Receptors of insulin and of insulin-like growth factor 1: Pathways of structural and functional divergence of two evolutionary related molecules

Journal of Evolutionary Biochemistry and Physiology

Volumn 34, Issue 1, 1998, Pages 62-71

  Leibush, B N ^a  

^a SECHENOV INSTITUTE OF EVOLUTIONARY PHYSIOLOGY AND BIOCHEMISTRY   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 22644449547     PISSN: 00220930     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (99)

1. De Pablo, F., Scott, L.A., and Roth, J., Insulin and Insulin-Like Growth Factor 1 in Early Development: Peptides, Receptors and Biological Events, Endocrine Rev., 1990, vol. 11, pp. 558-577.
2. King, G.L. and Kahn, C.R., The Growth Promoting Effects of Insulin, Growth and Growth Maturation Factors, Gruff, G., Ed., New York: Wiley, 1984, pp. 224-265.
3. Froesch, E.R., Schmid, C., Schwander, J., and Zapf, J., Actions of Insulin-Like Growth Factors, Ann. Rev. Physiol., 1985, vol. 47, pp. 443-467.
4. Riderknecht, E. and Humbel, R.E., The Amino Acid Sequence of Human Insulin-Like Growth Factor 1 and Its Structural Homology with Proinsulin, J. Biol. Chem., 1978, vol. 253, pp. 2769-2776.
5. Murray-Rust, J., McLeod, A.N., Blundell, T.L., and Wood, S.P., Structure and Evolution of Insulins: Implications for Receptor Binding, BioEssays, 1992, vol. 14, pp. 325-331.
6. Riderknecht, E. and Humbel, R.E., Primary Structure of Human Insulin-Like Growth Factor 2, FEBS Lett., 1978, vol. 89, pp. 283-286.
7. Schwabe, C., McDonald, J.K., and Steiner, B.G., Primary Structure of the β-Chain of Porcine Relaxin, Biochem. Biophys. Res. Comm., 1977, vol. 75, pp. 503-510.
8. Nagasawa, H., Suzuki, A., and Ishizaki, H., Amino Acid Sequence of a Prothoracicotrophic Hormone of the Silkworm Bombix more, Proc. Natl. Acad. Sci. USA, 1986, vol. 83, pp. 5840-5843.
9. Smit, A.B., Vreugdenhil, E., Ebberink, et al., Growth Controlling Molluscan Neurons Produce the Precursor of an Insulin-Related Peptide, Nature, 1988, vol. 331, pp. 535-538.
10. Rusakov, Yu.I., Bondareva, V.M., Karasev, V.S., et al., Some Biochemical Characteristics of Insulin-Like Substance of the Bivalved Mollusc Anadonta cyanea, Biokhimiya, 1991, vol. 56, pp. 718-726.
11. Ebina, Y., Ellis, L., Jarnagin, J., et al., The Human Insulin Receptor cDNA: the Structural Basis for Hormone-Activated Transmembrane Signaling, Cell, 1985, vol. 40, pp. 747-758.
12. Ullrich, A., Bell, J.R., Chen, E.Y., et al., Human Insulin Receptor and Its Relationship to the Tyrosine Kinase Family of Oncogenes, Nature, 1985, vol. 313, pp. 756-761.
13. Ullrich, A., Gray, A., Tam, A.W., et al., Insulin-Like Growth Factor 1 Receptor Primary Structure: Comparison with Insulin Receptor Suggests Structural Determinants that Define Functional Specificity, The EMBO J., 1986, vol. 5, pp. 2503-2512.
14. White, M.F. and Kahn, C.R., Mechanisms of Insulin Action, Insulin Resistance, Miller, D.E., Ed., New York: Wiley, 1993, pp. 9-47.
15. He, W., Craparo, A., Zhu, Y., et al., Interaction of Insulin Receptor Substrate 2 (IRS-2) with the Insulin and Insulin-Like Growth Factor 1 Receptors. Evidence for Two Distinct Phosphotyrosine-Dependent Interaction Domains with IRS-2, J. Biol. Chem., 1996, vol. 271, pp. 11641-11645.
16. Danielsen, A.G. and Roth, R.A., Role of the Juxtamembrane Tyrosine in Insulin Receptor-Mediated Tyrosine Phosphorylation of p60 Endogenous Substrates, Endocrinology, 1996, vol. 137, pp. 5326-5331.
17. White, M.F. and Kahn, C.R., The Insulin Signaling System, J. Biol. Chem., 1994, vol. 269, pp. 1-4.
18. Zapf, A., Hsu, D., and Olefsky, J.M., Comparison of the Intracellular Itineraries of Insulin-Like Growth Factor 1 and Insulin and their Receptors in Rat-1 Fibroblasts, Endocrinology, 1994, vol. 134, pp. 2445-2452.
19. Shoelson, S.E., White, M.F., and Kahn, C.R., Tryptic Activation of the Insulin Receptor. Proteolytic Truncation of the α-Subunit Releases the β-Subunit from Inhibitory Control, J. Biol. Chem., 1988, vol. 263, pp. 4852-4860.
20. Maddux, B.A. and Goldfine, I.D., Evidence that Insulin plus ATP May Induce a Conformational Change in the Subunit of the Insulin Receptor without Inducing Receptor Autophosphorylation, J. Biol. Chem., 1991, vol. 266, pp. 6731-6736.
21. Schlessinger, J. and Ullrich, A., Growth Factor Signaling by Receptor Tyrosine Kinases, Neuron, 1992, vol. 9, pp. 383-391.
22. Tobe, K., Tamemoto, H., Yamaguchi, T., et al. Identification of a 190-kDa Protein as a Novel Substrate for the Insulin Receptor Kinase Functionally Similar to Insulin Receptor Substrate-1, J. Biol. Chem., 1995, vol. 270, pp. 5698-5701.
23. Sun, X.J., Wang, L.-M., Zhang, Y., et al., Role of IRS-2 in Insulin and Cytokine Signaling, Nature, 1995, vol. 377, pp. 173-177.
24. Patti, M.E., Sun, X.J., Bruening, J.C., et al., 4PS/Insulin Receptor Substrate (IRS-2) is the Alternative Substrate of the Insulin Receptor in 1RS-1-Deficient Mice, J. Biol. Chem., 1995, vol. 270, pp. 24670-24673.
25. Myers, M.G., Sun, X.J., Cheatham, B., et al., IRS-1 is a Common Element in Insulin and Insulin-Like Growth Factor 1 Signaling to the Phosphatidylinositol 3′-Kinase, Endocrinology, 1993, vol. 132, pp. 1421-1430.
26. Graparo,A., O'Neil, T.J., and Gustafson, T.A., Non-SH2 Domains within Insulin Receptor Substrate 1 and SNC Mediate their Phosphotyrosine-Dependent Interaction with the NPEY Motif of the Insulin-Like Growth Factor 1 Receptor, J. Biol. Chem., 1995, vol. 270, pp. 15639-15643.
27. Xu, B., Bird, G., and Miller, W.T., Substrate Specificities of the Insulin and Insulin-Like Growth Factor 1 Receptor Tyrosine Kinase Catalytic Domains, J. Biol. Chem., 1995, vol. 270, pp. 29825-29830.
28. Seely, B.L., Reichart, D.R., Straub, P.A., et al., Localization of the Insulin-Like Growth Factor 1 Receptor Binding Sites for the SH2 Domain Proteins p85, Syp and GTPase Activating Protein, J. Biol. Chem., 1995, vol. 270, pp. 19151-19157.
29. Beitner-Johnson, D. and LeRoith, Insulin Growth Factor 1 Stimulates Tyrosine Phosphorylation of Endogenous cCrs, J. Biol. Chem., 1995, vol. 270, pp. 5187-5190.
30. Pertseva, M.N., Shpakov, A.O., and Plesneva, S.A., The Current Progress in Studies on Signaling Mechanisms of Action of Insulin and of Insulin-Like Peptides, Zh. Evol. Biokim. Fiziol., 1996, vol. 32, pp. 318-339.
31. Saltiel, A.R., Diverse Signaling Pathways in the Cellular Action of Insulin, Am. J. Physiol., 1996, vol. 270, pp. E375-E378.
32. Drasnin, B., Editorial: Insulin Signaling Network - Waiting for Copernicus, Endocrinology, 1996, vol. 137, pp. 2647-2648.
33. Rechler, M.M. and Nissley, S.P., The Nature and Regulation of the Receptors for Insulin-Like Growth Factors, Ann. Rev. Physiol., 1985, vol. 1985, pp. 425-442.
34. Seino, S., Seino, G., and Bell, G.J., Human Insulin-Receptor Gene, Diabetes, 1990, vol. 39, pp. 123-128.
35. Abbott, A.M., Bueno, R., Pedrini, M.T., et al., Insulin-Like Growth Factor 1 Receptor Gene Structure, J. Biol. Chem., 1992, vol. 267, pp. 10759-10763.
36. Shier, P. and Watt, V.M., Primary Structure of a Putative Receptor for a Ligand of the Insulin Family, J. Biol. Chem., 1989, vol. 264, pp. 14605-14608.
37. Zhang, B and Roth, R.A., The Insulin Receptor-Related Receptor. Tissue Expression, Ligand Binding Specificity and Signaling Capabilities, J. Biol. Chem., 1992, vol. 267, pp. 18320-18328.
38. Bajaj, M., Waterfield, M.D., and Schlessinger, J., On the Tertiary Structure of the Extracellular Domains of the Epidermal Growth Factor and Insulin Receptors, Biochim. Biophys. Acta, 1987, vol. 916, pp. 220-226.
39. Wedekind, F., Baer-Pontzen, K., Bala-Mohan, S., et al., Hormone Binding Site of the Insulin Receptor: Analysis Using Photoaffinity Mediated Adivin Complexing, Hoppe-Seyler J. Biol. Chem., 1989, vol. 370, pp. 251-258.
40. De Meyts, P., Gu, J.L., Shymko, R.M., et al., Identification of a Ligand-Binding Region of the Human Insulin Receptor Encoded by the Second Exon of the Gene, Mol. Endocrinol., 1990, vol. 409, pp. 409-416.
41. Kjeldsen, T., Andersen, A.S., Wiberg, F.C., et al., The Ligand Specificities of Insulin Receptor and the Insulin-Like Growth Factor 1 Receptor Reside in Different Regions of a Common Binding Site, Proc. Natl. Acad. Sci. USA, 1991, vol. 88, pp. 4404-4408.
42. Kadowaki, T., Kadowaki, H., Accili, D., and Taylor, S.J., Substitution of Lysine for Asparagine at Position 15 in the α-Subunit of Human Insulin Receptor. A Mutation that Impairs Transport of Receptors to the Cell Surface and Decreases the Affinity of Insulin Binding, J. Biol. Chem., 1990, vol. 265, pp. 19143-19150.
43. Kjeldsen, T., Wiberg, F.C., and Andersen, A.S., Chimeric Receptors Indicate that Phenylalanine 39 Is a Major Contributor to Insulin Specificity, J. Biol. Chem., 1994, vol. 269, pp. 32942-32946.
44. Gronskov, K., Vissing, H., and Shymko, R.M., Mutation of Arginine 86 to Proline in the Insulin Receptor Alpha Subunit Causes Lack of Transport of the Receptor to the Plasma Membrane, Loss of Binding Affinity and a Constitutively Activated Tyrosine Kinase in Transfected Cells, Biochem. Biophys. Res. Commun., 1993, vol. 192, pp. 905-911.
45. Nakae, J., Morioka, H., Ohtsuka, E., and Fujieda, K., Replacement of Leucine 87 in Human Insulin Receptor Alters Affinity for Insulin, J. Biol. Chem., 1995, vol. 270, pp. 22017-22022.
46. Fabry, M., Schaefer, E., Ellis, L., et al., Detection of a New Hormone Contact Site within the Insulin Receptor Ectodomain by the Use of a Novel Photoreactive Insulin, J. Biol. Chem., 1992, vol. 267, pp. 8950-8956.
47. Gustafson, T.A. and Rutter, W.J., The Cysteine-Rich Domains of the Insulin and Insulin-Like Growth Factor 1 Receptor are Primary Determinants of Hormone Binding Specificity, J. Biol. Chem., 1990, vol. 265, pp. 18663-18667.
48. Zhang, B and Roth, R.A., A Region of the Insulin Receptor Important for Ligand Binding (Residues 405-601) is Recognized by Patients Autoimmune Antibodies and Inhibitory Monoclonal Antibodies, Proc. Natl. Acad. Sci. USA, 1991, vol. 88, pp. 9858-9862.
49. Kadowaki, T., Accili, D., Taylor, S.J., et al., Two Mutant Alleles of the Insulin Receptor Gene in a Patient with Extreme Insulin Resistance, Science, 1988, vol. 240, pp. 787-790.
50. Roach, P., Zick, Y., Formisano, P., et al., A Novel Human Insulin Receptor Mutation Uniquely Inhibits Insulin Binding without Impairing Posttranslational Processing, Diabetes, 1994, vol. 43, pp. 1096-1102.
51. Vip, C.C., Hsu, H., Patel, R.G., et al., Localization of the Insulin-Binding Site to the Cysteine-Rich Region of the Insulin Receptor α-Subunit, Biochem. Biophys. Res. Commun., 1988, vol. 157, pp. 321-329.
52. Rafaeloff, R., Patel, R., Vip, C., et al., Mutation of the High Cysteine Region of the Human Insulin Receptor Binding Affinity and Transmembrane Signaling, J. Biol. Chem., 1989, vol. 264, pp. 15900-15904.
53. Schumacher, R., Mosthaf, L., Schlessinger, J., et al., Insulin and Insulin Growth Factor 1 Binding Specificity is Determined by Distinct Regions of their Cognate Receptors, J. Biol. Chem., 1991, vol. 266, pp. 19288-19295.
54. Schumacher, R., Soos, M.A., Schlessinger, J., et al., Signaling-Complement Receptor Chimeras Allow Mapping of Major Insulin Receptor Binding Domain Determinants, J. Biol. Chem., 1993, vol. 268, pp. 1087-1094.
55. Zhang, B. and Roth, R.A., Binding Properties of Chimeric Insulin Receptor Containing the Cysteine-Rich Domain of Either the Insulin-Like Growth Factor 1 Receptor or the Insulin Receptor Related Receptor, Biochemistry, 1991, vol. 30, pp. 5113-5117.
56. Seino, S. and Bell, G.J., Alternative Splicing of Human Insulin Receptor Messenger RNA, Biochem. Biophys. Res. Commun., 1989, vol. 159, pp. 312-316.
57. McClain, Mosthaf, L., and Ullrich, A., Properties of the Two Naturally Occurring Alternate Form of the Insulin Receptor, Diabetes, 1989, vol. 38, suppl. 2, p. 1A.
58. Moller, D.E., Yokota, A., Caro, J.F., and Fillier, J.S., Tissue-Specific Expression of Two Alternative Spliced Insulin Receptor mRNA's in Man, Mol. Endocrinol., 1989, vol. 3, pp. 1263-1269.
59. Mosthaf, L., Grako, K., and Dull, T.J., Functionally Distinct Insulin Receptors Generated by. Tissue-Specific Alternative Splicing, EMBO J., 1990, vol. 9, pp. 2409-2413.
60. Norgren, S., Zierath, J., Wedell, A., et al., Regulation of Human Insulin Receptor RNA Splicing in vivo, Proc. Natl. Acad. Sci. USA, 1994, vol. 91, pp. 1465-1469.
61. Hansen, T., Bjorbaek, C., Vestergaad, H., et al., Expression of Insulin Receptor Spliced Variants and Their Functional Correlates in Muscle from Patients with Non-Insulin-Dependent Diabetes Mellitus, J. Clin. Endocrinol. Metab., 1993, vol. 77, pp. 1500-1505.
62. McClain, D.A., Different Ligand Affinities of Two Human Insulin Receptor Splice Variants are Reflected in Parallel Changes in Sensitivity for Insulin Action, Mol. Endocrinol., 1991, vol. 5, pp. 734-739.
63. Vogt, B., Carrascosa, J.M., Ermel, B., et al., The Two Isotypes of the Human Insulin Receptor (HIR-A and HIR-B) Follow Different Internalization Kinetics, Biochem. Biophys. Res. Comun., 1991, vol. 177, pp. 1013-1018.
64. Yamaguchi, Y., Flier, J.S., Benecke, B.J., et al., Ligand-Binding Properties of the Two Isoforms of the Human Insulin Receptors, Endocrinology, 1993, vol. 132, pp. 1132-1138.
65. Kosaki, A., Pillay, T.S., Xu, L., and Webster, N.J.G., The B Isoform of the Insulin Receptor Signals More Efficiently than the A Isoform in Hep G2 Cells, J. Biol. Chem., 1995, vol. 270, pp. 20816-20823.
66. Condorelli, G., Bueno, R., and Smith, R.J., Two Alternatively Spliced Forms of the Human Insulin-Like Growth Factor 1 Receptor Have Distinct Biological Activities and Internalization Kinetics, J. Biol. Chem., 1994, vol. 269, pp. 8510-8516.
67. Moxham, C.P., Dumovo, V., and Jacobs, S., Insulin-Like Growth Factor 1 Receptor Beta-Subunit Heterogeneity: Evidence for Hybrid Tetramers Composed of Insulin-Like Growth Factor 1 and Insulin Receptor Heterodmers, J. Biol. Chem., 1989, vol. 264, pp. 1323-1344.
68. Soos, M.A. and Siddle, K., Immunological Relationships between Receptors for Insulin and Insulin-Like Growth Factor 1 Receptors Involving Hybrids with Insulin Receptors, Biochem. J., 1989, vol. 263, pp. 553-563.
69. Moss, A.M. and Livingston, J.N., Distinct β-Subunits are Present in Hybrid Insulin-Like Growth Factor 1 Receptors in Central Nervous System, Biochem. J., 1993, vol. 294, pp. 685-692.
70. Treadway, J.L., Morrison, B.D., Soon, M.A., et al., Transdominant Inhibition of Tyrosine Kinase Activity in Mutant Insulin/Insulin-Like Growth Factor 1 Hybrid Receptors, Proc. Natl. Acad. Sci. USA, 1991, vol. 88, pp. 214-218.
71. Frattali, A.L. and Pessin, J.E., Relationship between α-Subunit Ligand Occupancy and β-Subunit Autophosphorylation in Insulin/IGF-1 Hybrid Receptors, J. Biol. Chem., 1993, vol. 268, pp. 7393-7400.
72. Seely, B.L., Reichart, D.R., Takata, Y., et al., A Functional Assessment of Insulin/Insulin-Like Growth Factor 1 Hybrid Receptors, Endocrinology, 1995, vol. 136, pp. 1635-1641.
73. Alexandrides, T.K. and Smith, R.J., A Novel Fetal Insulin-Like Growth Factor 1 (IGF-1) Receptor. Mechanism for Increased IGF-1 and Insulin-Stimulated Tyrosine Kinase Activity in Fetal Muscle, J. Biol. Chem., 1989, vol. 264, pp. 12922-12930.
74. Chan, S.J., Nagamatsu, S., Cao, Q.P., and Steiner, D.F., Structure and Evolution of Insulin and Insulin-Like Growth Factors in Chordates, Prog. Brain Res., 1992, vol. 92, pp. 15-24.
75. Nagamatsu, S., Chan, S.J., Falkmer, S., and Steiner, D.F., Evolution of the Insulin Gene Suprafamily. Sequence of a Preproinsulin-Like Growth Factor cDNA from the Atlantic Hagfish, J. Biol. Chem., 1991, vol. 266, pp. 2397-2402.
76. Plashmforoush, M., Chan, S.J., and Steiner, D.F., Structure and Expression of the Insulin-Like Peptide Receptor from Amphioxus, Mol. Endocrinol., vol. 1996, vol. 10, pp. 857-866.
77. Leibush, B.N., Evolutionary Aspects in Study of Insulin Receptors, Biokhim. Cheloveka i Zhivotnykh (Kiev), 1992, vol. 16, pp. 33-44.
78. Drakenberg, K., Sara, Y.R., Falkmer, S., et al., Identification of IGF-1 Receptors in Primitive Vertebrates, Regul. Peptides, 1993, vol. 43, pp. 73-81.
79. Ruan, Y.S., Chen, Y., and Garofalo, R.S., The Drosophila Insulin Receptor Contains a Novel Carboxyl-Terminal Extension Likely to Play an Important Role in Signal Transduction, J. Biol. Chem., 1995, vol. 270, pp. 4236-4243.
80. Petruzelli, L.M., Herrera, R., and Garcia-Arenas, R., The Insulin Receptor of Drosophila melanogaster, Cold Spring Harbor Conferences of Cell Proliferation, 1985, vol. 3, pp. 115-121.
81. Fernandez-Almonacid, R. and Rosen, O.M., Drosophila melanogaster. Structure and Ligand Specificity of the Drosophila melanogaster Insulin Receptor, Mol. Cell Biol., 1987, vol. 1987, pp. 2718-2727.
82. Roovers, J.F.A., van Heerikhuizen, H., Geraerts, W.P., et al., The Isolation of Genes Encoding the Receptor(s) for Molluscan Insulin-Related Peptides (MIPs) from the Freshwater Snail Lymnaea stagnalis, Proc. of Symposium on Molluscan Neurobiology, Amsterdam, 1990, p. 121,
83. Leibush, B., Bayraktaroglu, E., Maestro, M.A., et al., IGF-1 and Insulin Binding in Molluscs, Abstracts of Papers, 18th Conference of European Comparative Endocrinologists. Annales d'Endocrinologie, 1996, suppl. 4, pp. 28-29.
84. Lappova, Y.L. and Leibush, B.N., Receptor-Mediated Endocytosis of Insulin in Lower Vertebrates and Intracellular Processing of [125-I]-Insulin in Isolated Hepatocytes of Lamprey and Frog, Gen. Gomp. Endocrinol., 1995, vol. 100, pp. 1-9.
85. Le Bail, P.Y., Gentil, V., Neil, O., and Veil, C., IGFs Structure, Function and Regulation in Fish, Abstracts of Papers, 18th Conference of European Comparative Endocrinologists. Annales d'Endocrinologie, 1996, suppl. 4, p. 4.
86. Stuart, C.A., Characterization of a Novel Insulin Receptor From Stingray Liver, J. Biol. Chem., 1988, vol. 263, pp. 7881-7886.
87. Parrizas, M., Plisetskaya, E.M., Planas, J., and Gutierrez, J., Abundant Insulin-Like Growth Factor 1 (IGF-1) Receptor Binding in Fish Skeletal Muscle, Gen. Comp. Endocrinol., 1995, vol. 98, pp. 16-25.
88. Leibush, B., Parrizas, M., Navarro, I., et al., Insulin and Insulin-Like Growth Factor 1 Receptors in Fish Brain, Regul. Peptides, 1996, vol. 61, pp. 155-161.
89. Leibush, B.N. and Lappova, Yu.L., The Insulin and Insulin-Like Growth Factor 1 Receptors in Evolution of Vertebrates, I(XI) Mezhdunarodnoe soveshchanie po evolyutsionnoi fiziologii. Tezisy dokladov (Abstr. of I(XI) International Meet. on Evolutionary Physiology), St. Petersburg, 1996, pp. 130-131.
90. Moriyama, S., Dickhoff, W.W., and Plisetskaya, E.M., Isolation and Characterization of Insulin-Like Growth Factor 1 From Rainbow Trout Onchorhyncus mykiss, Gen. Comp. Endocrinol., 1995, vol. 99, pp. 221-229.
91. Parrizas, M., Maestro, M.A., Banos, N., et al., Insulin/IGF-1 Binding Ratio in Skeletal and Cardiac Muscles of Vertebrates: a Phylogenetic Approach, Am. J. Physiol., 1995, vol. 269, pp. R1370-R1377.
92. Moon, T.W., Castejon, C., Banos, N., et al. Insulin and IGF-1 Binding in Isolated Trout Cardiomyocytes, Gen. Comp. Endocrinol., 1996, vol. 103, pp. 264-272.
93. Muggeo, M., Ginsberg, B.H., Roth, J., et al., The Insulin Receptor in Vertebrates is Functionally More Conserved During Evolution than Insulin itself, Endocrinology, 1979, vol. 104, pp. 1393-1402.
94. Leibush, B.N., Insulin Receptors of the Brain in Vertebrate Evolution, Zh. Evol. Biokhim. Fiziol., 1983, vol. 47, pp. 407-413.
95. Leibush, B.N., Lappova, Y.L., Gutierrez, J., and Plisetskaya, E.M., Lamprey but not Porcine Insulin Binds with Different Affinity to Lamprey and Rat Hepatocytes, Comp. Biochem. Physiol., 1997, vol. 116C, pp. 135-139.
96. Chu, Y.S., Hu, S.Q., Zong, L., et al., Insulin-Like Compounds Related to the Amphioxus Insulin-Like Peptide, Biochemistry, 1994, vol. 33, pp. 11278-11285.
97. Larhammar, D., Evolution of the NPY-PYY-PP Family and Their Receptors, Abstracts of Papers, Conference of European Comparative Endocrinologists. Annales d'Endocrinologie, 1996, suppl. 4, p. 17.
98. Millar, R., Illing, N., Hapgood, J., et al., Coordinated Structural Evolution of GnRHs and Their Receptors-Insights from Comparative Studies, Proc. of the Third Congress of the Asia and Oceania Society for Comparative Endocrinology, Sydney, Australia, 1996, pp. 13-17.
99. Upton, Z., Francis, G.L., Chan, S.J., et al. Evolution of Insulin-Like Growth Factor (IGF) Function: Production and Characterization of Recombinant Hagfish IGF, Gen. Comp. Endocrinol., 1997, vol. 105, pp. 79-90.