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. 2024 Sep 10;35(4):537–543. doi: 10.1007/s00335-024-10068-x

Commentary: The International Mouse Phenotyping Consortium: high-throughput in vivo functional annotation of the mammalian genome

K C Kent Lloyd 1,2,✉
PMCID: PMC11522054  PMID: 39254744

Abstract

The International Mouse Phenotyping Consortium (IMPC) is a worldwide effort producing and phenotyping knockout mouse lines to expose the pathophysiological roles of all genes in human diseases and make mice and data available and accessible to the global research community. It has created new knowledge on the function of thousands of genes for which little to anything was known. This new knowledge has informed the genetic basis of rare diseases, posited gene product influences on common diseases, influenced research on targeted therapies, revealed functional pleiotropy, essentiality, and sexual dimorphism, and many more insights into the role of genes in health and disease. Its scientific contributions have been many and widespread, however there remain thousands of “dark” genes yet to be illuminated. Nearing the end of its current funding cycle, IMPC is at a crossroads. The vision forward is clear, the path to proceed less so.

Every so often, a widening gap in knowledge, resources, and capabilities becomes so insurmountable for merely one group or even a single country to overcome, yet too critical for transformative innovation to disregard. Not long ago, the potential for genomics to resolve diagnostic odysseys, inform targeted therapies, and design prevention strategies for human diseases was hindered by the lack of holistic approaches to define the in vivo biological function of every gene in the mammalian genome (Hirschhorn and Daly 2005). Successfully overcoming this formidable obstacle to expeditiously translate the promise of genomic medicine into clinical practice would require an audacious plan to rapidly yet reliably uncover the pathophysiological roles of all genes in human diseases.

Conceived from a globally-shared vision (Austin et al. 2004; Auwerx et al. 2004), the International Mouse Phenotyping Consortium (IMPC) represents a groundbreaking, paradigm-shifting leap in the field of genetics and biomedical research. Self-assembled as a collectively-governed consortium of 21 academic research institutions across 15 countries on 5 continents, the IMPC aims to create a comprehensive catalog of mammalian gene function that is freely available and equally accessible to the global research community. Inspired by publications announcing the sequencing of the human (Lander et al. 2001; Venter et al. 2001) and then mouse (Mouse Genome Sequencing Consortium 2002) genomes, the IMPC emerged as the logical next step following the International Knockout Mouse Consortium (IKMC) which produced gene-targeted embryonic stem (ES) cells for nearly the entire mouse genome (International Mouse Knockout Consortium 2007). But more importantly, the IMPC was also motivated by the slow pace of progress resulting from limited and narrowly focused approaches to study gene function in vivo (Stoeger et al. 2018). Nearly all studies to that point were hypothesis-testing, focusing on incremental efforts that only partially annotated the function of a small number of well-characterized genes (Edwards et al. 2011) or “popular” gene sets (Eppig et al. 2011), typically in male mice only and often on ill-described genetic backgrounds (Perrin 2014). Within this rubric, grant applications posing hypotheses-generating experiments to unveil the function of understudied or overlooked genes were unlikely to pass peer review to successfully secure funding. To address the neglected “dark” coding genome and reveal new insights into heretofore unknown genetic associations and causes of disease, in 2011 the IMPC was established to reveal the function of every human orthogonal gene in the mouse genome (Brown and Moore 2012). Its ambitious goal was simple yet daunting: take an unbiased, systematic, broad-based, disease-agnostic approach to phenotype cohorts of male and female mice on a single, inbred genetic background (C57BL/6N) and associate analytical findings to human biology and disease mechanisms (Brown et al. 2009).

Similar to the challenges posed by the human genome sequencing project, the scale, technology, and complexity of resources, knowledge, and expertise needed to achieve the IMPC goal made international collaboration essential. Participating IMPC institutions received substantial funding from government agencies, research institutions, and philanthropic organizations, including the United States National Institutes of Health (NIH), European Union Horizon 2020, the Medical Research Council (MRC) and Wellcome Sanger Institute United Kingdom, Helmholtz Munich and the German Center for Diabetes Research (DZD), the French National Centre for Scientific Research (CNRS), the National Institute of Health and Medical Research (INSERM), and the Agence Nationale de la Recherche (ANR), Canadian Institutes of Health Research (CIHR) and Genome Canada, the Czech Academy of Sciences and the Ministry of Education, Youth and Sports of the Czech Republic, the Japanese Institute of Physical and Chemical Research (RIKEN) Japan, the National Key R&D program of China, and others. To date, those investments have resulted in the production of 9594 unique knockout mouse lines, of which 8901 have been phenotyped, generating over 30 million data points and images that have revealed 106,511 statistically-significant adult and embryo phenotype calls. Even more importantly, 1311 knockout lines for mouse genes with a human ortholog exhibit phenotypes associated with human disease, with many more expected (Cacheiro et al. 2024).

Initially, mouse lines were derived from IKMC-produced embryonic stem (ES) cells expressing either a complete null (Valenzuela et al. 2003) or “knockout first” conditional, loxP-flanked allele (Pettitt et al. 2009; Skarnes et al. 2011; Birling et al. 2021) and a LacZ reporter. More recently, knockouts have been created using CRISPR/Cas9 in mouse embryos to delete critical exons essential to gene function (Peterson and Murray 2022). Once produced, mice undergo a standardized, high-throughput phenotyping pipeline of tests and procedures covering a wide range of biological systems, including neurological (e.g., open field), metabolic (e.g., glucose tolerance test, body fat), cardiovascular (e.g., ECG), hematological (e.g., complete blood count), renal (e.g., blood urea nitrogen), musculoskeletal (e.g., X-ray), immunological (e.g., cytokines), reproductive (e.g., fertility), special senses (e.g., auditory brainstem response), and more (Brown et al. 2009; Mallon et al. 2008). Data and images are gathered under standard operating procedures and rigorous quality control measures (e.g., contemporary wildtype control mice) that are strictly adhered to by all participating IMPC Centers, ensuring consistent and accurate experimental outcomes (Kurbatova et al. 2015).

All test results are analyzed, curated, and posted online at www.impc.org where they are freely available to view, explore, and download (Groza et al. 2023). The IMPC employs robust bioinformatic and statistical methods to ensure experimental reliability and reproducibility. Beyond revealing previously unknown gene function, this extensive, broad-based analytical platform has uncovered scientifically significant features, including sexual dimorphism (Karp et al. 2017), pleiotropy (Muñoz-Fuentes et al. 2022), embryo lethality and neonatal subviability (Dickinson et al. 2016), and aging effects (publication pending) among homozygous and heterozygous gene knockout lines. This robust dataset is an invaluable resource, offering researchers a growing wealth of information that can be used to explore gene function and its implications for human health (Birling et al., 2021; Meehan et al. 2017). Indeed, the IMPC project has led to significant new scientific knowledge and insight into “rare” human Mendelian diseases, comparative genomics, drug discovery, and target development (Cacheiro et al. 2020; Cacheiro et al. 2022). For example, the IMPC has uncovered new genetic pathways and potential drug targets for a variety of conditions, including cardiomyopathies (Spielmann et al. 2022), schizophrenia (Garrett et al. 2024), ciliopathies (Higgins et al. 2022), pain (Wotton et al. 2022), osteoporosis (Swam et al. 2020), sleep disorders (Zhang et al. 2020), metabolic diseases (Rozman et al. 2018), deafness (Bowl et al. 2017), developmental defects (Dickinson et al. 2016), ocular disorders (Chee et al. 2023), dermatopathology (Moore et al. 2019), and diseases in other animal species (Muñoz-Fuentes et al. 2018). Newer and intriguing insights are sure to come.

IMPC data, resources, and expertise have been utilized by the worldwide research community contributing to a growing base of knowledge on genes and disease. Over two decades, an estimated 47,797 researchers at 1815 institutions in 99 countries have used IKMC and/or IMPC generated ES cells, mice, and/or data to publish 7281 papers in 764 scientific journals.1 Researchers have placed orders for more than 6000 IMPC mouse lines deposited in distribution repositories around the world, including the Mutant Mouse Resource and Research Center (MMRRC) in the United States (Amos-Landgraf et al. 2022), the European Mouse Mutant Archive (EMMA) in the European Union (Ali Khan et al. 2023), and the Asian Mouse Mutagenesis Resource Association (AMMRA) in the Asia Pacific (Chin et al. 2022), all of which are further described in their own articles published in this Special Issue. Interest in the latest information on IMPC lines continues, with over 18,000 research scientists registered for accounts and expressing interest in mouse lines and data at the MMRRC alone. In addition, the IMPC has played a crucial role in training the next generation of research scientists. Through workshops, conferences, and collaborative projects, the IMPC has provided valuable training opportunities for young scientists from diverse backgrounds, helping to build dedicated capacity and unique capability in the field of genetics and biomedical research using live mouse models. Further, investment in the IMPC has created a collaborative, internationally-coordinated group of highly reputable centers filled with expert scientists, experienced staff, and rigorous pipelines ready and prepared to produce and phenotype mouse models of human disease for future in vivo studies of functional genomics.

By 2027 when the current round of funding expires, the IMPC will have produced and phenotyped 11,846 knockout mouse lines representing ~ 60% of the human orthologous genome in the mouse.2 Although this progress over a short timeline has been phenomenal, 7328 orthologous genes will remain to be studied before IMPC can claim “mission accomplished”. Yet as of today, a plan to complete this goal has not been articulated. Foundering so close to success would not only be a disappointment scientifically, but a disservice to the community. Imagine if the human genome project had called off its trailblazing efforts after sequencing just 14 of the 23 pairs of chromosomes, leaving ~ 40% of the human genome undone.

But the impact of failing to deliver a complete and comprehensive catalog of mammalian gene function goes far beyond just an accounting of missing genes. Not only would the consequences of an incomplete phenotyping dataset be gaps in our understanding of gene function, the potential roles of many unstudied “dark” genes impacting mammalian biology and human disease would remain undiscovered, development of enhanced diagnostic tools would be delayed, publicly available databases that rely on IMPC data for comprehensive gene function information would become obsolete, and discovery of new targeted drug therapies would be hindered.

These shortfalls are not inevitable as long as the momentum, expertise, and processes invested in to date are not allowed to fizzle out. The IMPC has proven its scientific value as an unmatched powerhouse discovering new and essential knowledge about the mammalian genome…its capability, capacity, and will to define in vivo gene function is indisputable and indispensable. Unfortunately, IMPCs path to complete its vision of a comprehensive understanding of the biological function of all human orthologous genes in mice is less clear. Nevertheless, there is a way forward. First, curating the remaining genes will determine those with little, no, or ambiguous phenotypic information to inform a rationale for high-throughput production and systematic phenotyping of knockout mice. Second, engaging the scientific community on next steps will be key to making informed decisions on genomic loci to target, alleles to produce, and testing strategies to pursue. Third, establishing a roadmap, business plan, and timeline for a production and phenotyping strategy that maximizes the scientific value and research benefit of annotating the remaining genes will facilitate enabling discussions amongst international funding sources to collaborate on a sustainable financial commitment.

Challenging yes, and yet I have hope. The IMPC has made remarkable contributions to our understanding of gene function and its implications for human health. Through its comprehensive, rigorous, and collaborative approach to illuminating the “dark genome”, the IMPC has advanced translational research, shortened diagnostic odysseys for patients, facilitated drug discovery, and inspired new targeted therapeutics. Despite technical, financial, and logistical challenges inherent in a project of this vision and scale, the IMPC continues to probe the boundaries of biomedical research, offering new insights into the genetic basis of rare diseases.

The IMPC must continue to push beyond the protein coding genome and apply in vivo functional annotation to comprehensively decipher variation in function of enhancers, silencers, promoters, and insulators in the non-coding genome, systematically interrogate epigenomic regulation of gene expression, broadly incorporate large language models and artificial intelligence to find linkages between single-cell analyses and in vivo function, strategically explore polygenic effects on common diseases, and effectively translate functional biological knowledge of genetic variants to clinical knowledge and practice (Lloyd et al. 2020). If it does so, the IMPC will undoubtedly continue to shape the landscape of genetics and biomedicine, drive scientific discovery, and contribute to improvements in human health.

Acknowledgements

The author would like to acknowledge all the scientists, staff, students, and technicians at the 21 research institutions in 15 countries that participate in the International Mouse Phenotyping Consortium. The author also acknowledges funding from the National Institutes of Health, Division of Program Coordination, Planning, and Strategic Initiatives, Office of Research Infrastructure Programs, Division of Comparative Medicine (UM1OD023221 and U42OD012210).

Author contributions

The primary and corresponding author conceived of and wrote the manuscript.

Declarations

Conflict of interest

The author is funded by an NIH grant (UM1OD023221) to the Davis-Toronto-Collaborative-Consortium (DTCC) which supports participation in the International Mouse Phenotyping Consortium (IMPC).

Footnotes

1

data derived from Web of Science, InCites, and Scopus analysis of 7281 publications listed at www.mousephenotype.org/data/publications.

2

unpublished analysis by Kevin Peterson (The Jackson Laboratory) of mouse-human orthologs at www.informatics.jax.org/mgihome/homepages/stats/all_stats.shtml) compared to mouse genes completed and projected to finish at IMPC by 2027 at https://www.gentar.org/tracker.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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