The Non-Canonical Wnt/PKC Pathway Regulates Mitochondrial Dynamics through Degradation of the Arm-Like Domain-Containing Protein Alex3

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Serrat, Román ^a,b   López Doménech, Guillermo ^a,b   Mirra, Serena ^a,b   Quevedo, Martí ^a,b   Garcia Fernàndez, Jordi ^a   Ulloa, Fausto ^a,b   Burgaya, Ferrán ^a,b   Soriano, Eduardo ^a,b,c  

^a UNIVERSITY OF BARCELONA   (Spain)

^b CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED SOBRE ENFERMEDADES NEURODEGENERATIVAS CIBERNED   (Spain)

^c Instituto de Salud Carlos III   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN ALEX3; PROTEIN KINASE C; UNCLASSIFIED DRUG; WNT PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; CELL AGGREGATION; CELL MIGRATION; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; MITOCHONDRIAL DYNAMICS; PHENOTYPE; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN TARGETING; WNT SIGNALING PATHWAY;

AMINO ACID MOTIFS; ARMADILLO DOMAIN PROTEINS; GENE EXPRESSION REGULATION; GENES, REPORTER; GREEN FLUORESCENT PROTEINS; HEK293 CELLS; HUMANS; MITOCHONDRIA; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL PROTEINS; MOLECULAR SEQUENCE DATA; NAPHTHALENES; PROTEIN KINASE C; PROTEIN KINASE INHIBITORS; PROTEIN STABILITY; PROTEIN STRUCTURE, TERTIARY; PROTEOLYSIS; WNT PROTEINS; WNT SIGNALING PATHWAY;

EID: 84879744840     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0067773     Document Type: Article

References (56)

1. Nicholls DG, Budd SL, (2000) Mitochondria and neuronal survival. Physiol Rev 80: 315-360.
2. Chen H, Chan DC, (2009) Mitochondrial dynamics-fusion, fission, movement, and mitophagy-in neurodegenerative diseases. Hum Mol Genet 18: R169-176.
3. Han XJ, Tomizawa K, Fujimura A, Ohmori I, Nishiki T, et al. (2010) Regulation of mitochondrial dynamics and neurodegenerative diseases. Acta Med Okayama 65: 1-10.
4. Schon EA, Przedborski S, (2011) Mitochondria: the next (neurode)generation. Neuron 70: 1033-1053.
5. Lopez-Domenech G, Serrat R, Mirra S, D'Aniello S, Somorjai I, et al. (2012) The Eutherian Armcx genes regulate mitochondrial trafficking in neurons and interact with Miro and Trak2. Nat Commun 3: 814.
6. Hollenbeck PJ, Saxton WM, (2005) The axonal transport of mitochondria. J Cell Sci 118: 5411-5419.
7. Hollenbeck PJ, (1996) The pattern and mechanism of mitochondrial transport in axons. Front Biosci 1: d91-102.
8. MacAskill AF, Kittler JT, (2010) Control of mitochondrial transport and localization in neurons. Trends Cell Biol 20: 102-112.
9. Kurochkin IV, Yonemitsu N, Funahashi SI, Nomura H, (2001) ALEX1, a novel human armadillo repeat protein that is expressed differentially in normal tissues and carcinomas. Biochem Biophys Res Commun 280: 340-347.
10. Garcia-Frigola C, Burgaya F, Calbet M, Lopez-Domenech G, de Lecea L, et al. (2004) A collection of cDNAs enriched in upper cortical layers of the embryonic mouse brain. Brain Res Mol Brain Res 122: 133-150.
11. Mou Z, Tapper AR, Gardner PD, (2009) The Armadillo Repeat-containing Protein, ARMCX3, Physically and Functionally Interacts with the Developmental Regulatory Factor Sox10. J Biol Chem 284: 13629-13640.
12. Li Z, Okamoto K, Hayashi Y, Sheng M, (2004) The importance of dendritic mitochondria in the morphogenesis and plasticity of spines and synapses. Cell 119: 873-887.
13. Rintoul GL, Filiano AJ, Brocard JB, Kress GJ, Reynolds IJ, (2003) Glutamate decreases mitochondrial size and movement in primary forebrain neurons. J Neurosci 23: 7881-7888.
14. MacAskill AF, Rinholm JE, Twelvetrees AE, Arancibia-Carcamo IL, Muir J, et al. (2009) Miro1 is a calcium sensor for glutamate receptor-dependent localization of mitochondria at synapses. Neuron 61: 541-555.
15. Chen S, Owens GC, Crossin KL, Edelman DB, (2007) Serotonin stimulates mitochondrial transport in hippocampal neurons. Mol Cell Neurosci 36: 472-483.
16. Chen S, Owens GC, Edelman DB, (2008) Dopamine inhibits mitochondrial motility in hippocampal neurons. PLoS One 3: e2804.
17. Chada SR, Hollenbeck PJ, (2003) Mitochondrial movement and positioning in axons: the role of growth factor signaling. J Exp Biol 206: 1985-1992.
18. van Amerongen R, Nusse R, (2009) Towards an integrated view of Wnt signaling in development. Development 136: 3205-3214.
19. Nusse R, (2005) Wnt signaling in disease and in development. Cell Res 15: 28-32.
20. Smalley MJ, Dale TC, (1999) Wnt signalling in mammalian development and cancer. Cancer Metastasis Rev 18: 215-230.
21. Gavel Y, von Heijne G, (1990) Cleavage-site motifs in mitochondrial targeting peptides. Protein Eng 4: 33-37.
22. Mezhybovska M, Yudina Y, Abhyankar A, Sjolander A, (2009) Beta-catenin is involved in alterations in mitochondrial activity in non-transformed intestinal epithelial and colon cancer cells. Br J Cancer 101: 1596-1605.
23. Brocardo M, Lei Y, Tighe A, Taylor SS, Mok MT, et al. (2008) Mitochondrial targeting of adenomatous polyposis coli protein is stimulated by truncating cancer mutations: regulation of Bcl-2 and implications for cell survival. J Biol Chem 283: 5950-5959.
24. Liu C, Li Y, Semenov M, Han C, Baeg GH, et al. (2002) Control of beta-catenin phosphorylation/degradation by a dual-kinase mechanism. Cell 108: 837-847.
25. Yi M, Weaver D, Hajnoczky G, (2004) Control of mitochondrial motility and distribution by the calcium signal: a homeostatic circuit. J Cell Biol 167: 661-672.
26. Chan DC, (2006) Mitochondrial fusion and fission in mammals. Annu Rev Cell Dev Biol 22: 79-99.
27. Misko A, Jiang S, Wegorzewska I, Milbrandt J, Baloh RH, (2010) Mitofusin 2 is necessary for transport of axonal mitochondria and interacts with the Miro/Milton complex. J Neurosci 30: 4232-4240.
28. Saotome M, Safiulina D, Szabadkai G, Das S, Fransson A, et al. (2008) Bidirectional Ca2+-dependent control of mitochondrial dynamics by the Miro GTPase. Proc Natl Acad Sci U S A 105: 20728-20733.
29. Verstreken P, Ly CV, Venken KJ, Koh TW, Zhou Y, et al. (2005) Synaptic mitochondria are critical for mobilization of reserve pool vesicles at Drosophila neuromuscular junctions. Neuron 47: 365-378.
30. Winter EE, Ponting CP, (2005) Mammalian BEX, WEX and GASP genes: coding and non-coding chimaerism sustained by gene conversion events. BMC Evol Biol 5: 54.
31. McMahon AP, Moon RT, (1989) Ectopic expression of the proto-oncogene int-1 in Xenopus embryos leads to duplication of the embryonic axis. Cell 58: 1075-1084.
32. Wong GT, Gavin BJ, McMahon AP, (1994) Differential transformation of mammary epithelial cells by Wnt genes. Mol Cell Biol 14: 6278-6286.
33. Mikels AJ, Nusse R, (2006) Purified Wnt5a protein activates or inhibits beta-catenin-TCF signaling depending on receptor context. PLoS Biol 4: e115.
34. Samarzija I, Sini P, Schlange T, Macdonald G, Hynes NE, (2009) Wnt3a regulates proliferation and migration of HUVEC via canonical and non-canonical Wnt signaling pathways. Biochem Biophys Res Commun 386: 449-454.
35. Olsen JV, Blagoev B, Gnad F, Macek B, Kumar C, et al. (2006) Global, in vivo, and site-specific phosphorylation dynamics in signaling networks. Cell 127: 635-648.
36. Youle RJ, Narendra DP, (2011) Mechanisms of mitophagy. Nat Rev Mol Cell Biol 12: 9-14.
37. Kinoshita N, Iioka H, Miyakoshi A, Ueno N, (2003) PKC delta is essential for Dishevelled function in a noncanonical Wnt pathway that regulates Xenopus convergent extension movements. Genes Dev 17: 1663-1676.
38. Kowalczyk JE, Beresewicz M, Gajkowska B, Zablocka B, (2009) Association of protein kinase C delta and phospholipid scramblase 3 in hippocampal mitochondria correlates with neuronal vulnerability to brain ischemia. Neurochem Int 55: 157-163.
39. Dempsey EC, Newton AC, Mochly-Rosen D, Fields AP, Reyland ME, et al. (2000) Protein kinase C isozymes and the regulation of diverse cell responses. Am J Physiol Lung Cell Mol Physiol 279: L429-438.
40. Spinsanti P, De Vita T, Caruso A, Melchiorri D, Misasi R, et al. (2008) Differential activation of the calcium/protein kinase C and the canonical beta-catenin pathway by Wnt1 and Wnt7a produces opposite effects on cell proliferation in PC12 cells. J Neurochem 104: 1588-1598.
41. Yu JM, Kim JH, Song GS, Jung JS, (2006) Increase in proliferation and differentiation of neural progenitor cells isolated from postnatal and adult mice brain by Wnt-3a and Wnt-5a. Mol Cell Biochem 288: 17-28.
42. Koyanagi M, Iwasaki M, Haendeler J, Leitges M, Zeiher AM, et al. (2009) Wnt5a increases cardiac gene expressions of cultured human circulating progenitor cells via a PKC delta activation. PLoS One 4: e5765.
43. Santos A, Bakker AD, de Blieck-Hogervorst JM, Klein-Nulend J, (2010) WNT5A induces osteogenic differentiation of human adipose stem cells via rho-associated kinase ROCK. Cytotherapy 12: 924-932.
44. Liang H, Coles AH, Zhu Z, Zayas J, Jurecic R, et al. (2007) Noncanonical Wnt signaling promotes apoptosis in thymocyte development. J Exp Med 204: 3077-3084.
45. Zhang X, Zhu J, Yang GY, Wang QJ, Qian L, et al. (2007) Dishevelled promotes axon differentiation by regulating atypical protein kinase C. Nat Cell Biol. 9: 743-754.
46. Luna-Ulloa LB, Hernandez-Maqueda JG, Castaneda-Patlan MC, Robles-Flores M, (2011) Protein kinase C in Wnt signaling: Implications in cancer initiation and progression. IUBMB Life 63: 873-879.
47. Lee JM, Kim IS, Kim H, Lee JS, Kim K, et al. (2010) RORalpha attenuates Wnt/beta-catenin signaling by PKCalpha-dependent phosphorylation in colon cancer. Mol Cell 37: 183-195.
48. Dissanayake SK, Wade M, Johnson CE, O'Connell MP, Leotlela PD, et al. (2007) The Wnt5A/protein kinase C pathway mediates motility in melanoma cells via the inhibition of metastasis suppressors and initiation of an epithelial to mesenchymal transition. J Biol Chem 282: 17259-17271.
49. Medrano EE, (2007) Wnt5a and PKC, a deadly partnership involved in melanoma invasion. Pigment Cell Res 20: 258-259.
50. Morin PJ, Sparks AB, Korinek V, Barker N, Clevers H, et al. (1997) Activation of beta-catenin-Tcf signaling in colon cancer by mutations in beta-catenin or APC. Science 275: 1787-1790.
51. Chang DT, Reynolds IJ, (2006) Mitochondrial trafficking and morphology in healthy and injured neurons. Prog Neurobiol 80: 241-268.
52. Liu X, Hajnoczky G, (2009) Ca2+-dependent regulation of mitochondrial dynamics by the Miro-Milton complex. Int J Biochem Cell Biol 41: 1972-1976.
53. An JH, Yang JY, Ahn BY, Cho SW, Jung JY, et al. (2010) Enhanced mitochondrial biogenesis contributes to Wnt induced osteoblastic differentiation of C3H10T1/2 cells. Bone 47: 140-150.
54. Yoon JC, Ng A, Kim BH, Bianco A, Xavier RJ, et al. (2010) Wnt signaling regulates mitochondrial physiology and insulin sensitivity. Genes Dev 24: 1507-1518.
55. Deng L, Hu S, Baydoun AR, Chen J, Chen X, et al. (2009) Aspirin induces apoptosis in mesenchymal stem cells requiring Wnt/beta-catenin pathway. Cell Prolif 42: 721-730.
56. Wang Z, Havasi A, Gall JM, Mao H, Schwartz JH, et al. (2009) Beta-catenin promotes survival of renal epithelial cells by inhibiting Bax. J Am Soc Nephrol 20: 1919-1928.