Schwann cell‐specific deletion of the endosomal PI 3‐kinase Vps34 leads to delayed radial sorting of axons, arrested myelination, and abnormal ErbB2‐ErbB3 tyrosine kinase signaling
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The PI 3‐kinase Vps34 (Pik3c3) synthesizes phosphatidylinositol 3‐phosphate (PI3P), a lipid critical for both endosomal membrane traffic and macroautophagy. Human genetics have implicated PI3P dysregulation, and endosomal trafficking in general, as a recurring cause of demyelinating Charcot‐Marie‐Tooth (CMT) peripheral neuropathy. Here, we investigated the role of Vps34, and PI3P, in mouse Schwann cells by selectively deleting Vps34 in this cell type. Vps34‐Schwann cell knockout (Vps34 SCKO) mice show severe hypomyelination in peripheral nerves. Vps34–/– Schwann cells interact abnormally with axons, and there is a delay in radial sorting, a process by which large axons are selected for myelination. Upon reaching the promyelinating stage, Vps34–/– Schwann cells are significantly impaired in the elaboration of myelin. Nerves from Vps34 SCKO mice contain elevated levels of the LC3 and p62 proteins, indicating impaired autophagy. However, in the light of recent demonstrations that autophagy is dispensable for myelination, it is unlikely that hypomyelination in Vps34 SCKO mice is caused by impaired autophagy. Endosomal trafficking is also disturbed in Vps34–/– Schwann cells. We investigated the activation of the ErbB2/3 receptor tyrosine kinases in Vps34 SCKO nerves, as these proteins, which play essential roles in Schwann cell myelination, are known to traffic through endosomes. In Vps34 SCKO nerves, ErbB3 was hyperphosphorylated on a tyrosine known to be phosphorylated in response to neuregulin 1 exposure. ErbB2 protein levels were also decreased during myelination. Our findings suggest that the loss of Vps34 alters the trafficking of ErbB2/3 through endosomes. Abnormal ErbB2/3 signaling to downstream targets may contribute to the hypomyelination observed in Vps34 SCKO mice.
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Conditional deletion of Pik3c3 in murine Schwann cells results in hypomyelination and non-cell autonomous disruption of neuronal autophagic flux and dysregulated neuronal trafficking of ERBB2 or ERBB3 receptor tyrosine kinases.
“Furthermore, conditional deletion of Pik3c3 in murine Schwann cells not only results in hypomyelination, but also in non-cell autonomous disruption of neuronal autophagic flux and dysregulated neuronal trafficking of ERBB2 or ERBB3 receptor tyrosine kinases [460].”
From Autophagy and ALS: mechanistic insights and therapeutic implications (2022) · cites this paper as [460]
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Fiji: an open-source platform for biological-image analysis
Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B., et al. (2012) · Nature Methods · doi:10.1038/nmeth.2019 · Cited by 66,890 · see citing works
Guidelines for the use and interpretation of assays for monitoring autophagy
Klionsky, D. J., Abdalla, F. C., Abeliovich, H., Abraham, R. T., Acevedo-Arozena, A., Adeli, K., Agholme, L., Agnello, M., Agostinis, P., Aguirre-Ghiso, J. A., et al. (2012) · Autophagy · doi:10.4161/auto.19496 · Cited by 3,996 · see citing works
Phosphoinositides: Tiny Lipids With Giant Impact on Cell Regulation
Balla, T. (2013) · Physiological Reviews · doi:10.1152/physrev.00028.2012 · Cited by 1,638 · see citing works
EEA1 links PI(3)K function to Rab5 regulation of endosome fusion
Simonsen, A., Lippe, R., Christoforidis, S., Gaullier, J.-M., Brech, A., Callaghan, J., Toh, B.-H., Murphy, C., Zerial, M., & Stenmark, H. (1998) · Nature · doi:10.1038/28879 · Cited by 1,133 · see citing works
Myelination of the Nervous System: Mechanisms and Functions
Nave, K., & Werner, H. B. (2014) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-100913-013101 · Cited by 1,000 · see citing works
Phosphatidylinositol 3-Kinase Encoded by Yeast VPS 34 Gene Essential for Protein Sorting
Schu, P. V., Takegawa, K., Fry, M., Stack, J. H., Waterfield, M. D., & Emr, S. D. (1993) · Science · doi:10.1126/science.8385367 · Cited by 920 · see citing works
Krox-20 controls myelination in the peripheral nervous system
Topilko, P., Schneider‐Maunoury, S., Levi, G., Evercooren, A. B., Chennoufi, A. B. Y., Seitanidou, T., Babinet, C., & Charnay, P. (1994) · Nature · doi:10.1038/371796a0 · Cited by 794 · see citing works
Sox10, a Novel Transcriptional Modulator in Glial Cells
Kuhlbrodt, K., Herbarth, B., Sock, E., Hermans-Borgmeyer, I., & Wegner, M. (1998) · The Journal of Neuroscience · doi:10.1523/jneurosci.18-01-00237.1998 · Cited by 781 · see citing works
Schwann Cells: Development and Role in Nerve RepairPreprint
Jessen, K. R., Mirsky, R., & Lloyd, A. C. (2015) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a020487 · Cited by 759 · see citing works
Endocytosis and intracellular trafficking of ErbBs
Sorkin, A. D., & Goh, L. K. (2008) · Experimental Cell Research · doi:10.1016/j.yexcr.2008.07.029 · Cited by 756 · see citing works
Identification of the Switch in Early-to-Late Endosome Transition
Poteryaev, D., Datta, S., Ackema, K., Zerial, M., & Spang, A. (2010) · Cell · doi:10.1016/j.cell.2010.03.011 · Cited by 752 · see citing works
de Waegh, S. M., Lee, V. M. ‐., & Brady, S. T. (1992) · Cell · doi:10.1016/0092-8674(92)90183-d · Cited by 743 · see citing works
Neuregulin-1 Type III Determines the Ensheathment Fate of Axons
Taveggia, C., Zanazzi, G. J., Petrylak, A., Yano, H., D, J. R. M., Einheber, S., Xu, X., Esper, R. M., Loeb, J. A., Shrager, P. G., et al. (2005) · Neuron · doi:10.1016/j.neuron.2005.08.017 · Cited by 730 · see citing works
The regulation and function of Class III PI3Ks: novel roles for Vps34
Backer, J. (2008) · Biochemical Journal · doi:10.1042/bj20071427 · Cited by 659 · see citing works
Axon caliber related to neurofilaments and microtubules in sciatic nerve fibers of rats and mice
Friede, R. L., & Samorajski, T. (1970) · The Anatomical Record · doi:10.1002/ar.1091670402 · Cited by 538 · see citing works
Mutation of FIG4 causes neurodegeneration in the pale tremor mouse and patients with CMT4J
Chow, C. Y., Zhang, Y., Dowling, J. J., Jin, N., Adamska, M., Shiga, K., Szigeti, K., Shy, M. E., Li, J., Zhang, X., et al. (2007) · Nature · doi:10.1038/nature05876 · Cited by 516 · see citing works
Myelin-Associated Glycoprotein Is a Myelin Signal that Modulates the Caliber of Myelinated Axons
Yin, X., Crawford, T. O., Griffin, J. W., Tu, P., Lee, V. M. ‐., Li, C. C., Roder, J., & Trapp, B. D. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-06-01953.1998 · Cited by 491 · see citing works
Bolino, A., Muglia, M., Conforti, F. L., Leguern, É., Salih, M. A. M., Georgiou, D.-M., Christodoulou, K., Hausmanowa-Petrusewicz, I., Mandich, P., Schenone, A. E., et al. (2000) · Nature Genetics · doi:10.1038/75542 · Cited by 466 · see citing works
Schwann cell autophagy, myelinophagy, initiates myelin clearance from injured nerves
Gomez-Sanchez, J. A., Carty, L., Iruarrizaga-Lejarreta, M., Palomo-Irigoyen, M., Varela-Rey, M., Griffith, M., Hantke, J., Macias-Camara, N., Azkargorta, M., Aurrekoetxea, I., et al. (2015) · Journal of Cell Biology · doi:10.1083/jcb.201503019 · Cited by 453 · see citing works
Control of axonal caliber by neurofilament transport.
Hoffman, P. N., Griffin, J. W., & Price, D. L. (1984) · The Journal of Cell Biology · doi:10.1083/jcb.99.2.705 · Cited by 443 · see citing works
Trembler mouse carries a point mutation in a myelin gene
Suter, U., Welcher, A. A., Özçelık, T., Snipes, G. J., Kosaras, B., Francke, U., Billings‐Gagliardi, S., Sidman, R. L., & Shooter, E. M. (1992) · Nature · doi:10.1038/356241a0 · Cited by 426 · see citing works
Tofaris, G., Patterson, P., Jessen, K., & Mirsky, R. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-15-06696.2002 · Cited by 403 · see citing works
Class III PI3K Vps34 plays an essential role in autophagy and in heart and liver function
Jaber, N. L., Dou, Z., Chen, J., Catanzaro, J. M., Jiang, Y.-P., Ballou, L. M., Selinger, E. S., Ouyang, X., Lin, R. Z., Zhang, J., et al. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1112848109 · Cited by 386 · see citing works
Schwann Cell MyelinationPreprint
Salzer, J. L. (2015) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a020529 · Cited by 365 · see citing works
Goebbels, S., Oltrogge, J., Kemper, R., Heilmann, I., Bormuth, I., Wolfer, S., Wichert, S. P., Möbius, W., Liu, X., Lappe-Siefke, C., et al. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.0219-10.2010 · Cited by 329 · see citing works
Conditional disruption of β1 integrin in Schwann cells impedes interactions with axons
Feltri, M. L., Porta, D. G., Previtali, S. C., Nodari, A., Migliavacca, B., Cassetti, A., Littlewood-Evans, A., Reichardt, L. F., Messing, A., Quattrini, A., et al. (2002) · The Journal of Cell Biology · doi:10.1083/jcb.200109021 · Cited by 325 · see citing works
Le, N., Nagarajan, R., Wang, Y. T., Araki, T., Schmidt, R. E., & Milbrandt, J. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0407836102 · Cited by 302 · see citing works
The POU proteins Brn-2 and Oct-6 share important functions in Schwann cell developmentPreprint
Jaegle, M., Ghazvini, M., Mandemakers, W. J., Piirsoo, M., Driegen, S., Levavasseur, F., Raghoenath, S., Grosveld, F. G., & Meijer, D. (2003) · Genes & Development · doi:10.1101/gad.258203 · Cited by 300 · see citing works
Phosphoinositides in Control of Membrane Dynamics
Schink, K. O., Tan, K.-W., & Stenmark, H. (2016) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-111315-125349 · Cited by 283 · see citing works
Senderek, J. (2003) · Human Molecular Genetics · doi:10.1093/hmg/ddg030 · Cited by 275 · see citing works
Nrg1/ErbB signaling networks in Schwann cell development and myelination
Newbern, J. M., & Birchmeier, C. (2010) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2010.08.008 · Cited by 266 · see citing works
New insights on schwann cell development
Monk, K. R., Feltri, M. L., & Taveggia, C. (2015) · Glia · doi:10.1002/glia.22852 · Cited by 256 · see citing works
Human VPS34 is required for internal vesicle formation within multivesicular endosomes
Futter, C. E., Collinson, L., Backer, J., & Hopkins, C. R. (2001) · The Journal of Cell Biology · doi:10.1083/jcb.200108152 · Cited by 248 · see citing works
The molecular machinery of myelin gene transcription in Schwann cells
Svaren, J. P., & Meijer, D. (2008) · Glia · doi:10.1002/glia.20767 · Cited by 244 · see citing works
Integrin endosomal signalling suppresses anoikis
Alanko, J., Mai, A., Jacquemet, G., Schauer, K., Kaukonen, R., Saari, M. A., Goud, B., & Ivaska, J. (2015) · Nature Cell Biology · doi:10.1038/ncb3250 · Cited by 243 · see citing works
Krox-20 inhibits Jun-NH2-terminal kinase/c-Jun to control Schwann cell proliferation and death
Parkinson, D. B., Bhaskaran, A., Droggiti, A., Dickinson, S., D’Antonio, M., Mirsky, R., & Jessen, K. R. (2004) · The Journal of Cell Biology · doi:10.1083/jcb.200307132 · Cited by 240 · see citing works
Zhou, X., Wang, L., Hasegawa, H., Amin, P., Han, B.-X., Kaneko, S., He, Y.-W., & Wang, F. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0914725107 · Cited by 236 · see citing works
Wrapping it up: the cell biology of myelination
Simons, M., & Trotter, J. (2007) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2007.08.003 · Cited by 227 · see citing works
Multivesicular body morphogenesis requires phosphatidyl-inositol 3-kinase activity
Fernandez‐Borja, M., Wubbolts, R., Calafat, J., Janssen, H., Divecha, N., Dusseljee, S., & Neefjes, J. (1999) · Current Biology · doi:10.1016/s0960-9822(99)80048-7 · Cited by 214 · see citing works
P0‐Cre Transgenic Mice for Inactivation of Adhesion Molecules in Schwann Cells
Feltri, M. L., D’Antonio, M., Previtali, S. C., Fasolini, M., Messing, A., & Wrabetz, L. G. (1999) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1999.tb08574.x · Cited by 208 · see citing works
Feltri, M. L., Poitelon, Y., & Previtali, S. C. (2015) · The Neuroscientist · doi:10.1177/1073858415572361 · Cited by 205 · see citing works
Metabolic regulator LKB1 is crucial for Schwann cell–mediated axon maintenance
Beirowski, B., Babetto, E., Golden, J. P., Chen, Y., Yang, K., Gross, R. W., Patti, G. J., & Milbrandt, J. (2014) · Nature Neuroscience · doi:10.1038/nn.3809 · Cited by 197 · see citing works
Regulation of Mammalian Autophagy by Class II and III PI 3-Kinases through PI3P Synthesis
Devereaux, K. A., Dall’Armi, C., Alcázar-Román, A. R., Ogasawara, Y., Zhou, X., Wang, F., Yamamoto, A., Camilli, P. V. D., & Paolo, G. D. (2013) · PLoS ONE · doi:10.1371/journal.pone.0076405 · Cited by 196 · see citing works
Nodari, A., Zambroni, D., Quattrini, A., Court, F. A., D'Urso, A., Recchia, A., Tybulewicz, V. L. J., Wrabetz, L. G., & Feltri, M. L. (2007) · The Journal of Cell Biology · doi:10.1083/jcb.200610014 · Cited by 191 · see citing works
Mogha, A., Benesh, A. E., Patra, C., Engel, F. B., Schöneberg, T., Liebscher, I., & Monk, K. R. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.1809-13.2013 · Cited by 188 · see citing works
Neuron to glia signaling triggers myelin membrane exocytosis from endosomal storage sites
Trajkovic, K., Dhaunchak, A. S., Goncalves, J. T., Wenzel, D., Schneider, A., Bunt, G., Nave, K.-A., & Simons, M. (2006) · The Journal of Cell Biology · doi:10.1083/jcb.200509022 · Cited by 186 · see citing works
Willinger, T., & Flavell, R. A. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1205305109 · Cited by 183 · see citing works
Myelination determines the caliber of dorsal root ganglion neurons in culture
Aj, W., Wood, P. M., Bunge, R. P., & Pj, D. (1985) · Journal of Neuroscience · doi:10.1523/jneurosci.05-06-01563.1985 · Cited by 175 · see citing works
Molecular mechanisms of inherited demyelinating neuropathies
Scherer, S. S., & Wrabetz, L. G. (2008) · Glia · doi:10.1002/glia.20751 · Cited by 171 · see citing works
Arrest of Myelination and Reduced Axon Growth When Schwann Cells Lack mTOR
Sherman, D. L., Krols, M., Wu, L.-M. N., Grove, M., Nave, K., Gangloff, Y., & Brophy, P. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.4814-11.2012 · Cited by 144 · see citing works
Vps34 Deficiency Reveals the Importance of Endocytosis for Podocyte Homeostasis
Bechtel, W., Helmstädter, M., Balica, J., Hartleben, B., Kiefer, B., Hrnjic, F., Schell, C., Kretz, O., Liu, S., Geist, F., et al. (2013) · Journal of the American Society of Nephrology · doi:10.1681/asn.2012070700 · Cited by 132 · see citing works
ErbB2 directly activates the exchange factor Dock7 to promote Schwann cell migration
Yamauchi, J., Miyamoto, Y., Chan, J. R., & Tanoue, A. (2008) · The Journal of Cell Biology · doi:10.1083/jcb.200709033 · Cited by 131 · see citing works
Pereira, J. A., Benninger, Y., Baumann, R., Gonçalves, A. F., Özçelik, M., Buerki‐Thurnherr, T., Tricaud, N., Meijer, D., Fässler, R., Suter, U., et al. (2009) · The Journal of Cell Biology · doi:10.1083/jcb.200809008 · Cited by 122 · see citing works
The effect of myelinating Schwann cells on axons
Martini, R. (2001) · Muscle & Nerve · doi:10.1002/mus.1027 · Cited by 113 · see citing works
Johnson, E. E., Overmeyer, J. H., Gunning, W. T., & Maltese, W. A. (2006) · Journal of Cell Science · doi:10.1242/jcs.02833 · Cited by 111 · see citing works
FAK is required for axonal sorting by Schwann cells
Grove, M., Komiyama, N. H., Nave, K., Grant, S. G. N., Sherman, D. L., & Brophy, P. (2007) · The Journal of Cell Biology · doi:10.1083/jcb.200609021 · Cited by 107 · see citing works
Raiborg, C., Schink, K. O., & Stenmark, H. (2013) · FEBS Journal · doi:10.1111/febs.12116 · Cited by 103 · see citing works
Robertson, A., Perea, J., McGuigan, A., King, R. H. M., Muddle, J. R., Gabreëls‐Festen, A. A. W. M., Thomas, P. K., & Huxley, C. M. (2002) · Journal of Anatomy · doi:10.1046/j.1469-7580.2002.00039.x · Cited by 98 · see citing works
Promyelinating Schwann Cells Express Tst-1/SCIP/Oct-6
Arroyo, E. J., Bermingham, J. R., Rosenfeld, M. G., & Scherer, S. S. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-19-07891.1998 · Cited by 92 · see citing works
Conditional Disruption Of Beta 1 Integrin In Schwann Cells Impedes Interactions With Axons
Feltri, M., Porta, D., Previtali, S. C., Nodari, A., Migliavacca, B., Cassetti, A., Littlewood-Evans, A. J., Reichardt, L. F., Messing, A., Quattrini, A., et al. (2002) · Journal of the Peripheral Nervous System · doi:10.1046/j.1529-8027.2002.02026_1.x · Cited by 90 · see citing works
Akt/mTOR signalling in myelination
Norrmén, C., & Suter, U. (2013) · Biochemical Society Transactions · doi:10.1042/bst20130046 · Cited by 90 · see citing works
SET binding factor 1 ( SBF1 ) mutation causes Charcot-Marie-Tooth disease type 4B3
Nakhro, K., Park, J., Hong, Y. B., Park, J. H., Nam, S. H., Yoon, B. R., Yoo, J. H., Koo, H., Jung, S., Kim, H., et al. (2013) · Neurology · doi:10.1212/wnl.0b013e31829a3421 · Cited by 89 · see citing works
Myelin and macrophages in the PNS: An intimate relationship in trauma and disease
Klein, D., & Martini, R. (2015) · Brain Research · doi:10.1016/j.brainres.2015.11.033 · Cited by 89 · see citing works
Jerath, N. U., & Shy, M. E. (2014) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2014.07.031 · Cited by 88 · see citing works
Vaccari, I., Dina, G., Tronchère, H., Kaufman, E. L., Chicanne, G., Cerri, F., Wrabetz, L. G., Payrastre, B., Quattrini, A., Weisman, L. S., et al. (2011) · PLoS Genetics · doi:10.1371/journal.pgen.1002319 · Cited by 87 · see citing works
Omegasomes: PI3P platforms that manufacture autophagosomes
Roberts, R. L., & Ktistakis, N. T. (2013) · Essays in Biochemistry · doi:10.1042/bse0550017 · Cited by 86 · see citing works
Sidiropoulos, P. N. M., Miehe, M., Bock, T., Tinelli, E., Oertli, C. I., Kuner, R., Meijer, D., Wollscheid, B., Niemann, A., & Suter, U. (2012) · Brain · doi:10.1093/brain/aws061 · Cited by 77 · see citing works
Non-redundant function of dystroglycan and β1 integrins in radial sorting of axons
Berti, C., Bartesaghi, L., Ghidinelli, M., Zambroni, D., Figlia, G., Chen, Z.-L., Quattrini, A., Wrabetz, L. G., & Feltri, M. L. (2011) · Development · doi:10.1242/dev.065490 · Cited by 72 · see citing works
Wood, T., Bercury, K., Cifelli, S. E., Mursch, L. E., Min, J., Dai, J., & Macklin, W. (2013) · ASN Neuro · doi:10.1042/an20120092 · Cited by 67 · see citing works
Lysosomal exocytosis in Schwann cells contributes to axon remyelination
Chen, G., Zhang, Z., Wei, Z., Cheng, Q., Li, X., Li, W., Duan, S., & Gu, X. (2011) · Glia · doi:10.1002/glia.21263 · Cited by 63 · see citing works
Jang, S. Y., Shin, Y. K., Park, S. Y., Park, J. Y., Rha, S.-H., Kim, J. K., Lee, H. J., & Park, H. T. (2015) · PLOS ONE · doi:10.1371/journal.pone.0116624 · Cited by 61 · cited 4× · see citing works
“A similar degree of targeted protein persistence in sciatic nerves has been reported when using Schwann cell-specific Cre drivers and whole nerve extracts (Beirowski et al., 2014; Gomez-Sanchez et al., 2015; Jang et al., 2015; Nodari et al., 2007; Sherman et al., 2012).”
BackgroundResultInfluentialWatson, D. F., Nachtman, F. N., Kuncl, R. W., & Griffin, J. W. (1994) · Neurology · doi:10.1212/wnl.44.12.2383 · Cited by 55 · see citing works
Sh3tc2 deficiency affects neuregulin‐1/ErbB signaling
Gouttenoire, E. A., Lupo, V., Calpena, E., Bartesaghi, L., Schüpfer, F., Médard, J., Maurer, F., Beckmann, J. S., Senderek, J., Palau, F., et al. (2013) · Glia · doi:10.1002/glia.22493 · Cited by 47 · see citing works
Ng, A. A., Logan, A. M., Schmidt, E. J., & Robinson, F. L. (2013) · Human Molecular Genetics · doi:10.1093/hmg/dds562 · Cited by 40 · see citing works
Self-citationAtanasoski, S., Scherer, S. S., Nave, K., & Suter, U. (2002) · Journal of Neuroscience Research · doi:10.1002/jnr.10133 · Cited by 36 · see citing works
Wrabetz, L. G., Feltri, M. L., Kleopa, K. A., & Scherer, S. S. (2004) · Elsevier eBooks · doi:10.1016/b978-012439510-7/50092-9 · Cited by 28 · see citing works
Lee, S. M., Chin, L., & Li, L. (2016) · Molecular Neurobiology · doi:10.1007/s12035-015-9668-2 · Cited by 28 · see citing works
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Phosphoinositides: Regulators of Nervous System Function in Health and Disease
Raghu, P., Joseph, A., Krishnan, H., Singh, P. K., & Saha, S. (2019) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2019.00208 · Cited by 121 · see citing works
Neuroglial transmitophagy and Parkinson's disease
Moráles, I., Sánchez, A., Puertas‐Avendaño, R., Rodriguez‐Sabate, C., Perez‐Barreto, A., & Rodrı́guez, M. (2020) · Glia · doi:10.1002/glia.23839 · Cited by 95 · see citing works
PI3K inhibitors in thrombosis and cardiovascular disease
Durrant, T. N., & Hers, I. (2020) · Clinical and Translational Medicine · doi:10.1186/s40169-020-0261-6 · Cited by 85 · see citing works
Axo-glial interdependence in peripheral nerve development
Fledrich, R., Kungl, T., Nave, K., & Stassart, R. M. (2019) · Development · doi:10.1242/dev.151704 · Cited by 45 · see citing works
Review: Myelin clearance is critical for regeneration after peripheral nerve injury
Yuan, Y., Wang, Y., Wu, S., & Zhao, M. Y. (2022) · Frontiers in Neurology · doi:10.3389/fneur.2022.908148 · Cited by 43 · see citing works
Ulk4 deficiency leads to hypomyelination in mice
Liu, M., Xu, P., Guan, Z., Qian, X., Dockery, P., FitzGerald, U., O’Brien, T., & Shen, S. (2017) · Glia · doi:10.1002/glia.23236 · Cited by 35 · see citing works
Peripheral Nerve Development and the Pathogenesis of Peripheral Neuropathy: the Sorting Point
Previtali, S. C. (2021) · Neurotherapeutics · doi:10.1007/s13311-021-01080-z · Cited by 26 · see citing works
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Chen, Y., Deng, H., & Zhang, N. (2024) · Neural Regeneration Research · doi:10.4103/nrr.nrr-d-23-01948 · Cited by 19 · see citing works
Mammel, A., Delgado, K. C., Chin, A. L., Condon, A. F., Hill, J. Q., Aicher, S. A., Wang, Y., Fedorov, L. M., & Robinson, F. L. (2021) · Human Molecular Genetics · doi:10.1093/hmg/ddab311 · Cited by 18 · see citing works
Self-citationZeng, L., Ma, K., Huang, Y., Liao, B., Zhong, L., Zhao, Y., Lu, Y., Xu, K., Wang, S., Mu, N., et al. (2025) · Biomaterials · doi:10.1016/j.biomaterials.2025.123682 · Cited by 14 · see citing works
Huang, G., Hu, M., Lu, D., & Hong, L. (2021) · Journal of obstetrics and gynaecology research · doi:10.1111/jog.14968 · Cited by 14 · see citing works
Liu, W., Wang, K., Lin, Y.-T., Wang, L., Jin, X., Qiu, Y., Sun, W., Zhang, L., Sun, Y., Dou, X., et al. (2024) · Advanced Science · doi:10.1002/advs.202308823 · Cited by 13 · see citing works
Okagu, I. U., Akerele, O. A., Fillier, T. A., Pham, T. H., Thomas, R., Wilson, K. A., & Cheema, S. K. (2025) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2025.109891 · Cited by 9 · see citing works
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Horie, M., Yoshioka, N., Kusumi, S., Sano, H., Kurose, M., Watanabe‐Iida, I., Hossain, M. I., Chiken, S., Abe, M., Yamamura, K., et al. (2020) · Glia · doi:10.1002/glia.23843 · Cited by 8 · see citing works
McLean, J. W., Wilson, J. A., Tian, T. M., Watson, J. A., VanHart, M., Bean, A. J., Scherer, S. S., Crossman, D. K., Ubogu, E. E., & Wilson, S. M. (2022) · Journal of Neuroscience · doi:10.1523/jneurosci.2481-21.2022 · Cited by 8 · see citing works
Yang, X., Liang, X., Wang, B., Gao, X., Yang, W., Li, J., Cai, H., Tong, Z., & Chen, Y. (2025) · Bioactive Materials · doi:10.1016/j.bioactmat.2025.04.033 · Cited by 8 · see citing works
Rosa, L. D., Fasano, D., Zerillo, L., Valente, V., Izzo, A., Mollo, N., Amodio, G., Polishchuk, E., Polishchuk, R., Melone, M. A. B., et al. (2022) · Frontiers in Genetics · doi:10.3389/fgene.2022.867989 · Cited by 7 · see citing works
Robinson, D. C., Mammel, A., Logan, A. M., Larson, A. A., Schmidt, E. J., Condon, A. F., & Robinson, F. L. (2018) · ASN NEURO · doi:10.1177/1759091418803282 · Cited by 7 · see citing works
Self-citationGambarotto, L., Russo, L., Bresolin, S., Persano, L., D’Amore, R., Ronchi, G., Zen, F. D., Muratori, L., Cani, A., Negro, S., et al. (2024) · Advanced Science · doi:10.1002/advs.202308965 · Cited by 6 · see citing works
Aberrant Neuregulin 1/ErbB Signaling in Charcot-Marie-Tooth Type 4D Disease
Jiang, L., Chen, Y., Huang, J., Tong, W., Jin, L., & Li, L.-X. (2022) · Molecular and Cellular Biology · doi:10.1128/mcb.00559-21 · Cited by 4 · see citing works
Caloric restriction as a nutrition strategy in counteracting peripheral neuropathies
Marinelli, S. (2023) · Elsevier eBooks · doi:10.1016/b978-0-323-89834-8.00003-9
Gambarotto, L., Bresolin, S., Persano, L., D’Amore, R., Ronchi, G., Zen, F. D., Muratori, L., Russo, L., Cani, A., Braghetta, P., et al. (2023) · Research Square · doi:10.21203/rs.3.rs-3596800/v1
Elkader, H. A. E. A., Idrissi, S. E., Sellami, S., & Al‐Shami, A. S. (2025) · Biochemistry · doi:10.5772/intechopen.1008891
The involvement of AHR in peripehral myelination and nerve sheath tumorigenesis
Sampathkumar, N. K. (2018) · theses.fr (ABES) · doi:10.70675/2a3c9c86z51bez4349z9226z1b32c0210df5
Lederbogen, R. C., Hoffjan, S., Köhler, C., Thiels, C., Mau-Holzmann, U. A., Singer, S., Schreiber, S., Purczeld, A., Buchert, R., Yusenko, M. V., et al. (2026) · Human Genetics · doi:10.1007/s00439-026-02856-z
- Authors
- Logan, A. M., Mammel, A. E., Robinson, D. C., Chin, A. L., Condon, A. F., & Robinson, F. L.
- Affiliations
- Oregon Health & Science University (US)
- Corresponding author
- Robinson, Fred L.
- Venue
- Glia
- Publisher
- Wiley
- Published
- 2017-06-15
- Volume
- 65
- Issue
- 9
- Pages
- 1452-1470
- ISSN
- 0894-1491 (ISSN-L)
- 1098-1136
- PMC
- PMC5818149
- OpenAlex
- W2625542865
- Cited by
- 27
- References
- 77
- Citations by year
- 2026: 1 · 2025: 4 · 2024: 3 · 2023: 3 · 2022: 4 · 2021: 4 · 2020: 3 · 2019: 2 · 2018: 2 · 2017: 1
- FWCI
- 1.07
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Glia (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health
- National Institute of Neurological Disorders and Stroke (NS057903 and NS086812)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Hereditary Neurological Disorders
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Nerve injury and regeneration
- Keywords
- Vps34, PIK3C3, phosphatidylinositol 3-phosphate, Schwann cells, myelination, hypomyelination, endosomal trafficking, autophagy, ERBB2, HER3, neuregulin-1, receptor tyrosine kinase signaling, Charcot-Marie-Tooth disease, peripheral neuropathy
- MeSH terms
- Neuronal Outgrowth, Animals, Autophagy, Axons, Female, Male, Mice, Inbred C57BL, Motor Activity, Peripheral Nerves, Phosphorylation, Endosomes, Schwann Cells, Sciatic Nerve, Signal Transduction, Mice, Knockout, Receptor, ErbB-2, Erb-b2 Receptor Tyrosine Kinases, Receptor, ErbB-3, Cell Proliferation, Mice, 129 Strain, Class III Phosphatidylinositol 3-Kinases
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