Tissue plasminogen activator regulates Purkinje neuron development and survival

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 26, 2013, Pages

  Li, Jianxue ^a   Yu, Lili ^b   Gu, Xuesong ^a   Ma, Yinghua ^c   Pasqualini, Renata ^d   Arap, Wadih ^d   Snyder, Evan Y ^e   Sidman, Richard L ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c WEILL CORNELL MEDICAL COLLEGE   (United States)

^d UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^e BURNHAM INSTITUTE   (United States)

Author keywords

Plasma membrane integrity; Postnatal development; Spinocerebellar ataxia; Synaptic ultrastructure

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CASPASE 3; CYTOCHROME C OXIDASE; MARCKS PROTEIN; MESSENGER RNA; NEUROTROPHIN; PROTEIN KINASE C GAMMA; TISSUE PLASMINOGEN ACTIVATOR; VOLTAGE DEPENDENT ANION CHANNEL 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CELL DEATH; CELL GROWTH; CELL LOSS; CELL STRUCTURE; CELL SURVIVAL; CEREBELLUM CORTEX; CONTROLLED STUDY; DENDRITIC CELL; ENZYME ACTIVITY; IN VITRO STUDY; IN VIVO STUDY; MICROTUBULE ASSEMBLY; MITOCHONDRIAL MEMBRANE POTENTIAL; MOTOR COORDINATION; MOUSE; NERVE CELL DIFFERENTIATION; NERVE CELL NECROSIS; NERVE FIBER; NONHUMAN; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; PURKINJE CELL; SYNAPTOGENESIS;

PLASMA MEMBRANE INTEGRITY; POSTNATAL DEVELOPMENT; SPINOCEREBELLAR ATAXIA; SYNAPTIC ULTRASTRUCTURE;

ANIMALS; CELL DIFFERENTIATION; CELL SURVIVAL; CEREBELLAR CORTEX; FEMALE; FIBRINOLYSIN; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, NEUROLOGIC MUTANTS; NEUROGENESIS; PURKINJE CELLS; TISSUE PLASMINOGEN ACTIVATOR;

EID: 84879526242     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1305010110     Document Type: Article

References (70)

1. Palay SL, Chan-Palay V (1974) Cerebellar Cortex: Cytology and Organization. (Springer, Berlin).
2. Llinás RR, Walton KD, Lang EJ (2004) The Synaptic Organization of the Brain, ed Shepherd GM (Oxford Univ Press, New York), 5th Ed, pp 271-309.
3. Rossi F, Tempia F (2006) Unravelling the Purkinje neuron. Cerebellum 5(2):75-76.
4. Kapfhammer JP, Gugger OS (2012) The analysis of Purkinje cell dendritic morphology in organotypic slice cultures. J Vis Exp 61(61):e3637.
5. Seidel K, et al. (2012) Brain pathology of spinocerebellar ataxias. Acta Neuropathol 124(1):1-21.
6. Kasumu A, Bezprozvanny I (2012) Deranged calcium signaling in Purkinje cells and pathogenesis in spinocerebellar ataxia 2 (SCA2) and other ataxias. Cerebellum 11(3): 630-639.
7. Fatemi SH, et al. (2012) Consensus paper: Pathological role of the cerebellum in autism. Cerebellum 11(3):777-807.
8. Stȩpie-n T, Wierzba-Bobrowicz T, Lewandowska E, Szpak G (2012) Morphological and quantitative analysis of cerebellar cortical cells in Alzheimer's disease. Folia Neuropathol 50(3):250-260.
9. Sidman RL, GreenMC (1970) "Nervous", a newmutantmouse with cerebellar disease. In Les Mutants Pathologiques Chez L'animal. Leur Interpret pour la Recherche Biomedicale, ed Sabourdy M (Centre National de la Recherche Scientifique, Paris), pp 69-79.
10. Landis SC (1973) Ultrastructural changes in the mitochondria of cerebellar Purkinje cells of nervous mutant mice. J Cell Biol 57(3):782-797.
11. Wassef M, Sotelo C, Cholley B, Brehier A, Thomasset M (1987) Cerebellar mutations affecting the postnatal survival of Purkinje cells in the mouse disclose a longitudinal pattern of differentially sensitive cells. Dev Biol 124(2):379-389.
12. De Jager PL, Harvey D, Polydorides AD, Zuo J, Heintz N (1998) A high-resolution genetic map of the nervous locus on mouse chromosome 8. Genomics 48(3):346-353.
13. Li J, Imitola J, Snyder EY, Sidman RL (2006) Neural stem cells rescue nervous Purkinje neurons by restoring molecular homeostasis of tissue plasminogen activator and downstream targets. J Neurosci 26(30):7839-7848.
14. Li J, et al. (2006) Purkinje neuron degeneration in nervous (nr) mutant mice is mediated by a metabolic pathway involving excess tissue plasminogen activator. Proc Natl Acad Sci USA 103(20):7847-7852.
15. Seeds NW, Williams BL, Bickford PC (1995) Tissue plasminogen activator induction in Purkinje neurons after cerebellar motor learning. Science 270(5244):1992-1994.
16. Friedman GC, Seeds NW (1995) Tissue plasminogen activator mRNA expression in granule neurons coincides with their migration in the developing cerebellum. J Comp Neurol 360(4):658-670.
17. Basham ME, Seeds NW (2001) Plasminogen expression in the neonatal and adult mouse brain. J Neurochem 77(1):318-325.
18. NINDS rt-PA Stroke Study Group (1995) Tissue plasminogen activator for acute ischemic stroke. N Engl J Med 333(24):1581-1587.
19. Dusart I, Flamant F (2012) Profound morphological and functional changes of rodent Purkinje cells between the first and the second postnatal weeks: A metamorphosis? Front Neuroanat 6(11), 10.3389/fnana.2012.00011.
20. He K-L, et al. (2011) Feedback regulation of endothelial cell surface plasmin generation by PKC-dependent phosphorylation of annexin A2. J Biol Chem 286(17): 15428-15439.
21. Barmack NH, Qian Z, Yoshimura J (2000) Regional and cellular distribution of protein kinase C in rat cerebellar Purkinje cells. J Comp Neurol 427(2):235-254.
22. Schrenk K, Kapfhammer JP, Metzger F (2002) Altered dendritic development of cerebellar Purkinje cells in slice cultures from protein kinase C gamma-deficient mice. Neurosci 110(4):675-689.
23. Kapfhammer JP (2004) Cellular and molecular control of dendritic growth and development of cerebellar Purkinje cells. Prog Histochem Cytochem 39(3):131-182.
24. Tabata T, et al. (2000) A reliable method for culture of dissociated mouse cerebellar cells enriched for Purkinje neurons. J Neurosci Methods 104(1):45-53.
25. Sotelo C, Dusart I (2009) Intrinsic versus extrinsic determinants during the development of Purkinje cell dendrites. Neuroscience 162(3):589-600.
26. Chauhan N, Siegel G (1997) Age-dependent organotypic expression of microtubuleassociated proteins (MAP1, MAP2, and MAP5) in rat brain. Neurochem Res 22(6): 713-719.
27. Li J, et al. (2010) Nna1 mediates Purkinje cell dendritic development via lysyl oxidase propeptide and NF-κB signaling. Neuron 68(1):45-60.
28. Chen LJ, Wang YJ, Tseng GF (2010) Compression alters kinase and phosphatase activity and tau and MAP2 phosphorylation transiently while inducing the fast adaptive dendritic remodeling of underlying cortical neurons. J Neurotrauma 27(9): 1657-1669.
29. Mori A, et al. (1991) Site-specific phosphorylation by protein kinase C inhibits assembly-promoting activity of microtubule-associated protein 4. Biochemistry 30(38):9341-9346.
30. Carter AR, Chen C, Schwartz PM, Segal RA (2002) Brain-derived neurotrophic factor modulates cerebellar plasticity and synaptic ultrastructure. J Neurosci 22(4): 1316-1327.
31. Shoshan-Barmatz V, et al. (2010) VDAC, a multi-functional mitochondrial protein regulating cell life and death. Mol Aspects Med 31(3):227-285.
32. Shoshan-Barmatz V, Golan M (2012) Mitochondrial VDAC1: Function in cell life and death and a target for cancer therapy. Curr Med Chem 19(5):714-735.
33. Shoshan-Barmatz V, Ben-Hail D (2012) VDAC, a multi-functional mitochondrial protein as a pharmacological target. Mitochondrion 12(1):24-34.
34. Dusart I, Guenet JL, Sotelo C (2006) Purkinje cell death: Differences between developmental cell death and neurodegenerative death in mutant mice. Cerebellum 5(2):163-173.
35. Gonzalez-Gronow M, Ray R, Wang F, Pizzo SV (2013) The voltage-dependent anion channel (VDAC) binds tissue-type plasminogen activator and promotes activation of plasminogen on the cell surface. J Biol Chem 288(1):498-509.
36. Hiller S, et al. (2008) Solution structure of the integral human membrane protein VDAC-1 in detergent micelles. Science 321(5893):1206-1210.
37. Gonzalez-Gronow M, Kalfa T, Johnson CE, Gawdi G, Pizzo SV (2003) The voltagedependent anion channel is a receptor for plasminogen kringle 5 on human endothelial cells. J Biol Chem 278(29):27312-27318.
38. Mannella CA, Kinnally KW (2008) Reflections on VDAC as a voltage-gated channel and a mitochondrial regulator. J Bioenerg Biomembr 40(3):149-155.
39. ChaabaneW, et al. (2013) Autophagy, apoptosis, mitoptosis and necrosis: Interdependence between those pathways and effects on cancer. Arch Immunol Ther Exp (Warsz) 61(1):43-58.
40. Sashindranath M, et al. (2011) Compartment- and context-specific changes in tissuetype plasminogen activator (tPA) activity following brain injury and pharmacological stimulation. Lab Invest 91(7):1079-1091.
41. Lu W, Tsirka SE (2002) Partial rescue of neural apoptosis in the Lurcher mutant mouse through elimination of tissue plasminogen activator. Development 129(8):2043-2050.
42. Sotelo C, Triller A (1979) Fate of presynaptic afferents to Purkinje cells in the adult nervous mutant mouse: A model to study presynaptic stabilization. Brain Res 175(1): 11-36.
43. Haraguchi S, et al. (2012) Estradiol promotes Purkinje dendritic growth, spinogenesis, and synaptogenesis during neonatal life by inducing the expression of BDNF. Cerebellum 11(2):416-417.
44. Kline DD, Ogier M, Kunze DL, Katz DM (2010) Exogenous brain-derived neurotrophic factor rescues synaptic dysfunction in Mecp2-null mice. J Neurosci 30(15):5303-5310.
45. Furutani K, Okubo Y, Kakizawa S, Iino M (2006) Postsynaptic inositol 1,4,5- trisphosphate signaling maintains presynaptic function of parallel fiber-Purkinje cell synapses via BDNF. Proc Natl Acad Sci USA 103(22):8528-8533.
46. Hisatsune C, et al. (2006) Inositol 1,4,5-trisphosphate receptor type 1 in granule cells, not in Purkinje cells, regulates the dendritic morphology of Purkinje cells through brain-derived neurotrophic factor production. J Neurosci 26(42):10916-10924.
47. Bosman LW, et al. (2006) Requirement of TrkB for synapse elimination in developing cerebellar Purkinje cells. Brain Cell Biol 35(1):87-101.
48. Ng K-S, Leung H-W, Wong PT-H, Low C-M (2012) Cleavage of the NR2B subunit amino terminus of N-methyl-D-aspartate (NMDA) receptor by tissue plasminogen activator: Identification of the cleavage site and characterization of ifenprodil and glycine affinities on truncated NMDA receptor. J Biol Chem 287(30):25520-25529.
49. Samson AL, Medcalf RL (2006) Tissue-type plasminogen activator: A multifaceted modulator of neurotransmission and synaptic plasticity. Neuron 50(5):673-678.
50. Goldowitz D, Hamre KM (1998) The cells and molecules that make a cerebellum. Trends Neurosci 21(9):375-382.
51. Sajan SA, Waimey KE, Millen KJ (2010) Novel approaches to studying the genetic basis of cerebellar development. Cerebellum 9(3):272-283.
52. Sidman RL, Lane PW, Dickie MM (1962) Staggerer, a new mutation in the mouse affecting the cerebellum. Science 137(3530):610-612.
53. Hamilton BA, et al. (1996) Disruption of the nuclear hormone receptor RORalpha in staggerer mice. Nature 379(6567):736-739.
54. Berrebi AS, Mugnaini E (1988) Effects of the murine mutation 'nervous' on neurons in cerebellum and dorsal cochlear nucleus. J Neurocytol 17(4):465-484.
55. Vander Heiden MG, Chandel NS, Williamson EK, Schumacker PT, Thompson CB (1997) Bcl-xL regulates the membrane potential and volume homeostasis of mitochondria. Cell 91(5):627-637.
56. Vander Heiden MG, et al. (2000) Outer mitochondrial membrane permeability can regulate coupled respiration and cell survival. Proc Natl Acad Sci USA 97(9): 4666-4671.
57. Skulachev VP (2006) Bioenergetic aspects of apoptosis, necrosis and mitoptosis. Apoptosis 11(4):473-485.
58. Jangamreddy JR, Los MJ (2012) Mitoptosis, a novel mitochondrial death mechanism leading predominantly to activation of autophagy. Hepat Mon 12(8):e6159.
59. Weerasinghe P, Buja LM (2012) Oncosis: An important non-apoptotic mode of cell death. Exp Mol Pathol 93(3):302-308.
60. Galluzzi L, et al. (2009) Guidelines for the use and interpretation of assays for monitoring cell death in higher eukaryotes. Cell Death Differ 16(8):1093-1107.
61. Banerjee J, Ghosh S (2004) Interaction of mitochondrial voltage-dependent anion channel from rat brain with plasminogen protein leads to partial closure of the channel. Biochim Biophys Acta 1663(1-2):6-8.
62. Anflous K, Armstrong DD, Craigen WJ (2001) Altered mitochondrial sensitivity for ADP and maintenance of creatine-stimulated respiration in oxidative striated muscles from VDAC1-deficient mice. J Biol Chem 276(3):1954-1960.
63. Sampson MJ, et al. (2001) Immotile sperm and infertility in mice lacking mitochondrial voltage-dependent anion channel type 3. J Biol Chem 276(42):39206-39212.
64. Zuo J, et al. (1997) Neurodegeneration in Lurcher mice caused by mutation in delta2 glutamate receptor gene. Nature 388(6644):769-773.
65. Patil N, et al. (1995) A potassium channel mutation in weaver mice implicates membrane excitability in granule cell differentiation. Nat Genet 11(2):126-129.
66. Murtomäki S, Trenkner E, Wright JM, Saksela O, Liesi P (1995) Increased proteolytic activity of the granule neurons may contribute to neuronal death in the weaver mouse cerebellum. Dev Biol 168(2):635-648.
67. Bennett V (1992) Ankyrins. Adaptors between diverse plasma membrane proteins and the cytoplasm. J Biol Chem 267(13):8703-8706.
68. Peters LL, et al. (1991) Purkinje cell degeneration associated with erythroid ankyrin deficiency in nb/nb mice. J Cell Biol 114(6):1233-1241.
69. Jia Y, Mu JC, Ackerman SL (2012) Mutation of a U2 snRNA gene causes global disruption of alternative splicing and neurodegeneration. Cell 148(1-2):296-308.
70. Li J, Pelletier MR, Perez Velazquez JL, Carlen PL (2002) Reduced cortical synaptic plasticity and GluR1 expression associated with fragile X mental retardation protein deficiency. Mol Cell Neurosci 19(2):138-151.