Peroxisome proliferator-activated receptor γ agonists accelerate oligodendrocyte maturation and influence mitochondrial functions and oscillatory Ca2+ waves

Journal of Neuropathology and Experimental Neurology

Volumn 70, Issue 10, 2011, Pages 900-912

  De Nuccio, Chiara ^a   Bernardo, Antonietta ^a   De Simone, Roberta ^a   Mancuso, Enrico ^a   Magnaghi, Valerio ^b   Visentin, Sergio ^a   Minghetti, Luisa ^a  

^a ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^b UNIVERSITY OF MILAN   (Italy)

Author keywords

Ca2+ waves; Demyelination; Mitochondria; Myelin; Oligodendrocytes; Pioglitazone; PPAR

Indexed keywords

15 DEOXY DELTA12,14 PROSTAGLANDIN J2; ADENOSINE DIPHOSPHATE; CALCIUM ION; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PIOGLITAZONE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CALCIUM SIGNALING; CELL DIFFERENTIATION; CELL MATURATION; CONTROLLED STUDY; DEMYELINATION; DRUG EFFECT; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; NEWBORN; NONHUMAN; OLIGODENDROGLIA; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT; RESPIRATORY CHAIN; STEM CELL;

ANILINE COMPOUNDS; ANIMALS; ANIMALS, NEWBORN; BIOLOGICAL CLOCKS; CALCIUM; CELL DIFFERENTIATION; CELLS, CULTURED; ELECTRON TRANSPORT COMPLEX IV; GENE EXPRESSION REGULATION; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA; MYELIN BASIC PROTEINS; OLIGODENDROGLIA; ORGANOMETALLIC COMPOUNDS; PPAR GAMMA; PROSENCEPHALON; PROSTAGLANDIN D2; RATS; RATS, WISTAR; STEM CELLS; THIAZOLIDINEDIONES; XANTHENES;

EID: 80053372523     PISSN: 00223069     EISSN: 15546578     Source Type: Journal    
DOI: 10.1097/NEN.0b013e3182309ab1     Document Type: Article

References (42)

1. Baumann N, Pham-Dinh D. Biology of oligodendrocyte and myelin in the mammalian central nervous system. Physiol Rev 2001;81:871-927 (Pubitemid 32267079)
2. Kassmann CM, Lappe-Siefke C, Baes M, et al. Axonal loss and neuroinflammation caused by peroxisome-deficient oligodendrocytes. Nat Genet 2007;39:969-76 (Pubitemid 47185174)
3. Kassmann CM, Nave KA. Oligodendroglial impact on axonal function and survivalVA hypothesis. Curr Opin Neurol 2008;21:235-41 (Pubitemid 351653970)
4. Feng Y. Convergence and divergence in the etiology of myelin impairment in psychiatric disorders and drug addiction. Neurochem Res 2008; 33:1940-49
5. McIntosh AM, Hall J, Lymer GK, et al. Genetic risk for white matter abnormalities in bipolar disorder. Int Rev Psychiatry 2009;21:387-93
6. Yki-Jarvinen H. Thiazolidinediones. N Engl J Med 2004;351:1106-18
7. Sundararajan S, Jiang Q, Heneka MT, et al. PPARF as a therapeutic target in central nervous system diseases. Neurochem Intern 2006;49: 136-44 (Pubitemid 43867071)
8. Heneka MT, Landreth GE, Hüll M. Drug insight: Effects mediated by peroxisome proliferator-activated receptor-F in CNS disorders. Nat Clin Pract Neurol 2007;3:496-504 (Pubitemid 47377609)
9. Niino M, Iwabuchi K, Kikuchi S, et al. Amelioration of experimental autoimmune encephalomyelitis in C57BL/6 mice by an agonist of peroxisome proliferator-activated receptor-F. J Neuroimmunol 2001;116: 40-48 (Pubitemid 32322638)
10. Diab A, Deng C, Smith JD, et al. Peroxisome proliferator-activated receptor-gamma agonist 15-deoxy-$(12,14)-prostaglandin J(2) ameliorates experimental autoimmune encephalomyelitis. J Immunol 2002;168: 2508-15 (Pubitemid 34171857)
11. Feinstein DL, Galea E, Gavrilyuk V, et al. Peroxisome proliferatoractivated receptor-F agonists prevent experimental autoimmune encephalomyelitis. Ann Neurol 2002;51:694-702 (Pubitemid 34568847)
12. Natarajan C, Muthian G, Barak Y, et al. Peroxisome proliferatoractivated receptor-FYdeficient heterozygous mice develop an exacerbated neural antigenYinduced TH1 response and experimental allergic encephalomyelitis. J Immunol 2003;171:5743Y50 (Pubitemid 37467189)
13. Erratum in: J Immunol 2004;172: following 5127
14. Shukla DK, Kaiser CC, Stebbins GT, et al. Effects of pioglitazone on diffusion tensor imaging indices in multiple sclerosis patients. Neurosci Lett 2010;472:153-56
15. Kaiser CC, Shukla DK, Stebbins GT, et al. A pilot test of pioglitazone as an add-on in patients with relapsing remitting multiple sclerosis. J Neuroimmunol 2009;211:124-30
16. Bernardo A, Minghetti L. Regulation of glial cell functions by PPAR-F natural and synthetic agonists. PPAR Res 2008;2008:864140
17. Roth AD, Leisewitz AV, Jung JE, et al. PPAR F activators induce growth arrest and process extension in B12 oligodendrocyte-like cells and terminal differentiation of cultured oligodendrocytes. J Neurosci Res 2003; 72:425-35 (Pubitemid 36523417)
18. Sim FJ, Lang JK, Ali TA, et al. Statin treatment of adult human glial progenitors induces PPARF-mediated oligodendrocytic differentiation. Glia 2008;56:954-62
19. Bernardo A, Bianchi D, Magnaghi V, et al. Peroxisome proliferatoractivated receptor-F agonists promote differentiation and antioxidant defenses of oligodendrocyte progenitor cells. J Neuropathol Exp Neurol 2009;68:797-808
20. Haak LL, Grimaldi M, Russell JT. Mitochondria in myelinating cells: Calcium signaling in oligodendrocyte precursor cells. Cell Calcium 2000; 28:297-306 (Pubitemid 32049114)
21. Schoenfeld R, Wong A, Silva J, et al. Oligodendroglial differentiation induces mitochondrial genes and inhibition of mitochondrial function represses oligodendroglial differentiation. Mitochondrion 2010;10:143-50
22. Ziabreva I, Campbell G, Rist J, et al. Injury and differentiation following inhibition of mitochondrial respiratory chain Complex IV in rat oligodendrocytes. Glia 2010;58:1827-37
23. Mahad DJ, Ziabreva I, Campbell G, et al. Detection of cytochrome c oxidase activity and mitochondrial proteins in single cells. J Neurosci Methods 2009;184:310-19
24. Agresti C, Meomartini ME, Amadio S, et al. ATP regulates oligodendrocyte progenitor migration, proliferation, and differentiation: Involvement of metabotropic P2 receptors. Brain Res Brain Res Rev 2005;48: 157-65 (Pubitemid 40585746)
25. Berridge MJ, Bootman MD, Roderick HL. Calcium signalling: Dynamics, homeostasis and remodelling. Nat Rev Mol Cell Biol 2003;4:517-29 (Pubitemid 36773404)
26. Simpson PB, Russell JT. Mitochondria support inositol 1,4,5-trisphosphateYmediated Ca2+ waves in cultured oligodendrocytes. J Biol Chem 1996;271:33493-501
27. Dyer CA. The structure and function of myelin: From inert membrane to perfusion pump. Neurochem Res 2002;27:1279-92 (Pubitemid 36014142)
28. Campagnoni AT, Campagnoni CW. Myelin basic protein gene. In: Lazzarini RA, ed. Myelin Biology and Disorders. San Diego, CA: Elsevier Academic, 2004:387-400
29. Brookes PS, Yoon Y, Robotham JL, et al. Calcium, ATP, and ROS: A mitochondrial love-hate triangle. Am J Physiol Cell Physiol 2004;287: C817-33 (Pubitemid 39238305)
30. Hajnóczky G, Hager R, Thomas AP. Mitochondria suppress local feedback activation of inositol 1,4, 5-trisphosphate receptors by Ca2+. J Biol Chem 1999;274:14157-62
31. Gordienko DV, Greenwood IA, Bolton TB. Direct visualization of sarcoplasmic reticulum regions discharging Ca(2+) sparks in vascular myocytes. Cell Calcium 2001;29:13-28 (Pubitemid 32118046)
32. Marchant JS, Ramos V, Parker I. Structural and functional relationships between Ca2+ puffs and mitochondria in Xenopus oocytes. Am J Physiol Cell Physiol 2002;282:C1374-86 (Pubitemid 34663086)
33. Pacher P, Thomas AP, Hajnóczky G. Ca2+ marks: Miniature calcium signals in single mitochondria driven by ryanodine receptors. Proc Natl Acad Sci USA 2002;99:2380-85 (Pubitemid 34169069)
34. Haak LL, Grimaldi M, Smaili SS, et al. Mitochondria regulate Ca2+ wave initiation and inositol trisphosphate signal transduction in oligodendrocyte progenitors. J Neurochem 2002;80:405-15 (Pubitemid 36383024)
35. Walsh C, Barrow S, Voronina S, et al. Modulation of calcium signalling by mitochondria. Biochem Biophys Acta 2009;1787:1374-82
36. Mahad D, Ziabreva I, Lassmann H, et al. Mitochondrial defects in acute multiple sclerosis lesions. Brain 2008;131:1722-35 (Pubitemid 351957459)
37. Wood A, Wing MG, Benham CD, et al. Specific induction of intracellular calcium oscillations by complement membrane attack on oligodendroglia. J Neurosci 1993;13:3319-32 (Pubitemid 23241171)
38. Feinstein DL, Spagnolo A, Akar C, et al. Receptor-independent actions of PPAR thiazolidinedione agonists: Is mitochondrial function the key? Biochem Pharmacol 2005;70:177-88 (Pubitemid 40814400)
39. Dello Russo C, Gavrilyuk V, Weinberg G, et al. Peroxisome proliferatoractivated receptor F thiazolidinedione agonists increase glucose metabolism in astrocytes. J Biol Chem 2003;278:5828-36 (Pubitemid 36800829)
40. Miron VE, Zehntner SP, Kuhlmann T, et al. Statin therapy inhibits remyelination in the central nervous system. Am J Pathol 2009;174:1880-90
41. Maier O, De Jonge J, Nomden A, et al. Lovastatin induces the formation of abnormal myelin-like membrane sheets in primary oligodendrocytes. Glia 2009;57:402-13
42. Juurlink DN. Rosiglitazone and the case for safety over certainty. JAMA 2010;8:469-71