Steroid hormone regulation of the voltage-gated, calcium-activated potassium channel expression in developing muscular and neural systems

Developmental Neurobiology

Volumn 70, Issue 13, 2010, Pages 884-896

  Garrison, Sheldon L ^a   Witten, Jane L ^a  

^a UNIVERSITY OF WISCONSIN MILWAUKEE   (United States)

Author keywords

Cell excitability; Ecdysteroid receptor; KCNMA1; Manduca sexta; Ultraspiracle

Indexed keywords

CALCIUM ACTIVATED POTASSIUM CHANNEL; ECDYSONE; ECDYSONE RECEPTOR; PROTEIN; STEROID HORMONE; ULTRASPIRACLE PROTEIN; UNCLASSIFIED DRUG; VOLTAGE GATED POTASSIUM CHANNEL;

ARTICLE; CENTRAL NERVOUS SYSTEM; FLIGHT MUSCLE; GENE CONTROL; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; MANDUCA SEXTA; MSE75B GENE; MSSLO GENE; MUSCLE DEVELOPMENT; NERVE CELL EXCITABILITY; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; TRANSCRIPTION REGULATION;

ANIMALS; ECDYSONE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MANDUCA; MUSCLE, STRIATED; NERVOUS SYSTEM; POTASSIUM CHANNELS, VOLTAGE-GATED; STEROIDS;

EID: 78649362407     PISSN: 19328451     EISSN: 10974695     Source Type: Journal    
DOI: 10.1002/dneu.20830     Document Type: Article

References (82)

1. Adelman JP, Shen KZ, Kavanaugh MP, Warren RA, Wu YN, Lagrutta A, Bond CT, et al. 1992. Calcium-activated potassium channels expressed from cloned complementary DNAs. Neuron 9:209-216.
2. Antoniewski C, Laval M, Dahan A, Lepesant JA. 1994. The ecdysone response enhancer of the Fbp1 gene of Drosophila melanogaster is a direct target for the EcR/USP nuclear receptor. Mol Cell Biol 14:4465-4474.
3. Archer SL, Gragasin FS, Wu X, Wang S, McMurtry S, Kim DH, Platonov M, et al. 2003. Endothelium-derived hyperpolarizing factor in human internal mammary artery is 11,12-epoxyeicosatrienoic acid and causes relaxation by activating smooth muscle BK(Ca) channels. Circulation 107:769-776.
4. Bayline RJ, Duch C, Levine RB. 2001. Nerve-muscle interactions regulate motor terminal growth and myoblast distribution during muscle development. Dev Biol 231: 348-363.
5. Bernardo TJ, Dubrovskaya VA, Jannat H, Maughan B, Dubrovsky EB. 2009. Hormonal regulation of the E75 gene in Drosophila: Identifying functional regulatory elements through computational and biological analysis. J Mol Biol 387:794-808.
6. Bidmon HJ, Granger NA, Cherbas P, Maroy P, Stumpf WE. 1991. Ecdysteroid receptors in the central nervous system of Manduca sexta: Their changes in distribution and quantity during larval-pupal development. J Comp Neurol 310:337-355.
7. Bollenbacher WE, Smith SL, Goodman W, Gilbert LI. 1981. Ecdysteroid titer during larval-pupal-adult development of the tobacco hornworm Manduca sexta. Gen Comp Endocrinol 44:302-306.
8. Brandt N, Kuhn S, Munkner S, Braig C, Winter H, Blin N, Vonthein R, et al. 2007. Thyroid hormone deficiency affects postnatal spiking activity and expression of Ca2+ and K+ channels in rodent inner hair cells. J Neurosci 27:3174-3186.
9. Brenner R, Thomas TO, Becker MN, Atkinson NS. 1996. Tissue-specific expression of a Ca(2+)-activated K+ channel is controlled by multiple upstream regulatory elements. J Neurosci 16:1827-1835.
10. Carl A, Bayguinov O, Shuttleworth CW, Ward SM, Sanders KM. 1995. Role of Ca(2+)-activated K+ channels in electrical activity of longitudinal and circular muscle layers of canine colon. Am J Physiol 268:C619-C627.
11. Chen L, Tian L, MacDonald SH, McClafferty H, Hammond MS, Huibant JM, Ruth P, et al. 2005. Functionally diverse complement of large conductance calciumand voltage-activated potassium channel (BK) alpha-subunits generated from a single site of splicing. J Biol Chem 280:33599-33609.
12. Cherbas L, Lee K, Cherbas P. 1991. Identification of ecdysone response elements by analysis of the Drosophila Eip28/29 gene. Genes Dev 5:120-131.
13. Dryer SE, Lhuillier L, Cameron JS, Martin-Caraballo M. 2003. Expression of K(Ca) channels in identified populations of developing vertebrate neurons: Role of neurotrophic factors and activity. J Physiol Paris 97:49-58.
14. Duch C, Bayline RJ, Levine RB. 2000. Postembryonic development of the dorsal longitudinal flight muscle and its innervation in Manduca sexta. J Comp Neurol 422:1-17.
15. Duch C, Mentel T. 2003. Stage-specific activity patterns affect motoneuron axonal retraction and outgrowth during the metamorphosis of Manduca sexta. Eur J Neurosci 17:945-962.
16. Duch C, Mentel T. 2004. Activity affects dendritic shape and synapse elimination during steroid controlled dendritic retraction in Manduca sexta. J Neurosci 24:9826-9837.
17. Elkins T, Ganetzky B. 1988. The roles of potassium currents in Drosophila flight muscles. J Neurosci 8:428-434.
18. Elkins T, Ganetzky B, Wu CF. 1986. A Drosophila mutation that eliminates a calcium-dependent potassium current. Proc Natl Acad Sci USA 83:8415-8419.
19. Fahrbach SE. 1992. Developmental regulation of ecdysteroid receptors in the nervous system of Manduca sexta. J Exp Zool 261:245-253.
20. Favero M, Jiang DJ, Chiamulera C, Cangiano A, Fumagalli GF. 2008. Expression of small-conductance calcium-activated potassium channels (SK3) in skeletal muscle: Regulation by muscle activity. J Physiol 586:4763-4774.
21. Fujiwara H, Jindra M, Newitt R, Palli SR, Hiruma K, Riddiford LM. 1995. Cloning of an ecdysone receptor homolog from Manduca sexta and the developmental profile of its mRNA in wings. Insect Biochem Mol Biol 25:845-856.
22. Grunewald B, Levine RB. 1998. Ecdysteroid control of ionic current development in Manduca sexta motoneurons. J Neurobiol 37:211-223.
23. Hafidi A, Beurg M, Dulon D. 2005. Localization and developmental expression of BK channels in mammalian cochlear hair cells. Neuroscience 130:475-484.
24. Hegstrom CD, Riddiford LM, Truman JW. 1998. Steroid and neuronal regulation of ecdysone receptor expression during metamorphosis of muscle in the moth, Manduca sexta. J Neurosci 18:1786-1794.
25. Hegstrom CD, Truman JW. 1996. Steroid control of muscle remodeling during metamorphosis in Manduca sexta. J Neurobiol 29:535-550.
26. Hiruma K, Riddiford LM. 1985. Hormonal regulation of dopa decarboxylase during a larval molt. Dev Biol 110:509-513.
27. Holdiman AJFD, England SK. 2002. 17beta-Estradiol upregulates distinct maxi-K channel transcripts in mouse uterus. Mol Cell Endrocrinol 192:1-6.
28. Huet F, Ruiz C, Richards G. 1995. Sequential gene activation by ecdysone in Drosophila melanogaster: The hierarchical equivalence of early and early late genes. Development 121:1195-1204.
29. Jindra M, Huang JY, Malone F, Asahina M, Riddiford LM. 1997. Identification and mRNA developmental profiles of two ultraspiracle isoforms in the epidermis and wings of Manduca sexta. Insect Mol Biol 6:41-53.
30. Jindra M, Malone F, Hiruma K, Riddiford LM. 1996. Developmental profiles and ecdysteroid regulation of the mRNAs for two ecdysone receptor isoforms in the epidermis and wings of the tobacco hornworm, Manduca sexta. Dev Biol 180:258-272.
31. Kammer AE, Rheuben MB. 1976. Adult motor patterns produced by moth pupae during development. J Exp Biol 65:65-84.
32. Kammer AE, AK, SC. 1979. Maturation of the flight motor pattern without movement in Manduca sexta. J Comparative Physiol 130:29-37.
33. Keyser MR, Witten JL. 2005. Calcium-activated potassium channel of the tobacco hornworm, Manduca sexta: Molecular characterization and expression analysis. J Exp Biol 208:4167-4179.
34. Kukuljan M, Taylor A, Chouinard H, Olguin P, Rojas CV, Ribera AB. 2003. Selective regulation of xSlo splice variants during Xenopus embryogenesis. J Neurophysiol 90:3352-3360.
35. Kundu P, Alioua A, Stefani E, Toro L. 2007. Regulation of mouse Slo gene expression: Multiple promoters, transcription start sites, and genomic action of estrogen. J Biol Chem 282:27478-27492.
36. Lagrutta A, Shen KZ, North RA, Adelman JP. 1994. Functional differences among alternatively spliced variants of Slowpoke, a Drosophila calcium-activated potassium channel. J Biol Chem 269:20347-20351.
37. Lai GJ, McCobb DP. 2002. Opposing actions of adrenal androgens and glucocorticoids on alternative splicing of Slo potassium channels in bovine chromaffin cells. Proc Natl Acad Sci USA 99:7722-7727.
38. Lai GJ, McCobb DP. 2006. Regulation of alternative splicing of Slo K+ channels in adrenal and pituitary during the stress-hyporesponsive period of rat development. Endocrinology 147:3961-3967.
39. Larionov A, Krause A, Miller W. 2005. A standard curve based method for relative real time PCR data processing. BMC Bioinformatics 6:62.
40. Lee T, Marticke S, Sung C, Robinow S, Luo L. 2000. Cellautonomous requirement of the USP/EcR-B ecdysone receptor for mushroom body neuronal remodeling in Drosophila. Neuron 28:807-818.
41. Levitan ES, Gealy R, Trimmer JS, Takimoto K. 1995. Membrane depolarization inhibits Kv1.5 voltage-gated K+ channel gene transcription and protein expression in pituitary cells. J Biol Chem 270:6036-6041.
42. Lhuillier L, Dryer SE. 2000. Developmental regulation of neuronal KCa channels by TGFbeta 1: Transcriptional and posttranscriptional effects mediated by Erk MAP kinase. J Neurosci 20:5616-5622.
43. Lim HH, Park BJ, Choi HS, Park CS, Eom SH, Ahnn J. 1999. Identification and characterization of a putative C. elegans potassium channel gene (Ce-slo-2) distantly related to Ca(2+)-activated K(+) channels. Gene 240:35-43.
44. Lovell PV, King JT, McCobb DP. 2004. Acute modulation of adrenal chromaffin cell BK channel gating and cell excitability by glucocorticoids. J Neurophysiol 91:561-570.
45. Lovell PV, McCobb DP. 2001. Pituitary control of BK potassium channel function and intrinsic firing properties of adrenal chromaffin cells. J Neurosci 21:3429-3442.
46. Low P, Talian GC, Sass M. 2005. Up-and down-regulated genes in muscles that undergo developmentally programmed cell death in the insect Manduca sexta. FEBS Lett 579:4943-4948.
47. Lytle M. 2008. Developmental regulation and cellular-specific localization of a voltage-gated calcium activated potassion ion channel and two neuropeptide genes: Masallatotropin and MasF10 genes, in the tobacco hornworm, Manduca sexta. Biological Sciences, Vol. Ph.D. University of Wisconsin, Milwaukee.
48. MacDonald SH, Ruth P, Knaus HG, Shipston MJ. 2006. Increased large conductance calcium-activated potassium (BK) channel expression accompanied by STREX variant downregulation in the developing mouse CNS. BMC Dev Biol 6:37.
49. Martin-Caraballo M, Dryer SE. 2002. Activity-and target-dependent regulation of large-conductance Ca2+-activated K+ channels in developing chick lumbar motoneurons. J Neurosci 22:73-81.
50. Mori Y, Folco E, Koren G. 1995. GH3 cell-specific expression of Kv1.5 gene. Regulation by a silencer containing a dinucleotide repetitive element. J Biol Chem 270:27788-27796.
51. Moto K, Kojima H, Kurihara M, Iwami M, Matsumoto S. 2003. Cell-specific expression of enhanced green fluorescence protein under the control of neuropeptide gene promoters in the brain of the silkworm, Bombyx mori, using Bombyx mori nucleopolyhedrovirus-derived vectors Insect. Biochem Mol Biol 33:7-12.
52. Muller YL, Reitstetter R, Yool AJ. 1998. Regulation of Ca2+-dependent K+ channel expression in rat cerebellum during postnatal development. J Neurosci 18:16-25.
53. Muller YL, Reitstetter R, Yool AJ. 2000. Antisense knock-down of calcium-dependent K+ channels in developing cerebellar Purkinje neurons. Brain Res Dev Brain Res 120:135-140.
54. Muller YL, Yool AJ. 1998. Increased calcium-dependent K+ channel activity contributes to the maturation of cellular firing patterns in developing cerebellar Purkinje neurons. Brain Res Dev Brain Res 108:193-203.
55. Raffaelli G, Saviane C, Mohajerani MH, Pedarzani P, Cherubini E. 2004. BK potassium channels control transmitter release at CA3-CA3 synapses in the rat hippocampus. J Physiol 557:147-157.
56. Raingo J, Rebolledo A, Grassi de Gende AO, Sanz N, Tommasi J, Milesi V. 2005. pH effects on high conductance Ca2+-activated K+ channels (BK(Ca)) in human internal mammary artery smooth muscle cells. Life Sci 77:993-2003.
57. Rheuben MB, Kammer AE. 1980. Comparison of slow larval and fast adult muscle innervated by the same motor neurone. J Exp Biol 84:103-118.
58. Riddiford LM. 1993. Hormone receptors and the regulation of insect metamorphosis. Receptor 3:203-209.
59. Riddiford LM, Cherbas P, Truman JW. 2000. Ecdysone receptors and their biological actions. Vitam Horm 60:1-73.
60. Riddiford LM, Hiruma K, Zhou X, Nelson CA. 2003. Insights into the molecular basis of the hormonal control of molting and metamorphosis from Manduca sexta and Drosophila melanogaster. Insect Biochem Mol Biol 33:1327-1338.
61. Robinow S, Talbot WS, Hogness DS, Truman JW. 1993. Programmed cell death in the Drosophila CNS is ecdysone-regulated and coupled with a specific ecdysone receptor isoform. Development 119:1251-1259.
62. Saito M, Nelson C, Salkoff L, Lingle CJ. 1997. A cysteinerich domain defined by a novel exon in a slo variant in rat adrenal chromaffin cells and PC12 cells. J Biol Chem 272:11710-11717.
63. Salkoff LB, Wyman RJ. 1983. Ion currents in Drosophila flight muscles. J Physiol 337:687-709.
64. Schubiger M, Wade AA, Carney GE, Truman JW, Bender M. 1998. Drosophila EcR-B ecdysone receptor isoforms are required for larval molting and for neuron remodeling during metamorphosis. Development 125:2053-2062.
65. Schwartz LM, Jones ME, Kosz L, Kuah K. 1993. Selective repression of actin and myosin heavy chain expression during the programmed death of insect skeletal muscle. Dev Biol 158:448-455.
66. Schwartz LM, Myer A, Kosz L, Engelstein M, Maier C. 1990. Activation of polyubiquitin gene expression during developmentally programmed cell death. Neuron 5:411-419.
67. Schwartz LM, Truman JW. 1983. Hormonal control of rates of metamorphic development in the tobacco hornworm Manduca sexta. Dev Biol 99:103-114.
68. Shanavas A, Nayak BP, Dutta-Gupta A. 1996. Ecdysteroid mediated muscle actin synthesis during the larval development of rice moth, Corcyra cephalonica. Biochem Mol Biol Int 40:955-963.
69. Shao LR, Halvorsrud R, Borg-Graham L, Storm JF. 1999. The role of BK-type Ca2+-dependent K+ channels in spike broadening during repetitive firing in rat hippocampal pyramidal cells. J Physiol 521(Part 1):135-146.
70. Takimoto K, Fomina AF, Gealy R, Trimmer JS, Levitan ES. 1993. Dexamethasone rapidly induces Kv1.5 K+ channel gene transcription and expression in clonal pituitary cells. Neuron 11:359-369.
71. Talbot WS, Swyryd EA, Hogness DS. 1993. Drosophila tissues with different metamorphic responses to ecdysone express different ecdysone receptor isoforms. Cell 73:1323-1337.
72. Tian L, Duncan RR, Hammond MS, Coghill LS, Wen H, Rusinova R, Clark AG, et al. 2001. Alternative splicing switches potassium channel sensitivity to protein phosphorylation. J Biol Chem 276:7717-7720.
73. Tricarico D, Mele A, Conte Camerino D. 2005. Phenotype-dependent functional and pharmacological properties of BK channels in skeletal muscle: Effects of microgravity. Neurobiol Dis 20:296-302.
74. Truman JW, Talbot WS, Fahrbach SE, Hogness DS. 1994. Ecdysone receptor expression in the CNS correlates with stage-specific responses to ecdysteroids during Drosophila and Manduca development. Development 120:219-234.
75. Tweedie S, Ashburner M, Falls K, Leyland P, McQuilton P, Marygold S, Millburn G, et al. 2009. FlyBase: Enhancing Drosophila Gene Ontology annotations. Nucleic Acids Res 37:D555-D559.
76. Weevers RD. 1966. A lepidopteran saline: Effects of inorganic cation concentrations on sensory, reflex and motor responses in a herbivorous insect. J Exp Biol 44:163-175.
77. Xie J, Black DL. 2001. A CaMK IV responsive RNA element mediates depolarization-induced alternative splicing of ion channels. Nature 410:936-939.
78. Xie J, McCobb DP. 1998. Control of alternative splicing of potassium channels by stress hormones. Science 280:443-446.
79. Yu JY, Upadhyaya AB, Atkinson NS. 2006. Tissue-specific alternative splicing of BK channel transcripts in Drosophila. Genes Brain Behav 5:329-339.
80. Zhang Y, Joiner WJ, Bhattacharjee A, Rassendren F, Magoski NS, Kaczmarek LK. 2004. The appearance of a protein kinase A-regulated splice isoform of slo is associated with the maturation of neurons that control reproductive behavior. J Biol Chem 279:52324-52330.
81. Zhou B, Hiruma K, Jindra M, Shinoda T, Segraves WA, Malone F, Riddiford LM. 1998. Regulation of the transcription factor E75 by 20-hydroxyecdysone and juvenile hormone in the epidermis of the tobacco hornworm, Manduca sexta, during larval molting and metamorphosis. Dev Biol 193:127-138.
82. Zhu N, Eghbali M, Helguera G, Song M, Stefani E, Toro L. 2005. Alternative splicing of Slo channel gene programmed by estrogen, progesterone and pregnancy. FEBS Lett 579:4856-4860.