1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Materials Research
  4. Volume 52, 2022
  5. Article

Annual Review of Materials Research

Volume 52, 2022

Crystalline Cholesterol: The Material and Its Assembly Lines

Abstract

Cholesterol is an essential component of animal cell membranes because it influences and controls cell membrane fluidity. Cholesterol is also responsible for the most frequent lethal pathologies in developed countries because of its intimate association with atherosclerotic plaques, the rupture of which may cause heart attacks or strokes. The question is under which conditions cholesterol activity manifests itself, whether in physiology or in pathology. The answer is complex, and there is probably not one certain answer. This review article has its foundations in abundant published knowledge and evidence, but it cannot possibly be comprehensive, because the extent of cholesterol's involvement in chemistry, biology, biophysics, and medicine is so vast that we cannot embrace it all. We review cholesterol as a molecule and in its various crystalline polymorphs. We then examine cholesterol assembly pathways and, finally, cholesterol in biology and in pathology. We propose that cholesterol activity depends on its assembly states in cholesterol crystals or with other lipids in the form of more-or-less organized crystalline domains. In other words, we analyze cholesterol material properties because the assembly state of the cholesterol molecules profoundly affects the properties of the environment in which they reside.

Keyword(s): atherosclerosis, cell membrane domains, cholesterol, crystal polymorphs, gallstones, helical crystals
Loading

Article metrics loading...

/content/journals/10.1146/annurev-matsci-081720-112639
2022-07-01
2024-04-27
Loading full text...

Full text loading...

/deliver/fulltext/matsci/52/1/annurev-matsci-081720-112639.html?itemId=/content/journals/10.1146/annurev-matsci-081720-112639&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Chevreul ME. 1823. De la cholestérine. Recherches chimiques sur les corps gras d'origine animale153–60 Paris: F. G. Levrault
     [Google Scholar]
  2. 2.
    Dam H. 1958. Historical introduction to cholesterol. Chemistry, Biochemistry, and Pathology RP Cook 1–14 New York: Academic
     [Google Scholar]
  3. 3.
    Olson RE. 1998. Discovery of the lipoproteins, their role in fat transport and their significance as risk factors. J. Nutr. 128:439S–43S
     [Google Scholar]
  4. 4.
    Kuijpers PMJC. 2021. History in medicine: the story of cholesterol, lipids and cardiology. J. Cardiol. Pract. 19:9
     [Google Scholar]
  5. 5.
    Boudet M. 1833. Nouvelle recherches sur la composition du serum du sang Oncley. Ann. Chim. Phys. 52:337–48
     [Google Scholar]
  6. 6.
    Bloch K 1991. Cholesterol: evolution of structure and function. New Comprehensive Biochemistry, Vol. 20 DE Vance, JE Vance 363–81 Amsterdam: Elsevier
     [Google Scholar]
  7. 7.
    Berg JM, Tymoczko JL, Stryer L. 2002. Biochemistry: International Version New York: W.H. Freeman
  8. 8.
    Carlisle C, Crowfoot D. 1945. The crystal structure of cholesteryl iodide. Proc. R. Soc. A 184:64–83
     [Google Scholar]
  9. 9.
    Saad HY, Higuchi WI. 1965. Water solubility of cholesterol. J. Pharm. Sci. 54:1205–6
     [Google Scholar]
  10. 10.
    Alberts B, Johnson A, Lewis J, Raff M, Roberts K, Walter P. 2014. Molecular Biology of the Cell New York: W.W. Norton
  11. 11.
    Sackmann E 1995. Biological membranes architecture and function. Handbook of Biological Physics R Lipowsky, E Sackmann 1–63 Amsterdam: Elsevier
     [Google Scholar]
  12. 12.
    Summons RE, Albrecht P, McDonald G, Moldowan JM. 2008. Molecular biosignatures. Space Sci. Rev. 135:133–59
     [Google Scholar]
  13. 13.
    Bux K, Moin ST. 2020. Solvation of cholesterol in different solvents: a molecular dynamics simulation study. Phys. Chem. Chem. Phys. 22:1154–67
     [Google Scholar]
  14. 14.
    Haberland ME, Reynolds JA. 1973. Self-association of cholesterol in aqueous solution. PNAS 70:2313–16
     [Google Scholar]
  15. 15.
    Lalitha S, Kumar AS, Stine KJ, Covey DF. 2001. Chirality in membranes: first evidence that enantioselective interactions between cholesterol and cell membrane lipids can be a determinant of membrane physical properties. J. Supramol. Chem. 1:53–61
     [Google Scholar]
  16. 16.
    Feingold KR 2021. Introduction to lipids and lipoproteins. Endotext KR Feingold, B Anawalt, A Boyce, G Chrousos, WW de Herder et al. South Dartmouth, MA: MDText.com
     [Google Scholar]
  17. 17.
    Small DM, Shipley GG. 1974. Physical-chemical basis of lipid deposition in atherosclerosis. Science 185:222–29
     [Google Scholar]
  18. 18.
    Craven BM. 1976. Crystal structure of cholesterol monohydrate. Nature 260:727–29
     [Google Scholar]
  19. 19.
    Shieh H, Hoard L, Nordman C. 1977. Crystal structure of anhydrous cholesterol. Nature 267:287–89
     [Google Scholar]
  20. 20.
    Solomonov I, Weygand MJ, Kjaer K, Rapaport H, Leiserowitz L. 2005. Trapping crystal nucleation of cholesterol monohydrate: relevance to pathological crystallization. Biophys. J. 88:1809–17
     [Google Scholar]
  21. 21.
    Weihs D, Schmidt J, Goldiner I, Danino D, Rubin M et al. 2005. Biliary cholesterol crystallization characterized by single-crystal cryogenic electron diffraction. J. Lipid Res. 46:942–48
     [Google Scholar]
  22. 22.
    Al-Handawi MB, Commins P, Karothu DP, Raj G, Li L, Naumov P. 2018. Mechanical and crystallographic analysis of cholesterol crystals puncturing biological membranes. Chem. Eur. J. 24:11493–97
     [Google Scholar]
  23. 23.
    Shepelenko M, Hirsch A, Varsano N, Beghi F, Addadi Let al 2022. Polymorphism, structure, and nucleation of cholesterol·H2O at aqueous interfaces and in pathological media: revisited from a computational perspective. J. Am. Chem. Soc 1445304–14
  24. 24.
    Loomis CR, Shipley GG, Small DM. 1979. The phase behavior of hydrated cholesterol. J. Lipid Res. 20:525–35
     [Google Scholar]
  25. 25.
    Suhalim JL, Chung C-Y, Lilledahl MB, Lim RS, Levi M et al. 2012. Characterization of cholesterol crystals in atherosclerotic plaques using stimulated Raman scattering and second-harmonic generation microscopy. Biophys. J. 102:1988–95
     [Google Scholar]
  26. 26.
    Frincu MC, Fleming SD, Rohl AL, Swift JA. 2004. The epitaxial growth of cholesterol crystals from bile solutions on calcite substrates. J. Am. Chem. Soc. 126:7915–24
     [Google Scholar]
  27. 27.
    Abendan RS, Swift JA. 2002. Surface characterization of cholesterol monohydrate single crystals by chemical force microscopy. Langmuir 18:4847–53
     [Google Scholar]
  28. 28.
    Konikoff F, Chung D, Donovan J, Small D, Carey M. 1992. Filamentous, helical, and tubular microstructures during cholesterol crystallization from bile. Evidence that cholesterol does not nucleate classic monohydrate plates. J. Clin. Investig. 90:1155–60
     [Google Scholar]
  29. 29.
    Konikoff FM, Carey MC. 1994. Cholesterol crystallization from a dilute bile salt-rich model bile. J. Cryst. Growth 144:79–86
     [Google Scholar]
  30. 30.
    Zastavker YV, Asherie N, Lomakin A, Pande J, Donovan JM et al. 1999. Self-assembly of helical ribbons. PNAS 96:7883–87
     [Google Scholar]
  31. 31.
    Chung DS, Benedek GB, Konikoff FM, Donovan JM. 1993. Elastic free energy of anisotropic helical ribbons as metastable intermediates in the crystallization of cholesterol. PNAS 90:11341–45
     [Google Scholar]
  32. 32.
    Khaykovich B, Hossain C, McManus JJ, Lomakin A, Moncton DE, Benedek GB. 2007. Structure of cholesterol helical ribbons and self-assembling biological springs. PNAS 104:9656–60
     [Google Scholar]
  33. 33.
    Varsano N, Beghi F, Elad N, Pereiro E, Dadosh T et al. 2018. Two polymorphic cholesterol monohydrate crystal structures form in macrophage culture models of atherosclerosis. PNAS 115:7662–69
     [Google Scholar]
  34. 34.
    Varsano N, Beghi F, Dadosh T, Elad N, Pereiro E et al. 2019. The effect of the phospholipid bilayer environment on cholesterol crystal polymorphism. ChemPlusChem 84:338–44
     [Google Scholar]
  35. 35.
    Landi K, Sinard J, Crawford JM, Topazian M. 2003. Cholesterol crystal morphology in acalculous gallbladder disease. J. Clin. Gastroenterol. 36:364–66
     [Google Scholar]
  36. 36.
    Eshelby J. 1953. Screw dislocations in thin rods. Int. J. Appl. Phys. 24:176–79
     [Google Scholar]
  37. 37.
    Morin SA, Bierman MJ, Tong J, Jin S 2010. Mechanism and kinetics of spontaneous nanotube growth driven by screw dislocations. Science 328:476–80
     [Google Scholar]
  38. 38.
    Olson IA, Shtukenberg AG, Hakobyan G, Rohl AL, Raiteri P et al. 2016. Structure, energetics, and dynamics of screw dislocations in even n-alkane crystals. J. Phys. Chem. Lett. 7:3112–17
     [Google Scholar]
  39. 39.
    Shtukenberg AG, Punin YO, Gujral A, Kahr B. 2014. Growth actuated bending and twisting of single crystals. Angew. Chem. Int. Ed. 53:672–99
     [Google Scholar]
  40. 40.
    Selinger J, MacKintosh F, Schnur J. 1996. Theory of cylindrical tubules and helical ribbons of chiral lipid membranes. Phys. Rev. E 53:3804–18
     [Google Scholar]
  41. 41.
    Khaykovich B, Kozlova N, Choi W, Lomakin A, Hossain C et al. 2009. Thickness–radius relationship and spring constants of cholesterol helical ribbons. PNAS 106:15663–66
     [Google Scholar]
  42. 42.
    Schnur JM. 1993. Lipid tubules: a paradigm for molecularly engineered structures. Science 262:1669–76
     [Google Scholar]
  43. 43.
    Katz S, Shipley GG, Small D. 1976. Physical chemistry of the lipids of human atherosclerotic lesions. Demonstration of a lesion intermediate between fatty streaks and advanced plaques. J. Clin. Investig. 58:200–11
     [Google Scholar]
  44. 44.
    Abela GS, Aziz K, Vedre A, Pathak DR, Talbott JD, DeJong J. 2009. Effect of cholesterol crystals on plaques and intima in arteries of patients with acute coronary and cerebrovascular syndromes. Am. J. Cardiol 103:959–68
     [Google Scholar]
  45. 45.
    Kalavakunta JK, Mittal MK, Janoudi A, Abela OG, Alreefi F, Abela GS. 2017. Role of cholesterol crystals during acute myocardial infarction and cerebrovascular accident. Cardiovasc. Innov. Appl. 2:347–62
     [Google Scholar]
  46. 46.
    Abela GS, Aziz K 2006. Cholesterol crystals rupture biological membranes and human plaques during acute cardiovascular events-a novel insight into plaque rupture by scanning electron microscopy. Scanning 28:1–10
     [Google Scholar]
  47. 47.
    Nidorf M, Fiolet A, Abela GS. 2020. Viewing atherosclerosis through a crystal lens: how the evolving structure of cholesterol crystals in atherosclerotic plaque alters its stability. J. Clin. Lipidol. 14:619–30
     [Google Scholar]
  48. 48.
    Smith R, Tanford C. 1973. Hydrophobicity of long chain n-alkyl carboxylic acids, as measured by their distribution between heptane and aqueous solutions. PNAS 70:289–93
     [Google Scholar]
  49. 49.
    Harris SMJ, Higuchi T, Rytting JH. 1973. Thermodynamic group contributions from ion pair extraction equilibriums for use in the prediction of partition coefficients. Correlation of surface area with group contributions. J. Phys. Chem. A 77:2694–703
     [Google Scholar]
  50. 50.
    Gilbert DB, Tanford C, Reynolds JA. 1975. Cholesterol in aqueous solution. Hydrophobicity and self-association. Biochemistry 14:444–48
     [Google Scholar]
  51. 51.
    Yeagle PL. 1985. Cholesterol and the cell membrane. Biochim. Biophys. Acta Rev. Biomemb. 822:267–87
     [Google Scholar]
  52. 52.
    Ziblat R, Kjaer K, Leiserowitz L, Addadi L. 2009. Structure of cholesterol/lipid ordered domains in monolayers and single hydrated bilayers. Angew. Chem. Int. Ed. 48:8958–61
     [Google Scholar]
  53. 53.
    Ziblat R, Leiserowitz L, Addadi L. 2010. Crystalline domain structure and cholesterol crystal nucleation in single hydrated DPPC:cholesterol:POPC bilayers. J. Am. Chem. Soc. 132:9920–27
     [Google Scholar]
  54. 54.
    Ziblat R, Fargion I, Leiserowitz L, Addadi L. 2012. Spontaneous formation of two-dimensional and three-dimensional cholesterol crystals in single hydrated lipid bilayers. Biophys. J. 103:255–64
     [Google Scholar]
  55. 55.
    Ziblat R, Leiserowitz L, Addadi L. 2011. Crystalline lipid domains: characterization by X-ray diffraction and their relation to biology. Angew. Chem. Int. Ed. 50:3620–29
     [Google Scholar]
  56. 56.
    Rapaport H, Kuzmenko I, Lafont S, Kjaer K, Howes PB et al. 2001. Cholesterol monohydrate nucleation in ultrathin films on water. Biophys. J. 81:2729–36
     [Google Scholar]
  57. 57.
    Varsano N, Fargion I, Wolf SG, Leiserowitz L, Addadi L. 2015. Formation of 3D cholesterol crystals from 2D nucleation sites in lipid bilayer membranes: implications for atherosclerosis. J. Am. Chem. Soc. 137:1601–7
     [Google Scholar]
  58. 58.
    Róg T, Pasenkiewicz-Gierula M, Vattulainen I, Karttunen M. 2009. Ordering effects of cholesterol and its analogues. Biochim. Biophys. Acta Biomembr. 1788:97–121
     [Google Scholar]
  59. 59.
    Finegold L. 1992. Cholesterol in Membrane Models Boca Raton, FL: CRC Press
  60. 60.
    Ohvo-Rekilä H, Ramstedt B, Leppimäki P, Slotte JP. 2002. Cholesterol interactions with phospholipids in membranes. Prog. Lipid Res. 41:66–97
     [Google Scholar]
  61. 61.
    Marquardt D, Heberle FA, Greathouse DV, Koeppe RE, Standaert RF et al. 2016. Lipid bilayer thickness determines cholesterol's location in model membranes. Soft Matter 12:9417–28
     [Google Scholar]
  62. 62.
    Wei C, Pohorille A. 2014. Flip-flop of oleic acid in a phospholipid membrane: rate and mechanism. J. Phys. Chem. B 118:12919–26
     [Google Scholar]
  63. 63.
    Robalo JR, Ramalho JP, Loura LM. 2013. NBD-labeled cholesterol analogues in phospholipid bilayers: insights from molecular dynamics. J. Phys. Chem. B 117:13731–42
     [Google Scholar]
  64. 64.
    Ermilova I, Lyubartsev AP. 2019. Cholesterol in phospholipid bilayers: positions and orientations inside membranes with different unsaturation degrees. Soft Matter 15:78–93
     [Google Scholar]
  65. 65.
    Bennett WD, MacCallum JL, Hinner MJ, Marrink SJ, Tieleman DP. 2009. Molecular view of cholesterol flip-flop and chemical potential in different membrane environments. J. Am. Chem. Soc. 131:12714–20
     [Google Scholar]
  66. 66.
    Hancock JF. 2006. Lipid rafts: contentious only from simplistic standpoints. Nat. Rev. Mol. Cell Biol. 7:456–62
     [Google Scholar]
  67. 67.
    Lingwood D, Simons K. 2010. Lipid rafts as a membrane-organizing principle. Science 327:46–50
     [Google Scholar]
  68. 68.
    Schroeder F, Jefferson JR, Kier AB, Knittel J, Scallen TJ et al. 1991. Membrane cholesterol dynamics: cholesterol domains and kinetic pools. Proc. Soc. Exp. Biol. Med. 196:235–52
     [Google Scholar]
  69. 69.
    Frazier ML, Wright JR, Pokorny A, Almeida PF. 2007. Investigation of domain formation in sphingomyelin/cholesterol/POPC mixtures by fluorescence resonance energy transfer and Monte Carlo simulations. Biophys. J. 92:2422–33
     [Google Scholar]
  70. 70.
    Zachowski A. 1993. Phospholipids in animal eukaryotic membranes: transverse asymmetry and movement. Biochem. J. 294:1–14
     [Google Scholar]
  71. 71.
    Bandara A, Panahi A, Pantelopulos GA, Straub JE. 2017. Exploring the structure and stability of cholesterol dimer formation in multicomponent lipid bilayers. J. Comput. Chem. 38:1479–88
     [Google Scholar]
  72. 72.
    Mukherjee S, Chattopadhyay A. 1996. Membrane organization at low cholesterol concentrations: a study using 7-nitrobenz-2-oxa-1,3-diazol-4-yl-labeled cholesterol. Biochemistry 35:1311–22
     [Google Scholar]
  73. 73.
    Harris JS, Epps DE, Davio SR, Kezdy FJ. 1995. Evidence for transbilayer, tail-to-tail cholesterol dimers in dipalmitoylglycerophosphocholine liposomes. Biochemistry 34:3851–57
     [Google Scholar]
  74. 74.
    Brewster R, Safran SA. 2010. Line active hybrid lipids determine domain size in phase separation of saturated and unsaturated lipids. Biophys. J. 98:L21–23
     [Google Scholar]
  75. 75.
    Dietrich C, Bagatolli L, Volovyk Z, Thompson N, Levi M et al. 2001. Lipid rafts reconstituted in model membranes. Biophys. J. 80:1417–28
     [Google Scholar]
  76. 76.
    Veatch SL, Keller SL. 2002. Organization in lipid membranes containing cholesterol. Phys. Rev. Lett. 89:268101
     [Google Scholar]
  77. 77.
    Kahya N, Scherfeld D, Bacia K, Poolman B, Schwille P. 2003. Probing lipid mobility of raft-exhibiting model membranes by fluorescence correlation spectroscopy. Int. J. Biol. Chem. 278:28109–15
     [Google Scholar]
  78. 78.
    Crane JM, Tamm LK. 2004. Role of cholesterol in the formation and nature of lipid rafts in planar and spherical model membranes. Biophys. J. 86:2965–79
     [Google Scholar]
  79. 79.
    Rinia HA, Snel MM, van der Eerden JP, de Kruijff B. 2001. Visualizing detergent resistant domains in model membranes with atomic force microscopy. FEBS Lett 501:92–96
     [Google Scholar]
  80. 80.
    Zhao J, Wu J, Shao H, Kong F, Jain N et al. 2007. Phase studies of model biomembranes: macroscopic coexistence of Lα + Lβ, with light-induced coexistence of Lα + Lo phases. Biochim. Biophys. Acta Biomembr. 1768:2777–86
     [Google Scholar]
  81. 81.
    Ayuyan AG, Cohen FS. 2006. Lipid peroxides promote large rafts: effects of excitation of probes in fluorescence microscopy and electrochemical reactions during vesicle formation. Biophys. J. 91:2172–83
     [Google Scholar]
  82. 82.
    Feigenson GW. 2009. Phase diagrams and lipid domains in multicomponent lipid bilayer mixtures. Biochim. Biophys. Acta Biomembr. 1788:47–52
     [Google Scholar]
  83. 83.
    van Meer G, Voelker DR, Feigenson GW. 2008. Membrane lipids: where they are and how they behave. Nat. Rev. Mol. Cell Biol. 9:112–24
     [Google Scholar]
  84. 84.
    Bretscher MS, Munro S. 1993. Cholesterol and the Golgi apparatus. Science 261:1280–82
     [Google Scholar]
  85. 85.
    Chakraborty S, Doktorova M, Molugu TR, Heberle FA, Scott HL et al. 2020. How cholesterol stiffens unsaturated lipid membranes. PNAS 117:21896–905
     [Google Scholar]
  86. 86.
    Small D. 1988. George Lyman Duff memorial lecture. Progression and regression of atherosclerotic lesions. Insights from lipid physical biochemistry. Arterioscler. Thromb. Vasc. Biol. 8:103–29
     [Google Scholar]
  87. 87.
    Brown MS, Goldstein JL. 2009. Cholesterol feedback: from Schoenheimer's bottle to Scap's MELADL. J. Lipid Res. 50:S15–27
     [Google Scholar]
  88. 88.
    Shepherd J. 2001. The role of the exogenous pathway in hypercholesterolaemia. Eur. Heart J. Suppl. 3:E2–5
     [Google Scholar]
  89. 89.
    Sankaram MB, Thompson TE. 1990. Interaction of cholesterol with various glycerophospholipids and sphingomyelin. Biochemistry 29:10670–75
     [Google Scholar]
  90. 90.
    Nakanishi S, Vikstedt R, Söderlund S, Lee-Rueckert M, Hiukka A et al. 2009. Serum, but not monocyte macrophage foam cells derived from low HDL-C subjects, displays reduced cholesterol efflux capacity. J. Lipid Res. 50:183–92
     [Google Scholar]
  91. 91.
    Wolska A, Dunbar RL, Freeman LA, Ueda M, Amar MJ et al. 2017. Apolipoprotein C-II: new findings related to genetics, biochemistry, and role in triglyceride metabolism. Atherosclerosis 267:49–60
     [Google Scholar]
  92. 92.
    Jonas A, Phillips MC 2008. Lipoprotein structure. Biochemistry of Lipids, Lipoproteins and Membranes DE Vance, JE Vance 485–506 Amsterdam: Elsevier
     [Google Scholar]
  93. 93.
    Hevonoja T, Pentikäinen MO, Hyvönen MT, Kovanen PT, Ala-Korpela M. 2000. Structure of low density lipoprotein (LDL) particles: basis for understanding molecular changes in modified LDL. Biochim. Biophys. Acta Mol. Cell Biol. Lipids 1488:189–210
     [Google Scholar]
  94. 94.
    Ramms B, Gordts PL. 2018. Apolipoprotein C-III in triglyceride-rich lipoprotein metabolism. Curr. Opin. Lipidol. 29:171–79
     [Google Scholar]
  95. 95.
    Orlova EV, Sherman MB, Chiu W, Mowri H, Smith LC, Gotto AM. 1999. Three-dimensional structure of low density lipoproteins by electron cryomicroscopy. PNAS 96:8420–25
     [Google Scholar]
  96. 96.
    Walther TC, Farese RV Jr. 2009. The life of lipid droplets. Biochim. Biophys. Acta Mol. Cell Biol. Lipids 1791:459–66
     [Google Scholar]
  97. 97.
    Mahamid J, Tegunov D, Maiser A, Arnold J, Leonhardt H et al. 2019. Liquid-crystalline phase transitions in lipid droplets are related to cellular states and specific organelle association. PNAS 116:16866–71
     [Google Scholar]
  98. 98.
    Linton MF, Yancey PG, Davies SS, Jerome WG, Linton EF et al. 2019. The role of lipids and lipoproteins in atherosclerosis. Endotext KR Feingold, B Anawalt, A Boyce, G Chrousos, WW de Herder et al. South Dartmouth, MA: MDText.com
     [Google Scholar]
  99. 99.
    Moore KJ, Sheedy FJ, Fisher EA. 2013. Macrophages in atherosclerosis: a dynamic balance. Nat. Rev. Immunol. 13:709–21
     [Google Scholar]
  100. 100.
    Tangirala RK, Jerome WG, Jones N, Small DM, Johnson W et al. 1994. Formation of cholesterol monohydrate crystals in macrophage-derived foam cells. J. Lipid Res. 35:93–104
     [Google Scholar]
  101. 101.
    Kellner-Weibel G, Yancey P, Jerome W, Walser T, Mason R et al. 1999. Crystallization of free cholesterol in model macrophage foam cells. Arterioscler. Thromb. Vasc. Biol. 19:1891–98
     [Google Scholar]
  102. 102.
    Varsano N, Dadosh T, Kapishnikov S, Pereiro E, Shimoni E et al. 2016. Development of correlative cryo-soft X-ray tomography and stochastic reconstruction microscopy. A study of cholesterol crystal early formation in cells. J. Am. Chem. Soc. 138:14931–40
     [Google Scholar]
  103. 103.
    Kruth HS. 1997. Cholesterol deposition in atherosclerotic lesions. Cholesterol R Bittman 319–62 Boston: Springer
     [Google Scholar]
  104. 104.
    Lonsdale K. 1968. Epitaxy as a growth factor in urinary calculi and gallstones. Nature 217:56–58
     [Google Scholar]
  105. 105.
    Frincu MC, Sharpe RE, Swift JA. 2004. Epitaxial relationships between cholesterol crystals and mineral phases: implication for human disease. Cryst. Growth Des. 4:223–26
     [Google Scholar]
  106. 106.
    Abela GS. 2010. Cholesterol crystals piercing the arterial plaque and intima trigger local and systemic inflammation. J. Clin. Lipidol. 4:156–64
     [Google Scholar]
  107. 107.
    Køllgaard T, Enevold C, Bendtzen K, Hansen PR, Givskov M et al. 2017. Cholesterol crystals enhance TLR2- and TLR4-mediated pro-inflammatory cytokine responses of monocytes to the proatherogenic oral bacterium Porphyromonas gingivalis. PLOS ONE 12:e0172773
     [Google Scholar]
  108. 108.
    Grebe A, Latz E. 2013. Cholesterol crystals and inflammation. Curr. Rheumatol. Rep. 15:313
     [Google Scholar]
  109. 109.
    Gensini G, Dilaghi B. 2002. The unstable plaque. Eur. Heart J. 4:B22–27
     [Google Scholar]
  110. 110.
    Schroeder AP, Falk E. 1995. Vulnerable and dangerous coronary plaques. Atherosclerosis 118:S141–49
     [Google Scholar]
  111. 111.
    Virmani R, Kolodgie FD, Burke AP, Finn AV, Gold HK et al. 2005. Atherosclerotic plaque progression and vulnerability to rupture: angiogenesis as a source of intraplaque hemorrhage. Arterioscler. Thromb. Vasc. Biol. 25:2054–61
     [Google Scholar]
  112. 112.
    Kaloustian J, De La Porte PL, El-Moselhy T, Lafont H, Portugal H. 2005. Thermal analysis and microscopical characterization of cholesterol in gallstones. J. Therm. Anal. Calorim. 82:331–38
     [Google Scholar]
  113. 113.
    Sömjen GJ, Marikovsky Y, Lelkes P, Gilat T. 1986. Cholesterol-phospholipid vesicles in human bile: an ultrastructural study. Biochim. Biophys. Acta Lipids Lipid Metab. 879:14–21
     [Google Scholar]
  114. 114.
    Weihs D, Schmidt J, Danino D, Goldiner I, Leikin-Gobbi D et al. 2007. A comparative study of microstructural development in paired human hepatic and gallbladder biles. Biochim. Biophys. Acta Mol. Cell Biol. Lipids 1771:1289–98
     [Google Scholar]
  115. 115.
    Konikoff FM, Cohen DE, Carey MC. 1994. Phospholipid molecular species influence crystal habits and transition sequences of metastable intermediates during cholesterol crystallization from bile salt-rich model bile. J. Lipid Res. 35:60–70
     [Google Scholar]
  116. 116.
    Mouritsen OG, Zuckermann MJ. 2004. What's so special about cholesterol?. Lipids 39:1101–13
     [Google Scholar]
  117. 117.
    Kowalski PS, Rudra A, Miao L, Anderson DG. 2019. Delivering the messenger: advances in technologies for therapeutic mRNA delivery. Mol. Ther. 27:710–28
     [Google Scholar]
  118. 118.
    Wadhwa A, Aljabbari A, Lokras A, Foged C, Thakur A. 2020. Opportunities and challenges in the delivery of mRNA-based vaccines. Pharmaceutics 12:102
     [Google Scholar]
  119. 119.
    Stojančević M, Pavlović N, Goločorbin-Kon S, Mikov M. 2013. Application of bile acids in drug formulation and delivery. Front. Life Sci. 7:112–22
     [Google Scholar]
/content/journals/10.1146/annurev-matsci-081720-112639
Loading
Crystalline Cholesterol: The Material and Its Assembly Lines
Annual Review of Materials Research 52, 57 (2022); https://doi.org/10.1146/annurev-matsci-081720-112639
/content/journals/10.1146/annurev-matsci-081720-112639
/content/journals/10.1146/annurev-matsci-081720-112639
Loading

Data & Media loading...

  • Article Type: Review Article

Most Cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error