Our Work

The Benowitz Lab has had a long-standing interest in the repair of the central nervous system (CNS), with a primary focus on the optic nerve. Neurons cannot regenerate long-distance connections after traumatic, ischemic, or neurodegenerative damage to the CNS, and consequently, victims of stroke, traumatic brain injury, spinal cord injury, optic nerve damage, and other insults to the CNS commonly sustain life-long functional losses. The optic nerve conveys information from the eye to the brain and has been widely studied for its relevance to glaucoma and other visual disorders, as well as for insights into factors that may suppress or enhance axon regeneration in other parts of the CNS. Retinal ganglion cells (RGCs), the projection neurons of the eye, cannot regenerate their axons (nerve fibers) when the optic nerve is injured and soon begin to die, precluding visual recovery. Unexpectedly, we found that inducing inflammation reaction in the eye promotes optic nerve regeneration and RGC survival, and identified oncomodulin and other proteins secreted by inflammatory cells that mediate the beneficial effects of inflammation and that might be useful clinically. Combining oncomodulin or intraocular inflammation with treatments that counteract cell-extrinsic or cell-intrinsic suppressors of axon growth results in strongly synergistic effects, enabling some nerve fibers to regenerate all the way from the eye to the brain and restore simple visual responses. We have also investigated the intracellular signaling cascade and changes in gene expression that underlie successful axon regeneration; the role of TNF-alpha in animal models of glaucoma, the role of inosine in rewiring neural connections after stroke and spinal cord injury, and recently, the role of zinc dysregulation and intra-retinal communication networks in controlling outcome after optic nerve injury.

Larry Benowitz holds the Neurosurgical Innovation and Research Professorship at Boston Children's Hospital and is a Professor of Neurosurgery and Ophthalmology at Harvard Medical School. He received his PhD from Caltech with Nobel Laureate Roger Sperry and did postdoctoral research at MIT and Harvard Medical School before joining the Harvard faculty. He has mentored many students and postdoctoral fellows and is first- or senior author on over 150 papers, reviews and book chapters. He was named by Scientific American as one of the 50 leaders of the year in science and technology in 2006 and in 2013 was awarded the Lewis Rudin Prize for "the most significant scholarly article on glaucoma published in a peer-reviewed journal in the prior calendar year".

Over the past 5 years, Dr. Benowitz has served on the Standing Committee on Honors and Awards of Harvard Medical School (Co-chair), Steering Committee of the Postdoctoral Training Program in the Molecular Bases of Eye Diseases, Scientific Advisory Board of the Veteran’s Administration Spinal Cord Injury and Repair, Audacious Goals Working Group of the National Eye Institute, Faculty Council, Surgical Research Council, and Animal Resource Committee of Boston Children’s Hospital, Scientific Advisory Boards of the Vision Institute (l’Institut de la Vision, Paris), Glaucoma Research Foundation, Vanderbilt Eye Institute, and Whitehall Foundation. During this period, he has lectured at the Association for Ocular Pharmacology and Therapeutics (Alicante, Spain), Senior Society of the Society for Neurological Surgery (Boston), International Neural Regeneration Symposium (Shenyang, China), Turkish Neuroscience Society, Glaucoma Summer Camp (Sendai Japan), NEI National Advisory Eye Council, Lasker/IRRF Workshop on Restoring Vision to the Blind (Janelia Farm, VA), Research Update in Neuroscience for Neurosurgeons (Woods Hole, MA), Symposium on Ocular Regeneration (Schepens Eye Research Institute/MEEI, Boston), International Society for Zinc Biology (Asilomar, CA and Larnaca, Cyprus), Kentucky Spinal Cord and Head Injury Research Trust Conference (Lexington, KY), Symposium on the “Assembly and Disassembly of the Nervous System” (Weizmann Institute of Science, Rehovot, Israel), Winter Brain Conference Symposium on Zinc in the Brain (Big Sky Montana); Several symposia of the Association for Research in Ophthalmology (Denver, CO); Imperial College Ophthalmic Research Day (Keynote speaker, London, UK); NYU Medical Ctr., Dept. Neurology; NEI Audacious Goals Roundtable, Cambridge University, Fox Center for Vision Repair (Pittsburgh, Washington DC), National Neurotrauma Society (Santa Fe, NM), American Society for Neural Repair (Chicago, IL); Optic Nerve Conference (Obergürgl, Austria); Israel Society for Neuroscience (Eilat, Israel). NEI Audacious Goals Initiative on Optic nerve regeneration (Chicago IL); Wilmer Eye Center (Johns Hopkins School of Medicine, Baltimore), Winter Conference for Brain Research (Breckenridge, CO); Glaucoma 360 (San Francisco, CA); Gordon Research Conference on the Molecular Biology of the Neuron; Case Western Reserve Univ. (Cleveland); SUNY Upstate (Syracuse, NY); Chinese Glaucoma Society (Keynote speaker, Xuzhou, China); ARVO (Baltimore, MD: May 2017), Mass. Eye and Ear Infirmary; Conference on Low Vision (Berlin, Germany), Chinese Glaucoma Society (Keynote speaker, Guangzhou, China); Special Interest Group, ARVO “A Matter of Life and Death: Non cell-autonomous regulation of retinal ganglion cell survival” (Organizer); World Ophthalmology Congress (Barcelona, Spain); Neuroscience Virtual Conf.; NIPER-Ahmedabad, India (Web-based seminar), and the University of Montreal. Dr. Benowitz’ research is supported by the National Eye Institute (NEI, NIH), the Dr. Miriam and Sheldon G. Adelson Research Foundation, the U.S. Department of Defense, the Gilbert Vision Restoration Program, and the Boston Pediatric Neurosurgical Foundation.

Protection of RGCs in optic nerve injury and glaucoma: Role of zinc and TNF-a.

Intraocular inflammation, oncomodulin, and optic nerve regeneration.   

Inosine, stroke and spinal cord injury.

Publications

Protection of RGCs in optic nerve injury and glaucoma: Role of zinc and TNF-a.

Glaucoma is a leading cause of blindness worldwide, and although current treatments usually stem the progression of the disease, there are many cases in which this approach is unsuccessful. In two animal models of glaucoma, we elevated intraocular pressure by either episcleral vein cauterization (in rats) or angle closure (in mice) and observed a dramatic elevation of the cytokine TNF-a, activation of microglia12, and a delayed, progressive loss of RGCs, thus mimicking key features of the disease. In one study, we showed that deletion of the gene for TNF-a or one of its receptors, or use of an antibody to TNF-a greatly slowed or arrested the loss of RGCs despite persistently elevated intraocular pressure1. In the second study, we showed that Etanercept, an FDA-approved, soluble decoy receptor for TNF-a, arrested microglial activation at the optic nerve head along and stemmed the loss of RGCs2. These studies have contributed to a growing awareness of the role of TNF-a and inflammation as potentially critical factors in the pathophysiology of glaucoma.

In other work, we have found that one of the earliest events to occur in the eye after the optic nerve is injured is a rise in ionic zinc (Zn2+) in the synaptic terminals that amacrine cells make onto the dendrites of RGCs. Within 2 days or so, the Zn2+ accumulates in RGCs. This effect requires the Zn2+ transporter ZnT3 and nitric oxide. Chelating Zn2+ leads to the enduring survival of many RGCs and extensive axon regeneration3. Ongoing projects in the lab are aimed at understanding the cellular and molecular events that underlie the presynaptic accumulation of zinc after optic nerve injury and the role that zinc plays in suppressing cell survival and axon regeneration.

  1. Nakazawa T, Nakazawa C, Matsubara A, Noda K, Hisatomi T, She H, Michaud N, Hafezi-Moghadam A, Miller JW, Benowitz LI. J Neurosci Tumor necrosis factor-alpha mediates oligodendrocyte death and delayed retinal ganglion cell loss in a mouse model of glaucoma 2006;26(49):12633-41. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=17151265
  2. Roh M, Zhang Y, Murakami Y, Thanos A, Lee SC, Vavvas DG, Benowitz LI, Miller JW. PLoS One Etanercept, a widely used inhibitor of tumor necrosis factor-alpha (TNF-alpha), prevents retinal ganglion cell loss in a rat model of glaucoma 2012;7(7):e40065. http://www.ncbi.nlm.nih.gov/pubmed/22802951.3388998
  3. Li Y, Andereggen L, Yuki K, Omura K, Yin Y, Gilbert HY, Erdogan B, Asdourian MS, Shrock C, de Lima S, Apfel UP, Zhuo Y, Hershfinkel M, Lippard SJ, Rosenberg PA, Benowitz L. Proc Natl Acad Sci U S A Mobile zinc increases rapidly in the retina after optic nerve injury and regulates ganglion cell survival and optic nerve regeneration 2017;114(2):E209-E218. https://www.ncbi.nlm.nih.gov/pubmed/28049831.PMC5240690

 

Intraocular inflammation, oncomodulin, and optic nerve regeneration.

Due to its accessibility, simple anatomy, and functional importance, the optic nerve has been widely studied for insights into positive and negative regulators of axon regeneration in the CNS. We earlier discovered that intraocular inflammation enables retinal ganglion cells (RGCs), the projection neurons of the eye, to undergo dramatic changes in their program of gene expression, revert to an active growth state, and regenerate lengthy axons through the injured optic nerve1-3. We identified Oncomodulin (Ocm), a small Ca2+-binding protein, as a key mediator of these effects, and showed that Ocm binds to a high-affinity receptor on RGCs in a cAMP-dependent manner. Levels of Ocm mRNA and protein increase dramatically in the eye following intraocular inflammation, and gain-of-function and loss-of-function studies show that neutrophil-derived Ocm plays a central role in inflammation-induced regeneration4-6. Our studies also showed that other factors from inflammatory cells are required to enable Ocm to bind to its receptor and to promote RGC survival, and we recently identified a second protein that works synergistically with Ocm. Combining these molecules may enable us to promote regeneration in a clinically relevant manner.

Combinatorial treatments for long-distance axon regeneration and innervation of central target areas.

In other studies, we demonstrated a massive synergy between activating RGCs’ growth state via intraocular inflammation and knocking out the gene for pten, a potent cell-intrinsic suppressor of growth10. PTEN acts as a brake on activation of the PI3 kinase-Akt pathway, which controls cell growth, and deletion of PTEN was previously shown to be sufficient to cause appreciable regeneration on its own11. We then showed that combining intraocular inflammation, elevation of cAMP and PTEN deletion enables some RGCs to regenerate axons the full length of the optic nerve, reinervate the appropriate central target areas in the brain, and restore simple visual responses 12. This study represented the first to demonstrate the possibility of restoring the appropriate circuitry of the visual system after optic nerve damage.

Counteracting cell-extrinsic suppressors of axon growth.

Proteins associated with CNS myelin and the scar that forms at the site of a CNS injury inhibit axon growth in culture, yet counteracting the effects of these proteins has generally been found to be insufficient to promote extensive axon regeneration in vivo. Using a gene-therapy approach, we found that two genetic manipulations that render RGCs unresponsive to myelin and the glial scar failed to induce extensive axon regeneration after optic nerve injury. These treatments included virally-mediated expression of either a dominant-negative form of the Nogo receptor or of C3 ribosyltransferase to inactivate RhoA, a key part of the intracellular signal transduction pathway leading to growth arrest). However, when we combined methods to counteract cell-extrinsic suppressors of axon growth with methods to activate RGCs’ intrinsic growth state, we obtained 3-5 times more regeneration than the latter treatment alone37. Subsequent collaborative studies showed that deleting multiple isoforms of the Nogo receptor, along with PTP-sigma, one of several receptors for inhibitory molecules associated with the scar that forms at an injury site, enable somewhat greater regeneration than seen in our earlier studies, but that again, the effects of counteracting receptors for cell-extrinsic inhibitors of axon growth was greatly augmented by activating RGCs’ intrinsic growth state89. Together, these studies reinforce the insufficiency of counteracting inhibitory proteins as a means of promoting CNS regeneration in vivo while at the same time showing the synergistic effects of combining the latter approach with methods that activate neurons’ intrinsic growth state.

Ongoing projects

  • Understanding the cell signaling pathways and sequence of transcriptional changes that underlie successful regeneration in vivo
  • altering expression of genes identified thorugh this work to enhance levels of optic nerve regeneration
  • identifying the receptor through which Ocm induces axon outgrowth
  • developing translationally applicable methods to restore vision after optic nerve injury.

 

  1. Leon S, Yin Y, Nguyen J, Irwin N, Benowitz LI. J Neurosci Lens injury stimulates axon regeneration in the mature rat optic nerve 2000;20(12):4615-26.
  2. Yin Y, Cui Q, Li Y, Irwin N, Fischer D, Harvey AR, Benowitz LI. Journal of Neuroscience Macrophage-derived factors stimulate optic nerve regeneration 2003;23:2284-93.
  3. Fischer D, Petkova V, Thanos S, Benowitz LI. J Neurosci Switching mature retinal ganglion cells to a robust growth state in vivo: gene expression and synergy with RhoA inactivation 2004;24:8726-8740.
  4. Yin Y, Henzl MT, Lorber B, Nakazawa T, Thomas TT, Jiang F, Langer R, Benowitz LI. Nat Neurosci Oncomodulin is a macrophage-derived signal for axon regeneration in retinal ganglion cells 2006;9(6):843-52. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=16699509
  5. Yin Y, Cui Q, Gilbert HY, Yang Y, Yang Z, Berlinicke C, Li Z, Zaverucha-do-Valle C, He H, Petkova V, Zack DJ, Benowitz LI. Proc Natl Acad Sci U S A Oncomodulin links inflammation to optic nerve regeneration 2009;106(46):19587-92. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=19875691.2780793
  6. Kurimoto T, Yin Y, Habboub G, Gilbert HY, Li Y, Nakao S, Hafezi-Moghadam A, Benowitz LI. J Neurosci Neutrophils express oncomodulin and promote optic nerve regeneration 2013;33(37):14816-24. http://www.ncbi.nlm.nih.gov/pubmed/24027282.3771038
  7. Fischer D, He Z, Benowitz LI. J Neurosci Counteracting the Nogo receptor enhances optic nerve regeneration if retinal ganglion cells are in an active growth state 2004;24(7):1646-51. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=14973241.
  8. Wang X, Hasan O, Arzeno A, Benowitz LI, Cafferty WB, Strittmatter SM. Exp Neurol Axonal regeneration induced by blockade of glial inhibitors coupled with activation of intrinsic neuronal growth pathways 2012;237(1):55-69. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=22728374.3418451
  9. Dickendesher TL, Baldwin KT, Mironova YA, Koriyama Y, Raiker SJ, Askew KL, Wood A, Geoffroy CG, Zheng B, Liepmann CD, Katagiri Y, Benowitz LI, Geller HM, Giger RJ. Nat Neurosci NgR1 and NgR3 are receptors for chondroitin sulfate proteoglycans 2012;15(5):703-12. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=22406547.3337880
  10. Kurimoto T, Yin Y, Omura K, Gilbert HY, Kim D, Cen LP, Moko L, Kugler S, Benowitz LI. J Neurosci Long-distance axon regeneration in the mature optic nerve: contributions of oncomodulin, cAMP, and pten gene deletion 2010;30(46):15654-63. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=21084621.3001271
  11. Park KK, Liu K, Hu Y, Smith PD, Wang C, Cai B, Xu B, Connolly L, Kramvis I, Sahin M, He Z. Science Promoting axon regeneration in the adult CNS by modulation of the PTEN/mTOR pathway 2008;322(5903):963-6. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=18988856.2652400
  12. de Lima S, Koriyama Y, Kurimoto T, Oliveira JT, Yin Y, Li Y, Gilbert HY, Fagiolini M, Martinez AM, Benowitz L. Proc Natl Acad Sci U S A Full-length axon regeneration in the adult mouse optic nerve and partial recovery of simple visual behaviors 2012;109(23):9149-54. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=22615390.

 

Inosine, stroke and spinal cord injury.

Earlier studies from our lab showed that inosine, a metabolite of adenosine, acts through a direct intracellular mechanism to stimulate axon outgrowth from neurons in cell culture1. We went on to identify the target of insosine as Mst3b (STK24), a protein kinase that is an essential part of the cell-signaling pathway through which many trophic factors promote axon outgrowth in culture and in vivo23In vivo, we found that, after a unilateral stroke of the rat motor cortex, intraventricular delivery of inosine enhanced the ability of layer 5 pyramidal cells in the undamaged contralateral cortex to sprout axon collaterals into the denervated side of the spinal cord and improve skilled use of the impaired forepaw. This capacity was further enhanced by environmental enrichment or by combining inosine with a peptide antagonist of the Nogo receptor45. Additional studies showed that inosine promotes the formation of “detour circuits” in the spinal cord after transecting the corticospinal tract (CST) at the mid-thoracic level. Inosine enhanced the ability of transected CST axons to sprout collateral branches in the cervical spinal cord that formed synaptic contacts onto spinal interneurons that project from the cervical spinal cord to the lumbar level, thus providing indirect cortical input to the lumbar spinal cord and restoring some volitional control to the hindlimbs6.

  1. Benowitz LI, Jing Y, Tabibiazar R, Jo SA, Petrausch B, Stuermer CA, Rosenberg PA, Irwin N. J Biol Chem Axon outgrowth is regulated by an intracellular purine-sensitive mechanism in retinal ganglion cells 1998;273(45):29626-34.
  2. Irwin N, Li YM, O'Toole JE, Benowitz LI. Proc Natl Acad Sci U S A Mst3b, a purine-sensitive Ste20-like protein kinase, regulates axon outgrowth 2006;103:18320-5. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=17114295
  3. Lorber B, Howe ML, Benowitz LI, Irwin N. Nat Neurosci Mst3b, an Ste20-like kinase, regulates axon regeneration in mature CNS and PNS pathways 2009;12:1407-14. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=19855390.2770175
  4. Zai L, Ferrari C, Subbaiah S, Havton LA, Coppola G, Strittmatter S, Irwin N, Geschwind D, Benowitz LI. J Neurosci Inosine alters gene expression and axonal projections in neurons contralateral to a cortical infarct and improves skilled use of the impaired limb 2009;29(25):8187-97. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=19553458.
  5. Zai L, Ferrari C, Dice C, Subbaiah S, Havton LA, Coppola G, Geschwind D, Irwin N, Huebner E, Strittmatter SM, Benowitz LI. J Neurosci Inosine augments the effects of a Nogo receptor blocker and of environmental enrichment to restore skilled forelimb use after stroke 2011;31(16):5977-88. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=21508223.3101108
  6. Kim D, Zai L, Liang P, Schaffling C, Ahlborn D, Benowitz LI. PLoS One Inosine enhances axon sprouting and motor recovery after spinal cord injury 2013;8:e81948. http://www.ncbi.nlm.nih.gov/pubmed/24312612.3846725

 

Benowitz Lab Publications:

  1. Peterson SL, Benowitz LI. Mammalian dendritic regrowth: a new perspective on neural repair. Brain. 2018 Jul 01; 141(7):1891-1894. View abstract
  2. Chen W, Sinha B, Li Y, Benowitz L, Chen Q, Zhang Z, Patel NJ, Aziz-Sultan AM, Chiocca AE, Wang X. Monogenic, Polygenic, and MicroRNA Markers for Ischemic Stroke. Mol Neurobiol. 2018 Jun 08. View abstract
  3. Yin Y, Benowitz LI. In Vitro and In Vivo Methods for Studying Retinal Ganglion Cell Survival and Optic Nerve Regeneration. Methods Mol Biol. 2018; 1695:187-205. View abstract
  4. Trakhtenberg EF, Li Y, Feng Q, Tso J, Rosenberg PA, Goldberg JL, Benowitz LI. Zinc chelation and Klf9 knockdown cooperatively promote axon regeneration after optic nerve injury. Exp Neurol. 2018 Feb; 300:22-29. View abstract
  5. Calkins DJ, Pekny M, Cooper ML, Benowitz L. The challenge of regenerative therapies for the optic nerve in glaucoma. Exp Eye Res. 2017 04; 157:28-33. View abstract
  6. Li Y, Andereggen L, Yuki K, Omura K, Yin Y, Gilbert HY, Erdogan B, Asdourian MS, Shrock C, de Lima S, Apfel UP, Zhuo Y, Hershfinkel M, Lippard SJ, Rosenberg PA, Benowitz L. Mobile zinc increases rapidly in the retina after optic nerve injury and regulates ganglion cell survival and optic nerve regeneration. Proc Natl Acad Sci U S A. 2017 01 10; 114(2):E209-E218. View abstract
  7. Moore TL, Pessina MA, Finklestein SP, Killiany RJ, Bowley B, Benowitz L, Rosene DL. Inosine enhances recovery of grasp following cortical injury to the primary motor cortex of the rhesus monkey. Restor Neurol Neurosci. 2016 09 21; 34(5):827-48. View abstract
  8. Marin MA, de Lima S, Gilbert HY, Giger RJ, Benowitz L, Rasband MN. Reassembly of Excitable Domains after CNS Axon Regeneration. J Neurosci. 2016 08 31; 36(35):9148-60. View abstract
  9. Omura T, Omura K, Tedeschi A, Riva P, Painter MW, Rojas L, Martin J, Lisi V, Huebner EA, Latremoliere A, Yin Y, Barrett LB, Singh B, Lee S, Crisman T, Gao F, Li S, Kapur K, Geschwind DH, Kosik KS, Coppola G, He Z, Carmichael ST, Benowitz LI, Costigan M, Woolf CJ. Robust Axonal Regeneration Occurs in the Injured CAST/Ei Mouse CNS. Neuron. 2016 May 04; 90(3):662. View abstract
  10. Chandran V, Coppola G, Nawabi H, Omura T, Versano R, Huebner EA, Zhang A, Costigan M, Yekkirala A, Barrett L, Blesch A, Michaelevski I, Davis-Turak J, Gao F, Langfelder P, Horvath S, He Z, Benowitz L, Fainzilber M, Tuszynski M, Woolf CJ, Geschwind DH. A Systems-Level Analysis of the Peripheral Nerve Intrinsic Axonal Growth Program. Neuron. 2016 Mar 02; 89(5):956-70. View abstract
  11. Benowitz LI, He Z, Goldberg JL. Reaching the brain: Advances in optic nerve regeneration. Exp Neurol. 2017 Jan; 287(Pt 3):365-373. View abstract
  12. Chung YG, Seth A, Doyle C, Franck D, Kim D, Cristofaro V, Benowitz LI, Tu DD, Estrada CR, Mauney JR, Sullivan MP, Adam RM. Inosine Improves Neurogenic Detrusor Overactivity following Spinal Cord Injury. PLoS One. 2015; 10(11):e0141492. View abstract
  13. Li S, Nie EH, Yin Y, Benowitz LI, Tung S, Vinters HV, Bahjat FR, Stenzel-Poore MP, Kawaguchi R, Coppola G, Carmichael ST. GDF10 is a signal for axonal sprouting and functional recovery after stroke. Nat Neurosci. 2015 Dec; 18(12):1737-45. View abstract
  14. Omura T, Omura K, Tedeschi A, Riva P, Painter MW, Rojas L, Martin J, Lisi V, Huebner EA, Latremoliere A, Yin Y, Barrett LB, Singh B, Lee S, Crisman T, Gao F, Li S, Kapur K, Geschwind DH, Kosik KS, Coppola G, He Z, Carmichael ST, Benowitz LI, Costigan M, Woolf CJ. Robust Axonal Regeneration Occurs in the Injured CAST/Ei Mouse CNS. Neuron. 2015 Jun 03; 86(5):1215-27. View abstract
  15. Xiong W, MacColl Garfinkel AE, Li Y, Benowitz LI, Cepko CL. NRF2 promotes neuronal survival in neurodegeneration and acute nerve damage. J Clin Invest. 2015 Apr; 125(4):1433-45. View abstract
  16. Koriyama Y, Kurimoto T, de Lima S, Benowitz L. [Reinnervation of central visual areas and recovery of visual functions following optic nerve regeneration in adult mice]. Brain Nerve. 2014 Mar; 66(3):265-72. View abstract
  17. Dachir S, Shabashov D, Trembovler V, Alexandrovich AG, Benowitz LI, Shohami E. Inosine improves functional recovery after experimental traumatic brain injury. Brain Res. 2014 Mar 25; 1555:78-88. View abstract
  18. Kim D, Zai L, Liang P, Schaffling C, Ahlborn D, Benowitz LI. Inosine enhances axon sprouting and motor recovery after spinal cord injury. PLoS One. 2013; 8(12):e81948. View abstract
  19. Kurimoto T, Yin Y, Habboub G, Gilbert HY, Li Y, Nakao S, Hafezi-Moghadam A, Benowitz LI. Neutrophils express oncomodulin and promote optic nerve regeneration. J Neurosci. 2013 Sep 11; 33(37):14816-24. View abstract
  20. Seth A, Chung YG, Kim D, Ramachandran A, Cristofaro V, Gomez P, Tu D, Huang L, Benowitz LI, Di Vizio D, Sullivan MP, Adam RM. The impact of discrete modes of spinal cord injury on bladder muscle contractility. BMC Urol. 2013 May 13; 13:24. View abstract
  21. Roh M, Zhang Y, Murakami Y, Thanos A, Lee SC, Vavvas DG, Benowitz LI, Miller JW. Etanercept, a widely used inhibitor of tumor necrosis factor-a (TNF-a), prevents retinal ganglion cell loss in a rat model of glaucoma. PLoS One. 2012; 7(7):e40065. View abstract
  22. Wang X, Hasan O, Arzeno A, Benowitz LI, Cafferty WB, Strittmatter SM. Axonal regeneration induced by blockade of glial inhibitors coupled with activation of intrinsic neuronal growth pathways. Exp Neurol. 2012 Sep; 237(1):55-69. View abstract
  23. de Lima S, Koriyama Y, Kurimoto T, Oliveira JT, Yin Y, Li Y, Gilbert HY, Fagiolini M, Martinez AM, Benowitz L. Full-length axon regeneration in the adult mouse optic nerve and partial recovery of simple visual behaviors. Proc Natl Acad Sci U S A. 2012 Jun 05; 109(23):9149-54. View abstract
  24. Dickendesher TL, Baldwin KT, Mironova YA, Koriyama Y, Raiker SJ, Askew KL, Wood A, Geoffroy CG, Zheng B, Liepmann CD, Katagiri Y, Benowitz LI, Geller HM, Giger RJ. NgR1 and NgR3 are receptors for chondroitin sulfate proteoglycans. Nat Neurosci. 2012 Mar 11; 15(5):703-12. View abstract
  25. de Lima S, Habboub G, Benowitz LI. Combinatorial therapy stimulates long-distance regeneration, target reinnervation, and partial recovery of vision after optic nerve injury in mice. Int Rev Neurobiol. 2012; 106:153-72. View abstract
  26. Benowitz LI, Popovich PG. Inflammation and axon regeneration. Curr Opin Neurol. 2011 Dec; 24(6):577-83.View abstract
  27. Wang X, Duffy P, McGee AW, Hasan O, Gould G, Tu N, Harel NY, Huang Y, Carson RE, Weinzimmer D, Ropchan J, Benowitz LI, Cafferty WB, Strittmatter SM. Recovery from chronic spinal cord contusion after Nogo receptor intervention. Ann Neurol. 2011 Nov; 70(5):805-21. View abstract
  28. Benowitz L. Author's response to Steward et al., "A re-assessment of the effects of intra-cortical delivery of inosine….". Exp Neurol. 2012 Feb; 233(2):674-6. View abstract
  29. Zai L, Ferrari C, Dice C, Subbaiah S, Havton LA, Coppola G, Geschwind D, Irwin N, Huebner E, Strittmatter SM, Benowitz LI. Inosine augments the effects of a Nogo receptor blocker and of environmental enrichment to restore skilled forelimb use after stroke. J Neurosci. 2011 Apr 20; 31(16):5977-88. View abstract
  30. Kurimoto T, Yin Y, Omura K, Gilbert HY, Kim D, Cen LP, Moko L, Kügler S, Benowitz LI. Long-distance axon regeneration in the mature optic nerve: contributions of oncomodulin, cAMP, and pten gene deletion. J Neurosci. 2010 Nov 17; 30(46):15654-63. View abstract
  31. Benowitz LI, Yin Y. Optic nerve regeneration. Arch Ophthalmol. 2010 Aug; 128(8):1059-64. View abstract
  32. Benowitz LI, Carmichael ST. Promoting axonal rewiring to improve outcome after stroke. Neurobiol Dis. 2010 Feb; 37(2):259-66. View abstract
  33. Yin Y, Cui Q, Gilbert HY, Yang Y, Yang Z, Berlinicke C, Li Z, Zaverucha-do-Valle C, He H, Petkova V, Zack DJ, Benowitz LI. Oncomodulin links inflammation to optic nerve regeneration. Proc Natl Acad Sci U S A. 2009 Nov 17; 106(46):19587-92. View abstract
  34. Lorber B, Howe ML, Benowitz LI, Irwin N. Mst3b, an Ste20-like kinase, regulates axon regeneration in mature CNS and PNS pathways. Nat Neurosci. 2009 Nov; 12(11):1407-14. View abstract
  35. Zai L, Ferrari C, Subbaiah S, Havton LA, Coppola G, Strittmatter S, Irwin N, Geschwind D, Benowitz LI. Inosine alters gene expression and axonal projections in neurons contralateral to a cortical infarct and improves skilled use of the impaired limb. J Neurosci. 2009 Jun 24; 29(25):8187-97. View abstract
  36. Cui Q, Yin Y, Benowitz LI. The role of macrophages in optic nerve regeneration. Neuroscience. 2009 Feb 06; 158(3):1039-48. View abstract
  37. Cui Q, Benowitz L, Yin Y. Does CNTF mediate the effect of intraocular inflammation on optic nerve regeneration? Brain. 2008 Jun; 131(Pt 6):e96; author reply e97. View abstract
  38. Benowitz LI, Yin Y. Combinatorial treatments for promoting axon regeneration in the CNS: strategies for overcoming inhibitory signals and activating neurons' intrinsic growth state. Dev Neurobiol. 2007 Aug; 67(9):1148-65. View abstract
  39. Benowitz L, Yin Y. Rewiring the injured CNS: lessons from the optic nerve. Exp Neurol. 2008 Feb; 209(2):389-98. View abstract
  40. Nakazawa T, Hisatomi T, Nakazawa C, Noda K, Maruyama K, She H, Matsubara A, Miyahara S, Nakao S, Yin Y, Benowitz L, Hafezi-Moghadam A, Miller JW. Monocyte chemoattractant protein 1 mediates retinal detachment-induced photoreceptor apoptosis. Proc Natl Acad Sci U S A. 2007 Feb 13; 104(7):2425-30. View abstract
  41. Nakazawa T, Nakazawa C, Matsubara A, Noda K, Hisatomi T, She H, Michaud N, Hafezi-Moghadam A, Miller JW, Benowitz LI. Tumor necrosis factor-alpha mediates oligodendrocyte death and delayed retinal ganglion cell loss in a mouse model of glaucoma. J Neurosci. 2006 Dec 06; 26(49):12633-41. View abstract
  42. Irwin N, Li YM, O'Toole JE, Benowitz LI. Mst3b, a purine-sensitive Ste20-like protein kinase, regulates axon outgrowth. Proc Natl Acad Sci U S A. 2006 Nov 28; 103(48):18320-5. View abstract
  43. Piantino J, Burdick JA, Goldberg D, Langer R, Benowitz LI. An injectable, biodegradable hydrogel for trophic factor delivery enhances axonal rewiring and improves performance after spinal cord injury. Exp Neurol. 2006 Oct; 201(2):359-67. View abstract
  44. Yin Y, Henzl MT, Lorber B, Nakazawa T, Thomas TT, Jiang F, Langer R, Benowitz LI. Oncomodulin is a macrophage-derived signal for axon regeneration in retinal ganglion cells. Nat Neurosci. 2006 Jun; 9(6):843-52. View abstract
  45. Fischer D, Petkova V, Thanos S, Benowitz LI. Switching mature retinal ganglion cells to a robust growth state in vivo: gene expression and synergy with RhoA inactivation. J Neurosci. 2004 Oct 06; 24(40):8726-40. View abstract
  46. Fischer D, He Z, Benowitz LI. Counteracting the Nogo receptor enhances optic nerve regeneration if retinal ganglion cells are in an active growth state. J Neurosci. 2004 Feb 18; 24(7):1646-51. View abstract
  47. Li Y, Irwin N, Yin Y, Lanser M, Benowitz LI. Axon regeneration in goldfish and rat retinal ganglion cells: differential responsiveness to carbohydrates and cAMP. J Neurosci. 2003 Aug 27; 23(21):7830-8. View abstract
  48. Yin Y, Cui Q, Li Y, Irwin N, Fischer D, Harvey AR, Benowitz LI. Macrophage-derived factors stimulate optic nerve regeneration. J Neurosci. 2003 Mar 15; 23(6):2284-93. View abstract
  49. Irwin N, Chao S, Goritchenko L, Horiuchi A, Greengard P, Nairn AC, Benowitz LI. Nerve growth factor controls GAP-43 mRNA stability via the phosphoprotein ARPP-19. Proc Natl Acad Sci U S A. 2002 Sep 17; 99(19):12427-31. View abstract
  50. Chen P, Goldberg DE, Kolb B, Lanser M, Benowitz LI. Inosine induces axonal rewiring and improves behavioral outcome after stroke. Proc Natl Acad Sci U S A. 2002 Jun 25; 99(13):9031-6. View abstract
  51. Benowitz LI, Goldberg DE, Irwin N. Inosine stimulates axon growth in vitro and in the adult CNS. Prog Brain Res. 2002; 137:389-99. View abstract
  52. Benowitz LI, Goldberg DE, Irwin N. A purine-sensitive mechanism regulates the molecular program for axon growth. Restor Neurol Neurosci. 2001; 19(1-2):41-9. View abstract
  53. Petrausch B, Tabibiazar R, Roser T, Jing Y, Goldman D, Stuermer CA, Irwin N, Benowitz LI. A purine-sensitive pathway regulates multiple genes involved in axon regeneration in goldfish retinal ganglion cells. J Neurosci. 2000 Nov 01; 20(21):8031-41. View abstract
  54. Leon S, Yin Y, Nguyen J, Irwin N, Benowitz LI. Lens injury stimulates axon regeneration in the mature rat optic nerve. J Neurosci. 2000 Jun 15; 20(12):4615-26. View abstract
  55. Kim HA, Pomeroy SL, Whoriskey W, Pawlitzky I, Benowitz LI, Sicinski P, Stiles CD, Roberts TM. A developmentally regulated switch directs regenerative growth of Schwann cells through cyclin D1. Neuron. 2000 May; 26(2):405-16. View abstract
  56. Benowitz LI, Goldberg DE, Madsen JR, Soni D, Irwin N. Inosine stimulates extensive axon collateral growth in the rat corticospinal tract after injury. Proc Natl Acad Sci U S A. 1999 Nov 09; 96(23):13486-90. View abstract
  57. Jo SA, Wang E, Benowitz LI. Ciliary neurotrophic factor is an axogenesis factor for retinal ganglion cells. Neuroscience. 1999 Mar; 89(2):579-91. View abstract
  58. Madsen JR, MacDonald P, Irwin N, Goldberg DE, Yao GL, Meiri KF, Rimm IJ, Stieg PE, Benowitz LI. Tacrolimus (FK506) increases neuronal expression of GAP-43 and improves functional recovery after spinal cord injury in rats. Exp Neurol. 1998 Dec; 154(2):673-83. View abstract
  59. Benowitz LI, Jing Y, Tabibiazar R, Jo SA, Petrausch B, Stuermer CA, Rosenberg PA, Irwin N. Axon outgrowth is regulated by an intracellular purine-sensitive mechanism in retinal ganglion cells. J Biol Chem. 1998 Nov 06; 273(45):29626-34. View abstract
  60. Kawamata T, Dietrich WD, Schallert T, Gotts JE, Cocke RR, Benowitz LI, Finklestein SP. Intracisternal basic fibroblast growth factor enhances functional recovery and up-regulates the expression of a molecular marker of neuronal sprouting following focal cerebral infarction. Proc Natl Acad Sci U S A. 1997 Jul 22; 94(15):8179-84. View abstract
  61. Irwin N, Baekelandt V, Goritchenko L, Benowitz LI. Identification of two proteins that bind to a pyrimidine-rich sequence in the 3'-untranslated region of GAP-43 mRNA. Nucleic Acids Res. 1997 Mar 15; 25(6):1281-8. View abstract
  62. Benowitz LI, Routtenberg A. GAP-43: an intrinsic determinant of neuronal development and plasticity. Trends Neurosci. 1997 Feb; 20(2):84-91. View abstract
  63. Perrone-Bizzozero NI, Sower AC, Bird ED, Benowitz LI, Ivins KJ, Neve RL. Levels of the growth-associated protein GAP-43 are selectively increased in association cortices in schizophrenia. Proc Natl Acad Sci U S A. 1996 Nov 26; 93(24):14182-7. View abstract
  64. Chao S, Benowitz LI, Krainc D, Irwin N. Use of a two-hybrid system to investigate molecular interactions of GAP-43. Brain Res Mol Brain Res. 1996 Sep 01; 40(2):195-202. View abstract
  65. Schwalb JM, Gu MF, Stuermer C, Bastmeyer M, Hu GF, Boulis N, Irwin N, Benowitz LI. Optic nerve glia secrete a low-molecular-weight factor that stimulates retinal ganglion cells to regenerate axons in goldfish. Neuroscience. 1996 Jun; 72(4):901-10. View abstract
  66. Lu CR, Meng FT, Benowitz LI, Ju G. Evidence for axonal sprouting in the anterior pituitary following adrenalectomy in the rat. J Endocrinol. 1995 Oct; 147(1):161-6. View abstract
  67. Schwalb JM, Boulis NM, Gu MF, Winickoff J, Jackson PS, Irwin N, Benowitz LI. Two factors secreted by the goldfish optic nerve induce retinal ganglion cells to regenerate axons in culture. J Neurosci. 1995 Aug; 15(8):5514-25. View abstract
  68. Shea TB, Benowitz LI. Inhibition of neurite outgrowth following intracellular delivery of anti-GAP-43 antibodies depends upon culture conditions and method of neurite induction. J Neurosci Res. 1995 Jun 15; 41(3):347-54. View abstract
  69. Meyer RL, Miotke JA, Benowitz LI. Injury induced expression of growth-associated protein-43 in adult mouse retinal ganglion cells in vitro. Neuroscience. 1994 Nov; 63(2):591-602. View abstract
  70. Chong MS, Reynolds ML, Irwin N, Coggeshall RE, Emson PC, Benowitz LI, Woolf CJ. GAP-43 expression in primary sensory neurons following central axotomy. J Neurosci. 1994 Jul; 14(7):4375-84. View abstract
  71. Moya KL, Benowitz LI, Schneider GE, Allinquant B. The amyloid precursor protein is developmentally regulated and correlated with synaptogenesis. Dev Biol. 1994 Feb; 161(2):597-603. View abstract
  72. Paden CM, Moffett CW, Benowitz LI. Innervation of the rat anterior and neurointermediate pituitary visualized by immunocytochemistry for the growth-associated protein GAP-43. Endocrinology. 1994 Jan; 134(1):503-6. View abstract
  73. Schaechter JD, Benowitz LI. Activation of protein kinase C by arachidonic acid selectively enhances the phosphorylation of GAP-43 in nerve terminal membranes. J Neurosci. 1993 Oct; 13(10):4361-71. View abstract
  74. Kinney HC, Rava LA, Benowitz LI. Anatomic distribution of the growth-associated protein GAP-43 in the developing human brainstem. J Neuropathol Exp Neurol. 1993 Jan; 52(1):39-54. View abstract
  75. Winter J, Evison CJ, O'Brien C, Benowitz L, Lindsay RM, Mulderry P, Woolf C. Neurotoxic damage evokes regenerative responses from adult rat sensory neurones. Neurosci Lett. 1992 Oct 26; 146(1):48-52. View abstract
  76. Woolf CJ, Reynolds ML, Chong MS, Emson P, Irwin N, Benowitz LI. Denervation of the motor endplate results in the rapid expression by terminal Schwann cells of the growth-associated protein GAP-43. J Neurosci. 1992 Oct; 12(10):3999-4010. View abstract
  77. Gossels JM, Lewis SE, Perrone-Bizzozero NI, Benowitz LI. Changes in chromatin proteins during optic nerve regeneration in the goldfish. J Neurosci Res. 1992 Sep; 33(1):112-21. View abstract
  78. Moya KL, Benowitz LI, Sabel BA, Schneider GE. Changes in rapidly transported proteins associated with development of abnormal projections in the diencephalon. Brain Res. 1992 Jul 24; 586(2):265-72. View abstract
  79. Dunn-Meynell AA, Benowitz LI, Levin BE. Vibrissectomy induced changes in GAP-43 immunoreactivity in the adult rat barrel cortex. J Comp Neurol. 1992 Jan 08; 315(2):160-70. View abstract
  80. Perrone-Bizzozero NI, Neve RL, Irwin N, Lewis S, Fischer I, Benowitz LI. Post-transcriptional regulation of GAP-43 rnRNA levels during neuronal differentiation and nerve regeneration. Mol Cell Neurosci. 1991 Oct; 2(5):402-9. View abstract
  81. Shea TB, Perrone-Bizzozero NI, Beermann ML, Benowitz LI. Phospholipid-mediated delivery of anti-GAP-43 antibodies into neuroblastoma cells prevents neuritogenesis. J Neurosci. 1991 Jun; 11(6):1685-90. View abstract
  82. Reynolds ML, Fitzgerald M, Benowitz LI. GAP-43 expression in developing cutaneous and muscle nerves in the rat hindlimb. Neuroscience. 1991; 41(1):201-11. View abstract
  83. Fitzgerald M, Reynolds ML, Benowitz LI. GAP-43 expression in the developing rat lumbar spinal cord. Neuroscience. 1991; 41(1):187-99. View abstract
  84. Benowitz LI, Perrone-Bizzozero NI. The expression of GAP-43 in relation to neuronal growth and plasticity: when, where, how, and why? Prog Brain Res. 1991; 89:69-87. View abstract
  85. Dani JW, Armstrong DM, Benowitz LI. Mapping the development of the rat brain by GAP-43 immunocytochemistry. Neuroscience. 1991; 40(1):277-87. View abstract
  86. Benowitz LI, Perrone-Bizzozero NI. The relationship of GAP-43 to the development and plasticity of synaptic connections. Ann N Y Acad Sci. 1991; 627:58-74. View abstract
  87. Neve RL, Ivins KJ, Benowitz LI, During MJ, Geller AI. Molecular analysis of the function of the neuronal growth-associated protein GAP-43 by genetic intervention. Mol Neurobiol. 1991; 5(2-4):131-41. View abstract
  88. DiFiglia M, Roberts RC, Benowitz LI. Immunoreactive GAP-43 in the neuropil of adult rat neostriatum: localization in unmyelinated fibers, axon terminals, and dendritic spines. J Comp Neurol. 1990 Dec 22; 302(4):992-1001. View abstract
  89. Moya KL, Benowitz LI, Schneider GE. Abnormal retinal projections alter GAP-43 patterns in the diencephalon. Brain Res. 1990 Sep 17; 527(2):259-65. View abstract
  90. Benowitz LI, Rodriguez WR, Neve RL. The pattern of GAP-43 immunostaining changes in the rat hippocampal formation during reactive synaptogenesis. Brain Res Mol Brain Res. 1990 Jun; 8(1):17-23. View abstract
  91. Erzurumlu RS, Jhaveri S, Benowitz LI. Transient patterns of GAP-43 expression during the formation of barrels in the rat somatosensory cortex. J Comp Neurol. 1990 Feb 15; 292(3):443-56. View abstract
  92. Yankner BA, Benowitz LI, Villa-Komaroff L, Neve RL. Transfection of PC12 cells with the human GAP-43 gene: effects on neurite outgrowth and regeneration. Brain Res Mol Brain Res. 1990 Jan; 7(1):39-44. View abstract
  93. Woolf CJ, Reynolds ML, Molander C, O'Brien C, Lindsay RM, Benowitz LI. The growth-associated protein GAP-43 appears in dorsal root ganglion cells and in the dorsal horn of the rat spinal cord following peripheral nerve injury. Neuroscience. 1990; 34(2):465-78. View abstract
  94. Neve RL, Dawes LR, Yankner BA, Benowitz LI, Rodriguez W, Higgins GA. Genetics and biology of the Alzheimer amyloid precursor. Prog Brain Res. 1990; 86:257-67. View abstract
  95. Benowitz LI, Moya KL, Levine DN. Impaired verbal reasoning and constructional apraxia in subjects with right hemisphere damage. Neuropsychologia. 1990; 28(3):231-41. View abstract
  96. Benowitz LI, Perrone-Bizzozero NI, Neve RL, Rodriguez W. GAP-43 as a marker for structural plasticity in the mature CNS. Prog Brain Res. 1990; 86:309-20. View abstract
  97. Benowitz LI, Rodriguez W, Paskevich P, Mufson EJ, Schenk D, Neve RL. The amyloid precursor protein is concentrated in neuronal lysosomes in normal and Alzheimer disease subjects. Exp Neurol. 1989 Dec; 106(3):237-50. View abstract
  98. Moya KL, Jhaveri S, Schneider GE, Benowitz LI. Immunohistochemical localization of GAP-43 in the developing hamster retinofugal pathway. J Comp Neurol. 1989 Oct 01; 288(1):51-8. View abstract
  99. Erzurumlu RS, Jhaveri S, Moya KL, Benowitz LI. Peripheral nerve regeneration induces elevated expression of GAP-43 in the brainstem trigeminal complex of adult hamsters. Brain Res. 1989 Sep 25; 498(1):135-9. View abstract
  100. Perrone-Bizzozero NI, Benowitz LI, Apostolides PJ, Franck ER, Finklestein SP, Bizzozero OA. Protein fatty acid acylation in developing cortical neurons. J Neurochem. 1989 Apr; 52(4):1149-55. View abstract
  101. Benowitz LI, Perrone-Bizzozero NI, Finklestein SP, Bird ED. Localization of the growth-associated phosphoprotein GAP-43 (B-50, F1) in the human cerebral cortex. J Neurosci. 1989 Mar; 9(3):990-5. View abstract
  102. Caday CG, Apostolides PJ, Benowitz LI, Perrone-Bizzozero NI, Finklestein SP. Partial purification and characterization of a neurite-promoting factor from the injured goldfish optic nerve. Brain Res Mol Brain Res. 1989 Jan; 5(1):45-50. View abstract
  103. Moya KL, Benowitz LI, Jhaveri S, Schneider GE. Changes in rapidly transported proteins in developing hamster retinofugal axons. J Neurosci. 1988 Dec; 8(12):4445-54. View abstract
  104. Daniels EK, Shenton ME, Holzman PS, Benowitz LI, Coleman M, Levin S, Levine D. Patterns of thought disorder associated with right cortical damage, schizophrenia, and mania. Am J Psychiatry. 1988 Aug; 145(8):944-9. View abstract
  105. Perrone-Bizzozero NI, Weiner D, Hauser G, Benowitz LI. Extraction of major acidic Ca2+ dependent phosphoproteins from synaptic membranes. J Neurosci Res. 1988 Jul; 20(3):346-50. View abstract
  106. Finklestein SP, Apostolides PJ, Caday CG, Philips MF, Perrone-Bizzozero NI, Benowitz LI. A factor from the injured lower vertebrate CNS promotes outgrowth from human fetal brain neurons. Brain Res. 1988 May 17; 448(2):346-50. View abstract
  107. Neve RL, Finch EA, Bird ED, Benowitz LI. Growth-associated protein GAP-43 is expressed selectively in associative regions of the adult human brain. Proc Natl Acad Sci U S A. 1988 May; 85(10):3638-42. View abstract
  108. Kosik KS, Orecchio LD, Bruns GA, Benowitz LI, MacDonald GP, Cox DR, Neve RL. Human GAP-43: its deduced amino acid sequence and chromosomal localization in mouse and human. Neuron. 1988 Apr; 1(2):127-32.View abstract
  109. Benowitz LI, Apostolides PJ, Perrone-Bizzozero N, Finklestein SP, Zwiers H. Anatomical distribution of the growth-associated protein GAP-43/B-50 in the adult rat brain. J Neurosci. 1988 Jan; 8(1):339-52. View abstract
  110. Haber S, Finklestein SD, Benowitz LI, Collier TJ. Matrigel enhances survival and integration of grafted dopamine neurons into the striatum. Prog Brain Res. 1988; 78:427-33. View abstract
  111. Benowitz LI, Schmidt JT. Activity-dependent sharpening of the regenerating retinotectal projection in goldfish: relationship to the expression of growth-associated proteins. Brain Res. 1987 Aug 04; 417(1):118-26. View abstract
  112. Neve RL, Perrone-Bizzozero NI, Finklestein S, Zwiers H, Bird E, Kurnit DM, Benowitz LI. The neuronal growth-associated protein GAP-43 (B-50, F1): neuronal specificity, developmental regulation and regional distribution of the human and rat mRNAs. Brain Res. 1987 Jul; 388(2):177-83. View abstract
  113. Finklestein SP, Benowitz LI, Olson AJ, Perrone-Bizzozero NI, Majocha RE, Apostolides PJ. Conditioned media from the injured lower vertebrate CNS promote neurite outgrowth from mammalian brain neurons in vitro. Brain Res. 1987 Jun 16; 413(2):267-74. View abstract
  114. Katz DL, Frankenburg FR, Benowitz LI, Gilbert JM. Psychosis and prenatal exposure to diethylstilbestrol. J Nerv Ment Dis. 1987 May; 175(5):306-8. View abstract
  115. Benowitz LI, Perrone-Bizzozero NI, Finklestein SP. Molecular properties of the growth-associated protein GAP-43 (B-50). J Neurochem. 1987 May; 48(5):1640-7. View abstract
  116. Moya KL, Benowitz LI, Jhaveri S, Schneider GE. Enhanced visualization of axonally transported proteins in the immature CNS by suppression of systemic labeling. Brain Res. 1987 Feb; 428(2):183-91. View abstract
  117. Perrone-Bizzozero NI, Benowitz LI. Expression of a 48-kilodalton growth-associated protein in the goldfish retina. J Neurochem. 1987 Feb; 48(2):644-52. View abstract
  118. Perrone-Bizzozero NI, Finklestein SP, Benowitz LI. Synthesis of a growth-associated protein by embryonic rat cerebrocortical neurons in vitro. J Neurosci. 1986 Dec; 6(12):3721-30. View abstract
  119. Yoon MG, Benowitz LI, Baker FA. The optic tectum regulates the transport of specific proteins in regenerating optic fibers of goldfish. Brain Res. 1986 Sep 24; 382(2):339-51. View abstract
  120. Moya KL, Benowitz LI, Levine DN, Finklestein S. Covariant defects in visuospatial abilities and recall of verbal narrative after right hemisphere stroke. Cortex. 1986 Sep; 22(3):381-97. View abstract
  121. Levine DN, Warach JD, Benowitz L, Calvanio R. Left spatial neglect: effects of lesion size and premorbid brain atrophy on severity and recovery following right cerebral infarction. Neurology. 1986 Mar; 36(3):362-6. View abstract
  122. Strocchi P, Gilbert JM, Benowitz LI, Dahl D, Lewis ER. Cellular origin and biosynthesis of rat optic nerve proteins: a two-dimensional gel analysis. J Neurochem. 1984 Aug; 43(2):349-57. View abstract
  123. Benowitz LI, Lewis ER. Increased transport of 44,000- to 49,000-dalton acidic proteins during regeneration of the goldfish optic nerve: a two-dimensional gel analysis. J Neurosci. 1983 Nov; 3(11):2153-63. View abstract
  124. Benowitz LI, Yoon MG, Lewis ER. Transported proteins in the regenerating optic nerve: regulation by interactions with the optic tectum. Science. 1983 Oct 14; 222(4620):185-8. View abstract
  125. Benowitz LI, Bear DM, Rosenthal R, Mesulam MM, Zaidel E, Sperry RW. Hemispheric specialization in nonverbal communication. Cortex. 1983 Apr; 19(1):5-11. View abstract
  126. Finklestein S, Benowitz LI, Baldessarini RJ, Arana GW, Levine D, Woo E, Bear D, Moya K, Stoll AL. Mood, vegetative disturbance, and dexamethasone suppression test after stroke. Ann Neurol. 1982 Nov; 12(5):463-8. View abstract
  127. Benowitz LI, Shashoua VE, Yoon MG. Specific changes in rapidly transported proteins during regeneration of the goldfish optic nerve. J Neurosci. 1981 Mar; 1(3):300-7. View abstract
  128. Benowitz LI, Shashoua VE. Immunoreactive sites for nerve growth factor (NGF) in the goldfish brain. Brain Res. 1979 Aug 31; 172(3):561-5. View abstract
  129. Benowitz LI, Shashoua VE. Rapidly labeled and secreted proteins of the chick brain. J Neurochem. 1979 Mar; 32(3):797-809. View abstract
  130. Benowitz LI, Greene LA. Nerve growth factor in the goldfish brain: biological assay studies using pheochromocytoma cells. Brain Res. 1979 Feb 16; 162(1):164-8. View abstract
  131. Benowitz LI, Shashoua VE. Localization of a brain protein metabolically linked with behavioral plasticity in the goldfish. Brain Res. 1977 Nov 11; 136(2):227-42. View abstract
  132. Benowitz LI, Karten HJ. Organization of the tectofugal visual pathway in the pigeon: a retrograde transport study. J Comp Neurol. 1976 Jun 15; 167(4):503-20. View abstract
  133. Benowitz LI, Karten HJ. The tractus infundibuli and other afferents to the parahippocampal region of the pigeon. Brain Res. 1976 Jan 30; 102(1):174-80. View abstract
  134. Benowitz L. Conditions for the bilateral transfer of monocular learning in chicks. Brain Res. 1974 Jan 11; 65(2):203-13. View abstract
  135. Benowitz LI, Sperry RW. Amnesic effects of lithium chloride in chicks. Exp Neurol. 1973 Aug; 40(2):540-6. View abstract
  136. Benowitz L, Teng EL. Contrasting effects of three forebrain ablations on discrimination learning and reversal in chicks. J Comp Physiol Psychol. 1973 Aug; 84(2):391-7. View abstract
  137. Benowitz L, Magnus JG. Memory storage processes following one-trial aversive conditioning in the chick. Behav Biol. 1973 Mar; 8(3):367-80. View abstract
  138. Benowitz L. Effects of forebrain ablations on avoidance learning in chicks. Physiol Behav. 1972 Oct; 9(4):601-8. View abstract