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Prof. Martin D. Caffrey

Professor of Membrane Structural Biology

Department of Chemical and Environmental Sciences

Tel (direct): +353-61-234174 Fax: +353-61-202568;

Membrane Structural Biology

Bioinformatics, Biomaterials, Controlled Release, High-Throughput Crystallography, Databases, Drug Delivery, Lipidomics, Membrane Protein Structure and Function, Rational Design, Robotics, X-Ray Methods

The elucidation of the structure and function of cellular membranes remains today one of the grand challenges in structural biology. While much attention has been paid to the protein component of membranes in the past, the lipid component is increasingly being recognized as an active player in the life of the membrane. The cross-disciplinary research being conducted in my group is concerned with both membrane components. The reductionist approach is adopted which involves establishing behaviors of components in isolation first and then building up a view of the intact biological membrane in a series of reconstitution studies where lipids and proteins acting in concert are studied. What makes lipids so interesting as biomaterials is that they exhibit liquid crystalline properties. Much of our work focuses on this important property. A variety of biochemical, biophysical, synthetic and analytical techniques are used in this research program and a sizable effort is devoted to making state-of-the-art measurements at x-ray synchrotron facilities worldwide. A summary of our research interests in the area of membrane structure and function follows.

Membrane Protein Structure A major breakthrough in determining the structure and function of membrane proteins occurred recently with the advent of a technique for growing crystals of membrane proteins from lipid cubic mesophases. We are using our understanding of lipid phase science to decipher the mechanism of crystal growth and are extending the method to several important membrane proteins. A major effort is underway to miniaturize and to robotize the crystallization process. This is part of a high-throughput structural proteomics initiative aimed at determining the structure and function of the proteins in Mycobacterium tuberculosis, the organism responsible for tuberculosis.

Membrane Fusion Much of intra- and inter-cellular communication is mediated by a process that requires membranes to fuse. Our objective here is to understand the mechanism whereby lipids and proteins function in this ubiquitous and vital process. To this end, a method referred to as time-resolved x-ray diffraction has been developed that enables the direct and quantitative measurement of the dynamics of phase transitions believed to occur during membrane fusion. Mechanistic insights are provided by the ability to detect transition intermediates and by impulse-response studies. These investigations seek to augment our appreciation of the physiological role of membrane lipids and proteins in fusion and related cellular events.

Rational Design Principles / Environmental Chemistry The monoacylglycerols are important intermediates in fat metabolism. They display a remarkable variety of liquid crystal phases when dispersed in water. We wish to establish the rules governing liquid crystal phase propensity and mesoscopic topology as determined by molecular structure and are working with a series of synthetic monoacylglycerols for this purpose. The principles that emerge from this work will help decipher the membrane lipid dispersity enigma and will be used in rational design of biocompatible materials for encapsulation, controlled release, and uptake and drug delivery. This area of research involves organic synthesis, mesophase structure/materials characterization using x-ray diffraction, calorimetry and curvature elastic energy calculations, and transport studies with drugs, proteins, nucleic acids on the one hand, and environmentally sensitive chemicals (pollutants) on the other.

Cholesterol, Polyunsaturated Fatty Acids Cholesterol and polyunsaturated fatty acids-containing lipids have profound effects on the phase properties and thus, the function, of natural membranes. Domain, also known as raft, formation within the membrane is triggered by high cholesterol in a way that is sensitive to the polyunsaturated fatty acid-containing lipid profile of the membrane. Phase relations and lipid dynamics of these model membrane systems are being investigated using x-ray diffraction and nuclear magnetic resonance in collaboration with S. Wassall at IUPUI, Indianapolis, IN. The goal is to understand how domain formation and membrane function are regulated in vivo.

Radiation Damage The call for brighter synchrotron x-radiation sources for use in structural biology research is barely audible as we embark on the new millennium. Our brightest sources are already creating havoc when used at design specifications because of damage. The problem of radiation damage is particularly severe in studies involving kinetics and mechanism where cryotechniques are not always viable. Accordingly, we need to understand the very nature of radiation damage and to devise means for minimizing it. This is the thrust of the current project as applied to lipid membranes and mesophases, and to crystals of macromolecules. Thus far, we have reported on two very different types of radiation damage. One involves a dramatic phase transformation and the other a disordering of lamellar stacking. How beam energy, accumulated dose, dose-rate, scavengers, etc., affect damage is under investigation. The work highlights the nature of the damage process and the need for additional studies with a view to making most efficient use of an important resource, synchrotron radiation. We have demonstrated that damage is free radical mediated. This finding is of additional interest as it may have implications for age-related changes in membrane properties. Radiation damage as applied to crystals of macromolecules is being done in collaboration with Drs. R. Ravelli and S. McSweeney at the ESRF/EMBL (Grenoble, France) and with Dr. E. Garman (University of Oxford, England).

Bio- and Chemi-informatics Lipidomics is a fledgling discipline where lipids, also known as fats, take center stage. Of particular interest within the area are the distribution of lipids in biological systems in health and disease, and the relationship that exists between lipid structure and function. The Lipid Data Bank (LDB,www.caffreylabs.ul.ie) is a suite of web-based relational databases containing quantitative information critical to understanding the structure-function relationship and lipid distribution profiles. A long-term objective of lipidomics is the exploitation of this understanding for the purpose of rational design and control. The LDB is a collection of Web-based relational databases serving a diverse community with an interest in lipids and membranes. It includes i) LIPIDAT, a database of lipid phases, phase transition temperatures and enthalpy change values, ii) LIPIDAG, a database of phase diagrams dealing with lipid miscibility, and iii) LMSD, where lipid molecular structures are housed.

Biographical Sketch

Martin Caffrey received a B. Agr. Sc from University College, Dublin, in 1972. He then moved to Cornell University where he received an M.S. in food science in 1976 and a Ph.D. in biochemistry in 1982. He remained on as an independent investigator at Cornell University until 1988 when he joined the Department of Chemistry faculty at The Ohio State University. In the fall of 2003, he assumed the position of Professor of Membrane Structural Biology at The University of Limerick supported in part by an Investigatorship from Science Foundation Ireland. His objectives include establishing a Centre For Membrane Structural Biology at the University of Limerick. He continues to hold an adjunct professor position in the Chemistry Department at The Ohio State University.

Travel

Members of the research group including students will have an opportunity to work for several weeks to months at a time at The Ohio State University (Columbus, OH, USA), and at x-ray synchrotron facilities worldwide. Most of the group’s x-ray data collection is done currently at the Advanced Photon Source, Argonne National Laboratory (Chicago, USA), the Cornell High Energy Synchrotron Source (Ithaca, NY, USA), the National Synchrotron Light Source (Brookhaven, NY, USA), and the European Synchrotron Radiation Facility (Grenoble, France).

Student and Researcher Positions

Students interested in joining the group should apply immediately for an Embark Postgraduate Research Scholarship (www.ircset.ie) in consultation with Professor Caffrey. Suitable candidates who do not secure funding will be supported at the IRCSET level through Professor Caffrey’s SFI award. There are currently three studentships available in the group.

In addition, there are 3 senior research positions available in the group. These include a Senior Research Fellow, a University Research Scholar and a Postdoctoral Research Associate position. Click here for complete details.

Contact

Please contact Professor Caffrey directly by email (martin.caffrey@ul.ie) or by phone (UL office: 353-61-234174;

UL home: 353-61-202557)

Publications

Summary:

Books, 1

Electronic Media, 2

Peer Reviewed Journal Articles, 84

Reviews, 15

Papers in Proceedings

a. Books

Caffrey, M. 1993. LIPIDAT A database of thermodynamic data and associated information on lipid mesomorphic and polymorphic transitions. 305 pp., 1331 references, 10,704 records each with 28 fields. CRC Press, Inc., Boca Raton, FL.

b. Electronic Media

1. CAFFREY, M. 1993. Lipid thermotropic phase transitions LIPIDAT. NIST Standard Reference Database 34. Contains ca.11,000 records, each with 28 information fields, on over 900 lipids. Available on standard computer disks and can be used on Macintosh and PC compatible computers. Version 2.0, 15,000 records, released 12/94.

2. Lipid Data Bank. 1996 - present. A relational database of thermodynamic data on lipid mesophase and crystal polymorphic transitions on the Web. The database includes molecular structures and data can be submitted to the LIPIDAT database via the web. The Lipid Data Bank is available at www.caffreylabs.ul.ie

c. Peer Reviewed Journal Articles

1. Caffrey, M., Infante, J. and Kinsella, J. E. 1975. Isoenzymes of an acyltransferase from rabbit mammary gland: Evidence from biphasic substrate saturation kinetics. FEBS Lett. 52:116-120.

2. Caffrey, M. and Kinsella, J. E. 1975. Sensitivity of the molar absortivity value to sample and instrument characteristics, with reference to the Ellman Reagent (DTNB). Int. J. Biochem. 6:877-883.

3. Caffrey, M. and Kinsella, J. E. 1976. Isoenzymes of an acyltransferase from rabbit mammary gland: Solubilization of the micelle-specific species with Tritron X-100. Biochem. Biophys. Res. Commun. 71:484-491.

5. Caffrey, M. and Kinsella, J. E.. 1977. Growth and acyltransferase activity of rabbit mammary gland during pregnancy and lactation. J. Lipid Res. 18:44-52.

6. Caffrey, M. and Kinsella, J. E. 1977. Experimental difficulties in assaying a membrane-bound acyltransferase from rabbit mammary tissue. Int. J. Biochem. 8:39-51.

7. Caffrey, M. and Kinsella, J. E. 1977. Kinetics of a micelle specific palmitoyltransferase isoenzyme from rabbit mammary gland. Lipids 12:556-562.

8. Caffrey, M. and Kinsella, J. E. 1978. Properties of palmitoyl-CoA: monopalmitoyl-sn-glycerol-3-phosphate palmitoyltransferase from rabbit mammary gland. Int. J. Biochem. 9:239-248.

9. Caffrey, M. and Kinsella, J. E. 1978. Solubilization of a micelle specific acyltransferase from rat mammary microsomes. Int. J. Biochem. 9:381-384.

10. Caffrey, M. and Feigenson G. W. 1981. Fatty acyl chain characteristics of phosphatidylcholines affect Ca2+-ATPase enzymatic activity but not the affinity of the protein for these different lipid species. Biochem. Soc. Trans. 9:155-156.

11. Caffrey, M. and Feigenson, G. W. 1981. Fluorescence quenching in model membranes: The relationship between Ca2+-ATPase enzyme activity and the affinity of the protein for phosphatidylcholines with different acyl chain characteristics. Biochemistry 20:1949-1961.

12. Caffrey, M. and Bilderback, D. H. 1983. Real-time x-ray diffraction using synchrotron radiation: System characterization and applications. Nucl. Instr. Meth. 208:495-510.

13. Caffrey, M. and Feigenson, G. W. 1984. The influence of metal ions on the phase properties of phosphatidic acid in combination with natural and synthetic phosphatidylcholines: An x-ray diffraction study using synchrotron radiation. Biochemistry 23:323-331.

14. Caffrey, M. and Bilderback, D. H. 1984. Kinetics of the main phase transition of hydrated lecithin monitored by real-time x-ray diffraction. Biophys. J. 45:627-631.

15. Grubb, D. T., J.-H. Liu, Caffrey, M. and Bilderback, D. H. 1984. Real-time small-angle x-ray scattering during annealing of polymer single crystals. J. Polym. Sci. Polym. Phys. Ed. 22:367-378.

16. Caffrey, M. 1984. X-Radiation damage of hydrated lecithin membranes detected by real-time x-ray diffraction using wiggler-enchanced synchrotron radiation as the ionizing radiation source. Nucl. Instr. Meth. 222:329-338.

17. Caffrey, M. 1985. Kinetics and mechanism of the lamellar gel/lamellar liquid crystal and lamellar/inverted hexagonal phase transition in phosphatidylethanolamine: A real-time x-ray diffraction study using synchrotron radiation. Biochemistry 24:4826-4844.

18. Caffrey, M. and Lew, R. R. 1986. The Ca2+ induced phase transformation in soybean root microsomal membranes is a consequence of phospholipase activity. Plant Cell Physiol. 27:1091-1100.

19. Caffrey, M. and Hing, F. S. 1987. A temperature-gradient method for lipid phase diagram construction using time-resolved x-ray diffraction. Biophys. J. 51:37-46.

20. Dea, P., Pearson, L. T., Caffrey, M. and Chan, S.-I. 1987. Effect of chlorophyll a on the phase behavior of hydrated monogalactosyl diacylglyceride. Biochim. Biophys. Acta 896:11-18.

21. Caffrey, M. 1987. The combined and separate effects of temperature and freezing on membrane lipid mesomorphic phase behavior: Relevance to cryobiology. Biochim. Biophys. Acta 896:123-127.

22. Caffrey, M. 1987. Kinetics and mechanism of transitions involving the lamellar, cubic, inverted hexagonal and fluid isotropic phase of hydrated monoacylglycerides monitored by time-resolved x-ray diffraction. Biochemistry 26:6349-6363.

23. Caffrey, M., Morris, S. J. and Feigenson, G. W. 1987. Uranyl acetate induces gel phase formation in model lipid and biological membranes. Biophys. J. 52:501-505.

24. Caffrey, M., Werner, B. G. and Priestly, D. A. 1987. A crystalline lipid phase in a dry biological system: Evidence from x-ray diffraction analysis of Typha latifolia pollen. Biochim. Biophys. Acta 921:1214-1234.

25. Caffrey, M. and Bywater, M. 1988. Two new and rapid approaches for studying the phase properties of cosmetic lipids and oils. J. Soc. Cosmet. Chem. 39:159-167.

26. Caffrey, M., Fonseca, V. and Leopold, A. C. 1988. Lipid-sugar interaction: Relevance to anhydrous biology. Plant Physiol. 86:754-758.

27. Bedzyk, M., Bilderback, D. H., Bommarito, M., Caffrey, M., and Schildkraut, J. 1988. X-ray standing waves: A molecular yardstick for biological membranes. Science 241:1788-1791.

28. CAFFREY, M. 1989. A lyotrope gradient method for liquid crystal temperature-composition-mesomorph diagram construction using time-resolved x-ray diffraction. Biophys. J. 55:47-52.

29. GERRITSEN, H. and CAFFREY, M. 1990. Water transport in lyotropic liquid crystals and lipid-water systems: Mutual diffusion coefficient determination. J. Phys. Chem. 94:944-948.

30. BEDZYK, M., BOMMARITO, M., CAFFREY, M., and Penner, T. L. 1990. Diffuse-Double Layer at a Membrane/Aqueous Interface Measured with X-ray Standing Waves. Science 248:52-56.

31. CAFFREY, M., MAGIN, R. L., HUMMEL, B., and ZHANG, J. 1990. Kinetics of the lamellar and hexagonal phase transitions in phosphatidyl-ethanolamine: A time-resolved x-ray diffraction study using a microwave-induced temperature-jump. Biophys. J. 58:21-29.

32. Caffrey M., Fanger, G., MAGIN, R. L., and ZHANG, J. 1990. Kinetics of the premelting (Lb'-Pb') in hydrated DPPC: A time-resolved x-ray diffraction study using microwave-induced temperature-jumps. Biophys. J. 58:677-686.

33. CAFFREY, M., MOYNIHAN, D. and HOGAN, J. 1990. A database of lipid phase transition temperatures and enthalpy changes. Chem. Phys. Lipids 57:275-291.

34. MENCKE, A. P., and CAFFREY, M. 1991. Kinetics and Mechanism of the pressure-induced lamellar order/disorder transition in DHPE: A time-resolved x-ray diffraction study. Biochemistry, 30:2453-2463.

35. CAFFREY, M., Hogan, J. L., and RUDOLPH, A. S. 1991. Diacetylenic lipid microstructures: Characterization by x-ray diffraction and calorimetry. Biochemistry, 30:2134-2146.

36. CAFFREY, M, HOGAN J. L. and MENCKE, A. P. 1991. Kinetics of the barotropic ripple (Pb') - lamellar liquid crystal (La) phase transition in fullyhydrated DMPC monitored by time-resolved x-ray diffraction. Biophys. J., 60:456-466.

37. CAFFREY, M., MOYNIHAN, D. and HOGAN, J. 1991. A database of lipid phase transition temperatures and enthalpy changes. J. Chem. Inform. Comp. Sci., 31:275-284.

38. WANG, J., BEDZYK, M. J., PENNER, T. L. and CAFFREY, M. 1991. Structural studies of membranes and surface layers up to 1,000 Å thick using x-ray standing waves. Nature. 354:377-380.

39. CAFFREY, M. and HOGAN, J. 1992. LIPIDAT: A database of lipid phase transition temperatures and enthalpy changes. DMPC data subset analysis. Chem. Phys. Lipids. 61:1-109.

40. LYNCH, D. V., CAFFREY, M., HOGAN, J. and STEPONKUS, P. L. 1992. Calorimetric and x-ray diffraction studies of the thermotropic behavior of hydrated rye cerebrosides. Biophys. J. 61:1289-1300.

41. Mencke, A., Cheng, A-c. and Caffrey, M. 1993. A simple apparatus for time-resolved x-ray diffraction studies utilizing static pressures and pressure-jumps up to 300 MPa. Rev. Sci. Instrum. 64:383-389.

42. Chung, H. and Caffrey, M. 1992. Direct correlation of structure changes and thermal events in hydrated lipid established by simultaneous calorimetry and time-resolved x-ray difffraction. Biophys. J. 63:438-447.

43. CAFFREY, M. and WANG, J. 1992. Internal and interfacial structure of membranes using x-ray standing waves. Faraday Discuss. 94:283-293, 389-392.

44. WANG, J., BEDZYK, M. J. and CAFFREY, M. 1992. Resonance enhanced x-rays in thin films: A structure probe for membranes and surface layers. Science. 258:775-778..

45. CHENG, A-c., HOGAN, J. L. and CAFFREY, M. 1993. X-Rays destroy the lamellar structure of model membranes. J. Mol. Biol. 229:291-294.

46. Zhu, T. and Caffrey, M. 1993. Thermodynamics, thermomechanical and structure properties of an asymmetric phosphatidylcholine. Biophys. J. 65:939-954.

47. CHUNG, H. AND CAFFREY, M. 1994. The curvature elastic energy function of the cubic mesophase. Nature 368:224-226.

48. CHUNG, H. AND CAFFREY, M. 1994. The neutral area surface in cubic mesophases. Location and properties. Biophys. J. 66:377-381.

49. WANG, J. WALLACE, C., I. CLARK-LEWIS AND CAFFREY, M. 1994. Structure characterization of membrane bound and surface adsrobed protein. J. Mol. Biol. 237:1-4.

50. BRIGGS, J. AND CAFFREY, M. 1994. The temperature-composition phase diagram of the monomyristolein in water: Equilibrium and metastability aspects. Biophys. J. 66:573-587.

51. CHENG, A., B. HUMMEL, A. MENCKE AND M. CAFFREY. Kinetics and mechanism of the barotropic lamellar gel/lamellar liquid crystal phase transition in fully hydrated DHPE: A time-resolved x-ray diffraction study using pressure-jump. 1994. Biophys. J. 67:293-303.

52. Briggs, J. and Caffrey, M. 1994. The temperature-composition phase diagram and mesophase structure characterization of monopentadecenoin in water. Biophys. J. 67:1594-1602.

53. Wang, J., Caffrey, M., Bedzyk, M. J. and Penner T. L. 1994 . Structural changes in model membranes monitored by variable period x-ray standing waves. J. Phys. Chem. 98:10957-10968.

54. Wang, J., Caffrey, M. 1995. Locating calcium in membranes with x-ray standing waves. J. Am. Chem. Soc. 117:3304-3305.

55. Chung, H., Caffrey, M. 1995. Polymorphism, mesomorphism and metastability of monoelaidin in excess water. Biophys. J. 69:1951-1963.

56. Kirchner, S., Wang, J., Yin, Z., Caffrey, M. 1995. X-Ray standing waves as probes of surface structure: Incident beam energy effects. J. Appl. Physics. 78:2311-2322.

57. Cheng, A., Mencke, A., Caffrey, M. 1996. Manipulating mesophase behavior of hydrated DHPE: An x-ray diffraction study of temperature and pressure effects. J. Phys. Chem. 100:299-306.

58. Briggs, J., Chung, H., Caffrey, M. 1996. The temperature-composition phase diagram and mesophase structure characterization of the monoolein/water system. J. Physique II. France. 6:723-751.

59. Cheng, A., Caffrey, M. 1996. Mechanism of the Chain Melting Phase Transition In Model Membranes. J. Phys. Chem. 100:5608-5610.

60. Cheng, A., Caffrey, M. 1996. Free radical mediated x-ray damage of model membranes. Biophys. J. 70:2212-2222.

61. Itri, R., Zhang, R., Caffrey, M. 1997. Spatial resolution of the variable-period x-ray standing wave method as applied to model membranes. Biophys. J. 73:1506-1515.

62. Zhang, R., Itri, R. Caffrey, M. 1998. Membrane structure characterization using variable-period x-ray standing waves. Biophys. J. 74, 1924-1936.

63. Cheng, A., Hummel, B., Qiu, H., Caffrey, M. 1998. A Simple Mechanical Mixer for Small Viscous Lipid-Containing Samples. Chem. Phys. Lett. 95:11-21.

64. Qiu, H. Caffrey, M. 1998. Lyotropic and thermotropic phase behavior of hydrated monoacylglycerols: Structure characterization of monovaccenin. J. Phys. Chem. B. 102:4819- 4829.

65. Qiu, H., Caffrey, M. 1999. Lyotropic and Thermotropic Phase Behavior of Hydrated Monoeruccin. Chem. Phys. Lipids. 100:55-79

66. Qiu, H., Caffrey, M. 1999. Phase diagram of the monoolein/water system. Equilibrium and metastability aspects. Biomaterials. 21:223-234.

67. V. Cherezov, Cheng, A., Petit, J-M, Diat, O., Caffrey, M. 2000. Biophysics and Synchrotron Radiation. Where the Marriage Fails. X-Ray Damage of Lipid Membranes and Mesophases. Cell. Molec. Biology. 46:1133-1145.

68. Ai, X., Caffrey, M. 2000. Crystallizing membrane proteins in lipidic mesophases. Detergent effects. Biophys. J. 79: 394-405.

69. Clogston, J., Rathman, J., Tomasko, D., Walker, H., Caffrey, M. 2000. Phase behavior of a monoacylglycerol (Myverol 18-99K)/water system. Chem. Phys. Lipids 107:189-218.

70. Wang, J., Caffrey, M., Bedzyk, M., Penner, T. (2001) Direct Profiling and Reversibility of Ion Distribution at a Charged Membrane/Aqueous Interface: An X-ray Standing Wave Study. Langmuir 17; 3671-3681.

71. Cherezov, V., Fersi, H., Caffrey, M. Crystallization Screens: Compatibility with the lipidic cubic phase for in meso crystallization of membrane proteins. Biophys. J. 81: 225-242.

72. Y. Misquitta and M. Caffrey. (2001) Rational Design Of Lipid Molecular Structure. A Case Study Involving The C19:1c10 Monoacylglycerol. Biophys. J. 2001 81: 1047-1058.

73. M. R. Brzustowicz, V. Cherezov, M. Caffrey, W. Stillwell and S. R. Wassall. (2002) Molecular Organization of Cholesterol in Polyunsaturated Membranes: Microdomain Formation. Biophys. J. 82:285-298.

74. V. Cherezov, H. Qiu, V. Pector, M. Vandenbranden, J.-M. Ruysschaert and M. Caffrey. (2002) Biophysical and Transfection Studies of the diC14-Amidine/DNA Complex. Biophys. J. 82:3105-3117.

75. V. Cherezov, K. M. Riedl and M. Caffrey. (2002) Too hot to handle? Synchrotron x-ray damage of lipid membranes and mesophases. J. Synchrotron Radiation. 9:333-341.

76. Koynova, R., Caffrey, M. (2002). An index of lipid phase diagrams. Chem. Phys. Lipids. 115:107-219.

77. Brzustowicz, M. R., Cherezov, V., Zerouga, M., Caffrey, M., Stillwell, W., Wassall, S. R. (2002) Controlling Membrane Cholesterol Content. A Role for Polyunsaturated (Docosahexaenoate) Phospholipids.

Biochemistry 41:12509-12519.

78. Ravelli, R. B. G., Theveneau, P, McSweeney, S., Caffrey, M. (2002) Unit Cell Volume Change as a Metric of Radiation Damage in Crystals of Macromolecules. J. Synchrotron Rad. 9:355-360.

79. Cherezov, V. J. Clogston, Y. Misquitta, W. Abdel Gawad, M. Caffrey. (2002) Membrane Protein Crystallization In Meso. Lipid Type-Tailoring of the Cubic Phase. Biophys. J. 83:3393-3407.

80. Ravelli, R. B. G., Schrøder Leiros, H-K, Pan, B., Caffrey, M., McSweeney, S. Specific radiation damage can be used to solve macromolecular crystal structures. Structure. 11:217-224.

81. Cherezov, V., D. P. Siegel, W. Shaw, S. W. Burgess and M. Caffrey. 2003. The kinetics of non-lamellar phase formation in dope-me: relevance to biomembrane fusion. J. Memb. Biol. 195:165-182.

82. Shaikh, S. R., Cherezov, V., Caffrey, M., Stillwell, W., and Wassall, S. R. (2003) Interaction of Cholesterol with a Docosahexaenoic Acid Containing PE: Trigger for Microdomain/Raft Formation? Biochemistry. 42:12028-12037.

83. Cherezov, V., Caffrey, M. (2003) Nano-volume Plates with Excellent Optical Properties for Fast, Inexpensive Crystallization Screening of Membrane Proteins. J. Appl. Cryst. 36:1372-1377.

84. Misquitta, Y., Caffrey, M. (2003) Detergents Destabilize the Cubic Phase of Monoolein. Implications for Membrane Protein Crystallization. Biophys. J. 85:3084-3096.

85. Caffrey, M. (2003) Membrane Protein Crystallization. J. Struct. Biol. 142:108-132.

86. Shaikh, S. R., Cherezov, V., Caffrey, M., Stillwell, W., and Wassall, S. R. (2003) Interaction of

Cholesterol with a Docosahexaenoic Acid Containing PE: Trigger for Microdomain/Raft Formation?

Biochemistry. 42:12028-12037.

87. Cherezov, V., D. P. Siegel, W. Shaw, S. W. Burgess and M. Caffrey. 2003. The kinetics of non-lamellar phase formation in dope-me: relevance to biomembrane fusion. J. Memb. Biol. 195:165-182.

88. Cherezov, V., Caffrey, M. (2003) Nano-volume Plates with Excellent Optical Properties for Fast, Inexpensive Crystallization Screening of Membrane Proteins. J. Appl. Cryst. 36:1372-1377.

89. Misquitta, Y., Caffrey, M. (2003) Detergents Destabilize the Cubic Phase of Monoolein. Implications for Membrane Protein Crystallization. Biophys. J. 85:3084-3096.

90 Chen, W., Peddi, A., Zheng, Y.F. M. Caffrey. 2004. Automating Crystal Harvesting and Mounting for High-Throughput Macromolecular Crystallography. Proc. Of the 5th World Congress on Intelligent Control and Intelligent Automation, June 14-18, Hangzhou, China. In press.

91. Cherezov, V., Peddi, A., Muthusubramaniam, L., Zheng, Y.F. M. Caffrey. 2004. A Robotic System For Crystallizing Membrane And Soluble Proteins In Lipidic Mesophases. Acta Cryst. D60: 1795-1807.

92. Misquitta, Y., Cherezov, V., Havas, F., Patterson, S., Mohan, J., Wells, A., Hart, D., Caffrey, M. 2004. Rational Design of Lipid for Membrane Protein Crystallization. J. Struct. Biol. 148:169-175.

93. Wassall SR, Brzustowicz MR, Shaikh SR, Cherezov V, Caffrey M, Stillwell W. 2004. Order from disorder, corralling cholesterol with chaotic lipids. The role of polyunsaturated lipids in membrane raft formation. Chem Phys Lipids 132:79-88.

94. Misquitta, L.V., Misquitta, Y., Cherezov, V., Slattery, O., Mohan, J. M., Hart, D., Zhalnina, M., Cramer, W. A., Caffrey, M. 2004. Membrane protein crystallization in lipidic mesophases with tailored bilayers. Structure 12:2113-2124.

95. Clogston, J., Graciun, G., Hart, D. J., Caffrey, M. 2005. Controlling Release from the Lipidic Cubic Phase by Selective Alkylation. J. Controlled Release 102:441-461.

96. Liu, W., Caffrey, M. 2005. Gramicidin Structure and Disposition in Highly Curved Membranes. J. Struct. Biol. 150:23-40.

97. Cherezov, M., Caffrey, M. 2005. A simple and inexpensive nanoliter volume dispenser for highly viscous materials used in membrane protein crystallization. J. Appl. Cryst. 38:398-400.

98. Clogston, J., Caffrey, M. 2005. Controlling Release from the Cubic Phase. Amino acids, peptides, proteins and nucleic acids. J. Controlled Release 107:97-111.

99. Caffrey, M. 2005. Membrane protein crystallization in lipidic bicontinuous liquid crystals. In Bicontinuous Structured Liquid Crystals Surfactant Science Series. Vol. 127. Ed. Lynch, M., Spicer, P. T. pp. 307-319.

100. Peddi, A., Zheng, Y. F., Cherezov, V., Caffrey, M. 2005. Efficient and Effective Path for Automated Dispensing of Bio-Precipitant Solutions. Proc. IEEE Conference on Automation Science and Engineering, Edmonton, Canada.

101. Siegel, D. P., Cherezov, V., Greathouse, D. V., Koeppe II, R. E., Killian, J. A., Caffrey, M. 2006. Transmembrane Peptides Stabilize Inverted Cubic Phases in a Biphasic Length-dependent Manner: Implications for Protein-induced Membrane Fusion. Biophys. J. 90:200-211.

Raman, P., Cherezov, V., Caffrey, M. 2005. The Membrane Protein Data Bank. Cell Mol. Life Sci. 63:36-51.

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