Carboxypeptidase E modulates intestinal immune homeostasis and protects against experimental colitis in mice

PLoS ONE

Volumn 9, Issue 7, 2014, Pages

  Bär, Florian ^a,b   Föh, Bandik ^a   Pagel, René ^a   Schröder, Torsten ^a   Schlichting, Heidi ^a   Hirose, Misa ^a   Lemcke, Susanne ^a   Klinger, Antje ^b   König, Peter ^b   Karsten, Christian M ^b   Büning, Jürgen ^a   Lehnert, Hendrik ^a   Fellermann, Klaus ^a   Ibrahim, Saleh M ^a   Sina, Christian ^a  

^a UNIVERSITY HOSPITAL SCHLESWIG HOLSTEIN   (Germany)

^b UNIVERSITY OF LÜBECK   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOXYPEPTIDASE H; CHEMOKINE; INTERLEUKIN 6; NEUROPEPTIDE Y; NEUTROPHIL CHEMOKINE KC; PEPTIDE YY; UNCLASSIFIED DRUG; CHROMOGRANIN B; DEXTRAN SULFATE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL LINE; CHEMOTAXIS; COLON; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DEXTRAN SODIUM SULFATE-INDUCED COLITIS; ENTEROENDOCRINE CELL; ENZYME ACTIVITY; ENZYME DEFICIENCY; ILEUM; IMMUNE DEFICIENCY; IMMUNITY; IMMUNOMODULATION; INTESTINAL IMMUNE HOMEOSTASIS; INTESTINE CRYPT; INTESTINE MUCOSA; MACROPHAGE MIGRATION; MODE K CELL LINE; MOUSE; MOUSE MODEL; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PROCESSING; WILD TYPE; ANIMAL; BONE MARROW CELL; C57BL MOUSE; CELL CULTURE; CELL MOTION; CHEMICALLY INDUCED; COLITIS; ENZYMOLOGY; HOMEOSTASIS; HUMAN; IMMUNOLOGY; INFLAMMATORY BOWEL DISEASE; METABOLISM; PHYSIOLOGY; PROTEIN TRANSPORT;

ANIMALS; CARBOXYPEPTIDASE H; CELL MOVEMENT; CELLS, CULTURED; CHROMOGRANIN B; COLITIS; COLON; DEXTRAN SULFATE; HOMEOSTASIS; HUMANS; INFLAMMATORY BOWEL DISEASES; INTESTINAL MUCOSA; MICE, INBRED C57BL; MYELOID CELLS; NEUROPEPTIDE Y; PROTEIN TRANSPORT;

EID: 84904687041     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0102347     Document Type: Article

References (42)

1. Kaser A, Zeissig S, Blumberg RS (2010) Inflammatory bowel disease. Annu Rev Immunol 28: 573-621.
2. McGuckin MA, Eri R, Simms LA, Florin TH, Radford-Smith G (2009) Intestinal barrier dysfunction in inflammatory bowel diseases. Inflamm Bowel Dis 15(1): 100-113.
3. Turner JR (2009) Intestinal mucosal barrier function in health and disease. Nat Rev Immunol 9(11): 799-809.
4. Artis D (2008) Epithelial-cell recognition of commensal bacteria and maintenance of immune homeostasis in the gut. Nat Rev Immunol 8(6): 411-420.
5. Stead RH, Bienenstock J, Stanisz AM (1987) Neuropeptide regulation of mucosal immunity. Immunol Rev 100: 333-359. (Pubitemid 18017647)
6. Chandrasekharan B, Nezami BG, Srinivasan S (2013) Emerging neuropeptide targets in inflammation: NPY and VIP. Am J Physiol Gastrointest Liver Physiol 304(11): 949-957.
7. Koch TR, Roddy DR, Carney JA, Go VL (1988) Peptide YY concentrations in normal ileum and colon and in idiopathic inflammatory bowel disease. Dig Dis Sci 33(10): 1322-1328.
8. Mazumdar S, Das KM (1992) Immunocytochemical localization of vasoactive intestinal peptide and substance P in the colon from normal subjects and patients with inflammatory bowel disease. Am J Gastroenterol 87(2): 176-181.
9. Tari A, Teshima H, Sumii K, Haruma K, Ohgoshi H, et al. (1988) Peptide YY abnormalities in patients with ulcerative colitis. Jpn J Med 27(1): 49-55.
10. Watanabe T, Kubota Y, Sawada T, Muto T (1992) Distribution and quantification of somatostatin in inflammatory disease. Dis Colon Rectum 35(5): 488-494.
11. Moran GW, Pennock J, McLaughlin JT (2012) Enteroendocrine cells in terminal ileal Crohn's disease. J Crohns Colitis 6(9): Available: http://www.sciencedirect.com/science/article/pii/S1873994612000190. Accessed 2013 Nov 18.
12. Sakiyama T, Fujita H, Tsubouchi H (2008) Autoantibodies against ubiquitination factor E4A (UBE4A) are associated with severity of Crohn's disease. Inflamm Bowel Dis 14(3): 310-317. (Pubitemid 351441318)
13. Rioux JD, Xavier RJ, Taylor KD, Silverberg MS, Goyette P, et al. (2007) Genome-wide association study identifies new susceptibility loci for Crohn disease and implicates autophagy in disease pathogenesis. Nat Genet 39(5): 596-604. (Pubitemid 46676115)
14. Hougaard DM, Larsson LI (2004) Carboxypeptidase E in rat antropyloric mucosa: distribution in progenitor and mature endocrine cell types. Histochem Cell Biol 121(1): 55-61. (Pubitemid 38200080)
15. Sina C, Arlt A, Gavrilova O, Midtling E, Kruse ML, et al. (2010) Ablation of gly96/immediate early gene-X1 (gly96/iex-1) aggravates DSS-induced colitis in mice: role for gly96/iex-1 in the regulation of NF-kappaB. Inflamm Bowel Dis 16(2): 320-331.
16. Siegmund B, Lehr HA, Fantuzzi G, Dinarello CA (2001) IL-1-converting enzyme (caspase-1) in intestinal inflammation. Proc Natl Acad Sci USA 98(23): 13249-13254. (Pubitemid 33051348)
17. Becker C, Fantini MC, Neurath MF (2006) High resolution colonoscopy in live mice. Nat Protoc 1(6): 2900-2904.
18. Brubaker PL, Drucker DJ, Asa SL, Greenberg GR (1991) Regulation of peptide-YY synthesis and secretion in fetal rat intestinal cultures. Endocrinology 129(6): 3351-3358.
19. Vidal K, Grosjean I, Evillard JP, Gespach C, Kaiserlian D (1993) Immortalization of mouse intestinal epithelial cells by the SV40-large T gene. Phenotypic and immune characterization of the MODE-K cell line. J Immunol Methods 166(1): 63-73.
20. Karsten CM, Pandey MK, Figge J, Kilchenstein R, Taylor PR, et al. (2012) Anti-inflammatory activity of IgG1 mediated by Fc galactosylation and association of FccRIIB and dectin-1. Nat Med 18(9): 1401-1406.
21. Brakch N, Rist B, Beck-Sickinger AG, Goenaga J, Wittek R, et al. (1997) Role of prohormone convertases in pro-neuropeptide Y processing: coexpression and in vitro kinetic investigations. Biochemistry 36(51): 16309-16320. (Pubitemid 28065047)
22. Funkelstein L, Toneff T, Hwang SR, Reinheckel T, Peters C, et al. (2008) Cathepsin L participates in the production of neuropeptide Y in secretory vesicles, demonstrated by protease gene knockout and expression. J Neurochem 106(1): 384-391. (Pubitemid 351840225)
23. Paquet L, Massie B, Mains RE (1996) Proneuropeptide Y processing in large dense-core vesicles: manipulation of prohormone convertase expression in sympathetic neurons using adenoviruses. J Neurosci 16(3): 964-973. (Pubitemid 26140852)
24. Giusti-Paiva A, Elias LL, Antunes-Rodrigues J (2005) Inhibitory effect of gaseous neuromodulators in vasopressin and oxytocin release induced by endotoxin in rats. Neurosci Lett 381(3): 320-324. (Pubitemid 40719179)
25. Singer K, Morris DL, Oatmen KE, Wang T, DelProposto J, et al. (2013) Neuropeptide Y is produced by adipose tissue macrophages and regulates obesity-induced inflammation. PLoS One 8(3): Available: http://www.plosone.org/ article/info%3Adoi%2F10.1371%1372Fjournal.pone.0057929;jsessionid= 0059088ED0057929AE0057924EE0057025E0057314E0059541AC0057926E0057073D. Accessed 2013 Nov 05.
26. Worthington JJ, Samuelson LC, Grencis RK, McLaughlin JT (2013) Adaptive immunity alters distinct host feeding pathways during nematode induced inflammation, a novel mechanism in parasite expulsion. PLoS Pathog 9: Available: http://www.plospathogens.org/article/info%3Adoi%2F10.1371%1372Fjournal.ppat. 1003122. Accessed 2013 Nov 10.
27. Dickerson C, Undem B, Bullock B, Winchurch RA (1998) Neuropeptide regulation of proinflammatory cytokine responses. J Leukoc Biol 63(5): 602-605. (Pubitemid 28193773)
28. Levite M, Chowers Y (2001) Nerve-driven immunity: neuropeptides regulate cytokine secretion of T cells and intestinal epithelial cells in a direct, powerful and contextual manner. Ann Oncol (Suppl. 2): 19-25.
29. Lotz M, Vaughan JH, Carson DA (1988) Effect of neuropeptides on production of inflammatory cytokines by human monocytes. Science 241(4870): 1218-1221.
30. Krueger J, Ray A, Tamm I, Sehgal PB (1991) Expression and function of interleukin-6 in epithelial cells. J Cell Biochem 45(4): 327-334.
31. Parikh AA, Salzman AL, Kane CD, Fischer JE, Hasselgren PO (1997) IL-6 production in human intestinal epithelial cells following stimulation with IL-1 beta is associated with activation of the transcription factor NF-kappa B. J Surg Res 69(1): 139-144. (Pubitemid 27265840)
32. Song F, Ito K, Denning TL, Kuninger D, Papaconstantinou J, et al. (1999) Expression of the neutrophil chemokine KC in the colon of mice with enterocolitis and by intestinal epithelial cell lines: effects of flora and proinflammatory cytokines. J Immunol 162(4): 2275-2280. (Pubitemid 29288851)
33. Bures EJ, Courchesne PL, Douglass J, Chen K, Davis MT, et al. (2001) Identification of incompletely processed potential carboxypeptidase E substrates from CpEfat/CpEfat mice. Proteomics 1(1): 79-92. (Pubitemid 33791875)
34. Cool DR, Loh YP (1998) Carboxypeptidase E is a sorting receptor for prohormones: Binding and kinetic studies. Mol Cell Endocrinol 139: 7-13. (Pubitemid 28340053)
35. Cool DR, Normant E, Shen F, Chen HC, Pannell L, et al. (1997) Carboxypeptidase E is a regulated secretory pathway sorting receptor: genetic obliteration leads to endocrine disorders in Cpe(fat) mice. Cell 88(1): 73-83. (Pubitemid 27180332)
36. Selleri S, Palazzo M, Deola S, Wang E, Balsari A, et al. (2008) Induction of proinflammatory programs in enteroendocrine cells by the Toll-like receptor agonists flagellin and bacterial LPS. Int Immunol 20(8): 961-970.
37. Wheway J, Mackay CR, Newton RA, Sainsbury A, Boey D, et al. (2005) A fundamental bimodal role for neuropeptide Y1 receptor in the immune system. J Exp Med 202(11): 1527-1538. (Pubitemid 41746599)
38. Curfs JH, Meis JF, Hoogkamp-Korstanje JA (1997) A primer on cytokines: sources, receptors, effects, and inducers. Clin Microbiol Rev 10(4): 742-780.
39. Eckmann L, Kagnoff MF, Fierer J (1993) Epithelial cells secrete the chemokine interleukin-8 in response to bacterial entry. Infect Immun 61(11): 4569-4574. (Pubitemid 23320507)
40. Andres PG, Beck PL, Mizoguchi E, Mizoguchi A, Bhan AK, et al. (2000) Mice with a selective deletion of the CC chemokine receptors 5 or 2 are protected from dextran sodium sulfate-mediated colitis: lack of CC chemokine receptor 5 expression results in a NK1.1+ lymphocyte-associated Th2-type immune response in the intestine. J Immunol 164(12): 6303-6312. (Pubitemid 30408811)
41. Kim TW, Seo JN, Suh YH, Park HJ, Kim JH, et al. (2006) Involvement of lymphocytes in dextran sulfate sodium-induced experimental colitis. World J Gastroenterol 12(2): 302-305. (Pubitemid 43336932)
42. Sina C, Gavrilova O, Förster M, Till A, Derer S, et al. (2009) G protein-coupled receptor 43 is essential for neutrophil recruitment during intestinal inflammation. J Immunol 183(11): 7514-7522.