The role of follicular smooth muscle cells in hamster ovulation

Martin, Gary G.; Talbot, Prudence

doi:10.1002/jez.1402160316

Cited by 67 publications

(39 citation statements)

References 31 publications

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“…The scaffold of microfilaments may provide the mechanical integrity that is required to resist forward progression of the radular tooth while venom is pressurizing behind it. The morphology (invagination of the nuclei and interdigitating plasma membranes) of these cells is similar to that of SMCs involved in hamster ovulation (Martin and Talbot, 1981). This is not surprising, as it has been noted that a cone snail can extend its proboscis greater than 15 times its contracted length in search of prey [approximately 1.5ϫ shell length (Greene and Kohn, 1989)].…”

Section: Discussionsupporting

confidence: 58%

Venom kinematics during prey capture inConus: the biomechanics of a rapid injection system

Salisbury

Martin

Kier

et al. 2010

Journal of Experimental Biology

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high-speed video. Using light, fluorescence and transmission electron microscopy (TEM), we assessed the composition and function of specific tissues crucial for prey capture. Our integrative experimental approach offers a more comprehensive understanding of this well-developed mechanism in Conus.Kinematic studies of the mollusc-hunting C. pennaceus indicate that a high-speed prey capture mechanism is not unique to cone species that hunt fish prey capable of rapid escape responses. Conus pennaceus SUMMARY Cone snails use an extensile, tubular proboscis as a conduit to deliver a potent cocktail of bioactive venom peptides into their prey. Previous studies have focused mainly on understanding the venom's role in prey capture but successful prey capture requires both rapid physiological and biomechanical mechanisms. Conus catus, a fish-hunting species, uses a high-speed hydraulic mechanism to inject its hollow, spear-like radular tooth into prey. We take an integrated approach to investigating the biomechanics of this process by coupling kinematic studies with morphological analyses. Taking advantage of the opaque venom and translucent proboscis of a mollusc-hunting juvenile cone snail, Conus pennaceus, we have determined that a high-speed prey capture mechanism is not unique to cone species that hunt fish prey. Two morphological structures were found to play crucial roles in this process. A constriction of the lumen near the tip of the proboscis, composed of tall epithelial cells densely packed with microfilaments, impedes forward movement of the radular tooth prior to its propulsion. Proximal to the constriction, a muscular sphincter was found to regulate venom flow and pressurization in the proboscis. In C. pennaceus, the rapid appearance and flushing of venom within the proboscis during prey capture suggests a mechanism involving the delivery of a discrete quantity of venom. The interplay between these elements provides a unique and effective biomechanical injection system for the fast-acting cone snail venom peptides. Supplementary material available online at

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Section: Discussionsupporting

confidence: 58%

Venom kinematics during prey capture inConus: the biomechanics of a rapid injection system

Salisbury

Martin

Kier

et al. 2010

Journal of Experimental Biology

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“…Some have referred to them as smooth muscle-like cells or myofibroblasts; others have called them smooth muscle cells. Martin and Talbot [1981a] demonstrated cells with all the morphological features of smooth muscle cells, including filaments with the dimensions of myosin, in walls of the hamster follicle (Fig. 11).…”

Section: Mammalsmentioning

confidence: 96%

“…These contractions alone do not induce ovulation, but there are reasons to believe that contraction of follicular smooth muscle cells is important in the normal progression of a follicle to ovulation. In hamsters, the smooth muscle cells of the theca externa have been shown by morphological criteria to contract prior to ovulation [Martin and Talbot, 1981a;Talbot and Chacon, 19821. Contracted cells can be identified in the electron microscope by their indented nucleus and ruffled plasma membrane.…”

Section: Mammalsmentioning

confidence: 99%

Ovulation in the animal kingdom: A review with an emphasis on the role of contractile processes

Schroeder

Talbot

1985

Gamete Research

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INTRODUCTIONIn most sexually reproducing animals, oocytes develop within an organized tissue sac, the follicle; oocytes and follicle cells are assembled together in the unovulated follicle, which is solid in all but therian mammals. Before fertilization, the oocyte generally abandons the follicle and moves to another site for subsequent spawning or further development. The process of escape from the follicle is termed ovulation; we shall also use this term to refer to the escape of the oocyte from its surrounding tissue in those metazoans that lack an organized follicle. In general, ovulation is at least a two-part phenomenon involving enzymatic degradation and rupture of the follicle followed by the actual movement of the oocyte out of the follicle. These steps were proposed by Schochet [1916] for mammalian ovulation, and by Rugh El9351 for frogs, and seem to be generally applicable to those phyla in which no intrafollicular antral space is present at the time of ovulation.We have reviewed information on the mechanism of oocyte extrusion in animals throughout the phylogenetic series, paying particular attention to the role of contractility in the process. Contraction of a follicle implies the presence of contractile cells in or around the follicle. A variety of contractile systems has been described in follicles from diverse animal types, and we feel it is now worthwhile to review the question of contractile mechanisms in ovulation from an evolutionary point of view. For each group we discuss, we will examine, to the extent information is available, 1) evidence that contractile cells are present near the developing oocyte, 2) experimental evidence that contractile cells are involved in ovulation, and 3) factors that may regulate contraction of these cells. It will become apparent that information on the mechanics of ovulation in other than eutherian mammals is scarce. Current information makes it clear that cells that are contractile or potentially capable of

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“…In these studies, rupture was identified as the first appearance of the cumulus mass. The stimulus for these pre-ovulatory changes was proposed to be stretch (Martin & Talbot, 1981a, b, 1987, neurotransmitters or both (Talbot & Chacon, 1982). It is unfortunate that intrafollicular cumulus expansion prevented us from obtaining data during this period.…”

Section: Discussionmentioning

confidence: 99%

Relaxation-induced contraction of smooth muscle surrounding hamster ovarian follicles

Self¹,

Koch²,

Schroeder³

1989

Reproduction

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Summary. Changes in intrafollicular pressure and follicular diameter resulting from injecting or withdrawing fluid from the antrum were measured in preovulatory follicles and used as an assay for changes in tension in the follicular wall by applying the Laplace relationship for thin-walled spheres. Passive length\p=n-\tension curves were constructed from pressure\p=n-\volume measurements to establish baseline wall stiffness. Any subsequent change in pressure could then be compared to the length\p=n-\tension curves to evaluate whether it arose from active tension development or from passive stretch. When intact follicles (1\p=n-\2 h before ovulation) were subjected to release of passive stretch, they exhibited a contractile response that lasted 15 sec\p=n-\2min and was characterized by cyclic increases and decreases in tension, with a period of 1 cycle every 2\ p=n-\ 3 sec. The probability of activating a response in the tissue was most strongly correlated with the rate of release of passive stretch. Intrafollicular pressures generated during active contractile responses sometimes reached 80 mmHg (10\m=.\64mPa), corresponding to a wall tension of 5332 dynes/cm (5\m=.\332N/m) (for a 1 mm follicle) and were clearly well above the passive length\p=n-\tension curves. Passive stretching of the follicular wall during a contractile response to 5-hydroxytryptamine stimulation resulted in large reductions in active wall tension for the duration of the stretch. These results are consistent with a stretch-activated inhibition of contractile events.

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The role of follicular smooth muscle cells in hamster ovulation

Cited by 67 publications

References 31 publications

Venom kinematics during prey capture inConus: the biomechanics of a rapid injection system

Venom kinematics during prey capture inConus: the biomechanics of a rapid injection system

Ovulation in the animal kingdom: A review with an emphasis on the role of contractile processes

Relaxation-induced contraction of smooth muscle surrounding hamster ovarian follicles

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