Semen amyloids participate in spermatozoa selection and clearance

Nadia R. Roan; Nathallie Sandi-Monroy; Nargis Kohgadai; Shariq M. Usmani; Katherine G. Hamil; Jason Neidleman; Mauricio Montano; Ludger Ständker; Annika Röcker; Marielle Cavrois; Jared Rosen; Kara Marson; James F. Smith; Christopher D. Pilcher; Friedrich Gagsteiger; Olena Sakk; Michael O’Rand; Polina V. Lishko; Frank Kirchhoff; Jan Münch; Warner C. Greene

doi:10.7554/eLife.24888

Semen amyloids participate in spermatozoa selection and clearance

Nadia R. Roan, Nathallie Sandi-Monroy, Nargis Kohgadai, Shariq M. Usmani, Katherine G. Hamil, Jason Neidleman, Mauricio Montano, Ludger Ständker, Annika Röcker, Marielle Cavrois, Jared Rosen, Kara Marson, James F. Smith, Christopher D. Pilcher, Friedrich Gagsteiger, Olena Sakk, Michael O’Rand, Polina V. Lishko, Frank Kirchhoff, Jan MünchWarner C. Greene

Research output: Contribution to journal › Article › peer-review

Abstract

Unlike other human biological fluids, semen contains multiple types of amyloid fibrils in the absence of disease. These fibrils enhance HIV infection by promoting viral fusion to cellular targets, but their natural function remained unknown. The similarities shared between HIV fusion to host cell and sperm fusion to oocyte led us to examine whether these fibrils promote fertilization. Surprisingly, the fibrils inhibited fertilization by immobilizing sperm. Interestingly, however, this immobilization facilitated uptake and clearance of sperm by macrophages, which are known to infiltrate the female reproductive tract (FRT) following semen exposure. In the presence of semen fibrils, damaged and apoptotic sperm were more rapidly phagocytosed than healthy ones, suggesting that deposition of semen fibrils in the lower FRT facilitates clearance of poor-quality sperm. Our findings suggest that amyloid fibrils in semen may play a role in reproduction by participating in sperm selection and facilitating the rapid removal of sperm antigens.

Original language	English
Article number	e24888
Journal	eLife
Volume	6
DOIs	https://doi.org/10.7554/eLife.24888
State	Published - Jun 27 2017

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Roan, N. R., Sandi-Monroy, N., Kohgadai, N., Usmani, S. M., Hamil, K. G., Neidleman, J., Montano, M., Ständker, L., Röcker, A., Cavrois, M., Rosen, J., Marson, K., Smith, J. F., Pilcher, C. D., Gagsteiger, F., Sakk, O., O’Rand, M., Lishko, P. V., Kirchhoff, F., ... Greene, W. C. (2017). Semen amyloids participate in spermatozoa selection and clearance. eLife, 6, [e24888]. https://doi.org/10.7554/eLife.24888

@article{bf10ce1ccc114b9aa8de0ca747f481c8,

title = "Semen amyloids participate in spermatozoa selection and clearance",

abstract = "Unlike other human biological fluids, semen contains multiple types of amyloid fibrils in the absence of disease. These fibrils enhance HIV infection by promoting viral fusion to cellular targets, but their natural function remained unknown. The similarities shared between HIV fusion to host cell and sperm fusion to oocyte led us to examine whether these fibrils promote fertilization. Surprisingly, the fibrils inhibited fertilization by immobilizing sperm. Interestingly, however, this immobilization facilitated uptake and clearance of sperm by macrophages, which are known to infiltrate the female reproductive tract (FRT) following semen exposure. In the presence of semen fibrils, damaged and apoptotic sperm were more rapidly phagocytosed than healthy ones, suggesting that deposition of semen fibrils in the lower FRT facilitates clearance of poor-quality sperm. Our findings suggest that amyloid fibrils in semen may play a role in reproduction by participating in sperm selection and facilitating the rapid removal of sperm antigens.",

author = "Roan, {Nadia R.} and Nathallie Sandi-Monroy and Nargis Kohgadai and Usmani, {Shariq M.} and Hamil, {Katherine G.} and Jason Neidleman and Mauricio Montano and Ludger St{\"a}ndker and Annika R{\"o}cker and Marielle Cavrois and Jared Rosen and Kara Marson and Smith, {James F.} and Pilcher, {Christopher D.} and Friedrich Gagsteiger and Olena Sakk and Michael O{\textquoteright}Rand and Lishko, {Polina V.} and Frank Kirchhoff and Jan M{\"u}nch and Greene, {Warner C.}",

note = "Funding Information: We thank T Wirth at the Transgenic Mice Core Facility for helping with IVF assays; J Wong at the Gladstone Electron Microscopy Core Facility for generating the electron micrographs; N Mannowetz for assistance in sperm motility recording; AL Lucido for editorial assistance; T Roberts and C Good-fellow for assistance in preparing the figures; and S Cammack and R Givens for administrative assistance. This work was supported by the National Institutes of Health (K99AI104262, R00AI104262, R21AI116252, and R01AI127219 to NRR; pilot grant to NRR as part of parent grant P50HD055764 to Linda C Giudice; R01HD074511 to CP; and P01 AI083050 to WCG), the Deutsche Forschungsgemeinschaft (DFG) (MU 3115–2 to JM), and the European Research Council (ERC-AG-LS6 to FK). As part of a parent grant to Paul A Volberding, the National Institutes of Health also funded the grant P30AI027763 which provided money for instruments used in the paper. The Amnis Imagestream used in this study was funded by the Department of Defense (W81XWH-11-1-0562)., National Institutes of HealthP01 AI083050 Warner C Greene, U.S. Department of Defense W81XWH-11-1-0562 The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication. Publisher Copyright: {\textcopyright} Roan et al.",

year = "2017",

month = jun,

day = "27",

doi = "10.7554/eLife.24888",

language = "English",

volume = "6",

journal = "eLife",

issn = "2050-084X",

}

Roan, NR, Sandi-Monroy, N, Kohgadai, N, Usmani, SM, Hamil, KG, Neidleman, J, Montano, M, Ständker, L, Röcker, A, Cavrois, M, Rosen, J, Marson, K, Smith, JF, Pilcher, CD, Gagsteiger, F, Sakk, O, O’Rand, M, Lishko, PV, Kirchhoff, F, Münch, J & Greene, WC 2017, 'Semen amyloids participate in spermatozoa selection and clearance', eLife, vol. 6, e24888. https://doi.org/10.7554/eLife.24888

TY - JOUR

T1 - Semen amyloids participate in spermatozoa selection and clearance

AU - Roan, Nadia R.

AU - Sandi-Monroy, Nathallie

AU - Kohgadai, Nargis

AU - Usmani, Shariq M.

AU - Hamil, Katherine G.

AU - Neidleman, Jason

AU - Montano, Mauricio

AU - Ständker, Ludger

AU - Röcker, Annika

AU - Cavrois, Marielle

AU - Rosen, Jared

AU - Marson, Kara

AU - Smith, James F.

AU - Pilcher, Christopher D.

AU - Gagsteiger, Friedrich

AU - Sakk, Olena

AU - O’Rand, Michael

AU - Lishko, Polina V.

AU - Kirchhoff, Frank

AU - Münch, Jan

AU - Greene, Warner C.

N1 - Funding Information: We thank T Wirth at the Transgenic Mice Core Facility for helping with IVF assays; J Wong at the Gladstone Electron Microscopy Core Facility for generating the electron micrographs; N Mannowetz for assistance in sperm motility recording; AL Lucido for editorial assistance; T Roberts and C Good-fellow for assistance in preparing the figures; and S Cammack and R Givens for administrative assistance. This work was supported by the National Institutes of Health (K99AI104262, R00AI104262, R21AI116252, and R01AI127219 to NRR; pilot grant to NRR as part of parent grant P50HD055764 to Linda C Giudice; R01HD074511 to CP; and P01 AI083050 to WCG), the Deutsche Forschungsgemeinschaft (DFG) (MU 3115–2 to JM), and the European Research Council (ERC-AG-LS6 to FK). As part of a parent grant to Paul A Volberding, the National Institutes of Health also funded the grant P30AI027763 which provided money for instruments used in the paper. The Amnis Imagestream used in this study was funded by the Department of Defense (W81XWH-11-1-0562)., National Institutes of HealthP01 AI083050 Warner C Greene, U.S. Department of Defense W81XWH-11-1-0562 The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication. Publisher Copyright: © Roan et al.

PY - 2017/6/27

Y1 - 2017/6/27

N2 - Unlike other human biological fluids, semen contains multiple types of amyloid fibrils in the absence of disease. These fibrils enhance HIV infection by promoting viral fusion to cellular targets, but their natural function remained unknown. The similarities shared between HIV fusion to host cell and sperm fusion to oocyte led us to examine whether these fibrils promote fertilization. Surprisingly, the fibrils inhibited fertilization by immobilizing sperm. Interestingly, however, this immobilization facilitated uptake and clearance of sperm by macrophages, which are known to infiltrate the female reproductive tract (FRT) following semen exposure. In the presence of semen fibrils, damaged and apoptotic sperm were more rapidly phagocytosed than healthy ones, suggesting that deposition of semen fibrils in the lower FRT facilitates clearance of poor-quality sperm. Our findings suggest that amyloid fibrils in semen may play a role in reproduction by participating in sperm selection and facilitating the rapid removal of sperm antigens.

AB - Unlike other human biological fluids, semen contains multiple types of amyloid fibrils in the absence of disease. These fibrils enhance HIV infection by promoting viral fusion to cellular targets, but their natural function remained unknown. The similarities shared between HIV fusion to host cell and sperm fusion to oocyte led us to examine whether these fibrils promote fertilization. Surprisingly, the fibrils inhibited fertilization by immobilizing sperm. Interestingly, however, this immobilization facilitated uptake and clearance of sperm by macrophages, which are known to infiltrate the female reproductive tract (FRT) following semen exposure. In the presence of semen fibrils, damaged and apoptotic sperm were more rapidly phagocytosed than healthy ones, suggesting that deposition of semen fibrils in the lower FRT facilitates clearance of poor-quality sperm. Our findings suggest that amyloid fibrils in semen may play a role in reproduction by participating in sperm selection and facilitating the rapid removal of sperm antigens.

UR - http://www.scopus.com/inward/record.url?scp=85022319168&partnerID=8YFLogxK

U2 - 10.7554/eLife.24888

DO - 10.7554/eLife.24888

M3 - Article

C2 - 28653619

AN - SCOPUS:85022319168

SN - 2050-084X

VL - 6

JO - eLife

JF - eLife

M1 - e24888

ER -

Semen amyloids participate in spermatozoa selection and clearance

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