Deficiency of lymphotoxin-a does not exacerbate high-fat diet-induced obesity but does enhance inflammation in mice

American Journal of Physiology - Endocrinology and Metabolism

Volumn 302, Issue 8, 2012, Pages

  Pamir, Nathalie ^a   McMillen, Timothy S ^a   Edgel, Kimberly A ^a   Kim, Francis ^a   Leboeuf, Renée C ^a  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

Cytokines; Diabetes; Lymphocytes; Macrophages

Indexed keywords

ADIPOCYTOKINE; LYMPHOTOXIN; CYTOKINE; MESSENGER RNA;

ABDOMINAL FAT; ADIPOSE TISSUE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY COMPOSITION; BODY WEIGHT; CELL DIFFERENTIATION; CELL INFILTRATION; CELL MATURATION; CELL SPECIFICITY; CONTROLLED STUDY; FOOD INTAKE; GENE EXPRESSION; GLUCOSE METABOLISM; GLUCOSE TOLERANCE; INFLAMMATION; INSULIN RESISTANCE; LIPID DIET; LYMPHOCYTE; MACROPHAGE; MALE; MOUSE; NONHUMAN; OBESITY; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; WILD TYPE; ANIMAL; BLOOD; CELL LINE; GENE EXPRESSION REGULATION; GENETICS; GLUCOSE INTOLERANCE; IMMUNOLOGY; METABOLISM; MOUSE MUTANT; RANDOMIZATION; SUGAR INTAKE; WEIGHT GAIN; WHITE ADIPOSE TISSUE;

ADIPOKINES; ADIPOSE TISSUE, WHITE; ADIPOSITY; ANIMALS; CELL LINE; CYTOKINES; DIET, HIGH-FAT; DIETARY SUCROSE; GENE EXPRESSION; GENE EXPRESSION REGULATION; GLUCOSE INTOLERANCE; INSULIN RESISTANCE; LYMPHOTOXIN-ALPHA; MACROPHAGES; MALE; MICE; MICE, KNOCKOUT; OBESITY; RANDOM ALLOCATION; RNA, MESSENGER; T-LYMPHOCYTES; WEIGHT GAIN;

EID: 84859463300     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00447.2011     Document Type: Article

References (86)

1. Aggarwal BB, Eessalu TE, Hass PE. Characterization of receptors for human tumour necrosis factor and their regulation by gamma-interferon. Nature 318: 665-667, 1985.
2. Azagury DE, Lautz DB. Obesity overview: epidemiology, health and financial impact, and guidelines for qualification for surgical therapy. Gastrointest Endosc Clin N Am 21: 189-201, 2011.
3. Banim PJ, Luben RN, Bulluck H, Sharp SJ, Wareham NJ, Khaw KT, Hart AR. The aetiology of symptomatic gallstones quantification of the effects of obesity, alcohol and serum lipids on risk. Epidemiological and biomarker data from a UK prospective cohort study (EPIC-Norfolk). Eur J Gastroenterol Hepatol 23: 733-740, 2011.
4. Black BL, Croom J, Eisen EJ, Petro AE, Edwards CL, Surwit RS. Differential effects of fat and sucrose on body composition in A/J and C57BL/6 mice. Metabolism 47: 1354-1359, 1998.
5. Bouloumie A, Casteilla L, Lafontan M. Adipose tissue lymphocytes and macrophages in obesity and insulin resistance: makers or markers, and which comes first? Arterioscler Thromb Vasc Biol 28: 1211-1213, 2008.
6. Brunkow ME, Jeffery EW, Hjerrild KA, Paeper B, Clark LB, Yasayko SA, Wilkinson JE, Galas D, Ziegler SF, Ramsdell F. Disruption of a new forkhead/winged-helix protein, scurfin, results in the fatal lymphoproliferative disorder of the scurfy mouse. Nat Genet 27: 68-73, 2001.
7. Chaturvedi MM, LaPushin R, Aggarwal BB. Tumor necrosis factor and lymphotoxin. Qualitative and quantitative differences in the mediation of early and late cellular response. J Biol Chem 269: 14575-14583, 1994.
8. Chida D, Osaka T, Hashimoto O, Iwakura Y. Combined interleukin-6 and interleukin-1 deficiency causes obesity in young mice. Diabetes 55: 971-977, 2006.
9. Choi SJ, Kim F, Schwartz MW, Wisse BE. Cultured hypothalamic neurons are resistant to inflammation and insulin resistance induced by saturated fatty acids. Am J Physiol Endocrinol Metab 298: E1122-E1130, 2010.
10. Cyster JG. Lymphoid organ development and cell migration. Immunol Rev 195: 5-14, 2003.
11. De Togni P, Goellner J, Ruddle NH, Streeter PR, Fick A, Mariathasan S, Smith SC, Carlson R, Shornick LP, Strauss-Schoenberger J, Russell JH, Karr R, Chaplin DD. Abnormal development of peripheral lymphoid organs in mice deficient in lymphotoxin. Science 264: 703-707, 1994.
12. Elewaut D, Ware CF. The unconventional role of LT alpha beta in T cell differentiation. Trends Immunol 28: 169-175, 2007.
13. Fain JN. Release of inflammatory mediators by human adipose tissue is enhanced in obesity and primarily by the nonfat cells: a review. Mediators Inflamm 2010: 513948, 2010.
14. Feuerer M, Herrero L, Cipolletta D, Naaz A, Wong J, Nayer A, Lee J, Goldfine AB, Benoist C, Shoelson S, Mathis D. Lean, but not obese, fat is enriched for a unique population of regulatory T cells that affect metabolic parameters. Nat Med 15: 930-939, 2009.
15. Frederich RC, Hamann A, Anderson S, Lollmann B, Lowell BB, Flier JS. Leptin levels reflect body lipid content in mice: evidence for diet-induced resistance to leptin action. Nat Med 1: 1311-1314, 1995.
16. Garcia MC, Wernstedt I, Berndtsson A, Enge M, Bell M, Hultgren O, Horn M, Ahren B, Enerback S, Ohlsson C, Wallenius V, Jansson JO. Mature-onset obesity in interleukin-1 receptor I knockout mice. Diabetes 55: 1205-1213, 2006.
17. Gordon S. Alternative activation of macrophages. Nat Rev Immunol 3: 23-35, 2003.
18. Govers C, Sebestyen Z, Coccoris M, Willemsen RA, Debets R. T cell receptor gene therapy: strategies for optimizing transgenic TCR pairing. Trends Mol Med 16: 77-87, 2010.
19. Grundy SM. Metabolic complications of obesity. Endocrine 13: 155-165, 2000.
20. Harrington LE, Mangan PR, Weaver CT. Expanding the effector CD4 T-cell repertoire: the Th17 lineage. Curr Opin Immunol 18: 349-356, 2006.
21. Hayakawa T, Nagai Y, Taniguchi M, Yamashita H, Takamura T, Abe T, Nomura G, Kobayashi K. Tumor necrosis factor-beta gene NcoI polymorphism decreases insulin resistance in Japanese men. Metabolism 49: 1506-1509, 2000.
22. Hotamisligil GS. Inflammation and metabolic disorders. Nature 444: 860-867, 2006.
23. Hotamisligil GS, Shargill NS, Spiegelman BM. Adipose expression of tumor necrosis factor-alpha: direct role in obesity-linked insulin resistance. Science 259: 87-91, 1993.
24. Ivanov II, McKenzie BS, Zhou L, Tadokoro CE, Lepelley A, Lafaille JJ, Cua DJ, Littman DR. The orphan nuclear receptor RORgammat directs the differentiation program of proinflammatory IL-17+ T helper cells. Cell 126: 1121-1133, 2006.
25. Kanda H, Tateya S, Tamori Y, Kotani K, Hiasa K, Kitazawa R, Kitazawa S, Miyachi H, Maeda S, Egashira K, Kasuga M. MCP-1 contributes to macrophage infiltration into adipose tissue, insulin resistance, and hepatic steatosis in obesity. J Clin Invest 116: 1494-1505, 2006.
26. Kim KH, Lee K, Moon YS, Sul HS. A cysteine-rich adipose tissue-specific secretory factor inhibits adipocyte differentiation. J Biol Chem 276: 11252-11256, 2001.
27. Kintscher U, Hartge M, Hess K, Foryst-Ludwig A, Clemenz M, Wabitsch M, Fischer-Posovszky P, Barth TF, Dragun D, Skurk T, Hauner H, Bluher M, Unger T, Wolf AM, Knippschild U, Hombach V, Marx N. T-lymphocyte infiltration in visceral adipose tissue: a primary event in adipose tissue inflammation and the development of obesity-mediated insulin resistance. Arterioscler Thromb Vasc Biol 28: 1304-1310, 2008.
28. Liepinsh DJ, Grivennikov SI, Klarmann KD, Lagarkova MA, Druts-kaya MS, Lockett SJ, Tessarollo L, McAuliffe M, Keller JR, Kuprash DV, Nedospasov SA. Novel lymphotoxin alpha (LTalpha) knockout micewith unperturbed tumor necrosis factor expression: reassessing LTalpha biological functions. Mol Cell Biol 26: 4214-4225, 2006.
29. Liepinsh DJ, Kruglov AA, Galimov AR, Shakhov AN, Shebzukhov YV, Kuchmiy AA, Grivennikov SI, Tumanov AV, Drutskaya MS, Feigenbaum L, Kuprash DV, Nedospasov SA. Accelerated thymic atrophy as a result of elevated homeostatic expression of the genes encoded by the TNF/lymphotoxin cytokine locus. Eur J Immunol 39: 2906-2915, 2009.
30. Liu Y, Sheng H, Lu L, Wu Z, Chen Q, Xiao H, Jin W. Haplotype-based association of four lymphotoxin-alpha gene polymorphisms with the risk of coronary artery disease in Han Chinese. Tohoku J Exp Med 224: 119-125, 2011.
31. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2[-Delta Delta C(T)] Method. Methods 25: 402-408, 2001.
32. Lo JC, Basak S, James ES, Quiambo RS, Kinsella MC, Alegre ML, Weih F, Franzoso G, Hoffmann A, Fu YX. Coordination between NF-kappaB family members p50 and p52 is essential for mediating LTbetaR signals in the development and organization of secondary lymphoid tissues. Blood 107: 1048-1055, 2006.
33. Lumeng CN, Bodzin JL, Saltiel AR. Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J Clin Invest 117: 175-184, 2007.
34. Lumeng CN, Deyoung SM, Bodzin JL, Saltiel AR. Increased inflammatory properties of adipose tissue macrophages recruited during diet-induced obesity. Diabetes 56: 16-23, 2007.
35. Lumeng CN, Maillard I, Saltiel AR. T-ing up inflammation in fat. Nat Med 15: 846-847, 2009.
36. Lumeng CN, Saltiel AR. Inflammatory links between obesity and metabolic disease. J Clin Invest 121: 2111-2117, 2011.
37. Madge LA, Kluger MS, Orange JS, May MJ. Lymphotoxin-alpha 1 beta 2 and LIGHT induce classical and noncanonical NF-kappa B-dependent proinflammatory gene expression in vascular endothelial cells. J Immunol 180: 3467-3477, 2008.
38. Mahajan A, Tabassum R, Chavali S, Dwivedi OP, Chauhan G, Tandon N, Bharadwaj D. Obesity-dependent association of TNF-LTA locus with type 2 diabetes in North Indians. J Mol Med (Berl) 88: 515-522, 2011.
39. Matthews VB, Allen TL, Risis S, Chan MH, Henstridge DC, Watson N, Zaffino LA, Babb JR, Boon J, Meikle PJ, Jowett JB, Watt MJ, Jansson JO, Bruce CR, Febbraio MA. Interleukin-6-deficient mice develop hepatic inflammation and systemic insulin resistance. Diabetologia 53: 2431-2441, 2010.
40. McCarthy DD, Summers-Deluca L, Vu F, Chiu S, Gao Y, Gommerman JL. The lymphotoxin pathway: beyond lymph node development. Immunol Res 35: 41-54, 2006.
41. Murphy KM, Stockinger B. Effector T cell plasticity: flexibility in the face of changing circumstances. Nat Immunol 11: 674-680, 2010.
42. Murphy M, Walter BN, Pike-Nobile L, Fanger NA, Guyre PM, Browning JL, Ware CF, Epstein LB. Expression of the lymphotoxin beta receptor on follicular stromal cells in human lymphoid tissues. Cell Death Differ 5: 497-505, 1998.
43. Mystkowski P, Shankland E, Schreyer SA, LeBoeuf RC, Schwartz RS, Cummings DE, Kushmerick M, Schwartz MW. Validation of whole-body magnetic resonance spectroscopy as a tool to assess murine body composition. Int J Obes Relat Metab Disord 24: 719-724, 2000.
44. Nakayama T, Yamashita M. The TCR-mediated signaling pathways that control the direction of helper T cell differentiation. Semin Immunol 22: 303-309, 2010.
45. Neels JG, Olefsky JM. Inflamed fat: what starts the fire? J Clin Invest 116: 33-35, 2006.
46. Netea MG, Joosten LA, Lewis E, Jensen DR, Voshol PJ, Kullberg BJ, Tack CJ, van Krieken H, Kim SH, Stalenhoef AF, van de Loo FA, Verschueren I, Pulawa L, Akira S, Eckel RH, Dinarello CA, van den Berg W, van der Meer JW. Deficiency of interleukin-18 in mice leads to hyperphagia, obesity and insulin resistance. Nat Med 12: 650-656, 2006.
47. Nishimura S, Manabe I, Nagasaki M, Eto K, Yamashita H, Ohsugi M, Otsu M, Hara K, Ueki K, Sugiura S, Yoshimura K, Kadowaki T, Nagai R. CD8+ effector T cells contribute to macrophage recruitment and adipose tissue inflammation in obesity. Nat Med 15: 914-920, 2009.
48. Nitta T, Murata S, Ueno T, Tanaka K, Takahama Y. Thymic microenvironments for T-cell repertoire formation. Adv Immunol 99: 59-94, 2008.
49. Nyambayar D, Iwabuchi K, Hedlund E, Murakawa S, Shirai K, Iwabuchi C, Kon Y, Miyazaki Y, Yanagawa Y, Onoe K. Characterization of NKT-cell hybridomas expressing invariant T-cell antigen receptors. J Clin Exp Hematop 47: 1-8, 2007.
50. Obstfeld AE, Sugaru E, Thearle M, Francisco AM, Gayet C, Ginsberg HN, Ables EV, Ferrante AW Jr. C-C chemokine receptor 2 (CCR2) regulates the hepatic recruitment of myeloid cells that promote obesity-induced hepatic steatosis. Diabetes 59: 916-925, 2010.
51. Ohmura K, Ishimori N, Ohmura Y, Tokuhara S, Nozawa A, Horii S, Andoh Y, Fujii S, Iwabuchi K, Onoe K, Tsutsui H. Natural killer T cells are involved in adipose tissues inflammation and glucose intolerance in diet-induced obese mice. Arterioscler Thromb Vasc Biol 30: 193-199, 2010.
52. Olefsky JM, Glass CK. Macrophages, inflammation, and insulin resistance. Annu Rev Physiol 72: 219-246, 2010.
53. Pamir N, McMillen TS, Kaiyala KJ, Schwartz MW, LeBoeuf RC. Receptors for tumor necrosis factor-alpha play a protective role against obesity and alter adipose tissue macrophage status. Endocrinology 150: 4124-4134, 2009.
54. Qi Y, Nie Z, Lee YS, Singhal NS, Scherer PE, Lazar MA, Ahima RS. Loss of resistin improves glucose homeostasis in leptin deficiency. Diabetes 55: 3083-3090, 2006.
55. Reed JA, Clegg DJ, Smith KB, Tolod-Richer EG, Matter EK, Picard LS, Seeley RJ. GM-CSF action in the CNS decreases food intake and body weight. J Clin Invest 115: 3035-3044, 2005.
56. Roach DR, Briscoe H, Saunders B, France MP, Riminton S, Britton WJ. Secreted lymphotoxin-alpha is essential for the control of an intracellular bacterial infection. J Exp Med 193: 239-246, 2001.
57. Rocha VZ, Folco EJ, Sukhova G, Shimizu K, Gotsman I, Vernon AH, Libby P. Interferon-gamma, a Th1 cytokine, regulates fat inflammation: a role for adaptive immunity in obesity. Circ Res 103: 467-476, 2008.
58. Santos MJ, Fernandes D, Caetano-Lopes J, Perpetuo IP, Vidal B, Canhao H, Fonseca JE. Lymphotoxin-a 252 A>G polymorphism: a link between disease susceptibility and dyslipidemia in rheumatoid arthritis? J Rheumatol 38: 1244-1249, 2011.
59. Schreyer SA, Chua SC Jr, LeBoeuf RC. Obesity and diabetes in TNF-alpha receptor-deficient mice. J Clin Invest 102: 402-411, 1998.
60. Schreyer SA, Lystig TC, Vick CM, LeBoeuf RC. Mice deficient in apolipoprotein E but not LDL receptors are resistant to accelerated atherosclerosis associated with obesity. Atherosclerosis 171: 49-55, 2003.
61. Schreyer SA, Vick CM, LeBoeuf RC. Loss of lymphotoxin-alpha but not tumor necrosis factor-alpha reduces atherosclerosis in mice. J Biol Chem 277: 12364-12368, 2002.
62. Shaul ME, Bennett G, Strissel KJ, Greenberg AS, Obin MS. Dynamic, M2-like remodeling phenotypes of CD11c+ adipose tissue macrophages during high-fat diet-induced obesity in mice. Diabetes 59: 1171-1181, 2010.
63. Shoelson SE, Lee J, Goldfine AB. Inflammation and insulin resistance. J Clin Invest 116: 1793-1801, 2006.
64. Smith-Garvin JE, Koretzky GA, Jordan MS. T cell activation. Annu Rev Immunol 27: 591-619, 2009.
65. Stauber GB, Aggarwal BB. Characterization and affinity cross-linking of receptors for human recombinant lymphotoxin (tumor necrosis factor-beta) on a human histiocytic lymphoma cell line, U-937. J Biol Chem 264: 3573-3576, 1989.
66. Steppan CM, Bailey ST, Bhat S, Brown EJ, Banerjee RR, Wright CM, Patel HR, Ahima RS, Lazar MA. The hormone resistin links obesity to diabetes. Nature 409: 307-312, 2001.
67. Takahashi K, Mizuarai S, Araki H, Mashiko S, Ishihara A, Kanatani A, Itadani H, Kotani H. Adiposity elevates plasma MCP-1 levels leading to the increased CD11b-positive monocytes in mice. J Biol Chem 278: 46654-46660, 2003.
68. Tanaka R, Miwa Y, Mou K, Tomikawa M, Eguchi N, Urade Y, Takahashi-Yanaga F, Morimoto S, Wake N, Sasaguri T. Knockout of the l-pgds gene aggravates obesity and atherosclerosis in mice. Biochem Biophys Res Commun 378: 851-856, 2009.
69. Tateya S, Rizzo NO, Handa P, Cheng AM, Morgan-Stevenson V, Daum G, Clowes AW, Morton GJ, Schwartz MW, Kim F. Endothelial NO/cGMP/VASP signaling attenuates Kupffer cell activation and hepatic insulin resistance induced by high-fat feeding. Diabetes 60: 2792-2801, 2011.
70. Uysal KT, Wiesbrock SM, Hotamisligil GS. Functional analysis of tumor necrosis factor (TNF) receptors in TNF-alpha-mediated insulin resistance in genetic obesity. Endocrinology 139: 4832-4838, 1998.
71. Uysal KT, Wiesbrock SM, Marino MW, Hotamisligil GS. Protection from obesity-induced insulin resistance in mice lacking TNF-alpha function. Nature 389: 610-614, 1997.
72. Verwaerde C, Delanoye A, Macia L, Tailleux A, Wolowczuk I. Influence of high-fat feeding on both naive and antigen-experienced T-cell immune response in DO10.11 mice. Scand J Immunol 64: 457-466, 2006.
73. Wallenius V, Wallenius K, Ahren B, Rudling M, Carlsten H, Dickson SL, Ohlsson C, Jansson JO. Interleukin-6-deficient mice develop mature-onset obesity. Nat Med 8: 75-79, 2002.
74. Weisberg SP, McCann D, Desai M, Rosenbaum M, Leibel RL, Ferrante AW Jr. Obesity is associated with macrophage accumulation in adipose tissue. J Clin Invest 112: 1796-1808, 2003.
75. Wellen KE, Hotamisligil GS. Obesity-induced inflammatory changes in adipose tissue. J Clin Invest 112: 1785-1788, 2003.
76. Winer DA, Winer S, Shen L, Wadia PP, Yantha J, Paltser G, Tsui H, Wu P, Davidson MG, Alonso MN, Leong HX, Glassford A, Caimol M, Kenkel JA, Tedder TF, McLaughlin T, Miklos DB, Dosch HM, Engleman EG. B cells promote insulin resistance through modulation of T cells and production of pathogenic IgG antibodies. Nat Med 17: 610-617, 2011.
77. Winer S, Chan Y, Paltser G, Truong D, Tsui H, Bahrami J, Dorfman R, Wang Y, Zielenski J, Mastronardi F, Maezawa Y, Drucker DJ, Engleman E, Winer D, Dosch HM. Normalization of obesity-associated insulin resistance through immunotherapy. Nat Med 15: 921-929, 2009.
78. Wolf MJ, Seleznik GM, Zeller N, Heikenwalder M. The unexpected role of lymphotoxin beta receptor signaling in carcinogenesis: from lymphoid tissue formation to liver and prostate cancer development. Oncogene 29: 5006-5018, 2010.
79. Wu H, Ghosh S, Perrard XD, Feng L, Garcia GE, Perrard JL, Sweeney JF, Peterson LE, Chan L, Smith CW, Ballantyne CM. T-cell accumulation and regulated on activation, normal T cell expressed and secreted upregulation in adipose tissue in obesity. Circulation 115: 1029-1038, 2007.
80. Wu Q, Wang Y, Wang J, Hedgeman EO, Browning JL, Fu YX. The requirement of membrane lymphotoxin for the presence of dendritic cells in lymphoid tissues. J Exp Med 190: 629-638, 1999.
81. Xu H, Barnes GT, Yang Q, Tan G, Yang D, Chou CJ, Sole J, Nichols A, Ross JS, Tartaglia LA, Chen H. Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. J Clin Invest 112:1821-1830, 2003.
82. Yamakawa T, Tanaka S, Yamakawa Y, Kiuchi Y, Isoda F, Kawamoto S, Okuda K, Sekihara H. Augmented production of tumor necrosis factor-alpha in obese mice. Clin Immunol Immunopathol 75: 51-56, 1995.
83. Zeyda M, Huber J, Prager G, Stulnig TM. Inflammation correlates with markers of T-cell subsets including regulatory T cells in adipose tissue from obese patients. Obesity (Silver Spring) 19: 743-748, 2011.
84. Zhu J, Yamane H, Paul WE. Differentiation of effector CD4 T cell populations (*). Annu Rev Immunol 28: 445-489, 2010.
85. Ziegler SF, Buckner JH. FOXP3 and the regulation of Treg/Th17 differentiation. Microbes Infect 11: 594-598, 2009.
86. Zorrilla EP, Sanchez-Alavez M, Sugama S, Brennan M, Fernandez R, Bartfai T, Conti B. Interleukin-18 controls energy homeostasis by suppressing appetite and feed efficiency. Proc Natl Acad Sci USA 104: 11097-11102, 2007.