Domesticated animal biobanking: Land of opportunity

PERSPECTIVE Domes ica ed Animal Biobanking: Land o Oppo uni y Linn F. G oene eld 1 *, Sigbjø n G egusson 2 , Be n Guldb and sen 3 , Sipke J. Hiems a 4 , K is ian H eem 5 , Juha Kan anen 6,7 , Hannes Lohi 8 , Lina S oems ed 9 , Pee Be g 1 1No dGen— he No dic Gene ic Resou ce Cen e , Ås, No way, 2BioBank AS, Hama , No way, 3Aa hus Uni e si y, Aa hus, Denma k, 4Cen e o Gene ic Resou ces, he Ne he lands (CGN), Wageningen Uni e si y and Resea ch Cen e, Wageningen, he Ne he lands, 5Depa men o Public Heal h, No wegian Uni e si y o Science and Technology (NTNU), T ondheim, No way, 6Na u al Resou ces Ins i u e Finland (Luke), Helsinki, Finland, 7Depa men o En i onmen al and Biological Sciences, Uni e si y o Eas e n Finland, Kuopio, Finland, 8Resea ch P og ams Uni , Molecula Neu ology, and Depa men o Ve e ina y Biosciences, Uni e si y o Helsinki, Helsinki, Finland, 9SLU Biobank, Depa men o Animal B eeding and Gene ics, Swedish Uni e si y o Ag icul u al Sciences (SLU), Uppsala, Sweden *linn.g oene eld@no dgen.o g Abs ac In he pas decade, biobanking has uelled g ea scien i ic ad ances in he human medical sec o . Well-es ablished domes ica ed animal biobanks and in eg a ed ne wo ks likewise ha bou immense po en ial o g ea scien i ic ad ances wi h b oad socie al impac s, which a e cu en ly no being ully ealised. Poli ical and scien i ic leade s as well as jou nals and e hics commi ees should help o ensu e ha we a e well equipped o mee u u e demands in li es ock p oduc ion, animal models, and e e ina y ca e o companion animals. In he las decade, human biobanking has eme ged as an impo an d i e o scien i ic ac i i- ies, and biobanks a e indispu ably an in aluable esou ce o all ypes o esea ch aimed a imp o ing public heal h. The combina ion o accessible and well-cha ac e ized biological sam- ples o a ious ypes linked wi h a mul i ude o associa ed da a is d i ing scien i ic disco e ies a unp eceden ed speed and making p e iously un hinkable lines o esea ch a eali y [1,2]. Un o una ely, biobanking o animal samples is by a less well-es ablished. In Ma ch 2015, Na u e published an a icle, i led “Inside he i s pig biobank,”desc ibing a newly es ablished biobank o po cine samples o be used in s udying human diabe es and hailing i as a pionee - ing e o in animal biobanking [3]. A PubMed sea ch con i med ha in compa ison o human biobanking he e appea s o be negligible ac i i y in he animal biobanking sec o . Sea ching i les, abs ac s, and keywo ds wi h he sea ch keys “biobank,”“biobanking,”“genebank,”and “gene bank”and limi ing he esul s o publica ion da es in 2015, only 9 o 498 sea ch esul s e e ed o animal biobanks (see S1 Da a). This appa en lack o ac i i y in he animal biobank- ing sec o is also e lec ed in a 2015 edi o ial o Biop ese a ion and Biobanking, he o icial jou nal o he In e na ional Socie y o Biological and En i onmen al Reposi o ies (ISBER), which ca e s o biobanks o any species. The au ho s conclude ha e en hough he e has been PLOS Biology | DOI:10.1371/jou nal.pbio.1002523 July 28, 2016 1/6 a11111 OPEN ACCESS Ci a ion: G oene eld LF, G egusson S, Guldb and sen B, Hiems a SJ, H eem K, Kan anen J, e al. (2016) Domes ica ed Animal Biobanking: Land o Oppo uni y. PLoS Biol 14(7): e1002523. doi:10.1371/jou nal.pbio.1002523 Published: July 28, 2016 Copy igh : © 2016 G oene eld e al. This is an open access a icle dis ibu ed unde he e ms o he C ea i e Commons A ibu ion License, which pe mi s un es ic ed use, dis ibu ion, and ep oduc ion in any medium, p o ided he o iginal au ho and sou ce a e c edi ed. Funding: The au ho s ecei ed no speci ic unding o his wo k. Compe ing In e es s: The au ho s ha e decla ed ha no compe ing in e es s exis . Abb e ia ions: BBMRI, Biobanking and BioMolecula Resou ces Resea ch In as uc u e; EMBRC, Eu opean Ma ine Biological Resou ce Cen e; ESFRI, Eu opean Council’s Eu opean S a egy Fo um on Resea ch In as uc u es; EUGENA, Eu opean Genebank Ne wo k o Animal Gene ic Resou ces; GGBN, Global Genome Biodi e si y Ne wo k; IPN, in ec ious panc ea ic nec osis; ISBER, In e na ional Socie y o Biological and En i onmen al Reposi o ies; MIRRI, Mic obial Resou ce Resea ch In as uc u e; QTL, quan i a i e ai locus; SLU, Swedish Uni e si y o Ag icul u al Sciences inc easing pa icipa ion om he non-human biobanking sec o in he annual ISBER mee ings, he e is s ill a p onounced lack o submissions o he jou nal pe aining o non-human bio- banking, and human biobanking issues con inue o domina e ISBER ac i i ies [4]. The oad- map o he Eu opean Council’s Eu opean S a egy Fo um on Resea ch In as uc u es (ESFRI) e eals ha he e a e p ojec s unde way in ol ing human (Biobanking and BioMolecula Resou ces Resea ch In as uc u e [BBMRI]), ma ine (Eu opean Ma ine Biological Resou ce Cen e [EMBRC]), mic obial (Mic obial Resou ce Resea ch In as uc u e [MIRRI]), and mouse model (In a on ie ) biobanks, wi h gene al animal biobanks s a kly missing on ha lis [5]. Na u ally, some non-human biobanks s o ing animal samples, amongs o he s, do exis . The mos ac i e a e likely he na u al his o y collec ions, because hey ha e he in insic ask o collec , ca alogue, and s o e specimens. The Global Genome Biodi e si y Ne wo k (GGBN), es ablished in 2011, ac s as an umb ella o ganisa ion o biodi e si y eposi o ies and aims o es ablish s anda ds and bes p ac ices as well as inc ease sample accessibili y h ough i s da a po al [6]. A sea ch o he mos common domes ica ed animal species (ca le, sheep, goa , pig, ho se, chicken, and dog) yielded only 13 eco ds in he GGBN membe eposi o ies. Howe e , some domes ica ed animal biobanks and less o malized sample collec ions can be ound. Thei hos ing ins i u ions ange om e e ina y hospi als, zoos, b eeding and diag- nos ics companies, na ional a m animal gene ic esou ce gene banks, o esea ch ins i u es and uni e si ies. Depending on hei pu pose, he s o ed ypes o samples a y g ea ly and ange om heal hy issue samples, diseased pa hogenic issue samples, DNA, and RNA o ep oduc i e ma e ials. An example o a well-es ablished physical non-human biobanking in as uc u e se ing a uni e si y is he Swedish Uni e si y o Ag icul u al Sciences’(SLU) Biobank (h p://www.slu.se/slubiobank). This biobank also o e s a da a po al o inc easing he isibili y and accessibili y o non-human sample collec ions no ma e whe e hey a e s o ed. This da a po al would be edundan i all samples, oge he wi h hei associa ed da a, we e s o ed in es ablished biobanks ha ensu ed he isibili y o hei samples h ough a ne - wo k such as GGBN. In con as , he Eu opean Genebank Ne wo k o Animal Gene ic Resou ces (EUGENA), coo dina ed by he Eu opean Regional Focal Poin on Animal Gene ic Resou ces (h p://www. p-eu ope.o g), is an eme ging ne wo king ac i i y speci ically a ge - ing only na ional a m animal gene ic esou ce collec ions [7]. These dispa a e examples dem- ons a e ha he e is a lack o a uni ied and gene alized app oach o sample collec ions in he domes ica ed animal sec o . None heless, he e a e nume ous examples o how di e en disciplines and s akeholde s, and ul ima ely he gene al public, ha e al eady bene i ed om he a ailabili y o biobanked domes ica ed animal samples. E en hough he pig biobank was commended as a pionee ing e o [3], he e a e in ac a numbe o biobanks ha accommoda e animal models o he s udy o human disease. The domes ic dog, o example, wi h i s unique popula ion his o y, b eed s uc u e, and hund eds o spon aneous gene ic condi ions has p o en o be an excellen model o gene mapping in simple and complex diso de s [8]. Ta ge ed and e ec i e b eeding p og ams o e he pas 150 yea s ha e c ea ed hund eds o dis inc b eeds ha o m gene ic isola es wi h educed gene ic he e ogenei y. This simpli ies gene ic s udies because ewe suscep ibili y loci wi h highe impac con ibu e o complex disease and allow gene ic b eak h oughs wi h smalle s udy coho s as compa ed o he co esponding human condi ions [9]. The anno a ion o he canine genome acili a ed a apid e olu ion o genomic ools and de elopmen o se e al canine biobanks ac oss he con inen s [10]. Collec i ely, hese biobanks house hund eds o housands o DNA samples and issue specimens o hund eds o condi- ions wi h medical ele ance o humans. Impo an ly, many canine biobanks main ain ac i e PLOS Biology | DOI:10.1371/jou nal.pbio.1002523 July 28, 2016 2/6 collabo a i e ne wo ks wi h he b eede communi y and dog ancie s as well as e e ina y clin- ics and hospi als o pa ien ec ui men and heal h upda es. Besides playing an ins umen al ole o human heal h, biobanked animal samples hea ily impac de elopmen s in ood p oduc ion and he sus ainable managemen o he wo ld’s ini e esou ces. Biobanks in animal b eeding, o en e e ed o as gene banks, we e ini ially es ab- lished wi h he ad en o new ep oduc i e echniques, such as a i icial insemina ion, and ypi- cally s o ed semen and emb yos. These biobanks ecen ly played a c i ical ole in he swi implemen a ion o genomic selec ion, which uses genome-wide SNP ma ke s o p edic he gene ic me i o b eeding indi iduals [11,12]. The e icien use o genomic selec ion equi es la ge e e ence panels o indi iduals whose gene ic alues a e known wi h high con idence. In ca le b eeding, hese a e bulls wi h la ge numbe s o o sp ing wi h eco ded pe o mance da a, such as milk yield. Genomic selec ion could only be implemen ed so swi ly and success- ully because DNA o semen samples om a la ge numbe o bulls we e a ailable om ca le b eeding company biobanks, and hese samples could be linked o pe o mance eco ds o he espec i e bulls’o sp ing. This echnology was i s adop ed by he dai y indus y and can po en ially esul in a 60%–120% inc ease in he a e o gene ic gain. Toge he wi h ad anced geno yping and ep oduc i e echnologies, genomic selec ion has he po en ial o inc ease gene ic imp o emen bo h in o en neglec ed ai s, such as eed e iciency and e ili y, and in ai s ha only ecen ly ha e become o in e es , such as me hane ou pu in uminan s o adap- a ion o clima e change [12]. Imp o emen s in hese ai s a e o g ea in e es o ensu ing global ood secu i y and sus ainable managemen o ou limi ed esou ces. Wi hou he a ail- abili y o he gene bank samples, as well as associa ed pe o mance da a eco ds, his ans o - ma ion would ha e aken decades, i i had happened a all. Biobanks also play an in eg al pa in wo ldwide conse a ion e o s o coun e ac he well- documen ed loss o gene ic di e si y in p oduc ion animals [13,14]. Slowly, he gene al pe cep- ion ha hese eposi o ies a e only o be used in eme gencies and as a las eso is changing. In 2012, he USDA Na ional Animal Ge mplasm P og am, o example, ha bou ed mo e han 700,000 game e and issue samples om o e 18,000 animals ep esen ing mo e han 130 b eeds. F om his eposi o y, samples om mo e han 3,300 animals had been eques ed and dis ibu ed o use in esea ch and indus y by 2012. The applica ions included quan i a i e ai locus (QTL) s udies, assessmen o gene ic dis ances, c yobiology esea ch, gene a ion o an expe imen al esea ch line, educ ion o inb eeding, and e-in oduc ion o geno ypic com- bina ions los in cu en p oduc ion popula ions [14]. Samples om a e and endange ed b eeds a e also inding use in esea ch and de elopmen o he leading b eeding companies. Fo example, in he Ne he lands, a conso ium o uni e si y and dai y indus y pa ne s geno- yped samples om a e local ca le b eeds o gain insigh in o he gene ic backg ound o milk a y acid composi ion. Genomic-assis ed in og ession could ul ima ely be used o in oduce a ou able alleles ound in he a e b eeds in o mo e widely used b eeds. Biobanked samples also played an impo an ole in igh ing a i al in ec ion, in ec ious panc ea ic nec osis (IPN), which is common in a med ish. This i us can lead o a es o >90% mo ali y in a med A lan ic salmon, which, he e o e, poses a h ea o animal wel a e and aquacul u e indus ies. In 2008, a majo QTL o IPN- esis ance was de ec ed in A lan ic salmon. Al eady, a yea la e , AquaGen, which supplies abou 55% o A lan ic salmon eggs used comme cially in No way, was employing ma ke -assis ed selec ion o p oduce IPN- esis- an ish. This swi implemen a ion o he QTL in ma ke -assis ed selec ion was only possible due o he a ailabili y o biobanked samples collec ed in a challenge es in 2005 [15]. In addi ion o comba ing disease in animals, biobanked domes ic animal samples also play a c ucial ole in igh ing eme ging in ec ious diseases ha a e o en zoono ic, meaning ha hey can be ansmi ed be ween e eb a e animals and humans. Ha ing access o samples o PLOS Biology | DOI:10.1371/jou nal.pbio.1002523 July 28, 2016 3/6 species ha ac as ese oi s o a disease g ea ly acili a es he wo k o public heal h esponde s du ing in ec ious disease ou b eaks [16]. In his con ex , he collec ion and aceable link o associa ed samples, such as pa asi es, pa hogens, and o he mic obio a, o hei pa en sample becomes especially impo an . We a e con inced ha hese examples lea e no doub ha biobanked animal samples hold g ea po en ial bo h o ad ancing human and animal heal h and wel a e as well as secu ing u u e ood p oduc ion. Fu he mo e, he ecen ad en o cos -e icien gene modi ica ion echnologies [17] en isages many p oduc ion, pe o mance, and heal h applica ions in li e- s ock and companion animals and u he adds in e es in animal biobanks. When examining he causes o he low le els o ac i i y in la ge-scale domes ica ed animal biobanking, bo h in ega d o he es ablishmen o use o exis ing physical biobanking in a- s uc u es as well as o e a ching da a po als, a numbe o hypo heses come o mind. The indus ies connec ed o domes ica ed animal biobanking, such as li es ock and companion ani- mal p oduc ion and e e ina y ca e, a e dwa ed by he heal hca e indus y, so mone a y incen i es would p esumably play a much smalle ole. Legisla ion may ha e ac ed as a d i e in he o maliza ion and shaping o biobanks and di e en ial legisla ion ega ding he han- dling, s o age, and sha ing o human e sus animal biosamples, and associa ed da a may hus ha e led o dispa a e de elopmen s. I is mo eo e concei able ha he communi y a ound domes ica ed animal biobanking is mo e agmen ed and consis s o mo e di e se s akeholde s (academic, non-p o i , indus ial) han he human biobanking communi y, which could explain he absence o la ge-scale coope a i e umb ella p ojec s. Mo eo e , he e may be g ea e di icul ies in d a ing ma e ial ans e ag eemen s o ep oduc i e ma e ials han o o he ypes o samples. We will only be able o exploi he ull po en ial i we, in pa allel wi h human and biodi e - si y biobanking, ackle he challenges o s anda dized sampling, p ocessing, and s o age, sam- ple isibili y and accessibili y, s anda dized codes o diagnoses, collec ion and s o age o associa ed da a wi h he possibili y o upda es, as well as e hical and egula o y issues. He e, i is ad isable ha he domes ica ed animal sec o ensu es ull compa ibili y wi h and elies on exis ing ini ia i es whe e e easible. Especially impo an in his con ex is o ensu e a link be ween samples and associa ed phenomic and genomic da a, such as de i ed sequence da a. To achie e ag eemen on s anda ds, bo h in e ms o sample p ocessing and s o age and sam- ple isibili y and accessibili y, ac o s om e e ina y hospi als, zoos, b eeding and diagnos ics companies, na ional a m animal gene ic esou ce gene banks, esea ch ins i u es, uni e si ies, and policymake s need o join o ces. This is whe e we momen a ily see a lack o coo dina ed e o s. To espond o hese challenges and o ensu e ha we a e well equipped o mee u u e demands in li es ock p oduc ion, animal models, and e e ina y ca e o companion animals, we p opose ha scien i ic and poli ical leade s need o (i) acknowledge he inadequacy o he cu en si ua ion, (ii) c ea e oppo uni y and suppo o he es ablishmen o an in e na ional esea ch in as uc u e o animal biobanking, and (iii) mo i a e academic and indus ial s ake- holde s o de elop and coo dina e biobanks based on lessons lea ned om human and biodi- e si y biobanking. In Eu ope, he Eu opean Council’s ESFRI could play a leading ole in he es ablishmen o a domes ica ed animal biobanking ne wo k, including bes p ac ices, di ely needed s anda ds, and a common on ology. In a landscape analysis o Eu opean esea ch in as uc u es, he 2016 ESFRI oadmap acknowledges a gap in he ag icul u al and bio-economy sec o and explici ly lis s li es ock acili ies including gene banks [5]. While an inc ease in ac i i ies ega ding biobanking o a m animal gene ic esou ces is ce ainly ele an , we conside his no o be a - eaching enough. A s ep in he igh di ec ion would be o begin wi h compiling PLOS Biology | DOI:10.1371/jou nal.pbio.1002523 July 28, 2016 4/6 in o ma ion on all exis ing animal biobanks, analogous o BBMRI’s ca alogue o Eu opean human biobanks [18], which cu en ly con ains in o ma ion on 340 biobanks (h p://www. bbm ipo al.eu/). Mo eo e , e hics commi ees should equi e he s o age o samples and associa ed da a in o malized biobanks o he app o al o scien i ic expe imen s. Simila ly, jou nals should apply he same s anda d o samples and associa ed da a, as hey cu en ly apply o molecula da a, in e ms o s o age in o malized eposi o ies p io o publica ion. Suppo ing In o ma ion S1 Da a. PubMed sea ch. A PubMed sea ch was ca ied ou on Janua y 14, 2016. Ti les, abs ac s, and keywo ds we e sea ched wi h he sea ch keys "biobank," "biobanking," "gene- bank," and "gene bank," and esul s we e limi ed o publica ion da es in 2015. (XLSX) Re e ences 1. Simeon-Dubach D, Wa son P. Biobanking 3.0: E idence based and cus ome ocused biobanking. Clinical Biochemis y 2014; 47:300–8. doi: 10.1016/j.clinbiochem.2013.12.018 PMID: 24406300 2. Vaugh J. Biobanking Comes o Age: The T ansi ion o Biospecimen Science. Annu Re Pha macol Toxicol 2016; 56:211–28. doi: 10.1146/annu e -pha m ox-010715-103246 PMID: 26514206 3. Abbo A. Inside he i s pig biobank. Na u e 2015; 519:397–8. doi: 10.1038/519397a PMID: 25810182 4. Mullins P, Pugh R, Vaugh J. Following up on ISBER 2015: Call o En i onmen al Biobanking Pape s. Biop ese a ion and Biobanking 2015; 13:229–30. doi: 10.1089/bio.2015.29013.pm PMID: 26280500 5. Eu opean S a egy Fo um on Resea ch In as uc u es. S a egy epo on esea ch in as uc u es: Roadmap 2016. Science and Technology Facili ies Council; 2016. 6. D oege G, Ba ke K, As in JJ, Ba els P, Bu le C, Can ill D, e al. The Global Genome Biodi e si y Ne wo k (GGBN) Da a Po al. Nucleic Acids Resea ch 2014; 42:D607–12. doi: 10.1093/na /gk 928 PMID: 24137012 7. Hiems a SJ, Ma yniuk E, Duche ZI, Begemann F, o he s. Eu opean Gene Bank Ne wo k o Animal Gene ic Resou ces (EUGENA). P oceedings, 10 h Wo ld Cong ess o Gene ics Applied o Li es ock P oduc ion, 2014. 8. Lindblad-Toh K, Wade CM, Mikkelsen TS, Ka lsson EK, Ja e DB, Kamal M, e al. Genome sequence, compa a i e analysis and haplo ype s uc u e o he domes ic dog. Na u e 2005; 438:803–19. doi: 10. 1038/na u e04338 PMID: 16341006 9. Wilbe M, Jokinen P, T u é K, Seppala EH, Ka lsson EK, Biagi T, e al. Genome-wide associa ion map- ping iden i ies mul iple loci o a canine SLE- ela ed disease complex. Na u e Gene ics 2010; 42:250– 4. doi: 10.1038/ng.525 PMID: 20101241 10. Lequa é A-S, Ande sson L, And é C, F edholm M, Hi e C, Leeb T, e al. LUPA: A Eu opean ini ia i e aking ad an age o he canine genome a chi ec u e o un a elling complex diso de s in bo h human and dogs. The Ve e ina y Jou nal 2011; 189:155–9. doi: 10.1016/j. jl.2011.06.013 PMID: 21752675 11. Meuwissen THE, Hayes BJ, Godda d ME. P edic ion o o al gene ic alue using genome-wide dense ma ke maps. Gene ics 2001; 157:1819–1829. PMID: 11290733 12. Hayes BJ, Lewin HA, Godda d ME. The u u e o li es ock b eeding: genomic selec ion o e iciency, educed emissions in ensi y, and adap a ion. T ends in Gene ics 2013; 29:206–14. doi: 10.1016/j. ig. 2012.11.009 PMID: 23261029 13. FAO. The Second Repo on he S a e o he Wo ld’s Animal Gene ic Resou ces o Food and Ag icul- u e. Rome: FAO Commission on Gene ic Resou ces o Food and Ag icul u e Assessmen s; 2015. 14. Blackbu n H. Gene ic Selec ion and Conse a ion o Gene ic Di e si y*. Rep oduc ion in Domes ic Ani- mals 2012; 47:249–54. doi: 10.1111/j.1439-0531.2012.02083.x PMID: 22827378 15. Moen T, To ge sen J, San i N, Da idson WS, Ba anski M, Odega d J, e al. Epi helial Cadhe in De e - mines Resis ance o In ec ious Panc ea ic Nec osis Vi us in A lan ic Salmon. Gene ics 2015; 200:1313–26. doi: 10.1534/gene ics.115.175406 PMID: 26041276 16. DiEuliis D, Johnson KR, Mo se SS, Schindel DE. Opinion: Specimen collec ions should ha e a much bigge ole in in ec ious disease esea ch and esponse. P oceedings o he Na ional Academy o Sci- ences 2016; 113:4–7. doi: 10.1073/pnas.1522680112 PLOS Biology | DOI:10.1371/jou nal.pbio.1002523 July 28, 2016 5/6 17. Cong L, Ran FA, Cox D, Lin S, Ba e o R, Habib N, e al. Mul iplex Genome Enginee ing Using CRISPR/Cas Sys ems. Science 2013; 339:819–23. doi: 10.1126/science.1231143 PMID: 23287718 18. Wichmann H-E, Kuhn KA, Waldenbe ge M, Schmelche D, Schu enhaue S, Mei inge T, e al. Com- p ehensi e ca alog o Eu opean biobanks. Na u e Bio echnology 2011; 29:795–7. doi: 10.1038/nb . 1958 PMID: 21904320 PLOS Biology | DOI:10.1371/jou nal.pbio.1002523 July 28, 2016 6/6