Multipotent stromal cells alleviate inflammation, neuropathology, and symptoms associated with globoid cell leukodystrophy in the twitcher mouse

Stem Cells

Volumn 31, Issue 8, 2013, Pages 1523-1534

  Scruggs, Brittni A ^a   Zhang, Xiujuan ^a   Bowles, Annie C ^a,b   Gold, Peter A ^a   Semon, Julie A ^a   Fisher Perkins, Jeanne M ^c   Zhang, Shijia ^a   Bonvillain, Ryan W ^a   Myers, Leann ^d   Li, Su Chen ^a   Kalueff, Allan V ^a   Bunnell, Bruce A ^a,c  

^a TULANE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Tulane University   (United States)

^c TULANE UNIVERSITY   (United States)

^d TULANE UNIVERSITY   (United States)

Author keywords

Bone marrow derived stem cells; Globoid cell leukodystrophy; Mesenchymal stem cells multipotent stromal cells; Stem cell transplantation; Twitcher mouse

Indexed keywords

GALACTOSYLCERAMIDASE; GREEN FLUORESCENT PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; APOPTOSIS; ARTICLE; BODY WEIGHT; BRAIN LEVEL; CELL THERAPY; CELL TYPE; CONTROLLED STUDY; DISEASE COURSE; ENZYME ACTIVITY; FEMALE; GLOBOID CELL; GLOBOID CELL LEUKODYSTROPHY; HINDLIMB; IMMUNOFLUORESCENCE TEST; INFLAMMATORY CELL; LIFESPAN; LONGEVITY; MALE; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMA CELL; MOTOR PERFORMANCE; MOUSE; MULTIPOTENT STEM CELL; MUSCLE STRENGTH; NERVOUS SYSTEM INFLAMMATION; NEUROPATHOLOGY; NEWBORN; NONHUMAN; PHENOTYPE; REARING; SCIATIC NERVE; WESTERN BLOTTING;

BONE MARROW-DERIVED STEM CELLS; GLOBOID CELL LEUKODYSTROPHY; MESENCHYMAL STEM CELLS/MULTIPOTENT STROMAL CELLS; STEM CELL TRANSPLANTATION; TWITCHER MOUSE;

ANIMALS; BRAIN; DISEASE MODELS, ANIMAL; FEMALE; GENETIC THERAPY; INFLAMMATION; LEUKODYSTROPHY, GLOBOID CELL; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MULTIPOTENT STEM CELLS; STEM CELL TRANSPLANTATION; STROMAL CELLS; SURVIVAL ANALYSIS;

EID: 84883389121     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1002/stem.1397     Document Type: Article

References (69)

1. Hawkins-Salsbury JA, Reddy AS, Sands MS. Combination therapies for lysosomal storage disease: Is the whole greater than the sum of its parts? Hum Mol Genet 2011;20:R54-60.
2. Heese BA. Current strategies in the management of lysosomal storage diseases. Semin Pediatr Neurol 2008;15:119-126.
3. Hodges BL, Cheng SH. Cell and gene-based therapies for the lysosomal storage diseases. Curr Gene Ther 2006;6:227-241.
4. Suzuki K, Suzuki Y. Globoid cell leucodystrophy (Krabbe's disease): Deficiency of galactocerebroside beta-galactosidase. Proc Natl Acad Sci USA 1970;66:302-309.
5. Kolodny EH. Globoid Leukodystrophy. Amsterdam: Elsevier Science, 1996.
6. Sakai N. Pathogenesis of leukodystrophy for Krabbe disease: Molecular mechanism and clinical treatment. Brain Dev 2009;31:485-487.
7. Duffner PK, Barczykowski A, Jalal K et al. Early infantile Krabbe disease: Results of the World-Wide Krabbe Registry. Pediatr Neurol 2011;45:141-148.
8. Barone R, Brühl K, Stoeter P et al. Clinical and neuroradiological findings in classic infantile and late-onset globoid-cell leukodystrophy (Krabbe disease). Am J Med Genet 1996;63:209-217.
9. Costello DJ, Eichler AF, Eichler FS. Leukodystrophies: Classification, diagnosis, and treatment. Neurologist 2009;15:319-328.
10. Castelvetri LC, Givogri MI, Zhu H et al. Axonopathy is a compounding factor in the pathogenesis of Krabbe disease. Acta Neuropathol 2011;122:35-48.
11. Duchen LW, Eicher EM, Jacobs JM et al. Hereditary leucodystrophy in the mouse: The new mutant twitcher. Brain 1980;103:695-710.
12. Smith B, Galbiati F, Cantuti-Castelvetri L et al. Peripheral neuropathy in the Twitcher mouse involves the activation of axonal caspase 3. ASN Neuro 2011;3:e00066.
13. Scruggs BA, Bowles AC, Zhang X et al. High-throughput screening of stem cell therapy for globoid cell leukodystrophy using automated neurophenotyping of twitcher mice. Behav Brain Res 2012;236C:35-47.
14. Olmstead CE. Neurological and neurobehavioral development of the mutant 'twitcher' mouse. Behav Brain Res 1987;25:143-153.
15. Kobayashi T, Yamanaka T, Jacobs JM et al. The Twitcher mouse: An enzymatically authentic model of human globoid cell leukodystrophy (Krabbe disease). Brain Res 1980;202:479-483.
16. McGraw P, Liang L, Escolar M et al. Krabbe disease treated with hematopoietic stem cell transplantation: Serial assessment of anisotropy measurements - Initial experience. Radiology 2005;236:221-230.
17. Prasad VK, Kurtzberg J. Cord blood and bone marrow transplantation in inherited metabolic diseases: Scientific basis, current status and future directions. Br J Haematol 2010;148:356-372.
18. Escolar ML, Poe MD, Provenzale JM et al. Transplantation of umbilical-cord blood in babies with infantile Krabbe's disease. N Engl J Med 2005;352:2069-2081.
19. Hoogerbrugge PM, Poorthuis BJ, Romme AE et al. Effect of bone marrow transplantation on enzyme levels and clinical course in the neurologically affected twitcher mouse. J Clin Invest 1988;81:1790-1794.
20. Luzi P, Rafi MA, Zaka M et al. Biochemical and pathological evaluation of long-lived mice with globoid cell leukodystrophy after bone marrow transplantation. Mol Genet Metab 2005;86:150-159.
21. Wenger DA, Rafi MA, Luzi P et al. Krabbe disease: Genetic aspects and progress toward therapy. Mol Genet Metab 2000;70:1-9.
22. Lin D, Donsante A, Macauley S et al. Central nervous system-directed AAV2/5-mediated gene therapy synergizes with bone marrow transplantation in the murine model of globoid-cell leukodystrophy. Mol Ther 2007;15:44-52.
23. Qin EY, Hawkins-Salsbury JA, Jiang X et al. Bone marrow transplantation increases efficacy of central nervous system-directed enzyme replacement therapy in the murine model of globoid cell leukodystrophy. Mol Genet Metab 2012;107:186-196.
24. Martin PL, Carter SL, Kernan NA et al. Results of the cord blood transplantation study (COBLT): Outcomes of unrelated donor umbilical cord blood transplantation in pediatric patients with lysosomal and peroxisomal storage diseases. Biol Blood Marrow Transplant 2006;12: 184-194.
25. Reddy A, Wozniak D, Farber N et al. Bone marrow transplantation alters the tremor phenotype in the murine model of globoid-cell leukodystrophy. J Clin Med 2012;1:1-14.
26. Lee WC, Courtenay A, Troendle FJ et al. Enzyme replacement therapy results in substantial improvements in early clinical phenotype in a mouse model of globoid cell leukodystrophy. FASEB J 2005;19: 1549-1551.
27. Lee WC, Tsoi YK, Troendle FJ et al. Single-dose intracerebroventricular administration of galactocerebrosidase improves survival in a mouse model of globoid cell leukodystrophy. FASEB J 2007;21: 2520-2527.
28. Biswas S, LeVine SM. Substrate-reduction therapy enhances the benefits of bone marrow transplantation in young mice with globoid cell leukodystrophy. Pediatr Res 2002;51:40-47.
29. Galbiati F, Givogri MI, Cantuti L et al. Combined hematopoietic and lentiviral gene-transfer therapies in newborn Twitcher mice reveal contemporaneous neurodegeneration and demyelination in Krabbe disease. J Neurosci Res 2009;87:1748-1759.
30. Lin D, Fantz CR, Levy B et al. AAV2/5 vector expressing galactocerebrosidase ameliorates CNS disease in the murine model of globoidcell leukodystrophy more efficiently than AAV2. Mol Ther 2005;12: 422-430.
31. Dolcetta D, Perani L, Givogri MI et al. Design and optimization of lentiviral vectors for transfer of GALC expression in Twitcher brain. J Gene Med 2006;8:962-971.
32. Kagitani-Shimono K, Mohri I, Fujitani Y et al. Anti-inflammatory therapy by ibudilast, a phosphodiesterase inhibitor, in demyelination of twitcher, a genetic demyelination model. J Neuroinflammation 2005;2:10.
33. Beck M. Therapy for lysosomal storage disorders. IUBMB Life 2010; 62:33-40.
34. Le Blanc K, Ringden O. Mesenchymal stem cells: Properties and role in clinical bone marrow transplantation. Curr Opin Immunol 2006;18:586-591.
35. Hardy SA, Maltman DJ, Przyborski SA. Mesenchymal stem cells as mediators of neural differentiation. Curr Stem Cell Res Ther 2008;3:43-52.
36. Kassis I, Grigoriadis N, Gowda-Kurkalli B et al. Neuroprotection and immunomodulation with mesenchymal stem cells in chronic experimental autoimmune encephalomyelitis. Arch Neurol 2008;65:753-761.
37. Uccelli A, Moretta L, Pistoia V. Mesenchymal stem cells in health and disease. Nat Rev Immunol 2008;8:726-736.
38. Bunnell BA, Betancourt AM, Sullivan DE. New concepts on the immune modulation mediated by mesenchymal stem cells. Stem Cell Res Ther 2010;1:34.
39. Uccelli A, Benvenuto F, Laroni A et al. Neuroprotective features of mesenchymal stem cells. Best Pract Res Clin Haematol 2011;24: 59-64.
40. Ringden O, Le Blanc K. Mesenchymal stem cells for treatment of acute and chronic graft-versus-host disease, tissue toxicity and hemorrhages. Best Pract Res Clin Haematol 2011;24:65-72.
41. Giordano A, Galderisi U, Marino IR. From the laboratory bench to the patient's bedside: An update on clinical trials with mesenchymal stem cells. J Cell Physiol 2007;211:27-35.
42. Ringden O, Uzunel M, Rasmusson I et al. Mesenchymal stem cells for treatment of therapy-resistant graft-versus-host disease. Transplantation 2006;81:1390-1397.
43. Ripoll CB, Flaat M, Klopf-Eiermann J et al. Mesenchymal-lineage stem cells have pronounced anti-inflammatory effects in the twitcher mouse model of Krabbe's disease. Stem Cells 2011;29:67-77.
44. Terrell KA, Rasmussen TA, Trygg C et al. Molecular beacon genotyping for globoid cell leukodystrophy from hair roots in the twitcher mouse and rhesus macaque. J Neurosci Methods 2007;163:60-66.
45. Ripoll CB, Bunnell BA. Comparative characterization of mesenchymal stem cells from eGFP transgenic and non-transgenic mice. BMC Cell Biol 2009;10:3.
46. Kutner RH, Zhang XY, Reiser J. Production, concentration and titration of pseudotyped HIV-1-based lentiviral vectors. Nat Protoc 2009; 4:495-505.
47. Dolcetta D, Perani L, Givogri MI et al. Analysis of galactocerebrosidase activity in the mouse brain by a new histological staining method. J Neurosci Res 2004;77:462-464.
48. Schindelin J, Arganda-Carreras I, Frise E et al. Fiji: An open-source platform for biological-image analysis. Nat Methods 2012;9:676-682.
49. Raghavan S, Krusell A. Optimal assay conditions for enzymatic characterization of homozygous and heterozygous twitcher mouse. Biochim Biophys Acta 1986;877:1-8.
50. Potier M, Mameli L, Bélisle M et al. Fluorometric assay of neuraminidase with a sodium (4-methylumbelliferyl-alpha-D-N-acetylneuraminate) substrate. Anal Biochem 1979;94:287-296.
51. Miranda CO, Teixeira CA, Liz MA et al. Systemic delivery of bone marrow-derived mesenchymal stromal cells diminishes neuropathology in a mouse model of Krabbe's disease. Stem Cells 2011;29:1738-1751.
52. Jin HK, Carter JE, Huntley GW et al. Intracerebral transplantation of mesenchymal stem cells into acid sphingomyelinase-deficient mice delays the onset of neurological abnormalities and extends their life span. J Clin Invest 2002;109:1183-1191.
53. Lee H, Lee JK, Min WK et al. Bone marrow-derived mesenchymal stem cells prevent the loss of Niemann-Pick type C mouse Purkinje neurons by correcting sphingolipid metabolism and increasing sphingosine-1-phosphate. Stem Cells 2010;28:821-831.
54. Wicks SE, Londot H, Zhang B et al. Effect of intrastriatal mesenchymal stromal cell injection on progression of a murine model of Krabbe disease. Behav Brain Res 2011;225:415-425.
55. Kagitani-Shimono K, Mohri I, Yagi T et al. Peripheral neuropathy in the twitcher mouse: Accumulation of extracellular matrix in the endoneurium and aberrant expression of ion channels. Acta Neuropathol 2008;115:577-587.
56. Suzuki K, Taniike M. Murine model of genetic demyelinating disease: The twitcher mouse. Microsc Res Tech 1995;32:204-214.
57. Zafeiriou DI, Anastasiou AL, Michelakaki EM et al. Early infantile Krabbe disease: Deceptively normal magnetic resonance imaging and serial neurophysiological studies. Brain Dev 1997;19:488-491.
58. Sasaki M, Sakuragawa N, Takashima S et al. MRI and CT findings in Krabbe disease. Pediatr Neurol 1991;7:283-288.
59. Madec AM, Mallone R, Afonso G et al. Mesenchymal stem cells protect NOD mice from diabetes by inducing regulatory T cells. Diabetologia 2009;52:1391-1399.
60. Chiesa S, Morbelli S, Morando S et al. Mesenchymal stem cells impair in vivo T-cell priming by dendritic cells. Proc Natl Acad Sci USA 2011;108:17384-17389.
61. Chamberlain G, Fox J, Ashton B et al. Concise review: Mesenchymal stem cells: Their phenotype, differentiation capacity, immunological features, and potential for homing. Stem Cells 2007;25:2739-2749.
62. Zappia E, Casazza S, Pedemonte E et al. Mesenchymal stem cells ameliorate experimental autoimmune encephalomyelitis inducing Tcell anergy. Blood 2005;106:1755-1761.
63. Von Lüttichau I, Notohamiprodjo M, Wechselberger A et al. Human adult CD34- progenitor cells functionally express the chemokine receptors CCR1, CCR4, CCR7, CXCR5, and CCR10 but not CXCR4. Stem Cells Dev 2005;14:329-336.
64. Cox TM. Gaucher disease: Clinical profile and therapeutic developments. Biologics 2010;4:299-313.
65. White AB, Galbiati F, Givogri MI et al. Persistence of psychosine in brain lipid rafts is a limiting factor in the therapeutic recovery of a mouse model for Krabbe disease. J Neurosci Res 2011;89:352-364.
66. Chen X, Armstrong MA, Li G. Mesenchymal stem cells in immunoregulation. Immunol Cell Biol 2006;84:413-421.
67. Croitoru-Lamoury J, Williams KR, Lamoury FM et al. Neural transplantation of human MSC and NT2 cells in the twitcher mouse model. Cytotherapy 2006;8:445-458.
68. Gimble JM, Katz AJ, Bunnell BA. Adipose-derived stem cells for regenerative medicine. Circ Res 2007;100:1249-1260.
69. Koc ON, Peters C, Aubourg P et al. Bone marrow-derived mesenchymal stem cells remain host-derived despite successful hematopoietic engraftment after allogeneic transplantation in patients with lysosomal and peroxisomal storage diseases. Exp Hematol 1999;27:1675-1681.