Cholesterol metabolism changes under long-term dietary restrictions while the cholesterol homeostasis remains unaffected in the cortex and hippocampus of aging rats

Age

Volumn 36, Issue 3, 2014, Pages 1303-1314

  Smiljanic, Kosara ^a   Vanmierlo, Tim ^b   Mladenovic Djordjevic, Aleksandra ^a   Perovic, Milka ^a   Ivkovic, Sanja ^c   Lütjohann, Dieter ^d   Kanazir, Selma ^a  

^a UNIVERSITY OF BELGRADE   (Serbia)

^b HASSELT UNIVERSITY   (Belgium)

^c Institute for Molecular Medicine   (Portugal)

^d UNIVERSITY HOSPITAL BONN   (Germany)

Author keywords

24S hydroxycholesterol; Brain cholesterol metabolism; Dietary restriction; Hippocampus; Phytosterols; Rat cortex

Indexed keywords

CAMPESTEROL; CHOLESTEROL; CHOLESTEROL DERIVATIVE; DESMOSTEROL; HYDROXYCHOLESTEROL; LANOSTEROL; PHYTOSTEROL; SITOSTEROL; STIGMASTEROL; UNCLASSIFIED DRUG;

AGING; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CHOLESTEROL METABOLISM; CHOLESTEROL SYNTHESIS; CHOLESTEROL TRANSPORT; CONTROLLED STUDY; DEGRADATION; DIET RESTRICTION; FOOD INTAKE; HIPPOCAMPUS; HOMEOSTASIS; MALE; MASS FRAGMENTOGRAPHY; NONHUMAN; PROTEIN EXPRESSION; RAT; SERUM; WESTERN BLOTTING; WISTAR RAT; ANIMAL; FOLLOW UP; METABOLISM; PROCEDURES; PROTEIN RESTRICTION; TIME;

AGING; ANIMALS; CEREBRAL CORTEX; CHOLESTEROL; DIET, PROTEIN-RESTRICTED; FOLLOW-UP STUDIES; HIPPOCAMPUS; MALE; RATS; RATS, WISTAR; TIME FACTORS;

EID: 84905399905     PISSN: 01619152     EISSN: 15744647     Source Type: Journal    
DOI: 10.1007/s11357-014-9654-z     Document Type: Article

References (53)

1. Adams MM, Shi L, Linville MC, Forbes ME, Long AB, Bennett C, Newton IG, Carter CS, Sonntag WE, Riddle DR, Brunso-Bechtold JK (2008) Caloric restriction and age affect synaptic proteins in hippocampal CA3 and spatial learning ability. Exp Neurol 211:141-149
2. Asha Devi S (2009) Aging brain: prevention of oxidative stress by vitamin E and exercise. Sci World J 9:366-372
3. Bjorkhem I, Starck L, Andersson U, Lütjohann D, von Bahr S, Pikuleva I, Babiker A, Diczfalusy U (2001) Oxysterols in the circulation of patients with the Smith-Lemli-Opitz syndrome: abnormal levels of 24S- and 27-hydroxycholesterol. J Lipid Res 42:366-371 (Pubitemid 32270060)
4. Burke SN, Barnes CA (2006) Neural plasticity in the aging brain. Nat Neurosci 7:30-40
5. Camargo N, Brouwers JF, Loos M, Gutmann DH, Smit AB, Verheijen MH (2012) High-fat diet ameliorates neurological deficits caused by defective astrocyte lipid metabolism. FASEB J 6(10):4302-4315
6. Couillard-Despres S, Iglseder B, Aigner L (2011) Neurogenesis, cellular plasticity and cognition: the impact of stem cells in the adult and aging brain- a mini-review. Gerontology 57(6):559-564
7. Cutler RG, Mattson MP (2006) The adversities of aging. Ageing Res Rev 5:221-238
8. De Marinis E, Martini C, Trentalance A, Pallottini V (2008) Sex differences in hepatic regulation of cholesterol homeostasis. J Endocrinol 198(3):635-643
9. Dietschy JM, Turley SD (2001) Cholesterol metabolism in the brain. Curr Opin Lipidol 12(2):105-112 (Pubitemid 32242918)
10. Fon Tacer K, Pompon D, Rozman D (2010) Adaptation of cholesterol synthesis to fasting and TNF-alpha: profiling cholesterol intermediates in the liver, brain, and testis. J Steroid Biochem Mol Biol 121:619-625
11. Fontán-Lozano A, López-Lluch G, Delgado-García JM, Navas P, Carrión AM (2008) Molecular bases of caloric restriction regulation of neuronal synaptic plasticity. Mol Neurobiol 38(2):167-177
12. Goldstein JL, Brown MS (1990) Regulation of the mevalonate pathway. Nature 343(6257):425-430
13. Goritz C, Mauch DH, Frank W, Pfrieger FW (2005) Multiple mechanisms mediate cholesterol-induced synaptogenesis in a CNS neuron. Mol Cell Neurosci 29:190-201 (Pubitemid 40725610)
14. Hac-Wydro K, Wydro P, Dynarowicz-Łatka P, Paluch M (2009) Cholesterol and phytosterols effect on sphingomyelin/phosphatidylcholine model membranes - thermodynamic analysis of the interactions in ternary monolayers. J Colloid Interface Sci 329(2):265-272
15. Halagappa VK, Guo Z, Pearson M, Matsuoka Y, Cutler RG, Laferla FM, Mattson MP (2007) Intermittent fasting and caloric restriction ameliorate age-related behavioral deficits in the triple-transgenic mouse model of Alzheimer 's disease. Neurobiol Dis 26:212-220 (Pubitemid 46436499)
16. Hayakawa K, Mishima K, Nozako M, Hazekawa M, Aoyama Y, Ogata A, Harada K, Fujioka M, Abe K, Egashira N, Iwasaki K, Fujiwara M (2007) High-cholesterol feeding aggravates cerebral infarction via decreasing the CB1 receptor. Neurosci Lett 414:183-187 (Pubitemid 46273995)
17. Jansen PJ, Lutjohann D, Abildayeva K, Vanmierlo T, Plosch T, Plat J, von Bergmann K, Groen AK, Ramaekers FC, Kuipers F, Mulder M (2006) Dietary plant sterols accumulate in the brain. Biochim Biophys Acta 1761:445-453 (Pubitemid 43776461)
18. Jansen M, Wang W, Greco D, Bellenchi GC, di Porzio U, Brown AJ, Ikonen E (2013) What dictates the accumulation of desmosterol in the developing brain? FASEB J 27(3):865-870
19. Jessberger S, Gage FH (2008) Stem-cell-associated structural and functional plasticity in the aging hippocampus. Psychol Aging 23(4):684-691
20. Karasinska JM, Rinninger F, Lütjohann D, Ruddle P, Franciosi S, Kruit JK, Singaraja RR, Hirsch-Reinshagen V, Fan J, Brunham LR, Bissada N, Ramakrishnan R, Wellington CL, Parks JS, Hayden MR (2009) Specific loss of brain ABCA1 increases brain cholesterol uptake and influences neuronal structure and function. J Neurosci 29:3579-3589
21. Koivisto H, Grimm MO, Rothhaar TL, Berkecz R, Lütjohann D, Giniatullina R, Takalo M, Miettinen PO, Lahtinen HM, Giniatullin R, Penke B, Janáky T, Broersen LM, Hartmann T, Tanila H (2014) Special lipid-based diets alleviate cognitive deficits in the APPswe/PS1dE9 transgenic mouse model of Alzheimer 's disease independent of brain amyloid deposition. J Nutr Biochem 25(2):157-169
22. Ledesma MD, Martin MG, Dotti CG (2012) Lipid changes in the aged brain: effect on synaptic function and neuronal survival. Prog Lipid Res 51(1):23-35
23. Li-Hawkins J, Lund EG, Turley SD, Russell DW (2000) Disruption of the oxysterol 7alpha-hydroxylase gene in mice. J Biol Chem 275:16536-16542 (Pubitemid 30398877)
24. Lund EG, Guileyardo JM, Russell DW (1999) cDNA cloning of cholesterol 24-hydroxylase, amediator of cholesterol homeostasis in the brain. Proc Natl Acad Sci U S A 96:7238-7243 (Pubitemid 29299645)
25. Lutjohann D, Brzezinka A, Barth E, Abramowski D, Staufenbiel M, von Bergmann K, Beyreuther K, Multhaup G, Bayer TA (2002) Profile of cholesterol-related sterols in aged amyloid precursor protein transgenic mouse brain. J Lipid Res 43: 1078-1085 (Pubitemid 34760879)
26. Martini C, Pallottini V, Cavallini G, Donati A, Bergamini E, Trentalance A (2007) Caloric restrictions affect some factors involved in age-related hypercholesterolemia. J Cell Biochem 101:235-243 (Pubitemid 46652587)
27. Martini C, Pallottini V, De Marinis E, Marino M, Cavallini G, Donati A, Straniero S, Trentalance A (2008) Omega-3 as well as caloric restriction prevent the age-related modifications of cholesterol metabolism. Mech Ageing Dev 129:722-727
28. Mauch DH, Nagler K, Schumacher S et al (2001) CNS synaptogenesis promoted by glia-derived cholesterol. Science 294: 1354-1357 (Pubitemid 33063104)
29. Means LW, Higgins JL, Fernandez TJ (1993) Mid-life onset of dietary restriction extends life and prolongs cognitive functioning. Physiol Behav 54:503-508 (Pubitemid 23257187)
30. Mladenovic Djordjevic A, Perovic M, Tesic V, Tanic N, Rakic L, Ruzdijic S, Kanazir S (2010) Long-term dietary restriction modulates the level of presynaptic proteins in the cortex and hippocampus of the aging rat. Neurochem Int 56:250-255
31. Mora F, Segovia G, del Arco A (2007) Aging, plasticity and environmental enrichment: structural changes and neurotransmitter dynamics in several areas of brain. Brain Res Rev 55:78-88 (Pubitemid 47422232)
32. Mulas MF, Demuro G, Mulas C, Putzolu M, Cavallini G, Donati A, Bergamini E, Dessi S (2005) Dietary restriction counteracts age-related changes in cholesterol metabolism in the rat. Mech Ageing Dev 126:648-654 (Pubitemid 40693287)
33. Pallottini V, Marino M, Cavallini G, Bergamini E, Trentalance A (2003) Age-related changes of isoprenoid biosynthesis in rat liver and brain. Biogerontology 4:371-378 (Pubitemid 38088148)
34. Park JH, Glass Z, Sayed K, Michurina TV, Lazutkin A, Mineyeva O, Velmeshev D, Ward WF, Richardson A, Enikolopov G (2013) Calorie restriction alleviates the age-related decrease in neural progenitor cell division in the aging brain. Eur J Neurosci 37(12):1987-1993
35. Perovic M, Mladenovic Djordjevic A, Smiljanic K, Tanic N, Rakic L, Ruzdijic S, Kanazir S (2009) Expression of cholesterol homeostasis genes in the brain of the male rat is affected by age and dietary restriction. Biogerontology 10:735-745
36. Peterson DW(1958) Plant sterols and tissue cholesterol levels. Am J Clin Nutr 6:644-649
37. Pfrieger F (2002) Outsourcing in the brain: do neurons depend on cholesterol delivery by astrocytes. Bioessays 25:72-76
38. Pfrieger FW (2003) Role of cholesterol in synapse formation and function. Biochim Biophys Acta 1610:271-280
39. Pfrieger FW, Ungerer N (2011) Cholesterolmetabolismin neurons and astrocytes. Prog Lipid Res 50:357-371
40. Plat J, van Onselen EN, van Heugten MM, Mensink RP (2000) Effects on serum lipids, lipoproteins and fat soluble antioxidant concentrations of consumption frequency of margarines and shortenings enriched with plant stanol esters. Eur J Clin Nutr 54:671-677
41. Saito K, Dubreuil V, Arai Y, Wilsch-Bräuninger M, Schwudke D, Saher G, Miyata T, Breier G, Thiele C, Shevchenko A, Nave KA, Huttner WB (2009) Ablation of cholesterol biosynthesis in neural stem cells increases their VEGF expression and angiogenesis but causes neuron apoptosis. Proc Natl Acad Sci U S A 106:8350-8355
42. Sato Y, Suzuki I, Nakamura T, Bernier F, Aoshima K, Oda Y (2012) Identification of a new plasma biomarker of Alzheimer's disease using metabolomics technology. J Lipid Res 53(3):567-576
43. Segatto M, Trapani L, Lecis C, Pallottini V (2012) Regulation of cholesterol biosynthetic pathway in different regions of the rat central nervous system. Acta Physiol (Oxf) 206(1):62- 71
44. Segovia G, Yagüe AG, García-Verdugo JM, Mora F (2006) Environmental enrichment promotes neurogenesis and changes the extracellular concentrations of glutamate and GABA in the hippocampus of aged rats. Brain Res Bull 70: 8-14 (Pubitemid 43796308)
45. Siperstein MD, Fagan VM (1966) Feedback control of mevalonate synthesis by dietary cholesterol. J Biol Chem 241(3):602-609
46. Smiljanic K, Vanmierlo T, Mladenovic Djordjevic A, Perovic M, Loncarevic-Vasiljkovic N, Tesic V, Lj R, Ruzdijic S, Lutjohann D, Kanazir S (2013) Aging induces tissuespecific changes in cholesterol metabolism in rat brain and liver. Lipids 48:1069-1077
47. Stranahan AM, Cutler RG, Button C, Telljohann R, Mattson MP (2011) Diet-induced elevations in serum cholesterol are associated with alterations in hippocampal lipid metabolism and increased oxidative stress. J Neurochem 118(4):611-615
48. Thelen KM, Falkai P, Bayer TA, Lutjohann D (2006) Cholesterol synthesis rate in human hippocampus declines with aging. Neurosci Lett 403(1-2):15-19 (Pubitemid 43963235)
49. Trapani L and Pallottini V (2010) Age-related hypercholesterolemia and HMG-CoA reductase dysregulation: sex does matter (a gender perspective). Curr Gerontol Geriatr Res. doi:10. 1155/2010/420139
50. Vainio S, Jansen M, Koivusalo M, Róg T, Karttunen M, Vattulainen I, Ikonen E (2006) Significance of sterol structural specificity. Desmosterol cannot replace cholesterol in lipid rafts. J Biol Chem 281:348-355 (Pubitemid 43671195)
51. Vanmierlo T, Rutten K, van Vark-van der Zee LC, Friedrichs S, Bloks VW, Blokland A, Ramaekers FC, Sijbrands E, Steinbusch H, Prickaerts J, Kuipers F, Lütjohann D, Mulder M (2011) Cerebral accumulation of dietary derivable plant sterols does not interfere with memory and anxiety related behavior in Abcg5-/-mice. Plant Foods Hum Nutr 66(2):149-156
52. Vanmierlo T, Weingärtner O, van der Pol S, Husche C, Kerksiek A, Friedrichs S, Sijbrands E, Steinbusch H, Grimm M, Hartmann T, Laufs U, Böhm M, de Vries HE, Mulder M, Lütjohann D (2012) Dietary intake of plant sterols stably increases plant sterol levels in the murine brain. J Lipid Res 53(4):726-735
53. Wechsler A, Brafman A, Shafir M, Heverin M, Gottlieb H, Damari G, Gozlan-Kelner S, Spivak I, Moshkin O, Fridman E, Becker Y, Skaliter R, Einat P, Faerman A, Björkhem I, Feinstein E (2003) Generation of viable cholesterol-free mice. Science 302:2087 (Pubitemid 38017934)