Gene delivery to overcome astrocyte inhibition of axonal growth: An in vitro Model of the glial scar

Biotechnology and Bioengineering

Volumn 110, Issue 3, 2013, Pages 947-957

  Tuinstra, Hannah M ^a   Ducommun, Melissa M ^a   Briley, William E ^a   Shea, Lonnie D ^a,b,c  

^a Northwestern University   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

^c NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Astrocyte interface; Astrocyte neuron co culture; CSPG inhibition; Gene delivery

Indexed keywords

AXON GROWTH; AXONAL GROWTH; CENTRAL NERVOUS SYSTEMS; CHONDROITIN; CHONDROITIN POLYMERIZING FACTORS; CHONDROITIN SULFATE PROTEOGLYCANS; COCULTURE; EXTRACELLULAR MATRICES; GENE DELIVERY; GLIAL SCAR; IN-VITRO; INTERFACE MODEL; NEURITE GROWTH; NEURITES;

GENE TRANSFER; NEURONS; TISSUE;

ENZYME INHIBITION;

CHONDROITIN POLYMERIZING FACTOR; CHONDROITIN SYNTHASE 1; ENZYME; LENTIVIRUS VECTOR; PROTEOCHONDROITIN SULFATE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; ASTROCYTE; CELL ACTIVATION; CONTROLLED STUDY; DRUG DEGRADATION; DRUG SYNTHESIS; EMBRYO; GLIA SCAR; IN VITRO STUDY; NERVE CELL INHIBITION; NERVE FIBER GROWTH; NONHUMAN; RAT; RNA INTERFERENCE; SCAR; VIRAL GENE DELIVERY SYSTEM;

ANIMALS; ASTROCYTES; CELL LINE; CHONDROITIN SULFATE PROTEOGLYCANS; CHONDROITINASES AND CHONDROITIN LYASES; CICATRIX; GENE SILENCING; GENE TRANSFER TECHNIQUES; GENETIC VECTORS; LENTIVIRUS; MODELS, THEORETICAL; NEURONS; RATS; RNA, SMALL INTERFERING; TRANSDUCTION, GENETIC; TRANSFORMATION, GENETIC;

EID: 84872667552     PISSN: 00063592     EISSN: 10970290     Source Type: Journal    
DOI: 10.1002/bit.24750     Document Type: Article

References (52)

1. Asher RA, Morgenstern DA, Fidler PS, Adcock KH, Oohira A, Braistead JE, Levine JM, Margolis RU, Rogers JH, Fawcett JW. 2000. Neurocan is upregulated in injured brain and in cytokine-treated astrocytes. J Neurosci 20(7): 2427-2438.
2. Asher RA, Morgenstern DA, Moon LD, Fawcett JW. 2001. Chondroitin sulphate proteoglycans: Inhibitory components of the glial scar. Prog Brain Res 132: 611-619.
3. Asher RA, Morgenstern DA, Shearer MC, Adcock KH, Pesheva P, Fawcett JW. 2002. Versican is upregulated in CNS injury and is a product of oligodendrocyte lineage cells. J Neurosci 22(6): 2225-2236.
4. Avnur Z, Geiger B. 1984. Immunocytochemical localization of native chondroitin-sulfate in tissues and cultured cells using specific monoclonal antibody. Cell 38(3): 811-822.
5. Bandtlow CE, Zimmermann DR. 2000. Proteoglycans in the developing brain: New conceptual insights for old proteins. Physiol Rev 80(4): 1267-1290.
6. Barritt AW, Davies M, Marchand F, Hartley R, Grist J, Yip P, McMahon SB, Bradbury EJ. 2006. Chondroitinase ABC promotes sprouting of intact and injured spinal systems after spinal cord injury. J Neurosci 26(42): 10856-10867.
7. Bradbury EJ, Moon LD, Popat RJ, King VR, Bennett GS, Patel PN, Fawcett JW, McMahon SB. 2002. Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature 416(6881): 636-640.
8. Brummelkamp TR, Bernards R, Agami R. 2002. A system for stable expression of short interfering RNAs in mammalian cells. Science 296(5567): 550-553.
9. Chau CH, Shum DK, Li H, Pei J, Lui YY, Wirthlin L, Chan YS, Xu XM. 2004. Chondroitinase ABC enhances axonal regrowth through Schwann cell-seeded guidance channels after spinal cord injury. FASEB J 18(1): 194-196.
10. Davies SJ, Fitch MT, Memberg SP, Hall AK, Raisman G, Silver J. 1997. Regeneration of adult axons in white matter tracts of the central nervous system. Nature 390(6661): 680-683.
11. Davies SJ, Goucher DR, Doller C, Silver J. 1999. Robust regeneration of adult sensory axons in degenerating white matter of the adult rat spinal cord. J Neurosci 19(14): 5810-5822.
12. Dull T, Zufferey R, Kelly M, Mandel RJ, Nguyen M, Trono D, Naldini L. 1998. A third-generation lentivirus vector with a conditional packaging system. J Virol 72(11): 8463-8471.
13. East E, Golding JP, Phillips JB. 2009. A versatile 3D culture model facilitates monitoring of astrocytes undergoing reactive gliosis. J Tissue Eng Regen Med 3(8): 634-646.
14. Fidler PS, Schuette K, Asher RA, Dobbertin A, Thornton SR, Calle-Patino Y, Muir E, Levine JM, Geller HM, Rogers JH, Faissner A, Fawcett JW. 1999. Comparing astrocytic cell lines that are inhibitory or permissive for axon growth: The major axon-inhibitory proteoglycan is NG2. J Neurosci 19(20): 8778-8788.
15. Fok-Seang J, Smith-Thomas LC, Meiners S, Muir E, Du JS, Housden E, Johnson AR, Faissner A, Geller HM, Keynes RJ. et al. 1995. An analysis of astrocytic cell lines with different abilities to promote axon growth. Brain Res 689(2): 207-223.
16. Garcia-Alias G, Lin R, Akrimi SF, Story D, Bradbury EJ, Fawcett JW. 2008. Therapeutic time window for the application of chondroitinase ABC after spinal cord injury. Exp Neurol 210(2): 331-338.
17. Garcia-Alias G, Barkhuysen S, Buckle M, Fawcett JW. 2009. Chondroitinase ABC treatment opens a window of opportunity for task-specific rehabilitation. Nat Neurosci 12(9): 1145-1151.
18. Grimpe B, Silver J. 2004. A novel DNA enzyme reduces glycosaminoglycan chains in the glial scar and allows microtransplanted dorsal root ganglia axons to regenerate beyond lesions in the spinal cord. J Neurosci 24(6): 1393-1397.
19. Haas CA, Rauch U, Thon N, Merten T, Deller T. 1999. Entorhinal cortex lesion in adult rats induces the expression of the neuronal chondroitin sulfate proteoglycan neurocan in reactive astrocytes. J Neurosci 19(22): 9953-9963.
20. Houle JD, Tom VJ, Mayes D, Wagoner G, Phillips N, Silver J. 2006. Combining an autologous peripheral nervous system "bridge" and matrix modification by chondroitinase allows robust, functional regeneration beyond a hemisection lesion of the adult rat spinal cord. J Neurosci 26(28): 7405-7415.
21. Izumikawa T, Uyama T, Okuura Y, Sugahara K, Kitagawa H. 2007. Involvement of chondroitin sulfate synthase-3 (chondroitin synthase-2) in chondroitin polymerization through its interaction with chondroitin synthase-1 or chondroitin-polymerizing factor. Biochem J 403(3): 545-552.
22. Izumikawa T, Koike T, Shiozawa S, Sugahara K, Tamura J, Kitagawa H. 2008. Identification of chondroitin sulfate glucuronyltransferase as chondroitin synthase-3 involved in chondroitin polymerization: Chondroitin polymerization is achieved by multiple enzyme complexes consisting of chondroitin synthase family members. J Biol Chem 283(17): 11396-11406.
23. Jones LL, Tuszynski MH. 2001. Chronic intrathecal infusions after spinal cord injury cause scarring and compression. Microsc Res Tech 54(5): 317-324.
24. Jones LL, Yamaguchi Y, Stallcup WB, Tuszynski MH. 2002. NG2 is a major chondroitin sulfate proteoglycan produced after spinal cord injury and is expressed by macrophages and oligodendrocyte progenitors. J Neurosci 22(7): 2792-2803.
25. Jones LL, Margolis RU, Tuszynski MH. 2003. The chondroitin sulfate proteoglycans neurocan, brevican, phosphacan, and versican are differentially regulated following spinal cord injury. Exp Neurol 182(2): 399-411.
26. Kinnunen T, Raulo E, Nolo R, Maccarana M, Lindahl U, Rauvala H. 1996. Neurite outgrowth in brain neurons induced by heparin-binding growth-associated molecule (HB-GAM) depends on the specific interaction of HB-GAM with heparan sulfate at the cell surface. J Biol Chem 271(4): 2243-2248.
27. Kitagawa H, Uyama T, Sugahara K. 2001. Molecular cloning and expression of a human chondroitin synthase. J Biol Chem 276(42): 38721-38726.
28. Kitagawa H, Izumikawa T, Uyama T, Sugahara K. 2003. Molecular cloning of a chondroitin polymerizing factor that cooperates with chondroitin synthase for chondroitin polymerization. J Biol Chem 278(26): 23666-23671.
29. Laabs TL, Wang H, Katagiri Y, McCann T, Fawcett JW, Geller HM. 2007. Inhibiting glycosaminoglycan chain polymerization decreases the inhibitory activity of astrocyte-derived chondroitin sulfate proteoglycans. J Neurosci 27(52): 14494-14501.
30. Lemons ML, Sandy JD, Anderson DK, Howland DR. 2003. Intact aggrecan and chondroitin sulfate-depleted aggrecan core glycoprotein inhibit axon growth in the adult rat spinal cord. Exp Neurol 184(2): 981-990.
31. Li Y, Raisman G. 1995. Sprouts from cut corticospinal axons persist in the presence of astrocytic scarring in long-term lesions of the adult rat spinal cord. Exp Neurol 134(1): 102-111.
32. Lin R, Rosahl TW, Whiting PJ, Fawcett JW, Kwok JC. 2011. 6-Sulphated chondroitins have a positive influence on axonal regeneration. PLoS ONE 6(7): e21499.
33. McKeon RJ, Schreiber RC, Rudge JS, Silver J. 1991. Reduction of neurite outgrowth in a model of glial scarring following CNS injury is correlated with the expression of inhibitory molecules on reactive astrocytes. J Neurosci 11(11): 3398-3411.
34. McKeon RJ, Hoke A, Silver J. 1995. Injury-induced proteoglycans inhibit the potential for laminin-mediated axon growth on astrocytic scars. Exp Neurol 136(1): 32-43.
35. McKeon RJ, Jurynec MJ, Buck CR. 1999. The chondroitin sulfate proteoglycans neurocan and phosphacan are expressed by reactive astrocytes in the chronic CNS glial scar. J Neurosci 19(24): 10778-10788.
36. Moon LD, Asher RA, Rhodes KE, Fawcett JW. 2002. Relationship between sprouting axons, proteoglycans and glial cells following unilateral nigrostriatal axotomy in the adult rat. Neuroscience 109(1): 101-117.
37. Muir E, Du JS, Fok-Seang J, Smith-Thomas LC, Housden ES, Rogers J, Fawcett JW. 1998. Increased axon growth through astrocyte cell lines transfected with urokinase. Glia 23(1): 24-34.
38. Pfaffl MW. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29(9): e45.
39. Powell EM, Fawcett JW, Geller HM. 1997. Proteoglycans provide neurite guidance at an astrocyte boundary. Mol Cell Neurosci 10(1-2): 27-42.
40. Properzi F, Carulli D, Asher RA, Muir E, Camargo LM, van Kuppevelt TH, ten Dam GB, Furukawa Y, Mikami T, Sugahara K, et al. 2005. Chondroitin 6-sulphate synthesis is up-regulated in injured CNS, induced by injury-related cytokines and enhanced in axon-growth inhibitory glia. Eur J Neurosci 21(2): 378-390.
41. Rolls A, Shechter R, Schwartz M. 2009. The bright side of the glial scar in CNS repair. Nat Rev Neurosci 10(3): 235-241.
42. Sango K, Oohira A, Ajiki K, Tokashiki A, Horie M, Kawano H. 2003. Phosphacan and neurocan are repulsive substrata for adhesion and neurite extension of adult rat dorsal root ganglion neurons in vitro. Exp Neurol 182(1): 1-11.
43. Schwartz NB, Domowicz M. 2004. Proteoglycans in brain development. Glycoconj J 21(6): 329-341.
44. Silver J, Miller JH. 2004. Regeneration beyond the glial scar. Nat Rev Neurosci 5(2): 146-156.
45. Smith-Thomas LC, Fok-Seang J, Stevens J, Du JS, Muir E, Faissner A, Geller HM, Rogers JH, Fawcett JW. 1994. An inhibitor of neurite outgrowth produced by astrocytes. J Cell Sci 107(Pt 6): 1687-1695.
46. Snow DM, Lemmon V, Carrino DA, Caplan AI, Silver J. 1990. Sulfated proteoglycans in astroglial barriers inhibit neurite outgrowth in vitro. Exp Neurol 109(1): 111-130.
47. Stichel CC, Muller HW. 1998. The CNS lesion scar: New vistas on an old regeneration barrier. Cell Tissue Res 294(1): 1-9.
48. Tester NJ, Plaas AH, Howland DR. 2007. Effect of body temperature on chondroitinase ABC's ability to cleave chondroitin sulfate glycosaminoglycans. J Neurosci Res 85(5): 1110-1118.
49. Tom VJ, Steinmetz MP, Miller JH, Doller CM, Silver J. 2004. Studies on the development and behavior of the dystrophic growth cone, the hallmark of regeneration failure, in an in vitro model of the glial scar and after spinal cord injury. J Neurosci 24(29): 6531-6539.
50. Wang D, Ichiyama RM, Zhao R, Andrews MR, Fawcett JW. 2011. Chondroitinase combined with rehabilitation promotes recovery of forelimb function in rats with chronic spinal cord injury. J Neurosci 31(25): 9332-9344.
51. Yiu G, He Z. 2006. Glial inhibition of CNS axon regeneration. Nat Rev Neurosci 7(8): 617-627.
52. Yu X, Bellamkonda RV. 2001. Dorsal root ganglia neurite extension is inhibited by mechanical and chondroitin sulfate-rich interfaces. J Neurosci Res 66(2): 303-310.