Carboxypeptidase E knockout mice exhibit abnormal dendritic arborization and spine morphology in central nervous system neurons

Journal of Neuroscience Research

Volumn 88, Issue 1, 2010, Pages 64-72

  Woronowicz, Alicja ^a   Cawley, Niamh X ^a   Chang, Su Youne ^a   Koshimizu, Hisatsugu ^a   Phillips, Andrè W ^a   Xiong, Zhi Gang ^b   Loh, Y Peng ^a  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^b LEGACY RESEARCH   (United States)

Author keywords

BDNF; Carboxypeptidase E; Dendritic pruning; Hippocampus

Indexed keywords

CARBOXYPEPTIDASE H;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CELL; BRAIN CORTEX; BRAIN FUNCTION; BRANCHING MORPHOGENESIS; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; DENDRITIC CELL; HIPPOCAMPUS; KNOCKOUT MOUSE; MOUSE; NEUROLOGIC DISEASE; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; SPINE; WILD TYPE;

ANIMALS; CA1 REGION, HIPPOCAMPAL; CARBOXYPEPTIDASE H; CELL SHAPE; CEREBRAL CORTEX; DENDRITES; MICE; MICE, KNOCKOUT; SILVER STAINING;

EID: 73949104135     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.22174     Document Type: Article

References (57)

1. Bourne JN, Harris KM. 2008. Balancing structure and function at hippocampal dendritic spines. Annu Rev Neurosci 31:47-67.
2. Cawley NX, Zhou J, Hill JM, Abebe D, Romboz S, Yanik T, Rodriguiz RM, Wetsel WC. 2004. The carboxypeptidase E knockout mouse exhibits endocrinological and behavioral deficits. Endocrinology 145:5807-5819.
3. Chen Y, Wang PY, Ghosh A. 2005. Regulation of cortical dendrite development by Rap1 signaling. Mol Cell Neurosci 28:215-228.
4. Cobos I, Calcagnotto ME, Vilaythong AJ, Thwin MT, Noebels JL, Baraban SC, Rubenstein JL. 2005. Mice lacking Dlx1 show subtype-specific loss of interneurons, reduced inhibition and epilepsy. Nat Neurosci 8:1059-1068.
5. Cobos I, Borello U, Rubenstein JL. 2007. Dlx transcription factors promote migration through repression of axon and dendrite growth. Neuron 54:873-888.
6. Cool DR, Normant E, Shen F, Chen HC, Pannell L, Zhang Y, Loh YP. 1997. Carboxypeptidase E is a regulated secretory pathway sorting receptor: genetic obliteration leads to endocrine disorders in Cpe(fat) mice. Cell 88:73-83.
7. De Roo M, Klauser P, Garcia PM, Poglia L, Muller D. 2008. Spine dynamics and synapse remodeling during LTP and memory processes. Prog Brain Res 169:199-207.
8. Diamond DM, Campbell AM, Park CR, Woodson JC, Conrad CD, Bachstetter AD, Mervis RF. 2006. Influence of predator stress on the consolidation vs. retrieval of long-term spatial memory and hippocampal spinogenesis. Hippocampus 16:571-576.
9. Fink CC, Bayer KU, Myers JW, Ferrell JE Jr, Schulman H, Meyer T. 2003. Selective regulation of neurite extension and synapse formation by the beta but not the alpha isoform of CaMKII. Neuron 39:283-297.
10. Fricker LD, Evans CJ, Esch FS, Herbert E. 1986. Cloning and sequence analysis of cDNA for bovine carboxypeptidase E. Nature 323:461-464.
11. Fu Z, Lee SH, Simonetta A, Hansen J, Sheng M, Pak DT. 2007. Differential roles of Rap1 and Rap2 small GTPases in neurite retraction and synapse elimination in hippocampal spiny neurons. J Neurochem 100:118-131.
12. Groc L, Petanjek Z, Gustafsson B, Ben-Ari Y, Hanse E, Khazipov R. 2002. In vivo blockade of neural activity alters dendritic development of neonatal CA1 pyramidal cells. Eur J Neurosci 16:1931-1938.
13. Haas K, Li J, Cline HT. 2006. AMPA receptors regulate experience-dependent dendritic arbor growth in vivo. Proc Natl Acad Sci U S A 103:12127-12131.
14. Hand R, Bortone D, Mattar P, Nguyen L, Heng JI, Guerrier S, Boutt E, Peters E, Barnes AP, Parras C, Schuurmans C, Guillemot F, Polleux F. 2005. Phosphorylation of Neurogenin2 specifies the migration properties and the dendritic morphology of pyramidal neurons in the neocortex. Neuron 48:45-62.
15. Hu B, Nikolakopoulou AM, Cohen-Cory S. 2005. BDNF stabilizes synapses and maintains the structural complexity of optic axons in vivo. Development 132:4285-4298.
16. Hughes ME, Bortnick R, Tsubouchi A, Baumer P, Kondo M, Uemura T, Schmucker D. 2007. Homophilic Dscam interactions control complex dendrite morphogenesis. Neuron 54:417-427.
17. Jan YN, Jan LY. 2003. The control of dendrite development. Neuron 40:229-242.
18. Jansen P, Giehl K, Nyengaard JR, Teng K, Lioubinski O, Sjoegaard SS, Breiderhoff T, Gotthardt M, Lin F, Eilers A, Petersen CM, Lewin GR, Hempstead BL, Willnow TE, Nykjaer A. 2007. Roles for the pro-neurotrophin receptor sortilin in neuronal development, aging and brain injury. Nat Neurosci 10:1449-1457.
19. Jaworski J, Sheng M. 2006. The growing role of mTOR in neuronal development and plasticity. Mol Neurobiol 34:205-219.
20. Johnson EM, Craig ET, Yeh HH. 2007. TrkB is necessary for pruning at the climbing fibre-Purkinje cell synapse in the developing murine cerebellum. J Physiol 582:629-646.
21. Jossin Y, Goffinet AM. 2007. Reelin signals through phosphatidylinositol 3-kinase and Akt to control cortical development and through mTor to regulate dendritic growth. Mol Cell Biol 27:7113-7124.
22. Kohn J, Aloyz RS, Toma JG, Haak-Frendscho M, Miller FD. 1999. Functionally antagonistic interactions between the TrkA and p75 neurotrophin receptors regulate sympathetic neuron growth and target innervation. J Neurosci 19:5393-5408.
23. Kumar V, Zhang MX, Swank MW, Kunz J, Wu GY. 2005. Regulation of dendritic morphogenesis by Ras-PI3K-Akt-mTOR and Ras-MAPK signaling pathways. J Neurosci 25:11288-11299.
24. Lee KF, Bachman K, Landis S, Jaenisch R. 1994. Dependence on p75 for innervation of some sympathetic targets. Science 263:1447-1449.
25. Liu F, Day M, Muniz LC, Bitran D, Arias R, Revilla-Sanchez R, Grauer S, Zhang G, Kelley C, Pulito V, Sung A, Mervis RF, Navarra R, Hirst WD, Reinhart PH, Marquis KL, Moss SJ, Pangalos MN, Brandon NJ. 2008. Activation of estrogen receptor-beta regulates hippocampal synaptic plasticity and improves memory. Nat Neurosci 11:334-343.
26. Liu XB, Low LK, Jones EG, Cheng HJ. 2005. Stereotyped axon pruning via plexin signaling is associated with synaptic complex elimination in the hippocampus. J Neurosci 25:9124-9134.
27. Lou H, Kim SK, Zaitsev E, Snell CR, Lu B, Loh YP. 2005. Sorting and activity-dependent secretion of BDNF require interaction of a specific motif with the sorting receptor carboxypeptidase e. Neuron 45:245-255.
28. Lush ME, Ma L, Parada LF. 2005. TrkB signaling regulates the developmental maturation of the somatosensory cortex. Int J Dev Neurosci 23:523-536.
29. Malone JI, Hanna S, Saporta S, Mervis RF, Park CR, Chong L, Diamond DM. 2008. Hyperglycemia not hypoglycemia alters neuronal dendrites and impairs spatial memory. Pediatric Diabetes 9:531-539.
30. Matsuzaki M. 2007. Factors critical for the plasticity of dendritic spines and memory storage. Neurosci Res 57:1-9.
31. Morita A, Yamashita N, Sasaki Y, Uchida Y, Nakajima O, Nakamura F, Yagi T, Taniguchi M, Usui H, Katoh-Semba R, Takei K, Goshima Y. 2006. Regulation of dendritic branching and spine maturation by semaphorin3A-Fyn signaling. J Neurosci 26:2971-2980.
32. Negishi M, Katoh H. 2002. [Regulation of neurite formation by Rho family GTPases]. Seikagaku 74:395-398.
33. Neigh GN, Glasper ER, Kofler J, Traystman RJ, Mervis RF, Bachstetter A, DeVries AC. 2004. Cardiac arrest with cardiopulmonary resuscitation reduces dendritic spine density in CA1 pyramidal cells and selectively alters acquisition of spatial memory. Eur J Neurosci 20:1865-1872.
34. Park JJ, Cawley NX, Loh YP. 2008. A bi-directional carboxypeptidase E-driven transport mechanism controls BDNF vesicle homeostasis in hippocampal neurons. Mol Cell Neurosci 39:63-73.
35. Parrish JZ, Emoto K, Kim MD, Jan YN. 2007. Mechanisms that regulate establishment, maintenance, and remodeling of dendritic fields. Annu Rev Neurosci 30:399-423.
36. Pokorny J, Trojan S. 1983. Chronic changes in the receptive field of the pyramidal cells of the rat hippocampus after intermittent postnatal hypoxia. Physiol Bohemoslovaca 32:393-402.
37. Pokorny J, Trojan S. 1986. The development of hippocampal structure and how it is influenced by hypoxia. Acta Universitatis Carolinae Med 113:1-79.
38. Prithviraj R, Kelly KM, Espinoza-Lewis R, Hexom T, Clark AB, Inglis FM. 2008. Differential regulation of dendrite complexity by AMPA receptor subunits GluR1 and GluR2 in motor neurons. Dev Neurobiol 68:247-264.
39. Redmond L, Oh SR, Hicks C, Weinmaster G, Ghosh A. 2000. Nuclear Notch1 signaling and the regulation of dendritic development. Nat Neurosci 3:30-40.
40. Rosso SB, Sussman D, Wynshaw-Boris A, Salinas PC. 2005. Wnt signaling through Dishevelled, Rac and JNK regulates dendritic development. Nat Neurosci 8:34-42.
41. Schaefer AT, Larkum ME, Sakmann B, Roth A. 2003. Coincidence detection in pyramidal neurons is tuned by their dendritic branching pattern. J Neurophysiol 89:3143-3154.
42. Scott EK, Luo L. 2001. How do dendrites take their shape? Nat Neurosci 4:359-365.
43. Silva-Gomez AB, Rojas D, Juarez I, Flores G. 2003. Decreased dendritic spine density on prefrontal cortical and hippocampal pyramidal neurons in postweaning social isolation rats. Brain Res 983:128-136.
44. Sin WC, Haas K, Ruthazer ES, Cline HT. 2002. Dendrite growth increased by visual activity requires NMDA receptor and Rho GTPases. Nature 419:475-480.
45. Singh KK, Miller FD. 2005. Activity regulates positive and negative neurotrophin-derived signals to determine axon competition. Neuron 45:837-845.
46. Singh KK, Park KJ, Hong EJ, Kramer BM, Greenberg ME, Kaplan DR, Miller FD. 2008. Developmental axon pruning mediated by BDNF-p75NTR-dependent axon degeneration. Nat Neurosci 11:649-658.
47. Tolias KF, Bikoff JB, Burette A, Paradis S, Harrar D, Tavazoie S, Weinberg RJ, Greenberg ME. 2005. The Rac1-GEF Tiam1 couples the NMDA receptor to the activity-dependent development of dendritic arbors and spines. Neuron 45:525-538.
48. Tolwani RJ, Buckmaster PS, Varma S, Cosgaya JM, Wu Y, Suri C, Shooter EM. 2002. BDNF overexpression increases dendrite complexity in hippocampal dentate gyrus. Neuroscience 114:795-805.
49. Ueda S, Fujimoto S, Hiramoto K, Negishi M, Katoh H. 2008. Dock4 regulates dendritic development in hippocampal neurons. J Neurosci Res 86:3052-3061.
50. Valverde F. 2002. [Structure of the cerebral cortex. Intrinsic organization and comparative analysis of the neocortex]. Rev Neurol 34:758-780.
51. Waimey KE, Cheng HJ. 2006. Axon pruning and synaptic development: how are they per-plexin? Neuroscientist 12:398-409.
52. Wayman GA, Impey S, Marks D, Saneyoshi T, Grant WF, Derkach V, Soderling TR. 2006. Activity-dependent dendritic arborization mediated by CaM-kinase I activation and enhanced CREB-dependent transcription of Wnt-2. Neuron 50:897-909.
53. Wirth MJ, Brun A, Grabert J, Patz S, Wahle P. 2003. Accelerated dendritic development of rat cortical pyramidal cells and interneurons after biolistic transfection with BDNF and NT4/5. Development 130:5827-5838.
54. Wong RO, Ghosh A. 2002. Activity-dependent regulation of dendritic growth and patterning. Nat Rev Neurosci 3:803-812.
55. Woronowicz A, Koshimizu H, Chang SY, Cawley NX, Hill JM, Rodriguiz RM, Abebe D, Dorfman C, Senatorov V, Zhou A, Xiong ZG, Wetsel WC, Loh YP. 2008. Absence of carboxypeptidase E leads to adult hippocampal neuronal degeneration and memory deficits. Hippocampus 18:1051-1063.
56. Wu JI, Lessard J, Olave IA, Qiu Z, Ghosh A, Graef IA, Crabtree GR. 2007. Regulation of dendritic development by neuron-specific chromatin remodeling complexes. Neuron 56:94-108.
57. Zhu X, Rife L, Cawley NX, Brown B, Adams T, Teofilo K, Lillo C, Williams DS, Loh YP, Craft CM. 2005. Carboxypeptidase E is required for normal synaptic transmission from photoreceptors to the inner retina. J Neurochem 95:1351-1362.