The role of L-arginine and inducible nitric oxide synthase in intestinal permeability and bacterial translocation

Journal of Parenteral and Enteral Nutrition

Volumn 37, Issue 3, 2013, Pages 392-400

  Quirino, Iara Eliza Pacífico ^a   Cardoso, Valbert Nascimento ^a   Santos, Rosana Das Graças Carvalho Dos ^a   Evangelista, Warlley Pinheiro ^a   Arantes, Rosa Maria Esteves ^a   Fiúza, Jacqueline Araújo ^a,b   Glória, Maria Beatriz Abreu ^a   Alvarez Leite, Jacqueline Isaura ^a   Batista, Marina Andrade ^a   Correia, Maria Isabel Toulson Davisson ^a  

^a FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^b INSTITUTO OSWALDO CRUZ   (Brazil)

Author keywords

arginine supplementation; bacterial translocation; intestinal obstruction; intestinal permeability; nitric oxide knockout mice; polyamine

Indexed keywords

ARGININE; INDUCIBLE NITRIC OXIDE SYNTHASE; NITROGEN; POLYAMINE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BACTERIAL TRANSLOCATION; CALORIC INTAKE; COMPARATIVE STUDY; CONTROLLED STUDY; EDEMA; HISTOPATHOLOGY; ILEUM; INTESTINE MUCOSA PERMEABILITY; INTESTINE OBSTRUCTION; INTESTINE WALL; MALE; MORPHOMETRICS; MOUSE; NONHUMAN; POLYAMINE SYNTHESIS; POLYMORPHONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN INTAKE; SMALL INTESTINE; WEIGHT GAIN; WILD TYPE;

ANIMALS; ARGININE; BACTERIAL TRANSLOCATION; ESCHERICHIA COLI; ILEUM; INTESTINAL OBSTRUCTION; INTESTINE, SMALL; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; PERMEABILITY; POLYAMINES;

ANIMALIA; BACTERIA (MICROORGANISMS); MUS;

EID: 84876738480     PISSN: 01486071     EISSN: None     Source Type: Journal    
DOI: 10.1177/0148607112458325     Document Type: Article

References (48)

1. Fan J, Meng Q, Guo G, et al. Effects of early enteral nutrition supplemented with arginine on intestinal mucosal immunity in severely burned mice. Clin Nutr. 2010 ; 29: 124-130
2. Tan B, Li XG, Kong X, et al. Dietary L-arginine supplementation enhances the immune status in early-weaned piglets. Amino Acids. 2009 ; 37: 323-331
3. De Jonge WJ, Kwikkers KL, Te Velde AA, et al. Arginine deficiency affects early B cell maturation and lymphoid organ development in transgenic mice. J Clin Invest. 2002 ; 110: 1539-1548 (Pubitemid 35396924)
4. Sukhotnik I, Mogilner J, Krausz MM, et al. Oral arginine reduces gut mucosal injury caused by lipopolysaccharide in rat. J Surg Res. 2004 ; 122: 256-262 (Pubitemid 39535951)
5. Ersin S, Tuncyurek P, Esassolak M, et al. The prophylactic and therapeutic effects of glutamine and arginine enriched diets on radiation induced enteritis in rats. J Surg Res. 2000 ; 89: 121-125 (Pubitemid 30196514)
6. Gurbuz AT, Kunzelman J, Ratzer EE. Supplemental dietary arginine accelerates intestinal mucosal regeneration and enhances bacterial clearance following radiation enteritis in rats. J Surg Res. 1998 ; 74: 149-154 (Pubitemid 28270363)
7. Xie XQ, Shinozawa Y, Sasaki J, et al. The effects of arginine and selective nitric oxide synthase inhibitor on pathophysiology of sepsis in a CLP model. J Surg Res. 2008 ; 146: 298-303 (Pubitemid 351484141)
8. Aktan F. iNOS mediated nitric oxide production and its regulation. Life Sci. 2004 ; 75: 639-653 (Pubitemid 38686696)
9. Kubes P, McCafferty DM. Nitric oxide and intestinal inflammation. Am J Med. 2000 ; 109: 150-158
10. Naito Y, Takagi T, Ichikawa H, et al. A novel potent inhibitor of inducible nitric oxide inhibitor, ONO-1714, reduces intestinal ischemia-reperfusion injury in rats. Nitric Oxide. 2004 ; 10: 170-177 (Pubitemid 38668666)
11. Jia YX, Pan CS, Yang JH, et al. Altered L-arginine/nitric oxide synthase/nitric oxide pathway in the vascular adventitia of rats with sepsis. Clin Exp Pharmacol Physiol. 2006 ; 33: 1202-1208 (Pubitemid 44923909)
12. Strunk V, Hahnenkamp K, Schneuing M, Fischer LG, Rich GF. Selective iNOS inhibition prevents hypotension in septic rats while preserving endothelium-dependent vasodilatation. Anesth Analg. 2001 ; 92: 681-687 (Pubitemid 32185112)
13. Unno N, Wang H, Menconi MJ, et al. Inhibition of inducible nitric oxide synthase ameliorates endotoxin-induced gut mucosal barrier dysfunction in rats. Gastroenterology. 1997 ; 113: 1246-1257 (Pubitemid 27418978)
14. Hierholzer C, Kalff JC, Billiar TR, Bauer AJ, Tweardy DJ, Harbrecht BG. Induced nitric oxide promotes intestinal inflammation following hemorrhagic shock. Am J Physiol Gastrointest Liver Physiol. 2004 ; 286: G225 - G233
15. Barocelli E, Ballabeni V, Ghizzard P, et al. The selective inhibition of inducible nitric oxide synthase prevents intestinal ischemia-reperfusion injury in mice. Nitric Oxide. 2006 ; 14: 212-218
16. Katada K, Bihari A, Badhwar A, et al. Hindlimb ischemia/reperfusion- induced remote injury to the small intestine: role of inducible nitric-oxide synthase-derived nitric oxide. J Pharmacol Exp Ther. 2009 ; 329: 919-927
17. Sasaki M, Bharwani S, Jordan P, et al. Increased disease activity in eNOS-deficient mice in experimental colitis. Free Radic Biol Med. 2003 ; 35: 1679-1687 (Pubitemid 37532917)
18. Vallance BA, Dijkstra G, Qiu B, et al. Relative contributions of NOS isoforms during experimental colitis: endothelial-derived NOS maintains mucosal integrity. Am J Physiol Gastrointest Liver Physiol. 2004 ; 287: G865 - G874
19. Dahm PL, Thorne J, Myhre E, Grins E, Martensson L, Blomquist S. Intestinal and hepatic perfusion and metabolism in hypodynamic endotoxic shock: effects of nitric oxide synthase inhibition. Acta Anaesthesiol Scand. 1999 ; 43: 56-63 (Pubitemid 29014113)
20. Petersson J, Schreiber O, Steege A, et al. eNOS involved in colitis-induced mucosal blood flow increase. Am J Physiol Gastrointest Liver Physiol. 2007 ; 293: G1281 - G1287
21. Pedoto A, Tassiopoulos A, Oler A, et al. Treatment of septic shock in rats with nitric oxide synthase inhibitors and inhaled nitric oxide. Crit Care Med. 1999 ; 26: 2021-2028
22. Larquè E, Molina-Sabater M, Zamora S. Biological significance of dietary polyamines. Nutrition. 2007 ; 23: 87-95 (Pubitemid 44959765)
23. Zhang XP, Zhang J, Song Q, Chen H. Mechanism of acute pancreatitis complication with injury of intestinal barrier. J Zhejiang Univ Sci B. 2007 ; 12: 888-895
24. Zaloga GP, Siddiqui R, Terry C, Marik PE. Arginine: mediator or modulator of septicemia?. Nutr Clin Pract. 2004 ; 19: 201-215
25. Quirino IEP, Correia MITD, Cardoso VN. The impact of arginine on bacterial translocation in an intestinal obstruction model in rats. Clin Nutr. 2007 ; 26: 335-3450
26. Jorgensen VL, Nielsen SL, Espersen K, Perner A. Increased colorectal permeability in patients with severe sepsis and septic shock. Intensive Care Med. 2006 ; 32: 1790-1796 (Pubitemid 44607367)
27. Batista MA, Nicoli J, Martins FS, et al. Pretreatment with citrulline improves gut barrier after intestinal obstruction in mice. JPEN J Parenter Enteral Nutr. 2012 ; 36: 69-76
28. Santos RGC, Viana ML, Generoso SV, Arantes RME, Correia MITD, Cardoso VN. Glutamine supplementation decreases intestinal permeability and preserves gut mucosa integrity in an experimental mouse model. JPEN J Parenter Enteral Nutr. 2010 ; 34: 408-413
29. Vale SR, Glória MB. Determination of biogenic amines in cheese. J AOAC Int. 1997 ; 80: 1006-1012 (Pubitemid 127444492)
30. Kalil AC, Danner RL. L-arginine supplementation in sepsis: beneficial or harmful?. Curr Opin Crit Care. 2006 ; 12: 303-308 (Pubitemid 44078141)
31. Xie XQ, Shinozawa Y, Sasaki J, et al. The effects of ;arginine ;and selective inducible nitric oxide synthase inhibitor on pathophysiology of sepsis in a CLP model. J Surg Res. 2008 ; 146: 298-303 (Pubitemid 351484141)
32. Balzan S, Quadros CA, Cleva R, Ziberstein B, Cecconelo I. Bacterial translocation: overview of mechanisms and clinical impact. J Gastroenterol Hepatol. 2007 ; 22: 464-471 (Pubitemid 46435001)
33. Thomas S, Ramachandran A, Patra S, Vidyasagar S, Balasubramanian A. Nitric oxide protects the intestine from the damage induced by laparotomy and gut manipulation. J Surg Res. 2001 ; 99: 25-32 (Pubitemid 32613955)
34. Porras M, Martin MT, Yang PC, Jury J, Perdue MH, Vergara P. Correlation between cyclical epithelial barrier dysfunction on bacterial translocation in the relapses of intestinal inflammation. Inflamm Bowel Dis. 2006 ; 18: 843-852 (Pubitemid 44352711)
35. Hierholzer C, Kalff JC, Billiar TR, Bauer AJ, Tweardy DJ, Harbrecht B. Induced nitric oxide promotes intestinal inflammation following hemorrhagic shock. Am J Physiol Gastrointest Liver Physiol. 2003 ; 286: G226 - G233
36. Hardy I, Alany R, Russel B, Hardy G. Antimicrobial effects of arginine and nitrogen oxides and their potential role in septicemia. Curr Opin Clin Nutr Metab Care. 2006 ; 9: 222-232
37. Shang HF, Wang YY, Lai YN, Chiu WC, Yeh SL. Effects of arginine supplementation on mucosal immunity in rats with septic peritonitis. Clin Nutr. 2004 ; 23: 561-569
38. Sukhotnik I, Mogilner J, Krausz MM, Lurie M, Hirsh M, Coran AG. Oral arginine reduces gut mucosal injury caused by lipopolysaccharide in rat. J Sur Res. 2004 ; 122: 256-262 (Pubitemid 39535951)
39. Viana ML, Santos RGC, Generoso SV, Arantes RME, Correia MITD, Cardoso VN. Pretreatment with arginine preserves intestinal barrier integrity and reduces bacterial translocation in mice. Nutrition. 2010 ; 26: 218-223
40. Osaowska S, Neveux N, Nakib S, Lasserre V, Cynober L, Moinard C. Impairment of arginine metabolism in rats after massive intestinal resection: effect of parenteral nutrition supplemented nutrition with citrulline compared with arginine. Clin Sci. 2008 ; 115: 159-166
41. Gobert AP, Cheng Y, Akhtar M, et al. Protective role of arginase in a mouse model of colitis. J Immunol. 2004 ; 173: 2109-2117 (Pubitemid 38971649)
42. Wu G, Bazer FW, Davis TA, et al. Arginine metabolism and nutrition in growth, health and disease. Amino Acids. 2009 ; 37: 153-168
43. Moinard C, Cynober L, De Bandt JP. Polyamines: metabolism and implications in human diseases. Clin Nutr. 2005 ; 24: 184-197 (Pubitemid 40392801)
44. Czernichow B, Nsi-Emvo E, Galluser M, Gosse M, Raul F. Enteral supplementation with ornithine alpha ketoglutarate improves the early adaptive response to resection. Gut. 1997 ; 40: 67-72 (Pubitemid 27079753)
45. Noguchi Y, Meyer TA, Tiao G, Fischer JE, Hasselgren PO. Influence of septicemia and endotoxemia on polyamines metabolism in mucosa of small intestine in rats. Metabolism. 1996 ; 45: 28-33 (Pubitemid 26104264)
46. Duranton B, Schleiffer R, Gosse F, Raul F. Preventive administration of ornithine alpha-ketoglutarate improves mucosal repair after transient ischemia in rats. Crit Care Med. 1998 ; 26: 120-125 (Pubitemid 28028450)
47. Ochoa JB, Makarenkova V, Bansal V. A rational use of immune enhancing diets: when should we use dietary arginine supplementation?. Nutr Clin Pract. 2004 ; 19: 216-225 (Pubitemid 38747819)
48. Morris SM. Arginine: master and commander in innate immune responses. Sci Signal. 2010 ; 3: 27-31