Charles R. Sanders, II, Ph.D.


Visit Lab Site

Faculty Appointments
Professor of Biochemistry Aileen M. Lange and Annie Mary Lyle Chair in Cardiovascular ResearchProfessor of Medicine
Ph.D., Chemistry, Ohio State University, Columbus, OhioB.S., Chemistry and Mathematics, Milligan College, Milligan, Tennessee
Office Address
Nashville, TN 37232-8725
Research Description
Molecular Biophysical Basis of Diseases Related to Membrane Protein Dysfunction and Misfolding

A surprising number of diseases are caused or impacted by missense mutations in genes encoding membrane proteins that result in protein dysfunction and/or misfolding and mistrafficking early in the secretory pathway. We seek to elucidate the molecular biophysical mechanisms by which such mutations result in these defects. Our approach is to carry out studies of purified membrane proteins under well-controlled conditions and then correlating observations from these studies with what is known about the behavior of the corresponding mutant protein in vivo. We are pursuing several systems. We have discovered that the amyloid precursor protein (APP) that is closely associated with the development of Alzheimer's disease binds cholesterol in a way that may help to control production of the amyloid-beta polypeptide. We seek to understand exactly how and why cholesterol binds to APP and by what mechanisms this regulates amyloid-beta production. A second system involves Long QT Syndrome mutant forms of both the human KCNQ1 potassium channel and a modulatory partner, KCNE1. We are unraveling the mechanisms by which mutations in either of these proteins result in serious, even fatal cardiac arrhythmias. A third project involves a protein of the human peripheral nervous system known as peripheral myelin protein 22 (PMP22). PMP22 undergoes mutation-prompted misfolding which results in Charcot-Marie-Tooth Disease. We also study the integrin family or receptors that link the cell to the extracellular matrix, with a particular interest in integrins that are related to kidney function and fibrosis, as commonly occurs in type II diabetes. We also study TREM2, which seems to be a key player in neuroinflammation related to multiple neurodegenerative disorders, including Alzhheimer's, ALS, and Parkinson's These studies employ a wide range of techniques spanning the range from molecular biophysics/spectroscopy/biochemistry to cellular/molecular biology. Additional information is found at the lab web site:

Training in the Sanders Lab

Trainees in the Sanders lab are broadly trained in membrane protein biochemistry and biophysics. This often involves learning practical NMR spectroscopy. Trainees are also encouraged to broader their horizons even further by interacting closely with, or even carrying out experiments in the labs of our collaborators, who often more physiologically-oriented than the Sanders lab. Students are also constantly exhorted to master the literature related to their project and to develop a strong biomedical perspective for their work. Finally, the PI of this lab believes that is very important for trainees to be taught the ins and outs of the research culture, including funding strategies, peer review service, and how to be a good collaborator and colleague. See, for example the document "What is Expected of a Ph.D. Student or Postdoctoral Fellow in the Sanders Lab?" which can be viewed on-line at:
Clinical Description
A surprising number of diseases are caused or impacted by missense mutations in genes encoding membrane proteins that result in protein dysfunction and/or misfolding and mistrafficking early in the secretory pathway. We seek to elucidate the molecular biophysical mechanisms by which such mutations result in these defects.
Research Keywords
membrane proteins, disease, Alzheimer's, cardiac arrhythmias, kidney fibrosis, Charcot-Marie-Tooth, neurodegeneration, neurodegenerative, NMR, nuclear magenetic resonance, structural biology, structure, folding, misfolding, biochemistry, long QT syndrome, TREM2, amyloid, myelin, caveolin, membranes, lipid rafts, integrins, ion channels, lipids, personalized medicine, precision medicine
Clinical Research Keywords
Alzheimer's Charcot-Marie-Tooth Heart Disease Long QT Syndrome Kidney Disease ALS Parkinson's personalized medicine precision medicine
Sanders CR. Perplexing new insight into the dynamics of the EmrE transporter. J. Gen. Physiol [print-electronic]. 2015 Dec; 146(6): 441-4. PMID: 26573625, PMCID: PMC4664829, PII: jgp.201511523, DOI: 10.1085/jgp.201511523, ISSN: 1540-7748.

Chatterjee D, Eckert CE, Slavov C, Saxena K, Fürtig B, Sanders CR, Gurevich VV, Wachtveitl J, Schwalbe H. Influence of Arrestin on the Photodecay of Bovine Rhodopsin. Angew. Chem. Int. Ed. Engl [print-electronic]. 2015 Nov 11/9/2015; 54(46): 13555-60. PMID: 26383645, PMCID: PMC4685475, DOI: 10.1002/anie.201505798, ISSN: 1521-3773.

Zhang R, Sahu ID, Gibson KR, Muhammad NB, Bali AP, Comer RG, Liu L, Craig AF, Mccarrick RM, Dabney-Smith C, Sanders CR, Lorigan GA. Development of electron spin echo envelope modulation spectroscopy to probe the secondary structure of recombinant membrane proteins in a lipid bilayer. Protein Sci [print-electronic]. 2015 Nov; 24(11): 1707-13. PMID: 26355804, PMCID: PMC4622204, DOI: 10.1002/pro.2795, ISSN: 1469-896X.

Sahu ID, Craig AF, Dunagan MM, Troxel KR, Zhang R, Meiberg AG, Harmon CN, McCarrick RM, Kroncke BM, Sanders CR, Lorigan GA. Probing Structural Dynamics and Topology of the KCNE1 Membrane Protein in Lipid Bilayers via Site-Directed Spin Labeling and Electron Paramagnetic Resonance Spectroscopy. Biochemistry [print-electronic]. 2015 Oct 10/20/2015; 54(41): 6402-12. PMID: 26418890, DOI: 10.1021/acs.biochem.5b00505, ISSN: 1520-4995.

Schlebach JP, Narayan M, Alford C, Mittendorf KF, Carter BD, Li J, Sanders CR. Conformational Stability and Pathogenic Misfolding of the Integral Membrane Protein PMP22. J. Am. Chem. Soc [print-electronic]. 2015 Jul 7/15/2015; 137(27): 8758-68. PMID: 26102530, PMCID: PMC4507940, DOI: 10.1021/jacs.5b03743, ISSN: 1520-5126.

Deatherage CL, Lu Z, Kim JH, Sanders CR. Notch Transmembrane Domain: Secondary Structure and Topology. Biochemistry [print-electronic]. 2015 Jun 6/16/2015; 54(23): 3565-8. PMID: 26023825, PMCID: PMC4472088, DOI: 10.1021/acs.biochem.5b00456, ISSN: 1520-4995.

Schlebach JP, Sanders CR. Influence of Pathogenic Mutations on the Energetics of Translocon-Mediated Bilayer Integration of Transmembrane Helices. J. Membr. Biol [print-electronic]. 2015 Jun; 248(3): 371-81. PMID: 25192979, PMCID: PMC4362857, DOI: 10.1007/s00232-014-9726-0, ISSN: 1432-1424.

Kroncke BM, Vanoye CG, Meiler J, George AL, Sanders CR. Personalized biochemistry and biophysics. Biochemistry [print-electronic]. 2015 Apr 4/28/2015; 54(16): 2551-9. PMID: 25856502, PMCID: PMC4415889, DOI: 10.1021/acs.biochem.5b00189, ISSN: 1520-4995.

Wu J, Peng D, Zhang Y, Lu Z, Voehler M, Sanders CR, Li J. Biophysical characterization of interactions between the C-termini of peripheral nerve claudins and the PDZ1 domain of zonula occludens. Biochem. Biophys. Res. Commun [print-electronic]. 2015 Mar 3/27/2015; 459(1): 87-93. PMID: 25712527, PMCID: PMC4363178, PII: S0006-291X(15)00303-4, DOI: 10.1016/j.bbrc.2015.02.075, ISSN: 1090-2104.

Schlebach JP, Sanders CR. The safety dance: biophysics of membrane protein folding and misfolding in a cellular context. Q. Rev. Biophys [print-electronic]. 2015 Feb; 48(1): 1-34. PMID: 25420508, PMCID: PMC4339315, PII: S0033583514000110, DOI: 10.1017/S0033583514000110, ISSN: 1469-8994.

Chen Q, Vishnivetskiy SA, Zhuang T, Cho MK, Thaker TM, Sanders CR, Gurevich VV, Iverson TM. The rhodopsin-arrestin-1 interaction in bicelles. Methods Mol. Biol. 2015; 1271: 77-95. PMID: 25697518, PMCID: PMC4520306, DOI: 10.1007/978-1-4939-2330-4_6, ISSN: 1940-6029.

Sahu ID, Kroncke BM, Zhang R, Dunagan MM, Smith HJ, Craig A, McCarrick RM, Sanders CR, Lorigan GA. Structural investigation of the transmembrane domain of KCNE1 in proteoliposomes. Biochemistry [print-electronic]. 2014 Oct 10/14/2014; 53(40): 6392-401. PMID: 25234231, PMCID: PMC4196734, DOI: 10.1021/bi500943p, ISSN: 1520-4995.

Mittendorf KF, Kroncke BM, Meiler J, Sanders CR. The homology model of PMP22 suggests mutations resulting in peripheral neuropathy disrupt transmembrane helix packing. Biochemistry [print-electronic]. 2014 Oct 10/7/2014; 53(39): 6139-41. PMID: 25243937, PMCID: PMC4188248, DOI: 10.1021/bi500809t, ISSN: 1520-4995.

Kim JH, Peng D, Schlebach JP, Hadziselimovic A, Sanders CR. Modest effects of lipid modifications on the structure of caveolin-3. Biochemistry [print-electronic]. 2014 Jul 7/15/2014; 53(27): 4320-2. PMID: 24960539, PMCID: PMC4100780, DOI: 10.1021/bi5005238, ISSN: 1520-4995.

Peng D, Kim JH, Kroncke BM, Law CL, Xia Y, Droege KD, Van Horn WD, Vanoye CG, Sanders CR. Purification and structural study of the voltage-sensor domain of the human KCNQ1 potassium ion channel. Biochemistry [print-electronic]. 2014 Apr 4/1/2014; 53(12): 2032-42. PMID: 24606221, PMCID: PMC3977583, DOI: 10.1021/bi500102w, ISSN: 1520-4995.

Elias BC, Mathew S, Srichai MB, Palamuttam R, Bulus N, Mernaugh G, Singh AB, Sanders CR, Harris RC, Pozzi A, Zent R. The integrin ß1 subunit regulates paracellular permeability of kidney proximal tubule cells. J. Biol. Chem [print-electronic]. 2014 Mar 3/21/2014; 289(12): 8532-44. PMID: 24509849, PMCID: PMC3961677, PII: M113.526509, DOI: 10.1074/jbc.M113.526509, ISSN: 1083-351X.

Song Y, Mittendorf KF, Lu Z, Sanders CR. Impact of bilayer lipid composition on the structure and topology of the transmembrane amyloid precursor C99 protein. J. Am. Chem. Soc [print-electronic]. 2014 Mar 3/19/2014; 136(11): 4093-6. PMID: 24564538, PMCID: PMC3985881, DOI: 10.1021/ja4114374, ISSN: 1520-5126.

Song Y, Kenworthy AK, Sanders CR. Cholesterol as a co-solvent and a ligand for membrane proteins. Protein Sci [print-electronic]. 2014 Jan; 23(1): 1-22. PMID: 24155031, PMCID: PMC3892294, DOI: 10.1002/pro.2385, ISSN: 1469-896X.

Wu J, Peng D, Voehler M, Sanders CR, Li J. Structure and expression of a novel compact myelin protein - small VCP-interacting protein (SVIP). Biochem. Biophys. Res. Commun [print-electronic]. 2013 Oct 10/11/2013; 440(1): 173-8. PMID: 24055875, PMCID: PMC3828079, PII: S0006-291X(13)01537-4, DOI: 10.1016/j.bbrc.2013.09.056, ISSN: 1090-2104.

Sahu ID, McCarrick RM, Troxel KR, Zhang R, Smith HJ, Dunagan MM, Swartz MS, Rajan PV, Kroncke BM, Sanders CR, Lorigan GA. DEER EPR measurements for membrane protein structures via bifunctional spin labels and lipodisq nanoparticles. Biochemistry [print-electronic]. 2013 Sep 9/24/2013; 52(38): 6627-32. PMID: 23984855, PMCID: PMC3826088, DOI: 10.1021/bi4009984, ISSN: 1520-4995.

Song Y, Hustedt EJ, Brandon S, Sanders CR. Competition between homodimerization and cholesterol binding to the C99 domain of the amyloid precursor protein. Biochemistry [print-electronic]. 2013 Jul 7/30/2013; 52(30): 5051-64. PMID: 23865807, PMCID: PMC3758481, DOI: 10.1021/bi400735x, ISSN: 1520-4995.

Schlebach JP, Peng D, Kroncke BM, Mittendorf KF, Narayan M, Carter BD, Sanders CR. Reversible folding of human peripheral myelin protein 22, a tetraspan membrane protein. Biochemistry [print-electronic]. 2013 May 5/14/2013; 52(19): 3229-41. PMID: 23639031, PMCID: PMC3762913, DOI: 10.1021/bi301635f, ISSN: 1520-4995.

Barrett PJ, Chen J, Cho MK, Kim JH, Lu Z, Mathew S, Peng D, Song Y, Van Horn WD, Zhuang T, Sönnichsen FD, Sanders CR. The quiet renaissance of protein nuclear magnetic resonance. Biochemistry [print-electronic]. 2013 Feb 2/26/2013; 52(8): 1303-20. PMID: 23368985, PMCID: PMC3592982, DOI: 10.1021/bi4000436, ISSN: 1520-4995.

Yang T, Smith JA, Leake BF, Sanders CR, Meiler J, Roden DM. An allosteric mechanism for drug block of the human cardiac potassium channel KCNQ1. Mol. Pharmacol [print-electronic]. 2013 Feb; 83(2): 481-9. PMID: 23193163, PMCID: PMC3558809, PII: mol.112.081513, DOI: 10.1124/mol.112.081513, ISSN: 1521-0111.

Pester O, Barrett PJ, Hornburg D, Hornburg P, Pröbstle R, Widmaier S, Kutzner C, Dürrbaum M, Kapurniotu A, Sanders CR, Scharnagl C, Langosch D. The backbone dynamics of the amyloid precursor protein transmembrane helix provides a rationale for the sequential cleavage mechanism of ¿-secretase. J. Am. Chem. Soc [print-electronic]. 2013 Jan 1/30/2013; 135(4): 1317-29. PMID: 23265086, PMCID: PMC3560327, DOI: 10.1021/ja3112093, ISSN: 1520-5126.

Zhuang T, Chen Q, Cho MK, Vishnivetskiy SA, Iverson TM, Gurevich VV, Sanders CR. Involvement of distinct arrestin-1 elements in binding to different functional forms of rhodopsin. Proc. Natl. Acad. Sci. U.S.A [print-electronic]. 2013 Jan 1/15/2013; 110(3): 942-7. PMID: 23277586, PMCID: PMC3549108, PII: 1215176110, DOI: 10.1073/pnas.1215176110, ISSN: 1091-6490.

Howell SC, Fraser NJ, Mittal R, Huang L, Travis B, Breyer RM, Sanders CR. Correction to CHOBIMALT: A Cholesterol-Based Detergent. Biochemistry [print-electronic]. 2013 Jan 1/15/2013; 52(2): 445. PMID: 23289860, PMCID: PMC3560918, DOI: 10.1021/bi3017203, ISSN: 1520-4995.

Cymer F, Sanders CR, Schneider D. Analyzing oligomerization of individual transmembrane helices and of entire membrane proteins in E. coli: A hitchhiker's guide to GALLEX. Methods Mol. Biol. 2013; 932: 259-76. PMID: 22987358, DOI: 10.1007/978-1-62703-065-6_16, ISSN: 1940-6029.

Shi M, Pedchenko V, Greer BH, Van Horn WD, Santoro SA, Sanders CR, Hudson BG, Eichman BF, Zent R, Pozzi A. Enhancing integrin a1 inserted (I) domain affinity to ligand potentiates integrin a1ß1-mediated down-regulation of collagen synthesis. J. Biol. Chem [print-electronic]. 2012 Oct 10/12/2012; 287(42): 35139-52. PMID: 22888006, PMCID: PMC3471707, PII: M112.358648, DOI: 10.1074/jbc.M112.358648, ISSN: 1083-351X.

Mathew S, Lu Z, Palamuttam RJ, Mernaugh G, Hadziselimovic A, Chen J, Bulus N, Gewin LS, Voehler M, Meves A, Ballestrem C, Fässler R, Pozzi A, Sanders CR, Zent R. ß1 integrin NPXY motifs regulate kidney collecting-duct development and maintenance by induced-fit interactions with cytosolic proteins. Mol. Cell. Biol [print-electronic]. 2012 Oct; 32(20): 4080-91. PMID: 22869523, PMCID: PMC3457338, PII: MCB.00568-12, DOI: 10.1128/MCB.00568-12, ISSN: 1098-5549.

Mittendorf KF, Deatherage CL, Ohi MD, Sanders CR. Tailoring of membrane proteins by alternative splicing of pre-mRNA. Biochemistry [print-electronic]. 2012 Jul 7/17/2012; 51(28): 5541-56. PMID: 22708632, PMCID: PMC3448030, DOI: 10.1021/bi3007065, ISSN: 1520-4995.

Deatherage CL, Hadziselimovic A, Sanders CR. Purification and characterization of the human ¿-secretase activating protein. Biochemistry [print-electronic]. 2012 Jun 6/26/2012; 51(25): 5153-9. PMID: 22681044, PMCID: PMC3386298, DOI: 10.1021/bi300605u, ISSN: 1520-4995.

Barrett PJ, Song Y, Van Horn WD, Hustedt EJ, Schafer JM, Hadziselimovic A, Beel AJ, Sanders CR. The amyloid precursor protein has a flexible transmembrane domain and binds cholesterol. Science. 2012 Jun 6/1/2012; 336(6085): 1168-71. PMID: 22654059, PMCID: PMC3528355, PII: 336/6085/1168, DOI: 10.1126/science.1219988, ISSN: 1095-9203.

Lu Z, Van Horn WD, Chen J, Mathew S, Zent R, Sanders CR. Bicelles at low concentrations. Mol. Pharm [print-electronic]. 2012 Apr 4/2/2012; 9(4): 752-61. PMID: 22221179, PMCID: PMC3319193, DOI: 10.1021/mp2004687, ISSN: 1543-8392.

Van Horn WD, Sanders CR. Prokaryotic diacylglycerol kinase and undecaprenol kinase. Annu Rev Biophys [print-electronic]. 2012; 41: 81-101. PMID: 22224599, PMCID: PMC3575517, DOI: 10.1146/annurev-biophys-050511-102330, ISSN: 1936-1238.

Zhuang T, Jap BK, Sanders CR. Solution NMR approaches for establishing specificity of weak heterodimerization of membrane proteins. J. Am. Chem. Soc [print-electronic]. 2011 Dec 12/21/2011; 133(50): 20571-80. PMID: 22084929, PMCID: PMC3241871, DOI: 10.1021/ja208972h, ISSN: 1520-5126.

Barrett PJ, Sanders CR, Kaufman SA, Michelsen K, Jordan JB. NSAID-based ¿-secretase modulators do not bind to the amyloid-ß polypeptide. Biochemistry [print-electronic]. 2011 Nov 11/29/2011; 50(47): 10328-42. PMID: 21995415, PMCID: PMC3272834, DOI: 10.1021/bi201371j, ISSN: 1520-4995.

Sanders CR, Mittendorf KF. Tolerance to changes in membrane lipid composition as a selected trait of membrane proteins. Biochemistry [print-electronic]. 2011 Sep 9/20/2011; 50(37): 7858-67. PMID: 21848311, PMCID: PMC3172382, DOI: 10.1021/bi2011527, ISSN: 1520-4995.

Sakakura M, Hadziselimovic A, Wang Z, Schey KL, Sanders CR. Structural basis for the Trembler-J phenotype of Charcot-Marie-Tooth disease. Structure. 2011 Aug 8/10/2011; 19(8): 1160-9. PMID: 21827951, PMCID: PMC3154623, PII: S0969-2126(11)00203-6, DOI: 10.1016/j.str.2011.05.009, ISSN: 1878-4186.

Van Horn WD, Vanoye CG, Sanders CR. Working model for the structural basis for KCNE1 modulation of the KCNQ1 potassium channel. Curr. Opin. Struct. Biol [print-electronic]. 2011 Apr; 21(2): 283-91. PMID: 21296569, PMCID: PMC3070781, PII: S0959-440X(11)00002-9, DOI: 10.1016/, ISSN: 1879-033X.

Downey JD, Sanders CR, Breyer RM. Evidence for the presence of a critical disulfide bond in the mouse EP3¿ receptor. Prostaglandins Other Lipid Mediat [print-electronic]. 2011 Feb; 94(1-2): 53-8. PMID: 21236356, PMCID: PMC3065360, PII: S1098-8823(11)00006-2, DOI: 10.1016/j.prostaglandins.2010.12.007, ISSN: 1098-8823.

Borza CM, Chen X, Mathew S, Mont S, Sanders CR, Zent R, Pozzi A. Integrin {alpha}1{beta}1 promotes caveolin-1 dephosphorylation by activating T cell protein-tyrosine phosphatase. J. Biol. Chem [print-electronic]. 2010 Dec 12/17/2010; 285(51): 40114-24. PMID: 20940300, PMCID: PMC3000994, PII: M110.156729, DOI: 10.1074/jbc.M110.156729, ISSN: 1083-351X.

Zhuang T, Vishnivetskiy SA, Gurevich VV, Sanders CR. Elucidation of inositol hexaphosphate and heparin interaction sites and conformational changes in arrestin-1 by solution nuclear magnetic resonance. Biochemistry [print-electronic]. 2010 Dec 12/14/2010; 49(49): 10473-85. PMID: 21050017, PMCID: PMC3074303, DOI: 10.1021/bi101596g, ISSN: 1520-4995.

Howell SC, Mittal R, Huang L, Travis B, Breyer RM, Sanders CR. CHOBIMALT: a cholesterol-based detergent. Biochemistry. 2010 Nov 11/9/2010; 49(44): 9572-83. PMID: 20919740, PMCID: PMC3030671, DOI: 10.1021/bi101334j, ISSN: 1520-4995.

Koehler J, Sulistijo ES, Sakakura M, Kim HJ, Ellis CD, Sanders CR. Lysophospholipid micelles sustain the stability and catalytic activity of diacylglycerol kinase in the absence of lipids. Biochemistry. 2010 Aug 8/24/2010; 49(33): 7089-99. PMID: 20666483, PMCID: PMC2923640, DOI: 10.1021/bi100575s, ISSN: 1520-4995.

Beel AJ, Sakakura M, Barrett PJ, Sanders CR. Direct binding of cholesterol to the amyloid precursor protein: An important interaction in lipid-Alzheimer's disease relationships?. Biochim. Biophys. Acta [print-electronic]. 2010 Aug; 1801(8): 975-82. PMID: 20304095, PMCID: PMC2886191, PII: S1388-1981(10)00064-8, DOI: 10.1016/j.bbalip.2010.03.008, ISSN: 0006-3002.

Kelley KD, Olive LQ, Hadziselimovic A, Sanders CR. Look and see if it is time to induce protein expression in Escherichia coli cultures. Biochemistry. 2010 Jul 7/6/2010; 49(26): 5405-7. PMID: 20540494, PMCID: PMC2896908, DOI: 10.1021/bi1007194, ISSN: 1520-4995.

Vanoye CG, Welch RC, Tian C, Sanders CR, George AL. KCNQ1/KCNE1 assembly, co-translation not required. Channels (Austin) [print-electronic]. 2010 Mar; 4(2): 108-14. PMID: 20139709, PMCID: PMC3045044, PII: 11141, ISSN: 1933-6969.

Kang C, Vanoye CG, Welch RC, Van Horn WD, Sanders CR. Functional delivery of a membrane protein into oocyte membranes using bicelles. Biochemistry. 2010 Feb 2/2/2010; 49(4): 653-5. PMID: 20044833, PMCID: PMC2811756, DOI: 10.1021/bi902155t, ISSN: 1520-4995.

Van Horn WD, Beel AJ, Kang C, Sanders CR. The impact of window functions on NMR-based paramagnetic relaxation enhancement measurements in membrane proteins. Biochim. Biophys. Acta [print-electronic]. 2010 Feb; 1798(2): 140-9. PMID: 19751702, PMCID: PMC2812639, PII: S0005-2736(09)00301-0, DOI: 10.1016/j.bbamem.2009.08.022, ISSN: 0006-3002.

Beel AJ, Barrett P, Schnier PD, Hitchcock SA, Bagal D, Sanders CR, Jordan JB. Nonspecificity of binding of gamma-secretase modulators to the amyloid precursor protein. Biochemistry. 2009 Dec 12/22/2009; 48(50): 11837-9. PMID: 19928774, PMCID: PMC2794937, DOI: 10.1021/bi901839d, ISSN: 1520-4995.

Li Q, Mittal R, Huang L, Travis B, Sanders CR. Bolaamphiphile-class surfactants can stabilize and support the function of solubilized integral membrane proteins. Biochemistry. 2009 Dec 12/15/2009; 48(49): 11606-8. PMID: 19908902, PMCID: PMC2790596, DOI: 10.1021/bi9018708, ISSN: 1520-4995.

Kim HJ, Howell SC, Van Horn WD, Jeon YH, Sanders CR. Recent Advances in the Application of Solution NMR Spectroscopy to Multi-Span Integral Membrane Proteins. Prog Nucl Magn Reson Spectrosc. 2009 Nov 11/1/2009; 55(4): 335-60. PMID: 20161395, PMCID: PMC2782866, DOI: 10.1016/j.pnmrs.2009.07.002, ISSN: 1873-3301.

Vanacore R, Ham AJ, Voehler M, Sanders CR, Conrads TP, Veenstra TD, Sharpless KB, Dawson PE, Hudson BG. A sulfilimine bond identified in collagen IV. Science. 2009 Sep 9/4/2009; 325(5945): 1230-4. PMID: 19729652, PMCID: PMC2876822, PII: 325/5945/1230, DOI: 10.1126/science.1176811, ISSN: 1095-9203.

Vanoye CG, Welch RC, Daniels MA, Manderfield LJ, Tapper AR, Sanders CR, George AL. Distinct subdomains of the KCNQ1 S6 segment determine channel modulation by different KCNE subunits. J. Gen. Physiol [print-electronic]. 2009 Sep; 134(3): 207-17. PMID: 19687231, PMCID: PMC2737226, PII: jgp.200910234, DOI: 10.1085/jgp.200910234, ISSN: 1540-7748.

Koehler J, Woetzel N, Staritzbichler R, Sanders CR, Meiler J. A unified hydrophobicity scale for multispan membrane proteins. Proteins. 2009 Jul; 76(1): 13-29. PMID: 19089980, PMCID: PMC2761718, DOI: 10.1002/prot.22315, ISSN: 1097-0134.

Van Horn WD, Kim HJ, Ellis CD, Hadziselimovic A, Sulistijo ES, Karra MD, Tian C, Sönnichsen FD, Sanders CR. Solution nuclear magnetic resonance structure of membrane-integral diacylglycerol kinase. Science. 2009 Jun 6/26/2009; 324(5935): 1726-9. PMID: 19556511, PMCID: PMC2764269, PII: 324/5935/1726, DOI: 10.1126/science.1171716, ISSN: 1095-9203.

Abair TD, Sundaramoorthy M, Chen D, Heino J, Ivaska J, Hudson BG, Sanders CR, Pozzi A, Zent R. Cross-talk between integrins alpha1beta1 and alpha2beta1 in renal epithelial cells. Exp. Cell Res [print-electronic]. 2008 Nov 11/15/2008; 314(19): 3593-604. PMID: 18809396, PMCID: PMC2729514, PII: S0014-4827(08)00328-5, DOI: 10.1016/j.yexcr.2008.08.014, ISSN: 1090-2422.

Myers JK, Mobley CK, Sanders CR. The peripheral neuropathy-linked Trembler and Trembler-J mutant forms of peripheral myelin protein 22 are folding-destabilized. Biochemistry [print-electronic]. 2008 Oct 10/7/2008; 47(40): 10620-9. PMID: 18795802, PMCID: PMC2566783, DOI: 10.1021/bi801157p, ISSN: 1520-4995.

Beel AJ, Mobley CK, Kim HJ, Tian F, Hadziselimovic A, Jap B, Prestegard JH, Sanders CR. Structural studies of the transmembrane C-terminal domain of the amyloid precursor protein (APP): does APP function as a cholesterol sensor?. Biochemistry [print-electronic]. 2008 Sep 9/9/2008; 47(36): 9428-46. PMID: 18702528, PMCID: PMC2572687, DOI: 10.1021/bi800993c, ISSN: 1520-4995.

Kang C, Tian C, Sönnichsen FD, Smith JA, Meiler J, George AL, Vanoye CG, Kim HJ, Sanders CR. Structure of KCNE1 and implications for how it modulates the KCNQ1 potassium channel. Biochemistry [print-electronic]. 2008 Aug 8/5/2008; 47(31): 7999-8006. PMID: 18611041, PMCID: PMC2580054, DOI: 10.1021/bi800875q, ISSN: 1520-4995.

Beel AJ, Sanders CR. Substrate specificity of gamma-secretase and other intramembrane proteases. Cell. Mol. Life Sci. 2008 May; 65(9): 1311-34. PMID: 18239854, PMCID: PMC2569971, DOI: 10.1007/s00018-008-7462-2, ISSN: 1420-682X.

Smith JA, Vanoye CG, George AL, Meiler J, Sanders CR. Structural models for the KCNQ1 voltage-gated potassium channel. Biochemistry [print-electronic]. 2007 Dec 12/11/2007; 46(49): 14141-52. PMID: 17999538, PMCID: PMC2565492, DOI: 10.1021/bi701597s, ISSN: 0006-2960.

Tian C, Vanoye CG, Kang C, Welch RC, Kim HJ, George AL, Sanders CR. Preparation, functional characterization, and NMR studies of human KCNE1, a voltage-gated potassium channel accessory subunit associated with deafness and long QT syndrome. Biochemistry [print-electronic]. 2007 Oct 10/16/2007; 46(41): 11459-72. PMID: 17892302, PMCID: PMC2565491, DOI: 10.1021/bi700705j, ISSN: 0006-2960.

Mobley CK, Myers JK, Hadziselimovic A, Ellis CD, Sanders CR. Purification and initiation of structural characterization of human peripheral myelin protein 22, an integral membrane protein linked to peripheral neuropathies. Biochemistry [print-electronic]. 2007 Oct 10/2/2007; 46(39): 11185-95. PMID: 17824619, DOI: 10.1021/bi700855j, ISSN: 0006-2960.

Sanders CR. Visiting order on membrane proteins by using nanotechnology. Proc. Natl. Acad. Sci. U.S.A [print-electronic]. 2007 Apr 4/17/2007; 104(16): 6502-3. PMID: 17420448, PMCID: PMC1871815, PII: 0701950104, DOI: 10.1073/pnas.0701950104, ISSN: 0027-8424.

Mi D, Kim HJ, Hadziselimovic A, Sanders CR. Irreversible misfolding of diacylglycerol kinase is independent of aggregation and occurs prior to trimerization and membrane association. Biochemistry. 2006 Aug 8/22/2006; 45(33): 10072-84. PMID: 16906765, DOI: 10.1021/bi060887x, ISSN: 0006-2960.

Sanders CR, Sönnichsen F. Solution NMR of membrane proteins: practice and challenges. Magn Reson Chem. 2006 Jul; 44 Spec No: S24-40. PMID: 16826539, DOI: 10.1002/mrc.1816, ISSN: 0749-1581.

Tian C, Breyer RM, Kim HJ, Karra MD, Friedman DB, Karpay A, Sanders CR. Solution NMR spectroscopy of the human vasopressin V2 receptor, a G protein-coupled receptor. J. Am. Chem. Soc. 2005 Jun 6/8/2005; 127(22): 8010-1. PMID: 15926814, DOI: 10.1021/ja051161b, ISSN: 0002-7863.

Myers JK, Beihoffer LA, Sanders CR. Phenotology of disease-linked proteins. Hum. Mutat. 2005 Jan; 25(1): 90-7. PMID: 15580569, DOI: 10.1002/humu.20118, ISSN: 1098-1004.

Tian C, Karra MD, Ellis CD, Jacob J, Oxenoid K, Sönnichsen F, Sanders CR. Membrane protein preparation for TROSY NMR screening. Meth. Enzymol. 2005; 394: 321-34. PMID: 15808226, PII: S0076687905940123, DOI: 10.1016/S0076-6879(05)94012-3, ISSN: 0076-6879.

Oxenoid K, Kim HJ, Jacob J, Sönnichsen FD, Sanders CR. NMR assignments for a helical 40 kDa membrane protein. J. Am. Chem. Soc. 2004 Apr 4/28/2004; 126(16): 5048-9. PMID: 15099070, DOI: 10.1021/ja049916m, ISSN: 0002-7863.

Sanders CR, Kuhn Hoffmann A, Gray DN, Keyes MH, Ellis CD. French swimwear for membrane proteins. Chembiochem. 2004 Apr 4/2/2004; 5(4): 423-6. PMID: 15185363, DOI: 10.1002/cbic.200300830, ISSN: 1439-4227.

Nagy JK, Sanders CR. Destabilizing mutations promote membrane protein misfolding. Biochemistry. 2004 Jan 1/13/2004; 43(1): 19-25. PMID: 14705927, DOI: 10.1021/bi035918s, ISSN: 0006-2960.

Sanders CR, Myers JK. Disease-related misassembly of membrane proteins. Annu Rev Biophys Biomol Struct. 2004; 33: 25-51. PMID: 15139803, DOI: 10.1146/annurev.biophys.33.110502.140348, ISSN: 1056-8700.

Oxenoid K, Sönnichsen FD, Sanders CR. Topology and secondary structure of the N-terminal domain of diacylglycerol kinase. Biochemistry. 2002 Oct 10/22/2002; 41(42): 12876-82. PMID: 12379131, PII: bi020335o, ISSN: 0006-2960.

Gorzelle BM, Hoffman AK, Keyes MH, Gray DN, Ray DG, Sanders CR. Amphipols can support the activity of a membrane enzyme. J. Am. Chem. Soc. 2002 Oct 10/2/2002; 124(39): 11594-5. PMID: 12296714, PII: ja027051b, ISSN: 0002-7863.

Nagy JK, Sanders CR. A critical residue in the folding pathway of an integral membrane protein. Biochemistry. 2002 Jul 7/23/2002; 41(29): 9021-5. PMID: 12119015, PII: bi020318z, ISSN: 0006-2960.

Luchette PA, Prosser RS, Sanders CR. Oxygen as a paramagnetic probe of membrane protein structure by cysteine mutagenesis and (19)F NMR spectroscopy. J. Am. Chem. Soc. 2002 Feb 2/27/2002; 124(8): 1778-81. PMID: 11853456, PII: ja016748e, ISSN: 0002-7863.

Luchette, P.A., Prosser, R.S., and Sanders, C.R. Oxygen as a paramagnetic probe of membrane protein structure by cysteine mutagenesis and 19f NMR spectroscopy. J. American Chemical Society. 2002; 124: 1778-81.

Sanders CR, Ismail-Beigi F, McEnery MW. Mutations of peripheral myelin protein 22 result in defective trafficking through mechanisms which may be common to diseases involving tetraspan membrane proteins. Biochemistry. 2001 Aug 8/14/2001; 40(32): 9453-9. PMID: 11583144, ISSN: 0006-2960.

Nagy JK, Lonzer WL, Sanders CR. Kinetic study of folding and misfolding of diacylglycerol kinase in model membranes. Biochemistry. 2001 Jul 7/31/2001; 40(30): 8971-80. PMID: 11467959, PII: bi010202n, ISSN: 0006-2960.

Nagy JK, Kuhn Hoffmann A, Keyes MH, Gray DN, Oxenoid K, Sanders CR. Use of amphipathic polymers to deliver a membrane protein to lipid bilayers. FEBS Lett. 2001 Jul 7/20/2001; 501(2-3): 115-20. PMID: 11470268, PII: S0014-5793(01)02627-8, ISSN: 0014-5793.

Oxenoid K, Sönnichsen FD, Sanders CR. Conformationally specific misfolding of an integral membrane protein. Biochemistry. 2001 May 5/1/2001; 40(17): 5111-8. PMID: 11318632, PII: bi0029090, ISSN: 0006-2960.

Sanders CR, Oxenoid K. Customizing model membranes and samples for NMR spectroscopic studies of complex membrane proteins. Biochim. Biophys. Acta. 2000 Nov 11/23/2000; 1508(1-2): 129-45. PMID: 11090822, PII: S0005-2736(00)00308-4, ISSN: 0006-3002.

Czerski L, Sanders CR. Functionality of a membrane protein in bicelles. Anal. Biochem. 2000 Sep 9/10/2000; 284(2): 327-33. PMID: 10964416, PII: S0003-2697(00)94720-1, DOI: 10.1006/abio.2000.4720, ISSN: 0003-2697.

Sanders CR, Nagy JK. Misfolding of membrane proteins in health and disease: the lady or the tiger?. Curr. Opin. Struct. Biol. 2000 Aug; 10(4): 438-42. PMID: 10981632, PII: S0959-440X(00)00112-3, ISSN: 0959-440X.

Czerski L, Vinogradova O, Sanders CR. NMR-Based amide hydrogen-deuterium exchange measurements for complex membrane proteins: development and critical evaluation. J. Magn. Reson. 2000 Jan; 142(1): 111-9. PMID: 10617441, PII: S1090-7807(99)91920-1, DOI: 10.1006/jmre.1999.1920, ISSN: 1090-7807.

Czerski, L.,Sanders, C.R. Thiol modification of membrane proteins dependence upon protein site membrane disposition and reagent hydrophobicity. FEBS Letters. 2000; 472: 225-9.

L. Czerski, O. Vinogradova, and C.R. Sanders. NMR-based amide hydrogen-deuterium exchange measurements for complex membrane proteins: development and critical evaluation. J. of Magnetic Resonance. 2000; 142: 111-9.

Gorzelle BM, Nagy JK, Oxenoid K, Lonzer WL, Cafiso DS, Sanders CR. Reconstitutive refolding of diacylglycerol kinase, an integral membrane protein. Biochemistry. 1999 Dec 12/7/1999; 38(49): 16373-82. PMID: 10587463, PII: bi991292n, ISSN: 0006-2960.

Sanders CR, Prosser RS. Bicelles: a model membrane system for all seasons?. Structure. 1998 Oct 10/15/1998; 6(10): 1227-34. PMID: 9782059, PII: S0969-2126(98)00123-3, ISSN: 0969-2126.

Vinogradova O, Carlin C, Sonnichsen FD, Sanders CR. A membrane setting for the sorting motifs present in the adenovirus E3-13.7 protein which down-regulates the epidermal growth factor receptor. J. Biol. Chem. 1998 Jul 7/10/1998; 273(28): 17343-50. PMID: 9651317, ISSN: 0021-9258.

Vinogradova O, Sönnichsen F, Sanders CR. On choosing a detergent for solution NMR studies of membrane proteins. J. Biomol. NMR. 1998 May; 11(4): 381-6. PMID: 9691283, ISSN: 0925-2738.

Badola P, Sanders CR. Escherichia coli diacylglycerol kinase is an evolutionarily optimized membrane enzyme and catalyzes direct phosphoryl transfer. J. Biol. Chem. 1997 Sep 9/26/1997; 272(39): 24176-82. PMID: 9305868, ISSN: 0021-9258.

Vinogradova O, Badola P, Czerski L, Sönnichsen FD, Sanders CR. Escherichia coli diacylglycerol kinase: a case study in the application of solution NMR methods to an integral membrane protein. Biophys. J. 1997 Jun; 72(6): 2688-701. PMID: 9168044, PMCID: PMC1184466, PII: S0006-3495(97)78912-4, DOI: 10.1016/S0006-3495(97)78912-4, ISSN: 0006-3495.

Sanders CR, Landis GC. Reconstitution of membrane proteins into lipid-rich bilayered mixed micelles for NMR studies. Biochemistry. 1995 Mar 3/28/1995; 34(12): 4030-40. PMID: 7696269, ISSN: 0006-2960.

Smith RL, O'Toole JF, Maguire ME, Sanders CR. Membrane topology of Escherichia coli diacylglycerol kinase. J. Bacteriol. 1994 Sep; 176(17): 5459-65. PMID: 8071224, PMCID: PMC196734, ISSN: 0021-9193.

Sanders CR. Qualitative comparison of the bilayer-associated structures of diacylglycerol and a fluorinated analog based upon oriented sample NMR data. Chem. Phys. Lipids. 1994 Jun 6/24/1994; 72(1): 41-57. PMID: 7923479, PII: 0009-3084(94)90016-7, ISSN: 0009-3084.

C. R. Sanders and G. C. Landis. Facile Acquisition and Assignment of Oriented Sample NMR Spectra for Bilayer Surface-Associated Proteins. Journal of the American Chemical Society. 1994; 116: 6470-1.

C. R. Sanders, B. J. Hare, K. Howard, and James H. Prestegard. Magnetically Oriented Phospholipid Micelles as a Tool for the Study of Membrane-Associated Molecules. Progress in NMR Spectroscopy. 1994; 26: 421-44.

Hare BJ, Sanders CR, McIntyre SE, Prestegard JH. Synthesis and characterization of a 13C-labeled alpha-mannosyl glycolipid analog from [13C]glucose. Chem. Phys. Lipids. 1993 Nov; 66(1-2): 155-8. PMID: 8118915, PII: 0009-3084(93)90040-A, ISSN: 0009-3084.

Sanders CR, Schwonek JP. Simulation of NMR data from oriented membrane proteins: practical information for experimental design. Biophys. J. 1993 Oct; 65(4): 1460-9. PMID: 8274640, PMCID: PMC1225873, PII: S0006-3495(93)81215-3, DOI: 10.1016/S0006-3495(93)81215-3, ISSN: 0006-3495.

Sanders CR, Schwonek JP. An approximate model and empirical energy function for solute interactions with a water-phosphatidylcholine interface. Biophys. J. 1993 Sep; 65(3): 1207-18. PMID: 8241401, PMCID: PMC1225840, PII: S0006-3495(93)81158-5, DOI: 10.1016/S0006-3495(93)81158-5, ISSN: 0006-3495.

Sanders CR, Schaff JE, Prestegard JH. Orientational behavior of phosphatidylcholine bilayers in the presence of aromatic amphiphiles and a magnetic field. Biophys. J. 1993 Apr; 64(4): 1069-80. PMID: 8494971, PMCID: PMC1262425, PII: S0006-3495(93)81473-5, DOI: 10.1016/S0006-3495(93)81473-5, ISSN: 0006-3495.

Sanders CR. Solid state 13C NMR of unlabeled phosphatidylcholine bilayers: spectral assignments and measurement of carbon-phosphorus dipolar couplings and 13C chemical shift anisotropies. Biophys. J. 1993 Jan; 64(1): 171-81. PMID: 8431541, PMCID: PMC1262314, PII: S0006-3495(93)81352-3, DOI: 10.1016/S0006-3495(93)81352-3, ISSN: 0006-3495.

Ikeda-Saito M, Hori H, Andersson LA, Prince RC, Pickering IJ, George GN, Sanders CR, Lutz RS, McKelvey EJ, Mattera R. Coordination structure of the ferric heme iron in engineered distal histidine myoglobin mutants. J. Biol. Chem. 1992 Nov 11/15/1992; 267(32): 22843-52. PMID: 1429633, ISSN: 0021-9258.

Sanders CR, Schwonek JP. Characterization of magnetically orientable bilayers in mixtures of dihexanoylphosphatidylcholine and dimyristoylphosphatidylcholine by solid-state NMR. Biochemistry. 1992 Sep 9/22/1992; 31(37): 8898-905. PMID: 1390677, ISSN: 0006-2960.

Sanders CR, Prestegard JH. Magnetically orientable phospholipid bilayers containing small amounts of a bile salt analogue, CHAPSO. Biophys. J. 1990 Aug; 58(2): 447-60. PMID: 2207249, PMCID: PMC1280985, PII: S0006-3495(90)82390-0, DOI: 10.1016/S0006-3495(90)82390-0, ISSN: 0006-3495.

Sanders CR, Tian GC, Tsai MD. Mechanism of adenylate kinase. Is there a relationship between local substrate dynamics, local binding energy, and the catalytic mechanism?. Biochemistry. 1989 Nov 11/14/1989; 28(23): 9028-43. PMID: 2557915, ISSN: 0006-2960.

Sanders CR, Tsai MD. Ligand-protein interactions via nuclear magnetic resonance of quadrupolar nuclei. Meth. Enzymol. 1989; 177: 317-33. PMID: 2607986, PII: 0076-6879(89)77018-X, ISSN: 0076-6879.