A variable cytoplasmic domain segment is necessary for γ- protocadherin trafficking and tubulation in the endosome/lysosome pathway

Molecular Biology of the Cell

Volumn 22, Issue 22, 2011, Pages 4362-4372

  O'Leary, Robert ^a   Reilly, James E ^a   Hanson, Hugo H ^a   Kang, Semie ^a   Lou, Nicole ^a   Phillips, Greg R ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; CADHERIN; GAMMA PROTOCADHERIN; NERVE CELL ADHESION MOLECULE; UNCLASSIFIED DRUG;

ARTICLE; CELL DEATH; CELL INTERACTION; CELL MIGRATION; CELL ORGANELLE; CYTOPLASM; ENDOSOME; GENE CLUSTER; GENE DELETION; IN VIVO STUDY; LYSOSOME; PRIORITY JOURNAL;

ANIMALS; CADHERINS; CELL COMMUNICATION; CELL LINE; ENDOSOMES; HEK293 CELLS; HUMANS; LYSOSOMES; MICE; MULTIGENE FAMILY; NERVOUS SYSTEM; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT;

MUS;

EID: 81755161562     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E11-04-0283     Document Type: Article

References (39)

1. Aberle H, Schwartz H, Kemler R (1996). Cadherin-catenin complex: protein interactions and their implications for cadherin function. J Cell Biochem 61, 514-523. (Pubitemid 26240128)
2. Boya P, Andreau K, Poncet D, Zamzami N, Perfettini JL, Metivier D, Ojcius DM, Jaattela M, Kroemer G (2003). Lysosomal membrane permeabilization induces cell death in a mitochondrion-dependent fashion. J Exp Med 197, 1323-1334. (Pubitemid 36617779)
3. Buchanan SM, Schalm SS, Maniatis T (2010). Proteolytic processing of protocadherin proteins requires endocytosis. Proc Natl Acad Sci USA 107, 17774-17779.
4. Chen J, Lu Y, Meng S, Han MH, Lin C, Wang X (2009). alpha- and gamma-Protocadherins negatively regulate PYK2. J Biol Chem 284, 2880-2890.
5. Fernandez-Monreal M, Kang S, Phillips GR (2009). gamma-Protocadherin homophilic interaction and intracellular trafficking is controlled by the cytoplasmic domain in neurons. Mol Cell Neurosci 40, 344-353.
6. Fernandez-Monreal M, Oung T, Hanson HH, O'Leary R, Janssen WG, Dolios G, Wang R, Phillips GR (2010). gamma-Protocadherins are enriched and transported in specialized vesicles associated with the secretory pathway in neurons. Eur J Neurosci 32, 921-931.
7. Gorski JA, Gomez LL, Scott JD, Dell'Acqua ML (2005). Association of an A-kinase-anchoring protein signaling scaffold with cadherin adhesion molecules in neurons and epithelial cells. Mol Biol Cell 16, 3574-3590. (Pubitemid 41077071)
8. Gyrd-Hansen M et al. (2006). Apoptosome-independent activation of the lysosomal cell death pathway by caspase-9. Mol Cell Biol 26, 7880-7891. (Pubitemid 44630989)
9. Haas IG, Frank M, Veron N, Kemler R (2005). Presenilin-dependent processing and nuclear function of gamma-protocadherins. J Biol Chem 280, 9313-9319. (Pubitemid 40409624)
10. Han MH, Lin C, Meng S, Wang X (2010). Proteomics analysis reveals overlapping functions of clustered protocadherins. Mol Cell Proteomics 9, 71-83.
11. Hanson HH, Kang S, Fernandez-Monreal M, Oung T, Yildirim M, Lee R, Suyama K, Hazan RB, Phillips GR (2010a). LC3-dependent intracellular membrane tubules induced by gamma-protocadherins A3 and B2: A role for intraluminal interactions. J Biol Chem 285, 20982-20992.
12. Hanson HH, Reilly JE, Lee R, Janssen WG, Phillips GR (2010b). Streamlined embedding of cell monolayers on gridded live imaging dishes for correlative light and electron microscopy. Microsc Microanal 20, 1-8.
13. Jaattela M, Cande C, Kroemer G (2004). Lysosomes and mitochondria in the commitment to apoptosis: a potential role for cathepsin D and AIF. Cell Death Differ 11, 135-136. (Pubitemid 38159636)
14. Katori S, Hamada S, Noguchi Y, Fukuda E, Yamamoto T, Yamamoto H, Hasegawa S, Yagi T (2009). Protocadherin-alpha family is required for serotonergic projections to appropriately innervate target brain areas. J Neurosci 29, 9137-9147.
15. Kohmura N, Senzaki K, Hamada S, Kai N, Yasuda R, Watanabe M, Ishii H, Yasuda M, Mishina M, Yagi T (1998). Diversity revealed by a novel family of cadherins expressed in neurons at a synaptic complex. Neuron 20, 1137-1151. (Pubitemid 28293131)
16. Kreuzaler PA, Staniszewska AD, Li W, Omidvar N, Kedjouar B, Turkson J, Poli V, Flavell RA, Clarkson RW, Watson CJ (2011). Stat3 controls lysosomal-mediated cell death in vivo. Nat Cell Biol 13, 303-309.
17. Kroemer G, Jaattela M (2005). Lysosomes and autophagy in cell death control. Nat Rev Cancer 5, 886-897. (Pubitemid 41746033)
18. Lee JH et al. (2010). Lysosomal proteolysis and autophagy require presenilin 1 and are disrupted by Alzheimer-related PS1 mutations. Cell 141, 1146-1158.
19. Lefebvre JL, Zhang Y, Meister M, Wang X, Sanes JR (2008). γ-Protocadherins regulate neuronal survival but are dispensable for circuit formation in retina. Development 135, 4141-4151.
20. Lin C, Meng S, Zhu T, Wang X (2010). PDCD10/CCM3 acts downstream of γ-protocadherins to regulate neuronal survival. J Biol Chem 285, 41675-41685.
21. Lingwood D, Schuck S, Ferguson C, Gerl MJ, Simons K (2009). Generation of cubic membranes by controlled homotypic interaction of membrane proteins in the endoplasmic reticulum. J Biol Chem 284, 12041-12048.
22. Mironov AA, Beznoussenko GV (2009). Correlative microscopy: a potent tool for the study of rare or unique cellular and tissue events. J Microsc 235, 308-321.
23. Mutoh T, Hamada S, Senzaki K, Murata Y, Yagi T (2004). Cadherin-related neuronal receptor 1 (CNR1) has cell adhesion activity with beta1 integrin mediated through the RGD site of CNR1. Exp Cell Res 294, 494-508. (Pubitemid 38326747)
24. Nixon RA, Yang DS, Lee JH (2008). Neurodegenerative lysosomal disorders: a continuum from development to late age. Autophagy 4, 590-599.
25. Nose A, Nagafuchi A, Takeichi M (1988). Expressed recombinant cadherins mediate cell sorting in model systems. Cell 54, 993-1001.
26. Obata S, Sago H, Mori N, Rochelle JM, Seldin MF, Davidson M, St John T, Taketani S, Suzuki ST (1995). Protocadherin Pcdh2 shows properties similar to, but distinct from, those of classical cadherins. J Cell Sci 108, 3765-3773. (Pubitemid 26004029)
27. Phillips GR et al. (2001). The presynaptic particle web: ultrastructure, composition, dissolution, and reconstitution. Neuron 32, 63-77. (Pubitemid 32995890)
28. Phillips GR, Tanaka H, Frank M, Elste A, Fidler L, Benson DL, Colman DR (2003). Gamma-protocadherins are targeted to subsets of synapses and intracellular organelles in neurons. J Neurosci 23, 5096-5104. (Pubitemid 36793237)
29. Polishchuk RS, Polishchuk EV, Marra P, Alberti S, Buccione R, Luini A, Mironov AA (2000). Correlative light-electron microscopy reveals the tubular-saccular ultrastructure of carriers operating between Golgi apparatus and plasma membrane. J Cell Biol 148, 45-58. (Pubitemid 30046781)
30. Prasad T, Wang X, Gray PA, Weiner JA (2008). A differential developmental pattern of spinal interneuron apoptosis during synaptogenesis: insights from genetic analyses of the protocadherin-γ gene cluster. Development 135, 4153-4164.
31. Razi M, Tooze SA (2009). Correlative light and electron microscopy. Methods Enzymol 452, 261-275.
32. Reilly JE, Hanson HH, Phillips GR (2011). Persistence of excitatory shaft synapses adjacent to newly emerged dendritic protrusions. Mol Cell Neurosci 48, 129-136.
33. Schalm SS, Ballif BA, Buchanan SM, Phillips GR, Maniatis T (2010). Phosphorylation of protocadherin proteins by the receptor tyrosine kinase Ret. Proc Natl Acad Sci USA 107, 13894-13899.
34. Schreiner D, Weiner JA (2010). Combinatorial homophilic interaction between gamma-protocadherin multimers greatly expands the molecular diversity of cell adhesion. Proc Natl Acad Sci USA 107, 14893-14898.
35. Su H, Marcheva B, Meng S, Liang FA, Kohsaka A, Kobayashi Y, Xu AW, Bass J, Wang X (2010). Gamma-protocadherins regulate the functional integrity of hypothalamic feeding circuitry in mice. Dev Biol 339, 38-50.
36. Tasic B, Nabholz CE, Baldwin KK, Kim Y, Rueckert EH, Ribich SA, Cramer P, Wu Q, Axel R, Maniatis T (2002). Promoter choice determines splice site selection in protocadherin alpha and gamma pre-mRNA splicing. Mol Cell 10, 21-33. (Pubitemid 34876561)
37. Wang X, Weiner JA, Levi S, Craig AM, Bradley A, Sanes JR (2002). Gamma protocadherins are required for survival of spinal interneurons. Neuron 36, 843-854. (Pubitemid 35447856)
38. Weiner JA, Wang X, Tapia JC, Sanes JR (2005). Gamma protocadherins are required for synaptic development in the spinal cord. Proc Natl Acad Sci USA 102, 8-14. (Pubitemid 40094419)
39. Wu Q, Maniatis T (1999). A striking organization of a large family of human neural cadherin-like cell adhesion genes. Cell 97, 779-790. (Pubitemid 29278051)