Brain region-specific immunolocalization of the lipolysis-stimulated lipoprotein receptor (LSR) and altered cholesterol distribution in aged LSR +/- mice

Journal of Neurochemistry

Volumn 123, Issue 4, 2012, Pages 467-476

  Stenger, Christophe ^a   Pinçon, Anthony ^a   Hanse, Marine ^a   Royer, Laurent ^a   Comte, Audrey ^a   Koziel, Violette ^a   Olivier, Jean Luc ^a   Pillot, Thierry ^a   Yen, Frances T ^a  

^a UNIVERSITÉ DE LORRAINE   (France)

Author keywords

aging; brain; cholesterol; lipoprotein receptor

Indexed keywords

CHOLESTEROL; LIPOLYSIS STIMULATED LIPOPROTEIN RECEPTOR; LIPOPROTEIN RECEPTOR; UNCLASSIFIED DRUG;

AGED; AGING; ANATOMICAL VARIATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN FUNCTION; BRAIN REGION; CEREBROSPINAL FLUID; CHOLESTEROL METABOLISM; CHOROID PLEXUS; COGNITION; CONTROLLED STUDY; ENZYME ACTIVITY; EPENDYMA CELL; HETEROZYGOTE; HIPPOCAMPUS; IMMUNOLOCALIZATION; LIPID STORAGE; MALE; MOUSE; NERVE CELL; NONHUMAN; PARENCHYMA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PURKINJE CELL;

AGE FACTORS; AGING; ANIMALS; BRAIN; CHOLESTEROL; CHOROID PLEXUS; FILIPIN; GENE EXPRESSION REGULATION; GLIAL FIBRILLARY ACIDIC PROTEIN; MALE; MAZE LEARNING; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEURONS; PHOSPHOPYRUVATE HYDRATASE; RECEPTORS, LDL;

ANIMALIA; MUS;

EID: 84867578924     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2012.07922.x     Document Type: Article

References (51)

1. Bihain B. E., and, Yen F. T., (1992) Free fatty acids activate a high-affinity saturable pathway for degradation of low-density lipoproteins in fibroblasts from a subject homozygous for familial hypercholesterolemia. Biochemistry 31, 4628-4636.
2. Boyles J. K., Pitas R. E., Wilson E., Mahley R. W., and, Taylor J. M., (1985) Apolipoprotein E associated with astrocytic glia of the central nervous system and with nonmyelinating glia of the peripheral nervous system. J. Clin. Invest. 76, 1501-1513.
3. Burguiere E., Arabo A., Jarlier F., De Zeeuw C. I., and, Rondi-Reig L., (2010) Role of the cerebellar cortex in conditioned goal-directed behavior. J. Neurosci. 30, 13265-13271.
4. Burns M. P., Igbavboa U., Wang L., Wood W. G., and, Duff K., (2006) Cholesterol distribution, not total levels, correlate with altered amyloid precursor protein processing in statin-treated mice. Neuromolecular Med. 8, 319-328.
5. Calon F., (2011) Omega-3 polyunsaturated fatty acids in Alzheimer's disease: key questions and partial answers. Curr. Alzheimer Res. 8, 470-478.
6. Camargo N., Brouwers J. F., Loos M., Gutmann D. H., Smit A. B., and, Verheijen M. H., (2012) High-fat diet ameliorates neurological deficits caused by defective astrocyte lipid metabolism. FASEB J. Epub ahead of print, doi: 10.1096/fj.12-205807.
7. Cederholm T., and, Palmblad J., (2010) Are omega-3 fatty acids options for prevention and treatment of cognitive decline and dementia? Curr. Opin. Clin. Nutr. Metab. Care 13, 150-155.
8. Chen C. T., Ma D. W., Kim J. H., Mount H. T., and, Bazinet R. P., (2008) The low density lipoprotein receptor is not necessary for maintaining mouse brain polyunsaturated fatty acid concentrations. J. Lipid Res. 49, 147-152.
9. Daneman R., Zhou L., Agalliu D., Cahoy J. D., Kaushal A., and, Barres B. A., (2010) The mouse blood-brain barrier transcriptome: a new resource for understanding the development and function of brain endothelial cells. PLoS ONE 5, e13741.
10. Demeester N., Castro G., Desrumaux C., et al,. (2000) Characterization and functional studies of lipoproteins, lipid transfer proteins, and lecithin:cholesterol acyltransferase in CSF of normal individuals and patients with Alzheimer's disease. J. Lipid Res. 41, 963-974.
11. Dietrich M. O., Spuch C., Antequera D., Rodal I., de Yebenes J. G., Molina J. A., Bermejo F., and, Carro E., (2008) Megalin mediates the transport of leptin across the blood-CSF barrier. Neurobiol. Aging 29, 902-912.
12. Di Paolo G., and, Kim T. W., (2011) Linking lipids to Alzheimer's disease: cholesterol and beyond. Nat. Rev. Neurosci. 12, 284-296.
13. Elder G. A., Ragnauth A., Dorr N., Franciosi S., Schmeidler J., Haroutunian V., and, Buxbaum J. D., (2008) Increased locomotor activity in mice lacking the low-density lipoprotein receptor. Behav. Brain Res. 191, 256-265.
14. Fryer J. D., Demattos R. B., McCormick L. M., et al,. (2005) The low density lipoprotein receptor regulates the level of central nervous system human and murine apolipoprotein E but does not modify amyloid plaque pathology in PDAPP mice. J. Biol. Chem. 280, 25754-25759.
15. Fujiyoshi M., Tachikawa M., Ohtsuki S., et al,. (2011) Amyloid-beta peptide(1-40) elimination from cerebrospinal fluid involves low-density lipoprotein receptor-related protein 1 at the blood-cerebrospinal fluid barrier. J. Neurochem. 118, 407-415.
16. Gamba P., Testa G., Sottero B., Gargiulo S., Poli G., and, Leonarduzzi G., (2012) The link between altered cholesterol metabolism and Alzheimer's disease. Ann. N. Y. Acad. Sci. 1259, 54-64.
17. Garcia P., Youssef I., Utvik J. K., et al,. (2010) Ciliary neurotrophic factor cell-based delivery prevents synaptic impairment and improves memory in mouse models of Alzheimer's disease. J. Neurosci. 30, 7516-7527.
18. Goldberg I. J., Soprano D. R., Wyatt M. L., Vanni T. M., Kirchgessner T. G., and, Schotz M. C., (1989) Localization of lipoprotein lipase mRNA in selected rat tissues. J. Lipid Res. 30, 1569-1577.
19. Greenspan P., Mayer E. P., and, Fowler S. D., (1985) Nile red: a selective fluorescent stain for intracellular lipid droplets. J. Cell Biol. 100, 965-973.
20. Herz J., (2003) LRP: a bright beacon at the blood-brain barrier. J. Clin. Invest. 112, 1483-1485.
21. Herz J., and, Chen Y., (2006) Reelin, lipoprotein receptors and synaptic plasticity. Nat. Rev. Neurosci. 7, 850-859.
22. Herz J., Clouthier D. E., and, Hammer R. E., (1992) LDL receptor-related protein internalizes and degrades uPA-PAI-1 complexes and is essential for embryo implantation. Cell 71, 411-421.
23. Huang T. L., (2010) Omega-3 fatty acids, cognitive decline, and Alzheimer's disease: a critical review and evaluation of the literature. J. Alzheimers Dis. 21, 673-690.
24. Kim J., Basak J. M., and, Holtzman D. M., (2009a) The role of apolipoprotein E in Alzheimer's disease. Neuron 63, 287-303.
25. Kim J., Castellano J. M., Jiang H., Basak J. M., Parsadanian M., Pham V., Mason S. M., Paul S. M., and, Holtzman D. M., (2009b) Overexpression of low-density lipoprotein receptor in the brain markedly inhibits amyloid deposition and increases extracellular A beta clearance. Neuron 64, 632-644.
26. Krisanova N., Sivko R., Kasatkina L., and, Borisova T., (2012) Neuroprotection by lowering cholesterol: a decrease in membrane cholesterol content reduces transporter-mediated glutamate release from brain nerve terminals. Biochim. Biophys. Acta 1822, 1553-1561.
27. Ladu M. J., Reardon C., Van Eldik L., Fagan A. M., Bu G., Holtzman D., and, Getz G. S., (2000) Lipoproteins in the central nervous system. Ann. N. Y. Acad. Sci. 903, 167-175.
28. Liu Q., Trotter J., Zhang J., Peters M. M., Cheng H., Bao J., Han X., Weeber E. J., and, Bu G., (2010) Neuronal LRP1 knockout in adult mice leads to impaired brain lipid metabolism and progressive, age-dependent synapse loss and neurodegeneration. J. Neurosci. 30, 17068-17078.
29. Masuda S., Oda Y., Sasaki H., Ikenouchi J., Higashi T., Akashi M., Nishi E., and, Furuse M., (2011) LSR defines cell corners for tricellular tight junction formation in epithelial cells. J. Cell Sci. 124, 548-555.
30. Matsuo M., Campenot R. B., Vance D. E., Ueda K., and, Vance J. E., (2011) Involvement of low-density lipoprotein receptor-related protein and ABCG1 in stimulation of axonal extension by apoE-containing lipoproteins. Biochim. Biophys. Acta 1811, 31-38.
31. Mesli S., Javorschi S., Berard A. M., Landry M., Priddle H., Kivlichan D., Smith A. J., Yen F. T., Bihain B. E., and, Darmon M., (2004) Distribution of the lipolysis stimulated receptor in adult and embryonic murine tissues and lethality of LSR-/- embryos at 12.5 to 14.5 days of gestation. Eur. J. Biochem. 271, 3103-3114.
32. Mulder M., Lombardi P., Jansen H., van Berkel T. J., Frants R. R., and, Havekes L. M., (1993) Low density lipoprotein receptor internalizes low density and very low density lipoproteins that are bound to heparan sulfate proteoglycans via lipoprotein lipase. J. Biol. Chem. 268, 9369-9375.
33. Narvekar P., Berriel Diaz M., Krones-Herzig A., Hardeland U., Strzoda D., Stohr S., Frohme M., and, Herzig S., (2009) Liver-specific loss of lipolysis-stimulated lipoprotein receptor triggers systemic hyperlipidemia in mice. Diabetes 58, 1040-1049.
34. Pfrieger F. W., and, Ungerer N., (2011) Cholesterol metabolism in neurons and astrocytes. Prog. Lipid Res. 50, 357-371.
35. Pitas R. E., Boyles J. K., Lee S. H., Hui D., and, Weisgraber K. H., (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.
36. Qiu S., Korwek K. M., and, Weeber E. J., (2006) A fresh look at an ancient receptor family: emerging roles for low density lipoprotein receptors in synaptic plasticity and memory formation. Neurobiol. Learn. Mem. 85, 16-29.
37. Rapp A., Gmeiner B., and, Huttinger M., (2006) Implication of apoE isoforms in cholesterol metabolism by primary rat hippocampal neurons and astrocytes. Biochimie 88, 473-483.
38. Rochefort C., Arabo A., Andre M., Poucet B., Save E., and, Rondi-Reig L., (2011) Cerebellum shapes hippocampal spatial code. Science 334, 385-389.
39. Schreurs B. G., (2010) The effects of cholesterol on learning and memory. Neurosci. Biobehav. Rev. 34, 1366-1379.
40. Shepardson N. E., Shankar G. M., and, Selkoe D. J., (2011a) Cholesterol level and statin use in Alzheimer disease: II. Review of human trials and recommendations. Arch. Neurol. 68, 1385-1392.
41. Shepardson N. E., Shankar G. M., and, Selkoe D. J., (2011b) Cholesterol level and statin use in Alzheimer disease: I. Review of epidemiological and preclinical studies. Arch. Neurol. 68, 1239-1244.
42. Stenger C., Hanse M., Pratte D., et al,. (2010) Up-regulation of hepatic lipolysis stimulated lipoprotein receptor by leptin: a potential lever for controlling lipid clearance during the postprandial phase. FASEB J. 24, 4218-4228.
43. Taha A. Y., Chen C. T., Liu Z., Kim J. H., Mount H. T., and, Bazinet R. P., (2009) Brainstem concentrations of cholesterol are not influenced by genetic ablation of the low-density lipoprotein receptor. Neurochem. Res. 34, 311-315.
44. Tartaglia L. A., Dembski M., Weng X., et al,. (1995) Identification and expression cloning of a leptin receptor, OB-R. Cell 83, 1263-1271.
45. Tooyama I., Kawamata T., Akiyama H., Kimura H., Moestrup S. K., Gliemann J., Matsuo A., and, McGeer P. L., (1995) Subcellular localization of the low density lipoprotein receptor-related protein (alpha 2-macroglobulin receptor) in human brain. Brain Res. 691, 235-238.
46. Uranga R. M., and, Keller J. N., (2010) Diet and age interactions with regards to cholesterol regulation and brain pathogenesis. Curr. Gerontol. Geriatr. Res. 2010, 219683.
47. Vance J. E., and, Hayashi H., (2010) Formation and function of apolipoprotein E-containing lipoproteins in the nervous system. Biochim. Biophys. Acta 1801, 806-818.
48. Xian X., Liu T., Yu J., et al,. (2009) Presynaptic defects underlying impaired learning and memory function in lipoprotein lipase-deficient mice. J. Neurosci. 29, 4681-4685.
49. Yen F. T., Mann C. J., Guermani L. M., Hannouche N. F., Hubert N., Hornick C. A., Bordeau V. N., Agnani G., and, Bihain B. E., (1994) Identification of a lipolysis-stimulated receptor that is distinct from the LDL receptor and the LDL receptor-related protein. Biochemistry 33, 1172-1180.
50. Yen F. T., Masson M., Clossais-Besnard N., Andre P., Grosset J. M., Bougueleret L., Dumas J. B., Guerassimenko O., and, Bihain B. E., (1999) Molecular cloning of a lipolysis-stimulated remnant receptor expressed in the liver. J. Biol. Chem. 274, 13390-13398.
51. Yen F. T., Roitel O., Bonnard L., Notet V., Pratte D., Stenger C., Magueur E., and, Bihain B. E., (2008) Lipolysis stimulated lipoprotein receptor: A novel molecular link between hyperlipidemia, weight gain, and atherosclerosis in mice. J. Biol. Chem. 283, 25650-25659.