Negative control of mast cell degranulation and the anaphylactic response by the phosphatase lipin1

European Journal of Immunology

Volumn 43, Issue 1, 2013, Pages 240-248

  Shin, Jinwook ^a   Zhang, Ping ^a   Wang, Shang ^a   Wu, Jinhong ^a   Guan, Ziqiang ^a   Zhong, Xiao Ping ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Lipin1; Mast cells; Phosphatidic acid; PKC; SNAP 23

Indexed keywords

2,4 DINITROPHENOL; ALBUMIN ANTIBODY; BETA N ACETYLHEXOSAMINIDASE; FC EPSILON RECEPTOR I; FC RECEPTOR; INTERLEUKIN 6; LIPIN1; PHOSPHATIDATE PHOSPHATASE; PROSTAGLANDIN D2; PROTEIN KINASE C; SYNAPTOSOMAL ASSOCIATED PROTEIN 23; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANAPHYLAXIS; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL FUNCTION; CELL MEMBRANE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE EXACERBATION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME LINKED IMMUNOSORBENT ASSAY; IN VITRO STUDY; IN VIVO STUDY; MAST CELL; MAST CELL DEGRANULATION; MEDIATOR; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROSTAGLANDIN RELEASE; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; WILD TYPE;

ANAPHYLAXIS; ANIMALS; BETA-N-ACETYLHEXOSAMINIDASES; CELL DEGRANULATION; CELLS, CULTURED; IMMUNOSUPPRESSION; MAST CELLS; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; NUCLEAR PROTEINS; PHOSPHATIDATE PHOSPHATASE; PHOSPHORYLATION; PROSTAGLANDIN D2; PROTEIN KINASE C; QB-SNARE PROTEINS; QC-SNARE PROTEINS; RECEPTORS, IGE; SIGNAL TRANSDUCTION;

EID: 84872485396     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201242571     Document Type: Article

References (60)

1. Rivera, J. and Gilfillan, A. M., Molecular regulation of mast cell activation. J. Allergy. Clin. Immunol. 2006. 117: 1214-1225.
2. Metcalfe, D. D., Baram, D. and Mekori, Y. A., Mast cells. Physiol. Rev. 1997. 77: 1033-1079.
3. Galli, S. J., Nakae, S. and Tsai, M., Mast cells in the development of adaptive immune responses. Nat. Immunol. 2005. 6: 135-142.
4. Kambayashi, T. and Koretzky, G. A., Proximal signaling events in Fc epsilon RI-mediated mast cell activation. J. Allergy Clin. Immunol. 2007. 119: 544-552.
5. Kraft, S. and Kinet, J. P., New developments in FcεRI regulation, function and inhibition. Nat. Rev. Immunol. 2007. 7: 365-378.
6. Siraganian, R. P., Mast cell signal transduction from the high-affinity IgE receptor. Curr. Opin. Immunol. 2003. 15: 639-646.
7. Saitoh, S., Arudchandran, R., Manetz, T. S., Zhang, W., Sommers, C. L., Love, P. E., Rivera, J. et al., LAT is essential for FcεRI-mediated mast cell activation. Immunity 2000. 12: 525-535.
8. Pivniouk, V. I., Martin, T. R., Lu-Kuo, J. M., Katz, H. R., Oettgen, H. C. and Geha, R. S., SLP-76 deficiency impairs signaling via the high-affinity IgE receptor in mast cells. J. Clin. Invest. 1999. 103: 1737-1743.
9. Manetz, T. S., Gonzalez-Espinosa, C., Arudchandran, R., Xirasagar, S., Tybulewicz, V. and Rivera, J., Vav1 regulates phospholipase cγ activation and calcium responses in mast cells. Mol. Cell. Biol. 2001. 21: 3763-3774.
10. Hata, D., Kawakami, Y., Inagaki, N., Lantz, C. S., Kitamura, T., Khan, W. N., Maeda-Yamamoto, M. et al., Involvement of Bruton's tyrosine kinase in FcεRI-dependent mast cell degranulation and cytokine production. J. Exp. Med. 1998. 187: 1235-1247.
11. Fukao, T., Yamada, T., Tanabe, M., Terauchi, Y., Ota, T., Takayama, T., Asano, T. et al., Selective loss of gastrointestinal mast cells and impaired immunity in PI3K-deficient mice. Nat. Immunol. 2002. 3: 295-304.
12. Atkinson, T. P., Kaliner, M. A. and Hohman, R. J., Phospholipase C-γ 1 is translocated to the membrane of rat basophilic leukemia cells in response to aggregation of IgE receptors. J. Immunol. 1992. 148: 2194-2200.
13. Wen, R., Jou, S. T., Chen, Y., Hoffmeyer, A. and Wang, D., Phospholipase C γ2 is essential for specific functions of FcεR and FcγR. J. Immunol. 2002. 169: 6743-6752.
14. Chang, E. Y., Szallasi, Z., Acs, P., Raizada, V., Wolfe, P. C., Fewtrell, C., Blumberg, P. M. et al., Functional effects of overexpression of protein kinase C-α, -β, -δ, -ε, and -η in the mast cell line RBL-2H3. J. Immunol. 1997. 159: 2624-2632.
15. Zhang, C., Baumgartner, R. A., Yamada, K. and Beaven, M. A., Mitogen-activated protein (MAP) kinase regulates production of tumor necrosis factor-α and release of arachidonic acid in mast cells. Indications of communication between p38 and p42 MAP kinases. J. Biol. Chem. 1997. 272: 13397-13402.
16. Olenchock, B. A., Guo, R., Silverman, M. A., Wu, J. N., Carpenter, J. H., Koretzky, G. A. and Zhong, X. P., Impaired degranulation but enhanced cytokine production after FcεRI stimulation of diacylglycerol kinase ζ-deficient mast cells. J. Exp. Med. 2006. 203: 1471-1480.
17. Baumgartner, R. A., Yamada, K., Deramo, V. A. and Beaven, M. A., Secretion of TNF from a rat mast cell line is a brefeldin A-sensitive and a calcium/protein kinase C-regulated process. J. Immunol. 1994. 153: 2609-2617.
18. Hitomi, T., Zhang, J., Nicoletti, L. M., Grodzki, A. C., Jamur, M. C., Oliver, C. and Siraganian, R. P., Phospholipase D1 regulates high-affinity IgE receptor-induced mast cell degranulation. Blood 2004. 104: 4122-4128.
19. Peng, Z. and Beaven, M. A., An essential role for phospholipase D in the activation of protein kinase C and degranulation in mast cells. J. Immunol. 2005. 174: 5201-5208.
20. Peterfy, M., Phan, J., Xu, P. and Reue, K., Lipodystrophy in the fld mouse results from mutation of a new gene encoding a nuclear protein, lipin. Nat. Genet 2001. 27: 121-124.
21. Langner, C. A., Birkenmeier, E. H., Ben-Zeev, O., Schotz, M. C., Sweet, H. O., Davisson, M. T. and Gordon, J. I., The fatty liver dystrophy (fld) mutation. A new mutant mouse with a developmental abnormality in triglyceride metabolism and associated tissue-specific defects in lipoprotein lipase and hepatic lipase activities. J. Biol. Chem. 1989. 264: 7994-8003.
22. Langner, C. A., Birkenmeier, E. H., Roth, K. A., Bronson, R. T. and Gordon, J. I., Characterization of the peripheral neuropathy in neonatal and adult mice that are homozygous for the fatty liver dystrophy (fld) mutation. J. Biol. Chem. 1991. 266: 11955-11964.
23. Csaki, L. S. and Reue, K., Lipins: multifunctional lipid metabolism proteins. Annu. Rev. Nutr. 2010. 30: 257-272.
24. Carman, G. M. and Han, G. S., Roles of phosphatidate phosphatase enzymes in lipid metabolism. Trends Biochem. Sci. 2006. 31: 694-699.
25. Jamal, Z., Martin, A., Gomez-Munoz, A. and Brindley, D. N., Plasma membrane fractions from rat liver contain a phosphatidate phosphohydrolase distinct from that in the endoplasmic reticulum and cytosol. J. Biol. Chem. 1991. 266: 2988-2996.
26. Donkor, J., Sariahmetoglu, M., Dewald, J., Brindley, D. N. and Reue, K., Three mammalian lipins act as phosphatidate phosphatases with distinct tissue expression patterns. J. Biol. Chem. 2007. 282: 3450-3457.
27. Grimsey, N., Han, G. S., O'Hara, L., Rochford, J. J., Carman, G. M. and Siniossoglou, S., Temporal and spatial regulation of the phosphatidate phosphatases lipin 1 and 2. J. Biol. Chem. 2008. 283: 29166-29174.
28. Peterson, T. R., Sengupta, S. S., Harris, T. E., Carmack, A. E., Kang, S. A., Balderas, E., Guertin, D. A. et al., mTOR complex 1 regulates lipin 1 localization to control the SREBP pathway. Cell 2011. 146: 408-420.
29. Valdearcos, M., Esquinas, E., Meana, C., Gil-de-Gomez, L., Guijas, C., Balsinde, J. and Balboa, M. A., Subcellular localization and role of lipin-1 in human macrophages. J. Immunol. 2011. 186: 6004-6013.
30. Liu, G. H. and Gerace, L., Sumoylation regulates nuclear localization of lipin-1α in neuronal cells. PLoS One 2009. 4: e7031.
31. Nishida, K., Yamasaki, S., Ito, Y., Kabu, K., Hattori, K., Tezuka, T., Nishizumi, H. et al., FcεRI-mediated mast cell degranulation requires calcium-independent microtubule-dependent translocation of granules to the plasma membrane. J. Cell. Biol. 2005. 170: 115-126.
32. Hepp, R., Puri, N., Hohenstein, A. C., Crawford, G. L., Whiteheart, S. W. and Roche, P. A., Phosphorylation of SNAP-23 regulates exocytosis from mast cells. J. Biol. Chem. 2005. 280: 6610-6620.
33. Brindley, D. N., Pilquil, C., Sariahmetoglu, M. and Reue, K., Phosphatidate degradation: phosphatidate phosphatases (lipins) and lipid phosphate phosphatases. Biochim. Biophys. Acta 2009. 1791: 956-961.
34. Gorentla, B. K., Wan, C. K. and Zhong, X. P., Negative regulation of mTOR activation by diacylglycerol kinases through inhibition of the diacylglycerol-RasGRP1-Ras-Mek1/2-Erk1/2 pathway. Blood 2011. 117: 4022-4031.
35. Zhong, X. P., Guo, R., Zhou, H., Liu, C. and Wan, C. K., Diacylglycerol kinases in immune cell function and self-tolerance. Immunol. Rev. 2008. 224: 249-264.
36. Fu, G., Chen, Y., Yu, M., Podd, A., Schuman, J., He, Y., Di, L. et al., Phospholipase Cγ1 is essential for T-cell development, activation, and tolerance. J. Exp. Med. 2010. 207: 309-318.
37. Hikida, M., Casola, S., Takahashi, N., Kaji, T., Takemori, T., Rajewsky, K. and Kurosaki, T., PLC-γ2 is essential for formation and maintenance of memory B cells. J. Exp. Med. 2009. 206: 681-689.
38. Zhong, X. P., Hainey, E. A., Olenchock, B. A., Jordan, M. S., Maltzman, J. S., Nichols, K. E., Shen, H. et al., Enhanced T-cell responses due to diacylglycerol kinase ζ deficiency. Nat. Immunol. 2003. 4: 882-890.
39. Guo, R., Wan, C. K., Carpenter, J. H., Mousallem, T., Boustany, R. M., Kuan, C. T., Burks, A. W. et al., Synergistic control of T-cell development and tumor suppression by diacylglycerol kinase α and ζ Proc. Natl. Acad. Sci. USA 2008. 105: 11909-11914.
40. Olenchock, B. A., Guo, R., Carpenter, J. H., Jordan, M., Topham, M. K., Koretzky, G. A. and Zhong, X. P., Disruption of diacylglycerol metabolism impairs the induction of T-cell anergy. Nat. Immunol. 2006. 7: 1174-1181.
41. Liu, C. H., Machado, F. S., Guo, R., Nichols, K. E., Burks, A. W., Aliberti, J. C. and Zhong, X. P., Diacylglycerol kinase ζ regulates microbial recognition and host resistance to Toxoplasma gondii. J. Exp. Med. 2007. 204: 781-792.
42. Frank, C., Keilhack, H., Opitz, F., Zschornig, O. and Bohmer, F. D., Binding of phosphatidic acid to the protein-tyrosine phosphatase SHP-1 as a basis for activity modulation. Biochemistry 1999. 38: 11993-12002.
43. Zhao, C., Du, G., Skowronek, K., Frohman, M. A. and Bar-Sagi, D., Phospholipase D2-generated phosphatidic acid couples EGFR stimulation to Ras activation by Sos. Nat. Cell. Biol. 2007. 9: 706-712.
44. Jarquin-Pardo, M., Fitzpatrick, A., Galiano, F. J., First, E. A. and Davis, J. N., Phosphatidic acid regulates the affinity of the murine phosphatidylinositol 4-phosphate 5-kinase-Iβ for phosphatidylinositol-4-phosphate. J. Cell. Biochem. 2007. 100: 112-128.
45. Fang, Y., Vilella-Bach, M., Bachmann, R., Flanigan, A. and Chen, J., Phosphatidic acid-mediated mitogenic activation of mTOR signaling. Science 2001. 294: 1942-1945.
46. Kim, H. B., Kumar, A., Wang, L., Liu, G. H., Keller, S. R., Lawrence, J. C., Jr., Finck, B. N. et al., Lipin 1 represses NFATc4 transcriptional activity in adipocytes to inhibit secretion of inflammatory factors. Mol. Cell. Biol. 2010. 30: 3126-3139.
47. Finck, B. N., Gropler, M. C., Chen, Z., Leone, T. C., Croce, M. A., Harris, T. E., Lawrence, J. C., Jr. and Kelly, D. P., Lipin 1 is an inducible amplifier of the hepatic PGC-1α/PPARα regulatory pathway. Cell. Metabol. 2006. 4: 199-210.
48. Blank, U. and Rivera, J., The ins and outs of IgE-dependent mast-cell exocytosis. Trends Immunol. 2004. 25: 266-273.
49. Vicogne, J., Vollenweider, D., Smith, J. R., Huang, P., Frohman, M. A. and Pessin, J. E., Asymmetric phospholipid distribution drives in vitro reconstituted SNARE-dependent membrane fusion. Proc. Natl. Acad. Sci. USA 2006. 103: 14761-14766.
50. Suzuki, K. and Verma, I. M., Phosphorylation of SNAP-23 by IκB kinase 2 regulates mast cell degranulation. Cell 2008. 134: 485-495.
51. Polgar, J., Lane, W. S., Chung, S. H., Houng, A. K. and Reed, G. L., Phosphorylation of SNAP-23 in activated human platelets. J. Biol. Chem. 2003. 278: 44369-44376.
52. Klemm, S., Gutermuth, J., Hultner, L., Sparwasser, T., Behrendt, H., Peschel, C., Mak, T. W. et al., The Bcl10-Malt1 complex segregates FcεRI-mediated nuclear factor κB activation and cytokine production from mast cell degranulation. J. Exp. Med. 2006. 203: 337-347.
53. Nishida, K., Hasegawa, A., Nakae, S., Oboki, K., Saito, H., Yamasaki, S. and Hirano, T., Zinc transporter Znt5/Slc30a5 is required for the mast cell-mediated delayed-type allergic reaction but not the immediate-type reaction. J. Exp. Med. 2009. 206: 1351-1364.
54. Shin, J., Pan, H. and Zhong, X. P., Regulation of mast cell survival and function by tuberous sclerosis complex 1. Blood 2012. 119: 3306-3314.
55. Zeharia, A., Shaag, A., Houtkooper, R. H., Hindi, T., de Lonlay, P., Erez, G., Hubert, L. et al., Mutations in LPIN1 cause recurrent acute myoglobinuria in childhood. Am. J. Hum. Genet. 2008. 83: 489-494.
56. El-Shanti, H. I. and Ferguson, P. J., Chronic recurrent multifocal osteomyelitis: a concise review and genetic update. Clin. Orthop. Relat. Res. 2007. 462: 11-19.
57. Majeed, H. A., Al-Tarawna, M., El-Shanti, H., Kamel, B. and Al-Khalaileh, F., The syndrome of chronic recurrent multifocal osteomyelitis and congenital dyserythropoietic anaemia. Report of a new family and a review. Eur. J. Pediatr. 2001. 160: 705-710.
58. Ferguson, P. J., Chen, S., Tayeh, M. K., Ochoa, L., Leal, S. M., Pelet, A., Munnich, A. et al., Homozygous mutations in LPIN2 are responsible for the syndrome of chronic recurrent multifocal osteomyelitis and congenital dyserythropoietic anaemia (Majeed syndrome). J. Med. Genet. 2005. 42: 551-557.
59. Reue, K., The lipin family: mutations and metabolism. Curr. Opin. Lipidol. 2009. 20: 165-170.
60. Liu, Y., Zhu, M., Nishida, K., Hirano, T. and Zhang, W., An essential role for RasGRP1 in mast cell function and IgE-mediated allergic response. J. Exp. Med. 2007. 204: 93-103.