The Relative Contribution of Proximal 5′ Flanking Sequence and Microsatellite Variation on Brain Vasopressin 1a Receptor (Avpr1a) Gene Expression and Behavior

PLoS Genetics

Volumn 9, Issue 8, 2013, Pages

  Donaldson, Zoe R ^a,b   Young, Larry J ^b  

^a Och Spine at New York Presbyterian Hospitals   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

VASOPRESSIN V1A RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; COPING BEHAVIOR; DNA FLANKING REGION; DNA SEQUENCE; FORCED SWIMMING TEST; GENE EXPRESSION REGULATION; GENE FREQUENCY; GENE FUNCTION; GENE LOCUS; GENETIC ASSOCIATION; GENETIC VARIABILITY; HOMOLOGOUS RECOMBINATION; LEARNING; MALE; MEMORY; MENTAL TASK; MICROSATELLITE MARKER; MOUSE; NONHUMAN; PROTEIN BINDING; PROTEIN LOCALIZATION; RECEPTOR BINDING; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; SOCIAL BEHAVIOR; SPECIES COMPARISON; SPECIES DIFFERENCE; TASK PERFORMANCE; TRANSCRIPTION INITIATION SITE; TRANSCRIPTION REGULATION; VASOPRESSIN 1A RECEPTOR GENE;

5' FLANKING REGION; ANIMALS; ARVICOLINAE; BEHAVIOR, ANIMAL; BRAIN; GENE EXPRESSION; GENE EXPRESSION PROFILING; HOMOLOGOUS RECOMBINATION; HUMANS; MICE; MICROSATELLITE REPEATS; POLYMORPHISM, GENETIC; RECEPTORS, VASOPRESSIN; SPECIES SPECIFICITY;

EID: 84884653467     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003729     Document Type: Article

References (83)

1. Young LJ, Wang Z, (2004) The neurobiology of pair bonding. Nat Neurosci 7: 1048-1054.
2. Phelps SM, Campbell P, Zheng DJ, Ophir AG, (2010) Beating the boojum: comparative approaches to the neurobiology of social behavior. Neuropharmacology 58: 17-28.
3. Renn SC, Aubin-Horth N, Hofmann HA, (2008) Fish and chips: functional genomics of social plasticity in an African cichlid fish. The Journal of experimental biology 211: 3041-3056.
4. Goodson JL, Kelly AM, Kingsbury MA, (2012) Evolving nonapeptide mechanisms of gregariousness and social diversity in birds. Horm Behav 61: 239-250.
5. Fuentes A, (2002) Patterns and Trends in Primate Pair Bonds. International Journal of Primatology 23: 953.
6. Thierry B, Iwaniuk AN, Pellis SM, (2000) The Influence of Phylogeny on the Social Behaviour of Macaques (Primates: Cercopithecidae, genus Macaca). Ethology 106: 713-728.
7. Stern DL, Orgogozo V, (2009) Is genetic evolution predictable? Science 323: 746-751.
8. Preuss TM, Caceres M, Oldham MC, Geschwind DH, (2004) Human brain evolution: insights from microarrays. Nature reviews Genetics 5: 850-860.
9. de Bono M, Bargmann CI, (1998) Natural variation in a neuropeptide Y receptor homolog modifies social behavior and food response in C. elegans. Cell 94: 679-689.
10. Britten RJ, Davidson EH, (1969) Gene Regulation for Higher Cells: A Theory. Science 165: 349-357.
11. Vinces MD, Legendre M, Caldara M, Hagihara M, Verstrepen KJ, (2009) Unstable Tandem Repeats in Promoters Confer Transcriptional Evolvability. Science 324: 1213-1216.
12. Trifonov EN, (1989) The multiple codes of nucleotide sequences. Bulletin of mathematical biology 51: 417-432.
13. King MC, Wilson AC, (1975) Evolution at two levels in humans and chimpanzees. Science 188: 107-116.
14. Hoekstra HE, Coyne JA, (2007) The locus of evolution: evo devo and the genetics of adaptation. Evolution 61: 995-1016.
15. Feder ME, (2007) Evolvability of physiological and biochemical traits: evolutionary mechanisms including and beyond single-nucleotide mutation. The Journal of experimental biology 210: 1653-1660.
16. Fondon JW, (2008) Simple sequence repeats: genetic modulators of brain function and behavior. Trends Neurosci 31: 328-334.
17. Hammock EA, Young LJ, (2005) Microsatellite instability generates diversity in brain and sociobehavioral traits. Science 308: 1630-1634.
18. Engelmann M, Landgraf R, Wotjak CT, (2004) The hypothalamic-neurohypophysial system regulates the hypothalamic-pituitary-adrenal axis under stress: an old concept revisited. Frontiers in neuroendocrinology 25: 132-149.
19. Winslow JT, Hastings N, Carter CS, Harbaugh CR, Insel TR, (1993) A role for central vasopressin in pair bonding in monogamous prairie voles. Nature 365: 545-548.
20. Insel TR, (2010) The challenge of translation in social neuroscience: a review of oxytocin, vasopressin, and affiliative behavior. Neuron 65: 768-779.
21. Meyer-Lindenberg A, Domes G, Kirsch P, Heinrichs M, (2011) Oxytocin and vasopressin in the human brain: social neuropeptides for translational medicine. Nature Reviews Neuroscience 12: 524-538.
22. Caldwell HK, Young III WS (2006) Oxytocin and Vasopressin: Genetics and Behavioural Implications. In: Lim R, editor. Handbook or Neurochemistry and Molecular Neurobiology, 3rd Edition. New York: Springer. pp. 573-607.
23. Donaldson ZR, Young LJ, (2008) Oxytocin, vasopressin, and the neurogenetics of sociality. Science 322: 900-904.
24. Young LJ, Nilsen R, Waymire KG, MacGregor GR, Insel TR, (1999) Increased affiliative response to vasopressin in mice expressing the V1a receptor from a monogamous vole. Nature 400: 766-768.
25. Young LJ, (1999) Frank A. Beach Award. Oxytocin and vasopressin receptors and species-typical social behaviors. Horm Behav 36: 212-221.
26. Young LJ, Winslow JT, Nilsen R, Insel TR, (1997) Species differences in V1a receptor gene expression in monogamous and nonmonogamous voles: behavioral consequences. Behav Neurosci 111: 599-605.
27. Wang Z, Young LJ, Liu Y, Insel TR, (1997) Species differences in vasopressin receptor binding are evident early in development: comparative anatomic studies in prairie and montane voles. J Comp Neurol 378: 535-546.
28. Insel TR, Wang ZX, Ferris CF, (1994) Patterns of brain vasopressin receptor distribution associated with social organization in microtine rodents. J Neurosci 14: 5381-5392.
29. Lim MM, Young LJ, (2004) Vasopressin-dependent neural circuits underlying pair bond formation in the monogamous prairie vole. Neuroscience 125: 35-45.
30. Landgraf R, Frank E, Aldag JM, Neumann ID, Sharer CA, et al. (2003) Viral vector-mediated gene transfer of the vole V1a vasopressin receptor in the rat septum: improved social discrimination and active social behaviour. Eur J Neurosci 18: 403-411.
31. Pitkow LJ, Sharer CA, Ren X, Insel TR, Terwilliger EF, et al. (2001) Facilitation of affiliation and pair-bond formation by vasopressin receptor gene transfer into the ventral forebrain of a monogamous vole. J Neurosci 21: 7392-7396.
32. Gobrogge KL, Liu Y, Young LJ, Wang Z, (2009) Anterior hypothalamic vasopressin regulates pair-bonding and drug-induced aggression in a monogamous rodent. Proc Natl Acad Sci U S A 106: 19144-19149.
33. Barrett CE, Keebaugh AC, Ahern TH, Bass CE, Terwilliger EF, et al. (2013) Variation in vasopressin receptor (Avpr1a) expression creates diversity in behaviors related to monogamy in prairie voles. Horm Behav 63: 518-26.
34. Lim MM, Wang Z, Olazabal DE, Ren X, Terwilliger EF, et al. (2004) Enhanced partner preference in a promiscuous species by manipulating the expression of a single gene. Nature 429: 754-757.
35. Hammock EA, Young LJ, (2004) Functional microsatellite polymorphism associated with divergent social structure in vole species. Mol Biol Evol 21: 1057-1063.
36. Hammock EA, Lim MM, Nair HP, Young LJ, (2005) Association of vasopressin 1a receptor levels with a regulatory microsatellite and behavior. Genes Brain Behav 4: 289-301.
37. Ophir AG, Campbell P, Hanna K, Phelps SM, (2008) Field tests of cis-regulatory variation at the prairie vole avpr1a locus: association with V1aR abundance but not sexual or social fidelity. Horm Behav 54: 694-702.
38. Ebstein RP, Knafo A, Mankuta D, Chew SH, Lai PS, (2012) The contributions of oxytocin and vasopressin pathway genes to human behavior. Horm Behav 61: 359-379.
39. Hopkins WD, Donaldson ZR, Young LJ, (2012) A polymorphic indel containing the RS3 microsatellite in the 5′ flanking region of the vasopressin V1a receptor gene is associated with chimpanzee (Pan troglodytes) personality. Genes, brain, and behavior 11: 552-558.
40. Jarne P, Lagoda PJ, (1996) Microsatellites, from molecules to populations and back. Trends in Ecology & Evolution 11: 424-429.
41. Quandt K, Frech K, Karas H, Wingender E, Werner T, (1995) MatInd and MatInspector: new fast and versatile tools for detection of consensus matches in nucleotide sequence data. Nucleic Acids Res 23: 4878-4884.
42. MGI Mouse SNP Query, Mouse Genome Informatics website, The Jackson Laboratory, Bar Harbor, Maine. http://www.informatics.jax.org/javawi2/servlet/WIFetch?page=snpQF). Accessed May, 2013.
43. Eppig JT, Blake JA, Bult CJ, Kadin JA, Richardson JE, (2012) The Mouse Genome Database (MGD): comprehensive resource for genetics and genomics of the laboratory mouse. Nucleic Acids Res 40: D881-886.
44. Wang Z, Liu Y, Young LJ, Insel TR, (1997) Developmental changes in forebrain vasopressin receptor binding in prairie voles (Microtus ochrogaster) and montane voles (Microtus montanus). Ann N Y Acad Sci 807: 510-513.
45. Bielsky IF, Hu SB, Ren X, Terwilliger EF, Young LJ, (2005) The V1a vasopressin receptor is necessary and sufficient for normal social recognition: a gene replacement study. Neuron 47: 503-513.
46. Ebner K, Wotjak CT, Landgraf R, Engelmann M, (2002) Forced swimming triggers vasopressin release within the amygdala to modulate stress-coping strategies in rats. The European journal of neuroscience 15: 384-388.
47. Yang J, Pan YJ, Yin ZK, Hai GF, Lu L, et al. (2012) Effect of arginine vasopressin on the behavioral activity in the behavior despair depression rat model. Neuropeptides 46: 141-149.
48. Engelmann M, Wotjak CT, Neumann I, Ludwig M, Landgraf R, (1996) Behavioral Consequences of Intracerebral Vasopressin and Oxytocin: Focus on Learning and Memory. Neuroscience & Biobehavioral Reviews 20: 341-358.
49. van Wimersma Greidanus TB, van Ree JM, de Wied D, (1983) Vasopressin and memory. Pharmacol Ther 20: 437-458.
50. Denny CA, Burghardt NS, Schachter DM, Hen R, Drew MR, (2012) 4- to 6-week-old adult-born hippocampal neurons influence novelty-evoked exploration and contextual fear conditioning. Hippocampus 22: 1188-1201.
51. Brown MW, Aggleton JP, (2001) Recognition memory: what are the roles of the perirhinal cortex and hippocampus? Nature Reviews Neuroscience 2: 51-61.
52. Dubrovsky B, Tatarinov A, Gijsbers K, Harris J, Tsiodras A, (2003) Effects of arginine-vasopressin (AVP) on long-term potentiation in intact anesthetized rats. Brain research bulletin 59: 467-472.
53. Chen C, Diaz Brinton RD, Shors TJ, Thompson RF, (1993) Vasopressin induction of long-lasting potentiation of synaptic transmission in the dentate gyrus. Hippocampus 3: 193-203.
54. Cartharius K, Frech K, Grote K, Klocke B, Haltmeier M, et al. (2005) MatInspector and beyond: promoter analysis based on transcription factor binding sites. Bioinformatics 21: 2933-2942.
55. McCarthy M, (2006) Allen Brain Atlas maps 21,000 genes of the mouse brain. Lancet neurology 5: 907-908.
56. Tirosh I, Barkai N, Verstrepen KJ, (2009) Promoter architecture and the evolvability of gene expression. Journal of biology 8: 95.
57. O'Connell LA, Hofmann HA, (2012) Evolution of a vertebrate social decision-making network. Science 336: 1154-1157.
58. Lynch M, Sung W, Morris K, Coffey N, Landry CR, et al. (2008) A genome-wide view of the spectrum of spontaneous mutations in yeast. Proc Natl Acad Sci U S A 105: 9272-9277.
59. Belenky M, Castel M, Young WS, (1992) Ultrastructural immunolocalization of rat oxytocin-neurophysin in transgenic mice expressing the rat oxytocin gene. Brain Res 583: 279-286.
60. Ho MY, Carter DA, Ang HL, Murphy D, (1995) Bovine oxytocin transgenes in mice. Hypothalamic expression, physiological regulation, and interactions with the vasopressin gene. The Journal of Biological Chemistry 270: 27199-27205.
61. Ho MY, Murphy D, (1997) A bovine oxytocin transgene in mice: expression in the female reproductive organs and regulation during pregnancy, parturition and lactation. Molecular and cellular endocrinology 136: 15-21.
62. Young WS, (1990) Cell-specific expression of the rat oxytocin gene in transgenic mice. Journal of Neuroendocrinology 2: 917-925.
63. Venkatesh B, Si-Hoe SL, Murphy D, Brenner S, (1997) Transgenic rats reveal functional conservation of regulatory controls between the Fugu isotocin and rat oxytocin genes. Proceedings of the National Academy of Sciences of the United States of America 94: 12462-12466.
64. Turner LM, Young AR, Rompler H, Schoneberg T, Phelps SM, et al. (2010) Monogamy evolves through multiple mechanisms: evidence from V1aR in deer mice. Molecular biology and evolution 27: 1269-1278.
65. Kashi Y, King D, Soller M, (1997) Simple sequence repeats as a source of quantitative genetic variation. Trends Genet 13: 74-78.
66. Kashi Y, King DG, (2006) Simple sequence repeats as advantageous mutators in evolution. Trends Genet 22: 253-259.
67. Rosso L, Keller L, Kaessmann H, Hammond RL, (2008) Mating system and avpr1a promoter variation in primates. Biology letters 4: 375-378.
68. Curley JP, Jensen CL, Franks B, Champagne FA, (2012) Variation in maternal and anxiety-like behavior associated with discrete patterns of oxytocin and vasopressin 1a receptor density in the lateral septum. Horm Behav 61: 454-461.
69. Fink S, Excoffier L, Heckel G, (2006) Mammalian monogamy is not controlled by a single gene. Proc Natl Acad Sci U S A 103: 10956-10960.
70. Young LJ, Hammock EA, (2007) On switches and knobs, microsatellites and monogamy. Trends Genet 23: 209-212.
71. Donaldson ZR, Kondrashov FA, Putnam A, Bai Y, Stoinski TL, et al. (2008) Evolution of a behavior-linked microsatellite-containing element in the 5′ flanking region of the primate AVPR1A gene. BMC Evol Biol 8: 180.
72. Thibonnier M, Graves MK, Wagner MS, Chatelain N, Soubrier F, et al. (2000) Study of V(1)-vascular vasopressin receptor gene microsatellite polymorphisms in human essential hypertension. J Mol Cell Cardiol 32: 557-564.
73. David DJ, Klemenhagen KC, Holick KA, Saxe MD, Mendez I, et al. (2007) Efficacy of the MCHR1 antagonist N-[3-(1-{[4-(3,4-difluorophenoxy)phenyl]methyl}(4-piperidyl))-4-methylphenyl]-2-m ethylpropanamide (SNAP 94847) in mouse models of anxiety and depression following acute and chronic administration is independent of hippocampal neurogenesis. The Journal of Pharmacology and Experimental Therapeutics 321: 237-248.
74. Knafo A, Israel S, Darvasi A, Bachner-Melman R, Uzefovsky F, et al. (2008) Individual differences in allocation of funds in the dictator game associated with length of the arginine vasopressin 1a receptor RS3 promoter region and correlation between RS3 length and hippocampal mRNA. Genes Brain Behav 7: 266-275.
75. Meyer-Lindenberg A, Kolachana B, Gold B, Olsh A, Nicodemus KK, et al. (2008) Genetic variants in AVPR1A linked to autism predict amygdala activation and personality traits in healthy humans. Mol Psychiatry 14: 968-75.
76. Ebstein RP, (2006) The molecular genetic architecture of human personality: beyond self-report questionnaires. Mol Psychiatry 11: 427-445.
77. Bachner-melman R, Zohar AH, Bacon-Scnoor N, Elizur Y, Nemanov L, et al. (2005) Link between vasopressin receptor AVPR1A promoter region micorsatellites and measures of social behavior in humans. Journal of Individual Differences 26: 2-10.
78. Walum H, Westberg L, Henningsson S, Neiderhiser JM, Reiss D, et al. (2008) Genetic variation in the vasopressin receptor 1a (AVPR1A) associates with pair-bonding behavior in humans. Proceedings of the National Academy of Sciences 105: 14153-14156.
79. Wassink TH, Piven J, Vieland VJ, Pietila J, Goedken RJ, et al. (2004) Examination of AVPR1a as an autism susceptibility gene. Mol Psychiatry 9: 968-972.
80. Yirmiya N, Rosenberg C, Levi S, Salomon S, Shulman C, et al. (2006) Association between the arginine vasopressin 1a receptor (AVPR1a) gene and autism in a family-based study: mediation by socialization skills. Mol Psychiatry 11: 488-494.
81. Kim SJ, Young LJ, Gonen D, Veenstra-VanderWeele J, Courchesne R, et al. (2002) Transmission disequilibrium testing of arginine vasopressin receptor 1A (AVPR1A) polymorphisms in autism. Mol Psychiatry 7: 503-507.
82. Bielsky IF, Hu S-B, Ren X, Terwilliger EF, Young LJ, (2005) The V1a Vasopressin Receptor Is Necessary and Sufficient for Normal Social Recognition: A Gene Replacement Study. Neuron 47: 503-513.
83. Phelps SM, Young LJ, (2003) Extraordinary diversity in vasopressin (V1a) receptor distributions among wild prairie voles (Microtus ochrogaster): patterns of variation and covariation. The Journal of comparative neurology 466: 564-576.