Modulation of subventricular zone oligodendrogenesis: A role for hemopressin?

Frontiers in Cellular Neuroscience

Volumn 8, Issue FEB, 2014, Pages

  Xapelli, Sara ^a,b   Agasse, Fabienne ^a   Grade, Sofia ^a,c,d   Bernardino, Liliana ^a,e   Ribeiro, Filipa F ^b   Schitine, Clarissa S ^f   Heimann, Andrea S ^g   Ferro, Emer S ^h   Sebastião, Ana M ^b   De Melo Reis, Ricardo A ^f   Malva, João O ^a,i  

^a UNIVERSITY OF COIMBRA   (Portugal)

^b UNIVERSITY OF LISBON   (Portugal)

^c INSTITUTE OF EPIDEMIOLOGY   (Germany)

^d UNIVERSITY OF MUNICH   (Germany)

^e UNIVERSITY OF BEIRA INTERIOR   (Portugal)

^f FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^g Neurochemistry Laboratory Biophysics Institute Carlos Chagas Filho Federal University of Rio de Janeiro ^*  (Brazil)

^h UNIVERSITY OF SÃO PAULO   (Brazil)

ⁱ UNIVERSITY OF COIMBRA   (Portugal)

Author keywords

Endocannabinoids; Hemopressin; Myelin pathologies; Oligodendrogenesis; Subventricular zone

Indexed keywords

DNA NUCLEOTIDYLEXOTRANSFERASE; GALACTOSYLCERAMIDASE; GLIAL FIBRILLARY ACIDIC PROTEIN; HEMOGLOBIN DERIVATIVE; HEMOPRESSIN; HISTAMINE; OLIGODENDROCYTE TRANSCRIPTION FACTOR 2; PLATELET DERIVED GROWTH FACTOR ALPHA RECEPTOR; POTASSIUM CHLORIDE; PROTEOLIPID PROTEIN; THROMBIN; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL DEATH; CELL MATURATION; CELL PROLIFERATION; CELL VIABILITY; CONTROLLED STUDY; FLUORESCENCE IMAGING; IMMUNOCOMPETENT CELL; IMMUNOCYTOCHEMISTRY; IMMUNOREACTIVITY; MOUSE; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; NICK END LABELING; NONHUMAN; OLIGODENDROGENESIS; OLIGODENDROGLIA; ORGANOGENESIS; SUBVENTRICULAR ZONE; WESTERN BLOTTING;

EID: 84901347333     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2014.00059     Document Type: Article

References (71)

1. Agasse, F., Bernardino, L., Silva, B., Ferreira, R., Grade, S., and Malva, J. O. (2008). Response to histamine allows the functional identification of neuronal progenitors, neurons, astrocytes, and immature cells in subventricular zone cell cultures. Rejuvenation Res. 11, 187-200. doi: 10.1089/rej.2007.0600
2. Aguado, T., Monory, K., Palazuelos, J., Stella, N., Cravatt, B., Lutz, B., et al. (2005). The endocannabinoid system drives neural progenitor proliferation. FASEB J. 19, 1704-1706. doi: 10.1096/fj.05-3995fje
3. Akiyama, Y., Honmou, O., Kato, T., Uede, T., Hashi, K., and Kocsis, J. D. (2001). Transplantation of clonal neural precursor cells derived from adult human brain establishes functional peripheral myelin in the rat spinal cord. Exp. Neurol. 167, 27-39. doi: 10.1006/exnr.2000.7539
4. Arevalo-Martin, A., Garcia-Ovejero, D., Rubio-Araiz, A., Gomez, O., Molina-Holgado, F., and Molina-Holgado, E. (2007). Cannabinoids modulate Olig2 and polysialylated neural cell adhesion molecule expression in the subventricular zone of post-natal rats through cannabinoid receptor 1 and cannabinoid receptor 2. Eur. J. Neurosci. 26, 1548-1559. doi: 10.1111/j.1460-9568.2007.05782.x
5. Azim, K., Raineteau, O., and Butt, A. M. (2012). Intraventricular injection of FGF-2 promotes generation of oligodendrocyte-lineage cells in the postnatal and adult forebrain. Glia 60, 1977-1990. doi: 10.1002/glia.22413
6. Bergles, D. E., Jabs, R., and Steinhauser, C. (2010). Neuron-glia synapses in the brain. Brain Res. Rev. 63, 130-137. doi: 10.1016/j.brainresrev.2009.12.003
7. Blaschuk, K. L., Frost, E. E., and ffrench-Constant, C. (2000). The regulation of proliferation and differentiation in oligodendrocyte progenitor cells by alphaV integrins. Development 127, 1961-1969.
8. Bomar, M. G., and Galande, A. K. (2013). Modulation of the cannabinoid receptors by hemopressin peptides. Life Sci. 92, 520-524. doi: 10.1016/j.lfs.2012.07.028
9. Cayre, M., Bancila, M., Virard, I., Borges, A., and Durbec, P. (2006). Migrating and myelinating potential of subventricular zone neural progenitor cells in white matter tracts of the adult rodent brain. Mol. Cell. Neurosci. 31, 748-758. doi: 10.1016/j.mcn.2006.01.004
10. Clarke, L. E., Young, K. M., Hamilton, N. B., Li, H., Richardson, W. D., and Attwell, D. (2012). Properties and fate of oligodendrocyte progenitor cells in the corpus callosum, motor cortex, and piriform cortex of the mouse. J. Neurosci. 32, 8173-8185. doi: 10.1523/JNEUROSCI.0928-12.2012
11. Clemente, D., Ortega, M. C., Arenzana, F. J., and de, C. F. (2011). FGF-2 and Anosmin-1 are selectively expressed in different types of multiple sclerosis lesions. J. Neurosci. 31, 14899-14909. doi: 10.1523/JNEUROSCI.1158-11.2011
12. Colognato, H., Ramachandrappa, S., Olsen, I. M., and ffrench-Constant, C. (2004). Integrins direct Src family kinases to regulate distinct phases of oligodendrocyte development. J. Cell Biol. 167, 365-375. doi: 10.1083/jcb.200404076
13. Dimou, L., Simon, C., Kirchhoff, F., Takebayashi, H., and Gotz, M. (2008). Progeny of Olig2-expressing progenitors in the gray and white matter of the adult mouse cerebral cortex. J. Neurosci. 28, 10434-10442. doi: 10.1523/JNEUROSCI.2831-08.2008
14. Dobson, N. R., Zhou, Y. X., Flint, N. C., and Armstrong, R. C. (2008). Musashi1 RNA-binding protein regulates oligodendrocyte lineage cell differentiation and survival. Glia 56, 318-330. doi: 10.1002/glia.20615
15. Dodd, G. T., Mancini, G., Lutz, B., and Luckman, S. M. (2010). The peptide hemopressin acts through CB1 cannabinoid receptors to reduce food intake in rats and mice. J. Neurosci. 30, 7369-7376. doi: 10.1523/JNEUROSCI.5455-09.2010
16. Dodd, G. T., Worth, A. A., Hodkinson, D. J., Srivastava, R. K., Lutz, B., Williams, S. R., et al. (2013). Central functional response to the novel peptide cannabinoid, hemopressin. Neuropharmacology 71, 27-36. doi: 10.1016/j.neuropharm.2013.03.007
17. Franklin, R. J., and ffrench-Constant, C. (2008). Remyelination in the CNS: from biology to therapy. Nat. Rev. Neurosci. 9, 839-855. doi: 10.1038/nrn2480
18. Franklin, R. J., Zhao, C., and Sim, F. J. (2002). Ageing and CNS remyelination. Neuroreport 13, 923-928. doi: 10.1097/00001756-200205240-00001
19. Frohman, E. M., Racke, M. K., and Raine, C. S. (2006). Multiple sclerosis-the plaque and its pathogenesis. N. Engl. J. Med. 354, 942-955. doi: 10.1056/NEJMra052130
20. Furusho, M., Dupree, J. L., Nave, K. A., and Bansal, R. (2012). Fibroblast growth factor receptor signaling in oligodendrocytes regulates myelin sheath thickness. J. Neurosci. 32, 6631-6641. doi: 10.1523/JNEUROSCI.6005-11.2012
21. Furusho, M., Kaga, Y., Ishii, A., Hebert, J. M., and Bansal, R. (2011). Fibroblast growth factor signaling is required for the generation of oligodendrocyte progenitors from the embryonic forebrain. J. Neurosci. 31, 5055-5066. doi: 10.1523/JNEUROSCI.4800-10.2011
22. Galve-Roperh, I., Aguado, T., Palazuelos, J., and Guzman, M. (2008). Mechanisms of control of neuron survival by the endocannabinoid system. Curr. Pharm. Des. 14, 2279-2288. doi: 10.2174/138161208785740117
23. Gomes, I., Dale, C. S., Casten, K., Geigner, M. A., Gozzo, F. C., Ferro, E. S., et al. (2010). Hemoglobin-derived peptides as novel type of bioactive signaling molecules. AAPS J. 12, 658-669. doi: 10.1208/s12248-010-9217-x
24. Gomez, O., Arevalo-Martin, A., Garcia-Ovejero, D., Ortega-Gutierrez, S., Cisneros, J. A., Almazan, G., et al. (2010). The constitutive production of the endocannabinoid 2-arachidonoylglycerol participates in oligodendrocyte differentiation. Glia 58, 1913-1927. doi: 10.1002/glia.21061
25. Gomez, O., Sanchez-Rodriguez, A., Le, M., Sanchez-Caro, C., Molina-Holgado, F., and Molina-Holgado, E. (2011). Cannabinoid receptor agonists modulate oligodendrocyte differentiation by activating PI3K/Akt and the mammalian target of rapamycin (mTOR) pathways. Br. J. Pharmacol. 163, 1520-1532. doi: 10.1111/j.1476-5381.2011.01414.x
26. Goncalves, M. B., Suetterlin, P., Yip, P., Molina-Holgado, F., Walker, D. J., Oudin, M. J., et al. (2008). A diacylglycerol lipase-CB2 cannabinoid pathway regulates adult subventricular zone neurogenesis in an age-dependent manner. Mol. Cell. Neurosci. 38, 526-536. doi: 10.1016/j.mcn.2008.05.001
27. Gonzalez-Perez, O., and Alvarez-Buylla, A. (2011). Oligodendrogenesis in the subventricular zone and the role of epidermal growth factor. Brain Res. Rev. 67, 147-156. doi: 10.1016/j.brainresrev.2011.01.001
28. Grade, S., Agasse, F., Bernardino, L., Silva, C. G., Cortes, L., and Malva, J. O. (2010). Functional identification of neural stem cell-derived oligodendrocytes by means of calcium transients elicited by thrombin. Rejuvenation Res. 13, 27-37. doi: 10.1089/rej.2009.0889
29. Grade, S., Bernardino, L., and Malva, J. O. (2013). Oligodendrogenesis from neural stem cells: Perspectives for remyelinating strategies. Int. J. Dev. Neurosci. 31, 692-670. doi: 10.1016/j.ijdevneu.2013.01.004
30. Heimann, A. S., Gomes, I., Dale, C. S., Pagano, R. L., Gupta, A., de Souza, L. L., et al. (2007). Hemopressin is an inverse agonist of CB1 cannabinoid receptors. Proc. Natl. Acad. Sci. U.S.A. 104, 20588-20593. doi: 10.1073/pnas.0706980105
31. Jackson, E. L., Garcia-Verdugo, J. M., Gil-Perotin, S., Roy, M., Quinones-Hinojosa, A., VandenBerg, S., et al. (2006). PDGFR alpha-positive B cells are neural stem cells in the adult SVZ that form glioma-like growths in response to increased PDGF signaling. Neuron 51, 187-199. doi: 10.1016/j.neuron.2006.06.012
32. Jin, K., Xie, L., Kim, S. H., Parmentier-Batteur, S., Sun, Y., Mao, X. O., et al. (2004). Defective adult neurogenesis in CB1 cannabinoid receptor knockout mice. Mol. Pharmacol. 66, 204-208. doi: 10.1124/mol.66.2.204
33. Kaga, Y., Shoemaker, W. J., Furusho, M., Bryant, M., Rosenbluth, J., Pfeiffer, S. E., et al. (2006). Mice with conditional inactivation of fibroblast growth factor receptor-2 signaling in oligodendrocytes have normal myelin but display dramatic hyperactivity when combined with Cnp1 inactivation. J. Neurosci. 26, 12339-12350. doi: 10.1523/JNEUROSCI.3573-06.2006
34. Kang, S. H., Fukaya, M., Yang, J. K., Rothstein, J. D., and Bergles, D. E. (2010). NG2+ CNS glial progenitors remain committed to the oligodendrocyte lineage in postnatal life and following neurodegeneration. Neuron 68, 668-681. doi: 10.1016/j.neuron.2010.09.009
35. Keirstead, H. S., Ben-Hur, T., Rogister, B., O'Leary, M. T., Dubois-Dalcq, M., and Blakemore, W. F. (1999). Polysialylated neural cell adhesion molecule-positive CNS precursors generate both oligodendrocytes and Schwann cells to remyelinate the CNS after transplantation. J. Neurosci. 19, 7529-7536.
36. Kessaris, N., Fogarty, M., Iannarelli, P., Grist, M., Wegner, M., and Richardson, W. D. (2006). Competing waves of oligodendrocytes in the forebrain and postnatal elimination of an embryonic lineage. Nat. Neurosci. 9, 173-179. doi: 10.1038/nn1620
37. Kotter, M. R., Stadelmann, C., and Hartung, H. P. (2011). Enhancing remyelination in disease-can we wrap it up? Brain 134, 1882-1900. doi: 10.1093/brain/awr014
38. Laursen, L. S., Chan, C. W., and ffrench-Constant, C. (2011). Translation of myelin basic protein mRNA in oligodendrocytes is regulated by integrin activation and hnRNP-K. J. Cell Biol. 192, 797-811. doi: 10.1083/jcb.201007014
39. Levison, S. W., and Goldman, J. E. (1993). Both oligodendrocytes and astrocytes develop from progenitors in the subventricular zone of postnatal rat forebrain. Neuron 10, 201-212. doi: 10.1016/0896-6273(93)90311-E
40. Loulier, K., Ruat, M., and Traiffort, E. (2006). Increase of proliferating oligodendroglial progenitors in the adult mouse brain upon Sonic hedgehog delivery in the lateral ventricle. J. Neurochem. 98, 530-542. doi: 10.1111/j.1471-4159.2006.03896.x
41. Mackie, K. (2008). Cannabinoid receptors: where they are and what they do. J. Neuroendocrinol. 20(Suppl. 1), 10-14. doi: 10.1111/j.1365-2826.2008.01671.x
42. Maire, C. L., Wegener, A., Kerninon, C., and Nait-Oumesmar, B. (2010). Gain-of-function of Olig transcription factors enhances oligodendrogenesis and myelination. Stem Cells 28, 1611-1622. doi: 10.1002/stem.480
43. Menn, B., Garcia-Verdugo, J. M., Yaschine, C., Gonzalez-Perez, O., Rowitch, D., and Alvarez-Buylla, A. (2006). Origin of oligodendrocytes in the subventricular zone of the adult brain. J. Neurosci. 26, 7907-7918. doi: 10.1523/JNEUROSCI.1299-06.2006
44. Milner, R., Edwards, G., Streuli, C., and ffrench-Constant, C. (1996). A role in migration for the alpha V beta 1 integrin expressed on oligodendrocyte precursors. J. Neurosci. 16, 7240-7252.
45. Milner, R., and ffrench-Constant, C. (1994). A developmental analysis of oligodendroglial integrins in primary cells: changes in alpha v-associated beta subunits during differentiation. Development 120, 3497-3506.
46. Molina-Holgado, F., Rubio-Araiz, A., Garcia-Ovejero, D., Williams, R. J., Moore, J. D., Arevalo-Martin, A., et al. (2007). CB2 cannabinoid receptors promote mouse neural stem cell proliferation. Eur. J. Neurosci. 25, 629-634. doi: 10.1111/j.1460-9568.2007.05322.x
47. Nait-Oumesmar, B., Decker, L., Lachapelle, F., Avellana-Adalid, V., Bachelin, C., and Baron-Van, E. A. (1999). Progenitor cells of the adult mouse subventricular zone proliferate, migrate and differentiate into oligodendrocytes after demyelination. Eur. J. Neurosci. 11, 4357-4366. doi: 10.1046/j.1460-9568.1999.00873.x
48. Nait-Oumesmar, B., Picard-Riera, N., Kerninon, C., Decker, L., Seilhean, D., Hoglinger, G. U., et al. (2007). Activation of the subventricular zone in multiple sclerosis: evidence for early glial progenitors. Proc. Natl. Acad. Sci. U.S.A. 104, 4694-4699. doi: 10.1073/pnas.0606835104
49. Najm, F. J., Lager, A. M., Zaremba, A., Wyatt, K., Caprariello, A. V., Factor, D. C., et al. (2013). Transcription factor-mediated reprogramming of fibroblasts to expandable, myelinogenic oligodendrocyte progenitor cells. Nat. Biotechnol. 31, 426-433. doi: 10.1038/nbt.2561
50. Nakatani, H., Martin, E., Hassani, H., Clavairoly, A., Maire, C. L., Viadieu, A., et al. (2013). Ascl1/Mash1 Promotes Brain Oligodendrogenesis during Myelination and Remyelination. J. Neurosci. 33, 9752-9768. doi: 10.1523/JNEUROSCI.0805-13.2013
51. Nave, K. A., and Trapp, B. D. (2008). Axon-glial signaling and the glial support of axon function. Annu. Rev. Neurosci. 31, 535-561. doi: 10.1146/annurev.neuro.30.051606.094309
52. Nishiyama, A., Komitova, M., Suzuki, R., and Zhu, X. (2009). Polydendrocytes (NG2 cells): multifunctional cells with lineage plasticity. Nat. Rev. Neurosci. 10, 9-22. doi: 10.1038/nrn2495
53. Onaivi, E. S., Ishiguro, H., Gong, J. P., Patel, S., Perchuk, A., Meozzi, P. A., et al. (2006). Discovery of the presence and functional expression of cannabinoid CB2 receptors in brain. Ann. N. Y. Acad. Sci. 1074, 514-536. doi: 10.1196/annals.1369.052
54. Ortega, F., Gascon, S., Masserdotti, G., Deshpande, A., Simon, C., Fischer, J., et al. (2013). Oligodendrogliogenic and neurogenic adult subependymal zone neural stem cells constitute distinct lineages and exhibit differential responsiveness to Wnt signalling. Nat. Cell Biol. 15, 602-613. doi: 10.1038/ncb2736
55. Pacher, P., and Kunos, G. (2013). Modulating the endocannabinoid system in human health and disease-successes and failures. FEBS J. 280, 1918-1943. doi: 10.1111/febs.12260
56. Palazuelos, J., Aguado, T., Egia, A., Mechoulam, R., Guzman, M., and Galve-Roperh, I. (2006). Non-psychoactive CB2 cannabinoid agonists stimulate neural progenitor proliferation. FASEB J. 20, 2405-2407. doi: 10.1096/fj.06-6164fje
57. Picard-Riera, N., Decker, L., Delarasse, C., Goude, K., Nait-Oumesmar, B., Liblau, R., et al. (2002). Experimental autoimmune encephalomyelitis mobilizes neural progenitors from the subventricular zone to undergo oligodendrogenesis in adult mice. Proc. Natl. Acad. Sci. U.S.A. 99, 13211-13216. doi: 10.1073/pnas.192314199
58. Pluchino, S., Quattrini, A., Brambilla, E., Gritti, A., Salani, G., Dina, G., et al. (2003). Injection of adult neurospheres induces recovery in a chronic model of multiple sclerosis. Nature 422, 688-694. doi: 10.1227/01.neu.0000309408.99477.a5
59. Polito, A., and Reynolds, R. (2005). NG2-expressing cells as oligodendrocyte progenitors in the normal and demyelinated adult central nervous system. J. Anat. 207, 707-716. doi: 10.1111/j.1469-7580.2005.00454.x
60. Rafalski, V. A., Ho, P. P., Brett, J. O., Ucar, D., Dugas, J. C., Pollina, E. A., et al. (2013). Expansion of oligodendrocyte progenitor cells following SIRT1 inactivation in the adult brain. Nat. Cell Biol. 15, 614-624. doi: 10.1038/ncb2735
61. Ramirez-Castillejo, C., Sanchez-Sanchez, F., Andreu-Agullo, C., Ferron, S. R., roca-Aguilar, J. D., Sanchez, P., et al. (2006). Pigment epithelium-derived factor is a niche signal for neural stem cell renewal. Nat. Neurosci. 9, 331-339. doi: 10.1038/nn1657
62. Relucio, J., Menezes, M. J., Miyagoe-Suzuki, Y., Takeda, S., and Colognato, H. (2012). Laminin regulates postnatal oligodendrocyte production by promoting oligodendrocyte progenitor survival in the subventricular zone. Glia 60, 1451-1467. doi: 10.1002/glia.22365
63. Santra, M., Chopp, M., Zhang, Z. G., Lu, M., Santra, S., Nalani, A., et al. (2012). Thymosin beta 4 mediates oligodendrocyte differentiation by upregulating p38 MAPK. Glia 60, 1826-1838. doi: 10.1002/glia.22400
64. Smith, P. M., and Blakemore, W. F. (2000). Porcine neural progenitors require commitment to the oligodendrocyte lineage prior to transplantation in order to achieve significant remyelination of demyelinated lesions in the adult CNS. Eur. J. Neurosci. 12, 2414-2424. doi: 10.1046/j.1460-9568.2000.00137.x
65. Sohn, J., Selvaraj, V., Wakayama, K., Orosco, L., Lee, E., Crawford, S. E., et al. (2012). PEDF is a novel oligodendrogenic morphogen acting on the adult SVZ and corpus callosum. J. Neurosci. 32, 12152-12164. doi: 10.1523/JNEUROSCI.0628-12.2012
66. Solbrig, M. V., Fan, Y., Hermanowicz, N., Morgese, M. G., and Giuffrida, A. (2010). A synthetic cannabinoid agonist promotes oligodendrogliogenesis during viral encephalitis in rats. Exp. Neurol. 226, 231-241. doi: 10.1016/j.expneurol.2010.09.003
67. Sun, J., Fang, Y., Chen, T., Guo, J., Yan, J., Song, S., et al. (2013). WIN55, 212-2 promotes differentiation of oligodendrocyte precursor cells and improve remyelination through regulation of the phosphorylation level of the ERK 1/2 via cannabinoid receptor 1 after stroke-induced demyelination. Brain Res. 1491, 225-235. doi: 10.1016/j.brainres.2012.11.006
68. Velayudhan, L., Van, D. E., Marudkar, M., Hands, O., Suribhatla, S., Prettyman, R., et al. (2013). Therapeutic potential of cannabinoids in neurodegenerative disorders: a selective review. Curr. Pharm. Des. [Epub ahead of print].
69. Whittemore, S. R., Morassutti, D. J., Walters, W. M., Liu, R. H., and Magnuson, D. S. (1999). Mitogen and substrate differentially affect the lineage restriction of adult rat subventricular zone neural precursor cell populations. Exp. Cell Res. 252, 75-95. doi: 10.1006/excr.1999.4621
70. Xapelli, S., Agasse, F., Sarda-Arroyo, L., Bernardino, L., Santos, T., Ribeiro, F. F., et al. (2013). Activation of Type 1 cannabinoid receptor (CB1R) promotes neurogenesis in murine subventricular zone cell cultures. PLoS ONE 8:e63529. doi: 10.1371/journal.pone.0063529
71. Yang, N., Zuchero, J. B., Ahlenius, H., Marro, S., Ng, Y. H., Vierbuchen, T., et al. (2013). Generation of oligodendroglial cells by direct lineage conversion. Nat. Biotechnol. 31, 434-439. doi: 10.1038/nbt.2564