Rolling controls sperm navigation in response to the dynamic rheological properties of the environment
Mammalian sperm rolling around their longitudinal axes is a long-observed component of motility, but its function in the fertilization process, and more specifically in sperm migration within the female reproductive tract, remains elusive. While investigating bovine sperm motion under simple shear f...
| Main Authors: | , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
eLife Sciences Publications Ltd
2021-08-01
|
| Series: | eLife |
| Subjects: | |
| Online Access: | https://elifesciences.org/articles/68693 |
| _version_ | 1811201520360751104 |
|---|---|
| author | Meisam Zaferani Farhad Javi Amir Mokhtare Peilong Li Alireza Abbaspourrad |
| author_facet | Meisam Zaferani Farhad Javi Amir Mokhtare Peilong Li Alireza Abbaspourrad |
| author_sort | Meisam Zaferani |
| collection | DOAJ |
| description | Mammalian sperm rolling around their longitudinal axes is a long-observed component of motility, but its function in the fertilization process, and more specifically in sperm migration within the female reproductive tract, remains elusive. While investigating bovine sperm motion under simple shear flow and in a quiescent microfluidic reservoir and developing theoretical and computational models, we found that rolling regulates sperm navigation in response to the rheological properties of the sperm environment. In other words, rolling enables a sperm to swim progressively even if the flagellum beats asymmetrically. Therefore, a rolling sperm swims stably along the nearby walls (wall-dependent navigation) and efficiently upstream under an external fluid flow (rheotaxis). By contrast, an increase in ambient viscosity and viscoelasticity suppresses rolling, consequently, non-rolling sperm are less susceptible to nearby walls and external fluid flow and swim in two-dimensional diffusive circular paths (surface exploration). This surface exploration mode of swimming is caused by the intrinsic asymmetry in flagellar beating such that the curvature of a sperm’s circular path is proportional to the level of asymmetry. We found that the suppression of rolling is reversible and occurs in sperm with lower asymmetry in their beating pattern at higher ambient viscosity and viscoelasticity. Consequently, the rolling component of motility may function as a regulatory tool allowing sperm to navigate according to the rheological properties of the functional region within the female reproductive tract. |
| first_indexed | 2024-04-12T02:21:52Z |
| format | Article |
| id | doaj.art-15eaabf83a4d49519beefe0e3f25ade6 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-12T02:21:52Z |
| publishDate | 2021-08-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-15eaabf83a4d49519beefe0e3f25ade62022-12-22T03:52:05ZengeLife Sciences Publications LtdeLife2050-084X2021-08-011010.7554/eLife.68693Rolling controls sperm navigation in response to the dynamic rheological properties of the environmentMeisam Zaferani0Farhad Javi1Amir Mokhtare2Peilong Li3Alireza Abbaspourrad4https://orcid.org/0000-0001-5617-9220Department of Food Science, College of Agriculture and Life Sciences, Cornell University, Ithaca, United StatesDepartment of Food Science, College of Agriculture and Life Sciences, Cornell University, Ithaca, United StatesDepartment of Food Science, College of Agriculture and Life Sciences, Cornell University, Ithaca, United StatesDepartment of Food Science, College of Agriculture and Life Sciences, Cornell University, Ithaca, United StatesDepartment of Food Science, College of Agriculture and Life Sciences, Cornell University, Ithaca, United StatesMammalian sperm rolling around their longitudinal axes is a long-observed component of motility, but its function in the fertilization process, and more specifically in sperm migration within the female reproductive tract, remains elusive. While investigating bovine sperm motion under simple shear flow and in a quiescent microfluidic reservoir and developing theoretical and computational models, we found that rolling regulates sperm navigation in response to the rheological properties of the sperm environment. In other words, rolling enables a sperm to swim progressively even if the flagellum beats asymmetrically. Therefore, a rolling sperm swims stably along the nearby walls (wall-dependent navigation) and efficiently upstream under an external fluid flow (rheotaxis). By contrast, an increase in ambient viscosity and viscoelasticity suppresses rolling, consequently, non-rolling sperm are less susceptible to nearby walls and external fluid flow and swim in two-dimensional diffusive circular paths (surface exploration). This surface exploration mode of swimming is caused by the intrinsic asymmetry in flagellar beating such that the curvature of a sperm’s circular path is proportional to the level of asymmetry. We found that the suppression of rolling is reversible and occurs in sperm with lower asymmetry in their beating pattern at higher ambient viscosity and viscoelasticity. Consequently, the rolling component of motility may function as a regulatory tool allowing sperm to navigate according to the rheological properties of the functional region within the female reproductive tract.https://elifesciences.org/articles/68693sperm rollingambient rheologysurface explorationnavigationb. taurusfemale reproductive tract |
| spellingShingle | Meisam Zaferani Farhad Javi Amir Mokhtare Peilong Li Alireza Abbaspourrad Rolling controls sperm navigation in response to the dynamic rheological properties of the environment eLife sperm rolling ambient rheology surface exploration navigation b. taurus female reproductive tract |
| title | Rolling controls sperm navigation in response to the dynamic rheological properties of the environment |
| title_full | Rolling controls sperm navigation in response to the dynamic rheological properties of the environment |
| title_fullStr | Rolling controls sperm navigation in response to the dynamic rheological properties of the environment |
| title_full_unstemmed | Rolling controls sperm navigation in response to the dynamic rheological properties of the environment |
| title_short | Rolling controls sperm navigation in response to the dynamic rheological properties of the environment |
| title_sort | rolling controls sperm navigation in response to the dynamic rheological properties of the environment |
| topic | sperm rolling ambient rheology surface exploration navigation b. taurus female reproductive tract |
| url | https://elifesciences.org/articles/68693 |
| work_keys_str_mv | AT meisamzaferani rollingcontrolsspermnavigationinresponsetothedynamicrheologicalpropertiesoftheenvironment AT farhadjavi rollingcontrolsspermnavigationinresponsetothedynamicrheologicalpropertiesoftheenvironment AT amirmokhtare rollingcontrolsspermnavigationinresponsetothedynamicrheologicalpropertiesoftheenvironment AT peilongli rollingcontrolsspermnavigationinresponsetothedynamicrheologicalpropertiesoftheenvironment AT alirezaabbaspourrad rollingcontrolsspermnavigationinresponsetothedynamicrheologicalpropertiesoftheenvironment |