Interleukin-10 regulates progenitor differentiation and modulates neurogenesis in adult brain

Journal of Cell Science

Volumn 126, Issue 18, 2013, Pages 4208-4219

  Perez Asensio, Fernando J ^a,b,c   Perpiñá, Unai ^a,b   Planas, Anna M ^a,b   Pozas, Esther ^a,b  

^a INSTITUT D INVESTIGACIONS BIOMÈDIQUES AUGUST PI I SUNYER IDIBAPS   (Spain)

^b INST D INVESTIGACIONS B   (Spain)

^c UNIVERSITY OF BARCELONA   (Spain)

Author keywords

Adult neurogenesis; Cytokines; Neural stem cell; Neuronal differentiation

Indexed keywords

INTERLEUKIN 10; NESTIN; TRANSCRIPTION FACTOR SOX1; TRANSCRIPTION FACTOR SOX2;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; GENE EXPRESSION; IN VIVO STUDY; MARKER GENE; MOUSE; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NEUROBLAST; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; SUBVENTRICULAR ZONE; UPREGULATION;

ADULT NEUROGENESIS; CYTOKINES; NEURAL STEM CELL; NEURONAL DIFFERENTIATION;

ANIMALS; BRAIN; CELL DIFFERENTIATION; GENE EXPRESSION; HUMANS; INTERLEUKIN-10; MICE; NESTIN; NEURAL STEM CELLS; NEUROGENESIS; RATS; SIGNAL TRANSDUCTION;

EID: 84885460123     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.127803     Document Type: Article

References (67)

1. Abrieu, A., Fisher, D., Simon, M. N., Dorée, M. and Picard, A. (1997). MAPK inactivation is required for the G2 to M-phase transition of the first mitotic cell cycle. EMBO J. 16, 6407-6413.
2. Aguirre, A., Rubio, M. E. and Gallo, V. (2010). Notch and EGFR pathway interaction regulates neural stem cell number and self-renewal. Nature 467, 323-327.
3. Andreu-Agulló, C., Morante-Redolat, J. M., Delgado, A. C. and Fariñas, I. (2009). Vascular niche factor PEDF modulates Notch-dependent stemness in the adult subependymal zone. Nat. Neurosci. 12, 1514-1523.
4. Androutsellis-Theotokis, A., Leker, R. R., Soldner, F., Hoeppner, D. J., Ravin, R., Poser, S. W., Rueger, M. A., Bae, S. K., Kittappa, R. and McKay, R. D. (2006). Notch signalling regulates stem cell numbers in vitro and in vivo. Nature 442, 823-826.
5. Arvidsson, A., Collin, T., Kirik, D., Kokaia, Z. and Lindvall, O. (2002). Neuronal replacement from endogenous precursors in the adult brain after stroke. Nat. Med. 8, 963-970.
6. Baron, R., Nemirovsky, A., Harpaz, I., Cohen, H., Owens, T. and Monsonego, A. (2008). IFN-gamma enhances neurogenesis in wild-type mice and in a mouse model of Alzheimer's disease. FASEB J. 22, 2843-2852.
7. Brill, M. S., Ninkovic, J., Winpenny, E., Hodge, R. D., Ozen, I., Yang, R., Lepier, A., Gascón, S., Erdelyi, F., Szabo, G. et al. (2009). Adult generation of glutamatergic olfactory bulb interneurons. Nat. Neurosci. 12, 1524-1533.
8. Doetsch, F. and Alvarez-Buylla, A. (1996). Network of tangential pathways for neuronal migration in adult mammalian brain. Proc. Natl. Acad. Sci. USA 93, 14895-14900.
9. Doetsch, F., García-Verdugo, J. M. and Alvarez-Buylla, A. (1997). Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain. J. Neurosci. 17, 5046-5061.
10. Doetsch, F., García-Verdugo, J. M. and Alvarez-Buylla, A. (1999). Regeneration of a germinal layer in the adult mammalian brain. Proc. Natl. Acad. Sci. USA 96, 11619-11624.
11. Ekdahl, C. T., Claasen, J. H., Bonde, S., Kokaia, Z. and Lindvall, O. (2003). Inflammation is detrimental for neurogenesis in adult brain. Proc. Natl. Acad. Sci. USA 100, 13632-13637.
12. Fernando, R. N., Eleuteri, B., Abdelhady, S., Nussenzweig, A., Andäng, M. and Ernfors, P. (2011). Cell cycle restriction by histone H2AX limits proliferation of adult neural stem cells. Proc. Natl. Acad. Sci. USA 108, 5837-5842.
13. Ferron, S. R., Andreu-Agullo, C., Mira, H., Sanchez, P., Marques-Torrejon, M. A. and Farinas, I. (2007). A combined ex/in vivo assay to detect effects of exogenously added factors in neural stem cells. Nat. Protoc. 2, 849-859.
14. Geraerts, M., Eggermont, K., Hernandez-Acosta, P., Garcia-Verdugo, J. M., Baekelandt, V. and Debyser, Z. (2006). Lentiviral vectors mediate efficient and stable gene transfer in adult neural stem cells in vivo. Hum. Gene Ther. 17, 635-650.
15. Gómez-Nicola, D., Valle-Argos, B., Pallas-Bazarra, N. and Nieto-Sampedro, M. (2011). Interleukin-15 regulates proliferation and self-renewal of adult neural stem cells. Mol. Biol. Cell 22, 1960-1970.
16. Gonzalez, P., Burgaya, F., Acarin, L., Peluffo, H., Castellano, B. and Gonzalez, B. (2009). Interleukin-10 and interleukin-10 receptor-I are upregulated in glial cells after an excitotoxic injury to the postnatal rat brain. J. Neuropathol. Exp. Neurol. 68, 391-403.
17. Gonzalez-Perez, O., Romero-Rodriguez, R., Soriano-Navarro, M., Garcia-Verdugo, J. M. and Alvarez-Buylla, A. (2009). Epidermal growth factor induces the progeny of subventricular zone type B cells to migrate and differentiate into oligodendrocytes. Stem Cells 27, 2032-2043.
18. Gritti, A., Dal Molin, M., Foroni, C. and Bonfanti, L. (2009). Effects of developmental age, brain region, and time in culture on long-term proliferation and multipotency of neural stem cell populations. J. Comp. Neurol. 517, 333-349.
19. Guillemot, F. (2007). Spatial and temporal specification of neural fates by transcription factor codes. Development 134, 3771-3780.
20. Ihrie, R. A., Shah, J. K., Harwell, C. C., Levine, J. H., Guinto, C. D., Lezameta, M., Kriegstein, A. R. and Alvarez-Buylla, A. (2011). Persistent sonic hedgehog signaling in adult brain determines neural stem cell positional identity. Neuron 71, 250-262.
21. Imai, T., Tokunaga, A., Yoshida, T., Hashimoto, M., Mikoshiba, K., Weinmaster, G., Nakafuku, M. and Okano, H. (2001). The neural RNA-binding protein Musashi1 translationally regulates mammalian numb gene expression by interacting with its mRNA. Mol. Cell. Biol. 21, 3888-3900.
22. Iosif, R. E., Ekdahl, C. T., Ahlenius, H., Pronk, C. J., Bonde, S., Kokaia, Z., Jacobsen, S. E. and Lindvall, O. (2006). Tumor necrosis factor receptor 1 is a negative regulator of progenitor proliferation in adult hippocampal neurogenesis. J. Neurosci. 26, 9703-9712.
23. Jin, K., Galvan, V., Xie, L., Mao, X. O., Gorostiza, O. F., Bredesen, D. E. and Greenberg, D. A. (2004). Enhanced neurogenesis in Alzheimer's disease transgenic (PDGF-APPSw,Ind) mice. Proc. Natl. Acad. Sci. USA 101, 13363-13367.
24. Kakita, A. and Goldman, J. E. (1999). Patterns and dynamics of SVZ cell migration in the postnatal forebrain: monitoring living progenitors in slice preparations. Neuron 23, 461-472.
25. Kelsch, W., Mosley, C. P., Lin, C. W. and Lois, C. (2007). Distinct mammalian precursors are committed to generate neurons with defined dendritic projection patterns. PLoS Biol. 5, e300.
26. Khodosevich, K., Watanabe, Y. and Monyer, H. (2011). EphA4 preserves postnatal and adult neural stem cells in an undifferentiated state in vivo. J. Cell Sci. 124, 1268-1279.
27. Kiyota, T., Ingraham, K. L., Swan, R. J., Jacobsen, M. T., Andrews, S. J. and Ikezu, T. (2012). AAV serotype 2/1-mediated gene delivery of anti-inflammatory interleukin-10 enhances neurogenesis and cognitive function in APP+PS1 mice. Gene Ther. 19, 724-733.
28. Kohwi, M., Petryniak, M. A., Long, J. E., Ekker, M., Obata, K., Yanagawa, Y., Rubenstein, J. L. and Alvarez-Buylla, A. (2007). A subpopulation of olfactory bulb GABAergic interneurons is derived from Emx1-and Dlx5/6-expressing progenitors. J. Neurosci. 27, 6878-6891.
29. Kokaia, Z., Thored, P., Arvidsson, A. and Lindvall, O. (2006). Regulation of strokeinduced neurogenesis in adult brain-recent scientific progress. Cereb. Cortex 16 Suppl. 1, i162-i167.
30. Koo, J. W. and Duman, R. S. (2008). IL-1beta is an essential mediator of the antineurogenic and anhedonic effects of stress. Proc. Natl. Acad. Sci. USA 105, 751-756.
31. Kühn, R., Löhler, J., Rennick, D., Rajewsky, K. and Müller, W. (1993). Interleukin-10-deficient mice develop chronic enterocolitis. Cell 75, 263-274.
32. Kuo, C. T., Mirzadeh, Z., Soriano-Navarro, M., Rasin, M., Wang, D., Shen, J., Sestan, N., Garcia-Verdugo, J., Alvarez-Buylla, A., Jan, L. Y. et al. (2006). Postnatal deletion of Numb/Numblike reveals repair and remodeling capacity in the subventricular neurogenic niche. Cell 127, 1253-1264.
33. Kyritsis, N., Kizil, C., Zocher, S., Kroehne, V., Kaslin, J., Freudenreich, D., Iltzsche, A. and Brand, M. (2012). Acute inflammation initiates the regenerative response in the adult zebrafish brain. Science 338, 1353-1356.
34. Lacki, J. K., Klama, K., Mackiewicz, S. H., Mackiewicz, U. and Müller, W. (1995). Circulating interleukin 10 and interleukin-6 serum levels in rheumatoid arthritis patients treated with methotrexate or gold salts: preliminary report. Inflamm. Res. 44, 24-26.
35. Levy, D. E. and Darnell, J. E., Jr (2002). Stats: transcriptional control and biological impact. Nat. Rev. Mol. Cell Biol. 3, 651-662.
36. Li, H. S., Wang, D., Shen, Q., Schonemann, M. D., Gorski, J. A., Jones, K. R., Temple, S., Jan, L. Y. and Jan, Y. N. (2003). Inactivation of Numb and Numblike in embryonic dorsal forebrain impairs neurogenesis and disrupts cortical morphogenesis. Neuron 40, 1105-1118.
37. Li, L., Walker, T. L., Zhang, Y., Mackay, E. W. and Bartlett, P. F. (2010). Endogenous interferon gamma directly regulates neural precursors in the noninflammatory brain. J. Neurosci. 30, 9038-9050.
38. Lim, D. A., Huang, Y. C., Swigut, T., Mirick, A. L., Garcia-Verdugo, J. M., Wysocka, J., Ernst, P. and Alvarez-Buylla, A. (2009). Chromatin remodelling factor Mll1 is essential for neurogenesis from postnatal neural stem cells. Nature 458, 529-533.
39. Lois, C. and Alvarez-Buylla, A. (1994). Long-distance neuronal migration in the adult mammalian brain. Science 264, 1145-1148.
40. Marqués-Torrejón M. A. Porlan, E., Banito, A., Gómez-Ibarlucea, E., Lopez-Contreras, A. J., Fernández-Capetillo, O., Vidal, A., Gil, J., Torres, J. and Fariñas, I. (2013). Cyclin-dependent kinase inhibitor p21 controls adult neural stem cell expansion by regulating Sox2 gene expression. Cell Stem Cell 12, 88-100.
41. Marshall, C. A., Novitch, B. G. and Goldman, J. E. (2005). Olig2 directs astrocyte and oligodendrocyte formation in postnatal subventricular zone cells. J. Neurosci. 25, 7289-7298.
42. 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.
43. Merkle, F. T., Tramontin, A. D., García-Verdugo, J. M. and Alvarez-Buylla, A. (2004). Radial glia give rise to adult neural stem cells in the subventricular zone. Proc. Natl. Acad. Sci. USA 101, 17528-17532.
44. Merkle, F. T., Mirzadeh, Z. and Alvarez-Buylla, A. (2007). Mosaic organization of neural stem cells in the adult brain. Science 317, 381-384.
45. Mirzadeh, Z., Merkle, F. T., Soriano-Navarro, M., Garcia-Verdugo, J. M. and Alvarez-Buylla, A. (2008). Neural stem cells confer unique pinwheel architecture to the ventricular surface in neurogenic regions of the adult brain. Cell Stem Cell 3, 265-278.
46. Mobley, A. K., Tchaicha, J. H., Shin, J., Hossain, M. G. and McCarty, J. H. (2009). Beta8 integrin regulates neurogenesis and neurovascular homeostasis in the adult brain. J. Cell Sci. 122, 1842-1851.
47. Monje, M. L., Toda, H. and Palmer, T. D. (2003). Inflammatory blockade restores adult hippocampal neurogenesis. Science 302, 1760-1765.
48. Nam, S. C., Kim, Y., Dryanovski, D., Walker, A., Goings, G., Woolfrey, K., Kang, S. S., Chu, C., Chenn, A., Erdelyi, F. et al. (2007). Dynamic features of postnatal subventricular zone cell motility: a two-photon time-lapse study. J. Comp. Neurol. 505, 190-208.
49. Nishimoto, Y. and Okano, H. (2010). New insight into cancer therapeutics: induction of differentiation by regulating the Musashi/Numb/Notch pathway. Cell Res. 20, 1083-1085.
50. Ouyang, W., Rutz, S., Crellin, N. K., Valdez, P. A. and Hymowitz, S. G. (2011). Regulation and functions of the IL-10 family of cytokines in inflammation and disease. Annu. Rev. Immunol. 29, 71-109.
51. Parras, C. M., Galli, R., Britz, O., Soares, S., Galichet, C., Battiste, J., Johnson, J. E., Nakafuku, M., Vescovi, A. and Guillemot, F. (2004). Mash1 specifies neurons and oligodendrocytes in the postnatal brain. EMBO J. 23, 4495-4505.
52. Pastrana, E., Silva-Vargas, V. and Doetsch, F. (2011). Eyes wide open: a critical review of sphere-formation as an assay for stem cells. Cell Stem Cell 8, 486-498.
53. Pestka, S., Krause, C. D., Sarkar, D., Walter, M. R., Shi, Y. and Fisher, P. B. (2004). Interleukin-10 and related cytokines and receptors. Annu. Rev. Immunol. 22, 929-979.
54. Petersen, P. H., Zou, K., Krauss, S. and Zhong, W. (2004). Continuing role for mouse Numb and Numbl in maintaining progenitor cells during cortical neurogenesis. Nat. Neurosci. 7, 803-811.
55. Pozas, E. and Ibáñez, C. F. (2005). GDNF and GFRalpha1 promote differentiation and tangential migration of cortical GABAergic neurons. Neuron 45, 701-713.
56. Rabaneda, L. G., Carrasco, M., López-Toledano, M. A., Murillo-Carretero, M., Ruiz, F. A., Estrada, C. and Castro, C. (2008). Homocysteine inhibits proliferation of neuronal precursors in the mouse adult brain by impairing the basic fibroblast growth factor signaling cascade and reducing extracellular regulated kinase 1/2-dependent cyclin E expression. FASEB J. 22, 3823-3835.
57. Ramírez-Castillejo, C., Sánchez-Sánchez, F., Andreu-Agulló, C., Ferrón, S. R., Aroca-Aguilar, J. D., Sánchez, P., Mira, H., Escribano, J. and Fariñas, I. (2006). Pigment epithelium-derived factor is a niche signal for neural stem cell renewal. Nat. Neurosci. 9, 331-339.
58. Romero-Grimaldi, C., Murillo-Carretero, M., López-Toledano, M. A., Carrasco, M., Castro, C. and Estrada, C. (2011). ADAM-17/tumor necrosis factor-aconverting enzyme inhibits neurogenesis and promotes gliogenesis from neural stem cells. Stem Cells 29, 1628-1639.
59. Saraiva, M. and O'Garra, A. (2010). The regulation of IL-10 production by immune cells. Nat. Rev. Immunol. 10, 170-181.
60. Sawamoto, K., Wichterle, H., Gonzalez-Perez, O., Cholfin, J. A., Yamada, M., Spassky, N., Murcia, N. S., Garcia-Verdugo, J. M., Marin, O., Rubenstein, J. L. et al. (2006). New neurons follow the flow of cerebrospinal fluid in the adult brain. Science 311, 629-632.
61. Suh, H., Deng, W. and Gage, F. H. (2009). Signaling in adult neurogenesis. Annu. Rev. Cell Dev. Biol. 25, 253-275.
62. Teixeira, C. M., Kron, M. M., Masachs, N., Zhang, H., Lagace, D. C., Martinez, A., Reillo, I., Duan, X., Bosch, C., Pujadas, L. et al. (2012). Cell-autonomous inactivation of the reelin pathway impairs adult neurogenesis in the hippocampus. J. Neurosci. 32, 12051-12065.
63. Vila, N., Castillo, J., Dávalos, A., Esteve, A., Planas, A. M. and Chamorro, A. (2003). Levels of anti-inflammatory cytokines and neurological worsening in acute ischemic stroke. Stroke 34, 671-675.
64. Villeda, S. A., Luo, J., Mosher, K. I., Zou, B., Britschgi, M., Bieri, G., Stan, T. M., Fainberg, N., Ding, Z., Eggel, A. et al. (2011). The ageing systemic milieu negatively regulates neurogenesis and cognitive function. Nature 477, 90-94.
65. Wachs, F. P., Winner, B., Couillard-Despres, S., Schiller, T., Aigner, R., Winkler, J., Bogdahn, U. and Aigner, L. (2006). Transforming growth factorbeta1 is a negative modulator of adult neurogenesis. J. Neuropathol. Exp. Neurol. 65, 358-370.
66. Yang, J., Jiang, Z., Fitzgerald, D. C., Ma, C., Yu, S., Li, H., Zhao, Z., Li, Y., Ciric, B., Curtis, M. et al. (2009). Adult neural stem cells expressing IL-10 confer potent immunomodulation and remyelination in experimental autoimmune encephalitis. J. Clin. Invest. 119, 3678-3691.
67. Young, K. M., Fogarty, M., Kessaris, N. and Richardson, W. D. (2007). Subventricular zone stem cells are heterogeneous with respect to their embryonic origins and neurogenic fates in the adult olfactory bulb. J. Neurosci. 27, 8286-8296.