CURRENT FOCUS OF THE INSTITUTEMETABOLISM-SKELETAL MUSCLE-DIABETES(Bhanu P. Jena, Lars Larsson, Suzan Arslanturk)Cell Secretion
Secretion is a fundamental process through which cells communicate with their environment and exchange information in a multicellular context to reach homeostasis and sustain life. Secretion is a highly regulated cellular process in all living organisms, from yeast to cells in humans. Cellular cargo such as neurotransmitters in neurons, insulin in beta cells of the endocrine pancreas or digestive enzymes in the exocrine pancreas, are all packaged and stored in membrane-bound secretory vesicles that dock and fuse at the cell plasma membrane to release their contents during secretion. Cup-shaped lipoprotein structure at the cell plasma membrane called porosomes are involved in the transient docking, fusion and content release of secretory vesicles, with great precision at the cell plasma membrane during secretion. Although the nanoscale structure and composition of the porosome is established, understanding its atomic structure remains, and will be investigated (porosome-mediated secretion).Metabolism and Diabetes
Metabolic syndrome is a cluster of conditions that occur together, including obesity, type 2 diabetes, increased risk of cardiovascular disease and fatty liver disease. Both genetic and environmental factors contribute to the development of metabolic syndrome, as does aging and the microbiome. At a molecular level, these are all associated with insulin resistance, and the first site of insulin resistance in type 2 diabetes is at the level of skeletal muscle. Research in this area includes understanding the molecular basis of insulin action in skeletal muscle and other tissues, such as liver and fat, and how this is altered in insulin resistant states. Studies include animal and cellular models of disease with the emphasis of defining the fundamental defects underlying these disorders. The effects of exercise on insulin resistance and the impact of insulin resistance and diabetes on the brain and increased risk of Alzheimer’s Disease will also be investigated.Skeletal Muscle Cell Atlas
A large body of work demonstrates that with aging or prolonged periods of sedentary state, a major detriment to the physiology is accelerated wasting of skeletal muscles and loss of function. While muscle cells have been studied for over four centuries, much remains to be understood about how these cells precisely tune their behaviors in a tissue context to potentiate the proper function of the organism. In humans and most mammalian species, skeletal muscles composed of skeletal muscle cells constitute nearly 40% of body mass and under neuronal control among others, serve as major hubs of metabolism due to their role in locomotion. Thus, a prime candidate for modern systems biology approaches to understanding contextualized cell behavior is the skeletal muscle and its neuroendocrine control. A molecular and systems level understanding of the skeletal muscle cell structure and dynamics and the biological network that directs their activities is paramount to elucidating two of the most fundamental life processes: metabolism and movement.INFECTIOUS DISEASESMitigating Infection with Enveloped Viruses (HIV, Coronavirus and others)(Bhanu P. Jena, Octavian Bucur)
MMI is collaborating on a formulation to mitigate infection by enveloped viruses, such as HIV and Coronavirus (Covid-19). The active constituent used in this formulation is a U.S. Food and Drug Administration (FDA) approved product. The proposed effective dose of the active constituent in the formulation to be administered, falls within the FDA-specified guidelines. The proposed route of administration of the formulation is dermal, nasal and pulmonary using a soft mist inhaler to deliver a precise dose. The formulation has the additional potential of mitigating bacterial and fungal infections. A randomized double-blind placebo-controlled clinical study on 1,000 front-line health care workers is planned.Overcoming bacterial resistance to antibiotic and the spread of infectious diseases(Bhanu P. Jena)
Rapid urbanization resulting in increased population density combined with socioeconomic disparities is threatening global health. According to the World Health Organization, the major health challenges facing cities today are from infectious diseases like hepatitis, TB, Pneumonia and antibiotic resistance. Utilizing the inexpensive, precision nanoscale thermometry approach developed at MMI, the presence of antibiotic resistant bacteria can be detected and the precise antibiotics required for treatment determined.DIAGNOSTIC AND MOLECULAR PATHOLOGYDevelopment of a precision, rapid and inexpensive ‘Cancer Detection Tool-kit’ and non-invasive liquid biopsy approaches(Bhanu P. Jena, Victor Velculescu, Octavian Bucur)
MMI is involved in the development of a precision, rapid and inexpensive nanothermometry approach for early cancer detection, diagnosis and therapy. The published and patented study on the molecular motor myosin and on intact muscles demonstrate that molecular and cellular calorimetry at the single molecular level and in the mK scale is able to differentiate between normal and cancerous cells, based on the principle that as a result of increased cellular glycolytic metabolism and higher metabolic rate, cancer cells exhibit higher temperatures, hence their detection as a consequence in loss of fluorescence of nanometer scale quantum dot thermometers.
MMI will also pursue non-invasive liquid biopsy approaches for early detection and monitoring of cancer patients.Rapid and inexpensive approach of ‘Differential Expansion Microscopy’ combined with Machine Learning in ‘Diagnostic Pathology’(Bhanu P. Jena, Yougxin Zhao, Douglas J. Taatjes, Suzan Arslanturk, Octavian Bucur)
Expensive and time-consuming approaches of immunoelectron microscopy of biopsy tissues continues to serve as the gold-standard for diagnostic pathology. The recent development of differential expansion microscopy (DiExM) combined with machine learning capable of up to 8-fold lateral expansion and over 500-fold volumetric expansion of biological specimens, for their morphological examination at approximately 20 nm lateral resolution using an ordinary diffraction limited optical microscope, is a boon to diagnostic pathology. An automated tool-kit, which incorporates digital pathology and machine learning, is being developed for commercialization and use.Identification & Treatment of Immobilization-Induced Myopathy(Bhanu P. Jena, Lars Larsson)
Changes in muscle efficiency due to inactivity in long space flights and in the intensive care unit, can be precisely monitored and managed more effectively using nanothermometry.Understanding cellular pH regulation and gas transport(Walter F. Boron)
Focuses on three areas: the molecular physiology of the Na -coupled HCO3− transporters, molecular CO2/HCO–3 sensors and gas channels.
The development of new tools and technologies in imaging, proteomics, genomics, mathematical and computational approaches such as machine learning, provide for the first time the opportunity to understand the skeletal muscle cell and it’s neuronal and hormonal control at the systems level. The initial focus will be to establish a “Human Skeletal Muscle Cell Atlas” which will provide a global reference map and greater understanding of its structure and function. A consortium of independent investigators in the field will pool their intellectual and technical resources currently available through separate ongoing collaborations and utilize them to understand metabolism and movement in human skeletal muscle at the molecular scale and at the systems level. The institute with its multi-disciplinary approach, will serve as a powerful platform to train the next generation of investigators and educators and to generate public awareness on the beneficial impact of the proposed multi-disciplinary research to society.SELECTED PUBLICATIONS BY MMI MEMBERSSuzan Arslanturk
Walter F. Boron
- Pernal SP, Liyanaarachchi A, Gatti DL, Formosa B, Pulvender R, Kuhn ER, Ramos R, Naik AR, George K, Arslanturk S, Taatjes DJ, Jena BP. ‘Nanoscale imaging using differential expansion microscopy’, Histochem. & Cell Biol. (2020)
- Jena BP, Gatti DL, Arslanturk S, Pernal S, Taatjes DJ. Human Skeletal Muscle Cell Atlas: Unraveling Cellular Secrets Utilizing ‘Muscle-on-a-Chip’, Differential Expansion Microscopy, Mass Spectrometry, Nanothermometry and Machine Learning. Micron (2018) https://doi.org/10.1016/j.micron.2018.11.002
- Pernal SP, Liyanaarachchi A, Gatti DL, Formosa B, Pulvender R, Kuhn ER, Ramos R, Naik AR, George K, Arslanturk S, Taatjes DJ, Jena BP. Differential expansion microscopy. bioRxiv. (2019) July 11; doi: https://doi.org/10.1101/699579
- Gatti DL, Arslanturk S, Lal S, Jena BP. Deep learning strategies for differential expansion microscopy. bioRxiv. (2019) August 22; doi: https://doi.org/10.1101/743682
Won Jin Cho
- Boron WF, Weer PD. Intracellular pH transients in squid giant axons caused by CO2, NH3, and metabolic inhibitors. J. Gen. Physiol. (1976) 67:91–112. -First clear demonstration of the dynamic, active regulation of intracellular pH (pHi). Introduction of the now-widely-used “ammonium prepulse technique” for acid loading cells. First temporal, mathematical model of pHi regulation.
- Boron WF, Weer PD. Active proton transport stimulated by CO2/HCO3–, blocked by cyanide. Nature (1976) 259:240–241. -First demonstration that a pHi-regulating mechanism (that of the squid axon) imports HCO3−.
- Russell JM, Boron WF. Role of chloride transport in regulation of intracellular pH. Nature (1976) 264:73–74. -First demonstration that a pHi-regulating mechanism (that of the squid axon) exports Cl−.
- Boron WF. Intracellular pH transients in giant barnacle muscle fibers. Am. J. Physiol. (1977) 233:C61–C73. -First determination of pHi dependence of intracellular buffering power, which would later prove crucial for first characterization of the pHi dependence of a pHi-regulating mechanism.
- Boron WF, McCormick WC, Roos A. pH regulation in barnacle muscle fibers: dependence on intracellular and extracellular pH. Am. J. Physiol. (1979) 237:C185–C193. -First determination of pHi-dependence of the rate of “acid extrusion” by a pHi-regulating mechanism. Critical insights were utilization of pHi-dependence of buffering power, and correction for background acid-loading processes.
- Boron WF, Boulpaep EL. Intracellular pH regulation in the renal proximal tubule of the salamander: basolateral HCO3– transport. J. Gen. Physiol. (1983) 81:53–94. -Discovery and full characterization of the electrogenic Na/HCO3 cotransporter (later cloned by Boron Lab, and now known as NBCe1).
- Boron WF, Russell JM. Stoichiometry and ion dependencies of the intracellular-pH-regulating mechanism in squid giant axons. J. Gen. Physiol. (1983) 81:373–399. -First full characterization of the Na+-driven Cl-HCO3 exchanger (later cloned by Boron Lab, and now known as NDCBE). -First evidence that the extracellular substrate may be the NaCO3– ion pair.
- Siebens AW, Boron WF. Depolarization-induced alkalinization in proximal tubules. I. Characteristics and dependence on Na+. Am. J. Physiol. (1989) 256:F342–F353. -Discovery of depolarization-induced intracellular alkalinization (DIA). In nervous system, depolarization of astrocytes causes NBCe1 to raise pHi but also lower pH surrounding neurons, preventing runaway excitability.
- Ganz MB, Boyarsky G, Sterzel RB, Boron WF. Arginine vasopressin enhances pHi regulation in the presence of HCO3– by stimulating three acid-base transport systems. Nature (1989) 337:648–651. -Debunked then-current notion (based on experiments in absence of CO2/HCO3−) that growth factors trigger mitogenesis by raising pHi. This paper shows that, in presence of CO2/HCO3−, a mitogen actually lowers pHi.
- Kaplan DL, Boron WF. Long-term expression of c-H-ras stimulates Na-H and Na+-dependent Cl-HCO3 exchange in NIH-3T3 fibroblasts. J. Biol. Chem. (1994) 269:4116–4124. -Demonstration that an oncogene raises pHi by stimulating acid-extrusion mechanisms. This effect presumably allows cancer cells to survive in the acidic environment that they create by exporting lactic acid (Warburg effect).
- Zhao J, Hogan EM, Bevensee MO, Boron WF. Out-of-equilibrium CO2/HCO3− solutions and their use in characterizing a new K/HCO3 cotransporter. Nature (1995) 374:636–639. -Invention of out-of-equilibrium (OOE) CO2/HCO3− solutions, which permits one to change—one at a time—[CO2], [HCO3−], and pH. Enabled discovery that RPTPg is a dual CO2/HCO3− sensor. -Editorial on Zhao et al: Thomas RC. Bicarbonate briefly CO2-free. Nature(1995) 374: 597–598.
- Romero MF, Hediger MA, Boulpaep EL, Boron WF. Expression cloning of the renal electrogenic Na/HCO3 cotransporter. Nature (1997) 387:409–413. -Cloning of the cDNA encoding the first NBC, which defined the signature motif of the SLC4 family and led to the discovery and cloning of the 6 other family members.
- Gunshin H, Mackenzie B, Berger UV, Gunshin Y, Romero MF, Boron WF, Nussberger S, Gollan JL, HedigerMA. Cloning and characterization of a proton-coupled mammalian metal ion transporter. Nature (1997) 388: 482–488. -Cloning of the cDNA encoding the metal ion transporter DCT1 (now known as DMT1 or SLC11A2) and demonstration of its coupling to the transmembrane H+ gradient.
- Choi I, Aalkjær C, Boulpaep EL, Boron WF. An electroneutral sodium/bicarbonate cotransporter NBCn1 and associated sodium channel. Nature (2000) 405:571–575. -Cloning of cDNA’s encoding 3 variants of NBCn1 (SLC4A7), and characterization not only of electroneutral Na/HCO3 activity but intrinsic Na+-channel activity.
- Grichtchenko II, Choi I, Bray-Ward P, Russell JM, Choi I, Boron WF. Cloning, characterization and chromosomal mapping of a human electroneutral Na+-driven Cl-HCO3 exchanger. J. Biol. Chem. (2001) 276:8358–8363. -Cloning of cDNA encoding the Na+-driven Cl-HCO3 exchanger (NDCBE or SLC4A8).
- Zhou Y, Zhao J, Bouyer P, Boron WF. Evidence from renal proximal tubules that HCO3− and solute reabsorption are acutely regulated not by pH but by basolateral HCO3− and CO2. Proc. Natl. Acad. Sci. USA (2005) 102:3875–3880. -Demonstration, using OOE solutions, that renal proximal tubule (responsible for >80% of HCO3− transport in kidney) responds to changes in extracellular CO2 and HCO3− but not to pH. Led to discovery that RPTPg is the sensor.
- Parker MD, Musa-Aziz R, Rojas JD, Choi I, Daly CD, Boron WF. Characterization of human SLC4A10 as an electroneutral Na/HCO3 cotransporter (NBCn2) with Cl– self-exchange activity. J. Biol. Chem. (2008) 283:12777–12788. -Demonstration, using OOE solutions, that renal proximal tubule (responsible for >80% of HCO3− transport in kidney) responds to changes in extracellular CO2 and HCO3− but not to pH. Led to discovery that RPTPg is the sensor.
- Somersalo E, Occhipinti R, Boron WF, Calvetti D. A reaction-diffusion model of CO2 influx into an oocyte. J. Theor. Biol. (2012) 309:185–203. -First reaction-diffusion model (3 dimensional, time dependent) of CO2 into/out of a cell. Model accommodates carbonic anhydrases and an indefinite number of buffers. Led to model incorporating H+/HCO3−/CO3= transporters.
- Occhipinti R, Musa-Aziz R, Boron WF. Evidence from mathematical modeling that carbonic anhydrase II and IV enhance CO2 fluxes across Xenopus oocytes plasma membranes. Am. J. Physiol. Cell Physiol. (2014) 307: C841–C858. -Quantitative accounting for how carbonic anhydrases and buffers enhance CO2 fluxes across membranes. Explanation of how CAs on opposite sides of membrane have not additive, but multiplicative effects. -Editorial on 3 back-to-back papers: E Delpire: Am. J. Physiol. Cell Physiol. (2014) 307:C788-790.
- Zhou Y, Skelton LA, Xu L, Chandler PM, Berthiaume JM, Boron WF. Role of receptor protein tyrosine phosphatase g in sensing extracellular CO2 and HCO3−. J. Am. Soc. Nephrol. (2016) 27:2616–2621. -Demonstration, based on OOE solutions, that RPTPg senses extracellular molecular HCO3− and molecular CO2. -Editorial on Zhou et al: Soleimani M. Receptor protein tyrosine phosphatase g, CO2 sensing in the proximal tubule and acid base homeostasis. J. Am. Soc. Nephrol. (2016) 27:2253–2545.
- Cho WJ, Kim EJ, Lee SJ, Kim HD, Shin HJ, Lim WJ. Involvement of SPARC in in Vitro Differentiation of Skeletal Myoblasts. Biochem. Biophysic. Res. Comm. (2000) 271:630-634.
- Cho WJ, Drescher MJ, Hatfield JS, Bessert DA, Skoff RP, Drescher DG. Hyperpolarization-activated, cyclic AMP-gated, HCN1-like cation channel: The primary, full-length HCN isoform expressed in a saccular Hair-cell layer. Neuroscience (2003) 118:525-534.
- Abu-Hamdah R, Cho WJ, Cho SJ, Jeremic A, Kelly M, Ilie AE, Jena BP. Regulation of the water channel aquaporin-1: isolation and reconstitution of the regulatory complex. Cell Biol. Int. (2004) 28:7-17
- Cho WJ, Jeremic A, Rognlien KT, Zhvania MG, Lazrishvili I, Tamar B, Jena BP. Structure, isolation, composition and reconstitution of the neuronal fusion pore. Cell Biol. Int. (2004) 28:699-708.
- Kelly ML, Cho WJ, Jeremic A, Abu-Hamdah R, Jena BP. Vesicle swelling regulates content expulsion during secretion. Cell Biol. Int. (2005)28: 709-716.
- Cho WJ, Jeremic A, Jena BP. Direct interaction between SNAP-23 and L-type calcium channel. J. Cell Mol. Med. (2005) 9:380-386.
- Cho WJ, Jeremic A, Jena BP. Size of supramolecular SNARE complex: membrane- directed self-assembly. J. Am. Chem. Soc. (2005) 127:10156-10157.
- Cho WJ, Jeremic A, Jena BP. Involvement of water channels in synaptic vesicle swelling. Exp. Biol. Med. (2005) 230:674-680.
- Jeremic A, Quinn AS, Cho WJ, Taatjes DJ, Jena, B.P. Energy-dependent disassembly of self-assembled SNARE complex: observation at nanometer resolution using atomic force microscopy. J. Am. Chem. Soc. (2006) 128:26-27.
- Abu-Hamdah R, Cho WJ, Hörber JK, Jena BP. Secretory vesicles in live cells are not free-floating but tethered to filamentous structures: a study using photonic force microscopy. Ultramicroscopy (2006) 106: 670-673.
- Jeremic A, Cho WJ, Jena BP. Cholesterol is critical to the integrity of neuronal porosome/fusion pore. Ultramicroscopy. (2006) 106:674-677.
- Cho WJ, Jeremic A, Jin H, Ren G, Jena BP. Neuronal fusion pore assembly requires membrane cholesterol. Cell Biol. Int. (2007) 31:1301-1308.
- Cho WJ, Jena BP. NSF is a Right-Handed Molecular Motor. J. Biomed. Nanotech. (2007) 3:209-211.
- Cook JD, Cho WJ, Stemmler TL, Jena BP. Circular dichroism (CD) spectroscopy of the assembly and disassembly of SNAREs: the proteins involved in membrane fusion in cells. Chem. Phys. Lett. (2008) 462:6-9.
- Cho WJ, Ren G, Jena BP. EM 3D contour maps provide protein assembly at the nanoscale within the neuronal porosome complex. J. Microscopy (2008) 232:106-111.
- Lee JS, Cho WJ, Jeftinija K, Jeftinija S, Jena BP. Porosome in astrocytes. J. Cell Mol. Med. (2009) 13:365-372.
- Cho WJ, Ren G, Lee JS, Jeftinija K, Jeftinija S, Jena BP. Nanoscale three-dimensional contour map of protein assembly within the astrocyte porosome complex. Cell Biol. Int. (2009)33: 224-229.
- Shin L, Basi N, Lee JS, Cho WJ, Chen Z, Abu-Hamdah R, Oupicky D, Jena BP. Involvement of vH+-ATPase in synaptic vesicle swelling. J. Neurosci. Res. (2010) 88(1):95-101.
- Cho WJ, Shin L, Ren G, Jena BP. Structure of membrane-associated neuronal SNARE complex: Implication in neurotransmitter release.J. Cell Mol. Med. (2009) 13:4161-4165.
- Cho WJ, Trikha S, Jeremic AM. Cholesterol regulates assembly of human islet amyloid polypeptide on model membranes. J. Mole. Biol. (2009) 393:765-775.
- Shin L, Cho WJ, Cook J, Stemmler T, Jena, B. P. Membrane Lipids Influence Protein Complex Assembly-Disassembly. J. Am. Chem. Soc. (2010) 132:5596-5597.
- Cho WJ, Lee JS, Jena BP. Conformation states of the neuronal porosome complex. Cell Biol. Int. (2010) 34:1129-1132 9.
- Drescher MJ, Cho WJ, Folbe AJ, Selvakumar D, Kewson DT, Abu-Hamdan MD, Oh CK, Ramakrishnan NA, Hatfield JS, Khan KM, Anne S, Harpool EC, Drescher DG. An adenylyl cyclase signaling pathway predicts direct dopaminergic input to vestibular hair cells. Neuroscience (2010) 171:1054-1074.
- Cho WJ, Lee JS, Ren G, Zhang L, Shin L, Manke CW, Potoff JJ, Kotaria N, Zhvania MG, Jena BP. Membrane-directed molecular assembly of the neuronal SNARE complex. J. Cell Mol. Med. (2011) 15:31-37.
- Chen ZH, Lee JS, Shin L, Cho WJ, Jena BP. Involvement of β-adrenergic receptor in synaptic vesicle swelling and implication in neurotransmitter release. J. Cell Mol. Med. (2011) 15:572-576.
- Drescher DG, Cho WJ, Drescher MJ. Identification of the porosome complex in the hair cell. Cell Biol. Int. Rep. (2011) 18(1). 331-341.
- Wang S, Lee JS, Bishop N, Jeremic A, Cho WJ, Chen X, Mao G, Taatjes DJ, Jena BP. 3D organization and function of the cell: Golgi budding and vesicle biogenesis to docking at the porosome complex. Histochem Cell Biol. (2012) 137(6):703-718.
- Lee JS, Jeremic A, Shin L, Cho WJ, Chen X, Jena BP. Neuronal porosome proteome: Molecular dynamics and architecture. J. of Proteomics (2012) 75:3952-3962.
- Lee JS, Hou X, Bishop N, Wang S, Flack A, Cho WJ, Chen X, Mao G, Taatjes DJ, Sun F, Zhang K, Jena BP. Aquaporin-assisted and ER-mediated mitochondrial fission: A hypothesis. Micron (2013) 47:50-58.
- Kovari LC, Brunzelle JS, Lewis KT, Cho WJ, Lee JS, Taatjes DJ, Sun F, Zhang K, Jena BP. X-ray solution structure of the native neuronal porosome-synapticvesicle complex: Implication in neurotransmitter release. Micron (2014) 47:50-58.
- Mainetti LE, Zhe X, Diedrich J, Saliganan AD, Cho WJ, Cher ML, Heath E, Fridman R, Kim HRC, Bonfil DR. Bone-induced c-kit expression in prostate cancer: A driver of intraosseous tumor growth. Int. J. Cancer (2015) 136:11-20.
- Cho WJ, Oliveira DSM, Najy AJ, Mainetti LE, Aoun HD, Cher ML, Heath E, Kim HRC, Bonfil D. Gene expression analysis of bone metastasis and circulating tumor cells from metastatic castrate‑resistant prostate cancer patients. J. Translational Medicine (2016) 14:72-84.
- Kessel D, Cho WJ, Rakowski J, Kim HE, Kim HRC. Effects of HPV Status on Responsiveness to Ionizing Radiation vs Photodynamic Therapy in Head and Neck Cancer Cell lines. Photochem. Photobio. (2020) 96:652-657.
- Kessel D, Cho WJ, Rakowski J, Kim HE, Kim HRC. Characteristics of an Impaired PDT Response. Photochem. Photobio. (2021) 97:837-840.
- Cho WJ, Kessel D, Rakowski J, Loughery B, Najy AJ, Pham T, Kim S, Kwon YT, Kato I, Kim HE, Kim HRC. Photodynamic Therapy as a Potent Radiosensitizer in Head and Neck Squamous Cell Carcinoma. Cancers (2021) 13(6):1193-1206.
- Lee SH, Cho WJ, Najy AJ, Saliganan AD, Pham T, Rakowski J, Loughery B, Ji CH, Skar W, Kim S, Kato I, Kim HE, Kwon YT, Kim HRC. p62/SQSTM1-induced caspase-8 aggresomes are essential for ionizing radiation-mediated apoptosis. Cell Death & Disease (2021) 12:997-1007.
- Jena BP, Gatti DL, Arslanturk S, Pernal S, Taatjes DJ. Human skeletal muscle cell atlas: Unraveling cellular secrets utilizing 'muscle-on-a-chip', differential expansion microscopy, mass spectrometry, nanothermometry and machine learning. Micron (2019) 117, 55-59.
- Zhu F, Gatti DL, Yang KH. Nodal versus total axonal strain and the role of cholesterol in traumatic brain injury. J. Neurotrauma (2016) 33, 859-870.
- Ackerman SH, Tillier ER, Gatti DL. Accurate simulation and detection of coevolution signals in multiple sequence alignments. PLoS One. (2012) 7, Issue 10 | e47108.
- Acin-Perez R, Gatti DL, Bai Y, Manfredi G. Protein phosphorylation and prevention of cytochrome oxidase inhibition by ATP: coupled mechanisms of energy metabolism regulation. Cell Metab. (2011) 13, 712-719.
- Ludlam A, Brunzelle J, Pribyl T, Xu X, Gatti DL, Ackerman SH. Chaperones of F1-ATPase. J. Biol. Chem. (2009) 284, 17138-17146.
- Valkov N, Das A, Tucker NR, Li G, Salvador AM, Chaffin MD, Pereira De Oliveira Junior G, Kur I, Gokulnath P, Ziegler O, Yeri A, Lu S, Khamesra A, Xiao C, Rodosthenous R, Srinivasan S, Toxavidis V, Tigges J, Laurent LC, Momma S, Kitchen R, Ellinor P, Ghiran I, Das S. SnRNA sequencing defines signaling by RBC-derived extracellular vesicles in the murine heart. Life Sci Alliance. (2021) 12; 4(12). PMID: 34663679.
- Thompson L, Pinckney B, Lu S, Gregory M, Tigges J, Ghiran I. Quantification of Cellular Densities and Antigenic Properties using Magnetic Levitation. J. Vis. Exp. (2021) 05 17; (171). PMID: 34057455.
- Oliveira-Jr GP, Barbosa RH, Thompson L, Pinckney B, Murphy-Thornley M, Lu S, Jones J, Hansen CH, Tigges J, Wong WP, Ghiran IC. Electrophoretic mobility shift as a molecular beacon-based readout for miRNA detection. Biosens Bioelectron (2021) 189:113307. PMID: 34062334.
- Saha K, Sontheimer EJ, Brooks PJ, Dwinell MR, Gersbach CA, Liu DR, Murray SA, Tsai SQ, Wilson RC, Anderson DG, Asokan A, Banfield JF, Bankiewicz KS, Bao G, Bulte JWM, Bursac N, Campbell JM, Carlson DF, Chaikof EL, Chen ZY, Cheng RH, Clark KJ, Curiel DT, Dahlman JE, Deverman BE, Dickinson ME, Doudna JA, Ekker SC, Emborg ME, Feng G, Freedman BS, Gamm DM, Gao G, Ghiran IC, Glazer PM, Gong S, Heaney JD, Hennebold JD, Hinson JT, Khvorova A, Kiani S, Lagor WR, Lam KS, Leong KW, Levine JE, Lewis JA, Lutz CM, Ly DH, Maragh S, McCray PB, McDevitt TC, Mirochnitchenko O, Morizane R, Murthy N, Prather RS, Ronald JA, Roy S, Roy S, Sabbisetti V, Saltzman WM, Santangelo PJ, Segal DJ, Shimoyama M, Skala MC, Tarantal AF, Tilton JC, Truskey GA, Vandsburger M, Watts JK, Wells KD, Wolfe SA, Xu Q, Xue W, Yi G, Zhou J. The NIH Somatic Cell Genome Editing program. Nature (2021) 04; 592(7853):195-204.
- Marie AL, Ray S, Lu S, Jones J, Ghiran I, Ivanov AR. High-Sensitivity Glycan Profiling of Blood-Derived Immunoglobulin G, Plasma, and Extracellular Vesicle Isolates with Capillary Zone Electrophoresis-Mass Spectrometry. Anal. Chem. (2021) 93(4):1991-2002.
- Sharda AV, Barr AM, Harrison JA, Wilkie AR, Fang C, Mendez LM, Ghiran IC, Italiano JE, Flaumenhaft R. VWF maturation and release are controlled by 2 regulators of Weibel-Palade body biogenesis: exocyst and BLOC-2. Blood (2020) 136(24):2824-2837.
- Li J, Salvador AM, Li G, Valkov N, Ziegler O, Yeri A, Yang Xiao C, Meechoovet B, Alsop E, Rodosthenous RS, Kundu P, Huan T, Levy D, Tigges J, Pico AR, Ghiran I, Silverman MG, Meng X, Kitchen R, Xu J, Van Keuren-Jensen K, Shah R, Xiao J, Das S. Mir-30d Regulates Cardiac Remodeling by Intracellular and Paracrine Signaling. Circ. Res. (2021) 128(1):e1-e23. PMID: 33092465.
- Nelson BC, Maragh S, Ghiran IC, Jones JC, DeRose PC, Elsheikh E, Vreeland WN, Wang L. Measurement and standardization challenges for extracellular vesicle therapeutic delivery vectors. Nanomedicine (Lond). (2020) 15(22):2149-2170.
- Rodosthenous RS, Hutchins E, Reiman R, Yeri AS, Srinivasan S, Whitsett TG, Ghiran I, Silverman MG, Laurent LC, Van Keuren-Jensen K, Das S. Profiling Extracellular Long RNA Transcriptome in Human Plasma and Extracellular Vesicles for Biomarker Discovery. iScience (2020) 23(6):101182.
- Welsh JA, Van Der Pol E, Arkesteijn GJA, Bremer M, Brisson A, Coumans F, Dignat-George F, Duggan E, Ghiran I, Giebel B, Görgens A, Hendrix A, Lacroix R, Lannigan J, Libregts SFWM, Lozano-Andrés E, Morales-Kastresana A, Robert S, De Rond L, Tertel T, Tigges J, De Wever O, Yan X, Nieuwland R, Wauben MHM, Nolan JP, Jones JC. MIFlowCyt-EV: a framework for standardized reporting of extracellular vesicle flow cytometry experiments. J. Extracell. Vesicles (2020) 9(1):1713526. PMID: 32128070.
- Lee J, Vernet A, Redfield K, Lu S, Ghiran IC, Way JC, Silver PA. Rational Design of a Bifunctional AND-Gate Ligand To Modulate Cell-Cell Interactions. ACS Synth. Biol. (2020) 9(2):191-197. PMID: 31834794.
- Oliveira GP, Zigon E, Rogers G, Davodian D, Lu S, Jovanovic-Talisman T, Jones J, Tigges J, Tyagi S, Ghiran IC. Detection of Extracellular Vesicle RNA Using Molecular Beacons. iScience (2020) 23(1):100782. PMID: 31958756.
- Morales-Kastresana A, Musich TA, Welsh JA, Telford W, Demberg T, Wood JCS, Bigos M, Ross CD, Kachynski A, Dean A, Felton EJ, Van Dyke J, Tigges J, Toxavidis V, Parks DR, Overton WR, Kesarwala AH, Freeman GJ, Rosner A, Perfetto SP, Pasquet L, Terabe M, McKinnon K, Kapoor V, Trepel JB, Puri A, Kobayashi H, Yung B, Chen X, Guion P, Choyke P, Knox SJ, Ghiran I, Robert-Guroff M, Berzofsky JA, Jones JC. High-fidelity detection and sorting of nanoscale vesicles in viral disease and cancer. J. Extracell. Vesicles (2019) 8(1):1597603. PMID: 31258878.
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Bhanu P. Jena
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- Jena BP. (2020) Cellular Nanomachines Natures Engineered Marvels. Springer Nature, ISBN: 9783030444952
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- Jeremic A, Kelly M, Cho SJ, Stromer MH, Jena BP. Reconstituted fusion pore. Biophys. Journal.(2003) 85: 2035-2043.
- Cho WJ, Jeremic A, Rognlien KT, Zhvania MG, Lazrishvili I, Tamar B, Jena BP. Structure, isolation, composition and reconstitution of the neuronal fusion pore. Cell Biol. Int. (2004) 28: 699-708.
- Cho WJ, Ren G, Jena BP. EM 3D contour maps provide protein assembly at the nanoscale within the neuronal porosome complex. J. of Microscopy. (2008) 232: 106-111.
- Lee JS, Jeremic A, Shin L, Cho WJ, Chen X, Jena BP. Neuronal porosome proteome: Molecular dynamics and architecture. J.l of Proteomics (2012) 75: 3952-3962.
- Kovari LC, Brunzelle JS, Lewis KT, Cho WJ, Lee JS, Taatjes DJ, Jena BP. X-ray solution structure of the native neuronal porosome-synaptic vesicle complex: Implication in neurotransmitter release. Micron (2014) 56: 37-43.
- Naik AR, Kulkarni SP, Lewis KT, Taatjes DJ, Jena BP. Functional reconstitution of the insulin-secreting porosome complex in live cells. Endocrinology (2015) en20151653. PMID 26523491 DOI: 10.1210/en.2015-1653
- Cho SJ, Kelly M, Rognlien KT, Cho JA, Hörber JK, Jena BP. SNAREs in opposing bilayers interact in a circular array to form conducting pores. Biophys. Journal. (2002) 83: 2522-2527.
- Cho WJ, Jeremic A, Jena BP. Size of supramolecular SNARE complex: membrane-directed self-assembly. J. Ameri. Chem. Society (2005) 127: 10156-10157.
- Jeremic A, Quinn AS, Cho WJ, Taatjes DJ, Jena BP. Energy-dependent disassembly of self-assembled SNARE complex: observation at nanometer resolution using atomic force microscopy. J. Ameri. Chem. Society (2006) 128: 26-27.
- Shin L, Cho WJ, Cook JD, Stemmler TL, Jena BP. Membrane lipids influence protein complex assembly-disassembly. J. Ameri. Chem. Society (2010) 132: 5596-5597.
- Jena BP, Schneider SW, Geibel JP, Webster P, Oberleithner H, Sritharan KC. G(i) regulation of secretory vesicle swelling examined by atomic force microscopy. Proc. Natl. Acad. Sci. USA. (1997) 94: 13317-13322.
- Cho SJ, Sattar AK, Jeong EH, Satchi M, Cho JA, Dash S, Mayes MS, Stromer MH, Jena BP. Aquaporin 1 regulates GTP-induced rapid gating of water in secretory vesicles. Proc. Natl. Acad. Sci. USA. (2002) 99: 4720-4724.
- Kelly ML, Cho WJ, Jeremic A, Abu-Hamdah R, Jena BP. Vesicle swelling regulates content expulsion during secretion. Cell Biol. Int. (2004) 28: 709-716.
- Jeremic A, Cho WJ & Jena BP. Involvement of water channels in synaptic vesicle swelling. Exp. Biol. Med. (Maywood, N.J.) (2005) 230: 674-680.
- Shin L, Basi N, Jeremic A, Lee JS, Cho WJ, Chen Z, Abu-Hamdah R, Oupicky D, Jena BP. Involvement of vH(+)-ATPase in synaptic vesicle swelling. J. Neurosci. Res. (2010) 88: 95-101.
Douglas J. Taatjes
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- Corpeno Kalamgi R Salah H, Gastaldello S, Martinez-Redondo V, Ruas J, Fury W, Bai Y, Gromada J, Sartori R, Guttridge DC, Sandri M, Larsson L. Mechano Signaling Pathways in an Experimental Intensive Care Unit Model. J. Physiol. (2016) 1;594(15):4371-4388.
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- Lee JS, Hou X, Bishop N, Wang S, Flack A, Cho WJ, Chen X, Mao G, Taatjes DJ, Sun F, Zhang K, Jena BP. Aquaporin-assisted and ER-mediated mitochondrial fission: A hypothesis. Micron (2013) 47:50-58.
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- Sritharan KC, Quinn AS, Taatjes DJ, Jena BP. Binding contribution between synaptic vesicle membrane and plasma membrane proteins in neurons: An AFM study. Cell Biol. Int. (1998) 22, 649-655.
- Jeremic A, Quinn AS, Cho WJ, Taatjes DJ, Jena BP. Energy-dependent disassembly of self-assembled SNARE complex: Observation at nanometer resolution using atomic force microscopy. J. Am. Chem. Soc. (2006) 128, 26-27.
- Pang Y, von Turkovich M, Wu H, Mitchell J, Mount S, Taatjes DJ, Cooper K. The binding of thyroid transcription factor 1 and hepatocyte paraffin 1 to mitochondrial proteins in hepatocytes: A molecular and immunoelectron microscopic investigation. Am. J. Clin. Path. (2006) 125, 722-726.
- Taatjes DJ, Wadsworth MP, Zaman AKMT, Schneider DJ, and Sobel BE. A novel dual staining method for identification of apoptotic cells reveals a modest apoptotic response in infarcted mouse myocardium. Histochem. Cell Biol. (2007) 128, 275-283.
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Mazia G. Zhvania
- A. Klimas, B. Gallagher, P. Wijesekara, S. Fekir, E. F. DiBernardo, Z. Cheng, D. Stolz, F. Cambi, S. Watkins, S. L. Brody, A. Horani, A. L. Barth, C. Moore, X. Ren, Y. Zhao. Magnify is a universal molecular anchoring strategy for expansion microscopy. Nature Biotechnology. Published 02 Jan. 2023.
- F. Han, S. Gu, A. Klimas, N. Zhao, Y. Zhao* (co-corresponding), S-C, Chen*. Three-dimensional nanofabrication via ultrafast laser patterning and kinetically regulated material assembly. Science (2022) 378, 6626.
- A. Abdelfattah, S. Ahuja, T. Akkin, S.R. Allu, D.A. Boas, J. Brake, E.M. Buckley, ..., Y. Zhao. Neurophotonic tools for microscopic measurements and manipulation: status report. Neurophotonics (2022) 9 (S1), 013001 [Review]
- L. Shi, A. Klimas, B. Gallagher, Z. Cheng, F. Fu, P. Wijesekara, Y. Miao, X. Ren, Y. Zhao* (co-corresponding author), W Min*. Super-resolution vibrational imaging using expansion stimulated Raman scattering microscopy. Advanced Science (2022_) 2200315.
- B. Gallagher, Y. Zhao. Expansion microscopy: A powerful nanoscale imaging tool for neuroscientists. Neurobiology of Disease (2021) DOI: 10.1016/j.nbd.2021.105362.
- A. Klimas, Y. Zhao. Expansion Microscopy: Toward Nanoscale Imaging of a Diverse Range of Biomolecules. ACS Nano. (2020) 14, 7, 7689–7695. DOI: 10.1021/acsnano.0c04374.
- O. Bucur, F. Fu, M. Calderon, G. H. Mylvaganam, N. L. Ly, J. Day, S. Watkin, B. D. Walker, E. S. Boyden*, Y. Zhao. Expansion Pathology: Conventional and Rapid Protocols for Nanoscale Imaging of Clinical Specimens. Nature Protocol (2020, 4) https://doi.org/10.1038/s41596-020-0300-1.
- B. Gallagher, Y. Zhao. Nanoscale Imaging of Synaptic Connections with Expansion Microscopy. Discoveries (2019) 7, e101 [Cover paper]
- S. Cheng, Y. Zhao. Nanoscale imaging of E. coli cells by expansion microscopy. Discoveries (2019) 7, e98 [Cover paper]
- A. Klimas, B. Gallagher, Y. Zhao. Basics of Expansion Microscopy. Current Protocols in Cytometry (2019) 91 (1), e67
- A. Klimas, O. Bucur, B. Njeri, Y. Zhao. Nanoscopic Imaging of Human Tissue Sections via Physical and Isotropic Expansion. J. Vis. Exp. 2019, e60195.
- Y. Zhao, W. Zhang, Y. Zhao, R.E. Campbell, D.J. Harrison. A single-phase flow microfluidic cell sorter for multiparameter screening to assist the directed evolution of Ca2+ sensors. Lab on a Chip (2019) (22), 3880-3887.
- Y. Adam, J. J. Kim, S. Lou, Y. Zhao, M. E. Xie, D. Brinks, H. Wu, M. A. Mostajo-Radji, S. Kheifets, V. Parot, S. Chettih, K. J. Williams, B. Gmeiner, S. L. Farhi, L. Madisen, E. K. Buchanan, I. Kinsella, D. Zhou, L. Paninski, C. D. Harvey, H. Zeng, P. Arlotta, R. E. Campbell, A. E. Cohen. Voltage imaging and optogenetics reveal behaviour-dependent changes in hippocampal dynamics. Nature (2019) 569, 413–417.
- R. Gao, S. M. Asano, S. Upadhyayula, I. Pisarev, D. E. Milkie, T. L. Liu, V. Singh, A. Graves, G. H Huynh, Y. Zhao, J. Bogovic, J. Colonell, C. M Ott, C. Zugates, S. Tappan, A. Rodriguez, K. R Mosaliganti, S.-H. Sheu, H A. Pasolli, S. Pang, C S. Xu, S. G Megason, H. Hess, J. Lippincott-Schwartz, A. Hantman, G. M Rubin, T. Kirchhausen, S. Saalfeld, Y. Aso, E. S. Boyden, E. Betzig. Cortical column and whole-brain imaging with molecular contrast and nanoscale resolution. Science (2019) 363 (6424), eaau8302.
- A. T. Wassie (co-first), Y. Zhao (co-first), E.S. Boyden*. Expansion microscopy: principles and uses in biological research. Nature Methods (2019) 16, p. 33–41.
- O. Bucur*, Y. Zhao*. Nanoscale Imaging of Kidney Glomeruli Using Expansion Pathology. Frontiers in Medicine (2018) https://doi.org/10.3389/fmed.2018.00322
- Y. Zhao (equal contribution), O. Bucur (equal contribution), H. Irshad, F. Chen, A. Weins, A. L. Stancu, E – Y. Oh, M. DiStasio, V. Torous, B. Glass, I. E. Stillman, S. J. Schnitt, A. H. Beck*, E. S. Boyden*. Nanoscale imaging of clinical specimens using pathology-optimized expansion microscopy. Nature Biotechnology (2017) DOI: 10.1038/nbt.3892 [See also MIT News and BIDMC News]
- P. W. Tillberg, F. Chen, K.D. Piatkevich, Y. Zhao, C.-C. Yu, B. P. English, L. Gao, A. Martorell, H.-J. Suk, F. Yoshida, E. M. DeGennaro, D. H.Roossien, G.. Gong, U. Seneviratne, S. R. Tannenbaum, R. Desimone, D. Cai, E. S. Boyden*. Protein-retention expansion microscopy of cells and tissues labeled using standard fluorescent proteins and antibodies. Nature Biotechnology (2016) 34 (9), 987–992. [Cover article in September 2016 issue of Nature Biotechnology (volume 34, No. 9).]
- L. Tang, Y. Wang, W. Liu, Y. Zhao, R. E. Campbell, and C. Fang. Illuminating Photochemistry of an Excitation Ratiometric Fluorescent Protein Calcium Biosensor. The Journal of Physical Chemistry B (2017) 121 (14), 3016–3023.
- A. S. Abdelfattah, S. L. Farhi (equal contribution), Y. Zhao (equal contribution), D. Brinks, P. Zou, A. Ruangkittisaku, J. Platisa,V. A. Pieribone, K. Ballanyi, A. E. Cohen, and R. E. Campbell*. A bright and fast red fluorescent protein voltage indicator that reports neuronal activity in organotypic brain slices. The Journal of Neuroscience (2016) 36 (8): 2458-2472.
- F. Hatahet, J. L Blazyk, E. Martineau, E. Mandela, Y. Zhao, R. E Campbell, J. Beckwith, D. Boyd*. Altered Escherichia coli membrane protein assembly machinery allows proper membrane assembly of eukaryotic protein vitamin K epoxide reductase. Proceedings of the National Academy of Sciences (2015) 112 (49): 15184-15189.
- L. Tang, W. Liu, Y. Wang, Y. Zhao, B. G. Oscar, R. E. Campbell, C. Fang*. Unraveling ultrafast photoinduced proton transfer dynamics in a fluorescent protein biosensor for Ca2+ imaging. Chemistry-A European Journal (2015) 21 (17), 6481-6490.
- T. Albrecht (equal contribution), Y. Zhao (equal contribution), T. Nguyen, R. E. Campbell* and J. D. Johnson*. Fluorescent biosensors illuminate calcium levels within defined beta-cell endosome subpopulations. Cell Calcium. (2015) 57 (4), 263-274.
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