Skip to main content
SpringerLink
Log in

Delving into Membrane Heterogeneity Utilizing Fluorescence Lifetime Distribution Analysis

  • Published:
The Journal of Membrane Biology Aims and scope Submit manuscript

Abstract

Lipid bilayer membranes are indispensable parts of cellular architecture. One of the integral properties of bilayer membranes is the environmental heterogeneity over a wide range of spatiotemporal scales. The environmental heterogeneity is a manifestation of the dynamic and compositional anisotropy in the plane of the membrane as well as along the bilayer normal. Fluorescence lifetime distribution analysis provides a spectroscopic tool to quantitatively characterize such heterogeneities. The review discusses recent applications of fluorescence lifetime distribution analysis utilizing the maximum entropy method to characterize horizontal and vertical heterogeneities in membranes.

Graphical abstract

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

modified from Shrivastava et al. 2020

Fig. 2

Adapted and modified from Shrivastava et al. 2020

Fig. 3

Adapted and modified from Haldar et al. 2012c

Fig. 4

Adapted and modified from Haldar et al. 2012c

Fig. 5

Adapted and modified from Chakraborty et al. 2015

Similar content being viewed by others

References

  • Abrams FS, London E (1993) Extension of the parallax analysis of membrane penetration depth to the polar region of model membranes: use of fluorescence quenching by a spin-label attached to the phospholipid polar headgroup. Biochemistry 32:10826–10831

    Article  CAS  PubMed  Google Scholar 

  • Abrams FS, Chattopadhyay A, London E (1992) Determination of the location of fluorescent probes attached to fatty acids state and environment on depth using parallax analysis of fluorescence quenching: effect of carboxyl ionization. Biochemistry 31:5322–5327

    Article  CAS  PubMed  Google Scholar 

  • Beechem JM, Brand L (1985) Time-resolved fluorescence of proteins. Annu Rev Biochem 54:43–71

    Article  CAS  PubMed  Google Scholar 

  • Brahma R, Raghuraman H (2021) Novel insights in linking solvent relaxation dynamics and protein conformations utilizing red edge excitation shift approach. Emerg Top Life Sci 5:89–101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brochon JC (1994) Maximum entropy method of data analysis in time-resolved spectroscopy. Methods Enzymol 240:262–311

    Article  CAS  PubMed  Google Scholar 

  • Carquin M, D’Auria L, Pollet H, Bongarzone ER, Tyteca D (2016) Recent progress on lipid lateral heterogeneity in plasma membranes: From rafts to submicrometric domains. Prog Lipid Res. 62:1–24

    Article  CAS  PubMed  Google Scholar 

  • Chakraborty H, Haldar S, Chong PL, Kombrabail M, Krishnamoorthy G, Chattopadhyay A (2015) Depth-dependent organization and dynamics of archaeal and eukaryotic membranes: development of membrane anisotropy gradient with natural evolution. Langmuir 31:11591–11597

    Article  CAS  PubMed  Google Scholar 

  • Chatterjee S, Brahma R, Raghuraman H (2021) Gating-related structural dynamics of the MgtE magnesium channel in membrane-mimetics utilizing site-directed tryptophan fluorescence. J Mol Biol. 433:166691

    Article  CAS  PubMed  Google Scholar 

  • Chattopadhyay A, London E (1987) Parallax method for direct measurement of membrane penetration depth utilizing fluorescence quenching by spin-labeled phospholipids. Biochemistry 26:39–45

    Article  CAS  PubMed  Google Scholar 

  • Chattopadhyay A, London E (1988) Spectroscopic and Ionization properties of N-(7-nitrobenz2-oxa-1,3-diazol-4-yl)-labeled lipids in model membranes. Biochim Biophys Acta 938:24–34

    Article  CAS  PubMed  Google Scholar 

  • Chattopadhyay A, Mukherjee S (1999) Depth-dependent solvent relaxation in membranes: wavelength-selective fluorescence as a membrane dipstick. Langmuir 15:2142–2148

    Article  CAS  Google Scholar 

  • Chong PL-G (2010) Archaebacterial bipolar tetraether lipids: physico-chemical and membrane properties. Chem Phys Lipids 163:253–265

    Article  CAS  PubMed  Google Scholar 

  • Davenport L (1997) Fluorescence probes for studying membrane heterogeneity. Methods Enzymol 278:487–512

    Article  CAS  PubMed  Google Scholar 

  • de Almeida RF, Loura LM, Prieto M (2009) Membrane lipid domains and rafts: current applications of fluorescence lifetime spectroscopy and imaging. Chem Phys Lipids 157:61–77

    Article  PubMed  Google Scholar 

  • Gould SB (2018) Membranes and evolution. Curr Biol 28:R381–R385

    Article  CAS  PubMed  Google Scholar 

  • Haldar S, Kombrabail M, Krishnamoorthy G, Chattopadhyay A (2010) Monitoring membrane protein conformational heterogeneity by fluorescence lifetime distribution analysis using the maximum entropy method. J Fluoresc 20:407–413

    Article  CAS  PubMed  Google Scholar 

  • Haldar S, Chaudhuri A, Chattopadhyay A (2011) Organization and dynamics of membrane probes and proteins utilizing the red edge excitation shift. J Phys Chem B 115:5693–5706

    Article  CAS  PubMed  Google Scholar 

  • Haldar S, Chaudhuri A, Gu H, Koeppe RE 2nd, Kombrabail M, Krishnamoorthy G, Chattopadhyay A (2012a) Membrane organization and dynamics of “inner pair” and “outer pair” tryptophan residues in gramicidin channels. J Phys Chem B 116:11056–11064

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haldar S, Kanaparthi RK, Samanta A, Chattopadhyay A (2012b) Differential effect of cholesterol and its biosynthetic precursors on membrane dipole potential. Biophys J 102:1561–1569

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haldar S, Kombrabail M, Krishnamoorthy G, Chattopadhyay A (2012c) Depth-dependent heterogeneity in membranes by fluorescence lifetime distribution analysis. J Phys Chem Lett. 3:2676–81

    Article  CAS  PubMed  Google Scholar 

  • Ira KG (2001) Fluorescence lifetime distribution in characterizing membrane microheterogeneity. J Fluoresc 11:247–253

    Article  Google Scholar 

  • Jacobsen AC, Jensen SM, Fricker G, Brandl M, Treusch AH (2017) Archaeal lipids in oral delivery of therapeutic peptides. Eur J Pharm Sci 108:101–110

    Article  CAS  PubMed  Google Scholar 

  • Kalappurakkal JM, Sil P, Mayor S (2020) Toward a new picture of the living plasma membrane. Protein Sci 29:1355–1365

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kates M (1992) Archaebacterial lipids: structure, biosynthesis and function. Biochem. Soc. Symp. 58:51–72

    CAS  PubMed  Google Scholar 

  • Krishnamoorthy G (2018) Fluorescence spectroscopy for revealing mechanisms in biology: strengths and pitfalls. J Biosci 43:555–567

    Article  CAS  PubMed  Google Scholar 

  • Lakowicz JR (2006) Principles of Fluorescence Spectroscopy, 3rd edn. Springer, New York

    Book  Google Scholar 

  • Leikin S, Parsegian VA, Rau DC, Rand RP (1993) Hydration forces. Annu Rev Phys Chem 44:369–395

    Article  CAS  PubMed  Google Scholar 

  • Marsh D (2001) Polarity and permeation profiles in lipid membranes. Proc Natl Acad Sci USA 98:7777–7782

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Megha BO, London E (2006) Cholesterol precursors stabilize ordinary and ceramide-rich ordered lipid domains (lipid rafts) to different degrees. Implications for the Bloch hypothesis and sterol biosynthesis disorders. J Biol Chem 281:21903–21913

    Article  CAS  PubMed  Google Scholar 

  • Mukherjee S, Raghuraman H, Chattopadhyay A (2006) Membrane localization and dynamics of Nile Red: effect of cholesterol. Biochim Biophys Acta 1768:59–66

    Article  PubMed  Google Scholar 

  • Mukherjee S, Kombrabail M, Krishnamoorthy G, Chattopadhyay A (2007) Dynamics and heterogeneity of bovine hippocampal membranes: role of cholesterol and proteins. Biochim Biophys Acta 1768:2130–2144

    Article  CAS  PubMed  Google Scholar 

  • Oger PM, Cario A (2013) Adaptation of the membrane in archaea. Biophys Chem 183:42–56

    Article  CAS  PubMed  Google Scholar 

  • Pal S, Chattopadhyay A (2021) Hydration dynamics in biological membranes: emerging applications of terahertz spectroscopy. J Phys Chem Lett 12:9697–9709

    Article  CAS  PubMed  Google Scholar 

  • Sankaran J, Wohland T (2020) Fluorescence strategies for mapping cell membrane dynamics and structures. APL Bioeng. 4:020901

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sharpe HJ, Stevens TJ, Munro SA (2010) Comprehensive comparison of transmembrane domains reveals organelle-specific properties. Cell 142:158–169

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shaw TR, Ghosh S, Veatch SL (2021) Critical phenomena in plasma membrane organization and function. Annu Rev Phys Chem 72:51–72

    Article  CAS  PubMed  Google Scholar 

  • Shrivastava S, Paila YD, Kombrabail M, Krishnamoorthy G, Chattopadhyay A (2020) Role of cholesterol and its immediate biosynthetic precursors in membrane dynamics and heterogeneity: implications for health and disease. J Phys Chem B 124:6312–6320

    Article  CAS  PubMed  Google Scholar 

  • Stubbs CD, Ho C, Slater SJ (1995) Fluorescence techniques for probing water penetration into lipid bilayers. J Fluoresc 5:19–28

    Article  CAS  PubMed  Google Scholar 

  • Swaminathan R, Periasamy N (1996) Analysis of fluorescence decay by the maximum entropy method: influence of noise and analysis parameters on the width of the distribution of lifetimes. Proc Indian Acad Sci (chem Sci) 108:39–49

    Article  CAS  Google Scholar 

  • Swaminathan R, Krishnamoorthy G, Periasamy N (1994) Similarity of fluorescence lifetime distributions for single tryptophan proteins in the random coil state. Biophys J 67:2013–2023

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Valeur B (2002) Molecular Fluorescence. Wiley-VCH, Weinheim, Germany

    Google Scholar 

  • Villalain J, Prieto M (1991) Location and interaction of N-(9-anthroyloxy)-stearic acid probes incorporated in phosphatidylcholine vesicles. Chem Phys Lipids 59:9–16

    Article  CAS  Google Scholar 

  • Woese CR, Fox GE (1977) Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proc Natl Acad Sci USA 74:5088–5090

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The review is primarily based on the work conducted in the laboratory of Prof. Amitabha Chattopadhyay (CCMB, Hyderabad, India) and Prof. G. Krishnamoorthy (TIFR, Mumbai, India). Their support and encouragement are gratefully acknowledged. The author also acknowledges the Department of Biotechnology, Govt. of India for the Ramalingaswami Fellowship and the Division of Virus Research and Therapeutics, CSIR- Central Drug Research Institute, Lucknow, India for institutional support. CSIR-CDRI communication number 10395.

Author information

Authors and Affiliations

  1. Division of Virus Research and Therapeutics, CSIR- Central Drug Research Institute, Lucknow, Uttar Pradesh, 226031, India

    Sourav Haldar

Authors
  1. Sourav Haldar
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

SH wrote the whole manuscript and prepared figures and edited.

Corresponding author

Correspondence to Sourav Haldar.

Ethics declarations

Conflict of interest

The author declares that the author has no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Haldar, S. Delving into Membrane Heterogeneity Utilizing Fluorescence Lifetime Distribution Analysis. J Membrane Biol 255, 553–561 (2022). https://doi.org/10.1007/s00232-022-00235-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00232-022-00235-z

Keywords

Search

Navigation