Combinatorial cysteine mutagenesis reveals a critical intramonomer role for cysteines in prestin voltage sensing

Biophysical Journal

Volumn 99, Issue 1, 2010, Pages 85-94

  Bai, Jun Ping ^a   Surguchev, Alexei ^a   Bian, Shumin ^a   Song, Lei ^a   Santos Sacchi, Joseph ^a   Navaratnam, Dhasakumar ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANION TRANSPORT PROTEIN; CYSTEINE; DISULFIDE;

AMINO ACID SUBSTITUTION; ANIMAL; CHEMISTRY; CHO CELL LINE; CRICETULUS; ELECTRIC CAPACITANCE; ELECTRIC CONDUCTIVITY; GENETICS; GERBIL; HAMSTER; METABOLISM; MUTATION; PROTEIN FOLDING; PROTEIN MULTIMERIZATION; PROTEIN QUATERNARY STRUCTURE;

AMINO ACID SUBSTITUTION; ANIMALS; ANION TRANSPORT PROTEINS; CHO CELLS; CRICETINAE; CRICETULUS; CYSTEINE; DISULFIDES; ELECTRIC CAPACITANCE; ELECTRIC CONDUCTIVITY; GERBILLINAE; MUTATION; PROTEIN FOLDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY;

EID: 77954380094     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2010.03.066     Document Type: Article

References (37)

1. Zheng, J., L. D. Madison,..., P. Dallos, 2002. Prestin, the motor protein of outer hair cells. Audiol. Neurootol. 7:9-12. (Pubitemid 34253003)
2. Dallos, P., X. Wu,..., J. Zuo. 2008. Prestin-based outer hair cell motility is necessary for mammalian cochlear amplification. Neuron. 58:333-339. (Pubitemid 351615184)
3. Libennan, M. C., J. Gao,..., J. Zuo. 2002. Prestin is required for electromotility of the outer hair cell and for the cochlear amplifier. Nature. 419:300-304.
4. Santos-Sacchi, J., L. Song,..., A. L. Nuttall. 2006. Control of mammalian cochlear amplification by chloride anions. J. Neurosci. 26:3992-3998. (Pubitemid 44315419)
5. Brownell, W. E., C. R. Bader,..., Y. de Ribaupierre. 1985. Evoked mechanical responses of isolated cochlear outer hair cells. Science. 227:194-196.
6. Zheng, J., K. B. Long,..., P. Dallos. 2001 Prestin topology: localization of protein epitopes in relation to the plasma membrane. Neuroreport. 12:1929-1935.
7. Navaratnam, D., J. P. Bai,..., J. Santos-Sacchi. 2005. N-terminal-mediated homomultimerization of prestin, the outer hair cell motor protein. Biophys. J. 89:3345-3352. (Pubitemid 41636090)
8. Deak, L., J. Zheng,..., P. Dallos. 2005. Effects of cyclic nucleotides on the function of prestin. J. Physiol. 563:483-496.
9. Ludwig, J., D. Oliver,..., B. Fakler. 2001. Reciprocal electromechanical properties of rat prestin: The motor molecule from rat outer hair cells. Proc. Natl. Acad. Sci. USA. 98:4178-4183. (Pubitemid 32249918)
10. Gale, J. E., and J. F. Ashmore. 1994. Charge displacement induced by rapid stretch in the basolateral membrane of the guinea-pig outer hair cell. Proc. R. Soc. Lond. B. Biol. Sci. 255:243-249.
11. Kakehata, S., and J. Santos-Sacchi. 1995. Membrane tension directly shifts voltage dependence of outer hair cell motility and associated gating charge. Biophys. J. 68:2190-2197.
12. Iwasa, K. H. 2001. A two-state piezoelectric model for outer hair cell motility. Biophys. J. 81:2495-2506. (Pubitemid 33020039)
13. Iwasa, K. H. 1993. Effect of stress on the membrane capacitance of the auditory outer hair cell. Biophys. J. 65:492-498.
14. Bai, J. P., A. Surguchev,..., D. Navaratnam. 2009. Prestin's anion transport and voltage-sensing capabilities are independent. Biophys. J. 96:3179-3186.
15. Ashmore, J. F. 1989. Transducer motor coupling in cochlear outer hair cells. In Mechanics of Hearing. D. Kemp and J. P. Wilson, editors. Plenum Press, New York. 107-113.
16. Santos-Sacchi, J. 1991. Reversible inhibition of voltage-dependent outer hair cell motility and capacitance. J. Neurosci. 11:3096-3110.
17. Singh, R. 2008. A review of algorithmic techniques for disulfide-bond determination. Brief. Funct. Genomic. Proteomic 7:157-172. (Pubitemid 351728957)
18. Wedemeyer, W. J., E. Welker,..., H. A. Scheraga. 2000. Disulfide bonds and protein folding. Biochemistry. 39:4207-4216.
19. Hogg, P. J. 2003. Disulfide bonds as switches for protein function. Trends Biochem. Sci. 28:210-214.
20. Dorn, M., M. Weiwad,..., E. Bosse-Doenecke. 2009. Identification of a disulfide bridge essential for transport function, of the human proton-coupled amino acid transporter hPAT1. J. Biol. Chem. 284; 22123-22132.
21. Santos-Sacchi, J., and M. Wu. 2004. Protein- and lipid-reactive agents alter outer hair cell lateral membrane motor charge movement. J. Membr. Biol. 200:83-92.
22. Kalinec, F., and B. Kachar. 1993. Inhibition of outer hair cell electromotility by sulfhydryl specific reagents. Neurosci. Lett. 157:231-234. (Pubitemid 23245536)
23. McGuire, R., F. Pereira, and R. M. Raphael. 2008. Effects of cysteine mutations on prestin function and oligomerization. Assoc. Res. Otolaryngol. Abs. 675.
24. McGuire, R., F. Pereira, and R. M. Raphael. 2007. Modulation of prestin function due to cysteine point mutations. Assoc. Res. Otolaryngol. Abs. 1039.
25. Zheng, J., G. G. Du,..., M. Cheatham. 2006. Analysis of the oligomeric structure of the motor protein prestin. J. Biol. Chem. 281:19916-19924. (Pubitemid 44065765)
26. Santos-Sacchi, J. 2004. Determination of cell capacitance using the exact empirical solution of dY/dCm and its phase angle. Biophys. J. 87:714-727. (Pubitemid 38880123)
27. Santos-Sacchi, J., S. Kakehata, and S. Takahashi. 1998. Effects of membrane potential on the voltage dependence of motility-related charge in outer hair cells of the guinea-pig. J. Physiol. 510:225-235. (Pubitemid 28351937)
28. Mio, K., Y. Kubo,..., C. Sato. 2008. The motor protein prestin is a bullet-shaped molecule with inner cavities. J. Biol. Chem. 283:1137-1145.
29. Detro-Dassen, S., M. Schanzler,..., C. Fahlke. 2008. Conserved dimeric subunit stoichiometry of SLC26 multifunctional anion exchangers. J. Biol. Chem. 283:4177-4188.
30. Reference deleted in proof.
31. Ashmore, J. F. 1990. Forward and reverse transduction in the mammalian cochlea. Neurosci. Res. Suppl. 12:S39-S50.
32. Wolfenden, R., L. Andersson,..., C. C. Southgate. 1981. Affinities of amino acid side chains for solvent water. Biochemistry. 20:849-855.
33. Charton, M., and B. I. Charton. 1982. The structural dependence of amino acid hydrophobicity parameters. J. Theor. Biol. 99:629-644. (Pubitemid 13192303)
34. Okoruwa, O. E., M. D. Weston,..., K. W. Beisel. 2008. Evolutionary insights into the unique electromotility motor of mammalian outer hair cells. Evol. Dev. 10:300-315.
35. He, D. Z., K. W. Beisel,..., R. Salvi. 2003. Chick hair cells do not exhibit voltage-dependent somatic motility. J. Physiol. 546:511.-520.
36. Albert, J. T., H. Winter,..., D. Oliver. 2007. Voltage-sensitive prestin orthologue expressed in zebrafish hair cells. J. Physiol. 580:451-461.
37. Bon, S., F. Coussen, and J. Massoulie. 1997. Quaternary associations of acetylcholinesterase. II. The polyproline attachment domain of the collagen tail. J. Biol. Chem. 272:3016-3021. (Pubitemid 27053355)