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Circadian behavior of adult mice exposed to stress and fluoxetine during development

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Abstract

Introduction

Women of child-bearing age are the population at greatest risk for depression. The stress experienced during pregnancy and the associated antidepressant treatments can both affect fetal development. Fluoxetine (FLX) is among the most common antidepressants used by pregnant women. We have previously demonstrated that perinatal exposure to FLX can alter expression of circadian rhythms in adulthood. Here, we examine the combined effects of maternal stress during pregnancy and perinatal exposure to the antidepressant FLX on the circadian behavior of mice as adults.

Methods

Mouse dams were exposed to chronic unpredictable stress (embryonic (E) day 7 to E18), FLX (E15 to postnatal day 12), a combination of both stress and FLX, or were left untreated. At 2 months of age, male offspring were placed in recording chambers and circadian organization of wheel running rhythms and phase shifts to photic and non-photic stimuli were assessed.

Results

Mice exposed to prenatal stress (PS) had smaller light-induced phase delays. Mice exposed to perinatal FLX required more days to re-entrainment to an 8-h phase advance of their light–dark cycle. Mice subjected to either perinatal FLX or to PS had larger light-induced phase advances and smaller phase advances to 8-OH-DPAT. FLX treatment partially reversed the effect of PS on phase shifts to late-night light exposure and to 8-OH-DPAT.

Conclusions

Our results suggest that, in mice, perinatal exposure to either FLX, or PS, or their combination, leads to discernible, persistent changes in their circadian systems as adults.

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References

  • Abrahamson EE, Moore RY (2001) Suprachiasmatic nucleus in the mouse: retinal innervation, intrinsic organization and efferent projections. Brain Res 916:172–191

    Article  CAS  PubMed  Google Scholar 

  • Adler DA, Ammanuel S, Lei J, Dada T, Borbiev T, Johnston MV, Kadam SD, Burd I (2014) Circadian cycle-dependent EEG biomarkers of pathogenicity in adult mice following prenatal exposure to in utero inflammation. Neuroscience 275:305–313

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Andersson L, Sundström-Poromaa I, Bixo M, Wulff M, Bondestam K, Åström M (2003) Point prevalence of psychiatric disorders during the second trimester of pregnancy: a population-based study. Am J Obstet Gynecol 189:148–154

    Article  PubMed  Google Scholar 

  • Andrade SE, Raebel MA, Brown J, Lane K, Livingston J, Boudreau D, Rolnick SJ, Roblin D, Smith DH, Willy ME, Staffa JA, Platt R (2008) Use of antidepressant medications during pregnancy: a multisite study. Am J Obstet Gynecol 198:194.e1-5

    Article  PubMed  Google Scholar 

  • Andrade SE, Reichman ME, Mott K, Pitts M, Kieswetter C, Dinatale M, Stone MB, Popovic J, Haffenreffer K, Toh S (2016) Use of selective serotonin reuptake inhibitors (SSRIs) in women delivering liveborn infants and other women of child-bearing age within the U.S. Food and Drug Administration's Mini-Sentinel program. Arch Womens Ment Health. doi:10.1007/s00737-016-0637-1

    PubMed  Google Scholar 

  • Antle MC, Silver R (2005) Orchestrating time: arrangements of the brain circadian clock. Trends Neurosci 28:145–151

    Article  CAS  PubMed  Google Scholar 

  • Antle MC, Silver R (2016) Circadian insights into motivated behavior. Curr Top Behav Neurosci 27:137–169

    Article  PubMed  Google Scholar 

  • Antle MC, Sterniczuk R, Smith VM, Hagel K (2007) Non-photic modulation of phase shifts to long light pulses. J Biol Rhythm 22:524–533

    Article  Google Scholar 

  • Balsalobre A, Brown SA, Marcacci L, Tronche F, Kellendonk C, Reichardt HM, Schutz G, Schibler U (2000) Resetting of circadian time in peripheral tissues by glucocorticoid signaling. Science 289:2344–2347

    Article  CAS  PubMed  Google Scholar 

  • Barnard AR, Nolan PM (2008) When clocks go bad: neurobehavioural consequences of disrupted circadian timing. PLoS Genet 4:e1000040

    Article  PubMed  PubMed Central  Google Scholar 

  • Belenky MA, Pickard GE (2001) Subcellular distribution of 5-HT(1B) and 5-HT(7) receptors in the mouse suprachiasmatic nucleus. J Comp Neurol 432:371–388

    Article  CAS  PubMed  Google Scholar 

  • Bosch OJ, Kromer SA, Neumann ID (2006) Prenatal stress: opposite effects on anxiety and hypothalamic expression of vasopressin and corticotropin-releasing hormone in rats selectively bred for high and low anxiety. Eur J Neurosci 23:541–551

    Article  PubMed  Google Scholar 

  • Cabrera-Vera TM, Battaglia G (1998) Prenatal exposure to fluoxetine (Prozac) produces site-specific and age-dependent alterations in brain serotonin transporters in rat progeny: evidence from autoradiographic studies. J Pharmacol Exp Ther 286:1474–1481

    CAS  PubMed  Google Scholar 

  • Cabrera-Vera TM, Garcia F, Pinto W, Battaglia G (1997) Effect of prenatal fluoxetine (Prozac) exposure on brain serotonin neurons in prepubescent and adult male rat offspring. J Pharmacol Exp Ther 280:138–145

    CAS  PubMed  Google Scholar 

  • Carey RJ (2010) Serotonin and basal sensory-motor control. In: Müller CP, Jacobs BL (eds) Handbook of behavioral neurobiology of serotonin. Academic Press, San Diego, pp 325–330

    Chapter  Google Scholar 

  • Chen CP, Kuhn P, Advis JP, Sarkar DK (2006) Prenatal ethanol exposure alters the expression of period genes governing the circadian function of beta-endorphin neurons in the hypothalamus. J Neurochem 97:1026–1033

    Article  CAS  PubMed  Google Scholar 

  • Clancy B, Kersh B, Hyde J, Darlington RB, Anand KJ, Finlay BL (2007) Web-based method for translating neurodevelopment from laboratory species to humans. Neuroinformatics 5:79–94

    Article  PubMed  Google Scholar 

  • da Silva CM, Gonçalves L, Manhaes-de-Castro R, Nogueira MI (2010) Postnatal fluoxetine treatment affects the development of serotonergic neurons in rats. Neurosci Lett 483:179–183

    Article  PubMed  Google Scholar 

  • Duncan MJ, Hester JM, Hopper JA, Franklin KM (2010) The effects of aging and chronic fluoxetine treatment on circadian rhythms and suprachiasmatic nucleus expression of neuropeptide genes and 5-HT1B receptors. Eur J Neurosci 31:1646–1654

    PubMed  PubMed Central  Google Scholar 

  • Duncan MJ, Jennes L, Jefferson JB, Brownfield MS (2000) Localization of serotonin(5A) receptors in discrete regions of the circadian timing system in the Syrian hamster. Brain Res 869:178–185

    Article  CAS  PubMed  Google Scholar 

  • Duncan MJ, Short J, Wheeler DL (1999) Comparison of the effects of aging on 5-HT7 and 5-HT1A receptors in discrete regions of the circadian timing system in hamsters. Brain Res 829:39–45

    Article  CAS  PubMed  Google Scholar 

  • Edgar DM, Miller JD, Prosser RA, Dean RR, Dement WC (1993) Serotonin and the mammalian circadian system: II. Phase-shifting rat behavioral rhythms with serotonergic agonists. J Biol Rhythm 8:17–31

    Article  CAS  Google Scholar 

  • Francis DD, Champagne FA, Liu D, Meaney MJ (1999) Maternal care, gene expression, and the development of individual differences in stress reactivity. Ann N Y Acad Sci 896:66–84

    Article  CAS  PubMed  Google Scholar 

  • Gardani M, Biello SM (2008) The effects of photic and nonphotic stimuli in the 5-HT7 receptor knockout mouse. Neuroscience 152:245–253

    Article  CAS  PubMed  Google Scholar 

  • Gavin NI, Gaynes BN, Lohr KN, Meltzer-Brody S, Gartlehner G, Swinson T (2005) Perinatal depression: a systematic review of prevalence and incidence. Obstet Gynecol 106:1071–1083

    Article  PubMed  Google Scholar 

  • Gemmel M, Rayen I, Lotus T, van Donkelaar E, Steinbusch HW, De Lacalle S, Kokras N, Dalla C, Pawluski JL (2016) Developmental fluoxetine and prenatal stress effects on serotonin, dopamine, and synaptophysin density in the PFC and hippocampus of offspring at weaning. Dev Psychobiol 58:315–327

    Article  CAS  PubMed  Google Scholar 

  • Green CB, Takahashi JS, Bass J (2008) The meter of metabolism. Cell 134:728–742

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grippo AJ, Beltz TG, Johnson AK (2003) Behavioral and cardiovascular changes in the chronic mild stress model of depression. Physiol Behav 78:703–10

  • Hill MN, Hellemans KGC, Verma P, Gorzalka BB, Weinberg J (2012) Neurobiology of chronic mild stress: parallels to major depression. Neurosci Biobehav Rev 36:2085–2117

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hobfoll SE, Ritter C, Lavin J, Hulsizer MR, Cameron RP (1995) Depression prevalence and incidence among inner-city pregnant and postpartum women. J Consult Clin Psych 63:445–453

    Article  CAS  Google Scholar 

  • Ishiwata H, Shiga T, Okado N (2005) Selective serotonin reuptake inhibitor treatment of early postnatal mice reverses their prenatal stress-induced brain dysfunction. Neuroscience 133:893–901

    Article  CAS  PubMed  Google Scholar 

  • Joseph V, Mamet J, Lee F, Dalmaz Y, Van Reeth O (2002) Prenatal hypoxia impairs circadian synchronisation and response of the biological clock to light in adult rats. J Physiol 543:387–395

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kinney DK, Munir KM, Crowley DJ, Miller AM (2008) Prenatal stress and risk for autism. Neurosci Biobehav Rev 32:1519–1532

    Article  PubMed  PubMed Central  Google Scholar 

  • Kiryanova V, Dyck RH (2014) Increased aggression, improved spatial memory, and reduced anxiety-like behaviour in adult male mice exposed to fluoxetine early in life. Dev Neurosci 36:396–408

    Article  CAS  PubMed  Google Scholar 

  • Kiryanova V, Meunier SJ, Vecchiarelli HA, Hill MN, Dyck RH (2016) Effects of maternal stress and perinatal fluoxetine exposure on behavioral outcomes of adult male offspring. Neuroscience 320:281–296

    Article  CAS  PubMed  Google Scholar 

  • Kiryanova V, Smith VM, Dyck RH, Antle MC (2013) The effects of perinatal fluoxetine treatment on the circadian system of the adult mouse. Psychopharmacology 225:743–751

    Article  CAS  PubMed  Google Scholar 

  • Kitamura T, Shima S, Sugawara M, Toda MA (1993) Psychological and social correlates of the onset of affective-disorders among pregnant-women. Psychol Med 23:967–975

    Article  CAS  PubMed  Google Scholar 

  • Knaepen L, Rayen I, Charlier TD, Fillet M, Houbart V, van Kleef M, Steinbusch HW, Patijn J, Tibboel D, Joosten EA, Pawluski JL (2013) Developmental fluoxetine exposure normalizes the long-term effects of maternal stress on post-operative pain in Sprague-Dawley rat offspring. PLoS One 8:e57608

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kyriacou CP, Hastings MH (2010) Circadian clocks: genes, sleep, and cognition. Trends Cogn Sci 14:259–267

    Article  PubMed  Google Scholar 

  • Lovenberg TW, Baron BM, de Lecea L, Miller JD, Prosser RA, Rea MA, Foye PE, Racke M, Slone AL, Siegel BW, Danielson PE, Sutcliffe JG, Erlander MG (1993) A novel adenylyl cyclase-activating serotonin receptor (5-HT7) implicated in the regulation of mammalian circadian rhythms. Neuron 11:449–458

    Article  CAS  PubMed  Google Scholar 

  • Mandrioli R, Mercolini L, Saracino MA, Raggi MA (2012) Selective serotonin reuptake inhibitors (SSRIs): therapeutic drug monitoring and pharmacological interactions. Curr Med Chem 19:1846–1863

    Article  CAS  PubMed  Google Scholar 

  • Matrisciano F, Tueting P, Maccari S, Nicoletti F, Guidotti A (2012) Pharmacological activation of group-II metabotropic glutamate receptors corrects a schizophrenia-like phenotype induced by prenatal stress in mice. Neuropsychopharmacol 37:929–938

    Article  CAS  Google Scholar 

  • McAllister BB, Kiryanova V, Dyck RH (2012) Behavioural outcomes of perinatal maternal fluoxetine treatment. Neuroscience 226:356–366

    Article  CAS  PubMed  Google Scholar 

  • McKee MD, Cunningham M, Jankowski KR, Zayas L (2001) Health-related functional status in pregnancy: relationship to depression and social support in a multi-ethnic population. Obstet Gynecol 97:988–993

    CAS  PubMed  Google Scholar 

  • Meyer-Bernstein EL, Morin LP (1996) Differential serotonergic innervation of the suprachiasmatic nucleus and the intergeniculate leaflet and its role in circadian rhythm modulation. J Neurosci 16:2097–2111

    CAS  PubMed  Google Scholar 

  • Mistlberger RE, Antle MC (2006) The enigma of behavioral inputs to the circadian clock: a test of function using restraint. Physiol Behav 87:948–54

  • Mistlberger RE, Antle MC, Glass JD, Miller JD (2000) Behavioral and serotonergic regulation of circadian rhythms. Biol Rhythm Res 31:240–283

    Article  CAS  Google Scholar 

  • Miyagawa K, Tsuji M, Ishii D, Takeda K, Takeda H (2015) Prenatal stress induces vulnerability to stress together with the disruption of central serotonin neurons in mice. Behav Brain Res 277:228–236

    Article  CAS  PubMed  Google Scholar 

  • Moga MM, Moore RY (1997) Organization of neural inputs to the suprachiasmatic nucleus in the rat. J Comp Neurol 389:508–534

    Article  CAS  PubMed  Google Scholar 

  • Monroe SM, Hadjiyannakis K (2002) The social environment and depression: focusing on severe life stress. In: Gotlib IH, Hammen CL (eds) Handbook of depression. Guilford Press, New York, pp 314–340

    Google Scholar 

  • Morin LP (1999) Serotonin and the regulation of mammalian circadian rhythmicity. Ann Med 31:12–33

    Article  CAS  PubMed  Google Scholar 

  • Morin LP, Allen CN (2006) The circadian visual system, 2005. Brain Res Rev 51:1–60

    Article  CAS  PubMed  Google Scholar 

  • Moyer RW, Kennaway DJ (1999) Immunohistochemical localization of serotonin receptors in the rat suprachiasmatic nucleus. Neurosci Lett 271:147–150

    Article  CAS  PubMed  Google Scholar 

  • Oliver KR, Kinsey AM, Wainwright A, Sirinathsinghji DJ (2000) Localization of 5-ht(5A) receptor-like immunoreactivity in the rat brain. Brain Res 867:131–142

    Article  CAS  PubMed  Google Scholar 

  • Ordian NÉ, Pivina SG, Fedotova IO, Akulova VK (2010) Comparative efficacy of selective serotonin reuptake inhibitors in young prenatally stressed female rats (in Russian). Eksp Klin Farmakol 73:7–10

    CAS  PubMed  Google Scholar 

  • Orozco-Solis R, Matos RJ, Lopes de Souza S, Grit I, Kaeffer B, Manhaes de Castro R, Bolanos-Jimenez F (2011) Perinatal nutrient restriction induces long-lasting alterations in the circadian expression pattern of genes regulating food intake and energy metabolism. Int J Obes 35:990–1000

    Article  CAS  Google Scholar 

  • Pang RD, Holschneider DP, Miller JD (2012) Circadian rhythmicity in serotonin transporter knockout mice. Life Sci 91:365–368

    Article  CAS  PubMed  Google Scholar 

  • Paulus EV, Mintz EM (2013) Photic and nonphotic responses of the circadian clock in serotonin-deficient Pet-1 knockout mice. Chronobiol Int 30:1251–1260

    Article  CAS  PubMed  Google Scholar 

  • Peters DA (1982) Prenatal stress: effects on brain biogenic-amine and plasma-corticosterone levels. Pharmacol Biochem Behav 17:721–725

    Article  CAS  PubMed  Google Scholar 

  • Pickard GE, Weber ET, Scott PA, Riberdy AF, Rea MA (1996) 5HT1B receptor agonists inhibit light-induced phase shifts of behavioral circadian rhythms and expression of the immediate-early gene c-fos in the suprachiasmatic nucleus. J Neurosci 16:8208–8220

    CAS  PubMed  Google Scholar 

  • Portaluppi F, Vergnani L, Manfredini R, Fersini C (1996) Endocrine mechanisms of blood pressure rhythms. Ann N Y Acad Sci 783:113–131

    Article  CAS  PubMed  Google Scholar 

  • Prosser RA, Dean RR, Edgar DM, Heller HC, Miller JD (1993) Serotonin and the mammalian circadian system: I. In vitro phase shifts by serotonergic agonists and antagonists. J Biol Rhythm 8:1–16

    Article  CAS  Google Scholar 

  • Rayen I, Gemmel M, Pauley G, Steinbusch HW, Pawluski JL (2015) Developmental exposure to SSRIs, in addition to maternal stress, has long-term sex-dependent effects on hippocampal plasticity. Psychopharmacology 232:1231–1244

    Article  CAS  PubMed  Google Scholar 

  • Rayen I, Steinbusch HW, Charlier TD, Pawluski JL (2013) Developmental fluoxetine exposure and prenatal stress alter sexual differentiation of the brain and reproductive behavior in male rat offspring. Psychoneuroendocrinology 38:1618–1629

    Article  CAS  PubMed  Google Scholar 

  • Rayen I, van den Hove DL, Prickaerts J, Steinbusch HW, Pawluski JL (2011) Fluoxetine during development reverses the effects of prenatal stress on depressive-like behavior and hippocampal neurogenesis in adolescence. PLoS One 6:e24003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rodriguez A, Bohlin G (2005) Are maternal smoking and stress during pregnancy related to ADHD symptoms in children? J Child Psychol Psychiatry 46:246–254

    Article  PubMed  Google Scholar 

  • Romijn HJ, Hofman MA, Gramsbergen A (1991) At what age is the developing cerebral cortex of the rat comparable to that of the full-term newborn human baby? Early Hum Dev 26:61–67

    Article  CAS  PubMed  Google Scholar 

  • Ronald A, Pennell CE, Whitehouse AJO (2011) Prenatal maternal stress associated with ADHD and autistic traits in early childhood. Front Psychol 1:223. doi:10.3389/fpsyg.2010.00223

    Article  PubMed  PubMed Central  Google Scholar 

  • Salgado-Delgado R, Tapia Osorio A, Saderi N, Escobar C (2011) Disruption of circadian rhythms: a crucial factor in the etiology of depression. Depress Res Treat 2011:839743. doi:10.1155/2011/839743

    PubMed  PubMed Central  Google Scholar 

  • Saper CB, Scammell TE, Lu J (2005) Hypothalamic regulation of sleep and circadian rhythms. Nature 437:1257–1263

    Article  CAS  PubMed  Google Scholar 

  • Schraut KG, Jakob SB, Weidner MT, Schmitt AG, Scholz CJ, Strekalova T, El Hajj N, Eijssen LM, Domschke K, Reif A, Haaf T, Ortega G, Steinbusch HW, Lesch KP, Van den Hove DL (2014) Prenatal stress-induced programming of genome-wide promoter DNA methylation in 5-HTT-deficient mice. Transl Psychiatry 4:e473

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shelton J, Yun SJ, Olson SL, Turek F, Bonaventure P, Dvorak C, Lovenberg T, Dugovic C (2015) Selective pharmacological blockade of the 5-HT7 receptor attenuates light and 8-OH-DPAT induced phase shifts of mouse circadian wheel running activity. Front Behav Neurosci 8:453

    Article  PubMed  PubMed Central  Google Scholar 

  • Smith VM, Iannatonne S, Achal S, Jeffers RT, Antle MC (2014) The serotonergic anxiolytic buspirone attenuates circadian responses to light. Eur J Neurosci 40:3512–3525

    Article  PubMed  Google Scholar 

  • Smith VM, Jeffers RT, McAllister BB, Basu P, Dyck R, Antle MC (2015) Effects of lighting condition on circadian behavior in 5-HT1A receptor knockout mice. Physiol Behav 139:136–144

    Article  CAS  PubMed  Google Scholar 

  • Smith VM, Sterniczuk R, Phillips CI, Antle MC (2008) Altered photic and non-photic phase shifts in 5-HT(1A) receptor knockout mice. Neuroscience 157:513–523

    Article  CAS  PubMed  Google Scholar 

  • Smolensky MH, Hermida RC, Reinberg A, Sackett-Lundeen L, Portaluppi F (2016) Circadian disruption: new clinical perspective of disease pathology and basis for chronotherapeutic intervention. Chronobiol Int 33:1101–1119

    Article  PubMed  Google Scholar 

  • Stohr T, Schulte Wermeling D, Szuran T, Pliska V, Domeney A, Welzl H, Weiner I, Feldon J (1998) Differential effects of prenatal stress in two inbred strains of rats. Pharmacol Biochem Behav 59:799–805

    Article  CAS  PubMed  Google Scholar 

  • Takahashi JS, Hong H-K, Ko CH, McDearmon EL (2008) The genetics of mammalian circadian order and disorder: implications for physiology and disease. Nat Rev Genet 9:764–775

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Talge NM, Neal C, Glover V, Early Stress, Translational Research and Prevention Science Network: Fetal and Neonatal Experience on Child and Adolescent Mental Health (2007) Antenatal maternal stress and long-term effects on child neurodevelopment: how and why? J Child Psychol Psychiatry 48:245–261

  • Tennant C (2002) Life events, stress and depression: a review of recent findings. Aust N Z J Psychiatry 36:173–182

    Article  PubMed  Google Scholar 

  • Vallee M, Mayo W, Dellu F, LeMoal M, Simon H, Maccari S (1997) Prenatal stress induces high anxiety and postnatal handling induces low anxiety in adult offspring: correlation with stress-induced corticosterone secretion. J Neurosci 17:2626–2636

    CAS  PubMed  Google Scholar 

  • Webb IC, Antle MC, Mistlberger RE (2014) Regulation of circadian rhythms in mammals by behavioral arousal. Behav Neurosci 128:304–325

    Article  PubMed  Google Scholar 

  • Wollnik F (1992) Effects of chronic administration and withdrawal of antidepressant agents on circadian activity rhythms in rats. Pharmacol Biochem Behav 43:549–561

    Article  CAS  PubMed  Google Scholar 

  • Yamakawa GR, Antle MC (2010) Phenotype and function of raphe projections to the suprachiasmatic nucleus. Eur J Neurosci 31:1974–1983

    Article  PubMed  Google Scholar 

  • Yamakawa GR, Basu P, Cortese F, MacDonnell J, Whalley D, Smith VM, Antle MC (2016) The cholinergic forebrain arousal system acts directly on the circadian pacemaker. Proc Natl Acad Sci U S A 113:13498–13503

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This work was supported by the Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery Grants to RHD and MCA and by a Canadian Institutes of Health Research (CIHR) Operating Grant to RHD.

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Correspondence to Michael C. Antle.

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Kiryanova, V., Smith, V.M., Dyck, R.H. et al. Circadian behavior of adult mice exposed to stress and fluoxetine during development. Psychopharmacology 234, 793–804 (2017). https://doi.org/10.1007/s00213-016-4515-3

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