Interactions between cd36 and global intestinal alkaline phosphatase in mouse small intestine and effects of high-fat diet

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 301, Issue 6, 2011, Pages 1738-1747

  Lynes, Matthew ^a   Narisawa, Sonoko ^b   Millán, José Luis ^b   Widmaier, Eric P ^a  

^a Boston University   (United States)

^b BURNHAM INSTITUTE   (United States)

Author keywords

Adiposity; Enterocytes; Intestinal plasticity; Obesity; Phosphorylation

Indexed keywords

ALKALINE PHOSPHATASE; ALKALINE PHOSPHATASE ISOENZYME; ANTISERUM; CD36 ANTIGEN; ENZYME INHIBITOR; INTESTINE ENZYME; LEPTIN; LONG CHAIN FATTY ACID; RECOMBINANT ENZYME; SULFOSUCCINIMIDYL OLEATE; TRIACYLGLYCEROL; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INDUCTION; ENZYME LOCALIZATION; ENZYME PHOSPHORYLATION; ENZYME SUBSTRATE; FATTY ACID TRANSPORT; FLUORESCENCE; HORMONE BLOOD LEVEL; IMMUNOPRECIPITATION; INTESTINE CELL; LIPID DIET; MALE; MOUSE; NONHUMAN; OBESITY; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN EXPRESSION; PROTEIN INTERACTION; SMALL INTESTINE MUCOSA; TRIACYLGLYCEROL BLOOD LEVEL;

ALKALINE PHOSPHATASE; ANIMALS; ANTIGENS, CD36; CELLS, CULTURED; CHO CELLS; CRICETINAE; DIETARY FATS; ENTEROCYTES; GENE EXPRESSION REGULATION; INTESTINE, SMALL; ISOENZYMES; MALE; MICE; MICE, INBRED C57BL;

EID: 82755192256     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00235.2011     Document Type: Article

References (61)

1. Abumrad NA, Park JH, Park CR. Permeation of long-chain fatty acid into adipocytes. Kinetics, specificity, and evidence for involvement of a membrane protein. J Biol Chem 259: 8945-8953, 1984.
2. Asch AS, Barnwell J, Silverstein RL, Nachman RL. Isolation of the thrombospondin membrane receptor. J Clin Invest 79: 1054-1061, 1987.
3. Asch AS, Liu I, Briccetti FM, Barnwell JW, Kwakye-Berko F, Dokun A, Goldberger J, Pernambuco M. Analysis of CD36 binding domains: ligand specificity controlled by dephosphorylation of an ectodomain. Science 262: 1436-1440, 1993.
4. Bader A, Hansen T, Kirchner G, Allmeling C, Haverich A, Borlak JT. Primary porcine enterocyte and hepatocyte cultures to study drug oxidation reactions. Br J Pharmacol 129: 331-342, 2000.
5. Baillie AG, Coburn CT, Abumrad NA. Reversible binding of long-chain fatty acids to purified FAT, the adipose CD36 homolog. J Membr Biol 153: 75-81, 1996.
6. Bastie CC, Hajri T, Drover VA, Grimaldi PA, Abumrad NA. CD36 in myocytes channels fatty acids to a lipase-accessible triglyceride pool that is related to cell lipid and insulin responsiveness. Diabetes 53: 2209-2216, 2004.
7. Berglund L, Petersen TE, Rasmussen JT. Structural characterization of bovine CD36 from the milk fat globule membrane. Biochim Biophys Acta 1309: 63-68, 1996.
8. Bonen A, Campbell SE, Benton CR, Chabowski A, Coort SL, Han XX, Koonen DP, Glatz JF, Luiken JJ. Regulation of fatty acid transport by fatty acid translocase/CD36. Proc Nutr Soc 63: 245-249, 2004.
9. Bonen A, Luiken JJ, Liu S, Dyck DJ, Kiens B, Kristiansen S, Turcotte LP, Van Der Vusse GJ, Glatz JF. Palmitate transport and fatty acid transporters in red and white muscles. Am J Physiol Endocrinol Metab 275: E471-E478, 1998.
10. Bossi M, Hoylaerts MF, Millán JL. Modifications in a flexible surface loop modulate the isozyme-specific properties of mammalian alkaline phosphatases. J Biol Chem 268: 25409-25416, 1993.
11. Di Mauro S, Manes T, Hessle L, Kozlenkov A, Pizauro JM, Hoylaerts MF, Millán JL. Kinetic characterization of hypophosphatasia mutations with physiological substrates. J Bone Miner Res 17: 1383-1391, 2002.
12. Dobozy A, Hunyadi J, Bozoky B, Monostori E, Ando I, Kenderessy AS, Tiba A. The mouse erythrocyte binding receptor is expressed on human keratinocytes. Dermatol Monatsschr 176: 615-621, 1990.
13. Drover VA, Ajmal M, Nassir F, Davidson NO, Nauli AM, Sahoo D, Tso P, Abumrad NA. CD36 deficiency impairs intestinal lipid secretion and clearance of chylomicrons from the blood. J Clin Invest 115: 1290- 1297, 2005.
14. Ehehalt R, Sparla R, Kulaksiz H, Herrmann T, Fullekrug J, Stremmel W. Uptake of long chain fatty acids is regulated by dynamic interaction of FAT/CD36 with cholesterol/sphingolipid enriched microdomains (lipid rafts). BMC Cell Biol 9: 45, 2008.
15. Endemann G, Stanton LW, Madden KS, Bryant CM, White RT, Protter AA. CD36 is a receptor for oxidized low density lipoprotein. J Biol Chem 268: 11811-11816, 1993.
16. Glatz JF, Luiken JJ, Bonen A. Membrane fatty acid transporters as regulators of lipid metabolism: implications for metabolic disease. Physiol Rev 90: 367-417, 2010.
17. Greenwalt DE, Watt KW, So OY, Jiwani N. PAS IV, an integral membrane protein of mammary epithelial cells, is related to platelet and endothelial cell CD36 (GP IV). Biochemistry 29: 7054-7059, 1990.
18. Gregoire FM, Zhang Q, Smith SJ, Tong C, Ross D, Lopez H, West DB. Diet-induced obesity and hepatic gene expression alterations in C57BL/6J and ICAM-1-deficient mice. Am J Physiol Endocrinol Metab 282: E703-E713, 2002.
19. Guthmann F, Maehl P, Preiss J, Kolleck I, Rustow B. Ectoprotein kinase-mediated phosphorylation of FAT/CD36 regulates palmitate uptake by human platelets. Cell Mol Life Sci 59: 1999-2003, 2002.
20. Hajri T, Ibrahimi A, Coburn CT, Knapp FF Jr, Kurtz T, Pravenec M, Abumrad NA. Defective fatty acid uptake in the spontaneously hypertensive rat is a primary determinant of altered glucose metabolism, hyperinsulinemia, and myocardial hypertrophy. J Biol Chem 276: 23661-23666, 2001.
21. Hansen GH, Immerdal L, Thorsen E, Niels-Christiansen LL, Nystrom BT, Demant EJ, Danielsen EM. Lipid rafts exist as stable cholesterolindependent microdomains in the brush border membrane of enterocytes. J Biol Chem 276: 32338-32344, 2001.
22. Hansen GH, Niels-Christiansen LL, Immerdal L, Nystrom BT, Danielsen EM. Intestinal alkaline phosphatase: selective endocytosis from the enterocyte brush border during fat absorption. Am J Physiol Gastrointest Liver Physiol 293: G1325-G1332, 2007.
23. Harmon CM, Abumrad NA. Binding of sulfosuccinimidyl fatty acids to adipocyte membrane proteins: isolation and amino-terminal sequence of an 88-kD protein implicated in transport of long-chain fatty acids. J Membr Biol 133: 43-49, 1993.
24. Hatmi M, Gavaret JM, Elalamy I, Vargaftig BB, Jacquemin C. Evidence for cAMP-dependent platelet ectoprotein kinase activity that phosphorylates platelet glycoprotein IV (CD36). J Biol Chem 271: 24776-24780, 1996.
25. Hinnebusch BF, Siddique A, Henderson JW, Malo MS, Zhang W, Athaide CP, Abedrapo MA, Chen X, Yang VW, Hodin RA. Enterocyte differentiation marker intestinal alkaline phosphatase is a target gene of the gut-enriched Kruppel-like factor. Am J Physiol Gastrointest Liver Physiol 286: G23-G30, 2004.
26. Ho M, Hoang HL, Lee KM, Liu N, MacRae T, Montes L, Flatt CL, Yipp BG, Berger BJ, Looareesuwan S, Robbins SM. Ectophosphorylation of CD36 regulates cytoadherence of Plasmodium falciparum to microvascular endothelium under flow conditions. Infect Immun 73: 8179-8187, 2005.
27. Hoosdally SJ, Andress EJ, Wooding C, Martin CA, Linton KJ. The human scavenger receptor CD36: glycosylation status and its role in trafficking and function. J Biol Chem 284: 16277-16288, 2009.
28. Hwang EH, Taki J, Yasue S, Fujimoto M, Taniguchi M, Matsunari I, Nakajima K, Shiobara S, Ikeda T, Tonami N. Absent myocardial iodine-123-BMIPP uptake and platelet/monocyte CD36 deficiency. J Nucl Med 39: 1681-1684, 1998.
29. Ibrahimi A, Sfeir Z, Magharaie H, Amri EZ, Grimaldi P, Abumrad NA. Expression of the CD36 homolog (FAT) in fibroblast cells: effects on fatty acid transport. Proc Natl Acad Sci USA 93: 2646-2651, 1996.
30. Kannan S. E-NTPase/NTPDase: potential role as a regulatory element in inflammation. Med Hypotheses 58: 527-528, 2002.
31. Kannan S. Regulatory role of E-NTPase/NTPDase in FAT/CD36-mediated fatty acid uptake. Cell Biol Int 27: 147-151, 2003.
32. Kintaka T, Tanaka T, Imai M, Adachi I, Narabayashi I, Kitaura Y. CD36 genotype and long-chain fatty acid uptake in the heart. Circ J 66: 819-825, 2002.
33. Lalles JP. Intestinal alkaline phosphatase: multiple biological roles in maintenance of intestinal homeostasis and modulation by diet. Nutr Rev 68: 323-332, 2010.
34. Liang CP, Han S, Okamoto H, Carnemolla R, Tabas I, Accili D, Tall AR. Increased CD36 protein as a response to defective insulin signaling in macrophages. J Clin Invest 113: 764-773, 2004.
35. Lynes MD, Widmaier EP. Involvement of CD36 and intestinal alkaline phosphatases in fatty acid transport in enterocytes and the response to a high-fat diet. Life Sci 88: 384-391, 2011.
36. Millán JL. Alkaline phosphatases: structure, substrate specificity and functional relatedness to other members of a large superfamily of enzymes. Purinergic Signal 2: 335-341, 2006.
37. Millán JL. Mammalian Alkaline Phosphatases. From Biology to Applications in Medicine and Biotechnology. Weinheim: Wiley VCH, 2006.
38. Nakano T, Inoue I, Koyama I, Kanazawa K, Nakamura K, Narisawa S, Tanaka K, Akita M, Masuyama T, Seo M, Hokari S, Katayama S, Alpers DH, Millán JL, Komoda T. Disruption of the murine intestinal alkaline phosphatase gene Akp3 impairs lipid transcytosis and induces visceral fat accumulation and hepatic steatosis. Am J Physiol Gastrointest Liver Physiol 292: G1439-G1449, 2007.
39. Narisawa S, Hoylaerts MF, Doctor KS, Fukuda MN, Alpers DH, Millán JL. A novel phosphatase upregulated in Akp3 knockout mice. Am J Physiol Gastrointest Liver Physiol 293: G1068-G1077, 2007.
40. Narisawa S, Huang L, Iwasaki A, Hasegawa H, Alpers DH, Millán JL. Accelerated fat absorption in intestinal alkaline phosphatase knockout mice. Mol Cell Biol 23: 7525-7530, 2003.
41. Nassir F, Wilson B, Han X, Gross RW, Abumrad NA. CD36 is important for fatty acid and cholesterol uptake by the proximal but not distal intestine. J Biol Chem 282: 19493-19501, 2007.
42. Noushmehr H, D'Amico E, Farilla L, Hui H, Wawrowsky KA, Mlynarski W, Doria A, Abumrad NA, Perfetti R. Fatty acid translocase (FAT/CD36) is localized on insulin-containing granules in human pancreatic beta-cells and mediates fatty acid effects on insulin secretion. Diabetes 54: 472-481, 2005.
43. Nozaki S, Tanaka T, Yamashita S, Sohmiya K, Yoshizumi T, Okamoto F, Kitaura Y, Kotake C, Nishida H, Nakata A, Nakagawa T, Matsumoto K, Kameda-Takemura K, Tadokoro S, Kurata Y, Tomiyama Y, Kawamura K, Matsuzawa Y. CD36 mediates long-chain fatty acid transport in human myocardium: complete myocardial accumulation defect of radiolabeled long-chain fatty acid analog in subjects with CD36 deficiency. Mol Cell Biochem 192: 129-135, 1999.
44. Ottaway CA, Parrott DM. Regional blood flow and the localization of lymphoblasts in the small intestine of the mouse. I. Examination of normal small intestine. Immunology 41: 955-961, 1980.
45. Petit V, Arnould L, Martin P, Monnot MC, Pineau T, Besnard P, Niot I. Chronic high-fat diet affects intestinal fat absorption and postprandial triglyceride levels in the mouse. J Lipid Res 48: 278-287, 2007.
46. Pohl J, Ring A, Korkmaz U, Ehehalt R, Stremmel W. FAT/CD36- mediated long-chain fatty acid uptake in adipocytes requires plasma membrane rafts. Mol Biol Cell 16: 24-31, 2005.
47. Poirier H, Degrace P, Niot I, Bernard A, Besnard P. 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, 1996.
48. Rusu D, Loret S, Peulen O, Mainil J, Dandrifosse G. Immunochemical, biomolecular and biochemical characterization of bovine epithelial intestinal primocultures. BMC Cell Biol 6: 42, 2005.
49. Salah-Uddin H, Gordon MJ, Ford I, Tandon NN, Greaves M, Duttaroy AK. Surface expression of fatty acid translocase (FAT/CD36) on platelets in myeloproliferative disorders and non-insulin dependent diabetes mellitus: effect on arachidonic acid uptake. Mol Cell Biochem 239: 203-211, 2002.
50. Sandoval A, Fraisl P, Arias-Barrau E, Dirusso CC, Singer D, Sealls W, Black PN. Fatty acid transport and activation and the expression patterns of genes involved in fatty acid trafficking. Arch Biochem Biophys 477: 363-371, 2008.
51. Tanaka T, Nakata T, Oka T, Ogawa T, Okamoto F, Kusaka Y, Sohmiya K, Shimamoto K, Itakura K. Defect in human myocardial long-chain fatty acid uptake is caused by FAT/CD36 mutations. J Lipid Res 42: 751-759, 2001.
52. Tandon NN, Kralisz U, Jamieson GA. Identification of glycoprotein IV (CD36) as a primary receptor for platelet-collagen adhesion. J Biol Chem 264: 7576-7583, 1989.
53. Tandon NN, Lipsky RH, Burgess WH, Jamieson GA. Isolation and characterization of platelet glycoprotein IV (CD36). J Biol Chem 264: 7570-7575, 1989.
54. Tao N, Wagner SJ, Lublin DM. CD36 is palmitoylated on both N- and C-terminal cytoplasmic tails. J Biol Chem 271: 22315-22320, 1996.
55. Thorne RF, Ralston KJ, de Bock CE, Mhaidat NM, Zhang XD, Boyd AW, Burns GF. Palmitoylation of CD36/FAT regulates the rate of its post-transcriptional processing in the endoplasmic reticulum. Biochim Biophys Acta 1803: 1298-1307, 2010.
56. Townsend KL, Lorenzi MM, Widmaier EP. High-fat diet-induced changes in body mass and hypothalamic gene expression in wild-type and leptin-deficient mice. Endocr J 33: 176-188, 2008.
57. Tran TT, Poirier H, Clement L, Nassir F, Pelsers MM, Petit V, Degrace P, Monnot MC, Glatz JF, Abumrad NA, Besnard P, Niot I. Luminal lipid regulates CD36 levels and downstream signaling to stimulate chylomicron synthesis. J Biol Chem 286: 25201-25210, 2011.
58. Vega MA, Segui-Real B, Garcia JA, Cales C, Rodriguez F, Vanderkerckhove J, Sandoval IV. Cloning, sequencing, and expression of a cDNA encoding rat LIMP II, a novel 74-kDa lysosomal membrane protein related to the surface adhesion protein CD36. J Biol Chem 266: 16818-16824, 1991.
59. Watanabe K, Ohta Y, Toba K, Ogawa Y, Hanawa H, Hirokawa Y, Kodama M, Tanabe N, Hirono S, Ohkura Y, Nakamura Y, Kato K, Aizawa Y, Fuse I, Miyajima S, Kusano Y, Nagamoto T, Hasegawa G, Naito M. Myocardial CD36 expression and fatty acid accumulation in patients with type I and II CD36 deficiency. Ann Nucl Med 12: 261-266, 1998.
60. Weng S, Zemany L, Standley KN, Novack DV, La Regina M, Bernal-Mizrachi C, Coleman T, Semenkovich CF. β3-Integrin deficiency promotes atherosclerosis and pulmonary inflammation in high-fat-fed, hyperlipidemic mice. Proc Natl Acad Sci USA 100: 6730-6735, 2003.
61. Wollaeger EE. Role of the ileum in fat absorption. Mayo Clin Proc 48: 836-843, 1973.