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7/10/2016 Don’t edit the human germ line : Nature News & Comment

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Don’t edit the human germ line

12 March 2015

Heritable human genetic modifications pose serious risks, and the therapeutic benefits are tenuous, warn EdwardLanphier, Fyodor Urnov and colleagues.

It is thought that studies involving the use of genome-editing tools to modify the DNA of human embryos will be publishedshortly1.

There are grave concerns regarding the ethical and safety implications of this research. There is also fear of the negative impactit could have on important work involving the use of genome-editing techniques in somatic (non-reproductive) cells.

We are all involved in this latter area of work. One of us (F.U.) helped to develop the first genome-editing technology, zinc-fingernucleases2 (ZFNs), and is now senior scientist at the company developing them, Sangamo BioSciences of Richmond, California.The Alliance for Regenerative Medicine (ARM;; in which E.L., M.W. and S.E.H. are involved), is an international organization thatrepresents more than 200 life-sciences companies, research institutions, non-profit organizations, patient-advocacy groups andinvestors focused on developing and commercializing therapeutics, including those involving genome editing.

Edward Lanphier, Fyodor Urnov, Sarah Ehlen Haecker, Michael Werner & Joanna Smolenski

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“The precise effects ofgenetic modification to anembryo may be impossibleto know until after birth.”

Genome-editing technologies may offer a powerful approach to treat many human diseases,

including HIV/AIDS, haemophilia, sickle-cell anaemia and several forms of cancer3. All

techniques currently in various stages of clinical development focus on modifying the genetic

material of somatic cells, such as T cells (a type of white blood cell). These are not designed to

affect sperm or eggs.

In our view, genome editing in human embryos using current technologies could have

unpredictable effects on future generations. This makes it dangerous and ethically

unacceptable. Such research could be exploited for non-therapeutic modifications. We are

concerned that a public outcry about such an ethical breach could hinder a promising area of

therapeutic development, namely making genetic changes that cannot be inherited.

At this early stage, scientists should agree not to modify the DNA of human reproductive cells. Should a truly compelling case

ever arise for the therapeutic benefit of germ line modification, we encourage an open discussion around the appropriate course

of action.

Editing toolsGenome editing of human somatic cells aims to repair or eliminate a mutation that could cause disease. The premise is that

corrective changes to a sufficient number of cells carrying the mutation — in which the genetic fixes would last the lifetimes of the

modified cells and their progeny — could provide a ‘one and done’ curative treatment for patients.

For instance, ZFNs are DNA-binding proteins that can be engineered to induce a double-strand break in a section of DNA. Such

molecular scissors enable researchers to ‘knock out’ specific genes, repair a mutation or incorporate a new stretch of DNA into a

selected location.

Sangamo BioSciences is conducting clinical trials to evaluate an application of genome editing as a potential ‘functional cure’ for

HIV/AIDS4. The hope is that intravenous infusion of modified T cells will enable patients to stop taking anti retroviral drugs. A

phase I trial in patients with β-thalassaemia — a genetic blood disorder caused by insufficient haemoglobin production — is

scheduled to begin this year.

The newest addition to the genome-editing arsenal is CRISPR/Cas9, a bacteria-derived system that uses RNA molecules that

recognize specific human DNA sequences. The RNAs act as guides, matching the nuclease to corresponding locations in the

human genome. CRISPR/Cas9 is the simplest genome-editing tool to work with because it relies on RNA–DNA base pairing,

rather than the engineering of proteins that bind particular DNA sequences.

The CRISPR technique has dramatically expanded research on genome editing. But we

cannot imagine a situation in which its use in human embryos would offer a therapeutic

benefit over existing and developing methods. It would be difficult to control exactly how

many cells are modified. Increasing the dose of nuclease used would increase the likelihood

that the mutated gene will be corrected, but also raise the risk of cuts being made elsewhere

in the genome.

In an embryo, a nuclease may not necessarily cut both copies of the target gene, or the cell may start dividing before the

corrections are complete, resulting in a genetic mosaic. Studies using gene-editing in animals such as rats5, cattle6, sheep7 and

pigs8, indicate that it is possible to delete or disable genes in an embryo — a simpler process than actually correcting DNA

sequences — in onlysome of the cells.

The current ability to perform quality controls on only a subset of cells means that the precise effects of genetic modification to an



embryo may be impossible to know until after birth. Even then, potential problems may not surface for years. Established

methods, such as standard prenatal genetic diagnostics or in vitro fertilization (IVF) with the genetic profiling of embryos beforeimplantation, are much better options for parents who both carry the same mutation for a disease.

Legal casePatient safety is paramount among the arguments against modifying the human germ line (egg and sperm cells). If a mosaic

embryo is created, the embryo’s germ line may or may not carry the genetic alteration. But the use of CRISPR/Cas9 in human

embryos certainly makes onward human germline modification a possibility. Philosophically or ethically justifiable applications for

this technology — should any ever exist — are moot until it becomes possible to demonstrate safe outcomes and obtain

reproducible data over multiple generations.

Because of such concerns — as well as for serious ethical reasons — some countries discouraged or prohibited this type of

research a decade before the technical feasibility of germline modification was confirmed in rats in 2009 (ref. 9). (Today, around

40 countries discourage or ban it.)

Many countries do not have explicit legislation in place permitting or forbidding genetic engineering in humans — considering

such research experimental and not therapeutic (see go.nature.com/uvthmu). However, in nations with policies regarding

inheritable genetic modification, it has been prohibited by law or by measures having the force of law.

This consensus is most visible in western Europe, where 15 of 22 nations prohibit the modification of the germ line4. Although the

United States has not officially prohibited germline modification, the US National Institutes of Health’s Recombinant DNA Advisory

Committee explicitly states that it “will not at present entertain proposals for germ line alterations” (see go.nature.com/mgscb2).

In general, researchers who want to investigate the clinical uses of genetically engineered somatic cells must secure people’s

informed consent. In the United States, this takes place under the oversight of the Food and Drug Administration and the

Department of Health and Human Services. For research involving genetic modification of the germ line, it is unclear what

information would be needed — or obtainable — to adequately inform prospective parents of the risks, including to future

generations.

Many oppose germline modification on the grounds that permitting even unambiguously therapeutic interventions could start us

down a path towards non-therapeutic genetic enhancement. We share these concerns.

Dialogue neededTen years ago, the Genetics and Public Policy Center, now in Washington DC, brought together more than 80 experts from the

United States and Canada to consider the scientific and ethical consequences of genetically modifying the human germ line. Now

that the capability for human germline engineering has emerged, we urge the international scientific community to engage in this

type of dialogue. This is needed both to establish how to proceed in the immediate term, and to assess whether, and under what

circumstances — if any — future research involving genetic modification of human germ cells should take place. Such

discussions must include the public as well as experts and academics.

An excellent precedent for open, early discussion as new scientific capabilities emerge was set by the hearings, consultations

and reports involving scientists, bioethicists, regulators and the general public that preceded the UK government’s decision to

legalize mitochondrial DNA transfer in February. We are not, of course, making a comparison between the replacement of faulty

mitochondrial DNA in an egg or embryo with healthy DNA from a female donor and the use of genome-editing in human embryos.

In mitochondrial transfer, the aim is to prevent life-threatening diseases by replacing a known and tiny fraction of the overall

genome.

Key to all discussion and future research is making a clear distinction between genome editing in somatic cells and in germ cells.



Article PubMed ISI ChemPort



PubMed ChemPort

Article PubMed ChemPort

Article


A voluntary moratorium in the scientific community could be an effective way to discourage human germline modification and

raise public awareness of the difference between these two techniques. Legitimate concerns regarding the safety and ethical

impacts of germline editing must not impede the significant progress being made in the clinical development of approaches to

potentially cure serious debilitating diseases.

Nature 519, 410–411 (26 March 2015) doi:10.1038/519410a

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References

1. Regalado, A. MIT Tech. Rev. http://go.nature.com/2n2nfl (2015).

Show context

2. Urnov, F. D., Rebar, E. J., Holmes, M. C., Zhang. H. S. & Gregory, P. D. Nature Rev. Genet. 11, 636–646 (2010).Show context

3. Carroll, D. Annu. Rev. Biochem. 83, 409–439 (2014).Show context

4. Tebas, P. et al. N. Engl. J. Med. 370, 901–910 (2014).Show context

5. Yoshimi, K., Kaneko, T., Voigt, B. & Mashimo, T. Nature Commun. 5, 4240 (2014).Show context

6. Heo, T. Y. et al. Stem Cells Dev. 24, 393–402 (2015).Show context

7. Han, H. et al. Front. Agr. Sci. Eng. 1, 2–5 (2014).Show context

8. Kang, Q. et al. in Proc. 10th World Congr. Genet. Appl. Livestock Prod. http://go.nature.com/6mtz2d (2014).

Show context

9. Geurts, A. M. Science. 325, 433 (2009).Show context

Related stories and links

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Novartis secures first CRISPR pharma collaborations30 January 2015

Regulation: Sell help not hope16 June 2014

365 days: Nature's 1018 December 2013

A slippery slope to human germline modification

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11 comments Subscribe to comments

09 July 2013Cloning debate: Stem-cell researchers must stay engaged

12 June 2013

Author information

Affiliations

Edward Lanphier is president and chief executive officer of Sangamo BioSciences in Richmond, California, USA, and

chairman of the Alliance for Regenerative Medicine in Washington DC, USA.

Fyodor Urnov is senior scientist at Sangamo BioSciences in Richmond, California, USA.

Sarah Ehlen Haecker is director of technology sections at the Alliance for Regenerative Medicine in Washington DC,

USA.

Michael Werner is executive director of the Alliance for Regenerative Medicine in Washington DC, USA.

Joanna Smolenski is a PhD student in philosophy at the Graduate Center of the City University of New York, New York,

USA.

Competing financial interests

E.L. and F.U. are employees of Sangamo BioSciences, Inc.

Corresponding author

Correspondence to: Edward Lanphier

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mark miller • 2015-04-21 11:24 PM

"Such research could be exploited for non-therapeutic modifications. We are concerned that a public outcry about such anethical breach could hinder a promising area of therapeutic development, namely making genetic changes that cannot beinherited." The same could be said of nuclear fission. Any nation that wants it badly enough has gotten it. This technologydoesn't require state actors to fully exploit it. So the probability that it will _not_ be used for non-therapeutic modificationsis negligibly close to zero. Further more, as most of us suspect and will soon know, the Chinese have a vastly differentattitude toward the prospect of human self-improvement at the germ line level. Any outcry from Westerners will be dulynoted and utterly ignored. So, then, what is the concern _really_ of the authors? That the technology will not be effectiveor, as I suspect, that the technology will be too effective, laying to rest once and for all the "tabula rasa" narrative of theLeft?

Dan Gibbs • 2015-03-27 11:15 PM

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footer-margin:.5in;; mso-paper-source:0;; div.WordSection1 page:WordSection1;; --> I feel driven to point out a glaring

omission in this whole discussion on human germ-line editing, which is the incorrect and very dangerous assumption that

we as scientists and medical practitioners really do understand and are the best able to fully consider all of the ethical

consequences of CRISPR based gene editing for genetic disease in the germ-line of humans. Fundamentally, the majority

of scientists and medical practitioners (particularly in the US) are not willing or able to talk openly about the endemic bias

and discrimination that currently exists against people with genetic differences, in particular those with heritable

intellectual disabilities. Society in general views these vulnerable individuals as having intrinsically less value than

“normally developing” people. This innate bias and discrimination exists here, today. Our scientific and medical community

is no different, but does have more responsibility to address this failure openly and consider it fully when considering the

ethics of new technologies . The impact of this intrinsic bias and discrimination is woefully understudied. Those who have

conducted research document serious and often fatal consequences to the heath and wellbeing of these individuals as a

direct result of endemic bias and discriminatory attitudes in the biomedical and healthcare communities. All individuals

with genetic differences, many of whom are still thought of as having diseases to be fixed, are unique and valuable human

beings who contribute so much to the richness and much needed compassion that often is lacking in our lives and society,

yet who are clearly considered targets for “correction” by this technology. Any attempt to have a discussion on the

consequences of the CRISPR technology underlying human germ-line gene editing, without directly addressing the innate

biases of all involved is unethical. To continue to have this debate and look to legislation;; based solely on the viewpoint of

scientists without the direct and intimate involvement of individuals with genetic differences and their advocates has been

and continues to be completely unethical. Especially given the fact that no open discussion about ethics occurred when

this technology was under development or when initially published. The correct way is to first consider the ethics then do

the work, not the other way around. Below are the relevant references from a detailed search of PUBMED over the last 20

years (Keywords: Intellectual disability, discrimination, healthcare). Of the only 35 search results, 11 dealt directly with

healthcare discrimination against individuals with intellectual disabilities. Fundamentally, they all describe profound and

systematic discrimination against people with intellectual disabilities. Not one report came from the US. They conclude

that this systematic discrimination begins very early in life for those who differ from the norm, and prevents access to

adequate healthcare, as well as dramatically reducing the quality of care that they do receive. Children and adults with

intellectual disabilities were also identified by these studies as one of the MOST at-risk populations for suffering the

serious negative consequences of discrimination, not just in healthcare but in all areas. More so than groups

discriminated against on the basis of race, age, sex and gender. Even in the countries that have taken steps to investigate

this discrimination and propose solutions, the conclusion is that medical and social discrimination against people with

intellectual disabilities is still a major problem that needs much more effort to even begin to correct. Countries like the UK,

Canada, Mexico, Australia and Singapore have at least taken the first small steps by studying and acknowledging that



discrimination against such a vulnerable group exists. Our US healthcare system, government and scientific community isfailing even that basic responsibility. REFERENCES Discrimination and other barriers to accessing health care:perspectives of patients with mild and moderate intellectual disability and their carers. Ali A, Scior K, Ratti V, Strydom A,King M, Hassiotis A. PLoS One. 2013 Aug 12;;8(8):e70855. doi: 10.1371/journal.pone.0070855. eCollection 2013. Stigmaand restriction on the social life of families of children with intellectual disabilities in Vietnam. Ngo H, Shin JY, Nhan NV,Yang LH. Singapore Med J. 2012 Jul;;53(7):451-7. Validation of the attitudes toward intellectual disability: ATTIDquestionnaire. Morin D, Crocker AG, Beaulieu-Bergeron R, Caron J. J Intellect Disabil Res. 2013 Mar;;57(3):268-78. doi:10.1111/j.1365-2788.2012.01559.x. Epub 2012 Apr 25. Care adjustments for people with learning disabilities in hospitals.Blair J. Nurs Manag (Harrow). 2011 Dec;;18(8):21-4. Overcoming ignorance and stigma relating to intellectual disability inhealthcare: a potential solution. While AE, Clark LL. J Nurs Manag. 2010 Mar;;18(2):166-72. doi: 10.1111/j.1365-2834.2009.01039.x. Problems, problems: you are such a problem! Shaw S. J Intellect Disabil. 2009 Jun;;13(2):99-112. doi:10.1177/1744629509336484. The balance of power in therapeutic interactions with individuals who have intellectualdisabilities. Jahoda A, Selkirk M, Trower P, Pert C, Stenfert Kroese B, Dagnan D, Burford B. Br J Clin Psychol. 2009Mar;;48(Pt 1):63-77. doi: 10.1348/014466508X360746. Epub 2008 Oct 10. Attending to the health needs of people withintellectual disability: quality standards. O’Hara J. Salud Publica Mex. 2008;;50 Suppl 2:s154-9. Review. The experiencesof adults with intellectual disabilities and their carers in general hospitals: a focus group study. Gibbs SM, Brown MJ, MuirWJ. J Intellect Disabil Res. 2008 Dec;;52(12):1061-77. doi: 10.1111/j.1365-2788.2008.01057.x. Epub 2008 May 5.[Canadian mental health rights in an international perspective]. Weisstub DN, Arboleda-Flórez J. Sante Ment Que. 2006Spring;;31(1):19-46. French.

Paul Watson • 2015-04-14 06:59 PM

Engineering for increased prosociality would be likely to ameliorate the situation pointed out by Dan Gibbs, above --a wonderful side benefit to enhanced species sustainability. This also gives me the chance to emphasize thatengineering for increased prosociality and biophilia would involve providing (given needed research funding) geneticfixes for all "normal" humans. The fixes need to be pan-cultural, pan-ethnic, etc. We are dealing with species-typicaltraits that make virtually all of us not care enough about the welfare of other humans, not care enough aboutpollinators in crisis, etc., etc...

Paul Watson • 2015-03-24 06:36 PM

All the authors' concerns are totally valid, IMO, and I am strongly in favor of the moratorium, especially as regards germ-line genomic modifications. However, I think that as we ramp up our ethical discussion on this topic, we urgently andsoberly have to consider the following.

We are a congenitally unsustainable life form that causes untold suffering for fellow humans and countless other sentientbeings. Ponder this: all technologically powerful life forms across the cosmos, to render themselves sustainable, probablyhave had to stop natural selection, our ever active default eugenicist, from having its unhindered way with them,specifically in designing their brains and hence their emotions, moral deliberation processes, and their general grip onreality. We'll have to do the same to keep the human experiment running.

It's time we face the likelihood that, as we are genetically constituted, we will continue to be a ruthlessly tribal, resourceand power-grabbing, warring, extinction-bound species. Yes, we need to develop the strongest possible ethical andscientific framework for editing human genes. As part of this effort it is crucial that we consider our socioecologically graveand urgent situation.

Humans are amazing, wonderful creatures. But, there's a fact we must face, and now is the time. Having been designed



by natural selection, our unconscious, pan-cultural "prime directive" is to maximize individual lifetime inclusive fitness;; this

means that the unconscious drive to transmit our genes to future generations, using an incredible variety of direct and

indirect strategies, often including impressive albeit ruthlessly contingent, more or less parochial altruism, trumps and

"poisons everything." It is why we are so good at causing suffering for our fellow humans and the other creatures with

whom we "share" the Earth, all the while proceeding to cause a global, soon-to-be irreversible "Tragedy of the Commons."

It is why our heartfelt "real" higher values are expressed mainly in ways that directly and indirectly (e.g., via helping our

supporting in-group) attain fitness-enhancing goals.

Culture, that is, socioecological changes we come up with through the outputs of our naturally selected minds, seems

unlikely to save us, although innovative strategies obviously should be tried, along with less onerous epigenetic

engineering. However, the developing genetic editing tools that scientists and bioethicists so rightly worry about probably

are our principle long term way out of this trap. They offer up the miraculous and pivotal opportunity for humankind to

bring about a new age of "intentional evolution," ethically aimed at the rendering ourselves fundamentally more prosocial,

biophilic, and ecologically viable. These, I offer, are the traits that should be at the top of the list for "tuning up" via somatic

or germ-line editing.

mark miller • 2015-04-21 11:27 PM

Do you think any prospective moratorium will have more effect than, say, the Bush moratorium on stem cell

research? It will simply accelerate China's dominance in the field. Transglobal elites will happily consume the service

without regard to the flag it may be flying under. So in that light, by all means, I'm for a moratorium as well.

PJ Northway • 2015-03-20 04:47 PM

I call for a moratorium on moratoriums. There has been VERY little, if any, informed Public debate on ANY aspect of

Genetics, much less ground breaking germ line editing. There ARE serious ethical challenges inherent in the processes

and outcomes, but typically debate consists of pat answers and excuses, "We shouldn't play God" and that sort of thing.

We "play God" every, single day. We choose who has resources and who does not;; who goes to War and who does not;;

we experiment with the Climate, Earth, Air and Water almost daily. Genetic code is modified by a torrent of untested

chemicals and industrial processes and by-products. The Hallmark of the Anthropocene IS Human Experimentation on a

mass scale AND experimentation on Species that have no choice whatsoever.

Heeyoun Bunch • 2015-03-18 01:37 PM

In my knowledge, risks of inheriting an edited (deleted) chromosome/gene haven't been rigorously tested throughout

multiple generations. Editing embryonic cell may benefit that particular individual (if it is disposed to a certain, life-

threatening genetic disease) but there is no guarantee of not having destructive consequences or problems in a long run

from inheriting permanently modified genome. Considering the complexity of interwound cellular processes, editing a

genome seems to be 'taking a quick, easy way'---but we know that it is not always wise.

Stephen Wilson • 2015-03-16 06:52 PM

I am not a geneticist but a software professional and scientist. The genes-as-software parallel is widely cited but what's

not properly appreciated is the way software is verified. Complex software cannot be empirically tested and, I suggest,



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neither can the products of genetic editing. In software, it is received wisdom that most bugs result from imprudentchanges made to existing programs. Furthermore, editing one part of a program can have unpredictable and unboundedimpacts on any other part of the code. Input complexity means that all but the very simplest software is empiricallyuntestable. So mission critical software (like the implantable defibrillator code I used to work on) is always verified by acombination of methods, including unit testing, system testing, design review and painstaking code inspection. Becausemost problems come from human error, software excellence demands formal design and development processes, andhigh level programming languages, to preclude subtle errors that no amount of testing could ever hope to find. How manyof these software quality mechanisms are available to genetic engineers? Code inspection is moot when we don’t evenknow how genes normally interact with one another. Only recently was it found that junk DNA is not entirely junk.Geneticists obviously have an incomplete understanding of how genes interact. If we don't actually know how one "line" ofgenetic code impacts the rest of the "program", how can we possibly tell by inspection if an edited gene will interfere withthe "legacy" code? I'd say a moratorium is absolutely justified until such time as genetic "engineering" can rest oncomplete genetic science.

Bruce Bowen • 2015-03-13 11:04 PM

Once the techniques for converting somatic cells into germ cells is perfected, this whole argument will be moot.

Mike B • 2015-03-12 09:36 PM

Calling for a discussion is different than calling for a moratorium. A moratorium creates a paradox: don't do experimentson genome editing in germ cells until it can be proven (by experimentation) that it's safe to do experiments on genomeediting in germ cells. It seems what you are actually calling for is a discussion about the ethics of such research, alongwith tightly controlled experiments to elucidate the risks of genome editing in germ cells.

Paul Knoepfler • 2015-03-12 05:39 PM

The call for proactive discussion by diverse stakeholders seems sensible. Even though work toward heritable geneediting-based human genetic modification seems to be already ongoing in some quarters and its use may be inevitableraising the question of just how "proactive" these discussions would be, it is not too late for community-wide engagementto have major positive impact in charting the future course of research and implementation of this technology in humans.Readers may find this week's interview with George Church to be of interest,http://www.ipscell.com/2015/03/georgechurchinterview/, as his viewpoints are distinct from these authors in someinteresting ways that resonate.

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