Exogenous leukemia inhibitory factor stimulates oligodendrocyte progenitor cell proliferation and enhances hippocampal remyelination

Journal of Neuroscience

Volumn 32, Issue 6, 2012, Pages 2100-2109

  Deverman, Benjamin E ^a   Patterson, Paul H ^a  

^a CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CUPRIZONE; GLYCOPROTEIN GP 130; LEUKEMIA INHIBITORY FACTOR; MYELIN PROTEIN; PROTEOLIPID PROTEIN;

ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; DEMYELINATION; FEMALE; HIPPOCAMPAL CA3 REGION; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; NEURAL STEM CELL; NEUROFILAMENT; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; RANVIER NODE; REMYELINIZATION;

ANIMALS; CELL PROLIFERATION; FEMALE; HIPPOCAMPUS; LEUKEMIA INHIBITORY FACTOR; MALE; MICE; MICE, INBRED C57BL; MICE, INBRED CBA; MICE, TRANSGENIC; MYELIN SHEATH; NEUROGENESIS; OLIGODENDROGLIA; RANVIER'S NODES; STEM CELLS;

EID: 84857022922     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3803-11.2012     Document Type: Article

References (67)

1. Albrecht PJ, Murtie JC, Ness JK, Redwine JM, Enterline JR, Armstrong RC, Levison SW (2003) Astrocytes produce CNTF during the remyelination phase of viral-induced spinal cord demyelination to stimulate FGF-2 production. Neurobiol Dis 13:89-101.
2. Albrecht PJ, Enterline JC, Cromer J, Levison SW (2007) CNTF-activated astrocytes release a soluble trophic activity for oligodendrocyte progenitors. Neurochem Res 32:263-271.
3. Amato MP, Portaccio E, Goretti B, Zipoli V, Battaglini M, Bartolozzi ML, Stromillo ML, Guidi L, Siracusa G, Sorbi S, Federico A, De Stefano N (2007) Association of neocortical volume changes with cognitive deterioration in relapsing-remitting multiple sclerosis. Arch Neurol 64:1157-1161.
4. Arai K, Lo EH (2009) An oligovascular niche: cerebral endothelial cells promote the survival and proliferation of oligodendrocyte precursor cells. J Neurosci 29:4351-4355.
5. Armstrong RC, Le TQ, Frost EE, Borke RC, Vana AC (2002) Absence of fibroblast growth factor 2 promotes oligodendroglial repopulation of demyelinated white matter. J Neurosci 22:8574-8585.
6. Armstrong RC, Le TQ, Flint NC, Vana AC, Zhou YX (2006) Endogenous cell repair of chronic demyelination. J Neuropathol Exp Neurol 65:245-256.
7. Arnett HA, Mason J, Marino M, Suzuki K, Matsushima GK, Ting JP (2001) TNF alpha promotes proliferation of oligodendrocyte progenitors and remyelination. Nat Neurosci 4:1116-1122.
8. Baba H, Akita H, Ishibashi T, Inoue Y, Nakahira K, Ikenaka K (1999) Completion of myelin compaction, but not the attachment of oligodendroglial processes triggers K(+) channel clustering. J Neurosci Res 58:752-764.
9. Barres BA, Burne JF, Holtmann B, Thoenen H, Sendtner M, RaffMC (1996) Ciliary neurotrophic factor enhances the rate of oligodendrocyte generation. Mol Cell Neurosci 8:146-156.
10. Bauer S, Patterson PH (2006) Leukemia inhibitory factor promotes neural stem cell self-renewal in the adult brain. J Neurosci 26:12089-12099.
11. Betz UA, Bloch W, van den Broek M, Yoshida K, Taga T, Kishimoto T, Addicks K, Rajewsky K, Müller W (1998) Postnatally induced inactivation of gp130 in mice results in neurological, cardiac, hematopoietic, immunological, hepatic, and pulmonary defects. J Exp Med 188:1955-1965.
12. Bø L, Vedeler CA, Nyland HI, Trapp BD, Mork SJ (2003) Subpial demyelination in the cerebral cortex of multiple sclerosis patients. J Neuropathol Exp Neurol 62:723-732.
13. Brownell B, Hughes JT (1962) The distribution of plaques in the cerebrum in multiple sclerosis. J Neurol Neurosurg Psychiatry 25:315-320.
14. Butzkueven H, Zhang JG, Soilu-Hanninen M, Hochrein H, Chionh F, Shipham KA, Emery B, Turnley AM, Petratos S, Ernst M, Bartlett PF, Kilpatrick TJ (2002) LIF receptor signaling limits immune-mediated demyelination by enhancing oligodendrocyte survival. Nat Med 8:613-619.
15. Cai J, Chen Y, Cai WH, Hurlock EC, Wu H, Kernie SG, Parada LF, Lu QR (2007) A crucial role for Olig2 in white matter astrocyte development. Development 134:1887-1899.
16. Cao Q, Xu XM, Devries WH, Enzmann GU, Ping P, Tsoulfas P, Wood PM, Bunge MB, Whittemore SR (2005) Functional recovery in traumatic spinal cord injury after transplantation of multineurotrophin-expressing glial-restricted precursor cells. J Neurosci 25:6947-6957.
17. Cao W, Yang Y, Wang Z, Liu A, Fang L, Wu F, Hong J, Shi Y, Leung S, Dong C, Zhang JZ (2011) Leukemia inhibitory factor inhibits T helper 17 cell differentiation and confers treatment effects of neural progenitor cell therapy in autoimmune disease. Immunity 35:273-284.
18. Doetsch F, Caillé I, Lim DA, García-Verdugo JM, Alvarez-Buylla A (1999) Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97:703-716.
19. Dugas JC, Ibrahim A, Barres BA (2007) A crucial role for p57(Kip2) in the intracellular timer that controls oligodendrocyte differentiation. J Neurosci 27:6185-6196.
20. Ge Y, Grossman RI, Udupa JK, Babb JS, Mannon LJ, McGowan JC (2002) Magnetization transfer ratio histogram analysis of normal-appearing gray matter and normal-appearing white matter in multiple sclerosis. J Comput Assist Tomogr 26:62-68.
21. Geurts JJ, Bö L, Pouwels PJ, Castelijns JA, Polman CH, Barkhof F (2005) Cortical lesions in multiple sclerosis: combined postmortemMRimaging and histopathology. AJNR Am J Neuroradiol 26:572-577.
22. Geurts JJ, Bö L, Roosendaal SD, Hazes T, Daniëls R, Barkhof F, Witter MP, Huitinga I, van der Valk P (2007) Extensive hippocampal demyelination in multiple sclerosis. J Neuropathol Exp Neurol 66:819-827.
23. Geurts JJ, Blezer EL, Vrenken H, van der Toorn A, Castelijns JA, Polman CH, Pouwels PJ, Bö L, Barkhof F (2008) Does high-field MR imaging improve cortical lesion detection in multiple sclerosis? J Neurol 255:183-191.
24. Goddard DR, Berry M, Kirvell SL, Butt AM (2001) Fibroblast growth factor-2 inhibits myelin production by oligodendrocytes in vivo. Mol Cell Neurosci 18:557-569.
25. Hachem S, Aguirre A, Vives V, Marks A, Gallo V, Legraverend C (2005) Spatial and temporal expression of S100B in cells of oligodendrocyte lineage. Glia 51:81-97.
26. Haroon F, Drögemuller K, Händel U, Brunn A, Reinhold D, Nishanth G, Mueller W, Trautwein C, Ernst M, Deckert M, Schlüter D (2011) Gp130-dependent astrocytic survival is critical for the control of autoimmune central nervous system inflammation. J Immunol 186:6521-6531.
27. Harsan L, Steibel J, Zaremba A, Agin A, Sapin R, Poulet P, Guignard B, Parizel N, Grucker D, Boehm N, Miller RH, Ghandour MS (2008) Recovery from chronic demyelination by thyroid hormone therapy: myelinogenesis induction and assessment by diffusion tensor magnetic resonance imaging. J Neurosci 28:14189-14201.
28. Hendriks JJ, Slaets H, Carmans S, de Vries HE, Dijkstra CD, Stinissen P, Hellings N (2008) Leukemia inhibitory factor modulates production of inflammatory mediators and myelin phagocytosis by macrophages. J Neuroimmunol 204:52-57.
29. Ishibashi T, Dakin KA, Stevens B, Lee PR, Kozlov SV, Stewart CL, Fields RD (2006) Astrocytes promote myelination in response to electrical impulses. Neuron 49:823-832.
30. Ishibashi T, Lee PR, Baba H, Fields RD (2009) Leukemia inhibitory factor regulates the timing of oligodendrocyte development and myelination in the postnatal optic nerve. J Neurosci Res 87:3343-3355.
31. Keirstead HS, Nistor G, Bernal G, Totoiu M, Cloutier F, Sharp K, Steward O (2005) Human embryonic stem cell-derived oligodendrocyte progenitor cell transplants remyelinate and restore locomotion after spinal cord injury. J Neurosci 25:4694-4705.
32. Kerr BJ, Patterson PH (2004) Potent pro-inflammatory actions of leukemia inhibitory factor in the spinal cord of the adult mouse. Exp Neurol 188:391-407.
33. Kerr BJ, Patterson PH (2005) Leukemia inhibitory factor promotes oligodendrocyte survival after spinal cord injury. Glia 51:73-79.
34. Kidd D, Barkhof F, McConnell R, Algra PR, Allen IV, Revesz T (1999) Cortical lesions in multiple sclerosis. Brain 122:17-26.
35. Leibinger M, Müller A, Andreadaki A, Hauk TG, Kirsch M, Fischer D (2009) Neuroprotective and axon growth-promoting effects following inflammatory stimulation on mature retinal ganglion cells in mice depend on ciliary neurotrophic factor and leukemia inhibitory factor. J Neurosci 29:14334-14341.
36. Linker RA, Mäurer M, Gaupp S, Martini R, Holtmann B, Giess R, Rieckmann P, Lassmann H, Toyka KV, Sendtner M, Gold R (2002) CNTF is a major protective factor in demyelinating CNS disease: a neurotrophic cytokine as modulator in neuroinflammation. Nat Med 8:620-624.
37. Louis JC, Magal E, Takayama S, Varon S (1993) CNTF protection of oligodendrocytes against natural and tumor necrosis factor-induced death. Science 259:689-692.
38. Lowry N, Goderie SK, Adamo M, Lederman P, Charniga C, Gill J, Silver J, Temple S (2008) Multipotent embryonic spinal cord stem cells expanded by endothelial factors and Shh/RA promote functional recovery after spinal cord injury. Exp Neurol 209:510-522.
39. Marriott MP, Emery B, Cate HS, Binder MD, Kemper D, Wu Q, Kolbe S, Gordon IR, Wang H, Egan G, Murray S, Butzkueven H, Kilpatrick TJ (2008) Leukemia inhibitory factor signaling modulates both central nervous system demyelination and myelin repair. Glia 56:686-698.
40. Mason JL, Suzuki K, Chaplin DD, Matsushima GK (2001) Interleukin-1beta promotes repair of the CNS. J Neurosci 21:7046-7052.
41. Mason JL, Toews A, Hostettler JD, Morell P, Suzuki K, Goldman JE, Matsushima GK (2004) Oligodendrocytes and progenitors become progressively depleted within chronically demyelinated lesions. Am J Pathol 164:1673-1682.
42. Mayer M, Bhakoo K, Noble M (1994) Ciliary neurotrophic factor and leukemia inhibitory factor promote the generation, maturation and survival of oligodendrocytes in vitro. Development 120:143-153.
43. Menn B, Garcia-Verdugo JM, Yaschine C, Gonzalez-Perez O, Rowitch D, Alvarez-Buylla A (2006) Origin of oligodendrocytes in the subventricular zone of the adult brain. J Neurosci 26:7907-7918.
44. Nishiyama A (2007) Polydendrocytes: NG2 cells with many roles in development and repair of the CNS. Neuroscientist 13:62-76.
45. Ozerdem U, Grako KA, Dahlin-Huppe K, Monosov E, Stallcup WB (2001) NG2 proteoglycan is expressed exclusively by mural cells during vascular morphogenesis. Dev Dyn 222:218-227.
46. Pan W, Kastin AJ, Brennan JM (2000) Saturable entry of leukemia inhibitory factor from blood to the central nervous system. J Neuroimmunol 106:172-180.
47. Pan W, Yu C, Hsuchou H, Zhang Y, Kastin A (2008) Neuroinflammation facilitates LIF entry into brain: role of TNF. Am J Physiol Cell Physiol.
48. Pirko I, Lucchinetti CF, Sriram S, Bakshi R (2007) Gray matter involvement in multiple sclerosis. Neurology 68:634-642.
49. Rickmann M (1995) S100 immunoreactivity in a subpopulation of oligodendrocytes and Ranvier's nodes of adult rat brain 186:13-16.
50. Rivers LE, Young KM, Rizzi M, Jamen F, Psachoulia K, Wade A, Kessaris N, RichardsonWD (2008) PDGFRA/NG2 glia generate myelinating oligodendrocytes and piriform projection neurons in adult mice. Nat Neurosci 11:1392-1401.
51. Roosendaal SD, Moraal B, Vrenken H, Castelijns JA, Pouwels PJ, Barkhof F, Geurts JJ (2008) In vivoMRimaging of hippocampal lesions in multiple sclerosis. J Magn Reson Imaging 27:726-731.
52. Rosenberg SS, Kelland EE, Tokar E, De la Torre AR, Chan JR (2008) The geometric and spatial constraints of the microenvironment induce oligodendrocyte differentiation. Proc Natl Acad Sci U S A 105:14662-14667.
53. Rovaris M, Filippi M, Minicucci L, Iannucci G, Santuccio G, Possa F, Comi G (2000) Cortical/subcortical disease burden and cognitive impairment in patients with multiple sclerosis. AJNR Am J Neuroradiol 21:402-408.
54. Sicotte NL, Kern KC, Giesser BS, Arshanapalli A, Schultz A, Montag M, Wang H, Bookheimer SY (2008) Regional hippocampal atrophy in multiple sclerosis. Brain 131:1134-1141.
55. Slaets H, Hendriks JJ, Van den Haute C, Coun F, Baekelandt V, Stinissen P, Hellings N (2010) CNS-targeted LIF expression improves therapeutic efficacy and limits autoimmune-mediated demyelination in a model of multiple sclerosis. Mol Ther 18:684-691.
56. Srinivas S, Watanabe T, Lin CS, William CM, Tanabe Y, Jessell TM, Costantini F (2001) Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev Biol 1:4.
57. Sugiura S, Lahav R, Han J, Kou SY, Banner LR, de Pablo F, Patterson PH (2000) Leukaemia inhibitory factor is required for normal inflammatory responses to injury in the peripheral and central nervous systems in vivo and is chemotactic for macrophages in vitro. Eur J Neurosci 12:457-466.
58. Tatsumi K, Takebayashi H, Manabe T, Tanaka KF, Makinodan M, Yamauchi T, Makinodan E, Matsuyoshi H, Okuda H, Ikenaka K, Wanaka A (2008) Genetic fate mapping of Olig2 progenitors in the injured adult cerebral cortex reveals preferential differentiation into astrocytes. J Neurosci Res 86:3494-3502.
59. Temple S, Raff MC (1986) Clonal analysis of oligodendrocyte development in culture: evidence for a developmental clock that counts cell divisions. Cell 44:773-779.
60. Vrenken H, Pouwels PJ, Geurts JJ, Knol DL, Polman CH, Barkhof F, Castelijns JA (2006) Altered diffusion tensor in multiple sclerosis normalappearing brain tissue: cortical diffusion changes seem related to clinical deterioration. J Magn Reson Imaging 23:628-636.
61. Warrington AE, Bieber AJ, Ciric B, Pease LR, Van Keulen V, Rodriguez M (2007) A recombinant human IgM promotes myelin repair after a single, very low dose. J Neurosci Res 85:967-976.
62. Windrem MS, Schanz SJ, Guo M, Tian GF, Washco V, Stanwood N, Rasband M, Roy NS, Nedergaard M, Havton LA, Wang S, Goldman SA (2008) Neonatal chimerization with human glial progenitor cells can both remyelinate and rescue the otherwise lethally hypomyelinated shiverer mouse. Cell Stem Cell 2:553-565.
63. Woodruff RH, Fruttiger M, Richardson WD, Franklin RJ (2004) Plateletderived growth factor regulates oligodendrocyte progenitor numbers in adult CNS and their response following CNS demyelination. Mol Cell Neurosci 25:252-262.
64. Zang DW, Cheema SS (2003) Leukemia inhibitory factor promotes recovery of locomotor function following spinal cord injury in the mouse. J Neurotrauma 20:1215-1222.
65. Zhang Y, Taveggia C, Melendez-Vasquez C, Einheber S, Raine CS, Salzer JL, Brosnan CF, John GR (2006) Interleukin-11 potentiates oligodendrocyte survival and maturation, and myelin formation. J Neurosci 26:12174-12185.
66. Zhu M, Oishi K, Lee SC, Patterson PH (2001) Studies using leukemia inhibitory factor (LIF) knockout mice and a LIF adenoviral vector demonstrate a key anti-inflammatory role for this cytokine in cutaneous inflammation. J Immunol 166:2049-2054.
67. Zhu X, Bergles DE, Nishiyama A (2008) NG2 cells generate both oligodendrocytes and gray matter astrocytes. Development 135:145-157.