Abstract
Although insulin and the insulin-like growth factors (IGFs) share marked similarities in amino acid sequence and biological activity, their evolutionary origins have not been resolved. To investigate this issue, we recently cloned a cDNA encoding an insulin-like peptide (ILP) from a primitive chordate species, amphioxus (Branchiostoma californiensis). The deduced sequence of amphioxus preproILP indicates that it is a hybrid molecule containing features characteristic of both insulin and IGF. Like proinsulin, amphioxus proILP contains a C-peptide, which is flanked by paired basic residues and is probably removed by proteolysis. However, proILP also contains an extended carboxyl-terminal peptide region that can be divided into D and E domains similar to those of proIGF. Sequence comparisons show that the amphioxus ILP A and B domains are equally homologous to those of human insulin and IGF-I and -II. Based on these results and the exon-intron organization of the amphioxus ILP gene, we propose that IGF emerged at a very early stage in vertebrate evolution from an ancestral insulin-type gene.
MeSH Terms
Amino Acid Sequence
Animals
Base Sequence
Biological Evolution
Chordata, Nonvertebrate/genetics
Cloning, Molecular
DNA/genetics,isolation & purification
Insulin/genetics
Insulin-Like Growth Factor I/genetics
Insulin-Like Growth Factor II/genetics
Molecular Sequence Data
Molecular Weight
Oligonucleotide Probes
Polymerase Chain Reaction
RNA/genetics,isolation & purification
RNA, Messenger/genetics,isolation & purification
Restriction Mapping
Sequence Homology, Nucleic Acid
Chemicals
Insulin
Oligonucleotide Probes
RNA, Messenger
RNA
Insulin-Like Growth Factor I
Insulin-Like Growth Factor II
DNA
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Chan S J
Department of Biochemistry and Molecular Biology, Howard Hughes Medical Institute, University of Chicago, IL 60637.
Cao Q P
Steiner D F
References (23)
23 references, click to expand
-
Growth-controlling molluscan neurons produce the precursor of an insulin-related peptide.
Nature. 1988 Feb 11;331(6156):535-8
PMID: 3340203
-
The biological activity and the binding affinity of modified insulins determined on isolated rat fat cells.
Diabetologia. 1974 Apr;10(2):105-13
PMID: 4367434
-
The human insulin receptor cDNA: the structural basis for hormone-activated transmembrane signalling.
Cell. 1985 Apr;40(4):747-58
PMID: 2859121
-
Insulin-like growth factors and insulin: comparative aspects.
Diabetologia. 1985 Aug;28(8):485-93
PMID: 3902539
-
The structure of 2Zn pig insulin crystals at 1.5 A resolution.
Philos Trans R Soc Lond B Biol Sci. 1988 Jul 6;319(1195):369-456
PMID: 2905485
-
Organization and sequence of the human insulin-like growth factor I gene. Alternative RNA processing produces two insulin-like growth factor I precursor peptides.
J Biol Chem. 1986 Apr 15;261(11):4828-32
PMID: 2937782
-
Rapid production of full-length cDNAs from rare transcripts: amplification using a single gene-specific oligonucleotide primer.
Proc Natl Acad Sci U S A. 1988 Dec;85(23):8998-9002
PMID: 2461560
-
Conservation of the sequence of islet amyloid polypeptide in five mammals is consistent with its putative role as an islet hormone.
Proc Natl Acad Sci U S A. 1989 Aug;86(15):5738-42
PMID: 2668946
-
Nucleotide sequence and growth hormone-regulated expression of salmon insulin-like growth factor I mRNA.
Mol Endocrinol. 1989 Dec;3(12):2005-10
PMID: 2628735
-
cDNA structure and expression of bombyxin, an insulin-like brain secretory peptide of the silkmoth Bombyx mori.
J Biol Chem. 1989 May 5;264(13):7681-5
PMID: 2708384
-
Structure and evolution of the insulin gene.
Annu Rev Genet. 1985;19:463-84
PMID: 3909947
-
Identification of a ligand-binding region of the human insulin receptor encoded by the second exon of the gene.
Mol Endocrinol. 1990 Mar;4(3):409-16
PMID: 2188117
-
cDNAs from neurosecretory cells of brains of Locusta migratoria (Insecta, Orthoptera) encoding a novel member of the superfamily of insulins.
Eur J Biochem. 1990 Jan 12;187(1):249-54
PMID: 1688797
-
Immunohistochemical localization of polypeptide hormones in endocrine cells of the digestive tract of Branchiostoma lanceolatum.
Cell Tissue Res. 1981;219(3):445-56
PMID: 7023687
-
Structure of a genomic clone encoding biologically active human relaxin.
Nature. 1983 Feb 17-23;301(5901):628-31
PMID: 6298628
-
Messenger RNA sequence and primary structure of preproinsulin in a primitive vertebrate, the Atlantic hagfish.
J Biol Chem. 1981 Jul 25;256(14):7595-602
PMID: 6265453
-
Insulin-like growth factor II precursor gene organization in relation to insulin gene family.
Nature. 1984 Aug 30-Sep 5;310(5980):777-81
PMID: 6382022
-
Sequence of a cDNA clone encoding human preproinsulin-like growth factor II.
Nature. 1984 Aug 30-Sep 5;310(5980):775-7
PMID: 6382021
-
Sequence of cDNA encoding human insulin-like growth factor I precursor.
Nature. 1983 Dec 8-14;306(5943):609-11
PMID: 6358902
-
Insulin-like growth factor: a model for tertiary structure accounting for immunoreactivity and receptor binding.
Proc Natl Acad Sci U S A. 1978 Jan;75(1):180-4
PMID: 272633
-
Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease.
Biochemistry. 1979 Nov 27;18(24):5294-9
PMID: 518835
-
A general method for isolation of high molecular weight DNA from eukaryotes.
Nucleic Acids Res. 1976 Sep;3(9):2303-8
PMID: 987581
-
Insulin-like growth factor I receptor primary structure: comparison with insulin receptor suggests structural determinants that define functional specificity.
EMBO J. 1986 Oct;5(10):2503-12
PMID: 2877871