Comparative study on Hsp25 expression in Mongolian gerbil and mouse cerebellum

  • Published : 2006.12.30

Abstract

The term 'heat shock protein (Hsps)' was derived from the fact that these proteins were initially discovered to be induced by hyperthermic conditions. In response to a range of stressful stimuli, including hyperthermia, immobilization, UV radiation, amino acid analogues, arsenite, various chemicals, and drugs the mammalian brain demonstrates a rapid and intense induction of the heat shock protein. Moreover, Hsps were expressed on the various pathological conditions including trauma, focal or global ischemia, hypoxia, infarction, infections, starvation, and anoxia. Especially, Hsp25 has a protective activity, facilitated by the ability of the protein to decrease the intracellular levels of reactive oxygen species (ROS) as well as its chaperone activity, which favors the degradation of oxidized proteins. Recently, it has clearly demonstrated that Hsp25 is constitutively expressed in the adult mouse cerebellum by parasagittal bands of purkinje cells in three distinct regions, the central zone (lobule VI-VII) and nodular zone (lobule IX-X), and paraflocculus. The Mongolian gerbil has been introduced into stroke study model because of its unique brain vasculature. There are no significant connections between the basilarvertebral system and the carotid system. This anatomy feature renders the mongolian gerbil susceptible to forebrain ischemia-induced seizure. The present study is designed to examine the pattern of Hsp25 expression in the cerebellum of this animal in comparison with that in mouse.

Keywords

References

  1. Armstrong CL, Krueger-Naug AM, Currie RW, et al. 2000. Constitutive expression of the 25-kDa heat shock protein Hsp25 reveals novel parasagittal bands of Purkinje cells in the adult mouse cerebellar cortex. J Comp Neurol 416(3) : 383-397 https://doi.org/10.1002/(SICI)1096-9861(20000117)416:3<383::AID-CNE9>3.0.CO;2-M
  2. Tissieres A, Mitchell HK, Tracy UM. 1974. Protein synthesis in salivary glands of Drosophila melanogaster: Relation to chromosome puffs. J Mol Biol 85(3) : 389-398
  3. Brown IR. 1983. Hyperthermia induces the synthesis of a heat shock protein by polysomes isolated from the fetal and neonatal mammalian brain. J Neurochem 40(5) : 1490-1493 https://doi.org/10.1111/j.1471-4159.1983.tb13596.x
  4. Nowak TS Jr. 1985. Synthesis of a stress protein following transient ischemia in the gerbil. J Neurochem 45(5) : 1635-1641 https://doi.org/10.1111/j.1471-4159.1985.tb07236.x
  5. Craig EA, Weissman JS, Horwich AL. 1994. Heat shock proteins and molecular chaperones: mediators of protein conformation and turnover in the cell. Cell 78(3) : 365-372 https://doi.org/10.1016/0092-8674(94)90416-2
  6. Becker J, Craig EA. 1994. Heat-shock proteins as molecular chaperones. Eur J Biochem 219(1-2) : 11-23 https://doi.org/10.1111/j.1432-1033.1994.tb19909.x
  7. Pelham HR. 1986. Speculations on the functions of the major heat shock and glucose-regulated proteins. Cell 46(7) : 959-961 https://doi.org/10.1016/0092-8674(86)90693-8
  8. Ellis J. 1987. Proteins as molecular chaperones. Nature 328(6129) : 378-379 https://doi.org/10.1038/328378a0
  9. Ellis RJ, van der Vies SM. 1991. Molecular chaperones. Annu Rev Biochem 60 : 321-347 https://doi.org/10.1146/annurev.bi.60.070191.001541
  10. Georgopoulos C, Welch WJ. 1993. Role of the major heat shock proteins as molecular chaperones. Annu Rev Cell Biol 9 : 601-634 https://doi.org/10.1146/annurev.cb.09.110193.003125
  11. Hendrick JP, Hartl FU. 1993. Molecular chaperone functions of heat-shock proteins. Annu Rev Biochem 62 : 349-384 https://doi.org/10.1146/annurev.bi.62.070193.002025
  12. Plumier JC, Armstrong JN, Landry J, et al. 1996. Expression of the 27,000 mol. wt heat shock protein following kainic acid-induced status epilepticus in the rat. Neuroscience 75(3) : 849-856 https://doi.org/10.1016/0306-4522(96)00317-X
  13. Plumier JC, Hopkins DA, Robertson HA, et al. 1997. Constitutive expression of the 27-kDa heat shock protein(Hsp27) in sensory and motor neurons of the rat nervous system. J Comp Neurol 384(3) : 409-428 https://doi.org/10.1002/(SICI)1096-9861(19970804)384:3<409::AID-CNE7>3.0.CO;2-7
  14. Plumier JC, Armstrong JN, Wood NI, et al. 1997. Differential expression of c-fos, Hsp70 and Hsp27 after photothrombotic injury in the rat brain. Brain Res Mol Brain Res 45(2) : 239-246 https://doi.org/10.1016/S0169-328X(96)00255-0
  15. Plumier JC, David JC, Robertson HA, et al. 1997. Cortical application of potassium chloride induces the low-molecular weight heat shock protein (Hsp27) in astrocytes. J Cereb Blood Flow Metab 17(7) : 781-790
  16. Hopkins DA, Plumier JC, Currie RW 1998. Induction of the 27-kDa heat shock protein (Hsp27) in the rat medulla oblongata after vagus nerve injury. Exp Neurol 153(2) : 173-183 https://doi.org/10.1006/exnr.1998.6870
  17. Jakob U, Gaestel M, Engel K, et al. 1993. Small heat shock proteins are molecular chaperones. J Biol Chem 268(3) : 1517-1520
  18. Lavoie JN, Gingras-Breton G, Tanguay RM, et al. 1993. Induction of Chinese hamster HSP27 gene expression in mouse cells confers resistance to heat shock. HSP27 stabilization of the microfilament organization. J Biol Chem 268(5) : 3420-3429
  19. Lavoie JN, Hickey E, Weber LA, et al. 1993. Modulation of actin microfilament dynamics and fluid phase pinocytosis by phosphorylation of heat shock protein 27. J Biol Chem 268(32) : 24210-24214
  20. Mehlen P, Preville X, Chareyron P, et al. 1995. Constitutive expression of human hsp27, Drosophila hsp27, or human alpha B-crystallin confers resistance to TNF- and oxidative stress-induced cytotoxicity in stably transfected murine L929 fibroblasts. J Immunol 154(1) : 363-374
  21. Mehlen P, Kretz-Remy C, Preville X, et al. 1996. Human hsp27, Drosophila hsp27 and human alphaB-crystallin expression-mediated increase in glutathione is essential for the protective activity of these proteins against TNFalpha-induced cell death. EMBO J 15(11) : 2695-2706
  22. Mehlen P, Schulze-Osthoff K, Arrigo AP. 1996. Small stress proteins as novel regulators of apoptosis. Heat shock protein 27 blocks Fas/APO-1- and staurosporine-induced cell death. J Biol Chem 271(28) : 16510-16514 https://doi.org/10.1074/jbc.271.28.16510
  23. Samali A, Cotter TG. 1996. Heat shock proteins increase resistance to apoptosis. Exp Cell Res 223(1) : 163-170 https://doi.org/10.1006/excr.1996.0070
  24. Armstrong CL, Krueger-Naug AM, Currie RW, et al. 2001. Expression of heat-shock protein Hsp25 in mouse Purkinje cells during development reveals novel features of cerebellar compartmentation. J Comp Neurol 429(1) : 7-21 https://doi.org/10.1002/1096-9861(20000101)429:1<7::AID-CNE2>3.0.CO;2-Q
  25. Armstrong CL, Krueger-Naug AM, Currie RW, et al. 2001. Constitutive expression of heat shock protein HSP25 in the central nervous system of the developing and adult mouse. J Comp Neurol 434(3) : 262-274 https://doi.org/10.1002/cne.1176
  26. Gravel C, Hawkes R. 1990. Para-sagittal organization of the rat cerebellar cortex: direct comparison of Purkinje cell compartments and the organization of the spinocerebellar projection. J Comp Neurol 291(1) : 79-102 https://doi.org/10.1002/cne.902910107
  27. Gravel C, Eisenman LM, Sasseville R, et al. 1987. Parasagittal organization of the rat cerebellar cortex: direct correlation between antigenic Purkinje cell bands revealed by mabQ113 and the organization of the olivocerebellar projection. J Comp Neurol 265(2) : 294-310 https://doi.org/10.1002/cne.902650211
  28. Hawkes R. 1992. Antigenic markers of cerebellar modules in the adult mouse. Biochem Soc Trans 20(2) : 391-395 https://doi.org/10.1042/bst0200391
  29. Hawkes R, Gravel C. 1991. The modular cerebellum. Prog Neurobiol 36(4) : 309-327 https://doi.org/10.1016/0301-0082(91)90004-K
  30. Ji Z, Hawkes R. 1994. Topography of Purkinje cell compartments and mossy fiber terminal fields in lobules II and III of the rat cerebellar cortex: spino-cerebellar and cuneocerebellar projections. Neuroscience 61(4) : 935-954 https://doi.org/10.1016/0306-4522(94)90414-6
  31. Ji Z, Hawkes R. 1995. Developing mossy fiber terminal fields in the rat cerebellar cortex may segregate because of Purkinje cell compart-mentation and not competition. J Comp Neurol 359(2) : 197-212 https://doi.org/10.1002/cne.903590202
  32. Sotelo C, Wassef M. 1991. Cerebellar development: afferent organization and Purkinje cell hetero-geneity. Philos Trans R Soc Lond B Biol Sci 331(1261) : 307-313 https://doi.org/10.1098/rstb.1991.0022
  33. Bower JM. 1997. Control of sensory data acquisition. Int Rev Neurobiol 41 : 489-513 https://doi.org/10.1016/S0074-7742(08)60367-0
  34. Hallem JS, Thompson JH, GundappaSulur G, et al. 1999. Spatial corres-pondence between tactile projection patterns and the distribution of the antigenic Purkinje cell markers anti-zebrin I and anti-zebrin II in the cerebellar folium crus IIA of the rat. Neuroscience 93(3) : 1083-1094 https://doi.org/10.1016/S0306-4522(99)00144-X
  35. Hawkes R, Blyth S, Chockkan V, et al. 1993. Structural and molecular compartmentation in the cerebellum. Can J Neurol Sci 20(Suppl 3) : S29-35 https://doi.org/10.1017/S0317167100048502
  36. Van der Steen J, Simpson JI, Tan J. 1994. Functional and anatomic organization of three-dimensional eye movements in rabbit cerebellar flocculus. J Neurophysiol 72(1) : 31-46 https://doi.org/10.1152/jn.1994.72.1.31
  37. Welker WI. 1990. The significance of foliation and fissuration of cerebellar cortex. The cerebellar folium as a fundamental unit of sensorimotor integration. Arch Ital Biol 128(2-4) : 87-109
  38. Hawkes R, Eisenman LM. 1997. Stripes and zones: the origins of regionalization of the adult cerebellum. Perspect Dev Neurobiol 5(1) : 95-105
  39. Herrup K, Kuemerle B. 1997. The compartmentalization of the cerebellum. Annu Rev Neurosci 20 : 61-90 https://doi.org/10.1146/annurev.neuro.20.1.61
  40. Nunzi MG, Grillo M, Margolis FL, et al. 1999. Compartmental organization of Purkinje cells in the mature and developing mouse cerebellum as revealed by an olfactory marker pro-tein-lacZ transgene. J Comp Neurol 404(1) : 97-113 https://doi.org/10.1002/(SICI)1096-9861(19990201)404:1<97::AID-CNE8>3.0.CO;2-1
  41. Oberdick J, Baader SL, Schilling K. 1998. From zebra stripes to postal zones: deciphering patterns of gene expression in the cerebellum. Trends Neurosci 21(9) : 383-390 https://doi.org/10.1016/S0166-2236(98)01325-3
  42. Ozol K, Hayden JM, Oberdick J, et al. 1999. Transverse zones in the vermis of the mouse cerebellum. J Comp Neurol 412(1) : 95-111 https://doi.org/10.1002/(SICI)1096-9861(19990913)412:1<95::AID-CNE7>3.0.CO;2-Y
  43. Tan J, Gerrits NM, Nanhoe R, et al. 1995. Zonal organization of the climbing fiber projection to the flocculus and nodulus of the rabbit: a combined axonal tracing and acetyl-cholinesterase histochemical study. J Comp Neurol 356(1) : 23-50 https://doi.org/10.1002/cne.903560103
  44. Serapide MF, Cicirata F, Sotelo C, et al. 1994. The pontocerebellar projection: longitudinal zonal distribution of fibers from discrete regions of the pontine nuclei to vermal and para-floccular cortices in the rat. Brain Res 644(1) : 175-180 https://doi.org/10.1016/0006-8993(94)90362-X
  45. Tolbert DL, Gutting JC. 1997. Quantitative analysis of cuneocere-bellar projections in rats: differential topography in the anterior and posterior lobes. Neuroscience 80(2) : 359-371 https://doi.org/10.1016/S0306-4522(97)00081-X
  46. Pockley AG. 2003. Heat shock proteins as regulators of the immune response. Lancet 362 : 469-476 https://doi.org/10.1016/S0140-6736(03)14075-5
  47. Arrigo AP. 1995. Expression of stress genes during development. Neuro-pathol Appl Neurobiol 21(6) : 488-491 https://doi.org/10.1111/j.1365-2990.1995.tb01094.x
  48. Sanders BM, Martin LS, Howe SR, et al. 1994. Tissue-specific differences in accumulation of stress proteins in Mytilus edulis exposed to a range of copper concentrations. Toxicol Appl Pharmacol 125(2) : 206-213 https://doi.org/10.1006/taap.1994.1066
  49. Sanders BM. 1993. Stress proteins in aquatic organisms: an environmental perspective. Crit Rev Toxicol 23(1) : 49-75 https://doi.org/10.3109/10408449309104074
  50. Currie S, Tufts B. 1997. Synthesis of stress protein 70 (Hsp70) in rainbow trout (Oncorhynchus mykiss) red blood cells. J Exp Biol 200(Pt 3) : 607-614
  51. Dietz TJ. 1994. Acclimation of the threshold induction temperatures for 70-kDa and 90-kDa heat shock proteins in the fish Gillichthys mirabilis. J Exp Biol 188 : 333-338
  52. Schlesinger MJ. 1990. Heat shock proteins. J Biol Chem 265(21) : 12111-12114
  53. Kultz D. 1996. Plasticity and stresor specificity of osmotic and heat shock responses of Gillichthys mirabilis gill cells. Am J Physiol 271(4 Pt 1) : C1181-193 https://doi.org/10.1152/ajpcell.1996.271.4.C1181
  54. Mestril R, Chi SH, Sayen MR, et al. 1994. Isolation of a novel inducible rat heat-shock protein (HSP70) gene and its expression during ischaemia/hypoxia and heat shock. Biochem J 298(Pt 3) : 561-569 https://doi.org/10.1042/bj2980561
  55. Myrmel T, McCully JD, Malikin L, et al. 1994. Heat-shock protein 70 mRNA is induced by anaerobic metabolism in rat hearts. Circulation 90(5 Pt 2) : II299-305
  56. Costigan M, Mannion RJ, Kendall G, et al. 1998. Heat shock protein 27: developmental regulation and expression after peripheral nerve injury. J Neurosci 18(15) : 5891-5900 https://doi.org/10.1523/JNEUROSCI.18-15-05891.1998
  57. Head MW, Corbin E, Goldman JE. 1994. Coordinate and independent regulation of alpha B-crystallin and hsp27 expression in response to physiological stress. J Cell Physiol 159(1) : 41-50 https://doi.org/10.1002/jcp.1041590107
  58. Gernold M, Knauf U, Gaestel M, et al. 1993. Development and tissue-specific distribution of mouse small heat shock protein hsp25. Dev Genet 14(2) : 103-111 https://doi.org/10.1002/dvg.1020140204
  59. Mehlen P, Coronas V, Ljubic-Thibal V, et al. 1999. Small stress protein Hsp27 accumulation during dopamine-mediated differentiation of rat olfactory neurons counteracts apoptosis. Cell Death Differ 6(3) : 227-233 https://doi.org/10.1038/sj.cdd.4400483
  60. Wagstaff MJ, Collaco-Moraes Y, Smith J, et al. 1999. Protection of neuronal cells from apoptosis by Hsp27 delivered with a herpes simplex virus-based vector. J Biol Chem 274(8) : 5061-5069 https://doi.org/10.1074/jbc.274.8.5061
  61. Iwaki T, Iwaki A, Tateishi J, et al. 1993. Alpha B-crystallin and 27-kd heat shock protein are regulated by stress conditions in the central nervous system and accumulate in Rosenthal fibers. Am J Pathol 143(2) : 487-195
  62. Renkawek K, Bosman GJ, de Jong WW. 1994. Expression of small heat-shock protein hsp 27 in reactive gliosis in Alzheimer disease and other types of dementia. Acta Neuropathol (Berl) 87(5) : 511-519 https://doi.org/10.1007/BF00294178
  63. Shinohara H, Inaguma Y, Goto S, et al. 1993. Alpha B crystallin and HSP28 are enhanced in the cerebral cortex of patients with Alzheimer's disease. J Neurol Sci 119(2) : 203-208 https://doi.org/10.1016/0022-510X(93)90135-L
  64. Chung YH, Joo KM, Nam RH, et al. 2005. Immunohistochemical study on the distribution of the voltage-gated potassium channels in the gerbil cerebellum. Neurosci Lett 374(1) : 58-62 https://doi.org/10.1016/j.neulet.2004.10.029