Loss of ASP but not ROPN1 reduces mammalian ciliary motility

Cytoskeleton

Volumn 69, Issue 1, 2012, Pages 22-32

  Fiedler, Sarah E ^a,b   Sisson, Joseph H ^c   Wyatt, Todd A ^c   Pavlik, Jacqueline A ^c   Gambling, Todd M ^d   Carson, Johnny L ^d   Carr, Daniel W ^a,b  

^a PORTLAND VA MEDICAL CENTER   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^c UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^d UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

A kinase anchoring protein; OmniBank ; ROPN1L; Ropporin

Indexed keywords

CALCIUM BINDING PROTEIN; CALCIUM BINDING TYROSINE; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP DEPENDENT PROTEIN KINASE ANCHORING PROTEIN; ROPPORIN; SPERM PROTEIN 17; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL MOTILITY; CONTROLLED STUDY; FLAGELLUM; IN VIVO STUDY; MALE; MAMMAL CELL; MOUSE; MUTANT; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AMINO ACID SEQUENCE; ANIMALS; CILIA; CYCLIC AMP-DEPENDENT PROTEIN KINASES; GENOTYPE; MALE; MEMBRANE PROTEINS; MICE; MICE, MUTANT STRAINS; MOLECULAR SEQUENCE DATA; RHO GTP-BINDING PROTEINS; SIGNAL TRANSDUCTION; SPERM MOTILITY; SPERMATOZOA;

MAMMALIA; MUS;

EID: 84855920492     PISSN: 19493584     EISSN: 19493592     Source Type: Journal    
DOI: 10.1002/cm.20539     Document Type: Article

References (39)

1. Brody SL, Yan XH, Wuerffel MK, Song SK, Shapiro SD. 2000. Ciliogenesis and left-right axis defects in forkhead factor HFH-4-null mice. Am J Respir Cell Mol Biol 23 ( 1): 45-51.
2. Bush A, Cole P, Hariri M, Mackay I, Phillips G, O'Callaghan C, Wilson R, Warner JO. 1998. Primary ciliary dyskinesia: diagnosis and standards of care. Eur Respir J 12 ( 4): 982-988.
3. Carr DW, Newell AE. 2007. The role of A-kinase anchoring proteins (AKaps) in regulating sperm function. Soc Reprod Fertil Suppl 63: 135-141.
4. Carr DW, Fujita A, Stentz CL, Liberty GA, Olson GE, Narumiya S. 2001. Identification of sperm-specific proteins that interact with A-kinase anchoring proteins in a manner similar to the type II regulatory subunit of PKA. J Biol Chem 276 ( 20): 17332-17338.
5. Carr DW, Stofko-Hahn RE, Fraser ID, Bishop SM, Acott TS, Brennan RG, Scott JD. 1991. Interaction of the regulatory subunit (RII) of cAMP-dependent protein kinase with RII-anchoring proteins occurs through an amphipathic helix binding motif. J Biol Chem 266 ( 22): 14188-14192.
6. Chilvers MA, Rutman A, O'Callaghan C. 2003. Ciliary beat pattern is associated with specific ultrastructural defects in primary ciliary dyskinesia. J Allergy Clin Immunol 112 ( 3): 518-524.
7. de Iongh RU, Rutland J. 1995. Ciliary defects in healthy subjects, bronchiectasis, and primary ciliary dyskinesia. Am J Respir Crit Care Med 151 ( 5): 1559-1567.
8. Di Benedetto G, Manara-Shediac FS, Mehta A. 1991. Effect of cyclic AMP on ciliary activity of human respiratory epithelium. Eur Respir J 4 ( 7): 789-795.
9. Fiedler SE, Bajpai M, Carr DW. 2008. Identification and characterization of RHOA-interacting proteins in bovine spermatozoa. Biol Reprod 78 ( 1): 184-192.
10. Frayne J, Hall L. 2002. A re-evaluation of sperm protein 17 (Sp17) indicates a regulatory role in an A-kinase anchoring protein complex, rather than a unique role in sperm-zona pellucida binding. Reproduction 124 ( 6): 767-774.
11. Fujita A, Nakamura K, Kato T, Watanabe N, Ishizaki T, Kimura K, Mizoguchi A, Narumiya S. 2000. Ropporin, a sperm-specific binding protein of rhophilin, that is localized in the fibrous sheath of sperm flagella. J Cell Sci 113 ( Pt 1): 103-112.
12. Gaillard AR, Diener DR, Rosenbaum JL, Sale WS. 2001. Flagellar radial spoke protein 3 is an A-kinase anchoring protein (AKAP). J Cell Biol 153 ( 2): 443-448.
13. Gaillard AR, Fox LA, Rhea JM, Craige B, Sale WS. 2006. Disruption of the A-kinase anchoring domain in flagellar radial spoke protein 3 results in unregulated axonemal cAMP-dependent protein kinase activity and abnormal flagellar motility. Mol Biol Cell 17 ( 6): 2626-2635.
14. Hamasaki T, Barkalow K, Richmond J, Satir P. 1991. cAMP-stimulated phosphorylation of an axonemal polypeptide that copurifies with the 22S dynein arm regulates microtubule translocation velocity and swimming speed in Paramecium. Proc Natl Acad Sci USA 88 ( 18): 7918-7922.
15. Hasegawa E, Hayashi H, Asakura S, Kamiya R. 1987. Stimulation of in vitro motility of Chlamydomonas axonemes by inhibition of cAMP-dependent phosphorylation. Cell Motil Cytoskeleton 8 ( 4): 302-311.
16. Hendrickson TW, Perrone CA, Griffin P, Wuichet K, Mueller J, Yang P, Porter ME, Sale WS. 2004. IC138 is a WD-repeat dynein intermediate chain required for light chain assembly and regulation of flagellar bending. Mol Biol Cell 15 ( 12): 5431-5442.
17. Howard DR, Habermacher G, Glass DB, Smith EF, Sale WS. 1994. Regulation of Chlamydomonas flagellar dynein by an axonemal protein kinase. J Cell Biol 127 ( 6 Pt 1): 1683-1692.
18. Inglis PN, Boroevich KA, Leroux MR. 2006. Piecing together a ciliome. Trends Genet 22 ( 9): 491-500.
19. Jivan A, Earnest S, Juang YC, Cobb MH. 2009. Radial spoke protein 3 is a mammalian protein kinase A-anchoring protein that binds ERK1/2. J Biol Chem 284 ( 43): 29437-29445.
20. Kultgen PL, Byrd SK, Ostrowski LE, Milgram SL. 2002. Characterization of an A-kinase anchoring protein in human ciliary axonemes. Mol Biol Cell 13 ( 12): 4156-4166.
21. Livraghi A, Randell SH. 2007. Cystic fibrosis and other respiratory diseases of impaired mucus clearance. Toxicol Pathol 35 ( 1): 116-129.
22. Mall MA. 2008. Role of cilia, mucus, and airway surface liquid in mucociliary dysfunction: lessons from mouse models. J Aerosol Med Pulm Drug Deliv 21 ( 1): 13-24.
23. Naaby-Hansen S, Mandal A, Wolkowicz MJ, Sen B, Westbrook VA, Shetty J, Coonrod SA, Klotz KL, Kim YH, Bush LA, et al. 2002. CABYR, a novel calcium-binding tyrosine phosphorylation-regulated fibrous sheath protein involved in capacitation. Dev Biol 242 ( 2): 236-254.
24. Newell AE, Fiedler SE, Ruan JM, Pan J, Wang PJ, Deininger J, Corless CL, Carr DW. 2008. Protein kinase A RII-like (R2D2) proteins exhibit differential localization and AKAP interaction. Cell Motil Cytoskeleton 65 ( 7): 539-552.
25. Salathe M. 2007. Regulation of mammalian ciliary beating. Annu Rev Physiol 69: 401-422.
26. Salathe M, Pratt MM, Wanner A. 1993. Protein kinase C-dependent phosphorylation of a ciliary membrane protein and inhibition of ciliary beating. J Cell Sci 106 ( Pt 4): 1211-1220.
27. Sanderson MJ, Dirksen ER. 1989. Mechanosensitive and beta-adrenergic control of the ciliary beat frequency of mammalian respiratory tract cells in culture. Am Rev Respir Dis 139 ( 2): 432-440.
28. Sisson JH, Stoner JA, Ammons BA, Wyatt TA. 2003. All-digital image capture and whole-field analysis of ciliary beat frequency. J Microsc 211 ( Pt 2): 103-111.
29. Slager RE, Devasure JM, Pavlik JA, Sisson JH, Wyatt TA. 2008. RACK1, a PKC targeting protein, is exclusively localized to basal airway epithelial cells. J Histochem Cytochem 56 ( 1): 7-14.
30. Stannard W, O'Callaghan C. 2006. Ciliary function and the role of cilia in clearance. J Aerosol Med 19 ( 1): 110-115.
31. Tamaoki J, Kondo M, Takizawa T. 1989. Effect of cAMP on ciliary function in rabbit tracheal epithelial cells. J Appl Physiol 66 ( 3): 1035-1039.
32. Vander Top EA, Wyatt TA, Gentry-Nielsen MJ. 2005. Smoke exposure exacerbates an ethanol-induced defect in mucociliary clearance of Streptococcus pneumoniae. Alcohol Clin Exp Res 29 ( 5): 882-887.
33. Vijayaraghavan S, Goueli SA, Davey MP, Carr DW. 1997. Protein kinase A-anchoring inhibitor peptides arrest mammalian sperm motility. J Biol Chem 272 ( 8): 4747-4752.
34. Wirschell M, Zhao F, Yang C, Yang P, Diener D, Gaillard A, Rosenbaum JL, Sale WS. 2008. Building a radial spoke: flagellar radial spoke protein 3 (RSP3) is a dimer. Cell Motil Cytoskeleton 65 ( 3): 238-248.
35. Wong W, Scott JD. 2004. AKAP signalling complexes: focal points in space and time. Nat Rev Mol Cell Biol 5 ( 12): 959-970.
36. Wyatt TA, Spurzem JR, May K, Sisson JH. 1998. Regulation of ciliary beat frequency by both PKA and PKG in bovine airway epithelial cells. Am J Physiol 275 ( 4 Pt 1): L827-L835.
37. Yang C, Yang P. 2006. The flagellar motility of Chlamydomonas pf25 mutant lacking an AKAP-binding protein is overtly sensitive to medium conditions. Mol Biol Cell 17 ( 1): 227-238.
38. Yang P, Diener DR, Yang C, Kohno T, Pazour GJ, Dienes JM, Agrin NS, King SM, Sale WS, Kamiya R and others. 2006. Radial spoke proteins of Chlamydomonas flagella. J Cell Sci 119 ( Pt 6): 1165-1174.
39. Zambrowicz BP, Friedrich GA, Buxton EC, Lilleberg SL, Person C, Sands AT. 1998. Disruption and sequence identification of 2000 genes in mouse embryonic stem cells. Nature 392 ( 6676): 608-611.