Altered expression of genes functioning in lipid homeostasis is associated with lipid deposition in NOD mouse lacrimal gland

Experimental Eye Research

Volumn 89, Issue 3, 2009, Pages 319-332

  Wu, Kaijin ^a   Joffre, Corrine ^b   Li, Xiaodong ^a   MacVeigh Aloni, Michelle ^a   Hom, Melinda ^a   Hwang, Juliana ^a   Ding, Chuanqing ^a   Gregoire, Stephane ^b   Bretillon, Lionel ^b   Zhong, Jiang F ^a   Hamm Alvarez, Sarah F ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b CEMAGREF   (France)

Author keywords

apolipoprotein E; apolipoprotein F; lacrimal gland; lipid; microarray; NOD mouse; Sj gren's syndrome

Indexed keywords

ABC TRANSPORTER; ABC TRANSPORTER D1; ABC TRANSPORTER G1; ACYLGLYCEROL LIPASE; APOLIPOPROTEIN; APOLIPOPROTEIN E; APOLIPOPROTEIN F; CHOLESTEROL ESTER; LIPID; LIVER TRIACYLGLYCEROL LIPASE; MESSENGER RNA; PHOSPHOMEVALONATE KINASE; UNCLASSIFIED DRUG;

ACINAR CELL; AGE DISTRIBUTION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BAGG ALBINO MOUSE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DACRYOADENITIS; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE FUNCTION; HOMEOSTASIS; LACRIMAL GLAND; LACRIMAL GLAND DISEASE; LIPID METABOLISM; LIPID STORAGE; LIPID TRANSPORT; LIVER; LYMPHOCYTIC INFILTRATION; MALE; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; NONOBESE DIABETIC MOUSE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCID MOUSE; SEX DIFFERENCE; SJOEGREN SYNDROME; STRAIN DIFFERENCE; UPREGULATION;

AGING; ANIMALS; APOLIPOPROTEINS; APOLIPOPROTEINS E; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HOMEOSTASIS; HUMANS; LACRIMAL APPARATUS; LIPID METABOLISM; LYMPHOCYTES; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED NOD; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SJOGREN'S SYNDROME; SPECIES SPECIFICITY;

EID: 67651214085     PISSN: 00144835     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.exer.2009.03.020     Document Type: Article

References (68)

1. Ackman R.G. Flame ionization detection applied to thin-layer chromatography on coated quartz rods. Methods Enzymol. 72 (1981) 205-252
2. Baldan A., Tarr P., Vales C.S., Frank J., Shimotake T.K., Hawgood S., and Edwards P.A. Deletion of the transmembrane transporter ABCG1 results in progressive pulmonary lipidosis. J. Biol. Chem. 281 (2006) 29401-29410
3. Basu S.K., Goldstein J.L., and Brown M.S. Independent pathways for secretion of cholesterol and apolipoprotein E by macrophages. Science 219 (1983) 871-873
4. Bellosta S., Mahley R.W., Sanan D.A., Murata J., Newland D.L., Taylor J.M., and Pitas R.E. Macrophage-specific expression of human apolipoprotein E reduces atherosclerosis in hypercholesterolemic apolipoprotein E-null mice. J. Clin. Invest. 96 (1995) 2170-2179
5. Brooks-Wilson A., Marcil M., Clee S.M., Zhang L.H., Roomp K., Van Dam M., Yu L., Brewer C., Collins J.A., Molhuizen H.O., Loubser O., Ouelette B.F., Fichter K., Ashbourne-Excoffon K.J., Sensen C.W., Scherer S., Mott S., Denis M., Martindale D., Frohlich J., Morgan K., Koop B., Pimstone S., Kastelein J.J., Genest Jr. J., and Hayden M.R. Mutations in ABC1 in Tangier disease and familial high-density lipoprotein deficiency. Nat. Genet. 22 (1999) 336-345
6. Cartier N., Sarde C.O., Douar A.M., Mosser J., Mandel J.L., and Aubourg P. Abnormal messenger RNA expression and a missense mutation in patients with X-linked adrenoleukodystrophy. Hum. Mol. Genet. 2 (1993) 1949-1951
7. Cha S., Nagashima H., Brown V.B., Peck A.B., and Humphreys-Beher M.G. Two NOD Idd-associated intervals contribute synergistically to the development of autoimmune exocrinopathy (Sjogren's syndrome) on a healthy murine background. Arthritis Rheum. 46 (2002) 1390-1398
8. Day J.R., Albers J.J., Gilbert T.L., Whitmore T.E., Mcconathy W.J., and Wolfbauer G. Purification and molecular cloning of human apolipoprotein F. Biochem. Biophys. Res. Commun. 203 (1994) 1146-1151
9. Ding C., Macveigh M., Pidgeon M., Da Costa S.R., Wu K., Hamm-Alvarez S.F., and Schechter J.E. Unique ultrastructure of exorbital lacrimal glands in male NOD and BALB/c mice. Curr. Eye Res. 31 (2006) 13-22
10. Dory L. Synthesis and secretion of apoE in thioglycolate-elicited mouse peritoneal macrophages: effect of cholesterol efflux. J. Lipid Res. 30 (1989) 809-816
11. Dykstra M., Cherukuri A., Sohn H.W., Tzeng S.J., and Pierce S.K. Location is everything: lipid rafts and immune cell signaling. Annu. Rev. Immunol. 21 (2003) 457-481
12. Folch J., Lees M., and Sloane Stanley G.H. A simple method for the isolation and purification of total lipides from animal tissues. J. Biol. Chem. 226 (1957) 497-509
13. Fox R.I. Sjogren's syndrome: current therapies remain inadequate for a common disease. Expert Opin. Investig. Drugs 9 (2000) 2007-2016
14. Fox P.C. Autoimmune diseases and Sjogren's syndrome: an autoimmune exocrinopathy. Ann. N Y Acad. Sci. 1098 (2007) 15-21
15. Franklin R.M., Kenyon K.R., and Tomasi T.B.J. Immunohistologic studies of human lacrimal gland: localization of immunoglobulins, secretory component and Lactoferrin. J. Immunol. 110 (1973) 984-992
16. Gasymov O.K., Abduragimov A.R., Prasher P., Yusifov T.N., and Glasgow B.J. Tear lipocalin: evidence for a scavenging function to remove lipids from the human corneal surface. Invest Ophthalmol. Vis. Sci. 46 (2005) 3589-3596
17. Genain C.P., Cannella B., Hauser S.L., and Raine C.S. Identification of autoantibodies associated with myelin damage in multiple sclerosis. Nat. Med. 5 (1999) 170-175
18. Ghiselli G., Schaefer E.J., Gascon P., and Breser Jr. H.B. Type III hyperlipoproteinemia associated with apolipoprotein E deficiency. Science 214 (1981) 1239-1241
19. Hansson G.K. Inflammation and immune response in atherosclerosis. Curr. Atheroscler. Rep. 1 (1999) 150-155
20. Huang Z.H., Fitzgerald M.L., and Mazzone T. Distinct cellular loci for the ABCA1-dependent and ABCA1-independent lipid efflux mediated by endogenous apolipoprotein E expression. Arterioscler Thromb. Vasc. Biol. 26 (2006) 157-162
21. Hunger R.E., Carnaud C., Vogt I., and Mueller C. Male gonadal environment paradoxically promotes dacryoadenitis in nonobese diabetic mice. J. Clin. Invest. 101 (1998) 1300-1309
22. Ilyas A.A., Chen Z.W., and Cook S.D. Antibodies to sulfatide in cerebrospinal fluid of patients with multiple sclerosis. J. Neuroimmunol 139 (2003) 76-80
23. Izumi M., Eguchi K., Nakamura H., Nagataki S., and Nakamura T. Premature fat deposition in the salivary glands associated with Sjogren syndrome: MR and CT evidence. AJNR Am. J. Neuroradiol 18 (1997) 951-958
24. Izumi M., Eguchi K., Uetani M., Nakamura H., Takagi Y., Hayashi K., and Nakamura T. MR features of the lacrimal gland in Sjogren's syndrome. AJR Am. J. Roentgenol 170 (1998) 1661-1666
25. Jonsson R., Haga H.J., and Gordon T.P. Current concepts on diagnosis, autoantibodies and therapy in Sjogren's syndrome. Scand. J. Rheumatol. 29 (2000) 341-348
26. Kanter J.L., Narayana S., Ho P.P., Catz I., Warren K.G., Sobel R.A., Steinman L., and Robinson W.H. Lipid microarrays identify key mediators of autoimmune brain inflammation. Nat. Med. 12 (2006) 138-143
27. Kelly M.E., Clay M.A., Mistry M.J., Hsieh-Li H.M., and Harmony J.A. Apolipoprotein E inhibition of proliferation of mitogen-activated T lymphocytes: production of interleukin 2 with reduced biological activity. Cell Immunol. 159 (1994) 124-139
28. Kennedy M.A., Barrera G.C., Nakamura K., Baldan A., Tarr P., Fishbein M.C., Frank J., Francone O.L., and Edwards P.A. ABCG1 has a critical role in mediating cholesterol efflux to HDL and preventing cellular lipid accumulation. Cell Metab. 1 (2005) 121-131
29. Klenkler B., Sheardown H., and Jones L. Growth factors in the tear film: role in tissue maintenance, wound healing, and ocular pathology. Ocul. Surf 5 (2007) 228-239
30. Kohn L.D., Wallace B., Schwartz F., and Mccall K. Is type 2 diabetes an autoimmune-inflammatory disorder of the innate immune system?. Endocrinology 146 (2005) 4189-4191
31. Koren E., Mcconathy W.J., and Alaupovic P. Isolation and characterization of simple and complex lipoproteins containing apolipoprotein F from human plasma. Biochemistry 21 (1982) 5347-5351
32. Kurosaka D., Teramoto T., Matsushima T., Yokoyama T., Yamada A., Aikawa T., Miyamoto Y., and Kurokawa K. Apolipoprotein E deficiency with a depressed mRNA of normal size. Atherosclerosis 88 (1991) 15-20
33. Linton M.F., Atkinson J.B., and Fazio S. Prevention of atherosclerosis in apolipoprotein E-deficient mice by bone marrow transplantation. Science 267 (1995) 1034-1037
34. Lodde B.M., Sankar V., Kok M.R., Leakan R.A., Tak P.P., and Pillemer S.R. Serum lipid levels in Sjogren's syndrome. Rheumatology (Oxford) 45 (2006) 481-484
35. Mabuchi H., Itoh H., Takeda M., Kajinami K., Wakasugi T., Koizumi J., Takeda R., and Asagami C. A young type III hyperlipoproteinemic patient associated with apolipoprotein E deficiency. Metabolism 38 (1989) 115-119
36. Mazzanti B., Vergelli M., Riccio P., Martin R., Mcfarland H.F., Liuzzi G.M., Amaducci L., and Massacesi L. T-cell response to myelin basic protein and lipid-bound myelin basic protein in patients with multiple sclerosis and healthy donors. J. Neuroimmunol 82 (1998) 96-100
37. Mazzone T., and Reardon C. Expression of heterologous human apolipoprotein E by J774 macrophages enhances cholesterol efflux to HDL3. J. Lipid Res. 35 (1994) 1345-1353
38. Mistry M.J., Clay M.A., Kelly M.E., Steiner M.A., and Harmony J.A. Apolipoprotein E restricts interleukin-dependent T lymphocyte proliferation at the G1A/G1B boundary. Cell Immunol. 160 (1995) 14-23
39. Morton R.E., Gnizak H.M., Greene D.J., Cho K.H., and Paromov V.M. Lipid transfer inhibitor protein (apolipoprotein F) concentration in normolipidemic and hyperlipidemic subjects. J. Lipid Res. 49 (2008) 127-135
40. Nguyen K.H., Brayer J., Cha S., Diggs S., Yasunari U., Hilal G., Peck A.B., and Humphreys-Beher M.G. Evidence for antimuscarinic acetylcholine receptor antibody-mediated secretory dysfunction in nod mice. Arthritis Rheum. 43 (2000) 2297-2306
41. Nguyen C., Singson E., Kim J.Y., Cornelius J.G., Attia R., Doyle M.E., Bulosan M., Cha S., and Peck A.B. Sjogren's syndrome-like disease of C57BL/6.NOD-Aec1 Aec2 mice: gender differences in keratoconjunctivitis sicca defined by a cross-over in the chromosome 3 Aec1 locus. Scand. J. Immunol. 64 (2006) 295-307
42. Nishide T., Tollefson J.H., and Albers J.J. Inhibition of lipid transfer by a unique high density lipoprotein subclass containing an inhibitor protein. J. Lipid Res. 30 (1989) 149-158
43. Olofsson S.O., Mcconathy W.J., and Alaupovic P. Isolation and partial characterization of a new acidic apolipoprotein (apolipoprotein F) from high density lipoproteins of human plasma. Biochemistry 17 (1978) 1032-1036
44. Oram J.F. Tangier disease and ABCA1. Biochim Biophys. Acta 1529 (2000) 321-330
45. Palinski W., Tangirala R.K., Miller E., Young S.G., and Witztum J.L. Increased autoantibody titers against epitopes of oxidized LDL in LDL receptor-deficient mice with increased atherosclerosis. Arterioscler Thromb. Vasc. Biol. 15 (1995) 1569-1576
46. Palinski W., Horkko S., Miller E., Steinbrecher U.P., Powell H.C., Curtiss L.K., and Witztum J.L. Cloning of monoclonal autoantibodies to epitopes of oxidized lipoproteins from apolipoprotein E-deficient mice. Demonstration of epitopes of oxidized low density lipoprotein in human plasma. J. Clin. Invest 98 (1996) 800-814
47. Pender M.P., Csurhes P.A., Wolfe N.P., Hooper K.D., Good M.F., Mccombe P.A., and Greer J.M. Increased circulating T cell reactivity to GM3 and GQ1b gangliosides in primary progressive multiple sclerosis. J. Clin. Neurosci. 10 (2003) 63-66
48. Plump A.S., Smith J.D., Hayek T., Aalto-Setala K., Walsh A., Verstuyft J.G., Rubin E.M., and Breslow J.L. Severe hypercholesterolemia and atherosclerosis in apolipoprotein E-deficient mice created by homologous recombination in ES cells. Cell 71 (1992) 343-353
49. Redl B. Human tear lipocalin. Biochim Biophys. Acta 1482 (2000) 241-248
50. Ressot C., Lassagne H., Kemeny J.L., and Gachon A.M. Tissue expression of tear lipocalin in humans. Adv. Exp. Med. Biol. 438 (1998) 69-73
51. Robinson C.P., Yamamoto H., Peck A.B., and Humphreys-Beher M.G. Genetically programmed development of salivary gland abnormalities in the NOD (nonobese diabetic)-scid mouse in the absence of detectable lymphocytic infiltration: a potential trigger for sialoadenitis of NOD mice. Clin. Immunol. Immunopathol 79 (1996) 50-59
52. Robinson C.P., Yamachika S., Alford C.E., Cooper C., Pichardo E.L., Shah N., Peck A.B., and Humphreys-Beher M.G. Elevated levels of cysteine protease activity in saliva and salivary glands of the nonobese diabetic (NOD) mouse model for Sjogren syndrome. Proc. Natl. Acad. Sci. U S A 94 (1997) 5767-5771
53. Roselaar S.E., and Daugherty A. Apolipoprotein E-deficient mice have impaired innate immune responses to Listeria monocytogenes in vivo. J. Lipid Res. 39 (1998) 1740-1743
54. Sadatipour B.T., Greer J.M., and Pender M.P. Increased circulating antiganglioside antibodies in primary and secondary progressive multiple sclerosis. Ann. Neurol. 44 (1998) 980-983
55. Sébédio J., and Juaneda P. Quantitative lipid analyses using the new Iatroscan TLC-FID system. J. Planar Chrom. 4 (1991) 35-41
56. Shamshiev A., Donda A., Carena I., Mori L., Kappos L., and De Libero G. Self glycolipids as T-cell autoantigens. Eur. J. Immunol. 29 (1999) 1667-1675
57. Shaw P.X., Horkko S., Tsimikas S., Chang M.K., Palinski W., Silverman G.J., Chen P.P., and Witztum J.L. Human-derived anti-oxidized LDL autoantibody blocks uptake of oxidized LDL by macrophages and localizes to atherosclerotic lesions in vivo. Arterioscler Thromb. Vasc. Biol. 21 (2001) 1333-1339
58. Sullivan D.A., and Allansmith M.R. Source of IgA in tears of rats. Immunology 53 (1984) 791-799
59. Thiagarajan P. Atherosclerosis, autoimmunity, and systemic lupus erythematosus. Circulation 104 (2001) 1876-1877
60. Uhlig H., and Dernick R. Monoclonal autoantibodies derived from multiple sclerosis patients and control persons and their reactivities with antigens of the central nervous system. Autoimmunity 5 (1989) 87-99
61. Vaisar T., Pennathur S., Green P.S., Gharib S.A., Hoofnagle A.N., Cheung M.C., Byun J., Vuletic S., Kassim S., Singh P., Chea H., Knopp R.H., Brunzell J., Geary R., Chait A., Zhao X.Q., Elkon K., Marcovina S., Ridker P., Oram J.F., and Heinecke J.W. Shotgun proteomics implicates protease inhibition and complement activation in the antiinflammatory properties of HDL. J. Clin. Invest 117 (2007) 746-756
62. Van Blokland S.C., and Versnel M.A. Pathogenesis of Sjogren's syndrome: characteristics of different mouse models for autoimmune exocrinopathy. Clin. Immunol. 103 (2002) 111-124
63. Van Haeringen N.J. Clinical biochemistry of tears. Surv. Ophthalmol. 26 (1981) 84-96
64. Wang X., Driscoll D.M., and Morton R.E. Molecular cloning and expression of lipid transfer inhibitor protein reveals its identity with apolipoprotein F. J. Biol. Chem. 274 (1999) 1814-1820
65. Wang Y., Lam K.S., Kraegen E.W., Sweeney G., Zhang J., Tso A.W., Chow W.S., Wat N.M., Xu J.Y., Hoo R.L., and Xu A. Lipocalin-2 is an inflammatory marker closely associated with obesity, insulin resistance, and hyperglycemia in humans. Clin. Chem. 53 (2007) 34-41
66. Young S.G., and Fielding C.J. The ABCs of cholesterol efflux. Nat. Genet 22 (1999) 316-318
67. Zhang S.H., Reddick R.L., Piedrahita J.A., and Maeda N. Spontaneous hypercholesterolemia and arterial lesions in mice lacking apolipoprotein E. Science 258 (1992) 468-471
68. Zoukhri D. Effect of inflammation on lacrimal gland function. Exp. Eye Res. 82 (2006) 885-898