Endogenous versus exogenous fatty acid availability affects lysosomal acidity and MHC class II expression

Journal of Lipid Research

Volumn 47, Issue 11, 2006, Pages 2525-2537

  Schweitzer, S C ^a   Reding, A M ^a   Patton, H M ^a   Sullivan, T P ^a   Stubbs, C E ^a   Villalobos Menuey, E ^a   Huber, S A ^b   Newell, M K ^a  

^a UNIVERSITY OF COLORADO   (United States)

^b UNIVERSITY OF VERMONT   (United States)

Author keywords

Diet; Dyslipidemias; Inflammation; Major histocompatibility complex

Indexed keywords

CERULENIN; FATTY ACID; FATTY ACID DERIVATIVE; GAMMA INTERFERON; LIPID; LYSOSOME ENZYME; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; OLEOYL COENZYME A;

ACIDITY; ANIMAL CELL; ANTIGEN EXPRESSION; ARTICLE; CELL LINE; CELL SURFACE; CONTROLLED STUDY; ENZYME ACTIVITY; FATTY ACID SYNTHESIS; IN VITRO STUDY; IN VIVO STUDY; LYSOSOME; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; CELL MEMBRANE; FATTY ACIDS; FEMALE; GENES, MHC CLASS II; GLUCOSYLCERAMIDASE; HISTOCOMPATIBILITY ANTIGENS CLASS II; HUMANS; IMMUNE SYSTEM; INFLAMMATION; LIPIDS; LYSOSOMES; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL;

EID: 33845575810     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M600329-JLR200     Document Type: Article

References (77)

1. th edition. Elsevier, Amsterdam.
2. Brown, M. S., and J. L. Goldstein. 1986. A receptor mediated pathway for cholesterol homeostasis. Science. 232: 34-47.
3. Libby, P. 2003. Vascular biology of atherosclerosis: overview and state of the art. Am. J. Cardiol. 91: 3A-6A.
4. Hartil, K., and M. J. Charron. 2005. Genetic modification of the heart: transgenic modification of cardiac lipid and carbohydrate utilization. J. Mol. Cell. Cardiol. 39: 581-593.
5. Frayn, K., B. Fielding, and F. Karpe. 2005. Adipose tissue fatty acid metabolism and cardiovascular disease. Curr. Opin. Lipidol. 16: 409-415.
6. Raz, I., R. Eldor, S. Cernea, and E. Shafrir. 2005. Diabetes: insulin resistance and derangements in lipid metabolism. Cure through intervention in fat transport and storage. Diabetes Metab. Res. Rev. 21: 3-14.
7. Taskinen, M. 2005. Type 2 diabetes as a lipid disorder. Curr. Mol. Med. 5: 297-308.
8. Unger, R., and L. Orci. 2002. Lipoapoptosis: its mechanism and its diseases. Biochim. Biophys. Acta. 1585: 202-212.
9. Dobrzyn, A., and J. Ntambi. 2005. The role of stearoyl-CoA desaturase in the control of metabolism. Prostaglandins Leukot. Essent. Fatty Acids. 73: 35-41.
10. Degroote, S., J. Wolthoorn, and G. van Meer. 2004. The cell biology of glycosphingolipids. Cell Dev. Biol. 15: 375-387.
11. Ikonen, E., and M. Holtta-Vuori. 2004. Cellular pathology of Niemann-Pick type C disease. Cell Dev. Biol. 15: 445-454.
12. Futerman, A., and G. van Meer. 2004. The cell biology of lysosomal storage disorders. Nat. Rev. Mol. Cell Biol. 5: 554-565.
13. Shukla, S., G. Sun, W. Gibson Wood, M. Savolainen, C. Alling, and J. Hoek. 2001. Ethanol and lipid metabolic signaling. Alcohol Clin. Exp. Res. 25 (Suppl.): 33-39.
14. Nano, J., C. Nobili, F. Girard-Pipau, and P. Rampal. 2003. Effects of fatty acids on the growth of Caco-2 cells. Prostaglandins Leukot. Essent. Fatty Acids. 69: 207-215.
15. Lee, K., H. Lee, H. Cho, and Y. Kim. 2005. Role of the conjugated linoleic acid in the prevention of cancer. Crit. Rev. Food Sci. Nutr. 45: 135-144.
16. Huang, M., M. Graeler, G. Shankar, J. Spencer, and E. Goetzl. 2002. Lysophospholipid mediators of immunity and neoplasia. Biochim. Biophys. Acta. 1582: 161-167.
17. Frostegard, J., E. Svenungsson, R. Wu, I. Gunnarsson, I. Lundberg, L. Klareskog, S. Horkko, and J. Witztum. 2005. Lipid peroxidation is enhanced in patients with systemic lupus erythematosus and is associated with arterial and renal disease manifestations. Arthritis Rheum. 52: 192-200.
18. van Meeteren, M., C. Teunissen, C. Dijkstra, and E. van Tol. 2005. Antioxidants and polyunsaturated fatty acids in multiple sclerosis. Eur. J. Clin. Nutr. 59: 1347-1361.
19. Dube, M., and M. Fenton. 2003. Lipid abnormalities. Clin. Infect. Dis. 36 (Suppl. 2): 79-83.
20. Hanada, K. 2005. Sphingolipids in infectious diseases. Jpn. J. Infect. Dis. 58: 131-148.
21. Wenk, M. 2005. The emerging field of lipidomics. Nat. Rev. Drug Discov. 4: 594-610.
22. Huber, S., J. Kupperman, and M. Newell. 1999. Hormonal regulation of CD4(+) T-cell responses in coxsackievirus B-3-induced myocarditis in mice. J. Virol. 73: 4689-4695.
23. Yndestad, A., A. Holm, F. Muller, S. Simonsen, S. Froland, L. Gullestad, and P. Aukrust. 2003. Enhanced expression of inflammatory cytokines and activation markers in T-cells from patients with chronic heart failure. Cardiovasc. Res. 60: 141-146.
24. Lord, R., and Y. Bobryshev. 2002. Hallmarks of atherosclerotic lesion development with special reference to immune inflammatory mechanisms. Cardiovasc. Surg. 10: 405-414.
25. Stocker, R., and J. J. Keaney. 2004. Role of oxidative modifications in atherosclerosis. Physiol. Rev. 84: 1381-1478.
26. th edition. W. H. Freeman and Co., New York.
27. Cresswell, P., and A. Lanzavecchia. 2001. Antigen processing and recognition. Curr. Opin. Immunol. 13: 11-12.
28. Li, P., J. Gregg, N. Wang, D. Zhou, P. O'Donnell, J. Blum, and Y. Crotzer. 2005. Compartmentalization of class II antigen presentation: contributions of cytoplasmic and endosomal processing. Immunol. Rev. 207: 206-217.
29. Bretscher, P. 1975. The two signal model for B cell induction. Transplant. Rev. 23: 37-48.
30. Bretscher, P., and M. Cohn. 1970. The theory of self-nonself discrimination. Science. 169: 1042-1049.
31. Elenkov, I., D. Iezzoni, A. Daly, A. Harris, and G. Chrousos. 2005. Cytokine dysregulation, inflammation, and well-being. Neuroimmunomodulation. 12: 255-269.
32. Minor, L., F. Mahlberg, W. Jerome, J. Lewis, G. Rothblatt, and J. Glick. 1991. Lysosomal hydrolysis of lipids in a cell culture model of smooth muscle foam cells. Exp. Mol. Pathol. 54: 159-171.
33. Mouritsen, S., A. Hansen, B. Petersen, and S. Buus. 1992. pH dependence of the interaction between immunogenic peptides and MHC class II molecules. Evidence for an acidic intracellular compartment being the organelle of interaction. J. Immunol. 148: 1438-1444.
34. th edition. Molecular Probes, Eugene, OR.
35. van Es, H., M. Veldwijk, M. Havenga, and D. Valerio. 1997. A flow cytometric assay for lysosomal glucocerebrosidase. Anal. Biochem. 247: 268-271.
36. Leanderson, T., and M. Julius. 1986. Mouse B cells do not proliferate in human interleukin 2. Eur. J. Immunol. 16: 182-187.
37. Sharma, S., T. Budzich, M. Proffitt, D. Shepherd, and J. Remington. 1984. Regulation of natural killer cell activity by anti-I-region monoclonal antibodies. Cell. Immunol. 85: 125-134.
38. Groener, J., W. Bax, and B. Poorthuis. 1996. Metabolic fate of oleic acid derived from lysosomal degradation of cholesteryl oleate in human fibroblasts. J. Lipid Res. 37: 2271-2279.
39. Chow, A., and I. Mellman. 2005. Old lysosomes, new tricks: MHC II dynamics in DCs. Trends Immunol. 26: 72-78.
40. Collins, S., R. Gallo, and R. Gallagher. 1977. Continuous growth and differentiation of human myeloid leukemic cells in suspension culture. Nature. 270: 347-349.
41. Koren, H., S. Anderson, and J. Larrick. 1979. In vitro activation of a human macrophage-like cell line. Nature. 279: 328-331.
42. Hutchison, D., O. Ittensohn, and M. Bjerregaard. 1966. Growth of L1210 mouse leukemia cells in vitro. Exp. Cell Res. 42: 157-170.
43. Stemmel, W., L. Pohl, A. Ring, and T. Hermann. 2001. A new concept of cellular uptake and intracellular trafficking of long-chain fatty acids. Lipids. 36: 981-989.
44. Poole, B., and S. Ohkuma. 1981. Effect of weak bases on the intralysosomal pH in mouse peritoneal macrophages. J. Cell Biol. 90: 665-669.
45. Aukurst, P., L. Gulliestad, T. Ueland, J. Damas, and A. Yndestad. 2005. Inflammatory and anti-inflammatory cytokines in chronic heart failure: potential therapeutic implications. Ann. Med. 37: 74-85.
46. Nakagawa, T., and A. Rudensky. 1999. The role of lysosomal proteinases in MHC class II-mediated antigen processing and presentation. Immunol. Rev. 172: 121-129.
47. Kloetzel, P. 2004. The proteasome and MHC class I antigen processing. Biochim. Biophys. Acta. 1695: 217-225.
48. Lehner, P., and P. Cresswell. 2004. Recent developments in MHC-class-I-mediated antigenpresentation. Curr. Opin. Immunol. 16: 82-89.
49. Drayson, M., R. Mitchell, J. Durham, and G. Brown. 2001. Cell proliferation and CD11b expression are controlled independently during HL60 cell differentiation initiated by 1,25 alpha-dihydroxyvitamin D3 or all-trans-retinoic acid. Exp. Cell Res. 226: 126-134.
50. Delvig, A., J. Lee, Z. Chrzanowska-Lightowlers, and J. Robinson. 2002. TGF-beta and IFN-gamma cross regulate antigen presentation to CD4 T cells by macrophages. J. Leukoc. Biol. 72: 163-166.
51. Anderson, H., E. Hitbold, and P. Roche. 2000. Concentration of MHC class II molecules in lipid rafts facilitates antigen presentation. Nat. Immunol. 1: 156-162.
52. Goebel, J., K. Forrest, D. Flynn, R. Rao, and T. Roszman. 2002. Lipid rafts, major histocompatibility complex molecules and immune regulation. Hum. Immunol. 63: 813-820.
53. Hiltbold, E., N. Poloso, and P. Roche. 2003. MHC class II-peptide complexes and APC lipid rafts accumulate at the immunological synapse. J. Immunol. 170: 1329-1336.
54. Poloso, N., A. Muntasell, and P. Roche. 2004. MHC class II molecules traffic into lipid rafts during intracellular transport. J. Immunol. 173: 4539-4546.
55. D'Agnolo, G., I. Rosenfeld, J. Awaya, S. Omura, and P. Vagelos. 1973. Inhibition of fatty acid synthesis by the antibiotic cerulenin. Specific inactivation of beta-ketoacyl-acyl carrier protein synthase. Biochim. Biophys. Acta. 326: 155-156.
56. Kuhajda, F., E. Pizer, J. Li, N. Mani, G. Frehywot, and C. Townsend. 2000. Synthesis and antitumor activity of an inhibitor of fatty acid synthesis. Proc. Natl. Acad. Sci. USA. 97: 3450-3454.
57. Pizer, E., F. Wood, G. Pasternack, and F. Kuhajda. 1996. Fatty acid synthase (FAS): a target for cytotoxic antimetabolites in HL60 promyelocytic leukemia cells. Cancer Res. 56: 745-751.
58. Pizer, E., F. Chrest, J. DiGiuseppe, and W. Han. 1998. Pharmacological inhibitors of mammalian fatty acid synthase suppress DNA replication and induce apoptosis in tumor cell lines. Cancer Res. 58: 4611-4615.
59. Zhang, Y., C. Guo, and G. Yu. 2005. A pilot study of fatty acid metabolism in oral squamous cell carcinoma. Int. J. Oral Maxillofac. Surg. 34: 78-81.
60. Liu, X., Y. Shi, V. Giranda, and Y. Luo. 2006. Inhibition of the phosphatidylinositol 3-kinase/Akt pathway sensitizes MDA-MB468 human breast cancer cells to cerulenin-induced apoptosis. Mol. Cancer Ther. 5: 494-501.
61. Trombetta, E., M. Ebersold, W. Garrett, M. Pypaert, and I. Mellman. 2003. Activation of lysosomal function during dendritic cell maturation. Science. 299: 1400-1403.
62. Ma, D., J. Seo, K. Switzer, Y. Fan, D. McMurray, J. Lupton, and R. Chapkin. 2004. n-3 PUFA and membrane microdomains: a new frontier in bioactive lipid research. J. Nutr. Biochem. 15: 700-706.
63. Zeyda, M., G. Staffler, V. Horejsi, W. Waldhausl, and T. Stulnig. 2002. LAT displacement from lipid rafts as a molecular mechanism for the inhibition of T cell signaling by polyunsaturated fatty acids. J. Biol. Chem. 277: 28418-28423.
64. Pohl, J., A. Ring, R. Ehehalt, H. Schulze-Bergkamen, A. Schad, P. Verkade, and W. Stemmel. 2004. Long-chain fatty acid uptake into adipocytes depends on lipid raft function. Biochemistry. 43: 4179-4187.
65. van Laethem, F., X. Liang, F. Andris, J. Urbain, M. Vandenbranden, J. Ruysschaert, M. Resh, T. Stulnig, and O. Leo. 2003. Glucocorticoids alter the lipid and protein composition of membrane rafts of a murine T cell hybridoma. J. Immunol. 170: 2932-2939.
66. Fan, Y., L. Ly, R. Barhoumi, D. McMurray, and R. Chapkin. 2004. Dietary docosahexaenoic acid suppresses T cell protein kinase C theta lipid raft recruitment and IL-2 production. J. Immunol. 173: 6151-6160.
67. Fan, Y., D. McMurray, L. Ly, and R. Chapkin. 2003. Dietary (n-3) polyunsaturated fatty acids remodel mouse T-cell lipid rafts. J. Nutr. 133: 1913-1920.
68. Athanassakis, I., A. Ranella, and S. Vassiliadis. 2000. IFN-gamma facilitates release of class-II loaded intracellular pools in trophoblast cells: a novel property independent of protein synthesis. J. Interferon Cytokine Res. 20: 823-830.
69. Huss, R., C. Beckham, R. Storb, and H. Deeg. 1994. Major histocompatibility complex class II expression is required for post-transplant immunological but not hemopoietic reconstitution in mice. Transplantation. 58: 1366-1371.
70. Huber, S., J. Stone, D. J. Wagner, J. Kupperman, L. Pfeiffer, C. David, R. O'Brien, G. Davis, and M. Newell. 1999. Gamma delta+ T cells regulate major histocompatibility complex class II (IA and IE)-dependent susceptibility to coxsackievirus B3-induced autoimmune myocarditis. J. Virol. 73: 5630-5636.
71. Akdemir, R., H. Ozhan, H. Gunduz, E. Erbilen, M. Yazici, S. Duran, F. Orkunoglu, S. Albayrak, N. Imirzalioglu, and C. Uyan. 2004. HLA-DR B1 and DQ B1 polymorphisms in patients with coronary artery ectasia. Acta Cardiol. 59: 499-502.
72. Thorsby, E., and B. Lie. 2005. HLA associated genetic predisposition to autoimmune diseases: genes involved and possible mechanisms. Transpl. Immunol. 14: 175-182.
73. Segal, S., and A. Hill. 2003. Genetic susceptibility to infectious disease. Trends Microbiol. 11: 445-448.
74. Howell, W., P. Calder, and R. Grimble. 2002. Gene polymorphisms, inflammatory diseases and cancer. Proc. Nutr. Soc. 61: 447-456.
75. Holmes, S., C. Siebold, E. Jones, M. Friese, L. Fugger, and J. Bell. 2005. Multiple sclerosis: MHC associations and therapeutic implications. Expert Rev. Mol. Med. 7: 1-17.
76. Rozzo, S., T. Vyse, C. David, E. Palmer, S. Izui, and B. Kotzin. 1999. Analysis of MHC class II genes in the susceptibility to lupus in New Zealand mice. J. Immunol. 162: 2623-2630.
77. Weyand, C., and J. Goronzy. 2000. Association of MHC and rheumatoid arthritis. HLA polymorphisms in phenotypic variants of rheumatoid arthritis. Arthritis Res. 2: 203-204.