Variability of the IGF2 locus in the Suino Nero Lucano pig population and its effects on meat quality
Amalia Simonetti A , Andrea Rando A , Paola Di Gregorio A , Carmelisa Valluzzi A , Annamaria Perna A B and Emilio Gambacorta A
+ Author Affiliations
- Author Affiliations
A School of Agricultural, Forestry, Food and Environmental Sciences, University of Basilicata, Potenza, Viale dell’Ateneo Lucano 10 – 85100, Italy.
B Corresponding author. Email: anna.perna@unibas.it
Animal Production Science 58(11) 1976-1982 https://doi.org/10.1071/AN17051
Submitted: 30 January 2017 Accepted: 12 May 2017 Published: 30 June 2017
Abstract
The aim of this study was to analyse the polymorphisms in the two promoter regions, P1 and P2, of the porcine Insulin-like Growth Factor 2 (IGF2) gene and to investigate the effect of IGF2 genotypes on meat quality traits in the Italian autochthonous Suino Nero Lucano pig. Three polymorphic sites were analysed and only two of the eight potential haplotypes were observed in the Suino Nero Lucano pig population: A haplotype (–366A – –225G – –182C), and B haplotype (–366G – –225C – –182T). Muscle mass and meat quality characteristics were analysed in 30 castrated pigs (10 for each of the three IGF2 genotypes: A/A, A/B, and B/B). According to the results, B/B animals, at the same carcass weight, showed the highest Longissimus lumborum and Psoas weight (P < 0.05), whereas A/A animals showed a higher intramuscular fat percentage and lower Warner–Bratzler shear force, drip loss, and polyunsaturated fatty acids content. Meat from B/B animals showed also a higher L* value and myoglobin and deoxymyoglobin percentage compared with meat from A/A ones (P < 0.05).
Additional keywords: fatty acid, IGF2 polymorphism, Italian autochthonous pig, meat colour.
References
Affentranger P, Gerwig C, Seewer GJF, Schwörer D, Künzi N (1996) Growth and carcass characteristics as well as meat and fat quality of three types of pigs under different feeding regimes. Livestock Production Science 45, 187–196.| Growth and carcass characteristics as well as meat and fat quality of three types of pigs under different feeding regimes.Crossref | GoogleScholarGoogle Scholar |
Amarger V, Nguyen M, Van Laere A-S, Braunschweig M, Nezer C, Georges M, Andersson L (2002) Comparative sequence analysis of the Insulin-IGF2–H19 gene cluster in pigs. Mammalian Genome 13, 388–398.
| Comparative sequence analysis of the Insulin-IGF2–H19 gene cluster in pigs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xls12nsLo%3D&md5=dddb5bf1b74c78f15e1d18067e098f3aCAS |
AOAC (1995) ‘Official methods of analysis.’ 16th edn. (Association of Official Analytical Chemists: Arlington, VA)
Armand A-S, Lécolle S, Launay T, Pariset C, Fiore F, Della Gaspera B, Birnbaum D, Chanoine C, Charbonnier F (2004) IGF-II is up-regulated and myofibres are hypertrophied in regenerating soleus of mice lacking FGF6. Experimental Cell Research 297, 27–38.
| IGF-II is up-regulated and myofibres are hypertrophied in regenerating soleus of mice lacking FGF6.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXkvVKmsLw%3D&md5=adb1ff297d27ccceedeeb2cefe06cdceCAS |
Aslan O, Hamill RM, Davey G, McBryan J, Mullen AM, Gispert M, Sweeney T (2012) Variation in the IGF2 gene promoter region is associated with intramuscular fat content in porcine skeletal muscle. Molecular Biology Reports 39, 4101–4110.
| Variation in the IGF2 gene promoter region is associated with intramuscular fat content in porcine skeletal muscle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xjt12qtb0%3D&md5=df1b356c9f18f8e05081989b48cce1a8CAS |
Boles JA, Pegg R (2001) Meat color. Montana State University and Saskatchewan Food Product Innovation Program. Available at http://animalrange.montana.edu/ courses/meat/meatcol.pdf [Verified 16 June 2016]
Brown J, Jones EY, Forbes BE (2009) Keeping IGF-II under control: lessons from the IGF-II-IGF2R crystal structure. Trends in Biochemical Sciences 34, 612–619.
| Keeping IGF-II under control: lessons from the IGF-II-IGF2R crystal structure.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsV2hu7rF&md5=7217a5a3b758b80548e51617898d1e39CAS |
Burgos C, Galve A, Moreno C, Altarriba J, Reina R, García C, López-Buesa P (2012) The effects of two alleles of IGF2 on fat content in pig carcasses and pork. Meat Science 90, 309–313.
| The effects of two alleles of IGF2 on fat content in pig carcasses and pork.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsVWktrfE&md5=64ae14eccb096c4bd891e5fa76ba436cCAS |
Carrodeguas JA, Burgos C, Moreno C, Sanchez AC, Ventanas S, Tarrafeta L, Barcelona JA, Lopez MO, Oria R, Lopez-Buesa P (2005) Incidence in diverse pig populations of an IGF2 mutation with potential influence on meat quality and quantity: An assay based on real time PCR (RT-PCR). Meat Science 71, 577–582.
| Incidence in diverse pig populations of an IGF2 mutation with potential influence on meat quality and quantity: An assay based on real time PCR (RT-PCR).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXosVaiurc%3D&md5=038cf9eb9c5954ca9c5371fc65e42e18CAS |
Clark DL (2015) Regulation of skeletal muscle growth and gene expression by insulin-like growth factors and myostatin. Dissertation, University of Illinois at Urbana-Champaign.
De Smet S, Raes K, Demeyer D (2004) Meat fatty acid composition as affected by fatness and genetic factors: a review. Animal Research 53, 81–98.
| Meat fatty acid composition as affected by fatness and genetic factors: a review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXltFymtrs%3D&md5=6e4b7d79c9cf911f9704fa11df1ac7e8CAS |
Denley A, Cosgrove LJ, Booker GW, Wallace JC, Forbes BE (2005) Molecular interactions of the IGF system. Cytokine & Growth Factor Reviews 16, 421–439.
| Molecular interactions of the IGF system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmvVCnu7o%3D&md5=3695f17198c5365d274e90e1b9145cf3CAS |
Devaney JM, Hoffman EP, Gordish-Dressman H, Kearns A, Zambraski E, Clarkson PM (2007) IGF-II gene region polymorphisms related to exertional muscle damage. Journal of Applied Physiology 102, 1815–1823.
| IGF-II gene region polymorphisms related to exertional muscle damage.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmt1aqs7s%3D&md5=8fa3d7f380bb00d74e713685c7cea23cCAS |
Duan C, Ren H, Gao S (2010) Insulin-like growth factors (IGFs), IGF receptors, and IGF-binding proteins: Roles in skeletal muscle growth and differentiation. General and Comparative Endocrinology 167, 344–351.
| Insulin-like growth factors (IGFs), IGF receptors, and IGF-binding proteins: Roles in skeletal muscle growth and differentiation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXmslOhsb8%3D&md5=bc88e1871f7a0b9b590dc0fc20ce458bCAS |
Faustman C, Sun Q, Mancini R, Suman SP (2010) Myoglobin and lipid oxidation interactions: Mechanistic bases and control. Meat Science 86, 86–94.
| Myoglobin and lipid oxidation interactions: Mechanistic bases and control.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXos1Cntrk%3D&md5=bd9d6fedc37cd3913108fb9fe2de6bacCAS |
Fernandez X, Monin G, Talmant A, Mourot J, Lebret B (1999) Influence of intramuscular fat content on the quality of pig meat. Meat Science 53, 67–72.
| Influence of intramuscular fat content on the quality of pig meat.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3MbnsFentg%3D%3D&md5=260a3f390c98d65415e5e7a78838bb81CAS |
Florini JR, Magri KA, Ewton DZ, James PL, Grindstaff K, Rotwein PS (1991) Spontaneous’ differentiation of skeletal myoblasts is dependent upon autocrine secretion of insulin-like growth factor-II. The Journal of Biological Chemistry 266, 15917–15923.
Folch J, Lees M, Stanley GH (1957) A simple method for the isolation of total lipids from animal tissues. The Journal of Biological Chemistry 226, 497–509.
Fontanesi L, Speroni C, Buttazzoni L, Scotti E, Dall’Olio S, Nanni Costa L, Davoli R, Russo V (2010) The insulin-like growth factor 2 (IGF2) gene intron3-g.3072G>A polymorphism is not the only Sus scrofa chromosome 2p mutation affecting meat production and carcass traits in pigs: Evidence from the effects of a cathepsin D (CTSD) gene polymorphism. Journal of Animal Science 88, 2235–2245.
| The insulin-like growth factor 2 (IGF2) gene intron3-g.3072G>A polymorphism is not the only Sus scrofa chromosome 2p mutation affecting meat production and carcass traits in pigs: Evidence from the effects of a cathepsin D (CTSD) gene polymorphism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXos1KmsLo%3D&md5=35abd493058fa020e92a37985abc5f5bCAS |
Gardan D, Gondret F, Van den Maagdenberg K, Buys N, De Smet S, Louveau I (2008) Lipid metabolism and cellular features of skeletal muscle and subcutaneous adipose tissue in pigs differing in IGF-II genotype. Domestic Animal Endocrinology 34, 45–53.
| Lipid metabolism and cellular features of skeletal muscle and subcutaneous adipose tissue in pigs differing in IGF-II genotype.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlWkt7jI&md5=a20a4fbbcc96623dcf615ef6a3deeb18CAS |
Honikel KO (1998) Reference methods for the assessment of physical characteristics of meat. Meat Science 49, 447–457.
| Reference methods for the assessment of physical characteristics of meat.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3MbntlCntw%3D%3D&md5=e648f42a598b4c0effeae3aae84e22d1CAS |
Hornsey HC (1956) The colour of cooked cured pork. I. Estimation of the nitric oxide-haem pigments. Journal of the Science of Food and Agriculture 7, 534–540.
| The colour of cooked cured pork. I. Estimation of the nitric oxide-haem pigments.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaG28XnvFWlsA%3D%3D&md5=05d84983d98c3089918454a418e427bcCAS |
Huff-Lonergan E, Baas TJ, Malek M, Dekkers JC, Prusa K, Rothschild MF (2002) Correlations among selected pork quality traits. Journal of Animal Science 80, 617–627.
| Correlations among selected pork quality traits.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XmvV2isr0%3D&md5=e633d9cafa05d88a87e2a792c1198f06CAS |
ISO (1978) Preparation of methyl esters of fatty acids. ISO 5509. In ‘Animal and vegetable fats and oils’. (International Organization for Standardization: Geneva) Available at http://www.iso.org/iso/iso_catalogue/catalogue_ics/catalogue_detail_ics.htm?csnumber=1150 [Verified 12 December 2013]
Jeon J, Carlborg Ö, Törnsten A, Giuffra E, Amarger V, Chardon P, Andersson-Eklund L, Andersson K, Hansson I, Lundström K, Andersson L (1999) A paternally expressed QTL affecting skeletal and cardiac muscle mass in pigs maps to theIGF2 locus. Nature Genetics 21, 157–158.
| A paternally expressed QTL affecting skeletal and cardiac muscle mass in pigs maps to theIGF2 locus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXpsVCltw%3D%3D&md5=cb22ebede92624f26cf91d72092fd5a1CAS |
Joo ST, Kim GD, Hwang YH, Ryu YC (2013) Control of fresh meat quality through manipulation of muscle fiber characteristics. Meat Science 95, 828–836.
| Control of fresh meat quality through manipulation of muscle fiber characteristics.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3snmtlKqug%3D%3D&md5=1c16256aac2a66e0eddadea7fc46eea0CAS |
Kokta TA, Dodson MV, Gertler A, Hill RA (2004) Intercellular signaling between adipose tissue and muscle tissue. Domestic Animal Endocrinology 27, 303–331.
| Intercellular signaling between adipose tissue and muscle tissue.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXptFOqs7k%3D&md5=4359164f1d79ee28a91b46b5f383c4b2CAS |
Krzywicki K (1982) The determination of haem pigments in meat. Meat Science 7, 29–36.
| The determination of haem pigments in meat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38XlvVShuro%3D&md5=01dabccbfb175e7e10cbeeb8f8e42466CAS |
Livingstone C, Borai A (2014) Insulin-like growth factor-II: its role in metabolic and endocrine disease. Horumon To Rinsho 80, 773–781.
| Insulin-like growth factor-II: its role in metabolic and endocrine disease.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXnt1ejtro%3D&md5=9c591490e20ef5ed3402c0048c7aa19eCAS |
López-Buesa P, Burgos C, Galve A, Varona L (2014) Joint analysis of additive, dominant and first-order epistatic effects of four genes (IGF2, MC4R, PRKAG3 and LEPR) with known effects on fat content and fat distribution in pigs. Animal Genetics 45, 133–137.
| Joint analysis of additive, dominant and first-order epistatic effects of four genes (IGF2, MC4R, PRKAG3 and LEPR) with known effects on fat content and fat distribution in pigs.Crossref | GoogleScholarGoogle Scholar |
Mancini RA, Hunt MC (2005) Current research in meat color. Meat Science 71, 100–121.
| Current research in meat color.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmt1Wiurg%3D&md5=2dc31eb0b8823ccaff067ed45ecfe260CAS |
Mineo R, Fichera E, Liang S, Fujita-Yamaguchi Y (2000) Promoter Usage for Insulin-like Growth Factor-II in Cancerous and Benign Human Breast, Prostate, and Bladder Tissues, and Confirmation of a 10th Exon. Biochemical and Biophysical Research Communications 268, 886–892.
| Promoter Usage for Insulin-like Growth Factor-II in Cancerous and Benign Human Breast, Prostate, and Bladder Tissues, and Confirmation of a 10th Exon.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXhtFGisLc%3D&md5=9fe325a5d75c619a3feb11c8ec1fdf22CAS |
Nezer C, Moreau L, Brouwers B, Coppieters W, Detilleux J, Hanset R (1999) An imprinted QTL with major effect on muscle mass and fat deposition maps to the IGF2 locus in pigs. Nature Genetics 21, 155–156.
| An imprinted QTL with major effect on muscle mass and fat deposition maps to the IGF2 locus in pigs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXpsVCltg%3D%3D&md5=9b0f281be2f6043c7739b4965898adc1CAS |
Nezer C, Collette C, Moreau L, Brouwers B, Kim JJ, Giuffra E, Buys N, Andersson L, Georges M (2003) Haplotype sharing refines the location of an imprinted Quantitative Trait Locus with major effect on muscle mass to a 250-kb chromosome segment containing the porcine IGF2 gene. Genetics 165, 277–285.
Oczkowicz M, Tyra M, Walinowicz K, Rózycki M, Rejduch B (2009) Known mutation (A3072G) in intron 3 of the IGF2 gene is associated with growth and carcass composition in Polish pig breeds. Journal of Applied Genetics 50, 257–259.
| Known mutation (A3072G) in intron 3 of the IGF2 gene is associated with growth and carcass composition in Polish pig breeds.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1MnnslCqsQ%3D%3D&md5=f3cb7b462838cccf8338158862f69e35CAS |
Oczkowicz M, Tyra M, Ropka-Molik K, Mucha A, Żukowski K (2012) Effect of IGF2 intron3-g. 3072G > A on intramuscular fat (IMF) content in pigs raised in Poland. Livestock Science 149, 301–304.
Ohlsen SM, Lugenbeel KA, Wong EA (1994) Characterization of the linked ovine insulin and insulin-like growth factor-II genes. DNA and Cell Biology 13, 377–388.
| Characterization of the linked ovine insulin and insulin-like growth factor-II genes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXlvFOiurc%3D&md5=faa012bde020947a03d6cd90d56d145eCAS |
Oksbjerg N, Gondret F, Vestergaard M (2004) Basic principles of muscle development and growth in meat producing mammals as affected by the insulin-like growth factor (IGF) system. Domestic Animal Endocrinology 27, 219–240.
| Basic principles of muscle development and growth in meat producing mammals as affected by the insulin-like growth factor (IGF) system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnvV2rsLc%3D&md5=2c3dd63150678c793163f39d7a085e78CAS |
Perna A, Simonetti A, Intaglietta I, Gambacorta E (2015a) Fatty acids composition, cholesterol and vitamin E contents of Longissimus dorsi and Semitendinosus muscles of Suino Nero Lucano pigs slaughtered at two different weights. Animal Production Science 55, 1037–1043.
| Fatty acids composition, cholesterol and vitamin E contents of Longissimus dorsi and Semitendinosus muscles of Suino Nero Lucano pigs slaughtered at two different weights.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhtVOktrvE&md5=96f97a0c9bf828a1e6e8498cbb14bcd5CAS |
Perna A, Simonetti A, Intaglietta I, Gambacorta E (2015b) Quality and sensory characteristics of Culatello dry-cured products obtained from the Italian autochthonous pig Suino Nero Lucano and from a modern crossbred pig. Animal Production Science 55, 1192–1199.
| Quality and sensory characteristics of Culatello dry-cured products obtained from the Italian autochthonous pig Suino Nero Lucano and from a modern crossbred pig.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXht1CitLbN&md5=4586b0096993a885997dfdb56806c8eeCAS |
Pugliese C, Sirtori F (2012) Quality of meat and meat products produced from southern European pig breeds. Meat Science 90, 511–518.
| Quality of meat and meat products produced from southern European pig breeds.Crossref | GoogleScholarGoogle Scholar |
SAS Institute (1996) ‘SAS user’s guide: statistics. Version 7.’ (SAS Institute Inc.: Cary, NC)
Van den Maagdenberg K, Stinckens A, Claeys E, Buys N, De Smet S (2008) Effect of the insulin-like growth factor-II and RYR1 genotype in pigs on carcass and meat quality traits. Meat Science 80, 293–303.
| Effect of the insulin-like growth factor-II and RYR1 genotype in pigs on carcass and meat quality traits.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtVagu7%2FO&md5=afdc5245eecdf536f641ec8c28b34b2eCAS |
van Laack RL, Stevens SG, Stalder KJ (2001) The influence of ultimate pH and intramuscular fat content on pork tenderness and tenderization. Journal of Animal Science 79, 392–397.
| The influence of ultimate pH and intramuscular fat content on pork tenderness and tenderization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjsFCnsb0%3D&md5=10ccd17cf5b0f2f7bfe6844add4d4688CAS |
Van Laere AS, Nguyen M, Braunschweig M, Nezer C, Collette C, Moreau L, Archibald AL, Haley CS, Buys N, Tally M, Andersson G, Georges M, Andersson L (2003) A regulatory mutation in IGF2 causes a major QTL effect on muscle growth in the pig. Nature 425, 832–836.
| A regulatory mutation in IGF2 causes a major QTL effect on muscle growth in the pig.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXotlWqtro%3D&md5=89b52902f791cbf050fd896d27705b5eCAS |
