Bulk-like endocytosis plays an important role in the recycling of insulin granules in pancreatic beta cells

Du Wen1,4, Yanhong Xue1,4, Kuo Liang3, Tianyi Yuan2, Jingze Lu1, Wei Zhao1,4, Tao Xu1(), Liangyi Chen2()

PDF(852 KB)
PDF(852 KB)
Protein Cell ›› 2012, Vol. 3 ›› Issue (8) : 618-626. DOI: 10.1007/s13238-012-2938-0
RESEARCH ARTICLE
RESEARCH ARTICLE

Bulk-like endocytosis plays an important role in the recycling of insulin granules in pancreatic beta cells

  • Du Wen1,4, Yanhong Xue1,4, Kuo Liang3, Tianyi Yuan2, Jingze Lu1, Wei Zhao1,4, Tao Xu1(), Liangyi Chen2()
Author information +
History +

Abstract

Although bulk endocytosis has been found in a number of neuronal and endocrine cells, the molecular mechanism and physiological function of bulk endocytosis remain elusive. In pancreatic beta cells, we have observed bulk-like endocytosis evoked both by flash photolysis and trains of depolarization. Bulk-like endocytosis is a clathrin-independent process that is facilitated by enhanced extracellular Ca2+ entry and suppressed by the inhibition of dynamin function. Moreover, defects in bulklike endocytosis are accompanied by hyperinsulinemia in primary beta cells dissociated from diabetic KKAy mice, which suggests that bulk-like endocytosis plays an important role in maintaining the exo-endocytosis balance and beta cell secretory capability.

Keywords

bulk-like endocytosis / clathrin-independent endocytosis / dynamin / diabetic KKAy mice

Cite this article

Download citation ▾
Du Wen, Yanhong Xue, Kuo Liang, Tianyi Yuan, Jingze Lu, Wei Zhao, Tao Xu, Liangyi Chen. Bulk-like endocytosis plays an important role in the recycling of insulin granules in pancreatic beta cells. Prot Cell, 2012, 3(8): 618‒626 https://doi.org/10.1007/s13238-012-2938-0

References

[1] Anggono, V., Smillie, K.J., Graham, M.E., Valova, V.A., Cousin, M.A., and Robinson, P.J. (2006). Syndapin I is the phosphorylation-regulated dynamin I partner in synaptic vesicle endocytosis. Nat Neurosci 9, 752-760 .10.1038/nn1695
[2] Cao, H., Garcia, F., and McNiven, M.A. (1998). Differential distribution of dynamin isoforms in mammalian cells. Mol Biol Cell 9, 2595-2609 .
[3] Clayton, E.L., Anggono, V., Smillie, K.J., Chau, N., Robinson, P.J., and Cousin, M.A. (2009). The phospho-dependent dynaminsyndapin interaction triggers activity-dependent bulk endocytosis of synaptic vesicles. J Neurosci 29, 7706-7717 .10.1523/JNEUROSCI.1976-09.2009
[4] Clayton, E.L., and Cousin, M.A. (2009). The molecular physiology of activity-dependent bulk endocytosis of synaptic vesicles. J Neurochem 111, 901-914 .10.1111/j.1471-4159.2009.06384.x
[5] Clayton, E.L., Evans, G.J., and Cousin, M.A. (2008). Bulk synaptic vesicle endocytosis is rapidly triggered during strong stimulation. J Neurosci 28, 6627-6632 .10.1523/JNEUROSCI.1445-08.2008
[6] Clayton, E.L., Sue, N., Smillie, K.J., O'Leary, T., Bache, N., Cheung, G., Cole, A.R., Wyllie, D.J., Sutherland, C., Robinson, P.J.,.(2010). Dynamin I phosphorylation by GSK3 controls activitydependent bulk endocytosis of synaptic vesicles. Nat Neurosci 13, 845-851 .10.1038/nn.2571
[7] Duman, J.G., Chen, L., Palmer, A.E., and Hille, B. (2006). Contributions of intracellular compartments to calcium dynamics: implicating an acidic store. Traffic 7, 859-872 .10.1111/j.1600-0854.2006.00432.x
[8] Eliasson, L., Abdulkader, F., Braun, M., Galvanovskis, J., Hoppa, M.B., and Rorsman, P. (2008). Novel aspects of the molecular mechanisms controlling insulin secretion. J Physiol 586, 3313-3324 .10.1113/jphysiol.2008.155317
[9] Eliasson, L., Proks, P., Ammala, C., Ashcroft, F.M., Bokvist, K., Renstrom, E., Rorsman, P., and Smith, P.A. (1996). Endocytosis of secretory granules in mouse pancreatic beta-cells evoked by transient elevation of cytosolic calcium. J Physiol 493 (Pt 3), 755-767 .
[10] Hayashi, M., Raimondi, A., O'Toole, E., Paradise, S., Collesi, C., Cremona, O., Ferguson, S.M., and De Camilli, P. (2008). Celland stimulus-dependent heterogeneity of synaptic vesicle endocytic recycling mechanisms revealed by studies of dynamin 1-null neurons. Proc Natl Acad Sci U S A 105, 2175-2180 .10.1073/pnas.0712171105
[11] He, Z., Fan, J., Kang, L., Lu, J., Xue, Y., Xu, P., Xu, T., and Chen, L. (2008). Ca2+ triggers a novel clathrin-independent but actindependent fast endocytosis in pancreatic beta cells. Traffic 9, 910-923 .10.1111/j.1600-0854.2008.00730.x
[12] Heerssen, H., Fetter, R.D., and Davis, G.W. (2008). Clathrin dependence of synaptic-vesicle formation at the Drosophila neuromuscular junction. Curr Biol 18, 401-409 .10.1016/j.cub.2008.02.055
[13] Homo-Delarche, F. (1997). Beta-cell behaviour during the prediabetic stage. Part II. Non-insulin-dependent and insulin-dependent diabetes mellitus. Diabetes Metab 23, 473-505 .
[14] Hoppa, M.B., Jones, E., Karanauskaite, J., Ramracheya, R., Braun, M., Collins, S.C., Zhang, Q., Clark, A., Eliasson, L., Genoud, C.,.(2012). Multivesicular exocytosis in rat pancreatic beta cells. Diabetologia 55, 1001-1012 .10.1007/s00125-011-2400-5
[15] Kwan, E.P., and Gaisano, H.Y. (2005). Glucagon-like peptide 1 regulates sequential and compound exocytosis in pancreatic islet beta-cells. Diabetes 54, 2734-2743 .10.2337/diabetes.54.9.2734
[16] Lee, A.K., and Tse, A. (2001). Endocytosis in identified rat corticotrophs. J Physiol 533, 389-405 .10.1111/j.1469-7793.2001.0389a.x
[17] Lenzi, D., Crum, J., Ellisman, M.H., and Roberts, W.M. (2002). Depolarization redistributes synaptic membrane and creates a gradient of vesicles on the synaptic body at a ribbon synapse. Neuron 36, 649-659 .10.1016/S0896-6273(02)01025-5
[18] Liang, K., Du, W., Zhu, W., Liu, S., Cui, Y., Sun, H., Luo, B., Xue, Y., Yang, L., Chen, L.,.(2011). Contribution of different mechanisms to pancreatic beta-cell hyper-secretion in non-obese diabetic (NOD) mice during pre-diabetes. J Biol Chem 286, 39537-39545 .10.1074/jbc.M111.295931
[19] MacDonald, P.E., Braun, M., Galvanovskis, J., and Rorsman, P. (2006). Release of small transmitters through kiss-and-run fusion pores in rat pancreatic beta cells. Cell Metab 4, 283-290 .10.1016/j.cmet.2006.08.011
[20] Macia, E., Ehrlich, M., Massol, R., Boucrot, E., Brunner, C., and Kirchhausen, T. (2006). Dynasore, a cell-permeable inhibitor of dynamin. Dev Cell 10, 839-850 .10.1016/j.devcel.2006.04.002
[21] Newton, A.J., Kirchhausen, T., and Murthy, V.N. (2006). Inhibition of dynamin completely blocks compensatory synaptic vesicle endocytosis. Proc Natl Acad Sci U S A 103, 17955-17960 .10.1073/pnas.0606212103
[22] Orci, L., Malaisse-Lagae, F., Ravazzola, M., Amherdt, M., and Renold, A.E. (1973). Exocytosis-endocytosis coupling in the pancreatic beta cell. Science 181, 561-562 .10.1126/science.181.4099.561
[23] Ostenson, C.G., Gaisano, H., Sheu, L., Tibell, A., and Bartfai, T. (2006). Impaired gene and protein expression of exocytotic soluble N-ethylmaleimide attachment protein receptor complex proteins in pancreatic islets of type 2 diabetic patients. Diabetes 55, 435-440 .10.2337/diabetes.55.02.06.db04-1575
[24] Paillart, C., Li, J., Matthews, G., and Sterling, P. (2003). Endocytosis and vesicle recycling at a ribbon synapse. J Neurosci 23, 4092-4099 .
[25] Richards, D.A., Guatimosim, C., and Betz, W.J. (2000). Two endocytic recycling routes selectively fill two vesicle pools in frog motor nerve terminals. Neuron 27, 551-559 .10.1016/S0896-6273(00)00065-9
[26] Rorsman, P., and Trube, G. (1986). Calcium and delayed potassium currents in mouse pancreatic beta-cells under voltage-clamp conditions. J Physiol 374, 531-550 .
[27] Royle, S.J., and Lagnado, L. (2003). Endocytosis at the synaptic terminal. J Physiol 553, 345-355 .10.1113/jphysiol.2003.049221
[28] Srinivasan, K., and Ramarao, P. (2007). Animal models in type 2 diabetes research: an overview. Indian J Med Res 125, 451-472 .
[29] Takei, K., Mundigl, O., Daniell, L., and De Camilli, P. (1996). The synaptic vesicle cycle: a single vesicle budding step involving clathrin and dynamin. J Cell Biol 133, 1237-1250 .10.1083/jcb.133.6.1237
[30] Teng, H., Cole, J.C., Roberts, R.L., and Wilkinson, R.S. (1999). Endocytic active zones: hot spots for endocytosis in vertebrate neuromuscular terminals. J Neurosci 19, 4855-4866 .
[31] Tsai, C.C., Lin, C.L., Wang, T.L., Chou, A.C., Chou, M.Y., Lee, C.H., Peng, I.W., Liao, J.H., Chen, Y.T., and Pan, C.Y. (2009). Dynasore inhibits rapid endocytosis in bovine chromaffin cells. Am J Physiol Cell Physiol 297, C397-406 .10.1152/ajpcell.00562.2008
[32] Wu, W., and Wu, L.G. (2007). Rapid bulk endocytosis and its kinetics of fission pore closure at a central synapse. Proc Natl Acad Sci U S A 104, 10234-10239 .10.1073/pnas.0611512104
[33] Wu, X.S., McNeil, B.D., Xu, J., Fan, J., Xue, L., Melicoff, E., Adachi, R., Bai, L., and Wu, L.G. (2009). Ca(2+) and calmodulin initiate all forms of endocytosis during depolarization at a nerve terminal. Nat Neurosci 12, 1003-1010 .10.1038/nn.2355
AI Summary AI Mindmap
PDF(852 KB)

Accesses

Citations

Detail

Sections
Recommended

/