About My Research
Mass Eye and Ear Titles
Director, Cornea and Refractive Surgery Service
Associate Chief for Academic Programs
W. Clement Stone Clinical Research Scholar
Senior Scientist, Laboratory of Corneal Immunology, Transplantation and Regeneration
Harvard Medical School Titles
Director, Harvard-Vision Clinical Scientist Development Program
Co-Director, Cornea Center of Excellence
Member, PhD Program in Immunology
Center/Research Area Affiliations
Biography
Dr. Reza Dana is an internationally recognized expert in corneal disorders and ocular inflammation. He conducts both basic and translational research in the field of corneal and transplantation immunology. At Schepens Eye Research Institute of Mass. Eye and Ear, he studies the molecular and cellular mechanisms of ocular inflammation with applications to autoimmunity, transplantation, dry eye disease, and angiogenesis.
A Gold Fellow of the Association for Research in Vision and Ophthalmology (ARVO), he has authored more than 480 peer-reviewed articles and over 150 reviews and book chapters, and has presented more than 250 invited and named lectures worldwide. His published work has been cited more than 36,000 times and has an h-index of 94. Dr. Dana's translational research has led to several successful physician-sponsored IND applications to the FDA. His research is supported by several NIH and other federal grants.
Dr. Dana has trained more than 95 clinical fellows, and 140 postdoctoral fellows and students in his laboratory from over 36 countries to date, the significant majority holding full-time academic positions in ophthalmology and vision research. He is recipient of the Harvard Medical School A. Clifford Barger Excellence in Mentoring Award, ARVO’s Cogan (2003) and Fridenwald (2018) awards, the Ellis Island Medal of Honor (2019), as well as ISER’s Endre A. Balazs Prize (2016) and the Stein Innovation Award from Research to Prevent Blindness (2018)
Research Interests
Dr. Dana is an ophthalmologist and immunologist whose principal research interest is in determining the molecular and cellular regulation of corneal and ocular surface immunity. His laboratory focuses on the role of cytokines and chemokines in the induction of antigen-specific corneal immunity, activation of antigen-presenting cells, and the interface of hemangiogenesis and lymphangiogenesis in inflammation. Other areas of active research include the dysfunction of regulatory T cells in autoimmunity,and dry eye disease, and high-risk corneal transplantation. In addition, his group has broadened its focus to include novel animal models for high-risk corneal stem cell transplantation, keratoprosthesis and biosynthetic corneal constructs.
Dr. Dana leads one of the most active translational programs in ophthalmology. As of last count, 50+ prospective investigator-initiated studies were being performed by the Cornea Center faculty. Studies have focused on novel strategies to manage high-risk corneal and stem cell transplants, pathological corneal angiogenesis, dry eye, graft-versus-host disease (GVHD) and in vivo corneal immuno- and neuro-imaging. These studies have been facilitated by 15 successful FDA Investigational New Drug (IND) approvals received since 2008.
Dr. Dana has delivered more than 250 invited and named lectures worldwide, and has received multiple awards, including the Friedenwald Award from the Association for Research in Vision and Ophthalmology (ARVO), the Endre Balazs Prize from International Society for Eye Research, Research to Prevent Blindness (RPB) William and Mary Greve Special Scholar Award, RPB Physician-Scientist Merit Award, RPB Lew Wasserman Merit Award, the RPB Senior Investigator Award, the Achievement Award of the American Academy of Ophthalmology, the Cogan Award of ARVO, the Louisiana State University Chancellor’s Award in Neuroscience and Ophthalmology, and the Alcon Research Institute Award, among many others.
Teaching and Mentoring
A Harvard Medical School Clifford Barger Excellence in Mentoring Award recipient, Dr. Dana has focused extensively on teaching both clinical and basic researchers, which includes postdoctoral research fellows, clinical fellows and residents, medical students, and graduate students enrolled in various Harvard Medical School curricula. He has served as primary mentor to more than 140 laboratory trainees from 36 countries, as well as more than 95 clinical fellows. A strong advocate for clinical scientists in bridging the wide gap between basic science and clinical applications, he directs the Harvard-Vision Clinical Scientist Development Program—funded by the NIH K12 mechanism—with the express intent of recruiting, training, and retaining the brightest young minds to Harvard to contribute to our research efforts. He has served as PI/Director for this program since its inception at Harvard Ophthalmology in 2004.
Education
BA, Johns Hopkins University (1985)
MPH, Johns Hopkins University (1989)
MD, Johns Hopkins University (1989)
MSc, Health Care Management, Harvard University (2005)
Postgraduate Training
Internship: Greater Baltimore Medical Center (1989-1990)
Residency: Illinois Eye & Ear Infirmary (1990-1993)
Clinical Fellowship in Cornea and External Diseases: Wills Eye Hospital (1993-1994)
Clinical Fellowship in Immunology and Uveitis: Mass Eye and Ear (1994-1995)
Research Fellowship in Ocular and Transplantation Immunology: Schepens Eye Research Institute, Harvard Medical School (1994-1996)
Academic Appointments
1995: Instructor in Ophthalmology, Harvard Medical School
1997: Assistant Professor of Ophthalmology and Assistant Scientist, Schepens Eye Research Institute of Mass Eye and Ear
2000: Associate Professor of Ophthalmology, Harvard Medical School and Associate Scientist, Schepens Eye Research Institute of Mass Eye and Ear
2002-present: W. Clement Stone Scholar
2004-present: Senior Scientist, Schepens Eye Research Institute of Mass Eye and Ear
2006-present: Director of the Cornea and Refractive Surgery Service of Mass Eye and Ear
2007-present: Claes Dohlman Chair in Ophthalmology, Harvard Medical School
2008-present: Vice Chair for Academic Programs, Ophthalmology, Harvard Medical School and Associate Chief for Academic Programs, Mass Eye and Ear
Honors
2021: Susruta Lecture, University of Pittsburgh
2021: Bowman Club-David Easty Lecture, UK
2021: Snell Memorial Lecture, University of Rochester
2020: The Ophthalmologist ‘Power List’ 2020
2019: Champalimaud Lecture, LV Prasad Eye Institute
2019: Ellis Island Medal of Honor, New York NY
2018: C. Stephen and Frances Foster Lectureship, Duke University
2018: Honorary Keynote Lecture, 120th Korean Ophthalmological Society
2018: Stein Innovation Award, Research to Prevent Blindness
2018: Friedenwald Award, Association for Research in Vision and Ophthalmology (ARVO)
2017: Streilein Lecture, 30th Biennial Cornea Conference
2017: Senior Achievement Award, American Academy of Ophthalmology
2017: Plenary Address, 121st Meeting of the Japanese Ophthalmological Society
2016: Endre A. Balazs Prize, International Society for Eye Research
2016: Mooney Lecture, Irish College of Ophthalmologists, Rep. Ireland
2016: Elected, Academia Ophthalmologica Internationalis
2016: Roger Meyer Lecture, University of Michigan Kellogg Eye Center
2015: Keynote Address and Certificate of Honor, European Association for Vision and Eye Research
2015: Kersley Lecture, British Ocular Surface Society, London, England
2014: Thygeson Lecture, Ocular Microbiology and Immunology Group
2014: A. Clifford Barger Excellence in Mentoring Award, Harvard Medical School
2013: Keynote Speaker, European Society of Ophthalmology (SOE), Copenhagen, Denmark
2013: Gold Fellow, ARVO
2013: Senior Scientific Investigator Award, Research to Prevent Blindness
2012: Mentoring Award, European Young Investigator Network for Ocular Surface Inflammation
2012: LSU Chancellor’s Award in Neuroscience and Ophthalmology
2011: Joaquin Barraquer Lecture, Spanish Congress of Ophthalmology
2011: David Easty Lecturer, Bowman Club, Royal College of Surgeons, Edinburgh
2009: Research to Prevent Blindness Lew R. Wasserman-Merit Award
2008: Alcon Research Institute Award
2006: Service Recognition Award, American Academy of Ophthalmology
2005: Research to Prevent Blindness Physician Scientist-Merit Award
2004: Keynote Address, 28th All-Japan Cornea Conference, Yonago, Japan
2004: Alta Lecturer and visiting professorship, Univ. California San Francisco
2003: Dohlman Lecturer, Boston Biennial Cornea Conference
2003: Cogan Award, Association for Research In Vision and Ophthalmology
2002: Fry Memorial Lecturer, Wills Eye Hospital Biennial Cornea Conference
2002: Kronfeld Memorial Lecturer, Illinois Eye & Ear Infirmary
2002: Achievement Award, American Academy of Ophthalmology
1999: Research to Prevent Blindness William & Mary Greve Special Scholar
1996: Clinical Scientist Career Award (K08), National Institutes of Health
- Visual outcomes of children undergoing penetrating keratoplasty in the US. Ocul Surf. 2024 Feb 23.
- Epidermal Growth Factor Receptor Inhibitors for Lung Cancer and the Risk of Keratitis. JAMA Ophthalmol. 2024 Feb 01; 142(2):140-145.
- Therapeutic Effects of Stimulating the Melanocortin Pathway in Regulating Ocular Inflammation and Cell Death. Biomolecules. 2024 Jan 31; 14(2).
- Effector T Cells Promote Fibrosis in Corneal Transplantation Failure. Invest Ophthalmol Vis Sci. 2024 Jan 02; 65(1):40.
- Concurrence of Ocular Cicatricial Pemphigoid in Chronic Ocular Graft-Versus-Host Disease. Cornea. 2024 Mar 01; 43(3):387-390.
- Corneal Superficial Plaque Formation After Recombinant Human Nerve Growth Factor Use in a Patient With Neurotrophic Keratopathy and Limbal Stem Cell Deficiency From Mucous Membrane Pemphigoid. Cornea. 2023 Nov 27.
- The Neuropeptide a-Melanocyte-Stimulating Hormone Prevents Persistent Corneal Edema following Injury. Am J Pathol. 2024 Jan; 194(1):150-164.
- Insights into mustard gas keratopathy- characterizing corneal layer-specific changes in mice exposed to nitrogen mustard. Exp Eye Res. 2023 11; 236:109657.
- Cultivated autologous limbal epithelial cell (CALEC) transplantation: Development of manufacturing process and clinical evaluation of feasibility and safety. Sci Adv. 2023 08 18; 9(33):eadg6470.
- Opposing Roles of Blood-Borne Monocytes and Tissue-Resident Macrophages in Limbal Stem Cell Damage after Ocular Injury. Cells. 2023 08 18; 12(16).
- Innate Immune Cytokine Levels in Eyes With Late Endothelial Keratoplasty Failure. Cornea. 2024 Apr 01; 43(4):432-436.
- The impact of donor diabetes on corneal transplant immunity. Am J Transplant. 2023 09; 23(9):1345-1358.
- Possible Strategies to Mitigate Placebo or Vehicle Response in Dry Eye Disease Trials: A Narrative Review. Ophthalmol Ther. 2023 Aug; 12(4):1827-1849.
- Insights into mustard gas keratopathy: Characterizing corneal layer-specific changes in mice exposed to nitrogen mustard. Exp Eye Res. 2023 May 02; 109495.
- Symptom-based stratification algorithm for heterogeneous symptoms of dry eye disease: a feasibility study. Eye (Lond). 2023 11; 37(16):3484-3491.
- Autologous serum tears improve corneal nerve density and sensitivity in patients with ocular graft-versus-host disease-associated dry eye disease. Ocul Surf. 2023 04; 28:37-39.
- Conventional type I migratory CD103+ dendritic cells are required for corneal allograft survival. Mucosal Immunol. 2023 Oct; 16(5):711-726.
- Amplified Natural Killer Cell Activity and Attenuated Regulatory T-cell Function Are Determinants for Corneal Alloimmunity in Very Young Mice. Transplantation. 2023 06 01; 107(6):1302-1310.
- Descemet Stripping Only Technique for Corneal Endothelial Damage in Mice. Cornea. 2023 Apr 01; 42(4):470-475.
- Multicenter prospective validation study for international chronic ocular graft-versus-host disease consensus diagnostic criteria. Ocul Surf. 2022 10; 26:200-208.
- Therapeutic efficacy of topical blockade of substance P in experimental allergic red eye. Ocul Surf. 2022 10; 26:184-190.
- Ocular pain in ocular graft-versus-host disease patients with neurotrophic keratopathy. Ocul Surf. 2022 10; 26:142-147.
- Prevalence of neurotrophic keratopathy in patients with chronic ocular graft-versus-host disease. Ocul Surf. 2022 Oct; 26:13-18.
- Modulating the tachykinin: Role of substance P and neurokinin receptor expression in ocular surface disorders. Ocul Surf. 2022 07; 25:142-153.
- Neurotrophic Keratopathy in the United States: An Intelligent Research in Sight Registry Analysis. Ophthalmology. 2022 11; 129(11):1255-1262.
- Impact of aging on the pathophysiology of dry eye disease: A systematic review and meta-analysis. Ocul Surf. 2022 07; 25:108-118.
- A Randomized Trial of Topical Fibrinogen-Depleted Human Platelet Lysate Treatment of Dry Eye Secondary to Chronic Graft-versus-Host Disease. Ophthalmol Sci. 2022 Sep; 2(3):100176.
- A Novel Murine Model of Endothelial Keratoplasty. Cornea. 2023 Feb 01; 42(2):224-231.
- DryEyeRhythm: A reliable and valid smartphone application for the diagnosis assistance of dry eye. Ocul Surf. 2022 07; 25:19-25.
- Autoreactive memory Th17 cells are principally derived from T-bet+ROR?t+ Th17/1 effectors. J Autoimmun. 2022 05; 129:102816.
- Bevacizumab in High-Risk Corneal Transplantation: A Pilot Multicenter Prospective Randomized Control Trial. Ophthalmology. 2022 08; 129(8):865-879.
- Immune regulation of the ocular surface. Exp Eye Res. 2022 05; 218:109007.
- Smartphone-based digital phenotyping for dry eye toward P4 medicine: a crowdsourced cross-sectional study. NPJ Digit Med. 2021 Dec 20; 4(1):171.
- The Neuropeptide Alpha-Melanocyte-Stimulating Hormone Is Critical for Corneal Endothelial Cell Protection and Graft Survival after Transplantation. Am J Pathol. 2022 02; 192(2):270-280.
- Novel adaptation of a running suture technique in a mouse model of corneal transplantation. J Biol Methods. 2021; 8(4):e156.
- Development and characterization of a hydrogel-based adhesive patch for sealing open-globe injuries. Acta Biomater. 2022 01 01; 137:53-63.
- Autoimmunity in dry eye disease - An updated review of evidence on effector and memory Th17 cells in disease pathogenicity. Autoimmun Rev. 2021 Nov; 20(11):102933.
- Expert consensus on the identification, diagnosis, and treatment of neurotrophic keratopathy. BMC Ophthalmol. 2021 Sep 08; 21(1):327.
- Preclinical Evaluation of the Safety and Efficacy of Cryopreserved Bone Marrow Mesenchymal Stromal Cells for Corneal Repair. Transl Vis Sci Technol. 2021 08 12; 10(10):3.
- Limbal Stem Cell Deficiency Associated With Herpes Keratitis. Cornea. 2021 Aug 01; 40(8):967-971.
- Corneal lymphangiogenesis in dry eye disease is regulated by substance P/neurokinin-1 receptor system through controlling expression of vascular endothelial growth factor receptor 3. Ocul Surf. 2021 10; 22:72-79.
- Dry eye disease flares: A rapid evidence assessment. Ocul Surf. 2021 10; 22:51-59.
- A Review of Ocular Graft-versus-Host Disease: Pathophysiology, Clinical Presentation and Management. Ocul Immunol Inflamm. 2021 Aug 18; 29(6):1190-1199.
- Prevalence and Risk Factors Associated With Corneal Perforation in Chronic Ocular Graft-Versus-Host-Disease. Cornea. 2021 Jul 01; 40(7):877-882.
- Management of belantamab mafodotin-associated corneal events in patients with relapsed or refractory multiple myeloma (RRMM). Blood Cancer J. 2021 05 26; 11(5):103.
- Ocular redness - I: Etiology, pathogenesis, and assessment of conjunctival hyperemia. Ocul Surf. 2021 07; 21:134-144.
- Ocular redness - II: Progress in development of therapeutics for the management of conjunctival hyperemia. Ocul Surf. 2021 07; 21:66-77.
- Chemical and thermal ocular burns in the United States: An IRIS registry analysis. Ocul Surf. 2021 07; 21:345-347.
- Advances in the Medical Management of Neurotrophic Keratitis. Semin Ophthalmol. 2021 May 19; 36(4):335-340.
- Advanced nanodelivery platforms for topical ophthalmic drug delivery. Drug Discov Today. 2021 06; 26(6):1437-1449.
- Patient-reported burden of dry eye disease in the UK: a cross-sectional web-based survey. BMJ Open. 2021 03 04; 11(3):e039209.
- Long-term Outcomes of Punctal Cauterization in the Management of Ocular Surface Diseases. Cornea. 2021 Feb 01; 40(2):168-171.
- Corneal angiogenic privilege and its failure. Exp Eye Res. 2021 03; 204:108457.
- Pigment Epithelium-Derived Factor Enhances the Suppressive Phenotype of Regulatory T Cells in a Murine Model of Dry Eye Disease. Am J Pathol. 2021 04; 191(4):720-729.
- Heterogeneity of eye drop use among symptomatic dry eye individuals in Japan: large-scale crowdsourced research using DryEyeRhythm application. Jpn J Ophthalmol. 2021 Mar; 65(2):271-281.
- Growth factor-eluting hydrogels for management of corneal defects. Mater Sci Eng C Mater Biol Appl. 2021 Jan; 120:111790.
- Defining Dry Eye from a Clinical Perspective. Int J Mol Sci. 2020 Dec 04; 21(23).
- Regulatory T Cells in Angiogenesis. J Immunol. 2020 11 15; 205(10):2557-2565.
- Association of a-Melanocyte-Stimulating Hormone With Corneal Endothelial Cell Survival During Oxidative Stress and Inflammation-Induced Cell Loss in Donor Tissue. JAMA Ophthalmol. 2020 11 01; 138(11):1192-1195.
- Global Consensus on the Management of Limbal Stem Cell Deficiency. Cornea. 2020 Oct; 39(10):1291-1302.
- Ciprofloxacin-loaded bioadhesive hydrogels for ocular applications. Biomater Sci. 2020 Sep 15; 8(18):5196-5209.
- Immune checkpoint inhibitors and corneal transplant rejection: a call for awareness. Immunotherapy. 2020 09; 12(13):947-949.
- Efficacy of cyanoacrylate tissue adhesive in the management of corneal thinning and perforation due to microbial keratitis. Ocul Surf. 2020 10; 18(4):795-800.
- Clinical and Prodromal Ocular Symptoms in Coronavirus Disease: A Systematic Review and Meta-Analysis. Invest Ophthalmol Vis Sci. 2020 08 03; 61(10):29.
- Efficacy and retention of silicone punctal plugs for treatment of dry eye in patients with and without ocular graft-versus-host-disease. Ocul Surf. 2020 10; 18(4):731-735.
- Animal models of high-risk corneal transplantation: A comprehensive review. Exp Eye Res. 2020 09; 198:108152.
- Prevalence of Persistent Corneal Epithelial Defects in Chronic Ocular Graft-Versus-Host Disease. Am J Ophthalmol. 2020 10; 218:296-303.
- Stratification of Individual Symptoms of Contact Lens-Associated Dry Eye Using the iPhone App DryEyeRhythm: Crowdsourced Cross-Sectional Study. J Med Internet Res. 2020 06 26; 22(6):e18996.
- Restoration of Regulatory T-Cell Function in Dry Eye Disease by Antagonizing Substance P/Neurokinin-1 Receptor. Am J Pathol. 2020 09; 190(9):1859-1866.
- The role of Th17 immunity in chronic ocular surface disorders. Ocul Surf. 2021 01; 19:157-168.
- Pigment Epithelium-derived Factor secreted by corneal epithelial cells regulates dendritic cell maturation in dry eye disease. Ocul Surf. 2020 07; 18(3):460-469.
- The functions of IL-23 and IL-2 on driving autoimmune effector T-helper 17 cells into the memory pool in dry eye disease. Mucosal Immunol. 2021 01; 14(1):177-186.
- Aged Mice Exhibit Severe Exacerbations of Dry Eye Disease with an Amplified Memory Th17 Cell Response. Am J Pathol. 2020 07; 190(7):1474-1482.
- Patient-Reported Burden of Dry Eye Disease in the United States: Results of an Online Cross-Sectional Survey. Am J Ophthalmol. 2020 08; 216:7-17.
- Sensory neurons directly promote angiogenesis in response to inflammation via substance P signaling. FASEB J. 2020 05; 34(5):6229-6243.
- Association between dry eye and depressive symptoms: Large-scale crowdsourced research using the DryEyeRhythm iPhone application. Ocul Surf. 2020 04; 18(2):312-319.
- Advances and limitations of drug delivery systems formulated as eye drops. J Control Release. 2020 05 10; 321:1-22.
- Characteristics and Risk Factors Associated With Diagnosed and Undiagnosed Symptomatic Dry Eye Using a Smartphone Application. JAMA Ophthalmol. 2020 01 01; 138(1):58-68.
- Letter From the New Editor-in-Chief. Cornea. 2020 01; 39(1):1.
- Reply. Cornea. 2019 12; 38(12):e56-e57.
- Low-Dose IL-2 Therapy in Transplantation, Autoimmunity, and Inflammatory Diseases. J Immunol. 2019 12 01; 203(11):2749-2755.
- A standardized methodology for longitudinal assessment of corneal endothelial morphometry in eye banked corneas. J Biol Methods. 2019; 6(4):e120.
- Authors' Response. Optom Vis Sci. 2019 11; 96(11):892.
- Regulatory T cells promote corneal endothelial cell survival following transplantation via interleukin-10. Am J Transplant. 2020 02; 20(2):389-398.
- Neurokinin-1 Receptor Antagonism Ameliorates Dry Eye Disease by Inhibiting Antigen-Presenting Cell Maturation and T Helper 17 Cell Activation. Am J Pathol. 2020 01; 190(1):125-133.
- Limbal and Conjunctival Epithelial Thickness in Ocular Graft-Versus-Host Disease. Cornea. 2019 Oct; 38(10):1286-1290.
- Management of meibomian gland dysfunction: a review. Surv Ophthalmol. 2020 Mar - Apr; 65(2):205-217.
- Topical Recombinant Human Nerve Growth Factor (Cenegermin) for Neurotrophic Keratopathy: A Multicenter Randomized Vehicle-Controlled Pivotal Trial. Ophthalmology. 2020 01; 127(1):14-26.
- Conjunctival HLA-DR Expression and Its Association With Symptoms and Signs in the DREAM Study. Transl Vis Sci Technol. 2019 Jul; 8(4):31.
- Keratoconus progression associated with hormone replacement therapy. Am J Ophthalmol Case Rep. 2019 Sep; 15:100519.
- The purinergic receptor antagonist oxidized adenosine triphosphate suppresses immune-mediated corneal allograft rejection. Sci Rep. 2019 06 13; 9(1):8617.
- Methods for Assessing Corneal Opacity. Semin Ophthalmol. 2019; 34(4):205-210.
- Thrombospondin-1 in ocular surface health and disease. Ocul Surf. 2019 07; 17(3):374-383.
- Outcomes of Cyanoacrylate Tissue Adhesive Application in Corneal Thinning and Perforation. Cornea. 2019 Jun; 38(6):668-673.
- Impact of Dry Eye on Visual Acuity and Contrast Sensitivity: Dry Eye Assessment and Management Study. Optom Vis Sci. 2019 06; 96(6):387-396.
- Retinal microglia initiate neuroinflammation in ocular autoimmunity. Proc Natl Acad Sci U S A. 2019 05 14; 116(20):9989-9998.
- Medical and surgical management of conjunctivochalasis. Ocul Surf. 2019 07; 17(3):393-399.
- Descemet Membrane Endothelial Keratoplasty Failure Associated with Innate Immune Activation. Ophthalmology. 2019 10; 126(10):1462-1464.
- Oral guaifenesin for treatment of filamentary keratitis: A pilot study. Ocul Surf. 2019 07; 17(3):565-570.
- Sutureless repair of corneal injuries using naturally derived bioadhesive hydrogels. Sci Adv. 2019 03; 5(3):eaav1281.
- Global Consensus on Definition, Classification, Diagnosis, and Staging of Limbal Stem Cell Deficiency. Cornea. 2019 Mar; 38(3):364-375.
- In Vivo Confocal Microscopy Demonstrates Increased Immune Cell Densities in Corneal Graft Rejection Correlating With Signs and Symptoms. Am J Ophthalmol. 2019 07; 203:26-36.
- Estimated Prevalence and Incidence of Dry Eye Disease Based on Coding Analysis of a Large, All-age United States Health Care System. Am J Ophthalmol. 2019 06; 202:47-54.
- Dry eye disease ranking among common reasons for seeking eye care in a large US claims database. Clin Ophthalmol. 2019; 13:225-232.
- Ocular adhesives: Design, chemistry, crosslinking mechanisms, and applications. Biomaterials. 2019 03; 197:345-367.
- Local Delivery of Regulatory T Cells Promotes Corneal Allograft Survival. Transplantation. 2019 01; 103(1):182-190.
- Microglia Regulate Neuroglia Remodeling in Various Ocular and Retinal Injuries. J Immunol. 2019 01 15; 202(2):539-549.
- Risk Factors for Severe Dry Eye Disease: Crowdsourced Research Using DryEyeRhythm. Ophthalmology. 2019 05; 126(5):766-768.
- Permanent neuroglial remodeling of the retina following infiltration of CSF1R inhibition-resistant peripheral monocytes. Proc Natl Acad Sci U S A. 2018 11 27; 115(48):E11359-E11368.
- Comorbidities and Prescribed Medications in Patients With or Without Dry Eye Disease: A Population-Based Study. Am J Ophthalmol. 2019 02; 198:181-192.
- Regulatory T cell modulation of cytokine and cellular networks in corneal graft rejection. Curr Ophthalmol Rep. 2018 Dec; 6(4):266-274.
- Vasoactive Intestinal Peptide Promotes Corneal Allograft Survival. Am J Pathol. 2018 09; 188(9):2016-2024.
- The immunoregulatory role of corneal epithelium-derived thrombospondin-1 in dry eye disease. Ocul Surf. 2018 10; 16(4):470-477.
- Factors Influencing the Diagnostic Accuracy of Laser-Scanning In Vivo Confocal Microscopy for Acanthamoeba Keratitis. Cornea. 2018 Jul; 37(7):818-823.
- Corneal fluorescein staining and ocular symptoms but not Schirmer test are useful as indicators of response to treatment in chronic ocular GVHD. Ocul Surf. 2018 07; 16(3):377-381.
- Pathological conversion of regulatory T cells is associated with loss of allotolerance. Sci Rep. 2018 05 04; 8(1):7059.
- Meibomian Gland Dysfunction in Primary and Secondary Sjögren Syndrome. Ophthalmic Res. 2018; 59(4):193-205.
- The Role of Microglia and Peripheral Monocytes in Retinal Damage after Corneal Chemical Injury. Am J Pathol. 2018 07; 188(7):1580-1596.
- Reduced Efficacy of Low-dose Topical Steroids in Dry Eye Disease Associated With Graft-versus-Host Disease. Am J Ophthalmol. 2018 06; 190:17-23.
- A New Frontier in Curing Corneal Blindness. N Engl J Med. 2018 03 15; 378(11):1057-1058.
- Subtarsal Fibrosis Is Associated With Ocular Surface Epitheliopathy in Graft-Versus-Host Disease. Am J Ophthalmol. 2018 05; 189:102-110.
- Web-based longitudinal remote assessment of dry eye symptoms. Ocul Surf. 2018 04; 16(2):249-253.
- Chemical Burns of the Eye: The Role of Retinal Injury and New Therapeutic Possibilities. Cornea. 2018 Feb; 37(2):248-251.
- Cornea-Derived Mesenchymal Stromal Cells Therapeutically Modulate Macrophage Immunophenotype and Angiogenic Function. Stem Cells. 2018 05; 36(5):775-784.
- Therapeutic approaches for induction of tolerance and immune quiescence in corneal allotransplantation. Cell Mol Life Sci. 2018 05; 75(9):1509-1520.
- Corneal Tissue From Dry Eye Donors Leads to Enhanced Graft Rejection. Cornea. 2018 Jan; 37(1):95-101.
- Interleukin-6 neutralization prolongs corneal allograft survival. Curr Trends Immunol. 2018; 19:105-113.
- When Clarity Is Crucial: Regulating Ocular Surface Immunity. Trends Immunol. 2018 04; 39(4):288-301.
- Conjunctivochalasis: a systematic review. Surv Ophthalmol. 2018 Jul - Aug; 63(4):554-564.
- Scaling and maintenance of corneal thickness during aging. PLoS One. 2017; 12(10):e0185694.
- Corneal Mesenchymal Stromal Cells Are Directly Antiangiogenic via PEDF and sFLT-1. Invest Ophthalmol Vis Sci. 2017 10 01; 58(12):5507-5517.
- Transient Ingrowth of Lymphatic Vessels into the Physiologically Avascular Cornea Regulates Corneal Edema and Transparency. Sci Rep. 2017 08 03; 7(1):7227.
- Patients' Perceived Treatment Effectiveness in Dry Eye Disease. Cornea. 2017 Aug; 36(8):893-897.
- Reply. Am J Ophthalmol. 2017 10; 182:202-203.
- TFOS DEWS II Management and Therapy Report. Ocul Surf. 2017 07; 15(3):575-628.
- Evaluating Changes in Ocular Redness Using a Novel Automated Method. Transl Vis Sci Technol. 2017 Jul; 6(4):13.
- A Pilot Randomized Trial on Safety and Efficacy of a Novel Topical Combined Inhibitor of Janus Kinase 1/3 and Spleen Tyrosine Kinase for GVHD-Associated Ocular Surface Disease. Cornea. 2017 Jul; 36(7):799-804.
- Kinetics of Corneal Antigen Presenting Cells in Experimental Dry Eye Disease. BMJ Open Ophthalmol. 2017; 1(1):e000078.
- IFN-?-Expressing Th17 Cells Are Required for Development of Severe Ocular Surface Autoimmunity. J Immunol. 2017 08 01; 199(3):1163-1169.
- Review: The function of regulatory T cells at the ocular surface. Ocul Surf. 2017 10; 15(4):652-659.
- Determinants of Ocular Pain Severity in Patients With Dry Eye Disease. Am J Ophthalmol. 2017 Jul; 179:198-204.
- Evaluating Corneal Fluorescein Staining Using a Novel Automated Method. Invest Ophthalmol Vis Sci. 2017 05 01; 58(6):BIO168-BIO173.
- Sensitivity and Specificity of Laser-Scanning In Vivo Confocal Microscopy for Filamentous Fungal Keratitis: Role of Observer Experience. Am J Ophthalmol. 2017 Jul; 179:81-89.
- Treatment of donor corneal tissue with immunomodulatory cytokines: a novel strategy to promote graft survival in high-risk corneal transplantation. Sci Rep. 2017 04 20; 7(1):971.
- Mechanisms of Retinal Damage after Ocular Alkali Burns. Am J Pathol. 2017 Jun; 187(6):1327-1342.
- Kinetics of Angiogenic Responses in Corneal Transplantation. Cornea. 2017 Apr; 36(4):491-496.
- Proangiogenic Function of T Cells in Corneal Transplantation. Transplantation. 2017 04; 101(4):778-785.
- Exophiala phaeomuriformis Fungal Keratitis: Case Report and In Vivo Confocal Microscopy Findings. Eye Contact Lens. 2017 Mar; 43(2):e4-e6.
- Patients With Dry Eye Disease and Low Subbasal Nerve Density Are at High Risk for Accelerated Corneal Endothelial Cell Loss. Cornea. 2017 Feb; 36(2):196-201.
- T Cell-Derived Granulocyte-Macrophage Colony-Stimulating Factor Contributes to Dry Eye Disease Pathogenesis by Promoting CD11b+ Myeloid Cell Maturation and Migration. Invest Ophthalmol Vis Sci. 2017 02 01; 58(2):1330-1336.
- Elevated Neutrophil Elastase in Tears of Ocular Graft-Versus-Host Disease Patients. Am J Ophthalmol. 2017 Apr; 176:46-52.
- Systemic Immunomodulatory Strategies in High-risk Corneal Transplantation. J Ophthalmic Vis Res. 2017 Jan-Mar; 12(1):81-92.
- Novel Treatments for Corneal Angiogenesis. Int Ophthalmol Clin. 2017; 57(4):31-38.
- Impaired Function of Peripherally Induced Regulatory T Cells in Hosts at High Risk of Graft Rejection. Sci Rep. 2016 12 23; 6:39924.
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- Draining lymph nodes play an essential role in alloimmunity generated in response to high-risk corneal transplantation. Cornea. 2002 May; 21(4):405-9.
- Decreased levels of the goblet cell mucin MUC5AC in tears of patients with Sjögren syndrome. Invest Ophthalmol Vis Sci. 2002 Apr; 43(4):1004-11.
- Novel characterization of MHC class II-negative population of resident corneal Langerhans cell-type dendritic cells. Invest Ophthalmol Vis Sci. 2002 Mar; 43(3):639-46.
- Draining lymph nodes of corneal transplant hosts exhibit evidence for donor major histocompatibility complex (MHC) class II-positive dendritic cells derived from MHC class II-negative grafts. J Exp Med. 2002 Jan 21; 195(2):259-68.
- Sex steroids, meibomian gland dysfunction and evaporative dry eye in Sjögren's syndrome. Lupus. 2002; 11(10):667.
- Expression of vascular endothelial growth factor receptor-3 (VEGFR-3) in the conjunctiva--a potential link between lymphangiogenesis and leukocyte trafficking on the ocular surface. Adv Exp Med Biol. 2002; 506(Pt B):851-60.
- Impact of androgen deficiency on the lipid profiles in human meibomian gland secretions. Adv Exp Med Biol. 2002; 506(Pt A):449-58.
- Sex steroids, the meibomian gland and evaporative dry eye. Adv Exp Med Biol. 2002; 506(Pt A):389-99.
- Traumatic ruptured globe injuries in children. Int Ophthalmol Clin. 2002; 42(3):157-65.
- Correlations between nutrient intake and the polar lipid profiles of meibomian gland secretions in women with Sjögren's syndrome. Adv Exp Med Biol. 2002; 506(Pt A):441-7.
- Role of immunity and inflammation in corneal and ocular surface disease associated with dry eye. Adv Exp Med Biol. 2002; 506(Pt B):729-38.
- Economic and quality of life impact of dry eye symptoms in women with Sjögren's syndrome. Adv Exp Med Biol. 2002; 506(Pt B):1183-8.
- Epidemiology of dry eye syndrome. Adv Exp Med Biol. 2002; 506(Pt B):989-98.
- Hormone replacement therapy and dry eye syndrome. JAMA. 2001 Nov 07; 286(17):2114-9.
- Toward optimal health: the experts discuss dry eye syndrome. Interview by Jodi Godfrey Meisler. J Womens Health Gend Based Med. 2001 Oct; 10(8):725-9.
- Immune response to intragraft antigen in draining lymph nodes after corneal transplantation is mediated by interleukin-12. J Interferon Cytokine Res. 2001 Oct; 21(10):813-9.
- Phacoemulsification in patients after allogeneic bone marrow transplantation. Ophthalmology. 2001 Sep; 108(9):1682-7.
- Role of CD4+ and CD8+ T cells in allorecognition: lessons from corneal transplantation. J Immunol. 2001 Aug 15; 167(4):1891-9.
- Molecular mechanisms of immunity in corneal allotransplantation and xenotransplantation. Expert Rev Mol Med. 2001 Jul 16; 3(18):1-21.
- The critical role of lymph nodes in corneal alloimmunization and graft rejection. Invest Ophthalmol Vis Sci. 2001 May; 42(6):1293-8.
- Blockade of CD40-CD154 costimulatory pathway promotes survival of allogeneic corneal transplants. Invest Ophthalmol Vis Sci. 2001 Apr; 42(5):987-94.
- Visual rehabilitation in children with congenital hereditary endothelial dystrophy. Int Ophthalmol Clin. 2001; 41(4):9-18.
- Efficacy and tolerability outcomes after punctal occlusion with silicone plugs in dry eye syndrome. Am J Ophthalmol. 2001 Jan; 131(1):30-6.
- Interleukin-1 receptor antagonist therapy and induction of anterior chamber-associated immune deviation-type tolerance after corneal transplantation. Invest Ophthalmol Vis Sci. 2000 Dec; 41(13):4203-8.
- Effect of androgen deficiency on the human meibomian gland and ocular surface. J Clin Endocrinol Metab. 2000 Dec; 85(12):4874-82.
- Topical soluble tumor necrosis factor receptor type I suppresses ocular chemokine gene expression and rejection of allogeneic corneal transplants. Arch Ophthalmol. 2000 Dec; 118(12):1666-71.
- Twenty-five-year panorama of corneal immunology: emerging concepts in the immunopathogenesis of microbial keratitis, peripheral ulcerative keratitis, and corneal transplant rejection. Cornea. 2000 Sep; 19(5):625-43.
- Photodynamic biologic tissue glue in perforating rabbit corneal wounds. J Clin Laser Med Surg. 2000 Jun; 18(3):125-9.
- ICAM-1 deficiency suppresses host allosensitization and rejection of MHC-disparate corneal transplants. Transplantation. 2000 Mar 15; 69(5):1008-13.
- Differential chemokine gene expression in corneal transplant rejection. Invest Ophthalmol Vis Sci. 1999 Nov; 40(12):2892-7.
- Effect of topical interleukin-1 receptor antagonist (IL-1ra) on corneal allograft survival in presensitized hosts. Curr Eye Res. 1999 Nov; 19(5):456-9.
- Prevention of allergic eye disease by treatment with IL-1 receptor antagonist. Invest Ophthalmol Vis Sci. 1999 Nov; 40(12):3041-6.
- Role of tumor necrosis factor receptors TNFR-I (P55) and TNFR-II (P75) in corneal transplantation. Transplantation. 1999 Oct 15; 68(7):944-9.
- Androgens and dry eye in Sjögren's syndrome. Ann N Y Acad Sci. 1999 Jun 22; 876:312-24.
- Early expression of proinflammatory cytokines interleukin-1 and tumor necrosis factor-alpha after corneal transplantation. J Interferon Cytokine Res. 1999 Jun; 19(6):661-9.
- Expression of cell adhesion molecules on limbal and neovascular endothelium in corneal inflammatory neovascularization. Invest Ophthalmol Vis Sci. 1999 Jun; 40(7):1427-34.
- Does androgen insufficiency cause lacrimal gland inflammation and aqueous tear deficiency? Invest Ophthalmol Vis Sci. 1999 May; 40(6):1261-5.
- Anterior chamber-associated immune deviation, ocular immune privilege, and orthotopic corneal allografts. Transplant Proc. 1999 May; 31(3):1472-5.
- TNF-alpha regulates corneal Langerhans cell migration. J Immunol. 1999 Apr 01; 162(7):4235-9.
- High levels of plasma C-reactive protein and future risk of age-related cataract. Ann Epidemiol. 1999 Apr; 9(3):166-71.
- Corneal transplantation in young children with congenital hereditary endothelial dystrophy. Multicenter Pediatric Keratoplasty Study. Am J Ophthalmol. 1999 Apr; 127(4):373-8.
- Corneal transplantation in antibody-deficient hosts. Invest Ophthalmol Vis Sci. 1999 Jan; 40(1):250-3.
- Interleukin 1 receptor antagonist suppresses allosensitization in corneal transplantation. Arch Ophthalmol. 1998 Oct; 116(10):1351-7.
- Topical modulation of interleukin-1 activity in corneal neovascularization. Cornea. 1998 Jul; 17(4):403-9.
- The epidemic of Acanthamoeba keratitis: where do we stand? Cornea. 1998 Jan; 17(1):3-10.
- Androgen regulation of the meibomian gland. Adv Exp Med Biol. 1998; 438:327-31.
- Interleukin-1 receptor antagonist suppresses Langerhans cell activity and promotes ocular immune privilege. Invest Ophthalmol Vis Sci. 1998 Jan; 39(1):70-7.
- Immunity causing blindness: five different paths to herpes stromal keratitis. Immunol Today. 1997 Sep; 18(9):443-9.
- Topical interleukin 1 receptor antagonist promotes corneal transplant survival. Transplantation. 1997 May 27; 63(10):1501-7.
- Corneal topography after selective suture removal for astigmatism following keratoplasty. Ophthalmic Surg Lasers. 1997 Mar; 28(3):208-14.
- Visual outcomes prognosticators in juvenile rheumatoid arthritis-associated uveitis. Ophthalmology. 1997 Feb; 104(2):236-44.
- Loss and restoration of immune privilege in eyes with corneal neovascularization. Invest Ophthalmol Vis Sci. 1996 Nov; 37(12):2485-94.
- Prognosticators for visual outcome in sarcoid uveitis. Ophthalmology. 1996 Nov; 103(11):1846-53.
- Outcome of penetrating keratoplasty after ocular trauma in children. Arch Ophthalmol. 1995 Dec; 113(12):1503-7.
- Corneal neovascularization after penetrating keratoplasty. Cornea. 1995 Nov; 14(6):604-9.
- Positive donor rim culture in penetrating keratoplasty. Cornea. 1995 Sep; 14(5):457-62.
- The indications for and outcome in pediatric keratoplasty. A multicenter study. Ophthalmology. 1995 Aug; 102(8):1129-38.
- Suture erosion after penetrating keratoplasty. Cornea. 1995 May; 14(3):243-8.
- Predictors of occult scleral rupture. Ophthalmology. 1994 Dec; 101(12):1941-4.
- Dynamic shifts in corneal topography after radial and transverse keratotomy. Ophthalmology. 1994 Nov; 101(11):1818-26.
- Ocular manifestations of leprosy in a noninstitutionalized community in the United States. Arch Ophthalmol. 1994 May; 112(5):626-9.
- Artificial orbit for experimental surgery on the anterior segment. Arch Ophthalmol. 1994 Jan; 112(1):125-8.
- Spontaneous and traumatic vitreous hemorrhage. Ophthalmology. 1993 Sep; 100(9):1377-83.
- Contact lens failure in keratoconus management. Ophthalmology. 1992 Aug; 99(8):1187-92.
- Visual impairment in a rural Appalachian community. Prevalence and causes. JAMA. 1990 Nov 14; 264(18):2400-5.
- Low-dose ultraviolet-B irradiation of donor corneal endothelium and graft survival. Invest Ophthalmol Vis Sci. 1990 Nov; 31(11):2261-8.
- Pretreatment of donor corneal endothelium with ultraviolet-B irradiation. Transplant Proc. 1989 Feb; 21(1 Pt 3):3145-6.
- A comparison of six MMPI short forms: code type correspondence and indices of psychopathology. J Clin Psychol. 1983 Nov; 39(6):968-9.
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Identification of Novel APC Populations
Our studies let to several novel and unexpected discoveries. My lab was the first to discover several distinct populations of uniformly MHC class II— highly immature APCs (including epithelial Langerhans cells and stromal myeloid CD11c+ dendritic cells) in the central cornea (IOVS 2002, J Leuk Bio 2003), breaking a longstanding dogma that the cornea was devoid of functional antigen-presenting cells. We also showed that these immature/precursor myeloid populations can mature to acquire high levels of costimulatory molecules CD40 and CD80, as well as MHC class II expression as they egress the eye through selective upregulation of specific receptors to prime naïve T cells under conditions of inflammation. This discovery had practical implications, as it demonstrated how the cornea itself (including corneal transplants) can contribute to immunity through resident APC, a process known as ‘direct sensitization,’ particularly in states of high tissue inflammation (J Immunology 2004).
APC-Lymphatic Interactions
To determine precisely where and how corneal APC interact with T cells, we embarked on a series of investigations that established the local draining lymph nodes as the site of allosensitization (IOVS 2001; J Exp Med 2002). Remarkably, before these studies, the field was almost exclusively focused on APC-T cell interactions in the spleen. Subsequent studies showed that APC localization in these draining lymphoid tissues is reliant on a novel function of the VEGFR-3 receptor, known to be a growth factor for lymphatic and budding blood vessel endothelia. We determined that this receptor is acquired by mature MHC class IIhi dendritic cells in the cornea, and mediates their chemotactic mobilization into lymphatics, thereby allowing their egress from the inflamed eye. We also showed that blockade of this pathway can suppress the trafficking of APC from the eye to regional lymph nodes and suppress the induction of immunity to ocular antigens (Nature Medicine 2004). The identification of this novel role for VEGFR-3 in APC mobilization received considerable attention since subsquent work by others showed a similar mechanism to be operative for certain epithelial cancers and peritumor cells for gaining access to the lymphatic system for systemic spread.
Regulation of Corneal Angiogenesis and Lymphangiogenesis
Our studies on VEGFR-3 function stumbled us onto entirely unexpected insights into how corneal avascularity is maintained. We found high constitutive ‘ectopic’ expression of non-signaling VEGFR-3 by the corneal epithelium, and described how this “sink” mechanism for binding VEGF-C/D prevents their ligation of their receptors VEGFR-2/3, thereby functioning as a critical mechanism for maintaining corneal avascularity and regulating immunity (PNAS 2006). More recently, we have shown that this regulatory function can be subverted by IL-17 binding to epithelial cells, which have functional IL-17R signaling, inducing over-expression of VEGF-D by epithelial cells (Blood 2011).
Failure of Immunoregulatory Mechanisms in Inflammation
We have determined that Foxp3+ regulatory T cells (Tregs) become dysfunctional in hosts prone to reject allografts as well as in chronic ocular surface disease (J Immunology 2009). Our work has uncovered mechanisms that regulate Treg plasticity and regulatory breakdown in highly inflamed microenvironments, identifying different Treg phenotypes (Sci Reports 2016). We have identified Treg plasticity as a key factor in loss of allotolerance, and have defined novel strategies to (i) enhance Treg homing to the immune synapse (J Immunology 2014) and (ii) promote Treg expansion (Transplantation 2016) for induction of graft tolerance.
Dry Eye Disease (DED) Immunopathogenesis
Our work in corneal transplantation immunology permitted us since the mid-2000s to launch a program determining the immunopathogenesis of dry eye disease (DED), a chronic immune-mediated disease (and one of the most common reasons for patients seeking eye care) whose precise pathogenesis was barely understood even a few years earlier. We optimized a murine model for dry eye disease that did not rely on gene deletion or transgenic technology and used it in our basic research program to identify critical features in the immunopathogenesis of DED. Our work led to several novel discoveries, including identifying a select resistance of T helper-17 (Th17) cells, the principal pathogenic effectors in DED, to suppression by regulatory T cells (J Immunology 2009).
We subsequently showed that failure in Treg function in chronic DED leads not only to expansion of Th17 effectors but also development of classic immunologic memory mediated by effector memory IL-17 secreting cells (Mucosal Immunology 2014). Very recently, we have focused on the molecular mechanisms that lead to generation and maintenance of memory Th17 cells- an almost entirely unexplored area—and showed the critical function of IL-7 and IL-15 in this process (J Autoimmunity 2017).
Translational Research
In addition to these basic investigations, I am engaged in translational research. These projects have focused on novel immunomodulatory strategies to manage high-risk corneal and stem cell transplants, pathological corneal angiogenesis, graft-versus-host disease, dry eye, and in vivo corneal immuno- and neuro-imaging. Our group has been one of the first to develop and clinically test topical protein-based biologic approaches targeting specific inflammatory and pro-angiogenic cytokines (such as VEGF, IL-1, PDGF) in the management of corneal and ocular surface diseases in patients. These studies have been facilitated by 9 successful FDA Investigational New Drug (IND) submissions from my group since 2008.
New Areas of Investigation
While we have maintained our focus on immunology and immune regulation, our group has gradually broadened its focus to include novel animal models for high-risk corneal and stem cell transplantation, keratoprosthesis and biosynthetic corneal constructs. Our group was the first to develop a miniature keratoprosthesis for the mouse and stereotactic brain surgery models for corneal.
Executive Assistant
Linda Benson
Scientific Research Manager
Mojgan Pishyaren MT, MS
Laboratory manager
Qiang Zhang,MD
Postdoctoral Research Fellows
Hamid Alemi, MD, MPH
Tomas Blanco, PhD
Jimena Tatiana Carreno Galeano, MD
Francesca Kahale, MD
Seokjoo Lee, PhD
Catherine Liu, MD
Ayten Musayeva, MD
Gustavo Ortiz, PhD
Rohan Singh, MD
Shudan Wang, MD
Shuyan Zhu, MD
Pre-doctoral Research Fellows
Ann Yung, MA
Amirreza Naderi