Expression of the embryonal isoform (0n/3R) of the microtubule-associated protein tau in the adult rat central nervous system

Journal of Comparative Neurology

Volumn 518, Issue 13, 2010, Pages 2538-2553

  Bullmann, Torsten ^a   Härtig, Wolfgang ^a   Holzer, Max ^a   Arendt, Thomas ^a  

^a UNIVERSITY OF LEIPZIG   (Germany)

Author keywords

Acetylcholine; Hypocretin orexin; Microtubule binding repeats; Neurogenesis; Norepinephrine; Olfactory system; Oxytocin; Serotonin; Tau protein isoform; Vasopressin

Indexed keywords

COLLAPSIN RESPONSE MEDIATOR PROTEIN; DOUBLECORTIN; ISOPROTEIN; NERVE CELL ADHESION MOLECULE; TAU PROTEIN; MAPT PROTEIN, RAT;

ADULT ANIMAL; ALTERNATIVE RNA SPLICING; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; CENTRAL NERVOUS SYSTEM; CHEMICAL LABELING; CONTROLLED STUDY; DEVELOPMENT; EMBRYO; FEMALE; HYPOTHALAMUS; IMMUNOHISTOCHEMISTRY; LOCUS CERULEUS; MALE; MICROTUBULE; NERVE CELL; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NEWBORN; NONHUMAN; OLFACTORY BULB; OLFACTORY CORTEX; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN STRUCTURE; PYRIFORM CORTEX; RAPHE NUCLEUS; RAT; SOLITARY TRACT NUCLEUS; TISSUE SECTION; ADULT STEM CELL; AGING; ANIMAL; BRAIN; FLUORESCENT ANTIBODY TECHNIQUE; METABOLISM; MICROPHOTOGRAPHY; WESTERN BLOTTING; WISTAR RAT;

ADULT STEM CELLS; AGING; ANIMALS; BLOTTING, WESTERN; BRAIN; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; IMMUNOHISTOCHEMISTRY; MALE; NEURONS; PHOTOMICROGRAPHY; PROTEIN ISOFORMS; RATS; RATS, WISTAR; TAU PROTEINS;

EID: 77952112984     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.22351     Document Type: Article

References (67)

1. Aaron LI, Chesselet MF. 1989. Heterogeneous distribution of polysialylated neuronal-cell adhesion molecule during postnatal development and in the adult: an immunohistochemical study in the rat brain. Neuroscience 28:701-710.
2. AimP,LarssonB,EkbladE,SundlerF,AnderssonKE.1993. Immunohistochemicallocalizationofperipheralnitricoxidesynthase- containingnervesusingantibodiesraisedagainstsynthesizedC-andN- terminalfragmentsofaclonedenzymefromratbrain.ActaPhysiolScand148:421-429. (Pubitemid23234551)
3. Altman J, Sudarshan K. 1975. Postnatal development of locomotion in the laboratory rat. Anim Behav 23:896-920.
4. Bonfanti L, Olive S, Poulain DA, Theodosis DT. 1992. Mapping of the distribution of polysialylated neural cell adhesion molecule throughout the central nervous system of the adult rat: an immunohistochemical study. Neuroscience 49:419-436.
5. Brandt R, Léger J, Lee G. 1995. Interaction of tau with the neural plasma membrane mediated by tau's amino-terminal projection domain. J Cell Biol 131:1327-1340.
6. Brauer K, Schober A, Wolff JR, Winkelmann E, Luppa H, Lüth HJ, Böttcher H. 1991. Morphology of neurons in the rat basal forebrain nuclei: comparison between NADPH-diaphorase histochemistry and immunohistochemistry of glutamic acid decarboxylase, choline acetyltransferase, somatostatin and paralbumin. J Hirnforsch 32:1-17.
7. Brown JP, Couillard-Després S, Cooper-Kuhn CM, Winkler J, Aigner L, Kuhn HG. 2003. Transient expression of doublecortin during adult neurogenesis. J Comp Neurol 467:1-10. (Pubitemid 37339753)
8. Bullmann T, de Silva R, Holzer M, Mori H, Arendt T. 2007. The expression of embryonic tau protein isoforms persist during adult neurogenesis in the hippocampus. Hippocampus 17:98-102. (Pubitemid 46362604)
9. Bullmann T, Holzer M, Mori H, Arendt T. 2009. Pattern of tau isoforms expression during development in vivo. Int J Dev Neurosci 27:591-597.
10. Caceres A, Kosik KS. 1990. Inhibition of neurite polarity by tau antisense oligonucleotides in primary cerebellar neurons. Nature 343:461-463. (Pubitemid 20065232)
11. Castellino CB, Diekamp B, Ball GF. 2007. Noradrenergic projections to the song control nucleus area X of the medial striatum in male zebra finches (Taeniopygia guttata). J Comp Neurol 502:544-562. (Pubitemid 46732507)
12. Chen J, Kanai Y, Cowan NJ, Hirokawa N. 1992. Projection domains of MAP2 and tau determine spacings between microtubules in dendrites and axons. Nature 360: 674-677. (Pubitemid 23007681)
13. Chen M, Martins RN, Lardelli M. 2009. Complex splicing and neural expression of duplicated tau genes in zebrafish embryos. J Alzheimers Dis 18:305-317.
14. ChuongCM,EdelmanGM.1984. Alterationsinneuralcelladhesionmoleculesduringdevelopmentofdifferentregionsofth enervoussystem.JNeurosci4:2354-2368.(Pubitemid14010932)
15. Cleveland DW, Hwo SY, Kirschner MW. 1977. Physical and chemical properties of purified tau factor and the role of tau in microtubule assembly. J Mol Biol 116:227-247.
16. Crocker A, España RA, Papadopoulou M, Saper CB, Faraco J, Sakurai T, Honda M, Mignot E, Scammell TE. 2005. Concomitant loss of dynorphin, NARP, and orexin in narcolepsy. Neurology 65:1184-1188. (Pubitemid 41508208)
17. Dayanandan R, Van Slegtenhorst M, Mack TG, Ko L, Yen SH, Leroy K, Brion JP, Anderton, BH, Hutton M, Lovestone S. 1999. Mutations in tau reduce its microtubule binding properties in intact cells and affect its phosphorylation. FEBS Lett 446:228-232. (Pubitemid 29132731)
18. de Lecea L, Kilduff TS, Peyron C, Gao X, Foye PE, Danielson PE, Fukuhara C, Battenberg EL, Gautvik VT, Bartlett FS 2nd, Frankel WN, van den Pol AN, Bloom FE, Gautvik KM, Sutcliffe JG. 1998. The hypocretins: hypothalamus-specific peptides with neuroexcitatory activity. Proc Natl Acad Sci USA 95:322-327.
19. de Silva R, Lashley T, Gibb G, Hanger D, Hope A, Reid A, Bandopadhyay R, Utton M, Strand C, Jowett T, Khan N, Anderten B, Wood N, Holton J, Revesz T, Lees A. 2003. Pathological inclusion bodies in tauopathies contain distinct complements of tau with three or four microtubulebinding repeat domains as demonstrated by new specific monoclonal antibodies. Neuropathol Appl Neurobiol 29: 288-302. (Pubitemid 36718177)
20. Dehal P, Satou Y, Campbell RK, Chapman J, Degnan B, De Tomaso A, Davidson B, Di Gregorio A, Gelpke M, Goodstein DM, Harafuji N, Hastings KE, Ho I, Hotta K, Huang W, Kawashima T, Lemaire P, Martinez D, Meinertzhagen IA, Necula S, Nonaka M, Putnam N, Rash S, Saiga H, Satake M, Terry A, Yamada L, Wang HG, Awazu S, Azumi K, Boore J, Branno M, Chin-Bow S, DeSantis R, Doyle S, Francino P, Keys DN, Haga S, Hayashi H, Hino K, Imai KS, Inaba K, Kano S, Kobayashi K, Kobayashi M, Lee BI, Makabe KW, Manohar C, Matassi G, Medina M, Mochizuki Y, Mount S, Morishita T, Miura S, Nakayama A, Nishizaka S, Nomoto H, Ohta F, Oishi K, Rigoutsos I, Sano M, Sasaki A, Sasakura Y, Shoguchi E, Shin-i T, Spagnuolo A, Stainier D, Suzuki MM, Tassy O, Takatori N, Tokuoka M, Yagi K, Yoshizaki F, Wada S, Zhang C, Hyatt PD, Larimer F, Detter C, Doggett N, Glavina T, Hawkins T, Richardson P, Lucas S, Kohara Y, Levine M, Satoh N, Rokhsar DS. 2002. The draft genome of Ciona intestinalis: insights into chordate and vertebrate origins. Science 298:2157-2167. (Pubitemid 35471235)
21. Dehmelt L, Halpain S. 2006. The MAP2/Tau family of microtubule-associated proteins. Genome Biol 6:204.
22. Drubin DG, Feinstein SC, Shooter EM, Kirschner MW. 1985. Nerve growth factor-induced neunte outgrowth in PC 12 cells involves the coordinate induction of microtubule assembly and assembly-promoting factors. J Cell Biol 101: 1799-1807.
23. Ehret M, Gobaille S, Cash CD, Mandel P, Maitre M. 1987. Regional distribution in rat brain of tryptophan hydrolase apoenzyme determined by enzyme-linked immunoassay. Neurosci Lett 73:71-76. (Pubitemid 17207726)
24. Farrar CE, Huang CS, Clarke SG, Houser CR. 2005. Increased cell proliferation and granule cell number in the dentate gyrus of protein repair-deficient mice. J Comp Neurol 493: 524-537.
25. Fifková E. 1968. Changes in the visual cortex of rats after unilateral deprivation. Nature 220:379-381.
26. 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. 1999. Doublecortin is a developmentally regulated, microtubule-associated protein expressed in migrating and differentiating neurons. Neuron 23:247-256. (Pubitemid 29315721)
27. Goedert M, Jakes R. 2005. Mutations causing neurodegenerative tauopathies. Biochim Biophys Acta 1739:240-250.
28. Goedert M, Spillantini MG, Jakes R, Rutherford D, Crowther RA. 1989a. Multiple isoforms of human microtubule-associated protein tau: sequences and localization in neurofibrillary tangles of Alzheimer's disease. Neuron 3:519-526.
29. Goedert M, Spillantini MG, Potier MC, Ulrich J, Crowther RA. 1989b. Cloning and sequencing of the cDNA encoding an isoform of microtubule-associated protein tau containing four tandem repeats: differential expression of tau protein mRNAs in human brain. EMBO J 8:393-399. (Pubitemid 19274956)
30. Goedert M, Baur CP, Ahringer J, Jakes R, Hasegawa M, Spillantini MG, Smith MJ, Hill F. 1996. PTL-1, a microtubuleassociated protein with tau-like repeats from the nematode Caenorhabditis elegans. J Cell Sci 109:2661-2672. (Pubitemid 26388351)
31. Gómez-Climent MA, Castillo-Gómez E, Varea E, Guirado R, Blasco-Ibáñez JM, Crespo C, Martínez-Guijarro FJ, Nácher J. 2008. A population of prenatally generated cells in the rat paleocortex maintains an immature neuronal phenotype into adulthood. Cereb Cortex 18:2229-2240.
32. Goode BL, Feinstein SC. 1994. Identification of a novel microtubule binding and assembly domain in the developmentally regulated inter-repeat region of tau. J Cell Biol 124: 769-782. (Pubitemid 24983343)
33. Haycock JW. 1987. Stimulation-dependent phosphorylation of tyrosine hydroxylase in rat corpus striatum. Brain Res Bull 19:619-622.
34. Heidary G, Fortini ME. 2001. Identification and characterization of the Drosophila tau homolog. Mech Dev 108:171-178. (Pubitemid 32923065)
35. Holzer M, Craxton M, Jakes R, Arendt T, Goedert M. 2004. Tau gene (MAPT) sequence variation among primates. Gene 341:313-322. (Pubitemid 39335906)
36. Janke C, Beck M, Stahl T, Holzer M, Brauer K, Bigl V, Arendt T. 1999. Phylogenetic diversity of the expression of the microtubule-associated protein tau: implications for neurodegenerative disorders. Brain Res Mol Brain Res 68: 119-128. (Pubitemid 29244000)
37. Kaufling J, Veinante P, Pawlowski SA, Freund-Mercier MJ, Barrot M. 2009. Afferents to the GABAergic tail of the ventral tegmental area in the rat. J Comp Neurol 513:597-621.
38. Kerman IA, Akil H, Watson SJ. 2006. Rostral elements of sympatho-motor circuitry: a virally mediated transsynaptic tracing study. J Neurosci 26:3423-3433.
39. Kosik KS, Orecchio LD, Bakalis S, Neve RL. 1989. Developmentally regulated expression of specific tau sequences. Neuron 2:1389-1397.
40. Lee G, Cowan N, Kirschner M. 1988. The primary structure and heterogeneity of tau protein from mouse brain. Science 239:285-288. (Pubitemid 18061495)
41. Levy SF, Leboeuf AC, Massie MR, Jordan MA, Wilson L, Feinstein SC. 2005. Three- and four-repeat tau regulate the dynamic instability of two distinct microtubule subpopulations in qualitatively different manners-implications for neurodegeneration. J Biol Chem 280:13520-13528. (Pubitemid 40517243)
42. Liu Y, Xia J, Ma D, Faber DS, Fischer I. 1997. Tau-like proteins in the nervous system of goldfish. Neurochem Res 22: 1511-1516. (Pubitemid 27461128)
43. Luzzati F, Bonfanti L, Fasolo A, Peretto P. 2009. DCX and PSA-NCAM expression identifies a population of neurons preferentially distributed in associative areas of different palliai derivatives and vertebrate species. Cereb Cortex 19: 1028-1041.
44. McDermott JB, Aamodt S, Aamodt E. 1996. ptl-1, a Caenorhabditis elegans gene whose products are homologous to the tau microtubule-associated proteins. Biochemistry 35: 9415-9423. (Pubitemid 26320047)
45. McMillan P, Korvatska E, Poorkaj P, Evstafjeva Z, Robinson L, Greenup L, Leverenz J, Schellenberg GD, D'Souza I. 2008. Tau isoform regulation is region- and cell-specific in mouse brain. J Comp Neurol 511:788-803.
46. Nacher J, Rosell DR, McEwen BS. 2000. Widespread expression of rat collapsin response-mediated protein 4 in the telencephalon and other areas of the adult rat central nervous system. J Comp Neurol 424:628-639. (Pubitemid 30643055)
47. Nacher J, Crespo C, McEwen BS. 2001. Doublecortin expression in the adult rat telencephalon. Eur J Neurosci 14: 629-644.
48. Nagatsu T, Stjäme L. 1998. Catecholamine synthesis and release. Overview. Adv Pharmacol 42: 1-14.
49. Nelson PT, Stefansson K, Gulcher J, Saper CB. 1996. Molecular evolution of tau protein: implications for Alzheimer's disease. J Neurochem 67:1622-1632. (Pubitemid 26314220)
50. Ngwenya LB, Peters A, Rosene DL. 2006. Maturational sequence of newly generated neurons in the dentate gyrus of the young adult rhesus monkey. J Comp Neurol 498: 204-216. (Pubitemid 44182461)
51. Olesen OF, Kawabata-Fukui H, Yoshizato K, Noro N. 2002. Molecular cloning of XTP, a tau-like microtubule-associated protein from Xenopus laevis tadpoles. Gene 283:299-309. (Pubitemid 34178534)
52. Pan YZ, Li DP, Chen SR, Pan HL. 2004. Activation of muopioid receptors excites a population of locus coeruleusspinal neurons through presynaptic disinhibition. Brain Res 997:67-78.
53. Paxinos G, Watson C. 1986. The rat brain in stereotaxic coordinates. London: Academic Press.
54. Ren T, Sagar SM. 1992. Induction of c-fos immunostaining in the rat brain after the systemic administration of nicotine. Brain Res Bull 29:589-597.
55. Seki T, Arai Y. 1993. Distribution and possible roles of the highly polysialylated neural cell adhesion molecule (NCAMH) in the developing and adult central nervous system. Neurosci Res 17:265-290. (Pubitemid 23298835)
56. Simons DJ, Land PW. 1987. Early experience of tactile stimulation influences organization of somatic sensory cortex. Nature 326:694-697.
57. Succu S, Sanna F, Cocco C, Melis T, Boi A, Feri GL, Argiolas A, Melis MR. 2008. Oxytocin induces penile erection when injected into the ventral tegmental area of male rats: role of nitric oxide and cyclic GMP. Eur J Neurosci 28: 813-821.
58. Takuma H, Arawaka S, Mori H. 2003. Isoforms changes of tau protein during development in various species. Brain Res Dev Brain Res 142:121-127. (Pubitemid 36593156)
59. Theodosis DT, Trailin A, Poulain DA. 2006. Remodeling of astrocytes, a prerequisite for synapse turnover in the adult brain? Insights from the oxytocin system of the hypothalamus. Am J Physiol Regul lntegr Comp Physiol 290: R1175-1182.
60. Tomasiewicz HG, Wood JG. 1999. Characterization of microtubule-associated proteins in teleosts. Cell Motil Cytoskeleton 44:155-167.
61. Tucker RP, Matus Al. 1988. Microtubule-associated proteins characteristic of embryonic brain are found in the adult mammalian retina. Dev Biol 130:423-434.
62. Viereck C, Tucker RP, Matus A. 1989. The adult rat olfactory system expresses microtubule-associated proteins found in the developing brain. J Neurosci 9:3547-3557. (Pubitemid 19260027)
63. Wang LH, Strittmatter SM. 1996. A family of rat CRMP genes is differentially expressed in the nervous system. J Neurosci 16:6197-6207. (Pubitemid 26313994)
64. Weingarten MD, Lockwood AH, Hwo SY, Kirschner MW. 1975. A protein factor essential for microtubule assembly. Proc Natl Acad Sci USA 72:1858-1862.
65. Wozniak DF, Stewart GR, Finger S, Olney JW. 1989. Comparison of behavioral effects of nucleus basalis magnocellularis lesions and somatosensory cortex ablation in the rat. Neuroscience 32:685-700. (Pubitemid 20008297)
66. Xu Q, Tam M, Anderson SA. 2008. Fate mapping Nkx2.1-lineage cells in the mouse telencephalon. J Comp Neurol 506: 16-29. (Pubitemid 350293488)
67. Yoshida H, Goedert M. 2002. Molecular cloning and functional characterization of chicken brain tau: isoforms with up to five tandem repeats. Biochemistry 41:15203-15211. (Pubitemid 36008129)