Effect of estrogen on expression of prohibitin in white adipose tissue and liver of diet-induced obese rats

Choi, Minji; Chaudhari, Harmesh N.; Ji, Young Rae; Ryoo, Zae Young; Kim, Sang Woo; Yun, Jong Won

doi:10.1007/s11010-015-2468-1

Cited by 7Estrogen and related hormone effectsAdipose Tissue and MetabolismAdipokines, Inflammation, and Metabolic Diseases

Effect of estrogen on expression of prohibitin in white adipose tissue and liver of diet-induced obese rats

Choi, Minji, Chaudhari, Harmesh N., Ji, Young Rae, Ryoo, Zae Young, Kim, Sang Woo, Yun, Jong Won·2015·Molecular and Cellular Biochemistry

DOI 10.1007/s11010-015-2468-1

Open this paper in CoChat — free account

Abstract

Prohibitin (PHB) is a ubiquitously expressed and highly conserved protein that participates in diverse cellular processes, and its functions are linked to a variety of diseases. In the present study, to explore transcriptional activation and signaling pathways involved in PHB regulation in response to sex hormone treatment, we investigated the effects of estrogen (17-β-estradiol, E2) on regulation of PHB in several metabolic tissues from male and female rats. Elevated expression of PHB was prominent in white adipose tissue (WAT) and the liver, and E2 stimulated PHB expression in both ND and HFD-fed rats. To further confirm the expression of PHB which was increased in WAT and the liver, we analyzed PHB expression levels in 3T3-L1 and C9 cells after the treatment of E2. Transcription and protein levels of PHB were dose-dependently increased by E2 treatment in both cell types, supporting our in vivo data. To further evaluate the possible role of E2 in elevation of PHB via estrogen receptors (ER), the potent ER inhibitor fulvestrant was treated to 3T3-L1 and C9 cells. Fulvestrant markedly suppressed both transcription and protein levels of PHB, suggesting that PHB expression in both tissues may be regulated through ERs. GeneMANIA, a predictive web interface, was used to show that Phb is regulated via the intracellular steroid hormone receptor signaling pathway, suggesting a role for ERs in expression of Phb as well as other metabolically important genes. Based on these results, we expect that targeting PHB would be a useful therapeutic approach for treatment of obesity.

Integrity signals

Registry

Crossref · 10.1007/s11010-015-2468-1

Cites

64 of 64 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

In rat models, the expression of prohibitins responds to the levels of oestrogens in WAT.
“Further, in rat models, the expression of prohibitins responds to the levels of oestrogens in WAT. The level of prohibitins were stimulated by estradiol in WAT and liver in both, controls and high-fat fed rats (Choi et al., 2015).”
From Mitochondrial Activity and Dynamics Changes Regarding Metabolism in Ageing and Obesity (2017) · cites this paper as Choi et al., 2015
Levels of prohibitins were stimulated by estradiol in WAT and liver in both controls and high-fat fed rats.
“The level of prohibitins were stimulated by estradiol in WAT and liver in both, controls and high-fat fed rats (Choi et al., 2015).”
From Mitochondrial Activity and Dynamics Changes Regarding Metabolism in Ageing and Obesity (2017) · cites this paper as Choi et al., 2015
In rat models, expression of prohibitins responds to levels of oestrogens in WAT.
“in rat models, the expression of prohibitins responds to the levels of oestrogens in WAT.”
From Mitochondrial Activity and Dynamics Changes Regarding Metabolism in Ageing and Obesity (2017) · cites this paper as Choi et al., 2015

The GeneMANIA prediction server: Biological network integration for gene prioritization and predicting gene function
Warde-Farley, D., Donaldson, S. L., Comes, O., Zuberi, K., Badrawi, R., Chao, P., Franz, M., Grouios, C., Kazi, F., Lopes, C. T., et al. (2010) · Nucleic Acids Research · doi:10.1093/nar/gkq537 · Cited by 4,835 · see citing works
GeneMANIA: a real-time multiple association network integration algorithm for predicting gene function
Mostafavi, S., Ray, D., Warde-Farley, D., Grouios, C., & Morris, Q. (2008) · Genome biology · doi:10.1186/gb-2008-9-s1-s4 · Cited by 1,054 · see citing works
Interleukin-17–producing innate lymphoid cells and the NLRP3 inflammasome facilitate obesity-associated airway hyperreactivity
Kim, H. Y., Lee, H. J., Chang, Y., Pichavant, M., Shore, S. A., Fitzgerald, K. A., Iwakura, Y., Israel, E., Bolger, K., Faul, J. L., et al. (2013) · Nature Medicine · doi:10.1038/nm.3423 · Cited by 639 · see citing works
Reversal of obesity by targeted ablation of adipose tissue
Kolonin, M. G., Saha, P., Chan, L., Pasqualini, R., & Arap, W. (2004) · Nature Medicine · doi:10.1038/nm1048 · Cited by 596 · see citing works
Estrogen Regulation of Adiposity and Fuel Partitioning
D'Eon, T. M., Souza, S. C., Aronovitz, M. J., Obin, M. S., Fried, S. K., & Greenberg, A. S. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m507339200 · Cited by 506 · see citing works
USP15 stabilizes TGF-β receptor I and promotes oncogenesis through the activation of TGF-β signaling in glioblastoma
Eichhorn, P. J. A., Rodón, L., Gonzàlez-Juncà, A., Dirac, A., Gili, M., Martínez-Sáez, E., Aura, C., Barba, I., Peg, V., Prat, A., et al. (2012) · Nature Medicine · doi:10.1038/nm.2619 · Cited by 409 · see citing works
IL-17 regulates adipogenesis, glucose homeostasis, and obesity
Zúñiga, L. A., Shen, W.-J., Joyce-Shaikh, B., Pyatnova, E. A., Richards, A. G., Thom, C., Andrade, S. M., Cua, D. J., Kraemer, F. B., & Butcher, E. C. (2010) · The Journal of Immunology · doi:10.4049/jimmunol.1001269 · Cited by 394 · see citing works
Prohibitin is required for Ras-induced Raf–MEK–ERK activation and epithelial cell migration
Rajalingam, K., Wunder, C., Brinkmann, V., Churin, Y., Hekman, M., Sievers, C., Rapp, U. R., & Rudel, T. (2005) · Nature Cell Biology · doi:10.1038/ncb1283 · Cited by 356 · see citing works
The Prohibitins: emerging roles in diverse functions
Mishra, S., Murphy, L. C., & Murphy, L. J. (2006) · Journal of Cellular and Molecular Medicine · doi:10.1111/j.1582-4934.2006.tb00404.x · Cited by 288 · see citing works
Increased activity of interleukin-23/interleukin-17 proinflammatory axis in obese women
Šumarac-Dumanović, M., Stevanović, D., Ljubić, A., Jorga, J. B., Simic, M., Stamenkovic-Pejkovic, D., Starcevic, V. P., Trajković, V., & Micić, D. (2008) · International Journal of Obesity · doi:10.1038/ijo.2008.216 · Cited by 287 · see citing works
Prohibitin and mitochondrial biology
Artal‐Sanz, M., & Tavernarakis, N. (2009) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2009.04.004 · Cited by 285 · see citing works
IL-17 Signaling Accelerates the Progression of Nonalcoholic Fatty Liver Disease in Mice
Harley, I. T. W., Stankiewicz, T. E., Giles, D. A., Softic, S., Flick, L. M., Cappelletti, M., Sheridan, R. M., Xanthakos, S. A., Steinbrecher, K. A., Sartor, R. B., et al. (2013) · Hepatology · doi:10.1002/hep.26746 · Cited by 252 · see citing works
The diversity of sex steroid action: regulation of metabolism by estrogen signaling
Faulds, M. H., Zhao, C., Dahlman-Wright, K., & Gustafsson, J.-Å. (2012) · Journal of Endocrinology · doi:10.1530/joe-11-0044 · Cited by 230 · see citing works
Mechanisms of antidiabetogenic and body weight-lowering effects of estrogen in high-fat diet-fed mice
Bryzgalova, G., Lundholm, L., Portwood, N., Gustafsson, J.-Å., Khan, A., Efendić, S., & Dahlman‐Wright, K. (2008) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.90248.2008 · Cited by 217 · see citing works
Vi polysaccharide of Salmonella typhi targets the prohibitin family of molecules in intestinal epithelial cells and suppresses early inflammatory responses
Sharma, A., & Qadri, A. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0407536101 · Cited by 211 · see citing works
Lipoprotein lipase: cellular origin and functional distribution
Camps, L., Reina, M., Llobera, M., Vilaró, S., & Olivecrona, T. (1990) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.1990.258.4.c673 · Cited by 203 · see citing works
Effect of Ovariectomy on Adipose Tissue of Mice in the Absence of Estrogen Receptor Alpha (ERα): a Potential Role for Estrogen Receptor Beta (ERβ)
Naaz, A., Zakroczymski, M., Heine, P., Taylor, J., Saunders, P., Lubahn, D., & Cooke, P. S. (2002) · Hormone and Metabolic Research · doi:10.1055/s-2002-38259 · Cited by 188 · see citing works
Routine identification of proteins from sodium dodecyl sulfate‐polyacrylamide gel electrophoresis (SDS‐PAGE) gels or polyvinyl difluoride membranes using matrix assisted laser desorption/ionization‐time of flight‐mass spectrometry (MALDI‐TOF‐MS)
Fernandez, J., Gharahdaghi, F., & Mische, S. M. (1998) · Electrophoresis · doi:10.1002/elps.1150190619 · Cited by 180 · see citing works
Long-term administration of estradiol decreases expression of hepatic lipogenic genes and improves insulin sensitivity in ob/ob mice: a possible mechanism is through direct regulation of signal transducer and activator of transcription 3
Gao, H., Bryzgalova, G., Hedman, E., Khan, A., Efendic, S., Gustafsson, J.-A., & Dahlman-Wright, K. (2006) · Molecular Endocrinology · doi:10.1210/me.2006-0012 · Cited by 179 · see citing works
Estrogen Inhibits Transforming Growth Factor β Signaling by Promoting Smad2/3 Degradation
Ito, I., Hanyu, A., Wayama, M., Goto, N., Katsuno, Y., Kawasaki, S., Nakajima, Y., Kajiro, M., Komatsu, Y., Fujimura, A., et al. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.093039 · Cited by 171 · see citing works
The role and therapeutic potential of prohibitin in disease
Theiss, A. L., & Sitaraman, S. V. (2011) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2011.01.033 · Cited by 156 · see citing works
Prohibitin protects against oxidative stress in intestinal epithelial cells
Theiss, A. L., Idell, R. D., Srinivasan, S., Klapproth, J. A., Jones, D. P., Merlin, D., & Sitaraman, S. V. (2006) · The FASEB Journal · doi:10.1096/fj.06-6801com · Cited by 152 · see citing works
A Repressive Role for Prohibitin in Estrogen Signaling
He, B., Feng, Q. F., Mukherjee, A., Lonard, D. M., DeMayo, F. J., Katzenellenbogen, B. S., Lydon, J. P., & O’Malley, B. W. (2007) · Molecular Endocrinology · doi:10.1210/me.2007-0400 · Cited by 134 · see citing works
The Arl4 Family of Small G Proteins Can Recruit the Cytohesin Arf6 Exchange Factors to the Plasma Membrane
Hofmann, I., Thompson, A., Sanderson, C. M., & Munro, S. (2007) · Current Biology · doi:10.1016/j.cub.2007.03.007 · Cited by 128 · see citing works
Liver-Specific Deletion of Prohibitin 1 Results in Spontaneous Liver Injury, Fibrosis, and Hepatocellular Carcinoma in Mice
Ko, K. S., Tomasi, M. L., Iglesias–Ara, A., French, B. A., French, S. W., Ramani, K., Lozano, J. J., Oh, P., He, L., Stiles, B. L., et al. (2010) · Hepatology · doi:10.1002/hep.23919 · Cited by 123 · see citing works
Direct Effects of Testosterone, 17β-Estradiol, and Progesterone on Adrenergic Regulation in Cultured Brown Adipocytes: Potential Mechanism for Gender-Dependent Thermogenesis
Monjo, M., Rodríguez, A. M., Palou, A., & Roca, P. (2003) · Endocrinology · doi:10.1210/en.2003-0537 · Cited by 122 · see citing works
Androgens target prohibitin to regulate proliferation of prostate cancer cells
Gamble, S. C., Odontiadis, M., Waxman, J., Westbrook, J. A., Dunn, M. J., Wait, R., Lam, E. W. ‐., & Bevan, C. L. (2004) · Oncogene · doi:10.1038/sj.onc.1207444 · Cited by 114 · see citing works
C/EBPβ Reprograms White 3T3-L1 Preadipocytes to a Brown Adipocyte Pattern of Gene Expression
Karamanlidis, G., Karamitri, A., Docherty, K., Hazlerigg, D. G., & Lomax, M. A. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m703101200 · Cited by 113 · see citing works
Novel genes modulated by FSH in normal and immortalized FSH‐responsive cells: new insights into the mechanism of FSH action
Sasson, R., Dantes, A., Tajima, K., & Amsterdam, A. (2003) · The FASEB Journal · doi:10.1096/fj.02-0740com · Cited by 98 · see citing works
Prohibitin, a protein downregulated by androgens, represses androgen receptor activity
Gamble, S. C., Chotai, D., Odontiadis, M., Dart, D. A., Brooke, G., Powell, S., Reebye, V., Varela‐Carver, A., Kawano, Y., Waxman, J., et al. (2007) · Oncogene · doi:10.1038/sj.onc.1209967 · Cited by 94 · see citing works
Ligand-based targeted delivery of a peptide modified nanocarrier to endothelial cells in adipose tissue
Hossen, M. N., Kajimoto, K., Akita, H., Hyodo, M., Ishitsuka, T., & Harashima, H. (2010) · Journal of Controlled Release · doi:10.1016/j.jconrel.2010.07.100 · Cited by 93 · see citing works
Effect of 2 Years of Testosterone Replacement on Insulin Secretion, Insulin Action, Glucose Effectiveness, Hepatic Insulin Clearance, and Postprandial Glucose Turnover in Elderly Men
Basu, R., Man, C. D., Campioni, M., Basu, A., Nair, K. S., Jensen, M. D., Khosla, S., Klee, G., Toffolo, G., Cobelli, C., et al. (2007) · Diabetes Care · doi:10.2337/dc07-0359 · Cited by 91 · see citing works
IL-17 inhibits adipogenesis in part via C/EBPα, PPARγ and Krüppel-like factors
Ahmed, M., & Gaffen, S. L. (2013) · Cytokine · doi:10.1016/j.cyto.2012.12.007 · Cited by 87 · see citing works
Identification and characterization of a novel tyrosine kinase from megakaryocytes.
Bennett, B. D., Cowley, S. A., Jiang, S., London, R., Deng, B., Grabarek, J., Groopman, J. E., Goeddel, D. V., & Avraham, H. K. (1994) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)42222-8 · Cited by 82 · see citing works
TNF-α induces matrix metalloproteinase-9-dependent soluble intercellular adhesion molecule-1 release via TRAF2-mediated MAPKs and NF-κB activation in osteoblast-like MC3T3-E1 cells
Chia-Lan, T., Chen, W., Hsieh, H., Chi, P., Hsiao, L., & Yang, C. (2014) · Journal of Biomedical Science · doi:10.1186/1423-0127-21-12 · Cited by 82 · see citing works
Vascular-targeted nanotherapy for obesity: Unexpected passive targeting mechanism to obese fat for the enhancement of active drug delivery
Hossen, M. N., Kajimoto, K., Akita, H., Hyodo, M., & Harashima, H. (2012) · Journal of Controlled Release · doi:10.1016/j.jconrel.2012.09.002 · Cited by 81 · see citing works
Regulatory GTP-binding proteins (ADP-ribosylation factor, Gt, and RAS) are not activated directly by nucleoside diphosphate kinase.
Randazzo, P. A., Northup, J. K., & Kahn, R. (1992) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)37170-4 · Cited by 75 · see citing works
Mitochondrial Dysfunction and Adipogenic Reduction by Prohibitin Silencing in 3T3-L1 Cells
Liu, D., Lin, Y., Kang, T., Huang, B., Xu, W., Garcia-Barrio, M. T., Olatinwo, M. O., Matthews, R., Chen, Y., & Thompson, W. E. (2012) · PLoS ONE · doi:10.1371/journal.pone.0034315 · Cited by 74 · see citing works
BRG1/BRM and prohibitin are required for growth suppression by estrogen antagonists
Wang, S., Zhang, B., & Faller, D. V. (2004) · The EMBO Journal · doi:10.1038/sj.emboj.7600231 · Cited by 71 · see citing works
Prohibitin overexpression in adipocytes induces mitochondrial biogenesis, leads to obesity development, and affects glucose homeostasis in a sex-specific manner
Ande, S. R., Nguyen, K. H., Padilla-Meier, G. P., Wahida, W., Nyomba, B. L. G., & Mishra, S. (2014) · Diabetes · doi:10.2337/db13-1807 · Cited by 71 · see citing works
Reprogramming of the SWI/SNF complex for co-activation or co-repression in prohibitin-mediated estrogen receptor regulation
Zhang, B., Chambers, K. J., Faller, D. V., & Wang, S. (2007) · Oncogene · doi:10.1038/sj.onc.1210509 · Cited by 68 · see citing works
Prohibitin and the SWI/SNF ATPase subunit BRG1 are required for effective androgen antagonist-mediated transcriptional repression of androgen receptor-regulated genes
Dai, Y., Ngo, D., Jacob, J., Forman, L. W., & Faller, D. V. (2008) · Carcinogenesis · doi:10.1093/carcin/bgn117 · Cited by 63 · see citing works
Prohibitin has an important role in adipocyte differentiation
Ande, S. R., Xu, Z., Gu, Y., & Mishra, S. (2011) · International Journal of Obesity · doi:10.1038/ijo.2011.227 · Cited by 62 · see citing works
Prohibitin deficiency blocks proliferation and induces apoptosis in human hepatoma cells: Molecular mechanisms and functional implications
Sánchez‐Quiles, V., Santamaría, E., Segura, V., Sesma, L., Prìeto, J., & Corrales, F. J. (2010) · PROTEOMICS · doi:10.1002/pmic.200900757 · Cited by 57 · see citing works
Dynamic reciprocity: the role of annexin A2 in tissue integrity
Hitchcock, J. K., Katz, A. A., & Schäfer, G. (2014) · Journal of Cell Communication and Signaling · doi:10.1007/s12079-014-0231-0 · Cited by 57 · see citing works
Prohibitin attenuates insulin‐stimulated glucose and fatty acid oxidation in adipose tissue by inhibition of pyruvate carboxylase
Vessal, M., Mishra, S., Moulik, S., & Murphy, L. J. (2006) · FEBS Journal · doi:10.1111/j.1742-4658.2005.05090.x · Cited by 57 · see citing works
Manipulating prohibitin levels provides evidence for an in vivo role in androgen regulation of prostate tumours
Dart, D. A., Spencer‐Dene, B., Gamble, S. C., Waxman, J., & Bevan, C. L. (2009) · Endocrine Related Cancer · doi:10.1677/erc-09-0028 · Cited by 53 · see citing works
Expression of Prohibitin in Rat Seminiferous Epithelium1
Choongkittaworn, N., Kim, K. H., Danner, D. B., & Griswold, M. D. (1993) · Biology of Reproduction · doi:10.1095/biolreprod49.2.300 · Cited by 47 · see citing works
Gender Difference in Proteome of Brown Adipose Tissues between Male and Female Rats Exposed to a High Fat Diet
Choi, D. K., Oh, T. S., Choi, J., Mukherjee, R., Wang, X., Liu, H., & Yun, J. W. (2011) · Cellular Physiology and Biochemistry · doi:10.1159/000335807 · Cited by 44 · see citing works
Estrogen-Regulated Prohibitin Is Required for Mouse Uterine Development and Adult Function
He, B., Kim, T. H., Kommagani, R., Feng, Q. F., Lanz, R. B., Jeong, J., DeMayo, F. J., Katzenellenbogen, B. S., Lydon, J. P., & O’Malley, B. W. (2011) · Endocrinology · doi:10.1210/en.2010-0732 · Cited by 36 · see citing works
Prohibitin and prohibitone are contained in high-molecular weight complexes and interact with α-actinin and annexin A2
Bacher, S. (2002) · Biochimie · doi:10.1016/s0300-9084(02)00027-5 · Cited by 35 · see citing works
Growth inhibition of carcinogen-transformed MCF-12F breast epithelial cells and hormone-sensitive BT-474 breast cancer cells by 1α-hydroxyvitamin D5
Hussain-Hakimjee, E. A., Peng, X., Mehta, R. R., & Mehta, R. G. (2005) · Carcinogenesis · doi:10.1093/carcin/bgi231 · Cited by 31 · see citing works
Prohibitin-1 deficiency promotes inflammation and increases sensitivity to liver injury
Sánchez‐Quiles, V., Segura, V., Bigaud, E., He, B., O’Malley, B. W., Santamaría, E., Prìeto, J., & Corrales, F. J. (2012) · Journal of Proteomics · doi:10.1016/j.jprot.2012.08.009 · Cited by 29 · see citing works
Sex-Dependent Expression of Caveolin 1 in Response to Sex Steroid Hormones Is Closely Associated with Development of Obesity in Rats
Mukherjee, R., Kim, S. W., Choi, M. S., & Yun, J. W. (2014) · PLoS ONE · doi:10.1371/journal.pone.0090918 · Cited by 22 · see citing works
Signaling functions of ubiquitin in the 17β-estradiol (E2):estrogen receptor (ER) α network
Rosa, P. L., & Acconcia, F. (2011) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2011.07.008 · Cited by 21 · see citing works
Comparative hepatic proteome analysis between lean and obese rats fed a high‐fat diet reveals the existence of gender differences
Wang, X., Choi, J. W., Oh, T. S., Choi, D. K., Mukherjee, R., Liu, H., & Yun, J. W. (2011) · PROTEOMICS · doi:10.1002/pmic.201100271 · Cited by 20 · see citing works
Prohibitin in squamous cell carcinoma of the lung: its expression and possible clinical significance
Guo, F., Hiroshima, K., Wu, D., Satoh, M., Abulazi, M., Yoshino, I., Tomonaga, T., Nomura, F., & Nakatani, Y. (2012) · Human Pathology · doi:10.1016/j.humpath.2011.10.006 · Cited by 17 · see citing works
Prohibitin Expression Is Decreased in the Regenerating Liver but Not in Chemically Induced Hepatic Tumors in Rats
Tanno, S., Fukuda, I., Saito, Y., & Ogawa, K. (1997) · Japanese Journal of Cancer Research · doi:10.1111/j.1349-7006.1997.tb00344.x · Cited by 16 · see citing works
Roles of prohibitin in growth control and tumor suppression in human cancers.
Wang, S., & Faller, D. V. (2008) · PubMed · Cited by 14 · see citing works
Mild caloric restriction up-regulates the expression of prohibitin: A proteome study
Takahashi, S., Masuda, J., Shimagami, H., Ohta, Y., Kanda, T., Saito, K., & Kato, H. (2011) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2011.01.054 · Cited by 12 · see citing works
Detection of early gene expression changes during activation of human primary lymphocytes by in vitro synthesis of proteins from polysome‐associated mRNAs
Miyamoto, S., Qin, J., & Safer, B. (2001) · Protein Science · doi:10.1110/ps.21301 · Cited by 12 · see citing works
Gender-dimorphic regulation of antioxidant proteins in response to high-fat diet and sex steroid hormones in rats
Chaudhari, H. N., Kim, S. W., & Yun, J. W. (2014) · Free Radical Research · doi:10.3109/10715762.2014.896003 · Cited by 10 · see citing works
Cloning of cDNA for granzyme‐like protein III, a novel serine proteinase from rat duodenum
Grigorenko, G. M., Yarovoi, S. V., Paulauskaite, R., & Amerik, A. Y. (1994) · FEBS Letters · doi:10.1016/0014-5793(94)80516-4 · Cited by 7 · see citing works
Regulation of human estrogen receptor α-mediated gene transactivation in Saccharomyces cerevisiae by human coactivator and corepressor proteins
Bitter, G. A. (2006) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2006.11.001 · Cited by 4 · see citing works

Flagged first, then by citations

1 of the 65 references couldn’t be matched to a known paper.

Sorted by citations

Mitochondrial Activity and Dynamics Changes Regarding Metabolism in Ageing and Obesity
López-Lluch, G. (2017) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2016.12.005 · Cited by 103 · see citing works
“The level of prohibitins were stimulated by estradiol in WAT and liver in both, controls and high-fat fed rats (Choi et al., 2015).”
Background
Low-dose perfluorooctanoic acid stimulates steroid hormone synthesis in Leydig cells: Integrated proteomics and metabolomics evidence
Huang, Q., Luo, L., Han, X., Li, F., Zhang, X., & Tian, M. (2021) · Journal of Hazardous Materials · doi:10.1016/j.jhazmat.2021.127656 · Cited by 36 · see citing works
ERα36, a variant of estrogen receptor α, is predominantly localized in mitochondria of human uterine smooth muscle and leiomyoma cells
Yan, Y., Yu, L. C., Castro, L., & Dixon, D. (2017) · PLoS ONE · doi:10.1371/journal.pone.0186078 · Cited by 23 · see citing works
Estrogen Enhances Endometrial Cancer Cells Proliferation by Upregulation of Prohibitin
Yang, B., Chen, R., Liang, X., Shi, J., Wu, X., Zhang, Z., & Chen, X. (2019) · Journal of Cancer · doi:10.7150/jca.28218 · Cited by 22 · see citing works
Gonadectomy in Mito-Ob mice revealed a sex-dimorphic relationship between prohibitin and sex steroids in adipose tissue biology and glucose homeostasis
Xu, Y. X. Z., Ande, S. R., & Mishra, S. (2018) · Biology of Sex Differences · doi:10.1186/s13293-018-0196-4 · Cited by 16 · see citing works
Persistent mTORC1 activation underlies sex dimorphic progression of MASLD in mice with hepatocyte prohibitin-1 deficiencyPreprint
Alowaisi, A. A., Mahoney, J. C., Huo, R., Berdaweel, I. A., Crawford, R. M., Mallaro, K. J., McLendon, J. M., & Anderson, E. J. (2025) · Research Square · doi:10.21203/rs.3.rs-7481614/v1 · Cited by 2 · see citing works
Hyperactive mTORC1 underlies sex dimorphic progression of MASLD in mice with hepatocyte prohibitin-1 deficiency
Owaisi, A., Mahoney, J. C., Huo, R., Berdaweel, I. A., Crawford, R. M., Mallaro, K. J., McLendon, J. M., & Anderson, E. J. (2026) · Molecular Metabolism · doi:10.1016/j.molmet.2026.102458

Prohibitin: a prime candidate for a pleiotropic effector that mediates sex differences in obesity, insulin resistance, and metabolic dysregulation
Xu, Y. X. Z., Bassi, G., & Mishra, S. (2019) · Biology of Sex Differences · doi:10.1186/s13293-019-0239-5 · Cited by 13 · see citing works
The interaction between prohibitin-1 and sex steroid hormones in adipogenesis
Xu, Y. X. Z. (. (2017) · Mspace (University of Manitoba)
Prohibitin has an important role in adipocyte differentiation
Ande, S. R., Xu, Z., Gu, Y., & Mishra, S. (2011) · International Journal of Obesity · doi:10.1038/ijo.2011.227 · Cited by 62 · see citing works
Estrogen-Regulated Prohibitin Is Required for Mouse Uterine Development and Adult Function
He, B., Kim, T. H., Kommagani, R., Feng, Q. F., Lanz, R. B., Jeong, J., DeMayo, F. J., Katzenellenbogen, B. S., Lydon, J. P., & O’Malley, B. W. (2011) · Endocrinology · doi:10.1210/en.2010-0732 · Cited by 36 · see citing works
Prohibitin Plays an Important Role in Adipocyte Differentiation
Ande, S. R., Xu, Z., Gu, Y., & Mishra, S. (2012) · The FASEB Journal · doi:10.1096/fasebj.26.1_supplement.567.1

Authors: Choi, M., Chaudhari, H. N., Ji, Y. R., Ryoo, Z. Y., Kim, S. W., & Yun, J. W.
Affiliations: Daegu University (KR)
Kyungpook National University (KR)
Corresponding author: Yun, Jong Won
ORCID: Choi, Minji
Ji, Young Rae
Ryoo, Zae Young
Kim, Sang Woo
Yun, Jong Won
Venue: Molecular and Cellular Biochemistry
Publisher: Springer Science and Business Media LLC
Published: 2015-06-06
Volume: 407
Issue: 1-2
Pages: 181-196
ISSN: 0300-8177 (ISSN-L)
1573-4919
DOI: 10.1007/s11010-015-2468-1
OpenAlex: W2232545925
Cited by: 7
References: 65
Citations by year: 2026: 1 · 2025: 1 · 2021: 1 · 2019: 1 · 2018: 1 · 2017: 1 · 2016: 1
FWCI: 0.69
Type: journal article
Language: en
Open access: closed
Licence: www.springer.com/tdm (tdm)
Locations: Molecular and Cellular Biochemistry (publishedVersion)
PubMed (publishedVersion)
Funders: Mid-career Researcher Program (2013R1A2A2A05004195)
SRC Program (Center for Food and Nutritional Genomics (2015R1A5A6001906)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Estrogen and related hormone effects
Health Sciences › Medicine › Physiology › Adipose Tissue and Metabolism
Health Sciences › Medicine › Epidemiology › Adipokines, Inflammation, and Metabolic Diseases
Keywords: prohibitin, estrogen, estradiol, estrogen receptor, diet-induced obesity, white adipose tissue, liver, gene expression regulation, fulvestrant, 3T3-L1 cells, obesity treatment
MeSH terms: Prohibitins, Animals, Cell Line, Dose-Response Relationship, Drug, Estrogens, Female, Gene Expression Regulation, Liver, Male, Obesity, Organ Specificity, Receptors, Estrogen, Repressor Proteins, 3T3-L1 Cells, Mice, Rats, Adipose Tissue, White, Diet, High-Fat

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Effect of estrogen on expression of prohibitin in white adipose tissue and liver of diet-induced obese rats

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Cites

Cited by

Related

Record

About these checks