Blockage of lysophosphatidic acid signaling improves spinal cord injury outcomes

American Journal of Pathology

Volumn 181, Issue 3, 2012, Pages 978-992

  Goldshmit, Yona ^a,b   Matteo, Rosalia ^c   Sztal, Tamar ^b   Ellett, Felix ^b   Frisca, Frisca ^d   Moreno, Kelli ^c   Crombie, Duncan ^a,e   Lieschke, Graham J ^b   Currie, Peter D ^b   Sabbadini, Roger A ^c,f   Pébay, Alice ^a,d,e  

^a O'Brien Institute   (Australia)

^b MONASH UNIVERSITY   (Australia)

^c Lpath Inc   (United States)

^d UNIVERSITY OF MELBOURNE   (Australia)

^e ROYAL VICTORIAN EYE AND EAR HOSPITAL   (Australia)

^f SAN DIEGO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

B 3 MONOCLONAL ANTIBODY; LYSOPHOSPHATIDIC ACID; MONOCLONAL ANTIBODY; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTOSIS; CELL PROLIFERATION; CONTROLLED STUDY; GLIA; GLIA CELL; HUMAN; HUMAN CELL; MALE; MICROGLIA; MOUSE; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; SPINAL CORD INJURY; ZEBRA FISH;

ANIMALS; ANTIBODIES, MONOCLONAL; APOPTOSIS; CELL DEATH; CELL PROLIFERATION; CELL SURVIVAL; CHO CELLS; CRICETINAE; DISEASE MODELS, ANIMAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; HUMANS; INFLAMMATION; LYSOPHOSPHOLIPIDS; MICE; MICROGLIA; MOTOR ACTIVITY; NEURITES; NEUROPROTECTIVE AGENTS; RECEPTORS, LYSOPHOSPHATIDIC ACID; RECOVERY OF FUNCTION; SIGNAL TRANSDUCTION; SPINAL CORD INJURIES; ZEBRAFISH;

EID: 84865204026     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2012.06.007     Document Type: Article

References (50)

1. F. Frisca, R.A. Sabbadini, Y. Goldshmit, A. Pebay Biological effects of lysophosphatidic acid in the nervous system Int Rev Cell Mol Biol 296 2012 273 322
2. M.-E. Lin, D.R. Herr, J. Chun Lysophosphatidic acid (LPA) receptors: signaling properties and disease relevance Prostaglandins Other Lipid Mediat 91 2010 130 138
3. N. Fukushima LPA in neural cell development J Cell Biochem 92 2004 993 1003
4. T. Moller, D.B. Musante, B.R. Ransom Lysophosphatidic acid-induced calcium signals in cultured rat oligodendrocytes Neuroreport 10 1999 2929 2932
5. J.A. Weiner, J. Chun Schwann cell survival mediated by the signaling phospholipid lysophosphatidic acid Proc Natl Acad Sci U S A 96 1999 5233 5238
6. J.A. Weiner, J.H. Hecht, J. Chun Lysophosphatidic acid receptor gene vzg-1/lpA1/edg-2 is expressed by mature oligodendrocytes during myelination in the postnatal murine brain J Comp neurol 398 1998 587 598
7. B. Stankoff, S. Barron, J. Allard, G. Barbin, F. Noel, M.S. Aigrot, J. Premont, P. Sokoloff, B. Zalc, C. Lubetzki Oligodendroglial expression of Edg-2 receptor: developmental analysis and pharmacological responses to lysophosphatidic acid Mol Cell Neurosci 20 2002 415 428
8. T. Frugier, D. Crombie, A. Conquest, F. Tjhong, C. Taylor, T. Kulkarni, C. McLean, A. Pebay Modulation of LPA receptor expression in the human brain following neurotrauma Cell Mol Neurobiol 31 2011 569 577
9. J.J. Contos, J. Chun The mouse lp(A3)/Edg7 lysophosphatidic acid receptor gene: genomic structure, chromosomal localization, and expression pattern Gene 267 2001 243 253
10. C.W. Lee, R. Rivera, A.E. Dubin, J. Chun LPA(4)/GPR23 is a lysophosphatidic acid (LPA) receptor utilizing G(s)- G(q)/G(i)-mediated calcium signaling and G(12/13)-mediated Rho activation J Biol Chem 282 2007 4310 4317
11. K. Kotarsky, A. Boketoft, J. Bristulf, N.E. Nilsson, A. Norberg, S. Hansson, C. Owman, R. Sillard, L.M. Leeb-Lundberg, B. Olde Lysophosphatidic acid binds to and activates GPR92, a G protein-coupled receptor highly expressed in gastrointestinal lymphocytes J Pharmacol Exp Ther 318 2006 619 628
12. K. Sato, E. Malchinkhuu, T. Muraki, K. Ishikawa, K. Hayashi, M. Tosaka, A. Mochiduki, K. Inoue, H. Tomura, C. Mogi, H. Nochi, K. Tamoto, F. Okajima Identification of autotaxin as a neurite retraction-inducing factor of PC12 cells in cerebrospinal fluid and its possible sources J Neurochem 92 2005 904 914
13. M. Narita, J. Goji, H. Nakamura, K. Sano Molecular cloning, expression, and localization of a brain-specific phosphodiesterase I/nucleotide pyrophosphatase (PD-I alpha) from rat brain J Biol Chem 269 1994 28235 28242
14. B. Fuss, H. Baba, T. Phan, V.K. Tuohy, W.B. Macklin Phosphodiesterase I, a novel adhesion molecule and/or cytokine involved in oligodendrocyte function J Neurosci 17 1997 9095 9103
15. N.E. Savaskan, L. Rocha, M.R. Kotter, A. Baer, G. Lubec, L.A. van Meeteren, Y. Kishi, J. Aoki, W.H. Moolenaar, R. Nitsch, A.U. Brauer Autotaxin (NPP-2) in the brain: cell type-specific expression and regulation during development and after neurotrauma Cell Mol Life Sci 64 2007 230 243
16. J. Dennis, L. Nogaroli, B. Fuss Phosphodiesterase-Ialpha/autotaxin (PD-Ialpha/ATX): a multifunctional protein involved in central nervous system development and disease J Neurosci Res 82 2005 737 742
17. S.D. Sorensen, O. Nicole, R.D. Peavy, L.M. Montoya, C.J. Lee, T.J. Murphy, S.F. Traynelis, J.R. Hepler Common signaling pathways link activation of murine PAR-1, LPA, and S1P receptors to proliferation of astrocytes Mol Pharmacol 64 2003 1199 1209
18. S.J. Elmes, P.J. Millns, D. Smart, D.A. Kendall, V. Chapman Evidence for biological effects of exogenous LPA on rat primary afferent and spinal cord neurons Brain Res 1022 2004 205 213
19. R. Fujita, N. Kiguchi, H. Ueda LPA-mediated demyelination in ex vivo culture of dorsal root Neurochem Int 50 2007 351 355
20. H. Ueda Molecular mechanisms of neuropathic pain-phenotypic switch and initiation mechanisms Pharmacol Ther 109 2006 57 77
21. J.N. Keller, M.R. Steiner, F.W. Holtsberg, M.P. Mattson, S.M. Steiner Lysophosphatidic acid-induced proliferation-related signals in astrocytes J Neurochem 69 1997 1073 1084
22. F.W. Holtsberg, M.R. Steiner, J.N. Keller, R.J. Mark, M.P. Mattson, S.M. Steiner Lysophosphatidic acid induces necrosis and apoptosis in hippocampal neurons J Neurochem 70 1998 66 76
23. T. Moller, J.J. Contos, D.B. Musante, J. Chun, B.R. Ransom Expression and function of lysophosphatidic acid receptors in cultured rodent microglial cells J Biol Chem 276 2001 25946 25952
24. S. Brault, F. Gobeil Jr, A. Fortier, J.C. Honore, J.S. Joyal, P.S. Sapieha, A. Kooli, E. Martin, P. Hardy, A. Ribeiro-da-Silva, K. Peri, P. Lachapelle, D. Varma, S. Chemtob Lysophosphatidic acid induces endothelial cell death by modulating the redox environment Am J Physiol 292 2007 R1174 R1183
25. Y. Goldshmit, K. Munro, S.Y. Leong, A. Pebay, A.M. Turnley LPA receptor expression in the central nervous system in health and following injury Cell Tissue Res 341 2010 23 32
26. C.G. Becker, B.C. Lieberoth, F. Morellini, J. Feldner, T. Becker, M. Schachner L1.1 is involved in spinal cord regeneration in adult zebrafish J Neurosci 24 2004 7837 7842
27. T. Becker, M.F. Wullimann, C.G. Becker, R.R. Bernhardt, M. Schachner Axonal regrowth after spinal cord transection in adult zebrafish J Comp Neurol 377 1997 577 595
28. F. Ellett, L. Pase, J.W. Hayman, A. Andrianopoulos, G.J. Lieschke mpeg1 promoter transgenes direct macrophage-lineage expression in zebrafish Blood 117 2011 e49 e56
29. S.A. Renshaw, C.A. Loynes, D.M. Trushell, S. Elworthy, P.W. Ingham, M.K. Whyte A transgenic zebrafish model of neutrophilic inflammation Blood 108 2006 3976 3978
30. R.L. Bernardos, P.A. Raymond GFAP transgenic zebrafish Gene Expr Patterns 6 2006 1007 1013
31. O. Uemura, Y. Okada, H. Ando, M. Guedj, S. Higashijima, T. Shimazaki, N. Chino, H. Okano, H. Okamoto Comparative functional genomics revealed conservation and diversification of three enhancers of the isl1 gene for motor and sensory neuron-specific expression Dev Biol 278 2005 587 606
32. Y. Goldshmit, T. Sztal, T. Hall, P.R. Jusuf, M. Nguyen-Chi, P.D. Currie Fgf-dependent glial cell bridges facilitate spinal cord regeneration in zebrafish J Neurosci 32 2012 7477 7492
33. S.-J. Lee, T.-H. Chan, T.-C. Chen, B.-K. Liao, P.-P. Hwang, H. Lee LPA1 is essential for lymphatic vessel development in zebrafish FASEB J 22 2008 3706 3715
34. N. O'Brien, S.T. Jones, D.G. Williams, H.B. Cunningham, K. Moreno, B. Visentin, A. Gentile, J. Vekich, W. Shestowsky, M. Hiraiwa, R. Matteo, A. Cavalli, D. Grotjahn, M. Grant, G. Hansen, M.A. Campbell, R. Sabbadini Production and characterization of monoclonal anti-sphingosine-1-phosphate antibodies J Lipid Res 50 2009 2245 2257
35. M.F. Pera, J. Andrade, S. Houssami, B. Reubinoff, A. Trounson, E.G. Stanley, D.W. Oostwaard, C. Mummery Regulation of human embryonic stem cell differentiation by BMP-2 and its antagonist noggin J Cell Sci 117 2004 1269 1280
36. B.E. Reubinoff, P. Itsykson, T. Turetsky, M.F. Pera, E. Reinhartz, A. Itzik, T. Ben-Hur Neural progenitors from human embryonic stem cells Nat Biotechnol 19 2001 1134 1140
37. Y. Goldshmit, M.P. Galea, G. Wise, P.F. Bartlett, A.M. Turnley Axonal regeneration and lack of astrocytic gliosis in EphA4-deficient mice J Neurosci 24 2004 10064 10073
38. O. Steward, P.G. Popovich, W.D. Dietrich, N. Kleitman Replication and reproducibility in spinal cord injury research Exp Neurol 233 2012 597 605
39. Y. Goldshmit, M.D. Spanevello, S. Tajouri, L. Li, F. Rogers, M. Pearse, M. Galea, P.F. Bartlett, A.W. Boyd, A.M. Turnley EphA4 blockers promote axonal regeneration and functional recovery following spinal cord injury in mice PLoS One 6 2011 e24636
40. Y. Li, R.J. Oskouian, Y.J. Day, J.A. Kern, J. Linden Optimization of a mouse locomotor rating system to evaluate compression-induced spinal cord injury: correlation of locomotor and morphological injury indices J Neurosurg Spine 4 2006 165 173
41. M. Dottori, J. Leung, A.M. Turnley, A. Pebay Lysophosphatidic acid inhibits neuronal differentiation of neural stem/progenitor cells derived from human embryonic stem cells Stem Cells 26 2008 1146 1154
42. A. Hall Rho GT: pases and the actin cytoskeleton Science 279 1998 509 514
43. S. Wahl, H. Barth, T. Ciossek, K. Aktories, B.K. Mueller Ephrin-A5 induces collapse of growth cones by activating Rho and Rho kinase J Cell Biol 149 2000 263 270
44. C.I. Dubreuil, M.J. Winton, L. McKerracher Rho activation patterns after spinal cord injury and the role of activated Rho in apoptosis in the central nervous system J Cell Biol 162 2003 233 243
45. O. Steward, P.E. Schauwecker, L. Guth, Z. Zhang, M. Fujiki, D. Inman, J. Wrathall, G. Kempermann, F.H. Gage, K.E. Saatman, R. Raghupathi, T. McIntosh Genetic approaches to neurotrauma research: opportunities and potential pitfalls of murine models Exp Neurol 157 1999 19 42
46. Z. Zhang, L. Guth, O. Steward Mechanisms of motor recovery after subtotal spinal cord injury: insights from the study of mice carrying a mutation (WldS) that delays cellular responses to injury Exp Neurol 149 1998 221 229
47. L. Juvin, J.P. Le Gal, J. Simmers, D. Morin Cervicolumbar coordination in mammalian quadrupedal locomotion: role of spinal thoracic circuitry and limb sensory inputs J Neurosci 32 2012 953 965
48. L. Ma, J. Nagai, H. Ueda Microglial activation mediates de novo lysophosphatidic acid production in a model of neuropathic pain J Neurochem 115 2010 643 653
49. S.M. Pitson, and A. Pbay Regulation of stem cell pluripotency and neural differentiation by lysophospholipids Neurosignals 17 2009 242 254
50. A. Pebay, C.S. Bonder, S.M. Pitson Stem cell regulation by lysophospholipids Prostaglandins Other Lipid Mediat 84 2007 83 97