Activation of intestinal tuft cell-expressed sucnr1 triggers type 2 immunity in the mouse small intestine

Proceedings of the National Academy of Sciences of the United States of America

Volumn 115, Issue 21, 2018, Pages 5552-5557

  Lei, Weiwei ^a   Ren, Wenwen ^a   Ohmoto, Makoto ^a   Urban, Joseph F ^b   Matsumoto, Ichiro ^a   Margolskee, Robert F ^a   Jiang, Peihua ^a  

^a MONELL CHEMICAL SENSES CENTER   (United States)

^b BELTSVILLE HUMAN NUTRITION RESEARCH CENTER   (United States)

Author keywords

Gustducin; Sucnr1; Trpm5; Tuft cells; Type 2 immunity

Indexed keywords

CELL MARKER; GUSTDUCIN; MACROGOL; RECEPTOR; STREPTOMYCIN; SUCCINATE RECEPTOR 1; SUCCINIC ACID; TRANSIENT RECEPTOR POTENTIAL CHANNEL M5; UNCLASSIFIED DRUG; G PROTEIN COUPLED RECEPTOR; GPR91 PROTEIN, MOUSE;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CELL EXPANSION; CELL HYPERPLASIA; CONTROLLED STUDY; FEMALE; GOBLET CELL; INFECTIOUS AGENT; INTESTINE CELL; INTESTINE TUFT CELL; MALE; MICROORGANISM DETECTION; MOUSE; MUCOSAL IMMUNITY; NEMATODIASIS; NIPPOSTRONGYLUS BRASILIENSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SECONDARY IMMUNE RESPONSE; SMALL INTESTINE; ANIMAL; C57BL MOUSE; CELL CULTURE; CELL PROLIFERATION; DRUG EFFECT; EPITHELIUM CELL; IMMUNOLOGY; KNOCKOUT MOUSE; METABOLISM; MICROFLORA; NIPPOSTRONGYLUS; PARASITOLOGY; PATHOLOGY; PHYSIOLOGY; STRONGYLE INFECTION;

ANIMALS; CELL PROLIFERATION; CELLS, CULTURED; EPITHELIAL CELLS; FEMALE; GOBLET CELLS; IMMUNITY, MUCOSAL; INTESTINE, SMALL; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROBIOTA; NIPPOSTRONGYLUS; RECEPTORS, G-PROTEIN-COUPLED; STRONGYLIDA INFECTIONS; SUCCINIC ACID;

EID: 85047302258     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1720758115     Document Type: Article

References (51)

1. Peterson LW, Artis D (2014) Intestinal epithelial cells: Regulators of barrier function and immune homeostasis. Nat Rev Immunol 14:141–153.
2. Isomäki AM (1973) A new cell type (tuft cell) in the gastrointestinal mucosa of the rat. A transmission and scanning electron microscopic study. Acta Pathol Microbiol Scand [A] 240(Suppl):1–35.
3. Nabeyama A, Leblond CP (1974) “Caveolated cells” characterized by deep surface invaginations and abundant filaments in mouse gastro-intestinal epithelia. Am J Anat 140:147–165.
4. Höfer D, Drenckhahn D (1992) Identification of brush cells in the alimentary and respiratory system by antibodies to villin and fimbrin. Histochemistry 98:237–242.
5. Hammond JB, Ladeur L (1968) Fibrillovesicular cells in the fundic glands of the canine stomach: Evidence for a new cell type. Anat Rec 161:393–411.
6. von Moltke J, Ji M, Liang HE, Locksley RM (2016) Tuft-cell-derived IL-25 regulates an intestinal ILC2-epithelial response circuit. Nature 529:221–225.
7. Howitt MR, et al. (2016) Tuft cells, taste-chemosensory cells, orchestrate parasite type 2 immunity in the gut. Science 351:1329–1333.
8. Gerbe F, et al. (2016) Intestinal epithelial tuft cells initiate type 2 mucosal immunity to helminth parasites. Nature 529:226–230.
9. Höfer D, Jöns T, Kraemer J, Drenckhahn D (1998) From cytoskeleton to polarity and chemoreception in the gut epithelium. Ann N Y Acad Sci 859:75–84.
10. Bezençon C, le Coutre J, Damak S (2007) Taste-signaling proteins are coexpressed in solitary intestinal epithelial cells. Chem Senses 32:41–49.
11. Bezençon C, et al. (2008) Murine intestinal cells expressing Trpm5 are mostly brush cells and express markers of neuronal and inflammatory cells. J Comp Neurol 509: 514–525.
12. Kokrashvili Z, et al. (2009) Release of endogenous opioids from duodenal enteroendocrine cells requires Trpm5. Gastroenterology 137:598–606.e2.
13. Höfer D, Püschel B, Drenckhahn D (1996) Taste receptor-like cells in the rat gut identified by expression of alpha-gustducin. Proc Natl Acad Sci USA 93:6631–6634.
14. Koninkx JF, Mirck MH, Hendriks HG, Mouwen JM, van Dijk JE (1988) Nippostrongylus brasiliensis: Histochemical changes in the composition of mucins in goblet cells during infection in rats. Exp Parasitol 65:84–90.
15. Miller HR, Nawa Y (1979) Immune regulation of intestinal goblet cell differentiation. Specific induction of nonspecific protection against helminths? Nouv Rev Fr Hematol 21:31–45.
16. Matsumoto I, Ohmoto M, Narukawa M, Yoshihara Y, Abe K (2011) Skn-1a (Pou2f3) specifies taste receptor cell lineage. Nat Neurosci 14:685–687.
17. Fallon PG, et al. (2006) Identification of an interleukin (IL)-25-dependent cell population that provides IL-4, IL-5, and IL-13 at the onset of helminth expulsion. J Exp Med 203:1105–1116.
18. Fort MM, et al. (2001) IL-25 induces IL-4, IL-5, and IL-13 and Th2-associated pathologies in vivo. Immunity 15:985–995.
19. Pérez CA, et al. (2002) A transient receptor potential channel expressed in taste receptor cells. Nat Neurosci 5:1169–1176.
20. Zhang Y, et al. (2003) Coding of sweet, bitter, and umami tastes: Different receptor cells sharing similar signaling pathways. Cell 112:293–301.
21. He W, et al. (2004) Citric acid cycle intermediates as ligands for orphan G-protein-coupled receptors. Nature 429:188–193.
22. Gilroy FV, Edwards MR, Norton RS, O’Sullivan WJ (1988) Metabolic studies of the protozoan parasite, Crithidia luciliae, using proton nuclear magnetic resonance spectroscopy. Mol Biochem Parasitol 31:107–115.
23. Ferreyra JA, et al. (2014) Gut microbiota-produced succinate promotes C. difficile infection after antibiotic treatment or motility disturbance. Cell Host Microbe 16: 770–777.
24. Tsukahara T, Ushida K (2002) Succinate accumulation in pig large intestine during antibiotic-associated diarrhea and the constitution of succinate-producing flora. J Gen Appl Microbiol 48:143–154.
25. Correa PR, et al. (2007) Succinate is a paracrine signal for liver damage. J Hepatol 47: 262–269.
26. Toma I, et al. (2008) Succinate receptor GPR91 provides a direct link between high glucose levels and renin release in murine and rabbit kidney. J Clin Invest 118: 2526–2534.
27. Chouchani ET, et al. (2014) Ischaemic accumulation of succinate controls reperfusion injury through mitochondrial ROS. Nature 515:431–435.
28. Rubic T, et al. (2008) Triggering the succinate receptor GPR91 on dendritic cells enhances immunity. Nat Immunol 9:1261–1269.
29. Saz DK, Bonner TP, Karlin M, Saz HJ (1971) Biochemical observations on adult Nippostrongylus brasiliensis. J Parasitol 57:1159–1162.
30. Haber AL, et al. (2017) A single-cell survey of the small intestinal epithelium. Nature 551:333–339.
31. Barker N, et al. (2007) Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 449:1003–1007.
32. Gerbe F, Brulin B, Makrini L, Legraverend C, Jay P (2009) DCAMKL-1 expression identifies tuft cells rather than stem cells in the adult mouse intestinal epithelium. Gastroenterology 137:2179–2180; author reply 2180–2181.
33. Neill DR, et al. (2010) Nuocytes represent a new innate effector leukocyte that mediates type-2 immunity. Nature 464:1367–1370.
34. Wong GT, Gannon KS, Margolskee RF (1996) Transduction of bitter and sweet taste by gustducin. Nature 381:796–800.
35. Damak S, et al. (2006) Trpm5 null mice respond to bitter, sweet, and umami compounds. Chem Senses 31:253–264.
36. Rubic-Schneider T, et al. (2017) GPR91 deficiency exacerbates allergic contact dermatitis while reducing arthritic disease in mice. Allergy 72:444–452.
37. Sapieha P, et al. (2008) The succinate receptor GPR91 in neurons has a major role in retinal angiogenesis. Nat Med 14:1067–1076.
38. Aguiar CJ, et al. (2014) Succinate causes pathological cardiomyocyte hypertrophy through GPR91 activation. Cell Commun Signal 12:78.
39. Li YH, Woo SH, Choi DH, Cho EH (2015) Succinate causes α-SMA production through GPR91 activation in hepatic stellate cells. Biochem Biophys Res Commun 463:853–858.
40. Tannahill GM, et al. (2013) Succinate is an inflammatory signal that induces IL-1β through HIF-1α. Nature 496:238–242.
41. De Vadder F, et al. (2016) Microbiota-produced succinate improves glucose homeostasis via intestinal gluconeogenesis. Cell Metab 24:151–157.
42. Fischbach MA, Sonnenburg JL (2011) Eating for two: How metabolism establishes interspecies interactions in the gut. Cell Host Microbe 10:336–347.
43. Finger TE, et al. (2003) Solitary chemoreceptor cells in the nasal cavity serve as sentinels of respiration. Proc Natl Acad Sci USA 100:8981–8986.
44. Rhodin J, Dalhamn T (1956) Electron microscopy of the tracheal ciliated mucosa in rat. Z Zellforsch Mikrosk Anat 44:345–412.
45. Tizzano M, et al. (2010) Nasal chemosensory cells use bitter taste signaling to detect irritants and bacterial signals. Proc Natl Acad Sci USA 107:3210–3215.
46. Lee RJ, et al. (2012) T2R38 taste receptor polymorphisms underlie susceptibility to upper respiratory infection. J Clin Invest 122:4145–4159.
47. Jakobsdottir G, Xu J, Molin G, Ahrné S, Nyman M (2013) High-fat diet reduces the formation of butyrate, but increases succinate, inflammation, liver fat and cholesterol in rats, while dietary fibre counteracts these effects. PLoS One 8:e80476.
48. Hams E, Locksley RM, McKenzie AN, Fallon PG (2013) Cutting edge: IL-25 elicits innate lymphoid type 2 and type II NKT cells that regulate obesity in mice. J Immunol 191: 5349–5353.
49. Kashyap PC, et al. (2013) Complex interactions among diet, gastrointestinal transit, and gut microbiota in humanized mice. Gastroenterology 144:967–977.
50. Pulendran B, Artis D (2012) New paradigms in type 2 immunity. Science 337:431–435.
51. Buonomo EL, et al. (2016) Microbiota-regulated IL-25 increases eosinophil number to provide protection during Clostridium difficile infection. Cell Rep 16:432–443.