Differential sorting of lysosomal enzymes out of the regulated secretory pathway in pancreatic β-cells

Journal of Cell Biology

Volumn 137, Issue 3, 1997, Pages 595-608

  Kuliawat, Regina ^a   Klumperman, Judith ^b   Ludwig, Thomas ^c   Arvan, Peter ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b VU UNIVERSITY AMSTERDAM   (Netherlands)

^c Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CATHEPSIN; LYSOSOME ENZYME; SOMATOMEDIN B; SOMATOMEDIN B RECEPTOR;

ANIMAL CELL; ANTIBODY LABELING; EXOCYTOSIS; GOLGI COMPLEX; IMMUNOELECTRON MICROSCOPY; LYSOSOME; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN SECRETION; PROTEIN TARGETING; REVIEW; SECRETORY GRANULE; TRANSGENIC MOUSE;

ANIMALS; CATHEPSIN B; CATHEPSINS; CELL COMPARTMENTATION; CELL LINE; ENZYME INHIBITORS; ENZYME PRECURSORS; EXOCYTOSIS; GLYCOSYLATION; GOLGI APPARATUS; IMMUNOHISTOCHEMISTRY; INSULIN; ISLETS OF LANGERHANS; LYSOSOMES; MALE; MICE; MICE, KNOCKOUT; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, IGF TYPE 2; TUNICAMYCIN;

EID: 0030943904     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.137.3.595     Document Type: Review

References (101)

1. + pump activity. J. Cell Biol. 103:1257-1267.
2. Arvan, P., and J.D. Castle. 1987. Phasic release of newly synthesized secretory proteins in the unstimulated rat exocrine pancreas. J. Cell Biol. 104:243-252.
3. Arvan, P., and J.D. Castle. 1992. Protein sorting and secretion granule formation in regulated secretory cells. Trends Cell Biol. 2:327-331.
4. Arvan, P., and A. Chang. 1987. Constitutive protein secretion from the exocrine pancreas of fetal rats. J. Biol. Chem. 262:3886-3890.
5. Arvan, P., and J. Lee. 1991. Regulated and constitutive protein targeting can be distinguished by secretory polarity in thyroid epithelial cells. J. Cell Biol. 112:365-376.
6. Arvan, P., G. Rudnick, and J.D. Castle. 1984. Osmotic properties and internal pH of isolated rat parotid secretory granules. J. Biol. Chem. 259:13567-13572.
7. Arvan, P., G. Rudnick, and J.D. Castle. 1985. Relative lack of ATP-driven H+ translocase activity in isolated parotid secretory granules. J. Biol. Chem. 260: 14945-14952.
8. Arvan, P., R. Kuliawat, D. Prabakaran, A.M. Zavacki, D. Elahi, S. Wang, and D. Pilkey. 1991. Protein discharge from immature secretory granules displays both regulated and constitutive characteristics. J. Biol. Chem. 266: 14171-14174.
9. Asfari, M., D. Janjic, P. Meda, G. Li, P.A. Halban, and C.B. Wollheim. 1992. Establishment of 2-mercaptoethanol-dependent differentiated insulin-secreting cell lines. Endocrinology. 130:167-178.
10. Barrett, A.J., and H. Kirschke. 1981. Cathepsin B, cathepsin H, and cathepsin L. Methods Enzymol. 80(Pt C):535-561.
11. Bauerfeind, R., and W.B. Huttner. 1993. Biogenesis of constitutive secretory vesicles, secretory granules and synaptic vesicles. Curr. Opin. Cell Biol. 5: 628-635.
12. Bomsel, M., and K.E. Mostov. 1993. Possible role of both the α and βγ subunits of the heterotrimeric G protein, Gs, in transcytosis of the polymeric immunoglobulin receptor. J. Biol. Chem. 258:25824-25835.
13. Bonifacino, J.S., L. Yuan, and I.V. Sandoval. 1989. Internalization and recycling to serotonin-containing granules of the 80K integral membrane protein exposed on the surface of secreting rat basophilic leukaemia cells. J. Cell Sci. 92:701-712.
14. Borg, L.A., and A.H. Schnell. 1986. Lysosomes and pancreatic islet function: intracellular insulin degradation and lysosomal transformations. Diabetes Res. 3:277-285.
15. Borg, L.A., N. Dahl, and I. Swenne. 1995. Age-dependent differences in insulin secretion and intracellular handling of insulin in isolated pancreatic islets of the rat. Diabetes Metab. Rev. 21:408-414.
16. Brands, R., J.W. Slot, and H.J. Geuze. 1982. Immunocytochemical localization of β-glucuronidase in the rat preputial gland. Eur. J. Cell Biol. 27:213-220.
17. Burgess, T.L., and R.B. Kelly. 1987. Constitutive and regulated secretion of proteins. Annu. Rev. Cell Biol. 3:243-293.
18. Burkhardt, J.K., S. Hester, and Y. Argon. 1989. Two proteins targeted to the same lytic granule compartment undergo very different posttranslational processing. Proc. Natl. Acad. Sci. USA. 86:7128-7132.
19. Burkhardt, J.K., S. Hester, C.K. Lapham, and Y. Argon. 1990. The lytic granules of natural killer cells are dual-function organelles combining secretory and pre-lysosomal compartments. J. Cell Biol. 111:2327-2340.
20. Chavez, R.A., S.G. Miller, and H.-P.H. Moore. 1996. A biosynthetic regulated secretory pathway in constitutive secretory cells. J. Cell Biol. 133:1177-1191.
21. Conlon, J.M., A. Hoog, and L. Grimelius. 1995. Intracellular degradation of the C-peptide of proinsulin, in a human insulinoma: identification of sites of cleavage and evidence for a role for cathepsin B. Pancreas. 10:167-172.
22. Cool, D.R., E. Normant, F.-s. Shen, H.-C. Chen, L. Pannel, Y. Zhang, and Y.P. Loh. 1997. Carboxypeptidase E is a regulated secretory pathway sorting receptor: genetic obliteration leads to endocrine disorders in Cpe(fat) mice. Cell. 88:73-83.
23. Dittie, A.S., N. Hajibagheri, and S.A. Tooze. 1996. The AP-1 adaptor complex binds to immature secretory granules from PC12 cells, and is regulated by ADP-ribosylation factor. J. Cell Biol. 132:523-536.
24. Docherty, K., J.C. Hutton, and D.F. Steiner. 1984. Cathepsin B-related proteases in the insulin secretory granule. J. Biol. Chem. 259:6041-6044.
25. Dong, J., and G.G. Sahagian. 1990. Basis for low affinity binding of a lysosomal cysteine protease to the cation-independent mannose 6-phosphate receptor. J. Biol. Chem. 265:4210-4217.
26. Dong, J., E.M. Prence, and G.G. Sahagian. 1989. Mechanism for selective secretion of a lysosomal protease by transformed mouse fibroblasts. J. Biol. Chem. 264:7377-7383.
27. Fishman, J.B., and R. Fine. 1987. A trans Golgi-derived exocytic coated vesicle can contain both newly synthesized cholinesterase and internalized transferrin. Cell. 48:157-164.
28. Futter, C.E., C.N. Connolly, D.F. Cutler, and C.R. Hopkins. 1995. Newly synthesized transferrin receptors can be detected in the endosome before they appear on the cell surface. J. Biol. Chem. 270:10999-11003.
29. Garreau de Loubresse, N., M.-C. Gautier, and L. Sperling. 1994. Immature secretory granules are not acidic in Paramecium: implications for sorting to the regulated pathway. Biol. Cell. 82:139-147.
30. Gautier, M.-C., N. Garreau de Loubresse. L. Madeddu, and L. Sperling. 1994. Evidence for defects in membrane traffic in Paramecium secretory mutants unable to produce functional storage granules. J. Cell. Biol. 124:893-902.
31. Geuze, H.J., J.W. Slot, G.J.A.M. Strous, A. Hasilik, and K. von Figura. 1984. Ultrastructural localization of the mannose 6-phosphate receptor in rat liver. J. Cell Biol. 98:2047-2054.
32. Geuze, H.J., J.W. Slot, G.J.A.M. Strous, A. Hasilik, and K. von Figura. 1985. Possible pathways of lysosomal enzyme delivery. J. Cell Biol. 101:2253-2262.
33. Glickman, J.N., E. Conibear, and B.M.F. Pearse. 1989. Specificity of binding of clathrin adaptors to signals on the mannose-6-phosphate/insulin-like growth factor II receptor. EMBO (Eur. Mol. Biol. Organ.) J. 8:1041-1047.
34. Griffiths, G., B. Hoflack, K. Simons, I. Mellman, and S. Kornfeld. 1988. The mannose 6-phosphate receptor and the biogenesis of lysosomes. Cell. 52: 329-341.
35. Griffiths, G.M., and S. Isaaz. 1993. Granzymes A and B are targeted to the lytic granules of lymphocytes by the mannose-6-phosphate receptor. J. Cell Biol. 120:885-896.
36. Grimes, M., and R.B. Kelly. 1992. Intermediates in the constitutive and regulated secretory pathways released in vitro from semi-intact cells. J. Cell Biol. 117:539-550.
37. Halban, P.A. 1994. Proinsulin processing in the regulated and the constitutive secretory pathway. Diabetologia. 37:S65-S72.
38. Halban, P.A., R. Mutkoski, G. Dodson, and L. Orci. 1987. Resistance of the insulin crystal to lysosomal proteases: implications for pancreatic β-cell crinophagy. Diabetologia. 30:348-353.
39. Hanewinkel, H., J. Glossl, and H. Kresse. 1987. Biosynthesis of cathepsin B in cultured normal and 1-cell fibroblasts. J. Biol. Chem. 262:12351-12355.
40. Hansen, S.H., and J.E. Casanova. 1994. Gsa stimulates transcytosis and apical secretion in MDCK cells through cAMP and protein kinase A. J. Cell Biol. 126:677-687.
41. Hille, A., J. Klumperman, H.J. Geuze, C. Peter, F.M. Brodsky, and K. von Figura. 1992. Lysosomal acid phosphatase is internalized via clathrin-coated pits. Eur. J. Cell Biol. 59:106-115.
42. Hirano, T., T. Manabe, A.K. Saluja, and M.L. Steer. 1992. Pancreatic secretion of lysosomal enzymes stimulated by intraduodenal instillation of a liquid meal in rabbits. Clin. Sci. (Colch). 83:277-280.
43. Huang, X.F., and P. Arvan. 1994. Formation of the insulin-containing secretory granule core occurs within immature β-granules. J. Biol. Chem. 269:20838-20844.
44. Huang, X.F., and P. Arvan. 1995. Intracellular transport of proinsulin in pancreatic β-cells: structural maturation probed by disulfide accessibility. J. Biol. Chem. 270:20417-20423.
45. Kane, S.E. 1993. Mouse procathepsin L lacking a functional glycosylation site is properly folded, stable, and secreted by NIH 3T3 cells. J. Biol. Chem. 268: 11456-11462.
46. Kasper, D., F. Dittmer, K. von Figura, and R. Pohlmann. 1996. Neither type of mannose 6-phosphate receptor is sufficient for targeting of lysosomal enzymes along intracellular routes. J. Cell Biol. 134:615-623.
47. Kelly, R.B. 1985. Pathways of protein secretion in eukaryotes. Science (Wash. DC). 230:25-32.
48. Kelly, R.B. 1987. From organelle to organelle. Nature (Lond.). 326:14-15.
49. Kelly, R. 1991. Secretory granule and synaptic vesicle formation. Curr. Opin. Cell Biol. 3:654-660.
50. Koga, H., H. Yamada, Y. Nishimura, K. Kato, and T. Imoto. 1990. Comparative study on specificities of rat cathepsin L and papain: amino acid differences at substrate-binding sites are involved in their specificities. J. Biochem. 108: 976-982.
51. Kornfeld, S., and I. Mellman. 1989. The biogenesis of lysosomes. Annu. Rev. Cell Biol. 5:483-525.
52. Kuliawat, R., and P. Arvan. 1992. Protein targeting via the "constitutive-like" secretory pathway in isolated pancreatic islets: passive sorting in the immature granule compartment. J. Cell Biol. 118:521-529.
53. Kuliawat, R., and P. Arvan. 1994. Distinct molecular mechanisms for protein sorting within immature secretory granules of pancreatic β-cells. J. Cell Biol. 126:77-86.
54. Landstrom, A.H.S., J. Westman, and L.A.H. Borg. 1988. Lysosomes and pancreatic islet function. Diabetes. 37:309-316.
55. Landstrom, A.H.S., A. Andersson, and L.A. Borg. 1991. Lysosomes and pancreatic islet function: adaptation of beta-cell lysosomes to various metabolic demands. Metabolism. 40:399-405.
56. Lazzarino, D., and C.A. Gabel. 1990. Protein determinants impair recognition of procathepsin L phosphorylated oligosaccharides by the cation-independent mannose 6-phosphate receptor. J. Biol. Chem. 265:11864-11871.
57. Leblond, F.A., G. Viau, J. Laine, and D. Lebel. 1993. Reconstitution in vitro of the pH-dependent aggregation of pancreatic zymogens en route to the secretory granule: implication of GP-2. Biochem. J. 291:289-296.
58. Ludwig, T., G. Griffiths, and B. Hoflack. 1991. Distribution of newly synthesized lysosomal enzymes in the endocytic pathway of normal rat kidney cells. J. Cell Biol. 115:1561-1572.
59. Ludwig, T., C.E. Ovitt, U. Bauer, M. Hollinshead, J. Remmler, P. Lobel, U. Ruther, and B. Hoflack. 1993. Targeted disruption of the mouse cation-dependent mannose 6-phosphate receptor results in partial missorting of multiple lysosomal enzymes. EMBO (Eur. Mol. Biol. Organ.) J. 12:5225-5235.
60. Ludwig, T., H. Munier-Lehmann, U. Bauer, M. Hollinshead, C. Ovitt, P. Lobel, and B. Hoflack. 1994. Differential sorting of lysosomal enzymes in mannose-6-phosphate receptor-deficient fibroblasts. EMBO (Eur. Mol. Biol. Organ.) J. 13:3430-3437.
61. Mauxion, F., R. Le Borgne, H. Munier-Lehmann, and B. Hoflack. 1996. A casein kinase II phosphorylation site in the cytoplasmic domain of the cation-dependent mannose 6-phosphate receptor determines the high affinity interaction of the AP-1 Golgi assembly proteins with membranes. J. Biol. Chem. 271:2171-2178.
62. McIntyre, G.F., and A.H. Erickson. 1991. Procathepsins L and D are membrane-bound in acidic microsomal vesicles. J. Biol. Chem. 266:15438-15445.
63. McIntyre, G.F., and A.H. Erickson. 1993. The lysosomal proenzyme receptor that binds procathepsin L to microsomal membranes at pH 5 is a 43-kDa integral membrane protein. Proc. Natl. Acad. Sci. USA. 90:10588-10592.
64. McIntyre, G.F., G.D. Godbold, and A.H. Erickson. 1994. The pH-dependent membrane association of procathepsin L is mediated by a 9-residue sequence within the propeptide. J. Biol. Chem. 269:567-572.
65. Miller, S.G., L. Carnell, and H.-P.H. Moore. 1992. Post-Golgi membrane traffic: brefeldin A inhibits export from distal Golgi compartments to the cell surface but not recycling. J. Cell Biol. 118:267-285.
66. Moore, H.P.H., M.D. Walker, F. Lee, and R.B. Kelly. 1983. Expressing a human proinsulin cDNA in a mouse ACTH-secreting cell. Intracellular storage, proteolytic processing, and secretion on stimulation. Cell. 35:531-538.
67. Moore, H.-P.H., C. Brion, K.-N. Chung, L. Lehmicke, R. Rivas, and D. Quinn. 1989. Protein secretion by constitutive and regulated pathways. In Secretion and Its Control. G.S. Oxford and C.M. Armstrong, editors. Rockefeller University Press, New York. 189-201.
68. Natori, S., and W.B. Huttner. 1996. Chromogranin B (secretogranin I) promotes sorting to the regulated secretory pathway of processing intermediates derived from a peptide hormone precursor. Proc. Natl. Acad. Sci. USA. 93:4431-4436.
69. Neerman-Arbez, M., and P.A. Halban. 1993. Novel, non-crinophagic, degradation of connecting peptide (C-peptide) in transformed pancreatic beta cells. J. Biol. Chem. 268:16248-16252.
70. Orci, L., P. Halban, M. Amherdt, M. Ravazzola, J.D. Vassalli, and A. Perrelet. 1984a. Nonconverted, amino acid analog-modified proinsulin stays in a Golgi-derived clathrin-coated membrane compartment. J. Cell Biol. 99: 2187-2192.
71. Orci, L., M. Ravazzola, M. Amherdt, C. Yanaihara, N. Yanaihara, P. Halban, A.E. Renold, and A. Perrelet. 1984b. Insulin, not C-peptide (proinsulin), is present in crinophagic bodies of the pancreatic β-cell. J. Cell Biol. 98:222-228.
72. Orci, L., M. Ravazzola, M. Amherdt, O. Madsen, and J.D. Vassalli. 1985. Direct identification of prohormone conversion site in insulin-secreting cells. Cell. 42:671-681.
73. Orci, L., M. Ravazzola, M. Amherdt, O. Madsen, A. Perrelet, J.-D. Vassalli, and R.G.W. Anderson. 1986. Conversion of proinsulin to insulin occurs co-ordinately with acidification of maturing secretory vesicles. J. Cell Biol. 103: 2273-2281.
74. Orci, L., M. Ravazzola, and R.G.W. Anderson. 1987a. The condensing vacuole of exocrine cells is more acidic than the mature secretory vesicle. Nature (Lond.). 326:77-79.
75. Orci, L., M. Ravazzola, M.J. Storch, R.G.W. Anderson. J.D. Vassalli, and A. Perrelet. 1987b. Proteolytic maturation of insulin is a post-Golgi event which occurs in acidifying clathrin-coated secretory vesicles. Cell. 49:865-868.
76. Orci, L., P. Halban, A. Perrelet, M. Amherdt, M. Ravazzola, and R.G.W. Anderson. 1994. pH-independent and -dependent cleavage of proinsulin in the same secretory vesicle. J. Cell Biol. 126:1149-1156.
77. Palmer, D.J., and D.L. Christie. 1992. Identification of molecular aggregates containing glycoproteins III, J, K (carboxypeptidase H), and H (Kex2-related proteases) in the soluble and membrane fractions of adrenal medullary chromaffin granules. J. Biol. Chem. 267:19806-19812.
78. Pimplikar, S.W., and W.B. Huttner. 1992. Chromogranin B (secretogranin I), a secretory protein of the regulated pathway, is also present in a tightly membrane-associated form in PC12 cells. J. Biol. Chem. 267:4110-4118.
79. Rhodes, C.J., and P.A. Halban. 1987. Newly synthesized proinsulin/insulin and stored insulin are released from pancreatic B cells predominantly via a regulated, rather than a constitutive, pathway. J. Cell Biol. 105:145-153.
80. Rhodes, C.J., C.A. Lucas, R.L. Mutkoski, L. Orci, and P.A. Halban. 1987. Stimulation by ATP of proinsulin to insulin conversion in isolated rat pancreatic islet secretory granules. J. Biol. Chem. 262:10712-10717.
81. Rosa, P., F.A. Barr, J.C. Stinchcombe, C. Binacchi, and W.B. Huttner. 1992. Brefeldin A inhibits the formation of constitutive secretory vesicles and immature secretory granules from the trans-Golgi network. Eur. J. Cell Biol. 59:265-274.
82. Rowan, A.D., L. Mach, and J.S. Mort. 1992. Antibodies to rat procathepsin B recognize the active mature enzyme. Biol. Chem. Hoppe-Seyler. 373:427-432.
83. Schagger, H., and G. vonJagow. 1987. Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal. Biochem. 166:368-379.
84. Schnell, A.H., I. Swenne, and L.A.H. Borg. 1988. Lysosomes and pancreatic islet function. A quantitative estimation of crinophagy in the mouse pancreatic β-cell. Cell Tiss. Res. 252:9-15.
85. Sesso, A., J.E. Assis, V.Y. Kuwajima, and B. Kachar. 1980. Freeze-fracture and thin-section study of condensing vacuoles in rat pancreatic acinar cells. Acta Anat. 108:521-539.
86. Slot, J.W., H.J. Geuze, and A.J. Weerkamp. 1988. Localization of macromolecular components by application of the immunogold technique on cryosectioned bacteria. Methods Microbiol. 20:211-236.
87. Slot, J.W., H.J. Geuze, S. Gigengack, G.E. Lienhard, and D.E. James. 1991. Immunolocalization of the insulin regulatable glucose transporter in brown adipose tissue of the rat. J. Cell Biol. 113:123-135.
88. Stearns, N.A., J.M. Dong, J.X. Pan, D.A. Brenner, and G.G. Sahagian. 1990. Comparison of cathepsin L synthesized by normal and transformed cells at the gene, message, protein, and oligosaccharide levels. Arch. Biochem. Biophys. 283:447-457.
89. Steiner, D.F., J. Michael, R. Houghten, M. Mathieu, P.R. Gardner, M. Ravazzola, and L. Orci. 1987. Use of a synthetic peptide antigen to generate antisera reactive with a proteolytic processing site in native human proinsulin: demonstration of cleavage within clathrin-coated (pro)secretory vesicles. Proc. Natl. Acad. Sci. USA. 84:6184-6188.
90. Takio, K., T. Towatari, N. Katunuma, D.C. Teller, and K. Titani. 1983. Homology of amino acid sequences of rat liver cathepsins B and H with that of papain. Proc. Natl. Acad. Sci. USA. 80:3666-3670.
91. Taugner, R., and E. Hackenthal. 1988. On the character of the secretory granules in juxtaglomerular epithelioid cells. Int. Rev. Cytol. 110:93-131.
92. Tooze, J., and S.A. Tooze. 1986. Clathrin-coated vesicular transport of secretory proteins during the formation of ACTH-containing secretory granules in AtT20 cells. J. Cell Biol. 103:839-850.
93. Tooze, J., M. Hollinshead, G. Hensel, H.F. Kern, and B. Hoflack. 1991. Regulated secretion of mature cathepsin B from rat exocrine pancreatic cells. Eur. J. Cell Biol. 56:187-200.
94. Tooze, S.A., and W.B. Huttner. 1990. Cell-free protein sorting to the regulated and constitutive secretory pathways. Cell. 60:837-847.
95. Tooze, S.A., and J.C. Stinchcombe. 1992. Biogenesis of secretory granules. Semin. Cell Biol. 3:357-366.
96. von Figura, K. 1991. Molecular recognition and targeting of lysosomal proteins. Curr. Opin. Cell Biol. 3:642-646.
97. von Figura, K., and A. Hasilik. 1986. Lysosomal enzymes and their receptors. Annu. Rev. Biochem. 55:167-193.
98. vonZastrow, M., and J.D. Castle. 1987. Protein sorting among two distinct export pathways occurs from the content of maturing exocrine storage granules. J. Cell Biol. 105:2675-2684.
99. Wong, J.G., K.T. Izutsu, M.R. Robinovitch, J.M. Iversen, M.E. Cantino, and D.E. Johnson. 1991. Microprobe analysis of maturation-related elemental changes in rat parotid secretory granules. Am. J. Physiol. 261:C1033-1041.
100. Xu, H., and D. Shields. 1993. Prohormone processing in the trans-Golgi network: endoproteolytic cleavage of prosomatostatin and formation of nascent secretory vesicles in permeabilized cells. J. Cell Biol. 122:1169-1184.
101. Yoo, S.H. 1993. pH-dependent association of chromogranin A with secretory vesicle membrane and a putative membrane binding region of chromogranin A. Biochemistry. 32:8213-8219.