Native adipose Stromal cells egress from adipose tissue in vivo: Evidence during lymph node activation

Stem Cells

Volumn 31, Issue 7, 2013, Pages 1309-1320

  Gil Ortega, Marta ^a,b,c   Garidou, Lucile ^c   Barreau, Corinne ^a,b   Maumus, Marie ^c   Breasson Genevie, Ludovic ^c   Tavernier, V E ^c   García Prieto, Concha F ^d   Bouloumie, Anne ^c   Casteilla, Louis ^a,b   Sengenes, Coralie ^a,b,c  

^a Institut National de la Sant é et de la Recherche Medicale   (France)

^b ETABLISSEMENT FRANÇAIS DU SANG   (France)

^c University Hospital of Toulouse   (France)

^d UNIVERSIDAD SAN PABLO CEU   (Spain)

Author keywords

Chemotaxis; Immunization; Lymph node remodeling; Mesenchymal stem cells; Mobilization

Indexed keywords

CHEMOKINE RECEPTOR CXCR4; NEUTRALIZING ANTIBODY; PODOPLANIN;

ADIPOSE STROMAL CELL; ADIPOSE TISSUE; ANIMAL EXPERIMENT; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; EX VIVO STUDY; IN VIVO STUDY; LYMPH NODE; MALE; MOUSE; NONHUMAN; PERFUSION; PROTEIN INTERACTION; STROMA CELL; THORACIC DUCT;

CHEMOTAXIS; IMMUNIZATION; LYMPH NODE REMODELING; MESENCHYMAL STEM CELLS; MOBILIZATION;

ADIPOSE TISSUE; ANIMALS; CELL DIFFERENTIATION; CELL GROWTH PROCESSES; CHEMOKINE CXCL12; IMMUNOPHENOTYPING; LYMPH NODES; MALE; MESENCHYMAL STROMAL CELLS; MICE; MICE, INBRED C57BL; RECEPTORS, CXCR4;

MURINAE;

EID: 84879953132     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1002/stem.1375     Document Type: Article

References (59)

1. Gregoire FM, Smas CM, Sul HS. Understanding adipocyte differentiation. Physiol Rev 1998;78:783-809.
2. Nawrocki AR, Scherer PE. The delicate balance between fat and muscle: Adipokines in metabolic disease and musculoskeletal inflammation. Curr Opin Pharmacol 2004;4:281-289.
3. Waki H, Tontonoz P. Endocrine functions of adipose tissue. Ann Rev Pathol 2007;2:31-56.
4. Zuk PA, Zhu M, Mizuno H et al. Multilineage cells from human adipose tissue: Implications for cell-based therapies. Tissue Eng 2001;7: 211-228.
5. Gimble JM, Katz AJ, Bunnell BA. Adipose-derived stem cells for regenerative medicine. Circ Res 2007;100:1249-1260.
6. Wagner W, Wein F, Seckinger A et al. Comparative characteristics of mesenchymal stem cells from human bone marrow, adipose tissue, and umbilical cord blood. Exp Hematol 2005;33:1402-1416.
7. Niemeyer P, Kornacker M, Mehlhorn A et al. Comparison of immunological properties of bone marrow stromal cells and adipose tissuederived stem cells before and after osteogenic differentiation in vitro. Tissue Eng 2007;13:111-121.
8. Noel D, Caton D, Roche S et al. Cell specific differences between human adipose-derived and mesenchymal-stromal cells despite similar differentiation potentials. Exp Cell Res 2008;314:1575-1584.
9. Hsiao ST, Asgari A, Lokmic Z et al. Comparative analysis of paracrine factor expression in human adult mesenchymal stem cells derived from bone marrow, adipose, and dermal tissue. Stem Cells Dev 2012;21:2189-2203.
10. Zuk PA, Zhu M, Ashjian P et al. Human adipose tissue is a source of multipotent stem cells. Mol Biol Cell 2002;13:4279-4295.
11. Planat-Benard V, Silvestre JS, Cousin B et al. Plasticity of human adipose lineage cells toward endothelial cells: Physiological and therapeutic perspectives. Circulation 2004;109:656-663.
12. Rehman J, Traktuev D, Li J et al. Secretion of angiogenic and antiapoptotic factors by human adipose stromal cells. Circulation 2004; 109:1292-1298.
13. Miranville A, Heeschen C, Sengenes C et al. Improvement of postnatal neovascularization by human adipose tissue-derived stem cells. Circulation 2004;110:349-355.
14. Puissant B, Barreau C, Bourin P et al. Immunomodulatory effect of human adipose tissue-derived adult stem cells: Comparison with bone marrow mesenchymal stem cells. Br J Haematol 2005;129:118-129.
15. Yanez R, Lamana ML, Garcia-Castro J et al. Adipose tissue-derived mesenchymal stem cells have in vivo immunosuppressive properties applicable for the control of the graft-versus-host disease. Stem Cells 2006;24:2582-2591.
16. Gimble JM, Bunnell BA, Guilak F. Human adipose-derived cells: An update on the transition to clinical translation. Regen Med 2012;7: 225-235.
17. Bedford PA, Todorovic V, Westcott ED et al. Adipose tissue of human omentum is a major source of dendritic cells, which lose MHC class II and stimulatory function in Crohn's disease. J Leukoc Biol 2006;80:546-554.
18. Jing W, Xiao J, Xiong Z et al. Explant culture: An efficient method to isolate adipose-derived stromal cells for tissue engineering. Artif Organs 2010;35:105-112.
19. Sengenes C, Miranville A, Maumus M et al. Chemotaxis and differentiation of human adipose tissue CD34+/CD31 progenitor cells: Role of stromal derived factor-1 released by adipose tissue capillary endothelial cells. Stem Cells 2007;25:2269-2276.
20. Broxmeyer HE, Orschell CM, Clapp DW et al. Rapid mobilization of murine and human hematopoietic stem and progenitor cells with AMD3100, a CXCR4 antagonist. J Exp Med 2005;201:1307-1318.
21. Ionac M, Laskay T, Labahn D et al. Improved technique for cannulation of the murine thoracic duct: A valuable tool for the dissection of immune responses. J Immunol Methods 1997;202:35-40.
22. Wan DC, Shi YY, Nacamuli RP et al. Osteogenic differentiation of mouse adipose-derived adult stromal cells requires retinoic acid and bone morphogenetic protein receptor type IB signaling. Proc Natl Acad Sci USA 2006;103:12335-12340.
23. Okabe M, Ikawa M, Kominami K et al. 'Green mice' as a source of ubiquitous green cells. FEBS Lett 1997;407:313-319.
24. Otto WR. Fluorimetric DNA assay of cell number. Methods Mol Biol 2005;289:251-262.
25. Maumus M, Peyrafitte JA, D'Angelo R et al. Native human adipose stromal cells: Localization, morphology and phenotype. Int J Obes (Lond) 2011;35:1141-1153.
26. Sengenes C, Lolmede K, Zakaroff-Girard A et al. Preadipocytes in the human subcutaneous adipose tissue display distinct features from the adult mesenchymal and hematopoietic stem cells. J Cell Physiol 2005; 205:114-122.
27. Rodeheffer MS, Birsoy K, Friedman JM. Identification of white adipocyte progenitor cells in vivo. Cell 2008;135:240-249.
28. Li CL, Johnson GR. Murine hematopoietic stem and progenitor cells: I. Enrichment and biologic characterization. Blood 1995;85: 1472-1479.
29. Aicher A, Rentsch M, Sasaki K et al. Nonbone marrow-derived circulating progenitor cells contribute to postnatal neovascularization following tissue ischemia. Circ Res 2007;100:581-589.
30. Grenier G, Scime A, Le Grand F et al. Resident endothelial precursors in muscle, adipose, and dermis contribute to postnatal vasculogenesis. Stem Cells 2007;25:3101-3110.
31. Magnon C, Lucas D, Frenette PS. Trafficking of stem cells. Methods Mol Biol 2011;750:3-24.
32. Mazo IB, Massberg S, von Andrian UH. Hematopoietic stem and progenitor cell trafficking. Trends Immunol 2011;32:493-503.
33. Nagasawa T, Hirota S, Tachibana K et al. Defects of B-cell lymphopoiesis and bone-marrow myelopoiesis in mice lacking the CXC chemokine PBSF/SDF-1. Nature 1996;382:635-638.
34. Zou YR, Kottmann AH, Kuroda M et al. Function of the chemokine receptor CXCR4 in haematopoiesis and in cerebellar development. Nature 1998;393:595-599.
35. Lapidot T, Kollet O. The essential roles of the chemokine SDF-1 and its receptor CXCR4 in human stem cell homing and repopulation of transplanted immune-deficient NOD/SCID and NOD/SCID/B2m(null) mice. Leukemia 2002;16:1992-2003.
36. Balabanian K, Lagane B, Infantino S et al. The chemokine SDF-1/ CXCL12 binds to and signals through the orphan receptor RDC1 in T lymphocytes. J Biol Chem 2005;280:35760-35766.
37. Burns JM, Summers BC, Wang Y et al. A novel chemokine receptor for SDF-1 and I-TAC involved in cell survival, cell adhesion, and tumor development. J Exp Med 2006;203:2201-2213.
38. Boldajipour B, Mahabaleshwar H, Kardash E et al. Control of chemokine- guided cell migration by ligand sequestration. Cell 2008;132: 463-473.
39. Martin C, Burdon PC, Bridger G et al. Chemokines acting via CXCR2 and CXCR4 control the release of neutrophils from the bone marrow and their return following senescence. Immunity 2003;19: 583-593.
40. Levesque JP, Hendy J, Takamatsu Y et al. Disruption of the CXCR4/ CXCL12 chemotactic interaction during hematopoietic stem cell mobilization induced by GCSF or cyclophosphamide. J Clin Invest 2003; 111:187-196.
41. Kolonin MG. Progenitor cell mobilization from extramedullary organs. Methods Mol Biol 2012;904:243-252.
42. Roufosse CA, Direkze NC, Otto WR et al. Circulating mesenchymal stem cells. Int J Biochem Cell Biol 2004;36:585-597.
43. Massberg S, Schaerli P, Knezevic-Maramica I et al. Immunosurveillance by hematopoietic progenitor cells trafficking through blood, lymph, and peripheral tissues. Cell 2007;131:994-1008.
44. Laird DJ, von Andrian UH, Wagers AJ. Stem cell trafficking in tissue development, growth, and disease. Cell 2008;132:612-630.
45. Kobayashi H, Kawamoto S, Star RA et al. Micro-magnetic resonance lymphangiography in mice using a novel dendrimer-based magnetic resonance imaging contrast agent. Cancer Res 2003;63:271-276.
46. da Silva Meirelles L, Caplan AI, Nardi NB. In search of the in vivo identity of mesenchymal stem cells. Stem Cells 2008;26:2287-2299.
47. Nombela-Arrieta C, Ritz J, Silberstein LE. The elusive nature and function of mesenchymal stem cells. Nat Rev Mol Cell Biol 2011;12: 126-131.
48. Harvey NL. The link between lymphatic function and adipose biology. Ann N Y Acad Sci 2008;1131:82-88.
49. Pond CM, Mattacks CA. Interactions between adipose tissue around lymph nodes and lymphoid cells in vitro. J Lipid Res 1995;36: 2219-2231.
50. Mattacks CA, Sadler D, Pond CM. Site-specific differences in fatty acid composition of dendritic cells and associated adipose tissue in popliteal depot, mesentery, and omentum and their modulation by chronic inflammation and dietary lipids. Lymph Res Biol 2004;2: 107-129.
51. Pond CM, Mattacks CA. In vivo evidence for the involvement of the adipose tissue surrounding lymph nodes in immune responses. Immunol Lett 1998;63:159-167.
52. Eberl G, Marmon S, Sunshine MJ et al. An essential function for the nuclear receptor RORgamma(t) in the generation of fetal lymphoid tissue inducer cells. Nat Immunol 2004;5:64-73.
53. Benezech C, Mader E, Desanti G et al. Lymphotoxin-beta Receptor signaling through NF-kappaB2-RelB pathway reprograms adipocyte precursors as lymph node stromal cells. Immunity 2012;37:721-734.
54. Koning JJ, Mebius RE. Interdependence of stromal and immune cells for lymph node function. Trends Immunol 2012;33:264-270.
55. Katakai T, Suto H, Sugai M et al. Organizer-like reticular stromal cell layer common to adult secondary lymphoid organs. J Immunol 2008; 181:6189-6200.
56. Pabst O, Wahl B, Bernhardt G et al. Mesenteric lymph node stroma cells in the generation of intestinal immune responses. J Mol Med 2009;87:945-951.
57. Ame-Thomas P, Maby-El Hajjami H, Monvoisin C et al. Human mesenchymal stem cells isolated from bone marrow and lymphoid organs support tumor B-cell growth: Role of stromal cells in follicular lymphoma pathogenesis. Blood 2007;109:693-702.
58. Mueller SN, Germain RN. Stromal cell contributions to the homeostasis and functionality of the immune system. Nat Rev Immunol 2009; 9:618-629.
59. Klein RS, Rubin JB. Immune and nervous system CXCL12 and CXCR4: Parallel roles in patterning and plasticity. Trends Immunol 2004;25:306-314.