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Pathophysiology
Essential Role of Protein Arginine Methyltransferase 1 in Pancreas Development by Regulating Protein Stability of Neurogenin 3
Kanghoon Lee, Hyunki Kim, Joonyub Lee, Chang-Myung Oh, Heein Song, Hyeongseok Kim, Seung-Hoi Koo, Junguee Lee, Ajin Lim, Hail Kim
Diabetes Metab J. 2019;43(5):649-658.   Published online April 8, 2019
DOI: https://doi.org/10.4093/dmj.2018.0232
  • 5,122 View
  • 70 Download
  • 4 Web of Science
  • 5 Crossref
AbstractAbstract PDFPubReader   
Background

Protein arginine methyltransferase 1 (PRMT1) is a major enzyme responsible for the formation of methylarginine in mammalian cells. Recent studies have revealed that PRMT1 plays important roles in the development of various tissues. However, its role in pancreas development has not yet been elucidated.

Methods

Pancreatic progenitor cell-specific Prmt1 knock-out (Prmt1 PKO) mice were generated and characterized for their metabolic and histological phenotypes and their levels of Neurog3 gene expression and neurogenin 3 (NGN3) protein expression. Protein degradation assays were performed in mPAC cells.

Results

Prmt1 PKO mice showed growth retardation and a severely diabetic phenotype. The pancreatic size and β-cell mass were significantly reduced in Prmt1 PKO mice. Proliferation of progenitor cells during the secondary transition was decreased and endocrine cell differentiation was impaired. These defects in pancreas development could be attributed to the sustained expression of NGN3 in progenitor cells. Protein degradation assays in mPAC cells revealed that PRMT1 was required for the rapid degradation of NGN3.

Conclusion

PRMT1 critically contributes to pancreas development by destabilizing the NGN3 protein.

Citations

Citations to this article as recorded by  
  • Arginine 65 methylation of Neurogenin 3 by PRMT1 is required for pancreatic endocrine development of hESCs
    Gahyang Cho, Kwangbeom Hyun, Jieun Choi, Eunji Shin, Bumsoo Kim, Hail Kim, Jaehoon Kim, Yong-Mahn Han
    Experimental & Molecular Medicine.2023; 55(7): 1506.     CrossRef
  • Protein arginine methyltransferase 1 in the generation of immune megakaryocytes: A perspective review
    Xinyang Zhao, Zechen Chong, Yabing Chen, X. Long Zheng, Qian-Fei Wang, Yueying Li
    Journal of Biological Chemistry.2022; 298(11): 102517.     CrossRef
  • Arginine 65 Methylation of Neurogenin 3 by PRMT1 Is Required for Pancreatic Endocrine Development of hESCs
    Gahyang Cho, Kwangbeom Hyun, Jieun Choi, Eun Ji Shin, Bumsoo Kim, Hail Kim, Jaehoon Kim, Yong-Mahn Han
    SSRN Electronic Journal .2022;[Epub]     CrossRef
  • Protein Arginine Methyltransferase 1 Is Essential for the Meiosis of Male Germ Cells
    Sahar Waseem, Sudeep Kumar, Kanghoon Lee, Byoung-Ha Yoon, Mirang Kim, Hail Kim, Keesook Lee
    International Journal of Molecular Sciences.2021; 22(15): 7951.     CrossRef
  • Proteome-Wide Alterations of Asymmetric Arginine Dimethylation Associated With Pancreatic Ductal Adenocarcinoma Pathogenesis
    Meijin Wei, Chaochao Tan, Zhouqin Tang, Yingying Lian, Ying Huang, Yi Chen, Congwei Chen, Wen Zhou, Tao Cai, Jiliang Hu
    Frontiers in Cell and Developmental Biology.2020;[Epub]     CrossRef
Obesity and Metabolic Syndrome
Inhibition of Serotonin Synthesis Induces Negative Hepatic Lipid Balance
Jun Namkung, Ko Eun Shong, Hyeongseok Kim, Chang-Myung Oh, Sangkyu Park, Hail Kim
Diabetes Metab J. 2018;42(3):233-243.   Published online April 25, 2018
DOI: https://doi.org/10.4093/dmj.2017.0084
  • 4,649 View
  • 84 Download
  • 24 Web of Science
  • 22 Crossref
AbstractAbstract PDFPubReader   
Background

Hepatic steatosis is caused by metabolic stress associated with a positive lipid balance, such as insulin resistance and obesity. Previously we have shown the anti-obesity effects of inhibiting serotonin synthesis, which eventually improved insulin sensitivity and hepatic steatosis. However, it is not clear whether serotonin has direct effect on hepatic lipid accumulation. Here, we showed the possibility of direct action of serotonin on hepatic steatosis.

Methods

Mice were treated with para-chlorophenylalanine (PCPA) or LP-533401 to inhibit serotonin synthesis and fed with high fat diet (HFD) or high carbohydrate diet (HCD) to induce hepatic steatosis. Hepatic triglyceride content and gene expression profiles were analyzed.

Results

Pharmacological and genetic inhibition of serotonin synthesis reduced HFD-induced hepatic lipid accumulation. Furthermore, short-term PCPA treatment prevented HCD-induced hepatic steatosis without affecting glucose tolerance and browning of subcutaneous adipose tissue. Gene expression analysis revealed that the expressions of genes involved in de novo lipogenesis and triacylglycerol synthesis were downregulated by short-term PCPA treatment as well as long-term PCPA treatment.

Conclusion

Short-term inhibition of serotonin synthesis prevented hepatic lipid accumulation without affecting systemic insulin sensitivity and energy expenditure, suggesting the direct steatogenic effect of serotonin in liver.

Citations

Citations to this article as recorded by  
  • A new serotonin 2A receptor antagonist with potential benefits in Non-Alcoholic Fatty Liver Disease
    Lucia Sessa, Simona Concilio, Jesús Fominaya, Daniela Eletto, Stefano Piotto, Xavier Busquets
    Life Sciences.2023; 314: 121315.     CrossRef
  • Serotonin reuptake transporter deficiency promotes liver steatosis and impairs intestinal barrier function in obese mice fed a Western‐style diet
    Louisa Filipe Rosa, Eva Haasis, Annkathrin Knauss, Daria Guseva, Stephan C. Bischoff
    Neurogastroenterology & Motility.2023;[Epub]     CrossRef
  • Probiotics counteract hepatic steatosis caused by ketogenic diet and upregulate AMPK signaling in a model of infantile epilepsy
    Chunlong Mu, Naghmeh Nikpoor, Thomas A. Tompkins, Jong M. Rho, Morris H. Scantlebury, Jane Shearer
    eBioMedicine.2022; 76: 103838.     CrossRef
  • Research Progresses for 5-Hydroxytryptamine in Lipid Metabolism
    钰婷 吴
    Bioprocess.2022; 12(01): 1.     CrossRef
  • Platelet-Activating Factor Promotes the Development of Non-Alcoholic Fatty Liver Disease
    Hang Yin, Anhua Shi, Junzi Wu
    Diabetes, Metabolic Syndrome and Obesity: Targets and Therapy.2022; Volume 15: 2003.     CrossRef
  • Involvement of the liver-gut peripheral neural axis in nonalcoholic fatty liver disease pathologies via hepatic HTR2A
    Takashi Owaki, Kenya Kamimura, Masayoshi Ko, Itsuo Nagayama, Takuro Nagoya, Osamu Shibata, Chiyumi Oda, Shinichi Morita, Atsushi Kimura, Takeki Sato, Toru Setsu, Akira Sakamaki, Hiroteru Kamimura, Takeshi Yokoo, Shuji Terai
    Disease Models & Mechanisms.2022;[Epub]     CrossRef
  • Pancreatic Sirtuin 3 Deficiency Promotes Hepatic Steatosis by Enhancing 5-Hydroxytryptamine Synthesis in Mice With Diet-Induced Obesity
    Xing Ming, Arthur C.K. Chung, Dandan Mao, Huanyi Cao, Baoqi Fan, Willy K.K. Wong, Chin Chung Ho, Heung Man Lee, Kristina Schoonjans, Johan Auwerx, Guy A. Rutter, Juliana C.N. Chan, Xiao Yu Tian, Alice P.S. Kong
    Diabetes.2021; 70(1): 119.     CrossRef
  • Peripheral Selective Oxadiazolylphenyl Alanine Derivatives as Tryptophan Hydroxylase 1 Inhibitors for Obesity and Fatty Liver Disease
    Eun Jung Bae, Won Gun Choi, Haushabhau S. Pagire, Suvarna H. Pagire, Saravanan Parameswaran, Jun-Ho Choi, Jihyeon Yoon, Won-il Choi, Ji Hun Lee, Jin Sook Song, Myung Ae Bae, Mijin Kim, Jae-Han Jeon, In-Kyu Lee, Hail Kim, Jin Hee Ahn
    Journal of Medicinal Chemistry.2021; 64(2): 1037.     CrossRef
  • Modulation of serotonin in the gut-liver neural axis ameliorates the fatty and fibrotic changes in non-alcoholic fatty liver
    Masayoshi Ko, Kenya Kamimura, Takashi Owaki, Takuro Nagoya, Norihiro Sakai, Itsuo Nagayama, Yusuke Niwa, Osamu Shibata, Chiyumi Oda, Shinichi Morita, Atsushi Kimura, Ryosuke Inoue, Toru Setsu, Akira Sakamaki, Takeshi Yokoo, Shuji Terai
    Disease Models & Mechanisms.2021;[Epub]     CrossRef
  • Metabolic Disturbances in Rat Sublines with Constitutionally Altered Serotonin Homeostasis
    Maja Kesić, Petra Baković, Ranko Stojković, Jasminka Štefulj, Lipa Čičin-Šain
    International Journal of Molecular Sciences.2021; 22(10): 5400.     CrossRef
  • Role of 5-HT degradation in acute liver injury induced by carbon tetrachloride
    Yu-Xin Zhang, Chen Li, Xiu-Rui Liang, Jia-Qi Jin, Yi Zhang, Fan Xu, Jing Guan, Ying-Ying Ma, Xiao-Nan Ma, Run-Kun Liu, Ji-Hua Fu
    European Journal of Pharmacology.2021; 908: 174355.     CrossRef
  • Fluoxetine-induced hepatic lipid accumulation is linked to elevated serotonin production
    Ahmed Ayyash, Alison C. Holloway
    Canadian Journal of Physiology and Pharmacology.2021; 99(9): 983.     CrossRef
  • Brain-gut-liver interactions across the spectrum of insulin resistance in metabolic fatty liver disease
    Eleni Rebelos, Patricia Iozzo, Maria Angela Guzzardi, Maurizia Rossana Brunetto, Ferruccio Bonino
    World Journal of Gastroenterology.2021; 27(30): 4999.     CrossRef
  • Inhibiting serotonin signaling through HTR2B in visceral adipose tissue improves obesity-related insulin resistance
    Won Gun Choi, Wonsuk Choi, Tae Jung Oh, Hye-Na Cha, Inseon Hwang, Yun Kyung Lee, Seung Yeon Lee, Hyemi Shin, Ajin Lim, Dongryeol Ryu, Jae Myoung Suh, So-Young Park, Sung Hee Choi, Hail Kim
    Journal of Clinical Investigation.2021;[Epub]     CrossRef
  • Green tea and selenium-enriched green tea ameliorates non-alcoholic fatty liver disease through peripheral 5-hydroxytryptamine signals in high-fat diet-fed mice
    Lin Zhang, Jia-Ying Xu, Ya-Fang Du, Zhang-Min Wang, Jian-Xiang Li, N. Ou-Yang, Yan Wang, Xue-Bin Yin, Li-Qiang Qin
    International Food Research Journal.2021; 28(5): 996.     CrossRef
  • Inhibition of serotonin synthesis: A novel therapeutic paradigm
    Michael Bader
    Pharmacology & Therapeutics.2020; 205: 107423.     CrossRef
  • One-Carbon Metabolism in Fatty Liver Disease and Fibrosis: One-Carbon to Rule Them All
    da Silva Robin P, Eudy Brandon J, Deminice Rafael
    The Journal of Nutrition.2020; 150(5): 994.     CrossRef
  • Design, Synthesis, and Biological Evaluation of New Peripheral 5HT2A Antagonists for Nonalcoholic Fatty Liver Disease
    Minhee Kim, Inseon Hwang, Haushabhau S. Pagire, Suvarna H. Pagire, Wonsuk Choi, Won Gun Choi, Jihyeon Yoon, Won Mi Lee, Jin Sook Song, Eun Kyung Yoo, Seung Mi Lee, Mi-jin Kim, Myung Ae Bae, Dooseop Kim, Heejong Lee, Eun-Young Lee, Jae-Han Jeon, In-Kyu Lee
    Journal of Medicinal Chemistry.2020; 63(8): 4171.     CrossRef
  • Hepatic fibrosis is associated with total proteinuria in Korean patients with type 2 diabetes
    Eugene Han, Yongin Cho, Kyung-won Kim, Yong-ho Lee, Eun Seok Kang, Bong-Soo Cha, Byung-wan Lee
    Medicine.2020; 99(33): e21038.     CrossRef
  • The Role of the Gut Microbiota in Lipid and Lipoprotein Metabolism
    Yijing Yu, Fitore Raka, Khosrow Adeli
    Journal of Clinical Medicine.2019; 8(12): 2227.     CrossRef
  • Emerging Roles for Serotonin in Regulating Metabolism: New Implications for an Ancient Molecule
    Julian M Yabut, Justin D Crane, Alexander E Green, Damien J Keating, Waliul I Khan, Gregory R Steinberg
    Endocrine Reviews.2019; 40(4): 1092.     CrossRef
  • Serotonin signals through a gut-liver axis to regulate hepatic steatosis
    Wonsuk Choi, Jun Namkung, Inseon Hwang, Hyeongseok Kim, Ajin Lim, Hye Jung Park, Hye Won Lee, Kwang-Hyub Han, Seongyeol Park, Ji-Seon Jeong, Geul Bang, Young Hwan Kim, Vijay K. Yadav, Gerard Karsenty, Young Seok Ju, Chan Choi, Jae Myoung Suh, Jun Yong Par
    Nature Communications.2018;[Epub]     CrossRef

Diabetes Metab J : Diabetes & Metabolism Journal