Protein Malnutrition Induces Bone Marrow Mesenchymal Stem Cells Commitment to Adipogenic Differentiation Leading to Hematopoietic Failure

PLoS ONE

Volumn 8, Issue 3, 2013, Pages

  Cunha, Mayara Caldas Ramos ^a   Lima, Fabiana da Silva ^a   Vinolo, Marco Aurélio Ramirez ^b   Hastreiter, Araceli ^a   Curi, Rui ^a   Borelli, Primavera ^a   Fock, Ricardo Ambrósio ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b UNIVERSITY OF CAMPINAS   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

CCAAT ENHANCER BINDING PROTEIN ALPHA; CD45 ANTIGEN; GRANULOCYTE COLONY STIMULATING FACTOR; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 3; MESSENGER RNA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; STEM CELL FACTOR; STEM CELL FACTOR RECEPTOR; STEROL REGULATORY ELEMENT BINDING PROTEIN;

ADIPOCYTE; ANEMIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW DEPRESSION; BONE MARROW HYPOPLASIA; CELL DIFFERENTIATION; COLONY FORMING UNIT F; CONTROLLED STUDY; CYTOKINE PRODUCTION; GENETIC ASSOCIATION; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; IN VITRO STUDY; KWASHIORKOR; LEUKOPENIA; MALE; MESENCHYMAL STEM CELL; MOUSE; NONHUMAN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA GENE; PROTEIN EXPRESSION; PROTEIN RESTRICTION; SPLEEN DISEASE; STEROL REGULATORY ELEMENT BINDING PROTEIN GENE;

ADIPOCYTES; ADIPOGENESIS; ANIMALS; BODY WEIGHT; BONE MARROW CELLS; CCAAT-ENHANCER-BINDING PROTEINS; DIET; DIETARY PROTEINS; EATING; FIBROBLASTS; GRANULOCYTE-MACROPHAGE COLONY-STIMULATING FACTOR; HEMATOPOIESIS; INTERLEUKIN-3; MALE; MESENCHYMAL STROMAL CELLS; MICE; MICE, INBRED BALB C; PPAR GAMMA; PROTEIN-ENERGY MALNUTRITION; SERUM ALBUMIN; STEROL REGULATORY ELEMENT BINDING PROTEINS;

EID: 84875048070     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0058872     Document Type: Article

References (41)

1. Xavier JG, Favero ME, Vinolo MA, Rogero MM, Dagli ML, et al. (2007) Protein-energy malnutrition alters histological and ultrastructural characteristics of the bone marrow and decreases haematopoiesis in adult mice. Histol Histopathol 22: 651-660.
2. Borelli P, Barros FE, Nakajima K, Blatt SL, Beutler B, et al. (2009) Protein-energy malnutrition halts hemopoietic progenitor cells in the G0/G1 cell cycle stage, thereby altering cell production rates. Braz J Med Biol Res 42: 523-530.
3. Fock RA, Blatt SL, Beutler B, Pereira J, Tsujita M, et al. (2009) Study of lymphocyte subpopulations in bone marrow in a model of protein-energy malnutrition. Nutrition 10: 1021-1028.
4. Fock RA, Vinolo MA, de Moura Sá Rocha V, de Sá Rocha LC, Borelli P, (2007) Protein-energy malnutrition decreases the expression of TLR-4/MD-2 and CD14 receptors in peritoneal macrophages and reduces the synthesis of TNF-alpha in response to lipopolysaccharide (LPS) in mice. Cytokine 40: 105-114.
5. Bianco P, (2011) Bone and the hematopoietic niche: a tale of two stem cells. Blood 117: 5281-5288.
6. Méndez-Ferrer S, Michurina TV, Ferraro F, Mazloom AR, Macarthur BD, et al. (2010) Mesenchymal and haematopoietic stem cells form a unique bone marrow niche. Nature 466: 829-834.
7. Zapata AG, Alfaro D, García-Ceca J, (2012) Biology of stem cells: The role of microenvironments. Adv Exp Med Biol 741: 135-151.
8. Gimble JM, Robinson CE, Wu X, Kelly KA, (1996) The function of adipocytes in the bone marrow stroma: an update. Bone 19: 421-428.
9. 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.
10. Sekiya I, Larson BL, Vuoristo JT, Cui JG, Prockop DJ, (2004) Adipogenic differentiation of human adult stem cells from bone marrow stroma (MSCs). J Bone Miner Res 19: 256-264.
11. Rosen ED, Walkey CJ, Puigserver P, Spiegelman BM, (2000) Transcriptional regulation of adipogenesis. Genes Dev 14: 1293-1307.
12. Tontonoz P, Hu E, Spiegelman BM, (1994) Stimulation of adipogenesis in fibroblasts by PPAR gamma 2, a lipid-activated transcription factor. Cell 79: 1147-1156.
13. Vituri CL, Alvarez-Silva M, Trentin AG, Borelli P, (2000) Alterations in proteins of bone marrow extracellular matrix in undernourished mice. Braz J Med Biol Res 33: 889-895.
14. Reeves PG, Nielsen FH, Fahey GC Jr, (1993) AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. J Nutr 123: 1939-1951.
15. Ward PG, (1963) A Micro-Kjeldahl procedure for field use. J Med Lab Technol 20: 191-195.
16. Livak KJ, Schmittgen TD, (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408.
17. Friedenstein AJ, (1976) Precursor cells of mechanocytes. Int Rev Cytol 47: 327-359.
18. Friedenstein AJ, Chailakhjan RK, Lalykina KS, (1970) The development of fibroblast colonies in monolayer cultures of guinea-pig bone marrow and spleen cells. Cell Tissue Kinet 3: 393-403.
19. Caplan AI, (1991) Mesenchymal stem cells. J Orthop Res 9: 641-650.
20. Javazon EH, Beggs KJ, Flake AW, (2004) Mesenchymal stem cells: paradoxes of passaging. Exp Hematol 32: 414-425.
21. Kornberg A, Daft FS, Sebrell WH, (1946) Granulocytopenia and Anemia in Rats Fed Diets of Low Casein Content. Science 103: 646-648.
22. Aschkenasy A, (1957) On the pathogenesis of anemias and leukopenias induced by dietary protein deficiency. Am J Clin Nutr 5: 14-25.
23. Catchatourian R, Eckerling G, Fried W, (1980) Effect of short-term protein deprivation on hemopoietic functions of healthy volunteers. Blood 55: 625-628.
24. Landgraf MA, Martinez LL, Rastelli VM, Franco Mdo C, Soto-Suazo M, et al. (2005) Intrauterine undernutrition in rats interferes with leukocyte migration, decreasing adhesion molecule expression in leukocytes and endothelial cells. J Nutr 135: 1480-1485.
25. Martí J, Armadans L, Vaqué J, Segura F, Schwartz S, (2001) Protein-calorie malnutrition and lymphocytopenia as predictors of hospital infection in the elderly]. Med Clin 116: 446-450.
26. Fló J, Elías F, Benedetti R, Massouh E, (1996) Reversible effects on B and T cells of the gut-associated lymphoid tissues in rats malnourished during suckling: impaired induction of the immune response to intra-Peyer patches immunization with cholera toxin. Clin Immunol Immunopathol 80: 147-154.
27. Olmos S, Reinoso MF, Márquez MG, Roux ME, (2001) Cytogenetic studies in bone marrow cells from Wistar rats in protein malnutrition. Metabolism 50: 1025-1029.
28. Shivtiel S, Kollet O, Lapid K, Schajnovitz A, Goichberg P, et al. (2008) CD45 regulates retention, motility, and numbers of hematopoietic progenitors, and affects osteoclast remodeling of metaphyseal trabecules. J Exp Med 205: 2381-2395.
29. Ortiz M, Wine JW, Lohrey N, Ruscetti FW, Spence SE, et al. (1999) Functional characterization of a novel hematopoietic stem cell and its place in the c-Kit maturation pathway in bone marrow cell development. Immunity 10: 173-182.
30. Mourcin F, Grenier N, Mayol JF, Lataillade JJ, Sotto JJ, et al. (2005) Mesenchymal stem cells support expansion of in vitro irradiated CD34(+) cells in the presence of SCF, FLT3 ligand, TPO and IL3: potential application to autologous cell therapy in accidentally irradiated victims. Radiat Res 164: 1-9.
31. Kimura T, Sakabe H, Tanimukai S, Abe T, Urata Y, et al. (1997) Simultaneous activation of signals through gp130, c-kit, and interleukin-3 receptor promotes a trilineage blood cell production in the absence of terminally acting lineage-specific factors. Blood 90: 4767-4778.
32. Liesveld JL, Broudy VC, Harbol AW, Abboud CN, (1995) Effect of stem cell factor on myelopoiesis potential in human Dexter-type culture systems. Exp Hematol 23: 202-209.
33. Bernstein ID, Andrews RG, Zsebo KM, (1991) Recombinant human stem cell factor enhances the formation of colonies by CD34+ and CD34+lin- cells, and the generation of colony-forming cell progeny from CD34+lin- cells cultured with interleukin-3, granulocyte colony-stimulating factor, or granulocyte-macrophage colony-stimulating factor. Blood 77: 2316-2321.
34. Li T, Wu Y, (2011) Paracrine molecules of mesenchymal stem cells for hematopoietic stem cell niche. Bone Marrow Res 2011: 353878.
35. Carrancio S, Blanco B, Romo C, Muntion S, Lopez-Holgado N, et al. (2011) Bone marrow mesenchymal stem cells for improving hematopoietic function: an in vitro and in vivo model. Part 2: Effect on bone marrow microenvironment. PLoS One 6: e26241.
36. Dormady SP, Bashayan O, Dougherty R, Zhang XM, Basch RS, (2001) Immortalized multipotential mesenchymal cells and the hematopoietic microenvironment. J Hematother Stem Cell Res 10: 125-140.
37. Nauta AJ, Kruisselbrink AB, Lurvink E, Willemze R, Fibbe WE, (2006) Mesenchymal stem cells inhibit generation and function of both CD34+-derived and monocyte-derived dendritic cells. J Immunol 177: 2080-2087.
38. Fernández-Varón E, Villamayor L, (2007) Granulocyte and granulocyte macrophage colony-stimulating factors as therapy in human and veterinary medicine. Vet J 174: 33-41.
39. Musri MM, Párrizas M, (2012) Epigenetic regulation of adipogenesis. Curr Opin Clin Nutr Metab Care 15: 342-349.
40. Jeon Ti, Osborne Tf, (2012) Srebps: Metabolic Integrators in Physiology and Metabolism. Trends Endocrinol Metab 23: 65-72.
41. Sekiya I, Larson BL, Vuoristo JT, Cui JG, Prockop DJ, (2004) Adipogenic differentiation of human adult stem cells from bone marrow stroma (MSCs). J Bone Miner Res 19: 256-264.