Skip to main content
SpringerLink
Log in

Effect of taurine on intestinal recovery following intestinal ischemia-reperfusion injury in a rat

  • Original Article
  • Published:
Pediatric Surgery International Aims and scope Submit manuscript

Abstract

Purpose

Taurine (TAU) is a sulfur-containing amino acid that is involved in a diverse array of biological and physiological functions, including bile salt conjugation, osmoregulation, membrane stabilization, calcium modulation, anti-oxidation, and immunomodulation. Several studies have established that treatment with TAU significantly protects cerebral, cardiac and testicular injury from ischemia–reperfusion (IR). The purpose of the present study was to examine the effect of TAU on intestinal recovery and enterocyte turnover after intestinal IR injury in rats.

Methods

Male Sprague–Dawley rats were divided into four experimental groups: (1) Sham rats that underwent laparotomy, (2) Sham-TAU rats that underwent laparotomy and were treated with intraperitoneal (IP) TAU (250 mg/kg); (3) IR-rats that underwent occlusion of both superior mesenteric artery and portal vein for 30 min followed by 48 h of reperfusion, and (4) IR-TAU rats that underwent IR and were treated with IP TAU (250 mg/kg) immediately before abdominal closure. Intestinal structural changes, Park’s injury score, enterocyte proliferation and enterocyte apoptosis were determined 24 h following IR. The expression of Bax, Bcl-2, p-ERK and caspase-3 in the intestinal mucosa was determined using Western blot and immunohistochemistry.

Results

Treatment with TAU resulted in a significant decrease in Park’s injury score compared to IR animals. IR-TAU rats also demonstrated a significant increase in mucosal weight in jejunum and ileum, villus height in jejunum and ileum and crypt depth in ileum compared to IR animals. IR-TAU rats also experienced significantly lower apoptotic indices in jejunum and ileum which was accompanied by a higher Bcl-2/Bax ratio compared to IR animals.

Conclusions

Treatment with taurine prevents gut mucosal damage and inhibits intestinal epithelial cell apoptosis following intestinal IR in a rat.

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
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Haglund U, Bergqvist D (1999) Intestinal ischemia-the basics. Langenbecks Arch Surg 384:233–238

    Article  CAS  PubMed  Google Scholar 

  2. Young CM, Kingma SD, Neu J (2011) Ischemia-reperfusion and neonatal intestinal injury. J Pediatr 158(2 Suppl):e25–e28

    Article  PubMed  Google Scholar 

  3. Carden DL, Granger DN (2000) Pathophysiology of ischaemia-reperfusion injury. J Pathol 190:255–260

    Article  CAS  PubMed  Google Scholar 

  4. Granger DN, Hollwarth ME, Park DA (1986) Ishemia reperfusion injury: role of oxygen-derived free radicals. Acta Physiol Scand Suppl 548:47–52

    CAS  PubMed  Google Scholar 

  5. Yang Z, Deng Y, Su D, Tian J, Gao Y, He Z, Wang X (2013) TLR4 as receptor for HMGB1-mediated acute lung injury after liver ischemia/reperfusion injury. Lab Invest 93:792–800

    Article  CAS  PubMed  Google Scholar 

  6. Sánchez-Miralles A, Castellanos G, Badenes R, Conejero R (2013) Abdominal compartment syndrome and acute intestinal distress syndrome. Med Intensiva 37:99–109

    Article  PubMed  Google Scholar 

  7. Guzel A, Kanter M, Guzel A, Yucel AF, Erboga M (2013) Protective effect of curcumin on acute lung injury induced by intestinal ischaemia/reperfusion. Toxicol Ind Health 29:633–642

    Article  PubMed  Google Scholar 

  8. Schaffer SW, Jong CJ, Ito T, Azuma J (2014) Effect of taurine on ischemia-reperfusion injury. Amino Acids 46:21–30

    Article  CAS  PubMed  Google Scholar 

  9. Guler L, Tavlasoglu M, Yucel O, Guler A, Sahin MA, Kurkluoglu M, Sirin Y, Eken A, Gamsizkan M, Dakak M, Gurkok S, Genc O (2014) Taurine attenuates lung ischemia-reperfusion injury after lung transplantation in rats. J Anesth 28:347–353

    Article  PubMed  Google Scholar 

  10. Zhang Y, Yang L, Yang YJ, Liu XY, Jia JG, Qian JY, Wang KQ, Zuo J, Ge JB (2013) Low-dose taurine upregulates taurine transporter expression in acute myocardial ischemia. Int J Mol Med 31:817–824

    CAS  PubMed  Google Scholar 

  11. Sun M, Zhao YM, Gu Y, Xu C (2012) Therapeutic window of taurine against experimental stroke in rats. Transl Res 160:223–229

    Article  CAS  PubMed  Google Scholar 

  12. Abbasoğlu L, Kalaz EB, Soluk-Tekkeşin M, Olgaç V, Doğru-Abbasoğlu S, Uysal M (2012) Beneficial effects of taurine and carnosine in experimental ischemia/reperfusion injury in testis. Pediatr Surg Int 28:1125–1131

    Article  PubMed  Google Scholar 

  13. Haj B, Sukhotnik I, Shaoul R, Pollak Y, Coran AG, Bitterman A, Matter I (2014) Effect of ozone on intestinal recovery following intestinal ischemia-reperfusion injury in a rat. Pediatr Surg Int 30:181–188

    Article  PubMed  Google Scholar 

  14. Sukhotnik I, Slijper N, Pollak Y, Chemodanov E, Shaoul R, Coran AG, Mogilner JG (2011) Parenteral omega-3 fatty acids (Omegaven) modulate intestinal recovery after intestinal ischemia-reperfusion in a rat model. J Pediatr Surg 46:1353–1360

    Article  PubMed  Google Scholar 

  15. Chomczynski P (1993) A reagent for the single-step simultaneous isolation of RNA, DNA and proteins from cell and tissue samples. Bio Techniques 15:532–536

    CAS  Google Scholar 

  16. Park PO, Haglund U, Bulkley GB (1990) The sequence of development of intestinal tissue injury after strangulation ischemia and reperfusion. Surgery 107:574–580

    CAS  PubMed  Google Scholar 

  17. Wójcik OP, Koenig KL, Zeleniuch-Jacquotte A, Costa M, Chen Y (2010) The potential protective effects of Taurine on coronary heart disease. Atherosclerosis 208:19–25

    Article  PubMed Central  PubMed  Google Scholar 

  18. Redmond HP, Stapleton PP, Neary P, Bouchier-Hayes D (1998) Immunonutrition: the role of Taurine. Nutrition 14:599–604

    Article  CAS  PubMed  Google Scholar 

  19. Schaffer S, Azuma J, Takahashi K, Mozaffari M (2003) Why is Taurine cytoprotective? Adv Exp Med Biol 526:307–321

    Article  CAS  PubMed  Google Scholar 

  20. Rodrigues CM, Ma X, Linehan-Stieers C, Fan G, Kren BT (1999) Ursodeoxycholic acid prevents cytochrome c release in apoptosis by inhibiting mitochondrial membrane depolarization and channel formation. Cell Death Differ 6:842–854

    Article  CAS  PubMed  Google Scholar 

  21. Oz E, Erbaş D, Gelir E, Aricioğlu A (1999) Taurine and calcium interaction in protection of myocardium exposed to ischemic reperfusion injury. Gen Pharmacol 33:137–141

    Article  CAS  PubMed  Google Scholar 

  22. Pion PD, Kittleson MD, Thomas WP, Delellis LA, Rogers QR (1992) Response of cats with dilated cardiomyopathy to Taurine supplementation. J Am Vet Med Assoc 201:275–284

    CAS  PubMed  Google Scholar 

  23. Welty MC, Welty JD, McBroom MJ (1982) Effect of isoproterenol and Taurine on heart calcium in normal and cardiomyopathic hamsters. J Mol Cell Cardiol 14:353–357

    Article  CAS  PubMed  Google Scholar 

  24. Men X, Han S, Gao J, Cao G, Zhang L, Yu H, Lu H, Pu J (2010) Taurine protects against lung damage following limb ischemia reperfusion in the rat by attenuating endoplasmic reticulum stress-induced apoptosis. Acta Orthop 81:263–267

    Article  PubMed Central  PubMed  Google Scholar 

  25. Mozaffari MS, Abdelsayed R, Patel C, Wimborne H, Liu JY, Schaffer SW (2010) Differential effects of taurine treatment and taurine deficiency on the outcome of renal ischemia reperfusion injury. J Biomed Sci 24(Suppl 1):S32

    Article  Google Scholar 

  26. Guan W, Zhao Y, Xu C (2011) A Combined treatment with taurine and intra-arterial thrombolysis in an embolic model of stroke in rats: increased neuroprotective efficacy and extended therapeutic time window. Transl Stroke Res 2:80–91

    Article  CAS  PubMed  Google Scholar 

  27. Wei SM, Yan ZZ, Zhou J (2007) Beneficial effect of taurine on testicular ischemia-reperfusion injury in rats. Urology 70:1237–1242

    Article  PubMed  Google Scholar 

  28. Zhang F, Tong L, Qiao H, Dong X, Qiao G, Jiang H, Sun X (2008) Taurine attenuates multiple organ injury induced by intestinal ischemia reperfusion in rats. J Surg Res 149:101–109

    Article  CAS  PubMed  Google Scholar 

  29. Noda T, Iwakiri R, Fujimoto K, Matsuo S, Aw TY (1998) Programmed cell death induced by ischemia-reperfusion in rat intestinal mucosa. Am J Physiol 274:G270–G276

    CAS  PubMed  Google Scholar 

  30. Coopersmith CM, O’Donnell D, Gordon JI (1999) Bcl-2 inhibits ischemia-reperfusion-induced apoptosis in the intestinal epithelium of transgenic mice. Am J Physiol 276:G677–G682

    CAS  PubMed  Google Scholar 

  31. Han X, Yue J, Chesney RW (2009) Functional TauT protects against acute kidney injury. J Am Soc Nephrol 20:1323–1332

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  32. Gharibani PM, Modi J, Pan C, Menzie J, Ma Z, Chen PC, Tao R, Prentice H, Wu JY (2013) The mechanism of taurine protection against endoplasmic reticulum stress in an animal stroke model of cerebral artery occlusion and stroke-related conditions in primary neuronal cell culture. Adv Exp Med Biol 776:241–258

    Article  CAS  PubMed  Google Scholar 

  33. Kaplan B, Aricioglu A, Erbas D, Erbas S, Turkozkan N (1993) The effects of taurine on perfused heart muscle malondialdehyde levels. Gen Pharmacol 24:1411–1413

    Article  CAS  PubMed  Google Scholar 

  34. Ogino T, Than TA, Hosako M, Ozaki M, Omori M, Okada S (2009) Taurine chloramine: a possible oxidant reservoir. Adv Exp Med Biol 643:451–461

    Article  CAS  PubMed  Google Scholar 

  35. Kim C, Cha YN (2009) Production of reactive oxygen and nitrogen species in phagocytes is regulated by taurine chloramine. Adv Exp Med Biol 643:463–472

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Laboratory of Intestinal Adaptation and Recovery, The Bruce Rappaport Faculty of Medicine, Technion-Israel Institute of Technology, Haifa, Israel

    I. Sukhotnik, I. Aranovich, Y. Ben Shahar, N. Bitterman, Y. Pollak & D. Chepurov

  2. Department of Pediatric Surgery, Bnai Zion Medical Center, 47 Golomb St., P.O.B. 4940, Haifa, 31048, Israel

    I. Sukhotnik & I. Aranovich

  3. Department of Surgery, Carmel Medical Center, Haifa, Israel

    Y. Ben Shahar & A. Bitterman

  4. Department of Gastroenterology, Bnai Zion Medical Center, Haifa, Israel

    D. Berkowitz

  5. Section of Pediatric Surgery, C.S. Mott Children’s Hospital, University of Michigan Medical School, Ann Arbor, MI, USA

    A. G. Coran

Authors
  1. I. Sukhotnik
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. I. Aranovich
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Y. Ben Shahar
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. N. Bitterman
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Y. Pollak
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. D. Berkowitz
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. D. Chepurov
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. A. G. Coran
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. A. Bitterman
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to I. Sukhotnik.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sukhotnik, I., Aranovich, I., Ben Shahar, Y. et al. Effect of taurine on intestinal recovery following intestinal ischemia-reperfusion injury in a rat. Pediatr Surg Int 32, 161–168 (2016). https://doi.org/10.1007/s00383-015-3828-3

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00383-015-3828-3

Keywords

Search

Navigation