Abstract
Neuroblastoma is an embryonal tumor that typically arises in cells of the developing adrenal medulla. IGF-II mRNA is expressed at high levels in the adrenal cortex before birth but it is not detectable until after birth in the adrenal medulla. Neuroblastoma cell lines corresponding to early adrenal medullary precursors did not express IGF-II, although all three cell lines we tested were growth stimulated by IGF-II. Cell lines corresponding to more mature adrenal medullary cells expressed IGF-II, and one, SK-N-AS, grows by an IGF-II autocrine mechanism (J. Clin. Invest. 84:829-839) El-Badry, Romanus, Helman, Cooper, Rechler, and Israel. 1989. An examination of human neuroblastoma tumor tissues for IGF-II gene expression using in situ hybridization histochemistry revealed that IGF-II is expressed by tumor cells in only 5 of 21 neuroblastomas, but is detectable in cells of nonmalignant tissues including adrenal cortical cells, stromal fibroblasts, and eosinophils in all 21 tumors. These findings indicate that IGF-II may function as an autocrine growth factor for some neuroblastomas and as a paracrine growth factor for others. They suggest that the growth regulatory pathways utilized by neuroblastoma mimic those used in the precursor cell type from which individual tumors arise.
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Selected References
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- Brice A. L., Cheetham J. E., Bolton V. N., Hill N. C., Schofield P. N. Temporal changes in the expression of the insulin-like growth factor II gene associated with tissue maturation in the human fetus. Development. 1989 Jul;106(3):543–554. doi: 10.1242/dev.106.3.543. [DOI] [PubMed] [Google Scholar]
- 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]
- Cariani E., Lasserre C., Seurin D., Hamelin B., Kemeny F., Franco D., Czech M. P., Ullrich A., Brechot C. Differential expression of insulin-like growth factor II mRNA in human primary liver cancers, benign liver tumors, and liver cirrhosis. Cancer Res. 1988 Dec 1;48(23):6844–6849. [PubMed] [Google Scholar]
- 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]
- Cohen P. S., Seeger R. C., Triche T. J., Israel M. A. Detection of N-myc gene expression in neuroblastoma tumors by in situ hybridization. Am J Pathol. 1988 Jun;131(3):391–397. [PMC free article] [PubMed] [Google Scholar]
- Conover C. A., Rosenfeld R. G., Hintz R. L. Insulin-like growth factor II binding and action in human fetal fibroblasts. J Cell Physiol. 1987 Dec;133(3):560–566. doi: 10.1002/jcp.1041330318. [DOI] [PubMed] [Google Scholar]
- Cooper M. J., Hutchins G. M., Cohen P. S., Helman L. J., Mennie R. J., Israel M. A. Human neuroblastoma tumor cell lines correspond to the arrested differentiation of chromaffin adrenal medullary neuroblasts. Cell Growth Differ. 1990 Apr;1(4):149–159. [PubMed] [Google Scholar]
- El-Badry O. M., Minniti C., Kohn E. C., Houghton P. J., Daughaday W. H., Helman L. J. Insulin-like growth factor II acts as an autocrine growth and motility factor in human rhabdomyosarcoma tumors. Cell Growth Differ. 1990 Jul;1(7):325–331. [PubMed] [Google Scholar]
- El-Badry O. M., Romanus J. A., Helman L. J., Cooper M. J., Rechler M. M., Israel M. A. Autonomous growth of a human neuroblastoma cell line is mediated by insulin-like growth factor II. J Clin Invest. 1989 Sep;84(3):829–839. doi: 10.1172/JCI114243. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Evans A. E., Gerson J., Schnaufer L. Spontaneous regression of neuroblastoma. Natl Cancer Inst Monogr. 1976 Nov;44:49–54. [PubMed] [Google Scholar]
- Flier J. S., Usher P., Moses A. C. Monoclonal antibody to the type I insulin-like growth factor (IGF-I) receptor blocks IGF-I receptor-mediated DNA synthesis: clarification of the mitogenic mechanisms of IGF-I and insulin in human skin fibroblasts. Proc Natl Acad Sci U S A. 1986 Feb;83(3):664–668. doi: 10.1073/pnas.83.3.664. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Frolik C. A., Ellis L. F., Williams D. C. Isolation and characterization of insulin-like growth factor-II from human bone. Biochem Biophys Res Commun. 1988 Mar 30;151(3):1011–1018. doi: 10.1016/s0006-291x(88)80466-2. [DOI] [PubMed] [Google Scholar]
- Furlanetto R. W., DiCarlo J. N., Wisehart C. The type II insulin-like growth factor receptor does not mediate deoxyribonucleic acid synthesis in human fibroblasts. J Clin Endocrinol Metab. 1987 Jun;64(6):1142–1149. doi: 10.1210/jcem-64-6-1142. [DOI] [PubMed] [Google Scholar]
- Furlanetto R. W., Underwood L. E., Van Wyk J. J., D'Ercole A. J. Estimation of somatomedin-C levels in normals and patients with pituitary disease by radioimmunoassay. J Clin Invest. 1977 Sep;60(3):648–657. doi: 10.1172/JCI108816. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gray A., Tam A. W., Dull T. J., Hayflick J., Pintar J., Cavenee W. K., Koufos A., Ullrich A. Tissue-specific and developmentally regulated transcription of the insulin-like growth factor 2 gene. DNA. 1987 Aug;6(4):283–295. doi: 10.1089/dna.1987.6.283. [DOI] [PubMed] [Google Scholar]
- 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]
- Han V. K., Lund P. K., Lee D. C., D'Ercole A. J. Expression of somatomedin/insulin-like growth factor messenger ribonucleic acids in the human fetus: identification, characterization, and tissue distribution. J Clin Endocrinol Metab. 1988 Feb;66(2):422–429. doi: 10.1210/jcem-66-2-422. [DOI] [PubMed] [Google Scholar]
- Haselbacher G. K., Irminger J. C., Zapf J., Ziegler W. H., Humbel R. E. Insulin-like growth factor II in human adrenal pheochromocytomas and Wilms tumors: expression at the mRNA and protein level. Proc Natl Acad Sci U S A. 1987 Feb;84(4):1104–1106. doi: 10.1073/pnas.84.4.1104. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Höppener J. W., Mosselman S., Roholl P. J., Lambrechts C., Slebos R. J., de Pagter-Holthuizen P., Lips C. J., Jansz H. S., Sussenbach J. S. Expression of insulin-like growth factor-I and -II genes in human smooth muscle tumours. EMBO J. 1988 May;7(5):1379–1385. doi: 10.1002/j.1460-2075.1988.tb02954.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Israel M. A. The evolution of clinical molecular genetics. Neuroblastoma as a model tumor. Am J Pediatr Hematol Oncol. 1986 Summer;8(2):163–172. [PubMed] [Google Scholar]
- Levinovitz A., Norstedt G. Developmental and steroid hormonal regulation of insulin-like growth factor II expression. Mol Endocrinol. 1989 May;3(5):797–804. doi: 10.1210/mend-3-5-797. [DOI] [PubMed] [Google Scholar]
- Mohan S., Jennings J. C., Linkhart T. A., Baylink D. J. Primary structure of human skeletal growth factor: homology with human insulin-like growth factor-II. Biochim Biophys Acta. 1988 Jul 14;966(1):44–55. doi: 10.1016/0304-4165(88)90127-4. [DOI] [PubMed] [Google Scholar]
- Morgan D. O., Edman J. C., Standring D. N., Fried V. A., Smith M. C., Roth R. A., Rutter W. J. Insulin-like growth factor II receptor as a multifunctional binding protein. Nature. 1987 Sep 24;329(6137):301–307. doi: 10.1038/329301a0. [DOI] [PubMed] [Google Scholar]
- Ota A., Wilson G. L., Leroith D. Insulin-like growth factor I receptors on mouse neuroblastoma cells. Two beta subunits are derived from differences in glycosylation. Eur J Biochem. 1988 Jun 15;174(3):521–530. doi: 10.1111/j.1432-1033.1988.tb14130.x. [DOI] [PubMed] [Google Scholar]
- Ota A., Wilson G. L., Spilberg O., Pruss R., LeRoith D. Functional insulin-like growth factor I receptors are expressed by neural-derived continuous cell lines. Endocrinology. 1988 Jan;122(1):145–152. doi: 10.1210/endo-122-1-145. [DOI] [PubMed] [Google Scholar]
- Pillion D. J., Yang M., Grizzle W. E. Distribution of receptors for insulin and insulin-like growth factor I (somatomedin C) in the adrenal gland. Biochem Biophys Res Commun. 1988 Jul 15;154(1):138–145. doi: 10.1016/0006-291x(88)90661-4. [DOI] [PubMed] [Google Scholar]
- Recio-Pinto E., Ishii D. N. Insulin and insulinlike growth factor receptors regulating neurite formation in cultured human neuroblastoma cells. J Neurosci Res. 1988 Mar;19(3):312–320. doi: 10.1002/jnr.490190306. [DOI] [PubMed] [Google Scholar]
- Reeve A. E., Eccles M. R., Wilkins R. J., Bell G. I., Millow L. J. Expression of insulin-like growth factor-II transcripts in Wilms' tumour. Nature. 1985 Sep 19;317(6034):258–260. doi: 10.1038/317258a0. [DOI] [PubMed] [Google Scholar]
- Roth R. A. Structure of the receptor for insulin-like growth factor II: the puzzle amplified. Science. 1988 Mar 11;239(4845):1269–1271. doi: 10.1126/science.2964085. [DOI] [PubMed] [Google Scholar]
- Sandberg A. C., Engberg C., Lake M., von Holst H., Sara V. R. The expression of insulin-like growth factor I and insulin-like growth factor II genes in the human fetal and adult brain and in glioma. Neurosci Lett. 1988 Oct 31;93(1):114–119. doi: 10.1016/0304-3940(88)90022-5. [DOI] [PubMed] [Google Scholar]
- Sara V. R., Hall K., Misaki M., Fryklund L., Christensen N., Wetterberg L. Ontogenesis of somatomedin and insulin receptors in the human fetus. J Clin Invest. 1983 May;71(5):1084–1094. doi: 10.1172/JCI110858. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schoenle E., Zapf J., Humbel R. E., Froesch E. R. Insulin-like growth factor I stimulates growth in hypophysectomized rats. Nature. 1982 Mar 18;296(5854):252–253. doi: 10.1038/296252a0. [DOI] [PubMed] [Google Scholar]
- Scott J., Cowell J., Robertson M. E., Priestley L. M., Wadey R., Hopkins B., Pritchard J., Bell G. I., Rall L. B., Graham C. F. Insulin-like growth factor-II gene expression in Wilms' tumour and embryonic tissues. Nature. 1985 Sep 19;317(6034):260–262. doi: 10.1038/317260a0. [DOI] [PubMed] [Google Scholar]
- Shigematsu K., Niwa M., Kurihara M., Yamashita K., Kawai K., Tsuchiyama H. Receptor autoradiographic localization of insulin-like growth factor-I (IGF-I) binding sites in human fetal and adult adrenal glands. Life Sci. 1989;45(5):383–389. doi: 10.1016/0024-3205(89)90624-3. [DOI] [PubMed] [Google Scholar]
- Stracke M. L., Engel J. D., Wilson L. W., Rechler M. M., Liotta L. A., Schiffmann E. The type I insulin-like growth factor receptor is a motility receptor in human melanoma cells. J Biol Chem. 1989 Dec 25;264(36):21544–21549. [PubMed] [Google Scholar]
- Sturm M. A., Conover C. A., Pham H., Rosenfeld R. G. Insulin-like growth factor receptors and binding protein in rat neuroblastoma cells. Endocrinology. 1989 Jan;124(1):388–396. doi: 10.1210/endo-124-1-388. [DOI] [PubMed] [Google Scholar]
- Thiele C. J., McKeon C., Triche T. J., Ross R. A., Reynolds C. P., Israel M. A. Differential protooncogene expression characterizes histopathologically indistinguishable tumors of the peripheral nervous system. J Clin Invest. 1987 Sep;80(3):804–811. doi: 10.1172/JCI113137. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tricoli J. V., Rall L. B., Karakousis C. P., Herrera L., Petrelli N. J., Bell G. I., Shows T. B. Enhanced levels of insulin-like growth factor messenger RNA in human colon carcinomas and liposarcomas. Cancer Res. 1986 Dec;46(12 Pt 1):6169–6173. [PubMed] [Google Scholar]
- Ullrich A., Gray A., Tam A. W., Yang-Feng T., Tsubokawa M., Collins C., Henzel W., Le Bon T., Kathuria S., Chen E. 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):2503–2512. doi: 10.1002/j.1460-2075.1986.tb04528.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Van Wyk J. J., Graves D. C., Casella S. J., Jacobs S. Evidence from monoclonal antibody studies that insulin stimulates deoxyribonucleic acid synthesis through the type I somatomedin receptor. J Clin Endocrinol Metab. 1985 Oct;61(4):639–643. doi: 10.1210/jcem-61-4-639. [DOI] [PubMed] [Google Scholar]
- Voutilainen R., Miller W. L. Developmental and hormonal regulation of mRNAs for insulin-like growth factor II and steroidogenic enzymes in human fetal adrenals and gonads. DNA. 1988 Jan-Feb;7(1):9–15. doi: 10.1089/dna.1988.7.9. [DOI] [PubMed] [Google Scholar]
- Yee D., Cullen K. J., Paik S., Perdue J. F., Hampton B., Schwartz A., Lippman M. E., Rosen N. Insulin-like growth factor II mRNA expression in human breast cancer. Cancer Res. 1988 Dec 1;48(23):6691–6696. [PubMed] [Google Scholar]
- Yee D., Paik S., Lebovic G. S., Marcus R. R., Favoni R. E., Cullen K. J., Lippman M. E., Rosen N. Analysis of insulin-like growth factor I gene expression in malignancy: evidence for a paracrine role in human breast cancer. Mol Endocrinol. 1989 Mar;3(3):509–517. doi: 10.1210/mend-3-3-509. [DOI] [PubMed] [Google Scholar]
- van Dijk J. P., Tanswell A. K., Challis J. R. Insulin-like growth factor (IGF)-II and insulin, but not IGF-I, are mitogenic for fetal rat adrenal cells in vitro. J Endocrinol. 1988 Dec;119(3):509–516. doi: 10.1677/joe.0.1190509. [DOI] [PubMed] [Google Scholar]