Human mesenchymal stem cells inhibit neutrophil apoptosis: A model for neutrophil preservation in the bone marrow niche

Stem Cells

Volumn 26, Issue 1, 2008, Pages 151-162

  Raffaghello, Lizzia ^a   Bianchi, Giordano ^b   Bertolotto, Maria ^b   Montecucco, Fabrizio ^b   Busca, Alessandro ^c   Dallegri, Franco ^b   Ottonello, Luciano ^b   Pistoia, Vito ^a  

^a G GASLINI INSTITUTE   (Italy)

^b UNIVERSITY OF GENOA   (Italy)

^c MOLINETTE HOSPITAL   (Italy)

Author keywords

Bone marrow; Interleukin 6R interleukin 6 fusion protein; Mesenchymal stem cells; Neutrophils

Indexed keywords

CD11B ANTIGEN; COMPLEMENT COMPONENT C5A; FAS ANTIGEN; INTERLEUKIN 6; INTERLEUKIN 8; L SELECTIN; NEUTRALIZING ANTIBODY; PROTEIN BAX; PROTEIN MCL 1; REACTIVE OXYGEN METABOLITE; RECOMBINANT INTERLEUKIN 6; STAT3 PROTEIN; TRIPEPTIDE;

ANTIGEN EXPRESSION; APOPTOSIS; ARTICLE; BIOLOGICAL MODEL; CELL CONTACT; CELL METABOLISM; CELL PROTECTION; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME LINKED IMMUNOSORBENT ASSAY; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; INFLAMMATION; LEUKOCYTE ACTIVATION; MESENCHYMAL STEM CELL; NEUTROPHIL; NEUTROPHIL CHEMOTAXIS; NORMAL HUMAN; OXIDATION; PHAGOCYTOSIS; PRESERVATION; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; RESPIRATORY BURST; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

APOPTOSIS; BLOTTING, WESTERN; BONE MARROW; BONE MARROW CELLS; CELL ADHESION; CELL COMMUNICATION; CELL MOVEMENT; FLOW CYTOMETRY; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; IMMUNOHISTOCHEMISTRY; INTERLEUKIN-6; INTERLEUKIN-8; MESENCHYMAL STEM CELLS; N-FORMYLMETHIONINE LEUCYL-PHENYLALANINE; NEUTROPHILS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; STAT3 TRANSCRIPTION FACTOR;

EID: 38349048723     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1634/stemcells.2007-0416     Document Type: Article

References (64)

1. Wilson A, Trumpp A. Bone-marrow haematopoietic-stem-cell niches. Nat Rev Immunol 2006;6:93-106.
2. Tavassoli M, Friedenstein A. Hemopoietic stromal microenvironment. Am J Hematol 1983;15:195-203.
3. Yin T, Li L. The stem cell niches in bone. J Clin Invest 2006;116:1195-1201.
4. Dominici M, Le Blanc K, Mueller I et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 2006;8:315-317.
5. Keating A. Mesenchymal stromal cells. Curr Opin Hematol 2006;13:419-425.
6. Owen M, Friedenstein AJ. Stromal stem cells: Marrow-derived osteogenic precursors. Ciba Found Symp 1988;136:42-60.
7. Prockop DJ. Marrow stromal cells as stem cells for nonhematopoietic tissues. Science 1997;276:71-74.
8. Pittenger MF, Mackay AM, Beck SC et al. Multilineage potential of adult human mesenchymal stem cells. Science 1999;284:143-147.
9. Dexter TM. Stromal cell associated haemopoiesis. J Cell Physiol Suppl 1982;1:87-94.
10. Horwitz EM, Prockop DJ, Fitzpatrick LA et al. Transplantability and therapeutic effects of bone marrow-derived mesenchymal cells in children with osteogenesis imperfecta. Nat Med 1999;5:309-313.
11. Horwitz EM, Gordon PL, Koo WK et al. Isolated allogeneic bone marrow-derived mesenchymal cells engraft and stimulate growth in children with osteogenesis imperfecta: Implications for cell therapy of bone. Proc Natl Acad Sci U S A 2002;99:8932-8937.
12. Le Blanc K, Gotherstrom C, Ringden O et al. Fetal mesenchymal stem-cell engraftment in bone after in utero transplantation in a patient with severe osteogenesis imperfecta. Transplantation 2005;79:1607-1614.
13. Bianco P, Robey PG. Stem cells in tissue engineering. Nature 2001;414:118-121.
14. Uccelli A, Moretta L, Pistoia V. Immunoregulatory function of mesenchymal stem cells. Eur J Immunol 2006;36:2566-2573.
15. Bartholomew A, Sturgeon C, Siatskas M et al. Mesenchymal stem cells suppress lymphocyte proliferation in vitro and prolong skin graft survival in vivo. Exp Hematol 2002;30:42-48.
16. Corcione A, Benvenuto F, Ferretti E et al. Human mesenchymal stem cells modulate B-cell functions. Blood 2006;107:367-372.
17. Di Nicola M, Carlo-Stella C, Magni M et al. Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or nonspecific mitogenic stimuli. Blood 2002;99:3838-3843.
18. Glennie S, Soeiro I, Dyson PJ et al. Bone marrow mesenchymal stem cells induce division arrest anergy of activated T cells. Blood 2005;105:2821-2827.
19. Jiang XX, Zhang Y, Liu B et al. Human mesenchymal stem cells inhibit differentiation and function of monocyte-derived dendritic cells. Blood 2005;105:4120-4126.
20. Nauta AJ, Kruisselbrink AB, Lurvink E et al. Mesenchymal stem cells inhibit generation and function of both CD34+-derived and monocyte-derived dendritic cells. J Immunol 2006;177:2080-2087.
21. Spaggiari GM, Capobianco A, Becchetti S et al. Mesenchymal stem cell-natural killer cell interactions: Evidence that activated NK cells are capable of killing MSCs, whereas MSCs can inhibit IL-2-induced NK-cell proliferation. Blood 2006;107:1484-1490.
22. Rasmusson I. Immune modulation by mesenchymal stem cells. Exp Cell Res 2006;312:2169-2179.
23. Le Blanc K, Rasmusson I, Sundberg B et al. Treatment of severe acute graft-versus-host disease with third party haploidentical mesenchymal stem cells. Lancet 2004;363:1439-1441.
24. Craddock CG Jr, Perry S, Ventzke LE et al. Evaluation of marrow granulocytic reserves in normal and disease states. Blood 1960;15:840-855.
25. Golde D. Neutrophil kinetics. In: Williams WJ, Beutler E, Erslev AJ et al., eds. Hematology. Vol. 1. Singapore: McGraw-Hill Book Co., 1986:759-764.
26. Berkow RL, Dodson RW. Purification and functional evaluation of mature neutrophils from human bone marrow. Blood 1986;68:853-860.
27. Steele RW, Steele CR, Pilkington NS Jr et al. Functional capacity of marginated and bone marrow reserve granulocytes. Infect Immun 1987;55:2359-2363.
28. Bianco P, Gehron Robey P. Marrow stromal stem cells. J Clin Invest 2000;105:1663-1668.
29. Ottonello L, Tortolina G, Amelotti M et al. Soluble Fas ligand is chemotactic for human neutrophilic polymorphonuclear leukocytes. J Immunol 1999;162:3601-3606.
30. Frumento G, Ottonello L, Bertolotto M et al. Spontaneous apoptosis in neutrophils is associated with downregulation of HLA Class I and is prevented by ligation of Class I. J Leukoc Biol 2000;68:873-880.
31. Dibbert B, Daigle I, Braun D et al. Role for Bcl-xL in delayed eosinophil apoptosis mediated by granulocyte-macrophage colony-stimulating factor and interleukin-5. Blood 1998;92:778-783.
32. Ottonello L, Dapino P, Amelotti M et al. Activation of neutrophil respiratory burst by cytokines and chemoattractants. Regulatory role of extracellular matrix glycoproteins. Inflamm Res 1998;47:345-350.
33. Huang C, Yang L, Li Z et al. Detection of CCND1 amplification using laser capture microdissection coupled with real-time polymerase chain reaction in human esophageal squamous cell carcinoma. Cancer Genet Cytogenet 2007;175:19-25.
34. Witko-Sarsat V, Rieu P, Descamps-Latscha B et al. Neutrophils: Molecules, functions and pathophysiological aspects. Lab Invest 2000;80:617-653.
35. Ottonello L, Frumento G, Arduino N et al. Differential regulation of spontaneous and immune complex-induced neutrophil apoptosis by proinflammatory cytokines. Role of oxidants, Bax and caspase-3. J Leukoc Biol 2002;72:125-132.
36. Wesche DE, Lomas-Neira JL, Perl M et al. Leukocyte apoptosis and its significance in sepsis and shock. J Leukoc Biol 2005;78:325-337.
37. Dallegri F, Ottonello L. Tissue injury in neutrophilic inflammation. Inflamm Res 1997;46:382-391.
38. Fadeel B, Ahlin A, Henter JI et al. Involvement of caspases in neutrophil apoptosis: Regulation by reactive oxygen species. Blood 1998;92:4808-4818.
39. Watson RW. Redox regulation of neutrophil apoptosis. Antioxid Redox Signal 2002;4:97-104.
40. Fialkow L, Wang Y, Downey GP. Reactive oxygen and nitrogen species as signaling molecules regulating neutrophil function. Free Radic Biol Med 2007;42:153-164.
41. Kim DH, Yoo KH, Choi KS et al. Gene expression profile of cytokine and growth factor during differentiation of bone marrow-derived mesenchymal stem cell. Cytokine 2005;31:119-126.
42. Kogler G, Radke TF, Lefort A et al. Cytokine production and hematopoiesis supporting activity of cord blood-derived unrestricted somatic stem cells. Exp Hematol 2005;33:573-583.
43. Asensi V, Valle E, Meana A et al. In vivo interleukin-6 protects neutrophils from apoptosis in osteomyelitis. Infect Immun 2004;72:3823-3828.
44. Biffl WL, Moore EE, Moore FA et al. Interleukin-6 suppression of neutrophil apoptosis is neutrophil concentration dependent. J Leukoc Biol 1995;58:582-584.
45. Hirano T, Ishihara K, Hibi M. Roles of STAT3 in mediating the cell growth, differentiation and survival signals relayed through the IL-6 family of cytokine receptors. Oncogene 2000;19:2548-2556.
46. Dibbert B, Weber M, Nikolaizik WH et al. Cytokine-mediated Bax deficiency and consequent delayed neutrophil apoptosis: A general mechanism to accumulate effector cells in inflammation. Proc Natl Acad Sci U S A 1999;96:13330-13335.
47. Moulding DA, Quayle JA, Hart CA et al. Mcl-1 expression in human neutrophils: Regulation by cytokines and correlation with cell survival. Blood 1998;92:2495-2502.
48. Benvenuto F, Ferrari S, Gerdoni E et al. Human mesenchymal stem cells promote survival of T cells in a quiescent state. STEM CELLS 2007;25:1753-1760.
49. Brach MA, deVos S, Gruss HJ et al. Prolongation of survival of human polymorphonuclear neutrophils by granulocyte-macrophage colony-stimulating factor is caused by inhibition of programmed cell death. Blood 1992;80:2920-2924.
50. Colotta F, Re F, Polentarutti N et al. Modulation of granulocyte survival and programmed cell death by cytokines and bacterial products. Blood 1992;80:2012-2020.
51. Gunn WG, Conley A, Deininger L et al. A crosstalk between myeloma cells and marrow stromal cells stimulates production of DKK1 and interleukin-6: A potential role in the development of lytic bone disease and tumor progression in multiple myeloma. STEM CELLS 2006;24:986-991.
52. Wagner W, Roderburg C, Wein F et al. Molecular and secretory profiles of human mesenchymal stromal cells and their abilities to maintain primitive hematopoietic progenitors. STEM CELLS 2007;25:2638-2647.
53. Fanning NF, Porter J, Shorten GD et al. Inhibition of neutrophil apoptosis after elective surgery. Surgery 1999;126:527-534.
54. Matsuda T, Saito H, Fukatsu K et al. Cytokine-modulated inhibition of neutrophil apoptosis at local site augments exudative neutrophil functions and reflects inflammatory response after surgery. Surgery 2001;129:76-85.
55. Sato K, Ozaki K, Oh I et al. Nitric oxide plays a critical role in suppression of T-cell proliferation by mesenchymal stem cells. Blood 2007;109:228-234.
56. Dinauer MC, Orkin SH. Chronic granulomatous disease. Annu Rev Med 1992;43:117-124.
57. Babior BM. Phagocytes and oxidative stress. Am J Med 2000;109:33-44.
58. Suzuki K, Hino M, Hato F et al. Cytokine-specific activation of distinct mitogen-activated protein kinase subtype cascades in human neutrophils stimulated by granulocyte colony-stimulating factor, granulocyte-macrophage colony-stimulating factor, and tumor necrosis factor-alpha. Blood 1999;93:341-349.
59. Zhao T, Bokoch GM. Critical role of proline-rich tyrosine kinase 2 in reversion of the adhesion-mediated suppression of reactive oxygen species generation by human neutrophils. J Immunol 2005;174:8049-8055.
60. Glasser L, Fiederlein RL. Functional differentiation of normal human neutrophils. Blood 1987;69:937-944.
61. Mishler JM, Williams DM. Alkaline phosphatase as a marker of maturity in human neutrophils. Studies in normals dosed with aetiocholanolone and prednisolone. J Clin Pathol 1980;33:555-561.
62. Mishler JM 4th. Disparity between circulating and marginated neutrophils. Am J Hematol 1980;9:345-348.
63. Lama VN, Smith L, Badri L et al. Evidence for tissue-resident mesenchymal stem cells in human adult lung from studies of transplanted allografts. J Clin Invest 2007.
64. Meirelles LR, Billis A, Magna LA et al. Prostatic atrophy: Immunohistochemical study of hypoxia induced factors. Int Urol Nephrol 2006;38:577-581.