Skip to main content
SpringerLink
Log in

Neurotherapeutic Effects of Bee Venom in a Rotenone-Induced Mouse Model of Parkinson’s Disease

  • Published:
Neurophysiology Aims and scope

Parkinson’s disease (PD) is a widespread progressive neurodegenerative disease; its main neuropathological hallmark is massive loss of dopaminergic neurons. Most PD studies were focused on the basal ganglia. However, the cerebral cortex, hippocampus, and striatum also play certain roles in PD pathophysiology. Dopamine replacement therapies remain the most effective clinical option for PD patients despite the occasional severe side effects. Bee Venom (BV) produced by Africanized honey bee, Apis mellifera L., is rich in neuroactive molecules; this venom is an irrefutable source of neuroprotectors and neuromodulators. In our study, we evaluated the neurotherapeutic effects of Egyptian BV against PD hallmarks in a PD mouse model. Six subcutaneous injections of 1.5 mg/kg of rotenone at 48-h-long intervals induced significant reductions in the motor strength and motor coordination. Additionally, significant declines in the dopamine level and total antioxidant capacity combined with significant elevation in interleukin 1β and interleukin 6 were observed. Rotenone-treated mice showed nuclear pyknosis and neuronal degeneration in the cerebral cortex and hippocampus, eosinophilic plaques, and hemorrhages in the striatum focal area and nuclear pyknosis and neuronal degeneration with diffuse gliosis in other brain structures. In rotenone-treated mice, i.p. injections of BV (6 doses 1.0 mg/kg at 24-h-long interval) recovered motor strength and motor coordination. Moreover, BV markedly increased the dopamine level and total antioxidant capacity. Also, BV greatly reduced the interleukin 1β and interleukin 6 contents. Furthermore, BV preserved neurons in the dentate gyrus of the hippocampus with no histopathological alterations. Besides, BV restricted nuclear pyknosis and neuronal degeneration in a few neurons in the cerebral cortex, hippocampus, and focal area of the striatum. Overall, BV may be a promising biotherapy for PD patients.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. W. Dauer and S. Przedborski, “Parkinson’s disease: mechanisms and models,” Neuron, 39, No. 6, 889–909 (2003).

    CAS  Google Scholar 

  2. W. G. Meissner, M. Frasier, T. Gasser, et al., “Priorities in Parkinson’s disease research,” Nat. Rev. Drug Discov., 10¸ No. 5, 377–393 (2011).

  3. K. S. Kim, “Toward neuroprotective treatments of Parkinson’s disease,” Proc. Natl. Acad. Sci. USA, 114, No. 15, 3795–3797 (2017).

    CAS  PubMed  Google Scholar 

  4. G. C. Cotzias, P. S. Papavasiliou, and R. Gellene, “Modification of Parkinsonism--chronic treatment with L-dopa,” N. Engl. J. Med., 280, No. 7, 337–345 (1969).

    CAS  PubMed  Google Scholar 

  5. M. S. Okun, “Deep-brain stimulation for Parkinson’s disease,” N. Engl. J. Med., 367, No. 16, 1529-1538 (2012).

    CAS  PubMed  Google Scholar 

  6. S. Duty and P. Jenner, “Animal models of Parkinson’s disease: a source of novel treatments and clues to the cause of the disease,” Br. J. Pharmacol., 164, No. 4, 1357–1391 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  7. R. Betarbet, T. B. Sherer, G. MacKenzie, et al., “Chronic systemic pesticide exposure reproduces features of Parkinson’s disease,” Nat. Neurosci., 3, No. 12, 1301–1306 (2000).

    CAS  PubMed  Google Scholar 

  8. F. Cicchetti, J. Drouin-Ouellet, and R. E. Gross, “Environmental toxins and Parkinson’s disease: what have we learned from pesticide-induced animal models?” Trends Pharmacol. Sci., 30, No. 9, 475–483 (2009).

    CAS  PubMed  Google Scholar 

  9. J. T. Greenamyre, J. R. Cannon, R. Drolet, and P. G. Mastroberardino, “Lessons from the rotenone model of Parkinson’s disease,” Trends Pharmacol. Sci., 31, No. 4, 141–142, author reply 142–143 (2010).

  10. T. B. Sherer, R. Betarbet, C. M. Testa, et al., “Mechanism of toxicity in rotenone models of Parkinson’s disease,” J. Neurosci., 23, No. 34, 10756–10764 (2003).

    CAS  PubMed  Google Scholar 

  11. Z. I. Alam, S. E. Daniel, A. J. Lees, et al..”A generalised increase in protein carbonyls in the brain in Parkinson’s but not incidental Lewy body disease,” J. Neurochem., 69, No. 3, 1326–1329 (1997).

    CAS  PubMed  Google Scholar 

  12. T. B Sherer, R. Betarbet, J. H. Kim, and J. T. Greenamyre, “Selective microglial activation in the rat rotenone model of Parkinson’s disease,” Neurosci. Lett., 341, No. 2, 87–90 (2003).

    CAS  PubMed  Google Scholar 

  13. A. Gerhard, N. Pavese, G. Hotton, et al., “In vivo imaging of microglial activation with [11C](R)-PK11195 PET in idiopathic Parkinson’s disease,” Neurobiol. Dis., 21, No. 2, 404–412 (2006).

    CAS  PubMed  Google Scholar 

  14. P. S. Whitton, “Inflammation as a causative factor in the aetiology of Parkinson’s disease,” Br. J. Pharmacol., 150, No. 8, 963-976 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  15. M. G. Tansey and M. S. Goldberg, “Neuroinflammation in Parkinson’s disease: its role in neuronal death and implications for therapeutic intervention,” Neurobiol. Dis., 37, No. 3, 510–518 (2010).

    CAS  PubMed  Google Scholar 

  16. X. F. Wang, S. Li, A. P. Chou, and J. M. Bronstein, “Inhibitory effects of pesticides on proteasome activity: implication in Parkinson’s disease,” Neurobiol. Dis., 23, No. 1, 198–205 (2006).

    PubMed  Google Scholar 

  17. R. S. Ferreira-Junior, J. M. Sciani, R. Marques-Porto, et al., “Africanized honey bee (Apis mellifera) venom profiling: Seasonal variation of melittin and phospholipase A2 levels,” Toxicon, 56, No. 3, 355–362 (2010).

    PubMed  Google Scholar 

  18. J. M. Sciani, R. Marques-Porto, A. Lourenço Jun, et al., “Identification of a novel melittin isoform from Africanized Apis mellifera venom,” Peptides, 31, No. 8, 1473–1479 (2010).

    CAS  PubMed  Google Scholar 

  19. C. G. Dantas, T. L. G. M. Nunes, T. L. G. M. Nunes, et al., Pharmacological evaluation of bee venom and melittin,” Rev. Brasil. Farmacogn., 24, No. 1, 67–72 (2014).

    CAS  Google Scholar 

  20. D. J. Son, J. W. Lee, Y. H. Lee, et al., “Therapeutic application of anti-arthritis, pain-releasing, and anti-cancer effects of bee venom and its constituent compounds,” Pharmacol. Ther., 115, No. 2, 246–270 (2007).

    CAS  PubMed  Google Scholar 

  21. E. J. Yang, J. H. Jiang, S. M. Lee, et al., “Bee venom attenuates neuroinflammatory events and extends survival in amyotrophic lateral sclerosis models,” J. Neuroinflamm., 7, No. 1, 69–81 (2010).

    Google Scholar 

  22. E. J. Yang, S. H Kim, S. C. Yang, et al., “Melittin restores proteasome function in an animal model of ALS,” J. Neuroinflammation, 8, No. 1, 69-78 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  23. A. R. Doo, S. T. Kim, S. N. Kim, et al., “Neuroprotective effects of bee venom pharmaceutical acupuncture in acute 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridineinduced mouse model of Parkinson’s disease,” Neurol. Res., 32, Suppl. 1, 88–91 (2010).

    PubMed  Google Scholar 

  24. J. I. Kim, E. J. Yang, M. S. Lee, et al., “Bee venom reduces neuroinflammation in the MPTP-induced model of Parkinson’s disease,” Int. J. Neurosci., 121, No. 4, 209–217 (2011).

    CAS  PubMed  Google Scholar 

  25. A. R. Doo, S. N. Kim, S. T. Kim, et al., “Bee venom protects SH-SY5Y human neuroblastoma cells from 1-methyl-4-phenylpyridinium-induced apoptotic cell death,” Brain Res., 1429, 106–115 (2012).

    CAS  PubMed  Google Scholar 

  26. S. Y. Cho, S. R. Shim, H. Y. Rhee, et al., “Effectiveness of acupuncture and bee venom acupuncture in idiopathic Parkinson’s disease,” Parkinsonism Relat. Disord., 18, No. 8, 948–952 (2012).

    PubMed  Google Scholar 

  27. E. S. Chung, H. Kim, G. Lee, et al., “Neuro-protective effects of bee venom by suppression of neuroinflammatory responses in a mouse model of Parkinson’s disease: Role of regulatory T cells,” Brain Behav. Immun., 26, No. 8, 1322–1330 (2012).

    CAS  PubMed  Google Scholar 

  28. S. M. Lee, E. J. Yang, S. M. Choi, et al., “Effects of bee venom on glutamate-induced toxicity in neuronal and glial cells,” Evid. Based Complement. Alternat. Med., Article ID 368196, 9 pages, doi: 10.1155/2012/368196 (2012).

  29. Y. B. Kwon, H. J. Han, A. J. Beitz, and J. H. Lee, “Bee venom acupoint stimulation increases Fos expression in catecholaminergic neurons in the rat brain,” Mol. Cells, 17, No. 2, 329–333 (2004).

    CAS  PubMed  Google Scholar 

  30. K. W. Kim, H. W. Kim, J. Li, and Y. B. Kwon, “Effect of bee venom acupuncture on methamphetamine-induced hyperactivity, hyperthermia and Fos expression in mice,” Brain Res. Bull., 84, No. 1, 61–68 (2011).

    CAS  PubMed  Google Scholar 

  31. H. W. Kim, Y. B. Kwon, T. W. Ham, et al., “General pharmacological profiles of bee venom and its water soluble fractions in rodent models,” J. Vet. Sci., 5, No. 4, 309–318 (2004).

    PubMed  Google Scholar 

  32. Z. I. Nabil, A. A. Hussein, S. M. Zalat, and M. K. Rakha, “Mechanism of action of honey bee (Apis mellifera L.) venom on different types of muscles,” Hum. Exp. Toxicol., 17, No. 3, 185–190 (1998).

    CAS  PubMed  Google Scholar 

  33. J. O. Schmidt, “Toxinology of venoms from the honey bee, Genus Apis,” Toxicon, 33, No. 7, 917–927 (1995).

    CAS  PubMed  Google Scholar 

  34. W. K. Khalil, N. Assaf, S. A. El Shebiney, and N. A. Salem, “Neuroprotective effects of bee venom acupuncture therapy against rotenone-induced oxidative stress and apoptosis,” Neurochem. Int., 80, 79–86 (2015).

    CAS  PubMed  Google Scholar 

  35. R. M. Deacon, “Measuring motor coordination in mice,” J. Vis. Exp., 75, e2609 (2013).

  36. S. Chompoopong, S. Jarungjitaree, T. Punbanlaem, et al., “Neuroprotective effects of germinated brown rice in rotenone-induced Parkinson’s-like disease rats,” Neuromol. Med., 18, No. 3, 334–346 (2016).

    CAS  Google Scholar 

  37. J. D. Bancroft and M. Gamble, Theory and Practice of Histological Techniques, 6th ed., Churchill Livingstone, Edinburgh. 2008.

  38. K. Awad, A. I. Abushouk, A. H. AbdelKarim, et al., “Bee venom for the treatment of Parkinson’s disease: How far is it possible?” Biomed. Pharmacother., 91, 295–302 (2017).

    CAS  PubMed  Google Scholar 

  39. M. A. Cenci and M. Lundblad, “Utility of 6-hydroxydopamine lesioned rats in the preclinical screening of novel treatments of Parkinsonism disease” in Animal Models of Movement Disorders, Chapter B7, 193–208 (2005).

  40. A. Serretti, R. Calati, L Mandelli, and D. De Ronchi, “Serotonin transporter gene variants and behavior: a comprehensive review,” Curr. Drug Targets, 7, No. 12, 1659–1669 (2006).

  41. C. Zhou, Y. Huang, and S. Przedborski, “Oxidative stress in Parkinson’s disease: a mechanism of pathogenic and therapeutic significance,” Ann. N.Y. Acad. Sci., 1147, No. 1, 93–104 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  42. S. A. Thomas and R. D. Palmiter, “Disruption of the dopamine beta-hydroxylase gene in mice suggests roles for norepinephrine in motor function, learning, and memory,” Behav. Neurosci., 111, No. 3, 579–589 (1997).

    CAS  PubMed  Google Scholar 

  43. L. M. Shulman, X. Wen, W. J. Weiner, et al., “Acupuncture therapy for the symptoms of Parkinson’s disease,” Mov. Disord., 17, No. 4, 799–802 (2002).

    PubMed  Google Scholar 

  44. A. Cristian, M. Katz, E. Cutrone, and R. H. Walker, “Evaluation of acupuncture in the treatment of Parkinson’s disease: a double-blind pilot study,” Mov. Disord., 20, No. 9, 1185–1188 (2005).

    PubMed  Google Scholar 

  45. Y. Huang, X. Jiang, X. Zhuo, and Y. Wik, “Complementary acupuncture in Parkinson’s disease: a SPECT study,” Int. J. Neurosci., 120, No. 2, 150–154 (2010).

    CAS  PubMed  Google Scholar 

  46. J. Matysiak, C. E. Schmelzer, R. H. Neubert, and Z. J. Kokot, “Characterization of honeybee venom by MALDI-TOF and nanoESI-QqTOF mass spectrometry,” J. Pharm. Biomed. Anal., 54, No. 2, 273–278 (2011).

    CAS  PubMed  Google Scholar 

  47. D. Alvarez-Fischer, C. Noelker, F. Vulinović, et al., “Bee venom and its component apamin as neuroprotective agents in a Parkinson disease mouse model,” PLoS One, 8, No.4, e61700 (2013).

  48. N. Maurice, T. Deltheil, C. Melon, et al., Bee venom alleviates motor deficits and modulates the transfer of cortical information through the basal ganglia in rat models of Parkinson’s disease,” PLoS One, 10, No. 11, e0142838 (2015).

  49. J. D. Steketee and P. W. Kalivas, “Effect of microinjections of apamin into the A10 dopamine region of rats: a behavioral and neurochemical analysis,” J. Pharmacol. Exp. Ther., 254, No. 2, 711–719 (1990).

    CAS  PubMed  Google Scholar 

  50. S. Yang and G. Carrasquer, “Effect of melittin on ion transport across cell membranes,” Acta Pharmacol. Sin./ Zhongguo Yao Li Xue Bao, 18, No. 1, 3–5 (1997).

  51. B. Salthun-Lassalle, E. C. Hirsch, J. Wolfart, et al., “Rescue of mesencephalic dopaminergic neurons in culture by low-level stimulation of voltage-gated sodium channels,” J. Neurosci., 24, No. 26, 5922–5930 (2004).

    CAS  PubMed  Google Scholar 

  52. J. Sian, D. T Dexter, A. J. Lees, et al., “Alterations in glutathione levels in Parkinson’s disease and other neurodegenerative disorders affecting basal ganglia,” Ann. Neurol., 36, No. 3, 348–355 (1994).

    CAS  PubMed  Google Scholar 

  53. R. L. Miller, M. James-Kracke, G. Y. Sun, and A. Y. Sun, “Oxidative and inflammatory pathways in Parkinson’s disease,” Neurochem. Res., 34, No. 1, 55–65 (2009).

    CAS  PubMed  Google Scholar 

  54. E. Milusheva, M. Baranyi, E. Kormos, et al., “The effect of antiparkinsonian drugs on oxidative stress induced pathological [3H]dopamine efflux after in vitro rotenone exposure in rat striatal slices,” Neuropharmacology, 58, Nos. 4–5, 816–825 (2010).

  55. K. Radad, W. D. Rausch, and G. Gille, “Rotenone induces cell death in primary dopaminergic culture by increasing ROS production and inhibiting mitochondrial respiration,” Neurochem. Int., 49, No. 4, 379–386 (2006).

    CAS  PubMed  Google Scholar 

  56. H. M. A. Gawad, D. M. Abdallah, and H. S. El-Abhar, “Rotenone-induced Parkinson’s like disease: modulating role of coenzyme Q10,” J. Biol. Sci., 4, No. 4, 568–574 (2004).

    Google Scholar 

  57. S. A. Zaitone, D. M. Abo-Elmatty, and A. A. Shaalan, “Acetyl-L-carnitine and α-lipoic acid affect rotenoneinduced damage in nigral dopaminergic neurons of rat brain; implication for Parkinson’s disease therapy,” Pharmacol. Biochem. Behav., 100, No. 3, 347–360 (2012).

    CAS  PubMed  Google Scholar 

  58. M. Rosenblat and M. Aviram, “Paraoxonases role in the prevention of cardiovascular diseases,” Biofactors, 35, No. 1, 98–104 (2009).

    CAS  PubMed  Google Scholar 

  59. K. Ikeda, Y. Nakamura, T. Kiyozuka, et al., “Serological profiles of urate, paraoxonase-1, ferritin and lipid in Parkinson’s disease: changes linked to disease progression,” Neurodegener. Dis., 8, No. 4, 252–258 (2011).

    CAS  PubMed  Google Scholar 

  60. B. Drukarch and F. L. van Muiswinkel, “Drug treatment of Parkinson’s disease. Time for phase II,” Biochem. Pharmacol., 59, No. 9, 1023–1031 (2000).

  61. T. V. Ilic, M. Jovanovic, A. Jovicic, and M. Tomovic, “Oxidative stress indicators are elevated in de novo Parkinson’s disease patients,” Funct. Neurol., 14, No. 3, 141–147 (1999).

    CAS  PubMed  Google Scholar 

  62. A. Ghiselli, M. Serafini, F. Natella, and C. Scaccini, “Total antioxidant capacity as a tool to assess redox status: critical view and experimental data,” Free Radic. Biol. Med., 29, No. 11, 1106–1114 (2000).

    CAS  PubMed  Google Scholar 

  63. Y. G. Choi, J. H. Park, and S. Lim, “Acupuncture inhibits ferric iron deposition and ferritin-heavy chain reduction in an MPTP-induced parkinsonism model,” Neurosci. Lett., 450, No. 2, 92–96 (2009).

    CAS  PubMed  Google Scholar 

  64. H. M. Gao, B. Liu, W. Zhang, and J. S. Hong, “Novel anti-inflammatory therapy for Parkinson’s disease,” Trends Pharmacol. Sci., 24, No. 8, 395–401 (2003).

    CAS  PubMed  Google Scholar 

  65. M. Mogi, M. Harada, P. Riederer, et al., “Tumor necrosis factor-alpha (TNF-α) increases both in the brain and in the cerebrospinal fluid from parkinsonian patients,” Neurosci. Lett., 165, Nos. 1–2, 208–210 (1994).

  66. T. Nagatsu, M. Mogi, H. Ichinose, and A. Togari, “Cytokines in Parkinson’s disease,” J. Neural Transm. Suppl., 58, 143–151 (2000).

    Google Scholar 

  67. K. W. Nam, K. H. Je, J. H. Lee, et al., “Inhibition of COX-2 activity and proinflammatory cytokines (TNFalpha and IL-1beta) production by water-soluble subfractionated parts from bee (Apis mellifera) venom,” Arch. Pharm. Res., 26, No. 5, 383–388 (2003).

    CAS  PubMed  Google Scholar 

  68. H. J. Park, D. J. Son, C. W. Lee, et al., “Melittin inhibits inflammatory target gene expression and mediator generation via interaction with IkappaB kinase,” Biochem. Pharmacol., 73, No. 2, 237–247 (2007).

    CAS  PubMed  Google Scholar 

  69. J. H. Lee, Y. C. Li, S. W. Ip, et al., “The role of Ca2+ in baicalein-induced apoptosis in human breast MDA-MB-231 cancer cells through mitochondria- and caspase-3-dependent pathway,” Anticancer Res., 28, No. 3A, 1701–1711 (2008).

  70. H. S. Jang, S. K. Kim, J. B. Han, et al., “Effects of bee venom on the pro-inflammatory responses in RAW264.7 macrophage cell line,” J. Ethnopharmacol., 99, No. 1, 157–160 (2005).

    CAS  PubMed  Google Scholar 

  71. S. S. Saini, J. W. Peterson, and A. K. Chopra, “Melittin binds to secretory phospholipase A2 and inhibits its enzymatic activity,” Biochem. Biophys. Res. Commun., 238, No. 2, 436–442 (1997).

    CAS  PubMed  Google Scholar 

  72. E. D. Mihelich and R. W. Schevitz, “Structure-based design of a new class of anti-inflammatory drugs: secretory phospholipase A2 inhibitors, SPI,” Biochim. Biophys. Acta., 1441, Nos. 2–3, 223–228 (1999).

  73. D. O. Moon, S. Y. Park, K. J. Lee, et al., “Bee venom and melittin reduce proinflammatory mediators in lipopolysaccharide-stimulated BV2 microglia,”, Int. Immunopharmacol., 7, No. 8, 1092–1101 (2007).

  74. T. Lawrence, “The nuclear factor NF-кB pathway in inflammation,” Cold Spring Harb. Perspect. Biol., 1, No. 6, a001651 (2009).

  75. H. Mochizuki, K. Goto, H. Mori, and Y. Mizuno, “Histochemical detection of apoptosis in Parkinson’s disease,” J. Neurol. Sci., 137, No. 2, 120–123 (1996).

    CAS  PubMed  Google Scholar 

  76. D. Blum, S. Torch, N. Lambeng, et al., “Molecular pathways involved in the neurotoxicity of 6-OHDA, dopamine and MPTP: contribution to the apoptotic theory in Parkinson’s disease,” Prog. Neurobiol., 65, No. 2, 135–172 (2001).

  77. W. G. Tatton, R. Chalmers-Redman, D. Brown, and N. Tatton, “Apoptosis in Parkinson’s disease: signals for neuronal degradation,” Ann. Neurol., 53, No. 3, S61–S72 (2003).

    CAS  PubMed  Google Scholar 

  78. T. M. Miller, K. L. Moulder, C. M. Knudson, et al., “Bax deletion further orders the cell death pathway in cerebellar granule cells and suggests a caspaseindependent pathway to cell death,” J. Cell Biol., 139, No. 1, 205–217 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  79. D. A. Le, Y. Wu, Z. Huang, et al., “Caspase activation and neuroprotection in caspase-3-deficient mice after in vivo cerebral ischemia and in vitro oxygen glucose deprivation,” Proc. Natl. Acad. Sci., 99, No. 23, 15188–15193 (2002).

    CAS  PubMed  Google Scholar 

  80. E. M. Halvorsen, J. Dennis, P. Keeney, et al., “Methylpyridinium (MPP+)-and nerve growth factorinduced changes in pro-and anti-apoptotic signaling pathways in SH-SY5Y neuroblastoma cells,” Brain Res., 952, No. 1, 98–110 (2002).

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Pharmacology and Biochemistry Department, Faculty of Pharmacy, The British University in Egypt, Cairo, 11837, Egypt

    M. K. Rakha, R. A. Tawfiq, M. M. Sadek, M. A. Anwer, S. M. Salama, A. F. Mohamed, M. G. El-Hendy, Sh. E. El-Said, N. M. Ahmed, K. S. Mekawi, A. M. Abd El-Aziz & M. M. Elmazar

Authors
  1. M. K. Rakha
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. R. A. Tawfiq
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. M. M. Sadek
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. M. A. Anwer
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. S. M. Salama
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. A. F. Mohamed
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. M. G. El-Hendy
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Sh. E. El-Said
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. N. M. Ahmed
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. K. S. Mekawi
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. A. M. Abd El-Aziz
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. M. M. Elmazar
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to M. K. Rakha.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rakha, M.K., Tawfiq, R.A., Sadek, M.M. et al. Neurotherapeutic Effects of Bee Venom in a Rotenone-Induced Mouse Model of Parkinson’s Disease. Neurophysiology 50, 445–455 (2018). https://doi.org/10.1007/s11062-019-09777-w

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11062-019-09777-w

Keywords

Search

Navigation