Permeability of Membranes

  • Gaspar BanfalviEmail author


This chapter provides an overview of bilayer permeability and selectivity of permeabilization. Based on the hydrophobic nature of the lipid bilayer, cell membranes behave as diffusion barriers primarily for electrolytes, hydrophilic micro- and macromolecules in solutions. To overcome the permeability barrier different transport processes have been evolved for crossing the cell membrane. Small particles may be transported by passive transport, active transport or by carriers. To transport large particles through the membrane different strategies have been developed involving exocytosis, endocytosis and receptor mediated endocytosis. The importance of permeability is underlined by the integrity of cell membrane in maintaining the viability of cells. Different approaches have been applied to investigate membrane permeability as a measure of viability, by detecting permeability on account of hemolysis, turbidimetry and release of lactate dehydrogenase.


ABC transporter Active pumps Active transport Adhesion α-Helix Bacterial membranes ß-Barrel Channel proteins Chloroplast membranes Cytotoxicity assay Diffusion Electrochemical gradient Facilitated diffusion Filtration F1F0 ATPase Hemolysis Hydrophilic Hydrophobic Ion channels Ionophores Ligand-gated channels Lipid bilayer Membrane transport Organellar transport Osmosis Overton’s rule Passive transport Penetration Permeability Pore formation Protein targeting Receptors Selectivity Semipermeability Signaling Solubility Transition temperature Transmembrane proteins Transporter Vesicular transport Voltage-gated channels Water channels 


  1. Aeschbacher M, Reinhardt CA, Zbinden G (1986) A rapid cell membrane permeability test using fluorescent dyes and flow cytometry. Cell Biol Toxicol 2:247–255PubMedCrossRefGoogle Scholar
  2. Agre P (2006) The aquaporin water channels. Proc Am Thorac Soc 3:5–13PubMedCentralPubMedCrossRefGoogle Scholar
  3. Alberti KGMM, Bartley W (1963) The production of amino acids by cell fractions, particularly rat-liver mitochondria. Biochem J 87:104–114PubMedCentralPubMedCrossRefGoogle Scholar
  4. Babior BM (1999) NADPH oxidase: an update. Blood 93:1464–1476PubMedGoogle Scholar
  5. Baerends RJS, Faber KN, Kram AM, Kiel JAKW, Van Der Klei IJ, Veenhuis M (2000) A stretch of positively charged amino acids at the N terminals of Hansenula polymorpha Pex3p is involved in incorporation of the protein into the peroxisomal membrane. J Biol Chem 275:9986–9995PubMedCrossRefGoogle Scholar
  6. Banfalvi G (2009) Apoptotoc chromatin changes. Springer, Dordrecht, pp 269–273Google Scholar
  7. Banfalvi G (2014) Homeostasis – tumor – metastasis. Spinger, Dordrecht, p 28, p 30CrossRefGoogle Scholar
  8. Banfalvi G, Sarkar N (1983) Analysis of the 5′-termini of nascent DNA chains synthesized in permeable cells of Bacillus subtilis. J Mol Biol 163:147–169PubMedCrossRefGoogle Scholar
  9. Banfalvi G, Sooki-Toth A, Sarkar N, Csuzi S, Antoni F (1984) Nascent DNA chains synthesized in recersibly permeable cells of mouse thymocytes. Eur J Biochem 139:553–559PubMedCrossRefGoogle Scholar
  10. Banfield DK (2011) Mechanisms of protein retention in the Golgi. Cold Spring Harb Perspect Biol 3, 005264CrossRefGoogle Scholar
  11. Bӓrlund H (1929) Permeabilitatsstudien an Epidermiszellen von Rhoeo discolor. Acta Bot Fenn 5:1–117Google Scholar
  12. Baumgart J, Bintig W, Ngezahayo A, Willenbrock S, Murua Escobar H, Ertmer W, Lubatschowski H, Heisterkamp A (2008) Quantified femtosecond laser based opto-perforation of living GFSHR-17 and MTH53 a cells. Opt Express 16:3021–3031PubMedCrossRefGoogle Scholar
  13. Becker T, Böttinger L, Pfanner N (2012) Mitochondrial protein import: from transport pathways to an integrated network. Trends Biochem Sci 37:85–91PubMedCrossRefGoogle Scholar
  14. Berger NA, Johnson ES (1976) DNA synthesis in permeabilized mouse L cells. Biochim Biophys Acta 425:1–17PubMedCrossRefGoogle Scholar
  15. Blattner FR, Plunkett G 3rd, Bloch CA, Perna NT, Burland V, Riley M, Collado-Vides J, Glasner JD, Rode CK, Mayhew GF, Gregor J, Davis NW, Kirkpatrick HA, Goeden MA, Rose DJ, Mau B, Shao Y (1997) The complete genome sequence of Escherichia coli. Science 277:1453–1474PubMedCrossRefGoogle Scholar
  16. Bolender N, Sickmann A, Wagner R, Meisinger C, Pfanner N (2008) Multiple pathways for sorting mitochondrial precursor proteins. EMBO J 9:42–49CrossRefGoogle Scholar
  17. Brix J, Pfanner N (1997) Differential recognition of preproteins by the purified cytosolic domains of the mitochondrial import receptors Tom20, Tom22, and Tom70. J Biol Chem 272:20730–20735PubMedCrossRefGoogle Scholar
  18. Cammann K (1985) Ion-selective bulk membranes as models. Top Curr Chem 128:219–258CrossRefGoogle Scholar
  19. Cartier N, Hacein-Bey-Abina S, Bartholomae CC, Veres G, Schmidt M, Kutschera I, Vidaud M, Abel U, Dal-Cortivo L, Caccavelli L, Mahlaoui N, Kiermer V, Mittelstaedt D, Bellesme C, Lahlou N, Lefrère F, Blanche S, Audit M, Payen E, Leboulch P, l’Homme B, Bougnères P, Von Kalle C, Fischer A, Cavazzana-Calvo M, Aubourg P (2009) Hematopoietic stem cell gene therapy with a lentiviral vector in X-linked adrenoleukodystrophy. Science 326:818–823PubMedCrossRefGoogle Scholar
  20. Castro A, Ros J, Jiménez W, Clària J, Llibre J, Leivas A, Arroyo V, Rivera F, Rodés J (1994) Intracellular calcium concentration in vascular smooth muscle cells of rats with cirrhosis. J Hepatol 21:521–526PubMedCrossRefGoogle Scholar
  21. Catterall WA (2011) Voltage-gated calcium channels. Cold Spring Harb Perspect Biol 3(8):a003947PubMedCentralPubMedCrossRefGoogle Scholar
  22. Cavazzana-Calvo M, Hacein-Bey S, Basile G, Gross F, Yvon E, Nusbaum P, Selz F, Hue C, Certain S, Casanova J-L, Bousso P, Le Deist F, Fischer A (2000) Gene therapy of human severe combined immunodeficiency (SCID)-X1 disease. Science 288:669–672PubMedCrossRefGoogle Scholar
  23. Cavazzana-Calvo M, Payen E, Negre O, Wang G, Hehir K, Fusil F, Down J, Denaro M, Brady T, Westerman K, Cavallesco R, Gillet-Legrand B, Caccavelli L, Sgarra R, Maouche-Chrétien L, Bernaudin F, Girot R, Dorazio R, Mulder GJ, Polack A, Bank A, Soulier J, Larghero J, Kabbara N, Dalle B, Gourmel B, Socie G, Chrétien S, Cartier N, Aubourg P, Fischer A, Cornetta K, Galacteros F, Beuzard Y, Gluckman E, Bushman F, Hacein-Bey-Abina S, Leboulch P (2010) Transfusion independence and HMGA2 activation after gene therapy of human β-thalassaemia. Nature 467:318–322PubMedCentralPubMedCrossRefGoogle Scholar
  24. Cherny VV, Markin VS, DeCoursey TE (1995) The voltage-gated ion conductance in rat alveolar epithelial cells is determined by the pH gradient. J Gen Physiol 105:861–896PubMedCrossRefGoogle Scholar
  25. Choi CH (2005) ABC transporters as multidrug resistance mechanisms and the development of chemosensitizers for their reversal. Cancer Cell Int 5:30PubMedCentralPubMedCrossRefGoogle Scholar
  26. Dalbey RE, Wang P, Kuhn A (2011) Assembly of bacterial inner membrane proteins. Annu Rev Biochem 80:161–187PubMedCrossRefGoogle Scholar
  27. Darnell J, Lodish H, Baltimore D (eds) (1986) Molecular cell biology. Scientific American Books, New York, pp 625–632Google Scholar
  28. Dascher C, Matteson J, Balch WE (1994) Syntaxin 5 regulates endoplasmic reticulum to Golgi transport. J Biol Chem 269:29363–29366PubMedGoogle Scholar
  29. Davis AA, Farrar MJ, Nishimura N, Jin MM, Schaffer CB (2013) Optoporation and genetic manipulation of cells using femtosecond laser pulses. Biophys J 105:862–871PubMedCentralPubMedCrossRefGoogle Scholar
  30. DeCoursey TE, Cherny VV (1994) Na+-H+ antiport detected through hydrogen ion currents in rat alveolar epithelial cells and human neutrophils. J Gen Physiol 103:755–785PubMedCrossRefGoogle Scholar
  31. Dhakal K, Black B, Mohanty S (2014) Introduction of impermeable actin-staining molecules to mammalian cells by optoporation. Sci Rep 4:6553PubMedCentralPubMedCrossRefGoogle Scholar
  32. Djukic M, Munz M, Sörgel F, Holzgrabe U, Eiffert H, Nau R (2012) Overton’s rule helps to estimate the penetration of anti-infectives into patients’ cerebrospinal fluid. Antimicrob Agents Chemother 56:979–988PubMedCentralPubMedCrossRefGoogle Scholar
  33. Dolci A, Panteghini M (2014) Harmonization of automated hemolysis index assessment and use: is it possible? Clin Chim Acta 432:38–43PubMedCrossRefGoogle Scholar
  34. Dolezal P, Likic V, Tachezy J, Lithgow T (2006) Evolution of the molecular machines for protein import into mitochondria. Science 313:314–318PubMedCrossRefGoogle Scholar
  35. Dudek J, Rehling P, van der Laan M (2013) Mitochondrial protein import: common principles and physiological networks. Biochim Biophys Acta 1833:274–285PubMedCrossRefGoogle Scholar
  36. Facey SJ, Kuhn A (2010) Biogenesis of bacterial inner-membrane proteins. Cell Mol Life Sci 67:2343–2362PubMedCrossRefGoogle Scholar
  37. Farinas J, Kneen M, Moore M, Verkman AS (1997) Plasma membrane water permeability of cultured cells and epithelia measured by light microscopy with spatial filtering. J Gen Physiol 110:283–296PubMedCentralPubMedCrossRefGoogle Scholar
  38. Faull RJ, Ginsberg MH (1996) Inside-out signaling through integrins. J Am Soc Nephrol 7:1091–1097PubMedGoogle Scholar
  39. Fedoroff NV (2002) RNA-binding proteins in plants: the tip of an iceberg? Curr Opin Plant Biol 5:452–459PubMedCrossRefGoogle Scholar
  40. Gabriel K, Egan B, Lithgow T (2003) Tom40, the import channel of the mitochondrial outer membrane, plays an active role in sorting imported proteins. EMBO J 22:2380–2386PubMedCentralPubMedCrossRefGoogle Scholar
  41. Gagat P, Bodył A, Mackiewicz P (2013) How protein targeting to primary plastids via the endomembrane system could have evolved? A new hypothesis based on phylogenetic studies. Biol Direct 8:18PubMedCentralPubMedCrossRefGoogle Scholar
  42. Galdiero S, Galdiero M, Pedone C (2007) beta-Barrel membrane bacterial proteins: structure, function, assembly and interaction with lipids. Curr Protein Pept Sci 8:63–82PubMedCrossRefGoogle Scholar
  43. George R, Walsh P, Beddoe T, Lithgow T (2002) The nascent polypeptide-associated complex (NAC) promotes interaction of ribosomes with the mitochondrial surface in vivo. FEBS Lett 516:213–216PubMedCrossRefGoogle Scholar
  44. Gleeson PA (1998) Targeting of proteins to the Golgi apparatus. Histochem Cell Biol 109:517–532PubMedCrossRefGoogle Scholar
  45. Gleeson PA, Teasdale RD, Burke J (1994) Targeting of proteins to the Golgi apparatus. Glycoconj J 11:381–394PubMedCrossRefGoogle Scholar
  46. Glick BS, Nakano A (2009) Membrane traffic within the golgi apparatus. Annu Rev Cell Dev Biol 25:113–132PubMedCentralPubMedCrossRefGoogle Scholar
  47. Glover JR, Andrews DW, Rachubinski RA (1994) Saccharomyces cerevisiae peroxisomal thiolase is imported as a dimer. Proc Natl Acad Sci U S A 97:10541–10545CrossRefGoogle Scholar
  48. Gómez-Simón A, Navarro-Núñez L, Pérez-Ceballos E, Lozano ML, Candela MJ, Cascales A, Martínez C, Corral J, Vicente V, Rivera J (2007) Evaluation of four rapid methods for hemoglobin screening of whole blood donors in mobile collection settings. Transfus Apher Sci 36:235–242PubMedCrossRefGoogle Scholar
  49. Gonen T, Walz T (2006) The structure of aquaporins. Q Rev Biophys 39:361–396PubMedCrossRefGoogle Scholar
  50. Gonzalez E (1986) Glycoproteins in the matrix of glyoxysomes in endosperm of castor bean seedlings. Plant Physiol 80:950–955PubMedCentralPubMedCrossRefGoogle Scholar
  51. Gray MW (1992) The endosymbiont hypothesis revisited. Int Rev Cytol 141:233–357PubMedCrossRefGoogle Scholar
  52. Gray MW (2014) The pre-endosymbiont hypothesis: a new perspective on the origin and evolution of mitochondria. Cold Spring Harb Perspect Biol 6:a016097PubMedCrossRefGoogle Scholar
  53. Hall JE (2011) Guyton and hall textbook of medical physiology, 12th edn. Elsevier Saunders, Philadelphia, p 64Google Scholar
  54. Halldorsson H, Gray DA, Shall S (1978) Poly (ADP-ribose) polymerase activity in nucleotide permeable cells. FEBS Lett 85:349–352PubMedCrossRefGoogle Scholar
  55. Hansen SB, Tao X, MacKinnon R (2011) Structural basis of PIP2 activation of the classical inward rectifier K+ channel Kir2.2. Nature 477:495–498PubMedCentralPubMedCrossRefGoogle Scholar
  56. Hara KY (2009) Permeable cell assay: a method for high-throughput measurement of cellular ATP synthetic activity. Methods Mol Biol 577:251–258PubMedCrossRefGoogle Scholar
  57. Hara KY, Mori H (2006) An efficient method for quantitative determination of cellular ATP synthetic activity. J Biomol Screen 11:310–317PubMedCrossRefGoogle Scholar
  58. Hearps AC, Jans DA (2006) HIV-1 integrase is capable of targeting DNA to the nucleus via an Importin α/β-dependent mechanism. Biochem J 398:475–484PubMedCentralPubMedCrossRefGoogle Scholar
  59. Heldt HW, Sauer F (1971) The inner membrane of the chloroplast envelope as the site of specific metabolite transport. Biochim Biophys Acta 234:83–91PubMedCrossRefGoogle Scholar
  60. Honing S, Hunziker W (1995) Cytoplasmic determinants involved in direct lysosomal sorting, endocytosis, and basolateral targeting of rat lgp120 (lamp-I) in MDCK cells. J Cell Biol 128:321–332PubMedCrossRefGoogle Scholar
  61. Hyodo M, Suzuki K (1980) Chain elongation of DNA and joining of DNA intermediates in intact and permeabilized mouse cells. J Biochem (Tokyo) 88:17–25Google Scholar
  62. Inoue K (2007) The chloroplast outer envelope membrane: the edge of light and excitement. J Integr Plant Biol 49:1100–1111CrossRefGoogle Scholar
  63. Itier V, Bertrand D (2001) Neuronal nicotinic receptors: from protein structure to function. FEBS Lett 504:118–125PubMedCrossRefGoogle Scholar
  64. Jackson CL (2009) Mechanisms of transport through the golgi complex. J Cell Sci 122:443–452PubMedCrossRefGoogle Scholar
  65. Jacobs MH (1927) The exchange of materials between the erythrocyte and its surroundings. Harvey Lect 22:146–164Google Scholar
  66. Jacobs MH, Stewart DR (1932) A simple method for the quantitative measurement of cell permeability. J Comp Physiol 1:71–82Google Scholar
  67. Jansen RP (2001) mRNA localization: message on the move. Nat Rev Mol Cell Biol 2:247–256PubMedCrossRefGoogle Scholar
  68. Jarvis P (2008) Targeting of nucleus-encoded proteins to chloroplast in plants. New Phytol 179:257–285PubMedCrossRefGoogle Scholar
  69. Johnson S, Nguyen V, Coder D (2013) Assessment of cell viability. Curr Protoc Cytom Chapter 9, Unit9.2Google Scholar
  70. Jones KH, Senft JA (1985) An improved method to determine cell viability by simultaneous staining with fluorescein diacetate-propidium iodide. J Histochem Cytochem 33:77–79PubMedCrossRefGoogle Scholar
  71. Kang PJ, OstermannJ SJ, Neupert JW, Craig EA, Pfanner N (1990) Requirement for hsp70 in the mitochondrial matrix for translocation and folding of precursor proteins. Nature 348:137–143PubMedCrossRefGoogle Scholar
  72. Kaupp UB, Seifert R (2002) Cyclic nucleotide-gated ion channels. Physiol Rev 82:769–824PubMedCrossRefGoogle Scholar
  73. Kellems RE, Allison VF, Butow RA (1975) Cytoplasmic type 80S ribosomes associated with yeast mitochondria. IV. Attachment of ribosomes to the outer membrane of isolated mitochondria. J Cell Biol 65:1–14PubMedCrossRefGoogle Scholar
  74. Kennedy C, Angemuller S, King R et al (1996) A comparison of hemolysis rates using intravenous catheters versus venipuncture tubes for obtaining blood samples. J Emerg Nurs 22:566–569PubMedCrossRefGoogle Scholar
  75. Kessler F, Blobel G (1996) Interaction of the protein import and folding machineries in the chloroplast. Proc Natl Acad Sci U S A 93:7684–7689PubMedCentralPubMedCrossRefGoogle Scholar
  76. Kim E, Archibald JM (2009) Diversity and evolution of plastids and their genomes. In: Sandelius AS, Aronsson H (eds) The chloroplast. Plant cell monographs 13. Springer, Berlin, pp 1–39Google Scholar
  77. Kirchhausen T (2000) Chlatrin. Annu Rev Biochem 69:699–727PubMedCrossRefGoogle Scholar
  78. Kloc M, Zearfoss NR, Etkin LD (2002) Mechanisms of subcellular mRNA localization. Cell 108:533–544PubMedCrossRefGoogle Scholar
  79. Koebnik R, Locher KP, Van Gelder P (2000) Structure and function of bacterial outer membrane proteins: barrels in a nutshell. Mol Microbiol 37:239–253PubMedCrossRefGoogle Scholar
  80. Kornfeld S (1992) Structure and function of the mannose 6- phosphate/insulinlike growth factor II receptors. Annu Rev Biochem 61:307–330PubMedCrossRefGoogle Scholar
  81. Kruse E, Uehlein N, Kaldenhoff R (2006) The aquaporins. Genome Biol 7:206PubMedCentralPubMedCrossRefGoogle Scholar
  82. Kucera R, Paulus H (1982) Studied on ribonucleoside-diphosphate reductase in permeable animal cells. I. Reversible permeabilization of mouse L cells with dextran sulfate. Arch Biochem Biophys 214:102–113PubMedCrossRefGoogle Scholar
  83. Künkele K-P, Heins S, Dembowski M, Nargang FE, Benz R, Thieffry M, Walz J, Lill R, Nussberger S, Neupert W (1998) The preprotein translocation channel of the outer membrane of mitochondria. Cell 93:1009–1019PubMedCrossRefGoogle Scholar
  84. Lacal JC (1998) Oocytes microinjection assay to study the MAP-kinase cascade. Methods Mol Biol 84:139–152PubMedGoogle Scholar
  85. Lazarow PB, Fujiki Y (1985) Biogenesis of peroxisomes. Annu Rev Cell Biol 1:489–530PubMedCrossRefGoogle Scholar
  86. Li HM, Chiu C-C (2010) Protein transport into hloroplasts. Annu Rev Plant Biol 61:157–180PubMedCrossRefGoogle Scholar
  87. Lillie RS (1909) On the connection between stimulation and changes in the permeability of the plasma membranes of the irritable elements. Science 30:245–249PubMedCrossRefGoogle Scholar
  88. Linton KJ (2007) Structure and function of ABC transporters. Physiology 22:122–130PubMedCrossRefGoogle Scholar
  89. Lippi G, Blanckaert N, Bonini P, Green S, Kitchen S, Palicka V, Vassault AJ, Plebani M (2008) Haemolysis: an overview of the leading cause of unsuitable specimens in clinical laboratories. Clin Chem Lab Med 46:764–772PubMedGoogle Scholar
  90. Lippi G, Luca Salvagno G, Blanckaert N, Giavarina D, Green S, Kitchen S, Palicka V, Vassault AJ, Plebani M (2009) Multicenter evaluation of the hemolysis index in automated clinical chemistry systems. Clin Chem Lab Med 47:934–939PubMedGoogle Scholar
  91. Liu Q, Krzewska J, Liberek K, Craig EA (2001) Mitochondrial Hsp70 Ssc1: role in protein folding. J Biol Chem 276:6112–6118PubMedCrossRefGoogle Scholar
  92. Liu Q, D’Silva P, Walter W, Marszalek J, Craig EA (2003) Regulated cycling of mitochondrial Hsp70 at the protein import channel. Science 300:139–141PubMedCrossRefGoogle Scholar
  93. Lodish H, Berk A, Kaiser CA, Krieger K, Scott MP Bretscher A, Ploegh H, Matsudaira P (2007) Molecular cell biology, 6th edn. Scientific American Books, New York, p 546Google Scholar
  94. Louis KS, Siegel AC (2011) Cell viability analysis using trypan blue: manual and automated methods. Methods Mol Biol 740:7–12PubMedCrossRefGoogle Scholar
  95. Lübeck J, Soll J, Akita M, Nielsen E, Keegstra K (1996) Topology of IEP110, a component of the chloroplastic protein import machinery present in the inner envelope membrane. EMBO J 15:4230–4238PubMedCentralPubMedGoogle Scholar
  96. Lucké B, Hartline HK, Mccutcheon M (1931) Further studies on the kinetics of osmosis in living cells. J Gen Physiol 14:405–419PubMedCentralPubMedCrossRefGoogle Scholar
  97. Ludwig T, Le Borgne R, Hoflack B (1995) Roles for mannose 6-phosphate receptors in lysosomal enzyme sorting, IGF-II binding and clathrin-coat assembly. Trends Cell Biol 5:202–206PubMedCrossRefGoogle Scholar
  98. MacKenzie JA, Payne RM (2004) Ribosomes specifically bind to mammalian mitochondria via protease-sensitive proteins on the outer membrane. J Biol Chem 279:9803–9810PubMedCrossRefGoogle Scholar
  99. Mapa K, Sikor M, Kudryavtsev V, Waegemann K, Kalinin S, Seidel CA, Neupert W, Lamb DC, Mokranjac D (2010) The conformational dynamics of the mitochondrial Hsp70 chaperone. Mol Cell 38:89–100PubMedCrossRefGoogle Scholar
  100. Mascotti K, McCullough J, Burger SR (2000) HPC viability measurement: trypan blue versus acridine orange and propidium iodide. Transfusion 40:693–696PubMedCrossRefGoogle Scholar
  101. McCutcheon M, Lucké B (1928) The effect of certain electrolytes and non-electrolytes on the rate of osmosis and on permeability of living cells to water. J Gen Physiol 12:129–138PubMedCentralPubMedCrossRefGoogle Scholar
  102. McNew JA, Goodman JM (1994) An oligomeric protein is imported into peroxisomes in vivo. J Cell Biol 727:1245–1257CrossRefGoogle Scholar
  103. Meier I, Zhou X, Brkljacić J, Rose A, Zhao Q, Xu XM (2010) Targeting proteins to the plant nuclear envelope. Biochem Soc Trans 38:733–740PubMedCrossRefGoogle Scholar
  104. Mellman I (1996) Endocytosis and molecular sorting. Annu Rev Cell Dev Biol 12:575–625PubMedCrossRefGoogle Scholar
  105. Miller WL (2013) Steroid hormone synthesis in mitochondria. Mol Cell Endocrinol 379:62–73PubMedCrossRefGoogle Scholar
  106. Miller DG, Trobridge GD, Petek LM, Jacobs MA, Kaul R, Russell DW (2005) Large-scale analysis of adeno-associated virus vector integration sites in normal human cells. J Virol 79:11434–11442PubMedCentralPubMedCrossRefGoogle Scholar
  107. Moses RE, Richardson CC (1970) Replication and repair of DNA in cells of Escherichia coli treated with toluene. Proc Natl Acad Sci U S A 67:674–681PubMedCentralPubMedCrossRefGoogle Scholar
  108. Motley A, Hettema E, Distel B, Tabak H (1994) Differential protein import deficiencies in human peroxisome assembly disorders. J Cell Biol 125:755–767PubMedGoogle Scholar
  109. Naito K, Mizuguchi K, Nosé Y (1994) The need for standardizing the index of hemolysis. Special issue: quality in laboratory diagnostics: from theory to practice. Artif Organs 18:7–10PubMedCrossRefGoogle Scholar
  110. Neglia JP, FitzSimmons SC, Maisonneuve P, Schöni MH, Schöni-Affolter F, Corey M, Lowenfels AB (1995) The risk of cancer among patients with cystic fibrosis. N Engl J Med 332:494–499PubMedCrossRefGoogle Scholar
  111. Neumann E, Schaefer-Ridder M, Wang Y, Hofschneider PH (1982) Gene transfer into mouse lyoma cells by electroporation in high electric fields. EMBO J 1:841–845PubMedCentralPubMedGoogle Scholar
  112. Nichols BJ, Pelham HR (1998) SNAREs and membrane fusion in the Golgi apparatus. Biochim Biophys Acta 1404:9–31PubMedCrossRefGoogle Scholar
  113. Nikaido H (2003) Molecular basis of bacterial outer membrane permeability revisited. Microbiol Mol Biol Rev 67:593–656PubMedCentralPubMedCrossRefGoogle Scholar
  114. Nishio A, Uyeki EM (1982) Inhibition of DNA synthesis in permeabilized L cells by novobiocin. Biochem Biophys Res Commun 106:1448–1455PubMedCrossRefGoogle Scholar
  115. Northrop JH (1927) The kinetics of osmosis. J Gen Physiol 10:883–892PubMedCentralPubMedCrossRefGoogle Scholar
  116. Novikoff PM, Novikoff A (1972) Peroxisomes in absorptive cells of mammalian small intestine. J Cell Biol 53:532–560PubMedCentralPubMedCrossRefGoogle Scholar
  117. Okita TW, Choi S-B (2002) mRNA localization in plants: targeting to the cell’s cortical region and beyond. Curr Opin Plant Biol 5:553–559PubMedCrossRefGoogle Scholar
  118. Overton E (1895) Über die osmotischen Eigenschaften der lebenden Pflauzen. Vjsch Naturf Ges Zurich 40:159–201Google Scholar
  119. Overton E (1900) Studien über die Aufnahme der Anilinfarben durch die 19 lebende Zelle. Jahrb Wiss Bot 34:669–701Google Scholar
  120. Overton E (1907) Über den Mechanismus der Resorption und der Sekretion. Nagel’s Handb Physiol Menschen Braunschweig 2:744–898Google Scholar
  121. Pagliarini DJ, Rutter J (2013) Hallmarks of a new era in mitochondrial biochemistry. Genes Dev 27:2615–2627PubMedCentralPubMedCrossRefGoogle Scholar
  122. Pagliarini DJ, Calvo SE, Chang B, Sheth SA, Vafai SB, Ong SE, Walford GA, Sugiana C, Boneh A, Chen WK, Hill DE, Vidal M, Evans JG, Thorburn DR, Carr SA, Mootha VK (2008) A mitochondrial protein compendium elucidates complex I disease biology. Cell 134:112–123PubMedCentralPubMedCrossRefGoogle Scholar
  123. Palade GE (1983) Membrane biogenesis: an overview. Methods Enzymol 96:XXIX–LVPubMedCrossRefGoogle Scholar
  124. Pemberton LF, Paschal BM (2005) Mechanisms of receptor-mediated nuclear import and nuclear export. Traffic 6:187–198PubMedCrossRefGoogle Scholar
  125. Prokisch H, Ahting U (2007) MitoP2, an integrated database for mitochondrial proteins. Methods Mol Biol 372:573–586PubMedCrossRefGoogle Scholar
  126. Purves D, Augustine GJ, Fitzpatrick D, Hall WC, LaMantia A-S, McNamara JO, White LE (2008) Neuroscience, 4th edn. Sinauer Associates, Publishers, Sunderland, pp 122–126Google Scholar
  127. Quimby BB, Corbett AH (2001) Nuclear transport mechanisms. Cell Mol Life Sci 58:1766–1773PubMedCrossRefGoogle Scholar
  128. Rachubinski RA, Subramani S (1995) How proteins penetrate peroxisomes. Cell 83:525–528PubMedCrossRefGoogle Scholar
  129. Rawicz W, Olbrich KC, McIntosh T, Needham D, Evans E (2000) Effect of chain length and unsaturation on elasticity of lipid bilayers. Biophys J 79:328–339PubMedCentralPubMedCrossRefGoogle Scholar
  130. Reinders J, Zahedi RP, Pfanner N, Meisinger C, Sickmann A (2006) Toward the complete yeast mitochondrial proteome: multidimensional separation techniques for mitochondrial proteomics. J Proteome Res 5:1543–1554PubMedCrossRefGoogle Scholar
  131. Rother RP, Bell L, Hillmen P, Gladwin MT (2005) The clinical sequelae of intravascular hemolysis and extracellular plasma hemoglobin: a novel mechanism of human disease. JAMA 293:1653–1662PubMedCrossRefGoogle Scholar
  132. Rouillé Y, Rohn W, Hoflack B (2000) Targeting of lysosomal proteins. Semin Cell Dev Biol 11:165–171PubMedCrossRefGoogle Scholar
  133. Saier MH Jr, Yen MR, Noto K, Tamang DG, Elkan C (2009) The transporter classification database: recent advances. Nucleic Acids Res 37:D274–D278PubMedCentralPubMedCrossRefGoogle Scholar
  134. Sanchirico ME, Fox TD, Mason TL (1998) Accumulation of mitochondrially synthesized Saccharomyces cerevisiae Cox2p and Cox3p depends on targeting information in untranslated portions of their mRNAs. EMBO J 17:5796–5804PubMedCentralPubMedCrossRefGoogle Scholar
  135. Sandoval IV, Bakke O (1994) Targeting of membrane proteins to endosomes. Trends Cell Biol 4:292–297PubMedCrossRefGoogle Scholar
  136. Schatz G (2006) Chauvinism in science. In: Jeff’s view on science and scientists. Essays from FEBS Letters. Elsevier BV, Amsterdam, pp 163–176Google Scholar
  137. Schleiff E, Soll J (2005) Membrane protein insertion: mixing eukaryotic and prokaryotic concepts. EMBO Rep 6:1023–1027PubMedCentralPubMedCrossRefGoogle Scholar
  138. Schnell DJ, Blobel G, Keegstra K, Kessler F, Ko K, Soll J (1997) A consensus nomenclature for the protein-import components of the chloroplast envelope. Trends Cell Biol 7:303–304PubMedCrossRefGoogle Scholar
  139. Scott MP, Lodish HF, Berk A, Kaiser C, Krieger M, Bretscher A, Ploegh H, Amon A (2012) Molecular cell biology. W. H. Freeman, San FranciscoGoogle Scholar
  140. Sehy JV, Banks AA, Ackerman JJ, Neil JJ (2002) Importance of intracellular water apparent diffusion to the measurement of membrane permeability. Biophys J 83:2856–2863PubMedCentralPubMedCrossRefGoogle Scholar
  141. Shah VB, Shah BS, Puranik GV (2011) Evaluation of non cyanide methods for hemoglobin estimation. Indian J Pathol Microbiol 54:764–768PubMedGoogle Scholar
  142. Shen B, Delaney MK, Du X (2012) Inside-out, outside-in, and inside-outside-in: G protein signaling in integrin-mediated cell adhesion, spreading, and retraction. Curr Opin Cell Biol 24:600–606PubMedCentralPubMedCrossRefGoogle Scholar
  143. Shiraishi T, Hamzavi R, Nielsen PE (2005) Targeted delivery of plasmid DNA into the nucleus of cells via nuclear localization signal peptide conjugated to DNA intercalating bis- and trisacridines. Bioconjug Chem 16:1112–1116PubMedCrossRefGoogle Scholar
  144. Simons K, Warren G (1983) Semliki Forest virus: a probe for membrane traffic in the animal cell. Adv Protein Chem 36:79–132CrossRefGoogle Scholar
  145. Simons K, Garoff H, Helenius A (1982) How an animal virus gets into and out of its host cell. Sci Am 246:58–66PubMedCrossRefGoogle Scholar
  146. Simundic A-M, Topic E, Nikolac N, Lippi L (2010) Hemolysis detection and management of hemolysed specimens. Biochemia Med 20:154–159CrossRefGoogle Scholar
  147. Srinivasakumar N (2001) HIV-1 vector systems. Somat Cell Mol Genet 26:51–81PubMedCrossRefGoogle Scholar
  148. St. Johnston D (2005) Moving messages: the intracellular localization of mRNAs. Nat Rev Mol Cell Biol 6:363–375PubMedCrossRefGoogle Scholar
  149. Storrie B (2005) Maintenance of Golgi apparatus structure in the face of continuous protein recycling to the endoplasmic reticulum: making ends meet. Int Rev Cytol 244:69–94PubMedCrossRefGoogle Scholar
  150. Subramani S (1988) Components involved in peroxisome import, biogenesis, proliferation, turnover, and movement. Physiol Rev 78:171–188Google Scholar
  151. Sugiura M (1989) The chloroplast chromosomes in land plants. Annu Rev Cell Biol 5:51–70PubMedCrossRefGoogle Scholar
  152. Taanman J-W (1999) The mitochondrial genome: structure, transcription, translation and replication. Biochim Biophys Acta 1410:103–123PubMedCrossRefGoogle Scholar
  153. Tabak HF, Hoepfner D, Zand A v, Geuze HJ, Braakman I, Huynen MA (2006) Formation of peroxisomes: present and past. Biochim Biophys Acta 1763:1647–1654PubMedCrossRefGoogle Scholar
  154. ter Kuile BH, Cook M (1994) The kinetics of facilitated diffusion followed by enzymatic conversion of the substrate. Biochim Biophys Acta 1193:235–239PubMedCrossRefGoogle Scholar
  155. Thomas RC, Meech RW (1982) Hydrogen ion currents and intraceilular pH in depolarized voltage-clamped snail neurones. Nature 299:826–828PubMedCrossRefGoogle Scholar
  156. Thompson LA (2007) Passing the north carolina end of course test for biology. American Book Company, Woodstock, p 97Google Scholar
  157. Uemura T, Ueda T, Ohniwa RL, Nakano A, Takeyasu K, Sato MH (2004) Systematic analysis of SNARE molecules in Arabidopsis: dissection of the post-Golgi network in plant cells. Cell Struct Funct 29:49–65PubMedCrossRefGoogle Scholar
  158. Ungermann C, Neupert W, Cyr DM (1994) The role of Hsp70 in conferring unidirectionality on protein translocation into mitochondria. Science 266:1250–1253PubMedCrossRefGoogle Scholar
  159. Uniacke J, Zerges W (2009) Chloroplast protein targeting involves localized translation in Chlamydomonas. Proc Natl Acad Sci U S A 106:1439–1444PubMedCentralPubMedCrossRefGoogle Scholar
  160. van Assendelft OW, Zijlstra WG (1989) Observations on the alkaline haematin/detergent complex proposed for measuring haemoglobin concentration. J Clin Chem Clin Biochem 27:191–195PubMedGoogle Scholar
  161. van Breemen RB, Li Y (2005) Caco-2 cell permeability assays to measure drug absorption. Expert Opin Drug Metab Toxicol 1:175–185PubMedCrossRefGoogle Scholar
  162. Van de Bor V, Davis I (2004) mRNA localisation gets more complex. Curr Opin Cell Biol 16:300–307PubMedCrossRefGoogle Scholar
  163. Vögtle F-N, Wortelkamp S, Zahedi RP, Becker D, Leidhold C, Gevaert K, Kellermann J, Voos W, Sickmann A, Pfanner N, Meisinger C (2009) Global analysis of the mitochondrial N-proteome identifies a processing peptidase critical for protein stability. Cell 139:428–439PubMedCrossRefGoogle Scholar
  164. Voisine C, Craig EA, Zufall N, von Ahsen O, Pfanner N, Voos W (1999) The protein import motor of mitochondria: unfolding and trapping of preproteins are distinct and separable functions of matrix Hsp70. Cell 97:565–574PubMedCrossRefGoogle Scholar
  165. Wilson DP, Susnjar M, Kiss E, Sutherland C, Walsh MP (2005) Thromboxane A2-induced contraction of rat caudal arterial smooth muscle involves activation of Ca2+ entry and Ca2+ sensitization: Rho-associated kinase-mediated phosphorylation of MYPT1 at Thr-855, but not Thr-697. Biochem J 389:763–774PubMedCentralPubMedCrossRefGoogle Scholar
  166. Xu Y, Hu W, Liu J, Zhang J, Jia C, Miao H, Xu B, Jin Z (2014) A banana aquaporin gene. BMC Plant Biol 14:59PubMedCentralPubMedCrossRefGoogle Scholar
  167. Yamakage M, Namiki A (2002) Calcium channels – basic aspects of their structure, function and gene encoding; anesthetic action on the channels – a review. Can J Anaesth 49:151–164PubMedCrossRefGoogle Scholar
  168. Yang H, Curinga G, Giachelli CM (2004) Elevated extracellular calcium levels induce smooth muscle cell matrix mineralization in vitro. Kidney Int 66:2293–2299PubMedCrossRefGoogle Scholar
  169. Young JL, Benoit JN, Dean DA (2003) Effect of a DNA nuclear targeting sequence on gene transfer and expression of plasmids in the intact vasculature. Gene Ther 10:1465–1470PubMedCentralPubMedCrossRefGoogle Scholar
  170. Yu Q, Shi H, Wang J (1995) Simultaneous staining with fluorescein diacetate-propidium iodide to determine isolated cochlear outer hair cell viability of guinea pig (Article in Chinese). Zhonghua Er Bi Yan Hou Ke Za Zhi 30:152–153PubMedGoogle Scholar
  171. Yu P, Liu B, Kodadek T (2007) A convenient, high-throughput assay for measuring the relative cell permeability of synthetic compounds. Nat Protoc 2:23–30PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.University of DebrecenDebrecenHungary

Personalised recommendations