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miRNA and Protein Expression Profiles of Visceral Adipose Tissue Reveal miR-141/YWHAG and miR-520e/RAB11A as Two Potential miRNA/Protein Target Pairs Associated with Severe Obesity

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† Fondazione IRCCS SDN, Istituto di Ricerca Diagnostica e Nucleare, Via Gianturco 113, 80143 Naples, Italy
‡ Dipartimento di Biochimica e Biotecnologie Mediche, Università degli Studi di Napoli Federico II, Via Pansini 5, 80131 Naples, Italy
§ CEINGE Biotecnologie Avanzate S.C. a R.L., Via Gaetano Salvatore 486, 80145, Naples, Italy
∥ Dipartimento di Chirurgia Generale, Geriatrica, Oncologica e Tecnologie Avanzate, Università degli Studi di Napoli Federico II, Via Pansini 5, 80131 Naples, Italy
*Fax: 0039-081-7462404. Tel.: 0039-081-7463541. E-mail: [email protected]
Cite this: J. Proteome Res. 2012, 11, 6, 3358–3369
Publication Date (Web):April 27, 2012
https://doi.org/10.1021/pr300152z
Copyright © 2012 American Chemical Society
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    Abstract

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    Adipose tissues show selective gene expression patterns, to whom microRNAs (miRNAs) may contribute. We evaluated in visceral adipose tissue (VAT) from obese and nonobese females, both miRNA and protein expression profiles, to identify miRNA/protein target pairs associated with obesity (metabolic pathways miRNA-deregulated during obesity). Obese and nonobese females [BMI 42.2 ± 1.6 and 23.7 ± 1.2 kg/m2 (mean ± SEM), respectively] were enrolled in this study. Notably, most miRNAs were down-expressed in obese tissues, whereas most of the proteins from the investigated spots were up-expressed. Bioinformatics integration of miRNA expression and proteomic data highlighted two potential miRNA/protein target pairs: miR-141/YWHAG (tyrosine 3-monooxygenase/tryptophan 5-monooxygenase activation protein, gamma polypeptide) and miR-520e/RAB11A (Ras-related protein RAB-11A); the functional interaction between these miRNAs and their target sequences on the corresponding mRNAs was confirmed by luciferase assays. Both RAB11A and YWHAG proteins are involved in glucose homeostasis; YWHAG is also involved in lipid metabolism. Hence, the identified miRNA/protein target pairs are potential players in the obese phenotype.

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    Figure S1: Main bioinformatically predicted pathways that are deregulated by miRNAs in VAT from obese females. Putative target genes of deregulated miRNAs in VAT from obese patients were sorted into pathways using the Kegg database. In parentheses are the number of genes targeted by miRNAs. Table S1: The sequences and charge states of each peptide used for identification of the proteins by LC–MS/MS. This material is available free of charge via the Internet at http://pubs.acs.org.

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    8. Sandra Franco, Daniela Buccione, Cristina Tural, Miguel Angel Martinez. Circulating microRNA signatures that predict liver fibrosis progression in patients with HIV-1/hepatitis C virus coinfections. AIDS 2021, 35 (9) , 1355-1363. https://doi.org/10.1097/QAD.0000000000002895
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    10. Soudeh Ghafouri-Fard, Mohammad Taheri. The expression profile and role of non-coding RNAs in obesity. European Journal of Pharmacology 2021, 892 , 173809. https://doi.org/10.1016/j.ejphar.2020.173809
    11. Francesca Reggiani, Paolo Falvo, Francesco Bertolini. Cellular and Molecular Players in the Interplay between Adipose Tissue and Breast Cancer. International Journal of Molecular Sciences 2021, 22 (3) , 1359. https://doi.org/10.3390/ijms22031359
    12. Veronika Zubáňová, Zuzana Červinková, Otto Kučera, Vladimír Palička. The Connection between MicroRNAs from Visceral Adipose Tissue and Non-Alcoholic Fatty Liver Disease. Acta Medica (Hradec Kralove, Czech Republic) 2021, 64 (1) , 1-7. https://doi.org/10.14712/18059694.2021.1
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    14. Biagio Arcidiacono, Eusebio Chiefari, Anna Foryst-Ludwig, Giuseppe Currò, Giuseppe Navarra, Francesco S. Brunetti, Maria Mirabelli, Domenica M. Corigliano, Ulrich Kintscher, Domenico Britti, Vincenzo Mollace, Daniela P. Foti, Ira D. Goldfine, Antonio Brunetti. Obesity-related hypoxia via miR-128 decreases insulin-receptor expression in human and mouse adipose tissue promoting systemic insulin resistance. eBioMedicine 2020, 59 , 102912. https://doi.org/10.1016/j.ebiom.2020.102912
    15. Dawid Szczepankiewicz, Wojciech Langwiński, Paweł Kołodziejski, Ewa Pruszyńska-Oszmałek, Maciej Sassek, Joanna Nowakowska, Agata Chmurzyńska, Krzysztof W. Nowak, Aleksandra Szczepankiewicz. Allergic Inflammation Alters microRNA Expression Profile in Adipose Tissue in the Rat. Genes 2020, 11 (9) , 1034. https://doi.org/10.3390/genes11091034
    16. Sarah B. Withers, Toni Dewhurst, Chloe Hammond, Caroline H. Topham. MiRNAs as Novel Adipokines: Obesity-Related Circulating MiRNAs Influence Chemosensitivity in Cancer Patients. Non-Coding RNA 2020, 6 (1) , 5. https://doi.org/10.3390/ncrna6010005
    17. Yuxia Wang, Haifeng Yu, Fangmei Liu, Xiue Song. Analysis of key genes and their functions in placental tissue of patients with gestational diabetes mellitus. Reproductive Biology and Endocrinology 2019, 17 (1) https://doi.org/10.1186/s12958-019-0546-z
    18. Kadidia Diallo, Abel K. Oppong, Gareth E. Lim. Can 14-3-3 proteins serve as therapeutic targets for the treatment of metabolic diseases?. Pharmacological Research 2019, 139 , 199-206. https://doi.org/10.1016/j.phrs.2018.11.021
    19. Yuxiang Huang, Yuxiang Yan, Weicheng Xv, Ge Qian, Chijian Li, Hequn Zou, Yongqiang Li. A New Insight into the Roles of MiRNAs in Metabolic Syndrome. BioMed Research International 2018, 2018 , 1-15. https://doi.org/10.1155/2018/7372636
    20. Yves Mugabo, Gareth E Lim. Scaffold Proteins: From Coordinating Signaling Pathways to Metabolic Regulation. Endocrinology 2018, 159 (11) , 3615-3630. https://doi.org/10.1210/en.2018-00705
    21. Sandra Franco, Daniela Buccione, Raquel Pluvinet, Beatriz Mothe, Lidia Ruiz, Maria Nevot, Ana Jordan-Paiz, Laia Ramos, Susanna Aussó, Rosa M. Morillas, Lauro Sumoy, Miguel Angel Martinez, Cristina Tural. Large-scale screening of circulating microRNAs in individuals with HIV-1 mono-infections reveals specific liver damage signatures. Antiviral Research 2018, 155 , 106-114. https://doi.org/10.1016/j.antiviral.2018.05.008
    22. Yves Mugabo, Mina Sadeghi, Nancy N. Fang, Thibault Mayor, Gareth E. Lim. Elucidation of the 14-3-3ζ interactome reveals critical roles of RNA-splicing factors during adipogenesis. Journal of Biological Chemistry 2018, 293 (18) , 6736-6750. https://doi.org/10.1074/jbc.M117.816272
    23. M. Zaiou, H. El Amri, A. Bakillah. The clinical potential of adipogenesis and obesity-related microRNAs. Nutrition, Metabolism and Cardiovascular Diseases 2018, 28 (2) , 91-111. https://doi.org/10.1016/j.numecd.2017.10.015
    24. Alina Kuryłowicz, Zofia Wicik, Magdalena Owczarz, Marta Jonas, Marta Kotlarek, Michał Świerniak, Wojciech Lisik, Maurycy Jonas, Bartłomiej Noszczyk, Monika Puzianowska-Kuźnicka. NGS Reveals Molecular Pathways Affected by Obesity and Weight Loss-Related Changes in miRNA Levels in Adipose Tissue. International Journal of Molecular Sciences 2018, 19 (1) , 66. https://doi.org/10.3390/ijms19010066
    25. Ravi Kasiappan, Dheeran Rajarajan. Role of MicroRNA Regulation in Obesity-Associated Breast Cancer: Nutritional Perspectives. Advances in Nutrition 2017, 8 (6) , 868-888. https://doi.org/10.3945/an.117.015800
    26. Mandana Pahlavani, Theresa Ramalho, Iurii Koboziev, Monique J LeMieux, Shasika Jayarathne, Latha Ramalingam, Luciano R Filgueiras, Naima Moustaid-Moussa. Adipose Tissue Inflammation in Insulin Resistance: Review of Mechanisms Mediating Anti-Inflammatory Effects of Omega-3 Polyunsaturated Fatty Acids. Journal of Investigative Medicine 2017, 65 (7) , 1021-1027. https://doi.org/10.1136/jim-2017-000535
    27. João Tomé-Carneiro, M. Carmen Crespo, Estefanía García-Calvo, José L. Luque-García, Alberto Dávalos, Francesco Visioli. Proteomic evaluation of mouse adipose tissue and liver following hydroxytyrosol supplementation. Food and Chemical Toxicology 2017, 107 , 329-338. https://doi.org/10.1016/j.fct.2017.07.009
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    29. Adeline Divoux, Hui Xie, Jian‐Liang Li, Kalypso Karastergiou, Ranjan J. Perera, R. Jeffrey Chang, Susan K. Fried, Steven R. Smith. MicroRNA‐196 Regulates HOX Gene Expression in Human Gluteal Adipose Tissue. Obesity 2017, 25 (8) , 1375-1383. https://doi.org/10.1002/oby.21896
    30. Bruna B. Brandão, Beatriz A. Guerra, Marcelo A. Mori. Shortcuts to a functional adipose tissue: The role of small non-coding RNAs. Redox Biology 2017, 12 , 82-102. https://doi.org/10.1016/j.redox.2017.01.020
    31. Jian Zhang, Peiyuan Wang, Lin Wan, Shouping Xu, Da Pang. The emergence of noncoding RNAs as Heracles in autophagy. Autophagy 2017, 13 (6) , 1004-1024. https://doi.org/10.1080/15548627.2017.1312041
    32. Hongbin Wang, Hua Zhi, Dongzhou Ma, Tao Li. MiR-217 promoted the proliferation and invasion of glioblastoma by repressing YWHAG. Cytokine 2017, 92 , 93-102. https://doi.org/10.1016/j.cyto.2016.12.013
    33. Thomas Thomou, Marcelo A. Mori, Jonathan M. Dreyfuss, Masahiro Konishi, Masaji Sakaguchi, Christian Wolfrum, Tata Nageswara Rao, Jonathon N. Winnay, Ruben Garcia-Martin, Steven K. Grinspoon, Phillip Gorden, C. Ronald Kahn. Adipose-derived circulating miRNAs regulate gene expression in other tissues. Nature 2017, 542 (7642) , 450-455. https://doi.org/10.1038/nature21365
    34. Peng Wang, Yu Deng, XiangNing Fu. MiR-509-5p suppresses the proliferation, migration, and invasion of non-small cell lung cancer by targeting YWHAG. Biochemical and Biophysical Research Communications 2017, 482 (4) , 935-941. https://doi.org/10.1016/j.bbrc.2016.11.136
    35. Carmela Nardelli, Ilaria Granata, Laura Iaffaldano, Valeria D'Argenio, Valentina Del Monaco, Giuseppe Maria Maruotti, Daniela Omodei, Luigi Del Vecchio, Pasquale Martinelli, Francesco Salvatore, Mario Rosario Guarracino, Lucia Sacchetti, Lucio Pastore. miR-138/miR-222 Overexpression Characterizes the miRNome of Amniotic Mesenchymal Stem Cells in Obesity. Stem Cells and Development 2017, 26 (1) , 4-14. https://doi.org/10.1089/scd.2016.0127
    36. Carmela Nardelli, Laura Iaffaldano, Vincenzo Pilone, Giuseppe Labruna, Maddalena Ferrigno, Nicola Carlomagno, Concetta Anna Dodaro, Pietro Forestieri, Pasqualina Buono, Francesco Salvatore, Lucia Sacchetti. Changes in the MicroRNA Profile Observed in the Subcutaneous Adipose Tissue of Obese Patients after Laparoscopic Adjustable Gastric Banding. Journal of Obesity 2017, 2017 , 1-6. https://doi.org/10.1155/2017/6754734
    37. Valentina Capobianco, Marianna Caterino, Laura Iaffaldano, Carmela Nardelli, Angelo Sirico, Luigi Del Vecchio, Pasquale Martinelli, Lucio Pastore, Pietro Pucci, Lucia Sacchetti. Proteome analysis of human amniotic mesenchymal stem cells (hA-MSCs) reveals impaired antioxidant ability, cytoskeleton and metabolic functionality in maternal obesity. Scientific Reports 2016, 6 (1) https://doi.org/10.1038/srep25270
    38. Raghavendra Mysore, You Zhou, Sanja Sädevirta, Hanna Savolainen-Peltonen, P.A. Nidhina Haridas, Jarkko Soronen, Marja Leivonen, Antti-Pekka Sarin, Pamela Fischer-Posovszky, Martin Wabitsch, Hannele Yki-Järvinen, Vesa M. Olkkonen. MicroRNA-192* impairs adipocyte triglyceride storage. Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids 2016, 1861 (4) , 342-351. https://doi.org/10.1016/j.bbalip.2015.12.019
    39. R Perdigão-Henriques, F Petrocca, G Altschuler, M P Thomas, M T N Le, S M Tan, W Hide, J Lieberman. miR-200 promotes the mesenchymal to epithelial transition by suppressing multiple members of the Zeb2 and Snail1 transcriptional repressor complexes. Oncogene 2016, 35 (2) , 158-172. https://doi.org/10.1038/onc.2015.69
    40. Víctor Faundes, Lorena Santa María, Paulina Morales, Bianca Curotto, María M. Parraguez. Distal 7q11.23 Duplication, an Emerging Microduplication Syndrome: A Case Report and Further Characterisation. Molecular Syndromology 2016, 7 (5) , 287-291. https://doi.org/10.1159/000448698
    41. Lisette J. A. Kogelman, Daria V. Zhernakova, Harm-Jan Westra, Susanna Cirera, Merete Fredholm, Lude Franke, Haja N. Kadarmideen. An integrative systems genetics approach reveals potential causal genes and pathways related to obesity. Genome Medicine 2015, 7 (1) https://doi.org/10.1186/s13073-015-0229-0
    42. Gareth E. Lim, Tobias Albrecht, Micah Piske, Karnjit Sarai, Jason T. C Lee, Hayley S. Ramshaw, Sunita Sinha, Mark A. Guthridge, Amparo Acker-Palmer, Angel F. Lopez, Susanne M. Clee, Corey Nislow, James D. Johnson. 14-3-3ζ coordinates adipogenesis of visceral fat. Nature Communications 2015, 6 (1) https://doi.org/10.1038/ncomms8671
    43. Peter Arner, Agné Kulyté. MicroRNA regulatory networks in human adipose tissue and obesity. Nature Reviews Endocrinology 2015, 11 (5) , 276-288. https://doi.org/10.1038/nrendo.2015.25
    44. Eun Kim, Won Kim, Kyoung-Jin Oh, Baek Han, Sang Lee, Kwang-Hee Bae. Recent Advances in Proteomic Studies of Adipose Tissues and Adipocytes. International Journal of Molecular Sciences 2015, 16 (3) , 4581-4599. https://doi.org/10.3390/ijms16034581
    45. C Nardelli, L Iaffaldano, M Ferrigno, G Labruna, G M Maruotti, F Quaglia, V Capobianco, R Di Noto, L Del Vecchio, P Martinelli, L Pastore, L Sacchetti. Characterization and predicted role of the microRNA expression profile in amnion from obese pregnant women. International Journal of Obesity 2014, 38 (3) , 466-469. https://doi.org/10.1038/ijo.2013.121
    46. Laura Iaffaldano, Carmela Nardelli, Maddalena Raia, Elisabetta Mariotti, Maddalena Ferrigno, Filomena Quaglia, Giuseppe Labruna, Valentina Capobianco, Angela Capone, Giuseppe Maria Maruotti, Lucio Pastore, Rosa Di Noto, Pasquale Martinelli, Lucia Sacchetti, Luigi Del Vecchio. High Aminopeptidase N/CD13 Levels Characterize Human Amniotic Mesenchymal Stem Cells and Drive Their Increased Adipogenic Potential in Obese Women. Stem Cells and Development 2013, 22 (16) , 2287-2297. https://doi.org/10.1089/scd.2012.0499
    47. Mei Kuen Tang, Yong Jia Liang, John Yeuk Hon Chan, Sing Wan Wong, Elve Chen, Yao Yao, Jingyi Gan, Lihai Xiao, Hin Cheung Leung, Hsiang Fu Kung, Hua Wang, Kenneth Ka Ho Lee, . Promyelocytic Leukemia (PML) Protein Plays Important Roles in Regulating Cell Adhesion, Morphology, Proliferation and Migration. PLoS ONE 2013, 8 (3) , e59477. https://doi.org/10.1371/journal.pone.0059477
    48. Carmela Nardelli, Giuseppe Labruna, Rosario Liguori, Cristina Mazzaccara, Maddalena Ferrigno, Valentina Capobianco, Massimo Pezzuti, Giuseppe Castaldo, Eduardo Farinaro, Franco Contaldo, Pasqualina Buono, Lucia Sacchetti, Fabrizio Pasanisi. Haplogroup T Is an Obesity Risk Factor: Mitochondrial DNA Haplotyping in a Morbid Obese Population from Southern Italy. BioMed Research International 2013, 2013 , 1-5. https://doi.org/10.1155/2013/631082
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