Fragile TIM-4-expressing tissue resident macrophages are migratory and immunoregulatory

Journal of Clinical Investigation

Volumn 124, Issue 8, 2014, Pages 3443-3454

  Thornley, Thomas B ^a   Fang, Zemin ^a,b   Balasubramanian, Savithri ^a   Larocca, Rafael A ^a   Gong, Weihua ^a   Gupta, Shipra ^a   Csizmadia, Eva ^a   Degauque, Nicolas ^a,c   Kim, Beom Seok ^a,d   Koulmanda, Maria ^a   Kuchroo, Vijay K ^e   Strom, Terry B ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^c Inst Natl de la Recherche   (France)

^d Yonsei University College of Medicine   (South Korea)

^e MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHATIDYLSERINE; PROTEIN TIM 4; RECEPTOR PROTEIN; SIALOADHESIN; UNCLASSIFIED DRUG; MEMBRANE PROTEIN; SIGLEC1 PROTEIN, MOUSE; TIM-4 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CELL MIGRATION; CONTROLLED STUDY; GRAFT SURVIVAL; HEART TRANSPLANTATION; IMMUNE RESPONSE; IMMUNOREGULATION; IMMUNOSTIMULATION; LYMPH NODE; LYMPHOCYTIC INFILTRATION; LYMPHOID ORGAN; MACROPHAGE; MALE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; ALLOGRAFT; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; CELL DIFFERENTIATION; CELL MOTION; CELL PROLIFERATION; CYTOLOGY; DEFICIENCY; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; METABOLISM; MIXED LYMPHOCYTE CULTURE; PHYSIOLOGY; TRANSGENIC MOUSE; TRANSPLANTATION TOLERANCE;

ALLOGRAFTS; ANIMALS; APOPTOSIS; CELL DIFFERENTIATION; CELL MOVEMENT; CELL PROLIFERATION; GRAFT SURVIVAL; HEART TRANSPLANTATION; LYMPHOCYTE CULTURE TEST, MIXED; MACROPHAGES; MALE; MEMBRANE PROTEINS; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; OXIDATIVE STRESS; SIALIC ACID BINDING IG-LIKE LECTIN 1; T-LYMPHOCYTES, REGULATORY; TRANSPLANTATION TOLERANCE;

EID: 84905457502     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI73527     Document Type: Article

References (53)

1. Lawrence T, Natoli G. Transcriptional regulation of macrophage polarization: enabling diversity with identity. Nat Rev Immunol. 2011;11(11):750-761.
2. Murray PJ, Wynn TA. Protective and pathogenic functions of macrophage subsets. Nat Rev Immunol. 2011;11(11):723-737.
3. Hashimoto D, et al. Tissue-resident macrophages self-maintain locally throughout adult life with minimal contribution from circulating monocytes. Immunity. 2013;38(4):792-804.
4. Satoh T, et al. Critical role of Trib1 in differentiation of tissue-resident M2-like macrophages. Nature. 2013;495(7442):524-528.
5. Wang Y, et al. IL-34 is a tissue-restricted ligand of CSF1R required for the development of Langerhans cells and microglia. Nat Immunol. 2012;13(8):753-760.
6. Dupasquier M, Stoitzner P, van Oudenaren A, Romani N, Leenen P. Macrophages and dendritic cells constitute a major subpopulation of cells in the mouse dermis. J Invest Dermatol. 2004;123(5):876-885.
7. O'Neill AS, van den Berg TK, Mullen GE. Sialoadhesin - a macrophage-restricted marker of immunoregulation and inflammation. Immunology. 2013;138(3):198-207.
8. + macrophages at the crossroads of antigen presentation. Trends Immunol. 2012;33(2):66-136.
9. + regulatory T cells and promote airway tolerance. J Exp Med. 2013;210(4):775-788.
10. Miyake Y, Asano K, Kaise H, Uemura M, Nakayama M, Tanaka M. Critical role of macrophages in the marginal zone in the suppression of immune responses to apoptotic cell-associated antigens. J Clin Invest. 2007;117(8):2268-2278.
11. McGaha TL, Chen Y, Ravishankar B, van Rooijen N, Karlsson MC. Marginal zone macrophages suppress innate and adaptive immunity to apoptotic cells in the spleen. Blood. 2011;117(20):5403-5412.
12. Wu C, et al. Sialoadhesin-positive macrophages bind regulatory T cells, negatively controlling their expansion and autoimmune disease progression. J Immunology. 2009;182(10):6508-6524.
13. Ip CW, Kroner A, Crocker PR, Nave KA, Martini R. Sialoadhesin deficiency ameliorates myelin degeneration and axonopathic changes in the CNS of PLP overexpressing mice. Neurobiol Dis. 2007;25(1):105-111.
14. Kobsar I, Oetke C, Kroner A, Wessig C, Crocker P, Martini R. Attenuated demyelination in the absence of the macrophage-restricted adhesion molecule sialoadhesin (Siglec-1) in mice heterozygously deficient in P0. Mol Cell Neurosci. 2006;31(4):685-691.
15. Asano K, et al. CD169-positive macrophages dominate antitumor immunity by crosspresenting dead cell-associated antigens. Immunity. 2011;34(1):85-180.
16. Harel-Adar T, Ben Mordechai T, Amsalem Y, Feinberg M, Leor J, Cohen S. Modulation of cardiac macrophages by phosphatidylserinepresenting liposomes improves infarct repair. Proc Natl Acad Sci U S A. 2011;108(5):1827-1859.
17. Jansen A, Homo-Delarche F, Hooijkaas H, Leenen P, Dardenne M, Drexhage H. Immunohistochemical characterization of monocytesmacrophages and dendritic cells involved in the initiation of the insulitis and beta-cell destruction in NOD mice. Diabetes. 1994;43(5):667-742.
18. Hartnell A, Steel J, Turley H, Jones M, Jackson D, Crocker P. Characterization of human sialoadhesin, a sialic acid binding receptor expressed by resident and inflammatory macrophage populations. Blood. 2001;97(1):288-296.
19. Zhu C, et al. The Tim-3 ligand galectin-9 negatively regulates T helper type 1 immunity. Nat Immunol. 2005;6(12):1245-1252.
20. Deaglio S, et al. Adenosine generation catalyzed by CD39 and CD73 expressed on regulatory T cells mediates immune suppression. J Exp Med. 2007;204(6):1257-1265.
21. Eltzschig HK, Sitkovsky MV, Robson SC. Purinergic signaling during inflammation. N Engl J Med. 2013;368(13):1260.
22. Kobayashi N, et al. TIM-1 and TIM-4 glycoproteins bind phosphatidylserine and mediate uptake of apoptotic cells. Immunity. 2007;27(6):927-940.
23. Miyanishi M, Tada K, Koike M, Uchiyama Y, Kitamura T, Nagata S. Identification of Tim4 as a phosphatidylserine receptor. Nature. 2007;450(7168):435-439.
24. Meyers JH, et al. TIM-4 is the ligand for TIM-1, and the TIM-1-TIM-4 interaction regulates T cell proliferation. Nat Immunol. 2005;6(5):455-464.
25. Lee E, et al. Effect of di (n-butyl) phthalate on testicular oxidative damage and antioxidant enzymes in hyperthyroid rats. Environ Toxicol. 2007;22(3):245-255.
26. Corton JC, Lapinskas PJ. Peroxisome proliferatoractivated receptors: mediators of phthalate esterinduced effects in the male reproductive tract? Toxicol Sci. 2005;83(1):4-17.
27. D'Addio F, et al. The link between the PDL1 costimulatory pathway and Th17 in fetomaternal tolerance. J Immunol. 2011;187(9):4530-4541.
28. Liu Y, Janeway C. Interferon gamma plays a critical role in induced cell death of effector T cell: a possible third mechanism of self-tolerance. J Exp Med. 1990;172(6):1735-1739.
29. Markees TG, et al. Long-term survival of skin allografts induced by donor splenocytes and anti-CD154 antibody in thymectomized mice requires CD4 (+) T cells, interferon-gamma, and CTLA4. J Clin Invest. 1998;101(11):2446-2455.
30. + regulatory T cells. Eur J Immunol. 2008;38(9):2512-2527.
31. Degauque N, et al. Immunostimulatory Tim-1-specific antibody deprograms Tregs and prevents transplant tolerance in mice. J Clin Invest. 2008;118(2):735-741.
32. Rodriguez-Manzanet R, et al. TIM-4 expressed on APCs induces T cell expansion and survival. J Immunol. 2008;180(7):4706-4713.
33. Warren JR, Lalwani ND, Reddy JK. Phthalate esters as peroxisome proliferator carcinogens. Environ Health Perspect. 1982;45:35-40.
34. Brown JM, et al. The coincidence of myocardial reperfusion injury and hydrogen peroxide production in the isolated rat heart. Surgery. 1989;105(4):496-501.
35. Park D, Hochreiter-Hufford A, Ravichandran KS. The phosphatidylserine receptor TIM-4 does not mediate direct signaling. Curr Biol. 2009;19(4):346-351.
36. Jones ND, et al. Differential susceptibility of heart, skin, and islet allografts to T cell-mediated rejection. J Immunol. 2001;166(4):2824-2830.
37. Li Y, Li XC, Zheng XX, Wells AD, Turka LA, Strom TB. Blocking both signal 1 and signal 2 of T-cell activation prevents apoptosis of alloreactive T cells and induction of peripheral allograft tolerance. Nat Med. 1999;5(11):1298-1302.
38. Schmelzle M, et al. CD39 modulates hematopoietic stem cell recruitment and promotes liver regeneration in mice and humans after partial hepatectomy. Ann Surg. 2013;257(4):693-701.
39. Saldanha-Araujo F, et al. Mesenchymal stromal cells up-regulate CD39 and increase adenosine production to suppress activated T-lymphocytes. Stem Cell Res. 2011;7(1):66-74.
40. Soriano P. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat Genet. 1999;21(1):70-71.
41. Yeung MY, et al. Interruption of dendritic cellmediated TIM-4 signaling induces regulatory T cells and promotes skin allograft survival. J Immunol. 2013;191(8):4447-4455.
42. Ueno T, et al. The emerging role of T cell Ig mucin 1 in alloimmune responses in an experimental mouse transplant model. J Clin Invest. 2008;118(2):742-751.
43. Kuchroo V, Umetsu D, DeKruyff R, Freeman G. The TIM gene family: emerging roles in immunity and disease. Nat Rev Immunol. 2003;3(6):454-462.
44. + Tregs. J Clin Invest. 2012;122(7):2395-2404.
45. Murphy SP, Porrett PM, Turka LA. Innate immunity in transplant tolerance and rejection. Immunol Rev. 2011;241(1):39-48.
46. Berney T, Secchi A. Rapamycin in islet transplantation: friend or foe? Transpl Int. 2009;22(2):153-161.
47. Liu W, Xiao X, Demirci G, Madsen J, Li XC. Innate NK cells and macrophages recognize and reject allogeneic nonself in vivo via different mechanisms. J Immunol. 2012;188(6):2703-2711.
48. Riquelme P, Geissler EK, Hutchinson JA. Alternative approaches to myeloid suppressor cell therapy in transplantation: comparing regulatory macrophages to tolerogenic DCs and MDSCs. Transplant Res. 2012;1(1):17.
49. Abe Y, et al. TIM-4 has dual function in the induction and effector phases of murine arthritis. J Immunol. 2013;191(9):4562-4572.
50. + cells of the splenic marginal zone - a novel type of resident dendritic cells. J Leukoc Biol. 2011;89(4):607-622.
51. Rodriguez-Manzanet R, et al. T and B cell hyperactivity and autoimmunity associated with nichespecific defects in apoptotic body clearance in TIM-4-deficient mice. Proc Natl Acad Sci U S A. 2010;107(19):8706-8711.
52. Gaspari AA, Katz SI. Contact hypersensitivity. Curr Protoc Immunol Chapter. 2001; Chapter 4:Unit 4 2.
53. Strom TB, Tilney NL, Paradysz JM, Bancewicz J, Carpenter CB. Cellular components of allograft rejection: identity, specificity, and cytotoxic function of cells infiltrating acutely rejecting allografts. J Immunol. 1977;118(6):2020-2026. Kidney Diseases