Decline of the presynaptic network, including GABAergic terminals, in the aging suprachiasmatic nucleus of the mouse

Journal of Biological Rhythms

Volumn 23, Issue 3, 2008, Pages 220-231

  Palomba, Maria ^a   Nygård, Mikael ^b   Florenzano, Fulvio ^c   Bertini, Giuseppe ^a   Kristensson, Krister ^b   Bentivoglio, Marina ^a,d  

^a UNIVERSITY OF VERONA   (Italy)

^b KAROLINSKA INSTITUTE   (Sweden)

^c IRCCS FONDAZIONE SANTA LUCIA   (Italy)

^d UNIVERSITY OF VERONA   (Italy)

Author keywords

Axon terminals; Biological rhythms; GABA; Senescence; Synaptophysin

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; GLUTAMATE DECARBOXYLASE 67; SYNAPTOPHYSIN;

AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENZYME LOCALIZATION; GABAERGIC SYSTEM; GENETIC TRANSCRIPTION; MALE; MOUSE; NONHUMAN; PRESYNAPTIC NERVE; PRIORITY JOURNAL; PROTEIN ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; SUPRACHIASMATIC NUCLEUS; WESTERN BLOTTING;

AGING; ANIMALS; BASE SEQUENCE; DNA PRIMERS; GAMMA-AMINOBUTYRIC ACID; GLUTAMATE DECARBOXYLASE; MALE; MICE; MICE, INBRED C57BL; PRESYNAPTIC TERMINALS; RECEPTORS, GABA; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SUPRACHIASMATIC NUCLEUS;

ANIMALIA; MUS;

EID: 43249090814     PISSN: 07487304     EISSN: 15524531     Source Type: Journal    
DOI: 10.1177/0748730408316998     Document Type: Article

References (60)

1. Abrahamson EE and Moore RY (2001) Suprachiasmatic nucleus in the mouse: retinal innervation, intrinsic organization and efferent projections. Brain Res 916: 172-191.
2. Albus H., Vansteensel MJ, Michel S., Block GD, and Meijer JH (2005) A GABAergic mechanism is necessary for coupling dissociable ventral and dorsal regional oscillators within the circadian clock. Curr Biol 15: 886-893.
3. Ando S., Tanaka Y., Toyoda Y., Kon K., and Kawashima S-I. (2002) Turnover of synaptic membranes: age-related changes and modulation by dietary restriction. J Neurosci Res 70: 290-297.
4. Antle MC and Silver R. (2005) Orchestrating time: arrangements of the brain circadian clock. Trends Neurosci 28: 145-151.
5. Aton SJ, Huettner JE, Straume M., and Herzog ED (2006) GABA and Gi/o differentially control circadian rhythms and synchrony in clock neurons. Proc Natl Acad Sci U S A 103: 19188-19193.
6. Aujard F., Cayetanot F., Bentivoglio M., and Perret M. (2006) Age-related effects on the biological clock and its behavioural output in a primate. Chronobiol Int 23: 451-460.
7. Belenky MA, Sagiv N., Fritschy JM, and Yarom Y. (2003) Presynaptic and postsynaptic GABAA receptors in rat suprachiasmatic nucleus. Neuroscience 118: 909-923.
8. Bentivoglio M., Deng XH, Nygård M., Sadki A., and Kristensson K. (2006) The aging suprachiasmatic nucleus and cytokines: functional, molecular, and cellular changes in rodents. Chronobiol Int 23: 437-449.
9. Buijs RM, Hou YX, Shinn S., and Renaud LP (1994) Ultrastructural evidence for intra- and extranuclear projections of GABAergic neurons of the suprachiasmatic nucleus. J Comp Neurol 340: 381-391.
10. Burke SN and Barnes CA (2006) Neural plasticity in the ageing brain. Nat Rev Neurosci 7: 30-40.
11. Cagampang FR, Rattray M., Powell JF, Campbell IC, and Coen CW (1996) Circadian changes of glutamate decarboxylase 65 and 67 mRNA in the rat suprachiasmatic nuclei. Neuroreport 7: 1925-1928.
12. Cajochen C., Münch M., Knoblauch V., Blatter K., and Wirz-Justice A. (2006) Age-related changes in the circadian and homeostatic regulation of human sleep. Chronobiol Int 23: 461-474.
13. Castel M. and Morris JF (2000) Morphological heterogeneity of the GABAergic network in the suprachiasmatic nucleus, the brain's circadian pacemaker. J Anat 196: 1-13.
14. Cayetanot F., Bentivoglio M., and Aujard F. (2005) Argininevasopressin and vasointestinal polypeptide rhythms in the suprachiasmatic nucleus of the mouse lemur reveal aging-related alterations of circadian pacemaker neurons in a non-human primate. Eur J Neurosci 22: 902-910.
15. Chattopadhyaya B., Di Cristo C., Wu CZ, Knott G., Kuhlman S., Fu Y., Palmiter RD, and Huang ZJ (2007) GAD67-mediated GABA synthesis and signaling regulate inhibitory synaptic innervation in the visual cortex. Neuron 54: 889-903.
16. Davidson AJ, Sellix MT, Daniel J., Menaker M., and Block GD (2006) Chronic jet-lag increases mortality in aged mice. Curr Biol 16: R914 - R916.
17. Dong H., Martin MV, Chambers S., and Csermansky JC (2007) Spatial relationship between synapse loss and βamyloid deposition in Tg2576 mice. J Comp Neurol 500: 311-321.
18. Duncan MJ, Herron JM, and Hill SA (2001) Aging selectively suppresses vasoactive intestinal peptide messenger RNA expression in the suprachiasmatic nucleus of Syrian hamster. Mol Brain Res 87: 196-203.
19. Duncan MJ and Wheeler DL (1999) Aging and photoperiod regulate glutamic acid decarboxylase (67) messenger RNA expression. Mol Brain Res 71: 325-331.
20. Esclapez M., Niranjala JK, Kaufman DL, Tobin AJ, and Houser CR (1994) Comparative localization of two forms of glutamic acid decarboxylase and their mRNAs in rat brain supports the concept of functional differences between the forms. J Neurosci 14: 1834-1855.
21. Gao B., Fritschy JM, and Moore RY (1995) GABAA-receptor subunit composition in the circadian timing system. Brain Res 700: 142-156.
22. Gompf HS and Allen CN (2004) GABAergic synapses of the suprachiasmatic nucleus exhibit a diurnal rhythm of short-term synaptic plasticity. Eur J Neurosci 19: 2791-2798.
23. Helfert RH, Krenning J., Wilson TS, and Hughes LF (2003) Age-related synaptic changes in the anteroventral cochlear nucleus of Fischer-344 rats. Hear Res 183: 18-28.
24. Helfert RH, Sommer TJ, Meeks J., Hofstetter P., and Hughes LF (1999) Age-related synaptic changes in the central nucleus of the inferior colliculus of Fischer-344 rats. J Comp Neurol 406: 285-298.
25. Himeda T., Mizuno K., Kato H., and Araki T. (2005) Effects of age on immunohistochemical changes in the mouse hippocampus. Mech Ageing Dev 126: 673-677.
26. Hiscock JJ, Murphy S., and Willoughby JO (2000) Confocal microscopic estimation of GABAergic nerve terminals in the central nervous system. J Neurosci Meth 95: 1-11.
27. Hof PR and Morrison JH (2004) The aging brain: morphomolecular senescence of cortical circuits. Trends Neurosci 27: 607-613.
28. Hofman MA and Swaab DF (2006) Living by the clock: the circadian pacemaker in older people. Ageing Res Rev 5: 33-51.
29. Huhman KL, Hennessey AC, and Albers HE (1996) Rhythms of glutamic acid decarboxylase mRNA in the suprachiasmatic nucleus. J Biol Rhythms 11: 311-316.
30. Huhman KL, Jasnow AM, Sisitsky AK, and Albers HE (1999) Glutamic acid decarboxylase mRNA in the suprachiasmatic nucleus of rats housed in constant darkness. Brain Res 851: 266-269.
31. Jahn R., Schiebler W., Ouimet C., and Greengard PA (1985) A 38,000-dalton membrane protein present in synaptic vesicles. Proc Natl Acad Sci U S A 82: 4137-4141.
32. Jiao Y., Zhang C., Yanagawa Y., and Sur Q.-Q. (2006) Major effects of sensory experiences alter neocortical inhibitory circuits. J Neurosci 26: 8691-8701.
33. Kawakami F., Okamura H., Tamada Y., Maebayashi Y., Fukui K., and Ibata Y. (1997) Loss of day-night differences in VIP mRNA levels in the suprachiasmatic nucleus of aged rats. Neurosci Lett 222: 99-102.
34. King DL and Arendash GW (2002) Maintained synaptophysin immunoreactivity in Tg576 mice during aging: correlations with cognitive impairment. Brain Res 926: 58-68.
35. Kretschmannova K., Svobodova I., and Zemkova H. (2005) Circadian rhythmicity in AVP secretion and GABAergic synaptic transmission in the rat suprachiasmatic nucleus. Ann N Y Acad Sci 1048: 103-115.
36. Liu C. and Reppert SM (2000) GABA synchronizes clock cells within the suprachiasmatic circadian clock. Neuron 25: 123-128.
37. Livak KJ and Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T). method. Methods 25: 402-408.
38. Madeira MD, Sousa N., Santer RM, Paula-Barbosa MM, and Gundersen HJ (1995) Age and sex do not affect the volume, cell numbers, or cell size of the suprachiasmatic nucleus of the rat: an unbiased stereological study. J Comp Neurol 361: 585-601.
39. Majdi M., Ribeiro-da-Silva A., and Cuello AC (2007) Cognitive impairment and transmitter-specific pre- and postsynaptic changes in the rat cerebral cortex during ageing. Eur J Neurosci 26: 3583-3596.
40. Miller MM, Gould BE, and Nelson JF (1989) Aging and long-term ovariectomy alter the cytoarchitecture of the hypothalamic-preoptic area of the C57BL/6J mouse. Neurobiol Aging 10: 683-690.
41. Moore RY and Speh JC (1993) GABA is the principal neurotransmitter of the circadian system. Neurosci Lett 150: 112-116.
42. Morin LP (2007) SCN organization reconsidered. J Biol Rhythms 22: 3-13.
43. Morin LP and Allen CN (2006) The circadian visual system. Brain Res Rev 51: 1-60.
44. Morin LP, Shivers K-Y., Blanchard JH, and Muscat L. (2006) Complex organization of mouse and rat suprachiasmatic nucleus. Neuroscience 137: 1285-1297.
45. Naum OG, Fernanda Rubio M., and Golombek DA (2001) Rhythmic variation in gamma-aminobutyric acid(A)-receptor subunit composition in the circadian system and median eminence of Syrian hamsters. Neurosci Lett 310: 178-182.
46. Nygård M., Hill RH, Wikstrom MA, and Kristensson K. (2005) Age-related changes in electrophysiological properties of the mouse suprachiasmatic nucleus in vitro. Brain Res Bull 65: 149-154.
47. Nygård M. and Palomba M. (2006) The GABAergic network in the suprachiasmatic nucleus as a key regulator of the biological clock: does it change during senescence ? Chronobiol Int 23: 427-435.
48. O' Hara BF, Andretic R., Heller HC, Carter DB, and Kilduff TS (1995) GABAA, GABAC, and NMDA receptor subunit expression in the suprachiasmatic nucleus and other brain regions. Mol Brain Res 2: 239-250.
49. Peters A. (2002) The effects of normal aging on myelin and nerve fibers: a review. J Neurocytol 31: 581-593.
50. Peters A., Moss MB, and Sethares C. (2001) The effects of aging on layer I of primary visual cortex in the rhesus monkey. Cereb Cortex 11: 93-103.
51. Rangarajan R., Heller HC, and Miller JD (1994) Chloride channel block phase advances the single-unit activity rhythm in the SCN. Brain Res Bull 34: 69-72.
52. Sadki A., Bentivoglio M., Kristensson K., and Nygård M. (2007) Suppressors, receptors and effects of cytokines on the aging mouse biological clock. Neurobiol Aging 28: 296-305.
53. Schwartz WJ, Gross RA, and Morton MT (1987) The suprachiasmatic nuclei contain a tetrodotoxin-resistant circadian pacemaker. Proc Natl Acad Sci U S A 84: 1694-1698.
54. Shi L., Argenta AE, Winseck AK, and Brunso-Bechtold JK (2004) Stereological quantification of GAD-67-immunoreactive neurons and boutons in the hippocampus of middle-aged and old Fischer 344 Brown Norway rats. J Comp Neurol 478: 282-291.
55. Tsukahara S., Tanaka S., Ishida K., Hoshi N., and Kitagawa H. (2005) Age-related change and its sex differences in histoarchitecture of the hypothalamic suprachiasmatic nucleus of F344/N rats. Exp Gerontol 40: 147-155.
56. Valentinuzzi VS, Scarbrough K., Takahashi JS, and Turek FW (1997) Effects of aging on the circadian rhythm of wheel-running activity in C57BL/6 mice. Am J Physiol Reg Int Comp Physiol 273: 1957-1964.
57. Wagner S., Castel M., Gainer H., and Yarom Y. (1997) GABA in the mammalian suprachiasmatic nucleus and its role in diurnal rhythmicity. Nature 387: 598-603.
58. Weinert D. (2000) Age-dependent changes of the circadian system. Chronobiol Int 17: 261-283.
59. Wu Y-H. and Swaab DF (2007) Disturbance and strategies for reactivation of the circadian rhythm system in aging and Alzheimer's disease. Sleep Med 8: 623-636.
60. Yamaguchi S., Isejima H., Matsuo T., Okura R., Yagita K., Kobayashi M., and Okamura H. (2003) Synchronization of cellular clocks in the suprachiasmatic nucleus. Science 302: 1408-1412.