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The Journal of Membrane Biology

, Volume 252, Issue 6, pp 541–548 | Cite as

Life During Wartime: A Personal Recollection of the Circa 1990 Prestegard Lab and Its Contributions to Membrane Biophysics

  • Charles R. SandersEmail author
Topical Review

Abstract

A subjective account is presented of challenges and excitement of being a postdoctoral trainee in the lab of James H. Prestegard at Yale University in New Haven, Connecticut from 1989 to 1991. This includes accounts of the early development of bicelles and of oriented sample NMR results that contributed to our modern understanding of the properties of the water–lipid interface of disordered phase biological membranes.

Keywords

Bicelles Membranes Interface NMR Spectroscopy 

Notes

Acknowledgements

I am grateful for 1989–1991 support and many good memories to Jim and Bert Prestegard, all the members of the Prestegard lab and their partners/families, honorary Prestegard lab members from other labs, friends in the adjacent Moore, Crothers, Caradonna, Brudvig, and Zilm labs, the Yale NMR staff and community, Becky and our sons Stephen, and Noah (born 2 h after President Bush’s announcement of the end of the 1st Gulf War and only 20 min after we reached the Yale Hospital), our parents and siblings who encouraged us from Ohio and Illinois, and our friends from the gone-but-not-forgotten Westside Church of Christ. I thank Ming-Daw Tsai (now at the Academia Sinica in Taipei) for helping me to navigate his papers on phosphorothioate phospholipids. The writing of this document was supported by NIH Grants RO1 HL122010, RO1 NS095989, and RF1 AG056147. I thank Kathleen Howard and Blake Hill for their helpful comments and archival materials, including (from KH) the Yale era photo of Dr. Prestegard that appears in the Table of Contents graphic. Wade Van Horn, Larry Marnett, and Tony Forster are thanked for helpful suggestions.

Compliance with Ethical Standards

Conflict of interest

The author declares that he has no conflict of interest.

References

  1. Blumenthal R, Farber MA (November 1, 1991) Policing New Haven: patrols and politics: a special report. Chief with high profile uses streets to test new theories. New York TimesGoogle Scholar
  2. Bolla JR, Agasid MT, Mehmood S, Robinson CV (2019) Membrane protein–lipid interactions probed using mass spectrometry. Annu Rev Biochem 88:85–111CrossRefGoogle Scholar
  3. Chang SB, Alben JO, Wisner DA, Tsai MD (1986) Phospholipids chiral at phosphorus. 11. Phospholipids chiral at phosphorus: Fourier-transform infrared study on the gel-liquid crystalline transition of chiral thiophosphatidylcholine. Biochemistry 25:3435–3440CrossRefGoogle Scholar
  4. Corradi V, Sejdiu BI, Mesa-Galloso H, Abdizadeh H, Noskov SY, Marrink SJ, Tieleman DP (2019) Emerging diversity in lipid–protein interactions. Chem Rev 119:5775–5848PubMedPubMedCentralCrossRefGoogle Scholar
  5. De Loof H, Harvey SC, Segrest JP, Pastor RW (1991) Mean field stochastic boundary molecular dynamics simulation of a phospholipid in a membrane. Biochemistry 30:2099–2113CrossRefGoogle Scholar
  6. Dowhan W, Vitrac H, Bogdanov M (2019) Lipid-assisted membrane protein folding and topogenesis. Protein J 38:274–288CrossRefGoogle Scholar
  7. Dupureur CM, Deng TL, Kwak JG, Noel JP, Tsai MD (1990) Phospholipase-A2 engineering. 4. Can the active-site aspartate-99 function alone. J Am Chem Soc 112:7074–7076CrossRefGoogle Scholar
  8. Holak TA, Prestegard JH (1986) Secondary structure of acyl carrier protein as derived from two-dimensional H1 NMR spectroscopy. Biochemistry 25:5766–5774CrossRefGoogle Scholar
  9. Holak TA, Kearsley SK, Kim Y, Prestegard JH (1988) 3-Dimensional structure of acyl carrier protein determined by NMR pseudoenergy and distance geometry calculations. Biochemistry 27:6135–6142CrossRefGoogle Scholar
  10. Hristova K, Wimley WC, Mishra VK, Anantharamiah GM, Segrest JP, White SH (1999) An amphipathic alpha-helix at a membrane interface: a structural study using a novel X-ray diffraction method. J Mol Biol 290:99–117CrossRefGoogle Scholar
  11. Jones PJ, Holak TA, Prestegard JH (1987) Structural comparison of acyl carrier protein in acylated and sulfhydryl forms by two-dimensional H-1-NMR spectroscopy. Biochemistry 26:3493–3500CrossRefGoogle Scholar
  12. Kay LE, Prestegard JH (1987) Methyl-group dynamics from relaxation of double quantum filtered NMR signals: application to deoxycholate. J Am Chem Soc 109:3829–3835CrossRefGoogle Scholar
  13. Kim YM, Prestegard JH (1990a) Demonstration of a conformational equilibrium in acyl carrier protein from spinach using rotating frame nuclear-magnetic-resonance spectroscopy. J Am Chem Soc 112:3707–3709CrossRefGoogle Scholar
  14. Kim YM, Prestegard JH (1990b) Refinement of the NMR structures for acyl carrier protein with scalar coupling data. Proteins 8:377–385CrossRefGoogle Scholar
  15. Ladokhin AS, White SH (1999) Folding of amphipathic alpha-helices on membranes: energetics of helix formation by melittin. J Mol Biol 285:1363–1369CrossRefGoogle Scholar
  16. Lee AG (2011) Lipid–protein interactions. Biochem Soc Trans 39:761–766CrossRefGoogle Scholar
  17. Li M, Morales HH, Katsaras J, Kucerka N, Yang Y, Macdonald PM, Nieh MP (2013) Morphological characterization of DMPC/CHAPSO bicellar mixtures: a combined SANS and NMR study. Langmuir 29:15943–15957CrossRefGoogle Scholar
  18. Loffredo WM, Tsai MD (1990) Phospholipids chiral at phosphorus. 19. Phospholipids chiral at phosphorus: Synthesis and configurational assignment of phosphorothioate analogs of phosphatidylserine. Bioorg Chem 18:78–84CrossRefGoogle Scholar
  19. MacKenzie KR, Prestegard JH, Engelman DM (1997) A transmembrane helix dimer: structure and implications. Science 276:131–133CrossRefGoogle Scholar
  20. Marinko JT, Huang H, Penn WD, Capra JA, Schlebach JP, Sanders CR (2019) Folding and misfolding of human membrane proteins in health and disease: from single molecules to cellular proteostasis. Chem Rev 119:5537–5606PubMedPubMedCentralCrossRefGoogle Scholar
  21. Muller MP, Jiang T, Sun C, Lihan M, Pant S, Mahinthichaichan P, Trifan A, Tajkhorshid E (2019) Characterization of lipid–protein interactions and lipid-mediated modulation of membrane protein function through molecular simulation. Chem Rev 119:6086–6161CrossRefGoogle Scholar
  22. Noel JP, Tsai MD (1989) Phospholipase-A2 engineering: design, synthesis, and expression of a gene for bovine (pro)phospholipase-A2. J Cell Biochem 40:309–320CrossRefGoogle Scholar
  23. Popot JL, Engelman DM (1990) Membrane protein folding and oligomerization: the two-stage model. Biochemistry 29:4031–4037CrossRefPubMedPubMedCentralGoogle Scholar
  24. Prosser RS, Evanics F, Kitevski JL, Al-Abdul-Wahid MS (2006) Current applications of bicelles in NMR studies of membrane-associated amphiphiles and proteins. Biochemistry 45:8453–8465CrossRefGoogle Scholar
  25. Ram P, Prestegard JH (1988a) Headgroup orientation of a glycolipid analog from deuterium NMR data. J Am Chem Soc 110:2383–2388CrossRefGoogle Scholar
  26. Ram P, Prestegard JH (1988b) Magnetic-field induced ordering of bile-salt phospholipid micelles: new media for NMR structural investigations. Biochim Biophys Acta 940:289–294CrossRefGoogle Scholar
  27. Ram P, Mazzola L, Prestegard JH (1989) Orientational analysis of micelle-associated trehalose using an NMR-pseudoenergy approach. J Am Chem Soc 111:3176–3182CrossRefGoogle Scholar
  28. Rasmussen SGF, Choi HJ, Rosenbaum DM, Kobilka TS, Thian FS, Edwards PC, Burghammer M, Ratnala VRP, Sanishvili R, Fischetti RF, Schertler GFX, Weis WI, Kobilka BK (2007) Crystal structure of the human beta(2) adrenergic G-protein-coupled receptor. Nature 450:U383–U384CrossRefGoogle Scholar
  29. Rierden A (May 26, 1991) Armed youths turn new haven into a battleground. New York TimesGoogle Scholar
  30. Sanders CR (1993) Solid-state C-13 NMR of unlabeled phosphatidylcholine bilayers: spectral assignments and measurement of carbon phosphorus dipolar couplings and C-13 chemical-shift anisotropies. Biophys J 64:171–181PubMedPubMedCentralCrossRefGoogle Scholar
  31. Sanders CR (2006) Development and application of bicelles for use in biological NMR and other biophysical studies. In: Webb GA (ed) Springer, Dordrecht, pp 233–239Google Scholar
  32. Sanders CR, Landis GC (1995) Reconstitution of membrane proteins into lipid-rich bilayered mixed micelles for NMR studies. Biochemistry 34:4030–4040CrossRefGoogle Scholar
  33. Sanders CR, Mittendorf KF (2011) Tolerance to changes in membrane lipid composition as a selected trait of membrane proteins. Biochemistry 50:7858–7867PubMedPubMedCentralCrossRefGoogle Scholar
  34. Sanders CR, Prestegard JH (1990) Magnetically orientable phospholipid-bilayers containing small amounts of a bile-salt analog, Chapso. Biophys J 58:447–460PubMedPubMedCentralCrossRefGoogle Scholar
  35. Sanders CR, Prestegard JH (1991) Orientation and dynamics of beta-dodecyl glucopyranoside in phospholipid-bilayers by oriented sample nmr and order matrix analysis. J Am Chem Soc 113:1987–1996CrossRefGoogle Scholar
  36. Sanders CR, Prestegard JH (1992) Headgroup orientations of alkyl glycosides at a lipid bilayer interface. J Am Chem Soc 114:7096–7107CrossRefGoogle Scholar
  37. Sanders CR, Prosser RS (1998) Bicelles: a model membrane system for all seasons? Struct Fold Des 6:1227–1234CrossRefGoogle Scholar
  38. Sanders CR, Schwonek JP (1992) Characterization of magnetically orientable bilayers in mixtures of dihexanoylphosphatidylcholine and dimyristoylphosphatidylcholine by solid-state NMR. Biochemistry 31:8898–8905PubMedPubMedCentralCrossRefGoogle Scholar
  39. Sanders CR 2nd, Schwonek JP (1993) An approximate model and empirical energy function for solute interactions with a water–phosphatidylcholine interface. Biophys J 65:1207–1218PubMedPubMedCentralCrossRefGoogle Scholar
  40. Sanders CR, Tsai MD (1988) Mechanism of adenylate kinase. 3. Use of deuterium NMR to show lack of correlation between local substrate dynamics and local binding-energy. J Am Chem Soc 110:3323–3324CrossRefGoogle Scholar
  41. Sanders CR, Tian G, Tsai MD (1989) Mechanism of adenylate kinase: is there a relationship between local substrate dynamics, local binding-energy, and the catalytic mechanism. Biochemistry 28:9028–9043CrossRefGoogle Scholar
  42. Sanders CR, Hare BJ, Howard KP, Prestegard JH (1994) Magnetically-oriented phospholipid micelles as a tool for the study of membrane-associated molecules. Prog Nucl Mag Res Spectrosc 26:421–444CrossRefGoogle Scholar
  43. Sarvis HE, Loffredo W, Dluhy RA, Hernqvist L, Wisner DA, Tsai MD (1988) Phospholipids chiral at phosphorus: characterization of the subgel phase of thiophosphatidylcholines by use of X-ray-diffraction, P-31 nuclear magnetic-resonance, and Fourier-transform infrared-spectroscopy. Biochemistry 27:4625–4631CrossRefGoogle Scholar
  44. Singer SJ, Nicolson GL (1972) The fluid mosaic model of the structure of cell membranes. Science 175:720–731CrossRefPubMedGoogle Scholar
  45. Talking Heads (1979) Life during wartime (song). Fear of Music (Album), Sire RecordsGoogle Scholar
  46. Tjandra N, Bax A (1997) Direct measurement of distances and angles in biomolecules by NMR in a dilute liquid crystalline medium. Science 278:1111–1114CrossRefGoogle Scholar
  47. Tolman JR, Flanagan JM, Kennedy MA, Prestegard JH (1995) Nuclear magnetic dipole interactions in field-oriented proteins: information for structure determination in solution. Proc Natl Acad Sci USA 92:9279–9283CrossRefGoogle Scholar
  48. Tsai MD, Noel J, Deng T, Sundaralingam M (1990) Perfecting an enzyme: a phospholipase-A2 with significantly improved catalytic activity. Biochemistry 29:2184Google Scholar
  49. Waldrop MM (1989) Catalytic RNA wins chemistry Nobel. Science 246:325CrossRefGoogle Scholar
  50. Wiener MC, White SH (1992) Structure of a fluid dioleoylphosphatidylcholine bilayer determined by joint refinement of X-ray and neutron diffraction data. III. Complete structure. Biophys J 61:434–447PubMedPubMedCentralCrossRefGoogle Scholar
  51. Wikipedia (1989) 1989 Northeastern United State Tornado outbreak. https://en.wikipedia.org/wiki/1989_Northeastern_United_States_tornado_outbreak
  52. Wisner DA, Rosariojansen T, Tsai MD (1986) Phospholipids chiral at phosphorus. 12. Configurational effect on the thermotropic properties of chiral dipalmitoylthiophosphatidylcholine. J Am Chem Soc 108:8064–8068CrossRefGoogle Scholar
  53. Yeagle PL (2014) Non-covalent binding of membrane lipids to membrane proteins. Biochim Biophys Acta 1838:1548–1559CrossRefGoogle Scholar

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© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of BiochemistryVanderbilt University School of Medicine Basic SciencesNashvilleUSA

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