Characterization of retinaldehyde dehydrogenase-2 induction in NG2-positive glia after spinal cord contusion injury

International Journal of Developmental Neuroscience

Volumn 25, Issue 1, 2007, Pages 7-16

  Kern, Johanna ^a   Schrage, Kirsten ^a,b   Koopmans, Guido C ^b,c   Joosten, Elbert A ^c   McCaffery, Peter ^d   Mey, Jörg ^a,b  

^a RWTH AACHEN UNIVERSITY   (Germany)

^b EURON Graduate School of Neuroscience   (Netherlands)

^c MAASTRICHT UNIVERSITY MEDICAL CENTER   (Netherlands)

^d UNIVERSITY OF ABERDEEN   (United Kingdom)

Author keywords

RALDH2; RAR; Rat; Retinoic acid; RXR; Spinal cord injury

Indexed keywords

ANTIGEN; NEUROGLIAL ANTIGEN 2; PROTEIN DERIVATIVE; RETINAL DEHYDROGENASE 2; RETINOIC ACID; RETINOIC ACID RECEPTOR ALPHA; RETINOIC ACID RECEPTOR BETA; RETINOID X RECEPTOR ALPHA; RETINOID X RECEPTOR BETA; UNCLASSIFIED DRUG;

AMINO ACID SYNTHESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOCRINE EFFECT; BLOOD VESSEL; CONTROLLED STUDY; ENZYME ANALYSIS; GLIA CELL; IMMUNOCOMPETENT CELL; MALE; MENINX; NONHUMAN; OLIGODENDROGLIA; PARACRINE SIGNALING; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SPINAL CORD INJURY;

ALDEHYDE OXIDOREDUCTASES; ANIMALS; ANTIGENS; ENZYME INDUCTION; GENE EXPRESSION REGULATION; IMMUNOHISTOCHEMISTRY; MALE; MODELS, BIOLOGICAL; NEUROGLIA; PROTEOGLYCANS; RATS; RATS, INBRED LEW; RECEPTORS, RETINOIC ACID; SPINAL CORD INJURIES; TIME FACTORS;

MAMMALIA; RATTUS;

EID: 33846482549     PISSN: 07365748     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijdevneu.2006.11.006     Document Type: Article

References (62)

1. Aguirre A.A., Chittajallu R., Belachew S., and Gallo V. NG2-expressing cells in the subventricular zone are type C-like cells and contribute to interneuron generation in the postnatal hippocampus. J. Cell Biol. 165 (2004) 575-589
2. Basso D.M., Beattie M.S., and Bresnahan J.C. A sensitive and reliable locomotor rating scale for open field testing in rats. J. Neurotrauma 12 (1996) 1-21
3. Basso D.M., Beattie M.S., and Bresnahan J.C. Spinal cord contusion using the NYU weigth-drop device versus transection. Exp. Neurol. 139 (1996) 244-246
4. Berggren K., McCaffery P., Dräger U.C., and Forehand C.J. Differential distribution of retinoic acid synthesis in the chicken embryo as determined by immunolocalization of the retinoic acid synthetic enzyme, RALDH-2. Dev. Biol. 210 (1999) 288-304
5. Blomhoff R., and Blomhoff H.K. Overview of retinoid metabolism and function. J. Neurobiol. 66 (2006) 606-630
6. Butt A.M., Kiff J., Hubbard P., and Berry M. Synantocytes: new functions for novel NG2 expressing glia. J. Neurocytol. 31 (2002) 551-565
7. Chen Z.J., Negra M., Levine A., Ughrin Y., and Levine J.M. Oligodendrocyte precursor cells: reactive cells that inhibit axon growth and regeneration. J. Neurocytol. 31 (2002) 481-495
8. Choi W.-H., Ji K.-A., Jeon S.-B., Yang M.-S., Kim H., Min K., Shong M., Jou I., and Joe E.-H. Anti-inflammatory roles of retinoic acid in rat brain astrocytes: suppression of interferon-γ-induced JAK/STAT phosphorylation. Biochem. Biophys. Res. Commun. 329 (2005) 125-131
9. Clagett-Dame M. The role of all-trans retinoic acid in neurite outgrowth and axonal elongation. J. Neurobiol. 66 (2006) 739-756
10. Clark R.S., Chen J., Watkins S.C., Kochanek P.M., Chen M., Stetler R.A., Loeffert J.E., and Graham S.H. Apoptosis-suppressor gene bcl-2 expression after traumatic brain injury in rats. J. Neurosci. 17 (1997) 9172-9182
11. Corcoran J., Shroot B., Pizzey J., and Maden M. The role of retinoic acid receptors in neurite outgrowth from different populations of embryonic mouse dorsal root ganglia. J. Cell Sci. 113 (2000) 2567-2574
12. Corcoran J., So P.-L., Barber R.D., Vincent K.J., Mazarakis N.D., Mitrophanous K.A., Kingsman S.M., and Maden M. Retinoic acid receptor beta2 and neurite outgrowth in the adult mouse spinal cord in vitro. J. Cell Sci. 115 (2002) 3779-3786
13. Dawson M.R.L., Polito A., Levine J.M., and Reynolds R. NG2-expressing glial progenitor cells: an abundant and widespread population of cycling cells in the adult rat CNS. Mol. Cell. Neurosci. 24 (2003) 476-488
14. de Castro Jr. R., Tajrishi R., Claros J., and Stallcup W.B. Differential responses of spinal axons to transection: influence of the NG2 proteoglycan. Exp. Neurol. 192 (2005) 299-309
15. Fukushi J., Makagiansar I.T., and Stallcup W.B. NG2 proteoglycan promotes endothelial cell motility and angiogenesis via engagement of galectin-3 and α3β1 integrin. Mol. Biol. Cell 15 (2004) 3580-3590
16. Gaetano C., Catalano A., Illi B., Felici A., Minucci S., Palumbo R., Facchiano F., Mangoni A., Mancarella S., Mühlhauser J., and Capogrossi M.C. Retinoids induce fibroblast growth factor-2 production in endothelial cells via retinoic acid receptor α activation and stimulate angiogenesis in vitro and in vivo. Circ. Res. 88 (2001) e38-e47
17. Gross V., Villiger P.M., Zhang B., and Lotz M. Retinoic acid inhibits interleukin-1-induced cytokine synthesis in human monocytes. J. Leukocyte Biol. 54 (1993) 125-132
18. Haskell B.E., Stach R.W., Werrbach-Perez K., and Perez-Polo J.R. Effect of retinoic acid on nerve growth factor receptors. Cell Tissue Res. 247 (1987) 67-73
19. Haskell G.T., Maynard T.M., Shatzmiller R.A., and LaMantia A.-S. Retinoic acid signaling at sites of plasticity in the mature central nervous system. J. Comp. Neurol. 452 (2002) 228-241
20. Holst A.v., Lefcort F., and Rohrer H. TrkA expression levels of sympathetic neurons correlate with NGF-dependent survival during development and after treatment with retinoic acid. Eur. J. Neurosci. 9 (1997) 2169-2177
21. Holst A.v., Rodríguez-Tébar A., Michaille J.-J., Dhouailly D., Bäckström A., Ebendal T., and Rohrer H. Retinoic acid-mediated increase in TrkA expression is sufficient to elicit NGF-dependent survival of sympathetic neurons. Mol. Cell. Neurosci. 6 (1995) 185-198
22. Horner P.J., Thallmair M., and Gage F.H. Defining the NG2-expressing cell of the adult CNS. J. Neurocytol. 31 (2002) 469-480
23. Jones L.L., Sajed D., and Tuszynski M.H. Axonal regeneration through regions of chondroitin sulfate proteoglycan deposition after spinal cord injury: a balance of permissiveness and inhibition. J. Neurosci. 23 (2003) 9276-9288
24. Jones L.L., Yamaguchi Y., Stallcup W.B., and Tuszynski M.H. NG2 is a major chondroitin sulfate proteoglyan produced after spinal cord injury and is expressed by macrophages and oligodendrocyte progenitors. J. Neurosci. 22 (2002) 2792-2803
25. Keirstead H.S., Levine J.M., and Blakemore W.F. Response of the oligodendrocyte progenitor cell population (defined by NG2 labelling) to demyelination of the adult spinal cord. Glia 22 (1998) 161-179
26. Kim B.-H., Kang K.-S., and Lee Y.-S. Effect of retinoids on LPS-induced COX-2 expression and COX-2 associated PGE2 release from mouse peritoneal macrophages and TNFα release from rat peripheral blood mononuclear cells. Toxicol. Lett. 150 (2004) 191-201
27. Kini A.R., Peterson L.C., Tallman M.S., and Lingen M.W. Angiogenesis in acute promyeloytic leukemia: induction by vascular endothelial growth factor and inhibition by all-trans retinoic acid. Blood 97 (2001) 3919-3924
28. Levine J.M. Increased expression of the NG2 chondroitin-sulfate proteoglycan after brain injury. J. Neurosci. 14 (1994) 4716-4730
29. Lin S.-C., and Bergles D.E. Physiological characteristics of NG2-expressing glial cells. J. Neurocytol. 31 (2002) 537-549
30. Maden M. Retinoids and spinal cord development. J. Neurobiol. 66 (2006) 726-738
31. Maden M., Keen G., and Jones G. Retinoic acid as a chemotactic molecule in neuronal development. Int. J. Dev. Neurosci. 16 (1998) 317-322
32. McCaffery P., and Dräger U.C. Hot spots of retinoic acid synthesis in the developing spinal cord. Proc. Natl. Acad. Sci. U.S.A. 91 (1994) 7194-7197
33. McTigue D.M., Wei P., and Stokes B.T. Proliferation of NG2-positive cells and altered oligodendrocyte numbers in the contused rat spinal cord. J. Neurosci. 21 (2001) 3392-3400
34. Mey J. A new target for CNS injury? The role of retinoic acid signaling after nerve lesions. J. Neurobiol. 66 (2006) 757-779
35. Mey J., and Hammelmann S. OLN-93 oligodendrocytes synthesize all-trans retinoic acid in vitro. Cell Tissue Res. 302 (2000) 49-58
36. Mey J., and Henkes L. Retinoic acid enhances leukemia inhibitory factor expression in OLN-93 oligodendrocytes. Cell Tissue Res. 310 (2002) 155-161
37. Mey J., Morassutti D., Brook G., Liu R.-H., Zhang Y.-P., Koopmans G., and McCaffery P. Retinoic acid synthesis by a population of NG-2 positive cells in the injured spinal cord. Eur. J. Neurosci. 21 (2005) 1555-1568
38. Mey J., and Rombach N. Retinoic acid increases BDNF-dependent regeneration of chick retinal ganglion cells in vitro. Neuroreport 10 (1999) 3573-3577
39. Nielsen H.H., Ladeby R., Drøjdahl N., Peterson A.C., and Finsen B. Axonal degeneration stimulates the formation of NG2+ cells and oligodendrocytes in the mouse. Glia 54 (2006) 105-115
40. Nishiyama A., Watanabe M., Yang Z., and Bu J. Identity, distribution, and development of polydendrocytes: NG2-expressing glial cells. J. Neurocytol. 31 (2002) 437-455
41. Polito A., and Reynolds R. NG2-expressing cells as oligodendrocyte progenitors in the normal and demyelinated adult central nervous system. J. Anat. 207 (2005) 707-716
42. Quinn S.D.P., and De Boni U. Enhanced neuronal regeneration by retinoic acid of murine dorsal root ganglia and of fetal murine and human spinal cord in vitro. In Vitro Cell. Dev. Biol. A 27 (1991) 55-62
43. Reynolds R., Dawson M.R.L., Papadopoulos D., Polito A., Di Bello I.C., Pham-Dinh D., and Levine J. The response of NG2-expressing oligodendrocyte progenitors to demyelination in MOG-EAE and MS. J. Neurocytol. 31 (2002) 523-536
44. Rhodes K.E., Raivich G., and Fawcett J.W. The injury response of oligodendrocyte precursor cells is induced by platelets, macrophages and inflammation-associated cytokines. Neuroscience 140 (2006) 100
45. Rodríguez-Tébar A., and Rohrer H. Retinoic acid induces NGF-dependent survival response and high-affinity binding NGF receptors in immature chick sympathetic neurons. Development 112 (1991) 813-820
46. Schrage K., Koopmans G., Joosten E.A., and Mey J. Macrophages and neurons are targets of retinoic acid signaling after spinal cord contusion injury. Eur. J. Neurosci. 23 (2006) 285-295
47. Sirsjö A., Gidlof A.C., Olsson A., Torma H., Ares M., Kleiner H., Forstermann U., and Hansson G.K. Retinoic acid inhibits nitric oxide synthase-2 expression through the retinoic acid receptor-alpha. Biochem. Biophys. Res. Commun. 270 (2000) 846-851
48. Smith M.R., Xie T., Joshi I., and Schilder R.J. Dexamethasone plus retinoids decrease IL-6/IL-6 receptor and induce apoptosis in myeloma cells. Br. J. Hematol. 102 (1998) 1090-1097
49. So P.-L., Yip P.K., Bunting S., Wong L.-F., Mazarakis N.D., Hall S., McMahon S., Maden M., and Corcoran J.P.T. Interactions between retinoic acid, nerve growth factor and sonic hedgehog signalling pathways in neurite outgrowth. Dev. Biol. 298 (2006) 167-175
50. Song S., Ewald A.J., Stallcup W.B., Werb Z., and Bergers G. PDGFRβ+ perivascular progenitor cells in tumours regulate pericyte differentiation and vascular survival. Nat. Cell Biol. 7 (2006) 870-881
51. Tan A.M., Zhang W., and Levine J.M. NG2: a component of the glial scar that inhibits axon growth. J. Anat. 207 (2005) 717-725
52. Tong L., Werrbach-Perez K., and Perez-Polo J.R. Retinoic acid induces apoptosis in PC12 cells independent of neurotrophic factors. J. Neurochem. 68 (1997) 1424-1435
53. Vuillaume I., Schraen-Maschke S., Formstecher P., and Sablonniere B. Real time RT-PCR shows correlation between retinoid-induced apoptosis and NFG-R mRNA levels. Biochem. Biophys. Res. Commun. 289 (2001) 647-652
54. Wagner E., Luo T., and Dräger U.C. Retinoic acid synthesis in the postnatal mouse brain marks distinct developmental stages and functional systems. Cereb. Cortex 12 (2002) 1244-1253
55. Wilson H.C., Scolding N.J., and Raine C.S. Co-expression of PDGFα receptor and NG2 by oligodendrocyte precursors in human CNS and multiple sclerosis lesions. J. Neuroimmunol. 176 (2006) 162-173
56. Wong L.-F., Yip P.K., Battaglia A., Grist J., Corcoran J., Maden M., Azzouz M., Kingsman S.M., Kingsman A.J., Mazarakis N.D., and McMahon S.B. Retinoic acid receptor β2 promotes functional regeneration of sensory axons in the spinal cord. Nat. Neurosci. 9 (2006) 243-250
57. Wuarin L., and Sidell N. Differential susceptibilities of spinal cord neurons to retinoic acid-induced survival and differentiation. Dev. Biol. 144 (1991) 429-435
58. Wuarin L., Sidell N., and De Vellis J. Retinoids increase perinatal spinal cord neuronal survival and astroglial differentiation. Int. J. Dev. Neurosci. 8 (1990) 317-326
59. Yang Y.K., Park J.J., Lee M.C., Yoon B.H., Yang Y.S., and Kim S.U. Retinoic acid-mediated induction of neurons and glial cells from human umbilical cord-derived hematopoietic stem cells. J. Neurosci. Res. 75 (2004) 573-584
60. Yip P.K., Wong L.F., Pattinson D., Battaglia A., Grist J., Bradbury E.J., Maden M., McMahon S.B., and Mazarakis N.D. Lentiviral vector expressing retinoid acid receptor β2 promotes recovery of function after corticospinal tract injury in the adult rat spinal cord. Hum. Mol. Gen. 15 (2006) 3107-3118
61. Zhang J., Smith D., Yamamoto M., Ma L., and McCaffery P. The meninges is a source of retinoic acid for the late-developing hindbrain. J. Neurosci. 23 (2003) 7610-7620
62. Zhelyaznik N., Schrage K., McCaffery P., and Mey J. Activation of retinoic acid signaling after sciatic nerve injury: upregulation of cellular retinoid binding proteins. Eur. J. Neurosci. 18 (2003) 1033-1040