Toll-like receptor 3 and suppressor of cytokine signaling proteins regulate CXCR4 and CXCR7 expression in bone marrow-derived human multipotent stromal cells

PLoS ONE

Volumn 7, Issue 6, 2012, Pages

  Tomchuck, Suzanne L ^a,b   Henkle, Sarah L ^a,b   Coffelt, Seth B ^c   Betancourt, Aline M ^a,b  

^a TULANE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^b TULANE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c NETHERLANDS CANCER INSTITUTE   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CXCR4; CHEMOKINE RECEPTOR CXCR7; INTERFERON REGULATORY FACTOR 1; JANUS KINASE; STAT1 PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING 1; SUPPRESSOR OF CYTOKINE SIGNALING 3; TOLL LIKE RECEPTOR 3;

ARTICLE; BONE MARROW CELL; CELL SURFACE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DEGRADATION; DOWN REGULATION; ENZYME ACTIVATION; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; IMMUNOMODULATION; IMMUNOREGULATION; INTERNALIZATION; MULTIPOTENT STEM CELL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; STROMA CELL; UPREGULATION;

BONE MARROW CELLS; CELLS, CULTURED; HUMANS; RECEPTORS, CXCR; RECEPTORS, CXCR4; STAT1 TRANSCRIPTION FACTOR; STROMAL CELLS; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS; TOLL-LIKE RECEPTOR 3;

EID: 84862639379     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0039592     Document Type: Article

References (51)

1. Arminan A, Gandia C, Garcia-Verdugo JM, Lledo E, Trigueros C, et al. (2010) Mesenchymal stem cells provide better results than hematopoietic precursors for the treatment of myocardial infarction. J Am Coll Cardiol 55: 2244-2253.
2. Niyibizi C, Li F, (2009) Potential implications of cell therapy for osteogenesis imperfecta. Int J Clin Rheumtol 4: 57-66.
3. Lim JH, Lee MH, Yi HG, Kim CS, Kim JH, et al. (2010) Mesenchymal stromal cells for steroid-refractory acute graft-versus-host disease: a report of two cases. Int J Hematol 92: 204-207.
4. Liang J, Gu F, Wang H, Hua B, Hou Y, et al. (2010) Mesenchymal stem cell transplantation for diffuse alveolar hemorrhage in SLE. Nat Rev Rheumatol 6: 486-489.
5. Martino G, Franklin RJ, Baron Van Evercooren A, Kerr DA, (2010) Stem cell transplantation in multiple sclerosis: current status and future prospects. Nat Rev Neurol 6: 247-255.
6. Panes J, Ordas I, Ricart E, (2010) Stem cell treatment for Crohn's disease. Expert Rev Clin Immunol 6: 597-605.
7. Tyndall A, Uccelli A, (2009) Multipotent mesenchymal stromal cells for autoimmune diseases: teaching new dogs old tricks. Bone Marrow Transplant 43: 821-828.
8. Le Blanc K, Ringden O, (2007) Immunomodulation by mesenchymal stem cells and clinical experience. J Intern Med 262: 509-525.
9. Uccelli A, Mancardi G, Chiesa S, (2008) Is there a role for mesenchymal stem cells in autoimmune diseases? Autoimmunity.
10. Spaeth E, Klopp A, Dembinski J, Andreeff M, Marini F, (2008) Inflammation and tumor microenvironments: defining the migratory itinerary of mesenchymal stem cells. Gene Ther 15: 730-738.
11. Abraham EJ, Kodama S, Lin JC, Ubeda M, Faustman DL, et al. (2004) Human pancreatic islet-derived progenitor cell engraftment in immunocompetent mice. Am J Pathol 164: 817-830.
12. Ohtaki H, Ylostalo JH, Foraker JE, Robinson AP, Reger RL, et al. (2008) Stem/progenitor cells from bone marrow decrease neuronal death in global ischemia by modulation of inflammatory/immune responses. Proc Natl Acad Sci U S A 105: 14638-14643.
13. Prockop DJ, (2009) Repair of tissues by adult stem/progenitor cells (MSCs): controversies, myths, and changing paradigms. Mol Ther 17: 939-946.
14. Gao J, Dennis JE, Muzic RF, Lundberg M, Caplan AI, (2001) The dynamic in vivo distribution of bone marrow-derived mesenchymal stem cells after infusion. Cells Tissues Organs 169: 12-20.
15. Hwa Cho H, Bae YC, Jung JS, (2006) Role of Toll-Like Receptors on Human Adipose-Derived Stromal Cells. Stem Cells %R 101634/stemcells2006-0189 24: 2744-2752.
16. Pevsner-Fischer M, Morad V, Cohen-Sfady M, Rousso-Noori L, Zanin-Zhorov A, et al. (2006) Toll-like receptors and their ligands control mesenchymal stem cell functions. Blood %R 101182/blood-2006-06-028704 pp. blood-2006-2006-028704.
17. Tomchuck SL, Zwezdaryk KJ, Coffelt SB, Waterman RS, Danka ES, et al. (2008) Toll-like receptors on human mesenchymal stem cells drive their migration and immunomodulating responses. Stem Cells 26: 99-107.
18. Opitz CA, Litzenburger UM, Lutz C, Lanz TV, Tritschler I, et al. (2009) Toll-like receptor engagement enhances the immunosuppressive properties of human bone marrow-derived mesenchymal stem cells by inducing indoleamine-2,3-dioxygenase-1 via interferon-beta and protein kinase R. Stem Cells 27: 909-919.
19. Waterman RS, Tomchuck SL, Henkle SL, Betancourt AM, (2010) A new mesenchymal stem cell (MSC) paradigm: polarization into a pro-inflammatory MSC1 or an Immunosuppressive MSC2 phenotype. PLoS One 5: e10088.
20. Dalpke A, Heeg K, Bartz H, Baetz A, (2008) Regulation of innate immunity by suppressor of cytokine signaling (SOCS) proteins. Immunobiology 213: 225-235.
21. Mansell A, Smith R, Doyle SL, Gray P, Fenner JE, et al. (2006) Suppressor of cytokine signaling 1 negatively regulates Toll-like receptor signaling by mediating Mal degradation. Nat Immunol 7: 148-155.
22. Nakagawa R, Naka T, Tsutsui H, Fujimoto M, Kimura A, et al. (2002) SOCS-1 participates in negative regulation of LPS responses. Immunity 17: 677-687.
23. Ryo A, Suizu F, Yoshida Y, Perrem K, Liou YC, et al. (2003) Regulation of NF-kappaB signaling by Pin1-dependent prolyl isomerization and ubiquitin-mediated proteolysis of p65/RelA. Mol Cell 12: 1413-1426.
24. Dai X, Sayama K, Yamasaki K, Tohyama M, Shirakata Y, et al. (2006) SOCS1-negative feedback of STAT1 activation is a key pathway in the dsRNA-induced innate immune response of human keratinocytes. J Invest Dermatol 126: 1574-1581.
25. Zeng B, Li H, Liu Y, Zhang Z, Zhang Y, et al. (2008) Tumor-induced suppressor of cytokine signaling 3 inhibits toll-like receptor 3 signaling in dendritic cells via binding to tyrosine kinase 2. Cancer Res 68: 5397-5404.
26. Garzon R, Soriano SF, Rodriguez-Frade JM, Gomez L, Martin de Ana A, et al. (2004) CXCR4-mediated suppressor of cytokine signaling up-regulation inactivates growth hormone function. J Biol Chem 279: 44460-44466.
27. Soriano SF, Hernanz-Falcon P, Rodriguez-Frade JM, De Ana AM, Garzon R, et al. (2002) Functional inactivation of CXC chemokine receptor 4-mediated responses through SOCS3 up-regulation. J Exp Med 196: 311-321.
28. Sharma M, Afrin F, Satija N, Tripathi RP, Gangenahalli GU, (2010) Stromal-derived factor-1/CXCR4 signaling: indispensable role in homing and engraftment of hematopoietic stem cells in bone marrow. Stem Cells Dev 20: 933-946.
29. Pello OM, Moreno-Ortiz Mdel C, Rodriguez-Frade JM, Martinez-Munoz L, Lucas D, et al. (2006) SOCS up-regulation mobilizes autologous stem cells through CXCR4 blockade. Blood 108: 3928-3937.
30. Zanin-Zhorov A, Tal G, Shivtiel S, Cohen M, Lapidot T, et al. (2005) Heat shock protein 60 activates cytokine-associated negative regulator suppressor of cytokine signaling 3 in T cells: effects on signaling, chemotaxis, and inflammation. J Immunol 175: 276-285.
31. Dimitriou ID, Clemenza L, Scotter AJ, Chen G, Guerra FM, et al. (2008) Putting out the fire: coordinated suppression of the innate and adaptive immune systems by SOCS1 and SOCS3 proteins. Immunol Rev 224: 265-283.
32. Uccelli A, Pistoia V, Moretta L, (2007) Mesenchymal stem cells: a new strategy for immunosuppression? Trends Immunol 28: 219-226.
33. Chamberlain G, Fox J, Ashton B, Middleton J, (2007) Concise review: mesenchymal stem cells: their phenotype, differentiation capacity, immunological features, and potential for homing. Stem Cells 25: 2739-2749.
34. Sordi V, Malosio ML, Marchesi F, Mercalli A, Melzi R, et al. (2005) Bone marrow mesenchymal stem cells express a restricted set of functionally active chemokine receptors capable of promoting migration to pancreatic islets. Blood 106: 419-427.
35. Wynn RF, Hart CA, Corradi-Perini C, O'Neill L, Evans CA, et al. (2004) A small proportion of mesenchymal stem cells strongly expresses functionally active CXCR4 receptor capable of promoting migration to bone marrow. Blood 104: 2643-2645.
36. Chen J, Li Y, Wang L, Zhang Z, Lu D, et al. (2001) Therapeutic benefit of intravenous administration of bone marrow stromal cells after cerebral ischemia in rats. Stroke 32: 1005-1011.
37. Askari AT, Unzek S, Popovic ZB, Goldman CK, Forudi F, et al. (2003) Effect of stromal-cell-derived factor 1 on stem-cell homing and tissue regeneration in ischaemic cardiomyopathy. Lancet 362: 697-703.
38. Coffelt SB, Marini FC, Watson K, Zwezdaryk KJ, Dembinski JL, et al. (2009) The pro-inflammatory peptide LL-37 promotes ovarian tumor progression through recruitment of multipotent mesenchymal stromal cells. Proc Natl Acad Sci U S A 106: 3806-3811.
39. Bolte S, Cordelieres FP, (2006) A guided tour into subcellular colocalization analysis in light microscopy. J Microsc 224: 213-232.
40. Kinjyo I, Hanada T, Inagaki-Ohara K, Mori H, Aki D, et al. (2002) SOCS1/JAB is a negative regulator of LPS-induced macrophage activation. Immunity 17: 583-591.
41. Schlee M, Hornung V, Hartmann G, (2006) siRNA and isRNA: two edges of one sword. Mol Ther 14: 463-470.
42. Sioud M, (2007) RNA interference and innate immunity. Adv Drug Deliv Rev 59: 153-163.
43. Kim HK, Kim JE, Chung J, Han KS, Cho HI, (2007) Surface expression of neutrophil CXCR4 is down-modulated by bacterial endotoxin. Int J Hematol 85: 390-396.
44. Kortesidis A, Zannettino A, Isenmann S, Shi S, Lapidot T, et al. (2005) Stromal-derived factor-1 promotes the growth, survival, and development of human bone marrow stromal stem cells. Blood 105: 3793-3801.
45. Balabanian K, Lagane B, Infantino S, Chow KY, Harriague J, et al. (2005) The chemokine SDF-1/CXCL12 binds to and signals through the orphan receptor RDC1 in T lymphocytes. J Biol Chem 280: 35760-35766.
46. Levoye A, Balabanian K, Baleux F, Bachelerie F, Lagane B, (2009) CXCR7 heterodimerizes with CXCR4 and regulates CXCL12-mediated G protein signaling. Blood 113: 6085-6093.
47. Naumann U, Cameroni E, Pruenster M, Mahabaleshwar H, Raz E, et al. (2010) CXCR7 functions as a scavenger for CXCL12 and CXCL11. PLoS One 5: e9175.
48. Gao H, Priebe W, Glod J, Banerjee D, (2009) Activation of signal transducers and activators of transcription 3 and focal adhesion kinase by stromal cell-derived factor 1 is required for migration of human mesenchymal stem cells in response to tumor cell-conditioned medium. Stem Cells 27: 857-865.
49. Liu H, Xue W, Ge G, Luo X, Li Y, et al. (2010) Hypoxic preconditioning advances CXCR4 and CXCR7 expression by activating HIF-1alpha in MSCs. Biochem Biophys Res Commun 401: 509-515.
50. Croker BA, Kiu H, Nicholson SE, (2008) SOCS regulation of the JAK/STAT signalling pathway. Semin Cell Dev Biol 19: 414-422.
51. Ahmed CM, Dabelic R, Martin JP, Jager LD, Haider SM, et al. (2010) Enhancement of antiviral immunity by small molecule antagonist of suppressor of cytokine signaling. J Immunol 185: 1103-1113.