Extracellular low pH modulates phosphatidylserine-dependent phagocytosis in macrophages by increasing stabilin-1 expression

Journal of Biological Chemistry

Volumn 287, Issue 14, 2012, Pages 11261-11271

  Park, Seung Yoon ^b   Bae, Dong Jun ^a   Kim, Mi Jin ^b   Piao, Mei Lan ^a   Kim, In San ^a,c  

^a Kyungpook National University School of Medicine   (South Korea)

^b Dongguk University College of Medicine   (South Korea)

^c Korea Institute of Science and Technology   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

APOPTOTIC CELLS; EXTRACELLULAR; IMMUNE FUNCTION; IMMUNE SYSTEMS; MICROENVIRONMENTS; PH-RESPONSIVE; PHAGOCYTIC ACTIVITY; PHAGOCYTIC CAPACITY; RED BLOOD CELL; REPORTER ASSAY; TISSUE HOMEOSTASIS; TRANSCRIPTIONAL ACTIVATIONS;

ANTIGEN-ANTIBODY REACTIONS; ENZYME ACTIVITY; MACROPHAGES; TISSUE;

PH EFFECTS;

CD36 ANTIGEN; MEMBRANE RECEPTOR; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; STABILIN 1; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR ETS 2; UNCLASSIFIED DRUG;

ACIDIFICATION; ACIDITY; ANIMAL CELL; ARTICLE; BINDING SITE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; GENE EXPRESSION REGULATION; GENE TRANSLOCATION; HOMEOSTASIS; MACROPHAGE FUNCTION; MOUSE; NONHUMAN; PERITONEUM MACROPHAGE; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STABILITY; PROTEIN TRANSPORT; TRANSCRIPTION INITIATION;

ANIMALS; CELL ADHESION MOLECULES, NEURONAL; CELL LINE; EXTRACELLULAR SPACE; GENE EXPRESSION REGULATION; HUMANS; HYDROGEN-ION CONCENTRATION; MACROPHAGES, PERITONEAL; MAP KINASE KINASE 4; MICE; MICE, INBRED C57BL; PHAGOCYTOSIS; PHOSPHATIDYLSERINES; PROMOTER REGIONS, GENETIC; RATS; TRANSCRIPTIONAL ACTIVATION;

EID: 84859510048     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.310953     Document Type: Article

References (41)

1. Dubos, R. J. (1955) The micro-environment of inflammation or Metchnikoff revisited. Lancet 269, 1-5
2. Kopaniak, M. M., Issekutz, A. C., and Movat, H. Z. (1980) Kinetics of acute inflammation induced by E. coli in rabbits. Quantitation of blood flow, enhanced vascular permeability, hemorrhage, and leukocyte accumulation. Am. J. Pathol. 98, 485-498 (Pubitemid 10095801)
3. Grimshaw, M. J., and Balkwill, F. R. (2001) Inhibition of monocyte and macrophage chemotaxis by hypoxia and inflammation. A potential mechanism. Eur. J. Immunol. 31, 480-489 (Pubitemid 32166603)
4. van Zwieten, R., Wever, R., Hamers, M. N., Weening, R. S., and Roos, D. (1981) Extracellular proton release by stimulated neutrophils. J. Clin. Invest. 68, 310-313 (Pubitemid 11048105)
5. Edlow, D. W., and Sheldon, W. H. (1971) The pH of inflammatory exudates. Proc. Soc. Exp. Biol. Med. 137, 1328-1332
6. Ward, T. T., and Steigbigel, R. T. (1978) Acidosis of synovial fluid correlates with synovial fluid leukocytosis. Am. J. Med. 64, 933-936 (Pubitemid 8358584)
7. Tannock, I. F., and Rotin, D. (1989) Acid pH in tumors and its potential for therapeutic exploitation. Cancer Res. 49, 4373-4384 (Pubitemid 19208329)
8. Vaupel, P., Kallinowski, F., and Okunieff, P. (1989) Blood flow, oxygen and nutrient supply, and metabolic microenvironment of human tumors. A review. Cancer Res. 49, 6449-6465 (Pubitemid 20008770)
9. Savill, J., and Fadok, V. (2000) Corpse clearance defines the meaning of cell death. Nature 407, 784-788
10. Ravichandran, K. S., and Lorenz, U. (2007) Engulfment of apoptotic cells. Signals for a good meal. Nat. Rev. Immunol. 7, 964-974 (Pubitemid 350166061)
11. Erwig, L. P., and Henson, P. M. (2008) Clearance of apoptotic cells by phagocytes. Cell Death Differ. 15, 243-250
12. Hanly, E. J., Aurora, A. A., Shih, S. P., Fuentes, J. M., Marohn, M. R., De Maio, A., and Talamini, M. A. (2007) Peritoneal acidosis mediates immunoprotection in laparoscopic surgery. Surgery 142, 357-364 (Pubitemid 47302031)
13. Mogi, C., Tobo, M., Tomura, H., Murata, N., He, X. D., Sato, K., Kimura, T., Ishizuka, T., Sasaki, T., Sato, T., Kihara, Y., Ishii, S., Harada, A., and Okajima, F. (2009) Involvement of proton-sensing TDAG8 in extracellular acidification-induced inhibition of proinflammatory cytokine production in peritoneal macrophages. J. Immunol. 182, 3243-3251
14. Kzhyshkowska, J., Gratchev, A., and Goerdt, S. (2006) Stabilin-1, a homeostatic scavenger receptor with multiple functions. J. Cell Mol. Med. 10, 635-649 (Pubitemid 44874274)
15. Goerdt, S., Bhardwaj, R., and Sorg, C. (1993) Inducible expression of MS-1 high-molecular-weight protein by endothelial cells of continuous origin and by dendritic cells/macrophages in vivo and in vitro. Am. J. Pathol. 142, 1409-1422 (Pubitemid 24058128)
16. Politz, O., Gratchev, A., McCourt, P. A., Schledzewski, K., Guillot, P., Johansson, S., Svineng, G., Franke, P., Kannicht, C., Kzhyshkowska, J., Longati, P., Velten, F. W., and Goerdt, S. (2002) Stabilin-1 and -2 constitute a novel family of fasciclin-like hyaluronan receptor homologues. Biochem. J. 362, 155-164 (Pubitemid 34174473)
17. Adachi, H., and Tsujimoto, M. (2002) FEEL-1, a novel scavenger receptor with in vitro bacteria-binding and angiogenesis-modulating activities. J. Biol. Chem. 277, 34264-34270
18. Tamura, Y., Adachi, H., Osuga, J., Ohashi, K., Yahagi, N., Sekiya, M., Okazaki, H., Tomita, S., Iizuka, Y., Shimano, H., Nagai, R., Kimura, S., Tsujimoto, M., and Ishibashi, S. (2003) FEEL-1 and FEEL-2 are endocytic receptors for advanced glycation end products. J. Biol. Chem. 278, 12613-12617 (Pubitemid 36800020)
19. Kzhyshkowska, J., Gratchev, A., Brundiers, H., Mamidi, S., Krusell, L., and Goerdt, S. (2005) Phosphatidylinositide 3-kinase activity is required for stabilin-1-mediated endosomal transport of acLDL. Immunobiology 210, 161-173 (Pubitemid 41025157)
20. Kzhyshkowska, J., Workman, G., Cardó-Vila, M., Arap, W., Pasqualini, R., Gratchev, A., Krusell, L., Goerdt, S., and Sage, E. H. (2006) Novel function of alternatively activated macrophages. Stabilin-1-mediated clearance of SPARC. J. Immunol. 176, 5825-5832
21. Kzhyshkowska, J., Mamidi, S., Gratchev, A., Kremmer, E., Schmuttermaier, C., Krusell, L., Haus, G., Utikal, J., Schledzewski, K., Scholtze, J., and Goerdt, S. (2006) Novel stabilin-1 interacting chitinase-like protein (SI-CLP) is up-regulated in alternatively activated macrophages and secreted via lysosomal pathway. Blood 107, 3221-3228
22. Kzhyshkowska, J., Gratchev, A., Schmuttermaier, C., Brundiers, H., Krusell, L., Mamidi, S., Zhang, J., Workman, G., Sage, E. H., Anderle, C., Sedlmayr, P., and Goerdt, S. (2008) Alternatively activated macrophages regulate extracellular levels of the hormone placental lactogen via receptor-mediated uptake and transcytosis. J. Immunol. 180, 3028-3037
23. Park, S. Y., Jung, M. Y., Lee, S. J., Kang, K. B., Gratchev, A., Riabov, V., Kzhyshkowska, J., and Kim, I. S. (2009) Stabilin-1 mediates phosphatidylserine-dependent clearance of cell corpses in alternatively activated macrophages. J. Cell Sci. 122, 3365-3373
24. Lee, S. J., Park, S. Y., Jung, M. Y., Bae, S. M., and Kim, I. S. (2011) Mechanism for phosphatidylserine-dependent erythrophagocytosis in mouse liver. Blood 117, 5215-5223
25. Park, S. Y., Jung, M. Y., Kim, H. J., Lee, S. J., Kim, S. Y., Lee, B. H., Kwon, T. H., Park, R. W., and Kim, I. S. (2008) Rapid cell corpse clearance by stabilin-2, a membrane phosphatidylserine receptor. Cell Death Differ. 15, 192-201
26. Kim, S., Bae, D. J., Hong, M., Park, S. Y., and Kim, I. S. (2010) The conserved histidine in epidermal growth factor-like domains of stabilin-2 modulates pH-dependent recognition of phosphatidylserine in apoptotic cells. Int. J. Biochem. Cell Biol. 42, 1154-1163
27. Yoshida, H., Kawane, K., Koike, M., Mori, Y., Uchiyama, Y., and Nagata, S. (2005) Phosphatidylserine-dependent engulfment by macrophages of nuclei from erythroid precursor cells. Nature 437, 754-758 (Pubitemid 41486546)
28. Bellocq, A., Suberville, S., Philippe, C., Bertrand, F., Perez, J., Fouqueray, B., Cherqui, G., and Baud, L. (1998) Low environmental pH is responsible for the induction of nitric-oxide synthase in macrophages. Evidence for involvement of nuclear factor-κB activation. J. Biol. Chem. 273, 5086-5092 (Pubitemid 28108668)
29. Martínez, D., Vermeulen, M., von Euw, E., Sabatté, J., Maggíni, J., Ceballos, A., Trevani, A., Nahmod, K., Salamone, G., Barrio, M., Giordano, M., Amigorena, S., and Geffner, J. (2007) Extracellular acidosis triggers the maturation of human dendritic cells and the production of IL-12. J. Immunol. 179, 1950-1959
30. Serrano, C. V., Jr., Fraticelli, A., Paniccia, R., Teti, A., Noble, B., Corda, S., Faraggiana, T., Ziegelstein, R. C., Zweier, J. L., and Capogrossi, M. C. (1996) pH dependence of neutrophil-endothelial cell adhesion and adhesion molecule expression. Am. J. Physiol. 271, C962-C970
31. Chung, S. W., Chen, Y. H., Yet, S. F., Layne, M. D., and Perrella, M. A. (2006) Endotoxin-induced down-regulation of Elk-3 facilitates heme oxygenase-1 induction in macrophages. J. Immunol. 176, 2414-2420 (Pubitemid 43201691)
32. Chung, S. W., Chen, Y. H., and Perrella, M. A. (2005) Role of Ets-2 in the regulation of heme oxygenase-1 by endotoxin. J. Biol. Chem. 280, 4578-4584 (Pubitemid 40288625)
33. Han, M., Yan, W., Guo, W., Xi, D., Zhou, Y., Li, W., Gao, S., Liu, M., Levy, G., Luo, X., and Ning, Q. (2008) Hepatitis B virus-induced hFGL2 transcription is dependent on c-Ets-2 and MAPK signal pathway. J. Biol. Chem. 283, 32715-32729
34. Libera, J., Pomorski, T., Müller, P., and Herrmann, A. (1997) Influence of pH on phospholipid redistribution in human erythrocyte membrane. Blood 90, 1684-1693 (Pubitemid 27355443)
35. Yordy, J. S., and Muise-Helmericks, R. C. (2000) Signal transduction and the Ets family of transcription factors. Oncogene 19, 6503-6513 (Pubitemid 32108440)
36. Yamamoto, H., Flannery, M. L., Kupriyanov, S., Pearce, J., McKercher, S. R., Henkel, G. W., Maki, R. A., Werb, Z., and Oshima, R. G. (1998) Defective trophoblast function in mice with a targeted mutation of Ets2. Genes Dev. 12, 1315-1326 (Pubitemid 28213407)
37. Lardner, A. (2001) The effects of extracellular pH on immune function. J. Leukocyte Biol. 69, 522-530
38. Savill, J. S., Henson, P. M., and Haslett, C. (1989) Phagocytosis of aged human neutrophils by macrophages is mediated by a novel "charge- sensitive"recognition mechanism. J. Clin. Invest. 84, 1518-1527 (Pubitemid 19272240)
39. Köhler, G., Hering, U., Zschörnig, O., and Arnold, K. (1997) Annexin V interaction with phosphatidylserine-containing vesicles at low and neutral pH. Biochemistry 36, 8189-8194 (Pubitemid 27284197)
40. Park, S. Y., Kim, S. Y., Jung, M. Y., Bae, D. J., and Kim, I. S. (2008) Epidermal growth factor-like domain repeat of stabilin-2 recognizes phosphatidylserine during cell corpse clearance. Mol. Cell Biol. 28, 5288-5298
41. Bratton, D. L., and Henson, P. M. (2008) Apoptotic cell recognition. Will the real phosphatidylserine receptor(s) please stand up? Curr. Biol. 18, R76-R79