Chronic caloric restriction attenuates a loss of sulfatide content in PGC-1α -/- mouse cortex: A potential lipidomic role of PGC-1α in neurodegeneration

Journal of Lipid Research

Volumn 53, Issue 2, 2012, Pages 273-281

  Kiebish, Michael A ^a   Young, Dee M ^a   Lehman, John J ^a   Han, Xianlin ^b  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b BURNHAM INSTITUTE   (United States)

Author keywords

Alzheimer's disease; Apolipoprotein E; Shotgun lipidomics; Sphingolipidomics

Indexed keywords

APOLIPOPROTEIN E; LIVER X RECEPTOR; MYELIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; RETINOID X RECEPTOR; SULFATIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CALORIC RESTRICTION; CONTROLLED STUDY; HOMEOSTASIS; LIPID ANALYSIS; LIPIDOMICS; MOUSE; NERVE DEGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; WESTERN BLOTTING; WILD TYPE;

ANIMALS; APOLIPOPROTEINS E; CALORIC RESTRICTION; CEREBRAL CORTEX; CEREBROSIDE-SULFATASE; ENZYMES; HOMEOSTASIS; MEMBRANE TRANSPORT PROTEINS; MICE; MICE, MUTANT STRAINS; MYELIN PROTEINS; NEURODEGENERATIVE DISEASES; ORPHAN NUCLEAR RECEPTORS; PROTEOLIPIDS; RETINOID X RECEPTORS; SULFOGLYCOSPHINGOLIPIDS; SULFOTRANSFERASES; TRANS-ACTIVATORS;

EID: 84855694801     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M020628     Document Type: Article

References (61)

1. Puigserver, P., and B. M. Spiegelman. 2003. Peroxisome proliferator-activated receptor-gamma coactivator 1 alpha (PGC-1 alpha): transcriptional coactivator and metabolic regulator. Endocr. Rev. 24: 78-90. (Pubitemid 36223280)
2. Lai, L., T. C. Leone, C. Zechner, P. J. Schaeffer, S. M. Kelly, D. P. Flanagan, D. M. Medeiros, A. Kovacs, and D. P. Kelly. 2008. Transcriptional coactivators PGC-1alpha and PGC-lbeta control overlapping programs required for perinatal maturation of the heart. Genes Dev. 22: 1948-1961. (Pubitemid 352008642)
3. Finck, B. N., and D. P. Kelly. 2006. PGC-1 coactivators: inducible regulators of energy metabolism in health and disease. J. Clin. Invest. 116: 615-622. (Pubitemid 43326866)
4. Rowe, G. C., A. Jiang, and Z. Arany. 2010. PGC-1 coactivators in cardiac development and disease. Circ. Res. 107: 825-838.
5. Banke, N. H., A. R. Wende, T. C. Leone, J. M. O'Donnell, E. D. Abel, D. P. Kelly, and E. D. Lewandowski. 2010. Preferential oxidation of triacylglyceride-derived fatty acids in heart is augmented by the nuclear receptor PPARalpha. Circ. Res. 107: 233-241.
6. Lehman, J. J., P. M. Barger, A. Kovacs, J. E. Saffitz, D. M. Medeiros, and D. P. Kelly. 2000. Peroxisome proliferator-activated receptor gamma coactivator-1 promotes cardiac mitochondrial biogenesis. J. Clin. Invest. 106: 847-856.
7. Lin, J., P. H. Wu, P. T. Tarr, K. S. Lindenberg, J. St-Pierre, C. Y. Zhang, V. K. Mootha, S. Jager, C. R. Vianna, R. M. Reznick, et al. 2004. Defects in adaptive energy metabolism with CNS-linked hyperactivity in PGC-1alpha null mice. Cell. 119: 121-135. (Pubitemid 39349325)
8. Leone, T. C., J. J. Lehman, B. N. Finck, P. J. Schaeffer, A. R. Wende, S. Boudina, M. Courtois, D. F. Wozniak, N. Sambandam, C. Bernal-Mizrachi, et al. 2005. PGC-1alpha deficiency causes multi-system energy metabolic derangements: muscle dysfunction, abnormal weight control and hepatic steatosis. PLoS Biol. 3: e101.
9. Lehman, J. J., S. Boudina, N. H. Banke, N. Sambandam, X. Han, D. M. Young, T. C. Leone, R. W. Gross, E. D. Lewandowski, E. D. Abel, et al. 2008. The transcriptional coactivator PGC-1alpha is essential for maximal and efficient cardiac mitochondrial fatty acid oxidation and lipid homeostasis. Am. J. Physiol. Heart Circ. Physiol. 295: H185-H196.
10. Arany, Z., H. He, J. Lin, K. Hoyer, C. Handschin, O. Toka, F. Ahmad, T. Matsui, S. Chin, P. H. Wu, et al. 2005. Transcriptional coactivator PGC-1 alpha controls the energy state and contractile function of cardiac muscle. Cell Metab. 1: 259-271. (Pubitemid 43960608)
11. Handschin, C., and B. M. Spiegelman. 2006. Peroxisome proliferator-activated receptor gamma coactivator 1 coactivators, energy homeostasis, and metabolism. Endocr. Rev. 27: 728-735. (Pubitemid 44936056)
12. Róna-Vörös, K., and P. Weydt. 2010. The role of PGC-1alpha in the pathogenesis of neurodegenerative disorders. Curr. Drug Targets. 11: 1262-1269.
13. St-Pierre, J., S. Drori, M. Uldry, J. M. Silvaggi, J. Rhee, S. Jager, C. Handschin, K. Zheng, J. Lin, W. Yang, et al. 2006. Suppression of reactive oxygen species and neurodegeneration by the PGC-1 transcriptional coactivators. Cell. 127: 397-408. (Pubitemid 44572377)
14. Ma, D., S. Li, E. K. Lucas, R. M. Cowell, and J. D. Lin. 2010. Neuronal inactivation of peroxisome proliferator-activated receptor gamma coactivator 1alpha (PGC-1alpha) protects mice from diet-induced obesity and leads to degenerative lesions. J. Biol. Chem. 285: 39087-39095.
15. Qin, W., V. Haroutunian, P. Katsel, C. P. Cardozo, L. Ho, J. D. Buxbaum, and G. M. Pasinetti. 2009. PGC-1alpha expression decreases in the Alzheimer disease brain as a function of dementia. Arch. Neurol. 66: 352-361.
16. Han, X., D. M. Holtzman, D. W. McKeel, Jr., J. Kelley, and J. C. Morris. 2002. Substantial sulfatide deficiency and ceramide elevation in very early Alzheimer's disease: potential role in disease pathogenesis. J. Neurochem. 82: 809-818.
17. Cheng, H., J. Xu, D. W. McKeel, Jr., and X. Han. 2003. Specificity and potential mechanism of sulfatide deficiency in Alzheimer's disease: an electrospray ionization mass spectrometric study. Cell. Mol. Biol. 49: 809-818.
18. Han, X., A. M. Fagan, H. Cheng, J. C. Morris, C. Xiong, and D. M. Holtzman. 2003. Cerebrospinal fluid sulfatide is decreased in subjects with incipient dementia. Ann. Neurol. 54: 115-119. (Pubitemid 36764988)
19. Han, X., H. Cheng, J. D. Fryer, A. M. Fagan, and D. M. Holtzman. 2003. Novel role for apolipoprotein E in the central nervous system: modulation of sulfatide content. J. Biol. Chem. 278: 8043-8051. (Pubitemid 36800543)
20. Cheng, H., Y. Zhou, D. M. Holtzman, and X. Han. 2010. Apolipoprotein E mediates sulfatide depletion in amyloid precursor protein transgenic animal models of Alzheimer's disease. Neurobiol. Aging. 31: 1188-1196.
21. Han, X. 2010. The pathogenic implication of abnormal interaction between apolipoprotein E isoforms, amyloid-beta peptides, and sulfatides in Alzheimer's disease. Mol. Neurobiol. 41: 97-106.
22. Han, X., and R. W. Gross. 2005. Shotgun lipidomics: electrospray ionization mass spectrometric analysis and quantitation of the cellular lipidomes directly from crude extracts of biological samples. Mass Spectrom. Rev. 24: 367-412. (Pubitemid 40665798)
23. Han, X., K. Yang, and R. W. Gross. 2011. Multi-dimensional mass spectrometry-based shotgun lipidomics and novel strategies for lipidomic analyses. Mass Spectrom. Rev. Epub ahead of print. July 13, 2011; doi:10.1002/mas.20342.
24. Yang, K., H. Cheng, R. W. Gross, and X. Han. 2009. Automated lipid identification and quantification by multi-dimensional mass spectrometry-based shotgun lipidomics. Anal. Chem. 81: 4356-4368.
25. th edition. The Oily Press, Bridgwater, England.
26. Kiebish, M. A., X. Han, H. Cheng, A. Lunceford, C. F. Clarke, H. Moon, J. H. Chuang, and T. N. Seyfried. 2008. Lipidomic analysis and electron transport chain activities in C57BL/6J mouse brain mitochondria. J. Neurochem. 106: 299-312. (Pubitemid 351840212)
27. Han, X., K. Yang, and R. W. Gross. 2008. Microfluidics-based electrospray ionization enhances intrasource separation of lipid classes and extends identification of individual molecular species through multi-dimensional mass spectrometry: development of an automated high throughput platform for shotgun lipidomics. Rapid Commun. Mass Spectrom. 22: 2115-2124. (Pubitemid 351956698)
28. Jiang, X., H. Cheng, K. Yang, R. W. Gross, and X. Han. 2007. Alkaline methanolysis of lipid extracts extends shotgun lipidomics analyses to the low-abundance regime of cellular sphingolipids. Anal. Biochem. 371: 135-145. (Pubitemid 350015971)
29. Holz, A., N. Schaeren-Wiemers, C. Schaefer, U. Pott, R. J. Colello, and M. E. Schwab. 1996. Molecular and developmental characterization of novel cDNAs of the myelin-associated/oligodendrocytic basic protein. J. Neurosci. 16: 467-477.
30. Ishibashi, T., J. L. Dupree, K. Ikenaka, Y. Hirahara, K. Honke, E. Peles, B. Popko, K. Suzuki, H. Nishino, and H. Baba. 2002. A myelin galactolipid, sulfatide, is essential for maintenance of ion channels on myelinated axon but not essential for initial cluster formation. J. Neurosci. 22: 6507-6514. (Pubitemid 35386407)
31. Smith, R. 1992. The basic protein of CNS myelin: its structure and ligand binding. J. Neurochem. 59: 1589-1608
32. Sun, Y., D. P. Witte, H. Ran, M. Zamzow, S. Barnes, H. Cheng, X. Han, M. T. Williams, M. R. Skelton, C. V. Vorhees, et al. 2008. Neurological deficits and glycosphingolipid accumulation in saposin B deficient mice. Hum. Mol. Genet. 17: 2345-2356.
33. Frank, M., M. E. van der Haar, N. Schaeren-Wiemers, and M. E. Schwab. 1998. rMAL is a glycosphingolipid-associated protein of myelin and apical membranes of epithelial cells in kidney and stomach. J. Neurosci. 18: 4901-4913. (Pubitemid 28285399)
34. Frank, M. 2000. MAL, a proteolipid in glycosphingolipid enriched domains: functional implications in myelin and beyond. Prog. Neurobiol. 60: 531-544. (Pubitemid 30100398)
35. Saravanan, K., N. Schaeren-Wiemers, D. Klein, R. Sandhoff, A. Schwarz, A. Yaghootfam, V. Gieselmann, and S. Franken. 2004. Specific downregulation and mistargeting of the lipid raft-associated protein MAL in a glycolipid storage disorder. Neurobiol. Dis. 16: 396-406. (Pubitemid 38757321)
36. Schaeren-Wiemers, N., A. Bonnet, M. Erb, B. Erne, U. Bartsch, F. Kern, N. Mantei, D. Sherman, and U. Suter. 2004. The raft-associated protein MAL is required for maintenance of proper axon-glia interactions in the central nervous system. J. Cell Biol. 166: 731-742. (Pubitemid 39181010)
37. Han, X. 2004. The role of apolipoprotein E in lipid metabolism in the central nervous system. Cell. Mol. Life Sci. 61: 1896-1906. (Pubitemid 39094797)
38. Han, X. 2007. Potential mechanisms contributing to sulfatide depletion at the earliest clinically recognizable stages of Alzheimer's disease: a tale of shotgun lipidomics. J. Neurochem. 103 (Suppl. 1) : 171-179.
39. Cheng, H., X. Jiang, and X. Han. 2007. Alterations in lipid homeostasis of mouse dorsal root ganglia induced by apolipoprotein E deficiency: a shotgun lipidomics study. J. Neurochem. 101: 57-76. (Pubitemid 46426466)
40. Ruzdijic, S., M. Perovic, A. Mladenovic, D. Milanovic, L. Rakic, S. Petanceska, and S. Kanazir. 2005. The impact of aging, dietary restriction, and glucocorticoids on ApoE gene expression in rat brain. Ann. N. Y. Acad. Sci. 1053: 231-232. (Pubitemid 43031101)
41. Cui, L., H. Jeong, F. Borovecki, C. N. Parkhurst, N. Tanese, and D. Krainc. 2006. Transcriptional repression of PGC-1alpha by mutant huntingtin leads to mitochondrial dysfunction and neurodegeneration. Cell. 127: 59-69. (Pubitemid 44466642)
42. Vos, J. P., M. Lopes-Cardozo, and B. M. Gadella. 1994. Metabolic and functional aspects of sulfogalactolipids. Biochim. Biophys. Acta. 1211: 125-149. (Pubitemid 24076045)
43. Ishizuka, I. 1997. Chemistry and functional distribution of sulfoglycolipids. Prog. Lipid Res. 36: 245-319. (Pubitemid 28132555)
44. Ikami, T., H. Ishida, and M. Kiso. 2000. Synthesis and biological activity of glycolipids, with a focus on gangliosides and sulfatide analogs. Methods Enzymol. 311: 547-568.
45. Marcus, J., and B. Popko. 2002. Galactolipids are molecular determinants of myelin development and axo-glial organization. Biochim. Biophys. Acta. 1573: 406-413. (Pubitemid 35335451)
46. von Figura, K., V. Gieselmann, and J. Jaeken. 2001. Metachromatic leukodystrophy: lysosomal disorders. In The Metabolic and Molecular Bases of Inherited Diseases. H. S. Sachdev, A. L. Beaudet, W. S. Sly, and D. Valle, editors. McGraw-Hill, New York. 3695-3724.
47. Molander-Melin, M., Z. Pernber, S. Franken, V. Gieselmann, J. E. Mansson, and P. Fredman. 2004. Accumulation of sulfatide in neuronal and glial cells of arylsulfatase A deficient mice. J. Neurocytol. 33: 417-427. (Pubitemid 39463164)
48. Bosio, A., E. Binczek, and W. Stoffel. 1996. Functional breakdown of the lipid bilayer of the myelin membrane in central and peripheral nervous system by disrupted galactocerebroside synthesis. Proc. Natl. Acad. Sci. USA. 93: 13280-13285. (Pubitemid 26382807)
49. Coetzee, T., N. Fujita, J. Dupree, R. Shi, A. Blight, K. Suzuki, and B. Popko. 1996. Myelination in the absence of galactocerebroside and sulfatide: normal structure with abnormal function and regional instability. Cell. 86: 209-219. (Pubitemid 26286104)
50. Coetzee, T., J. L. Dupree, and B. Popko. 1998. Demyelination and altered expression of myelin-associated glycoprotein isoforms in the central nervous system of galactolipid-deficient mice. J. Neurosci. Res. 54: 613-622. (Pubitemid 28546064)
51. Bosio, A., H. Bussow, J. Adam, and W. Stoffel. 1998. Galac to sphingolipids and axono-glial interaction in myelin of the central nervous system. Cell Tissue Res. 292: 199-210. (Pubitemid 28230207)
52. Marcus, J., S. Honigbaum, S. Shroff, K. Honke, J. Rosenbluth, and J. L. Dupree. 2006. Sulfatide is essential for the maintenance of CNS myelin and axon structure. Glia. 53: 372-381.
53. nd ASMS Conference, Nashville, TN, May 23-27, 2004).
54. Liang, Y., S. Lin, T. P. Beyer, Y. Zhang, X. Wu, K. R. Bales, R. B. DeMattos, P. C. May, S. D. Li, X. C. Jiang, et al. 2004. A liver X receptor and retinoid X receptor heterodimer mediates apolipoprotein E expression, secretion and cholesterol homeostasis in astrocytes. J. Neurochem. 88: 623-634. (Pubitemid 38140207)
55. Hirsch-Reinshagen, V., L. F. Maia, B. L. Burgess, J. F. Blain, K. E. Naus, S. A. McIsaac, P. F. Parkinson, J. Y. Chan, G. H. Tansley, M. R. Hayden, et al. 2005. The absence of ABCA1 decreases soluble ApoE levels but does not diminish amyloid deposition in two murine models of Alzheimer disease. J. Biol. Chem. 280: 43243-43256. (Pubitemid 43049291)
56. Koldamova, R., M. Staufenbiel, and I. Lefterov. 2005. Lack of ABCA1 considerably decreases brain ApoE level and increases amyloid deposition in APP23 mice. J. Biol. Chem. 280: 43224-43235. (Pubitemid 43049289)
57. Li, A. C., and C. K. Glass. 2004. PPAR- and LXR-dependent pathways controlling lipid metabolism and the development of atherosclerosis. J. Lipid Res. 45: 2161-2173. (Pubitemid 39602963)
58. Jiang, Q., M. Heneka, and G. E. Landreth. 2008. The role of peroxisome proliferator-activated receptor-gamma (PPARgamma) in Alzheimer's disease: therapeutic implications. CNS Drugs. 22: 1-14. (Pubitemid 350243363)
59. Chawla, A., W. A. Boisvert, C. H. Lee, B. A. Laffitte, Y. Barak, S. B. Joseph, D. Liao, L. Nagy, P. A. Edwards, L. K. Curtiss, et al. 2001. A PPAR gamma-LXR-ABCA1 pathway in macrophages is involved in cholesterol efflux and atherogenesis. Mol. Cell. 7: 161-171. (Pubitemid 32162909)
60. Yoshikawa, T., T. Ide, H. Shimano, N. Yahagi, M. Amemiya-Kudo, T. Matsuzaka, S. Yatoh, T. KitamineI, H. Okazaki, Y. Tamura, et al. 2003. Cross-talk between peroxisome proliferator-activated receptor (PPAR) and liver X receptor (LXR) in nutritional regulation of fatty acid metabolism. I. PPARs suppress sterol regulatory element binding protein-1c promoter through inhibition of LXR signaling. Mol. Endocrinol. 17: 1240-1254. (Pubitemid 36819948)
61. Corton, J. C., U. Apte, S. P. Anderson, P. Limaye, L. Yoon, J. Latendresse, C. Dunn, J. I. Everitt, K. A. Voss, C. Swanson, et al. 2004. Mimetics of caloric restriction include agonists of lipidactivated nuclear receptors. J. Biol. Chem. 279: 46204-46212. (Pubitemid 39491615)