Modulation of Chlamydomonas Reinhardtii Flagellar Motility by Redox Poise

Overview

Journal J Cell Biol

Specialty Cell Biology

Date 2006 Jun 7

PMID 16754958

Citations 48

Authors

Ken-Ichi Wakabayashi

Stephen M King

Affiliations

Soon will be listed here.

Abstract

Redox-based regulatory systems are essential for many cellular activities. Chlamydomonas reinhardtii exhibits alterations in motile behavior in response to different light conditions (photokinesis). We hypothesized that photokinesis is signaled by variations in cytoplasmic redox poise resulting from changes in chloroplast activity. We found that this effect requires photosystem I, which generates reduced NADPH. We also observed that photokinetic changes in beat frequency and duration of the photophobic response could be obtained by altering oxidative/reductive stress. Analysis of reactivated cell models revealed that this redox poise effect is mediated through the outer dynein arms (ODAs). Although the global redox state of the thioredoxin-related ODA light chains LC3 and LC5 and the redox-sensitive Ca2+ -binding subunit of the docking complex DC3 did not change upon light/dark transitions, we did observe significant alterations in their interactions with other flagellar components via mixed disulfides. These data indicate that redox poise directly affects ODAs and suggest that it may act in the control of flagellar motility.

Citing Articles

COP5/HKR1 changes ciliary beat pattern and biases cell steering during chemotaxis in Chlamydomonas reinhardtii.

Strain A, Kratzberg N, Vu D, Miller E, Wakabayashi K, Melvin A Sci Rep. 2024; 14(1):30354.

PMID: 39639079 PMC: 11621555. DOI: 10.1038/s41598-024-81455-2.

Transcriptional analysis of primary ciliary dyskinesia airway cells reveals a dedicated cilia glutathione pathway.

Koenitzer J, Gupta D, Twan W, Xu H, Hadas N, Hawkins F JCI Insight. 2024; 9(17).

PMID: 39042459 PMC: 11385084. DOI: 10.1172/jci.insight.180198.

The methylome of motile cilia.

King S, Sakato-Antoku M, Patel-King R, Balsbaugh J Mol Biol Cell. 2024; 35(7):ar89.

PMID: 38696262 PMC: 11244166. DOI: 10.1091/mbc.E24-03-0130.

Analysis of Unique Motility of the Unicellular Green Alga at Low Temperatures down to -8 °C.

Yamashita K, Yamaguchi T, Ikeno S, Koyama A, Aono T, Mori A Micromachines (Basel). 2024; 15(3).

PMID: 38542657 PMC: 10972011. DOI: 10.3390/mi15030410.

Structure and Function of Dynein's Non-Catalytic Subunits.

Rao L, Gennerich A Cells. 2024; 13(4.

PMID: 38391943 PMC: 10886578. DOI: 10.3390/cells13040330.

References

Casey D, Inaba K, Pazour G, Takada S, Wakabayashi K, Wilkerson C . DC3, the 21-kDa subunit of the outer dynein arm-docking complex (ODA-DC), is a novel EF-hand protein important for assembly of both the outer arm and the ODA-DC. Mol Biol Cell. 2003; 14(9):3650-63. PMC: 196557. DOI: 10.1091/mbc.e03-01-0057. View

Gorman D, Levine R . Cytochrome f and plastocyanin: their sequence in the photosynthetic electron transport chain of Chlamydomonas reinhardi. Proc Natl Acad Sci U S A. 1965; 54(6):1665-9. PMC: 300531. DOI: 10.1073/pnas.54.6.1665. View

Finkel T, Holbrook N . Oxidants, oxidative stress and the biology of ageing. Nature. 2000; 408(6809):239-47. DOI: 10.1038/35041687. View

Sakakibara H, Mitchell D, Kamiya R . A Chlamydomonas outer arm dynein mutant missing the alpha heavy chain. J Cell Biol. 1991; 113(3):615-22. PMC: 2288963. DOI: 10.1083/jcb.113.3.615. View

Goyer A, Haslekas C, Miginiac-Maslow M, Klein U, Le Marechal P, Jacquot J . Isolation and characterization of a thioredoxin-dependent peroxidase from Chlamydomonas reinhardtii. Eur J Biochem. 2002; 269(1):272-82. DOI: 10.1046/j.0014-2956.2001.02648.x. View

Ogawa K, Mohri H . Studies on flagellar ATPase from sea urchin spermatozoa. I. Purification and some properties of the enzyme. Biochim Biophys Acta. 1972; 256(1):142-55. DOI: 10.1016/0005-2728(72)90169-7. View

Sakato M, King S . Calcium regulates ATP-sensitive microtubule binding by Chlamydomonas outer arm dynein. J Biol Chem. 2003; 278(44):43571-9. DOI: 10.1074/jbc.M305894200. View

Sadek C, Jimenez A, Damdimopoulos A, Kieselbach T, Nord M, Gustafsson J . Characterization of human thioredoxin-like 2. A novel microtubule-binding thioredoxin expressed predominantly in the cilia of lung airway epithelium and spermatid manchette and axoneme. J Biol Chem. 2003; 278(15):13133-42. PMC: 3158135. DOI: 10.1074/jbc.M300369200. View

Sakakibara H, Takada S, King S, Witman G, Kamiya R . A Chlamydomonas outer arm dynein mutant with a truncated beta heavy chain. J Cell Biol. 1993; 122(3):653-61. PMC: 2119660. DOI: 10.1083/jcb.122.3.653. View

10.

Padma P, Hozumi A, Ogawa K, Inaba K . Molecular cloning and characterization of a thioredoxin/nucleoside diphosphate kinase related dynein intermediate chain from the ascidian, Ciona intestinalis. Gene. 2001; 275(1):177-83. DOI: 10.1016/s0378-1119(01)00661-8. View

11.

Higo T, Hattori M, Nakamura T, Natsume T, Michikawa T, Mikoshiba K . Subtype-specific and ER lumenal environment-dependent regulation of inositol 1,4,5-trisphosphate receptor type 1 by ERp44. Cell. 2005; 120(1):85-98. DOI: 10.1016/j.cell.2004.11.048. View

12.

Josef K, Saranak J, Foster K . Ciliary behavior of a negatively phototactic Chlamydomonas reinhardtii. Cell Motil Cytoskeleton. 2005; 61(2):97-111. DOI: 10.1002/cm.20069. View

13.

Aksenov M, Aksenova M, Butterfield D, Geddes J, Markesbery W . Protein oxidation in the brain in Alzheimer's disease. Neuroscience. 2001; 103(2):373-83. DOI: 10.1016/s0306-4522(00)00580-7. View

14.

Hegemann P . Vision in microalgae. Planta. 1997; 203(3):265-74. DOI: 10.1007/s004250050191. View

15.

Huber H, Tabor S, Richardson C . Escherichia coli thioredoxin stabilizes complexes of bacteriophage T7 DNA polymerase and primed templates. J Biol Chem. 1987; 262(33):16224-32. View

16.

Witman G . Chlamydomonas phototaxis. Trends Cell Biol. 1993; 3(11):403-8. DOI: 10.1016/0962-8924(93)90091-e. View

17.

Shimizu T, Kimura I . Effects of N-ethylmaleimide on dynein adenosinetriphosphatase activity and its recombining ability with outer fibers. J Biochem. 1974; 76(5):1001-8. View

18.

Kunkel T, Patel S, Johnson K . Error-prone replication of repeated DNA sequences by T7 DNA polymerase in the absence of its processivity subunit. Proc Natl Acad Sci U S A. 1994; 91(15):6830-4. PMC: 44291. DOI: 10.1073/pnas.91.15.6830. View

19.

Baker M, Aitken R . The importance of redox regulated pathways in sperm cell biology. Mol Cell Endocrinol. 2004; 216(1-2):47-54. DOI: 10.1016/j.mce.2003.10.068. View

20.

Gibbons I, Fronk E . A latent adenosine triphosphatase form of dynein 1 from sea urchin sperm flagella. J Biol Chem. 1979; 254(1):187-96. View