Evaluation of heritable determinants of blood and brain serotonin homeostasis using recombinant inbred mice

Genes, Brain and Behavior

Volumn 13, Issue 3, 2014, Pages 247-260

  Ye, R ^a   Carneiro, A M D ^a   Airey, D ^a   Sanders Bush, E ^a   Williams, R W ^b   Lu, L ^b   Wang, J ^c   Zhang, B ^c   Blakely, R D ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

^c Department of Biomedical Informatics ^*  (United States)

Author keywords

Blood; Brain; BXD; Genetics; Heritability; Metabolism; Mouse; Neurochemistry; Serotonin; Transcriptome

Indexed keywords

5 HYDROXYINDOLEACETIC ACID; MESSENGER RNA; SEROTONIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD; BRAIN REGION; BRAIN TISSUE; CAUSAL ATTRIBUTION; CONTROLLED STUDY; CROSS BREEDING; DIENCEPHALON; FEMALE; GENDER; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENETIC VARIABILITY; GENOMICS; HERITABILITY; HOMEOSTASIS; HYPOTHALAMUS; INBRED MOUSE STRAIN; MALE; MESENCEPHALON; MOUSE; NEUROCHEMISTRY; NONHUMAN; OVERLAPPING GENE; PARENT; PHENOTYPE; PHENOTYPIC VARIATION; PRIORITY JOURNAL; RNA ISOLATION; SEROTONIN BLOOD LEVEL; SEROTONIN BRAIN LEVEL; SEROTONIN METABOLISM; SIGNAL TRANSDUCTION; THALAMUS;

MUS;

BLOOD; BRAIN; BXD; GENETICS; HERITABILITY; METABOLISM; MOUSE; NEUROCHEMISTRY; SEROTONIN; TRANSCRIPTOME;

ANIMALS; BRAIN; HOMEOSTASIS; INBREEDING; MICE; MICE, INBRED C57BL; MICE, INBRED DBA; ORGAN SPECIFICITY; PHENOTYPE; QUANTITATIVE TRAIT LOCI; SEROTONIN; SEX FACTORS;

EID: 84896735007     PISSN: 16011848     EISSN: 1601183X     Source Type: Journal    
DOI: 10.1111/gbb.12092     Document Type: Article

References (77)

1. Alagramam, K.N., Murcia, C.L., Kwon, H.Y., Pawlowski, K.S., Wright, C.G. & Woychik, R.P. (2001a) The mouse Ames waltzer hearing-loss mutant is caused by mutation of Pcdh15, a novel protocadherin gene. Nat Genet 27, 99-102.
2. Alagramam, K.N., Yuan, H., Kuehn, M.H., Murcia, C.L., Wayne, S., Srisailpathy, C.R., Lowry, R.B., Knaus, R., Van Laer, L., Bernier, F.P., Schwartz, S., Lee, C., Morton, C.C., Mullins, R.F., Ramesh, A., Van Camp, G., Hageman, G.S., Woychik, R.P. & Smith, R.J. (2001b) Mutations in the novel protocadherin PCDH15 cause Usher syndrome type 1F. Hum Mol Genet 10, 1709-1718.
3. Anderson, A.D., Oquendo, M.A., Parsey, R.V., Milak, M.S., Campbell, C. & Mann, J.J. (2004) Regional brain responses to serotonin in major depressive disorder. J Affect Disord 82, 411-417.
4. Arias, B., Catalan, R., Gasto, C., Gutierrez, B. & Fananas, L. (2003) 5-HTTLPR polymorphism of the serotonin transporter gene predicts non-remission in major depression patients treated with citalopram in a 12-weeks follow up study. J Clin Psychopharmacol 23, 563-567.
5. Ayada, K., Tadano, T. & Endo, Y. (2002) Gnawing behavior of a mouse in a narrow cylinder: a simple system for the study of muscle activity, fatigue, and stress. Physiol Behav 77, 161-166.
6. Barnes, N.M. & Sharp, T. (1999) A review of central 5-HT receptors and their function. Neuropharmacology 38, 1083-1152.
7. Barondes, S.H. (1994) Thinking about Prozac. Science 263, 1102-1103.
8. Barr, L.C., Goodman, W.K., McDougle, C.J., Delgado, P.L., Heninger, G.R., Charney, D.S. & Price, L.H. (1994) Tryptophan depletion in patients with obsessive-compulsive disorder who respond to serotonin reuptake inhibitors. Arch Gen Psychiatry 51, 309-317.
9. Barton, D.A., Esler, M.D., Dawood, T., Lambert, E.A., Haikerwal, D., Brenchley, C., Socratous, F., Hastings, J., Guo, L., Wiesner, G., Kaye, D.M., Bayles, R., Schlaich, M.P. & Lambert, G.W. (2008) Elevated brain serotonin turnover in patients with depression: effect of genotype and therapy. Arch Gen Psychiatry 65, 38-46.
10. Bonnin, A., Torii, M., Wang, L., Rakic, P. & Levitt, P. (2007) Serotonin modulates the response of embryonic thalamocortical axons to netrin-1. Nat Neurosci 10, 588-597.
11. Bonnin, A., Goeden, N., Chen, K., Wilson, M.L., King, J., Shih, J.C., Blakely, R.D., Deneris, E.S. & Levitt, P. (2011) A transient placental source of serotonin for the fetal forebrain. Nature 472, 347-350.
12. Carneiro, A.M., Airey, D.C., Thompson, B., Zhu, C.B., Lu, L., Chesler, E.J., Erikson, K.M. & Blakely, R.D. (2009) Functional coding variation in recombinant inbred mouse lines reveals multiple serotonin transporter-associated phenotypes. Proc Natl Acad Sci U S A 106, 2047-2052.
13. Caspi, A., McClay, J., Moffitt, T.E., Mill, J., Martin, J., Craig, I.W., Taylor, A. & Poulton, R. (2002) Role of genotype in the cycle of violence in maltreated children. Science 297, 851-854.
14. Caspi, A., Sugden, K., Moffitt, T.E., Taylor, A., Craig, I.W., Harrington, H., McClay, J., Mill, J., Martin, J., Braithwaite, A. & Poulton, R. (2003) Influence of life stress on depression: moderation by a polymorphism in the 5-HTT gene. Science 301, 386-389.
15. Chen, K., Wu, H.F. & Shih, J.C. (1993) The deduced amino acid sequences of human platelet and frontal cortex monoamine oxidase B are identical. J Neurochem 61, 187-190.
16. Cook, E.H. & Leventhal, B.L. (1996) The serotonin system in autism. Curr Opin Pediatr 8, 348-354.
17. Cross, S., Kim, S.J., Weiss, L.A., Delahanty, R.J., Sutcliffe, J.S., Leventhal, B.L., Cook, E.H. Jr. & Veenstra-Vanderweele, J. (2008) Molecular genetics of the platelet serotonin system in first-degree relatives of patients with autism. Neuropsychopharmacology 33, 353-360.
18. Cryan, J.F., Mombereau, C. & Vassout, A. (2005) The tail suspension test as a model for assessing antidepressant activity: review of pharmacological and genetic studies in mice. Neurosci Biobehav Rev 29, 571-625.
19. Curzon, G. (1990) Serotonin and appetite. Ann N Y Acad Sci 600, 521-530 discussion 530-521.
20. Dawson, N., Ferrington, L., Olverman, H.J., Harmar, A.J. & Kelly, P.A. (2009) Sex influences the effect of a lifelong increase in serotonin transporter function on cerebral metabolism. J Neurosci Res 87, 2375-2385.
21. Delgado, P.L., Charney, D.S., Price, L.H., Aghajanian, G.K., Landis, H. & Heninger, G.R. (1990) Serotonin function and the mechanism of antidepressant action. Reversal of antidepressant-induced remission by rapid depletion of plasma tryptophan. Arch Gen Psychiatry 47, 411-418.
22. Dupuis, J. & Siegmund, D. (1999) Statistical methods for mapping quantitative trait loci from a dense set of markers. Genetics 151, 373-386.
23. Flood, Z.C., Engel, D.L., Simon, C.C., Negherbon, K.R., Murphy, L.J., Tamavimok, W., Anderson, G.M. & Janusonis, S. (2012) Brain growth trajectories in mouse strains with central and peripheral serotonin differences: relevance to autism models. Neuroscience 210, 286-295.
24. Gershon, M.D. (2013) 5-Hydroxytryptamine (serotonin) in the gastrointestinal tract. Curr Opin Endocrinol Diabetes Obes 20, 14-21.
25. Gjerris, A., Sorensen, A.S., Rafaelsen, O.J., Werdelin, L., Alling, C. & Linnoila, M. (1987) 5-HT and 5-HIAA in cerebrospinal fluid in depression. J Affect Disord 12, 13-22.
26. Hawrylycz, M., Ng, L., Page, D., Morris, J., Lau, C., Faber, S., Faber, V., Sunkin, S., Menon, V., Lein, E. & Jones, A. (2011) Multi-scale correlation structure of gene expression in the brain. Neural Netw 24, 933-942.
27. Hegmann, J.P. & Possidente, B. (1981) Estimating genetic correlations from inbred strains. Behav Genet 11, 103-114.
28. Houtkooper, R.H., Mouchiroud, L., Ryu, D., Moullan, N., Katsyuba, E., Knott, G., Williams, R.W. & Auwerx, J. (2013) Mitonuclear protein imbalance as a conserved longevity mechanism. Nature 497, 451-457.
29. Hugot, J.P., Chamaillard, M., Zouali, H., Lesage, S., Cezard, J.P., Belaiche, J., Almer, S., Tysk, C., O'Morain, C.A., Gassull, M., Binder, V., Finkel, Y., Cortot, A., Modigliani, R., Laurent-Puig, P., Gower-Rousseau, C., Macry, J., Colombel, J.F., Sahbatou, M. & Thomas, G. (2001) Association of NOD2 leucine-rich repeat variants with susceptibility to Crohn's disease. Nature 411, 599-603.
30. Jahng, J.W., Houpt, T.A., Wessel, T.C., Chen, K., Shih, J.C. & Joh, T.H. (1997) Localization of monoamine oxidase A and B mRNA in the rat brain by in situ hybridization. Synapse 25, 30-36.
31. Janusonis, S., Gluncic, V. & Rakic, P. (2004) Early serotonergic projections to Cajal-Retzius cells: relevance for cortical development. J Neurosci 24, 1652-1659.
32. Karg, K., Burmeister, M., Shedden, K. & Sen, S. (2011) The serotonin transporter promoter variant (5-HTTLPR), stress, and depression meta-analysis revisited: evidence of genetic moderation. Arch Gen Psychiatry 68, 444-454.
33. Katori, S., Hamada, S., Noguchi, Y., Fukuda, E., Yamamoto, T., Yamamoto, H., Hasegawa, S. & Yagi, T. (2009) Protocadherin-alpha family is required for serotonergic projections to appropriately innervate target brain areas. J Neurosci 29, 9137-9147.
34. Lander, E.S. & Botstein, D. (1989) Mapping Mendelian factors underlying quantitative traits using RFLP linkage maps. Genetics 121, 185-199.
35. Lander, E. & Kruglyak, L. (1995) Genetic dissection of complex traits: guidelines for interpreting and reporting linkage results. Nat Genet 11, 241-247.
36. de Lecea, L., Kilduff, T.S., Peyron, C., Gao, X., Foye, P.E., Danielson, P.E., Fukuhara, C., Battenberg, E.L., Gautvik, V.T., Bartlett, F.S. II, Frankel, W.N., van den Pol, A.N., Bloom, F.E., Gautvik, K.M. & Sutcliffe, J.G. (1998) The hypocretins: hypothalamus-specific peptides with neuroexcitatory activity. Proc Natl Acad Sci U S A 95, 322-327.
37. Lelli, A., Kazmierczak, P., Kawashima, Y., Muller, U. & Holt, J.R. (2010) Development and regeneration of sensory transduction in auditory hair cells requires functional interaction between cadherin-23 and protocadherin-15. J Neurosci 30, 11259-11269.
38. Lenders, J.W., Eisenhofer, G., Abeling, N.G., Berger, W., Murphy, D.L., Konings, C.H., Wagemakers, L.M., Kopin, I.J., Karoum, F., van Gennip, A.H. & Brunner, H.G. (1996) Specific genetic deficiencies of the A and B isoenzymes of monoamine oxidase are characterized by distinct neurochemical and clinical phenotypes. J Clin Invest 97, 1010-1019.
39. Lesch, K.P., Bengel, D., Heils, A., Sabol, S.Z., Greenberg, B.D., Petri, S., Benjamin, J., Muller, C.R., Hamer, D.H. & Murphy, D.L. (1996) Association of anxiety-related traits with a polymorphism in the serotonin transporter gene regulatory region. Science 274, 1527-1531.
40. Lu, L., Wei, L., Peirce, J.L., Wang, X., Zhou, J., Homayouni, R., Williams, R.W. & Airey, D.C. (2008) Using gene expression databases for classical trait QTL candidate gene discovery in the BXD recombinant inbred genetic reference population: mouse forebrain weight. BMC Genomics 9, 444.
41. Mann, J.J., McBride, P.A., Brown, R.P., Linnoila, M., Leon, A.C., DeMeo, M., Mieczkowski, T., Myers, J.E. & Stanley, M. (1992) Relationship between central and peripheral serotonin indexes in depressed and suicidal psychiatric inpatients. Arch Gen Psychiatry 49, 442-446.
42. Marazziti, D., Rossi, A., Giannaccini, G., Baroni, S., Lucacchini, A. & Cassano, G.B. (1998) Presence and characterization of the serotonin transporter in human resting lymphocytes. Neuropsychopharmacology 19, 154-159.
43. Mazer, C., Muneyyirci, J., Taheny, K., Raio, N., Borella, A. & Whitaker-Azmitia, P. (1997) Serotonin depletion during synaptogenesis leads to decreased synaptic density and learning deficits in the adult rat: a possible model of neurodevelopmental disorders with cognitive deficits. Brain Res 760, 68-73.
44. Miceli-Richard, C., Lesage, S., Rybojad, M., Prieur, A.M., Manouvrier-Hanu, S., Hafner, R., Chamaillard, M., Zouali, H., Thomas, G. & Hugot, J.P. (2001) CARD15 mutations in Blau syndrome. Nat Genet 29, 19-20.
45. Munro, C.A., Workman, C.I., Kramer, E., Hermann, C., Ma, Y., Dhawan, V., Chaly, T., Eidelberg, D. & Smith, G.S. (2012) Serotonin modulation of cerebral glucose metabolism: sex and age effects. Synapse 66, 955-964.
46. Ogura, Y., Bonen, D.K., Inohara, N., Nicolae, D.L., Chen, F.F., Ramos, R., Britton, H., Moran, T., Karaliuskas, R., Duerr, R.H., Achkar, J.P., Brant, S.R., Bayless, T.M., Kirschner, B.S., Hanauer, S.B., Nunez, G. & Cho, J.H. (2001) A frameshift mutation in NOD2 associated with susceptibility to Crohn's disease. Nature 411, 603-606.
47. Paulmann, N., Grohmann, M., Voigt, J.P., Bert, B., Vowinckel, J., Bader, M., Skelin, M., Jevsek, M., Fink, H., Rupnik, M. & Walther, D.J. (2009) Intracellular serotonin modulates insulin secretion from pancreatic beta-cells by protein serotonylation. PLoS Biol 7, e1000229.
48. Peirce, J.L., Lu, L., Gu, J., Silver, L.M. & Williams, R.W. (2004) A new set of BXD recombinant inbred lines from advanced intercross populations in mice. BMC Genet 5, 7.
49. Pietraszek, M.H., Takada, Y., Yan, D., Urano, T., Serizawa, K. & Takada, A. (1992) Relationship between serotonergic measures in periphery and the brain of mouse. Life Sci 51, 75-82.
50. Pineyro, G., Castanon, N., Hen, R. & Blier, P. (1995) Regulation of [3H]5-HT release in raphe, frontal cortex and hippocampus of 5-HT1B knock-out mice. Neuroreport 7, 353-359.
51. Pollock, B.G., Ferrell, R.E., Mulsant, B.H., Mazumdar, S., Miller, M., Sweet, R.A., Davis, S., Kirshner, M.A., Houck, P.R., Stack, J.A., Reynolds, C.F. & Kupfer, D.J. (2000) Allelic variation in the serotonin transporter promoter affects onset of paroxetine treatment response in late-life depression. Neuropsychopharmacology 23, 587-590.
52. Prasad, H.C., Zhu, C.B., McCauley, J.L., Samuvel, D.J., Ramamoorthy, S., Shelton, R.C., Hewlett, W.A., Sutcliffe, J.S. & Blakely, R.D. (2005) Human serotonin transporter variants display altered sensitivity to protein kinase G and p38 mitogen-activated protein kinase. Proc Natl Acad Sci U S A 102, 11545-11550.
53. Rainero, I., Ostacoli, L., Rubino, E., Gallone, S., Picci, L.R., Fenoglio, P., Negro, E., Rosso, C., De Martino, P., De Marchi, M., Furlan, P.M. & Pinessi, L. (2011) Association between major mood disorders and the hypocretin receptor 1 gene. J Affect Disord 130, 487-491.
54. Rand, M. & Reid, G. (1951) Source of 'serotonin' in serum. Nature 168, 385.
55. Risch, N., Herrell, R., Lehner, T., Liang, K.Y., Eaves, L., Hoh, J., Griem, A., Kovacs, M., Ott, J. & Merikangas, K.R. (2009) Interaction between the serotonin transporter gene (5-HTTLPR), stressful life events, and risk of depression: a meta-analysis. JAMA 301, 2462-2471.
56. Saito, M., Yamagata, T., Matsumoto, A., Shiba, Y., Nagashima, M., Taniguchi, S., Jimbo, E. & Momoi, M.Y. (2013) MAOA/B deletion syndrome in male siblings with severe developmental delay and sudden loss of muscle tonus. Brain Dev (in press).
57. Sakurai, T., Amemiya, A., Ishii, M. et al. (1998) Orexins and orexin receptors: a family of hypothalamic neuropeptides and G protein-coupled receptors that regulate feeding behavior. Cell 92, 573-585.
58. Santarelli, L., Saxe, M., Gross, C., Surget, A., Battaglia, F., Dulawa, S., Weisstaub, N., Lee, J., Duman, R., Arancio, O., Belzung, C. & Hen, R. (2003) Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 301, 805-809.
59. Schain, R.J. & Freedman, D.X. (1961) Studies on 5-hydroxyindole metabolism in autistic and other mentally retarded children. J Pediatr 58, 315-320.
60. Scott, M.M., Marcus, J.N., Pettersen, A., Birnbaum, S.G., Mochizuki, T., Scammell, T.E., Nestler, E.J., Elmquist, J.K. & Lutter, M. (2011) Hcrtr1 and 2 signaling differentially regulates depression-like behaviors. Behav Brain Res 222, 289-294.
61. Serretti, A., Kato, M., De Ronchi, D. & Kinoshita, T. (2007) Meta-analysis of serotonin transporter gene promoter polymorphism (5-HTTLPR) association with selective serotonin reuptake inhibitor efficacy in depressed patients. Mol Psychiatry 12, 247-257.
62. Stamford, J.A., Davidson, C., McLaughlin, D.P. & Hopwood, S.E. (2000) Control of dorsal raphe 5-HT function by multiple 5-HT(1) autoreceptors: parallel purposes or pointless plurality? Trends Neurosci 23, 459-465.
63. Steinbusch, H.W. (1981) Distribution of serotonin-immunoreactivity in the central nervous system of the rat-cell bodies and terminals. Neuroscience 6, 557-618.
64. Strober, W. & Watanabe, T. (2011) NOD2, an intracellular innate immune sensor involved in host defense and Crohn's disease. Mucosal Immunol 4, 484-495.
65. Sullivan, G.M., Oquendo, M.A., Huang, Y.Y. & Mann, J.J. (2006) Elevated cerebrospinal fluid 5-hydroxyindoleacetic acid levels in women with comorbid depression and panic disorder. Int J Neuropsychopharmacol 9, 547-556.
66. Taylor, B.A., Bedigian, H.G. & Meier, H. (1977) Genetic studies of the Fv-1 locus of mice: linkage with Gpd-1 in recombinant inbred lines. J Virol 23, 106-109.
67. Taylor, B.A., Wnek, C., Kotlus, B.S., Roemer, N., MacTaggart, T. & Phillips, S.J. (1999) Genotyping new BXD recombinant inbred mouse strains and comparison of BXD and consensus maps. Mamm Genome 10, 335-348.
68. Visscher, P.M., Thompson, R. & Haley, C.S. (1996) Confidence intervals in QTL mapping by bootstrapping. Genetics 143, 1013-1020.
69. Walther, D.J., Peter, J.U., Bashammakh, S., Hortnagl, H., Voits, M., Fink, H. & Bader, M. (2003a) Synthesis of serotonin by a second tryptophan hydroxylase isoform. Science 299, 76.
70. Walther, D.J., Peter, J.U., Winter, S., Holtje, M., Paulmann, N., Grohmann, M., Vowinckel, J., Alamo-Bethencourt, V., Wilhelm, C.S., Ahnert-Hilger, G. & Bader, M. (2003b) Serotonylation of small GTPases is a signal transduction pathway that triggers platelet alpha-granule release. Cell 115, 851-862.
71. Watson, C. & Paxinos, G. (2010) Chemoarchitectonic Atlas of the Mouse Brain. Academic, London.
72. Weiss, L.A., Abney, M., Parry, R., Scanu, A.M., Cook, E.H. Jr. & Ober, C. (2005) Variation in ITGB3 has sex-specific associations with plasma lipoprotein(a) and whole blood serotonin levels in a population-based sample. Hum Genet 117, 81-87.
73. Welsh, C.E., Miller, D.R., Manly, K.F., Wang, J., McMillan, L., Morahan, G., Mott, R., Iraqi, F.A., Threadgill, D.W. & de Villena, F.P. (2012) Status and access to the collaborative cross population. Mamm Genome 23, 706-712.
74. Whibley, A., Urquhart, J., Dore, J., Willatt, L., Parkin, G., Gaunt, L., Black, G., Donnai, D. & Raymond, F.L. (2010) Deletion of MAOA and MAOB in a male patient causes severe developmental delay, intermittent hypotonia and stereotypical hand movements. Eur J Hum Genet 18, 1095-1099.
75. Wylie, C.J., Hendricks, T.J., Zhang, B., Wang, L., Lu, P., Leahy, P., Fox, S., Maeno, H. & Deneris, E.S. (2010) Distinct transcriptomes define rostral and caudal serotonin neurons. J Neurosci 30, 670-684.
76. Yadav, V.K., Oury, F., Suda, N., Liu, Z.W., Gao, X.B., Confavreux, C., Klemenhagen, K.C., Tanaka, K.F., Gingrich, J.A., Guo, X.E., Tecott, L.H., Mann, J.J., Hen, R., Horvath, T.L. & Karsenty, G. (2009) A serotonin-dependent mechanism explains the leptin regulation of bone mass, appetite, and energy expenditure. Cell 138, 976-989.
77. Ye, R. & Blakely, R.D. (2011) Natural and engineered coding variation in antidepressant-sensitive serotonin transporters. Neuroscience 197, 28-36.