Competing molecular interactions of aPKC isoforms regulate neuronal polarity

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

Volumn 110, Issue 35, 2013, Pages 14450-14455

  Parker, Sara S ^a   Mandell, Edward K ^a   Hapak, Sophie M ^a   Maskaykina, Irina Y ^a   Kusne, Yael ^b   Kim, Ji Young ^a   Moy, Jamie K ^a   St John, Paul A ^a   Wilson, Jean M ^a   Gothard, Katalin M ^c   Price, Theodore J ^a   Ghosh, Sourav ^a,b  

^a Department of Cellular and Molecular Medicine ^*  (United States)

^b ARIZONA STATE UNIVERSITY   (United States)

^c UNIVERSITY OF ARIZONA   (United States)

Author keywords

Axonogenesis; Neurodevelopment; Symmetry breaking

Indexed keywords

ATYPICAL PROTEIN KINASE C LAMBDA; ATYPICAL PROTEIN KINASE C ZETA; CELL PROTEIN; PROTEIN KINASE C; PROTEIN PAR3; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BINDING COMPETITION; CELL POLARITY; CONTROLLED STUDY; EMBRYO; ENZYME LOCALIZATION; GENE OVEREXPRESSION; HIPPOCAMPUS; MOLECULAR INTERACTION; NERVE CELL POLARITY; NERVE FIBER; NEURITE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT;

AXONOGENESIS; NEURODEVELOPMENT; SYMMETRY BREAKING;

ANIMALS; CELL POLARITY; CELLS, CULTURED; FEMALE; HIPPOCAMPUS; ISOENZYMES; NEURONS; PREGNANCY; PROTEIN KINASE C; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84883378900     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1301588110     Document Type: Article

References (46)

1. Goldstein B, Macara IG (2007) The PAR proteins: Fundamental players in animal cell polarization. Dev Cell 13(5):609-622.
2. McCaffrey LM, Macara IG (2012) Signaling pathways in cell polarity. Cold Spring Harb Perspect Biol 4(6), 10.1101/cshperspect.a009654.
3. Thompson BJ (2013) Cell polarity: Models and mechanisms from yeast, worms and flies. Development 140(1):13-21.
4. Hirai T, Chida K (2003) Protein kinase Czeta (PKCzeta): Activation mechanisms and cellular functions. J Biochem 133(1):1-7.
5. Hernandez AI, et al. (2003) Protein kinase M zeta synthesis from a brain mRNA encoding an independent protein kinase C zeta catalytic domain. Implications for the molecular mechanism of memory. J Biol Chem 278(41):40305-40316.
6. Sacktor TC (2012) Memory maintenance by PKMζ-an evolutionary perspective. Mol Brain 5:31.
7. Ohno S (2001) Intercellular junctions and cellular polarity: The PAR-aPKC complex, a conserved core cassette playing fundamental roles in cell polarity. Curr Opin Cell Biol 13(5):641-648.
8. Henrique D, Schweisguth F (2003) Cell polarity: The ups and downs of the Par6/aPKC complex. Curr Opin Genet Dev 13(4):341-350.
9. Ghosh S, et al. (2008) Instructive role of aPKCzeta subcellular localization in the assembly of adherens junctions in neural progenitors. Proc Natl Acad Sci USA 105(1): 335-340.
10. Sacktor TC (2011) How does PKMζ maintain long-term memory? Nat Rev Neurosci 12(1):9-15.
11. Asiedu MN, et al. (2011) Spinal protein kinase M ζ underlies the maintenance mechanism of persistent nociceptive sensitization. J Neurosci 31(18):6646-6653.
12. Banker GA, Cowan WM (1977) Rat hippocampal neurons in dispersed cell culture. Brain Res 126(3):397-425.
13. Dotti CG, Sullivan CA, Banker GA (1988) The establishment of polarity by hippocampal neurons in culture. J Neurosci 8(4):1454-1468.
14. Polleux F, Snider W (2010) Initiating and growing an axon. Cold Spring Harb Perspect Biol 2(4):a001925.
15. Dotti CG, Banker GA (1987) Experimentally induced alteration in the polarity of developing neurons. Nature 330(6145):254-256.
16. Insolera R, Chen S, Shi SH (2011) Par proteins and neuronal polarity. Dev Neurobiol 71(6):483-494.
17. Cheng PL, Poo MM (2012) Early events in axon/dendrite polarization. Annu Rev Neurosci 35:181-201.
18. Wiggin GR, Fawcett JP, Pawson T (2005) Polarity proteins in axon specification and synaptogenesis. Dev Cell 8(6):803-816.
19. Barnes AP, Polleux F (2009) Establishment of axon-dendrite polarity in developing neurons. Annu Rev Neurosci 32:347-381.
20. Shi SH, Jan LY, Jan YN (2003) Hippocampal neuronal polarity specified by spatially localized mPar3/mPar6 and PI 3-kinase activity. Cell 112(1):63-75.
21. Wu-Zhang AX, Schramm CL, Nabavi S, Malinow R, Newton AC (2012) Cellular pharmacology of protein kinase Mζ (PKMζ) contrasts with its in vitro profile: Implications for PKMζ as a mediator of memory. J Biol Chem 287(16):12879-12885.
22. Volk LJ, Bachman JL, Johnson R, Yu Y, Huganir RL (2013) PKM-ζ is not required for hippocampal synaptic plasticity, learning and memory. Nature 493(7432):420-423.
23. Lee AM, et al. (2013) Prkcz null mice show normal learning and memory. Nature 493(7432):416-419.
24. Zhang X, et al. (2007) Dishevelled promotes axon differentiation by regulating atypical protein kinase C. Nat Cell Biol 9(7):743-754.
25. Chen YM, et al. (2006) Microtubule affinity-regulating kinase 2 functions downstream of the PAR-3/PAR-6/atypical PKC complex in regulating hippocampal neuronal polarity. Proc Natl Acad Sci USA 103(22):8534-8539.
26. Jiang X, Naik MU, Hrabe J, Sacktor TC (1994) Developmental expression of the protein kinase C family in rat hippocampus. Brain Res Dev Brain Res 78(2):291-295.
27. Schwamborn JC, Püschel AW (2004) The sequential activity of the GTPases Rap1B and Cdc42 determines neuronal polarity. Nat Neurosci 7(9):923-929.
28. Zhang H, Macara IG (2008) The PAR-6 polarity protein regulates dendritic spine morphogenesis through p190 RhoGAP and the Rho GTPase. Dev Cell 14(2):216-226.
29. Zhang H, Macara IG (2006) The polarity protein PAR-3 and TIAM1 cooperate in dendritic spine morphogenesis. Nat Cell Biol 8(3):227-237.
30. Ruiz-Canada C, et al. (2004) New synaptic bouton formation is disrupted by misregulation of microtubule stability in aPKC mutants. Neuron 42(4):567-580.
31. Nagai-Tamai Y, Mizuno K, Hirose T, Suzuki A, Ohno S (2002) Regulated proteinprotein interaction between aPKC and PAR-3 plays an essential role in the polarization of epithelial cells. Genes Cells 7(11):1161-1171.
32. Wang C, Shang Y, Yu J, Zhang M (2012) Substrate recognition mechanism of atypical protein kinase Cs revealed by the structure of PKCι{phonetic} in complex with a substrate peptide from Par-3. Structure 20(5):791-801.
33. Chau AH, Walter JM, Gerardin J, Tang C, Lim WA (2012) Designing synthetic regulatory networks capable of self-organizing cell polarization. Cell 151(2):320-332.
34. Howell AS, et al. (2012) Negative feedback enhances robustness in the yeast polarity establishment circuit. Cell 149(2):322-333.
35. Fletcher GC, Lucas EP, Brain R, Tournier A, Thompson BJ (2012) Positive feedback and mutual antagonism combine to polarize Crumbs in the Drosophila follicle cell epithelium. Curr Biol 22(12):1116-1122.
36. Chen S, et al. (2013) Regulation of microtubule stability and organization by mammalian Par3 in specifying neuronal polarity. Dev Cell 24(1):26-40.
37. Rolls MM, Doe CQ (2004) Baz, Par-6 and aPKC are not required for axon or dendrite specification in Drosophila. Nat Neurosci 7(12):1293-1295.
38. Imai F, et al. (2006) Inactivation of aPKClambda results in the loss of adherens junctions in neuroepithelial cells without affecting neurogenesis in mouse neocortex. Development 133(9):1735-1744.
39. Faulkner RL, Low LK, Cheng HJ (2007) Axon pruning in the developing vertebrate hippocampus. Dev Neurosci 29(1-2):6-13.
40. Luo L, O'Leary DD (2005) Axon retraction and degeneration in development and disease. Annu Rev Neurosci 28:127-156.
41. Fievet BT, et al. (2013) Systematic genetic interaction screens uncover cell polarity regulators and functional redundancy. Nat Cell Biol 15(1):103-112.
42. Smith L, et al. (2000) Activation of atypical protein kinase C zeta by caspase processing and degradation by the ubiquitin-proteasome system. J Biol Chem 275(51): 40620-40627.
43. Frutos S, Moscat J, Diaz-Meco MT (1999) Cleavage of zetaPKC but not lambda/iotaPKC by caspase-3 during UV-induced apoptosis. J Biol Chem 274(16):10765-10770.
44. Kaech S, Banker G (2006) Culturing hippocampal neurons. Nat Protoc 1(5):2406-2415.
45. Zheng L, Baumann U, Reymond JL (2004) An efficient one-step site-directed and sitesaturation mutagenesis protocol. Nucleic Acids Res 32(14):e115.
46. James P, Halladay J, Craig EA (1996) Genomic libraries and a host strain designed for highly efficient two-hybrid selection in yeast. Genetics 144(4):1425-1436.