Non-mammalian model systems for studying neuro-immune interactions after spinal cord injury

Experimental Neurology

Volumn 258, Issue , 2014, Pages 130-140

  Bloom, Ona ^a,b  

^a FEINSTEIN INSTITUTE FOR MEDICAL RESEARCH   (United States)

^b DONALD AND BARBARA ZUCKER SCHOOL OF MEDICINE AT HOFSTRA NORTHWELL   (United States)

Author keywords

Immune system; Inflammation; Regeneration; Spinal cord injury

Indexed keywords

MYELIN ASSOCIATED GLYCOPROTEIN;

ANURA; CONVALESCENCE; EXPERIMENTAL MODEL; GLIOSIS; IMMUNE RESPONSE; LAMPREY; MEDICAL RESEARCH; NERVOUS SYSTEM DEVELOPMENT; NEUROBIOLOGY; NONHUMAN; PRIORITY JOURNAL; REGENERATIVE ABILITY; REVIEW; SALAMANDER; SCAR FORMATION; SPINAL CORD INJURY; TURTLE; ZEBRA FISH; ANIMAL; DISEASE MODEL; HUMAN; IMMUNE SYSTEM; IMMUNOLOGY; IMMUNOMODULATION; INFLAMMATION; METABOLISM; PATHOLOGY; PHYLOGENY; PHYSIOLOGY; REGENERATION; SPINAL CORD REGENERATION;

IMMUNE SYSTEM; INFLAMMATION; REGENERATION; SPINAL CORD INJURY;

ANIMALS; DISEASE MODELS, ANIMAL; HUMANS; NEUROIMMUNOMODULATION; PHYLOGENY; SPINAL CORD INJURIES; SPINAL CORD REGENERATION;

EID: 84904793560     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2013.12.023     Document Type: Review

References (196)

1. Abdullayev I., Kirkham M., Bjorklund A.K., Simon A., Sandberg R. A reference transcriptome and inferred proteome for the salamander Notophthalmus viridescens. Exp. Cell Res. 2013, 319:1187-1197.
2. Adrian E.K., Williams M.G., George F.C. Fine structure of reactive cells in injured nervous tissue labeled with 3H-thymidine injected before injury. J. Comp. Neurol. 1978, 180:815-839.
3. Alder M.N., Rogozin I.B., Iyer L.M., Glazko G.V., Cooper M.D., Pancer Z. Diversity and function of adaptive immune receptors in a jawless vertebrate. Science 2005, 310:1970-1973.
4. Alder M.N., Herrin B.R., Sadlonova A., Stockard C.R., Grizzle W.E., Gartland L.A., Gartland G.L., Boydston J.A., Turnbough C.L., Cooper M.D. Antibody responses of variable lymphocyte receptors in the lamprey. Nat. Immunol. 2008, 9:319-327.
5. Alexander J.K., Popovich P.G. Neuroinflammation in spinal cord injury: therapeutic targets for neuroprotection and regeneration. Prog. Brain Res. 2009, 175:125-137.
6. Alvarez-Buylla A., Nottebohm F. Migration of young neurons in adult avian brain. Nature 1988, 335:353-354.
7. Bajoghli B., Guo P., Aghaallaei N., Hirano M., Strohmeier C., McCurley N., Bockman D.E., Schorpp M., Cooper M.D., Boehm T. A thymus candidate in lampreys. Nature 2011, 470:90-94.
8. Bao F., Bailey C.S., Gurr K.R., Bailey S.I., Rosas-Arellano M.P., Brown A., Dekaban G.A., Weaver L.C. Human spinal cord injury causes specific increases in surface expression of beta integrins on leukocytes. J. Neurotrauma 2010, 28:269-280.
9. Barros-Becker F., Romero J., Pulgar A., Feijoo C.G. Persistent oxytetracycline exposure induces an inflammatory process that improves regenerative capacity in zebrafish larvae. PLoS One 2012, 7:e36827.
10. Bartholdi D., Schwab M.E. Methylprednisolone inhibits early inflammatory processes but not ischemic cell death after experimental spinal cord lesion in the rat. Brain Res. 1995, 672:177-186.
11. Bartholdi D., Schwab M.E. Expression of pro-inflammatory cytokine and chemokine mRNA upon experimental spinal cord injury in mouse: an in situ hybridization study. Eur. J. Neurosci. 1997, 9:1422-1438.
12. Baumgart E.V., Barbosa J.S., Bally-Cuif L., Gotz M., Ninkovic J. Stab wound injury of the zebrafish telencephalon: a model for comparative analysis of reactive gliosis. Glia 2011, 60:343-357.
13. Beck C.W., Christen B., Slack J.M. Molecular pathways needed for regeneration of spinal cord and muscle in a vertebrate. Dev. Cell 2003, 5:429-439.
14. Becker T., Becker C.G. Regenerating descending axons preferentially reroute to the gray matter in the presence of a general macrophage/microglial reaction caudal to a spinal transection in adult zebrafish. J. Comp. Neurol. 2001, 433:131-147.
15. Becker C.G., Becker T. Repellent guidance of regenerating optic axons by chondroitin sulfate glycosaminoglycans in zebrafish. J. Neurosci. 2002, 22:842-853.
16. Becker C.G., Becker T. Growth and pathfinding of regenerating axons in the optic projection of adult fish. J. Neurosci. Res. 2007, 85:2793-2799.
17. Becker C.G., Becker T. Adult zebrafish as a model for successful central nervous system regeneration. Restor. Neurol. Neurosci. 2008, 26:71-80.
18. Becker T., Wullimann M.F., Becker C.G., Bernhardt R.R., Schachner M. Axonal regrowth after spinal cord transection in adult zebrafish. J. Comp. Neurol. 1997, 377:577-595.
19. Becker T., Bernhardt R.R., Reinhard E., Wullimann M.F., Tongiorgi E., Schachner M. Readiness of zebrafish brain neurons to regenerate a spinal axon correlates with differential expression of specific cell recognition molecules. J. Neurosci. 1998, 18:5789-5803.
20. Becker C.G., Lieberoth B.C., Morellini F., Feldner J., Becker T., Schachner M. L1.1 is involved in spinal cord regeneration in adult zebrafish. J. Neurosci. 2004, 24:7837-7842.
21. Benowitz L.I., Popovich P.G. Inflammation and axon regeneration. Curr. Opin. Neurol. 2011, 24:577-583.
22. Bethea J.R., Castro M., Keane R.W., Lee T.T., Dietrich W.D., Yezierski R.P. Traumatic spinal cord injury induces nuclear factor-kappaB activation. J. Neurosci. 1998, 18:3251-3260.
23. Bhatt D.H., Otto S.J., Depoister B., Fetcho J.R. Cyclic AMP-induced repair of zebrafish spinal circuits. Science 2004, 305:254-258.
24. Bhatt D.H., Patzelova H., McLean D.L., Fetcho J.R., Zottoli S.J. Functional regeneration in the larval zebrafish spinal cord. Model Organisms in Spinal Cord Regeneration 2007, 263-288. WILEY-VCH Verlag GmbH & Co. KgaA, Weihnheim. C.G. Becker, T. Becker (Eds.).
25. Boehm T. Design principles of adaptive immune systems. Nat. Rev. Immunol. 2011, 11:307-317.
26. Bradbury E.J., Carter L.M. Manipulating the glial scar: chondroitinase ABC as a therapy for spinal cord injury. Brain. Res. Bull. 2011, 84:306-316.
27. Bradbury E.J., Moon L.D., Popat R.J., King V.R., Bennett G.S., Patel P.N., Fawcett J.W., McMahon S.B. Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature 2002, 416:636-640.
28. Brambilla R., Bracchi-Ricard V., Hu W.H., Frydel B., Bramwell A., Karmally S., Green E.J., Bethea J.R. Inhibition of astroglial nuclear factor kappaB reduces inflammation and improves functional recovery after spinal cord injury. J. Exp. Med. 2005, 202:145-156.
29. Buchli A.D., Schwab M.E. Inhibition of Nogo: a key strategy to increase regeneration, plasticity and functional recovery of the lesioned central nervous system. Ann. Med. 2005, 37:556-567.
30. Busch D.J., Morgan J.R. Synuclein accumulation is associated with cell-specific neuronal death after spinal cord injury. J. Comp. Neurol. 2012, 520:1751-1771.
31. Cannon J.P., Haire R.N., Pancer Z., Mueller M.G., Skapura D., Cooper M.D., Litman G.W. Variable domains and a VpreB-like molecule are present in a jawless vertebrate. Immunogenetics 2005, 56:924-929.
32. Carlson S.L., Parrish M.E., Springer J.E., Doty K., Dossett L. Acute inflammatory response in spinal cord following impact injury. Exp. Neurol. 1998, 151:77-88.
33. Castellucci V.F., Kandel E.R., Schwartz J.H., Wilson F.D., Nairn A.C., Greengard P. Intracellular injection of t he catalytic subunit of cyclic AMP-dependent protein kinase simulates facilitation of transmitter release underlying behavioral sensitization in Aplysia. Proc. Natl. Acad. Sci. U. S. A. 1980, 77:7492-7496.
34. Chen Z., Lee H., Henle S.J., Cheever T.R., Ekker S.C., Henley J.R. Primary neuron culture for nerve growth and axon guidance studies in zebrafish (Danio rerio). PLoS One 2013, 8:e57539.
35. Cline H.T., Kelly D. Xenopus as an experimental system for developmental neuroscience: introduction to a special issue. Dev. Neurobiol. 2012, 72:463-464.
36. Cohen S., Levi-Montalcini R., Hamburger V. A nerve growth-stimulating factor isolated from Sarcom as 37 and 180. Proc. Natl. Acad. Sci. U. S. A. 1954, 40:1014-1018.
37. Cohen A.H., Mackler S.A., Selzer M.E. Functional regeneration following spinal transection demonstrated in the isolated spinal cord of the larval sea lamprey. Proc. Natl. Acad. Sci. U. S. A. 1986, 83:2763-2766.
38. Cohen A.H., Mackler S.A., Selzer M.E. Behavioral recovery following spinal transection: functional regeneration in the lamprey CNS. Trends Neurosci. 1988, 11:227-231.
39. Cohen A.H., Baker M.T., Dobrov T.A. Evidence for functional regeneration in the adult lamprey spinal cord following transection. Brain Res. 1989, 496:368-372.
40. Cohen A.H., Kiemel T., Pate V., Blinder J., Guan L. Temperature can alter the function outcome of spinal cord regeneration in larval lampreys. Neuroscience 1999, 90:957-965.
41. Corriveau R.A., Huh G.S., Shatz C.J. Regulation of class I MHC gene expression in the developing and mature CNS by neural activity. Neuron 1998, 21:505-520.
42. Das S., Hirano M., Aghaallaei N., Bajoghli B., Boehm T., Cooper M.D. Organization of lamprey variable lymphocyte receptor C locus and repertoire development. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:6043-6048.
43. David S., Kroner A. Repertoire of microglial and macrophage responses after spinal cord injury. Nat. Rev. Neurosci. 2011, 12:388-399.
44. Davies A.L., Hayes K.C., Dekaban G.A. Clinical correlates of elevated serum concentrations of cytokines and autoantibodies in patients with spinal cord injury. Arch. Phys. Med. Rehabil. 2007, 88:1384-1393.
45. Davis B.M., Ayers J.L., Koran L., Carlson J., Anderson M.C., Simpson S.B. Time course of salamander spinal cord regeneration and recovery of swimming: HRP retrograde pathway tracing and kinematic analysis. Exp. Neurol. 1990, 108:198-213.
46. DetloffM.R., Fisher L.C., McGaughy V., Longbrake E.E., Popovich P.G., Basso D.M. Remote activation of microglia and pro-inflammatory cytokines predict the onset and severity of below-level neuropathic pain after spinal cord injury in rats. Exp. Neurol. 2008, 212:337-347.
47. Dinarello C.A., Simon A., van der Meer J.W. Treating inflammation by blocking interleukin-1 in a broad spectrum of diseases. Nat. Rev. Drug Discov. 2012, 11:633-652.
48. Donnelly D.J., Longbrake E.E., Shawler T.M., Kigerl K.A., Lai W., Tovar C.A., RansohoffR.M., Popovich P.G. Deficient CX3CR1 signaling promotes recovery after mouse spinal cord injury by limiting the recruitment and activation of Ly6Clo/iNOS+ macrophages. J. Neurosci. 2011, 31:9910-9922.
49. Ellett F., Pase L., Hayman J.W., Andrianopoulos A., Lieschke G.J. mpeg1 promoter transgenes direct macrophage-lineage expression in zebrafish. Blood 2010, 117:e49-e56.
50. Elmer B.M., McAllister A.K. Major histocompatibility complex class I proteins in brain development and plasticity. Trends Neurosci. 2012, 35:660-670.
51. Fang P., Pan H.C., Lin S.L., Zhang W.Q., Rauvala H., Schachner M., Shen Y.Q. HMGB1 Contributes to Regeneration After Spinal Cord Injury in Adult Zebrafish 2013, Mol. Neurobiol, (in press).
52. Fatt P., Katz B. An analysis of the end-plate potential recorded with an intracellular electrode. J. Physiol. 1951, 115:320-370.
53. Filbin M.T. Myelin-associated inhibitors of axonal regeneration in the adult mammalian CNS. Nat. Rev. Neurosci. 2003, 4:703-713.
54. Fitch M.T., Silver J. Activated macrophages and the blood-brain barrier: inflammation after CNS injury leads to increases in putative inhibitory molecules. Exp. Neurol. 1997, 148:587-603.
55. Fitch M.T., Doller C., Combs C.K., Landreth G.E., Silver J. Cellular and molecular mechanisms of glial scarring and progressive cavitation: in vivo and in vitro analysis of inflammation-induced secondary injury after CNS trauma. J. Neurosci. 1999, 19:8182-8198.
56. Fleming J.C., Norenberg M.D., Ramsay D.A., Dekaban G.A., Marcillo A.E., Saenz A.D., Pasquale-Styles M., Dietrich W.D., Weaver L.C. The cellular inflammatory response in human spinal cords after injury. Brain 2006, 129:3249-3269.
57. Fukazawa T., Naora Y., Kunieda T., Kubo T. Suppression of the immune response potentiates tadpole tail regeneration during the refractory period. Development 2009, 136:2323-2327.
58. Garcia G., Libisch G., Trujillo-Cenoz O., Robello C., Russo R.E. Modulation of gene expression during early stages of reconnection of the turtle spinal cord. J. Neurochem. 2012, 121:996-1006.
59. Garcia-Alias G., Barkhuysen S., Buckle M., Fawcett J.W. Chondroitinase ABC treatment opens a window of opportunity for task-specific rehabilitation. Nat. Neurosci. 2009, 12:1145-1151.
60. Gemberling M., Bailey T.J., Hyde D.R., Poss K.D. The zebrafish as a model for complex tissue regeneration. Trends Genet. 2013, 29:611-620.
61. Genovese T., Mazzon E., Crisafulli C., Di Paola R., Muia C., Bramanti P., Cuzzocrea S. Immunomodulatory effects of etanercept in an experimental model of spinal cord injury. J. Pharmacol. Exp. Ther. 2006, 316:1006-1016.
62. Genovese T., Mazzon E., Crisafulli C., Di Paola R., Muia C., Esposito E., Bramanti P., Cuzzocrea S. TNF-alpha blockage in a mouse model of SCI: evidence for improved outcome. Shock 2008, 29:32-41.
63. Genovese T., Mazzon E., Esposito E., Di Paola R., Caminiti R., Meli R., Bramanti P., Cuzzocrea S. Effect of thalidomide on signal transduction pathways and secondary damage in experimental spinal cord trauma. Shock 2008, 30:231-240.
64. Gensel J.C., Donnelly D.J., Popovich P.G. Spinal cord injury therapies in humans: an overview of current clinical trials and their potential effects on intrinsic CNS macrophages. Expert Opin. Ther. Targets 2011, 15:505-518.
65. Gensel J.C., Kigerl K.A., Mandrekar-Colucci S.S., Gaudet A.D., Popovich P.G. Achieving CNS axon regeneration by manipulating convergent neuro-immune signaling. Cell Tissue Res. 2012, 349:201-213.
66. Gibbs K.M., Szaro B.G. Regeneration of descending projections in Xenopus laevis tadpole spinal cord demonstrated by retrograde double labeling. Brain Res. 2006, 1088:68-72.
67. Gibbs K.M., Chittur S.V., Szaro B.G. Metamorphosis and the regenerative capacity of spinal cord axons in Xenopus laevis. Eur. J. Neurosci. 2011, 33:9-25.
68. Giger R.J., Hollis E.R., Tuszynski M.H. Guidance molecules in axon regeneration. Cold Spring Harb. Perspect. Biol. 2010, 2:a001867.
69. Ginhoux F., Lim S., Hoeffel G., Low D., Huber T. Origin and differentiation of microglia. Front. Cell. Neurosci. 2013, 7:45.
70. Godwin J.W., Pinto A.R., Rosenthal N.A. Macrophages are required for adult salamander limb regeneration. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:9415-9420.
71. Goldshmit Y., Matteo R., Sztal T., Ellett F., Frisca F., Moreno K., Crombie D., Lieschke G.J., Currie P.D., Sabbadini R.A., Pebay A. Blockage of lysophosphatidic acid signaling improves spinal cord injury outcomes. Am. J. Pathol. 2012, 181:978-992.
72. Goldshmit Y., Sztal T.E., Jusuf P.R., Hall T.E., Nguyen-Chi M., Currie P.D. Fgf-dependent glial cell bridges facilitate spinal cord regeneration in zebrafish. J. Neurosci. 2012, 32:7477-7492.
73. Gonzenbach R.R., Schwab M.E. Disinhibition of neurite growth to repair the injured adult CNS: focusing on Nogo. Cell. Mol. Life Sci. 2008, 65:161-176.
74. Goodbrand I.A., Gaze R.M. Microglia in tadpoles of Xenopus laevis: normal distribution and the response to optic nerve injury. Anat. Embryol. (Berl) 1991, 184:71-82.
75. Goritz C., Dias D.O., Tomilin N., Barbacid M., Shupliakov O., Frisen J. A pericyte origin of spinal cord scar tissue. Science 2011, 333:238-242.
76. Grillner S., Jessell T.M. Measured motion: searching for simplicity in spinal locomotor networks. Curr. Opin. Neurobiol. 2009, 19:572-586.
77. Guo P., Hirano M., Herrin B.R., Li J., Yu C., Sadlonova A., Cooper M.D. Dual nature of the adaptive immune system in lampreys. Nature 2009, 459:796-801.
78. Guth L., Brewer C.R., Collins W.F., Goldberger M.E., Perl E.R. Criteria for evaluating spinal cord regeneration experiments. Surg. Neurol. 1980, 14:392.
79. Harty M., NeffA.W., King M.W., Mescher A.L. Regeneration or scarring: an immunologic perspective. Dev. Dyn. 2003, 226:268-279.
80. Hayes K.C., Hull T.C., Delaney G.A., Potter P.J., Sequeira K.A., Campbell K., Popovich P.G. Elevated serum titers of proinflammatory cytokines and CNS autoantibodies in patients with chronic spinal cord injury. J. Neurotrauma 2002, 19:753-761.
81. Herbomel P., Thisse B., Thisse C. Zebrafish early macrophages colonize cephalic mesenchyme and developing brain, retina, and epidermis through a M-CSF receptor-dependent invasive process. Dev. Biol. 2001, 238:274-288.
82. Herrmann J.E., Imura T., Song B., Qi J., Ao Y., Nguyen T.K., Korsak R.A., Takeda K., Akira S., Sofroniew M.V. STAT3 is a critical regulator of astrogliosis and scar formation after spinal cord injury. J. Neurosci. 2008, 28:7231-7243.
83. Hirano M., Guo P., McCurley N., Schorpp M., Das S., Boehm T., Cooper M.D. Evolutionary implications of a third lymphocyte lineage in lampreys. Nature 2013, 501:435-438.
84. Hodgkin A.L., Huxley A.F. Action potentials recorded from inside a nerve fiber. Nature 1939, 144:710-711.
85. Horn K.P., Busch S.A., Hawthorne A.L., van Rooijen N., Silver J. Another barrier to regeneration in the CNS: activated macrophages induce extensive retraction of dystrophic axons through direct physical interactions. J. Neurosci. 2008, 28:9330-9341.
86. Howe K., Clark M.D., Torroja C.F., Torrance J., Berthelot C., Muffato M., Collins J.E., Humphray S., McLaren K., Matthews L., McLaren S., Sealy I., Caccamo M., Churcher C., Scott C., Barrett J.C., Koch R., Rauch G.J., White S., Chow W., Kilian B., Quintais L.T., Guerra-Assuncao J.A., Zhou Y., Gu Y., Yen J., Vogel J.H., Eyre T., Redmond S., Banerjee R., Chi J., Fu B., Langley E., Maguire S.F., Laird G.K., Lloyd D., Kenyon E., Donaldson S., Sehra H., Almeida-King J., Loveland J., Trevanion S., Jones M., Quail M., Willey D., Hunt A., Burton J., Sims S., McLay K., Plumb B., Davis J., Clee C., Oliver K., Clark R., Riddle C., Eliott D., Threadgold G., Harden G., Ware D., Mortimer B., Kerry G., Heath P., Phillimore B., Tracey A., Corby N., Dunn M., Johnson C., Wood J., Clark S., Pelan S., Griffiths G., Smith M., Glithero R., Howden P., Barker N., Stevens C., Harley J., Holt K., Panagiotidis G., Lovell J., Beasley H., Henderson C., Gordon D., Auger K., Wright D., Collins J., Raisen C., Dyer L., Leung K., Robertson L., Ambridge K., Leongamornlert D., McGuire S., Gilderthorp R., Griffiths C., Manthravadi D., Nichol S., Barker G., Whitehead S., Kay M., Brown J., Murnane C., Gray E., Humphries M., Sycamore N., Barker D., Saunders D., Wallis J., Babbage A., Hammond S., Mashreghi-Mohammadi M., Barr L., Martin S., Wray P., Ellington A., Matthews N., Ellwood M., Woodmansey R., Clark G., Cooper J., Tromans A., Grafham D., Skuce C., Pandian R., Andrews R., Harrison E., Kimberley A., Garnett J., Fosker N., Hall R., Garner P., Kelly D., Bird C., Palmer S., Gehring I., Berger A., Dooley C.M., Ersan-Urun Z., Eser C., Geiger H., Geisler M., Karotki L., Kirn A., Konantz J., Konantz M., Oberlander M., Rudolph-Geiger S., Teucke M., Osoegawa K., Zhu B., Rapp A., Widaa S., Langford C., Yang F., Carter N.P., Harrow J., Ning Z., Herrero J., Searle S.M., Enright A., Geisler R., Plasterk R.H., Lee C., Westerfield M., de Jong P.J., Zon L.I., Postlethwait J.H., Nusslein-Volhard C., Hubbard T.J., Roest Crollius H., Rogers J., Stemple D.L. The zebrafish reference genome sequence and its relationship to the human genome. Nature 2013, 496:498-503.
87. Hu J., Zhang K.G., Selzer M.E. Effects of chondroitinase on regeneration and survival of axotomized spinal-projecting neurons in the lamprey. Neuroscience Meeting Planner online 2013.
88. Hui S.P., Dutta A., Ghosh S. Cellular response after crush injury in adult zebrafish spinal cord. Dev. Dyn. 2010, 239:2962-2979.
89. Hui S.P., Monaghan J.R., Voss S.R., Ghosh S. Expression pattern of Nogo-A, MAG, and NgR in regenerating urodele spinal cord. Dev. Dyn. 2013, 242:847-860.
90. Ihrie R.A., Alvarez-Buylla A. Lake-front property: a unique germinal niche by the lateral ventricles of the adult brain. Neuron 2011, 70:674-686.
91. Jacobs A.J., Swain G.P., Snedeker J.A., Pijak D.S., Gladstone L.J., Selzer M.E. Recovery of neurofilament expression selectively in regenerating reticulospinal neurons. J. Neurosci. 1997, 17:5206-5220.
92. Jin L.Q., Zhang G., Jamison C., Takano H., Haydon P.G., Selzer M.E. Axon regeneration in the absence of growth cones: acceleration by cyclic AMP. J. Comp. Neurol. 2009, 515:295-312.
93. Kanyilmaz S., Hepguler S., Atamaz F.C., Gokmen N.M., Ardeniz O., Sin A. Phagocytic and oxidative burst activity of neutrophils in patients with spinal cord injury. Arch. Phys. Med. Rehabil. 2012, 94:369-374.
94. Kasamatsu J., Sutoh Y., Fugo K., Otsuka N., Iwabuchi K., Kasahara M. Identification of a third variable lymphocyte receptor in the lamprey. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:14304-14308.
95. Khalturin K., Panzer Z., Cooper M.D., Bosch T.C. Recognition strategies in the innate immune system of ancestral chordates. Mol. Immunol. 2004, 41:1077-1087.
96. Kigerl K.A., Popovich P.G. Toll-like receptors in spinal cord injury. Curr. Top. Microbiol. Immunol. 2009, 336:121-136.
97. Kimura Y., Madhavan M., Call M.K., Santiago W., Tsonis P.A., Lambris J.D., Del Rio-Tsonis K. Expression of complement 3 and complement 5 in newt limb and lens regeneration. J. Immunol. 2003, 170:2331-2339.
98. Kirkham M., Berg D.A., Simon A. Microglia activation during neuroregeneration in the adult vertebrate brain. Neurosci. Lett. 2011, 497:11-16.
99. Kizil C., Dudczig S., Kyritsis N., Machate A., Blaesche J., Kroehne V., Brand M. The chemokine receptor cxcr5 regulates the regenerative neurogenesis response in the adult zebrafish brain. Neural Dev. 2012, 7:27.
100. Kizil C., Kyritsis N., Dudczig S., Kroehne V., Freudenreich D., Kaslin J., Brand M. Regenerative neurogenesis from neural progenitor cells requires injury-induced expression of Gata3. Dev. Cell 2012, 23:1230-1237.
101. Klusman I., Schwab M.E. Effects of pro-inflammatory cytokines in experimental spinal cord injury. Brain Res. 1997, 762:173-184.
102. Kopf M., Bachmann M.F., Marsland B.J. Averting inflammation by targeting the cytokine environment. Nat. Rev. Drug Discov. 2010, 9:703-718.
103. Kupfermann I., Kandel E.R. Neuronal controls of a behavioral response mediated by the abdominal ganglion of Aplysia. Science 1969, 164:847-850.
104. Kwon B.K., Casha S., Hurlbert R.J., Yong V.W. Inflammatory and structural biomarkers in acute traumatic spinal cord injury. Clin. Chem. Lab. Med. 2010, 49:425-433.
105. Kyritsis N., Kizil C., Zocher S., Kroehne V., Kaslin J., Freudenreich D., Iltzsche A., Brand M. Acute inflammation initiates the regenerative response in the adult zebrafish brain. Science 2012, 338:1353-1356.
106. Kyritsis N., Kizil C., Brand M. Neuroinflammation and central nervous system regeneration in vertebrates. Trends Cell Biol. 2014, 24(2):128-135. (Electronic publication ahead of print 2013 Sep 9). 10.1016/j.tcb.2013.08.004.
107. Laramore C., Maymind E., Shifman M.I. Expression of neurotrophin and its tropomyosin-related kinase receptors (Trks) during axonal regeneration following spinal cord injury in larval lamprey. Neuroscience 2011, 183:265-277.
108. Lau B.Y., Fogerson S.M., Walsh R.B., Morgan J.R. Cyclic AMP promotes axon regeneration, lesion repair and neuronal survival in lampreys after spinal cord injury. Exp. Neurol. 2013, 250:31-42.
109. Li Y., Du X.F., Liu C.S., Wen Z.L., Du J.L. Reciprocal regulation between resting microglial dynamics and neuronal activity in vivo. Dev. Cell 2012, 23:1189-1202.
110. Lieschke G.J., Currie P.D. Animal models of human disease: zebrafish swim into view. Nat. Rev. Genet. 2007, 8:353-367.
111. Lin G., Chen Y., Slack J.M. Imparting regenerative capacity to limbs by progenitor cell transplantation. Dev. Cell 2012, 24:41-51.
112. Lin G., Chen Y., Slack J.M. Transgenic analysis of signaling pathways required for Xenopus tadpole spinal cord and muscle regeneration. Anat. Rec. (Hoboken) 2012, 295:1532-1540.
113. Love N.R., Chen Y., Bonev B., Gilchrist M.J., Fairclough L., Lea R., Mohun T.J., Paredes R., Zeef L.A., Amaya E. Genome-wide analysis of gene expression during Xenopus tropicalis tadpole tail regeneration. BMC Dev. Biol. 2011, 11:70.
114. Love N.R., Chen Y., Ishibashi S., Kritsiligkou P., Lea R., Koh Y., Gallop J.L., Dorey K., Amaya E. Amputation-induced reactive oxygen species are required for successful Xenopus tadpole tail regeneration. Nat. Cell Biol. 2013, 15:222-228.
115. Lu P., Wang Y., Graham L., McHale K., Gao M., Wu D., Brock J., Blesch A., Rosenzweig E.S., Havton L.A., Zheng B., Conner J.M., Marsala M., Tuszynski M.H. Long-distance growth and connectivity of neural stem cells after severe spinal cord injury. Cell 2012, 150:1264-1273.
116. Lurie D.I., Selzer M.E. The need for cellular elements during axonal regeneration in the sea lamprey spinal cord. Exp. Neurol. 1991, 112:64-71.
117. Lurie D.I., Selzer M.E. Preferential regeneration of spinal axons through the scar in hemisected lamprey spinal cord. J. Comp. Neurol. 1991, 313:669-679.
118. Lurie D.I., Pijak D.S., Selzer M.E. Structure of reticulospinal axon growth cones and their cellular environment during regeneration in the lamprey spinal cord. J. Comp. Neurol. 1994, 344:559-580.
119. Marder E. Non-mammalian models for studying neural development and function. Nature 2002, 417:318-321.
120. Marz M., Schmidt R., Rastegar S., Strahle U. Regenerative response following stab injury in the adult zebrafish telencephalon. Dev. Dyn. 2011, 240:2221-2231.
121. Mayer W.E., Uinuk-Ool T., Tichy H., Gartland L.A., Klein J., Cooper M.D. Isolation and characterization of lymphocyte-like cells from a lamprey. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:14350-14355.
122. Medicine C.f. S.C. Early acute management in adults with spinal cord injury: a Clinical Practice Guideline for health-care providers. Clinical Practice Guidelines 2013, Paralyzed Veterans of America, Washington, DC.
123. Mescher A.L., NeffA.W. Regenerative capacity and the developing immune system. Adv. Biochem. Eng. Biotechnol. 2005, 93:39-66.
124. Mescher A.L., NeffA.W. Limb regeneration in amphibians: immunological considerations. ScientificWorldJournal 2006, 6(Suppl. 1):1-11.
125. Mescher A.L., Wolf W.L., Moseman E.A., Hartman B., Harrison C., Nguyen E., NeffA.W. Cells of cutaneous immunity in Xenopus: studies during larval development and limb regeneration. Dev. Comp. Immunol. 2007, 31:383-393.
126. Monaghan J.R., Walker J.A., Page R.B., Putta S., Beachy C.K., Voss S.R. Early gene expression during natural spinal cord regeneration in the salamander Ambystoma mexicanum. J. Neurochem. 2007, 101:27-40.
127. Murphy K., Travers P., Walport M. Janeway's Immunobiology 2008, Garland, New York. 7th ed.
128. Najakshin A.M., Mechetina L.V., Alabyev B.Y., Taranin A.V. Identification of an IL-8 homolog in lamprey (Lampetra fluviatilis): early evolutionary divergence of chemokines. Eur. J. Immunol. 1999, 29:375-382.
129. Okada S., Nakamura M., Katoh H., Miyao T., Shimazaki T., Ishii K., Yamane J., Yoshimura A., Iwamoto Y., Toyama Y., Okano H. Conditional ablation of Stat3 or Socs3 discloses a dual role for reactive astrocytes after spinal cord injury. Nat. Med. 2006, 12:829-834.
130. Olofsson P.S., Rosas-Ballina M., Levine Y.A., Tracey K.J. Rethinking inflammation: neural circuits in the regulation of immunity. Immunol. Rev. 2012, 248:188-204.
131. Page D.M., Wittamer V., Bertrand J.Y., Lewis K.L., Pratt D.N., Delgado N., Schale S.E., McGue C., Jacobsen B.H., Doty A., Pao Y., Yang H., Chi N.C., Magor B.G., Traver D. An evolutionarily conserved program of B-cell development and activation in zebrafish. Blood 2013, 122:e1-e11.
132. Pancer Z., Amemiya C.T., Ehrhardt G.R., Ceitlin J., Gartland G.L., Cooper M.D. Somatic diversification of variable lymphocyte receptors in the agnathan sea lamprey. Nature 2004, 430:174-180.
133. Peri F., Nusslein-Volhard C. Live imaging of neuronal degradation by microglia reveals a role for v0-ATPase a1 in phagosomal fusion in vivo. Cell 2008, 133:916-927.
134. Pernet V., Schwab M.E. The role of Nogo-A in axonal plasticity, regrowth and repair. Cell Tissue Res. 2012, 349:97-104.
135. Peterson S.L., Anderson A.J. Complement and spinal cord injury: Traditional and non-traditional aspects of complement cascade function in the injured spinal cord microenvironment. Exp. Neurol. 2014, 258:35-47. (in this issue).
136. Popovich P.G., Hickey W.F. Bone marrow chimeric rats reveal the unique distribution of resident and recruited macrophages in the contused rat spinal cord. J. Neuropathol. Exp. Neurol. 2001, 60:676-685.
137. Popovich P.G., Streit W.J., Stokes B.T. Differential expression of MHC class II antigen in the contused rat spinal cord. J. Neurotrauma 1993, 10:37-46.
138. Popovich P.G., Wei P., Stokes B.T. Cellular inflammatory response after spinal cord injury in Sprague-Dawley and Lewis rats. J. Comp. Neurol. 1997, 377:443-464.
139. Popovich P.G., Guan Z., McGaughy V., Fisher L., Hickey W.F., Basso D.M. The neuropathological and behavioral consequences of intraspinal microglial/macrophage activation. J. Neuropathol. Exp. Neurol. 2002, 61:623-633.
140. Popovich P.G., van Rooijen N., Hickey W.F., Preidis G., McGaughy V. Hematogenous macrophages express CD8 and distribute to regions of lesion cavitation after spinal cord injury. Exp. Neurol. 2003, 182:275-287.
141. Pratt K.G., Khakhalin A.S. Modeling human neurodevelopmental disorders in the Xenopus tadpole: from mechanisms to therapeutic targets. Dis. Model. Mech. 2013, 6:1057-1065.
142. Rao N., Jhamb D., Milner D.J., Li B., Song F., Wang M., Voss S.R., Palakal M., King M.W., Saranjami B., Nye H.L., Cameron J.A., Stocum D.L. Proteomic analysis of blastema formation in regenerating axolotl limbs. BMC Biol. 2009, 7:83.
143. Rehermann M.I., Marichal N., Russo R.E., Trujillo-Cenoz O. Neural reconnection in the transected spinal cord of the freshwater turtle Trachemys dorbignyi. J. Comp. Neurol. 2009, 515:197-214.
144. Rehermann M.I., Santinaque F.F., Lopez-Carro B., Russo R.E., Trujillo-Cenoz O. Cell proliferation and cytoarchitectural remodeling during spinal cord reconnection in the fresh-water turtle Trachemys dorbignyi. Cell Tissue Res. 2011, 344:415-433.
145. Reimer M.M., Sorensen I., Kuscha V., Frank R.E., Liu C., Becker C.G., Becker T. Motor neuron regeneration in adult zebrafish. J. Neurosci. 2008, 28:8510-8516.
146. Reimer M.M., Kuscha V., Wyatt C., Sorensen I., Frank R.E., Knuwer M., Becker T., Becker C.G. Sonic hedgehog is a polarized signal for motor neuron regeneration in adult zebrafish. J. Neurosci. 2009, 29:15073-15082.
147. Reimer M.M., Norris A., Ohnmacht J., Patani R., Zhong Z., Dias T.B., Kuscha V., Scott A.L., Chen Y.C., Rozov S., Frazer S.L., Wyatt C., Higashijima S., Patton E.E., Panula P., Chandran S., Becker T., Becker C.G. Dopamine from the brain promotes spinal motor neuron generation during development and adult regeneration. Dev. Cell 2013, 25:478-491.
148. Renshaw S.A., Trede N.S. A model 450millionyears in the making: zebrafish and vertebrate immunity. Dis. Model. Mech. 2012, 5:38-47.
149. Renshaw S.A., Loynes C.A., Trushell D.M., Elworthy S., Ingham P.W., Whyte M.K. A transgenic zebrafish model of neutrophilic inflammation. Blood 2006, 108:3976-3978.
150. Rovainen C.M. Physiological and anatomical studies on large neurons of central nervous system of the sea lamprey (Petromyzon marinus). II. Dorsal cells and giant interneurons. J. Neurophysiol. 1967, 30:1024-1042.
151. Rovainen C.M. Regeneration of Muller and Mauthner axons after spinal transection in larval lampreys. J. Comp. Neurol. 1976, 168:545-554.
152. Rudge J.S., Silver J. Inhibition of neurite outgrowth on astroglial scars in vitro. J. Neurosci. 1990, 10:3594-3603.
153. Rudge J.S., Smith G.M., Silver J. An in vitro model of wound healing in the CNS: analysis of cell reaction and interaction at different ages. Exp. Neurol. 1989, 103:1-16.
154. Sabelstrom H., Stenudd M., Reu P., Dias D.O., Elfineh M., Zdunek S., Damberg P., Goritz C., Frisen J. Resident neural stem cells restrict tissue damage and neuronal loss after spinal cord injury in mice. Science 2013, 342:637-640.
155. Sato A., Uinuk-ool T.S., Kuroda N., Mayer W.E., Takezaki N., Dongak R., Figueroa F., Cooper M.D., Klein J. Macrophage migration inhibitory factor (MIF) of jawed and jawless fishes: implications for its evolutionary origin. Dev. Comp. Immunol. 2003, 27:401-412.
156. Schnell L., Schneider R., Berman M.A., Perry V.H., Schwab M.E. Lymphocyte recruitment following spinal cord injury in mice is altered by prior viral exposure. Eur. J. Neurosci. 1997, 9:1000-1007.
157. Schnell L., Fearn S., Schwab M.E., Perry V.H., Anthony D.C. Cytokine-induced acute inflammation in the brain and spinal cord. J. Neuropathol. Exp. Neurol. 1999, 58:245-254.
158. Selzer M.E. Mechanisms of functional recovery and regeneration after spinal cord transection in larval sea lamprey. J. Physiol. 1978, 277:395-408.
159. Shechter R., Schwartz M. Harnessing monocyte-derived macrophages to control central nervous system pathologies: no longer 'if' but 'how'. J. Pathol. 2013, 229:332-346.
160. Shifman M.I., Selzer M.E. Differential expression of class 3 and 4 semaphorins and netrin in the lamprey spinal cord during regeneration. J. Comp. Neurol. 2007, 501:631-646.
161. Shifman M.I., Zhang G., Selzer M.E. Delayed death of identified reticulospinal neurons after spinal cord injury in lampreys. J. Comp. Neurol. 2008, 510:269-282.
162. Shifman M.I., Yumul R.E., Laramore C., Selzer M.E. Expression of the repulsive guidance molecule RGM and its receptor neogenin after spinal cord injury in sea lamprey. Exp. Neurol. 2009, 217:242-251.
163. Sieger D., Moritz C., Ziegenhals T., Prykhozhij S., Peri F. Long-range Ca2+ waves transmit brain-damage signals to microglia. Dev. Cell 2012, 22:1138-1148.
164. Silver J., Miller J.H. Regeneration beyond the glial scar. Nat. Rev. Neurosci. 2004, 5:146-156.
165. Slack J.M., Lin G., Chen Y. The Xenopus tadpole: a new model for regeneration research. Cell. Mol. Life Sci. 2008, 65:54-63.
166. Smith G.M., Miller R.H., Silver J. Changing role of forebrain astrocytes during development, regenerative failure, and induced regeneration upon transplantation. J. Comp. Neurol. 1986, 251:23-43.
167. Smith G.M., Rutishauser U., Silver J., Miller R.H. Maturation of astrocytes in vitro alters the extent and molecular basis of neurite outgrowth. Dev. Biol. 1990, 138:377-390.
168. Smith J., Morgan J.R., Zottoli S.J., Smith P.J., Buxbaum J.D., Bloom O. Regeneration in the era of functional genomics and gene network analysis. Biol. Bull. 2011, 221:18-34.
169. Smith J.J., Kuraku S., Holt C., Sauka-Spengler T., Jiang N., Campbell M.S., Yandell M.D., Manousaki T., Meyer A., Bloom O.E., Morgan J.R., Buxbaum J.D., Sachidanandam R., Sims C., Garruss A.S., Cook M., Krumlauf R., Wiedemann L.M., Sower S.A., Decatur W.A., Hall J.A., Amemiya C.T., Saha N.R., Buckley K.M., Rast J.P., Das S., Hirano M., McCurley N., Guo P., Rohner N., Tabin C.J., Piccinelli P., Elgar G., Ruffier M., Aken B.L., Searle S.M., Muffato M., Pignatelli M., Herrero J., Jones M., Brown C.T., Chung-Davidson Y.W., Nanlohy K.G., Libants S.V., Yeh C.Y., McCauley D.W., Langeland J.A., Pancer Z., Fritzsch B., de Jong P.J., Zhu B., Fulton L.L., Theising B., Flicek P., Bronner M.E., Warren W.C., Clifton S.W., Wilson R.K., Li W. Sequencing of the sea lamprey (Petromyzon marinus) genome provides insights into vertebrate evolution. Nat. Genet. 2013, 45:415-421. (421e411-412).
170. Snow D.M., Lemmon V., Carrino D.A., Caplan A.I., Silver J. Sulfated proteoglycans in astroglial barriers inhibit neurite outgrowth in vitro. Exp. Neurol. 1990, 109:111-130.
171. Spitzbarth I., Bock P., Haist V., Stein V.M., Tipold A., Wewetzer K., Baumgartner W., Beineke A. Prominent microglial activation in the early proinflammatory immune response in naturally occurring canine spinal cord injury. J. Neuropathol. Exp. Neurol. 2011, 70:703-714.
172. Stein A., Panjwani A., Sison C., Rosen L., Chugh R., Metz C., Bank M., Bloom O. Pilot study: elevated circulating levels of the proinflammatory cytokine macrophage migration inhibitory factor in patients with chronic spinal cord injury. Arch. Phys. Med. Rehabil. 2013, 94:1498-1507.
173. Stephan A.H., Barres B.A., Stevens B. The complement system: an unexpected role in synaptic pruning during development and disease. Annu. Rev. Neurosci. 2012, 35:369-389.
174. Stevens B., Allen N.J., Vazquez L.E., Howell G.R., Christopherson K.S., Nouri N., Micheva K.D., Mehalow A.K., Huberman A.D., Stafford B., Sher A., Litke A.M., Lambris J.D., Smith S.J., John S.W., Barres B.A. The classical complement cascade mediates CNS synapse elimination. Cell 2007, 131:1164-1178.
175. Stewart R., Rascon C.A., Tian S., Nie J., Barry C., Chu L.F., Ardalani H., Wagner R.J., Probasco M.D., Bolin J.M., Leng N., Sengupta S., Volkmer M., Habermann B., Tanaka E.M., Thomson J.A., Dewey C.N. Comparative RNA-seq analysis in the unsequenced axolotl: the oncogene burst highlights early gene expression in the blastema. PLoS Comput. Biol. 2013, 9:e1002936.
176. Streit W.J., Semple-Rowland S.L., Hurley S.D., Miller R.C., Popovich P.G., Stokes B.T. Cytokine mRNA profiles in contused spinal cord and axotomized facial nucleus suggest a beneficial role for inflammation and gliosis. Exp. Neurol. 1998, 152:74-87.
177. Sunyer J.O. Fishing for mammalian paradigms in the teleost immune system. Nat. Immunol. 2013, 14:320-326.
178. Svahn A.J., Graeber M.B., Ellett F., Lieschke G.J., Rinkwitz S., Bennett M.R., Becker T.S. Development of ramified microglia from early macrophages in the zebrafish optic tectum. Dev. Neurobiol. 2012, 73:60-71.
179. Tanaka E.M., Ferretti P. Considering the evolution of regeneration in the central nervous system. Nat. Rev. Neurosci. 2009, 10:713-723.
180. Tazaki A., Kitayama A., Terasaka C., Watanabe K., Ueno N., Mochii M. Macroarray-based analysis of tail regeneration in Xenopus laevis larvae. Dev. Dyn. 2005, 233:1394-1404.
181. Thuret S., Moon L.D., Gage F.H. Therapeutic interventions after spinal cord injury. Nat. Rev. Neurosci. 2006, 7:628-643.
182. Tsutsui S., Nakamura O., Watanabe T. Lamprey (Lethenteron japonicum) IL-17 upregulated by LPS-stimulation in the skin cells. Immunogenetics 2007, 59:873-882.
183. Uinuk-Ool T., Mayer W.E., Sato A., Dongak R., Cooper M.D., Klein J. Lamprey lymphocyte-like cells express homologs of genes involved in immunologically relevant activities of mammalian lymphocytes. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:14356-14361.
184. Uinuk-ool T.S., Mayer W.E., Sato A., Takezaki N., Benyon L., Cooper M.D., Klein J. Identification and characterization of a TAP-family gene in the lamprey. Immunogenetics 2003, 55:38-48.
185. Wanner I.B., Anderson M.A., Song B., Levine J., Fernandez A., Gray-Thompson Z., Ao Y., Sofroniew M.V. Glial scar borders are formed by newly proliferated, elongated astrocytes that interact to corral inflammatory and fibrotic cells via STAT3-dependent mechanisms after spinal cord injury. J. Neurosci. 2013, 33:12870-12886.
186. Wilson M.A., Gaze R.M., Goodbrand I.A., Taylor J.S. Regeneration in the Xenopus tadpole optic nerve is preceded by a massive macrophage/microglial response. Anat. Embryol. (Berl) 1992, 186:75-89.
187. Wood M.R., Cohen M.J. Synaptic regeneration in identified neurons of the lamprey spinal cords. Science 1979, 206:344-347.
188. Wood M.R., Cohen M.J. Synaptic regeneration and glial reactions in the transected spinal cord of the lamprey. J. Neurocytol. 1981, 10:57-79.
189. Yin H.S., Selzer M.E. Electrophysiologic evidence of regeneration of lamprey spinal neurons. Exp. Neurol. 1984, 83:618-628.
190. Zammit P.S., Clarke J.D., Golding J.P., Goodbrand I.A., Tonge D.A. Macrophage response during axonal regeneration in the axolotl central and peripheral nervous system. Neuroscience 1993, 54:781-789.
191. Zhang L., Palmer R., McClellan A.D. Conditioning lesions enhance axonal regeneration of descending brain neurons in spinal-cord-transected larval lamprey. J. Comp. Neurol. 2004, 478:395-404.
192. Zhang Y., Guan Z., Reader B., Shawler T., Mandrekar-Colucci S., Huang K., Weil Z., Bratasz A., Wells J., Powell N.D., Sheridan J.F., Whitacre C.C., Rabchevsky A.G., Nash M.S., Popovich P.G. Autonomic dysreflexia causes chronic immune suppression after spinal cord injury. J. Neurosci. 2013, 33:12970-12981.
193. Zhang G., Hu J., Li S., Huang L., Selzer M.E. Expression of CSPG receptors PTPsigma and LAR selectively in poorly regenerating reticulospinal neurons of lamprey 2013, J. Comp, Neurol, (press).
194. Zhang G., Pizarro I.V., Swain G.P., Kang S.H., Selzer M.E. Neurogenesis in the lamprey CNS following spinal cord transection. J Comp Neurol 2014 Apr 15, 522(6):1316-1332. 10.1002/cne.23485.
195. Zhang B., Gensel J.C. Is neuroinflammation in the injured spinal cord different than in the brain? Examining intrinsic differences between the brain and spinal cord. Exp. Neurol. 2014, 258:112-120. (in this issue).
196. Zukor K.A., Kent D.T., Odelberg S.J. Meningeal cells and glia establish a permissive environment for axon regeneration after spinal cord injury in newts. Neural Dev. 2011, 6:1.