Heparan sulfate inhibits hematopoietic stem and progenitor cell migration and engraftment in mucopolysaccharidosis I

Journal of Biological Chemistry

Volumn 289, Issue 52, 2014, Pages 36194-36203

  Watson, H Angharad ^a   Holley, Rebecca J ^a,b   Langford Smith, Kia J ^a   Wilkinson, Fiona L ^a   Van Kuppevelt, Toin H ^c   Wynn, Robert F ^d   Wraith, J Edmond ^e   Merry, Catherine L R ^b   Bigger, Brian W ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

^c RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^d ROYAL MANCHESTER CHILDREN S HOSPITAL   (United Kingdom)

^e ST MARY S HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CELLS; CYTOLOGY; PATIENT TREATMENT; SULFUR COMPOUNDS;

DERMATAN SULFATE; GENETIC DEFICIENCIES; GLYCOSAMINOGLYCANS; HEMATOPOIETIC CELL; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HEPARAN SULFATES; NEURODEGENERATION; POTENTIAL MECHANISM;

STEM CELLS;

DERMATAN SULFATE; GIANTIN; HEPARAN SULFATE; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 2; MEMBRANE PROTEIN; STROMAL CELL DERIVED FACTOR 1; UNCLASSIFIED DRUG; CXCL12 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW; BONE MARROW STROMA CELL; CELL COUNT; CELL HOMING; CELL SURFACE; COLONY FORMING UNIT; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENGRAFTMENT; EXTRACELLULAR MATRIX; FLOW CYTOMETRY; HEMATOPOIETIC STEM CELL; HURLER SYNDROME; LYSOSOME; MIGRATION INHIBITION; MOUSE; NONHUMAN; PROTEIN BINDING; PROTEIN INTERACTION; PROTEIN LOCALIZATION; ANIMAL; C57BL MOUSE; CELL MOTION; GRAFT SURVIVAL; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMAN; KNOCKOUT MOUSE; METABOLISM; MUCOPOLYSACCHARIDOSIS I; PATHOLOGY; PHYSIOLOGY; STEM CELL NICHE;

MUS;

ANIMALS; BONE MARROW; CELL MOVEMENT; CHEMOKINE CXCL12; GRAFT SURVIVAL; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HEMATOPOIETIC STEM CELLS; HEPARITIN SULFATE; HUMANS; MICE, INBRED C57BL; MICE, KNOCKOUT; MUCOPOLYSACCHARIDOSIS I; STEM CELL NICHE;

EID: 84919797754     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.599944     Document Type: Article

References (46)

1. Muenzer, J., Wraith, J. E., Clarke, L. A., and and the International Consensus Panel on the Management and Treatment of Mucopolysaccharidosis, I. (2009) Mucopolysaccharidosis I: Management and Treatment Guidelines. Pediatrics 123, 19-29
2. Wraith, J. E. (2005) The first 5 years of clinical experience with laronidase enzyme replacement therapy for mucopolysaccharidosis I. Expert Opin. Pharmacother 6, 489-506
3. Wraith, J. E. (2006) Limitations of enzyme replacement therapy: current and future. J. Inherit. Metab. Dis. 29, 442-447
4. Wilkinson, F. L., Sergijenko, A., Langford-Smith, K. J., Malinowska, M., Wynn, R. F., and Bigger, B. W. (2013) Busulfan conditioning enhances engraftment of hematopoietic donor-derived cells in the brain compared with irradiation. Molecular Therapy 21, 868-876
5. Boelens, J. J., Rocha, V., Aldenhoven, M., Wynn, R., O'Meara, A., Michel, G., Ionescu, I., Parikh, S., Prasad, V. K., Szabolcs, P., Escolar, M., Gluckman, E., Cavazzana-Calvo, M., Kurtzberg, J., Eurocord, I. e. W. P. o. E., and Duke, U. (2009) Risk factor analysis of outcomes after unrelated cord blood transplantation in patients with hurler syndrome. Biol. Blood Marrow Transplant 15, 618-625
6. Boelens, J. J., Wynn, R. F., O'Meara, A., Veys, P., Bertrand, Y., Souillet, G., Wraith, J. E., Fischer, A., Cavazzana-Calvo, M., Sykora, K. W., Sedlacek, P., Rovelli, A., Uiterwaal, C. S., and Wulffraat, N. (2007) Outcomes of hematopoietic stem cell transplantation for Hurler's syndrome in Europe: a risk factor analysis for graft failure. Bone Marrow Transplant 40, 225-233
7. Wynn, R. F., Wraith, J. E., Mercer, J., O'Meara, A., Tylee, K., Thornley, M., Church, H. J., and Bigger, B. W. (2009) Improved metabolic correction in patients with lysosomal storage disease treated with hematopoietic stem cell transplant compared with enzyme replacement therapy. J. Pediatr. 154, 609-611
8. de Ru, M. H., van der Tol, L., van Vlies, N., Bigger, B. W., Hollak, C. E., Ijlst, L., Kulik, W., van Lenthe, H., Saif, M. A., Wagemans, T., van der Wal, W. M., Wanders, R. J., and Wijburg, F. A. (2013) Plasma and urinary levels of dermatan sulfate and heparan sulfate derived disaccharides after longterm enzyme replacement therapy (ERT) in MPS I: correlation with the timing of ERT and with total urinary excretion of glycosaminoglycans. J. Inherited Metabolic Disease 36, 247-255
9. Fuller, M., Meikle, P. J., and Hopwood, J. J. (2004) Glycosaminoglycan degradation fragments in mucopolysaccharidosis I. Glycobiology 14, 443-450
10. Holley, R. J., Deligny, A., Wei, W., Watson, H. A., Niñonuevo, M. R., Dagälv, A., Leary, J. A., Bigger, B. W., Kjellén, L., and Merry, C. L. (2011) Mucopolysaccharidosis type I, unique structure of accumulated heparan sulfate and increased N-sulfotransferase activity in mice lacking α-l-iduronidase. J. Biol. Chem. 286, 37515-37524
11. Murphy, J. W., Cho, Y., Sachpatzidis, A., Fan, C., Hodsdon, M. E., and Lolis, E. (2007) Structural and functional basis of CXCL12 (stromal cellderived factor-1α) binding to heparin. J. Biol. Chem. 282, 10018-10027
12. Netelenbos, T., Zuijderduijn, S., Van Den Born, J., Kessler, F. L., Zweegman, S., Huijgens, P. C., and Dräger, A. M. (2002) Proteoglycans guide SDF-1-induced migration of hematopoietic progenitor cells. J. Leukocyte Biol. 72, 353-362
13. Proudfoot, A. E., Handel, T. M., Johnson, Z., Lau, E. K., LiWang, P., Clark-Lewis, I., Borlat, F., Wells, T. N., and Kosco-Vilbois, M. H. (2003) Glycosaminoglycan binding and oligomerization are essential for the in vivo activity of certain chemokines. Proc. Natl. Acad. Sci. U.S.A. 100, 1885-1890
14. Kuschert, G. S. V., Coulin, F., Power, C. A., Proudfoot, A. E. I., Hubbard, R. E., Hoogewerf, A. J., and Wells, T. N. C. (1999) Glycosaminoglycans Interact Selectively with Chemokines and Modulate Receptor Binding and Cellular Responses. Biochemistry 38, 12959-12968
15. Merry, C. L., Lyon, M., Deakin, J. A., Hopwood, J. J., and Gallagher, J. T. (1999) Highly sensitive sequencing of the sulfated domains of heparan sulfate. J. Biol. Chem. 274, 18455-18462
16. Wright, D. E., Bowman, E. P., Wagers, A. J., Butcher, E. C., and Weissman, I. L. (2002) Hematopoietic stem cells are uniquely selective in their migratory response to chemokines. J. Exp. Med. 195, 1145-1154
17. Ceradini, D. J., Kulkarni, A. R., Callaghan, M. J., Tepper, O. M., Bastidas, N., Kleinman, M. E., Capla, J. M., Galiano, R. D., Levine, J. P., and Gurtner, G. C. (2004) Progenitor cell trafficking is regulated by hypoxic gradients through HIF-1 induction of SDF-1. Nat. Med. 10, 858-864
18. Ponomaryov, T., Peled, A., Petit, I., Taichman, R. S., Habler, L., Sandbank, J., Arenzana-Seisdedos, F., Magerus, A., Caruz, A., Fujii, N., Nagler, A., Lahav, M., Szyper-Kravitz, M., Zipori, D., and Lapidot, T. (2000) Induction of the chemokine stromal-derived factor-1 following DNA damage improves human stem cell function. J. Clin. Invest. 106, 1331-1339
19. O'Boyle, G., Mellor, P., Kirby, J. A., and Ali, S. (2009) Anti-inflammatory therapy by intravenous delivery of non-heparan sulfate-binding CXCL12. FASEB J. 23, 3906-3916
20. Sadir, R., Baleux, F., Grosdidier, A., Imberty, A., and Lortat-Jacob, H. (2001) Characterization of the stromal cell-derived factor-1α-heparin complex. J. Biol. Chem. 276, 8288-8296
21. Clarke, L. A., Russell, C. S., Pownall, S., Warrington, C. L., Borowski, A., Dimmick, J. E., Toone, J., and Jirik, F. R. (1997) Murine mucopolysaccharidosis type I: targeted disruption of the murine α-L-iduronidase gene. Hum. Mol. Genet. 6, 503-511
22. Langford-Smith, A., Wilkinson, F. L., Langford-Smith, K. J., Holley, R. J., Sergijenko, A., Howe, S. J., Bennett, W. R., Jones, S. A., Wraith, J., Merry, C. L., Wynn, R. F., and Bigger, B. W. (2012) Hematopoietic Stem Cell and Gene Therapy Corrects Primary Neuropathology and Behavior in Mucopolysaccharidosis IIIA Mice. Molecular Therapy 20, 1610-1621
23. Sergijenko, A., Langford-Smith, A., Liao, A. Y., Pickford, C. E., McDermott, J., Nowinski, G., Langford-Smith, K. J., Merry, C. L., Jones, S. A., Wraith, J. E., Wynn, R. F., Wilkinson, F. L., and Bigger, B. W. (2013) Myeloid/Microglial Driven Autologous Hematopoietic Stem Cell Gene Therapy Corrects a Neuronopathic Lysosomal Disease. Molecular Therapy 21, 1938-1949
24. Siapati, E. K., Bigger, B. W., Miskin, J., Chipchase, D., Parsley, K. L., Mitrophanous, K., Themis, M., Thrasher, A. J., and Bonnet, D. (2005) Comparison of HIV- and EIAV-based vectors on their efficiency in transducing murine and human hematopoietic repopulating cells. Molecular Therapy 12, 537-546
25. Russo, F. P., Alison, M. R., Bigger, B. W., Amofah, E., Florou, A., Amin, F., Bou-Gharios, G., Jeffery, R., Iredale, J. P., and Forbes, S. J. (2006) The bone marrow functionally contributes to liver fibrosis. Gastroenterology 130, 1807-1821
26. Baldwin, R. J., ten Dam, G. B., van Kuppevelt, T. H., Lacaud, G., Gallagher, J. T., Kouskoff, V., and Merry, C. L. (2008) A developmentally regulated heparan sulfate epitope defines a subpopulation with increased blood potential during mesodermal differentiation. Stem cells 26, 3108-3118
27. Johnson, C. E., Crawford, B. E., Stavridis, M., Ten Dam, G., Wat, A. L., Rushton, G., Ward, C. M., Wilson, V., van Kuppevelt, T. H., Esko, J. D., Smith, A., Gallagher, J. T., and Merry, C. L. (2007) Essential alterations of heparan sulfate during the differentiation of embryonic stem cells to Sox1-enhanced green fluorescent protein-expressing neural progenitor cells. Stem Cells 25, 1913-1923
28. Wilkinson, F. L., Holley, R. J., Langford-Smith, K. J., Badrinath, S., Liao, A., Langford-Smith, A. W. W., Cooper, J. D., Jones, S. A., Wraith, J. E., Wynn, R. F., Merry, C. L. R., and Bigger, B. W. (2012) Neuropathology in Mouse Models of Mucopolysaccharidosis Type I, IIIA and IIIB. PLoS One 7, e35787
29. Baxter, M. A., Wynn, R. F., Schyma, L., Holmes, D. K., Wraith, J. E., Fairbairn, L. J., and Bellantuono, I. (2005) Marrow stromal cells from patients affected by MPS I differentially support haematopoietic progenitor cell development. J. Inherit. Metab. Dis. 28, 1045-1053
30. Albanese, P., Caruelle, D., Frescaline, G., Delbé, J., Petit-Cocault, L., Huet, E., Charnaux, N., Uzan, G., Papy-Garcia, D., and Courty, J. (2009) Glycosaminoglycan mimetics-induced mobilization of hematopoietic progenitors and stem cells into mouse peripheral blood: structure/function insights. Exp. Hematol. 37, 1072-1083
31. Sweeney, E. A., and Papayannopoulou, T. (2001) Increase in circulating SDF-1 after treatment with sulfated glycans. The role of SDF-1 in mobilization. Ann. N.Y. Acad. Sci. 938, 48-52; discussion 52-43
32. Gupta, P. (2006) Impairment of the activity of glycosaminoglycan-binding cytokines by functionally abnormal heparan sulfates: a novel mechanism underlying disease pathophysiology. Scientific World Journal 6, 452-456
33. Khan, S. A., Nelson, M. S., Pan, C., Gaffney, P. M., and Gupta, P. (2008) Endogenous Heparan Sulfate and Heparin Modulate Bone Morphogenetic Protein-4 (BMP-4) Signaling And Activity. Am. J. Physiol. Cell Physiol. 294, 1387-1397
34. Pan, C., Nelson, M. S., Reyes, M., Koodie, L., Brazil, J. J., Stephenson, E. J., Zhao, R. C., Peters, C., Selleck, S. B., Stringer, S. E., and Gupta, P. (2005) Functional abnormalities of heparan sulfate in mucopolysaccharidosis-I are associated with defective biologic activity of FGF-2 on human multipotent progenitor cells. Blood 106, 1956-1964
35. Deakin, J. A., and Lyon, M. (2008) A simplified and sensitive fluorescent method for disaccharide analysis of both heparan sulfate and chondroitin/ dermatan sulfates from biological samples. Glycobiology 18, 483-491
36. Lensen, J. F., Rops, A. L., Wijnhoven, T. J., Hafmans, T., Feitz, W. F., Oosterwijk, E., Banas, B., Bindels, R. J., van den Heuvel, L. P., van der Vlag, J., Berden, J. H., and van Kuppevelt, T. H. (2005) Localization and functional characterization of glycosaminoglycan domains in the normal human kidney as revealed by phage display-derived single chain antibodies. J. Am. Soc. Nephrol. 16, 1279-1288
37. Ten Dam, G. B., Kurup, S., van de Westerlo, E. M., Versteeg, E. M., Lindahl, U., Spillmann, D., and van Kuppevelt, T. H. (2006) 3-O-sulfated oligosaccharide structures are recognized by anti-heparan sulfate antibody HS4C3. J. Biol. Chem. 281, 4654-4662
38. van Kuppevelt, T. H., Dennissen, M. A., van Venrooij, W. J., Hoet, R. M. A., and Veerkamp, J. H. (1998) Generation and Application of Type-specific Anti-Heparan Sulfate Antibodies Using Phage Display Technology. Fur-ther Evidence for Heparan Sulfate Heterogeneity in the Kidney. J. Biol. Chem. 273, 12960-12966
39. Saif, M. A., Bigger, B. W., Brookes, K. E., Mercer, J., Tylee, K. L., Church, H. J., Bonney, D. K., Jones, S., Wraith, J. E., and Wynn, R. F. (2012) Hematopoietic stem cell transplantation improves the high incidence of neutralizing allo-antibodies observed in Hurler's syndrome after pharmacological enzyme replacement therapy. Haematologica 97, 1320-1328
40. David, G., Bai, X. M., Van der Schueren, B., Cassiman, J. J., and Van den Berghe, H. (1992) Developmental changes in heparan sulfate expression: in situ detection with mAbs. J. Cell Biol. 119, 961-975
41. Wilson, S., Hashamiyan, S., Clarke, L., Saftig, P., Mort, J., Dejica, V. M., and Brömme, D. (2009) Glycosaminoglycan-mediated loss of cathepsin K collagenolytic activity in MPS I contributes to osteoclast and growth plate abnormalities. Am. J. Pathol. 175, 2053-2062
42. Lawrence, R., Brown, J. R., Al-Mafraji, K., Lamanna, W. C., Beitel, J. R., Boons, G. J., Esko, J. D., and Crawford, B. E. (2012) Disease-specific nonreducing end carbohydrate biomarkers for mucopolysaccharidoses. Nat. Chem. Biol. 8, 197-204
43. Rueda, P., Richart, A., Récalde, A., Gasse, P., Vilar, J., Guérin, C., Lortat-Jacob, H., Vieira, P., Baleux, F., Chretien, F., Arenzana-Seisdedos, F., and Silvestre, J. S. (2012) Homeostatic and tissue reparation defaults in mice carrying selective genetic invalidation of CXCL12/proteoglycan interactions. Circulation 126, 1882-1895
44. Langford-Smith, K., Arasaradnam, M., Wraith, J. E., Wynn, R., and Bigger, B. W. (2010) Evaluation of heparin cofactor II-thrombin complex as a biomarker on blood spots from mucopolysaccharidosis I, IIIA and IIIB mice. Molecular Genetics Metabolism 99, 269-274
45. Langford-Smith, K. J., Mercer, J., Petty, J., Tylee, K., Church, H., Roberts, J., Moss, G., Jones, S., Wynn, R., Wraith, J. E., and Bigger, B. W. (2011) Heparin cofactor II-thrombin complex and dermatan sulphate:chondroitin sulphate ratio are biomarkers of short- and long-term treatment effects in mucopolysaccharide diseases. J. Inherited Metab. Dis. 34, 499-508
46. Langford-Smith, K. J., Sandiford, Z., Langford-Smith, A., Wilkinson, F. L., Jones, S. A., Wraith, J. E., Wynn, R. F., and Bigger, B. W. (2013) Signal One and Two Blockade Are Both Critical for Non-Myeloablative Murine HSCT across a Major Histocompatibility Complex Barrier. PloS one 8, e77632