Single nucleotide polymorphisms in several porcine cathepsin genes are associated with growth, carcass, and production traits in Italian Large White pigs

Journal of Animal Science

Volumn 86, Issue 12, 2008, Pages 3300-3314

  Russo, V ^a   Fontanesi, L ^a   Scotti, E ^a   Beretti, F ^a   Davoli, R ^a   Nanni Costa, L ^a   Virgili, R ^b   Buttazzoni, L ^c  

^a UNIVERSITY OF BOLOGNA   (Italy)

^b Stazione Sperimentale per 1'Industria delle Conserve Alimentari ^*  (Italy)

^c Associazione Nazionale Allevatori Suini   (Italy)

Author keywords

Candidate gene; Cathepsin; Cystatin; Meat production; Pig; Single nucleotide polymorphism

Indexed keywords

ANIMALIA; HUMAN HERPESVIRUS 4; PIERIS BRASSICAE; SUIDAE; SUS;

CATHEPSIN;

ANIMAL; ARTICLE; CHROMOSOME MAP; FEMALE; GENE FREQUENCY; GENETIC MARKER; GENETICS; GROWTH, DEVELOPMENT AND AGING; MALE; MEAT; MISSENSE MUTATION; PHYSIOLOGY; SINGLE NUCLEOTIDE POLYMORPHISM; STANDARD; SWINE;

ANIMALS; CATHEPSINS; CHROMOSOME MAPPING; FEMALE; GENE FREQUENCY; GENETIC MARKERS; MALE; MEAT; MUTATION, MISSENSE; POLYMORPHISM, SINGLE NUCLEOTIDE; SWINE;

EID: 58749089294     PISSN: 00218812     EISSN: 15253163     Source Type: Journal    
DOI: 10.2527/jas.2008-0920     Document Type: Article

References (79)

1. Abrahamson, M., M. Alvarez-Fernandez, and C. M. Nathanson. 2003. Cystatins. Biochem. Soc. Symp. 70:179-199.
2. Archibald, A. L., C. S. Haley, J. F. Brown, S. Couperwhite, H. A. McQueen, D. Nicolson, W. Coppieters, A. Van de Weghe, A. Stratil, A. K. Wintero, M. Fredholm, N. Larson, V. Nielsen, D. Milan, N. Olosyzyn, A. Robic, M. Dalens, J. Riquet, J. Gellin, J. C. Caritez, D. Hue, G. Burgaud, L. Ollivier, J. P. Bidanel, M. Aimau, C. Renard, H. Geldermann, R. Davoli, D. Ruyter, E. Vesterge, M. Groenen, W. Davis, B. Hoyheim, A. Keisereud, L. Andersson, H. Ellegren, M. Johansson, L. Marklund, M. Rothschild, C. Tuggle, D. Vaske, J. Helm, H. C. Liu, A. Rahaman, T. P. Yu, R. G. Larson, and C. Schmitz. 1995. The PiGMaP consortium linkage map of the pig (Sus scrofa). Mamm. Genome 6:157-175.
3. Bagnato, A., F. Schiavini, A. Rossoni, C. Maltecca, M. Dolezal, I. Medugorac, J. Sölkner, V. Russo, L. Fontanesi, A. Friedmann, M. Soller, and E. Lipkin. 2008. Quantitative trait loci affecting milk yield and protein percentage in a three-country Brown Swiss population. J. Dairy Sci. 91:767-783.
4. Barrett, A. J., N. D. Rawlings, and J. F. Woessner. 1998. Handbook of Proteolytic Enzymes. Academic Press, London, UK.
5. Barros, N. M., L. Puzer, I. L. Tersariol, M. L. Oliva, C. A. Sampaio, A. K. Carmona, and G. da Motta. 2004. Plasma prekallikrein/kallikrein processing by lysosomal cysteine proteases. Biol. Chem. 385:1087-1091.
6. Bidanel, J. P., D. Milan, N. Iannuccelli, Y. Amigues, M. Y. Boscher, F. Bourgeois, J. C. Caritez, J. Gruand, P. Le Roy, H. Lagant, R. Quintanilla, C. Renard, J. Gellin, L. Ollivier, and C. Chevalet. 2001. Detection of quantitative trait loci for growth and fatness in pigs. Genet. Sel. Evol. 33:289-309.
7. Bosi, P., and V. Russo. 2004. The production of the heavy pig for high quality processed products. Ital. J. Anim. Sci. 3:309-321.
8. Brix, K., A. Dunkhorst, K. Mayer, and S. Jordans. 2008. Cysteine cathepsins: Cellular roadmap to different functions. Biochimie 90:194-207.
9. Brix, K., M. Linke, C. Tepel, and V. Herzog. 2001. Cysteine proteinases mediate extracellular prohormone processing in the thyroid. Biol. Chem. 382:717-725.
10. Brunham, L. R., R. R. Singaraja, T. D. Pape, A. Kejariwal, P. D. Thomas, and M. R. Hayden. 2005. Accurate prediction of the functional significance of single nucleotide polymorphisms and mutations in the ABCA1 gene. PLoS Genet. 1:e83.
11. Davoli, R., L. Fontanesi, S. Braglia, I. Nisi, E. Scotti, L. Buttazzoni, and V. Russo. 2006. Investigation of SNPs in the ATP1A2, CAS and DECRl genes mapped to porcine chromosome 4: analysis in groups of pigs divergent for meat production and quality traits. Ital. J. Anim. Sci. 5:249-263.
12. de Koning, D. J., L. L. Janss, A. P. Rattink, P. A. van Oers, B. J. de Vries, M. A. Groenen, J. J. van der Poel, P. N. de Groot, E. W. Brascamp, and J. A. van Arendonk. 1999. Detection of quantitative trait loci for backfat thickness and intramuscular fat content in pigs (Sus scrofa). Genetics 152:1679-1690.
13. de Vries, A. G., A. Sosnicki, J. P. Gamier, and G. S. Plastow. 1998. The role of major genes and DNA technology in selection for meat quality in pigs. Meat Sci. 49(Suppl.1):S245-S255.
14. Dragos-Wendrich, M., I. Sternstein, C. Bruusch, G. Moser, H. Bartenschlager, G. Reiner, and H. Geldermann. 2003. Linkage and QTL mapping for Sus scrofa chromosome 14. J. Anim. Breed. Genet. 120(Suppl. 1):111-118.
15. Dunn, A. D., H. E. Crutchfield, and J. T. Dunn. 1991. Thyroglobulin processing by thyroidal proteases. Major sites of cleavage by cathepsins B, D, and L. J. Biol. Chem. 266:20198-20204.
16. Fernando, R. L., D. Nettleton, B. R. Southey, J. C. Dekkers, M. F. Rothschild, and M. Soller. 2004. Controlling the proportion of false positives in multiple dependent tests. Genetics 166:611-619.
17. Fontanesi, L., R. Davoli, J. Mile, and V. Russo. 2001a. The porcine sarcolipin (SLN) gene: Identification of an SNP and linkage mapping to chromosome 9. Anim. Genet. 32:109-110.
18. Fontanesi, L., R. Davoli, M. Yerle, C. Zijlstra, A. A. Bosma, and V. Russo. 2001b. Regional localization of the porcine cathepsin H (CTSH) and cathepsin L (CTSL) genes. Anim. Genet. 32:321-323.
19. Fujii, J., K. Otsu, F. Zorzato, S. de Leon, V. K. Khanna, J. E. Weiler, P. J. O'Brien, and D. H. MacLennan. 1991. Identification of a mutation in porcine ryanodine receptor associated with malignant hyperthermia. Science 253:448-451.
20. Garcia-Garrido, J. A., R. Quiles-Zafra, J. Tapiador, and M. D. Luque de Castro. 2000. Activity of cathepsin B, D, H and L in Spanish dry-cured ham of normal and defective texture. Meat Sci. 56:1-6.
21. Gilbert, H., P. Le Roy, D. Milan, and J. P. Bidanel. 2007. Linked and pleiotropic QTLs influencing carcass composition traits detected on porcine chromosome 7. Genet. Res. 89:65-72.
22. Green, P., K. Falls, and S. Crooks. 1990. Documentation for CRIMAP, Version 2.4. Washington University School of Medicine, St Louis, MO.
23. Hayes, B. J., K. Nielsen, P. R. Berg, E. Grindflek, and S. Lien. 2007. SNP detection exploiting multiple sources of redundancy in large EST collections improves validation rates. Bioinformatics 23:1692-1693.
24. Hook, V., S. Yasothornsrikul, D. Greenbaum, K. F. Medzihradszky, K. Troutner, T. Toneff, R. Bundey, A. Logrinova, T. Reinheckel, C. Peters, and M. Bogyo. 2004. Cathepsin L and Arg/Lys aminopeptidase: A distinct prohormone processing pathway for the biosynthesis of peptide neurotransmitters and hormones. Biol. Chem. 385:473-480.
25. Houston, R. D., C. S. Haley, A. L. Archibald, and K. A. Rance. 2005. A QTL affecting daily feed intake maps to chromosome 2 in pigs. Mamm. Genome 16:464-470.
26. Jeon, J.-T., Ö. Carlborg, A. Törusten, E. Giuffra, V. Amarger, P. Chardon, L. Andersson-Eklund, K. Andersson, I. Hansson, K. Lundstöm, and L. Andersson. 1999. A paternally expressed QTL affecting skeletal and cardiac muscle mass in pigs maps to the IGF2 locus. Nat. Genet. 21:157-158.
27. Jungerius, B. J., A. S. van Laere, M. F. Te Pas, B. A. van Oost, L. Andersson, and M. A. Groenen. 2004. The IGF2-intron3-G3072A substitution explains a major imprinted QTL effect on backfat thickness in a Meishan x European white pig intercross. Genet. Res. 84:95-101.
28. Kim, C. W., Y. H. Hong, S. -I. Yun, S. -R. Lee, Y. H. Kim, M.-S. Kim, K. H. Chung, W. Y. Jung, E. J. Kwon, S. S. Hwang, D. H. Park, K. K. Cho, J. G. Lee, B. W. Kim, J. W. Kim, Y. S. Kang, J. S. Yeo, and K.-T. Chang. 2006. Use of microsatellite markers to detect quantitative trait loci in Yorkshire pigs. J. Reprod. Dev. 52:229-237.
29. Knott, S. A., L. Marklund, C. S. Haley, K. Andersson, W. Davies, H. Ellegren, M. Fredholm, I. Hansson, B. Hoyheim, K. Lundström, M. Moller, and L. Andersson. 1998. Multiple marker mapping of quantitative trait loci in a cross between outbred wild boar and Large White pigs. Genetics 149:1069-1080.
30. Lee, H. K., J. C. M. Dekkers, M. Soller, M. Malek, R. L. Fernando, and M. F. Rothschild. 2002. Application of the false discovery rate to QTL interval mapping with multiple traits. Genetics 161:905-914.
31. Lee, S. S., Y. Chen, C. Moran, S. Cepica, G. Reiner, H. Bartenschlager, G. Moser, and H. Geldermann. 2003. Linkage and QTL mapping for Sus scrofa chromosome 2. J. Anim. Breed. Genet. 120(Suppl. 1):11-19.
32. Lenarčič, B., I. Križč, P. Žunec, and V. Turk. 1996. Differences in specificity for the interactions of stefins A, B and D with cysteine proteinases. FEBS Lett. 395:113-118.
33. Lenney, J. F., J. R. Tolan, W. J. Sugai, and A. G. Lee. 1979. Thermostable endogenous inhibitors of cathepsins B and H. Eur. J. Biochem. 101:153-161.
34. Malek, M., J. C. M. Dekkers, H. K. Lee, T. J. Baas, K. Prusa, E. Huff-Lonergan, and M. F. Rothschild. 2001a. A molecular genome scan analysis to identify chromosomal regions influencing economic traits in the pig. II. Meat and muscle composition. Mamm. Genome 12:637-645.
35. Malek, M., J. C. M. Dekkers, H. K. Lee, T. J. Baas, and M. F. Rothschild. 2001b. A molecular genome scan analysis to identify chromosomal regions influencing economic traits in the pig. I. Growth and body composition. Mamm. Genome 12:630-636.
36. Mohamed, M. M., and B. F. Sloane. 2006. Cysteine cathepsins: Multifunctional enzymes in cancer. Nat. Rev. Cancer 6:764-775.
37. Monin, G., A. Mejenes-Quijano, A. Talmant, and P. Sellier. 1987. Influence of breed and muscle metabolic type on muscle glycolytic potential and meat pH in pigs. Meat Sci. 20:149-158.
38. Monin, G., and P. Sellier. 1985. Pork of low technological quality with a normal rate of muscle pH fall in the immediate postmortem period: The case of the Hampshire breed. Meat Sci. 13:49-63.
39. Nanni Costa, L., F. Tassone, R. Davoli, L. Fontanesi, S. Dall'Olio, M. Colombo, and V. Russo. 2008. Glycolytic potential in semimembranosus muscle of Italian Large White pigs. J. Muscle Foods . In press.
40. Nezer, C., L. Moreau, B. Brouwers, W. Coppieters, J. Detilleux, R. Hanset, L. Karim, A. Kvasz, P. Leroy, and M. Georges. 1999. An imprinted QTL with major effect on muscle mass and fat deposition maps to the IGF2 locus in pigs. Nat. Genet. 21:155-156.
41. Nezer, C., L. Moreau, D. Wagenaar, and M. Georges. 2002. Results of a whole genome scan targeting QTL for growth and carcass traits in a Piétrain x Large White intercross. Genet. Sel. Evol. 34:371-387.
42. 2 pig population. J. Anim. Sci. 80:2801-2808.
43. Parolari, G., R. Virgili, and C. Schivazappa. 1994. Relationship between cathepsin B activity and compositional parameters in dry-cured hams of normal and defective texture. Meat Sci. 38:117-122.
44. Parreño, M., R. Cussó, M. Gil, and C. Sárraga. 1994. Development of cathepsin B, L and H activities and cystatin-like activity during two different manufacturing processes for Spanish dry-cured ham. Food Chem. 49:15-21.
45. Paszek, A. A., P. J. Wilkie, G. H. Flickinger, L. M. Miller, C. F. Louis, G. A. Rohrer, L. J. Alexander, C. W. Beattie, and L. B. Schook. 2001. Interval mapping of carcass and meat quality traits in a divergent swine cross. Anim. Biotechnol. 12:155-165.
46. Pierzchala, M., D. Cieslak, G. Reiner, H. Bartenschlager, G. Moser, and H. Geldermann. 2003. Linkage and QTL mapping for Sus seroja chromosome 17. J. Anim. Breed. Genet. 120(Suppl. 1):132-137.
47. Ramos, A. M., K. L. Glenn, T. V. Serenius, K. J. Stalder, and M. F. Rothschild. 2008. Genetic markers for the production of US country hams. J. Anim. Breed. Genet. 125:1-10.
48. Ramos, A. M., J. Helm, J. Sherwood, D. Rocha, and M. F. Rothschild. 2006. Mapping of 21 genetic markers to a QTL region for meat quality on pig chromosome 17. Anim. Genet. 37:296-297.
49. Reiner, G., L. Heinricy, E. Müller, H. Geldermann, and V. Dzapo. 2002. Indications of associations of the porcine FOS proto-oncogene with skeletal muscle fibre traits. Anim. Genet. 33:49-55.
50. Rink, A., K. Eyer, B. Roelofs, K. J. Priest, K. J. Sharkey-Brockmeier, S. Lekhong, E. K. Karajusuf, J. Bang, M. Yerle, D. Milan, W. S. Liu, and C. W. Beattie. 2006. Radiation hybrid map of the porcine genome comprising 2035 EST loci. Mamm. Genome 17:878-885.
51. Rohrer, G. A., and J. W. Keele. 1998a. Identification of quantitative trait loci affecting carcass composition in swine: I. Fat deposition traits. J. Anim. Sci. 76:2247-2254.
52. Rohrer, G. A., and J. W. Keele. 1998b. Identification of quantitative trait loci affecting carcass composition in swine: II. Muscling and wholesale product yield traits. J. Anim. Sci. 76:2255-2262.
53. 2 population. Anim. Genet. 37:17-27.
54. Rothschild, M. F., H. C. Liu, C. K. Tuggle, T. P. Yu, and L. Wang. 1995. Analysis of pig chromosome 7 genetic markers for growth and carcass performance traits. J. Anim. Breed. Genet. 112:341-348.
55. Russo, V., L. Buttazzoni, C. Baiocco, R. Davoli, L. Nanni Costa, C. Schivazappa, and R. Virgili. 2000. Heritability of muscular cathepsin B activity in Italian Large White pigs. J. Anim. Breed. Genet. 117:37-42.
56. Russo, V., R. Davoli, L. Nanni Costa, L. Fontanesi, C. Baiocco, L. Buttazzoni, S. Galli, and R. Virgili. 2003. Association of the CTSB, CTSF and CSTB genes with growth, carcass and meat quality traits in heavy pigs. Ital. J. Anim. Sci. 2(Suppl. 1):67-69.
57. Russo, V., R. Davoli, J. Tagliavini, J. S. Dall'Olio, D. Bigi, E. Costosi, and L. Fontanesi. 1993. Identificazione del genotipo dei suini per la sensibilità all'alotano a livello di DNA mediante PCR. Zoot. Nutr. Anim. 19:89-93.
58. Russo, V., L. Fontanesi, R. Davoli, and S. Galli. 2004. Linkage mapping of the porcine cathepsin F ( CTSF) gene close to the QTL regions for meat and fat deposition traits on pig chromosome 2. Anim. Genet. 35:155-157.
59. Russo, V., L. Fontanesi, R. Davoli, L. Nanni Costa, M. Cagnazzo, L. Buttazzoni, R. Virgili, and M. Yerle. 2002. Investigation of candidate genes for meat quality in dry-cured ham production: The porcine cathepsin B (CTSB) and cystatin B (CSTB) genes. Anim. Genet. 33:123-131.
60. Russo, V., and L. Nanni Costa. 1995. Suitability of pig meat for salting and the production of quality processed products. Pig News Inform. 16:7N-26N.
61. Sanchez, M. P., J. Riquet, N. Iannuccelli, J. Gogué, Y. Billon, O. Demeure, J. C. Caritez, G. Burgaud, K. Fève, M. Bonnet, C. Péry, H. Lagant, P. Le Roy, J. P. Bidanel, and D. Milan. 2006. Effects of quantitative trait loci on chromosomes 1, 2, 4, and 7 on growth, carcass, and meat quality traits in backcross Meishan x Large White pigs. J. Anim. Sci. 84:526-537.
62. Sellier, P. 1998. Genetics of meat and carcass traits. Pages 463-510 in The Genetics of the Pig. M. F. Rothschild and A. Ruvinski, ed. CAB International, Oxon, UK.
63. 2 and sib-pair analyses. J. Anim. Sci. 83:1481-1493.
64. Stephens, M., N. J. Smith, and P. Donnelly. 2001. A new statistical method for haplotype reconstruction from population data. Am. J. Hum. Genet. 68:978-989.
65. Stoka, V., V. Turk, and B. Turk. 2007. Lysosomal cysteine cathepsins: Signaling pathways in apoptosis. Biol. Chem. 388:555-560.
66. Thomas, P. D., M. J. Campbell, A. Kejariwal, H. Mi, B. Karlak, R. Daverman, K. Diemer, A. Muruganujan, and A. Narechania. 2003. PANTHER: A library of protein families and subfamilies indexed by function. Genome Res. 13:2129-2141.
67. Thomas, P. D., and A. Kejariwal. 2004. Coding single-nucleotide polymorphisms associated with complex vs. Mendelian disease: Evolutionary evidence for differences in molecular effects. Proc. Natl. Acad. Sci. USA 101:15398-15403.
68. Thomseu, H., H. K. Lee, M. F. Rothschild, M. Malek, and J. C. M. Dekkers. 2004. Characterization of quantitative trait loci for growth and meat quality in a cross between commercial breeds of swine. J. Anim. Sci. 82:2213-2228.
69. Toldrá, F., and D. J. Etherington. 1988. Examination of cathepsin B, D, H and L activities in dry-cured hams. Meat Sci. 23:1-7.
70. Turk, V., and W. Bode. 1991. The cystatins: Protein inhibitors of cysteine proteinases. FEBS Lett. 2:213-219.
71. Van Laere, A.-S., M. Nguyen, M. Braunschweig, C. Nezer, C. Collette, L. Moreau, A. L. Archibald, C. S. Haley, N. Buys, M. Tally, G. Andersson, M. Georges, and L. Andersson. 2003. A regulatory mutation in IGF2 causes a major QTL effect on muscle growth in the pig. Nature 425:832-836.
72. Virgili, R., G. Parolari, C. Schivazappa, C. Soresi Bordini, and M. Borri. 1995a. Sensory and texture quality of dry-cured ham as affected by endogenous cathepsin B activity and muscle composition . J. Food Sci. 6:1183-1186.
73. Virgili, R., G. Parolari, C. Schivazappa, C. Soresi Bondini, and R. Volta. 1998. Proteases in fresh pork muscle and their influence on bitter taste formation in dry-cured ham. J. Food Biochem. 22:53-63.
74. Virgili, R., G. Parolari, C. Schivazappa, C. Soresi Bordini, and R. Volta. 1995b. Effects of raw material on proteolysis and texture of typical Parma ham. Ind. Conserve 70:21-31.
75. Virgili, R., and C. Schivazappa. 2002. Muscle traits for long matured dried meats. Meat Sci. 62:331-343.
76. Weller, J. L, J. Z. Song, D. W. Heyen, H. A. Lewin, and M. Ron. 1998. A new approach to the problem of multiple comparisons in the genetic dissection of complex traits. Genetics 150:1699-1706.
77. Yue, G., A. Stratil, S. Cepica, J. Schröffel Jr., D. Schröffelova, L. Fontanesi, M. Cagnazzo, G. Moser, H. Bartenschlager, G. Reiner, and H. Geldermann. 2003. Linkage and QTL mapping for Sus seroja chromosome 7. J. Anim. Breed. Genet. 120(Suppl. 1):56-65.
78. Zavašnik-Bergant, T., and B. Turk. 2006. Cysteine cathepsins in the immune response. Tissue Antigens 67:349-355.
79. Zhao, J. H. 2004. 2LD, GENECOUNTING and HAP: Computer programs for linkage disequilibrium analysis. Bioinformatics 20:1325-1326.