Betaine stabilizes cell volume and protects against apoptosis in human corneal epithelial cells under hyperosmotic stress

Experimental Eye Research

Volumn 108, Issue , 2013, Pages 33-41

  Garrett, Qian ^a,b   Khandekar, Neeta ^a   Shih, Sharon ^a   Flanagan, Judith L ^a   Simmons, Peter ^c   Vehige, Joseph ^c   Willcox, Mark D P ^a,b  

^a BRIEN HOLDEN VISION INSTITUTE   (Australia)

^b UNIVERSITY OF NEW SOUTH WALES   (Australia)

^c ALLERGAN INC   (United States)

Author keywords

Apoptosis; Betaine; Betaine transport; BGT 1; Cell shrinkage; Human corneal epithelial cells; Hyperosmolarity; Osmoprotection

Indexed keywords

4 AMINOBUTYRIC ACID CARRIER; BETAINE; BGT 1 PROTEIN; CASPASE 3; CASPASE 7; CASPASE 8; CASPASE 9; PROTECTIVE AGENT; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CELL VIABILITY; CELL VOLUME; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CORNEA CELL; EPITHELIUM CELL; FLOW CYTOMETRY; HUMAN; HUMAN CELL; HUMAN CORNEAL LIMBAL EPITHELIAL CELL; HYPEROSMOTIC STRESS; IN VITRO STUDY; PRIORITY JOURNAL;

ANTIBODIES; APOPTOSIS; BETAINE; CARRIER PROTEINS; CASPASES; CELL LINE; CELL SIZE; CELL SURVIVAL; CYTOPROTECTION; EPITHELIAL CELLS; EPITHELIUM, CORNEAL; FLOW CYTOMETRY; HUMANS; MICROSCOPY, CONFOCAL; MITOCHONDRIA; OSMOTIC PRESSURE; SALINE SOLUTION, HYPERTONIC; TIME FACTORS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84872421173     PISSN: 00144835     EISSN: 10960007     Source Type: Journal    
DOI: 10.1016/j.exer.2012.12.001     Document Type: Article

References (81)

1. Alfieri R.R., Cavazzoni A., Petronini P.G., Bonelli M.A., Caccamo A.E., Borghetti A.F., Wheeler K.P. Compatible osmolytes modulate the response of porcine endothelial cells to hypertonicity and protect them from apoptosis. J. Physiol. 2002, 540:499-508.
2. Beck F.X., Burger-Kentischer A., Muller E. Cellular response to osmotic stress in the renal medulla. Pflugers Arch. 1998, 436:814-827.
3. Bildin V.N., Yang H., Crook R.B., Fischbarg J., Reinach P.S. Adaptation by corneal epithelial cells to chronic hypertonic stress depends on upregulation of Na:K:2Cl cotransporter gene and protein expression and ion transport activity. J. Membr. Biol. 2000, 177:41-50.
4. Bron A.J., Tiffany J.M., Yokoi N., Gouveia S.M. Using osmolarity to diagnose dry eye: a compartmental hypothesis and review of our assumptions. Adv. Exp. Med. Biol. 2002, 506:1087-1095.
5. Burg M.B., Ferraris J.D., Dmitrieva N.I. Cellular response to hyperosmotic stresses. Physiol. Rev. 2007, 87:1441-1474.
6. Burg M.B., Kwon E.D., Kültz D. Osmotic regulation of gene expression. FASEB. J. 1996, 10:1598-1606.
7. Burg M.B., Kwon E.D., Kultz D. Regulation of gene expression by hypertonicity. Annu. Rev. Physiol. 1997, 59:437-455.
8. Capó-Aponte J.E., Wang Z., Bildin V.N., Pokorny K.S., Reinach P.S. Fate of hypertonicity-stressed corneal epithelial cells depends on differential MAPK activation and p38MAPK/Na-K-2Cl cotransporter1 interaction. Exp. Eye Res. 2007, 84:361-372.
9. Cayley S., Record M.T. Roles of cytoplasmic osmolytes, water, and crowding in the response of Escherichia coli to osmotic stress: biophysical basis of osmoprotection by glycine betaine. Biochemistry 2003, 42:12596-12609.
10. Chen G., Goeddel D.V. TNF-R1 signaling: a beautiful pathway. Science 2002, 296:1634-1635.
11. Chen W., Zhang X., Liu M., Zhang J., Ye Y., Lin Y., Luyckx J., Qu J. Trehalose protects against ocular surface disorders in experimental murine dry eye through suppression of apoptosis. Exp. Eye Res. 2009, 89:311-318.
12. Choe K.P., Strange K. Genome-wide RNAi screen and in vivo protein aggregation reporters identify degradation of damaged proteins as an essential hypertonic stress response. Am. J. Physiol. - Cell Physiol. 2008, 295:C1488-C1498.
13. Chuang S.M., Wang I.C., Yang J.L. Roles of JNK, p38 and ERK mitogen-activated protein kinases in the growth inhibition and apoptosis induced by cadmium. Carcinogenesis 2000, 21:1423-1432.
14. Clouzeau C., Godefroy D., Riancho L., Rostene W., Baudouin C., Brignole-Baudouin F. Hyperosmolarity potentiates toxic effects of benzalkonium chloride on conjunctival epithelial cells in vitro. Mol. Vis. 2012, 18:851-863.
15. Corrales R.M., Luo L., Chang E.Y., Pflugfelder S.C. Effects of osmoprotectants on hyperosmolar stress in cultured human corneal epithelial cells. Cornea 2008, 27:574-579.
16. Corrales R.M., Stern M.E., De Paiva C.S., Welch J., Li D.-Q., Pflugfelder S.C. Desiccating stress stimulates expression of matrix metalloproteinases by the corneal epithelium. Invest. Ophthalmol. Vis. Sci. 2006, 47:3293-3302.
17. Corrales R.M., Villarreal A., Farley W., Stern M.E., Li D.Q., Pflugfelder S.C. Strain-related cytokine profiles on the murine ocular surface in response to desiccating stress. Cornea 2007, 26:579-584.
18. Edwards B.S., Oprea T., Prossnitz E.R., Sklar L.A. Flow cytometry for high-throughput, high-content screening. Curr. Opin. Chem. Biol. 2004, 8:392-398.
19. Elmore S. Apoptosis: a review of programmed cell death. Toxicol. Pathol. 2007, 35:495-516.
20. Fan T.J., Han L.H., Cong R.S., Liang J. Caspase family proteases and apoptosis. Acta Biochim. Biophys. Sin. (Shanghai) 2005, 37:719-727.
21. Friis M.B., Friborg C.R., Schneider L., Nielsen M.-B., Lambert I.H., Christensen S.T., Hoffmann E.K. Cell shrinkage as a signal to apoptosis in NIH 3T3 fibroblasts. J. Physiol. 2005, 567:427-443.
22. Furuichi S., Hashimoto S., Gon Y., Matsumoto K., Horie T. p38 mitogen-activated protein kinase and c-Jun-NH2-terminal kinase regulate interleukin-8 and RANTES production in hyperosmolarity stimulated human bronchial epithelial cells. Respirology 2002, 7:193-200.
23. Gaffney E.A., Tiffany J.M., Yokoi N., Bron A.J. A mass and solute balance model for tear volume and osmolarity in the normal and the dry eye. Prog. Retin. Eye Res. 2010, 29:59-78.
24. Gao J., Schwalb T.A., Addeo J.V., Ghosn C.R., Stern M.E. The role of apoptosis in the pathogenesis of canine keratoconjunctivitis sicca: the effect of topical Cyclosporin A therapy. Cornea 1998, 17:654-663.
25. Garrett Q., Xu S., Simmons P.A., Vehige J., Flanagan J.L., Willcox M.D. Expression and localization of carnitine/organic cation transporter OCTN1 and OCTN2 in ocular epithelium. Invest. Ophthalmol. Vis. Sci. 2008, 49:4844-4849.
26. Gilbard J.P. Human tear film electrolyte concentrations in health and dry eye disease. Int. Ophthalmol. Clin. 1994, 34:27-36.
27. Gilbard J.P., Farris R.L. Tear osmolarity and ocular surface disease in keratoconjunctivitis sicca. Arch. Ophthalmol. 1979, 97:1642-1646.
28. Gilbard J.P., Farris R.L., Santamaria J. Osmolarity of tear microvolumes in keratoconjunctivitis sicca. Arch. Ophthalmol. 1978, 96:677-681.
29. Handler J.S., Kwon H.M. Transcriptional regulation by changes in tonicity. Kidney Int. 2001, 60:408-411.
30. Haussinger D. Neural control of hepatic osmolytes and parenchymal cell hydration. Anat. Rec. A Discov. Mol. Cell. Evol. Biol. 2004, 280:893-900.
31. Horio M., Ito A., Matsuoka Y., Moriyama T., Orita Y., Takenaka M., Imai E. Apoptosis induced by hypertonicity in Madin Darley canine kidney cells: protective effect of betaine. Nephrol. Dial. Transplant. 2001, 16:483-490.
32. Huang Z., Tunnacliffe A. Response of human cells to desiccation: comparison with hyperosmotic stress response. J. Physiol. 2004, 558:181-191.
33. Kempson S.A., Montrose M.H. Osmotic regulation of renal betaine transport: transcription and beyond. Pflügers Arch. Eur. J. Physiol. 2004, 449:227-234.
34. Lang F. Mechanisms and significance of cell volume regulation. J. Am. Coll. Nutr. 2007, 26:613S-623S.
35. Lang K.L., Fillon S.F., Schneider D.S., Rammensee H.G.R., Lang F.L. Stimulation of TNFa expression by hyperosmotic stress. Pflügers Arch. Eur. J. Physiol. 2002, 443:798-803.
36. Lee J.H., Kim M., Im Y.S., Choi W., Byeon S.H., Lee H.K. NFAT5 induction and its role in hyperosmolar stressed human limbal epithelial cells. Invest. Ophthalmol. Vis. Sci. 2008, 49:1827-1835.
37. Lemp M.A., Bron A.J., Baudouin C., Benítez del Castillo J.M., Geffen D., Tauber J., Foulks G.N., Pepose J.S., Sullivan B.D. Tear osmolarity in the diagnosis and management of dry eye disease. Am. J. Ophthalmol. 2011, 151:792-798.
38. Li D.-Q., Luo L., Chen Z., Kim H.-S., Song X.J., Pflugfelder S.C. JNK and ERK MAP kinases mediate induction of IL-1beta, TNF-alpha and IL-8 following hyperosmolar stress in human limbal epithelial cells. Exp. Eye Res. 2006, 82:588-596.
39. Li H., Lin X. Positive and negative signaling components involved in TNFα-induced NF-κB activation. Cytokine 2008, 41:1-8.
40. Lim C.H., Bot A.G.M., de Jonge H.R., Tilly B.C. Osmosignaling and volume regulation in intestinal epithelial cells. Methods in Enzymology 2007, 325-342. Academic Press. H. Dieter, S. Helmut (Eds.).
41. Liu H., Begley C., Chen M., Bradley A., Bonanno J., McNamara N.A., Nelson J.D., Simpson T. A link between tear instability and hyperosmolarity in dry eye. Invest. Ophthalmol. Vis. Sci. 2009, 50:3671-3679.
42. Lopez-Rodriguez C., Aramburu J., Jin L., Rakeman A.S., Michino M., Rao A. Bridging the NFAT and NF-kappaB families: NFAT5 dimerization regulates cytokine gene transcription in response to osmotic stress. Immunity 2001, 15:47-58.
43. Lowry O.H., Rosebrough N.J., Farr A.L., Randall R.J. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 1951, 193:265-275.
44. Luo L., Li D.-Q., Doshi A., Farley W., Corrales R.M., Pflugfelder S.C. Experimental dry eye stimulates production of inflammatory cytokines and MMP-9 and activates MAPK signaling pathways on the ocular surface. Invest. Ophthalmol. Vis. Sci. 2004, 45:4293-4301.
45. Luo L., Li D.Q., Corrales R.M., Pflugfelder S.C. Hyperosmolar saline is a proinflammatory stress on the mouse ocular surface. Eye Contact Lens 2005, 31:186-193.
46. Luo L., Li D.Q., Pflugfelder S.C. Hyperosmolarity-induced apoptosis in human corneal epithelial cells is mediated by cytochrome c and MAPK pathways. Cornea 2007, 26:452-460.
47. Luo X., Budihardjo I., Zou H., Slaughter C., Wang X. Bid, a Bcl2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors. Cell 1998, 94:481-490.
48. Maeno E., Ishizaki Y., Kanaseki T., Hazama A., Okada Y. Normotonic cell shrinkage because of disordered volume regulation is an early prerequisite to apoptosis. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:9487-9492.
49. McManus M.L., Churchwell K.B., Strange K. Regulation of cell volume in health and disease. N. Engl. J. Med. 1995, 333:1260-1267.
50. Miyakawa H., Woo S.K., Dahl S.C., Handler J.S., Kwon H.M. Tonicity-responsive enhancer binding protein, a rel-like protein that stimulates transcription in response to hypertonicity. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:2538-2542.
51. Neuhofer W., Beck F.X. Cell survival in the hostile environment of the renal medulla. Annu. Rev. Physiol. 2005, 67:531-555.
52. Olsen M., Sarup A., Larsson O.M., Schousboe A. Effect of hyperosmotic conditions on the expression of the betaine-GABA-transporter (BGT-1) in cultured mouse astrocytes. Neurochem. Res. 2005, 30:855-865.
53. Orlov S.N., Novikov K.N. The regulation of cell volume: the mechanisms, coupled cellular reactions and pathophysiological significance. Fiziol. Zh. Im. I. M. Sechenova 1996, 82:1-15.
54. Peluso G., Barbarisi A., Savica V., Reda E., Nicolai R., Benatti P., Calvani M. Carnitine: an osmolyte that plays a metabolic role. J. Cell. Biochem. 2000, 80:1-10.
55. Petronini P.G., Alfieri R.R., Losio M.N., Caccamo A.E., Cavazzoni A., Bonelli M.A., Borghetti A.F., Wheeler K.P. Induction of BGT-1 and amino acid system A transport activities in endothelial cells exposed to hyperosmolarity. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2000, 279:R1580-R1589.
56. Pflugfelder S.C., de Paiva C.S., Li D.-Q., Stern M.E. Epithelial-immune cell interaction in dry eye. Cornea 2008, 27:S9-S11. 10.1097.
57. Pflugfelder S.C., Jones D., Ji Z., Afonso A., Monroy D. Altered cytokine balance in the tear fluid and conjunctiva of patients with Sjogren's syndrome keratoconjunctivitis sicca. Curr. Eye Res. 1999, 19:201-211.
58. Png E., Samivelu G.K., Yeo S.H., Chew J., Chaurasia S.S., Tong L. Hyperosmolarity-mediated mitochondrial dysfunction requires transglutaminase-2 in human corneal epithelial cells. J. Cell. Physiol. 2011, 226:693-699.
59. Schliess F., Haussinger D. The cellular hydration state: a critical determinant for cell death and survival. Biol. Chem. 2002, 383:577-583.
60. Schneider-Brachert W., Tchikov V., Neumeyer J., Jakob M., Winoto-Morbach S., Held-Feindt J., Heinrich M., Merkel O., Ehrenschwender M., Adam D., Mentlein R., Kabelitz D., Schutze S. Compartmentalization of TNF receptor 1 signaling: internalized TNF receptosomes as death signaling vesicles. Immunity 2004, 21:415-428.
61. Smith J. The epidemiology of dry eye disease: report of the epidemiology subcommittee of the international dry eye workshop (2007). Ocul. Surf. 2007, 5:93-107.
62. Somero G.N. Protons, osmolytes, and fitness of internal milieu for protein function. Am. J. Physiol. 1986, 251:R197-R213.
63. Strong B., Farley W., Stern M.E., Pflugfelder S.C. Topical cyclosporine inhibits conjunctival epithelial apoptosis in experimental murine keratoconjunctivitis sicca. Cornea 2005, 24:80-85.
64. Sullivan B.D., Whitmer D., Nichols K.K., Tomlinson A., Foulks G.N., Geerling G., Pepose J.S., Kosheleff V., Porreco A., Lemp M.A. An objective approach to dry eye disease severity. Invest. Ophthalmol. Vis. Sci. 2010, 51:6125-6130.
65. Tomlinson A., Khanal S., Ramaesh K., Diaper C., McFadyen A. Tear film osmolarity: determination of a referent for dry eye diagnosis. Invest. Ophthalmol. Vis. Sci. 2006, 47:4309-4315.
66. Uchida S., Yamauchi A., Preston A.S., Kwon H.M., Handler J.S. Medium tonicity regulates expression of the Na(+)- and Cl(-)-dependent betaine transporter in Madin-Darby canine kidney cells by increasing transcription of the transporter gene. J. Clin. Invest. 1993, 91:1604-1607.
67. Venkatesu P., Lee M.J., Lin H.M. Osmolyte counteracts urea-induced denaturation of alpha-chymotrypsin. J. Phys. Chem. B 2009, 113:5327-5338.
68. Verbalis J.G. Brain volume regulation in response to changes in osmolality. Neuroscience 2010, 168:862-870.
69. Waldegger S., Steuer S., Risler T., Heidland A., Capasso G., Massry S., Lang F. Mechanisms and clinical significance of cell volume regulation. Nephrol. Dial. Transplant. 1998, 13:867-874.
70. Wang L., Dai W., Lu L. Hyperosmotic stress-induced corneal epithelial cell death through activation of Polo-like kinase 3 and c-Jun. Invest. Ophthalmol. Vis. Sci. 2011, 52:3200-3206.
71. Warskulat U., Brookmann S., Felsner I., Brenden H., Grether-Beck S., Haussinger D. Ultraviolet A induces transport of compatible organic osmolytes in human dermal fibroblasts. Exp. Dermatol. 2008, 17:1031-1036.
72. Warskulat U., Reinen A., Grether-Beck S., Krutmann J., Haussinger D. The osmolyte strategy of normal human keratinocytes in maintaining cell homeostasis. J. Invest. Dermatol. 2004, 123:516-521.
73. Wehner F., Olsen H., Tinel H., Kinne-Saffran E., Kinne R.K.H. Cell volume regulation: osmolytes, osmolyte transport, and signal transduction. Rev. Physiol. Biochem. Pharmacol. 2003, 1-80. Springer, Berlin, Heidelberg.
74. Woo S.K., Lee S.D., Kwon H.M. TonEBP transcriptional activator in the cellular response to increased osmolality. Pflugers Arch. 2002, 444:579-585.
75. Wood J.M., Bremer E., Csonka L.N., Kraemer R., Poolman B., van der Heide T., Smith L.T. Osmosensing and osmoregulatory compatible solute accumulation by bacteria. Comp. Biochem. Physiol. A - Mol. Integr. Physiol. 2001, 130:437-460.
76. Xia Z., Dickens M., Raingeaud J., Davis R.J., Greenberg M.E. Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis. Science 1995, 270:1326-1331.
77. Yamauchi A., Uchida S., Kwon H.M., Preston A.S., Robey R.B., Garcia-Perez A., Burg M.B., Handler J.S. Cloning of a Na(+)- and Cl(-)-dependent betaine transporter that is regulated by hypertonicity. J. Biol. Chem. 1992, 267:649-652.
78. Yeh S., Song X.J., Farley W., Li D.Q., Stern M.E., Pflugfelder S.C. Apoptosis of ocular surface cells in experimentally induced dry eye. Invest. Ophthalmol. Vis. Sci. 2003, 44:124-129.
79. Yu S.P., Choi D.W. Ions, cell volume, and apoptosis. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:9360-9362.
80. Zhou Y., Holmseth S., Hua R., Lehre A.C., Olofsson A.M., Poblete-Naredo I., Kempson S.A., Danbolt N.C. The betaine-GABA transporter (BGT1, slc6a12) is predominantly expressed in the liver and at lower levels in the kidneys and at the brain surface. Am. J. Physiol. Renal Physiol. 2012, 302:F316-F328.
81. Zoukhri D. Effect of inflammation on lacrimal gland function. Exp. Eye Res. 2006, 82:885-898.