High fat diet rapidly suppresses B lymphopoiesis by disrupting the supportive capacity of the bone marrow niche

PLoS ONE

Volumn 9, Issue 3, 2014, Pages

  Adler, Benjamin J ^a   Green, Danielle E ^a   Pagnotti, Gabriel M ^a   Chan, M Ete ^a   Rubin, Clinton T ^a  

^a St Francis Hospital The Heart Center   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; EBF 1 PROTEIN; INTERLEUKIN 7; TRANSCRIPTION FACTOR PAX5; UNCLASSIFIED DRUG;

ABDOMINAL OBESITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; B LYMPHOCYTE; BONE MARROW; C57BL 6 MOUSE; CELL LINEAGE; CONTROLLED STUDY; CYTOKINE RELEASE; EPIDIDYMIS FAT; HEMATOPOIETIC STEM CELL; LIPID DIET; LYMPHOCYTE DIFFERENTIATION; LYMPHOPOIESIS; MALE; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN;

ANIMALS; B-LYMPHOCYTES; BONE MARROW; BONE MARROW CELLS; DIET, HIGH-FAT; LYMPHOPOIESIS; MALE; MICE; MICE, INBRED C57BL;

EID: 84897057783     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0090639     Document Type: Article

References (42)

1. Foudi A, Hochedlinger K, Van Buren D, Schindler JW, Jaenisch R, et al. (2009) Analysis of histone 2B-GFP retention reveals slowly cycling hematopoietic stem cells. Nat Biotechnol 27: 84-90.
2. Kiel MJ, Morrison SJ (2008) Uncertainty in the niches that maintain haematopoietic stem cells. Nat Rev Immunol 8: 290-301. (Pubitemid 351432804)
3. Cheshier SH, Prohaska SS, Weissman IL (2007) The Effect of Bleeding on Hematopoietic Stem Cell Cycling and Self-Renewal. Stem Cells Dev 16: 707- 718.
4. Wilson A, Laurenti E, Oser G, van der Wath RC, Blanco-Bose W, et al. (2008) Hematopoietic Stem Cells Reversibly Switch from Dormancy to Self-Renewal during Homeostasis and Repair. Cell 135: 1118-1129.
5. Kollet O, Dar A, Shivtiel S, Kalinkovich A, Lapid K, et al. (2006) Osteoclasts degrade endosteal components and promote mobilization of hematopoietic progenitor cells. Nat Med 12: 657-664. (Pubitemid 43865234)
6. Gottschling S, Saffrich R, Seckinger A, Krause U, Horsch K, et al. (2007) Human Mesenchymal Stromal Cells Regulate Initial Self-Renewing Divisions of Hematopoietic Progenitor Cells by a β1-Integrin-Dependent Mechanism. Stem Cells 25: 798-806. (Pubitemid 46354240)
7. Tokoyoda K, Egawa T, Sugiyama T, Choi B-I, Nagasawa T (2004) Cellular Niches Controlling B Lymphocyte Behavior within Bone Marrow during Development. Immunity 20: 707-718. (Pubitemid 38757441)
8. Tsapogas P, Zandi S, Åhsberg J, Zetterblad J, Welinder E, et al. (2011) IL-7 mediates Ebf-1-dependent lineage restriction in early lymphoid progenitors. Blood 118: 1283-1290.
9. Wijga A, Scholtens S, Bemelmans W, de Jongste J, Kerkhof M, et al. (2010) Comorbidities of obesity in school children: a cross-sectional study in the PIAMA birth cohort. BMC Public Health 10: 184.
10. Nieman DC, Henson DA, Nehlsen-Cannarella SL, Ekkens M, Utter AC, et al. (1999) Influence of Obesity on Immune Function. J Am Diet Assoc 99: 294-299. (Pubitemid 29186037)
11. Naveiras O, Nardi V, Wenzel PL, Hauschka PV, Fahey F, et al. (2009) Bone-marrow adipocytes as negative regulators of the haematopoietic microenvironment. Nature 460: 259-263.
12. Kajkenova O, Lecka-Czernik B, Gubrij I, Hauser SP, Takahashi K, et al. (1997) Increased Adipogenesis and Myelopoiesis in the Bone Marrow of SAMP6, a Murine Model of Defective Osteoblastogenesis and Low Turnover Osteopenia. J Bone Miner Res 12: 1772-1779. (Pubitemid 27500188)
13. Trudel G, Payne M, Madler B, Ramachandran N, Lecompte M, et al. (2009) Bone marrow fat accumulation after 60 days of bed rest persisted 1 year after activities were resumed along with hemopoietic stimulation: the Women International Space Simulation for Exploration study. J Appl Physiol 107: 540-548.
14. Chan ME, Adler BJ, Green DE, Rubin CT (2012) Bone structure and B-cell populations, crippled by obesity, are partially rescued by brief daily exposure to low-magnitude mechanical signals. FASEB J 26: 4855-4863.
15. Yang H, Youm Y-H, Vandanmagsar B, Ravussin A, Gimble JM, et al. (2010) Obesity Increases the Production of Proinflammatory Mediators from Adipose Tissue T Cells and Compromises TCR Repertoire Diversity: Implications for Systemic Inflammation and Insulin Resistance. J Immunol 185: 1836-1845.
16. Karlsson EA, Sheridan PA, Beck MA (2010) Diet-Induced Obesity in Mice Reduces the Maintenance of Influenza-Specific CD8+ Memory T Cells. J Nutr 140: 1691-1697.
17. Luu YK, Lublinsky S, Ozcivici E, Capilla E, Pessin JE, et al. (2009) In vivo quantification of subcutaneous and visceral adiposity by micro-computed tomography in a small animal model. Med Eng Phys 31: 34-41.
18. Lublinsky S, Luu Y, Rubin C, Judex S (2009) Automated Separation of Visceral and Subcutaneous Adiposity in In Vivo Microcomputed Tomographies of Mice. J Digit Imaging 22: 222-231.
19. Challen GA, Boles N, Lin KK, Goodell MA (2009) Mouse hematopoietic stem cell identification and analysis. Cytometry Part A: the journal of the International Society for Analytical Cytology 75: 14-24.
20. Telford WG, Bradford J, Godfrey W, Robey RW, Bates SE (2007) Side Population Analysis Using a Violet-Excited Cell-Permeable DNA Binding Dye. Stem Cells 25: 1029-1036. (Pubitemid 46572601)
21. Weksberg DC, Chambers SM, Boles NC, Goodell MA (2008) CD150- side population cells represent a functionally distinct population of long-term hematopoietic stem cells. Blood 111: 2444-2451. (Pubitemid 351451458)
22. Noda S, Ichikawa H, Miyoshi H (2009) Hematopoietic stem cell aging is associated with functional decline and delayed cell cycle progression. Biochem Biophys Res Commun 383: 210-215.
23. Biro FM, Wien M (2010) Childhood obesity and adult morbidities. Am J Clin Nutr 91: 1499S-1505.
24. Karlsson EA, Beck MA (2010) The burden of obesity on infectious disease. Exp Biol Med 235: 1412-1424.
25. Dixit VD (2008) Adipose-immune interactions during obesity and caloric restriction: reciprocal mechanisms regulating immunity and health span. J Leukoc Biol 84: 882-892.
26. Smith AG, Sheridan PA, Harp JB, Beck MA (2007) Diet-Induced Obese Mice Have Increased Mortality and Altered Immune Responses When Infected with Influenza Virus. J Nutr 137: 1236-1243. (Pubitemid 46701917)
27. Yang H, Youm Y-H, Vandanmagsar B, Rood J, Kumar KG, et al. (2009) Obesity accelerates thymic aging. Blood 114: 3803-3812.
28. Nishimura S, Manabe I, Nagasaki M, Eto K, Yamashita H, et al. (2009) CD8+ effector T cells contribute to macrophage recruitment and adipose tissue inflammation in obesity. Nat Med 15: 914-920.
29. Györy I, Boller S, Nechanitzky R, Mandel E, Pott S, et al. (2012) Transcription factor Ebf1 regulates differentiation stage-specific signaling, proliferation, and survival of B cells. Genes Dev 26: 668-682.
30. Vilagos B, Hoffmann M, Souabni A, Sun Q, Werner B, et al. (2012) Essential role of EBF1 in the generation and function of distinct mature B cell types. J Exp Med 209: 775-792.
31. Aguila HL, Mun SH, Kalinowski J, Adams DJ, Lorenzo JA, et al. (2012) Osteoblast-specific overexpression of human interleukin-7 rescues the bone mass phenotype of interleukin-7-deficient female mice. J Bone Miner Res 27: 1030-1042.
32. Wu JY, Purton LE, Rodda SJ, Chen M, Weinstein LS, et al. (2008) Osteoblastic regulation of B lymphopoiesis is mediated by Gsα- dependent signaling pathways. Proc Natl Acad Sci U S A 105: 16976-16981.
33. Calvi LM, Adams GB, Weibrecht KW, Weber JM, Olson DP, et al. (2003) Osteoblastic cells regulate the haematopoietic stem cell niche. Nature 425: 841-846. (Pubitemid 37351468)
34. Devlin MJ, Cloutier AM, Thomas NA, Panus DA, Lotinun S, et al. (2010) Caloric restriction leads to high marrow adiposity and low bone mass in growing mice. J Bone Miner Res 25: 2078-2088.
35. Green DE, Adler BJ, Chan ME, Rubin CT (2011) Devastation of adult stem cell pools by irradiation precedes collapse of trabecular bone quality and quantity. J Bone Miner Res: n/a-n/a.
36. Baldridge MT, King KY, Goodell MA (2011) Inflammatory signals regulate hematopoietic stem cells. Trends Immunol 32: 57-65.
37. Singh P, Yao Y, Weliver A, Broxmeyer HE, Hong S-C, et al. (2008) Vaccinia Virus Infection Modulates the Hematopoietic Cell Compartments in the Bone Marrow. Stem Cells 26: 1009-1016.
38. Feng J, Iwama A, Satake M, Kohu K (2009) MicroRNA-27 enhances differentiation of myeloblasts into granulocytes by post-transcriptionally downregulating Runx1. Br J Haematol 145: 412-423.
39. Lemieux ME, Cheng Z, Zhou Q, White R, Cornell J, et al. (2011) Inactivation of a Single Copy of Crebbp Selectively Alters Pre-mRNA Processing in Mouse Hematopoietic Stem Cells. PLoS ONE 6: e24153.
40. Challen GA, Goodell MA (2010) Runx1 isoforms show differential expression patterns during hematopoietic development but have similar functional effects in adult hematopoietic stem cells. Exp Hematol 38: 403-416.
41. Zimmer SN, Zhou Q, Zhou T, Cheng Z, Abboud-Werner SL, et al. (2011) Crebbp haploinsufficiency in mice alters the bone marrow microenvironment, leading to loss of stem cells and excessive myelopoiesis. Blood 118: 69-79.
42. Jacob B, Osato M, Yamashita N, Wang CQ, Taniuchi I, et al. (2010) Stem cell exhaustion due to Runx1 deficiency is prevented by Evi5 activation in leukemogenesis. Blood 115: 1610-1620.