Lacritin and the tear proteome as natural replacement therapy for dry eye

Experimental Eye Research

Volumn 117, Issue , 2013, Pages 39-52

  Karnati, Roy ^a   Laurie, Diane E ^b   Laurie, Gordon W ^c,d  

^a UNIVERSITY OF HYDERABAD   (India)

^b VIRGINIA MARYLAND REGIONAL COLLEGE OF VETERINARY MEDICINE   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

^d UNIVERSITY OF VIRGINIA   (United States)

Author keywords

Cornea; Dry eye; Lacrimal gland; Lacritin; Tear lipocalin; Tear proteome

Indexed keywords

LACRITIN; LIPOCALIN 1; MESSENGER RNA; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE; TEAR PROTEIN; UNCLASSIFIED DRUG;

ANGIOGENESIS; BINDING AFFINITY; CELL PROTECTION; CELL SURFACE; CELL SURVIVAL; DRY EYE; EPITHELIUM CELL; EYE INFLAMMATION; GLYCOSYLATION; HUMAN; INNATE IMMUNITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; PROTEIN STRUCTURE; REVIEW; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; SUBSTITUTION THERAPY; TARGET CELL;

CORNEA; DRY EYE; LACRIMAL GLAND; LACRITIN; TEAR LIPOCALIN; TEAR PROTEOME;

DRY EYE SYNDROMES; EYE PROTEINS; GLYCOPROTEINS; HUMANS; LIPOCALIN 1; PROTEOME;

EID: 84888137227     PISSN: 00144835     EISSN: 10960007     Source Type: Journal    
DOI: 10.1016/j.exer.2013.05.020     Document Type: Review

References (108)

1. Abduragimov A.R., Gasymov O.K., Yusifov T.N., Glasgow B.J. Functional cavity dimensions of tear lipocalin. Curr. Eye Res. 2000, 21:824-832.
2. Albig A.R., Neil J.R., Schiemann W.P. Fibulins 3 and 5 antagonize tumor angiogenesis invivo. Cancer Res. 2006, 66:2621-2629.
3. Ambati B.K., Nozaki M., Singh N., Takeda A., Jani P.D., Suthar T., Albuquerque R.J., Richter E., Sakurai E., Newcomb M.T., Kleinman M.E., Caldwell R.B., Lin Q., Ogura Y., Orecchia A., Samuelson D.A., Agnew D.W., St Leger J., Green W.R., Mahasreshti P.J., Curiel D.T., Kwan D., Marsh H., Ikeda S., Leiper L.J., Collinson J.M., Bogdanovich S., Khurana T.S., Shibuya M., Baldwin M.E., Ferrara N., Gerber H.P., De Falco S., Witta J., Baffi J.Z., Raisler B.J., Ambati J. Corneal avascularity is due to soluble VEGF receptor-1. Nature 2006, 443:993-997.
4. Ananthi S., Santhosh R.S., Nila M.V., Prajna N.V., Lalitha P., Dharmalingam K. Comparative proteomics of human male and female tears by two-dimensional electrophoresis. Exp. Eye Res. 2011, 92:454-463.
5. Ananthi S., Venkatesh Prajna N., Lalitha P., Valarnila M., Dharmalingam K. Pathogen induced changes in the protein profile of human tears from Fusarium keratitis patients. PLoS One 2013, 8:e53018.
6. Arber S., Krause K.H., Caroni P. s-cyclophilin is retained intracellularly via a unique COOH-terminal sequence and colocalizes with the calcium storage protein calreticulin. J.Cell Biol. 1992, 116:113-125.
7. Beckner M.E., Jagannathan S., Peterson V.A. Extracellular angio-associated migratory cell protein plays a positive role in angiogenesis and is regulated by astrocytes in coculture. Microvasc. Res. 2002, 63:259-269.
8. Boehm N., Funke S., Wiegand M., Wehrwein N., Pfeiffer N., Grus F.H. Alterations in the tear proteome of dry-eye patients - a matter of the clinical phenotype. Invest. Ophthalmol. Vis. Sci. 2013, 54:2385-2392.
9. Bonavida B., Sapse A.T., Sercarz E.E. Specific tear prealbumin: a unique lachrymal protein absent from serum and other secretions. Nature 1969, 221:375-376.
10. Breustedt D.A., Korndörfer I.P., Redl B., Skerra A. The 1.8-A crystal structure of human tear lipocalin reveals an extended branched cavity with capacity for multiple ligands. J.Biol. Chem. 2005, 280:484-493.
11. Chakravarti S., Magnuson T., Lass J.H., Jepsen K.J., LaMantia C., Carroll H. Lumican regulates collagen fibril assembly: skin fragility and corneal opacity in the absence of lumican. J.Cell Biol. 1998, 141:1277-1286.
12. Chen L., Glass J.D., Walton S.C., Laurie G.W. Role of laminin-1, collagen IV, and an autocrine factor(s) in regulated secretion by lacrimal acinar cells. Am. J. Physiol. 1998, 275:278-284.
13. Chen Z., Tong L., Li Z., Yoon K.C., Qi H., Farley W., Li D.Q., Pflugfelder S.C. Hyperosmolarity-induced cornification of human corneal epithelial cells is regulated by JNK MAPK. Invest. Ophthalmol. Vis. Sci. 2008, 49:539-549.
14. Dartt D.A. Neural regulation of lacrimal gland secretory processes: relevance in dry eye diseases. Prog. Retin. Eye Res. 2009, 28:155-177.
15. Dartt D.A. Tear lipocalin: structure and function. Ocul. Surf. 2011, 9:126-138.
16. de Souza G.A., Godoy L.M., Mann M. Identification of 491 proteins in the tear fluid proteome reveals a large number of proteases and protease inhibitors. Genome Biol. 2006, 7:R72.
17. Erickson O.F., Feeney L., McEwen W.K. Filter-paper electrophoresis of tears. II. Animal tears and the presence of a slow-moving lysozyme. AMA Arch. Ophthalmol. 1956, 55:800-806.
18. Eylan E., Ronen D., Romano A., Smetana O. Lysozyme tear level in patients with herpes simplex virus eye infection. Invest. Ophthalmol. Vis. Sci. 1977, 16:850-853.
19. Fleming A., Allison V.D. On specificity of the protein of human tears. Brit. J. Exp. Path. 1925, 6:87-90.
20. Fluckinger M., Haas H., Merschak P., Glasgow B.J., Redl B. Human tear lipocalin exhibits antimicrobial activity by scavenging microbial siderophores. Antimicrob. Agents Chemother. 2004, 48:3367-3372.
21. Fluckinger M., Merschak P., Hermann M., Haertlé T., Redl B. Lipocalin-interacting-membrane-receptor (LIMR) mediates cellular internalization of beta-lactoglobulin. Biochim. Biophys. Acta 2008, 1778:342-347.
22. Fujii A., Morimoto-Tochigi A., Walkup R.D., Shearer T.R., Azuma M. Lacritin-induced secretion of tear proteins from cultured monkey lacrimal acinar cells. Invest. Ophthalmol. Vis. Sci. 2013, 54:2533-2540.
23. Fullard R.J., Kissner D.M. Purification of the isoforms of tear specific prealbumin. Curr. Eye Res. 1991, 10:613-628.
24. Gasymov O.K., Abduragimov A.R., Yusifov T.N., Glasgow B.J. Interaction of tear lipocalin with lysozyme and lactoferrin. Biochem. Biophys. Res. Commun. 1999, 265:322-325.
25. Gasymov O.K., Abduragimov A.R., Yusifov T.N., Glasgow B.J. Binding studies of tear lipocalin: the role of the conserved tryptophan in maintaining structure, stability and ligand affinity. Biochim. Biophys. Acta 1999, 1433:307-320.
26. Gasymov O.K., Abduragimov A.R., Yusifov T.N., Glasgow B.J. Site-directed tryptophan fluorescence reveals the solution structure of tear lipocalin: evidence for features that confer promiscuity in ligand binding. Biochemistry 2001, 40:14754-14762.
27. Gasymov O.K., Abduragimov A.R., Yusifov T.N., Glasgow B.J. Relaxation of beta-structure in tear lipocalin and enhancement of retinoid binding. Invest. Ophthalmol. Vis. Sci. 2002, 43:3165-3173.
28. Glasgow B.J., Gasymov O.K. Focus on molecules: tear lipocalin. Exp. Eye Res. 2011, 92:242-243.
29. Glasgow B.J., Abduragimov A.R., Farahbakhsh Z.T., Faull K.F., Hubbell W.L. Tear lipocalins bind a broad array of lipid ligands. Curr. Eye Res. 1995, 14:363-372.
30. Green-Church K.B., Nichols J.J. Mass spectrometry-based proteomic analyses of contact lens deposition. Mol. Vis. 2008, 14:291-297.
31. Green-Church K.B., Nichols K.K., Kleinholz N.M., Zhang L., Nichols J.J. Investigation of the human tear film proteome using multiple proteomic approaches. Mol. Vis. 2008, 14:456-470.
32. Hall M.O., Prieto A.L., Obin M.S., Abrams T.A., Burgess B.L., Heeb M.J., Agnew B.J. Outer segment phagocytosis by cultured retinal pigment epithelial cells requires Gas6. Exp. Eye Res. 2001, 73:509-520.
33. Hassell J.R., Newsome D.A., Krachmer J.H., Rodrigues M.M. Macular corneal dystrophy: failure to synthesize a mature keratan sulfate proteoglycan. Proc. Natl. Acad. Sci. U. S. A. 1980, 77:3705-3709.
34. Heit J.J., Apelqvist A.A., Gu X., Winslow M.M., Neilson J.R., Crabtree G.R., Kim S.K. Calcineurin/NFAT signalling regulates pancreatic beta-cell growth and function. Nature 2006, 443:345-349.
35. Hollander A., D'Onofrio P.M., Magharious M.M., Lysko M.D., Koeberle P.D. Quantitative retinal protein analysis after optic nerve transection reveals a neuroprotective role for hepatoma-derived growth factor on injured retinal ganglion cells. Invest. Ophthalmol. Vis. Sci. 2012, 53:3973-3989.
36. Holzfeind P., Merschak P., Rogatsch H., Culig Z., Feichtinger H., Klocker H., Redl B. Expression of the gene for tear lipocalin/von Ebner's gland protein in human prostate. FEBS Lett. 1996, 395:95-98.
37. Husi H., Zurini M.G. Comparative binding studies of cyclophilins to cyclosporin A and derivatives by fluorescence measurements. Anal. Biochem. 1994, 222:251-255.
38. Josephson A.S., Lockwood D.W. Immunoelectrophoretic studies of the protein components of normal tears. J.Immunol. 1964, 93:532-539.
39. 2+-channel activation modulate phagocytosis by retinal pigment epithelium. Cell. Signal. 2008, 20:1159-1168.
40. Katz J.B., Muller A.J., Prendergast G.C. Indoleamine 2,3-dioxygenase in T-cell tolerance and tumoral immune escape. Immunol. Rev. 2008, 222:206-221.
41. Klenotic P.A., Munier F.L., Marmorstein L.Y., Anand-Apte B. Tissue inhibitor of metalloproteinases-3 (TIMP-3) is a binding partner of epithelial growth factor-containing fibulin-like extracellular matrix protein 1 (EFEMP1). Implications for macular degenerations. J.Biol. Chem. 2004, 279:30469-30473.
42. Kokenyesi R., Bernfield M. Core protein structure and sequence determine the site and presence of heparan sulfate and chondroitin sulfate on syndecan-1. J.Biol. Chem. 1994, 269:12304-12309.
43. Koo B.S., Lee D.Y., Ha H.S., Kim J.C., Kim C.W. Comparative analysis of the tear protein expression in blepharitis patients using two-dimensional electrophoresis. J.Proteome Res. 2005, 4:719-724.
44. Kumar R., Huebner A., Laurie G.W. Genetic separation of the human lacritin gene ("LACRT") and triple A (Allgrove) syndrome on 12q13. Adv. Exp. Med. Biol. 2002, 506:167-174.
45. Laurie G.W., Olsakovsky L.A., Conway B.P., McKown R.L., Kitagawa K., Nichols J.J. Dry eye and designer ophthalmics. Optom. Vis. Sci. 2008, 85:643-652.
46. Laurie D.E., Splan R.K., Green K., Still K.M., McKown R.L., Laurie G.W. Detection of prosecretory mitogen lacritin in nonprimate tears primarily as a C-terminal-like fragment. Invest. Ophthalmol. Vis. Sci. 2012, 53:6130-6136.
47. Lei H., Velez G., Hovland P., Hirose T., Kazlauskas A. Plasmin is the major protease responsible for processing PDGF-C in the vitreous of patients with proliferative vitreoretinopathy. Invest. Ophthalmol. Vis. Sci. 2008, 49:42-48.
48. Lei Z., Beuerman R.W., Chew A.P., Koh S.K., Cafaro T.A., Urrets-Zavalia E.A., Urrets-Zavalia J.A., Li S.F., Serra H.M. Quantitative analysis of N-linked glycoproteins in tear fluid of climatic droplet keratopathy by glycopeptide capture and iTRAQ. J.Proteome Res. 2009, 8:1992-2003.
49. Li X., Pontén A., Aase K., Karlsson L., Abramsson A., Uutela M., Bäckström G., Hellström M., Boström H., Li H., Soriano P., Betsholtz C., Heldin C.H., Alitalo K., Ostman A., Eriksson U. PDGF-C is a new protease-activated ligand for the PDGF alpha-receptor. Nat. Cell Biol. 2000, 2:302-309.
50. Lin P.Y., Cheng C.Y., Hsu W.M., Tsai S.Y., Lin M.W., Liu J.H., Chou P. Association between symptoms and signs of dry eye among an elderly Chinese population in Taiwan: the Shihpai eye study. Invest. Ophthalmol. Vis. Sci. 2005, 46:1593-1598.
51. Ma P., Beck S.L., Raab R.W., McKown R.L., Coffman G.L., Utani A., Chirico W.J., Rapraeger A.C., Laurie G.W. Heparanase deglycanation of syndecan-1 is required for binding of the epithelial-restricted prosecretory mitogen lacritin. J.Cell Biol. 2006, 174:1097-1106.
52. Massingale M.L., Li X., Vallabhajosyula M., Chen D., Wei Y., Asbell P.A. Analysis of inflammatory cytokines in the tears of dry eye patients. Cornea 2009, 28:1023-1027.
53. Mathers W.D. Ocular evaporation in meibomian gland dysfunction and dry eye. Ophthalmology 1993, 100:347-351.
54. McKown R.L., Wang N., Raab R.W., Karnati R., Zhang Y., Williams P.B., Laurie G.W. Lacritin and other new proteins of the lacrimal functional unit. Exp. Eye Res. 2009, 88:848-858.
55. McKown R.L., Raab R.W., Kachelries P., Caldwell S., Laurie G.W. Conserved regional 3' grouping of rare codons in the coding sequence of ocular prosecretory mitogen lacritin. Invest. Ophthalmol. Vis. Sci. 2013, 54:1979-1987.
56. Meier F.M., Frommer K.W., Peters M.A., Brentano F., Lefèvre S., Schröder D., Kyburz D., Steinmeyer J., Rehart S., Gay S., Müller-Ladner U., Neumann E. Visfatin/pre-B-cell colony-enhancing factor (PBEF), a proinflammatory and cell motility-changing factor in rheumatoid arthritis. J.Biol. Chem. 2012, 287:28378-28385.
57. Millar T.J., Mudgil P., Butovich I.A., Palaniappan C.K. Adsorption of human tear lipocalin to human meibomian lipid films. Invest. Ophthalmol. Vis. Sci. 2009, 50:140-151.
58. Montés-Micó R. Role of the tear film in the optical quality of the human eye. J.Cataract Refract. Surg. 2007, 33:1631-1635.
59. Morimoto-Tochigi A., Walkup R.D., Nakajima E., Shearer T.R., Azuma M. Mechanism for carbachol-induced secretion of lacritin in cultured monkey lacrimal acinar cells. Invest. Ophthalmol. Vis. Sci. 2010, 51:4395-4406.
60. Moschen A.R., Kaser A., Enrich B., Mosheimer B., Theurl M., Niederegger H., Tilg H. Visfatin, an adipocytokine with proinflammatory and immunomodulating properties. J.Immunol. 2007, 178:1748-1758.
61. Müller L.J., Pels L., Vrensen G.F. Ultrastructural organization of human corneal nerves. Invest. Ophthalmol. Vis. Sci. 1996, 37:476-488.
62. Na K.S., Mok J.W., Kim J.Y., Rho C.R., Joo C.K. Correlations between tear cytokines, chemokines, and soluble receptors and clinical severity of dry eye disease. Invest. Ophthalmol. Vis. Sci. 2012, 53:5443-5450.
63. Nakajima T., Walkup R.D., Tochigi A., Shearer T.R., Azuma M. Establishment of an appropriate animal model for lacritin studies: cloning and characterization of lacritin in monkey eyes. Exp. Eye Res. 2007, 85:651-658.
64. Nichols J.J., Green-Church K.B. Mass spectrometry-based proteomic analyses in contact lens-related dry eye. Cornea 2009, 28:1109-1117.
65. Ozyildirim A.M., Wistow G.J., Gao J., Wang J., Dickinson D.P., Frierson H.F., Laurie G.W. The lacrimal gland transcriptome is an unusually rich source of rare and poorly characterized gene transcripts. Invest. Ophthalmol. Vis. Sci. 2005, 46:1572-1580.
66. Paulsen F.P., Woon C.W., Varoga D., Jansen A., Garreis F., Jager K., Amm M., Podolsky D.K., Steven P., Barker N.P., Sel S. Intestinal trefoil factor/TFF3 promotes re-epithelialization of corneal wounds. J.Biol. Chem. 2008, 283:13418-13427.
67. Pertovaara M., Raitala A., Uusitalo H., Pukander J., Helin H., Oja S.S., Hurme M. Mechanisms dependent on tryptophan catabolism regulate immune responses in primary Sjogren's syndrome. Clin. Exp. Immunol. 2005, 142:155-161.
68. Pervaiz S., Brew K. Homology and structure-function correlations between alpha 1-acid glycoprotein and serum retinol-binding protein and its relatives. FASEB J. 1987, 1:209-214.
69. Pilch B., Mann M. Large-scale and high-confidence proteomic analysis of human seminal plasma. Genome Biol. 2006, 7:R40.
70. Plowman G.D., Green J.M., Neubauer M.G., Buckley S.D., McDonald V.L., Todaro G.J., Shoyab M. The epithelin precursor encodes two proteins with opposing activities on epithelial cell growth. J.Biol. Chem. 1992, 267:13073-13078.
71. Redl B., Holzfeind P., Lottspeich F. cDNA cloning and sequencing reveals human tear prealbumin to be a member of the lipophilic-ligand carrier protein superfamily. J.Biol. Chem. 1992, 267:20282-20287.
72. Redl B., Wojnar P., Ellemunter H., Feichtinger H. Identification of a lipocalin in mucosal glands of the human tracheobronchial tree and its enhanced secretion in cystic fibrosis. Lab. Invest. 1998, 78:1121-1129.
73. Sack R.A., Conradi L., Krumholz D., Beaton A., Sathe S., Morris C. Membrane array characterization of 80 chemokines, cytokines, and growth factors in open- and closed-eye tears: angiogenin and other defense system constituents. Invest. Ophthalmol. Vis. Sci. 2005, 46:1228-1238.
74. Sack R., Conradi L., Beaton A., Sathe S., McNamara N., Leonardi A. Antibody array characterization of inflammatory mediators in allergic and normal tears in the open and closed eye environments. Exp. Eye Res. 2007, 85:528-538.
75. Samudre S., Lattanzio F.A., Lossen V., Hosseini A., Sheppard J.D., McKown R.L., Laurie G.W., Williams P.B. Lacritin, a novel human tear glycoprotein, promotes sustained basal tearing and is well tolerated. Invest. Ophthalmol. Vis. Sci. 2011, 52:6265-6270.
76. Sanghi S., Kumar R., Lumsden A., Dickinson D., Klepeis V., Trinkaus-Randall V., Frierson H.F., Laurie G.W. cDNA and genomic cloning of lacritin, a novel secretion enhancing factor from the human lacrimal gland. J.Mol. Biol. 2001, 310:127-139.
77. Schaumberg D.A., Sullivan D.A., Buring J.E., Dana M.R. Prevalence of dry eye syndrome among US women. Am. J. Ophthalmol. 2003, 136:318-326.
78. Schenk S., Schoenhals G.J., de Souza G., Mann M. Ahigh confidence, manually validated human blood plasma protein reference set. BMC Med. Genomics 2008, 15:1-41.
79. Schoenwald R.D., Vidvauns S., Wurster D.E., Barfknecht C.F. The influence of tear proteins on the film stability of rabbit tear extracts. J.Ocul. Pharmacol. Ther. 1998, 14:15-29.
80. Seifert K., Gandia N.C., Wilburn J.K., Bower K.S., Sia R.K., Ryan D.S., Deaton M.L., Still K.M., Vassilev V.C., Laurie G.W., McKown R.L. Tear lacritin levels by age, sex, and time of day in healthy adults. Invest. Ophthalmol. Vis. Sci. 2012, 53:6610-6616.
81. Sen D.K., Sarin G.S. Immunoassay of tear lysozyme in conjunctival diseases. Br. J. Ophthalmol. 1982, 66:732-735.
82. Shao H., Scott S.G., Nakata C., Hamad A.R., Chakravarti S. Extracellular matrix protein lumican promotes clearance and resolution of Pseudomonas aeruginosa keratitis in a mouse model. PLoS One 2013, 8:e54765.
83. Sitaramamma T., Shivaji S., Rao G.N. Effect of storage on protein concentration of tear samples. Curr. Eye Res. 1998, 17:1027-1035.
84. Sonawane S., Khanolkar V., Namavari A., Chaudhary S., Gandhi S., Tibrewal S., Jassim S.H., Shaheen B., Hallak J., Horner J.H., Newcomb M., Sarkar J., Jain S. Ocular surface extracellular DNA and nuclease activity imbalance: a new paradigm for inflammation in dry eye disease. Invest. Ophthalmol. Vis. Sci. 2012, 53:8253-8263.
85. Soria J., Durán J.A., Etxebarria J., Merayo J., González N., Reigada R., García I., Acera A., Suárez T. Tear proteome and protein network analyses reveal a novel pentamarker panel for tear film characterization in dry eye and meibomian gland dysfunction. J.Proteomics 2013, 78:94-112.
86. Srinivasan S., Thangavelu M., Zhang L., Green K.B., Nichols K.K. iTRAQ quantitative proteomics in the analysis of tears in dry eye patients. Invest. Ophthalmol. Vis. Sci. 2012, 53:5052-5059.
87. Tsai P.S., Evans J.E., Green K.M., Sullivan R.M., Schaumberg D.A., Richards S.M., Dana M.R., Sullivan D.A. Proteomic analysis of human meibomian gland secretions. Br. J. Ophthalmol. 2006, 90:372-377.
88. Tsukamoto S., Fujiwara K., Ikeguchi M. Fatty acids bound to recombinant tear lipocalin and their role in structural stabilization. J.Biochem. 2009, 146:343-350.
89. Ubels J.L., Gipson I.K., Spurr-Michaud S.J., Tisdale A.S., Van Dyken R.E., Hatton M.P. Gene expression in human accessory lacrimal glands of Wolfring. Invest. Ophthalmol. Vis. Sci. 2012, 53:6738-6747.
90. van't Hof W., Blankenvoorde M.F., Veerman E.C., Amerongen A.V. The salivary lipocalin von Ebner's gland protein is a cysteine proteinase inhibitor. J.Biol. Chem. 1997, 272:1837-1841.
91. Velez V.F., Romano J.A., McKown R.L., Green K., Zhang L., Raab R.W., Ryan D.S., Hutnik C.M., Frierson H.F., Laurie G.W. Tissue transglutaminase is a negative regulator of monomeric lacritin bioactivity. Invest. Ophthalmol. Vis. Sci. 2013, 54:2123-2132.
92. Velos P., Cherry P.M., Miller D. An improved method for measuring human tear lysozyme concentration. Arch. Ophthalmol. 1985, 103:31-33.
93. Wang J., Wang N., Xie J., Walton S.C., McKown R.L., Raab R.W., Ma P., Beck S.L., Coffman G.L., Hussaini I.M., Laurie G.W. Restricted epithelial proliferation by lacritin via PKCalpha-dependent NFAT and mTOR pathways. J.Cell Biol. 2006, 174:689-700.
94. Wang N., Zimmerman K., Raab R.W., McKown R.L., Hutnik C.M., Talla V., Tyler M.F., Lee J.K., Laurie G.W. Lacritin Rescues Stressed Epithelia via Rapid Forkhead Box O3 (FOXO3)-associated Autophagy That Restores Metabolism. J.Biol. Chem. 2013, 288(25):18146-18161.
95. Weigelt B., Bosma A.J., van 't Veer L.J. Expression of a novel lacrimal gland gene lacritin in human breast tissues. J.Cancer Res. Clin. Onco. 2003, 129:735-736.
96. Wojnar P., Lechner M., Merschak P., Redl B. Molecular cloning of a novel lipocalin-1 interacting human cell membrane receptor using phage display. J.Biol. Chem. 2001, 276:20206-20212.
97. Wojnar P., Dirnhofer S., Ladurner P., Berger P., Redl B. Human lipocalin-1, a physiological scavenger of lipophilic compounds, is produced by corticotrophs of the pituitary gland. J.Histochem. Cytochem. 2002, 50:433-435.
98. Wojnar P., Lechner M., Redl B. Antisense down-regulation of lipocalin-interacting membrane receptor expression inhibits cellular internalization of lipocalin-1 in human NT2 cells. J.Biol. Chem. 2003, 278:16209-16215.
99. Yusifov T.N., Abduragimov A.R., Gasymov O.K., Glasgow B.J. Endonuclease activity in lipocalins. Biochem. J. 2000, 347:815-819.
100. Yusifov T.N., Abduragimov A.R., Narsinh K., Gasymov O.K., Glasgow B.J. Tear lipocalin is the major endonuclease in tears. Mol. Vis. 2008, 14:180-188.
101. Zeeuwen P.L., van Vlijmen-Willems I.M., Cheng T., Rodijk-Olthuis D., Hitomi K., Hara-Nishimura I., John S., Smyth N., Reinheckel T., Hendriks W.J., Schalkwijk J. The cystatin M/E-cathepsin L balance is essential for tissue homeostasis in epidermis, hair follicles, and cornea. FASEB J. 2010, 24:3744-3755.
102. Zhang W., Baban B., Rojas M., Tofigh S., Virmani S.K., Patel C., Behzadian M.A., Romero M.J., Caldwell R.W., Caldwell R.B. Arginase activity mediates retinal inflammation in endotoxin-induced uveitis. Am. J. Pathol. 2009, 175:891-902.
103. Zhang Y., Wang N., Raab R.W., McKown R.L., Irwin J.A., Kwon I., van Kuppevelt T.H., Laurie G.W. Targeting of heparanase-modified syndecan-1 by prosecretory mitogen lacritin requires conserved core GAGAL plus heparan and chondroitin sulfate as a novel hybrid binding site that enhances selectivity. J.Biol. Chem. 2013, 288:12090-12101.
104. Zhao Y., Yang J., Liao W., Liu X., Zhang H., Wang S., Wang D., Feng J., Yu L., Zhu W.G. Cytosolic FOXO1 is essential for the induction of autophagy and tumour suppressor activity. Nat. Cell Biol. 2010, 12:665-675.
105. Zhou L., Huang L.Q., Beuerman R.W., Grigg M.E., Li S.F., Chew F.T., Ang L., Stern M.E., Tan D. Proteomic analysis of human tears: defensin expression after ocular surface surgery. J.Proteome Res. 2004, 3:410-416.
106. Zhou L., Beuerman R.W., Chan C.M., Zhao S.Z., Li X.R., Yang H., Tong L., Liu S., Stern M.E., Tan D. Identification of tear fluid biomarkers in dry eye syndrome using iTRAQ quantitative proteomics. J.Proteome Res. 2009, 8:4889-4905.
107. Zhou L., Zhao S.Z., Koh S.K., Chen L., Vaz C., Tanavde V., Li X.R., Beuerman R.W. In-depth analysis of the human tear proteome. J.Proteomics 2012, 75:3877-3885.
108. Zhu C., Anderson A.C., Schubart A., Xiong H., Imitola J., Khoury S.J., Zheng X.X., Strom T.B., Kuchroo V.K. The Tim-3 ligand galectin-9 negatively regulates T helper type 1 immunity. Nat. Immunol. 2005, 6:1245-1252.