Milk fat globule epidermal growth factor-factor 8 mitigates inflammation and tissue injury after hemorrhagic shock in experimental animals

Journal of Trauma and Acute Care Surgery

Volumn 72, Issue 4, 2012, Pages 861-869

  Zhang, Fangming ^b   Shah, Kavin G ^a   Qi, Lei ^b   Wu, Rongqian ^b   Barrera, Rafael ^a   Nicastro, Jeffrey ^a   Coppa, Gene F ^a   Wang, Ping ^a,b  

^a DONALD AND BARBARA ZUCKER SCHOOL OF MEDICINE AT HOFSTRA NORTHWELL   (United States)

^b FEINSTEIN INSTITUTE FOR MEDICAL RESEARCH   (United States)

Author keywords

Apoptosis; Hemorrhage; Inflammatory cytokines; Resuscitation; RhMFG E8; Shock

Indexed keywords

CASPASE 3; INTERLEUKIN 1BETA; INTERLEUKIN 6; LACTADHERIN; RECOMBINANT LACTADHERIN; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; MEMBRANE ANTIGEN; MFGE8 PROTEIN, HUMAN; MILK PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME LINKED IMMUNOSORBENT ASSAY; HEMORRHAGIC SHOCK; INFLAMMATION; LUNG ALVEOLUS CELL; MALE; MOUSE; NEUTROPHIL CHEMOTAXIS; NICK END LABELING; NONHUMAN; POST TREATMENT SURVIVAL; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; SPLEEN CELL; TISSUE INJURY; ANIMAL; BLOOD; C57BL MOUSE; DRUG EFFECT;

ANIMALS; ANTIGENS, SURFACE; APOPTOSIS; CASPASE 3; INFLAMMATION; INTERLEUKIN-1BETA; MALE; MICE; MICE, INBRED C57BL; MILK PROTEINS; NEUTROPHIL INFILTRATION; SHOCK, HEMORRHAGIC; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84862726870     PISSN: 21630755     EISSN: 21630763     Source Type: Journal    
DOI: 10.1097/TA.0b013e318249a97c     Document Type: Article

References (46)

1. Cothren CC, Moore EE, Hedegaard HB, Meng K. Epidemiology of urban trauma deaths: a comprehensive reassessment 10 years later. World J Surg. 2007;31:1507-1511.
2. Moore EE, Knudson MM, Jurkovich GJ, Fildes JJ, Meredith JW. Emergency traumatologist or trauma and acute care surgeon: decision time. J Am Coll Surg. 2009;209:394-395.
3. Maegele M, Lefering R, Yucel N, et al; AG Polytrauma of the German Trauma Society (DGU). Early coagulopathy in multiple injury: an analysis from the German Trauma Registry on 8724 patients. Injury. 2007;38:298-304.
4. Neuman TS, Bockman MA, Moody P, et al. An autopsy study of traumatic deaths; San Diego County, 1979. Am J Surg. 1982;144:722-727.
5. Rossaint R, Bouillon B, Cerny V, et al; Task Force for Advanced Bleeding Care in Trauma. Management of bleeding following major trauma: an updated European guideline. Crit Care. 2010;14:R52.
6. Frith D, Goslings JC, Gaarder C, et al. Definition and drivers of acute traumatic coagulopathy: clinical and experimental investigations. J Thromb Haemost. 2010;8:1919-1925.
7. Yang FL, Subeq YM, Lee CJ, Lee RP, Peng TC, Hsu BG. Melatonin ameliorates hemorrhagic shock-induced organ damage in rats. J Surg Res. 2011;167:e315-e321.
8. Lotze MT, Tracey KJ. High-mobility group box 1 protein (HMGB1): nuclear weapon in the immune arsenal. Nat Rev Immunol. 2005;5:331-342.
9. Zacharias N, Sailhamer EA, Li Y, et al. Histone deacetylase inhibitors prevent apoptosis following lethal hemorrhagic shock in rodent kidney cells. Resuscitation. 2011;82:105-109.
10. Fink SL, Cookson BT. Apoptosis, pyroptosis, and necrosis: mechanistic description of dead and dying eukaryotic cells. Infect Immun. 2005;73: 1907-1916.
11. Stubbs JD, Lekutis C, Singer KL, et al. cDNA cloning of a mouse mammary epithelial cell surface protein reveals the existence of epidermal growth factor-like domains linked to factor VIII-like sequences. Proc Natl Acad Sci U S A. 1990;87:8417-8421.
12. Hanayama R, Tanaka M, Miyasaka K, et al. Autoimmune disease and impaired uptake of apoptotic cells in MFG-E8-deficient mice. Science. 2004;304:1147-1150.
13. Hanayama R, Tanaka M, Miwa K, Shinohara A, Iwamatsu A, Nagata S. Identification of a factor that links apoptotic cells to phagocytes. Nature. 2002;417:182-187.
14. Oshima K, Aoki N, Negi M, Kishi M, Kitajima K, Matsuda T. Lactationdependent expression of an mRNA splice variant with an exon for a multiply O-glycosylated domain of mouse milk fat globule glycoprotein MFG-E8. Biochem Biophys Res Commun. 1999;254:522-528.
15. Komura H, Miksa M, Wu R, Goyert SM, Wang P. Milk fat globule epidermal growth factor-factor VIII is down-regulated in sepsis via the lipopolysaccharide-CD14 pathway. J Immunol. 2009;182:581-587.
16. Miksa M, Wu R, Dong W, Das P, Yang D, Wang P. Dendritic cell-derived exosomes containing milk fat globule epidermal growth factor-factor VIII attenuate proinflammatory responses in sepsis. Shock. 2006;25:586-593.
17. Miksa M, Wu R, Dong W, et al. Immature dendritic cell-derived exosomes rescue septic animals via milk fat globule epidermal growth factor-factor VIII [corrected]. J Immunol. 2009;183:5983-5990.
18. Wu R, Dong W, Zhou M, Cui X, Simms HH, Wang P. A novel approach to maintaining cardiovascular stability after hemorrhagic shock: beneficial effects of adrenomedullin and its binding protein. Surgery. 2005; 137:200-208.
19. Wu R, Higuchi S, Dong W, et al. Reversing established sepsis in rats with human vasoactive hormone adrenomedullin and its binding protein. Mol Med. 2009;15:28-33.
20. Shah KG, Wu R, Jacob A, et al. Recombinant human milk fat globule - EGF factor 8 produces dose-dependent benefits in sepsis. Intensive Care Med. 2012;38:128-136.
21. Qiang X, Li J, Wu R, et al. Expression and characterization of recombinant human milk fat globule-EGF factor VIII. Int J Mol Med. 2011; 28:1071-1076.
22. Kohut LK, Darwiche SS, Brumfield JM, Frank AM, Billiar TR. Fixed volume or fixed pressure: a murine model of hemorrhagic shock. J Vis Exp. 2011;(52). pii: 2068.
23. Shah KG, Wu R, Jacob A, et al. Human ghrelin ameliorates organ injury and improves survival after radiation injury combined with severe sepsis. Mol Med. 2009;15:407-414.
24. Cui T, Miksa M, Wu R, et al. Milk fat globule epidermal growth factor 8 attenuates acute lung injury in mice after intestinal ischemia and reperfusion. Am J Respir Crit Care Med. 2010;181:238-246.
25. Aziz M, Jacob A, Matsuda A, Wang P. Review: milk fat globule-EGF factor 8 expression, function and plausible signal transduction in resolving inflammation. Apoptosis. 2011;16:1077-1086.
26. Smail N, Messiah A, Edouard A, et al. Role of systemic inflammatory response syndrome and infection in the occurrence of early multiple organ dysfunction syndrome following severe trauma. Intensive Care Med. 1995;21:813-816.
27. Hollenberg SM. Vasoactive drugs in circulatory shock. Am J Respir Crit Care Med. 2011;183:847-855.
28. Duchesne JC, McSwain NE Jr, Cotton BA, et al. Damage control resuscitation: the new face of damage control. J Trauma. 2010;69:976-990.
29. Sharar SR, Mihelcic DD, Han KT, Harlan JM, Winn RK. Ischemia reperfusion injury in the rabbit ear is reduced by both immediate and delayed CD18 leukocyte adherence blockade. J Immunol. 1994;153: 2234-2238.
30. Lauber K, Blumenthal SG, Waibel M, Wesselborg S. Clearance of apoptotic cells: getting rid of the corpses. Mol Cell. 2004;14:277-287.
31. Wu R, Chaung WW, Zhou M, et al. Milk fat globule EGF factor 8 attenuates sepsis-induced apoptosis and organ injury in alcohol-intoxicated rats. Alcohol Clin Exp Res. 2010;34:1625-1633.
32. Aziz MM, Ishihara S, Mishima Y, et al. MFG-E8 attenuates intestinal inflammation in murine experimental colitis by modulating osteopontindependent alphavbeta3 integrin signaling. J Immunol. 2009;182:7222-7232.
33. Jinushi M, Nakazaki Y, Carrasco DR, et al. Milk fat globule EGF-8 promotes melanoma progression through coordinated Akt and twist signaling in the tumor microenvironment. Cancer Res. 2008;68:8889-8898.
34. Miksa M, Amin D, Wu R, et al. Maturation-induced down-regulation of MFG-E8 impairs apoptotic cell clearance and enhances endotoxin response. Int J Mol Med. 2008;22:743-748.
35. Hu CY, Wu CS, Tsai HF, Chang SK, Tsai WI, Hsu PN. Genetic polymorphism in milk fat globule-EGF factor 8 (MFG-E8) is associated with systemic lupus erythematosus in human. Lupus. 2009;18:676-681.
36. Larocca D, Peterson JA, Urrea R, Kuniyoshi J, Bistrain AM, Ceriani RL. A Mr 46,000 human milk fat globule protein that is highly expressed in human breast tumors contains factor VIII-like domains. Cancer Res. 1991;51:4994-4998.
37. Loria V, Dato I, Graziani F, Biasucci LM. Myeloperoxidase: a new biomarker of inflammation in ischemic heart disease and acute coronary syndromes. Mediators Inflamm. 2008;2008:135625.
38. Ulloa L, Tracey KJ. The "cytokine profile": a code for sepsis. Trends Mol Med. 2005;11:56-63.
39. Frink M, van Griensven M, Kobbe P, et al. IL-6 predicts organ dysfunction and mortality in patients with multiple injuries. Scand J Trauma Resusc Emerg Med. 2009;17:49.
40. Pecoits-Filho R, Barany P, Lindholm B, Heimburger O, Stenvinkel P. Interleukin-6 is an independent predictor of mortality in patients starting dialysis treatment. Nephrol Dial Transplant. 2002;17:1684-1688.
41. Haasper C, Kalmbach M, Dikos GD, et al. Prognostic value of procalcitonin (PCT) and/or interleukin-6 (IL-6) plasma levels after multiple trauma for the development of multi organ dysfunction syndrome (MODS) or sepsis. Technol Health Care. 2010;18:89-100.
42. Coopersmith CM, Stromberg PE, Dunne WM, et al. Inhibition of intestinal epithelial apoptosis and survival in a murine model of pneumonia-induced sepsis. JAMA. 2002;287:1716-1721.
43. Parrino J, Hotchkiss RS, Bray M. Prevention of immune cell apoptosis as potential therapeutic strategy for severe infections. Emerg Infect Dis. 2007;13:191-198.
44. Matsuda A, Jacob A, Wu R, et al. Milk fat globule-EGF factor VIII in sepsis and ischemia-reperfusion injury. Mol Med. 2011;17:126-133.
45. Jinushi M, Sato M, Kanamoto A, et al. Milk fat globule epidermal growth factor-8 blockade triggers tumor destruction through coordinated cell-autonomous and immune-mediated mechanisms. J Exp Med. 2009; 206:1317-1326.
46. Atabai K, Jame S, Azhar N, et al. Mfge8 diminishes the severity of tissue fibrosis in mice by binding and targeting collagen for uptake by macrophages. J Clin Invest. 2009;119:3713-3722.