Skip to main content
NCBI home page
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1993 Feb 1;120(3):639–645. doi: 10.1083/jcb.120.3.639

Expression of the murine small heat shock proteins hsp 25 and alpha B crystallin in the absence of stress

PMCID: PMC2119529  PMID: 8425893

Abstract

Stress induces the synthesis of several large and small heat shock proteins (hsp's). Two related small hsp's, hsp25 and alpha B crystallin exist in mice. alpha B crystallin is an abundant protein in several tissues even in the absence of stress. Particularly high amounts accumulate in the eye lens. Here we show that hsp25 is likewise constitutively expressed in many normal adult tissues. In the absence of stress the protein is most abundant in the eye lens, heart, stomach, colon, lung, and bladder. The stress-independent expression pattern of the two small hsp's is distinct. In several tissues the amount of hsp25 exceeds that accumulating in NIH 3T3 fibroblasts in response to heat stress. hsp25, like alpha B crystallin, exists in a highly aggregated form in the eye lens. The expression of hsp25 and alpha B crystallin in normal tissues suggests an essential, but distinct function of the two related proteins under standard physiological conditions.

Full Text

The Full Text of this article is available as a PDF (1.1 MB).

Selected References

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

  1. Arrigo A. P., Tanguay R. M. Expression of heat shock proteins during development in Drosophila. Results Probl Cell Differ. 1991;17:106–119. doi: 10.1007/978-3-540-46712-0_8. [DOI] [PubMed] [Google Scholar]
  2. Arrigo A. P. Tumor necrosis factor induces the rapid phosphorylation of the mammalian heat shock protein hsp28. Mol Cell Biol. 1990 Mar;10(3):1276–1280. doi: 10.1128/mcb.10.3.1276-1280.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Atomi Y., Yamada S., Strohman R., Nonomura Y. Alpha B-crystallin in skeletal muscle: purification and localization. J Biochem. 1991 Nov;110(5):812–822. doi: 10.1093/oxfordjournals.jbchem.a123665. [DOI] [PubMed] [Google Scholar]
  4. Berger E. M., Woodward M. P. Small heat shock proteins in Drosophila may confer thermal tolerance. Exp Cell Res. 1983 Sep;147(2):437–442. doi: 10.1016/0014-4827(83)90225-2. [DOI] [PubMed] [Google Scholar]
  5. Bhat S. P., Nagineni C. N. alpha B subunit of lens-specific protein alpha-crystallin is present in other ocular and non-ocular tissues. Biochem Biophys Res Commun. 1989 Jan 16;158(1):319–325. doi: 10.1016/s0006-291x(89)80215-3. [DOI] [PubMed] [Google Scholar]
  6. Blake M. J., Gershon D., Fargnoli J., Holbrook N. J. Discordant expression of heat shock protein mRNAs in tissues of heat-stressed rats. J Biol Chem. 1990 Sep 5;265(25):15275–15279. [PubMed] [Google Scholar]
  7. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987 Apr;162(1):156–159. doi: 10.1006/abio.1987.9999. [DOI] [PubMed] [Google Scholar]
  8. Ciocca D. R., Adams D. J., Edwards D. P., Bjercke R. J., McGuire W. L. Distribution of an estrogen-induced protein with a molecular weight of 24,000 in normal and malignant human tissues and cells. Cancer Res. 1983 Mar;43(3):1204–1210. [PubMed] [Google Scholar]
  9. Corces V., Holmgren R., Freund R., Morimoto R., Meselson M. Four heat shock proteins of Drosophila melanogaster coded within a 12-kilobase region in chromosome subdivision 67B. Proc Natl Acad Sci U S A. 1980 Sep;77(9):5390–5393. doi: 10.1073/pnas.77.9.5390. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Crête P., Landry J. Induction of HSP27 phosphorylation and thermoresistance in Chinese hamster cells by arsenite, cycloheximide, A23187, and EGTA. Radiat Res. 1990 Mar;121(3):320–327. [PubMed] [Google Scholar]
  11. Darbon J. M., Issandou M., Tournier J. F., Bayard F. The respective 27 kDa and 28 kDa protein kinase C substrates in vascular endothelial and MCF-7 cells are most probably heat shock proteins. Biochem Biophys Res Commun. 1990 Apr 30;168(2):527–536. doi: 10.1016/0006-291x(90)92353-2. [DOI] [PubMed] [Google Scholar]
  12. DiDomenico B. J., Bugaisky G. E., Lindquist S. Heat shock and recovery are mediated by different translational mechanisms. Proc Natl Acad Sci U S A. 1982 Oct;79(20):6181–6185. doi: 10.1073/pnas.79.20.6181. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. DiDomenico B. J., Bugaisky G. E., Lindquist S. The heat shock response is self-regulated at both the transcriptional and posttranscriptional levels. Cell. 1982 Dec;31(3 Pt 2):593–603. doi: 10.1016/0092-8674(82)90315-4. [DOI] [PubMed] [Google Scholar]
  14. Dubin R. A., Gopal-Srivastava R., Wawrousek E. F., Piatigorsky J. Expression of the murine alpha B-crystallin gene in lens and skeletal muscle: identification of a muscle-preferred enhancer. Mol Cell Biol. 1991 Sep;11(9):4340–4349. doi: 10.1128/mcb.11.9.4340-4349.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Dubin R. A., Wawrousek E. F., Piatigorsky J. Expression of the murine alpha B-crystallin gene is not restricted to the lens. Mol Cell Biol. 1989 Mar;9(3):1083–1091. doi: 10.1128/mcb.9.3.1083-1091.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Edington B. V., Hightower L. E. Induction of a chicken small heat shock (stress) protein: evidence of multilevel posttranscriptional regulation. Mol Cell Biol. 1990 Sep;10(9):4886–4898. doi: 10.1128/mcb.10.9.4886-4898.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Feder J. H., Rossi J. M., Solomon J., Solomon N., Lindquist S. The consequences of expressing hsp70 in Drosophila cells at normal temperatures. Genes Dev. 1992 Aug;6(8):1402–1413. doi: 10.1101/gad.6.8.1402. [DOI] [PubMed] [Google Scholar]
  18. Feinberg A. P., Vogelstein B. "A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity". Addendum. Anal Biochem. 1984 Feb;137(1):266–267. doi: 10.1016/0003-2697(84)90381-6. [DOI] [PubMed] [Google Scholar]
  19. 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]
  20. Feuerstein N., Cooper H. L. Rapid phosphorylation-dephosphorylation of specific proteins induced by phorbol ester in HL-60 cells. Further characterization of the phosphorylation of 17-kilodalton and 27-kilodalton proteins in myeloid leukemic cells and human monocytes. J Biol Chem. 1984 Mar 10;259(5):2782–2788. [PubMed] [Google Scholar]
  21. Feuerstein N., Cooper H. L. Rapid protein phosphorylation induced by phorbol ester in HL-60 cells. Unique alkali-stable phosphorylation of a 17,000-dalton protein detected by two-dimensional gel electrophoresis. J Biol Chem. 1983 Sep 10;258(17):10786–10793. [PubMed] [Google Scholar]
  22. Fuqua S. A., Blum-Salingaros M., McGuire W. L. Induction of the estrogen-regulated "24K" protein by heat shock. Cancer Res. 1989 Aug 1;49(15):4126–4129. [PubMed] [Google Scholar]
  23. Gaestel M., Gross B., Benndorf R., Strauss M., Schunk W. H., Kraft R., Otto A., Böhm H., Stahl J., Drabsch H. Molecular cloning, sequencing and expression in Escherichia coli of the 25-kDa growth-related protein of Ehrlich ascites tumor and its homology to mammalian stress proteins. Eur J Biochem. 1989 Jan 15;179(1):209–213. doi: 10.1111/j.1432-1033.1989.tb14542.x. [DOI] [PubMed] [Google Scholar]
  24. Gaestel M., Schröder W., Benndorf R., Lippmann C., Buchner K., Hucho F., Erdmann V. A., Bielka H. Identification of the phosphorylation sites of the murine small heat shock protein hsp25. J Biol Chem. 1991 Aug 5;266(22):14721–14724. [PubMed] [Google Scholar]
  25. Gaestel M., Schröder W., Benndorf R., Lippmann C., Buchner K., Hucho F., Erdmann V. A., Bielka H. Identification of the phosphorylation sites of the murine small heat shock protein hsp25. J Biol Chem. 1991 Aug 5;266(22):14721–14724. [PubMed] [Google Scholar]
  26. Hepburn A., Demolle D., Boeynaems J. m., Fiers W., Dumont J. E. Rapid phosphorylation of a 27 kDa protein induced by tumor necrosis factor. FEBS Lett. 1988 Jan 25;227(2):175–178. doi: 10.1016/0014-5793(88)80892-5. [DOI] [PubMed] [Google Scholar]
  27. Hickey E. D., Weber L. A. Modulation of heat-shock polypeptide synthesis in HeLa cells during hyperthermia and recovery. Biochemistry. 1982 Mar 30;21(7):1513–1521. doi: 10.1021/bi00536a008. [DOI] [PubMed] [Google Scholar]
  28. Holbrook N. J., Carlson S. G., Choi A. M., Fargnoli J. Induction of HSP70 gene expression by the antiproliferative prostaglandin PGA2: a growth-dependent response mediated by activation of heat shock transcription factor. Mol Cell Biol. 1992 Apr;12(4):1528–1534. doi: 10.1128/mcb.12.4.1528-1534.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Iida H., Yahara I. Durable synthesis of high molecular weight heat shock proteins in G0 cells of the yeast and other eucaryotes. J Cell Biol. 1984 Jul;99(1 Pt 1):199–207. doi: 10.1083/jcb.99.1.199. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Iwaki T., Iwaki A., Liem R. K., Goldman J. E. Expression of alpha B-crystallin in the developing rat kidney. Kidney Int. 1991 Jul;40(1):52–56. doi: 10.1038/ki.1991.178. [DOI] [PubMed] [Google Scholar]
  31. Iwaki T., Kume-Iwaki A., Goldman J. E. Cellular distribution of alpha B-crystallin in non-lenticular tissues. J Histochem Cytochem. 1990 Jan;38(1):31–39. doi: 10.1177/38.1.2294148. [DOI] [PubMed] [Google Scholar]
  32. Johnston R. N., Kucey B. L. Competitive inhibition of hsp70 gene expression causes thermosensitivity. Science. 1988 Dec 16;242(4885):1551–1554. doi: 10.1126/science.3201244. [DOI] [PubMed] [Google Scholar]
  33. Jones D., Dixon D. K., Graham R. W., Candido E. P. Differential regulation of closely related members of the hsp16 gene family in Caenorhabditis elegans. DNA. 1989 Sep;8(7):481–490. doi: 10.1089/dna.1.1989.8.481. [DOI] [PubMed] [Google Scholar]
  34. Kato K., Shinohara H., Goto S., Inaguma Y., Morishita R., Asano T. Copurification of small heat shock protein with alpha B crystallin from human skeletal muscle. J Biol Chem. 1992 Apr 15;267(11):7718–7725. [PubMed] [Google Scholar]
  35. Kato K., Shinohara H., Kurobe N., Inaguma Y., Shimizu K., Ohshima K. Tissue distribution and developmental profiles of immunoreactive alpha B crystallin in the rat determined with a sensitive immunoassay system. Biochim Biophys Acta. 1991 May 24;1074(1):201–208. doi: 10.1016/0304-4165(91)90062-l. [DOI] [PubMed] [Google Scholar]
  36. Kaur P., Saklatvala J. Interleukin 1 and tumour necrosis factor increase phosphorylation of fibroblast proteins. FEBS Lett. 1988 Dec 5;241(1-2):6–10. doi: 10.1016/0014-5793(88)81019-6. [DOI] [PubMed] [Google Scholar]
  37. Kim Y. J., Shuman J., Sette M., Przybyla A. Nuclear localization and phosphorylation of three 25-kilodalton rat stress proteins. Mol Cell Biol. 1984 Mar;4(3):468–474. doi: 10.1128/mcb.4.3.468-474.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Klemenz R., Fröhli E., Aoyama A., Hoffmann S., Simpson R. J., Moritz R. L., Schäfer R. Alpha B crystallin accumulation is a specific response to Ha-ras and v-mos oncogene expression in mouse NIH 3T3 fibroblasts. Mol Cell Biol. 1991 Feb;11(2):803–812. doi: 10.1128/mcb.11.2.803-812.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Klemenz R., Fröhli E., Steiger R. H., Schäfer R., Aoyama A. Alpha B-crystallin is a small heat shock protein. Proc Natl Acad Sci U S A. 1991 May 1;88(9):3652–3656. doi: 10.1073/pnas.88.9.3652. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Krone P. H., Heikkila J. J. Expression of microinjected hsp 70/CAT and hsp 30/CAT chimeric genes in developing Xenopus laevis embryos. Development. 1989 Jun;106(2):271–281. doi: 10.1242/dev.106.2.271. [DOI] [PubMed] [Google Scholar]
  41. Kurtz S., Rossi J., Petko L., Lindquist S. An ancient developmental induction: heat-shock proteins induced in sporulation and oogenesis. Science. 1986 Mar 7;231(4742):1154–1157. doi: 10.1126/science.3511530. [DOI] [PubMed] [Google Scholar]
  42. Landry J., Chrétien P., Lambert H., Hickey E., Weber L. A. Heat shock resistance conferred by expression of the human HSP27 gene in rodent cells. J Cell Biol. 1989 Jul;109(1):7–15. doi: 10.1083/jcb.109.1.7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Lee S. J. Expression of HSP86 in male germ cells. Mol Cell Biol. 1990 Jun;10(6):3239–3242. doi: 10.1128/mcb.10.6.3239-3242.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Lindquist S., Craig E. A. The heat-shock proteins. Annu Rev Genet. 1988;22:631–677. doi: 10.1146/annurev.ge.22.120188.003215. [DOI] [PubMed] [Google Scholar]
  45. Longoni S., Lattonen S., Bullock G., Chiesi M. Cardiac alpha-crystallin. II. Intracellular localization. Mol Cell Biochem. 1990 Sep 21;97(2):121–128. doi: 10.1007/BF00221053. [DOI] [PubMed] [Google Scholar]
  46. Lowe D. G., Moran L. A. Molecular cloning and analysis of DNA complementary to three mouse Mr = 68,000 heat shock protein mRNAs. J Biol Chem. 1986 Feb 15;261(5):2102–2112. [PubMed] [Google Scholar]
  47. McMaster G. K., Carmichael G. G. Analysis of single- and double-stranded nucleic acids on polyacrylamide and agarose gels by using glyoxal and acridine orange. Proc Natl Acad Sci U S A. 1977 Nov;74(11):4835–4838. doi: 10.1073/pnas.74.11.4835. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Mendelsohn M. E., Zhu Y., O'Neill S. The 29-kDa proteins phosphorylated in thrombin-activated human platelets are forms of the estrogen receptor-related 27-kDa heat shock protein. Proc Natl Acad Sci U S A. 1991 Dec 15;88(24):11212–11216. doi: 10.1073/pnas.88.24.11212. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Milarski K. L., Morimoto R. I. Expression of human HSP70 during the synthetic phase of the cell cycle. Proc Natl Acad Sci U S A. 1986 Dec;83(24):9517–9521. doi: 10.1073/pnas.83.24.9517. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Morrissey J. H. Silver stain for proteins in polyacrylamide gels: a modified procedure with enhanced uniform sensitivity. Anal Biochem. 1981 Nov 1;117(2):307–310. doi: 10.1016/0003-2697(81)90783-1. [DOI] [PubMed] [Google Scholar]
  51. Mosser D. D., Theodorakis N. G., Morimoto R. I. Coordinate changes in heat shock element-binding activity and HSP70 gene transcription rates in human cells. Mol Cell Biol. 1988 Nov;8(11):4736–4744. doi: 10.1128/mcb.8.11.4736-4744.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. O'Farrell P. H. High resolution two-dimensional electrophoresis of proteins. J Biol Chem. 1975 May 25;250(10):4007–4021. [PMC free article] [PubMed] [Google Scholar]
  53. Phillips B., Morimoto R. I. Transcriptional regulation of human hsp70 genes: relationship between cell growth, differentiation, virus infection, and the stress response. Results Probl Cell Differ. 1991;17:167–187. doi: 10.1007/978-3-540-46712-0_12. [DOI] [PubMed] [Google Scholar]
  54. Piatigorsky J. Lens crystallins and their genes: diversity and tissue-specific expression. FASEB J. 1989 Jun;3(8):1933–1940. doi: 10.1096/fasebj.3.8.2656357. [DOI] [PubMed] [Google Scholar]
  55. Piatigorsky J. Lens crystallins. Innovation associated with changes in gene regulation. J Biol Chem. 1992 Mar 5;267(7):4277–4280. [PubMed] [Google Scholar]
  56. Piatigorsky J., Wistow G. J. Enzyme/crystallins: gene sharing as an evolutionary strategy. Cell. 1989 Apr 21;57(2):197–199. doi: 10.1016/0092-8674(89)90956-2. [DOI] [PubMed] [Google Scholar]
  57. Piatigorsky J., Wistow G. The recruitment of crystallins: new functions precede gene duplication. Science. 1991 May 24;252(5009):1078–1079. doi: 10.1126/science.252.5009.1078. [DOI] [PubMed] [Google Scholar]
  58. Regazzi R., Eppenberger U., Fabbro D. The 27,000 daltons stress proteins are phosphorylated by protein kinase C during the tumor promoter-mediated growth inhibition of human mammary carcinoma cells. Biochem Biophys Res Commun. 1988 Apr 15;152(1):62–68. doi: 10.1016/s0006-291x(88)80680-6. [DOI] [PubMed] [Google Scholar]
  59. Robaye B., Hepburn A., Lecocq R., Fiers W., Boeynaems J. M., Dumont J. E. Tumor necrosis factor-alpha induces the phosphorylation of 28kDa stress proteins in endothelial cells: possible role in protection against cytotoxicity? Biochem Biophys Res Commun. 1989 Aug 30;163(1):301–308. doi: 10.1016/0006-291x(89)92135-9. [DOI] [PubMed] [Google Scholar]
  60. Santoro M. G., Garaci E., Amici C. Prostaglandins with antiproliferative activity induce the synthesis of a heat shock protein in human cells. Proc Natl Acad Sci U S A. 1989 Nov;86(21):8407–8411. doi: 10.1073/pnas.86.21.8407. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Schaffner W., Weissmann C. A rapid, sensitive, and specific method for the determination of protein in dilute solution. Anal Biochem. 1973 Dec;56(2):502–514. doi: 10.1016/0003-2697(73)90217-0. [DOI] [PubMed] [Google Scholar]
  62. Schuetz T. J., Gallo G. J., Sheldon L., Tempst P., Kingston R. E. Isolation of a cDNA for HSF2: evidence for two heat shock factor genes in humans. Proc Natl Acad Sci U S A. 1991 Aug 15;88(16):6911–6915. doi: 10.1073/pnas.88.16.6911. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Schütze S., Scheurich P., Pfizenmaier K., Krönke M. Tumor necrosis factor signal transduction. Tissue-specific serine phosphorylation of a 26-kDa cytosolic protein. J Biol Chem. 1989 Feb 25;264(6):3562–3567. [PubMed] [Google Scholar]
  64. Seymour L., Bezwoda W. R., Meyer K., Behr C. Detection of P24 protein in human breast cancer: influence of receptor status and oestrogen exposure. Br J Cancer. 1990 Jun;61(6):886–890. doi: 10.1038/bjc.1990.198. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Sorger P. K., Pelham H. R. Yeast heat shock factor is an essential DNA-binding protein that exhibits temperature-dependent phosphorylation. Cell. 1988 Sep 9;54(6):855–864. doi: 10.1016/s0092-8674(88)91219-6. [DOI] [PubMed] [Google Scholar]
  66. Susek R. E., Lindquist S. Transcriptional derepression of the Saccharomyces cerevisiae HSP26 gene during heat shock. Mol Cell Biol. 1990 Dec;10(12):6362–6373. doi: 10.1128/mcb.10.12.6362-6373.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Thor A., Benz C., Moore D., 2nd, Goldman E., Edgerton S., Landry J., Schwartz L., Mayall B., Hickey E., Weber L. A. Stress response protein (srp-27) determination in primary human breast carcinomas: clinical, histologic, and prognostic correlations. J Natl Cancer Inst. 1991 Feb 6;83(3):170–178. doi: 10.1093/jnci/83.3.170. [DOI] [PubMed] [Google Scholar]
  68. Welch W. J. Phorbol ester, calcium ionophore, or serum added to quiescent rat embryo fibroblast cells all result in the elevated phosphorylation of two 28,000-dalton mammalian stress proteins. J Biol Chem. 1985 Mar 10;260(5):3058–3062. [PubMed] [Google Scholar]
  69. Wiederrecht G., Seto D., Parker C. S. Isolation of the gene encoding the S. cerevisiae heat shock transcription factor. Cell. 1988 Sep 9;54(6):841–853. doi: 10.1016/s0092-8674(88)91197-x. [DOI] [PubMed] [Google Scholar]
  70. Wistow G. J., Piatigorsky J. Lens crystallins: the evolution and expression of proteins for a highly specialized tissue. Annu Rev Biochem. 1988;57:479–504. doi: 10.1146/annurev.bi.57.070188.002403. [DOI] [PubMed] [Google Scholar]
  71. Wistow G. Evolution of a protein superfamily: relationships between vertebrate lens crystallins and microorganism dormancy proteins. J Mol Evol. 1990 Feb;30(2):140–145. doi: 10.1007/BF02099940. [DOI] [PubMed] [Google Scholar]
  72. Wu B. J., Morimoto R. I. Transcription of the human hsp70 gene is induced by serum stimulation. Proc Natl Acad Sci U S A. 1985 Sep;82(18):6070–6074. doi: 10.1073/pnas.82.18.6070. [DOI] [PMC free article] [PubMed] [Google Scholar]
  73. Yost H. J., Petersen R. B., Lindquist S. RNA metabolism: strategies for regulation in the heat shock response. Trends Genet. 1990 Jul;6(7):223–227. doi: 10.1016/0168-9525(90)90183-7. [DOI] [PubMed] [Google Scholar]
  74. Zantema A., de Jong E., Lardenoije R., van der Eb A. J. The expression of heat shock protein hsp27 and a complexed 22-kilodalton protein is inversely correlated with oncogenicity of adenovirus-transformed cells. J Virol. 1989 Aug;63(8):3368–3375. doi: 10.1128/jvi.63.8.3368-3375.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  75. Zimmerman J. L., Petri W., Meselson M. Accumulation of a specific subset of D. melanogaster heat shock mRNAs in normal development without heat shock. Cell. 1983 Apr;32(4):1161–1170. doi: 10.1016/0092-8674(83)90299-4. [DOI] [PubMed] [Google Scholar]
  76. de Jong W. W., Leunissen J. A., Leenen P. J., Zweers A., Versteeg M. Dogfish alpha-crystallin sequences. Comparison with small heat shock proteins and Schistosoma egg antigen. J Biol Chem. 1988 Apr 15;263(11):5141–5149. [PubMed] [Google Scholar]

Articles from The Journal of Cell Biology are provided here courtesy of The Rockefeller University Press

RESOURCES