Obese mice exhibit an altered behavioural and inflammatory response to lipopolysaccharide

DMM Disease Models and Mechanisms

Volumn 5, Issue 5, 2012, Pages 649-659

  Lawrence, Catherine B ^a   Brough, David ^a   Knight, Elysse M ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; INTERLEUKIN 1BETA; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; PROTEIN FOS;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANOREXIA; ARTICLE; BEHAVIOR DISORDER; BODY WEIGHT; BRAIN CELL; BRAIN NUCLEUS; BRAIN REGION; CONTROLLED STUDY; CORE TEMPERATURE; CYTOKINE RELEASE; FEVER; FOOD INTAKE; INFLAMMATION; LIVER; MALE; MOUSE; NERVE CONDUCTION; NONHUMAN; OBESITY; PERITONEUM MACROPHAGE; PLASMA; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPLEEN;

ANIMALS; BEHAVIOR, ANIMAL; BODY TEMPERATURE; BODY WEIGHT; BRAIN; CELLS, CULTURED; CYTOKINES; DIET, HIGH-FAT; FEEDING BEHAVIOR; INFLAMMATION; INJECTIONS, INTRAPERITONEAL; LIPOPOLYSACCHARIDES; LIVER; MACROPHAGES, PERITONEAL; MALE; MICE; MICE, INBRED C57BL; MICE, OBESE; OBESITY; PROTO-ONCOGENE PROTEINS C-FOS; SPLEEN;

ANIMALIA; MUS;

EID: 84865484380     PISSN: 17548403     EISSN: 17548411     Source Type: Journal    
DOI: 10.1242/dmm.009068     Document Type: Article

References (72)

1. Al Zahrani, M. S., Bissada, N. F. and Borawskit, E. A. (2003). Obesity and periodontal disease in young, middle-aged, and older adults. J. Periodontol. 74, 610-615. (Pubitemid 36701374)
2. Altunkaynak, B. Z., Ozbek, E. and Altunkaynak, M. E. (2007). A stereological and histological analysis of spleen on obese female rats, fed with high fat diet. Saudi Med. J. 28, 353-357. (Pubitemid 46605052)
3. Amar, S., Zhou, Q., Shaik-Dasthagirisaheb, Y. and Leeman, S. (2007). Diet-induced obesity in mice causes changes in immune responses and bone loss manifested by bacterial challenge. Proc. Natl. Acad. Sci. USA 104, 20466-20471.
4. Arons, M. M., Wheeler, A. P., Bernard, G. R., Christman, B. W., Russell, J. A., Schein, R., Summer, W. R., Steinberg, K. P., Fulkerson, W., Wright, P., Dupont, W. D. and Swindell, B. B. (1999). Effects of ibuprofen on the physiology and survival of hypothermic sepsis. Ibuprofen in Sepsis Study Group. Crit. Care Med. 27, 699-707. (Pubitemid 29218201)
5. Bercault, N., Boulain, T., Kuteifan, K., Wolf, M., Runge, I. and Fleury, J. C. (2004). Obesity-related excess mortality rate in an adult intensive care unit: A risk-adjusted matched cohort study. Crit. Care Med. 32, 998-1003. (Pubitemid 38471522)
6. Bessesen, D. H. (2008). Update on obesity. J. Clin. Endocrinol. Metab. 93, 2027-2034.
7. Cartmell, T., Luheshi, G. N. and Rothwell, N. J. (1999). Brain sites of action of endogenous interleukin-1 in the febrile response to localized inflammation in the rat. J. Physiol. 518, 585-594. (Pubitemid 29366753)
8. Cartmell, T., Poole, S., Turnbull, A. V., Rothwell, N. J. and Luheshi, G. N. (2000). Circulating interleukin-6 mediates the febrile response to localised inflammation in rats. J. Physiol. 526, 653-661. (Pubitemid 30654768)
9. Cartmell, T., Luheshi, G. N., Hopkins, S. J., Rothwell, N. J. and Poole, S. (2001). Role of endogenous interleukin-1 receptor antagonist in regulating fever induced by localised inflammation in the rat. J. Physiol. 531, 171-180. (Pubitemid 32178035)
10. Chandra, R. K. (1980). Cell-mediated immunity in genetically obese C57BL/6J ob/ob) mice. Am. J. Clin. Nutr. 33, 13-16.
11. Clemmer, T. P., Fisher, C. J., Jr, Bone, R. C., Slotman, G. J., Metz, C. A. and Thomas, F. O. (1992). Hypothermia in the sepsis syndrome and clinical outcome. The Methylprednisolone Severe Sepsis Study Group. Crit. Care Med. 20, 1395-1401.
12. Cohen, J. (2002). The immunopathogenesis of sepsis. Nature 420, 885-891.
13. Cousin, B., Andre, M., Casteilla, L. and Penicaud, L. (2001). Altered macrophage-like functions of preadipocytes in inflammation and genetic obesity. J. Cell Physiol. 186, 380-386. (Pubitemid 32147721)
14. Dantzer, R. (2004). Cytokine-induced sickness behaviour: a neuroimmune response to activation of innate immunity. Eur. J. Pharmacol. 500, 399-411.
15. Dantzer, R. and Kelley, K. W. (2007). Twenty years of research on cytokine-induced sickness behavior. Brain Behav. Immun. 21, 153-160. (Pubitemid 46038917)
16. Day, H. E. and Akil, H. (1996). Differential pattern of c-fos mRNA in rat brain following central and systemic administration of interleukin-1-beta: implications for mechanism of action. Neuroendocrinology 63, 207-218. (Pubitemid 26070807)
17. Faggioni, R., Fuller, J., Moser, A., Feingold, K. R. and Grunfeld, C. (1997). LPSinduced anorexia in leptin-deficient (ob/ob) and leptin receptor-deficient (db/db) mice. Am. J. Physiol. 273, R181-R186.
18. Faggioni, R., Fantuzzi, G., Gabay, C., Moser, A., Dinarello, C. A., Feingold, K. R. and Grunfeld, C. (1999). Leptin deficiency enhances sensitivity to endotoxin-induced lethality. Am. J. Physiol. 276, R136-R142. (Pubitemid 29061699)
19. Falagas, M. E. and Kompoti, M. (2006). Obesity and infection. Lancet. Infect. Dis. 6, 438-446.
20. Fantuzzi, G. (2005). Adipose tissue, adipokines, and inflammation. J. Allergy Clin. Immunol. 115, 911-919.
21. Farooqi, I. S. (2008). Monogenic human obesity. Front. Horm. Res. 36, 1-11.
22. Franklin, K. and Paxinos, G. (1997). The Mouse Brain in Stereotaxic Coordinates. New York, USA: Elsevier.
23. Garcia, H. L. (2002). Dermatological complications of obesity. Am. J. Clin. Dermatol. 3, 497-506.
24. Gottschlich, M. M., Mayes, T., Khoury, J. C. and Warden, G. D. (1993). Significance of obesity on nutritional, immunologic, hormonal, and clinical outcome parameters in burns. J. Am. Diet. Assoc. 93, 1261-1268. (Pubitemid 23333470)
25. Hirsch, E., Irikura, V. M., Paul, S. M. and Hirsh, D. (1996). Functions of interleukin 1 receptor antagonist in gene knockout and overproducing mice. Proc. Natl. Acad. Sci. USA 93, 11008-11013. (Pubitemid 26333108)
26. Hsu, A., Aronoff, D. M., Phipps, J., Goel, D. and Mancuso, P. (2007). Leptin improves pulmonary bacterial clearance and survival in ob/ob mice during pneumococcal pneumonia. Clin. Exp. Immunol. 150, 332-339. (Pubitemid 47609568)
27. Huang, H., Liu, T., Rose, J. L., Stevens, R. L. and Hoyt, D. G. (2007). Sensitivity of mice to lipopolysaccharide is increased by a high saturated fat and cholesterol diet. J. Inflamm. (Lond.) 4, 22.
28. Ikejima, S., Sasaki, S., Sashinami, H., Mori, F., Ogawa, Y., Nakamura, T., Abe, Y., Wakabayashi, K., Suda, T. and Nakane, A. (2005). Impairment of host resistance to Listeria monocytogenes infection in liver of db/db and ob/ob mice. Diabetes 54, 182-189. (Pubitemid 40105111)
29. Ivanov, A. I. and Romanovsky, A. A. (2002). Fever responses of Zucker rats with and without fatty mutation of the leptin receptor. Am. J. Physiol. Regul. Integr. Comp. Physiol. 282, R311-R316. (Pubitemid 34663941)
30. Ivanov, A. I., Kulchitsky, V. A. and Romanovsky, A. A. (2001). Does obesity affect febrile responsiveness? Int. J. Obes. Relat. Metab. Disord. 25, 586-589. (Pubitemid 32289655)
31. Jeffery, N. M., Sanderson, P., Newsholme, E. A. and Calder, P. C. (1997). Effects of varying the type of saturated fatty acid in the rat diet upon serum lipid levels and spleen lymphocyte functions. Biochim. Biophys. Acta 1345, 223-236. (Pubitemid 27171200)
32. Juge-Aubry, C. E., Henrichot, E. and Meier, C. A. (2005). Adipose tissue: a regulator of inflammation. Best Pract. Res. Clin. Endocrinol. Metab. 19, 547-566. (Pubitemid 41823815)
33. Kiki, I., Altunkaynak, B. Z., Altunkaynak, M. E., Vuraler, O., Unal, D. and Kaplan, S. (2007). Effect of high fat diet on the volume of liver and quantitative feature of Kupffer cells in the female rat: a stereological and ultrastructural study. Obes. Surg. 17, 1381-1388.
34. Kjerrulf, M., Berke, Z., Aspegren, A., Umaerus, M., Nilsson, T., Svensson, L. and Hurt-Camejo, E. (2006). Reduced cholesterol accumulation by leptin deficient (ob/ob) mouse macrophages. Inflamm. Res. 55, 300-309. (Pubitemid 44359134)
35. Lam, Q. L. and Lu, L. (2007). Role of leptin in immunity. Cell Mol. Immunol. 4, 1-13.
36. Lamas, O., Martinez, J. A. and Marti, A. (2004). Decreased splenic mRNA expression levels of TNF-alpha and IL-6 in diet-induced obese animals. J. Physiol. Biochem. 60, 279-283.
37. Le Feuvre, R. A., Brough, D., Iwakura, Y., Takeda, K. and Rothwell, N. J. (2002). Priming of macrophages with lipopolysaccharide potentiates P2X7-mediated cell death via a caspase-1-dependent mechanism, independently of cytokine production. J. Biol. Chem. 277, 3210-3218. (Pubitemid 34953183)
38. Lee, F. Y., Li, Y., Yang, E. K., Yang, S. Q., Lin, H. Z., Trush, M. A., Dannenberg, A. J. and Diehl, A. M. (1999). Phenotypic abnormalities in macrophages from leptindeficient, obese mice. Am. J. Physiol. 276, C386-C394. (Pubitemid 29100562)
39. Li, Z., Soloski, M. J. and Diehl, A. M. (2005). Dietary factors alter hepatic innate immune system in mice with nonalcoholic fatty liver disease. Hepatology 42, 880-885. (Pubitemid 41401126)
40. Loffreda, S., Yang, S. Q., Lin, H. Z., Karp, C. L., Brengman, M. L., Wang, D. J., Klein, A. S., Bulkley, G. B., Bao, C., Noble, P. W., Lane, M. D. and Diehl, A. M. (1998). Leptin regulates proinflammatory immune responses. FASEB J. 12, 57-65. (Pubitemid 28060271)
41. Lugarini, F., Hrupka, B. J., Schwartz, G. J., Plata-Salaman, C. R. and Langhans, W. (2005). Acute and chronic administration of immunomodulators induces anorexia in Zucker rats. Physiol. Behav. 84, 165-173. (Pubitemid 40092077)
42. Mancuso, P., Gottschalk, A., Phare, S. M., Peters-Golden, M., Lukacs, N. W. and Huffnagle, G. B. (2002). Leptin-deficient mice exhibit impaired host defense in Gram-negative pneumonia. J. Immunol. 168, 4018-4024. (Pubitemid 34298407)
43. Mito, N., Hosoda, T., Kato, C. and Sato, K. (2000). Change of cytokine balance in dietinduced obese mice. Metabolism 49, 1295-1300.
44. Miyazaki, Y., Iwabuchi, K., Iwata, D., Miyazaki, A., Kon, Y., Niino, M., Kikuchi, S., Yanagawa, Y., Kaer, L. V., Sasaki, H. and Onoe, K. (2008). Effect of high fat diet on NKT cell function and NKT cell-mediated regulation of Th1 responses. Scand. J. Immunol. 67, 230-237. (Pubitemid 351197163)
45. Morrow, W. J., Ohashi, Y., Hall, J., Pribnow, J., Hirose, S., Shirai, T. and Levy, J. A. (1985). Dietary fat and immune function. I. Antibody responses, lymphocyte and accessory cell function in (NZB x NZW)F1 mice. J. Immunol. 135, 3857-3863. (Pubitemid 16250359)
46. O'Connor, J. C., Satpathy, A., Hartman, M. E., Horvath, E. M., Kelley, K. W., Dantzer, R., Johnson, R. W. and Freund, G. G. (2005). IL-1beta-mediated innate immunity is amplified in the db/db mouse model of type 2 diabetes. J. Immunol. 174, 4991-4997.
47. Ordway, D., Henao-Tamayo, M., Smith, E., Shanley, C., Harton, M., Troudt, J., Bai, X., Basaraba, R. J., Orme, I. M. and Chan, E. D. (2008). Animal model of Mycobacterium abscessus lung infection. J. Leukoc. Biol. 83, 1502-1511. (Pubitemid 351960332)
48. Park, S., Rich, J., Hanses, F. and Lee, J. C. (2009). Defects in innate immunity predispose C57BL/6J-Leprdb/Leprdb mice to infection by Staphylococcus aureus. Infect. Immun. 77, 1008-1014.
49. Plotkin, B. J., Paulson, D., Chelich, A., Jurak, D., Cole, J., Kasimos, J., Burdick, J. R. and Casteel, N. (1996). Immune responsiveness in a rat model for type II diabetes (Zucker rat, fa/fa): susceptibility to Candida albicans infection and leucocyte function. J. Med. Microbiol. 44, 277-283. (Pubitemid 26153290)
50. Pohl, J., Woodside, B. and Luheshi, G. N. (2009). Changes in hypothalamically mediated acute-phase inflammatory responses to lipopolysaccharide in dietinduced obese rats. Endocrinology 150, 4901-4910.
51. Romanovsky, A. A., Almeida, M. C., Aronoff, D. M., Ivanov, A. I., Konsman, J. P., Steiner, A. A. and Turek, V. F. (2005). Fever and hypothermia in systemic inflammation: recent discoveries and revisions. Front. Biosci. 10, 2193-2216. (Pubitemid 40905292)
52. Rosenthal, M., Roth, J., Storr, B. and Zeisberger, E. (1996). Fever response in lean (Fa/-) and obese (fa/fa) Zucker rats and its lack to repeated injections of LPS. Physiol. Behav. 59, 787-793. (Pubitemid 26110700)
53. Roth, J. and De Souza, G. E. (2001). Fever induction pathways: evidence from responses to systemic or local cytokine formation. Braz. J. Med. Biol. Res. 34, 301-314. (Pubitemid 33605793)
54. Rudaya, A. Y., Steiner, A. A., Robbins, J. R., Dragic, A. S. and Romanovsky, A. A. (2005). Thermoregulatory responses to lipopolysaccharide in the mouse: dependence on the dose and ambient temperature. Am. J. Physiol. Regul. Integr. Comp. Physiol. 289, R1244-R1252. (Pubitemid 41507387)
55. Sabato, R., Guido, P., Salerno, F. G., Resta, O., Spanevello, A. and Barbaro, M. P. (2006). Airway inflammation in patients affected by obstructive sleep apnea. Monaldi. Arch. Chest Dis. 65, 102-105. (Pubitemid 44209761)
56. Sagar, S. M., Price, K. J., Kasting, N. W. and Sharp, F. R. (1995). Anatomic patterns of Fos immunostaining in rat brain following systemic endotoxin administration. Brain Res. Bull. 36, 381-392.
57. Salerno, F. G., Carpagnano, E., Guido, P., Bonsignore, M. R., Roberti, A., Aliani, M., Vignola, A. M. and Spanevello, A. (2004). Airway inflammation in patients affected by obstructive sleep apnea syndrome. Respir. Med. 98, 25-28. (Pubitemid 38100751)
58. Smith, A. G., Sheridan, P. A., Harp, J. B. and Beck, M. A. (2007). Diet-induced obese mice have increased mortality and altered immune responses when infected with influenza virus. J. Nutr. 137, 1236-1243. (Pubitemid 46701917)
59. Steiner, A. A. and Romanovsky, A. A. (2007). Leptin: at the crossroads of energy balance and systemic inflammation. Prog. Lipid Res. 46, 89-107. (Pubitemid 46654230)
60. Steiner, A. A., Dogan, M. D., Ivanov, A. I., Patel, S., Rudaya, A. Y., Jennings, D. H., Orchinik, M., Pace, T. W., O'connor, K. A., Watkins, L. R. and Romanovsky, A. A. (2004). A new function of the leptin receptor: mediation of the recovery from lipopolysaccharide-induced hypothermia. FASEB J. 18, 1949-1951.
61. Stewart-Phillips, J. L., Lough, J. and Phillips, N. C. (1991). The effect of a high-fat diet on murine macrophage activity. Int. J. Immunopharmacol. 13, 325-332.
62. Strandberg, L., Verdrengh, M., Enge, M., Andersson, N., Amu, S., Onnheim, K., Benrick, A., Brisslert, M., Bylund, J., Bokarewa, M., Nilsson, S. and Jansson, J. O. (2009). Mice chronically fed high-fat diet have increased mortality and disturbed immune response in sepsis. PLoS ONE 4, e7605.
63. Thorsteinsdottir, B., Tleyjeh, I. M. and Baddour, L. M. (2005). Abdominal wall cellulitis in the morbidly obese. Scand. J. Infect. Dis. 37, 605-608.
64. Vachharajani, V. (2008). Influence of obesity on sepsis. Pathophysiology. 15, 123-134.
65. Vilar-Compte, D., Mohar, A., Sandoval, S., de la Rosa, M., Gordillo, P. and Volkow, P. (2000). Surgical site infections at the National Cancer Institute in Mexico: a casecontrol study. Am. J. Infect. Control 28, 14-20. (Pubitemid 30120934)
66. Vlach, K. D., Boles, J. W. and Stiles, B. G. (2000). Telemetric evaluation of body temperature and physical activity as predictors of mortality in a murine model of staphylococcal enterotoxic shock. Comp. Med. 50, 160-166. (Pubitemid 30227812)
67. Wallace, F. A., Neely, S. J., Miles, E. A. and Calder, P. C. (2000). Dietary fats affect macrophage-mediated cytotoxicity towards tumour cells. Immunol. Cell Biol. 78, 40-48. (Pubitemid 30090988)
68. Wang, J., Ando, T. and Dunn, A. J. (1997). Effect of homologous interleukin-1, interleukin-6 and tumor necrosis factor-alpha on the core body temperature of mice. Neuroimmunomodulation. 4, 230-236. (Pubitemid 28231584)
69. Wehrens, A., Aebischer, T., Meyer, T. F. and Walduck, A. K. (2008). Leptin receptor signaling is required for vaccine-induced protection against Helicobacter pylori. Helicobacter 13, 94-102. (Pubitemid 351347662)
70. Wood, N., Johnson, R. B. and Streckfus, C. F. (2003). Comparison of body composition and periodontal disease using nutritional assessment techniques: Third National Health and Nutrition Examination Survey (NHANES III). J. Clin. Periodontol. 30, 321-327. (Pubitemid 38019392)
71. Yaegashi, M., Jean, R., Zuriqat, M., Noack, S. and Homel, P. (2005). Outcome of morbid obesity in the intensive care unit. J. Intensive Care Med. 20, 147-154. (Pubitemid 43086466)
72. Yaqoob, P., Newsholme, E. A. and Calder, P. C. (1994). Inhibition of natural killer cell activity by dietary lipids. Immunol. Lett. 41, 241-247. (Pubitemid 24279496)