Abstract
Actin carries out many of its cellular functions through its filamentous form; thus, understanding the detailed structure of actin filaments is an essential step in achieving a mechanistic understanding of actin function. The acrosomal bundle in the Limulus sperm has been shown to be a quasi-crystalline array with an asymmetric unit composed of a filament with 14 actin-scruin pairs. The bundle in its true discharge state penetrates the jelly coat of the egg. Our previous electron crystallographic reconstruction demonstrated that the actin filament cross-linked by scruin in this acrosomal bundle state deviates significantly from a perfect F-actin helix. In that study, the tertiary structure of each of the 14 actin protomers in the asymmetric unit of the bundle filament was assumed to be constant. In the current study, an actin filament atomic model in the acrosomal bundle has been refined by combining rigid-body docking with multiple actin crystal structures from the Protein Data Bank and constrained energy minimization. Our observation demonstrates that actin protomers adopt different tertiary conformations when they form an actin filament in the bundle. The scruin and bundle packing forces appear to influence the tertiary and quaternary conformations of actin in the filament of this biologically active bundle.
MeSH Terms
Acrosome Reaction
Actin Cytoskeleton/chemistry,ultrastructure
Actins/chemistry,ultrastructure
Animals
Biomechanical Phenomena
Crystallography, X-Ray
Horseshoe Crabs/chemistry,ultrastructure
Male
Models, Molecular
Protein Conformation
Protein Structure, Quaternary
Protein Structure, Tertiary
Spermatozoa/chemistry,ultrastructure
Chemicals
Actins
scruin protein, Horseshoe Crab
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Cong Yao
National Center for Macromolecular Imaging and Verna and Marrs McLean Department of Biochemistry and Molecular Biology, Baylor College of Medicine, Houston, TX 77030, USA. mschmid@bcm.tmc.edu
Topf Maya
Sali Andrej
Matsudaira Paul
Dougherty Matthew
Chiu Wah
Schmid Michael F
References (14)
14 references, click to expand
-
Stored elastic energy powers the 60-microm extension of the Limulus polyphemus sperm actin bundle.
J Cell Biol. 2003 Sep 29;162(7):1183-8
PMID: 14517201
-
Atomic structure of the actin:DNase I complex.
Nature. 1990 Sep 6;347(6288):37-44
PMID: 2395459
-
Actin-destabilizing factors disrupt filaments by means of a time reversal of polymerization.
Proc Natl Acad Sci U S A. 2004 Dec 21;101(51):17664-8
PMID: 15591338
-
Atomic model of the actin filament.
Nature. 1990 Sep 6;347(6288):44-9
PMID: 2395461
-
Hydrophobic loop dynamics and actin filament stability.
Biochemistry. 2006 Nov 14;45(45):13576-84
PMID: 17087511
-
Conformational dynamics of loop 262-274 in G- and F-actin.
Biochemistry. 2006 May 23;45(20):6541-9
PMID: 16700564
-
Using situs for flexible and rigid-body fitting of multiresolution single-molecule data.
J Struct Biol. 2001 Feb-Mar;133(2-3):193-202
PMID: 11472090
-
Crystal structure of polymerization-competent actin.
J Mol Biol. 2006 Sep 8;362(1):140-50
PMID: 16893553
-
Structure of the acrosomal bundle.
Nature. 2004 Sep 2;431(7004):104-7
PMID: 15343340
-
Motility powered by supramolecular springs and ratchets.
Science. 2000 Apr 7;288(5463):95-100
PMID: 10753126
-
Locking the hydrophobic loop 262-274 to G-actin surface by a disulfide bridge prevents filament formation.
Biochemistry. 2002 Sep 3;41(35):10787-93
PMID: 12196017
-
Cofilin changes the twist of F-actin: implications for actin filament dynamics and cellular function.
J Cell Biol. 1997 Aug 25;138(4):771-81
PMID: 9265645
-
Crystallographic analysis of acrosomal bundle from Limulus sperm.
J Mol Biol. 1991 Sep 20;221(2):711-25
PMID: 1920441
-
How does ATP hydrolysis control actin's associations?
Proc Natl Acad Sci U S A. 2002 Aug 20;99(17):10945-7
PMID: 12167670