Phylogenetic Analysis and Taste Cell  Expression of Calpain 9 in Catfish  (Ictalurus punctatus)

Tetsuya Ookura; Eiki Koyama; Anne Hansen; John H. Teeter; Yukio Kawamura; Joseph G. Brand

doi:10.4236/ns.2015.73016

Home > Journals > Biomedical & Life Sciences | Chemistry & Materials Science > NS

NS> Vol.7 No.3, March 2015

Share This Article:

Open Access

Phylogenetic Analysis and Taste Cell Expression of Calpain 9 in Catfish (Ictalurus punctatus)

Abstract Full-Text HTML XML

Download as PDF (Size:1137KB) PP. 143-150

DOI: 10.4236/ns.2015.73016 2,772 Downloads 3,160 Views Citations

Author(s) Leave a comment

Tetsuya Ookura^1,2, Eiki Koyama^3,4, Anne Hansen⁵, John H. Teeter¹, Yukio Kawamura^2,6, Joseph G. Brand^1,3,7

Affiliation(s)

¹Monell Chemical Senses Center, Philadelphia, USA.
²Division of Food Function, National Food Research Institute, Tsukuba, Japan.
³Department of Biochemistry, School of Dental Medicine, University of Pennsylvania, Philadelphia, USA.
⁴Division of Orthopedic Surgery, The Children’s Hospital of Philadelphia, Philadelphia, USA.
⁵Cell and Developmental Biology, School of Medicine, University of Colorado, Denver, USA.
⁶Department of Food and Nutrition, Kyoto Women’s University, Kyoto, Japan.
⁷Veterans Affairs Medical Center, University of Pennsylvania, Philadelphia, USA.

ABSTRACT

The calpains, calcium-activated neutral proteases, play important roles in calcium-regulated intra-cellular signal transduction cascades. Here we report the isolation and initial characterization of a cDNA encoding a calpain 9, digestive tract specific calpain, from catfish taste epithelium. This calpain 9 (Ip-CAPN9a) shares 61% identity with human calpain 9. Phylogenetic analysis provides evidence that catfish calpain 9 and the related enzymes from Oncorhynchus mykiss, Danio rerio, Xenopus laevis, Mus musculus, Rattus norvegicus and Homo sapiens make up a distinct clade within the tissue-specific calpain family. Northern blot analysis reveals that Ip-CAPN9a is predominantly expressed in barbell and digestive tract, but not expressed in brain. An antibody against the N-terminal segment of Ip-CAPN9a recognizes cells within the taste buds in catfish barbells.

KEYWORDS

Gene Evolution, Taste, Novel Type

Conflicts of Interest

The authors declare no conflicts of interest.

Cite this paper

Ookura, T. , Koyama, E. , Hansen, A. , Teeter, J. , Kawamura, Y. and Brand, J. (2015) Phylogenetic Analysis and Taste Cell Expression of Calpain 9 in Catfish (Ictalurus punctatus). Natural Science, 7, 143-150. doi: 10.4236/ns.2015.73016.

References

[1]	Sorimachi, H., Toyama-Sorimachi, N., Saido, T.C., Kawasaki, H., Sugita, H., Miyasaka, M., Arahata, K., Ishiura, S. and Suzuki, K. (1993) Muscle-Specific Calpain, p94, Is Degraded by Autolysis Immediately after Translation, Resulting in Disappearance from Muscle. Journal of Biological Chemistry, 268, 10593-10605.

[2]	Richard, I., Broux, O., Allamand, V., Fougerousse, F., Chiannilkulchai, N., Bourg, N., Brenguier, L., Devaud, C., Pasturaud, P., Roudaut, C., et al. (1995) Mutations in the Proteolytic Enzyme Calpain 3 Cause Limb-Girdle Muscular Dystrophy Type 2A. Cell, 81, 27-40. http://dx.doi.org/10.1016/0092-8674(95)90368-2

[3]	Ma, H., Fukiage, C., Azuma, M. and Shearer, T.R. (1998) Cloning and Expression of mRNA for Calpain Lp82 from Rat Lens: Splice Variant of p94. Investigative Ophthalmology Visual Science, 39, 454-461.

[4]	Sorimachi, H., Ishiura, S. and Suzuki, K. (1993) A Novel Tissue-Specific Calpain Species Expressed Predominantly in the Stomach Comprises Two Alternative Splicing Products with and without Ca(2+)-Binding Domain. Journal of Biological Chemistry, 268, 19476-19482.

[5]	Lee, H.J., Sorimachi, H., Jeong, S.Y., Ishiura, S. and Suzuki, K. (1998) Molecular Cloning and Characterization of a Novel Tissue-Specific Calpain Predominantly Expressed in the Digestive Tract. Biological Chemistry, 379, 175-183. http://dx.doi.org/10.1515/bchm.1998.379.2.175

[6]	Hata, S., Abe, M., Suzuki, H., Kitamura, F., Toyama-Sorimachi, N., Abe, K., Sakimura, K. and Sorimachi, H. (2010) Calpain 8/nCL-2 and Calpain 9/nCL-4 Constitute an Active Protease Complex, G-Calpain, Involved in Gastric Mucosal Defense. PLoS Genetics, 6, e1001040. http://dx.doi.org/10.1371/journal.pgen.1001040

[7]	Yoshikawa, Y., Mukai, H., Hino, F., Asada, K. and Kato, I. (2000) Isolation of Two Novel Genes, Down-Regulated in Gastric Cancer. Japanese Journal of Cancer Research, 91, 459-463. http://dx.doi.org/10.1111/j.1349-7006.2000.tb00967.x

[8]	Markmann, A., Schafer, S., Linz, W., Lohn, M., Busch, A.E. and Wohlfart, P. (2005) Down-Regulation of Calpain 9 Is Linked to Hypertensive Heart and Kidney. Cellular Physiology and Biochemistry, 15, 109-116. http://dx.doi.org/10.1159/000083643

[9]	Sorimachi, H., Ishiura, S. and Suzuki, K. (1997) Structure and Physiological Function of Calpains. Biochemical Journal, 328, 721-732.

[10]	Lin, G.D., Chattopadhyay, D., Maki, M., Wang, K.K., Carson, M., Jin, L., Yuen, P.W., Takano, E., Hatanaka, M., DeLucas, L.J. and Narayana, S.V. (1997) Crystal Structure of Calcium Bound Domain VI of Calpain at 1.9 A Resolution and Its Role in Enzyme Assembly, Regulation, and Inhibitor Binding. Nature Structural Molecular Biology, 4, 539-547. http://dx.doi.org/10.1038/nsb0797-539

[11]	Blanchard, H., Grochulski, P., Li, Y., Arthur, J.S., Davies, P.L., Elce, J.S. and Cygler, M. (1997) Structure of a Calpain Ca2+-Binding Domain Reveals a Novel EF-Hand and Ca2+-Induced Conformational Changes. Nature Structural Biology, 4, 532-538. http://dx.doi.org/10.1038/nsb0797-532

[12]	Lee, H.J., Tomioka, S., Kinbara, K., Masumoto, H., Jeong, S.Y., Sorimachi, H., Ishiura, S. and Suzuki, K. (1999) Characterization of a Human Digestive Tract-Specific Calpain, nCL-4, Expressed in the Baculovirus System. Archives of Biochemistry and Biophysics, 362, 22-31. http://dx.doi.org/10.1006/abbi.1998.1021

[13]	Azarian, S.M., King, A.J., Hallett, M.A. and Williams, D.S. (1995) Selective Proteolysis of Arrestin by Calpain. Molecular and Its Effect on Rhodopsin Dephosphorylation. The Journal of Biological Chemistry, 270, 24375-24384. http://dx.doi.org/10.1074/jbc.270.41.24375,

[14]	Magnusson, A., Haug, L.S., Walaas, S.I. and Ostvolt, A.C. (1993) Calcium-Induced Degradation of the Inositol(1,4,5)-Trisphosphate Receptor/Ca2+-Channel. FEBS Letters, 323, 229-232. http://dx.doi.org/10.1016/0014-5793(93)81345-Z

[15]	Banno, Y., Nakashima, S., Hachiya, T. and Nozawa, Y. (1995) Endogenous Cleavage of Phospholipase C-beta3 by Agonist-Induced Activation of Calpain in Human Platelets. The Journal of Biological Chemistry, 270, 4318-4324. http://dx.doi.org/10.1074/jbc.270.9.4318

[16]	Greenwood, A.F. and Jope, R.S. (1994) Brain G-Protein Proteolysis by Calpain: Enhancement by Lithium. Brain Research, 636, 320-326. http://dx.doi.org/10.1016/0006-8993(94)91031-6

[17]	Shinozaki, K., Maruyama, K., Kume, H., Tomita, T., Saido, T.C., Iwatsubo, T. and Obata, K. (1998) The Presenilin 2 Loop Domain Interacts with the Mu-Calpain C-Terminal Region. International Journal of Molecular Medicine, 1, 797-799.

[18]	Roper, S.D. (2006) Signaling in the Chemosensory Systems. Cellular and Molecular Life Sciences, 63, 1494-1500. http://dx.doi.org/10.1007/s00018-006-6112-9

[19]	Ookura, T., Koyama, E., Puchalski, R.B., Teeter, J.H., Bayley, D.L. and Brand, J.G. (1997) Molecular Cloning of Calpain from Taste Epithelium of the Channel Catfish, Ictalurus punctatus. Chemical Senses, 22,764-765.

[20]	Katoh, K., Kuma, K., Toh, H. and Miyata, T. (2005) MAFFT Version 5: Improvement in Accuracy of Multiple Sequence Alignment. Nucleic Acids Research, 33, 511-518. http://dx.doi.org/10.1093/nar/gki198

[21]	Felsenstein, J. (1981) Evolutionary Trees from DNA Sequences: A Maximum Likelihood Approach. Journal of Molecular Evolution, 17, 368-376. http://dx.doi.org/10.1007/BF01734359

[22]	Stamatakis, A. (2006) RAxML-VI-HPC: Maximum Likelihood-Based Phylogenetic Analyses with Thousands of Taxa and Mixed Models. Bioinformatics, 22, 2688-2690. http://dx.doi.org/10.1093/bioinformatics/btl446

[23]	Jones, D.T., Taylor, W.R. and Thornton, J.M. (1992) The Rapid Generation of Mutation Data Matrices from Protein Sequences. Computer Applications in the Biosciences, 8, 275-282.

[24]	Tamura, K., Dudley, J., Nei, M. and Kumar, S. (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) Software Version 4.0. Molecular Biology and Evolution, 24, 1596-1599. http://dx.doi.org/10.1093/molbev/msm092

[25]	Toyohara, H. and Makinodan, Y. (1989) Comparison of Calpain I and Calpain II from Carp Muscle. Comparative Biochemistry and Physiology Part B: Comparative Biochemistry, 92, 577-581. http://dx.doi.org/10.1016/0305-0491(89)90134-X

[26]	Salem, M., Nath, J., Rexroad, C.E., Killefer, J. and Yao, J. (2005) Identification and Molecular Characterization of the Rainbow Trout Calpains (Capn1 and Capn2): Their Expression in Muscle Wasting during Starvation. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 140, 63-71. http://dx.doi.org/10.1016/j.cbpc.2004.09.007

[27]	Salem, M., Rexroad, C.E. and Yao, J. (2006) Identification of a Novel Gill-Specific Calpain from Rainbow Trout (Oncorhynchus mykiss). Fish Physiology and Biochemistry, 32, 1-6. http://dx.doi.org/10.1007/s10695-005-0560-2

[28]	Jekely, G. and Friedrich, P. (1999) The Evolution of the Calpain Family as Reflected in Paralogous Chromosome Regions. Journal of Molecular Evolution, 49, 272-281. http://dx.doi.org/10.1007/PL00006549

[29]	Maki, M., Narayana, S.V.L. and Hitomi, K. (1997) A Growing Family of the Ca2+-Binding Proteins with Five EF-Hand Motifs. Biochemical Journal, 328, 718-720.

[30]	Theopold, U., Pinter, M., Daffre, S., Tryselius, Y., Friedrich, P., Nassel, D.R. and Hultmark, D. (1995) CalpA, a Drosophila Calpain Homologue Specifically Expressed in a Small Set of Nerve, Midgut, and Blood Cells. Molecular and Cellular Biology, 15, 824-834.

[31]	Sorimachi, H., Tsukahara, T., Okada-Ban, M., Sugita, H., Ishiura, S. and Suzuki, K. (1995) Identification of a Third Ubiquitous Calpain Species-Chicken Muscle Expresses Four Distinct Calpains. Biochimica et Biophysica Acta (BBA)-Gene Structure and Expression, 1261, 381-393. http://dx.doi.org/10.1016/0167-4781(95)00027-E