Emergence of Upstream Swimming via a Hydrodynamic Transition

Tung, Chih-kuan; Ardón, Florencia; Roy, Anubhab; Koch, Donald L.; Suárez, Susan S.; Wu, Mingming

doi:10.1103/physrevlett.114.108102

Cited by 111 publications

(107 citation statements)

References 42 publications

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“…Sperm motility behaviors were robust, as little variability was seen across samples from three different bulls. We reported in a previous publication that the chiral trajectories are caused by the near-surface resistive force exerted on the sperm head (11). Chiral swimming trajectories are characteristics of all near-surface pusher microswimmers (16,17).…”

Section: Resultsmentioning

confidence: 86%

“…Our work demonstrated that sperm upstream swimming is governed by near-surface hydrodynamic interaction, via the interactions of a front-back asymmetric microswimmer with a solid boundary. Therefore, when sperm are far away from a solid surface, there will be no force that orients them upstream (11). Moreover, the upstream swimming is governed by hydrodynamic bifurcation theory, which applies to a broad class of microswimmers that swim close to a surface and in a chiral trajectory (11).…”

Section: Sperm Swam Against a Gentle Flow Whereas T Foetus Were Sweptmentioning

confidence: 99%

“…Therefore, when sperm are far away from a solid surface, there will be no force that orients them upstream (11). Moreover, the upstream swimming is governed by hydrodynamic bifurcation theory, which applies to a broad class of microswimmers that swim close to a surface and in a chiral trajectory (11). In contrast, T. foetus exhibit swimming behaviors that are distinctly different from those of sperm.…”

Section: Sperm Swam Against a Gentle Flow Whereas T Foetus Were Sweptmentioning

confidence: 99%

“…In humans, a similar sexually transmitted pathogen, Trichomonas vaginalis, is reported by the World Health Organization to affect ∼170 million people annually worldwide and is associated with preterm birth and low birth weight (10). Although extensive work has been carried out in learning how sperm swim upstream to ascend the female tract (4,11), little is known about how pathogens gain access to upper regions of a female reproductive tract. In mammals, the female reproductive tract must protect itself against invasion by pathogens, yet facilitate passage of sperm to the site of fertilization (12).…”

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confidence: 99%

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Microgrooves and fluid flows provide preferential passageways for sperm over pathogen Tritrichomonas foetus

Tung¹,

Fiore³

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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Successful mammalian reproduction requires that sperm migrate through a long and convoluted female reproductive tract before reaching oocytes. For many years, fertility studies have focused on biochemical and physiological requirements of sperm. Here we show that the biophysical environment of the female reproductive tract critically guides sperm migration, while at the same time preventing the invasion of sexually transmitted pathogens. Using a microfluidic model, we demonstrate that a gentle fluid flow and microgrooves, typically found in the female reproductive tract, synergistically facilitate bull sperm migration toward the site of fertilization. In contrast, a flagellated sexually transmitted bovine pathogen, Tritrichomonas foetus, is swept downstream under the same conditions. We attribute the differential ability of sperm and T. foetus to swim against flow to the distinct motility types of sperm and T. foetus; specifically, sperm swim using a posterior flagellum and are near-surface swimmers, whereas T. foetus swims primarily via three anterior flagella and demonstrates much lower attraction to surfaces. This work highlights the importance of biophysical cues within the female reproductive tract in the reproductive process and provides insight into coevolution of males and females to promote fertilization while suppressing infection. Furthermore, the results provide previously unidentified directions for the development of in vitro fertilization devices and contraceptives.cell motility | cervix | microfluidics | microswimmer | trichomoniasis

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Section: Resultsmentioning

confidence: 86%

Section: Sperm Swam Against a Gentle Flow Whereas T Foetus Were Sweptmentioning

confidence: 99%

Section: Sperm Swam Against a Gentle Flow Whereas T Foetus Were Sweptmentioning

confidence: 99%

mentioning

confidence: 99%

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Microgrooves and fluid flows provide preferential passageways for sperm over pathogen Tritrichomonas foetus

Tung¹,

Fiore³

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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“…3E). The two distinct turning behaviors can then be inferred from basic force balance considerations (32,33,62): Approximating the flagellar beat envelope by a cone rotating counterclockwise around its symmetry axis, hydrodynamic interactions with the wall effectively result in a left-turning torque (Fig. 4).…”

Section: Discussionmentioning

confidence: 99%

Bimodal rheotactic behavior reflects flagellar beat asymmetry in human sperm cells

Bukatin

Kukhtevich

Stoop

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

101

125

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Rheotaxis, the directed response to fluid velocity gradients, has been shown to facilitate stable upstream swimming of mammalian sperm cells along solid surfaces, suggesting a robust physical mechanism for long-distance navigation during fertilization. However, the dynamics by which a human sperm orients itself relative to an ambient flow is poorly understood. Here, we combine microfluidic experiments with mathematical modeling and 3D flagellar beat reconstruction to quantify the response of individual sperm cells in time-varying flow fields. Single-cell tracking reveals two kinematically distinct swimming states that entail opposite turning behaviors under flow reversal. We constrain an effective 2D model for the turning dynamics through systematic large-scale parameter scans, and find good quantitative agreement with experiments at different shear rates and viscosities. Using a 3D reconstruction algorithm to identify the flagellar beat patterns causing left or right turning, we present comprehensive 3D data demonstrating the rolling dynamics of freely swimming sperm cells around their longitudinal axis. Contrary to current beliefs, this 3D analysis uncovers ambidextrous flagellar waveforms and shows that the cell's turning direction is not defined by the rolling direction. Instead, the different rheotactic turning behaviors are linked to a broken mirror symmetry in the midpiece section, likely arising from a buckling instability. These results challenge current theoretical models of sperm locomotion.sperm swimming | rheotaxis | fluid dynamics | microfluidics | simulations T axis, the directed kinematic response to external signals, is a defining feature of living things that affects their reproduction, foraging, migration, and survival strategies (1-4). Higher organisms rely on sophisticated networks of finely tuned sensory mechanisms to move efficiently in the presence of chemical or physical stimuli. However, various fundamental forms of taxis are already manifest at the unicellular level, ranging from chemotaxis in bacteria (5) and phototaxis in unicellular green algae (2) to the mechanical response (durotaxis) of fibroblasts (6) and rheotaxis (7, 8) in spermatozoa (3, 9-12). Over the last few decades, much progress has been made in deciphering chemotactic, phototactic, and durotactic pathways in prokaryotic and eukaryotic model systems. In contrast, comparatively little is known about the physical mechanisms that enable flow gradient sensing in sperm cells (3, 9-13). Recent studies (3, 12) suggest that mammalian sperm use rheotaxis for long-distance navigation, but it remains unclear how shear flows alter flagellar beat patterns in the vicinity of surfaces and, in particular, how such changes in the beat dynamics affect the steering process. Answering these questions will be essential for evaluating the importance of chemical (14) and physical (4) signals during mammalian fertilization (15-17).A necessary requirement for any form of directed kinematic response is the ability to change the direction of loco...

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Toll‐like receptor 2 mediates the immune response of the bovine oviductal ampulla to sperm binding

Morillo

Akthar

Fiorenza

et al. 2020

Molecular Reproduction Devel

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We previously reported that sperm binding to cultured bovine oviduct epithelial cells induces an anti-inflammatory immune response. Now we have developed a differentiated explant model to focus on the oviductal ampulla, where fertilization occurs, and to study the effect of sperm capacitation on the immune response. We used heparin to stimulate bovine sperm capacitation. Fluorescence imaging showed that 5,5ʹ,6,6ʹ-tetrachloro-1,1ʹ,3,3ʹ-tetraethylbenzimidazolyl-carbocyanine iodidelabeled sperm pretreated with (Hep (+)) or without (Hep (−)) heparin rapidly attached to the explant ciliated epithelium in similar numbers. However, only Hep (+) sperm upregulated explant messenger RNA (mRNA) transcription of TLR2, IL8, TGFB1, and PGES, without changes in TNFA and IL-10 expression, while Hep (−) sperm only upregulated PGES. The responses were primarily anti-inflammatory, with a greater response produced by Hep (+) sperm, which also produced a substantial increase in TLR2 protein expression in the epithelium. The addition of TLR1/2 (toll-like receptor 1/2) antagonist to the Hep (+) and (Hep (−)) sperm-explant coincubations reduced sperm attachment to the epithelium and inhibited TLR2 protein expression and some of the Hep (+) sperm-induced mRNA transcription. Our observations suggest that the ampullar epithelium immunologically reacts more strongly to sperm that have undergone heparin stimulation of capacitation. This anti-inflammatory

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Emergence of Upstream Swimming via a Hydrodynamic Transition

Cited by 111 publications

References 42 publications

Microgrooves and fluid flows provide preferential passageways for sperm over pathogen Tritrichomonas foetus

Microgrooves and fluid flows provide preferential passageways for sperm over pathogen Tritrichomonas foetus

Bimodal rheotactic behavior reflects flagellar beat asymmetry in human sperm cells

Toll‐like receptor 2 mediates the immune response of the bovine oviductal ampulla to sperm binding

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