Proenkephalin A is Expressed in Mesodermal Lineages During Organogenesis

Overview

Journal EMBO J

Specialties Biotechnology
Molecular Biology

Date 1989 Oct 1

PMID 2583085

Citations 14

Authors

E Keshet

R D Polakiewicz

A Itin

A Ornoy

H Rosen

Affiliations

Soon will be listed here.

Abstract

Proenkephalin A (PEA) encodes several neuropeptides with an opioid activity, as well as other peptides with as yet unknown functions. As an initial step toward finding possible roles for PEA gene products in non-neuronal tissues, we have determined sites of PEA expression during mouse embryonic development, employing in situ hybridization. We report here the unexpected observation that in addition to its abundance in brain, PEA RNA is expressed in non-differentiated mesodermal cells of diverse lineages in the process of their development into several adult tissues and organs; it drops to undetectable levels upon terminal differentiation of these tissues. In a particular example of differentiating mesoderm, the developing kidney, the transient expression of PEA mRNA and of its encoded peptide Met-enkephalin was demonstrated by both in situ and Northern blot hybridizations, as well as by a radioimmunoassay. These findings suggest a novel role for PEA-derived peptide(s) in mesoderm growth or differentiation during organogenesis.

Citing Articles

Disparate Effects of Stressors on Met-Enkephalin System Parameters and on Plasma Concentrations of Corticosterone in Young Female Chickens.

Scanes C, Pierzchala-Koziec K Animals (Basel). 2024; 14(15).

PMID: 39123727 PMC: 11310960. DOI: 10.3390/ani14152201.

Pre-proenkephalin 1 is Downregulated Under Unloading and is Involved in Osteoblast Biology.

Puri C, Dannenberg C, Ucci A, Ponzetti M, Pucci E, Silvestri L Calcif Tissue Int. 2024; 114(5):524-534.

PMID: 38506955 PMC: 11061007. DOI: 10.1007/s00223-024-01199-z.

A "Drug-Dependent" Immune System Can Compromise Protection against Infection: The Relationships between Psychostimulants and HIV.

Assis M, Carranza P, Ambrosio E Viruses. 2021; 13(5).

PMID: 33919273 PMC: 8143316. DOI: 10.3390/v13050722.

Distinct cell proliferation, myogenic differentiation, and gene expression in skeletal muscle myoblasts of layer and broiler chickens.

Nihashi Y, Umezawa K, Shinji S, Hamaguchi Y, Kobayashi H, Kono T Sci Rep. 2019; 9(1):16527.

PMID: 31712718 PMC: 6848216. DOI: 10.1038/s41598-019-52946-4.

Localization of , , , , and Expression in the Developing Retina, Muscle, and Sclera of the Embryonic Mouse Eye.

Wan Y, White C, Robert N, Rogers M, Szabo-Rogers H J Histochem Cytochem. 2019; 67(12):863-871.

PMID: 31638440 PMC: 6882067. DOI: 10.1369/0022155419885112.

References

Hughes J, Smith T, KOSTERLITZ H, Fothergill L, Morgan B, Morris H . Identification of two related pentapeptides from the brain with potent opiate agonist activity. Nature. 1975; 258(5536):577-80. DOI: 10.1038/258577a0. View

Gurdon J, Mohun T, Sharpe C, Taylor M . Embryonic induction and muscle gene activation. Trends Genet. 1989; 5(2):51-6. DOI: 10.1016/0168-9525(89)90022-x. View

Noda M, Furutani Y, Takahashi H, Toyosato M, Hirose T, INAYAMA S . Cloning and sequence analysis of cDNA for bovine adrenal preproenkephalin. Nature. 1982; 295(5846):202-6. DOI: 10.1038/295202a0. View

Gubler U, Seeburg P, HOFFMAN B, Gage L, UDENFRIEND S . Molecular cloning establishes proenkephalin as precursor of enkephalin-containing peptides. Nature. 1982; 295(5846):206-8. DOI: 10.1038/295206a0. View

Comb M, Seeburg P, Adelman J, Eiden L, Herbert E . Primary structure of the human Met- and Leu-enkephalin precursor and its mRNA. Nature. 1982; 295(5851):663-6. DOI: 10.1038/295663a0. View

Liston D, Vanderhaeghen J, Rossier J . Presence in brain of synenkephalin, a proenkephalin-immunoreactive protein which does not contain enkephalin. Nature. 1983; 302(5903):62-5. DOI: 10.1038/302062a0. View

Uhler M, Herbert E, DEustachio P, Ruddle F . The mouse genome contains two nonallelic pro-opiomelanocortin genes. J Biol Chem. 1983; 258(15):9444-53. View

Akil H, Watson S, Young E, Lewis M, Khachaturian H, Walker J . Endogenous opioids: biology and function. Annu Rev Neurosci. 1984; 7:223-55. DOI: 10.1146/annurev.ne.07.030184.001255. View

Douglass J, Civelli O, Herbert E . Polyprotein gene expression: generation of diversity of neuroendocrine peptides. Annu Rev Biochem. 1984; 53:665-715. DOI: 10.1146/annurev.bi.53.070184.003313. View

10.

Rosen H, Douglass J, Herbert E . Isolation and characterization of the rat proenkephalin gene. J Biol Chem. 1984; 259(22):14309-13. View

11.

Nilsson J, von Euler A, Dalsgaard C . Stimulation of connective tissue cell growth by substance P and substance K. Nature. 1985; 315(6014):61-3. DOI: 10.1038/315061a0. View

12.

Civelli O, Douglass J, Goldstein A, Herbert E . Sequence and expression of the rat prodynorphin gene. Proc Natl Acad Sci U S A. 1985; 82(12):4291-5. PMC: 397984. DOI: 10.1073/pnas.82.12.4291. View

13.

Kilpatrick D, Howells R, Noe M, Bailey L, UDENFRIEND S . Expression of preproenkephalin-like mRNA and its peptide products in mammalian testis and ovary. Proc Natl Acad Sci U S A. 1985; 82(21):7467-9. PMC: 391366. DOI: 10.1073/pnas.82.21.7467. View

14.

Imura H, Kato Y, Nakai Y, Nakao K, Tanaka I, Jingami H . Endogenous opioids and related peptides: from molecular biology to clinical medicine. The Sir Henry Dale lecture for 1985. J Endocrinol. 1985; 107(2):147-57. DOI: 10.1677/joe.0.1070147. View

15.

Liebisch D, Weber E, Kosicka B, Gramsch C, Herz A, Seizinger B . Isolation and structure of a C-terminally amidated nonopioid peptide, amidorphin-(8-26), from bovine striatum: a major product of proenkephalin in brain but not in adrenal medulla. Proc Natl Acad Sci U S A. 1986; 83(6):1936-40. PMC: 323199. DOI: 10.1073/pnas.83.6.1936. View

16.

Howells R, Kilpatrick D, Bailey L, Noe M, UDENFRIEND S . Proenkephalin mRNA in rat heart. Proc Natl Acad Sci U S A. 1986; 83(6):1960-3. PMC: 323204. DOI: 10.1073/pnas.83.6.1960. View

17.

Zurawski G, Benedik M, Kamb B, Abrams J, Zurawski S, Lee F . Activation of mouse T-helper cells induces abundant preproenkephalin mRNA synthesis. Science. 1986; 232(4751):772-5. DOI: 10.1126/science.2938259. View

18.

Kilpatrick D, Millette C . Expression of proenkephalin messenger RNA by mouse spermatogenic cells. Proc Natl Acad Sci U S A. 1986; 83(14):5015-8. PMC: 323880. DOI: 10.1073/pnas.83.14.5015. View

19.

Yoshikawa K, Sabol S . Expression of the enkephalin precursor gene in C6 rat glioma cells: regulation by beta-adrenergic agonists and glucocorticoids. Brain Res. 1986; 387(1):75-83. DOI: 10.1016/0169-328x(86)90022-7. View

20.

Kilpatrick D, Borland K, Jin D . Differential expression of opioid peptide genes by testicular germ cells and somatic cells. Proc Natl Acad Sci U S A. 1987; 84(16):5695-9. PMC: 298929. DOI: 10.1073/pnas.84.16.5695. View