Fibronectin Matrix Assembly after Spinal Cord Injury

Journal of Neurotrauma

Volumn 32, Issue 15, 2015, Pages 1158-1167

  Zhu, Yunjiao ^a   Soderblom, Cynthia ^a   Trojanowsky, Michelle ^a   Lee, Do Hun ^a   Lee, Jae K ^a  

^a UNIVERSITY OF MIAMI   (United States)

Author keywords

fibronectin; fibrotic scar; macrophages; microglia; spinal cord injury

Indexed keywords

FIBRONECTIN; VERY LATE ACTIVATION ANTIGEN 5;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; CONTROLLED STUDY; FEMALE; FIBROBLAST; GENE DELETION; MACROPHAGE ACTIVATION; MICROGLIA; MOUSE; NONHUMAN; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; RAT; SCAR FORMATION; SPINAL CORD INJURY; ANIMAL; DISEASE MODEL; EXTRACELLULAR MATRIX; METABOLISM; PATHOLOGY; POLYMERASE CHAIN REACTION; SCAR; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; CICATRIX; DISEASE MODELS, ANIMAL; EXTRACELLULAR MATRIX; FEMALE; FIBROBLASTS; FIBRONECTINS; INTEGRIN ALPHA5BETA1; MICE; POLYMERASE CHAIN REACTION; RATS; SPINAL CORD INJURIES;

EID: 84937000986     PISSN: 08977151     EISSN: 15579042     Source Type: Journal    
DOI: 10.1089/neu.2014.3703     Document Type: Article

References (54)

1. Cregg, J.M., Depaul, M.A., Filous, A.R., Lang, B.T., Tran, A. and Silver, J. (2014). Functional regeneration beyond the glial scar. Exp. Neurol. 253C, 197-207.
2. Burda, J.E. and Sofroniew, M.V. (2014). Reactive gliosis and the multicellular response to CNS damage and disease. Neuron 81, 229-248.
3. Shearer, M.C. and Fawcett, J.W. (2001). The astrocyte/meningeal cell interface-a barrier to successful nerve regeneration? Cell Tissue Res. 305, 267-273.
4. Kimura-Kuroda, J., Teng, X., Komuta, Y., Yoshioka, N., Sango, K., Kawamura, K., Raisman, G., and Kawano, H. (2010). An in vitro model of the inhibition of axon growth in the lesion scar formed after central nervous system injury. Mol. Cell. Neurosci. 43, 177-187.
5. Wanner, I.B., Deik, A., Torres, M., Rosendahl, A., Neary, J.T., Lemmon, V.P., and Bixby, J.L. (2008). A new in vitro model of the glial scar inhibits axon growth. Glia 56, 1691-1709.
6. Goritz, C., Dias, D.O., Tomilin, N., Barbacid, M., Shupliakov, O., and Frisen, J. (2011). A pericyte origin of spinal cord scar tissue. Science 333, 238-242.
7. Herrmann, J.E., Shah, R.R., Chan, A.F., and Zheng, B. (2010). EphA4 deficient mice maintain astroglial-fibrotic scar formation after spinal cord injury. Exp. Neurol. 223, 582-598.
8. Bundesen, L.Q., Scheel, T.A., Bregman, B.S., and Kromer, L.F. (2003). Ephrin-B2 and EphB2 regulation of astrocyte-meningeal fibroblast interactions in response to spinal cord lesions in adult rats. J. Neurosci. 23, 7789-7800.
9. Stoffels, J.M., de Jonge, J.C., Stancic, M., Nomden, A., van Strien, M.E., Ma, D., Siskova, Z., Maier, O., Ffrench-Constant, C., Franklin, R.J., Hoekstra, D., Zhao, C., and Baron, W. (2013). Fibronectin aggregation in multiple sclerosis lesions impairs remyelination. Brain 136, 116-131.
10. Gratchev, A., Guillot, P., Hakiy, N., Politz, O., Orfanos, C.E., Schledzewski, K., and Goerdt, S. (2001). Alternatively activated macrophages differentially express fibronectin and its splice variants and the extracellular matrix protein betaIG-H3. Scand. J. Immunol. 53, 386-392.
11. Singh, P., Carraher, C., and Schwarzbauer, J.E. (2010). Assembly of fibronectin extracellular matrix. Annu. Rev. Cell Dev. Biol. 26, 397-419.
12. Danen, E.H. and Yamada, K.M. (2001). Fibronectin, integrins, and growth control. J. Cell Physiol. 189, 1-13.
13. Schwarzbauer, J.E. and DeSimone, D.W. (2011). Fibronectins, their fibrillogenesis, and in vivo functions. Cold Spring Harb. Perspect. Biol. 3.
14. To, W.S. and Midwood, K.S. (2011). Plasma and cellular fibronectin: distinct and independent functions during tissue repair. Fibrogenesis Tissue Repair 4, 21.
15. Soderblom, C., Luo, X., Blumenthal, E., Bray, E., Lyapichev, K., Ramos, J., Krishnan, V., Lai-Hsu, C., Park, K.K., Tsoulfas, P., and Lee, J.K. (2013). Perivascular fibroblasts form the fibrotic scar after contusive spinal cord injury. J. Neurosci. 33, 13882-13887.
16. Norenberg, M.D., Smith, J., and Marcillo, A. (2004). The pathology of human spinal cord injury: defining the problems. J. Neurotrauma 21, 429-440.
17. Guest, J.D., Hiester, E.D., and Bunge, R.P. (2005). Demyelination and Schwann cell responses adjacent to injury epicenter cavities following chronic human spinal cord injury. Exp. Neurol. 192, 384-393.
18. Yata, Y., Scanga, A., Gillan, A., Yang, L., Reif, S., Breindl, M., Brenner, D.A., and Rippe, R.A. (2003). DNase I-hypersensitive sites enhance alpha1(I) collagen gene expression in hepatic stellate cells. Hepatology 37, 267-276.
19. Arenkiel, B.R., Hasegawa, H., Yi, J.J., Larsen, R.S., Wallace, M.L., Philpot, B.D., Wang, F., and Ehlers, M.D. (2011). Activity-induced remodeling of olfactory bulb microcircuits revealed by monosynaptic tracing. PLoS One 6, e29423.
20. Moriya, K., Bae, E., Honda, K., Sakai, K., Sakaguchi, T., Tsujimoto, I., Kamisoyama, H., Keene, D.R., Sasaki, T., and Sakai, T. (2011). A fibronectin-independent mechanism of collagen fibrillogenesis in adult liver remodeling. Gastroenterology 140, 1653-1663.
21. Basso, D.M., Fisher, L.C., Anderson, A.J., Jakeman, L.B., McTigue, D.M., and Popovich, P.G. (2006). Basso Mouse Scale for locomotion detects differences in recovery after spinal cord injury in five common mouse strains. J. Neurotrauma 23, 635-659.
22. Wierzbicka-Patynowski, I., Mao, Y., and Schwarzbauer, J.E. (2004). Analysis of fibronectin matrix assembly. Curr. Protoc. Cell Biol. Chapter 10, Unit 10 12.
23. Welinder, C. and Ekblad, L. (2011). Coomassie staining as loading control in Western blot analysis. J Proteome Res 10, 1416-1419.
24. Clausen, B.E., Burkhardt, C., Reith, W., Renkawitz, R., and Forster, I. (1999). Conditional gene targeting in macrophages and granulocytes using LysMcre mice. Transgenic Res. 8, 265-277.
25. Goldmann, T., Wieghofer, P., Muller, P.F., Wolf, Y., Varol, D., Yona, S., Brendecke, S.M., Kierdorf, K., Staszewski, O., Datta, M., Luedde, T., Heikenwalder, M., Jung, S., and Prinz, M. (2013). A new type of microglia gene targeting shows TAK1 to be pivotal in CNS autoimmune inflammation. Nat. Neurosci. 16, 1618-1626.
26. Abram, C.L., Roberge, G.L., Hu, Y., and Lowell, C.A. (2014). Comparative analysis of the efficiency and specificity of myeloid-Cre deleting strains using ROSA-EYFP reporter mice. J. Immunol. Methods 408, 89-100.
27. van der Flier, A., Badu-Nkansah, K., Whittaker, C.A., Crowley, D., Bronson, R.T., Lacy-Hulbert, A., and Hynes, R.O. (2010). Endothelial alpha5 and alphav integrins cooperate in remodeling of the vasculature during development. Development 137, 2439-2449.
28. Yang, J.T., Bader, B.L., Kreidberg, J.A., Ullman-Cullere, M., Trevithick, J.E., and Hynes, R.O. (1999). Overlapping and independent functions of fibronectin receptor integrins in early mesodermal development. Dev. Biol. 215, 264-277.
29. Takahashi, S., Leiss, M., Moser, M., Ohashi, T., Kitao, T., Heckmann, D., Pfeifer, A., Kessler, H., Takagi, J., Erickson, H.P., and Fassler, R. (2007). The RGD motif in fibronectin is essential for development but dispensable for fibril assembly. J. Cell Biol. 178, 167-178.
30. Kigerl, K.A., McGaughy, V.M., and Popovich, P.G. (2006). Comparative analysis of lesion development and intraspinal inflammation in four strains of mice following spinal contusion injury. J Comp. Neurol. 494, 578-594.
31. Byrnes, K.R., Fricke, S.T., and Faden, A.I. (2010). Neuropathological differences between rats and mice after spinal cord injury. J. Magn. Reson. Imaging 32, 836-846.
32. Sroga, J.M., Jones, T.B., Kigerl, K.A., McGaughy, V.M., and Popovich, P.G. (2003). Rats and mice exhibit distinct inflammatory reactions after spinal cord injury. J. Comp. Neurol. 462, 223-240.
33. Surey, S., Berry, M., Logan, A., Bicknell, R., and Ahmed, Z. (2014). Differential cavitation, angiogenesis and wound-healing responses in injured mouse and rat spinal cords. Neuroscience 275, 62-80.
34. Donnelly, D.J. and Popovich, P.G. (2008). Inflammation and its role in neuroprotection, axonal regeneration and functional recovery after spinal cord injury. Exp. Neurol. 209, 378-388.
35. Singer, A.J. and Clark, R.A. (1999). Cutaneous wound healing. N Engl. J. Med. 341, 738-746.
36. Rhett, J.M., Ghatnekar, G.S., Palatinus, J.A., OQuinn, M., Yost, M.J., and Gourdie, R.G. (2008). Novel therapies for scar reduction and regenerative healing of skin wounds. Trends Biotechnol. 26, 173-180.
37. Gharaee-Kermani, M., Wiggins, R., Wolber, F., Goyal, M., and Phan, S.H. (1996). Fibronectin is the major fibroblast chemoattractant in rabbit anti-glomerular basement membrane disease. Am. J. Pathol. 148, 961-967.
38. Trial, J., Baughn, R.E., Wygant, J.N., McIntyre, B.W., Birdsall, H.H., Youker, K.A., Evans, A., Entman, M.L., and Rossen, R.D. (1999). Fibronectin fragments modulate monocyte VLA-5 expression and monocyte migration. J. Clin. Invest. 104, 419-430.
39. Nasu-Tada, K., Koizumi, S., and Inoue, K. (2005). Involvement of beta1 integrin in microglial chemotaxis and proliferation on fibronectin: different regulations by ADP through PKA. Glia 52, 98-107.
40. Abshire, M.Y., Thomas, K.S., Owen, K.A. and Bouton, A.H. (2011). Macrophage motility requires distinct alpha5beta1/FAK and alpha4-beta1/paxillin signaling events. J. Leukoc. Biol. 89, 251-257.
41. Geller, H.M. and Fawcett, J.W. (2002). Building a bridge: engineering spinal cord repair. Exp. Neurol. 174, 125-136.
42. King, V.R., Alovskaya, A., Wei, D.Y., Brown, R.A., and Priestley, J.V. (2010). The use of injectable forms of fibrin and fibronectin to support axonal ingrowth after spinal cord injury. Biomaterials 31, 4447-4456.
43. King, V.R., Hewazy, D., Alovskaya, A., Phillips, J.B., Brown, R.A., and Priestley, J.V. (2010). The neuroprotective effects of fibronectin mats and fibronectin peptides following spinal cord injury in the rat. Neuroscience 168, 523-530.
44. Tate, C.C., Shear, D.A., Tate, M.C., Archer, D.R., Stein, D.G., and LaPlaca, M.C. (2009). Laminin and fibronectin scaffolds enhance neural stem cell transplantation into the injured brain. Journal of tissue engineering and regenerative medicine 3, 208-217.
45. Tate, C.C., Garcia, A.J., and LaPlaca, M.C. (2007). Plasma fibronectin is neuroprotective following traumatic brain injury. Exp. Neurol. 207, 13-22.
46. Sakai, T., Johnson, K.J., Murozono, M., Sakai, K., Magnuson, M.A., Wieloch, T., Cronberg, T., Isshiki, A., Erickson, H.P., and Fassler, R. (2001). Plasma fibronectin supports neuronal survival and reduces brain injury following transient focal cerebral ischemia but is not essential for skin-wound healing and hemostasis. Nat. Med. 7, 324-330.
47. Tang, X., Davies, J.E., and Davies, S.J. (2003). Changes in distribution, cell associations, and protein expression levels of NG2, neurocan, phosphacan, brevican, versican V2, and tenascin-C during acute to chronic maturation of spinal cord scar tissue. J. Neurosci. Res. 71, 427-444.
48. Camand, E., Morel, M.P., Faissner, A., Sotelo, C., and Dusart, I. (2004). Long-term changes in the molecular composition of the glial scar and progressive increase of serotoninergic fibre sprouting after hemisection of the mouse spinal cord. Eur. J. Neurosci. 20, 1161-1176.
49. Perkins, M.E., Ji, T.H., and Hynes, R.O. (1979). Cross-linking of fibronectin to sulfated proteoglycans at the cell surface. Cell 16, 941-952.
50. Lewandowska, K., Choi, H.U., Rosenberg, L.C., Zardi, L., and Culp, L.A. (1987). Fibronectin-mediated adhesion of fibroblasts: inhibition by dermatan sulfate proteoglycan and evidence for a cryptic glycosaminoglycanbinding domain. J. Cell Biol. 105, 1443-1454.
51. Isemura, M., Sato, N., Yamaguchi, Y., Aikawa, J., Munakata, H., Hayashi, N., Yosizawa, Z., Nakamura, T., Kubota, A., Arakawa, M., et al. (1987). Isolation and characterization of fibronectin-binding proteoglycan carrying both heparan sulfate and dermatan sulfate chains from human placenta. J. Biol. Chem 262, 8926-8933.
52. Noble, L.J. and Wrathall, J.R. (1989). Distribution and time course of protein extravasation in the rat spinal cord after contusive injury. Brain Res. 482, 57-66.
53. Whetstone, W.D., Hsu, J.Y., Eisenberg, M., Werb, Z., and Noble-Haeusslein, L.J. (2003). Blood-spinal cord barrier after spinal cord injury: relation to revascularization and wound healing. J. Neurosci. Res. 74, 227-239.
54. Metz, G.A., Curt, A., van de Meent, H., Klusman, I., Schwab, M.E., and Dietz, V. (2000). Validation of the weight-drop contusion model in rats: a comparative study of human spinal cord injury. J. Neurotrauma 17, 1-17.