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    Hemant Khanna PhD

    TitleAssistant Professor
    InstitutionUniversity of Massachusetts Medical School
    DepartmentOphthalmology
    AddressUniversity of Massachusetts Medical School
    368 Plantation Street, AS6-2043
    Worcester MA 01605
      Other Positions
      InstitutionUMMS - School of Medicine
      DepartmentGene Therapy Center

      InstitutionUMMS - Graduate School of Biomedical Sciences
      DepartmentCell Biology

      InstitutionUMMS - Graduate School of Biomedical Sciences
      DepartmentInterdisciplinary Graduate Program

      InstitutionUMMS - Graduate School of Biomedical Sciences
      DepartmentNeuroscience

      InstitutionUMMS - Graduate School of Biomedical Sciences
      DepartmentTranslational Science

        Overview 
        Narrative

        Lab Website

        Additional Affiliations

        Program in Cell Dynamics

        Neurotherapeutics Institute

        Research

        Dr. Hemant KhannaCILIA are unique cellular organelles that extend from the surface of the cell in the form of an antenna. They are generated and maintained by an elaborate process of vesicular protein trafficking, microtubule extension and resorption and stringently regulated activity of microtubule motor proteins. This process is called Intraflagellar Transport (IFT). Cilia are involved in regulating diverse developmental and adulthood signaling cascades, including sonic hedgehog signaling and Wnt signaling. Being nearly ubiquitous, dysfunction of cilia results in severe developmental disorders, including neurodegenerative diseases of the eye and brain.

        Photoreceptors (rods and cones) are highly polarized neurons with a distinct inner segment and a photosensitive outer segment. To carry out visual signaling cascades, photoreceptors undergo immense but stringently regulated trafficking of proteins from the site of synthesis in the inner segment to the outer segment. The outer segments are considered an extension of primary or sensory cilia, which are near ubiquitous organelles formed by the extension of the plasma membrane in a post-mitotic cell. Slight perturbations in the cilia-dependent protein trafficking machinery result in severe photoreceptor degenerative disorders, such as Retinitis Pigmentosa and Leber congenital amaurosis.

         

        Schematic of a rod photoreceptor cell.

        This electron microscopy image of a zebrafish photoreceptor depicts the remarkable development of sensory cilium with outer segment discs. The cilium extends from the basal body, continues into a transition zone followed by axoneme extension into the outer segment. All outer segment components are synthesized in the inner segment and transported directionally to the outer segment via the cilium.

        Our lab investigates the Molecular and Cell Biological basis of Neurodegenerative Diseases of the Eye, with special focus on those caused due to defects of ciliary function in the photoreceptors, the light-sensing neurons of the Retina. These diseases include Retinitis Pigmentosa (RP) and Leber congenital amaurosis (LCA) and are characterized by progressive loss of night and day vision in patients. Photoreceptors are polarized sensory neurons with a distinct inner segment (IS) and the photosensory outer segment (OS). The OS is a sensory (or primary) cilium, which contains membranous discs arranged in a coin-stack like fashion. These discs are periodically shed at the tip and are renewed at the base. Such phenomena require a high level of stringently regulated trafficking of membrane and protein components from IS to OS via a narrow bridge-like structure, called the transition zone (TZ). The unique and distinct protein composition of the ciliary OS membrane of photoreceptors is essential to maintain the polar nature of the photoreceptors. Consistently, any defects in the trafficking machinery of photoreceptors due to dysfunction of the cilia results in degeneration and blindness.

        The TZ of photoreceptor cilium is implicated in regulating the sorting and trafficking of specific protein and other cargo components to the OS. We are interested in understanding the development, composition and function of the photoreceptor ciliary TZ in order to obtain mechanistic insights into the mode of regulated protein trafficking and maintenance of photoreceptor polarity. Our studies have identified three key ciliary proteins that are involved in photoreceptor ciliary protein: RPGR (retinitis pigmentosa GTPase regulator), RP2 (retinitis pigmentosa 2), and CEP290 (centrosomal protein of 290 kDa). These proteins not only modulate ciliary transport but are also mutated in various forms of human retinal degenerative diseases. Following three major projects are currently being carried out in our laboratory:

        PROJECT I: Functional Analysis of RPGR: RPGR is a ciliary protein mutated in a majority of X-linked RP cases (>75%) and is one of the most common cause of RP in humans. This project focuses on investigating the role of the TZ-associated protein RPGR in photoreceptor cilia. Our recent studies have revealed that RPGR exists in multiple protein complexes in mammalian retina, such as with Nephronophthisis (NPHP)-associated proteins and IFT proteins. Moreover, RPGR acts as a guanine exchange factor (GEF) for the small GTPase RAB8A, which is involved in cilia formation and photoreceptor protein trafficking. Our studies are specifically aimed at (i) delineating the role of RPGR as a GEF in photoreceptors, (ii) the cargo that is specifically delivered by RPGR to the outer segment, and (iii) the effect of human disease mutations on the function of RPGR. We have developed zebrafish and mouse models of RPGR dysfunction, which represent the human disease condition. Our investigations have also led to a successful gene therapy study to ameliorate RPGR-associated disease in two canine models.

        PROJECT II: RP2 in X-linked RP: The RP2 gene is mutated in 10-15% of X-linked RP cases. Previous studies indicate a role of RPGR in ciliary trafficking and maintenance. However, its precise role in photoreceptors is still unclear. Our lab utilizes cell culture and animal models to investigate the function of RP2 and pathology of associated disease.

        PROJECT III: LCA due to CEP290 mutations: CEP290 is another ciliary protein involved in regulating cilia formation. Mutations in CEP290 are a frequent cause of LCA, a childhood blindness disorder. Our lab has identified a naturally occurring mouse mutant of Cep290. Additionally, we have shown that CEP290 interacts with several distinct ciliary proteins in the retina and is involved in regulating protein trafficking as well as protein degradation. This project focuses on delineating the role of CEP290 in regulating photoreceptor cilia formation and maintenance and understanding the pathogenesis of CEP290-associated retinal degenerative diseases.

        Our approach includes:

        Proteomics: We utilize yeast two-hybrid, co-immunoprecipitation & Mass Spectrometry analyses to identify components of macromolecular complexes of photoreceptor cilia. Our previous studies have successfully identified a number of potential RPGR- and CEP290 -interacting proteins, which are involved in photoreceptor development and function.

        Animal and in vitro models: To study disease progression and pathogenesis, we are generating knock out and transgenic mouse lines representing the human disease phenotype. Our analysis includes assessment of age-dependent photoreceptor degeneration and examination of defects in protein trafficking in photoreceptors. We are also generating in vivo gene knockdown mouse models using Cre/loxp system or by subretinal injection of shRNA -encoding viral vectors. A major focus of the lab is also on utilizing zebrafish as a model to delineate the function of ciliary disease proteins and the effect of mutations on photoreceptor development and maintenance. We are also generating in vitro cell line models of knockdown by using shRNA technology in neuronal as well as non-neuronal cell lines.

         

        Injection of anti-sense morpholino (rpgr-MO) into zebrafish embryos

        Injection of anti-sense morpholino (rpgr-MO) into aebrafish embryos result in developmental disorder, including shortened body axis and edema at 4 dpf.  Uninjected wild-type (WT) and embryo injected with the 5 base mismatch (Mm) control (rpgr-Mm)are also shown.  Arrows in the rpgr-MO panel depict the different morphological phenotypes observed in the defective embryos (left_) panels; hydrocephaly and kinked tail; right panel; edma).  Source:  Ghosh et al., Hum Mol Genet, 2010.

        NEWS

        Lab Personnel

        Linjing Li, PhD-Postdoctoral Fellow

        K Nageswara Rao, PhD-Postdoctoral Fellow

        Balaji Subramanian, PhD-Postdoctoral Fellow

        Wei Zhang, PhD-Postdoctoral Fellow

        Manisha Anand, Research Associate I



        Rotation Projects
        Different rotation projects are available for interested students. These projects will involve examination of animal and cell culture models to study protein-protein interactions and polarized trafficking of proteins. The students will have the opportunity to learn basic molecular biology and cell biological techniques including use of siRNA technology to knockdown gene expression in animal models. Specific research topics can be decided based on the interest of the student.

        Post Docs

        This position involves research projects, which focus on understanding the development and function of neuronal cilia, specifically photoreceptor cilia and development of therapeutic strategies for associated disorders. The work entails the use of bacterial, cell culture and animal models (mice and zebrafish). Experience in molecular biology and protein biochemistry are a requirement for this position. Prior experience of in vivo injections in mice and zebrafish is desirable.  Interested candidates should send their resume and a short statement of interest to: Manisha Anand (manisha.anand@umassmed.edu).

        Bibliographic 
        selected publications
        List All   |   Timeline
        1. Li L, Khan N, Hurd T, Ghosh AK, Cheng C, Molday R, Heckenlively JR, Swaroop A, Khanna H. Ablation of the X-linked retinitis pigmentosa 2 (Rp2) gene in mice results in opsin mislocalization and photoreceptor degeneration. Invest Ophthalmol Vis Sci. 2013 Jul; 54(7):4503-11.
          View in: PubMed
        2. Khanna H, Baehr W. Retina ciliopathies: from genes to mechanisms and treatment. Vision Res. 2012 Dec 15; 75:1.
          View in: PubMed
        3. Yildiz O, Khanna H. Ciliary signaling cascades in photoreceptors. Vision Res. 2012 Dec 15; 75:112-6.
          View in: PubMed
        4. Anand M, Khanna H. Ciliary transition zone (TZ) proteins RPGR and CEP290: role in photoreceptor cilia and degenerative diseases. Expert Opin Ther Targets. 2012 Jun; 16(6):541-51.
          View in: PubMed
        5. Thompson DA, Khan NW, Othman MI, Chang B, Jia L, Grahek G, Wu Z, Hiriyanna S, Nellissery J, Li T, Khanna H, Colosi P, Swaroop A, Heckenlively JR. Rd9 is a naturally occurring mouse model of a common form of retinitis pigmentosa caused by mutations in RPGR-ORF15. PLoS One. 2012; 7(5):e35865.
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        6. Luo N, West CC, Murga-Zamalloa CA, Sun L, Anderson RM, Wells CD, Weinreb RN, Travers JB, Khanna H, Sun Y. OCRL localizes to the primary cilium: a new role for cilia in Lowe syndrome. Hum Mol Genet. 2012 Aug 1; 21(15):3333-44.
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        7. Rachel RA, May-Simera HL, Veleri S, Gotoh N, Choi BY, Murga-Zamalloa C, McIntyre JC, Marek J, Lopez I, Hackett AN, Zhang J, Brooks M, den Hollander AI, Beales PL, Li T, Jacobson SG, Sood R, Martens JR, Liu P, Friedman TB, Khanna H, Koenekoop RK, Kelley MW, Swaroop A. Combining Cep290 and Mkks ciliopathy alleles in mice rescues sensory defects and restores ciliogenesis. J Clin Invest. 2012 Apr 2; 122(4):1233-45.
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        8. Beltran WA, Cideciyan AV, Lewin AS, Iwabe S, Khanna H, Sumaroka A, Chiodo VA, Fajardo DS, Román AJ, Deng WT, Swider M, Alemán TS, Boye SL, Genini S, Swaroop A, Hauswirth WW, Jacobson SG, Aguirre GD. Gene therapy rescues photoreceptor blindness in dogs and paves the way for treating human X-linked retinitis pigmentosa. Proc Natl Acad Sci U S A. 2012 Feb 7; 109(6):2132-7.
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        9. Hemant Khanna, Wolfgang Baehr. Retina Ciliopathies: From genes to mechanisms and treatment. Vision Research. 2012; 1.
        10. Bian ZM, Elner SG, Khanna H, Murga-Zamalloa CA, Patil S, Elner VM. Expression and functional roles of caspase-5 in inflammatory responses of human retinal pigment epithelial cells. Invest Ophthalmol Vis Sci. 2011 Nov; 52(12):8646-56.
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        11. Patil SB, Hurd TW, Ghosh AK, Murga-Zamalloa CA, Khanna H. Functional analysis of retinitis pigmentosa 2 (RP2) protein reveals variable pathogenic potential of disease-associated missense variants. PLoS One. 2011; 6(6):e21379.
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        12. Murga-Zamalloa CA, Ghosh AK, Patil SB, Reed NA, Chan LS, Davuluri S, Peränen J, Hurd TW, Rachel RA, Khanna H. Accumulation of the Raf-1 kinase inhibitory protein (Rkip) is associated with Cep290-mediated photoreceptor degeneration in ciliopathies. J Biol Chem. 2011 Aug 12; 286(32):28276-86.
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        13. Yao J, Feathers KL, Khanna H, Thompson D, Tsilfidis C, Hauswirth WW, Heckenlively JR, Swaroop A, Zacks DN. XIAP therapy increases survival of transplanted rod precursors in a degenerating host retina. Invest Ophthalmol Vis Sci. 2011 Mar; 52(3):1567-72.
          View in: PubMed
        14. Chakarova CF, Khanna H, Shah AZ, Patil SB, Sedmak T, Murga-Zamalloa CA, Papaioannou MG, Nagel-Wolfrum K, Lopez I, Munro P, Cheetham M, Koenekoop RK, Rios RM, Matter K, Wolfrum U, Swaroop A, Bhattacharya SS. TOPORS, implicated in retinal degeneration, is a cilia-centrosomal protein. Hum Mol Genet. 2011 Mar 1; 20(5):975-87.
          View in: PubMed
        15. Otto EA, Hurd TW, Airik R, Chaki M, Zhou W, Stoetzel C, Patil SB, Levy S, Ghosh AK, Murga-Zamalloa CA, van Reeuwijk J, Letteboer SJ, Sang L, Giles RH, Liu Q, Coene KL, Estrada-Cuzcano A, Collin RW, McLaughlin HM, Held S, Kasanuki JM, Ramaswami G, Conte J, Lopez I, Washburn J, Macdonald J, Hu J, Yamashita Y, Maher ER, Guay-Woodford LM, Neumann HP, Obermüller N, Koenekoop RK, Bergmann C, Bei X, Lewis RA, Katsanis N, Lopes V, Williams DS, Lyons RH, Dang CV, Brito DA, Dias MB, Zhang X, Cavalcoli JD, Nürnberg G, Nürnberg P, Pierce EA, Jackson PK, Antignac C, Saunier S, Roepman R, Dollfus H, Khanna H, Hildebrandt F. Candidate exome capture identifies mutation of SDCCAG8 as the cause of a retinal-renal ciliopathy. Nat Genet. 2010 Oct; 42(10):840-50.
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        16. Patil SB, Verma R, Venkatareddy M, Khanna H. Expression and localization of the ciliary disease protein retinitis pigmentosa GTPase regulator in mammalian kidney. Kidney Int. 2010 Sep; 78(6):622-3.
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        17. Hurd T, Zhou W, Jenkins P, Liu CJ, Swaroop A, Khanna H, Martens J, Hildebrandt F, Margolis B. The retinitis pigmentosa protein RP2 interacts with polycystin 2 and regulates cilia-mediated vertebrate development. Hum Mol Genet. 2010 Nov 15; 19(22):4330-44.
          View in: PubMed
        18. Murga-Zamalloa CA, Desai NJ, Hildebrandt F, Khanna H. Interaction of ciliary disease protein retinitis pigmentosa GTPase regulator with nephronophthisis-associated proteins in mammalian retinas. Mol Vis. 2010; 16:1373-81.
          View in: PubMed
        19. Murga-Zamalloa CA, Atkins SJ, Peranen J, Swaroop A, Khanna H. Interaction of retinitis pigmentosa GTPase regulator (RPGR) with RAB8A GTPase: implications for cilia dysfunction and photoreceptor degeneration. Hum Mol Genet. 2010 Sep 15; 19(18):3591-8.
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        20. Jayasundera T, Branham KE, Othman M, Rhoades WR, Karoukis AJ, Khanna H, Swaroop A, Heckenlively JR. RP2 phenotype and pathogenetic correlations in X-linked retinitis pigmentosa. Arch Ophthalmol. 2010 Jul; 128(7):915-23.
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        21. Patzke S, Redick S, Warsame A, Murga-Zamalloa CA, Khanna H, Doxsey S, Stokke T. CSPP is a ciliary protein interacting with Nephrocystin 8 and required for cilia formation. Mol Biol Cell. 2010 Aug 1; 21(15):2555-67.
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        22. O'Toole JF, Liu Y, Davis EE, Westlake CJ, Attanasio M, Otto EA, Seelow D, Nurnberg G, Becker C, Nuutinen M, Kärppä M, Ignatius J, Uusimaa J, Pakanen S, Jaakkola E, van den Heuvel LP, Fehrenbach H, Wiggins R, Goyal M, Zhou W, Wolf MT, Wise E, Helou J, Allen SJ, Murga-Zamalloa CA, Ashraf S, Chaki M, Heeringa S, Chernin G, Hoskins BE, Chaib H, Gleeson J, Kusakabe T, Suzuki T, Isaac RE, Quarmby LM, Tennant B, Fujioka H, Tuominen H, Hassinen I, Lohi H, van Houten JL, Rotig A, Sayer JA, Rolinski B, Freisinger P, Madhavan SM, Herzer M, Madignier F, Prokisch H, Nurnberg P, Jackson PK, Jackson P, Khanna H, Katsanis N, Hildebrandt F. Individuals with mutations in XPNPEP3, which encodes a mitochondrial protein, develop a nephronophthisis-like nephropathy. J Clin Invest. 2010 Mar; 120(3):791-802.
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        23. Murga-Zamalloa C, Swaroop A, Khanna H. Multiprotein complexes of Retinitis Pigmentosa GTPase regulator (RPGR), a ciliary protein mutated in X-linked Retinitis Pigmentosa (XLRP). Adv Exp Med Biol. 2010; 664:105-14.
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        24. Ghosh AK, Murga-Zamalloa CA, Chan L, Hitchcock PF, Swaroop A, Khanna H. Human retinopathy-associated ciliary protein retinitis pigmentosa GTPase regulator mediates cilia-dependent vertebrate development. Hum Mol Genet. 2010 Jan 1; 19(1):90-8.
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        25. Murga-Zamalloa CA, Swaroop A, Khanna H. RPGR-containing protein complexes in syndromic and non-syndromic retinal degeneration due to ciliary dysfunction. J Genet. 2009 Dec; 88(4):399-407.
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        26. Paul E, Kielbasinski M, Sedivy JM, Murga-Zamalloa C, Khanna H, Klysik JE. Widespread expression of the Supv3L1 mitochondrial RNA helicase in the mouse. Transgenic Res. 2010 Aug; 19(4):691-701.
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        27. Wu DM, Khanna H, Atmaca-Sonmez P, Sieving PA, Branham K, Othman M, Swaroop A, Daiger SP, Heckenlively JR. Long-term follow-up of a family with dominant X-linked retinitis pigmentosa. Eye (Lond). 2010 May; 24(5):764-74.
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        28. Khanna H, Davis EE, Murga-Zamalloa CA, Estrada-Cuzcano A, Lopez I, den Hollander AI, Zonneveld MN, Othman MI, Waseem N, Chakarova CF, Maubaret C, Diaz-Font A, MacDonald I, Muzny DM, Wheeler DA, Morgan M, Lewis LR, Logan CV, Tan PL, Beer MA, Inglehearn CF, Lewis RA, Jacobson SG, Bergmann C, Beales PL, Attié-Bitach T, Johnson CA, Otto EA, Bhattacharya SS, Hildebrandt F, Gibbs RA, Koenekoop RK, Swaroop A, Katsanis N. A common allele in RPGRIP1L is a modifier of retinal degeneration in ciliopathies. Nat Genet. 2009 Jun; 41(6):739-45.
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        29. Tsang WY, Bossard C, Khanna H, Peränen J, Swaroop A, Malhotra V, Dynlacht BD. CP110 suppresses primary cilia formation through its interaction with CEP290, a protein deficient in human ciliary disease. Dev Cell. 2008 Aug; 15(2):187-97.
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        30. Siffroi-Fernandez S, Felder-Schmittbuhl MP, Khanna H, Swaroop A, Hicks D. FGF19 exhibits neuroprotective effects on adult mammalian photoreceptors in vitro. Invest Ophthalmol Vis Sci. 2008 Apr; 49(4):1696-704.
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        31. Cideciyan AV, Aleman TS, Jacobson SG, Khanna H, Sumaroka A, Aguirre GK, Schwartz SB, Windsor EA, He S, Chang B, Stone EM, Swaroop A. Centrosomal-ciliary gene CEP290/NPHP6 mutations result in blindness with unexpected sparing of photoreceptors and visual brain: implications for therapy of Leber congenital amaurosis. Hum Mutat. 2007 Nov; 28(11):1074-83.
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        32. He S, Parapuram SK, Hurd TW, Behnam B, Margolis B, Swaroop A, Khanna H. Retinitis Pigmentosa GTPase Regulator (RPGR) protein isoforms in mammalian retina: insights into X-linked Retinitis Pigmentosa and associated ciliopathies. Vision Res. 2008 Feb; 48(3):366-76.
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        33. Chakarova CF, Papaioannou MG, Khanna H, Lopez I, Waseem N, Shah A, Theis T, Friedman J, Maubaret C, Bujakowska K, Veraitch B, Abd El-Aziz MM, Prescott de Q, Parapuram SK, Bickmore WA, Munro PM, Gal A, Hamel CP, Marigo V, Ponting CP, Wissinger B, Zrenner E, Matter K, Swaroop A, Koenekoop RK, Bhattacharya SS. Mutations in TOPORS cause autosomal dominant retinitis pigmentosa with perivascular retinal pigment epithelium atrophy. Am J Hum Genet. 2007 Nov; 81(5):1098-103.
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        34. McEwen DP, Koenekoop RK, Khanna H, Jenkins PM, Lopez I, Swaroop A, Martens JR. Hypomorphic CEP290/NPHP6 mutations result in anosmia caused by the selective loss of G proteins in cilia of olfactory sensory neurons. Proc Natl Acad Sci U S A. 2007 Oct 2; 104(40):15917-22.
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        35. Oh EC, Khan N, Novelli E, Khanna H, Strettoi E, Swaroop A. Transformation of cone precursors to functional rod photoreceptors by bZIP transcription factor NRL. Proc Natl Acad Sci U S A. 2007 Jan 30; 104(5):1679-84.
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        36. Khanna H, Akimoto M, Siffroi-Fernandez S, Friedman JS, Hicks D, Swaroop A. Retinoic acid regulates the expression of photoreceptor transcription factor NRL. J Biol Chem. 2006 Sep 15; 281(37):27327-34.
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        37. Sayer JA, Otto EA, O'Toole JF, Nurnberg G, Kennedy MA, Becker C, Hennies HC, Helou J, Attanasio M, Fausett BV, Utsch B, Khanna H, Liu Y, Drummond I, Kawakami I, Kusakabe T, Tsuda M, Ma L, Lee H, Larson RG, Allen SJ, Wilkinson CJ, Nigg EA, Shou C, Lillo C, Williams DS, Hoppe B, Kemper MJ, Neuhaus T, Parisi MA, Glass IA, Petry M, Kispert A, Gloy J, Ganner A, Walz G, Zhu X, Goldman D, Nurnberg P, Swaroop A, Leroux MR, Hildebrandt F. The centrosomal protein nephrocystin-6 is mutated in Joubert syndrome and activates transcription factor ATF4. Nat Genet. 2006 Jun; 38(6):674-81.
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        38. Chang B, Khanna H, Hawes N, Jimeno D, He S, Lillo C, Parapuram SK, Cheng H, Scott A, Hurd RE, Sayer JA, Otto EA, Attanasio M, O'Toole JF, Jin G, Shou C, Hildebrandt F, Williams DS, Heckenlively JR, Swaroop A. In-frame deletion in a novel centrosomal/ciliary protein CEP290/NPHP6 perturbs its interaction with RPGR and results in early-onset retinal degeneration in the rd16 mouse. Hum Mol Genet. 2006 Jun 1; 15(11):1847-57.
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        39. Khanna H, Hurd TW, Lillo C, Shu X, Parapuram SK, He S, Akimoto M, Wright AF, Margolis B, Williams DS, Swaroop A. RPGR-ORF15, which is mutated in retinitis pigmentosa, associates with SMC1, SMC3, and microtubule transport proteins. J Biol Chem. 2005 Sep 30; 280(39):33580-7.
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        40. Shu X, Fry AM, Tulloch B, Manson FD, Crabb JW, Khanna H, Faragher AJ, Lennon A, He S, Trojan P, Giessl A, Wolfrum U, Vervoort R, Swaroop A, Wright AF. RPGR ORF15 isoform co-localizes with RPGRIP1 at centrioles and basal bodies and interacts with nucleophosmin. Hum Mol Genet. 2005 May 1; 14(9):1183-97.
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        41. Otto EA, Loeys B, Khanna H, Hellemans J, Sudbrak R, Fan S, Muerb U, O'Toole JF, Helou J, Attanasio M, Utsch B, Sayer JA, Lillo C, Jimeno D, Coucke P, De Paepe A, Reinhardt R, Klages S, Tsuda M, Kawakami I, Kusakabe T, Omran H, Imm A, Tippens M, Raymond PA, Hill J, Beales P, He S, Kispert A, Margolis B, Williams DS, Swaroop A, Hildebrandt F. Nephrocystin-5, a ciliary IQ domain protein, is mutated in Senior-Loken syndrome and interacts with RPGR and calmodulin. Nat Genet. 2005 Mar; 37(3):282-8.
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        42. Friedman JS, Khanna H, Swain PK, Denicola R, Cheng H, Mitton KP, Weber CH, Hicks D, Swaroop A. The minimal transactivation domain of the basic motif-leucine zipper transcription factor NRL interacts with TATA-binding protein. J Biol Chem. 2004 Nov 5; 279(45):47233-41.
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        43. Cheng H, Khanna H, Oh EC, Hicks D, Mitton KP, Swaroop A. Photoreceptor-specific nuclear receptor NR2E3 functions as a transcriptional activator in rod photoreceptors. Hum Mol Genet. 2004 Aug 1; 13(15):1563-75.
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        44. Mitton KP, Swain PK, Khanna H, Dowd M, Apel IJ, Swaroop A. Interaction of retinal bZIP transcription factor NRL with Flt3-interacting zinc-finger protein Fiz1: possible role of Fiz1 as a transcriptional repressor. Hum Mol Genet. 2003 Feb 15; 12(4):365-73.
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