Neutrophil apoptosis is delayed in an equine model of colitis: Implications for the development of systemic inflammatory response syndrome

Equine Veterinary Journal

Volumn 49, Issue 3, 2017, Pages 383-388

  Anderson, S L ^a   Singh, B ^a  

^a UNIVERSITY OF SASKATCHEWAN   (Canada)

Author keywords

horse; systemic inflammatory response syndrome

Indexed keywords

FRUCTOSE OLIGOSACCHARIDE; OLIGOSACCHARIDE;

ANIMAL; APOPTOSIS; CHEMICALLY INDUCED; COLITIS; HORSE; HORSE DISEASE; METABOLISM; NEUTROPHIL; PATHOLOGY; PHYSIOLOGY; SYSTEMIC INFLAMMATORY RESPONSE SYNDROME; VETERINARY;

ANIMALS; APOPTOSIS; COLITIS; HORSE DISEASES; HORSES; NEUTROPHILS; OLIGOSACCHARIDES; SYSTEMIC INFLAMMATORY RESPONSE SYNDROME;

EID: 84971441084     PISSN: 04251644     EISSN: 20423306     Source Type: Journal    
DOI: 10.1111/evj.12576     Document Type: Article

References (41)

1. Moore, J.N. and Vandenplas, M.L. (2014) Is it the systemic inflammatory response syndrome or endotoxemia in horses with colic? Vet. Clin. Equine 30, 337-351.
2. Epstein, K.L., Brainard, B.M., Gomez-Ibanez, S.E., Lopez, M.A.F., Barton, M.H. and Moore, J.N. (2011) Thrombelastography in horses with acute gastrointestinal disease. J. Vet. Intern. Med. 25, 307-314.
3. Senior, J.M., Proudman, C.J., Leuwer, M. and Carter, S.D. (2011) Plasma endotoxin in horses presented to an equine referral hospital: correlation to selected clinical parameters and outcomes. Equine Vet. J. 43, 585-591.
4. Milinovich, G.J., Klieve, A.V., Pollitt, C.C. and Trott, D.J. (2010) Microbial events in the hindgut during carbohydrate-induced equine laminitis. Vet. Clin. N. Am. Equine Pract. 26, 79-94.
5. Belknap, J.K., Moore, J.N. and Crouser, E.C. (2009) Sepsis – from human organ failure to laminar failure. Vet. Immunol. Immunopathol. 129, 155-157.
6. Kalck, K.A., Frank, N., Elliott, S.B. and Boston, R.C. (2009) Effects of low-dose oligofructose treatment administered via nasogastric intubation on induction of laminitis and associated alterations in glucose and insulin dynamics in horses. Am. J. Vet. Res. 70, 624-632.
7. Nourian, A.R., Baldwin, G.I., van Eps, A.W. and Pollitt, C.C. (2007) Equine laminitis: ultrastructural lesions detected 24–30 hours after induction with oligofructose. Equine Vet. J. 39, 360-364.
8. Fanning, N.F., Kell, M.R., Shorten, G.D., Kirwan, W.O., Bouchier-Hayes, D., Cotter, T.G. and Redmond, H.P. (1999) Circulating granulocyte macrophage colony-stimulating factor in plasma of patients with the systemic inflammatory response syndrome delays neutrophil apoptosis through inhibition of spontaneous reactive oxygen species generation. Shock 11, 167-174.
9. Jimenez, M.F., Watson, R.W., Parodo, J., Evans, D., Foster, D., Steinberg, M., Rotstein, O.D. and Marshall, J.C. (1997) Dysregulated expression of neutrophil apoptosis in the systemic inflammatory response syndrome. Arch. Surg. 132, 1263-1269.
10. Paunel-Görgülü, A., Zörnig, M., Lögters, T., Altrichter, J., Rabenhorst, U., Cinatl, J., Windolf, J. and Scholz, M. (2009) Mcl-1-mediated impairment of the intrinsic apoptosis pathway in circulating neutrophils from critically ill patients can be overcome by Fas stimulation. J. Immunol. 183, 6198-6206.
11. Shang, D., Qi, Q.H., Wang, B.Z., Chen, H.L., Bi, W. and Guan, F.L. (2007) Role of polymorphonuclear neutrophil apoptosis and expression of Fas and caspase-3 in the systemic inflammatory response syndrome. Zhongguo Wei Zhong Bing Ji Jiu Yi Xue 19, 11-13.
12. Fadok, V.A., Bratton, D.L., Konowal, A., Freed, P.W., Westcott, J.Y. and Henson, P.M. (1998) Macrophages that have ingested apoptotic cells in vitro inhibit proinflammatory cytokine production through autocrine/paracrine mechanisms involving TGF-β, PGE2, and PAF. J. Clin. Invest. 101, 890-898.
13. Hofman, P. (2004) Molecular regulation of neutrophil apoptosis and potential targets for therapeutic strategy against the inflammatory process. Curr. Drug Targets Inflamm. Allergy 3, 1-9.
14. Lucas, M., Stuart, L.M., Savill, J. and Lacy-Hulbert, A. (2003) Apoptotic cells and innate immune stimuli combine to regulate macrophage cytokine secretion. J. Immunol. 171, 2610-2615.
15. Wright, H.L., Moots, R.J., Bucknall, R.C. and Edwards, S.W. (2010) Neutrophil function in inflammation and inflammatory disease. Rheumatology 49, 1618-1631.
16. Colotta, F., Polentarutti, N., Sozzani, S. and Mantovani, A. (1992) Modulation of granulocyte survival and programmed cell death by cytokines and bacterial products. Blood 80, 2012-2020.
17. Sweeney, J.F., Nguyen, P.K., Omann, G.M. and Hinshaw, D.B. (1998) Lipopolysaccharide protects polymorphonuclear leukocytes from apoptosis via tyrosine phosphorylation-dependent signal transduction pathway. J. Surg. Res. 74, 64-70.
18. Edwards, S.W., Derouet, M., Howse, M. and Moots, R.J. (2004) Regulation of neutrophil apoptosis by Mcl-1. Biochem. Soc. Trans. 32, 489-492.
19. François, S., El Benna, J., Dang, P.M., Pedruzzi, E., Gougerot-Pocidalo, M.A. and Elbim, C. (2005) Inhibition of neutrophil apoptosis by TLR agonists in whole blood: involvement of the phosphoinositide 3-kinase/Akt and NF-kappa B signaling pathways, leading to increased level of Mcl-1, A2, and phosphorylated Bad. J. Immunol. 174, 3633-3642.
20. Hannah, S., Nadra, I., Dransfield, I., Pryde, J.G., Rossi, A.G. and Haslett, C. (1998) Constitutive neutrophil apoptosis in culture is modulated by cell density independently of beta2 integrin-mediated adhesion. FEBS Lett. 421, 141-146.
21. Atallah, M., Krispin, A., Trahtemberg, U., Ben-Hamron, S., Grau, A., Verbovetski, I. and Mevorach, D. (2012) Constitutive neutrophil apoptosis: regulation by cell concentration via S100 A8/9 and the MEK–ERK Pathway. PLoS One 7, e29333.
22. Cook, V.L., Neuder, L.E., Blikslager, A.T. and Jones, S.L. (2009) The effect of lidocaine on in vitro adhesion and migration of equine neutrophils. Vet. Immunol. Immunopathol. 129, 137-142.
23. Brazil, T.J., Dixon, P.M., Haslett, C., Murray, J. and McGorum, B.C. (2014) Constitutive apoptosis in equine peripheral blood neutrophils in vitro. Vet. J. 202, 536-542.
24. Milot, E., Fotouhi-Ardakani, N. and Filep, J.G. (2012) Myeloid nuclear differentiation antigen, neutrophil apoptosis and sepsis. Front Immunol. 3, 397.
25. Sano, J., Oguma, K., Kano, R., Yazawa, M., Tsujimoto, H. and Hasegawa, A. (2005) High expression of Bcl-xL in delayed apoptosis of canine neutrophils induced by lipopolysaccharide. Res. Vet. Sci. 78, 183-187.
26. Bailey, S.R., Adair, H.S., Reinemeyer, C.R., Morgan, S.J., Brooks, A.C., Longhofer, S.L. and Elliot, J. (2009) Plasma concentrations of endotoxin and platelet activation in the developmental stage of oligofructose-induced laminitis. Vet. Immunol. Immunopathol. 129, 167-173.
27. Fessler, J.F., Bottoms, G.D., Coppoc, G.L., Gimarc, S., Latshaw, H.S. and Noble, J.K. (1989) Plasma endotoxin concentrations in experimental and clinical equine subjects. Equine Vet. J. 7, Suppl. 21, 24-28.
28. Milinovich, G.J., Burrell, P.C., Pollitt, C.C., Klieve, A.V., Blackall, L.L., Ouwerkerk, D., Woodland, E. and Trott, D.J. (2008) Microbial ecology of the equine hindgut during oligofructose-induced laminitis. ISME J. 2, 1089-1100.
29. Taneja, R., Parodo, J., Jia, S.H., Kapus, A., Rotstein, O.D. and Marshall, J.C. (2004) Delayed neutrophil apoptosis in sepsis is associated with maintenance of mitochondrial transmembrane potential and reduced caspase-9 activity. Crit. Care Med. 32, 1460-1469.
30. Bone, R.C. (1996) Sir Isaac Newton, sepsis, SIRS, and CARS. Crit. Care Med. 24, 1125-1128.
31. Cavaillon, J.M. and Adib-Conquy, M. (2006) Bench-to-bedside review: endotoxin tolerance as a model of leukocyte reprogramming in sepsis. Crit. Care 10, 233.
32. Kopanakis, K., Tzepi, I.M., Pistiki, A., Carrer, D.P., Netea, M.G., Georgitsi, M., Lymperi, M., Droggiti, D.I., Liakakos, T., Machairas, A. and Giamarellos-Bourboulis, E.J. (2013) Pre-treatment with low-dose endotoxin prolongs survival from experimental lethal endotoxic shock: benefit for lethal peritonitis by Escherichia coli. Cytokine 62, 382-388.
33. Medvedev, A.E., Sabroe, I., Hasday, J.D. and Vogel, S.N. (2006) Tolerance to microbial TLR ligands: molecular mechanisms and relevance to disease. J. Endotoxin Res. 12, 133-150.
34. Allen, G.K., Campbell-Beggs, C., Robinson, J.A., Johnson, P.J. and Green, E.M. (1996) Induction of early-phase endotoxin tolerance in horses. Equine Vet. J. 28, 269-274.
35. Parker, L.C., Jones, E.C., Prince, L.R., Dower, S.K., Whyte, M.K. and Sabroe, I. (2005) Endotoxin tolerance induces selective alterations in neutrophil function. J. Leukoc. Biol. 78, 1301-1305.
36. McCall, C.E., Grosso-Wilmoth, L.M., LaRue, K., Guzman, R.N. and Cousart, S.L. (1993) Tolerance to endotoxin-induced expression of interleukin-1β gene in blood neutrophils of humans with sepsis syndrome. J. Clin. Invest. 91, 853-861.
37. Colletti, L.M., Remick, D.G. and Campbell, D.A. Jr (1994) LPS pretreatment protects from hepatic ischemia/reperfusion. J. Surg. Res. 57, 337-343.
38. He, W., Fong, Y., Marano, M.A., Gershenwald, J.E., Yurt, R.W., Moldawer, L.L. and Lowry, S.F. (1992) Tolerance to endotoxin prevents mortality in infected thermal injury: association with attenuated cytokine responses. J. Infect. Dis. 165, 859-864.
39. Burrows, G.E. (1981) Dose-response of ponies to parenteral Escherichia coli endotoxin. Can. J. Comp. Med. 45, 207-210.
40. Frauenfelder, H.C., Fessler, J.F., Moore, A.B., Bottoms, G.D. and Boon, G.D. (1982) Effects of dexamethasone on endotoxin shock in the anesthetized pony: hematologic, blood gas, and coagulation changes. Am. J. Vet. Res. 43, 405-411.
41. Wagener, J.G. and Roth, R.A. (1999) Neutrophil migration during endotoxemia. J. Leuk. Biol. 66, 10-24.