Overcoming endogenous constraints on neuronal regeneration

IEEE Transactions on Biomedical Engineering

Volumn 58, Issue 7, 2011, Pages 1900-1906

  Mokarram, Nassir ^a   Bellamkonda, Ravi V ^b  

^a Georgia Institute of Technology   (United States)

^b Emory University   (United States)

Author keywords

Central nervous system (CNS); immunomodulation; nerve regeneration; peripheral nervous system (PNS)

Indexed keywords

BIOCHEMICAL PATHWAY; CENTRAL NERVOUS SYSTEMS; CNS REGENERATION; GRAND CHALLENGE; IMMUNE CELLS; IMMUNOMODULATION; INFLAMMATORY RESPONSE; NERVE REGENERATION; NEURAL TISSUE; NEUROENGINEERING; PERIPHERAL NERVOUS SYSTEM; PERIPHERAL NERVOUS SYSTEM (PNS); RATE-LIMITING PROCESS; STATE OF THE ART;

TISSUE;

GAMMA INTERFERON; INTERLEUKIN 4; MYELIN; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; BLOOD BRAIN BARRIER; CENTRAL NERVOUS SYSTEM; EXTRACELLULAR MATRIX; HUMAN; IMMUNE SYSTEM; IMMUNOCOMPETENT CELL; IMMUNOMODULATION; INFLAMMATION; MACROGLIA; MACROPHAGE; MICROGLIA; NERVE CELL PLASTICITY; NERVE DEGENERATION; NERVE REGENERATION; PERIPHERAL NERVOUS SYSTEM; SCAR FORMATION;

ANIMALS; CENTRAL NERVOUS SYSTEM; HUMANS; IMMUNOMODULATION; MACROPHAGES; MICROGLIA; NERVE REGENERATION; PERIPHERAL NERVOUS SYSTEM; WOUND HEALING;

EID: 79959556551     PISSN: 00189294     EISSN: 15582531     Source Type: Journal    
DOI: 10.1109/TBME.2010.2103075     Document Type: Article

References (79)

1. G. Gurtner, S. Werner, Y. Barrandon, and M. Longaker, "Wound repair and regeneration," Nature, vol. 453, pp. 314-321, 2008. (Pubitemid 351693137)
2. M. Ferguson and S. OKane, "Scar-free healing: from embryonic mechanisms to adult therapeutic intervention," Philos. Trans. B, vol. 359, p. 839, 2004.
3. G. Yiu and Z. He, "Glial inhibition of CNS axon regeneration," Nat. Rev. Neurosc., vol. 7, pp. 617-627, 2006. (Pubitemid 44106744)
4. S. Odelberg, "Unraveling the molecular basis for regenerative cellular plasticity," PLoS Biol., vol. 2, p. E232, 2004.
5. P.Martin, "Wound healing-aiming for perfect skin regeneration," Science, vol. 276, p. 75, 1997.
6. M. Harty, A. Neff, M. King, and A. Mescher, "Regeneration or scarring: an immunologic perspective," Dev. Dyn., vol. 226, pp. 268-279, 2003. (Pubitemid 36158171)
7. S. Nodder and P. Martin, "Wound healing in embryos: a review," Anatomy Embryol., vol. 195, pp. 215-228, 1997. (Pubitemid 27116444)
8. G. Gurtner, M. Callaghan, and M. Longaker, "Progress and potential for regenerative medicine," Annu. Rev. Med., vol. 58, pp. 299-312, 2007. (Pubitemid 46706516)
9. L. DiPietro, "Wound healing: The role of the macrophage and other immune cells," Shock, vol. 4, p. 233, 1995.
10. S. Lucas, N. Rothwell, and R. Gibson, "The role of inflammation in CNS injury and disease," Br. J. Pharmacol., vol. 147, pp. S232-S240, 2006. (Pubitemid 43077281)
11. D. Donnelly and P. Popovich, "Inflammation and its role in neuroprotection, axonal regeneration and functional recovery after spinal cord injury," Exp. Neurol., vol. 209, pp. 378-388, 2008. (Pubitemid 351181428)
12. T.Wilgus, "Immune cells in the healing skin wound: Influential players at each stage of repair," Pharmacol. Res., vol. 58, pp. 112-116, 2008.
13. C. Baum and C. Arpey, "Normal cutaneous wound healing: Clinical correlation with cellular and molecular events," Dermatol. Surg., vol. 31, pp. 674-686, 2005. (Pubitemid 43093424)
14. T. Eubank and C. Marsh, "Cytokines and growth factors in the regulation of wound inflammation," 2010, 2011.
15. B. Cameron and G. Landreth, "Inflammation, microglia, and alzheimers disease," Neurobiol. Dis., pp. 503-509, 2009.
16. C. Colton, "Heterogeneity of microglial activation in the innate immune response in the brain," J. Neuroimmune Pharmacol., vol. 4, pp. 399-418, 2009.
17. O. Butovsky, Y. Ziv, A. Schwartz, G. Landa, A. Talpalar, S. Pluchino, G. Martino, and M. Schwartz, "Microglia activated by IL-4 or IFN-[gamma] differentially induce neurogenesis and oligodendrogenesis from adult stem/progenitor cells," Mol. Cell. Neurosci., vol. 31, pp. 149-160, 2006. (Pubitemid 43049908)
18. P. Mountziaris and A. Mikos, "Modulation of the inflammatory response for enhanced bone tissue regeneration," Tissue Eng. Part B: Rev., vol. 14, pp. 179-186, 2008. (Pubitemid 351839215)
19. O. Butovsky, A. Talpalar, K. Ben-Yaakov, and M. Schwartz, "Activation of microglia by aggregated [beta]-amyloid or lipopolysaccharide impairs MHC-II expression and renders them cytotoxicwhereas IFN-[gamma] and IL-4 render them protective," Mol. Cell. Neurosci., vol. 29, pp. 381-393, 2005. (Pubitemid 40799211)
20. H. Arnett, J. Mason, M. Marino, K. Suzuki, G. Matsushima, and J. Ting, "TNF promotes proliferation of oligodendrocyte progenitors and remyelination," Nat. Neurosci., vol. 4, pp. 1116-1122, 2001. (Pubitemid 34116557)
21. A. Belmadani, P. Tran, D. Ren, and R. Miller, "Chemokines regulate the migration of neural progenitors to sites of neuroinflammation," J. Neurosci., vol. 26, pp. 3182-3191, 2006.
22. A. Cashen,H. Lazarus, and S. Devine, "Mobilizing stem cells from normal donors: is it possible to improve upon G-CSF?," Bone Marrow Transplantation, vol. 39, pp. 577-588, 2007. (Pubitemid 46729051)
23. L. To, D. Haylock, P. Simmons, and C. Juttner, "The biology and clinical uses of blood stem cells," Blood, vol. 89, pp. 2233-2258, 1997. (Pubitemid 27143269)
24. Y. Yan, K. Sailor, B. Lang, S. Park, R. Vemuganti, and R. Dempsey, "Monocyte chemoattractant protein-1 plays a critical role in neuroblast migration after focal cerebral ischemia," J. Cerebral Blood Flow Metab., vol. 27, pp. 1213-1224, 2006.
25. C. Mills, K. Kincaid, J. Alt, M. Heilman, and A. Hill, "M-1/M-2 macrophages and the Th1/Th2 paradigm," J. Immunol., vol. 164, pp. 6166-6173, 2000. (Pubitemid 30408793)
26. D. Mosser, "The many faces of macrophage activation," J. Leukocyte Biol., vol. 73, pp. 209-212, 2003. (Pubitemid 36158295)
27. S. Gordon and P. Taylor, "Monocyte and macrophage heterogeneity," Nat. Rev. Immunol., vol. 5, pp. 953-964, 2005. (Pubitemid 41746764)
28. J. Edwards, X. Zhang, K. Frauwirth, and D. Mosser, "Biochemical and functional characterization of three activated macrophage populations," J. Leukocyte Biol., vol. 80, pp. 1298-1307, 2006. (Pubitemid 44904968)
29. D. Mosser and J. Edwards, "Exploring the full spectrum of macrophage activation," Nat. Rev. Immunol., vol. 8, pp. 958-969, 2008.
30. J. Folkman and M. Klagsbrun, "Angiogenic factors," Science, vol. 235, pp. 442-447, 1987. (Pubitemid 17009577)
31. C. Krarup, S. Archibald, and R. Madison, "Factors that influence peripheral nerve regeneration: an electrophysiological study of the monkey median nerve," Ann. Neurol., vol. 51, pp. 69-81, 2002. (Pubitemid 34027979)
32. A. Höke and T. Brushart, "Introduction to special issue: Challenges and opportunities for regeneration in the peripheral nervous system," Exp. Neurol., 2009.
33. E. Verdú, D. Ceballos, J. Vilches, and X. Navarro, "Influence of aging on peripheral nerve function and regeneration," J. Peripheral Nerv. Syst., vol. 5, pp. 191-208, 2000. (Pubitemid 32037991)
34. S. Fu and T. Gordon, "Contributing factors to poor functional recovery after delayed nerve repair: Prolonged axotomy," J. Neurosci., vol. 15, pp. 3876-3885, 1995.
35. S. Fu and T. Gordon, "Contributing factors to poor functional recovery after delayed nerve repair: Prolonged denervation," J. Neurosci., vol. 15, pp. 3886-3895, 1995.
36. M. Groves, R. McKeon, E. Werner, M. Nagarsheth, W. Meador, and A. English, "Axon regeneration in peripheral nerves is enhanced by proteoglycan degradation," Exp. Neurol., vol. 195, pp. 278-292, 2005. (Pubitemid 41309054)
37. J. Zuo, Y. Hernandez, and D. Muir, "Chondroitin sulfate proteoglycan with neurite-inhibiting activity is up-regulated following peripheral nerve injury," J. Neurobiol., vol. 34, pp. 41-54, 1998. (Pubitemid 28032425)
38. M. Patel and J. McNamara, "Selective enhancement of axonal branching of cultured dentate gyrus neurons by neurotrophic factors," Neuroscience, vol. 69, pp. 763-770, 1995.
39. T. Kennedy and M. Tessier-Lavigne, "Guidance and induction of branch formation in developing axons by target-derived diffusible factors," Curr. Opin. Neurobiol., vol. 5, pp. 83-90, 1995.
40. R. Bellamkonda, "Peripheral nerve regeneration: An opinion on channels, scaffolds and anisotropy," Biomaterials, vol. 27, pp. 3515-3518, 2006.
41. P. Horner and F. Gage, "Regenerating the damaged central nervous system," Nature, vol. 407, pp. 963-970, 2000.
42. P. Richardson, U. McGuinness, and A. Aguayo, "Axons from CNS neurones regenerate into PNS grafts,", 1980.
43. S. David and A. Aguayo, "Axonal elongation into peripheral nervous system" bridges" after central nervous system injury in adult rats," Science, vol. 214, pp. 931-933, 1981. (Pubitemid 12220099)
44. G. Siegel, Basic Neurochemistry. Boston: Little Brown and Company, 1981.
45. M. Schwab and H. Thoenen, "Dissociated neurons regenerate into sciatic but not optic nerve explants in culture irrespective of neurotrophic factors," J. Neurosci., vol. 5, pp. 2415-23, 1985. (Pubitemid 15226933)
46. M. Vargas and B. Barres, "Why is Wallerian degeneration in the CNS so slow?" 2007.
47. B. Barres, M. Jacobson, R. Schmid, M. Sendtner, and M. Raff, "Does oligodendrocyte survival depend on axons?" Curr. Biol., vol. 3, pp. 489-497, 1993.
48. M. Carson, J. Doose, B. Melchior, C. Schmid, and C. Ploix, "CNS immune privilege: hiding in plain sight," Immunol. Rev., vol. 213, pp. 48-65, 2006. (Pubitemid 44401493)
49. I. Galea, I. Bechmann, and V. Perry, "What is immune privilege (not)?," Trends Immunol., vol. 28, pp. 12-18, 2007. (Pubitemid 44960159)
50. F. Gage, "Mammalian neural stem cells," Science, vol. 287, pp. 1433-8, 2000. (Pubitemid 30127128)
51. N. Gaiano and G. Fishell, "Transplantation as a tool to study progenitors within the vertebrate nervous system," J. Neurobiol., vol. 36, pp. 152-161, 1998. (Pubitemid 28363228)
52. H. Nakatomi, T. Kuriu, S. Okabe, S. Yamamoto, O. Hatano, N. Kawahara, A. Tamura, T. Kirino, and M. Nakafuku, "Regeneration of hippocampal pyramidal neurons after ischemic brain injury by recruitment of endogenous neural progenitors," Cell, vol. 110, pp. 429-441, 2002. (Pubitemid 35232287)
53. J. McDonald, X. Liu, Y. Qu, S. Liu, S. Mickey, D. Turetsky, D. Gottlieb, and D. Choi, "Transplanted embryonic stem cells survive, differentiate and promote recovery in injured rat spinal cord," Nat. Med., vol. 5, pp. 1410-1412, 1999.
54. A. Vescovi, E. Parati, A. Gritti, P. Poulin, M. Ferrario, E. Wanke, P. Frölichsthal-Schoeller, L. Cova, M. Arcellana-Panlilio, and A. Colombo, "Isolation and cloning of multipotential stem cells from the embryonic human CNS and establishment of transplantable human neural stem cell lines by epigenetic stimulation? 1," Exp. Neurol., vol. 156, pp. 71-83, 1999. (Pubitemid 29152984)
55. H. Keirstead, "Stem cell transplantation into the central nervous system and the control of differentiation," J. Neurosci. Res., vol. 63, pp. 233-236, 2001. (Pubitemid 32115284)
56. G. Yancopoulos, S. Davis, N. Gale, J. Rudge, S. Wiegand, and J. Holash, "Vascular-specific growth factors and blood vessel formation," Nature, vol. 407, pp. 242-248, 2000.
57. M. Hobson, C. Green, and G. Terenghi, "VEGF enhances intraneural angiogenesis and improves nerve regeneration after axotomy," J. Anatomy, vol. 197, pp. 591-605, 2001. (Pubitemid 32051540)
58. A. Gratchev, J. Kzhyshkowska, K. Köthe, I. Muller-Molinet, S. Kannookadan, J. Utikal, and S. Goerdt, "M [?] 1 and M [?] 2 can be repolarized by Th2 or Th1 cytokines, respectively, and respond to exogenous danger signals," Immunobiology, vol. 211, pp. 473-486, 2006.
59. R. Stout, C. Jiang, B. Matta, I. Tietzel, S. Watkins, and J. Suttles, "Macrophages sequentially change their functional phenotype in response to changes in microenvironmental influences," J. Immunol., vol. 175, pp. 342-349, 2005. (Pubitemid 40884337)
60. C. Farina, F.Aloisi, and E.Meinl, "Astrocytes are active players in cerebral innate immunity," Trends Immunol., vol. 28, pp. 138-145, 2007. (Pubitemid 46283692)
61. Y. Liu, I. Teige, B. Birnir, and S. Issazadeh-Navikas, "Neuron-mediated generation of regulatory T cells from encephalitogenic T cells suppresses EAE," Nat. Med., vol. 12, pp. 518-525, 2006.
62. J. Herz, F. Zipp, and V. Siffrin, "Neurodegeneration in autoimmune CNS inflammation," Exp. Neuro., 2009.
63. W. Nöel, G. Raes, G. Hassanzadeh, Ghassabeh, P. De Baetselier, and A. Beschin, "Alternatively activated macrophages during parasite infections," Trends Parasitol., vol. 20, pp. 126-133, 2004. (Pubitemid 38264445)
64. M. Schwartz, O. Butovsky,W. Brück, and U. Hanisch, "Microglial phenotype: is the commitment reversible?," Trends Neurosci., vol. 29, pp. 68-74, 2006. (Pubitemid 43202595)
65. I. Shaked, D. Tchoresh, R. Gersner, G. Meiri, S. Mordechai, X. Xiao, R. Hart, and M. Schwartz, "Protective autoimmunity: Interferon-enables microglia to remove glutamate without evoking inflammatory mediators," J. Neurochem., vol. 92, pp. 997-1009, 2005. (Pubitemid 40344291)
66. W. Brück, Y. Brück, and R. Friede, "TNF-[alpha] suppresses CR3-mediated myelin removal by macrophages," J. Neuroimmunol., vol. 38, pp. 9-17, 1992.
67. R. Saha, X. Liu, and K. Pahan, "Up-regulation of BDNF in astrocytes by TNF-: a case for the neuroprotective role of cytokine," J. Neuroimmune Pharmacol., vol. 1, pp. 212-222, 2006. (Pubitemid 44244127)
68. J. Mason, K. Suzuki, D. Chaplin, and G. Matsushima, "Interleukin-1 {beta} Promotes Repair of the CNS," J. Neurosci., vol. 21, p. 7046, 2001.
69. J. OKusky, P.Ye, and A. DErcole, "Insulin-like growth factor-I promotes neurogenesis and synaptogenesis in the hippocampal dentate gyrus during postnatal development," J. Neurosci., vol. 20, pp. 8435-42, 2000.
70. J. Hsieh, J. Aimone, B. Kaspar, T. Kuwabara, K. Nakashima, and F. Gage, "IGF-I instructs multipotent adult neural progenitor cells to become oligodendrocytes," J. Cell Biol., vol. 164, pp. 111-122, 2004. (Pubitemid 38082462)
71. R. Lichtenwalner, M. Forbes, S. Bennett, C. Lynch, W. Sonntag, and D. Riddle, "Intracerebroventricular infusion of insulin-like growth factor-I ameliorates the age-related decline in hippocampal neurogenesis," Neuroscience, vol. 107, pp. 603-613, 2001. (Pubitemid 33097497)
72. I. Napoli and H. Neumann, "Protective effects of microglia in multiple sclerosis," Exp. Neurol., 2009.
73. V. Mukhatyar, L. Karumbaiah, J. Yeh, and R. Bellamkonda, "Tissue engineering strategies designed to realize the endogenous regenerative potential of peripheral nerves," Adv. Mater., vol. 21, pp. 4670-4679, 2009.
74. K. McNeeley, E. Karathanasis, A. Annapragada, and R. Bellamkonda, "Masking and triggered unmasking of targeting ligands on nanocarriers to improve drug delivery to brain tumors," Biomaterials, vol. 30, pp. 3986-3995, 2009.
75. Y. Kim, J. Caldwell, and R. Bellamkonda, "Nanoparticle-mediated local delivery of methylprednisolone after spinal cord injury," Biomaterials, vol. 30, pp. 2582-2590, 2009.
76. Y. Kim, V. Haftel, S. Kumar, and R. Bellamkonda, "The role of aligned polymer fiber-based constructs in the bridging of long peripheral nerve gaps," Biomaterials, vol. 29, pp. 3117-3127, 2008.
77. M. Dodla and R. Bellamkonda, "Differences between the effect of anisotropic and isotropic laminin and nerve growth factor presenting scaffolds on nerve regeneration across long peripheral nerve gaps," Biomaterials, vol. 29, pp. 33-46, 2008. (Pubitemid 47599652)
78. A. Jain, Y. Kim, R. McKeon, and R. Bellamkonda, "In situ gelling hydrogels for conformal repair of spinal cord defects, and local delivery of BDNF after spinal cord injury," Biomaterials, vol. 27, pp. 497-504, 2006. (Pubitemid 41457252)
79. I. Clements, Y. Kim, A. English, X. Lu, A. Chung, and R. Bellamkonda, "Thin-film enhanced nerve guidance channels for peripheral nerve repair," Biomaterials, vol. 30, pp. 3834-3846, 2009.