دورية أكاديمية
Enteroendocrine cells sense bacterial tryptophan catabolites to activate enteric and vagal neuronal pathways.
| العنوان: | Enteroendocrine cells sense bacterial tryptophan catabolites to activate enteric and vagal neuronal pathways. |
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| المؤلفون: | Ye L; Department of Molecular Genetics and Microbiology, Duke Microbiome Center, Duke University School of Medicine, Durham, NC 27710, USA; Division of Gastroenterology, Department of Medicine, Duke University School of Medicine, Durham, NC 27710, USA., Bae M; Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Boston, MA 02115, USA., Cassilly CD; Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Boston, MA 02115, USA., Jabba SV; Department of Anesthesiology, Duke University School of Medicine, Durham, NC 27710, USA., Thorpe DW; Flinders Medical Research Institute, College of Medicine and Public Health, Flinders University, Adelaide, Australia., Martin AM; Flinders Medical Research Institute, College of Medicine and Public Health, Flinders University, Adelaide, Australia., Lu HY; Department of Molecular Genetics and Microbiology, Duke Microbiome Center, Duke University School of Medicine, Durham, NC 27710, USA., Wang J; Division of Cardiology, School of Medicine, Emory University, Atlanta, GA 30322, USA., Thompson JD; Department of Cell Biology, Regeneration Next, Duke University School of Medicine, Durham, NC 27710, USA., Lickwar CR; Department of Molecular Genetics and Microbiology, Duke Microbiome Center, Duke University School of Medicine, Durham, NC 27710, USA; Division of Gastroenterology, Department of Medicine, Duke University School of Medicine, Durham, NC 27710, USA., Poss KD; Department of Cell Biology, Regeneration Next, Duke University School of Medicine, Durham, NC 27710, USA., Keating DJ; Flinders Medical Research Institute, College of Medicine and Public Health, Flinders University, Adelaide, Australia., Jordt SE; Department of Anesthesiology, Duke University School of Medicine, Durham, NC 27710, USA., Clardy J; Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Boston, MA 02115, USA., Liddle RA; Division of Gastroenterology, Department of Medicine, Duke University School of Medicine, Durham, NC 27710, USA; Department of Veterans Affairs, Durham, NC 27705, USA., Rawls JF; Department of Molecular Genetics and Microbiology, Duke Microbiome Center, Duke University School of Medicine, Durham, NC 27710, USA; Division of Gastroenterology, Department of Medicine, Duke University School of Medicine, Durham, NC 27710, USA. Electronic address: john.rawls@duke.edu. |
| المصدر: | Cell host & microbe [Cell Host Microbe] 2021 Feb 10; Vol. 29 (2), pp. 179-196.e9. Date of Electronic Publication: 2020 Dec 21. |
| نوع المنشور: | Journal Article; Research Support, N.I.H., Extramural; Research Support, Non-U.S. Gov't |
| اللغة: | English |
| بيانات الدورية: | Publisher: Cell Press Country of Publication: United States NLM ID: 101302316 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1934-6069 (Electronic) Linking ISSN: 19313128 NLM ISO Abbreviation: Cell Host Microbe Subsets: MEDLINE |
| أسماء مطبوعة: | Original Publication: Cambridge, Mass. : Cell Press |
| مواضيع طبية MeSH: | Edwardsiella tarda/*metabolism , Enteric Nervous System/*metabolism , Enteroendocrine Cells/*physiology , Intestinal Mucosa/*metabolism , TRPA1 Cation Channel/*metabolism, Animals ; Animals, Genetically Modified ; Cholinergic Neurons/metabolism ; Enteric Nervous System/cytology ; Gastrointestinal Motility/physiology ; Intestinal Mucosa/cytology ; Intestinal Mucosa/innervation ; Proto-Oncogene Proteins c-ret/genetics ; Serotonin/metabolism ; Signal Transduction ; Tryptophan/metabolism ; Zebrafish ; Zebrafish Proteins/genetics |
| مستخلص: | The intestinal epithelium senses nutritional and microbial stimuli using epithelial sensory enteroendocrine cells (EEC). EECs communicate nutritional information to the nervous system, but whether they also relay signals from intestinal microbes remains unknown. Using in vivo real-time measurements of EEC and nervous system activity in zebrafish, we discovered that the bacteria Edwardsiella tarda activate EECs through the receptor transient receptor potential ankyrin A1 (Trpa1) and increase intestinal motility. Microbial, pharmacological, or optogenetic activation of Trpa1 + EECs directly stimulates vagal sensory ganglia and activates cholinergic enteric neurons by secreting the neurotransmitter 5-hydroxytryptamine (5-HT). A subset of indole derivatives of tryptophan catabolism produced by E. tarda and other gut microbes activates zebrafish EEC Trpa1 signaling. These catabolites also directly stimulate human and mouse Trpa1 and intestinal 5-HT secretion. These results establish a molecular pathway by which EECs regulate enteric and vagal neuronal pathways in response to microbial signals. Competing Interests: Declaration of interests The authors declare no competing interests. (Copyright © 2020 Elsevier Inc. All rights reserved.) |
| التعليقات: | Comment in: Cell Host Microbe. 2021 Feb 10;29(2):145-147. (PMID: 33571438) |
| References: | Curr Pharm Biotechnol. 2011 Jan 1;12(1):24-34. (PMID: 20932260) Nature. 2012 Apr 25;484(7395):479-84. (PMID: 22538609) Curr Opin Endocrinol Diabetes Obes. 2013 Feb;20(1):14-21. (PMID: 23222853) Aliment Pharmacol Ther. 2004 Nov;20 Suppl 7:3-14. (PMID: 15521849) PLoS One. 2012;7(5):e36987. (PMID: 22590641) Eur J Gastroenterol Hepatol. 2014 Jul;26(7):753-60. (PMID: 24849768) Elife. 2019 Dec 03;8:. (PMID: 31793875) Cell. 2006 Mar 24;124(6):1269-82. (PMID: 16564016) Proc Natl Acad Sci U S A. 2011 Sep 20;108(38):16050-5. (PMID: 21876150) Immunity. 2014 Aug 21;41(2):296-310. (PMID: 25065623) Annu Rev Physiol. 2006;68:279-305. (PMID: 16460274) Neurogastroenterol Motil. 2018 Sep;30(9):e13351. (PMID: 29722095) Cell Microbiol. 2020 Mar;22(3):e13152. (PMID: 31872937) Proc Natl Acad Sci U S A. 2003 Nov 25;100(24):13940-5. (PMID: 14615590) Physiol Behav. 2006 Nov 30;89(4):517-24. (PMID: 16996546) Cell Tissue Res. 2008 Nov;334(2):147-61. (PMID: 18855018) Front Neurosci. 2018 Feb 07;12:49. (PMID: 29467611) PLoS Biol. 2017 Feb 16;15(2):e2000689. (PMID: 28207737) Endocrinology. 2018 Jul 1;159(7):2826-2835. (PMID: 29688303) J Neurosci. 2011 Jun 15;31(24):8998-9009. (PMID: 21677183) Cell. 2006 Oct 20;127(2):423-33. (PMID: 17055441) Syst Appl Microbiol. 2018 Jan;41(1):30-37. (PMID: 29150173) J Exp Med. 1897 Sep 1;2(5):543-7. (PMID: 19866850) Development. 2011 May;138(10):2015-24. (PMID: 21490065) Cell Rep. 2014 Nov 20;9(4):1202-8. (PMID: 25456122) Annu Rev Med. 2015;66:343-59. (PMID: 25587655) Proc Natl Acad Sci U S A. 2012 Jan 31;109(5):1506-11. (PMID: 22307605) Development. 2017 Aug 15;144(16):2889-2895. (PMID: 28811310) Neuron. 2019 Mar 20;101(6):998-1002. (PMID: 30897366) Nat Methods. 2015 Nov;12(11):1039-46. (PMID: 26778924) Genome Biol. 2014;15(12):550. (PMID: 25516281) Nat Rev Gastroenterol Hepatol. 2016 Jul;13(7):389-401. (PMID: 27251213) Mol Pharmacol. 2014 May;85(5):777-88. (PMID: 24563545) Dev Dyn. 2007 Nov;236(11):3088-99. (PMID: 17937395) Nat Protoc. 2008;3(12):1862-75. (PMID: 19008873) J Vis Exp. 2013 Feb 20;(72):e4434. (PMID: 23463135) Proc Natl Acad Sci U S A. 2009 Mar 3;106(9):3408-13. (PMID: 19211797) Front Neurosci. 2018 Apr 09;12:216. (PMID: 29686603) Nat Rev Gastroenterol Hepatol. 2013 May;10(5):286-96. (PMID: 23438947) Infect Immun. 2003 Mar;71(3):1343-51. (PMID: 12595451) J Appl Microbiol. 2013 Mar;114(3):644-54. (PMID: 23167785) Front Pediatr. 2019 Sep 04;7:363. (PMID: 31552207) J Clin Invest. 2015 Feb;125(2):782-6. (PMID: 25555217) PLoS One. 2020 Jul 9;15(7):e0234906. (PMID: 32645011) Methods Enzymol. 2012;504:183-200. (PMID: 22264535) Vet Res. 2012 Oct 04;43:67. (PMID: 23035843) Br J Pharmacol. 2017 May;174(9):867-879. (PMID: 28240768) Mol Pharmacol. 2012 Jan;81(1):3-11. (PMID: 21967751) J Neurosci. 2008 Oct 1;28(40):10102-10. (PMID: 18829968) JCI Insight. 2019 May 2;4(9):. (PMID: 31045572) Nat Methods. 2012 Jun 28;9(7):676-82. (PMID: 22743772) Nat Chem Biol. 2013 Apr;9(4):257-63. (PMID: 23396078) PLoS Pathog. 2019 Mar 7;15(3):e1007381. (PMID: 30845179) FEBS Lett. 2008 Apr 30;582(10):1514-8. (PMID: 18396169) Diabetes. 2019 May;68(5):1062-1072. (PMID: 30733330) Neurogastroenterol Motil. 2011 Dec;23(12):1132-9. (PMID: 21988661) Cell. 2016 Nov 3;167(4):947-960.e20. (PMID: 27814522) Zebrafish. 2014 Apr;11(2):85-97. (PMID: 24428354) Cell Rep. 2019 Dec 17;29(12):4172-4185.e5. (PMID: 31851941) Immunity. 2016 Oct 18;45(4):861-876. (PMID: 27760340) Adv Exp Med Biol. 2014;817:39-71. (PMID: 24997029) Environ Toxicol. 2017 Oct;32(10):2316-2322. (PMID: 28722335) Development. 1999 Jun;126(12):2785-97. (PMID: 10331988) Front Endocrinol (Lausanne). 2018 May 09;9:230. (PMID: 29867763) Development. 2016 May 15;143(10):1688-96. (PMID: 26989176) J Physiol. 2011 Apr 1;589(Pt 7):1543-9. (PMID: 21078588) Trends Endocrinol Metab. 2020 Nov;31(11):818-834. (PMID: 32284282) Science. 2018 Sep 21;361(6408):. (PMID: 30237325) Genome Biol. 2007;8 Suppl 1:S7. (PMID: 18047699) Channels (Austin). 2011 Nov-Dec;5(6):525-9. (PMID: 21993194) BMC Genomics. 2013 Sep 22;14:642. (PMID: 24053667) Nat Commun. 2014;5:3125. (PMID: 24445575) Nature. 2007 Feb 1;445(7127):541-5. (PMID: 17237762) Development. 2012 Feb;139(3):591-600. (PMID: 22190641) Neural Dev. 2012 Jun 27;7:23. (PMID: 22738203) J Clin Endocrinol Metab. 2019 Jul 1;104(7):2668-2674. (PMID: 30759215) Annu Rev Physiol. 2013;75:181-200. (PMID: 23020579) Sci Rep. 2015 Aug 03;5:12689. (PMID: 26235394) Science. 2015 Feb 13;347(6223):755-60. (PMID: 25678659) Proc Natl Acad Sci U S A. 2020 Jul 7;117(27):15837-15845. (PMID: 32571957) Cell. 2015 Apr 9;161(2):264-76. (PMID: 25860609) Cell. 2018 Oct 18;175(3):665-678.e23. (PMID: 30245012) Immunity. 2013 Aug 22;39(2):372-85. (PMID: 23973224) Cell. 2017 Jun 29;170(1):185-198.e16. (PMID: 28648659) Am J Physiol. 1999 Nov;277(5):G922-8. (PMID: 10564096) J Neurophysiol. 2000 Jul;84(1):102-11. (PMID: 10899188) Proc Natl Acad Sci U S A. 2019 Aug 20;116(34):16961-16970. (PMID: 31391308) Cell Host Microbe. 2018 Jun 13;23(6):775-785.e5. (PMID: 29902441) FASEB J. 2018 Sep;32(9):4744-4752. (PMID: 29570391) Int J Obes (Lond). 2009 Apr;33 Suppl 1:S11-5. (PMID: 19363500) ISME J. 2016 Mar;10(3):644-54. (PMID: 26339860) Dev Biol. 2013 Apr 15;376(2):171-86. (PMID: 23353550) Nature. 2017 Nov 16;551(7680):333-339. (PMID: 29144463) Front Immunol. 2018 Jan 05;8:1927. (PMID: 29354132) Environ Pollut. 2019 Dec;255(Pt 3):113357. (PMID: 31671369) J Neurophysiol. 2006 Sep;96(3):973-4. (PMID: 16837658) Dev Biol. 2013 Oct 1;382(1):330-43. (PMID: 23644063) Gut Liver. 2017 Mar 15;11(2):196-208. (PMID: 28274108) Nat Rev Gastroenterol Hepatol. 2013 Dec;10(12):729-40. (PMID: 24061204) Neuron. 2019 Jul 3;103(1):21-38.e5. (PMID: 31147152) Gut. 2015 Apr;64(4):618-26. (PMID: 25015642) Nutr Metab (Lond). 2015 Dec 15;12:55. (PMID: 26673561) Biochemistry. 1998 Aug 18;37(33):11508-15. (PMID: 9708986) Front Psychiatry. 2018 Mar 13;9:44. (PMID: 29593576) Trends Immunol. 2014 Nov;35(11):538-48. (PMID: 25220948) Cell Host Microbe. 2020 Feb 12;27(2):238-248.e7. (PMID: 31901518) J Neurosci. 2000 May 1;20(9):3295-309. (PMID: 10777793) Development. 2014 Mar;141(5):1110-9. (PMID: 24504339) |
| معلومات مُعتمدة: | R01 GM074057 United States GM NIGMS NIH HHS; F32 AT010415 United States AT NCCIH NIH HHS; R35 HL150713 United States HL NHLBI NIH HHS; R01 DK093399 United States DK NIDDK NIH HHS; K01 DK125527 United States DK NIDDK NIH HHS; T32 DK007568 United States DK NIDDK NIH HHS; S10 OD020010 United States OD NIH HHS; R01 DK109368 United States DK NIDDK NIH HHS; U01 ES030672 United States ES NIEHS NIH HHS; I01 BX002230 United States BX BLRD VA |
| فهرسة مساهمة: | Keywords: Danio rerio; bacterial tryptophan catabolism; enteroendocrine cells; gut microbes; gut-brain axis communication; indole; indole-3-carboxaldehyde; intestinal peristalsis; serotonin |
| المشرفين على المادة: | 0 (TRPA1 Cation Channel) 0 (Zebrafish Proteins) 333DO1RDJY (Serotonin) 8DUH1N11BX (Tryptophan) EC 2.7.10.1 (Proto-Oncogene Proteins c-ret) EC 2.7.10.1 (Ret protein, zebrafish) |
| تواريخ الأحداث: | Date Created: 20201222 Date Completed: 20210816 Latest Revision: 20220211 |
| رمز التحديث: | 20231215 |
| مُعرف محوري في PubMed: | PMC7997396 |
| DOI: | 10.1016/j.chom.2020.11.011 |
| PMID: | 33352109 |
| قاعدة البيانات: | MEDLINE |
| تدمد: | 1934-6069 |
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| DOI: | 10.1016/j.chom.2020.11.011 |