Introduction of the human AVPR1A gene substantially alters brain receptor expression patterns and enhances aspects of social behavior in transgenic mice

DMM Disease Models and Mechanisms

Volumn 7, Issue 8, 2014, Pages 1013-1022

  Charles, Rhonda ^a   Sakurai, Takeshi ^a   Takahashi, Nagahide ^a   Elder, Gregory A ^a,b   Gama Sosa, Miguel A ^a,b   Young, Larry J ^c   Buxbaum, Joseph D ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Autism; AVPR1A; Humanized mouse; Microsatellite; Social behavior; Species specific

Indexed keywords

VASOPRESSIN RECEPTOR;

AGING; ANIMAL; ANTIBODY SPECIFICITY; BACTERIAL ARTIFICIAL CHROMOSOME; BRAIN; GENETICS; HUMAN; METABOLISM; PHYSIOLOGY; PREPULSE INHIBITION; SENSORY GATING; SOCIAL BEHAVIOR; STARTLE REFLEX; TASK PERFORMANCE; TRANSGENIC MOUSE;

AGING; ANIMALS; BRAIN; CHROMOSOMES, ARTIFICIAL, BACTERIAL; HUMANS; MICE, TRANSGENIC; ORGAN SPECIFICITY; PREPULSE INHIBITION; RECEPTORS, VASOPRESSIN; REFLEX, STARTLE; SENSORY GATING; SOCIAL BEHAVIOR; TASK PERFORMANCE AND ANALYSIS;

EID: 84905861138     PISSN: 17548403     EISSN: 17548411     Source Type: Journal    
DOI: 10.1242/dmm.017053     Document Type: Article

References (55)

1. Albers, H. E. (2012). The regulation of social recognition, social communication and aggression: vasopressin in the social behavior neural network. Horm. Behav. 61, 283-292.
2. Appenrodt, E., Schnabel, R. and Schwarzberg, H. (1998). Vasopressin administration modulates anxiety-related behavior in rats. Physiol. Behav. 64, 543- 547.
3. Bachner-Melman (2005). Linkage between vasopressin receptor AVPR1A promoter region microsatellites and measures of social behavior in humans. J. Individ. Differ. 26, 2-10.
4. Bachner-Melman, R., Dina, C., Zohar, A. H., Constantini, N., Lerer, E., Hoch, S., Sella, S., Nemanov, L., Gritsenko, I., Lichtenberg, P. et al. (2005). AVPR1a and SLC6A4 gene polymorphisms are associated with creative dance performance. PLoS Genet. 1, e42.
5. Bielsky, I. F., Hu, S. B., Szegda, K. L., Westphal, H. and Young, L. J. (2004). Profound impairment in social recognition and reduction in anxiety-like behavior in vasopressin V1a receptor knockout mice. Neuropsychopharmacology 29, 483-493. (Pubitemid 38372087)
6. Bielsky, I. F., Hu, S. B., Ren, X., Terwilliger, E. F. and Young, L. J. (2005a). The V1a vasopressin receptor is necessary and sufficient for normal social recognition: a gene replacement study. Neuron 47, 503-513. (Pubitemid 41149052)
7. Bielsky, I. F., Hu, S. B. and Young, L. J. (2005b). Sexual dimorphism in the vasopressin system: lack of an altered behavioral phenotype in female V1a receptor knockout mice. Behav. Brain Res. 164, 132-136. (Pubitemid 41258166)
8. Braff, D. L., Geyer, M. A. and Swerdlow, N. R. (2001). Human studies of prepulse inhibition of startle: normal subjects, patient groups, and pharmacological studies. Psychopharmacology (Berl.) 156, 234-258. (Pubitemid 32705488)
9. Caldwell, H. K., Lee, H. J., Macbeth, A. H. and Young, W. S., III (2008). Vasopressin: behavioral roles of an "original" neuropeptide. Prog. Neurobiol. 84, 1-24. (Pubitemid 350256874)
10. Donaldson, Z. R. and Young, L. J. (2008). Oxytocin, vasopressin, and the neurogenetics of sociality. Science 322, 900-904.
11. Donaldson, Z. R. and Young, L. J. (2013). The relative contribution of proximal 5? flanking sequence and microsatellite variation on brain vasopressin 1a receptor (Avpr1a) gene expression and behavior. PLoS Genet. 9, e1003729.
12. Dubois-Dauphin, M., Barberis, C. and de Bilbao, F. (1996). Vasopressin receptors in the mouse (Mus musculus) brain: sex-related expression in the medial preoptic area and hypothalamus. Brain Res. 743, 32-39. (Pubitemid 27028753)
13. Ebner, K., Wotjak, C. T., Holsboer, F., Landgraf, R. and Engelmann, M. (1999). Vasopressin released within the septal brain area during swim stress modulates the behavioural stress response in rats. Eur. J. Neurosci. 11, 997-1002.
14. Egashira, N., Tanoue, A., Higashihara, F., Mishima, K., Fukue, Y., Takano, Y., Tsujimoto, G., Iwasaki, K. and Fujiwara, M. (2004). V1a receptor knockout mice exhibit impairment of spatial memory in an eight-arm radial maze. Neurosci. Lett. 356, 195-198. (Pubitemid 38186685)
15. Egashira, N., Tanoue, A., Tsujimoto, G., Mishima, K., Takano, Y., Iwasaki, K. and Fujiwara, M. (2006). [Vasopressin receptor knockout mice as an animal model of psychiatric disorders]. Nihon Shinkei Seishin Yakurigaku Zasshi 26, 101-105.
16. Egashira, N., Tanoue, A., Matsuda, T., Koushi, E., Harada, S., Takano, Y., Tsujimoto, G., Mishima, K., Iwasaki, K. and Fujiwara, M. (2007). Impaired social interaction and reduced anxiety-related behavior in vasopressin V1a receptor knockout mice. Behav. Brain Res. 178, 123-127.
17. Egashira, N., Mishima, K., Iwasaki, K., Nakanishi, H., Oishi, R. and Fujiwara, M. (2009). [Role of vasopressin receptor in psychological and cognitive functions]. Nippon Yakurigaku Zasshi 134, 3-7.
18. Ferris, C. F., Lu, S. F., Messenger, T., Guillon, C. D., Heindel, N., Miller, M., Koppel, G., Robert Bruns, F. and Simon, N. G. (2006). Orally active vasopressin V1a receptor antagonist, SRX251, selectively blocks aggressive behavior. Pharmacol. Biochem. Behav. 83, 169-174.
19. Hammock, E. A. and Young, L. J. (2002). Variation in the vasopressin V1a receptor promoter and expression: implications for inter- and intraspecific variation in social behaviour. Eur. J. Neurosci. 16, 399-402. (Pubitemid 35471856)
20. Hammock, E. A. and Young, L. J. (2004). Functional microsatellite polymorphism associated with divergent social structure in vole species. Mol. Biol. Evol. 21, 1057-1063. (Pubitemid 38658213)
21. Hammock, E. A. and Young, L. J. (2005). Microsatellite instability generates diversity in brain and sociobehavioral traits. Science 308, 1630-1634. (Pubitemid 40807513)
22. Hammock, E. A., Lim, M. M., Nair, H. P. and Young, L. J. (2005). Association of vasopressin 1a receptor levels with a regulatory microsatellite and behavior. Genes Brain Behav. 4, 289-301. (Pubitemid 41002404)
23. Insel, T. R. (2010). The challenge of translation in social neuroscience: a review of oxytocin, vasopressin, and affiliative behavior. Neuron 65, 768-779.
24. Insel, T. R., Wang, Z. X. and Ferris, C. F. (1994). Patterns of brain vasopressin receptor distribution associated with social organization in microtine rodents. J. Neurosci. 14, 5381-5392. (Pubitemid 24279058)
25. Israel, S., Lerer, E., Shalev, I., Uzefovsky, F., Reibold, M., Bachner-Melman, R., Granot, R., Bornstein, G., Knafo, A., Yirmiya, N. et al. (2008). Molecular genetic studies of the arginine vasopressin 1a receptor (AVPR1a) and the oxytocin receptor (OXTR) in human behaviour: from autism to altruism with some notes in between. Prog. Brain Res. 170, 435-449. (Pubitemid 352010246)
26. Johnson, A. E., Audigier, S., Rossi, F., Jard, S., Tribollet, E. and Barberis, C. (1993). Localization and characterization of vasopressin binding sites in the rat brain using an iodinated linear AVP antagonist. Brain Res. 622, 9-16. (Pubitemid 23264941)
27. Kim, S. J., Young, L. J., Gonen, D., Veenstra-VanderWeele, J., Courchesne, R., Courchesne, E., Lord, C., Leventhal, B. L., Cook, E. H., Jr and Insel, T. R. (2002). Transmission disequilibrium testing of arginine vasopressin receptor 1A (AVPR1A) polymorphisms in autism. Mol. Psychiatry 7, 503-507. (Pubitemid 34712902)
28. Knafo, A., Israel, S., Darvasi, A., Bachner-Melman, R., Uzefovsky, F., Cohen, L., Feldman, E., Lerer, E., Laiba, E., Raz, Y. 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. (Pubitemid 351490230)
29. Kohl, S., Heekeren, K., Klosterkötter, J. and Kuhn, J. (2013). Prepulse inhibition in psychiatric disorders - apart from schizophrenia. J. Psychiatr. Res. 47, 445-452.
30. Koshimizu, T. A., Nakamura, K., Egashira, N., Hiroyama, M., Nonoguchi, H. and Tanoue, A. (2012). Vasopressin V1a and V1b receptors: from molecules to physiological systems. Physiol. Rev. 92, 1813-1864.
31. Levin, R., Heresco-Levy, U., Bachner-Melman, R., Israel, S., Shalev, I. and Ebstein, R. P. (2009). Association between arginine vasopressin 1a receptor (AVPR1a) promoter region polymorphisms and prepulse inhibition. Psychoneuroendocrinology 34, 901-908.
32. Liebsch, G., Wotjak, C. T., Landgraf, R. and Engelmann, M. (1996). Septal vasopressin modulates anxiety-related behaviour in rats. Neurosci. Lett. 217, 101-104. (Pubitemid 26358812)
33. Lim, M. M., Wang, Z., Olazábal, D. E., Ren, X., Terwilliger, E. F. and Young, L. J. (2004). Enhanced partner preference in a promiscuous species by manipulating the expression of a single gene. Nature 429, 754-757. (Pubitemid 38833125)
34. Loup, F., Tribollet, E., Dubois-Dauphin, M. and Dreifuss, J. J. (1991). Localization of high-affinity binding sites for oxytocin and vasopressin in the human brain. An autoradiographic study. Brain Res. 555, 220-232.
35. Manning, M., Misicka, A., Olma, A., Bankowski, K., Stoev, S., Chini, B., Durroux, T., Mouillac, B., Corbani, M. and Guillon, G. (2012). Oxytocin and vasopressin agonists and antagonists as research tools and potential therapeutics. J. Neuroendocrinol. 24, 609-628.
36. Meyer-Lindenberg, A., Kolachana, B., Gold, B., Olsh, A., Nicodemus, K. K., Mattay, V., Dean, M. and Weinberger, D. R. (2009). Genetic variants in AVPR1A linked to autism predict amygdala activation and personality traits in healthy humans. Mol. Psychiatry 14, 968-975.
37. Meyer-Lindenberg, A., Domes, G., Kirsch, P. and Heinrichs, M. (2011). Oxytocin and vasopressin in the human brain: social neuropeptides for translational medicine. Nat. Rev. Neurosci. 12, 524-538.
38. Pitkow, L. J., Sharer, C. A., Ren, X., Insel, T. R., Terwilliger, E. F. and Young, L. J. (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. (Pubitemid 32846986)
39. Ring, R. H. (2005). The central vasopressinergic system: examining the opportunities for psychiatric drug development. Curr. Pharm. Des. 11, 205-225.
40. Ryckmans, T. (2010). Modulation of the vasopressin system for the treatment of CNS diseases. Curr. Opin. Drug Discov. Devel. 13, 538-547.
41. Simon, N. G., Guillon, C., Fabio, K., Heindel, N. D., Lu, S. F., Miller, M., Ferris, C. F., Brownstein, M. J., Garripa, C. and Koppel, G. A. (2008). Vasopressin antagonists as anxiolytics and antidepressants: recent developments. Recent Pat. CNS Drug Discov. 3, 77-93.
42. Tansey, K. E., Hill, M. J., Cochrane, L. E., Gill, M., Anney, R. J. and Gallagher, L. (2011). Functionality of promoter microsatellites of arginine vasopressin receptor 1A (AVPR1A): implications for autism. Mol. Autism 2, 3.
43. Tribollet, E., Goumaz, M., Raggenbass, M. and Dreifuss, J. J. (1991). Appearance and transient expression of vasopressin and oxytocin receptors in the rat brain. J. Recept. Res. 11, 333-346.
44. van Londen, L., Goekoop, J. G., van Kempen, G. M., Frankhuijzen- Sierevogel, A. C., Wiegant, V. M., van der Velde, E. A. and De Wied, D. (1997). Plasma levels of arginine vasopressin elevated in patients with major depression. Neuropsychopharmacology 17, 284-292. (Pubitemid 27440650)
45. Vogel, F., Wagner, S., Başkaya, O., Leuenberger, B., Mobascher, A., Dahmen, N., Lieb, K. and Tadić, A. (2012). Variable number of tandem repeat polymorphisms of the arginine vasopressin receptor 1A gene and impulsive aggression in patients with borderline personality disorder. Psychiatr. Genet. 22, 105-106.
46. Volpi, S., Rabadan-Diehl, C. and Aguilera, G. (2004). Vasopressinergic regulation of the hypothalamic pituitary adrenal axis and stress adaptation. Stress 7, 75-83. (Pubitemid 39013697)
47. Walum, H., Westberg, L., Henningsson, S., Neiderhiser, J. M., Reiss, D., Igl, W., Ganiban, J. M., Spotts, E. L., Pedersen, N. L., Eriksson, E. et al. (2008). Genetic variation in the vasopressin receptor 1a gene (AVPR1A) associates with pair-bonding behavior in humans. Proc. Natl. Acad. Sci. USA 105, 14153-14156.
48. Wassink, T. H., Piven, J., Vieland, V. J., Pietila, J., Goedken, R. J., Folstein, S. E. and Sheffield, V. C. (2004). Examination of AVPR1a as an autism susceptibility gene. Mol. Psychiatry 9, 968-972. (Pubitemid 39381961)
49. Wersinger, S. R., Caldwell, H. K., Martinez, L., Gold, P., Hu, S. B. and Young, W. S., III (2007). Vasopressin 1a receptor knockout mice have a subtle olfactory deficit but normal aggression. Genes Brain Behav. 6, 540-551. (Pubitemid 47246220)
50. Yang, S. Y., Cho, S. C., Yoo, H. J., Cho, I. H., Park, M., Kim, B. N., Kim, J. W., Shin, M. S., Park, T. W., Son, J. W. et al. (2010). Association study between single nucleotide polymorphisms in promoter region of AVPR1A and Korean autism spectrum disorders. Neurosci. Lett. 479, 197-200.
51. Yirmiya, N., Rosenberg, C., Levi, S., Salomon, S., Shulman, C., Nemanov, L., Dina, C. and Ebstein, R. P. (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.
52. Young, L. J. and Wang, Z. (2004). The neurobiology of pair bonding. Nat. Neurosci. 7, 1048-1054. (Pubitemid 41184443)
53. Young, L. J., Winslow, J. T., Nilsen, R. and Insel, T. R. (1997). Species differences in V1a receptor gene expression in monogamous and nonmonogamous voles: behavioral consequences. Behav. Neurosci. 111, 599-605. (Pubitemid 27251329)
54. Young, L. J., Nilsen, R., Waymire, K. G., MacGregor, G. R. and Insel, T. R. (1999a). Increased affiliative response to vasopressin in mice expressing the V1a receptor from a monogamous vole. Nature 400, 766-768. (Pubitemid 29399537)
55. Young, L. J., Toloczko, D. and Insel, T. R. (1999b). Localization of vasopressin (V1a) receptor binding and mRNA in the rhesus monkey brain. J. Neuroendocrinol. 11, 291-297. (Pubitemid 29149883)