The micro-architecture of mitochondria at active zones: Electron tomography reveals novel anchoring scaffolds and cristae structured for high-rate metabolism

Journal of Neuroscience

Volumn 30, Issue 3, 2010, Pages 1015-1026

  Perkins, Guy A ^a   Tjong, Jonathan ^a   Brown, Joshua M ^a   Poquiz, Patrick H ^a   Scott, Raymond T ^a   Kolson, Douglas R ^a   Ellisman, Mark H ^a,b   Spirou, George A ^c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c WEST VIRGINIA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; BIOTIN; BIOTINYLATED DEXTRAN AMINE; CYCLOOXYGENASE 1; DEXTRAN; DRUG DERIVATIVE; MICROTUBULE ASSOCIATED PROTEIN; VESICULAR GLUTAMATE TRANSPORTER;

ANIMAL TISSUE; ARTICLE; BRAIN MITOCHONDRION; CAT; CELL COMMUNICATION; CELL ORGANELLE; CELL POLARITY; CELL STRUCTURE; CYTOSKELETON; DENSITY; ELECTRON TOMOGRAPHY; METABOLIC CAPACITY; METABOLIC RATE; MITOCHONDRIAL MEMBRANE; NERVE ENDING; NONHUMAN; OUTER MEMBRANE; PRESYNAPTIC MEMBRANE; PRIORITY JOURNAL; REGULATORY MECHANISM; SYNAPSE VESICLE; TOMOGRAPHY; ANIMAL; IMAGE PROCESSING; METABOLISM; METHODOLOGY; MITOCHONDRION; PONS; SYNAPSE; SYNAPTOSOME; ULTRASTRUCTURE;

ANIMALS; BIOTIN; CATS; CYCLOOXYGENASE 1; CYTOSKELETON; DEXTRANS; ELECTRON MICROSCOPE TOMOGRAPHY; IMAGE PROCESSING, COMPUTER-ASSISTED; MICROTUBULE-ASSOCIATED PROTEINS; MITOCHONDRIA; PONS; PRESYNAPTIC TERMINALS; SYNAPSES; SYNAPTIC VESICLES; VESICULAR GLUTAMATE TRANSPORT PROTEINS;

EID: 75749098116     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1517-09.2010     Document Type: Article

References (71)

1. Attwell D, Laughlin SB (2001) An energy budget for signaling in the grey matter of the brain. J Cereb Blood Flow Metab 21:1133-1145.
2. Benfenati F, Valtorta F, Rossi MC, Onofri F, Sihra T, Greengard P (1993) Interactions of synapsin I with phospholipids: possible role in synaptic vesicle clustering and in the maintenance of bilayer structures. J Cell Biol 123:1845-1855.
3. Billups B, Forsythe ID (2002) Presynaptic mitochondrial calcium sequestration influences transmission at mammalian central synapses. J Neurosci 22:5840-5847.
4. Bollmann JH, Sakmann B, Borst JG (2000) Calcium sensitivity of glutamate release in a calyx-type terminal. Science 289:953-957.
5. Brodin L, Bakeeva L, Shupliakov O (1999) Presynaptic mitochondria and the temporal pattern of neurotransmitter release. Philos Trans R Soc Lond B Biol Sci 354:365-372.
6. Cant NB, Morest DK (1979) The bushy cells in the anteroventral cochlear nucleus of the cat. A study with the electron microscope. Neuroscience 4:1925-1945
7. Chang DT, Honick AS, Reynolds IJ (2006) Mitochondrial trafficking to synapses in cultured primary cortical neurons. J Neurosci 26:7035-7045.
8. Denton RM, McCormack JG (1980) The role of calcium in the regulation of mitochondrial metabolism. Biochem Soc Trans 8:266-268.
9. Doussau F, Augustine GJ (2000) The actin cytoskeleton and neurotransmitter release: an overview. Biochimie 82:353-363.
10. Frank J (2006) Electron tomography, Ed. 2. New York: Plenum.
11. Frey TG, Perkins GA, Ellisman MH (2006) Electron tomography of membrane-bound cellular organelles. Annu Rev Biophys Biomol Struct 35:199-224.
12. Gilkerson RW, Selker JM, Capaldi RA (2003) The cristal membrane of mitochondria is the principal site of oxidative phosphorylation. FEBS Lett 546:355-358.
13. Gotow T, Miyaguchi K, Hashimoto PH (1991) Cytoplasmic architecture of the axon terminal: filamentous strands specifically associated with synaptic vesicles. Neuroscience 40:587-598.
14. Gray EG (1963) Electron microscopy of presynaptic organelles of the spinal cord. J Anat 97:101-106.
15. Guo X, Macleod GT, Wellington A, Hu F, Panchumarthi S, Schoenfield M, Marin L, Charlton MP, Atwood HL, Zinsmaier KE (2005) The GTPase dMiro is required for axonal transport of mitochondria to Drosophila synapses. Neuron 47:379-393.
16. Gustafsson JS, Birinyi A, Crum J, Ellisman M, Brodin L, Shupliakov O (2002) Ultrastructural organization of lamprey reticulospinal synapses in three dimensions. J Comp Neurol 450:167-182.
17. He L, Perkins GA, Poblenz AT, Harris JB, Hung M, Ellisman MH, Fox DA (2003) Bcl-xL overexpression blocks bax-mediated mitochondrial contact site formation and apoptosis in rod photoreceptors of lead-exposed mice. Proc Natl Acad Sci U S A 100:1022-1027.
18. Hirokawa N, Sobue K, Kanda K, Harada A, Yorifuji H (1989) The cytoskeletal architecture of the presynaptic terminal and molecular structure of synapsin 1. J Cell Biol 108:111-126.
19. Hoffpauir BK, Pope BA, Spirou GA (2007) Serial sectioning and electron microscopy of large tissue volumes for 3D analysis and reconstruction: a case study of the calyx of Held. Nat Protoc 2:9-22.
20. Hüttemann M, Lee I, Samavati L, Yu H, Doan JW (2007) Regulation of mitochondrial oxidative phosphorylation through cell signaling. Biochim Biophys Acta 1773:1701-1720.
21. Johnson JE Jr, Perkins GA, Giddabasappa A, Chaney S, Xiao W, White AD, Brown JM, Waggoner J, Ellisman MH, Fox DA (2007) Spatiotemporal regulation of ATP and Ca2+ dynamics in vertebrate rod and cone ribbon synapses. Mol Vis 13:887-919.
22. Jonas EA, Buchanan J, Kaczmarek LK (1999) Prolonged activation of mitochondrial conductances during synaptic transmission. Science 286:1347-1350.
23. Joris PX, Smith PH, Yin TC (1994) Enhancement of neural synchronization in the anteroventral cochlear nucleus. II. Responses in the tuning curve tail. J Neurophysiol 71:1037-1051.
24. Ju WK, Liu Q, Kim KY, Crowston JG, Lindsey JD, Agarwal N, Ellisman MH, Perkins GA, Weinreb RN (2007) Elevated hydrostatic pressure triggers mitochondrial fission and decreases cellular ATP in differentiated RGC-5 cells. Invest Ophthalmol Vis Sci 48:2145-2151.
25. Ju WK, Kim KY, Lindsey JD, Angert M, Duong-Polk KX, Scott RT, Kim JJ, Kukhmazov I, Ellisman MH, Perkins GA, Weinreb RN (2008) Intraocular pressure elevation induces mitochondrial fission and triggers OPA1 release in glaucomatous optic nerve. Invest Ophthalmol Vis Sci 49:4903-4911.
26. Kang JS, Tian JH, Pan PY, Zald P, Li C, Deng C, Sheng ZH (2008) Docking of axonal mitochondria by syntaphilin controls their mobility and affects short-term facilitation. Cell 132:137-148.
27. Kimura RS, Bongiorno CL, Iverson NA (1987) Synapses and ephapses in the spiral ganglion. Acta Otolaryngol Suppl 438:1-18.
28. Kremer JR, Mastronarde DN, McIntosh JR (1996) Computer visualization of three-dimensional image data using IMOD. J Struct Biol 116:71-76.
29. Landis DM, Hall AK, Weinstein LA, Reese TS (1988) The organization of cytoplasm at the presynaptic active zone of a central nervous system synapse. Neuron 1:201-209.
30. Lawrence A, Bouwer JC, Perkins G, Ellisman MH (2006) Transform-based backprojection for volume reconstruction of large format electron microscope tilt series. J Struct Biol 154:144-167.
31. Lee JS, Kim MH, Ho WK, Lee SH (2008) Presynaptic release probability and readily releasable pool size are regulated by two independent mechanisms during posttetanic potentiation at the calyx of Held synapse. J Neurosci 28:7945-7953.
32. Lieberman AR, Spacek J (1997) Filamentous contacts: the ultrastructure and three-dimensional organization of specialized non-synaptic interneuronal appositions in thalamic relay nuclei. Cell Tissue Res 288:43-57.
33. Mannella CA, Marko M, Penczek P, Barnard D, Frank J (1994) The internal compartmentation of rat-liver mitochondria: tomographic study using the high-voltage transmission electron microscope. Microsc Res Tech 27:278-283.
34. Mannella CA, Marko M, Buttle K (1997) Reconsidering mitochondrial structure: new views of an old organelle. Trends Biochem Sci 22:37-38.
35. Mannella CA, Pfeiffer DR, Bradshaw PC, Moraru II, Slepchenko B, Loew LM, Hsieh CE, Buttle K, Marko M (2001) Topology of the mitochondrial inner membrane: dynamics and bioenergetic implications. IUBMB Life 52:93-100.
36. Nguyen PV, Marin L, Atwood HL (1997) Synaptic physiology and mitochondrial function in crayfish tonic and phasic motor neurons. J Neurophysiol 78:281-294.
37. Perkins G, Renken C, Martone ME, Young SJ, Ellisman M, Frey T (1997a) Electron tomography of neuronal mitochondria: three-dimensional structure and organization of cristae and membrane contacts. J Struct Biol 119:260-272.
38. Perkins GA, Renken CW, Song JY, Frey TG, Young SJ, Lamont S, Martone ME, Lindsey S, Ellisman MH (1997b) Electron tomography of large, multicomponent biological structures. J Struct Biol 120:219-227.
39. Perkins GA, Song JY, Tarsa L, Deerinck TJ, Ellisman MH, Frey TG (1998) Electron tomography of mitochondria from brown adipocytes reveals crista junctions. J Bioenerg Biomembr 30:431-442.
40. Perkins GA, Renken CW, Frey TG, Ellisman MH (2001) Membrane architecture of mitochondria in neurons of the central nervous system. J Neurosci Res 66:857-865.
41. Perkins GA, Ellisman MH, Fox DA (2003) Three-dimensional analysis of mouse rod and cone mitochondrial cristae architecture: bioenergetic and functional implications. Mol Vis 9:60-73.
42. Peters A, Palay SL, Webster Hd (1991) The fine structure of the nervous system. New York: Oxford UP.
43. 2+-dependent interaction with the synaptobrevin-synaptophysin complex. J Cell Biol 137:1589-1601.
44. Renken C, Siragusa G, Perkins G, Washington L, Nulton J, Salamon P, Frey TG (2002) A thermodynamic model describing the nature of the crista junction; a structural motif in the mitochondrion. J Struct Biol 138:137-144.
45. Rikhy R, Kamat S, Ramagiri S, Sriram V, Krishnan KS (2007) Mutations in dynamin-related protein result in gross changes in mitochondrial morphology and affect synaptic vesicle recycling at the Drosophila neuromuscular junction. Genes Brain Behav 6:42-53.
46. Rowland KC, Irby NK, Spirou GA (2000) Specialized synapse-associated structures within the calyx of Held. J Neurosci 20:9135-9144.
47. Saitoh N, Hori T, Takahashi T (2001) Activation of the epsilon isoform of protein kinase C in the mammalian nerve terminal. Proc Natl Acad Sci U S A 98:14017-14021.
48. Sakaba T, Neher E (2001) Calmodulin mediates rapid recruitment of fast-releasing synaptic vesicles at a calyx-type synapse. Neuron 32:1119-1131.
49. Sakaba T, Neher E (2003) Involvement of actin polymerization in vesicle recruitment at the calyx of Held synapse. J Neurosci 23:837-846.
50. Sätzler K, Söhl LF, Bollmann JH, Borst JG, Frotscher M, Sakmann B, Lübke JH (2002) Three-dimensional reconstruction of a calyx of Held and its postsynaptic principal neuron in the medial nucleus of the trapezoid body. J Neurosci 22:10567-10579.
51. Schneggenburger R, Forsythe ID (2006) The calyx of Held. Cell Tissue Res 326:311-337.
52. Schneggenburger R, Neher E (2000) Intracellular calcium dependence of transmitter release rates at a fast central synapse. Nature 406:889-893.
53. Shepherd GM, Harris KM (1998) Three-dimensional structure and composition of CA3-CA1 axons in rat hippocampal slices: implications for presynaptic connectivity and compartmentalization. J Neurosci 18:8300-8310.
54. Siksou L, Rostaing P, Lechaire JP, Boudier T, Ohtsuka T, Fejtová A, Kao HT, Greengard P, Gundelfinger ED, Triller A, Marty S (2007) Three-dimensional architecture of presynaptic terminal cytomatrix. J Neurosci 27:6868-6877.
55. Sosinsky GE, Crum J, Jones YZ, Lanman J, Smarr B, Terada M, Martone ME, Deerinck TJ, Johnson JE, Ellisman MH (2008) The combination of chemical fixation procedures with high pressure freezing and freeze substitution preserves highly labile tissue ultrastructure for electron tomography applications. J Struct Biol 161:359-371.
56. Spacek J, Harris KM (1998) Three-dimensional organization of cell adhesion junctions at synapses and dendritic spines in area CA1 of the rat hippocampus. J Comp Neurol 393:58-68.
57. Spirou GA, Brownell WE, Zidanic M (1990) Recordings from cat trapezoid body and HRP labeling of globular bushy cell axons. J Neurophysiol 63:1169-1190.
58. Spirou GA, Rowland KC, Berrebi AS (1998) Ultrastructure of neurons and large synaptic terminals in the lateral nucleus of the trapezoid body of the cat. J Comp Neurol 398:257-272.
59. Spirou GA, Chirila FV, von Gersdorff H, Manis PB (2008) Heterogeneous Ca2+ influx along the adult calyx of held: a structural and computational study. Neuroscience 154:171-185.
60. Srinivasan G, Kim JH, von Gersdorff H (2008) The pool of fast releasing vesicles is augmented by myosin light chain kinase inhibition at the calyx of Held synapse. J Neurophysiol 99:1810-1824.
61. Stowers RS, Megeath LJ, Górska-Andrzejak J, Meinertzhagen IA, Schwarz TL (2002) Axonal transport of mitochondria to synapses depends on milton, a novel Drosophila protein. Neuron 36:1063-1077.
62. Tang Y, Zucker RS (1997) Mitochondrial involvement in post-tetanic potentiation of synaptic transmission. Neuron 18:483-491.
63. Thiers FA, Burgess BJ, Nadol JB Jr (2000) Prevalence and ultrastructural morphology of axosomatic synapses on spiral ganglion cells in humans of different ages. Hear Res 150:119-131.
64. Thiers FA, Burgess BJ, Nadol JB Jr (2002) Axodendritic and dendrodendritic synapses within outer spiral bundles in a human. Hear Res 164:97-104.
65. Tolbert LP, Morest DK (1982) The neuronal architecture of the anteroventral cochlear nucleus of the cat in the region of the cochlear nerve root: electron microscopy. Neuroscience 7:3053-3067.
66. Verstreken P, Ly CV, Venken KJ, Koh TW, Zhou Y, Bellen HJ (2005) Synaptic mitochondria are critical for mobilization of reserve pool vesicles at Drosophila neuromuscular junctions. Neuron 47:365-378.
67. Vogel F, Bornhövd C, Neupert W, Reichert AS (2006) Dynamic subcompartmentalization of the mitochondrial inner membrane. J Cell Biol 175:237-247.
68. Wimmer VC, Horstmann H, Groh A, Kuner T (2006) Donut-like topology of synaptic vesicles with a central cluster of mitochondria wrapped into membrane protrusions: a novel structure-function module of the adult calyx of Held. J Neurosci 26:109-116.
69. Wölfel M, Lou X, Schneggenburger R (2007) A mechanism intrinsic to the vesicle fusion machinery determines fast and slow transmitter release at a large CNS synapse. J Neurosci 27:3198-3210.
70. Yamaguchi R, Lartigue L, Perkins G, Scott RT, Dixit A, Kushnareva Y, Kuwana T, Ellisman MH, Newmeyer DD (2008) Opa1-mediated cristae opening is Bax/Bak and BH3 dependent, required for apoptosis, and independent of Bak oligomerization. Mol Cell 31:557-569.
71. Yoshizaki K, Watari H, Radda GK (1990) Role of phosphocreatine in energy transport in skeletal muscle of bullfrog studied by 31P-NMR. Biochim Biophys Acta 1051:144-150.