Protein kinase Cα and integrin-linked kinase mediate the negative axon guidance effects of Sonic hedgehog

Molecular and Cellular Neuroscience

Volumn 50, Issue 1, 2012, Pages 82-92

  Guo, Daorong ^a   Standley, Clive ^a   Bellve, Karl ^a   Fogarty, Kevin ^a   Bao, Zheng Zheng ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

Axon guidance; ILK; PKC ; Shh

Indexed keywords

CALCIUM ION; INTEGRIN LINKED KINASE; PROTEIN KINASE C ALPHA; SONIC HEDGEHOG PROTEIN; THREONINE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CALCIUM CELL LEVEL; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; EMBRYO; ENZYME ACTIVATION; ENZYME ASSAY; ENZYME PHOSPHORYLATION; GROWTH CONE; NERVE FIBER GROWTH; NERVE PROJECTION; NONHUMAN; OPTIC CHIASM; OPTIC DISK; PINOCYTOSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETINA GANGLION CELL; SIGNAL TRANSDUCTION;

ACETOPHENONES; ANIMALS; AXONS; BENZOPYRANS; CALCIUM; CELLS, CULTURED; CHICK EMBRYO; ENZYME INHIBITORS; GROWTH CONES; HEDGEHOG PROTEINS; MUTATION; PHOSPHORYLATION; PROTEIN KINASE C-ALPHA; PROTEIN-SERINE-THREONINE KINASES; RETINAL GANGLION CELLS; THREONINE;

ERINACEIDAE;

EID: 84860613389     PISSN: 10447431     EISSN: 10959327     Source Type: Journal    
DOI: 10.1016/j.mcn.2012.03.008     Document Type: Article

References (63)

1. Acconcia F., Barnes C.J., Singh R.R., Talukder A.H., Kumar R. Phosphorylation-dependent regulation of nuclear localization and functions of integrin-linked kinase. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:6782-6787.
2. Bao Z.Z. Intraretinal projection of retinal ganglion cell axons as a model system for studying axon navigation. Brain Res. 2008, 1192:165-177.
3. Bourikas D., Pekarik V., Baeriswyl T., Grunditz A., Sadhu R., Nardo M., Stoeckli E.T. Sonic hedgehog guides commissural axons along the longitudinal axis of the spinal cord. Nat. Neurosci. 2005, 8:297-304.
4. Campeau E., Ruhl V.E., Rodier F., Smith C.L., Rahmberg B.L., Fuss J.O., Campisi J., Yaswen P., Cooper P.K., Kaufman P.D. A versatile viral system for expression and depletion of proteins in mammalian cells. PLoS One 2009, 4:e6529.
5. Charron F., Stein E., Jeong J., McMahon A.P., Tessier-Lavigne M. The morphogen Sonic hedgehog is an axonal chemoattractant that collaborates with Netrin-1 in midline axon guidance. Cell 2003, 113:11-23.
6. Chau M.D., Tuft R., Fogarty K., Bao Z.Z. Notch signaling plays a key role in cardiac cell differentiation. Mech. Dev. 2006, 123:626-640.
7. Chiswell B.P., Zhang R., Murphy J.W., Boggon T.J., Calderwood D.A. The structural basis of integrin-linked kinase-PINCH interactions. Proc. Natl. Acad. Sci. 2008, 105:20677-20682.
8. Chiswell B.P., Stiegler A.L., Razinia Z., Nalibotski E., Boggon T.J., Calderwood D.A. Structural basis of competition between PINCH1 and PINCH2 for binding to the ankyrin repeat domain of integrin-linked kinase. J. Struct. Biol. 2010, 170:157-163.
9. Dempsey E.C., Newton A.C., Mochly-Rosen D., Fields A.P., Reyland M.E., Insel P.A., Messing R.O. Protein kinase C isozymes and the regulation of diverse cell responses. Am. J. Physiol. Lung Cell. Mol. Physiol. 2000, 279:L429-L438.
10. Dent E.W., Gertler F.B. Cytoskeletal dynamics and transport in growth cone motility and axon guidance. Neuron 2003, 40:209-227.
11. Ensslen S.E., Brady-Kalnay S.M. PTPmu signaling via PKCdelta is instructive for retinal ganglion cell guidance. Mol. Cell. Neurosci. 2004, 25:558-571.
12. Erskine L., Williams S.E., Brose K., Kidd T., Rachel R.A., Goodman C.S., Tessier-Lavigne M., Mason C.A. Retinal ganglion cell axon guidance in the mouse optic chiasm: expression and function of robos and slits. J. Neurosci. 2000, 20:4975-4982.
13. Fabre P.J., Shimogori T., Charron F. Segregation of ipsilateral retinal ganglion cell axons at the optic chiasm requires the Shh receptor Boc. J. Neurosci. 2010, 30:266-275.
14. Fukuda K., Gupta S., Chen K., Wu C., Qin J. The pseudoactive site of ILK is essential for its binding to alpha-Parvin and localization to focal adhesions. Mol. Cell 2009, 36:819-830.
15. Ginnan R., Pfleiderer P.J., Pumiglia K., Singer H.A. PKC-delta and CaMKII-delta 2 mediate ATP-dependent activation of ERK1/2 in vascular smooth muscle. Am. J. Physiol. Cell Physiol. 2004, 286:C1281-C1289.
16. Grimmer S., van Deurs B., Sandvig K. Membrane ruffling and macropinocytosis in A431 cells require cholesterol. J. Cell Sci. 2002, 115:2953-2962.
17. Guo W., Jiang H., Gray V., Dedhar S., Rao Y. Role of the integrin-linked kinase (ILK) in determining neuronal polarity. Dev. Biol. 2007, 306:457-468.
18. Hannigan G.E., Leung-Hagesteijn C., Fitz-Gibbon L., Coppolino M.G., Radeva G., Filmus J., Bell J.C., Dedhar S. Regulation of cell adhesion and anchorage-dependent growth by a new beta 1-integrin-linked protein kinase. Nature 1996, 379:91-96.
19. Hannigan G., Troussard A.A., Dedhar S. Integrin-linked kinase: a cancer therapeutic target unique among its ILK. Nat. Rev. Cancer 2005, 5:51-63.
20. Hines J.H., Abu-Rub M., Henley J.R. Asymmetric endocytosis and remodeling of beta1-integrin adhesions during growth cone chemorepulsion by MAG. Nat. Neurosci. 2010, 13:829-837.
21. Hong K., Nishiyama M., Henley J., Tessier-Lavigne M., Poo M. Calcium signalling in the guidance of nerve growth by netrin-1. Nature 2000, 403:93-98.
22. Ishii T., Satoh E., Nishimura M. Integrin-linked kinase controls neurite outgrowth in N1E-115 neuroblastoma cells. J. Biol. Chem. 2001, 276:42994-43003.
23. Jin Z., Zhang J., Klar A., Chedotal A., Rao Y., Cepko C.L., Bao Z.Z. Irx4-mediated regulation of Slit1 expression contributes to the definition of early axonal paths inside the retina. Development 2003, 130:1037-1048.
24. Kolpak A., Zhang J., Bao Z.Z. Sonic hedgehog has a dual effect on the growth of retinal ganglion axons depending on its concentration. J. Neurosci. 2005, 25:3432-3441.
25. Kolpak A.L., Jiang J., Guo D., Standley C., Bellve K., Fogarty K., Bao Z.Z. Negative guidance factor-induced macropinocytosis in the growth cone plays a critical role in repulsive axon turning. J. Neurosci. 2009, 29:10488-10498.
26. Legate K.R., Montanez E., Kudlacek O., Fassler R. ILK, PINCH and parvin: the tIPP of integrin signalling. Nat. Rev. Mol. Cell Biol. 2006, 7:20-31.
27. Lin Y.F., Leu S.J., Huang H.M., Tsai Y.H. Selective activation of specific PKC isoforms dictating the fate of CD14(+) monocytes towards differentiation or apoptosis. J. Cell. Physiol. 2011, 226:122-131.
28. Linding R., Jensen L.J., Ostheimer G.J., van Vugt M.A., Jorgensen C., Miron I.M., Diella F., Colwill K., Taylor L., Elder K., Metalnikov P., Nguyen V., Pasculescu A., Jin J., Park J.G., Samson L.D., Woodgett J.R., Russell R.B., Bork P., Yaffe M.B., Pawson T. Systematic discovery of in vivo phosphorylation networks. Cell 2007, 129:1415-1426.
29. Lowery L.A., Van Vactor D. The trip of the tip: understanding the growth cone machinery. Nat. Rev. Mol. Cell Biol. 2009, 10:332-343.
30. Ma H.T., Lin W.W., Zhao B., Wu W.T., Huang W., Li Y., Jones N.L., Kruth H.S. Protein kinase C beta and delta isoenzymes mediate cholesterol accumulation in PMA-activated macrophages. Biochem. Biophys. Res. Commun. 2006, 349:214-220.
31. Madigan J.P., Bodemann B.O., Brady D.C., Dewar B.J., Keller P.J., Leitges M., Philips M.R., Ridley A.J., Der C.J., Cox A.D. Regulation of Rnd3 localization and function by protein kinase C alpha-mediated phosphorylation. Biochem. J. 2009, 424:153-161.
32. Marcus R.C., Mason C.A. The first retinal axon growth in the mouse optic chiasm: axon patterning and the cellular environment. J. Neurosci. 1995, 15:6389-6402.
33. Martiny-Baron G., Kazanietz M.G., Mischak H., Blumberg P.M., Kochs G., Hug H., Marme D., Schachtele C. Selective inhibition of protein kinase C isozymes by the indolocarbazole Go 6976. J. Biol. Chem. 1993, 268:9194-9197.
34. Mehta D., Rahman A., Malik A.B. Protein kinase C-alpha signals rho-guanine nucleotide dissociation inhibitor phosphorylation and rho activation and regulates the endothelial cell barrier function. J. Biol. Chem. 2001, 276:22614-22620.
35. Meier O., Boucke K., Hammer S.V., Keller S., Stidwill R.P., Hemmi S., Greber U.F. Adenovirus triggers macropinocytosis and endosomal leakage together with its clathrin-mediated uptake. J. Cell Biol. 2002, 158:1119-1131.
36. Mills J., Digicaylioglu M., Legg A.T., Young C.E., Young S.S., Barr A.M., Fletcher L., O'Connor T.P., Dedhar S. Role of integrin-linked kinase in nerve growth factor-stimulated neurite outgrowth. J. Neurosci. 2003, 23:1638-1648.
37. Mogami H., Zhang H., Suzuki Y., Urano T., Saito N., Kojima I., Petersen O.H. Decoding of short-lived Ca2+ influx signals into long term substrate phosphorylation through activation of two distinct classes of protein kinase C. J. Biol. Chem. 2003, 278:9896-9904.
38. Oancea E., Meyer T. Protein kinase C as a molecular machine for decoding calcium and diacylglycerol signals. Cell 1998, 95:307-318.
39. Ohno S., Konno Y., Akita Y., Yano A., Suzuki K. A point mutation at the putative ATP-binding site of protein kinase C alpha abolishes the kinase activity and renders it down-regulation-insensitive. A molecular link between autophosphorylation and down-regulation. J. Biol. Chem. 1990, 265:6296-6300.
40. O'Leary D.M., Gerfen C.R., Cowan W.M. The development and restriction of the ipsilateral retinofugal projection in the chick. Brain Res. 1983, 312:93-109.
41. Pang H., Bitar K.N. Direct association of RhoA with specific domains of PKC-alpha. Am. J. Physiol. Cell Physiol. 2005, 289:C982-C993.
42. Prada C., Puga J., Perez-Mendez L., Lopez, Ramirez G. Spatial and temporal patterns of neurogenesis in the chick retina. Eur. J. Neurosci. 1991, 3:1187.
43. Riobo N.A., Haines G.M., Emerson C.P. Protein kinase C-delta and mitogen-activated protein/extracellular signal-regulated kinase-1 control GLI activation in hedgehog signaling. Cancer Res. 2006, 66:839-845.
44. Rosse C., Linch M., Kermorgant S., Cameron A.J., Boeckeler K., Parker P.J. PKC and the control of localized signal dynamics. Nat. Rev. Mol. Cell Biol. 2010, 11:103-112.
45. Sanchez-Camacho C., Bovolenta P. Autonomous and non-autonomous Shh signalling mediate the in vivo growth and guidance of mouse retinal ganglion cell axons. Development 2008, 135:3531-3541.
46. Sarkar K., Kruhlak M.J., Erlandsen S.L., Shaw S. Selective inhibition by rottlerin of macropinocytosis in monocyte-derived dendritic cells. Immunology 2005, 116:513-524.
47. Shirai Y., Saito N. Activation mechanisms of protein kinase C: maturation, catalytic activation, and targeting. J. Biochem. 2002, 132:663-668.
48. Slater S.J., Seiz J.L., Stagliano B.A., Stubbs C.D. Interaction of protein kinase C isozymes with Rho GTPases. Biochemistry 2001, 40:4437-4445.
49. Soh J.W., Weinstein I.B. Roles of specific isoforms of protein kinase C in the transcriptional control of cyclin D1 and related genes. J. Biol. Chem. 2003, 278:34709-34716.
50. Steinberg S.F. Structural basis of protein kinase C isoform function. Physiol. Rev. 2008, 88:1341-1378.
51. Swanson J.A. Shaping cups into phagosomes and macropinosomes. Nat. Rev. Mol. Cell Biol. 2008, 9:639-649.
52. Tanaka M., Sagawa S., Hoshi J., Shimoma F., Matsuda I., Sakoda K., Sasase T., Shindo M., Inaba T. Synthesis of anilino-monoindolylmaleimides as potent and selective PKCbeta inhibitors. Bioorg. Med. Chem. Lett. 2004, 14:5171-5174.
53. Tojima T., Akiyama H., Itofusa R., Li Y., Katayama H., Miyawaki A., Kamiguchi H. Attractive axon guidance involves asymmetric membrane transport and exocytosis in the growth cone. Nat. Neurosci. 2007, 10:58-66.
54. Tojima T., Itofusa R., Kamiguchi H. Asymmetric clathrin-mediated endocytosis drives repulsive growth cone guidance. Neuron 2010, 66:370-377.
55. Trousse F., Marti E., Gruss P., Torres M., Bovolenta P. Control of retinal ganglion cell axon growth: a new role for Sonic hedgehog. Dev. Suppl. 2001, 128:3927-3936.
56. Wickstrom S.A., Lange A., Montanez E., Fassler R. The ILK/PINCH/parvin complex: the kinase is dead, long live the pseudokinase!. EMBO J. 2010, 29:281-291.
57. Wolf A.M., Lyuksyutova A.I., Fenstermaker A.G., Shafer B., Lo C.G., Zou Y. Phosphatidylinositol-3-kinase-atypical protein kinase C signaling is required for Wnt attraction and anterior-posterior axon guidance. J. Neurosci. 2008, 28:3456-3467.
58. Wong E.V., Kerner J.A., Jay D.G. Convergent and divergent signaling mechanisms of growth cone collapse by ephrinA5 and slit2. J. Neurobiol. 2004, 59:66-81.
59. Wu C., Dedhar S. Integrin-linked kinase (ILK) and its interactors: a new paradigm for the coupling of extracellular matrix to actin cytoskeleton and signaling complexes. J. Cell Biol. 2001, 155:505-510.
60. Wu D.Y., Zheng J.Q., McDonald M.A., Chang B., Twiss J.L. PKC isozymes in the enhanced regrowth of retinal neurites after optic nerve injury. Invest. Ophthalmol. Vis. Sci. 2003, 44:2783-2790.
61. Xiang Y., Li Y., Zhang Z., Cui K., Wang S., Yuan X.B., Wu C.P., Poo M.M., Duan S. Nerve growth cone guidance mediated by G protein-coupled receptors. Nat. Neurosci. 2002, 5:843-848.
62. Yam P.T., Langlois S.D., Morin S., Charron F. Sonic hedgehog guides axons through a noncanonical, Src-family-kinase-dependent signaling pathway. Neuron 2009, 62:349-362.
63. Zhou and Cohan Growth cone collapse through coincident loss of actin bundles and leading edge actin without actin depolymerization. J. Cell Biol. 2001, 153:1071-1083.