The low density lipoprotein receptor is not necessary for maintaining mouse brain polyunsaturated fatty acid concentrations

Journal of Lipid Research

Volumn 49, Issue 1, 2008, Pages 147-152

  Chen, Chuck T ^a   Ma, David W L ^a,c   Kim, John H ^b   Mount, Howard T J ^b   Bazinet, Richard P ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY OF GUELPH   (Canada)

Author keywords

Arachidonic acid; Docosahexaenoic acid; Knockout; Transport

Indexed keywords

ETHANOLAMINE; LOW DENSITY LIPOPROTEIN RECEPTOR; MONOUNSATURATED FATTY ACID; PHOSPHATIDYLCHOLINE; PHOSPHATIDYLINOSITOL; PHOSPHATIDYLSERINE; POLYUNSATURATED FATTY ACID; SATURATED FATTY ACID;

ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN METABOLISM; BRAIN STEM; CONTROLLED STUDY; FATTY ACID METABOLISM; FATTY ACID TRANSPORT; LIPOPROTEIN METABOLISM; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEOMICS;

ANIMALS; BRAIN; BRAIN STEM; CEREBRAL CORTEX; DIETARY FATS, UNSATURATED; FATTY ACIDS, UNSATURATED; MICE; MICE, KNOCKOUT; RECEPTORS, LDL;

EID: 38049098106     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M700386-JLR200     Document Type: Article

References (74)

1. Diau, G. Y., A. T. Hsieh, E. A. Sarkadi-Nagy, V. Wijendran, P. W. Nathanielsz, and J. T. Brenna. 2005. The influence of long chain polyunsaturate supplementation on docosahexaenoic acid and arachidonic acid in baboon neonate central nervous system. BMC Med. 3: 11.
2. Akbar, M., F. Calderon, Z. Wen, and H. Y. Kim. 2005. Docosahexaenoic acid: a positive modulator of Akt signaling in neuronal survival. Proc. Natl. Acad. Sci. USA. 102: 10858-10863.
3. Bazan, N. G. 2005. Synaptic signaling by lipids in the life and death of neurons. Mol. Neurobiol. 31: 219-230.
4. Rao, J. S., R. N. Ertley, H. J. Lee, J. C. DeMar, Jr., J. T. Arnold, S. I. Rapoport, and R. P. Bazinet. 2007. n-3 polyunsaturated fatty acid deprivation in rats decreases frontal cortex BDNF via a p38 MAPK-dependent mechanism. Mol. Psychiatry. 12: 36-46.
5. Axelrod, J. 1990. Receptor-mediated activation of phospholipase A2 and arachidonic acid release in signal transduction. Biochem. Soc. Trans. 18: 503-507.
6. Innis, S. M. 2007. Dietary (n-3) fatty acids and brain development. J. Nutr. 137: 855-859.
7. Kothapalli, K. S., J. C. Anthony, B. S. Pan, A. T. Hsieh, P. W. Nathanielsz, and J. T. Brenna. 2007. Differential cerebral cortex transcriptomes of baboon neonates consuming moderate and high docosahexaenoic acid formulas. PLoS One. 2: e370.
8. Sinclair, A. J., D. Begg, M. Mathai, and R. S. Weisinger. 2007. Omega 3 fatty acids and the brain: review of studies in depression. Asia Pac. J. Clin. Nutr. 16 (Suppl. 1): 391-397.
9. Calon, F., G. P. Lim, F. Yang, T. Morihara, B. Teter, O. Ubeda, P. Rostaing, A. Triller, N. Salem, Jr., K. H. Ashe, et al. 2004. Docosahexaenoic acid protects from dendritic pathology in an Alzheimer's disease mouse model. Neuron. 43: 633-645.
10. Phillis, J. W., L. A. Horrocks, and A. A. Farooqui. 2006. Cyclo-oxygenases, lipoxygenases, and epoxygenases in CNS: their role and involvement in neurological disorders. Brain Res. Brain Res. Rev. 52: 201-243.
11. Scott, B. L., and N. G. Bazan. 1989. Membrane docosahexaenoate is supplied to the developing brain and retina by the liver. Proc. Natl. Acad. Sci. USA. 86: 2903-2907.
12. Lefkowitz, W., S. Y. Lim, Y. Lin, and N. Salem, Jr. 2005. Where does the developing brain obtain its docosahexaenoic acid? Relative contributions of dietary alpha-linolenic acid, docosahexaenoic acid, and body stores in the developing rat. Pediatr. Res. 57: 157-165.
13. Cunnane, S. C., V. Francescutti, J. T. Brenna, and M. A. Crawford. 2000. Breast-fed infants achieve a higher rate of brain and whole body docosahexaenoate accumulation than formula-fed infants not consuming dietary docosahexaenoate. Lipids. 35: 105-111.
14. Williard, D. E., S. D. Harmon, T. L. Kaduce, M. Preuss, S. A. Moore, M. E. Robbins, and A. A. Spector. 2001. Docosahexaenoic acid synthesis from n-3 polyunsaturated fatty acids in differentiated rat brain astrocytes. J. Lipid Res. 42: 1368-1376.
15. DeMar, J. C., Jr., H. J. Lee, K. Ma, L. Chang, J. M. Bell, S. I. Rapoport, and R. P. Bazinet. 2006. Brain elongation of linoleic acid is a negligible source of the arachidonate in brain phospholipids of adult rats. Biochim. Biophys. Acta. 1761: 1050-1059.
16. DeMar, J. C., Jr., K. Ma, L. Chang, J. M. Bell, and S. I. Rapoport. 2005. α-Linolenic acid does not contribute appreciably to docosahexaenoic acid within brain phospholipids of adult rats fed a diet enriched in docosahexaenoic acid. J. Neurochem. 94: 1063-1076.
17. Igarashi, M., J. C. DeMar, Jr., K. Ma, L. Chang, J. M. Bell, and S. I. Rapoport. 2007. Docosahexaenoic acid synthesis from alphalinolenic acid by rat brain is unaffected by dietary n-3 PUFA deprivation. J. Lipid Res. 48: 1150-1158.
18. Igarashi, M., J. C. DeMar, Jr., K. Ma, L. Chang, J. M. Bell, and S. I. Rapoport. 2007. Upregulated liver conversion of alpha-linolenic acid to docosahexaenoic acid in rats on a 15 week n-3 PUFA-deficient diet. J. Lipid Res. 48: 152-164.
19. Igarashi, M., K. Ma, L. Chang, J. M. Bell, and S. I. Rapoport. 2007. Dietary n-3 PUFA deprivation for 15 weeks upregulates elongase and desaturase expression in rat liver but not brain. J. Lipid Res. 48: 2463-2470.
20. No author listed. 2001. Brain uptake and utilization of fatty acids: applications to peroxisomal biogenesis disorders. Proceedings and abstracts of an international workshop, Bethesda, Maryland, USA, March 2-4, 2000. J. Mol. Neurosci. 16: 87-342.
21. Qi, K., M. Hall, and R. J. Deckelbaum. 2002. Long-chain polyunsaturated fatty acid accretion in brain. Curr. Opin. Clin. Nutr. Metab. Care. 5: 133-138.
22. Katz, R., J. A. Hamilton, A. A. Spector, S. A. Moore, H. W. Moser, M. J. Noetzel, and P. A. Watkins. 2001. Brain uptake and utilization of fatty acids: recommendations for future research. J. Mol. Neurosci. 16: 333-335.
23. Hamilton, J. A., and K. Brunaldi. 2007. A model for fatty acid transport into the brain. J. Mol. Neurosci. 33: 12-17.
24. Rapoport, S. I., M. C. Chang, and A. A. Spector. 2001. Delivery and turnover of plasma-derived essential PUFAs in mammalian brain. J. Lipid Res. 42: 678-685.
25. Hamilton, J. A., R. A. Johnson, B. Corkey, and F. Kamp. 2001. Fatty acid transport: the diffusion mechanism in model and biological membranes. J. Mol. Neurosci. 16: 99-108 (discussion 151-157).
26. Spector, A. A. 2001. Plasma free fatty acid and lipoproteins as sources of polyunsaturated fatty acid for the brain. J. Mol. Neurosci. 16: 159-165 (discussion 215-221).
27. Edmond, J. 2001. Essential polyunsaturated fatty acids and the barrier to the brain: the components of a model for transport. J. Mol. Neurosci. 16: 181-193 (discussion 215-221).
28. Kamp, F., and J. A. Hamilton. 1992. pH gradients across phospholipid membranes caused by fast flip-flop of un-ionized fatty acids. Proc. Natl. Acad. Sci. USA. 89: 11367-11370.
29. Kamp, F., D. Zakim, F. Zhang, N. Noy, and J. A. Hamilton. 1995. Fatty acid flip-flop in phospholipid bilayers is extremely fast. Biochemistry. 34: 11928-11937.
30. Robinson, P. J., J. Noronha, J. J. DeGeorge, L. M. Freed, T. Nariai, and S. I. Rapoport. 1992. A quantitative method for measuring regional in vivo fatty-acid incorporation into and turnover within brain phospholipids: review and critical analysis. Brain Res. 17: 187-214.
31. Innis, S. M., H. Sprecher, D. Hachey, J. Edmond, and R. E. Anderson. 1999. Neonatal polyunsaturated fatty acid metabolism. Lipids. 34: 139-149.
32. Edmond, J., T. A. Higa, R. A. Korsak, E. A. Bergner, and W. N. Lee. 1998. Fatty acid transport and utilization for the developing brain. J. Neurochem. 70: 1227-1234.
33. Marbois, B. N., H. O. Ajie, R. A. Korsak, D. K. Sensharma, and J. Edmond. 1992. The origin of palmitic acid in brain of the developing rat. Lipids. 27: 587-592.
34. Polozova, A., E. Gionfriddo, and N. Salem, Jr. 2006. Effect of docosahexaenoic acid on tissue targeting and metabolism of plasma lipoproteins. Prostaglandins Leukot. Essent. Fatty Acids. 75: 183-190.
35. Hofmann, S. L., D. W. Russell, J. L. Goldstein, and M. S. Brown. 1987. mRNA for low density lipoprotein receptor in brain and spinal cord of immature and mature rabbits. Proc. Natl. Acad. Sci. USA. 84: 6312-6316.
36. Meresse, S., C. Delbart, J. C. Fruchart, and R. Cecchelli. 1989. Low-density lipoprotein receptor on endothelium of brain capillaries. J. Neurochem. 53: 340-345.
37. Hanaka, S., T. Abe, H. Itakura, and A. Matsumoto. 2000. Gene expression related to cholesterol metabolism in mouse brain during development. Brain Dev. 22: 321-326.
38. Osono, Y., L. A. Woollett, J. Herz, and J. M. Dietschy. 1995. Role of the low density lipoprotein receptor in the flux of cholesterol through the plasma and across the tissues of the mouse. J. Clin. Invest. 95: 1124-1132.
39. Ishibashi, S., M. S. Brown, J. L. Goldstein, R. D. Gerard, R. E. Hammer, and J. Herz. 1993. Hypercholesterolemia in low density lipoprotein receptor knockout mice and its reversal by adenovirus-mediated gene delivery. J. Clin. Invest. 92: 883-893.
40. Lein, E. S., M. J. Hawrylycz, N. Ao, M. Ayres, A. Bensinger, A. Bernard, A. F. Boe, M. S. Boguski, K. S. Brockway, E. J. Byrnes, et al. 2007. Genome-wide atlas of gene expression in the adult mouse brain. Nature. 445: 168-176.
41. Olfert, E. D., B. M. Cross, and A. A. McWilliam, editors. 1993. Guide to the Care and Use of Experimental Animals. Canadian Council on Animal Care, Ottawa.
42. Rapoport, S. I. 1976. Blood-Brain Barrier in Physiology and Medicine. Raven Press, New York.
43. Dobbing, J., and J. Sands. 1979. Comparative aspects of the brain growth spurt. Early Hum. Dev. 3: 79-83.
44. Ward, G., J. Woods, M. Reyzer, and N. Salem, Jr. 1996. Artificial rearing of infant rats on milk formula deficient in n-3 essential fatty acids: a rapid method for the production of experimental n-3 deficiency. Lipids. 31: 71-77.
45. Ma, K., R. Langenbach, S. I. Rapoport, and M. Basselin. 2007. Altered brain lipid composition in cyclooxygenase-2 knockout mouse. J. Lipid Res. 48: 848-854.
46. Lee, H. J., J. S. Rao, L. Chang, S. I. Rapoport, and R. P. Bazinet. 2007. Chronic lamotrigine does not alter the turnover of arachidonic acid within brain phospholipids of the unanesthetized rat: implications for the treatment of bipolar disorder. Psychopharmacology (Berl.). 193: 467-474.
47. Lee, H. J., J. S. Rao, S. I. Rapoport, and R. P. Bazinet. 2007. Antimanic therapies target brain arachidonic acid signaling: lessons learned about the regulation of brain fatty acid metabolism. Prostaglandins Leukot. Essent. Fatty Acids. In press.
48. Bazinet, R. P., H. J. Lee, C. C. Felder, A. C. Porter, S. I. Rapoport, and T. A. Rosenberger. 2005. Rapid high-energy microwave fixation is required to determine the anandamide (N-arachidonoylethanolamine) concentration of rat brain. Neurochem. Res. 30: 597-601.
49. Deutsch, J., S. I. Rapoport, and A. D. Purdon. 1997. Relation between free fatty acid and acyl-CoA concentrations in rat brain following decapitation. Neurochem. Res. 22: 759-765.
50. Folch, J., M. Lees, and G. H. Sloane Stanley. 1957. A simple method for the isolation and purification of total lipides from animal tissues. J. Biol. Chem. 226: 497-509.
51. Bazinet, R. P., J. S. Rao, L. Chang, S. I. Rapoport, and H. J. Lee. 2006. Chronic carbamazepine decreases the incorporation rate and turnover of arachidonic acid but not docosahexaenoic acid in brain phospholipids of the unanesthetized rat: relevance to bipolar disorder. Biol. Psychiatry. 59: 401-407.
52. Levant, B., M. K. Ozias, and S. E. Carlson. 2007. Specific brain regions of female rats are differentially depleted of docosahexaenoic acid by reproductive activity and an (n-3) fatty acid-deficient diet. J. Nutr. 137: 130-134.
53. Shetty, H. U., Q. R. Smith, K. Washizaki, S. I. Rapoport, and A. D. Purdon. 1996. Identification of two molecular species of rat brain phosphatidylcholine that rapidly incorporate and turn over arachidonic acid in vivo. J. Neurochem. 67: 1702-1710.
54. Bazinet, R. P., J. S. Rao, L. Chang, S. I. Rapoport, and H. J. Lee. 2005. Chronic valproate does not alter the kinetics of docosahexaenoic acid within brain phospholipids of the unanesthetized rat. Psychopharmacology (Berl.). 182: 180-185.
55. Lee, H. J., S. Ghelardoni, L. Chang, F. Bosetti, S. I. Rapoport, and R. P. Bazinet. 2005. Topiramate does not alter the kinetics of arachidonic or docosahexaenoic acid in brain phospholipids of the unanesthetized rat. Neurochem. Res. 30: 677-683.
56. Kim, H. Y., J. Bigelow, and J. H. Kevala. 2004. Substrate preference in phosphatidylserine biosynthesis for docosahexaenoic acid containing species. Biochemistry. 43: 1030-1036.
57. Chilton, F. H., and R. C. Murphy. 1986. Remodeling of arachidonate-containing phosphoglycerides within the human neutrophil. J. Biol. Chem. 261: 7771-7777.
58. Bazinet, R. P., A. K. Bhattacharjee, and H. J. Lee. 2007. Haloperidol targets brain arachidonic acid signaling. Prog. Neuropsychopharmacol. Biol. Psychiatry. 31: 314-315 (author reply 316).
59. Kozarsky, K. F., M. H. Donahee, A. Rigotti, S. N. Iqbal, E. R. Edelman, and M. Krieger. 1997. Overexpression of the HDL receptor SR-BI alters plasma HDL and bile cholesterol levels. Nature. 387: 414-417.
60. Beisiegel, U., W. Weber, G. Ihrke, J. Herz, and K. K. Stanley. 1989. The LDL-receptor-related protein, LRP, is an apolipoprotein E-binding protein. Nature. 341: 162-164.
61. Wyne, K. L., K. Pathak, M. C. Seabra, and H. H. Hobbs. 1996. Expression of the VLDL receptor in endothelial cells. Arterioscler. Thromb. Vasc. Biol. 16: 407-415.
62. Jaye, M., K. J. Lynch, J. Krawiec, D. Marchadier, C. Maugeais, K. Doan, V. South, D. Amin, M. Perrone, and D. J. Rader. 1999. A novel endothelial-derived lipase that modulates HDL metabolism. Nat. Genet. 21: 424-428.
63. Sovic, A., U. Panzenboeck, A. Wintersperger, I. Kratzer, A. Hammer, S. Levak-Frank, S. Frank, D. J. Rader, E. Malle, and W. Sattler. 2005. Regulated expression of endothelial lipase by porcine brain capillary endothelial cells constituting the blood-brain barrier. J. Neurochem. 94: 109-119.
64. Chen, S., and P. V. Subbaiah. 2007. Phospholipid and fatty acid specificity of endothelial lipase: potential role of the enzyme in the delivery of docosahexaenoic acid (DHA) to tissues. Biochim. Biophys. Acta. 1771: 1319-1328.
65. Hamilton, J. A., W. Guo, and F. Kamp. 2002. Mechanism of cellular uptake of long-chain fatty acids: do we need cellular proteins? Mol. Cell. Biochem. 239: 17-23.
66. Lee, H. J., J. S. Rao, L. Chang, S. I. Rapoport, and R. P. Bazinet. 2007. Chronic lamotrigine does not alter the turnover of arachidonic acid within brain phospholipids of the unanesthetized rat: implications for the treatment of bipolar disorder. Psychopharmacology (Berl). 193: 467-474.
67. Lee, H. J., J. S. Rao, R. N. Ertley, L. Chang, S. I. Rapoport, and R. P. Bazinet. 2007. Chronic fluoxetine increases cytosolic phospholipase A(2) activity and arachidonic acid turnover in brain phospholipids of the unanesthetized rat. Psychopharmacology (Berl.). 190: 103-115.
68. Golovko, M. Y., and E. J. Murphy. 2006. Uptake and metabolism of plasma-derived erucic acid by rat brain. J. Lipid Res. 47: 1289-1297.
69. DeMar, J. C., Jr., K. Ma, J. M. Bell, and S. I. Rapoport. 2004. Halflives of docosahexaenoic acid in rat brain phospholipids are prolonged by 15 weeks of nutritional deprivation of n-3 polyunsaturated fatty acids. J. Neurochem. 91: 1125-1137.
70. Purdon, D., T. Arai, and S. Rapoport. 1997. No evidence for direct incorporation of esterified palmitic acid from plasma into brain lipids of awake adult rat. J. Lipid Res. 38: 526-530.
71. Brown, M. S., and J. L. Goldstein. 1986. A receptor-mediated pathway for cholesterol homeostasis. Science. 232: 34-47.
72. Tolleshaug, H., J. L. Goldstein, W. J. Schneider, and M. S. Brown. 1982. Posttranslational processing of the LDL receptor and its genetic disruption in familial hypercholesterolemia. Cell. 30: 715-724.
73. Turley, S. D., D. K. Burns, C. R. Rosenfeld, and J. M. Dietschy. 1996. Brain does not utilize low density lipoprotein-cholesterol during fetal and neonatal development in the sheep. J. Lipid Res. 37: 1953-1961.
74. Spady, D. K., M. Huettinger, D. W. Bilheimer, and J. M. Dietschy. 1987. Role of receptor-independent low density lipoprotein transport in the maintenance of tissue cholesterol balance in the normal and WHHL rabbit. J. Lipid Res. 28: 32-41.