Source: UNIV OF MARYLAND submitted to
GENOME EDITING TO CREATE GERM CELL DEFICIENT LIVESTOCK
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
TERMINATED
Funding Source
Reporting Frequency
Annual
Accession No.
1015153
Grant No.
2018-67015-27575
Project No.
MD-ANSC-05436
Proposal No.
2017-05436
Multistate No.
(N/A)
Program Code
A1211
Project Start Date
Mar 1, 2018
Project End Date
Feb 28, 2021
Grant Year
2018
Project Director
Keefer, C.
Recipient Organization
UNIV OF MARYLAND
(N/A)
COLLEGE PARK,MD 20742
Performing Department
Animal & Avian Sciences
Non Technical Summary
Genetic gain in food animal production is critical for enhancing growth efficiency, animal health, and product quality. In pig production, genetic gain is achieved via selective breeding with desirable sires. At present, artificial insemination (AI) is a widely used option for exploiting this principle. However, the number of sperm that can be collected from an individual boar is a major limiting factor for widespread dissemination in the commercial pig production. Also, AI methodology limits the gains to the reproductive lifespan of a male, thereby resulting in the loss of superior genetic merit, and necessitating a new round of recruitment and identification of desirable sires. Thus, development of novel approaches for expanding the output and preservation of germline from desirable sires is of significant need. An overarching goal of this project is to generate lines of boar that completely lack endogenous spermatogonial stem cell (SSC), and use them as surrogates for exogenous SSC transplantation and spermatogenesis. To achieve this objective, we utilized the CRISPR/Cas9 system to edit the NANOS2 gene in pig embryos to generate offspring with mono-allelic and bi-allelic mutations. We found that NANOS2 knockout males lack germline but other aspects of testicular development are normal. In this study, the NANOS2-null animals will be propagated and exogenous SSC transplanted for initiation of spermatogenesis. This study will for the first time generate SSC-deficient animals by genome editing and test the feasibility of SSC transplantation in a large animal species. Arguably this project will have wide ranging applications in germline preservation technologies.
Animal Health Component
0%
Research Effort Categories
Basic
90%
Applied
10%
Developmental
(N/A)
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
30335991050100%
Knowledge Area
303 - Genetic Improvement of Animals;

Subject Of Investigation
3599 - Swine, general/other;

Field Of Science
1050 - Developmental biology;
Goals / Objectives
There are two major goals in this proposal: Aim-1. Generate a line of male pigs with testes that lack a germline but retain normal functions of somatic support cells. To achieve this, we have utilized recent advances in gene editing technologies (i.e., CRISPR/Cas9) to generate lines of pigs with an inactivate NANOS2 gene that is required for the survival of SSCs(1). We provide evidence that the biological role of NANOS2 is conserved in pigs, and that loss-of-function will result in elimination of the SSC population during fetal development. Importantly, this loss does not impact the functional capacity of somatic support cell populations.Aim-2. Determine the effectiveness of germline ablated pigs to serve as recipients for SSC transplantation. To achieve this, NANOS2 null male pigs will be transplanted with a cell suspension of undifferentiated spermatogonia isolated both from donor pig testes directly, and following a period of in vitro maintenance and expansion. Donor-derived spermatogenesis will then be assessed several months later. Also, the capacity of NANOS2 null recipient pigs to derive offspring with the donor haplotype via natural mating or AI will be evaluated. We anticipate that vast areas of donor-derived spermatogenesis will occur in recipient testes. Furthermore, the amount of sperm produced will be sufficient to generate offspring of the donor genotype similar to what has been achieved with SSC transplantation in germline ablated rodent models.
Project Methods
We will utilizethe site specific nucleases, specifically the CRISPR/Cas9 system to site specifically introduce double stranded breaks and ablate the NANOS2 gene in pig embryos to generate male offspring that s lack germline but other aspects of testicular development are normal. The NANOS2-null animals will be propagated and exogenous germ cells from donor boars will betransplanted for initiation of spermatogenesis. This study will, for the first time, generate germ cell-deficient animals by genome editing and test the feasibility of germ cell transplantation in a large animal species.

Progress 03/01/18 to 02/28/21

Outputs
Target Audience:The target audience are: 1) Industry. The project was supported partially with funds from Genus plc. The proposed project has great relevance for the livestock genetics companies for accelerating genetic selection and independent introduction of genetics into livestock multiplication systems. Additionally, the project employes next generation breeding technologies such as CRISPR/Cas genome editing to specifically target the genes involved in spermatogonial stem cell maintenance. 2) Academia: The foundation of the project is genome editing and stem cell culture/maintenance. The project has relevance to broader audience in academia who are practitioners of the genome editing and genetic engineering practices. Changes/Problems:We have banked the fetal fibroblasts from NANOS2 knockout boars. These could be used for generating additional animals via SCNT and for refining SSC transfer for colonization of the gonads and induction of spermatogenesis What opportunities for training and professional development has the project provided?Graduate students, undergraduates, and postdoctoral fellows were involved with the research. How have the results been disseminated to communities of interest?Presentations at scientific conferences including the Society for the Study of Reproduction, American Society of Andrology, Transgenic Technology Conference, Large Animal Genetic Engineering Conference, and International Embryo Transfer Society What do you plan to do during the next reporting period to accomplish the goals?Refine the testicular injection technique by conducting additional SSC transplantation procedures in NANOS2 knockout boars. Several new knockout boars have been produced and will be subjected to additional transplantations to determine whether a greater level of donor stem cell engraftment can occur.

Impacts
What was accomplished under these goals? We transplanted homologous SSCs isolated from wild-type donor testes into the testes of 5 NANOS2 knockout boars. At ~90 days post-transplantation, presumptive round spermatids were detected in the ejaculates of two transplanted boars and motile spermatozoa were observed at ~100 days post-transplantation for one boar. The sperm were confirmed by genotyping analysis to be donor-derived and production persisted in the NANOS2 knockout recipient's testes for >2 yrs. In contrast, sperm production was never observed over a 2 year period in NANOS2 knockout boars that did not receive donor SSC transplantation. These findings demonstrate that the testicular soma is intact in males that lack germline due to NANOS2 deficiency and donor SSC engraftment can occur.

Publications

  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Donor-derived spermatogenesis following stem cell transplantation in sterile NANOS2 knockout males. Ciccarelli M, Giassetti MI, Miao D, Oatley MJ, Robbins C, Lopez-Biladeau B, Waqas MS, Tibary A, Whitelaw B, Lillico S, Park CH, Park KE, Telugu B, Fan Z, Liu Y, Regouski M, Polejaeva IA, Oatley JM. Proc Natl Acad Sci U S A. 2020 Sep 29;117(39):24195-24204. doi: 10.1073/pnas.2010102117. Epub 2020 Sep 14.
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Genome editing and genetic engineering in livestock for advancing agricultural and biomedical applications. Telugu BP, Park KE, Park CH. Mamm Genome. 2017 Aug;28(7-8):338-347. doi: 10.1007/s00335-017-9709-4. Epub 2018 Jul 15. PMID: 28712062 Review.