Hostname: page-component-586b7cd67f-dsjbd Total loading time: 0 Render date: 2024-11-22T19:27:55.574Z Has data issue: false hasContentIssue false
  • English
  • Français

Rabbit milk protein genes: from mRNA identification to chromatin structure

Published online by Cambridge University Press:  01 March 2008

G. Jolivet ,
N. Daniel-Carlier ,
D. Thépot ,
S. Rival-Gervier  and
L. M. Houdebine
G. Jolivet*
Affiliation:
INRA, UMR 1198; ENVA; CNRS, FRE 2857, Biologie du Développement et Reproduction, Jouy en Josas F-78350, France
N. Daniel-Carlier
Affiliation:
INRA, UMR 1198; ENVA; CNRS, FRE 2857, Biologie du Développement et Reproduction, Jouy en Josas F-78350, France
D. Thépot
Affiliation:
INRA, UMR 1198; ENVA; CNRS, FRE 2857, Biologie du Développement et Reproduction, Jouy en Josas F-78350, France
S. Rival-Gervier
Affiliation:
INRA, UMR 1198; ENVA; CNRS, FRE 2857, Biologie du Développement et Reproduction, Jouy en Josas F-78350, France
L. M. Houdebine
Affiliation:
INRA, UMR 1198; ENVA; CNRS, FRE 2857, Biologie du Développement et Reproduction, Jouy en Josas F-78350, France
*
E-mail: [email protected]
Get access

Abstract

Milk protein genes are among the most intensively expressed and they are active only in epithelial mammary cells of lactating animals. They code for proteins which represent 30% of the proteins consumed by humans in developed countries. Mammary gland development occurs essentially during each pregnancy. This offers experimenters attractive models to study the expression mechanisms of genes controlled by known hormones and factors (prolactin, glucocorticoids, progesterone, insulin-like growth factor-1 and others) as well as extracellular matrix. In the mid-1970s, it became possible to identify and quantify mRNAs from higher living organisms using translation in reticulocyte lysate. A few years later, the use of radioactive cDNAs as probes made it possible for the quantification of mRNA in various physiological situations using hybridisation in the liquid phase. Gene cloning offered additional tools to measure milk protein mRNAs and also to identify transcription factors. Gene transfer in cultured mammary cells and in animals contributed greatly to these studies. It is now well established that most if not all genes of higher eukaryotes are under the control of multiple distal regulatory elements and that local modifications of the chromatin structure play an essential role in the mechanisms of differentiation from embryos to adults. The technique, known as ChIP (chromatin immunoprecipitation), is being implemented to identify the factors that modify chromatin structure at the milk protein gene level during embryo development, mammogenesis and lactogenesis, including the action of hormones and extracellular matrix. Transgenesis is not just a tool to study gene regulation and function, it is also currently used for various biotechnological applications including the preparation of pharmaceutical proteins in milk. This implies the design of efficient vectors capable of directing the secretion of recombinant proteins in milk at a high concentration. Milk protein gene promoters and long genomic-DNA fragments containing essentially all the regulatory elements of milk protein genes are used to optimise recombinant protein production in milk.

Keywords

chromatindevelopmentpromotertransgenesis
Type
Full Paper
Information
animal , Volume 2 , Issue 3 , March 2008 , pp. 336 - 343
Copyright
Copyright © The Animal Consortium 2008

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Al-Gubory, KH, Houdebine, LM 2006. In vivo imaging of green fluorescent protein expressing cells in transgenic animals using fibered confocal fluorescence microscopy. European Journal of Cell Biology 85, 837–845.Google Scholar
Assairi, L, Delouis, C, Gaye, P, Houdebine, LM, Bousquet, MO, Denamur, R 1974. Inhibition by progesterone of the lactogenic effect of prolactin in the pseudopregnant rabbit. Biochemical Journal 144, 245–252.CrossRefGoogle ScholarPubMed
Attal, J, Théron, MC, Puissant, C, Houdebine, LM 1999. Effect of intercistronic length on internal ribosome entry site (IRES) efficiency in bicistronic mRNA. Gene Expression 8, 299–309.Google ScholarPubMed
Baranyi, M, Aszodi, A, Devinoy, E, Fontaine, ML, Houdebine, LM, Bosze, Z 1996. Structure of the rabbit κ-casein encoding gene: expression of the cloned gene in the mammary gland of transgenic mice. Gene 174, 27–34.CrossRefGoogle ScholarPubMed
Baranyi, M, Hiripi, L, Szabó, L, Catunda, AP, Harsänyi, I, Komäromy, P, Bősze, Z 2007. Isolation and some effects of functional, low-phenylalanine κ-casein expressed in the milk of transgenic rabbits. Journal of Biotechnology 128, 383–392.CrossRefGoogle ScholarPubMed
Bischoff, R, Degryse, E, Perraud, F, Dalemans, W, Ali-Hadji, D, Thépot, D, Devinoy, E, Houdebine, LM, Pavirani, A 1992. A 17.6 kbp region located upstream of the rabbit WAP gene directs high level expression of a functional human protein variant in transgenic mouse milk. FEBS Letters 305, 265–268.CrossRefGoogle ScholarPubMed
Bleck, GT, White, BR, Miller, DJ, Wheeler, MB 1998. Production of bovine alpha-lactalbumin in the milk of transgenic pigs. Journal of Animal Science 76, 3072–3078.CrossRefGoogle ScholarPubMed
Bodrogi, L, Brands, R, Raaben, W, Seinen, W, Baranyi, M, Fiechter, D, Bosze, Z 2006. High level expression of tissue-nonspecific alkaline phosphatase in the milk of transgenic rabbits. Transgenic Research 15, 627–636.Google Scholar
Bösze, Z, Houdebine, LM 2006. Application of rabbits in biomedical research: a review. World Rabbit Science 14, 1–14.Google Scholar
Brophy, B, Smolenski, G, Wheeler, T, Wells, D, L’Huillier, P, Laible, G 2003. Cloned transgenic cattle produce milk with higher levels of beta-casein and kappa-casein. Nature Biotechnology 21, 138–139.Google Scholar
Chourrout, D, Guyomard, R, Houdebine, LM 1986. High efficiency gene transfer in rainbow trout (Salmo gairdneri Rich.) by microinjection into egg cytoplasm. Aquaculture 51, 143–150.CrossRefGoogle Scholar
Cirillo, LA, Lin, FR, Cuesta, I, Friedman, D, Jarnik, M, Zaret, KS 2002. Opening of compacted chromatin by early developmental transcription factors HNF3 (FoxA) and GATA-4. Molecular Cell 9, 279–289.CrossRefGoogle ScholarPubMed
Devinoy, E, Houdebine, LM, Delouis, C 1978. Role of prolactin and glucocorticoids in the expression of casein genes in rabbit mammary gland organ culture. Quantification of casein mRNA. Biochimica Biophysica Acta 517, 360–366.CrossRefGoogle ScholarPubMed
Devinoy, E, Hubert, C, Schaerer, E, Houdebine, LM, Kraehenbuhl, JP 1988a. Sequence of the rabbit whey acidic protein cDNA. Nucleic Acids Research 16, 8180.CrossRefGoogle ScholarPubMed
Devinoy, E, Schaerer, E, Jolivet, G, Fontaine, ML, Kraehenbuhl, JP, Houdebine, LM 1988b. Sequence of the rabbit alpha S1-casein cDNA. Nucleic Acids Research 16, 11813.CrossRefGoogle ScholarPubMed
Devinoy, E, Malienou-N’Gassa, R, Thépot, D, Puissant, C, Houdebine, LM 1991. Hormone responsive elements within the upstream sequences of the rabbit whey acidic protein (WAP) gene direct chloramphenicol acetyl transferase (CAT) reporter gene expression in transfected rabbit mammary cells. Molecular and Cellular Endocrinology 81, 185–193.CrossRefGoogle ScholarPubMed
Devinoy, E, Thépot, D, Stinnakre, MG, Fontaine, ML, Grabowski, H, Puissant, C, Pavirani, A, Houdebine, LM 1994. High level production of human growth hormone in the milk of transgenic mice: the upstream region of the rabbit whey protein (WAP) gene targets transgene expression to the mammary gland. Transgenic Research 3, 79–89.CrossRefGoogle Scholar
Devinoy, E, Montoliu, L, Baranyi, M, Thépot, D, Hiripi, L, Fontaine, ML, Bodrogi, L, Bosze, Z 2005. Analysis of the efficiency of the rabbit whey acidic protein gene 5′ flanking region in controlling the expression of homologous and heterologous linked genes. Journal of Dairy Research 72, 113–119.Google Scholar
Doppler, W 1994. Regulation of gene expression by prolactin. Reviews of Physiology, Biochemistry and Pharmacology 124, 93–130.Google Scholar
Edwards, GM, Wilford, FH, Liu, X, Hennighausen, L, Djiane, J, Streuli, CH 1998. Regulation of mammary differentiation by extracellular matrix involves protein-tyrosine phosphatases. Journal of Biological Chemistry 273, 9495–9500.CrossRefGoogle ScholarPubMed
Galet, C, Le Bourhis, CM, Chopineau, M, Le Griec, G, Perrin, A, Magallon, T, Attal, J, Viglietta, C, Houdebine, LM, Guillou, F 2001. Expression of a single beta–alpha chain protein of equine LH/CG in milk of transgenic rabbits and its biological activity. Molecular and Cellular Endocrinology 174, 31–40.Google Scholar
Gaye, P, Houdebine, LM 1975. Isolation and characterization of casein mRNAs from lactating ewe mammary glands. Nucleic Acids Research 2, 707–722.Google Scholar
Gaye, P, Houdebine, LM, Pétrissant, G, Denamur, R 1973. Protein synthesis in mammary gland. Acta Endocrinologica. Supplementum 180, 426–463.Google Scholar
Ghareeb, BA, Thépot, D, Puissant, C, Cajero-Juarez, M, Houdebine, LM 1998. Cloning, structural organization and tissue-specific expression of the rabbit transferrin gene. Biochimica et Biophysica Acta 1398, 387–392.CrossRefGoogle ScholarPubMed
Giraldo, P, Rival-Gervier, S, Houdebine, LM, Montoliu, L 2003. The potential benefits of insulators on heterogonous constructs in transgenic. Transgenic Research 12, 751–755.CrossRefGoogle Scholar
Grabowski, H, Le Bars, D, Chene, N, Attal, J, Malienou-Ngassa, R, Puissant, C, Houdebine, LM 1991. Rabbit whey acidic protein concentration in milk, serum, mammary gland extract, and culture medium. Journal of Dairy Science 74, 4143–4150.Google Scholar
Hajjoubi, S, Rival-Gervier, S, Hayes, H, Floriot, S, Eggen, A, Piumi, F, Chardon, P, Houdebine, LM, Thépot, D 2006. Ruminant genome no longer contains whey acidic protein gene but only a pseudogene. Gene 370, 104–112.CrossRefGoogle Scholar
Hiripi, L, Baranyi, M, Szabó, L, Tóth, S, Fontaine, ML, Devinoy, E, Bösze, Z 2000. Effect of rabbit kappa-casein expression on the properties of milk from transgenic mice. Journal of Dairy Research 67, 541–550.Google Scholar
Houdebine, LM 1976. Effects of prolactin and progesterone on expression of casein genes. Titration of casein mRNA by hybridization with complementary DNA. European. Journal of Biochemistry 68, 219–225.Google Scholar
Houdebine, LM 1979. Role of prolactin in the expression of casein genes in the virgin rabbit. Cell Differentiation 8, 49–59.Google Scholar
Houdebine, LM 2002. Antibody manufacture in transgenic animals, comparisons with other systems. Current Opinion in Biotechnology 13, 625–629.CrossRefGoogle ScholarPubMed
Houdebine, LM 2003a. Preparation of recombinant proteins in milk. In Recombinant gene expression protocols, methods in molecular biology , vol. 267 (ed. E Balbas), pp. 485–494. Human Press, NJ, USA.Google Scholar
Houdebine, LM 2003b. Animal transgenesis and cloning. Wiley and Sons, Hoboken, NJ, USA.CrossRefGoogle Scholar
Houdebine, LM 2004. Preparation of recombinant proteins in milk. Methods in Molecular Biology 267, 485–494.Google ScholarPubMed
Houdebine, LM 2005. Use of transgenic animals to improve human health and animal production. Reproduction in Domestic Animals 40, 269–281.CrossRefGoogle ScholarPubMed
Houdebine LM 2007a. Production of pharmaceutical proteins by transgenic animals. Comparative Immunology, Microbiology and Infectious Diseases, in press.Google Scholar
Houdebine, LM 2007b. Transgenic animal models and target validation. Methods in Molecular Biology 360, 163–202.Google Scholar
Houdebine, LM, Gaye, P 1975a. Absence of mRNA for casein in free polysomes of lactating ewe mammary gland. Nucleic Acids Research 2, 165–178.CrossRefGoogle ScholarPubMed
Houdebine, LM, Gaye, P 1975b. Regulation of casein synthesis in the rabbit mammary gland. Titration of mRNA activity for casein under prolactin and progesterone treatments. Molecular and Cellular Endocrinology 3, 37–55.Google Scholar
Houdebine, LM, Gaye, P 1976. Purification of the mRNAs for ewe alphaS1-casein and beta-casein by immunoprecipitation of polysomes. European Journal of Biochemistry 63, 9–14.Google Scholar
Houdebine, LM, Gaye, P, Favre, A 1974. Lack of poly(A) sequence in half of the messenger RNA coding for ewe alpha S casein. Nucleic Acids Research 1, 413–426.Google Scholar
Houdebine, LM, Delouis, C, Devinoy, E 1978a. Post-transcriptional stimulation of casein synthesis by thyroid hormone. Biochimie 60, 809–812.CrossRefGoogle ScholarPubMed
Houdebine, LM, Devinoy, E, Delouis, C 1978b. Role of spermidine in casein gene expression in the rabbit. Biochimie 60, 735–741.Google Scholar
Houdebine, LM, Devinoy, E, Delouis, C 1978c. Stabilization of casein mRNA by prolactin and glucocorticoids. Biochimie 60, 57–63.Google Scholar
Houdebine, LM, Farmer, SW, Prunet, P 1981. Induction of rabbit casein synthesis in organ culture by tilapia prolactin and growth hormone. General and Comparative Endocrinology 45, 61–65.Google Scholar
Houdebine, LM, Attal, J, Vilotte, JL 2002. Vector design for transgene expression. In Transgenic animal technology, 2nd edition (ed. A Carl and E Pinkert), pp. 419–458. Academic Press, San Diego, CA, USA.CrossRefGoogle Scholar
Jolivet, G, Devinoy, E, Fontaine, ML, Houdebine, LM 1992. Structure of the gene encoding rabbit αs1-casein. Gene 113, 257–262.CrossRefGoogle Scholar
Jolivet, G, L’Hotte, C, Pierre, S, Tourkine, N, Houdebine, LM 1996. A MGF/STAT5 binding site is necessary in the distal enhancer for high prolactin induction of transfected rabbit alpha s1-casein-CAT gene transcription. FEBS Letters 389, 257–262.Google Scholar
Jolivet, G, Pantano, T, Houdebine, LM 2005. Regulation by the extracellular matrix (EMC) of prolactin-induced alpha-s1-casein gene expression in rabbit primary cells. Role of STAT5, C/EBP and chromatin structure. Journal of Cellular Biochemistry 95, 313–327.Google Scholar
Koles, K, van Berkel, PH, Pieper, FR, Nuijens, JH, Mannesse, ML, Vliegenthart, JF, Kamerling, JP 2004. N- and O-glycans of recombinant human C1 inhibitor expressed in the milk of transgenic rabbits. Glycobiology 14, 51–64.Google Scholar
de Laat, W, Grosveld, F 2003. Spatial organization of gene expression: the active chromatin hub. Chromosome Research 11, 447–459.CrossRefGoogle ScholarPubMed
Lomvardas, S, Thanos, D 2002. Opening chromatin. Molecular Cell 9, 209–211.CrossRefGoogle ScholarPubMed
Long, X, Miano, JM 2007. Remote control of gene expression. Journal of Biological Chemistry 282, 15941–15945.CrossRefGoogle ScholarPubMed
Martel, P, Houdebine, LM, Teyssot, B, Djiane, J 1983. Effects of phorbol esters on multiplication and differentiation of mammary cells. Biologie Cellulaire 49, 119–126.Google Scholar
Martinet, J, Houdebine, LM, Head, HH 1999. Biology of lactation second edition. INRA Editions Publisher, Versailles, France.Google Scholar
Massoud, M, Attal, J, Thépot, D, Pointu, H, Stinnakre, MG, Théron, MC, Lopez, C, Houdebine, LM 1996. The deleterious effects of human erythropoietin gene driven by the rabbit whey acidic protein gene promoter in transgenic rabbits. Reproduction, Nutrition, Development 36, 555–563.CrossRefGoogle ScholarPubMed
Millot, B, Fontaine, ML, Thépot, D, Devinoy, E 2001. A distal region, hypersensitive to DNase I, plays a key role in regulating rabbit whey acidic protein gene expression. Biochemical Journal 359, 557–565.Google Scholar
O’Neill, LP, VerMilyea, MD, Turner, BM 2006. Epigenetic characterization of the early embryo with a chromatin immunoprecipitation protocol applicable to small cell populations. Nature Genetics 38, 835–841.Google Scholar
Pantano, T, Jolivet, G, Prince, S, Menck-Le Bourhis, C, Maeder, C, Viglietta, C, Rival, S, Houdebine, LM 2002. Effect of the rabbit αs1-casein gene distal enhancer on the expression of a reporter gene in vitro and in vivo. Biochemical and Biophysical Research Communications 290, 53–61.CrossRefGoogle ScholarPubMed
Pantano, T, Rival-Gervier, S, Menck-Le Bourhis, C, Maeder, C, Viglietta, C, Houdebine, LM, Jolivet, G 2003. In vitro and in vivo effects of a multimerized αS-1 casein enhancer on whey acidic protein gene promoter activity. Molecular Reproduction and Development 65, 262–268.Google Scholar
Pierre, S, Jolivet, G, Devinoy, E, Théron, MC, Malienou-N’Gassa, R, Puissant, C, Houdebine, LM 1992. A distal region enhances the prolactin induced promoter activity of the rabbit alpha s1-casein gene. Molecular and Cellular Endocrinology 87, 147–156.Google Scholar
Pierre, S, Jolivet, G, Devinoy, E, Houdebine, LM 1994. A combination of distal and proximal regions is required for efficient prolactin regulation of transfected rabbit alpha s1-casein chloramphenicol acetyltransferase constructs. Molecular Endocrinology 8, 1720–1730.Google Scholar
Praskova, ML, Jolivet, G, Houdebine, LM, Mitev, V 2005. Possible involvement of protein kinase Cμ in the activation of rabbit αS1-casein gene. Bulletin de l’Académie des Sciences Bulgares 58, 1229–1234.Google Scholar
Puissant, C, Bayat-Sarmadi, M, Devinoy, E, Houdebine, LM 1994. Variation of transferrin mRNA concentration in the rabbit mammary gland during the pregnancy–lactation–weaning cycle and in cultured mammary cells. A comparison with the other major milk protein mRNAs. European Journal of Endocrinology 130, 522–529.Google Scholar
Rival, S, Attal, J, Delville-Giraud, C, Yerle, M, Laffont, P, Rogel-Gaillard, C, Houdebine, LM 2001. Cloning, transcription and chromosomal localization of the porcine whey acidic protein gene and its expression in HC11 cell line. Gene 267, 37–47.Google Scholar
Rival-Gervier, S, Viglietta, C, Maeder, C, Attal, J, Houdebine, LM 2002. Position-independent and tissue specific expression of porcine whey acidic protein gene from a bacterial artificial chromosome in transgenic mice. Molecular Reproduction and Development 63, 161–167.CrossRefGoogle ScholarPubMed
Rival-Gervier, S, Maeder, C, Viglietta, C, Prince, S, Houdebine, LM 2003. Effect of 5′HS4 insulator on rabbit WAP gene action in transgenic mice. Transgenic Research 12, 723–730.CrossRefGoogle Scholar
Saidi, S, Rival-Gervier, S, Daniel-Carlier, N, Thépot, D, Morgenthaler, C, Viglietta, C, Prince, S, Passet, B, Houdebine, LM, Jolivet, G 2007. Distal control of the pig whey acidic protein (WAP) locus in transgenic mice. Gene 15, 97–107.Google Scholar
Schaerer, E, Devinoy, E, Kraehenbuhl, JP, Houdebine, LM 1988. Sequence of the rabbit beta-casein cDNA: comparison with other casein cDNA sequences. Nucleic Acids Research 16, 11814.CrossRefGoogle ScholarPubMed
Schmidt, C 2006. Belated approval of first recombinant protein from animal. Nature Biotechnology 24, 877.Google Scholar
Shackleton, M, Vaillnat, F, Simpson, KJ, Stingl, J, Smyth, GK, Asselin-Labat, ML, Wu, L, Lindeman, GJ, Visvader, JE 2006. Generation of a functional mammary gland from a single stem cell. Nature 439, 84–88.CrossRefGoogle ScholarPubMed
Shuster, RC, Houdebine, LM, Gaye, P 1976. Studies on the synthesis of casein messenger RNA during pregnancy in the rabbit. European Journal of Biochemistry 71, 193–199.Google Scholar
Soler, E, Le Saux, A, Guinut, F, Passet, B, Cohen, R, Merle, C, Charpilienne, A, Fourgeux, C, Sorel, V, Piriou, A, Schwartz-Cornil, I, Cohen, J, Houdebine, LM 2005. Production of two vaccinating recombinant rotavirus proteins in the milk of transgenic rabbits. Transgenic Research 14, 833–844.Google Scholar
Soler, E, Thépot, D, Rival-Gervier, S, Jolivet, G, Houdebine, LM 2006. Preparation of recombinant proteins in milk to improve human and animal health. Reproduction, Nutrition, Development 46, 579–588.CrossRefGoogle ScholarPubMed
Sternlicht, MD 2006. Key stages in mammary gland development: the cues that regulate ductal branching morphogenesis. Breast Cancer Research 8, 201.Google Scholar
Strömqvist, M, Houdebine, LM, Andersson, JO, Edlund, A, Johanson, T, Viglietta, C, Puissant, C, Hannson, L 1996. Recombinant human extracellular superoxide dismutase produced in milk of transgenic rabbits. Transgenic Research 6, 271–278.CrossRefGoogle Scholar
Taboit-Dameron, F, Malassagne, B, Viglietta, C, Puissant, C, Leroux-Coyau, M, Chereau, C, Attal, J, Weill, B, Houdebine, LM 1999. Association of the 5′HS4 sequence of the chicken beta-globin locus control region with human EF1 alpha gene promoter induces ubiquitous and high expression of human CD55 and CD59 cDNAs in transgenic rabbits. Transgenic Research 8, 223–235.Google Scholar
Thépot, D, Devinoy, E, Fontaine, ML, Hubert, C, Houdebine, LM 1990a. Complete sequence of the rabbit whey acidic protein gene. Nucleic Acids Research 18, 3641.Google Scholar
Thépot, D, Devinoy, E, Fontaine, ML, Houdebine, LM 1990b. Structure of the gene encoding rabbit beta-casein. Gene 97, 301–306.Google Scholar
Thépot, D, Devinoy, E, Fontaine, ML, Stinnakre, MG, Massoud, M, Kann, G, Houdebine, LM 1995. Rabbit whey acidic protein gene upstream region controls high-level expression of bovine growth hormone in the mammary gland of transgenic mice. Molecular Reproduction and Development 42, 261–267.CrossRefGoogle ScholarPubMed
Tong, Q, Hotamisligh, GS 2007. Cell fate in the mammary gland. Nature 445, 724–726.CrossRefGoogle ScholarPubMed
Tourkine, N, Schindler, C, Larose, M, Houdebine, LM 1995. Activation of STAT factors by prolactin, interferon-gamma, growth hormones, and a tyrosine phosphatase inhibitor in rabbit primary mammary epithelial cells. Journal of Biological Chemistry 270, 20952–20961.Google Scholar