Mast cell deficiency exacerbates inflammatory bowel symptoms in interleukin-10-deficient mice

World Journal of Gastroenterology

Volumn , Issue 27, 2014, Pages 9106-9115

  Zhang, Hanying ^a,b   Xue, Yansong ^a   Wang, Hui ^b   Huang, Yan ^b   Du, Min ^a   Yang, Qiyuan ^a   Zhu, Mei Jun ^a  

^a WASHINGTON STATE UNIVERSITY   (United States)

^b UNIVERSITY OF WYOMING   (United States)

Author keywords

Colitis; Inflammation; Inflammatory bowel disease; Interleukin 10; Mast cells; Mice

Indexed keywords

CLAUDIN 2; CLAUDIN 3; GAMMA INTERFERON; INTERLEUKIN 10; MYELOPEROXIDASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 1; SYNAPTOTAGMIN I; TUMOR NECROSIS FACTOR ALPHA; AUTACOID; IL10 PROTEIN, MOUSE; PEROXIDASE; STEM CELL FACTOR RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COLITIS; COLORIMETRY; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; GENE SEQUENCE; GLUCOSE TOLERANCE TEST; HISTOLOGY; IMMUNOBLOTTING; INFLAMMATORY BOWEL DISEASE; INTESTINE FLORA; INTESTINE MUCOSA PERMEABILITY; MALE; MAST CELL; MOUSE; MRNA EXPRESSION ASSAY; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STOMACH MUCOSA LESION; ANIMAL; C57BL MOUSE; COLON; DEFICIENCY; DISEASE MODEL; FECES; GENETICS; GENOTYPE; IMMUNOLOGY; INTESTINE MUCOSA; KNOCKOUT MOUSE; METABOLISM; MICROBIOLOGY; PATHOLOGY; PHENOTYPE; SIGNAL TRANSDUCTION; TH1 CELL; TIME;

ANIMALS; COLITIS; COLON; DISEASE MODELS, ANIMAL; FECES; GENOTYPE; INFLAMMATION MEDIATORS; INFLAMMATORY BOWEL DISEASES; INTERFERON-GAMMA; INTERLEUKIN-10; INTESTINAL MUCOSA; MALE; MAST CELLS; MICE, INBRED C57BL; MICE, KNOCKOUT; OXIDATIVE STRESS; PEROXIDASE; PHENOTYPE; PROTO-ONCOGENE PROTEINS C-KIT; SIGNAL TRANSDUCTION; TH1 CELLS; TIME FACTORS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84905380032     PISSN: 10079327     EISSN: 22192840     Source Type: Journal    
DOI: 10.3748/wjg.v20.i27.9106     Document Type: Article

References (47)

1. Yen D, Cheung J, Scheerens H, Poulet F, McClanahan T, McKenzie B, Kleinschek MA, Owyang A, Mattson J, Blumenschein W, Murphy E, Sathe M, Cua DJ, Kastelein RA, Rennick D. IL-23 is essential for T cell-mediated colitis and promotes inflammation via IL-17 and IL-6. J Clin Invest 2006; 116: 1310-1316 [PMID: 16670770 DOI: 10.1172/JCI21404]
2. Okayama Y, Kawakami T. Development, migration, and survival of mast cells. Immunol Res 2006; 34: 97-115 [PMID: 16760571]
3. Bischoff SC, Wedemeyer J, Herrmann A, Meier PN, Trautwein C, Cetin Y, Maschek H, Stolte M, Gebel M, Manns MP. Quantitative assessment of intestinal eosinophils and mast cells in inflammatory bowel disease. Histopathology 1996; 28: 1-13 [PMID: 8838115]
4. Jacob C, Yang PC, Darmoul D, Amadesi S, Saito T, Cottrell GS, Coelho AM, Singh P, Grady EF, Perdue M, Bunnett NW. Mast cell tryptase controls paracellular permeability of the intestine. Role of protease-activated receptor 2 and beta-arrestins. J Biol Chem 2005; 280: 31936-31948 [PMID: 16027150 DOI: 10.1074/jbc.M506338200]
5. McDermott JR, Bartram RE, Knight PA, Miller HR, Garrod DR, Grencis RK. Mast cells disrupt epithelial barrier function during enteric nematode infection. Proc Natl Acad Sci USA 2003; 100: 7761-7766 [PMID: 12796512 DOI: 10.1073/pnas.1231488100]
6. Konturek PC, Brzozowski T, Konturek SJ. Stress and the gut: pathophysiology, clinical consequences, diagnostic approach and treatment options. J Physiol Pharmacol 2011; 62: 591-599 [PMID: 22314561]
7. Bischoff SC. Physiological and pathophysiological functions of intestinal mast cells. Semin Immunopathol 2009; 31: 185-205 [PMID: 19533134 DOI: 10.1007/s00281-009-0165-4]
8. De Winter BY, van den Wijngaard RM, de Jonge WJ. Intestinal mast cells in gut inflammation and motility disturbances. Biochim Biophys Acta 2012; 1822: 66-73 [PMID: 21497195 DOI: 10.1016/j.bbadis.2011.03.016]
9. Stoyanova II, Gulubova MV. Mast cells and inflammatory mediators in chronic ulcerative colitis. Acta Histochem 2002; 104: 185-192 [PMID: 12086339]
10. Hamilton MJ, Sinnamon MJ, Lyng GD, Glickman JN, Wang X, Xing W, Krilis SA, Blumberg RS, Adachi R, Lee DM, Stevens RL. Essential role for mast cell tryptase in acute experimental colitis. Proc Natl Acad Sci USA 2011; 108: 290-295 [PMID: 21173247 DOI: 10.1073/pnas.1005758108]
11. Rijnierse A, Koster AS, Nijkamp FP, Kraneveld AD. Critical role for mast cells in the pathogenesis of 2,4-dinitrobenzene-induced murine colonic hypersensitivity reaction. J Immunol 2006; 176: 4375-4384 [PMID: 16547276]
12. Vicario M, Guilarte M, Alonso C, Yang P, Martínez C, Ramos L, Lobo B, González A, Guilà M, Pigrau M, Saperas E, Azpiroz F, Santos J. Chronological assessment of mast cell-mediated gut dysfunction and mucosal inflammation in a rat model of chronic psychosocial stress. Brain Behav Immun 2010; 24: 1166-1175 [PMID: 20600818 DOI: 10.1016/j.bbi.2010.06.002]
13. Söderholm JD, Yang PC, Ceponis P, Vohra A, Riddell R, Sherman PM, Perdue MH. Chronic stress induces mast cell-dependent bacterial adherence and initiates mucosal inflammation in rat intestine. Gastroenterology 2002; 123: 1099-1108 [PMID: 12360472]
14. Groschwitz KR, Ahrens R, Osterfeld H, Gurish MF, Han X, Abrink M, Finkelman FD, Pejler G, Hogan SP. Mast cells regulate homeostatic intestinal epithelial migration and barrier function by a chymase/Mcpt4-dependent mechanism. Proc Natl Acad Sci USA 2009; 106: 22381-22386 [PMID: 20018751 DOI: 10.1073/pnas.0906372106]
15. Chichlowski M, Westwood GS, Abraham SN, Hale LP. Role of mast cells in inflammatory bowel disease and inflammation-associated colorectal neoplasia in IL-10-deficient mice. PLoS One 2010; 5: e12220 [PMID: 20808919 DOI: 10.1371/journal.pone.0012220]
16. Cani PD, Possemiers S, Van de Wiele T, Guiot Y, Everard A, Rottier O, Geurts L, Naslain D, Neyrinck A, Lambert DM, Muccioli GG, Delzenne NM. Changes in gut microbiota control inflammation in obese mice through a mechanism involving GLP-2-driven improvement of gut permeability. Gut 2009; 58: 1091-1103 [PMID: 19240062 DOI: 10.1136/gut.2008.165886]
17. Zhu MJ, Han B, Tong J, Ma C, Kimzey JM, Underwood KR, Xiao Y, Hess BW, Ford SP, Nathanielsz PW, Du M. AMP-activated protein kinase signalling pathways are down regulated and skeletal muscle development impaired in fetuses of obese, over-nourished sheep. J Physiol 2008; 586: 2651-2664 [PMID: 18372306 DOI: 10.1113/jphysiol.2007.149633]
18. Burich A, Hershberg R, Waggie K, Zeng W, Brabb T, Westrich G, Viney JL, Maggio-Price L. Helicobacter-induced inflammatory bowel disease in IL-10- and T cell-deficient mice. Am J Physiol Gastrointest Liver Physiol 2001; 281: G764-G778 [PMID: 11518689]
19. Pellegrinet L, Rodilla V, Liu Z, Chen S, Koch U, Espinosa L, Kaestner KH, Kopan R, Lewis J, Radtke F. Dll1- and dll4-mediated notch signaling are required for homeostasis of intestinal stem cells. Gastroenterology 2011; 140: 1230-1240.e1-7 [PMID: 21238454 DOI: 10.1053/j.gastro.2011.01.005]
20. Tinnikov AA, Boonstra R. Colorimetric micro-determination of free fatty acids in plasma using microplate readers. Clin Chim Acta 1999; 281: 159-162 [PMID: 10217636]
21. Zhu MJ, Du M, Nathanielsz PW, Ford SP. Maternal obesity up-regulates inflammatory signaling pathways and enhances cytokine expression in the mid-gestation sheep placenta. Placenta 2010; 31: 387-391 [PMID: 20185176 DOI: 10.1016/j.placenta.2010.02.002]
22. Kamizato M, Nishida K, Masuda K, Takeo K, Yamamoto Y, Kawai T, Teshima-Kondo S, Tanahashi T, Rokutan K. Interleukin 10 inhibits interferon gamma- and tumor necrosis factor alpha-stimulated activation of NADPH oxidase 1 in human colonic epithelial cells and the mouse colon. J Gastroenterol 2009; 44: 1172-1184 [PMID: 19714290 DOI: 10.1007/s00535-009-0119-6]
23. Arrieta MC, Madsen K, Doyle J, Meddings J. Reducing small intestinal permeability attenuates colitis in the IL10 gene-deficient mouse. Gut 2009; 58: 41-48 [PMID: 18829978 DOI: 10.1136/gut.2008.150888]
24. Huffman DM, Barzilai N. Contribution of adipose tissue to health span and longevity. Interdiscip Top Gerontol 2010; 37: 1-19 [PMID: 20703052 DOI: 10.1159/000319991]
25. Cai C, Cao Z, Loughran PA, Kim S, Darwiche S, Korff S, Billiar TR. Mast cells play a critical role in the systemic inflammatory response and end-organ injury resulting from trauma. J Am Coll Surg 2011; 213: 604-615 [PMID: 21920785 DOI: 10.1016/j.jamcollsurg.2011.08.009]
26. Liu Z, Feng BS, Yang SB, Chen X, Su J, Yang PC. Interleukin (IL)-23 suppresses IL-10 in inflammatory bowel disease. J Biol Chem 2012; 287: 3591-3597 [PMID: 22158873 DOI: 10.1074/jbc.M111.304949]
27. Matharu KS, Mizoguchi E, Cotoner CA, Nguyen DD, Mingle B, Iweala OI, McBee ME, Stefka AT, Prioult G, Haigis KM, Bhan AK, Snapper SB, Murakami H, Schauer DB, Reinecker HC, Mizoguchi A, Nagler CR. Toll-like receptor 4-mediated regulation of spontaneous Helicobacter-dependent colitis in IL-10-deficient mice. Gastroenterology 2009; 137: 1380-1390. e1-3 [PMID: 19596011 DOI: 10.1053/j.gastro.2009.07.004]
28. Zhu H, Li YR. Oxidative stress and redox signaling mechanisms of inflammatory bowel disease: updated experimental and clinical evidence. Exp Biol Med (Maywood) 2012; 237: 474-480 [PMID: 22442342 DOI: 10.1258/ebm.2011.011358]
29. Turner JR, Rill BK, Carlson SL, Carnes D, Kerner R, Mrsny RJ, Madara JL. Physiological regulation of epithelial tight junctions is associated with myosin light-chain phosphorylation. Am J Physiol 1997; 273: C1378-C1385 [PMID: 9357784]
30. Koch S, Capaldo CT, Hilgarth RS, Fournier B, Parkos CA, Nusrat A. Protein kinase CK2 is a critical regulator of epithelial homeostasis in chronic intestinal inflammation. Mucosal Immunol 2013; 6: 136-145 [PMID: 22763408 DOI: 10.1038/mi.2012.57]
31. Alhouayek M, Lambert DM, Delzenne NM, Cani PD, Muccioli GG. Increasing endogenous 2-arachidonoylglycerol levels counteracts colitis and related systemic inflammation. FASEB J 2011; 25: 2711-2721 [PMID: 21551239 DOI: 10.1096/fj.10-176602]
32. Barbosa-da-Silva S, Fraulob-Aquino JC, Lopes JR, Mandarim-de-Lacerda CA, Aguila MB. Weight cycling enhances adipose tissue inflammatory responses in male mice. PLoS One 2012; 7: e39837 [PMID: 22848362 DOI: 10.1371/journal.pone.0039837]
33. Gutierrez DA, Puglisi MJ, Hasty AH. Impact of increased adipose tissue mass on inflammation, insulin resistance, and dyslipidemia. Curr Diab Rep 2009; 9: 26-32 [PMID: 19192421]
34. Lionetti L, Mollica MP, Lombardi A, Cavaliere G, Gifuni G, Barletta A. From chronic overnutrition to insulin resistance: the role of fat-storing capacity and inflammation. Nutr Metab Cardiovasc Dis 2009; 19: 146-152 [PMID: 19171470 DOI: 10.1016/j.numecd.2008.10.010]
35. Liu J, Divoux A, Sun J, Zhang J, Clément K, Glickman JN, Sukhova GK, Wolters PJ, Du J, Gorgun CZ, Doria A, Libby P, Blumberg RS, Kahn BB, Hotamisligil GS, Shi GP. Genetic deficiency and pharmacological stabilization of mast cells reduce diet-induced obesity and diabetes in mice. Nat Med 2009; 15: 940-945 [PMID: 19633655 DOI: 10.1038/nm.1994]
36. Tanaka A, Nomura Y, Matsuda A, Ohmori K, Matsuda H. Mast cells function as an alternative modulator of adipogenesis through 15-deoxy-delta-12, 14-prostaglandin J2. Am J Physiol Cell Physiol 2011; 301: C1360-C1367 [PMID: 21865589 DOI: 10.1152/ajpcell.00514.2010]
37. Altintas MM, Azad A, Nayer B, Contreras G, Zaias J, Faul C, Reiser J, Nayer A. Mast cells, macrophages, and crown-like structures distinguish subcutaneous from visceral fat in mice. J Lipid Res 2011; 52: 480-488 [PMID: 21148461 DOI: 10.1194/jlr.M011338]
38. Arsenault BJ, Beaumont EP, Després JP, Larose E. Mapping body fat distribution: a key step towards the identification of the vulnerable patient? Ann Med 2012; 44: 758-772 [PMID: 22149719 DOI: 10.3109/07853890.2011.605387]
39. Sartor RB. Microbial influences in inflammatory bowel diseases. Gastroenterology 2008; 134: 577-594 [PMID: 18242222 DOI: 10.1053/j.gastro.2007.11.059]
40. Albenberg LG, Lewis JD, Wu GD. Food and the gut microbiota in inflammatory bowel diseases: a critical connection. Curr Opin Gastroenterol 2012; 28: 314-320 [PMID: 22573192 DOI: 10.1097/MOG.0b013e328354586f]
41. Kang S, Denman SE, Morrison M, Yu Z, Dore J, Leclerc M, McSweeney CS. Dysbiosis of fecal microbiota in Crohn's disease patients as revealed by a custom phylogenetic microarray. Inflamm Bowel Dis 2010; 16: 2034-2042 [PMID: 20848492 DOI: 10.1002/ibd.21319]
42. Wang H, Xue Y, Zhang H, Huang Y, Yang G, Du M, Zhu MJ. Dietary grape seed extract ameliorates symptoms of inflammatory bowel disease in IL10-deficient mice. Mol Nutr Food Res 2013; 57: 2253-2257 [PMID: 23963706 DOI: 10.1002/mnfr.201300146]
43. Cani PD, Bibiloni R, Knauf C, Waget A, Neyrinck AM, Delzenne NM, Burcelin R. Changes in gut microbiota control metabolic endotoxemia-induced inflammation in high-fat diet-induced obesity and diabetes in mice. Diabetes 2008; 57: 1470-1481 [PMID: 18305141 DOI: 10.2337/db07-1403]
44. Barman M, Unold D, Shifley K, Amir E, Hung K, Bos N, Salzman N. Enteric salmonellosis disrupts the microbial ecology of the murine gastrointestinal tract. Infect Immun 2008; 76: 907-915 [PMID: 18160481 DOI: 10.1128/IAI.01432-07]
45. Matsuda K, Tsuji H, Asahara T, Kado Y, Nomoto K. Sensitive quantitative detection of commensal bacteria by rRNA-targeted reverse transcription-PCR. Appl Environ Microbiol 2007; 73: 32-39 [PMID: 17071791 DOI: 10.1128/AEM.01224-06]
46. Amann RI, Binder BJ, Olson RJ, Chisholm SW, Devereux R, Stahl DA. Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Appl Environ Microbiol 1990; 56: 1919-1925 [PMID: 2200342]
47. Bartosch S, Fite A, Macfarlane GT, McMurdo ME. Characterization of bacterial communities in feces from healthy elderly volunteers and hospitalized elderly patients by using real-time PCR and effects of antibiotic treatment on the fecal microbiota. Appl Environ Microbiol 2004; 70: 3575-3581 [PMID: 15184159 DOI: 10.1128/AEM.70.6.3575-3581.2004]