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Membranes as the third genetic code

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Abstract

Biological membranes and their compositions influence cellular function, age and disease states of organisms. They achieve this by effecting the outcome of bound enzymes/proteins and carbohydrate moieties. While the membrane-bound carbohydrates give rise to antigenicity, membranes impact the eventual outcome of protein structures that would function even outside their enclosure. This is achieved by membrane modulation of translational and post-translational protein folding. Thus, the eventual 3D structures and functions of proteins might not be solely dependent on their primary amino acid sequences and surrounding environments. The 3D protein structures would also depend on enclosing membrane properties such as fluidity, other intrinsic and extrinsic proteins and carbohydrate functionalities. Also, membranes moderate DNA activities with consequences on gene activation–inactivation mechanisms. Consequently, membranes are almost indispensable to the functioning of other cell compositions and serve to modulate these other components. Besides, membrane lipid compositions are also moderated by nutrition and diets and the converse is true. Thus, it could be argued that membranes are the third genetic codes. Suggestively, membranes are at the center of the interplay between nature and nurture in health and disease states.

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References

  1. Anfinsen CB (1973) Principles that govern the folding of protein chains. Science 181:223–230. https://doi.org/10.1126/science.181.4096.223

    Article  CAS  PubMed  Google Scholar 

  2. Laage D, Elsaesser T, Hynes JT (2017) Water dynamics in the hydration shells of biomolecules. Chem Rev 117:10694–10725. https://doi.org/10.1021/acs.chemrev.6b00765

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Bianco V, Pagès-Gelabert N, Coluzza I, Franzese G (2017) How the stability of a folded protein depends on interfacial water properties and residue-residue interactions. J Mol Liq. https://doi.org/10.1016/j.molliq.2017.08.026

    Article  Google Scholar 

  4. Bellissent-Funel MC, Hassanali A, Havenith M et al (2016) Water determines the structure and dynamics of proteins. Chem Rev 116:7673–7697. https://doi.org/10.1021/acs.chemrev.5b00664

    Article  CAS  PubMed  Google Scholar 

  5. Wigley WC, Corboy MJ, Cutler TD et al (2002) A protein sequence that can encode native structure by disfavoring alternate conformations. Nat Struct Biol. https://doi.org/10.1038/nsb784

    Article  PubMed  Google Scholar 

  6. Richardson JS (1981) The anatomy and taxonomy of protein structure. Adv Protein Chem. https://doi.org/10.1016/S0065-3233(08)60520-3

    Article  PubMed  Google Scholar 

  7. Pandurangan S, Khader S, Sreenivasan R et al (2010) A bioinformatics protocol for the identification of spatial clusters and the calculation of higher order residue interactions in protein structures. Protoc Exch. https://doi.org/10.1038/nprot.2010.91

    Article  Google Scholar 

  8. Alberts B, Johnson A, Lewis J, et al. (2002), Molecular Biology of the Cell, 4th edn. Garland Science, New York

  9. Redfern OC, Dessailly B, Orengo CA (2008) Exploring the structure and function paradigm. Curr Opin Struct Biol 18:394–402. https://doi.org/10.1016/j.sbi.2008.05.007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Lee D, Redfern O, Orengo C (2007) Predicting protein function from sequence and structure. Nat Rev Mol Cell Biol 8:995–1005. https://doi.org/10.1038/nrm2281

    Article  CAS  PubMed  Google Scholar 

  11. Stetefeld J, Ruegg MA (2005) Structural and functional diversity generated by alternative mRNA splicing. Trends Biochem Sci 30:515–521. https://doi.org/10.1016/j.tibs.2005.07.001

    Article  CAS  PubMed  Google Scholar 

  12. Tompa P, Szász C, Buday L (2005) Structural disorder throws new light on moonlighting. Trends Biochem Sci. https://doi.org/10.1016/j.tibs.2005.07.008

    Article  PubMed  Google Scholar 

  13. Min KW, Lee SH, Baek SJ (2016) Moonlighting proteins in cancer. Cancer Lett 370:108–116. https://doi.org/10.1016/j.canlet.2015.09.022

    Article  CAS  PubMed  Google Scholar 

  14. Jaffe EK (2005) Morpheeins—a new structural paradigm for allosteric regulation. Trends Biochem Sci. https://doi.org/10.1016/j.tibs.2005.07.003

    Article  PubMed  Google Scholar 

  15. Nwamba CO, Ibrahim K (2014) The role of protein conformational switches in pharmacology: its implications in metabolic reprogramming and protein evolution. Cell Biochem Biophys. https://doi.org/10.1007/s12013-013-9748-8

    Article  PubMed  Google Scholar 

  16. Michielssens S, Peters JH, Ban D et al (2014) A designed conformational shift to control protein binding specificity. Angew Chem Int Ed Engl. https://doi.org/10.1002/anie.201403102

    Article  PubMed  PubMed Central  Google Scholar 

  17. Ma B, Nussinov R (2016) Protein dynamics: conformational footprints. Nat Chem Biol 12:890–891. https://doi.org/10.1038/nchembio.2212

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Liu J, Nussinov R (2016) Allostery: an overview of its history, concepts, methods, and applications. PLoS Comput Biol 12:e1004966. https://doi.org/10.1371/journal.pcbi.1004966

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Nussinov R (2016) Introduction to protein ensembles and allostery. Chem Rev. https://doi.org/10.1021/acs.chemrev.6b00283

    Article  PubMed  PubMed Central  Google Scholar 

  20. Forman-Kay JD, Mittag T (2013) From sequence and forces to structure, function, and evolution of intrinsically disordered proteins. Structure 21:1492–1499. https://doi.org/10.1016/j.str.2013.08.001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Mohan A, Uversky VN, Radivojac P (2009) Influence of sequence changes and environment on intrinsically disordered proteins. PLoS Comput Biol. https://doi.org/10.1371/journal.pcbi.1000497

    Article  PubMed  PubMed Central  Google Scholar 

  22. Oldfield CJ, Dunker AK (2014) Intrinsically disordered proteins and intrinsically disordered protein regions. Annu Rev Biochem. https://doi.org/10.1146/annurev-biochem-072711-164947

    Article  PubMed  Google Scholar 

  23. Van Regenmortel MHV (2002) A paradigm shift is needed in proteomics: “structure determines function” should be replaced by “binding determines function”. J Mol Recognit 15:349–351. https://doi.org/10.1002/jmr.603

    Article  CAS  PubMed  Google Scholar 

  24. Dyson HJ, Wright PE (2005) Intrinsically unstructured proteins and their functions. Nat Rev Mol Cell Biol 6:349–351. https://doi.org/10.1038/nrm1589

    Article  CAS  Google Scholar 

  25. Arai M, Sugase K, Dyson HJ, Wright PE (2015) Conformational propensities of intrinsically disordered proteins influence the mechanism of binding and folding. Proc Natl Acad Sci. USA. https://doi.org/10.1073/pnas.1512799112

    Article  PubMed  Google Scholar 

  26. Clancy S, Brown W (2008) Translation : DNA to mRNA to protein. Nat Educ 1:101

    Google Scholar 

  27. Kozak M (1984) Point mutations close to the AUG initiator codon affect the efficiency of translation of rat preproinsulin in vivo. Nature. https://doi.org/10.1038/308241a0

    Article  PubMed  Google Scholar 

  28. Borel AC, Simon SM (1996) Biogenesis of polytopic membrane proteins: membrane segments assemble within translocation channels prior to membrane integration. Cell. https://doi.org/10.1016/S0092-8674(00)81116-2

    Article  PubMed  Google Scholar 

  29. Hung D, Falcone D, Lin J et al (1996) The cotranslational integration of membrane proteins into the phospholipid bilayer is a multistep process. Cell. https://doi.org/10.1016/S0092-8674(00)81115-0

    Article  Google Scholar 

  30. Heinrich SU, Mothes W, Brunner J, Rapoport TA (2000) The Sec61p complex mediates the integration of a membrane protein by allowing lipid partitioning of the transmembrane domain. Cell. https://doi.org/10.1016/S0092-8674(00)00028-3

    Article  PubMed  Google Scholar 

  31. Langecker M, Arnaut V, List J, Simmel FC (2014) DNA nanostructures interacting with lipid bilayer membranes. Acc Chem Res. https://doi.org/10.1021/ar500051r

    Article  PubMed  Google Scholar 

  32. Antipina AY, Gurtovenko AA (2015) Molecular mechanism of calcium-induced adsorption of DNA on zwitterionic phospholipid membranes. J Phys Chem B. https://doi.org/10.1021/acs.jpcb.5b01256

    Article  PubMed  Google Scholar 

  33. Cockburn JJB, Abrescia NGA, Grimes JM et al (2004) Membrane structure and interactions with protein and DNA in bacteriophage PRD1. Nature. https://doi.org/10.1038/nature03053

    Article  PubMed  Google Scholar 

  34. Seitz P, Blokesch M (2014) DNA transport across the outer and inner membranes of naturally transformable vibrio cholerae is spatially but not temporally coupled. mBio. https://doi.org/10.1128/mbio.01409-14

    Article  PubMed  PubMed Central  Google Scholar 

  35. Burton B, Dubnau D (2010) Membrane-associated DNA transport machines. Cold Spring Harb Perspect Biol 2:a000406. https://doi.org/10.1101/cshperspect.a000406

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Huang K-T, Han TH, Hyduke DR et al (2002) Modulation of nitric oxide bioavailability by erythrocytes. Proc Natl Acad Sci USA. https://doi.org/10.1073/pnas.201276698

    Article  PubMed  Google Scholar 

  37. Singer SJ, Nicolson GL (1972) The fluid mosaic model of the structure of cell membranes. Science. https://doi.org/10.1126/science.175.4023.720

    Article  PubMed  Google Scholar 

  38. Tomita M (2001) Whole-cell simulation: a grand challenge of the 21st century. Trends Biotechnol 19:205–210. https://doi.org/10.1016/S0167-7799(01)01636-5

    Article  CAS  PubMed  Google Scholar 

  39. Stuart MJ, Nagel RL, Jefferson T (2004) Sickle-cell disease. Lancet 364:1343–1360

    Article  Google Scholar 

  40. Connor J, Bucana C, Fidler IJ, Schroit AJ (2006) Differentiation-dependent expression of phosphatidylserine in mammalian plasma membranes: quantitative assessment of outer-leaflet lipid by prothrombinase complex formation. Proc Natl Acad Sci USA. https://doi.org/10.1073/pnas.86.9.3184

    Article  PubMed  Google Scholar 

  41. Bogdanov M, Dowhan W (1998) Phospholipid-assisted protein folding: phosphatidylethanolamine is required at a late step of the conformational maturation of the polytopic membrane protein lactose permease. EMBO J. https://doi.org/10.1093/emboj/17.18.5255

    Article  PubMed  PubMed Central  Google Scholar 

  42. Bogdanov M, Dowhan W (1999) Lipid-assisted protein folding. J Biol Chem 274:36827–36830. https://doi.org/10.1074/jbc.274.52.36827

    Article  CAS  PubMed  Google Scholar 

  43. Mitchell DC (2012) Progress in understanding the role of lipids in membrane protein folding. Biochim Biophys Acta 1818:951–956. https://doi.org/10.1016/j.bbamem.2011.12.029

    Article  CAS  PubMed  Google Scholar 

  44. Fiedler S, Broecker J, Keller S (2010) Protein folding in membranes. Cell Mol Life Sci 67:1779–1798. https://doi.org/10.1007/s00018-010-0259-0

    Article  CAS  PubMed  Google Scholar 

  45. Mogensen JE, Otzen DE (2005) Interactions between folding factors and bacterial outer membrane proteins. Mol Microbiol 57:326–346. https://doi.org/10.1111/j.1365-2958.2005.04674.x

    Article  CAS  PubMed  Google Scholar 

  46. Killian JA, Van Meer G (2001) The “double lives” of membrane lipids. EMBO Rep. https://doi.org/10.1093/embo-reports/kve029

    Article  PubMed  PubMed Central  Google Scholar 

  47. Schmitz ML, Dos Santos Silva MA, Altmann H et al (1994) Structural and functional analysis of the NF-κB p65 C terminus. An acidic and modular transactivation domain with the potential to adopt an α-helical conformation. J Biol Chem 269:25613–25620

    CAS  PubMed  Google Scholar 

  48. Sachs JN, Engelman DM (2006) Introduction to the membrane protein reviews: the interplay of structure, dynamics, and environment in membrane protein function. Annu Rev Biochem 75:707–712. https://doi.org/10.1146/annurev.biochem.75.110105.142336

    Article  CAS  PubMed  Google Scholar 

  49. Mucsi Z, Hudecz F, Hollósi M et al (2009) Binding-induced folding transitions in calpastatin subdomains A and C. Protein Sci 12:2327–2336. https://doi.org/10.1110/ps.03138803

    Article  CAS  Google Scholar 

  50. San Miguel M, Marrington R, Rodger PM et al (2003) An Escherichia coli twin-arginine signal peptide switches between helical and unstructured conformations depending on the hydrophobicity of the environment. Eur J Biochem 270:3345–3352. https://doi.org/10.1046/j.1432-1033.2003.03710.x

    Article  CAS  PubMed  Google Scholar 

  51. Jewett AI, Baumketner A, Shea JE (2004) Accelerated folding in the weak hydrophobic environment of a chaperonin cavity: creation of an alternate fast folding pathway. Proc Natl Acad Sci U S A 101:13192–13197. https://doi.org/10.1073/pnas.0400720101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Baldwin RL, Rose GD (2016) How the hydrophobic factor drives protein folding. Proc Natl Acad Sci U S A 113:12462–12466. https://doi.org/10.1073/pnas.1610541113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Koldewey P, Stull F, Horowitz S et al (2016) Forces driving chaperone action. Cell 166:369–379. https://doi.org/10.1016/j.cell.2016.05.054

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Boyd D, Manoil C, Beckwith JON (1987) Determinants of membrane protein topology. Proc Natl Acad Sci USA 84:8525–8529

    Article  CAS  Google Scholar 

  55. Dowhan W, Bogdanov M (2015) Lipid–protein interactions as determinants of membrane protein structure and function. Biochem Soc Trans. https://doi.org/10.1042/bst0390767

    Article  Google Scholar 

  56. Bogdanov M, Dowhan W, Vitrac H (2014) Lipids and topological rules governing membrane protein assembly. Biochim Biophys Acta 1843:1475–1488. https://doi.org/10.1016/j.bbamcr.2013.12.007

    Article  CAS  PubMed  Google Scholar 

  57. Lee H, Kim H (2014) Membrane topology of transmembrane proteins: Determinants and experimental tools. Biochem Biophys Res Commun 453:268–276. https://doi.org/10.1016/j.bbrc.2014.05.111

    Article  CAS  PubMed  Google Scholar 

  58. Dowhan W, Vitrac H, Bogdanov M (2019) Lipid-assisted membrane protein folding and topogenesis. Protein J 38:274–288. https://doi.org/10.1007/s10930-019-09826-7

    Article  CAS  PubMed  Google Scholar 

  59. Los DA, Murata N (2004) Membrane fluidity and its roles in the perception of environmental signals. Biochim Biophys Acta 1666:142–157. https://doi.org/10.1016/j.bbamem.2004.08.002

    Article  CAS  PubMed  Google Scholar 

  60. McMahon HT, Gallop JL (2005) Membrane curvature and mechanisms of dynamic cell membrane remodelling. Nature 438:590–596. https://doi.org/10.1038/nature04396

    Article  CAS  PubMed  Google Scholar 

  61. Donaldson JG, Jackson CL (2011) ARF family G proteins and their regulators: roles in membrane transport, development and disease. Nat Rev Mol Cell Biol 12:362–375. https://doi.org/10.1038/nrm3117

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Pomorski T, Hrafnsdóttir S, Devaux PF, Van Meer G (2001) Lipid distribution and transport across cellular membranes. Semin Cell Dev Biol. https://doi.org/10.1006/scdb.2000.0231

    Article  PubMed  Google Scholar 

  63. Vanderheyden PML, Benachour N (2017) Influence of the cellular environment on ligand binding kinetics at membrane-bound targets. Bioorganic Med Chem Lett 27:3621–3628. https://doi.org/10.1016/j.bmcl.2017.06.051

    Article  CAS  Google Scholar 

  64. Strasser A, Wittmann HJ, Seifert R (2017) Binding kinetics and pathways of ligands to GPCRs. Trends Pharmacol Sci 38:717–732. https://doi.org/10.1016/j.tips.2017.05.005

    Article  CAS  PubMed  Google Scholar 

  65. Wu W, Shi X, Xu C (2016) Regulation of T cell signalling by membrane lipids. Nat Rev Immunol 16:690–701. https://doi.org/10.1038/nri.2016.103

    Article  CAS  PubMed  Google Scholar 

  66. Diaz M, Sanchez-Barrena MJ, Gonzalez-Rubio JM et al (2015) Calcium-dependent oligomerization of CAR proteins at cell membrane modulates ABA signaling. Proc Natl Acad Sci USA. https://doi.org/10.1073/pnas.1512779113

    Article  PubMed  Google Scholar 

  67. Spector AA, Yorek MA (1985) Membrane lipid composition and cellular function. J Lipid Res 26:1015–1035

    CAS  PubMed  Google Scholar 

  68. Connor WE, Lin DS, Thomas G et al (1997) Abnormal phospholipid molecular species of erythrocytes in sickle cell anemia. J Lipid Res 38:2516–2528

    CAS  PubMed  Google Scholar 

  69. Grouleff J, Irudayam SJ, Skeby KK, Schiøtt B (2015) The influence of cholesterol on membrane protein structure, function, and dynamics studied by molecular dynamics simulations. Biochim Biophys Acta 1848:1783–1795. https://doi.org/10.1016/j.bbamem.2015.03.029

    Article  CAS  PubMed  Google Scholar 

  70. Jurczyszyn A, Czepiel J, Gdula-Argasińska J et al (2014) Erythrocyte membrane fatty acids in multiple myeloma patients. Leuk Res. https://doi.org/10.1016/j.leukres.2014.08.009

    Article  PubMed  Google Scholar 

  71. Alvarez E, Santa-María C, Ruiz-Gutiérrez V, Sobrino F (2001) Age-related changes in membrane lipid composition, fluidity and respiratory burst in rat peritoneal neutrophils. Clin Exp Immunol. https://doi.org/10.1046/j.1365-2249.2001.01490.x

    Article  PubMed  PubMed Central  Google Scholar 

  72. Clamp AG, Ladha S, Clark DC et al (1997) The influence of dietary lipids on the composition and membrane fluidity of rat hepatocyte plasma membrane. Lipids. https://doi.org/10.1007/s11745-997-0022-3

    Article  PubMed  Google Scholar 

  73. Abbott SK, Else PL, Atkins TA, Hulbert AJ (2012) Fatty acid composition of membrane bilayers: importance of diet polyunsaturated fat balance. Biochim Biophys Acta. https://doi.org/10.1016/j.bbamem.2012.01.011

    Article  PubMed  PubMed Central  Google Scholar 

  74. Field CJ, Ryan EA, Thomson ABR, Clandinin MT (1990) Diet fat composition alters membrane phospholipid composition, insulin binding, and glucose metabolism in adipocytes from control and diabetic animals. J Biol Chem 265:11143–11150

    CAS  PubMed  Google Scholar 

  75. Raatz SK, Bibus D, Thomas W, Kris-Etherton P (2001) Total fat intake modifies plasma fatty acid composition in humans. J Nutr. https://doi.org/10.1093/jn/131.2.231

    Article  PubMed  Google Scholar 

  76. Fishman MA, Prensky AL, Dodge PR (1969) Low content of cerebral lipids in infants suffering from malnutrition. Nature. https://doi.org/10.1038/221552a0

    Article  PubMed  Google Scholar 

  77. Thaiss CA, Itav S, Rothschild D et al (2016) Persistent microbiome alterations modulate the rate of post-dieting weight regain. Nature. https://doi.org/10.1038/nature20796

    Article  PubMed  Google Scholar 

  78. Wei X, Song H, Yin L et al (2016) Fatty acid synthesis configures the plasma membrane for inflammation in diabetes. Nature. https://doi.org/10.1038/nature20117

    Article  PubMed  PubMed Central  Google Scholar 

  79. Thaiss CA, Shapiro H, Elinav E (2017) Post-dieting weight gain: the role of persistent microbiome changes. Future Microbiol. https://doi.org/10.2217/fmb-2017-0045

    Article  PubMed  Google Scholar 

  80. Jaszczur MM, Vo DD, Stanciauskas R et al (2019) Conformational regulation of Escherichia coli DNA polymerase V by RecA and ATP. PLoS Genet. https://doi.org/10.1371/journal.pgen.1007956

    Article  PubMed  PubMed Central  Google Scholar 

  81. Dobrynin D, Fridman G, Friedman G, Fridman A (2009) Physical and biological mechanisms of direct plasma interaction with living tissue. New J Phys. https://doi.org/10.1088/1367-2630/11/11/115020

    Article  Google Scholar 

  82. Barlan AU, Danthi P, Wiethoff CM (2011) Lysosomal localization and mechanism of membrane penetration influence nonenveloped virus activation of the NLRP3 inflammasome. Virology. https://doi.org/10.1016/j.virol.2011.01.019

    Article  PubMed  PubMed Central  Google Scholar 

  83. Robinson A, McDonald JP, Caldas VEA et al (2015) Regulation of mutagenic DNA polymerase V activation in space and time. PLoS Genet. https://doi.org/10.1371/journal.pgen.1005482

    Article  PubMed  PubMed Central  Google Scholar 

  84. Perez Vidakovics MLA, Jendholm J, Mörgelin M et al (2010) B cell activation by outer membrane vesicles—a novel virulence mechanism. PLoS Pathog. https://doi.org/10.1371/journal.ppat.1000724

    Article  PubMed Central  Google Scholar 

  85. Adams DW, Wu LJ, Errington J (2015) Nucleoid occlusion protein Noc recruits DNA to the bacterial cell membrane. EMBO J 39(4):491–501

    Article  Google Scholar 

  86. Bjorge JD, Jakymiw A, Fujita DJ (2000) Selected glimpses into the activation and function of Src kinase. Oncogene 19:5620–5635. https://doi.org/10.1038/sj.onc.1203923

    Article  CAS  PubMed  Google Scholar 

  87. Vitrac H, MacLean DM, Karlstaedt A et al (2017) Dynamic lipid-dependent modulation of protein topology by post-translational phosphorylation. J Biol Chem 292:1613–1624. https://doi.org/10.1074/jbc.M116.765719

    Article  CAS  PubMed  Google Scholar 

  88. Vitrac H, Mallampalli VKPS, Dowhan W (2019) Importance of phosphorylation/dephosphorylation cycles on lipid-dependent modulation of membrane protein topology by posttranslational phosphorylation. J Biol Chem 294:18853–18862. https://doi.org/10.1074/jbc.RA119.010785

    Article  CAS  PubMed  Google Scholar 

  89. Harris DA, True HL (2006) New insights into prion structure and toxicity. Neuron 50:353–357. https://doi.org/10.1016/j.neuron.2006.04.020

    Article  CAS  PubMed  Google Scholar 

  90. Chesebro B, Coomaraswamy J, Bolmont T et al (2005) Anchorless prion protein results in infectious amyloid disease without clinical scrapie. Science. https://doi.org/10.1126/science.1110837

    Article  PubMed  Google Scholar 

  91. Wulf MA, Senatore A, Aguzzi A (2017) The biological function of the cellular prion protein: an update. BMC Biol 15:34. https://doi.org/10.1186/s12915-017-0375-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Godsave SF, Peters PJ, Wille H (2015) Subcellular distribution of the prion protein in sickness and in health. Virus Res. https://doi.org/10.1016/j.virusres.2015.02.004

    Article  PubMed  Google Scholar 

  93. Westergard L, Christensen HM, Harris DA (2007) The cellular prion protein (PrPC): its physiological function and role in disease. Biochim Biophys Acta 1772:629–644. https://doi.org/10.1016/j.bbadis.2007.02.011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Biasini E, Turnbaugh JA, Unterberger U, Harris DA (2012) Prion protein at the crossroads of physiology and dssisease. Trends Neurosci 35:92–103. https://doi.org/10.1016/j.tins.2011.10.002

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

OCN thanks Professor Jean'ne M. Shreeve for proofreading this manuscript and offering invaluable advice and insight.

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  1. Department of Chemistry, University of Idaho, Moscow, ID, 83843, USA

    Okechukwu Charles Nwamba

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Nwamba, O.C. Membranes as the third genetic code. Mol Biol Rep 47, 4093–4097 (2020). https://doi.org/10.1007/s11033-020-05437-z

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