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Interaction of Gravity with Cellular Compounds

  • Wolfgang Hanke
  • Florian P. M. Kohn
  • Maren Neef
  • Rüdiger Hampp
Chapter
Part of the SpringerBriefs in Space Life Sciences book series (BRIEFSSLS)

Abstract

During evolution, the majority of organisms have developed specific sensors for gravity, the only constant environmental cue on earth. Nevertheless, a variety of gravity effects on molecular, cellular, and physiological level has also been reported in single-cell organisms and cell types of plants and animals which do not seem to possess specific sensors. We have found that the cellular membrane, common to all cells, itself is interacting with gravity by changing its fluidity. Thus, it delivers a basic mechanism for gravity perception for all existing cells and living systems. In the following, we discuss the physical principles and the consequences of our findings for membrane-bound processes, for life on earth, and for manned space travel. In addition, a first model is proposed, how a sensor system for gravity based on membrane thermodynamics could be structured.

Keywords

Neuronal cells Gravity perception Membrane fluidity 

References

  1. Acedo LA (2009) Cellular automation model for collective neural dynamics. Math Comput Model 50:717–725CrossRefGoogle Scholar
  2. Albi E, Ambesi-Impiombato FS, Peverini MM, Damaskopolus E, Fontanini E, Lazzarini R, Curcio F, Perella G (2011) Thyrotropin receptor a membrane interactions in FRTL-5 thyroid cell strain in microgravity. Astrobiology 11:57–64PubMedCrossRefGoogle Scholar
  3. Aloia RC, Boggs JM (1985) Membrane fluidity in biology. Academic Press, Orlando, FLGoogle Scholar
  4. Belousov BP (1959) Eine periodische Reaktion und ihr Mechanismus (translated from Russian to German). In Sbornik referatov po radiacionoj medicine za. Moskau 147:145Google Scholar
  5. Boheim G (1974) Statistical analysis of alamethicin channels in black lipid membranes. J Membr Biol 19(1):277–303PubMedCrossRefGoogle Scholar
  6. Boheim G, Hanke W, Jung G (1983) Alamethicin pore formation, voltage dependent flip-flop of a-helix dipoles. Biophys Struct Mech 9:188–197CrossRefGoogle Scholar
  7. Boheim G, Hanke W, Jung G (1984) The alamethicin pore is formed by a voltage-gated flip-flop of a-helix dipoles. In: Welter W et al (eds) Chemistry of peptides. W. de Gruyter, Berlin, pp 281–289Google Scholar
  8. Cafiso DS (1994) Alamethicin: a peptide model for voltage gating and protein-membrane interactions. Annu Rev Biophys Biomol Struct 23:141–165PubMedCrossRefGoogle Scholar
  9. Dowhan W, Bogdanov M (2002) Functional roles of lipids in membranes. In: Vance DE, Vance JE (eds) Biochemistry of lipids, lipoproteins and membranes. Elsevier, Amsterdam, pp 1–35Google Scholar
  10. Epstein IR, Pojman JA (1998) An introduction to nonlinear chemical dynamics. Oxford University Press, Oxford. ISBN 978-0195096705Google Scholar
  11. Fernades de Lima VM, Piqueira JRC, Hanke W (2015) The tight coupling and non-linear relationship between the macroscopic electrical and optical concomitants of electrochemical CNS waves reflect the non-linear dynamics of neural glial propagation. Open J Biophys 5(1):11Google Scholar
  12. Goldermann M, Hanke W (2001) Ion channels are sensitive to gravity changes. J Microgravity Sci Technol XIII/1:35–38CrossRefGoogle Scholar
  13. Goldman DE (1943) Potential, impedance, and rectification in membranes. J Gen Physiol 27:37–60PubMedPubMedCentralCrossRefGoogle Scholar
  14. Häder D-P, Hemmersbach R, Lebert M (2005) Gravity and the behavior of unicellular organisms. Cambridge University Press, New York, NYCrossRefGoogle Scholar
  15. Hall JE, Vodyanoy I, Balasubramanian TM, Marshall GR (1984) Alamethicin. A rich model for channel behavior. Biophys J 45(1):233–247PubMedPubMedCentralCrossRefGoogle Scholar
  16. Hamill OP, Neher E, Sakmann B, Sigworth FJ (1981) Improved patch-clamp techniques for high-resolution current recordings from cells and cell-free membrane patches. Pflügers Archiv 391:85–100PubMedCrossRefGoogle Scholar
  17. Hanke W (1995) Studies of the interaction of gravity with biological membranes using alamethicin doped planar lipid bilayers as a model system. Adv Space Res 6/7:143–150Google Scholar
  18. Hanke W, Schlue W-R (1993) Planar lipid bilayer experiments: techniques and application. Academic Press, OxfordGoogle Scholar
  19. Hauslage J, Albrecht M, Hanke L, Hemmersbach R, Koch C, Hanke W, Kohn PM (2016) Cytosolic calcium concentration changes in neuronal cells under clinorotation and in parabolic flight missions. Microgravity Sci Technol 28(6):633–638.  https://doi.org/10.1007/s12217-016-9520-y CrossRefGoogle Scholar
  20. Hausmann N, Fengler S, Henning A, Franz-Wachtel M, Hampp R, Neef M (2014) Cytosolic calcium, hydrogen peroxide and related gene expression and protein modulation in Arabidopsis thaliana cell cultures respond immediately to altered gravitation: parabolic flight data. Plant Biol 16(Suppl 1):120–128PubMedCrossRefGoogle Scholar
  21. Heimburg T (2010) Lipid ion channels. Biophys Chem 150:2–22PubMedCrossRefGoogle Scholar
  22. Klinke N, Goldermann M, Hanke W (2000) The properties of alamethicin incorporated into planar lipid bilayers under the influence of microgravity. Acta Astron 47:771–773CrossRefGoogle Scholar
  23. Klymchuk DO, Baranenko VV, Vorobyova TV, Dubovoy VD (2006) Fluidity of pea root plasma membranes under altered gravity. http://adsabs.harvard.edu/abs/2004cosp.35.1356K
  24. Kohn F (2010) Patch clamp experiments with human neuron-like cells under different gravity conditions. PhD thesis. University of Hohenheim, Stuttgart, GermanyGoogle Scholar
  25. Kohn F (2013) High throughput fluorescent screening of membrane potential and intracellular calcium concentration under variable gravity conditions. Microgravity Sci Technol 25(2):113–120CrossRefGoogle Scholar
  26. Kohn FPM, Ritzmann R (2017) Gravity and neuronal adaptation, in vitro and in vivo-from neuronal cells up to neuromuscular responses: a first model. Eur Biophys J.  https://doi.org/10.1007/s00249-017-1233-7 PubMedPubMedCentralCrossRefGoogle Scholar
  27. Kohn F, Hauslage J, Hanke W (2017) Membrane fluidity changes, a basic mechanism of interaction of gravity with cells? Microgravity Sci Technol.  https://doi.org/10.1007/s12217-017-9552-y CrossRefGoogle Scholar
  28. Kordyum EL, Neduhka OM, Grakhov VP, Melnik AK, Vorbyova TM, Klimeko OM, Zhupanov IV (2015) Study of the influence of simulated microgravity on the cytoplasmic membrane lipid bilayer of plant cells. Kosm Nauka Tehnol 21:40–47CrossRefGoogle Scholar
  29. Lacowicz JR (2006) Principles in fluorescence spectroscopy. Springer, New York, NYCrossRefGoogle Scholar
  30. Layne CS, Spooner BS (1990) EMG analysis of human postural during parabolic flight microgravity episodes. Aviat Space Environ Med 6:994–998Google Scholar
  31. Leitgeb B, Szekeres A, Manczinger L, Vagvölgyi C, Kredics L (2007) The history of alamethicin: A review of the most extensively studied peptaibol. Chem Biodivers 4:1027–1051PubMedCrossRefGoogle Scholar
  32. Mallipattu SK, Haidekker MA, Von Dassow P, Latz M, Frangos J (2002) Evidence for shear-induced increase in membrane fluidity in the dinoflagellate Lingulodinium polyedrum. J Comp Physiol 188:409–416CrossRefGoogle Scholar
  33. Martins-Ferreira H, de Oliveira-Castro GD (1966) Light scattering changes accompanying spreading depression in isolated retina. J Neurophysiol 29:715–726PubMedCrossRefGoogle Scholar
  34. Meissner K, Hanke W (2002) Patch clamp experiments under microgravity. J Grav Physiol 9(1):377–378Google Scholar
  35. Meissner K, Hanke W (2005) Action potential properties are gravity dependent. Microgravity Sci Technol 17(2):38–43CrossRefGoogle Scholar
  36. Murray JD (2002) Mathematical biology. An introduction. Springer, New YorkGoogle Scholar
  37. Neef M, Ecke M, Hampp R (2015) Real-time recording of cytosolic calcium levels in Arabidopsis thaliana cell cultures during parabolic flights. Microgravity Sci Technol 27:305–312CrossRefGoogle Scholar
  38. Novespace (2009) A300 Zero-G rules and guidelines, RG-2009-2Google Scholar
  39. Pandis C, Metastasio A, Mastrandrea F (2009) Effects of gravity on ulnar nerve latency of activation. http://eea.spaceflight.esa.int/attachments/parabolicflights/ID49661e9539c5f.pdf
  40. Pandolfi C, Masi E, Yoigt B, Mugnai S, Volkmann D, Mancuso S (2014) Gravity affects the closure of the trap in Dionaea muscipula. BioMed Res Int.  https://doi.org/10.1155/2014/964203 CrossRefGoogle Scholar
  41. Richard S, Henggeler D, Ille F, Vadrucci Beck S, Moeckli M, Forster IC, Franco-Obregón A, Egli M (2012) A semi-automated electrophysiology system for recording from Xenopus Oocytes under microgravity conditions. Microgravity Sci Technol 24(4):237–244.  https://doi.org/10.1007/s12217-012-9307-8 CrossRefGoogle Scholar
  42. Rüegg DG, Kakebeeke TH, Studer LM (2000) Einfluss der Schwerkraft auf die Fortleitungsgeschwindigkeit von Muskel-Aktionspotentialen. In: Kelle H, Sahm PR (eds) Bilanzsymposium Forschung unter Weltraumbedingungen. WPF, Aachen, pp 752–759Google Scholar
  43. Sagués F, Epstein IR (2003) Nonlinear chemical dynamics. Dalton Trans 7:1201–1217CrossRefGoogle Scholar
  44. Sieber M, Hanke W, Kohn FPM (2014) Modification of membrane fluidity by gravity. Open J Biophys 4(4):105–111CrossRefGoogle Scholar
  45. Sieber M, Kaltenbach S, Hanke W, Kohn F (2016) Conductance and capacity of plain lipid membranes under conditions of variable gravity. J Biomed Sci Eng 9:361–366CrossRefGoogle Scholar
  46. Singer SJ, Nicholson GL (1972) The fluid mosaic model of the structure of cell membranes. Science 175(4023):720–731PubMedPubMedCentralCrossRefGoogle Scholar
  47. Tabony J (2006) Microtubules viewed as molecular ant colonies. Biol Cell 98:603–617PubMedCrossRefGoogle Scholar
  48. Tasaki I (2004) On the conduction velocity of non-myelinated nerve fibers. J Integr Neurosci 3:115–124PubMedCrossRefGoogle Scholar
  49. Torchilin VP, Weissig V (2003) Liposomes: a practical approaches. Oxford University Press, New YorkGoogle Scholar
  50. Vaquer S, Cuyas E, Rabadan A, Gonzale A, Fenollosa F, de la Torre R (2014) Active membrane drug transport in microgravity: a validation study using an ABC transporter model. F1000Research 3:201.  https://doi.org/10.12688/f1000research.4909.1 PubMedPubMedCentralCrossRefGoogle Scholar
  51. Volinsky R, Kolusheva S, Berman A, Jelinek R (2004) Microscopic visualization of alamethicin incorporation into model membrane monolayers. Langmuir 20:11084–11091PubMedCrossRefGoogle Scholar
  52. Wiedemann M, Hanke W (2002) Gravity sensing in the central nervous system. J Grav Physiol 9(1):43–44Google Scholar
  53. Wiedemann M, Rahmann H, Hanke W (2003) Gravitational impact on ion channels incorporated into planar lipid bilayers. In: Tien HT, Ottova A (eds) Planar lipid bilayers and their applications. Elsevier Sciences, Amsterdam, pp 669–698Google Scholar
  54. Wiedemann M, Kohn FPM, Rösner H, Hanke WRL (2011) Self-organization and pattern-formation in neuronal systems under conditions of variable gravity. Springer, Berlin. isbn:978-3-642-14471-4CrossRefGoogle Scholar
  55. Wolfram S (2002) A new kind of science. Wolfram Media, Champaign, ILGoogle Scholar
  56. Woolley GA, Wallace BA (1992) Model ion channels: gramicidin and alamethicin. J Membr Biol 129(2):109–136PubMedGoogle Scholar
  57. Zaikin AN, Zhabotinsky AM (1970) Concentration wave propagation in two-dimensional liquid-phase self-oscillating system. Nature 225:535–537CrossRefGoogle Scholar
  58. Zanello LP, Aztiria E, Antollini A, Barrantes FJ (1996) Nicotinic acetylcholine receptor channels are influenced by the physical state of their membrane environment. Biophys J 70:2155–2164PubMedPubMedCentralCrossRefGoogle Scholar
  59. Zhao H, Lappalainen P (2012) A simple guide to biochemical approaches for analyzing protein-lipid interactions. Mol Biol Cell 23(15):2823–2830.  https://doi.org/10.1091/mbc.e11-07-0645 PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  • Wolfgang Hanke
    • 1
  • Florian P. M. Kohn
    • 1
  • Maren Neef
    • 2
  • Rüdiger Hampp
    • 2
  1. 1.Institute of PhysiologyUniversity of HohenheimStuttgartGermany
  2. 2.Institute for Microbiology and Infection Biology Tübingen (IMIT)University of TübingenTübingenGermany

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