Differential effects of simvastatin and pravastatin on expression of Alzheimer's disease-related genes in human astrocytes and neuronal cells

Journal of Lipid Research

Volumn 50, Issue 10, 2009, Pages 2095-2102

  Dong, Weijiang ^a,b   Vuletic, Simona ^a   Albers, John J ^b  

^a UNIVERSITY OF WASHINGTON   (United States)

^b MEDICAL SCHOOL OF XI AN JIAOTONG UNIVERSITY   (China)

Author keywords

Amyloid precursor protein; Apolipoprotein E; ATP binding cassette transporter A1; Gene expression; Microtubule associated protein tau; Phospholipid transfer protein

Indexed keywords

ABC TRANSPORTER A1; AMYLOID PRECURSOR PROTEIN; APOLIPOPROTEIN E; CYCLIN DEPENDENT KINASE 5; GLYCOGEN SYNTHASE KINASE 3BETA; PRAVASTATIN; SIMVASTATIN; TAU PROTEIN;

ALZHEIMER DISEASE; ANIMAL CELL; ARTICLE; ASTROCYTE; CONTROLLED STUDY; DRUG ACTIVITY; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETIC ANALYSIS; HUMAN; HUMAN CELL; NERVE CELL; NERVE DEGENERATION; NEUROBLASTOMA; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION;

ALZHEIMER DISEASE; APOLIPOPROTEINS E; ASTROCYTES; ATP-BINDING CASSETTE TRANSPORTERS; BLOTTING, WESTERN; CELLS, CULTURED; ELECTROPHORESIS; GENE EXPRESSION; HUMANS; HYDROXYMETHYLGLUTARYL-COA REDUCTASE INHIBITORS; NEURONS; PHOSPHOLIPID TRANSFER PROTEINS; POLYMERASE CHAIN REACTION; PRAVASTATIN; SIMVASTATIN; TAU PROTEINS;

EID: 70350351085     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M900236-JLR200     Document Type: Article

References (53)

1. Auer, J., and B. Eber. 2001. A clinical focus on statins. Curr. Opin. Investig. Drugs. 2: 382-388.
2. Jick, H., G. L. Zornberg, S. S. Jick, S. Seshadri, and D. A. Drachman. 2000. Statins and the risk of dementia. Lancet. 356: 1627-1631.
3. Wolozin, B., W. Kellman, P. Ruosseau, G. G. Celesia, and G. Siegal. 2000. Decreased prevalence of Alzheimer disease associated with 3-hydroxy-3methylglutaryl coenzyme A reductase inhibitors. Arch. Neurol. 57: 1439-1443.
4. Hajjar, I., J. Schumpert, V. Hirth, D. Wieland, and G. P. Eleazer. 2002. The impact of the use of statins on the prevalence of dementia and the progression of cognitive impairment. J. Gerontol. A Biol. Sci. Med. Sci. 57: M414-M418.
5. Rockwood, K., S. Kirkland, D. B. Hogan, C. MacKnight, H. Merry, R. Verreault, C. Wolfson, and I. McDowell. 2002. Use of lipid-lowering agents, indication bias, and the risk of dementia in community-dwelling elderly people. Arch. Neurol. 59: 223-227.
6. Zamrini, E., G. McGwin, and J. M. Roseman. 2004. Association between statin use and Alzheimer's disease. Neuroepidemiology. 23: 94-98.
7. Friedhoff, L. T., E. I. Cullen, N. S. Goeghagen, and J. D. Buxbaum. 2001. Treatment with controlled-release lovastatin decreases serum concentrations of human beta-amyloid (A beta) peptide. Int. J. Neuropsychopharmacol. 4: 127-130.
8. Fassbender, K., M. Stroick, T. Bertsch, A. Ragoschke, S. Kuehl, S. Walter, K. Brechtel, F. Muehlhauser, K. von Bergmann, and D. Lutjohann. 2002. Effects of statins on human cerebral cholesterol metabolism and secretion of Alzheimer amyloid peptide. Neurology. 59: 1257-1258.
9. Locatelli, S., D. Lutjohann, H. H. Schimdt, C. Otto, U. Beisiegel, and K. von Bergmann. 2002. Reduction of plasma 24S-hydroxy cholesterol (cerebrosterol) levels using high-dosage simvastatin in patients with hypercholesterolemia: evidence that simvastatin affects cholesterol metabolism in the human brain. Arch. Neurol. 59: 213-216.
10. Simons, M., F. Schwarzler, D. Lutjohann, K. von Bergmann, K. Beyreuther, J. Dichgans, H. Wormstall, T. Hartmann, and J. B. Schulz. 2002. Treatment with simvastatin in normocholesterolemic patients with Alzheimer's disease: a 26-week randomized, placebo-controlled, double-blind trial. Ann. Neurol. 52: 346-350.
11. Vega, G. L., M. F. Weiner, A. M. Lipton, K. von Bergmann, D. Lutjohann, C. Moore, and D. Svetlik. 2003. Reduction in levels of 24S-hydroxycholesterol by statin treatment in patients with Alzheimer disease. Arch. Neurol. 60: 510-515.
12. Doraiswamy, P. M., D. C. Steffens, and D. R. McQipod. 2004. Statin use and hippocampal volumes in elderly subjects at risk for Alzheimer's disease: a pilot observational study. Am. J. Alzheimers Dis. Other Demen. 19: 275-278.
13. Algotsson, A., and B. Winblad. 2004. Patients with Alzheimer's disease may be particularly susceptible to adverse effects of statins. Dement. Geriatr. Cogn. Disord. 17: 109-116.
14. Orsi, A., O. Sherman, and Z. Woldeselassie. 2001. Simvastatinassociated memory loss. Pharmacotherapy. 21: 767-769.
15. King, D. S., A. J. Wilburn, M. R. Wofford, T. K. Harrell, B. J. Lindley, and D. W. Jones. 2003. Cognitive impairment associated with atorvastatin and simvastatin. Pharmacotherapy. 23: 1663-1667.
16. Wagstaff, L. R., M. W. Mitton, B. M. Arvik, and P. M. Doraiswamy. 2003. Statin-associated memory loss: analysis of 60 case reports and review of the literature. Pharmacotherapy. 23: 871-880.
17. Riekse R. G., G. Li, E. C. Petrie, J. B. Leverenz, D. Vavrek, S. Vuletic, J. J. Albers, T. J. Montine, V. M. Lee, M. Lee, et al. 2006. Effects of statins on Alzheimer's disease biomarkers in cerebrospinal fluid. J. Alzheimers Dis. 9: 1-8.
18. Vuletic, S., R. G. Riekse, S. M. Marcovina, E. R. Peskind, W. R. Hazzard, and J. J. Albers. 2006. Statins of different brain penetrability differentially affect CSF PLTP activity. Dement. Geriatr. Cogn. Disord. 22: 392-398.
19. Yagle, K., H. Lu, M. Guizzetti, T. Moller, and L. G. Costa. 2001. Activation of mitogen-activated protein kinase by muscarinic receptors in astroglial cells: role in DNA synthesis and effect of ethanol. Glia. 35: 111-120.
20. Cheung, M. C., G. Wolfbauer, and J. J. Albers. 1996. Plasma phospholipid mass transfer rate: relationship to plasma phospholipid and cholesteryl ester transfer activities and lipid parameters. Biochim. Biophys. Acta. 1303: 103-110.
21. Hiesberger, T., M. Trommsdorff, B. W. Howell, A. Goffi net, M. C. Mumby, J. A. Cooper, and J. Herz. 1999. Direct binding of Reelin to VLDL receptor and apoE receptor 2 induces tyrosine phosphorylation of disabled-1 and modulates tau phosphorylation. Neuron. 24: 481-489.
22. Wen, Y., E. Planel, M. Herman, H. Y. Figueroa, L. Wang, L. Liu, L. F. Lau, W. H. Yu, and K. E. Duff. 2008. Interplay between cyclin-dependent kinase 5 and glycogen synthase kinase 3 beta mediated by neuregulin signaling leads to differential effects on tau phosphorylation and amyloid precursor protein processing. J. Neurosci. 28: 2624-2632.
23. Oram, J. F. 2003. HDL apolipoproteins and ABCA1: partners in the removal of excess cellular cholesterol. Arterioscler. Thromb. Vasc. Biol. 23: 720-727.
24. Hirsch-Reinshagen, V., S. Zhou, B. L. Burgess, L. Bernier, S. A. McIsaac, J. Y. Chan, G. H. Tansley, J. S. Cohn, M. R. Hayden, and C. L. Wellington. 2004. Deficiency of ABCA1 impairs apolipoprotein E metabolism in brain. J. Biol. Chem. 279: 41197-41207.
25. Wahrle, S. E., H. Jiang, M. Parsadanian, J. Legleiter, X. Han, J. D. Fryer, T. Kowalewski, and D. M. Holtzman. 2004. ABCA1 is required for normal central nervous system apoE levels and for lipidation of astrocyte-secreted apoE. J. Biol. Chem. 279: 40987-40993.
26. Roheim, P. S., M. Carey, T. Forte, and G. L. Vega. 1979. Apolipoproteins in human cerebrospinal fluid. Proc. Natl. Acad. Sci. USA. 76: 4646-4649.
27. Pitas, R. E., J. K. Boyles, S. H. Lee, D. Hui, and K. H. Weisgraber. 1987. Lipoproteins and their receptors in the central nervous system. Characterization of the lipoproteins in cerebrospinal fluid and identification of apolipoprotein B, E (LDL) receptors in the brain. J. Biol. Chem. 262: 14352-14360.
28. Linton, M. F., R. Gish, S. T. Hubl, E. Butler, C. Esquivel, W. I. Bry, J. K. Boyles, M. R. Wardell, and S. G. Young. 1991. Phenotypes of apolipoprotein B and apolipoprotein E after liver transplantation. J. Clin. Invest. 88: 270-281.
29. Hoe, H. S., A. Pocivavsek, H. Dai, G. Chakraborty, D. C. Harris, and G. W. Rebeck. 2006. Effects of apoE on neuronal signaling and APP processing in rodent brain. Brain Res. 1112: 70-79.
30. Handelmann, G. E., J. K. Boyles, K. H. Weisgraber, R. H. Mahley, and R. E. Pitas. 1992. Effects of apolipoprotein E, very low-density lipoproteins, and cholesterol on the extension of neurites by rabbit dorsal root ganglion neurons in vitro. J. Lipid Res. 33: 1677-1688.
31. Ignatius, M. J., P. J. Gebicke-Harter, J. H. Skene, J. W. Schilling, K. H. Weisgraber, R. W. Mahley, and E. M. Shooter. 1986. Expression of apolipoprotein E during nerve degeneration and regeneration. Proc. Natl. Acad. Sci. USA. 83: 1125-1129.
32. Boyles, J. K., C. D. Zoellner, L. J. Anderson, L. M. Kosik, R. E. Pitas, K. H. Weisgraber, D. Y. Hui, R. W. Mahley, P. J. Gebicke-Haerter, and M. J. Ignatius. 1989. A role for apolipoprotein E, apolipoprotein A-I, and low density lipoprotein receptors in cholesterol transport during regeneration and remyelination of the rat sciatic nerve. J. Clin. Invest. 83: 1015-1031.
33. Graham, D. I., K. Horsburgh, J. A. Nicoll, and G. M. Taesdale. 2000. Apolipoprotein E and the response of the brain to injury. Acta Neurochir. Suppl. 73: 89-92.
34. Helkala, E. L., K. Koivisto, T. Hanninen, M. Vanhanen, K. Kervinen, J. Kuusisto, L. Mykkanen, Y. A. Kesaniemi, M. Laakso, and P. Sr. Riekkinen. 1995. The association of apolipoprotein E polymorphism with memory: a population based study. Neurosci. Lett. 191: 141-144.
35. Gordon, I., E. Grauer, I. Genis, E. Sehayek, and D. M. Michaelson. 1995. Memory deficits and cholinergic impairments in apolipoprotein E-deficient mice. Neurosci. Lett. 199: 1-4.
36. Trommer, B. L., C. Shah, S. H. Yun, G. Gamkrelidze, E. S. Pasternak, W. B. Stine, A. Manelli, P. Sullivan, J. F. Pasternak, and M. J. LaDu. 2005. ApoE isoform-specific effects on LTP: blockade by oligomeric amyloid-beta 1-42. Neurobiol. Dis. 18: 75-82.
37. Mauch, D. H., J. Nagler, S. Schumacher, E. C. Gortiz, A. Otto, and F. W. Pfrieger. 2001. CNS synaptogenesis promoted by glia-derived cholesterol. Science. 294: 1354-1357.
38. Koudinov, A. R., and N. V. Koudinova. 2001. Essential role for cholesterol in synaptic plasticity and neuronal degeneration. FASEB J. 15: 1858-1860.
39. Soderberg, M., C. Edlund, K. Kristensson, and G. Dallner. 1990. Lipid composition of different regions of the human brain during aging. J. Neurochem. 54: 415-423.
40. Soderberg, M., C. Edlund, K. Kristensson, and G. Dallner. 1991. Fatty acid composition of brain phospholipids in aging and in Alzheimer's disease. Lipids. 26: 412-425.
41. Svennerholm, L., K. Bostrom, C. G. Helander, and B. Jungbjer. 1991. Membrane lipids in the aging human brain. J. Neurochem. 56: 2051-2059.
42. Svennerholm, L., K. Bostrom, B. Jungbjer, and L. Olsson. 1994. Membrane lipids of adult human brain: lipid composition of frontal and temporal lobe in subjects of age 20 to 100 years. J. Neurochem. 63: 1802-1811.
43. Pantlia, A. S., M. K. Pantlia, A. K. Singh, and I. Singh. 2008. Inhibition of rho family functions by lovastatin promotes myelin repair in ameliorating experimental autoimmune encephalomyelitis. Mol. Pharmacol. 73: 1381-1393.
44. Bar-On, P., L. Crews, A. O. Koob, H. Mizuno, A. Adame, B. Spencer, and E. Masliah. 2008. Statins reduce neuronal alpha-synuclein aggregation in in vitro models of Parkinson's disease. J. Neurochem. 105: 1656-1667.
45. Schuster, S., A. Nadjar, J. T. Guo, Q. Li, C. Ittrich, B. Hengerer, and E. Bezard. 2008. The 3-hydroxy-3-methylglutaryl-CoA reductase inhibitor lovastatin reduces severity of L-DOPA-induced abnormal involuntary movements in experimental Parkinson's disease. J. Neurosci. 28: 4311-4316.
46. Wu, H., D. Lu, H. Jiang, Y. Xiong, C. Qu, B. Li, A. Mahmood, D. Zhou, and M. Chopp. 2008. Simvastatin-mediated upregulation of VEGF and BDNF, activation of the PI3K/Akt pathway, and increase of neurogenesis are associated with therapeutic improvement after traumatic brain injury. J. Neurotrauma. 25: 130-139.
47. Wang, H., J. R. Lynch, P. Song, H. J. Yang, R. B. Yates, B. Mace, D. S. Warner, J. R. Guyton, and D. T. Laskowitz. 2007. Simvastatin and atorvastatin improve behavioral outcome, reduce hippocampal degeneration, and improve cerebral blood fl ow after experimental traumatic brain injury. Exp. Neurol. 206: 59-69.
48. Coetsee, T. N., P. J. Pretorius, G. Terre'blanche, and J. J. Bergh. 2008. Investigating the potential neuroprotective effects of statins on DNA damage in mouse striatum. Food Chem. Toxicol. 46: 3186-3192.
49. Konat, G. W., A. Krasowska-Zoladek, and M. Kraszpulski. 2008. Statins enhance toll-like receptor 4-mediated cytokine gene expression in astrocytes: implication of Rho proteins in negative feedback regulation. J. Neurosci. Res. 86: 603-609.
50. Tsai, H. I., L. H. Tsai, M. Y. Chen, and Y. C. Chou. 2006. Cholesterol defi ciency perturbs actin signaling and glutamate homeostasis in hippocampal astrocytes. Brain Res. 1104: 27-38.
51. Pannu, R., E. Barbosa, A. K. Singh, and I. Singh. 2005. Attenuation of acute infl ammatory response by atorvastatin after spinal cord injury in rats. J. Neurosci. Res. 79: 340-350.
52. Pahan, K., F. G. Sheikh, A. M. Namboodiri, and I. Singh. 1997. Lovastatin and phenylacetate inhibit the induction of nitric oxide synthase and cytokines in rat primary astrocytes, microglia, and macrophages. J. Clin. Invest. 100: 2671-2679.
53. Pavlov, O. V., Yu. V. Bobryshev, Yu. V. Balabanov, and K. Ashwell. 1995. An in vitro study of the effects of lovastatin on human fetal brain cells. Neurotoxicol. Teratol. 17: 31-39.