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. 1994 Dec 2;127(6):1603–1616. doi: 10.1083/jcb.127.6.1603

The polymeric immunoglobulin receptor accumulates in specialized endosomes but not synaptic vesicles within the neurites of transfected neuroendocrine PC12 cells

PMCID: PMC2120272  PMID: 7798315

Abstract

We have expressed in neuroendocrine PC12 cells the polymeric immunoglobulin receptor (pIgR), which is normally targeted from the basolateral to the apical surface of epithelial cells. In the presence of nerve growth factor, PC12 cells extend neurites which contain synaptic vesicle-like structures and regulated secretory granules. By immunofluorescence microscopy, pIgR, like the synaptic vesicle protein synaptophysin, accumulates in both the cell body and the neurites. On the other hand, the transferrin receptor, which normally recycles at the basolateral surface in epithelial cells, and the cation-independent mannose 6-phosphate receptor, a marker of late endosomes, are largely restricted to the cell body. pIgR internalizes ligand into endosomes within the cell body and the neurites, while uptake of ligand by the low density lipoprotein receptor occurs primarily into endosomes within the cell body. We conclude that transport of membrane proteins to PC12 neurites as well as to specialized endosomes within these processes is selective and appears to be governed by similar mechanisms that dictate sorting in epithelial cells. Additionally, two types of endosomes can be identified in polarized PC12 cells by the differential uptake of ligand, a housekeeping type in the cell bodies and a specialized endosome in the neurites. Recent findings suggest that specialized axonal endosomes in neurons are likely to give rise to synaptic vesicles (Mundigl, O., M. Matteoli, L. Daniell, A. Thomas-Reetz, A. Metcalf, R. Jahn, and P. De Camilli. 1993. J. Cell Biol. 122:1207- 1221). Although pIgR reaches the specialized endosomes in the neurites of PC12 cells, we find by subcellular fractionation that under a variety of conditions it is efficiently excluded from synaptic vesicle- like structures as well as from secretory granules.

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Selected References

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  1. Apodaca G., Katz L. A., Mostov K. E. Receptor-mediated transcytosis of IgA in MDCK cells is via apical recycling endosomes. J Cell Biol. 1994 Apr;125(1):67–86. doi: 10.1083/jcb.125.1.67. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Aroeti B., Kosen P. A., Kuntz I. D., Cohen F. E., Mostov K. E. Mutational and secondary structural analysis of the basolateral sorting signal of the polymeric immunoglobulin receptor. J Cell Biol. 1993 Dec;123(5):1149–1160. doi: 10.1083/jcb.123.5.1149. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Aroeti B., Mostov K. E. Polarized sorting of the polymeric immunoglobulin receptor in the exocytotic and endocytotic pathways is controlled by the same amino acids. EMBO J. 1994 May 15;13(10):2297–2304. doi: 10.1002/j.1460-2075.1994.tb06513.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Barroso M., Sztul E. S. Basolateral to apical transcytosis in polarized cells is indirect and involves BFA and trimeric G protein sensitive passage through the apical endosome. J Cell Biol. 1994 Jan;124(1-2):83–100. doi: 10.1083/jcb.124.1.83. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bauerfeind R., Régnier-Vigouroux A., Flatmark T., Huttner W. B. Selective storage of acetylcholine, but not catecholamines, in neuroendocrine synaptic-like microvesicles of early endosomal origin. Neuron. 1993 Jul;11(1):105–121. doi: 10.1016/0896-6273(93)90275-v. [DOI] [PubMed] [Google Scholar]
  6. Beisiegel U., Schneider W. J., Goldstein J. L., Anderson R. G., Brown M. S. Monoclonal antibodies to the low density lipoprotein receptor as probes for study of receptor-mediated endocytosis and the genetics of familial hypercholesterolemia. J Biol Chem. 1981 Nov 25;256(22):11923–11931. [PubMed] [Google Scholar]
  7. Bomsel M., Prydz K., Parton R. G., Gruenberg J., Simons K. Endocytosis in filter-grown Madin-Darby canine kidney cells. J Cell Biol. 1989 Dec;109(6 Pt 2):3243–3258. doi: 10.1083/jcb.109.6.3243. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Bordier C. Phase separation of integral membrane proteins in Triton X-114 solution. J Biol Chem. 1981 Feb 25;256(4):1604–1607. [PubMed] [Google Scholar]
  9. Breitfeld P. P., Casanova J. E., Harris J. M., Simister N. E., Mostov K. E. Expression and analysis of the polymeric immunoglobulin receptor in Madin-Darby canine kidney cells using retroviral vectors. Methods Cell Biol. 1989;32:329–337. doi: 10.1016/s0091-679x(08)61178-4. [DOI] [PubMed] [Google Scholar]
  10. Breitfeld P. P., Casanova J. E., McKinnon W. C., Mostov K. E. Deletions in the cytoplasmic domain of the polymeric immunoglobulin receptor differentially affect endocytotic rate and postendocytotic traffic. J Biol Chem. 1990 Aug 15;265(23):13750–13757. [PubMed] [Google Scholar]
  11. Brewer C. B., Roth M. G. A single amino acid change in the cytoplasmic domain alters the polarized delivery of influenza virus hemagglutinin. J Cell Biol. 1991 Aug;114(3):413–421. doi: 10.1083/jcb.114.3.413. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Böj S., Goldstein M., Fischer-Colbrie R., Dahlström A. Calcitonin gene-related peptide and chromogranin A: presence and intra-axonal transport in lumbar motor neurons in the rat, a comparison with synaptic vesicle antigens in immunohistochemical studies. Neuroscience. 1989;30(2):479–501. doi: 10.1016/0306-4522(89)90267-4. [DOI] [PubMed] [Google Scholar]
  13. Cameron P. L., Südhof T. C., Jahn R., De Camilli P. Colocalization of synaptophysin with transferrin receptors: implications for synaptic vesicle biogenesis. J Cell Biol. 1991 Oct;115(1):151–164. doi: 10.1083/jcb.115.1.151. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Cardone M. H., Smith B. L., Song W., Mochly-Rosen D., Mostov K. E. Phorbol myristate acetate-mediated stimulation of transcytosis and apical recycling in MDCK cells. J Cell Biol. 1994 Mar;124(5):717–727. doi: 10.1083/jcb.124.5.717. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Casanova J. E., Breitfeld P. P., Ross S. A., Mostov K. E. Phosphorylation of the polymeric immunoglobulin receptor required for its efficient transcytosis. Science. 1990 May 11;248(4956):742–745. doi: 10.1126/science.2110383. [DOI] [PubMed] [Google Scholar]
  16. Clift-O'Grady L., Linstedt A. D., Lowe A. W., Grote E., Kelly R. B. Biogenesis of synaptic vesicle-like structures in a pheochromocytoma cell line PC-12. J Cell Biol. 1990 May;110(5):1693–1703. doi: 10.1083/jcb.110.5.1693. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Costello B., Lin L. H., Meymandi A., Bock S., Norden J. J., Freeman J. A. Expression of the growth- and plasticity-associated neuronal protein, GAP-43, in PC12 pheochromocytoma cells. Prog Brain Res. 1991;89:47–67. [PubMed] [Google Scholar]
  18. Craig A. M., Jareb M., Banker G. Neuronal polarity. Curr Opin Neurobiol. 1992 Oct;2(5):602–606. doi: 10.1016/0959-4388(92)90025-g. [DOI] [PubMed] [Google Scholar]
  19. Davis C. G., Lehrman M. A., Russell D. W., Anderson R. G., Brown M. S., Goldstein J. L. The J.D. mutation in familial hypercholesterolemia: amino acid substitution in cytoplasmic domain impedes internalization of LDL receptors. Cell. 1986 Apr 11;45(1):15–24. doi: 10.1016/0092-8674(86)90533-7. [DOI] [PubMed] [Google Scholar]
  20. De Camilli P., Jahn R. Pathways to regulated exocytosis in neurons. Annu Rev Physiol. 1990;52:625–645. doi: 10.1146/annurev.ph.52.030190.003205. [DOI] [PubMed] [Google Scholar]
  21. Deitcher D. L., Neutra M. R., Mostov K. E. Functional expression of the polymeric immunoglobulin receptor from cloned cDNA in fibroblasts. J Cell Biol. 1986 Mar;102(3):911–919. doi: 10.1083/jcb.102.3.911. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Dotti C. G., Parton R. G., Simons K. Polarized sorting of glypiated proteins in hippocampal neurons. Nature. 1991 Jan 10;349(6305):158–161. doi: 10.1038/349158a0. [DOI] [PubMed] [Google Scholar]
  23. Dotti C. G., Simons K. Polarized sorting of viral glycoproteins to the axon and dendrites of hippocampal neurons in culture. Cell. 1990 Jul 13;62(1):63–72. doi: 10.1016/0092-8674(90)90240-f. [DOI] [PubMed] [Google Scholar]
  24. Elferink L. A., Peterson M. R., Scheller R. H. A role for synaptotagmin (p65) in regulated exocytosis. Cell. 1993 Jan 15;72(1):153–159. doi: 10.1016/0092-8674(93)90059-y. [DOI] [PubMed] [Google Scholar]
  25. Fletcher T. L., Cameron P., De Camilli P., Banker G. The distribution of synapsin I and synaptophysin in hippocampal neurons developing in culture. J Neurosci. 1991 Jun;11(6):1617–1626. doi: 10.1523/JNEUROSCI.11-06-01617.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Forte J. G., Hanzel D. K., Urushidani T., Wolosin J. M. Pumps and pathways for gastric HCl secretion. Ann N Y Acad Sci. 1989;574:145–158. doi: 10.1111/j.1749-6632.1989.tb25153.x. [DOI] [PubMed] [Google Scholar]
  27. Fuller S. D., Simons K. Transferrin receptor polarity and recycling accuracy in "tight" and "leaky" strains of Madin-Darby canine kidney cells. J Cell Biol. 1986 Nov;103(5):1767–1779. doi: 10.1083/jcb.103.5.1767. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Ginzburg I. Neuronal polarity: targeting of microtubule components into axons and dendrites. Trends Biochem Sci. 1991 Jul;16(7):257–261. doi: 10.1016/0968-0004(91)90099-h. [DOI] [PubMed] [Google Scholar]
  29. Goldstein J. L., Basu S. K., Brown M. S. Receptor-mediated endocytosis of low-density lipoprotein in cultured cells. Methods Enzymol. 1983;98:241–260. doi: 10.1016/0076-6879(83)98152-1. [DOI] [PubMed] [Google Scholar]
  30. Gorman C. M., Howard B. H., Reeves R. Expression of recombinant plasmids in mammalian cells is enhanced by sodium butyrate. Nucleic Acids Res. 1983 Nov 11;11(21):7631–7648. doi: 10.1093/nar/11.21.7631. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Goslin K., Schreyer D. J., Skene J. H., Banker G. Development of neuronal polarity: GAP-43 distinguishes axonal from dendritic growth cones. Nature. 1988 Dec 15;336(6200):672–674. doi: 10.1038/336672a0. [DOI] [PubMed] [Google Scholar]
  32. Green S. A., Kelly R. B. Low density lipoprotein receptor and cation-independent mannose 6-phosphate receptor are transported from the cell surface to the Golgi apparatus at equal rates in PC12 cells. J Cell Biol. 1992 Apr;117(1):47–55. doi: 10.1083/jcb.117.1.47. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Green S. A., Setiadi H., McEver R. P., Kelly R. B. The cytoplasmic domain of P-selectin contains a sorting determinant that mediates rapid degradation in lysosomes. J Cell Biol. 1994 Feb;124(4):435–448. doi: 10.1083/jcb.124.4.435. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Hirt R. P., Hughes G. J., Frutiger S., Michetti P., Perregaux C., Poulain-Godefroy O., Jeanguenat N., Neutra M. R., Kraehenbuhl J. P. Transcytosis of the polymeric Ig receptor requires phosphorylation of serine 664 in the absence but not the presence of dimeric IgA. Cell. 1993 Jul 30;74(2):245–255. doi: 10.1016/0092-8674(93)90416-n. [DOI] [PubMed] [Google Scholar]
  35. Huber L. A., Pimplikar S., Parton R. G., Virta H., Zerial M., Simons K. Rab8, a small GTPase involved in vesicular traffic between the TGN and the basolateral plasma membrane. J Cell Biol. 1993 Oct;123(1):35–45. doi: 10.1083/jcb.123.1.35. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Huber L. A., de Hoop M. J., Dupree P., Zerial M., Simons K., Dotti C. Protein transport to the dendritic plasma membrane of cultured neurons is regulated by rab8p. J Cell Biol. 1993 Oct;123(1):47–55. doi: 10.1083/jcb.123.1.47. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Hudson A. W., Fingar D. C., Seidner G. A., Griffiths G., Burke B., Birnbaum M. J. Targeting of the "insulin-responsive" glucose transporter (GLUT4) to the regulated secretory pathway in PC12 cells. J Cell Biol. 1993 Aug;122(3):579–588. doi: 10.1083/jcb.122.3.579. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Hughson E. J., Hopkins C. R. Endocytic pathways in polarized Caco-2 cells: identification of an endosomal compartment accessible from both apical and basolateral surfaces. J Cell Biol. 1990 Feb;110(2):337–348. doi: 10.1083/jcb.110.2.337. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Ikonen E., Parton R. G., Hunziker W., Simons K., Dotti C. G. Transcytosis of the polymeric immunoglobulin receptor in cultured hippocampal neurons. Curr Biol. 1993 Oct 1;3(10):635–644. doi: 10.1016/0960-9822(93)90061-r. [DOI] [PubMed] [Google Scholar]
  40. Jahn R., Schiebler W., Ouimet C., Greengard P. A 38,000-dalton membrane protein (p38) present in synaptic vesicles. Proc Natl Acad Sci U S A. 1985 Jun;82(12):4137–4141. doi: 10.1073/pnas.82.12.4137. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Jahn R., Südhof T. C. Synaptic vesicle traffic: rush hour in the nerve terminal. J Neurochem. 1993 Jul;61(1):12–21. doi: 10.1111/j.1471-4159.1993.tb03533.x. [DOI] [PubMed] [Google Scholar]
  42. Johnston P. A., Cameron P. L., Stukenbrok H., Jahn R., De Camilli P., Südhof T. C. Synaptophysin is targeted to similar microvesicles in CHO and PC12 cells. EMBO J. 1989 Oct;8(10):2863–2872. doi: 10.1002/j.1460-2075.1989.tb08434.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Kelly R. B., Grote E. Protein targeting in the neuron. Annu Rev Neurosci. 1993;16:95–127. doi: 10.1146/annurev.ne.16.030193.000523. [DOI] [PubMed] [Google Scholar]
  44. Linstedt A. D., Kelly R. B. Synaptophysin is sorted from endocytotic markers in neuroendocrine PC12 cells but not transfected fibroblasts. Neuron. 1991 Aug;7(2):309–317. doi: 10.1016/0896-6273(91)90269-6. [DOI] [PubMed] [Google Scholar]
  45. Maher P. A., Singer S. J. Anomalous interaction of the acetylcholine receptor protein with the nonionic detergent Triton X-114. Proc Natl Acad Sci U S A. 1985 Feb;82(4):958–962. doi: 10.1073/pnas.82.4.958. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Margolis T. P., Marchand C. M., Kistler H. B., Jr, LaVail L. H. Uptake and anterograde axonal transport of wheat germ agglutinin from retina to optic tectum in the chick. J Cell Biol. 1981 Apr;89(1):152–156. doi: 10.1083/jcb.89.1.152. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Matter K., Whitney J. A., Yamamoto E. M., Mellman I. Common signals control low density lipoprotein receptor sorting in endosomes and the Golgi complex of MDCK cells. Cell. 1993 Sep 24;74(6):1053–1064. doi: 10.1016/0092-8674(93)90727-8. [DOI] [PubMed] [Google Scholar]
  48. Mostov K. E., Deitcher D. L. Polymeric immunoglobulin receptor expressed in MDCK cells transcytoses IgA. Cell. 1986 Aug 15;46(4):613–621. doi: 10.1016/0092-8674(86)90887-1. [DOI] [PubMed] [Google Scholar]
  49. Mostov K. E., Friedlander M., Blobel G. The receptor for transepithelial transport of IgA and IgM contains multiple immunoglobulin-like domains. Nature. 1984 Mar 1;308(5954):37–43. doi: 10.1038/308037a0. [DOI] [PubMed] [Google Scholar]
  50. Mostov K. E. Transepithelial transport of immunoglobulins. Annu Rev Immunol. 1994;12:63–84. doi: 10.1146/annurev.iy.12.040194.000431. [DOI] [PubMed] [Google Scholar]
  51. Mostov K., Apodaca G., Aroeti B., Okamoto C. Plasma membrane protein sorting in polarized epithelial cells. J Cell Biol. 1992 Feb;116(3):577–583. doi: 10.1083/jcb.116.3.577. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Muller S. R., Huff S. Y., Goode B. L., Marschall L., Chang J., Feinstein S. C. Molecular analysis of the nerve growth factor inducible ornithine decarboxylase gene in PC12 cells. J Neurosci Res. 1993 Feb 15;34(3):304–314. doi: 10.1002/jnr.490340307. [DOI] [PubMed] [Google Scholar]
  53. Muller S. R., Sullivan P. D., Clegg D. O., Feinstein S. C. Efficient transfection and expression of heterologous genes in PC12 cells. DNA Cell Biol. 1990 Apr;9(3):221–229. doi: 10.1089/dna.1990.9.221. [DOI] [PubMed] [Google Scholar]
  54. Mundigl O., Matteoli M., Daniell L., Thomas-Reetz A., Metcalf A., Jahn R., De Camilli P. Synaptic vesicle proteins and early endosomes in cultured hippocampal neurons: differential effects of Brefeldin A in axon and dendrites. J Cell Biol. 1993 Sep;122(6):1207–1221. doi: 10.1083/jcb.122.6.1207. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Musil L. S., Baenziger J. U. Cleavage of membrane secretory component to soluble secretory component occurs on the cell surface of rat hepatocyte monolayers. J Cell Biol. 1987 Jun;104(6):1725–1733. doi: 10.1083/jcb.104.6.1725. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Navone F., Jahn R., Di Gioia G., Stukenbrok H., Greengard P., De Camilli P. Protein p38: an integral membrane protein specific for small vesicles of neurons and neuroendocrine cells. J Cell Biol. 1986 Dec;103(6 Pt 1):2511–2527. doi: 10.1083/jcb.103.6.2511. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Parton R. G., Prydz K., Bomsel M., Simons K., Griffiths G. Meeting of the apical and basolateral endocytic pathways of the Madin-Darby canine kidney cell in late endosomes. J Cell Biol. 1989 Dec;109(6 Pt 2):3259–3272. doi: 10.1083/jcb.109.6.3259. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Parton R. G., Simons K., Dotti C. G. Axonal and dendritic endocytic pathways in cultured neurons. J Cell Biol. 1992 Oct;119(1):123–137. doi: 10.1083/jcb.119.1.123. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Pietrini G., Suh Y. J., Edelmann L., Rudnick G., Caplan M. J. The axonal gamma-aminobutyric acid transporter GAT-1 is sorted to the apical membranes of polarized epithelial cells. J Biol Chem. 1994 Feb 11;269(6):4668–4674. [PubMed] [Google Scholar]
  60. Powell S. K., Lisanti M. P., Rodriguez-Boulan E. J. Thy-1 expresses two signals for apical localization in epithelial cells. Am J Physiol. 1991 Apr;260(4 Pt 1):C715–C720. doi: 10.1152/ajpcell.1991.260.4.C715. [DOI] [PubMed] [Google Scholar]
  61. Rodriguez-Boulan E., Powell S. K. Polarity of epithelial and neuronal cells. Annu Rev Cell Biol. 1992;8:395–427. doi: 10.1146/annurev.cb.08.110192.002143. [DOI] [PubMed] [Google Scholar]
  62. Ruda M., Coulter J. D. Axonal and transneuronal transport of wheat germ agglutinin demonstrated by immunocytochemistry. Brain Res. 1982 Oct 14;249(2):237–246. doi: 10.1016/0006-8993(82)90057-9. [DOI] [PubMed] [Google Scholar]
  63. Sano M., Katoh-Semba R., Kitajima S., Sato C. Changes in levels of microtubule-associated proteins in relation to the outgrowth of neurites from PC12D cells, a forskolin- and nerve growth factor-responsive subline of PC12 pheochromocytoma cells. Brain Res. 1990 Mar 5;510(2):269–276. doi: 10.1016/0006-8993(90)91377-s. [DOI] [PubMed] [Google Scholar]
  64. Sheetz M. P., Steuer E. R., Schroer T. A. The mechanism and regulation of fast axonal transport. Trends Neurosci. 1989 Nov;12(11):474–478. doi: 10.1016/0166-2236(89)90099-4. [DOI] [PubMed] [Google Scholar]
  65. Slot J. W., Geuze H. J., Gigengack S., Lienhard G. E., James D. E. Immuno-localization of the insulin regulatable glucose transporter in brown adipose tissue of the rat. J Cell Biol. 1991 Apr;113(1):123–135. doi: 10.1083/jcb.113.1.123. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Solari R., Kühn L., Kraehenbuhl J. P. Antibodies recognizing different domains of the polymeric immunoglobulin receptor. J Biol Chem. 1985 Jan 25;260(2):1141–1145. [PubMed] [Google Scholar]
  67. Song W., Bomsel M., Casanova J., Vaerman J. P., Mostov K. Stimulation of transcytosis of the polymeric immunoglobulin receptor by dimeric IgA. Proc Natl Acad Sci U S A. 1994 Jan 4;91(1):163–166. doi: 10.1073/pnas.91.1.163. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Steindler D. A., Deniau J. M. Anatomical evidence for collateral branching of substantia nigra neurons: a combined horseradish peroxidase and [3H]wheat germ agglutinin axonal transport study in the rat. Brain Res. 1980 Aug 25;196(1):228–236. doi: 10.1016/0006-8993(80)90729-5. [DOI] [PubMed] [Google Scholar]
  69. Sztul E., Colombo M., Stahl P., Samanta R. Control of protein traffic between distinct plasma membrane domains. Requirement for a novel 108,000 protein in the fusion of transcytotic vesicles with the apical plasma membrane. J Biol Chem. 1993 Jan 25;268(3):1876–1885. [PubMed] [Google Scholar]
  70. Vallee R. B., Bloom G. S. Mechanisms of fast and slow axonal transport. Annu Rev Neurosci. 1991;14:59–92. doi: 10.1146/annurev.ne.14.030191.000423. [DOI] [PubMed] [Google Scholar]
  71. Van Hooff C. O., Holthuis J. C., Oestreicher A. B., Boonstra J., De Graan P. N., Gispen W. H. Nerve growth factor-induced changes in the intracellular localization of the protein kinase C substrate B-50 in pheochromocytoma PC12 cells. J Cell Biol. 1989 Mar;108(3):1115–1125. doi: 10.1083/jcb.108.3.1115. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Verkman A. S. Water channels in cell membranes. Annu Rev Physiol. 1992;54:97–108. doi: 10.1146/annurev.ph.54.030192.000525. [DOI] [PubMed] [Google Scholar]
  73. White S., Miller K., Hopkins C., Trowbridge I. S. Monoclonal antibodies against defined epitopes of the human transferrin receptor cytoplasmic tail. Biochim Biophys Acta. 1992 Jul 22;1136(1):28–34. doi: 10.1016/0167-4889(92)90081-l. [DOI] [PubMed] [Google Scholar]
  74. Wiedenmann B., Rehm H., Knierim M., Becker C. M. Fractionation of synaptophysin-containing vesicles from rat brain and cultured PC12 pheochromocytoma cells. FEBS Lett. 1988 Nov 21;240(1-2):71–77. doi: 10.1016/0014-5793(88)80342-9. [DOI] [PubMed] [Google Scholar]
  75. Zuber M. X., Strittmatter S. M., Fishman M. C. A membrane-targeting signal in the amino terminus of the neuronal protein GAP-43. Nature. 1989 Sep 28;341(6240):345–348. doi: 10.1038/341345a0. [DOI] [PubMed] [Google Scholar]

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