Loss of input from the mossy cells blocks maturation of newly generated granule cells

Hippocampus

Volumn 17, Issue 7, 2007, Pages 510-524

  Marqués Marí, Ana Isabel ^a   Nacher, Juan ^a   Crespo, Carlos ^a   Gutièrrez Mecinas, María ^a   Martínez Guijarro, Francisco José ^a   Blasco Ibáñez, José Miguel ^a  

^a UNIVERSITY OF VALENCIA   (Spain)

Author keywords

Calretinin; Epilepsy; Mossy fibers; Pilocarpine; Sprouting

Indexed keywords

BROXURIDINE; CALRETININ; PILOCARPINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL MATURATION; CELL SURVIVAL; CONTROLLED STUDY; EPILEPSY; EPILEPTOGENESIS; FEMALE; GRANULE CELL; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MOSSY FIBER; MOUSE; NERVE CELL DIFFERENTIATION; NERVE SPROUTING; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; ANTICONVULSANTS; BIOLOGICAL MARKERS; BROMODEOXYURIDINE; CALCIUM-BINDING PROTEIN, VITAMIN D-DEPENDENT; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; CONVULSANTS; DENTATE GYRUS; DIAZEPAM; EPILEPSY; FEMALE; IMMUNOHISTOCHEMISTRY; MICE; MOSSY FIBERS, HIPPOCAMPAL; MUSCARINIC ANTAGONISTS; NERVE DEGENERATION; NERVE TISSUE PROTEINS; NEURONAL PLASTICITY; NUCLEAR PROTEINS; PILOCARPINE; SCOPOLAMINE; STATUS EPILEPTICUS; STEM CELLS;

EID: 34447500604     PISSN: 10509631     EISSN: 10981063     Source Type: Journal    
DOI: 10.1002/hipo.20290     Document Type: Article

References (65)

1. Acsády L, Katona I, Martínez-Guijarro FJ, Buzsaki G, Freund TF. 2000. Unusual target selectivity of perisomatic inhibitory cells in the hilar region of the rat hippocampus. J Neurosci 20:6907-6919.
2. Arida RM, Scorza FA, Peres CA, Cavalheiro EA. 1999. The course of untreated seizures in the pilocarpine model of epilepsy. Epilepsy Res 34:99-107.
3. Blasco-Ibáñez JM, Freund TF. 1997. Distribution, ultrastructure, and connectivity of calretinin immunoreactive mossy cells of the mouse dentate gyrus. Hippocampus 7:307-320.
4. Blasco-Ibáñez JM, Martínez-Guijarro FJ, Freund TF. 2000. Recurrent mossy fibers preferentially innervate parvalbumin-immunoreactive interneurons in the granule cell layer of the rat dentate gyrus. Neuroreport 11:3219-3225.
5. Brandt MD, Jessberger S, Steiner B, Kronenberg G, Reuter K, Bick-Sander A, von der Behrens W, Kempermann G. 2003. Transient calretinin expression defines early postmitotic step of neuronal differentiation in adult hippocampal neurogenesis of mice. Mol Cell Neurosci 24:603-613.
6. Brown J, Cooper-Kuhn CM, Kempermann G, Van Praag H, Winkler J, Gage FH, Kuhn HG. 2003a. Enriched environment and physical activity stimulate hippocampal but not olfactory bulb neurogenesis. Eur J Neurosci 17:2042-2046.
7. Brown JP, Couillard-Despres S, Cooper-Kuhn CM, Winkler J, Aigner L, Kuhn HG. 2003b. Transient expression of doublecortin during adult neurogenesis. J Comp Neurol 467:1-10.
8. Buckmaster PS, Strowbridge BW, Schwartzkroin PA. 1993. A comparison of rat hippocampal mossy cells and CA3c pyramidal cells. J Neurophysiol 70:1281-1299.
9. Buckmaster PS, Zhang GF, Yamawaki R. 2002. Axon sprouting in a model of temporal lobe epilepsy creates a predominantly excitatory feedback circuit. J Neurosci 22:6650-6658.
10. Cameron HA, McKay RD. 2001. Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus. J Comp Neurol 435:406-417.
11. Cavalheiro EA, Santos NF, Priel MR. 1996. The pilocarpine model of epilepsy in mice. Epilepsia 37:1015-1019.
12. Christie BR, Cameron HA. 2006. Neurogenesis in the adult hippocampus. Hippocampus 16:199-207.
13. Ciaroni S, Cecchini T, Ferri P, Ambrogini P, Cuppini R, Riccio M, Lombardelli G, Papa S, Del Grande P. 2002. Impairment of neural precursor proliferation increases survival of cell progeny in the adult rat dentate gyrus. Mech Ageing Dev 123:1341-1352.
14. Covolan L, Ribeiro LT, Longo BM, Mello LE. 2000. Cell damage and neurogenesis in the dentate granule cell layer of adult rats after pilocarpine- or kainate-induced status epilepticus. Hippocampus 10:169-180.
15. Dash PK, Mach SA, Moore AN. 2001. Enhanced neurogenesis in the rodent hippocampus following traumatic brain injury. J Neurosci Res 63:313-319.
16. Dayer AG, Ford AA, Cleaver KM, Yassaee M, Cameron HA. 2003. Short-term and long-term survival of new neurons in the rat dentate gyrus. J Comp Neurol 460:563-572.
17. Domínguez MI, Blasco-Ibáñez JM, Crespo C, Marqués-Marí AI, Martínez-Guijarro FJ. 2003a. Calretinin/PSA-NCAM immunoreactive granule cells after hippocampal damage produced by kainic acid and DEDTC treatment in mouse. Brain Res 966:206-217.
18. Domínguez MI, Blasco-Ibáñez JM, Crespo C, Marqués-Marí AI, Martínez-Guijarro FJ. 2003b. Zinc chelation during non-lesioning overexcitation results in neuronal death in the mouse hippocampus. Neuroscience 116:791-806.
19. Domínguez MI, Blasco-Ibáñez JM, Crespo C, Nacher J, Marqués-Marí AI, Martínez-Guijarro FJ. 2006. Neural overexcitation and implication of NMDA and AMPA receptors in a mouse model of temporal lobe epilepsy implying zinc chelation. Epilepsia 47:887-899.
20. Franck JE, Pokorny J, Kunkel DD, Schwartzkroin PA. 1995. Physiologic and morphologic characteristics of granule cell circuitry in human epileptic hippocampus. Epilepsia 36:543-558.
21. Gould E, Beylin A, Tanapat P, Reeves A, Shors TJ. 1999. Learning enhances adult neurogenesis in the hippocampal formation. Nat Neurosci 2:260-265.
22. Gould E, Tanapat P, Rydel T, Hastings N. 2000. Regulation of hippocampal neurogenesis in adulthood. Biol Psychiatry 48:715-720.
23. Gould E, Vail N, Wagers M, Gross CG. 2001. Adult-generated hippocampal and neocortical neurons in macaques have a transient existence. Proc Natl Acad Sci USA 98:10910-10917.
24. Hayes NL, Nowakowski RS. 2002. Dynamics of cell proliferation in the adult dentate gyrus of two inbred strains of mice. Brain Res Dev Brain Res 134:77-85.
25. Jones SP, Rahimi O, O'Boyle MP, Diaz DL, Claiborne BJ. 2003. Maturation of granule cell dendrites after mossy fiber arrival in hippocampal field CA3. Hippocampus 13:413-427.
26. Kaplan MS, Bell DH. 1984. Mitotic neuroblasts in the 9-day-old and 11-month-old rodent hippocampus. J Neurosci 4:1429-1441.
27. Kee NJ, Preston E, Wojtowicz JM. 2001. Enhanced neurogenesis after transient global ischemia in the dentate gyrus of the rat. Exp Brain Res 136:313-320.
28. Kempermann G, Gage FH. 1999. Experience-dependent regulation of adult hippocampal neurogenesis: Effects of long-term stimulation and stimulus withdrawal. Hippocampus 9:321-332.
29. Kempermann G, Kuhn HG, Gage FH. 1997. Genetic influence on neurogenesis in the dentate gyrus of adult mice. Proc Natl Acad Sci USA 94:10409-10414.
30. Kempermann G, Kuhn HG, Gage FH. 1998. Experience-induced neurogenesis in the senescent dentate gyrus. J Neurosci 18:3206-3212.
31. Kempermann G, Gast D, Gage FH. 2002. Neuroplasticity in old age: Sustained fivefold induction of hippocampal neurogenesis by long-term environmental enrichment. Ann Neurol 52:135-143.
32. Kempermann G, Gast D, Kronenberg G, Yamaguchi M, Gage FH. 2003. Early determination and long-term persistence of adult-generated new neurons in the hippocampus of mice. Development 130:391-399.
33. Kempermann G, Jessberger S, Steiner B, Kronenberg G. 2004a. Milestones of neuronal development in the adult hippocampus. Trends Neurosci 27:447-452.
34. Kempermann G, Wiskott L, Gage FH. 2004b. Functional significance of adult neurogenesis. Curr Opin Neurobiol 14:186-191.
35. Kuhn HG, Dickinson-Anson H, Gage FH. 1996. Neurogenesis in the dentate gyrus of the adult rat: Age-related decrease of neuronal progenitor proliferation. J Neurosci 16:2027-2033.
36. Laurberg S, Zimmer J. 1981. Lesion-induced sprouting of hippocampal mossy fiber collaterals to the fascia dentata in developing and adult rats. J Comp Neurol 200:433-459.
37. Lemos T, Cavalheiro EA. 1996. Status epilepticus and the late development of spontaneous seizures in the pilocarpine model of epilepsy. Epilepsy Res Suppl 12:137-144.
38. Liu Y, Fujise N, Kosaka T. 1996. Distribution of calretinin immunoreactivity in the mouse dentate gyrus. I. General description Exp Brain Res 108:389-403.
39. Longo B, Covolan L, Chadi G, Mello LE. 2003. Sprouting of mossy fibers and the vacating of postsynaptic targets in the inner molecular layer of the dentate gyrus. Exp Neurol 181:57-67.
40. Magloczky Z, Acsady L, Freund TF. 1994. Principal cells are the postsynaptic targets of supramammillary afferents in the hippocampus of the rat. Hippocampus 4:322-334.
41. Mello LE, Cavalheiro EA, Tan AM, Pretorius JK, Babb TL, Finch DM. 1992. Granule cell dispersion in relation to mossy fiber sprouting, hippocampal cell loss, silent period and seizure frequency in the pilocarpine model of epilepsy. Epilepsy Res Suppl 9:51-59.
42. Mello LE, Cavalheiro EA, Tan AM, Kupfer WR, Pretorius JK, Babb TL, Finch DM. 1993. Circuit mechanisms of seizures in the pilocarpine model of chronic epilepsy: Cell loss and mossy fiber sprouting. Epilepsia 34:985-995.
43. Murakawa R, Kosaka T. 1999. Diversity of the calretinin immunoreactivity in the dentate gyrus of gerbils, hamsters, guinea pigs, and laboratory shrews. J Comp Neurol 411:413-430.
44. Nilsson M, Perfilieva E, Johansson U, Orwar O, Eriksson PS. 1999. Enriched environment increases neurogenesis in the adult rat dentate gyrus and improves spatial memory. J Neurobiol 39:569-578.
45. Olariu A, Cleaver KM, Shore LE, Brewer MD, Cameron HA. 2005. A natural form of learning can increase and decrease the survival of new neurons in the dentate gyrus. Hippocampus 15:750-762.
46. Overstreet-Wadiche LS, Bromberg DA, Bensen AL, Westbrook GL. 2006. Seizures accelerate functional integration of adult-generated granule cells. J Neurosci 26:4095-4103.
47. Parent JM, Yu TW, Leibowitz RT, Geschwind DH, Sloviter RS, Lowenstein DH. 1997. Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network reorganization in the adult rat hippocampus. J Neurosci 17:3727-3738.
48. Represa A, Tremblay E, Ben Ari Y. 1990. Sprouting of mossy fibers in the hippocampus of epileptic human and rat. Adv Exp Med Biol 268:419-424.
49. Represa A, Niquet J, Pollard H, Khrestchatisky M, Ben Ari Y. 1994. From seizures to neo-synaptogenesis: Intrinsic and extrinsic determinants of mossy fiber sprouting in the adult hippocampus. Hippocampus 4:270-274.
50. Scharfman HE, Kunkel DD, Schwartzkroin PA. 1990. Synaptic connections of dentate granule cells and hilar neurons: Results of paired intracellular recordings and intracellular horseradish peroxidase injections. Neuroscience 37:693-707.
51. Seki T. 2002. Expression patterns of immature neuronal markers PSA-NCAM, CRMP-4 and NeuroD in the hippocampus of young adult and aged rodents. J Neurosci Res 70:327-334.
52. Seki T, Arai Y. 1991. The persistent expression of a highly polysialylated NCAM in the dentate gyrus of the adult rat. Neurosci Res 12:501-513.
53. Seki T, Arai Y. 1993. Distribution and possible roles of the highly polysialylated neural cell adhesion molecule (NCAM-H) in the developing and adult central nervous system. Neurosci Res 17:265-290.
54. Seri B, García-Verdugo JM, McEwen BS, Álvarez-Buylla A. 2001. Astrocytes give rise to new neurons in the adult mammalian hippocampus. J Neurosci 21:7153-7160.
55. Seri B, Garcia-Verdugo JM, Collado-Morente L, McEwen BS, Alvarez-Buylla A. 2004. Cell types, lineage, and architecture of the germinal zone in the adult dentate gyrus. J Comp Neurol 478:359-378.
56. Shibley H, Smith BN. 2002. Pilocarpine-induced status epilepticus results in mossy fiber sprouting and spontaneous seizures in C57BL/6 and CD-1 mice. Epilepsy Res 49:109-120.
57. Steiner B, Kronenberg G, Jessberger S, Brandt MD, Reuter K, Kempermann G. 2004. Differential regulation of gliogenesis in the context of adult hippocampal neurogenesis in mice. Glia 46:41-52.
58. Sutula T, Cascino G, Cavazos J, Parada I, Ramírez L. 1989. Mossy fiber synaptic reorganization in the epileptic human temporal lobe. Ann Neurol 26:321-330.
59. Tamamaki N. 1999. Development of afferent fiber lamination in the infrapyramidal blade of the rat dentate gyrus. J Comp Neurol 411:257-266.
60. Tauck DL, Nadler JV. 1985. Evidence of functional mossy fiber sprouting in hippocampal formation of kainic acid-treated rats. J Neurosci 5:1016-1022.
61. van Praag H, Kempermann G, Gage FH. 1999. Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat Neurosci 2:266-270.
62. Witter MP, Amaral DG. 1991. Entorhinal cortex of the monkey: V. Projections to the dentate gyrus, hippocampus, and subicular complex. J Comp Neurol 307:437-459.
63. Yagita Y, Kitagawa K, Ohtsuki T, Takasawa ki, Miyata T, Okano H, Hori M, Matsumoto M. 2001. Neurogenesis by progenitor cells in the ischemic adult rat hippocampus. Stroke 32:1890-1896.
64. Zhao C, Teng EM, Summers RG Jr, Ming GL, Gage FH. 2006. Distinct morphological stages of dentate granule neuron maturation in the adult mouse hippocampus. J Neurosci 26:3-11.
65. Zhao S, Forster E, Chai X, Frotscher M. 2003. Different signals control laminar specificity of commissural and entorhinal fibers to the dentate gyrus. J Neurosci 23:7351-7357.