Gaucher iPSC-derived macrophages produce elevated levels of inflammatory mediators and serve as a new platform for therapeutic development

Stem Cells

Volumn 32, Issue 9, 2014, Pages 2338-2349

  Panicker, Leelamma M ^a   Miller, Diana ^a   Awad, Ola ^a   Bose, Vivek ^a   Lun, Yu ^a   Park, Tea Soon ^b,c   Zambidis, Elias T ^b,c   Sgambato, Judi A ^a   Feldman, Ricardo A ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

Cell biology; Experimental models; Induced pluripotent stem cells; Monocyte; Reprogramming

Indexed keywords

AMBROXOL; CHAPERONE; CHITOTRIOSIDASE; IMIGLUCERASE; INTERLEUKIN 1BETA; INTERLEUKIN 6; ISOFAGOMINE; LIPOPOLYSACCHARIDE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; CYTOKINE;

ANIMAL CELL; ARTICLE; BONE MARROW BIOPSY; CELL DIFFERENTIATION; CONTROLLED STUDY; DISEASE CLASSIFICATION; ERYTHROCYTE; GAUCHER DISEASE; HUMAN; HUMAN CELL; MACROPHAGE; MACROPHAGE ACTIVATION; MALE; MOUSE; MULTIPLE MYELOMA; NONHUMAN; PHENOTYPE; PLURIPOTENT STEM CELL; ANIMAL; BIOSYNTHESIS; DRUG EFFECTS; FEMALE; GENETICS; METABOLISM; NONOBESE DIABETIC MOUSE; PATHOLOGY; SCID MOUSE;

ANIMALS; CELL DIFFERENTIATION; CYTOKINES; FEMALE; GAUCHER DISEASE; HUMANS; INDUCED PLURIPOTENT STEM CELLS; MACROPHAGES; MALE; MICE; MICE, INBRED NOD; MICE, SCID;

EID: 84906248420     PISSN: 10665099     EISSN: 15494918     Source Type: Journal    
DOI: 10.1002/stem.1732     Document Type: Article

References (60)

1. Messner MC, Cabot MC,. Glucosylceramide in Humans. Adv Exp Med Biol 2010; 688: 156-164.
2. Beutler E, Grabowski GA., Gaucher disease. In:, Scriver C, Beaudet AL, Sly WS, Valle D, eds. The Metabolic and Molecular Bases of Inherited Disease. 8th ed. New York: McGraw-Hill; 2001; 3635-3668.
3. Jmoudiak M, Futerman AH,. Gaucher disease: Pathological mechanisms and modern management. Br J Haematol 2005; 129: 178-188.
4. Sidransky E,. Gaucher disease: Complexity in a "simple" disorder. Mol Genet Metab 2004; 83: 6-15.
5. Barak V, Acker M, Nirman B, et al. Cytokines in Gaucher's disease. Eur Cytokine Netw 1999; 10: 205-210.
6. Hollak CE, van Weely S, van Oers MH, et al. Marked elevation of plasma chitotriosidase activity. A novel hallmark of Gaucher disease. J Clin Invest 1994; 93: 1288-1292.
7. Boot RG, Renkema GH, Verhoek M, et al. The human chitotriosidase gene. Nature of inherited enzyme deficiency. J Biol Chem 1998; 273: 25680-25685.
8. Brady RO,. Enzyme replacement for lysosomal diseases. Annu Rev Med 2006; 57: 283-296.
9. Ron I, Horowitz M,. ER retention and degradation as the molecular basis underlying Gaucher disease heterogeneity. Hum Mol Genet 2005; 14: 2387-2398.
10. Shen JS, Edwards NJ, Hong YB, et al. Isofagomine increases lysosomal delivery of exogenous glucocerebrosidase. Biochem Biophys Res Commun 2008; 369: 1071-1075.
11. Yu Z, Sawkar AR, Kelly JW,. Pharmacologic chaperoning as a strategy to treat Gaucher disease. FEBS J 2007; 274: 4944-4950.
12. Maegawa GHB, Tropak MB, Buttner JD, et al. Identification and characterization of ambroxol as an enzyme enhancement agent for Gaucher disease. J Biol Chem 2009; 284: 23502-23516.
13. Khanna R, Benjamin ER, Pellegrino L, et al. The pharmacological chaperone isofagomine increases the activity of the Gaucher disease L444P mutant form of β-glucosidase. FEBS J 2010; 277: 1618-1638.
14. Sun Y, Lou B, Xu YH, et al. Ex vivo and in vivo effects of isofagomine on acid β-glucosidase variants and substrate levels in Gaucher disease. J Biol Chem 2011; 287: 4275-4287.
15. Zimran A, Altarescu G, Elstein D., Pilot study using ambroxol as a pharmacological chaperone in type 1 Gaucher disease. Blood Cells Mol Dis 2013; 50: 134-137.
16. Takahashi K, Tanabe K, Ohnuki M, et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007; 131: 861-872.
17. Park IH, Arora N, Huo H, et al. Disease-specific induced pluripotent stem cells. Cell 2008; 134: 877-886.
18. Yu J, Vodyanik MA, Smuga-Otto K, et al. Induced pluripotent stem cell lines derived from human somatic cells. Science 2007; 318: 1917-1920.
19. Cherry AB, Daley GQ,. Reprogrammed cells for disease modeling and regenerative medicine. Annu Rev Med 2013; 64: 277-290.
20. Robinton DA, Daley GQ,. The promise of induced pluripotent stem cells in research and therapy. Nature 2012; 481: 295-305.
21. Panicker LM, Miller D, Park TS, et al. Induced pluripotent stem cell model recapitulates pathologic hallmarks of Gaucher disease. Proc Natl Acad Sci U S A 2012; 109: 18054-18059.
22. Tucker KL, Wang Y, Dausman J, et al. A transgenic mouse strain expressing four drug-selectable marker genes. Nucl Acids Res 1997; 25: 3745-3746.
23. Sommer CA, Stadtfeld M, Murphy GJ, et al. Induced pluripotent stem cell generation using a single lentiviral stem cell cassette. Stem Cells 2009; 27: 543-549.
24. Cormand B, Harboe TL, Gort L, et al. Mutation analysis of Gaucher disease patients from Argentina: High prevalence of the RecNciI mutation. Am J Med Genet 1998; 80: 343-351.
25. Ban H, Nishishita N, Fusaki N, et al. Efficient generation of transgene-free human induced pluripotent stem cells (iPSCs) by temperature-sensitive Sendai virus vectors. Proc Natl Acad Sci U S A 2011; 108: 14234-14239.
26. Choi JH, Stubblefield B, Cookson MR, et al. Aggregation of-α-synuclein in brain samples from subjects with glucocerebrosidase mutations. Mol Genet Metab 2011; 104: 185-188.
27. van Eijk M, van Roomen CP, Renkema GH, et al. Characterization of human phagocyte-derived chitotriosidase, a component of innate immunity. Int Immunol 2005; 17: 1505-1512.
28. Sutterwala FS, Noel GJ, Salgame P, et al. Reversal of proinflammatory responses by ligating the macrophage Fcgamma receptor type I. J Exp Med 1998; 188: 217-222.
29. Hollak CE, Evers L, Aerts JM, et al. Elevated levels of M-CSF, sCD14 and IL8 in type 1 Gaucher disease. Blood Cells Mol Dis 1997; 23: 201-212.
30. Michelakakis H, Spanou C, Kondyli A, et al. Plasma tumor necrosis factor-a (TNF-a) levels in Gaucher disease. Biochim Biophys Acta 1996; 1317: 219-222.
31. Adelino TE, Martins GG, Gomes AA, et al. Biochemical and molecular chitotriosidase profiles in patients with Gaucher disease type 1 in Minas Gerais, Brazil: New mutation in CHIT1 gene. JIMD Rep 2012; 9: 85-91.
32. Bussink AP, van Eijk M, Renkema GH, et al. The biology of the Gaucher cell: The cradle of human chitinases. Int Rev Cytol 2006; 252: 71-128.
33. Dekker N, van Dussen L, Hollak CE, et al. Elevated plasma glucosylsphingosine in Gaucher disease: Relation to phenotype, storage cell markers, and therapeutic response. Blood 2011; 118: e118-127.
34. Tropak MB, Kornhaber GJ, Rigat BA, et al. Identification of pharmacological chaperones for Gaucher disease and characterization of their effects on β-glucocerebrosidase by hydrogen/deuterium exchange mass spectrometry. Chembiochem 2008; 9: 2650-2662.
35. Bebdikov-Bar I, MG, Filocamo, M, Horowitz, M,. Ambroxol as a pharmacological chaperone for mutant glucocerebrosidase. Blood Cells Mol Dis. 2013; 50: 141-145.
36. Naito M, Takahashi K, Hojo H,. An ultrastructural and experimental study on the development of tubular structures in the lysosomes of Gaucher cells. Lab Invest 1988; 58: 590-598.
37. Bitton A, Etzell J, Grenert JP, et al. Erythrophagocytosis in Gaucher cells. Arch Pathol Lab Med 2004; 128: 1191-1192.
38. Mistry PK, Liu J, Yang M, et al. Glucocerebrosidase gene-deficient mouse recapitulates Gaucher disease displaying cellular and molecular dysregulation beyond the macrophage. Proc Natl Acad Sci U S A 2010; 107: 19473-19478.
39. Xu YH, Jia L, Quinn B, et al. Global gene expression profile progression in Gaucher disease mouse models. BMC Genomics 2011; 12: 20.
40. Ito S, Ansari P, Sakatsume M, et al. Interleukin-10 inhibits expression of both interferon-α- and interferon gamma-induced genes by suppressing tyrosine phosphorylation of STAT1. Blood 1999; 93: 1456-1463.
41. Donnelly RP, Dickensheets H, Finbloom DS,. The interleukin-10 signal transduction pathway and regulation of gene expression in mononuclear phagocytes. J Interferon Cytokine Res 1999; 19: 563-573.
42. Taddei TH, Kacena KA, Yang M, et al. The underrecognized progressive nature of N370S Gaucher disease and assessment of cancer risk in 403 patients. Am J Hematol 2009; 84: 208-214.
43. de Fost M, Out TA, de Wilde FA, et al. Immunoglobulin and free light chain abnormalities in Gaucher disease type I: Data from an adult cohort of 63 patients and review of the literature. Ann Hematol 2008; 87: 439-449.
44. Liu J, Halene S, Yang M, et al. Gaucher disease gene GBA functions in immune regulation. Proc Natl Acad Sci U S A 2012; 109: 10018-10023.
45. Pavlova EV, Wang SZ, Archer J, et al. B cell lymphoma and myeloma in murine Gaucher's disease. J Pathol. 2013; 231: 88-97.
46. Torcia M, Lucibello M, Vannier E, et al. Modulation of osteoclast-activating factor activity of multiple myeloma bone marrow cells by different interleukin-1 inhibitors. Exp Hematol 1996; 24: 868-874.
47. Lust JA, Donovan KA,. The role of interleukin-1 β in the pathogenesis of multiple myeloma. Hematol Oncol Clin North Am 1999; 13: 1117-1125.
48. Dinarello CA,. A clinical perspective of IL-1β as the gatekeeper of inflammation. Eur J Immunol 2011; 41: 1203-1217.
49. Dinarello CA,. Blocking interleukin-1β in acute and chronic autoinflammatory diseases. J Intern Med 2011; 269: 16-28.
50. Brautbar A, Elstein D, Pines G, et al. Effect of enzyme replacement therapy on gammopathies in Gaucher disease. Blood Cells Mol Dis 2004; 32: 214-217.
51. Grosbois B, Rose C, Noel E, et al. Gaucher disease and monoclonal gammopathy: A report of 17 cases and impact of therapy. Blood Cells Mol Dis 2009; 43: 138-139.
52. Machaczka M, Klimkowska M, Regenthal S, et al. Gaucher disease with foamy transformed macrophages and erythrophagocytic activity. J Inherit Metab Dis 2011; 34: 233-235.
53. Czartoryska B, Tylki-Szymanska A, Gorska D,. Serum chitotriosidase activity in Gaucher patients on enzyme replacement therapy (ERT). Clin Biochem 1998; 31: 417-420.
54. de Fost M, Hollak CE, Groener JE, et al. Superior effects of high-dose enzyme replacement therapy in type 1 Gaucher disease on bone marrow involvement and chitotriosidase levels: A 2-center retrospective analysis. Blood 2006; 108: 830-835.
55. Dwek RA, Butters TD, Platt FM, et al. Targeting glycosylation as a therapeutic approach. Nat Rev Drug Discov 2002; 1: 65-75.
56. Grace ME, Graves PN, Smith FI, et al. Analyses of catalytic activity and inhibitor binding of human acid β-glucosidase by site-directed mutagenesis. Identification of residues critical to catalysis and evidence for causality of two Ashkenazi Jewish Gaucher disease type 1 mutations. J Biol Chem 1990; 265: 6827-6835.
57. Babajani G, Tropak MB, Mahuran DJ, et al. Pharmacological chaperones facilitate the post-ER transport of recombinant N370S mutant β-glucocerebrosidase in plant cells: Evidence that N370S is a folding mutant. Mol Genet Metab 2012; 106: 323-329.
58. Hodanova K, Melkova Z, Horowitz M, et al. Transient expression of wild-type and mutant glucocerebrosidases in hybrid vaccinia expression system. Eur J Hum Genet 2003; 11: 369-374.
59. Oulaidi F, Front-Deschamps S, Gallienne E, et al. Second-generation iminoxylitol-based pharmacological chaperones for the treatment of Gaucher disease. Chem Med Chem 2011; 6: 353-361.
60. Steet RA, Chung S, Wustman B, et al. The iminosugar isofagomine increases the activity of N370S mutant acid β-glucosidase in Gaucher fibroblasts by several mechanisms. Proc Natl Acad Sci U S A 2006; 103: 13813-13818.\