Glycoengineering of E-Selectin Ligands by Intracellular versus Extracellular Fucosylation Differentially Affects Osteotropism of Human Mesenchymal Stem Cells

Stem Cells

Volumn 34, Issue 10, 2016, Pages 2501-2511

  Dykstra, Brad ^a,b   Lee, Jungmin ^b,c   Mortensen, Luke J ^d   Yu, Haixiao ^e   Wu, Zhengliang L ^e   Lin, Charles P ^f   Rossi, Derrick J ^b,c   Sackstein, Robert ^a,b,g  

^a HARVARD MEDICAL SCHOOL   (United States)

^b HARVARD UNIVERSITY   (United States)

^c Harvard University   (United States)

^d UNIVERSITY OF GEORGIA   (United States)

^e R D Systems Inc   (United States)

^f MASSACHUSETTS GENERAL HOSPITAL   (United States)

^g BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

E selectin; Exofucosylation; Fucosyltransferase; GPS; HCELL; Intravital microscopy; Mesenchymal stromal cell; Modified mRNA; sialyl Lewis X

Indexed keywords

ENDOTHELIAL LEUKOCYTE ADHESION MOLECULE 1; FUCOSYLTRANSFERASE; FUCOSYLTRANSFERASE VI; LIGAND; MESSENGER RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BIOCHEMICAL ANALYSIS; BIOENGINEERING; CALVARIA; COMPARATIVE STUDY; CONTROLLED STUDY; ENDOTHELIUM CELL; FUCOSYLATION; FUT6 GENE; GENE; GENETIC TRANSFECTION; GLYCOENGINEERING; HUMAN; HUMAN CELL; MESENCHYMAL STEM CELL; MOUSE; NONHUMAN; PROTEIN EXPRESSION;

EID: 84990833591     PISSN: 10665099     EISSN: 15494918     Source Type: Journal    
DOI: 10.1002/stem.2435     Document Type: Article

References (32)

1. 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.
2. Griffin MD, Elliman SJ, Cahill E et al. Adult mesenchymal stromal cell therapy for inflammatory diseases: How well are we joining the dots? Stem Cells 2013;31:2033–2031.
3. Sipkins DA, Wei X, Wu JW et al. In vivo imaging of specialized bone marrow endothelial microdomains for tumour engraftment. Nature 2005;435:969–973.
4. Schweitzer KM, Dräger AM, van der Valk P et al. Constitutive expression of E-selectin and vascular cell adhesion molecule-1 on endothelial cells of hematopoietic tissues. Am J Pathol 1996;148:165–175.
5. Sackstein R. Glycosyltransferase-programmed stereosubstitution (GPS) to create HCELL: Engineering a roadmap for cell migration. Immunol Rev 2009;230:51–74.
6. Dimitroff CJ, Lee JY, Rafii S et al. Cd44 is a major E-selectin ligand on human hematopoietic progenitor cells. J Cell Biol 2001;153:1277–1286.
7. Sackstein R, Merzaban JS, Cain DW et al. Ex vivo glycan engineering of CD44 programs human multipotent mesenchymal stromal cell trafficking to bone. Nat Med 2008;14:181–187.
8. Schrepfer S, Deuse T, Reichenspurner H et al. Stem cell transplantation: The lung barrier. Transplant Proc 2007;39:573–576.
9. Lee RH, Pulin AA, Seo MJ et al. Intravenous hMSCs improve myocardial infarction in mice because cells embolized in lung are activated to secrete the anti-inflammatory protein TSG-6. Cell Stem Cell 2009;5:54–63.
10. Ankrum J, Karp JM. Mesenchymal stem cell therapy: Two steps forward, one step back. Trends Mol Med 2010;16:203–209.
11. Levy O, Zhao W, Mortensen LJ et al. mRNA-engineered mesenchymal stem cells for targeted delivery of interleukin-10 to sites of inflammation. Blood 2013;122:e22–e32.
12. Warren L, Manos PD, Ahfeldt T et al. Highly efficient reprogramming to pluripotency and directed differentiation of human cells with synthetic modified mRNA. Cell Stem Cell 2010;7:618–630.
13. Mandal PK, Rossi DJ. Reprogramming human fibroblasts to pluripotency using modified mRNA. Nat Protoc 2013;8:568–582.
14. Borsig L, Katopodis AG, Bowen BR et al. Trafficking and localization studies of recombinant alpha1, 3-fucosyltransferase VI stably expressed in CHO cells. Glycobiology 1998;8:259–268.
15. Mortensen LJ, Levy O, Phillips JP et al. Quantification of mesenchymal stem cell (MSC) delivery to a target site using in vivo confocal microscopy. PloS One 2013;8:e78145.
16. Galipeau J. The mesenchymal stromal cells dilemma–does a negative phase III trial of random donor mesenchymal stromal cells in steroid-resistant graft-versus-host disease represent a death knell or a bump in the road? Cytotherapy 2013;15:2–8.
17. Cheng H, Byrska-Bishop M, Zhang CT et al. Stem cell membrane engineering for cell rolling using peptide conjugation and tuning of cell-selectin interaction kinetics. Biomaterials 2012;33:5004–5012.
18. Lo CY, Antonopoulos A, Dell A et al. The use of surface immobilization of P-selectin glycoprotein ligand-1 on mesenchymal stem cells to facilitate selectin mediated cell tethering and rolling. Biomaterials 2013;34:8213–8222.
19. Sarkar D, Spencer JA, Phillips JA et al. Engineered cell homing. Blood 2011;118:e184–e191. 1
20. Xia L, McDaniel JM, Yago T et al. Surface fucosylation of human cord blood cells augments binding to P-selectin and E-selectin and enhances engraftment in bone marrow. Blood 2004;104:3091–3096.
21. Wan X, Sato H, Miyaji H et al. Fucosyltransferase VII improves the function of selectin ligands on cord blood hematopoietic stem cells. Glycobiology 2013;23:1184–1191.
22. Popat U, Mehta RS, Rezvani K et al. Enforced fucosylation of cord blood hematopoietic cells accelerates neutrophil and platelet engraftment after transplantation. Blood 2015;125:2885–2892.
23. Parmar S, Liu X, Najjar A et al. Ex vivo fucosylation of third-party human regulatory T cells enhances anti-graft-versus-host disease potency in vivo. Blood 2015;125:1502–1506.
24. Merzaban JS, Imitola J, Starossom SC et al. Cell surface glycan engineering of neural stem cells augments neurotropism and improves recovery in a murine model of multiple sclerosis. Glycobiology 2015;25:1392–1409.
25. Liao W, Pham V, Liu L et al. Mesenchymal stem cells engineered to express selectin ligands and IL-10 exert enhanced therapeutic efficacy in murine experimental autoimmune encephalomyelitis. Biomaterials 2016;77:87–97.
26. Yao W, Guan M, Jia J et al. Reversing bone loss by directing mesenchymal stem cells to bone. Stem Cells 2013;31:2003–2014.
27. Wynn RF, Hart CA, Corradi-Perini C et al. A small proportion of mesenchymal stem cells strongly expresses functionally active CXCR4 receptor capable of promoting migration to bone marrow. Blood 2004;104:2643–2645.
28. Shi M, Li J, Liao L et al. Regulation of CXCR4 expression in human mesenchymal stem cells by cytokine treatment: role in homing efficiency in NOD/SCID mice. Haematologica 2007;92:897–904.
29. Jones GN, Moschidou D, Lay K et al. Upregulating CXCR4 in human fetal mesenchymal stem cells enhances engraftment and bone mechanics in a mouse model of osteogenesis imperfecta. Stem Cells Transl Med 2012;1:70–78.
30. Kumar S Ponnazhagan S. Bone homing of mesenchymal stem cells by ectopic alpha 4 integrin expression. FASEB J 2007;21:3917–3927.
31. Srouji S, Ben-David D, Fromigue O et al. Lentiviral-mediated integrin alpha5 expression in human adult mesenchymal stromal cells promotes bone repair in mouse cranial and long-bone defects. Hum Gene Ther 2012;23:167–172.
32. Hamidouche Z, Fromigue O, Ringe J et al. Priming integrin alpha5 promotes human mesenchymal stromal cell osteoblast differentiation and osteogenesis. Proc Natl Acad Sci USA 2009;106:18587–18591.