Stress coping stimulates hippocampal neurogenesis in adult monkeys

Proceedings of the National Academy of Sciences of the United States of America

Volumn 107, Issue 33, 2010, Pages 14823-14827

  Lyons, David M ^a   Buckmaster, Paul S ^a   Lee, Alex G ^a   Wu, Christine ^a   Mitra, Rupshi ^a   Duffey, Lauren M ^a   Buckmaster, Christine L ^a   Her, Song ^a,c   Patel, Paresh D ^b   Schatzberg, Alan F ^a  

^a STANFORD UNIVERSITY MEDICAL CENTER   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

^c Korea Basic Science Institute (KBSI)   (South Korea)

Author keywords

Gene expression; Hippocampus; Learning; Neuroplasticity; Resilience

Indexed keywords

HYDROCORTISONE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; COPING BEHAVIOR; FEEDBACK SYSTEM; FOLLOW UP; GENE EXPRESSION; GRANULE CELL; HIPPOCAMPUS; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; LEARNING; MALE; NERVE CELL MEMBRANE POTENTIAL; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; SOCIAL STRESS; SPATIAL MEMORY; SQUIRREL MONKEY; ADAPTIVE BEHAVIOR; ANIMAL; CEBIDAE; CELL PROLIFERATION; CYTOLOGY; DNA MICROARRAY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; IN SITU HYBRIDIZATION; MENTAL STRESS; METABOLISM; NERVE CELL; PATHOPHYSIOLOGY; PHYSIOLOGY; SOCIAL BEHAVIOR;

RODENTIA; SAIMIRI;

ADAPTATION, PSYCHOLOGICAL; ANIMALS; CELL PROLIFERATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HIPPOCAMPUS; HYDROCORTISONE; IN SITU HYBRIDIZATION; LEARNING; MALE; NEUROGENESIS; NEURONS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; SAIMIRI; SOCIAL BEHAVIOR; STRESS, PSYCHOLOGICAL;

EID: 77957088311     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0914568107     Document Type: Article

References (53)

1. Jayatissa MN, Bisgaard C, Tingström A, Papp M, Wiborg O (2006) Hippocampal cytogenesis correlates to escitalopram-mediated recovery in a chronic mild stress rat model of depression. Neuropsychopharmacology 31:2395-2404. (Pubitemid 44607057)
2. Czéh B, et al. (2001) Stress-induced changes in cerebral metabolites, hippocampal volume, and cell proliferation are prevented by antidepressant treatment with tianeptine. Proc Natl Acad Sci USA 98:12796-12801. (Pubitemid 33020024)
3. Coe CL, et al. (2003) Prenatal stress diminishes neurogenesis in the dentate gyrus of juvenile rhesus monkeys. Biol Psychiatry 54:1025-1034.
4. Pham K, Nacher J, Hof PR, McEwen BS (2003) Repeated restraint stress suppresses neurogenesis and induces biphasic PSA-NCAM expression in the adult rat dentate gyrus. Eur J Neurosci 17:879-886. (Pubitemid 36315258)
5. Mirescu C, Gould E (2006) Stress and adult neurogenesis. Hippocampus 16:233-238.
6. Parihar VK, Hattiangady B, Kuruba R, Shuai B, Shetty AK (2009) Predictable chronic mild stress improves mood, hippocampal neurogenesis and memory. Mol Psychiatry, 10.1038/mp.2009.130.
7. Sahay A, Hen R (2007) Adult hippocampal neurogenesis in depression. Nat Neurosci 10:1110-1115.
8. Feder A, Nestler EJ, Charney DS (2009) Psychobiology and molecular genetics of resilience. Nat Rev Neurosci 10:446-457.
9. Rakic P (2002) Neurogenesis in adult primates. Prog Brain Res 138:3-14.
10. Bonanno GA (2004) Loss, trauma, and human resilience: Have we underestimated the human capacity to thrive after extremely aversive events? Am Psychol 59:20-28.
11. Epstein S (1983) Stress Reduction and Prevention, eds Meichenbaum D, Jaremko ME (Plenum Press, New York), pp 39-66.
12. Boinski S, Kauffman L, Ehmke E, Schet S, Vreedzaam A (2005) Dispersal patterns among three species of squirrel monkeys (Saimiri oerstedii, S. boliviensis, and S. sciureus): I. Divergent costs and benefits. Behaviour 142:525-632. (Pubitemid 40946623)
13. Baldwin JD (1992) Agression and Peacefulness in Humans and Other Primates, eds Silverberg J, Gray JP (Oxford University Press, Oxford), pp 72-99.
14. Karssen AM, et al. (2007) Stress-induced changes in primate prefrontal profiles of gene expression. Mol Psychiatry 12:1089-1102.
15. Coe CL, Franklin D, Smith ER, Levine S (1982) Hormonal responses accompanying fear and agitation in the squirrel monkey. Physiol Behav 29:1051-1057. (Pubitemid 13091823)
16. Friedman EM, Coe CL, Ershler WB (1991) Time-dependent effects of peer separation on lymphocyte proliferation responses in juvenile squirrel monkeys. Dev Psychobiol 24:159-173.
17. Lyons DM, Parker KJ, Zeitzer JM, Buckmaster CL, Schatzberg AF (2007) Preliminary evidence that hippocampal volumes in monkeys predict stress levels of adrenocorticotropic hormone. Biol Psychiatry 62:1171-1174.
18. Deng W, Saxe MD, Gallina IS, Gage FH (2009) Adult-born hippocampal dentate granule cells undergoing maturation modulate learning and memory in the brain. J Neurosci 29:13532-13542.
19. Imayoshi I, et al. (2008) Roles of continuous neurogenesis in the structural and functional integrity of the adult forebrain. Nat Neurosci 11:1153-1161.
20. Dupret D, et al. (2008) Spatial relational memory requires hippocampal adult neurogenesis. PLoS One 3:e1959. (Pubitemid 351984392)
21. Zhang CL, Zou Y, He W, Gage FH, Evans RM (2008) A role for adult TLX-positive neural stem cells in learning and behaviour. Nature 451:1004-1007. (Pubitemid 351301727)
22. Overall JE, Doyle SR (1994) Estimating sample sizes for repeated measurement designs. Control Clin Trials 15:100-123.
23. van Praag H, Kempermann G, Gage FH (2000) Neural consequences of environmental enrichment. Nat Rev Neurosci 1:191-198.
24. Kempermann G (2008) The neurogenic reserve hypothesis: What is adult hippocampal neurogenesis good for? Trends Neurosci 31:163-169.
25. Nottebohm F (2002) Neuronal replacement in adult brain. Brain Res Bull 57:737-749.
26. Shors TJ (2008) From stem cells to grandmother cells: How neurogenesis relates to learning and memory. Cell Stem Cell 3:253-258.
27. Ninkovic J, Mori T, Götz M (2007) Distinct modes of neuron addition in adult mouse neurogenesis. J Neurosci 27:10906-10911. (Pubitemid 47535849)
28. Kempermann G, Kuhn HG, Gage FH (1997) More hippocampal neurons in adult mice living in an enriched environment. Nature 386:493-495. (Pubitemid 27164074)
29. Bayer SA, Yackel JW, Puri PS (1982) Neurons in the rat dentate gyrus granular layer substantially increase during juvenile and adult life. Science 216:890-892.
30. Kessels RP, de Haan EH, Kappelle LJ, Postma A (2001) Varieties of human spatial memory: A meta-analysis on the effects of hippocampal lesions. Brain Res Brain Res Rev 35:295-303. (Pubitemid 32566202)
31. Jacobs BL, van Praag H, Gage FH (2000) Adult brain neurogenesis and psychiatry: A novel theory of depression. Mol Psychiatry 5:262-269.
32. Boldrini M, et al. (2009) Antidepressants increase neural progenitor cells in the human hippocampus. Neuropsychopharmacology 34:2376-2389.
33. Perera TD, et al. (2007) Antidepressant-induced neurogenesis in the hippocampus of adult nonhuman primates. J Neurosci 27:4894-4901.
34. Gould E, Vail N, Wagers M, Gross CG (2001) Adult-generated hippocampal and neocortical neurons in macaques have a transient existence. Proc Natl Acad Sci USA 98:10910-10917. (Pubitemid 32878718)
35. 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.
36. Dayer AG, Ford AA, Cleaver KM, Yassaee M, Cameron HA (2003) Short-term and long-term survival of new neurons in the rat dentate gyrus. J Comp Neurol 460:563-572.
37. Kempermann G, Gast D, Kronenberg G, Yamaguchi M, Gage FH (2003) Early determination and long-term persistence of adult-generated new neurons in the hippocampus of mice. Development 130:391-399.
38. Li XC, Jarvis ED, Alvarez-Borda B, Lim DA, Nottebohm F (2000) A relationship between behavior, neurotrophin expression, and new neuron survival. Proc Natl Acad Sci USA 97:8584-8589.
39. Rossi C, et al. (2006) Brain-derived neurotrophic factor (BDNF) is required for the enhancement of hippocampal neurogenesis following environmental enrichment. Eur J Neurosci 24:1850-1856.
40. Newton SS, et al. (2003) Gene profile of electroconvulsive seizures: Induction of neurotrophic and angiogenic factors. J Neurosci 23:10841-10851.
41. Newton SS, Collier EF, Bennett AH, Russell DS, Duman RS (2004) Regulation of growth factor receptor bound 2 by electroconvulsive seizure. Brain Res Mol Brain Res 129: 185-188.
42. Bondy CA, Cheng CM (2004) Signaling by insulin-like growth factor 1 in brain. Eur J Pharmacol 490:25-31.
43. Schlett K (2006) Glutamate as a modulator of embryonic and adult neurogenesis. Curr Top Med Chem 6:949-960.
44. Lin CI, et al. (2001) Modulation of the neuronal glutamate transporter EAAC1 by the interacting protein GTRAP3-18. Nature 410:84-88.
45. Lavreysen H, Dautzenberg FM (2008) Therapeutic potential of group III metabotropic glutamate receptors. Curr Med Chem 15:671-684.
46. Brognard J, Sierecki E, Gao T, Newton AC (2007) PHLPP and a second isoform, PHLPP2, differentially attenuate the amplitude of Akt signaling by regulating distinct Akt isoforms. Mol Cell 25:917-931.
47. Shimizu K, Phan T, Mansuy IM, Storm DR (2007) Proteolytic degradation of SCOP in the hippocampus contributes to activation of MAP kinase and memory. Cell 128: 1219-1229.
48. Bräuer AU, Nitsch R (2008) Plasticity-related genes (PRGs/LRPs): A brain-specific class of lysophospholipid-modifying proteins. Biochim Biophys Acta 1781:595-600.
49. Matas-Rico E, et al. (2008) Deletion of lysophosphatidic acid receptor LPA1 reduces neurogenesis in the mouse dentate gyrus. Mol Cell Neurosci 39:342-355.
50. Li C, Wong WH (2001) Model-based analysis of oligonucleotide arrays: Expression index computation and outlier detection. Proc Natl Acad Sci USA 98:31-36.
51. Karssen AM, et al. (2006) Application of microarray technology in primate behavioral neuroscience research. Methods 38:227-234.
52. Patel PD, Katz M, Karssen AM, Lyons DM (2008) Stress-induced changes in corticosteroid receptor expression in primate hippocampus and prefrontal cortex. Psychoneuroendocrinology 33:360-367.
53. Gergen JA, MacLean PD (1962) A Stereotaxic Atlas of the Squirrel Monkey's Brain (Saimiri sciureus) (Public Health Service, Bethesda).