Measurement of systemic mitochondrial function in advanced Primary Open-Angle Glaucoma and leber hereditary optic neuropathy

PLoS ONE

Volumn 10, Issue 10, 2015, Pages

  Van Bergen, Nicole J ^a   Crowston, Jonathan G ^a   Craig, Jamie E ^b   Burdon, Kathryn P ^b   Kearns, Lisa S ^a   Sharma, Shiwani ^b   Hewitt, Alex W ^a   Mackey, David A ^c,d   Trounce, Ian A ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b FLINDERS UNIVERSITY   (Australia)

^c UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^d LIONS EYE INSTITUTE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; CYTOCHROME C OXIDASE; GALACTOSE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE);

AGED; ARTICLE; CELL FUNCTION; CELL GROWTH; CELL PROLIFERATION; CLINICAL ARTICLE; COMPARATIVE STUDY; CONTROLLED STUDY; DISEASE COURSE; DISEASE SEVERITY; ENZYME ACTIVITY; ENZYME SYNTHESIS; FEMALE; HUMAN; HUMAN CELL; LEBER HEREDITARY OPTIC NEUROPATHY; LYMPHOBLAST; MALE; MITOCHONDRION; OPEN ANGLE GLAUCOMA; POLYMERASE CHAIN REACTION; VALIDATION STUDY; VERY ELDERLY; METABOLISM; MIDDLE AGED; PHYSIOLOGY;

ADENOSINE TRIPHOSPHATE; AGED; CELL PROLIFERATION; FEMALE; GALACTOSE; GLAUCOMA, OPEN-ANGLE; HUMANS; MALE; MIDDLE AGED; MITOCHONDRIA; OPTIC ATROPHY, HEREDITARY, LEBER;

EID: 84949477602     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0140919     Document Type: Article

References (78)

1. Van Bergen N, Chakrabarti R, O'Neill E, Crowston J, Trounce I (2011) Mitochondrial disorders and the eye. Eye and Brain 3: 29-47.
2. Chrysostomou V, Rezania F, Trounce IA, Crowston JG (2013) Oxidative stress and mitochondrial dysfunction in glaucoma. Curr Opin Pharmacol 13: 12-15. doi: 10.1016/j.coph.2012.09.008 PMID: 23069478
3. Chrysostomou V, Trounce IA, Crowston JG (2010) Mechanisms of retinal ganglion cell injury in aging and glaucoma. Ophthalmic Res 44: 173-178. doi: 10.1159/000316478 PMID: 20829641
4. Lee S, Van Bergen NJ, Kong GY, Chrysostomou V, Waugh HS, et al. (2011) Mitochondrial dysfunction in glaucoma and emerging bioenergetic therapies. Exp Eye Res 93: 204-212. doi: 10.1016/j.exer. 2010.07.015 PMID: 20691180
5. Kong GY, Van Bergen NJ, Trounce IA, Crowston JG (2009) Mitochondrial dysfunction and glaucoma. J Glaucoma 18: 93-100. doi: 10.1097/IJG.0b013e318181284f PMID: 19225343
6. Osborne NN (2008) Pathogenesis of ganglion "cell death" in glaucoma and neuroprotection: focus on ganglion cell axonal mitochondria. Prog Brain Res 173: 339-352. doi: 10.1016/S0079-6123(08)01124-2 PMID: 18929120
7. Osborne NN (2010) Mitochondria: Their role in ganglion cell death and survival in primary open angle glaucoma. Experimental Eye Research 90: 750-757.
8. Osborne NN, Alvarez CN, del Olmo Aguado S (2014) Targeting mitochondrial dysfunction as in aging and glaucoma. Drug Discov Today 19: 1613-1622. doi: 10.1016/j.drudis.2014.05.010 PMID: 24880106
9. Osborne NN, del Olmo-Aguado S (2013) Maintenance of retinal ganglion cell mitochondrial functions as a neuroprotective strategy in glaucoma. Curr Opin Pharmacol 13: 16-22. doi: 10.1016/j.coph.2012. 09.002 PMID: 22999653
10. Mackey DA, Oostra RJ, Rosenberg T, Nikoskelainen E, Bronte-Stewart J, et al. (1996) Primary pathogenic mtDNA mutations in multigeneration pedigrees with Leber hereditary optic neuropathy. Am J Hum Genet 59: 481-485. PMID: 8755941
11. Alexander C, Votruba M, Pesch UE, Thiselton DL, Mayer S, et al. (2000) OPA1, encoding a dynaminrelated GTPase, is mutated in autosomal dominant optic atrophy linked to chromosome 3q28. Nat Genet 26: 211-215. PMID: 11017080
12. Delettre C, Lenaers G, Griffoin J, Gigarel N, Lorenzo C, et al. (2000) Nuclear gene OPA1, encoding a mitochondrial dynamin-related protein, is mutated in dominant optic atrophy. Nat Genet 26: 207-210. PMID: 11017079
13. Van Bergen NJ, Crowston JG, Kearns LS, Staffieri SE, Hewitt AW, et al. (2011) Mitochondrial oxidative phosphorylation compensation may preserve vision in patients with OPA1-linked autosomal dominant optic atrophy. PLoS One 6: e21347. doi: 10.1371/journal.pone.0021347 PMID: 21731710
14. Mashima Y, Kimura I, Yamamoto Y, Ohde H, Ohtake Y, et al. (2003) Optic disc excavation in the atrophic stage of Leber's hereditary optic neuropathy: comparison with normal tension glaucoma. Graefes Arch Clin Exp Ophthalmol 241: 75-80. PMID: 12605258
15. Trobe JD, Glaser JS, Cassady J, Herschler J, Anderson DR (1980) Nonglaucomatous excavation of the optic disc. Arch Ophthalmol 98: 1046-1050. PMID: 7387507
16. O'Neill EC, Danesh-Meyer HV, Kong GX, Hewitt AW, Coote MA, et al. (2011) Optic disc evaluation in optic neuropathies: the optic disc assessment project. Ophthalmology 118: 964-970. doi: 10.1016/j. ophtha.2010.09.002 PMID: 21126771
17. Barron MJ, Griffiths P, Turnbull DM, Bates D, Nichols P (2004) The distributions of mitochondria and sodium channels reflect the specific energy requirements and conduction properties of the human optic nerve head. Br J Ophthalmol 88: 286-290. PMID: 14736793
18. Leske MC, Heijl A, Hyman L, Bengtsson B, Dong L, et al. (2007) Predictors of long-term progression in the early manifest glaucoma trial. Ophthalmology 114: 1965-1972. PMID: 17628686
19. Heijl A, Leske MC, Bengtsson B, Hyman L, Hussein M (2002) Reduction of intraocular pressure and glaucoma progression: results from the Early Manifest Glaucoma Trial. Arch Ophthalmol 120: 1268-1279. PMID: 12365904
20. Coleman AL (1999) Glaucoma. Lancet 354: 1803-1810. PMID: 10577657
21. Lascaratos G, Garway-Heath DF, Willoughby CE, Chau KY, Schapira AH (2012) Mitochondrial dysfunction in glaucoma: understanding genetic influences. Mitochondrion 12: 202-212. doi: 10.1016/j. mito.2011.11.004 PMID: 22138560
22. Abu-Amero KK, Morales J, Bosley TM (2006) Mitochondrial abnormalities in patients with primary open-angle glaucoma. Invest Ophthalmol Vis Sci 47: 2533-2541. PMID: 16723467
23. He Y, Leung KW, Zhang YH, Duan S, Zhong XF, et al. (2008) Mitochondrial complex I defect induces ROS release and degeneration in trabecular meshwork cells of POAG patients: protection by antioxidants. Invest Ophthalmol Vis Sci 49: 1447-1458. doi: 10.1167/iovs.07-1361 PMID: 18385062
24. Lee S, Sheck L, Crowston JG, Van Bergen NJ, O'Neill EC, et al. (2012) Impaired complex-I-linked respiration and ATP synthesis in primary open-angle glaucoma patient lymphoblasts. Invest Ophthalmol Vis Sci 53: 2431-2437. doi: 10.1167/iovs.12-9596 PMID: 22427588
25. Lascaratos G, Chau KY, Zhu H, Gkotsi D, King R, et al. (2015) Resistance to the most common optic neuropathy is associated with systemic mitochondrial efficiency. Neurobiol Dis 82: 78-85. doi: 10.1016/j.nbd.2015.05.012 PMID: 26054436
26. Souzeau E, Burdon KP, Dubowsky A, Grist S, Usher B, et al. (2013) Higher prevalence of myocilin mutations in advanced glaucoma in comparison with less advanced disease in an Australasian disease registry. Ophthalmology 120: 1135-1143. doi: 10.1016/j.ophtha.2012.11.029 PMID: 23453510
27. Souzeau E, Goldberg I, Healey PR, Mills RA, Landers J, et al. (2012) Australian and New Zealand Registry of Advanced Glaucoma: methodology and recruitment. Clin Experiment Ophthalmol 40: 569-575. doi: 10.1111/j.1442-9071.2011.02742.x PMID: 22171965
28. Burdon KP, Hewitt AW, Mackey DA, Mitchell P, Craig JE (2010) Tag SNPs detect association of the CYP1B1 gene with primary open angle glaucoma. Mol Vis 16: 2286-2293. PMID: 21139974
29. Burdon KP, Macgregor S, Hewitt AW, Sharma S, Chidlow G, et al. (2011) Genome-wide association study identifies susceptibility loci for open angle glaucoma at TMCO1 and CDKN2B-AS1. Nat Genet 43: 574-578. doi: 10.1038/ng.824 PMID: 21532571
30. Thorleifsson G, Walters GB, Hewitt AW, Masson G, Helgason A, et al. (2010) Common variants near CAV1 and CAV2 are associated with primary open-angle glaucoma. Nat Genet 42: 906-909. doi: 10.1038/ng.661 PMID: 20835238
31. Young TK, Souzeau E, Liu L, Kearns LS, Burdon KP, et al. (2012) Compound heterozygote myocilin mutations in a pedigree with high prevalence of primary open-angle glaucoma. Mol Vis 18: 3064-3069. PMID: 23304066
32. Yu-Wai-Man P, Votruba M, Moore AT, Chinnery PF (2014) Treatment strategies for inherited optic neuropathies: past, present and future. Eye (Lond) 28: 521-537.
33. Yu-Wai-Man P, Griffiths PG, Hudson G, Chinnery PF (2009) Inherited mitochondrial optic neuropathies. J Med Genet 46: 145-158. doi: 10.1136/jmg.2007.054270 PMID: 19001017
34. Van Bergen NJ, Blake RE, Crowston JG, Trounce IA (2014) Oxidative phosphorylation measurement in cell lines and tissues. Mitochondrion 15: 24-33. doi: 10.1016/j.mito.2014.03.003 PMID: 24657935
35. Robinson BH, Petrova-Benedict R, Buncic JR, Wallace DC (1992) Nonviability of cells with oxidative defects in galactose medium: a screening test for affected patient fibroblasts. Biochem Med Metab Biol 48: 122-126. PMID: 1329873
36. Holloszy JO, Oscai LB, Don IJ, Mole PA (1970) Mitochondrial citric acid cycle and related enzymes: adaptive response to exercise. Biochem Biophys Res Commun 40: 1368-1373. PMID: 4327015
37. Williams RS, Salmons S, Newsholme EA, Kaufman RE, Mellor J (1986) Regulation of nuclear and mitochondrial gene expression by contractile activity in skeletal muscle. J Biol Chem 261: 376-380. PMID: 3941082
38. Bonora E, Porcelli AM, Gasparre G, Biondi A, Ghelli A, et al. (2006) Defective oxidative phosphorylation in thyroid oncocytic carcinoma is associated with pathogenic mitochondrial DNA mutations affecting complexes I and III. Cancer Res 66: 6087-6096. PMID: 16778181
39. Manfredi G, Yang L, Gajewski CD, Mattiazzi M (2002) Measurements of ATP in mammalian cells. Methods 26: 317-326. PMID: 12054922
40. Zanna C, Ghelli A, Porcelli AM, Martinuzzi A, Carelli V, et al. (2005) Caspase-independent death of Leber's hereditary optic neuropathy cybrids is driven by energetic failure and mediated by AIF and Endonuclease G. Apoptosis 10: 997-1007. PMID: 16151635
41. McKenzie M, Chiotis M, Pinkert CA, Trounce IA (2003) Functional respiratory chain analyses in murid xenomitochondrial cybrids expose coevolutionary constraints of cytochrome b and nuclear subunits of complex III. Mol Biol Evol 20: 1117-1124. PMID: 12777531
42. Haas RH, Parikh S, Falk MJ, Saneto RP, Wolf NI, et al. (2008) The in-depth evaluation of suspected mitochondrial disease. Mol Genet Metab 94: 16-37. doi: 10.1016/j.ymgme.2007.11.018 PMID: 18243024
43. Brown MD, Trounce IA, Jun AS, Allen JC, Wallace DC (2000) Functional analysis of lymphoblast and cybrid mitochondria containing the 3460, 11778, or 14484 Leber's hereditary optic neuropathy mitochondrial DNA mutation. J Biol Chem 275: 39831-39836. PMID: 10976107
44. Giordano C, Iommarini L, Giordano L, Maresca A, Pisano A, et al. (2013) Efficient mitochondrial biogenesis drives incomplete penetrance in Leber's hereditary optic neuropathy. Brain.
45. Wallace DC, Fan W, Procaccio V (2010) Mitochondrial energetics and therapeutics. Annu Rev Pathol 5: 297-348. doi: 10.1146/annurev.pathol.4.110807.092314 PMID: 20078222
46. Thorburn DR, Chow CW, Kirby DM (2004) Respiratory chain enzyme analysis in muscle and liver. Mitochondrion 4: 363-375. PMID: 16120398
47. Trounce I, Kim Y, Jun A, Wallace D (1996) Assessment of mitochondrial oxidative phosphorylation in patient muscle biopsies, lymphoblasts, and transmitochondrial cell lines. Methods Enzymol 264: 484-509. PMID: 8965721
48. Brown M, Trounce I, Jun A, Allen J, Wallace D (2000) Functional analysis of lymphoblast and cybrid mitochondria containing the 11778, 3460 or 14484 Leber's hereditary optic neuropathy mitochondrial DNA mutation. J Biol Chem 275: 39831-39836. PMID: 10976107
49. Mayorov VI, Lowrey AJ, Biousse V, Newman NJ, Cline SD, et al. (2008) Mitochondrial oxidative phosphorylation in autosomal dominant optic atrophy. BMC Biochem 9: 22. doi: 10.1186/1471-2091-9-22 PMID: 18783614
50. Xu Y, Sutachan JJ, Plesken H, Kelley RI, Schlame M (2005) Characterization of lymphoblast mitochondria from patients with Barth syndrome. Lab Invest 85: 823-830. PMID: 15806137
51. Tatuch Y, Robinson BH (1993) The mitochondrial DNA mutation at 8993 associated with NARP slows the rate of ATP synthesis in isolated lymphoblast mitochondria. Biochemical and Biophysical Research Communications 192: 124-128. PMID: 8476414
52. Gill KP, Hewitt AW, Davidson KC, Pébay A, Wong RCB (2014) Methods of Retinal Ganglion Cell Differentiation From Pluripotent Stem Cells. Translational Vision Science & Technology 3: 2.
53. Takahashi K, Yamanaka S (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126: 663-676. PMID: 16904174
54. Fan BJ, Leung YF, Wang N, Lam SC, Liu Y, et al. (2004) Genetic and environmental risk factors for primary open-angle glaucoma. Chin Med J (Engl) 117: 706-710.
55. Janssen SF, Gorgels TG, Ramdas WD, Klaver CC, van Duijn CM, et al. (2013) The vast complexity of primary open angle glaucoma: disease genes, risks, molecular mechanisms and pathobiology. Prog Retin Eye Res 37: 31-67. doi: 10.1016/j.preteyeres.2013.09.001 PMID: 24055863
56. Shin DH, Becker B, Kolker AE (1977) Family history in primary open-angle glaucoma. Arch Ophthalmol 95: 598-600. PMID: 849183
57. Charliat G, Jolly D, Blanchard F (1994) Genetic risk factor in primary open-angle glaucoma: a case-control study. Ophthalmic Epidemiol 1: 131-138. PMID: 8790619
58. Green CM, Kearns LS, Wu J, Barbour JM, Wilkinson RM, et al. (2007) How significant is a family history of glaucoma? Experience from the Glaucoma Inheritance Study in Tasmania. Clin Experiment Ophthalmol 35: 793-799. doi: 10.1111/j.1442-9071.2007.01612.x PMID: 18173405
59. Rezaie T, Child A, Hitchings R, Brice G, Miller L, et al. (2002) Adult-onset primary open-angle glaucoma caused by mutations in optineurin. Science 295: 1077-1079. PMID: 11834836
60. Sheffield VC, Stone EM, Alward WL, Drack AV, Johnson AT, et al. (1993) Genetic linkage of familial open angle glaucoma to chromosome 1q21-q31. Nat Genet 4: 47-50. PMID: 8513321
61. Stone EM, Fingert JH, Alward WL, Nguyen TD, Polansky JR, et al. (1997) Identification of a gene that causes primary open angle glaucoma. Science 275: 668-670. PMID: 9005853
62. Awadalla MS, Fingert JH, Roos BE, Chen S, Holmes R, et al. (2015) Copy number variations of TBK1 in Australian patients with primary open-angle glaucoma. Am J Ophthalmol 159: 124-130 e121. doi: 10.1016/j.ajo.2014.09.044 PMID: 25284765
63. Gharahkhani P, Burdon KP, Fogarty R, Sharma S, Hewitt AW, et al. (2014) Common variants near ABCA1, AFAP1 and GMDS confer risk of primary open-angle glaucoma. Nat Genet 46: 1120-1125. doi: 10.1038/ng.3079 PMID: 25173105
64. Chen Y, Lin Y, Vithana EN, Jia L, Zuo X, et al. (2014) Common variants near ABCA1 and in PMM2 are associated with primary open-angle glaucoma. Nat Genet 46: 1115-1119. doi: 10.1038/ng.3078 PMID: 25173107
65. Hysi PG, Cheng CY, Springelkamp H, Macgregor S, Bailey JN, et al. (2014) Genome-wide analysis of multi-ancestry cohorts identifies new loci influencing intraocular pressure and susceptibility to glaucoma. Nat Genet 46: 1126-1130. doi: 10.1038/ng.3087 PMID: 25173106
66. Carnes MU, Liu YP, Allingham RR, Whigham BT, Havens S, et al. (2014) Discovery and functional annotation of SIX6 variants in primary open-angle glaucoma. PLoS Genet 10: e1004372. doi: 10.1371/journal.pgen.1004372 PMID: 24875647
67. Tam SP, Mok L, Chimini G, Vasa M, Deeley RG (2006) ABCA1 mediates high-affinity uptake of 25-hydroxycholesterol by membrane vesicles and rapid efflux of oxysterol by intact cells. Am J Physiol Cell Physiol 291: C490-502. PMID: 16611739
68. Wong YC, Holzbaur EL (2014) Optineurin is an autophagy receptor for damaged mitochondria in parkin-mediated mitophagy that is disrupted by an ALS-linked mutation. Proc Natl Acad Sci U S A 111: E4439-4448. doi: 10.1073/pnas.1405752111 PMID: 25294927
69. He Y, Leung KW, Zhuo YH, Ge J (2009) Pro370Leu mutant myocilin impairs mitochondrial functions in human trabecular meshwork cells. Mol Vis 15: 815-825. PMID: 19390644
70. Joe MK, Tomarev SI (2010) Expression of myocilin mutants sensitizes cells to oxidative stress-induced apoptosis: implication for glaucoma pathogenesis. Am J Pathol 176: 2880-2890. doi: 10.2353/ajpath. 2010.090853 PMID: 20382707
71. Nemesure B, Leske MC, He Q, Mendell N (1996) Analyses of reported family history of glaucoma: a preliminary investigation. The Barbados Eye Study Group. Ophthalmic Epidemiol 3: 135-141. PMID: 8956317
72. Mitchell P, Rochtchina E, Lee AJ, Wang JJ (2002) Bias in self-reported family history and relationship to glaucoma: the Blue Mountains Eye Study. Ophthalmic Epidemiol 9: 333-345. PMID: 12528918
73. Gramer G, Weber BH, Gramer E (2014) Results of a patient-directed survey on frequency of family history of glaucoma in 2170 patients. Invest Ophthalmol Vis Sci 55: 259-264. doi: 10.1167/iovs.13-13020 PMID: 24327611
74. Banerjee D, Banerjee A, Mookherjee S, Vishal M, Mukhopadhyay A, et al. (2013) Mitochondrial genome analysis of primary open angle glaucoma patients. PLoS One 8: e70760. doi: 10.1371/journal. pone.0070760 PMID: 23940637
75. Sundaresan P, Simpson DA, Sambare C, Duffy S, Lechner J, et al. (2014) Whole-mitochondrial genome sequencing in primary open-angle glaucoma using massively parallel sequencing identifies novel and known pathogenic variants. Genet Med 17: 279-284. doi: 10.1038/gim.2014.121 PMID: 25232845
76. Manolio TA, Brooks LD, Collins FS (2008) A HapMap harvest of insights into the genetics of common disease. J Clin Invest 118: 1590-1605. doi: 10.1172/JCI34772 PMID: 18451988
77. Wiggs JL, Yaspan BL, Hauser MA, Kang JH, Allingham RR, et al. (2012) Common variants at 9p21 and 8q22 are associated with increased susceptibility to optic nerve degeneration in glaucoma. PLoS Genet 8: e1002654. doi: 10.1371/journal.pgen.1002654 PMID: 22570617
78. Bailey JN, Yaspan BL, Pasquale LR, Hauser MA, Kang JH, et al. (2014) Hypothesis-independent pathway analysis implicates GABA and acetyl-CoA metabolism in primary open-angle glaucoma and normal-pressure glaucoma. Hum Genet 133: 1319-1330. doi: 10.1007/s00439-014-1468-7 PMID: 25037249