Effects of isoflurane or propofol on postnatal hippocampal neurogenesis in young and aged rats

Brain Research

Volumn 1530, Issue , 2013, Pages 1-12

  Erasso, Diana M ^a   Camporesi, Enrico M ^b,c   Mangar, Devanand ^c   Saporta, Samuel ^a  

^a UNIVERSITY OF SOUTH FLORIDA   (United States)

^b UNIVERSITY OF SOUTH FLORIDA   (United States)

^c TAMPA GENERAL HOSPITAL   (United States)

Author keywords

Hippocampal neurogenesis; Isoflurane; Propofol

Indexed keywords

INTRALIPID; ISOFLURANE; PROPOFOL;

AGE; AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN MATURATION; CELL COUNT; CELL MATURATION; CELL PROLIFERATION; COGNITIVE DEFECT; CONTROLLED STUDY; DRUG EXPOSURE; GENERAL ANESTHESIA; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; LASER MICROSCOPY; MALE; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; RAT;

RATTUS;

HIPPOCAMPAL NEUROGENESIS; ISOFLURANE; PROPOFOL;

AGING; ANESTHESIA, GENERAL; ANESTHETICS, INHALATION; ANIMALS; CELL DIFFERENTIATION; CELL PROLIFERATION; DENTATE GYRUS; HIPPOCAMPUS; ISOFLURANE; MALE; MEMORY; NEUROGENESIS; NEURONS; PROPOFOL; RATS; RATS, INBRED F344;

EID: 84883237704     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2013.07.035     Document Type: Article

References (80)

1. H. Abildstrom, L.S. Rasmussen, P. Rentowl, C.D. Hanning, H. Rasmussen, P.A. Kristensen, and J.T. Moller Cognitive dysfunction 1-2 years after non-cardiac surgery in the elderly. ISPOCD group. International study of post-operative cognitive dysfunction Acta Anaesthesiol. Scand. 44 2000 1246 1251
2. J. Altman, and G.D. Das Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats J. Comp. Neurol. 124 1965 319 335
3. Y. Ben-Ari Excitatory actions of gaba during development: the nature of the nurture. Nature reviews Neuroscience 3 2002 728 739
4. M.J. Berridge Calcium signalling and cell proliferation BioEssays: News Rev Mol Cell Dev Biol 17 1995 491 500
5. J.L. Bizon, and M. Gallagher Production of new cells in the rat dentate gyrus over the lifespan: relation to cognitive decline Eur. J. Neurosci. 18 2003 215 219
6. J.L. Bizon, H.J. Lee, and M. Gallagher Neurogenesis in a rat model of age-related cognitive decline Aging Cell 3 2004 227 234
7. M.A. Bonaguidi, J. Song, G.L. Ming, and H. Song A unifying hypothesis on mammalian neural stem cell properties in the adult hippocampus Curr. Opin. Neurobiol. 22 2012 754 761
8. N.J. Broadbent, L.R. Squire, and R.E. Clark Spatial memory, recognition memory, and the hippocampus Proc. Natl. Acad. Sci. USA 101 2004 14515 14520
9. H.A. Cameron, and R.D. McKay Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus J. Comp. Neurol. 435 2001 406 417
10. J. Canet, J. Raeder, L.S. Rasmussen, M. Enlund, H.M. Kuipers, C.D. Hanning, J. Jolles, K. Korttila, V.D. Siersma, C. Dodds, H. Abildstrom, J.R. Sneyd, P. Vila, T. Johnson, L. Munoz Corsini, J.H. Silverstein, I.K. Nielsen, and J.T. Moller Cognitive dysfunction after minor surgery in the elderly Acta Anaesthesiol. Scand. 47 2003 1204 1210
11. J.P. Cata, B. Abdelmalak, and E. Farag Neurological biomarkers in the perioperative period Br. J. Anaesth. 107 2011 844 858
12. C.D. Clelland, M. Choi, C. Romberg, G.D. Clemenson Jr., A. Fragniere, P. Tyers, S. Jessberger, L.M. Saksida, R.A. Barker, F.H. Gage, and T.J. Bussey A functional role for adult hippocampal neurogenesis in spatial pattern separation Science 325 2009 210 213
13. D.J. Culley, M. Baxter, R. Yukhananov, and G. Crosby The memory effects of general anesthesia persist for weeks in young and aged rats Anesth. Analg. 96 2003 1004 1009 (table of contents)
14. D.J. Culley, M.G. Baxter, C.A. Crosby, R. Yukhananov, and G. Crosby Impaired acquisition of spatial memory 2 weeks after isoflurane and isoflurane-nitrous oxide anesthesia in aged rats Anesth. Analg. 99 2004 1393 1397 (table of contents)
15. D.J. Culley, Z. Xie, and G. Crosby General anesthetic-induced neurotoxicity: an emerging problem for the young and old? Curr. Opin. Anaesthesiol. 20 2007 408 413
16. D.J. Culley, J.D. Boyd, A. Palanisamy, Z. Xie, K. Kojima, C.A. Vacanti, R.E. Tanzi, and G. Crosby Isoflurane decreases self-renewal capacity of rat cultured neural stem cells Anesthesiology 115 2011 754 763
17. W. Deng, M.D. Saxe, I.S. Gallina, and F.H. Gage Adult-born hippocampal dentate granule cells undergoing maturation modulate learning and memory in the brain J. Neuroscience: Off. J. Soc. Neurosci. 29 2009 13532 13542
18. R. Donato Functional roles of S100 proteins, calcium-binding proteins of the EF-hand type Biochim. Biophys. Acta 1450 1999 191 231
19. R. Donato, B.R. Cannon, G. Sorci, F. Riuzzi, K. Hsu, D.J. Weber, and C.L. Geczy Functions of S100 proteins Curr. Mol. Med. 13 2013 24 57
20. Diprivan Inc, A.C., 2004. DIPRIVAN® 1% w/v propofol injection 10 mg/mL.
21. D. Dupret, J.M. Revest, M. Koehl, F. Ichas, F. De Giorgi, P. Costet, D.N. Abrous, and P.V. Piazza Spatial relational memory requires hippocampal adult neurogenesis PLoS One 3 2008 e1959
22. X. Duan, E. Kang, C.Y. Liu, G.L. Ming, and H. Song Development of neural stem cell in the adult brain Curr. Opin. Neurobiol. 18 2008 108 115
23. D.M. Erasso, R.E. Chaparro, C.E. Quiroga Del Rio, R. Karlnoski, E.M. Camporesi, and S. Saporta Quantitative assessment of new cell proliferation in the dentate gyrus and learning after isoflurane or propofol anesthesia in young and aged rats Brain Res. 1441 2012 38 46
24. V. Galvan, and K. Jin Neurogenesis in the aging brain Clin. Interventions Aging 2 2007 605 610
25. F.H. Gage Neurogenesis in the adult brain J Neurosci. 22 2002 612 613
26. S. Ge, D.A. Pradhan, G.L. Ming, and H. Song GABA sets the tempo for activity-dependent adult neurogenesis Trends Neurosci. 30 2007 1 8
27. S. Jessberger, R.E. Clark, N.J. Broadbent, G.D. Clemenson Jr., A. Consiglio, D.C. Lie, L.R. Squire, and F.H. Gage Dentate gyrus-specific knockdown of adult neurogenesis impairs spatial and object recognition memory in adult rats Learn. Mem. 16 2009 147 154
28. V. Jevtovic-Todorovic, R.E. Hartman, Y. Izumi, N.D. Benshoff, K. Dikranian, C.F. Zorumski, J.W. Olney, and D.F. Wozniak Early exposure to common anesthetic agents causes widespread neurodegeneration in the developing rat brain and persistent learning deficits J Neurosci. 23 2003 876 882
29. T. Johnson, T. Monk, L.S. Rasmussen, H. Abildstrom, P. Houx, K. Korttila, H.M. Kuipers, C.D. Hanning, V.D. Siersma, D. Kristensen, J. Canet, M.T. Ibanaz, and J.T. Moller Postoperative cognitive dysfunction in middle-aged patients Anesthesiology 96 2002 1351 1357
30. Kempermann, G., Gage, F.H., 2000. Neurogenesis in the adult hippocampus. In: Proceedings of the Novartis Foundation Symposium, vol. 231, pp. 220-235. (Discussion 235-241, 302-306).
31. G. Kempermann Why new neurons? Possible functions for adult hippocampal neurogenesis J. Neurosci.: Off. J. Soc. Neurosci. 22 2002 635 638
32. G. Kempermann Why new neurons? Possible functions for adult hippocampal neurogenesis J. Neurosci. 22 2002 635 638
33. G. Kempermann Neuronal stem cells and adult neurogenesis Ernst Schering Res. Found. Workshop 2002 17 28
34. G. Kempermann, D. Gast, and F.H. Gage Neuroplasticity in old age: sustained fivefold induction of hippocampal neurogenesis by long-term environmental enrichment Ann. Neurol. 52 2002 135 143
35. G. Kempermann, S. Jessberger, B. Steiner, and G. Kronenberg Milestones of neuronal development in the adult hippocampus Trends Neurosci. 27 2004 447 452
36. Konze, A., 2007. Humane Endpoints (in laboratory animal experimentation).
37. H.G. Kuhn, H. Dickinson-Anson, and F.H. Gage Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation J. Neurosci. 16 1996 2027 2033
38. O. Lazarov, M.P. Mattson, D.A. Peterson, S.W. Pimplikar, and H. van Praag When neurogenesis encounters aging and disease Trends Neurosci. 33 2010 569 579
39. B. Leuner, E. Gould, and T.J. Shors Is there a link between adult neurogenesis and learning? Hippocampus 16 2006 216 224
40. Li, Y., Liang, G., Wang, S., Meng, Q., Wang, Q., Wei, H., 2007. Effects of fetal exposure to isoflurane on postnatal memory and learning in rats. Neuropharmacol. 53, 942-950.
41. G. Liang, Q. Wang, Y. Li, B. Kang, M.F. Eckenhoff, R.G. Eckenhoff, and H. Wei A presenilin-1 mutation renders neurons vulnerable to isoflurane toxicity Anesth. Analg. 106 2008 492 500 (table of contents)
42. A.W. Loepke, and S.G. Soriano An assessment of the effects of general anesthetics on developing brain structure and neurocognitive function Anesth. Analg. 106 2008 1681 1707
43. J.J. LoTurco, D.F. Owens, M.J. Heath, M.B. Davis, and A.R. Kriegstein GABA and glutamate depolarize cortical progenitor cells and inhibit DNA synthesis Neuron 15 1995 1287 1298
44. G.L. Ming, and H. Song Adult neurogenesis in the mammalian central nervous system Annu. Rev. Neurosci. 28 2005 223 250
45. J.T. Moller, P. Cluitmans, L.S. Rasmussen, P. Houx, H. Rasmussen, J. Canet, P. Rabbitt, J. Jolles, K. Larsen, C.D. Hanning, O. Langeron, T. Johnson, P.M. Lauven, P.A. Kristensen, A. Biedler, H. van Beem, O. Fraidakis, J.H. Silverstein, J.E. Beneken, and J.S. Gravenstein Long-term postoperative cognitive dysfunction in the elderly ISPOCD1 study. ISPOCD investigators. International Study of Post-Operative Cognitive Dysfunction Lancet 351 1998 857 861
46. T.G. Monk, B.C. Weldon, C.W. Garvan, D.E. Dede, M.T. van der Aa, K.M. Heilman, and J.S. Gravenstein Predictors of cognitive dysfunction after major noncardiac surgery Anesthesiology 108 2008 18 30
47. M. Moscovitch, R.S. Rosenbaum, A. Gilboa, D.R. Addis, R. Westmacott, C. Grady, M.P. McAndrews, B. Levine, S. Black, G. Winocur, and L. Nadel Functional neuroanatomy of remote episodic, semantic and spatial memory: a unified account based on multiple trace theory J. Anat. 207 2005 35 66
48. P.R. Mouton Principles and Practices of Unbiased Stereology: An Introduction for Bioscientistss 2002 The Johns Hopkins University Press Baltimore, Maryland
49. T. Nakashiba, J.Z. Young, T.J. McHugh, D.L. Buhl, and S. Tonegawa Transgenic inhibition of synaptic transmission reveals role of CA3 output in hippocampal learning Science 319 2008 1260 1264
50. T.D. Palmer, A.R. Willhoite, and F.H. Gage Vascular niche for adult hippocampal neurogenesis J. Comp. Neurol. 425 2000 479 494
51. V.C. Piatti, M.S. Esposito, and A.F. Schinder The timing of neuronal development in adult hippocampal neurogenesis Neurosci.: Rev. J. Bringing Neurobiol. Neurol. Psychiatry 12 2006 463 468
52. A. Pignatelli, and O. Belluzzi Neurogenesis in the Adult Olfactory Bulb A. Menini, The Neurobiology of Olfaction. Frontiers in Neuroscience 2010
53. B.L. Plassman, K.M. Langa, G.G. Fisher, S.G. Heeringa, D.R. Weir, M.B. Ofstedal, J.R. Burke, M.D. Hurd, G.G. Potter, W.L. Rodgers, D.C. Steffens, J.J. McArdle, R.J. Willis, and R.B. Wallace Prevalence of cognitive impairment without dementia in the United States Ann. Intern. Med. 148 2008 427 434
54. J. Popic, V. Pesic, D. Milanovic, S. Todorovic, S. Kanazir, V. Jevtovic-Todorovic, and S. Ruzdijic Propofol-induced changes in neurotrophic signaling in the developing nervous system in vivo PLoS One 7 2012 e34396
55. M. Rothermundt, M. Peters, J.H. Prehn, and V. Arolt S100B in brain damage and neurodegeneration Microsc. Res. Tech. 60 2003 614 632
56. J.W. Sall, G. Stratmann, J. Leong, W. McKleroy, D. Mason, S. Shenoy, S.J. Pleasure, and P.E. Bickler Isoflurane inhibits growth but does not cause cell death in hippocampal neural precursor cells grown in culture Anesthesiology 110 2009 826 833
57. C. Schmitz, and P.R. Hof Design-based stereology in neuroscience Neuroscience 130 2005 813 831
58. B.W. Schafer, and C.W. Heizmann The S100 family of EF-hand calcium-binding proteins: functions and pathology Trends Biochem. Sci. 21 1996 134 140
59. T. Scholzen, and J. Gerdes The Ki-67 protein: from the known and the unknown J. Cell. Physiol. 182 2000 311 322
60. T. Seki, and Y. Arai Age-related production of new granule cells in the adult dentate gyrus Neuroreport 6 1995 2479 2482
61. A. Shruster, E. Melamed, and D. Offen Neurogenesis in the aged and neurodegenerative brain Apoptosis 15 11 2010 1415 1421
62. J. Steiner, H.G. Bernstein, H. Bielau, A. Berndt, R. Brisch, C. Mawrin, G. Keilhoff, and B. Bogerts Evidence for a wide extra-astrocytic distribution of S100B in human brain BMC Neurosci. 8 2007 2
63. J. Steiner, B. Bogerts, M.L. Schroeter, and H.G. Bernstein S100B protein in neurodegenerative disorders Clin. Chem. Lab. Med.: CCLM/FESCC 49 2011 409 424
64. G. Stratmann, J.W. Sall, L.D. May, J.S. Bell, K.R. Magnusson, V. Rau, K.H. Visrodia, R.S. Alvi, B. Ku, M.T. Lee, and R. Dai Isoflurane differentially affects neurogenesis and long-term neurocognitive function in 60-day-old and 7-day-old rats Anesthesiology 110 2009 834 848
65. G. Stratmann, J.W. Sall, J.S. Bell, R.S. Alvi, L.V. May, B. Ku, M. Dowlatshahi, R. Dai, P.E. Bickler, I. Russell, M.T. Lee, M.W. Hrubos, and C. Chiu Isoflurane does not affect brain cell death, hippocampal neurogenesis, or long-term neurocognitive outcome in aged rats Anesthesiology 112 2010 305 315
66. L. Sun Early childhood general anaesthesia exposure and neurocognitive development Br. J. Anaesth. 105 2010 I61 I68
67. S. Sultan, N. Mandairon, F. Kermen, S. Garcia, J. Sacquet, and A. Didier Learning-dependent neurogenesis in the olfactory bulb determines long-term olfactory memory FASEB J.: Off. Publ. Fed. Am. Soc. Exp. Biol. 24 2010 2355 2363
68. A. Tung, S. Herrera, C.A. Fornal, and B.L. Jacobs The effect of prolonged anesthesia with isoflurane, propofol, dexmedetomidine, or ketamine on neural cell proliferation in the adult rat Anesth. Analg. 106 2008 1772 1777
69. H. van Praag, T. Shubert, C. Zhao, and F.H. Gage Exercise enhances learning and hippocampal neurogenesis in aged mice J Neurosci. 25 2005 8680 8685
70. C.J. Vega, and D.A. Peterson Stem cell proliferative history in tissue revealed by temporal halogenated thymidine analog discrimination Nat. Methods 2 2005 167 169
71. Y. Wan, J. Xu, D. Ma, Y. Zeng, M. Cibelli, and M. Maze Postoperative impairment of cognitive function in rats: a possible role for cytokine-mediated inflammation in the hippocampus Anesthesiology 106 2007 436 443
72. X. Wu, Y. Lu, Y. Dong, G. Zhang, Y. Zhang, Z. Xu, D.J. Culley, G. Crosby, E.R. Marcantonio, R.E. Tanzi, and Z. Xie The inhalation anesthetic isoflurane increases levels of proinflammatory TNF-alpha, IL-6, and IL-1beta Neurobiol. Aging 2010
73. G. Xie, W. Zhang, Y. Chang, and Q. Chu Relationship between perioperative inflammatory response and postoperative cognitive dysfunction in the elderly Med. Hypotheses 73 2009 402 403
74. Z. Xie, Y. Dong, U. Maeda, R.D. Moir, W. Xia, D.J. Culley, G. Crosby, and R.E. Tanzi The inhalation anesthetic isoflurane induces a vicious cycle of apoptosis and amyloid beta-protein accumulation J. Neurosci. 27 2007 1247 1254
75. Z. Xie, and Z. Xu General anesthetics and beta-amyloid protein Prog Neuropsychopharmacol Biol Psychiatry 2012
76. D. Yu, Y. Jiang, J. Gao, B. Liu, and P. Chen Repeated exposure to propofol potentiates neuroapoptosis and long-term behavioral deficits in neonatal rats Neurosci. Lett. 534 2013 41 46
77. C. Zeng, F. Pan, L.A. Jones, M.M. Lim, E.A. Griffin, Y.I. Sheline, M.A. Mintun, D.M. Holtzman, and R.H. Mach Evaluation of 5-ethynyl-2′- deoxyuridine staining as a sensitive and reliable method for studying cell proliferation in the adult nervous system Brain Res. 1319 2010 21 32
78. Zhao, Y., Liang, G., Chen, Q., Joseph, D.J., Meng, Q., Eckenhoff, R.G., Eckenhoff, M.F., Wei, H., 2010. Anesthetic-induced neurodegeneration mediated via inositol 1,4,5-trisphosphate receptors. J. Pharmacol. Exp. Ther. 333, 14-22.
79. X. Zhao, Z. Yang, G. Lianq, Z. Wu, Y. Peng, DJ. Joseph, S. Inan, and H. Wei Dual effects of isoflurane on proliferation, differentiation, and survival in human neuroprogenitor cells Anesthesiology 118 2013 537 549
80. Zhu, C., Gao, J., Karlsson, N., Li, Q., Zhang, Y., Huang, Z., Li, H., Kuhn, H.G., Blomgren, K., 2010. Isoflurane anesthesia induced persistent, progressive memory impairment, caused a loss of neural stem cells, and reduced neurogenesis in young, but not adult, rodents. J. Cereb. Blood Flow Metab. 30, 1017-1030