A direct and melanopsin-dependent fetal light response regulates mouse eye development
Open accessAbstract
Vascular patterning is critical for organ function. In the eye, there is simultaneous regression of embryonic hyaloid vasculature (important to clear the optical path) and formation of the retinal vasculature (important for the high metabolic demands of retinal neurons). These events occur postnatally in the mouse. Here we have identified a light-response pathway that regulates both processes. We show that when mice are mutated in the gene (Opn4) for the atypical opsin melanopsin, or are dark-reared from late gestation, the hyaloid vessels are persistent at 8 days post-partum and the retinal vasculature overgrows. We provide evidence that these vascular anomalies are explained by a light-response pathway that suppresses retinal neuron number, limits hypoxia and, as a consequence, holds local expression of vascular endothelial growth factor (VEGFA) in check. We also show that the light response for this pathway occurs in late gestation at about embryonic day 16 and requires the photopigment in the fetus and not the mother. Measurements show that visceral cavity photon flux is probably sufficient to activate melanopsin-expressing retinal ganglion cells in the mouse fetus. These data thus show that light--the stimulus for function of the mature eye--is also critical in preparing the eye for vision by regulating retinal neuron number and initiating a series of events that ultimately pattern the ocular blood vessels.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
As fetuses develop, they become sensitive to light cues penetrating through the mother's abdomen.
“As fetuses develop, they become sensitive to light cues penetrating through the mother’s abdomen59.”
From Maternal and Early-Life Circadian Disruption Have Long-Lasting Negative Consequences on Offspring Development and Adult Behavior in Mice (2017) · cites this paper as [59]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
The biology of VEGF and its receptors
Ferrara, N., Gerber, H.-P., & LeCouter, J. (2003) · Nature Medicine · doi:10.1038/nm0603-669 · Cited by 9,591 · see citing works
Self-citationA robust and high-throughput Cre reporting and characterization system for the whole mouse brain
Madisen, L., Zwingman, T. A., Sunkin, S. M., Oh, S. W., Zariwala, H. A., Gu, H., Ng, L. L., Palmiter, R. D., Hawrylycz, M. J., Jones, A. R., et al. (2010) · Nature Neuroscience · doi:10.1038/nn.2467 · Cited by 6,907 · see citing works
VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia
Gerhardt, H., Golding, M., Fruttiger, M., Ruhrberg, C., Lundkvist, A., Abramsson, A., Jeltsch, M., Mitchell, C., Alitalo, K., Shima, D., et al. (2003) · The Journal of Cell Biology · doi:10.1083/jcb.200302047 · Cited by 2,894 · see citing works
Hattar, S., Liao, H.-W., Takao, M., Berson, D. M., & Yau, K.-W. (2002) · Science · doi:10.1126/science.1069609 · Cited by 2,734 · see citing works
Adamis, A. P., Miller, J. W., Bernal, M.-T., D’Amico, D. J., Folkman, J., Yeo, T.-K., & Yeo, K.-T. J. (1994) · American Journal of Ophthalmology · doi:10.1016/s0002-9394(14)75794-0 · Cited by 1,296 · see citing works
Melanopsin: An opsin in melanophores, brain, and eye
Provencio, I., Jiang, G., De Grip, W. J., Hayes, W. P., & Rollag, M. D. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.1.340 · Cited by 975 · see citing works
Melanopsin ( <i>Opn4</i> ) Requirement for Normal Light-Induced Circadian Phase Shifting
Panda, S., Sato, T. K., Castrucci, A. M., Rollag, M. D., DeGrip, W. J., Hogenesch, J. B., Provencio, I., & Kay, S. A. (2002) · Science · doi:10.1126/science.1076848 · Cited by 861 · see citing works
Connor, K. M., Krah, N. M., Dennison, R. J., Aderman, C. M., Chen, J., Guerin, K. I., Sapieha, P. S., Stahl, A., Willett, K. L., & Smith, L. E. H. (2009) · Nature Protocols · doi:10.1038/nprot.2009.187 · Cited by 742 · see citing works
Ecker, J. L., Dumitrescu, O. N., Wong, K. Y., Alam, N. M., Chen, S., LeGates, T. A., Renna, J. M., Prusky, G. T., Berson, D. M., & Hattar, S. S. (2010) · Neuron · doi:10.1016/j.neuron.2010.05.023 · Cited by 669 · see citing works
Development of the retinal vasculature
Fruttiger, M. (2007) · Angiogenesis · doi:10.1007/s10456-007-9065-1 · Cited by 510 · see citing works
Amacrine-Signaled Loss of Intrinsic Axon Growth Ability by Retinal Ganglion Cells
Goldberg, J. L., Klassen, M. P., Hua, Y., & Barres, B. A. (2002) · Science · doi:10.1126/science.1068428 · Cited by 488 · see citing works
Intrinsically Photosensitive Retinal Ganglion Cells
Do, M. T. H., & Yau, K. (2010) · Physiological Reviews · doi:10.1152/physrev.00013.2010 · Cited by 477 · see citing works
Deletion of vascular endothelial growth factor in myeloid cells accelerates tumorigenesis
Stockmann, C., Doedens, A. L., Weidemann, A., Zhang, N., Takeda, N., Greenberg, J. I., Cheresh, D. A., & Johnson, R. S. (2008) · Nature · doi:10.1038/nature07445 · Cited by 473 · see citing works
WNT7b mediates macrophage-induced programmed cell death in patterning of the vasculature
Lobov, I. B., Rao, S., Carroll, T. J., Vallance, J. E., Ito, M., Ondr, J. K., Kurup, S., Glass, D. A., Patel, M. S., Shu, W., et al. (2005) · Nature · doi:10.1038/nature03928 · Cited by 429 · see citing works
Self-citationDevelopment and pathology of the hyaloid, choroidal and retinal vasculature
Saint‐Geniez, M., & D'Amore, P. A. (2004) · The International Journal of Developmental Biology · doi:10.1387/ijdb.041895ms · Cited by 413 · see citing works
Lichtenberger, B. M., Tan, P. K., Niederleithner, H., Ferrara, N., Petzelbauer, P., & Sibilia, M. C. (2010) · Cell · doi:10.1016/j.cell.2009.12.046 · Cited by 356 · see citing works
Self-citationRowan, S., & Cepko, C. L. (2004) · Developmental Biology · doi:10.1016/j.ydbio.2004.03.039 · Cited by 326 · see citing works
Visual Stimulation Is Required for Refinement of ON and OFF Pathways in Postnatal Retina
Tian, N., & Copenhagen, D. R. (2003) · Neuron · doi:10.1016/s0896-6273(03)00389-1 · Cited by 304 · see citing works
Self-citationRegulation of angiogenesis by a non-canonical Wnt–Flt1 pathway in myeloid cells
Stefater, J. A., Lewkowich, I. P., Rao, S., Mariggi, G., Carpenter, A. C., Burr, A. R., Fan, J., Ajima, R., Molkentin, J. D., Williams, B. O., et al. (2011) · Nature · doi:10.1038/nature10085 · Cited by 274 · see citing works
Self-citationCortical and retinal defects caused by dosage-dependent reductions in VEGF-A paracrine signaling
Haigh, J. J., Morelli, P. I., Gerhardt, H., Haigh, K., Tsien, J., Damert, A., Miquerol, L., Mühlner, U., Klein, R., Ferrara, N., et al. (2003) · Developmental Biology · doi:10.1016/s0012-1606(03)00356-7 · Cited by 271 · see citing works
Self-citationPhysiologic Diversity and Development of Intrinsically Photosensitive Retinal Ganglion Cells
Tu, D. C., Zhang, D., Demas, J., Slutsky, E. B., Provencio, I., Holy, T. E., & Gelder, R. N. V. (2005) · Neuron · doi:10.1016/j.neuron.2005.09.031 · Cited by 236 · see citing works
Regression of the hyaloid vessels and pupillary membrane of the mouse
Ito, M., & Yoshioka, M. (1999) · Anatomy and Embryology · doi:10.1007/s004290050289 · Cited by 217 · see citing works
Melanopsin-Dependent Photoreception Provides Earliest Light Detection in the Mammalian Retina
Sekaran, S., Lupi, D., Jones, S. L., Sheely, C. J., Hattar, S. S., Yau, K., Lucas, R. J., Foster, F., & Hankins, M. W. (2005) · Current Biology · doi:10.1016/j.cub.2005.05.053 · Cited by 189 · see citing works
A Retinal Ganglion Cell That Can Signal Irradiance Continuously for 10 Hours
Wong, K. Y. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.1423-12.2012 · Cited by 158 · see citing works
Macrophages induce apoptosis in normal cells in vivo
Diez‐Roux, G., & Lang, R. A. (1997) · Development · doi:10.1242/dev.124.18.3633 · Cited by 154 · see citing works
Self-citationMelanopsin-dependent light avoidance in neonatal mice
Johnson, J., Wu, V., Donovan, M. H., Majumdar, S., Renterı́a, R. C., Porco, T. C., Gelder, R. N. V., & Copenhagen, D. R. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1008533107 · Cited by 147 · see citing works
Self-citationVEGF deprivation-induced apoptosis is a component of programmed capillary regression
Meeson, A. P., Argilla, M., Ko, K. A., Witte, L., & Lang, R. A. (1999) · Development · doi:10.1242/dev.126.7.1407 · Cited by 147 · see citing works
Self-citationExpression of opsin genes early in ocular development of humans and mice
Tarttelin, E. E., Bellingham, J., Bibb, L. C., Foster, F., Hankins, M. W., Gregory-Evans, K., Gregory, C. Y., Wells, D. J., & Lucas, R. J. (2003) · Experimental Eye Research · doi:10.1016/s0014-4835(02)00300-7 · Cited by 87 · see citing works
Kurihara, T., Kubota, Y., Ozawa, Y., Takubo, K., Noda, K., Simon, M. C., Johnson, R. S., Suematsu, M., Tsubota, K., Ishida, S., et al. (2010) · Development · doi:10.1242/dev.049015 · Cited by 74 · see citing works
The deletion of Math5 disrupts retinal blood vessel and glial development in mice
Edwards, M. M., McLeod, D. S., Li, R., Grebe, R. R., Bhutto, I. A., Mu, X., & Lutty, G. A. (2011) · Experimental Eye Research · doi:10.1016/j.exer.2011.12.005 · Cited by 59 · see citing works
Lange, C., Caprara, C., Tanimoto, N., Beck, S. C., Huber, G., Samardzija, M., Seeliger, M. W., & Grimm, C. (2010) · Neurobiology of Disease · doi:10.1016/j.nbd.2010.08.028 · Cited by 22 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Broad targeting of angiogenesis for cancer prevention and therapy
Wang, Z., Dabrosin, C., Yin, X., Fuster, M. M., Arreola, A., Rathmell, W. K., Generali, D., Nagaraju, G. P., El‐Rayes, B. F., Ribatti, D., et al. (2015) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2015.01.001 · Cited by 470 · see citing works
The Human Fetus Preferentially Engages with Face-like Visual Stimuli
Reid, V. M., Dunn, K., Young, R. J., Amu, J., Donovan, T., & Reissland, N. (2017) · Current Biology · doi:10.1016/j.cub.2017.05.044 · Cited by 421 · see citing works
Retinal vasculature development in health and disease
Selvam, S., Kumar, T., & Fruttiger, M. (2017) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2017.11.001 · Cited by 357 · see citing works
Melanopsin and the Intrinsically Photosensitive Retinal Ganglion Cells: Biophysics to Behavior
Do, M. T. H. (2019) · Neuron · doi:10.1016/j.neuron.2019.07.016 · Cited by 305 · see citing works
Mechanisms of Vessel Pruning and Regression
Korn, C., & Augustin, H. G. (2015) · Developmental Cell · doi:10.1016/j.devcel.2015.06.004 · Cited by 302 · see citing works
Retinal ganglion cell maps in the brain: implications for visual processing
Dhande, O. S., & Huberman, A. D. (2013) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2013.08.006 · Cited by 206 · see citing works
Joyal, J., Gantner, M. L., & Smith, L. E. H. (2017) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2017.11.002 · Cited by 186 · see citing works
Pathophysiology, screening and treatment of ROP: A multi-disciplinary perspective
Chan‐Ling, T., Gole, G. A., Quinn, G. E., Adamson, S. J., & Darlow, B. A. (2017) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2017.09.002 · Cited by 176 · see citing works
Diversity of intrinsically photosensitive retinal ganglion cells: circuits and functions
Aranda, M. L., & Schmidt, T. M. (2020) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-020-03641-5 · Cited by 164 · see citing works
The Role of Daylight for Humans: Gaps in Current Knowledge
Münch, M. Y., Wirz‐Justice, A., Brown, S. A., Kantermann, T., Martiny, K., Stefani, O., Vetter, C., Wright, K. P., Wulff, K., & Skene, D. J. (2020) · Clocks & Sleep · doi:10.3390/clockssleep2010008 · Cited by 157 · see citing works
Violet-light suppression of thermogenesis by opsin 5 hypothalamic neurons
Zhang, K. X., D’Souza, S., Upton, B. A., Kernodle, S., Vemaraju, S., Nayak, G., Gaitonde, K. D., Holt, A. L., Linne, C. D., Smith, A. N., et al. (2020) · Nature · doi:10.1038/s41586-020-2683-0 · Cited by 154 · see citing works
Self-citationUnconventional Roles of Opsins
Leung, N. Y., & Montell, C. (2017) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-100616-060432 · Cited by 157 · see citing works
Advances in understanding and management of retinopathy of prematurity
Hartnett, M. E. (2016) · Survey of Ophthalmology · doi:10.1016/j.survophthal.2016.12.004 · Cited by 148 · see citing works
Asymmetry of brain and behavior in animals: Its development, function, and human relevance
Rogers, L. J. (2014) · genesis · doi:10.1002/dvg.22741 · Cited by 145 · see citing works
Sonoda, T., Lee, S. K., Birnbaumer, L., & Schmidt, T. M. (2018) · Neuron · doi:10.1016/j.neuron.2018.06.032 · Cited by 137 · see citing works
Endothelial cell apoptosis in angiogenesis and vessel regression
Watson, E. L., Grant, Z. L., & Coultas, L. (2017) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-017-2577-y · Cited by 138 · see citing works
Melanopsin-Driven Light Adaptation in Mouse Vision
Allen, A. E., Storchi, R., Martial, F. P., Petersen, R. S., Montemurro, M. A., Brown, T. M., & Lucas, R. J. (2014) · Current Biology · doi:10.1016/j.cub.2014.09.015 · Cited by 132 · see citing works
Melanopsin mediates light-dependent relaxation in blood vessels
Sikka, G., Hussmann, G. P., Pandey, D., Cao, S., Hori, D., Park, J. T., Steppan, J., Kim, J. H., Barodka, V. M., Myers, A. C., et al. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1420258111 · Cited by 128 · see citing works
Melanopsin Tristability for Sustained and Broadband Phototransduction
Emanuel, A. J., & Do, M. T. H. (2015) · Neuron · doi:10.1016/j.neuron.2015.02.011 · Cited by 129 · see citing works
Perturbed neural activity disrupts cerebral angiogenesis during a postnatal critical period
Whiteus, C., Freitas, C., & Grutzendler, J. (2013) · Nature · doi:10.1038/nature12821 · Cited by 122 · see citing works
Current understanding of photophobia, visual networks and headaches
Noseda, R., Copenhagen, D. R., & Burstein, R. (2018) · Cephalalgia · doi:10.1177/0333102418784750 · Cited by 117 · see citing works
Self-citationAn opsin 5–dopamine pathway mediates light-dependent vascular development in the eye
Nguyen, M., Vemaraju, S., Nayak, G., Odaka, Y., Buhr, E. D., Alonzo, N., Tran, U., Batie, M. R., Upton, B. A., Darvas, M., et al. (2019) · Nature Cell Biology · doi:10.1038/s41556-019-0301-x · Cited by 113 · see citing works
Self-citationCui, Q., Ren, C., Sollars, P. J., Pickard, G. E., & So, K. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.11.002 · Cited by 110 · see citing works
A visual circuit uses complementary mechanisms to support transient and sustained pupil constriction
Keenan, W. T., Rupp, A. C., Ross, R., Somasundaram, P., Hiriyanna, S., Wu, Z., Badea, T. C., Robinson, P. R., Lowell, B. B., & Hattar, S. S. (2016) · eLife · doi:10.7554/elife.15392 · Cited by 102 · see citing works
Neuronal and glial regulation of CNS angiogenesis and barriergenesis
Biswas, S., Cottarelli, A., & Agalliu, D. (2020) · Development · doi:10.1242/dev.182279 · Cited by 107 · see citing works
Melanopsin Contributions to the Representation of Images in the Early Visual System
Allen, A. E., Storchi, R., Martial, F. P., Bedford, R. A., & Lucas, R. J. (2017) · Current Biology · doi:10.1016/j.cub.2017.04.046 · Cited by 104 · see citing works
Adaptive Thermogenesis in Mice Is Enhanced by Opsin 3-Dependent Adipocyte Light Sensing
Nayak, G., Zhang, K. X., Vemaraju, S., Odaka, Y., Buhr, E. D., Holt-Jones, A., Kernodle, S., Smith, A. N., Upton, B. A., D’Souza, S. P., et al. (2020) · Cell Reports · doi:10.1016/j.celrep.2019.12.043 · Cited by 98 · see citing works
Self-citationThe Retina and Other Light-sensitive Ocular Clocks
Besharse, J. C., & McMahon, D. G. (2016) · Journal of Biological Rhythms · doi:10.1177/0748730416642657 · Cited by 90 · see citing works
Chew, K. S., Renna, J. M., McNeill, D. S., Fernandez, D. C., Keenan, W. T., Thomsen, M. B., Ecker, J. L., Loevinsohn, G. S., VanDunk, C., Vicarel, D. C., et al. (2017) · eLife · doi:10.7554/elife.22861 · Cited by 86 · see citing works
Smarr, B. L., Grant, A. D., Perez, L., Zucker, I., & Kriegsfeld, L. J. (2017) · Scientific Reports · doi:10.1038/s41598-017-03406-4 · Cited by 86 · see citing works
VEGF is an autocrine/paracrine neuroprotective factor for injured retinal ganglion neurons
Froger, N., Matonti, F., Roubeix, C., Forster, V., Ivković, I., Brunel, N., Baudouin, C., Sahel, J., & Picaud, S. A. (2020) · Scientific Reports · doi:10.1038/s41598-020-68488-z · Cited by 86 · see citing works
Melanopsin retinal ganglion cells mediate light-promoted brain development
Hu, J., Shi, Y., Zhang, J., Huang, X., Wang, Q., Zhao, H., Shen, J., Chen, Z., Song, W., Zheng, P., et al. (2022) · Cell · doi:10.1016/j.cell.2022.07.009 · Cited by 83 · see citing works
Signalling by melanopsin (OPN4) expressing photosensitive retinal ganglion cells
Hughes, S., Jagannath, A., Rodgers, J., Hankins, M. W., Peirson, S. N., & Foster, F. (2016) · Eye · doi:10.1038/eye.2015.264 · Cited by 81 · see citing works
Variability of the Surface Area of the V1, V2, and V3 Maps in a Large Sample of Human Observers
Benson, N. C., Yoon, J. M. D., Forenzo, D., Engel, S. A., Kay, K., & Winawer, J. A. (2022) · Journal of Neuroscience · doi:10.1523/jneurosci.0690-21.2022 · Cited by 75 · see citing works
Light Prior to Eye Opening Promotes Retinal Waves and Eye-Specific Segregation
Tiriac, A., Smith, B. E., & Feller, M. B. (2018) · Neuron · doi:10.1016/j.neuron.2018.10.011 · Cited by 73 · see citing works
Enlightening the brain: Linking deep brain photoreception with behavior and physiology
Fernandes, A. M., Fero, K. C., Driever, W., & Burgess, H. A. (2013) · BioEssays · doi:10.1002/bies.201300034 · Cited by 70 · see citing works
Peripheral Sensory Neurons Expressing Melanopsin Respond to Light
Matynia, A., Nguyen, E. K., Sun, X., Blixt, F. W., Parikh, S., Kessler, J., Müller, L. P. D. S., Habib, S., Kim, P., Wang, Z. Z., et al. (2016) · Frontiers in Neural Circuits · doi:10.3389/fncir.2016.00060 · Cited by 69 · see citing works
Sewduth, R. N., Jaspard‐Vinassa, B., Peghaire, C. R., Guillabert, A., Franzl, N., Larrieu-Lahargue, F., Moreau, C., Fruttiger, M., Dufourcq, P., Couffinhal, T., et al. (2014) · Nature Communications · doi:10.1038/ncomms5832 · Cited by 67 · see citing works
An Expanding Role for Nonvisual Opsins in Extraocular Light Sensing Physiology
Andrabi, M., Upton, B. A., Lang, R. A., & Vemaraju, S. (2023) · Annual Review of Vision Science · doi:10.1146/annurev-vision-100820-094018 · Cited by 69 · see citing works
Self-citationEphrinB2 controls vessel pruning through STAT1-JNK3 signalling
Salvucci, O., Ohnuki, H., Maric, D., Hou, X., Li, X., Yoon, S. O., Segarra, M., Eberhart, C. G., Acker‐Palmer, A., & Tosato, G. (2015) · Nature Communications · doi:10.1038/ncomms7576 · Cited by 66 · see citing works
Sondereker, K. B., Stabio, M. E., & Renna, J. M. (2020) · The Journal of Comparative Neurology · doi:10.1002/cne.24873 · Cited by 63 · see citing works
Hartnett, M. E., Morrison, M. A., Smith, S. E., Yanovitch, T. L., Young, T. L., Colaizy, T. T., Momany, A. M., Dagle, J. M., Carlo, W. A., Clark, E., et al. (2014) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.14-14841 · Cited by 62 · see citing works
Clinical implications of the melanopsin-based non–image-forming visual system
Ksendzovsky, A., Pomeraniec, I. J., Zaghloul, K. A., Provencio, J. J., & Provencio, I. (2017) · Neurology · doi:10.1212/wnl.0000000000003761 · Cited by 60 · see citing works
Photoreceptor glucose metabolism determines normal retinal vascular growth
Fu, Z., Löfqvist, C., Liegl, R. G.-H., Wang, Z., Sun, Y., Gong, Y. Q., Liu, C., Meng, S. S., Burnim, S. B., Arellano, I. A., et al. (2017) · EMBO Molecular Medicine · doi:10.15252/emmm.201707966 · Cited by 60 · see citing works
Developmental regression of hyaloid vasculature is triggered by neurons
Yoshikawa, Y., Yamada, T., Tai-Nagara, I., Okabe, K., Kitagawa, Y., Ema, M., & Kubota, Y. (2016) · The Journal of Experimental Medicine · doi:10.1084/jem.20151966 · Cited by 57 · see citing works
Schroeder, M. M., Harrison, K. R., Jaeckel, E. R., Berger, H. N., Zhao, X., Flannery, M. P., Pierre, E. S., Pateqi, N., Jachimska, A., Chervenak, A. P., et al. (2018) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2018.00203 · Cited by 55 · see citing works
Storchi, R., Milosavljevic, N., Eleftheriou, C. G., Martial, F. P., Orlowska‐Feuer, P., Bedford, R. A., Brown, T. M., Montemurro, M. A., Petersen, R. S., & Lucas, R. J. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1505274112 · Cited by 55 · see citing works
Control of cerebrovascular patterning by neural activity during postnatal development
Lacoste, B., & Gu, C. (2015) · Mechanisms of Development · doi:10.1016/j.mod.2015.06.003 · Cited by 55 · see citing works
Pathophysiology of Retinopathy of Prematurity
Hartnett, M. E. (2023) · Annual Review of Vision Science · doi:10.1146/annurev-vision-093022-021420 · Cited by 54 · see citing works
Melanopsin-Encoded Response Properties of Intrinsically Photosensitive Retinal Ganglion Cells
Mure, L. S., Hatori, M., Zhu, Q., Demas, J. A., Kim, I., Nayak, S. K., & Panda, S. (2016) · Neuron · doi:10.1016/j.neuron.2016.04.016 · Cited by 53 · see citing works
Watson, E. L., Koenig, M. N., Grant, Z. L., Whitehead, L. W., Trounson, E., Dewson, G., & Coultas, L. (2016) · Development · doi:10.1242/dev.137513 · Cited by 53 · see citing works
Lucas, R. J., Allen, A. E., Brainard, G. C., Brown, T. M., Dauchy, R. T., Didikoğlu, A., Do, M. T. H., Gaskill, B. N., Hattar, S. S., Hawkins, P., et al. (2024) · PLoS Biology · doi:10.1371/journal.pbio.3002535 · Cited by 55 · see citing works
Evolutionary Constraint on Visual and Nonvisual Mammalian Opsins
Upton, B. A., Díaz, N. M., Gordon, S. A., Gelder, R. N. V., Buhr, E. D., & Lang, R. A. (2021) · Journal of Biological Rhythms · doi:10.1177/0748730421999870 · Cited by 52 · see citing works
Self-citationLight-dependent pathways for dopaminergic amacrine cell development and function
Munteanu, T., Noronha, K. J., Leung, A. C., Pan, S., Lucas, J. A., & Schmidt, T. M. (2018) · eLife · doi:10.7554/elife.39866 · Cited by 51 · see citing works
Fan, J., Ponferrada, V. G., Sato, T., Vemaraju, S., Fruttiger, M., Gerhardt, H., Ferrara, N., & Lang, R. A. (2013) · Development · doi:10.1242/dev.097949 · Cited by 48 · see citing works
Self-citationRetinal ganglion cell interactions shape the developing mammalian visual system
D’Souza, S. P., & Lang, R. A. (2020) · Development · doi:10.1242/dev.196535 · Cited by 45 · see citing works
Self-citationArroyo, D. A., Kirkby, L. A., & Feller, M. B. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.0572-16.2016 · Cited by 45 · see citing works
The potential influence of LED lighting on mental illness
Bauer, M., Glenn, T., Monteith, S., Gottlieb, J. F., Ritter, P. S., Geddes, J. R., & Whybrow, P. C. (2017) · The World Journal of Biological Psychiatry · doi:10.1080/15622975.2017.1417639 · Cited by 45 · see citing works
Photoperiod-Induced Neuroplasticity in the Circadian System
Porcu, A., Riddle, M., Dulcis, D., & Welsh, D. K. (2018) · Neural Plasticity · doi:10.1155/2018/5147585 · Cited by 43 · see citing works
From remodeling to quiescence: The transformation of the vascular network
Ouarné, M., Pena, A., & Franco, C. A. (2021) · Cells and Development · doi:10.1016/j.cdev.2021.203735 · Cited by 42 · see citing works
Hazelhoff, E. M., Dudink, J., Meijer, J. H., & Kervezee, L. (2021) · Frontiers in Neuroscience · doi:10.3389/fnins.2021.634034 · Cited by 41 · see citing works
Nayak, G., Odaka, Y., Prasad, V., Solano, A. F., Yeo, E.-J., Vemaraju, S., Molkentin, J. D., Trumpp, A., Williams, B. O., Rao, S., et al. (2018) · Development · doi:10.1242/dev.154898 · Cited by 38 · see citing works
Self-citationMelanopsin Retinal Ganglion Cells Regulate Cone Photoreceptor Lamination in the Mouse Retina
Tufford, A., Onyak, J. R., Sondereker, K. B., Lucas, J. A., Earley, A. M., Mattar, P. A., Hattar, S. S., Schmidt, T. M., Renna, J. M., & Cayouette, M. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.04.086 · Cited by 38 · see citing works
Opsin3 Downregulation Induces Apoptosis of Human Epidermal Melanocytes via Mitochondrial Pathway
Wang, Y., Lan, Y., & Lü, H. (2019) · Photochemistry and Photobiology · doi:10.1111/php.13178 · Cited by 38 · see citing works
Melanopsin-Derived Visual Responses under Light Adapted Conditions in the Mouse dLGN
Davis, K. E., Eleftheriou, C. G., Allen, A. E., Procyk, C. A., & Lucas, R. J. (2015) · PLoS ONE · doi:10.1371/journal.pone.0123424 · Cited by 38 · see citing works
Circadian Perinatal Photoperiod Has Enduring Effects on Retinal Dopamine and Visual Function
Jackson, C. R., Capozzi, M. E., Dai, H., & McMahon, D. G. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.4887-13.2014 · Cited by 36 · see citing works
Brain and Cognitive Development
Stiles, J., Brown, T. T., Haist, F., & Jernigan, T. L. (2015) · Wiley eBooks · doi:10.1002/9781118963418.childpsy202 · Cited by 37 · see citing works
A Cre Mouse Line for Probing Irradiance- and Direction-Encoding Retinal Networks
Sabbah, S., Berg, D. J., Papendorp, C. M., Briggman, K. L., & Berson, D. M. (2017) · eNeuro · doi:10.1523/eneuro.0065-17.2017 · Cited by 35 · see citing works
Biswas, S., Shahriar, S., Bachay, G., Arvanitis, P., Jamoul, D., Brunken, W. J., & Agalliu, D. (2024) · Neuron · doi:10.1016/j.neuron.2024.03.011 · Cited by 34 · see citing works
Sexton, T. J., Bleckert, A., Turner, M. H., & Gelder, R. N. V. (2015) · Neural Development · doi:10.1186/s13064-015-0042-x · Cited by 34 · see citing works
Light-Induced Covalent Buffer Adducts to Histidine in a Model Protein
Lei, M., Quan, C. P., Wang, Y. J., Kao, Y., & Schöneich, C. (2018) · Pharmaceutical Research · doi:10.1007/s11095-017-2339-4 · Cited by 33 · see citing works
Length of Day during Early Gestation as a Predictor of Risk for Severe Retinopathy of Prematurity
Yang, M. B., Rao, S., Copenhagen, D. R., & Lang, R. A. (2013) · Ophthalmology · doi:10.1016/j.ophtha.2013.07.051 · Cited by 33 · see citing works
Self-citationAbsence of lymphatic vessels in the developing human sclera
Schlereth, S. L., Neuser, B., Herwig‐Carl, M. C., Müller, A. M., Koch, K. R., Reitsamer, H. A., Schroedl, F., Cursiefen, C., & Heindl, L. M. (2014) · Experimental Eye Research · doi:10.1016/j.exer.2014.06.010 · Cited by 33 · see citing works
The Influence of Light on Temperature Preference in Drosophila
Head, L. M., Tang, X., Hayley, S. E., Goda, T., Umezaki, Y., Chang, E. C., Leslie, J. R., Fujiwara, M., Garrity, P., & Hamada, F. N. (2015) · Current Biology · doi:10.1016/j.cub.2015.02.038 · Cited by 33 · see citing works
Biology, Development, and Human Systems
Lickliter, R. E., & Honeycutt, H. G. (2015) · Wiley eBooks · doi:10.1002/9781118963418.childpsy105 · Cited by 31 · see citing works
A Risk of Sensory Deprivation in the Neonatal Intensive Care Unit
Jobe, A. H. (2014) · The Journal of Pediatrics · doi:10.1016/j.jpeds.2014.01.072 · Cited by 30 · see citing works
The circadian clock and hypoxia in tumor cell de-differentiation and metastasis
Jensen, L. D. (2014) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2014.10.025 · Cited by 29 · see citing works
Ocular Photoreception for Circadian Rhythm Entrainment in Mammals
Gelder, R. N. V., & Buhr, E. D. (2016) · Annual Review of Vision Science · doi:10.1146/annurev-vision-111815-114558 · Cited by 28 · see citing works
Circadian Rhythms in Cell Maturation
du Pré, B. C., van Veen, T. A. B., Young, M. E., Vos, M. A., Doevendans, P. A., & Laake, L. W. V. (2014) · Physiology · doi:10.1152/physiol.00036.2013 · Cited by 28 · see citing works
Lucas, J. A., & Schmidt, T. M. (2019) · Neural Development · doi:10.1186/s13064-019-0132-2 · Cited by 27 · see citing works
Ocular and extraocular roles of neuropsin in vertebrates
Calligaro, H., Dkhissi‐Benyahya, O., & Panda, S. (2021) · Trends in Neurosciences · doi:10.1016/j.tins.2021.11.008 · Cited by 27 · see citing works
Elsner, A. E., Chui, T. Y. P., Feng, L., Song, H. X., Papay, J. A., & Burns, S. A. (2016) · Vision Research · doi:10.1016/j.visres.2016.06.015 · Cited by 27 · see citing works
Mure, L. S., Hatori, M., Ruda, K., Benegiamo, G., Demas, J. A., & Panda, S. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.11.008 · Cited by 27 · see citing works
Circuit mechanisms underlying embryonic retinal waves
Voufo, C., Chen, A. Q., Smith, B. E., Yan, R.-S., Feller, M. B., & Tiriac, A. (2023) · eLife · doi:10.7554/elife.81983 · Cited by 26 · see citing works
The retinal clock in mammals: role in health and disease
Felder‐Schmittbuhl, M., Calligaro, H., & Dkhissi‐Benyahya, O. (2017) · ChronoPhysiology and Therapy · doi:10.2147/cpt.s115251 · Cited by 25 · see citing works
The Development of Mid-Wavelength Photoresponsivity in the Mouse Retina
Bonezzi, P. J., Stabio, M. E., & Renna, J. M. (2018) · Current Eye Research · doi:10.1080/02713683.2018.1433859 · Cited by 23 · see citing works
Neuronal Bmal1 regulates retinal angiogenesis and neovascularization in mice
Jidigam, V. K., Sawant, O. B., Fuller, R. D., Wilcots, K., Singh, R., Lang, R. A., & Rao, S. (2022) · Communications Biology · doi:10.1038/s42003-022-03774-2 · Cited by 25 · see citing works
Self-citationMcDowell, R. J., Didikoğlu, A., Woelders, T., Gatt, M. J., Moffatt, F., Notash, S., Hut, R. A., Brown, T. M., & Lucas, R. J. (2024) · BMC Biology · doi:10.1186/s12915-024-02038-1 · Cited by 23 · see citing works
Sawant, O., Horton, A. M., Shukla, M., Rayborn, M. E., Peachey, N. S., Hollyfield, J. G., & Rao, S. (2015) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.15-17743 · Cited by 24 · see citing works
Self-citationβA3/A1-crystallin and persistent fetal vasculature (PFV) disease of the eye
Zigler, J. S., Valapala, M., Shang, P., Hose, S., Goldberg, M. F., & Sinha, D. (2015) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2015.05.017 · Cited by 24 · see citing works
Myeloid Wnt ligands are required for normal development of dermal lymphatic vasculature
Muley, A., Odaka, Y., Lewkowich, I. P., Vemaraju, S., Yamaguchi, T. P., Shawber, C. J., Dickie, B., & Lang, R. A. (2017) · PLoS ONE · doi:10.1371/journal.pone.0181549 · Cited by 23 · see citing works
Self-citationNon-image-forming functional roles of OPN3, OPN4 and OPN5 photopigments
Ramanujam, K., Davies, W. I. L., & Gunhaga, L. (2023) · Journal of Photochemistry and Photobiology · doi:10.1016/j.jpap.2023.100177 · Cited by 21 · see citing works
Non-image-forming photoreceptors improve visual orientation selectivity and image perception
Shi, Y., Zhang, J., Li, X., Han, Y., Guan, J., Li, Y., Shen, J., Tzvetanov, T., Yang, D., Luo, X., et al. (2024) · Neuron · doi:10.1016/j.neuron.2024.11.015 · Cited by 29 · see citing works
Characterization of Tbr2‐expressing retinal ganglion cells
Chen, C.-K., Kiyama, T., Weber, N., Whitaker, C. M., Pan, P., Badea, T. C., Massey, S. C., & Mao, C. (2021) · The Journal of Comparative Neurology · doi:10.1002/cne.25208 · Cited by 23 · see citing works
Jensen, L. D., Gyllenhaal, C., & Block, K. I. (2014) · BioMolecular Concepts · doi:10.1515/bmc-2014-0009 · Cited by 22 · see citing works
Hyperoxia Depletes (6R)-5,6,7,8-Tetrahydrobiopterin Levels in the Neonatal Retina
Edgar, K. S., Matesanz, N., Gardiner, T. A., Katušić, Z. S., & McDonald, D. (2015) · American Journal Of Pathology · doi:10.1016/j.ajpath.2015.02.021 · Cited by 21 · see citing works
The Newborn's Reaction to Light as the Determinant of the Brain's Activation at Human Birth
Polese, D., Riccio, M. L., Fagioli, M., Mazzetta, A., Fagioli, F., Parisi, P., & Fagioli, M. (2022) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2022.933426 · Cited by 22 · see citing works
Melanopsin ganglion cells extend dendrites into the outer retina during early postnatal development
Renna, J. M., Chellappa, D. K., Ross, C. L., Stabio, M. E., & Berson, D. M. (2014) · Developmental Neurobiology · doi:10.1002/dneu.22260 · Cited by 21 · see citing works
Functional characterisation of naturally occurring mutations in human melanopsin
Rodgers, J., Peirson, S. N., Hughes, S., & Hankins, M. W. (2018) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-018-2813-0 · Cited by 21 · see citing works
Genomics in the neonatal nursery: Focus on ROP
Hartnett, M. E., & Cotten, C. M. (2015) · Seminars in Perinatology · doi:10.1053/j.semperi.2015.09.007 · Cited by 21 · see citing works
- Authors
- Rao, S., Chun, C., Fan, J., Kofron, J. M., Yang, M. B., Hegde, R. S., Ferrara, N., Copenhagen, D. R., & Lang, R. A.
- Affiliations
- Cincinnati Children's Hospital Medical Center (US)
- University of California, San Francisco (US)
- Genentech (US)
- Corresponding author
- Copenhagen, David R.
- Lang, Richard A.
- ORCID
- Venue
- Nature
- Published
- 2013-01-16
- Volume
- 494
- Issue
- 7436
- Pages
- 243-246
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC3746810
- OpenAlex
- W2088406510
- Cited by
- 240
- References
- 31
- Citations by year
- 2026: 22 · 2025: 21 · 2024: 19 · 2023: 22 · 2022: 15 · 2021: 14 · 2020: 15 · 2019: 11 · 2018: 17 · 2017: 21 · 2016: 15 · 2015: 21 · 2014: 17 · 2013: 10
- FWCI
- 9.40
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- National Eye Institute (R01EY022917, R01EY021636, R01EY014648, R01EY023179, R01EY001869)
- National Institute of Arthritis and Musculoskeletal and Skin Diseases (AR47363, P30AR047363)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Retinal Development and Disorders
- Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Retinopathy of Prematurity Studies
- Health Sciences › Medicine › Ophthalmology › Retinal Diseases and Treatments
- Keywords
- melanopsin, retinal angiogenesis, retinal vasculature development, VEGF-A, retinal ganglion cells, photoreceptors, hypoxia, eye development, vascular patterning
- MeSH terms
- Melanopsin, Animals, Cell Count, Eye, Female, Fetus, Light, Mice, Inbred C57BL, Neovascularization, Pathologic, Retinal Ganglion Cells, Cell Hypoxia, Rod Opsins, Photons, Neovascularization, Physiologic, Vascular Endothelial Growth Factor A, Mice, Retinal Neurons, Light Signal Transduction
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
