Gold Nanorod Induced Warming of Embryos from the Cryogenic State Enhances Viability

Kanav Khosla; Yiru Wang; Mary Hagedorn; Zhenpeng Qin; John C Bischof

doi:10.1021/acsnano.7b02216

Gold Nanorod Induced Warming of Embryos from the Cryogenic State Enhances Viability

Kanav Khosla, Yiru Wang, Mary Hagedorn, Zhenpeng Qin, John C Bischof

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

93 Scopus citations

Abstract

Zebrafish embryos can attain a stable cryogenic state by microinjection of cryoprotectants followed by rapid cooling, but the massive size of the embryo has consistently led to failure during the convective warming process. Here we address this zebrafish cryopreservation problem by using gold nanorods (GNRs) to assist in the warming process. Specifically, we microinjected the cryoprotectant propylene glycol into zebrafish embryos along with GNRs, and the samples were cooled at a rate of 90 000 °C/min in liquid nitrogen. We demonstrated the ability to unfreeze the zebrafish rapidly (1.4 × 10⁷ °C/min) by irradiating the sample with a 1064 nm laser pulse for 1 ms due to the excitation of GNRs. This rapid warming process led to the outrunning of ice formation, which can damage the embryos. The results from 14 trials (n = 223) demonstrated viable embryos with consistent structure at 1 h (31%) and continuing development at 3 h (17%) and movement at 24 h (10%) postwarming. This compares starkly with 0% viability, structure, or movement at all time points in convectively warmed controls (n = 50, p < 0.001, ANOVA). Our nanoparticle-based warming process could be applied to the storage of fish, and with proper modification, can potentially be used for other vertebrate embryos.

Original language	English (US)
Pages (from-to)	7869-7878
Number of pages	10
Journal	ACS nano
Volume	11
Issue number	8
DOIs	https://doi.org/10.1021/acsnano.7b02216
State	Published - Aug 22 2017

Bibliographical note

Funding Information:
J.B. received support from the Kuhrmeyer Chair and the Institute for Engineering in Medicine at University of Minnesota. M.H. received support from the Anela Kolohe Foundation, the Cedarhill Foundation, the Skippy Frank Translational Medicine Fund, the Roddenberry Foundation, the Paul M. Angell Family Foundation, the Hawaii Institute of Marine Biology, and the Smithsonian Institution. The manuscript was approved for publication by the Hawaii Institute of Marine Biology as contribution no. 1672. We thank the Zebrafish Core and College of Science and Engineering research shop at the University of Minnesota for access to zebrafish and the 1064 nm laser, respectively. We also thank Mr. Marc Tye for microinjection training, Dr. Zhe Gao for helping with transmission electron microscopy, and University Imaging Centers at the University of Minnesota for imaging.

Publisher Copyright:
© 2017 American Chemical Society.

Keywords

cryopreservation
gold nanoparticles
laser warming
zebrafish

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10.1021/acsnano.7b02216

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@article{17b2e64c7968435f9df97fe947269897,

title = "Gold Nanorod Induced Warming of Embryos from the Cryogenic State Enhances Viability",

abstract = "Zebrafish embryos can attain a stable cryogenic state by microinjection of cryoprotectants followed by rapid cooling, but the massive size of the embryo has consistently led to failure during the convective warming process. Here we address this zebrafish cryopreservation problem by using gold nanorods (GNRs) to assist in the warming process. Specifically, we microinjected the cryoprotectant propylene glycol into zebrafish embryos along with GNRs, and the samples were cooled at a rate of 90 000 °C/min in liquid nitrogen. We demonstrated the ability to unfreeze the zebrafish rapidly (1.4 × 107 °C/min) by irradiating the sample with a 1064 nm laser pulse for 1 ms due to the excitation of GNRs. This rapid warming process led to the outrunning of ice formation, which can damage the embryos. The results from 14 trials (n = 223) demonstrated viable embryos with consistent structure at 1 h (31%) and continuing development at 3 h (17%) and movement at 24 h (10%) postwarming. This compares starkly with 0% viability, structure, or movement at all time points in convectively warmed controls (n = 50, p < 0.001, ANOVA). Our nanoparticle-based warming process could be applied to the storage of fish, and with proper modification, can potentially be used for other vertebrate embryos.",

keywords = "cryopreservation, gold nanoparticles, laser warming, zebrafish",

author = "Kanav Khosla and Yiru Wang and Mary Hagedorn and Zhenpeng Qin and Bischof, {John C}",

note = "Funding Information: J.B. received support from the Kuhrmeyer Chair and the Institute for Engineering in Medicine at University of Minnesota. M.H. received support from the Anela Kolohe Foundation, the Cedarhill Foundation, the Skippy Frank Translational Medicine Fund, the Roddenberry Foundation, the Paul M. Angell Family Foundation, the Hawaii Institute of Marine Biology, and the Smithsonian Institution. The manuscript was approved for publication by the Hawaii Institute of Marine Biology as contribution no. 1672. We thank the Zebrafish Core and College of Science and Engineering research shop at the University of Minnesota for access to zebrafish and the 1064 nm laser, respectively. We also thank Mr. Marc Tye for microinjection training, Dr. Zhe Gao for helping with transmission electron microscopy, and University Imaging Centers at the University of Minnesota for imaging. Publisher Copyright: {\textcopyright} 2017 American Chemical Society.",

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AU - Bischof, John C

N1 - Funding Information: J.B. received support from the Kuhrmeyer Chair and the Institute for Engineering in Medicine at University of Minnesota. M.H. received support from the Anela Kolohe Foundation, the Cedarhill Foundation, the Skippy Frank Translational Medicine Fund, the Roddenberry Foundation, the Paul M. Angell Family Foundation, the Hawaii Institute of Marine Biology, and the Smithsonian Institution. The manuscript was approved for publication by the Hawaii Institute of Marine Biology as contribution no. 1672. We thank the Zebrafish Core and College of Science and Engineering research shop at the University of Minnesota for access to zebrafish and the 1064 nm laser, respectively. We also thank Mr. Marc Tye for microinjection training, Dr. Zhe Gao for helping with transmission electron microscopy, and University Imaging Centers at the University of Minnesota for imaging. Publisher Copyright: © 2017 American Chemical Society.

PY - 2017/8/22

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N2 - Zebrafish embryos can attain a stable cryogenic state by microinjection of cryoprotectants followed by rapid cooling, but the massive size of the embryo has consistently led to failure during the convective warming process. Here we address this zebrafish cryopreservation problem by using gold nanorods (GNRs) to assist in the warming process. Specifically, we microinjected the cryoprotectant propylene glycol into zebrafish embryos along with GNRs, and the samples were cooled at a rate of 90 000 °C/min in liquid nitrogen. We demonstrated the ability to unfreeze the zebrafish rapidly (1.4 × 107 °C/min) by irradiating the sample with a 1064 nm laser pulse for 1 ms due to the excitation of GNRs. This rapid warming process led to the outrunning of ice formation, which can damage the embryos. The results from 14 trials (n = 223) demonstrated viable embryos with consistent structure at 1 h (31%) and continuing development at 3 h (17%) and movement at 24 h (10%) postwarming. This compares starkly with 0% viability, structure, or movement at all time points in convectively warmed controls (n = 50, p < 0.001, ANOVA). Our nanoparticle-based warming process could be applied to the storage of fish, and with proper modification, can potentially be used for other vertebrate embryos.

AB - Zebrafish embryos can attain a stable cryogenic state by microinjection of cryoprotectants followed by rapid cooling, but the massive size of the embryo has consistently led to failure during the convective warming process. Here we address this zebrafish cryopreservation problem by using gold nanorods (GNRs) to assist in the warming process. Specifically, we microinjected the cryoprotectant propylene glycol into zebrafish embryos along with GNRs, and the samples were cooled at a rate of 90 000 °C/min in liquid nitrogen. We demonstrated the ability to unfreeze the zebrafish rapidly (1.4 × 107 °C/min) by irradiating the sample with a 1064 nm laser pulse for 1 ms due to the excitation of GNRs. This rapid warming process led to the outrunning of ice formation, which can damage the embryos. The results from 14 trials (n = 223) demonstrated viable embryos with consistent structure at 1 h (31%) and continuing development at 3 h (17%) and movement at 24 h (10%) postwarming. This compares starkly with 0% viability, structure, or movement at all time points in convectively warmed controls (n = 50, p < 0.001, ANOVA). Our nanoparticle-based warming process could be applied to the storage of fish, and with proper modification, can potentially be used for other vertebrate embryos.

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KW - gold nanoparticles

KW - laser warming

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Gold Nanorod Induced Warming of Embryos from the Cryogenic State Enhances Viability

Abstract

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Gold Nanorod Induced Warming of Embryos from the Cryogenic State Enhances Viability

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Bibliographical note

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Nikon C2 Upright Spectral Confocal and Widefield Imaging System

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