Attenuation of sepsis-induced organ injury in mice by vitamin C

Journal of Parenteral and Enteral Nutrition

Volumn 38, Issue 7, 2014, Pages 825-839

  Fisher, Bernard J ^a   Kraskauskas, Donatas ^a   Martin, Erika J ^b   Farkas, Daniela ^a   Puri, Puneet ^a   Massey, H Davis ^b   Idowu, Michael O ^b   Brophy, Donald F ^b   Voelkel, Norbert F ^a   Fowler, Alpha A ^a   Natarajan, Ramesh ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

Author keywords

coagulation; inflammation; L gulono lactone oxidase; multiple organ dysfunction syndrome; sepsis; vitamin C

Indexed keywords

ALANINE AMINOTRANSFERASE; ASCORBIC ACID; ASPARTATE AMINOTRANSFERASE; CHITINASE; CHITINASE 3 LIKE 3; GELATINASE B; GLYCOSIDASE; NEUTROPHIL GELATINASE ASSOCIATED LIPOCALIN; SODIUM CHLORIDE; THROMBOMODULIN; TISSUE FACTOR PATHWAY INHIBITOR; UNCLASSIFIED DRUG; GULONOLACTONE OXIDASE; VITAMIN;

ACUTE KIDNEY FAILURE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASCORBIC ACID DEFICIENCY; BLOOD CLOTTING; CONTROLLED STUDY; LIVER INJURY; MOUSE; MULTIPLE ORGAN FAILURE; NEUTROPHIL LYMPHOCYTE RATIO; NONHUMAN; PERITONITIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEPSIS; THROMBOCYTE AGGREGATION; THROMBOELASTOGRAPHY; VISCOELASTICITY; ANIMAL; BLOOD CELL; COMPLICATION; DEFICIENCY; INFUSION; KIDNEY; KNOCKOUT MOUSE; LIVER; LUNG; METABOLISM;

GULO; MUS;

ANIMALS; ASCORBIC ACID; ASCORBIC ACID DEFICIENCY; BLOOD CELLS; BLOOD COAGULATION; INFUSIONS, PARENTERAL; KIDNEY; L-GULONOLACTONE OXIDASE; LIVER; LUNG; MICE, KNOCKOUT; MULTIPLE ORGAN FAILURE; SEPSIS; VITAMINS;

EID: 84908247494     PISSN: 01486071     EISSN: 19412444     Source Type: Journal    
DOI: 10.1177/0148607113497760     Document Type: Article

References (53)

1. Vincent JL, Rello J, Marshall J, et al. International study of the prevalence and outcomes of infection in intensive care units. JAMA. 2009 ; 302: 2323-2329
2. Annane D, Bellissant E, Cavaillon JM. Septic shock. Lancet. 2005 ; 365: 63-78
3. Esmon CT. Sepsis. A myriad of responses. Lancet. 2001 ;: S61
4. Ware LB, Matthay MA. The acute respiratory distress syndrome. N Engl J Med. 2000 ; 342: 1334-1349
5. Edelstein CL, Schrier RW Disease of the Kidney and Urinary Tract. Schrier RW, ed. Philadelphia, PA: Lippincott Williams and Wilkins ; 2007: 930-961.
6. Mehta RL, Bouchar J, Soroko SB, et al. Sepsis as a cause and consequence of acute kidney injury: program to improve care in acute renal disease. Intensive Care Med. 2011 ; 37: 241-248
7. Deutschman CS, Cereda M, Ochroch EA, Raj NR. Sepsis-induced cholestasis, steatosis, hepatocellular injury, and impaired hepatocellular regeneration are enhanced in interleukin-6-/- mice. Crit Care Med. 2006 ; 34: 2613-2620
8. Regel G, Grotz M, Weltner T, Sturm JA, Tscherne H. Pattern of organ failure following severe trauma. World J Surg. 1996 ; 20: 422-429
9. Schouten M, Wiersinga WJ, Levi M, van der Poll T. Inflammation, endothelium, and coagulation in sepsis. J Leukoc Biol. 2008 ; 83: 536-545
10. Bastarache JA, Wang L, Wang Z, Albertine KH, Matthay MA, Ware LB. Intra-alveolar tissue factor pathway inhibitor is not sufficient to block tissue factor procoagulant activity. Am J Physiol Lung Cell Mol Physiol. 2008 ; 294: L874 - L881
11. Li W, Maeda N, Beck MA. Vitamin C deficiency increases the lung pathology of influenza virus-infected gulo-/- mice. J Nutr. 2006 ; 136: 2611-2616
12. Gaut JP, Belaaouaj A, Byun J, et al. Vitamin C fails to protect amino acids and lipids from oxidation during acute inflammation. Free Radic Biol Med. 2006 ; 40: 1494-1501
13. Borrelli E, Roux-Lombard P, Grau GE, et al. Plasma concentrations of cytokines, their soluble receptors, and antioxidant vitamins can predict the development of multiple organ failure in patients at risk. Crit Care Med. 1996 ; 24: 392-397
14. Galley HF, Davies MJ, Webster NR. Ascorbyl radical formation in patients with sepsis: effect of ascorbate loading. Free Radic Biol Med. 1996 ; 20: 139-143
15. Evans RM, Currie L, Campbell A. The distribution of ascorbic acid between various cellular components of blood, in normal individuals, and its relation to the plasma concentration. Br J Nutr. 1982 ; 47: 473-482
16. Bergsten P, Amitai G, Kehrl J, Dhariwal KR, Klein HG, Levine M. Millimolar concentrations of ascorbic acid in purified human mononuclear leukocytes. Depletion and reaccumulation. J Biol Chem. 1990 ; 265: 2584-2587
17. Leibovitz B, Siegel BV. Ascorbic acid and the immune response. Adv Exp Med Biol. 1981 ; 135: 1-25
18. Hemila H, Douglas RM. Vitamin C and acute respiratory infections. Int J Tuberc Lung Dis. 1999 ; 3: 756-761
19. Fisher BJ, Seropian IM, Kraskauskas D, et al. Ascorbic acid attenuates lipopolysaccharide-induced acute lung injury. Crit Care Med. 2011 ; 39: 1454-1460
20. Fisher BJ, Kraskauskas D, Martin EJ, et al. Mechanisms of attenuation of abdominal sepsis induced acute lung injury by ascorbic acid. Am J Physiol Lung Cell Mol Physiol. 2012 ; 303: L20 - L32
21. Nishikimi M, Fukuyama R, Minoshima S, Shimizu N, Yagi K. Cloning and chromosomal mapping of the human nonfunctional gene for L-gulono-gamma-lactone oxidase, the enzyme for L-ascorbic acid biosynthesis missing in man. J Biol Chem. 1994 ; 269: 13685-13688
22. Maeda N, Hagihara H, Nakata Y, Hiller S, Wilder J, Reddick R. Aortic wall damage in mice unable to synthesize ascorbic acid. Proc Natl Acad Sci U S A. 2000 ; 97: 841-846
23. Vissers MC, Wilkie RP. Ascorbate deficiency results in impaired neutrophil apoptosis and clearance and is associated with up-regulation of hypoxia-inducible factor 1alpha. J Leukoc Biol. 2007 ; 81: 1236-1244
24. Harrison FE, Yu SS, Van Den Bossche KL, Li L, May JM, McDonald MP. Elevated oxidative stress and sensorimotor deficits but normal cognition in mice that cannot synthesize ascorbic acid. J Neurochem. 2008 ; 106: 1198-1208
25. Kim H, Bae S, Yu Y, et al. The analysis of vitamin C concentration in organs of gulo(-/-) mice upon vitamin C withdrawal. Immune Netw. 2012 ; 12: 18-26
26. Henry ML, Davidson LB, Wilson JE, et al. Whole blood aggregation and coagulation in db/db and ob/ob mouse models of type 2 diabetes. Blood Coagul Fibrinolysis. 2008 ; 19: 124-34
27. Mazzaccara C, Labruna G, Cito G, et al. Age-related reference intervals of the main biochemical and hematological parameters in C57BL/6J, 129SV/EV and C3H/HeJ mouse strains. PLoS One. 2008 ; 3: e3772
28. Zahorec R. Ratio of neutrophil to lymphocyte counts - rapid and simple parameter of systemic inflammation and stress in critically ill. Bratisl Lek Listy. 2001 ; 102: 5-14
29. Angrinia MA, Leslieb JC. Vitamin C attenuates the physiological and behavioural changes induced by long-term exposure to noise. Behav Pharmacol. 2012 ; 23: 119-125
30. Chatterjee A, Dimitropoulou C, Drakopanayiotakis F. Heat shock protein 90 inhibitors prolong survival, attenuate inflammation, and reduce lung injury in murine sepsis. Am J Respir Crit Care Med. 2007 ; 176: 667-675
31. Vincent JL, Ferreira F, Moreno R. Scoring systems for assessing organ dysfunction and survival. Crit Care Clin. 2000 ; 16: 353-366
32. Wickel DJ, Cheadle WG, Mercer-Jones MA, Garrison RN. Poor outcome from peritonitis is caused by disease acuity and organ failure, not recurrent peritoneal infection. Ann Surg. 1997 ; 225: 744-756
33. Schrier RW, Wang W. Acute renal failure and sepsis. N Engl J Med. 2004 ; 351: 159-169
34. Brivet FG, Kleinknecht DJ, Loirat P, Landais PJ. Acute renal failure in intensive care units - causes, outcome, and prognostic factors of hospital mortality: a prospective, multicenter study. French Study Group on Acute Renal Failure. Crit Care Med. 1996 ; 24: 192-198
35. Urbschat A, Obermüller N, Haferkamp A. Biomarkers of kidney injury. Biomarkers. 2011 ; 16: S22 - S30
36. Jin HM, Copeland NG, Gilbert DJ, Jenkins NA, Kirkpatrick RB, Rosenberg M. Genetic characterization of the murine YM1 gene and identification of a cluster of highly homologous genes. Genomics. 1998 ; 54: 316-322
37. Johansen JS, Krabbe KS, Moller K, Pedersen BK. Circulating YKL-40 levels during human endotoxemia. Clin Exp Immunol. 2005 ; 140: 343-348
38. Hattori N, Oda S, Sadahiro T, et al. YKL-40 identified by proteomic analysis as a biomarker of sepsis. Shock. 2009 ; 32: 393-400
39. Wu L, Tiwari MM, Messer KJ, et al. Peritubular capillary dysfunction and renal tubular epithelial cell stress following lipopolysaccharide administration in mice. Am J Physiol Renal Physiol. 2007 ; 292: F261 - F268
40. Stojiljkovic N, Stoiljkovic M, Randjelovic P, Veljkovic S, Mihailovic D. Cytoprotective effect of vitamin C against gentamicin-induced acute kidney injury in rats. Exp Toxicol Pathol. 2012 ; 64: 69-74
41. Keck T, Balcom JH, Fernandez-del Castillo C, Antoniu BA, Warshaw AL. Matrix metalloproteinase-9 promotes neutrophil migration and alveolar capillary leakage in pancreatitis associated lung injury in the rat. Gastroenterology. 2002 ; 122: 188-201
42. Teng L, Yu M, Li JM, et al. Matrix metalloproteinase-9 as new biomarkers of severity in multiple organ dysfunction syndrome caused by trauma and infection. Mol Cell Biochem. 2012 ; 360: 271-277
43. Semeraro N, Ammollo CT, Semeraro F, Colucci M. Sepsis-associated disseminated intravascular coagulation and thromboembolic disease. Mediterr J Hematol Infect Dis. 2010 ; 2: e2010024
44. Tyml K. Critical role for oxidative stress, platelets, and coagulation in capillary blood flow impairment in sepsis. Microcirculation. 2011 ; 18: 152-162
45. Sunden-Cullberg J, Norrby-Teglund A, Treutiger CJ. The role of high mobility group box-1 protein in severe sepsis. Curr Opin Infect Dis. 2006 ; 19: 231-236
46. de Jager CP, van Wijk PT, Mathoera RB, de Jongh-Leuvenink J, van der Poll T, Wever PC. Lymphocytopenia and neutrophil-lymphocyte count ratio predict bacteremia better than conventional infection markers in an emergency care unit. Crit Care. 2010 ; 14: R192
47. Jilma B, Blann A, Pernerstorfer T. Regulation of adhesion molecules during human endotoxaemia. No acute effects of aspirin. Amer J Resp Crit Care Med. 1999 ; 159: 857-863
48. Ayala A, Herndon C, Lehman D, Ayala CA, Chaudry IH. Differential induction of apoptosis in lymphoid tissue during sepsis: variation in onset, frequency and nature of the mediators. Blood. 1996 ; 87: 4261-4275
49. Hotchkiss RS, Swanson PE, Freeman BD, et al. Apoptotic cell death in patients with sepsis, shock and multiple organ dysfunction. Crit Care Med. 1999 ; 27: 1230-1251
50. Omaye ST, Schaus EE, Kutnink MA, Hawkes WC. Measurement of vitamin C in blood components by high-performance liquid chromatography. Implication in assessing vitamin C status. Ann N Y Acad Sci. 1987 ; 498: 389-401
51. Welch RW, Wang Y, Crossman A, Park JB, Kirk KL, Levine M. Accumulation of vitamin C (ascorbate) and its oxidized metabolite dehydroascorbic acid occurs by separate mechanisms. J Biol Chem. 1995 ; 270: 12584-12592
52. Vissers MC, Bozonet SM, Pearson JF, Braithwaite LJ. Dietary ascorbate intake affects steady state tissue concentrations in vitamin C-deficient mice: tissue deficiency after suboptimal intake and superior bioavailability from a food source (kiwifruit). Am J Clin Nutr. 2011 ; 93: 292-301
53. Kennedy AD, DeLeo FR. Neutrophil apoptosis and the resolution of infection. Immunol Res. 2009 ; 43: 25-61