Remyelination by Resident Oligodendrocyte Precursor Cells in a Xenopus laevis Inducible Model of Demyelination

Developmental Neuroscience

Volumn 37, Issue 3, 2015, Pages 232-242

  Sekizar, Sowmya ^a,b   Mannioui, Abdelkrim ^a,b   Azoyan, Loris ^a,b   Colin, Catherine ^a,b   Thomas, Jean León ^a,b,c,e   Du Pasquier, David ^d   Mallat, Michel ^a,b   Zalc, Bernard ^a,b,c  

^a SORBONNE UNIVERSITÉ   (France)

^b INSTITUT DU CERVEAU ET DE LA MOELLE ÉPINIÈRE   (France)

^c PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^d WATCHFROG S A   (France)

^e YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Isolectin B4; Microglia; Multiple sclerosis; Myelin; Myelin repair; Sox10; Transgenic Xenopus model

Indexed keywords

ANKYRIN; ANKYRIN G; GREEN FLUORESCENT PROTEIN; METRONIDAZOLE; MYELIN; MYELIN BASIC PROTEIN; NITROREDUCTASE; PROTEIN NODAL; TRANSCRIPTION FACTOR SOX10; UNCLASSIFIED DRUG; ANTIINFECTIVE AGENT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DEMYELINATING DISEASE; DEMYELINATION; GENE EXPRESSION; MICROGLIA; MYELIN SHEATH; NONHUMAN; OLIGODENDROCYTE PRECURSOR CELL; OLIGODENDROGLIA; OPTIC NERVE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; REGULATORY SEQUENCE; REMYELINIZATION; TRANSGENE; TRANSGENIC ANIMAL; XENOPUS LAEVIS; ANIMAL; CHEMICALLY INDUCED; DISEASE MODEL; DRUG EFFECTS; METABOLISM; NERVE REGENERATION; NEURAL STEM CELL; PATHOLOGY; PHYSIOLOGY;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; ANTI-INFECTIVE AGENTS; DEMYELINATING DISEASES; DISEASE MODELS, ANIMAL; METRONIDAZOLE; MICROGLIA; MYELIN SHEATH; NERVE REGENERATION; NEURAL STEM CELLS; OLIGODENDROGLIA; XENOPUS LAEVIS;

EID: 84937643002     PISSN: 03785866     EISSN: 14219859     Source Type: Journal    
DOI: 10.1159/000380817     Document Type: Article

References (46)

1. Zalc B, Goujet D, Colman D: The origin of the myelination program in vertebrates. Curr Biol 2008; 18:R511-R512.
2. Lucchinetti CF, Bruck W, Rodriguez M, Lassmann H: Distinct patterns of multiple sclerosis pathology indicates heterogeneity on pathogenesis. Brain Pathol 1996; 6: 259-274.
3. Dowling P, Ming X, Raval S, Husar W, Casaccia-Bonnefil P, Chao M, Cook S, Blumberg B: Up-regulated p75NTR neurotrophin receptor on glial cells in MS plaques. Neurology 1999; 53: 1676-1682.
4. Feigenbaum V, Gelot A, Casanova P, Daumas-Duport C, Aubourg P, Dubois-Dalcq M: Apoptosis in the central nervous system of cerebral adrenoleukodystrophy patients. Neurobiol Dis 2000; 7: 600-612.
5. Kettenmann H, Hanisch UK, Noda M, Verkhratsky A: Physiology of microglia. Physiol Rev 2011; 91: 461-553.
6. Marburg O: Die sogenannte 'akute multiple Sklerose'. Leipzig, Deuticke, 1906, pp 37 and 47.
7. Perier O, Gregoire A: Electron microscopic features of multiple sclerosis lesions. Brain 1965; 88: 937-952.
8. Levine JM, Reynolds R: Activation and proliferation of endogenous oligodendrocyte precursor cells during ethidium bromide-induced demyelination. Exp Neurol 1999; 160: 333-347.
9. Kaya F, Mannioui A, Chesneau A, Sekizar S, Maillard E, Ballagny C, Houel-Renault L, Dupasquier D, Bronchain O, Holtzmann I, Desmazieres A, Thomas JL, Demeneix BA, Brophy PJ, Zalc B, Mazabraud A: Live imaging of targeted cell ablation in Xenopus: a new model to study demyelination and repair. J Neurosci 2012; 32: 12885-12895.
10. De Luze A, Sachs L, Demeneix B: Thyroid hormone-dependent transcriptional regulation of exogenous genes transferred into Xenopus tadpole muscle in vivo. Proc Natl Acad Sci USA 1993; 90: 7322-7326.
11. Nieuwkoop PD, Faber J: Normal Table of Xenopus laevis (Daudin). New York, Garland Publishing, 1994.
12. Yoshida M: Oligodendrocyte maturation in Xenopus laevis. J Neurosci Res 1997; 50: 169-176.
13. Cima C, Grant P: Development of the optic nerve in Xenopus laevis. II. Gliogenesis, myelination and metamorphic remodelling. J Embryol Exp Morphol 1982; 72: 251-267.
14. Guillery RW: On counting and counting errors. J Comp Neurol 2002; 447: 1-7.
15. Stankoff B, Demerens C, Goujet-Zalc C, Monge M, Peyron F, Mikoshiba K, Zalc B, Lubetzki C: Transcription of myelin basic protein promoted by regulatory elements in the proximal 5 sequence requires myelinogenesis. Mult Scler 1996; 2: 125-132.
16. Small RK, Riddle P, Noble M: Evidence for migration of oligodendrocyte-type-2 astrocyte progenitor cells into the developing rat optic nerve. Nature 1987; 328: 155-157.
17. Giess MC, Soula C, Duprat AM, Cochard P: Cells from the early chick optic nerve generate neurons but not oligodendrocytes in vitro. Brain Res Dev Brain Res 1992; 70: 163-171.
18. Ono K, Yasui Y, Rutishauser U, Miller RH: Focal ventricular origin and migration of oligodendrocyte precursors into the chick optic nerve. Neuron 1997; 19: 283-292.
19. Kuhlbrodt K, Herbarth B, Sock E, Hermans-Borgmeyer I, Wegner M: Sox10, a novel transcriptional modulator in glial cells. J Neurosci 1998; 18: 237-250.
20. Stolt CC, Rehberg S, Ader M, Lommes P, Riethmacher D, Schachner M, Bartsch U, Wegner M: Terminal differentiation of myelinforming oligodendrocytes depends on the transcription factor Sox10. Genes Dev 2002; 16: 165-170.
21. Robinson S, Miller RH: Contact with central nervous system myelin inhibits oligodendrocyte progenitor maturation. Dev Biol 1999; 216: 359-368.
22. Kotter MR, Li WW, Zhao C, Franklin RJ: Myelin impairs CNS remyelination by inhibiting oligodendrocyte precursor cell differentiation. J Neurosci 2006; 26: 328-332.
23. Nielsen HH, Ladeby R, Fenger C, Toft-Hansen H, Babcock AA, Owens T, Finsen B: Enhanced microglial clearance of myelin debris in T cell-infiltrated central nervous system. J Neuropathol Exp Neurol 2009; 68: 845-856.
24. Gaudet AD, Popovich PG, Ramer MS: Wallerian degeneration: gaining perspective on inflammatory events after peripheral nerve injury. J Neuroinflamm 2011; 8: 110.
25. Gudi V, Gingele S, Skripuletz T, Stangel M: Glial response during cuprizone-induced deand remyelination in the CNS: lessons learned. Front Cell Neurosci 2014; 8: 73.
26. Smith AJ, Liu Y, Peng H, Beers R, Racke MK, Lovett-Racke AE: Comparison of a classical Th1 bacteria versus a Th17 bacteria as adjuvant in the induction of experimental autoimmune encephalomyelitis. J Neuroimmunol 2011; 237: 33-38.
27. Streit WJ, Kreutzberg GW: Lectin binding by resting and reactive microglia. J Neurocytol 1987; 16: 249-260.
28. Naujoks-Manteuffel C, Niemann U: Microglial cells in the brain of Pleurodeles waltl (Urodela, Salamandridae) after wallerian degeneration in the primary visual system using Bandeiraea simplicifolia isolectin B4-cytochemistry. Glia 1994; 10: 101-113.
29. McGlade-McCulloh E, Morrissey AM, Norona F, Muller KJ: Individual microglia move rapidly and directly to nerve lesions in the leech central nervous system. Proc Natl Acad Sci USA 1989; 86: 1093-1097.
30. Goodbrand IA, Gaze RM: Microglia in tadpoles of Xenopus laevis: normal distribution and the response to optic nerve injury. Anat Embryol (Berl) 1991; 184: 71-82.
31. Cuadros MA, Martin C, Coltey P, Almendros A, Navascues J: First appearance, distribution, and origin of macrophages in the early development of the avian central nervous system. J Comp Neurol 1993; 330: 113-129.
32. Herbomel P, Thisse B, Thisse C: Zebrafish early macrophages colonize cephalic mesenchyme and developing brain, retina, and epidermis through a M-CSF receptor-dependent invasive process. Dev Biol 2001; 238: 274-288.
33. Ginhoux F, Greter M, Leboeuf M, Nandi S, See P, Gokhan S, Mehler MF, Conway SJ, Ng LG, Stanley ER, Samokhvalov IM, Merad M: Fate mapping analysis reveals that adult microglia derive from primitive macrophages. Science 2010; 330: 841-845.
34. Schulz C, Gomez Perdiguero E, Chorro L, Szabo-Rogers H, Cagnard N, Kierdorf K, Prinz M, Wu B, Jacobsen SE, Pollard JW, Frampton J, Liu KJ, Geissmann F: A lineage of myeloid cells independent of Myb and hematopoietic stem cells. Science 2012; 336: 86-90.
35. Hochreiter-Hufford A, Ravichandran KS: Clearing the dead: apoptotic cell sensing, recognition, engulfment, and digestion. Cold Spring Harb Perspect Biol 2013; 5:a008748.
36. Corriden R, Insel PA: New insights regarding the regulation of chemotaxis by nucleotides, adenosine, and their receptors. Purinergic Signal 2012; 8: 587-598.
37. Honda S, Sasaki Y, Ohsawa K, Imai Y, Nakamura Y, Inoue K, Kohsaka S: Extracellular ATP or ADP induce chemotaxis of cultured microglia through Gi/o-coupled P2Y receptors. J Neurosci 2001; 21: 1975-1982.
38. Nagata S, Hanayama R, Kawane K: Autoimmunity and the clearance of dead cells. Cell 2010; 140: 619-630.
39. Marin-Teva JL, Dusart I, Colin C, Gervais A, van Rooijen N, Mallat M: Microglia promote the death of developing Purkinje cells. Neuron 2004; 41: 535-547.
40. Sierra A, Abiega O, Shahraz A, Neumann H: Janus-faced microglia: beneficial and detrimental consequences of microglial phagocytosis. Front Cell Neurosci 2013; 7: 6.
41. Gaze RM, Peters A: The development, structure and composition of the optic nerve of Xenopus laevis (Daudin). Q J Exp Physiol Cogn Med Sci 1961; 46: 299-309.
42. Wolswijk G, Noble M: Identification of an adult-specific glial progenitor cell. Development 1989; 105: 387-400.
43. Dawson MR, Polito A, Levine JM, Reynolds R: NG2-expressing glial progenitor cells: an abundant and widespread population of cycling cells in the adult rat CNS. Mol Cell Neurosci 2003; 24: 476-488.
44. Chari DM, Blakemore WF: Efficient recolonisation of progenitor-depleted areas of the CNS by adult oligodendrocyte progenitor cells. Glia 2002; 37: 307-313.
45. Fancy SP, Zhao C, Franklin RJ: Increased expression of Nkx2.2 and Olig2 identifies reactive oligodendrocyte progenitor cells responding to demyelination in the adult CNS. Mol Cell Neurosci 2004; 27: 247-254.
46. Nait-Oumesmar B, Picard-Riera N, Kerninon C, Decker L, Seilhean D, Hoglinger GU, Hirsch EC, Reynolds R, Baron-Van Evercooren A: Activation of the subventricular zone in multiple sclerosis: evidence for early glial progenitors. Proc Natl Acad Sci USA 2007; 104: 4694-4699.