Identification of a Chr 11 quantitative trait locus that modulates proliferation in the rostral migratory stream of the adult mouse brain

European Journal of Neuroscience

Volumn 32, Issue 4, 2010, Pages 523-537

  Poon, Anna ^a   Li, Zhiyou ^b   Wolfe, Gregory W ^c   Lu, Lu ^b   Williams, Robert W ^b   Hayes, Nancy L ^d   Nowakowski, Richard S ^e   Goldowitz, Daniel ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

^c University of Texas Medical Branch School of Medicine   (United States)

^d RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

^e FLORIDA STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

Bromodeoxyuridine; Cell cycle; Neural progenitors; Olfactory bulb neurogenesis; Recombinant inbred mice

Indexed keywords

ANIMAL CELL; ANIMAL TISSUE; ANTERIOR HYPOTHALAMUS; ARTICLE; CELL CYCLE PARAMETERS; CELL PROLIFERATION; CHROMOSOME 11; CHROMOSOME 3; CONTROLLED STUDY; DENTATE GYRUS; FEMALE; GENE MAPPING; GENETIC VARIABILITY; MALE; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; QUANTITATIVE TRAIT LOCUS; RECOMBINANT INBRED STRAIN;

ANIMALS; BRAIN; CELL CYCLE; CELL MOVEMENT; CELL PROLIFERATION; CHROMOSOME MAPPING; CHROMOSOMES, MAMMALIAN; MICE; MICE, INBRED C57BL; MICE, INBRED STRAINS; MOLECULAR SEQUENCE DATA; QUANTITATIVE TRAIT LOCI;

EID: 77955736595     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2010.07316.x     Document Type: Article

References (54)

1. Alonso, M., Viollet, C., Gabellec., M.M., Meas-Yedid, V., Olivo-Marin, J.C. Lledo, P.M. (2006) Olfactory discrimination learning increases the survival of adult-born neurons in the olfactory bulb. J. Neurosci., 26, 10508 10513.
2. Alvarez-Buylla, A. Garcia-Verdugo, J.M. (2002) Neurogenesis in adult subventricular zone. J. Neurosci., 22, 629 634.
3. Basak, O. Taylor, V. (2009) Stem cells of the adult mammalian brain and their niche. Cell. Mol. Life Sci., 66, 1057 1072.
4. Bock, N.A., Kovacevic, N., Lipina, T.V., Roder, J.C., Ackerman, S.L. Henkelman, R.M. (2006) In vivo magnetic resonance imaging and semiautomated image analysis extend the brain phenotype for cdf/cdf mice. J. Neurosci., 26, 4455 4459.
5. Braun, K., Hölzl, G., Soucek, T., Geisen, C., Möröy, T. Hengstschläger, M. (1998) Investigation of the cell cycle regulation of cdk3-associated kinase activity and the role of cdk3 in proliferation and transformation. Oncogene, 17, 2259 2269.
6. Bull, N.D. Bartlett, P.F. (2005) The adult mouse hippocampal progenitor is neurogenic but not a stem cell. J. Neurosci., 25, 10815 10821.
7. Churchill, G.A. Doerge, R.W. (1994) Empirical threshold values for quantitative trait mapping. Genetics, 138, 963 971.
8. Doetsch, F., García-Verdugo, J.M. 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.
9. Doetsch, F., Petreanu, L., Caille, I., Garcia-Verdugo, J.M. Alvarez-Buylla, A. (2002) EGF converts transit-amplifying neurogenic precursors in the adult brain into multipotent stem cells. Neuron, 36, 1021 1034.
10. Elder, G.A., De Gasperi, R. Gama Sosa, M.A. (2006) Research update: neurogenesis in adult brain and neuropsychiatric disorders. Mt Sinai J. Med., 73, 931 940.
11. Enwere, E., Shingo, T., Gregg, C., Fujikawa, H., Ohta, S. Weiss, S. (2004) Aging results in reduced epidermal growth factor receptor signaling, diminished olfactory neurogenesis, and deficits in fine olfactory discrimination. J. Neurosci., 24, 8354 8365.
12. Frinchi, M., Bonomo, A., Trovato-Salinaro, A., Condorelli, D.F., Fuxe, K., Spampinato, M.G. Mudò, G. (2008) Fibroblast growth factor-2 and its receptor expression in proliferating precursor cells of the subventricular zone in the adult rat brain. Neurosci. Lett., 447, 20 25.
13. Gheusi, G., Cremer, H., McLean, H., Chazal, G., Vincent, J.-D. Lledo, P.-M. (2000) Importance of newly generated neurons in the adult olfactory bulb for odor discrimination. Proc. Natl Acad. Sci. USA, 97, 1823 1828.
14. Gonzalez, M.E., Makarova, O., Peterson, E.A., Privette, L.M. Petty, E.M. (2009) Up-regulation of SEPT9-v1 stabilizes c-Jun-N-terminal kinase and contributes to its pro-proliferative activity in mammary epithelial cells. Cell. Signal., 21, 477 487.
15. Hait, N.C., Oskeritzian, C.A., Paugh, S.W., Milstien, S. Spiegel, S. (2006) Sphingosine kinases, sphingosine 1-phosphate, apoptosis and diseases. Biochim. Biophys. Acta, 1758, 2016 2026.
16. Harada, J., Foley, M., Moskowitz, M.A. Waeber, C. (2004) Sphingosine-1-phosphate induces proliferation and morphological changes of neural progenitor cells. J. Neurochem., 88, 1026 1039.
17. Hayes, N.L. Nowakowski, R.S. (2002) Dynamics of cell proliferation in the adult dentate gyrus of two inbred strains of mice. Brain Res. Dev. Brain Res., 134, 77 85.
18. Imayoshi, I., Sakamoto, M., Ohtsuka, T., Takao, K., Miyakawa, T., Yamaguchi, M., Mori, K., Ikeda, T., Itohara, S. Kageyama, R. (2008) Roles of continuous neurogenesis in the structural and functional integrity of the adult forebrain. Nat. Neurosci., 11, 1153 1161.
19. Kempermann, G. Gage, F.H. (2002) Genetic influence on phenotypic differentiation in adult hippocampal neurogenesis. Brain Res. Dev. Brain Res., 134, 1 12.
20. Kempermann, G., Gast, D., Kronenberg, G., Yamaguchi, M. Gage, F.H. (2003) Early determination and long-term persistence of adult-generated new neurons in the hippocampus of mice. Development, 130, 391 399.
21. Kempermann, G., Chesler, E.J., Lu, L., Williams, R.W. Gage, F.H. (2006) Natural variation and genetic covariance in adult hippocampal neurogenesis. Proc. Natl Acad. Sci. USA, 103, 780 785.
22. Knott, S.A., Nystrom, P.E., Andersson-Eklund, L., Stern, S., Marklund, L., Andersson, L. Haley, C.S. (2002) Approaches to interval mapping of QTL in multigeneration pedigree: the example of porcine chromosome 4. Anim. Genet., 33, 26 32.
23. Kohama, T., Olivera, A., Edsall, L., Nagiec, M.M., Dickson, R. Spiegel, S. (1998) Molecular cloning and functional characterization of murine sphingosine kinase. J. Biol. Chem., 273, 23722 23728.
24. Lander, E.S. Botstein, D. (1989) Mapping mendelian factors underlying quantitative traits using RFLP linkage maps. Genetics, 121, 185 199.
25. Lauter, N. Doebley, J. (2002) Genetic variation for phenotypically invariant traits detected in teosinte: implications for the evolution of novel forms. Genetics, 160, 333 342.
26. Lee, A.W., Emsley, J.G., Brown, R.E. Hagg, T. (2003) Marked differences in olfactory sensitivity and apparent speed of forebrain neuroblast migration in three inbred strains of mice. Neuroscience, 118, 263 270.
27. Lim, D.A., Tramontin, A.D., Trevejo, J.M., Herrera, D.G., Garcia-Verdugo, J.M. Alvarez-Buylla, A. (2000) Noggin antagonizes BMP signalling to create a niche for adult neurogenesis. Neuron, 28, 713 726.
28. Liu, H.K., Belz, T., Bock, D., Takacs, A., Wu, H., Lichter, P., Chai, M. Schütz, G. (2008) The nuclear receptor tailless is required for neurogenesis in the adult subventricular zone. Genes Dev., 22, 2473 2478.
29. Lledo, P.M., Merkle, F.T. Alvarez-Buylla, A. (2008) Origin and function of olfactory bulb interneuron diversity. Trends Neurosci., 31, 392 400.
30. Lois, C. Alvarez-Buylla, A. (1994) Long-distance neuronal migration in the adult mammalian brain. Science, 264, 1145 1148.
31. Lu, X., Sharkey, L. Bartfai, T. (2007) The brain galanin receptors: targets for novel antidepressant drugs. CNS Neurol. Disord. Drug Targets, 6, 183 192.
32. Lu, L., Wei, L., Peirce, J.L., Wang, X., Zhou, J., Homayouni, R., Williams, R.W. Airey, D.C. (2008) Using gene expression databases for classical trait QTL candidate gene discovery in the BXD recombinant inbred genetic reference population: mouse forebrain weight. BMC Genomics, 9, 444.
33. Ma, J., Shan, L., Yu, L.L. Yuan, C.G. (2008) Expression of galanin and galanin receptors in neurogenesis regions of adult mouse brain and effect of galanin on the neural stem cell's differentiation. Fen Zi Xi Bao Sheng Wu Xue Bao, 41, 359 366.
34. Mandairon, N., Sacquet, J., Garcia, S., Ravel, N., Jourdan, F. Didier, A. (2006) Neurogenic correlates of an olfactory discrimination task in the adult olfactory bulb. Eur. J. Neurosci., 24, 3578 3588. (Pubitemid 44952623)
35. Manichaikul, A., Dupuis, J., Sen, S. Broman, K.W. (2006) Poor performance of bootstrap confidence intervals for the location of a quantitative trait locus. Genetics, 174, 481 489.
36. Maysami, S., Lan, J.Q., Minami, M. Simon, R.P. (2008) Proliferating progenitor cells: a required cellular element for induction of ischemic tolerance in the brain. J. Cereb. Blood Flow Metab., 28, 1104 1113.
37. Mazarati, A., Lu, X., Kilk, K., Langel, U., Wasterlain, C. Bartfai, T. (2004) Galanin type 2 receptors regulate neuronal survival, susceptibility to seizures and seizure-induced neurogenesis in the dentate gyrus. Eur. J. Neurosci., 19, 3235 3244.
38. Merkle, F.T., Mirzadeh, Z. Alvarez-Buylla, A. (2007) Mosaic organization of neural stem cells in the adult brain. Science, 317, 381 384.
39. Merson, T.D., Dixon, M.P., Collin, C., Rietze, R.L., Bartlett, P.F., Thomas, T. Voss, A.K. (2006) The transcriptional coactivator Querkopf controls adult neurogenesis. J. Neurosci., 26, 11359 11370.
40. Mizugishi, K., Yamashita, T., Olivera, A., Miller, G.F., Spiegel, S. Proia, R.L. (2005) Essential role for sphingosine kinases in neural and vascular development. Mol. Cell. Biol., 25, 11113 11121.
41. Mudò, G., Bonomo, A., Di Liberto, V., Frinchi, M., Fuxe, K. Belluardo, N. (2009) The FGF-2/FGFRs neurotrophic system promotes neurogenesis in the adult brain. J. Neural Transm., 116, 995 1005.
42. Nowakowski, R.S., Lewin, S.B. Miller, M.W. (1989) Bromodeoxyuridine immunohistochemical determination of the lengths of the cell cycle and the DNA-synthetic phase for an anatomically defined population. J. Neurocytol., 18, 311 318.
43. Ramirez-Castillejo, C., Sanchez-Sanchez, F., Andreu-Agullo, C., Ferron, S.R., Aroca-Aguilar, J.D., Sanchez, P., Mira, H., Escribano, J. Farinas, I. (2006) Pigment epithelium-derived factor is a niche signal for neural stem cell renewal. Nat. Neurosci., 9, 331 339.
44. Rochefort, C., Gheusi, G., Vincent, J.-D. Lledo, P.-M. (2002) Enriched odor exposure increases the number of newborn neurons in the adult olfactory bulb and improves odor memory. J. Neurosci., 22, 2679 2689.
45. Rosen, G.D., Pung, C.J., Owens, C.B., Caplow, J., Kim, H., Mozhui, K., Lu, L. Williams, R.W. (2009) Genetic modulation of striatal volume by loci on Chrs 6 and 17 in BXD recombinant inbred mice. Genes Brain Behav., 8, 296 308.
46. Seaberg, R.M. van der Kooy, D. (2002) Adult rodent neurogenic regions: the ventricular subependyma contains neural stem cells, but the dentate gyrus contains restricted progenitors. J. Neurosci., 22, 1784 1793.
47. Soria, J.M., Taglialatela, P., Gil-Perotin, S., Galli, R., Gritti, A., Verdugo, J.M. Bertuzzi, S. (2004) Defective postnatal neurogenesis and disorganization of the rostral migratory stream in absence of the Vax1 homeobox gene. J. Neurosci., 24, 11171 11181.
48. Takahashi, T., Nowakowski, R.S. Caviness, V.S. Jr. (1995) The cell cycle of the pseudostratified ventricular epithelium of the embryonic murine cerebral wall. J. Neurosci., 15, 6046 6057.
49. Tanapat, P., Hastings, N.B., Reeves, A.J. Gould, E. (1999) Estrogen stimulates a transient increase in the number of new neurons in the dentate gyrus of the adult female rat. J. Neurosci., 19, 5792 5801.
50. Wang, S., Hashemi, T., Fried, S., Clemmons, A.L. Hawes, B.E. (1998) Differential intracellular signaling of the GalR1 and GalR2 galanin receptor subtypes. Biochemistry, 37, 6711 6717. (Pubitemid 28228104)
51. Weller, J.I., Soller, M. Brody, T. (1998) Linkage Analysis of quantitative traits in an interspecific cross of tomato (Lycopersicon esculentum×Lycopersicon pimpinellifolium) by means of genetic markers. Genetics, 118, 329 339.
52. Williams, R.W., Airey, D.C., Kulkarni, A., Zhou, G. Lu, L. (2001) Genetic dissection of the olfactory bulbs of mice: QTLs on four chromosomes modulate bulb size. Behav. Genet., 31, 61 77.
53. Wittko, I.M., Schänzer, A., Kuzmichev, A., Schneider, F.T., Shibuya, M., Raab, S. Plate, K.H. (2009) VEGFR-1 regulates adult olfactory bulb neurogenesis and migration of neural progenitors in the rostral migratory stream in vivo. J. Neurosci., 29, 8704 8714.
54. Zhao, C., Deng, W. Gage, F.H. (2008) Mechanisms and functional implications of adult neurogenesis. Cell, 22, 645 660.