorial therapies for CNS regeneration. Exp Neurol 2008, 209:313-320.
5. James N.D., Bartus K., Grist J., Bennett D.L., McMahon S.B., Bradbury E.J. Conduction failure following spinal cord injury: functional and anatomical changes from acute to chronic stages. JNeurosci 2011, 31:18543-18555.
6. Horner P.J., Power A.E., Kempermann G., Kuhn H.G., Palmer T.D., Winkler J., et al. Proliferation and differentiation of progenitor cells throughout the intact adult rat spinal cord. JNeurosci 2000, 20:2218-2228.
7. Lowry N., Goderie S.K., Adamo M., Lederman P., Charniga C., Gill J., et al. Multipotent embryonic spinal cord stem cells expanded by endothelial factors and Shh/RA promote functional recovery after spinal cord injury. Exp Neurol 2008, 209:510-522.
8. Jessell T.M. Neuronal specification in the spinal cord: inductive signals and transcriptional codes. Nat Rev Genet 2000, 1:20-29.
9. Sussman C.R., Davies J.E., Miller R.H. Extracellular and intracellular regulation of oligodendrocyte development: roles of Sonic hedgehog and expression of E proteins. Glia 2002, 40:55-64.
10. Tekki-Kessaris N., Woodruff R., Hall A.C., Gaffield W., Kimura S., Stiles C.D., et al. Hedgehog-dependent oligodendrocyte lineage specification in the telencephalon. Development 2001, 128:2545-2554.
11. Agius E., Soukkarieh C., Danesin C., Kan P., Takebayashi H., Soula C., et al. Converse control of oligodendrocyte and astrocyte lineage development by Sonic hedgehog in the chick spinal cord. Dev Biol 2004, 270:308-321.
12. Charron F., Stein E., Jeong J., McMahon A.P., Tessier-Lavigne M. The morphogen sonic hedgehog is an axonal chemoattractant that collaborates with netrin-1 in midline axon guidance. Cell 2003, 113:11-23.
13. So P.L., Yip P.K., Bunting S., Wong L.F., Mazarakis N.D., Hall S., et al. Interactions between retinoic acid, nerve growth factor and sonic hedgehog signalling pathways in neurite outgrowth. Dev Biol 2006, 298:167-175.
14. Akazawa C., Tsuzuki H., Nakamura Y., Sasaki Y., Ohsaki K., Nakamura S., et al. Theupregulated expression of sonic hedgehog in motor neurons after rat facial nerve axotomy. JNeurosci 2004, 24:7923-7930.
15. Bambakidis N.C., Miller R.H. Transplantation of oligodendrocyte precursors and sonic hedgehog results in improved function and white matter sparing in the spinal cords of adult rats after contusion. Spine J 2004, 4:16-26.
16. Shi L., Caulfield M.J., Chern R.T., Wilson R.A., Sanyal G., Volkin D.B. Pharmaceutical and immunological evaluation of a single-shot hepatitis B vaccine formulated with PLGA microspheres. JPharm Sci 2002, 91:1019-1035.
17. Qian X., Davis A.A., Goderie S.K., Temple S. FGF2 concentration regulates the generation of neurons and glia from multipotent cortical stem cells. Neuron 1997, 18:81-93.
18. Li S., Kim J.E., Budel S., Hampton T.G., Strittmatter S.M. Transgenic inhibition of Nogo-66 receptor function allows axonal sprouting and improved locomotion after spinal injury. Mol Cell Neurosci 2005, 29:26-39.
19. Hashimoto M., Sun D., Rittling S.R., Denhardt D.T., Young W. Osteopontin-deficient mice exhibit less inflammation, greater tissue damage, and impaired locomotor recovery from spinal cord injury compared with wild-type controls. JNeurosci 2007, 27:3603-3611.
20. Basso D.M., Fisher L.C., Anderson A.J., Jakeman L.B., McTigue D.M., Popovich P.G. Basso Mouse Scale for locomotion detects differences in recovery after spinal cord injury in five common mouse strains. JNeurotrauma 2006, 23:635-659.
21. Smith R.R., Burke D.A., Baldini A.D., Shum-Siu A., Baltzley R., Bunger M., et al. TheLouisville Swim Scale: a novel assessment of hindlimb function following spinal cord injury in adult rats. JNeurotrauma 2006, 23:1654-1670.
22. Wang X., Baughman K.W., Basso D.M., Strittmatter S.M. Delayed Nogo receptor therapy improves recovery from spinal cord contusion. Ann Neurol 2006, 60:540-549.
23. Galvin K.E., Ye H., Wetmore C. Differential gene induction by genetic and ligand-mediated activation of the Sonic hedgehog pathway in neural stem cells. Dev Biol 2007, 308:331-342.
24. Li S., Liu B.P., Budel S., Li M., Ji B., Walus L., et al. Blockade of Nogo-66, myelin-associated glycoprotein, and oligodendrocyte myelin glycoprotein by soluble Nogo-66 receptor promotes axonal sprouting and recovery after spinal injury. JNeurosci 2004, 24:10511-11020.
25. Palma V., Lim D.A., Dahmane N., Sánchez P., Brionne T.C., Herzberg C.D., et al. Sonic hedgehog controls stem cell behavior in the postnatal and adult brain. Development 2005, 132:335-344.
26. Ahn S., Joyner A.L. Invivo analysis of quiescent adult neural stem cells responding to Sonic hedgehog. Nature 2005, 437:894-897.
27. Talac R., Friedman J.A., Moore M.J., Lu L., Jabbari E., Windebank A.J., et al. Animal models of spinal cord injury for evaluation of tissue engineering treatment strategies. Biomaterials 2004, 25:1505-1510.
28. Belachew S., Chittajallu R., Aguirre A.A., Yuan X., Kirby M., Anderson S., et al. Postnatal NG2 proteoglycan-expressing progenitor cells are intrinsically multipotent and generate functional neurons. JCell Biol 2003, 161:169-186.
29. Busch S.A., Horn K.P., Cuascut F.X., Hawthorne A.L., Bai L., Miller R.H., et al. Adult NG2+ cells are permissive to neurite outgrowth and stabilize sensory axons during macrophage-induced axonal dieback after spinal cord injury. Neurosci 2010, 30:255-265.
30. Goodrich L.V., Milenković L., Higgins K.M., Scott M.P. Altered neural cell fates and medulloblastoma in mouse patched mutants. Science 1997, 277:1109-1113.
31. Zai L.J., Wrathall J.R. Cell proliferation and replacement following contusive spinal cord injury. Glia 2005, 50:247-257.
32. Zhu X., Hill R.A., Dietrich D., Komitova M., Suzuki R., Nishiyama A. Age-dependent fate and lineage restriction of single NG2 cells. Development 2011, 138:745-753.
33. Lytle J.M., Chittajallu R., Wrathall J.R., Gallo V. NG2 cell response in the CNP-EGFP mouse after contusive spinal cord injury. Glia 2009, 57:270-285.
34. Sellers D.L., Maris D.O., Horner P.J. Postinjury niches induce temporal shifts in progenitor fates to direct lesion repair after spinal cord injury. JNeurosci 2009, 29:6722-6733.
35. Yang Z., Suzuki R., Daniels S.B., Brunquell C.B., Sala C.J., Nishiyama A. NG2 glial cells provide a favorable substrate for growing axons. JNeurosci 2006, 26:3829-3839.
36. Fuccillo M., Joyner A.L., Fishell G. Morphogen to mitogen: the multiple roles of hedgehog signalling in vertebrate neural development. Nat Rev Neurosci 2006, 7:772-783.
37. Bai C.B., Joyner A.L. Gli1 can rescue the invivo function of Gli2. Development 2001, 128:5161-5172.
38. Pan Y., Bai C.B., Joyner A.L., Wang B. Sonic hedgehog signaling regulates Gli2 transcriptional activity by suppressing its processing and degradation. Mol Cell Biol 2006, 26:3365-3377.
39. Litingtung Y., Chiang C. Specification of ventral neuron types is mediated by an antagonistic interaction between Shh and Gli3. Nat Neurosci 2000, 3:979-985.
40. Bai C.B., Stephen D., Joyner A.L. All mouse ventral spinal cord patterning by hedgehog is Gli dependent and involves an activator function of Gli3. Dev Cell 2004, 6:103-115.
41. Hayhurst M., McConnell S.K. Mouse models of holoprosencephaly. Curr Opin Neurol 2003, 16:135-141.
42. Hu B.Y., Du Z.W., Li X.J., Ayala M., Zhang S.C. Human oligodendrocytes from embryonic stem cells: conserved SHH signaling networks and divergent FGF effects. Development 2009, 136:1443-1452.
43. Reimer M.M., Kuscha V., Wyatt C., Sörensen I., Frank R.E., Knüwer M., et al. Sonic hedgehog is a polarized signal for motor neuron regeneration in adult zebrafish. JNeurosci 2009, 29:15073-15082.
44. Ratan R.R., Noble M. Novel multi-modal strategies to promote brain and spinal cord injury recovery. Stroke 2009, 40:S130-S132.
45. Jin Y., Neuhuber B., Singh A., Bouyer J., Lepore A., Bonner J., et al. Transplantation of human glial restricted progenitors and derived astrocytes into a contusion model of spinal cord injury. JNeurotrauma 2011, 28:579-594.
46. Chang Y.W., Goff L.A., Li H., Kane-Goldsmith N., Tzatzalos E., Hart R.P., et al. Rapid induction of genes associated with tissue protection and neural development in contused adult spinal cord after radial glial cell transplantation. JNeurotrauma 2009, 26:979-993.
47. Kwon B.K., Sekhon L.H., Fehlings M.G. Emerging repair, regeneration, and translational research advances for spinal cord injury. Spine 2010, 35(21S):S263-S270.