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Journal of Immunology Research
Volume 2015 (2015), Article ID 192761, 6 pages
http://dx.doi.org/10.1155/2015/192761
Review Article

Pathogenesis of Bone Alterations in Gaucher Disease: The Role of Immune System

IIFP, Departamento de Ciencias Biológicas, Facultad de Ciencias Exactas, Universidad Nacional de La Plata y CONICET, 47 y 115, 1900 La Plata, Argentina

Received 8 October 2014; Revised 9 January 2015; Accepted 11 January 2015

Academic Editor: Giacomina Brunetti

Copyright © 2015 Juan Marcos Mucci and Paula Rozenfeld. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. P. J. Delves and I. M. Roitt, “The immune system. First of two parts,” The New England Journal of Medicine, vol. 343, no. 1, pp. 37–49, 2000. View at Publisher · View at Google Scholar · View at Scopus
  2. J. Xiong and C. A. O'Brien, “Osteocyte RANKL: new insights into the control of bone remodeling,” Journal of Bone and Mineral Research, vol. 27, no. 3, pp. 499–505, 2012. View at Publisher · View at Google Scholar · View at Scopus
  3. T. J. de Vries, T. Schoenmaker, B. Hooibrink, P. J. M. Leenen, and V. Everts, “Myeloid blasts are the mouse bone marrow cells prone to differentiate into osteoclasts,” Journal of Leukocyte Biology, vol. 85, no. 6, pp. 919–927, 2009. View at Publisher · View at Google Scholar · View at Scopus
  4. H. Takayanagi, K. Sato, A. Takaoka, and T. Taniguchi, “Interplay between interferon and other cytokine systems in bone metabolism,” Immunological Reviews, vol. 208, pp. 181–193, 2005. View at Publisher · View at Google Scholar · View at Scopus
  5. T. Yin and L. Li, “The stem cell niches in bone,” The Journal of Clinical Investigation, vol. 116, no. 5, pp. 1195–1201, 2006. View at Publisher · View at Google Scholar
  6. W. J. Boyle, W. S. Simonet, and D. L. Lacey, “Osteoclast differentiation and activation,” Nature, vol. 423, no. 6937, pp. 337–342, 2003. View at Publisher · View at Google Scholar · View at Scopus
  7. W. S. Simonet, D. L. Lacey, C. R. Dunstan et al., “Osteoprotegerin: a novel secreted protein involved in the regulation of bone density,” Cell, vol. 89, no. 2, pp. 309–319, 1997. View at Publisher · View at Google Scholar
  8. R. Siddappa, H. Fernandes, J. Liu, C. van Blitterswijk, and J. de Boer, “The response of human mesenchymal stem cells to osteogenic signals and its impact on bone tissue engineering,” Current Stem Cell Research and Therapy, vol. 2, no. 3, pp. 209–220, 2007. View at Publisher · View at Google Scholar · View at Scopus
  9. A. Leibbrandt and J. M. Penninger, “RANK/RANKL: regulators of immune responses and bone physiology,” Annals of the New York Academy of Sciences, vol. 1143, pp. 123–150, 2008. View at Publisher · View at Google Scholar · View at Scopus
  10. F. Kanamaru, H. Iwai, T. Ikeda, A. Nakajima, I. Ishikawa, and M. Azuma, “Expression of membrane-bound and soluble receptor activator of NF-kappaB ligand (RANKL) in human T cells,” Immunology Letters, vol. 94, no. 3, pp. 239–246, 2004. View at Publisher · View at Google Scholar · View at Scopus
  11. T. Nakashima, M. Hayashi, T. Fukunaga et al., “Evidence for osteocyte regulation of bone homeostasis through RANKL expression,” Nature Medicine, vol. 17, no. 10, pp. 1231–1234, 2011. View at Publisher · View at Google Scholar · View at Scopus
  12. T. Nakashima, Y. Kobayashi, S. Yamasaki et al., “Protein expression and functional difference of membrane-bound and soluble receptor activator of NF-κB ligand: modulation of the expression by osteotropic factors and cytokines,” Biochemical and Biophysical Research Communications, vol. 275, no. 3, pp. 768–775, 2000. View at Publisher · View at Google Scholar · View at Scopus
  13. H. Takayanagi, “Osteoimmunology: shared mechanisms and crosstalk between the immune and bone systems,” Nature Reviews Immunology, vol. 7, no. 4, pp. 292–304, 2007. View at Publisher · View at Google Scholar · View at Scopus
  14. E. M. Gravallese, Y. Harada, J.-T. Wang, A. H. Gorn, T. S. Thornhill, and S. R. Goldring, “Identification of cell types responsible for bone resorption in rheumatoid arthritis and juvenile rheumatoid arthritis,” The American Journal of Pathology, vol. 152, no. 4, pp. 943–951, 1998. View at Google Scholar · View at Scopus
  15. H. Takayanagi, H. Oda, S. Yamamoto et al., “A new mechanism of bone destruction in rheumatoid arthritis: synovial fibroblasts induce osteoclastogenesis,” Biochemical and Biophysical Research Communications, vol. 240, no. 2, pp. 279–286, 1997. View at Publisher · View at Google Scholar · View at Scopus
  16. R. L. Jilka, G. Hangoc, G. Girasole et al., “Increased osteoclast development after estrogen loss: mediation by interleukin-6,” Science, vol. 257, no. 5066, pp. 88–91, 1992. View at Publisher · View at Google Scholar · View at Scopus
  17. R. Pacifici, “Estrogen deficiency, T cells and bone loss,” Cellular Immunology, vol. 252, no. 1-2, pp. 68–80, 2008. View at Publisher · View at Google Scholar · View at Scopus
  18. L. Hillman, C. Schlotzhauer, D. Lee et al., “Decreased bone mineralization in children with phenylketonuria under treatment,” European Journal of Pediatrics, vol. 155, supplement 1, pp. S148–S152, 1996. View at Publisher · View at Google Scholar
  19. M. P. A. Hoeks, M. den Heijer, and M. C. H. Janssen, “Adult issues in phenylketonuria,” The Netherlands Journal of Medicine, vol. 67, no. 1, pp. 2–7, 2009. View at Google Scholar · View at Scopus
  20. I. Roato, F. Porta, A. Mussa et al., “Bone impairment in phenylketonuria is characterized by circulating osteoclast precursors and activated T cell increase,” PLoS ONE, vol. 5, no. 11, Article ID e14167, 2010. View at Publisher · View at Google Scholar · View at Scopus
  21. P. J. Meikle, J. J. Hopwood, A. E. Clague, and W. F. Carey, “Prevalence of lysosomal storage disorders,” The Journal of the American Medical Association, vol. 281, no. 3, pp. 249–254, 1999. View at Google Scholar
  22. J. Wittmann, E. Karg, S. Turi et al., “Newborn screening for lysosomal storage disorders in Hungary,” JIMD Reports, vol. 6, pp. 117–125, 2012. View at Publisher · View at Google Scholar
  23. G. A. Grabowski, “Gaucher disease and other storage disorders,” Hematology, vol. 2012, no. 1, pp. 13–18, 2012. View at Google Scholar · View at Scopus
  24. N. W. Barton, R. O. Brady, J. M. Dambrosia et al., “Replacement therapy for inherited enzyme deficiency—macrophage-targeted glucocerebrosidase for Gaucher's disease,” The New England Journal of Medicine, vol. 324, no. 21, pp. 1464–1470, 1991. View at Publisher · View at Google Scholar · View at Scopus
  25. P. Mistry and D. P. Germain, “Phenotype variations in Gaucher disease,” La Revue de Médecine Interne, vol. 27, supplement 1, pp. S3–S10, 2006. View at Publisher · View at Google Scholar
  26. A. Zimran, G. Altarescu, B. Rudensky, A. Abrahamov, and D. Elstein, “Survey of hematological aspects of Gaucher disease,” Hematology, vol. 10, no. 2, pp. 151–156, 2005. View at Publisher · View at Google Scholar · View at Scopus
  27. M. Itzchaki, E. Lebel, A. Dweck et al., “Orthopedic considerations in Gaucher disease since the advent of enzyme replacement therapy,” Acta Orthopaedica Scandinavica, vol. 75, no. 6, pp. 641–653, 2004. View at Publisher · View at Google Scholar · View at Scopus
  28. R. J. Wenstrup, M. Roca-Espiau, N. J. Weinreb, and B. Bembi, “Skeletal aspects of Gaucher disease: a review,” The British Journal of Radiology, vol. 75, supplement 1, pp. A2–A12, 2002. View at Publisher · View at Google Scholar · View at Scopus
  29. R. Katz, T. Booth, R. Hargunani, P. Wylie, and B. Holloway, “Radiological aspects of Gaucher disease,” Skeletal Radiology, vol. 40, no. 12, pp. 1505–1513, 2011. View at Publisher · View at Google Scholar · View at Scopus
  30. D. Elstein, A. J. Foldes, D. Zahrieh et al., “Significant and continuous improvement in bone mineral density among type 1 Gaucher disease patients treated with velaglucerase alfa: 69-month experience, including dose reduction,” Blood Cells, Molecules, & Diseases, vol. 47, no. 1, pp. 56–61, 2011. View at Publisher · View at Google Scholar · View at Scopus
  31. K. B. Sims, G. M. Pastores, N. J. Weinreb et al., “Improvement of bone disease by imiglucerase (Cerezyme) therapy in patients with skeletal manifestations of type 1 Gaucher disease: results of a 48-month longitudinal cohort study,” Clinical Genetics, vol. 73, no. 5, pp. 430–440, 2008. View at Publisher · View at Google Scholar · View at Scopus
  32. N. J. Weinreb, J. Goldblatt, J. Villalobos et al., “Long-term clinical outcomes in type 1 Gaucher disease following 10 years of imiglucerase treatment,” Journal of Inherited Metabolic Disease, vol. 36, no. 3, pp. 543–553, 2013. View at Publisher · View at Google Scholar
  33. J. Stirnemann, N. Belmatoug, C. Vincent, O. Fain, B. Fantin, and F. Mentré, “Bone events and evolution of biologic markers in Gaucher disease before and during treatment,” Arthritis Research and Therapy, vol. 12, no. 4, article R156, 2010. View at Google Scholar · View at Scopus
  34. P. K. Mistry, N. J. Weinreb, P. Kaplan, J. A. Cole, A. R. Gwosdow, and T. Hangartner, “Osteopenia in Gaucher disease develops early in life: response to imiglucerase enzyme therapy in children, adolescents and adults,” Blood Cells, Molecules, and Diseases, vol. 46, no. 1, pp. 66–72, 2011. View at Publisher · View at Google Scholar · View at Scopus
  35. H. Andersson, P. Kaplan, K. Kacena, and J. Yee, “Eight-year clinical outcomes of long-term enzyme replacement therapy for 884 children with gaucher disease type 1,” Pediatrics, vol. 122, no. 6, pp. 1182–1190, 2008. View at Publisher · View at Google Scholar · View at Scopus
  36. V. Barak, M. Acker, B. Nisman et al., “Cytokines in Gaucher's disease,” European Cytokine Network, vol. 10, no. 2, pp. 205–210, 1999. View at Google Scholar · View at Scopus
  37. C. E. M. Hollak, L. Evers, J. M. F. G. Aerts, and M. H. J. van Oers, “Elevated levels of M-CSF, sCD14 and IL8 in type 1 Gaucher disease,” Blood Cells, Molecules and Diseases, vol. 23, no. 2, pp. 201–212, 1997. View at Publisher · View at Google Scholar · View at Scopus
  38. H. Michelakakis, C. Spanou, A. Kondyli et al., “Plasma tumor necrosis factor-a (TNF-a) levels in Gaucher disease,” Biochimica et Biophysica Acta, vol. 1317, no. 3, pp. 219–222, 1996. View at Publisher · View at Google Scholar · View at Scopus
  39. R. G. Boot, M. Verhoek, M. de Fost et al., “Marked elevation of the chemokine CCL18/PARC in Gaucher disease: a novel surrogate marker for assessing therapeutic intervention,” Blood, vol. 103, no. 1, pp. 33–39, 2004. View at Publisher · View at Google Scholar · View at Scopus
  40. M. J. van Breemen, M. de Fost, J. S. A. Voerman et al., “Increased plasma macrophage inflammatory protein (MIP)-1alpha and MIP-1beta levels in type 1 Gaucher disease,” Biochimica et Biophysica Acta—Molecular Basis of Disease, vol. 1772, no. 7, pp. 788–796, 2007. View at Publisher · View at Google Scholar · View at Scopus
  41. M. Yoshino, Y. Watanabe, Y. Tokunaga et al., “Roles of specific cytokines in bone remodeling and hematopoiesis in Gaucher disease,” Pediatrics International, vol. 49, no. 6, pp. 959–965, 2007. View at Publisher · View at Google Scholar · View at Scopus
  42. S. Gordon and F. O. Martinez, “Alternative activation of macrophages: mechanism and functions,” Immunity, vol. 32, no. 5, pp. 593–604, 2010. View at Publisher · View at Google Scholar · View at Scopus
  43. L. A. Boven, M. van Meurs, R. G. Boot et al., “Gaucher cells demonstrate a distinct macrophage phenotype and resemble alternatively activated macrophages,” The American Journal of Clinical Pathology, vol. 122, no. 3, pp. 359–369, 2004. View at Publisher · View at Google Scholar · View at Scopus
  44. C. Braudeau, J. Graveleau, M. Rimbert et al., “Altered innate function of plasmacytoid dendritic cells restored by enzyme replacement therapy in Gaucher disease,” Blood Cells, Molecules, and Diseases, vol. 50, no. 4, pp. 281–288, 2013. View at Publisher · View at Google Scholar · View at Scopus
  45. F. Camou and J.-F. Viallard, “Extended remission of B-cell lymphoma with monoclonal gammopathy in a patient with type 1 Gaucher disease treated with enzyme replacement therapy,” Blood Cells, Molecules, and Diseases, vol. 48, no. 1, pp. 51–52, 2012. View at Publisher · View at Google Scholar · View at Scopus
  46. L. Lacerda, F. A. Arosa, R. Lacerda et al., “T cell numbers relate to bone involvement in Gaucher disease,” Blood Cells, Molecules, and Diseases, vol. 25, no. 2, pp. 130–138, 1999. View at Publisher · View at Google Scholar · View at Scopus
  47. A. Balreira, L. Lacerda, C. Sá Miranda, and F. A. Arosa, “Evidence for a link between sphingolipid metabolism and expression of CD1d and MHC-class II: monocytes from Gaucher disease patients as a model,” British Journal of Haematology, vol. 129, no. 5, pp. 667–676, 2005. View at Publisher · View at Google Scholar · View at Scopus
  48. G. E. Marti, E. T. Ryan, N. M. Papadopoulos et al., “Polyclonal B-cell lymphocytosis and hypergammaglobulinemia in patients with Gaucher disease,” American Journal of Hematology, vol. 29, no. 4, pp. 189–194, 1988. View at Publisher · View at Google Scholar · View at Scopus
  49. T. H. Taddei, K. A. Kacena, M. Yang et al., “The underrecognized progressive nature of N370S Gaucher disease and assessment of cancer risk in 403 patients,” American Journal of Hematology, vol. 84, no. 4, pp. 208–214, 2009. View at Publisher · View at Google Scholar · View at Scopus
  50. P. K. Mistry, J. Liu, M. Yang et al., “Glucocerebrosidase gene-deficient mouse recapitulates Gaucher disease displaying cellular and molecular dysregulation beyond the macrophage,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 45, pp. 19473–19478, 2010. View at Publisher · View at Google Scholar
  51. J. Liu, S. Halene, M. Yang et al., “Gaucher disease gene GBA functions in immune regulation,” Proceedings of the National Academy of Sciences of the United States of America, vol. 109, no. 25, pp. 10018–10023, 2012. View at Publisher · View at Google Scholar · View at Scopus
  52. M. K. Pandey, R. Rani, W. Zhang, K. Setchell, and G. A. Grabowski, “Immunological cell type characterization and Th1-Th17 cytokine production in a mouse model of Gaucher disease,” Molecular Genetics and Metabolism, vol. 106, no. 3, pp. 310–322, 2012. View at Publisher · View at Google Scholar · View at Scopus
  53. L. M. Panicker, D. Miller, O. Awad et al., “Gaucher iPSC-derived macrophages produce elevated levels of inflammatory mediators and serve as a new platform for therapeutic development,” Stem Cells (Dayton, Ohio), vol. 32, no. 9, pp. 2338–2349, 2014. View at Publisher · View at Google Scholar
  54. P. K. Mistry, J. Liu, L. Sun et al., “Glucocerebrosidase 2 gene deletion rescues type 1 Gaucher disease,” Proceedings of the National Academy of Sciences of the United States of America, vol. 111, no. 13, pp. 4934–4939, 2014. View at Publisher · View at Google Scholar · View at Scopus
  55. S. Lecourt, V. Vanneaux, A. Cras et al., “Bone marrow microenvironment in an in vitro model of gaucher disease: consequences of glucocerebrosidase deficiency,” Stem Cells and Development, vol. 21, no. 2, pp. 239–248, 2012. View at Publisher · View at Google Scholar · View at Scopus
  56. J. M. Mucci, R. Scian, P. N. De Francesco et al., “Induction of osteoclastogenesis in an in vitro model of Gaucher disease is mediated by T cells via TNF-α,” Gene, vol. 509, no. 1, pp. 51–59, 2012. View at Publisher · View at Google Scholar · View at Scopus
  57. J. M. Mucci, F. Suqueli García, P. N. de Francesco et al., “Uncoupling of osteoblast-osteoclast regulation in a chemical murine model of gaucher disease,” Gene, vol. 532, no. 2, pp. 186–191, 2013. View at Publisher · View at Google Scholar · View at Scopus
  58. M. Reed, R. J. Baker, A. B. Mehta, and D. A. Hughes, “Enhanced differentiation of osteoclasts from mononuclear precursors in patients with Gaucher disease,” Blood Cells, Molecules, and Diseases, vol. 51, no. 3, pp. 185–194, 2013. View at Publisher · View at Google Scholar · View at Scopus