Detachment of surface membrane invagination systems by cationic amphiphilic drugs

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Osman, Sangar ^a   Taylor, Kirk A ^a,b   Allcock, Natalie ^a   Rainbow, Richard D ^a   Mahaut Smith, Martyn P ^a  

^a UNIVERSITY OF LEICESTER   (United Kingdom)

^b ANGLIA RUSKIN UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

1 [[6 (3 METHOXYESTRA 1,3,5(10) TRIEN 17BETA YL)AMINO]HEXYL] 2,5 PYRROLIDINEDIONE; 1-(6-((3-METHOXYESTRA-1,3,5(10)-TRIEN-17-YL)AMINO)HEXYL)-1H-PYRROLE-2,5-DIONE; 2 PYRROLIDONE DERIVATIVE; ESTRANE DERIVATIVE; N (6 AMINOHEXYL) 5 CHLORO 1 NAPHTHALENESULFONAMIDE; PHENOTHIAZINE DERIVATIVE; SULFONAMIDE;

ANIMAL; CARDIAC MUSCLE CELL; CELL CULTURE; CELL SURFACE; DRUG EFFECTS; MALE; MEGAKARYOCYTE; PHYSIOLOGY; PRECLINICAL STUDY; ULTRASTRUCTURE; WISTAR RAT;

ANIMALS; CELL SURFACE EXTENSIONS; CELLS, CULTURED; DRUG EVALUATION, PRECLINICAL; ESTRENES; MALE; MEGAKARYOCYTES; MYOCYTES, CARDIAC; PHENOTHIAZINES; PYRROLIDINONES; RATS, WISTAR; SULFONAMIDES;

EID: 84953280507     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep18536     Document Type: Article

References (70)

1. Fain, G. L., Hardie, R. & Laughlin, S. B. Phototransduction and the evolution of photoreceptors. Curr. Biol. 20, R114-124 (2010).
2. Hardie, R. C. & Juusola, M. Phototransduction in Drosophila. Curr. Opin. Neurobiol. 34, 37-45 (2015).
3. Mustafi, D., Engel, A. H. & Palczewski, K. Structure of cone photoreceptors. Prog. Retin. Eye Res. 28, 289-302 (2009).
4. Peachey, L. D. Electron Microscopic Observations on the Accumulation of Divalent Cations in Intramitochondrial Granules. J. Cell Biol. 20, 95-111 (1964).
5. Franzini-Armstrong, C., Landmesser, L. & Pilar, G. Size and shape of transverse tubule openings in frog twitch muscle fibers. J. Cell Biol. 64, 493-497 (1975).
6. Al-Qusairi, L. & Laporte, J. T-tubule biogenesis and triad formation in skeletal muscle and implication in human diseases. Skelet. Muscle 1, 26 (2011).
7. Stenger, R. J. & Spiro, D. The Ultrastructure of Mammalian Cardiac Muscle. J. Biophys. Biochem. Cytol. 9, 325-351 (1961).
8. Brette, F. & Orchard, C. T-tubule function in mammalian cardiac myocytes. Circ. Res. 92, 1182-1192 (2003).
9. Sipido, K. R. & Cheng, H. T-tubules and ryanodine receptor microdomains: On the road to translation. Cardiovasc. Res. 98, 159-161 (2013).
10. Guo, A., Zhang, C., Wei, S., Chen, B. & Song, L. S. Emerging mechanisms of T-tubule remodelling in heart failure. Cardiovasc. Res. 98, 204-215 (2013).
11. Ibrahim, M., Gorelik, J., Yacoub, M. H. & Terracciano, C. M. The structure and function of cardiac t-tubules in health and disease. Proc. Biol. Sci. 278, 2714-2723 (2011).
12. Lyon, A. R. et al. Loss of T-tubules and other changes to surface topography in ventricular myocytes from failing human and rat heart. Proc. Natl. Acad. Sci.USA 106, 6854-6859 (2009).
13. Machlus, K. R. & Italiano, J. E., Jr. The incredible journey: From megakaryocyte development to platelet formation. J. Cell Biol. 201, 785-796 (2013).
14. Yamada, E. The fine structure of the megakaryocyte in the mouse spleen. Acta Anat. 29, 267-290 (1957).
15. Behnke, O. An electron microscope study of the megacaryocyte of the rat bone marrow. I. The development of the demarcation membrane system and the platelet surface coat. J. Ultrastruct. Res. 24, 412-433 (1968).
16. Han, S. S. & Baker, B. L. The Ultrastructure of Megakaryocytes and Blood Platelets in the Rat Spleen. Anat. Rec. 149, 251-267 (1964).
17. Schulze, H. et al. Characterization of the megakaryocyte demarcation membrane system and its role in thrombopoiesis. Blood 107, 3868-3875 (2006).
18. Grozovsky, R., Hoffmeister, K. M. & Falet, H. Novel clearance mechanisms of platelets. Curr. Opin. Hematol. 17, 585-589 (2010).
19. Poujol, C., Ware, J., Nieswandt, B., Nurden, A. T. & Nurden, P. Absence of GPIb? is responsible for aberrant membrane development during megakaryocyte maturation: Ultrastructural study using a transgenic model. Exp. Hematol. 30, 352-360 (2002).
20. Ware, J., Russell, S. & Ruggeri, Z. M. Generation and rescue of a murine model of platelet dysfunction: The Bernard-Soulier syndrome. Proc. Natl. Acad. Sci. USA 97, 2803-2808 (2000).
21. Escolar, G., Leistikow, E. & White, J. G. The fate of the open canalicular system in surface and suspension-activated platelets. Blood 74, 1983-1988 (1989).
22. White, J. G. & Clawson, C. C. The surface-connected canalicular system of blood platelets-a fenestrated membrane system. Am. J. Pathol. 101, 353-364 (1980).
23. Thon, J. N. & Italiano, J. E. Platelets: Production, morphology and ultrastructure. Handb. Exp. Pharmacol. 3-22 (2012).
24. Eckly, A. et al. Characterization of megakaryocyte development in the native bone marrow environment. Meth. Mol. Biol. 788, 175-192 (2012).
25. Mahaut-Smith, M. P. et al. Properties of the demarcation membrane system in living rat megakaryocytes. Biophys. J. 84, 2646-2654 (2003).
26. Gardiner, E. E., Arthur, J. F., Kahn, M. L., Berndt, M. C. & Andrews, R. K. Regulation of platelet membrane levels of glycoprotein VI by a platelet-derived metalloproteinase. Blood 104, 3611-3617 (2004).
27. Gardiner, E. E. et al. Controlled shedding of platelet glycoprotein (GP)VI and GPIb-IX-V by ADAM family metalloproteinases. J. Thromb. Haemost. 5, 1530-1537 (2007).
28. Mahaut-Smith, M. P. Patch-clamp recordings of electrophysiological events in the platelet and megakaryocyte. Meth. Mol. Biol. 273, 277-300 (2004).
29. Papayannopoulou, T., Nakamoto, B., Yokochi, T., Chait, A. & Kannagi, R. Human erythroleukemia cell line (HEL) undergoes a drastic macrophage-like shift with TPA. Blood 62, 832-845 (1983).
30. Balon, R., Berchou, R. & Zethelius, M. Thrombocytopenia associated with chlorpromazine, haloperidol and thiothixene: A case report. Can. J. Psychiatry. 32, 149-150 (1987).
31. Holt, R. J. Neuroleptic drug-induced changes in platelet levels. J. Clin. Psychopharmacol. 4, 130-132 (1984).
32. Shawver, J. R. & Tarnowski, S. M. Thrombocytopenia in prolonged chlorpromazine therapy. Am. J. Psychiatry 116, 845-846 (1960).
33. Sheetz, M. P. & Singer, S. J. Biological membranes as bilayer couples. A molecular mechanism of drug-erythrocyte interactions. Proc. Natl. Acad. Sci. USA 71, 4457-4461 (1974).
34. Sheetz, M. P., Painter, R. G. & Singer, S. J. Biological membranes as bilayer couples. III. Compensatory shape changes induced in membranes. J. Cell Biol. 70, 193-203 (1976).
35. Bleasdale, J. E. et al. Selective inhibition of receptor-coupled phospholipase C-dependent processes in human platelets and polymorphonuclear neutrophils. J. Pharmacol. Exp. Ther. 255, 756-768 (1990).
36. Soeller, C. & Cannell, M. B. Examination of the transverse tubular system in living cardiac rat myocytes by 2-photon microscopy and digital image-processing techniques. Circ. Res. 84, 266-275 (1999).
37. Han, R., Grounds, M. D. & Bakker, A. J. Measurement of sub-membrane [Ca2+] in adult myofibers and cytosolic [Ca2+] in myotubes from normal and mdx mice using the Ca2+ indicator FFP-18. Cell Calcium 40, 299-307 (2006).
38. Halliwell, W. H. Cationic amphiphilic drug-induced phospholipidosis. Toxicol. Pathol. 25, 53-60 (1997).
39. McLaughlin, S., Wang, J., Gambhir, A. & Murray, D. PIP2 and proteins: Interactions, organization, and information flow. Annu. Rev. Biophys. Biomol. Struct. 31, 151-175 (2002).
40. Suetsugu, S., Kurisu, S. & Takenawa, T. Dynamic shaping of cellular membranes by phospholipids and membrane-deforming proteins. Physiol. Rev. 94, 1219-1248 (2014).
41. Yin, H. L. & Janmey, P. A. Phosphoinositide regulation of the actin cytoskeleton. Annu. Rev. Physiol. 65, 761-789 (2003).
42. Frost, A., Unger, V. M. & De Camilli, P. The BAR domain superfamily: Membrane-molding macromolecules. Cell 137, 191-196 (2009).
43. McMahon, H. T. & Boucrot, E. Membrane curvature at a glance. J. Cell Sci. 128, 1065-1070 (2015).
44. Lee, E. et al. Amphiphysin 2 (Bin1) and T-tubule biogenesis in muscle. Science 297, 1193-1196 (2002).
45. Caldwell, J. L. et al. Dependence of cardiac transverse tubules on the BAR domain protein amphiphysin II (BIN-1). Circ. Res. 115, 986-996 (2014).
46. Begonja, A. et al. FlnA binding to PACSIN2 F-BAR domain regulates membrane tubulation in megakaryocytes and platelets. Blood 126, 80-88 (2015).
47. Chen, Y. et al. Loss of the F-BAR protein CIP4 reduces platelet production by impairing membrane-cytoskeleton remodeling. Blood 122, 1695-1706 (2013).
48. Patel-Hett, S. et al. The spectrin-based membrane skeleton stabilizes mouse megakaryocyte membrane systems and is essential for proplatelet and platelet formation. Blood 118, 1641-1652 (2011).
49. Fugier, C. et al. Misregulated alternative splicing of BIN1 is associated with T tubule alterations and muscle weakness in myotonic dystrophy. Nat. Med. 17, 720-725 (2011).
50. Evans, N. J. & Walker, J. W. Endothelin-1 mobilizes profilin-1-bound PIP2 in cardiac muscle. Exp. Biol. Med. 231, 882-887 (2006).
51. Singh, N. et al. PIP2 Modulates T-Tubule remodeling during heart failure by working as a binding substrate for BIN1. Biophys. J. 106, 447a-447a (2014).
52. Hong, T. et al. Cardiac BIN1 folds T-tubule membrane, controlling ion flux and limiting arrhythmia. Nat. Med. 20, 624-632 (2014).
53. Hong, T. T. et al. BIN1 localizes the L-type calcium channel to cardiac T-tubules. PLoS Biol. 8, e1000312 (2010).
54. Strange, P. G. Mechanisms of action of anti-psychotic drugs. Biochem. Soc. Trans. 27, 175-178 (1999).
55. Giardina, E. G., Bigger, J. T., Jr, Glassman, A. H., Perel, J. M. & Kantor, S. J. The electrocardiographic and antiarrhythmic effects of imipramine hydrochloride at therapeutic plasma concentrations. Circulation 60, 1045-1052 (1979).
56. Lucas, C. M. et al. Imipramine induced heart failure in the dog: A model to study the effect of cardiac assist devices. Cardiovasc. Res. 26, 804-809 (1992).
57. Hoehns, J. D. et al. Torsades de pointes associated with chlorpromazine: Case report and review of associated ventricular arrhythmias. Pharmacotherapy 21, 871-883 (2001).
58. Reilly, J. G., Ayis, S. A., Ferrier, I. N., Jones, S. J. & Thomas, S. H. QTc-interval abnormalities and psychotropic drug therapy in psychiatric patients. Lancet 355, 1048-1052 (2000).
59. Cohen, B. M., Lipinski, J. F., Harris, P. Q., Pope, H. G., Jr. & Friedman, M. Clinical use of the radioreceptor assay for neuroleptics. Psychiatry Res. 2, 173-178 (1980).
60. Liu, X. & De Haan, S. Chlorpromazine dose for people with schizophrenia. Cochrane Database Syst. Rev. CD007778 (2009).
61. Guth, P. S. & Spirtes, M. A. The Phenothiazinetranquilizers: Biochemical and Biophysical Actions. Int. Rev. Neurobiol. 7, 231-278 (1964).
62. Sunderland, T. & Cohen, B. M. Blood to brain distribution of neuroleptics. Psychiatry Res. 20, 299-305 (1987).
63. Suh, B. C. & Hille, B. PIP2 is a necessary cofactor for ion channel function: How and why? Annu. Rev. Biophys. 37, 175-195 (2008).
64. Anishkin, A., Loukin, S. H., Teng, J. & Kung, C. Feeling the hidden mechanical forces in lipid bilayer is an original sense. Proc. Natl. Acad. Sci. USA 111, 7898-7905 (2014).
65. Hansen, S. B. Lipid agonism: The PIP paradigm of ligand-gated ion channels. Biochim. Biophys. Acta 1851, 620-628 (2015).
66. Sanchez, A., Hallam, T. J. & Rink, T. J. Trifluoperazine and chlorpromazine block secretion from human platelets evoked at basal cytoplasmic free calcium by activators of C-kinase. FEBS Lett. 164, 43-46 (1983).
67. Suda, J. & Aoki, N. Inhibition of platelet function by a calmodulin interacting agent, W-7. Thromb. Res. 21, 447-455 (1981).
68. Nishikawa, M., Tanaka, T. & Hidaka, H. Ca2+-calmodulin-dependent phosphorylation and platelet secretion. Nature 287, 863-865 (1980).
69. Sims, M. W. et al. PKC-mediated toxicity of elevated glucose concentration on cardiomyocyte function. Am. J. Physiol. Heart Circ. Physiol. 307, H587-597 (2014).
70. Rolf, M. G., Brearley, C. A. & Mahaut-Smith, M. P. Platelet shape change evoked by selective activation of P2X1 purinoceptors with ? ,?-methylene ATP. Thromb. Haemost. 85, 303-308 (2001).