Cell surface glycan engineering of neural stem cells augments neurotropism and improves recovery in a murine model of multiple sclerosis

Glycobiology

Volumn 25, Issue 12, 2015, Pages 1392-1409

  Merzaban, Jasmeen S ^a,c   Imitola, Jaime ^b,d   Starossom, Sarah C ^b,e   Zhu, Bing ^b   Wang, Yue ^b   Lee, Jack ^a   Ali, Amal J ^c   Olah, Marta ^b   Abuelela, Ayman F ^c   Khoury, Samia J ^b,f   Sackstein, Robert ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c KING ABDULLAH UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Saudi Arabia)

^d THE OHIO STATE UNIVERSITY WEXNER MEDICAL CENTER   (United States)

^e CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^f AMERICAN UNIVERSITY OF BEIRUT   (Lebanon)

Author keywords

Exofucosylation; Glycan engineering; HCELL; Multiple sclerosis; Neural stem cell

Indexed keywords

CELL SURFACE GLYCAN; ENDOTHELIAL LEUKOCYTE ADHESION MOLECULE 1; GLYCAN; GLYCOSYLTRANSFERASE; L SELECTIN; LIGAND; NERVE CELL ADHESION MOLECULE; UNCLASSIFIED DRUG; HEMATOPOIETIC CELL E- AND L-SELECTIN LIGAND, HUMAN; HERMES ANTIGEN; POLYSACCHARIDE; SELECTIN;

ADULT STEM CELL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ENGINEERING; CELL HOMING; CELL MIGRATION; CONTROLLED STUDY; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; HEMATOPOIETIC CELL; INFLAMMATION; MOUSE; MULTIPLE SCLEROSIS; NERVE FIBER; NERVOUS SYSTEM INFLAMMATION; NEURAL STEM CELL; NEUROTROPISM; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; TISSUE SPECIFICITY; ANIMAL; C57BL MOUSE; CELL MOTION; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; GENE THERAPY; GENETICS; METABOLISM; NERVE REGENERATION; TRANSPLANTATION;

ANIMALS; ANTIGENS, CD44; CELL MOVEMENT; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; GENETIC THERAPY; MICE; MICE, INBRED C57BL; NERVE REGENERATION; NEURAL CELL ADHESION MOLECULES; NEURAL STEM CELLS; POLYSACCHARIDES; SELECTINS;

EID: 84940508549     PISSN: 09596658     EISSN: 14602423     Source Type: Journal    
DOI: 10.1093/glycob/cwv046     Document Type: Article

References (77)

1. AbuSamra DB, Al-Kilani A, Hamdan SM, Sakashita K, Gadhoum SZ, Merzaban JS. 2015. Quantitative characterization of E-selectin interaction with native CD44 and P-selectin glycoprotein ligand-1 (PSGL-1) using a real-time immunoprecipitation-based binding assay. J Biol Chem. 290:21213-21230.
2. Alam HB, Sun L, Ruff P, Austin B, Burris D, Rhee P. 2000. E- and P-selectin expression depends on the resuscitation fluid used in hemorrhaged rats. The Journal of Surgical Research. 94:145-152.
3. Alon R, Feizi T, Yuen CT, Fuhlbrigge RC, Springer TA. 1995. Glycolipid ligands for selectins support leukocyte tethering and rolling under physiologic flow conditions. Journal of Immunology. 154:5356-5366.
4. Back SA, Tuohy TM, Chen H, Wallingford N, Craig A, Struve J, Luo NL, Banine F, Liu Y, Chang A, et al. 2005. Hyaluronan accumulates in demyelinated lesions and inhibits oligodendrocyte progenitor maturation. Nature Medicine. 11:966-972.
5. Ben-Hur T, Einstein O, Mizrachi-Kol R, Ben-Menachem O, Reinhartz E, Karussis D, Abramsky O. 2003. Transplanted multipotential neural precursor cells migrate into the inflamed white matter in response to experimental autoimmune encephalomyelitis. Glia. 41:73-80.
6. Berlin C, Bargatze RF, Campbell JJ, von Andrian UH, Szabo MC, Hasslen SR, Nelson RD, Berg EL, Erlandsen SL, Butcher EC. 1995. Alpha 4 integrins mediate lymphocyte attachment and rolling under physiologic flow. Cell. 80:413-422.
7. Bezzi P, Domercq M, Brambilla L, Galli R, Schols D, De Clercq E, Vescovi A, Bagetta G, Kollias G, Meldolesi J, et al. 2001. CXCR4-activated astrocyte glutamate release via TNFalpha: Amplification by microglia triggers neurotoxicity. Nature Neuroscience. 4:702-710.
8. Butcher EC. 1991. Leukocyte-endothelial cell recognition: Three (or more) steps to specificity and diversity. Cell. 67:1033-1036.
9. Campos LS, Decker L, Taylor V, Skarnes W. 2006. Notch, epidermal growth factor receptor, and beta1-integrin pathways are coordinated in neural stem cells. The Journal of Biological Chemistry. 281:5300-5309.
10. Campos LS, Leone DP, Relvas JB, Brakebusch C, Fassler R, Suter U, ffrench-Constant C. 2004. Beta1 integrins activate a MAPK signalling pathway in neural stem cells that contributes to their maintenance. Development. 131:3433-3444.
11. Caplan AI. 2009. Why are MSCs therapeutic? New data: New insight. The Journal of Pathology. 217:318-324.
12. Chitnis T, Najafian N, Abdallah KA, Dong V, Yagita H, Sayegh MH, Khoury SJ. 2001. CD28-independent induction of experimental autoimmune encephalomyelitis. J Clin Invest. 107:575-583.
13. Deboux C, Ladraa S, Cazaubon S, Ghribi-Mallah S, Weiss N, Chaverot N, Couraud PO, Baron-Van Evercooren A. 2013. Overexpression of CD44 in neural precursor cells improves trans-endothelial migration and facilitates their invasion of perivascular tissues in vivo. PloS One. 8:e57430.
14. Dimitroff CJ, Lee JY, Fuhlbrigge RC, Sackstein R. 2000. A distinct glycoform of CD44 is an L-selectin ligand on human hematopoietic cells. Proceedings of the National Academy of Sciences of the United States of America. 97:13841-13846.
15. Dimitroff CJ, Lee JY, Rafii S, Fuhlbrigge RC, Sackstein R. 2001. CD44 is a major E-selectin ligand on human hematopoietic progenitor cells. J Cell Biol. 153:1277-1286.
16. Ding ZM, Babensee JE, Simon SI, Lu H, Perrard JL, Bullard DC, Dai XY, Bromley SK, Dustin ML, Entman ML, et al. 1999. Relative contribution of LFA-1 and Mac-1 to neutrophil adhesion and migration. Journal of Immunology. 163:5029-5038.
17. Drake TA, Cheng J, Chang A, Taylor FB Jr 1993. Expression of tissue factor, thrombomodulin, and E-selectin in baboons with lethal Escherichia coli sepsis. The American Journal of Pathology. 142:1458-1470.
18. Einstein O, Fainstein N, Vaknin I, Mizrachi-Kol R, Reihartz E, Grigoriadis N, Lavon I, Baniyash M, Lassmann H, Ben-Hur T. 2007. Neural precursors attenuate autoimmune encephalomyelitis by peripheral immunosuppression. Annals of Neurology. 61:209-218.
19. Einstein O, Grigoriadis N, Mizrachi-Kol R, Reinhartz E, Polyzoidou E, Lavon I, Milonas I, Karussis D, Abramsky O, Ben-Hur T. 2006. Transplanted neural precursor cells reduce brain inflammation to attenuate chronic experimental autoimmune encephalomyelitis. Experimental Neurology. 198:275-284.
20. Emamgholipour S, Eshaghi SM, Hossein-nezhad A, Mirzaei K, Maghbooli Z, Sahraian MA. 2013. Adipocytokine profile, cytokine levels and foxp3 expression in multiple sclerosis: A possible link to susceptibility and clinical course of disease. PloS One. 8:e76555.
21. Flax JD, Aurora S, Yang C, Simonin C, Wills AM, Billinghurst LL, Jendoubi M, Sidman RL, Wolfe JH, Kim SU, et al. 1998. Engraftable human neural stem cells respond to developmental cues, replace neurons, and express foreign genes. Nat Biotechnol. 16:1033-1039.
22. Fu J, Yang QY, Sai K, Chen FR, Pang JC, Ng HK, Kwan AL, Chen ZP. 2013. TGM2 inhibition attenuates ID1 expression in CD44-high glioma-initiating cells. Neuro-oncology. 15:1353-1365.
23. Fuhlbrigge RC, Kieffer JD, Armerding D, Kupper TS. 1997. Cutaneous lymphocyte antigen is a specialized form of PSGL-1 expressed on skin-homing T cells. Nature. 389:978-981.
24. Fuhlbrigge RC, King SL, Dimitroff CJ, Kupper TS, Sackstein R. 2002. Direct real-time observation of E- and P-selectin-mediated rolling on cutaneous lymphocyte-associated antigen immobilized on western blots. Journal of Immunology. 168:5645-5651.
25. Gadhoum SZ, Sackstein R. 2008. CD15 expression in human myeloid cell differentiation is regulated by sialidase activity. Nat Chem Biol. 4:751-757.
26. Gascon E, Vutskits L, Kiss JZ. 2007. Polysialic acid-neural cell adhesion molecule in brain plasticity: From synapses to integration of new neurons. Brain Res Rev. 56:101-118.
27. Glaser T, Brose C, Franceschini I, Hamann K, Smorodchenko A, Zipp F, Dubois-Dalcq M, Brustle O. 2007. Neural cell adhesion molecule polysialylation enhances the sensitivity of embryonic stem cell-derived neural precursors to migration guidance cues. Stem Cells. 25:3016-3025.
28. Goncharova V, Das S, Niles W, Schraufstatter I, Wong AK, Povaly T, Wakeman D, Miller L, Snyder EY, Khaldoyanidi SK. 2014. Homing of neural stem cells from the venous compartment into a brain infarct does not involve conventional interactions with vascular endothelium. Stem Cells Translational Medicine. 3:229-240.
29. Hess DC, Borlongan CV. 2008. Stem cells and neurological diseases. Cell Proliferation. 41 Suppl 1:94-114.
30. Horie K, Sakagami M, Kuramochi K, Ito T, Hamana H. 2000. Effect of the sialyl Lewis X (SLe(x)) moiety on splenic accumulation of SLe(x)-carboxymethylpullulan conjugate. Microbiology and Immunology. 44:401-404.
31. Horie K, Sakagami M, Masuda K, Notoya M, Hamana H, Yoshikawa T, Hirano K. 2004. Sialyl Lewis X-carboxymethylpullulan conjugate: A novel homing device to spleen and lymph nodes. Biological & Pharmaceutical Bulletin. 27:1275-1280.
32. Imitola J, Chitnis T, Khoury SJ. 2006. Insights into the molecular pathogenesis of progression in multiple sclerosis: Potential implications for future therapies. Arch Neurol. 63:25-33.
33. Imitola J, Comabella M, Chandraker AK, Dangond F, Sayegh MH, Snyder EY, Khoury SJ. 2004. Neural stem/progenitor cells express costimulatory molecules that are differentially regulated by inflammatory and apoptotic stimuli. The American Journal of Pathology. 164:1615-1625.
34. Imitola J, Cote D, Rasmussen S, Xie XS, Liu Y, Chitnis T, Sidman RL, Lin CP, Khoury SJ. 2011. Multimodal coherent anti-Stokes Raman scattering microscopy reveals microglia-associated myelin and axonal dysfunction in multiple sclerosis-like lesions in mice. Journal of Biomedical Optics. 16:021109.
35. Imitola J, Raddassi K, Park KI, Mueller FJ, Nieto M, Teng YD, Frenkel D, Li J, Sidman RL, Walsh CA, et al. 2004. Directed migration of neural stem cells to sites of CNS injury by the stromal cell-derived factor 1alpha/CXC chemokine receptor 4 pathway. Proceedings of the National Academy of Sciences of the United States of America. 101:18117-18122.
36. Ji JF, He BP, Dheen ST, Tay SS. 2004. Expression of chemokine receptors CXCR4, CCR2, CCR5 and CX3CR1 in neural progenitor cells isolated from the subventricular zone of the adult rat brain. Neuroscience Letters. 355:236-240.
37. Justicia C, Martin A, Rojas S, Gironella M, Cervera A, Panes J, Chamorro A, Planas AM. 2006. Anti-VCAM-1 antibodies did not protect against ischemic damage either in rats or in mice. J Cereb Blood Flow Metab. 26:421-432.
38. Kumar A, Torii T, Ishino Y, Muraoka D, Yoshimura T, Togayachi A, Narimatsu H, Ikenaka K, Hitoshi S. 2013. The Lewis X-related alpha1, 3-fucosyltransferase, Fut10, is required for the maintenance of stem cell populations. The Journal of Biological Chemistry. 288:28859-28868.
39. Laterza C, Merlini A, De Feo D, Ruffini F, Menon R, Onorati M, Fredrickx E, Muzio L, Lombardo A, Comi G, et al. 2013. iPSC-derived neural precursors exert a neuroprotective role in immune-mediated demyelination via the secretion of LIF. Nature Communications. 4:2597.
40. Lavdas AA, Franceschini I, Dubois-Dalcq M, Matsas R. 2006. Schwann cells genetically engineered to express PSA show enhanced migratory potential without impairment of their myelinating ability in vitro. Glia. 53:868-878.
41. Lee SJ, Benveniste EN. 1999. Adhesion molecule expression and regulation on cells of the central nervous system. Journal of Neuroimmunology. 98:77-88.
42. Lee ST, Chu K, Jung KH, Kim SJ, Kim DH, Kang KM, Hong NH, Kim JH, Ban JJ, Park HK, et al. 2008. Anti-inflammatory mechanism of intravascular neural stem cell transplantation in haemorrhagic stroke. Brain: A Journal of Neurology. 131:616-629.
43. Leone DP, Relvas JB, Campos LS, Hemmi S, Brakebusch C, Fassler R, Ffrench-Constant C, Suter U. 2005. Regulation of neural progenitor proliferation and survival by beta1 integrins. J Cell Sci. 118:2589-2599.
44. Leppanen A, White SP, Helin J, McEver RP, Cummings RD. 2000. Binding of glycosulfopeptides to P-selectin requires stereospecific contributions of individual tyrosine sulfate and sugar residues. The Journal of Biological Chemistry. 275:39569-39578.
45. Liu H, Zhang J, Liu CY, Wang IJ, Sieber M, Chang J, Jester JV, Kao WW. 2010. Cell therapy of congenital corneal diseases with umbilical mesenchymal stem cells: Lumican null mice. PloS One. 5:e10707.
46. Maness PF, Schachner M. 2007. Neural recognition molecules of the immunoglobulin superfamily: Signaling transducers of axon guidance and neuronal migration. Nature Neuroscience. 10:19-26.
47. Martino G, Pluchino S. 2006. The therapeutic potential of neural stem cells. Nat Rev Neurosci. 7:395-406.
48. Merzaban JS, Burdick MM, Gadhoum SZ, Dagia NM, Chu JT, Fuhlbrigge RC, Sackstein R. 2011. Analysis of glycoprotein E-selectin ligands on human and mouse marrow cells enriched for hematopoietic stem/progenitor cells. Blood. 118:1774-1783.
49. Mollicone R, Moore SE, Bovin N, Garcia-Rosasco M, Candelier JJ, Martinez-Duncker I, Oriol R. 2009. Activity, splice variants, conserved peptide motifs, and phylogeny of two new alpha1,3-fucosyltransferase families (FUT10 and FUT11). The Journal of Biological Chemistry. 284:4723-4738.
50. Phinney DG, Prockop DJ. 2007. Concise review: Mesenchymal stem/multipotent stromal cells: The state of transdifferentiation and modes of tissue repair - current views. Stem cells (Dayton, Ohio). 25:2896-2902.
51. Piccio L, Rossi B, Colantonio L, Grenningloh R, Gho A, Ottoboni L, Homeister JW, Scarpini E, Martinello M, Laudanna C, et al. 2005. Efficient recruitment of lymphocytes in inflamed brain venules requires expression of cutaneous lymphocyte antigen and fucosyltransferase-VII. Journal of Immunology. 174:5805-5813.
52. Piccio L, Rossi B, Scarpini E, Laudanna C, Giagulli C, Issekutz AC, Vestweber D, Butcher EC, Constantin G. 2002. Molecular mechanisms involved in lymphocyte recruitment in inflamed brain microvessels: Critical roles for P-selectin glycoprotein ligand-1 and heterotrimeric G(i)-linked receptors. Journal of Immunology. 168:1940-1949.
53. Pluchino S, Quattrini A, Brambilla E, Gritti A, Salani G, Dina G, Galli R, Del Carro U, Amadio S, Bergami A, et al. 2003. Injection of adult neurospheres induces recovery in a chronic model of multiple sclerosis. Nature. 422:688-694.
54. Pluchino S, Zanotti L, Brini E, Ferrari S, Martino G. 2009. Regeneration and repair in multiple sclerosis: The role of cell transplantation. Neuroscience Letters. 456:101-106.
55. Pluchino S, Zanotti L, Rossi B, Brambilla E, Ottoboni L, Salani G, Martinello M, Cattalini A, Bergami A, Furlan R, et al. 2005. Neurosphere-derived multipotent precursors promote neuroprotection by an immunomodulatory mechanism. Nature. 436:266-271.
56. Politi LS, Bacigaluppi M, Brambilla E, Cadioli M, Falini A, Comi G, Scotti G, Martino G, Pluchino S. 2007. Magnetic-resonance-based tracking and quantification of intravenously injected neural stem cell accumulation in the brains of mice with experimental multiple sclerosis. Stem Cells. 25:2583-2592.
57. Polley MJ, Phillips ML, Wayner E, Nudelman E, Singhal AK, Hakomori S, Paulson JC. 1991. CD62 and endothelial cell-leukocyte adhesion molecule 1 (ELAM-1) recognize the same carbohydrate ligand, sialyl-Lewis x. Proceedings of the National Academy of Sciences of the United States of America. 88:6224-6228.
58. Rampon C, Weiss N, Deboux C, Chaverot N, Miller F, Buchet D, Tricoire-Leignel H, Cazaubon S, Baron-Van Evercooren A, Couraud PO. 2008. Molecular mechanism of systemic delivery of neural precursor cells to the brain: Assembly of brain endothelial apical cups and control of transmigration by CD44. Stem Cells. 26:1673-1682.
59. Rasmussen S, Wang Y, Kivisakk P, Bronson RT, Meyer M, Imitola J, Khoury SJ. 2007. Persistent activation of microglia is associated with neuronal dysfunction of callosal projecting pathways and multiple sclerosis-like lesions in relapsing - remitting experimental autoimmune encephalomyelitis. Brain: A Journal of Neurology. 130:2816-2829.
60. Redl H, Dinges HP, Buurman WA, van der Linden CJ, Pober JS, Cotran RS, Schlag G. 1991. Expression of endothelial leukocyte adhesion molecule-1 in septic but not traumatic/hypovolemic shock in the baboon. The American Journal of Pathology. 139:461-466.
61. Rosen SD. 2004. Ligands for L-selectin: Homing, inflammation, and beyond. Annu Rev Immunol. 22:129-156.
62. Rutishauser U. 2008. Polysialic acid in the plasticity of the developing and adult vertebrate nervous system. Nat Rev Neurosci. 9:26-35.
63. Sackstein R. 2004. The bone marrow is akin to skin: HCELL and the biology of hematopoietic stem cell homing. J Invest Dermatol. 122:1061-1069.
64. Sackstein R. 2005. The lymphocyte homing receptors: Gatekeepers of the multistep paradigm. Curr Opin Hematol. 12:444-450.
65. Sackstein R, Fuhlbrigge R. 2006. The blot rolling assay: A method for identifying adhesion molecules mediating binding under shear conditions. Methods in Molecular Biology. 341:217-226.
66. Sackstein R, Merzaban JS, Cain DW, Dagia NM, Spencer JA, Lin CP, Wohlgemuth R. 2008. Ex vivo glycan engineering of CD44 programs human multipotent mesenchymal stromal cell trafficking to bone. Nature Medicine. 14:181-187.
67. Schweitzer KM, Drager AM, van der Valk P, Thijsen SF, Zevenbergen A, Theijsmeijer AP, van der Schoot CE, Langenhuijsen MM. 1996. Constitutive expression of E-selectin and vascular cell adhesion molecule-1 on endothelial cells of hematopoietic tissues. The American Journal of Pathology. 148:165-175.
68. Springer TA. 1994. Traffic signals for lymphocyte recirculation and leukocyte emigration: The multistep paradigm. Cell. 76:301-314.
69. Vitry S, Avellana-Adalid V, Lachapelle F, Evercooren AB. 2001. Migration and multipotentiality of PSA-NCAM+ neural precursors transplanted in the developing brain. Molecular and Cellular Neurosciences. 17:983-1000.
70. Wang Y, Imitola J, Rasmussen S, O'Connor KC, Khoury SJ. 2008. Paradoxical dysregulation of the neural stem cell pathway sonic hedgehog-Gli1 in autoimmune encephalomyelitis and multiple sclerosis. Annals of Neurology. 64:417-427.
71. Wang L, Shi J, van Ginkel FW, Lan L, Niemeyer G, Martin DR, Snyder EY, Cox NR. 2009. Neural stem/progenitor cells modulate immune responses by suppressing T lymphocytes with nitric oxide and prostaglandin E2. Experimental Neurology. 216:177-183.
72. Washington R, Burton J, Todd RF 3rd, Newman W, Dragovic L, Dore-Duffy P. 1994. Expression of immunologically relevant endothelial cell activation antigens on isolated central nervous system microvessels from patients with multiple sclerosis. Annals of Neurology. 35:89-97.
73. Weishaupt A, Jander S, Bruck W, Kuhlmann T, Stienekemeier M, Hartung T, Toyka KV, Stoll G, Gold R. 2000. Molecular mechanisms of high-dose antigen therapy in experimental autoimmune encephalomyelitis: Rapid induction of Th1-type cytokines and inducible nitric oxide synthase. Journal of Immunology. 165:7157-7163.
74. Zarbock A, Kempf T, Wollert KC, Vestweber D. 2012. Leukocyte integrin activation and deactivation: Novel mechanisms of balancing inflammation. Journal of Molecular Medicine. 90:353-359.
75. Zarbock A, Lowell CA, Ley K. 2007. Spleen tyrosine kinase Syk is necessary for E-selectin-induced alpha(L)beta(2) integrin-mediated rolling on intercellular adhesion molecule-1. Immunity. 26:773-783.
76. Zhang H, Vutskits L, Calaora V, Durbec P, Kiss JZ. 2004. A role for the polysialic acid-neural cell adhesion molecule in PDGF-induced chemotaxis of oligodendrocyte precursor cells. J Cell Sci. 117:93-103.
77. Ziv Y, Avidan H, Pluchino S, Martino G, Schwartz M. 2006. Synergy between immune cells and adult neural stem/progenitor cells promotes functional recovery from spinal cord injury. Proceedings of the National Academy of Sciences of the United States of America. 103:13174-13179.