The pancreas anatomy conditions the origin and properties of resident macrophages

Journal of Experimental Medicine

Volumn 212, Issue 10, 2015, Pages 1497-1512

  Calderon, Boris ^a   Carrero, Javier A ^a   Ferris, Stephen T ^a   Sojka, Dorothy K ^a   Moore, Lindsay ^a   Epelman, Slava ^b   Murphy, Kenneth M ^a   Yokoyama, Wayne M ^a   Randolph, Gwendalyn J ^a   Unanue, Emil R ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b University in St Louis   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 1BETA; TUMOR NECROSIS FACTOR ALPHA; CCR2 PROTEIN, MOUSE; CD11 ANTIGEN; CHEMOKINE RECEPTOR CCR2; COLONY STIMULATING FACTOR 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD CELL; BONE MARROW CELL; CELL PLASTICITY; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; GENOTOXICITY; HEMATOPOIESIS; IRRADIATION; LEUKOCYTE; MACROPHAGE; MOUSE; NONHUMAN; PANCREAS; PRIORITY JOURNAL; PROTEIN EXPRESSION; STEADY STATE; ANATOMY AND HISTOLOGY; ANIMAL; C57BL MOUSE; CELL PROLIFERATION; CYTOLOGY; DIET; EMBRYOLOGY; GENE EXPRESSION PROFILING; GENETICS; METABOLISM; MUTANT MOUSE STRAIN; NEWBORN; PANCREAS ISLET; PHYSIOLOGY;

ANIMALS; ANIMALS, NEWBORN; ANTIGENS, CD11; CELL PROLIFERATION; DIET; GENE EXPRESSION PROFILING; ISLETS OF LANGERHANS; LEUKOCYTES; MACROPHAGE COLONY-STIMULATING FACTOR; MACROPHAGES; MICE, INBRED C57BL; MICE, MUTANT STRAINS; PANCREAS; RECEPTORS, CCR2;

EID: 84943384367     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20150496     Document Type: Article

References (63)

1. Ajami, B., J.L. Bennett, C. Krieger, K.M. McNagny, and F.M. Rossi. 2011. Infiltrating monocytes trigger EAE progression, but do not contribute to the resident microglia pool. Nat. Neurosci. 14: 1142-1149. http://dx.doi.org/ 10.1038/nn.2887
2. Bain, C.C., A. Bravo-Blas, C.L. Scott, E. Gomez Perdiguero, F. Geissmann, S. Henri, B. Malissen, L.C. Osborne, D. Artis, and A.M. Mowat. 2014. Constant replenishment from circulating monocytes maintains the macrophage pool in the intestine of adult mice. Nat. Immunol. 15: 929-937. http://dx.doi.org/10.1038/ni.2967
3. Banaei-Bouchareb, L., V. Gouon-Evans, D. Samara-Boustani, M.C. Castellotti, P. Czernichow, J.W. Pollard, and M. Polak. 2004. Insulin cell mass is altered in Csf1op/Csf1op macrophage-deficient mice. J. Leukoc. Biol. 76: 359-367. http://dx.doi.org/10.1189/jlb.1103591
4. Böiers, C., N. Buza-Vidas, C.T. Jensen, C.J. Pronk, S. Kharazi, L. Wittmann, E. Sitnicka, A. Hultquist, and S.E. Jacobsen. 2010. Expression and role of FLT3 in regulation of the earliest stage of normal granulocyte-monocyte progenitor development. Blood. 115: 5061-5068. http://dx.doi.org/10.1182/blood-2009-12-258756
5. Boyer, S.W., A.V. Schroeder, S. Smith-Berdan, and E.C. Forsberg. 2011. All hematopoietic cells develop from hematopoietic stem cells through Flk2/Flt3-positive progenitor cells. Cell Stem Cell. 9: 64-73. http://dx .doi.org/10.1016/j.stem.2011.04.021
6. Boyer, S.W., A.E. Beaudin, and E.C. Forsberg. 2012. Mapping differentiation pathways from hematopoietic stem cells using Flk2/Flt3 lineage tracing. Cell Cycle. 11: 3180-3188. http://dx.doi.org/10.4161/cc.21279
7. Buza-Vidas, N., P. Woll, A. Hultquist, S. Duarte, M. Lutteropp, T. Bouriez-Jones, H. Ferry, S. Luc, and S.E. Jacobsen. 2011. FLT3 expression initiates in fully multipotent mouse hematopoietic progenitor cells. Blood. 118: 1544-1548. http://dx.doi.org/10.1182/blood-2010-10-316232
8. Calderon, B., A. Suri, M.J. Miller, and E.R. Unanue. 2008. Dendritic cells in islets of Langerhans constitutively present β cell-derived peptides bound to their class II MHC molecules. Proc. Natl. Acad. Sci. USA. 105: 6121-6126. http://dx.doi.org/10.1073/pnas.0801973105
9. Calderon, B., J.A. Carrero, and E.R. Unanue. 2014. The central role of antigen presentation in islets of Langerhans in autoimmune diabetes. Curr. Opin. Immunol. 26: 32-40. http://dx.doi.org/10.1016/j.coi.2013.10.011
10. Carrero, J.A., H. Vivanco-Cid, and E.R. Unanue. 2012. Listeriolysin O is strongly immunogenic independently of its cytotoxic activity. PLoS ONE. 7:e32310. http://dx.doi.org/10.1371/journal.pone.0032310
11. Chu, G.C., A.C. Kimmelman, A.F. Hezel, and R.A. DePinho. 2007. Stromal biology of pancreatic cancer. J. Cell. Biochem. 101: 887-907. http://dx .doi.org/10.1002/jcb.21209
12. Clark, C.E., S.R. Hingorani, R. Mick, C. Combs, D.A. Tuveson, and R.H. Vonderheide. 2007. Dynamics of the immune reaction to pancreatic cancer from inception to invasion. Cancer Res. 67: 9518-9527. http://dx.doi.org/10.1158/0008-5472.CAN-07-0175
13. Cucak, H., L.G. Grunnet, and A. Rosendahl. 2014. Accumulation of M1-like macrophages in type 2 diabetic islets is followed by a systemic shift in macrophage polarization. J. Leukoc. Biol. 95: 149-160. http://dx .doi.org/10.1189/jlb.0213075
14. DeFalco, T., I. Bhattacharya, A.V. Williams, D.M. Sams, and B. Capel. 2014. Yolk-sac-derived macrophages regulate fetal testis vascularization and morphogenesis. Proc. Natl. Acad. Sci. USA. 111:E2384-E2393. http://dx.doi.org/10.1073/pnas.1400057111
15. Ehses, J.A., A. Perren, E. Eppler, P. Ribaux, J.A. Pospisilik, R. Maor-Cahn, X. Gueripel, H. Ellingsgaard, M.K. Schneider, G. Biollaz, et al. 2007. Increased number of islet-associated macrophages in type 2 diabetes. Diabetes. 56: 2356-2370. http://dx.doi.org/10.2337/db06-1650
16. Epelman, S., K.J. Lavine, A.E. Beaudin, D.K. Sojka, J.A. Carrero, B. Calderon, T. Brija, E.L. Gautier, S. Ivanov, A.T. Satpathy, et al. 2014a. Embryonic and adult-derived resident cardiac macrophages are maintained through distinct mechanisms at steady state and during inflammation. Immunity. 40: 91-104. http://dx.doi.org/10.1016/j.immuni.2013.11.019
17. Epelman, S., K.J. Lavine, and G.J. Randolph. 2014b. Origin and functions of tissue macrophages. Immunity. 41: 21-35. http://dx.doi.org/10.1016/j.immuni.2014.06.013
18. Ferrante, A.W. Jr. 2013. The immune cells in adipose tissue. Diabetes Obes. Metab. 15: 34-38. http://dx.doi.org/10.1111/dom.12154
19. Ferris, S.T., J.A. Carrero, J.F. Mohan, B. Calderon, K.M. Murphy, and E.R. Unanue. 2014. A minor subset of Batf3-dependent antigen-presenting cells in islets of Langerhans is essential for the development of autoimmune diabetes. Immunity. 41: 657-669. http://dx.doi.org/10.1016/j.immuni.2014.09.012
20. Gautier, E.L., T. Shay, J. Miller, M. Greter, C. Jakubzick, S. Ivanov, J. Helft, A. Chow, K.G. Elpek, S. Gordonov, et al. Immunological Genome Consortium. 2012. Gene-expression profiles and transcriptional regulatory pathways that underlie the identity and diversity of mouse tissue macrophages. Nat. Immunol. 13: 1118-1128. http://dx.doi.org/10.1038/ni.2419
21. Geutskens, S.B., T. Otonkoski, M.A. Pulkkinen, H.A. Drexhage, and P.J. Leenen. 2005. Macrophages in the murine pancreas and their involvement in fetal endocrine development in vitro. J. Leukoc. Biol. 78: 845-852. http://dx.doi.org/10.1189/jlb.1004624
22. Ginhoux, F., M. Greter, M. Leboeuf, S. Nandi, P. See, S. Gokhan, M.F. Mehler, S.J. Conway, L.G. Ng, E.R. Stanley, et al. 2010. Fate mapping analysis reveals that adult microglia derive from primitive macrophages. Science. 330: 841-845. http://dx.doi.org/10.1126/science.1194637
23. Gordon, S., A. Plüddemann, and F. Martinez Estrada. 2014. Macrophage heterogeneity in tissues: phenotypic diversity and functions. Immunol. Rev. 262: 36-55. http://dx.doi.org/10.1111/imr.12223
24. Gosselin, D., V.M. Link, C.E. Romanoski, G.J. Fonseca, D.Z. Eichenfield, N.J. Spann, J.D. Stender, H.B. Chun, H. Garner, F. Geissmann, and C.K. Glass. 2014. Environment drives selection and function of enhancers controlling tissue-specific macrophage identities. Cell. 159: 1327-1340. http://dx.doi.org/10.1016/j.cell.2014.11.023
25. Guilliams, M., I. De Kleer, S. Henri, S. Post, L. Vanhoutte, S. De Prijck, K. Deswarte, B. Malissen, H. Hammad, and B.N. Lambrecht. 2013. Alveolar macrophages develop from fetal monocytes that differentiate into long-lived cells in the first week of life via GM-CSF. J. Exp. Med. 210:1977-1992.
26. Haniffa, M., F. Ginhoux, X.N. Wang, V. Bigley, M. Abel, I. Dimmick, S. Bullock, M. Grisotto, T. Booth, P. Taub, et al. 2009. Differential rates of replacement of human dermal dendritic cells and macrophages during hematopoietic stem cell transplantation. J. Exp. Med. 206: 371-385. http://dx.doi.org/10.1084/jem.20081633
27. Hashimoto, D., A. Chow, C. Noizat, P. Teo, M.B. Beasley, M. Leboeuf, C.D. Becker, P. See, J. Price, D. Lucas, et al. 2013. Tissue-resident macrophages self-maintain locally throughout adult life with minimal contribution from circulating monocytes. Immunity. 38: 792-804. http://dx.doi.org/10.1016/j.immuni.2013.04.004
28. Hoeffel, G., Y. Wang, M. Greter, P. See, P. Teo, B. Malleret, M. Leboeuf, D. Low, G. Oller, F. Almeida, et al. 2012. Adult Langerhans cells derive predominantly from embryonic fetal liver monocytes with a minor contribution of yolk sac-derived macrophages. J. Exp. Med. 209: 1167-1181. http://dx.doi.org/10.1084/jem.20120340
29. Hume, D.A., D. Halpin, H. Charlton, and S. Gordon. 1984. The mononuclear phagocyte system of the mouse defined by immunohistochemical localization of antigen F4/80: macrophages of endocrine organs. Proc. Natl. Acad. Sci. USA. 81: 4174-4177. http://dx.doi.org/10.1073/pnas.81.13.4174
30. Ino, K., M. Masuya, I. Tawara, E. Miyata, K. Oda, Y. Nakamori, K. Suzuki, K. Ohishi, and N. Katayama. 2014. Monocytes infiltrate the pancreas via the MCP-1/CCR2 pathway and differentiate into stellate cells. PLoS ONE. 9:e84889. http://dx.doi.org/10.1371/journal.pone.0084889
31. Kumaravelu, P., L. Hook, A.M. Morrison, J. Ure, S. Zhao, S. Zuyev, J. Ansell, and A. Medvinsky. 2002. Quantitative developmental anatomy of definitive haematopoietic stem cells/long-term repopulating units (HSC/RUs):role of the aorta-gonad-mesonephros (AGM) region and the yolk sac in colonisation of the mouse embryonic liver. Development. 129:4891-4899.
32. Lavin, Y., D. Winter, R. Blecher-Gonen, E. David, H. Keren-Shaul, M. Merad, S. Jung, and I. Amit. 2014. Tissue-resident macrophage enhancer landscapes are shaped by the local microenvironment. Cell. 159: 1312-1326. http://dx.doi.org/10.1016/j.cell.2014.11.018
33. Lewis, K.L., M.L. Caton, M. Bogunovic, M. Greter, L.T. Grajkowska, D. Ng, A. Klinakis, I.F. Charo, S. Jung, J.L. Gommerman, et al. 2011. Notch2 receptor signaling controls functional differentiation of dendritic cells in the spleen and intestine. Immunity. 35: 780-791. http://dx.doi.org/10.1016/j.immuni.2011.08.013
34. Li, D.S., Y.H. Yuan, H.J. Tu, Q.L. Liang, and L.J. Dai. 2009. A protocol for islet isolation from mouse pancreas. Nat. Protoc. 4: 1649-1652. http://dx.doi.org/10.1038/nprot.2009.150
35. Lichanska, A.M., and D.A. Hume. 2000. Origins and functions of phagocytes in the embryo. Exp. Hematol. 28: 601-611. http://dx.doi.org/10.1016/S0301-472X(00)00157-0
36. Lichanska, A.M., C.M. Browne, G.W. Henkel, K.M. Murphy, M.C. Ostrowski, S.R. McKercher, R.A. Maki, and D.A. Hume. 1999. Differentiation of the mononuclear phagocyte system during mouse embryogenesis: the role of transcription factor PU.1. Blood. 94:127-138.
37. Lin, H., E. Lee, K. Hestir, C. Leo, M. Huang, E. Bosch, R. Halenbeck, G. Wu, A. Zhou, D. Behrens, et al. 2008. Discovery of a cytokine and its receptor by functional screening of the extracellular proteome. Science. 320: 807-811. http://dx.doi.org/10.1126/science.1154370
38. Lumeng, C.N., J.L. Bodzin, and A.R. Saltiel. 2007. Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J. Clin. Invest. 117: 175-184. http://dx.doi.org/10.1172/JCI29881
39. Melli, K., R.S. Friedman, A.E. Martin, E.B. Finger, G. Miao, G.L. Szot, M.F. Krummel, and Q. Tang. 2009. Amplification of autoimmune response through induction of dendritic cell maturation in inflamed tissues. J. Immunol. 182: 2590-2600. http://dx.doi.org/10.4049/jimmunol .0803543
40. Merad, M., P. Sathe, J. Helft, J. Miller, and A. Mortha. 2013. The dendritic cell lineage: ontogeny and function of dendritic cells and their subsets in the steady state and the inflamed setting. Annu. Rev. Immunol. 31: 563-604. http://dx.doi.org/10.1146/annurev-immunol-020711-074950
41. Meredith, M.M., K. Liu, G. Darrasse-Jeze, A.O. Kamphorst, H.A. Schreiber, P. Guermonprez, J. Idoyaga, C. Cheong, K.H. Yao, R.E. Niec, and M.C. Nussenzweig. 2012. Expression of the zinc finger transcription factor zDC (Zbtb46, Btbd4) defines the classical dendritic cell lineage. J. Exp. Med. 209: 1153-1165. http://dx.doi.org/10.1084/jem .20112675
42. Mohan, J.F., M.G. Levisetti, B. Calderon, J.W. Herzog, S.J. Petzold, and E.R. Unanue. 2010. Unique autoreactive T cells recognize insulin peptides generated within the islets of Langerhans in autoimmune diabetes. Nat. Immunol. 11: 350-354. http://dx.doi.org/10.1038/ni.1850
43. Molawi, K., Y. Wolf, P.K. Kandalla, J. Favret, N. Hagemeyer, K. Frenzel, A.R. Pinto, K. Klapproth, S. Henri, B. Malissen, et al. 2014. Progressive replacement of embryo-derived cardiac macrophages with age. J. Exp. Med. 211: 2151-2158. http://dx.doi.org/10.1084/jem.20140639
44. Murray, P.J., and T.A. Wynn. 2011. Protective and pathogenic functions of macrophage subsets. Nat. Rev. Immunol. 11: 723-737. http://dx.doi.org/ 10.1038/nri3073
45. Murray, P.J., J.E. Allen, S.K. Biswas, E.A. Fisher, D.W. Gilroy, S. Goerdt, S. Gordon, J.A. Hamilton, L.B. Ivashkiv, T. Lawrence, et al. 2014. Macrophage activation and polarization: nomenclature and experimental guidelines. Immunity. 41: 14-20. http://dx.doi.org/10.1016/j.immuni.2014.06.008
46. Peng, H., X. Jiang, Y. Chen, D.K. Sojka, H. Wei, X. Gao, R. Sun, W.M. Yokoyama, and Z. Tian. 2013. Liver-resident NK cells confer adaptive immunity in skin-contact inflammation. J. Clin. Invest. 123: 1444-1456. http://dx.doi.org/10.1172/JCI66381
47. Pinto, A.R., R. Paolicelli, E. Salimova, J. Gospocic, E. Slonimsky, D. Bilbao-Cortes, J.W. Godwin, and N.A. Rosenthal. 2012. An abundant tissue macrophage population in the adult murine heart with a distinct alternatively-activated macrophage profile. PLoS ONE. 7:e36814. http://dx.doi.org/10.1371/journal.pone.0036814
48. Pollard, J.W., M.G. Dominguez, S. Mocci, P.E. Cohen, and E.R. Stanley. 1997. Effect of the colony-stimulating factor-1 null mutation, osteopetrotic (csfm(op)), on the distribution of macrophages in the male mouse reproductive tract. Biol. Reprod. 56: 1290-1300. http://dx.doi.org/10.1095/biolreprod56.5.1290
49. Richardson, S.J., A. Willcox, A.J. Bone, A.K. Foulis, and N.G. Morgan. 2009. Islet-associated macrophages in type 2 diabetes. Diabetologia. 52: 1686-1688. http://dx.doi.org/10.1007/s00125-009-1410-z
50. Salvalaggio, P.R., S. Deng, C.E. Ariyan, I. Millet, W.S. Zawalich, G.P. Basadonna, and D.M. Rothstein. 2002. Islet filtration: a simple and rapid new purification procedure that avoids ficoll and improves islet mass and function. Transplantation. 74: 877-879. http://dx.doi.org/10.1097/ 00007890-200209270-00023
51. Satpathy, A.T., W. Kc, J.C. Albring, B.T. Edelson, N.M. Kretzer, D. Bhattacharya, T.L. Murphy, and K.M. Murphy. 2012. Zbtb46 expression distinguishes classical dendritic cells and their committed progenitors from other immune lineages. J. Exp. Med. 209: 1135-1152. http://dx.doi.org/10.1084/jem.20120030
52. Satpathy, A.T., C.G. Briseño, J.S. Lee, D. Ng, N.A. Manieri, W. Kc, X. Wu, S.R. Thomas, W.L. Lee, M. Turkoz, et al. 2013. Notch2-dependent classical dendritic cells orchestrate intestinal immunity to attachingand-effacing bacterial pathogens. Nat. Immunol. 14: 937-948. http://dx .doi.org/10.1038/ni.2679
53. Schulz, C., E. Gomez Perdiguero, L. Chorro, H. Szabo-Rogers, N. Cagnard, K. Kierdorf, M. Prinz, B. Wu, S.E. Jacobsen, J.W. Pollard, et al. 2012. A lineage of myeloid cells independent of Myb and hematopoietic stem cells. Science. 336: 86-90. http://dx.doi.org/10.1126/science .1219179
54. Serbina, N.V., and E.G. Pamer. 2006. Monocyte emigration from bone marrow during bacterial infection requires signals mediated by chemokine receptor CCR2. Nat. Immunol. 7: 311-317. http://dx.doi.org/10.1038/ni1309
55. Shaul, M.E., G. Bennett, K.J. Strissel, A.S. Greenberg, and M.S. Obin. 2010. Dynamic, M2-like remodeling phenotypes of CD11c+ adipose tissue macrophages during high-fat diet-induced obesity in mice. Diabetes. 59: 1171-1181. http://dx.doi.org/10.2337/db09-1402
56. Sica, A., and A. Mantovani. 2012. Macrophage plasticity and polarization:in vivo veritas. J. Clin. Invest. 122: 787-795. http://dx.doi.org/10.1172/JCI59643
57. Sojka, D.K., B. Plougastel-Douglas, L. Yang, M.A. Pak-Wittel, M.N. Artyomov, Y. Ivanova, C. Zhong, J.M. Chase, P.B. Rothman, J. Yu, et al. 2014. Tissue-resident natural killer (NK) cells are cell lineages distinct from thymic and conventional splenic NK cells. eLife. 3:e01659. http://dx.doi.org/10.7554/eLife.01659
58. Spits, H., D. Artis, M. Colonna, A. Diefenbach, J.P. Di Santo, G. Eberl, S. Koyasu, R.M. Locksley, A.N. McKenzie, R.E. Mebius, et al. 2013. Innate lymphoid cells-a proposal for uniform nomenclature. Nat. Rev. Immunol. 13: 145-149. http://dx.doi.org/10.1038/nri3365
59. Wang, Y., K.J. Szretter, W. Vermi, S. Gilfillan, C. Rossini, M. Cella, A.D. Barrow, M.S. Diamond, and M. Colonna. 2012. IL-34 is a tissue-restricted ligand of CSF1R required for the development of Langerhans cells and microglia. Nat. Immunol. 13: 753-760. http://dx.doi.org/10.1038/ni.2360
60. Westwell-Roper, C.Y., J.A. Ehses, and C.B. Verchere. 2014. Resident macrophages mediate islet amyloid polypeptide-induced islet IL-1β production and β-cell dysfunction. Diabetes. 63: 1698-1711. http://dx.doi .org/10.2337/db13-0863
61. Xiao, X., I. Gaffar, P. Guo, J. Wiersch, S. Fischbach, L. Peirish, Z. Song, Y. El-Gohary, K. Prasadan, C. Shiota, and G.K. Gittes. 2014. M2 macrophages promote beta-cell proliferation by up-regulation of SMAD7. Proc. Natl. Acad. Sci. USA. 111:E1211-E1220. http://dx.doi.org/10.1073/pnas.1321347111
62. Yin, N., N. Zhang, G. Lal, J. Xu, M. Yan, Y. Ding, and J.S. Bromberg. 2011. Lymphangiogenesis is required for pancreatic islet inflammation and diabetes. PLoS ONE. 6:e28023. http://dx.doi.org/10.1371/journal .pone.0028023
63. Yona, S., K.W. Kim, Y. Wolf, A. Mildner, D. Varol, M. Breker, D. Strauss-Ayali, S. Viukov, M. Guilliams, A. Misharin, et al. 2013. Fate mapping reveals origins and dynamics of monocytes and tissue macrophages under homeostasis. Immunity. 38: 79-91. http://dx.doi.org/10.1016/j.immuni.2012.12.001