Hematopoietic Kit Deficiency, rather than Lack of Mast Cells, Protects Mice from Obesity and Insulin Resistance

Cell Metabolism

Volumn 21, Issue 5, 2015, Pages 678-691

  Gutierrez, Dario A ^a   Muralidhar, Sathya ^a   Feyerabend, Thorsten B ^a   Herzig, Stephan ^b   Rodewald, Hans Reimer ^a  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FEMALE; GENETIC BACKGROUND; HEMATOPOIETIC SYSTEM; IMMUNOPATHOLOGY; IMMUNOREGULATION; INSULIN RESISTANCE; MALE; MAST CELL; METABOLIC SYNDROME X; MOUSE; MOUSE STRAIN; NONHUMAN; OBESITY; PRIORITY JOURNAL; WEIGHT GAIN; ANIMAL; C57BL MOUSE; GENE DELETION; GENETICS; HEMATOPOIESIS; IMMUNOLOGY; METABOLISM; PATHOLOGY;

STEM CELL FACTOR; TRANSCRIPTOME;

ANIMALS; GENE DELETION; HEMATOPOIESIS; INSULIN RESISTANCE; MALE; MAST CELLS; METABOLIC SYNDROME X; MICE; MICE, INBRED C57BL; OBESITY; STEM CELL FACTOR; TRANSCRIPTOME;

EID: 84940197047     PISSN: 15504131     EISSN: 19327420     Source Type: Journal    
DOI: 10.1016/j.cmet.2015.04.013     Document Type: Article

References (51)

1. Altintas, M.M., Azad, A., Nayer, B., Contreras, G., Zaias, J., Faul, C., Reiser, J., Nayer, A., Mast cells, macrophages, and crown-like structures distinguish subcutaneous from visceral fat in mice. J. Lipid Res. 52 (2011), 480–488.
2. Antsiferova, M., Martin, C., Huber, M., Feyerabend, T.B., Förster, A., Hartmann, K., Rodewald, H.R., Hohl, D., Werner, S., Mast cells are dispensable for normal and activin-promoted wound healing and skin carcinogenesis. J. Immunol. 191 (2013), 6147–6155.
3. Chappaz, S., Gärtner, C., Rodewald, H.R., Finke, D., Kit ligand and Il7 differentially regulate Peyer's patch and lymph node development. J. Immunol. 185 (2010), 3514–3519.
4. Divoux, A., Moutel, S., Poitou, C., Lacasa, D., Veyrie, N., Aissat, A., Arock, M., Guerre-Millo, M., Clément, K., Mast cells in human adipose tissue: link with morbid obesity, inflammatory status, and diabetes. J. Clin. Endocrinol. Metab. 97 (2012), E1677–E1685.
5. Dudeck, A., Dudeck, J., Scholten, J., Petzold, A., Surianarayanan, S., Köhler, A., Peschke, K., Vöhringer, D., Waskow, C., Krieg, T., et al. Mast cells are key promoters of contact allergy that mediate the adjuvant effects of haptens. Immunity 34 (2011), 973–984.
6. Eheim, A., Medrikova, D., Herzig, S., Immune cells and metabolic dysfunction. Semin. Immunopathol. 36 (2014), 13–25.
7. Feng, Z.C., Li, J., Turco, B.A., Riopel, M., Yee, S.P., Wang, R., Critical role of c-Kit in beta cell function: increased insulin secretion and protection against diabetes in a mouse model. Diabetologia 55 (2012), 2214–2225.
8. Feyerabend, T.B., Weiser, A., Tietz, A., Stassen, M., Harris, N., Kopf, M., Radermacher, P., Möller, P., Benoist, C., Mathis, D., et al. Cre-mediated cell ablation contests mast cell contribution in models of antibody- and T cell-mediated autoimmunity. Immunity 35 (2011), 832–844.
9. Gomez-Pinilla, P.J., Farro, G., Di Giovangiulio, M., Stakenborg, N., Némethova, A., de Vries, A., Liston, A., Feyerabend, T.B., Rodewald, H.R., Boeckxstaens, G.E., Matteoli, G., Mast cells play no role in the pathogenesis of postoperative ileus induced by intestinal manipulation. PLoS ONE, 9, 2014, e85304.
10. Gordon, J.R., Galli, S.J., Mast cells as a source of both preformed and immunologically inducible TNF-alpha/cachectin. Nature 346 (1990), 274–276.
11. Grimbaldeston, M.A., Chen, C.C., Piliponsky, A.M., Tsai, M., Tam, S.Y., Galli, S.J., 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 (2005), 835–848.
12. Gutierrez, D.A., Fu, W., Schonefeldt, S., Feyerabend, T.B., Ortiz-Lopez, A., Lampi, Y., Liston, A., Mathis, D., Rodewald, H.R., Type 1 diabetes in NOD mice unaffected by mast cell deficiency. Diabetes 63 (2014), 3827–3834.
13. Hill, A.A., Reid Bolus, W., Hasty, A.H., A decade of progress in adipose tissue macrophage biology. Immunol. Rev. 262 (2014), 134–152.
14. Hotamisligil, G.S., Erbay, E., Nutrient sensing and inflammation in metabolic diseases. Nat. Rev. Immunol. 8 (2008), 923–934.
15. Hotamisligil, G.S., Arner, P., Caro, J.F., Atkinson, R.L., Spiegelman, B.M., Increased adipose tissue expression of tumor necrosis factor-alpha in human obesity and insulin resistance. J. Clin. Invest. 95 (1995), 2409–2415.
16. Huizinga, J.D., Thuneberg, L., Klüppel, M., Malysz, J., Mikkelsen, H.B., Bernstein, A., W/kit gene required for interstitial cells of Cajal and for intestinal pacemaker activity. Nature 373 (1995), 347–349.
17. Ishii, S., Tsuji, S., Tsujii, M., Nishida, T., Watabe, K., Iijima, H., Takehara, T., Kawano, S., Hayashi, N., Restoration of gut motility in Kit-deficient mice by bone marrow transplantation. J. Gastroenterol. 44 (2009), 834–841.
18. Katz, H.R., Austen, K.F., Mast cell deficiency, a game of kit and mouse. Immunity 35 (2011), 668–670.
19. Kawakami, T., A crucial door to the mast cell mystery knocked in. J. Immunol. 183 (2009), 6861–6862.
20. Kiss, E.A., Vonarbourg, C., Kopfmann, S., Hobeika, E., Finke, D., Esser, C., Diefenbach, A., Natural aryl hydrocarbon receptor ligands control organogenesis of intestinal lymphoid follicles. Science 334 (2011), 1561–1565.
21. Kitamura, Y., Yokoyama, M., Matsuda, H., Shimada, M., Coincidental development of forestomach papilloma and prepyloric ulcer in nontreated mutant mice of W/Wv and SI/SId genotypes. Cancer Res. 40 (1980), 3392–3397.
22. Liu, J., Divoux, A., Sun, J., Zhang, J., Clément, K., Glickman, J.N., Sukhova, G.K., Wolters, P.J., Du, J., Gorgun, C.Z., et al. Genetic deficiency and pharmacological stabilization of mast cells reduce diet-induced obesity and diabetes in mice. Nat. Med. 15 (2009), 940–945.
23. Maeda, H., Yamagata, A., Nishikawa, S., Yoshinaga, K., Kobayashi, S., Nishi, K., Nishikawa, S., Requirement of c-kit for development of intestinal pacemaker system. Development 116 (1992), 369–375.
24. Magnol, L., Chevallier, M.C., Nalesso, V., Retif, S., Fuchs, H., Klempt, M., Pereira, P., Riottot, M., Andrzejewski, S., Doan, B.T., et al. KIT is required for hepatic function during mouse post-natal development. BMC Dev. Biol., 7, 2007, 81.
25. Mathis, D., Immunological goings-on in visceral adipose tissue. Cell Metab. 17 (2013), 851–859.
26. McNelis, J.C., Olefsky, J.M., Macrophages, immunity, and metabolic disease. Immunity 41 (2014), 36–48.
27. Michel, A., Schüler, A., Friedrich, P., Döner, F., Bopp, T., Radsak, M., Hoffmann, M., Relle, M., Distler, U., Kuharev, J., et al. Mast cell-deficient Kit(W-sh) “Sash” mutant mice display aberrant myelopoiesis leading to the accumulation of splenocytes that act as myeloid-derived suppressor cells. J. Immunol. 190 (2013), 5534–5544.
28. Milenkovic, N., Frahm, C., Gassmann, M., Griffel, C., Erdmann, B., Birchmeier, C., Lewin, G.R., Garratt, A.N., Nociceptive tuning by stem cell factor/c-Kit signaling. Neuron 56 (2007), 893–906.
29. Mraz, M., Haluzik, M., The role of adipose tissue immune cells in obesity and low-grade inflammation. J. Endocrinol. 222 (2014), R113–R127.
30. Nakano, T., Sonoda, T., Hayashi, C., Yamatodani, A., Kanayama, Y., Yamamura, T., Asai, H., Yonezawa, T., Kitamura, Y., Galli, S.J., Fate of bone marrow-derived cultured mast cells after intracutaneous, intraperitoneal, and intravenous transfer into genetically mast cell-deficient W/Wv mice. Evidence that cultured mast cells can give rise to both connective tissue type and mucosal mast cells. J. Exp. Med. 162 (1985), 1025–1043.
31. Nigrovic, P.A., Gray, D.H., Jones, T., Hallgren, J., Kuo, F.C., Chaletzky, B., Gurish, M., Mathis, D., Benoist, C., Lee, D.M., Genetic inversion in mast cell-deficient (Wsh) mice interrupts corin and manifests as hematopoietic and cardiac aberrancy. Am. J. Pathol. 173 (2008), 1693–1701.
32. Oka, T., Kalesnikoff, J., Starkl, P., Tsai, M., Galli, S.J., Evidence questioning cromolyn's effectiveness and selectivity as a ‘mast cell stabilizer’ in mice. Lab. Invest. 92 (2012), 1472–1482.
33. Peschke, K., Dudeck, A., Rabenhorst, A., Hartmann, K., Roers, A., Cre/loxP-based mouse models of mast cell deficiency and mast cell-specific gene inactivation. Methods Mol. Biol. 1220 (2015), 403–421.
34. Piconese, S., Costanza, M., Musio, S., Tripodo, C., Poliani, P.L., Gri, G., Burocchi, A., Pittoni, P., Gorzanelli, A., Colombo, M.P., Pedotti, R., Exacerbated experimental autoimmune encephalomyelitis in mast-cell-deficient Kit W-sh/W-sh mice. Lab. Invest. 91 (2011), 627–641.
35. Puddington, L., Olson, S., Lefrançois, L., Interactions between stem cell factor and c-Kit are required for intestinal immune system homeostasis. Immunity 1 (1994), 733–739.
36. Reber, L.L., Marichal, T., Galli, S.J., New models for analyzing mast cell functions in vivo. Trends Immunol. 33 (2012), 613–625.
37. Rodewald, H.R., Feyerabend, T.B., Widespread immunological functions of mast cells: fact or fiction?. Immunity 37 (2012), 13–24.
38. Russell, E.S., Hereditary anemias of the mouse: a review for geneticists. Adv. Genet. 20 (1979), 357–459.
39. Schönhuber, N., Seidler, B., Schuck, K., Veltkamp, C., Schachtler, C., Zukowska, M., Eser, S., Feyerabend, T.B., Paul, M.C., Eser, P., et al. A next-generation dual-recombinase system for time- and host-specific targeting of pancreatic cancer. Nat. Med. 20 (2014), 1340–1347.
40. Sergeant, G.P., Large, R.J., Beckett, E.A., McGeough, C.M., Ward, S.M., Horowitz, B., Microarray comparison of normal and W/Wv mice in the gastric fundus indicates a supersensitive phenotype. Physiol. Genomics 11 (2002), 1–9.
41. Shimada, M., Kitamura, Y., Yokoyama, M., Miyano, Y., Maeyama, K., Yamatodani, A., Takahashi, Y., Tatsuta, M., Spontaneous stomach ulcer in genetically mast-cell depleted W/Wv mice. Nature 283 (1980), 662–664.
42. Takagi, K., Okuda-Ashitaka, E., Mabuchi, T., Katano, T., Ohnishi, T., Matsumura, S., Ohnaka, M., Kaneko, S., Abe, T., Hirata, T., et al. Involvement of stem cell factor and its receptor tyrosine kinase c-kit in pain regulation. Neuroscience 153 (2008), 1278–1288.
43. Tanaka, A., Nomura, Y., Matsuda, A., Ohmori, K., Matsuda, H., Mast cells function as an alternative modulator of adipogenesis through 15-deoxy-delta-12, 14-prostaglandin J2. Am. J. Physiol. Cell Physiol. 301 (2011), C1360–C1367.
44. Uysal, K.T., Wiesbrock, S.M., Marino, M.W., Hotamisligil, G.S., Protection from obesity-induced insulin resistance in mice lacking TNF-alpha function. Nature 389 (1997), 610–614.
45. Wang, J., Shi, G.P., Mast cell stabilization: novel medication for obesity and diabetes. Diabetes Metab. Res. Rev. 27 (2011), 919–924.
46. Wang, J., Sjöberg, S., Tia, V., Secco, B., Chen, H., Yang, M., Sukhova, G.K., Shi, G.P., Pharmaceutical stabilization of mast cells attenuates experimental atherogenesis in low-density lipoprotein receptor-deficient mice. Atherosclerosis 229 (2013), 304–309.
47. Waskow, C., Rodewald, H.R., Lymphocyte development in neonatal and adult c-Kit-deficient (c-KitW/W) mice. Adv. Exp. Med. Biol. 512 (2002), 1–10.
48. Waskow, C., Paul, S., Haller, C., Gassmann, M., Rodewald, H.R., Viable c-Kit(W/W) mutants reveal pivotal role for c-kit in the maintenance of lymphopoiesis. Immunity 17 (2002), 277–288.
49. Waskow, C., Madan, V., Bartels, S., Costa, C., Blasig, R., Rodewald, H.R., Hematopoietic stem cell transplantation without irradiation. Nat. Methods 6 (2009), 267–269.
50. Willenborg, S., Eckes, B., Brinckmann, J., Krieg, T., Waisman, A., Hartmann, K., Roers, A., Eming, S.A., Genetic ablation of mast cells redefines the role of mast cells in skin wound healing and bleomycin-induced fibrosis. J. Invest. Dermatol. 134 (2014), 2005–2015.
51. Zhou, J.S., Xing, W., Friend, D.S., Austen, K.F., Katz, H.R., Mast cell deficiency in Kit(W-sh) mice does not impair antibody-mediated arthritis. J. Exp. Med. 204 (2007), 2797–2802.