Apoptotic cells suppress mast cell inflammatory responses via the CD300a immunoreceptor

Journal of Experimental Medicine

Volumn 209, Issue 8, 2012, Pages 1493-1503

  Nakahashi Oda, Chigusa ^a   Tahara Hanaoka, Satoko ^a   Shoji, Masamichi ^a   Okoshi, Yasushi ^a   Nakano Yokomizo, Takako ^a   Ohkohchi, Nobuhiro ^a   Yasui, Teruhito ^b   Kikutani, Hitoshi ^b   Honda, Shin ichiro ^a   Shibuya, Kazuko ^a   Nagata, Shigekazu ^c   Shibuya, Akira ^a  

^a UNIVERSITY OF TSUKUBA   (Japan)

^b OSAKA UNIVERSITY   (Japan)

^c KYOTO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CD300A IMMUNORECEPTOR; MEMBRANE RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; BACTERIAL CLEARANCE; BONE MARROW CELL; CECAL LIGATION AND PUNCTURE; CONTROLLED STUDY; CYTOKINE PRODUCTION; HUMAN; IN VITRO STUDY; IN VIVO STUDY; LIGATION; MACROPHAGE; MAST CELL; MOUSE; NONHUMAN; PERITONEAL CAVITY; PHAGOCYTE; PHAGOCYTOSIS; PRIORITY JOURNAL; PUNCTURE; RAT; WILD TYPE;

ANIMALS; APOPTOSIS; CHEMOKINES; CYTOKINES; HUMANS; INFLAMMATION; MACROPHAGES; MAST CELLS; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; NEUTROPHIL INFILTRATION; NEUTROPHILS; NIH 3T3 CELLS; PHAGOCYTOSIS; PHOSPHATIDYLSERINES; RECEPTORS, IMMUNOLOGIC;

EID: 84866455143     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20120096     Document Type: Article

References (71)

1. Abraham, S.N., and A.L. St John. 2010. Mast cell-orchestrated immunity to pathogens. Nat. Rev. Immunol. 10:440-452. http://dx.doi.org/10.1038/nri2782
2. Alvarez, Y., X. Tang, J.E. Coligan, and F. Borrego. 2008. The CD300a (IRp60) inhibitory receptor is rapidly up-regulated on human neutrophils in response to inflammatory stimuli and modulates CD32a (FcgammaRIIa) mediated signaling. Mol. Immunol. 45:253-258. http://dx.doi.org/10.1016/j.molimm.2007.05.006
3. An, H., W. Zhao, J. Hou, Y. Zhang, Y. Xie, Y. Zheng, H. Xu, C. Qian, J. Zhou, Y. Yu, et al. 2006. SHP-2 phosphatase negatively regulates the TRIF adaptor protein-dependent type I interferon and proinflammatory cytokine production. Immunity. 25:919-928. http://dx.doi.org/10.1016/j.immuni.2006.10.014
4. Angus, D.C., and R.S. Wax. 2001. Epidemiology of sepsis: an update. Crit. Care Med. 29:S109-S116. http://dx.doi.org/10.1097/00003246-200107001-00035
5. Baumhofer, J.M., B.G. Beinhauer, J.E. Wang, H. Brandmeier, K. Geissler, U. Losert, R. Philip, G. Aversa, and M.A. Rogy. 1998. Gene transfer with IL-4 and IL-13 improves survival in lethal endotoxemia in the mouse and ameliorates peritoneal macrophages immune competence. Eur. J. Immunol. 28:610-615. http://dx.doi.org/10.1002/(SICI)1521-4141(199802)28:02610::AID-IMMU6103.0.CO;2-5
6. Bischoff, S.C. 2007. Role of mast cells in allergic and non-allergic immune responses: comparison of human and murine data. Nat. Rev. Immunol. 7:93-104. http://dx.doi.org/10.1038/nri2018
7. Can, I., S. Tahara-Hanaoka, K. Hitomi, T. Nakano, C. Nakahashi-Oda, N. Kurita, S. Honda, K. Shibuya, and A. Shibuya. 2008. Caspase-independent cell death by CD300LF (MAIR-V), an inhibitory immunoglobulin-like receptor on myeloid cells. J. Immunol. 180:207-213.
8. Cantoni, C., C. Bottino, R. Augugliaro, L. Morelli, E. Marcenaro, R. Castriconi, M. Vitale, D. Pende, S. Sivori, R. Millo, et al. 1999. Molecular and functional characterization of IRp60, a member of the immunoglobulin superfamily that functions as an inhibitory receptor in human NK cells. Eur. J. Immunol. 29:3148-3159. http://dx.doi.org/10.1002/(SICI)1521-4141(199910)29:103148::AID-IMMU31483.0.CO;2-L
9. Choi, S.C., V.R. Simhadri, L. Tian, A. Gil-Krzewska, K. Krzewski, F. Borrego, and J.E. Coligan. 2011. Cutting edge: mouse CD300f (CMRF- 35-like molecule-1) recognizes outer membrane-exposed phosphatidylserine and can promote phagocytosis. J. Immunol. 187:3483-3487. http://dx.doi.org/10.4049/jimmunol.1101549
10. Chung, D.H., M.B. Humphrey, M.C. Nakamura, D.G. Ginzinger, W.E. Seaman, and M.R. Daws. 2003. CMRF-35-like molecule-1, a novel mouse myeloid receptor, can inhibit osteoclast formation. J. Immunol. 171:6541-6548.
11. Clark, G.J., B.J. Green, and D.N. Hart. 2000. The CMRF-35H gene structure predicts for an independently expressed member of an ITIM/ITAM pair of molecules localized to human chromosome 17. Tissue Antigens. 55:101-109. http://dx.doi.org/10.1034/j.1399-0039.2000.550201.x
12. Clark, G.J., B. Cooper, S. Fitzpatrick, B.J. Green, and D.N. Hart. 2001. The gene encoding the immunoregulatory signaling molecule CMRF-35A localized to human chromosome 17 in close proximity to other members of the CMRF-35 family. Tissue Antigens. 57:415-423. http://dx.doi.org/10.1034/j.1399-0039.2001.057005415.x
13. Cohen, J. 2002. The immunopathogenesis of sepsis. Nature. 420:885-891. http://dx.doi.org/10.1038/nature01326
14. Daëron, M., S. Jaeger, L. Du Pasquier, and E. Vivier. 2008. Immunoreceptor tyrosine-based inhibition motifs: a quest in the past and future. Immunol. Rev. 224:11-43. http://dx.doi.org/10.1111/j.1600-065X.2008.00666.x
15. Dudeck, A., J. Dudeck, J. Scholten, A. Petzold, S. Surianarayanan, A. Köhler, K. Peschke, D. Vöhringer, C. Waskow, T. Krieg, et al. 2011. Mast cells are key promoters of contact allergy that mediate the adjuvant effects of haptens. Immunity. 34:973-984. http://dx.doi.org/10.1016/j.immuni.2011.03.028
16. Echtenacher, B., D.N. Männel, and L. Hültner. 1996. Critical protective role of mast cells in a model of acute septic peritonitis. Nature. 381:75-77. http://dx.doi.org/10.1038/381075a0
17. Enomoto, Y., Y. Yamanishi, K. Izawa, A. Kaitani, M. Takahashi, A. Maehara, T. Oki, R. Takamatsu, M. Kajikawa, T. Takai, et al. 2010. Characterization of leukocyte mono-immunoglobulin-like receptor 7 (LMIR7)/CLM-3 as an activating receptor: its similarities to and differences from LMIR4/CLM-5. J. Biol. Chem. 285:35274-35283. http://dx.doi.org/10.1074/jbc.M110.137166
18. Fadok V.A., D.R. Voelker, P.A. Campbell, J.J. Cohen, D.L. Bratton, and P.M. Henson. 1992. Exposure of phosphatidylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal by macrophages. J. Immunol. 148:2207-2216.
19. Fadok, V.A., D.L. Bratton, A. Konowal, P.W. Freed, J.Y. Westcott, and P.M. Henson. 1998. 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. 101:890-898. http://dx.doi.org/10.1172/JCI1112
20. Fujimoto, M., H. Takatsu, and H. Ohno. 2006. CMRF-35-like molecule- 5 constitutes novel paired receptors, with CMRF-35-like molecule-1, to transduce activation signal upon association with FcRgamma. Int. Immunol. 18:1499-1508. http://dx.doi.org/10.1093/intimm/dxl083
21. Gilfillan, A.M., and C. Tkaczyk. 2006. Integrated signalling pathways for mast-cell activation. Nat. Rev. Immunol. 6:218-230. http://dx.doi.org/10.1038/nri1782
22. Grimbaldeston, M.A., C.C. Chen, A.M. Piliponsky, M. Tsai, S.Y. Tam, and S.J. Galli. 2005. Mast cell-deficient W-sash c-kit mutant Kit W-sh/W-sh mice as a model for investigating mast cell biology in vivo. Am. J. Pathol. 167:835-848. http://dx.doi.org/10.1016/S0002-9440(10)62055-X
23. Hanayama, R., M. Tanaka, K. Miwa, A. Shinohara, A. Iwamatsu, and S. Nagata. 2002. Identification of a factor that links apoptotic cells to phagocytes. Nature. 417:182-187. http://dx.doi.org/10.1038/417182a
24. Hanayama, R., M. Tanaka, K. Miyasaka, K. Aozasa, M. Koike, Y. Uchiyama, and S. Nagata. 2004. Autoimmune disease and impaired uptake of apoptotic cells in MFG-E8-deficient mice. Science. 304:1147-1150. http://dx.doi.org/10.1126/science.1094359
25. Harris, E.N., S.V. Kyosseva, J.A. Weigel, and P.H. Weigel. 2007. Expression, processing, and glycosaminoglycan binding activity of the recombinant human 315-kDa hyaluronic acid receptor for endocytosis (HARE). J. Biol. Chem. 282:2785-2797. http://dx.doi.org/10.1074/jbc.M607787200
26. Hotchkiss, R.S., and D.W. Nicholson. 2006. Apoptosis and caspases regulate death and inflammation in sepsis. Nat. Rev. Immunol. 6:813-822. http://dx.doi.org/10.1038/nri1943
27. Izawa, K., J. Kitaura, Y. Yamanishi, T. Matsuoka, T. Oki, F. Shibata, H. Kumagai, H. Nakajima, M. Maeda-Yamamoto, J.P. Hauchins, et al. 2007. Functional analysis of activating receptor LMIR4 as a counterpart of inhibitory receptor LMIR3. J. Biol. Chem. 282:17997-18008. http://dx.doi.org/10.1074/jbc.M701100200
28. Izawa, K., J. Kitaura, Y. Yamanishi, T. Matsuoka, A. Kaitani, M. Sugiuchi, M. Takahashi, A. Maehara, Y. Enomoto, T. Oki, et al. 2009. An activating and inhibitory signal from an inhibitory receptor LMIR3/ CLM-1: LMIR3 augments lipopolysaccharide response through association with FcRgamma in mast cells. J. Immunol. 183:925-936. http://dx.doi.org/10.4049/jimmunol.0900552
29. Ju, X., M. Zenke, D.N. Hart, and G.J. Clark. 2008. CD300a/c regulate type I interferon and TNF-alpha secretion by human plasmacytoid dendritic cells stimulated with TLR7 and TLR9 ligands. Blood. 112:1184-1194. http://dx.doi.org/10.1182/blood-2007-12-127951
30. Karra, L., B. Berent-Maoz, M. Ben-Zimra, and F. Levi-Schaffer. 2009. Are we ready to downregulate mast cells? Curr. Opin. Immunol. 21:708-714. http://dx.doi.org/10.1016/j.coi.2009.09.010
31. Kobayashi, N., P. Karisola, V. Peña-Cruz, D.M. Dorfman, M. Jinushi, S.E. Umetsu, M.J. Butte, H. Nagumo, I. Chernova, B. Zhu, et al. 2007. TIM-1 and TIM-4 glycoproteins bind phosphatidylserine and mediate uptake of apoptotic cells. Immunity. 27:927-940. http://dx.doi.org/10.1016/j.immuni.2007.11.011
32. Kuchroo, V.K., V. Dardalhon, S. Xiao, and A.C. Anderson. 2008. New roles for TIM family members in immune regulation. Nat. Rev. Immunol. 8:577-580. http://dx.doi.org/10.1038/nri2366
33. Kumagai, H., T. Oki, K. Tamitsu, S.Z. Feng, M. Ono, H. Nakajima, Y.C. Bao, Y. Kawakami, K. Nagayoshi, N.G. Copeland, et al. 2003. Identification and characterization of a new pair of immunoglobulin- like receptors LMIR1 and 2 derived from murine bone marrow-derived mast cells. Biochem. Biophys. Res. Commun. 307:719-729. http://dx.doi.org/10.1016/S0006-291X(03)01245-2
34. Lanier, L.L. 2001. Face off-the interplay between activating and inhibitory immune receptors. Curr. Opin. Immunol. 13:326-331. http://dx.doi.org/10.1016/S0952-7915(00)00222-3
35. Lankry, D., H. Simic, Y. Klieger, F. Levi-Schaffer, S. Jonjic, and O. Mandelboim. 2010. Expression and function of CD300 in NK cells. J. Immunol. 185:2877-2886. http://dx.doi.org/10.4049/jimmunol.0903347
36. Luo, K., W. Zhang, L. Sui, N. Li, M. Zhang, X. Ma, L. Zhang, and X. Cao. 2001. DIgR1, a novel membrane receptor of the immunoglobulin gene superfamily, is preferentially expressed by antigen-presenting cells. Biochem. Biophys. Res. Commun. 287:35-41. http://dx.doi.org/10.1006/bbrc.2001.5539
37. Malaviya, R., T. Ikeda, E. Ross, and S.N. Abraham. 1996. Mast cell modulation of neutrophil influx and bacterial clearance at sites of infection through TNF-alpha. Nature. 381:77-80. http://dx.doi.org/10.1038/381077a0
38. Malbec, O., D.C. Fong, M. Turner, V.L. Tybulewicz, J.C. Cambier, W.H. Fridman, and M. Daëron. 1998. Fc epsilon receptor I-associated lyndependent phosphorylation of Fc gamma receptor IIB during negative regulation of mast cell activation. J. Immunol. 160:1647-1658.
39. Marshall, J.S. 2004. Mast-cell responses to pathogens. Nat. Rev. Immunol. 4:787-799. http://dx.doi.org/10.1038/nri1460
40. Matsukawa, A., C.M. Hogaboam, N.W. Lukacs, P.M. Lincoln, R.M. Strieter, and S.L. Kunkel. 1999. Endogenous monocyte chemoattractant protein-1 (MCP-1) protects mice in a model of acute septic peritonitis: cross-talk between MCP-1 and leukotriene B4. J. Immunol. 163:6148-6154.
41. Miksa, M., H. Komura, R. Wu, K.G. Shah, and P. Wang. 2009. A novel method to determine the engulfment of apoptotic cells by macro-phages using pHrodo succinimidyl ester. J. Immunol. Methods. 342:71-77. http://dx.doi.org/10.1016/j.jim.2008.11.019
42. Miyanishi, M., K. Tada, M. Koike, Y. Uchiyama, T. Kitamura, and S. Nagata. 2007. Identification of Tim4 as a phosphatidylserine receptor. Nature. 450:435-439. http://dx.doi.org/10.1038/nature06307
43. Mori, K., Y. Kanemura, H. Fujikawa, A. Nakano, H. Ikemoto, I. Ozaki, T. Matsumoto, K. Tamura, M. Yokota, and N. Arita. 2002. Brain-specific angiogenesis inhibitor 1 (BAI1) is expressed in human cerebral neuronal cells. Neurosci. Res. 43:69-74. http://dx.doi.org/10.1016/S0168-0102(02)00018-4
44. Munitz, A., I. Bachelet, and F. Levi-Schaffer. 2006. Reversal of airway inflammation and remodeling in asthma by a bispecific antibody fragment linking CCR3 to CD300a. J. Allergy Clin. Immunol. 118:1082-1089. http://dx.doi.org/10.1016/j.jaci.2006.07.041
45. Nagata, S. 2005. DNA degradation in development and programmed cell death. Annu. Rev. Immunol. 23:853-875. http://dx.doi.org/10.1146/annurev.immunol.23.021704.115811
46. Nagata, S., R. Hanayama, and K. Kawane. 2010. Autoimmunity and the clearance of dead cells. Cell. 140:619-630. http://dx.doi.org/10.1016/j.cell.2010.02.014
47. Nakahashi, C., S. Tahara-Hanaoka, N. Totsuka, Y. Okoshi, T. Takai, N. Ohkohchi, S. Honda, K. Shibuya, and A. Shibuya. 2007. Dual assemblies of an activating immune receptor, MAIR-II, with ITAM-bearing adapters DAP12 and FcRgamma chain on peritoneal macrophages. J. Immunol. 178:765-770. url
48. Nakahashi-Oda, C., S. Tahara-Hanaoka, S.I. Honda, K. Shibuya, and A. Shibuya. 2012. Identification of phosphatidylserine as a ligand for the CD300a immunoreceptor. Biochem. Biophys. Res. Commun. 417:646-650. http://dx.doi.org/10.1016/j.bbrc.2011.12.025
49. Nakano, N., C. Nishiyama, S. Kanada, Y. Niwa, N. Shimokawa, H. Ushio, M. Nishiyama, K. Okumura, and H. Ogawa. 2007. Involvement of mast cells in IL-12/23 p40 production is essential for survival from polymicrobial infections. Blood. 109:4846-4855. http://dx.doi.org/10.1182/blood-2006-09-045641
50. Nakano, T., Y. Ishimoto, J. Kishino, M. Umeda, K. Inoue, K. Nagata, K. Ohashi, K. Mizuno, and H. Arita. 1997. Cell adhesion to phosphatidylserine mediated by a product of growth arrest-specific gene 6. J. Biol. Chem. 272:29411-29414. http://dx.doi.org/10.1074/jbc.272.47.29411
51. Nakano, T., S. Tahara-Hanaoka, C. Nakahashi, I. Can, N. Totsuka, S. Honda, K. Shibuya, and A. Shibuya. 2008. Activation of neutrophils by a novel triggering immunoglobulin-like receptor MAIR-IV. Mol. Immunol. 45:289-294. http://dx.doi.org/10.1016/j.molimm.2007.04.011
52. Nakano-Yokomizo, T., S. Tahara-Hanaoka, C. Nakahashi-Oda, T. Nabekura, N.K. Tchao, M. Kadosaki, N. Totsuka, N. Kurita, K. Nakamagoe, A. Tamaoka, et al. 2011. The immunoreceptor adapter protein DAP12 suppresses B lymphocyte-driven adaptive immune responses. J. Exp. Med. 208:1661-1671. http://dx.doi.org/10.1084/jem.20101623
53. Okoshi, Y., S. Tahara-Hanaoka, C. Nakahashi, S. Honda, A. Miyamoto, H. Kojima, T. Nagasawa, K. Shibuya, and A. Shibuya. 2005. Requirement of the tyrosines at residues 258 and 270 of MAIR-I in inhibitory effect on degranulation from basophilic leukemia RBL-2H3. Int. Immunol. 17:65-72. http://dx.doi.org/10.1093/intimm/dxh187
54. Park, D., A.C. Tosello-Trampont, M.R. Elliott, M. Lu, L.B. Haney, Z. Ma, A.L. Klibanov, J.W. Mandell, and K.S. Ravichandran. 2007. BAI1 is an engulfment receptor for apoptotic cells upstream of the ELMO/Dock180/Rac module. Nature. 450:430-434. http://dx.doi.org/10.1038/nature06329
55. Park, S.Y., M.Y. Jung, H.J. Kim, S.J. Lee, S.Y. Kim, B.H. Lee, T.H. Kwon, R.W. Park, and I.S. Kim. 2008. Rapid cell corpse clearance by stabilin- 2, a membrane phosphatidylserine receptor. Cell Death Differ. 15:192-201. http://dx.doi.org/10.1038/sj.cdd.4402242
56. Plitas, G., B.M. Burt, H.M. Nguyen, Z.M. Bamboat, and R.P. DeMatteo. 2008. Toll-like receptor 9 inhibition reduces mortality in polymicrobial sepsis. J. Exp. Med. 205:1277-1283. http://dx.doi.org/10.1084/jem.20080162
57. Ravetch, J.V., and L.L. Lanier. 2000. Immune inhibitory receptors. Science. 290:84-89. http://dx.doi.org/10.1126/science.290.5489.84
58. Ravichandran, K.S., and U. Lorenz. 2007. Engulfment of apoptotic cells: signals for a good meal. Nat. Rev. Immunol. 7:964-974. http://dx.doi.org/10.1038/nri2214
59. Riedemann, N.C., R.F. Guo, and P.A. Ward. 2003. Novel strategies for the treatment of sepsis. Nat. Med. 9:517-524. http://dx.doi.org/10.1038/nm0503-517
60. Russell, J.A. 2006. Management of sepsis. N. Engl. J. Med. 355:1699-1713. http://dx.doi.org/10.1056/NEJMra043632
61. Savill, J., I. Dransfield, C. Gregory, and C. Haslett. 2002. A blast from the past: clearance of apoptotic cells regulates immune responses. Nat. Rev. Immunol. 2:965-975. http://dx.doi.org/10.1038/nri957
62. Scott, R.S., E.J. McMahon, S.M. Pop, E.A. Reap, R. Caricchio, P.L. Cohen, H.S. Earp, and G.K. Matsushima. 2001. Phagocytosis and clearance of apoptotic cells is mediated by MER. Nature. 411:207-211. http://dx.doi.org/10.1038/35075603
63. Shi, L., K. Luo, D. Xia, T. Chen, G. Chen, Y. Jiang, N. Li, and X. Cao. 2006. DIgR2, dendritic cell-derived immunoglobulin receptor 2, is one representative of a family of IgSF inhibitory receptors and mediates negative regulation of dendritic cell-initiated antigen-specific T-cell responses. Blood. 108:2678-2686. http://dx.doi.org/10.1182/blood-2006-04-015404
64. Smith, K.G., D.M. Tarlinton, G.M. Doody, M.L. Hibbs, and D.T. Fearon. 1998. Inhibition of the B cell by CD22: a requirement for Lyn. J. Exp. Med. 187:807-811. http://dx.doi.org/10.1084/jem.187.5.807
65. Tahara-Hanaoka, S., K. Shibuya, Y. Onoda, H. Zhang, S. Yamazaki, A. Miyamoto, S. Honda, L.L. Lanier, and A. Shibuya. 2004. Functional characterization of DNAM-1 (CD226) interaction with its ligands PVR (CD155) and nectin-2 (PRR-2/CD112). Int. Immunol. 16:533-538. http://dx.doi.org/10.1093/intimm/dxh059
66. Van Rooijen, N. 1989. The liposome-mediated macrophage 'suicide' technique. J. Immunol. Methods. 124:1-6. http://dx.doi.org/10.1016/0022-1759(89)90178-6
67. Xi, H., K.J. Katschke Jr., K.Y. Helmy, P.A. Wark, N. Kljavin, H. Clark, J. Eastham-Anderson, T. Shek, M. Roose-Girma, N. Ghilardi, and M. van Lookeren Campagne. 2010. Negative regulation of autoimmune demyelination by the inhibitory receptor CLM-1. J. Exp. Med. 207:7-16. http://dx.doi.org/10.1084/jem.20091508
68. Yamanishi, Y., J. Kitaura, K. Izawa, A. Kaitani, Y. Komeno, M. Nakamura, S. Yamazaki, Y. Enomoto, T. Oki, H. Akiba, et al. 2010. TIM1 is an endogenous ligand for LMIR5/CD300b: LMIR5 deficiency ameliorates mouse kidney ischemia/reperfusion injury. J. Exp. Med. 207: 1501-1511. http://dx.doi.org/10.1084/jem.20090581
69. Yang, Y., and B. Seed. 2003. Site-specific gene targeting in mouse embryonic stem cells with intact bacterial artificial chromosomes. Nat. Biotechnol. 21:447-451. http://dx.doi.org/10.1038/nbt803
70. Yotsumoto, K., Y. Okoshi, K. Shibuya, S. Yamazaki, S. Tahara-Hanaoka, S. Honda, M. Osawa, A. Kuroiwa, Y. Matsuda, D.G. Tenen, et al. 2003. Paired activating and inhibitory immunoglobulin-like receptors, MAIR-I and MAIR-II, regulate mast cell and macrophage activation. J. Exp. Med. 198:223-233. http://dx.doi.org/10.1084/jem.20021825
71. Zhou, Z. 2007. New phosphatidylserine receptors: clearance of apoptotic cells and more. Dev. Cell. 13:759-760. http://dx.doi.org/10.1016/j.devcel.2007.11.009