Inhibition of CD36-dependent Phagocytosis by Prostaglandin E2 Contributes to the Development of Endometriosis

Overview

Journal Am J Pathol

Publisher Elsevier

Specialty Pathology

Date 2009 Dec 26

PMID 20035060

Citations 34

Authors

Pei-Chin Chuang

Yiu-Juian Lin

Meng-Hsing Wu

Lih-Yuh C Wing

Yutaka Shoji

Shaw-Jenq Tsai

Affiliations

Soon will be listed here.

Abstract

Dysfunction in macrophage-mediated phagocytosis of aberrant cells that undergo retrograde transport to the peritoneal cavity is considered an important factor in the development of endometriosis. However, the mechanisms responsible for the loss of function of macrophages remain largely unknown. Herein, we report that prostaglandin (PG) E(2), via the EP2 receptor-dependent signaling pathway, inhibits the expression of CD36 in peritoneal macrophages, resulting in reduced phagocytic ability. PGE(2)-mediated inhibition of macrophage phagocytic capability was restored by ectopic expression of CD36. Treatment with PGE(2) inhibited CD36-dependent phagocytosis of peritoneal macrophages and increased the number and size of endometriotic lesions in mice. In contrast, blockade of PGE(2) production by cyclooxygenase inhibitors enhanced the phagocytic ability of peritoneal macrophages and reduced endometriotic lesion formation. Taken together, our findings reveal a potential mechanism of immune dysfunction during endometriosis development and may contribute to the design of an effective prevention/treatment regimen.

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References

Hsu C, Lu C, Huang B, Wu M, Tsai S . Cyclic adenosine 3',5'-monophosphate response element-binding protein and CCAAT/enhancer-binding protein mediate prostaglandin E2-induced steroidogenic acute regulatory protein expression in endometriotic stromal cells. Am J Pathol. 2008; 173(2):433-41. PMC: 2475780. DOI: 10.2353/ajpath.2008.080199. View

Tamura M, Sebastian S, Yang S, Gurates B, Fang Z, Bulun S . Interleukin-1beta elevates cyclooxygenase-2 protein level and enzyme activity via increasing its mRNA stability in human endometrial stromal cells: an effect mediated by extracellularly regulated kinases 1 and 2. J Clin Endocrinol Metab. 2002; 87(7):3263-73. DOI: 10.1210/jcem.87.7.8594. View

Somigliana E, Vigano P, Rossi G, Carinelli S, Vignali M, Panina-Bordignon P . Endometrial ability to implant in ectopic sites can be prevented by interleukin-12 in a murine model of endometriosis. Hum Reprod. 1999; 14(12):2944-50. DOI: 10.1093/humrep/14.12.2944. View

Wu M, Wang C, Lin C, Chen L, Chang W, Tsai S . Distinct regulation of cyclooxygenase-2 by interleukin-1beta in normal and endometriotic stromal cells. J Clin Endocrinol Metab. 2004; 90(1):286-95. DOI: 10.1210/jc.2004-1612. View

Dunn G, Old L, Schreiber R . The immunobiology of cancer immunosurveillance and immunoediting. Immunity. 2004; 21(2):137-48. DOI: 10.1016/j.immuni.2004.07.017. View

Dmowski W, Gebel H, Braun D . The role of cell-mediated immunity in pathogenesis of endometriosis. Acta Obstet Gynecol Scand Suppl. 1994; 159:7-14. View

Greenwalt D, Lipsky R, Ockenhouse C, Ikeda H, Tandon N, Jamieson G . Membrane glycoprotein CD36: a review of its roles in adherence, signal transduction, and transfusion medicine. Blood. 1992; 80(5):1105-15. View

Baranao R, Etchepareborda J, Meresman G, Rumi L . Functional and phenotypic alterations in peritoneal macrophages from patients with early and advanced endometriosis. Arch Gynecol Obstet. 1998; 261(3):147-57. DOI: 10.1007/s004040050214. View

Savill J, Hogg N, Ren Y, Haslett C . Thrombospondin cooperates with CD36 and the vitronectin receptor in macrophage recognition of neutrophils undergoing apoptosis. J Clin Invest. 1992; 90(4):1513-22. PMC: 443198. DOI: 10.1172/JCI116019. View

10.

Bulun S . Endometriosis. N Engl J Med. 2009; 360(3):268-79. DOI: 10.1056/NEJMra0804690. View

11.

Trial J, Rice L . Erythropoietin withdrawal leads to the destruction of young red cells at the endothelial-macrophage interface. Curr Pharm Des. 2004; 10(2):183-90. DOI: 10.2174/1381612043453423. View

12.

Rigotti A, Acton S, Krieger M . The class B scavenger receptors SR-BI and CD36 are receptors for anionic phospholipids. J Biol Chem. 1995; 270(27):16221-4. DOI: 10.1074/jbc.270.27.16221. View

13.

Stuart L, Deng J, Silver J, Takahashi K, Tseng A, Hennessy E . Response to Staphylococcus aureus requires CD36-mediated phagocytosis triggered by the COOH-terminal cytoplasmic domain. J Cell Biol. 2005; 170(3):477-85. PMC: 2171464. DOI: 10.1083/jcb.200501113. View

14.

Linton M, Fazio S . Class A scavenger receptors, macrophages, and atherosclerosis. Curr Opin Lipidol. 2001; 12(5):489-95. DOI: 10.1097/00041433-200110000-00003. View

15.

Guy E, Kuchibhotla S, Silverstein R, Febbraio M . Continued inhibition of atherosclerotic lesion development in long term Western diet fed CD36o /apoEo mice . Atherosclerosis. 2006; 192(1):123-30. DOI: 10.1016/j.atherosclerosis.2006.07.015. View

16.

Janabi M, Yamashita S, Hirano K, Sakai N, Hiraoka H, Matsumoto K . Oxidized LDL-induced NF-kappa B activation and subsequent expression of proinflammatory genes are defective in monocyte-derived macrophages from CD36-deficient patients. Arterioscler Thromb Vasc Biol. 2000; 20(8):1953-60. DOI: 10.1161/01.atv.20.8.1953. View

17.

Wu M, Shoji Y, Wu M, Chuang P, Lin C, Huang M . Suppression of matrix metalloproteinase-9 by prostaglandin E(2) in peritoneal macrophage is associated with severity of endometriosis. Am J Pathol. 2005; 167(4):1061-9. PMC: 1603672. DOI: 10.1016/S0002-9440(10)61195-9. View

18.

Oquendo P, Hundt E, Lawler J, Seed B . CD36 directly mediates cytoadherence of Plasmodium falciparum parasitized erythrocytes. Cell. 1989; 58(1):95-101. DOI: 10.1016/0092-8674(89)90406-6. View

19.

Chuang P, Wu M, Shoji Y, Tsai S . Downregulation of CD36 results in reduced phagocytic ability of peritoneal macrophages of women with endometriosis. J Pathol. 2009; 219(2):232-41. DOI: 10.1002/path.2588. View

20.

Banu S, Lee J, Speights Jr V, Starzinski-Powitz A, Arosh J . Cyclooxygenase-2 regulates survival, migration, and invasion of human endometriotic cells through multiple mechanisms. Endocrinology. 2007; 149(3):1180-9. DOI: 10.1210/en.2007-1168. View