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. 1988 Apr 1;106(4):1289–1297. doi: 10.1083/jcb.106.4.1289

Neurite extension of chicken peripheral nervous system neurons on fibronectin: relative importance of specific adhesion sites in the central cell-binding domain and the alternatively spliced type III connecting segment

PMCID: PMC2115016  PMID: 3360854

Abstract

Fibronectin contains at least two domains that support cell adhesion. One is the central cell-binding domain that is recognized by a variety of cell types, including fibroblasts. The second, originally identified by its ability to support melanoma cell adhesion, is located in the alternatively spliced type III connecting segment (IIICS). Using specific adhesive ligands and inhibitory probes, we have examined the role of each of these domains in fibronectin-mediated neurite extension of neurons from chick embryo dorsal root and sympathetic ganglia. In studies using explanted ganglia, both fl3, a 75-kD tryptic fragment of human plasma fibronectin containing the central cell-binding domain, and CS1-IgG, a synthetic peptide-IgG conjugate containing the principal cell adhesion site from the IIICS, supported neurite outgrowth after adsorption onto the substrate. The maximal activities of fl3 and CSl- IgG were 45-55% and 25-30% that of intact fibronectin, respectively. Co- coating of the substrate with f13 and CS1-IgG produced an additive stimulation of neurite outgrowth, the extent of which approached that obtained with fibronectin. Similar results were obtained with purified neuronal cell preparations isolated by tryptic dissociation of dorsal root ganglia. In complementary studies, blockage of the adhesive function of either the central cell-binding domain (with mAb 333, an antiadhesive monoclonal antibody) or the IIICS (with CS1 peptide), resulted in approximately 60 or 30% reduction in fibronectin-mediated neurite outgrowth, respectively. When tested in combination, the inhibitory activities of mAb 333 and CSl were additive. From these results, we conclude that neurons from the peripheral nervous system can extend neurites on both the central cell-binding domain and the IIICS region of fibronectin, and that these cells are therefore the first normal, embryonic cell type shown to adhere to the IIICS. These results suggest that spatiotemporal fluctuations in the alternative mRNA splicing of the IIICS region of fibronectin may be important in regulation of cell adhesive events during development of the peripheral nervous system.

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Selected References

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  1. Adler R., Jerdan J., Hewitt A. T. Responses of cultured neural retinal cells to substratum-bound laminin and other extracellular matrix molecules. Dev Biol. 1985 Nov;112(1):100–114. doi: 10.1016/0012-1606(85)90124-1. [DOI] [PubMed] [Google Scholar]
  2. Akers R. M., Mosher D. F., Lilien J. E. Promotion of retinal neurite outgrowth by substratum-bound fibronectin. Dev Biol. 1981 Aug;86(1):179–188. doi: 10.1016/0012-1606(81)90328-6. [DOI] [PubMed] [Google Scholar]
  3. Akeson R., Warren S. L. PC12 adhesion and neurite formation on selected substrates are inhibited by some glycosaminoglycans and a fibronectin-derived tetrapeptide. Exp Cell Res. 1986 Feb;162(2):347–362. doi: 10.1016/0014-4827(86)90340-x. [DOI] [PubMed] [Google Scholar]
  4. Akiyama S. K., Hasegawa E., Hasegawa T., Yamada K. M. The interaction of fibronectin fragments with fibroblastic cells. J Biol Chem. 1985 Oct 25;260(24):13256–13260. [PubMed] [Google Scholar]
  5. Akiyama S. K., Yamada K. M. The interaction of plasma fibronectin with fibroblastic cells in suspension. J Biol Chem. 1985 Apr 10;260(7):4492–4500. [PubMed] [Google Scholar]
  6. Akiyama S. K., Yamada S. S., Yamada K. M. Characterization of a 140-kD avian cell surface antigen as a fibronectin-binding molecule. J Cell Biol. 1986 Feb;102(2):442–448. doi: 10.1083/jcb.102.2.442. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Al-Ghaith L. K., Lewis J. H. Pioneer growth cones in virgin mesenchyme: an electron-microscope study in the developing chick wing. J Embryol Exp Morphol. 1982 Apr;68:149–160. [PubMed] [Google Scholar]
  8. Baron-Van Evercooren A., Kleinman H. K., Ohno S., Marangos P., Schwartz J. P., Dubois-Dalcq M. E. Nerve growth factor, laminin, and fibronectin promote neurite growth in human fetal sensory ganglia cultures. J Neurosci Res. 1982;8(2-3):179–193. doi: 10.1002/jnr.490080208. [DOI] [PubMed] [Google Scholar]
  9. Bate C. M. Pioneer neurones in an insect embryo. Nature. 1976 Mar 4;260(5546):54–56. doi: 10.1038/260054a0. [DOI] [PubMed] [Google Scholar]
  10. Berlot J., Goodman C. S. Guidance of peripheral pioneer neurons in the grasshopper: adhesive hierarchy of epithelial and neuronal surfaces. Science. 1984 Feb 3;223(4635):493–496. doi: 10.1126/science.223.4635.493. [DOI] [PubMed] [Google Scholar]
  11. Bozyczko D., Horwitz A. F. The participation of a putative cell surface receptor for laminin and fibronectin in peripheral neurite extension. J Neurosci. 1986 May;6(5):1241–1251. doi: 10.1523/JNEUROSCI.06-05-01241.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Bunge R. P., Bunge M. B., Eldridge C. F. Linkage between axonal ensheathment and basal lamina production by Schwann cells. Annu Rev Neurosci. 1986;9:305–328. doi: 10.1146/annurev.ne.09.030186.001513. [DOI] [PubMed] [Google Scholar]
  13. Carbonetto S. T., Gruver M. M., Turner D. C. Nerve fiber growth on defined hydrogel substrates. Science. 1982 May 21;216(4548):897–899. doi: 10.1126/science.7079743. [DOI] [PubMed] [Google Scholar]
  14. Castellani P., Siri A., Rosellini C., Infusini E., Borsi L., Zardi L. Transformed human cells release different fibronectin variants than do normal cells. J Cell Biol. 1986 Nov;103(5):1671–1677. doi: 10.1083/jcb.103.5.1671. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Cornbrooks C. J., Carey D. J., McDonald J. A., Timpl R., Bunge R. P. In vivo and in vitro observations on laminin production by Schwann cells. Proc Natl Acad Sci U S A. 1983 Jun;80(12):3850–3854. doi: 10.1073/pnas.80.12.3850. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Edgar D., Timpl R., Thoenen H. The heparin-binding domain of laminin is responsible for its effects on neurite outgrowth and neuronal survival. EMBO J. 1984 Jul;3(7):1463–1468. doi: 10.1002/j.1460-2075.1984.tb01997.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Ehrismann R., Chiquet M., Turner D. C. Mode of action of fibronectin in promoting chicken myoblast attachment. Mr = 60,000 gelatin-binding fragment binds native fibronectin. J Biol Chem. 1981 Apr 25;256(8):4056–4062. [PubMed] [Google Scholar]
  18. Faivre-Bauman A., Puymirat J., Loudes C., Barret A., Tixier-Vidal A. Laminin promotes attachment and neurite elongation of fetal hypothalamic neurons grown in serum-free medium. Neurosci Lett. 1984 Jan 27;44(1):83–89. doi: 10.1016/0304-3940(84)90225-8. [DOI] [PubMed] [Google Scholar]
  19. Goodman C. S., Bastiani M. J., Doe C. Q., du Lac S., Helfand S. L., Kuwada J. Y., Thomas J. B. Cell recognition during neuronal development. Science. 1984 Sep 21;225(4668):1271–1279. doi: 10.1126/science.6474176. [DOI] [PubMed] [Google Scholar]
  20. Hahn L. H., Yamada K. M. Isolation and biological characterization of active fragments of the adhesive glycoprotein fibronectin. Cell. 1979 Dec;18(4):1043–1051. doi: 10.1016/0092-8674(79)90217-4. [DOI] [PubMed] [Google Scholar]
  21. Hall D. E., Neugebauer K. M., Reichardt L. F. Embryonic neural retinal cell response to extracellular matrix proteins: developmental changes and effects of the cell substratum attachment antibody (CSAT). J Cell Biol. 1987 Mar;104(3):623–634. doi: 10.1083/jcb.104.3.623. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Hammarback J. A., Letourneau P. C. Neurite extension across regions of low cell-substratum adhesivity: implications for the guidepost hypothesis of axonal pathfinding. Dev Biol. 1986 Oct;117(2):655–662. doi: 10.1016/0012-1606(86)90334-9. [DOI] [PubMed] [Google Scholar]
  23. Hammarback J. A., Palm S. L., Furcht L. T., Letourneau P. C. Guidance of neurite outgrowth by pathways of substratum-adsorbed laminin. J Neurosci Res. 1985;13(1-2):213–220. doi: 10.1002/jnr.490130115. [DOI] [PubMed] [Google Scholar]
  24. Hasegawa T., Hasegawa E., Chen W. T., Yamada K. M. Characterization of a membrane-associated glycoprotein complex implicated in cell adhesion to fibronectin. J Cell Biochem. 1985;28(4):307–318. doi: 10.1002/jcb.240280409. [DOI] [PubMed] [Google Scholar]
  25. Hatten M. E., Furie M. B., Rifkin D. B. Binding of developing mouse cerebellar cells to fibronectin: a possible mechanism for the formation of the external granular layer. J Neurosci. 1982 Sep;2(9):1195–1206. doi: 10.1523/JNEUROSCI.02-09-01195.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Hayashi M., Yamada K. M. Domain structure of the carboxyl-terminal half of human plasma fibronectin. J Biol Chem. 1983 Mar 10;258(5):3332–3340. [PubMed] [Google Scholar]
  27. Ho R. K., Goodman C. S. Peripheral pathways are pioneered by an array of central and peripheral neurones in grasshopper embryos. Nature. 1982 Jun 3;297(5865):404–406. doi: 10.1038/297404a0. [DOI] [PubMed] [Google Scholar]
  28. Horwitz A., Duggan K., Greggs R., Decker C., Buck C. The cell substrate attachment (CSAT) antigen has properties of a receptor for laminin and fibronectin. J Cell Biol. 1985 Dec;101(6):2134–2144. doi: 10.1083/jcb.101.6.2134. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Humphries M. J., Akiyama S. K., Komoriya A., Olden K., Yamada K. M. Identification of an alternatively spliced site in human plasma fibronectin that mediates cell type-specific adhesion. J Cell Biol. 1986 Dec;103(6 Pt 2):2637–2647. doi: 10.1083/jcb.103.6.2637. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Humphries M. J., Komoriya A., Akiyama S. K., Olden K., Yamada K. M. Identification of two distinct regions of the type III connecting segment of human plasma fibronectin that promote cell type-specific adhesion. J Biol Chem. 1987 May 15;262(14):6886–6892. [PubMed] [Google Scholar]
  31. Hynes R. O., Patel R., Miller R. H. Migration of neuroblasts along preexisting axonal tracts during prenatal cerebellar development. J Neurosci. 1986 Mar;6(3):867–876. doi: 10.1523/JNEUROSCI.06-03-00867.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Hynes R. Molecular biology of fibronectin. Annu Rev Cell Biol. 1985;1:67–90. doi: 10.1146/annurev.cb.01.110185.000435. [DOI] [PubMed] [Google Scholar]
  33. Kornblihtt A. R., Umezawa K., Vibe-Pedersen K., Baralle F. E. Primary structure of human fibronectin: differential splicing may generate at least 10 polypeptides from a single gene. EMBO J. 1985 Jul;4(7):1755–1759. doi: 10.1002/j.1460-2075.1985.tb03847.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Letourneau P. C. Cell-substratum adhesion of neurite growth cones, and its role in neurite elongation. Exp Cell Res. 1979 Nov;124(1):127–138. doi: 10.1016/0014-4827(79)90263-5. [DOI] [PubMed] [Google Scholar]
  35. Letourneau P. C. Cell-to-substratum adhesion and guidance of axonal elongation. Dev Biol. 1975 May;44(1):92–101. doi: 10.1016/0012-1606(75)90379-6. [DOI] [PubMed] [Google Scholar]
  36. Liesi P., Dahl D., Vaheri A. Neurons cultured from developing rat brain attach and spread preferentially to laminin. J Neurosci Res. 1984;11(3):241–251. doi: 10.1002/jnr.490110304. [DOI] [PubMed] [Google Scholar]
  37. Liesi P. Do neurons in the vertebrate CNS migrate on laminin? EMBO J. 1985 May;4(5):1163–1170. doi: 10.1002/j.1460-2075.1985.tb03755.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Liesi P., Kaakkola S., Dahl D., Vaheri A. Laminin is induced in astrocytes of adult brain by injury. EMBO J. 1984 Mar;3(3):683–686. doi: 10.1002/j.1460-2075.1984.tb01867.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Linder E., Vaheri A., Ruoslahti E., Wartiovaara J. Distribution of fibroblast surface antigen in the developing chick embryo. J Exp Med. 1975 Jul 1;142(1):41–49. doi: 10.1084/jem.142.1.41. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Manthorpe M., Engvall E., Ruoslahti E., Longo F. M., Davis G. E., Varon S. Laminin promotes neuritic regeneration from cultured peripheral and central neurons. J Cell Biol. 1983 Dec;97(6):1882–1890. doi: 10.1083/jcb.97.6.1882. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Mayer B. W., Jr, Hay E. D., Hynes R. O. Immunocytochemical localization of fibronectin in embryonic chick trunk and area vasculosa. Dev Biol. 1981 Mar;82(2):267–286. doi: 10.1016/0012-1606(81)90451-6. [DOI] [PubMed] [Google Scholar]
  42. McCarthy J. B., Hagen S. T., Furcht L. T. Human fibronectin contains distinct adhesion- and motility-promoting domains for metastatic melanoma cells. J Cell Biol. 1986 Jan;102(1):179–188. doi: 10.1083/jcb.102.1.179. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. McDonald J. A., Kelley D. G. Degradation of fibronectin by human leukocyte elastase. Release of biologically active fragments. J Biol Chem. 1980 Sep 25;255(18):8848–8858. [PubMed] [Google Scholar]
  44. McDonald J. A., Quade B. J., Broekelmann T. J., LaChance R., Forsman K., Hasegawa E., Akiyama S. Fibronectin's cell-adhesive domain and an amino-terminal matrix assembly domain participate in its assembly into fibroblast pericellular matrix. J Biol Chem. 1987 Mar 5;262(7):2957–2967. [PubMed] [Google Scholar]
  45. Miekka S. I., Ingham K. C., Menache D. Rapid methods for isolation of human plasma fibronectin. Thromb Res. 1982 Jul 1;27(1):1–14. doi: 10.1016/0049-3848(82)90272-9. [DOI] [PubMed] [Google Scholar]
  46. Minier L. N., Lasher R. S., Erickson P. F. Distribution of the LETS protein (fibronectin) in rat cerebellum. An in vitro and in vivo developmental study. Cell Tissue Res. 1981;214(3):491–500. doi: 10.1007/BF00233490. [DOI] [PubMed] [Google Scholar]
  47. Newgreen D., Thiery J. P. Fibronectin in early avian embryos: synthesis and distribution along the migration pathways of neural crest cells. Cell Tissue Res. 1980;211(2):269–291. doi: 10.1007/BF00236449. [DOI] [PubMed] [Google Scholar]
  48. Norton P. A., Hynes R. O. Alternative splicing of chicken fibronectin in embryos and in normal and transformed cells. Mol Cell Biol. 1987 Dec;7(12):4297–4307. doi: 10.1128/mcb.7.12.4297. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Ott U., Odermatt E., Engel J., Furthmayr H., Timpl R. Protease resistance and conformation of laminin. Eur J Biochem. 1982 Mar;123(1):63–72. doi: 10.1111/j.1432-1033.1982.tb06499.x. [DOI] [PubMed] [Google Scholar]
  50. Paetau A., Mellström K., Vaheri A., Haltia M. Distribution of a major connective tissue protein, fibronectin, in normal and neoplastic human nervous tissue. Acta Neuropathol. 1980;51(1):47–51. doi: 10.1007/BF00688849. [DOI] [PubMed] [Google Scholar]
  51. Palm S. L., Furcht L. T. Production of laminin and fibronectin by Schwannoma cells: cell-protein interactions in vitro and protein localization in peripheral nerve in vivo. J Cell Biol. 1983 May;96(5):1218–1226. doi: 10.1083/jcb.96.5.1218. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Paul J. I., Schwarzbauer J. E., Tamkun J. W., Hynes R. O. Cell-type-specific fibronectin subunits generated by alternative splicing. J Biol Chem. 1986 Sep 15;261(26):12258–12265. [PubMed] [Google Scholar]
  53. Pierschbacher M. D., Ruoslahti E. Cell attachment activity of fibronectin can be duplicated by small synthetic fragments of the molecule. Nature. 1984 May 3;309(5963):30–33. doi: 10.1038/309030a0. [DOI] [PubMed] [Google Scholar]
  54. Pytela R., Pierschbacher M. D., Ruoslahti E. Identification and isolation of a 140 kd cell surface glycoprotein with properties expected of a fibronectin receptor. Cell. 1985 Jan;40(1):191–198. doi: 10.1016/0092-8674(85)90322-8. [DOI] [PubMed] [Google Scholar]
  55. Rakic P. Neuron-glia relationship during granule cell migration in developing cerebellar cortex. A Golgi and electronmicroscopic study in Macacus Rhesus. J Comp Neurol. 1971 Mar;141(3):283–312. doi: 10.1002/cne.901410303. [DOI] [PubMed] [Google Scholar]
  56. Rao C. N., Margulies I. M., Tralka T. S., Terranova V. P., Madri J. A., Liotta L. A. Isolation of a subunit of laminin and its role in molecular structure and tumor cell attachment. J Biol Chem. 1982 Aug 25;257(16):9740–9744. [PubMed] [Google Scholar]
  57. Rogers S. L., Edson K. J., Letourneau P. C., McLoon S. C. Distribution of laminin in the developing peripheral nervous system of the chick. Dev Biol. 1986 Feb;113(2):429–435. doi: 10.1016/0012-1606(86)90177-6. [DOI] [PubMed] [Google Scholar]
  58. Rogers S. L., Letourneau P. C., Palm S. L., McCarthy J., Furcht L. T. Neurite extension by peripheral and central nervous system neurons in response to substratum-bound fibronectin and laminin. Dev Biol. 1983 Jul;98(1):212–220. doi: 10.1016/0012-1606(83)90350-0. [DOI] [PubMed] [Google Scholar]
  59. Rogers S. L., Letourneau P. C., Peterson B. A., Furcht L. T., McCarthy J. B. Selective interaction of peripheral and central nervous system cells with two distinct cell-binding domains of fibronectin. J Cell Biol. 1987 Sep;105(3):1435–1442. doi: 10.1083/jcb.105.3.1435. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Rogers S. L., McCarthy J. B., Palm S. L., Furcht L. T., Letourneau P. C. Neuron-specific interactions with two neurite-promoting fragments of fibronectin. J Neurosci. 1985 Feb;5(2):369–378. doi: 10.1523/JNEUROSCI.05-02-00369.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Sanes J. R. Roles of extracellular matrix in neural development. Annu Rev Physiol. 1983;45:581–600. doi: 10.1146/annurev.ph.45.030183.003053. [DOI] [PubMed] [Google Scholar]
  62. Schwarzbauer J. E., Tamkun J. W., Lemischka I. R., Hynes R. O. Three different fibronectin mRNAs arise by alternative splicing within the coding region. Cell. 1983 Dec;35(2 Pt 1):421–431. doi: 10.1016/0092-8674(83)90175-7. [DOI] [PubMed] [Google Scholar]
  63. Sidman R. L., Rakic P. Neuronal migration, with special reference to developing human brain: a review. Brain Res. 1973 Nov 9;62(1):1–35. doi: 10.1016/0006-8993(73)90617-3. [DOI] [PubMed] [Google Scholar]
  64. Silver J., Lorenz S. E., Wahlsten D., Coughlin J. Axonal guidance during development of the great cerebral commissures: descriptive and experimental studies, in vivo, on the role of preformed glial pathways. J Comp Neurol. 1982 Sep 1;210(1):10–29. doi: 10.1002/cne.902100103. [DOI] [PubMed] [Google Scholar]
  65. Smalheiser N. R., Crain S. M., Reid L. M. Laminin as a substrate for retinal axons in vitro. Brain Res. 1984 Jan;314(1):136–140. doi: 10.1016/0165-3806(84)90184-6. [DOI] [PubMed] [Google Scholar]
  66. Stewart G. R., Pearlman A. L. Fibronectin-like immunoreactivity in the developing cerebral cortex. J Neurosci. 1987 Oct;7(10):3325–3333. doi: 10.1523/JNEUROSCI.07-10-03325.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Tack B. F., Dean J., Eilat D., Lorenz P. E., Schechter A. N. Tritium labeling of proteins to high specific radioactivity by reduction methylation. J Biol Chem. 1980 Sep 25;255(18):8842–8847. [PubMed] [Google Scholar]
  68. Thiery J. P., Duband J. L., Delouvée A. Pathways and mechanisms of avian trunk neural crest cell migration and localization. Dev Biol. 1982 Oct;93(2):324–343. doi: 10.1016/0012-1606(82)90121-x. [DOI] [PubMed] [Google Scholar]
  69. Timpl R., Johansson S., van Delden V., Oberbäumer I., Hök M. Characterization of protease-resistant fragments of laminin mediating attachment and spreading of rat hepatocytes. J Biol Chem. 1983 Jul 25;258(14):8922–8927. [PubMed] [Google Scholar]
  70. Tobey S. L., McClelland K. J., Culp L. A. Neurite extension by neuroblastoma cells on substratum-bound fibronectin's cell-binding fragment but not on the heparan sulfate-binding protein, platelet factor-4. Exp Cell Res. 1985 Jun;158(2):395–412. doi: 10.1016/0014-4827(85)90464-1. [DOI] [PubMed] [Google Scholar]
  71. Tomaselli K. J., Reichardt L. F., Bixby J. L. Distinct molecular interactions mediate neuronal process outgrowth on non-neuronal cell surfaces and extracellular matrices. J Cell Biol. 1986 Dec;103(6 Pt 2):2659–2672. doi: 10.1083/jcb.103.6.2659. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Tosney K. W., Landmesser L. T. Development of the major pathways for neurite outgrowth in the chick hindlimb. Dev Biol. 1985 May;109(1):193–214. doi: 10.1016/0012-1606(85)90360-4. [DOI] [PubMed] [Google Scholar]
  73. Waite K. A., Mugnai G., Culp L. A. A second cell-binding domain on fibronectin (RGDS-independent) for neurite extension of human neuroblastoma cells. Exp Cell Res. 1987 Apr;169(2):311–327. doi: 10.1016/0014-4827(87)90193-5. [DOI] [PubMed] [Google Scholar]
  74. Yamada K. M., Kennedy D. W. Dualistic nature of adhesive protein function: fibronectin and its biologically active peptide fragments can autoinhibit fibronectin function. J Cell Biol. 1984 Jul;99(1 Pt 1):29–36. doi: 10.1083/jcb.99.1.29. [DOI] [PMC free article] [PubMed] [Google Scholar]

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