Evolution of major milk proteins in Mus musculus and Mus spretus mouse species: A genoproteomic analysis

BMC Genomics

Volumn 12, Issue , 2011, Pages

  Boumahrou, Nisrine ^a   Bevilacqua, Claudia ^a   Beauvallet, Christian ^a   Miranda, Guy ^a   Andrei, Sanda ^a,b   Rebours, Emmanuelle ^a   Panthier, Jean Jacques ^c   Bellier, Sylvain ^a,d   Martin, Patrice ^a  

^a UMR1313 GÉNÉTIQUE ANIMALE ET BIOLOGIE INTÉGRATIVE   (France)

^b Universitatea de Stiinte Agricole si Medicina Veterinara Cluj Napoca ^*  (Romania)

^c CNRS   (France)

^d UMR955 de Génétique Fonctionnelle et Médicale   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ACID PROTEIN; ALPHA CASEIN; BETA CASEIN; MILK PROTEIN; UNCLASSIFIED DRUG; WHEY ACIDIC PROTEIN;

3' UNTRANSLATED REGION; AMINO ACID SUBSTITUTION; ANIMAL TISSUE; ARTICLE; C57BL 6 MOUSE; CONTROLLED STUDY; CSN1S1 GENE; CSN2 GENE; DNA SEQUENCE; DNA SPLICING; FEMALE; GENE; GENE DELETION; GENOMICS; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MOLECULAR EVOLUTION; MOUSE; MOUSE STRAIN; MURIDAE; MUS SPRETUS; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN ANALYSIS; PROTEOMICS; REVERSED PHASE HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; SEG PAS MOUSE; SINGLE NUCLEOTIDE POLYMORPHISM; STRAIN DIFFERENCE; TWO DIMENSIONAL ELECTROPHORESIS; WAP GENE; AMINO ACID SEQUENCE; ANIMAL; C57BL MOUSE; COMPARATIVE STUDY; GENETICS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; MOLECULAR GENETICS; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN PROCESSING; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TWO DIMENSIONAL GEL ELECTROPHORESIS;

MUS; MUS MUSCULUS; MUS SPRETUS;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; ELECTROPHORESIS, POLYACRYLAMIDE GEL; EVOLUTION, MOLECULAR; FEMALE; GENOMICS; MICE; MICE, INBRED C57BL; MILK PROTEINS; MOLECULAR SEQUENCE DATA; POLYMORPHISM, SINGLE NUCLEOTIDE; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN SPLICING; PROTEOMICS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS, DNA; SEQUENCE DELETION; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

EID: 79251589080     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-12-80     Document Type: Article

References (42)

1. Guenet JL, Bonhomme F. Wild mice: an ever-increasing contribution to a popular mammalian model. Trends Genet 2003, 19(1):24-31. 10.1016/S0168-9525(02)00007-0, 12493245.
2. de Gouyon B, Melanitou E, Richard MF, Requarth M, Hahn IH, Guenet JL, Demenais F, Julier C, Lathrop GM, Boitard C, et al. Genetic analysis of diabetes and insulitis in an interspecific cross of the nonobese diabetic mouse with Mus spretus. Proc Natl Acad Sci USA 1993, 90(5):1877-1881. 10.1073/pnas.90.5.1877, 45983, 8446602.
3. Stephan K, Smirnova I, Jacque B, Poltorak A. Genetic analysis of the innate immune responses in wild-derived inbred strains of mice. Eur J Immunol 2007, 37(1):212-223. 10.1002/eji.200636156, 17163447.
4. Burgio G, Baylac M, Heyer E, Montagutelli X. Genetic analysis of skull shape variation and morphological integration in the mouse using interspecific recombinant congenic strains between C57BL/6 and mice of the mus spretus species. Evolution 2009, 63(10):2668-2686. 10.1111/j.1558-5646.2009.00737.x, 19490077.
5. Klose J, Nock C, Herrmann M, Stuhler K, Marcus K, Bluggel M, Krause E, Schalkwyk LC, Rastan S, Brown SD, et al. Genetic analysis of the mouse brain proteome. Nat Genet 2002, 30(4):385-393. 10.1038/ng861, 11912495.
6. Mikkat S, Lorenz P, Scharf C, Yu X, Glocker MO, Ibrahim SM. MS characterization of qualitative protein polymorphisms in the spinal cords of inbred mouse strains. Proteomics 2010, 10(5):1050-1062.
7. Ramanathan P, Martin I, Thomson P, Taylor R, Moran C, Williamson P. Genomewide analysis of secretory activation in mouse models. J Mammary Gland Biol Neoplasia 2007, 12(4):305-314. 10.1007/s10911-007-9052-6, 17994195.
8. Ron M, Israeli G, Seroussi E, Weller JI, Gregg JP, Shani M, Medrano JF. Combining mouse mammary gland gene expression and comparative mapping for the identification of candidate genes for QTL of milk production traits in cattle. BMC Genomics 2007, 8:183. 10.1186/1471-2164-8-183, 1906769, 17584498.
9. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976, 72:248-254. 10.1016/0003-2697(76)90527-3, 942051.
10. Boumahrou N, Andrei S, Miranda G, Henry C, Panthier JJ, Martin P, Bellier S. The major protein fraction of mouse milk revisited using proven proteomics tools. J Physiol Pharmacol 2009, 60(suppl 3):113-118.
11. Bevilacqua C, Helbling JC, Miranda G, Martin P. Translational efficiency of casein transcripts in the mammary tissue of lactating ruminants. Reprod Nutr Dev 2006, 46(5):567-578. 10.1051/rnd:2006028, 17107646.
12. Piletz JE, Ganschow RE. Genetic variation of milk proteins in mice. Biochem Genet 1981, 19(9-10):1023-1030. 10.1007/BF00504265, 7332524.
13. Ragueneau S. Early development in mice. IV: Quantity and gross composition of milk in five inbred strains. Physiol Behav 1987, 40(4):431-435. 10.1016/0031-9384(87)90027-8, 3628540.
14. Riley LG, Zubair M, Thomson PC, Holt M, Xavier SP, Wynn PC, Sheehy PA. Lactational performance of Quackenbush Swiss line 5 mice. J Anim Sci 2006, 84(8):2118-2125. 10.2527/jas.2005-609, 16864872.
15. Martin P, Ferranti P, Leroux C, Addeo F. Non-bovine caseins: quantitative variability and molecular diversity. Advanced Dairy Chemistry: Proteins 2003, 277-318.
16. Rudolph MC, McManaman JL, Hunter L, Phang T, Neville MC. Functional development of the mammary gland: use of expression profiling and trajectory clustering to reveal changes in gene expression during pregnancy, lactation, and involution. J Mammary Gland Biol Neoplasia 2003, 8(3):287-307. 10.1023/B:JOMG.0000010030.73983.57, 14973374.
17. Piletz JE, Heinlen M, Ganschow RE. Biochemical characterization of a novel whey protein from murine milk. J Biol Chem 1981, 256(22):11509-11516.
18. Ranganathan S, Simpson KJ, Shaw DC, Nicholas KR. The whey acidic protein family: a new signature motif and three-dimensional structure by comparative modeling. J Mol Graph Model 1999, 17(2):106-113. 10.1016/S1093-3263(99)00023-6, 10680116.
19. Simpson KJ, Bird P, Shaw D, Nicholas K. Molecular characterisation and hormone-dependent expression of the porcine whey acidic protein gene. J Mol Endocrinol 1998, 20(1):27-35. 10.1677/jme.0.0200027, 9513079.
20. Litersky JM, Scott CW, Johnson GV. Phosphorylation, calpain proteolysis and tubulin binding of recombinant human tau isoforms. Brain Res 1993, 604(1-2):32-40. 10.1016/0006-8993(93)90349-R, 8384512.
21. Wiltfang J, Smirnov A, Schnierstein B, Kelemen G, Matthies U, Klafki HW, Staufenbiel M, Huther G, Ruther E, Kornhuber J. Improved electrophoretic separation and immunoblotting of beta-amyloid (A beta) peptides 1-40, 1-42, and 1-43. Electrophoresis 1997, 18(3-4):527-532. 10.1002/elps.1150180332, 9150936.
22. Triplett AA, Sakamoto K, Matulka LA, Shen L, Smith GH, Wagner KU. Expression of the whey acidic protein (Wap) is necessary for adequate nourishment of the offspring but not functional differentiation of mammary epithelial cells. Genesis 2005, 43:1-11. 10.1002/gene.20149, 16106354.
23. Hennighausen LG, Sippel AE. Mouse whey acidic protein is a novel member of the family of 'four-disulfide core' proteins. Nucleic Acids Res 1982, 10(8):2677. 10.1093/nar/10.8.2677, 320642, 6896234.
24. Miclo L, Girardet JM, Egito AS, Mollé D, Martin P, Gaillard JL. The primary structure of a low-Mr multiphosphorylated variant of beta-casein in equine milk. Proteomics 2007, 7(8):1327-1335. 10.1002/pmic.200600683, 17366489, 17366489.
25. Smith CW, Chu TT, Nadal-Ginard B. Scanning and competition between AGs are involved in 3'splice site selection in mammalian introns. Mol Cell Biol 1993, 13(8):4939. 360135, 8336728.
26. Leroux C, Mazure N, Martin P. Mutations away from splice site recognition sequences might cis-modulate alternative splicing of goat alpha s1-casein transcripts. Structural organization of the relevant gene. J Biol Chem 1992, 267(9):6147-6157.
27. Ferranti P, Malorni A, Nitti G, Laezza P, Pizzano R, Chianese L, Addeo F. Primary structure of ovine alpha s1-caseins: localization of phosphorylation sites and characterization of genetic variants A, C and D. J Dairy Res 1995, 62(2):281-296. 10.1017/S0022029900030983, 7601973.
28. Ferranti P, Lilla S, Chianese L, Addeo F. Alternative nonallelic deletion is constitutive of ruminant alpha(s1)-casein. J Protein Chem 1999, 18(5):595-602. 10.1023/A:1020659518748, 10524777.
29. Martin P, Brignon G, Furet JP, Leroux C. The gene encoding αs1-casein is expressed in human mammary epithelial cells during lactation. Lait 1996, 76:523-535.
30. Martin P, Szymanowska M, Zwierzchowski L, Leroux C. The impact of genetic polymorphisms on the protein composition of ruminant milks. Reprod Nutr Dev 2002, 42(5):433-459. 10.1051/rnd:2002036, 12537255.
31. Lu K, Lee MH, Yu H, Zhou Y, Sandell SA, Salen G, Patel SB. Molecular cloning, genomic organization, genetic variations, and characterization of murine sterolin genes Abcg5 and Abcg8. The Journal of Lipid Research 2002, 43(4):565.
32. Lu K, Lee MH, Hazard S, Brooks-Wilson A, Hidaka H, Kojima H, Ose L, Stalenhoef AFH, Mietinnen T, Bjorkhem I. Two genes that map to the STSL locus cause sitosterolemia: genomic structure and spectrum of mutations involving sterolin-1 and sterolin-2, encoded by ABCG5 and ABCG8, respectively. The American Journal of Human Genetics 2001, 69(2):278-290.
33. Condorelli G, Bueno R, Smith RJ. Two alternatively spliced forms of the human insulin-like growth factor I receptor have distinct biological activities and internalization kinetics. J Biol Chem 1994, 269(11):8510-8516.
34. Vogan KJ, Underhill DA, Gros P. An alternative splicing event in the Pax-3 paired domain identifies the linker region as a key determinant of paired domain DNA-binding activity. Mol Cell Biol 1996, 16(12):6677-6686. 231670, 8943322.
35. Hiller M, Platzer M. Widespread and subtle: alternative splicing at short-distance tandem sites. Trends Genet 2008, 24(5):246-255. 10.1016/j.tig.2008.03.003, 18394746.
36. Johnsen LB, Rasmussen LK, Petersen TE, Berglund L. Characterization of three types of human alpha s1-casein mRNA transcripts. Biochem J 1995, 309(Pt 1):237. 1135825, 7619062.
37. Rijnkels M. Multispecies comparison of the casein gene loci and evolution of casein gene family. J Mammary Gland Biol Neoplasia 2002, 7(3):327-345. 10.1023/A:1022808918013, 12751895.
38. Lemay DG, Lynn DJ, Martin WF, Neville MC, Casey TM, Rincon G, Kriventseva EV, Barris WC, Hinrichs AS, Molenaar AJ, et al. The bovine lactation genome: insights into the evolution of mammalian milk. Genome Biol 2009, 10(4):R43. 10.1186/gb-2009-10-4-r43, 2688934, 19393040.
39. Mercier JC, Chobert JM, Addeo F. Comparative study of the amino acid sequences of the caseinomacropeptides from seven species. FEBS Lett 1976, 72(2):208-214. 10.1016/0014-5793(76)80972-6, 16386026.
40. Capuco AV, Akers RM. The origin and evolution of lactation. J Biol 2009, 8(4):37. 10.1186/jbiol139, 2688910, 19439024.
41. Mikkelsen TS, Wakefield MJ, Aken B, Amemiya CT, Chang JL, Duke S, Garber M, Gentles AJ, Goodstadt L, Heger A, et al. Genome of the marsupial Monodelphis domestica reveals innovation in non-coding sequences. Nature 2007, 447(7141):167-177. 10.1038/nature05805, 17495919.
42. Sharp JA, Lefèvre C, Nicholas KR, et al. Molecular evolution of monotreme and marsupial whey acidic protein genes. Evol Dev 2007, 9(4):378-392.