Improvement of neurological disorders in postmenopausal model rats by administration of royal jelly

Abstract Objective: Royal jelly (RJ) from honeybees (Apis mellifera) has estrogenic activity. Estrogen deficiency after menopause leads to a high risk of memory impairment and depression as well as metabolic syndrome and osteoporosis. We here investigated the effect of RJ on memory impairment and depression-like behaviors in ovariectomized (OVX) rats. Methods: OVX rats were administered with RJ for 82 days. Hippocampus-dependent spatial memory and depression-like behaviors were assessed by the Morris water maze test and the forced swimming test, respectively. The weights of body, brain and uterus and the contents of protein and myelin galactolipids including galactosylceramide and sulfatide were measured. Results: Memory impairment and depression-like behaviors in OVX rats were recovered to the levels of sham-operated rats by RJ administration. Increased body weight and decreased uterine weight in OVX rats were recovered to the levels of sham-operated rats by 17β-estradiol (E2) administration but not by RJ administration. In contrast, brain weight was slightly increased by RJ administration but not by E2 administration. The contents of protein and myelin galactolipids were higher in the brains of RJ-administered OVX rats than in the brains of E2-administered OVX rats. Conclusion: The results suggest that RJ has a beneficial effect on neurological symptoms of a menopausal disorder.

[1]  H. Kenna,et al.  Cognitive Effects of Hormone Therapy Continuation or Discontinuation in a Sample of Women at Risk for Alzheimer Disease. , 2015, The American journal of geriatric psychiatry : official journal of the American Association for Geriatric Psychiatry.

[2]  V. Beral,et al.  Menopausal hormone use and ovarian cancer risk: individual participant meta-analysis of 52 epidemiological studies. , 2015, Lancet.

[3]  V. Beral,et al.  Menopausal hormone use and ovarian cancer risk: individual participant meta-analysis of 52 epidemiological studies , 2015, The Lancet.

[4]  Xujuan Yang,et al.  Anticipatory Estrogen Activation of the Unfolded Protein Response is Linked to Cell Proliferation and Poor Survival in Estrogen Receptor α Positive Breast Cancer , 2014, Oncogene.

[5]  H. Matsushita,et al.  Improvement of depression-like behavior and memory impairment with the ethanol extract of Pleurotus eryngii in ovariectomized rats. , 2013, Biological & pharmaceutical bulletin.

[6]  C. López-Rubalcava,et al.  The antidepressant-like effect of ethynyl estradiol is mediated by both serotonergic and noradrenergic systems in the forced swimming test , 2013, Neuroscience.

[7]  P. Heydarpour,et al.  Estradiol reduces depressive-like behavior through inhibiting nitric oxide/cyclic GMP pathway in ovariectomized mice , 2013, Hormones and Behavior.

[8]  T. Pan,et al.  Beneficial effects of phytoestrogens and their metabolites produced by intestinal microflora on bone health , 2013, Applied Microbiology and Biotechnology.

[9]  V. Luine,et al.  Estrogens facilitate memory processing through membrane mediated mechanisms and alterations in spine density , 2012, Frontiers in Neuroendocrinology.

[10]  A. Fernández-Guasti,et al.  Synergistic effect of estradiol and fluoxetine in young adult and middle-aged female rats in two models of experimental depression , 2012, Behavioural Brain Research.

[11]  Shu-Lin Liu,et al.  The antidepressant effect of secoisolariciresinol, a lignan-type phytoestrogen constituent of flaxseed, on ovariectomized mice , 2012, Journal of Natural Medicines.

[12]  P. Kandi,et al.  Nicotine and 17β-estradiol produce an antidepressant-like effect in female ovariectomized rats , 2011, Brain Research Bulletin.

[13]  V. Ramirez-Amaya,et al.  Increase of mushroom spine density in CA1 apical dendrites produced by water maze training is prevented by ovariectomy , 2011, Brain Research.

[14]  G. Chrousos,et al.  Fatty Acids Derived from Royal Jelly Are Modulators of Estrogen Receptor Functions , 2010, PloS one.

[15]  D. Lorrain,et al.  Estrogen receptor (ER) subtype agonists alter monoamine levels in the female rat brain , 2010, The Journal of Steroid Biochemistry and Molecular Biology.

[16]  V. Luine,et al.  Estradiol and ERβ agonists enhance recognition memory, and DPN, an ERβ agonist, alters brain monoamines , 2010, Neurobiology of Learning and Memory.

[17]  W. Wuttke,et al.  Effects of estrogen receptor alpha- and beta-selective substances in the metaphysis of the tibia and on serum parameters of bone and fat tissue metabolism of ovariectomized rats. , 2008, Bone.

[18]  V. Henderson Cognitive changes after menopause: influence of estrogen. , 2008, Clinical obstetrics and gynecology.

[19]  P. Mermelstein,et al.  Membrane Estrogen Receptors Acting Through Metabotropic Glutamate Receptors: An Emerging Mechanism of Estrogen Action in Brain , 2008, Molecular Neurobiology.

[20]  D. Kimmel,et al.  Agonist-like SERM effects on ERα-mediated repression of MMP1 promoter activity predict in vivo effects on bone and uterus , 2008, The Journal of Steroid Biochemistry and Molecular Biology.

[21]  L. Abramson,et al.  The ABCs of depression: integrating affective, biological, and cognitive models to explain the emergence of the gender difference in depression. , 2008, Psychological review.

[22]  T. Miyata,et al.  Estrogenic Activities of Fatty Acids and a Sterol Isolated from Royal Jelly , 2007, Evidence-based complementary and alternative medicine : eCAM.

[23]  A. Walf,et al.  Antisense oligodeoxynucleotides for estrogen receptor-beta and alpha attenuate estradiol's modulation of affective and sexual behavior, respectively. , 2008, Neuropsychopharmacology : official publication of the American College of Neuropsychopharmacology.

[24]  A. Walf,et al.  Antisense Oligodeoxynucleotides for Estrogen Receptor-β and α Attenuate Estradiol's Modulation of Affective and Sexual Behavior, Respectively , 2008, Neuropsychopharmacology.

[25]  H. Fukumitsu,et al.  Royal jelly and its unique fatty acid, 10-hydroxy-trans-2-decenoic acid, promote neurogenesis by neural stem/progenitor cells in vitro. , 2007, Biomedical research.

[26]  H. Fukumitsu,et al.  Royal jelly-induced neurite outgrowth from rat pheochromocytoma PC12 cells requires integrin signal independent of activation of extracellular signal-regulated kinases. , 2007, Biomedical research.

[27]  L. Altshuler,et al.  Estrogen and response to sertraline in postmenopausal women with major depressive disorder: a pilot study. , 2007, Journal of psychiatric research.

[28]  K. Anstey,et al.  Hormone replacement therapy and cognitive performance in postmenopausal women—a review by cognitive domain , 2006, Neuroscience & Biobehavioral Reviews.

[29]  V. Luine,et al.  Ovariectomized rats show decreased recognition memory and spine density in the hippocampus and prefrontal cortex , 2006, Brain Research.

[30]  M. Sammel,et al.  Associations of hormones and menopausal status with depressed mood in women with no history of depression. , 2006, Archives of general psychiatry.

[31]  I. Lambrinoudaki,et al.  Quality of life and psychological symptoms in Greek postmenopausal women: Association with hormone therapy , 2006, Gynecological endocrinology : the official journal of the International Society of Gynecological Endocrinology.

[32]  S. Gentile The Role of Estrogen Therapy in Postpartum Psychiatric Disorders: An Update , 2005, CNS Spectrums.

[33]  Peter J. Schmidt Depression, the Perimenopause, and Estrogen Therapy , 2005, Annals of the New York Academy of Sciences.

[34]  C. Bincoletto,et al.  Effects produced by Royal Jelly on haematopoiesis: relation with host resistance against Ehrlich ascites tumour challenge. , 2005, International immunopharmacology.

[35]  B. Rocha,et al.  17 Beta-estradiol-induced antidepressant-like effect in the forced swim test is absent in estrogen receptor-beta knockout (BERKO) mice. , 2005, Psychopharmacology.

[36]  B. Rocha,et al.  17β-Estradiol-induced antidepressant-like effect in the Forced Swim Test is absent in estrogen receptor-β knockout (BERKO) mice , 2005, Psychopharmacology.

[37]  D. Bick Caesarean Section. Clinical Guideline. National Collaborating Centre for Women's and Children's Health: commissioned by the National Institute for Clinical Excellence. , 2004, Worldviews on evidence-based nursing.

[38]  E. Weiderpass,et al.  Risks of breast and endometrial cancer after estrogen and estrogen–progestin replacement , 1999, Cancer Causes & Control.

[39]  K. Kohno,et al.  Major royal jelly protein 3 modulates immune responses in vitro and in vivo. , 2003, Life sciences.

[40]  A. Fernández-Guasti,et al.  Antidepressant-Like Effect of Different Estrogenic Compounds in the Forced Swimming Test , 2003, Neuropsychopharmacology.

[41]  K Yaffe,et al.  Hormone replacement therapy for cognitive function in postmenopausal women. , 2008, The Cochrane database of systematic reviews.

[42]  P. Albertazzi Purified phytoestrogens in postmenopausal bone health: is there a role for genistein? , 2002, Climacteric : the journal of the International Menopause Society.

[43]  D. Pfaff,et al.  Printed in U.S.A. Copyright © 2001 by The Endocrine Society Deficits in E2-Dependent Control of Feeding, Weight Gain, and Cholecystokinin Satiation in ER- � Null Mice , 2022 .

[44]  J. Janowsky,et al.  Hormone replacement therapy and cognition: systematic review and meta-analysis. , 2001, JAMA.

[45]  R. Dahiya,et al.  Regulation of Progesterone Receptors and Decidualization in Uterine Stroma of the Estrogen Receptor-α Knockout Mouse1 , 2001, Biology of reproduction.

[46]  D. Pfaff,et al.  Deficits in E2-dependent control of feeding, weight gain, and cholecystokinin satiation in ER-alpha null mice. , 2001, Endocrinology.

[47]  K. Korach Estrogen Receptor Knock-Out Mice: Molecular and Endocrine Phenotypes , 2000, The Journal of the Society for Gynecologic Investigation: JSGI.

[48]  D. Pfaff,et al.  Estrogen alters behavior and forebrain c-fos expression in ovariectomized rats subjected to the forced swim test. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[49]  B. Popko,et al.  New perspectives on the function of myelin galactolipids , 1998, Trends in Neurosciences.

[50]  U. Halbreich Role of estrogen in postmenopausal depression , 1997, Neurology.

[51]  C. Woolley,et al.  Estradiol Increases the Sensitivity of Hippocampal CA1 Pyramidal Cells to NMDA Receptor-Mediated Synaptic Input: Correlation with Dendritic Spine Density , 1997, The Journal of Neuroscience.

[52]  B. Sherwin,et al.  "Add-back" estrogen reverses cognitive deficits induced by a gonadotropin-releasing hormone agonist in women with leiomyomata uteri. , 1997, The Journal of clinical endocrinology and metabolism.

[53]  B. Gorzalka,et al.  Serum estradiol concentration required to maintain body weight, attractivity, proceptivity, and receptivity in the ovariectomized female rat , 1991, Physiology & Behavior.

[54]  S. Tagliavini,et al.  Influence of ovariectomy, estradiol and progesterone on the behavior of mice in an experimental model of depression , 1989, Physiology & Behavior.