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was started by stimulating Ach release since the hippocampal formation receives its dopaminergic inputs from the VTA (Scatton et al., 1980; Umegaki et al., 2001) the nicotine-induced hippocampal ACh release may be mediated, in part, via the activation of nAChRs located in the VTA. Dopaminergic regulation of hippocampal ACh release is established from anatomical and functional studies as summarized below.
Hippocampal dopamine receptors have been localized to the molecular layer of the dentate gyrus and the dorsal hippocampus (Tiberi et al., 1991). Significant loss of hippocampal dopamine receptors with a concomitant loss of choline acetyltransferase activity (ChAT) after fimbriaectomy (Hersi et al., 1995) suggests that a subpopulation of the dopamine receptors are presynaptically localized on the cholinergic afferents. These observations, taken together, further support the involvement of nAChR activation of VTA-hippocampal DA-ergic pathway, DA release, dopamine receptor activation in nicotine-induced hippocampal ACh release in vivo. The abundance of Ach in brains leads to increase acetylcholinesterase activity to degrade the Ach to choline and acetate (Dvir et al., 2010), furthermore the important roles of dopaminergic system particularly the critical function of D1 and D2 receptors in nicotine dependence are intriguing to be investigated.
Since dopamine mediates nicotine dependence through the nucleus accumbens and hippocampus, we performed CPP test for 28 days administration of nicotine to establish the nicotine-induced CPP as representative of nicotine reward and reinforcement. Next, we assessed Ca2+/calmodulin-dependent protein kinase II (CaMKII) and extracellular signal-regulated kinase (ERK) signals. We first found that, in addition to D1R antagonist (SCH23390), D2R antagonist (eticlopride) administration with 30 minutes prior to nicotine administration completely abolishes the nicotine dependence in both 2 and 4 weeks nicotine conditioning mice. Although the involvement of dopamine D1 receptor (D1R) has been well
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documented in the nicotine dependence, however, the role of D2R remains unclear. Thus, we investigated whether D2R is critical for nicotine dependence behaviors using D2R knock out (D2RKO) mice. We first assessed the nicotine-induced CPP behaviors in wild type (WT) and D2RKO mice. D2RKO mice were then subjected to neurochemical analyses after conditioning with CPP. Interestingly, D2RKO mice failed to develop the
nicotine-induced CPP behaviors after continuous nicotine administration with 0.5 mg/kg for 4 weeks.
Since both nucleus accumbens and hippocamus have central role in the nicotine-induced CPP behaviors, we investigated both CaMKII and ERK signaling both in the nucleus accumbens and hippocampal CA1 region after 4 weeks administration of nicotine.
Notably, both CaMKII and ERK phosphorylation in both regions were elevated by nicotine administration in WT mice. However, these kinase pathways were unchanged in D2RKO mice. Moreover, the basal levels of CaMKII and ERK phosphorylation were significantly reduced in D2RKO mice. Consistent with immunoblotting results, immunostaining analyses showed the number of phosphorylated CaMKII and ERK positive cells in nucleus accumbens elevated on WT mice but not in D2KO mice after nicotine treatment for 4 weeks administration.
The nicotine-induced CPP behaviors were associated with elevation of Pro-BDNF and BDNF protein levels in WT mice. On the other hand, Pro-BDNF and BDNF protein levels were unchanged after chronic nicotine administration for 28 consecitive days in D2RKO mice. Taken together we propose the possible mechanism how the dopamine D2R pathway generates nicotine-induced CPP behaviors. Nicotine administration activates α4β2nAChRs and α7nAChRs in the dopaminergic terminals. Nicotine administration enhances DA release by stimulation of both nAChRs in wild type mice. The released DA stimulates D2R thereby enhancing MEK and ERK1/2 pathway through enhancement of
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cytosolic tyrosine kinase and in turn causes CREB phosphorylation in nucleus accumbens.
Additionally, D2R activation elevates CaMKII signaling by elevation of intracellular calcium. The CaMKII activation also mediates CREB phosphorylation followed by pro-BDNF production. The pro-pro-BDNF is degraded by proteolytic enzyme to produce mature BDNF. BDNF may be essential for synaptic rearrangement accounting for nicotine-induced CPP behavior. As shown previously, D1R stimulation also mediates BDNF expression through cyclic AMP-dependent protein kinase (PKA) pathway in the different neurons from D2R expressing neurons.
In opposite with WT mice in D2KO mice, stimulation of dopamine release by nicotinic acetylcholine receptor on dopaminergic neuron ((Anderson et al., 2009) unaffected dopamine receptor. Deletion of dopamine D2 receptor on D2KO mice decrease the basal condition of ERK1/2 due to ERK activation induced by dopamine D2R stimulation in mesencephalic dopaminergic neurons related by nuclear ophan receptor Nurr1(Kim, 2006), Besides that absence of D2R reduces the CaMKII activity in D2KO mice, CaMKII binds with the D2R in intracellular loop 3 (IL3) domain (S. Zhang et al., 2014). ERK1/2 and CaMKII activity influenced phosphorylation of CREB in nucleolus (Impey et al., 1998; Yan et al., 2016) and the further action influence BDNF through maturation of proBDNF.
Inactivation D1 receptor by removing D2 receptor in KO mice to have not an impact on activation the PKC pathway and stabilized the BDNF expression via preCREB and proBDNF cycle.
In conclusion, activation of CaMKII and ERK1/2 terminate by the increase of BDNF through D2R are associated with nicotine-induced CPP behavior. Like D1R, D2R is critical for nicotine-induced CPP behavior. BDNF as a new potential target to prevents nicotine dependence due to BDNF involve in LTP of memory formation during nicotine
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administration by activation of NMDA receptor through stimulation tyrosine kinase receptor. On the other hand, activation of BDNF influence spine morphology, BDNF increased spine density by reducing thin spine type and increasing mushroom spine type for affecting neural plasticity during nicotine dependence. Another evidence provide, BDNF Val66Met polymorphism gene involved on nicotine dependence (Lee et al., 2015). We also propose curcuminoid as therapeutic candidate to ameliorate nicotine dependence and relapse.
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ACKNOWLEDGEMENT
In the Name of Allah Subhanallahu wa Ta’ala the Most Compassionate and the Most Merciful. All praise is for Allah Subhanallahu wa Ta’ala due to the blessing in finishing this Ph.D Journey.
I am using this opportunity to express my greatest appreciation to my supervisor, Prof. Dr.
Kohji Fukunaga, for his great supervision, excellent academic advice and strong encouragement during my study on his Laboratory. He taught me the spirit of researcher in finding the novelty of a research. His valuable suggestion, tireless support and unconditional guidance are very important for me in accomplished my mission to pursue my Ph.D degree.
I would like to show the gratitude and respect to my doctoral dissertation committees and doctoral manuscript evaluator Prof. Dr. Noriyasu Hirasawa and Dr. Yasuo Uchida for the fruitful discussion, exchange opinion and constructive suggestion on process of create the scientific manuscript.
I am particularly grateful for the assistance given by Dr. Yasuharu Shinoda, Dr. Yasushi Yabuki, Dr. Shigeki Moriguchi and Dr. Ichiro Kawahata. They countless help to me on performed the experiments have a big contribution on finishing my Ph.D Study.
My gratefulness addressed to all of Prof. Fukunaga’s lab members for their kind help and support throughout the years.
Special thank you would be delivered to Indonesia Endowment Fund for Education (LPDP), Minister of Fund Republic of Indonesia for financial support on my Study and for the Research Grants.
Sincerely thank you addressed to Rector of Universitas Padjadjaran, to the Dean and all of Staffs Faculty of Pharmacy, Universitas Padjadjaran, Bandung, Indonesia for countless
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support and gave me an exit permit to continue my education in School of Pharmaceutical, Tohoku University, Japan.
At this point of my life, I have nothing else to say but word gratitude to everyone who helped me achieve this dream. Become a Ph.D student was never an easy task, but my Family (My Mother, My Wife, and My Daughters), Friends, Colleagues and everybody else have made me to pass it. The journey doesn’t end here, it is only the start of a more challenging chapter in my life, in a future I will dedicate this study to improve the quality of life Indonesian people particularly in supporting the tobacco cessation program by Indonesian Government.
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