CD38 is expressed on inflammatory cells of the intestine and promotes intestinal inflammation

PLoS ONE

Volumn 10, Issue 5, 2015, Pages

  Schneider, Michael ^a   Schumacher, Valéa ^a   Lischke, Timo ^a   Lücke, Karsten ^a   Meyer Schwesinger, Catherine ^a   Velden, Joachim ^a   Koch Nolte, Friedrich ^a   Mittrücker, Hans Willi ^a  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CD38 ANTIGEN; CXCL1 CHEMOKINE; CXCL2 CHEMOKINE; DEXTRAN SULFATE; INTERLEUKIN 10; INTERLEUKIN 23P19; INTERLEUKIN 6; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTICLE; BONE MARROW CELL; CELL INFILTRATION; COLITIS; COLON MUCOSA; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE MODEL; DISEASE SEVERITY; GRANULOCYTE; HISTOPATHOLOGY; IMMUNOCOMPETENT CELL; INFLAMMATORY CELL; MACROPHAGE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; WILD TYPE; ANIMAL; C57BL MOUSE; CHEMICALLY INDUCED; COLON; CYTOLOGY; GENETICS; INTESTINE; INTESTINE MUCOSA; KNOCKOUT MOUSE; LEUKOCYTE; METABOLISM;

ANIMALIA; MUS;

ANIMALS; ANTIGENS, CD38; COLITIS; COLON; DEXTRAN SULFATE; DISEASE MODELS, ANIMAL; INTESTINAL MUCOSA; INTESTINES; LEUKOCYTES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT;

EID: 84929207298     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0126007     Document Type: Article

References (43)

1. Lund FE. (2006) Signaling properties of CD38 in the mouse immune system: enzyme-dependent andindependent roles in immunity. Mol Med 12: 328-333. PMID: 17380200
2. Malavasi F, Deaglio S, Funaro A, Ferrero E, Horenstein AL, Ortolan E, et al. (2008) Evolution and function of the ADP ribosyl cyclase/CD38 gene family in physiology and pathology. Physiol Rev 88: 841-886 doi: 10.1152/physrev.00035.2007 PMID: 18626062
3. Zhao YJ, Lam CM, Lee HC. (2012) The membrane-bound enzyme CD38 exists in two opposing orientations. Sci Signal 5:ra67.
4. Howard M, Grimaldi JC, Bazan JF, Lund FE, Santos-Argumedo L, Parkhouse RM, et al. (1993) Formation and hydrolysis of cyclic ADP-ribose catalyzed by lymphocyte antigen CD38. Science 262: 1056-1059. PMID: 8235624
5. Zocchi E, Franco L, Guida L, Benatti U, Bargellesi A, Malavasi F, et al. (1993) A single protein immunologically identified as CD38 displays NAD+ glycohydrolase, ADP-ribosyl cyclase and cyclic ADP-ribose hydrolase activities at the outer surface of human erythrocytes. Biochem Biophys Res Commun 196: 1459-1465. PMID: 8250903
6. Grahnert A, Grahnert A, Klein C, Schilling E, Wehrhahn J, Hauschildt S. (2011) NAD +: a modulator of immune functions. Innate Immun 17: 212-233. doi: 10.1177/1753425910361989 PMID: 20388721
7. Ernst IM, Fliegert R, Guse AH. 2013. Adenine dinucleotide second messengers and T-lymphocyte calcium signaling. Front Immunol 4: 259. doi: 10.3389/fimmu.2013.00259 PMID: 24009611
8. Partida-Sánchez S, Cockayne DA, Monard S, Jacobson EL, Oppenheimer N, Garvy B, et al. (2001) Cyclic ADP-ribose production by CD38 regulates intracellular calcium release, extracellular calcium influx and chemotaxis in neutrophils and is required for bacterial clearance in vivo. Nat Med 7: 1209-1216. PMID: 11689885
9. Partida-Sánchez S, Goodrich S, Kusser K, Oppenheimer N, Randall TD, Lund FE. (2004) Regulation of dendritic cell trafficking by the ADP-ribosyl cyclase CD38: impact on the development of humoral immunity. Immunity 20: 279-291. PMID: 15030772
10. Partida-Sánchez S, Iribarren P, Moreno-García ME, Gao JL, Murphy PM, Oppenheimer N, et al. (2004) Chemotaxis and calcium responses of phagocytes to formyl peptide receptor ligands is differentially regulated by cyclic ADP ribose. J Immunol 172: 1896-1906. PMID: 14734775
11. Partida-Sánchez S, Randall TD, Lund FE. (2003) Innate immunity is regulated by CD38, an ecto-enzyme with ADP-ribosyl cyclase activity. Microbes Infect 5: 49-58. PMID: 12593973
12. Lischke T, Heesch K, Schumacher V, Schneider M, Haag F, Koch-Nolte F, et al. (2013) CD38 controls the innate immune response against Listeria monocytogenes. Infect Immun 81: 4091-4099. doi: 10.1128/IAI.00340-13 PMID: 23980105
13. Longhi MS, Robson SC, Bernstein SH, Serra S, Deaglio S. (2013) Biological functions of ecto-enzymes in regulating extracellular adenosine levels in neoplastic and inflammatory disease states. J Mol Med 91: 165-172. doi: 10.1007/s00109-012-0991-z PMID: 23292173
14. Adriouch S, Haag F, Boyer O, Seman M, Koch-Nolte F. (2012) Extracellular NAD(+): a danger signal hindering regulatory T cells. Microbes Infect 14: 1284-1292. doi: 10.1016/j.micinf.2012.05.011 PMID: 22634347
15. Lischke T, Schumacher V, Wesolowski J, Hurwitz R, Haag F, Koch-Nolte F, et al. (2013) CD8β ADP-ribosylation affects CD8+ T-cell function. Eur J Immunol 43: 1828-1838. doi: 10.1002/eji.201243231 PMID: 23575529
16. Seman M, Adriouch S, Scheuplein F, Krebs C, Freese D, Glowacki G, et al. (2003) NAD-induced T cell death: ADP-ribosylation of cell surface proteins by ART2 activates the cytolytic P2X7 purinoceptor. Immunity 19: 571-582. PMID: 14563321
17. Viegas MS, do Carmo A, Silva T, Seco F, Serra V, Lacerda M, et al. (2007) CD38 plays a role in effective containment of mycobacteria within granulomata and polarization of Th1 immune responses against Mycobacterium avium. Microbes Infect 9: 847-854. PMID: 17533152
18. Estrada-Figueroa LA, Ramírez-Jiménez Y, Osorio-Trujillo C, Shibayama M, Navarro-García F, García-Tovar C, et al. (2011) Absence of CD38 delays arrival of neutrophils to the liver and innate immune response development during hepatic amoebiasis by Entamoeba histolytica. Parasite Immunol 33: 661-668. doi: 10.1111/j.1365-3024.2011.01333.x PMID: 21919917
19. Cervantes-Sandoval I, Serrano-Luna JdeJ, García-Latorre E, Tsutsumi V, Shibayama M. (2008) Characterization of brain inflammation during primary amoebic meningoencephalitis. Parasitol Int 57: 307-313. doi: 10.1016/j.parint.2008.01.006 PMID: 18374627
20. Postigo J, Iglesias M, Cerezo-Wallis D, Rosal-Vela A, García-Rodríguez S, Zubiaur M, et al. (2012) Mice deficient in CD38 develop an attenuated form of collagen type II-induced arthritis. PLoS One 7: e33534. doi: 10.1371/journal.pone.0033534 PMID: 22438945
21. Choe CU, Lardong K, Gelderblom M, Ludewig P, Leypoldt F, Koch-Nolte F, et al. (2011) CD38 exacerbates focal cytokine production, postischemic inflammation and brain injury after focal cerebral ischemia. PLoS One 6: e19046. doi: 10.1371/journal.pone.0019046 PMID: 21625615
22. Gally F, Hartney JM, Janssen WJ, Perraud AL. (2009) CD38 plays a dual role in allergen-induced airway hyperresponsiveness. Am J Respir Cell Mol Biol 40: 433-442. doi: 10.1165/rcmb.2007-0392OC PMID: 18931329
23. Chen YG, Chen J, Osborne MA, Chapman HD, Besra GS, Porcelli SA, et al. (2006) CD38 is required for the peripheral survival of immunotolerogenic CD4+ invariant NK T cells in nonobese diabetic mice. J Immunol 177: 2939-2947. PMID: 16920929
24. Chen J, Chen YG, Reifsnyder PC, Schott WH, Lee CH, Osborne M, et al. (2006) Targeted disruption of CD38 accelerates autoimmune diabetes in NOD/Lt mice by enhancing autoimmunity in an ADP-ribosyltransferase 2-dependent fashion. J Immunol 176: 4590-4599. PMID: 16585549
25. Cockayne DA, Muchamuel T, Grimaldi JC, Muller-Steffner H, Randall TD, Lund FE, et al. (1998) Mice deficient for the ecto-nicotinamide adenine dinucleotide glycohydrolase CD38 exhibit altered humoral immune responses. Blood 92: 1324-1333. PMID: 9694721
26. Cooper HS, Murthy SN, Shah RS, Sedergran DJ. (1993) Clinicopathologic study of dextran sulfate sodium experimental murine colitis. Lab Invest 69: 238-249. PMID: 8350599
27. Castaneda FE, Walia B, Vijay-Kumar M, Patel NR, Roser S, Kolachala VL, et al. (2005) Targeted deletion of metalloproteinase 9 attenuates experimental colitis in mice: central role of epithelial-derived MMP. Gastroenterology 129: 1991-2008. PMID: 16344067
28. Meyer-Schwesinger C, Dehde S, Klug P, Becker JU, Mathey S, Arefi K, et al. (2011) Nephrotic syndrome and subepithelial deposits in a mouse model of immune-mediated anti-podocyte glomerulonephritis. J Immunol 187: 3218-3229. doi: 10.4049/jimmunol.1003451 PMID: 21844386
29. Lo Buono N, Morone S, Giacomino A, Parrotta R, Ferrero E, Malavasi F, et al. (2014) CD157 at the intersection between leukocyte trafficking and epithelial ovarian cancer invasion. Front Biosci (Landmark Ed) 19: 366-378. PMID: 24389190
30. Mora JR, Bono MR, Manjunath N, Weninger W, Cavanagh LL, Rosemblatt M, et al. (2003) Selective imprinting of gut-homing T cells by Peyer's patch dendritic cells. Nature 424: 88-93. PMID: 12840763
31. Iwata M, Hirakiyama A, Eshima Y, Kagechika H, Kato C, Song SY. (2004) Retinoic acid imprints guthoming specificity on T cells. Immunity 21: 527-538. PMID: 15485630
32. Schulz O, Jaensson E, Persson EK, Liu X, Worbs T, Agace WW, et al. (2009) Intestinal CD103+, but not CX3CR1+, antigen sampling cells migrate in lymph and serve classical dendritic cell functions. J Exp Med 206: 3101-3114. doi: 10.1084/jem.20091925 PMID: 20008524
33. du Pré MF, van Berkel LA, Ráki M, van Leeuwen MA, de Ruiter LF, Broere F, et al. (2011) CD62L(neg) CD38+ expression on circulating CD4+ T cells identifies mucosally differentiated cells in protein fed mice and in human celiac disease patients and controls. Am J Gastroenterol 106: 1147-1159. doi: 10. 1038/ajg.2011.24 PMID: 21386831
34. Kontani K, Nishina H, Ohoka Y, Takahashi K, Katada T. (1993) NAD glycohydrolase specifically induced by retinoic acid in human leukemic HL-60 cells. Identification of the NAD glycohydrolase as leukocyte cell surface antigen CD38. J Biol Chem 268: 16895-16898. PMID: 8394323
35. Drach J, Zhao S, Malavasi F, Mehta K. (1993) Rapid induction of CD38 antigen on myeloid leukemia cells by all trans-retinoic acid. Biochem Biophys Res Commun 195: 545-550. PMID: 7690555
36. Deaglio S, Mallone R, Baj G, Donati D, Giraudo G, Corno F, et al. (2001) Human CD38 and its ligand CD31 define a unique lamina propria T lymphocyte signaling pathway. FASEB J 15: 580-582. PMID: 11259373
37. McNagny KM, Cazenave PA, Cooper MD. (1988) BP3 alloantigen. A cell surface glycoprotein that marks early B lineage cells and mature myeloid lineage cells in mice. J Immunol 141: 2551-2556. PMID: 3262662
38. Yilmaz ÖH, Katajisto P, Lamming DW, Gültekin Y, Bauer-Rowe KE, Sengupta S, et al. (2012) mTORC1 in the Paneth cell niche couples intestinal stem-cell function to calorie intake. Nature 486:490-495. doi: 10.1038/nature11163 PMID: 22722868
39. Hussain AM, Lee HC, Chang CF. (1998) Functional expression of secreted mouse BST-1 in yeast. Protein Expr Purif 12: 133-137. PMID: 9473467
40. Yamamoto S, Shimizu S, Kiyonaka S, Takahashi N, Wajima T, Hara Y, et al. (2008) TRPM2-mediated Ca2+influx induces chemokine production in monocytes that aggravates inflammatory neutrophil infiltration. Nat Med 14: 738-747. doi: 10.1038/nm1758 PMID: 18542050
41. Heiss K, Jänner N, Mähnß B, Schumacher V, Koch-Nolte F, Haag F, et al. (2008) High sensitivity of intestinal CD8+ T cells to nucleotides indicates P2X7 as a regulator for intestinal T cell responses. J Immunol 181: 3861-3869. PMID: 18768840
42. Hubert S, Rissiek B, Klages K, Huehn J, Sparwasser T, Haag F, et al. (2010) Extracellular NAD+ shapes the Foxp3+ regulatory T cell compartment through the ART2-P2X7 pathway. J Exp Med 207: 2561-2568. doi: 10.1084/jem.20091154 PMID: 20975043
43. Kahl S, Nissen M, Girisch R, Duffy T, Leiter EH, Haag F, et al. (2000) Metalloprotease-mediated shedding of enzymatically active mouse ecto-ADP-ribosyltransferase ART2.2 upon T cell activation. J Immunol 165: 4463-4469. PMID: 11035085