The multiple roles of fatty acid handling proteins in brain

Frontiers in Physiology

Volumn 3 SEP, Issue , 2012, Pages

  Moullé, Valentine S F ^a   Cansell, Céline ^a   Luquet, Serge ^a   Cruciani Guglielmacci, Céline ^a  

^a UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

Brain; CD36; Cognition; FABP; FATP; Fatty acids; GPR40; Neuronal differentiation

Indexed keywords

EID: 84867120169     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2012.00385     Document Type: Short Survey

References (62)

1. Abumrad, N. A., Ajmal, M., Pothakos, K., and Robinson, J. K. (2005). CD36 expression and brain function: does CD36 deficiency impact learning ability? Prostaglandins Other Lipid Mediat. 77, 77-83.
2. Abumrad, N. A., El-Maghrabi, M. R., Amri, E. Z., Lopez, E., and Grimaldi, P. A. (1993). Cloning of a rat adipocyte membrane protein implicated in binding or transport of long-chain fatty acids that is induced during preadipocyte differentiation. Homology with human CD36. J. Biol. Chem. 268, 17665-17668.
3. Anthony, T. E., Mason, H. A., Gridley T.,Fishell,G.,andHeintz,N. (2005). Brain lipid-binding protein is a direct target of Notch signaling in radial glial cells. Genes Dev. 19, 1028-1033.
4. Baillie, A. G., Coburn, C. T., and Abumrad, N. A. (1996). Reversible binding of long-chain fatty acids to purified FAT, the adipose CD36 homolog. J. Membr. Biol. 153, 75-81.
5. Baruch, D. I., Ma, X. C., Pasloske B.,Howard,R.J.,andMiller, L. H. (1999). CD36 peptides that block cytoadherence define the CD36 binding region for Plasmodium falciparuminfected erythrocytes. Blood 94, 2121-2127.
6. Bazinet, R. P., Weis, M. T., Rapoport, S. I., and Rosenberger, T. A. (2006). Valproic acid selectively inhibits conversion of arachidonic acid to arachidonoyl-CoA by brain microsomal long-chain fatty acyl-CoA synthetases: relevance to bipolar disorder. Psychopharmacology (Berl.) 184, 122-129.
7. Benarroch, E. E. (2011). Circumventricular organs: receptive and homeostatic functions and clinical implications. Neurology 77, 1198-1204.
8. Boneva, N. B., Kaplamadzhiev, D. B., Sahara, S., Kikuchi, H., Pyko, I. V., Kikuchi, M., Tonchev, A. B., and Yamashima, T. (2011). Expression of fatty acid-binding proteins in adult hippocampal neurogenic niche of postischemic monkeys. Hippocampus 21, 162-171.
9. Bourre, J. M. (2004). Roles of unsaturated fatty acids (especially omega-3 fatty acids) in the brain at various ages and during ageing. J. Nutr. Health Aging 8, 163-174.
10. Briscoe, C. P., Tadayyon, M., Andrews, J. L., Benson, W. G., Chambers, J. K., Eilert, M. M., Ellis, C., Elshourbagy, N. A., Goetz, A. S., Minnick, D. T.,Murdock,P.R.,Sauls,H.R.Jr., Shabon, U., Spinage, L. D., Strum, J. C., Szekeres, P. G., Tan, K. B., Way,J.M.,Ignar,D.M.,Wilson,S., and Muir, A. I. (2003). The orphan G protein-coupled receptor GPR40 is activated by medium and long chain fatty acids. J. Biol. Chem. 278, 11303-11311.
11. Cho, Y. Y. (2012). A novel role of braintype ACS4 isotype in neuronal differentiation. Biochem. Biophys. Res. Commun. 419, 505-510.
12. Cruciani-Guglielmacci, C., Hervalet, A., Douared, L., Sanders, N. M., Levin, B. E., Ktorza, A., and Magnan, C. (2004). Beta oxidation in the brain is required for the effects of non-esterified fatty acids on glucose-induced insulin secretion in rats. Diabetologia 47, 2032-2038.
13. Dawson, D. W., Pearce, S. F., Zhong, R., Silverstein, R. L., Frazier, W. A., and Bouck, N. P. (1997). CD36 mediates the in vitro inhibitory effects of thrombospondin-1 on endothelial cells. J. Cell Biol. 138, 707-717.
14. 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.
15. Elmquist,J.K.,andMarcus,J.N. (2003). Rethinking the central causes of diabetes. Nat. Med. 9, 645-647.
16. El-Yassimi, A., Hichami, A., Besnard, P., and Khan, N. A. (2008). Linoleic acid induces calcium signaling, Src kinase phosphorylation, and neurotransmitter release in mouse CD36-positive gustatory cells. J. Biol. Chem. 283, 12949-12959.
17. Farr, S. A., Yamada, K. A., Butterfield, D. A., Abdul, H. M., Xu, L., Miller, N. E., Banks, W. A., and Morley, J. E. (2008). Obesity and hypertriglyceridemia produce cognitive impairment. Endocrinology 149, 2628-2636.
18. Feng, L., Hatten, M. E., and Heintz, N. (1994). Brain lipid-binding protein (BLBP): a novel signaling system in the developing mammalian CNS. Neuron 12, 895-908.
19. Feng, L., and Heintz, N. (1995). Differentiating neurons activate transcription of the brain lipidbinding protein gene in radial glia through a novel regulatory element. Development 121, 1719-1730.
20. Gaillard, D., Laugerette, F., Darcel, N., El-Yassimi, A., Passilly-Degrace P.,Hichami,A.,Khan,N.A., Montmayeur,J.P.,andBesnard,P. (2008). The gustatory pathway is involved in CD36-mediated orosensory perception of long-chain fatty acids in the mouse. FASEB J. 22, 1458-1468.
21. Hamilton, J. A., and Brunaldi, K. (2007). A model for fatty acid transport into the brain. J. Mol. Neurosci. 33, 12-17.
22. Hawkins, B. T., and Davis, T. P. (2005). The blood-brain barrier/neurovascular unit in health and disease. Pharmacol. Rev. 57, 173-185.
23. Itoh, Y., Kawamata, Y., Harada, M., Kobayashi, M., Fujii, R., Fukusumi, S., Ogi, K., Hosoya, M., Tanaka, Y., Uejima, H., Tanaka, H., Maruyama, M., Satoh, R., Okubo, S., Kizawa, H., Komatsu, H., Matsumura, F., Noguchi Y.,Shinohara,T.,Hinuma,S., Fujisawa, Y., and Fujino, M. (2003). Free fatty acids regulate insulin secretion from pancreatic beta cells through GPR40. Nature 422, 173-176.
24. Iwayama, Y., Hattori, E., Maekawa, M., Yamada, K., Toyota, T., Ohnishi, T., Iwata, Y., Tsuchiya, K. J., Sugihara, G., Kikuchi, M., Hashimoto, K., Iyo, M., Inada, T., Kunugi, H., Ozaki, N., Iwata, N., Nanko, S., Iwamoto K.,Okazaki,Y.,Kato,T.,and Yoshikawa, T. (2010). Association analyses between brain-expressed fatty-acid binding protein (FABP) genes and schizophrenia and bipolar disorder. Am. J. Med. Genet. B Neuropsychiatr. Genet. 153B, 484-493.
25. Kan, I., Melamed, E., Offen, D., and Green, P. (2007). Docosahexaenoic acid and arachidonic acid are fundamental supplements for the induction of neuronal differentiation. J. Lipid Res. 48, 513-517.
26. Kang, M. J., Fujino, T., Sasano, H., Minekura, H., Yabuki, N., Nagura, H., Iijima, H., and Yamamoto, T. T. (1997). A novel arachidonatepreferring acyl-CoA synthetase is present in steroidogenic cells of the rat adrenal, ovary, and testis. Proc. Natl. Acad. Sci. U.S.A. 94, 2880-2884.
27. Kasser, T. R., Deutch, A., and Martin, R. J. (1986). Uptake and utilization of metabolites in specific brain sites relative to feeding status. Physiol. Behav. 36, 1161-1165.
28. Kee, H. J., Koh, J. T., Yang, S. Y., Lee, Z. H., Baik, Y. H., and Kim, K. K. (2003). A novel murine long-chain acyl-CoA synthetase expressed in brain participates in neuronalcellproliferation.Biochem. Biophys. Res. Commun. 305, 925-933.
29. Kotarsky, K., Nilsson, N. E., Olde, B., and Owman, C. (2003). Progress in methodology. Improved reporter gene assays used to identify ligands acting on orphan seven-transmembrane receptors. Pharmacol. Toxicol. 93, 249-258.
30. Le Foll, C., Irani, B. G., Magnan, C., Dunn-Meynell, A. A., and Levin, B. E. (2009). Characteristics and mechanisms of hypothalamic neuronal fatty acid sensing. Am. J. Physiol. Regul. Integr. Comp. Physiol. 297, R655-R664.
31. Liu, J. W., Almaguel, F. G., Bu, L. DeLeon,D.D.,andDeLeon, M. (2008). Expression of E-FABP in PC12 cells increases neurite extension during differentiation: involvement of n-3 and n-6 fatty acids. J. Neurochem. 106, 2015-2029.
32. Liu, R. Z., Mita, R., Beaulieu, M., Gao, Z., and Godbout, R. (2010). Fatty acid binding proteins in brain development and disease. Int. J. Dev. Biol. 54, 1229-1239.
33. Ma,D.,Lu,L.,Boneva,N.B., Warashina, S., Kaplamadzhiev, D. B., Mori, Y., Nakaya, M. A., Kikuchi, M.,Tonchev,A.B.,Okano,H.,and Yamashima, T. (2008). Expression of free fatty acid receptor GPR40 in the neurogenic niche of adult monkey hippocampus. Hippocampus 18, 326-333.
34. Ma,D.,Tao,B.,Warashina,S.,Kotani, S., Lu, L., Kaplamadzhiev, D. B., Mori, Y., Tonchev, A. B., and Yamashima, T. (2007). Expression of free fatty acid receptor GPR40 in the central nervous system of adult monkeys. Neurosci. Res. 58, 394-401.
35. Migrenne, S., Le Foll, C., Levin, B. E., and Magnan, C. (2011). Brain lipid sensing and nervous control of energy balance. Diabetes Metab. 37, 83-88.
36. Mitchell, R. W., and Hatch, G. M. (2011). Fatty acid transport into the brain: of fatty acid fables and lipid tails. Prostaglandins Leukot. Essent. Fatty Acids 85, 293-302.
37. Mitchell, R. W., On, N. H., Del Bigio, M.R.,Miller,D.W.,andHatch,G. M. (2011). Fatty acid transport protein expression in human brain and potential role in fatty acid transport across human brain microvessel endothelial cells. J. Neurochem. 117, 735-746.
38. Murphy, E. J., Owada, Y., Kitanaka, N., Kondo, H., and Glatz, J. F. (2005). Brain arachidonic acid incorporation is decreased in heart fatty acid binding protein gene-ablated mice. Biochemistry 44, 6350-6360.
39. Nakamoto, K., Nishinaka, T., Matsumoto, K., Kasuya, F., Mankura, M., Koyama, Y., and Tokuyama, S. (2012). Involvement of the long-chain fatty acid receptor GPR40 as a novel pain regulatory system. Brain Res. 1432, 74-83.
40. Neuringer, M., Anderson, G. J., and Connor, W. E. (1988). The essentiality of n-3 fatty acids for the development and function of the retina and brain. Annu. Rev. Nutr. 8, 517-541.
41. Obici, S., Feng, Z., Arduini, A., Conti, R., and Rossetti, L. (2003). Inhibition of hypothalamic carnitine palmitoyltransferase-1 decreases food intake and glucose production. Nat. Med. 9, 756-761.
42. Owada, Y. (2008). Fatty acid binding protein: localization and functional significance in the brain. Tohoku J. Exp. Med. 214, 213-220.
43. Owada, Y., Abdelwahab, S. A., Kitanaka, N., Sakagami, H., Takano, H., Sugitani, Y., Sugawara M.,Kawashima,H.,Kiso,Y., Mobarakeh, J. I., Yanai, K., Kaneko, K., Sasaki, H., Kato, H., SainoSaito, S., Matsumoto, N., Akaike, N., Noda, T., and Kondo, H. (2006). Altered emotional behavioral responses in mice lacking brain-type fatty acid-binding protein gene. Eur. J. Neurosci. 24, 175-187.
44. Owada, Y., Suzuki, I., Noda, T., and Kondo, H. (2002). Analysis on the phenotype of E-FABP-gene knockout mice. Mol. Cell. Biochem. 239, 83-86.
45. Owada, Y., Yoshimoto, T., and Kondo, H. (1996). Spatio-temporally differential expression of genes for three members of fatty acid binding proteins in developing and mature rat brains. J. Chem. Neuroanat. 12, 113-122.
46. Park, L., Wang, G., Zhou, P., Zhou J.,Pitstick,R.,Previti,M.L., Younkin, L., Younkin, S. G., Van Nostrand, W. E., Cho, S., Anrather, J., Carlson, G. A., and Iadecola, C. (2011). Scavenger receptor CD36 is essential for the cerebrovascular oxidative stress and neurovascular dysfunction induced by amyloidbeta. Proc. Natl. Acad. Sci. U.S.A. 108, 5063-5068.
47. Puente Navazo, M. D., Daviet, L., Ninio, E., and McGregor, J. L. (1996). Identification on human CD36 of a domain (155-183) implicated in binding oxidized low-density lipoproteins (Ox-LDL). Arterioscler. Thromb. Vasc. Biol. 16, 1033-1039.
48. Rapoport, S. I., Chang, M. C., and Spector, A. A. (2001). Delivery and turnover of plasma-derived essential PUFAs in mammalian brain. J. Lipid Res. 42, 678-685.
49. Salvati, S., Attorri, L., Di Benedetto, R., Di Biase, A., and Leonardi, F. (2006). Polyunsaturated fatty acids and neurological diseases. Mini Rev. Med. Chem. 6, 1201-1211.
50. Sawzdargo, M., George, S. R., Nguyen, T., Xu, S., Kolakowski, L. F., and O'dowd, B. F. (1997). A cluster of four novel human G proteincoupled receptor genes occurring in close proximity to CD22 gene on chromosome 19q13.1. Biochem. Biophys. Res. Commun. 239, 543-547.
51. Schaffer, J. E., and Lodish, H. F. (1994). Expression cloning and characterization of a novel adipocyte long chain fatty acid transport protein. Cell 79, 427-436.
52. Sellner, P. A., Chu, W., Glatz, J. F., and Berman, N. E. (1995). Developmental role of fatty acidbinding proteins in mouse brain. BrainRes.Dev.BrainRes.89, 33-46.
53. Setnik, B., and Nobrega, J. N. (2004). Long-chain acyl-CoenzymeA synthetase-2 mRNA: increased cerebral cortex expression in an animal model of depression. Prog. Neuropsychopharmacol. Biol. Psychiatry 28, 577-582.
54. Shioda, N., Yamamoto, Y., Watanabe, M., Binas, B., Owada, Y., and Fukunaga, K. (2010). Heart-type fatty acid binding protein regulates dopamine D-2 receptor function in mouse brain. J. Neurosci. 30, 3146-3155.
55. Song, B. J., Elbert, A., Rahman, T., Orr, S. K., Chen, C. T., Febbraio, M., and Bazinet, R. P. (2010). Genetic ablation of CD36 does not alter mouse brain polyunsaturated fatty acid concentrations. Lipids 45, 291-299.
56. Stewart, C. R., Stuart, L. M., Wilkinson, K.,VanGils,J.M.,Deng,J.,Halle, A., Rayner, K. J., Boyer, L., Zhong R.,Frazier,W.A.,Lacy-Hulbert, A., El Khoury, J., Golenbock, D. T., and Moore, K. J. (2010). CD36 ligands promote sterile inflammation through assembly of a Toll-like receptor 4 and 6 heterodimer. Nat. Immunol. 11, 155-161.
57. Stranahan, A. M., Norman, E. D., Lee, K., Cutler, R. G., Telljohann, R. S., Egan, J. M., and Mattson, M. P. (2008). Diet-induced insulin resistance impairs hippocampal synaptic plasticity and cognition in middle-aged rats. Hippocampus 18, 1085-1088.
58. Takeuchi, Y., and Fukunaga, K. (2003). Differential subcellular localization of two dopamine D2 receptor isoforms in transfected NG108-15 cells. J. Neurochem. 85, 1064-1074.
59. Utsunomiya, A., Owada, Y., Yoshimoto, T., and Kondo, H. (1997). Localization of mRNA for fatty acid transport protein in developing and mature brain of rats. Brain Res. Mol. Brain Res. 46, 217-222.
60. Watanabe, A., Toyota, T., Owada, Y., Hayashi, T., Iwayama, Y., Matsumata, M., Ishitsuka, Y., Nakaya, A., Maekawa, M., Ohnishi, T., Arai, R., Sakurai, K., Yamada, K., Kondo, H., Hashimoto, K., Osumi, N., and Yoshikawa, T. (2007). Fabp7 maps to a quantitative trait locus for a schizophrenia endophenotype. PLoS Biol. 5:e297. doi: 10.1371/journal.pbio.0050297
61. Wilkinson,K.,Boyd,J.D.,Glicksman, M., Moore, K. J., and El Khoury, J. (2011). A high content drug screen identifies ursolic acid as an inhibitor of amyloid beta protein interactions with its receptor CD36. J. Biol. Chem. 286, 34914-34922.
62. Yamashima, T. (2012). 'PUFA-GPR40CREB signaling' hypothesis for the adult primate neurogenesis. Prog. Lipid Res. 51, 221-231.