Information
References
Contents
Download
[1]A. Du Toit: Endocytosis. A new gateway into cells. Nat Rev Mol Cell Biol, 16(2), 68 (2015)
[2]H. T. McMahon and E. Boucrot: Molecular mechanism and physiological functions of clathrin-mediated endocytosis. Nat Rev Mol Cell Biol, 12(8), 517-33 (2011)
[3]Z. J. Cheng, R. D. Singh, D. L. Marks and R. E. Pagano: Membrane microdomains, caveolae, and caveolar endocytosis of sphingolipids. Mol Membr Biol, 23(1), 101-10 (2006)
[4]R. C. Aguilar and B. Wendland: Endocytosis of membrane receptors: two pathways are better than one. Proc Natl Acad Sci U S A, 102(8), 2679-80 (2005)
[5]G. Kourouniotis, Y. Wang, S. Pennock, X. Chen and Z. Wang: Non-Ligand-Induced Dimerization is Sufficient to Initiate the Signalling and Endocytosis of EGF Receptor. Int J Mol Sci, 17(8) (2016)
[6]D. P. Poole and N. W. Bunnett: G Protein-Coupled Receptor Trafficking and Signalling in the Enteric Nervous System: The Past, Present and Future. Adv Exp Med Biol, 891, 145-52 (2016)
[7]H. Cao, X. Yin, Y. Cao, Y. Jin, S. Wang, Y. Kong, Y. Chen, J. Gao, S. Heller and Z. Xu: FCHSD1 and FCHSD2 are expressed in hair cell stereocilia and cuticular plate and regulate actin polymerization in vitro. PLoS One, 8(2), e56516 (2013)
[8]W. M. Henne, E. Boucrot, M. Meinecke, E. Evergren, Y. Vallis, R. Mittal and H. T. McMahon: FCHo proteins are nucleators of clathrin-mediated endocytosis. Science, 328(5983), 1281-4 (2010)
[9]X. Huang, R. Gong, X. Li, A. Virtue, F. Yang, I. H. Yang, A. H. Tran, X. F. Yang and H. Wang: Identification of novel pretranslational regulatory mechanisms for NF-kappaB activation. J Biol Chem, 288(22), 15628-40 (2013)
[10]N. C. Chen, F. Yang, L. M. Capecci, Z. Gu, A. I. Schafer, W. Durante, X. F. Yang and H. Wang: Regulation of homocysteine metabolism and methylation in human and mouse tissues. FASEB J, 24(8), 2804-17 (2010)
[11]X. Li, J. Mai, A. Virtue, Y. Yin, R. Gong, X. Sha, S. Gutchigian, A. Frisch, I. Hodge, X. Jiang, H. Wang and X. F. Yang: IL-35 is a novel responsive anti-inflammatory cytokine--a new system of categorizing anti-inflammatory cytokines. PLoS One, 7(3), e33628 (2012)
[12]H. Iioka and I. G. Macara: Detection of RNA-Protein Interactions Using Tethered RNA Affinity Capture. Methods Mol Biol, 1316, 67-73 (2015)
[13]M. Barrios-Rodiles, K. R. Brown, B. Ozdamar, R. Bose, Z. Liu, R. S. Donovan, F. Shinjo, Y. Liu, J. Dembowy, I. W. Taylor, V. Luga, N. Przulj, M. Robinson, H. Suzuki, Y. Hayashizaki, I. Jurisica and J. L. Wrana: High-throughput mapping of a dynamic signaling network in mammalian cells. Science, 307(5715), 1621-5 (2005)
[14]M. Kotlyar, C. Pastrello, F. Pivetta, A. Lo Sardo, C. Cumbaa, H. Li, T. Naranian, Y. Niu, Z. Ding, F. Vafaee, F. Broackes-Carter, J. Petschnigg, G. B. Mills, A. Jurisicova, I. Stagljar, R. Maestro and I. Jurisica: In silico prediction of physical protein interactions and characterization of interactome orphans. Nat Methods, 12(1), 79-84 (2015)
[15]Z. Lu and T. Hunter: Degradation of activated protein kinases by ubiquitination. Annu Rev Biochem, 78, 435-75 (2009)
[16]M. Galovic, D. Xu, L. B. Areces, R. van der Kammen and M. Innocenti: Interplay between N-WASP and CK2 optimizes clathrin-mediated endocytosis of EGFR. J Cell Sci, 124(Pt 12), 2001-12 (2011)
[17]R. B. Jones, A. Gordus, J. A. Krall and G. MacBeath: A quantitative protein interaction network for the ErbB receptors using protein microarrays. Nature, 439(7073), 168-74 (2006)
[18]J. Tong, P. Taylor, S. M. Peterman, A. Prakash and M. F. Moran: Epidermal growth factor receptor phosphorylation sites Ser991 and Tyr998 are implicated in the regulation of receptor endocytosis and phosphorylations at Ser1039 and Thr1041. Mol Cell Proteomics, 8(9), 2131-44 (2009)
[19]F. Bornke: Corrigendum: The complex becomes more complex: protein-protein interactions of SnRK1 with DUF581 family proteins provide a framework for cell- and stimulus type-specific SnRK1 signaling in plants. Front Plant Sci, 5, 693 (2014)
[20]X. Tang, X. Hu, X. Yang, Y. Fan, Y. Li, W. Hu, Y. Liao, M. C. Zheng, W. Peng and L. Gao: Predicting diabetes mellitus genes via protein-protein interaction and protein subcellular localization information. BMC Genomics, 17 Suppl 4, 433 (2016)
[21]B. Pyrzynska, I. Pilecka and M. Miaczynska: Endocytic proteins in the regulation of nuclear signaling, transcription and tumorigenesis. Mol Oncol, 3(4), 321-38 (2009)
[22]Y. Mosesson, K. Shtiegman, M. Katz, Y. Zwang, G. Vereb, J. Szollosi and Y. Yarden: Endocytosis of receptor tyrosine kinases is driven by monoubiquitylation, not polyubiquitylation. J Biol Chem, 278(24), 21323-6 (2003)
[23]C. Le Roy and J. L. Wrana: Clathrin- and non-clathrin-mediated endocytic regulation of cell signalling. Nat Rev Mol Cell Biol, 6(2), 112-26 (2005)
[24]C. Basquin, M. Trichet, H. Vihinen, V. Malarde, T. Lagache, L. Ripoll, E. Jokitalo, J. C. Olivo-Marin, A. Gautreau and N. Sauvonnet: Membrane protrusion powers clathrin-independent endocytosis of interleukin-2 receptor. EMBO J, 34(16), 2147-61 (2015)
[25]S. Liu, X. Xiong, X. Zhao, X. Yang and H. Wang: F-BAR family proteins, emerging regulators for cell membrane dynamic changes-from structure to human diseases. J Hematol Oncol, 8, 47 (2015)
[26]I. K. Jarsch, F. Daste and J. L. Gallop: Membrane curvature in cell biology: An integration of molecular mechanisms. J Cell Biol, 214(4), 375-87 (2016)
[27]R. Sousa, H. S. Liao, J. Cuellar, S. Jin, J. M. Valpuesta, A. J. Jin and E. M. Lafer: Clathrin-coat disassembly illuminates the mechanisms of Hsp70 force generation. Nat Struct Mol Biol, 23(9), 821-9 (2016)
[28]J. Hu, F. Troglio, A. Mukhopadhyay, S. Everingham, E. Kwok, G. Scita and A. W. Craig: F-BAR-containing adaptor CIP4 localizes to early endosomes and regulates Epidermal Growth Factor Receptor trafficking and downregulation. Cell Signal, 21(11), 1686-97 (2009)
[29]E. E. Mulkearns and J. A. Cooper: FCH domain only-2 organizes clathrin-coated structures and interacts with Disabled-2 for low-density lipoprotein receptor endocytosis. Mol Biol Cell, 23(7), 1330-42 (2012)
[30]B. J. de Kreuk, E. C. Anthony, D. Geerts and P. L. Hordijk: The F-BAR protein PACSIN2 regulates epidermal growth factor receptor internalization. J Biol Chem, 287(52), 43438-53 (2012)
[31]K. M. Cooper, D. A. Bennin and A. Huttenlocher: The PCH family member proline-serine-threonine phosphatase-interacting protein 1 targets to the leukocyte uropod and regulates directed cell migration. Mol Biol Cell, 19(8), 3180-91 (2008)
[32]S. Liu, X. Xiong, S. V. Thomas, Y. Xu, X. Cheng, X. Zhao, X. Yang and H. Wang: Analysis for Carom complex, signaling and function by database mining. Front Biosci (Landmark Ed), 21, 856-72 (2016)
[33]I. Kovacevic, J. Hu, A. Siehoff-Icking, N. Opitz, A. Griffin, A. C. Perkins, A. L. Munn, W. Muller-Esterl, R. Popp, I. Fleming, B. Jungblut, M. Hoffmeister and S. Oess: The F-BAR protein NOSTRIN participates in FGF signal transduction and vascular development. EMBO J, 31(15), 3309-22 (2012)
[34]J. Modregger, B. Ritter, B. Witter, M. Paulsson and M. Plomann: All three PACSIN isoforms bind to endocytic proteins and inhibit endocytosis. J Cell Sci, 113 Pt 24, 4511-21 (2000)
[35]A. A. Bizet, K. Liu, N. Tran-Khanh, A. Saksena, J. Vorstenbosch, K. W. Finnson, M. D. Buschmann and A. Philip: The TGF-beta co-receptor, CD109, promotes internalization and degradation of TGF-beta receptors. Biochim Biophys Acta, 1813(5), 742-53 (2011)
[36]M. Chandra, S. Zang, H. Li, L. J. Zimmerman, J. Champer, A. Tsuyada, A. Chow, W. Zhou, Y. Yu, H. Gao, X. Ren, R. J. Lin and S. E. Wang: Nuclear translocation of type I transforming growth factor beta receptor confers a novel function in RNA processing. Mol Cell Biol, 32(12), 2183-95 (2012)
[37]H. A. Alwan, E. J. van Zoelen and J. E. van Leeuwen: Ligand-induced lysosomal epidermal growth factor receptor (EGFR) degradation is preceded by proteasome-dependent EGFR de-ubiquitination. J Biol Chem, 278(37), 35781-90 (2003)
[38]Y. N. Wang and M. C. Hung: Nuclear functions and subcellular trafficking mechanisms of the epidermal growth factor receptor family. Cell Biosci, 2(1), 13 (2012)
[39]G. Levkowitz, H. Waterman, E. Zamir, Z. Kam, S. Oved, W. Y. Langdon, L. Beguinot, B. Geiger and Y. Yarden: c-Cbl/Sli-1 regulates endocytic sorting and ubiquitination of the epidermal growth factor receptor. Genes Dev, 12(23), 3663-74 (1998)
[40]X. Long and K. P. Nephew: Fulvestrant (ICI 182,780)-dependent interacting proteins mediate immobilization and degradation of estrogen receptor-alpha. J Biol Chem, 281(14), 9607-15 (2006)
[41]A. Tomas, C. E. Futter and E. R. Eden: EGF receptor trafficking: consequences for signaling and cancer. Trends Cell Biol, 24(1), 26-34 (2014)
[42]A. Horowitz and H. R. Seerapu: Regulation of VEGF signaling by membrane traffic. Cell Signal, 24(9), 1810-20 (2012)
[43]P. Balogh, S. Katz and A. L. Kiss: The role of endocytic pathways in TGF-beta signaling. Pathol Oncol Res, 19(2), 141-8 (2013)
[44]L. K. Goh and A. Sorkin: Endocytosis of receptor tyrosine kinases. Cold Spring Harb Perspect Biol, 5(5), a017459 (2013)
[45]W. L. Lee, M. Bezanilla and T. D. Pollard: Fission yeast myosin-I, Myo1p, stimulates actin assembly by Arp2/3 complex and shares functions with WASp. J Cell Biol, 151(4), 789-800 (2000)
[46]S. B. Padrick, L. K. Doolittle, C. A. Brautigam, D. S. King and M. K. Rosen: Arp2/3 complex is bound and activated by two WASP proteins. Proc Natl Acad Sci U S A, 108(33), E472-9 (2011)
[47]M. N. Okur, J. Ooi, C. W. Fong, N. Martinez, C. Garcia-Dominguez, J. M. Rojas, G. Guy and J. P. O’Bryan: Intersectin 1 enhances Cbl ubiquitylation of epidermal growth factor receptor through regulation of Sprouty2-Cbl interaction. Mol Cell Biol, 32(4), 817-25 (2012)
[48]R. C. Piper, I. Dikic and G. L. Lukacs: Ubiquitin-dependent sorting in endocytosis. Cold Spring Harb Perspect Biol, 6(1) (2014)
[49]K. Haglund and I. Dikic: The role of ubiquitylation in receptor endocytosis and endosomal sorting. J Cell Sci, 125(Pt 2), 265-75 (2012)
[50]C. A. Clement, K. D. Ajbro, K. Koefoed, M. L. Vestergaard, I. R. Veland, M. P. Henriques de Jesus, L. B. Pedersen, A. Benmerah, C. Y. Andersen, L. A. Larsen and S. T. Christensen: TGF-beta signaling is associated with endocytosis at the pocket region of the primary cilium. Cell Rep, 3(6), 1806-14 (2013)
[51]M. M. Sak, K. Breen, S. B. Ronning, N. M. Pedersen, V. Bertelsen, E. Stang and I. H. Madshus: The oncoprotein ErbB3 is endocytosed in the absence of added ligand in a clathrin-dependent manner. Carcinogenesis, 33(5), 1031-9 (2012)
[52]L. Henriksen, M. V. Grandal, S. L. Knudsen, B. van Deurs and L. M. Grovdal: Internalization mechanisms of the epidermal growth factor receptor after activation with different ligands. PLoS One, 8(3), e58148 (2013)
[53]K. Roepstorff, L. Grovdal, M. Grandal, M. Lerdrup and B. van Deurs: Endocytic downregulation of ErbB receptors: mechanisms and relevance in cancer. Histochem Cell Biol, 129(5), 563-78 (2008)
[54]M. Zhen, R. Heinlein, D. Jones, S. Jentsch and E. P. Candido: The ubc-2 gene of Caenorhabditis elegans encodes a ubiquitin-conjugating enzyme involved in selective protein degradation. Mol Cell Biol, 13(3), 1371-7 (1993)
[55]M. R. Rogel, A. Jaitovich and K. M. Ridge: The role of the ubiquitin proteasome pathway in keratin intermediate filament protein degradation. Proc Am Thorac Soc, 7(1), 71-6 (2010)
[56]A. G. Manford, C. J. Stefan, H. L. Yuan, J. A. Macgurn and S. D. Emr: ER-to-plasma membrane tethering proteins regulate cell signaling and ER morphology. Dev Cell, 23(6), 1129-40 (2012)
[57]F. Alber, S. Dokudovskaya, L. M. Veenhoff, W. Zhang, J. Kipper, D. Devos, A. Suprapto, O. Karni-Schmidt, R. Williams, B. T. Chait, A. Sali and M. P. Rout: The molecular architecture of the nuclear pore complex. Nature, 450(7170), 695-701 (2007)
[58]B. A. Hocevar, C. Prunier and P. H. Howe: Disabled-2 (Dab2) mediates transforming growth factor beta (TGFbeta)-stimulated fibronectin synthesis through TGFbeta-activated kinase 1 and activation of the JNK pathway. J Biol Chem, 280(27), 25920-7 (2005)
[59]J. Kang, Y. Shi, B. Xiang, B. Qu, W. Su, M. Zhu, M. Zhang, G. Bao, F. Wang, X. Zhang, R. Yang, F. Fan, X. Chen, G. Pei and L. Ma: A nuclear function of beta-arrestin1 in GPCR signaling: regulation of histone acetylation and gene transcription. Cell, 123(5), 833-47 (2005)
[60]T. M. Brand, M. Iida, C. Li and D. L. Wheeler: The nuclear epidermal growth factor receptor signaling network and its role in cancer. Discov Med, 12(66), 419-32 (2011)
[61]Y. N. Wang, H. H. Lee, H. J. Lee, Y. Du, H. Yamaguchi and M. C. Hung: Membrane-bound trafficking regulates nuclear transport of integral epidermal growth factor receptor (EGFR) and ErbB-2. J Biol Chem, 287(20), 16869-79 (2012)
[62]D. M. Bryant, F. G. Wylie and J. L. Stow: Regulation of endocytosis, nuclear translocation, and signaling of fibroblast growth factor receptor 1 by E-cadherin. Mol Biol Cell, 16(1), 14-23 (2005)
[63]A. V. Vieira, C. Lamaze and S. L. Schmid: Control of EGF receptor signaling by clathrin-mediated endocytosis. Science, 274(5295), 2086-9 (1996)
[64]H. M. Jopling, A. F. Odell, C. Pellet-Many, A. M. Latham, P. Frankel, A. Sivaprasadarao, J. H. Walker, I. C. Zachary and S. Ponnambalam: Endosome-to-Plasma Membrane Recycling of VEGFR2 Receptor Tyrosine Kinase Regulates Endothelial Function and Blood Vessel Formation. Cells, 3(2), 363-85 (2014)
[65]I. Domingues, J. Rino, J. A. Demmers, P. de Lanerolle and S. C. Santos: VEGFR2 translocates to the nucleus to regulate its own transcription. PLoS One, 6(9), e25668 (2011)
Article Metrics
Download
- Contents
Information
Download
Contents
Frontiers in Bioscience-Landmark (FBL) is published by IMR Press from Volume 26 Issue 5 (2021). Previous articles were published by another publisher on a subscription basis, and they are hosted by IMR Press on imrpress.com as a courtesy and upon agreement with Frontiers in Bioscience.
Endocytosis and membrane receptor internalization: implication of F-BAR protein Carom
1 Center Department of Cardiology, Second Affiliated Hospital of Nanchang University, Nan Chang, Jiang Xi, 330006, China
2 Center for Metabolic Disease Research, Temple University School of Medicine, Philadelphia, PA, 19140, USA
3 Cardiovascular Research, Temple University School of Medicine, Philadelphia, PA, 19140, USA
4 Thrombosis Research, Temple University School of Medicine, Philadelphia, PA, 19140, USA
5 Department of Pharmacology, Temple University School of Medicine, Philadelphia, PA, 19140, USA
6 Department of Cardiology, Changhai Hospital, Second Military Medical University, Shanghai, 200433, China
7 Department of Orthopedics, Second Affiliated Hospital of Nanchang University, Nan Chang, Jiang Xi, 330006, China
Abstract
Endocytosis is a cellular process mostly responsible for membrane receptor internalization. Cell membrane receptors bind to their ligands and form a complex which can be internalized. We previously proposed that F-BAR protein initiates membrane curvature and mediates endocytosis via its binding partners. However, F-BAR protein partners involved in membrane receptor endocytosis and the regulatory mechanism remain unknown. In this study, we established database mining strategies to explore mechanisms underlying receptor-related endocytosis. We identified 34 endocytic membrane receptors and 10 regulating proteins in clathrin-dependent endocytosis (CDE), a major process of membrane receptor internalization. We found that F-BAR protein FCHSD2 (Carom) may facilitate endocytosis via 9 endocytic partners. Carom is highly expressed, along with highly expressed endocytic membrane receptors and partners, in endothelial cells and macrophages. We established 3 models of Carom-receptor complexes and their intracellular trafficking based on protein interaction and subcellular localization. We conclude that Carom may mediate receptor endocytosis and transport endocytic receptors to the cytoplasm for receptor signaling and lysosome/proteasome degradation, or to the nucleus for RNA processing, gene transcription and DNA repair.
Keywords
- F-BAR proteins
- Membrane receptor
- Cellular trafficking
- Nuclear translocation
- Endocytosis
- Review
References
- [1] A. Du Toit: Endocytosis. A new gateway into cells. Nat Rev Mol Cell Biol, 16(2), 68 (2015)
- [2] H. T. McMahon and E. Boucrot: Molecular mechanism and physiological functions of clathrin-mediated endocytosis. Nat Rev Mol Cell Biol, 12(8), 517-33 (2011)
- [3] Z. J. Cheng, R. D. Singh, D. L. Marks and R. E. Pagano: Membrane microdomains, caveolae, and caveolar endocytosis of sphingolipids. Mol Membr Biol, 23(1), 101-10 (2006)
- [4] R. C. Aguilar and B. Wendland: Endocytosis of membrane receptors: two pathways are better than one. Proc Natl Acad Sci U S A, 102(8), 2679-80 (2005)
- [5] G. Kourouniotis, Y. Wang, S. Pennock, X. Chen and Z. Wang: Non-Ligand-Induced Dimerization is Sufficient to Initiate the Signalling and Endocytosis of EGF Receptor. Int J Mol Sci, 17(8) (2016)
- [6] D. P. Poole and N. W. Bunnett: G Protein-Coupled Receptor Trafficking and Signalling in the Enteric Nervous System: The Past, Present and Future. Adv Exp Med Biol, 891, 145-52 (2016)
- [7] H. Cao, X. Yin, Y. Cao, Y. Jin, S. Wang, Y. Kong, Y. Chen, J. Gao, S. Heller and Z. Xu: FCHSD1 and FCHSD2 are expressed in hair cell stereocilia and cuticular plate and regulate actin polymerization in vitro. PLoS One, 8(2), e56516 (2013)
- [8] W. M. Henne, E. Boucrot, M. Meinecke, E. Evergren, Y. Vallis, R. Mittal and H. T. McMahon: FCHo proteins are nucleators of clathrin-mediated endocytosis. Science, 328(5983), 1281-4 (2010)
- [9] X. Huang, R. Gong, X. Li, A. Virtue, F. Yang, I. H. Yang, A. H. Tran, X. F. Yang and H. Wang: Identification of novel pretranslational regulatory mechanisms for NF-kappaB activation. J Biol Chem, 288(22), 15628-40 (2013)
- [10] N. C. Chen, F. Yang, L. M. Capecci, Z. Gu, A. I. Schafer, W. Durante, X. F. Yang and H. Wang: Regulation of homocysteine metabolism and methylation in human and mouse tissues. FASEB J, 24(8), 2804-17 (2010)
- [11] X. Li, J. Mai, A. Virtue, Y. Yin, R. Gong, X. Sha, S. Gutchigian, A. Frisch, I. Hodge, X. Jiang, H. Wang and X. F. Yang: IL-35 is a novel responsive anti-inflammatory cytokine--a new system of categorizing anti-inflammatory cytokines. PLoS One, 7(3), e33628 (2012)
- [12] H. Iioka and I. G. Macara: Detection of RNA-Protein Interactions Using Tethered RNA Affinity Capture. Methods Mol Biol, 1316, 67-73 (2015)
- [13] M. Barrios-Rodiles, K. R. Brown, B. Ozdamar, R. Bose, Z. Liu, R. S. Donovan, F. Shinjo, Y. Liu, J. Dembowy, I. W. Taylor, V. Luga, N. Przulj, M. Robinson, H. Suzuki, Y. Hayashizaki, I. Jurisica and J. L. Wrana: High-throughput mapping of a dynamic signaling network in mammalian cells. Science, 307(5715), 1621-5 (2005)
- [14] M. Kotlyar, C. Pastrello, F. Pivetta, A. Lo Sardo, C. Cumbaa, H. Li, T. Naranian, Y. Niu, Z. Ding, F. Vafaee, F. Broackes-Carter, J. Petschnigg, G. B. Mills, A. Jurisicova, I. Stagljar, R. Maestro and I. Jurisica: In silico prediction of physical protein interactions and characterization of interactome orphans. Nat Methods, 12(1), 79-84 (2015)
- [15] Z. Lu and T. Hunter: Degradation of activated protein kinases by ubiquitination. Annu Rev Biochem, 78, 435-75 (2009)
- [16] M. Galovic, D. Xu, L. B. Areces, R. van der Kammen and M. Innocenti: Interplay between N-WASP and CK2 optimizes clathrin-mediated endocytosis of EGFR. J Cell Sci, 124(Pt 12), 2001-12 (2011)
- [17] R. B. Jones, A. Gordus, J. A. Krall and G. MacBeath: A quantitative protein interaction network for the ErbB receptors using protein microarrays. Nature, 439(7073), 168-74 (2006)
- [18] J. Tong, P. Taylor, S. M. Peterman, A. Prakash and M. F. Moran: Epidermal growth factor receptor phosphorylation sites Ser991 and Tyr998 are implicated in the regulation of receptor endocytosis and phosphorylations at Ser1039 and Thr1041. Mol Cell Proteomics, 8(9), 2131-44 (2009)
- [19] F. Bornke: Corrigendum: The complex becomes more complex: protein-protein interactions of SnRK1 with DUF581 family proteins provide a framework for cell- and stimulus type-specific SnRK1 signaling in plants. Front Plant Sci, 5, 693 (2014)
- [20] X. Tang, X. Hu, X. Yang, Y. Fan, Y. Li, W. Hu, Y. Liao, M. C. Zheng, W. Peng and L. Gao: Predicting diabetes mellitus genes via protein-protein interaction and protein subcellular localization information. BMC Genomics, 17 Suppl 4, 433 (2016)
- [21] B. Pyrzynska, I. Pilecka and M. Miaczynska: Endocytic proteins in the regulation of nuclear signaling, transcription and tumorigenesis. Mol Oncol, 3(4), 321-38 (2009)
- [22] Y. Mosesson, K. Shtiegman, M. Katz, Y. Zwang, G. Vereb, J. Szollosi and Y. Yarden: Endocytosis of receptor tyrosine kinases is driven by monoubiquitylation, not polyubiquitylation. J Biol Chem, 278(24), 21323-6 (2003)
- [23] C. Le Roy and J. L. Wrana: Clathrin- and non-clathrin-mediated endocytic regulation of cell signalling. Nat Rev Mol Cell Biol, 6(2), 112-26 (2005)
- [24] C. Basquin, M. Trichet, H. Vihinen, V. Malarde, T. Lagache, L. Ripoll, E. Jokitalo, J. C. Olivo-Marin, A. Gautreau and N. Sauvonnet: Membrane protrusion powers clathrin-independent endocytosis of interleukin-2 receptor. EMBO J, 34(16), 2147-61 (2015)
- [25] S. Liu, X. Xiong, X. Zhao, X. Yang and H. Wang: F-BAR family proteins, emerging regulators for cell membrane dynamic changes-from structure to human diseases. J Hematol Oncol, 8, 47 (2015)
- [26] I. K. Jarsch, F. Daste and J. L. Gallop: Membrane curvature in cell biology: An integration of molecular mechanisms. J Cell Biol, 214(4), 375-87 (2016)
- [27] R. Sousa, H. S. Liao, J. Cuellar, S. Jin, J. M. Valpuesta, A. J. Jin and E. M. Lafer: Clathrin-coat disassembly illuminates the mechanisms of Hsp70 force generation. Nat Struct Mol Biol, 23(9), 821-9 (2016)
- [28] J. Hu, F. Troglio, A. Mukhopadhyay, S. Everingham, E. Kwok, G. Scita and A. W. Craig: F-BAR-containing adaptor CIP4 localizes to early endosomes and regulates Epidermal Growth Factor Receptor trafficking and downregulation. Cell Signal, 21(11), 1686-97 (2009)
- [29] E. E. Mulkearns and J. A. Cooper: FCH domain only-2 organizes clathrin-coated structures and interacts with Disabled-2 for low-density lipoprotein receptor endocytosis. Mol Biol Cell, 23(7), 1330-42 (2012)
- [30] B. J. de Kreuk, E. C. Anthony, D. Geerts and P. L. Hordijk: The F-BAR protein PACSIN2 regulates epidermal growth factor receptor internalization. J Biol Chem, 287(52), 43438-53 (2012)
- [31] K. M. Cooper, D. A. Bennin and A. Huttenlocher: The PCH family member proline-serine-threonine phosphatase-interacting protein 1 targets to the leukocyte uropod and regulates directed cell migration. Mol Biol Cell, 19(8), 3180-91 (2008)
- [32] S. Liu, X. Xiong, S. V. Thomas, Y. Xu, X. Cheng, X. Zhao, X. Yang and H. Wang: Analysis for Carom complex, signaling and function by database mining. Front Biosci (Landmark Ed), 21, 856-72 (2016)
- [33] I. Kovacevic, J. Hu, A. Siehoff-Icking, N. Opitz, A. Griffin, A. C. Perkins, A. L. Munn, W. Muller-Esterl, R. Popp, I. Fleming, B. Jungblut, M. Hoffmeister and S. Oess: The F-BAR protein NOSTRIN participates in FGF signal transduction and vascular development. EMBO J, 31(15), 3309-22 (2012)
- [34] J. Modregger, B. Ritter, B. Witter, M. Paulsson and M. Plomann: All three PACSIN isoforms bind to endocytic proteins and inhibit endocytosis. J Cell Sci, 113 Pt 24, 4511-21 (2000)
- [35] A. A. Bizet, K. Liu, N. Tran-Khanh, A. Saksena, J. Vorstenbosch, K. W. Finnson, M. D. Buschmann and A. Philip: The TGF-beta co-receptor, CD109, promotes internalization and degradation of TGF-beta receptors. Biochim Biophys Acta, 1813(5), 742-53 (2011)
- [36] M. Chandra, S. Zang, H. Li, L. J. Zimmerman, J. Champer, A. Tsuyada, A. Chow, W. Zhou, Y. Yu, H. Gao, X. Ren, R. J. Lin and S. E. Wang: Nuclear translocation of type I transforming growth factor beta receptor confers a novel function in RNA processing. Mol Cell Biol, 32(12), 2183-95 (2012)
- [37] H. A. Alwan, E. J. van Zoelen and J. E. van Leeuwen: Ligand-induced lysosomal epidermal growth factor receptor (EGFR) degradation is preceded by proteasome-dependent EGFR de-ubiquitination. J Biol Chem, 278(37), 35781-90 (2003)
- [38] Y. N. Wang and M. C. Hung: Nuclear functions and subcellular trafficking mechanisms of the epidermal growth factor receptor family. Cell Biosci, 2(1), 13 (2012)
- [39] G. Levkowitz, H. Waterman, E. Zamir, Z. Kam, S. Oved, W. Y. Langdon, L. Beguinot, B. Geiger and Y. Yarden: c-Cbl/Sli-1 regulates endocytic sorting and ubiquitination of the epidermal growth factor receptor. Genes Dev, 12(23), 3663-74 (1998)
- [40] X. Long and K. P. Nephew: Fulvestrant (ICI 182,780)-dependent interacting proteins mediate immobilization and degradation of estrogen receptor-alpha. J Biol Chem, 281(14), 9607-15 (2006)
- [41] A. Tomas, C. E. Futter and E. R. Eden: EGF receptor trafficking: consequences for signaling and cancer. Trends Cell Biol, 24(1), 26-34 (2014)
- [42] A. Horowitz and H. R. Seerapu: Regulation of VEGF signaling by membrane traffic. Cell Signal, 24(9), 1810-20 (2012)
- [43] P. Balogh, S. Katz and A. L. Kiss: The role of endocytic pathways in TGF-beta signaling. Pathol Oncol Res, 19(2), 141-8 (2013)
- [44] L. K. Goh and A. Sorkin: Endocytosis of receptor tyrosine kinases. Cold Spring Harb Perspect Biol, 5(5), a017459 (2013)
- [45] W. L. Lee, M. Bezanilla and T. D. Pollard: Fission yeast myosin-I, Myo1p, stimulates actin assembly by Arp2/3 complex and shares functions with WASp. J Cell Biol, 151(4), 789-800 (2000)
- [46] S. B. Padrick, L. K. Doolittle, C. A. Brautigam, D. S. King and M. K. Rosen: Arp2/3 complex is bound and activated by two WASP proteins. Proc Natl Acad Sci U S A, 108(33), E472-9 (2011)
- [47] M. N. Okur, J. Ooi, C. W. Fong, N. Martinez, C. Garcia-Dominguez, J. M. Rojas, G. Guy and J. P. O’Bryan: Intersectin 1 enhances Cbl ubiquitylation of epidermal growth factor receptor through regulation of Sprouty2-Cbl interaction. Mol Cell Biol, 32(4), 817-25 (2012)
- [48] R. C. Piper, I. Dikic and G. L. Lukacs: Ubiquitin-dependent sorting in endocytosis. Cold Spring Harb Perspect Biol, 6(1) (2014)
- [49] K. Haglund and I. Dikic: The role of ubiquitylation in receptor endocytosis and endosomal sorting. J Cell Sci, 125(Pt 2), 265-75 (2012)
- [50] C. A. Clement, K. D. Ajbro, K. Koefoed, M. L. Vestergaard, I. R. Veland, M. P. Henriques de Jesus, L. B. Pedersen, A. Benmerah, C. Y. Andersen, L. A. Larsen and S. T. Christensen: TGF-beta signaling is associated with endocytosis at the pocket region of the primary cilium. Cell Rep, 3(6), 1806-14 (2013)
- [51] M. M. Sak, K. Breen, S. B. Ronning, N. M. Pedersen, V. Bertelsen, E. Stang and I. H. Madshus: The oncoprotein ErbB3 is endocytosed in the absence of added ligand in a clathrin-dependent manner. Carcinogenesis, 33(5), 1031-9 (2012)
- [52] L. Henriksen, M. V. Grandal, S. L. Knudsen, B. van Deurs and L. M. Grovdal: Internalization mechanisms of the epidermal growth factor receptor after activation with different ligands. PLoS One, 8(3), e58148 (2013)
- [53] K. Roepstorff, L. Grovdal, M. Grandal, M. Lerdrup and B. van Deurs: Endocytic downregulation of ErbB receptors: mechanisms and relevance in cancer. Histochem Cell Biol, 129(5), 563-78 (2008)
- [54] M. Zhen, R. Heinlein, D. Jones, S. Jentsch and E. P. Candido: The ubc-2 gene of Caenorhabditis elegans encodes a ubiquitin-conjugating enzyme involved in selective protein degradation. Mol Cell Biol, 13(3), 1371-7 (1993)
- [55] M. R. Rogel, A. Jaitovich and K. M. Ridge: The role of the ubiquitin proteasome pathway in keratin intermediate filament protein degradation. Proc Am Thorac Soc, 7(1), 71-6 (2010)
- [56] A. G. Manford, C. J. Stefan, H. L. Yuan, J. A. Macgurn and S. D. Emr: ER-to-plasma membrane tethering proteins regulate cell signaling and ER morphology. Dev Cell, 23(6), 1129-40 (2012)
- [57] F. Alber, S. Dokudovskaya, L. M. Veenhoff, W. Zhang, J. Kipper, D. Devos, A. Suprapto, O. Karni-Schmidt, R. Williams, B. T. Chait, A. Sali and M. P. Rout: The molecular architecture of the nuclear pore complex. Nature, 450(7170), 695-701 (2007)
- [58] B. A. Hocevar, C. Prunier and P. H. Howe: Disabled-2 (Dab2) mediates transforming growth factor beta (TGFbeta)-stimulated fibronectin synthesis through TGFbeta-activated kinase 1 and activation of the JNK pathway. J Biol Chem, 280(27), 25920-7 (2005)
- [59] J. Kang, Y. Shi, B. Xiang, B. Qu, W. Su, M. Zhu, M. Zhang, G. Bao, F. Wang, X. Zhang, R. Yang, F. Fan, X. Chen, G. Pei and L. Ma: A nuclear function of beta-arrestin1 in GPCR signaling: regulation of histone acetylation and gene transcription. Cell, 123(5), 833-47 (2005)
- [60] T. M. Brand, M. Iida, C. Li and D. L. Wheeler: The nuclear epidermal growth factor receptor signaling network and its role in cancer. Discov Med, 12(66), 419-32 (2011)
- [61] Y. N. Wang, H. H. Lee, H. J. Lee, Y. Du, H. Yamaguchi and M. C. Hung: Membrane-bound trafficking regulates nuclear transport of integral epidermal growth factor receptor (EGFR) and ErbB-2. J Biol Chem, 287(20), 16869-79 (2012)
- [62] D. M. Bryant, F. G. Wylie and J. L. Stow: Regulation of endocytosis, nuclear translocation, and signaling of fibroblast growth factor receptor 1 by E-cadherin. Mol Biol Cell, 16(1), 14-23 (2005)
- [63] A. V. Vieira, C. Lamaze and S. L. Schmid: Control of EGF receptor signaling by clathrin-mediated endocytosis. Science, 274(5295), 2086-9 (1996)
- [64] H. M. Jopling, A. F. Odell, C. Pellet-Many, A. M. Latham, P. Frankel, A. Sivaprasadarao, J. H. Walker, I. C. Zachary and S. Ponnambalam: Endosome-to-Plasma Membrane Recycling of VEGFR2 Receptor Tyrosine Kinase Regulates Endothelial Function and Blood Vessel Formation. Cells, 3(2), 363-85 (2014)
- [65] I. Domingues, J. Rino, J. A. Demmers, P. de Lanerolle and S. C. Santos: VEGFR2 translocates to the nucleus to regulate its own transcription. PLoS One, 6(9), e25668 (2011)
