Chronic expression of PPAR-δ by oligodendrocyte lineage cells in the injured rat spinal cord

Journal of Comparative Neurology

Volumn 518, Issue 6, 2010, Pages 785-799

  Almad, Akshata ^a   McTigue, Dana M ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

Cell genesis; Differentiation; Myelin; PPAR ; Proliferation; Spinal cord injury

Indexed keywords

ALPHA TUBULIN; BROXURIDINE; MESSENGER RNA; NEURON SPECIFIC NUCLEAR PROTEIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR DELTA; PROTEIN ANTIBODY; TRANSCRIPTION FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL COUNT; CELL DIFFERENTIATION; CELL LINEAGE; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; GRAY MATTER; IMMUNOHISTOCHEMISTRY; NERVE CELL; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; RAT; REAL TIME POLYMERASE CHAIN REACTION; SPINAL CORD INJURY; WESTERN BLOTTING; WHITE MATTER;

ANIMALS; CELL COUNT; CELL LINEAGE; FEMALE; NERVE FIBERS, MYELINATED; NERVE FIBERS, UNMYELINATED; NEURONS; OLIGODENDROGLIA; PPAR DELTA; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; SPINAL CORD; SPINAL CORD INJURIES; STEM CELLS; TIME FACTORS;

EID: 77949413835     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.22242     Document Type: Article

References (59)

1. Benani A, Heurtaux T, Netter P, Minn A. 2004. Activation of peroxisome proliferator-activated receptor alpha in rat spinal cord after peripheral noxious stimulation. Neurosci Lett 369:59-63.
2. Bhat RV, Axt KJ, Fosnaugh JS, Smith KJ, Johnson KA, Hill DE, Kinzler KW, Baraban JM. 1996. Expression of the APC tumor supressor protein in oligodendroglia. Glia 17:169-174.
3. Braissant O, Wahli W. 1998. Differential expression of peroxisome proliferator-activated receptor-alpha,-beta, and -gamma during rat embryonic development. Endocrinology 139:2748-2754.
4. Coggeshall RE, Lekan HA. 1996. Methods for determining numbers of cells and synapses: a cse for more uniform standards of review. J Comp Neurol. 364:6-15.
5. Crowe MJ, Bresnahan JC, Shuman SL, Masters JN, Beattie MS. 1997. Apoptosis and delayed degeneration after spinal cord injury in rats and monkeys [published erratum appears in Nat Med 1997;3:240]. Nat Med 3:73-76.
6. Dugas JC, Ibrahim A, Barres BA. 2007. A crucial role for p57(Kip2) in the intracellular timer that controls oligodendrocyte differentiation. J Neurosci 27:6185-6196.
7. Fuss B, Mallon B, Phan T, Ohlemeyer C, Kirchoff F, Nishiyama A, Macklin WB. 2000. Purification and analysis of in vivo-differentiated oligodendrocytes expressing the green fluorescent protein. Dev Biol 218:259-274.
8. Grako KA, Ochiya T, Barritt D, Nishiyama A, Stallcup WB. 1999. PDGF (alpha)-receptor is unresponsive to PDGF-AA in aortic smooth muscle cells from the NG2 knockout mouse. J Cell Sci 112:905-915.
9. Granneman J, Skoff R, Yang X. 1998. Member of the peroxisome proliferator-activated receptor family of transcription factors is differentially expressed by oligodendrocytes. J Neurosci Res 51:563-573.
10. Grossman SD, Rosenberg LJ, Wrathall JR. 2001. Temporal-spatial pattern of acute neuronal and glial loss after spinal cord contusion. Exp Neurol 168:273-282.
11. Guillery RW, Herrup K. 1997. Quantification without pontification: choosing a method for counting objects in sectioned tissues. J Comp Neurol. 386:2-7.
12. Hall MG, Quignodon L, Desvergne B. 2008. Peroxisome proliferator- activated receptor beta/delta in the brain: facts and hypothesis. PPAR Res 2008:780452.
13. Han SW, Ritzenthaler JD, Zheng Y, Roman J. 2008. PPAR-β/δ agonist stimulates human lung carcinoma cell growth through inhibition of PTEN expression: the involvement of P13K and NF-κB signals. Am J Physiol Lung Cell Mol Physiol. 294:L1238-L1249.
14. Hihi AK, Michalik L, Wahli W. 2002. PPARs: transcriptional effectors of fatty acids and their derivatives. Cell Mol Life Sci 59:790-798.
15. Horky LL, Galimi F, Gage FH, Horner PJ. 2006. Fate of endogenous stem/progenitor cells following spinal cord injury. J Comp Neurol 498:525-538.
16. Ikeda O, Murakami M, Ino H, Yamazaki M, Nemoto T, Koda M, Nakayama C, Moriya H. 2001. Acute up-regulation of brain-derived neurotrophic factor expression resulting from experimentally induced injury in the rat spinal cord. Acta Neuropathol 102:239-245.
17. Issemann I, Green S. 1990. Activation of a member of the steroid hormone receptor superfamily by peroxisome proliferators. Nature 347:645-650.
18. Iwashita A, Muramatsu Y, Yamazaki T, Muramoto M, Kita Y, Yamazaki S, Mihara K, Moriguchi A, Matsuoka N. 2007. Neuroprotective efficacy of the peroxisome proliferator-activated receptor delta-selective agonists in vitro and in vivo. J Pharmacol Exp Ther 320:1087-1096.
19. Kakudo N, Shimotsuma A, Kusumoto K. 2007. Fibroblast growth factor-2 stimulates adipogenic differentiation of human adipose-derived stem cells. Biochem Biophys Res Commun 359:239-244.
20. Kim DJ, Bility MT, Billin AN, Willson TM, Gonzalez FJ, Peters JM. 2006. PPARbeta/delta selectively induces differentiation and inhibits cell proliferation. Cell Death Differ 13:53-60.
21. Koshinaga M, Sanon HR, Whittemore SR. 1993. Altered acidic and basic fibroblast growth factor expression following spinal cord injury. Exp Neurol 120:32-48.
22. Kuhlmann T, Remington L, Maruschak B, Owens T, Bruck W. 2007. Nogo-A is a reliable oligodendroglial marker in adult human and mouse CNS and in demyelinated lesions. J Neuropathol Exp Neurol 66:238-246.
23. Ligon KL, Kesari S, Kitada M, Sun T, Arnett HA, Alberta JA, Anderson DJ, Stiles CD, Rowitch DH. 2006. Development of NG2 neural progenitor cells requires Olig gene function. Proc Natl Acad Sci U S A 103:7853-7858.
24. Linares D, Taconis M, Mana P, Correcha M, Fordham S, Staykova M, Willenberg DO. 2006. Neuronal nitric oxide synthase plays a key role in CNS demyelination. J Neurosci 26:12672-12681.
25. Liu QS, Gao M, Zhu SY, Li SJ, Zhang L, Wang QJ, Du GH. 2007. The novel mechanism of recombinant human ciliary neurotrophic factor on the anti-diabetes activity. Basic Clin Pharmacol Toxicol 101:78-84.
26. Lu QR, Cai L, Rowitch D, Cepko CL, Stiles CD. 2001. Ectopic expression of Olig1 promotes oligodendrocyte formation and reduces neuronal survival in developing mouse cortex. Nat Neurosci 4:973-974.
27. Madrigal JL, Kalinin S, Richardson JC, Feinstein DL. 2007. Neuroprotective actions of noradrenaline: effects on glutathione synthesis and activation of peroxisome proliferator activated receptor delta. J Neurochem 103:2092-2101.
28. Matsusue K, Peters JM, Gonzalez FJ. 2004. PPARbeta/delta potentiates PPARgamma-stimulated adipocyte differentiation. FASEB J 18:1477-1479.
29. McTigue DM, Horner PJ, Stokes BT, Gage FH. 1998. Neurotrophin-3 and brain-derived neurotrophic factor induce oligodendrocyte proliferation and myelination of regenerating axons in the contused adult rat spinal cord. J Neurosci 18:5354-5365.
30. McTigue DM, Wei P, Stokes BT. 2001. Proliferation of NG2-positive cells and altered oligodendrocyte numbers in the contused rat spinal cord. J Neurosci 21:3392-3400.
31. McTigue DM, Tripathi R, Wei P. 2006. NG2 colocalizes with axons and is expressed by a mixed cell population in spinal cord lesions. J Neuropathol Exp Neurol 65:406-420.
32. Mocchetti I, Rabin SJ, Colangelo AM, Whittemore SR, Wrathall JR. 1996. Increased basic fibroblast growth factor expression following contusive spinal cord injury. Exp Neurol 141:154-164.
33. Moya-Camarena SY, Van den Heuvel JP, Belury MA. 1999. Conjugated linoleic acid activates peroxisome proliferator-activated receptor alpha and beta subtypes but does not induce hepatic peroxisome proliferation in Sprague-Dawley rats. Biochim Biophys Acta 1436:331-342.
34. Muller-Brusselbach S, Komhoff M, Rieck M, Meissner W, Kaddatz K, Adamkiewicz J, Keil B, Klose KJ, Moll R, Burdick AD, Peters JM, Muller R. 2007. Deregulation of tumor angiogenesis and blockade of tumor growth in PPARbeta-deficient mice. EMBO J 26:3686-3698.
35. Mutti E, Veber D, Stampachiacchiere B, Triaca V, Gammella E, Tacchini L, Aloe L, Scalabrino G. 2007. Cobalamin deficiency-induced downregulation of p75-immunoreactive cell levels in rat central nervous system. Brain Res 1157:92-99.
36. Nadra K, Anghel SI, Joye E, Tan NS, Basu-Modak S, Trono D, Wahli W, Desvergne B. 2006. Differentiation of trophoblast giant cells and their metabolic functions are dependent on peroxisome proliferator-activated receptor beta/delta. Mol Cell Biol 26:3266-3281.
37. Neubauer M, Fischbach C, Bauer-Kreisel P, Lieb E, Hacker M, Tessmar J, Schulz MB, Goepferich A, Blunk T. 2004. Basic fibroblast growth factor enhances PPARgamma ligand-induced adipogenesis of mesenchymal stem cells. FEBS Lett 577:277-283.
38. Oliver WR Jr, Shenk JL, Snaith MR, Russell CS, Plunket KD, Bodkin NL, Lewis MC, Winegar DA, Sznaidman ML, Lambert MH, Xu HE, Sternbach DD, Kliewer SA, Hansen BC, Willson TM. 2001. A selective peroxisome proliferator-activated receptor delta agonist promotes reverse cholesterol transport. Proc Natl Acad Sci U S A 98:5306-5311.
39. Peters JM, Lee SS, Li W, Ward JM, Gavrilova O, Everett C, Reitman ML, Hudson LD, Gonzalez FJ. 2000. Growth, adipose, brain, and skin alterations resulting from targeted disruption of the mouse peroxisome proliferator- activated receptor beta-(delta). Mol Cell Biol 20:5119-5128.
40. Polak PE, Kalinin S, Dello RC, Gavrilyuk V, Sharp A, Peters JM, Richardson J, Willson TM, Weinberg G, Feinstein DL. 2005. Protective effects of a peroxisome proliferator-activated receptor-beta/delta agonist in experimental autoimmune encephalomyelitis. J Neuroimmunol 168:65-75.
41. Qi C, Zhu Y, Reddy JK. 2000. Peroxisome proliferator-activated receptors, coactivators, and downstream targets. Cell Biochem Biophys 32:187-204.
42. Rabchevsky AG, Sullivan PG, Scheff SW. 2007. Temporal-spatial dynamics in oligodendrocyte and glial progenitor cell numbers throughout ventrolateral white matter following contusion spinal cord injury. Glia 55:831-843.
43. Ririe KM, Rasmussen RP, Wittwer CT. 1997. Product differentiation by analysis of DNA melting curves during the polymerase chain reaction. Anal Biochem 245:154-160.
44. Saluja I, Granneman JG, Skoff RP. 2001. PPAR delta agonists stimulate oligodendrocyte differentiation in tissue culture. Glia 33:191-204.
45. T method. Nature protocols 3:1101-1108.
46. Schmuth M, Haqq CM, Cairns WJ, Holder JC, Dorsam S, Chang S, Lau P, Fowler AJ, Chuang G, Moser AH, Brown BE, Mao-Qiang M, Uchida Y, Schoonjans K, Auwerx J, Chambon P, Willson TM, Elias PM, Feingold KR. 2004. Peroxisome proliferator-activated receptor (PPAR)-beta/delta stimulates differentiation and lipid accumulation in keratinocytes. J Invest Dermatol 122:971-983.
47. Smith SA, Monteith GR, Robinson JA, Venkata NG, May FJ, Roberts-Thomson SJ. 2004. Effect of the peroxisome proliferator-activated receptor beta activator GW0742 in rat cultured cerebellar granule neurons. J Neurosci Res 77:240-249.
48. Talbott JF, Loy DN, Liu Y, Qiu MS, Bunge MB, Rao MS, Whittemore SR. 2005. Endogenous Nkx2.2+/Olig2+ oligodendrocyte precursor cells fail to remyelinate the demyelinated adult rat spinal cord in the absence of astrocytes. Exp Neurol 192:11-24.
49. Talbott JF, Cao Q, Bertram J, Nkansah M, Benton RL, Lavik E, Whittemore SR. 2007. CNTF promotes the survival and differentiation of adult spinal cord-derived oligodendrocyte precursor cells in vitro but fails to promote remyelination in vivo. Exp Neurol 204:485-489.
50. Tan NS, Icre G, Montagner A, Bordier-ten-Heggeler B, Wahli W, Michalik L. 2007. The nuclear hormone receptor peroxisome proliferator-activated receptor beta/delta potentiates cell chemotactism, polarization, and migration. Mol Cell Biol 27:7161-7175.
51. Tripathi R, McTigue DM. 2007. Prominent oligodendrocyte genesis along the border of spinal contusion lesions. Glia 55:698-711.
52. Tripathi RB, McTigue DM. 2008. Chronically increased ciliary neurotrophic factor and fibroblast growth factor-2 expression after spinal contusion in rats. J Comp Neurol 510:129-144.
53. Wang YX, Zhang CL, Yu RT, Cho HK, Nelson MC, Bayuga-Ocampo CR, Ham J, Kang H, Evans RM. 2004. Regulation of muscle fiber type and running endurance by PPARdelta. PLoS Biol 2:e294.
54. Widenfalk J, Lundstromer K, Jubran M, Brene S, Olson L. 2001. Neurotrophic factors and receptors in the immature and adult spinal cord after mechanical injury or kainic acid. J Neurosci 21:3457-3475.
55. Woods JW, Tanen M, Figueroa DJ, Biswas C, Zycband E, Moller DE, Austin CP, Berger JP. 2003. Localization of PPARdelta in murine central nervous system: expression in oligodendrocytes and neurons. Brain Res 975:10-21.
56. Yasuda E, Tokuda H, Ishisaki A, Hirade K, Kanno Y, Hanai Y, Nakamura N, Noda T, Katagiri Y, Kozawa O. 2005. PPAR-gamma ligands up-regulate basic fibroblast growth factor-induced VEGF release through amplifying SAPK/JNK activation in osteoblasts. Biochem Biophys Res Commun 328:137-143.
57. Yoo S, Wrathall JR. 2007. Mixed primary culture and clonal analysis provide evidence that NG2 proteoglycan-expressing cells after spinal cord injury are glial progenitors. Dev Neurobiol 67:860-874.
58. Zai LJ, Wrathall JR. 2005. Cell proliferation and replacement following contusive spinal cord injury. Glia 50:247-257.
59. Zai LJ, Yoo S, Wrathall JR. 2005. Increased growth factor expression and cell proliferation after contusive spinal cord injury. Brain Res 1052:147-155.