A screening-based platform for the assessment of cellular respiration in Caenorhabditis elegans

Nature Protocols

Volumn 11, Issue 10, 2016, Pages 1798-1816

  Koopman, Mandy ^a   Michels, Helen ^a   Dancy, Beverley M ^b   Kamble, Rashmi ^c   Mouchiroud, Laurent ^d   Auwerx, Johan ^d   Nollen, Ellen A A ^a   Houtkooper, Riekelt H ^c  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^b NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

^c ACADEMIC MEDICAL CENTER   (Netherlands)

^d EPFL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

AGING; ARTICLE; CAENORHABDITIS ELEGANS; CELL CULTURE; CELL FUNCTION; CLINICAL PROTOCOL; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; HIGH THROUGHPUT SCREENING; IN VIVO STUDY; INTERMETHOD COMPARISON; MITOCHONDRIAL FUNCTION; MITOCHONDRIAL RESPIRATION; NONHUMAN; PRIORITY JOURNAL; PROCESS OPTIMIZATION; RESPIROMETRY; ANIMAL; BIOCHEMISTRY; CELL RESPIRATION; CYTOLOGY; DEVICES; EQUIPMENT DESIGN; METABOLISM; MITOCHONDRION; OXYGEN CONSUMPTION; PROCEDURES;

ANIMALS; BIOCHEMISTRY; CAENORHABDITIS ELEGANS; CELL RESPIRATION; EQUIPMENT DESIGN; MITOCHONDRIA; OXYGEN CONSUMPTION;

EID: 84988632787     PISSN: 17542189     EISSN: 17502799     Source Type: Journal    
DOI: 10.1038/nprot.2016.106     Document Type: Article

References (73)

1. Perry, C. G. R., Kane, D. A., Lanza, I. R. & Neufer, P. D. Methods for assessing mitochondrial function in diabetes. Diabetes 62, 1041-1053 (2013).
2. Hatefi, Y. The mitochondrial electron transport and oxidative phosphorylation system. Annu. Rev. Biochem. 54, 1015-1069 (1985).
3. Brand, M. D. & Nicholls, D. G. Assessing mitochondrial dysfunction in cells. Biochem. J. 435, 297-312 (2011).
4. Goldenthal, M. J. & Marín-García, J. Mitochondrial signaling pathways: A receiver/integrator organelle. Mol. Cell Biochem. 262, 1-16 (2004).
5. Galluzzi, L., Kepp, O. & Kroemer, G. Mitochondria: master regulators of danger signalling. Nat. Rev. Mol. Cell Biol. 13, 780-788 (2012).
6. Rizzuto, R., De Stefani, D., Raffaello, A. & Mammucari, C. Mitochondria as sensors and regulators of calcium signalling. Nat. Rev. Mol. Cell Biol. 13, 566-578 (2012).
7. Fernyhough, P., Roy Chowdhury, S. K. & Schmidt, R. E. Mitochondrial stress and the pathogenesis of diabetic neuropathy. Expert Rev. Endocrinol. Metab. 5, 39-49 (2010).
8. Ferreira, I. L., Resende, R., Ferreiro, E., Rego, A. C. & Pereira, C. F. Multiple defects in energy metabolism in Alzheimer's disease. Curr. Drug Targets 11, 1193-1206 (2010).
9. Jarrett, S. F., Lewin, A. S. & Boulton, M. E. The importance of mitochondria in age-related and inherited eye disorders. Opthalmic Res. 44, 179-190 (2010).
10. Kawamata, H. & Manfredi, G. Mitochondrial dysfunction and intracellular calcium dysregulation in ALS. Mech. Ageing Dev. 131, 517-526 (2010).
11. Ren, J., Pulakat, L., Whaley-Connell, A. & Sowers, J. R. Mitochondrial biogenesis in the metabolic syndrome and cardiovascular disease. J. Mol. Med. 88, 993-1001 (2010).
12. Rosenstock, T. R., Duarte, A. I. & Rego, A. C. Mitochondrial-associated metabolic changes and neurodegeneration in Huntington's disease-from clinical features to the bench. Curr. Drug Targets 11, 1218-1236 (2010).
13. Vafai, S. B. & Mootha, V. K. Mitochondrial disorders as windows into an ancient organelle. Nature 491, 374-383 (2012).
14. Andreux, P. A., Houtkooper, R. H. & Auwerx, J. Pharmacological approaches to restore mitochondrial function. Nat. Rev. Drug Discov. 12, 465-483 (2013).
15. Andreux, P. A. et al. A method to identify and validate mitochondrial modulators using mammalian cells and the worm C. Elegans. Sci. Rep. 4, 05285 (2014).
16. Felkai, S. et al. CLK-1 controls respiration, behaviour and aging in the nematode Caenorhabditis elegans. EMBO J. 18, 1783-1792 (1999).
17. Kamo, N., Muratsugu, M., Hongoh, R. & Kobatake, Y. Membrane potential of mitochondria measured with an electrode sensitive to tetraphenyl phosphonium and relationship between proton electrochemical potential and phosphorylation potential in steady state. J. Membr. Biol. 49, 105-121 (1979).
18. Drew, B. & Leeuwenburgh, C. Method for measuring ATP production in isolated mitochondria: ATP production in brain and liver mitochondria of Fischer-344 rats with age and caloric restriction. Am. J. Physiol. Regul. Integr. Comp. Physiol. 285, R1259-R1267 (2003).
19. Pan, X. et al. The physiological role of mitochondrial calcium revealed by mice lacking the mitochondrial calcium uniporter. Nat. Cell Biol. 15, 1464-1472 (2013).
20. Chance, B. & Williams, G. R. Respiratory enzymes in oxidative phosphorylation. I. Kinetics of oxygen utilization. J. Biol. Chem. 217, 383-393 (1955).
21. Wu, M. et al. Multiparameter metabolic analysis reveals a close link between attenuated mitochondrial bioenergetics function and enhanced glycolysis dependency in human tumor cells. Am. J. Physiol. Cell Physiol. 292, C125-C136 (2007).
22. Gerencser, A. A. et al. Quantitative microplate-based respirometry with correction for oxygen diffusion. Anal. Chem. 81, 6868-6878 (2009).
23. Will, Y., Hynes, J., Ogurtsov, V. I. & Papkovsky, D. B. Analysis of mitochondrial function using phosphorescent oxygen-sensitive probes. Nat. Protoc. 1, 2563-2572 (2006).
24. Nadanaciva, S. et al. Assessment of drug-induced mitochondrial dysfunction via altered cellular respiration and acidification measured in 96-well platform. J. Bioenerg. Biomembr. 44, 421-437 (2012).
25. Yamamoto, H. et al. NCoR1 is a conserved physiological modulator of muscle mass and oxidative function. Cell 147, 827-839 (2011).
26. Houtkooper, R. H. et al. Mitonuclear protein imbalance as a conserved longevity mechanism. Nature 497, 451-457 (2013).
27. Mouchiroud, L. et al. The NAD+/sirtuin pathway modulates longevity through activation of mitochondrial UPR and FOXO signaling. Cell 154, 430-441 (2013).
28. Luz, A. L. et al. Mitochondrial morphology and fundamental parameters of the mitochondrial respiratory chain are altered in Caenorhabditis elegans strains deficient in mitochondrial dynamics and homeostasis processes. PLoS One 10, e0130940 (2015).
29. Lee, S. S. et al. A systematic RNAi screen identifies a critical role for mitochondria in C. Elegans longevity. Nat. Genet. 33, 40-48 (2002).
30. Fire, A. Z. Gene silencing by double-stranded RNA. Cell Death Differ. 14, 1998-2012 (2007).
31. Grishok, A., Tabara, H. & Mello, C. C. Genetic requirements for inheritance of RNAi in C. Elegans. Science 287, 2494-2497 (2000).
32. Dickinson, D. J., Ward, J. D., Reiner, D. J. & Goldstein, B. Engineering the Caenorhabditis elegans genome using Cas9-triggered homologous recombination. Nat. Methods 10, 1028-1034 (2013).
33. Wadsworth, W. G. & Riddle, D. L. Developmental regulation of energy metabolism in Caenorhabditis elegans. Dev. Biol. 132, 167-173 (1989).
34. Li, J. et al. Proteomics analysis of mitochondria from Caenorhabditis elegans. Proteomics 9, 4539-4554 (2009).
35. Mullaney, B. C. & Ashrafi, K. C. Elegans fat storage and metabolic regulation. Biochim. Biophys. Acta 1791, 474-478 (2009).
36. Dancy, B. M., Sedensky, M. M. & Morgan, P. G. Mitochondrial bioenergetics and disease in Caenorhabditis elegans. Front Biosci. (Landmark Ed.) 20, 198-228 (2015).
37. Hill, B. G., Dranka, B. P., Zou, L., Chatham, J. C. & Darley-Usmar, V. M. Importance of the bioenergetics reserve capacity in response to cardiomyocyte stress induced by 4-hydroxynonenal. Biochem. J. 424, 99-107 (2009).
38. Dranka, B. P. et al. Assessing bioenergetic function in response to oxidative stress by metabolic profiling. Free. Radic. Biol. Med. 51, 1621-1635 (2011).
39. Sansbury, B. E., Jones, S. P., Riggs, D. W., Darley-Usmar, V. M. & Hill, B. G. Bioenergetic function in cardiovascular cells: The importance of the reserve capacity and its biological regulation. Chem. Biol. Interact. 191, 288-295 (2011).
40. Readnower, R. D., Brainard, R. E., Hill, B. G. & Jones, S. P. Standardized bioenergetics profiling of adult mouse cardiomyocytes. Physiol. Genomics 44, 1208-1213 (2012).
41. Wilson, D. F., Vinogradov, S., Lo, L. W. & Huang, L. Oxygen dependent quenching of phosphorescence: A status report. Adv. Exp. Med. Biol. 388, 101-107 (1996).
42. Schulz, T. J. et al. Glucose restriction extends Caenorhabditis elegans life span by inducing mitochondrial respiration and increasing oxidative stress. Cell Metab. 6, 280-293 (2007).
43. Ehrismann, D. et al. Studies on the activity of the hypoxia-inducible-factor hydroxylases using an oxygen consumption assay. Biochem. J. 401, 227-234 (2007).
44. Rand, J. B. & Johnson, C. D. Genetic pharmacology: Interactions between drugs and gene products in Caenorhabditis elegans. Methods Cell Biol. 48, 187-204 (1995).
45. Burns, A. R. et al. A predictive model for drug bioaccumulation and bioactivity in Caenorhabditis elegans. Nat. Chem. Biol. 6, 549-557 (2010).
46. Zheng, S.-Q., Ding, A.-J., Li, G.-P., Wu, G.-S. & Luo, H.-R. Drug absorption efficiency in Caenorhabditis elegans delivered by different methods. PLoS One 8, e56877 (2013).
47. Massie, M. R., Lapoczka, E. M., Boggs, K. D., Stine, K. E. & White, G. E. Exposure to the metabolic inhibitor sodium azide induces stress protein expression and thermotolerance in the nematode Caenorhabditis elegans. Cell Stress Chaperones 8, 1-7 (2003).
48. Lanza, I. R. & Nair, K. S. Functional assessment of isolated mitochondria in vivo. Methods Enzymol. 457, 349-372 (2009).
49. Salabei, J. K., Gibb, A. A. & Hill, B. G. Comprehensive measurement of respiratory activity in permeabilized cells using extracellular flux analysis. Nat. Protoc. 9, 421-438 (2014).
50. Piper, H. M. et al. Development of ischemia-induced damage in defined mitochondrial subpopulations. J. Mol. Cell Cardio. 17, 885-896 (1985).
51. Picard, M. et al. Mitochondrial functional impairment with aging is exaggerated in isolated mitochondria compared to permeabilized myofibers. Aging Cell 9, 1032-1046 (2010).
52. Picard, M. et al. Mitochondrial structure and function are disrupted by standard isolation methods. PLoS One 6, e18317 (2011).
53. Picard, M., Taivassalo, T., Gouspillou, G. & Hepple, R. T. Mitochondria: Isolation, structure and function. J. Physiol. 598, 4413-4421 (2011).
54. Kayser, E. B., Morgan, P. G., Hoppel, C. L. & Sedensky, M. M. Mitochondrial expression and function of GAS-1 in Caenorhabditis elegans. J. Biol. Chem. 276, 20551-20558 (2001).
55. Rivera-Ingraham, G. A., Bickmeyer, U. & Abele, D. The physiological response of the marine platyhelminth Macrostomum ligano to different environmental oxygen concentrations. J. Exp. Biol. 216, 2741-2751 (2013).
56. Steele, S. L., Prykhozhij, S. V. & Berman, J. N. Zebrafish as a model system for mitochondrial biology and diseases. Transl. Res. 163, 79-98 (2014).
57. Gibert, Y., McGee, S. L. & Ward, A. C. Metabolic profile analysis of zebrafish embryos. J. Vis. Exp. 14, e4300 (2013).
58. Hartman, N. et al. Mitochondrial DNA copy number and function decrease with age in the short-lived fish Nothobranchius furzeri. Aging Cell 10, 824-831 (2011).
59. Porta-de-la-Riva, M., Fontrodona, L., Villanueva, A. & Cerón, J. Basic Caenorhabditis elegans methods: Synchronization and observation. J. Vis. Exp. 10, e4019 (2012).
60. Mitchell, D. H., Stiles, J. W., Santelli, J. & Sanadi, D. R. Synchronous growth and aging of Caenorhabditis elegans in the presence of fluorodeoxyuridine. J. Gerontol. 34, 28-36 (1979).
61. Davies, S. K., Leroi, A. M. & Bundy, J. G. Fluorodeoxyuridine affects the identification of metabolic responses to daf-2 status in Caenorhabditis elegans. Mech. Ageing Dev. 133, 46-49 (2012).
62. Rooney, J. P. et al. Effects of 5'-fluoro-2-deoxyuridine on mitochondrial biology in Caenorhabditis elegans. Exp. Gerontol. 56, 69-76 (2014).
63. Gruber, J., Ng, L. F., Poovathingsal, S. K. & Halliwell, B. Deceptively simple but simply deceptive-Caenorhabditis elegans lifespan studies: Consideration for aging and antioxidant effects. FEBS Lett. 583, 3377-3387 (2009).
64. Boyd, W. A. et al. A high-throughput method for assessing chemical toxicity using a Caenorhabditis elegans reproduction assay. Toxicol. Appl. Pharmacol. 245, 153-159 (2010).
65. Zubovych, I. O., Straud, S. & Roth, M. G. Mitochondrial dysfunction confers resistance to multiple drugs in Caenorhabditis elegans. Mol. Biol. Cell 21, 956-969 (2010).
66. Wu, Y. et al. Multilayered genetic and omics dissection of mitochondrial activity in a mouse reference population. Cell 158, 1415-1430 (2014).
67. Weimer, S. et al. D-glucosamine supplementation extends life span of nematodes and ageing mice. Nat. Commun. 5, 3563 (2014).
68. Partridge, F. A., Tearle, A. W., Gravato-Nobre, M. J., Schafer, W. R. & Hodgkin, J. The C. Elegans glycosyltransferase BUS-8 has two distinct and essential roles in epidermal morphogenesis. Dev. Biol. 317, 549-559 (2008).
69. MacVicar, T. D. & Lane, J. D. Impaired OMA1-dependent cleavage of OPA1 and reduced DRP1 fission activity combine to prevent mitophagy in cells that are dependent on oxidative phosphorylation. J. Cell Sci. 127, 2313-2325 (2014).
70. Fraser, A. et al. Functional genomic analysis of C. Elegans chromosome I by systematic RNA interference. Nature 408, 325-330 (2000).
71. Kamath, R. S. et al. Systematic functional analysis of the C. Elegans genome using RNAi. Nature 421, 231-237 (2003).
72. Stiernagle, T. Maintenance of C. Elegans. in WormBook (ed. The C. Elegans Research Community) doi:10. 1895/wormbook. 1. 101. 1 (2006).
73. Dancy, B. M. et al. Glutathione S-transferase mediates an ageing response to mitochondrial dysfunction. Mech. Ageing Dev. 153, 14-21 (2015).