The role of neutrophils in corneal wound healing in HO-2 null mice

PLoS ONE

Volumn 6, Issue 6, 2011, Pages

  Marrazzo, Giuseppina ^a,b   Bellner, Lars ^a   Halilovic, Adna ^a   Li Volti, Giovanni ^b   Drago, Filippo ^b   Dunn, Michael W ^a   Laniado Schwartzman, Michal ^a  

^a NEW YORK MEDICAL COLLEGE   (United States)

^b UNIVERSITY OF CATANIA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

HEME OXYGENASE 2; MIDKINE; VASCULAR ENDOTHELIAL CADHERIN; HEME OXYGENASE; HEME OXYGENASE 1; HEME OXYGENASE-2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ADHESION; CELL FUNCTION; CELL INFILTRATION; CONTROLLED STUDY; CORNEA EPITHELIUM; CORNEA INJURY; DISEASE EXACERBATION; INNATE IMMUNITY; MOUSE; NEUTROPENIA; NEUTROPHIL; NONHUMAN; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; WOUND HEALING; ANIMAL; CELL COUNT; CORNEA; CYTOLOGY; ENDOTHELIUM CELL; ENZYMOLOGY; GENE DELETION; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; INFLAMMATION; INJURY; METABOLISM; NEUTROPHIL CHEMOTAXIS; PATHOLOGY;

MUS;

ANIMALS; CELL ADHESION; CELL COUNT; CORNEA; ENDOTHELIAL CELLS; GENE DELETION; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HEME OXYGENASE (DECYCLIZING); HEME OXYGENASE-1; INFLAMMATION; MICE; NEUTROPHIL INFILTRATION; NEUTROPHILS; WOUND HEALING;

EID: 79959230629     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0021180     Document Type: Article

References (41)

1. Wilson SE, Mohan RR, Mohan RR, Ambrosio R Jr, Hong J, et al. (2001) The corneal wound healing response: cytokine-mediated interaction of the epithelium, stroma, and inflammatory cells. Prog Retin Eye Res 20: 625-637.
2. Ahmadi AJ, Jakobiec FA, (2002) Corneal wound healing: cytokines and extracellular matrix proteins. Int Ophthalmol Clin 42: 13-22.
3. O'Brien TP, Li Q, Ashraf MF, Matteson DM, Stark WJ, et al. (1998) Inflammatory response in the early stages of wound healing after excimer laser keratectomy. Arch Ophthalmol 116: 1470-1474.
4. Li Z, Burns AR, Smith CW, (2006) Two waves of neutrophil emigration in response to corneal epithelial abrasion: distinct adhesion molecule requirements. Invest Ophthalmol Vis Sci 47: 1947-1955.
5. Martin P, Leibovich SJ, (2005) Inflammatory cells during wound repair: the good, the bad and the ugly. Trends Cell Biol 15: 599-607.
6. McDonald B, Pittman K, Menezes GB, Hirota SA, Slaba I, et al. (2010) Intravascular danger signals guide neutrophils to sites of sterile inflammation. Science 330: 362-366.
7. Ueno M, Lyons BL, Burzenski LM, Gott B, Shaffer DJ, et al. (2005) Accelerated wound healing of alkali-burned corneas in MRL mice is associated with a reduced inflammatory signature. Invest Ophthalmol Vis Sci 46: 4097-4106.
8. Gan L, Fagerholm P, Kim HJ, (1999) Effect of leukocytes on corneal cellular proliferation and wound healing. Invest Ophthalmol Vis Sci 40: 575-581.
9. Ma C, Martins-Green M, (2009) Second-hand cigarette smoke inhibits wound healing of the cornea by stimulating inflammation that delays corneal reepithelialization. Wound Repair Regen 17: 387-396.
10. Willoughby DA, Moore AR, Colville-Nash PR, Gilroy D, (2000) Resolution of inflammation. Int J Immunopharmacol 22: 1131-1135.
11. Abraham NG, Kappas A, (2008) Pharmacological and clinical aspects of heme oxygenase. Pharmacol Rev 60: 79-127.
12. Bellner L, Vitto M, Patil KA, Dunn MW, Regan R, et al. (2008) Exacerbated corneal inflammation and neovascularization in the HO-2 null mice is ameliorated by biliverdin. Exp Eye Res 87: 268-278.
13. Seta F, Bellner L, Rezzani R, Regan RF, Dunn MW, et al. (2006) Heme oxygenase-2 is a critical determinant for execution of an acute inflammatory and reparative response. Am J Pathol 169: 1612-1623.
14. Bellner L, Wolstein J, Patil KA, Dunn MW, Laniado-Schwartzman M, (2011) Biliverdin rescues the HO-2 null mouse phenotype of unresolved chronic inflammation following corneal epithelial injury. Invest Ophthalmol Vis Sci.
15. Poss KD, Thomas MJ, Ebralidze AK, O'Dell TJ, Tonegawa S, (1995) Hippocampal long-term potentiation is normal in heme oxygenase-2 mutant mice. Neuron 15: 867-873.
16. Rogers B, Yakopson V, Teng ZP, Guo Y, Regan RF, (2003) Heme oxygenase-2 knockout neurons are less vulnerable to hemoglobin toxicity. Free Radic Biol Med 35: 872-881.
17. Daley JM, Thomay AA, Connolly MD, Reichner JS, Albina JE, (2008) Use of Ly6G-specific monoclonal antibody to deplete neutrophils in mice. J Leukoc Biol 83: 64-70.
18. Bellner L, Martinelli L, Halilovic A, Patil K, Puri N, et al. (2009) Heme oxygenase-2 deletion causes endothelial cell activation marked by oxidative stress, inflammation, and angiogenesis. J Pharmacol Exp Ther 331: 925-932.
19. Gronert K, Maheshwari N, Khan N, Hassan IR, Dunn M, et al. (2005) A role for the mouse 12/15-lipoxygenase pathway in promoting epithelial wound healing and host defense. J Biol Chem 280: 15267-15278.
20. Serhan CN, Savill J, (2005) Resolution of inflammation: the beginning programs the end. Nat Immunol 6: 1191-1197.
21. Takada T, Toriyama K, Muramatsu H, Song XJ, Torii S, et al. (1997) Midkine, a retinoic acid-inducible heparin-binding cytokine in inflammatory responses: chemotactic activity to neutrophils and association with inflammatory synovitis. J Biochem 122: 453-458.
22. van Buul JD, van Alphen FP, Hordijk PL, (2009) The presence of alpha-catenin in the VE-cadherin complex is required for efficient transendothelial migration of leukocytes. Int J Biol Sci 5: 695-705.
23. Gan L, Hamberg-Nystrom H, Fagerholm P, Van Setten G, (2001) Cellular proliferation and leukocyte infiltration in the rabbit cornea after photorefractive keratectomy. Acta Ophthalmol Scand 79: 488-492.
24. Gagen D, Laubinger S, Li Z, Petrescu MS, Brown ES, et al. (2010) ICAM-1 mediates surface contact between neutrophils and keratocytes following corneal epithelial abrasion in the mouse. Exp Eye Res 91: 676-684.
25. Conners MS, Stoltz RA, Dunn MW, Levere RD, Abraham NG, et al. (1995) A closed eye-contact lens model of corneal inflammation. II. Inhibition of cytochrome P450 arachidonic acid metabolism alleviates inflammatory sequelae. Invest Ophthalmol Vis Sci 36: 841-850.
26. Laniado Schwartzman M, Abraham NG, Conners MS, Dunn MW, Levere RD, et al. (1997) Heme oxygenase induction with attenuation of experimentally-induced corneal inflammation. BiochemPharmacol 53: 1069-1075.
27. Patil K, Bellner L, Cullaro G, Gotlinger KH, Dunn MW, et al. (2008) Heme oxygenase-1 induction attenuates corneal inflammation and accelerates wound healing after epithelial injury. Invest Ophthalmol Vis Sci 49: 3379-3386.
28. Wagener FA, da Silva JL, Farley T, de Witte T, Kappas A, et al. (1999) Differential effects of heme oxygenase isoforms on heme mediation of endothelial intracellular adhesion molecule 1 expression. J Pharmacol Exp Ther 291: 416-423.
29. Wagener FA, Volk HD, Willis D, Abraham NG, Soares MP, et al. (2003) Different faces of the heme-heme oxygenase system in inflammation. Pharmacol Rev 55: 551-571.
30. Morse D, Pischke SE, Zhou Z, Davis RJ, Flavell RA, et al. (2003) Suppression of inflammatory cytokine production by carbon monoxide involves the JNK pathway and AP-1. J Biol Chem 278: 36993-36998.
31. Sarady-Andrews JK, Liu F, Gallo D, Nakao A, Overhaus M, et al. (2005) Biliverdin administration protects against endotoxin-induced acute lung injury in rats. Am J Physiol Lung Cell Mol Physiol 289: L1131-1137.
32. Wegiel B, Baty CJ, Gallo D, Csizmadia E, Scott JR, et al. (2009) Cell surface biliverdin reductase mediates biliverdin-induced anti-inflammatory effects via phosphatidylinositol 3-kinase and Akt. J Biol Chem 284: 21369-21378.
33. Kampfer H, Kolb N, Manderscheid M, Wetzler C, Pfeilschifter J, et al. (2001) Macrophage-derived heme-oxygenase-1: expression, regulation, and possible functions in skin repair. Mol Med 7: 488-498.
34. Hanselmann C, Mauch C, Werner S, (2001) Haem oxygenase-1: a novel player in cutaneous wound repair and psoriasis? Biochem J 353: 459-466.
35. Wagener FA, van Beurden HE, von den Hoff JW, Adema GJ, Figdor CG, (2003) The heme-heme oxygenase system: a molecular switch in wound healing. Blood 102: 521-528.
36. Burns AR, Li Z, Smith CW, (2005) Neutrophil migration in the wounded cornea: the role of the keratocyte. Ocul Surf 3: S173-176.
37. Petrescu MS, Larry CL, Bowden RA, Williams GW, Gagen D, et al. (2007) Neutrophil interactions with keratocytes during corneal epithelial wound healing: a role for CD18 integrins. Invest Ophthalmol Vis Sci 48: 5023-5029.
38. Muller WA, (2003) Leukocyte-endothelial-cell interactions in leukocyte transmigration and the inflammatory response. Trends Immunol 24: 327-334.
39. Sato W, Kadomatsu K, Yuzawa Y, Muramatsu H, Hotta N, et al. (2001) Midkine is involved in neutrophil infiltration into the tubulointerstitium in ischemic renal injury. J Immunol 167: 3463-3469.
40. Fahmy RG, Waldman A, Zhang G, Mitchell A, Tedla N, et al. (2006) Suppression of vascular permeability and inflammation by targeting of the transcription factor c-Jun. Nat Biotechnol 24: 856-863.
41. Marmon S, Cammer M, Raine CS, Lisanti MP, (2009) Transcellular migration of neutrophils is a quantitatively significant pathway across dermal microvascular endothelial cells. Exp Dermatol 18: 88-90.