pH is an intracellular effector controlling differentiation of oligodendrocyte precursors in culture via activation of the ERK1/2 pathway

Journal of Neuroscience Research

Volumn 84, Issue 7, 2006, Pages 1392-1401

  Bernard, Frédéric ^a,b,c   Vanhoutte, Peter ^b,c   Bennasroune, Amar ^a   Labourdette, Gérard ^a   Perraut, Martine ^a   Aunis, Dominique ^a   Gaillard, Stéphane ^a,d  

^a INSERM   (France)

^b Université Pierre et Marie Curie   (France)

^c SORBONNE UNIVERSITÉ   (France)

^d CENTRE DE NEUROCHIMIE   (France)

Author keywords

Differentiation; ERK; Oligodendrocyte; pH; Retinoic acid; Signaling

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; RETINOIC ACID; STRESS ACTIVATED PROTEIN KINASE; UO 126;

ACIDITY; ALKALINITY; ANIMAL CELL; ARTICLE; CELL PH; CONTROLLED STUDY; DRUG INHIBITION; DRUG MECHANISM; ENZYME ACTIVATION; ENZYME INHIBITION; NERVE CELL CULTURE; NERVE CELL DIFFERENTIATION; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; RAT;

ANIMALS; ANIMALS, NEWBORN; BLOTTING, WESTERN; BUTADIENES; CELL DIFFERENTIATION; CELLS, CULTURED; CEREBELLUM; ENZYME ACTIVATION; ENZYME INHIBITORS; EXTRACELLULAR FLUID; GANGLIOSIDES; HYDROGEN-ION CONCENTRATION; IMMUNOHISTOCHEMISTRY; MAP KINASE SIGNALING SYSTEM; MITOGEN-ACTIVATED PROTEIN KINASE 3; NERVE TISSUE PROTEINS; NITRILES; OLIGODENDROGLIA; OLIGOSACCHARIDES; RATS; STEM CELLS; TIME FACTORS; TRETINOIN;

EID: 33750591169     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.21051     Document Type: Article

References (58)

1. Alvarez J, Garcia-Sancho J, Mollinedo F, Sanchez A. 1989. Intracellular Ca2+ potentiates Na+/H+ exchange and cell differentiation induced by phorbol ester in U937 cells. Eur J Biochem 183:709-714.
2. Balazs R, Gallo V, Kingsbury A. 1988. Effect of depolarization on the maturation of cerebellar granule cells in culture. Brain Res 468:269-276.
3. Baron W, Metz B, Bansal R, Hoekstra D, de Vries H. 2000. PDGF and FGF-2 signaling in oligodendrocyte progenitor cells: regulation of proliferation and differentiation by multiple intracellular signaling pathways. Mol Cell Neurosci 15:314-329.
4. Barres BA, Lazar MA, Raff MC. 1994. A novel role for thyroid hormone, glucocorticoids and retinoic acid in timing oligodendrocyte development. Development 120:1097-1108.
5. Bernard F, Bossu JL, Gaillard S. 2001. Identification of living oligodendrocyte developmental stages by fractal analysis of cell morphology. J Neurosci Res 65:439-445.
6. Besnard F, Perraud F, Sensenbrenner M, Labourdette G. 1989. Effects of acidic and basic fibroblast growth factors on proliferation and maturation of cultured rat oligodendrocytes. Int J Dev Neurosci 7:401-409.
7. Bevensee MO, Bashi E, Boron WF. 1999. Effect of trace levels of nigericin on intracellular pH and acid-base transport in rat renal mesangial cells. J Membr Biol 169:131-139.
8. Bhat NR, Zhang P. 1996. Activation of mitogen-activated protein kinases in oligodendrocytes. J Neurochem 66:1986-1994.
9. Billon N, Tokumoto Y, Fotrest D, Raff M. 2001. Role of thyroid hormone receptors in timing oligodendrocyte differentiation. Dev Biol 235:110-120.
10. Bogler O, Wren D, Barnett SC, Land H, Noble M. 1990. Cooperation between two growth factors promotes extended self-renewal and inhibits differentiation of oligodendrocyte-type-2 astrocyte (O-2A) progenitor cells. Proc Natl Acad Sci U S A 87:6368-6372.
11. Boron WF, De Weer P. 1976. Intracellular pH transients in squid giant axons caused by CO2, NH3, and metabolic inhibitors. J Gen Physiol 67:91-112.
12. Boussouf A, Gaillard S. 2000. Intracellular pH changes during oligodendrocyte differentiation in primary culture. J Neurosci Res 59:731-739.
13. Boussouf A, Lambert RC, Gaillard S. 1997. Voltage-dependent Na(+)-HCO3- cotransporter and Na+/H+ exchanger are involved in intracellular pH regulation of cultured mature rat cerebellar oligodendrocytes. Glia 19:74-84.
14. Chittajallu R, Chen Y, Wang H, Yuan X, Ghiani CA, Heckman T, McBain CJ, Gallo V. 2002. Regulation of KvI subunit expression in oligodendrocyte progenitor cells and their role in G1/S phase progression of the cell cycle. Proc Natl Acad Sci U S A 99:2350-2355.
15. Dyck JR, Fliegel L. 1995. Specific activation of the Na+/H+ exchanger gene during neuronal differentiation of embryonal carcinoma cells. J Biol Chem 270:10420-10427.
16. Gaillard S, Bossu JL. 1995. Voltage-gated ionic currents in mature oligodendrocytes isolated from rat cerebellum. Neurosci Lett 190:191-194.
17. Gallo V, Zhou JM, McBain CJ, Wright P, Knutson PL, Armstrong RC. 1996. Oligodendrocyte progenitor cell proliferation and lineage progression are regulated by glutamate receptor-mediated K+ channel block. J Neurosci 16:2659-2670.
18. Gensert JM, Goldman JE. 1997. Endogenous progenitors remyelinated demyelinated axons in the adult CNS. Neuron 19:197-203.
19. Ghiani CA, Eisen AM, Yuan X, DePinho RA, McBain CJ, Gallo V. 1999a. Neurotransmitter receptor activation triggers p27(Kip1)and p21(CIP1) accumulation and G1 cell cycle arrest in oligodendrocyte progenitors. Development 126:1077-1090.
20. Ghiani CA, Yuan X, Eisen AM, Knutson PL, DePinho RA, McBain CJ, Gallo V. 1999b. Voltage-activated K+ channels and membrane depolarization regulate accumulation of the cyclin-dependent kinase inhibitors p27(Kip1) and p21 (CIP1) in glia1 progenitor cells. J Neurosci 19:5380-5392.
21. Grinspan JB, Franceschini B. 1995. Platelet-derived growth factor is a survival factor for PSA-NCAM+ oligodendrocyte pre-progenitor cells. J Neurosci Res 41:540-551.
22. Grinstein S, Rothstein A. 1986. Mechanisms of regulation of the Na+/H+ exchanger. J Membr Biol 90:1-12.
23. Grinstein S, Rotin D, Mason MJ. 1989. Na+/H+ exchange and growth factor-induced cytosolic pH changes. Role in cellular proliferation. Biochim Biophys Acta 988:73-97.
24. Hazav P, Shany S, Moran A, Levy R. 1989. Involvement of intracellular pH elevation in the effect of 1,25-dihydroxyvitamin D3 on HL-60 cells. Cancer Res 49:72-75.
25. Ho WC, Uniyal S, Zhou H, Morris VL, Chan BM. 2005. Threshold levels of ERK activation for chemotactic migration differ for NGF and EGF in rat pheochromocytoma PC 12 cells. Mol Cell Biochem 271:29-41.
26. Hu X, Jin L, Feng L. 2004. Erk1/2 but not PI3K pathway is required for neurotrophin 3-induced oligodendrocyte differentiation of post-natal neural stem cells. J Neurochem 90:1339-1347.
27. Ladoux A, Cragoe EJ Jr, Geny B, AbitaJP, Frelin C. 1987. Differentiation of human promyelocytic HL 60 cells by retinoic acid is accompanied by an increase in the intracellular pH. The role of the Na+/H+ exchange system. J Biol Chem 262:811-816.
28. Marcinkowska E. 2001. Evidence that activation of MEK1,2/erk1,2 signal transduction pathway is necessary for calcitriol-induced differentiation of HL-60 cells. Anticancer Res 21:499-504.
29. Marshall CJ. 1995. Specificity of receptor tyrosine kinase signaling: transient versus sustained extracellular signal-regulated kinase activation. Cell 80:179-185.
30. McAdams TA, Miller WM, Papoutsakis ET. 1998. pH is a potent modulator of erythroid differentiation. Br J Haematol 103:317-325.
31. McCaffery PJ, Adams J, Maden M, Rosa-Molinar E. 2003. Too much of a good thing: retinoic acid as an endogenous regulator of neural differentiation and exogenous teratogen. Eur J Neurosci 18:457-472.
32. McNulty S, Crouch M, Smart D, Rumsby M. 2001. Differentiation of bipolar CG-4 line oligodendrocytes is associated with regulation of CREB, MAP kinase and PKC signalling pathways. Neurosci Res 41:217-226.
33. Mukhin YV, Garnovskaya MN, Ullian ME, Raymond JR. 2004. ERK is regulated by sodium-proton exchanger in rat aortic vascular smooth muscle cells. J Biol Chem 279:1845-1852.
34. Murphy LO, MacKeigan JP, Blenis J. 2004. A network of immediate early gene products propagates subtle differences in mitogen-activated protein kinase signal amplitude and duration. Mol Cell Biol 24:144-153.
35. Neusch C, Rozengurt N, Jacobs RE, Lester HA, Kofuji P. 2001. Kir4.1 potassium channel subunit is crucial for oligodendrocyte development and in vivo myelination. J Neurosci 21:5429-5438.
36. Ohtsubo T, Wang X, Takahashi A, Ohnishi K, Saito H, Song CW, Ohnishi T. 1997. p53-dependent induction of WAF1 by a low-pH culture condition in human glioblastoma cells. Cancer Res 57:3910-3913.
37. Padanilam BJ, Lu T, Hoshi T, Padanilam BA, Shibata EF, Lee HC. 2002. Molecular determinants of intracellular pH modulation of human Kv1.4 N-type inactivation. Mol Pharmacol 62:127-134.
38. Pappas CA, Ullrich N, Sontheimer H. 1994. Reduction of glial proliferation by K+ channel blockers is mediated by changes in pHi. Neuroreport 6:193-196.
39. Pessia M, Imbrici P, D'Adamo MC, Salvatore L, Tucker SJ. 2001. Differential pH sensitivity of Kir4.1 and Kir4.2 potassium channels and their modulation by heteropolymerisation with Kir5.1. J Physiol 532:359-367.
40. Putney LK, Barber DL. 2003. Na-H exchange-dependent increase in intracellular pH times G2/M entry and transition. J Biol Chem 278:44645-44649.
41. Raff MC, Mirsky R, Fields KL, Lisak RP, Dorfman SH, Silberberg DH, Gregson NA, Leibowitz S, Kennedy MC. 1978. Galactocerebroside is a specific cell-surface antigenic marker for oligodendrocytes in culture. Nature 274:813-816.
42. Ranscht B, Clapshaw PA, Price J, Noble M, Seifert W. 1982. Development of oligodendrocytes and Schwann cells studied with a monoclonal antibody against galactocerebroside. Proc Natl Acad Sci U S A 79:2709-2713.
43. Rao GN, Sardet C, Pouyssegur J, Berk BC. 1992. Na+/H+ antiporter gene expression increases during retinoic acid-induced granulocytic differentiation of HL60 cells. J Cell Physiol 151:361-366.
44. Roos A, Boron WF. 1981. Intracellular pH. Physiol Rev 61:296-434.
45. Sarosi GA Jr, Jaiswal K, Herndon E, Lopez-Guzman C, Spechler SJ, Souza RF. 2005. Acid increases MAPK-mediated proliferation in Barrett's esophageal adenocarcinoma cells via intracellular acidification through a Cl-/HCO3-exchanger. Am J Physiol Gastrointest Liver Physiol 289:G991-997.
46. Shrode LD, Rubie EA, Woodgett JR, Grinstein S. 1997a. Cytosolic alkalinization increases stress-activated protein kinase/c-Jun NH2-terminal kinase (SAPK/JNK) activity and p38 mitogen-activated protein kinase activity by a calcium-independent mechanism. J Biol Chem 272:13653-13659.
47. Shrode LD, Tapper H, Grinstein S. 1997b. Role of intracellular pH in proliferation, transformation, and apoptosis. J Bioenerg Biomembr 29:393-399.
48. Souza RF, Shewmake K, Terada LS, Spechler SJ. 2002. Acid exposure activates the mitogen-activated protein kinase pathways in Barrett's esophagus. Gastroenterology 122:299-307.
49. Staines WA, Craig J, Reuhl K, McBurney MW. 1996. Retinoic acid treated P19 embryonal carcinoma cells differentiate into oligodendrocytes capable of myelination. Neuroscience 71:845-853.
50. Tokumoto YM, Durand B, Raff MC. 1999. An analysis of the early events when oligodendrocyte precursor cells are triggered to differentiate by thyroid hormone, retinoic acid, or PDGF withdrawal. Dev Biol 213:327-339.
51. Tokumoto YM, Tang DG, Raff MC. 2001. Two molecularly distinct intracellular pathways to oligodendrocyte differentiation: role of a p53 family protein. EMBO J 20:5261-5268.
52. Vanhoutte P, Bamier JV, Guibert B, Pages C, Besson MJ, Hipskind RA, Caboche J. 1999. Glutamate induces phosphorylation of Elk-1 and CREB, along with c-fos activation, via an extracellular signal-regulated kinase-dependent pathway in brain slices. Mol Cell Biol 19:136-146.
53. Wang H, Singh D, Fliegel L. 1997. The Na+/H+ antiporter potentiates growth and retinoic acid-induced differentiation of P19 embryonal carcinoma cells. J Biol Chem 272:26545-26549.
54. Werlen G, Hausmann B, Naeher D, Palmer E. 2003. Signaling life and death in the thymus: timing is everything. Science 299:1859-1863.
55. Wolswijk G. 2002. Oligodendrocyte precursor cells in the demyelinated multiple sclerosis spinal cord. Brain 125:338-349.
56. Xu H, Cui N, Yang Z, Qu Z, Jiang C. 2000. Modulation of kir4.1 and kir5.1 by hypercapnia and intracellular acidosis. J Physiol 524:725-735.
57. Yen A, Roberson MS, Varvayanis S, Lee AT. 1998. Retinoic acid induced mitogen-activated protein (MAP)/extracellular signal-regulated kinase (ERK) kinase-dependent MAP kinase activation needed to elicit HL-60 cell differentiation and growth arrest. Cancer Res 58:3163-3172.
58. Zheng M, Reynolds C, Jo SH, Wersto R, Han Q, Xiao RP. 2005. Intracellular acidosis-activated p38 MAPK signaling and its essential role in cardiomyocyte hypoxic injury. FASEBJ 19:109-111.