Login Register Cart 0
Generic placeholder image

Current Protein & Peptide Science

Editor-in-Chief

ISSN (Print): 1389-2037
ISSN (Online): 1875-5550

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
Review Article

Sequential and Asynchronous Strengthening of the Influence of Temperature on the Endo- and Exocytosis of Insulin in the Isolated Vertebrata Hepatocytes: Summing up Previous Studies

Author(s): Alexander P. Kolychev*, Maxim A. Terpilovskii and Vladimir N. Uversky

Volume 21, Issue 1, 2020

Page: [22 - 35] Pages: 14

DOI: 10.2174/1389203720666190325101804

Price: $65

Abstract

Insulin internalization and processing of the Insulin Receptor Complex (IRC) inside the cell are important components of the intracellular Mechanism of Insulin Action (MIA). They define the continuation of intracellular signaling of IRC and allow utilization of the parts of the complex after ligand dissociation. Traditionally, changes in the insulin regulatory system associated with the vertebrate phylogenesis have been evaluated by changes of its two elements: the hormone and its receptor. A hormone-competent cell was considered as an evolutionarily completed element of insulin regulatory system. However, previous studies of the isolated hepatocytes of four classes of vertebrates (lamprey, frog, chicken, and rat) revealed significant differences in the state of internalization of 125I-insulin and intracellular IRC processing. Radical differences were noted in the regulation of 125I-insulin internalization and the intracellular fate of the IRC. Here, cytosolic efficient insulin degradation and a complete lack of 125I-insulin exocytosis were observed in the cyclostome cells, whereas in amphibians the hormone underwent lysosomal degradation and showed low levels of exocytosis, while birds and mammals were characterized by high volumes of the excreted 125Iinsulin containing proteolytic 125I-insulin fragments. Despite the established recognition of the importance of the temperature factor, a complete understanding of the molecular mechanisms underlying the temperature effects on MIA is still missing. This poorly studied problem of the MIA temperature dependence can be behind the differences in the effect of temperature on the intracellular action of insulin and IGF-I. In fact, at different phylogenetic stages, successive changes were reported for the temperature dependence of the 125Iinsulin internalization and exocytosis. The following regularities were reported for the effect of temperature on the 125I-insulin internalization in isolated hepatocytes of different origin: complete lack of receptibility of the process to temperature in lampreys, receptibility of the process in a narrow range of low temperatures (0-5°C) in amphibians, and flexible regulation of 125I-insulin internalization in a wide temperature range (6- 37°C) in the cells from endothermic organisms. Reported data make it possible to observe three stages in the alteration of temperature regulation of 125I-insulin internalization (in cells of cyclostomes, amphibians, and endothermic organisms) and two stages of temperature regulation of 125I-insulin exocytosis in cells of amphibians, birds, and mammals. The data presented in this study reflect the specificity of the developmental reorganization of the intracellular MIA regulation and hormone utilization, and emphasize the central role of temperature in selective MIA formation during vertebrate phylogenesis.

Keywords: Insulin, internalization, endocytosis, exocytosis, degradation, insulin-receptor complex, phylogenesis, temperature, poikilothermic, endodermic, receptibility.

« Previous Next »
Graphical Abstract

[1]
Zick, Y. Molecular basis of insulin action. Novartis Foundation Symposium, 2004, pp. 36-50.
[2]
Foti, M.; Moukil, M.A.; Dudognon, P.; Carpentier, J.L. Insulin and IGF‐1 receptor trafficking and signalling n Biology of IGF-1: Its Interaction with Insulin in Health and Malignant States:Novartis Foundation Symposium, 2004, 262, 125-147.
[3]
Kolychev, A.P.; Ternovskaya, E.E. Insulin and insulin-like growth factor 1 (IGF-1) induce different receptor endocytosis mechanisms in isolated rat hepatocytes, In: Euroasian Scientists Union Journal. IV International scientific-practical conference “Modern conceptions of scientific research”; , 2014; 4, pp. 77-88.
[4]
Sonne, O. Receptor-mediated endocytosis and degradation of insulin. Physiol. Rev., 1988, 68(4), 1129-1196.
[http://dx.doi.org/10.1152/physrev.1988.68.4.1129] [PMID: 3054947]
[5]
Smythe, E.; Warren, G. The mechanism of receptor-mediated endocytosis. Eur. J. Biochem., 1991, 202(3), 689-699.
[http://dx.doi.org/10.1111/j.1432-1033.1991.tb16424.x] [PMID: 1662613]
[6]
Kolychev, A.P. The binding ability of insulin-related peptides as the clue to the search for their functional role in phylogenesis. Introduction to the problem. J. Evol. Biochem. Physiol., 2008, 44, 766.
[http://dx.doi.org/10.1134/S0022093008060148]
[7]
Smit, A.B.; van Marle, A.; van Elk, R.; Bogerd, J.; van Heerikhuizen, H.; Geraerts, W.P.M. Evolutionary conservation of the insulin gene structure in invertebrates: cloning of the gene encoding molluscan insulin-related peptide III from Lymnaea stagnalis. J. Mol. Endocrinol., 1993, 11(1), 103-113.
[http://dx.doi.org/10.1677/jme.0.0110103] [PMID: 8240668]
[8]
Pierce, S.B.; Costa, M.; Wisotzkey, R.; Devadhar, S.; Homburger, S.A.; Buchman, A.R.; Ferguson, K.C.; Heller, J.; Platt, D.M.; Pasquinelli, A.A.; Liu, L.X.; Doberstein, S.K.; Ruvkun, G. Regulation of DAF-2 receptor signaling by human insulin and ins-1, a member of the unusually large and diverse C. elegans insulin gene family. Genes Dev., 2001, 15(6), 672-686.
[http://dx.doi.org/10.1101/gad.867301] [PMID: 11274053]
[9]
King, G.L.; Kahn, C.R. Non-parallel evolution of metabolic and growth-promoting functions of insulin. Nature, 1981, 292(5824), 644-646.
[http://dx.doi.org/10.1038/292644a0] [PMID: 7019727]
[10]
Chan, S.J.; Cao, Q-P.; Steiner, D.F. Evolution of the insulin superfamily: cloning of a hybrid insulin/insulin-like growth factor cDNA from amphioxus. Proc. Natl. Acad. Sci. USA, 1990, 87(23), 9319-9323.
[http://dx.doi.org/10.1073/pnas.87.23.9319] [PMID: 1701257]
[11]
Steiner, D.F.; Chan, S.J.; Welsh, J.M.; Kwok, S.C.M. Structure and evolution of the insulin gene. Annu. Rev. Genet., 1985, 19, 463-484.
[http://dx.doi.org/10.1146/annurev.ge.19.120185.002335] [PMID: 3909947]
[12]
Nagamatsu, S.; Chan, S.J.; Falkmer, S.; Steiner, D.F. Evolution of the insulin gene superfamily. Sequence of a preproinsulin-like growth factor cDNA from the Atlantic hagfish. J. Biol. Chem., 1991, 266(4), 2397-2402.
[PMID: 1989990]
[13]
Chan, S.J.; Nagamatsu, S.; Cao, Q-P.; Steiner, D.F. Structure and evolution of insulin and insulin-like growth factors in chordates. Prog. Brain Res, 1992, 92, 15-24.
[http://dx.doi.org/ 10.1016/S0079-6123(08)61161-9] [PMID: 1302874]
[14]
Conlon, J.M.; Bondareva, V.; Rusakov, Y.; Plisetskaya, E.M.; Mynarcik, D.C.; Whittaker, J. Characterization of insulin, glucagon, and somatostatin from the river lamprey, Lampetra fluviatilis. Gen. Comp. Endocrinol., 1995, 100(1), 96-105.
[http://dx.doi.org/10.1006/gcen.1995.1138] [PMID: 8575665]
[15]
Upton, Z.; Francis, G.L.; Chan, S.J.; Steiner, D.F.; Wallace, J.C.; Ballard, F.J. Evolution of insulin-like growth factor (IGF) function: production and characterization of recombinant hagfish IGF. Gen. Comp. Endocrinol., 1997, 105(1), 79-90.
[http://dx.doi.org/10.1006/gcen.1996.6802] [PMID: 9000470]
[16]
Shamblott, M.J.; Chen, T.T. Identification of a second insulin-like growth factor in a fish species. Proc. Natl. Acad. Sci. USA, 1992, 89(19), 8913-8917.
[http://dx.doi.org/10.1073/pnas.89.19.8913] [PMID: 1409585]
[17]
Conlon, M.J. Molecular Evolution of Insulin in Non-Mammalian Vertebrates. Am. Zool., 2000, 40, 200-212.
[18]
Conlon, J.M. Evolution of the insulin molecule: insights into structure-activity and phylogenetic relationships. Peptides, 2001, 22(7), 1183-1193.
[http://dx.doi.org/10.1016/S0196-9781(01)00423-5] [PMID: 11445250]
[19]
Murray-Rust, J.; McLeod, A.N.; Blundell, T.L.; Wood, S.P. Structure and evolution of insulins: implications for receptor binding. BioEssays, 1992, 14(5), 325-331.
[http://dx.doi.org/10.1002/bies.950140507] [PMID: 1322139]
[20]
Leibush, B.N. Receptors of the Insulin Family Peptides in Evolution of Vertebrates; Insulin and the Insulin-Like Growth Factor-1 - Receptor Interaction in Fissues of Lamprey Lampetra fluviatilis. Zh. Evol. Biokhim. Fiziol., 1999, 35, 204-210.
[21]
Muggeo, M.; Ginsberg, B.H.; Roth, J.; Neville, D.M., Jr; De Meyts, P.; Kahn, C.R. The insulin receptor in vertebrates is functionally more conserved during evolution than insulin itself. Endocrinology, 1979, 104(5), 1393-1402.
[http://dx.doi.org/10.1210/endo-104-5-1393] [PMID: 35339]
[22]
Leibush, B.; Párrizas, M.; Navarro, I.; Lappova, Y.; Maestro, M.A.; Encinas, M.; Plisetskaya, E.M.; Gutiérrez, J. Insulin and insulin-like growth factor-I receptors in fish brain. Regul. Pept., 1996, 61(2), 155-161.
[http://dx.doi.org/10.1016/0167-0115(95)00154-9] [PMID: 8852819]
[23]
Leibush, B.N.; Lappova, Y.L.; Gutiérrez, J.; Plisetskaya, E.M. Lamprey but not porcine insulin binds with different affinity to lamprey and rat hepatocytes. Comp. Biochem. Physiol. C Pharmacol. Toxicol. Endocrinol., 1997, 116(2), 135-139.
[http://dx.doi.org/10.1016/S0742-8413(96)00195-8] [PMID: 9134699]
[24]
Leibush, B.N. Insulin and insulin-like growth factor 1 receptors: structural and functional divergence of two evolutionary related molecules. Zh. Evol. Biokhim. Fiziol., 1998, 34(1), 82-96.
[PMID: 9720152]
[25]
Kahn, C.R.; Freychet, P.; Roth, J.; Neville, D.M., Jr Quantitative aspects of the insulin-receptor interaction in liver plasma membranes. J. Biol. Chem., 1974, 249(7), 2249-2257.
[PMID: 4362069]
[26]
Lappova, Y.L.; Leibush, B.N. Receptor-mediated endocytosis of insulin in lower vertebrates: internalization and intracellular processing of 125I-insulin in isolated hepatocytes of lamprey and frog. Gen. Comp. Endocrinol., 1995, 100(1), 1-9.
[http://dx.doi.org/10.1006/gcen.1995.1125] [PMID: 8575649]
[27]
Freychet, P.; Roth, J.; Neville, D.M., Jr Insulin receptors in the liver: specific binding of (125 I)insulin to the plasma membrane and its relation to insulin bioactivity. Proc. Natl. Acad. Sci. USA, 1971, 68(8), 1833-1837.
[http://dx.doi.org/10.1073/pnas.68.8.1833] [PMID: 4331561]
[28]
Maggi, D.; Andraghetti, G.; Carpentier, J.L.; Cordera, R. Cys860 in the extracellular domain of insulin receptor β-subunit is critical for internalization and signal transduction. Endocrinology, 1998, 139(2), 496-504.
[http://dx.doi.org/10.1210/endo.139.2.5744] [PMID: 9449617]
[29]
Ceresa, B.P.; Kao, A.W.; Santeler, S.R.; Pessin, J.E. Inhibition of clathrin-mediated endocytosis selectively attenuates specific insulin receptor signal transduction pathways. Mol. Cell. Biol., 1998, 18(7), 3862-3870.
[http://dx.doi.org/10.1128/MCB.18.7.3862] [PMID: 9632770]
[30]
Leibush, B.N.; Lappova, Y.L. Insulin receptor downregulation in isolated hepatocytes of river lamprey (Lampetra fluviatilis). Gen. Comp. Endocrinol., 1995, 100(1), 10-17.
[http://dx.doi.org/10.1006/gcen.1995.1126] [PMID: 8575650]
[31]
Lappova, Y.L.; Leibush, B.N. Receptor-mediated endocytosis in poikilothermic cells. I-Insulin internalization in lamprey and frog hepatocytes. Tsitologia, 1994, 36, 972-977. [Article in Russian
[32]
Lappova, Y.L.; Leibush, B.N. Receptor-mediated endocytosis in poikilothermic cells. II-Internalized 125I-insulin fate in isolated lamprey and frog hepatocytes. Tsitologia, 1994, 36, 978-985.
[33]
Kolychev, A.P.; Ternovskaya, E.E. Peculiarities of distribution of 125-I-insulin and 125I-insulin-like growth factor-I (IGF-I) at internalization in isolated rat hepatocytes. Zh. Evol. Biokhim. Fiziol., 2014, 50(1), 51-58.
[PMID: 25486806]
[34]
Kolychev, A.P.; Ternovskaya, E.E.; Arsenyeva, A.V.; Shapkina, E.V. Differences in time course of internalization of receptors of insulin and insulin-like growth factor (IGF-1) in isolated rat hepatocytes. J. Evol. Biochem. Physiol., 2013, 49, 597-607.
[http://dx.doi.org/10.1134/S0022093013060078]
[35]
Kolychev, A.P.; Ternovskaya, E.E. Different 125I-insulin and 125I-IGF-I internalization ways are in chicken hepatocytes. They are same in birds and mammals roceeding of II International Scientific & Practical Conference “World Science”, “Topical. Problems Of Modern Science & Possible Solutions, 2015, 2, 24-36.
[36]
Kolychev, A.P.; Ternovskaya, E.E. 125I-Insulin and 125I-Insulinlike Growth Factor-I in Chicken Hepatocytes Internalization. The Peptides Distribution and Action in Birds. Curr. Chem. Biol., 2018, 12, 150-157.
[http://dx.doi.org/10.2174/2212796812666180524095558]
[37]
Kolychev, A.P.; Ternovskaya, E.E. Role of 125I-insulin and 125IIGF- I exocytose in adaptation of rat isolated hepatocytes to low temperature. In IGF & Insulin System in Physiology & Disease. The IGFs and Insulin System: Emerging Themes in Aging, Diabetes, Cancer and Other Diseases (Gordon IGF Conference), 2015.
[38]
Kolychev, A.P.; Korf, E.A.; Terpilovskii, M.A. Comparative aspect of 125I-insulin and 125I-insulin-like growth factor-I (IGF-I) exocytosis in isolated rat and chicken hepatocytes. To the question of insulin functional role in chicken International conference materials “Receptors and intracellular signalling” (International Pushchino Conference), 2017, 2, 759-765.
[39]
Kolychev, A.P.; Ternovskaya, E.E. Insulin-like growth factor I (IGF-I) and insulin receptor distribution during endocytosis in cellkey element in development of IGF-I and insulin functional role in organism Materials of IX International scientific-practical conference “Modern advantages of science -2013, 2013, 59, 61-65.
[40]
Bhaumick, B.; Armstrong, E.A. Differential binding and internalization of insulin-like growth factor (IGF)-I in cultured human trophoblast and JEG-3 cells: possible modulatory effect of IGF binding proteins (BP). Endocrine, 1995, 3(9), 677-683.
[http://dx.doi.org/10.1007/BF02746344] [PMID: 21153226]
[41]
Giudice, J.; Barcos, L.S.; Guaimas, F.F.; Penas-Steinhardt, A.; Giordano, L.; Jares-Erijman, E.A.; Coluccio Leskow, F. Insulin and insulin like growth factor II endocytosis and signaling via insulin receptor B. Cell Commun. Signal., 2013, 11(1), 18.
[http://dx.doi.org/10.1186/1478-811X-11-18] [PMID: 23497114]

Rights & Permissions Print Cite
Article Metrics
13
2
© 2024 Bentham Science Publishers | Privacy Policy