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Caffeine improves mitochondrial function in PINK1B9-null mutant Drosophila melanogaster

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Abstract

Mitochondrial dysfunction plays a central role in Parkinson’s disease (PD) and can be triggered by xenobiotics and mutations in mitochondrial quality control genes, such as the PINK1 gene. Caffeine has been proposed as a secondary treatment to relieve PD symptoms mainly by its antagonistic effects on adenosine receptors (ARs). Nonetheless, the potential protective effects of caffeine on mitochondrial dysfunction could be a strategy in PD treatment but need further investigation. In this study, we used high-resolution respirometry (HRR) to test caffeine’s effects on mitochondrial dysfunction in PINK1B9-null mutants of Drosophila melanogaster. PINK1 loss-of-function induced mitochondrial dysfunction in PINK1B9-null flies observed by a decrease in O2 flux related to oxidative phosphorylation (OXPHOS) and electron transfer system (ETS), respiratory control ratio (RCR) and ATP synthesis compared to control flies. Caffeine treatment improved OXPHOS and ETS in PINKB9-null mutant flies, increasing the mitochondrial O2 flux compared to untreated PINKB9-null mutant flies. Moreover, caffeine treatment increased O2 flux coupled to ATP synthesis and mitochondrial respiratory control ratio (RCR) in PINK 1B9-null mutant flies. The effects of caffeine on respiratory parameters were abolished by rotenone co-treatment, suggesting that caffeine exerts its beneficial effects mainly by stimulating the mitochondrial complex I (CI). In conclusion, we demonstrate that caffeine may improve mitochondrial function by increasing mitochondrial OXPHOS and ETS respiration in the PD model using PINK1 loss-of-function mutant flies.

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Data Availability

The data that support the findings of this study are available from the corresponding author upon reasonable request.

References

  1. Poewe W, Seppi K, Tanner CM, Halliday GM, Brundin P, Volkmann J, Schrag A-E, Lang AE (2017) Parkinson disease. Nat Reviews Disease Primers 3:17013. https://doi.org/10.1038/nrdp.2017.13

    Article  PubMed  Google Scholar 

  2. Beal MF (1995) Aging, energy, and oxidative stress in neurodegenerative diseases. Ann Neurol 38:357–366. https://doi.org/10.1002/ana.410380304

    Article  CAS  PubMed  Google Scholar 

  3. Goetz CG (2011) The history of Parkinson’s disease: early clinical descriptions and neurological therapies. Cold Spring Harbor Perspectives in Medicine 1:a008862. https://doi.org/10.1101/cshperspect.a008862

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Devine MJ, Plun-Favreau H, Wood NW (2011) Parkinson’s disease and cancer: two wars, one front. Nat Rev Cancer 11:812–823. https://doi.org/10.1038/nrc3150

    Article  CAS  PubMed  Google Scholar 

  5. Anandhan A, Jacome MS, Lei S, Hernandez-Franco P, Pappa A, Panayiotidis MI, Powers R, Franco R (2017) Metabolic dysfunction in Parkinson’s Disease: Bioenergetics, Redox Homeostasis and Central Carbon Metabolism. Brain Res Bull 133:12–30. https://doi.org/10.1016/j.brainresbull.2017.03.009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Hao X-M, Li L-D, Duan C-L, Li Y-J (2017) Neuroprotective effect of α-mangostin on mitochondrial dysfunction and α-synuclein aggregation in rotenone-induced model of Parkinson’s disease in differentiated SH-SY5Y cells. J Asian Nat Prod Res 19:833–845. https://doi.org/10.1080/10286020.2017.1339349

    Article  CAS  PubMed  Google Scholar 

  7. Gautier CA, Kitada T, Shen J (2008) Loss of PINK1 causes mitochondrial functional defects and increased sensitivity to oxidative stress, Proceedings of the National Academy of Sciences, 105 11364–11369. https://doi.org/10.1073/pnas.0802076105

  8. Gonçalves DF, Courtes AA, Hartmann DD, da Rosa PC, Oliveira DM, Soares FAA (2019) Dalla Corte, 6-Hydroxydopamine induces different mitochondrial bioenergetics response in brain regions of rat. Neurotoxicology 70:1–11. https://doi.org/10.1016/j.neuro.2018.10.005

    Article  CAS  PubMed  Google Scholar 

  9. Klein C, Lohmann-Hedrich K (2007) Impact of recent genetic findings in Parkinson’s disease. Curr Opin Neurol 20:453–464. https://doi.org/10.1097/WCO.0b013e3281e6692b

    Article  CAS  PubMed  Google Scholar 

  10. Sai Y, Zou Z, Peng K, Dong Z (2012) The Parkinson’s disease-related genes act in mitochondrial homeostasis. Neurosci Biobehavioral Reviews 36:2034–2043. https://doi.org/10.1016/J.NEUBIOREV.2012.06.007

    Article  CAS  Google Scholar 

  11. Murphy AN (2009) In a flurry of PINK, mitochondrial bioenergetics takes a leading role in Parkinson’s disease. EMBO Mol Med 1:81–84. https://doi.org/10.1002/emmm.200900020

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Costa AC, Loh SHY, Martins LM (2013) Drosophila Trap1 protects against mitochondrial dysfunction in a PINK1/parkin model of Parkinson’s disease. Cell Death Dis 4:e467–e467. https://doi.org/10.1038/cddis.2012.205

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Aryal B, Lee Y (2018) Disease model organism for Parkinson Disease: Drosophila melanogaster. BMB Reports

  14. Pimenta de Castro I, Costa AC, Lam D, Tufi R, Fedele V, Moisoi N, Dinsdale D, Deas E, Loh SHY, Martins LM (2012) Genetic analysis of mitochondrial protein misfolding in Drosophila melanogaster. Cell Death & Differentiation 19:1308–1316. https://doi.org/10.1038/cdd.2012.5

    Article  CAS  Google Scholar 

  15. Creed RB, Goldberg MS (2018) New Developments in genetic rat models of Parkinson’s Disease, Movement Disorders. Official J Mov Disorder Soc 33:717–729. https://doi.org/10.1002/mds.27296

    Article  Google Scholar 

  16. Chen Y, Dorn GW (2013) PINK1-Phosphorylated mitofusin 2 is a parkin receptor for Culling Damaged Mitochondria. Science 340:471–475. https://doi.org/10.1126/science.1231031

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Narendra DP, Jin SM, Tanaka A, Suen D-F, Gautier CA, Shen J, Cookson MR, Youle RJ (2010) PINK1 is selectively stabilized on impaired mitochondria to activate parkin. PLoS Biol 8:e1000298. https://doi.org/10.1371/journal.pbio.1000298

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Ren X, Chen J-F (2020) Caffeine and Parkinson’s Disease: multiple benefits and emerging mechanisms. Front NeuroSci 14. https://doi.org/10.3389/fnins.2020.602697

  19. Postuma RB, Anang J, Pelletier A, Joseph L, Moscovich M, Grimes D, Furtado S, Munhoz RP, Appel-Cresswell S, Moro A, Borys A, Hobson D, Lang AE (2017) Caffeine as symptomatic treatment for Parkinson disease (Café-PD), neurology, 89. 1795–1803. https://doi.org/10.1212/WNL.0000000000004568

  20. Ribeiro JA, Sebastião AM, Caffeine, Adenosine (2010) J Alzheimer’s Disease 20:S3–S15. https://doi.org/10.3233/JAD-2010-1379

    Article  CAS  Google Scholar 

  21. Pinna A, Serra M, Morelli M, Simola N (2018) Role of adenosine A2A receptors in motor control: relevance to Parkinson’s disease and dyskinesia. J Neural Transm 125:1273–1286. https://doi.org/10.1007/s00702-018-1848-6

    Article  CAS  PubMed  Google Scholar 

  22. Vaughan RA, Garcia-Smith R, Bisoffi M, Trujillo KA, Conn CA (2012) Effects of Caffeine on Metabolism and Mitochondria Biogenesis in Rhabdomyosarcoma cells compared with 2,4-Dinitrophenol, Nutrition and metabolic insights. 5:59. https://doi.org/10.4137/NMI.S10233

  23. Gonçalves DF, Tassi CC, Amaral GP, Stefanello ST, Dalla Corte CL, Soares FA, Posser T, Franco, JL, Carvalho NR (2020) Effects of caffeine on brain antioxidant status and mitochondrial respiration in acetaminophen-intoxicated mice. Toxicol Res 9:726–734. https://doi.org/10.1093/toxres/tfaa075

    Article  Google Scholar 

  24. Gonçalves DF, de Carvalho NR, Leite MB, Courtes AA, Hartmann DD, Stefanello ST, da Silva IK, Franco JL, Soares FAA (2018) Dalla Corte, Caffeine and acetaminophen association: Effects on mitochondrial bioenergetics. Life Sci 193:234–241. https://doi.org/10.1016/j.lfs.2017.10.039

    Article  CAS  PubMed  Google Scholar 

  25. Mishra J, Kumar A (2014) Improvement of mitochondrial NAD+/FAD+-linked state-3 respiration by caffeine attenuates quinolinic acid induced motor impairment in rats: implications in Huntington’s disease. Pharmacol Rep 66:1148–1155. https://doi.org/10.1016/j.pharep.2014.07.006

    Article  CAS  PubMed  Google Scholar 

  26. Schepici G, Silvestro S, Bramanti P, Mazzon E (2020) Caffeine: an overview of its Beneficial Effects in experimental models and clinical trials of Parkinson’s Disease. Int J Mol Sci 21:4766. https://doi.org/10.3390/ijms21134766

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Keebaugh ES, Park JH, Su C, Yamada R, Ja WW (2017) Nutrition influences caffeine-mediated sleep loss in drosophila. Sleep 40. https://doi.org/10.1093/sleep/zsx146

  28. Pesta D, Gnaiger E, Respirometry H-R (2012) OXPHOS protocols for human cells and permeabilized fibers from small biopsies of human muscle. 25–58. https://doi.org/10.1007/978-1-61779-382-0_3

  29. Schöpf B, Schäfer G, Weber A, Talasz H, Eder IE, Klocker H, Gnaiger E (2016) Oxidative phosphorylation and mitochondrial function differ between human prostate tissue and cultured cells. FEBS J 283:2181–2196. https://doi.org/10.1111/febs.13733

    Article  CAS  PubMed  Google Scholar 

  30. Rovenko BM, Kubrak OI, Gospodaryov DV, Yurkevych IS, Sanz A, Lushchak OV, Lushchak VI (2015) Restriction of glucose and fructose causes mild oxidative stress independently of mitochondrial activity and reactive oxygen species in drosophila melanogaster, comparative biochemistry and physiology -part A : Molecular and Integrative Physiology. 187:27–39. https://doi.org/10.1016/j.cbpa.2015.04.012

  31. Scialò F, Sriram A, Fernández-Ayala D, Gubina N, Lõhmus M, Nelson G, Logan A, Cooper HM, Navas P, Enríquez JA, Murphy MP, Sanz A (2016) Mitochondrial ROS produced via Reverse Electron Transport Extend Animal Lifespan. Cell Metabol 23:725–734. https://doi.org/10.1016/j.cmet.2016.03.009

    Article  CAS  Google Scholar 

  32. Simard C, Lebel A, Allain EP, Touaibia M, Hebert-Chatelain E, Pichaud N (2020) Metabolic characterization and consequences of mitochondrial pyruvate carrier deficiency in drosophila melanogaster. Metabolites 10:1–16. https://doi.org/10.3390/metabo10090363

    Article  CAS  Google Scholar 

  33. Burtscher J, Zangrandi L, Schwarzer C, Gnaiger E (2015) Differences in mitochondrial function in homogenated samples from healthy and epileptic specific brain tissues revealed by high-resolution respirometry. Mitochondrion 25:104–112. https://doi.org/10.1016/J.MITO.2015.10.007

    Article  CAS  PubMed  Google Scholar 

  34. Cho J, Hur JH, Graniel J, Benzer S, Walker DW (2012) Expression of yeast NDI1 rescues a Drosophila complex I assembly defect. PLoS One 7:e50644. doi: https://doi.org/10.1371/journal.pone.0050644

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Long J, Ma J, Luo C, Mo X, Sun L, Zang W, Liu J (2009) Comparison of two methods for assaying complex I activity in mitochondria isolated from rat liver, brain and heart. Life Sci 85:276–280. doi: https://doi.org/10.1016/j.lfs.2009.05.019

    Article  CAS  PubMed  Google Scholar 

  36. Spinazzi M, Casarin A, Pertegato V et al (2012) Assessment of mitochondrial respiratory chain enzymatic activities on tissues and cultured cells. Nat Protoc 7:1235–1246. https://doi.org/10.1038/nprot.2012.058

    Article  CAS  PubMed  Google Scholar 

  37. Jimenez-Del-Rio M, Guzman-Martinez C, Velez-Pardo C (2010) The Effects of polyphenols on survival and locomotor activity in Drosophila melanogaster exposed to Iron and Paraquat. Neurochem Res 35:227–238. doi:https://doi.org/10.1007/s11064-009-0046-1

    Article  CAS  PubMed  Google Scholar 

  38. Moreira PI, Zhu X, Wang X, Lee H, Nunomura A, Petersen RB, Perry G, Smith MA (2010) Mitochondria: a therapeutic target in neurodegeneration, Biochimica et Biophysica Acta (BBA) - molecular basis of Disease. 1802:212–220. https://doi.org/10.1016/j.bbadis.2009.10.007

  39. Fernández-Moriano C, González-Burgos E, Gómez-Serranillos MP (2015) Mitochondria-Targeted Protective Compounds in Parkinson’s and Alzheimer’s Diseases, Oxidative Medicine and Cellular Longevity, (2015) 1–30. https://doi.org/10.1155/2015/408927

  40. Kolahdouzan M, Hamadeh MJ (2017) The neuroprotective effects of caffeine in neurodegenerative diseases. CNS Neurosci Ther 23:272–290. https://doi.org/10.1111/cns.12684

    Article  PubMed  PubMed Central  Google Scholar 

  41. Costa J, Lunet N, Santos C, Santos J, Vaz-Carneiro A (2010) Caffeine exposure and the risk of Parkinson’s Disease: a systematic review and Meta-analysis of Observational Studiess. J Alzheimer’s Disease 20:S221–S238. https://doi.org/10.3233/JAD-2010-091525

    Article  CAS  Google Scholar 

  42. Nehlig A (2016) Effects of coffee/caffeine on brain health and disease: what should I tell my patients? Pract Neurol 16:89–95. https://doi.org/10.1136/practneurol-2015-001162

    Article  PubMed  Google Scholar 

  43. Prediger RDS (2010) Effects of Caffeine in Parkinson’s Disease: from neuroprotection to the management of motor and non-motor symptoms. J Alzheimer’s Disease 20:S205–S220. doi: https://doi.org/10.3233/JAD-2010-091459

    Article  CAS  Google Scholar 

  44. Morais VA, Verstreken P, Roethig A, Smet J, Snellinx A, Vanbrabant M, Haddad D, Frezza C, Mandemakers W, Vogt-Weisenhorn D, van Coster R, Wurst W, Scorrano L, de Strooper B (2009) Parkinson’s disease mutations in PINK1 result in decreased Complex I activity and deficient synaptic function. EMBO Mol Med 1:99–111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Morais VA, Haddad D, Craessaerts K, de Bock P-J, Swerts J, Vilain S, Aerts L, Overbergh L, Grünewald A, Seibler P, Klein C, Gevaert K, de Verstreken P (2014) Strooper, PINK1 loss-of-function mutations affect mitochondrial complex I activity via NdufA10 Ubiquinone Uncoupling. Science 344:203–207. doi: https://doi.org/10.1126/science.1249161

    Article  CAS  PubMed  Google Scholar 

  46. Pogson JH, Ivatt RM, Sanchez-Martinez A, Tufi R, Wilson E, Mortiboys H, Whitworth AJ (2014) The Complex I subunit NDUFA10 selectively rescues Drosophila pink1 mutants through a mechanism Independent of Mitophagy. PLoS Genet 10:e1004815. https://doi.org/10.1371/journal.pgen.1004815

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. v. Schapira AH, Cooper JM, Dexter D, Clark JB, Jenner P, Marsden CD (1990) Mitochondrial complex I Deficiency in Parkinson’s Disease. J Neurochem 54:823–827. doi: https://doi.org/10.1111/j.1471-4159.1990.tb02325.x

    Article  Google Scholar 

  48. Devi L, Raghavendran V, Prabhu BM, Avadhani NG, Anandatheerthavarada HK (2008) Mitochondrial Import and Accumulation of α-Synuclein impair complex I in human dopaminergic neuronal cultures and Parkinson Disease Brain. J Biol Chem 283:9089–9100. doi: https://doi.org/10.1074/jbc.M710012200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Polito L, Greco A, Seripa D, Profile G (2016) Environmental Exposure, and Their Interaction in Parkinson’s Disease, Parkinson’s Disease, (2016) 1–9. doi: https://doi.org/10.1155/2016/6465793

  50. Connolly S, Kingsbury TJ (2010) Caffeine modulates CREB-dependent gene expression in developing cortical neurons. Biochem Biophys Res Commun 397:152–156

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Camandola S, Mattson MP (2017) Brain metabolism in health, aging, and neurodegeneration. EMBO J 36:1474–1492. doi: https://doi.org/10.15252/embj.201695810

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Dragicevic N, Delic V, Cao C, Copes N, Lin X, Mamcarz M, Wang L, Arendash GW, Bradshaw PC (2012) Caffeine increases mitochondrial function and blocks melatonin signaling to mitochondria in Alzheimer’s mice and cells. Neuropharmacology 63:1368–1379. https://doi.org/10.1016/j.neuropharm.2012.08.018

    Article  CAS  PubMed  Google Scholar 

  53. Alvira D, Yeste-Velasco M, Folch J, Casadesús G, Smith MA, Pallàs M, Camins A (2007) Neuroprotective effects of caffeine against complex I inhibition–induced apoptosis are mediated by inhibition of the Atm/p53/E2F-1 path in cerebellar granule neurons. J Neurosci Res 85:3079–3088. doi: https://doi.org/10.1002/jnr.21427

    Article  CAS  PubMed  Google Scholar 

  54. Portela JL, Bianchini MC, Roos DH, de Ávila DS, Puntel RL (2021) Caffeic acid and caffeine attenuate toxicity associated with malonic or methylmalonic acid exposure in Drosophila melanogaster. Naunyn-Schmiedeberg’s Archives of Pharmacology 394:227–240. https://doi.org/10.1007/s00210-020-01974-3

    Article  CAS  PubMed  Google Scholar 

  55. Freddo N, Soares SM, Fortuna M, Pompermaier A, Varela ACC, Maffi VC, Mozzato MT, de Alcantara Barcellos HH, Koakoski G, Barcellos LJG (2021) Rossato-Grando, Stimulants cocktail: methylphenidate plus caffeine impairs memory and cognition and alters mitochondrial and oxidative status, Progress in Neuro-Psychopharmacology and Biological Psychiatry. 106:110069. https://doi.org/10.1016/j.pnpbp.2020.110069

  56. Muddapu VR, Chakravarthy VS (2021) Influence of energy deficiency on the subcellular processes of Substantia Nigra Pars Compacta cell for understanding parkinsonian neurodegeneration. Sci Rep 11:1754. https://doi.org/10.1038/s41598-021-81185-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Zong WX, Rabinowitz JD, White E, Mitochondria, Cancer (2016) Mol Cell 61:667–676. https://doi.org/10.1016/j.molcel.2016.02.011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Lu J, Tan M, Cai Q (2015) The Warburg effect in tumor progression: mitochondrial oxidative metabolism as an anti-metastasis mechanism. Cancer Lett 356:156–164. https://doi.org/10.1016/j.canlet.2014.04.001

    Article  CAS  PubMed  Google Scholar 

  59. Thomas HE, Zhang Y, Stefely JA, Veiga SR, Thomas G, Kozma SC, Mercer CA (2018) Mitochondrial complex I activity is required for maximal autophagy. Cell Rep 24:2404–2417e8. doi: https://doi.org/10.1016/j.celrep.2018.07.101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Park J, Lee SB, Lee S, Kim Y, Song S, Kim S, Bae E, Kim J, Shong M, Kim JM, Chung J (2006) Mitochondrial dysfunction in Drosophila PINK1 mutants is complemented by parkin. Nature 441:1157–1161. doi: https://doi.org/10.1038/nature04788

    Article  CAS  PubMed  Google Scholar 

  61. Tellone E, Galtieri A, Russo A, Ficarra S (2019) Protective Effects of the Caffeine Against Neurodegenerative Diseases. Curr Med Chem 26:5137–5151. https://doi.org/10.2174/0929867324666171009104040

    Article  CAS  PubMed  Google Scholar 

  62. McLellan TM, Caldwell JA, Lieberman HR (2016) A review of caffeine’s effects on cognitive, physical and occupational performance. Neurosci Biobehavioral Reviews 71:294–312. https://doi.org/10.1016/j.neubiorev.2016.09.001

    Article  CAS  Google Scholar 

  63. Fredholm BB, Yang J, Wang Y (2016) Low, but not high, dose caffeine is a readily available probe for adenosine actions. Mol Aspects Med. https://doi.org/10.1016/j.mam.2016.11.011

    Article  PubMed  Google Scholar 

  64. Wikoff D, Welsh BT, Henderson R, Brorby GP, Britt J, Myers E, Goldberger J, Lieberman HR, O’Brien C, Peck J, Tenenbein M, Weaver C, Harvey S, Urban J, Doepker C (2017) Systematic review of the potential adverse effects of caffeine consumption in healthy adults, pregnant women, adolescents, and children. Food Chem Toxicol 109:585–648. https://doi.org/10.1016/j.fct.2017.04.002

    Article  CAS  PubMed  Google Scholar 

  65. Madeira MH, Boia R, Ambrósio AF, Santiago AR (2017) Having a coffee break: the impact of caffeine consumption on microglia-mediated inflammation in neurodegenerative Diseases. Mediat Inflamm 2017:1–12. https://doi.org/10.1155/2017/4761081

    Article  CAS  Google Scholar 

  66. Muriel P, Arauz J (2010) Coffee and liver diseases. 81:297–305. https://doi.org/10.1016/j.fitote.2009.10.003

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Funding

Financial support for this study was provided by Fundação de Amparo à pesquisa do Estado do RS (FAPERGS), Brazilian National Council of Technological and Scientific Development (CNPq), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Brazilian National Institute for Science and Technology (INCT), “Programa de Apoio a Núcleos Emergentes” (PRONEM) and MCTI/CNPq [grant numbers 472669/2011-7, 475896/2012-2]. Programa de excelência acadêmica (PROEX) process number 88882.182139/2018-01.

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  1. Centro de Ciências Naturais e Exatas, Departamento de Bioquímica e Biologia Molecular, Programa de Pós-graduação em Ciências Biológicas: Bioquímica Toxicológica, Universidade Federal de Santa Maria, Camobi, 97105- 900, Santa Maria, RS, Brazil

    Débora F. Gonçalves, Leahn R. Senger, João V.P. Foletto, Paula Michelotti, Félix A. A. Soares & Cristiane L. Dalla Corte

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  1. Débora F. Gonçalves
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Débora F. Gonçalves and Cristiane L. Dalla Corte contributed to the study’s conception and design. Material preparation, data collection, and analysis were performed by Débora F. Gonçalves, Leahn R. Senger, João V.P. Foletto, Paula Michelotti, Félix A. A. Soares, Cristiane L. Dalla Corte. The first draft of the manuscript was written by Débora F. Gonçalves and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

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Gonçalves, D.F., Senger, L.R., Foletto, J.V. et al. Caffeine improves mitochondrial function in PINK1B9-null mutant Drosophila melanogaster. J Bioenerg Biomembr 55, 1–13 (2023). https://doi.org/10.1007/s10863-022-09952-5

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