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Research Article

Nanomechanical vibration profiling of oocytes

Yongpei Peng1,§, Junhui Zhang2,3,4,§, Weiwei Xue1, Wenjie Wu1, Yu Wang1, Kainan Mei1, Ye Chen1, Depeng Rao1, Tianhao Yan1, Jianye Wang1, Yunxia Cao2,3,4(), Shangquan Wu1 (), Qingchuan Zhang1 ()
CAS Key Laboratory of Mechanical Behavior and Design of Material, Department of Modern Mechanics, University of Science and Technology of China, Hefei 230027, China
Department of Obstetrics and Gynecology, The First Affiliated Hospital of Anhui Medical University, Hefei 230027, China
NHC Key Laboratory of Study on Abnormal Gametes and Reproductive Tract, Anhui Medical University, Hefei 230027, China
Key Laboratory of Population Health Across Life Cycle, Ministry of Education of the People’s Republic of China, Anhui Medical University, Hefei 230027, China

§ Yongpei Peng and Junhui Zhang contributed equally to this work.

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Herein, we studied oocytes from nanomotions and characterized the typical life activities of oocytes by nanomechanical vibrations. We combined mechanical research methods with biochemical methods to establish a link between biochemical changes and nanomotions in oocyte development. The exploring of the relationship between nanomechanical signals and the oocytes does not only contribute to assessing oocytes by nanomechanical activities, but also help to both clinical applications and mechanistic studies of development of oocytes.

Abstract

The beginning of a mammalian life commences with a fertilized oocyte. The study of oocytes is certainly one of the most intriguing scientific questions of our time. Herein, we studied oocytes from a mechanical perspective and characterized the typical life activities of oocytes by nanomechanical vibrations. During the development of oocytes from the germinal vesicle (GV) stage to the zygotes, the GV stage oocytes induced a significant nanomechanical vibration, compared with the oocytes in meiosis I (MI) and meiosis II (MII) stages and zygotes. We analyzed the characteristics of mechanical vibrations of oocytes, including the amplitude as well as the frequency. It showed that the amplitude and frequency of nanomechanical vibrations induced by oocytes were caused by the cytoskeleton (microfilaments) and the distribution of metabolic characteristics (mitochondria) within oocytes. This work provides a new perspective for clinical quality assessment and basic research of oocytes, and can open new doors for development of life science.

Keywords

oocytesnanomechanical sensorsnanomechaincal vibrationmetabolismmicrofilaments

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References

[1]

Keefe, D.; Kumar, M.; Kalmbach, K. Oocyte competency is the key to embryo potential. Fertil. Steril. 2015, 103, 317–322.

Crossref Google Scholar
[2]

Sun, H.; Gong, T. T.; Jiang, Y. T.; Zhang, S.; Zhao, Y. H.; Wu, Q. J. Global, regional, and national prevalence and disability-adjusted life-years for infertility in 195 countries and territories, 1990–2017: Results from a global burden of disease study, 2017. Aging (Albany NY) 2019, 11, 10952–10991.

Google Scholar
[3]
Rizk, B.; Agarwal, A.; Sabanegh, E. S. Jr. Male Infertility in Reproductive Medicine: Diagnosis and Management; CRC Press: New York, 2019.
[4]

Cohen, J.; Trounson, A.; Dawson, K.; Jones, H.; Hazekamp, J.; Nygren, K. G.; Hamberger, L. The early days of IVF outside the UK. Hum. Reprod. Update 2005, 11, 439–460.

Crossref Google Scholar
[5]

Niringiyumukiza, J. D.; Cai, H. C.; Xiang, W. P. Prostaglandin E2 involvement in mammalian female fertility: Ovulation, fertilization, embryo development and early implantation. Reprod. Biol. Endocrinol. 2018, 16, 43.

Crossref Google Scholar
[6]

Ouandaogo, Z. G.; Frydman, N.; Hesters, L.; Assou, S.; Haouzi, D.; Dechaud, H.; Frydman, R.; Hamamah, S. Differences in transcriptomic profiles of human cumulus cells isolated from oocytes at GV, MI and MII stages after in vivo and in vitro oocyte maturation. Hum. Reprod. 2012, 27, 2438–2447.

Crossref Google Scholar
[7]

Zaninovic, N.; Rosenwaks, Z. Artificial intelligence in human in vitro fertilization and embryology. Fertil. Steril. 2020, 114, 914–920.

Crossref Google Scholar
[8]

Labarta, E.; de Los Santos, M. J.; Escribá, M. J.; Pellicer, A.; Herraiz, S. Mitochondria as a tool for oocyte rejuvenation. Fertil. Steril. 2019, 111, 219–226.

Crossref Google Scholar
[9]

Liu, C. J.; Su, K. T.; Chen, L.; Zhao, Z. J.; Wang, X.; Yuan, C. F.; Liang, Y. Q.; Ji, H. L.; Li, C. J.; Zhou, X. Prediction of oocyte quality using mRNA transcripts screened by RNA sequencing of human granulosa cells. Reprod. BioMed. Online 2021, 43, 413–420.

Crossref Google Scholar
[10]

Dumollard, R.; Ward, Z.; Carroll, J.; Duchen, M. R. Regulation of redox metabolism in the mouse oocyte and embryo. Development 2007, 134, 455–465.

Crossref Google Scholar
[11]

Sutton-McDowall, M. L.; Gilchrist, R. B.; Thompson, J. G. The pivotal role of glucose metabolism in determining oocyte developmental competence. Reproduction 2010, 139, 685–695.

Crossref Google Scholar
[12]

Lee, S.; Kang, H. G.; Jeong, P. S.; Nanjidsuren, T.; Song, B. S.; Jin, Y. B.; Lee, S. R.; Kim, S. U.; Sim, B. W. Effect of oocyte quality assessed by brilliant cresyl blue (BCB) staining on cumulus cell expansion and sonic hedgehog signaling in porcine during in vitro maturation. Int. J. Mol. Sci. 2020, 21, 4423.

Crossref Google Scholar
[13]

Zhang, Z. G.; Mu, Y. Q.; Ding, D.; Zou, W. W.; Li, X. Y.; Chen, B. L.; Leung, P. C.; Chang, H. M.; Zhu, Q.; Wang, K. J. et al. Melatonin improves the effect of cryopreservation on human oocytes by suppressing oxidative stress and maintaining the permeability of the oolemma. J. Pineal Res. 2021, 70, e12707.

Google Scholar
[14]

Ling, L.; Feng, X. S.; Wei, T. Q.; Wang, Y.; Wang, Y. P.; Wang, Z. L.; Tang, D. Y.; Luo, Y. J.; Xiong, Z. G. Human amnion-derived mesenchymal stem cell (HAD-MSC) transplantation improves ovarian function in rats with premature ovarian insufficiency (POI) at least partly through a paracrine mechanism. Stem Cell Res. Ther. 2019, 10, 46.

Crossref Google Scholar
[15]

Longo, G.; Alonso-Sarduy, L.; Rio, L. M.; Bizzini, A.; Trampuz, A.; Notz, J.; Dietler, G.; Kasas, S. Rapid detection of bacterial resistance to antibiotics using AFM cantilevers as nanomechanical sensors. Nat. Nanotechnol. 2013, 8, 522–526.

Crossref Google Scholar
[16]

Kasas, S.; Ruggeri, F. S.; Benadiba, C.; Maillard, C.; Stupar, P.; Tournu, H.; Dietler, G.; Longo, G. Detecting nanoscale vibrations as signature of life. Proc. Natl. Acad. Sci. USA 2015, 112, 378–381.

Crossref Google Scholar
[17]

Nelson, S. L.; Proctor, D. T.; Ghasemloonia, A.; Lama, S.; Zareinia, K.; Ahn, Y.; Al-Saiedy, M. R.; Green, F. H.; Amrein, M. W.; Sutherland, G. R. Vibrational profiling of brain tumors and cells. Theranostics 2017, 7, 2417–2430.

Crossref Google Scholar
[18]

Wu, S. Q.; Liu, X. L.; Zhou, X. R.; Liang, X. M.; Gao, D. Y.; Liu, H.; Zhao, G.; Zhang, Q. C.; Wu, X. P. Quantification of cell viability and rapid screening anti-cancer drug utilizing nanomechanical fluctuation. Biosens. Bioelectron. 2016, 77, 164–173.

Crossref Google Scholar
[19]

Pelling, A. E.; Sehati, S.; Gralla, E. B.; Gimzewski, J. K. Time dependence of the frequency and amplitude of the local nanomechanical motion of yeast. Nanomedicine 2005, 1, 178–183.

Crossref Google Scholar
[20]
Pelling, A. E.; Sehati, S.; Gralla, E. B.; Valentine, J. S.; Gimzewski, J. K. Local nanomechanical motion of the cell wall of Saccharomyces cerevisiae. Science 2004, 305, 1147–1150.
[21]

Wu, S. Q.; Zhang, Z. G.; Zhou, X. R.; Liu, H.; Xue, C. G.; Zhao, G.; Cao, Y. X.; Zhang, Q. C.; Wu, X. P. Nanomechanical sensors for direct and rapid characterization of sperm motility based on nanoscale vibrations. Nanoscale 2017, 9, 18258–18267.

Crossref Google Scholar
[22]

Wu, S. Q.; Liu, H.; Cheng, T.; Zhou, X. R.; Wang, B. M.; Zhang, Q. C.; Wu, X. P. Highly sensitive nanomechanical assay for the stress transmission of carbon chain. Sens. Actuators B Chem. 2013, 186, 353–359.

Crossref Google Scholar
[23]

Wu, S. Q.; Nan, T. G.; Xue, C. G.; Cheng, T.; Liu, H.; Wang, B. M.; Zhang, Q. C.; Wu, X. P. Mechanism and enhancement of the surface stress caused by a small-molecule antigen and antibody binding. Biosens. Bioelectron. 2013, 48, 67–74.

Crossref Google Scholar
[24]

Stupar, P.; Opota, O.; Longo, G.; Prod'Hom, G.; Dietler, G.; Greub, G.; Kasas, S. Nanomechanical sensor applied to blood culture pellets: A fast approach to determine the antibiotic susceptibility against agents of bloodstream infections. Clin. Microbiol. Infect. 2017, 23, 400–405.

Crossref Google Scholar
[25]

Rong, W. Z.; Pelling, A. E.; Ryan, A.; Gimzewski, J. K.; Friedlander, S. K. Complementary TEM and AFM force spectroscopy to characterize the nanomechanical properties of nanoparticle chain aggregates. Nano Lett. 2004, 4, 2287–2292.

Crossref Google Scholar
[26]
Cross, S. E.; Kreth, J.; Zhu, L.; Qi, F. X.; Pelling, A. E.; Shi, W. Y.; Gimzewski, J. K. Atomic force microscopy study of the structure–function relationships of the biofilm-forming bacterium Streptococcus mutans. Nanotechnology 2006, 17, S1–S7.
[27]

Andolfi, L.; Masiero, E.; Giolo, E.; Martinelli, M.; Luppi, S.; Dal Zilio, S.; Delfino, I.; Bortul, R.; Zweyer, M.; Ricci, G. et al. Investigating the mechanical properties of zona pellucida of whole human oocytes by atomic force spectroscopy. Integr. Biol. (Camb) 2016, 8, 886–893.

Crossref Google Scholar
[28]

Pujol-Vila, F.; Escudero, P.; Güell-Grau, P.; Pascual-Izarra, C.; Villa, R.; Alvarez, M. Direct color observation of light-driven molecular conformation-induced stress. Small Methods 2022, 6, e2101283.

Crossref Google Scholar
[29]

Vandenberg, E. T.; Bertilsson, L.; Liedberg, B.; Uvdal, K.; Erlandsson, R.; Elwing, H.; Lundström, I. Structure of 3-aminopropyl triethoxy silane on silicon oxide. J. Colloid Interface Sci. 1991, 147, 103–118.

Crossref Google Scholar
[30]

Liu, Y. M.; Wang, J. Y.; Su, Y.; Xu, X. H.; Liu, H.; Mei, K. N.; Lan, S. H.; Zhang, S. B.; Wu, X. P.; Cao, Y. X. et al. Quantifying 3D cell-matrix interactions during mitosis and the effect of anticancer drugs on the interactions. Nano Res. 2021, 14, 4163–4172.

Crossref Google Scholar
[31]

Yan, T. H.; Rao, D. P.; Chen, Y.; Wang, Y.; Zhang, Q. C.; Wu, S. Q. Magnetic nanocomposite hydrogel with tunable stiffness for probing cellular responses to matrix stiffening. Acta Biomater. 2022, 138, 112–123.

Crossref Google Scholar
[32]

Sun, Y.; Wan, K. T.; Roberts, K. P.; Bischof, J. C.; Nelson, B. J. Mechanical property characterization of mouse zona pellucida. IEEE Trans. Nanobioscience 2003, 2, 279–286.

Crossref Google Scholar
[33]

Şen, U. Maturation of bovine oocytes under low culture temperature decreased glutathione peroxidase activity of both oocytes and blastocysts. Pol. J. Vet. Sci. 2021, 24, 93–99.

Google Scholar
[34]
Jin, X.; Wang, K. H.; Wang, L.; Liu, W. W.; Zhang, C.; Qiu, Y. X.; Liu, W.; Zhang, H. Y.; Zhang, D.; Yang, Z. X. et al. RAB7 activity is required for the regulation of mitophagy in oocyte meiosis and oocyte quality control during ovarian aging. Autophagy, in press, https://doi.org/10.1080/15548627.2021.1946739.
[35]

Mertens, J.; Cuervo, A.; Carrascosa, J. L. Nanomechanical detection of Escherichia coli infection by bacteriophage T7 using cantilever sensors. Nanoscale 2019, 11, 17689–17698.

Crossref Google Scholar
[36]

Gordon, J. L. Extracellular ATP: Effects, sources and fate. Biochem. J. 1986, 233, 309–319.

Crossref Google Scholar
[37]

Stupar, P.; Chomicki, W.; Maillard, C.; Mikeladze, D.; Kalauzi, A.; Radotić, K.; Dietler, G.; Kasas, S. Mitochondrial activity detected by cantilever based sensor. Mech. Sci. 2017, 8, 23–28.

Crossref Google Scholar
[38]

Duan, X.; Sun, S. C. Actin cytoskeleton dynamics in mammalian oocyte meiosis. Biol. Reprod. 2019, 100, 15–24.

Crossref Google Scholar
[39]

Dufrêne, Y. F.; Pelling, A. E. Force nanoscopy of cell mechanics and cell adhesion. Nanoscale 2013, 5, 4094–4104.

Crossref Google Scholar
Nano Research
Volume 16 Issue 2,
February 2023
Pages 2672-2681
DOI: 10.1007/s12274-022-4439-7
Cite this article:
Peng Y, Zhang J, Xue W, et al. Nanomechanical vibration profiling of oocytes. Nano Research, 2023, 16(2): 2672-2681. https://doi.org/10.1007/s12274-022-4439-7
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