Regulated Spatial Distribution of Cyclooxygenases and Lipoxygenases in Crohn's Ulcer

Mao, Yao; Ren, Jian'an; Li, Jieshou

doi:https://doi.org/10.1155/MI/2006/89581

Mediators of Inflammation

On this page

Abstract References Copyright Related Articles

Research Communication | Open Access

Volume 2006 | Article ID 089581 | https://doi.org/10.1155/MI/2006/89581

Regulated Spatial Distribution of Cyclooxygenases and Lipoxygenases in Crohn's Ulcer

Yao Mao,¹Jian'an Ren,¹and Jieshou Li¹

Received05 Dec 2005

Revised14 Mar 2006

Accepted15 Mar 2006

Published12 Apr 2006

Abstract

Background and Aims. Arachidonic acid metabolism actively participates in the initiation, climaxing, and resolution phases of inflammation, and its close connection with inflammatory bowel diseases has been only recently discovered. We aimed to clarify the role of different arachidonic pathways and the interrelationships between them in Crohn's disease. Methods. Seventeen specimens of Crohn's disease dated between 2003/1/1 and 2005/1/1 were collected and underwent immunohistochemical analyses with cylcooxygenase 1, cyclooxygenase 2, 5-lipoxygenase, and 15-lipoxygenase-1 antibodies. Results. (1) The spatial distribution of the three leading enzymes in arachidonic acid pathway—cyclooxygenase 2, 5-lipoxygenase, and 15-lipoxygenase-1—followed sequential arrangement in Crohn's ulcer: neutrophils highly expressing 5-lipoxygenase were in the utmost surface which bordered the band of cyclooxygenase-2 expression that is located just beneath it, and in the lower layers and below the granulation region were eosinophils carrying 15-lipoxygeanse-1. (2) Cyclooxygenase-2 and 15-Lipoxygenase-1-positive cells formed two barrier-like structures that possibly inhibited neutrophil infiltration. Conclusion. The regulated distribution indicated coordinated interplay between inflammatory cells and parenchymal cells, between arachidonic acid pathways, and between innate and adaptive immunity; and the barrier-like structures indicated protective roles for cyclooxygenase 2 and 15-Lipoxygenase-1 in Crohn's disease.

References

J P Hugot, M Chamaillard, H Zouali et al., “Association of NOD2 leucine-rich repeat variants with susceptibility to Crohn's disease,” Nature, vol. 411, no. 6837, pp. 599–603, 2001.
View at: Google Scholar
Y Ogura, D K Bonen, N Inohara et al., “A frameshift mutation in NOD2 associated with susceptibility to Crohn's disease,” Nature, vol. 411, no. 6837, pp. 603–606, 2001.
View at: Google Scholar
D W Gilroy, P R Colville-Nash, D Willis, J Chivers, M J Paul-Clark, and D A Willoughby, “Inducible cyclooxygenase may have anti-inflammatory properties,” Nature Medicine, vol. 5, no. 6, pp. 698–701, 1999.
View at: Google Scholar
C N Serhan, “Lipoxins and aspirin-triggered 15-epi-lipoxin biosynthesis: an update and role in anti-inflammation and pro-resolution,” Prostaglandins and Other Lipid Mediators, vol. 68-69, pp. 433–455, 2002.
View at: Google Scholar
B D Levy, C B Clish, B Schmidt, K Gronert, and C N Serhan, “Lipid mediator class switching during acute inflammation: signals in resolution,” Nature Immunology, vol. 2, no. 7, pp. 612–619, 2001.
View at: Google Scholar
S Fiorucci, J L Wallace, A Mencarelli et al., “A $\beta$ -oxidation-resistant lipoxin A4 analog treats hapten-induced colitis by attenuating inflammation and immune dysfunction,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 44, pp. 15736–15741, 2004.
View at: Google Scholar
M Arita, M Yoshida, S Hong et al., “Resolvin E1, an endogenous lipid mediator derived from omega-3 eicosapentaenoic acid, protects against 2,4,6-trinitrobenzene sulfonic acid-induced colitis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 21, pp. 7671–7676, 2005.
View at: Google Scholar
R D Newberry, J S McDonough, W F Stenson, and R G Lorenz, “Spontaneous and continuous cyclooxygenase-2-dependent prostaglandin E2 production by stromal cells in the murine small intestine lamina propria: directing the tone of the intestinal immune response,” Journal of Immunology, vol. 166, no. 7, pp. 4465–4472, 2001.
View at: Google Scholar
H Harizi, M Juzan, C Grosset, M Rashedi, and N Gualde, “Dendritic cells issued in vitro from bone marrow produce PGE2 that contributes to the immunomodulation induced by antigen-presenting cells,” Cellular Immunology, vol. 209, no. 1, pp. 19–28, 2001.
View at: Google Scholar
B Hinz, K Brune, and A Pahl, “Prostaglandin E(2) upregulates cyclooxygenase-2 expression in lipopolysaccharide-stimulated RAW 264.7 macrophages,” Biochemical and Biophysical Research Communications, vol. 272, no. 3, pp. 744–748, 2000.
View at: Google Scholar
J L Wallace, W McKnight, B K Reuter, and N Vergnolle, “NSAID-induced gastric damage in rats: requirement for inhibition of both cyclooxygenase 1 and 2,” Gastroenterology, vol. 119, no. 3, pp. 706–714, 2000.
View at: Google Scholar
C M Hilkens, A Snijders, F G Snijdewint, E A Wierenga, and M L Kapsenberg, “Modulation of T-cell cytokine secretion by accessory cell-derived products,” The European Respiratory Journal. Supplement, vol. 22, pp. 90s–94s, 1996.
View at: Google Scholar
P Garrone, L Galibert, F Rousset, S M Fu, and J Banchereau, “Regulatory effects of prostaglandin E2 on the growth and differentiation of human B lymphocytes activated through their CD40 antigen,” Journal of Immunology, vol. 152, no. 9, pp. 4282–4290, 1994.
View at: Google Scholar
E R Fedyk, S G Harris, J Padilla, and R P Phipps, “Prostaglandin receptors of the EP2 and EP4 subtypes regulate B lymphocyte activation and differentiation to IgE-secreting cells,” Advances in Experimental Medicine and Biology, vol. 433, pp. 153–157, 1997.
View at: Google Scholar
T Tanigawa, T Watanabe, M Hamaguchi et al., “Anti-inflammatory effect of two isoforms of COX in H. pylori-induced gastritis in mice: possible involvement of PGE2,” American Journal of Physiology-Gastrointestinal and Liver Physiology, vol. 286, no. 1, pp. G148–G156, 2004.
View at: Google Scholar
B K Reuter, S Asfaha, A Buret, K A Sharkey, and J L Wallace, “Exacerbation of inflammation-associated colonic injury in rat through inhibition of cyclooxygenase-2,” Journal of Clinical Investigation, vol. 98, no. 9, pp. 2076–2085, 1996.
View at: Google Scholar
O Morteau, S G Morham, R Sellon et al., “Impaired mucosal defense to acute colonic injury in mice lacking cyclooxygenase-1 or cyclooxygenase-2,” Journal of Clinical Investigation, vol. 105, no. 4, pp. 469–478, 2000.
View at: Google Scholar
J L Wallace, K Chapman, and W McKnight, “Limited anti-inflammatory efficacy of cyclo-oxygenase-2 inhibition in carrageenan-airpouch inflammation,” British Journal of Pharmacology, vol. 126, no. 5, pp. 1200–1204, 1999.
View at: Google Scholar
G Sigthorsson, R J Simpson, M Walley et al., “COX-1 and 2, intestinal integrity, and pathogenesis of nonsteroidal anti-inflammatory drug enteropathy in mice,” Gastroenterology, vol. 122, no. 7, pp. 1913–1923, 2002.
View at: Google Scholar
W Inauen, P A Wyss, S Kayser et al., “Influence of prostaglandins, omeprazole, and indomethacin on healing of experimental gastric ulcers in the rat,” Gastroenterology, vol. 95, no. 3, pp. 636–641, 1988.
View at: Google Scholar
J Y Wang, S Yamasaki, K Takeuchi et al., “Delayed healing of acetic acid-induced gastric ulcers in rats by indomethacin,” Gastroenterology, vol. 96, no. 21, pp. 393–402, 1989.
View at: Google Scholar
S P Colgan, C N Serhan, C A Parkos, C Delp-Archer, and J L Madara, “Lipoxin A4 modulates transmigration of human neutrophils across intestinal epithelial monolayers,” Journal of Clinical Investigation, vol. 92, no. 1, pp. 75–82, 1993.
View at: Google Scholar
J Raud, U Palmertz, S E Dahlen, and P Hedqvist, “Lipoxins inhibit microvascular inflammatory actions of leukotriene B4,” Advances in Experimental Medicine and Biology, vol. 314, pp. 185–192, 1991.
View at: Google Scholar
J F Maddox and C N Serhan, “Lipoxin A4 and B4 are potent stimuli for human monocyte migration and adhesion: selective inactivation by dehydrogenation and reduction,” Journal of Experimental Medicine, vol. 183, no. 1, pp. 137–146, 1996.
View at: Google Scholar
K Gronert, N Maheshwari, N Khan, I R Hassan, M Dunn, and M Laniado Schwartzman, “A role for the mouse 12/15-lipoxygenase pathway in promoting epithelial wound healing and host defense,” Journal of Biological Chemistry, vol. 280, no. 15, pp. 15267–15278, 2005.
View at: Google Scholar
A R Martin, I Villegas, C La Casa, and C A De La Lastra, “Resveratrol, a polyphenol found in grapes, suppresses oxidative damage and stimulates apoptosis during early colonic inflammation in rats,” Biochemical Pharmacology, vol. 67, no. 7, pp. 1399–1410, 2004.
View at: Google Scholar
S Vaidya, E P Somers, S D Wright, P A Detmers, and V S Bansal, “15-deoxy- $\Delta$ 12,14-prostaglandin J2 inhibits the $\beta$ 2 integrin-dependent oxidative burst: involvement of a mechanism distinct from peroxisome proliferator-activated receptor $\gamma$ ligation,” Journal of Immunology, vol. 163, no. 11, pp. 6187–6192, 1999.
View at: Google Scholar
X Zhang, J M Wang, W H Gong, N Mukaida, and H A Young, “Differential regulation of chemokine gene expression by 15-deoxy- $\Delta$ 12,14 prostaglandin J2,” Journal of Immunology, vol. 166, no. 12, pp. 7104–7111, 2001.
View at: Google Scholar
C D Funk, “Prostaglandins and leukotrienes: advances in eicosanoid biology,” Science, vol. 294, no. 5548, pp. 1871–1875, 2001.
View at: Google Scholar
J Y Vanderhoek, R W Bryant, and J M Bailey, “Inhibition of leukotriene biosynthesis by the leukocyte product 15-hydroxy-5,8,11,13-eicosatetraenoic acid,” Journal of Biological Chemistry, vol. 255, no. 21, pp. 10064–10066, 1980.
View at: Google Scholar
S G Harris, J Padilla, L Koumas, D Ray, and R P Phipps, “Prostaglandins as modulators of immunity,” Trends in Immunology, vol. 23, no. 3, pp. 144–150, 2002.
View at: Google Scholar
C G Maloney, W A Kutchera, K H Albertine, T M McIntyre, S M Prescott, and G A Zimmerman, “Inflammatory agonists induce cyclooxygenase type 2 expression by human neutrophils,” Journal of Immunology, vol. 160, no. 3, pp. 1402–1410, 1998.
View at: Google Scholar
M Barrios-Rodiles and K Chadee, “Novel regulation of cyclooxygenase-2 expression and prostaglandin E production by IFN- $\gamma$ in human macrophages,” Journal of Experimental Medicine, vol. 199, pp. 1317–1330, 2004.
View at: Google Scholar
G M Nassar, J D Morrow, L J II Roberts, F G Lakkis, and K F Badr, “Induction of 15-lipoxygenase by interleukin-13 in human blood monocytes,” Journal of Biological Chemistry, vol. 269, no. 44, pp. 27631–27634, 1994.
View at: Google Scholar
E Sigal and D J Conrad, “Human 15-lipoxygenase: a potential effector molecule for interleukin-4,” Advances in Prostaglandin, Thromboxane, and Leukotriene Research, vol. 22, pp. 309–316, 1994.
View at: Google Scholar
T Katoh, F G Lakkis, N Makita, and K F Badr, “Co-regulated expression of glomerular 12/15-lipoxygenase and interleukin- 4 mRNAs in rat nephrotoxic nephritis,” Kidney International, vol. 46, no. 2, pp. 341–349, 1994.
View at: Google Scholar

Copyright

Copyright © 2006 Yao Mao et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

PDF Download Citation Order printed copies

Views

164

Downloads

623

Citations