Differences in hematopoietic stem cells contribute to sexually dimorphic inflammatory responses to high fat diet-induced obesity

Journal of Biological Chemistry

Volumn 290, Issue 21, 2015, Pages 13250-13262

  Singer, Kanakadurga ^a,d   Maley, Nidhi ^a   Mergian, Taleen ^a   DelProposto, Jennifer ^a   Cho, Kae Won ^b   Zamarron, Brian F ^a   Martinez Santibanez, Gabriel ^a   Geletka, Lynn ^a   Muir, Lindsey ^a   Wachowiak, Phillip ^c   Demirjian, Chaghig ^c   Lumeng, Carey N ^a,c  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b Soonchunhyang University   (South Korea)

^c UNIVERSITY OF MICHIGAN   (United States)

^d Department of Obstetrics and Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELLS; CHEMICAL ACTIVATION; CYTOLOGY; MACROPHAGES; MAMMALS; METABOLISM; STEM CELLS; TISSUE;

ADIPOCYTE HYPERTROPHY; BONE MARROW TRANSPLANT; GLUCOSE METABOLISM; HEMATOPOIETIC CELL; HEMATOPOIETIC STEM CELLS; INFLAMMATORY RESPONSE; METABOLIC DISEASE; POSTMENOPAUSAL WOMEN;

NUTRITION;

GLUCOSE; BIOLOGICAL MARKER; GLUCOSE BLOOD LEVEL; LIPID;

ADIPOCYTE; ADIPOSE TISSUE; ARTICLE; CELL ACTIVATION; CONTROLLED STUDY; FEMALE; GLUCOSE METABOLISM; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; INFLAMMATION; LEUKOCYTE; LEUKOCYTE ACTIVATION; LIPID DIET; MACROPHAGE; MALE; MOUSE; NONHUMAN; OBESITY; PRIORITY JOURNAL; SEX DIFFERENCE; WEIGHT GAIN; ADVERSE EFFECTS; ANIMAL; C57BL MOUSE; CELL CULTURE; CFU COUNTING; COMPLICATION; CYTOLOGY; FLOW CYTOMETRY; GLUCOSE BLOOD LEVEL; GLUCOSE TOLERANCE TEST; IMMUNOHISTOCHEMISTRY; IMMUNOLOGY; METABOLISM; MYELOPOIESIS; PATHOLOGY; PHYSIOLOGY;

MUS; RODENTIA;

ADIPOSE TISSUE; ANIMALS; BIOMARKERS; BLOOD GLUCOSE; CELLS, CULTURED; COLONY-FORMING UNITS ASSAY; DIET, HIGH-FAT; FEMALE; FLOW CYTOMETRY; GLUCOSE TOLERANCE TEST; HEMATOPOIETIC STEM CELLS; IMMUNOHISTOCHEMISTRY; INFLAMMATION; LIPIDS; MALE; MICE; MICE, INBRED C57BL; MYELOPOIESIS; OBESITY; SEX FACTORS; WEIGHT GAIN;

EID: 84930002072     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.634568     Document Type: Article

References (43)

1. Meyer, M. R., Haas, E., and Barton, M. (2006) Gender differences of cardiovascular disease: new perspectives for estrogen receptor signaling. Hypertension 47, 1019-1026
2. Barrett-Connor, E. (2009) Women and heart disease: neglected directions for future research. J. Cardiovasc. Transl. Res. 2, 256-257
3. Karastergiou, K., Smith, S. R., Greenberg, A. S., and Fried, S. K. (2012) Sex differences in human adipose tissues: the biology of pear shape. Biol. Sex Differ. 3, 13
4. Gregor, M. F., and Hotamisligil, G. S. (2011) Inflammatory mechanisms in obesity. Ann. Rev. Immunol. 29, 415-445
5. Olefsky, J. M., and Glass, C. K. (2010) Macrophages, inflammation, and insulin resistance. Annu. Rev. Physiol. 72, 219-246
6. Singer, K., DelProposto, J., Morris, D. L., Zamarron, B., Mergian, T., Maley, N., Cho, K. W., Geletka, L., Subbaiah, P., Muir, L., Martinez-Santibanez, G., and Lumeng, C. N. (2014) Diet-induced obesity promotes myelopoiesis in hematopoietic stem cells. Mol. Metab. 3, 664-675
7. Nagareddy, P. R., Kraakman, M., Masters, S. L., Stirzaker, R. A., Gorman, D. J., Grant, R. W., Dragoljevic, D., Hong, E. S., Abdel-Latif, A., Smyth, S. S., Choi, S. H., Korner, J., Bornfeldt, K. E., Fisher, E. A., Dixit, V. D., Tall, A. R., Goldberg, I. J., and Murphy, A. J. (2014) Adipose tissue macrophages promote myelopoiesis and monocytosis in obesity. Cell Metab. 19, 821-835
8. Nagareddy, P. R., Murphy, A. J., Stirzaker, R. A., Hu, Y., Yu, S., Miller, R. G., Ramkhelawon, B., Distel, E., Westerterp, M., Huang, L. S., Schmidt, A. M., Orchard, T. J., Fisher, E. A., Tall, A. R., and Goldberg, I. J. (2013) Hyperglycemia promotes myelopoiesis and impairs the resolution of atherosclerosis. Cell Metab. 17, 695-708
9. Weisberg, S. P., Hunter, D., Huber, R., Lemieux, J., Slaymaker, S., Vaddi, K., Charo, I., Leibel, R. L., and Ferrante, A. W., Jr. (2006) CCR2 modulates inflammatory and metabolic effects of high-fat feeding. J. Clin. Invest. 116, 115-124
10. Westcott, D. J., Delproposto, J. B., Geletka, L. M., Wang, T., Singer, K., Saltiel, A. R., and Lumeng, C. N. (2009) MGL1 promotes adipose tissue inflammation and insulin resistance by regulating 7/4hi monocytes in obesity. J. Exp. Med. 206, 3143-3156
11. Lumeng, C. N., Deyoung, S. M., Bodzin, J. L., and Saltiel, A. R. (2007) Increased inflammatory properties of adipose tissue macrophages recruited during diet-induced obesity. Diabetes 56, 16-23
12. Grove, K. L., Fried, S. K., Greenberg, A. S., Xiao, X. Q., and Clegg, D. J. (2010) A microarray analysis of sexual dimorphism of adipose tissues in high-fat-diet-induced obese mice. Int. J. Obes. 34, 989-1000
13. Nteeba, J., Ortinau, L. C., Perfield, J. W., 2nd, and Keating, A. F. (2013) Diet-induced obesity alters immune cell infiltration and expression of inflammatory cytokine genes in mouse ovarian and peri-ovarian adipose depot tissues. Mol. Reprod. Dev. 80, 948-958
14. Estrany, M. E., Proenza, A. M., Gianotti, M., and Lladó, I. (2013) High-fat diet feeding induces sex-dependent changes in inflammatory and insulin sensitivity profiles of rat adipose tissue. Cell Biochem. Funct. 31, 504-510
15. Pennell, L. M., Galligan, C. L., and Fish, E. N. (2012) Sex affects immunity. J. Autoimmun. 38, J282-291
16. Marriott, I., and Huet-Hudson, Y. M. (2006) Sexual dimorphism in innate immune responses to infectious organisms. Immunol. Res. 34, 177-192
17. Imahara, S. D., Jelacic, S., Junker, C. E., and O'Keefe, G. E. (2005) The influence of gender on human innate immunity. Surgery 138, 275-282
18. Shi, H., Kokoeva, M. V., Inouye, K., Tzameli, I., Yin, H., and Flier, J. S. (2006) TLR4 links innate immunity and fatty acid-induced insulin resistance. J. Clin. Invest. 116, 3015-3025
19. Mukundan, L., Odegaard, J. I., Morel, C. R., Heredia, J. E., Mwangi, J. W., Ricardo-Gonzalez, R. R., Goh, Y. P., Eagle, A. R., Dunn, S. E., Awakuni, J. U., Nguyen, K. D., Steinman, L., Michie, S. A., and Chawla, A. (2009) PPAR-δ senses and orchestrates clearance of apoptotic cells to promote tolerance. Nat. Med. 15, 1266-1272
20. Vandanmagsar, B., Youm, Y. H., Ravussin, A., Galgani, J. E., Stadler, K., Mynatt, R. L., Ravussin, E., Stephens, J. M., and Dixit, V. D. (2011) The NLRP3 inflammasome instigates obesity-induced inflammation and insulin resistance. Nat. Med. 17, 179-188
21. Pratt, G. M., Learn, C. A., Hughes, G. D., Clark, B. L., Warthen, M., and Pories, W. (2009) Demographics and outcomes at American Society for Metabolic and Bariatric Surgery Centers of Excellence. Surg. Endosc. 23, 795-799
22. Morris, D. L., Oatmen, K. E., Wang, T., DelProposto, J. L., and Lumeng, C. N. (2012) CX3CR1 deficiency does not influence trafficking of adipose tissue macrophages in mice with diet-induced obesity. Obesity 20, 1189-1199
23. Lumeng, C. N., DelProposto, J. B., Westcott, D. J., and Saltiel, A. R. (2008) Phenotypic switching of adipose tissue macrophages with obesity is generated by spatiotemporal differences in macrophage subtypes. Diabetes 57, 3239-3246
24. Pronk, C. J., Rossi, D. J., Månsson, R., Attema, J. L., Norddahl, G. L., Chan, C. K., Sigvardsson, M., Weissman, I. L., and Bryder, D. (2007) Elucidation of the phenotypic, functional, and molecular topography of a myeloerythroid progenitor cell hierarchy. Cell Stem Cell 1, 428-442
25. Erickson, J. C., Clegg, K. E., and Palmiter, R. D. (1996) Sensitivity to leptin and susceptibility to seizures of mice lacking neuropeptide Y. Nature 381, 415-421
26. Gautier, E. L., Shay, T., Miller, J., Greter, M., Jakubzick, C., Ivanov, S., Helft, J., Chow, A., Elpek, K. G., Gordonov, S., Mazloom, A. R., Ma'ayan, A., Chua, W. J., Hansen, T. H., Turley, S. J., Merad, M., and Randolph, G. J. (2012) Gene-expression profiles and transcriptional regulatory pathways that underlie the identity and diversity of mouse tissue macrophages. Nat. Immunol. 13, 1118-1128
27. Vander Lugt, B., Tubo, N. J., Nizza, S. T., Boes, M., Malissen, B., Fuhlbrigge, R. C., Kupper, T. S., and Campbell, J. J. (2013) CCR7 plays no appreciable role in trafficking of central memory CD4 T cells to lymph nodes. J. Immunol. 191, 3119-3127
28. Riant, E., Waget, A., Cogo, H., Arnal, J. F., Burcelin, R., and Gourdy, P. (2009) Estrogens protect against high-fat diet-induced insulin resistance and glucose intolerance in mice. Endocrinology 150, 2109-2117
29. Medrikova, D., Jilkova, Z. M., Bardova, K., Janovska, P., Rossmeisl, M., and Kopecky, J. (2012) Sex differences during the course of diet-induced obesity in mice: adipose tissue expandability and glycemic control. Int. J. Obes. 36, 262-272
30. Pettersson, U. S., Waldén, T. B., Carlsson, P. O., Jansson, L., and Phillipson, M. (2012) Female mice are protected against high-fat diet induced metabolic syndrome and increase the regulatory T cell population in adipose tissue. PloS One 7, e46057
31. Whitacre, C. C., Reingold, S. C., and O'Looney, P. A. (1999) A gender gap in autoimmunity. Science 283, 1277-1278
32. Kim, W. K., Choi, E. K., Sul, O. J., Park, Y. K., Kim, E. S., Yu, R., Suh, J. H., and Choi, H. S. (2013) Monocyte chemoattractant protein-1 deficiency attenuates oxidative stress and protects against ovariectomy-induced chronic inflammation in mice. PloS One 8, e72108
33. Marriott, I., Bost, K. L., and Huet-Hudson, Y. M. (2006) Sexual dimorphism in expression of receptors for bacterial lipopolysaccharides in murine macrophages: a possible mechanism for gender-based differences in endotoxic shock susceptibility. J. Reprod. Immunol. 71, 12-27
34. Clayton, J. A., and Collins, F. S. (2014) Policy: NIH to balance sex in cell and animal studies. Nature 509, 282-283
35. Bolego, C., Cignarella, A., Staels, B., and Chinetti-Gbaguidi, G. (2013) Macrophage function and polarization in cardiovascular disease: a role of estrogen signaling? Arterioscler. Thromb. Vasc. Biol. 33, 1127-1134
36. Ribas, V., Drew, B. G., Le, J. A., Soleymani, T., Daraei, P., Sitz, D., Mohammad, L., Henstridge, D. C., Febbraio, M. A., Hewitt, S. C., Korach, K. S., Bensinger, S. J., and Hevener, A. L. (2011) Myeloid-specific estrogen receptor α deficiency impairs metabolic homeostasis and accelerates atherosclerotic lesion development. Proc. Natl. Acad. Sci. U.S.A. 108, 16457-16462
37. Gui, Y., Silha, J. V., and Murphy, L. J. (2004) Sexual dimorphism and regulation of resistin, adiponectin, and leptin expression in the mouse. Obes. Res. 12, 1481-1491
38. Orr, J. S., Puglisi, M. J., Ellacott, K. L., Lumeng, C. N., Wasserman, D. H., and Hasty, A. H. (2012) Toll-like receptor 4 deficiency promotes the alternative activation of adipose tissue macrophages. Diabetes 61, 2718-2727
39. Megís, J., Yáez, A., Moriano, S., O'Connor, J. E., Gozalbo, D., and Gil, M. L. (2012) Direct Toll-like receptor-mediated stimulation of hematopoietic stem and progenitor cells occurs in vivo and promotes differentiation toward macrophages. Stem Cells 30, 1486-1495
40. Calippe, B., Douin-Echinard, V., Delpy, L., Laffargue, M., Lélu, K., Krust, A., Pipy, B., Bayard, F., Arnal, J. F., Guéry, J. C., and Gourdy, P. (2010) 17β-Estradiol promotes TLR4-triggered proinflammatory mediator production through direct estrogen receptor alpha signaling in macrophages in vivo. J. Immunol. 185, 1169-1176
41. Iwasa, T., Matsuzaki, T., Kinouchi, R., Gereltsetseg, G., Murakami, M., Munkhzaya, M., Altankhuu, T., Kuwahara, A., Yasui, T., and Irahara, M. (2014) Changes in central and peripheral inflammatory responses to lipopolysaccharide in ovariectomized female rats. Cytokine 65, 65-73
42. Iwasa, T., Matsuzaki, T., Matsui, S., Munkhzaya, M., Tungalagsuvd, A., Kawami, T., Murakami, M., Kato, T., Kuwahara, A., Yasui, T., and Irahara, M. (2014) The effects of LPS-induced endotoxemia on the expression of adiponectin and its receptors in female rats. Endocr. J. 61, 891-900
43. Finkelstein, J. S., Lee, H., Burnett-Bowie, S. A., Pallais, J. C., Yu, E. W., Borges, L. F., Jones, B. F., Barry, C. V., Wulczyn, K. E., Thomas, B. J., and Leder, B. Z. (2013) Gonadal steroids and body composition, strength, and sexual function in men. N. Engl. J. Med. 369, 1011-1022