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. 1989 Sep 1;109(3):1351–1362. doi: 10.1083/jcb.109.3.1351

In situ hybridization reveals temporal and spatial changes in cellular expression of mRNA for a laminin receptor, laminin, and basement membrane (type IV) collagen in the developing kidney

PMCID: PMC2115755  PMID: 2527859

Abstract

The appearance of extracellular matrix molecules and their receptors represent key events in the differentiation of cells of the kidney. Steady-state mRNA levels for a laminin receptor, the laminin B1, B2, and A chains, and the alpha 1-chain of collagen IV (alpha 1[IV]), were examined in mouse kidneys at 16 d gestation and birth, when cell differentiation is active, and 1-3 wk after birth when this activity has subsided. Northern analysis revealed that mRNA expression of laminin receptor precedes the alpha 1(IV) and laminin B chains whereas laminin A chain mRNA expression was very low. In situ hybridization reflected this pattern and revealed the cells responsible for expression. At 16 d gestation, laminin receptor mRNA was elevated in cells of newly forming glomeruli and proximal and distal tubules of the nephrogenic zone located in the kidney cortex. These cells also expressed mRNA for alpha 1(IV) and laminin chains. At birth, mRNA expression of receptor and all chains remained high in glomeruli but was reduced in proximal and distal tubules. At 1 wk after birth, expression was located in the medulla over collecting ducts and loops of Henle. Little expression was detectable by 3 wk. These results suggest that cellular expression of steady-state mRNA for laminin receptor, laminin, and collagen IV is temporally linked, with laminin receptor expression proceeding first and thereafter subsiding.

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Selected References

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  1. Abrahamson D. R. Recent studies on the structure and pathology of basement membranes. J Pathol. 1986 Aug;149(4):257–278. doi: 10.1002/path.1711490402. [DOI] [PubMed] [Google Scholar]
  2. Angerer L. M., Angerer R. C. Detection of poly A+ RNA in sea urchin eggs and embryos by quantitative in situ hybridization. Nucleic Acids Res. 1981 Jun 25;9(12):2819–2840. doi: 10.1093/nar/9.12.2819. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Aufderheide E., Chiquet-Ehrismann R., Ekblom P. Epithelial-mesenchymal interactions in the developing kidney lead to expression of tenascin in the mesenchyme. J Cell Biol. 1987 Jul;105(1):599–608. doi: 10.1083/jcb.105.1.599. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Berger C. N. In situ hybridization of immunoglobulin-specific RNA in single cells of the B lymphocyte lineage with radiolabelled DNA probes. EMBO J. 1986 Jan;5(1):85–93. doi: 10.1002/j.1460-2075.1986.tb04181.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Boot-Handford R. P., Kurkinen M., Prockop D. J. Steady-state levels of mRNAs coding for the type IV collagen and laminin polypeptide chains of basement membranes exhibit marked tissue-specific stoichiometric variations in the rat. J Biol Chem. 1987 Sep 15;262(26):12475–12478. [PubMed] [Google Scholar]
  6. Carlin B., Jaffe R., Bender B., Chung A. E. Entactin, a novel basal lamina-associated sulfated glycoprotein. J Biol Chem. 1981 May 25;256(10):5209–5214. [PubMed] [Google Scholar]
  7. Chan Y. L., Olvera J., Wool I. G. The structure of rat 28S ribosomal ribonucleic acid inferred from the sequence of nucleotides in a gene. Nucleic Acids Res. 1983 Nov 25;11(22):7819–7831. doi: 10.1093/nar/11.22.7819. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Charonis A. S., Tsilibary E. C., Yurchenco P. D., Furthmayr H. Binding of laminin to type IV collagen: a morphological study. J Cell Biol. 1985 Jun;100(6):1848–1853. doi: 10.1083/jcb.100.6.1848. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Cooper A. R., Kurkinen M., Taylor A., Hogan B. L. Studies on the biosynthesis of laminin by murine parietal endoderm cells. Eur J Biochem. 1981 Sep;119(1):189–197. doi: 10.1111/j.1432-1033.1981.tb05593.x. [DOI] [PubMed] [Google Scholar]
  10. Doege K., Sasaki M., Horigan E., Hassell J. R., Yamada Y. Complete primary structure of the rat cartilage proteoglycan core protein deduced from cDNA clones. J Biol Chem. 1987 Dec 25;262(36):17757–17767. [PubMed] [Google Scholar]
  11. Ebihara I., Killen P. D., Laurie G. W., Huang T., Yamada Y., Martin G. R., Brown K. S. Altered mRNA expression of basement membrane components in a murine model of polycystic kidney disease. Lab Invest. 1988 Mar;58(3):262–269. [PubMed] [Google Scholar]
  12. Ekblom P. Formation of basement membranes in the embryonic kidney: an immunohistological study. J Cell Biol. 1981 Oct;91(1):1–10. doi: 10.1083/jcb.91.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Engel J., Odermatt E., Engel A., Madri J. A., Furthmayr H., Rohde H., Timpl R. Shapes, domain organizations and flexibility of laminin and fibronectin, two multifunctional proteins of the extracellular matrix. J Mol Biol. 1981 Jul 25;150(1):97–120. doi: 10.1016/0022-2836(81)90326-0. [DOI] [PubMed] [Google Scholar]
  14. Gehlsen K. R., Dillner L., Engvall E., Ruoslahti E. The human laminin receptor is a member of the integrin family of cell adhesion receptors. Science. 1988 Sep 2;241(4870):1228–1229. doi: 10.1126/science.2970671. [DOI] [PubMed] [Google Scholar]
  15. Hafen E., Levine M., Garber R. L., Gehring W. J. An improved in situ hybridization method for the detection of cellular RNAs in Drosophila tissue sections and its application for localizing transcripts of the homeotic Antennapedia gene complex. EMBO J. 1983;2(4):617–623. doi: 10.1002/j.1460-2075.1983.tb01472.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Han J. H., Stratowa C., Rutter W. J. Isolation of full-length putative rat lysophospholipase cDNA using improved methods for mRNA isolation and cDNA cloning. Biochemistry. 1987 Mar 24;26(6):1617–1625. doi: 10.1021/bi00380a020. [DOI] [PubMed] [Google Scholar]
  17. Hand P. H., Thor A., Schlom J., Rao C. N., Liotta L. Expression of laminin receptor in normal and carcinomatous human tissues as defined by a monoclonal antibody. Cancer Res. 1985 Jun;45(6):2713–2719. [PubMed] [Google Scholar]
  18. Harper M. E., Marselle L. M., Gallo R. C., Wong-Staal F. Detection of lymphocytes expressing human T-lymphotropic virus type III in lymph nodes and peripheral blood from infected individuals by in situ hybridization. Proc Natl Acad Sci U S A. 1986 Feb;83(3):772–776. doi: 10.1073/pnas.83.3.772. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Hayashi M., Ninomiya Y., Parsons J., Hayashi K., Olsen B. R., Trelstad R. L. Differential localization of mRNAs of collagen types I and II in chick fibroblasts, chondrocytes, and corneal cells by in situ hybridization using cDNA probes. J Cell Biol. 1986 Jun;102(6):2302–2309. doi: 10.1083/jcb.102.6.2302. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Hayashi S., Gillam I. C., Delaney A. D., Tener G. M. Acetylation of chromosome squashes of Drosophila melanogaster decreases the background in autoradiographs from hybridization with [125I]-labeled RNA. J Histochem Cytochem. 1978 Aug;26(8):677–679. doi: 10.1177/26.8.99471. [DOI] [PubMed] [Google Scholar]
  21. Klein G., Langegger M., Timpl R., Ekblom P. Role of laminin A chain in the development of epithelial cell polarity. Cell. 1988 Oct 21;55(2):331–341. doi: 10.1016/0092-8674(88)90056-6. [DOI] [PubMed] [Google Scholar]
  22. Kleinman H. K., Ebihara I., Killen P. D., Sasaki M., Cannon F. B., Yamada Y., Martin G. R. Genes for basement membrane proteins are coordinately expressed in differentiating F9 cells but not in normal adult murine tissues. Dev Biol. 1987 Aug;122(2):373–378. doi: 10.1016/0012-1606(87)90302-2. [DOI] [PubMed] [Google Scholar]
  23. Kleinman H. K., Graf J., Iwamoto Y., Kitten G. T., Ogle R. C., Sasaki M., Yamada Y., Martin G. R., Luckenbill-Edds L. Role of basement membranes in cell differentiation. Ann N Y Acad Sci. 1987;513:134–145. doi: 10.1111/j.1749-6632.1987.tb25004.x. [DOI] [PubMed] [Google Scholar]
  24. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  25. Laurie G. W., Bing J. T., Kleinman H. K., Hassell J. R., Aumailley M., Martin G. R., Feldmann R. J. Localization of binding sites for laminin, heparan sulfate proteoglycan and fibronectin on basement membrane (type IV) collagen. J Mol Biol. 1986 May 5;189(1):205–216. doi: 10.1016/0022-2836(86)90391-8. [DOI] [PubMed] [Google Scholar]
  26. Laurie G. W., Inoue S., Bing J. T., Hassell J. R. Visualization of the large heparan sulfate proteoglycan from basement membrane. Am J Anat. 1988 Mar;181(3):320–326. doi: 10.1002/aja.1001810308. [DOI] [PubMed] [Google Scholar]
  27. Lawrence J. B., Singer R. H. Quantitative analysis of in situ hybridization methods for the detection of actin gene expression. Nucleic Acids Res. 1985 Mar 11;13(5):1777–1799. doi: 10.1093/nar/13.5.1777. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Ledbetter S. R., Tyree B., Hassell J. R., Horigan E. A. Identification of the precursor protein to basement membrane heparan sulfate proteoglycans. J Biol Chem. 1985 Jul 5;260(13):8106–8113. [PubMed] [Google Scholar]
  29. Lesot H., Kühl U., Mark K. Isolation of a laminin-binding protein from muscle cell membranes. EMBO J. 1983;2(6):861–865. doi: 10.1002/j.1460-2075.1983.tb01514.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Malinoff H. L., Wicha M. S. Isolation of a cell surface receptor protein for laminin from murine fibrosarcoma cells. J Cell Biol. 1983 May;96(5):1475–1479. doi: 10.1083/jcb.96.5.1475. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Melton D. A., Krieg P. A., Rebagliati M. R., Maniatis T., Zinn K., Green M. R. Efficient in vitro synthesis of biologically active RNA and RNA hybridization probes from plasmids containing a bacteriophage SP6 promoter. Nucleic Acids Res. 1984 Sep 25;12(18):7035–7056. doi: 10.1093/nar/12.18.7035. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Nomura S., Wills A. J., Edwards D. R., Heath J. K., Hogan B. L. Developmental expression of 2ar (osteopontin) and SPARC (osteonectin) RNA as revealed by in situ hybridization. J Cell Biol. 1988 Feb;106(2):441–450. doi: 10.1083/jcb.106.2.441. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Oberbäumer I., Laurent M., Schwarz U., Sakurai Y., Yamada Y., Vogeli G., Voss T., Siebold B., Glanville R. W., Kühn K. Amino acid sequence of the non-collagenous globular domain (NC1) of the alpha 1(IV) chain of basement membrane collagen as derived from complementary DNA. Eur J Biochem. 1985 Mar 1;147(2):217–224. doi: 10.1111/j.1432-1033.1985.tb08739.x. [DOI] [PubMed] [Google Scholar]
  34. Paulsson M., Yurchenco P. D., Ruben G. C., Engel J., Timpl R. Structure of low density heparan sulfate proteoglycan isolated from a mouse tumor basement membrane. J Mol Biol. 1987 Sep 20;197(2):297–313. doi: 10.1016/0022-2836(87)90125-2. [DOI] [PubMed] [Google Scholar]
  35. Rao N. C., Barsky S. H., Terranova V. P., Liotta L. A. Isolation of a tumor cell laminin receptor. Biochem Biophys Res Commun. 1983 Mar 29;111(3):804–808. doi: 10.1016/0006-291x(83)91370-0. [DOI] [PubMed] [Google Scholar]
  36. Rhodes C., Doege K., Sasaki M., Yamada Y. Alternative splicing generates two different mRNA species for rat link protein. J Biol Chem. 1988 May 5;263(13):6063–6067. [PubMed] [Google Scholar]
  37. Sariola H., Aufderheide E., Bernhard H., Henke-Fahle S., Dippold W., Ekblom P. Antibodies to cell surface ganglioside GD3 perturb inductive epithelial-mesenchymal interactions. Cell. 1988 Jul 15;54(2):235–245. doi: 10.1016/0092-8674(88)90556-9. [DOI] [PubMed] [Google Scholar]
  38. Sasaki M., Kato S., Kohno K., Martin G. R., Yamada Y. Sequence of the cDNA encoding the laminin B1 chain reveals a multidomain protein containing cysteine-rich repeats. Proc Natl Acad Sci U S A. 1987 Feb;84(4):935–939. doi: 10.1073/pnas.84.4.935. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Sasaki M., Kleinman H. K., Huber H., Deutzmann R., Yamada Y. Laminin, a multidomain protein. The A chain has a unique globular domain and homology with the basement membrane proteoglycan and the laminin B chains. J Biol Chem. 1988 Nov 15;263(32):16536–16544. [PubMed] [Google Scholar]
  40. Sasaki M., Yamada Y. The laminin B2 chain has a multidomain structure homologous to the B1 chain. J Biol Chem. 1987 Dec 15;262(35):17111–17117. [PubMed] [Google Scholar]
  41. Strickland S., Smith K. K., Marotti K. R. Hormonal induction of differentiation in teratocarcinoma stem cells: generation of parietal endoderm by retinoic acid and dibutyryl cAMP. Cell. 1980 Sep;21(2):347–355. doi: 10.1016/0092-8674(80)90471-7. [DOI] [PubMed] [Google Scholar]
  42. Sugrue S. The interaction of extracellular matrix with the basal cell surface of embryonic corneal epithelia. Prog Clin Biol Res. 1984;151:77–87. [PubMed] [Google Scholar]
  43. Taub M., Sato G. Growth of functional primary cultures of kidney epithelial cells in defined medium. J Cell Physiol. 1980 Nov;105(2):369–378. doi: 10.1002/jcp.1041050220. [DOI] [PubMed] [Google Scholar]
  44. Timpl R., Dziadek M. Structure, development, and molecular pathology of basement membranes. Int Rev Exp Pathol. 1986;29:1–112. [PubMed] [Google Scholar]
  45. Vestweber D., Kemler R., Ekblom P. Cell-adhesion molecule uvomorulin during kidney development. Dev Biol. 1985 Nov;112(1):213–221. doi: 10.1016/0012-1606(85)90135-6. [DOI] [PubMed] [Google Scholar]
  46. Wewer U. M., Liotta L. A., Jaye M., Ricca G. A., Drohan W. N., Claysmith A. P., Rao C. N., Wirth P., Coligan J. E., Albrechtsen R. Altered levels of laminin receptor mRNA in various human carcinoma cells that have different abilities to bind laminin. Proc Natl Acad Sci U S A. 1986 Oct;83(19):7137–7141. doi: 10.1073/pnas.83.19.7137. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Wewer U. M., Taraboletti G., Sobel M. E., Albrechtsen R., Liotta L. A. Role of laminin receptor in tumor cell migration. Cancer Res. 1987 Nov 1;47(21):5691–5698. [PubMed] [Google Scholar]
  48. Yannariello-Brown J., Wewer U., Liotta L., Madri J. A. Distribution of a 69-kD laminin-binding protein in aortic and microvascular endothelial cells: modulation during cell attachment, spreading, and migration. J Cell Biol. 1988 May;106(5):1773–1786. doi: 10.1083/jcb.106.5.1773. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Yow H. K., Wong J. M., Chen H. S., Lee C. G., Davis S., Steele G. D., Jr, Chen L. B. Increased mRNA expression of a laminin-binding protein in human colon carcinoma: complete sequence of a full-length cDNA encoding the protein. Proc Natl Acad Sci U S A. 1988 Sep;85(17):6394–6398. doi: 10.1073/pnas.85.17.6394. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Zamboni L., De Martino C. Embryogenesis of the human renal glomerulus. I. A histologic study. Arch Pathol. 1968 Sep;86(3):279–291. [PubMed] [Google Scholar]

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