Nematode sperm motility: nonpolar filament polymerization mediated by end-tracking motors.
In nematode sperm cell motility, major sperm protein (MSP) filament assembly results in dynamic membrane protrusions in a manner that closely resembles actin-based motility in other eukaryotic cells. Paradoxically, whereas actin-based motility is driven by addition of ATP-bound actin subunits onto actin filament plus-ends located at the cell membrane, MSP dimers assemble from solution into nonpolar filaments that lack a nucleotide binding site. Thus, filament polarity and on-filament ATP hydrolysis, although essential for actin-based motility, appear to be unnecessary for membrane protrusions by MSP. As a potential resolution to this paradox, we propose a model for MSP filament assembly and force generation by MSP filament end-tracking proteins. In this model, ATP hydrolysis drives affinity-modulated, processive interactions between membrane-associated proteins and elongating filament ends. However, in contrast to the "actoclampin" model for actin filament end-tracking motors, ATP activates the tracking protein (or a soluble cofactor) rather than the MSP subunits themselves (in contrast to activation of actin subunits by ATP binding). The MSP end-tracking model predicts properties that are consistent with several key observations of MSP-based motility, including persistent membrane attachment, polymerization of filament ends at the membrane with depolymerization of free-filament ends away from the membrane, as well as a saturating dependence of polymerization rate on the concentration of non-MSP soluble cytoplasmic components.
Dickinson
Richard B
RB
Department of Chemical Engineering, College of Engineeringne, University of Florida, Gainesville, Florida 32611, USA. dickinso@che.ufl.edu
Purich
Daniel L
DL
D000199:Actins / Q000737:chemistry / Q000502:physiology*; D000818:Animals; D003198:Computer Simulation; D015801:Helminth Proteins / Q000737:chemistry / Q000502:physiology*; D008297:Male; D008954:Models, Biological; D008956:Models, Chemical; D008958:Models, Molecular; D020409:Molecular Motor Proteins / Q000737:chemistry / Q000502:physiology*; D009348:Nematoda / Q000737:chemistry / Q000502:physiology*; D011108:Polymers / Q000737:chemistry; D013081:Sperm Motility / Q000502:physiology*; D013094:Spermatozoa / Q000737:chemistry / Q000502:physiology*
D000199:Actins; D015801:Helminth Proteins; D020409:Molecular Motor Proteins; D011108:Polymers; C050602:major sperm protein, nematode