P21-Activated kinase (PAK) is required for Bone Morphogenetic Protein (BMP)-induced dendritogenesis in cortical neurons

Molecular and Cellular Neuroscience

Volumn 57, Issue , 2013, Pages 83-92

  Podkowa, Monika ^a   Christova, Tania ^a   Zhao, Xin ^a   Jian, Yongqiang ^a   Attisano, Liliana ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

Bone Morphogenetic Proteins (BMP); Cytoskeleton; Dendritogenesis; LIM Kinase; Neurons; P21 Activated kinase (PAK); Receptor serine threonine kinases

Indexed keywords

ALK2 PROTEIN; BONE MORPHOGENETIC PROTEIN RECEPTOR 1; BONE MORPHOGENETIC PROTEIN RECEPTOR 2; COFILIN; LIM KINASE; OSTEOGENIC PROTEIN 1; P21 ACTIVATED KINASE 1; SMAD PROTEIN; UNCLASSIFIED DRUG;

ACTIN FILAMENT; ANIMAL CELL; ARTICLE; BRAIN NERVE CELL; CANCER CELL CULTURE; CONTROLLED STUDY; CYTOSKELETON; DENDRITOGENESIS; EMBRYO; ENZYME ACTIVATION; MOUSE; NERVE CELL DIFFERENTIATION; NERVE FIBER GROWTH; NERVOUS SYSTEM; NEUROBLASTOMA CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION;

BONE MORPHOGENETIC PROTEINS (BMP); CYTOSKELETON; DENDRITOGENESIS; LIM KINASE; NEURONS; P21-ACTIVATED KINASE (PAK); RECEPTOR SERINE THREONINE KINASES;

ACTIN CYTOSKELETON; ACTIN DEPOLYMERIZING FACTORS; ACTIVIN RECEPTORS, TYPE I; ANIMALS; BONE MORPHOGENETIC PROTEIN 7; CELL LINE, TUMOR; CELLS, CULTURED; CEREBRAL CORTEX; DENDRITES; LIM KINASES; MICE; NEUROGENESIS; P21-ACTIVATED KINASES; PHOSPHORYLATION; PROTEIN BINDING;

EID: 84887351931     PISSN: 10447431     EISSN: 10959327     Source Type: Journal    
DOI: 10.1016/j.mcn.2013.10.005     Document Type: Article

References (65)

1. Aberle H., Haghighi A.P., Fetter R.D., McCabe B.D., Magalhaes T.R., Goodman C.S. Wishful thinking encodes a BMP type II receptor that regulates synaptic growth in Drosophila. Neuron 2002, 33:545-558.
2. Allen K.M., Gleeson J.G., Bagrodia S., Partington M.W., MacMillan J.C., Cerione R.A., Mulley J.C., Walsh C.A. PAK3 mutation in nonsyndromic X-linked mental retardation. Nat. Genet. 1998, 20:25-30.
3. Asrar S., Meng Y., Zhou Z., Todorovski Z., Huang W.W., Jia Z. Regulation of hippocampal long-term potentiation by p21-activated protein kinase 1 (PAK1). Neuropharmacology 2009, 56:73-80.
4. Barrios-Rodiles M., Brown K.R., Ozdamar B., Bose R., Liu Z., Donovan R.S., Shinjo F., Liu Y., Dembowy J., Taylor I.W., Luga V., Przulj N., Robinson M., Suzuki H., Hayashizaki Y., Jurisica I., Wrana J.L. High-throughput mapping of a dynamic signaling network in mammalian cells. Science 2005, 307:1621-1625.
5. Beppu H., Kawabata M., Hamamoto T., Chytil A., Minowa O., Noda T., Miyazono K. BMP type II receptor is required for gastrulation and early development of mouse embryos. Dev. Biol. 2000, 221:249-258.
6. Bernard O. Lim kinases, regulators of actin dynamics. Int. J. Biochem. Cell Biol. 2007, 39:1071-1076.
7. Bond A.M., Bhalala O.G., Kessler J.A. The dynamic role of bone morphogenetic proteins in neural stem cell fate and maturation. Dev. Neurobiol. 2012, 72:1068-1084.
8. Chan P.M., Manser E. PAKs in human disease. Prog. Mol. Biol. Transl. Sci. 2012, 106:171-187.
9. Chan M.C., Nguyen P.H., Davis B.N., Ohoka N., Hayashi H., Du K., Lagna G., Hata A. A novel regulatory mechanism of the bone morphogenetic protein (BMP) signaling pathway involving the carboxyl-terminal tail domain of BMP type II receptor. Mol. Cell Biol. 2007, 27:5776-5789.
10. Daniels R.H., Hall P.S., Bokoch G.M. Membrane targeting of p21-activated kinase 1 (PAK1) induces neurite outgrowth from PC12 cells. EMBO J. 1998, 17:754-764.
11. Daub H., Gevaert K., Vandekerckhove J., Sobel A., Hall A. Rac/Cdc42 and p65PAK regulate the microtubule-destabilizing protein stathmin through phosphorylation at serine 16. J. Biol. Chem. 2001, 276:1677-1680.
12. Du Y., Yip H. Effects of bone morphogenetic protein 2 on Id expression and neuroblastoma cell differentiation. Differentiation 2010, 79:84-92.
13. Eaton B.A., Davis G.W. LIM Kinase1 controls synaptic stability downstream of the type II BMP receptor. Neuron 2005, 47:695-708.
14. Etienne-Manneville S., Hall A. Rho GTPases in cell biology. Nature 2002, 420:629-635.
15. Foletta V.C., Lim M.A., Soosairajah J., Kelly A.P., Stanley E.G., Shannon M., He W., Das S., Massague J., Bernard O. Direct signaling by the BMP type II receptor via the cytoskeletal regulator LIMK1. J. Cell Biol. 2003, 162:1089-1098.
16. Frisch A., Wright C.V. XBMPRII, a novel Xenopus type II receptor mediating BMP signaling in embryonic tissues. Development 1998, 125:431-442.
17. Fukuda T., Kohda M., Kanomata K., Nojima J., Nakamura A., Kamizono J., Noguchi Y., Iwakiri K., Kondo T., Kurose J., Endo K., Awakura T., Fukushi J., Nakashima Y., Chiyonobu T., Kawara A., Nishida Y., Wada I., Akita M., Komori T., Nakayama K., Nanba A., Maruki Y., Yoda T., Tomoda H., Yu P.B., Shore E.M., Kaplan F.S., Miyazono K., Matsuoka M., Ikebuchi K., Ohtake A., Oda H., Jimi E., Owan I., Okazaki Y., Katagiri T. Constitutively activated ALK2 and increased SMAD1/5 cooperatively induce bone morphogenetic protein signaling in fibrodysplasia ossificans progressiva. J. Biol. Chem. 2009, 284:7149-7156.
18. Gamell C., Osses N., Bartrons R., Ruckle T., Camps M., Rosa J.L., Ventura F. BMP2 induction of actin cytoskeleton reorganization and cell migration requires PI3-kinase and Cdc42 activity. J. Cell Sci. 2008, 121:3960-3970.
19. Gamell C., Susperregui A.G., Bernard O., Rosa J.L., Ventura F. The p38/MK2/Hsp25 pathway is required for BMP-2-induced cell migration. PLoS One 2011, 6:e16477.
20. Georges P.C., Hadzimichalis N.M., Sweet E.S., Firestein B.L. The yin-yang of dendrite morphology: unity of actin and microtubules. Mol. Neurobiol. 2008, 38:270-284.
21. Govek E.E., Newey S.E., Van Aelst L. The role of the Rho GTPases in neuronal development. Genes Dev. 2005, 19:1-49.
22. Haghighi A.P., McCabe B.D., Fetter R.D., Palmer J.E., Hom S., Goodman C.S. Retrograde control of synaptic transmission by postsynaptic CaMKII at the Drosophila neuromuscular junction. Neuron 2003, 39:255-267.
23. Hayashi M.L., Choi S.Y., Rao B.S., Jung H.Y., Lee H.K., Zhang D., Chattarji S., Kirkwood A., Tonegawa S. Altered cortical synaptic morphology and impaired memory consolidation in forebrain-specific dominant-negative PAK transgenic mice. Neuron 2004, 42:773-787.
24. Henriquez J.P., Krull C.E., Osses N. The Wnt and BMP families of signaling morphogens at the vertebrate neuromuscular junction. Int. J. Mol. Sci. 2011, 12:8924-8946.
25. Hocking J.C., Hehr C.L., Bertolesi G., Funakoshi H., Nakamura T., McFarlane S. LIMK1 acts downstream of BMP signaling in developing retinal ganglion cell axons but not dendrites. Dev. Biol. 2009, 330:273-285.
26. Huang W., Zhou Z., Asrar S., Henkelman M., Xie W., Jia Z. p21-Activated kinases 1 and 3 control brain size through coordinating neuronal complexity and synaptic properties. Mol. Cell Biol. 2011, 31:388-403.
27. Jacobs T., Causeret F., Nishimura Y.V., Terao M., Norman A., Hoshino M., Nikolic M. Localized activation of p21-activated kinase controls neuronal polarity and morphology. J. Neurosci. 2007, 27:8604-8615.
28. Jaffe A.B., Hall A. Rho GTPases: biochemistry and biology. Annu. Rev. Cell Dev. Biol. 2005, 21:247-269.
29. Knaus U.G., Morris S., Dong H.J., Chernoff J., Bokoch G.M. Regulation of human leukocyte p21-activated kinases through G protein-coupled receptors. Science 1995, 269:221-223.
30. Kreis P., Barnier J.V. PAK signalling in neuronal physiology. Cell. Signal. 2009, 21:384-393.
31. Labbe E., Letamendia A., Attisano L. Association of Smads with lymphoid enhancer binding factor 1/T cell-specific factor mediates cooperative signaling by the transforming growth factor-beta and Wnt pathways. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:8358-8363.
32. Lee-Hoeflich S.T., Causing C.G., Podkowa M., Zhao X., Wrana J.L., Attisano L. Activation of LIMK1 by binding to the BMP receptor, BMPRII, regulates BMP-dependent dendritogenesis. EMBO J. 2004, 23:4792-4801.
33. Lei M., Lu W., Meng W., Parrini M.C., Eck M.J., Mayer B.J., Harrison S.C. Structure of PAK1 in an autoinhibited conformation reveals a multistage activation switch. Cell 2000, 102:387-397.
34. Machado R.D., Rudarakanchana N., Atkinson C., Flanagan J.A., Harrison R., Morrell N.W., Trembath R.C. Functional interaction between BMPR-II and Tctex-1, a light chain of Dynein, is isoform-specific and disrupted by mutations underlying primary pulmonary hypertension. Hum. Mol. Genet. 2003, 12:3277-3286.
35. Marques G., Zhang B. Retrograde signaling that regulates synaptic development and function at the Drosophila neuromuscular junction. Int. Rev. Neurobiol. 2006, 75:267-285.
36. Marques G., Bao H., Haerry T.E., Shimell M.J., Duchek P., Zhang B., O'Connor M.B. The Drosophila BMP type II receptor Wishful Thinking regulates neuromuscular synapse morphology and function. Neuron 2002, 33:529-543.
37. Maruta H., He H., Nheu T. Interfering with Ras signaling using membrane-permeable peptides or drugs. Methods Mol. Biol. 2002, 189:75-85.
38. Miller F.D., Kaplan D.R. Signaling mechanisms underlying dendrite formation. Curr. Opin. Neurobiol. 2003, 13:391-398.
39. Miller B.W., Lau G., Grouios C., Mollica E., Barrios-Rodiles M., Liu Y., Datti A., Morris Q., Wrana J.L., Attisano L. Application of an integrated physical and functional screening approach to identify inhibitors of the Wnt pathway. Mol. Syst. Biol. 2009, 5:315.
40. Miyagi M., Mikawa S., Hasegawa T., Kobayashi S., Matsuyama Y., Sato K. Bone morphogenetic protein receptor expressions in the adult rat brain. Neuroscience 2011, 176:93-109.
41. Miyagi M., Mikawa S., Sato T., Hasegawa T., Kobayashi S., Matsuyama Y., Sato K. BMP2, BMP4, noggin, BMPRIA, BMPRIB, and BMPRII are differentially expressed in the adult rat spinal cord. Neuroscience 2012, 203:12-26.
42. Miyazono K., Kamiya Y., Morikawa M. Bone morphogenetic protein receptors and signal transduction. J. Biochem. 2010, 147:35-51.
43. Morrell N.W. Role of bone morphogenetic protein receptors in the development of pulmonary arterial hypertension. Adv. Exp. Med. Biol. 2011, 661:251-264.
44. Mu Y., Gudey S.K., Landstrom M. Non-Smad signaling pathways. Cell Tissue Res. 2012, 347:11-20.
45. Nahm M., Lee M.J., Parkinson W., Lee M., Kim H., Kim Y.J., Kim S., Cho Y.S., Min B.M., Bae Y.C., Broadie K., Lee S. Spartin regulates synaptic growth and neuronal survival by inhibiting BMP-mediated microtubule stabilization. Neuron 2013, 77:680-695.
46. Narimatsu M., Bose R., Pye M., Zhang L., Miller B., Ching P., Sakuma R., Luga V., Roncari L., Attisano L., Wrana J.L. Regulation of planar cell polarity by Smurf ubiquitin ligases. Cell 2009, 137:295-307.
47. Ng J. TGF-beta signals regulate axonal development through distinct Smad-independent mechanisms. Development 2008, 135:4025-4035.
48. Nikolic M. The Pak1 kinase: an important regulator of neuronal morphology and function in the developing forebrain. Mol. Neurobiol. 2008, 37:187-202.
49. Park K.S., Gumbiner B.M. Cadherin-6B stimulates an epithelial mesenchymal transition and the delamination of cells from the neural ectoderm via LIMK/cofilin mediated non-canonical BMP receptor signaling. Dev. Biol. 2012, 366:232-243.
50. Parrini M.C., Lei M., Harrison S.C., Mayer B.J. Pak1 kinase homodimers are autoinhibited in trans and dissociated upon activation by Cdc42 and Rac1. Mol. Cell 2002, 9:73-83.
51. Perron J.C., Dodd J. Inductive specification and axonal orientation of spinal neurons mediated by divergent bone morphogenetic protein signaling pathways. Neural Dev. 2011, 6:36.
52. Podkowa M., Zhao X., Chow C.W., Coffey E.T., Davis R.J., Attisano L. Microtubule stabilization by bone morphogenetic protein receptor-mediated scaffolding of c-Jun N-terminal kinase promotes dendrite formation. Mol. Cell Biol. 2010, 30:2241-2250.
53. Sanchez-Camacho C., Bovolenta P. Emerging mechanisms in morphogen-mediated axon guidance. Bioessays 2009, 31:1013-1025.
54. Santiago-Medina M., Gregus K.A., Gomez T.M. PAK-PIX interactions regulate adhesion dynamics and membrane protrusion to control neurite outgrowth. J. Cell Sci. 2013, 126:1122-1133.
55. Sieber C., Kopf J., Hiepen C., Knaus P. Recent advances in BMP receptor signaling. Cytokine Growth Factor Rev. 2009, 20:343-355.
56. Stiess M., Bradke F. Neuronal polarization: the cytoskeleton leads the way. Dev. Neurobiol. 2011, 71:430-444.
57. Suzuki A., Thies R.S., Yamaji N., Song J.J., Wozney J.M., Murakami K., Ueno N. A truncated bone morphogenetic protein receptor affects dorsal-ventral patterning in the early Xenopus embryo. Proc. Natl. Acad. Sci. U. S. A. 1994, 91:10255-10259.
58. Taipale M., Krykbaeva I., Koeva M., Kayatekin C., Westover K.D., Karras G.I., Lindquist S. Quantitative analysis of HSP90-client interactions reveals principles of substrate recognition. Cell 2012, 150:987-1001.
59. Tremblay R.G., Sikorska M., Sandhu J.K., Lanthier P., Ribecco-Lutkiewicz M., Bani-Yaghoub M. Differentiation of mouse Neuro 2A cells into dopamine neurons. J. Neurosci. Methods 2010, 186:60-67.
60. Varelas X., Miller B.W., Sopko R., Song S., Gregorieff A., Fellouse F.A., Sakuma R., Pawson T., Hunziker W., McNeill H., Wrana J.L., Attisano L. The Hippo pathway regulates Wnt/beta-catenin signaling. Dev. Cell 2010, 18:579-591.
61. Wen Z., Han L., Bamburg J.R., Shim S., Ming G.L., Zheng J.Q. BMP gradients steer nerve growth cones by a balancing act of LIM kinase and Slingshot phosphatase on ADF/cofilin. J. Cell Biol. 2007, 178:107-119.
62. Wieser R., Wrana J.L., Massague J. GS domain mutations that constitutively activate T beta R-I, the downstream signaling component in the TGF-beta receptor complex. EMBO J. 1995, 14:2199-2208.
63. Wilkes M.C., Murphy S.J., Garamszegi N., Leof E.B. Cell-type-specific activation of PAK2 by transforming growth factor beta independent of Smad2 and Smad3. Mol. Cell Biol. 2003, 23:8878-8889.
64. Wong W.K., Knowles J.A., Morse J.H. Bone morphogenetic protein receptor type II C-terminus interacts with c-Src: implication for a role in pulmonary arterial hypertension. Am. J. Respir. Cell Mol. Biol. 2005, 33:438-446.
65. Wu G., Fang Y., Lu Z.H., Ledeen R.W. Induction of axon-like and dendrite-like processes in neuroblastoma cells. J. Neurocytol. 1998, 27:1-14.