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Effect of testosterone replacement on feeding behaviors after acute and chronic stress in gonadectomized male NMRI mice

  • Research Article
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Frontiers in Biology

Abstract

Background

We study the role of gonadectomy on the response to unavoidable stress and the role of testosterone replacement on gonadectomy in the male Naval Medical Research Institute mice (30±5 g) were studied. For this purpose, the hormonal and metabolic changes were investigated.

Methods

In the experimental group, the gonads were surgically removed, and a cannula was inserted into the left lateral ventricle. For acute and chronic stress induction, animals were placed in the communication box for 30 min for one day and four consecutive days, respectively. The animals received different doses of intraventricular (ICV) testosterone (0.01, 0.05, 0.1 μg/mouse) 5 minutes or intraperitoneal (IP) testosterone (0.05, 0.01, 0.1 mg/kg) 30 minutes before the stress induction.

Results

The results showed that acute and chronic stress increases plasma cortisol concentration. IP testosterone injections of testosterone did not decrease cortisol concentrations in response to acute stress, whereas ICV injections did reduce cortisol concentrations. The stress reduced anorexia time, while the administration of testosterone increased anorexia time. In addition, acute stress reduced food intake in the gonadectomized mice. IP testosterone at 0.01 and 0.05 mg/kg increased food intake. Additionally, stress in gonadectomized mice reduced water intake, while the IP injection of testosterone in chronic stress further reduced water intake. Also, stress reduced the animals’ brain/adrenal volumes, while the IP and ICVinjection of testosterone at 0.01 mg/kg inhibited this effect.

Conclusion

The results showed that the IP (0.05, 0.01, 0.1 mg/kg) and ICV (0.01, 0.05, 0.1 μg/mouse) administration of testosterone in the gonadectomized mice can modulate hormonal and metabolic changes induced by stress.

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References

  • Adam T C, Epel E S (2007). Stress, eating and the reward system. Physiol Behav, 91(4): 449–458

    Article  CAS  PubMed  Google Scholar 

  • Amouei N, Sahraei H, Alibeik H, Meftahi G H, Bahari Z, Mohammadi A (2016). Intrahippocampal and peripheral effects of nicotine injection on the metabolic and behavioral response to inescapable stress. Biosci Biotechnol Res Asia, 13(3): 1363–1371

    Article  Google Scholar 

  • Arun S, Burawat J, Sukhorum W, Sampannang A, Uabundit N, Iamsaard S (2016). Changes of testicular phosphorylated proteins in response to restraint stress in male rats. J Zhejiang Univ Sci B, 17(1): 21–29

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Asalgoo S, Jahromi G P, Meftahi G H, Sahraei H (2015). Posttraumatic Stress Disorder (PTSD): Mechanisms and possible treatments. Neurophysiology, 47(6): 482–489

    Article  CAS  Google Scholar 

  • Baldwin D S (2001). Depression and sexual dysfunction. Br Med Bull, 57(1): 81–99

    Article  CAS  PubMed  Google Scholar 

  • Chuang J C, Zigman J M (2010). Ghrelin’s roles in stress, mood, and anxiety regulation. Int J Pept, 2010: 460549

    PubMed  PubMed Central  Google Scholar 

  • Connan F, Lightman S L, Landau S, Wheeler M, Treasure J, Campbell I C (2007). An investigation of hypothalamic-pituitary-adrenal axis hyperactivity in anorexia nervosa: the role of CRH and AVP. J Psychiatr Res, 41(1-2): 131–143

    Article  PubMed  Google Scholar 

  • Cotrufo P, Monteleone P, d’Istria M, Fuschino A, Serino I, Maj M (2000). Aggressive behavioral characteristics and endogenous hormones in women with Bulimia nervosa. Neuropsychobiology, 42(2): 58–61

    Article  CAS  PubMed  Google Scholar 

  • Curtis AL, Bethea T, Valentino R J. Sexually dimorphic responses of the brain norepinephrine system to stress and corticotropin-releasing factor Neuropsychopharmacol. 2006;31(3):544–54

    CAS  Google Scholar 

  • Dallman M F, Akana S F, Scribner K A, Bradbury M J, Walker C D, Strack A M, Cascio C S (1992). Stress, feedback and facilitation in the hypothalamo-pituitary-adrenal axis. J Neuroendocrinol, 4(5): 517–526

    Article  CAS  PubMed  Google Scholar 

  • Dallman MF, Pecoraro N, Akana S F, La Fleur S E, Gomez F, Houshyar H, Bell M E, Bhatnagar S, Laugero K D, Manalo S (2003). Chronic stress and obesity: a new view of “comfort food”. Proc Natl Acad Sci USA, 100(20): 11696–11701

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dalooei J R, Sahraei H, Meftahi G H, Khosravi M, Bahari Z, Hatef B, Mohammadi A, Nicaeili F, Eftekhari F, Ghamari F, Hadipour M, Kaka G (2016). Temporary amygdala inhibition reduces stress effects in female mice. J Adv Res, 7(5): 643–649

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Derijk R H, van Leeuwen N, Klok M D, Zitman F G (2008). Corticosteroid receptor-gene variants: modulators of the stressresponse and implications for mental health. Eur J Pharmacol, 585 (2-3): 492–501

    Article  CAS  PubMed  Google Scholar 

  • Ehteram B Z, Sahraei H, Meftahi G H, Khosravi M (2017). Effect of intermittent feeding on gonadal function in male and female NMRI mice during chronic stress. Braz Arch Biol Technol, 60(0): e17160607

    Article  Google Scholar 

  • Erfani M, Sahraei H, Bahari Z, Meftahi G H, Hatef B, Mohammadi A, Hosseini S H (2017). Evaluation of the effect of time change in cognitive function in volunteers in Tehran. Glob J Health Sci, 9(2): 119–126

    Article  Google Scholar 

  • Eslamizade M J, Saffarzadeh F, Mousavi S M, Meftahi G H, Hosseinmardi N, Mehdizadeh M, Janahmadi M (2015). Alterations in CA1 pyramidal neuronal intrinsic excitability mediated by Ih channel currents in a rat model of amyloid beta pathology. Neuroscience, 305: 279–292

    Article  CAS  PubMed  Google Scholar 

  • Evanson N K, Herman J P (2015). Role of paraventricular nucleus glutamate signaling in regulation of HPA axis stress responses. Interdiscip Inf Sci, 21(3): 253–260

    PubMed  PubMed Central  Google Scholar 

  • Ghobadi N, Sahraei H, Meftahi G H, Bananej M, Salehi S (2016). Effect of estradiol replacement in ovariectomized NMRI micein response to acute and chronic stress. J Appl Pharm Sci, 6(11): 176–184

    Article  Google Scholar 

  • Habhab S, Sheldon J P, Loeb R C (2009). The relationship between stress, dietary restraint, and food preferences in women. Appetite, 52 (2): 437–444

    Article  PubMed  Google Scholar 

  • Hammond J, Le Q, Goodyer C, Gelfand M, Trifiro M, LeBlanc A (2001). Testosterone mediated neuroprotection through the androgen receptor in human primary neurons. J Neurochem,77(5):1319–1326

    Article  CAS  PubMed  Google Scholar 

  • Handa R J, Nunley KM, Lorens S A, Louie J P, McGivern R F, Bollnow M R (1994). Androgen regulation of adrenocorticotropin and corticosterone secretion in the male rat following novelty and foot shock stressors. Physiol Behav, 55(1): 117–124

    Article  CAS  PubMed  Google Scholar 

  • Hardy MP, Gao H B, Dong Q, Ge R, Wang Q, Chai WR, Feng X, Sottas C (2005). Stress hormone and male reproductive function. Cell Tissue Res, 322(1): 147–153

    Article  CAS  PubMed  Google Scholar 

  • Hari Priya P, Reddy PS. Effect of restraint stress on lead induced male reproductive toxicity in rats. J Exp Zool A Ecol Genet Physiol 2012;317(7): 455–65

    Article  CAS  PubMed  Google Scholar 

  • Hassantash M, Sahraei H, Bahari Z, Meftahi G H, Vesali R (2017). The role of dopamine D2 receptors in the amygdala in metabolic and behavioral responses to stress in male Swiss-Webster mice. Front Biol, 12(4): 298–310

    Article  CAS  Google Scholar 

  • Hill J W (2010). Gene expression and the control of food intake by hypothalamic POMC/CART neurons. Open Neuroendocrinol J, 3: 21–27

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kennedy SH, Dickens SE, Eisfeld BS, Bagby RM. Sexual dysfunction before ntidepressant therapy in major depression. 62TJ Affect Disord 1999;56:201–208

    Article  CAS  Google Scholar 

  • Krahn D D, Gosnell B A, Majchrzak MJ (1990). The anorectic effects of CRH and restraint stress decrease with repeated exposures. Biol Psychiatry, 27(10): 1094–1102

    Article  CAS  PubMed  Google Scholar 

  • Lee T, Jarome T, Li S J, Kim J J, Helmstetter F J (2009). Chronic stress selectively reduces hippocampal volume in rats: a longitudinal MRI study. Neuroreport, 25: 1554–1558

    Article  Google Scholar 

  • Liston C, Miller M M, Goldwater D S, Radley J J, Rocher A B, Hof P R, Morrison J H, McEwen B S (2006). Stress-induced alterations in prefrontal cortical dendritic morphology predict selective impairments in perceptual attentional set-shifting. J Neurosci, 26(30): 7870–7874

    Article  CAS  PubMed  Google Scholar 

  • Lund T D, Hinds L R, Handa R J (2006). The androgen 5alphadihydrotestosterone and its metabolite 5alpha-androstan-3beta, 17beta-diol inhibit the hypothalamo-pituitary-adrenal response to stress by acting through estrogen receptor beta-expressing neurons in the hypothalamus. J Neurosci, 26(5): 1448–1456

    Article  CAS  PubMed  Google Scholar 

  • Lund T D, Munson D J, Haldy M E, Handa R J (2004). Androgen inhibits, while oestrogen enhances, restraint-induced activation of neuropeptide neurones in the paraventricular nucleus of the hypothalamus. J Neuroendocrinol, 16(3): 272–278

    Article  CAS  PubMed  Google Scholar 

  • Majzoub J A (2006). Corticotropin-releasing hormone physiology. Eur J Endocrinol, 155(suppl_1): 71–76

    Article  Google Scholar 

  • McEwen B S (2007). Physiology and neurobiology of stress and adaptation: central role of the brain. Physiol Rev, 87(3): 873–904

    Article  PubMed  Google Scholar 

  • McEwen B S (2012). Brain on stress: how the social environment gets under the skin. Proc Natl Acad Sci USA, 109(2 Suppl 2): 17180–17185

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McEwen B S (2016). In pursuit of resilience: stress, epigenetics, and brain plasticity. Ann N Y Acad Sci, 1373(1): 56–64

    Article  PubMed  Google Scholar 

  • McEwen B S, Milner T A (2007). Hippocampal formation: shedding light on the influence of sex and stress on the brain. Brain Res Brain Res Rev, 55(2): 343–355

    Article  Google Scholar 

  • McEwen B S, Nasca C, Gray J D (2016). Stress effects on neuronal structure: hippocampus, amygdala, and prefrontal cortex. Neuropsychopharmacology, 41(1): 3–23

    Article  CAS  PubMed  Google Scholar 

  • Meftahi G, Ghotbedin Z, Eslamizade M J, Hosseinmardi N, Janahmadi M(2015). Suppressive effects of resveratrol treatment on the intrinsic evoked excitability of CA1 pyramidal neurons. Cell J, 17(3): 532–539

    PubMed  PubMed Central  Google Scholar 

  • Meftahi G H, Janahmadi M, Eslamizade M J (2014). Effects of resveratrol on intrinsic neuronal properties of CA1 pyramidal neurons in rat hippocampal slices. Physiol Pharmacol, 18: 144–155

    Google Scholar 

  • Mikolajczyk R T, El Ansari W, Maxwell A E (2009). Food consumption frequency and perceived stress and depressive symptoms among students in three European countries. Nutr J, 8(1): 31

    Article  PubMed  PubMed Central  Google Scholar 

  • Miyamoto H, Mitani F, Mukai K, Suematsu M, Ishimura Y (1999). Studies on cytogenesis in adult rat adrenal cortex: circadian and zonal variations and their modulation by adrenocorticotropic hormone. J Biochem, 126(6): 1175–1183

    Article  CAS  PubMed  Google Scholar 

  • Mohammadian Z, Sahraei H, Meftahi G H, Ali-Beik H (2017). Effects of unilatral- and bilateral inhibition of rostral ventral tegmental area and central nucleus of amygdala on morphine-induced place conditioning in male Wistar rat. Clin Exp Pharmacol Physiol, 44(3): 403–412

    Article  CAS  PubMed  Google Scholar 

  • Motahari A A, Sahraei H, Meftahi G H (2016). Role of nitric oxide on dopamine release and morphine-dependency. Basic Clin Neurosci, 7 (4): 283–290

    CAS  PubMed  PubMed Central  Google Scholar 

  • Osanloo N, Sarahian N, Zardooz H, Sahraei H, Sahraei M, Sadeghi B (2015). Effects of memantine, an NMDA antagonist, on metabolic syndromes in female NMRI mice. Basic Clin Neurosci, 6(4): 239–252

    PubMed  PubMed Central  Google Scholar 

  • Papadopoulos A D, Wardlaw S L (2000). Testosterone suppresses the response of the hypothalamic-pituitary-adrenal axis to interleukin-6. Neuroimmunomodulation, 8(1): 39–44

    Article  CAS  PubMed  Google Scholar 

  • Paxinos G, Franklin K B JThe mouse brain in stereotaxic coordinates. 2nd Edition, San Diego Academic Press, 2001

    Google Scholar 

  • Pourhashemi S F, Sahraei H, Meftahi G H, Hatef B, Gholipour B (2016). The effect of 20 minutes scuba diving on cognitive function of professional scuba divers. Asian J Sports Med, 7(3): e38633

    PubMed  PubMed Central  Google Scholar 

  • Rai J, Pandey S N, Srivastava R K (2004). Testosterone hormone level in albino rats following restraint stress of long duration. J Anat Soc India, 53: 17–19

    Google Scholar 

  • Rubinow D R, Roca C A, Schmidt P J, Danaceau M A, Putnam K, Cizza G, Chrousos G, Nieman L (2005). Testosterone suppression of CRHstimulated cortisol in men. Neuropsychopharmacology, 30(10): 1906–1912

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sadeghi-Gharajehdaghi S, Sahraei H, Bahari Z, Meftahi G H, Jahromi G P, Ali-Beik H (2017). Effect of amygdaloid complex inhibition on nicotine-induced conditioned place preference in rats. J Appl Pharm Sci,7(03): 40–47

    Google Scholar 

  • Salleh M R (2008). Life event, stress and illness. Malays J Med Sci, 15 (4): 9–18

    PubMed  PubMed Central  Google Scholar 

  • Segerstrom S C, Miller G E (2004). Psychological stress and the human immune system: a meta-analytic study of 30 years of inquiry. Psychol Bull, 130(4): 601–630

    Article  PubMed  PubMed Central  Google Scholar 

  • Spritzer M D, Galea L A M (2007). Testosterone and dihydrotestoster-one, but not estradiol, enhance survival of new hippocampal neurons in adult male rats. Dev Neurobiol, 67(10): 1321–1333

    Article  CAS  PubMed  Google Scholar 

  • Ulrich-Lai YM, Figueiredo H F, Ostrander MM, Choi D C, Engeland W C, Herman J P (2006). Chronic stress induces adrenal hyperplasia and hypertrophy in a subregion-specific manner. Am J Physiol Endocrinol Metab, 291(5): e965–E973

    Article  CAS  PubMed  Google Scholar 

  • Venero C, Borrell J (1999). Rapid glucocorticoid effects on excitatory amino acid levels in the hippocampus: a microdialysis study in freely moving rats. Eur J Neurosci, 11(7): 2465–2473

    Article  CAS  PubMed  Google Scholar 

  • Viau V, Meaney M J (1996). The inhibitory effect of testosterone on hypothalamic-pituitary-adrenal responses to stress is mediated by the medial preoptic area. J Neurosci, 16(5): 1866–1876

    Article  CAS  PubMed  Google Scholar 

  • Williamson M, Bingham B, Viau V (2005). Central organization of androgen-sensitive pathways to the hypothalamic-pituitary-adrenal axis: implications for individual differences in responses to homeostatic threat and predisposition to disease. Prog Neuropsychopharmacol Biol Psychiatry, 29(8): 1239–1248

    Article  CAS  PubMed  Google Scholar 

  • Wright A F, Goedert M, Hastie N D (1991). Familial Alzheimer’s disease. Beta amyloid resurrected. Nature, 349(6311): 653–654

    CAS  PubMed  Google Scholar 

  • Yuen E Y, Wei J, Liu W, Zhong P, Li X, Yan Z (2012). Repeated stress suppresses glutamate receptor expression and function in prefrontal cortex and impairs object recognition memory. Neuron, 73: 962–977

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This work was supported by the Neuroscience Research Center of Baqiyatallah University of Medical Sciences, Tehran, Iran.

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Authors and Affiliations

  1. Department of Biology, School of Biological Sciences, Islamic Azad University, North Tehran Branch, Tehran, Iran

    Sara Salehi Shemiran & Negin Ghobadi

  2. Neuroscience Research Center, Baqiyatallah University of Medical Sciences, Tehran, Iran

    Gholam Hossein Meftahi & Hedayat Sahraei

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  1. Sara Salehi Shemiran
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  2. Gholam Hossein Meftahi
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  3. Hedayat Sahraei
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  4. Negin Ghobadi
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Correspondence to Gholam Hossein Meftahi.

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Shemiran, S.S., Meftahi, G.H., Sahraei, H. et al. Effect of testosterone replacement on feeding behaviors after acute and chronic stress in gonadectomized male NMRI mice. Front. Biol. 12, 430–441 (2017). https://doi.org/10.1007/s11515-017-1470-2

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  • DOI: https://doi.org/10.1007/s11515-017-1470-2

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