413
Views
14
CrossRef citations to date
0
Altmetric
Review

Using Xenopus oocytes in neurological disease drug discovery

, &
Pages 39-52 | Received 12 Jul 2019, Accepted 17 Oct 2019, Published online: 01 Nov 2019

References

  • Gooch CL, Pracht E, Borenstein AR. The burden of neurological disease in the United States: A summary report and call to action. Ann Neurol. 2017;81(4):479–484.
  • Huang Y, Mucke L. Alzheimer mechanisms and therapeutic strategies. Cell. 2012;148(6):1204–1222.
  • Marmiroli P, Cavaletti G. Drugs for the treatment of peripheral neuropathies. Expert Opin Pharmacother. 2016;17(3):381–394.
  • Mazarati A, Sankar R. Common mechanisms underlying epileptogenesis and the comorbidities of epilepsy. Cold Spring Harb Perspect Med. 2016;6:7.
  • Moustafa AA, Phillips J, Kéri S, et al. On the complexity of brain disorders: a symptom-based approach. Front Comput Neurosci. 2016;10:16.
  • Kumar P, Kumar D, Jha SK, et al. Ion channels in neurological disorders. Adv Protein Chem Struct Biol. 2016;103:97–136.
  • Waszkielewicz AM, Gunia A, Szkaradek N, et al. Ion channels as drug targets in central nervous system disorders. Curr Med Chem. 2013;20(10):1241–1285.
  • Hart IK. Acquired neuromyotonia: a new autoantibody-mediated neuronal potassium channelopathy. Am J Med Sci. 2000;319(4):209–216.
  • Browne DL, Gancher ST, Nutt JG, et al. Episodic ataxia/myokymia syndrome is associated with point mutations in the human potassium channel gene, KCNA1. Nat Genet. 1994;8(2):136–140.
  • Heron SE, Crossland KM, Andermann E, et al. Sodium-channel defects in benign familial neonatal-infantile seizures. Lancet. 2002;360(9336):851–852.
  • Benatar M. Neurological potassium channelopathies. QJM. 2000;93(12):787–797.
  • Cummins TR, Dib-Hajj SD, Waxman SG. Electrophysiological properties of mutant Nav1.7 sodium channels in a painful inherited neuropathy. J Neurosci. 2004;24(38):8232–8236.
  • Meisler MH, Kearney JA. Sodium channel mutations in epilepsy and other neurological disorders. J Clin Invest. 2005;115(8):2010–2017.
  • Casamassima F, Hay AC, Benedetti A, et al. L-type calcium channels and psychiatric disorders: A brief review. Am J Med Genet B Neuropsychiatr Genet. 2010;153B(8):1373–1390.
  • Shaw G, Morse S, Ararat M, et al. Preferential transformation of human neuronal cells by human adenoviruses and the origin of HEK 293 cells. Faseb J. 2002;16(8):869–871.
  • Atkin TA, Maher CM, Gerlach AC, et al. A comprehensive approach to identifying repurposed drugs to treat SCN8A epilepsy. Epilepsia. 2018;59(4):802–813.
  • Miledi R, Parker I, Sumikawa K. Synthesis of chick brain GABA receptors by frog oocytes. Proc R Soc Lond B Biol Sci. 1982;216(1205):509–515.
  • Hellsten U, Harland RM, Gilchrist MJ, et al. The genome of the western clawed frog Xenopus tropicalis. Science (New York, NY). 2010;328(5978):633–636.
  • Schultz Ms PTW, Dawson PhD DA. Housing and husbandry of Xenopus for oocyte production. Lab Anim (NY). 2003;32:34.
  • Kvist T, Hansen KB, Bräuner-Osborne H. The use of Xenopus oocytes in drug screening. Expert Opin Drug Discov. 2011;6(2):141–153.
  • Gurdon JB, Lane CD, Woodland HR, et al. Use of frog eggs and oocytes for the study of messenger RNA and its translation in living cells. Nature. 1971;233(5316):177–182.
  • Kusano K, Miledi R, Stinnakre J. Acetylcholine receptors in the oocyte membrane. Nature. 1977;270(5639):739–741.
  • Wood C, Williams C, Waldron GJ. Patch clamping by numbers. Drug Discov Today. 2004;9(10):434–441.
  • Lacerda A, Kramer J, Shen K-Z, et al. Comparison of block among cloned cardiac potassium channels by non-antiarrhythmic drugs. Eur Heart J Suppl. 2001;3(suppl_K):K23–K30.
  • Gurdon JB, Hopwood N. The introduction of Xenopus laevis into developmental biology: of empire, pregnancy testing and ribosomal genes. Int J Dev Biol. 2000;44(1):43–50.
  • Gurdon JB, Wickens MP. 28 - The use of Xenopus oocytes for the expression of cloned genes. In: Wu R, Grossman L, Moldave K, editors. Recombinant DNA methodology. San Diego: Academic Press; 1989. p. 489–505.
  • Partin K, Patneau D, Winters C, et al. Selective modulation of desensitization at AMPA versus kainate receptors by cyclothiazide and concanavalin A. Neuron. 1993;11(6):1069–1082.
  • Kobayashi T, Hirai H, Iino M, et al. Inhibitory effects of the antiepileptic drug ethosuximide on G protein-activated inwardly rectifying K+ channels. Neuropharmacology. 2009;56(2):499–506.
  • Rammes G, Danysz W, Parsons CG. Pharmacodynamics of memantine: an update. Curr Neuropharmacol. 2008;6(1):55–78.
  • Ryu JH, Lee PB, Kim JH, et al. Effects of pregabalin on the activity of glutamate transporter type 3. Br J Anaesth. 2012;109(2):234–239.
  • Chen X, Qiu L, Li M, et al. Diarylamidines: high potency inhibitors of acid-sensing ion channels. Neuropharmacology. 2010;58(7):1045–1053.
  • Christian Wolff BM, Ghisdal P, Provins L, et al. Functional characterization of padsevonil on gaba-a receptors. Abst. 1.270, American Epilepsy Society, Annual Meeting Abstracts. 2017.
  • Ruffolo G, Di Bonaventura C, Cifelli P, et al. A novel action of lacosamide on GABAA currents sets the ground for a synergic interaction with levetiracetam in treatment of epilepsy. Neurobiol Dis. 2018;115:59–68.
  • Palma E, Esposito V, Mileo AM, et al. Expression of human epileptic temporal lobe neurotransmitter receptors in Xenopus oocytes: an innovative approach to study epilepsy. Proc Natl Acad Sci U S A. 2002;99(23):15078–15083.
  • Palma E, Spinelli G, Torchia G, et al. Abnormal GABAA receptors from the human epileptic hippocampal subiculum microtransplanted to Xenopus oocytes. Proc Natl Acad Sci U S A. 2005;102(7):2514–2518.
  • Hardwick LJA, Philpott A. An oncologist׳s friend: how Xenopus contributes to cancer research. Dev Biol. 2015;408(2):180–187.
  • Limon A, Reyes-Ruiz JM, Miledi R. Microtransplantation of neurotransmitter receptors from postmortem autistic brains to Xenopus oocytes. Proc Natl Acad Sci U S A. 2008;105(31):10973–10977.
  • Sicca F, Ambrosini E, Marchese M, et al. Gain-of-function defects of astrocytic Kir4.1 channels in children with autism spectrum disorders and epilepsy. Sci Rep. 2016;6:34325.
  • Kaya F, Mannioui A, Chesneau A, et al. Live imaging of targeted cell ablation in Xenopus: a new model to study demyelination and repair. J Neurosci. 2012;32(37):12885–12895.
  • Levis RA, Rae JL. [14] Low-noise patch-clamp techniques. In: Conn PM, editor. Methods in enzymology. New York (NY): Academic Press; 1998. p. 218–266.
  • Rasar MA, Hammes SR. The physiology of the Xenopus laevis ovary. Methods Mol Biol. 2006;322:17–30.
  • Webb DJ, Nuccitelli R. Fertilization potential and electrical properties of the Xenopus laevis egg. Dev Biol. 1985;107(2):395–406.
  • Wagner CA, Friedrich B, Setiawan I, et al. The use of Xenopus laevis oocytes for the functional characterization of heterologously expressed membrane proteins. Cell Physiol Biochem. 2000;10(1–2):1–12.
  • Terhag J, Cavara NA, Hollmann M. Cave canalem:how endogenous ion channels may interfere with heterologous expression in Xenopus oocytes. Methods. 2010;51(1):66–74.
  • Gradogna A, Gaitán-Peñas H, Boccaccio A, et al. Cisplatin activates volume sensitive LRRC8 channel mediated currents in Xenopus oocytes. Channels. 2017;11(3):254–260.
  • Dumont JN. Oogenesis in Xenopus laevis (Daudin). I. Stages of oocyte development in laboratory maintained animals. J Morphol. 1972;136(2):153–179.
  • Richter JD, Lasko P. Translational control in oocyte development. Cold Spring Harb Perspect Biol. 2011;3(9):a002758–a58.
  • Asselbergs FAM, Van Venrooij WJ, Bloemendal H. Messenger RNA competition in living Xenopus oocytes. Eur J Biochem. 1979;94(1):249–254.
  • Colman A, Bhamra S, Valle G. Post-translational modification of exogenous proteins in Xenopus laevis oocytes. Biochem Soc Trans. 1984;12(6):932–937.
  • Cohen S, Au S, Panté N. Microinjection of Xenopus laevis oocytes. J Vis Exp. 2009;24:1106.
  • Miledi R, Eusebi F, Martinez-Torres A, et al. Expression of functional neurotransmitter receptors in Xenopus oocytes after injection of human brain membranes. Proc Natl Acad Sci U S A. 2002;99(20):13238–13242.
  • Aguero T, Newman K, King ML. Microinjection of Xenopus oocytes. Cold Spring Harb Protoc. 2018;2018(2):pdb.prot096974.
  • Hogg RC, Bandelier F, Benoit A, et al. An automated system for intracellular and intranuclear injection. J Neurosci Methods. 2008;169(1):65–75.
  • Schnizler K, Küster M, Methfessel C, et al. The roboocyte: automated cDNA/mRNA injection and subsequent TEVC recording on Xenopus oocytes in 96-well microtiter plates. Recept Channels. 2003;9(1):41–48.
  • Graf SF, Madigou T, Li R, et al. Fully automated microinjection system for Xenopus laevis oocytes with integrated sorting and collection. JALA J Assoc Lab Autom. 2011;16(3):186–196.
  • Papke RL, Stokes C. Working with OpusXpress: methods for high volume oocyte experiments. Methods. 2010;51(1):121–133.
  • Yajuan X, Xin L, Zhiyuan L. A comparison of the performance and application differences between manual and automated patch-clamp techniques. Curr Chem Genomics. 2012;6:87–92.
  • Comley J. Automated patch clamping finally achieves high throughout! Drug Discovery World. 2014;45–56.
  • Yang XC, Karschin A, Labarca C, et al. Expression of ion channels and receptors in Xenopus oocytes using vaccinia virus. Faseb J. 1991;5(8):2209–2216.
  • Palma E, Trettel F, Fucile S, et al. Microtransplantation of membranes from cultured cells to Xenopus oocytes: A method to study neurotransmitter receptors embedded in native lipids. Proc Nat Acad Sci. 2003;100(5):2896–2900.
  • Marsal J, Tigyi G, Miledi R. Incorporation of acetylcholine receptors and Cl- channels in Xenopus oocytes injected with Torpedo electroplaque membranes. Proc Natl Acad Sci U S A. 1995;92(11):5224–5228.
  • Sanna E, Motzo C, Murgia A, et al. Expression of native GABAA receptors in Xenopus oocytes injected with rat brain synaptosomes. J Neurochem. 1996;67(5):2212–2214.
  • Murenzi E, Toltin AC, Symington SB, et al. Evaluation of microtransplantation of rat brain neurolemma into Xenopus laevis oocytes as a technique to study the effect of neurotoxicants on endogenous voltage-sensitive ion channels. Neurotoxicology. 2017;60:260–273.
  • Miledi R, Dueñas Z, Martinez-Torres A, et al. Microtransplantation of functional receptors and channels from the Alzheimer’s brain to frog oocytes. Proc Natl Acad Sci U S A. 2004;101(6):1760–1763.
  • Hernández-Ochoa EO, Schneider MF. Voltage clamp methods for the study of membrane currents and SR Ca(2+) release in adult skeletal muscle fibres. Prog Biophys Mol Biol. 2012;108(3):98–118.
  • Guan B, Chen X, Zhang H. Two-electrode voltage clamp. Methods Mol Biol. 2013;998:79–89.
  • Varjabedian A, Kita A, Bement W. Chapter 11 - living Xenopus oocytes, eggs, and embryos as models for cell division. In: Maiato H, Schuh M, editors. Methods in cell biology. Cambridge (MA): Academic Press; 2018. p. 259–285.
  • Dascal N. Voltage clamp recordings from Xenopus oocytes. Curr Protoc Neurosci. 2001. Chapter 6:Unit6.12.
  • Chapter 5. Advanced Methods in Electrophysiology. The Axon™ guide. 3rd ed. Molecular Devices; 2012. p. 303.
  • Hamill OP, Marty A, Neher E, et al. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflügers Archiv. 1981;391(2):85–100.
  • Denyer J, Worley J, Cox B, et al. HTS approaches to voltage-gated ion channel drug discovery. Drug Discov Today. 1998;3(7):323–332.
  • Pantazis A, Olcese R. Cut-open oocyte voltage-clamp technique. In: Roberts GCK, editor. Encyclopedia of biophysics. Berlin, Heidelberg: Springer; 2013. p. 406–413.
  • Baburin I, Beyl S, Hering S. Automated fast perfusion of Xenopus oocytes for drug screening. Pflugers Arch. 2006;453(1):117–123.
  • Mannuzzu LM, Moronne MM, Isacoff EY. Direct physical measure of conformational rearrangement underlying potassium channel gating. Science. 1996;271(5246):213–216.
  • Zhu W, Varga Z, Silva JR. Molecular motions that shape the cardiac action potential: insights from voltage clamp fluorometry. Prog Biophys Mol Biol. 2016;120(1):3–17.
  • Osteen JD, Gonzalez C, Sampson KJ, et al. KCNE1 alters the voltage sensor movements necessary to open the KCNQ1 channel gate. Proc Nat Acad Sci. 2010;107(52):22710–22715.
  • Cha A, Zerangue N, Kavanaugh M, et al. [38] Fluorescence techniques for studying cloned channels and transporters expressed in Xenopus oocytes. In: Amara SG, editor. Methods in enzymology. San Diego (CA): Academic Press; 1998. p. 566–578.
  • Akk G, Steinbach Joe H. Structural studies of the actions of anesthetic drugs on the γ-aminobutyric acid type a receptor. Anesthesiol J Am Soc Anesthesiologists. 2011;115(6):1338–1348.
  • Treger JS, Priest MF, Iezzi R, et al. Real-time imaging of electrical signals with an infrared FDA-approved dye. Biophys J. 2014;107(6):L09–L12.
  • Eaton MM, Lim YB, Covey DF, et al. Modulation of the human ρ1 GABAA receptor by inhibitory steroids. Psychopharmacology (Berl). 2014;231(17):3467–3478.
  • Stefani E, Bezanilla F. Cut-open oocyte voltage-clamp technique. In: Conn PM, editor. Methods in enzymology. New York (NY): Elsevier; 1998. p. 300–318.
  • Zheng J, Zagotta WN. Gating rearrangements in cyclic nucleotide-gated channels revealed by patch-clamp fluorometry. Neuron. 2000;28(2):369–374.
  • Kusch J, Zifarelli G. Patch-clamp fluorometry: electrophysiology meets fluorescence. Biophys J. 2014;106(6):1250–1257.
  • Braak E, Griffing K, Arai K, et al. Neuropathology of Alzheimer’s disease: what is new since A. Alzheimer? Eur Arch Psychiatry Clin Neurosci. 1999;249(Suppl 3):14–22.
  • Reitz C, Mayeux R. Alzheimer disease: epidemiology, diagnostic criteria, risk factors and biomarkers. Biochem Pharmacol. 2014;88(4):640–651.
  • Grossberg GT, Tong G, Burke AD, et al. Present algorithms and future treatments for Alzheimer’s disease. J Alzheimers Dis. 2019;67(4):1157–1171.
  • Briggs R, Kennelly SP, O’Neill D. Drug treatments in Alzheimer’s disease. Clin Med (Lond). 2016;16(3):247–253.
  • Parodi J, Ochoa-de la Paz L, Miledi R, et al. Functional and structural effects of amyloid-β aggregate on Xenopus laevis oocytes. Mol Cells. 2012;34(4):349–355.
  • Morales A, Aleu J, Ivorra I, et al. Incorporation of reconstituted acetylcholine receptors from Torpedo into the Xenopus oocyte membrane. Proc Natl Acad Sci U S A. 1995;92(18):8468–8472.
  • Arbilla S, Depoortere H, George P, et al. Pharmacological profile of the imidazopyridine zolpidem at benzodiazepine receptors and electrocorticogram in rats. Naunyn-Schmiedeberg’s Arch Pharmacol. 1985;330(3):248–251.
  • Mazzo F, Zwart R, Serratto GM, et al. Reconstitution of synaptic Ion channels from rodent and human brain in Xenopus oocytes: a biochemical and electrophysiological characterization. J Neurochem. 2016;138(3):384–396.
  • Arispe N, Pollard HB, Rojas E. The ability of amyloid beta-protein [A beta P (1-40)] to form Ca2+ channels provides a mechanism for neuronal death in Alzheimer’s disease. Ann N Y Acad Sci. 1994;747:256–266.
  • Wang H-Y, Lee DHS, D’Andrea MR, et al. β-Amyloid1–42 binds to α7 nicotinic acetylcholine receptor with high affinity: implications for alzheimer’s disease pathology. J Biol Chem. 2000;275(8):5626–5632.
  • Yang T, Xiao T, Sun Q, et al. The current agonists and positive allosteric modulators of α7 nAChR for CNS indications in clinical trials. Acta Pharm Sin B. 2017;7(6):611–622.
  • Stokes C, Papke JKP, Horenstein NA, et al. The structural basis for GTS-21 selectivity between human and rat nicotinic α7 receptors. Mol Pharmacol. 2004;66(1):14–24.
  • Gault LM, Lenz RA, Ritchie CW, et al. ABT-126 monotherapy in mild-to-moderate Alzheimer’s dementia: randomized double-blind, placebo and active controlled adaptive trial and open-label extension. Alzheimers Res Ther. 2016;8(1):44.
  • Hauser TA, Kucinski A, Jordan KG, et al. TC-5619: an alpha7 neuronal nicotinic receptor-selective agonist that demonstrates efficacy in animal models of the positive and negative symptoms and cognitive dysfunction of schizophrenia. Biochem Pharmacol. 2009;78(7):803–812.
  • Weed MR, Polino J, Signor L, et al. Nicotinic alpha 7 receptor agonists EVP-6124 and BMS-933043, attenuate scopolamine-induced deficits in visuo-spatial paired associates learning. PloS One. 2017;12(12):e0187609–e09.
  • Callahan PM, Bertrand D, Bertrand S, et al. Tropisetron sensitizes α7 containing nicotinic receptors to low levels of acetylcholine in vitro and improves memory-related task performance in young and aged animals. Neuropharmacology. 2017;117:422–433.
  • Yu J, Zhu X, Zhang L, et al. Species specificity of rat and human α7 nicotinic acetylcholine receptors towards different classes of peptide and protein antagonists. Neuropharmacology. 2018;139:226–237.
  • Petrov D, Mansfield C, Moussy A, et al. ALS clinical trials review: 20 years of failure. Are we any closer to registering a new treatment? Front Aging Neurosci. 2017;9:68.
  • Cozzolino M, Ferri A, Teresa Carrì M. Amyotrophic lateral sclerosis: from current developments in the laboratory to clinical implications. Antioxid Redox Signal. 2007;10(3):405–444.
  • Loeffler J-P, Picchiarelli G, Dupuis L, et al. The role of skeletal muscle in amyotrophic lateral sclerosis. Brain Pathol. 2016;26(2):227–236.
  • Palma E, Inghilleri M, Conti L, et al. Physiological characterization of human muscle acetylcholine receptors from ALS patients. Proc Nat Acad Sci. 2011;108(50):20184–20188.
  • Clemente S. Amyotrophic lateral sclerosis treatment with ultramicronized palmitoylethanolamide: a case report. CNS Neurol Disord Drug Targets. 2012;11(7):933–936.
  • Palma E, Reyes-Ruiz JM, Lopergolo D, et al. Acetylcholine receptors from human muscle as pharmacological targets for ALS therapy. Proc Nat Acad Sci. 2016;113(11):3060–3065.
  • Darcq E, Kieffer BL. Opioid receptors: drivers to addiction? Nat Rev Neurosci. 2018;19(8):499–514.
  • Freitas ACN, Peigneur S, Macedo FHP, et al. The peptide PnPP-19, a spider toxin derivative, activates μ-opioid receptors and modulates calcium channels. Toxins (Basel). 2018;10(1):43.
  • Varagic Z, Ramerstorfer J, Huang S, et al. Subtype selectivity of α+ β− site ligands of GABAA receptors: identification of the first highly specific positive modulators at α6β2/3γ2 receptors. Br J Pharmacol. 2013;169(2):384–399.
  • Puppe A, Limmroth V. GABAergic drugs for the treatment of migraine. CNS & Neurol Disord Drug Targets. 2007;6(4):247–250.
  • Vasović D, Divović B, Treven M, et al. Trigeminal neuropathic pain development and maintenance in rats are suppressed by a positive modulator of α6 GABAA receptors. Eur J Pain. 2019;23(5):973–984.
  • Kambur O, Kaunisto MA, Winsvold BS, et al. Genetic variation in P2RX7 and pain tolerance. Pain. 2018;159(6):1064–1073.
  • Chessell IP, Hatcher JP, Bountra C, et al. Disruption of the P2X7 purinoceptor gene abolishes chronic inflammatory and neuropathic pain. Pain. 2005;114(3):386–396.
  • Marques-da-Silva C, Chaves MM, Castro NG, et al. Colchicine inhibits cationic dye uptake induced by ATP in P2X2 and P2X7 receptor-expressing cells: implications for its therapeutic action. Br J Pharmacol. 2011;163(5):912–926.
  • Okura D, Horishita T, Ueno S, et al. Lidocaine preferentially inhibits the function of purinergic P2X7 receptors expressed in xenopus oocytes. Anesthesia Analg. 2015;120(3):597–605.
  • Romero HK, Christensen SB, Di Cesare Mannelli L, et al. Inhibition of α9α10 nicotinic acetylcholine receptors prevents chemotherapy-induced neuropathic pain. Proc Nat Acad Sci. 2017;114(10):E1825–E32.
  • Hone AJ, Servent D, McIntosh JM. α9-containing nicotinic acetylcholine receptors and the modulation of pain. Br J Pharmacol. 2018;175(11):1915–1927.
  • Lafaire AV, Schwarz W. Voltage dependence of the rheogenic Na+/K+ ATPase in the membrane of oocytes of Xenopus laevis. J Membr Biol. 1986;91(1):43–51.
  • Wu M, Gerhart J. Chapter 1: Raising Xenopus in the laboratory. In: Kay BK, Peng HB, editors. Methods in cell biology: Xenopus laevis, Practical Uses in Cell and Molecular Biology, vol 36. San Diego (CA): Academic Press; 1991. p. 3–18.
  • Dascal N. The use of Xenopus oocytes for the study of ion channel. Crit Rev Biochem. 1987;22(4):317–387.
  • Papke RL, Porter Papke JK. Comparative pharmacology of rat and human alpha7 nAChR conducted with net charge analysis. Br J Pharmacol. 2002;137(1):49–61.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.