Cytoplasmic dynein regulates its attachment to microtubules via nucleotide state-switched mechanosensing at multiple AAA domains

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 20, 2015, Pages 6371-6376

  Nicholas, Matthew P ^a   Berger, Florian ^b,c   Rao, Lu ^a   Brenner, Sibylle ^a   Cho, Carol ^d   Gennerich, Arne ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b MAX PLANCK INSTITUTE OF COLLOIDS AND INTERFACES   (Germany)

^c ROCKEFELLER UNIVERSITY   (United States)

^d STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

AAA+ ATPases; Cytoplasmic dynein; Mechanosensing; Microtubules; Optical tweezers

Indexed keywords

AAA1 ADENOSINE TRIPHOSPHATASE; AAA3 ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATASE; CYTOPLASMIC DYNEIN; FUNGAL ENZYME; NUCLEOTIDE; UNCLASSIFIED DRUG; ACYLTRANSFERASE; DYNEIN ADENOSINE TRIPHOSPHATASE; GREEN FLUORESCENT PROTEIN; NAT1 PROTEIN, S CEREVISIAE; PRIMER DNA; PROTEIN BINDING; SACCHAROMYCES CEREVISIAE PROTEIN;

ANISOTROPY; ARTICLE; BINDING AFFINITY; CELL ADHESION; CELL INTERACTION; CELLULAR, SUBCELLULAR AND MOLECULAR BIOLOGICAL PHENOMENA AND FUNCTIONS; CONTROLLED STUDY; CRYSTAL STRUCTURE; DICTYOSTELIUM; ENZYME CONFORMATION; ENZYME REGULATION; FORCE; HISTOGRAM; HYDROLYSIS; MECHANOSENSING; MICROTUBULE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN INTERACTION; YEAST; BIOMECHANICS; CYTOPLASM; GENETICS; IMMUNOLOGY; ISOLATION AND PURIFICATION; MECHANOTRANSDUCTION; METABOLISM; MUTAGENESIS; OPTICAL TWEEZERS; PHYSIOLOGY; SACCHAROMYCES CEREVISIAE;

ACETYLTRANSFERASES; ANISOTROPY; BIOMECHANICAL PHENOMENA; CYTOPLASM; DNA PRIMERS; DYNEINS; GREEN FLUORESCENT PROTEINS; MECHANOTRANSDUCTION, CELLULAR; MICROTUBULES; MUTAGENESIS; OPTICAL TWEEZERS; PROTEIN BINDING; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84929590759     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1417422112     Document Type: Article

References (50)

1. Vallee RB, McKenney RJ, Ori-McKenney KM (2012) Multiple modes of cytoplasmic dynein regulation. Nat Cell Biol 14(3):224-230.
2. Kardon JR, Vale RD (2009) Regulators of the cytoplasmic dynein motor. Nat Rev Mol Cell Biol 10(12):854-865.
3. Schmidt H, Gleave ES, Carter AP (2012) Insights into dynein motor domain function from a 3.3-Å crystal structure. Nat Struct Mol Biol 19(5):492-497, S1.
4. Kon T, et al. (2012) The 2.8 Å crystal structure of the dynein motor domain. Nature 484(7394):345-350.
5. Kon T, et al. (2009) Helix sliding in the stalk coiled coil of dynein couples ATPase and microtubule binding. Nat Struct Mol Biol 16(3):325-333.
6. Gibbons IR, et al. (2005) The affinity of the dynein microtubule-binding domain is modulated by the conformation of its coiled-coil stalk. J Biol Chem 280(25):23960-23965.
7. Kon T, Mogami T, Ohkura R, Nishiura M, Sutoh K (2005) ATP hydrolysis cycle-dependent tail motions in cytoplasmic dynein. Nat Struct Mol Biol 12(6):513-519.
8. Toropova K, et al. (2014) Lis1 regulates dynein by sterically blocking its mechanochemical cycle. eLife 3:e02641.
9. Bhabha G, et al. (2014) Allosteric communication in the dynein motor domain. Cell 159(4):857-868.
10. Reck-Peterson SL, et al. (2006) Single-molecule analysis of dynein processivity and stepping behavior. Cell 126(2):335-348.
11. Gennerich A, Carter AP, Reck-Peterson SL, Vale RD (2007) Force-induced bidirectional stepping of cytoplasmic dynein. Cell 131(5):952-965.
12. DeWitt MA, Chang AY, Combs PA, Yildiz A (2012) Cytoplasmic dynein moves through uncoordinated stepping of the AAA+ ring domains. Science 335(6065):221-225.
13. Qiu W, et al. (2012) Dynein achieves processive motion using both stochastic and coordinated stepping. Nat Struct Mol Biol 19(2):193-200.
14. Uemura S, et al. (2002) Kinesin-microtubule binding depends on both nucleotide state and loading direction. Proc Natl Acad Sci USA 99(9):5977-5981.
15. Yildiz A, Tomishige M, Gennerich A, Vale RD (2008) Intramolecular strain coordinates kinesin stepping behavior along microtubules. Cell 134(6):1030-1041.
16. Uemura S, Ishiwata S (2003) Loading direction regulates the affinity of ADP for kinesin. Nat Struct Biol 10(4):308-311.
17. Gebhardt JCM, Clemen AE-M, Jaud J, Rief M (2006) Myosin-V is a mechanical ratchet. Proc Natl Acad Sci USA 103(23):8680-8685.
18. Oguchi Y, et al. (2008) Load-dependent ADP binding to myosins V and VI: Implications for subunit coordination and function. Proc Natl Acad Sci USA 105(22):7714-7719.
19. Dunn AR, Chuan P, Bryant Z, Spudich JA (2010) Contribution of the myosin VI tail domain to processive stepping and intramolecular tension sensing. Proc Natl Acad Sci USA 107(17):7746-7750.
20. Cleary FB, et al. (2014) Tension on the linker gates the ATP-dependent release of dynein from microtubules. Nat Commun 5:4587.
21. Gibbons IR, et al. (1987) Photosensitized cleavage of dynein heavy chains. Cleavage at the "V1 site" by irradiation at 365 nm in the presence of ATP and vanadate. J Biol Chem 262(6):2780-2786.
22. Silvanovich A, Li MG, Serr M, Mische S, Hays TS (2003) The third P-loop domain in cytoplasmic dynein heavy chain is essential for dynein motor function and ATP-sensitive microtubule binding. Mol Biol Cell 14(4):1355-1365.
23. Kon T, Nishiura M, Ohkura R, Toyoshima YY, Sutoh K (2004) Distinct functions of nucleotide-binding/hydrolysis sites in the four AAA modules of cytoplasmic dynein. Biochemistry 43(35):11266-11274.
24. Takahashi Y, Edamatsu M, Toyoshima YY (2004) Multiple ATP-hydrolyzing sites that potentially function in cytoplasmic dynein. Proc Natl Acad Sci USA 101(35):12865-12869.
25. Cho C, Reck-Peterson SL, Vale RD (2008) Regulatory ATPase sites of cytoplasmic dynein affect processivity and force generation. J Biol Chem 283(38):25839-25845.
26. Reck-Peterson SL, Vale RD (2004) Molecular dissection of the roles of nucleotide binding and hydrolysis in dynein's AAA domains in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 101(6):1491-1495.
27. Evans E, Ritchie K (1997) Dynamic strength of molecular adhesion bonds. Biophys J 72(4):1541-1555.
28. Rakshit S, Zhang Y, Manibog K, Shafraz O, Sivasankar S (2012) Ideal, catch, and slip bonds in cadherin adhesion. Proc Natl Acad Sci USA 109(46):18815-18820.
29. Dembo M (1994) On peeling an adherent cell from a surface. Lectures on Mathematics in the Life Sciences, Some Mathematical Problems in Biology (American Mathematical Society, Providence, RI) Vol 24, pp 51-77.
30. Evans E (2001) Probing the relation between force - lifetime - and chemistry in single molecular bonds. Annu Rev Biophys Biomol Struct 30:105-128.
31. Kunwar A, et al. (2011) Mechanical stochastic tug-of-war models cannot explain bidirectional lipid-droplet transport. Proc Natl Acad Sci USA 108(47):18960-18965.
32. Leidel C, Longoria RA, Gutierrez FM, Shubeita GT (2012) Measuring molecular motor forces in vivo: Implications for tug-of-war models of bidirectional transport. Biophys J 103(3):492-500.
33. Rai AK, Rai A, Ramaiya AJ, Jha R, Mallik R (2013) Molecular adaptations allow dynein to generate large collective forces inside cells. Cell 152(1-2):172-182.
34. DeWitt MA, Cypranowska CA, Cleary FB, Belyy V, Yildiz A (2015) The AAA3 domain of cytoplasmic dynein acts as a switch to facilitate microtubule release. Nat Struct Mol Biol 22(1):73-80.
35. Yakovenko O, et al. (2008) FimH forms catch bonds that are enhanced by mechanical force due to allosteric regulation. J Biol Chem 283(17):11596-11605.
36. rd Ed.
37. Thomas W (2008) Catch bonds in adhesion. Annu Rev Biomed Eng 10:39-57.
38. Thomas WE, Vogel V, Sokurenko E (2008) Biophysics of catch bonds. Annu Rev Biophys 37:399-416.
39. Dudko OK, Hummer G, Szabo A (2008) Theory, analysis, and interpretation of single-molecule force spectroscopy experiments. Proc Natl Acad Sci USA 105(41):15755-15760.
40. Imamula K, Kon T, Ohkura R, Sutoh K (2007) The coordination of cyclic microtubule association/dissociation and tail swing of cytoplasmic dynein. Proc Natl Acad Sci USA 104(41):16134-16139.
41. Carter AP, et al. (2008) Structure and functional role of dynein's microtubule-binding domain. Science 322(5908):1691-1695.
42. Redwine WB, et al. (2012) Structural basis for microtubule binding and release by dynein. Science 337(6101):1532-1536.
43. Krebs A, Goldie KN, Hoenger A (2004) Complex formation with kinesin motor domains affects the structure of microtubules. J Mol Biol 335(1):139-153.
44. Huang J, Roberts AJ, Leschziner AE, Reck-Peterson SL (2012) Lis1 acts as a "clutch" between the ATPase and microtubule-binding domains of the dynein motor. Cell 150(5):975-986.
45. Carter AP (2013) Crystal clear insights into how the dynein motor moves. J Cell Sci 126(Pt 3):705-713.
46. Holzbaur ELF, Goldman YE (2010) Coordination of molecular motors: From in vitro assays to intracellular dynamics. Curr Opin Cell Biol 22(1):4-13.
47. Nicholas MP, Rao L, Gennerich A (2014) Covalent immobilization of microtubules on glass surfaces for molecular motor force measurements and other single-molecule assays. Methods Mol Biol 1136:137-169.
48. Gutiérrez-Medina B, Fehr AN, Block SM (2009) Direct measurements of kinesin torsional properties reveal flexible domains and occasional stalk reversals during stepping. Proc Natl Acad Sci USA 106(40):17007-17012.
49. Swoboda M, et al. (2012) Enzymatic oxygen scavenging for photostability without pH drop in single-molecule experiments. ACS Nano 6(7):6364-6369.
50. Nicholas MP, Rao L, Gennerich A (2014) An improved optical tweezers assay for measuring the force generation of single kinesin molecules. Methods Mol Biol 1136:171-246.