Endostatin Is a Trans-Synaptic Signal for Homeostatic Synaptic Plasticity

Neuron

Volumn 83, Issue 3, 2014, Pages 616-629

  Wang, Tingting ^a   Hauswirth, Anna G ^a   Tong, Amy ^a   Dickman, Dion K ^a   Davis, Graeme W ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AGENTS INTERACTING WITH TRANSMITTER, HORMONE OR DRUG RECEPTORS; CALCIUM; CALCIUM CHANNEL; COLLAGEN; DROSOPHILA PROTEIN; ENDOSTATIN; MULTIPLEXIN PROTEIN, DROSOPHILA; PROTEOCHONDROITIN SULFATE;

ANIMAL; DROSOPHILA MELANOGASTER; HOMEOSTASIS; HUMAN; METABOLISM; NERVE CELL PLASTICITY; PHYSIOLOGY; SIGNAL TRANSDUCTION; SYNAPSE;

ANIMALS; CALCIUM; CALCIUM CHANNELS; CHONDROITIN SULFATE PROTEOGLYCANS; COLLAGEN; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; ENDOSTATINS; HOMEOSTASIS; HUMANS; NEURONAL PLASTICITY; NEUROTRANSMITTER AGENTS; SIGNAL TRANSDUCTION; SYNAPSES;

EID: 84905575091     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2014.07.003     Document Type: Article

References (44)

1. Ackley B.D., Crew J.R., Elamaa H., Pihlajaniemi T., Kuo C.J., Kramer J.M. The NC1/endostatin domain of Caenorhabditis elegans type XVIII collagen affects cell migration and axon guidance. J. Cell Biol. 2001, 152:1219-1232.
2. Ackley B.D., Kang S.H., Crew J.R., Suh C., Jin Y., Kramer J.M. The basement membrane components nidogen and type XVIII collagen regulate organization of neuromuscular junctions in Caenorhabditis elegans. J. Neurosci. 2003, 23:3577-3587.
3. Burrone J., O'Byrne M., Murthy V.N. Multiple forms of synaptic plasticity triggered by selective suppression of activity in individual neurons. Nature 2002, 420:414-418.
4. Chalfie M. Neurosensory mechanotransduction. Nat. Rev. Mol. Cell Biol. 2009, 10:44-52.
5. Chang J.H., Javier J.A., Chang G.Y., Oliveira H.B., Azar D.T. Functional characterization of neostatins, the MMP-derived, enzymatic cleavage products of type XVIII collagen. FEBS Lett. 2005, 579:3601-3606.
6. Cull-Candy S.G., Miledi R., Trautmann A., Uchitel O.D. On the release of transmitter at normal, myasthenia gravis and myasthenic syndrome affected human end-plates. J. Physiol. 1980, 299:621-638.
7. Davis G.W. Homeostatic signaling and the stabilization of neural function. Neuron 2013, 80:718-728.
8. Dhanabal M., Ramchandran R., Waterman M.J., Lu H., Knebelmann B., Segal M., Sukhatme V.P. Endostatin induces endothelial cell apoptosis. J. Biol. Chem. 1999, 274:11721-11726.
9. Dickman D.K., Davis G.W. The schizophrenia susceptibility gene dysbindin controls synaptic homeostasis. Science 2009, 326:1127-1130.
10. Felbor U., Dreier L., Bryant R.A., Ploegh H.L., Olsen B.R., Mothes W. Secreted cathepsin L generates endostatin from collagen XVIII. EMBO J. 2000, 19:1187-1194.
11. Frank C.A., Kennedy M.J., Goold C.P., Marek K.W., Davis G.W. Mechanisms underlying the rapid induction and sustained expression of synaptic homeostasis. Neuron 2006, 52:663-677.
12. Goold C.P., Davis G.W. The BMP ligand Gbb gates the expression of synaptic homeostasis independent of synaptic growth control. Neuron 2007, 56:109-123.
13. Gottmann K. Transsynaptic modulation of the synaptic vesicle cycle by cell-adhesion molecules. J. Neurosci. Res. 2008, 86:223-232.
14. Hanai J., Gloy J., Karumanchi S.A., Kale S., Tang J., Hu G., Chan B., Ramchandran R., Jha V., Sukhatme V.P., Sokol S. Endostatin is a potential inhibitor of Wnt signaling. J. Cell Biol. 2002, 158:529-539.
15. Harrington A.W., Ginty D.D. Long-distance retrograde neurotrophic factor signalling in neurons. Nat. Rev. Neurosci. 2013, 14:177-187.
16. Heljasvaara R., Nyberg P., Luostarinen J., Parikka M., Heikkilä P., Rehn M., Sorsa T., Salo T., Pihlajaniemi T. Generation of biologically active endostatin fragments from human collagen XVIII by distinct matrix metalloproteases. Exp. Cell Res. 2005, 307:292-304.
17. Iremonger K.J., Wamsteeker Cusulin J.I., Bains J.S. Changing the tune: plasticity and adaptation of retrograde signals. Trends Neurosci. 2013, 36:471-479.
18. Jakawich S.K., Nasser H.B., Strong M.J., McCartney A.J., Perez A.S., Rakesh N., Carruthers C.J., Sutton M.A. Local presynaptic activity gates homeostatic changes in presynaptic function driven by dendritic BDNF synthesis. Neuron 2010, 68:1143-1158.
19. Kawasaki F., Zou B., Xu X., Ordway R.W. Active zone localization of presynaptic calcium channels encoded by the cacophony locus of Drosophila. J. Neurosci. 2004, 24:282-285.
20. Kim S.H., Ryan T.A. CDK5 serves as a major control point in neurotransmitter release. Neuron 2010, 67:797-809.
21. Kim Y.M., Hwang S., Kim Y.M., Pyun B.J., Kim T.Y., Lee S.T., Gho Y.S., Kwon Y.G. Endostatin blocks vascular endothelial growth factor-mediated signaling via direct interaction with KDR/Flk-1. J. Biol. Chem. 2002, 277:27872-27879.
22. Kittel R.J., Wichmann C., Rasse T.M., Fouquet W., Schmidt M., Schmid A., Wagh D.A., Pawlu C., Kellner R.R., Willig K.I., et al. Bruchpilot promotes active zone assembly, Ca2+ channel clustering, and vesicle release. Science 2006, 312:1051-1054.
23. Liu G., Tsien R.W. Properties of synaptic transmission at single hippocampal synaptic boutons. Nature 1995, 375:404-408.
24. Liu J., Schrank B., Waterston R.H. Interaction between a putative mechanosensory membrane channel and a collagen. Science 1996, 273:361-364.
25. Liu K.S., Siebert M., Mertel S., Knoche E., Wegener S., Wichmann C., Matkovic T., Muhammad K., Depner H., Mettke C., et al. RIM-binding protein, a central part of the active zone, is essential for neurotransmitter release. Science 2011, 334:1565-1569.
26. McCabe B.D., Marqués G., Haghighi A.P., Fetter R.D., Crotty M.L., Haerry T.E., Goodman C.S., O'Connor M.B. The BMP homolog Gbb provides a retrograde signal that regulates synaptic growth at the Drosophila neuromuscular junction. Neuron 2003, 39:241-254.
27. Meyer F., Moussian B. Drosophila multiplexin (Dmp) modulates motor axon pathfinding accuracy. Dev. Growth Differ. 2009, 51:483-498.
28. Momota R., Naito I., Ninomiya Y., Ohtsuka A. Drosophila type XV/XVIII collagen, Mp, is involved in Wingless distribution. Matrix Biol. 2011, 30:258-266.
29. 2+ influx achieves homeostatic potentiation of neurotransmitter release. Curr. Biol. 2012, 22:1102-1108.
30. Müller M., Pym E.C., Tong A., Davis G.W. Rab3-GAP controls the progression of synaptic homeostasis at a late stage of vesicle release. Neuron 2011, 69:749-762.
31. Myllyharju J., Kivirikko K.I. Collagens, modifying enzymes and their mutations in humans, flies and worms. Trends Genet. 2004, 20:33-43.
32. O'Reilly M.S., Boehm T., Shing Y., Fukai N., Vasios G., Lane W.S., Flynn E., Birkhead J.R., Olsen B.R., Folkman J. Endostatin: an endogenous inhibitor of angiogenesis and tumor growth. Cell 1997, 88:277-285.
33. Passos-Bueno M.R., Suzuki O.T., Armelin-Correa L.M., Sertié A.L., Errera F.I., Bagatini K., Kok F., Leite K.R. Mutations in collagen 18A1 and their relevance to the human phenotype. An. Acad. Bras. Cienc. 2006, 78:123-131.
34. Peixoto R.T., Kunz P.A., Kwon H., Mabb A.M., Sabatini B.L., Philpot B.D., Ehlers M.D. Transsynaptic signaling by activity-dependent cleavage of neuroligin-1. Neuron 2012, 76:396-409.
35. Petersen S.A., Fetter R.D., Noordermeer J.N., Goodman C.S., DiAntonio A. Genetic analysis of glutamate receptors in Drosophila reveals a retrograde signal regulating presynaptic transmitter release. Neuron 1997, 19:1237-1248.
36. Pielage J., Cheng L., Fetter R.D., Carlton P.M., Sedat J.W., Davis G.W. A presynaptic giant ankyrin stabilizes the NMJ through regulation of presynaptic microtubules and transsynaptic cell adhesion. Neuron 2008, 58:195-209.
37. Plomp J.J., van Kempen G.T., Molenaar P.C. Adaptation of quantal content to decreased postsynaptic sensitivity at single endplates in alpha-bungarotoxin-treated rats. J. Physiol. 1992, 458:487-499.
38. Seppinen L., Pihlajaniemi T. The multiple functions of collagen XVIII in development and disease. Matrix Biol. 2011, 30:83-92.
39. Sertié A.L., Sossi V., Camargo A.A., Zatz M., Brahe C., Passos-Bueno M.R. Collagen XVIII, containing an endogenous inhibitor of angiogenesis and tumor growth, plays a critical role in the maintenance of retinal structure and in neural tube closure (Knobloch syndrome). Hum. Mol. Genet. 2000, 9:2051-2058.
40. Suzuki O.T., Sertié A.L., Der Kaloustian V.M., Kok F., Carpenter M., Murray J., Czeizel A.E., Kliemann S.E., Rosemberg S., Monteiro M., et al. Molecular analysis of collagen XVIII reveals novel mutations, presence of a third isoform, and possible genetic heterogeneity in Knobloch syndrome. Am. J. Hum. Genet. 2002, 71:1320-1329.
41. Wickström S.A., Alitalo K., Keski-Oja J. Endostatin associates with integrin alpha5beta1 and caveolin-1, and activates Src via a tyrosyl phosphatase-dependent pathway in human endothelial cells. Cancer Res. 2002, 62:5580-5589.
42. Yamaguchi N., Anand-Apte B., Lee M., Sasaki T., Fukai N., Shapiro R., Que I., Lowik C., Timpl R., Olsen B.R. Endostatin inhibits VEGF-induced endothelial cell migration and tumor growth independently of zinc binding. EMBO J. 1999, 18:4414-4423.
43. Younger M.A., Müller M., Tong A., Pym E.C., Davis G.W. A presynaptic ENaC channel drives homeostatic plasticity. Neuron 2013, 79:1183-1196.
44. Zhao C., Dreosti E., Lagnado L. Homeostatic synaptic plasticity through changes in presynaptic calcium influx. J. Neurosci. 2011, 31:7492-7496.