Transfer of mitochondria from astrocytes to neurons after stroke

Nature

Volumn 535, Issue 7613, 2016, Pages 551-555

  Hayakawa, Kazuhide ^a   Esposito, Elga ^a   Wang, Xiaohua ^a,b   Terasaki, Yasukazu ^a   Liu, Yi ^a,b   Xing, Changhong ^a   Ji, Xunming ^b   Lo, Eng H ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b CAPITAL MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; CD38 ANTIGEN; CYCLIC ADENOSINE DIPHOSPHATE RIBOSE; SMALL INTERFERING RNA; CALCIUM; CD38 PROTEIN, MOUSE; MEMBRANE PROTEIN;

CELLS AND CELL COMPONENTS; NEUROLOGY; RNA; RODENT; SENSORY SYSTEM; STROKE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN ISCHEMIA; CALCIUM SIGNALING; CELL SIZE; CELL SURVIVAL; CONTROLLED STUDY; ENDOCYTOSIS; FLUORESCENCE ACTIVATED CELL SORTING; GENE SILENCING; IN VIVO STUDY; INTRACELLULAR SIGNALING; MALE; MICROGLIA; MITOCHONDRION; MOUSE; NERVE CELL; NERVE CELL PLASTICITY; NEUROPROTECTION; NONHUMAN; OLIGODENDROGLIA; PERICYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; ANIMAL; C57BL MOUSE; CEREBROVASCULAR ACCIDENT; DEFICIENCY; GENETICS; METABOLISM; PATHOLOGY; PHYSIOLOGICAL STRESS; PROTECTION; SIGNAL TRANSDUCTION;

MUS;

ANIMALS; ANTIGENS, CD38; ASTROCYTES; BRAIN ISCHEMIA; CALCIUM; CELL SURVIVAL; CYCLIC ADP-RIBOSE; MALE; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED C57BL; MITOCHONDRIA; NEURONAL PLASTICITY; NEURONS; PROTECTIVE FACTORS; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL; STROKE;

EID: 84982732315     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature18928     Document Type: Article

References (37)

1. Davis, C. H. et al. Transcellular degradation of axonal mitochondria. Proc. Natl Acad. Sci. USA 111, 9633-9638 (2014).
2. Iadecola, C., Nedergaard, M. Glial regulation of the cerebral microvasculature. Nat. Neurosci. 10, 1369-1376 (2007).
3. Attwell, D. et al. Glial and neuronal control of brain blood flow. Nature 468, 232-243 (2010).
4. Khakh, B. S., Sofroniew, M. V. Diversity of astrocyte functions and phenotypes in neural circuits. Nat. Neurosci. 18, 942-952 (2015).
5. Rosenberg, P. A., Aizenman, E. Hundred-fold increase in neuronal vulnerability to glutamate toxicity in astrocyte-poor cultures of rat cerebral cortex. Neurosci. Lett. 103, 162-168 (1989).
6. Wang, X. F., Cynader, M. S. Pyruvate released by astrocytes protects neurons from copper-catalyzed cysteine neurotoxicity. J. Neurosci. 21, 3322-3331 (2001).
7. Ouyang, Y. B. et al. Astrocyte-enriched miR-29a targets PUMA and reduces neuronal vulnerability to forebrain ischemia. Glia 61, 1784-1794 (2013).
8. Nagai, M. et al. Astrocytes expressing ALS-linked mutated SOD1 release factors selectively toxic to motor neurons. Nat. Neurosci. 10, 615-622 (2007).
9. Haidet-Phillips, A. M. et al. Astrocytes from familial and sporadic ALS patients are toxic to motor neurons. Nat. Biotechnol. 29, 824-828 (2011).
10. Voloboueva, L. A., Suh, S. W., Swanson, R. A., Giffard, R. G. Inhibition of mitochondrial function in astrocytes: implications for neuroprotection. J. Neurochem. 102, 1383-1394 (2007).
11. Anne Stetler, R., Leak, R. K., Gao, Y., Chen, J. The dynamics of the mitochondrial organelle as a potential therapeutic target. J. Cereb. Blood Flow Metab. 33, 22-32 (2013).
12. Falchi, A. M. et al. Astrocytes shed large membrane vesicles that contain mitochondria, lipid droplets and ATP. Histochem. Cell Biol. 139, 221-231 (2013).
13. Islam, M. N. et al. Mitochondrial transfer from bone-marrow-derived stromal cells to pulmonary alveoli protects against acute lung injury. Nat. Med. 18, 759-765 (2012).
14. Aksoy, P., White, T. A., Thompson, M., Chini, E. N. Regulation of intracellular levels of NAD: a novel role for CD38. Biochem. Biophys. Res. Commun. 345, 1386-1392 (2006).
15. Guse, A. H., Lee, H. C. NAADP: a universal Ca2+ trigger. Sci. Signal. 1, re10 (2008).
16. Bruzzone, S. et al. Glutamate-mediated overexpression of CD38 in astrocytes cultured with neurones. J. Neurochem. 89, 264-272 (2004).
17. Levy, A. et al. CD38 facilitates recovery from traumatic brain injury. J. Neurotrauma 26, 1521-1533 (2009).
18. Higashida, H. et al. Social memory, amnesia, and autism: brain oxytocin secretion is regulated by NAD+ metabolites and single nucleotide polymorphisms of CD38. Neurochem. Int. 61, 828-838 (2012).
19. Choe, C. U. et al. CD38 exacerbates focal cytokine production, postischemic inflammation and brain injury after focal cerebral ischemia. PLoS One 6, e19046 (2011).
20. Frühbeis, C. et al. Neurotransmitter-triggered transfer of exosomes mediates oligodendrocyte-neuron communication. PLoS Biol. 11, e1001604 (2013).
21. Bowen, S. et al. The phagocytic capacity of neurones. Eur. J. Neurosci. 25, 2947-2955 (2007).
22. Winkler, E. A., Bell, R. D., Zlokovic, B. V. Central nervous system pericytes in health and disease. Nat. Neurosci. 14, 1398-1405 (2011).
23. Hu, X. et al. Microglial and macrophage polarization-new prospects for brain repair. Nat. Rev. Neurol. 11, 56-64 (2015).
24. Xin, H. et al. Increasing tPA activity in astrocytes induced by multipotent mesenchymal stromal cells facilitate neurite outgrowth after stroke in the mouse. PLoS One 5, e9027 (2010).
25. Hayakawa, K., Pham, L. D., Katusic, Z. S., Arai, K., Lo, E. H. Astrocytic high-mobility group box 1 promotes endothelial progenitor cell-mediated neurovascular remodeling during stroke recovery. Proc. Natl Acad. Sci. USA 109, 7505-7510 (2012).
26. Proia, P. et al. Astrocytes shed extracellular vesicles that contain fibroblast growth factor-2 and vascular endothelial growth factor. Int. J. Mol. Med. 21, 63-67 (2008).
27. Li, Y., Liu, Z., Xin, H., Chopp, M. The role of astrocytes in mediating exogenous cell-based restorative therapy for stroke. Glia 62, 1-16 (2014).
28. Lo, E. H. Degeneration and repair in central nervous system disease. Nat. Med. 16, 1205-1209 (2010).
29. Xing, C., Lo, E. H. Help-me signaling: Non-cell autonomous mechanisms of neuroprotection and neurorecovery. Prog. Neurobiol. http://dx.doi.org/10.1016/j.pneurobio.2016.04.004 (2016).
30. Rah, S. Y., Park, K. H., Han, M. K., Im, M. J., Kim, U. H. Activation of CD38 by interleukin-8 signaling regulates intracellular Ca2+ level and motility of lymphokine-activated killer cells. J. Biol. Chem. 280, 2888-2895 (2005).
31. Graeff, R. M., Walseth, T. F., Fryxell, K., Branton, W. D., Lee, H. C. Enzymatic synthesis and characterizations of cyclic GDP-ribose. A procedure for distinguishing enzymes with ADP-ribosyl cyclase activity. J. Biol. Chem. 269, 30260-30267 (1994).
32. Bi, B. et al. Cortical glial fibrillary acidic protein-positive cells generate neurons after perinatal hypoxic injury. J. Neurosci. 31, 9205-9221 (2011).
33. Cruz, F. C. et al. New technologies for examining the role of neuronal ensembles in drug addiction and fear. Nat. Rev. Neurosci. 14, 743-754 (2013).
34. Vogel, R. et al. Quantitative sizing of nano/microparticles with a tunable elastomeric pore sensor. Anal. Chem. 83, 3499-3506 (2011).
35. Hayakawa, K. et al. Inhibition of reactive astrocytes with fluorocitrate retards neurovascular remodeling and recovery after focal cerebral ischemia in mice. J. Cereb. Blood Flow Metab. 30, 871-882 (2010).
36. Hayakawa, K., Arai, K., Lo, E. H. Role of ERK map kinase and CRM1 in IL-1?-stimulated release of HMGB1 from cortical astrocytes. Glia 58, 1007-1015 (2010).
37. Dehmelt, L., Poplawski, G., Hwang, E., Halpain, S. NeuriteQuant: an open source toolkit for high content screens of neuronal morphogenesis. BMC Neurosci. 12, 100 (2011).