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The chemokine receptor CXCR4 and its ligand CXCL12 regulate oculomotor nerve development; mice with loss of either molecule have oculomotor synkinesis. In a consanguineous family with congenital ptosis and elevation of the ptotic eyelid with ipsilateral abduction, we identified a co-segregating homozygous missense variant (c.772G&gt;A) in ACKR3, which encodes an atypical chemokine receptor that binds CXCL12 and functions as a scavenger receptor, regulating levels of CXCL12 available for CXCR4 signaling. The mutant protein (p.V258M) is expressed and traffics to the cell surface but has a lower binding affinity for CXCL12. Mice with loss of Ackr3 have variable phenotypes that include misrouting of the oculomotor and abducens nerves. All embryos show oculomotor nerve misrouting, ranging from complete misprojection in the midbrain, to aberrant peripheral branching, to a thin nerve, which aberrantly innervates the lateral rectus (as seen in Duane syndrome). The abducens nerve phenotype ranges from complete absence, to aberrant projections within the orbit, to a normal trajectory. Loss of ACKR3 in the midbrain leads to downregulation of CXCR4 protein, consistent with reports that excess CXCL12 causes ligand-induced degradation of CXCR4. Correspondingly, excess CXCL12 applied to ex vivo oculomotor slices causes axon misrouting, similar to inhibition of CXCR4. Thus, ACKR3, through its regulation of CXCL12 levels, is an important regulator of axon guidance in the oculomotor system; complete loss causes oculomotor synkinesis in mice, while reduced function causes oculomotor synkinesis in humans.<\/jats:p>","DOI":"10.1093\/hmg\/ddz137","type":"journal-article","created":{"date-parts":[[2019,6,11]],"date-time":"2019-06-11T15:11:19Z","timestamp":1560265879000},"page":"3113-3125","source":"Crossref","is-referenced-by-count":18,"title":["Decreased ACKR3 (CXCR7) function causes oculomotor synkinesis in mice and humans"],"prefix":"10.1093","volume":"28","author":[{"given":"Mary C","family":"Whitman","sequence":"first","affiliation":[{"name":"Department of Ophthalmology, Boston Children's Hospital, Boston, MA, USA"},{"name":"Department of Ophthalmology, Harvard Medical School, Boston, MA, USA"},{"name":"F.M. Kirby Neurobiology Center, Boston Children's Hospital, Boston, MA, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Noriko","family":"Miyake","sequence":"additional","affiliation":[{"name":"F.M. Kirby Neurobiology Center, Boston Children's Hospital, Boston, MA, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Elaine H","family":"Nguyen","sequence":"additional","affiliation":[{"name":"Department of Ophthalmology, Boston Children's Hospital, Boston, MA, USA"},{"name":"F.M. Kirby Neurobiology Center, Boston Children's Hospital, Boston, MA, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jessica L","family":"Bell","sequence":"additional","affiliation":[{"name":"Department of Ophthalmology, Boston Children's Hospital, Boston, MA, USA"},{"name":"F.M. Kirby Neurobiology Center, Boston Children's Hospital, Boston, MA, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Paola M","family":"Matos Ruiz","sequence":"additional","affiliation":[{"name":"F.M. Kirby Neurobiology Center, Boston Children's Hospital, Boston, MA, USA"},{"name":"Department of Neurology, Boston Children's Hospital, Boston, MA, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wai-Man","family":"Chan","sequence":"additional","affiliation":[{"name":"F.M. Kirby Neurobiology Center, Boston Children's Hospital, Boston, MA, USA"},{"name":"Department of Neurology, Boston Children's Hospital, Boston, MA, USA"},{"name":"Howard Hughes Medical Institute, Chevy Chase, MD, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Silvio Alessandro","family":"Di Gioia","sequence":"additional","affiliation":[{"name":"F.M. Kirby Neurobiology Center, Boston Children's Hospital, Boston, MA, USA"},{"name":"Department of Neurology, Boston Children's Hospital, Boston, MA, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nisha","family":"Mukherjee","sequence":"additional","affiliation":[{"name":"F.M. Kirby Neurobiology Center, Boston Children's Hospital, Boston, MA, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Brenda J","family":"Barry","sequence":"additional","affiliation":[{"name":"F.M. Kirby Neurobiology Center, Boston Children's Hospital, Boston, MA, USA"},{"name":"Department of Neurology, Boston Children's Hospital, Boston, MA, USA"},{"name":"Howard Hughes Medical Institute, Chevy Chase, MD, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"T M","family":"Bosley","sequence":"additional","affiliation":[{"name":"Department of Ophthalmology, King Khaled Eye Specialist Hospital, Riyadh, Saudi Arabia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Arif O","family":"Khan","sequence":"additional","affiliation":[{"name":"Division of Pediatric Ophthalmology, King Khaled Eye Specialist Hospital, Riyadh, Saudi Arabia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Elizabeth C","family":"Engle","sequence":"additional","affiliation":[{"name":"Department of Ophthalmology, Boston Children's Hospital, Boston, MA, USA"},{"name":"Department of Ophthalmology, Harvard Medical School, Boston, MA, USA"},{"name":"F.M. Kirby Neurobiology Center, Boston Children's Hospital, Boston, MA, USA"},{"name":"Department of Neurology, Boston Children's Hospital, Boston, MA, USA"},{"name":"Department of Neurology, Harvard Medical School, Boston, MA, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2019,6,18]]},"reference":[{"key":"2019091103382750000_ref1","doi-asserted-by":"crossref","first-page":"R37","DOI":"10.1093\/hmg\/ddx168","article-title":"Ocular congenital cranial dysinnervation disorders (CCDDs): insights into axon growth and guidance","volume":"26","author":"Whitman","year":"2017","journal-title":"Hum. Mol. Genet."},{"key":"2019091103382750000_ref2","doi-asserted-by":"crossref","first-page":"1664","DOI":"10.1172\/JCI88502","article-title":"Mutant alpha2-chimaerin signals via bidirectional ephrin pathways in Duane retraction syndrome","volume":"127","author":"Nugent","year":"2017","journal-title":"J. Clin. 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