Deoxyribozyme-mediated knockdown of xylosyltransferase-1 mRNA promotes axon growth in the adult rat spinal cord

Brain

Volumn 131, Issue 10, 2008, Pages 2596-2605

  Hurtado, Andres ^a,b   Podinin, Heidrun ^b,c   Oudega, Martin ^a,b   Grimpe, Barbara ^b,c,d  

^a KENNEDY KRIEGER INSTITUTE   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF MIAMI   (United States)

Author keywords

Brevican; DNA enzyme; Neurocan; Scar; XT

Indexed keywords

BREVICAN; CHONDROITIN SULFATE; DEOXYRIBOZYME; HEPARAN SULFATE; MESSENGER RNA; NEUROCAN; PROTEOGLYCAN; TRANSFERASE; UNCLASSIFIED DRUG; XYLOSYLTRANSFERASE I;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FEMALE; GLYCOSYLATION; NERVE FIBER GROWTH; NERVE GRAFT; NONHUMAN; PRIORITY JOURNAL; RAT; SPINAL CORD; SPINE;

EID: 54949152772     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awn206     Document Type: Article

References (69)

1. Abbaszade I, Liu QR, Yang F, Rosenfeld SA, Ross OH, Link JR, et al. Cloning and characterization of ADAMTS11, an aggrecanase from the aDAMTS family. J Biol Chem 1999; 274: 23444-50.
2. Aspberg A, Adam S, Kostka G, Timpl R, Heinegard D. Fibulin-1 is a ligand for the C-type lectin domains of aggrecan and versican. J Biol Chem 1999; 274: 20444-9.
3. Bamber NI, Li H, Lu X, Oudega M, Aebischer P, Xu XM. Neurotrophins BDNF and NT-3 promote axonal re-entry into the distal host spinal cord through Schwann cell-seeded mini-channels. Eur J Neurosci 2001; 13 (2): 257-68.
4. Beckerman M, editor. Molecular and cellular signaling. New York: Springer Science and Business Media Inc.; 2005. pp. 196-217.
5. Bradbury EJ, Moon LD, Popat RJ, King VR, Bennett GS, Patel PN, et al. Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature 2000; 416: 636-40.
6. Brambilla R, Bracchi-Ricard V, Hu WH, Frydel B, Bramwell A, Karmally S, et al. Inhibition of astroglial nuclear factor κB reduces inflammation and improves functional recovery after spinal cord injury. J Exp Med 2005; 202: 145-56.
7. Bundesen LQ, Scheel TA, Bregman BS, Kromer LF. Ephrin-B2 and EphB2 regulation of astrocyte-meningeal fibroblast interactions in response to spinal cord lesions in adult rats. J Neurosci 2003; 23: 7789-800.
8. Bush TG, Puvanachandra N, Horner CH, Polito A, Ostenfeld T, Svendsen CN, et al. Leukocyte infiltration, neuronal degeneration, and neurite outgrowth after ablation of scar-forming, reactive astrocytes in adult transgenic mice. Neuron 1999; 23 (2): 297-308.
9. Cafferty WBJ, Yang SH, Duffy PJ, Li S, Strittmatter SM (2007) Functional axonal regeneration through scar genetically modified to digest chondroitin sulfate proteoglycans. J Neurosci 2007; 27: 2176-85.
10. Caggiano AO, Zimber MP, Ganguly A, Blight AR, Gruskin EA. Chondroitinase ABC improves locomotion and bladder function following contusion injury of the rat spinal cord. J Neurotrauma 2005; 22: 226-39.
11. Clarris HJ, Rauch U, Key B. Dynamic spatiotemporal expression patterns of neurocan and phosphacan indicate diverse roles in developing and adult mouse olfactory system. J Comp Neurol 2000; 423: 99-111.
12. Chau CH, Shum DK, Li H, Pei J, Lui YY, Wirthlin L, et al. Chondroitinase ABC enhances axonal regrowth through Schwann cell-seeded guidance channels after spinal cord injury. FASEB J 2004; 18: 194-6.
13. Dergham P, Ellezam B, Essagian C, Avedissian H, Lubell WD, McKerracher L. Rho signaling pathway targeted to promote spinal cord repair. J Neurosci 2002; 22 (15): 6570-7.
14. Faulkner JR, Herrmann JE, Woo MJ, Tansey KE, Doan NB, Sofroniew MV. Reactive astrocytes protect tissue and preserve function after spinal cord injury. J Neurosci 2004; 24 (9): 2143-55.
15. Fidler PS, Schuette K, Asher RA, Dobbertin A, Thornton SR, Calle-Patino Y, et al. Comparing astrocytic cell lines that are inhibitory or permissive for axon growth: The major axon-inhibitory proteoglycans is NG2. J Neurosci 1999; 19: 8778-88.
16. Fournier AE, Takizawa BT, Strittmatter SM. Rho kinase inhibition enhances axonal regeneration in the injured CNS. J Neurosci 2003; 23 (4): 1416-23.
17. Garwood J, Schnädelbach O, Clement A, Schütte K, Bach A, Faissner A. DSD-1 proteoglycan is the mouse homolog of phosphacan and displays opposing effects on neurite outgrowth dependent on neuronal lineage. J Neurosci 1999; 19: 3888-99.
18. Gocombining double acute accenttting C, Kuhn J, Zahn R, Brinkmann T, Kleesiek K. Molecular cloning and expression of human UDP-d-Xylose: proteoglycan core protein beta-d-xylosyltransferase and its first isoform XT-II. J Mol Biol 2000; 304: 517-28.
19. GrandPré T, Li S, Strittmatter SM. Nogo-66 receptor antagonist peptide promotes axonal regeneration. Nature 2002; 417 (6888): 547-51.
20. Gries P, Tighe A, Levin D, Sharma R, Brown A. Transcriptional regulation of scar gene expression in primary astrocytes. Glia 2007; 55: 1145-55.
21. Grimpe B. Isolierung und Charakterisierung des Neurocan-Promotors. Aachen: Shaker; 1996. p. 63.
22. Grimpe B, Silver J. The extracellular matrix in axon regeneration. Prog Brain Res 2002; 137: 333-49.
23. Grimpe B, Silver J. A novel DNA enzyme reduces glycosaminoglycan chains in gliar scar and allows mircrotransplanted dorsal root ganglia axons to regenerate beyond lesions in the spinal cord. J Neurosci 2004; 24: 1393-7.
24. Grumet M, Milev P, Sakurai T, Karthikeyan L, Bourdon M, Margolis RK, et al. Interactions with tenasicn and differential effects on cell adhesion of neurocan and phosphacan, two major chondroitin sulfate proteoglycans of nervous tissue. J Biol Chem 1994; 269: 12142-6.
25. Hagino S, Iseki K, Mori T, Zhang Y, Hikake T, Yokoya S, et al. Slit and glypican-1 mRNAs are coexpressed in the reactive astrocytes of the injured adult brain. Glia 2003; 42: 130-8.
26. Hardingham TE, Fosang AJ. The structure of aggrecan and its turnover in cartilage. J Rheumatol Suppl 1995; 43: 86-90.
27. Houle JD, Tom VJ, Mayers D, Wagoner G, Phillips N, Silver J. 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 2006; 26: 7405-15.
28. Iijima N, Oohira A, Mori T, Kitabatake K, Kohsaka S. Core protein of chondroitin sulfate proteoglycans promotes neurite outgrowth from cultured neocortical neurons. J Neurochem 1991; 56: 706-8.
29. Inatani M, Irie F, Plump AS, Tessier-Lavigne M, Yamaguchi Y. Mammalian brain morphogenesis and midline axon guidance require heparan sulfate. Science 2003; 302: 1044-6.
30. Jones LL, Margolis RU, Tuszynski MH. The chondroitin sulfate proteoglycans neurocan, brevican, phosphacan, and versican are differentially regulated following spinal cord injury. Exp Neurol 2003; 182: 399-411.
31. Koprivica V, Cho KS, Park JB, Yiu G, Atwal J, Gore B, et al. EGFR activation mediates inhibition of axon regeneration by myelin and chondrotin sulfate proteoglycans. Science 2005; 310: 106-10.
32. Krohn K, Rozovsky I, Wals P, Teter B, Anderson CP, Finch CE. Glial fibrillary acidic protein transcription responses to transforming growth factor-beta 1 and interleukine-1beta are mediated by a nuclear factor-1-like site in the near-uprstream promoter. J Neurochem 1999; 72: 1353-61.
33. Laabs TL, Wang H, Katagiri Y, McCann T, Fawcett JW, Geller HM. Inhibiting glycosaminoglycan chain polymerization decreases the inhibitory activity of astrocyte-derived chondroitin sulfate proteoglycans. J Neuosci 2007; 27: 14494-501.
34. Law AK, Gupta D, Levy S, Wallace DC, McKeon RJ, Buck CR. TGF-beta 1 induction of the adenine nucleotide translocator 1 in astrocytes occurs through Smads and Sp1 transcription factors. BMC Neurosci 2004; 5: 1-14.
35. Li Y, Field PM, Raisman G. Repair of adult rat corticospinal tract by transplants of olfactory ensheathing cells. Science 1997; 277: 2000-2.
36. Li Y, Field PM, Raisman G. Regeneration of adult rat corticospinal axons induced by transplanted olfactory ensheathing cells. J Neurosci 1998; 18: 10514-24.
37. Lu P, Yang H, Jones LL, Filbin MT, Tuszynski MH. Combinatorial therapy with neurotrophins and cAMP promotes axonal regeneration beyond sites of spinal cord injury. J Neurosci 2004; 24: 6402-9.
38. Maeda N, Noda M. 6B4 proteoglycan/phosphacan is a repulsive substratum but promotes morphological differentiation of cortical neurons. Development 1996; 122: 647-58.
39. Milev P, Chiba A, Haring M, Rauvala H, Schachner M, Ranscht B, et al. High affinity binding and overlapping localization of neurocan and phosphacan/protein-tyrosine phophatase-ζ/β with tenascin-R, amphoterin, and the heparin-binding growth-associated molecule. J Biol Chem 1998; 273: 6998-7005.
40. Milev P, Maurel P, Haring M, Margolis RK, Margolis RU. TAG-1/axonin-1 is a high-affinity ligand of neurocan, phosphacan/protein-tyrosine phophatase-ζ/β, and N-CAM. J Biol Chem 1996; 271: 15716-23.
41. Moon LD, Asher RA, Rhodes KE, Fawcett JW. Regeneration of CNS axons back to their target following treatment of adult rat brain with chondroitinase ABC. Nature 2001; 4 (5): 465-6.
42. Oudega M, Hagg T. Nerve growth factor promotes regeneration of sensory axons into adult rat spinal cord. Exp Neurol 1996; 140: 218-29.
43. Oudega M, Hagg T. Neurotrophins promote regeneration of sensory axons in the adult rat spinal cord. Brain Res 1999; 818: 432-8.
44. Oudega M, Varon S, Hagg T. Regeneration of adult rat sensory axons into intraspinal nerve graft: promoting effects of conditioning lesion and graft predegeneration. Exp Neurol 1994; 129: 194-206.
45. Pasterkamp RJ, Anderson PN, Verhaagen J. Peripheral nerve injury fails to induce growth of lesioned ascending dorsal column axons into spinal cord scar tissue expressing the axon repellent semaphoring 3A. Eur J Neurosci 2001; 13: 457-71.
46. Preston E, Webster J, Small D. Characteristics of sustained blood-brain barrier opening and tissue injury in a model for focal trauma in the rat. J. Neurotrauma 2001; 18: 83-92.
47. Ramon-Cueto A, Cordero MI, Santos-Bernito FF, Avila J. Functional recovery of paraplegic rats and motor axon regeneration in their spinal cords by olfactory ensheathing glia. Neuron 2000; 25: 425-35.
48. Ramon-Cueto A, Plant GW, Avila J, Bunge MB. Long distance axonal regeneration in the transected adult rat spinal cord is promoted by olfactory ensheathing glia tansplants. J Neurosci 1998; 18: 3803-15.
49. Rauch U, Grimpe B, Kulbe G, Arnold-Ammer I, Beier DR, Fassler R. Structure and chromosomal localization of the mouse neurocan gene. Genomics 1995; 28: 405-10.
50. Rauch U, Meyer H, Brakebusch C, Seidenbecker C, Gundelfinger ED, Beier DR, et al. Sequence and chromosomal localization of the mouse brevican gene. Genomics 1997; 44: 15-21.
51. Retzler C, Göhring W, Rauch U. Analysis of neurocan structures interacting with the neural cell adhesion molecule N-CAM. J Biol Chem 1996; 271: 27304-10.
52. Reuss B, von Bohlen und Halbach O. Fibroblast growth factors and their receptors in the central nervous system. Cell Tissue Res 2003; 313: 139-57.
53. Rhodes KE, Fawcett JW. Chondroitin sulphate proteoglycans: preventing plasticity or protecting the CNS? J Anat 2004; 204 (1): 33-48.
54. Sango K, Oohira A, Ajiki K, Tokashiki A, Horie M, Kawano H. Phosphacan and neurocan are repulsive substrata for adhesion and neurite extension of adult rat dorsal root ganglion neurons in vitro. Exp Neurol 2003; 182 (1): 1-11.
55. Silver J, Miller J. Regeneration beyond the glial scar. Nature 2004; 5: 146-56.
56. Sivasankaran R, Pei J, Wang KC, Zhang YP, Shields CB, Xu XM, et al. PKC mediates inhibitory effects of myelin and chondroitin sulfate proteoglycans on axonal regeneration. Nature Neurosci 2004; 7: 261-8.
57. Smith GM, Strunz C. Growth factor and cytokine regulation of chondroitin sulfate proteoglycans by astrocytes. Glia 2005; 52: 209-18.
58. Smith KJ, Bennet BJ. Topographic and quantitative description of rat dorsal column fibres arising from the lumbar dorsal roots. J Anat 1987; 153: 203-15.
59. Snow DM, Atkinson PB, Hassinger TD, Letourneau PC, Kater SB. Chondroitin sulfate proteoglycan elevates cytoplasmic calcium in DRG neurons. Dev Biol 1994; 166: 87-100.
60. Taylor L, Jones L, Tuszynski MH, Blesch A. Neurotrophin-3 gradients established by lentiviral gene delivery promte short-distance axonal bridging beyond cellular graft in the injured spinal cord. J Neurosci 2006; 26: 9713-21.
61. Tortorella MD, Burn TC, Pratta MA, Abbaszade I, Hollis JM, Liu R, et al. Purification and cloning of aggrecanase-1: a member of the ADAMTS family of proteins. Science 1999; 284: 1664-6.
62. Tsirka SE. Tissue plasminogen activator as a modulator of neuronal survival and function. Biochem Soc Trans 2002; 30: 222-5.
63. Yayon A, Klagsbrun M, Eskos JD, Leder P, Ornitz DM. Cell surface, heparin-like molecules are required for binding of basic fibroblast growth factor to its high affinity receptor. Cell 1991; 64: 841-8.
64. Yick LW, Cheung PT, So KF, Wu W. Axonal regeneration of Clarke's neurons beyond the spinal cord injury scar after treatment with chondroitinase ABC. Exp Neurol 2003; 182: 160-8.
65. Yue X, Li X, Nquyen HT, Chin DR, Sullivan DE, Lasky JA. TGF-beta 1 induces heparan sulfate 6-O-endosulfatase 1 expression in vitro and in vivo. J Biol Chem 2008 [Epub ahead of print].
66. Zhang F, McLellan JS, Ayala AM, Leahy DJ, Linhardt RJ. Kinetic and structural studies on interactions between heparin and heparan sulfate and proteins of the hedgehog signaling pathway. Biochem 2007; 46: 3933-41.
67. Zhang Y, Winterbottom JK, Schachner M, Lieberman AR, Anderson PN. Tenascin-C expression and axonal sprouting following injury to the spinal dorsal column in the adult rat. J. Neurosci 1997; 49: 433-50.
68. Zhang Y, Yeung MN, Liu J, Chau CH, Chan YS, Shum DK. Mapping heparanase expression in the spinal cord of adult rats. J Comp Neurol 2006; 494: 345-57.
69. Zuo J, Neubauer D, Dyess K, Ferguson TA, Muir D. Degradation of chondroitin sulfate proteoglycans enhances the neurite-promoting potential of spinal cord tissue. Exp Neurol 1998; 154: 654-62.