Publications 2011-present
Joshua St Clair, Matthew J. Westacott, Jose Miranda, Nikki L. Farnsworth, Vira Kravets, Wolfgang E Schleicher, Claire H Levitt, Audrey Heintz, Nurin W.F. Ludin, Richard KP Benninger. “Restoring Connexin-36 Function in Diabetogenic Environment Precludes Mouse and Human Islet Dysfunction and Beta-Cell Death”. Journal of Physiology (2023) Online ahead of print. doi.org/10.1113/JP282114
Jennifer K. Briggs, Vira Kravets, JaeAnn M. Dwulet, Richard KP Benninger. “What do Functional Synchronization Networks Indicate About Underlying Structure and System Dynamics? A network theory study in the islet” bioRxiv doi.org/10.1101/2022.01.06.479331 [pre-print].
Jillian Collins, Robert Piscopio, Wolfgang Schleicher, Mary E. Reyland, Richard KP Benninger, Nikki L. Farnsworth. “Cleavage of Protein Kinase C δ by Caspase-3 Mediates Pro-inflammatory Cytokine-Induced Apoptosis in the Pancreatic Islet”. bioRxiv doi.org/10.1101/2022.07.20.500512 [pre-print].
Yong Kyung Kim, Jay Walters, Nicole D. Moss, Kristen L. Wrasman, Ryan Sheridan, Jose Miranda, Richard K. P. Benninger, Richard M. O’Brien, Lori Sussel, Howard W. Davidson. “Zinc Transporter Haploinsufficiency Protects Against Beta Cell Dysfunction in Type 1 Diabetes by Increasing Mitochondrial Respiration” Molecular Metabolism (2022) 66:101632. doi.org/10.1016/j.molmet.2022.101632.
Vira Kravets, JaeAnn M. Dwulet, Wolfgang E. Schleicher, David J. Hodson, Anna M. Davis, Laura Pyle, Robert A. Piscopio, Maura Sticco-Ivins, Richard K.P. Benninger. “Functional architecture of pancreatic islets identifies a population of first responder cells that drive the first-phase calcium response” PLoS Biology (2022) 13 e3001761. doi.org/10.1371/journal.pbio.3001761.
Nikki L. Farnsworth, Robert A. Piscopio, Wolfgang E Schleicher, David G. Ramirez, Jose G. Miranda, Richard KP Benninger. “Modulation of Gap Junction Coupling within the Islet of Langerhans During the Development of Type 1 Diabetes”. Frontiers in Physiology-Metabolic Physiology (2022) 13:913611. doi.org/10.3389/fphys.2022.913611
Vinh Pham, David G. Ramirez, Richard KP Benninger. Contrast-enhanced ultrasound measurement of pancreatic blood flow dynamics predicts type1 diabetes therapeutic reversal in preclinical models. Ultrasound in Medicine and Biology (2022) 48(7): 1336-1347. doi/org/10.1016/j.ultrasmedbio.2022.03.013
Jose G. Miranda, Wolfgang E. Schleicher, David G. Ramirez, Samantha Payne-Landgrave, Richard K.P. Benninger. “Dynamic changes in β-cell electrical activity and [Ca2+] regulates NFATc3 activation and downstream gene transcription”. Molecular Metabolism (2022) 57:101430. doi.org/10.1016/j.molmet.2021.101430
Lixue Shi, Mian Wei, Yupeng Miao, Naixin Qian, Lingyan Shi, Ruth A. Singer, Richard K.P. Benninger, Wei Min. “Highly-multiplexed volumetric mapping with Raman dye imaging and tissue clearing”. Nature Biotechnology (2021). 40(3):364-373. doi.org/10.1038/s41587-021-01041-z.
Fiona M. Docherty, Kent A. Riemondy, Roberto Castro-Gutierrez, JaeAnn M. Dwulet, Ali H. Shilleh, Maria S. Hansen, Shane P.M. Williams, Lucas H. Armitage, Katherine E. Santostefano, Mark A. Wallet, Clayton E. Mathews, Taylor M. Triolo, Richard K.P. Benninger, Holger A. Russ. “ENTPD3 Marks Mature Stem Cell Derived Beta Cells Formed by Self-Aggregation in Vitro.” Diabetes (2021) 70(11):2554-2567 doi.org/10.2337/db20-0873.
David G. Ramirez, Mark Ciccaglione, Awaneesh Uphady, Vinh T. Pham, Mark A Borden, Richard K.P. Benninger. “Detecting Insulitis in Type 1 Diabetes with Ultrasound Phase-change Contrast Agents”. P.N.A.S. (2021) 118 e2022523118.
doi.org/10.1073/pnas.2022523118.
Melissa T. Adams, JaeAnn M. Dwulet, Jennifer K Briggs, Christopher A. Reissaus, Erli Jin, Joseph M. Szulczewski, Melissa R. Lyman, Sophia M. Sdao, Vira Kravets, Sutichot D. Nimkulrat, Suzanne M. Ponik, Matthew J. Merrins, Raghavendra G. Mirmira, Amelia K. Linnemann, Richard K.P. Benninger, Barak Blum. “Reduced synchroneity of intra-islet Ca2+ oscillations in vivo in Robo-deficient β cells ”. eLife (2021) 10:e61308. doi.org/10.7554/eLife.61308.
JaeAnn M Dwulet, Jennifer K. Briggs, Richard KP Benninger. Small subpopulations of β-cells do not drive islet oscillatory [Ca2+] dynamics via gap junction communication. PLoS Computational Biology (2021) 17(5): e1008948.
doi.org/10.1371/journal.pcbi.1008948
Alec N. Thomas, Kang-Ho Song, Awaneesh Upadhyay, Virginie Papadopoulou, David Ramirez, Richard K. P. Benninger, Matthew Lowerison, Pengfei Song, Todd W. Murray and Mark A. Borden “Contrast-enhanced sonography with biomimetic lung surfactant nanodrops” Langmuir (2021) 37, 7, 2386–2396. doi.org/10.1021/acs.langmuir.0c03349.
Arjun K. Fontaine, David G. Ramirez, Samuel Littich, Vira Kravets, John H. Caldwell, Richard F. Weir, Richard K.P. Benninger. “Optogenetic Stimulation of Pancreatic Function via Vagal Cholinergic Axons”. Scientific Reports, (2021) 11, 3670.
doi.org/10.1038/s41598-021-83361-3.
David G. Ramirez, Eric Abenojar, Christopher Hernandez, David S. Lorberbaum, Lucine A. Papazian, Samantha Passman, Vinh Pham, Agata A. Exner, Richard KP Benninger. “Contrast-enhanced ultrasound with sub-micron sized contrast agents detects insulitis in mouse models of type 1 diabetes”. Nature Communications (2020) 11(1) p2238. doi.org/10.1038/s41467-020-15957-8
Maria Esméria Corezola do Amaral, Vira Kravets, JaeAnn M. Dwulet, Nikki L. Farnsworth, Robert Piscopio, Wolfgang E. Schleicher, Jose G. Miranda and Richard K. P. Benninger. "Caloric Restriction recovers impaired β-cell-β-cell coupling, calcium oscillation coordination and insulin secretion in obese, prediabetic mice." American journal of Physiology - Endocrinology and Metabolism (2020) American Journal of Physiology – Endocrinology & Metabolism. (2020) 319 ppE709-720. doi.org/10.1152/ajpendo.00132.2020
Kelly M.T. Shekiro, Thomas H. Hraha, Abigail B. Bernard, Richard K.P. Benninger, Kristi S. Anseth. “Uniform, 3-dimensional pseudo-islets from primary murine islets with improved functional properties”. bioRxiv (2020) doi.org/10.1101/2020.02.07.939538 [pre-print].
JaeAnn Dwulet*, Nurin F.W. Ludin*, Robert Piscopio, Wolf Schleicher Ong Moua, Matthew J. Westacott, Richard KP Benninger. “How gap junction electrical coupling regulates the electrical response of β-cells that are heterogeneous in glucokinase activity.” Biophysical Journal (2019) 117(11) pp2188-2203 (* Equal contributors) doi.org/10.1016/j.bpj.2019.10.037
Karin J. Bosma, Kristen E. Syring, James K. Oeser, Jason D. Lee, Richard K.P. Benninger, Matthew E. Pamenter, and Richard M. O’Brien. “Evidence That Evolution of the Diabetes Susceptibility Gene SLC30A8 that Encodes the Zinc Transporter ZnT8 Drives Variations in Pancreatic Islet Zinc Content in Multiple Species”. Journal of Molecular Evolution (2019) 87(4-6) pp147-151.
doi.org/10.1007/s00239-019-09898-0
Nikki L. Farnsworth*, Rachelle S Walter*, Robert Piscopio, Wolfgang Schleicher, Richard K.P. Benninger. “Exendin-4 Overcomes Cytokine-Induced Decreases in Electrical Coupling via PKA and Epac2 in Mouse and Human Islets”. Journal of Physiology (2019) 597(2) pp431-447. (* Equal contributors) doi.org/10.1113/JP276106
Joshua R St Clair, David Ramirez, Samantha Passman, Richard K.P. Benninger. “Contrast-enhanced ultrasound measurement of pancreatic blood flow dynamics predicts type1 diabetes progression and therapeutic reversal.” Nature Communications (2018) 9 pp1742. doi.org/10.1038/s41467-018-03953-y
Matthew J. Westacott, Nurin W. Ludin, Richard K.P. Benninger. “Spatially organized sub-populations of cells control electrical activity and dynamics across the islets of Langerhans”. Biophysical Journal (2017) 113(5) pp1093-1108.
doi.org/10.1016/j.bpj.2017.07.021
Matthew J. Westacott, Nikki L Farnsworth, Joshua R St Clair, Audrey Heintz, Greg Poffenberger, Audrey Heintz, Nurin L Ludin, Nathaniel Hart, Alvin C Powers, Richard K.P. Benninger. “Age-dependent decline in the coordinated [Ca2+] and insulin secretory response in human pancreatic islets”. Diabetes. (2017) 66(9) pp2436-2445. doi.org/10.2337/db17-0137
Aleena M. Notary, Matthew J. Westacott, Thomas H. Hraha, Marina Pozzoli, Richard K.P. Benninger. “Gap junction modulation recovers [Ca2+] and insulin secretion in Neonatal Diabetes Mellitus dependent on beta cell heterogeneity and noise”. PLoS Computational Biology. (2016) 12(9) e1005116. doi.org/10.1371/journal.pcbi.1005116
Nikki L. Farnsworth, Rachelle Walter, Alireza Hemmati, Matthew J. Westacott, Richard K.P. Benninger. “Proinflammatory Cytokines Decrease Gap Junction Coupling through NO Mediated PKCδ Phosphorylation of Connexin36 in Mouse and Human Islets”. Journal of Biological Chemistry (2015) 291 pp3184-96. doi.org/10.1074/jbc.M115.679506
Eva Nozik-Grayck, Crystal Woods, Joann M. Taylor, Richard K.P. Benninger, Richard D. Johnson, Leah R. Villegas, Kurt R. Stenmark, David Harrison, Susan M. Majka, David Irwin, Kathryn N. Farrow. “Selective depletion of vascular EC-SOD augments chronic hypoxic pulmonary hypertension” American Journal of Physiology- Lung Cellular and Molecular Physiology (2014) 307 L868-876. doi.org/10.1152/ajplung.00096.2014
Richard K.P. Benninger, Troy Hutchens, W. Steven Head, Min Zhang, Sylvain J. Le Marchand, Leslie S. Satin, David W. Piston. “Intrinsic islet heterogeneity and gap junction coupling determine spatiotemporal Ca2+ wave dynamics” Biophysical Journal (2014) 107 pp2723-2733. doi.org/10.1016/j.bpj.2014.10.048
Nikki L. Farnsworth, Alireza Hemmati, Marina Pozzoli, Richard K.P. Benninger. “Fluorescence Recovery After Photobleaching Reveals Regulation and Distribution of Cx36 Gap Junction Coupling within Mouse Islets of Langerhans” Journal of Physiology (2014) 592 pp4431-4446. doi.org/10.1113/jphysiol.2014.276733
Thomas H. Hraha*, Matthew J. Westacott*, Marina Pozzoli, Aleena M. Notary, P. Mason McClatchey, Richard K.P. Benninger. “Phase Transitions in the Multi-cellular Regulatory Behavior of Pancreatic Islet Excitability” PLoS Computational Biology (2014) 10(9) e1003819. (* Equal contributors) doi.org/10.1371/journal.pcbi.1003819
John M. Hartney, Timothy Stidham, David A. Goldstrohm, Rebecca E. Oberley-Deegan, Michael R. Weaver, Zuzana Valnickova-Hansen, Carsten Scavenius, Richard K.P. Benninger, Katelyn F. Leahy, Richard Johnson, Fabienne Gally, Beata Kosmider , Angela K. Zimmermann, Jan J. Enghild, Eva Nozik-Grayck, Russell P. Bowler. “A common polymorphism in extracellular superoxide dismutase (SOD3) affects cardiopulmonary disease risk by altering tissue protein distribution” Circulation: Cardiovascular Genetics (2014) 7 pp659-666. doi.org/10.1161/CIRCGENETICS.113.000504
Yan Hang, Tsunehiko Yamamoto, Richard K.P. Benninger, Marcela Brissova, Min Guo, Frederick H. Thompson, Will Bush, David Piston, Alvin C Powers, Mark Magnuson, Debbie Thurmond, Roland Stein. “The MafA transcription factor becomes important to islet β-cells soon after birth” Diabetes (2014) 63 pp1994-2005. doi.org/10.2337/db13-1001
Linda M. Nguyen, Marina Pozzoli, Thomas H. Hraha, Richard K.P. Benninger. “Decreasing Cx36 gap junction coupling compensates for overactive KATP channels to restore insulin secretion and prevent hyperglycemia in a mouse model of neonatal diabetes” Diabetes (2014) 63(5) pp1685-97. doi.org/10.2337/db13-1048
Thomas H. Hraha, Abigail B. Bernard, Linda M Nguyen, Kristi S. Anseth, Richard K.P. Benninger. “Dimensionality and size scaling of coordinated Ca2+ dynamics in pancreatic β-cell clusters” Biophysical Journal (2014) 106 pp299-309. doi.org/10.1016/j.bpj.2013.11.026
W. Steven Head, Meredith L. Orseth, Craig S. Nunemaker, Leslie S. Satin, David W. Piston, Richard K.P. Benninger. “Connexin-36 gap junctions regulate in-vivo first and second phase insulin secretion dynamics and glucose tolerance in the conscious mouse” Diabetes (2012) 6 pp1700-07. *Special Commentary. doi.org/10.2337/db11-1312
Jennifer K. Briggs, Vira Kravets, JaeAnn M. Dwulet, Richard KP Benninger. “What do Functional Synchronization Networks Indicate About Underlying Structure and System Dynamics? A network theory study in the islet” bioRxiv doi.org/10.1101/2022.01.06.479331 [pre-print].
Jillian Collins, Robert Piscopio, Wolfgang Schleicher, Mary E. Reyland, Richard KP Benninger, Nikki L. Farnsworth. “Cleavage of Protein Kinase C δ by Caspase-3 Mediates Pro-inflammatory Cytokine-Induced Apoptosis in the Pancreatic Islet”. bioRxiv doi.org/10.1101/2022.07.20.500512 [pre-print].
Yong Kyung Kim, Jay Walters, Nicole D. Moss, Kristen L. Wrasman, Ryan Sheridan, Jose Miranda, Richard K. P. Benninger, Richard M. O’Brien, Lori Sussel, Howard W. Davidson. “Zinc Transporter Haploinsufficiency Protects Against Beta Cell Dysfunction in Type 1 Diabetes by Increasing Mitochondrial Respiration” Molecular Metabolism (2022) 66:101632. doi.org/10.1016/j.molmet.2022.101632.
Vira Kravets, JaeAnn M. Dwulet, Wolfgang E. Schleicher, David J. Hodson, Anna M. Davis, Laura Pyle, Robert A. Piscopio, Maura Sticco-Ivins, Richard K.P. Benninger. “Functional architecture of pancreatic islets identifies a population of first responder cells that drive the first-phase calcium response” PLoS Biology (2022) 13 e3001761. doi.org/10.1371/journal.pbio.3001761.
Nikki L. Farnsworth, Robert A. Piscopio, Wolfgang E Schleicher, David G. Ramirez, Jose G. Miranda, Richard KP Benninger. “Modulation of Gap Junction Coupling within the Islet of Langerhans During the Development of Type 1 Diabetes”. Frontiers in Physiology-Metabolic Physiology (2022) 13:913611. doi.org/10.3389/fphys.2022.913611
Vinh Pham, David G. Ramirez, Richard KP Benninger. Contrast-enhanced ultrasound measurement of pancreatic blood flow dynamics predicts type1 diabetes therapeutic reversal in preclinical models. Ultrasound in Medicine and Biology (2022) 48(7): 1336-1347. doi/org/10.1016/j.ultrasmedbio.2022.03.013
Jose G. Miranda, Wolfgang E. Schleicher, David G. Ramirez, Samantha Payne-Landgrave, Richard K.P. Benninger. “Dynamic changes in β-cell electrical activity and [Ca2+] regulates NFATc3 activation and downstream gene transcription”. Molecular Metabolism (2022) 57:101430. doi.org/10.1016/j.molmet.2021.101430
Lixue Shi, Mian Wei, Yupeng Miao, Naixin Qian, Lingyan Shi, Ruth A. Singer, Richard K.P. Benninger, Wei Min. “Highly-multiplexed volumetric mapping with Raman dye imaging and tissue clearing”. Nature Biotechnology (2021). 40(3):364-373. doi.org/10.1038/s41587-021-01041-z.
Fiona M. Docherty, Kent A. Riemondy, Roberto Castro-Gutierrez, JaeAnn M. Dwulet, Ali H. Shilleh, Maria S. Hansen, Shane P.M. Williams, Lucas H. Armitage, Katherine E. Santostefano, Mark A. Wallet, Clayton E. Mathews, Taylor M. Triolo, Richard K.P. Benninger, Holger A. Russ. “ENTPD3 Marks Mature Stem Cell Derived Beta Cells Formed by Self-Aggregation in Vitro.” Diabetes (2021) 70(11):2554-2567 doi.org/10.2337/db20-0873.
David G. Ramirez, Mark Ciccaglione, Awaneesh Uphady, Vinh T. Pham, Mark A Borden, Richard K.P. Benninger. “Detecting Insulitis in Type 1 Diabetes with Ultrasound Phase-change Contrast Agents”. P.N.A.S. (2021) 118 e2022523118.
doi.org/10.1073/pnas.2022523118.
Melissa T. Adams, JaeAnn M. Dwulet, Jennifer K Briggs, Christopher A. Reissaus, Erli Jin, Joseph M. Szulczewski, Melissa R. Lyman, Sophia M. Sdao, Vira Kravets, Sutichot D. Nimkulrat, Suzanne M. Ponik, Matthew J. Merrins, Raghavendra G. Mirmira, Amelia K. Linnemann, Richard K.P. Benninger, Barak Blum. “Reduced synchroneity of intra-islet Ca2+ oscillations in vivo in Robo-deficient β cells ”. eLife (2021) 10:e61308. doi.org/10.7554/eLife.61308.
JaeAnn M Dwulet, Jennifer K. Briggs, Richard KP Benninger. Small subpopulations of β-cells do not drive islet oscillatory [Ca2+] dynamics via gap junction communication. PLoS Computational Biology (2021) 17(5): e1008948.
doi.org/10.1371/journal.pcbi.1008948
Alec N. Thomas, Kang-Ho Song, Awaneesh Upadhyay, Virginie Papadopoulou, David Ramirez, Richard K. P. Benninger, Matthew Lowerison, Pengfei Song, Todd W. Murray and Mark A. Borden “Contrast-enhanced sonography with biomimetic lung surfactant nanodrops” Langmuir (2021) 37, 7, 2386–2396. doi.org/10.1021/acs.langmuir.0c03349.
Arjun K. Fontaine, David G. Ramirez, Samuel Littich, Vira Kravets, John H. Caldwell, Richard F. Weir, Richard K.P. Benninger. “Optogenetic Stimulation of Pancreatic Function via Vagal Cholinergic Axons”. Scientific Reports, (2021) 11, 3670.
doi.org/10.1038/s41598-021-83361-3.
David G. Ramirez, Eric Abenojar, Christopher Hernandez, David S. Lorberbaum, Lucine A. Papazian, Samantha Passman, Vinh Pham, Agata A. Exner, Richard KP Benninger. “Contrast-enhanced ultrasound with sub-micron sized contrast agents detects insulitis in mouse models of type 1 diabetes”. Nature Communications (2020) 11(1) p2238. doi.org/10.1038/s41467-020-15957-8
Maria Esméria Corezola do Amaral, Vira Kravets, JaeAnn M. Dwulet, Nikki L. Farnsworth, Robert Piscopio, Wolfgang E. Schleicher, Jose G. Miranda and Richard K. P. Benninger. "Caloric Restriction recovers impaired β-cell-β-cell coupling, calcium oscillation coordination and insulin secretion in obese, prediabetic mice." American journal of Physiology - Endocrinology and Metabolism (2020) American Journal of Physiology – Endocrinology & Metabolism. (2020) 319 ppE709-720. doi.org/10.1152/ajpendo.00132.2020
Kelly M.T. Shekiro, Thomas H. Hraha, Abigail B. Bernard, Richard K.P. Benninger, Kristi S. Anseth. “Uniform, 3-dimensional pseudo-islets from primary murine islets with improved functional properties”. bioRxiv (2020) doi.org/10.1101/2020.02.07.939538 [pre-print].
JaeAnn Dwulet*, Nurin F.W. Ludin*, Robert Piscopio, Wolf Schleicher Ong Moua, Matthew J. Westacott, Richard KP Benninger. “How gap junction electrical coupling regulates the electrical response of β-cells that are heterogeneous in glucokinase activity.” Biophysical Journal (2019) 117(11) pp2188-2203 (* Equal contributors) doi.org/10.1016/j.bpj.2019.10.037
Karin J. Bosma, Kristen E. Syring, James K. Oeser, Jason D. Lee, Richard K.P. Benninger, Matthew E. Pamenter, and Richard M. O’Brien. “Evidence That Evolution of the Diabetes Susceptibility Gene SLC30A8 that Encodes the Zinc Transporter ZnT8 Drives Variations in Pancreatic Islet Zinc Content in Multiple Species”. Journal of Molecular Evolution (2019) 87(4-6) pp147-151.
doi.org/10.1007/s00239-019-09898-0
Nikki L. Farnsworth*, Rachelle S Walter*, Robert Piscopio, Wolfgang Schleicher, Richard K.P. Benninger. “Exendin-4 Overcomes Cytokine-Induced Decreases in Electrical Coupling via PKA and Epac2 in Mouse and Human Islets”. Journal of Physiology (2019) 597(2) pp431-447. (* Equal contributors) doi.org/10.1113/JP276106
Joshua R St Clair, David Ramirez, Samantha Passman, Richard K.P. Benninger. “Contrast-enhanced ultrasound measurement of pancreatic blood flow dynamics predicts type1 diabetes progression and therapeutic reversal.” Nature Communications (2018) 9 pp1742. doi.org/10.1038/s41467-018-03953-y
Matthew J. Westacott, Nurin W. Ludin, Richard K.P. Benninger. “Spatially organized sub-populations of cells control electrical activity and dynamics across the islets of Langerhans”. Biophysical Journal (2017) 113(5) pp1093-1108.
doi.org/10.1016/j.bpj.2017.07.021
Matthew J. Westacott, Nikki L Farnsworth, Joshua R St Clair, Audrey Heintz, Greg Poffenberger, Audrey Heintz, Nurin L Ludin, Nathaniel Hart, Alvin C Powers, Richard K.P. Benninger. “Age-dependent decline in the coordinated [Ca2+] and insulin secretory response in human pancreatic islets”. Diabetes. (2017) 66(9) pp2436-2445. doi.org/10.2337/db17-0137
Aleena M. Notary, Matthew J. Westacott, Thomas H. Hraha, Marina Pozzoli, Richard K.P. Benninger. “Gap junction modulation recovers [Ca2+] and insulin secretion in Neonatal Diabetes Mellitus dependent on beta cell heterogeneity and noise”. PLoS Computational Biology. (2016) 12(9) e1005116. doi.org/10.1371/journal.pcbi.1005116
Nikki L. Farnsworth, Rachelle Walter, Alireza Hemmati, Matthew J. Westacott, Richard K.P. Benninger. “Proinflammatory Cytokines Decrease Gap Junction Coupling through NO Mediated PKCδ Phosphorylation of Connexin36 in Mouse and Human Islets”. Journal of Biological Chemistry (2015) 291 pp3184-96. doi.org/10.1074/jbc.M115.679506
Eva Nozik-Grayck, Crystal Woods, Joann M. Taylor, Richard K.P. Benninger, Richard D. Johnson, Leah R. Villegas, Kurt R. Stenmark, David Harrison, Susan M. Majka, David Irwin, Kathryn N. Farrow. “Selective depletion of vascular EC-SOD augments chronic hypoxic pulmonary hypertension” American Journal of Physiology- Lung Cellular and Molecular Physiology (2014) 307 L868-876. doi.org/10.1152/ajplung.00096.2014
Richard K.P. Benninger, Troy Hutchens, W. Steven Head, Min Zhang, Sylvain J. Le Marchand, Leslie S. Satin, David W. Piston. “Intrinsic islet heterogeneity and gap junction coupling determine spatiotemporal Ca2+ wave dynamics” Biophysical Journal (2014) 107 pp2723-2733. doi.org/10.1016/j.bpj.2014.10.048
Nikki L. Farnsworth, Alireza Hemmati, Marina Pozzoli, Richard K.P. Benninger. “Fluorescence Recovery After Photobleaching Reveals Regulation and Distribution of Cx36 Gap Junction Coupling within Mouse Islets of Langerhans” Journal of Physiology (2014) 592 pp4431-4446. doi.org/10.1113/jphysiol.2014.276733
Thomas H. Hraha*, Matthew J. Westacott*, Marina Pozzoli, Aleena M. Notary, P. Mason McClatchey, Richard K.P. Benninger. “Phase Transitions in the Multi-cellular Regulatory Behavior of Pancreatic Islet Excitability” PLoS Computational Biology (2014) 10(9) e1003819. (* Equal contributors) doi.org/10.1371/journal.pcbi.1003819
John M. Hartney, Timothy Stidham, David A. Goldstrohm, Rebecca E. Oberley-Deegan, Michael R. Weaver, Zuzana Valnickova-Hansen, Carsten Scavenius, Richard K.P. Benninger, Katelyn F. Leahy, Richard Johnson, Fabienne Gally, Beata Kosmider , Angela K. Zimmermann, Jan J. Enghild, Eva Nozik-Grayck, Russell P. Bowler. “A common polymorphism in extracellular superoxide dismutase (SOD3) affects cardiopulmonary disease risk by altering tissue protein distribution” Circulation: Cardiovascular Genetics (2014) 7 pp659-666. doi.org/10.1161/CIRCGENETICS.113.000504
Yan Hang, Tsunehiko Yamamoto, Richard K.P. Benninger, Marcela Brissova, Min Guo, Frederick H. Thompson, Will Bush, David Piston, Alvin C Powers, Mark Magnuson, Debbie Thurmond, Roland Stein. “The MafA transcription factor becomes important to islet β-cells soon after birth” Diabetes (2014) 63 pp1994-2005. doi.org/10.2337/db13-1001
Linda M. Nguyen, Marina Pozzoli, Thomas H. Hraha, Richard K.P. Benninger. “Decreasing Cx36 gap junction coupling compensates for overactive KATP channels to restore insulin secretion and prevent hyperglycemia in a mouse model of neonatal diabetes” Diabetes (2014) 63(5) pp1685-97. doi.org/10.2337/db13-1048
Thomas H. Hraha, Abigail B. Bernard, Linda M Nguyen, Kristi S. Anseth, Richard K.P. Benninger. “Dimensionality and size scaling of coordinated Ca2+ dynamics in pancreatic β-cell clusters” Biophysical Journal (2014) 106 pp299-309. doi.org/10.1016/j.bpj.2013.11.026
W. Steven Head, Meredith L. Orseth, Craig S. Nunemaker, Leslie S. Satin, David W. Piston, Richard K.P. Benninger. “Connexin-36 gap junctions regulate in-vivo first and second phase insulin secretion dynamics and glucose tolerance in the conscious mouse” Diabetes (2012) 6 pp1700-07. *Special Commentary. doi.org/10.2337/db11-1312
Review articles 2011-present
Richard K P Benninger, Vira Kravets. “The Physiological role of Beta cell Heterogeneity” Nature Reviews Endocrinology (2022) 18(1): 9-22. doi.org/10.1038/s41574-021-00568-0
Vira Kravets, Richard K P Benninger. “From the Transcriptome to Electrophysiology: Searching for the Underlying Cause of Diabetes” Cell Metabolism (2020) 31(5) pp888-889. doi.org/10.1016/j.cmet.2020.04.012
Richard K.P. Benninger, Craig Dorrell, David J Hodson, Guy A Rutter “The Impact of Pancreatic Beta Cell Heterogeneity on Type 1 Diabetes Pathogenesis.” Current Diabetes Reports. (2018) 18(11) p112.
doi.org/10.1007/s11892-018-1085-2
Richard K.P. Benninger and David J Hodson “New understanding of beta cell heterogeneity and in-situ islet function” Diabetes (2018) 67(4) pp537-547. doi.org/10.2337/dbi17-0040
Craig S. Nunemaker, Richard K.P. Benninger. “Zinc Transport Gets Its Zing Back: Double-Knockout of ZnT7 and ZnT8 Reveals the Importance of Zinc Transporters to Insulin Secretion”.Endocrinology. (2016) 157(12):4542-4544.
doi.org/10.1210/en.2016-1797
Richard K.P. Benninger “Fluorescence Linear Dichroism Imaging for Quantifying Membrane Order” (2015) 1232:pp161-179. Methods in Membrane Lipids Ed: D.M.Owen. doi.org/10.1007/978-1-4939-1752-5_14
David W. Piston, Richard K.P. Benninger. “Cellular Communication and Heterogeneity in the Dynamics of Pancreatic Islet Insulin Secretion” Trends in Endocrinology and Metabolism. (2014) 25(8) pp399-406. Invited Review.
doi.org/10.1016/j.tem.2014.02.005
Nikki L. Farnsworth, Richard K.P. Benninger. “New insights into the role of connexins in pancreatic islet function and diabetes” FEBS Letters. (2014) 588(8) pp1278-1287, Invited Review. doi.org/10.1016/j.febslet.2014.02.035
Richard K.P. Benninger and David W. Piston “Two-Photon Excitation Microscopy for the Study of Living Cells, Tissue and In-vivo” Current Protocols in Cell Biology, (2013) 59:4.11.1-4.11.24. doi.org/10.1002/0471143030.cb0411s59
Vira Kravets, Richard K P Benninger. “From the Transcriptome to Electrophysiology: Searching for the Underlying Cause of Diabetes” Cell Metabolism (2020) 31(5) pp888-889. doi.org/10.1016/j.cmet.2020.04.012
Richard K.P. Benninger, Craig Dorrell, David J Hodson, Guy A Rutter “The Impact of Pancreatic Beta Cell Heterogeneity on Type 1 Diabetes Pathogenesis.” Current Diabetes Reports. (2018) 18(11) p112.
doi.org/10.1007/s11892-018-1085-2
Richard K.P. Benninger and David J Hodson “New understanding of beta cell heterogeneity and in-situ islet function” Diabetes (2018) 67(4) pp537-547. doi.org/10.2337/dbi17-0040
Craig S. Nunemaker, Richard K.P. Benninger. “Zinc Transport Gets Its Zing Back: Double-Knockout of ZnT7 and ZnT8 Reveals the Importance of Zinc Transporters to Insulin Secretion”.Endocrinology. (2016) 157(12):4542-4544.
doi.org/10.1210/en.2016-1797
Richard K.P. Benninger “Fluorescence Linear Dichroism Imaging for Quantifying Membrane Order” (2015) 1232:pp161-179. Methods in Membrane Lipids Ed: D.M.Owen. doi.org/10.1007/978-1-4939-1752-5_14
David W. Piston, Richard K.P. Benninger. “Cellular Communication and Heterogeneity in the Dynamics of Pancreatic Islet Insulin Secretion” Trends in Endocrinology and Metabolism. (2014) 25(8) pp399-406. Invited Review.
doi.org/10.1016/j.tem.2014.02.005
Nikki L. Farnsworth, Richard K.P. Benninger. “New insights into the role of connexins in pancreatic islet function and diabetes” FEBS Letters. (2014) 588(8) pp1278-1287, Invited Review. doi.org/10.1016/j.febslet.2014.02.035
Richard K.P. Benninger and David W. Piston “Two-Photon Excitation Microscopy for the Study of Living Cells, Tissue and In-vivo” Current Protocols in Cell Biology, (2013) 59:4.11.1-4.11.24. doi.org/10.1002/0471143030.cb0411s59
Publications and Review articles pre-2011
Richard K.P. Benninger, W. Steven Head, Min Zhang, Leslie S. Satin, David W. Piston. “Gap junctions act in combination with other mechanisms of cell-cell communication to suppress basal insulin secretion in the islet of Langerhans” Journal of Physiology (2011) 589 pp5453-66. doi.org/10.1113/jphysiol.2011.218909
Richard K.P. Benninger, Maria S. Remedi, Alessandro Ustione, W. Steven Head, David W. Piston, Colin G. Nichols. “Defects in β-cell Ca2+ signalling and glucose metabolism underlie defective insulin secretion in a model of KATP channel-induced neonatal diabetes mellitus” Diabetologia (2011) 54 pp1087-97. doi.org/10.1007/s00125-010-2039-7
Aizhen Zhao, Yuhan Hao, Marcella Brissova, Richard K.P. Benninger, Joel Abramowitz, Guylain Boulay Alvin C. Powers, David W. Piston, Meisheng Jiang, Lutz Birnbaumer, Guoqiang Gu. “GαO represses insulin secretion by regulating insulin vesicular docking in pancreatic β cells” Diabetes (2010) 59 pp2522-9.
doi.org/10.2337/db09-1719
Michael Meyer-Hermann, Richard K. P. Benninger “A mathematical model of β-cells in an islet of Langerhans sensing a glucose gradient” HFSP Journal (2010) 4 pp61-71. doi.org/10.2976/1.3354862
Lynley D. Pound, Suparna Sarkar, Richard K.P. Benninger, Yingda Wang, Adisak Suwanichkul, Melanie K. Shadoan, Richard L. Printz, James K. Oeser, Catherine E. Lee, David W. Piston, Owen P. McGuinness, John C. Hutton, David R. Powell, Richard M. O'Brien “Deletion of the Mouse Slc30a8 Gene Encoding Zinc Transporter-8 Results in Impaired Insulin Secretion” Biochemical Journal (2009) 421 pp371-376. doi.org/10.1042/BJ20090530
Christopher J. Easley, Richard K.P. Benninger, Jesse H. Shaver, W. Steven Head, David W. Piston “Rapid and inexpensive fabrication of polymeric microfluidic devices via toner transfer masking” Lab on a Chip (2009) 9 pp1119-1127. doi.org/10.1039/b816575k
Subhadra C. Gunawardana, Richard K.P. Benninger, David W. Piston “Subcutaneous transplantation of embryonic pancreas for correction of type 1 diabetes” American Journal of Physiology- Endocrinology and Metabolism (2009) 296 E323-332. doi.org/10.1152/ajpendo.90544.2008
Richard K.P. Benninger, Bruno Vanherberghen, Stephen Young, Sabrina Tanner, Fiona F. Culley, Tim Schnyder, Mark A.A. Neil, Daniel Wüstner, Paul M.W. French, Daniel M. Davis, Björn Önfelt “Live cell linear dichroism imaging reveals extensive membrane ruffling within the docking structure of Natural Killer cell immune synapses” Biophysical Journal- Biophysical Letters (2009) 96 L13-15. doi.org/10.1016/j.bpj.2008.10.005
David W. Piston, Gert-Jan Kremers, Richard K.P. Benninger, and Michael W. Davidson “Photoactivation in Fluorescence Microscopy” Microscopy Today (2009) 17 pp8-13. doi.org/10.1017/S1551929509000194
Richard K.P. Benninger, David W Piston. “Recent Advances in Single-photon-counting Detection Technology in Fluorescence Microscopy” Laser Focus World. (2009) June: pp59-63.
Richard K.P. Benninger, William J. Ashby, Elisabeth A. Ring, David W. Piston “A single-photon counting detector for increased sensitivity in two-photon laser scanning microscopy” Optics Letters (2008) 33: pp2895-7.
doi.org/10.1364/OL.33.002895
Richard K.P. Benninger, Min Zhang, W. Steven Head, Leslie S Satin, David W. Piston “Gap Junction Coupling and Calcium Waves in the Pancreatic Islet” Biophysical Journal (2008) 95: pp5048- 5061.
doi.org/10.1529/biophysj.108.140863
Richard K.P. Benninger*, Shu Mao*, Yuling Yan, Chutima Petchprayoon, David Jackson, Chistopher J. Easley, David W. Piston, Gerard Marriott “Optical lock-in detection of fluorescence resonance energy transfer using synthetic and genetically-encoded optical switches” Biophysical Journal (2008) 94: pp4515-24. (* Equal contributors).
doi.org/10.1529/biophysj.107.124859
Richard K.P. Benninger, Mingming Hao, David W. Piston. “Multi-photon Excitation Imaging of Dynamic Processes in Living Cells and Tissues” Reviews of Physiology, Biochemistry and Pharmacology (2008) 160: pp71-92. doi.org/10.1007/112_2008_801
Sunil Kumar, Christopher Dunsby, Pieter A.A. DeBeule, Dylan M. Owen, U Anand, Peter M.P. Lanigan, Richard K.P. Benninger, Daniel M. Davis, Mark A.A. Neil, Praveen Anand, Cristopher Benham, Alan Naylor, Paul M.W. French. “Multifocal multiphoton excitation and time correlated single photon counting detection for 3-D fluorescence lifetime imaging” Optics Express. (2007) 15: pp12548-12561. doi.org/10.1364/OE.15.012548
Richard K.P. Benninger, Oliver Hoffman, Björn Önfelt, Ian Munro, Christopher Dunsby, Daniel M. Davis, Mark A.A. Neil, Paul M.W. French, Andrew J. deMello. “Fluorescence Lifetime Imaging of Dye: DNA Interactions within Continuous Flow Microfluidic Systems” Angewandte Chemie International Edition (English). (2007) 46: pp2228-2231. doi.org/10.1002/anie.200604112
Pieter DeBeule, Dylan M. Owen, Hugh B. Manning, Clifford B. Talbot, Jose Requejo-Isidro, Christopher Dunsby, James McGinty, Richard K.P. Benninger, Daniel Elson, Ian Munro, M. John Lever, Pravene Anand, Mark A.A. Neil, Paul M.W. French. “Rapid Hyperspectral Fluorescence Lifetime Imaging” Microscopy Research Techniques (2007) 70: pp481-484. doi.org/10.1002/jemt.20434
Björn Önfelt, Shlomo Nedvetski, Richard K.P. Benninger, Mark A Perbhoo, Stefanie Sowinski, Alistair N. Hume, Miguel C. Seabra, Mark A.A. Neil, Paul M.W. French, Daniel M. Davis. “Structurally Distinct Membrane Nanotubes between Human Macrophages Support Long-Distance Vesicular Traffic or Surfing of Bacteria” Journal Immunology (2006) 177: pp8476-83. doi.org/10.4049/jimmunol.177.12.8476
Richard K.P. Benninger, Yasemin Koç, Oliver Hoffman, Jose Requejo-Isidro, Mark A.A. Neil, Paul M.W. French, Andrew J. deMello. “Quantitative 3D Mapping of Fluidic Temperatures within Microchannel Networks Using Fluorescence Lifetime Imaging” Analytical. Chemistry (2006) 78: pp2272-2278. doi.org/10.1021/ac051990f
Richard K.P. Benninger, Oliver Hoffman, James McGinty, Jose Requejo-Isidro, Ian Munro, Mark A.A. Neil, Andrew J. deMello, Paul M.W. French. “Time-resolved fluorescence imaging of solvent interactions in microfluidic devices” Optics Express. (2006) 13: pp6275-6285. doi.org/10.1364/OPEX.13.006275
Richard K.P. Benninger, Björn Önfelt, Mark A.A. Neil, Daniel M. Davis, Paul M.W. French. “Fluorescence Imaging of Two-Photon Linear Dichroism: Cholesterol Depletion disrupts Molecular Orientation in Cell Membranes.” Biophysical Journal (2005) 88: pp609-622. doi.org/10.1529/biophysj.104.050096
Daniel Elson, Jose Requejo-Isidro, Ian Munro, Fred Reavell, Jan Siegel, Klaus Suhling, Paul Tadrous, Richard Benninger, Peter Lanigan, James McGinty, Clifford Talbot, Bebhinn Treanor, Stephen Webb, Anne Sandison, Andrew Wallace, Daniel Davis, John Lever, Mark Neil, David Phillips, Gordon Stamp, Paul French. “A Perspective: Time-domain fluorescence lifetime imaging applied to biological tissue.” Photochemical Photobiological Sciences (2004) 3: pp795–801. doi.org/10.1039/B316456J
Richard K.P. Benninger, Maria S. Remedi, Alessandro Ustione, W. Steven Head, David W. Piston, Colin G. Nichols. “Defects in β-cell Ca2+ signalling and glucose metabolism underlie defective insulin secretion in a model of KATP channel-induced neonatal diabetes mellitus” Diabetologia (2011) 54 pp1087-97. doi.org/10.1007/s00125-010-2039-7
Aizhen Zhao, Yuhan Hao, Marcella Brissova, Richard K.P. Benninger, Joel Abramowitz, Guylain Boulay Alvin C. Powers, David W. Piston, Meisheng Jiang, Lutz Birnbaumer, Guoqiang Gu. “GαO represses insulin secretion by regulating insulin vesicular docking in pancreatic β cells” Diabetes (2010) 59 pp2522-9.
doi.org/10.2337/db09-1719
Michael Meyer-Hermann, Richard K. P. Benninger “A mathematical model of β-cells in an islet of Langerhans sensing a glucose gradient” HFSP Journal (2010) 4 pp61-71. doi.org/10.2976/1.3354862
Lynley D. Pound, Suparna Sarkar, Richard K.P. Benninger, Yingda Wang, Adisak Suwanichkul, Melanie K. Shadoan, Richard L. Printz, James K. Oeser, Catherine E. Lee, David W. Piston, Owen P. McGuinness, John C. Hutton, David R. Powell, Richard M. O'Brien “Deletion of the Mouse Slc30a8 Gene Encoding Zinc Transporter-8 Results in Impaired Insulin Secretion” Biochemical Journal (2009) 421 pp371-376. doi.org/10.1042/BJ20090530
Christopher J. Easley, Richard K.P. Benninger, Jesse H. Shaver, W. Steven Head, David W. Piston “Rapid and inexpensive fabrication of polymeric microfluidic devices via toner transfer masking” Lab on a Chip (2009) 9 pp1119-1127. doi.org/10.1039/b816575k
Subhadra C. Gunawardana, Richard K.P. Benninger, David W. Piston “Subcutaneous transplantation of embryonic pancreas for correction of type 1 diabetes” American Journal of Physiology- Endocrinology and Metabolism (2009) 296 E323-332. doi.org/10.1152/ajpendo.90544.2008
Richard K.P. Benninger, Bruno Vanherberghen, Stephen Young, Sabrina Tanner, Fiona F. Culley, Tim Schnyder, Mark A.A. Neil, Daniel Wüstner, Paul M.W. French, Daniel M. Davis, Björn Önfelt “Live cell linear dichroism imaging reveals extensive membrane ruffling within the docking structure of Natural Killer cell immune synapses” Biophysical Journal- Biophysical Letters (2009) 96 L13-15. doi.org/10.1016/j.bpj.2008.10.005
David W. Piston, Gert-Jan Kremers, Richard K.P. Benninger, and Michael W. Davidson “Photoactivation in Fluorescence Microscopy” Microscopy Today (2009) 17 pp8-13. doi.org/10.1017/S1551929509000194
Richard K.P. Benninger, David W Piston. “Recent Advances in Single-photon-counting Detection Technology in Fluorescence Microscopy” Laser Focus World. (2009) June: pp59-63.
Richard K.P. Benninger, William J. Ashby, Elisabeth A. Ring, David W. Piston “A single-photon counting detector for increased sensitivity in two-photon laser scanning microscopy” Optics Letters (2008) 33: pp2895-7.
doi.org/10.1364/OL.33.002895
Richard K.P. Benninger, Min Zhang, W. Steven Head, Leslie S Satin, David W. Piston “Gap Junction Coupling and Calcium Waves in the Pancreatic Islet” Biophysical Journal (2008) 95: pp5048- 5061.
doi.org/10.1529/biophysj.108.140863
Richard K.P. Benninger*, Shu Mao*, Yuling Yan, Chutima Petchprayoon, David Jackson, Chistopher J. Easley, David W. Piston, Gerard Marriott “Optical lock-in detection of fluorescence resonance energy transfer using synthetic and genetically-encoded optical switches” Biophysical Journal (2008) 94: pp4515-24. (* Equal contributors).
doi.org/10.1529/biophysj.107.124859
Richard K.P. Benninger, Mingming Hao, David W. Piston. “Multi-photon Excitation Imaging of Dynamic Processes in Living Cells and Tissues” Reviews of Physiology, Biochemistry and Pharmacology (2008) 160: pp71-92. doi.org/10.1007/112_2008_801
Sunil Kumar, Christopher Dunsby, Pieter A.A. DeBeule, Dylan M. Owen, U Anand, Peter M.P. Lanigan, Richard K.P. Benninger, Daniel M. Davis, Mark A.A. Neil, Praveen Anand, Cristopher Benham, Alan Naylor, Paul M.W. French. “Multifocal multiphoton excitation and time correlated single photon counting detection for 3-D fluorescence lifetime imaging” Optics Express. (2007) 15: pp12548-12561. doi.org/10.1364/OE.15.012548
Richard K.P. Benninger, Oliver Hoffman, Björn Önfelt, Ian Munro, Christopher Dunsby, Daniel M. Davis, Mark A.A. Neil, Paul M.W. French, Andrew J. deMello. “Fluorescence Lifetime Imaging of Dye: DNA Interactions within Continuous Flow Microfluidic Systems” Angewandte Chemie International Edition (English). (2007) 46: pp2228-2231. doi.org/10.1002/anie.200604112
Pieter DeBeule, Dylan M. Owen, Hugh B. Manning, Clifford B. Talbot, Jose Requejo-Isidro, Christopher Dunsby, James McGinty, Richard K.P. Benninger, Daniel Elson, Ian Munro, M. John Lever, Pravene Anand, Mark A.A. Neil, Paul M.W. French. “Rapid Hyperspectral Fluorescence Lifetime Imaging” Microscopy Research Techniques (2007) 70: pp481-484. doi.org/10.1002/jemt.20434
Björn Önfelt, Shlomo Nedvetski, Richard K.P. Benninger, Mark A Perbhoo, Stefanie Sowinski, Alistair N. Hume, Miguel C. Seabra, Mark A.A. Neil, Paul M.W. French, Daniel M. Davis. “Structurally Distinct Membrane Nanotubes between Human Macrophages Support Long-Distance Vesicular Traffic or Surfing of Bacteria” Journal Immunology (2006) 177: pp8476-83. doi.org/10.4049/jimmunol.177.12.8476
Richard K.P. Benninger, Yasemin Koç, Oliver Hoffman, Jose Requejo-Isidro, Mark A.A. Neil, Paul M.W. French, Andrew J. deMello. “Quantitative 3D Mapping of Fluidic Temperatures within Microchannel Networks Using Fluorescence Lifetime Imaging” Analytical. Chemistry (2006) 78: pp2272-2278. doi.org/10.1021/ac051990f
Richard K.P. Benninger, Oliver Hoffman, James McGinty, Jose Requejo-Isidro, Ian Munro, Mark A.A. Neil, Andrew J. deMello, Paul M.W. French. “Time-resolved fluorescence imaging of solvent interactions in microfluidic devices” Optics Express. (2006) 13: pp6275-6285. doi.org/10.1364/OPEX.13.006275
Richard K.P. Benninger, Björn Önfelt, Mark A.A. Neil, Daniel M. Davis, Paul M.W. French. “Fluorescence Imaging of Two-Photon Linear Dichroism: Cholesterol Depletion disrupts Molecular Orientation in Cell Membranes.” Biophysical Journal (2005) 88: pp609-622. doi.org/10.1529/biophysj.104.050096
Daniel Elson, Jose Requejo-Isidro, Ian Munro, Fred Reavell, Jan Siegel, Klaus Suhling, Paul Tadrous, Richard Benninger, Peter Lanigan, James McGinty, Clifford Talbot, Bebhinn Treanor, Stephen Webb, Anne Sandison, Andrew Wallace, Daniel Davis, John Lever, Mark Neil, David Phillips, Gordon Stamp, Paul French. “A Perspective: Time-domain fluorescence lifetime imaging applied to biological tissue.” Photochemical Photobiological Sciences (2004) 3: pp795–801. doi.org/10.1039/B316456J