Dr Garcia received his PhD (2015) from the Kolling Institute of Medical Research for his study of the Na+, K+ ATPase and the effect of redox signalling on the kinetics of the functional cycle of the protein. Following his PhD, Dr Garcia was postdoctoral researcher with A/Prof. Clarke at the University of Sydney where he studied the interaction of the ATPase with the surrounding cell membrane. In 2018, Dr Garcia was appointed a UTS CPDRF to study protein-membrane interactions. Based on the results of his initial investigations at UTS, this has expanded into developing a novel paradigm for the interaction of ions with phospholipid bilayers. Understanding how ions and proteins interact with the surface of a cell membrane will enable us to determine how large macromolecular structures can be formed through protein association and ion-induced phase separation. This work will provide an ability to define the role of cell membrane in cellular processes. It will describe how the disruption of cell membranes, through exogenous compounds or changes due to pathophysiological processes (e.g. lipid oxidation) alter protein function. It also provides an avenue to improve the design and implementation of lipid-based bionanosensors.
Dr Garcia studies the interactions at the water-lipid interface, especially in phospholipid membranes. His research combines biophysical techniques to understand how proteins and ions interact with model mammalian cell membranes. The knowledge garnered from this can be used to develop new approaches to understand basic membrane-associated cellular processes.
Keywords: protein membrane interactions, ion membrane interactions, membrane biophysics.
Garcia, A, Zou, H, Hossain, KR, Xu, QH, Buda, A & Clarke, RJ 2019, 'Polar Interactions Play an Important Role in the Energetics of the Main Phase Transition of Phosphatidylcholine Membranes', ACS Omega, vol. 4, no. 1, pp. 518-527.View/Download from: Publisher's site
© 2019 American Chemical Society. Conformational changes of membrane proteins are accompanied by deformation in the surrounding lipid bilayer. To gain insight into the energetics of membrane deformation, the phase behavior of dimyristoylphosphatidylcholine (DMPC) membranes in the presence of the dipole potential, d, modifiers was investigated by differential scanning calorimetry. 7-Ketocholesterol, which weakens d and reduces membrane-perpendicular dipole-dipole repulsion, causes a discrete second peak on the high-temperature side of the main transition, whereas 6-ketocholestanol, which strengthens d and increases membrane-perpendicular dipole-dipole repulsion, merely produces a shoulder. Measurements on pure DMPC vesicles showed that the observed temperature profile could not be explained by a single endothermic process, that is, breaking of van der Waals forces between hydrocarbon chains alone. Removal of NaCl from the buffer caused an increase in the main transition temperature and the appearance of an obvious shoulder, implicating polar interactions. Consideration of the phosphatidylcholine (PC) head group dipole moment indicates direct interactions between PC dipoles that are unlikely to account for the additional process. It seems more likely that the breaking of an in-plane hydrogen-bonded network consisting of hydrating water dipoles together with zwitterionic lipid head groups is responsible. The evidence presented supports the idea that the breaking of van der Waals forces between lipid tails required for the main phase transition of PC membranes is coupled to partial breaking of a hydrogen-bonded network at the membrane surface.
Garcia, A, Lev, B, Hossain, KR, Gorman, A, Diaz, D, Pham, THN, Cornelius, F, Allen, TW & Clarke, RJ 2019, 'Cholesterol depletion inhibits Na,K-ATPase activity in a near-native membrane environment', Journal of Biological Chemistry, vol. 294, no. 15, pp. 5956-5969.View/Download from: Publisher's site
© 2019 Garcia et al. Cholesterol's effects on Na,K-ATPase reconstituted in phospholipid vesicles have been extensively studied. However, previous studies have reported both cholesterol-mediated stimulation and inhibition of Na,K-ATPase activity. Here, using partial reaction kinetics determined via stopped-flow experiments, we studied cholesterol's effect on Na,K-ATPase in a near-native environment in which purified membrane fragments were depleted of cholesterol with methyl-cyclodextrin (mCD). The mCD-treated Na,K-ATPase had significantly reduced overall activity and exhibited decreased observed rate constants for ATP phosphorylation (ENa 3 3 E2P, i.e. phosphorylation by ATP and Na occlusion from the cytoplasm) and K deocclusion with subsequent intracellular Na binding (E2K 2 3 E1Na 3 ). However, cholesterol depletion did not affect the observed rate constant for K occlusion by phosphorylated Na,K-ATPase on the extracellular face and subsequent dephosphorylation (E2P 3 E2K 2 ). Thus, partial reactions involving cation binding and release at the protein's intracellular side were most dependent on cholesterol. Fluorescence measurements with the probe eosin indicated that cholesterol depletion stabilizes the unphosphorylated E2 state relative to E1, and the cholesterol depletion-induced slowing of ATP phosphorylation kinetics was consistent with partial conversion of Na,K-ATPase into the E2 state, requiring a slow E2 3 E1 transition before the phosphorylation. Molecular dynamics simulations of Na,K-ATPase in membranes with 40 mol % cholesterol revealed cholesterol interaction sites that differ markedly among protein conformations. They further indicated state-dependent effects on membrane shape, with the E2 state being likely disfavored in cholesterol-rich bilayers relative to the E1P
Garcia, A, Pochinda, S, Elgaard-Jørgensen, PN, Khandelia, H & Clarke, RJ 2019, 'Evidence for ATP Interaction with Phosphatidylcholine Bilayers.', Langmuir : the ACS journal of surfaces and colloids, vol. 35, no. 30, pp. 9944-9953.View/Download from: UTS OPUS or Publisher's site
ATP is a fundamental intracellular molecule and is thought to diffuse freely throughout the cytosol. Evidence obtained from nucleotide-sensing sarcolemmal ion channels and red blood cells, however, suggest that ATP is compartmentalized or buffered, especially beneath the sarcolemma, but no definitive mechanism for restricted diffusion or potential buffering system has been postulated. In this study, we provide evidence from alterations to membrane dipole potential, membrane conductance, changes in enthalpy of phospholipid phase transition, and from free energy calculations that ATP associates with phospholipid bilayers. Furthermore, all-atom molecular dynamics simulations show that ATP can form aggregates in the aqueous phase at high concentrations. ATP interaction with membranes provides a new model to understand the diffusion of ATP through the cell. Coupled with previous reports of diffusion restriction in the subsarcolemmal space, these findings support the existence of compartmentalized or buffered pools of ATP.
Alghalayini, A, Garcia, A, Berry, T & Cranfield, CG 2019, 'The Use of Tethered Bilayer Lipid Membranes to Identify the Mechanisms of Antimicrobial Peptide Interactions with Lipid Bilayers', ANTIBIOTICS-BASEL, vol. 8, no. 1.View/Download from: UTS OPUS or Publisher's site
Deplazes, E, White, J, Murphy, C, Cranfield, CG & Garcia, A 2019, 'Competing for the same space: protons and alkali ions at the interface of phospholipid bilayers.', Biophysical reviews, vol. 11, no. 3, pp. 483-490.View/Download from: UTS OPUS or Publisher's site
Maintaining gradients of solvated protons and alkali metal ions such as Na+ and K+ across membranes is critical for cellular function. Over the last few decades, both the interactions of protons and alkali metal ions with phospholipid membranes have been studied extensively and the reported interactions of these ions with phospholipid headgroups are very similar, yet few studies have investigated the potential interdependence between proton and alkali metal ion binding at the water-lipid interface. In this short review, we discuss the similarities between the proton-membrane and alkali ion-membrane interactions. Such interactions include cation attraction to the phosphate and carbonyl oxygens of the phospholipid headgroups that form strong lipid-ion and lipid-ion-water complexes. We also propose potential mechanisms that may modulate the affinities of these cationic species to the water-phospholipid interfacial oxygen moieties. This review aims to highlight the potential interdependence between protons and alkali metal ions at the membrane surface and encourage a more nuanced understanding of the complex nature of these biologically relevant processes.
Nguyen, K, Garcia, A, Sani, M-A, Diaz, D, Dubey, V, Clayton, D, Dal Poggetto, G, Cornelius, F, Payne, RJ, Separovic, F, Khandelia, H & Clarke, RJ 2018, 'Interaction of N-terminal peptide analogues of the Na+,K+-ATPase with membranes.', Biochimica et biophysica acta. Biomembranes, vol. 1860, no. 6, pp. 1282-1291.View/Download from: UTS OPUS or Publisher's site
The Na+,K+-ATPase, which is present in the plasma membrane of all animal cells, plays a crucial role in maintaining the Na+ and K+ electrochemical potential gradients across the membrane. Recent studies have suggested that the N-terminus of the protein's catalytic α-subunit is involved in an electrostatic interaction with the surrounding membrane, which controls the protein's conformational equilibrium. However, because the N-terminus could not yet be resolved in any X-ray crystal structures, little information about this interaction is so far available. In measurements utilising poly-l-lysine as a model of the protein's lysine-rich N-terminus and using lipid vesicles of defined composition, here we have identified the most likely origin of the interaction as one between positively charged lysine residues of the N-terminus and negatively charged headgroups of phospholipids (notably phosphatidylserine) in the surrounding membrane. Furthermore, to isolate which segments of the N-terminus could be involved in membrane binding, we chemically synthesized N-terminal fragments of various lengths. Based on a combination of results from RH421 UV/visible absorbance measurements and solid-state 31P and 2H NMR using these N-terminal fragments as well as MD simulations it appears that the membrane interaction arises from lysine residues prior to the conserved LKKE motif of the N-terminus. The MD simulations indicate that the strength of the interaction varies significantly between different enzyme conformations.
Jiang, Q, Garcia, A, Han, M, Cornelius, F, Apell, H-J, Khandelia, H & Clarke, RJ 2017, 'Electrostatic Stabilization Plays a Central Role in Autoinhibitory Regulation of the Na+,K+-ATPase.', Biophysical Journal, vol. 112, no. 2, pp. 288-299.View/Download from: UTS OPUS or Publisher's site
The Na+,K+-ATPase is present in the plasma membrane of all animal cells. It plays a crucial role in maintaining the Na+ and K+ electrochemical potential gradients across the membrane, which are essential in numerous physiological processes, e.g., nerve, muscle, and kidney function. Its cellular activity must, therefore, be under tight metabolic control. Consideration of eosin fluorescence and stopped-flow kinetic data indicates that the enzyme's E2 conformation is stabilized by electrostatic interactions, most likely between the N-terminus of the protein's catalytic α-subunit and the adjacent membrane. The electrostatic interactions can be screened by increasing ionic strength, leading to a more evenly balanced equilibrium between the E1 and E2 conformations. This represents an ideal situation for effective regulation of the Na+,K+-ATPase's enzymatic activity, because protein modifications, which perturb this equilibrium in either direction, can then easily lead to activation or inhibition. The effect of ionic strength on the E1:E2 distribution and the enzyme's kinetics can be mathematically described by the Gouy-Chapman theory of the electrical double layer. Weakening of the electrostatic interactions and a shift toward E1 causes a significant increase in the rate of phosphorylation of the enzyme by ATP. Electrostatic stabilization of the Na+,K+-ATPase's E2 conformation, thus, could play an important role in regulating the enzyme's physiological catalytic turnover.
Garcia, A, Pratap, PR, Lüpfert, C, Cornelius, F, Jacquemin, D, Lev, B, Allen, TW & Clarke, RJ 2017, 'The voltage-sensitive dye RH421 detects a Na+,K+-ATPase conformational change at the membrane surface.', BBA - Biochimica et Biophysica Acta, vol. 1859, no. 5, pp. 813-823.View/Download from: UTS OPUS or Publisher's site
RH421 is a voltage-sensitive fluorescent styrylpyridinium dye which has often been used to probe the kinetics of Na+,K+-ATPase partial reactions. The origin of the dye's response has up to now been unclear. Here we show that RH421 responds to phosphorylation of the Na+,K+-ATPase by inorganic phosphate with a fluorescence increase. Analysis of the kinetics of the fluorescence response indicates that the probe is not detecting phosphorylation itself but rather a shift in the protein's E1/E2 conformational equilibrium induced by preferential phosphate binding to and phosphorylation of enzyme in the E2 conformation. Molecular dynamics simulations of crystal structures in lipid bilayers indicate some change in the protein's hydrophobic thickness during the E1-E2 transition, which may influence the dye response. However, the transition is known to involve significant rearrangement of the protein's highly charged lysine-rich cytoplasmic N-terminal sequence. Using poly-l-lysine as a model of the N-terminus, we show that an analogous response of RH421 to the E1→E2P conformational change is produced by poly-l-lysine binding to the surface of the Na+,K+-ATPase-containing membrane fragments. Thus, it seems that the prime origin of the RH421 fluorescence response is a change in the interaction of the protein's N-terminus with the surrounding membrane. Quantum mechanical calculations of the dye's visible absorption spectrum give further support to this conclusion. The results obtained indicate that membrane binding and release of the N-terminus of the Na+,K+-ATPase α-subunit are intimately involved in the protein's catalytic cycle and could represent an effective site of regulation.
Galougahi, KK, Liu, C-C, Garcia, A, Gentile, C, Fry, NA, Hamilton, EJ, Hawkins, CL & Figtree, GA 2016, 'beta 3 Adrenergic Stimulation Restores Nitric Oxide/Redox Balance and Enhances Endothelial Function in Hyperglycemia', JOURNAL OF THE AMERICAN HEART ASSOCIATION, vol. 5, no. 2.View/Download from: Publisher's site
Garcia, A, Liu, C-C, Cornelius, F, Clarke, RJ & Rasmussen, HH 2016, 'Glutathionylation-Dependence of Na+-K+-Pump Currents Can Mimic Reduced Subsarcolemmal Na+ Diffusion', BIOPHYSICAL JOURNAL, vol. 110, no. 5, pp. 1099-1109.View/Download from: Publisher's site
Lambropoulos, N, Garcia, A & Clarke, RJ 2016, 'Stimulation of Na+,K+-ATPase Activity as a Possible Driving Force in Cholesterol Evolution', JOURNAL OF MEMBRANE BIOLOGY, vol. 249, no. 3, pp. 251-259.View/Download from: Publisher's site
Galougahi, KK, Liu, C-C, Garcia, A, Fry, NA, Hamilton, EJ, Figtree, GA & Rasmussen, HH 2015, 'beta(3)-Adrenoceptor activation relieves oxidative inhibition of the cardiac Na+-K+ pump in hyperglycemia induced by insulin receptor blockade', AMERICAN JOURNAL OF PHYSIOLOGY-CELL PHYSIOLOGY, vol. 309, no. 5, pp. C286-C295.View/Download from: Publisher's site
Chia, KKM, Liu, C-C, Hamilton, EJ, Garcia, A, Fry, NA, Hannam, W, Figtree, GA & Rasmussen, HH 2015, 'Stimulation of the cardiac myocyte Na+-K+ pump due to reversal of its constitutive oxidative inhibition', AMERICAN JOURNAL OF PHYSIOLOGY-CELL PHYSIOLOGY, vol. 309, no. 4, pp. C239-C250.View/Download from: Publisher's site
Garcia, A, Eljack, ND, Sani, M-A, Separovic, F, Rasmussen, HH, Kopec, W, Khandelia, H, Cornelius, F & Clarke, RJ 2015, 'Membrane accessibility of glutathione', BIOCHIMICA ET BIOPHYSICA ACTA-BIOMEMBRANES, vol. 1848, no. 10, pp. 2430-2436.View/Download from: Publisher's site
Galougahi, KK, Liu, CC, Gentile, C, Kok, C, Nunez, A, Garcia, A, Fry, NAS, Davies, MJ, Hawkins, CL, Rasmussen, HH & Figtree, GA 2014, 'Glutathionylation mediates angiotensin II-induced eNOS uncoupling, amplifying NADPH oxidase-dependent endothelial dysfunction.', Journal of the American Heart Association, vol. 3, no. 2.View/Download from: Publisher's site
Glutathionylation of endothelial nitric oxide synthase (eNOS) "uncouples" the enzyme, switching its function from nitric oxide (NO) to O2(*-) generation. We examined whether this reversible redox modification plays a role in angiotensin II (Ang II)-induced endothelial dysfunction. Ang II increased eNOS glutathionylation in cultured human umbilical vein endothelial cells (HUVECs), rabbit aorta, and human arteries in vitro. This was associated with decreased NO bioavailability and eNOS activity as well as increased O2(*-) generation. Ang II-induced decrease in eNOS activity was mediated by glutathionylation, as shown by restoration of function by glutaredoxin-1. Moreover, Ang II-induced increase in O2(*-) and decrease in NO were abolished in HUVECs transiently transfected, with mutant eNOS rendered resistant to glutathionylation. Ang II effects were nicotinamide adenine dinucleotide phosphate (NADPH) oxidase dependent because preincubation with gp 91ds-tat, an inhibitor of NADPH oxidase, abolished the increase in eNOS glutathionylation and loss of eNOS activity. Functional significance of glutathionylation in intact vessels was supported by Ang II-induced impairment of endothelium-dependent vasorelaxation that was abolished by the disulfide reducing agent, dithiothreitol. Furthermore, attenuation of Ang II signaling in vivo by administration of an angiotensin converting enzyme (ACE) inhibitor reduced eNOS glutathionylation, increased NO, diminished O2(*-), improved endothelium-dependent vasorelaxation and reduced blood pressure. Uncoupling of eNOS by glutathionylation is a key mediator of Ang II-induced endothelial dysfunction, and its reversal is a mechanism for cardiovascular protection by ACE inhibition. We suggest that Ang II-induced O2(*-) generation in endothelial cells, although dependent on NADPH oxidase, is amplified by glutathionylation-dependent eNOS uncoupling.
Mares, LJ, Garcia, A, Rasmussen, HH, Cornelius, F, Mahmmoud, YA, Berlin, JR, Lev, B, Allen, TW & Clarke, RJ 2014, 'Identification of Electric-Field-Dependent Steps in the Na+,K+-Pump Cycle', BIOPHYSICAL JOURNAL, vol. 107, no. 6, pp. 1352-1363.View/Download from: Publisher's site
Galougahi, KK, Liu, C-C, Garcia, A, Fry, NAS, Hamilton, EJ, Rasmussen, HH & Figtree, GA 2013, 'Protein kinase-dependent oxidative regulation of the cardiac Na+-K+ pump: evidence from in vivo and in vitro modulation of cell signalling', JOURNAL OF PHYSIOLOGY-LONDON, vol. 591, no. 12, pp. 2999-3015.View/Download from: Publisher's site
Liu, C-C, Galougahi, KK, Weisbrod, RM, Hansen, T, Ravaie, R, Nunez, A, Liu, YB, Fry, N, Garcia, A, Hamilton, EJ, Sweadner, KJ, Cohen, RA & Figtree, GA 2013, 'Oxidative inhibition of the vascular Na+-K+ pump via NADPH oxidase-dependent pi-subunit glutathionylation: Implications for angiotensin beta(1)-induced vascular dysfunction', FREE RADICAL BIOLOGY AND MEDICINE, vol. 65, pp. 563-572.View/Download from: Publisher's site
Garcia, A, Rasmussen, HH, Apell, HJ & Clarke, RJ 2013, 'Erratum: Kinetic comparisons of heart and kidney Na+,K+-ATPases (Biophysical Journal (2012) 103 (677-688))', Biophysical Journal, vol. 104, no. 5, p. 1214.View/Download from: Publisher's site
Garcia, A, Fry, NAS, Karimi, K, Liu, C-C, Apell, H-J, Rasmussen, HH & Clarke, RJ 2013, 'Extracellular Allosteric Na+ Binding to the Na+,K+-ATPase in Cardiac Myocytes', BIOPHYSICAL JOURNAL, vol. 105, no. 12, pp. 2695-2705.View/Download from: Publisher's site
Liu, C-C, Fry, NAS, Hamilton, EJ, Chia, KKM, Garcia, A, Galougahi, KK, Figtree, GA, Clarke, RJ, Bundgaard, H & Rasmussen, HH 2013, 'Redox-dependent regulation of the Na+-K+ pump: New twists to an old target for treatment of heart failure', JOURNAL OF MOLECULAR AND CELLULAR CARDIOLOGY, vol. 61, pp. 94-101.View/Download from: Publisher's site
Garcia, A, Rasmussen, HH, Apell, H-J & Clarke, RJ 2012, 'Kinetic Comparisons of Heart and Kidney Na+,K+-ATPases', BIOPHYSICAL JOURNAL, vol. 103, no. 4, pp. 677-688.View/Download from: Publisher's site
Liu, C-C, Garcia, A, Mahmmoud, YA, Hamilton, EJ, Galougahi, KK, Fry, NAS, Figtree, GA, Cornelius, F, Clarke, RJ & Rasmussen, HH 2012, 'Susceptibility of beta 1 Na+-K+ Pump Subunit to Glutathionylation and Oxidative Inhibition Depends on Conformational State of Pump', JOURNAL OF BIOLOGICAL CHEMISTRY, vol. 287, no. 15, pp. 12353-12364.View/Download from: Publisher's site
Bibert, S, Liu, C-C, Figtree, GA, Garcia, A, Hamilton, EJ, Marassi, FM, Sweadner, KJ, Cornelius, F, Geering, K & Rasmussen, HH 2011, 'FXYD Proteins Reverse Inhibition of the Na+-K+ Pump Mediated by Glutathionylation of Its beta(1) Subunit', JOURNAL OF BIOLOGICAL CHEMISTRY, vol. 286, no. 21, pp. 18562-18572.View/Download from: Publisher's site
White, CN, Liu, C-C, Garcia, A, Hamilton, EJ, Chia, KKM, Figtree, GA & Rasmussen, HH 2010, 'Activation of cAMP-dependent Signaling Induces Oxidative Modification of the Cardiac Na+-K+ Pump and Inhibits Its Activity', JOURNAL OF BIOLOGICAL CHEMISTRY, vol. 285, no. 18, pp. 13712-13720.View/Download from: Publisher's site
Bundgaard, H, Liu, C-C, Garcia, A, Hamilton, EJ, Huang, Y, Chia, KKM, Hunyor, SN, Figtree, GA & Rasmussen, HH 2010, 'beta(3) Adrenergic Stimulation of the Cardiac Na+ -K+ Pump by Reversal of an Inhibitory Oxidative Modification', CIRCULATION, vol. 122, no. 25, pp. 2699-U209.View/Download from: Publisher's site
Figtree, GA, Liu, C-C, Bibert, S, Hamilton, EJ, Garcia, A, White, CN, Chia, KKM, Cornelius, F, Geering, K & Rasmussen, HH 2009, 'Reversible Oxidative Modification A Key Mechanism of Na+-K+ Pump Regulation', CIRCULATION RESEARCH, vol. 105, no. 2, pp. 185-U187.View/Download from: Publisher's site
White, CN, Figtree, GA, Liu, C-C, Garcia, A, Hamilton, EJ, Chia, KKM & Rasmussen, HH 2009, 'Angiotensin II inhibits the Na+-K+ pump via PKC-dependent activation of NADPH oxidase', AMERICAN JOURNAL OF PHYSIOLOGY-CELL PHYSIOLOGY, vol. 296, no. 4, pp. C693-C700.View/Download from: Publisher's site
White, CN, Hamilton, EJ, Garcia, A, Wang, D, Chia, KKM, Figtree, GA & Rasmussen, HH 2008, 'Opposing effects of coupled and uncoupled NOS activity on the Na+-K+ pump in cardiac myocytes', AMERICAN JOURNAL OF PHYSIOLOGY-CELL PHYSIOLOGY, vol. 294, no. 2, pp. C572-C578.View/Download from: Publisher's site
William, M, Hamilton, EJ, Garcia, A, Bundgaard, H, Chia, KKM, Figtree, GA & Rasmussen, HH 2008, 'Natriuretic peptides stimulate the cardiac sodium pump via NPR-C-coupled NOS activation', AMERICAN JOURNAL OF PHYSIOLOGY-CELL PHYSIOLOGY, vol. 294, no. 4, pp. C1067-C1073.View/Download from: Publisher's site
Hansen, PS, Clarke, RJ, Buhagiar, KA, Hamilton, E, Garcia, A, White, C & Rasmussen, HH 2007, 'Alloxan-induced diabetes reduces sarcolemmal Na+-K+ pump function in rabbit ventricular myocytes', AMERICAN JOURNAL OF PHYSIOLOGY-CELL PHYSIOLOGY, vol. 292, no. 3, pp. C1070-C1077.View/Download from: Publisher's site
Allan, CM, Garcia, A, Spaliviero, J & Jimenez, M 2006, 'Maintenance of spermatogenesis by the activated human (Asp567Gly) FSH receptor during testicular regression due to hormonal withdrawal', BIOLOGY OF REPRODUCTION, vol. 74, no. 5, pp. 938-944.View/Download from: Publisher's site
Allan, CM, Garcia, A, Spaliviero, J, Jimenez, M & Handelsman, DJ 2006, 'Erratum: Maintenance of spermatogenesis by the activated human (Asp567Gly) FSH receptor during testicular regression due to hormonal withdrawal (Biology of Reproduction (2006) 74, (938-944) DOI: 10.1095/biolreprod.105.048413)', Biology of Reproduction, vol. 74, no. 6, p. 1121.View/Download from: Publisher's site
William, M, Vien, J, Hamilton, E, Garcia, A, Bundgaard, H, Clarke, RJ & Rasmussen, HH 2005, 'The nitric oxide donor sodium nitroprusside stimulates the Na+-K+ pump in isolated rabbit cardiac myocytes', JOURNAL OF PHYSIOLOGY-LONDON, vol. 565, no. 3, pp. 815-825.View/Download from: Publisher's site
Allan, CM, Garcia, A, Spaliviero, J, Zhang, FP, Jimenez, M, Huhtaniemi, I & Handelsman, DJ 2004, 'Complete sertoli cell proliferation induced by follicle-stimulating hormone (FSH) independently of luteinizing hormone activity: Evidence from genetic models of isolated FSH action', ENDOCRINOLOGY, vol. 145, no. 4, pp. 1587-1593.View/Download from: Publisher's site
White, C, Hamilton, E, Garcia, A & Rasmussen, HH 2006, 'Angiotensin II regulates the Na+-K+ pump in rabbit ventricular myocytes via the epsilon-isoform of protein kinase C, NAD(P)H oxidase and reactive oxygen/nitrogen species', CIRCULATION, 79th Annual Scientific Session of the American-Heart-Association, LIPPINCOTT WILLIAMS & WILKINS, Chicago, IL, pp. 3-3.