Impaired apoptotic cell clearance in CGD due to altered macrophage programming is reversed by phosphatidylserine-dependent production of IL-4

Blood

Volumn 113, Issue 9, 2009, Pages 2047-2055

  Fernandez Boyanapalli, Ruby F ^a   Frasch, S Courtney ^a   McPhillips, Kathleen ^b   Vandivier, R William ^c   Harry, Brian L ^c   Riches, David W H ^a   Henson, Peter M ^a   Bratton, Donna L ^a  

^a NATIONAL JEWISH MEDICAL AND RESEARCH CENTER   (United States)

^b UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^c DENVER HEALTH AND HOSPITAL AUTHORITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARACHIDONATE 12 LIPOXYGENASE; ARACHIDONATE 15 LIPOXYGENASE; GAMMA INTERFERON; INTERLEUKIN 4; LIPOPOLYSACCHARIDE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PHOSPHATIDYLSERINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CHRONIC GRANULOMATOUS DISEASE; COMPREHENSION; CONTROLLED STUDY; CYTOKINE PRODUCTION; EX VIVO STUDY; FEMALE; HYPOTHESIS; IN VIVO STUDY; INFLAMMATION; INJECTION; MACROPHAGE; MALE; MOUSE; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; WILD TYPE;

EID: 61849091325     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2008-05-160564     Document Type: Article

References (52)

1. Gardai SJ, McPhillips KA, Frasch SC, et al. Cell-surface calreticulin initiates clearance of viable or apoptotic cells through trans-activation of LRP on the phagocyte. Cell. 2005;123:321-334.
2. deCathelineau AM, Henson PM. The final step in programmed cell death: phagocytes carry apo-ptotic cells to the grave. Essays Biochem. 2003; 39:105-117.
3. Freire-de-Lima CG, Xiao YQ, Gardai SJ, Bratton DL, Schiemann WP, Henson PM. Apoptotic cells, through transforming growth factor-beta, coordinately induce anti-inflammatory and suppress pro-inflammatory eicosanoid and NO synthesis in murine macrophages. J Biol Chem. 2006;281: 38376-38384.
4. Taylor PR, Carugati A, Fadok VA, et al. A hierarchical role for classical pathway complement proteins in the clearance of apoptotic cells in vivo. J Exp Med. 2000;192:359-366.
5. Vandivier RW, Fadok VA, Hoffmann PR, et al. Elastase-mediated phosphatidylserine receptor cleavage impairs apoptotic cell clearance in cystic fibrosis and bronchiectasis. J Clin Invest. 2002;109:661-670.
6. Segal BH, Leto TL, Gallin JI, Malech HL, Holland SM. Genetic, biochemical, and clinical features of chronic granulomatous disease. Medicine (Baltimore). 2000;79:170-200.
7. Romani L, Fallarino F, De Luca A, et al. Defective tryptophan catabolism underlies inflammation in mouse chronic granulomatous disease. Nature. 2008;451:211-215.
8. Assari T. Chronic granulomatous disease: fundamental stages in our understanding of CGD. Med Immunol. 2006;5:4.
9. Winkelstein JA, Marino MC, Johnston RB Jr, et al. Chronic granulomatous disease: report on a national registry of 368 patients. Medicine (Baltimore). 2000;79:155-169.
10. Brown JR, Goldblatt D, Buddle J, Morton L, Thrasher AJ. Diminished production of anti-inflammatory mediators during neutrophil apoptosis and macrophage phagocytosis in chronic granulomatous disease (CGD). J Leukoc Biol. 2003;73: 591-599.
11. Morgenstern DE, Gifford MA, Li LL, Doerschuk CM, Dinauer MC. Absence of respiratory burst in X-linked chronic granulomatous disease mice leads to abnormalities in both host defense and inflammatory response to Aspergillus fumigatus. J Exp Med. 1997;185:207-218.
12. WarrisA, Netea MG, Wang JE, et al. Cytokine release in healthy donors and patients with chronic granulomatous disease upon stimulation with Aspergillus fumigatus. Scand J Infect Dis. 2003;35:482-487.
13. Segal BH, Kuhns DB, Ding L, Gallin JI, Holland SM. Thioglycollate peritonitis in mice lacking C5, 5-lipoxygenase, or p47(phox): complement, leu-kotrienes, and reactive oxidants in acute inflammation. J Leukoc Biol. 2002;71:410-416.
14. Gallin JI, Buescher ES. Abnormal regulation of inflammatory skin responses in male patients with chronic granulomatous disease. Inflammation. 1983;7:227-232.
15. Jackson SH, Gallin JI, Holland SM. The p47phox mouse knock-out model of chronic granulomatous disease. J Exp Med. 1995;182:751-758.
16. Arroyo A, Modriansky M, Serinkan FB, et al. NADPH oxidase-dependent oxidation and externalization of phosphatidylserine during apoptosis in Me2SO-differentiated HL-60 cells. Role in phagocytic clearance. J Biol Chem. 2002;277: 49965-49975.
17. Hampton MB, Vissers MC, Keenan JI, Winterbourn CC. Oxidant-mediated phosphatidylserine exposure and macrophage uptake of activated neutrophils: possible impairment in chronic granulomatous disease. J Leukoc Biol. 2002;71:775-781.
18. YamamotoA, Taniuchi S, Tsuji S, Hasui M, Kobayashi Y. Role of reactive oxygen species in neutrophil apoptosis following ingestion of heat-killed Staphylococcus aureus. Clin Exp Immunol. 2002;129:479-484.
19. Fadok VA, Savill JS, Haslett C, et al. Different populations of macrophages use either the vitro-nectin receptor or the phosphatidylserine receptor to recognize and remove apoptotic cells. J Immunol. 1992;149:4029-4035.
20. Riches DW, Underwood GA. Expression of interferon-beta during the triggering phase of macrophage cytocidal activation: evidence for an auto-crine/paracrine role in the regulation of this state. J Biol Chem. 1991;266:24785-24792.
21. Haslett C, Guthrie LA, Kopaniak MM, Johnston RB Jr, Henson PM. Modulation of multiple neutrophil functions by preparative methods and trace amounts of bacterial lipopolysaccharide. Am J Pathol. 1985;119:101-110.
22. Hoffmann PR, Kench JA, VondracekA, et al. Interaction between phosphatidylserine and the phosphatidylserine receptor inhibits immune responses in vivo. J Immunol. 2005;174:1393-1404.
23. Morimoto K, Janssen WJ, Fessler MB, et al. Lovastatin enhances clearance of apoptotic cells (efferocytosis) with implications for chronic obstructive pulmonary disease. J Immunol. 2006; 176:7657-7665.
24. Yan JJ, Jung JS, Lee JE, et al. Therapeutic effects of lysophosphatidylcholine in experimental sepsis. Nat Med. 2004;10:161-167.
25. Montaner LJ, da Silva RP, Sun J, et al. Type 1 and type 2 cytokine regulation of macrophage endocytosis: differential activation by IL-4/IL-13 as opposed to IFN-gamma or IL-10. J Immunol. 1999;162:4606-4613.
26. Ogden CA, Pound JD, Batth BK, et al. Enhanced apoptotic cell clearance capacity and B cell survival factor production by IL-10-activated macro-phages: implications for Burkitt's lymphoma. J Immunol. 2005;174:3015-3023.
27. Sampson LL, Heuser J, Brown EJ. Cytokine regulation of complement receptor-mediated ingestion by mouse peritoneal macrophages. M-CSF and IL-4 activate phagocytosis by a common mechanism requiring autostimulation by IFN-beta. J Immunol. 1991;146:1005-1013.
28. Capsoni F, Minonzio F, Ongari AM, Carbonelli V, Galli A, Zanussi C. IL-10 up-regulates human monocyte phagocytosis in the presence of IL-4 and IFN-gamma. J Leukoc Biol. 1995;58:351-358.
29. Xu W, RoosA, Schlagwein N, Woltman AM, Daha MR, van Kooten C. IL-10-producing macro-phages preferentially clear early apoptotic cells. Blood. 2006;107:4930-4937.
30. Gratchev A, Kzhyshkowska J, Utikal J, Goerdt S. Interleukin-4 and dexamethasone counterregu-late extracellular matrix remodelling and phagocytosis in type-2 macrophages. Scand J Immunol. 2005;61:10-17.
31. Savill J, Hogg N, Ren Y, Haslett C.Throm-bospondin cooperates with CD36 and the vitronectin receptor in macrophage recognition of neutrophils undergoing apoptosis. J Clin Invest. 1992;90:1513-1522.
32. Gregory CD, Devitt A. CD14 and apoptosis. Apoptosis. 1999;4:11-20.
33. Asada K, Sasaki S, SudaT, Chida K, Nakamura H. Antiinflammatory roles of peroxisome proliferator-activated receptor gamma in human alveolar macrophages. Am J Respir Crit Care Med. 2004; 169:195-200.
34. Majai G, Sarang Z, Csomos K, Zahuczky G, Fesus L. PPARgamma-dependent regulation of human macrophages in phagocytosis of apoptotic cells. Eur J Immunol. 2007;37:1343-1354.
35. Huang JT, Welch JS, Ricote M, et al. Interleukin-4-dependent production of PPAR-gamma ligands in macrophages by 12/15-lipoxygenase. Nature. 1999;400:378-382.
36. Profita M, SalaA, Siena L, et al. Leukotriene B4 production in human mononuclear phagocytes is modulated by interleukin-4-induced 15-lipoxygenase. J Pharmacol ExpTher. 2002;300:868-875.
37. 3). J Immunol. 1998;161:6250-6257.
38. Cohen PL, Caricchio R, Abraham V, et al. Delayed apoptotic cell clearance and lupus-like autoimmunity in mice lacking the c-mer membrane tyrosine kinase. J Exp Med. 2002;196:135-140.
39. van der Kleij D, Latz E, Brouwers JF, et al. A novel host-parasite lipid cross-talk: schistosomal lyso-phosphatidylserine activates toll-like receptor 2 and affects immune polarization. J Biol Chem. 2002;277:48122-48129.
40. Nagy L, Tontonoz P, Alvarez JG, Chen H, Evans RM. Oxidized LDL regulates macrophage gene expression through ligand activation of PPAR-gamma. Cell. 1998;93:229-240.
41. Henderson WR, Klebanoff SJ. Leukotriene production and inactivation by normal, chronic granulomatous disease and myeloperoxidase-deficient neutrophils. J Biol Chem. 1983;258: 13522-13527.
42. 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.
43. Miyanishi M, Tada K, Koike M, Uchiyama Y, Kitamura T, Nagata S. Identification of Tim4 as a phosphatidylserine receptor. Nature. 2007;450: 435-439.
44. Park D, Tosello-Trampont AC, Elliott MR, et al. BAI1 is an engulfment receptor for apoptotic cells upstream of the ELMO/Dock180/Rac module. Nature. 2007;450:430-434.
45. Park SY, Jung MY, Kim HJ, et al. Rapid cell corpse clearance by stabilin-2, a membrane phosphatidylserine receptor. Cell Death Differ. 2008;15:192-201.
46. Bratton DL, Henson PM. Apoptotic cell recognition: will the real phosphatidylserine receptor(s) please stand up? Curr Biol. 2008;18:R76-R79.
47. Stark MA, Huo Y, Burcin TL, Morris MA, Olson TS, Ley K. Phagocytosis of apoptotic neutrophils regulates granulopoiesis via IL-23 and IL-17. Immunity. 2005;22:285-294.
48. Gordon S. Alternative activation of macrophages. Nat Rev Immunol. 2003;3:23-35.
49. Mantovani A, Sozzani S, Locati M, Allavena P, Sica A. Macrophage polarization: tumor-associated macrophages as a paradigm for polarized M2 mononuclear phagocytes. Trends Immunol. 2002;23:549-555.
50. Wang Y, Wang YP, Zheng G, et al. Ex vivo programmed macrophages ameliorate experimental chronic inflammatory renal disease. Kidney Int. 2007;72:290-299.
51. Bladon J, Taylor P. Extracorporeal photopheresis reduces the number of mononuclear cells that produce pro-inflammatory cytokines, when tested ex-vivo. J Clin Apher. 2002;17:177-182.
52. Setterblad N, Garban F, Weigl R, et al. Extracorporeal photophoresis increases sensitivity of monocytes from patients with graft-versus-host disease to HLA-DR-mediated cell death. Transfusion. 2008;48:169-177.