Altered age-related changes in bioenergetic properties and mitochondrial morphology in fibroblasts from sporadic amyotrophic lateral sclerosis patients

Neurobiology of Aging

Volumn 36, Issue 10, 2015, Pages 2893-2903

  Allen, Scott P ^a   Duffy, Lynn M ^a   Shaw, Pamela J ^a   Grierson, Andrew J ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

Aging; ALS; Metabolism; Mitochondria; Sporadic

Indexed keywords

GLUCOSE;

ACIDIFICATION; ADULT; AGED; AGING; AMYOTROPHIC LATERAL SCLEROSIS; ARTICLE; BIOENERGY; CELL METABOLISM; CELL STRUCTURE; CLINICAL ARTICLE; CONTROLLED STUDY; ENERGY METABOLISM; FEMALE; FIBROBLAST; GLYCOLYSIS; HUMAN; HUMAN CELL; MALE; MIDDLE AGED; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; OXIDATION; OXYGEN CONSUMPTION; PRIORITY JOURNAL; SPORADIC AMYOTROPHIC LATERAL SCLEROSIS; CELL CULTURE; METABOLISM; PATHOLOGY; PHYSIOLOGY; ULTRASTRUCTURE;

ADULT; AGED; AGING; AMYOTROPHIC LATERAL SCLEROSIS; CELLS, CULTURED; ENERGY METABOLISM; FEMALE; FIBROBLASTS; GLYCOLYSIS; HUMANS; MALE; MIDDLE AGED; MITOCHONDRIA; OXYGEN CONSUMPTION;

EID: 84940938999     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2015.07.013     Document Type: Article

References (61)

1. Ahmed I., Ponery A.S., Nur-E-Kamal A., Kamal J., Meshel A.S., Sheetz M.P., Schindler M., Meiners S. Morphology, cytoskeletal organization, and myosin dynamics of mouse embryonic fibroblasts cultured on nanofibrillar surfaces. Mol. Cell Biochem. 2007, 301:241-249.
2. Allen S.P., Rajan S., Duffy L., Mortiboys H., Higginbottom A., Grierson A.J., Shaw P.J. Superoxide dismutase 1 mutation in a cellular model of amyotrophic lateral sclerosis shifts energy generation from oxidative phosphorylation to glycolysis. Neurobiol. Aging 2014, 35:1499-1509.
3. Attwell D., Laughlin S.B. An energy budget for signaling in the grey matter of the brain. J. Cereb. Blood Flow Metab. 2001, 21:1133-1145.
4. Benard G., Bellance N., James D., Parrone P., Fernandez H., Letellier T., Rossignol R. Mitochondrial bioenergetics and structural network organization. J. Cell Sci. 2007, 120:838-848.
5. Borthwick G.M., Johnson M.A., Ince P.G., Shaw P.J., Turnbull D.M. Mitochondrial enzyme activity in amyotrophic lateral sclerosis: implications for the role of mitochondria in neuronal cell death. Ann. Neurol. 1999, 46:787-790.
6. Bowling A.C., Schulz J.B., Brown R.H., Beal M.F. Superoxide dismutase activity, oxidative damage, and mitochondrial energy metabolism in familial and sporadic amyotrophic lateral sclerosis. J. Neurochem. 1993, 61:2322-2325.
7. Carrasco D.I., Bichler E.K., Rich M.M., Wang X., Seburn K.L., Pinter M.J. Motor terminal degeneration unaffected by activity changes in SOD1(G93A) mice; a possible role for glycolysis. Neurobiol. Dis. 2012, 48:132-140.
8. Carri M.T., Ferri A., Battistoni A., Famhy L., Gabbianelli R., Poccia F., Rotilio G. Expression of a Cu,Zn superoxide dismutase typical of familial amyotrophic lateral sclerosis induces mitochondrial alteration and increase of cytosolic Ca2+ concentration in transfected neuroblastoma SH-SY5Y cells. FEBS Lett. 1997, 414:365-368.
9. Chen H., Chan D.C. Mitochondrial dynamics-fusion, fission, movement, and mitophagy-in neurodegenerative diseases. Hum. Mol. Genet. 2009, 18:R169-R176.
10. Chen H., McCaffery J.M., Chan D.C. Mitochondrial fusion protects against neurodegeneration in the cerebellum. Cell 2007, 130:548-562.
11. Chio A., Logroscino G., Hardiman O., Swingler R., Mitchell D., Beghi E., Traynor B.G., Eurals C. Prognostic factors in ALS: a critical review. Amyotroph. Lateral Scler. 2009, 10:310-323.
12. De Vos K.J., Allan V.J., Grierson A.J., Sheetz M.P. Mitochondrial function and actin regulate dynamin-related protein 1-dependent mitochondrial fission. Curr. Biol. 2005, 15:678-683.
13. De Vos K.J., Chapman A.L., Tennant M.E., Manser C., Tudor E.L., Lau K.F., Brownlees J., Ackerley S., Shaw P.J., McLoughlin D.M., Shaw C.E., Leigh P.N., Miller C.C., Grierson A.J. Familial amyotrophic lateral sclerosis-linked SOD1 mutants perturb fast axonal transport to reduce axonal mitochondria content. Hum. Mol. Genet. 2007, 16:2720-2728.
14. De Vos K.J., Grierson A.J., Ackerley S., Miller C.C. Role of axonal transport in neurodegenerative diseases. Annu. Rev. Neurosci. 2008, 31:151-173.
15. De Vos K.J., Sheetz M.P. Visualization and quantification of mitochondrial dynamics in living animal cells. Methods Cell Biol. 2007, 80:627-682.
16. del Aguila M.A., Longstreth W.T., McGuire V., Koepsell T.D., van Belle G. Prognosis in amyotrophic lateral sclerosis: a population-based study. Neurology 2003, 60:813-819.
17. Desler C., Hansen T.L., Frederiksen J.B., Marcker M.L., Singh K.K., Juel Rasmussen L. Is there a Link between mitochondrial Reserve respiratory capacity and aging?. J. Aging Res. 2012, 2012:192503.
18. Ferraiuolo L., Kirby J., Grierson A.J., Sendtner M., Shaw P.J. Molecular pathways of motor neuron injury in amyotrophic lateral sclerosis. Nat. Rev. Neurol. 2011, 7:616-630.
19. Forbes R.B., Colville S., Swingler R.J. The epidemiology of amyotrophic lateral sclerosis (ALS/MND) in people aged 80 or over. Age Ageing 2004, 33:131-134. Scottish, A.L.S.M.N.D.R.
20. Fujita K., Yamauchi M., Shibayama K., Ando M., Honda M., Nagata Y. Decreased cytochrome c oxidase activity but unchanged superoxide dismutase and glutathione peroxidase activities in the spinal cords of patients with amyotrophic lateral sclerosis. J. Neurosci. Res. 1996, 45:276-281.
21. Giedt R.J., Pfeiffer D.R., Matzavinos A., Kao C.Y., Alevriadou B.R. Mitochondrial dynamics and motility inside living vascular endothelial cells: role of bioenergetics. Ann. Biomed. Eng. 2012, 40:1903-1916.
22. Gomes L.C., Di Benedetto G., Scorrano L. During autophagy mitochondria elongate, are spared from degradation and sustain cell viability. Nat. Cell Biol. 2011, 13:589-598.
23. Greco M., Villani G., Mazzucchelli F., Bresolin N., Papa S., Attardi G. Marked aging-related decline in efficiency of oxidative phosphorylation in human skin fibroblasts. FASEB J. 2003, 17:1706-1708.
24. Guillery O., Malka F., Frachon P., Milea D., Rojo M., Lombes A. Modulation of mitochondrial morphology by bioenergetics defects in primary human fibroblasts. Neuromuscul. Disord. 2008, 18:319-330.
25. Harman D. Aging: a theory based on free radical and radiation chemistry. J. Gerontol. 1956, 11:298-300.
26. Hekimi S., Lapointe J., Wen Y. Taking a "good" look at free radicals in the aging process. Trends Cell Biol. 2011, 21:569-576.
27. Indo H.P., Davidson M., Yen H.C., Suenaga S., Tomita K., Nishii T., Higuchi M., Koga Y., Ozawa T., Majima H.J. Evidence of ROS generation by mitochondria in cells with impaired electron transport chain and mitochondrial DNA damage. Mitochondrion 2007, 7:106-118.
28. Jongkind J.F., Verkerk A., Poot M. Glucose flux through the hexose-monophosphate shunt and Nadp(H) levels during Invitro aging of human-skin fibroblasts. Gerontology 1987, 33:281-286.
29. Karbowski M., Youle R.J. Dynamics of mitochondrial morphology in healthy cells and during apoptosis. Cell Death Differ. 2003, 10:870-880.
30. Karni-Schmidt O., Friedler A., Zupnick A., McKinney K., Mattia M., Beckerman R., Bouvet P., Sheetz M., Fersht A., Prives C. Energy-dependent nucleolar localization of p53 in vitro requires two discrete regions within the p53 carboxyl terminus. Oncogene 2007, 26:3878-3891.
31. Kirby J., Halligan E., Baptista M.J., Allen S., Heath P.R., Holden H., Barber S.C., Loynes C.A., Wood-Allum C.A., Lunec J., Shaw P.J. Mutant SOD1 alters the motor neuronal transcriptome: implications for familial ALS. Brain 2005, 128:1686-1706.
32. Kirk K., Gennings C., Hupf J.C., Tadesse S., D'Aurelio M., Kawamata H., Valsecchi F., Mitsumoto H., Manfredi G. Bioenergetic markers in skin fibroblasts of sporadic amyotrophic lateral sclerosis and progressive lateral sclerosis patients. Ann. Neurol. 2014, 76:620-624. for the, A.L.S.P.L.S.C.S.G.
33. Kirkwood T.B. Time of our lives. What controls the length of life?. EMBO Rep. 2005, 6 Spec No:S4-S8.
34. Koopman W.J., Visch H.J., Verkaart S., van den Heuvel L.W., Smeitink J.A., Willems P.H. Mitochondrial network complexity and pathological decrease in complex I activity are tightly correlated in isolated human complex I deficiency. Am. J. Physiol. Cell Physiol. 2005, 289:C881-C890.
35. Lin M.T., Beal M.F. Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 2006, 443:787-795.
36. Logroscino G., Traynor B.J., Hardiman O., Chio A., Mitchell D., Swingler R.J., Millul A., Benn E., Beghi E. Incidence of amyotrophic lateral sclerosis in Europe. J. Neurol. Neurosurg. Psychiatry 2010, 81:385-390. Eurals.
37. Magrane J., Hervias I., Henning M.S., Damiano M., Kawamata H., Manfredi G. Mutant SOD1 in neuronal mitochondria causes toxicity and mitochondrial dynamics abnormalities. Hum. Mol. Genet. 2009, 18:4552-4564.
38. Mattiazzi M., D'Aurelio M., Gajewski C.D., Martushova K., Kiaei M., Beal M.F., Manfredi G. Mutated human SOD1 causes dysfunction of oxidative phosphorylation in mitochondria of transgenic mice. J. Biol. Chem. 2002, 277:29626-29633.
39. Meacci E., Vannini F., Vasta V., Farnararo M., Bruni P. Effect of aging on insulin Regulation of fructose 2,6-Bisphosphate metabolism in human fibroblasts. Biochem. Mol. Biol. Int. 1993, 30:91-98.
40. Mead R.J., Higginbottom A., Allen S.P., Kirby J., Bennett E., Barber S.C., Heath P.R., Coluccia A., Patel N., Gardner I., Brancale A., Grierson A.J., Shaw P.J. S[+] Apomorphine is a CNS penetrating activator of the Nrf2-ARE pathway with activity in mouse and patient fibroblast models of amyotrophic lateral sclerosis. Free Radic. Biol. Med. 2013, 61C:438-452.
41. Menzies F.M., Cookson M.R., Taylor R.W., Turnbull D.M., Chrzanowska-Lightowlers Z.M., Dong L., Figlewicz D.A., Shaw P.J. Mitochondrial dysfunction in a cell culture model of familial amyotrophic lateral sclerosis. Brain 2002, 125:1522-1533.
42. Mortiboys H., Johansen K.K., Aasly J.O., Bandmann O. Mitochondrial impairment in patients with Parkinson disease with the G2019S mutation in LRRK2. Neurology 2010, 75:2017-2020.
43. Pich S., Bach D., Briones P., Liesa M., Camps M., Testar X., Palacin M., Zorzano A. The Charcot-Marie-Tooth type 2A gene product, Mfn2, up-regulates fuel oxidation through expression of OXPHOS system. Hum. Mol. Genet. 2005, 14:1405-1415.
44. Raimondi A., Mangolini A., Rizzardini M., Tartari S., Massari S., Bendotti C., Francolini M., Borgese N., Cantoni L., Pietrini G. Cell culture models to investigate the selective vulnerability of motoneuronal mitochondria to familial ALS-linked G93ASOD1. Eur. J. Neurosci. 2006, 24:387-399.
45. Ramamoorthy M., Sykora P., Scheibye-Knudsen M., Dunn C., Kasmer C., Zhang Y., Becker K.G., Croteau D.L., Bohr V.A. Sporadic Alzheimer disease fibroblasts display an oxidative stress phenotype. Free Radic. Biol. Med. 2012, 53:1371-1380.
46. Raman R., Allen S.P., Goodall E.F., Kramer S., Ponger L.L., Heath P.R., Milo M., Hollinger H.C., Walsh T., Highley J.R., Olpin S., McDermott C.J., Shaw P.J., Kirby J. Gene expression signatures in motor neuron disease fibroblasts reveal dysregulation of metabolism, hypoxia-response and RNA processing functions. Neuropathol. Appl. Neurobiol. 2014, 41:201-226.
47. Rambold A.S., Kostelecky B., Elia N., Lippincott-Schwartz J. Tubular network formation protects mitochondria from autophagosomal degradation during nutrient starvation. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:10190-10195.
48. Rambold A.S., Kostelecky B., Lippincott-Schwartz J. Together we are stronger: fusion protects mitochondria from autophagosomal degradation. Autophagy 2011, 7:1568-1569.
49. Reddy P.H. Mitochondrial medicine for aging and neurodegenerative diseases. Neuromolecular Med. 2008, 10:291-315.
50. Sasaki S., Iwata M. Mitochondrial alterations in the spinal cord of patients with sporadic amyotrophic lateral sclerosis. J. Neuropathol. Exp. Neurol. 2007, 66:10-16.
51. Seo A.Y., Joseph A.M., Dutta D., Hwang J.C., Aris J.P., Leeuwenburgh C. New insights into the role of mitochondria in aging: mitochondrial dynamics and more. J. Cell Sci. 2010, 123:2533-2542.
52. Shutt T., Geoffrion M., Milne R., McBride H.M. The intracellular redox state is a core determinant of mitochondrial fusion. EMBO Rep. 2012, 13:909-915.
53. Swerdlow R.H. Mitochondria in cybrids containing mtDNA from persons with mitochondriopathies. J. Neurosci. Res. 2007, 85:3416-3428.
54. Terman A., Brunk U.T. The aging myocardium: roles of mitochondrial damage and lysosomal degradation. Heart Lung Circ. 2005, 14:107-114.
55. Terman A., Dalen H., Eaton J.W., Neuzil J., Brunk U.T. Mitochondrial recycling and aging of cardiac myocytes: the role of autophagocytosis. Exp. Gerontol. 2003, 38:863-876.
56. Testa D., Lovati R., Ferrarini M., Salmoiraghi F., Filippini G. Survival of 793 patients with amyotrophic lateral sclerosis diagnosed over a 28-year period. Amyotroph. Lateral Scler. Other Motor Neuron Disord. 2004, 5:208-212.
57. Tran A.D., Marmo T.P., Salam A.A., Che S., Finkelstein E., Kabarriti R., Xenias H.S., Mazitschek R., Hubbert C., Kawaguchi Y., Sheetz M.P., Yao T.P., Bulinski J.C. HDAC6 deacetylation of tubulin modulates dynamics of cellular adhesions. J. Cell Sci. 2007, 120:1469-1479.
58. Vergauwen B., De Vos D., Van Beeumen J.J. Characterization of the bifunctional gamma-glutamate-cysteine ligase/glutathione synthetase (GshF) of pasteurella multocida. J. Biol. Chem. 2006, 281:4380-4394.
59. Yoon Y.S., Yoon D.S., Lim I.K., Yoon S.H., Chung H.Y., Rojo M., Malka F., Jou M.J., Martinou J.C., Yoon G. Formation of elongated giant mitochondria in DFO-induced cellular senescence: involvement of enhanced fusion process through modulation of Fis1. J. Cell Physiol. 2006, 209:468-480.
60. Zala D., Hinckelmann M.V., Yu H., Lyra da Cunha M.M., Liot G., Cordelieres F.P., Marco S., Saudou F. Vesicular glycolysis provides on-board energy for fast axonal transport. Cell 2013, 152:479-491.
61. Zorzano A., Liesa M., Sebastian D., Segales J., Palacin M. Mitochondrial fusion proteins: dual regulators of morphology and metabolism. Semin. Cell Dev. Biol. 2010, 21:566-574.