Impairment of Host Resistance toListeria monocytogenesInfection in Liver ofdb/dbandob/obMice

Diabetes - Tập 54 Số 1 - Trang 182-189 - 2005
Shin Ikejima1,2, Sanae Sasaki1, Hiroshi Sashinami1, Fumiaki Mori3, Yoshiji Ogawa2, Teruo Nakamura4, Yoshinao Abe5, Koichi Wakabayashi3, Toshihiro Suda2, Akio Nakane1
1Department of Bacteriology, Hirosaki University School of Medicine, Hirosaki, Aomori, Japan
2Third Department of Medicine, Hirosaki University School of Medicine, Hirosaki, Aomori, Japan
3Department of Molecular Biology, Institute of Brain Science, Hirosaki University School of Medicine, Hirosaki, Aomori, Japan
4Department of Medical Technology, Hirosaki University School of Health Sciences, Hirosaki University, Hirosaki, Aomori, Japan
5Department of Radiology, Hirosaki University School of Medicine, Hirosaki, Aomori, Japan.

Tóm tắt

Leptin is an adipocyte-derived hormone that regulates a number of physiological functions, including energy homeostasis and immune function. In immune responses, leptin plays a role in the induction of inflammation. We investigated a role of leptin in Listeria monocytogenes infection using leptin receptor–deficient db/db mice and leptin-deficient ob/ob mice. These mutant mice were highly susceptible to L. monocytogenes, and the elimination of bacteria from the liver was inhibited. After infection, the induction of monocyte chemoattractant protein-1 (MCP-1) and KC mRNA in the liver of db/db mice and the MCP-1 mRNA expression in the liver of ob/ob mice was decreased compared with their heterozygote littermates. Leptin replacement in ob/ob mice resulted in improvement of anti-listerial resistance and the MCP-1 mRNA expression. The elimination of L. monocytogenes was significantly enhanced, and the expression of MCP-1 and KC mRNA was completely reversed in db/db mice by insulin treatment. These results suggest that leptin is required for host resistance to L. monocytogenes infection and that hyperglycemia caused by leptin deficiency is involved in the inefficient elimination of bacteria from the liver. Moreover, defect of MCP-1 expression in the liver may be involved in the attenuated host resistance in these mutant mice.

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Tài liệu tham khảo

Zhang Y, Proenca R, Maffel M, Barone M, Leopold L, Friedman JM: Positional cloning of the mouse obese gene and its human homologue. Nature 372:425–432,1994

Halaas JL, Gajiwals KS, Maffei M, Cohen SL, Chait BT, Rabinowitz D, Lallone RL, Burley SK, Friedman JM: Weight-reducing effects of the plasma protein encoded by the obese gene. Science 269:543–546,1995

Chen H, Charlat O, Tartaglia LA, Woolf EA, Weng X, Ellis SJ, Lakey ND, Culpepper J, Moore KJ, Breitbart RE, Duyk GM, Tepper RI, Morgenstem JP: Evidence that the diabetes gene encodes the leptin receptor: identification of a mutation in the leptin receptor gene in db/db mice. Cell 84:491–495,1996

Coleman DL: Obese and diabetes: two mutant genes causing diabetes-obesity syndromes in mice. Diabetologia 14:141–148,1978

Ahima RS, Saper CB, Flier JS, Elmquist JK: Leptin regulation of neuroendocrine systems. Front Neuroendocrinol 21:263–307,2000

Fantussi G, Faggioni R: Leptin in the regulation of immunity, inflammation, and hematopoiesis. J Leukoc Biol 68:437–446,2000

Lord GM, Matarese G, Howard JK, Baker RJ, Bloom SR, Lechler RI: Leptin modulates the T-cell immune response and reverses starvation-induced immunosuppression. Nature 394:897–901,1998

Matarese G, Di Giacomo A, Sanna V, Lord GM, Howard JK, Di Tuoro A, Bloom SR, Lechler RI, Zappacosta S, Fontana S: Requirement for leptin in the induction and progression of autoimmune encephalomyelitis. J Immunol 166:5909–5916,2001

Busso N, So A, Chobaz-Peclat V, Morard C, martinez-Soria E, Talabot-Ayer, Gabay C: Leptin signaling deficiency impairs humoral and cellular immune responses and attenuates experimental arthritis. J Immunol 168:875–882,2002

Caldefie-Chezet F, Poulin A, Tridon A, Sion B, Vasson M-P: Leptin: a potential regulator of polymorphonuclear neutrophil bactericidal action?J Leukoc Biol 69:414–418,2001

Mancuso P, Gottschalk A, Phare SM, Peters-Golden M, Lukacs NW, Huffnagle GB: Leptin-decifient mice exhibit impaired host defense in Gram-negative pneumonia. J Immunol 168:4018–4024,2002

Moore SI, Huffnagel GB, Chen G-H, White ES, Mancuso P: Leptin modulates neutrophil phagocytosis of Klebsiella pneumoniae. Infect Immun 71:4182–4185,2003

Rayfield EJ, Ault MJ, Keusch GT, Brothers MJ, Nechemias C, Smith H: Infection and diabetes: the case for glucose control. Am J Med 72:439–450,1982

Joshi N, Caputo GM, Weitekamp MR, Karchmer AW: Infections in patients with diabetes mellitus. N Engl J Med 341:1906–1912,1999

Skogberg K, Syrjanen J, Jahkola M, Renkonen OV, Paavonen J, Ahonen J, Kontiainen S, Ruutu P, Valtonen V: Clinical presentation and outcome of listeriosis in patients with and without immnosuppressive therapy. Clin Infect Dis 14:815–821,1992

Hsieh C-S, Macatonis SE, Tripp CS, Wolf SF, O’Garra A, Murphy KM: Development of Th1 CD4+ T-cells through IL-12 produced by Listeria-induced macrophages. Science 260:547–549,1993

Buchmeier NA, Schreiber RD: Requirement of endogenous interferon-γ for resolution of Listeria monocytogenes infection. Proc Natl Acad Sci U S A 82:7404–7408,1985

Huang S, Hendriks W, Althage A, Hemmi S, Bluthmann H, Kamijo R, Vilcek J, Zinkernagel RM, Aguet M: Immune response in mice that lack the intereferon-γ receptor. Science 259:1742–1745,1993

Mackaness GB: Cellular resistance to infection. J Exp Med 116:381–402,1962

Conlan JW, North RJ: Neutrophils are essential for early anti-Listeria defense in the liver, but not in the spleen or peritoneal cavity, as revealed by a granulocyte-depleting monoclonal antibody. J Exp Med 179:259–268,1994

Luster AD: Chemokines: chemotactic cytokines that mediate inflammation. N Engl J Med 338:436–445,1998

Kurihara T, Warr G, Loy J, Bravo R: Defects in macrophage recruitment and host defense in mice lacking the CCR2 chemokine receptor. J Exp Med 186:1757–1762,1997

Czuprynski CJ, Brown JF, Steinberg H, Carroll D: Mice lacking the murine interleukin-8 receptor homologue demonstrate paradoxical responses to acute and chronic experimental infection with Listeria monocytogenes. Microb Pathog 24:17–23,1998

Chensue SW: Molecular machinations: chemokine signals in host-pathogen interactions. Clin Microbiol Rev 14:821–835,2001

Nakane A, Minagawa T, Kohanawa M, Chen Y, Sato H, Moriyama M, Tsuruoka N: Interactions between endogenous gamma interferon and tumor necrosis factor in host resistance against primary and secondary Listeria monocytogenes infections. Infect Immun 57:3331–3337,1989

Chomczynski P, Sacci N: Single step method for RNA isolation by acid guanidium thiocyanate-phenol-chloroform extraction. Anal Biochem 162:156–159,1987

Ishida Y, Konda T, Ohshima T, Fujiwara H, Iwakura Y, Mukaida N: A pivotal involvement of IFN-γ in the pathogenesis of acetaminophen-induced acute liver injury. FASEB J 16:1227–1236,2002

Yang S, Lin H, Diehl AM: Fatty liver vulnerability to endotoxin-induced damage despite NF-κB induction and inhibited caspase 3 activity. Am J Physiol Gastrointest Liver Physiol 281:G382–G392,2001

Sasaki T, Mieno M, Udono H, Yamaguchi K, Usui T, Hara K, Shiku H, Nakayama E: Roles of CD4+ and CD8+ cells, and the effect of administration of recombinant murine interferon γ in listerial infection. J Exp Med 171:1141–1154,1990

Gregory SH, Sagnimeni AJ, Wing EJ: Bacteria in the bloodstream are trapped in the liver and killed by immigrating neutrophils. J Immunol 157:2514–2520,1996

Rutledge BJ, Rayburn H, Rosenberg R, North RJ, Gladue RP, Crless CL, Rollins BJ: High level monocyte chemoattractant protein-1 expression in transgenic mice increases their susceptibility to intracellular pathogens. J Immunol 155:4838–4843,1995

Peters W, Scott HM, Chambers HF, Flynn JL, Charo IF, Ernst JD: Chemokine receptor 2 serves an early and essential role in resistance to Mycobacterium tuberculosis. Proc Natl Acad Sci U S A 98:7958–7963,2001

Kielian T, Barry B, Hickey WF: CXC chemokine receptor-2 ligands are required for neutrophil-mediated host defense in experimental brain abscesses. J Immunol 166:4634–4643,2001

Greenberger MJ, Strieter RM, Kunkel SL, Danforth JM, Laichalk LL, McGillicuddy DC, Standiford TJ: Neutralization of macrophage inflammatory protein-2 attenuates neutrophil recruitment and bacterial clearance in murine Klebsiella pneumonia. J Infect Dis 173:159–165,1996

Tauzon CU, Perez A, Kishiba T, Sheegren JN: Staphylococcus aureus among insulin-injecting diabetic patients. JAMA 231:1272,1975

Robbins SL, Tucker AW Jr: The cause of death in diabetes: a report of 307 autopsied cases. N Engl J Med 231:865,1944