Histamine H2 receptor signaling in the pathogenesis of sepsis: Studies in a murine diabetes model

Journal of Immunology

Volumn 191, Issue 3, 2013, Pages 1373-1382

  Carlos, Daniela ^a   Spiller, Fernando ^a   Souto, Fabricio O ^a   Trevelin, Silvia C ^a   Borges, Vanessa F ^a   De Freitas, Andressa ^a   Alves Filho, Jose C ^a   Silva, Joao S ^a   Ryffel, Bernhard ^b   Cunha, Fernando Q ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b UNIVERSITÉ D'ORLÉANS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CXCR2; G PROTEIN COUPLED RECEPTOR KINASE 2; HISTAMINE H2 RECEPTOR;

ALLOXAN DIABETES MELLITUS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTEREMIA; CELL GRANULE; CONTROLLED STUDY; DISEASE SEVERITY; DOWN REGULATION; FEMALE; HISTAMINE RELEASE; INFECTION CONTROL; INFLAMMATION; INSULIN DEPENDENT DIABETES MELLITUS; LEUKOCYTE MIGRATION; MAST CELL; MORTALITY; MOUSE; NEUTROPHIL; NONHUMAN; PATHOGENESIS; PERITONEAL CAVITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEPSIS; SURVIVAL; SYSTEMIC INFLAMMATORY RESPONSE; UPREGULATION;

ALLOXAN; ANIMALS; BACTEREMIA; CELL MOVEMENT; DIABETES MELLITUS, EXPERIMENTAL; DOWN-REGULATION; FEMALE; G-PROTEIN-COUPLED RECEPTOR KINASE 2; HISTAMINE; HISTAMINE H2 ANTAGONISTS; INFLAMMATION; MAST CELLS; MICE; MICE, INBRED BALB C; MICE, INBRED NOD; NEUTROPHILS; P-METHOXY-N-METHYLPHENETHYLAMINE; RECEPTORS, HISTAMINE H2; RECEPTORS, INTERLEUKIN-8B; SEPSIS; UP-REGULATION;

EID: 84880690488     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1202907     Document Type: Article

References (69)

1. Smitherman, K. O., and J. E. Peacock, Jr. 1995. Infectious emergencies in patients with diabetes mellitus. Med. Clin. North Am. 79: 53-77.
2. Joshi, N., G. M. Caputo, M. R. Weitekamp, and A. W. Karchmer. 1999. Infections in patients with diabetes mellitus. N. Engl. J. Med. 341: 1906-1912.
3. Wu, J. H., and C. G. Tsai. 2005. Infectivity of hepatic strain Klebsiella pneumoniae in diabetic mice. Exp. Biol. Med. (Maywood) 230: 757-761.
4. Ikejima, S., S. Sasaki, H. Sashinami, F. Mori, Y. Ogawa, T. Nakamura, Y. Abe, K. Wakabayashi, T. Suda, and A. Nakane. 2005. Impairment of host resistance to Listeria monocytogenes infection in liver of db/db and ob/ob mice. Diabetes 54: 182-189.
5. Puliti, M., F. Bistoni, G. Orefici, and L. Tissi. 2006. Exacerbation of group B streptococcal sepsis and arthritis in diabetic mice. Microbes Infect. 8: 2376-2383.
6. Martens, G. W., M. C. Arikan, J. Lee, F. Ren, D. Greiner, and H. Kornfeld. 2007. Tuberculosis susceptibility of diabetic mice. Am. J. Respir. Cell Mol. Biol. 37: 518-524.
7. Geerlings, S. E., and A. I. Hoepelman. 1999. Immune dysfunction in patients with diabetes mellitus (DM). FEMS Immunol. Med. Microbiol. 26: 259-265.
8. Geerlings, S. E., R. P. Stolk, M. J. Camps, P. M. Netten, T. J. Collet, and A. I. Hoepelman; Diabetes Women Asymptomatic Bacteriuria Utrecht Study Group. 2000. Risk factors for symptomatic urinary tract infection in women with diabetes. Diabetes Care 23: 1737-1741.
9. Delamaire, M., D. Maugendre, M. Moreno, M. C. Le Goff, H. Allannic, and B. Genetet. 1997. Impaired leucocyte functions in diabetic patients. Diabet Med. 14: 29-34.
10. Sannomiya, P., M. A. Oliveira, and Z. B. Fortes. 1997. Aminoguanidine and the prevention of leukocyte dysfunction in diabetes mellitus: a direct vital microscopic study. Br. J. Pharmacol. 122: 894-898.
11. Panneerselvam, S., and S. Govindasamy. 2003. Sodium molybdate improves the phagocytic function in alloxan-induced diabetic rats. Chem. Biol. Interact. 145: 159-163.
12. Alba-Loureiro, T. C., S. M. Hirabara, J. R. Mendonça, R. Curi, and T. C. Pithon-Curi. 2006. Diabetes causes marked changes in function and metabolism of rat neutrophils. J. Endocrinol. 188: 295-303.
13. Rios-Santos, F., J. C. Alves-Filho, F. O. Souto, F. Spiller, A. Freitas, C. M. Lotufo, M. B. Soares, R. R. Dos Santos, M. M. Teixeira, and F. Q. Cunha. 2007. Down-regulation of CXCR2 on neutrophils in severe sepsis is mediated by inducible nitric oxide synthase-derived nitric oxide. Am. J. Respir. Crit. Care Med. 175: 490-497.
14. Dal-Secco, D., T. M. Cunha, A. Freitas, J. C. Alves-Filho, F. O. Souto, S. Y. Fukada, R. Grespan, N. M. Alencar, A. F. Neto, M. A. Rossi, et al. 2008. Hydrogen sulfide augments neutrophil migration through enhancement of adhesion molecule expression and prevention of CXCR2 internalization: role of ATP-sensitive potassium channels. J. Immunol. 181: 4287-4298.
15. Ishii, M., K. Asano, H. Namkoong, S. Tasaka, K. Mizoguchi, T. Asami, H. Kamata, Y. Kimizuka, H. Fujiwara, Y. Funatsu, et al. 2012. CRTH2 is a critical regulator of neutrophil migration and resistance to polymicrobial sepsis. J. Immunol. 188: 5655-5664.
16. Alves-Filho, J. C., A. de Freitas, M. Russo, and F. Q. Cunha. 2006. Toll-like receptor 4 signaling leads to neutrophil migration impairment in polymicrobial sepsis. Crit. Care Med. 34: 461-470.
17. Alves-Filho, J. C., A. Freitas, F. O. Souto, F. Spiller, H. Paula-Neto, J. S. Silva, R. T. Gazzinelli, M. M. Teixeira, S. H. Ferreira, and F. Q. Cunha. 2009. Regulation of chemokine receptor by Toll-like receptor 2 is critical to neutrophil migration and resistance to polymicrobial sepsis. Proc. Natl. Acad. Sci. USA 106: 4018-4023.
18. Arraes, S. M., M. S. Freitas, S. V. da Silva, H. A. de Paula Neto, J. C. Alves-Filho, M. Auxiliadora Martins, A. Basile-Filho, B. M. Tavares-Murta, C. Barja-Fidalgo, and F. Q. Cunha. 2006. Impaired neutrophil chemotaxis in sepsis associates with GRK expression and inhibition of actin assembly and tyrosine phosphorylation. Blood 108: 2906-2913.
19. Marshall, J. S. 2004. Mast-cell responses to pathogens. Nat. Rev. Immunol. 4: 787-799.
20. Supajatura, V., H. Ushio, A. Nakao, S. Akira, K. Okumura, C. Ra, and H. Ogawa. 2002. Differential responses of mast cell Toll-like receptors 2 and 4 in allergy and innate immunity. J. Clin. Invest. 109: 1351-1359.
21. Malaviya, R., T. Ikeda, E. Ross, and S. N. Abraham. 1996. Mast cell modulation of neutrophil influx and bacterial clearance at sites of infection through TNFalpha. Nature 381: 77-80.
22. Echtenacher, B., D. N. Männel, and L. Hültner. 1996. Critical protective role of mast cells in a model of acute septic peritonitis. Nature 381: 75-77.
23. Carvalho, M., C. Benjamim, F. Santos, S. Ferreira, and F. Cunha. 2005. Effect of mast cells depletion on the failure of neutrophil migration during sepsis. Eur. J. Pharmacol. 525: 161-169.
24. Piliponsky, A. M., C. C. Chen, M. A. Grimbaldeston, S. M. Burns-Guydish, J. Hardy, J. Kalesnikoff, C. H. Contag, M. Tsai, and S. J. Galli. 2010. Mast cellderived TNF can exacerbate mortality during severe bacterial infections in C57BL/6-KitW-sh/W-sh mice. Am. J. Pathol. 176: 926-938.
25. Wescott, S., and M. Kaliner. 1983. Histamine H-1 binding site on human polymorphonuclear leukocytes. Inflammation 7: 291-300.
26. Gespach, C., and J. P. Abita. 1982. Human polymorphonuclear neutrophils. Pharmacological characterization of histamine receptors mediating the elevation of cyclic AMP. Mol. Pharmacol. 21: 78-85.
27. Bury, T. B., J. L. Corhay, and M. F. Radermecker. 1992. Histamine-induced inhibition of neutrophil chemotaxis and T-lymphocyte proliferation in man. Allergy 47: 624-629.
28. Seligmann, B. E., M. P. Fletcher, and J. I. Gallin. 1983. Histamine modulation of human neutrophil oxidative metabolism, locomotion, degranulation, and membrane potential changes. J. Immunol. 130: 1902-1909.
29. Burde, R., R. Seifert, A. Buschauer, and G. Schultz. 1989. Histamine inhibits activation of human neutrophils and HL-60 leukemic cells via H2-receptors. Naunyn Schmiedebergs Arch. Pharmacol. 340: 671-678.
30. Flamand, N., H. Plante, S. Picard, M. Laviolette, and P. Borgeat. 2004. Histamine-induced inhibition of leukotriene biosynthesis in human neutrophils: involvement of the H2 receptor and cAMP. Br. J. Pharmacol. 141: 552-561.
31. Benjamim, C. F., C. Canetti, F. Q. Cunha, S. L. Kunkel, and M. Peters-Golden. 2005. Opposing and hierarchical roles of leukotrienes in local innate immune versus vascular responses in a model of sepsis. J. Immunol. 174: 1616-1620.
32. Gill, D. S., M. A. Barradas, V. A. Fonseca, and P. Dandona. 1989. Plasma histamine concentrations are elevated in patients with diabetes mellitus and peripheral vascular disease. Metabolism 38: 243-247.
33. Hollis, T. M., J. A. Kern, N. A. Enea, and A. J. Cosgarea. 1985. Changes in plasma histamine concentration in the streptozotocin-diabetic rat. Exp. Mol. Pathol. 43: 90-96.
34. Oguri, S., K. Motegi, and Y. Endo. 2003. Augmented lipopolysaccharideinduction of the histamine-forming enzyme in streptozotocin-induced diabetic mice. Biochim. Biophys. Acta 1637: 83-90.
35. Clark, D. 1996. Guide for the Care and Use of Laboratory Animals. The National Academies Press, Washington, DC.
36. Wichterman, K. A., A. E. Baue, and I. H. Chaudry. 1980. Sepsis and septic shock -A review of laboratory models and a proposal. J. Surg. Res. 29: 189-201.
37. Alves-Filho, J. C., F. Sǒnego, F. O. Souto, A. Freitas, W. A. Verri, Jr., M. Auxiliadora-Martins, A. Basile-Filho, A. N. McKenzie, D. Xu, F. Q. Cunha, and F. Y. Liew. 2010. Interleukin-33 attenuates sepsis by enhancing neutrophil influx to the site of infection. Nat. Med. 16: 708-712.
38. Moreno, S. E., J. C. Alves-Filho, G. Bertozi, T. M. Alfaya, J. Théze, S. H. Ferreira, and B. B. Vargaftig. 2006. Systemic administration of interleukin-2 inhibits inflammatory neutrophil migration: role of nitric oxide. Br. J. Pharmacol. 148: 1060-1066.
39. im Walde, S. S., C. Dohle, P. Schott-Ohly, and H. Gleichmann. 2002. Molecular target structures in alloxan-induced diabetes in mice. Life Sci. 71: 1681-1694.
40. Ferry, X., S. Brehin, R. Kamel, and Y. Landry. 2002. G protein-dependent activation of mast cell by peptides and basic secretagogues. Peptides 23: 1507-1515.
41. Souto, F. O., J. C. Alves-Filho, W. M. Turato, M. Auxiliadora-Martins, A. Basile-Filho, and F. Q. Cunha. 2011. Essential role of CCR2 in neutrophil tissue infiltration and multiple organ dysfunction in sepsis. Am. J. Respir. Crit. Care Med. 183: 234-242.
42. Hirasawa, N., H. Ohtsu, T. Watanabe, and K. Ohuchi. 2002. Enhancement of neutrophil infiltration in histidine decarboxylase-deficient mice. Immunology 107: 217-221.
43. Hori, Y., Y. Nihei, Y. Kurokawa, A. Kuramasu, Y. Makabe-Kobayashi, T. Terui, H. Doi, S. Satomi, E. Sakurai, A. Nagy, et al. 2002. Accelerated clearance of Escherichia coli in experimental peritonitis of histamine-deficient mice. J. Immunol. 169: 1978-1983.
44. Kannan, Y., M. Tokunaga, M. Moriyama, H. Kinoshita, and Y. Nakamura. 2004. Beneficial effects of troglitazone on neutrophil dysfunction in multiple low-dose streptozotocin-induced diabetic mice. Clin. Exp. Immunol. 137: 263-271.
45. de Oliveira Martins, J., A. R. Meyer-Pflug, T. C. Alba-Loureiro, H. Melbostad, J. W. Costa da Cruz, R. Coimbra, R. Curi, and P. Sannomiya. 2006. Modulation of lipopolysaccharide-induced acute lung inflammation: role of insulin. Shock 25: 260-266.
46. Mlac, M., M. Melato, and G. Marin. 1975. Mast cells in the islets of Langerhans. A study of their behaviour in connection with diabetes and with insular amyloidosis. Virchows Arch. A Pathol. Anat. Histol. 365: 213-220.
47. Maiti, A. K., and S. R. Dasgupta. 1980. Mast cells in different tissues of alloxan diabetic rat. Indian J. Exp. Biol. 18: 1152-1155.
48. Hollmann, T. J., S. L. Mueller-Ortiz, M. C. Braun, and R. A. Wetsel. 2008. Disruption of the C5a receptor gene increases resistance to acute Gram-negative bacteremia and endotoxic shock: opposing roles of C3a and C5a. Mol. Immunol. 45: 1907-1915.
49. Baggiolini, M. 1998. Chemokines and leukocyte traffic. Nature 392: 565-568.
50. Mehrad, B., R. M. Strieter, T. A. Moore, W. C. Tsai, S. A. Lira, and T. J. Standiford. 1999. CXC chemokine receptor-2 ligands are necessary components of neutrophil-mediated host defense in invasive pulmonary aspergillosis. J. Immunol. 163: 6086-6094.
51. Tsai, W. C., R. M. Strieter, B. Mehrad, M. W. Newstead, X. Zeng, and T. J. Standiford. 2000. CXC chemokine receptor CXCR2 is essential for protective innate host response in murine Pseudomonas aeruginosa pneumonia. Infect. Immun. 68: 4289-4296.
52. Chishti, A. D., B. K. Shenton, J. A. Kirby, and S. V. Baudouin. 2004. Neutrophil chemotaxis and receptor expression in clinical septic shock. Intensive Care Med. 30: 605-611.
53. Gainetdinov, R. R., L. M. Bohn, J. K. Walker, S. A. Laporte, A. D. Macrae, M. G. Caron, R. J. Lefkowitz, and R. T. Premont. 1999. Muscarinic supersensitivity and impaired receptor desensitization in G protein-coupled receptor kinase 5-deficient mice. Neuron 24: 1029-1036.
54. Rios-Santos, F., C. F. Benjamim, D. Zavery, S. H. Ferreira, and Fde. Q. Cunha. 2003. A critical role of leukotriene B4 in neutrophil migration to infectious focus in cecal ligaton and puncture sepsis. Shock 19: 61-65.
55. Scott, M. J., W. G. Cheadle, J. J. Hoth, J. C. Peyton, K. Subbarao, W. H. Shao, and B. Haribabu. 2004. Leukotriene B4 receptor (BLT-1) modulates neutrophil influx into the peritoneum but not the lung and liver during surgically induced bacterial peritonitis in mice. Clin. Diagn. Lab. Immunol. 11: 936-941.
56. Matsukawa, A., C. M. Hogaboam, N. W. Lukacs, P. M. Lincoln, R. M. Strieter, and S. L. Kunkel. 1999. Endogenous monocyte chemoattractant protein-1 (MCP-1) protects mice in a model of acute septic peritonitis: cross-talk between MCP-1 and leukotriene B4. J. Immunol. 163: 6148-6154.
57. Houser, D. D., C. E. Arbesman, K. Ito, and K. Wicher. 1970. Cold urticaria. Immunologic studies. Am. J. Med. 49: 23-33.
58. Soter, N. A., S. I. Wasserman, and K. F. Austen. Cold urticaria: release into the circulation of histamine and eosinophil chemotactic factor of anaphylaxis during cold challenge. 1976. N. Engl. J. Med. 294: 687-690.
59. Wasserman, S. I., N. A. Soter, D. M. Center, and K. F. Austen. 1977. Cold urticaria. Recognition and characterization of a neutrophil chemotactic factor which appears in serum during experimental cold challenge. J. Clin. Invest. 60: 189-196.
60. Radermecker, M., and M. P. Maldague. 1981. Depression of neutrophil chemotaxis in atopic individuals. An H2 histamine receptor response. Int. Arch. Allergy Appl. Immunol. 65: 144-152.
61. Kubes, P., and S. Kanwar. 1994. Histamine induces leukocyte rolling in postcapillary venules. A P-selectin-mediated event. J. Immunol. 152: 3570-3577.
62. Yamaki, K., H. Thorlacius, X. Xie, L. Lindbom, P. Hedqvist, and J. Raud. 1998. Characteristics of histamine-induced leukocyte rolling in the undisturbed microcirculation of the rat mesentery. Br. J. Pharmacol. 123: 390-399.
63. Schaefer, U., V. Schmitz, A. Schneider, and E. Neugebauer. 1999. Histamine induced homologous and heterologous regulation of histamine receptor subtype mRNA expression in cultured endothelial cells. Shock 12: 309-315.
64. Anderson, R., A. Glover, and A. R. Rabson. 1977. The in vitro effects of histamine and metiamide on neutrophil motility and their relationship to intracellular cyclic nucleotide levels. J. Immunol. 118: 1690-1696.
65. Carlos, D., C. Fremond, A. Samarina, V. Vasseur, I. Maillet, S. G. Ramos, F. Erard, V. Quesniaux, H. Ohtsu, C. L. Silva, et al. 2009. Histamine plays an essential regulatory role in lung inflammation and protective immunity in the acute phase of Mycobacterium tuberculosis infection. Infect. Immun. 77: 5359-5368.
66. Sutherland, R. E., J. S. Olsen, A. McKinstry, S. A. Villalta, and P. J. Wolters. 2008. Mast cell IL-6 improves survival from Klebsiella pneumonia and sepsis by enhancing neutrophil killing. J. Immunol. 181: 5598-5605.
67. Thakurdas, S. M., E. Melicoff, L. Sansores-Garcia, D. C. Moreira, Y. Petrova, R. L. Stevens, and R. Adachi. 2007. The mast cell-restricted tryptase mMCP-6 has a critical immunoprotective role in bacterial infections. J. Biol. Chem. 282: 20809-20815.
68. Seeley, E. J., R. E. Sutherland, S. S. Kim, and P. J. Wolters. 2011. Systemic mast cell degranulation increases mortality during polymicrobial septic peritonitis in mice. J. Leukoc. Biol. 90: 591-597.
69. Anderson, M. S., and J. A. Bluestone. 2005. The NOD mouse: a model of immune dysregulation. Annu. Rev. Immunol. 23: 447-485.