Gas6 enhances axonal ensheathment by MBP+ membranous processes in human DRG/OL promyelinating co-cultures

ASN Neuro

Volumn 6, Issue 1, 2014, Pages 29-42

  O'Guin, Kathleen N ^a   Gruber, Ross C ^a   Raine, Cedric S ^a   Guzik, Hillary M ^a   Poulos, Bradford K ^a   Shafit Zagardo, Bridget ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

Growth arrest specific protein 6; Human OPC DRG co culture; Myelination; Oligodendrocyte

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; GROWTH ARREST SPECIFIC PROTEIN 6; MYELIN ASSOCIATED GLYCOPROTEIN; MYELIN BASIC PROTEIN; NEUROFILAMENT PROTEIN; SOMATOMEDIN C;

ARTICLE; CONFOCAL MICROSCOPY; ELECTRON MICROSCOPY; ENZYME LINKED IMMUNOSORBENT ASSAY; FETUS; FLUORESCENCE MICROSCOPY; GANGLION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOFLUORESCENCE; MYELINATION; NICK END LABELING; OLIGODENDROCYTE PRECURSOR CELL;

EID: 84893480618     PISSN: 17590914     EISSN: None     Source Type: Journal    
DOI: 10.1042/AN20130022     Document Type: Article

References (36)

1. Aggarwal S, Yurlova L, Snaidero N, Reetz C, Frey S, Zimmermann J, Pahler G, Janshoff A, Friedrichs J, Muller DJ, Goebel C, Simons M (2011) A size barrier limits protein diffusion at the cell surface to generate lipid-rich myelin-membrane sheets. Dev Cell 21:445-456.
2. Allen MP, Zeng C, Schneider K, Xiong X, Meintzer MK, Bellosta P, Basilico C, Varnum B, Heidenreich KA, Wierman ME (1999) Growth arrest-specific gene 6 (Gas6)/adhesion related kinase (Ark) signaling promotes gonadotropin-releasing hormone neuronal survival via extracellular signal-regulated kinase (ERK) and Akt. Mol Endocrinol 13:191-201.
3. Arnett HA, Fancy SP, Alberta JA, Zhao C, Plant SR, Kaing S, Raine CS, Rowitch DH, Franklin RJ, Stiles CD (2004) bHLH transcription factor Olig1 is required to repair demyelinated lesions in the CNS. Science 306:2111-2115.
4. Avanzi GC, Gallicchio M, Bottarel F, Gammaitoni L, Cavalloni G, Buonfiglio D, Bragardo M, Bellomo G, Albano E, Fantozzi R, Garbarino G, Varnum B, Aglietta M, Saglio G, Dianzani U, Dianzani C (1998) GAS6 inhibits granulocyte adhesion to endothelial cells. Blood 91:2334-2340.
5. Bakhti M, Snaidero N, Schneider D, Aggarwal S, Mobius W, Janshoff A, Eckhardt M, Nave KA, Simons M (2013) Loss of electrostatic cell-surface repulsion mediates myelin membrane adhesion and compaction in the central nervous system. Proc Natl Acad Sci USA 110:3143-3148.
6. Binder MD, Xiao J, Kemper D, Ma GZ, Murray SS, Kilpatrick TJ (2011) Gas6 increases myelination by oligodendrocytes and its deficiency delays recovery following cuprizone-induced demyelination. PLoS ONE 6:e17727.
7. Brown JE, Krodel M, Pazos M, Lai C, Prieto AL (2012) Cross-phosphorylation, signaling and proliferative functions of the tyro3 and axl receptors in rat2 cells. PLoS ONE 7:e36800.
8. Carson MJ, Behringer RR, Brinster RL, McMorris FA (1993) Insulin-like growth factor I increases brain growth and central nervous system myelination in transgenic mice. Neuron 10:729-740.
9. Chan JR, Watkins TA, Cosgaya JM, Zhang C, Chen L, Reichardt LF, Shooter EM, Barres BA (2004) NGF controls axonal receptivity to myelination by Schwann cells or oligodendrocytes. Neuron 43:183-191.
10. Crosier KE, Crosier PS (1997) New insights into the control of cell growth; the role of the AxI family. Pathology 29:131-135.
11. Cui QL, Fragoso G, Miron VE, Darlington PJ, Mushynski WE, Antel J, Almazan G (2010) Response of human oligodendrocyte progenitors to growth factors and axon signals. J Neuropathol Exp Neurol 69:930-944.
12. Emery B (2010) Regulation of oligodendrocyte differentiation and myelination. Science 330:779-782.
13. Fridell YW, Jin Y, Quilliam LA, Burchert A, McCloskey P, Spizz G, Varnum B, Der C, Liu ET (1996) Differential activation of the Ras/extracellularsignal- regulated protein kinase pathway is responsible for the biological consequences induced by the Axl receptor tyrosine kinase. Mol Cell Biol 16:135-145.
14. Furusho M, Dupree JL, Nave KA, Bansal R (2012) Fibroblast growth factor receptor signaling in oligodendrocytes regulates myelin sheath thickness. J Neurosci 32:6631-6641.
15. Gundersen RW, Barrett JN (1979) Neuronal chemotaxis: chick dorsal-root axons turn toward high concentrations of nerve growth factor. Science 206:1079-1080.
16. Hannila SS, Filbin MT (2008) The role of cyclic AMP signaling in promoting axonal regeneration after spinal cord injury. Exp Neurol 209:321-332.
17. Jana M, Jana A, Pal U, Pahan K (2007) A simplified method for isolating highly purified neurons, oligodendrocytes, astrocytes, and microglia from the same human fetal brain tissue. Neurochem Res 32:2015-2022.
18. Li R, Chen J, Hammonds G, Phillips H, Armanini M, Wood P, Bunge R, Godowski PJ, Sliwkowski MX, Mather JP (1996) Identification of Gas6 as a growth factor for human Schwann cells. J Neurosci 16:2012-2019.
19. Nave KA (2010) Myelination and the trophic support of long axons. Nat Rev Neurosci 11:275-283.
20. Piaton G, Gould RM, Lubetzki C (2010) Axon-oligodendrocyte interactions during developmental myelination, demyelination and repair. J Neurochem 114:1243-1260.
21. Prieto AL, Weber JL, Lai C (2000) Expression of the receptor protein-tyrosine kinases Tyro-3, Axl, and mer in the developing rat central nervous system. J Comp Neurol 425:295-314.
22. Prieto AL, Weber JL, Tracy S, Heeb MJ, Lai C (1999) Gas6, a ligand for the receptor protein-tyrosine kinase Tyro-3, is widely expressed in the central nervous system. Brain Res 816:646-661.
23. Sainaghi PP, Collimedaglia L, Alciato F, Leone MA, Puta E, Naldi P, Castello L, Monaco F, Avanzi GC (2008) Elevation of Gas6 protein concentration in cerebrospinal fluid of patients with chronic inflammatory demyelinating polyneuropathy (CIDP). J Neurol Sci 269:138-142.
24. Sainaghi PP, Collimedaglia L, Alciato F, Molinari R, Sola D, Ranza E, Naldi P, Monaco F, Leone M, Pirisi M, Avanzi GC (2013) Growth arrest specific gene 6 protein concentration in cerebrospinal fluid correlates with relapse severity in multiple sclerosis. Mediators Inflamm 2013:406483.
25. Shankar SL, O'Guin K, Cammer M, McMorris FA, Stitt TN, Basch RS, Varnum B, Shafit-Zagardo B (2003) The growth arrest-specific gene product Gas6 promotes the survival of human oligodendrocytes via a phosphatidylinositol 3-kinase-dependent pathway. J Neurosci 23:4208-4218.
26. Shankar SL, O'Guin K, Kim M, Varnum B, Lemke G, Brosnan CF, Shafit-Zagardo B (2006) Gas6/Axl signaling activates the phosphatidylinositol 3-kinase/Akt1 survival pathway to protect oligodendrocytes from tumor necrosis factor alpha-induced apoptosis. J Neurosci 26:5638-5648.
27. Taveggia C, Thaker P, Petrylak A, Caporaso GL, Toews A, Falls DL, Einheber S, Salzer JL (2008) Type III neuregulin-1 promotes oligodendrocyte myelination. Glia 56:284-293.
28. Terada N, Kidd GJ, Kinter M, Bjartmar C, Moran-Jones K, Trapp BD (2005) Beta IV tubulin is selectively expressed by oligodendrocytes in the central nervous system. Glia 50:212-222.
29. Tsiperson V, Li X, Schwartz GJ, Raine CS, Shafit-Zagardo B (2010) GAS6 enhances repair following cuprizone-induced demyelination. PLoS ONE 5:e15748.
30. +/- mice exhibit deficits in oligodendrocyte lineage cells of the basal forebrain. Glia 58:848-856.
31. VonDran MW, Singh H, Honeywell JZ, Dreyfus CF (2011) Levels of BDNF impact oligodendrocyte lineage cells following a cuprizone lesion. J Neurosci 31:14182-14190.
32. Wang H, Rusielewicz T, Tewari A, Leitman EM, Einheber S, Melendez-Vasquez CV (2012) Myosin II is a negative regulator of oligodendrocyte morphological differentiation. J Neurosci Res 90:1547-1556.
33. Weinger JG, Brosnan CF, Loudig O, Goldberg MF, Macian F, Arnett HA, Prieto AL, Tsiperson V, Shafit-Zagardo B (2011) Loss of the receptor tyrosine kinase Axl leads to enhanced inflammation in the CNS and delayed removal of myelin debris during experimental autoimmune encephalomyelitis. J Neuroinflammation 8: 49.
34. Weinger JG, Gohari P, Yan Y, Backer JM, Varnum B, Shafit-Zagardo B (2008) In brain, Axl recruits Grb2 and the p85 regulatory subunit of PI3 kinase; in vitro mutagenesis defines the requisite binding sites for downstream Akt activation. J Neurochem 106:134-146.
35. Wood TL, Bercury KK, Cifelli SE, Mursch LE, Min J, Dai J, Macklin WB (2013) mTOR: a link from the extracellular milieu to transcriptional regulation of oligodendrocyte development. ASN NEURO 5:art:e00108, doi:10.1042/AN20120092.
36. Ye P, Li L, Richards RG, DiAugustine RP, D'Ercole AJ (2002) Myelination is altered in insulin-like growth factor-I null mutant mice. J Neurosci 22:6041-6051.