Cited by 54Extracellular vesicles in diseaseParkinson's Disease Mechanisms and TreatmentsNeuroinflammation and Neurodegeneration Mechanisms

Small Extracellular Vesicles Secreted by Nigrostriatal Astrocytes Rescue Cell Death and Preserve Mitochondrial Function in Parkinson's Disease

Open access
Leggio, Loredana, L'Episcopo, Francesca, Magrì, Andrea, Ulloa‐Navas, María José, Paternò, Greta, Vivarelli, Silvia, Bastos, Carlos A. P., Tirolo, Cataldo +14 more·2022·Advanced Healthcare Materials

Abstract

Extracellular vesicles (EVs) are emerging as powerful players in cell‐to‐cell communication both in healthy and diseased brain. In Parkinson's disease (PD)—characterized by selective dopaminergic neuron death in ventral midbrain (VMB) and degeneration of their terminals in striatum (STR)—astrocytes exert dual harmful/protective functions, with mechanisms not fully elucidated. Here, this study shows that astrocytes from the VMB‐, STR‐, and VMB/STR‐depleted brains release a population of small EVs in a region‐specific manner. Interestingly, VMB‐astrocytes secreted the highest rate of EVs, which is further exclusively increased in response to CCL3, a chemokine that promotes robust dopaminergic neuroprotection in different PD models. The neuroprotective potential of nigrostriatal astrocyte‐EVs is investigated in differentiated versus undifferentiated SH‐SY5Y cells exposed to oxidative stress and mitochondrial toxicity. EVs from both VMB‐ and STR‐astrocytes counteract H 2 O 2 ‐induced caspase‐3 activation specifically in differentiated cells, with EVs from CCL3‐treated astrocytes showing a higher protective effect. High resolution respirometry further reveals that nigrostriatal astrocyte‐EVs rescue neuronal mitochondrial complex I function impaired by the neurotoxin MPP + . Notably, only EVs from VMB‐astrocyte fully restore ATP production, again specifically in differentiated SH‐SY5Y. These results highlight a regional diversity in the nigrostriatal system for the secretion and activities of astrocyte‐EVs, with neuroprotective implications for PD.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1002/adhm.202201203

Cites

13 of 13 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • The presence of EV markers, mitochondrial, Golgi, and ER components within varicosities indicates potential roles in cellular communication, metabolic stress management, and intercellular signaling under pathological or inflammatory conditions.

    “indicating potential roles in cellular communication, metabolic stress management, and intercellular signaling under pathological or inflammatory conditions, as previously reported for reactive astrocytes (26, 42, 43).”

    From Varicose projection astrocytes: Conserved reactive cells in brain pathology (2026) · cites this paper as [43]

    Split into 2 atoms — 0 confirmed, 2 partially supported, 0 disputed, 0 misattributed, 0 unverifiable. Expand the claim to see per-atom verdicts.

    Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 161

  1. [1]L. A. Mulcahy, R. C. Pink, D. R. F. Carter, J. Extracell. Vesicles 2014, 3, 24641. PMC4122821 25143819
  2. [2]B. L. Deatheragea, B. T. Cooksona, Infect. Immun. 2012, 80, 1948. 22409932 PMC3370574
  3. [3]D. G. Robinson, Y. Ding, L. Jiang, Protoplasma 2016, 253, 31. 26410830
  4. [4]R. Kalluri, V. S. LeBleu, Science 2020, 367, eaau6977. 32029601 PMC7717626
  5. [5]D. K. Jeppesen, A. M. Fenix, J. L. Franklin, J. N. Higginbotham, Q. Zhang, L. J. Zimmerman, D. C. Liebler, J. Ping, Qi Liu, R. Evans, W. H. Fissell, J. G. Patton, L. H. Rome, D. T. Burnette, R. J. Coffey, Cell 2019, 177, 428. 30951670 PMC6664447
  6. [6]C. Théry, K. W. Witwer, E. Aikawa, M. J. Alcaraz, J. D. Anderson, R. Andriantsitohaina, A. Antoniou, T. Arab, F. Archer, G. K. Atkin‐Smith, D. C. Ayre, J.‐M. Bach, D. Bachurski, H. Baharvand, L. Balaj, S. Baldacchino, N. N. Bauer, A. A. Baxter, M. Bebawy, C. Beckham, A. Bedina Zavec, A. Benmoussa, A. C. Berardi, P. Bergese, E. Bielska, C. Blenkiron, S. Bobis‐Wozowicz, E. Boilard, W. Boireau, A. Bongiovanni, et al., J. Extracell. Vesicles 2018, 7, 1535750. 30637094 PMC6322352
  7. [7]K. W. Witwer, D. C. Goberdhan, L. O'Driscoll, C. Théry, J. A. Welsh, C. Blenkiron, E. I. Buzãs, D. Di Vizio, U. Erdbrügger, J. M. Falcón‐Pérez, Q. L. Fu, A. F. Hill, M. Lenassi, J. Lötvall, R. Nieuwland, T. Ochiya, S. Rome, S. Sahoo, L. Zheng, J. Extracell. Vesicles 2021, 10, e12182. 34953156 PMC8710080
  8. [8]N. Iraci, T. Leonardi, F. Gessler, B. Vega, S. Pluchino, Int. J. Mol. Sci. 2016, 17, 171. 26861302 PMC4783905
  9. [9]S. El‐Andaloussi, Y. Lee, S. Lakhal‐Littleton, J. Li, Y. Seow, C. Gardiner, L. Alvarez‐Erviti, I. L. Sargent, M. J. A. Wood, Nat. Protoc. 2012, 7, 2112. 23154783
  10. [10]O. G. de Jong, D. E. Murphy, I. Mäger, E. Willms, A. Garcia‐Guerra, J. J. Gitz‐Francois, J. Lefferts, D. Gupta, S. C. Steenbeek, J. van Rheenen, S. El Andaloussi, R. M. Schiffelers, M. J. A. Wood, P. Vader, Nat. Commun. 2020, 11, 1113. 32111843 PMC7048928
  11. [11]I. K. Herrmann, M. J. A. Wood, G. Fuhrmann, Nat. Nanotechnol. 2021, 16, 748. 34211166
  12. [12]G. van Niel, D. R. F. Carter, A. Clayton, D. W. Lambert, G. Raposo, P. Vader, Nat. Rev. Mol. Cell Biol. 2022, 23, 369. 35260831
  13. [13]L. Leggio, S. Vivarelli, F. L'Episcopo, C. Tirolo, S. Caniglia, N. Testa, B. Marchetti, N. Iraci, Int. J. Mol. Sci. 2017, 18, 2698. 29236052 PMC5751299
  14. [14]M. Shi, C. Liu, T. J. Cook, K. M. Bullock, Y. Zhao, C. Ginghina, Y. Li, P. Aro, R. Dator, C. He, M. J. Hipp, C. P. Zabetian, E. R. Peskind, S.‐C. Hu, J. F. Quinn, D. R. Galasko, W. A. Banks, J. Zhang, Acta Neuropathol. 2014, 128, 639. 24997849 PMC4201967
  15. [15]R. Kojima, D. Bojar, G. Rizzi, G. C. El Hamri, M. D. El‐Baba, P. Saxena, S. Ausländer, K. R. Tan, M. Fussenegger, Nat. Commun. 2018, 9, 1305. 29610454 PMC5880805
  16. [16]A. Fuster‐Matanzo, F. Gessler, T. Leonardi, N. Iraci, S. Pluchino, Stem Cell Res. Ther. 2015, 6, 227. 26631254 PMC4668616
  17. [17]D. Buschmann, V. Mussack, J. B. Byrd, Adv. Drug Delivery Rev. 2021, 174, 348. PMC8217305 33964356
  18. [18]Z. H. Zhao, Z. T. Chen, R. L. Zhou, X. Zhang, Q. Y. Ye, Y. Z. Wang, Front. Aging Neurosci. 2019, 10. PMC6339871 30692923
  19. [19]S. Wang, Z. Liu, T. Ye, O. S. Mabrouk, T. Maltbie, J. Aasly, A. B. West, Acta Neuropathol. Commun. 2017, 5, 86. 29166931 PMC5700679
  20. [20]L. Leggio, G. Arrabito, V. Ferrara, S. Vivarelli, G. Paternò, B. Marchetti, B. Pignataro, N. Iraci, Adv. Healthcare Mater. 2020, 9, 2000731. 32864899
  21. [21]A. Clayton, E. Boilard, E. I. Buzas, L. Cheng, J. M. Falcón‐Perez, C. Gardiner, D. Gustafson, A. Gualerzi, A. Hendrix, A. Hoffman, J. Jones, C. Lässer, C. Lawson, M. Lenassi, I. Nazarenko, L. O'Driscoll, R. Pink, P. R.‐M. Siljander, C. Soekmadji, M. Wauben, J. A. Welsh, K. Witwer, L. Zheng, R. Nieuwland, J. Extracell. Vesicles 2019, 8, 1647027. 31489143 PMC6711123
  22. [22]A. Jarmalavičiute, V. Tunaitis, U. Pivoraite, A. Venalis, A. Pivoriunas, Cytotherapy 2015, 17, 932. 25981557
  23. [23]K. Narbute, V. Piļipenko, J. Pupure, Z. Dzirkale, U. Jonavičė, V. Tunaitis, K. Kriaučiūnaitė, A. Jarmalavičiūtė, B. Jansone, V. Kluša, A. Pivoriūnas, Stem Cells Transl. Med. 2019, 8, 490. 30706999 PMC6477008
  24. [24]M. J. Haney, Y. Zhao, E. B. Harrison, V. Mahajan, S. Ahmed, Z. He, P. Suresh, S. D. Hingtgen, N. L. Klyachko, R. L Mosley, H. E. Gendelman, A. V. Kabanov, E. V. Batrakova, PLoS One 2013, 8, e61852. 23620794 PMC3631190
  25. [25]M. J. Haney, N. L. Klyachko, Y. Zhao, R. Gupta, E. G. Plotnikova, Z. He, T. Patel, A. Piroyan, M. Sokolsky, A. V. Kabanov, E. V. Batrakova, J. Controlled Release 2015, 207, 18. PMC4430381 25836593
  26. [26]G. C. Terstappen, A. H. Meyer, R. D. Bell, W. Zhang, Nat. Rev. Drug Discovery 2021, 20, 362. 33649582
  27. [27]J. Saint‐Pol, F. Gosselet, S. Duban‐Deweer, G. Pottiez, Y. Karamanos, Cells 2020, 9, 851. 32244730 PMC7226770
  28. [28]X. Zhu, M. Badawi, S. Pomeroy, D. S. Sutaria, Z. Xie, A. Baek, J. Jiang, O. A. Elgamal, X. Mo, K. L. Perle, J. Chalmers, T. D. Schmittgen, M. A. Phelps, J. Extracell. Vesicles 2017, 6, 1324730. 28717420 PMC5505007
  29. [29]W.‐C. Wu, J. Tian, D. Xiao, Y.‐X. Guo, Y. Xiao, X.‐Y. Wu, G. Casella, J. Rasouli, Y.‐P. Yan, A. Rostami, L.‐B. Wang, Y. Zhang, X. Li, Nanoscale 2022, 14, 2393. 35088795
  30. [30]Z. Yan, S. Dutta, Z. Liu, X. Yu, N. Mesgarzadeh, F. Ji, G. Bitan, Y. H. Xie, ACS Sens. 2019, 4, 488. 30644736
  31. [31]A. Hoshino, H. S. Kim, L. Bojmar, K. E. Gyan, M. Cioffi, J. Hernandez, C. P. Zambirinis, G. Rodrigues, H. Molina, S. Heissel, M. T. Mark, L. Steiner, A. Benito‐Martin, S. Lucotti, A. Di Giannatale, K. Offer, M. Nakajima, C. Williams, L. Nogués, F. A. P. Vatter, A. Hashimoto, A. E. Davies, D. Freitas, C. M. Kenific, Y. Ararso, W. Buehring, P. Lauritzen, Y. Ogitani, K. Sugiura, N. Takahashi, et al., Cell 2020, 182, 1044. 32795414 PMC7522766
  32. [32]H. Zhang, D. Freitas, H. S. Kim, K. Fabijanic, Z. Li, H. Chen, M. T. Mark, H. Molina, A. B. Martin, L. Bojmar, J. Fang, S. Rampersaud, A. Hoshino, I. Matei, C. M. Kenific, M. Nakajima, A. P. Mutvei, P. Sansone, W. Buehring, H. Wang, J. P. Jimenez, L. Cohen‐Gould, N. Paknejad, M. Brendel, K. Manova‐Todorova, A. Magalhães, J. A. Ferreira, H. Osório, A. M. Silva, A. Massey, et al., Nat. Cell Biol. 2018, 20, 332. 29459780 PMC5931706
  33. [33]M. Durcin, A. Fleury, E. Taillebois, G. Hilairet, Z. Krupova, C. Henry, S. Truchet, M. Trötzmüller, H. Köfeler, G. Mabilleau, O. Hue, R. Andriantsitohaina, P. Martin, S. Le Lay, J. Extracell. Vesicles 2017, 6, 1305677. 28473884 PMC5405565
  34. [34]G. Van Niel, G. D'Angelo, G. Raposo, Nat. Rev. Mol. Cell Biol. 2018, 19, 213. 29339798
  35. [35]M. Sardar Sinha, A. Ansell‐Schultz, L. Civitelli, C. Hildesjö, M. Larsson, L. Lannfelt, M. Ingelsson, M. Hallbeck, Acta Neuropathol. 2018, 136, 41. 29934873 PMC6015111
  36. [36]J. M. Silverman, S. M. Fernando, L. I. Grad, A. F. Hill, B. J. Turner, J. J. Yerbury, N. R. Cashman, Cell. Mol. Neurobiol. 2016, 36, 377. 26908139 PMC11482315
  37. [37]K. M. Danzer, L. R. Kranich, W. P. Ruf, O. Cagsal‐Getkin, A. R. Winslow, L. Zhu, C. R. Vanderburg, P. J. McLean, Mol. Neurodegener. 2012, 7, 42. 22920859 PMC3483256
  38. [38]A. Vogel, R. Upadhya, A. K. Shetty, eBioMedicine 2018, 38, 273. 30472088 PMC6306394
  39. [39]B. Marchetti, L. Leggio, F. L'Episcopo, S. Vivarelli, C. Tirolo, G. Paternò, C. Giachino, S. Caniglia, M. F. Serapide, N. Iraci, J. Clin. Med. 2020, 9, 1941. 32575923 PMC7356371
  40. [40]F. L'Episcopo, C. Tirolo, M. F. Serapide, S. Caniglia, N. Testa, L. Leggio, S. Vivarelli, N. Iraci, S. Pluchino, B. Marchetti, Front. Aging Neurosci. 2018, 10, 12. 29483868 PMC5816064
  41. [41]B. Marchetti, M. P. Abbracchio, Trends Pharmacol. Sci. 2005, 26, 517. 16126283
  42. [42]K. Kuter, Ł. Olech, U. Głowacka, Mol. Neurobiol. 2018, 55, 3049. 28466266 PMC5842510
  43. [43]F. L'Episcopo, C. Tirolo, L. Peruzzotti‐Jametti, M. F. Serapide, N. Testa, S. Caniglia, B. Balzarotti, S. Pluchino, B. Marchetti, Stem Cells 2018, 36, 1179. 29575325
  44. [44]B. Marchetti, C. Tirolo, F. L'Episcopo, S. Caniglia, N. Testa, J. A. Smith, S. Pluchino, M. F. Serapide, Aging Cell 2020, 19, e13101. 32050297 PMC7059166
  45. [45]F. L'Episcopo, C. Tirolo, N. Testa, S. Caniglia, M. C. Morale, B. Marchetti, CNS Neurol. Disord.: Drug Targets 2010, 9, 349. 20438439
  46. [46]P. L. McGeer, E. G. McGeer, Mov. Disord. 2008, 23, 474. 18044695
  47. [47]M. V. Sofroniew, H. V. Vinters, Acta Neuropathol. 2010, 119, 7. 20012068 PMC2799634
  48. [48]H. D. E. Booth, W. D. Hirst, R. Wade‐Martins, Trends Neurosci. 2017, 40, 358. 28527591 PMC5462417
  49. [49]J. E. Burda, M. V. Sofroniew, Neuron 2014, 81, 229. 24462092 PMC3984950
  50. [50]M. Bélanger, P. J. Magistretti, Dialogues Clin. Neurosci. 2009, 11, 281. 19877496 PMC3181926
  51. [51]P. C. Chen, M. R. Vargas, A. K. Pani, R. J. Smeyne, D. A. Johnson, Y. W. Kan, J. A. Johnson, Proc. Natl. Acad. Sci. USA 2009, 106, 2933. 19196989 PMC2650368
  52. [52]E. C. Hirsch, P. Jenner, S. Przedborski, Mov. Disord. 2013, 28, 24. 22927094
  53. [53]C. M. Tanner, S. M. Goldman, Neurol. Clin. 1996, 14, 317. 8827174 PMC7173037
  54. [54]O. Hornykiewicz, Neurology 1998, 51, S2. 9711973
  55. [55]J. T. Bendor, T. P. Logan, R. H. Edwards, Neuron 2013, 79, 1044. 24050397 PMC3866954
  56. [56]A. H. V. Schapira, C. W. Olanow, J. T. Greenamyre, E. Bezard, Lancet 2014, 384, 545. 24954676
  57. [57]J. Jankovic, Mov. Disord. 2019, 34, 41. 30484897
  58. [58]V. S. Van Laar, J. Chen, A. D. Zharikov, Q. Bai, R. Di Maio, A. A. Dukes, T. G. Hastings, S. C. Watkins, J. T. Greenamyre, C. M. St Croix, E. A. Burton, Redox Biol. 2020, 37, 101695. 32905883 PMC7486459
  59. [59]J. Drouin‐Ouellet, F. Cicchetti, Trends Pharmacol. Sci. 2012, 33, 542. 22944460
  60. [60]E. C. Hirsch, S. Vyas, S. Hunot, Parkinsonism Relat. Disord. 2012, 18, S210. 22166438
  61. [61]J. R. Cannon, J. T. Greenamyre, Neurobiol. Dis. 2013, 57, 38. 22776331 PMC3815566
  62. [62]E. C. Hirsch, D. G. Standaert, Mov. Disord. 2021, 36, 16. 32357266
  63. [63]B. Marchetti, P. A. Serra, C. Tirolo, F. L'Episcopo, S. Caniglia, F. Gennuso, N. Testa, E. Miele, S. Desole, N. Barden, M. C. Morale, Brain Res. Rev. 2005, 48, 302. 15850669
  64. [64]A. H. Schapira, Lancet Neurol. 2008, 7, 97. 18093566
  65. [65]M. Szelechowski, A. Bétourné, Y. Monnet, C. A. Ferré, A. Thouard, C. Foret, J. M. Peyrin, S. Hunot, D. Gonzalez‐Dunia, Nat. Commun. 2014, 5, 5181. 25333748
  66. [66]P. P. Michel, E. C. Hirsch, S. Hunot, Neuron 2016, 90, 675. 27196972
  67. [67]S. R. Subramaniam, M. F. Chesselet, Prog. Neurobiol. 2013, 106, 17. 23643800 PMC3742021
  68. [68]J. Blesa, I. Trigo‐Damas, A. Quiroga‐Varela, V. R. Jackson‐Lewis, Front. Neuroanat. 2015, 9. PMC4495335 26217195
  69. [69]S. J. Chinta, C. A. Lieu, M. Demaria, R. M. Laberge, J. Campisi, J. K. Andersen, J. Intern. Med. 2013, 273, 429. 23600398 PMC3633085
  70. [70]J. Blesa, S. Przedborski, Front. Neuroanat. 2014, 8. PMC4266040 25565980
  71. [71]B. Marchetti, P. A. Serra, F. L'Episcopo, C. Tirolo, S. Caniglia, N. Testa, S. Cioni, F. Gennuso, G. Rocchitta, M. S. Desole, M. C. Mazzarino, E. Miele, M. C. Morale, Ann. N. Y. Acad. Sci. 2005, 1057, 296. 16399902
  72. [72]M. C. Morale, P. A. Serra, F. L'Episcopo, C. Tirolo, S. Caniglia, N. Testa, F. Gennuso, G. Giaquinta, G. Rocchitta, M. S. Desole, E. Miele, B. Marchetti, Neuroscience 2006, 138, 869. 16337092
  73. [73]B. Marchetti, Redox Biol. 2020, 36, 101664. 32863224 PMC7395594
  74. [74]E. C. Hirsch, Ann. Neurol. 1992, 32, S88. 1510386
  75. [75]M. C. Morale, P. A. Serra, M. R. Delogu, R. Migheli, G. Rocchitta, C. Tirolo, S. Caniglia, N. Testa, F. L'Episcopo, F. Gennuso, G. M. Scoto, N. Barden, E. Miele, M. Speranza Desole, B. Marchetti, FASEB J. 2004, 18, 164. 14630699
  76. [76]L. Maatouk, C. Yi, M.‐A. Carrillo‐de Sauvage, A.‐C. Compagnion, S. Hunot, P. Ezan, E. C. Hirsch, A. Koulakoff, F. W. Pfrieger, F. Tronche, L. Leybaert, C. Giaume, S. Vyas, Cell Death Differ. 2019, 26, 580. 30006609 PMC6370798
  77. [77]B. E. Clarke, D. M. Taha, G. E. Tyzack, R. Patani, Glia 2021, 69, 20. 32749770
  78. [78]L. Soreq, J. Rose, E. Soreq, J. Hardy, D. Trabzuni, M. R. Cookson, C. Smith, M. Ryten, R. Patani, J. Ule, Cell Rep. 2017, 18, 557. 28076797 PMC5263238
  79. [79]M. Asanuma, N. Okumura‐Torigoe, I. Miyazaki, S. Murakami, Y. Kitamura, T. Sendo, Int. J. Mol. Sci. 2019, 20, 598. 30704073 PMC6387089
  80. [80]L. Morel, M. S. R. Chiang, H. Higashimori, T. Shoneye, L. K. Iyer, J. Yelick, A. Tai, Y. Yang, J. Neurosci. 2017, 37, 8706. 28821665 PMC5588463
  81. [81]M. V. Sofroniew, Trends Immunol. 2020, 41, 758. 32819810 PMC7484257
  82. [82]L. Ben Haim, D. H. Rowitch, Nat. Rev. Neurosci. 2017, 18, 31. 27904142
  83. [83]L. M. De Biase, K. E. Schuebel, Z. H. Fusfeld, K. Jair, I. A. Hawes, R. Cimbro, H.‐Y. Zhang, Q.‐R. Liu, H. Shen, Z.‐X. Xi, D. Goldman, A. Bonci, Neuron 2017, 95, 341. 28689984 PMC5754189
  84. [84]H. Chai, B. Diaz‐Castro, E. Shigetomi, E. Monte, J. C Octeau, X. Yu, W. Cohn, P. S. Rajendran, T. M. Vondriska, J. P. Whitelegge, G. Coppola, B. S. Khakh, Neuron 2017, 95, 531. 28712653 PMC5811312
  85. [85]W. Xin, K. E. Schuebel, K. Jair, R. Cimbro, L. M. De Biase, D. Goldman, A. Bonci, Neuropsychopharmacology 2019, 44, 344. 30054584 PMC6300565
  86. [86]A. V. Molofsk, R. Krenick, E. Ullian, H. H. Tsai, B. Deneen, W. D. Richardson, B. A. Barres, D. H. Rowitch, Genes Dev. 2012, 26, 891. 22549954 PMC3347787
  87. [87]E. W. Kostuk, J. Cai, L. Iacovitti, Glia 2019, 67, 1542. 31025779 PMC6594409
  88. [88]L. E. Clarke, S. A. Liddelow, C. Chakraborty, A. E. Münch, M. Heiman, B. A. Barres, Proc. Natl. Acad. Sci. USA 2018, 115, E1896. 29437957 PMC5828643
  89. [89]M. F. Serapide, F. L'Episcopo, C. Tirolo, N. Testa, S. Caniglia, C. Giachino, B. Marchetti, Front. Aging Neurosci. 2020, 12, 24. 32226376 PMC7081734
  90. [90]I. Miyazaki, M. Asanuma, Cells 2020, 9, 2623. 33297340 PMC7762285
  91. [91]F. Trettel, M. A. Di Castro, C. Limatola, Neuroscience 2020, 439, 230. 31376422
  92. [92]C. Lauro, M. Catalano, F. Trettel, C. Limatola, Ann. N. Y. Acad. Sci. 2015, 1351, 141. 26084002
  93. [93]B. Marchetti, S. Pluchino, Trends Mol. Med. 2013, 19, 144. 23312954 PMC3595301
  94. [94]F. L'Episcopo, C. Tirolo, N. Testa, S. Caniglia, M. C. Morale, C. Cossetti, P. D'Adamo, E. Zardini, L. Andreoni, A. E. C. Ihekwaba, P. A. Serra, D. Franciotta, G. Martino, S. Pluchino, B. Marchetti, Neurobiol. Dis. 2011, 41, 508. 21056667 PMC3558878
  95. [95]F. L'Episcopo, C. Tirolo, N. Testa, S. Caniglia, M. C. Morale, M. Deleidi, M. F. Serapide, S. Pluchino, B. Marchetti, J. Neurosci. 2012, 32, 2062. 22323720 PMC3556384
  96. [96]F. L'Episcopo, C. Tirolo, N. Testa, S. Caniglia, M. C. Morale, M. F. Serapide, S. Pluchino, B. Marchetti, Stem Cells 2014, 32, 2147. 24648001 PMC4106883
  97. [97]C. Cossetti, N. Iraci, T. R. Mercer, T. Leonardi, E. Alpi, D. Drago, C. Alfaro‐Cervello, H. K. Saini, M. P. Davis, J. Schaeffer, B. Vega, M. Stefanini, C. J. Zhao, W. Muller, J. M. Garcia‐Verdugo, S. Mathivanan, A. Bachi, A. J. Enright, J. S. Mattick, S. Pluchino, Mol. Cell 2014, 56, 193. 25242146 PMC4578249
  98. [98]N. Iraci, E. Gaude, T. Leonardi, A. S. H. Costa, C. Cossetti, L. Peruzzotti‐Jametti, J. D. Bernstock, H. K. Saini, M. Gelati, A. L. Vescovi, C. Bastos, N. Faria, L. G. Occhipinti, A. J. Enright, C. Frezza, S. Pluchino, Nat. Chem. Biol. 2017, 13, 951. 28671681 PMC5563455
  99. [99]A. Mueller, P. G. Strange, FEBS Lett. 2004, 570, 126. 15251452
  100. [100]L. Cartier, O. Hartley, M. Dubois‐Dauphin, K.‐H. Krause, Brain Res. Rev. 2005, 48, 16. 15708626
  101. [101]F. L'Episcopo, M. F. Serapide, C. Tirolo, N. Testa, S. Caniglia, M. C. Morale, S. Pluchino, B. Marchetti, Mol. Neurodegener. 2011, 6, 49. 21752258 PMC3162575
  102. [102]F. L'Episcopo, C. Tirolo, N. Testa, S. Caniglia, M. C. Morale, F. Impagnatiello, S. Pluchino, B. Marchetti, J. Neurosci. 2013, 33, 1462. 23345222 PMC3564519
  103. [103]F. L'Episcopo, C. Tirolo, S. Caniglia, N. Testa, M. C. Morale, M. F. Serapide, S. Pluchino, B. Marchetti, J. Mol. Cell Biol. 2014, 6, 13. 24431301 PMC4061726
  104. [104]C. A. Reichel, M. Rehberg, P. Bihari, C. M. Moser, S. Linder, A. Khandoga, F. Krombach, J. Leukocyte Biol. 2008, 83, 864. 18174361
  105. [105]C. A. Reichel, M. Rehberg, M. Lerchenberger, N. Berberich, P. Bihari, A. G. Khandoga, S. Zahler, F. Krombach, Arterioscler., Thromb., Vasc. Biol. 2009, 29, 1787. 19608967
  106. [106]P. Risiglione, L. Leggio, S. A. M. Cubisino, S. Reina, G. Paternò, B. Marchetti, A. Magrì, N. Iraci, A. Messina, Int. J. Mol. Sci. 2020, 21, 7809. 33105548 PMC7659480
  107. [107]F. M. Lopes, R. Schröder, M. L. C. da F. Júnior, A. Zanotto‐Filho, C. B. Müller, A. S. Pires, R. T. Meurer, G. D. Colpo, D. P. Gelain, F. Kapczinski, J. C. Fonseca Moreira, M. da Cruz Fernandes, F. Klamt, Brain Res. 2010, 1337, 85. 20380819
  108. [108]R. A. Ross, J. L. Biedler, Cancer Res. 1985, 45, 1628. 2983884
  109. [109]J. Bahney, C. S. von Bartheld, Anat. Rec. 2018, 301, 697. PMC5845477 29150977
  110. [110]C. S. von Bartheld, J. Bahney, S. Herculano‐Houzel, J. Comp. Neurol. 2016, 524, 3865. 27187682 PMC5063692
  111. [111]A. Baumann, A. Jorge‐Finnigan, K. Jung‐Kc, A. Sauter, I. Horvath, L. A. Morozova‐Roche, A. Martinez, Sci. Rep. 2016, 6, 39488. 28004763 PMC5177901
  112. [112]E. Eitan, E. R. Hutchison, K. Marosi, J. Comotto, M. Mustapic, S. M. Nigam, C. Suire, C. Maharana, G. A. Jicha, D. Liu, V. Machairaki, K. W. Witwer, D. Kapogiannis, M. P. Mattson, NPJ Aging Mech. Dis. 2016, 2, 16019. 27928512 PMC5137253
  113. [113]Z. Liao, H. Liu, L. Ma, J. Lei, B. Tong, G. Li, W. Ke, K. Wang, X. Feng, W. Hua, S. Li, C. Yang, ACS Nano 2021, 15, 14709. 34476937
  114. [114]K. Takov, D. M. Yellon, S. M. Davidson, J. Extracell. Vesicles 2017, 6, 1388731. 29184625 PMC5699187
  115. [115]J. B. Simonsen, J. Extracell. Vesicles 2019, 8, 1582237. 30815239 PMC6383605
  116. [116]D. B. Zorov, M. Juhaszova, S. J. Sollott, Physiol. Rev. 2014, 94, 909. 24987008 PMC4101632
  117. [117]J. W. Langston, J. Parkinson's Dis. 2017, 7, S11. 28282815 PMC5345642
  118. [118]P. Maiti, J. Manna, G. L. Dunbar, P. Maiti, G. L. Dunbar, Transl. Neurodegener. 2017, 6. PMC5655877 29090092
  119. [119]C. Christensen, H. Þorsteinsson, V. H. Maier, K. Æ. Karlsson, Front. Behav. Neurosci. 2020, 14. PMC7775599 33390914
  120. [120]N. Ismail, M. Ismail, M. U. Imam, N. H. Azmi, S. F. Fathy, J. B. Foo, M. F. Abu Bakar, BMC Complementary Altern. Med. 2014, 14, 467. PMC4528700 25475556
  121. [121]H. Guan, H. Yang, M. Yang, D. Yanagisawa, J.‐P. Bellier, M. Mori, S. Takahata, T. Nonaka, S. Zhao, I. Tooyama, Exp. Neurol. 2017, 291, 51. 28163159
  122. [122]C.‐F. Jhuo, S.‐K. Hsieh, C.‐J. Chen, W.‐Y. Chen, J. T. C. Tzen, Nutrients 2020, 12, 3665. 33260513 PMC7759814
  123. [123]W. J. Nicklas, I. Vyas, R. E. Heikkila, Life Sci. 1985, 36, 2503. 2861548
  124. [124]M. S. T. Mapa, V. Q. Le, K. Wimalasena, PLoS One 2018, 13, e0197946. 30138351 PMC6107127
  125. [125]R. R. Fritz, C. W. Abell, N. T. Patel, W. Gessner, A. Brossi, FEBS Lett. 1985, 186, 224. 3874094
  126. [126]T. E. Whittaker, A. Nagelkerke, V. Nele, U. Kauscher, M. M. Stevens, J. Extracell. Vesicles 2020, 9, 1807674. 32944192 PMC7480412
  127. [127]J. K. Sandhu, M. Gardaneh, R. Iwasiow, P. Lanthier, S. Gangaraju, M. Ribecco‐Lutkiewicz, R. Tremblay, K. Kiuchi, M. Sikorska, Neurobiol. Dis. 2009, 33, 405. 19118631
  128. [128]S. A. Liddelow, K. A. Guttenplan, L. E. Clarke, F. C. Bennett, C. J. Bohlen, L. Schirmer, M. L. Bennett, A. E. Münch, W. S. Chung, T. C. Peterson, D. K. Wilton, A. Frouin, B. A. Napier, N. Panicker, M. Kumar, M. S. Buckwalter, D. H. Rowitch, V. L. Dawson, T. M. Dawson, B. Stevens, B. A. Barres, Nature 2017, 541, 481. 28099414 PMC5404890
  129. [129]L. De Boni, A. H. Watson, L. Zaccagnini, A. Wallis, K. Zhelcheska, N. Kim, J. Sanderson, H. Jiang, E. Martin, A. Cantlon, M. Rovere, L. Liu, M. Sylvester, T. Lashley, U. Dettmer, Z. Jaunmuktane, T. Bartels, Acta Neuropathol. 2022, 143, 453. 35141810 PMC8960659
  130. [130]C. Cossetti, J. A. Smith, N. Iraci, T. Leonardi, C. Alfaro‐Cervello, S. Pluchino, Front. Physiol. 2012, 3. PMC3340916 22557978
  131. [131]J. A. Smith, T. Leonardi, B. Huang, N. Iraci, B. Vega, S. Pluchino, Biogerontology 2015, 16, 147. 24973266 PMC4578234
  132. [132]L. Leggio, G. Paternò, S. Vivarelli, G. G. Falzone, C. Giachino, B. Marchetti, N. Iraci, Aging Dis. 2021, 12, 1494. 34527424 PMC8407885
  133. [133]C. Escartin, E. Galea, A. Lakatos, J. P. O'Callaghan, G. C. Petzold, A. Serrano‐Pozo, C. Steinhäuser, A. Volterra, G. Carmignoto, A. Agarwal, N. J. Allen, A. Araque, L. Barbeito, A. Barzilai, D. E. Bergles, G. Bonvento, A. M. Butt, W.‐T. Chen, M. Cohen‐Salmon, C. Cunningham, B. Deneen, B. De Strooper, B. Díaz‐Castro, C. Farina, M. Freeman, V. Gallo, J. E. Goldman, S. A. Goldman, M. Götz, A. Gutiérrez, et al., Nat. Neurosci. 2021, 24, 312. 33589835 PMC8007081
  134. [134]M. A. S. Pavlou, L. Grandbarbe, N. J. Buckley, S. P. Niclou, A. Michelucci, Prog. Neurobiol. 2019, 174, 36. 30599178
  135. [135]G. E. Tyzack, S. Sitnikov, D. Barson, K. L. Adams‐Carr, N. K. Lau, J. C. Kwok, C. Zhao, R. J. M. Franklin, R. T. Karadottir, J. W. Fawcett, A. Lakatos, Nat. Commun. 2014, 5, 4294. 25014177 PMC4104454
  136. [136]M. Sidoryk‐Wegrzynowicz, Y. N. Gerber, M. Ries, M. Sastre, A. M. Tolkovsky, M. G. Spillantini, Acta Neuropathol. Commun. 2017, 5, 89. 29187256 PMC6389177
  137. [137]A. Venturini, M. Passalacqua, S. Pelassa, F. Pastorino, M. Tedesco, K. Cortese, M. C. Gagliani, G. Leo, G. Maura, D. Guidolin, L. F. Agnati, M. Marcoli, C. Cervetto, Front. Pharmacol. 2019, 10. PMC6901013 31849688
  138. [138]R. Pascua‐Maestro, E. González, C. Lillo, M. D. Ganfornina, J. M. Falcón‐Pérez, D. Sanchez, Front. Cell. Neurosci. 2019, 12. PMC6335244 30687015
  139. [139]N. Shakespear, M. Ogura, J. Yamaki, Y. Homma, Neurochem. Res. 2020, 45, 1020. 32016794
  140. [140]A. Datta Chaudhuri, R. M. Dasgheyb, L. R. DeVine, H. Bi, R. N. Cole, N. J. Haughey, Glia 2020, 68, 128. 31469478
  141. [141]K. Guitart, G. Loers, F. Buck, U. Bork, M. Schachner, R. Kleene, Glia 2016, 64, 896. 26992135
  142. [142]L. Leggio, G. Paternò, S. Vivarelli, F. L'Episcopo, C. Tirolo, G. Raciti, F. Pappalardo, C. Giachino, S. Caniglia, M. F. Serapide, B. Marchetti, N. Iraci, Biomolecules 2020, 10, 1327. 32948090 PMC7563168
  143. [143]A. H. V. Schapira, Exp. Neurol. 2010, 224, 331. 20362572
  144. [144]A. H. V. Schapira, J. M. Cooper, D. Dexter, J. B. Clark, P. Jenner, C. D. Marsden, J. Neurochem. 1990, 54, 823. 2154550
  145. [145]A. L. Bulteau, N. P. Mena, F. Auchère, I. Lee, A. Prigent, C. S. Lobsiger, J. M. Camadro, E. C. Hirsch, Free Radic. Biol. Med. 2017, 108, 236. 28365360
  146. [146]R. Morigaki, S. Goto, Brain Sci. 2017, 7, 63. 28590448 PMC5483636
  147. [147]K. Kaur, J. S. Gill, P. K. Bansal, R. Deshmukh, J. Neurol. Sci. 2017, 381, 308. 28991704
  148. [148]S. Saxena, P. Caroni, Neuron 2011, 71, 35. 21745636
  149. [149]J. Creus‐Muncunill, M. E. Ehrlich, Neurotherapeutics 2019, 16, 957. 31529216 PMC6985401
  150. [150]D. Liu, Z. Dong, J. Wang, Y. Tao, X. Sun, X. Yao, Mitochondrion 2020, 54, 122. 32861876
  151. [151]K. Todkar, L. Chikhi, V. Desjardins, F. El‐Mortada, G. Pépin, M. Germain, Nat. Commun. 2021, 12, 1971. 33785738 PMC8009912
  152. [152]A. Picca, F. Guerra, R. Calvani, C. Bucci, M. R. Lo Monaco, A. R. Bentivoglio, H. J. Coelho‐Júnior, F. Landi, R. Bernabei, E. Marzetti, Int. J. Mol. Sci. 2019, 20, 805. 30781825 PMC6412692
  153. [153]A. Picca, F. Guerra, R. Calvani, F. Marini, A. Biancolillo, G. Landi, R. Beli, F. Landi, R. Bernabei, A. Bentivoglio, M. R. Lo Monaco, C. Bucci, E. Marzetti, J. Clin. Med. 2020, 9, 504. 32059608 PMC7074517
  154. [155]M. Zhao, S. Liu, C. Wang, Y. Wang, M. Wan, F. Liu, M. Gong, Y. Yuan, Y. Chen, J. Cheng, Y. Lu, J. Liu, ACS Nano 2021, 15, 1519. 33369392
  155. [156]X. Wang, I. Weidling, S. Koppel, B. Menta, J. P. Ortiz, A. Kalani, H. M. Wilkins, R. H. Swerdlow, Mitochondrion 2020, 55, 100. 32980480 PMC7669644
  156. [157]J. A. Korecka, R. E. van Kesteren, E. Blaas, S. O. Spitzer, J. H. Kamstra, A. B. Smit, D. F. Swaab, J. Verhaagen, K. Bossers, PLoS One 2013, 8, e63862. 23724009 PMC3665836
  157. [158]A. Merlevede, E. M. Legault, V. Drugge, R. A. Barker, J. Drouin‐Ouellet, V. Olariu, Sci. Rep. 2021, 11, 1514. 33452356 PMC7810861
  158. [159]K. Wang, L. Ye, H. Lu, H. Chen, Y. Zhang, Y. Huang, J. C. Zheng, J. Neuroinflammation 2017, 14. PMC5399318 28427419
  159. [160]A. Ertürk, Y. Wang, M. Sheng, J. Neurosci. 2014, 34, 1672. 24478350 PMC6827581
  160. [161]D. Pesta, E. Gnaiger, Methods Mol. Biol. 2012, 810, 25. 22057559
  161. [162]EV‐TRACK Consortium, J. Van Deun, P. Mestdagh, P. Agostinis, Ö. Akay, S. Anand, J. Anckaert, Z. A. Martinez, T. Baetens, E. Beghein, L. Bertier, G. Berx, J. Boere, S. Boukouris, M. Bremer, D. Buschmann, J. B. Byrd, C. Casert, L. Cheng, A. Cmoch, D. Daveloose, E. De Smedt, S. Demirsoy, V. Depoorter, B. Dhondt, T. A. P. Driedonks, A. Dudek, A. Elsharawy, I. Floris, A. D. Foers, et al., Nat. Methods 2017, 14, 228. 28245209

Cited by

Sorted by citations

Authors
Leggio, L., L'Episcopo, F., Magrì, A., Ulloa‐Navas, M. J., Paternò, G., Vivarelli, S., Bastos, C. A. P., Tirolo, C., Testa, N., Caniglia, S., Risiglione, P., Pappalardo, F., Serra, A., García‐Tárraga, P., Faria, N., Powell, J. J., Peruzzotti‐Jametti, L., Pluchino, S., García‐Verdugo, J. M., Messina, A., Marchetti, B., & Iraci, N.
Affiliations
  • University of Catania (IT)
  • Oasi Research Institute‐IRCCS Troina 94018 Italy
  • Laboratory of Compared Neurobiology University of Valencia‐CIBERNED Paterna 46980 Spain
  • University of Cambridge (GB)
  • Luminex B.V. ‘s‐Hertogenbosch 5115 MV The Netherlands
  • Universitat de València (ES)
Corresponding author
  • Marchetti, Bianca
  • Iraci, Nunzio
Venue
Advanced Healthcare Materials
Publisher
Wiley
Published
2022-08-15
Volume
11
Issue
20
Pages
e2201203-e2201203
ISSN
  • 2192-2640 (ISSN-L)
  • 2192-2659
OpenAlex
W4286002205
Cited by
54
References
13
Citations by year
2026: 13 · 2025: 12 · 2024: 15 · 2023: 13 · 2022: 1
FWCI
3.33
Type
journal article
Language
en
Open access
Locations
  • Advanced Healthcare Materials (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
Funders
  • Ministerio de Ciencia, Innovación y Universidades (PCI2018-093062)
  • Ministero della Salute
  • Ministero dell’Istruzione, dell’Università e della Ricerca (linea 1., PONa3_00136, PRIN 2015, AIM1833071)
  • Università di Catania (PONa3_00136, AIM1833071)
  • Fondazione CON IL SUD
  • Medical Research Council (MR/R005699/1)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Extracellular vesicles in disease
  • Health Sciences › Medicine › Neurology › Parkinson's Disease Mechanisms and Treatments
  • Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
Keywords
Parkinson's disease, extracellular vesicles, astrocytes, nigrostriatal pathway, dopaminergic neuron death, neuroprotection, mitochondrial complex I, MPP+ neurotoxicity, oxidative stress, caspase-3 activation, SH-SY5Y cells, ventral midbrain, striatum, ATP production
MeSH terms
Extracellular Vesicles, Adenosine Triphosphate, Astrocytes, Dopamine, Humans, Mitochondria, Neuroblastoma, Neurotoxins, Parkinson Disease, Cell Death, Caspase 3, Dopaminergic Neurons

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review