Skip to main content
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1988 Jan;85(1):141–145. doi: 10.1073/pnas.85.1.141

Expression of the insulin-like growth factor II gene in the choroid plexus and the leptomeninges of the adult rat central nervous system.

F Stylianopoulou 1, J Herbert 1, M B Soares 1, A Efstratiadis 1
PMCID: PMC279499  PMID: 3422410

Abstract

The rat insulin-like growth factor II gene, encoding a fetal somatomedin, expresses a multitranscript family in embryonic/fetal tissues and in the adult brain and spinal cord. By performing in situ hybridization on tissue sections of adult brain and spinal cord, we have found that these transcripts are not expressed in neural or glial cells but are expressed in the epithelium of the choroid plexus of each cerebral ventricle and in the leptomeninges. We propose that the choroidal epithelial cells synthesize and secrete insulin-like growth factor II into the cerebrospinal fluid.

Full text

PDF
144

Images in this article

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Agnew W. F., Alvarez R. B., Yuen T. G., Crews A. K. Protein synthesis and transport by the rat choroid plexus and ependyma: an autoradiographic study. Cell Tissue Res. 1980;208(2):261–281. doi: 10.1007/BF00234876. [DOI] [PubMed] [Google Scholar]
  2. Alguacil-Garcia A., Pettigrew N. M., Sima A. A. Secretory meningioma. A distinct subtype of meningioma. Am J Surg Pathol. 1986 Feb;10(2):102–111. doi: 10.1097/00000478-198602000-00003. [DOI] [PubMed] [Google Scholar]
  3. Ashton I. K., Zapf J., Einschenk I., MacKenzie I. Z. Insulin-like growth factors (IGF) 1 and 2 in human foetal plasma and relationship to gestational age and foetal size during midpregnancy. Acta Endocrinol (Copenh) 1985 Dec;110(4):558–563. doi: 10.1530/acta.0.1100558. [DOI] [PubMed] [Google Scholar]
  4. Baxter R. C. The somatomedins: insulin-like growth factors. Adv Clin Chem. 1986;25:49–115. doi: 10.1016/s0065-2423(08)60124-9. [DOI] [PubMed] [Google Scholar]
  5. Binoux M., Hossenlopp P., Hardouin S., Seurin D., Lassarre C., Gourmelen M. Somatomedin (insulin-like growth factors)-binding proteins. Molecular forms and regulation. Horm Res. 1986;24(2-3):141–151. doi: 10.1159/000180553. [DOI] [PubMed] [Google Scholar]
  6. Bothwell M. Insulin and somatemedin MSA promote nerve growth factor-independent neurite formation by cultured chick dorsal root ganglionic sensory neurons. J Neurosci Res. 1982;8(2-3):225–231. doi: 10.1002/jnr.490080212. [DOI] [PubMed] [Google Scholar]
  7. Brown A. L., Graham D. E., Nissley S. P., Hill D. J., Strain A. J., Rechler M. M. Developmental regulation of insulin-like growth factor II mRNA in different rat tissues. J Biol Chem. 1986 Oct 5;261(28):13144–13150. [PubMed] [Google Scholar]
  8. Carlsson-Skwirut C., Jörnvall H., Holmgren A., Andersson C., Bergman T., Lundquist G., Sjögren B., Sara V. R. Isolation and characterization of variant IGF-1 as well as IGF-2 from adult human brain. FEBS Lett. 1986 May 26;201(1):46–50. doi: 10.1016/0014-5793(86)80568-3. [DOI] [PubMed] [Google Scholar]
  9. Chirgwin J. M., Przybyla A. E., MacDonald R. J., Rutter W. J. Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry. 1979 Nov 27;18(24):5294–5299. doi: 10.1021/bi00591a005. [DOI] [PubMed] [Google Scholar]
  10. Dermietzel R. Junctions in the central nervous system of the cat. V. The junctional complex of the pia-arachnoid membrane. Cell Tissue Res. 1975 Dec 10;164(3):309–329. doi: 10.1007/BF00223012. [DOI] [PubMed] [Google Scholar]
  11. Dickson P. W., Aldred A. R., Marley P. D., Bannister D., Schreiber G. Rat choroid plexus specializes in the synthesis and the secretion of transthyretin (prealbumin). Regulation of transthyretin synthesis in choroid plexus is independent from that in liver. J Biol Chem. 1986 Mar 15;261(8):3475–3478. [PubMed] [Google Scholar]
  12. Dickson P. W., Aldred A. R., Marley P. D., Tu G. F., Howlett G. J., Schreiber G. High prealbumin and transferrin mRNA levels in the choroid plexus of rat brain. Biochem Biophys Res Commun. 1985 Mar 29;127(3):890–895. doi: 10.1016/s0006-291x(85)80027-9. [DOI] [PubMed] [Google Scholar]
  13. Enberg G., Tham A., Sara V. R. The influence of purified somatomedins and insulin on foetal rat brain DNA synthesis in vitro. Acta Physiol Scand. 1985 Oct;125(2):305–308. doi: 10.1111/j.1748-1716.1985.tb07720.x. [DOI] [PubMed] [Google Scholar]
  14. Feinberg A. P., Vogelstein B. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem. 1983 Jul 1;132(1):6–13. doi: 10.1016/0003-2697(83)90418-9. [DOI] [PubMed] [Google Scholar]
  15. Fremeau R. T., Jr, Lundblad J. R., Pritchett D. B., Wilcox J. N., Roberts J. L. Regulation of pro-opiomelanocortin gene transcription in individual cell nuclei. Science. 1986 Dec 5;234(4781):1265–1269. doi: 10.1126/science.3775385. [DOI] [PubMed] [Google Scholar]
  16. Froesch E. R., Schmid C., Schwander J., Zapf J. Actions of insulin-like growth factors. Annu Rev Physiol. 1985;47:443–467. doi: 10.1146/annurev.ph.47.030185.002303. [DOI] [PubMed] [Google Scholar]
  17. Frunzio R., Chiariotti L., Brown A. L., Graham D. E., Rechler M. M., Bruni C. B. Structure and expression of the rat insulin-like growth factor II (rIGF-II) gene. rIGF-II RNAs are transcribed from two promoters. J Biol Chem. 1986 Dec 25;261(36):17138–17149. [PubMed] [Google Scholar]
  18. Gammeltoft S., Haselbacher G. K., Humbel R. E., Fehlmann M., Van Obberghen E. Two types of receptor for insulin-like growth factors in mammalian brain. EMBO J. 1985 Dec 16;4(13A):3407–3412. doi: 10.1002/j.1460-2075.1985.tb04097.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Gee C. E., Roberts J. L. In situ hybridization histochemistry: a technique for the study of gene expression in single cells. DNA. 1983;2(2):157–163. doi: 10.1089/dna.1983.2.157. [DOI] [PubMed] [Google Scholar]
  20. Gil D. R., Ratto G. D. Contribution to the study of the origin of leptomeninges in the human embryo. Acta Anat (Basel) 1973;85(4):620–623. doi: 10.1159/000144099. [DOI] [PubMed] [Google Scholar]
  21. Graham D. E., Rechler M. M., Brown A. L., Frunzio R., Romanus J. A., Bruni C. B., Whitfield H. J., Nissley S. P., Seelig S., Berry S. Coordinate developmental regulation of high and low molecular weight mRNAs for rat insulin-like growth factor II. Proc Natl Acad Sci U S A. 1986 Jun;83(12):4519–4523. doi: 10.1073/pnas.83.12.4519. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Han V. K., D'Ercole A. J., Lund P. K. Cellular localization of somatomedin (insulin-like growth factor) messenger RNA in the human fetus. Science. 1987 Apr 10;236(4798):193–197. doi: 10.1126/science.3563497. [DOI] [PubMed] [Google Scholar]
  23. Haselbacher G. K., Schwab M. E., Pasi A., Humbel R. E. Insulin-like growth factor II (IGF II) in human brain: regional distribution of IGF II and of higher molecular mass forms. Proc Natl Acad Sci U S A. 1985 Apr;82(7):2153–2157. doi: 10.1073/pnas.82.7.2153. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Haselbacher G., Humbel R. Evidence for two species of insulin-like growth factor II (IGF II and "big" IGF II) in human spinal fluid. Endocrinology. 1982 May;110(5):1822–1824. doi: 10.1210/endo-110-5-1822. [DOI] [PubMed] [Google Scholar]
  25. Herbert J., Wilcox J. N., Pham K. T., Fremeau R. T., Jr, Zeviani M., Dwork A., Soprano D. R., Makover A., Goodman D. S., Zimmerman E. A. Transthyretin: a choroid plexus-specific transport protein in human brain. The 1986 S. Weir Mitchell award. Neurology. 1986 Jul;36(7):900–911. doi: 10.1212/wnl.36.7.900. [DOI] [PubMed] [Google Scholar]
  26. Hossenlopp P., Seurin D., Segovia-Quinson B., Binoux M. Identification of an insulin-like growth factor-binding protein in human cerebrospinal fluid with a selective affinity for IGF-II. FEBS Lett. 1986 Nov 24;208(2):439–444. doi: 10.1016/0014-5793(86)81065-1. [DOI] [PubMed] [Google Scholar]
  27. Hu N., Messing J. The making of strand-specific M13 probes. Gene. 1982 Mar;17(3):271–277. doi: 10.1016/0378-1119(82)90143-3. [DOI] [PubMed] [Google Scholar]
  28. Kato M., Soprano D. R., Makover A., Kato K., Herbert J., Goodman D. S. Localization of immunoreactive transthyretin (prealbumin) and of transthyretin mRNA in fetal and adult rat brain. Differentiation. 1986;31(3):228–235. doi: 10.1111/j.1432-0436.1986.tb00402.x. [DOI] [PubMed] [Google Scholar]
  29. Keep R. F., Jones H. C., Cawkwell R. D. A morphometric analysis of the development of the fourth ventricle choroid plexus in the rat. Brain Res. 1986 Jun;392(1-2):77–85. doi: 10.1016/0165-3806(86)90234-8. [DOI] [PubMed] [Google Scholar]
  30. Krisch B., Leonhardt H., Oksche A. The meningeal compartments of the median eminence and the cortex. A comparative analysis in the rat. Cell Tissue Res. 1983;228(3):597–640. doi: 10.1007/BF00211479. [DOI] [PubMed] [Google Scholar]
  31. Lim R., Miller J. F., Hicklin D. J., Holm A. C., Ginsberg B. H. Mitogenic activity of glia maturation factor. Interaction with insulin and insulin-like growth factor-II. Exp Cell Res. 1985 Aug;159(2):335–343. doi: 10.1016/s0014-4827(85)80007-0. [DOI] [PubMed] [Google Scholar]
  32. Lund P. K., Moats-Staats B. M., Hynes M. A., Simmons J. G., Jansen M., D'Ercole A. J., Van Wyk J. J. Somatomedin-C/insulin-like growth factor-I and insulin-like growth factor-II mRNAs in rat fetal and adult tissues. J Biol Chem. 1986 Nov 5;261(31):14539–14544. [PubMed] [Google Scholar]
  33. Mattsson M. E., Enberg G., Ruusala A. I., Hall K., Påhlman S. Mitogenic response of human SH-SY5Y neuroblastoma cells to insulin-like growth factor I and II is dependent on the stage of differentiation. J Cell Biol. 1986 May;102(5):1949–1954. doi: 10.1083/jcb.102.5.1949. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. McLone D. G., Bondareff W. Developmental morphology of the subarachnoid space and contiguous structures in the mouse. Am J Anat. 1975 Mar;142(3):273–293. doi: 10.1002/aja.1001420302. [DOI] [PubMed] [Google Scholar]
  35. Morse D. E., Cova J. L. Pigmented cells in the leptomeninges of the cat. Anat Rec. 1984 Sep;210(1):125–132. doi: 10.1002/ar.1092100115. [DOI] [PubMed] [Google Scholar]
  36. Morse D. E., Low F. N. The fine structure of the pia mater of the rat. Am J Anat. 1972 Mar;133(3):349–367. doi: 10.1002/aja.1001330309. [DOI] [PubMed] [Google Scholar]
  37. Moses A. C., Nissley S. P., Short P. A., Rechler M. M., White R. M., Knight A. B., Higa O. Z. Increased levels of multiplication-stimulating activity, an insulin-like growth factor, in fetal rat serum. Proc Natl Acad Sci U S A. 1980 Jun;77(6):3649–3653. doi: 10.1073/pnas.77.6.3649. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Murphy L. J., Bell G. I., Friesen H. G. Tissue distribution of insulin-like growth factor I and II messenger ribonucleic acid in the adult rat. Endocrinology. 1987 Apr;120(4):1279–1282. doi: 10.1210/endo-120-4-1279. [DOI] [PubMed] [Google Scholar]
  39. PEASE D. C., SCHULTZ R. L. Electron microscopy of rat cranial meninges. Am J Anat. 1958 Mar;102(2):301–321. doi: 10.1002/aja.1001020207. [DOI] [PubMed] [Google Scholar]
  40. Pardridge W. M. Mechanisms of neuropeptide interaction with the blood-brain barrier. Ann N Y Acad Sci. 1986;481:231–249. doi: 10.1111/j.1749-6632.1986.tb27154.x. [DOI] [PubMed] [Google Scholar]
  41. Recio-Pinto E., Ishii D. N. Effects of insulin, insulin-like growth factor-II and nerve growth factor on neurite outgrowth in cultured human neuroblastoma cells. Brain Res. 1984 Jun 8;302(2):323–334. doi: 10.1016/0006-8993(84)90246-4. [DOI] [PubMed] [Google Scholar]
  42. Recio-Pinto E., Rechler M. M., Ishii D. N. Effects of insulin, insulin-like growth factor-II, and nerve growth factor on neurite formation and survival in cultured sympathetic and sensory neurons. J Neurosci. 1986 May;6(5):1211–1219. doi: 10.1523/JNEUROSCI.06-05-01211.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Rutka J. T., Giblin J., Dougherty D. V., McCulloch J. R., DeArmond S. J., Rosenblum M. L. An ultrastructural and immunocytochemical analysis of leptomeningeal and meningioma cultures. J Neuropathol Exp Neurol. 1986 May;45(3):285–303. doi: 10.1097/00005072-198605000-00012. [DOI] [PubMed] [Google Scholar]
  44. Schachenmayr W., Friede R. L. The origin of subdural neomembranes. I. Fine structure of the dura-arachnoid interface in man. Am J Pathol. 1978 Jul;92(1):53–68. [PMC free article] [PubMed] [Google Scholar]
  45. Schwechheimer K., Kartenbeck J., Moll R., Franke W. W. Vimentin filament-desmosome cytoskeleton of diverse types of human meningiomas. A distinctive diagnostic feature. Lab Invest. 1984 Nov;51(5):584–591. [PubMed] [Google Scholar]
  46. Soares M. B., Turken A., Ishii D., Mills L., Episkopou V., Cotter S., Zeitlin S., Efstratiadis A. Rat insulin-like growth factor II gene. A single gene with two promoters expressing a multitranscript family. J Mol Biol. 1986 Dec 20;192(4):737–752. doi: 10.1016/0022-2836(86)90025-2. [DOI] [PubMed] [Google Scholar]
  47. Tennyson V. M., Appas G. D. The fine structure of the choroid plexus adult and developmental stages. Prog Brain Res. 1968;29:63–85. doi: 10.1016/s0079-6123(08)64149-7. [DOI] [PubMed] [Google Scholar]
  48. Waggener J. D., Beggs J. The membranous coverings of neural tissues: an electron microscopy study. J Neuropathol Exp Neurol. 1967 Jul;26(3):412–426. doi: 10.1097/00005072-196707000-00005. [DOI] [PubMed] [Google Scholar]
  49. Wuenschell C. W., Fisher R. S., Kaufman D. L., Tobin A. J. In situ hybridization to localize mRNA encoding the neurotransmitter synthetic enzyme glutamate decarboxylase in mouse cerebellum. Proc Natl Acad Sci U S A. 1986 Aug;83(16):6193–6197. doi: 10.1073/pnas.83.16.6193. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Zapf J., Froesch E. R. Insulin-like growth factors/somatomedins: structure, secretion, biological actions and physiological role. Horm Res. 1986;24(2-3):121–130. doi: 10.1159/000180551. [DOI] [PubMed] [Google Scholar]
  51. Zeitlin S., Efstratiadis A. In vivo splicing products of the rabbit beta-globin pre-mRNA. Cell. 1984 Dec;39(3 Pt 2):589–602. doi: 10.1016/0092-8674(84)90466-5. [DOI] [PubMed] [Google Scholar]
  52. de Pagter-Holthuizen P., Jansen M., van Schaik F. M., van der Kammen R., Oosterwijk C., Van den Brande J. L., Sussenbach J. S. The human insulin-like growth factor II gene contains two development-specific promoters. FEBS Lett. 1987 Apr 20;214(2):259–264. doi: 10.1016/0014-5793(87)80066-2. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES