Vacuolation in T-tubules as a model for tubular-vesicular transformations in biomembrane systems

Cell Biology International

Volumn 26, Issue 10, 2002, Pages 893-904

  Krolenko, Sergei A ^a   Lucy, Jack A ^b  

^a INSTITUTE OF CYTOLOGY   (Russian Federation)

^b ROYAL FREE AND UNIVERSITY COLLEGE MEDICAL SCHOOL   (United Kingdom)

Author keywords

Reversible vacuolation; Skeletal muscle; T system; T tubules; Tubular vesicular transformations

Indexed keywords

CAVEOLIN 3; CELL MEMBRANE PROTEIN; HYPOTONIC SOLUTION;

ACID SECRETION; ANIMAL CELL; CAVEOLA; CELL CULTURE; CELL MEMBRANE; CELL MEMBRANE TRANSPORT; CELL TYPE; CELL VACUOLE; CYTOSKELETON; ENDOCYTOSIS; ENDOPLASMIC RETICULUM; ENDOSOME; ENDOTHELIUM CELL; ERYTHROCYTE; GOLGI COMPLEX; LYSOSOME; MICROSCOPY; MICROTUBULE; MUSCLE FIBER CONTRACTION; NERVE CELL; NONHUMAN; PHOSPHOLIPID MEMBRANE; REVIEW; SKELETAL MUSCLE; TRANSVERSE TUBULAR SYSTEM; ANIMAL; BIOLOGICAL MODEL; CELL ORGANELLE; COMPARATIVE STUDY; CYTOPLASM VESICLE; HUMAN; INTRACELLULAR MEMBRANE; METABOLISM; MUSCLE CELL; ULTRASTRUCTURE;

ANIMALS; CELL MEMBRANE; CYTOPLASMIC VESICLES; HUMANS; INTRACELLULAR MEMBRANES; MODELS, BIOLOGICAL; MUSCLE CELLS; MUSCLE, SKELETAL; ORGANELLES; VACUOLES;

EID: 0036434874     PISSN: 10656995     EISSN: None     Source Type: Journal    
DOI: 10.1006/cbir.2002.0945     Document Type: Article

References (64)

1. Ayala J, 1994. Transport and internal organization of membranes: Vesicles, membrane networks and GTP-binding proteins. J Cell Sci 107: 753-763.
2. Bar-Ziv R, Tlusty T, Moses E, Safran SA, Bershadsky A, 1999. Pearling in cells: A clue to understanding cell shape. Proc Natl Acad Sci USA 96: 10140-10145.
3. Bendayan M, Gisiger V, 2001. Demonstration of acetylcholinesterase molecular forms in a continuous tubular lysosomal system of rat pancreatic acinar cells. J Histochem Cytochem 49: 29-39.
4. Bendayan M, Rasio A, 1997. Evidence of a tubular system for transendothelial transport in arterial capillaries of the rete mirabile. J Histochem Cytochem 45: 1365-1378.
5. Berk DA, Hochmuth RM, 1992. Lateral mobility of integral proteins in red blood cell tethers. Biophys J 61: 9-18.
6. Blum R, Stephens DJ, Schulz I, 2000. Lumen targeted GFP, used as a marker of soluble cargo, visualizes rapid ERGIC to Golgi traffic by a tubular vesicular network. J Cell Sci 113: 3151-3159.
7. Carozzi AJ, Ikonen E, Lindsay MR, Parton RG, 2000. Role of cholesterol in developing T-tubules: Analgous mechanisms for T-tubules and caveolae biogenesis. Traffic 1: 326-341.
8. Cluett EB, Wood SA, Banta M, Brown WJ, 1993. Tubulation of Golgi membranes in vivo and in vitro in the absence of brefeldin A. J Cell Biol 120: 273-285.
9. De Figueiredo P, Brown WJ, 1995. A role for calmodulin in organelle membrane tubulation. Mol Biol Cell 6: 871-887.
10. Dvorak AM, Feng D, 2001. The vesiclo-vacuolar organelle (VVO): A new endothelial cell permeability organelle. J Histochem Cytochem 49: 419-432.
11. Evans E, Needham D, 1987. Physical properties of surfactant bilayer membranes: Thermal transitions, elasticity, rigidity, cohesion, and colloidal interactions. J Phys Chem 91: 4219-4228.
12. Franzini-Armstrong C, 1994. The sarcoplasmic reticulum and the transverse tubules. In: Engel AS, Franzini-Armstrong C, eds. Myology (2nd Ed.). New York, McGraw-Hill Inc. 176-199.
13. Franzini-Armstrong C, 1996. Functional significance of membrane architecture in skeletal and cardiac muscle. Soc Gen Physiologist 49: 3-18.
14. Fuchs H, Gessner R, Tauber, Ghosh R, 1995. Functional reconstitution of the human placental transferrin receptor into phospholipid bilayers leads to long tubular structures proceeding from the vesicle surface. Biochemistry 34: 6196-6207.
15. Gabriel D, Hacker U, Köhler J, Müller-Taubenberger A, Schwartz J-M, Westphal M, Gerisch G, 1999. The contractile network of Dictyostelium as a distinct organelle: Its dynamics visualized by GFP marker protein. J Cell Sci 112: 3995-4995.
16. Galbiati F, Engelman JA, Volonte D, Zhang XL, Minetti C, Li M, Hou H, Kneitz B, Edelmann W, Lisanti MP, 2001. Caveolin-3 null mice show a loss of caveolae, changes in the microdomain distribution of the dystrophin-glycoprotein complex, and T-tubule abnormalities. J Biol Chem 276: 21425-21433.
17. Gibson A, Futter CE, Maxwell EH, Allchin EH, Shipman M, Kraehenbuhl J-P, Domingo D, Odorizzo G, Trowbridge IS, Hopkins CR, 1998. Sorting mechanisms regulating membrane protein traffic in the apical transcytotic pathway of polarized MDCK cells. J Cell Biol 143: 81-94.
18. Heinrich V, Božič B, Svetina S, Zekš B, 1999. Vesicle deformation by an axial load: From elongated shapes to tethered vesicles. Biophys J 76: 2056-2071.
19. Herring TL, Juranka P, McNally J, Lesiuk H, Morris CF, 2000. The spectrin skeleton of newly-invaginated plasma membrane. J Muscle Res Cell Motil 21: 67-77.
20. Heuser J, Zhu Q, Clarke M, 1993. Proton pumps populate the contractile vacuoles of Dictyostelium amoebae. J Cell Biol 121: 1311-1327.
21. Ho̧oper NM, 1999. Detergent-insoluble glycosphingolpid/cholesterol-rich membrane domains, lipid rafts and caveolae. Molec Membr Biol 16: 145-156.
22. Hopkins CR, Gibson A, Shipman M, Miller K, 1990. Movement of internalized ligand receptor complexes along a continuous endosomal reticulum. Nature 346: 335-339.
23. Hopkins CR, Gibson A, Shipman M, Strickland DK, Trowbridge IS, 1994. In migrating fibroblasts, recycling receptors are concentrated in narrow tubules in the pericentriolar area, and then routed to the plasma membrane of the leading lamella. J Cell Biol 125: 1265-1274.
24. Ishida M, Fok AK, Aihara S, Allen RD, 1996. Hyperosmotic stress leads to reversible dissociation of proton pump-bearing tubules from the contractile vacuole complex in Paramecium. J Cell Sci 109: 229-237.
25. Kano F, Sako Y, Tagaya M, Yanagida T, Murata M, 2000. Reconstitution of brefeldin A-induced Golgi tubulation and fusion with the endoplasmic reticulum in semi-intact chinese hamster ovary cells. Mol Biol Cell 11: 3073-3081.
26. Khan KN, Skepper JN, Hockaday AR, Burgess AJ, Huang CL-H, 2000. Loop diuretics inhibit detubulation and vacuolation in amphibian muscle fibers exposed to osmotic shock. J Muscle Res Cell Motil 21: 79-90.
27. Kleijmeer M, Ramm G, Schuurhuis D, Griffith J, Rescigno M, Ricciardi-Castagnoli P, Rudensky AY, Ossendorp F, Melief CJM, Stoorvogel W, Geuze HJ, 2001. Reorganization of multivesicular bodies regulates MHC class II antigen presentation by dendritic cells. J Cell Biol 155: 53-63.
28. Krolenko SA, Adamyan SY, 2000. Stereological analysis of the T-system vacuolation in frog muscle fibre revealed by confocal fluorescence microscopy. Tsitologiya 42: 1125-1133 (in Russian).
29. Krolenko SA, Lucy JA, 2001. Reversible vacuolation of T-tubules in skeletal muscle: Mechanisms and implications for cell biology. Int Rev Cytol 202: 243-298.
30. Krolenko SA, Adamyan SY, Lucy JA, 1997. Functional role of vacuolation in the T-system of skeletal muscle. Tsitologiya 39: 878-888 (in Russian).
31. Krolenko SA, Amos WB, Brown SC, Tarunina MV, Lucy JA, 1998. Accessibility of T-tubule vacuoles to extracellular dextran and DNA: Mechanism and potential application of vacuolation. J Muscle Res Cell Motil 19: 603-611.
32. Lännergren J, Bruton JD, Westerblad H, 1999. Vacuole formation in fatigued muscle fibres from frog and mouse. J Muscle Res Cell Motil 20: 19-32.
33. 2+] abolishes excitation-contraction coupling in skeletal muscle fibres of rat and toad. J Physiol 489: 349-362.
34. Leverrier Y, Ridley AJ, 2001. Apoptosis: Caspases orchestrate the ROCK 'n' bleb. Nature Cell Biology 3: E91-E93.
35. Lew VL, Hockaday A, Freeman CJ, Bookchin RM, 1988. Mechanism of spontaneous inside-out vesiculation of red cell membranes. J Cell Biol 106: 1893-1901.
36. Libelius R, Jirmanova I, Lundquist I, Thesleff S, Barnard EA, 1979. T-tubule endocytosis in dystrophic chicken muscle and its relation to muscle fiber degeneration. Acta Neuropathol 48: 31-38.
37. Marks B, Stowell MHB, Vallis Y, Mills IG, Gibson A, Hopkins CR, McMahon HT, 2001. GTPase activity of dynamin and resulting comformational change are essential for endocytosis. Nature 410: 231-235.
38. Marsh BJ, Mastronarde DN, Buttle KF, Kathryn E, Howell KE, McIntosh JR, 2001. Organellar relationships in the Golgi region of the pancreatic beta cell line, HIT-T15, visualized by high resolution electron tomography. Proc Natl Acad Sci USA 98: 2399-2406.
39. Mathivet L, Cribier S, Devaux PF, 1996. Shape change and physical properties of giant phospholipid vesicles prepared in the presence of an AC electric field. Biophys J 70: 1112-1121.
40. Mills LR, Morris CE, 1998. Neuronal plasma membrane dynamics evoked by osmomechanical perturbations. J Membr Biol 166: 223-235.
41. Mironov AA, Weidman P, Luini A, 1997. Variations of intracellular transport theme: Maturating cisternae and trafficking tubules. J Cell Biol 138: 481-484.
42. Morris CE, Homann U, 2001. Cell surface area regulation and membrane tension. J Membr Biol 179: 79-102.
43. Mui BL-S, Döbereiner H-G, Madden TD, Cullis PR, 1995. Influence of transbilayer area asymmetry on the morphology of large unilamellar vesicles. Biophys J 69: 930-941.
44. Mukherjee S, Soe TT, Maxfield FR, 1999. Endocytic sorting of lipid analogues differing solely in the chemistry of their hydrophobic tails. J Cell Biol 144: 1271-1284.
45. Müller O, Sattler T, Flotenmeyer M, Schwartz H, Plattner H, Mayer A, 2000. Autophagic tubules: Vacuolar invaginations involved in lateral membrane sorting and inverse vesicle budding. J Cell Biol 151: 519-528.
46. Muñoz P, Rosemblatt M, Testar X, Palacin M, Thoidis G, Pilch PF, Zorzano A, 1995. The T-tubule is a cell-surface target for insulin-regulated recycling of membrane proteins in skeletal muscle. Biochem J 312: 393-400.
47. Nik-Zainal S, Skepper JN, Hockaday A, Huang CL-H, 1999. Cardiac glycosides inhibit detubulation in amphibian skeletal muscle fibers exposed to osmotic shock. J Muscle Res Cell Motil 20: 45-53.
48. Parton RG, Carrozzi A, Gustavson J, 2000. Caves and labyrinths: Caveolae and transverse tubules in skeletal muscle. Protoplasma 212: 15-23.
49. Pelham HR, Rothman JE, 2000. The debate about transport in the Golgi - Two side of the same coin. Cell 102: 713-719.
50. Pettitt JM, Drier Van IR, Toh B-H, Gleeson PA, 1996. From coiled tubules to a secretory canaliculus: A new model for membrane transformation and acid secretion by gastric parietal cells. Trends Cell Biol 6: 49-53.
51. Rahkila P, Takala TES, Parton RG, Metsikkö K, 2001. Protein targeting to the plasma membrane of adult skeletal muscle fibre: An organized mosaic of functional domains. Exp Cell Res 267: 61-72.
52. Reuzeau C, Mills LR, Harris ZA, Morris CE 1995. Discrete and reversible vacuole-like dilations induced by osmomechanical peturbation of neurons. J Membr Biol 145: 33-37.
53. Rosemblatt M, Hidalgo C, Vergara C, 1981. Immunological and biochemical properties of transverse tubule membrane isolated from rabbit skeletal muscle. J Biol Chem 256: 8140-8148.
54. Roux A, Cappello G, Cartaud J, Prost J, Goud B, Bassereau P, 2002. A minimal system allowing tabulation with molecular motors pulling on giant liposomes. Proc Nat Acad Sci USA 99: 5394-5399.
55. Sackmann E, 1994. Membrane bending energy concept of vesicle- and cell-shapes and shape-transitions. Febs Lett 346: 3-16.
56. Schmidt A, Hannah MJ, Hutter WB, 1997. Synaptic-like microvesicles of neuroendocrine cells originate from a novel compartment that is continuous with the plasma membrane and devoid of transferrin receptor. J Cell Biol 137: 445-458.
57. Sciaky N, Presley J, Smith C, Zaal KJM, Cole N, Moreira JE, Terasaki M, Siggia E, Lippincott-Schwartz J, 1997. Golgi tubule traffic and the effects of brefeldin A visualized in living cells. J Cell Biol 139: 1137-1155.
58. Snigirevskaya ES, 1983. A comparative analysis of the vacuolar system of the frog urinary bladder granular cells and the protozoan contractile vacuole complex. Tsitologiya 25: 889-895 (in Russian).
59. Tani T, Allen RD, Naitoh Y, 2001. Cellular membranes that undergo cyclic changes in tension: Direct measurement of force generation by an in vitro contractile vacuole of Paramecium multimicronucleatum. J Cell Sci 114: 785-795.
60. Tooze J, Hollinshead M, 1991. Tubular early endosomal networks in AtT20 and other cells. J Cell Biol 115: 635-653.
61. Torgerson RR, McNiven MA, 1998. The actin-myosin cytoskeleton mediates reversible agonist induced membrane blebbing. J Cell Sci 111: 2911-2922.
62. Volchuk A, Amherdt M, Ravazzola M, Brügger B, Rivera VM, Clackson N, Perrelet A, Söllner TH, Rothman JE, Orci L, 2000. Megavesicles implicated in the rapid transport of intracisternal aggregates across the Golgi stack. Cell 102: 335-348.
63. Wood SA, Brown WJ, 1992. The morphology but not the function of endosomes and lysosomes is altered by brefeldin A. J Cell Biol 119: 273-285.
64. Zhang M, Dwyer NK, Love DC, Cooney A, Comly M, Neufeld E, Pentchev PG, Blanchette-Mackie EJ, Hanover JA, 2001. Cessation of rapid late endosomal tubulovesicular trafficking in Niemann-Pick type C1 disease. Proc Nat Acad Sci USA 98: 4466-4471.