IRE1β Evolves to Be a Guardian of Respiratory and Gastrointestinal Mucosa

Overview

Journal Heliyon

Specialty Social Sciences

Date 2024 Nov 11

PMID 39524875

Authors

Hui Luo

Wen-Yan Gong

Yuan-Yuan Zhang

Ying-Ying Liu

Zhen Chen

Xing-Lin Feng

Qi-Bin Jiao

Xing-Wei Zhang

Affiliations

Soon will be listed here.

Abstract

Inositol-requiring enzyme 1 (IRE1), a mediator of the unfolded protein response, shows the highest degree of evolutionary conservation. Vertebrates express two IRE1 paralogs: IRE1α, which is universally expressed and IRE1β, which shows specific expression within mucus secreted cells in respiratory and gastrointestinal tracts. The biological properties and regulation of the two IRE1 duplicates show evolutionary differences. As recently suggested, IRE1β-deficient mice display impairment in secreted protein expression and mucosal homeostasis. Abnormal changes in IRE1β caused by external and internal factors can disrupt mucosal homeostasis and further lead to respiratory and gastrointestinal diseases. Here, we highlight the physiological functions of IRE1β in the respiratory and gastrointestinal tracts in response to environmental microbes, viruses, toxins, and food components.

References

Maurel M, Chevet E, Tavernier J, Gerlo S . Getting RIDD of RNA: IRE1 in cell fate regulation. Trends Biochem Sci. 2014; 39(5):245-54. DOI: 10.1016/j.tibs.2014.02.008. View

Julve J, Martin-Campos J, Escola-Gil J, Blanco-Vaca F . Chylomicrons: Advances in biology, pathology, laboratory testing, and therapeutics. Clin Chim Acta. 2016; 455:134-48. DOI: 10.1016/j.cca.2016.02.004. View

Kaser A, Lee A, Franke A, Glickman J, Zeissig S, Tilg H . XBP1 links ER stress to intestinal inflammation and confers genetic risk for human inflammatory bowel disease. Cell. 2008; 134(5):743-56. PMC: 2586148. DOI: 10.1016/j.cell.2008.07.021. View

Simakov O, Marletaz F, Yue J, OConnell B, Jenkins J, Brandt A . Deeply conserved synteny resolves early events in vertebrate evolution. Nat Ecol Evol. 2020; 4(6):820-830. PMC: 7269912. DOI: 10.1038/s41559-020-1156-z. View

Iqbal J, Dai K, Seimon T, Jungreis R, Oyadomari M, Kuriakose G . IRE1beta inhibits chylomicron production by selectively degrading MTP mRNA. Cell Metab. 2008; 7(5):445-55. PMC: 2435513. DOI: 10.1016/j.cmet.2008.03.005. View

Cloots E, Simpson M, De Nolf C, Lencer W, Janssens S, Grey M . Evolution and function of the epithelial cell-specific ER stress sensor IRE1β. Mucosal Immunol. 2021; 14(6):1235-1246. PMC: 8528705. DOI: 10.1038/s41385-021-00412-8. View

Hollien J, Lin J, Li H, Stevens N, Walter P, Weissman J . Regulated Ire1-dependent decay of messenger RNAs in mammalian cells. J Cell Biol. 2009; 186(3):323-31. PMC: 2728407. DOI: 10.1083/jcb.200903014. View

Bansil R, Turner B . The biology of mucus: Composition, synthesis and organization. Adv Drug Deliv Rev. 2017; 124:3-15. DOI: 10.1016/j.addr.2017.09.023. View

Bertolotti A, Wang X, Novoa I, Jungreis R, Schlessinger K, Cho J . Increased sensitivity to dextran sodium sulfate colitis in IRE1beta-deficient mice. J Clin Invest. 2001; 107(5):585-93. PMC: 199427. DOI: 10.1172/JCI11476. View

10.

Oikawa D, Tokuda M, Hosoda A, Iwawaki T . Identification of a consensus element recognized and cleaved by IRE1 alpha. Nucleic Acids Res. 2010; 38(18):6265-73. PMC: 2952871. DOI: 10.1093/nar/gkq452. View

11.

Holland L, Ocampo Daza D . A new look at an old question: when did the second whole genome duplication occur in vertebrate evolution?. Genome Biol. 2018; 19(1):209. PMC: 6260733. DOI: 10.1186/s13059-018-1592-0. View

12.

Han D, Lerner A, Vande Walle L, Upton J, Xu W, Hagen A . IRE1alpha kinase activation modes control alternate endoribonuclease outputs to determine divergent cell fates. Cell. 2009; 138(3):562-75. PMC: 2762408. DOI: 10.1016/j.cell.2009.07.017. View

13.

Zundell J, Fukumoto T, Lin J, Fatkhudinov N, Nacarelli T, Kossenkov A . Targeting the IRE1α/XBP1 Endoplasmic Reticulum Stress Response Pathway in -Mutant Ovarian Cancers. Cancer Res. 2021; 81(20):5325-5335. PMC: 8723353. DOI: 10.1158/0008-5472.CAN-21-1545. View

14.

Hollien J, Weissman J . Decay of endoplasmic reticulum-localized mRNAs during the unfolded protein response. Science. 2006; 313(5783):104-7. DOI: 10.1126/science.1129631. View

15.

Unger S, Bogaert D . The respiratory microbiome and respiratory infections. J Infect. 2017; 74 Suppl 1:S84-S88. DOI: 10.1016/S0163-4453(17)30196-2. View

16.

Carr-Locke D . Mucin hypersecreting neoplasms. Ann Oncol. 1999; 10 Suppl 4:99-103. View

17.

Cooke C, An H, Kim J, Canfield D, Torres J, Lebrilla C . Modification of gastric mucin oligosaccharide expression in rhesus macaques after infection with Helicobacter pylori. Gastroenterology. 2009; 137(3):1061-71, 1071.e1-8. DOI: 10.1053/j.gastro.2009.04.014. View

18.

Persson S, Rosenquist M, Knoblach B, Khosravi-Far R, Sommarin M, Michalak M . Diversity of the protein disulfide isomerase family: identification of breast tumor induced Hag2 and Hag3 as novel members of the protein family. Mol Phylogenet Evol. 2005; 36(3):734-40. DOI: 10.1016/j.ympev.2005.04.002. View

19.

Lin R, Sun Y, Ye W, Zheng T, Wen J, Deng Y . T-2 toxin inhibits the production of mucin via activating the IRE1/XBP1 pathway. Toxicology. 2019; 424:152230. DOI: 10.1016/j.tox.2019.06.001. View

20.

Oikawa D, Kitamura A, Kinjo M, Iwawaki T . Direct association of unfolded proteins with mammalian ER stress sensor, IRE1β. PLoS One. 2012; 7(12):e51290. PMC: 3517461. DOI: 10.1371/journal.pone.0051290. View