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A Minireview on Temperature Dependent Protein Conformational Sampling

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Abstract

In this minireview we discuss the role of the more subtle conformational change—protein conformational sampling and connect it to the classic relationship of protein structure and function. The theory of pre-existing functional states of protein are discussed in context of alternate protein conformational sampling. Last, we discuss how temperature, ligand binding and mutations affect the protein conformational sampling mode which is linked to the protein function regulation. The review includes several protein systems that showed temperature dependent protein conformational sampling. We also specifically included two enzyme systems, thermophilic alcohol dehydrogenase (ht-ADH) and thermolysin which we previously studied when discussing temperature dependent protein conformational sampling.

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References

  1. Eisenmesser EZ, Bosco DA, Akke M, Kern D (2002) Enzyme dynamics during catalysis. Science 295(5559):1520–1523. https://doi.org/10.1126/science.1066176

    Article  CAS  PubMed  Google Scholar 

  2. Henzler-Wildman KA, Lei M, Thai V, Kerns SJ, Karplus M, Kern D (2007) A Hierarchy of timescales in protein dynamics is linked to enzyme catalysis. Nature 450(7171):913–916

    Article  CAS  PubMed  Google Scholar 

  3. Henzler-Wildman KA, Thai V, Lei M, Ott M, Wolf-Watz M, Fenn T, Pozharski E et al (2007) Intrinsic motions along an enzymatic reaction trajectory. Nature 450(7171):838–844

    Article  CAS  PubMed  Google Scholar 

  4. Liang ZX, Lee T, Resing KA, Ahn NG, Klinman JP (2004) Thermal-activated protein mobility and its correlation with catalysis in thermophilic alcohol dehydrogenase. Proc Natl Acad Sci 101(26):9556–9561

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Liang ZX, Tsigos I, Lee T, Bouriotis V, Resing KA, Ahn NG, Klinman JP (2004) Evidence for increased local flexibility in psychrophilic alcohol dehydrogenase relative to its thermophilic homologue. Biochemistry 43(46):14676–14683

    Article  CAS  PubMed  Google Scholar 

  6. Wolf-Watz M, Thai V, Henzler-Wildman K, Hadjipavlou G, Eisenmesser EZ, Kern D (2004) Linkage between Dynamics and catalysis in a thermophilic-mesophilic enzyme pair. Nat Struct Mol Biol 11(10):945–949

    Article  CAS  PubMed  Google Scholar 

  7. Tilton RF, Dewan JC, Petsko GA (1992) Effects of temperature on protein structure and dynamics: X-Ray crystallographic studies of the protein Ribonuclease-A at nine different temperatures from 98 to 320 K. Biochemistry 31(9):2469–2481

    Article  CAS  PubMed  Google Scholar 

  8. Tilton RF, Dewan JC, Gregory A, Petsko A (1992) Effects of temperature on protein structure and dynamics: X-Ray crystallographic studies of the protein Ribonuclease-A at nine different temperatures from 98 to 320 K. Biochemistry 31(9):2469–2481. https://doi.org/10.1021/bi00124a006

    Article  CAS  PubMed  Google Scholar 

  9. Závodszky P, Kardos J, Svingor Á, Petsko GA (1998) Adjustment of conformational flexibility is a key event in the thermal adaptation of proteins. Proc Natl Acad Sci USA 95(13):7406–7411. https://doi.org/10.1073/pnas.95.13.7406

    Article  PubMed  PubMed Central  Google Scholar 

  10. Liu Y-H, Konermann L (2008) Conformational dynamics of free and catalytically active thermolysin are indistinguishable by hydrogen/deuterium exchange mass spectrometry. Biochemistry 47(24):6342–6351. https://doi.org/10.1021/bi800463q

    Article  CAS  PubMed  Google Scholar 

  11. Boehr DD, Nussinov R, Wright PE (2009) The role of dynamic conformational ensembles in biomolecular recognition. Nat Chem Biol 5(11):789–796. https://doi.org/10.1038/nchembio.232

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Meadows Corey W, Ryan Ou, Klinman Judith P (2014) Picosecond-resolved fluorescent probes at functionally distinct tryptophans within a thermophilic alcohol dehydrogenase: relationship of temperature-dependent changes in fluorescence to catalysis. J Phys Chem B. https://doi.org/10.1021/jp500825x

    Article  PubMed  PubMed Central  Google Scholar 

  13. Axe Jennifer M, O’Rourke Kathleen F, Kerstetter Nicole E, Yezdimer Eric M, Chan Yan M, Chasin Alexander, Boehr David D (2015) Severing of a hydrogen bond disrupts amino acid networks in the catalytically active state of the alpha subunit of tryptophan synthase. Protein Sci 24:484–94. https://doi.org/10.1002/pro.2598

    Article  CAS  PubMed  Google Scholar 

  14. Axe JM, Yezdimer EM, ’Rourke KFO, Kerstetter NE, You W, Chang C-EA, Boehr DD et al (2014) Amino acid networks in a 8 barrel enzyme change during catalytic turnover. J. Am. Chem. Soc. 136:6818–21. https://doi.org/10.1021/ja501602t

    Article  CAS  PubMed  Google Scholar 

  15. de Kreij A, Van Den Burg B, Venema G, Vriend G, Eijsink VGH, Nielsen JE (2002) The effects of modifying the surface charge on the catalytic activity of a thermolysin-like protease. J Biol Chem 277(18):15432–15438. https://doi.org/10.1074/jbc.M200807200

    Article  CAS  PubMed  Google Scholar 

  16. Doshi U, Holliday MJ, Eisenmesser EZ, Hamelberg D (2016) Dynamical network of residue-residue contacts reveals coupled allosteric effects in recognition, catalysis, and mutation. Proc Natl Acad Sci USA 113(17):4735–4740. https://doi.org/10.1073/pnas.1523573113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Palmer AG (2015) Enzyme dynamics from NMR spectroscopy. Acc Chem Res 48(2):457–465. https://doi.org/10.1021/ar500340a

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Grebner C, Iegre J, Ulander J, Edman K, Hogner A, Tyrchan C (2016) Binding mode and induced fit predictions for prospective computational drug design. J Chem Inf Model 56(4):774–787. https://doi.org/10.1021/acs.jcim.5b00744

    Article  CAS  PubMed  Google Scholar 

  19. Dong YW, Liao ML, Meng XL, Somero GN (2018) Structural flexibility and protein adaptation to temperature: molecular dynamics analysis of malate dehydrogenases of marine molluscs. Proc Natl Acad Sci USA 115(6):1274–1279. https://doi.org/10.1073/pnas.1718910115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Ollikainen N, Smith CA, Fraser JS, Kortemme T (2013) Methods in enzymology: " flexible backbone sampling methods to model and design protein alternative conformations &quot. Methods Enzymol. https://doi.org/10.1016/B978-0-12-394292-0.00004-7

    Article  PubMed  PubMed Central  Google Scholar 

  21. Wall ME, Van Benschoten AH, Sauter NK, Adams PD, Fraser JS, Terwilliger TC (2014) Conformational dynamics of a crystalline protein from microsecond-scale molecular dynamics simulations and diffuse X-Ray scattering. Proc Natl Acad Sci USA 111(50):17887–17892. https://doi.org/10.1073/pnas.1416744111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Heilmann N, Wolf M, Kozlowska M, Sedghamiz E, Setzler J, Brieg M, Wenzel W (2020) Sampling of the conformational landscape of small proteins with Monte Carlo methods. Sci Rep 10(1):1–13. https://doi.org/10.1038/s41598-020-75239-7

    Article  CAS  Google Scholar 

  23. Campbell EC, Correy GJ, Mabbitt PD, Buckle AM, Tokiriki N, Jackson CJ (2018) Laboratory evolution of protein conformational dynamics. Curr Opin Struct Biol 50:49–57. https://doi.org/10.1016/j.sbi.2017.09.005

    Article  CAS  PubMed  Google Scholar 

  24. Campbell E, Kaltenbach M, Correy GJ, Carr PD, Porebski BT, Livingstone EK, Afriat-Jurnou L et al (2016) The role of protein dynamics in the evolution of new enzyme function. Nat Chem Biol 12(11):944–950. https://doi.org/10.1038/nchembio.2175

    Article  CAS  PubMed  Google Scholar 

  25. Klinman JP, Offenbacher AR, Shenshen Hu (2017) Origins of enzyme catalysis: experimental findings for C-H activation, new models, and their relevance to prevailing theoretical constructs. J Am Chem Soc 139(51):18409–18427. https://doi.org/10.1021/jacs.7b08418

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Katava M, Stirnemann G, Zanatta M, Capaccioli S, Maria Pachetti KL, Ngai FS, Paciaroni A (2017) Critical structural fluctuations of proteins upon thermal unfolding challenge the lindemann criterion. Proc Natl Acad Sci USA 114(35):9361–9366. https://doi.org/10.1073/pnas.1707357114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Norn C, Wicky BIM, Juergens D, Liu S, Kim D, Tischer D, Koepnick B et al (2021) Protein sequence design by conformational landscape optimization. Proc Natl Acad Sci USA 118(11):1–7. https://doi.org/10.1073/PNAS.2017228118

    Article  Google Scholar 

  28. Davey JA, Damry AM, Goto NK, Chica RA (2017) Rational design of proteins that exchange on functional timescales. Nat Chem Biol 13(12):1280–1285. https://doi.org/10.1038/nchembio.2503

    Article  CAS  PubMed  Google Scholar 

  29. Oyeyemi OA, Sours KM, Lee T, Resing KA, Ahn NG, Klinman JP (2010) Temperature dependence of protein motions in a thermophilic dihydrofolate reductase and its relationship to catalytic efficiency. Proc Natl Acad Sci 107(22):10074–79. https://doi.org/10.1073/pnas.1003678107

    Article  PubMed  PubMed Central  Google Scholar 

  30. Rasmussen BF, Stock AM, Ringe D, Petsko GA (1992) Crystalline ribonuclease a loses function below the dynamical transition at 220 K. Nature 357(6377):423–424

    Article  CAS  PubMed  Google Scholar 

  31. Dong M, Lauro ML, Koblish TJ, Bahnson BJ (2020) Conformational Sampling and kinetics changes across a non-arrhenius break point in the enzyme thermolysin. Struct Dyn 014101:1–11. https://doi.org/10.1063/1.5130582

    Article  CAS  Google Scholar 

  32. Nagel ZD, Dong M, Bahnson BJ, Klinman JP (2011) Impaired protein conformational landscapes as revealed in anomalous Arrhenius Prefactors. Proc Natl Acad Sci 108(26):10520–10525

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Nagel ZD, Medows CW, Dong M, Bahnson BJ, Klinman JP (2012) Active site hydrophobic residues impact hydrogen tunneling differently in a thermophilic alcohol dehydrogenase at optimal versus nonoptimal temperatures. Biochemistry 51(20):4147–4156

    Article  CAS  PubMed  Google Scholar 

  34. Nagel Zachary D, Meadows Corey W, Dong Ming, Bahnson Brian J, Klinman Judith P (2012) Active site hydrophobic residues impact hydrogen tunneling differently in a thermophilic alcohol dehydrogenase at optimal versus nonoptimal temperatures. Biochemistry. https://doi.org/10.1021/bi3001352

    Article  PubMed  Google Scholar 

  35. Nocek JM, Stemp EDA, Finnegan MG, Koshy TI, Johnson MK, Margoliash E, Mauk AG, Smith IM, Hoffman BM (1991) Low-temperature, cooperative conformational transition within [Zn-Cytochrome c Peroxidase, Cytochrome c Complexes: Variation with Cytochrome]. J Am Chem Soc 113(6):6822–6831

    Article  CAS  Google Scholar 

  36. Doster W, Cusack S, Petry W (1989) Dynamical transition of myoglobin revealed by inelastic neutron scattering. Letters to Nature 337(23):754–756

    Article  CAS  Google Scholar 

  37. Ostermann A, Waschipky R, Parak FG, Nienhaus GU (2000) Ligand binding and conformational motions in myoglobin. Nature 404(6774):205–208. https://doi.org/10.1038/35004622

    Article  CAS  PubMed  Google Scholar 

  38. Kohen A, Cannio R, Bartoluccl S, Klinman JP, Bartolucci S, Klinman JP (1999) Enzyme dynamics and hydrogen tunnelling in a thermophilic alcohol dehydrogenase. Nature 399(6735):496–499. https://doi.org/10.1038/20981

    Article  CAS  PubMed  Google Scholar 

  39. Schotte F, Lim M, Jackson TA, Smirnov AV, Soman J, Olson JS, Phillips GN, Wulff M, Anfinrud PA (2003) Watching a protein as it functions with 150-Ps time-resolved x-Ray crystallography. Science 300(5627):1944–47. https://doi.org/10.1126/science.1078797

    Article  CAS  PubMed  Google Scholar 

  40. Hammes-Schiffer S, Benkovic SJ (2006) Relating protein motion to catalysis. Annu Rev Biochem 75:519–541. https://doi.org/10.1146/annurev.biochem.75.103004.142800

    Article  CAS  PubMed  Google Scholar 

  41. Shenshen Hu, Sharma Sudhir C, Scouras Alexander D, Soudackov Alexander V, Marcus Cody A, Carr Sharon Hammes-Schiffer, Alber Tom, Klinman Judith P (2014) Extremely elevated room-temperature kinetic isotope effects quantify the critical role of barrier width in enzymatic C-H activation. J Am Chem Soc. https://doi.org/10.1021/ja502726s

    Article  Google Scholar 

  42. Keedy DA, Fraser JS, van den Bedem H (2015) Exposing hidden alternative backbone conformations in X-Ray crystallography using QFit. PLoS Comput Biol 11(10):1–22. https://doi.org/10.1371/journal.pcbi.1004507

    Article  CAS  Google Scholar 

  43. Keedy DA, Kenner LR, Warkentin M, Woldeyes RA, Hopkins JB, Thompson MC, Brewster AS et al (2015) Mapping the conformational landscape of a dynamic enzyme by multitemperature and XFEL crystallography. Elife 4(7574):1–26. https://doi.org/10.7554/eLife.07574

    Article  Google Scholar 

  44. Réat V, Patzelt H, Ferrand M, Pfister C, Oesterhelt D, Zaccai G (1998) Dynamics of different functional parts of bacteriorhodopsin: H-2H labeling and neutron scattering. Proc Natl Acad Sci USA 95(9):4970–4975. https://doi.org/10.1073/pnas.95.9.4970

    Article  PubMed  PubMed Central  Google Scholar 

  45. Zaccai Giuseppe (2000) How soft is a protein? A protein dynamics force constant measured by neutron scattering. Science (New York, N.Y.) 288(5471):1604–7. https://doi.org/10.1126/science.288.5471.1604

    Article  CAS  Google Scholar 

  46. Petsko GA, Ringe D (1984) Fluctuations in protein structure from X-Ray diffraction. Annu Rev Biophys Bioeng. https://doi.org/10.1146/annurev.bb.13.060184.001555

    Article  PubMed  Google Scholar 

  47. Sun Z, Liu Q, Ge Qu, Feng Y, Reetz MT (2019) Utility of B-factors in protein science: interpreting rigidity, flexibility, and internal motion and engineering thermostability. Chem Rev. https://doi.org/10.1021/acs.chemrev.8b00290

    Article  PubMed  PubMed Central  Google Scholar 

  48. Fraser JS, van den Bedem H, Samelson AJ, Therese Lang P, Holton JM, Echols N, Alber T (2011) Accessing protein conformational ensembles using room-temperature X-Ray crystallography. Proc Natl Acad Sci USA 108(39):16247–16252. https://doi.org/10.1073/pnas.1111325108

    Article  PubMed  PubMed Central  Google Scholar 

  49. Lang PT, Ng HL, Fraser JS, Corn JE, Echols N, Sales M, Holton JM, Alber T (2010) Automated electron-density sampling reveals widespread conformational polymorphism in proteins. Protein Sci 19(7):1420–1431

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Fraser JS, Clarkson MW, Degnan SC, Erion R, Kern D, Alber T (2009) Hidden alternative structures of proline isomerase essential for catalysis. Nature 462(7273):669–673

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Kao TY, Tsai CJ, Lan YJ, Chiang YW (2017) The role of conformational heterogeneity in regulating the apoptotic activity of BAX protein. Phys Chem Chem Phys 19(14):9584–9591. https://doi.org/10.1039/c7cp00401j

    Article  CAS  PubMed  Google Scholar 

  52. Zhang XH, Bruice TC (2007) Temperature-dependent structure of the E x S complex of bacillus stearothermophilus alcohol dehydrogenase. Biochemistry 46(3):837–843

    Article  CAS  PubMed  Google Scholar 

  53. Glass DC, Krishnan M, Nutt DR, Smith JC (2010) Temperature dependence of protein dynamics simulated with three different water models. J Chem Theory Comput 6(4):1390–1400. https://doi.org/10.1021/ct9006508

    Article  CAS  Google Scholar 

  54. Merkley ED, Parson WW, Daggett V (2010) Temperature dependence of the flexibility of thermophilic and mesophilic flavoenzymes of the nitroreductase fold. Protein Eng Des Sel 23(5):327–336. https://doi.org/10.1093/protein/gzp090

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Childers MC, Daggett V (2018) Validating molecular dynamics simulations against experimental observables in light of underlying conformational ensembles. J Phys Chem B 122(26):6673–6689. https://doi.org/10.1021/acs.jpcb.8b02144

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Michetti Davide, Brandsdal Bjørn Olav, Bon Davide, Isaksen Geir Villy, Tiberti Matteo, Papaleo Elena (2017) A comparative study of cold-and warmadapted endonucleases a using sequence analyses and molecular dynamics simulations. PLoS One. https://doi.org/10.1371/journal.pone.0169586

    Article  PubMed  PubMed Central  Google Scholar 

  57. Bowman GR, Geissler PL (2014) Extensive conformational heterogeneity within protein cores. J Phys Chem B 19(24):6417–6423. https://doi.org/10.1021/jp4105823

    Article  CAS  Google Scholar 

  58. Jephthah S, Staby L, Kragelund BB, Skepö M (2019) Temperature dependence of intrinsically disordered proteins in simulations: what are we missing? J Chem Theory Comput 15(4):2672–2683. https://doi.org/10.1021/acs.jctc.8b01281

    Article  CAS  PubMed  Google Scholar 

  59. Sang Peng, Liu Shu Qun, Yang Li Quan (2020) New insight into mechanisms of protein adaptation to high temperatures: a comparative molecular dynamics simulation study of thermophilic and mesophilic subtilisin-like serine proteases. Int J Mol Sci. https://doi.org/10.3390/ijms21093128

    Article  PubMed  PubMed Central  Google Scholar 

  60. Adamczyk AJ, Cao J, Kamerlin SCL, Warshel A (2011) Catalysis by dihydrofolate reductase and other enzymes arises from electrostatic preorganization, not conformational motions. Proc Natl Acad Sci USA 108(34):14115–14120. https://doi.org/10.1073/pnas.1111252108

    Article  PubMed  PubMed Central  Google Scholar 

  61. Levsh O, Chiang YC, Tung CF, Noel JP, Wang Yi, Weng JK (2016) Dynamic conformational states dictate selectivity toward the native substrate in a substrate-permissive acyltransferase. Biochemistry 55(45):6314–6326. https://doi.org/10.1021/acs.biochem.6b00887

    Article  CAS  PubMed  Google Scholar 

  62. Jiménez-Osés G, Osuna S, Gao X, Sawaya MR, Gilson L, Collier SJ, Huisman GW, Yeates TO, Tang Yi, Houk KN (2018) The role of distant mutations and allosteric regulation on LovD active site dynamics. Physiol Behav 176(5):139–148. https://doi.org/10.1038/nchembio.1503.The

    Article  Google Scholar 

  63. Gardner JM, Biler M, Risso VA, Sanchez-Ruiz JM, Kamerlin SCL (2020) Manipulating conformational dynamics to repurpose ancient proteins for modern catalytic functions. ACS Catal 10(9):4863–4870. https://doi.org/10.1021/acscatal.0c00722

    Article  CAS  Google Scholar 

  64. Bhabha Gira, Biel Justin T, Fraser James S (2015) Keep on moving: discovering and perturbing the conformational dynamics of enzymes. Acc Chem Res 48(2):423–30. https://doi.org/10.1021/ar5003158

    Article  CAS  PubMed  Google Scholar 

  65. Doyle CM, Rumfeldt JA, Broom HR, Sekhar A, Kay LE, Meiering EM (2016) Concurrent increases and decreases in local stability and conformational heterogeneity in Cu, Zn superoxide dismutase variants revealed by temperature-dependence of amide chemical shifts. Biochemistry 55(9):1346–1361. https://doi.org/10.1021/acs.biochem.5b01133

    Article  CAS  PubMed  Google Scholar 

  66. van den Bedem H, Bhabha G, Yang K, Wright PE, Fraser JS (2013) Automated identification of functional dynamic contact networks from x-ray crystallography. Nat Methods 10(9):896–902. https://doi.org/10.1038/nmeth.2592

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Romero-Rivera A, Garcia-Borràs M, Osuna S (2017) Role of conformational dynamics in the evolution of retro-aldolase activity. ACS Catal 7(12):8524–8532. https://doi.org/10.1021/acscatal.7b02954

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Kaczmarski JA, Mahawaththa MC, Feintuch A, Clifton BE, Adams LA, Goldfarb D, Otting G, Jackson CJ (2020) Altered conformational sampling along an evolutionary trajectory changes the catalytic activity of an enzyme. Nat Commun 11(1):1–32. https://doi.org/10.1038/s41467-020-19695-9

    Article  CAS  Google Scholar 

  69. Perticaroli S, Nickels JD, Ehlers G, Mamontov E, Sokolov AP (2014) Dynamics and rigidity in an intrinsically disordered protein, β-casein. J Phys Chem B 118(26):7317–7326. https://doi.org/10.1021/jp503788r

    Article  CAS  PubMed  Google Scholar 

  70. Döring K, Surrey T, Nollert P, Jähnig F (1999) Effects of ligand binding on the internal dynamics of maltose-binding protein. FEBS J 266(2):477–483

    Google Scholar 

  71. Lang PT, Holton JM, Fraser JS, Alber T (2014) Protein structural ensembles are revealed by redefining X-Ray electron density noise. Proc Natl Acad Sci USA 111(1):237–242. https://doi.org/10.1073/pnas.1302823110

    Article  CAS  PubMed  Google Scholar 

  72. Callaway E (2020) ‘It will change everything’: deepmind’s ai makes gigantic leap in solving protein structures. Nature 588(7837):203–204. https://doi.org/10.1038/d41586-020-03348-4

    Article  CAS  PubMed  Google Scholar 

  73. Hong Nan-Sook, Petrović Dušan, Lee Richmond, Gryn’ova Ganna, Purg Miha, Saunders Jake, Bauer Paul, Carr Paul D, Lin Ching-Yeh, Mabbitt Peter D, Zhang William, Altamore Timothy, Easton Chris, Coote Michelle L, Kamerlin Shina C. L, Jackson Colin J (2018) The evolution of multiple active site configurations in a designed enzyme. Nat Commun. https://doi.org/10.1038/s41467-018-06305-y

    Article  PubMed  PubMed Central  Google Scholar 

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Dong, M. A Minireview on Temperature Dependent Protein Conformational Sampling. Protein J 40, 545–553 (2021). https://doi.org/10.1007/s10930-021-10012-x

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