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J Gericke Orcid.Org/ 0000-0003-0038-3374 Evaluating the antidepressant-like properties of Sceletium tortuosum, alone and as adjunctive treatment J Gericke orcid.org/ 0000-0003-0038-3374 Dissertation submitted in fulfilment of the requirements for the degree Master of Science in Pharmacology at the North West University Supervisor: Prof BH Harvey Co-supervisor: Dr M Lekhooa Examination: May 2019 Student number: 25045288 “Science without religion is lame. Religion without science is blind." Albert Einstein Abstract ABSTRACT BACKGROUND: Millions of people worldwide suffer from major depressive disorder (MDD) which can cause physical and emotional suffering for patients and their loved-ones. Unfortunately current treatment fails in approximately a third of MDD patients. This may be attributed to numerous side effects, delayed onset of action, and ineffective targeting of the many different, interrelated biological systems. This includes structural and functional brain alterations driven especially by decreased brain-derived neurotrophic factor (BDNF), and neurotransmitter abnormalities such as reduced monoamines (serotonin (5-HT), dopamine (DA) and norepinephrine (NE)). Evidently, new and more effective treatments are urgently needed. Fortunately, complementary medicines like plants and herbs with antidepressant effects offer untapped potential. This study set out to evaluate the antidepressant potential of the South African plant, Sceletium tortuosum (L.) N.E.Br. (Zembrin®) (ST), which displays diverse pharmacological attributes that offer potential antidepressant activity, e.g. 5-HT transporter (SERT) inhibition, upregulation of vesicular monoamine transporter 2 (VMAT-2), mild MAO-A inhibition, and inhibition of phosphodiesterase 4 (PDE4). These mechanisms have almost all been studied in vitro, leaving an urgent need for in vivo studies. Furthermore, ST has not been tested in combination with known antidepressant compounds to evaluate its potential as a possible augmentative therapy for MDD. AIM: To use acute and sub-chronic treatment paradigms with biobehavioural parameters to evaluate the antidepressant-like properties of ST, alone and in combination with the selective 5-HT reuptake inhibitor (SSRI), escitalopram (ESC), in the FSL rat. METHODOLOGY: 1) A fingerprint analysis of the alkaloid profile of ST was done using an ultra- performance liquid chromatography - tandem mass spectrometer (UPLC-MS). 2) Behavioural confirmation of the FSL model of MDD. 12 saline-treated FSL and 6 Flinders Resistant Line (FRL) rats (reference control) were used to confirm the depressive phenotype of the FSL rat, using the open field test (OFT) and forced swim test (FST). 3) Acute dose response studies in FSLs, using a 3-tier dose response with escitalopram oxalate (ESC) (3 groups (n = 10); 5, 10 or 20 mg/kg), and a 5-tier dose response with ST (5 groups (n = 10); 5, 10, 25, 50 or 100 mg/kg). Treatment spanned over 24 hours, followed by the OFT and FST. The results were used to establish a low- dose of ESC, and a therapeutic dose of ST. 4) A sub-chronic treatment response study wherein four groups of FSL rats (n = 12) received a) saline, b) low dose of ESC, c) a therapeutic dose of ST or d) combination therapy of ESC + ST, over 15 days. After the OFT and FST on days 13 and i Abstract 15, animals were decapitated, with hippocampus and frontal cortex samples harvested for analysis of monoamines and BDNF. RESULTS: Four main alkaloids were identified and quantified in an UPLSC-MS chromatogram. FSL rats presented with significantly decreased swimming and struggling, and increased immobility versus FRL controls, thus reaffirming its face validity as a rodent model of MDD. ST and ESC showed dose-dependent antidepressant responses following acute treatment. ESC 5 mg/kg (ESC 5) was chosen as a low dose of ESC and ST 50 mg/kg (ST 50) was selected as the therapeutic dose of ST. Sub-chronically, ESC 5 and ST 50 alone displayed similar neurochemical changes with no significant antidepressant-like effects. ESC+ST significantly increased hippocampal 5-HT and NE, and locomotor activity, which is normally deemed positive in MDD treatment. However, increased immobility and decreased struggling are indicative of depressogenic effects. Furthermore, hippocampal 5-HT was significantly increased, possibly due to synergistic serotonergic effects of ST 50 and ESC 5. A hypersensitive inhibitory 5-HT1A response, characteristic of FSL rats, could have prompted 5-HT1A receptor-mediated “5-HT behavioural syndrome” presenting as passive coping in the FST and increased locomotion in the OFT. The apparent lack of antidepressant effects in the alone treatment groups may be due to delayed response attributed to delayed desensitization of inhibitory 5-HT1A receptors, typical of SSRIs. ST 50 alone increased hippocampal BDNF indicating potential of ST in the treatment of impaired cognition, ESC + ST reduced frontal cortical BDNF levels. CONCLUSION: ST and ESC induced dose-dependent antidepressant-like effects after acute treatment, however not after sub-chronic treatment. Combined sub-chronic treatment with ESC + ST appears to be depressogenic, displaying significant serotonergic activity at behavioural and neurochemical levels. ST 50 increasing hippocampal BDNF levels suggests promise in the treatment of mood and cognitive disorders. Keywords Major depressive disorder (MDD), Sceletium tortuosum, forced swim test, open field test, 5-HT1A, 5-HT2A, brain-derived neurotrophic factor (BDNF), neuroplasticity, serotonin behavioural syndrome. ii Abstract Graphical abstract iii Congress Proceedings CONGRESS PROCEEDINGS Excerpts from this study were presented as a podium presentation at the 2019 SANS symposium as part of the Biological Psychiatry Congress in Cape Town, South Africa (20 – 23 September 2019) under the title: Preliminary evidence of the antidepressant-like properties of Sceletium tortuosum (ZembrinTM) in a genetic animal model of depression Johané Gericke, Brian H. Harvey, Makhotso Lekhooa, Stephan Steyn, Alvaro M. Viljoen iv Acknowledgements ACKNOWLEDGEMENTS Firstly, thank you Lord for the opportunity you gave me to gain knowledge and skills which helped me realise how small yet complex we as humans are. You intricately made us in such a way that, no matter how hard we try, we will never be able to fully understand the inner mechanisms of life and nature. Thank you for carrying me through these two years with all its joys, frustrations, stress and victories. Thank you for sending amazing new friends and colleagues on my way in addition to my wonderful, loving family and “old” friends. I know that without you, I would be nothing. I would like to thank the following people for their help, guidance, motivation, moral support and kindness. You carried me through the most challenging two years of my life. I could not have done it without any of you. To my brilliant and patient study leader and mentor, Prof Brian Harvey. Thank you for teaching me how to think, act and write like a researcher. Thank you for your hard work and exceptional guidance throughout these two years. You showed me what a passionate, talented researcher looks like and I hope that one day I could live up to your example. To my talented and passionate assistant study leader, Dr Makhotso Lekhooa. Thank you for teaching me the skills to be a successful woman in science. Our conversations always made me see things in a new perspective – scientifically and personally. Thank you for your kindness, mentorship, and motivational speeches when I needed it the most. To my colleagues and close friends, Carmen and Cailin. You guys kept me sane through these two years. Each of you holds a special place in my heart and I can’t imagine doing any of this without you. We experienced a lot of emotional rollercoasters together, and I would not ask for anyone else to share this experience with. Thank you for your love, support, pep talks, socials, jokes and laughter. I love you guys! To my other colleagues, Dr Mr Chair (Geoff), Joné, Heslie, Mandi, Ané, Khulekani, and Juandré. Thank you for all your help, chats, kindness and friendship. You all made a lasting impression on me which I will always be grateful for. You made my time here fun and meaningful. To Prof Linda Brand. Thank you for all your kindness, support and interest. It is always nice to pop in and say hallo. You are always available to help in any way you can and you always listen to us whenever we need a shoulder to cry on. I aspire to be like you – personally and professionally. v Acknowledgements To Dr Stephan Steyn and Dr De Wet Wolmarans. I don’t know what I would have done without the two of you. You taught me how to be passionate about science. You are both brilliant researchers and mentors. Apart from that, you always had time for a problem solving session, crash course on practical aspects of research, and a quick pep talk. Your care and understanding meant the world to me. Thank you for everything from the bottom of my heart. To Dr Francois Viljoen, thank you for your friendly chats and all your help with neurochemical analyses. And to Walter Dreyer, thank you for your help with the ELISA kits. To every other person, lecturer, student and cleaner on our floor. Thank you for your friendliness, input, help and conversations. You all contributed to a very pleasant working environment. To Antoinette Fick, Kobus Venter, Cor Bester, Dr Nico Minnaar, and all other Vivarium personnel. Thank your friendliness and for your assistance during my animal studies. Thank you for teaching me the skills I needed to be able to do this study. I appreciate all your effort. To Prof Alvaro Viljoen. Thank you for all your insets, funding and help with this study. To HG&H. Thank you for supplying the Zembrin used in the study, and for all your help and information regarding Sceletium tortuosum. Mamma en Pappa. Baie dankie vir al die geduld, liefde en ondersteuning wat Ma en Pa vir my gegee het, nie net deur die twee jaar nie, maar deur my 24 jaar op aarde.
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