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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Efficacy of the porcine species in biomedical research</title><author><name sortKey="Gutierrez, Karina" sort="Gutierrez, Karina" uniqKey="Gutierrez K" first="Karina" last="Gutierrez">Karina Gutierrez</name><affiliation><nlm:aff id="aff1"><institution>Department of Animal Science, McGill University, Sainte-Anne-de-Bellevue</institution><country>QC, Canada</country></nlm:aff></affiliation></author><author><name sortKey="Dicks, Naomi" sort="Dicks, Naomi" uniqKey="Dicks N" first="Naomi" last="Dicks">Naomi Dicks</name><affiliation><nlm:aff id="aff1"><institution>Department of Animal Science, McGill University, Sainte-Anne-de-Bellevue</institution><country>QC, Canada</country></nlm:aff></affiliation></author><author><name sortKey="Glanzner, Werner G" sort="Glanzner, Werner G" uniqKey="Glanzner W" first="Werner G." last="Glanzner">Werner G. Glanzner</name><affiliation><nlm:aff id="aff1"><institution>Department of Animal Science, McGill University, Sainte-Anne-de-Bellevue</institution><country>QC, Canada</country></nlm:aff></affiliation></author><author><name sortKey="Agellon, Luis B" sort="Agellon, Luis B" uniqKey="Agellon L" first="Luis B." last="Agellon">Luis B. Agellon</name><affiliation><nlm:aff id="aff2"><institution>School of Dietetics and Human Nutrition, McGill University, Sainte-Anne-de-Bellevue</institution><country>QC, Canada</country></nlm:aff></affiliation></author><author><name sortKey="Bordignon, Vilceu" sort="Bordignon, Vilceu" uniqKey="Bordignon V" first="Vilceu" last="Bordignon">Vilceu Bordignon</name><affiliation><nlm:aff id="aff1"><institution>Department of Animal Science, McGill University, Sainte-Anne-de-Bellevue</institution><country>QC, Canada</country></nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">26442109</idno><idno type="pmc">4584988</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4584988</idno><idno type="RBID">PMC:4584988</idno><idno type="doi">10.3389/fgene.2015.00293</idno><date when="2015">2015</date><idno type="wicri:Area/Pmc/Corpus">000059</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000059</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Efficacy of the porcine species in biomedical research</title><author><name sortKey="Gutierrez, Karina" sort="Gutierrez, Karina" uniqKey="Gutierrez K" first="Karina" last="Gutierrez">Karina Gutierrez</name><affiliation><nlm:aff id="aff1"><institution>Department of Animal Science, McGill University, Sainte-Anne-de-Bellevue</institution><country>QC, Canada</country></nlm:aff></affiliation></author><author><name sortKey="Dicks, Naomi" sort="Dicks, Naomi" uniqKey="Dicks N" first="Naomi" last="Dicks">Naomi Dicks</name><affiliation><nlm:aff id="aff1"><institution>Department of Animal Science, McGill University, Sainte-Anne-de-Bellevue</institution><country>QC, Canada</country></nlm:aff></affiliation></author><author><name sortKey="Glanzner, Werner G" sort="Glanzner, Werner G" uniqKey="Glanzner W" first="Werner G." last="Glanzner">Werner G. Glanzner</name><affiliation><nlm:aff id="aff1"><institution>Department of Animal Science, McGill University, Sainte-Anne-de-Bellevue</institution><country>QC, Canada</country></nlm:aff></affiliation></author><author><name sortKey="Agellon, Luis B" sort="Agellon, Luis B" uniqKey="Agellon L" first="Luis B." last="Agellon">Luis B. Agellon</name><affiliation><nlm:aff id="aff2"><institution>School of Dietetics and Human Nutrition, McGill University, Sainte-Anne-de-Bellevue</institution><country>QC, Canada</country></nlm:aff></affiliation></author><author><name sortKey="Bordignon, Vilceu" sort="Bordignon, Vilceu" uniqKey="Bordignon V" first="Vilceu" last="Bordignon">Vilceu Bordignon</name><affiliation><nlm:aff id="aff1"><institution>Department of Animal Science, McGill University, Sainte-Anne-de-Bellevue</institution><country>QC, Canada</country></nlm:aff></affiliation></author></analytic><series><title level="j">Frontiers in Genetics</title><idno type="eISSN">1664-8021</idno><imprint><date when="2015">2015</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Since domestication, pigs have been used extensively in agriculture and kept as companion animals. More recently they have been used in biomedical research, given they share many physiological and anatomical similarities with humans. Recent technological advances in assisted reproduction, somatic cell cloning, stem cell culture, genome editing, and transgenesis now enable the creation of unique porcine models of human diseases. Here, we highlight the potential applications and advantages of using pigs, particularly minipigs, as indispensable large animal models in fundamental and clinical research, including the development of therapeutics for inherited and chronic disorders, and cancers.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Abukawa, H" uniqKey="Abukawa H">H. Abukawa</name></author><author><name sortKey="Terai, H" uniqKey="Terai H">H. Terai</name></author><author><name sortKey="Hannouche, D" uniqKey="Hannouche D">D. Hannouche</name></author><author><name sortKey="Vacanti, J P" uniqKey="Vacanti J">J. P. 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Front Genet</journal-id><journal-id journal-id-type="iso-abbrev">Front Genet</journal-id><journal-id journal-id-type="publisher-id">Front. Genet.</journal-id><journal-title-group><journal-title>Frontiers in Genetics</journal-title></journal-title-group><issn pub-type="epub">1664-8021</issn><publisher><publisher-name>Frontiers Media S.A.</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">26442109</article-id><article-id pub-id-type="pmc">4584988</article-id><article-id pub-id-type="doi">10.3389/fgene.2015.00293</article-id><article-categories><subj-group subj-group-type="heading"><subject>Genetics</subject><subj-group><subject>Perspective</subject></subj-group></subj-group></article-categories><title-group><article-title>Efficacy of the porcine species in biomedical research</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Gutierrez</surname><given-names>Karina</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/192415/overview"></uri></contrib><contrib contrib-type="author"><name><surname>Dicks</surname><given-names>Naomi</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/183378/overview"></uri></contrib><contrib contrib-type="author"><name><surname>Glanzner</surname><given-names>Werner G.</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/205628/overview"></uri></contrib><contrib contrib-type="author"><name><surname>Agellon</surname><given-names>Luis B.</given-names></name><xref ref-type="aff" rid="aff2"><sup>2</sup></xref><xref ref-type="author-notes" rid="fn001"><sup>*</sup></xref><uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/191704/overview"></uri></contrib><contrib contrib-type="author"><name><surname>Bordignon</surname><given-names>Vilceu</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><xref ref-type="author-notes" rid="fn001"><sup>*</sup></xref><uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/205268/overview"></uri></contrib></contrib-group><aff id="aff1"><sup>1</sup><institution>Department of Animal Science, McGill University, Sainte-Anne-de-Bellevue</institution><country>QC, Canada</country></aff><aff id="aff2"><sup>2</sup><institution>School of Dietetics and Human Nutrition, McGill University, Sainte-Anne-de-Bellevue</institution><country>QC, Canada</country></aff><author-notes><fn fn-type="edited-by"><p>Edited by: <italic>Tiago Collares, Federal University of Pelotas, Brazil</italic></p></fn><fn fn-type="edited-by"><p>Reviewed by: <italic>Thomas John, Ludwig Institute for Cancer Research, Australia; Howard Donninger, University of Louisville, USA</italic></p></fn><corresp id="fn001">*Correspondence: <italic>Vilceu Bordignon, Department of Animal Science, McGill University, Sainte-Anne-de-Bellevue, QC H9X 3V9, Canada, <email xlink:type="simple">vilceu.bordignon@mcgill.ca</email>; Luis B. Agellon, School of Dietetics and Human Nutrition, McGill University, Sainte-Anne-de-Bellevue, QC H9X 3V9, Canada, <email xlink:type="simple">luis.agellon@mcgill.ca</email></italic></corresp><fn fn-type="other" id="fn002"><p>This article was submitted to Cancer Genetics, a section of the journal Frontiers in Genetics</p></fn></author-notes><pub-date pub-type="epub"><day>16</day><month>9</month><year>2015</year></pub-date><pub-date pub-type="collection"><year>2015</year></pub-date><volume>6</volume><elocation-id>293</elocation-id><history><date date-type="received"><day>30</day><month>6</month><year>2015</year></date><date date-type="accepted"><day>04</day><month>9</month><year>2015</year></date></history><permissions><copyright-statement>Copyright © 2015 Gutierrez, Dicks, Glanzner, Agellon and Bordignon.</copyright-statement><copyright-year>2015</copyright-year><copyright-holder>Gutierrez, Dicks, Glanzner, Agellon and Bordignon</copyright-holder><license xlink:href="http://creativecommons.org/licenses/by/4.0/"><license-p>This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.</license-p></license></permissions><abstract><p>Since domestication, pigs have been used extensively in agriculture and kept as companion animals. More recently they have been used in biomedical research, given they share many physiological and anatomical similarities with humans. Recent technological advances in assisted reproduction, somatic cell cloning, stem cell culture, genome editing, and transgenesis now enable the creation of unique porcine models of human diseases. Here, we highlight the potential applications and advantages of using pigs, particularly minipigs, as indispensable large animal models in fundamental and clinical research, including the development of therapeutics for inherited and chronic disorders, and cancers.</p></abstract><kwd-group><kwd>Large animal models</kwd><kwd>biomedical research</kwd><kwd>swine</kwd><kwd>pigs</kwd><kwd>minipigs</kwd><kwd>clones</kwd><kwd>transgenics</kwd></kwd-group><counts><fig-count count="1"></fig-count><table-count count="1"></table-count><equation-count count="0"></equation-count><ref-count count="121"></ref-count><page-count count="9"></page-count><word-count count="0"></word-count></counts></article-meta></front><body><sec sec-type="intro"><title>Introduction</title><p>The first evidence of swine domestication dates back to approximately 7000–9000 years ago (<xref rid="B43" ref-type="bibr">Jones, 1998</xref>; <xref rid="B66" ref-type="bibr">McGlone and Pond, 2003</xref>; <xref rid="B46" ref-type="bibr">Köhn, 2011</xref>; <xref rid="B55" ref-type="bibr">Larson et al., 2011</xref>; <bold>Figure <xref ref-type="fig" rid="F1">1A</xref></bold>). China and Europe have been, since domestication, the pig-breeding centers dictating the profile of the pig breeds (<xref rid="B43" ref-type="bibr">Jones, 1998</xref>; <xref rid="B3" ref-type="bibr">Amills et al., 2001</xref>). The reason for domestication was to provide meat as a source of food protein, which stimulated pig selection and farming (<xref rid="B43" ref-type="bibr">Jones, 1998</xref>; <xref rid="B46" ref-type="bibr">Köhn, 2011</xref>). Studies have been conducted using genome-wide genotyping and genetic variability to trace the migration, selection, and improvement from ancient wild species to modern swine (<xref rid="B32" ref-type="bibr">Giuffra et al., 2000</xref>; <xref rid="B7" ref-type="bibr">Bosse et al., 2014a</xref>,<xref rid="B8" ref-type="bibr">b</xref>). It is generally accepted that the majority of all modern breeds are derived from the Eurasian wild boar (European and Asian wild boars; <xref rid="B87" ref-type="bibr">Porter, 1993</xref>; <xref rid="B8" ref-type="bibr">Bosse et al., 2014b</xref>). Although pig selection started just after domestication, it has only been since the mid-20th century that performance has been used as the main tool in the animal selection process (<xref rid="B94" ref-type="bibr">Safranski, 2008</xref>). More recently, molecular biology technologies, genome-wide association studies, and next-generation sequencing have been applied to enhance the selection process of domesticated pig breeds (e.g., Duroc, Landrace, Pietrain, Yorkshire, etc.) to further improve traits of high economic value such as feed conversion, meat quality, growth, precocious puberty, and prolificity (<xref rid="B95" ref-type="bibr">Sahana et al., 2013</xref>; <xref rid="B111" ref-type="bibr">Tart et al., 2013</xref>; <xref rid="B41" ref-type="bibr">Jiang et al., 2014</xref>; <xref rid="B96" ref-type="bibr">Sanchez et al., 2014</xref>).</p><fig id="F1" position="float"><label>FIGURE 1</label><caption><p><bold>History of pigs in agriculture and research since domestication. (A)</bold> Timeline, significant events and application of different technologies in the selection and breeding of the porcine species (<xref rid="B43" ref-type="bibr">Jones, 1998</xref>; <xref rid="B75" ref-type="bibr">Onishi et al., 2000</xref>; <xref rid="B86" ref-type="bibr">Polejaeva et al., 2000</xref>; <xref rid="B66" ref-type="bibr">McGlone and Pond, 2003</xref>; <xref rid="B9" ref-type="bibr">Brevini et al., 2007a</xref>,<xref rid="B10" ref-type="bibr">b</xref>; <xref rid="B26" ref-type="bibr">Estrada et al., 2008</xref>; <xref rid="B94" ref-type="bibr">Safranski, 2008</xref>; <xref rid="B114" ref-type="bibr">Wakai et al., 2008</xref>; <xref rid="B25" ref-type="bibr">Esteban et al., 2009</xref>; <xref rid="B27" ref-type="bibr">Ezashi et al., 2009</xref>; <xref rid="B37" ref-type="bibr">Hauschild et al., 2011</xref>; <xref rid="B46" ref-type="bibr">Köhn, 2011</xref>; <xref rid="B55" ref-type="bibr">Larson et al., 2011</xref>; <xref rid="B13" ref-type="bibr">Carlson et al., 2012</xref>; <xref rid="B36" ref-type="bibr">Hai et al., 2014</xref>; <xref rid="B118" ref-type="bibr">Whitworth et al., 2014</xref>). <bold>(B)</bold> Use of the porcine species in research, and <bold>(C)</bold> application of minipig models in a variety of studies (based on articles indexed by PubMed, from 1970 to the present date).</p></caption><graphic xlink:href="fgene-06-00293-g001"></graphic></fig><p>The variety of modern pig breeds available today (<xref rid="B11" ref-type="bibr">Buchanan and Stalder, 2011</xref>), are a product of human intervention since domestication, but especially during the last century (<bold>Figure <xref ref-type="fig" rid="F1">1A</xref></bold>). Besides breeds specialized for food production, smaller sized breeds (miniature- and micro-pigs) with certain characteristics such as obedience, friendly nature, and cognitive ability have also been selected for the purpose of companion animals. In addition, their use in biomedical research has been increasing considerably in the last years (<bold>Figure <xref ref-type="fig" rid="F1">1B</xref></bold>).</p><p>Compared with other animals used in research (e.g., mice, rats, rabbits, and dogs), domestic farm pigs are much larger (>300 kg adult size), therefore, requiring more space and feed, and making them harder to handle. Mini- or micro-pigs are hence more desirable for research use. The adult sizes vary among breeds, reaching around 20–30 kg for a Panepinto micropig to 100 kg for a Munich minipig (<xref rid="B46" ref-type="bibr">Köhn, 2011</xref>). Although many minipig breeds are a product of crossbreeding, some breeds, like the Yucatan pigs, are naturally occurring stocks (<xref rid="B77" ref-type="bibr">Panepinto, 1996</xref>; <xref rid="B46" ref-type="bibr">Köhn, 2011</xref>). Since the late 1940s, minipigs have been further developed specifically for biomedical research purposes (<xref rid="B24" ref-type="bibr">England and Panepinto, 1986</xref>; <xref rid="B46" ref-type="bibr">Köhn, 2011</xref>).</p><p>There are now several minipig breeds available for use in research (<xref rid="B77" ref-type="bibr">Panepinto, 1996</xref>). The main breeds developed in the USA are Yucatan, Sinclair (also known as Minnesota or Hormel miniature pig), Hanford, NIH minipig and Panepinto miniature pig. The minipig breeds developed in Europe are Göttingen, Munich, Berlin, Mini-Lewe, Czech-Republic, Vietnamese potbellied and Mini-Sib. In Asia, the breeds include Ohmini, Clawn, Lee Sung, and Chinese minipigs. The Göttingen and Yucatan breeds are the most commonly used minipigs in research, although there is no apparent clear reason for preference. Unlike the Yucatan, a natural breed, the Göttingen minipig was developed specifically for research use. Other breeds are used only by specific research groups, thus limiting their widespread availability in research. Nevertheless, the interest in the use of pigs in biomedical research has been rising over the last 40–45 years (<bold>Figure <xref ref-type="fig" rid="F1">1B</xref></bold>).</p></sec><sec><title>Use of Pigs in Biomedical Research</title><p>Biomedical research is broad, spanning studies on underlying disease mechanisms to the evaluation of safety and effectiveness of preventative measures, diagnostic tests, and therapies. Most animal studies in recent times have used the murine species due to their small size, fast reproductive cycles and short lifespan. In addition, the availability of murine embryonic stem cells, fully annotated genome, and facile tools for targeted genetic manipulation have all contributed to the elucidation of gene functions and disease pathophysiology. However, in many cases, mouse models do not adequately represent features of human disorders (<xref rid="B101" ref-type="bibr">Seok et al., 2013</xref>). In this regard, animals that better represent human pathophysiology are required. Pigs and humans share many similarities such as size, physiology, anatomy, metabolic profile, and longer lifespan (<xref rid="B77" ref-type="bibr">Panepinto, 1996</xref>; <xref rid="B104" ref-type="bibr">Spurlock and Gabler, 2008</xref>; <xref rid="B51" ref-type="bibr">Kuzmuk and Schook, 2011</xref>; <xref rid="B107" ref-type="bibr">Swindle et al., 2012</xref>). For example, pig skin is structurally similar to human skin regarding thickness and spacing between hair follicles, making it useful for studies on wound healing and burn lesions (<xref rid="B106" ref-type="bibr">Sullivan et al., 2001</xref>). Pigs also share anatomical and physiological similarities with respect to the renal system, making them valuable for pharmacological studies (<xref rid="B18" ref-type="bibr">Dalgaard, 2014</xref>; <xref rid="B39" ref-type="bibr">Huppertz et al., 2015</xref>). Pigs can also be useful in the study of nutrient absorption and intestinal transport, as well as the pathogenesis of gastrointestinal diseases (<xref rid="B97" ref-type="bibr">Sangild et al., 2014</xref>). All these characteristics contribute to the development of superior models of human conditions (<xref rid="B51" ref-type="bibr">Kuzmuk and Schook, 2011</xref>).</p><p>The choice between outbred or inbred strains can have a significant impact on research outcomes (<xref rid="B30" ref-type="bibr">Festing, 2014</xref>). While, outbred strains may be better suited for quantitative trait loci studies, experiments addressing mechanistic aspects would benefit from the use of inbred strains (<xref rid="B14" ref-type="bibr">Chia et al., 2005</xref>). Some minipig breeds are already established for specific applications due to their unique characteristics (<bold>Table <xref ref-type="table" rid="T1">1</xref></bold>). Pigs have also been used for testing new therapies, devices, and efficacy and safety of new drugs prior to human trials. For instance, a novel endovascular chemotherapy filter, designed to reduce circulatory drug excess <italic>in vitro</italic>, was successfully tested in pigs (<xref rid="B79" ref-type="bibr">Patel et al., 2014</xref>). As well, a new method for pediatric liver transplantation was validated using pigs (<xref rid="B56" ref-type="bibr">Leal et al., 2015</xref>). Regarding pharmacokinetic and cytotoxic tests, pigs have been used for testing topical skin formulations (<xref rid="B69" ref-type="bibr">Mitra et al., 2015</xref>), and are considered a better choice compared to dogs for the study of drugs that are metabolized by the aldehyde oxidase (AOX1), <italic>N</italic>-acetyltransferase (NAT1 or NAT2) or cytochrome (CYP2C9-like) enzymes (<xref rid="B18" ref-type="bibr">Dalgaard, 2014</xref>).</p><table-wrap id="T1" position="float"><label>Table 1</label><caption><p>Characteristics and applications of minipig breeds for the study of human conditions.</p></caption><table frame="hsides" rules="groups" cellspacing="5" cellpadding="5"><thead><tr><th valign="top" align="left" rowspan="1" colspan="1">Parameter</th><th valign="top" align="left" rowspan="1" colspan="1">Yucatan</th><th valign="top" align="left" rowspan="1" colspan="1">Gottingen</th><th valign="top" align="left" rowspan="1" colspan="1">Hanford</th><th valign="top" align="left" rowspan="1" colspan="1">Sinclair/Minnesota</th></tr></thead><tbody><tr><td valign="top" align="left" rowspan="1" colspan="1">Adult body size (kg)</td><td valign="top" align="left" rowspan="1" colspan="1">70–83</td><td valign="top" align="left" rowspan="1" colspan="1">~45</td><td valign="top" align="left" rowspan="1" colspan="1">80–95</td><td valign="top" align="left" rowspan="1" colspan="1">55–70</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Average litter size</td><td valign="top" align="left" rowspan="1" colspan="1">6</td><td valign="top" align="left" rowspan="1" colspan="1">6.5</td><td valign="top" align="left" rowspan="1" colspan="1">6.7</td><td valign="top" align="left" rowspan="1" colspan="1">7.2</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Age to puberty (months)</td><td valign="top" align="left" rowspan="1" colspan="1">4–6</td><td valign="top" align="left" rowspan="1" colspan="1">3–5</td><td valign="top" align="left" rowspan="1" colspan="1">4–6</td><td valign="top" align="left" rowspan="1" colspan="1">4–6</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Genetic background</td><td valign="top" align="left" rowspan="1" colspan="1">Purebred</td><td valign="top" align="left" rowspan="1" colspan="1">Outbred</td><td valign="top" align="left" rowspan="1" colspan="1">Outbred</td><td valign="top" align="left" rowspan="1" colspan="1">Outbred</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Cloning</td><td valign="top" align="left" rowspan="1" colspan="1">somatic cell nuclear transfer (SCNT; <xref rid="B26" ref-type="bibr">Estrada et al., 2008</xref>)</td><td valign="top" align="left" rowspan="1" colspan="1">SCNT (<xref rid="B114" ref-type="bibr">Wakai et al., 2008</xref>)</td><td valign="top" align="left" rowspan="1" colspan="1">Information not available</td><td valign="top" align="left" rowspan="1" colspan="1">SCNT (<xref rid="B22" ref-type="bibr">Do et al., 2012</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Transgenics</td><td valign="top" align="left" rowspan="1" colspan="1">Homologous recombination<break></break><italic>BRCA1</italic> (breast cancer susceptibility gene 1) – gene knockout by rAAV – model for breast cancer (<xref rid="B64" ref-type="bibr">Luo et al., 2011</xref>, <xref rid="B63" ref-type="bibr">2012</xref>)<sup>∗</sup><break></break>Introduction of missense mutation via rAAV – <italic>TP53</italic> gene – cancer cells (<xref rid="B102" ref-type="bibr">Sieren et al., 2014</xref>)<break></break>Introduction of nonsense mutation via rAAV – <italic>SCN5A</italic> gene – cardiac arrhythmia (<xref rid="B78" ref-type="bibr">Park et al., 2015</xref>)</td><td valign="top" align="left" rowspan="1" colspan="1">Homologous recombination<break></break><italic>BRCA1</italic> (breast cancer susceptibility gene 1) – gene knockout by rAAV – model for breast cancer (<xref rid="B63" ref-type="bibr">Luo et al., 2012</xref>)<sup>†</sup><break></break>rAAV vectors encoding GFP (<xref rid="B48" ref-type="bibr">Kornum et al., 2010</xref>)</td><td valign="top" align="left" rowspan="1" colspan="1">Information not available</td><td valign="top" align="left" rowspan="1" colspan="1">ZFN – mono and biallelic knockout pigs – <italic>CMAH</italic> gene – xenoantigen involved in the rejection phenomenon (<xref rid="B52" ref-type="bibr">Kwon et al., 2013</xref>)<break></break>TALEN – biallelic modified pigs – <italic>RAG2</italic> gene – immune system (<xref rid="B57" ref-type="bibr">Lee et al., 2014</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Applications</td><td valign="top" align="left" rowspan="1" colspan="1">Wound healing (<xref rid="B23" ref-type="bibr">Eggleston et al., 2000</xref>)<break></break>Cardiovascular model for ventricular septal defect (VSD; <xref rid="B108" ref-type="bibr">Swindle et al., 1990</xref>)<break></break>Metabolic Disorder (<xref rid="B84" ref-type="bibr">Phillips et al., 1982</xref>)</td><td valign="top" align="left" rowspan="1" colspan="1">Toxicity Studies (<xref rid="B6" ref-type="bibr">Bollen and Ellegaard, 1997</xref>; <xref rid="B113" ref-type="bibr">van Mierlo et al., 2013</xref>)<break></break>Skin pharmacokinetics tests (<xref rid="B69" ref-type="bibr">Mitra et al., 2015</xref>)<break></break>Metabolic Syndrome (<xref rid="B42" ref-type="bibr">Johansen et al., 2001</xref>)<break></break>Neurodegenerative disease – Parkinson Model (<xref rid="B5" ref-type="bibr">Bjarkam et al., 2008</xref>)<break></break>Obesity (<xref rid="B15" ref-type="bibr">Christoffersen et al., 2013</xref>)<break></break>Heart failure (<xref rid="B100" ref-type="bibr">Schuleri et al., 2008</xref>)</td><td valign="top" align="left" rowspan="1" colspan="1">Dermal studies – toxicology (<xref rid="B58" ref-type="bibr">Leigh et al., 2012</xref>)<break></break>Wound healing (<xref rid="B90" ref-type="bibr">Reger et al., 1999</xref>)<break></break>Surgery training (<xref rid="B89" ref-type="bibr">Purohit et al., 1993</xref>)<break></break>Tests of new therapies in tissue regeneration (<xref rid="B112" ref-type="bibr">Van Dyke et al., 2015</xref>)</td><td valign="top" align="left" rowspan="1" colspan="1">Oncology (malignant spontaneously regression melanoma; <xref rid="B76" ref-type="bibr">Oxenhandler et al., 1979</xref>)<break></break>Dermatology – skin depigmentation (<xref rid="B68" ref-type="bibr">Millikan et al., 1974</xref>)<break></break>Models of human alcoholism (<xref rid="B20" ref-type="bibr">Dexter et al., 1976</xref>)<break></break>Pediatric hypothyroidism (<xref rid="B110" ref-type="bibr">Tank et al., 2013</xref>)</td></tr></tbody></table><table-wrap-foot><attrib><italic><sup>∗</sup>The animals died 18 days after birth.</italic></attrib><attrib><italic><sup>†</sup>Cloned animals were not yet born at the time of publication.</italic></attrib></table-wrap-foot></table-wrap><p>In general, there is low incidence of naturally occurring pathologies described in pigs. The reason for this is twofold. First, human intervention by way of selective breeding has eliminated genes that increased disease susceptibility. Second, the majority of the domestic farm pigs are slaughtered at a young age (< 6 months old), precluding the detection of late onset diseases such as cancer. On the other hand, Vietnamese potbellied minipigs raised as companion animals do reach old ages. Indeed, a retrospective study found a variety of neoplasms with widespread metastases in these pigs of advanced age (~11 years; <xref rid="B73" ref-type="bibr">Newman and Rohrbach, 2012</xref>). The most common malignances found included hepatic and intestinal carcinomas, and uterine and ovarian smooth muscle tumors (<xref rid="B73" ref-type="bibr">Newman and Rohrbach, 2012</xref>).</p><p>Occurrence of malignant spontaneously regressing melanomas has been described in Sinclair minipigs (<xref rid="B68" ref-type="bibr">Millikan et al., 1974</xref>; <xref rid="B76" ref-type="bibr">Oxenhandler et al., 1979</xref>). Selective interbreeding, by removing animals with red coat color that do not develop the lesions, increased the frequency of tumor formation in these selected minipigs (<xref rid="B68" ref-type="bibr">Millikan et al., 1974</xref>). The tumors appear from birth and culminate in skin depigmentation after tumor regression showing a phenotype similar to human vitiligo (<xref rid="B68" ref-type="bibr">Millikan et al., 1974</xref>). Studies conducted in these minipigs have shown decreased telomerase activity during melanoma regression (<xref rid="B80" ref-type="bibr">Pathak et al., 2000</xref>), which has also been observed by inhibiting telomerase activity in human melanoma cells (<xref rid="B12" ref-type="bibr">Burchett et al., 2014</xref>). Therefore, these minipigs may represent a useful model to study malignant melanomas because the tumors appear spontaneously and then either regress or grow progressively and metastasize similarly to human melanomas (<xref rid="B76" ref-type="bibr">Oxenhandler et al., 1979</xref>).</p><p>Another example of a naturally occurring condition in pigs is the dwarf phenotype, caused by a single amino acid change in the α1 chain of type X collagen (<xref rid="B74" ref-type="bibr">Nielsen et al., 2000</xref>). The <italic>COL10A1</italic> gene, which encodes type X collagen, is expressed in hypertrophic chondrocytes during endochondral ossification. In humans, an amino acid variation in the same position of the type X collagen protein has been shown to be the cause of Schmid metaphyseal chondrodysplasia (SMCD), a mild skeletal disorder associated with dwarfism (<xref rid="B115" ref-type="bibr">Warman et al., 1993</xref>). Since mice lacking type X collagen do not develop abnormalities in long bone development (<xref rid="B93" ref-type="bibr">Rosati et al., 1994</xref>), pigs represent a better animal model of human SMCD.</p><p>Another naturally occurring disease observed in Yucatan minipigs mimics human ventricular septal defect (VSD; <xref rid="B108" ref-type="bibr">Swindle et al., 1990</xref>). The VSD in pigs can be observed in fetal stages similar to the congenital anomaly in humans, and can be used for the study of new methods of diagnosis or therapies (<xref rid="B108" ref-type="bibr">Swindle et al., 1990</xref>; <xref rid="B4" ref-type="bibr">Amin et al., 2006</xref>).</p><p>Despite a number of natural occurring pig phenotypes that resemble human diseases, for most of human pathologies it is difficult to find representative animal models in nature. Thus, manipulation of diet, use of drugs and/or surgeries has been necessary to generate appropriate models. For example, minipig models for Type I diabetes were induced via administration of streptozotocin or alloxan to selectively destroy insulin-producing cells (<xref rid="B85" ref-type="bibr">Phillips et al., 1980</xref>; <xref rid="B54" ref-type="bibr">Larsen et al., 2002</xref>). High-energy diets in young minipigs lead to the development of obesity and metabolic syndromes, with increased visceral fat deposition, glucose intolerance, decreased insulin sensitivity, and higher levels of blood cholesterol and triglycerides, which progress to Type 2 Diabetes mellitus (<xref rid="B120" ref-type="bibr">Xi et al., 2004</xref>; <xref rid="B72" ref-type="bibr">Neeb et al., 2010</xref>; <xref rid="B47" ref-type="bibr">Koopmans and Schuurman, 2015</xref>). Other chemicals have been used to induce cellular dysregulation and damage in pigs including the administration of <italic>N</italic>-nitrosodiethylamine to produce a liver cancer model (<xref rid="B61" ref-type="bibr">Li et al., 2006</xref>).</p></sec><sec><title>Use of Engineered Pigs in Biomedical Research</title><p>Genetically modified animals have been instrumental in advancing our understanding of gene function and significance of inappropriate gene expression in metabolic malfunction in mammals. Genome editing holds great promise in generating these models, and has already permitted the rapid development of new pig models of several human diseases (<xref rid="B91" ref-type="bibr">Rogers et al., 2008</xref>; <xref rid="B88" ref-type="bibr">Prather et al., 2013</xref>; <xref rid="B36" ref-type="bibr">Hai et al., 2014</xref>; <xref rid="B21" ref-type="bibr">Dicks, 2015</xref>).</p><p>The cystic fibrosis (CF) model is an example of genetically engineered pigs created by targeted inactivation of the cystic fibrosis transmembrane conductance regulator (<italic>CFTR</italic>) gene (<xref rid="B91" ref-type="bibr">Rogers et al., 2008</xref>). The resulting pigs exhibit clinical features and disease progression consistent with those observed in CF infants. In contrast, inactivation of the <italic>CFTR</italic> gene in mice did not produce the comorbidities typically observed in human CF patients (<xref rid="B103" ref-type="bibr">Snouwaert et al., 1992</xref>).</p><p>Advanced reproductive technologies, such as somatic cell nuclear transfer (SCNT), can now be routinely applied to large animal species, including minipigs. Minipigs of different breeds have been cloned from different cell types, including genetically modified cells (<xref rid="B26" ref-type="bibr">Estrada et al., 2008</xref>; <xref rid="B50" ref-type="bibr">Kurome et al., 2008</xref>; <xref rid="B114" ref-type="bibr">Wakai et al., 2008</xref>; <xref rid="B121" ref-type="bibr">Zhao et al., 2009</xref>). In addition SCNT offers the possibility of creating isogenic and immunocompatible animals from the same cell line. Importantly, models of severe disorders can be generated from engineered cultured cells without the need of breeding sick animals. The sequencing of the pig genome is another key development in the production of gene-modified pigs in the post-genomic era (<xref rid="B98" ref-type="bibr">Schook et al., 2015a</xref>). Genome editing techniques, including zinc finger nucleases (ZFN), transcription activator-like effector nucleases (TALEN), and clustered, regularly interspaced, short palindromic repeats (CRISPR) together with CRISPR associated (Cas) nucleases (CRISPR/Cas), now allow the precise manipulation of gene sequences in germ, embryonic and somatic cells (<xref rid="B37" ref-type="bibr">Hauschild et al., 2011</xref>; <xref rid="B13" ref-type="bibr">Carlson et al., 2012</xref>; <xref rid="B16" ref-type="bibr">Cong et al., 2013</xref>; <xref rid="B36" ref-type="bibr">Hai et al., 2014</xref>; <xref rid="B118" ref-type="bibr">Whitworth et al., 2014</xref>; <xref rid="B21" ref-type="bibr">Dicks, 2015</xref>). Among these methods, the CRISPR/Cas9 system is emerging as the method of choice because it permits gene editing to be accomplished in only one step by injecting both the specific guide RNAs and endonuclease into zygotes (<xref rid="B36" ref-type="bibr">Hai et al., 2014</xref>; <xref rid="B118" ref-type="bibr">Whitworth et al., 2014</xref>).</p><p>Another example of human disease that has the potential to be studied in genetically engineered pigs is heart arrhythmias (<xref rid="B78" ref-type="bibr">Park et al., 2015</xref>). Mutations in the <italic>SCN5A</italic> gene, which encodes a subunit of the cardiac sodium channel Na<sub>v</sub>1.5 required for excitability and conduction in the myocardium, were found in patients with Bruguda syndrome (<xref rid="B38" ref-type="bibr">Hedley et al., 2009</xref>). <italic>SCN5A<sup>E558X/+</sup></italic> engineered Yucatan minipigs with reduced expression of the sodium channel Na<sub>v</sub>1.5 have been created and these animals exhibit conduction abnormalities and susceptibility to ventricular arrhythmias (<xref rid="B78" ref-type="bibr">Park et al., 2015</xref>). There has also been considerable interest in genetically modified pig strains suitable for xenotransplantation. Most research into the development of appropriate xenotransplantation strains focused on addressing hyperacute rejection, which is initiated rapidly and involves preformed natural human antibodies and the complement system (<xref rid="B17" ref-type="bibr">Cooper et al., 2002</xref>). This has been possible by targeting cell surface antigens such as α-1,3 galactosyltransferase (<xref rid="B70" ref-type="bibr">Miyagawa et al., 2001</xref>; <xref rid="B53" ref-type="bibr">Lai et al., 2002</xref>; <xref rid="B83" ref-type="bibr">Phelps et al., 2003</xref>; <xref rid="B109" ref-type="bibr">Takahagi et al., 2005</xref>) or complement regulatory proteins such as human decay accelerating factor (<xref rid="B71" ref-type="bibr">Murakami et al., 2002</xref>). The pigs made deficient of α-1,3 galactosyltransferase have contributed to the reduction of immunogenicity of donor tissue/organs (<xref rid="B83" ref-type="bibr">Phelps et al., 2003</xref>). Transgenic pigs expressing antibodies against cytotoxic T-cell lymphocyte antigen receptor, a cell-mediated immune response suppressor, were also developed (<xref rid="B82" ref-type="bibr">Phelps et al., 2009</xref>).</p><p>A pig model for the human familial adenomatous polyposis was generated by inactivation of the adenomatous polyposis coli (<italic>APC</italic>) gene (<xref rid="B31" ref-type="bibr">Flisikowska et al., 2012</xref>). Mice lacking the <italic>APC</italic> gene exhibit non-metastatic neoplasias only in the small intestine (<xref rid="B105" ref-type="bibr">Su et al., 1992</xref>). However, the pig model of colon and rectal cancer reproduces the human features of the disease, which includes the development of polyps spread along the whole large bowel in young animals. A candidate gene for the development of breast and ovarian cancer models is the breast cancer-associated gene 1 (<italic>BRCA1</italic>), which has been manipulated in both Yucatan and Göttingen cells, but lines of modified minipigs remain to be produced (<xref rid="B64" ref-type="bibr">Luo et al., 2011</xref>, <xref rid="B63" ref-type="bibr">2012</xref>). The <italic>TP53</italic> gene, which encodes the tumor suppressor protein p53 and is the most commonly observed suppressed gene in human tumors, was found to be mutated in Li-Fraumeni patients having increased risk to develop multiple types of cancers (<xref rid="B33" ref-type="bibr">Gonzalez et al., 2009</xref>). Suppression of p53 in mesenchymal stem cells derived from pig bone marrow exhibits chemoresistance <italic>in vitro</italic> (<xref rid="B59" ref-type="bibr">Leuchs et al., 2012</xref>). Mutation of <italic>TP53</italic> gene in Yucatan minipigs resulted in development of lymphomas and osteogenic tumors (<xref rid="B102" ref-type="bibr">Sieren et al., 2014</xref>). More recently, a new engineered pig strain termed “oncopig” was developed, which promises inducible formation of a wide variety of cancers that are potentially novel platforms for research and therapeutics development (<xref rid="B99" ref-type="bibr">Schook et al., 2015b</xref>). These examples illustrate the potential of genetically engineered pigs as robust models for the study of human pathologies that are not well represented in small laboratory animal species.</p></sec><sec><title>Improving the Usefulness of Pigs in Biomedical Research</title><p>Rodents have been the choice animal model for basic research, but are not always suitable for translational research due to marked differences in size, lifespan as well as metabolic, anatomical, and physiological discrepancies. On the other hand, the pig is more closely related to humans in terms of these parameters (<xref rid="B107" ref-type="bibr">Swindle et al., 2012</xref>) and, therefore, is better suited for recapitulation of human diseases. Indeed, the use of the pig in translational research is increasingly gaining acceptance (<bold>Figure <xref ref-type="fig" rid="F1">1C</xref></bold>). Dogs and non-human primates have traditionally been used for this purpose, but rising ethical concerns have reduced their favor and increased demand for alternatives (<xref rid="B107" ref-type="bibr">Swindle et al., 2012</xref>). The number of peer-reviewed papers describing the use of pigs as biomedical models has risen eightfold over the past 30 years (<bold>Figure <xref ref-type="fig" rid="F1">1B</xref></bold>). Already, the pig has become well established in many areas of research and training. For instance, in the past 20 years the pig has replaced the dog as a model for surgical training and has also gained FDA approval for the testing of surgical implantation devices intended for human use (<xref rid="B107" ref-type="bibr">Swindle et al., 2012</xref>; <xref rid="B98" ref-type="bibr">Schook et al., 2015a</xref>). Minipig models, which are much smaller in size compared to the domestic farm breeds, offer lower operating costs compared to other large animal models and also reduce the concern of ethical acceptance given the already widespread use of pigs in agriculture (<xref rid="B6" ref-type="bibr">Bollen and Ellegaard, 1997</xref>; <xref rid="B107" ref-type="bibr">Swindle et al., 2012</xref>).</p><p>Pigs offer many exciting applications, including stem cell research, tissue engineering and xenotransplantation. Although incredible advances in transgenic pigs harboring various engineered alterations designed to minimize graft versus host rejection (<xref rid="B53" ref-type="bibr">Lai et al., 2002</xref>; <xref rid="B83" ref-type="bibr">Phelps et al., 2003</xref>, <xref rid="B82" ref-type="bibr">2009</xref>; <xref rid="B44" ref-type="bibr">Klose et al., 2005</xref>; <xref rid="B109" ref-type="bibr">Takahagi et al., 2005</xref>; <xref rid="B37" ref-type="bibr">Hauschild et al., 2011</xref>; <xref rid="B81" ref-type="bibr">Petersen et al., 2011</xref>; <xref rid="B40" ref-type="bibr">Jeong et al., 2013</xref>), much work remains to be accomplished since multiple genes need to be manipulated given the various types of tissue rejection reactions (<xref rid="B109" ref-type="bibr">Takahagi et al., 2005</xref>; <xref rid="B119" ref-type="bibr">Whyte and Prather, 2011</xref>; <xref rid="B40" ref-type="bibr">Jeong et al., 2013</xref>). Porcine induced pluripotent stem cells (iPSCs) have been produced (<xref rid="B25" ref-type="bibr">Esteban et al., 2009</xref>) and chimeric pigs were generated using iPSC (<xref rid="B116" ref-type="bibr">West et al., 2010</xref>, <xref rid="B117" ref-type="bibr">2011</xref>). This is highly relevant since study of porcine iPSCs have eventual human applications (<xref rid="B25" ref-type="bibr">Esteban et al., 2009</xref>), such as cell-based therapies. However, the mechanisms of cellular reprogramming, directed cell differentiation and species-specific cell culture requirements necessitate further investigation (<xref rid="B28" ref-type="bibr">Ezashi et al., 2012</xref>). The International Society for Stem Cell Research has indicated in their guidelines for translational use that validation must occur in both small and large animal models (<xref rid="B2" ref-type="bibr">Aigner et al., 2010</xref>). Tissue repair is another potential application of engineered pig models. Cartilage tissue grafts have been created using chondrocytes isolated from infant minipigs (<xref rid="B19" ref-type="bibr">Deponti et al., 2014</xref>), and mandibular condyle grafts have been generated from Yucatan minipig adipose-derived mesenchymal stem cells (<xref rid="B1" ref-type="bibr">Abukawa et al., 2003</xref>). There has also been successful regeneration of bone defects using engineered bone graft tissues in minipig models (<xref rid="B34" ref-type="bibr">Gröger et al., 2003</xref>). If custom donor transgenic minipig strains can be created, this could open the doors to other engineered tissue replacements for human uses. For example, the use of blastocyst complementation and pluripotent stem cells has been applied to direct the development of otherwise missing organs in pigs (<xref rid="B65" ref-type="bibr">Matsunari et al., 2013</xref>). This has increased the hope that it may one day be possible to create non-immunogenic donor organs in pigs using human iPSCs (<xref rid="B65" ref-type="bibr">Matsunari et al., 2013</xref>; <xref rid="B29" ref-type="bibr">Feng et al., 2015</xref>). Finally, similarities in the porcine and human immune system have sparked interest in vaccine development and efficacy testing in pigs (<xref rid="B67" ref-type="bibr">Meurens et al., 2012</xref>).</p><p>The completion of the porcine genome project in 2012 has further facilitated the use of pigs in research. Data from this project has enabled the comparative analysis of genetic sequences and development of the necessary tools to create and validate targeted genetic alterations in the porcine genome (<xref rid="B35" ref-type="bibr">Gun and Kues, 2014</xref>; <xref rid="B98" ref-type="bibr">Schook et al., 2015a</xref>). In addition, the development of RNASeq technology has facilitated transcriptome analysis, which further improves our ability to identify important targets related to certain phenotypic traits (<xref rid="B92" ref-type="bibr">Ropka-Molik et al., 2014</xref>). Other recent achievements in the pig include the use of inducible or conditional systems to control transgene expression (<xref rid="B49" ref-type="bibr">Kues et al., 2006</xref>; <xref rid="B45" ref-type="bibr">Klymiuk et al., 2012</xref>), and tissue-specific expression of the Cre recombinase (<xref rid="B60" ref-type="bibr">Li et al., 2009</xref>; <xref rid="B62" ref-type="bibr">Luo et al., 2014</xref>). These advances will ensure the continued development of various pig strains for research, similar to what has already been accomplished in mice.</p></sec><sec><title>Summary</title><p>It is clear that the use of the pig as a biomedical model is increasingly gaining approval due to physiopathological similarities with humans. However, some obstacles remain to be overcome in order to realize the full potential of the porcine species in developing new diagnostic and therapeutic approaches. Despite the sequencing of the porcine genome, full annotation has yet to be completed. This is essential to facilitate interrogation of the pig genome and investigation of less characterized genes. Efforts to develop a complete porcine proteome map as well as epigenome map are currently underway (<xref rid="B67" ref-type="bibr">Meurens et al., 2012</xref>; <xref rid="B98" ref-type="bibr">Schook et al., 2015a</xref>). These databases are necessary to understand disease pathogenesis (<xref rid="B67" ref-type="bibr">Meurens et al., 2012</xref>; <xref rid="B98" ref-type="bibr">Schook et al., 2015a</xref>). Moreover, the availability of both inbred and outbred breeds of minipigs extends the utility of these species as a viable large animal model. Continuing refinements and adaptation of technologies for genome editing, cell/tissue-specific gene targeting strategies, stem cells and somatic cell cloning will further facilitate the creation of specialized pig strains for biomedical research.</p></sec><sec><title>Conflict of Interest Statement</title><p>The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.</p></sec></body><back><ack><p>Research in our laboratories is funded by grants from the Natural Sciences and Engineering Research Council of Canada (to VB and to LA). KG is supported by a scholarship from the Science without Borders Program of the Brazilian Coordination for the Improvement of Higher Education Personnel (CAPES). WG is supported by a scholarship from the Brazilian National Council for Scientific and Technological Development (CNPq). 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