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Influence of Hormones on Synthesis and Secretion of Milk Proteins by Mammary Tissue from Male and Female Cattle of Beef and Dairy Breeds

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Influence of Hormones on Synthesis and Secretion of Milk Proteins by Mammary Tissue from Male and Female Cattle of Beef and Dairy Breeds INFLUENCE OF HORMONES ON SYNTHESIS AND SECRETION OF MILK PROTEINS BY MAMMARY TISSUE FROM MALE AND FEMALE CATTLE OF BEEF AND DAIRY BREEDS by Thomas Bernard McFadden Thesis submitted to the Faculty of the Virginia Polytechnic Institute and State University in partial fulfillment of the requirements for the degree of MASTER OF SCIENCE in Dairy Science APPROVED: R.M. Akers, Chairman W.E. Beal F.C. Gwazdauskas J.M. White, Department Head March, 1985 Blacksburg, Virginia INFLUENCE OF HORMONES ON SYNTHESIS AND SECRETION OF MILK PROTEINS BY MAMMARY TISSUE FROM MALE AND FEMALE CATTLE OF BEEF AND DAIRY BREEDS by Thomas B. McFadden (ABSTRACT) The ability of mammary tissue from prepubertal bulls and heifers of beef and dairy breeds to respond to hormonal stimuli through synthesis and secretion of milk proteins was studied. Experimental animals were six to eight month old Angus and Holstein cattle. All subjects were injected with estradiol and progesterone for seven days and slaughtered on day 15. Mammary tissue was explanted and cultured for 96 h in basal medium (B) which contained hormones necessary for maintenance, or stimulatory medium (P), further supplemented with prolactin. Selected cultures were incubated for 24 h in B or P medium containing 3 H-amino acids. Concentrations of non-labeled alpha-lactalbumin (Alac), 3 H-Alac, and 3 H-total protein (TP) were determined in media and in ex- plant homogenates. Among cultures of bull mammary tissue, Angus explants secreted greater overall quantities of 3 H-TP and 3 H-Alac than Holstein explants (p<.05). Secretion of Alac was also greater in Angus cultures at two of eight treatment periods (p<.01). Concentrations of all three protein fractions were likewise enhanced in homogenates of Angus explants for at least three of four treatment periods (p~.05). Presence of prolactin in medium stimulated secretion of Alac (p<.005), and accumulation of all three fractions in explants (p<.10). Holstein heifer explants secreted more Alac at three of eight treatment periods than Angus explants (p<.0005). Ove- rall secretion of 3 H-TP and 3 H-Alac also was elevated in Holstein over Angus females (p<.10), as were concentrations of all three fractions in homogenates (p~.01). Presence of prolactin had no direct effect on any protein parameters in female tissue. I conclude that mammary tissue of immature bulls and heifers can be hormonally induced to express it's genetic merit for milk production (based on breed differences), through synthesis and secretion of milk proteins. Prolactin stimulated protein production in bulls but not in heifers. These findings indicate that similar methods of stimulating mammary tissue to produce milk proteins may be adaptable for commercial evaluation of genetic potential for milk produc- tion, especially in young bulls. ACKNOWLEDGEMENTS I would like to express my sincere appreciation to the following people, who were instrumental in helping me pre- pare this thesis: Dr. R.M. Akers - I am convinced that I couldn't find a better major professor anywhere, which explains why I'm staying on for a PhD. Need I say more? Dr. W.E. Beal - For many and varied instances of assis- tance and encouragement, but particularly for his enthusiasm toward, and philosophies of teaching. Dr. F.C. Gwazdauskas - For much valuable classroom in- struction as well as encouragement and advice throughout my graduate studies. Dr. J.M. White - For exceptional enthusiasm and support toward myself and the entire department, not to mention some good jokes. Many thanks and a few apologies are due my wife, Holli, who more than anyone bore the brunt of my own special brand of thesis blues. Her constant love and encouragement prac- tically earned her a co-authorship. Finally I thank God for giving me the health and strength to complete this task. iii TABLE OF CONTENTS ABSTRACT ii ACKNOWLEDGEMENTS iii Chapter I. INTRODUCTION 1 I I. REVIEW OF LITERATURE 3 Induced Lactation and Mammary Growth 3 Hormonal Control of Lactogenesis: Laboratory Species . 18 Hormonal Control of Specific Protein Synthesis, In Vitro . 24 Hormonal Control of Lactogenesis: Ruminants 28 Lactation in Male Mammals 37 III. MATERIALS AND METHODS 42 Animals . 42 Hormone Pretreatment of Subjects 43 Organ Culture of Mammary Explants 43 Incubation Medium .... 44 Incubation Protocol 46 3 H-Thymidine Incorporation 48 3 H-protein Quantification 49 Protein Radioimmunoassays (RIAs) . 52 Statistical Methods 52 IV. RESULTS . 53 Experiment I. Males 53 Media Alpha-lactalbumin ........ 53 3 H-Total Protein and Alpha-lactalbumin in Media . 54 3 H-Total Protein and Alpha-lactalbumin in Homogenates ........... 56 Non-radiolabeled Alpha-lactalbumin Concentrations in Media and Explant Homogenates ........... 60 Synthesis versus Secretion of Proteins by Cultured Mammary Explants from Angµs and Holstein Bulls 64 Correlations 71 iv 3 H-Thymidine Incorporation into Mammary Explant DNA. 71 Serum Prolactin and Alpha-lactalbumin 73 Experiment II. Females . 73 Media Alpha-lactalbumin. 73 3 H-Total Protein and Alpha-lactalbumin in Media . 75 3 H-Total Protein and Alphalactalbumin in Explant Homogenates . 79 Non-radiolabeled Alpha-lactalbumin in Media and Homogenates . 83 Synthesis versus Secretion of Proteins by Cultured Mammary Explants from Angus and Holstein Heifers . 86 Correlations . 90 3 H-Thymidine Incorporation into Mammary Explant DNA. 92 Serum Prolactin and Alpha-lactalbumin 92 v. DISCUSSION 96 Experiment I. Males 96 General 96 Breed Differences . 97 Effect of Treatment and Incubation Time on Productive Indices . 102 Synthesis versus Secretion of Milk Proteins 104 Other Considerations 106 Experiment II. Females 111 General . 111 Breed Differences. 112 Effect of Treatment on Protein Synthesis and Secretion .............. 113 Synthesis versus Secretion of Milk Proteins 116 Other Considerations 118 VI. SUMMARY AND CONCLUSIONS .. 121 LITERATURE CITED 125 VII. APPENDIX A 134 V LIST OE' TABLES Table 1. Synthesis and secretion of milk proteins by cultured mammary explants from Angus and Holstein bulls .. 68 2. Incorporation of 3 H-thymidine into DNA of mammary explants from Angus and Holstein bulls. 73 3. Concentrations of prolactin in serum of Angus and Holstein bulls during steroid pretreatment. 75 4. Synthesis and secretion of milk proteins by cultured mammary explants from Angus and Holstein heifers. 90 5. Incorporation of 3 H-thymidine into DNA of mammary explants from Angus and Holstein heifers. 94 6. Concentrations of prolactin in serum of Angus and Holstein heifers during steroid pretreatment ... 95 vi LIST OE' FIGURES Figure 1. Secretion of Alac into medium by mammary explants from Angus and Holstein bulls. .... 55 2. Secretion of 3 H-TP into media by Angus and Holstein bull explants. ... 57 3. Secretion of 3 H-Alac into media by Angus and Holstein bull explants. ... 58 4. Concentrations of 3 H-TP in homogenates of Angus and Holstein bull explants . 60 5. Concentrations of 3 H-Alac in homogenates of Angus and Holstein bull explants ............ 61 6. Secretion of non-radiolabeled Alac into media by bull explants exposed to 3 H-amino acids during culture. 64 7. Concentrations of non-radiolabeled Alac in homogenates of bull explants exposed to 3 H-amino acids during culture ............... 65 8. Secretion of Alac into medium by mammary explants from Angus and Holstein heifers. .... 76 9. Secretion of 3 H-TP into media by Angus and Holstein heifer explants. ... 78 10. Secretion of 3 H-Alac into media by Angus and Holstein heifer explants. ... 79 11. Concentrations of 3 H-TP in homogenates of Angus and Holstein heifer explants ............. 82 12. Concentrations of 3 H-Alac in homogenates of Angus and Holstein heifer explants ........... 84 13. Secretion of non-radiolabeled Alac into media by heifer explants exposed to 3 H-amino acids during culture. ................... 87 vii 14. Concentrations of non-radiolabeled Alac in homogenates of heifer explants exposed to 3 H- amino acids during culture. 88 viii Chapter I INTRODUCTION Mammary growth and milk production are highly-integrated, hormonally- regulated developmental processes, which ulti- mately allow the mammalian mother to provide for the nour- ishment of her offspring. In the dairy cow, a lactating fe- male provides milk not only for her progeny, but also for a host of "symbiotic" humans as well, thus forming the basis of the dairy industry. It is this outside demand for milk which has lead to the extreme specialization of dairy breeds, and which exerts a profound demand for ever-increas- ing efficiency of milk production. The critical role of hormones and genetic merit of individual animals in deter- mining milk yield has stimulated much research activity; hormonal induction of lactation and sire-selection programs being primary examples of each. Because hormones play an essential role in eliciting ex- pression of genes involved in production of milk, endocri- nology and genetics may be studied as integrated elements directed toward a common goal, milk production. This con- cept formed the basis for the present study. Expression of differential in genetic potential for milk production, mea- sured by synthesis and secretion of milk proteins, was stu- 1 2 died through hormonal manipulation of mammary tissue from high- (dairy) and low- (beef) yielding breeds, in vivo and in vitro. Thus the primary objective of this thesis was to develop a "bioassay" for genetic potential to produce milk. Such a system might find applications in the sire selection industry, and also yields useful information on hormonal control of genes involved in milk production. Maximal se- lection for, and expression of these genes are the major goals of research related to the dairy industry. Chapter II REVIEW OF LITERATURE INDUCED LACTATION AND MAMMARY GROWTH The influence of the reproductive tract on the develop- ment of the mammary gland has long been apparent. Increased mammary growth at puberty followed by more extensive devel- opment during pregnancy has been a clear indication of the relationship between reproductive status and mammary devel- opment.
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