Skip to main content
SpringerLink
Log in

Peculiarities of Endoplasmic Reticulum Stress Regulator XBP1 Expression in the Gut-Associated Lymphoid Tissue of Wistar Rats under Chronic Stress

  • Experimental Papers
  • Published:
Journal of Evolutionary Biochemistry and Physiology Aims and scope Submit manuscript

An Erratum to this article was published on 01 December 2022

This article has been updated

Abstract

Chronic social stress (CSS) can cause physiological disturbances, provoking the development of depression and anxiety, and stress-induced immune dysregulation is a trigger for the development of many pathological conditions, including inflammatory bowel diseases. New data in human and animal models suggest an intriguing relationship between endoplasmic reticulum stress, depression and inflammation. Under cellular stress, the number of protein folding disorders increases, which leads to the development of endoplasmic reticulum stress (ERS). The ERS, in turn, activates the “unfolded protein response” system (unfolded protein response, UPR), the IRE1–XBP1 signaling system is very important. The transcription factor XBP1 is responsible for regulating the expression of a large number of genes involved in the proper folding and maturation of proteins, the degradation of misfolded proteins and regulation of immune responses. In addition, changes in XBP1 expression can significantly affect the risk of developing the disease and the progression of inflammatory and autoimmune diseases, including inflammatory bowel disease.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.
Fig. 2.
Fig. 3.

Similar content being viewed by others

Change history

REFERENCES

  1. Dhabhar F (2014) Effects of stress on immune function: the good, the bad, and the beautiful. Immunol Res 58(2–3): 193–210. https://doi.org/10.1007/s12026-014-8517-0

    Article  CAS  PubMed  Google Scholar 

  2. Almanza A, Carlesso A, Chintha C, Creedican S, Doultsinos D, Leuzzi B, Luis A, McCarthy N, Montibeller L, More S, Papaioannou A, Püschel F, Sassano ML, Skoko J, Agostinis P, Jackie de Belleroche, Eriksson LA, Fulda S, Gorman AM, Healy S, Kozlov A, Muñoz-Pinedo C, Rehm M, Chevet E (2019) Endoplasmic reticulum stress signalling—from basic mechanisms to clinical applications. FEBS J 286: 241–278. https://doi.org/10.1111/febs.14608

    Article  CAS  PubMed  Google Scholar 

  3. Schwarz DS, Blower MD (2016) The endoplasmic reticulum: Structure, function and response to cellular signaling. Cell Mol Life Sci 73: 79–94. https://doi.org/10.1007/s00018-015-2052-6

    Article  CAS  PubMed  Google Scholar 

  4. Dedov II, Smirnova OM, Gorelyshev AS (2012) Stress of endoplasmic reticulum: the cytological “scenario” of pathogenesis of human diseases. Probl Endokrinol 58(5): 57–65. (In Russ).

    Article  Google Scholar 

  5. Zverev YF, Bryuhanov VM (2013) Endoplasmic reticulum stress in terms of nephrologist (message ii). Nephrology (Saint-Petersburg) 17(2): 39–54. https://doi.org/10.24884/1561-6274-2013-17-2-39-546

  6. Kaser A, Blumberg R (2010) Endoplasmic reticulum stress and intestinal inflammation. Mucos Immunol 3: 11–16. https://doi.org/10.1038/mi.2009.122

    Article  CAS  Google Scholar 

  7. Kaser A, Flak M, Blumberg R (2011) The unfolded protein response and its role in intestinal homeostasis and inflammation. Exp Cell Res 15: 2772–2779. https://doi.org/10.1016/j.yexcr.2011.07.008

    Article  CAS  Google Scholar 

  8. Mesitov MV, Moskovtsev AA, Kubatiev AA (2013) Molecular logic of the endoplasmic reticulum stress signal pathways: the system of unfolded protein response Patol Fiziol Eksp Ter 4: 97–108. (In Russ).

  9. Hillary RF, FitzGerald U (2018) A lifetime of stress: ATF6 in development and homeostasis. J Biomed Sci 25(1): 48. https://doi.org/10.1186/s12929-018-0453-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Glimcher L (2010) XBP1: the last two decades. Ann Rheum Dis 69: 67–71. https://doi.org/10.1136/ard.2009.119388

    Article  CAS  Google Scholar 

  11. Martinon F, Glimcher L (2011) Regulation of Innate Immunity by signaling pathways emerging from the endoplasmic reticulum. Curr Opin Immunol 23: 35–40. https://doi.org/10.1016/j.coi.2010.10.016

    Article  CAS  PubMed  Google Scholar 

  12. Martinon F, Chen X, Glimcher L (2010) Toll-like receptor activation of XBP1 regulates innate immune responses in macrophages. Nat Immunol 11: 411–418. https://doi.org/10.1038/ni.1857

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Wu R, Zhang QH, Lu Y-Ju, Ren K,Yi GH (2015) Involvement of the IRE1α-XBP1 pathway and XBP1s-dependent transcriptional reprogramming in metabolic diseases DNA. Cell Biol 34(1): 6–18. https://doi.org/10.1089/dna.2014.2552

    Article  CAS  Google Scholar 

  14. Kaufman R, Cao S (2010) Inositol-requiring 1/X-box-binding protein 1 is a regulatory hub that links endoplasmic reticulum homeostasis with innate immunity and metabolism. EMBO Mol Med 6: 189–192. https://doi.org/10.1002/emmm.201000076

    Article  CAS  Google Scholar 

  15. Zhang Y, Liu W, Zhou Y, Ma C, Li S, Cong B (2014) Endoplasmic reticulum stress is involved in restraint stress-induced hippocampal apoptosis and cognitive impairments in rats. Physiol Behav 131: 41–48. https://doi.org/10.1016/j.physbeh.2014.04.014

    Article  CAS  PubMed  Google Scholar 

  16. Zhao T, Huang GB, Muna SS, Bagalkot TR, Jin HM, Chae HM, Chung Y-Ch (2013) Effects of chronic social defeat stress on behavior and choline acetyltransferase, 78-kDa glucose-regulated protein, and CCAAT/enhancer-binding protein (C/EBP) homologous protein in adult mice. Psychopharmacology 228: 217–230. https://doi.org/10.1007/s00213-013-3028-6

    Article  CAS  PubMed  Google Scholar 

  17. Timberlake M, Roy Bh, Dwivedi Y (2019) A Novel Animal Model for Studying Depression Featuring the Induction of the Unfolded Protein Response in Hippocampus. Mol Neurobiol 56(12): 8524–8536. https://doi.org/10.1007/s12035-019-01687-6

    Article  CAS  Google Scholar 

  18. Wu J, Rutkowski TD, Dubois M, Swathirajan J, Saunders T, Junying Wang, Benbo Song, Yau Grace D-Y, Kaufman RJ (2007) ATF6α Optimizes Long-Term Endoplasmic Reticulum Function to Protect Cells from Chronic Stress. Development Cell 13(3): 351–364. https://doi.org/doi.org/10.1016/j.devcel.2007.07.005

    Article  CAS  Google Scholar 

  19. Gao H, He C, Hua R, Guo Y, Wang B, Liang C, Gao L, Shang H, Xu JD (2022) Endoplasmic Reticulum Stress of Gut Enterocyte and Intestinal Diseases. Front Mol Biosci 24(9): 817392. https://doi.org/10.3389/fmolb.2022.817392.

    Article  Google Scholar 

  20. Amikishieva AV (2009) Behavioral phenotyping: Modern methods and equipment. Bull VOGiS 13(3): 529–542. (In Russ).

    Google Scholar 

  21. Porsolt RD, Pichon ML, Jalfre M (1977) Depression: a new animal model sensitive to antidepressant treatment. Nature 266: 730–732.

    Article  CAS  PubMed  Google Scholar 

  22. Kaser A, Lee AH, Franke A, Glickman JN, Zeissig S, Tilg H, Nieuwenhuis ES, Higgins DE, Schreiber S, Glimcher LH, Blumberg RS (2008) XBP1 links ER stress to intestinal inflammation and confers genetic risk for human inflammatory bowel disease. Cell 134(5): 743–756. https://doi.org/10.1016/j.cell.2008.07.021

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Ma X, Dai Z, Sun K, Zhang Y, Chen J, Yang Y, Tso P, Wu G, Wu Z (2017) Intestinal Epithelial Cell Endoplasmic Reticulum Stress and Inflammatory Bowel Disease Pathogenesis: An Update Review. Front Immunol 8: 1271. https://doi.org/10.1016/S0140-6736(19)30038-8

    Article  PubMed  PubMed Central  Google Scholar 

  24. Reverendo M, Mendes A, Argüello RJ, Gatti E, Pierre P (2019) At the crossway of ER-stress and pro-inflammatory responses. The FEBS J 286(2): 297–310. https://doi.org/10.1111/febs.14391

    Article  CAS  PubMed  Google Scholar 

  25. Giraud-Billoud M, Fader CM, Aguero R, Ezquer F, Ezquer M (2018) Diabetic nephropathy, autophagy and proximal tubule protein endocytic transport: a potentially harmful relationship. Biocell 42(2): 35–40. https://doi.org/10.32604/biocell.2018.07010

    Article  CAS  Google Scholar 

  26. Hooper KM, Barlow PG, Henderson P, Stevens C (2019) Interactions between autophagy and the unfolded protein response: implications for inflammatory bowel disease. Inflam Bowel Dis 25 (4): 661–671. https://doi.org/10.1093/ibd/izy

    Article  Google Scholar 

  27. Coleman OI, Haller D (2019) ER Stress and the UPR in Shaping Intestinal Tissue Homeostasis and Immunity. Front Immunol 10: 2825. https://doi.org/10.3389/fimmu.2019.02825

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Lotrich F (2012) Inflammatory Cytokines, Growth Factors, and Depression. Curr Pharm Des 18: 5920–5935. https://doi.org/10.2174/138161212803523680

    Article  CAS  PubMed  Google Scholar 

  29. Liu L, Zhao Z, Lu L, Liu JL, Sun J, Wu X, Dong J (2019) Icariin and icaritin ameliorated hippocampus neuroinflammation via inhibiting HMGB1-related pro-inflammatory signals in lipopolysaccharide-induced inflammation model in C57BL/6J mice. Int Immunopharmacol 68: 95–105. https://doi.org/10.1016/j.intimp.2018.12.055

    Article  CAS  PubMed  Google Scholar 

  30. So J-S (2018) Roles of endoplasmic reticulum stress in immune responses. Mol Cells 41: 705–716. https://doi.org/10.14348/molcells.2018.0241

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Cao SS, Luo KL, Shi L (2016) Endoplasmic reticulum stress interacts with inflammation in human disease. J Cell Physiol 231: 288–294. https://doi.org/10.1002/jcp.25098

    Article  CAS  PubMed  Google Scholar 

  32. Oakes SA, Papa FR (2015) The role of endoplasmic reticulum stress in human pathology. Annu Rev Pathol Mech Dis 10: 173–194. https://doi.org/10.1146/annurev-pathol-012513-104649

    Article  CAS  Google Scholar 

  33. Wu R, Zhang Q-H, Lu Y-J, Ren K, Yi G-H (2015) Involvement of the IRE1alpha-XBP1 pathway and XBP1s-dependent transcriptional reprogramming in metabolic diseases. DNA Cell Biol 34: 6–18. https://doi.org/10.1089/dna.2014.2552

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Hirayama D, Iida T, Nakase H (2018) Phagocytic function of macrophages—providing innate immunity and tissue homeostasis. Int J Mol Sci 19: 92. https://doi.org/10.3390/ijms19010092

    Article  CAS  Google Scholar 

  35. Park SM, Kang TI, So JS (2021) Roles of XBP1s in Transcriptional Regulation of Target Genes. Biomedicines 9(7): 791. https://doi.org/10.3390/biomedicines9070791

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Kazantseva AV, Davydova YD, Enikeeva RF Valinurov RG, Gareeva AE Khusnutdinova NN, Khusnutdinova EK (2021) The association study of polymorphic variants of hypothalamic-pituitary-adrenal system genes (AVPR1B, OXTR) and aggressive behavior manifestation: a focus on social environment. Res Results Biomed 7(3): 232–244. https://doi.org/10.18413/2658-6533-2021-7-3-0-3

    Article  Google Scholar 

  37. Wang Y, Zhang Y, Yi P, Dong W, Nalin AP, Zhang J, Zhu Z, Chen L, Benson DM, Mundy-Bosse BL, Freud AG, Caligiuri MA, Jianhua Yu (2019) The IL-15-AKT-XBP1s signaling pathway contributes to effector functions and survival in human NK cells. Nat Immunol 20: 10–17. https://doi.org/10.1038/s41590-018-0265-1

    Article  CAS  PubMed  Google Scholar 

  38. Brunsing R, Omori S, Niwa M (2008) B- and T-cell Development Both Involve Activity of the Unfolded Protein Response Pathway. J Biol Chem 283: 17954–17961. https://doi.org/10.1074/jbc.M801395200

    Article  CAS  PubMed  Google Scholar 

  39. Stadhouders R, Lubberts E, Hendriks RW (2018) A cellular and molecular view of T helper 17 cell plasticity in autoimmunity. J Autoimmun 87: 1–15.

    Article  CAS  PubMed  Google Scholar 

  40. Saravia J, Chapman NM, Chi H (2019) Helper T cell differentiation. Cell Mol Immunol 16: 634–643. https://doi.org/10.1038/s41423-019-0220-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Pramanik J, Chen X, Kar G, Henriksson J, Gomes T, Park J-E, Natarajan K, Meyer KB, Miao Z, McKenzie ANJ, Mahata B, Teichmann SA (2018) Genome-wide analyses reveal the IRE1α-XBP1 pathway promotes T helper cell differentiation by resolving secretory stress and accelerating proliferation. Genome Med 10: 76. https://doi.org/10.1186/s13073-018-0589-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Walker JA, McKenzie ANJ (2018) TH2 cell development and function. Nat Rev Immunol 18: 121–133. https://doi.org/10.1038/nri.2017.118

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

The work was carried out within the research work “The role of disorders of the lymphoid and epithelial compartments of the immune system of the mucous membranes in the development of experimental pathology” (research work no. 0108U005113).

Author information

Authors and Affiliations

  1. Belgorod State National Research University, Belgorod, Russia

    I. A. Topol, I. S. Polyakova & A. V. Elykova

  2. Ternopil State Medical University, Ternopil, Ukraine

    A. M. Kamyshny

Authors
  1. I. A. Topol
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. I. S. Polyakova
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. V. Elykova
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. A. M. Kamyshny
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Idea of work and planning of the experiment (K.A.M.), data collection (T.I.A., P.I.S., E.A.V.), data processing (T.I.A., P.I.S., E.A.V.), writing and editing the article (T.I.A., K.A.M.).

Corresponding author

Correspondence to I. A. Topol.

Ethics declarations

CONFLICT OF INTEREST

The authors declare no apparent or potential conflicts of interest related to the publication of this article.

Additional information

Translated by A. Dyomina

Russian Text © The Author(s), 2022, published in Rossiiskii Fiziologicheskii Zhurnal imeni I.M. Sechenova, 2022, Vol. 108, No. 10, pp. 1279–1290https://doi.org/10.31857/S0869813922100119.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Topol, I.A., Polyakova, I.S., Elykova, A.V. et al. Peculiarities of Endoplasmic Reticulum Stress Regulator XBP1 Expression in the Gut-Associated Lymphoid Tissue of Wistar Rats under Chronic Stress. J Evol Biochem Phys 58, 1583–1591 (2022). https://doi.org/10.1134/S002209302205026X

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S002209302205026X

Keywords:

Search

Navigation