Linoleic Acid Induces Calcium Signaling, Src Kinase Phosphorylation, and Neurotransmitter Release in Mouse CD36-positive Gustatory Cells
Year: 2008
Type: article
Abstract: We have recently demonstrated that the cells expressing CD36, localized apically on the taste buds of mouse lingual circumvallate papillae, act as gustatory cells. In the present study we isolated these CD36-positive cells from mouse circumvallate papillae and investigated intracellular signaling events, triggered by a long-chain polyunsaturated fatty acid, i.e. linoleic acid (LA). LA induced increases in free intracellular calcium concentrations, [Ca2+]i, by recruiting calcium from endoplasmic reticulum pool via inositol 1,4,5-triphosphate production followed by calcium influx via opening of store-operated calcium (SOC) channels. LA also induced phosphorylation of Src-protein-tyrosine kinases (Src-PTKs), particularly of Fyn59 and Yes62. LA-evoked phosphorylation of Fyn59 and Yes62 was implicated in the activation of SOC channels. Reverse transcription-quantitative PCR revealed that the CD36-positive gustatory cells possessed mRNA of enzymes like tryptophan hydroxylase-1, l-aromatic amino acid decarboxylase, tyrosine hydroxylase, and dopamine β-hydroxylase, involved in the synthesis of monoamine neurotransmitters. Interestingly, the addition of LA to these cells induced the release of 5-hydroxytryptamine and noradrenalin to the extracellular environment. The LA-induced release of these neurotransmitters was curtailed by SOC channel blockers and Src-PTK inhibitors. These results altogether demonstrate that LA binds to mouse CD36-positive gustatory cells, induces Src-PTKs phosphorylation, triggers calcium signaling, and evokes the release of 5-hydroxytryptamine and noradrenalin, which in turn may be implicated in the downstream signaling to the afferent nerve fibers, thus transmitting the output signal from taste buds to the central nervous system. We have recently demonstrated that the cells expressing CD36, localized apically on the taste buds of mouse lingual circumvallate papillae, act as gustatory cells. In the present study we isolated these CD36-positive cells from mouse circumvallate papillae and investigated intracellular signaling events, triggered by a long-chain polyunsaturated fatty acid, i.e. linoleic acid (LA). LA induced increases in free intracellular calcium concentrations, [Ca2+]i, by recruiting calcium from endoplasmic reticulum pool via inositol 1,4,5-triphosphate production followed by calcium influx via opening of store-operated calcium (SOC) channels. LA also induced phosphorylation of Src-protein-tyrosine kinases (Src-PTKs), particularly of Fyn59 and Yes62. LA-evoked phosphorylation of Fyn59 and Yes62 was implicated in the activation of SOC channels. Reverse transcription-quantitative PCR revealed that the CD36-positive gustatory cells possessed mRNA of enzymes like tryptophan hydroxylase-1, l-aromatic amino acid decarboxylase, tyrosine hydroxylase, and dopamine β-hydroxylase, involved in the synthesis of monoamine neurotransmitters. Interestingly, the addition of LA to these cells induced the release of 5-hydroxytryptamine and noradrenalin to the extracellular environment. The LA-induced release of these neurotransmitters was curtailed by SOC channel blockers and Src-PTK inhibitors. These results altogether demonstrate that LA binds to mouse CD36-positive gustatory cells, induces Src-PTKs phosphorylation, triggers calcium signaling, and evokes the release of 5-hydroxytryptamine and noradrenalin, which in turn may be implicated in the downstream signaling to the afferent nerve fibers, thus transmitting the output signal from taste buds to the central nervous system. The tongue contains primarily four types of papillae. Filiforms are involved in the somesthesic perception of foods, whereas fungiforms, foliates, and circumvallates, which contain taste buds, are responsible for the chemosensory perception of basic taste modalities (sweet, bitter, salt, sour, umami). Recent evidences have strongly suggested the existence of an additive oro-sensory system devoted to the dietary fat perception in rodents. Gilbertson et al. (1Gilbertson T.A. Fontenot D.T. Liu L. Zhang H. Monroe W.T. Am. J. Physiol. 1997; 272: C1203-C1210Crossref PubMed Google Scholar) have reported that lipids may be sensed by isolated rat fungiform taste receptor cells (TRC) 2The abbreviations used are: TRC, taste receptor cells; CVP, circumvallate papillae; 5-HT, 5-hydroxytryptamine (serotonin); PLC, phospholipase C; PTK, protein-tyrosine kinase; SSO, sulfo-N-succinimidyl oleate; PBS, phosphate-buffered saline; IP3, inositol 1,4,5-triphosphate; LA, linoleic acid; PVDF, polyvinylidene difluoride; TBS, Tris-buffered saline; RT, reverse transcription; Ct, cycle threshold; HPLC, high performance liquid chromatography; ER, endoplasmic reticulum; NA, noradrenalin; SOC, store-operated calcium. via the inhibition of the delayed rectifying K+ channels by polyunsaturated fatty acids. Fukuwatari et al. (2Fukuwatari T. Kawada T. Tsuruta M. Hiraoka T. Iwanaga T. Sugimoto E. Fushiki T. FEBS Lett. 1997; 414: 461-464Crossref PubMed Scopus (208) Google Scholar) and Laugerette et al. (3Laugerette F. Passilly-Degrace P. Patris B. Niot I. Febbraio M. Montmayeur J.P. Besnard P. J. Clin. Investig. 2005; 115: 3177-3184Crossref PubMed Scopus (518) Google Scholar) documented the expression of the receptor-like lipid-binding protein CD36 in rat and mouse taste bud cells, respectively. Kawai and Fushiki (4Kawai T. Fushiki T. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2003; 285: 447-454Crossref PubMed Scopus (189) Google Scholar) demonstrated that the addition of a lipase inhibitor diminished the spontaneous preference for triglycerides. These investigators proposed that the lingual lipase, present in the rodent saliva, might release free fatty acids that would be detected by gustatory cells. The immunolocalization of CD36 in the apical side of few TRC in circumvallate papillae (3Laugerette F. Passilly-Degrace P. Patris B. Niot I. Febbraio M. Montmayeur J.P. Besnard P. J. Clin. Investig. 2005; 115: 3177-3184Crossref PubMed Scopus (518) Google Scholar) is especially adequate for this function since CD36 is known to exhibit a very high affinity for long-chain fatty acids (5Baillie A.G. Coburn C.T. Abumrad N.A. J. Membr. Biol. 1996; 153: 75-81Crossref PubMed Scopus (188) Google Scholar). Consistent with this assumption, we have recently provided the first evidence that CD36-positive gustatory cells play a significant role in dietary lipid perception in the mouse (3Laugerette F. Passilly-Degrace P. Patris B. Niot I. Febbraio M. Montmayeur J.P. Besnard P. J. Clin. Investig. 2005; 115: 3177-3184Crossref PubMed Scopus (518) Google Scholar). Indeed, the CD36 gene inactivation fully abolished the spontaneous preference for long-chain fatty acids observed in wild-type mice (3Laugerette F. Passilly-Degrace P. Patris B. Niot I. Febbraio M. Montmayeur J.P. Besnard P. J. Clin. Investig. 2005; 115: 3177-3184Crossref PubMed Scopus (518) Google Scholar). It is noteworthy that this effect on feeding behavior is lipid-specific since sweet preference and bitter aversion are not affected in these transgenic mice (3Laugerette F. Passilly-Degrace P. Patris B. Niot I. Febbraio M. Montmayeur J.P. Besnard P. J. Clin. Investig. 2005; 115: 3177-3184Crossref PubMed Scopus (518) Google Scholar). To further explore whether a sixth taste modality devoted to the “fat” functionally exists in rodents, the downstream signaling events triggered by the free fatty acid/CD36 interaction in gustatory cells must be studied. We have for the first time purified the CD36-positive gustatory cells from mouse CVP and demonstrated that linoleic acid induced increases in [Ca2+]i in these cells via CD36 (6Gaillard, D., Laugerette, F., Darcel, N., El-Yassimi, A., Degrace-Passily, P., Hichami, A., Khan, N. A., Montmayeur, J. P., and Besnard, P. (2007) FASEB J., in pressGoogle Scholar). In the present study we have extended these investigations to characterize the mechanisms of action of linoleic acid on calcium signaling/protein phosphorylation, leading to the release of neurotransmitters, which might be implicated in the activation of afferent nerve fibers. Materials—C57BL/6J mice were obtained from Janvier Elevage (Le Genest-st-isle, France). Sulfo-N-succinimidyloleate (SSO) was a generous gift from JF Glatz (Maastricht, The Netherlands). The culture medium RPMI 1640 and l-glutamine were purchased from Lonza Verviers SPRL (Verviers, Belgium). Fura-2/AM was procured from Invitrogen. All other chemicals including linoleic acid (18:2 n-6), collagenase type-I, and trypsin inhibitor were obtained from Sigma. SKF96365, econazole, and SU6656 were purchased from Calbiochem. Elastase and dispase were purchased from Serlabo (Bonneuil/Marne, France) and Roche Diagnostics, respectively. Anti-CD36 antibody coupled to phycoerythrin and anti-α-gustducin antibody were procured from Santa Cruz Biotechnology, Inc. Anti-p-Fyn59, anti-p-Lyn53/56, and anti-p-Yes62 antibodies were bought from Tebu-Bio (Paris, France), and anti-phosphotyrosine kinase (p-PTK) antibody was obtained from Chemicon (Dundee, UK). Anti-CD36 antibody was procured from Cell Sciences®. All the experiments on animals were conducted as per declaration of Helsinki and European ethical guidelines, and the protocols were approved by the Regional Ethical Committee. Isolation of CD36-positive Cells from Mouse Circumvallate Papillae (CVP)—Mouse lingual CVP were isolated according to previously published procedure (3Laugerette F. Passilly-Degrace P. Patris B. Niot I. Febbraio M. Montmayeur J.P. Besnard P. J. Clin. Investig. 2005; 115: 3177-3184Crossref PubMed Scopus (518) Google Scholar). Lingual epithelium was separated from connective tissues by enzymatic dissociation (elastase and dispase mixture, 2 mg/ml each, in Tyrode buffer: 120 mm NaCl, 5 mm KCl, 10 mm HEPES, 1 mm CaCl2, 1 mm MgCl2, 10 mm glucose, 10 mm sodium pyruvate, pH 7.4), and papillae were dissected under a microscope. The CD36-positive cells from mouse CVP were purified as described elsewhere (6Gaillard, D., Laugerette, F., Darcel, N., El-Yassimi, A., Degrace-Passily, P., Hichami, A., Khan, N. A., Montmayeur, J. P., and Besnard, P. (2007) FASEB J., in pressGoogle Scholar). In brief, cells were isolated by incubation in RPMI 1640 medium containing 2 mm EDTA, 1.2 mg/ml elastase, 0.6 mg/ml collagenase (type I), and 0.6 mg/ml trypsin inhibitor for followed by a 10 The of was with antibody coupled to phycoerythrin for 2 followed by a with 10 and in a containing coupled to The CD36-positive cells were isolated by the of the system. The cells the whereas CD36-positive cells were the cells were in a RPMI 1640 medium containing and mg/ml a and for the of this cells were used for the experiments with to To the of CD36-positive cells, we an of CD36 and were in and in PBS, pH were in containing and for incubation with a of CD36 antibody a of It is noteworthy that the also mouse CD36 (3Laugerette F. Passilly-Degrace P. Patris B. Niot I. Febbraio M. Montmayeur J.P. Besnard P. J. Clin. Investig. 2005; 115: 3177-3184Crossref PubMed Scopus (518) Google Scholar). were for 2 with for CD36 expression with for was by in the of with PBS, a of medium was on the for the under of and CD36-positive gustatory cells, for were with PBS, pH The of was as mm mm mm The cells were with Fura-2/AM for in which mm NaCl, mm KCl, mm mm MgCl2, mm mm mm 1.2 mm CaCl2, and the pH was to the cells were 10 and in the experiments in was by [Ca2+]i was according to et al. M. J. Biol. PubMed Scopus Google Scholar). The were in the in and and The cells were the The were the in with in The intracellular of free [Ca2+]i, were by the [Ca2+]i is the dissociation for is the with by is the in the of is the of [Ca2+]i, and is the of and of for was the and were obtained by the addition of and respectively. The SOC channel blockers and CD36 inhibitor protein-tyrosine kinase and were to the cells for the addition of linoleic of The and CD36-positive gustatory cells were with LA in the of for The for cells were with Cell was with acid the was for production according to the with the is on and for to The is separated from the free by which the protein to the of the The free in the is by the The is with a and of we detected the of CD36 and kinases and in CD36-positive cells by the antibodies we detected LA-induced phosphorylation tyrosine by the cells were with for not with LA as described in the of and cells were for 1 with of mm HEPES, pH 2 mm EDTA, mm NaCl, 1 mm 1 mm sodium mg/ml in the of mm 10 5 The were and were to To of of was in the To the phosphorylation of we first the gustatory cells with and with antibodies and 1 of protein was with 1 of antibody and of were with and with were separated on and the for 1 in the mm NaCl, with the was with antibodies for 2 in the the was for 1 with antibody in with The was in and in The were revealed with the from To the of the of of and was in of mRNA of in the of by PCR and was from and CD36-positive gustatory cells by and to the of was with according to the time PCR was on the time and was by were on the of mice gene in The was in a of that of mm KCl, mm pH mm MgCl2, mm of and and of and of the used to study the expression of mRNA of in a The of an for 5 as a followed by for and for with a the of the the of the the was from to a of 2 and the was to the The were for gene of to PCR All were in of to were by including and cycle of mRNA in was as of gene of of of CD36-positive cells of cells. was as was in the as described for followed by a of for 10 were on a with The was by of by of monoamine neurotransmitters was as described elsewhere F. L. P. J. Comp. PubMed Scopus Google Scholar). and CD36-positive gustatory cells were with LA, as in the and the of incubation was and with of acid, mm EDTA, mm sodium of an was to were for The were by with a reverse 5 with as described previously PubMed Scopus Google Scholar). The of the was The of sodium mm EDTA, mm acid, pH The were and in with the of was used to in isolated CD36-positive gustatory cells. is to the and is not to the cells PubMed Scopus Google Scholar). these experiments the cells were as described for [Ca2+]i the cells were to the and of was The of was in The cells were to with the and 10 were The were and of was France). The of the was by of followed by a significant the the was in [Ca2+]i in CD36-positive explore whether LA triggers a calcium via CD36 we purified the CD36-positive gustatory cells which CD36 and a as a of TRC We observed that LA induced a in [Ca2+]i which was followed by a in and LA-induced increases in [Ca2+]i were in in calcium We also the production of IP3, known to calcium from endoplasmic reticulum that LA induced increases in production in to cells. To on whether LA induces the production of via to CD36, we sulfo-N-succinimidyl of (SSO) which is known to the of fatty acids to CD36 Abumrad N.A. J. Membr. Biol. PubMed Scopus Google Scholar). We observed that curtailed LA-induced increases in in these cells. as the cells are we observed that these cells, in to LA, a in [Ca2+]i in the in in cells, LA to and effect on It is to that effect on of the as by LA via a in CD36-positive LA-induced increases in [Ca2+]i are in calcium in is that LA a calcium to calcium from in CD36-positive gustatory cells. To this we conducted experiments in calcium in the of and econazole, the of store-operated calcium (SOC) channels. that the addition of diminished the LA-induced increases in [Ca2+]i in CD36-positive gustatory cells. These SOC channel blockers effect on gustatory cells have to the activation of SOC channels J. Biol. PubMed Scopus Google we investigated the of in the LA-induced SOC We used the of to the of in a known to and SU6656 inhibitor of and We observed that in CD36-positive gustatory cells, these abolished the increases in [Ca2+]i, induced by these in cells LA the of and in CD36-positive observed that mouse lingual CD36-positive gustatory cells CD36, and and The cells also these Src-PTK to a CD36-positive cells. The not the of Src-PTK that LA induced the phosphorylation of which was 5 and of the LA-induced phosphorylation of was abolished by in these cells In cells, LA to phosphorylation, and effect on the we the with and detected of We that LA induced the phosphorylation of Fyn59 and not of 5 and of incubation mRNA of the in the of in CD36-positive we have the expression of mRNA of the enzymes involved in the synthesis of and We have tryptophan mRNA as the gene that for the synthesis of tryptophan in tissues M. N. E. L. F. M. Am. J. Physiol. Physiol. PubMed Scopus Google Scholar). to We have also detected l-aromatic amino acid that to amino acid detected in and cells T. PubMed Scopus Google Scholar). We have also the mRNA of the enzymes involved in the of like tyrosine that tyrosine to and dopamine that dopamine to We the expression of monoamine implicated in the and release of neurotransmitters. We observed that CD36-positive gustatory cells a high of tryptophan and l-aromatic amino acid mRNA and tyrosine are in purified CD36-positive gustatory cells and were present in and cells monoamine mRNA is in CD36-positive gustatory cells and It is also noteworthy that the cells also in the and of and in CD36-positive first we the of neurotransmitters. the of a of the of CD36-positive gustatory cells, the of and in these cells. dopamine was and the was not we the of by the the and a of dopamine was in these cells. cells to and a of which that in CD36-positive cells in CD36-positive gustatory cells, LA induced increases in the release of and with cells. To on whether the of LA to CD36 is implicated in the release of and NA, we We observed that curtailed the LA-induced release of neurotransmitters the extracellular and Interestingly, LA to the release of and in cells, and effect on the and We further SOC channel blockers and to the of SOC channels and phosphorylation in the release of and that and diminished the LA-induced release of neurotransmitters the extracellular from CD36-positive cells the from cells and SU6656 the release of and from CD36-positive cells the from cells We also to demonstrate that an in [Ca2+]i is for the release of neurotransmitters. we observed that this [Ca2+]i in types of cells and this induced the release of and from CD36-positive cells not from cells and LA in CD36-positive To whether LA induces we the in the in these cells by We observed that LA induced the in CD36-positive cells a we used KCl, and as this also induced in these cells are to CD36-positive cells as the cells not We have recently isolated the CD36-positive gustatory cells to a high of from mouse lingual These purified cells, and have to CD36 mRNA (6Gaillard, D., Laugerette, F., Darcel, N., El-Yassimi, A., Degrace-Passily, P., Hichami, A., Khan, N. A., Montmayeur, J. P., and Besnard, P. (2007) FASEB J., in pressGoogle with of CD36 and in circumvallate papillae (3Laugerette F. Passilly-Degrace P. Patris B. Niot I. Febbraio M. Montmayeur J.P. Besnard P. J. Clin. Investig. 2005; 115: 3177-3184Crossref PubMed Scopus (518) Google Scholar). we have that LA induced a significant in [Ca2+]i (6Gaillard, D., Laugerette, F., Darcel, N., El-Yassimi, A., Degrace-Passily, P., Hichami, A., Khan, N. A., Montmayeur, J. P., and Besnard, P. (2007) FASEB J., in pressGoogle we not whether this fatty acid calcium from an intracellular extracellular environment. In the present study we have the of action of LA in isolated CD36-positive gustatory cells. We have observed that LA induces increases in [Ca2+]i in the of calcium in the extracellular that LA calcium from intracellular We further observed that LA induced the production of IP3, and diminished this in CD36-positive gustatory cells. These that LA, by to CD36, calcium from pool via a Interestingly, LA to increases in [Ca2+]i in cells, and effect on the on increases in [Ca2+]i the study of et al. M. B. J. Physiol. 1996; Scopus Google Scholar) have the production of and increases in [Ca2+]i in to in rat to be whether CD36 is coupled to activation of in CD36-positive gustatory cells. is known on the of CD36 to et al. F. PubMed Scopus Google Scholar) have that CD36 and are in in and activation of results in the phosphorylation of Src-PTK and activation of The may be in lipid gustatory cells. the like which may Src-PTK phosphorylation and activation in CD36-positive cells, to be J. PubMed Scopus Google Scholar). TRC have to J. Comp. PubMed Scopus Google Scholar). per the of calcium the of intracellular of calcium is followed by calcium influx via the opening of calcium channels to the intracellular Physiol. 2005; PubMed Scopus Google Scholar). These channels have calcium and is as as the are not Physiol. 2005; PubMed Scopus Google Scholar). To whether LA-induced of calcium from pool results in the opening of SOC we SOC channel which as the LA-induced calcium in calcium The SOC channel blockers effect in cells. results on CD36-positive gustatory cells are in with et al. F. Cell 2003; PubMed Scopus Google have that mouse TRC SOC channels. as the of SOC channels is have suggested a role for phosphorylation I. B. PubMed Scopus Google PubMed Scopus Google Scholar). It is also noteworthy that CD36 to be coupled to Src-PTK phosphorylation in types like and cells PubMed Scopus Google Scholar). We observed that of and kinases diminished the LA-induced increases in [Ca2+]i in CD36-positive gustatory cells. These effect on cells. the of LA to CD36 to in the phosphorylation of as phosphorylation, by this fatty acid in CD36-positive gustatory cells. We also that Fyn59 and the were also by LA in CD36-positive gustatory cells. We would like to that the cells of these the CD36-positive gustatory cells, and LA induced the phosphorylation in the It is to that is not by types of cells. We further observed that Fyn59 and Yes62 the opening of SOC channels in to LA in CD36-positive gustatory cells. be by the results of et al. J. Biol. 1997; 272: PubMed Scopus Google Scholar) have that is diminished in from and SOC influx be to by with in [Ca2+]i have to be involved in including release M. P. M. Biol. PubMed Scopus Google Scholar). have proposed for gustatory TRC and afferent fibers, including NA, 5-HT, amino acids and and and Physiol. PubMed Scopus Google T. 1996; PubMed Scopus Google Scholar). these that may be the taste bud PubMed Scopus Google M. Cell PubMed Scopus Google E. I. Biol. 2005; Google Scholar). To whether CD36-positive gustatory cells the neurotransmitters and release with LA, we conducted further We observed that CD36-positive gustatory cells the of tryptophan and l-aromatic amino acid that have reported the of l-aromatic amino acid T. Cell Biol. PubMed Scopus Google Scholar) and tryptophan T. F. FEBS Lett. PubMed Scopus Google Scholar) in mouse taste Interestingly, tyrosine and dopamine were also present to a in these cells. We further observed that the addition of LA to CD36-positive gustatory cells induced a significant release of and the extracellular environment. To is the first study to and in mouse of the conducted have detected these neurotransmitters M. N. PubMed Scopus Google Scholar) with E. I. Biol. 2005; Google Scholar). LA-induced release of and is via CD36 as curtailed the Interestingly, the release of these neurotransmitters to be by calcium influx as SOC channel blockers abolished the LA-induced release of neurotransmitters. We that the phosphorylation Src-PTKs is implicated in the opening of SOC channels. the Src-PTKs abolished the LA-induced release of the the extracellular The of further the of calcium in the of neurotransmitters as this induced increases in [Ca2+]i and the release of and in CD36-positive gustatory cells. the of et al. E. I. Biol. 2005; Google Scholar) have by that increases in [Ca2+]i release in to taste et al. J. PubMed Scopus Google Scholar) have reported the release of amino acids in a in of 2003; PubMed Scopus Google Scholar) demonstrated that activation of kinases is responsible of the release of in rat nerve The for the first time evidence on the of with the release of and in lipid gustatory cells. We would like to that we have detected the mRNA of monoamine which is implicated in monoamine neurotransmitters for and We have also observed that CD36-positive gustatory cells are as LA and induced the which may also to the of neurotransmitters in these cells. It is noteworthy that the in these cells be to calcium influx via calcium channels since and the of and calcium to the LA-induced calcium and these diminished the of on and calcium influx not is that the receptor channels may be implicated in LA-induced as Liu and 2003; PubMed Scopus Google Scholar) have that an in [Ca2+]i channels which responsible for the of the The TRC have to the receptor channels PubMed Scopus Google Scholar). et al. Am. J. Physiol. Regul. Integr. Comp. Physiol. PubMed Scopus Google Scholar) have demonstrated that receptor mice preference for fat and the of these channels in lipid taste the of the release of these neurotransmitters, we that these might via present on the cells. Indeed, and are in rat taste the is present on TRC, and the is on afferent N. T. Am. J. Physiol. Regul. Integr. Comp. Physiol. PubMed Scopus Google Scholar). on the of in papillae, a of TRC to and and of N. T. J. Physiol. Scopus Google Scholar). we that and from lipid gustatory cells may in a the present on afferent nerve fibers. be by the of et al. T. Cell Biol. PubMed Scopus Google Scholar) have that a of taste bud cells, which contains the with nerve the of we that LA, by to CD36, the phosphorylation of Src-PTK and activation of PLC, leading to the production of IP3, which from the followed by calcium influx via the opening of SOC channels. the opening of SOC channels in CD36-positive gustatory cells in [Ca2+]i of and the extracellular and these in turn afferent nerve fibers, which on the and of taste to the to be as to which of cells (type the CD36-positive gustatory cells are to whether CD36-positive gustatory cells nerve and whether these cells the protein and as is used by in the central nervous system for The investigations in these are in in We to J. F. the for the generous gift of We J. for the of neurotransmitters. We also to of of for the generous gift of the mouse
Source: Journal of Biological Chemistry
Institutions: Université de Bourgogne, Inserm
Language: English
Subfield: Nutrition and Dietetics
Field: Nursing
Domain: Health Sciences
Open Access status: hybrid
Estimated APC paid: $3,430
OpenAlex ID: W2016612191