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Frontiers in veterinary science2022; 9; 947482; doi: 10.3389/fvets.2022.947482

Adaptive mechanisms in no flow vs. low flow ischemia in equine jejunum epithelium: Different paths to the same destination.

Abstract: Intestinal ischemia reperfusion injury (IRI) is a frequent complication of equine colic. Several mechanisms may be involved in adaptation of the intestinal epithelium to IRI and might infer therapeutic potential, including hypoxia-inducible factor (HIF) 1α, AMP-activated protein kinase (AMPK), nuclear factor-erythroid 2-related factor 2 (NRF2), and induction of autophagy. However, the mechanisms supporting adaptation and thus cellular survival are not completely understood yet. We investigated the activation of specific adaptation mechanisms in both no and low flow ischemia and reperfusion simulated in equine jejunum epithelium in vivo. We found an activation of HIF1α in no and low flow ischemia as indicated by increased levels of HIF1α target genes and phosphorylation of AMPKα tended to increase during ischemia. Furthermore, the protein expression of the autophagy marker LC3B in combination with decreased expression of nuclear-encoded mitochondrial genes indicates an increased rate of mitophagy in equine intestinal IRI, possibly preventing damage by mitochondria-derived reactive oxygen species (ROS). Interestingly, ROS levels were increased only shortly after the onset of low flow ischemia, which may be explained by an increased antioxidative defense, although NFR2 was not activated in this setup. In conclusion, we could demonstrate that a variety of adaptation mechanisms manipulating different aspects of cellular homeostasis are activated in IRI irrespective of the ischemia model, and that mitophagy might be an important factor for epithelial survival following small intestinal ischemia in horses that should be investigated further.
Publication Date: 2022-09-08 PubMed ID: 36157182PubMed Central: PMC9493374DOI: 10.3389/fvets.2022.947482Google Scholar: Lookup
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  • Journal Article

Summary

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The research article discusses the different adaptive mechanisms observed in both no flow and low flow ischemia conditions in the equine jejunum epithelium connected to intestinal ischemia reperfusion injury (IRI), which is a common problem with equine colic. They discovered that several adaptation mechanisms are apprehended during IRI irrespective of the ischemia model, indicating that mitophagy could be key for epithelial survival.

Adaptive Mechanisms in Intestinal Ischemia Reperfusion Injury

  • The researchers investigate the adaptive methods of the intestinal epithelium to Intestinal Ischemia Reperfusion Injury (IRI), a common issue linked to equine colic. This injury results from reduced blood flow, causing tissue damage and subsequent inflammation when the blood reinstates.
  • They look into specific mechanisms, including hypoxia-inducible factor 1α (HIF1α), AMP-activated protein kinase (AMPK), nuclear factor-erythroid 2-related factor 2 (NFR2), and autophagy induction. These mechanisms support adaptation and cellular survival, though their operations are not fully comprehended.
  • The activation of these mechanisms is examined in different conditions of no and low flow ischemia (a lack of blood flow and reduced blood flow, respectively), and their reperfusion (restoration of blood flow), specifically in the equine jejunum epithelium (part of the small intestine in horses).

Findings and Implications

  • The findings illustrate an activation of HIF1α in both no flow and low flow ischemia. This conclusion is drawn from observed elevated levels of HIF1α target genes and a tendency of AMPKα phosphorylation to increase during ischemia.
  • The researchers also find an increased rate of mitophagy (a type of autophagy where cells recycle their own components) in equine intestinal IRI, indicated by the protein expression of the autophagy marker LC3B alongside a reduced expression of nuclear-encoded mitochondrial genes.
  • This could suggest that mitophagy could help prevent damage caused by reactive oxygen species (ROS) originating from the mitochondria.
  • ROS levels were observed to increase briefly at the onset of low flow ischemia. This could be due to an increased antioxidative defense, although NFR2 was not activated in this situation.
  • The variety of adaptive mechanisms demonstrated in this research elucidates different aspects of cellular homeostasis and highlights the potential importance of mitophagy in terms of epithelial survival after small intestinal ischemia in horses, an area which requires further investigation.

Cite This Article

APA
Dengler F, Sternberg F, Grages M, Kästner SB, Verhaar N. (2022). Adaptive mechanisms in no flow vs. low flow ischemia in equine jejunum epithelium: Different paths to the same destination. Front Vet Sci, 9, 947482. https://doi.org/10.3389/fvets.2022.947482

Publication

ISSN: 2297-1769
NlmUniqueID: 101666658
Country: Switzerland
Language: English
Volume: 9
Pages: 947482

Researcher Affiliations

Dengler, Franziska
  • Department of Biochemical Sciences, Institute of Physiology, Pathophysiology and Biophysics, University of Veterinary Medicine, Vienna, Austria.
Sternberg, Felix
  • Department of Biochemical Sciences, Institute of Physiology, Pathophysiology and Biophysics, University of Veterinary Medicine, Vienna, Austria.
Grages, Marei
  • Clinic for Horses, University of Veterinary Medicine Hannover, Hannover, Germany.
Kästner, Sabine Br
  • Clinic for Horses, University of Veterinary Medicine Hannover, Hannover, Germany.
  • Small Animal Clinic, University of Veterinary Medicine Hannover, Hannover, Germany.
Verhaar, Nicole
  • Clinic for Horses, University of Veterinary Medicine Hannover, Hannover, Germany.

Conflict of Interest Statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

References

This article includes 71 references
  1. van der Linden MA, Laffont CM, van Sloet Oldruitenborgh-Oosterbaan MM. Prognosis in equine medical and surgical colic.. J Vet Intern Med (2003) 17:343–8.
  2. Moore RM, Muir WW, Granger DN. Mechanisms of gastrointestinal ischemia-reperfusion injury and potential therapeutic interventions: a review and its implications in the horse.. J Vet Intern Med (1995) 9:115–32.
  3. Blikslager A, Gonzalez L. Equine intestinal mucosal pathobiology.. Annu Rev Anim Biosci (2018) 6:157–75.
  4. Mallick IH, Yang W, Winslet MC, Seifalian AM. Ischemia-reperfusion injury of the intestine and protective strategies against injury.. Dig Dis Sci (2004) 49:1359–77.
  5. Pascoe PJ, McDonell WN, Trim CM, van Gorder J. Mortality rates and associated factors in equine colic operations - a retrospective study of 341 operations.. Can Vet J (1983) 24:76–85.
    pmc: PMC1790318pubmed: 17422234
  6. Kaufman JM, Nekouei O, Doyle AJ, Biermann NM. Clinical findings, diagnoses, and outcomes of horses presented for colic to a referral hospital in Atlantic Canada (2000-2015).. Can Vet J (2020) 61:281–8.
    pmc: PMC7020639pubmed: 32165752
  7. Hunt JM, Edwards GB, Clarke KW. Incidence, diagnosis and treatment of postoperative complications in colic cases.. Equine Vet J (1986) 18:264–70.
  8. Gerard MP, Blikslager AT, Roberts MC, Tate LP, Argenzio RA. The characteristics of intestinal injury peripheral to strangulating obstruction lesions in the equine small intestine.. Equine Vet J (1999) 31:331–5.
  9. El-Malkey NF, Alsemeh AE, Ashour W, Hassan NH, Edrees HM. Fetuin-A exerts a protective effect against experimentally induced intestinal ischemia/reperfusion by suppressing autophagic cell death.. Exp Biol Med (2021) 246:1307–17.
    doi: 10.1177/1535370221995207pmc: PMC8371312pubmed: 33653159google scholar: lookup
  10. VanderBroek AR, Engiles JB, Kästner SB, Kopp V, Verhaar N, Hopster K. Protective effects of dexmedetomidine on small intestinal ischaemia-reperfusion injury in horses.. Equine Vet J (2021) 53:569–78.
    doi: 10.1111/evj.13337pubmed: 32862437google scholar: lookup
  11. Thoefner MB, Ersbøll AK, Jensen AL, Hesselholt M. Factor analysis of the interrelationships between clinical variables in horses with colic.. Prev Vet Med (2001) 48:201–14.
    doi: 10.1016/s0167-5877(00)00193-8pubmed: 11182463google scholar: lookup
  12. Grootjans J, Lenaerts K, Buurman WA, Dejong CH, Derikx JP. Life and death at the mucosal-luminal interface: New perspectives on human intestinal ischemia-reperfusion.. World J Gastroenterol (2016) 22:2760–70.
    doi: 10.3748/wjg.v22.i9.2760pmc: PMC4777998pubmed: 26973414google scholar: lookup
  13. Verhaar N, Buhr N de, Köckritz-Blickwede M von, Hewicker-Trautwein M, Pfarrer C, Mazzuoli-Weber G. Ischaemic postconditioning reduces apoptosis in experimental jejunal ischaemia in horses.. BMC Vet Res (2021) 17:175.
    doi: 10.1186/s12917-021-02877-ypmc: PMC8077964pubmed: 33902575google scholar: lookup
  14. Verhaar N, Pfarrer C, Neudeck S, König K, Rohn K, Twele L. Preconditioning with lidocaine and xylazine in experimental equine jejunal ischaemia.. Equine Vet J (2021) 53:125–33.
    doi: 10.1111/evj.13251pubmed: 32119148google scholar: lookup
  15. Verhaar N, Breves G, Hewicker-Trautwein M, Pfarrer C, Rohn K, Burmester M. The effect of ischaemic postconditioning on mucosal integrity and function in equine jejunal ischaemia.. Equine Vet J (2022) 54:427–37.
    doi: 10.1111/evj.13450pubmed: 34003501google scholar: lookup
  16. König KS, Verhaar N, Hopster K, Pfarrer C, Neudeck S, Rohn K. Ischaemic preconditioning and pharmacological preconditioning with dexmedetomidine in an equine model of small intestinal ischaemia-reperfusion.. PLoS ONE (2020) 15:e0224720.
  17. Fandrey J, Schödel J, Eckardt K-U, Katschinski DM, Wenger RH. Now a Nobel gas: oxygen.. Pflugers Arch (2019) 471:1343–58.
    doi: 10.1007/s00424-019-02334-8pubmed: 31754831google scholar: lookup
  18. Semenza GL. Oxygen sensing, hypoxia-inducible factors, and disease pathophysiology.. Annu Rev Pathol (2014) 9:47–71.
  19. Bauck AG, Grosche A, Morton AJ, Graham AS, Vickroy TW, Freeman DE. Effect of lidocaine on inflammation in equine jejunum subjected to manipulation only and remote to intestinal segments subjected to ischemia.. Am J Vet Res (2017) 78:977–89.
    doi: 10.2460/ajvr.78.8.977pubmed: 28738006google scholar: lookup
  20. Ceulaer K de, Delesalle C, van Elzen R, van Brantegem L, Weyns A, van Ginneken C. Morphological changes in the small intestinal smooth muscle layers of horses suffering from small intestinal strangulation. Is there a basis for predisposition for reduced contractility?. Equine Vet J (2011) 43:439–45.
  21. Hardie DG. AMPK–sensing energy while talking to other signaling pathways.. Cell Metab (2014) 20:939–52.
    doi: 10.1016/j.cmet.2014.09.013pmc: PMC5693325pubmed: 25448702google scholar: lookup
  22. Herzig S, Shaw RJ. AMPK: guardian of metabolism and mitochondrial homeostasis.. Nat Rev Mol Cell Biol (2018) 19:121–35.
    doi: 10.1038/nrm.2017.95pmc: PMC5780224pubmed: 28974774google scholar: lookup
  23. Mungai PT, Waypa GB, Jairaman A, Prakriya M, Dokic D, Ball MK. Hypoxia triggers AMPK activation through reactive oxygen species-mediated activation of calcium release-activated calcium channels.. Mol Cell Biol (2011) 31:3531–45.
    doi: 10.1128/MCB.05124-11pmc: PMC3165558pubmed: 21670147google scholar: lookup
  24. Dengler F. Activation of AMPK under hypoxia: many roads leading to Rome.. Int J Mol Sci (2020) 21:2428.
    doi: 10.3390/ijms21072428pmc: PMC7177550pubmed: 32244507google scholar: lookup
  25. Qi D, Young LH. AMPK: energy sensor and survival mechanism in the ischemic heart.. Trends Endocrinol Metab (2015) 26:422–9.
    doi: 10.1016/j.tem.2015.05.010pmc: PMC4697457pubmed: 26160707google scholar: lookup
  26. Hayes HV, Wolfe V, O'Connor M, Levinsky NC, Piraino G, Zingarelli B. Deficiency of AMPKα1 exacerbates intestinal injury and remote acute lung injury in mesenteric ischemia and reperfusion in mice.. Int J Mol Sci (2021) 22:9911.
    doi: 10.3390/ijms22189911pmc: PMC8468919pubmed: 34576076google scholar: lookup
  27. Dengler F, Gäbel G. The fast lane of hypoxic adaptation: glucose transport is modulated via a HIF-hydroxylase-AMPK-axis in jejunum epithelium.. Int J Mol Sci (2019) 20:4993.
    doi: 10.3390/ijms20204993pmc: PMC6834319pubmed: 31601024google scholar: lookup
  28. Dengler F, Rackwitz R, Pfannkuche H, Gäbel G. Glucose transport across lagomorph jejunum epithelium is modulated by AMP-activated protein kinase (AMPK) under hypoxia.. J Appl Physiol (1985) 123:1487–500.
  29. Haq S, Grondin J, Banskota S, Khan WI. Autophagy: roles in intestinal mucosal homeostasis and inflammation.. J Biomed Sci (2019) 26:19.
    doi: 10.1186/s12929-019-0512-2pmc: PMC6375151pubmed: 30764829google scholar: lookup
  30. Han X, Tai H, Wang X, Wang Z, Zhou J, Wei X. AMPK activation protects cells from oxidative stress-induced senescence via autophagic flux restoration and intracellular NAD(+) elevation.. Aging Cell (2016) 15:416–27.
    doi: 10.1111/acel.12446pmc: PMC4854918pubmed: 26890602google scholar: lookup
  31. Murrow L, Debnath J. Autophagy as a stress-response and quality-control mechanism: implications for cell injury and human disease.. Annu Rev Pathol (2013) 8:105–37.
  32. Wen J, Xu B, Sun Y, Lian M, Li Y, Lin Y. Paeoniflorin protects against intestinal ischemia/reperfusion by activating LKB1/AMPK and promoting autophagy.. Pharmacol Res (2019) 146:104308.
    doi: 10.1016/j.phrs.2019.104308pubmed: 31181335google scholar: lookup
  33. Wu M-Y, Yiang G-T, Liao W-T, Tsai AP-Y, Cheng Y-L, Cheng P-W. Current mechanistic concepts in ischemia and reperfusion injury.. Cell Physiol Biochem (2018) 46:1650–67.
    doi: 10.1159/000489241pubmed: 29694958google scholar: lookup
  34. Zhang Y, Liu D, Hu H, Zhang P, Xie R, Cui W. HIF-1α/BNIP3 signaling pathway-induced-autophagy plays protective role during myocardial ischemia-reperfusion injury.. Biomed Pharmacother (2019) 120:109464.
    doi: 10.1016/j.biopha.2019.109464pubmed: 31590128google scholar: lookup
  35. Mariño G, Niso-Santano M, Baehrecke EH, Kroemer G. Self-consumption: the interplay of autophagy and apoptosis.. Nat Rev Mol Cell Biol (2014) 15:81–94.
    doi: 10.1038/nrm3735pmc: PMC3970201pubmed: 24401948google scholar: lookup
  36. Ma S, Wang Y, Chen Y, Cao F. The role of the autophagy in myocardial ischemia/reperfusion injury.. Biochim Biophys Acta (2015) 1852:271–6.
    doi: 10.1016/j.bbadis.2014.05.010pubmed: 24859226google scholar: lookup
  37. Hao M, Zhu S, Hu L, Zhu H, Wu X, Li Q. Myocardial ischemic postconditioning promotes autophagy against ischemia reperfusion injury via the activation of the nNOS/AMPK/mTOR pathway.. Int J Mol Sci (2017) 18:614.
    doi: 10.3390/ijms18030614pmc: PMC5372630pubmed: 28287478google scholar: lookup
  38. Huang Q, Lou T, Wang M, Xue L, Lu J, Zhang H. Compound K inhibits autophagy-mediated apoptosis induced by oxygen and glucose deprivation/reperfusion via regulating AMPK-mTOR pathway in neurons.. Life Sci (2020) 254:117793.
    doi: 10.1016/j.lfs.2020.117793pubmed: 32416164google scholar: lookup
  39. Caleb I, Erlitz L, Telek V, Vecsernyés M, Sétáló G, Hardi P. Characterizing autophagy in the cold ischemic injury of small bowel grafts: evidence from rat jejunum.. Metabolites (2021) 11:396.
    doi: 10.3390/metabo11060396pmc: PMC8234201pubmed: 34204418google scholar: lookup
  40. Li Y, Luo Y, Li B, Niu L, Liu J, Duan X. miRNA-182/Deptor/mTOR axis regulates autophagy to reduce intestinal ischaemia/reperfusion injury.. J Cell Mol Med (2020) 24:7873–83.
    doi: 10.1111/jcmm.15420pmc: PMC7348187pubmed: 32510855google scholar: lookup
  41. Cadenas S. ROS and redox signaling in myocardial ischemia-reperfusion injury and cardioprotection.. Free Radic Biol Med (2018) 117:76–89.
  42. Vatistas NJ, Snyder JR, Nieto J, Hildebrand SV, Woliner MJ, Harmon FA. Morphologic changes and xanthine oxidase activity in the equine jejunum during low flow ischemia and reperfusion.. Am J Vet Res (1998) 59:772–6.
    pubmed: 9622750
  43. Hilton H, Nieto JE, Moore PF, Harmon FA, Naydan DK, Snyder JR. Expression of cyclooxygenase genes in the jejunum of horses during low-flow ischemia and reperfusion.. Am J Vet Res (2011) 72:681–6.
    doi: 10.2460/ajvr.72.5.681pubmed: 21529221google scholar: lookup
  44. Reichert C, Kästner SB, Hopster K, Rohn K, Rötting AK. Use of micro-lightguide spectrophotometry for evaluation of microcirculation in the small and large intestines of horses without gastrointestinal disease.. Am J Vet Res (2014) 75:990–6.
    doi: 10.2460/ajvr.75.11.990pubmed: 25350089google scholar: lookup
  45. Xie F, Xiao P, Chen D, Xu L, Zhang B. miRDeepFinder: a miRNA analysis tool for deep sequencing of plant small RNAs.. Plant Mol Biol (2012) 80:75–84.
    doi: 10.1007/s11103-012-9885-2pubmed: 22290409google scholar: lookup
  46. Kehrer JP, Paraidathathu T. The use of fluorescent probes to assess oxidative processes in isolated-perfused rat heart tissue.. Free Radic Res Commun (1992) 16:217–25.
    doi: 10.3109/10715769209049175pubmed: 1505782google scholar: lookup
  47. Ko S-F, Chen K-H, Wallace CG, Yang C-C, Sung P-H, Shao P-L. Protective effect of combined therapy with hyperbaric oxygen and autologous adipose-derived mesenchymal stem cells on renal function in rodent after acute ischemia-reperfusion injury.. Am J Transl Res (2020) 12:3272–87.
    pmc: PMC7407680pubmed: 32774699
  48. Soares RO, Losada DM, Jordani MC, Évora P, Castro-E-Silva O. Ischemia/reperfusion injury revisited: an overview of the latest pharmacological strategies.. Int J Mol Sci (2019) 20:5034.
    doi: 10.3390/ijms20205034pmc: PMC6834141pubmed: 31614478google scholar: lookup
  49. Albrecht M, Zitta K, Bein B, Wennemuth G, Broch O, Renner J. Remote ischemic preconditioning regulates HIF-1α levels, apoptosis and inflammation in heart tissue of cardiosurgical patients: a pilot experimental study.. Basic Res Cardiol (2013) 108:314.
    doi: 10.1007/s00395-012-0314-0pubmed: 23203207google scholar: lookup
  50. Hummitzsch L, Zitta K, Berndt R, Wong YL, Rusch R, Hess K. Remote ischemic preconditioning attenuates intestinal mucosal damage: insight from a rat model of ischemia-reperfusion injury.. J Transl Med (2019) 17:136.
    doi: 10.1186/s12967-019-1885-4pmc: PMC6489261pubmed: 31036020google scholar: lookup
  51. Kant R, Diwan V, Jaggi AS, Singh N, Singh D. Remote renal preconditioning-induced cardioprotection: a key role of hypoxia inducible factor-prolyl 4-hydroxylases.. Mol Cell Biochem (2008) 312:25–31.
    doi: 10.1007/s11010-008-9717-5pubmed: 18273560google scholar: lookup
  52. Levine B, Kroemer G. Autophagy in the pathogenesis of disease.. Cell (2008) 132:27–42.
    doi: 10.1016/j.cell.2007.12.018pmc: PMC2696814pubmed: 18191218google scholar: lookup
  53. Klionsky DJ, Abdel-Aziz AK, Abdelfatah S, Abdellatif M, Abdoli A, Abel S. Guidelines for the use and interpretation of assays for monitoring autophagy (4th edition)1.. Autophagy (2021) 17:1–382.
  54. Zhang Z, Singh R, Aschner M. Methods for the detection of autophagy in mammalian cells.. Curr Protoc Toxicol (2016) 69:20.12.1–20.12.26.
    doi: 10.1002/cptx.11pmc: PMC4982470pubmed: 27479363google scholar: lookup
  55. Grosche A, Morton AJ, Graham AS, Sanchez LC, Blikslager AT, Polyak MM. Ultrastructural changes in the equine colonic mucosa after ischaemia and reperfusion.. Equine Vet J Suppl (2011) 43:8–15.
  56. Kleinbongard P, Skyschally A, Heusch G. Cardioprotection by remote ischemic conditioning and its signal transduction.. Pflugers Arch (2017) 469:159–81.
    doi: 10.1007/s00424-016-1922-6pubmed: 27928644google scholar: lookup
  57. Kalogeris T, Bao Y, Korthuis RJ. Mitochondrial reactive oxygen species: a double edged sword in ischemia/reperfusion vs preconditioning.. Redox Biol (2014) 2:702–14.
    doi: 10.1016/j.redox.2014.05.006pmc: PMC4060303pubmed: 24944913google scholar: lookup
  58. Seppet E, Gruno M, Peetsalu A, Gizatullina Z, Nguyen HP, Vielhaber S. Mitochondria and energetic depression in cell pathophysiology.. Int J Mol Sci (2009) 10:2252–303.
    doi: 10.3390/ijms10052252pmc: PMC2695278pubmed: 19564950google scholar: lookup
  59. Mata A, Cadenas S. The antioxidant transcription factor Nrf2 in cardiac ischemia-reperfusion injury.. Int J Mol Sci (2021) 22:11939.
    doi: 10.3390/ijms222111939pmc: PMC8585042pubmed: 34769371google scholar: lookup
  60. Bhattacharyya A, Chattopadhyay R, Mitra S, Crowe SE. Oxidative stress: an essential factor in the pathogenesis of gastrointestinal mucosal diseases.. Physiol Rev (2014) 94:329–54.
    doi: 10.1152/physrev.00040.2012pmc: PMC4044300pubmed: 24692350google scholar: lookup
  61. Jin C, Fu W-L, Zhang D-D, Xing W-W, Xia W-R, Wei Z. The protective role of IL-1Ra on intestinal ischemia reperfusion injury by anti-oxidative stress via Nrf2/HO-1 pathway in rat.. Biomed J (2019) 42:36–45.
    doi: 10.1016/j.bj.2018.11.001pmc: PMC6468113pubmed: 30987703google scholar: lookup
  62. Yan J, Li J, Zhang L, Sun Y, Jiang J, Huang Y. Nrf2 protects against acute lung injury and inflammation by modulating TLR4 and Akt signaling.. Free Radic Biol Med (2018) 121:78–85.
  63. Zhang Y, Xu Z, Wang H, Dong Y, Shi HN, Culley DJ. Anesthetics isoflurane and desflurane differently affect mitochondrial function, learning, and memory.. Ann Neurol (2012) 71:687–98.
    doi: 10.1002/ana.23536pmc: PMC3942786pubmed: 22368036google scholar: lookup
  64. Wang J, Sun J, Qiao S, Li H, Che T, Wang C. Effects of isoflurane on complex II-associated mitochondrial respiration and reactive oxygen species production: Roles of nitric oxide and mitochondrial KATP channels.. Mol Med Rep (2019) 20:4383–90.
    doi: 10.3892/mmr.2019.10658pubmed: 31545457google scholar: lookup
  65. Hartmann RM, Licks F, Schemitt EG, Colares JR, do Couto Soares M, Zabot GP. Protective effect of glutamine on the main and adjacent organs damaged by ischemia-reperfusion in rats.. Protoplasma (2017) 254:2155–68.
    doi: 10.1007/s00709-017-1102-3pubmed: 28382390google scholar: lookup
  66. Wang A-L, Niu Q, Shi N, Wang J, Jia X-F, Lian H-F. Glutamine ameliorates intestinal ischemia-reperfusion Injury in rats by activating the Nrf2/Are signaling pathway.. Int J Clin Exp Pathol (2015) 8:7896–904.
    pmc: PMC4555682pubmed: 26339354
  67. Tahir M, Arshid S, Fontes B, Castro MS, Luz IS, Botelho KL. Analysis of the effect of intestinal ischemia and reperfusion on the rat neutrophils proteome.. Front Mol Biosci (2018) 5:89.
    doi: 10.3389/fmolb.2018.00089pmc: PMC6281993pubmed: 30555831google scholar: lookup
  68. Gutiérrez-Sánchez G, García-Alonso I, Gutiérrez Sáenz de Santa María J, Alonso-Varona A, La Herrero de Parte B. Antioxidant-based therapy reduces early-stage intestinal ischemia-reperfusion injury in rats.. Antioxidants (2021) 10:853.
    doi: 10.3390/antiox10060853pmc: PMC8226848pubmed: 34071753google scholar: lookup
  69. Blikslager AT, Roberts MC, Gerard MP, Argenzio RA. How important is intestinal reperfusion injury in horses?. J Am Vet Med Assoc (1997) 211:1387–9.
    pubmed: 9394886
  70. Laws EG, Freeman DE. Significance of reperfusion injury after venous strangulation obstruction of equine jejunum.. J Invest Surg (1995) 8:263–70.
    doi: 10.3109/08941939509031600pubmed: 8519742google scholar: lookup
  71. Graham AS, Grosche A, Morton AJ, Polyak MM, Freeman DE. In vitro and in vivo responses of mucosa from the large colon of horses to ischemia and reperfusion.. Am J Vet Res (2011) 72:982–9.
    doi: 10.2460/ajvr.72.7.982pubmed: 21728860google scholar: lookup

Citations

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  1. Windhaber C, Heckl A, Csukovich G, Pratscher B, Burgener IA, Biermann N, Dengler F. A matter of differentiation: equine enteroids as a model for the in vivo intestinal epithelium. Vet Res 2024 Mar 16;55(1):30.
    doi: 10.1186/s13567-024-01283-0pubmed: 38493107google scholar: lookup
  2. Dengler F, Domenig O, Kather S, Burgener IA, Steiner JM, Heilmann RM. Dysregulation of intestinal epithelial electrolyte transport in canine chronic inflammatory enteropathy and the role of the renin-angiotensin-aldosterone-system. Front Vet Sci 2023;10:1217839.
    doi: 10.3389/fvets.2023.1217839pubmed: 37720474google scholar: lookup
  3. Verhaar N, de Buhr N, von Köckritz-Blickwede M, Dümmer K, Hewicker-Trautwein M, Pfarrer C, Dengler F, Kästner S. Hypoxia signaling in the equine small intestine: Expression and distribution of hypoxia inducible factors during experimental ischemia. Front Vet Sci 2023;10:1110019.
    doi: 10.3389/fvets.2023.1110019pubmed: 36908508google scholar: lookup