Characteristics of induced mutations in offspring derived from irradiated mouse spermatogonia and mature oocytes

Satoh, Yasunari; Asakawa, Jun-ichi; Nishimura, Mayumi; Kuo, Tony; Shinkai, Norio; Cullings, Harry M.; Minakuchi, Yohei; Sese, Jun; Toyoda, Atsushi; Shimada, Yoshiya; Nakamura, Nori; Uchimura, Arikuni

doi:10.1038/s41598-019-56881-2

Title: Characteristics of induced mutations in offspring derived from irradiated mouse spermatogonia and mature oocytes

Journal Article · Wed Jan 08 00:00:00 UTC 2020 · Scientific Reports

DOI: https://doi.org/10.1038/s41598-019-56881-2 · OSTI ID:1624520

^[1]; Asakawa, Jun-ichi ^[2]; Nishimura, Mayumi ^[3]; Kuo, Tony ^[4]; Shinkai, Norio ^[5]; Cullings, Harry M. ^[6]; Minakuchi, Yohei ^[7]; Sese, Jun ^[8];

^[9]; Shimada, Yoshiya ^[10]; Nakamura, Nori ^[2]; Uchimura, Arikuni ^[2]

Radiation Effects Research Foundation, Dept. of Molecular Biosciences, Hiroshima (Japan); DOE/OSTI
Radiation Effects Research Foundation, Dept. of Molecular Biosciences, Hiroshima (Japan)
Department of Radiation Effects Research, National Institute of Radiological Sciences (NIRS), National Institutes for Quantum and Radiological Science and Technology (QST), Chiba (Japan)
Artificial Intelligence Research Center, AIST, 2-3-26 Aomi, Koto-ku, Tokyo (Japan); Real World Big-Data Computation Open Innovation Laboratory, AIST-Tokyo Tech, 2-12-1 Okayama, Meguro-ku, Tokyo (Japan)
Artificial Intelligence Research Center, AIST, 2-3-26 Aomi, Koto-ku, Tokyo (Japan)
Radiation Effects Research Foundation, 5-2 Hijiyama Park, Minami-ku, Hiroshima (Japan). Dept. of Statistics
National Institute of Genetics, Mishima (Japan). Comparative Genomics Laboratory
Artificial Intelligence Research Center, AIST, 2-3-26 Aomi, Koto-ku, Tokyo (Japan); Real World Big-Data Computation Open Innovation Laboratory, AIST-Tokyo Tech, 2-12-1 Okayama, Meguro-ku, Tokyo (Japan); Humanome Lab, Inc., L-HUB 3F, 1-4, Shumomiyabi-cho, Sinjuku-ku, Tokyo (Japan)
National Institute of Genetics, Mishima (Japan). Comparative Genomics Laboratory
Tokyo Metropolitan University, Tokyo (Japan). Dept. of Radiological Sciences, Graduate School of Human Health Sciences; Executive Director, QST, Chiba (Japan)

The exposure of germ cells to radiation introduces mutations in the genomes of offspring, and a previous whole-genome sequencing study indicated that the irradiation of mouse sperm induces insertions/deletions (indels) and multisite mutations (clustered single nucleotide variants and indels). However, the current knowledge on the mutation spectra is limited, and the effects of radiation exposure on germ cells at stages other than the sperm stage remain unknown. Here, we performed whole-genome sequencing experiments to investigate the exposure of spermatogonia and mature oocytes. We compared de novo mutations in a total of 24 F1 mice conceived before and after the irradiation of their parents. The results indicated that radiation exposure, 4 Gy of gamma rays, induced 9.6 indels and 2.5 multisite mutations in spermatogonia and 4.7 indels and 3.1 multisite mutations in mature oocytes in the autosomal regions of each F1 individual. Notably, we found two types of deletions, namely, small deletions (mainly 1~12 nucleotides) in non-repeat sequences, many of which showed microhomology at the breakpoint junction, and single-nucleotide deletions in mononucleotide repeat sequences. The results suggest that these deletions and multisite mutations could be a typical signature of mutations induced by parental irradiation in mammals.

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Research Organization:: National Academy of Sciences, Washington, DC (United States)

Sponsoring Organization:: USDOE Office of Environment, Health, Safety and Security (AU)

Grant/Contract Number:: HS0000031

OSTI ID:: 1624520

Journal Information:: Scientific Reports, Journal Name: Scientific Reports Journal Issue: 1 Vol. 10; ISSN 2045-2322

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

References (73)

Heavy-ion-induced mutations in thegpt delta transgenic mouse: Comparison of mutation spectra induced by heavy-ion, X-ray, and ?-ray radiation Masumura, Ken-ichi; Kuniya, Kensuke; Kurobe, Toshihiro Environmental and Molecular Mutagenesis, Vol. 40, Issue 3 https://doi.org/10.1002/em.10108	journal	January 2002
Repair capacity of fertilized mouse eggs for X-ray damage induced in sperm and mature oocytes Matsuda, Yoichi; Tobari, Izuo Mutation Research/Fundamental and Molecular Mechanisms of Mutagenesis, Vol. 210, Issue 1 https://doi.org/10.1016/0027-5107(89)90042-0	journal	January 1989
Comparison of the duration of spermatogenesis between male rodents and humans Adler, Ilse-Dore Mutation Research/Fundamental and Molecular Mechanisms of Mutagenesis, Vol. 352, Issue 1-2 https://doi.org/10.1016/0027-5107(95)00223-5	journal	June 1996
Chromatin dynamics during spermiogenesis Rathke, Christina; Baarends, Willy M.; Awe, Stephan Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms, Vol. 1839, Issue 3 https://doi.org/10.1016/j.bbagrm.2013.08.004	journal	March 2014
Genomic Patterns of De Novo Mutation in Simplex Autism Turner, Tychele N.; Coe, Bradley P.; Dickel, Diane E. Cell, Vol. 171, Issue 3 https://doi.org/10.1016/j.cell.2017.08.047	journal	October 2017
Radiation-induced clustered DNA lesions: Repair and mutagenesis Sage, Evelyne; Shikazono, Naoya Free Radical Biology and Medicine, Vol. 107 https://doi.org/10.1016/j.freeradbiomed.2016.12.008	journal	June 2017
Delayed repair of radiation induced clustered DNA damage: Friend or foe? Eccles, Laura J.; O’Neill, Peter; Lomax, Martine E. Mutation Research/Fundamental and Molecular Mechanisms of Mutagenesis, Vol. 711, Issue 1-2 https://doi.org/10.1016/j.mrfmmm.2010.11.003	journal	June 2011
Evidence relevant to untargeted and transgenerational effects in the offspring of irradiated parents Little, Mark P.; Goodhead, Dudley T.; Bridges, Bryn A. Mutation Research/Reviews in Mutation Research, Vol. 753, Issue 1 https://doi.org/10.1016/j.mrrev.2013.04.001	journal	July 2013
Genome-based, mechanism-driven computational modeling of risks of ionizing radiation: The next frontier in genetic risk estimation? Sankaranarayanan, K.; Nikjoo, H. Mutation Research/Reviews in Mutation Research, Vol. 764 https://doi.org/10.1016/j.mrrev.2014.12.003	journal	April 2015
Should we worry about inherited radiation risks? Brenner, David J. The Lancet Oncology, Vol. 16, Issue 13 https://doi.org/10.1016/s1470-2045(15)00270-3	journal	October 2015
Human minisatellite mutation rate after the Chernobyl accident Dubrova, Yuri E.; Nesterov, Valeri N.; Krouchinsky, Nicolay G. Nature, Vol. 380, Issue 6576 https://doi.org/10.1038/380683a0	journal	April 1996
p63 protects the female germ line during meiotic arrest Suh, Eun-Kyung; Yang, Annie; Kettenbach, Arminja Nature, Vol. 444, Issue 7119 https://doi.org/10.1038/nature05337	journal	November 2006
Rate of de novo mutations and the importance of father’s age to disease risk Kong, Augustine; Frigge, Michael L.; Masson, Gisli Nature, Vol. 488, Issue 7412 https://doi.org/10.1038/nature11396	journal	August 2012
High-throughput discovery of novel developmental phenotypes Dickinson, Mary E.; Flenniken, Ann M.; Ji, Xiao Nature, Vol. 537, Issue 7621 https://doi.org/10.1038/nature19356	journal	September 2016
Parental influence on human germline de novo mutations in 1,548 trios from Iceland Jónsson, Hákon; Sulem, Patrick; Kehr, Birte Nature, Vol. 549, Issue 7673 https://doi.org/10.1038/nature24018	journal	September 2017
Mutational signatures of ionizing radiation in second malignancies Behjati, Sam; Gundem, Gunes; Wedge, David C. Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms12605	journal	September 2016
Targeted introduction of heritable point mutations into the plant mitochondrial genome Forner, Joachim; Kleinschmidt, Dennis; Meyer, Etienne H. Nature Plants, Vol. 8, Issue 3 https://doi.org/10.1038/s41477-022-01108-y	journal	March 2022
Genome-wide CRISPR screen identifies PRC2 and KMT2D-COMPASS as regulators of distinct EMT trajectories that contribute differentially to metastasis Zhang, Yun; Donaher, Joana Liu; Das, Sunny Nature Cell Biology, Vol. 24, Issue 4 https://doi.org/10.1038/s41556-022-00877-0	journal	April 2022
Germline de novo mutation clusters arise during oocyte aging in genomic regions with high double-strand-break incidence Goldmann, Jakob M.; Seplyarskiy, Vladimir B.; Wong, Wendy S. W. Nature Genetics, Vol. 50, Issue 4 https://doi.org/10.1038/s41588-018-0071-6	journal	March 2018
Multisite de novo mutations in human offspring after paternal exposure to ionizing radiation Holtgrewe, Manuel; Knaus, Alexej; Hildebrand, Gabriele Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-33066-x	journal	October 2018
8-oxoguanine causes spontaneous de novo germline mutations in mice Ohno, Mizuki; Sakumi, Kunihiko; Fukumura, Ryutaro Scientific Reports, Vol. 4, Issue 1 https://doi.org/10.1038/srep04689	journal	April 2014
Similar Mutation Rates but Highly Diverse Mutation Spectra in Ascomycete and Basidiomycete Yeasts Long, Hongan; Behringer, Megan G.; Williams, Emily Genome Biology and Evolution, Vol. 8, Issue 12 https://doi.org/10.1093/gbe/evw286	journal	December 2016
Error-prone polymerase activity causes multinucleotide mutations in humans Harris, Kelley; Nielsen, Rasmus Genome Research, Vol. 24, Issue 9 https://doi.org/10.1101/gr.170696.113	journal	July 2014
Germline mutation rates and the long-term phenotypic effects of mutation accumulation in wild-type laboratory mice and mutator mice Uchimura, Arikuni; Higuchi, Mayumi; Minakuchi, Yohei Genome Research, Vol. 25, Issue 8 https://doi.org/10.1101/gr.186148.114	journal	June 2015
Artificial Transmutation of the gene Muller, H. J. Science, Vol. 66, Issue 1699 https://doi.org/10.1126/science.66.1699.84	journal	July 1927
Radiation Effects on Human Heredity Nakamura, Nori; Suyama, Akihiko; Noda, Asao Annual Review of Genetics, Vol. 47, Issue 1 https://doi.org/10.1146/annurev-genet-111212-133501	journal	November 2013
Multi-nucleotide de novo Mutations in Humans Besenbacher, Søren; Sulem, Patrick; Helgason, Agnar PLOS Genetics, Vol. 12, Issue 11 https://doi.org/10.1371/journal.pgen.1006315	journal	November 2016
Genome-Wide Deletion Screening with the Array CGH Method in Mouse Offspring Derived from Irradiated Spermatogonia Indicates that Mutagenic Responses are Highly Variable among Genes Asakawa, Jun-ichi; Kodaira, Mieko; Miura, Akiko Radiation Research, Vol. 186, Issue 6 https://doi.org/10.1667/rr14402.1	journal	November 2016
No Evidence of Radiation Effect on Mutation Rates at Hypervariable Minisatellite Loci in the Germ Cells of Atomic Bomb Survivors Kodaira, Mieko; Izumi, Shizue; Takahashi, Norio Radiation Research, Vol. 162, Issue 4 https://doi.org/10.1667/rr3243	journal	October 2004
Resistance of Differentiating Spermatogonia to Radiation-Induced Apoptosis and Loss in p53-Deficient Mice Hasegawa, Masatoshi; Zhang, Yun; Niibe, Hideo Radiation Research, Vol. 149, Issue 3 https://doi.org/10.2307/3579959	journal	March 1998
Spi? selection: An efficient method to detect ?-ray-induced deletions in transgenic mice Nohmi, T.; Suzuki, M.; Masumura, K. Environmental and Molecular Mutagenesis, Vol. 34, Issue 1 https://doi.org/10.1002/(SICI)1098-2280(1999)34:1<9::AID-EM2>3.0.CO;2-E	journal	January 1999
Molecular nature of mutations induced by a high dose of x-rays in spleen, liver, and brain of thelacZ-transgenic mouse Ono, T.; Ikehata, H.; Nakamura, S. Environmental and Molecular Mutagenesis, Vol. 34, Issue 2-3 https://doi.org/10.1002/(SICI)1098-2280(1999)34:2/3<97::AID-EM7>3.0.CO;2-M	journal	January 1999
From FastQ Data to High‐Confidence Variant Calls: The Genome Analysis Toolkit Best Practices Pipeline Auwera, Geraldine A.; Carneiro, Mauricio O.; Hartl, Christopher Current Protocols in Bioinformatics, Vol. 43, Issue 1 https://doi.org/10.1002/0471250953.bi1110s43	journal	October 2013
Flow cytometric characterization of viable meiotic and postmeiotic cells by Hoechst 33342 in mouse spermatogenesis Bastos, Henri; Lassalle, Bruno; Chicheportiche, Alexandra Cytometry Part A, Vol. 65A, Issue 1 https://doi.org/10.1002/cyto.a.20129	journal	January 2005
Heavy-ion-induced mutations in thegpt delta transgenic mouse: Comparison of mutation spectra induced by heavy-ion, X-ray, and ?-ray radiation Masumura, Ken-ichi; Kuniya, Kensuke; Kurobe, Toshihiro Environmental and Molecular Mutagenesis, Vol. 40, Issue 3 https://doi.org/10.1002/em.10108	journal	January 2002
Repair capacity of fertilized mouse eggs for X-ray damage induced in sperm and mature oocytes Matsuda, Yoichi; Tobari, Izuo Mutation Research/Fundamental and Molecular Mechanisms of Mutagenesis, Vol. 210, Issue 1 https://doi.org/10.1016/0027-5107(89)90042-0	journal	January 1989
Comparison of the duration of spermatogenesis between male rodents and humans Adler, Ilse-Dore Mutation Research/Fundamental and Molecular Mechanisms of Mutagenesis, Vol. 352, Issue 1-2 https://doi.org/10.1016/0027-5107(95)00223-5	journal	June 1996
Risk of death among children of atomic bomb survivors after 62 years of follow-up: a cohort study Grant, Eric J.; Furukawa, Kyoji; Sakata, Ritsu The Lancet Oncology, Vol. 16, Issue 13 https://doi.org/10.1016/S1470-2045(15)00209-0	journal	October 2015
Chromatin dynamics during spermiogenesis Rathke, Christina; Baarends, Willy M.; Awe, Stephan Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms, Vol. 1839, Issue 3 https://doi.org/10.1016/j.bbagrm.2013.08.004	journal	March 2014
Genomic Patterns of De Novo Mutation in Simplex Autism Turner, Tychele N.; Coe, Bradley P.; Dickel, Diane E. Cell, Vol. 171, Issue 3 https://doi.org/10.1016/j.cell.2017.08.047	journal	October 2017
Radiation-induced clustered DNA lesions: Repair and mutagenesis Sage, Evelyne; Shikazono, Naoya Free Radical Biology and Medicine, Vol. 107 https://doi.org/10.1016/j.freeradbiomed.2016.12.008	journal	June 2017
Delayed repair of radiation induced clustered DNA damage: Friend or foe? Eccles, Laura J.; O’Neill, Peter; Lomax, Martine E. Mutation Research/Fundamental and Molecular Mechanisms of Mutagenesis, Vol. 711, Issue 1-2 https://doi.org/10.1016/j.mrfmmm.2010.11.003	journal	June 2011
Evidence relevant to untargeted and transgenerational effects in the offspring of irradiated parents Little, Mark P.; Goodhead, Dudley T.; Bridges, Bryn A. Mutation Research/Reviews in Mutation Research, Vol. 753, Issue 1 https://doi.org/10.1016/j.mrrev.2013.04.001	journal	July 2013
Genome-based, mechanism-driven computational modeling of risks of ionizing radiation: The next frontier in genetic risk estimation? Sankaranarayanan, K.; Nikjoo, H. Mutation Research/Reviews in Mutation Research, Vol. 764 https://doi.org/10.1016/j.mrrev.2014.12.003	journal	April 2015
Human minisatellite mutation rate after the Chernobyl accident Dubrova, Yuri E.; Nesterov, Valeri N.; Krouchinsky, Nicolay G. Nature, Vol. 380, Issue 6576 https://doi.org/10.1038/380683a0	journal	April 1996
p63 protects the female germ line during meiotic arrest Suh, Eun-Kyung; Yang, Annie; Kettenbach, Arminja Nature, Vol. 444, Issue 7119 https://doi.org/10.1038/nature05337	journal	November 2006
Rate of de novo mutations and the importance of father’s age to disease risk Kong, Augustine; Frigge, Michael L.; Masson, Gisli Nature, Vol. 488, Issue 7412 https://doi.org/10.1038/nature11396	journal	August 2012
High-throughput discovery of novel developmental phenotypes Dickinson, Mary E.; Flenniken, Ann M.; Ji, Xiao Nature, Vol. 537, Issue 7621 https://doi.org/10.1038/nature19356	journal	September 2016
Parental influence on human germline de novo mutations in 1,548 trios from Iceland Jónsson, Hákon; Sulem, Patrick; Kehr, Birte Nature, Vol. 549, Issue 7673 https://doi.org/10.1038/nature24018	journal	September 2017
Integrative genomics viewer Robinson, James T.; Thorvaldsdóttir, Helga; Winckler, Wendy Nature Biotechnology, Vol. 29, Issue 1 https://doi.org/10.1038/nbt.1754	journal	January 2011
New observations on maternal age effect on germline de novo mutations Wong, Wendy S. W.; Solomon, Benjamin D.; Bodian, Dale L. Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms10486	journal	January 2016
Mutational signatures of ionizing radiation in second malignancies Behjati, Sam; Gundem, Gunes; Wedge, David C. Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms12605	journal	September 2016
The genome-wide effects of ionizing radiation on mutation induction in the mammalian germline Adewoye, Adeolu B.; Lindsay, Sarah J.; Dubrova, Yuri E. Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms7684	journal	March 2015
Production of viable chicken by allogeneic transplantation of primordial germ cells induced from somatic cells Zhao, Ruifeng; Zuo, Qisheng; Yuan, Xia Nature Communications, Vol. 12, Issue 1 https://doi.org/10.1038/s41467-021-23242-5	journal	May 2021
Germline de novo mutation clusters arise during oocyte aging in genomic regions with high double-strand-break incidence Goldmann, Jakob M.; Seplyarskiy, Vladimir B.; Wong, Wendy S. W. Nature Genetics, Vol. 50, Issue 4 https://doi.org/10.1038/s41588-018-0071-6	journal	March 2018
Multisite de novo mutations in human offspring after paternal exposure to ionizing radiation Holtgrewe, Manuel; Knaus, Alexej; Hildebrand, Gabriele Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-33066-x	journal	October 2018
8-oxoguanine causes spontaneous de novo germline mutations in mice Ohno, Mizuki; Sakumi, Kunihiko; Fukumura, Ryutaro Scientific Reports, Vol. 4, Issue 1 https://doi.org/10.1038/srep04689	journal	April 2014
The Sequence Alignment/Map format and SAMtools Li, H.; Handsaker, B.; Wysoker, A. Bioinformatics, Vol. 25, Issue 16 https://doi.org/10.1093/bioinformatics/btp352	journal	June 2009
Fast and accurate long-read alignment with Burrows–Wheeler transform Li, Heng; Durbin, Richard Bioinformatics, Vol. 26, Issue 5 https://doi.org/10.1093/bioinformatics/btp698	journal	January 2010
Similar Mutation Rates but Highly Diverse Mutation Spectra in Ascomycete and Basidiomycete Yeasts Long, Hongan; Behringer, Megan G.; Williams, Emily Genome Biology and Evolution, Vol. 8, Issue 12 https://doi.org/10.1093/gbe/evw286	journal	December 2016
Differential Response of Mouse Male Germ-Cell Stages to Radiation-Induced Specific-Locus and Dominant Mutations Russell, W. L.; Bangham, Jean W.; Russell, Liane B. Genetics, Vol. 148, Issue 4 https://doi.org/10.1093/genetics/148.4.1567	journal	April 1998
Germline De Novo Mutation Clusters Arise During Oocyte Aging in Genomic Regions With High Double-Strand-Break Incidence Goldmann, Jakob M.; Seplyarskiy, Vladimir B.; Wong, Wendy S. W. Obstetrical & Gynecological Survey, Vol. 73, Issue 9 https://doi.org/10.1097/ogx.0000000000000604	journal	January 2018
Error-prone polymerase activity causes multinucleotide mutations in humans Harris, Kelley; Nielsen, Rasmus Genome Research, Vol. 24, Issue 9 https://doi.org/10.1101/gr.170696.113	journal	July 2014
Germline mutation rates and the long-term phenotypic effects of mutation accumulation in wild-type laboratory mice and mutator mice Uchimura, Arikuni; Higuchi, Mayumi; Minakuchi, Yohei Genome Research, Vol. 25, Issue 8 https://doi.org/10.1101/gr.186148.114	journal	June 2015
Artificial Transmutation of the gene Muller, H. J. Science, Vol. 66, Issue 1699 https://doi.org/10.1126/science.66.1699.84	journal	July 1927
Radiation Effects on Human Heredity Nakamura, Nori; Suyama, Akihiko; Noda, Asao Annual Review of Genetics, Vol. 47, Issue 1 https://doi.org/10.1146/annurev-genet-111212-133501	journal	November 2013
Multi-nucleotide de novo Mutations in Humans Besenbacher, Søren; Sulem, Patrick; Helgason, Agnar PLOS Genetics, Vol. 12, Issue 11 https://doi.org/10.1371/journal.pgen.1006315	journal	November 2016
Genome-Wide Deletion Screening with the Array CGH Method in Mouse Offspring Derived from Irradiated Spermatogonia Indicates that Mutagenic Responses are Highly Variable among Genes Asakawa, Jun-ichi; Kodaira, Mieko; Miura, Akiko Radiation Research, Vol. 186, Issue 6 https://doi.org/10.1667/RR14402.1	journal	November 2016
No Evidence of Radiation Effect on Mutation Rates at Hypervariable Minisatellite Loci in the Germ Cells of Atomic Bomb Survivors Kodaira, Mieko; Izumi, Shizue; Takahashi, Norio Radiation Research, Vol. 162, Issue 4 https://doi.org/10.1667/RR3243	journal	October 2004
Mutational signatures of ionizing radiation in second malignancies Behjati, Sam; Gundem, G.; Wedge, Dc Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.8737	text	January 2016
Resistance of Differentiating Spermatogonia to Radiation-Induced Apoptosis and Loss in p53-Deficient Mice Hasegawa, Masatoshi; Zhang, Yun; Niibe, Hideo Radiation Research, Vol. 149, Issue 3 https://doi.org/10.2307/3579959	journal	March 1998
A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w Cingolani, Pablo; Platts, Adrian; Wang, Le Lily Fly, Vol. 6, Issue 2 https://doi.org/10.4161/fly.19695	journal	April 2012
Error-prone polymerase activity causes multinucleotide mutations in humans Harris, Kelley; Nielsen, Rasmus arXiv https://doi.org/10.48550/arxiv.1312.1395	preprint	January 2013

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