Wound healing defect of Vav3-/- mice due to impaired β2-integrin-dependent macrophage phagocytosis of apoptotic neutrophils

Blood

Volumn 113, Issue 21, 2009, Pages 5266-5276

  Sindrilaru, Anca ^a   Peters, Thorsten ^a   Schymeinsky, Jürgen ^b   Oreshkova, Tsvetelina ^a   Wang, Honglin ^a   Gompf, Anne ^a   Mannella, Francesca ^a   Wlaschek, Meinhard ^a   Tter, Cord Sunderkö ^c   Rudolph, Karl Lenhard ^a   Walzog, Barbara ^b   Bustelo, Xosé R ^d   Fischer, Klaus D ^a,e   Scharffetter Kochanek, Karin ^a  

^a UNIVERSITY OF ULM   (Germany)

^b LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^c UNIVERSITY OF MÜNSTER   (Germany)

^d UNIVERSITY OF SALAMANCA   (Spain)

^e OTTO VON GUERICKE UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BETA2 INTEGRIN; INTERCELLULAR ADHESION MOLECULE 1; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG; VAV PROTEIN; VAV3 PROTEIN; CD18 ANTIGEN; TRANSFORMING GROWTH FACTOR BETA; VAV3 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOKINE RELEASE; IMMUNOPRECIPITATION; MACROPHAGE; MALE; MEMBRANE BINDING; MOUSE; MYOFIBROBLAST; NEUTROPHIL; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN LOCALIZATION; WOUND CONTRACTION; WOUND HEALING IMPAIRMENT; ANIMAL; IMMUNOLOGY; LEUKOCYTE; MOUSE MUTANT; PHYSIOLOGY; WOUND HEALING;

ANIMALS; ANTIGENS, CD18; APOPTOSIS; LEUKOCYTES; MACROPHAGES; MICE; MICE, KNOCKOUT; NEUTROPHILS; PHAGOCYTOSIS; PROTO-ONCOGENE PROTEINS C-VAV; TRANSFORMING GROWTH FACTOR BETA; WOUND HEALING;

EID: 67149130583     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2008-07-166702     Document Type: Article

References (54)

1. Martin P. Wound healing - aiming for perfect skin regeneration [review]. Science. 1997;276:75-81. (Pubitemid 27161246)
2. Singer AJ, Clark RA. Cutaneous wound healing. N Engl J Med. 1999;341:738-746.
3. Fadok VA, Bratton DL, Konowal A, Freed PW, Westcott JY, Henson PM. Macrophages that have ingested apoptotic cells in vitro inhibit proinflammatory cytokine production through autocrine/paracrine mechanisms involving TGF-beta, PGE2, and PAF. J Clin Invest. 1998;101:890-898. (Pubitemid 28096086)
4. Peters T, Sindrilaru A, Hinz B, et al. Wound-healing defect of CD18(-/-) mice due to a decrease in TGF-beta1 and myofibroblast differentiation. Embo J. 2005;24:3400-3410. (Pubitemid 41486778)
5. Roberts AB, Sporn MB, Assoian RK, et al. Transforming growth factor type beta: rapid induction of fibrosis and angiogenesis in vivo and stimulation of collagen formation in vitro. Proc Natl Acad Sci U S A. 1986;83:4167-4171.
6. Springer TA, Anderson DC. Leukocyte complement receptors and adhesion proteins in the inflammatory response: insights from an experiment of nature. Biochem Soc Symp. 1986;51:47-57.
7. Arnaout MA. Structure and function of the leukocyte adhesion molecules CD11/CD18. Blood. 1990;75:1037-1050. (Pubitemid 20086807)
8. Chiriac MT, Roesler J, Sindrilaru A, Scharffetter- Kochanek K, Zillikens D, Sitaru C. NADPH oxidase is required for neutrophil-dependent autoantibody-induced tissue damage. J Pathol. 2007;212:56-65. (Pubitemid 46746290)
9. Mizgerd JP, Kubo H, Kutkoski GJ, et al. Neutrophil emigration in the skin, lungs, and peritoneum: different requirements for CD11/CD18 revealed by CD18-deficient mice. J Exp Med. 1997;186:1357-1364. (Pubitemid 27469031)
10. Scharffetter-Kochanek K, Lu H, Norman K, et al. Spontaneous skin ulceration and defective T cell function in CD18 null mice. J Exp Med. 1998;188:119-131. (Pubitemid 28328611)
11. Sindrilaru A, Seeliger S, Ehrchen JM, et al. Site of blood vessel damage and relevance of CD18 in a murine model of immune complex-mediated vasculitis. J Invest Dermatol. 2007;127:447-454. (Pubitemid 46106924)
12. Liu Z, Zhao M, Li N, Diaz LA, Mayadas TN. Differential roles for beta2 integrins in experimental autoimmune bullous pemphigoid. Blood. 2006;107:1063-1069. (Pubitemid 43156306)
13. Auffray C, Fogg D, Garfa M, et al. Monitoring of blood vessels and tissues by a population of monocytes with patrolling behavior. Science. 2007;317:666-670. (Pubitemid 47229966)
14. Mevorach D, Mascarenhas JO, Gershov D, Elkon KB. Complement-dependent clearance of apoptotic cells by human macrophages. J Exp Med. 1998;188:2313-2320. (Pubitemid 29028503)
15. Bunting M, Harris ES, McIntyre TM, Prescott SM, Zimmerman GA. Leukocyte adhesion deficiency syndromes: adhesion and tethering defects involving beta 2 integrins and selectin ligands. Curr Opin Hematol. 2002;9:30-35. (Pubitemid 34025309)
16. Bowen TJ, Ochs HD, Altman LC, et al. Severe recurrent bacterial infections associated with defective adherence and chemotaxis in two patients with neutrophils deficient in a cell-associated glycoprotein. J Pediatr. 1982;101:932-940.
17. Mocsai A, Abram CL, Jakus Z, Hu Y, Lanier LL, Lowell CA. Integrin signaling in neutrophils and macrophages uses adaptors containing immunoreceptor tyrosine-based activation motifs. Nat Immunol. 2006;7:1326-1333. (Pubitemid 46111254)
18. Schymeinsky J, Mocsai A, Walzog B. Neutrophil activation via beta2 integrins (CD11/CD18): molecular mechanisms and clinical implications. Thromb Haemost. 2007;98:262-273. (Pubitemid 47260290)
19. Bustelo XR. Regulatory and signaling properties of the Vav family. Mol Cell Biol. 2000;20:1461-1477.
20. Turner M, Billadeau DD. VAV proteins as signal integrators for multi-subunit immune-recognition receptors. Nat Rev Immunol. 2002;2:476-486. (Pubitemid 37328739)
21. Fischer KD, Tedford K, Penninger JM. Vav links antigen-receptor signaling to the actin cytoskeleton. Semin Immunol. 1998;10:317-327. (Pubitemid 28375307)
22. Holsinger LJ, Graef IA, Swat W, et al. Defects in actin-cap formation in Vav-deficient mice implicate an actin requirement for lymphocyte signal transduction. Curr Biol. 1998;8:563-572. (Pubitemid 28222890)
23. Doody GM, Bell SE, Vigorito E, et al. Signal transduction through Vav-2 participates in humoral immune responses and B cell maturation. Nat Immunol. 2001;2:542-547. (Pubitemid 33705857)
24. Tedford K, Nitschke L, Girkontaite I, et al. Compensation between Vav-1 and Vav-2 in B cell development and antigen receptor signaling. Nat Immunol. 2001;2:548-555. (Pubitemid 33705858)
25. Fujikawa K, Miletic AV, Alt FW, et al. Vav1/2/3-null mice define an essential role for Vav family proteins in lymphocyte development and activation but a differential requirement in MAPK signaling in T and B cells. J Exp Med. 2003;198:1595-1608. (Pubitemid 37467173)
26. Yron I, Deckert M, Reff ME, Munshi A, Schwartz MA, Altman A. Integrin-dependent tyrosine phosphorylation and growth regulation by Vav. Cell Adhes Commun. 1999;7:1-11. (Pubitemid 29158602)
27. Cichowski K, Brugge JS, Brass LF. Thrombin receptor activation and integrin engagement stimulate tyrosine phosphorylation of the proto-oncogene product, p95vav, in platelets. J Biol Chem. 1996;271:7544-7550. (Pubitemid 26107030)
28. Gakidis MA, Cullere X, Olson T, et al. Vav GEFs are required for beta2 integrin-dependent functions of neutrophils. J Cell Biol. 2004;166:273-282. (Pubitemid 38988779)
29. Utomo A, Cullere X, Glogauer M, Swat W, Mayadas TN. Vav proteins in neutrophils are required for FcgammaR-mediated signaling to Rac GTPases and nicotinamide adenine dinucleotide phosphate oxidase component p40(phox). J Immunol. 2006;177:6388-6397. (Pubitemid 44628857)
30. Utomo A, Hirahashi J, Mekala D, et al. Requirement for Vav proteins in post-recruitment neutrophil cytotoxicity in IgG but not Ccmplement C3-dependent injury. J Immunol. 2008;180:6279-6287.
31. Hall AB, Gakidis MA, Glogauer M, et al. Requirements for Vav guanine nucleotide exchange factors and Rho GTPases in FcgammaR- and complement-mediated phagocytosis. Immunity. 2006;24:305-316.
32. Faccio R, Teitelbaum SL, Fujikawa K, et al. Vav3 regulates osteoclast function and bone mass. Nat Med. 2005;11:284-290. (Pubitemid 40460556)
33. Sauzeau V, Sevilla MA, Rivas-Elena JV, et al. Vav3 proto-oncogene deficiency leads to sympathetic hyperactivity and cardiovascular dysfunction. Nat Med. 2006;12:841-845. (Pubitemid 44050076)
34. Gabbiani G, Hirschel BJ, Ryan GB, Statkov PR, Majno G. Granulation tissue as a contractile organ. A study of structure and function. J Exp Med. 1972;135:719-734.
35. Tomasek JJ, Gabbiani G, Hinz B, Chaponnier C, Brown RA. Myofibroblasts and mechano-regulation of connective tissue remodelling. Nat Rev Mol Cell Biol. 2002;3:349-363. (Pubitemid 34619269)
36. Barcellos-Hoff MH, Dix TA. Redox-mediated activation of latent transforming growth factor-beta 1. Mol Endocrinol. 1996;10:1077-1083. (Pubitemid 26299216)
37. Wahl SM, Hunt DA, Wakefield LM, et al. Transforming growth factor type beta induces monocyte chemotaxis and growth factor production. Proc Natl Acad Sci U S A. 1987;84:5788-5792.
38. Fallman M, Andersson R, Andersson T. Signaling properties of CR3 (CD11b/CD18) and CR1 (CD35) in relation to phagocytosis of complement- opsonized particles. J Immunol. 1993;151:330-338. (Pubitemid 23206998)
39. Wilson RW, Ballantyne CM, Smith CW, et al. Gene targeting yields a CD18-mutant mouse for study of inflammation. J Immunol. 1993;151:1571-1578.
40. Anderson DC, Smith CW. Leukocyte Adhesion Deficiencies. New York, NY: McGraw-Hill; 2001.
41. Serini G, Gabbiani G. Mechanisms of myofibroblast activity and phenotypic modulation. Exp Cell Res. 1999;250:273-283. (Pubitemid 29367440)
42. Arora PD, McCulloch CA. Dependence of collagen remodelling on alpha-smooth muscle actin expression by fibroblasts. J Cell Physiol. 1994;159:161-175. (Pubitemid 24234588)
43. Hinz B, Celetta G, Tomasek JJ, Gabbiani G, Chaponnier C. Alpha-smooth muscle actin expression upregulates fibroblast contractile activity. Mol Biol Cell. 2001;12:2730-2741. (Pubitemid 33051938)
44. Desmouliere A, Geinoz A, Gabbiani F, Gabbiani G. Transforming growth factor-beta 1 induces alpha-smooth muscle actin expression in granulation tissue myofibroblasts and in quiescent and growing cultured fibroblasts. J Cell Biol. 1993;122:103-111. (Pubitemid 23188802)
45. Cowin AJ, Holmes TM, Brosnan P, Ferguson MW. Expression of TGF-beta and its receptors in murine fetal and adult dermal wounds. Eur J Dermatol. 2001;11:424-431. (Pubitemid 32801338)
46. Vedham V, Phee H, Coggeshall KM. Vav activation and function as a rac guanine nucleotide exchange factor in macrophage colony-stimulating factor-induced macrophage chemotaxis. Mol Cell Biol. 2005;25:4211-4220. (Pubitemid 40617666)
47. Graham DB, Robertson CM, Bautista J, et al. Neutrophil-mediated oxidative burst and host defense are controlled by a Vav-PLCgamma2 signaling axis in mice. J Clin Invest. 2007;117:3445-3452. (Pubitemid 350097000)
48. 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;90:1513-1522.
49. Castagna M, Takai Y, Kaibuchi K, Sano K, Kikkawa U, Nishizuka Y. Direct activation of calcium-activated, phospholipid-dependent protein kinase by tumor-promoting phorbol esters. J Biol Chem. 1982;257:7847-7851. (Pubitemid 12043279)
50. Ross GD, Vetvicka V. CR3 (CD11b, CD18): a phagocyte and NK cell membrane receptor with multiple ligand specificities and functions. Clin Exp Immunol. 1993;92:181-184. (Pubitemid 23151023)
51. Ren Y, Stuart L, Lindberg FP, et al. Nonphlogistic clearance of late apoptotic neutrophils by macrophages: efficient phagocytosis independent of beta 2 integrins. J Immunol. 2001;166:4743-4750. (Pubitemid 32233763)
52. Reynolds LE, Conti FJ, Lucas M, et al. Accelerated re-epithelialization in beta3-integrin-deficient mice is associated with enhanced TGF-beta1 signaling. Nat Med. 2005;11:167-174. (Pubitemid 40321352)
53. Colgan J, Rothman P. Manipulation of signaling to control allergic inflammation. Curr Opin Allergy Clin Immunol. 2007;7:51-56. (Pubitemid 46095886)
54. Wynn TA. Cellular and molecular mechanisms of fibrosis. J Pathol. 2008;214:199-210.