Mesenchymal stem cells yield transient improvements in motor function in an infant rhesus macaque with severe early-onset krabbe disease

Stem Cells Translational Medicine

Volumn 6, Issue 1, 2017, Pages 99-109

  Isakova, Irina A ^a   Baker, Kate C ^b   Dufour, Jason ^b   Phinney, Donald G ^c  

^a Donahue s Consulting Inc   (United States)

^b TULANE NATIONAL PRIMATE RESEARCH CENTER   (United States)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

Cell therapy; Globoid cell leukodystrophy; Krabbe disease; Mesenchymal stem cells; Mesenchymal stromal cells; Nerve conduction; Nonhuman primates

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR ASSESSMENT; CONTROLLED STUDY; DISEASE COURSE; FEMALE; FLOW CYTOMETRY; GLOBOID CELL LEUKODYSTROPHY; HISTOPATHOLOGY; IMMUNE RESPONSE; INFANT; LYMPHOCYTE; LYMPHOCYTE COUNT; MAJOR HISTOCOMPATIBILITY COMPLEX; MALE; MESENCHYMAL STEM CELL; MESENCHYMAL STEM CELL TRANSPLANTATION; MOTOR PERFORMANCE; NERVE CONDUCTION; NEUTROPHIL COUNT; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; POLYMERASE CHAIN REACTION; PYROSEQUENCING; RHESUS MONKEY; ALLOTRANSPLANTATION; ANIMAL; ANIMAL BEHAVIOR; CYTOLOGY; DISEASE EXACERBATION; IMMUNOLOGY; MOTOR ACTIVITY; NEWBORN; PATHOPHYSIOLOGY; PHENOTYPE;

ANIMALS; ANIMALS, NEWBORN; BEHAVIOR, ANIMAL; DISEASE PROGRESSION; FEMALE; LEUKODYSTROPHY, GLOBOID CELL; MACACA MULATTA; MAGNETIC RESONANCE IMAGING; MAJOR HISTOCOMPATIBILITY COMPLEX; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STEM CELLS; MOTOR ACTIVITY; NEURAL CONDUCTION; PHENOTYPE; TRANSPLANTATION, HOMOLOGOUS;

EID: 85017381181     PISSN: 21576564     EISSN: 21576580     Source Type: Journal    
DOI: 10.5966/sctm.2015-0317     Document Type: Article

References (46)

1. Perlman SJ, Mar S. Leukodystrophies. Adv Exp Med Biol 2012;724:154-171.
2. Wenger DA. Krabbe disease. In: Pagon RA, Adam MP, Ardinger HH et al., eds. eneReviews. Seattle, WA: University of Washington, 1993.
3. Lund TC. Hematopoietic stem cell transplant for lysosomal storage diseases. Pediatr Endocrinol Rev 2013;11(suppl 1): 91-98.
4. 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.
5. Ohashi T. Enzymereplacement therapy for lysosomal storage diseases. Pediatr Endocrinol Rev 2012;10(suppl 1):26-34.
6. Noh H, Lee JI. Current and potential therapeutic strategies for mucopolysaccharidoses. J Clin Pharm Ther 2014;39:215-224.
7. Weinreb NJ. Oral small molecule therapy for lysosomal storage diseases. Pediatr Endocrinol Rev 2013;11(suppl 1):77-90.
8. Duchen LW, Eicher EM, Jacobs JM et al. Hereditary leucodystrophy in the mouse: The new mutant twitcher. Brain 1980;103: 695-710.
9. Ohno M, Komiyama A, Martin PM et al. Proliferation of microglia/macrophages in the demyelinating CNS and PNS of twitcher mouse. Brain Res 1993;602:268-274.
10. Mohri I, Taniike M, Taniguchi H et al. Prostaglandin D2-mediated microglia/astrocyte interaction enhances astrogliosis anddemyelination in twitcher. J Neurosci 2006;26:4383-4393.
11. Matsushima GK, Taniike M, Glimcher LH et al. Absence of MHC class II molecules reduces CNS demyelination, microglial/macrophage infiltration, and twitching in murine globoid cell leukodystrophy. Cell 1994;78:645-656.
12. Ohno M, Komiyama A, Martin PM et al. MHC class II antigen expression and T-cell infiltration in the demyelinating CNS and PNS of the twitcher mouse. Brain Res 1993;625: 186-196.
13. LeVine SM, Brown DC. IL-6 and TNFalpha expression in brains of twitcher, quaking and normal mice. J Neuroimmunol 1997;73:47-56.
14. Wu YP, Matsuda J, Kubota A et al. Infiltration of hematogenous lineage cells into the demyelinating central nervous system of twitcher mice. J Neuropathol Exp Neurol 2000; 59:628-639.
15. 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.
16. Luzi P, Abraham RM, Rafi MA et al. Effects of treatments on inflammatory and apoptotic markers in the CNS of mice with globoid cell leukodystrophy. Brain Res 2009;1300:146-158.
17. Pasqui AL, Di Renzo M, Auteri A et al. Increased TNF-alpha production by peripheral bloodmononuclear cells in patients with Krabbe’s disease: Effect of psychosine. Eur J Clin Invest 2007;37:742-745.
18. Caplan AI, Correa D. The MSC: An injury drugstore. Cell Stem Cell 2011;9:11-15.
19. Caplan AI, Dennis JE. Mesenchymal stem cells as trophic mediators. J Cell Biochem 2006; 98:1076-1084.
20. Nauta AJ, Fibbe WE. Immunomodulatory properties of mesenchymal stromal cells. Blood 2007;110:3499-3506.
21. Phinney DG. Biochemical heterogeneity of mesenchymal stem cell populations: Clues to their therapeutic efficacy. Cell Cycle 2007; 6:2884-2889.
22. Phinney DG. A SAGE view of mesenchymal stem cells. Int J Stem Cells 2009;2:1-10.
23. Phinney DG, Isakova IA. Mesenchymal stem cells as cellular vectors for pediatric neurological disorders. Brain Res 2014; 1573:92-107.
24. Isakova IA, Baker K, Dufour J et al. Preclinical evaluation of adult stem cell engraftment and toxicity in the CNS of rhesus macaques. Mol Ther 2006;13:1173-1184.
25. Isakova IA, Baker K, Du Treil M et al. Ageand dose-related effects on MSC engraftment levels and anatomical distribution in the central nervous systems of nonhuman primates: Identification of novel MSC subpopulations that respond to guidance cues in brain. STEM CELLS 2007;25:3261-3270.
26. Isakova IA, Dufour J, Lanclos C et al. Celldose-dependent increases in circulating levels of immune effector cells in rhesus macaques following intracranial injection of allogeneic MSCs. Exp Hematol 2010;38:957-967.e1.
27. Isakova IA, Lanclos C, Bruhn J et al. Alloreactivity of mesenchymal stem cells in rhesus macaques is dose and haplotype dependent and limits durable cell engraftment in vivo. PLoS One 2014;9:e87238.
28. 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.
29. Scruggs BA, Zhang X, Bowles AC et al. Multipotent stromal cells alleviate inflammation, neuropathology, and symptoms associated with globoid cell leukodystrophy in the twitcher mouse. STEM CELLS 2013;31: 1523-1534.
30. Baskin GB, Ratterree M, Davison BB et al. Genetic galactocerebrosidase deficiency (globoid cell leukodystrophy, Krabbe disease) in rhesus monkeys (Macaca mulatta). Lab Anim Sci 1998;48:476-482.
31. Wiseman RW, Karl JA, Bimber BN et al. Major histocompatibility complex genotyping with massively parallel pyrosequencing. Nat Med 2009;15:1322-1326.
32. Als H, Tronick E, Lester BM et al. The Brazelton Neonatal Behavioral Assessment Scale (BNBAS). J Abnorm Child Psychol 1977;5:215-231.
33. Bayley N. Bayley Scales of Infant Development, 2nd ed. San Antonio, TX: The Psychological Corporation, 1993.
34. Schneider M, Suomi S. Neurobehavioral assessment in rhesus monkey neonates (Macaca mulatto): Developmental changes, behavior stability and early experience. Infant Behav Dev 1992;15:155-177.
35. Weimer MB, Gutierrez A, Baskin GB et al. Serial electrophysiologic studies in rhesus monkeyswith Krabbe disease. Muscle Nerve 2005;32:185-190.
36. Galbiati F, Basso V, Cantuti L et al. Autonomic denervation of lymphoid organs leads to epigenetic immune atrophy in a mouse model of Krabbe disease. J Neurosci 2007;27: 13730-13738.
37. Luzi P, Rafi MA, Victoria T et al. Characterization of the rhesus monkey galactocerebrosidase (GALC) cDNA and gene and identification of the mutation causing globoid cell leukodystrophy (Krabbe disease) in this primate. Genomics 1997;42:319-324.
38. Crigler L, Robey RC, Asawachaicharn A et al. Human mesenchymal stem cell ubpopulations express a variety of neuro-regulatory molecules and promote neuronal cell survival and neuritogenesis. Exp Neurol 2006; 198:54-64.
39. Scuteri A, Cassetti A, Tredici G. Adult mesenchymal stem cells rescue dorsal root ganglia neurons from dying. Brain Res 2006;1116: 75-81.
40. Wilkins A, Kemp K, Ginty M et al. Human bone marrow-derived mesenchymal stem cells secrete brain-derived neurotrophic factor which promotes neuronal survival in vitro. Stem Cell Res (Amst) 2009;3:63-70.
41. Kemp K, Hares K, Mallam E et al. Mesenchymal stem cell-secreted superoxide dismutase promotes cerebellar neuronal survival. J Neurochem 2010;114:1569-1580.
42. Jaramillo-Merchán J, Jones J, Ivorra JL et al. Mesenchymal stromal-cell transplants induce oligodendrocyte progenitor migration and remyelination in a chronic demyelinationmodel. Cell Death Dis 2013;4:e779.
43. Bai L, Lennon DP, Caplan AI et al. Hepatocyte growth factor mediates mesenchymal stem cell-induced recovery in multiple sclerosis models. Nat Neurosci 2012;15:862-870.
44. Jadasz JJ, Kremer D, Göttle P et al. Mesenchymal stem cell conditioning promotes rat oligodendroglial cell maturation. PLoS One 2013; 8:e71814.
45. Cristofanilli M, Harris VK, Zigelbaum A et al. Mesenchymal stem cells enhance the engraftment and myelinating ability of allogeneic oligodendrocyte progenitors in dysmyelinated mice. Stem Cells Dev 2011;20: 2065-2076.
46. 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.