The opiate analgesic buprenorphine decreases proliferation of adult hippocampal neuroblasts and increases survival of their progeny

Neuroscience

Volumn 200, Issue , 2012, Pages 211-222

  Pettit, A S ^a   DesRoches, R ^a   Bennett, S A L ^a  

^a UNIVERSITY OF OTTAWA   (Canada)

Author keywords

Analgesia; Buprenorphine; Hippocampus; Neuroblasts; Neurogenesis; Opiate

Indexed keywords

BUPRENORPHINE; DOUBLECORTIN; GLIAL FIBRILLARY ACIDIC PROTEIN; IDOXURIDINE; NESTIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL LABELING; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; DENTATE GYRUS; DOSAGE SCHEDULE COMPARISON; DRUG DOSE REGIMEN; HIPPOCAMPUS; MALE; MOUSE; NEURAL STEM CELL; NEUROBLAST; NONHUMAN; PRIORITY JOURNAL;

ADULT STEM CELLS; ANALGESICS; ANALYSIS OF VARIANCE; ANIMALS; ANTIGENS; BROMODEOXYURIDINE; BUPRENORPHINE; CELL PROLIFERATION; CELL SURVIVAL; DEOXYURIDINE; GLIAL FIBRILLARY ACIDIC PROTEIN; HIPPOCAMPUS; IN SITU NICK-END LABELING; MALE; MICE; MICE, INBRED C57BL; MICROTUBULE-ASSOCIATED PROTEINS; NEUROGENESIS; NEUROGLIA; NEUROPEPTIDES; PHOSPHOPYRUVATE HYDRATASE; PROTEOGLYCANS; TIME FACTORS;

EID: 84855190955     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2011.10.039     Document Type: Article

References (80)

1. Ables J.L., Decarolis N.A., Johnson M.A., Rivera P.D., Gao Z., Cooper D.C., Radtke F., Hsieh J., Eisch A.J. Notch1 is required for maintenance of the reservoir of adult hippocampal stem cells. J Neurosci 2010, 30:10484-10492.
2. Ackermann J., Ashton G., Lyons S., James D., Hornung J.P., Jones N., Breitwieser W. Loss of ATF2 function leads to cranial motoneuron degeneration during embryonic mouse development. PLoS One 2011, 6:e19090.
3. Arguello A.A., Fischer S.J., Schonborn J.R., Markus R.W., Brekken R.A., Eisch A.J. Effect of chronic morphine on the dentate gyrus neurogenic microenvironment. Neuroscience 2009, 159:1003-1010.
4. Arguello A.A., Harburg G.C., Schonborn J.R., Mandyam C.D., Yamaguchi M., Eisch A.J. Time course of morphine's effects on adult hippocampal subgranular zone reveals preferential inhibition of cells in S phase of the cell cycle and a subpopulation of immature neurons. Neuroscience 2008, 157:70-79.
5. Barha C.K., Brummelte S., Lieblich S.E., Galea L.A. Chronic restraint stress in adolescence differentially influences hypothalamic-pituitary-adrenal axis function and adult hippocampal neurogenesis in male and female rats. Hippocampus 2011, 21:1216-1227.
6. Beaudreau S.A., O'Hara R. Late-life anxiety and cognitive impairment: a review. Am J Geriatr Psychiatry 2008, 16:790-803.
7. Ben Abdallah N.M., Slomianka L., Vyssotski A.L., Lipp H.P. Early age-related changes in adult hippocampal neurogenesis in C57 mice. Neurobiol Aging 2010, 31:151-161.
8. Berglund C.M., Aarum J., Haeberlein S.L., Nyengaard J.R., Hökfelt T., Sandberg K., Näslund J., Persson M.A. Characterization of long-term mouse brain aggregating cultures: evidence for maintenance of neural precursor cells. J Comp Neurol 2004, 474:246-260.
9. Bérubé N.G., Mangelsdorf M., Jagla M., Vanderluit J., Garrick D., Gibbons R.J., Higgs D.R., Slack R.S., Picketts D.J. The chromatin-remodeling protein ATRX is critical for neuronal survival during corticogenesis. J Clin Invest 2005, 115:258-267.
10. Blunt D. Statistics of Scientific Procedures on Living Animals 2009, The Stationary Office, London. http://webarchive.nationalarchives.gov.uk/+/http://www.homeoffice.gov.uk/publications/science-research-statistics/research-statistics/science-research/spanimals09/, (HMSO, ed).
11. Bryant H.U., Bernton E.W., Kenner J.R., Holaday J.W. Role of adrenal cortical activation in the immunosuppressive effects of chronic morphine treatment. Endocrinology 1991, 128:3253-3258.
12. Coe C.L., Kramer M., Czéh B., Gould E., Reeves A.J., Kirschbaum C., Fuchs E. Prenatal stress diminishes neurogenesis in the dentate gyrus of juvenile rhesus monkeys. Biol Psychiatry 2003, 54:1025-1034.
13. Coulter C.A., Flecknell P.A., Leach M.C., Richardson C.A. Reported analgesic administration to rabbits undergoing experimental surgical procedures. BMC Vet Res 2011, 7:12.
14. Curtin L.I., Grakowsky J.A., Suarez M., Thompson A.C., DiPirro J.M., Martin L.B., Kristal M.B. Evaluation of buprenorphine in a postoperative pain model in rats. Comp Med 2009, 59:60-71.
15. Davis M.P. What is new in neuropathic pain?. Support Care Cancer 2007, 15:363-372.
16. Deng W., Aimone J.B., Gage F.H. New neurons and new memories: how does adult hippocampal neurogenesis affect learning and memory?. Nat Rev Neurosci 2010, 11:339-350.
17. Dobromylskyi P., Flecknell P., Lascelles B., Pascoe P., Taylor P., Waterman-Pearson A. Management of postoperative and other acute pain. Pain management in animals 2000, 81-147. WB Saunders, London. P.A. Flecknell, A. Waterman-Pearson (Eds.).
18. Doetsch F. The glial identity of neural stem cells. Nat Neurosci 2003, 6:1127-1134.
19. Dolcos F., Strungaru C., Dolcos S.M., Turcu E. The involvement of endogenous opiates in emotional-cognitive interaction in stress. Rom. J Physiol 1998, 35:259-274.
20. Dong H.W., Swanson L.W., Chen L., Fanselow M.S., Toga A.W. Genomic-anatomic evidence for distinct functional domains in hippocampal field CA1. Proc Natl Acad Sci U S A 2009, 106:11794-11799.
21. Dubois N.C., Hofmann D., Kaloulis K., Bishop J.M., Trumpp A. Nestin-Cre transgenic mouse line Nes-Cre1 mediates highly efficient Cre/loxP mediated recombination in the nervous system, kidney, and somite-derived tissues. Genesis 2006, 44:355-360.
22. Eisch A.J., Barrot M., Schad C.A., Self D.W., Nestler E.J. Opiates inhibit neurogenesis in the adult rat hippocampus. Proc Natl Acad Sci U S A 2000, 97:7579-7584.
23. Faden A.I. Neurotoxic versus neuroprotective actions of endogenous opioid peptides: implications for treatment of CNS injury. NIDA Res Monogr 1996, 163:318-330.
24. Fanselow M.S., Dong H.W. Are the dorsal and ventral hippocampus functionally distinct structures?. Neuron 2010, 65:7-19.
25. Gage F.H. Mammalian neural stem cells. Science 2000, 287:1433-1438.
26. Garber J.C., Barbee R.W., Bielitzki J.T., Clayton L.A., Hendriksen C.F.M., Kohn D.F., Lipman N.S., Locke P.A., Melcher J., Quimby F.W., Turner P.V., Wood G.A., Würbel H. Guide for the Care and Use of Laboratory Animals 2011, National Academies Press. http://www.aaalacorg/resources/Guide_2010pdf, 8th ed.
27. Garcia A.D., Doan N.B., Imura T., Bush T.G., Sofroniew M.V. GFAP-expressing progenitors are the principal source of constitutive neurogenesis in adult mouse forebrain. Nat Neurosci 2004, 7:1233-1241.
28. Gebhart G.F., B A.I., Flecknell P., Goodly L., Karas A.Z., Kelley S.T., Lacher K., Mason G., Sneddon L.U., Soriano S.G. Recognition and alleviation of pain in laboratory animals 2009, The National Academies Press. http://www.napedu/catalogphp?record_id=12526.
29. Gomez-Flores R., Weber R.J. Differential effects of buprenorphine and morphine on immune and neuroendocrine functions following acute administration in the rat mesencephalon periaqueductal gray. Immunopharmacology 2000, 48:145-156.
30. Guo F., Maeda Y., Ma J., Xu J., Horiuchi M., Miers L., Vaccarino F., Pleasure D. Pyramidal neurons are generated from oligodendroglial progenitor cells in adult piriform cortex. J Neurosci 2010, 30:12036-12049.
31. Gutstein H.B., Rubie E.A., Mansour A., Akil H., Woodgett J.R. Opioid effects on mitogen-activated protein kinase signaling cascades. Anesthesiology 1997, 87:1118-1126.
32. Hanson N.D., Owens M.J., Boss-Williams K.A., Weiss J.M., Nemeroff C.B. Several stressors fail to reduce adult hippocampal neurogenesis. Psychoneuroendocrinology 2011, 36:1520-1529.
33. Hart R.P., Martelli M.F., Zasler N.D. Chronic pain and neuropsychological functioning. Neuropsychol Rev 2000, 10:131-149.
34. Hart R.P., Wade J.B., Martelli M.F. Cognitive impairment in patients with chronic pain: the significance of stress. Curr Pain Headache Rep 2003, 7:116-126.
35. Hauser K.F., Stiene-Martin A., Mattson M.P., Elde R.P., Ryan S.E., Godleske C.C. mu-Opioid receptor-induced Ca2+ mobilization and astroglial development: morphine inhibits DNA synthesis and stimulates cellular hypertrophy through a Ca (2+)-dependent mechanism. Brain Res 1996, 720:191-203.
36. Hawk T., Leary S.L., Moris T.H. Formulary for Laboratory Animals 2005, Wiley-Blackwell, New York. 3rd ed.
37. Hof P.Y., Bloom F.E., Belichenko P.V., Celio M.R. Comparative cytoarchitectonic Atlas of the C57BL/6 and 129/Sv mouse brains 2001, Elsevier Science, London.
38. Howland R.H. The diverse clinical uses of opioid receptor drugs. J Psychosoc Nurs Ment Health Serv 2010, 48:11-14.
39. Jensen M.L., Sjøgren P., Upton R.N., Foster D.J., Bonde P., Graae C., Skram U., Stevner L., Christrup L.L. Pharmacokinetic-pharmacodynamic relationships of cognitive and psychomotor effects of intravenous buprenorphine infusion in human volunteers. Basic Clin Pharmacol Toxicol 2008, 103:94-101.
40. Kahn L., Alonso G., Normand E., Manzoni O.J. Repeated morphine treatment alters polysialylated neural cell adhesion molecule, glutamate decarboxylase-67 expression and cell proliferation in the adult rat hippocampus. Eur J Neurosci 2005, 21:493-500.
41. Kee N., Teixeira C.M., Wang A.H., Frankland P.W. Preferential incorporation of adult-generated granule cells into spatial memory networks in the dentate gyrus. Nat Neurosci 2007, 10:355-362.
42. Kempermann G., Jessberger S., Steiner B., Kronenberg G. Milestones of neuronal development in the adult hippocampus. Trends Neurosci 2004, 27:447-452.
43. Kheirbek M.A., Hen R. Dorsal vs ventral hippocampal neurogenesis: implications for cognition and mood. Neuropsychopharmacology 2011, 36:373-374.
44. Kronenberg G., Reuter K., Steiner B., Brandt M.D., Jessberger S., Yamaguchi M., Kempermann G. Subpopulations of proliferating cells of the adult hippocampus respond differently to physiologic neurogenic stimuli. J Comp Neurol 2003, 467:455-463.
45. Kugawa F., Ueno A., Aoki M. Apoptosis of NG108-15 cells induced by buprenorphine hydrochloride occurs via the caspase-3 pathway. Biol Pharm Bull 2000, 23:930-935.
46. Learish R.D., Bruss M.D., Haak-Frendscho M. Inhibition of mitogen-activated protein kinase kinase blocks proliferation of neural progenitor cells. Brain Res Dev Brain Res 2000, 122:97-109.
47. Likar R., Lorenz V., Korak-Leiter M., Kager I., Sittl R. Transdermal buprenorphine patches applied in a 4-day regimen versus a 3-day regimen: a single-site, Phase III, randomized, open-label, crossover comparison. Clin Ther 2007, 29:1591-1606.
48. Loftsson T., Jarho P., Másson M., Järvinen T. Cyclodextrins in drug delivery. Expert Opin Drug Deliv 2005, 2:335-351.
49. Martin L.B., Thompson A.C., Martin T., Kristal M.B. Analgesic efficacy of orally administered buprenorphine in rats. Comp Med 2001, 51:43-48.
50. McDermott L.M., Ebmeier K.P. A meta-analysis of depression severity and cognitive function. J Affect Disord 2009, 119:1-8.
51. Melanson-Drapeau L., Beyko S., Davé S., Hebb A.L., Franks D.J., Sellitto C., Paul D.L., Bennett S.A. Oligodendrocyte progenitor enrichment in the connexin32 null-mutant mouse. J Neurosci 2003, 23:1759-1768.
52. Mollereau C., Parmentier M., Mailleux P., Butour J.L., Moisand C., Chalon P., Caput D., Vassart G., Meunier J.C. ORL1, a novel member of the opioid receptor family. Cloning, functional expression and localization. FEBS Lett 1994, 341:33-38.
53. Nowakowski R.S., Lewin S.B., Miller M.W. Bromodeoxyuridine immunohistochemical determination of the lengths of the cell cycle and the DNA-synthetic phase for an anatomically defined population. J Neurocytol 1989, 18:311-318.
54. Olfe J., Domanska G., Schuett C., Kiank C. Different stress-related phenotypes of BALB/c mice from in-house or vendor: alterations of the sympathetic and HPA axis responsiveness. BMC Physiol 2010, 10:2.
55. Olferts E.B., Cross B.M., McWilliam A.A.E. Control of animal pain in research, testing and teaching. Guide to the care and use of experimental animals 1993, Vol. 1. Canadian Council on Animal Care. http://www.ccacca/en/CCAC_Programs/Guidelines_Policies/GUIDES/ENGLISH/V1_93/CHAP/CHXHTM.
56. Ozden S., Isenmann S. Neuroprotective properties of different anesthetics on axotomized rat retinal ganglion cells in vivo. J Neurotrauma 2004, 21:73-82.
57. Panksepp J., Herman B., Conner R., Bishop P., Scott J.P. The biology of social attachments: opiates alleviate separation distress. Biol Psychiatry 1978, 13:607-618.
58. Persson A.I., Thorlin T., Bull C., Eriksson P.S. Opioid-induced proliferation through the MAPK pathway in cultures of adult hippocampal progenitors. Mol Cell Neurosci 2003, 23:360-372.
59. Piersma F.E., Daemen M.A., Bogaard A.E., Buurman W.A. Interference of pain control employing opioids in in vivo immunological experiments. Lab Anim 1999, 33:328-333.
60. Russell W.M.S., Birch R.L. The principles of humane experimental technique 1959, Charles S Thomas, Springfield.
61. Sargeant T.J., Miller J.H., Day D.J. Opioidergic regulation of astroglial/neuronal proliferation: where are we now?. J Neurochem 2008, 107:883-897.
62. Schultz K.M., Banisadr G., Lastra R.O., McGuire T., Kessler J.A., Miller R.J., McGarry T.J. Geminin-deficient neural stem cells exhibit normal cell division and normal neurogenesis. PLoS One 2011, 6:e17736.
63. Shavit Y., Fridel K., Beilin B. Postoperative pain management and proinflammatory cytokines: animal and human studies. J Neuroimmune Pharmacol 2006, 1:443-451.
64. Skyers P.S., Einheber S., Pierce J.P., Milner T.A. Increased mu-opioid receptor labeling is found on inner molecular layer terminals of the dentate gyrus following seizures. Exp Neurol 2003, 179:200-209.
65. Smythe D.H. Alternatives to animal experiments 1978, Scholar Press-Royal Defence Society, London.
66. Song H., Stevens C.F., Gage F.H. Astroglia induce neurogenesis from adult neural stem cells. Nature 2002, 417:39-44.
67. Stokes E.L., Flecknell P.A., Richardson C.A. Reported analgesic and anaesthetic administration to rodents undergoing experimental surgical procedures. Lab Anim 2009, 43:149-154.
68. Tallent M.K., Madamba S.G., Siggins G.R. Nociceptin reduces epileptiform events in CA3 hippocampus via presynaptic and postsynaptic mechanisms. J Neurosci 2001, 21:6940-6948.
69. Taupin P. BrdU immunohistochemistry for studying adult neurogenesis: paradigms, pitfalls, limitations, and validation. Brain Res Rev 2007, 53:198-214.
70. Thallmair M., Ray J., Stallcup W.B., Gage F.H. Functional and morphological effects of NG2 proteoglycan deletion on hippocampal neurogenesis. Exp Neurol 2006, 202:167-178.
71. Urquhart J., Fara J.W., Willis K.L. Rate-controlled delivery systems in drug and hormone research. Annu Rev Pharmacol Toxicol 1984, 24:199-236.
72. Vega C.J., Peterson D.A. Stem cell proliferative history in tissue revealed by temporal halogenated thymidine analog discrimination. Nat Methods 2005, 2:167-169.
73. Wade J.B., Price D.D., Hamer R.M., Schwartz S.M., Hart R.P. An emotional component analysis of chronic pain. Pain 1990, 40:303-310.
74. Winocur G., Wojtowicz J.M., Sekeres M., Snyder J.S., Wang S. Inhibition of neurogenesis interferes with hippocampus-dependent memory function. Hippocampus 2006, 16:296-304.
75. Witta J., Buzas B., Cox B.M. Traumatic brain injury induces nociceptin/orphanin FQ expression in neurons of the rat cerebral cortex. J Neurotrauma 2003, 20:523-532.
76. Yasuda K., Raynor K., Kong H., Breder C.D., Takeda J., Reisine T., Bell G.I. Cloning and functional comparison of kappa and delta opioid receptors from mouse brain. Proc Natl Acad Sci U S A 1993, 90:6736-6740.
77. Yoshiki A., Moriwaki K. Mouse phenome research: implications of genetic background. ILAR J 2006, 47:94-102.
78. Zhao C., Deng W., Gage F.H. Mechanisms and functional implications of adult neurogenesis. Cell 2008, 132:645-660.
79. Zheng H., Zeng Y., Zhang X., Chu J., Loh H.H., Law P.Y. mu-Opioid receptor agonists differentially regulate the expression of miR-190 and NeuroD. Mol Pharmacol 2010, 77:102-109.
80. Zhu C., Gao J., Karlsson N., Li Q., Zhang Y., Huang Z., Li H., Kuhn H.G., Blomgren K. 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 2010, 30:1017-1030.