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

Volumn 28, Issue 4, 2010, Pages 821-831

  Lee, Hyun ^a   Lee, Jong Kil ^a   Min, Woo Kie ^a   Bae, Jae Hoon ^b   He, Xingxuan ^c   Schuchman, Edward H ^c   Bae, Jae Sung ^a   Jin, Hee Kyung ^a,d  

^a Kyungpook National University Hospital   (South Korea)

^b Keimyung University   (South Korea)

^c MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^d Kyungpook National University   (South Korea)

Author keywords

Apoptosis; Bone marrow derived mesenchymal stem cells; Niemann pick type C disease model; Purkinje neuron; Sphingosine 1 phosphate; Therapeutic potential

Indexed keywords

CALCIUM; SPHINGOLIPID; SPHINGOSINE; SPHINGOSINE 1 PHOSPHATE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CALCIUM CELL LEVEL; CALCIUM HOMEOSTASIS; CELL LEVEL; CELL SURVIVAL; CEREBELLUM; CONTROLLED STUDY; LIPID METABOLISM; LYSOSOME MEMBRANE; MESENCHYMAL STEM CELL TRANSPLANTATION; MOUSE; NERVE CELL DEGENERATION; NERVE CELL NECROSIS; NEUROPROTECTION; NIEMANN PICK DISEASE; NONHUMAN; PURKINJE CELL; THERAPY EFFECT; UPREGULATION; WILD TYPE;

ANIMALS; APOPTOSIS; BONE MARROW CELLS; CALCIUM; CELL DIFFERENTIATION; CELLS, CULTURED; COCULTURE TECHNIQUES; LYSOPHOSPHOLIPIDS; LYSOSOMES; MESENCHYMAL STEM CELL TRANSPLANTATION; MICE; MICE, INBRED BALB C; NIEMANN-PICK DISEASES; PURKINJE CELLS; SPHINGOSINE; STEM CELLS;

MUS;

EID: 77951004675     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1002/stem.401     Document Type: Article

References (46)

1. Vanier MT, Suzuki K. Recent advances in elucidating Niemann-Pick C disease. Brain Pathol 1998;8:163-174. (Pubitemid 28055772)
2. Butler JD, Vanier MT, Pentchev PG. Niemann-Pick C disease: cystine and lipids accumulate in the murine model of this lysosomal cholesterol lipidosis. Biochem Biophys Res Commun 1993;196:154-159.
3. te Vruchte D, Lloyd-Evans E, Veldman RJ et al. Accumulation of glycosphingolipids in Niemann-Pick C disease disrupts endosomal transport. J Biol Chem 2004;279:26167-26175.
4. Tanaka J, Nakamura H, Miyawaki S. Cerebellar involvement in murine sphingomyelinosis: a new model of Niemann-Pick disease. J Neuropathol Exp Neurol 1988;47:291-300.
5. Walkley SU, Suzuki K. Consequences of NPC1 and NPC2 loss of function in mammalian neurons. Biochim Biophys Acta 2004;1685:48-62. (Pubitemid 39311809)
6. Carstea ED, Morris JA, Coleman KG et al. Niemann-Pick C1 disease gene: homology to mediators of cholesterol homeostasis. Science 1997;277:228-231. (Pubitemid 27446076)
7. Lloyd-Evans E, Morgan AJ, He X et al. Niemann-Pick disease type C1 is a sphingosine storage disease that causes deregulation of lysosomal calcium. Nat Med 2008;14:1247-1255.
8. Singh IN, Hall ED. Multifaceted roles of sphingosine-1-phosphate: how does this bioactive sphingolipid fit with acute neurological injury? J Neurosci Res 2008;86:1419-1433.
9. Wu YP, Mizukami H, Matsuda J et al. Apoptosis accompanied by upregulation of TNF-alpha death pathway genes in the brain of Niemann-Pick type C disease. Mol Genet Metab 2005;84:9-17. (Pubitemid 40082600)
10. Li H, Repa JJ, Valasek MA et al. Molecular, anatomical, and biochemical events associated with neurodegeneration in mice with Niemann-Pick type C disease. J Neuropathol Exp Neurol 2005;64:323-333. (Pubitemid 40489559)
11. Bae JS, Furuya S, Shinoda Y et al. Neurodegeneration augments the ability of bone marrow-derived mesenchymal stem cells to fuse with Purkinje neurons in Niemann-Pick type C mice. Hum Gene Ther 2005;16:1006-1011. (Pubitemid 41153869)
12. Bae JS, Han HS, Youn DH et al. Bone marrow-derived mesenchymal stem cells promote neuronal networks with functional synaptic transmission after transplantation into mice with neurodegeneration. Stem Cells 2007;25:1307-1316.
13. Loftus SK, Morris JA, Carstea ED et al. Murine model of Niemann-Pick C disease: mutation in a cholesterol homeostasis gene. Science 1997;277:232-235. (Pubitemid 27446077)
14. Furuya S, Makino A, Hirabayashi Y. An improved method for culturing cerebellar Purkinje cells with differentiated dendrites under a mixed monolayer setting. Brain Res Protoc 1998;3:192-198. (Pubitemid 28527101)
15. Tabata T, Sawada S, Araki K et al. A reliable method for culture of dissociated mouse cerebellar cells enriched for Purkinje neurons. J Neurosci Methods 2000;104:45-53. (Pubitemid 32037162)
16. Lee HY, Greene LA, Mason CA et al. Isolation and culture of postnatal mouse cerebellar granule neuron progenitor cells and neurons. J Vis Exp 2009;10:3791-13790
17. He X, Dagan A, Gatt S et al. Simultaneous quantitative analysis of ceramide and sphingosine in mouse blood by naphthalene-2, 3-dicarboxyaldehyde derivatization after hydrolysis with ceramidase. Anal Biochem 2005;340:113-122. (Pubitemid 40404107)
18. Christensen KA, Myers JT, Swanson JA. pH-dependent regulation of lysosomal calcium in macrophages. J Cell Sci 2002;115:599-607.
19. Bae JH, Mun KC, Park WK et al. EGCG attenuates AMPA-induced intracellular calcium increase in hippocampal neurons. Biochem Biophys Res Commun 2002;290:1506-1512.
20. Bae JS, Furuya S, Ahn SJ et al. Neuroglial activation in Niemann- Pick Type C mice is suppressed by intraral transplantation of bone marrow-derived mesenchymal stem cells. Neurosci Lett 2005;381:234-236. (Pubitemid 40719163)
21. Baudry M, Yao Y, Simmons D et al. Postnatal development of inflammation in a murine model of Niemann-Pick type C disease: immunohistochemical observations of microglia and astroglia. Exp Neurol 2003;184:887-903. (Pubitemid 38182817)
22. Hait NC, Oskeritzian CA, Paugh SW et al. Sphingosine kinases, sphingosine 1-phosphate, apoptosis and diseases. Biochim Biophys Acta 2006;1758:2016-2026.
23. Betito S, Cuvillier O. Regulation by sphingosine 1-phosphate of Bax and Bad activities during apoptosis in a MEK-dependent manner. Biochem Biophys Res Commun 2006;340:1273-1277. (Pubitemid 43083415)
24. Weigert A, Johann AM, von Knethen A et al. Apoptotic cells promote macrophage survival by releasing the antiapoptotic mediator sphingosine-1- phosphate. Blood 2006;108:1635-1642. (Pubitemid 44316132)
25. Goldman S. Stem and progenitor cell-based therapy of the human central nervous system. Nat Biotechnol 2005;23:862-871. (Pubitemid 43093130)
26. Sonntag KC, Simantov R, Isacson O. Stem cells may reshape the prospect of Parkinson's disease therapy. Brain Res Mol Brain Res 2005;134:34-51. (Pubitemid 40403638)
27. Miller RH. The promise of stem cells for neural repair. Brain Res 2006;1091:258-264. (Pubitemid 43993886)
28. Liechty KW, MacKenzie TC, Shaaban AF et al. Human mesenchymal stem cells engraft and demonstrate site-specific differentiation after in utero transplantation in sheep. Nat Med 2000;6:1282-1286.
29. Mezey E, Key S, Vogelsang G et al. Transplanted bone marrow generates new neurons in human brains. Proc Natl Acad Sci U S A 2003;100:1364-1369. (Pubitemid 36184007)
30. Weimann JM, Charlton CA, Brazelton TR et al. Contribution of transplanted bone marrow cells to Purkinje neurons in human adult brains. Proc Natl Acad Sci U S A 2003;100:2088-2093.
31. Parr AM, Tator CH, Keating A. Bone marrow-derived mesenchymal stromal cells for the repair of central nervous system injury. Bone Marrow Transplant 2007;40:609-619. (Pubitemid 47456475)
32. Prockop DJ. "Stemness" does not explain the repair of many tissues by mesenchymal stem/multipotent stromal cells (MSCs). Clin Pharmacol Ther 2007;82:241-243.
33. Munoz JR, Stoutenger BR, Robinson AP et al. Human stem/progenitor cells from bone marrow promote neurogenesis of endogenous neural stem cells in the hippocampus of mice. Proc Natl Acad Sci U S A 2005;102:18171-18176.
34. Prockop DJ, Gregory CA, Spees JL. One strategy for cell and gene therapy: harnessing the power of adult stem cells to repair tissues. Proc Natl Acad Sci USA 2003;100 Suppl 1:11917-11923.
35. Iso Y, Spees JL, Serrano C et al. Multipotent human stromal cells improve cardiac function after myocardial infarction in mice without long-term engraftment. Biochem Biophys Res Commun 2007;354:700-706. (Pubitemid 46186241)
36. Vanier MT. Lipid changes in Niemann-Pick disease type C brain: personal experience and review of the literature. Neurochem Res 1999;24:481-489.
37. Kitatani K, Idkowiak-Baldys J, Hannun YA. The sphingolipid salvage pathway in ceramide metabolism and signaling. Cell Signal 2008;20:1010-1018.
38. Okada T, Kajimoto T, Jahangeer S et al. Sphingosine kinase/sphingosine 1-phosphate signalling in central nervous system. Cell Signal 2009;21:7-13.
39. Higashi Y, Murayama S, Pentchev PG et al. Cerebellar degeneration in the Niemann-Pick type C mouse. Acta Neuropathol 1993;85:175-184. (Pubitemid 23068507)
40. Ong WY, Kumar U, Switzer RC et al. Neurodegeneration in Niemann- Pick type C disease mice. Exp Brain Res 2001;141:218-231. (Pubitemid 33020850)
41. Zhang H, Desai NN, Olivera A et al. Sphingosine-1-phosphate, a novel lipid, involved in cellular proliferation. J Cell Biol 1991;114:155-167. (Pubitemid 21909788)
42. Cuvillier O, Pirianov G, Kleuser B et al. Suppression of ceramidemediated programmed cell death by sphingosine-1-phosphate. Nature 1996;381:800-803. (Pubitemid 26243122)
43. Jeyakumar M. Storage solutions: treating lysosomal disorders of the brain. Nat Rev Neurosci 2005;6:713-725. (Pubitemid 44773245)
44. 2+ stores in the pancreatic acinar cell. Biochim Biophys Acta 1994;1195:45-50.
45. Olivera A, Spiegel S. Sphingosine-1-phosphate as a second messenger in cell proliferation induced by PDGF and FCS mitogens. Nature 1993;365:557-560. (Pubitemid 23317779)
46. Spiegel S, Cuvillier O, Edsall LC et al. Sphingosine-1-phosphate in cell growth and cell death. Ann NY Acad Sci 1998;845:11-18.