A requirement for the p85 PI3K adapter protein BCAP in the protection of macrophages from apoptosis induced by endoplasmic reticulum stress

Journal of Immunology

Volumn 187, Issue 2, 2011, Pages 619-625

  Song, SungWon ^a   Chew, Claude ^a   Dale, Benjamin M ^a   Traum, Daniel ^a   Peacock, James ^a   Yamazaki, Tetsuo ^b   Clynes, Raphael ^a   Kurosaki, Tomohiro ^c,d   Greenberg, Steven ^a  

^a Columbia University ^*  (United States)

^b KYOTO UNIVERSITY   (Japan)

^c Institute of Physical and Chemical Research   (Japan)

^d OSAKA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

B CELL ADAPTER PROTEIN; MEMBRANE PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; PROTEIN P85; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE; THAPSIGARGIN; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; BINDING SITE; CELL SURVIVAL; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; ENZYME ACTIVITY; HUMAN; HUMAN CELL; INNATE IMMUNITY; MACROPHAGE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN PHOSPHORYLATION; SARCOPLASMIC RETICULUM; SIGNAL TRANSDUCTION; UPREGULATION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; APOPTOSIS; BONE MARROW CELLS; CELL SURVIVAL; ENDOPLASMIC RETICULUM; IMMUNITY, INNATE; LIGANDS; LIPOPOLYSACCHARIDES; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PHOSPHATIDYLINOSITOL 3-KINASES; STRESS, PHYSIOLOGICAL; UP-REGULATION;

EID: 79960505654     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0903425     Document Type: Article

References (50)

1. Tabas, I. 2005. Consequences and therapeutic implications of macrophage apoptosis in atherosclerosis: the importance of lesion stage and phagocytic efficiency. Arterioscler. Thromb. Vasc. Biol. 25: 2255-2264.
2. Endo, M., M. Mori, S. Akira, and T. Gotoh. 2006. C/EBP homologous protein (CHOP) is crucial for the induction of caspase-11 and the pathogenesis of lipopolysaccharide-induced inflammation. J. Immunol. 176: 6245-6253.
3. Maiti, D., A. Bhattacharyya, and J. Basu. 2001. Lipoarabinomannan from Mycobacterium tuberculosis promotes macrophage survival by phosphorylating Bad through a phosphatidylinositol 3-kinase/Akt pathway. J. Biol. Chem. 276: 329-333.
4. Marsh, C. B., R. P. Pomerantz, J. M. Parker, A. V. Winnard, E. L. Mazzaferri, Jr., N. Moldovan, T. W. Kelley, E. Beck, and M. D. Wewers. 1999. Regulation of monocyte survival in vitro by deposited IgG: role of macrophage colony-stimulating factor. J. Immunol. 162: 6217-6225.
5. Monick, M. M., R. K. Mallampalli, A. B. Carter, D. M. Flaherty, D. McCoy, P. K. Robeff, M. W. Peterson, and G. W. Hunninghake. 2001. Ceramide regulates lipopolysaccharide-induced phosphatidylinositol 3-kinase and Akt activity in human alveolar macrophages. J. Immunol. 167: 5977-5985.
6. Gu, H., R. J. Botelho, M. Yu, S. Grinstein, and B. G. Neel. 2003. Critical role for scaffolding adapter Gab2 in Fc g R-mediated phagocytosis. J. Cell Biol. 161: 1151-1161.
7. Okada, T., A. Maeda, A. Iwamatsu, K. Gotoh, and T. Kurosaki. 2000. BCAP: the tyrosine kinase substrate that connects B cell receptor to phosphoinositide 3-kinase activation. Immunity 13: 817-827. (Pubitemid 32041804)
8. Yamazaki, T., and T. Kurosaki. 2003. Contribution of BCAP to maintenance of mature B cells through c-Rel. Nat. Immunol. 4: 780-786.
9. MacFarlane, A. W., IV, T. Yamazaki, M. Fang, L. J. Sigal, T. Kurosaki, and K. S. Campbell. 2008. Enhanced NK-cell development and function in BCAP-deficient mice. Blood 112: 131-140.
10. Yamazaki, T., K. Takeda, K. Gotoh, H. Takeshima, S. Akira, and T. Kurosaki. 2002. Essential immunoregulatory role for BCAP in B cell development and function. J. Exp. Med. 195: 535-545.
11. Stanley, E. R., and P. M. Heard. 1977. Factors regulating macrophage production and growth. Purification and some properties of the colony stimulating factor from medium conditioned by mouse L cells. J. Biol. Chem. 252: 4305-4312.
12. Kawasaki, H., T. Morooka, S. Shimohama, J. Kimura, T. Hirano, Y. Gotoh, and E. Nishida. 1997. Activation and involvement of p38 mitogen-activated protein kinase in glutamate-induced apoptosis in rat cerebellar granule cells. J. Biol. Chem. 272: 18518-18521.
13. Aiba, Y., M. Kameyama, T. Yamazaki, T. F. Tedder, and T. Kurosaki. 2008. Regulation of B-cell development by BCAP and CD19 through their binding to phosphoinositide 3-kinase. Blood 111: 1497-1503. (Pubitemid 351213438)
14. Battersby, A., A. Csiszár, M. Leptin, and R. Wilson. 2003. Isolation of proteins that interact with the signal transduction molecule Dof and identification of a functional domain conserved between Dof and vertebrate BCAP. J. Mol. Biol. 329: 479-493.
15. Carnero, A., C. Blanco-Aparicio, O. Renner, W. Link, and J. F. Leal. 2008. The PTEN/PI3K/AKT signalling pathway in cancer, therapeutic implications. Curr. Cancer Drug Targets 8: 187-198.
16. Marone, R., V. Cmiljanovic, B. Giese, and M. P. Wymann. 2008. Targeting phosphoinositide 3-kinase: moving towards therapy. Biochim. Biophys. Acta 1784: 159-185.
17. Parcellier, A., L. A. Tintignac, E. Zhuravleva, and B. A. Hemmings. 2008. PKB and the mitochondria: AKTing on apoptosis. Cell. Signal. 20: 21-30.
18. Wang, Y., M. M. Zeigler, G. K. Lam, M. G. Hunter, T. D. Eubank, V. V. Khramtsov, S. Tridandapani, C. K. Sen, and C. B. Marsh. 2007. The role of the NADPH oxidase complex, p38 MAPK, and Akt in regulating human monocyte/macrophage survival. Am. J. Respir. Cell Mol. Biol. 36: 68-77.
19. Liu, H., H. Perlman, L. J. Pagliari, and R. M. Pope. 2001. Constitutively activated Akt-1 is vital for the survival of human monocyte-differentiated macrophages. Role of Mcl-1, independent of nuclear factor (NF)-kappaB, Bad, or caspase activation. J. Exp. Med. 194: 113-126.
20. Ruhland, A., N. Leal, and P. E. Kima. 2007. Leishmania promastigotes activate PI3K/Akt signalling to confer host cell resistance to apoptosis. Cell. Microbiol. 9: 84-96.
21. Perlman, H., L. J. Pagliari, C. Georganas, T. Mano, K. Walsh, and R. M. Pope. 1999. FLICE-inhibitory protein expression during macrophage differentiation confers resistance to fas-mediated apoptosis. J. Exp. Med. 190: 1679-1688.
22. Lin, H., C. Chen, and B. D. Chen. 2001. Resistance of bone marrow-derived macrophages to apoptosis is associated with the expression of X-linked inhibitor of apoptosis protein in primary cultures of bone marrow cells. Biochem. J. 353: 299-306.
23. Liu, H., Y. Ma, L. J. Pagliari, H. Perlman, C. Yu, A. Lin, and R. M. Pope. 2004. TNF-α-induced apoptosis of macrophages following inhibition of NF-kappa B: a central role for disruption of mitochondria. J. Immunol. 172: 1907-1915.
24. Devries-Seimon, T., Y. Li, P. M. Yao, E. Stone, Y. Wang, R. J. Davis, R. Flavell, and I. Tabas. 2005. Cholesterol-induced macrophage apoptosis requires ER stress pathways and engagement of the type A scavenger receptor. J. Cell Biol. 171: 61-73. (Pubitemid 41434602)
25. Han, S., C. P. Liang, T. DeVries-Seimon, M. Ranalletta, C. L. Welch, K. Collins-Fletcher, D. Accili, I. Tabas, and A. R. Tall. 2006. Macrophage insulin receptor deficiency increases ER stress-induced apoptosis and necrotic core formation in advanced atherosclerotic lesions. Cell Metab. 3: 257-266.
26. Kim, K. H., Y. Gao, K. Walder, G. R. Collier, J. Skelton, and A. H. Kissebah. 2007. SEPS1 protects RAW264.7 cells from pharmacological ER stress agent-induced apoptosis. Biochem. Biophys. Res. Commun. 354: 127-132.
27. Zhou, J., S. Lhoták, B. A. Hilditch, and R. C. Austin. 2005. Activation of the unfolded protein response occurs at all stages of atherosclerotic lesion development in apolipoprotein E-deficient mice. Circulation 111: 1814-1821.
28. Lytton, J., M. Westlin, and M. R. Hanley. 1991. Thapsigargin inhibits the sarcoplasmic or endoplasmic reticulum Ca-ATPase family of calcium pumps. J. Biol. Chem. 266: 17067-17071.
29. Seimon, T. A., A. Obstfeld, K. J. Moore, D. T. Golenbock, and I. Tabas. 2006. Combinatorial pattern recognition receptor signaling alters the balance of life and death in macrophages. Proc. Natl. Acad. Sci. USA 103: 19794-19799.
30. Hundal, R. S., B. S. Salh, J. W. Schrader, A. Gómez-Muñoz, V. Duronio, and U. P. Steinbrecher. 2001. Oxidized low density lipoprotein inhibits macrophage apoptosis through activation of the PI 3-kinase/PKB pathway. J. Lipid Res. 42: 1483-1491.
31. Iida, K. T., H. Suzuki, H. Sone, H. Shimano, H. Toyoshima, S. Yatoh, T. Asano, Y. Okuda, and N. Yamada. 2002. Insulin inhibits apoptosis of macrophage cell line, THP-1 cells, via phosphatidylinositol-3-kinase-dependent pathway. Arterioscler. Thromb. Vasc. Biol. 22: 380-386.
32. Koh, J. S., W. Lieberthal, S. Heydrick, and J. S. Levine. 1998. Lysophosphatidic acid is a major serum noncytokine survival factor for murine macrophages which acts via the phosphatidylinositol 3-kinase signaling pathway. J. Clin. Invest. 102: 716-727.
33. Murray, J. T., G. Craggs, L. Wilson, and S. Kellie. 2000. Mechanism of phosphatidylinositol 3-kinase-dependent increases in BAC1.2F5 macrophage-like cell density in response to M-CSF: phosphatidylinositol 3-kinase inhibitors increase the rate of apoptosis rather than inhibit DNA synthesis. Inflamm. Res. 49: 610-618.
34. Scheid, M. P., R. W. Lauener, and V. Duronio. 1995. Role of phosphatidylinositol 3-OH-kinase activity in the inhibition of apoptosis in haemopoietic cells: phosphatidylinositol 3-OH-kinase inhibitors reveal a difference in signalling between interleukin-3 and granulocyte-macrophage colony stimulating factor. Biochem. J. 312: 159-162.
35. Yamaki, K., J. Hong, K. Hiraizumi, J. W. Ahn, O. Zee, and K. Ohuchi. 2002. Participation of various kinases in staurosporine induced apoptosis of RAW 264.7 cells. J. Pharm. Pharmacol. 54: 1535-1544.
36. Choi, H. J., and T. E. Smithgall. 2004. HIV-1 Nef promotes survival of TF-1 macrophages by inducing Bcl-XL expression in an extracellular signal-regulated kinase-dependent manner. J. Biol. Chem. 279: 51688-51696.
37. L)and XIAP in the prolonged survival of monocytic cells. Leukemia 17: 390-400.
38. Lombardo, E., A. Alvarez-Barrientos, B. Maroto, L. Boscá, and U. G. Knaus. 2007. TLR4-mediated survival of macrophages is MyD88 dependent and requires TNF-α autocrine signalling. J. Immunol. 178: 3731-3739.
39. Monick, M. M., L. S. Powers, C. W. Barrett, S. Hinde, A. Ashare, D. J. Groskreutz, T. Nyunoya, M. Coleman, D. R. Spitz, and G. W. Hunninghake. 2008. Constitutive ERK MAPK activity regulates macrophage ATP production and mitochondrial integrity. J. Immunol. 180: 7485-7496.
40. Nyunoya, T., M. M. Monick, L. S. Powers, T. O. Yarovinsky, and G. W. Hunninghake. 2005. Macrophages survive hyperoxia via prolonged ERK activation due to phosphatase down-regulation. J. Biol. Chem. 280: 26295-26302.
41. Fettucciari, K., I. Fetriconi, A. Bartoli, R. Rossi, and P. Marconi. 2003. Involvement of mitogen-activated protein kinases in Group B Streptococcus-induced macrophage apoptosis. Pharmacol. Res. 47: 355-362.
42. Jaworowski, A., N. J. Wilson, E. Christy, R. Byrne, and J. A. Hamilton. 1999. Roles of the mitogen-activated protein kinase family in macrophage responses to colony stimulating factor-1 addition and withdrawal. J. Biol. Chem. 274: 15127-15133.
43. Cuesta, N., Q. M. Nhu, E. Zudaire, S. Polumuri, F. Cuttitta, and S. N. Vogel. 2007. IFN regulatory factor-2 regulates macrophage apoptosis through a STAT1/3- and caspase-1-dependent mechanism. J. Immunol. 178: 3602-3611.
44. Melcher, M., B. Unger, U. Schmidt, I. A. Rajantie, K. Alitalo, and W. Ellmeier. 2008. Essential roles for the Tec family kinases Tec and Btk in M-CSF receptor signaling pathways that regulate macrophage survival. J. Immunol. 180: 8048-8056.
45. Wang, Z., B. Liu, P. Wang, X. Dong, C. Fernandez-Hernando, Z. Li, T. Hla, Z. Li, K. Claffey, J. D. Smith, and D. Wu. 2008. Phospholipase C beta3 deficiency leads to macrophage hypersensitivity to apoptotic induction and reduction of atherosclerosis in mice. J. Clin. Invest. 118: 195-204.
46. Glantschnig, H., J. E. Fisher, G. Wesolowski, G. A. Rodan, and A. A. Reszka. 2003. M-CSF, TNFalpha and RANK ligand promote osteoclast survival by signaling through mTOR/S6 kinase. Cell Death Differ. 10: 1165-1177.
47. Lennartz, M. R. 1999. Phospholipases and phagocytosis: the role of phospholipid-derived second messengers in phagocytosis. Int. J. Biochem. Cell Biol. 31: 415-430.
48. Botelho, R. J., C. C. Scott, and S. Grinstein. 2004. Phosphoinositide involvement in phagocytosis and phagosome maturation. Curr. Top. Microbiol. Immunol. 282: 1-30.
49. Bocchino, M., D. Galati, A. Sanduzzi, V. Colizzi, E. Brunetti, and G. Mancino. 2005. Role of mycobacteria-induced monocyte/macrophage apoptosis in the pathogenesis of human tuberculosis. Int. J. Tuberc. Lung Dis. 9: 375-383.
50. Saunders, B. M., and W. J. Britton. 2007. Life and death in the granuloma: immunopathology of tuberculosis. Immunol. Cell Biol. 85: 103-111.