Lineage-specific duplication and loss of pepsinogen genes in hominoid evolution

Journal of Molecular Evolution

Volumn 70, Issue 4, 2010, Pages 313-324

  Narita, Yuichi ^a,d   Oda, Sen Ichi ^b   Takenaka, Osamu ^c   Kageyama, Takashi ^a  

^a KYOTO UNIVERSITY   (Japan)

^b NAGOYA UNIVERSITY   (Japan)

^c KYOTO UNIVERSITY   (Japan)

^d FRIEDRICH MIESCHER INSTITUTE FOR BIOMEDICAL RESEARCH   (Switzerland)

Author keywords

Gene duplication; Hominoid; Orangutan; Pepsinogen; Positive selection

Indexed keywords

COMPLEMENTARY DNA; PEPSINOGEN;

AMINO ACID SEQUENCE; ANIMAL; ARTICLE; BIOLOGICAL MODEL; CHEMISTRY; CLUSTER ANALYSIS; GENE DUPLICATION; GENETICS; HUMAN; MOLECULAR EVOLUTION; MOLECULAR GENETICS; ORANG UTAN; PHYLOGENY; SEQUENCE ALIGNMENT;

AMINO ACID SEQUENCE; ANIMALS; CLUSTER ANALYSIS; DNA, COMPLEMENTARY; EVOLUTION, MOLECULAR; GENE DUPLICATION; HUMANS; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; PEPSINOGEN A; PHYLOGENY; PONGO PYGMAEUS; SEQUENCE ALIGNMENT;

HOMINOIDEA; HOMO; MAMMALIA; PAN; PONGO PYGMAEUS; PRIMATES;

EID: 77954460188     PISSN: 00222844     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00239-010-9320-8     Document Type: Article

References (54)

1. Athauda SB, Tanji M, Kageyama T, Takahashi K (1989) A comparative study on the NH2-terminal amino acid sequences and some other properties of six isozymic forms of human pepsinogens and pepsins. J Biochem 106:920-927
2. Bankowska A, Roszkowska-Jakimiec W, Worowki K (1998) Inhibitors of pepsin, trypsin and chymotrypsin in seeds of plants consumed by humans and animals. I. Evaluation of pepsin, trypsin, and chymotrypsin inhibitors activity in seeds of 26 plant species. Rocz Akad Med Bialymst 43:278-286
3. Borrelli L, De Stasio R, Filosa S, Parisi E, Riggio M, Scudiero R, Trinchella F (2006) Evolutionary fate of duplicate genes encoding aspartic proteinases. Nothepsin case study. Gene 368:101-109
4. Carginale V, Trinchella F, Capasso C, Scudiero R, Riggio M, Parisi E (2004) Adaptive evolution and functional divergence of pepsin gene family. Gene 333:81-90
5. Chirgwin JM, Przybyla AE, MacDonald RJ, Rutter WJ (1979) Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry 18:5294-5299
6. Christeller JT, Farley PC, Ramsay RJ, Sullivan PA, Laing WA (1998) Purification, characterization and cloning of an aspartic protein-ase inhibitor from squash phloem exudate. Eur J Biochem 254:160-167
7. Cottrell TJ, Harris LJ, Tanaka T, Yada RY (1995) The sole lysine residue in porcine pepsin works as a key residue for catalysis and conformational flexibility. J Biol Chem 270:19974-19978
8. Dumas L, Kim YH, Karimpour-Fard A, Cox M, Hopkins J, Pollack JR, Sikela JM (2007) Gene copy number variation spanning 60 million years of human and primate evolution. Genome Res 17:1266-1277
9. Evers MP, Zelle B, Bebelman JP, van Beusechem V, Kraakman L, Hoffer MJ, Pronk JC, Mager WH, Planta RJ, Eriksson AW, Frants RR (1989) Nucleotide sequence comparison of five human pepsinogen A (PGA) genes: evolution of the PGA multigene family. Genomics 4:232-239
10. Feng S, Li W, Lin H (2008) Characterization and expression of the pepsinogen C gene and determination of pepsin-like enzyme activity from orange-spotted grouper (Epinephelus coioides). Comp Biochem Physiol B Biochem Mol Biol 149:275-284
11. Finch CE, Stanford CB (2004) Meat-adaptive genes and the evolution of slower aging in humans. Q Rev Biol 79:3-50
12. Foltmann B (1981) Gastric proteinases\structure, function, evolution and mechanism of action. Essays Biochem 17:52-84
13. Foltmann B (1992) Chymosin: a short review on foetal and neonatal gastric proteases. Scand J Clin Lab Invest 52(Suppl. 210):65-79
14. Fortna A, Kim Y, MacLaren E, Marshall K, Hahn G, Meltesen L, Brenton M, Hink R, Burgers S, Hernandez-Boussard T, Karim-pour-Fard A, Glueck D, McGavran L, Berry R, Pollack J, Sikela JM (2004) Lineage-specific gene duplication and loss in human and great ape evolution. PLoS Biol 2:E207
15. Frazer KA, Chen X, Hinds DA, Pant PV, Patil N, Cox DR (2003) Genomic DNA insertions and deletions occur frequently between humans and nonhuman primates. Genome Res 13: 341-346
16. Galdikas BMF (1988) Orangutan diet, range, and activity at Tanjung Puting, Central Borneo. Int J Primatol 9:1-35
17. Goodman M, Bailey WJ, Hayasaka K, Stanhope MJ, Slightom J, Czelusniak J (1994) Molecular evidence on primate phylogeny from DNA sequences. Am J Phys Anthropol 94:3-24
18. Goodman M, Porter CA, Czelusniak J, Page SL, Schneider H, Shoshani J, Gunnell G, Groves CP (1998) Toward a phyloge-netic classification of primates based on DNA evidence complemented by fossil evidence. Mol Phylogenet Evol 9: 585-598
19. Gubler U, Hoffman BJ (1983) A simple and very efficient method for generating cDNA libraries. Gene 25:263-269
20. Harding RSO (1981) An order of omnivores: nonhuman primate diets in the wild. In: Harding RSO, Teleki G (eds) Omnivorous primates. Columbia University Press, New York, pp 191-214
21. Hasegawa M, Kishino H, Yano T (1985) Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22:160-174
22. Kageyama T (2000) New world monkey pepsinogens A and C, and prochymosins. Purification, characterization of enzymatic properties, cDNA cloning, and molecular evolution. J Biochem 127:761-770
23. Kageyama T (2002) Pepsinogens, progastricsins, and prochymosins: structure, function, evolution, and development. Cell Mol Life Sci 59:288-306
24. Kageyama T (2004) Role of S'1 loop residues in the substrate specificities of pepsin A and chymosin. Biochemistry 43:15122-15130
25. Kageyama T (2006) Roles of Tyr13 and Phe219 in the unique substrate specificity of pepsin B. Biochemistry 45:14415-14426
26. Kageyama T, Takahashi K (1976) Pepsinogens and pepsins from gastric mucosa of Japanese Monkey. Purification and characterization. J Biochem 79:455-468
27. Kageyama T, Takahashi K (1977) The carbohydrate moiety of Japanese monkey pepsinogens. Its composition and site of attachment to protein. Biochem Biophys Res Commun 74:789-795
28. Kageyama T, Takahashi K (1984) Rabbit pepsinogens. Purification, characterization, analysis of the conversion process to pepsin and determination of the NH2-terminal amino-acid sequences. Eur J Biochem 141:261-269
29. Kageyama T, Tanabe K, Koiwai O (1990) Structure and development of rabbit pepsinogens. Stage-specific zymogens, nucleotide sequences of cDNAs, molecular evolution, and gene expression during development. J Biol Chem 265:17031-17038
30. Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111-120
31. Kishino H, Hasegawa M (1989) Evaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data, and the branching order in hominoidea. J Mol Evol 29:170-179
32. Miyamoto MM, Koop BF, Slightom JL, Goodman M, Tennant MR (1988) Molecular systematics of higher primates: genealogical relations and classification. Proc Natl Acad Sci USA 85:7627-7631
33. Narita Y, Kageyama T (2003) Diversity of ape pepsinogen genes (in Japanese with English summary). Primate Res 19:125-133
34. Narita Y, Oda S, Moriyama A, Takenaka O, Kageyama T (1997) Pepsinogens and pepsins from house musk shrew, Suncus murinus: purification, characterization, determination of the amino-acid sequences of the activation segments, and analysis of proteolytic specificities. J Biochem 121:1010-1017
35. Narita Y, Oda S, Takenaka O, Kageyama T (2000) Multiplicities and some enzymatic characteristics of ape pepsinogens and pepsins. J Med Primatol 29:402-410
36. Narita Y, Oda S, Takenaka O, Kageyama T (2001) Phylogenetic position of Eulipotyphla inferred from the cDNA sequences of pepsinogens A and C. Mol Phylogenet Evol 21:32-42
37. Narita Y, Oda S, Moriyama A, Kageyama T (2002) Primary structure, unique enzymatic properties, and molecular evolution of pepsin-ogen B and pepsin B. Arch Biochem Biophys 404:177-185
38. O'hUigin C, Satta Y, Takahata N, Klein J (2002) Contribution of homoplasy and of ancestral polymorphism to the evolution of genes in anthropoid primates. Mol Biol Evol 19:1501-1513
39. Ordonez GR, Hillier LW, Warren WC, Grutzner F, Lopez-Otin C, Puente XS (2008) Loss of genes implicated in gastric function during platypus evolution. Genome Biol 9:R81
40. Perry GH, Dominy NJ, Claw KG, Lee AS, Fiegler H, Redon R, Werner J, Villanea FA, Mountain JL, Misra R, Carter NP, Lee C, Stone AC (2007) Diet and the evolution of human amylase gene copy number variation. Nat Genet 39:1256-1260 (Pubitemid 47482688)
41. Robinson-Rechavi M, Huchon D (2000) RRTree: relative-rate tests between groups of sequences on a phylogenetic tree. Bioinfor-matics 16:296-297
42. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406-425
43. Sali A, Blundell TL (1993) Comparative protein modelling by satisfaction of spatial restraints. J Mol Biol 234:779-815
44. Samloff IM (1971) Pepsinogens, pepsins, and pepsin inhibitors. Gastroenterology 60:586-604
45. Schoniger M, von Haeseler A (1994) A stochastic model for the evolution of autocorrelated DNA sequences. Mol Phylogenet Evol 3:240-247
46. Steiper ME, Young NM (2006) Primate molecular divergence dates. Mol Phylogenet Evol 41:384-394
47. Strimmer K, von Haeseler M (1996) Quartet puzzling: a quartet maximum-likelihood method for reconstructing tree topologies. Mol Biol Evol 13:964-969
48. Suchodolski JS, Steiner JM, Ruaux CG, Boari A, Williams DA (2002) Purification and partial characterization of canine pepsinogen A and B. Am J Vet Res 63:1585-1590
49. Swofford DL (1998) PAUP*. Phylogenetic analysis using parsimony and other methods. Sinauer Associates
50. Sunderland, MA Tang J, Sepulveda P, Marciniszyn J Jr, Chen KC, Huang WY, Tao N, Liu D, Lanier JP (1973) Amino-acid sequence of porcine pepsin. Proc Natl Acad Sci USA 70:3437-3439
51. Yang Z (1998) Likelihood ratio tests for detecting positive selection and application to primate lysozyme evolution. Mol Biol Evol 15:568-573
52. Yang Z (2007) PAML 4: a phylogenetic analysis by maximum likelihood. Mol Biol Evol 24:1586-1591
53. Yang Z, Nielsen R (1998) Synonymous and nonsynonymous rate variation in nuclear genes of mammals. J Mol Evol 46:409-418
54. Zelle B, Evers MP, Groot PC, Bebelman JP, Mager WH, Planta RJ, Pronk JC, Meuwissen SG, Hofker MH, Eriksson AW, Frants RR (1988) Genomic structure and evolution of the human pepsin-ogen A multigene family. Hum Genet 78:79-82