Interchromosomal segmental duplications explain the unusual structure of PRSS3, the gene for an inhibitor-resistant trypsinogen

Molecular Biology and Evolution

Volumn 22, Issue 8, 2005, Pages 1712-1720

  Rowen, Lee ^a   Williams, Eleanor ^b   Glusman, Gustavo ^a   Linardopoulou, Elena ^b   Friedman, Cynthia ^b   Ahearn, Mary Ellen ^c   Seto, Jason ^d   Boysen, Cecilie ^e   Qin, Shizhen ^a   Wang, Kai ^f   Kaur, Amardeep ^a   Bloom, Scott ^a   Hood, Leroy ^a   Trask, Barbara J ^b  

^a INSTITUTE FOR SYSTEMS BIOLOGY   (United States)

^b Fred Hutchinson Cancer Research Center   (United States)

^c UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^d GEORGE MASON UNIVERSITY   (United States)

^e ViaLogy ^*  (United States)

^f PhenoGenomics Corporation   (United States)

Author keywords

Fusion gene; Segmental duplication; Selection; Trypsinogen

Indexed keywords

MEMBRANE PROTEIN; MESSENGER RNA; TRYPSINOGEN;

ANIMAL CELL; ARTICLE; BRAIN; CHEMICAL STRUCTURE; CHROMOSOME DUPLICATION; COMPARATIVE STUDY; EXON; FUSION GENE; GENE DUPLICATION; GENE FUNCTION; GENE STRUCTURE; GENETIC TRANSCRIPTION; HOMINID; HUMAN; MOUSE; MULTIGENE FAMILY; NONHUMAN; NUCLEOTIDE SEQUENCE; PANCREAS; PROTEIN EXPRESSION; PROTEIN FUNCTION;

CHROMOSOMES, HUMAN; EVOLUTION, MOLECULAR; EXONS; HUMANS; QUANTITATIVE TRAIT LOCI; SELECTION (GENETICS); TRYPSIN; TRYPSIN INHIBITORS; TRYPSINOGEN;

CERCOPITHECIDAE; HOMINIDAE; HOMO SAPIENS;

EID: 25444511520     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msi166     Document Type: Article

References (51)

1. Bailey, J. A., A. M. Yavor, H. F. Massa, B. J. Trask, and E. E. Eichler. 2001. Segmental duplications: organization and impact within the current human genome project assembly. Genome Res. 11:1005-1017.
2. Charmley, P., S. Wei, and P. Concannon. 1993. Polymorphisms in the Tcrb-V2 gene segments localize the Tcrb orphon genes to human chromosome 9p21. Immunogenetics 38:283-286.
3. Chen, F. C., and W. H. Li. 2001. Genomic divergences between humans and other hominoids and the effective population size of the common ancestor of humans and chimpanzees. Am. J. Hum. Genet. 68:444-456.
4. Chen, J. M., and C. Ferec. 2000. Gene conversion-like missense mutations in the human cationic trypsinogen gene and insights into the molecular evolution of the human trypsinogen family. Mol. Genet. Metab. 71:463-469.
5. Cockell, M., B. J. Stevenson, M. Strubin, O. Hagenbuchle, and P. K. Wellauer. 1989. Identification of a cell-specific DNA-binding activity that interacts with a transcriptional activator of genes expressed in the acinar pancreas. Mol. Cell. Biol. 9:464-476.
6. Cottrell, G. S., S. Amadesi, E. F. Grady, and N. W. Bunnett. 2004. Trypsin IV: a novel agonist of protease-activated receptors 2 and 4. J. Biol. Chem. 279:13532-13539.
7. Craik, C. S., and S. Halfon. 1998. Trypsin. Pp. 12-21 in A. J. Barrett, N. D. Rawlings and J. F. Woessner, eds. Handbook of proteolytic enzymes. Academic Press, London.
8. Daza-Vamenta, R., G. Glusman, L. Rowen, B. Guthrie, and D. Geraghty. 2004. Genetic divergence of the rhesus macaque major histocompatibility complex. Genome Res. 14: 1501-1515.
9. Diederichs, S., E. Bulk, B. Steffen et al. (14 co-authors). 2004. S100 family members and trypsinogens are predictors of distant metastasis and survival in early-state non-small cell lung cancer. Cancer Res. 64:5564-5569.
10. Gaboriaud, C., L. Serre, O. Guy-Crotte, E. Forest, and J.-C. Fontecilla-Camps. 1996. Crystal structure of human trypsin 1: unexpected phosphorylation of Tryp151. J. Mol. Biol. 259:995-1010.
11. Hood, L., L. Rowen, and B. F. Koop. 1995. Human and mouse T-cell receptor loci: genomics, evolution, diversity, and serendipity. Ann. NY Acad. Sci. 758:390-412.
12. Hurles, M. 2004. Gene duplication: the genomic trade in spare parts. PLoS Biol. 2:E206.
13. Jukes, T. H., and C. R. Cantor. 1969. Evolution of protein molecules. Pp. 21-123 in H. N. Munro and J. B. Allison, eds. Mammalian protein metabolism. Academic Press, New York.
14. Kaestner, K. H., C. S. Lee, L. M. Scearce et al. (20 co-authors). 2003. Transcriptional program of the endocrine pancreas in mice and humans. Diabetes 52:1604-1610.
15. Kent, W. J. 2002. BLAT - the BLAST-like alignment tool. Genome Res. 12:656-664.
16. Kitamoto, Y., X. Yuan, Q. Wu, D. W. McCourt, and J. E. Sadler. 1994. Enterokinase, the initiator of intestinal digestion, is a mosaic protease composed of a distinctive assortment of domains. Proc. Natl. Acad. Sci. USA 91:7588-7592.
17. Krapp, A., M. Knofler, S. Frutiger, G. J. Hughes, O. Hagenbuchle, and P. K. Wellauer. 1996. The p48 DNA-binding subunit of transcription factor PTF1 is a new exocrine pancreas-specific basic helix-loop-helix protein. EMBO J. 15:4317-4329.
18. Minn, A., M. Schubert, W. F. Neiss, and B. Muller-Hill. 1998. Enhanced GFAP expression in astrocytes of transgenic mice expressing the human brain-specific trypsinogen IV. Glia 22:338-47.
19. Miyata, S., N. Koshikawa, H. Yasumitsu, and K. Miyazaki. 2000. Trypsin stimulates integrin alpha(5)beta(1)-dependent adhesion to fibronectin and proliferation of human gastric carcinoma cells through activation of proteinase-activated receptor-2. J. Biol. Chem. 275:4592-4598.
20. Molloy, S. S., P. A. Bresnahan, S. H. Leppla, K. R. Klimpel, and G. Thomas. 1992. Human furin is a calcium-dependent serine endoprotease that recognizes the sequence Arg-X-X-Arg and efficiently cleaves anthrax toxin protective antigen. J. Biol. Chem. 267:16396-16402.
21. Nyaruhucha, C. N. M., M. Kito, S.-I. Fukuoka. 1997. Identification and expression of the cDNA-encoding human mesotrypsin(ogen), an isoform of trypsin with inhibitor resistance. J. Biol. Chem. 272:10573-10578.
22. Rinderknecht, H., I. G. Renner, S. B. Abramson, and C. Carmack. 1984. Mesotrypsin: a new inhibitor-resistant protease from a zymogen in human pancreatic tissue and fluid. Gastroenterology 86:681-692.
23. Roach, J. C., K. Wang, L. Gan, and L. Hood. 1997. The molecular evolution of the vertebrate trypsinogens. J. Mol. Evol. 45:640-652.
24. Robinson, M. A., M. P. Mitchell, S. Wei, C. E. Day, T. M. Zhao, and P. Concannon. 1993. Organization of human T-cell receptor beta-chain genes: clusters of V beta genes are present on chromosomes 7 and 9. Proc. Natl. Acad. Sci. USA 90: 2433-2437.
25. Rowen, L., B. F. Koop, and L. Hood. 1996. The complete 685-kilobase DNA sequence of the human beta T cell receptor locus. Science 272:1755-1762.
26. Rowen, L., S. Lasky, and L. Hood. 1999. Deciphering genomes through automated large-scale sequencing. Methods Microbiol. 28:155-192.
27. Sawyer, S. 1989. Statistical tests for detecting gene conversion. Mol. Biol. Evol. 6:526-538.
28. Scheele, G., D. Bartelt, and W. Bieger. 1981. Characterization of human exocrine pancreatic proteins by two-dimensional isoelectric focusing/sodium dodecyl sulfate gel electrophoresis. Gastroenterology 80:461-473.
29. Seboun, E., M. A. Robinson, T. J. Kindt, and S. L. Hauser. 1989. Insertion/deletion-related polymorphisms in the human T cell receptor beta gene complex. J. Exp. Med. 170:263-270.
30. Smit, A. F. A., R. Hubley, and P. Green. 1996-2004. Repeat-Masker Open-3.0. http://www.repeatmasker.org.
31. Stevenson, B. J., O. Hagenbuchle, and P. K. Wellauer. 1986. Sequence organisation and transcriptional regulation of the mouse elastase II and trypsin genes. Nucleic Acids Res. 14:8307-8330.
32. Strachan, T., and A. P. Read. 1999. Human molecular genetics 2. 2nd edition. John Wiley & Sons. New York.
33. Suzuki, Y., and T. Gojobori. 1999. A method for detecting positive selection at single amino acid sites. Mol. Biol. Evol. 16:1315-1328.
34. Suzuki, Y., T. Gojobori, and M. Nei. 2001. ADAPTSITE: detecting natural selection at single amino acid sites. Bioinformatics 17:660-661.
35. Suzuki, Y., and M. Nei. 2004. False-positive selection identified by ML-based methods: examples from the Sig1 gene of the diatom Thalassiosira weissflogii and the tax gene of a human T-cell lymphotropic virus. Mol. Biol. Evol. 21:914-921.
36. Swofford, D. L. 2003. PAUP*: phylogenetic analysis using parsimony (*and other methods). Version 4. Sinauer Associates, Sunderland, Mass.
37. Szmola, R., Z. Kukor, and M. Sahin-Toth. 2003. Human mesotrypsin is a unique digestive protease specialized for the degradation of trypsin inhibitors. J. Biol. Chem. 278:8580-8589.
38. Takezaki, N., A. Rzhetsky, and M. Nei. 1995. Phylogenetic test of the molecular clock and linearized trees. Mol. Biol. Evol. 12:823-833.
39. Tatusova, T. A., and T. L. Madden. 1999. BLAST 2 sequences, a new tool for comparing protein and nucleotide sequences. FEMS Microbiol. Lett. 174:247-250.
40. Thompson, J. D., D. G. Higgins, and T. J. Gibson. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680.
41. Trask, B. 1999. Fluorescence in situ hybridization. Pp. 303-413 in B. Birren, E. D. Green, P. Hieter, S. Klapholz, R. M. Myers, H. Riethman, and J. Roskams, eds. Genome analysis: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
42. Wang, K., L. Gan, I. Lee, and L. Hood. 1995. Isolation and characterization of the chicken trypsinogen gene family. Biochem. J. 307:471-479.
43. Whitcomb, D. C., M. C. Gorry, R. A. Preston et al. (15 co-authors). 1996. Hereditary pancreatitis is caused by a mutation in the cationic trypsinogen gene. Nat. Genet. 14:141-145.
44. Wiegand, U., S. Corbach, A. Minn, J. Kang, and B. Muller-Hill. 1993. Cloning of the cDNA encoding human brain trypsinogen and characterization of its product. Gene 136:167-175.
45. Wong, W. S. W., Z. Yang, N. Goldman, and R. Nielsen. 2004. Accuracy and power of statistical methods for detecting adaptive evolution in protein coding sequences and for identifying positively selected sites. Genetics 168:1041-1051.
46. Yamamoto, H., S. Iku, Y. Adachi et al. (11 co-authors). 2003. Association of trypsin expression with tumour progression and matryilysin expression in human colorectal cancer. J. Pathol. 199:176-184.
47. Yang, Z. 1997. PAML: a program package for phylogenetic analysis by maximum likelihood. CABIOS 13:555-556.
48. Yang, Z., and R. Nielsen. 2000. Estimating synonymous and non-synonymous substitution rates under realistic evolutionary models. Mol. Biol. Evol. 17:32-43.
49. Yang, Z., R. Nielsen, N. Goldman, and A. K. Pedersen. 2000. Codon-subsitution models for heterogeneous selection pressure at amino acid sites. Genetics 155:431-449.
50. Yang, Z., W. S. W. Wong, and R. Nielsen. 2005. Bayes Empirical Bayes inference of amino acid sites under positive selection. Mol. Biol. Evol. 22:1107-1118.
51. Yi, S., D. L. Ellsworth, and W. H. Li. 2002. Slow molecular clocks in Old World monkeys, apes, and humans. Mol. Biol. Evol. 19:2191-2198.