Variability of doublecortin-associated dendrite maturation in adult hippocampal neurogenesis is independent of the regulation of precursor cell proliferation

BMC Neuroscience

Volumn 7, Issue , 2006, Pages

  Plümpe, Tobias ^a   Ehninger, Dan ^a,c   Steiner, Barbara ^a,b   Klempin, Friederike ^a,b   Jessberger, Sebastian ^b,d   Brandt, Moritz ^a   Römer, Benedikt ^a,e   Rodriguez, Gerardo Ramirez ^a   Kronenberg, Golo ^a   Kempermann, Gerd ^a,b  

^a MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^c UCLA MEDICAL CENTER   (United States)

^d SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^e CENTRAL INSTITUTE OF MENTAL HEALTH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLECORTIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN NERVE CELL; CELL CYCLE PROGRESSION; CELL MATURATION; CELL POPULATION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; DENDRITE; DEVELOPMENTAL STAGE; FEMALE; HIPPOCAMPUS; INFORMATION PROCESSING; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NONHUMAN; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS;

AGE FACTORS; ANIMALS; ASTROCYTES; BEHAVIOR, ANIMAL; BLOTTING, WESTERN; BROMODEOXYURIDINE; CELL COUNT; CELL PROLIFERATION; CELL SURVIVAL; DENDRITES; FEMALE; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; IN SITU NICK-END LABELING; KAINIC ACID; MAZE LEARNING; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROTUBULE-ASSOCIATED PROTEINS; NEURONS; NEUROPEPTIDES; ORGANOGENESIS; PHYSICAL CONDITIONING, ANIMAL; SEIZURES;

EID: 33845235682     PISSN: 14712202     EISSN: 14712202     Source Type: Journal    
DOI: 10.1186/1471-2202-7-77     Document Type: Article

References (72)

1. Seri B, Garcia-Verdugo JM, Collado-Morente L, McEwen BS, Alvarez-Buylla A: Cell types, lineage, and architecture of the germinal zone in the adult dentate gyrus. J Comp Neurol 2004, 478(4):359.
2. Kempermann G, Jessberger S, Steiner B, Kronenberg G: Milestones of neuronal development in the adult hippocampus. Trends Neurosci 2004, 27(8):447-452.
3. Kempermann G, Gast D, Kronenberg G, Yamaguchi M, Gage FH: Early determination and long-term persistence of adult-generated new neurons in the hippocampus of mice. Development 2003, 130(2):391-399.
4. Seri B, Garcia-Verdugo JM, McEwen BS, Alvarez-Buylla A: Astrocytes give rise to new neurons in the adult mammalian hippocampus. J Neurosci 2001, 21(18):7153-7160.
5. Filippov V, Kronenberg G, Pivneva T, Reuter K, Steiner B, Wang LP, Yamaguchi M, Kettenmann H, Kempermann G: Subpopulation of nestin-expressing progenitor cells in the adult murine hippocampus shows electrophysiological and morphological characteristics of astrocytes. Mol Cell Neurosci 2003, 23(3):373-382.
6. Wang LP, Kempermann G, Kettenmann H: A subpopulation of precursor cells in the mouse dentate gyrus receives synaptic GABAergic input. Mol Cell Neurosci 2005, 29(2):181-189.
7. Tozuka Y, Fukuda S, Namba T, Seki T, Hisatsune T: GABAergic excitation promotes neuronal differentiation in adult hippocampal progenitor cells. Neuron 2005, 47(6):803-815.
8. Brandt MD, Jessberger S, Steiner B, Kronenberg G, Reuter K, Bick-Sander A, Von der Behrens W, Kempermann G: Transient calretinin-expression defines early postmitotic step of neuronal differentiation in adult hippocampal neurogenesis of mice. Mol Cell Neurosci 2003, 24:603-613.
9. Rao MS, Shetty AK: Efficacy of doublecortin as a marker to analyse the absolute number and dendritic growth of newly generated neurons in the adult dentate gyrus. Eur J Neurosci 2004, 19(2):234-246.
10. Couillard-Despres S, Winner B, Schaubeck S, Aigner R, Vroemen M, Weidner N, Bogdahn U, Winkler J, Kuhn HG, Aigner L: Doublecortin expression levels in adult brain reflect neurogenesis. Eur J Neurosci 2005, 21(1):1-14.
11. Nacher J, Crespo C, McEwen BS: Doublecortin expression in the adult rat telencephalon. Eur J Neurosci 2001, 14(4):629-644.
12. Steiner B, Klempin F, Wang L, Kott M, Kettenmann H, Kempermann G: Type-2 cells as link between glial and neuronal lineage in adult hippocampal neurogenesis. Glia 2006, 54(8):805-814.
13. Deuel TA, Liu JS, Corbo JC, Yoo SY, Rorke-Adams LB, Walsh CA: Genetic interactions between doublecortin and doublecortin-like kinase in neuronal migration and axon outgrowth. Neuron 2006, 49(1):41-53.
14. Francis F, Koulakoff A, Boucher D, Chafey P, Schaar B, Vinet MC, Friocourt G, McDonnell N, Reiner O, Kahn A, McConnell SK, Berwald-Netter Y, Denoulet P, Chelly J: Doublecortin is a developmentally regulated, microtubule-associated protein expressed in migrating and differentiating neurons. Neuron 1999, 23(2):247-256.
15. Gleeson JG, Lin PT, Flanagan LA, Walsh CA: Doublecortin is a microtubule-associated protein and is expressed widely by migrating neurons. Neuron 1999, 23(2):257-271.
16. Gleeson JG, Minnerath SR, Fox JW, Allen KM, Luo RF, Hong SE, Berg MJ, Kuzniecky R, Reitnauer PJ, Borgatti R, Mira AP, Guerrini R, Holmes GL, Rooney CM, Berkovic S, Scheffer I, Cooper EC, Ricci S, Cusmai R, Crawford TO, Leroy R, Andermann E, Wheless JW, Dobyns WB, Walsh CA, et al.: Characterization of mutations in the gene doublecortin in patients with double cortex syndrome. Ann Neurol 1999, 45(2):146-153.
17. Meyer G, Perez-Garcia CG, Gleeson JG: Selective expression of doublecortin and LIS1 in developing human cortex suggests unique modes of neuronal movement. Cereb Cortex 2002, 12(12):1225-1236.
18. Ribak CE, Korn MJ, Shan Z, Obenaus A: Dendritic growth cones and recurrent basal dendrites are typical features of newly generated dentate granule cells in the adult hippocampus. Brain Res 2004, 1000(1-2):195-199.
19. Steiner B, Kronenberg G, Jessberger S, Brandt MD, Reuter K, Kempermann G: Differential regulation of gliogenesis in the context of adult hippocampal neurogenesis in mice. Glia 2004, 46(1):41-52.
20. Brown JP, Couillard-Despres S, Cooper-Kuhn CM, Winkler J, Aigner L, Kuhn HG: Transient expression of doublecortin during adult neurogenesis. J Comp Neurol 2003, 467(1):1-10.
21. Konenberg G, Bick-Sander A, Bunk E, Wolf C, Ehninger D, Kempermann G: Physical exercise prevents age-related decline in precursor cell activity in the mouse dentate gyrus. Neurobiol Aging 2006, 27(10):1505-1513.
22. Kronenberg G, Reuter K, Steiner B, Brandt MD, Jessberger S, Yamaguchi M, Kempermann G: Subpopulations of proliferating cells of the adult hippocampus respond differently to physiologic neurogenic stimuli. J Comp Neurol 2003, 467(4):455-463.
23. Kempermann G, Chester EJ, Lu L, Williams RW, Gage FH: Natural variation and genetic covariance in adult hippocampal neurogenesis. Proc Natl Acad Sci U S A 2006, 103(3):780-785.
24. Jessberger S, Romer B, Babu H, Kempermann G: Seizures induce proliferation and dispersion of doublecortin-positive hippocampal progenitor cells. Exp Neurol 2005, 196(2):342-351.
25. van Praag H, Schinder AF, Christie BR, Toni N, Palmer TD, Gage FH: Functional neurogenesis in the adult hippocampus. Nature 2002, 415(6875):1030-1034.
26. Esposito MS, Piatti VC, Laplagne DA, Morgenstern NA, Ferrari CC, Pitossi FJ, Schinder AF: Neuronal differentiation in the adult hippocampus recapitulates embryonic development. J Neurosci 2005, 25(44):10074-10086.
27. Zhao C, Teng EM, Summers RG Jr., Ming GL, Gage FH: Distinct morphological stages of dentate granule neuron maturation in the adult mouse hippocampus. J Neurosci 2006, 26(1):3-11.
28. Jones SP, Rahimi O, O'Boyle MP, Diaz DL, Claiborne BJ: Maturation of granule cell dendrites after mossy fiber arrival in hippocampal field CA3. Hippocampus 2003, 13(3):413-427.
29. Rao M: Stern and precursor cells in the nervous system. J Neurotrauma 2004, 21(4):415-427.
30. Seki T: Hippocampal adult neurogenesis occurs in a microenvironment provided by PSA-NCAM-expressing immature neurons. J Neurosci Res 2002, 69(6):772-783.
31. Overstreet-Wadiche LS, Bensen AL, Westbrook GL: Delayed development of adult-generated granule cells in dentate gyrus. J Neurosci 2006, 26(8):2326-2334.
32. Overstreet-Wadiche LS, Westbrook GL: Functional maturation of adult-generated granule cells. Hippocampus 2006, 16(3):208-215.
33. Scholzen T, Gerdes J: The Ki-67 protein: from the known and the unknown. J Cell Physiol 2000, 182(3):311-322.
34. Nowakowski RS, Lewin SB, Miller MW: Bromodeoxyuridine immunohistochemical determination of the lengths of the cell cycle and the DNA-synthetic phase for an anatomically defined population. J Neurocytol 1989, 18(3):311-318.
35. Seki T, Arai Y: Temporal and spacial relationships between PSA-NCAM-expressing, newly generated granule cells, and radial glia-like cells in the adult dentate gyrus. J Comp Neurol 1999, 410(3):503-513.
36. Shapiro LA, Korn MJ, Shan Z, Ribak CE: GFAP-expressing radial glia-like cell bodies are involved in a one-to-one relationship with doublecortin-immunolabeled newborn neurons in the adult dentate gyrus. Brain Res 2005, 1040:81-91.
37. Nolte C, Matyash M, Pivneva T, Schipke CG, Ohlemeyer C, Hanisch UK, Kirchhoff F, Kettenmann H: GFAP promoter-controlled EGFP-expressing transgenic mice: a tool to visualize astrocytes and astrogliosis in living brain tissue. Glia 2001, 33(1):72-86.
38. Hastings NB, Gould E: Rapid extension of axons into the CA3 region by adult-generated granule cells. J Comp Neurol 1999, 413(1):146-154.
39. Van Praag H, Kempermann G, Gage FH: Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat Neurosci 1999, 2(3):266-270.
40. Bengzon J, Kokaia Z, Elmér E, Nanobashvili A, Kokaia M, Lindvall O: Apoptosis and proliferation of dentate gyrus neurons after single and intermittent limbic seizures. Proc Natl Acad Sci USA 1997, 94:10432-10437.
41. Parent JM, Yu TW, Leibowitz RT, Geschwind DH, Sloviter RS, Lowenstein DH: Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network reorganization in the adult rat hippocampus. J Neurosci 1997, 17:3727-3738.
42. Scharfman HE, Goodman JH, Sollas AL: Granule-like neurons at the hilar/ CA3 border after status epilepticus and their synchrony with area CA3 pyramidal cells: functional implications of seizure-induced neurogenesis. J Neurosci 2000, 20(16):6144-6158.
43. Huttmann K, Sadgrove M, Wallraff A, Hinterkeuser S, Kirchhoff F, Steinhauser C, Gray WP: Seizures preferentially stimulate proliferation of radial glia-like astrocytes in the adult dentate gyrus: functional and immunocytochemical analysis. Eur J Neurosci 2003, 18(10):2769-2778.
44. Ehninger D, Kempermann G: Paradoxical effects of learning the Morris water maze on adult hippocampal neurogenesis in mice may be explained by a combination of stress and physical activity. Genes Brain Behav 2006, 5(1):29-39.
45. Cameron HA, Gould E: Adult neurogenesis is regulated by adrenal steroids in the dentate gyrus. Neuroscience 1994, 61(2):203-209.
46. Gould E, Cameron HA, Daniels DC, Woolley CS, McEwen BS: Adrenal hormones suppress cell division in the adult rat dentate gyrus. J Neurosci 1992, 12(9):3642-3650.
47. Gould E, McEwen BS, Tanapat P, Galea LAM, Fuchs E: Neurogenesis in the dentate gyrus of the adult tree shrew is regulated by psychosocial stress and NMDA receptor activation. J Neurosci 1997, 17:2492-2498.
48. Heine VM, Maslam S, Zareno J, Joels M, Lucassen PJ: Suppressed proliferation and apoptotic changes in the rat dentate gyrus after acute and chronic stress are reversible. Eur J Neurosci 2004, 19(1):131-144.
49. Pham K, Nacher J, Hof PR, McEwen BS: Repeated restraint stress suppresses neurogenesis and induces biphasic PSA-NCAM expression in the adult rat dentate gyrus. Eur J Neurosci 2003, 17(4):879-886.
50. Dobrossy MD, Drapeau E, Aurousseau C, Le Moal M, Piazza PV, Abrous DN: Differential effects of learning on neurogenesis: learning increases or decreases the number of newly born cells depending on their birth date. Mol Psychiatry 2003, 8(12):974-982.
51. Gould E, Beylin A, Tanapat P, Reeves A, Shors TJ: Learning enhances adult neurogenesis in the hippoampal formation. Nat Neurosci 1999, 2:260-265.
52. Hairston IS, Little MT, Scanlon MD, Barakat MT, Palmer TD, Sapolsky RM, Heller HC: Sleep restriction suppresses neurogenesis induced by hippocampus-dependent learning. J Neurophysiol 2005, 94(6):4224-4233.
53. Schmidt-Hieber C, Jonas P, Bischofberger J: Enhanced synaptic plasticity in newly generated granule cells of the adult hippocampus. Nature 2004, 429(6988):184-187.
54. Wang S, Scott BW, Wojtowicz JM: Heterogenous properties of dentate granule neurons in the adult rat. J Neurobiol 2000, 42(2):248-257.
55. Snyder JS, Kee N, Wojtowicz JM: Effects of adult neurogenesis on synaptic plasticity in the rat dentate gyrus. J Neurophysiol 2001, 85(6):2423-2431.
56. Ambrogini P, Lattanzi D, Ciuffoli S, Agostini D, Bertini L, Stocchi V, Santi S, Cuppini R: Morpho-functional characterization of neuronal cells at different stages of maturation in granule cell layer of adult rat dentate gyrus. Brain Res 2004, 1017(1-2):21-31.
57. Ge S, Goh EL, Sailor KA, Kitabatake Y, Ming GL, Song H: GABA regulates synaptic integration of newly generated neurons in the adult brain. Nature 2006, 439(7076):589-593.
58. Snyder JS, Hong NS, McDonald RJ, Wojtowicz JM: A role for adult neurogenesis in spatial long-term memory. Neuroscience 2005, 130(4):843-852.
59. Leuner B, Mendolia-Loffredo S, Kozorovitskiy Y, Samburg D, Gould E, Shors TJ: Learning enhances the survival of new neurons beyond the time when the hippocampus is required for memory. J Neurosci 2004, 24(34):7477-7481.
60. Kempermann G: Why new neurons? Possible functions for adult hippocampal neurogenesis. J Neurosci 2002, 22(3):635-638.
61. Song H, Kempermann G, Wadiche LO, Zhao C, Schinder AF, Bischofberger J: New neurons in the adult mammalian brain: synaptogenesis and functional integration. J Neurosci 2005, 25(45):10366-10368.
62. Jessberger S, Kempermann G: Adult-born hippocampal neurons mature into activity-dependent responsiveness. Eur J Neurosci 2003, 18(10):2707-2712.
63. Gould E: The effects of adrenal steroids and excitatory input on neuronal birth and survival. Ann N Y Acad Sci 1994, 743:73-92; discussion 92-3.
64. Cameron HA, McEwen BS, Gould E: Regulation of adult neurogenesis by excitatory input and NMDA receptor activation in the dentate gyrus. J Neurosci 1995, 15(6):4687-4692.
65. Bernabeu R, Sharp FR: NMDA and AMPA/kainate glutamate receptors modulate dentate neurogenesis and CA3 synapsin-I in normal and ischemic hippocampus. J Cereb Blood Flow Metab 2000, 20(12):1669-1680.
66. Deisseroth K, Singla S, Toda H, Monje M, Palmer TD, Malenka RC: Excitation-neurogenesis coupling in adult neural stem/progenitor cells. Neuron 2004, 42(4):535-552.
67. Ribak CE, Tran PH, Spigelman I, Okazaki MM, Nadler JV: Status epilepticus-induced hilar basal dendrites on rodent granule cells contribute to recurrent excitatory circuitry. J Comp Neurol 2000, 428(2):240-253.
68. Tanaka T, Serneo, FF, Higgins C, Gambello MJ, Wynshaw-Boris A, Gleeson JG: Lis1 and doublecortin function with dynein to mediate coupling of the nucleus to the centrosome in neuronal migration. J Cell Biol 2004, 165(5):709-721.
69. Yamaguchi M, Saito H, Suzuki M, Mori K: Visualization of neurogenesis in the central nervous system using nestin promoter-GFP transgenic mice. Neuroreport 2000, 11(9):1991-1996.
70. Wolfer DP, Stagljar-Bozicevic M, Errington ML, Lipp HP: Spatial Memory and Learning in Transgenic Mice: Fact or Artifact? News Physiol Sci 1998, 13:118-123.
71. Laemmli UK: Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227(5259):680-685.
72. Gavrieli Y, Sherman Y, Ben-Sasson SA: Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J Cell Biol 1992, 119(3):493-501.