Neurofibromatosis-1 heterozygosity impairs CNS neuronal morphology in a cAMP/PKA/ROCK-dependent manner

Molecular and Cellular Neuroscience

Volumn 49, Issue 1, 2012, Pages 13-22

  Brown, Jacquelyn A ^a   Diggs Andrews, Kelly A ^a   Gianino, Scott M ^a   Gutmann, David H ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Brain neurons; Cyclic AMP; Neurite extension; Neurofibromin; Rho

Indexed keywords

CYCLIC AMP; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MYOSIN LIGHT CHAIN; NEUROFIBROMIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; CELL STRUCTURE; CENTRAL NERVOUS SYSTEM; GENE EXPRESSION; HETEROZYGOSITY; IN VITRO STUDY; IN VIVO STUDY; MORPHOLOGY; MOUSE; NEURITE; NEUROFIBROMATOSIS; NONHUMAN; PERIPHERAL NERVOUS SYSTEM; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION;

ANIMALS; CELLS, CULTURED; CENTRAL NERVOUS SYSTEM; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; GENES, NEUROFIBROMATOSIS 1; GROWTH CONES; HETEROZYGOTE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEURITES; NEUROFIBROMATOSIS 1; NEUROFIBROMIN 1; NEURONS; RHO-ASSOCIATED KINASES; SIGNAL TRANSDUCTION;

MUS;

EID: 84155163268     PISSN: 10447431     EISSN: 10959327     Source Type: Journal    
DOI: 10.1016/j.mcn.2011.08.008     Document Type: Article

References (66)

1. Abel T., Nguyen P.V., Barad M., Deuel T.A., Kandel E.R., Bourtchouladze R. Genetic demonstration of a role for PKA in the late phase of LTP and in hippocampus-based long-term memory. Cell 1997, 7:615-626.
2. Aizawa H., Wakatsuki S., Ishii A., Moriyama K., Sasaki Y., Ohashi K., Sekine-Aizawa Y., Sehara-Fujisawa A., Mizuno K., Goshima Y., Yahara I. Phosphorylation of cofilin by LIM-kinase is necessary for semaphorin 3A-induced growth cone collapse. Nat. Neurosci. 2001, 4:367-373.
3. Amano M., Chihara K., Nakamura N., Fukata Y., Yano T., Shibata M., Ikebe M., Kaibuchi K. Myosin II activation promotes neurite retraction during the action of Rho and Rho-kinase. Genes Cells 1998, 3:177-188.
4. Banerjee S., Byrd J.N., Gianino S.M., Harpstrite S.E., Rodriguez F.J., Tuskan R.G., Reilly K.M., Piwnica-Worms D.R., Gutmann D.H. The neurofibromatosis type 1 tumor suppressor controls cell growth by regulating signal transducer and activator of transcription-3 activity in vitro and in vivo. Cancer Res. 2010, 70:1356-1366.
5. Bridgman P.C., Dave S., Asnes C.F., Tullio A.N., Adelstein R.S. Myosin IIB is required for growth cone motility. J. Neurosci. 2001, 21:6159-6169.
6. Brown J.A., Bridgman P.C. Disruption of the cytoskeleton during Semaphorin 3A induced growth cone collapse correlates with differences in actin organization and associated binding proteins. Dev. Neurobiol. 2009, 69:633-646.
7. Brown J.A., Emnett R.J., White C.R., Yuede C.M., Conyers S.B., O'Malley K.L., Wozniak D.F., Gutmann D.H. Reduced striatal dopamine underlies the attention system dysfunction in neurofibromatosis-1 mutant mice. Hum. Mol. Genet. 2010, 19:4515-4528.
8. Brown J.A., Gianino S.M., Gutmann D.H. Defective cAMP generation underlies the sensitivity of CNS neurons to neurofibromatosis-1 heterozygosity. J. Neurosci. 2010, 30:5579-5589.
9. Brown J.A., Wysolmerski R.B., Bridgman P.C. Dorsal root ganglion neurons react to semaphorin 3A application through a biphasic response that requires multiple myosin II isoforms. Mol. Biol. Cell 2009, 20:1167-1179.
10. Clarris H.J., Nurcombe V., Small D.H., Beyreuther K., Master C.L. Secretion of nerve growth factor from septum stimulates neurite outgrowth and release of the amyloid protein precursor of Alzheimer's disease from hippocampal explants. J. Neurosci. Res. 1994, 38:248-258.
11. Costa R.M., Federov N.B., Kogan J.H., Murphy G.G., Stern J., Ohno M., Kucherlapati R., Jacks T., Silva A.J. Mechanism for the learning deficits in a mouse model of neurofibromatosis type 1. Nature 2002, 415:526-530.
12. Cui Y., Costa R.M., Murphy G.G., Elgersma Y., Zhu Y., Gutmann D.H., Parada L.F., Mody I., Silva A.J. Neurofibromin regulation of ERK signaling modulates GABA release and learning. Cell 2008, 135:549-560.
13. Dasgupta B., Dugan L.L., Gutmann D.H. The neurofibromatosis 1 gene product neurofibromin regulates pituitary adenylate cyclase-activating polypeptide-mediated signaling in astrocytes. J. Neurosci. 2003, 23:8948-8954.
14. Dasgupta B., Gutmann D.H. Neurofibromin regulates neural stem cell proliferation, survival, and astroglial differentiation in vitro and in vivo. J. Neurosci. 2005, 25:5584-5594.
15. Eliason M.J. Neurofibromatosis: implications for learning and behavior. J. Dev. Behav. Pediatr. 1986, 7:175-179.
16. Gelinas J.N., Banko J.L., Peters M.M., Klann E., Weeber E.J., Nguyen P.V. Activation of exchange protein activated by cyclic-AMP enhances long-lasting synaptic potentiation in the hippocampus. Learn. Mem. 2008, 15:403-411.
17. Gong B., Vitolo O.V., Trinchese F., Liu S., Shelanski M., Arancio O. Persistent improvement in synaptic and cognitive functions in an Alzheimer mouse model after rolipram treatment. J. Clin. Invest. 2004, 114:1624-1634.
18. Hannan F., Ho I., Tong J.J., Zhu Y., Nurnberg P., Zhong Y. Effect of neurofibromatosis type I mutations on a novel pathway for adenylyl cyclase activation requiring neurofibromin and Ras. Hum. Mol. Genet. 2006, 15:1087-1098.
19. Hansen M.J., Dallal G.E., Flanagan J.G. Retinal axon response to ephrin-as shows a graded, concentration-dependent transition from growth promotion to inhibition. Neuron 2004, 42:717-730.
20. Hatakeyama M., Yumoto N., Yu X., Shirouzu M., Yokoyama S., Konagaya A. Transformation potency of ErbB heterodimer signaling is determined by B-Raf kinase. Oncogene 2004, 23:5023-5031.
21. Hegedus B., Dasgupta B., Shin J.E., Emnett R.J., Hart-Mahon E.K., Elghazi L., Bernal-Mizrachi E., Gutmann D.H. Neurofibromatosis-1 regulates neuronal and glial cell differentiation from neuroglial progenitors in vivo by both cAMP- and Ras-dependent mechanisms. Cell Stem Cell 2007, 1:443-457.
22. Hegedus B., Yeh T.H., Lee da Y., Emnett R.J., Li J., Gutmann D.H. Neurofibromin regulates somatic growth through the hypothalamic-pituitary axis. Hum. Mol. Genet. 2008, 17:2956-2966.
23. Ho I.S., Hannan F., Guo H.F., Hakker I., Zhong Y. Distinct functional domains of neurofibromatosis type 1 regulate immediate versus long-term memory formation. J. Neurosci. 2007, 27:6852-6857.
24. Hyman S.L., Arthur Shores E., North K.N. Learning disabilities in children with neurofibromatosis type 1: subtypes, cognitive profile, and attention-deficit-hyperactivity disorder. Dev. Med. Child Neurol. 2006, 48:973-977.
25. Johannessen C.M., Reczek E.E., James M.F., Brems H., Legius E., Cichowski K. The NF1 tumor suppressor critically regulates TSC2 and mTOR. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:8573-8578.
26. Johansson G., Mahller Y.Y., Collins M.H., Kim M.O., Nobukuni T., Perentesis J., Cripe T.P., Lane H.A., Kozma S.C., Thomas G., Ratner N. Effective in vivo targeting of the mammalian target of rapamycin pathway in malignant peripheral nerve sheath tumors. Mol. Cancer Ther. 2008, 7:1237-1245.
27. Kang G., Chepurny O.G., Malester B., Rindler M.J., Rehmann H., Bos J.L., Schwede F., Coetzee W.A., Holz G.G. cAMP sensor Epac as a determinant of ATP-sensitive potassium channel activity in human pancreatic beta cells and rat INS-1 cells. J. Physiol. 2006, 573:595-609.
28. Klesse L.J., Parada L.F. p21 ras and phosphatidylinositol-3 kinase are required for survival of wild-type and NF1 mutant sensory neurons. J. Neurosci. 1998, 18:10420-10428.
29. Kloss S., Srivastava R., Mulsch A. Down-regulation of soluble guanylyl cyclase expression by cyclic AMP is mediated by mRNA-stabilizing protein HuR. Mol. Pharmacol. 2004, 65:1440-1451.
30. Kroeber S., Meissl H., Maronde E., Korf H.W. Analyses of signal transduction cascades reveal an essential role of calcium ions for regulation of melatonin biosynthesis in the light-sensitive pineal organ of the rainbow trout (Oncorhynchus mykiss). J. Neurochem. 2000, 74:2478-2489.
31. Lankford K., Cypher C., Letourneau P. Nerve growth cone motility. Curr. Opin. Cell Biol. 1990, 2:80-85.
32. Lauchle J.O., Kim D., Le D.T., Akagi K., Crone M., Krisman K., Warner K., Bonifas J.M., Li Q., Coakley K.M., Diaz-Flores E., Gorman M., Przybranowski S., Tran M., Kogan S.C., Roose J.P., Copeland N.G., Jenkins N.A., Parada L., Wolff L., Sebolt-Leopold J., Shannon K. Response and resistance to MEK inhibition in leukaemias initiated by hyperactive Ras. Nature 2009, 461:411-414.
33. Lecuona E., Ridge K., Pesce L., Batlle D., Sznajder J.I. The GTP-binding protein RhoA mediates Na, K-ATPase exocytosis in alveolar epithelial cells. Mol. Biol. Cell 2003, 14:3888-3897.
34. Ledig M.M., Haj F., Bixby J.L., Stoker A.W., Mueller B.K. The receptor tyrosine phosphatase CRYPalpha promotes intraretinal axon growth. J. Cell Biol. 1999, 147:375-388.
35. Leemhuis J., Boutillier S., Schmidt G., Meyer D.K. The protein kinase A inhibitor H89 acts on cell morphology by inhibiting Rho kinase. J. Pharmacol. Exp. Ther. 2002, 300:1000-1007.
36. Lei H., Venkatakrishnan A., Yu S., Kazlauskas A. Protein kinase A-dependent translocation of Hsp90 alpha impairs endothelial nitric-oxide synthase activity in high glucose and diabetes. J. Biol. Chem. 2007, 282:9364-9371.
37. Li W., Cui Y., Kushner S.A., Brown R.A., Jentsch J.D., Frankland P.W., Cannon T.D., Silva A.J. The HMG-CoA reductase inhibitor lovastatin reverses the learning and attention deficits in a mouse model of neurofibromatosis type 1. Curr. Biol. 2005, 15:1961-1967.
38. Li Y.F., Cheng Y.F., Huang Y., Conti M., Wilson S.P., O'Donnell J.M., Zhang H.T. Phosphodiesterase-4D knock-out and RNA interference-mediated knock-down enhance memory and increase hippocampal neurogenesis via increased cAMP signaling. J. Neurosci. 2011, 31:172-183.
39. Listernick R., Louis D.N., Packer R.J., Gutmann D.H. Optic pathway gliomas in children with neurofibromatosis 1: consensus statement from the NF1 Optic Pathway Glioma Task Force. Ann. Neurol. 1997, 41:143-149.
40. Mueller B.K. Growth cone guidance: first steps towards a deeper understanding. Annu. Rev. Neurosci. 1999, 22:351-388.
41. North K., Joy P., Yuille D., Cocks N., Hutchins P. Cognitive function and academic performance in children with neurofibromatosis type 1. Dev. Med. Child Neurol. 1995, 37:427-436.
42. North K.N., Riccardi V., Samango-Sprouse C., Ferner R., Moore B., Legius E., Ratner N., Denckla M.B. Cognitive function and academic performance in neurofibromatosis. 1: consensus statement from the NF1 Cognitive Disorders Task Force. Neurology 1997, 48:1121-1127.
43. Ouyang M., Zhang L., Zhu J.J., Schwede F., Thomas S.A. Epac signaling is required for hippocampus-dependent memory retrieval. Proc Natl Acad Sci USA 2008, 105:11993-11997.
44. Ozonoff S. Cognitive impairment in neurofibromatosis type 1. Am. J. Med. Genet. 1999, 89:45-52.
45. Qi M., Zhou M., Skalhegg B.S., Brandon E.P., Kandel E.R., McKnight G.S., Idzerda R.L. Impaired hippocampal plasticity in mice lacking the Cbeta1 catalytic subunit of cAMP-dependent protein kinase. Proc Natl Acad Sci USA 1996, 93:1571-1576.
46. Rochlin M.W., Itoh K., Adelstein R.S., Bridgman P.C. Localization of myosin II A and B isoforms in cultured neurons. J. Cell Sci. 1995, 108(Pt 12):3661-3670.
47. Romero M.I., Lin L., Lush M.E., Lei L., Parada L.F., Zhu Y. Deletion of Nf1 in neurons induces increased axon collateral branching after dorsal root injury. J. Neurosci. 2007, 27:2124-2134.
48. Rosenfeld A., Listernick R., Charrow J., Goldman S. Neurofibromatosis type 1 and high-grade tumors of the central nervous system. Childs Nerv. Syst. 2010, 26:663-667.
49. Rosser T.L., Packer R.J. Neurocognitive dysfunction in children with neurofibromatosis type 1. Curr. Neurol. Neurosci. Rep. 2003, 3:129-136.
50. Sandsmark D.K., Zhang H., Hegedus B., Pelletier C.L., Weber J.D., Gutmann D.H. Nucleophosmin mediates mammalian target of rapamycin-dependent actin cytoskeleton dynamics and proliferation in neurofibromin-deficient astrocytes. Cancer Res. 2007, 67:4790-4799.
51. Schmitt J.M., Stork P.J. PKA phosphorylation of Src mediates cAMP's inhibition of cell growth via Rap1. Mol. Cell 2002, 9:85-94.
52. Shilyansky C., Karlsgodt K.H., Cummings D.M., Sidiropoulou K., Hardt M., James A.S., Ehninger D., Bearden C.E., Poirazi P., Jentsch J.D., Cannon T.D., Levine M.S., Silva A.J. Neurofibromin regulates corticostriatal inhibitory networks during working memory performance. Proc Natl Acad Sci USA 2010, 107:13141-13146.
53. Silva A.J., Frankland P.W., Marowitz Z., Friedman E., Laszlo G.S., Cioffi D., Jacks T., Bourtchuladze R. A mouse model for the learning and memory deficits associated with neurofibromatosis type I. Nat. Genet. 1997, 15:281-284.
54. Ster J., de Bock F., Bertaso F., Abitbol K., Daniel H., Bockaert J., Fagni L. Epac mediates PACAP-dependent long-term depression in the hippocampus. J. Physiol. 2009, 587:101-113.
55. Tanelian D.L., Barry M.A., Johnston S.A., Le T., Smith G.M. Semaphorin III can repulse and inhibit adult sensory afferents in vivo. Nat. Med. 1997, 3:1398-1401.
56. Tominaga-Yoshino K., Kondo S., Tamotsu S., Ogura A. Repetitive activation of protein kinase A induces slow and persistent potentiation associated with synaptogenesis in cultured hippocampus. Neurosci. Res. 2002, 44:357-367.
57. Tong J., Hannan F., Zhu Y., Bernards A., Zhong Y. Neurofibromin regulates G protein-stimulated adenylyl cyclase activity. Nat. Neurosci. 2002, 5:95-96.
58. Tullio A.N., Bridgman P.C., Tresser N.J., Chan C.C., Conti M.A., Adelstein R.S., Hara Y. Structural abnormalities develop in the brain after ablation of the gene encoding nonmuscle myosin II-B heavy chain. J. Comp. Neurol. 2001, 433:62-74.
59. Vogel K.S., Brannan C.I., Jenkins N.A., Copeland N.G., Parada L.F. Loss of neurofibromin results in neurotrophin-independent survival of embryonic sensory and sympathetic neurons. Cell 1995, 82:733-742.
60. Vogel K.S., Parada L.F. Sympathetic neuron survival and proliferation are prolonged by loss of p53 and neurofibromin. Mol. Cell. Neurosci. 1998, 11:19-28.
61. Wang Z., Phan T., Storm D.R. The type 3 adenylyl cyclase is required for novel object learning and extinction of contextual memory: role of cAMP signaling in primary cilia. J. Neurosci. 2011, 31:5557-5561.
62. Warrington N.M., Gianino S.M., Jackson E., Goldhoff P., Garbow J.R., Piwnica-Worms D., Gutmann D.H., Rubin J.B. Cyclic AMP suppression is sufficient to induce gliomagenesis in a mouse model of neurofibromatosis-1. Cancer Res. 2010, 70:5717-5727.
63. Warrington N.M., Woerner B.M., Dagninakatte G.C., Dasgupta B., Perry A., Gutmann D.H., Rubin J.B. Spatiotemporal differences in CXCL12 expression and cyclic AMP underlie the unique pattern of optic glioma growth in neurofibromatosis type 1. Cancer Res. 2007, 67:8588-8595.
64. Yamakita Y., Yamashiro S., Matsumura F. In vivo phosphorylation of regulatory light chain of myosin II during mitosis of cultured cells. J. Cell Biol. 1994, 124:129-137.
65. Yamamoto M., Urakubo T., Tominaga-Yoshino K., Ogura A. Long-lasting synapse formation in cultured rat hippocampal neurons after repeated PKA activation. Brain Res. 2005, 1042:6-16.
66. Yamauchi J., Hirasawa A., Miyamoto Y., Itoh H., Tsujimoto G. Beta2-adrenergic receptor/cyclic adenosine monophosphate (cAMP) leads to JNK activation through Rho family small GTPases. Biochem. Biophys. Res. Commun. 2001, 284:1199-1203.