The developmentally regulated expression of Menkes protein ATP7A suggests a role in axon extension and synaptogenesis

Developmental Neuroscience

Volumn 27, Issue 5, 2005, Pages 333-348

  El Meskini, Rajaâ ^a   Cline, Laura B ^b   Eipper, Betty A ^a   Ronnett, Gabriele V ^b  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

ATP7A; Menkes disease; Neurodevelopment; Olfactory receptor neurons; Olfactory system; Process outgrowth; Regeneration; Synaptogenesis

Indexed keywords

MENKES PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FEMALE; MALE; MOUSE; NERVE CELL DIFFERENTIATION; NERVE FIBER; NERVE GROWTH; NERVE REGENERATION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; OLFACTORY SYSTEM; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY MECHANISM; SYNAPTOGENESIS;

ADENOSINE TRIPHOSPHATASES; ANIMALS; AXONS; AXOTOMY; BLOTTING, WESTERN; CATION TRANSPORT PROTEINS; EMBRYO; IMMUNOHISTOCHEMISTRY; MALE; MICE; NERVE REGENERATION; NEURONS; OLFACTORY BULB; OLFACTORY MUCOSA; RATS; SYNAPSES;

EID: 24144458246     PISSN: 03785866     EISSN: None     Source Type: Journal    
DOI: 10.1159/000086713     Document Type: Article

References (81)

1. Ajiro K, Yoda K, Utsumi K, Nishikawa Y (1996): Alteration of cell cycle-dependent histone phosphorylations by okadaic acid. Induction of mitosis-specific H3 phosphorylation and chromatin condensation in mammalian interphase cells. J Biol Chem 271:13197-13201.
2. Arimura A, Somogyvari-Vigh A, Weill C, Fiore RC, Tatsuno I, Bay V, Brenneman DE (1994): PACAP functions as a neurotrophic factor. Ann NY Acad Sci 739:228-243.
3. Baker H (1990): Calcitonin gene-related peptide in the developing mouse olfactory system. Brain Res Dev Brain Res 54:295-298.
4. Baker H, Grillo M, Margolis FL (1989): Biochemical and immunocytochemical characterization of olfactory marker protein in the rodent central nervous system. J Comp Neurol 285:246-61.
5. Buck LB (1996): Information coding in the vertebrate olfactory system. Ann Rev Neurosci 19:517-544.
6. Caggiano M, Kauer JS, Hunter DD (1994): Globose basal cells are neuronal progenitors in the olfactory epithelium: A lineage analysis using a replication-incompetent retrovirus. Neuron 13:339-352.
7. Calof AL, Chikaraishi DM (1989): Analysis of neurogenesis in a mammalian neuroepithelium: Proliferation and differentiation of an olfactory neuron precursor in vitro. Neuron 3:115-127.
8. Carr VM, Farbman AI (1992): Ablation of the olfactory bulb up-regulates the rate of neurogenesis and induces precocious cell death in olfactory epithelium. Exp Neurol 115:55-59.
9. Carr VM, Farbman AI (1993): The dynamics of cell death in the olfactory epithelium. Exp Neurol 124:308-314.
10. Chelly J, Turmer Z, Tonnerson T (1993): Isolation of a candidate gene for Menkes disease that encodes a potential heavy metal binding protein. Nat Genet 3:14-19.
11. Constanzo RM, Graziadei PPC (1983): A qualitative analysis of changes in the olfactory epithelium following bulbectomy in hamster. J Comp Neurol 215:370-381.
12. Cummings DM, Emge DK, Small SL, Margolis FL (2000): Pattern of olfactory bulb innervation returns after recovery from reversible peripheral deafferentation. J Comp Neurol 421:362-373.
13. Cuschieri A, Bannister LH (1975): The development of the olfactory mucosa in the mouse: electron microscopy. J Anat 119:471-498.
14. Davis JA, Reed RR (1996): Role of Olf-1 and Pax-6 transcription factors in neurodevelopment. J Neurosci 16:5082-5094.
15. Denis-Donini S, Chini B, Vitadello M (1993): Developmentally regulated expression of CGRP in the mouse olfactory pathway. Eur J Neurosci 5:648-656.
16. DiCicco-Bloom E (1996): Region-specific regulation of neurogenesis by VIP and PACAP: Direct and indirect modes of action. Ann NY Acad Sci 805:244-258.
17. El Meskini R, Mains RE, Eipper BA (2000): Cell type-specific metabolism of peptidylglycine alpha-amidating monooxygenase in anterior pituitary. Endocrinology 141:3020-3034.
18. Farbman A (1977): Differentiation of olfactory receptor cells in organ culture. Anat Rec 189:187-199.
19. Farbman AI (1991): Developmental neurobiology of the olfactory system; in Getchell TV, Doty RL, Bartoshuk LM, Snow JB Jr (eds): Smell and Taste in Health and Disease. New York, Raven Press, pp 199-233.
20. Farbman AI (1992): Development and plasticity; in Barlow PW, Bray D, Green PB, Slack LMW (eds): Cell Biology of Olfaction. Cambridge, Cambridge University Press, pp 167-206.
21. Getchell TV (1986): Functional properties of vertebrate olfactory receptor neurons. Physiol Rev 66:772-818.
22. Goldstein BJ, Schwob JE (1996): Analysis of the globose basal cell compartment in rat olfactory epithelium using GBC-1, a new monoclonal antibody against globose basal cells. J Neurosci 16:4005-4016.
23. Graziadei PPC (1971): The olfactory mucosa of vertebrates; in Beidler LM (ed): Handbook of Sensory Physiology. Vol IV. Chemical Senses. Part 1. Olfaction. Berlin, Springer, pp 27-58.
24. Graziadei PPC, Metcalf JF (1971): Autoradiographic and ultrastructural observation on the frog's olfactory mucosa. Z Zellforsch Mikrosk Anal 116:305-318.
25. Grimes A, Hearn CJ, Lockhart P, Newgreen DF, Mercer JF (1997): Molecular basis of the brindled mouse mutant (Mo(br)): A murine model of Menkes disease. Hum Mol Genet 6:1037-1042.
26. Halasz N, Greer CA (1993): Terminal arborizations of olfactory nerve fibers in the glomeruli of the olfactory bulb. J Comp Neurol 337:307-316.
27. Hansel DE, Eipper BA, Ronnett GV (2001): Neuropeptide Y functions as a neuroproliferative factor. Nature 410:940-944.
28. Harrison MD, Dameron CT (1999): Molecular mechanisms of copper metabolism and the role of the Menkes disease protein. J Biochem Mol Toxicol 13:93-106.
29. Hartman BK, Margolis FL (1975): Immunofluorescence localization of the olfactory marker protein. Brain Res 96:176-180.
30. Hinds JW (1968): Autoradiographic study of histogenesis in the mouse olfactory bulb. 1. Time of origin of neurons and neuroglia. J Comp Neurol 134:287-304.
31. Hirsch JD, Margolis FL (1980): Influence of unilateral olfactory bulbectomy on opiate and other binding sites in the contralateral bulb. Brain Res 199:39-47.
32. Holcomb JD, Mumm JS, Calof AL (1995): Apoptosis in the neuronal lineage of the mouse olfactory epithelium: Regulation in vivo and in vitro. Dev Biol 172:307-323.
33. Horn N, Tonnesen T, Tumer Z (1992): Menkes disease: An X-linked neurological disorder of the copper metabolism. Brain Pathol 2:351-362.
34. Hsi G, Cox DW (2004): A comparison of the mutation spectra of Menkes disease and Wilson disease. Hum Genet 114:165-172.
35. Huard JM, Youngentob SL, Goldstein BJ, Luskin MB, Schwob JE (1998): Adult olfactory epithelium contains multipotent progenitors that give rise to neurons and non-neural cells. J Comp Neurol 400:469-486.
36. Iwase T, Nishimura M, Sugimura H, Igarashi H, Ozawa F, Shinmura K, Suzuki M, Tanaka M, Kino I (1996): Localization of Menkes gene expression in the mouse brain; its association with neurological manifestations in Menkes model mice. Acta Neuropathol (Berl) 91:482-488.
37. Keller A, Margolis FL (1975): Immunological studies of the rat olfactory marker protein. J Neurochem 24:1101-1106.
38. La Fontaine S, Firth SD, Lockhart PJ, Brooks H, Camakaris J, Mercer JF (1999): Intracellular localization and loss of copper responsiveness of Mnk, the murine homologue of the Menkes protein, in cells from blotchy (Mo blo) and brindled (Mo br) mouse mutants. Hum Mol Genet 8:1069-1075.
39. La Fontaine S, Firth SD, Lockhart PJ, Brooks H, Parton RG, Camakaris J, Mercer JF (1998): Functional analysis and intracellular localization of the human Menkes protein (MNK) stably expressed from a cDNA construct in Chinese hamster ovary cells (CHO-K1). Hum Mol Genet 7:1293-1300.
40. Labarca P, Bacigalupo J (1988): Ion channels from chemosensory olfactory neurons. J Bioenerg Biomembr 20:551-569.
41. Laemmli UK (1970): Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
42. Lee J, Prohaska JR, Thiele DJ (2001): Essential role for mammalian copper transporter Ctr1 in copper homeostasis and embryonic development. Proc Natl Acad Sci USA 98:6842-6847.
43. Legrier ME, Ducray A, Propper A, Chao M, Kastner A (2001): Cell cycle regulation during mouse olfactory neurogenesis. Cell Growth Differ 12:591-601.
44. Lowe G, Gold GH (1991): The spatial distributions of odorant sensitivity and odorant-induced currents in salamander olfactory receptor cells. J Physiol 442:147-168.
45. Lowe G, Gold GH (1993): Contribution of the ciliary cyclic nucleotide-gated conductance to olfactory transduction in the salamander. J Physiol 462:175-196.
46. Luskin MB, Zigova T, Soteres BJ, Stewart RR (1997): Neuronal progenitor cells derived from the anterior subventricular zone of the neonatal rat forebrain continue to proliferate in vitro and express a neuronal phenotype. Mol Cell Neurosci 8:351-366.
47. Mackay-Sim A, Kittel P (1991): Cell dynamics in the adult mouse olfactory epithelium: A quantitative autoradiographic study. J Neurosci 11:979-984.
48. Mann JR, Camakaris J, Danks DM, Walliczek EG (1979): Copper metabolism in mottled mouse mutants: Copper therapy of brindled (Mobr) mice. Biochem J 180:605-612.
49. Margolis FL, Verhaagen J, Biffo S, Huang FL, Grillo M (1991): Regulation of gene expression in the olfactory neuroepithelium: A neurogenetic matrix. Prog Brain Res 89:97-122.
50. Memberg SP, Hall AK (1995): Dividing neuron precursors express neuron-specific tubulin. J Neurobiol 27:26-43.
51. Menkes J, Alter M, Steigleder G, Weakley D, Sungs J (1962): A sex-linked recessive disorder with retardation of growth, peculiar hair and focal cerebral and cerebellar degeneration. Paediatrics 29:764-779.
52. Menkes JH (1997): Disorders of Copper Metabolism. Boston, Butterworth-Heinemann.
53. Mercer J (1998): Menkes syndrome and animal models. Am J Clin Nutr 67:S1022-S1028.
54. Mercer J, Livingston J, Hall B (1993): Isolation of a partial candidate gene for Menkes disease by positional cloning. Nat Genet 3:20-25.
55. Mercer JF (2001): The molecular basis of copper-transport diseases. Trends Mol Med 7:64-69.
56. Moon C, Yoo JY, Matarazzo V, Sung YK, Kim EJ, Ronnett GV (2002): Leukemia inhibitory factor inhibits neuronal terminal differentiation through STAT3 activation. Proc Natl Acad Sci USA 99:9015-9020.
57. Mori K, Nagao H, Yoshihara Y (1999): The olfactory bulb: Coding and processing of odor molecule information. Science 286:711-715.
58. Moulton DG, Beidler LM (1967): Structure and function in the peripheral olfactory system. Physiol Rev 47:1-52.
59. Murata Y, Kodama H, Abe T, Ishida N, Nishimura M, Levinson B, Gitschier J, Packman S (1997): Mutation analysis and expression of the mottled gene in the macular mouse model of Menkes disease. Pediatr Res 42:436-442.
60. Nittis T, Gitlin JD (2004): Role of copper in the proteosome-mediated degradation of the multicopper oxidasehephaestin. J Biol Chem 279:25696-25702.
61. Petris MJ, Mercer JF, Culvenor JG, Lockhart P, Gleeson PA, Camakaris J (1996): Ligand-regulated transport of the Menkes copper P-type ATPase efflux pump from the Golgi apparatus to the plasma membrane: A novel mechanism of regulated trafficking. EMBO J 15:6084-6095.
62. Prohaska JR, Gybina AA (2004): Intracellular copper transport in mammals. J Nutr 134:1003-1006.
63. Reed V, Boyd Y (1997): Mutation analysis provides additional proof that mottled is the mouse homologue of Menkes' disease. Hum Mol Genet 6:417-423.
64. Rogers KE, Dasgupta P, Gubler U, Grillo M, Khew-Goodall YS, Margolis FL (1987): Molecular cloning and sequencing of a cDNA for olfactory marker protein. Proc Natl Acad Sci USA 84:1704-1708.
65. Rogers KE, Grillo M, Sydor W, Poonian M, Margolis FL (1985): Olfactory neuron-specific protein is translated from a large poly(A)+ mRNA. Proc Natl Acad Sci USA 82:5218-5222.
66. Ronnett GV, Payne R (1995): A tale of two senses. Neuron 15:11-16.
67. Ronnett GV, Snyder SH (1992): Molecular messengers of olfaction. Trends Neurosci 15:508-513.
68. Roskams AJ, Bethel MA, Hurt KJ, Ronnett GV (1996): Sequential expression of Trks A, B, C in the regenerating olfactory neuroepithelium. J Neurosci 16:1294-1307.
69. Roskams AJ, Bredt DS, Dawson TM, Ronnett GV (1994): Nitric oxide mediates the formation of synaptic connections in developing and regenerating olfactory receptor neurons. Neuron 13:289-299.
70. Roskams AJI, Cai X, Ronnett GV (1998): Expression of neuron-specific beta-III tubulin during olfactory neurogenesis in the embryonic and adult rat. Neuroscience 83:191-200.
71. Schlief ML, Craig AM, Gitlin JD (2005): NMDA receptor activation mediates copper homeostasis in hippocampal neurons. J Neurosci 25:239-246.
72. Schwartz Levey M, Chikaraishi DM, Kauer JS (1991): Characterization of potential precursor populations in the mouse olfactory epithelium using immunocytochemistry and autoradiography. J Neurosci 11:3556-3564.
73. Schwob JE, Farber NB, Gottlieb DI (1986): Neurons of the olfactory epithelium in adult rats contain vimentin. J Neurosci 6:208-217.
74. Schwob JE, Mieleszko Szumowski KE, Stasky AA (1992): Olfactory sensory neurons are trophically dependent on the olfactory bulb for their prolonged survival. J Neurosci 12:3896-3919.
75. Simpson PJ, Wang E, Moon C, Matarazzo V, Cohen DR, Liebl DJ, Ronnett GV (2003): Neurotrophin-3 signaling maintains maturational homeostasis between neuronal populations in the olfactory epithelium. Mol Cell Neurosci 24:858-874.
76. Solioz M, Vulpe C (1996): CPx-type ATPases: A class of P-type ATPases that pump heavy metals. Trends Biochem Sci 21:237-241.
77. Steveson TC, Ciccotosto GD, Ma XM, Mueller GP, Mains RE, Eipper BA (2003): Menkes protein contributes to the function of peptidylglycine alpha-amidating monooxygenase. Endocrinology 144:188-200.
78. Tumer Z, Birk Moller L, Horn N (2003): Screening of 383 unrelated patients affected with Menkes disease and finding of 57 gross deletions in ATP7A. Hum Mutat 22:457-464.
79. Tumer Z, Horn N (1996): Menkes disease: Recent advances and new insights into copper metabolism. Ann Med 28:121-129.
80. Vulpe C, Levinson B, Whitney S, Packman S, Gitschier J (1993): Isolation of a candidate gene for Menkes disease and evidence that it encodes a copper-transporting ATPase. Nat Genet 3:7-13.
81. Waggoner DJ, Bartnikas TB, Gitlin JD (1999): The role of copper in neurodegenerative disease. Neurobiol Dis 6:221-230.