Expansion of Islet-Resident Macrophages Leads to Inflammation Affecting β Cell Proliferation and Function in Obesity

Cell Metabolism

Volumn 29, Issue 2, 2019, Pages 457-474.e5

  Ying, Wei ^a   Lee, Yun Sok ^a   Dong, Yi ^b   Seidman, Jason S ^a,c   Yang, Meixiang ^b,d   Isaac, Roi ^a   Seo, Jong Bae ^a   Yang, Bi Huei ^b   Wollam, Joshua ^a   Riopel, Matthew ^a   McNelis, Joanne ^a   Glass, Christopher K ^a,c   Olefsky, Jerrold M ^a   Fu, Wenxian ^b  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d JINAN UNIVERSITY   (China)

Author keywords

islet inflammation; local macrophages proliferation; macrophages; obesity; cell function; cell proliferation

Indexed keywords

GLYCOPROTEIN P 15095; TRANSCRIPTOME; PLATELET DERIVED GROWTH FACTOR RECEPTOR;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL POPULATION; CELL PROLIFERATION; COMPARATIVE STUDY; CONTROLLED STUDY; DISEASE ASSOCIATION; FLOW CYTOMETRY; IMMUNOCOMPETENT CELL; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; INSULIN RELEASE; MACROPHAGE; MALE; MIN6 CELL LINE; MONOCYTE; MOUSE; NONHUMAN; OBESITY; PANCREAS ISLET BETA CELL; PHENOTYPE; PRIORITY JOURNAL; SECRETORY GRANULE; SIGNAL TRANSDUCTION; ANIMAL; C57BL MOUSE; CELL LINE; CYTOLOGY; IMMUNOLOGY; INFLAMMATION; METABOLISM; MOUSE MUTANT; PATHOLOGY;

ANIMALS; CELL LINE; CELL PROLIFERATION; INFLAMMATION; INSULIN SECRETION; INSULIN-SECRETING CELLS; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; MICE, OBESE; OBESITY; RECEPTORS, PLATELET-DERIVED GROWTH FACTOR;

EID: 85060733725     PISSN: 15504131     EISSN: 19327420     Source Type: Journal    
DOI: 10.1016/j.cmet.2018.12.003     Document Type: Article

References (113)

1. Aamodt, K.I., Powers, A.C., Signals in the pancreatic islet microenvironment influence β-cell proliferation. Diabetes Obes. Metab. 19:Suppl 1 (2017), 124–136.
2. Alonso, L.C., Yokoe, T., Zhang, P., Scott, D.K., Kim, S.K., O'Donnell, C.P., Garcia-Ocaña, A., Glucose infusion in mice: a new model to induce beta-cell replication. Diabetes 56 (2007), 1792–1801.
3. Amano, S.U., Cohen, J.L., Vangala, P., Tencerova, M., Nicoloro, S.M., Yawe, J.C., Shen, Y., Czech, M.P., Aouadi, M., Local proliferation of macrophages contributes to obesity-associated adipose tissue inflammation. Cell Metab. 19 (2014), 162–171.
4. Araújo, T.G., Oliveira, A.G., Carvalho, B.M., Guadagnini, D., Protzek, A.O., Carvalheira, J.B., Boschero, A.C., Saad, M.J., Hepatocyte growth factor plays a key role in insulin resistance-associated compensatory mechanisms. Endocrinology 153 (2012), 5760–5769.
5. Assmann, A., Ueki, K., Winnay, J.N., Kadowaki, T., Kulkarni, R.N., Glucose effects on beta-cell growth and survival require activation of insulin receptors and insulin receptor substrate 2. Mol. Cell. Biol. 29 (2009), 3219–3228.
6. Banaei-Bouchareb, L., Gouon-Evans, V., Samara-Boustani, D., Castellotti, M.C., Czernichow, P., Pollard, J.W., Polak, M., Insulin cell mass is altered in Csf1op/Csf1op macrophage-deficient mice. J. Leukoc. Biol. 76 (2004), 359–367.
7. Bensellam, M., Jonas, J.C., Laybutt, D.R., Mechanisms of β-cell dedifferentiation in diabetes: recent findings and future research directions. J. Endocrinol. 236 (2018), R109–R143.
8. Braune, J., Weyer, U., Hobusch, C., Mauer, J., Brüning, J.C., Bechmann, I., Gericke, M., IL-6 regulates M2 polarization and local proliferation of adipose tissue macrophages in obesity. J. Immunol. 198 (2017), 2927–2934.
9. Brooks-Worrell, B.M., Juneja, R., Minokadeh, A., Greenbaum, C.J., Palmer, J.P., Cellular immune responses to human islet proteins in antibody-positive type 2 diabetic patients. Diabetes 48 (1999), 983–988.
10. Brooks-Worrell, B.M., Greenbaum, C.J., Palmer, J.P., Pihoker, C., Autoimmunity to islet proteins in children diagnosed with new-onset diabetes. J. Clin. Endocrinol. Metab. 89 (2004), 2222–2227.
11. Butcher, M.J., Hallinger, D., Garcia, E., Machida, Y., Chakrabarti, S., Nadler, J., Galkina, E.V., Imai, Y., Association of proinflammatory cytokines and islet resident leucocytes with islet dysfunction in type 2 diabetes. Diabetologia 57 (2014), 491–501.
12. Calderon, B., Carrero, J.A., Ferris, S.T., Sojka, D.K., Moore, L., Epelman, S., Murphy, K.M., Yokoyama, W.M., Randolph, G.J., Unanue, E.R., The pancreas anatomy conditions the origin and properties of resident macrophages. J. Exp. Med. 212 (2015), 1497–1512.
13. Chen, H., Gu, X., Liu, Y., Wang, J., Wirt, S.E., Bottino, R., Schorle, H., Sage, J., Kim, S.K., PDGF signalling controls age-dependent proliferation in pancreatic β-cells. Nature 478 (2011), 349–355.
14. Chera, S., Baronnier, D., Ghila, L., Cigliola, V., Jensen, J.N., Gu, G., Furuyama, K., Thorel, F., Gribble, F.M., Reimann, F., Herrera, P.L., Diabetes recovery by age-dependent conversion of pancreatic δ-cells into insulin producers. Nature 514 (2014), 503–507.
15. Chintalgattu, V., Rees, M.L., Culver, J.C., Goel, A., Jiffar, T., Zhang, J., Dunner, K. Jr., Pati, S., Bankson, J.A., Pasqualini, R., et al. Coronary microvascular pericytes are the cellular target of sunitinib malate-induced cardiotoxicity. Sci. Transl. Med., 5, 2013, 187ra69.
16. Criscimanna, A., Coudriet, G.M., Gittes, G.K., Piganelli, J.D., Esni, F., Activated macrophages create lineage-specific microenvironments for pancreatic acinar- and beta-cell regeneration in mice. Gastroenterology 147 (2014), 1106–1118.
17. Cucak, H., Grunnet, L.G., Rosendahl, A., Accumulation of M1-like macrophages in type 2 diabetic islets is followed by a systemic shift in macrophage polarization. J. Leukoc. Biol. 95 (2014), 149–160.
18. Dalmas, E., Lehmann, F.M., Dror, E., Wueest, S., Thienel, C., Borsigova, M., Stawiski, M., Traunecker, E., Lucchini, F.C., Dapito, D.H., et al. Interleukin-33-activated islet-resident innate lymphoid cells promote insulin secretion through myeloid cell retinoic acid production. Immunity 47 (2017), 928–942.
19. Demirci, C., Ernst, S., Alvarez-Perez, J.C., Rosa, T., Valle, S., Shridhar, V., Casinelli, G.P., Alonso, L.C., Vasavada, R.C., García-Ocana, A., Loss of HGF/c-Met signaling in pancreatic β-cells leads to incomplete maternal β-cell adaptation and gestational diabetes mellitus. Diabetes 61 (2012), 1143–1152.
20. Diana, J., Simoni, Y., Furio, L., Beaudoin, L., Agerberth, B., Barrat, F., Lehuen, A., Crosstalk between neutrophils, B-1a cells and plasmacytoid dendritic cells initiates autoimmune diabetes. Nat. Med. 19 (2013), 65–73.
21. Dobin, A., Davis, C.A., Schlesinger, F., Drenkow, J., Zaleski, C., Jha, S., Batut, P., Chaisson, M., Gingeras, T.R., STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29 (2013), 15–21.
22. Donath, M.Y., Targeting inflammation in the treatment of type 2 diabetes. Diabetes Obes. Metab. 15:Suppl 3 (2013), 193–196.
23. Donath, M.Y., Shoelson, S.E., Type 2 diabetes as an inflammatory disease. Nat. Rev. Immunol. 11 (2011), 98–107.
24. Donath, M.Y., Schumann, D.M., Faulenbach, M., Ellingsgaard, H., Perren, A., Ehses, J.A., Islet inflammation in type 2 diabetes: from metabolic stress to therapy. Diabetes Care 31:Suppl 2 (2008), S161–S164.
25. Donath, M.Y., Størling, J., Berchtold, L.A., Billestrup, N., Mandrup-Poulsen, T., Cytokines and beta-cell biology: from concept to clinical translation. Endocr. Rev. 29 (2008), 334–350.
26. Donath, M.Y., Dalmas, É., Sauter, N.S., Böni-Schnetzler, M., Inflammation in obesity and diabetes: islet dysfunction and therapeutic opportunity. Cell Metab. 17 (2013), 860–872.
27. Ebato, C., Uchida, T., Arakawa, M., Komatsu, M., Ueno, T., Komiya, K., Azuma, K., Hirose, T., Tanaka, K., Kominami, E., et al. Autophagy is important in islet homeostasis and compensatory increase of beta cell mass in response to high-fat diet. Cell Metab. 8 (2008), 325–332.
28. Eguchi, K., Nagai, R., Islet inflammation in type 2 diabetes and physiology. J. Clin. Invest. 127 (2017), 14–23.
29. Eguchi, K., Manabe, I., Oishi-Tanaka, Y., Ohsugi, M., Kono, N., Ogata, F., Yagi, N., Ohto, U., Kimoto, M., Miyake, K., et al. Saturated fatty acid and TLR signaling link β cell dysfunction and islet inflammation. Cell Metab. 15 (2012), 518–533.
30. Ehses, J.A., Perren, A., Eppler, E., Ribaux, P., Pospisilik, J.A., Maor-Cahn, R., Gueripel, X., Ellingsgaard, H., Schneider, M.K., Biollaz, G., et al. Increased number of islet-associated macrophages in type 2 diabetes. Diabetes 56 (2007), 2356–2370.
31. El Ouaamari, A., Dirice, E., Gedeon, N., Hu, J., Zhou, J.Y., Shirakawa, J., Hou, L., Goodman, J., Karampelias, C., Qiang, G., et al. SerpinB1 promotes pancreatic β cell proliferation. Cell Metab. 23 (2016), 194–205.
32. Fu, W., Wojtkiewicz, G., Weissleder, R., Benoist, C., Mathis, D., Early window of diabetes determinism in NOD mice, dependent on the complement receptor CRIg, identified by noninvasive imaging. Nat. Immunol. 13 (2012), 361–368.
33. Fu, W., Farache, J., Clardy, S.M., Hattori, K., Mander, P., Lee, K., Rioja, I., Weissleder, R., Prinjha, R.K., Benoist, C., Mathis, D., Epigenetic modulation of type-1 diabetes via a dual effect on pancreatic macrophages and β cells. eLife, 3, 2014, e04631.
34. Gagnerault, M.C., Luan, J.J., Lotton, C., Lepault, F., Pancreatic lymph nodes are required for priming of beta cell reactive T cells in NOD mice. J. Exp. Med. 196 (2002), 369–377.
35. Garcia-Ocaña, A., Takane, K.K., Syed, M.A., Philbrick, W.M., Vasavada, R.C., Stewart, A.F., Hepatocyte growth factor overexpression in the islet of transgenic mice increases beta cell proliferation, enhances islet mass, and induces mild hypoglycemia. J. Biol. Chem. 275 (2000), 1226–1232.
36. Gautier, E.L., Shay, T., Miller, J., Greter, M., Jakubzick, C., Ivanov, S., Helft, J., Chow, A., Elpek, K.G., Gordonov, S., et al., Immunological Genome Consortium. Gene-expression profiles and transcriptional regulatory pathways that underlie the identity and diversity of mouse tissue macrophages. Nat. Immunol. 13 (2012), 1118–1128.
37. Geutskens, S.B., Otonkoski, T., Pulkkinen, M.A., Drexhage, H.A., Leenen, P.J., Macrophages in the murine pancreas and their involvement in fetal endocrine development in vitro. J. Leukoc. Biol. 78 (2005), 845–852.
38. Goel, A., Chiu, H., Felton, J., Palmer, J.P., Brooks-Worrell, B., T-cell responses to islet antigens improves detection of autoimmune diabetes and identifies patients with more severe beta-cell lesions in phenotypic type 2 diabetes. Diabetes 56 (2007), 2110–2115.
39. Gordon, S., Plüddemann, A., Tissue macrophages: heterogeneity and functions. BMC Biol., 15, 2017, 53.
40. Gosselin, D., Link, V.M., Romanoski, C.E., Fonseca, G.J., Eichenfield, D.Z., Spann, N.J., Stender, J.D., Chun, H.B., Garner, H., Geissmann, F., Glass, C.K., Environment drives selection and function of enhancers controlling tissue-specific macrophage identities. Cell 159 (2014), 1327–1340.
41. Gregor, M.F., Hotamisligil, G.S., Inflammatory mechanisms in obesity. Annu. Rev. Immunol. 29 (2011), 415–445.
42. Haase, J., Weyer, U., Immig, K., Klöting, N., Blüher, M., Eilers, J., Bechmann, I., Gericke, M., Local proliferation of macrophages in adipose tissue during obesity-induced inflammation. Diabetologia 57 (2014), 562–571.
43. Haataja, L., Gurlo, T., Huang, C.J., Butler, P.C., Islet amyloid in type 2 diabetes, and the toxic oligomer hypothesis. Endocr. Rev. 29 (2008), 303–316.
44. Hasnain, S.Z., Borg, D.J., Harcourt, B.E., Tong, H., Sheng, Y.H., Ng, C.P., Das, I., Wang, R., Chen, A.C., Loudovaris, T., et al. Glycemic control in diabetes is restored by therapeutic manipulation of cytokines that regulate beta cell stress. Nat. Med. 20 (2014), 1417–1426.
45. Heinz, S., Benner, C., Spann, N., Bertolino, E., Lin, Y.C., Laslo, P., Cheng, J.X., Murre, C., Singh, H., Glass, C.K., Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol. Cell 38 (2010), 576–589.
46. Heng, T.S., Painter, M.W., Immunological Genome Project Consortium. The Immunological Genome Project: networks of gene expression in immune cells. Nat. Immunol. 9 (2008), 1091–1094.
47. Höglund, P., Mintern, J., Waltzinger, C., Heath, W., Benoist, C., Mathis, D., Initiation of autoimmune diabetes by developmentally regulated presentation of islet cell antigens in the pancreatic lymph nodes. J. Exp. Med. 189 (1999), 331–339.
48. Hotamisligil, G.S., Endoplasmic reticulum stress and the inflammatory basis of metabolic disease. Cell 140 (2010), 900–917.
49. Hotamisligil, G.S., Inflammation, metaflammation and immunometabolic disorders. Nature 542 (2017), 177–185.
50. Hull, R.L., Kodama, K., Utzschneider, K.M., Carr, D.B., Prigeon, R.L., Kahn, S.E., Dietary-fat-induced obesity in mice results in beta cell hyperplasia but not increased insulin release: evidence for specificity of impaired beta cell adaptation. Diabetologia 48 (2005), 1350–1358.
51. Jablonski, K.A., Amici, S.A., Webb, L.M., Ruiz-Rosado, Jde.D., Popovich, P.G., Partida-Sanchez, S., Guerau-de-Arellano, M., Novel markers to delineate murine M1 and M2 macrophages. PLoS One, 10, 2015, e0145342.
52. Jaguin, M., Fardel, O., Lecureur, V., AhR-dependent secretion of PDGF-BB by human classically activated macrophages exposed to DEP extracts stimulates lung fibroblast proliferation. Toxicol. Appl. Pharmacol. 285 (2015), 170–178.
53. Jakubzick, C., Gautier, E.L., Gibbings, S.L., Sojka, D.K., Schlitzer, A., Johnson, T.E., Ivanov, S., Duan, Q., Bala, S., Condon, T., et al. Minimal differentiation of classical monocytes as they survey steady-state tissues and transport antigen to lymph nodes. Immunity 39 (2013), 599–610.
54. Jenkins, S.J., Ruckerl, D., Cook, P.C., Jones, L.H., Finkelman, F.D., van Rooijen, N., MacDonald, A.S., Allen, J.E., Local macrophage proliferation, rather than recruitment from the blood, is a signature of TH2 inflammation. Science 332 (2011), 1284–1288.
55. Jenkins, S.J., Ruckerl, D., Thomas, G.D., Hewitson, J.P., Duncan, S., Brombacher, F., Maizels, R.M., Hume, D.A., Allen, J.E., IL-4 directly signals tissue-resident macrophages to proliferate beyond homeostatic levels controlled by CSF-1. J. Exp. Med. 210 (2013), 2477–2491.
56. Kamata, K., Mizukami, H., Inaba, W., Tsuboi, K., Tateishi, Y., Yoshida, T., Yagihashi, S., Islet amyloid with macrophage migration correlates with augmented β-cell deficits in type 2 diabetic patients. Amyloid 21 (2014), 191–201.
57. Kratz, M., Coats, B.R., Hisert, K.B., Hagman, D., Mutskov, V., Peris, E., Schoenfelt, K.Q., Kuzma, J.N., Larson, I., Billing, P.S., et al. Metabolic dysfunction drives a mechanistically distinct proinflammatory phenotype in adipose tissue macrophages. Cell Metab. 20 (2014), 614–625.
58. Lackey, D.E., Olefsky, J.M., Regulation of metabolism by the innate immune system. Nat. Rev. Endocrinol. 12 (2016), 15–28.
59. Lavin, Y., Winter, D., Blecher-Gonen, R., David, E., Keren-Shaul, H., Merad, M., Jung, S., Amit, I., Tissue-resident macrophage enhancer landscapes are shaped by the local microenvironment. Cell 159 (2014), 1312–1326.
60. Lee, Y.S., Morinaga, H., Kim, J.J., Lagakos, W., Taylor, S., Keshwani, M., Perkins, G., Dong, H., Kayali, A.G., Sweet, I.R., Olefsky, J., The fractalkine/CX3CR1 system regulates β cell function and insulin secretion. Cell 153 (2013), 413–425.
61. Lee, Y.S., Wollam, J., Olefsky, J.M., An integrated view of immunometabolism. Cell 172 (2018), 22–40.
62. Levitt, H.E., Cyphert, T.J., Pascoe, J.L., Hollern, D.A., Abraham, N., Lundell, R.J., Rosa, T., Romano, L.C., Zou, B., O'Donnell, C.P., et al. Glucose stimulates human beta cell replication in vivo in islets transplanted into NOD-severe combined immunodeficiency (SCID) mice. Diabetologia 54 (2011), 572–582.
63. Li, P., Lu, M., Nguyen, M.T., Bae, E.J., Chapman, J., Feng, D., Hawkins, M., Pessin, J.E., Sears, D.D., Nguyen, A.K., et al. Functional heterogeneity of CD11c-positive adipose tissue macrophages in diet-induced obese mice. J. Biol. Chem. 285 (2010), 15333–15345.
64. Li, P., Oh, D.Y., Bandyopadhyay, G., Lagakos, W.S., Talukdar, S., Osborn, O., Johnson, A., Chung, H., Maris, M., Ofrecio, J.M., et al. LTB4 promotes insulin resistance in obese mice by acting on macrophages, hepatocytes and myocytes. Nat. Med. 21 (2015), 239–247.
65. Lumeng, C.N., DelProposto, J.B., Westcott, D.J., Saltiel, A.R., Phenotypic switching of adipose tissue macrophages with obesity is generated by spatiotemporal differences in macrophage subtypes. Diabetes 57 (2008), 3239–3246.
66. Maedler, K., Schumann, D.M., Sauter, N., Ellingsgaard, H., Bosco, D., Baertschiger, R., Iwakura, Y., Oberholzer, J., Wollheim, C.B., Gauthier, B.R., Donath, M.Y., Low concentration of interleukin-1beta induces FLICE-inhibitory protein-mediated beta-cell proliferation in human pancreatic islets. Diabetes 55 (2006), 2713–2722.
67. Mass, E., Ballesteros, I., Farlik, M., Halbritter, F., Günther, P., Crozet, L., Jacome-Galarza, C.E., Händler, K., Klughammer, J., Kobayashi, Y., et al. Specification of tissue-resident macrophages during organogenesis. Science, 353, 2016, aaf4238.
68. Masters, S.L., Dunne, A., Subramanian, S.L., Hull, R.L., Tannahill, G.M., Sharp, F.A., Becker, C., Franchi, L., Yoshihara, E., Chen, Z., et al. Activation of the NLRP3 inflammasome by islet amyloid polypeptide provides a mechanism for enhanced IL-1β in type 2 diabetes. Nat. Immunol. 11 (2010), 897–904.
69. Mathis, D., Immunological goings-on in visceral adipose tissue. Cell Metab. 17 (2013), 851–859.
70. McLaughlin, T., Ackerman, S.E., Shen, L., Engleman, E., Role of innate and adaptive immunity in obesity-associated metabolic disease. J. Clin. Invest. 127 (2017), 5–13.
71. Medzhitov, R., Origin and physiological roles of inflammation. Nature 454 (2008), 428–435.
72. Meier, D.T., Morcos, M., Samarasekera, T., Zraika, S., Hull, R.L., Kahn, S.E., Islet amyloid formation is an important determinant for inducing islet inflammation in high-fat-fed human IAPP transgenic mice. Diabetologia 57 (2014), 1884–1888.
73. Meredith, M.M., Liu, K., Kamphorst, A.O., Idoyaga, J., Yamane, A., Guermonprez, P., Rihn, S., Yao, K.H., Silva, I.T., Oliveira, T.Y., et al. Zinc finger transcription factor zDC is a negative regulator required to prevent activation of classical dendritic cells in the steady state. J. Exp. Med. 209 (2012), 1583–1593.
74. Miller, J.C., Brown, B.D., Shay, T., Gautier, E.L., Jojic, V., Cohain, A., Pandey, G., Leboeuf, M., Elpek, K.G., Helft, J., et al., Immunological Genome Consortium. Deciphering the transcriptional network of the dendritic cell lineage. Nat. Immunol. 13 (2012), 888–899.
75. Miyazaki, J., Araki, K., Yamato, E., Ikegami, H., Asano, T., Shibasaki, Y., Oka, Y., Yamamura, K., Establishment of a pancreatic beta cell line that retains glucose-inducible insulin secretion: special reference to expression of glucose transporter isoforms. Endocrinology 127 (1990), 126–132.
76. Moreno, S.G., Depleting macrophages in vivo with clodronate-liposomes. Methods Mol. Biol. 1784 (2018), 259–262.
77. Mosser, R.E., Maulis, M.F., Moullé V.S., Dunn, J.C., Carboneau, B.A., Arasi, K., Pappan, K., Poitout, V., Gannon, M., High-fat diet-induced β-cell proliferation occurs prior to insulin resistance in C57Bl/6J male mice. Am. J. Physiol. Endocrinol. Metab. 308 (2015), E573–E582.
78. Murray, P.J., Macrophage polarization. Annu. Rev. Physiol. 79 (2017), 541–566.
79. Murray, P.J., Wynn, T.A., Protective and pathogenic functions of macrophage subsets. Nat. Rev. Immunol. 11 (2011), 723–737.
80. Nackiewicz, D., Dan, M., He, W., Kim, R., Salmi, A., Rütti, S., Westwell-Roper, C., Cunningham, A., Speck, M., Schuster-Klein, C., et al. TLR2/6 and TLR4-activated macrophages contribute to islet inflammation and impair beta cell insulin gene expression via IL-1 and IL-6. Diabetologia 57 (2014), 1645–1654.
81. Naphade, S., Sharma, J., Gaide Chevronnay, H.P., Shook, M.A., Yeagy, B.A., Rocca, C.J., Ur, S.N., Lau, A.J., Courtoy, P.J., Cherqui, S., Brief reports: Lysosomal cross-correction by hematopoietic stem cell-derived macrophages via tunneling nanotubes. Stem Cells 33 (2015), 301–309.
82. Nawaz, M., Fatima, F., Extracellular vesicles, tunneling nanotubes, and cellular interplay: synergies and missing links. Front. Mol. Biosci., 4, 2017, 50.
83. Okabe, M., Ikawa, M., Kominami, K., Nakanishi, T., Nishimune, Y., ‘Green mice’ as a source of ubiquitous green cells. FEBS Lett. 407 (1997), 313–319.
84. Onogi, Y., Wada, T., Kamiya, C., Inata, K., Matsuzawa, T., Inaba, Y., Kimura, K., Inoue, H., Yamamoto, S., Ishii, Y., et al. PDGFRβ regulates adipose tissue expansion and glucose metabolism via vascular remodeling in diet-induced obesity. Diabetes 66 (2017), 1008–1021.
85. Palmer, J.P., Hampe, C.S., Chiu, H., Goel, A., Brooks-Worrell, B.M., Is latent autoimmune diabetes in adults distinct from type 1 diabetes or just type 1 diabetes at an older age?. Diabetes 54:Suppl 2 (2005), S62–S67.
86. Patsouris, D., Li, P.P., Thapar, D., Chapman, J., Olefsky, J.M., Neels, J.G., Ablation of CD11c-positive cells normalizes insulin sensitivity in obese insulin resistant animals. Cell Metab. 8 (2008), 301–309.
87. Peyot, M.L., Pepin, E., Lamontagne, J., Latour, M.G., Zarrouki, B., Lussier, R., Pineda, M., Jetton, T.L., Madiraju, S.R., Joly, E., Prentki, M., Beta-cell failure in diet-induced obese mice stratified according to body weight gain: secretory dysfunction and altered islet lipid metabolism without steatosis or reduced beta-cell mass. Diabetes 59 (2010), 2178–2187.
88. Picelli, S., Björklund, A.K., Faridani, O.R., Sagasser, S., Winberg, G., Sandberg, R., Smart-seq2 for sensitive full-length transcriptome profiling in single cells. Nat. Methods 10 (2013), 1096–1098.
89. Pirzgalska, R.M., Seixas, E., Seidman, J.S., Link, V.M., Sánchez, N.M., Mahú I., Mendes, R., Gres, V., Kubasova, N., Morris, I., et al. Sympathetic neuron-associated macrophages contribute to obesity by importing and metabolizing norepinephrine. Nat. Med. 23 (2017), 1309–1318.
90. Porat, S., Weinberg-Corem, N., Tornovsky-Babaey, S., Schyr-Ben-Haroush, R., Hija, A., Stolovich-Rain, M., Dadon, D., Granot, Z., Ben-Hur, V., White, P., et al. Control of pancreatic β cell regeneration by glucose metabolism. Cell Metab. 13 (2011), 440–449.
91. Richardson, S.J., Willcox, A., Bone, A.J., Foulis, A.K., Morgan, N.G., Islet-associated macrophages in type 2 diabetes. Diabetologia 52 (2009), 1686–1688.
92. Riley, K.G., Pasek, R.C., Maulis, M.F., Dunn, J.C., Bolus, W.R., Kendall, P.L., Hasty, A.H., Gannon, M., Macrophages are essential for CTGF-mediated adult β-cell proliferation after injury. Mol. Metab. 4 (2015), 584–591.
93. Robertson, R.P., Beta-cell deterioration during diabetes: what's in the gun?. Trends Endocrinol. Metab. 20 (2009), 388–393.
94. Rocca, C.J., Goodman, S.M., Dulin, J.N., Haquang, J.H., Gertsman, I., Blondelle, J., Smith, J.L.M., Heyser, C.J., Cherqui, S., Transplantation of wild-type mouse hematopoietic stem and progenitor cells ameliorates deficits in a mouse model of Friedreich's ataxia. Sci. Transl. Med., 9, 2017, eaaj2347.
95. Saederup, N., Cardona, A.E., Croft, K., Mizutani, M., Cotleur, A.C., Tsou, C.L., Ransohoff, R.M., Charo, I.F., Selective chemokine receptor usage by central nervous system myeloid cells in CCR2-red fluorescent protein knock-in mice. PLoS ONE, 5, 2010, e13693.
96. Satpathy, A.T., Kc, W., Albring, J.C., Edelson, B.T., Kretzer, N.M., Bhattacharya, D., Murphy, T.L., Murphy, K.M., Zbtb46 expression distinguishes classical dendritic cells and their committed progenitors from other immune lineages. J. Exp. Med. 209 (2012), 1135–1152.
97. Sell, H., Habich, C., Eckel, J., Adaptive immunity in obesity and insulin resistance. Nat. Rev. Endocrinol. 8 (2012), 709–716.
98. Shalapour, S., Karin, M., Immunity, inflammation, and cancer: an eternal fight between good and evil. J. Clin. Invest. 125 (2015), 3347–3355.
99. Shimokado, K., Raines, E.W., Madtes, D.K., Barrett, T.B., Benditt, E.P., Ross, R., A significant part of macrophage-derived growth factor consists of at least two forms of PDGF. Cell 43 (1985), 277–286.
100. Stamateris, R.E., Sharma, R.B., Hollern, D.A., Alonso, L.C., Adaptive β-cell proliferation increases early in high-fat feeding in mice, concurrent with metabolic changes, with induction of islet cyclin D2 expression. Am. J. Physiol. Endocrinol. Metab. 305 (2013), E149–E159.
101. Talchai, C., Lin, H.V., Kitamura, T., Accili, D., Genetic and biochemical pathways of beta-cell failure in type 2 diabetes. Diabetes Obes. Metab. 11:Suppl 4 (2009), 38–45.
102. Talchai, C., Xuan, S., Lin, H.V., Sussel, L., Accili, D., Pancreatic β cell dedifferentiation as a mechanism of diabetic β cell failure. Cell 150 (2012), 1223–1234.
103. Tardelli, M., Zeyda, K., Moreno-Viedma, V., Wanko, B., Grün, N.G., Staffler, G., Zeyda, M., Stulnig, T.M., Osteopontin is a key player for local adipose tissue macrophage proliferation in obesity. Mol. Metab. 5 (2016), 1131–1137.
104. Thorel, F., Népote, V., Avril, I., Kohno, K., Desgraz, R., Chera, S., Herrera, P.L., Conversion of adult pancreatic alpha-cells to beta-cells after extreme beta-cell loss. Nature 464 (2010), 1149–1154.
105. Thornley, T.B., Agarwal, K.A., Kyriazis, P., Ma, L., Chipashvili, V., Aker, J.E., Korniotis, S., Csizmadia, E., Strom, T.B., Koulmanda, M., Contrasting roles of islet resident immunoregulatory macrophages and dendritic cells in experimental autoimmune Type 1 Diabetes. PLoS One, 11, 2016, e0150792.
106. Tripathi, S., Pohl, M.O., Zhou, Y., Rodriguez-Frandsen, A., Wang, G., Stein, D.A., Moulton, H.M., DeJesus, P., Che, J., Mulder, L.C., et al. Meta- and orthogonal integration of influenza “OMICs” data defines a role for UBR4 in virus budding. Cell Host Microbe 18 (2015), 723–735.
107. Vomund, A.N., Zinselmeyer, B.H., Hughes, J., Calderon, B., Valderrama, C., Ferris, S.T., Wan, X., Kanekura, K., Carrero, J.A., Urano, F., Unanue, E.R., Beta cells transfer vesicles containing insulin to phagocytes for presentation to T cells. Proc. Natl. Acad. Sci. USA 112 (2015), E5496–E5502.
108. Weisberg, S.P., Hunter, D., Huber, R., Lemieux, J., Slaymaker, S., Vaddi, K., Charo, I., Leibel, R.L., Ferrante, A.W. Jr., CCR2 modulates inflammatory and metabolic effects of high-fat feeding. J. Clin. Invest. 116 (2006), 115–124.
109. Westwell-Roper, C.Y., Ehses, J.A., Verchere, C.B., Resident macrophages mediate islet amyloid polypeptide-induced islet IL-1β production and β-cell dysfunction. Diabetes 63 (2014), 1698–1711.
110. Xiao, X., Gaffar, I., Guo, P., Wiersch, J., Fischbach, S., Peirish, L., Song, Z., El-Gohary, Y., Prasadan, K., Shiota, C., Gittes, G.K., M2 macrophages promote beta-cell proliferation by up-regulation of SMAD7. Proc. Natl. Acad. Sci. USA 111 (2014), E1211–E1220.
111. Yona, S., Kim, K.W., Wolf, Y., Mildner, A., Varol, D., Breker, M., Strauss-Ayali, D., Viukov, S., Guilliams, M., Misharin, A., et al. Fate mapping reveals origins and dynamics of monocytes and tissue macrophages under homeostasis. Immunity 38 (2013), 79–91.
112. Zhou, X., Franklin, R.A., Adler, M., Jacox, J.B., Bailis, W., Shyer, J.A., Flavell, R.A., Mayo, A., Alon, U., Medzhitov, R., Circuit design features of a stable two-cell system. Cell 172 (2018), 744–757.
113. Zinselmeyer, B.H., Vomund, A.N., Saunders, B.T., Johnson, M.W., Carrero, J.A., Unanue, E.R., The resident macrophages in murine pancreatic islets are constantly probing their local environment, capturing beta cell granules and blood particles. Diabetologia 61 (2018), 1374–1383.