CD36-dependent signaling mediates fatty acid-induced gut release of secretin and cholecystokinin

FASEB Journal

Volumn 27, Issue 3, 2013, Pages 1191-1202

  Sundaresan, Sinju ^a   Shahid, Rafiq ^c   Riehl, Terrence E ^b   Chandra, Rashmi ^c   Nassir, Fatiha ^a   Stenson, William F ^b   Liddle, Rodger A ^c   Abumrad, Nada A ^a  

^a Center for Human Nutrition   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Calcium; CAMP; CCK

Indexed keywords

CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CD36 ANTIGEN; CHOLECYSTOKININ; CHROMOGRANIN A; CHYLOMICRON; CYCLIC AMP DEPENDENT PROTEIN KINASE; FATTY ACID; SECRETIN;

ANIMAL TISSUE; ARTICLE; CELL SUBPOPULATION; COCULTURE; CONTROLLED STUDY; DUODENUM; ENTEROENDOCRINE CELL; ENZYME ACTIVATION; HOMEOSTASIS; HORMONE RELEASE; IMMUNODETECTION; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; JEJUNUM; LIPID ABSORPTION; LIPID METABOLISM; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN SECRETION; SIGNAL TRANSDUCTION;

ANIMALS; ANTIGENS, CD36; CACO-2 CELLS; CHOLECYSTOKININ; CYCLIC AMP-DEPENDENT PROTEIN KINASES; DUODENUM; ENTEROENDOCRINE CELLS; ENZYME ACTIVATION; FATTY ACIDS; HUMANS; JEJUNUM; MICE; MICE, KNOCKOUT; SECRETIN; SIGNAL TRANSDUCTION;

EID: 84874610750     PISSN: None     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.12-217703     Document Type: Article

References (60)

1. Beglinger, C., and Degen, L. (2004) Fat in the intestine as a regulator of appetite-role of CCK. Physiol. Behav. 83, 617-621 (Pubitemid 40038512)
2. Liou, A. P., Lu, X., Sei, Y., Zhao, X., Pechhold, S., Carrero, R. J., Raybould, H. E., and Wank, S. (2011) The G-protein-coupled receptor GPR40 directly mediates long-chain fatty acid-induced secretion of cholecystokinin. Gastroenterology 140, 903-912
3. Liddle, R. A. (2000) Regulation of cholecystokinin secretion in humans. J. Gastroenterol. 35, 181-187 (Pubitemid 30195629)
4. Buchan, A. M., Polak, J. M., Solcia, E., Capella, C., Hudson, D., and Pearse, A. G. (1978) Electron immunohistochemical evidence for the human intestinal I cell as the source of CCK. Gut 19, 403-407 (Pubitemid 8342986)
5. Lam, I. P., Lee, L. T., Choi, H. S., and Chow, B. K. (2006) Localization of small heterodimer partner (SHP) and secretin in mouse duodenal cells. Ann. N. Y. Acad. Sci. 1070, 371-375 (Pubitemid 44126671)
6. Polak, J. M., Bloom, S., Coulling, I., and Pearse, A. G. (1971) Immunofluorescent localization of secretin in the canine duodenum. Gut 12, 605-610
7. Polak, J. M., Coulling, I., Bloom, S., and Pearse, A. G. (1971) Immunofluorescent localization of secretin and enteroglucagon in human intestinal mucosa. Scand. J. Gastroenterol. 6, 739-744
8. Little, T. J., and Feinle-Bisset, C. (2011) Effects of dietary fat on appetite and energy intake in health and obesity-oral and gastrointestinal sensory contributions. Physiol. Behav. 104, 613-620
9. Sclafani, A., and Ackroff, K. (2012) Role of gut nutrient sensing in stimulating appetite and conditioning food preferences. Am. J. Physiol. Regul. Integr. Comp. Physiol. 302, R1119-R1133
10. Berna, M. J., and Jensen, R. T. (2007) Role of CCK/gastrin receptors in gastrointestinal/metabolic diseases and results of human studies using gastrin/CCK receptor agonists/antagonists in these diseases. Curr. Top. Med. Chem. 7, 1211-1231 (Pubitemid 47044737)
11. Chey, W. Y., and Chang, T. M. (2003) Secretin, 100 years later. J. Gastroenterol. 38, 1025-1035 (Pubitemid 38016361)
12. Cheng, C. Y., Chu, J. Y., and Chow, B. K. (2011) Central and peripheral administration of secretin inhibits food intake in mice through the activation of the melanocortin system. Neuropsychopharmacology 36, 459-471
13. Dockray, G. J. (2012) Cholecystokinin. Curr. Opin. Endocrinol. Diabetes Obes. 19, 8-12
14. Hajri, T., and Abumrad, N. A. (2002) Fatty acid transport across membranes: relevance to nutrition and metabolic pathology. Annu. Rev. Nutr. 22, 383-415 (Pubitemid 35221466)
15. Oh, D. Y., and Lagakos, W. S. (2011) The role of G-protein-coupled receptors in mediating the effect of fatty acids on inflammation and insulin sensitivity. Curr. Opin. Clin. Nutr. Metab. Care 14, 322-327
16. Vinolo, M. A., Hirabara, S. M., and Curi, R. (2012) G-protein-coupled receptors as fat sensors. Curr. Opin. Clin. Nutr. Metab. Care 15, 112-116
17. Hirasawa, A., Tsumaya, K., Awaji, T., Katsuma, S., Adachi, T., Yamada, M., Sugimoto, Y., Miyazaki, S., and Tsujimoto, G. (2005) Free fatty acids regulate gut incretin glucagon-like peptide-1 secretion through GPR120. Nat. Med. 11, 90-94 (Pubitemid 40215843)
18. Oh, D. Y., Talukdar, S., Bae, E. J., Imamura, T., Morinaga, H., Fan, W., Li, P., Lu, W. J., Watkins, S. M., and Olefsky, J. M. (2010) GPR120 is an omega-3 fatty acid receptor mediating potent anti-inflammatory and insulin-sensitizing effects. Cell 142, 687-698
19. 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
20. Kuda, O., Jenkins, C. M., Skinner, J. R., Moon, S. H., Su, X., Gross, R. W., and Abumrad, N. A. (2011) CD36 protein is involved in store-operated calcium flux, phospholipase A2 activation, and production of prostaglandin E2. J. Biol. Chem. 286, 17785-17795
21. Khan, N. A., and Besnard, P. (2009) Oro-sensory perception of dietary lipids: new insights into the fat taste transduction. Biochim. Biophys. Acta 1791, 149-155
22. Laugerette, F., Passilly-Degrace, P., Patris, B., Niot, I., Febbraio, M., Montmayeur, J. P., and Besnard, P. (2005) CD36 involvement in orosensory detection of dietary lipids, spontaneous fat preference, and digestive secretions. J. Clin. Invest. 115, 3177-3184 (Pubitemid 41567582)
23. Pepino, M. Y., Love-Gregory, L., Klein, S., and Abumrad, N. A. (2012) The fatty acid translocase gene CD36 and lingual lipase influence oral sensitivity to fat in obese subjects. J. Lipid Res. 53, 561-566
24. Lobo, M. V., Huerta, L., Ruiz-Velasco, N., Teixeiro, E., de la Cueva, P., Celdran, A., Martin-Hidalgo, A., Vega, M. A., and Bragado, R. (2001) Localization of the lipid receptors CD36 and CLA-1/SR-BI in the human gastrointestinal tract: towards the identification of receptors mediating the intestinal absorption of dietary lipids. J. Histochem. Cytochem. 49, 1253-1260 (Pubitemid 32885388)
25. Nassir, F., Wilson, B., Han, X., Gross, R. W., and Abumrad, N. A. (2007) CD36 is important for fatty acid and cholesterol uptake by the proximal but not distal intestine. J. Biol. Chem. 282, 19493-19501 (Pubitemid 47100088)
26. Drover, V. A., Ajmal, M., Nassir, F., Davidson, N. O., Nauli, A. M., Sahoo, D., Tso, P., and Abumrad, N. A. (2005) CD36 deficiency impairs intestinal lipid secretion and clearance of chylomicrons from the blood. J. Clin. Invest. 115, 1290-1297 (Pubitemid 40629048)
27. Hsieh, J., Longuet, C., Maida, A., Bahrami, J., Xu, E., Baker, C. L., Brubaker, P. L., Drucker, D. J., and Adeli, K. (2009) Glucagon-like peptide-2 increases intestinal lipid absorption and chylomicron production via CD36. Gastroenterology 137, 997-1005, 1005.e1-1005.e4
28. Nauli, A. M., Nassir, F., Zheng, S., Yang, Q., Lo, C. M., Vonlehmden, S. B., Lee, D., Jandacek, R. J., Abumrad, N. A., and Tso, P. (2006) CD36 is important for chylomicron formation and secretion and may mediate cholesterol uptake in the proximal intestine. Gastroenterology 131, 1197-1207 (Pubitemid 44498699)
29. Edfalk, S., Steneberg, P., and Edlund, H. (2008) Gpr40 is expressed in enteroendocrine cells and mediates free fatty acid stimulation of incretin secretion. Diabetes 57, 2280-2287
30. Chang, C. H., Chey, W. Y., Erway, B., Coy, D. H., and Chang, T. M. (1998) Modulation of secretin release by neuropeptides in secretin-producing cells. Am. J. Physiol. 275, G192-G202
31. Parker, H. E., Reimann, F., and Gribble, F. M. (2010) Molecular mechanisms underlying nutrient-stimulated incretin secretion. Expert Rev. Mol. Med. 12, e1
32. Prpic, V., Basavappa, S., Liddle, R. A., and Mangel, A. W. (1994) Regulation of cholecystokinin secretion by calcium-dependent calmodulin kinase II: differential effects of phenylalanine and cAMP. Biochem. Biophys. Res. Commun. 201, 1483-1489 (Pubitemid 24234256)
33. Chandra, R., Samsa, L. A., Vigna, S. R., and Liddle, R. A. (2010) Pseudopod-like basal cell processes in intestinal cholecystokinin cells. Cell Tissue Res. 341, 289-297
34. Suzuki, S., Suzuki, H., Horiguchi, K., Tsugawa, H., Matsuzaki, J., Takagi, T., Shimojima, N., and Hibi, T. (2010) Delayed gastric emptying and disruption of the interstitial cells of Cajal network after gastric ischaemia and reperfusion. Neurogastroenterol. Motil. 22, 585-593, e126
35. Liddle, R. A., Goldfine, I. D., and Williams, J. A. (1984) Bioassay of plasma cholecystokinin in rats: effects of food, trypsin inhibitor, and alcohol. Gastroenterology 87, 542-549 (Pubitemid 14061405)
36. Tashiro, M., Samuelson, L. C., Liddle, R. A., and Williams, J. A. (2004) Calcineurin mediates pancreatic growth in protease inhibitor-treated mice. Am. J. Physiol. Gastrointest. Liver Physiol. 286, G784-G790 (Pubitemid 38506810)
37. Rehfeld, J. F. (1998) Accurate measurement of cholecystokinin in plasma. Clin. Chem. 44, 991-1001 (Pubitemid 28213139)
38. Smith, J., Su, X., El-Maghrabi, R., Stahl, P. D., and Abumrad, N. A. (2008) Opposite regulation of CD36 ubiquitination by fatty acids and insulin: effects on fatty acid uptake. J. Biol. Chem. 283, 13578-13585
39. Poirier, H., Degrace, P., Niot, I., Bernard, A., and Besnard, P. (1996) Localization and regulation of the putative membrane fatty-acid transporter (FAT) in the small intestine. Comparison with fatty acid-binding proteins (FABP). Eur. J. Biochem. 238, 368-373
40. Tran, T. T., Poirier, H., Clement, L., Nassir, F., Pelsers, M. M., Petit, V., Degrace, P., Monnot, M. C., Glatz, J. F., Abumrad, N. A., Besnard, P., and Niot, I. (2011) Luminal lipid regulates CD36 levels and downstream signaling to stimulate chylomicron synthesis. J. Biol. Chem. 286, 25201-25210
41. Varndell, I. M., Lloyd, R. V., Wilson, B. S., and Polak, J. M. (1985) Ultrastructural localization of chromogranin: a potential marker for the electron microscopical recognition of endocrine cell secretory granules. Histochem. J. 17, 981-992 (Pubitemid 16256478)
42. Cheung, A. T., Dayanandan, B., Lewis, J. T., Korbutt, G. S., Rajotte, R. V., Bryer-Ash, M., Boylan, M. O., Wolfe, M. M., and Kieffer, T. J. (2000) Glucose-dependent insulin release from genetically engineered K cells. Science 290, 1959-1962
43. Rindi, G., Grant, S. G., Yiangou, Y., Ghatei, M. A., Bloom, S. R., Bautch, V. L., Solcia, E., and Polak, J. M. (1990) Development of neuroendocrine tumors in the gastrointestinal tract of transgenic mice. Heterogeneity of hormone expression. Am. J. Pathol. 136, 1349-1363 (Pubitemid 20210334)
44. Lipsky, R. H., Eckert, D. M., Tang, Y., and Ockenhouse, C. F. (1997) The carboxyl-terminal cytoplasmic domain of CD36 is required for oxidized low-density lipoprotein modulation of NF-κB activity by tumor necrosis factor-α. Recept. Signal Transduct. 7, 1-11
45. Silverstein, R. L. (2009) Type 2 scavenger receptor CD36 in platelet activation: the role of hyperlipemia and oxidative stress. Clin. Lipidol. 4, 767
46. Harmon, C. M., Luce, P., Beth, A. H., and Abumrad, N. A. (1991) Labeling of adipocyte membranes by sulfo-N-succinimidyl derivatives of long-chain fatty acids: inhibition of fatty acid transport. J. Membr. Biol. 121, 261-268
47. Hussain, M. M. (2000) A proposed model for the assembly of chylomicrons. Atherosclerosis 148, 1-15
48. Levy, E., and Bendayan, M. (2000) Use of immunoelectron microscopy and intestinal models to explore the elaboration of apolipoproteins required for intraenterocyte lipid transport. Microsc. Res. Tech. 49, 374-382 (Pubitemid 30407773)
49. Mathias, A., Duc, M., Favre, L., Benyacoub, J., Blum, S., and Corthesy, B. (2010) Potentiation of polarized intestinal Caco-2 cell responsiveness to probiotics complexed with secretory IgA. J. Biol. Chem. 285, 33906-33913
50. Scott, L., Prpic, V., Capel, W. D., Basavappa, S., Mangel, A. W., Gettys, T. W., and Liddle, R. A. (1996) β-Adrenergic regulation of cholecystokinin secretion in STC-1 cells. Am. J. Physiol. 270, G291-G297
51. Seino, S., and Shibasaki, T. (2005) PKA-dependent and PKAindependent pathways for cAMP-regulated exocytosis. Physiol. Rev. 85, 1303-1342 (Pubitemid 41362272)
52. 2+ in two enteroendocrine cell lines, STC-1 and GLUTag. J. Physiol. 528 (Pt. 1), 165-176
53. Abumrad, N. A., and Davidson, N. O. (2012) Role of the gut in lipid homeostasis. Physiol. Rev. 92, 1061-1085
54. Tanaka, T., Katsuma, S., Adachi, T., Koshimizu, T. A., Hirasawa, A., and Tsujimoto, G. (2008) Free fatty acids induce cholecystokinin secretion through GPR120. Naunyn-Schmiedebergs Arch. Pharmacol. 377, 523-527
55. Burgoyne, R. D., and Morgan, A. (2003) Secretory granule exocytosis. Physiol. Rev. 83, 581-632 (Pubitemid 36378679)
56. Habib, A. M., Richards, P., Cairns, L. S., Rogers, G. J., Bannon, C. A., Parker, H. E., Morley, T. C., Yeo, G. S., Reimann, F., and Gribble, F. M. (2012) Overlap of endocrine hormone expression in the mouse intestine revealed by transcriptional profiling and flow cytometry. Endocrinology 153, 3054-3065
57. Portela-Gomes, G. M., Stridsberg, M., Johansson, H., and Grimelius, L. (1997) Complex co-localization of chromogranins and neurohormones in the human gastrointestinal tract. J. Histochem. Cytochem. 45, 815-822 (Pubitemid 27248797)
58. Lam, I. P., Siu, F. K., Chu, J. Y., and Chow, B. K. (2008) Multiple actions of secretin in the human body. Int. Rev. Cytol. 265, 159-190 (Pubitemid 351215988)
59. Love-Gregory, L., Sherva, R., Schappe, T., Qi, J. S., McCrea, J., Klein, S., Connelly, M. A., and Abumrad, N. A. (2011) Common CD36 SNPs reduce protein expression and may contribute to a protective atherogenic profile. Hum. Mol. Genet. 20, 193-201
60. Masuda, D., Hirano, K., Oku, H., Sandoval, J. C., Kawase, R., Yuasa-Kawase, M., Yamashita, Y., Takada, M., Tsubakio-Yamamoto, K., Tochino, Y., Koseki, M., Matsuura, F., Nishida, M., Kawamoto, T., Ishigami, M., Hori, M., Shimomura, I., and Yamashita, S. (2009) Chylomicron remnants are increased in the postprandial state in CD36 deficiency. J. Lipid Res. 50, 999-1011