Endothelial ERα promotes glucose tolerance by enhancing endothelial insulin transport to skeletal muscle
Open accessAbstract
The estrogen receptor (ER) designated ERα has actions in many cell and tissue types that impact glucose homeostasis. It is unknown if these include mechanisms in endothelial cells, which have the potential to influence relative obesity, and processes in adipose tissue and skeletal muscle that impact glucose control. Here we show that independent of impact on events in adipose tissue, endothelial ERα promotes glucose tolerance by enhancing endothelial insulin transport to skeletal muscle. Endothelial ERα-deficient male mice are glucose intolerant and insulin resistant, and in females the antidiabetogenic actions of estradiol (E2) are absent. The glucose dysregulation is due to impaired skeletal muscle glucose disposal that results from attenuated muscle insulin delivery. Endothelial ERα activation stimulates insulin transcytosis by skeletal muscle microvascular endothelial cells. Mechanistically this involves nuclear ERα-dependent upregulation of vesicular trafficking regulator sorting nexin 5 (SNX5) expression, and PI3 kinase activation that drives plasma membrane recruitment of SNX5. Thus, coupled nuclear and non-nuclear actions of ERα promote endothelial insulin transport to skeletal muscle to foster normal glucose homeostasis.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
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?
Estrogen's metabolic effects are not only mediated through direct action on adipocytes, but also through endothelial mechanisms of ERα that improve insulin transport to skeletal muscle.
“estrogen’s metabolic effects are not only mediated through direct action on adipocytes, but also through endothelial mechanisms of ERα that improve insulin transport to skeletal muscle (146).”
From Metabolic impact of endogenously produced estrogens by adipose tissue in females and males across the lifespan (2025) · cites this paper as [146]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
STAR: ultrafast universal RNA-seq aligner
Dobin, A., Davis, C. A., Schlesinger, F., Drenkow, J., Zaleski, C., Jha, S., Batut, P., Chaisson, M., & Gingeras, T. R. (2013) · Bioinformatics · doi:10.1093/bioinformatics/bts635 · Cited by 51,709 · see citing works
Robinson, M. D., McCarthy, D. J., & Smyth, G. K. (2010) · Bioinformatics · doi:10.1093/bioinformatics/btp616 · Cited by 41,364 · see citing works
featureCounts: an efficient general purpose program for assigning sequence reads to genomic features
Liao, Y., Smyth, G. K., & Shi, W. (2014) · Bioinformatics · doi:10.1093/bioinformatics/btt656 · Cited by 27,219 · see citing works
ShinyGO: a graphical gene-set enrichment tool for animals and plants
Ge, S. X., Jung, D., & Yao, R. (2020) · Bioinformatics · doi:10.1093/bioinformatics/btz931 · Cited by 5,270 · see citing works
The Gene Ontology resource: enriching a GOld mine
The Gene Ontology Consortium, Carbon, S., Douglass, E., Good, B. M., Unni, D. R., Harris, N. L., Mungall, C. J., Basu, S., Chisholm, R. L., Dodson, R. J., et al. (2021) · Nucleic Acids Research · doi:10.1093/nar/gkaa1113 · Cited by 3,555 · see citing works
Estrogen Resistance Caused by a Mutation in the Estrogen-Receptor Gene in a Man
Smith, E. P., Boyd, J., Frank, G. R., Takahashi, H., Cohen, R. M., Specker, B., Williams, T. C., Lubahn, D. B., & Korach, K. S. (1994) · New England Journal of Medicine · doi:10.1056/nejm199410203311604 · Cited by 2,471 · see citing works
The role of estrogens in control of energy balance and glucose homeostasis
Mauvais-Jarvis, F., Clegg, D. J., & Hevener, A. L. (2013) · Endocrine Reviews · doi:10.1210/er.2012-1055 · Cited by 1,329 · see citing works
Functional domains of the human estrogen receptor
Kumar, V., Green, S., Stack, G., Berry, M., Jin, J.-R., & Chambon, P. (1987) · Cell · doi:10.1016/0092-8674(87)90581-2 · Cited by 1,316 · see citing works
Regulated transport of the glucose transporter GLUT4
Bryant, N. J., Govers, R., & James, D. E. (2002) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm782 · Cited by 1,183 · see citing works
Proteome-wide identification of ubiquitin interactions using UbIA-MS
Zhang, X.-F., Smits, A. H., van Tilburg, G. B. A., Ovaa, H., Huber, W. K., & Vermeulen, M. (2018) · Nature Protocols · doi:10.1038/nprot.2017.147 · Cited by 813 · see citing works
Zisman, A., Peroni, O. D., Abel, E. D., Michael, M. D., Mauvais-Jarvis, F., Lowell, B. B., Wojtaszewski, J. F. P., Hirshman, M. F., Virkamaki, A., Goodyear, L. J., et al. (2000) · Nature Medicine · doi:10.1038/78693 · Cited by 743 · see citing works
Integration of the extranuclear and nuclear actions of estrogen
Levin, E. R. (2005) · Molecular Endocrinology · doi:10.1210/me.2004-0390 · Cited by 708 · see citing works
Estrogen Modulation of Endothelial Nitric Oxide Synthase
Chambliss, K. L., & Shaul, P. W. (2002) · Endocrine Reviews · doi:10.1210/er.2001-0045 · Cited by 572 · see citing works
Self-citationMusatov, S. A., Chen, W. W., Pfaff, D. W., Mobbs, C. V., Yang, X.-J., Clegg, D. J., Kaplitt, M. G., & Ogawa, S. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0610787104 · Cited by 518 · see citing works
Regulation of Splanchnic and Peripheral Glucose Uptake by Insulin and Hyperglycemia in Man
DeFronzo, R. A., Ferrannini, E., Hendler, R., Felig, P., & Wahren, J. (1983) · Diabetes · doi:10.2337/diab.32.1.35 · Cited by 509 · see citing works
Alva, J. A., Zovein, A. C., Monvoisin, A., Murphy, T. J., Salazar, A., Harvey, N. L., Carmeliet, P., & Iruela‐Arispe, M. L. (2006) · Developmental Dynamics · doi:10.1002/dvdy.20643 · Cited by 455 · see citing works
Keske, M. A., Clerk, L. H., Lindner, J. R., Klibanov, A. L., Clark, M. G., Rattigan, S., & Barrett, E. J. (2004) · Diabetes · doi:10.2337/diabetes.53.6.1418 · Cited by 439 · see citing works
Kubota, T., Kubota, N., Kumagai, H., Yamaguchi, S., Kozono, H., Takahashi, T., Inoue, M., Itoh, S., Takamoto, I., Sasako, T., et al. (2011) · Cell Metabolism · doi:10.1016/j.cmet.2011.01.018 · Cited by 435 · cited 1× · see citing works
“Since insulin receptor substrate-2 in endothelial cells is critical to insulin transport 64 , its expression was also assessed and it was unchanged by SNX5 knockdown (Supplementary Fig.”
Estrogens protect against high-fat diet-induced insulin resistance and glucose intolerance in mice
Riant, E., Waget, A., Cogo, H., Arnal, J.-F., Burcelin, R., & Gourdy, P. (2009) · Endocrinology · doi:10.1210/en.2008-0971 · Cited by 421 · see citing works
Chambliss, K. L., Yuhanna, I. S., Mineo, C., Liu, P., German, Z., Sherman, T. S., Mendelsohn, M. E., Anderson, R. G. W., & Shaul, P. W. (2000) · Circulation Research · doi:10.1161/01.res.87.11.e44 · Cited by 416 · see citing works
Self-citationSorting out the cellular functions of sorting nexins
Worby, C. A., & Dixon, J. E. (2002) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm974 · Cited by 412 · see citing works
SR-B1 drives endothelial cell LDL transcytosis via DOCK4 to promote atherosclerosis
Huang, L., Chambliss, K. L., Gao, X., Yuhanna, I. S., Behling‐Kelly, E. L., Bergaya, S., Ahmed, M. H., Michaely, P., Luby‐Phelps, K., Darehshouri, A., et al. (2019) · Nature · doi:10.1038/s41586-019-1140-4 · Cited by 354 · see citing works
Self-citationEstrogen-Receptor Biology: Continuing Progress and Therapeutic Implications
Osborne, C. K., & Schiff, R. (2005) · Journal of Clinical Oncology · doi:10.1200/jco.2005.10.036 · Cited by 350 · see citing works
MAFFEI, L. E., Murata, Y., Rochira, V., Gloria, T., Aranda, C., Vázquez, M., Clyne, C. D., Davis, S. R., Simpson, E. R., & Carani, C. (2004) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2003-030313 · Cited by 343 · see citing works
Barrett, E. J., Eggleston, E. M., Inyard, A. C., Wang, H., Li, G., Chai, W., & Liu, Z. (2009) · Diabetologia · doi:10.1007/s00125-009-1313-z · Cited by 323 · see citing works
Cooperation of proto‐signals for nuclear accumulation of estrogen and progesterone receptors.
Ylikomi, T. J., Bocquel, M. T., Berry, M., Gronemeyer, H., & Chambon, P. (1992) · The EMBO Journal · doi:10.1002/j.1460-2075.1992.tb05453.x · Cited by 319 · see citing works
Estrogen acutely stimulates nitric oxide synthase activity in fetal pulmonary artery endothelium
Lantin-Hermoso, R. L., Rosenfeld, C. R., Yuhanna, I. S., German, Z., Chen, Z., & Shaul, P. W. (1997) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.1997.273.1.l119 · Cited by 284 · see citing works
Self-citationDavis, K. E., D. Neinast, M., Sun, K., M. Skiles, W., D. Bills, J., A. Zehr, J., Zeve, D., D. Hahner, L., W. Cox, D., M. Gent, L., et al. (2013) · Molecular Metabolism · doi:10.1016/j.molmet.2013.05.006 · Cited by 278 · see citing works
Feng, Y., Manka, D. R., Wagner, K., & Khan, S. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0706933104 · Cited by 275 · see citing works
Self-citationPhysiologic Hyperinsulinemia Enhances Human Skeletal Muscle Perfusion by Capillary Recruitment
Coggins, M. P., Lindner, J. R., Rattigan, S., Jahn, L. A., Fasy, E. A., Kaul, S., & Barrett, E. J. (2001) · Diabetes · doi:10.2337/diabetes.50.12.2682 · Cited by 260 · see citing works
Chambliss, K. L., Wu, Q., Oltmann, S. C., Konaniah, E. S., Umetani, M., Korach, K. S., Thomas, G. D., Mineo, C., Yuhanna, I. S., Kim, S. H., et al. (2010) · Journal of Clinical Investigation · doi:10.1172/jci38291 · Cited by 249 · see citing works
Self-citationHarrington, W. R., Kim, S. H., Funk, C. C., Madak‐Erdogan, Z., Schiff, R., Katzenellenbogen, J. A., & Katzenellenbogen, B. S. (2005) · Molecular Endocrinology · doi:10.1210/me.2005-0186 · Cited by 246 · see citing works
Self-citationHaft, C. R., de la Luz Sierra, M., Barr, V. A., Haft, D. H., & Taylor, S. I. (1998) · Molecular and Cellular Biology · doi:10.1128/mcb.18.12.7278 · Cited by 244 · see citing works
Estrogen Receptors and Endothelium
Arnal, J., Fontaine, C., Billon-Galés, A., Favre, J., Laurell, H., Lenfant, F., & Gourdy, P. (2010) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.109.191221 · Cited by 232 · see citing works
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
The effects of oestrogen and progesterone on insulin sensitivity in female rats
KUMAGAI, S., Holmäng, A. B., & Björntorp, P. A. (1993) · Acta Physiologica Scandinavica · doi:10.1111/j.1748-1716.1993.tb09596.x · Cited by 193 · see citing works
Umetani, M., Ghosh, P., Ishikawa, T., Umetani, J., Ahmed, M. H., Mineo, C., & Shaul, P. W. (2014) · Cell Metabolism · doi:10.1016/j.cmet.2014.05.013 · Cited by 192 · see citing works
Self-citationProgression of Metabolic Syndrome Severity During the Menopausal Transition
Gurka, M. J., Vishnu, A., Santen, R. J., & DeBoer, M. D. (2016) · Journal of the American Heart Association · doi:10.1161/jaha.116.003609 · Cited by 183 · see citing works
Takeda, K., Toda, K., Saibara, T., Nakagawa, M., Saika, K., Onishi, T., Sugiura, T., & Shizuta, Y. (2003) · Journal of Endocrinology · doi:10.1677/joe.0.1760237 · Cited by 182 · see citing works
Ribas, V., Drew, B. G., Le, J., Soleymani, T., Daraei, P., Sitz, D., Mohammad, L., Henstridge, D. C., Febbraio, M. A., Hewitt, S. C., et al. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1104533108 · Cited by 180 · see citing works
The role of estrogen receptors in the control of energy and glucose homeostasis
Ropero, A. B., Alonso-Magdalena, P., Quesada, I., & Nadal, A. (2008) · Steroids · doi:10.1016/j.steroids.2007.12.018 · Cited by 170 · see citing works
A large family of endosome-localized proteins related to sorting nexin 1
Teasdale, R. D., David, L. O. C. I., Houghton, F. J., Karlsson, L., & Gleeson, P. A. (2001) · Biochemical Journal · doi:10.1042/0264-6021:3580007 · Cited by 163 · see citing works
Interplay between adipose tissue and blood vessels in obesity and vascular dysfunction
Gu, P., & Xu, A. (2013) · Reviews in Endocrine and Metabolic Disorders · doi:10.1007/s11154-012-9230-8 · Cited by 160 · see citing works
Participation of ERα and ERβ in glucose homeostasis in skeletal muscle and white adipose tissue
Barros, R. P. A., Gabbi, C., Morani, A., Warner, M., & Gustafsson, J.-Å. (2009) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00189.2009 · Cited by 155 · see citing works
Dawson, D. K., Vincent, M. A., Barrett, E. J., Kaul, S., Clark, A., Leong-Poi, H. M., & Lindner, J. R. (2002) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00373.2001 · Cited by 152 · see citing works
Influence of menopause on diabetes and diabetes risk
Szmuilowicz, E. D., Stuenkel, C. A., & Seely, E. W. (2009) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2009.166 · Cited by 150 · see citing works
Vigh, J. P., Kincses, A., Ozgür, B., Walter, F. R., Santa-Maria, A. R., Valkai, S., Vastag, M., Neuhaus, W., Brodin, B., Dér, A., et al. (2021) · Micromachines · doi:10.3390/mi12060685 · Cited by 129 · see citing works
Zhou, P., Zhang, Y., Ma, Q., Gu, F., Day, D. S., He, A., Zhou, B., Li, J., Stevens, S. M., Romo, D., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1304124110 · Cited by 116 · see citing works
Impaired estrogen receptor action in the pathogenesis of the metabolic syndrome
Hevener, A. L., Clegg, D. J., & Mauvais-Jarvis, F. (2015) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2015.05.020 · Cited by 112 · see citing works
Non-nuclear Estrogen Receptor Signaling in the Endothelium
Wu, Q., Chambliss, K. L., Umetani, M., Mineo, C., & Shaul, P. W. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.r110.191791 · Cited by 110 · see citing works
Self-citationHeianza, Y., Arase, Y., Kodama, S., Hsieh, S. D., Tsuji, H., Saito, K., Shimano, H., Hara, S., & Sone, H. (2013) · Diabetes Care · doi:10.2337/dc13-1048 · Cited by 108 · see citing works
Nilsson, B. (2007) · Inflammation Research · doi:10.1007/s00011-007-6198-z · Cited by 107 · see citing works
Kinetics of Insulin Action In Vivo: Identification of Rate-Limiting Steps
Miles, P. D. G., Levisetti, M. G., Reichart, D. R., Khoursheed, M., Moossa, A. R., & Olefsky, J. M. (1995) · Diabetes · doi:10.2337/diab.44.8.947 · Cited by 101 · see citing works
Chiu, J. D., Richey, J. M., Harrison, L. N., Zuniga, E. A., Kolka, C. M., Kirkman, E. L., Ellmerer, M., & Bergman, R. N. (2008) · Diabetes · doi:10.2337/db07-1444 · Cited by 96 · see citing works
Tanigaki, K., Sacharidou, A., Peng, J.-Q., Chambliss, K., Yuhanna, I. S., Ghosh, D., Ahmed, M., Szalai, A., Vongpatanasin, W., Mattrey, R., et al. (2017) · Journal of Clinical Investigation · doi:10.1172/jci89333 · Cited by 91 · see citing works
Self-citationThe endothelial cell: An “early responder” in the development of insulin resistance
Barrett, E. J., & Liu, Z. (2013) · Reviews in Endocrine and Metabolic Disorders · doi:10.1007/s11154-012-9232-6 · Cited by 88 · see citing works
Quantitative Mapping of Tumor Vascularity Using Volumetric Contrast-Enhanced Ultrasound
Hoyt, K., Sorace, A. G., & Saini, R. (2011) · Investigative Radiology · doi:10.1097/rli.0b013e318234e6bc · Cited by 88 · see citing works
Self-citationSacharidou, A., Chambliss, K. L., Ulrich, V., Salmon, J. E., Shen, Y.-M. P., Herz, J., Hui, D. Y., Terada, L. S., Shaul, P. W., & Mineo, C. (2018) · Blood · doi:10.1182/blood-2017-11-814681 · Cited by 78 · see citing works
Self-citationWagenmakers, A. J. M., Strauss, J. A., Shepherd, S. O., Keske, M. A., & Cocks, M. (2016) · The Journal of Physiology · doi:10.1113/jphysiol.2014.284513 · Cited by 78 · see citing works
Mohamad, M., Mitchell, S. J., Wu, L. E., White, M. Y., Cordwell, S. J., Mach, J., Solon‐Biet, S. M., Boyer, D., Nines, D., Das, A., et al. (2016) · Aging Cell · doi:10.1111/acel.12481 · Cited by 77 · see citing works
Ultrasound Imaging of Breast Tumor Perfusion and Neovascular Morphology
Hoyt, K., Umphrey, H. R., Lockhart, M. E., Robbin, M. L., & Forero, A. (2015) · Ultrasound in Medicine & Biology · doi:10.1016/j.ultrasmedbio.2015.04.016 · Cited by 75 · see citing works
Self-citationMerino‐Trigo, A., Kerr, M. C., Houghton, F. J., Lindberg, A. L., Mitchell, C. A., Teasdale, R. D., & Gleeson, P. A. (2004) · Journal of Cell Science · doi:10.1242/jcs.01561 · Cited by 73 · see citing works
Menazza, S., Sun, J., Appachi, S., Chambliss, K. L., Kim, S. H., Aponte, A. M., Khan, S., Katzenellenbogen, J. A., Katzenellenbogen, B. S., Shaul, P. W., et al. (2017) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2017.04.004 · Cited by 71 · see citing works
Self-citationRecent developments in dynamic contrast-enhanced ultrasound imaging of tumor angiogenesis
Saini, R., & Hoyt, K. (2014) · Imaging in Medicine · doi:10.2217/iim.13.74 · Cited by 68 · see citing works
Self-citationThe microcirculation in adipose tissue inflammation
Scalia, R. G. (2013) · Reviews in Endocrine and Metabolic Disorders · doi:10.1007/s11154-013-9236-x · Cited by 65 · see citing works
Ghosh, D., Peng, J., Brown, K., Sirsi, S. R., Mineo, C., Shaul, P. W., & Hoyt, K. (2019) · Journal of Ultrasound in Medicine · doi:10.1002/jum.14956 · Cited by 64 · see citing works
Self-citationWagner, J. D., Thomas, M. J., Williams, J. K., Zhang, L., Greaves, K. A., & Cefalu, W. T. (1998) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.83.3.4628 · Cited by 56 · see citing works
Tanigaki, K., Vongpatanasin, W., Barrera, J. A., Atochin, D. N., Huang, P. L., Bonvini, E., Shaul, P. W., & Mineo, C. (2012) · Diabetes · doi:10.2337/db12-0133 · Cited by 54 · see citing works
Self-citationKim, S. H., & Katzenellenbogen, J. A. (2006) · Angewandte Chemie International Edition · doi:10.1002/anie.200601923 · Cited by 53 · see citing works
Self-citationLu, Q. R., Schnitzler, G. R., Ueda, K., Iyer, L. K., Diomede, O. I., Andrade, T., & Karas, R. H. (2016) · PLoS ONE · doi:10.1371/journal.pone.0152807 · Cited by 52 · see citing works
Barrera, J. A., Chambliss, K. L., Ahmed, M. H., Tanigaki, K., Thompson, B. M., McDonald, J. G., Mineo, C., & Shaul, P. W. (2014) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00653.2013 · Cited by 49 · see citing works
Self-citationRochira, V., Madeo, B., Zirilli, L., Caffagni, G., MAFFEI, L. E., & Carani, C. (2007) · Diabetic Medicine · doi:10.1111/j.1464-5491.2007.02304.x · Cited by 45 · see citing works
Wagner, J. D. (1998) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.83.3.896 · Cited by 41 · see citing works
Protocols for endothelial cell isolation from mouse tissues: brain, choroid, lung, and muscle
Conchinha, N. V., Sokol, L., Teuwen, L.-A. M. N., Veys, K., Dumas, S. J., Meta, E., García‐Caballero, M., Geldhof, V., Chen, R., Treps, L., et al. (2021) · STAR Protocols · doi:10.1016/j.xpro.2021.100508 · Cited by 39 · see citing works
Nonnuclear Estrogen Receptor Activation Improves Hepatic Steatosis in Female Mice
Chambliss, K. L., Barrera, J. A., Umetani, M., Umetani, J., Kim, S. H., Madak‐Erdogan, Z., Huang, L., Katzenellenbogen, B. S., Katzenellenbogen, J. A., Mineo, C., et al. (2016) · Endocrinology · doi:10.1210/en.2015-1629 · Cited by 36 · see citing works
Self-citationThe extra-nuclear interactome of the estrogen receptors: implications for physiological functions
Acconcia, F., Fiocchetti, M., Busonero, C., Fernandez, V. S., Montalesi, E., Cipolletti, M., Pallottini, V., & Marino, M. (2021) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2021.111452 · Cited by 36 · see citing works
Cirillo, F., Nassa, G., Tarallo, R., Stellato, C., Filippo, M. R. D., Ambrosino, C., Baumann, M., Nyman, T. A., & Weisz, A. (2012) · Journal of Proteome Research · doi:10.1021/pr300753u · Cited by 36 · see citing works
Manrique, C. M., Lastra, G., Ramirez‐Perez, F. I., Haertling, D., DeMarco, V. G., Aroor, A. R., Jia, G., Chen, D., Barron, B. J., Garro, M., et al. (2016) · Endocrinology · doi:10.1210/en.2015-1681 · Cited by 28 · see citing works
Endothelium-derived essential signals involved in pancreas organogenesis.
Talavera-Adame, D., & Dafoe, D. (2015) · World Journal of Experimental Medicine · doi:10.5493/wjem.v5.i2.40 · Cited by 27 · see citing works
Tanigaki, K., Chambliss, K. L., Yuhanna, I. S., Sacharidou, A., Ahmed, M. H., Atochin, D. N., Huang, P. L., Shaul, P. W., & Mineo, C. (2016) · Diabetes · doi:10.2337/db15-1605 · Cited by 26 · see citing works
Self-citationTransendothelial Insulin Transport is Impaired in Skeletal Muscle Capillaries of Obese Male Mice
Williams, I. M., McClatchey, P. M., Bracy, D. P., Bonner, J. S., Valenzuela, F. A., & Wasserman, D. H. (2020) · Obesity · doi:10.1002/oby.22683 · Cited by 22 · see citing works
Stellato, C., Nassa, G., Tarallo, R., Giurato, G., Ravo, M., Rizzo, F. M., Marchese, G., Alexandrova, E., Cordella, A., Baumann, M., et al. (2015) · PROTEOMICS · doi:10.1002/pmic.201400404 · Cited by 19 · see citing works
Li, F., Yang, J., Jones, J. E., Villar, V. A. M., Yu, P., Armando, I., Felder, R. A., & José, P. A. (2015) · Endocrinology · doi:10.1210/en.2014-1638 · Cited by 17 · see citing works
Özdemir, İ., Peng, J., Ghosh, D., Sirsi, S. R., Mineo, C., Shaul, P. W., & Hoyt, K. (2020) · Journal of medical imaging · doi:10.1117/1.jmi.7.3.034001 · Cited by 17 · see citing works
Self-citationLigand Accessibility and Bioactivity of a Hormone–Dendrimer Conjugate Depend on pH and pH History
Kim, S. H., Madak‐Erdogan, Z., Bae, S. C., Carlson, K. E., Mayne, C. G., Granick, S., Katzenellenbogen, B. S., & Katzenellenbogen, J. A. (2015) · Journal of the American Chemical Society · doi:10.1021/jacs.5b05952 · Cited by 15 · see citing works
Self-citation
Flagged first, then by citations
Research works printed but not linked: 2
- [48]Tanigaki K Hyposialylated IgG activates endothelial IgG receptor FcgammaRIIB to promote obesity-induced insulin resistance J. Clin. Invest. 2018 128 309 322 29202472 PMC5749535
- [71]Tanigaki K C-reactive protein causes insulin resistance in mice through Fcgamma receptor IIB-mediated inhibition of skeletal muscle glucose delivery Diabetes 2013 62 721 731 23069625 PMC3581204
Cited by
Sorted by citations
Sex difference in human diseases: mechanistic insights and clinical implications
Shi, Y., Ma, J., Li, S.-J., Liu, C., Liu, Y.-N., Chen, J., Liu, N.-N., Liu, S.-M., & Huang, H. (2024) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-024-01929-7 · Cited by 71 · see citing works
Lee, A. A., & Den Hartigh, L. J. (2025) · Frontiers in Endocrinology · doi:10.3389/fendo.2025.1682231 · Cited by 32 · see citing works
Liu, B., Wei, Y., He, J., Feng, B., Chen, Y., Guo, R., Griffin, M. D., Hynes, S. O., Shen, S., Liu, Y., et al. (2024) · Stem Cell Research & Therapy · doi:10.1186/s13287-024-03715-2 · Cited by 25 · see citing works
Nuclear receptors in metabolism and diseases: Mechanistic and therapeutic insights
Zhu, C.-Y., Yu, P., Sun, Q., Hong, D., Yang, C., & Naranmandura, H. (2025) · Pharmacological Research · doi:10.1016/j.phrs.2025.107862 · Cited by 18 · see citing works
Sex Differences in Kidney Health and Disease
Harvey, B. J., & de la Rosa, D. Á. (2024) · The Nephron journals/Nephron journals · doi:10.1159/000541352 · Cited by 20 · see citing works
Jang, W., Kim, S., Son, Y., Kim, S., Kim, H. J., Jo, H., Park, J., Lee, K., Lee, H., Tully, M. A., et al. (2024) · JMIR Public Health and Surveillance · doi:10.2196/59571 · Cited by 12 · see citing works
Self-citationMeng, Q., Li, Y., Xu, Y., & Wang, Y. (2023) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2023.166901 · Cited by 10 · see citing works
Zhuang, Z., Huang, S., Zhang, X., Han, X., Hua, M., Liang, Z., Lou, N.-J., Lv, L., Zheng, F., Zhang, L. N., et al. (2025) · International Immunopharmacology · doi:10.1016/j.intimp.2025.114266 · Cited by 9 · see citing works
Irfan, M., Ahmad, R., Ahmed, M. S., Khan, A. M., Aamir, Z., Imran, R., & Ahmed, R. (2025) · Life · doi:10.3390/life15060852 · Cited by 6 · see citing works
Regulation of Insulin Transcytosis Across Endothelium in Metabolic Health and Disease
Mineo, C., & Shaul, P. W. (2025) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.125.321545 · Cited by 6 · see citing works
Self-citationMetformin as antiviral therapy protects hyperglycemic and diabetic patients
Wang, X., Zheng, X., Ge, H., Cui, N., Lin, L., Yue, M., Zhu, C., Zhou, Q., Song, P., Shang, X., et al. (2025) · mBio · doi:10.1128/mbio.00634-25 · Cited by 5 · see citing works
Hung, T., Broz, K. S., Walk, R. E., & Tang, S. Y. (2025) · Mechanobiology in Medicine · doi:10.1016/j.mbm.2025.100132 · Cited by 5 · see citing works
FAM20A is a golgi-localized Type II transmembrane protein
Siddiqui, M. F., Li, J., Wang, S., Zhang, H., Qin, C., & Lu, Y. (2024) · Scientific Reports · doi:10.1038/s41598-024-57007-z · Cited by 5 · see citing works
Sex steroids, SHBG and type 2 diabetes in women: what do we really know?
Verhoog, N. J. D., Africander, D., & Storbeck, K. (2026) · Diabetologia · doi:10.1007/s00125-025-06647-5 · Cited by 4 · see citing works
Jia, X., Cao, X., Wang, Y., Yang, S., & Ji, L. (2025) · Nutrients · doi:10.3390/nu17132128 · Cited by 3 · see citing works
Sacharidou, A., Chambliss, K. L., Peng, J., Tanigaki, K., Islam, M. N., Sirsi, S. R., Lemoff, A. S., Hoyt, K., Mineo, C., & Shaul, P. W. (2025) · Molecular Metabolism · doi:10.1016/j.molmet.2025.102238 · Cited by 3 · see citing works
Self-citationWegermann, K., Suzuki, A., Sarmiento, E. J., Boyd, L. J., Li, Y., Wilson, L., Lloyd, A. R., Debroy, P., Price, J. C., Woreta, T. A., et al. (2025) · Open Forum Infectious Diseases · doi:10.1093/ofid/ofaf637 · Cited by 2 · see citing works
Manolopoulos, A., Mustapić, M., Nogueras‐Ortiz, C. J., Delgado‐Peraza, F., Pucha, K. A., Yao, P. J., Blommer, J. M., Vreones, M. P., York, W., Knight, D. L., et al. (2025) · Annals of Clinical and Translational Neurology · doi:10.1002/acn3.70143 · Cited by 2 · see citing works
Xin, Y., Lyu, S., Wang, Y., & Yang, Y. (2026) · International Journal of Surgery · doi:10.1097/js9.0000000000005016 · Cited by 1 · see citing works
Endothelial NPR-C promotes insulin resistance via Caveolin-1-mediated insulin transcytosis
Xu, Z.-Q., Yu, X., Wei, J., Deng, Q.-W., Zhai, W.-H., Rong, W., Li, M.-Y., Zhang, Q.-R., Gao, P., Li, X.-D., et al. (2026) · Metabolism · doi:10.1016/j.metabol.2026.156686 · Cited by 1 · see citing works
A comparison of adiponectin-deficient mice reveals the fundamental role of intracellular adiponectinPreprint
Onodera, T., Kim, D.-S., Wang, M.-Y., Virostek, M., Chen, S., Kipp, Z. A., Bates, E. A., Li, Y., Crewe, C., Li, C., et al. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.07.12.664095
Self-supervised localization of microbubbles for super-resolution ultrasound
Palaskar, R. J., & Hoyt, K. (2025) · IEEE International Ultrasonics Symposium · doi:10.1109/ius62464.2025.11201861
Self-citationBeyond GnRH analogues: The renaissance of estrogens in prostate cancer management
Matthys, M., Klein, C., Roumeguère, T., Bladou, F., Robert, G., & TOMBAL, B. F. (2026) · The French Journal of Urology · doi:10.1016/j.fjurol.2026.103139
Loss of Female Cardiovascular Protection in Diabetes: From Mechanisms to Intervention
Gady, J. P., Akter, S., VandeWiele, M., & Dong, F. (2026) · Cells · doi:10.3390/cells15211972
- Authors
- Sacharidou, A., Chambliss, K., Peng, J., Barrera, J., Tanigaki, K., Luby-Phelps, K., Özdemir, İ., Khan, S., Sirsi, S. R., Kim, S. H., Katzenellenbogen, B. S., Katzenellenbogen, J. A., Kanchwala, M., Sathe, A. A., Lemoff, A., Xing, C., Hoyt, K., Mineo, C., & Shaul, P. W.
- Affiliations
- The University of Texas Southwestern Medical Center (US)
- The University of Texas at Dallas (US)
- University of Illinois Urbana-Champaign (US)
- Corresponding author
- Mineo, Chieko
- Shaul, Philip W.
- ORCID
- Venue
- Nature Communications
- Published
- 2023-08-17
- Volume
- 14
- Issue
- 1
- Pages
- 4989-4989
- ISSN
- 2041-1723 (ISSN-L)
- PMC
- PMC10435471
- OpenAlex
- W4385954947
- Cited by
- 25
- References
- 85
- Citations by year
- 2026: 6 · 2025: 13 · 2024: 5 · 2023: 1
- FWCI
- 4.15
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Nature Communications (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- U.S. Department of Health & Human Services | NIH | National Heart, Lung, and Blood Institute (HL144572, HL098040)
- American Heart Association (19POST34390001)
- Breast Cancer Research Foundation (BCRF-083, BCRF-084)
- U.S. Department of Health & Human Services | NIH | National Institute of Diabetes and Digestive and Kidney Diseases (DK015556, DK126833, DK110127)
- U.S. Department of Health & Human Services | NIH | National Cancer Institute (CA220284)
- U.S. Department of Health & Human Services | NIH | National Institute of Biomedical Imaging and Bioengineering (EB025841)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Estrogen and related hormone effects
- Health Sciences › Medicine › Epidemiology › Adipokines, Inflammation, and Metabolic Diseases
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolism, Diabetes, and Cancer
- Keywords
- estrogen receptor alpha, endothelial cells, glucose tolerance, insulin resistance, PI3-kinase, estradiol, glucose homeostasis, obesity
- MeSH terms
- Animals, Female, Glucose, Insulin, Male, Receptors, Estrogen, Muscle, Skeletal, Endothelial Cells, Estrogen Receptor alpha, Mice
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