Evolution of immune functions of the mammary gland and protection of the infant

Breastfeeding Medicine

Volumn 7, Issue 3, 2012, Pages 132-142

  Goldman, Armond S ^a  

^a University of Texas Medical Branch School of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BREAST MILK; ENVIRONMENTAL CHANGE; EVOLUTION; HEREDITY; HUMAN; IMMUNE FUNCTION TEST; LACTATION; LEUKOCYTE; MAMMARY GLAND; MARSUPIAL; MONOTREMATE; NONHUMAN; OROPHARYNX; PALATE; PLACENTAL MAMMALS; PRIORITY JOURNAL; REVIEW; SKIN GLAND;

ANIMALS; BIOLOGICAL EVOLUTION; BREAST; FEMALE; HUMANS; IMMUNE SYSTEM; IMMUNITY, MATERNALLY-ACQUIRED; INFANT; INFANT, NEWBORN; MAMMARY GLANDS, ANIMAL; MILK, HUMAN; PREGNANCY;

EID: 84863956544     PISSN: 15568253     EISSN: 15568342     Source Type: Journal    
DOI: 10.1089/bfm.2012.0025     Document Type: Review

References (123)

1. Owen R. Report on British Fossil Reptiles, Part 2. Report on the Eleventh Meeting of the British Association for the Advancement of Science Held in Plymouth, England in July 1841. Murray, London, 1842.
2. Sereno PC. The evolution of dinosaurs. Science 1999;284: 2137-2147. (Pubitemid 29297468)
3. nd ed. (Weishampel DB, Dodson P, Osmólska H, eds.). University of California Press, Berkeley, 2004, pp. 7-19.
4. Lloyd GT, Davis KE, Pisani D, et al. Dinosaurs and the Cretaceous terrestrial revolution. Proc R Soc Biol 2008; 275:2483-2490.
5. Schmidt AR, Ragazzi E, Copplellotti O, et al. A microworld in Triassic amber. Nature 2006;444:835. (Pubitemid 46024987)
6. Perri E, Tucker M. Bacterial fossils and microbial dolomite in Triassic stromatolites. Geology 2007;35:207-210. (Pubitemid 46437822)
7. Irmis RB, Nesbitt SJ, Pardian K, et al. A late Triassic dino-sauromorph assemblage from New Mexico and the rise of dinosaurs. Science 2007;317:358-361. (Pubitemid 47106373)
8. Martinez RN, Sereno PC, Alcober OA, et al. A basal dinosaur from the dawn of the dinosaur era in Southwestern Pangaea. Science 2011;331:206-210.
9. Sanchez-Villagra MR. Developmental palaeontology in synapsids: The fossil record of ontogeny in mammals and their closest relatives. Proc Biol Sci 2010;277:1139-1147.
10. Romer AS. Cynodont reptile with incipient mammalian jaw articulation. Science 1969;166:681-682.
11. Davis D. Origin of the mammalian feeding mechanism. Am Zoologist 1961;1061;1:229-234.
12. Gould SJ, Vrba ES. Exaptation-A missing term in the science of form. Paleobiology 1982;8:4-15. (Pubitemid 13281606)
13. Lillegraven JA, Kielan-Jaworowska Z, Clemens WA. Me-sozoic Mammals: The First Two-Thirds of Mammalian History. University of California Press, Berkeley, 1979.
14. Damiani R, Modesto S, Yates A, et al. Earliest evidence of cynodont burrowing. Proc Biol Sci R Soc 2003;270:1747-1751. (Pubitemid 37041297)
15. Kielan-Jaworowska Z, Hurum JH. Phylogeny and system-atics of multituberculate mammals. Palaeontology 2001;44: 389-429.
16. Metchnikoff E. Untersuchung ü ber die intracelluläre Verdauung beim wirbellosen Tieren. Arb Zool Inst Universitaet Wien Zool Station Thriest (Wien) 1883;5:141-68.
17. Metchnikoff E. Untersuchung über die mesodermalen Phagocyten einiger Wirbeltiere. Biol Centralblatt 1883;3:560-565.
18. Metchnikoff E. Uber eine Sprosspilzkrankheit der Daphnien: Beitrag zur Lehre über den Kampf der Phagocyten gegen Krankheitserreger. Arch Pathol Anat Physiol Klin Med 1884;96:177-195.
19. Metchnikoff E. Immunity in Infectious Diseases. Cambridge University Press, Cambridge, UK, 1905.
20. Frank SA. Immunology and Evolution of Infectious Disease. Princeton University Press, Princeton, NJ, 2002.
21. Lander ES, Linton LM, Birren B, et al. Initial sequencing and analysis of the human genome. Nature 2001;409:860-921. (Pubitemid 32165345)
22. Barclay AN. Membrane proteins with immunoglobulin-like domains-A master superfamily of interaction molecules. Semin Immunol 2003;15:215-223. (Pubitemid 38167234)
23. Musser AM, Archer M. New information about the skull and dentary of the Miocene platypus Obdurodon dicksoni, and a discussion of ornithorhynchid relationships. Philos Trans R Soc Lond B Biol Sci 1998;353:1063-1979.
24. Vullo R, Gheerbrant E, de Muizon C, et al. The oldest modern therian mammal from Europe and its bearing on stem marsupial paleobiogeography. Proc Natl Acad Sci U S A 2009;106:19910-19915.
25. Ji Q, Luo ZX, Yuan CX, et al. The earliest known eutherian mammal. Nature 2002;416:816-822. (Pubitemid 34453732)
26. Bininda-Emonds ORP, Cardillo M, Jones KE, et al. The delayed riseofpresent-day mammals. Nature 2007;446:507-512.
27. Stewart ME. Sebaceous gland lipids. Semin Dermatol 1992; 11:100-105.
28. Qasba PK, Kumar S. Molecular divergence of lysozymes and a-lactalbumin. Crit Rev Biochem Mol Biol 1997;32:255-306.
29. Ansai S, Koseki S, Hozumi Y, Kondo S. An immunohisto-chemical study of lysozyme, CD-15 (Leu M1), and gross cystic disease fluid protein-15 in various skin tumors. Assessment of the specificity and sensitivity of markers of apocrine differentiation. Am J Dermatopathol 1995;17:249-255.
30. Alemany R, Vila MR, Franci C, et al. Glycosyl phosphati-dylinositol membrane anchoring of melanotransferrin (p97): Apical compartmentalization in intestinal epithelial cells. J Cell Sci 1993;104:1155-1162. (Pubitemid 23154323)
31. Blackburn DG, Hayssen V, Murphy CJ. The origins of lactation and the evolution of milk-A review with new hypotheses. Mammal Rev 1989;19:1-26. (Pubitemid 19325661)
32. Brawand D, Wahli W, Kaessmann H. Loss of egg yolk genes in mammals and the origin of lactation and placen-tation. PLoS Biol 2008;6:e63.
33. Griffiths M. The platypus. Sci Am 1988;258:84-91.
34. Rens W, O'Brien PC, Grützner F, et al. The multiple sex chromosomes of platypus and echidna are not completely identical and several share homology with the avian Z. Genome Biol 2007;8:R243.
35. Warren WC, Hillier LW, Marshall Graves JA, et al. Genome analysis of the platypus reveals unique signatures of evolution. Nature 2008;453:175-183. (Pubitemid 351667983)
36. Owen R. On the mammary glands of the Ornithorhynchus paradoxus. Philos Trans R Soc Lond 1832;122:517-538.
37. Killian JK, Buckley TR, Stewart N, et al. Marsupials and Eutherians reunited: Genetic evidence for the Theria hypothesis of mammalian evolution. Mamm Genome 2001; 12:513-517. (Pubitemid 32552765)
38. Nilsson MA, Churakov G, Sommer M, et al. Tracking marsupial evolution using archaic genomic retroposon insertions. PLoS Biol 2010;8:e1000436.
39. Capuco AV, Akers RM. The origin and evolution of lactation. J Biol 2009;8:37.
40. Nicholas KR, Messer M, Elliott C, et al. A novel whey protein synthesized only in late lactation by the mammary gland from the tammar (Macropus eugenii). Biochem J 1987;241:899-904.
41. Young L, Basden K, Cooper DW, et al. Cellular components of the milk of the tammar wallaby (Macropus eugenii). Aust J Zool 1997;45:423-433. (Pubitemid 27484288)
42. Piotte CP, Marshall CJ, Hubbard M.J, Collet C, Grigor MR. Lysozyme and a-lactalbumin from the milk of a marsupial, the common brush-tailed possum (Trichosurus vulpecula). Biochim Biophys Acta 1997;1336:235-242. (Pubitemid 27364178)
43. Adamski FM, Demmer J. Immunological protection of the vulnerable marsupial pouch young: Two periods of immune transfer during lactation in Trichosurus vulpecula (brushtail possum). Dev Comp Immunol 2000;24:491-502. (Pubitemid 30227352)
44. Joss JL, Molloy MP, Hinds L, et al. A longitudinal study of the protein components of marsupial milk from birth to weaning in the tammar wallaby (Macropus eugenii). Dev Comp Immunol 2009;33:152-161.
45. Daly KA, Digby M, Lefèvre C, et al. Analysis of the expression of immunoglobulins throughout lactation suggests two periods of immune transfer in the tammar wallaby (Macropus eugenii). Vet Immunol Immunpathol 2007; 120:187-200. (Pubitemid 47632814)
46. Khalil E, Digby MR, O'Donnell P, et al. Changes in milk protein composition during acute involution at different phases of tammar wallaby (Macropus eugenii) lactation. Comp Biochem Physiol B Biochem Mol Biol 2008;151:64-69.
47. Archibald JD, Rose KD. Introduction. In: The Rise of Pla-cental Mammals (Rose KD, Archibald JD, eds.). Johns Hopkins University Press, Baltimore, 2005, pp. 1-8.
48. Wildman DE, Chen C, Erez O, et al. Evolution of the mammalian placenta revealed by phylogenetic analysis. Proc Natl Acad Sci U S A 2006;103:3203-3208. (Pubitemid 43346448)
49. Brawand D, Wahli W, Kaessmann H. Loss of egg yolk genes in mammals and the origin of lactation and placen-tation. PLoS Biol 2008;6:e63.
50. Eizirik E, Murphy WJ, O'Brien SJ. Molecular dating and biogeography of the early placental mammal radiation. J Hered 2001;92:212-219. (Pubitemid 32521993)
51. Easteal S. Molecular evidence for the early divergence of placental mammals. Bioessays 1999;21:1052-1058.
52. Murphy WJ, Eizirik E, O'Brien SJ, et al. Resolution of the early placental mammal radiation using Bayesian phylo-genetics. Science 2001;294:2348-2351. (Pubitemid 33140557)
53. Hill A, Ward S, Deino A, et al. Earliest Homo. Nature 1992;355:719-722.
54. Wood B. Origin and evolution of the genus Homo. Nature 1992;355:783-790.
55. Takahata N, Satta Y, Klein J. Divergence time and population size in the lineage leading to modern humans. Theor Popul Biol 1995;48:198-221. (Pubitemid 26460272)
56. Ayala FJ. The myth of Eve: Molecular biology and human origins. Science 1995;270:1930-1936. (Pubitemid 26097180)
57. Hammer MF. A recent common ancestry for human Y chromosomes. Nature 1995;378:376-378.
58. Goodman M, Bailey WJ, Hayasaka K, et al. Molecular evidence on primate phylogeny from DNA sequences. Am J Phys Anthropol 1994;94:3-24. (Pubitemid 24136795)
59. Shoshani J, Groves CP, Simons EL, et al. Primate phylog-eny: Morphological vs. molecular results. Mol Phylogenet Evol 1996;5:102-154. (Pubitemid 126317000)
60. Edwards JH. Comparative genome mapping in mammals. Curr Opin Genet Dev 1994;4:861-867.
61. Pemberton L, Taylor-Papadimitriou J, Gendler SJ. Antibodies to the cytoplasmic domain of the MUC 1 mucin show conservation throughout mammals. Biochem Biophys Res Commun 1992;185:167-175.
62. Braathen R, Hohman VS, Brandtzaeg P, et al. Secretory antibody formation: Conserved binding interactions between J chain and polymeric Ig receptor from humans and amphibians. J Immunol 2007;178:1589-1597. (Pubitemid 46154630)
63. Newburg DS. Oligosaccharides and glycoconjugates in human milk: Their role in host defense. J Mammary Gland Biol Neoplasia 1996;1:271-283.
64. Gopal PK, Gill HS. Oligosaccharides and glycoconjugates in bovine milk and colostrum. Br J Nutr 2000;84 (Suppl 1):S69-S74. (Pubitemid 32106831)
65. Warren CD, Chaturvedi P, Newburg AR, et al. Comparison of oligosaccharides in milk specimens from humans and twelve other species. Adv Exp Med Biol 2001;501:325-332. (Pubitemid 34102212)
66. Norcross NL. Secretion and composition of colostrum and milk. J Am Vet Med Assoc 1982;181:1057-1060. (Pubitemid 13215471)
67. Goldblum RM, Garza C, Johnson CA, et al. Human milk banking. II. Relative stability of immunologic factors in stored colostrum. Acta Paediatr Scand 1982;71:143-144.
68. Goldman AS, Garza C, Johnson CA, et al. Immunologic factors in human milk during the first year of lactation. J Pediatr 1982;100:563-567. (Pubitemid 12136026)
69. Goldman AS, Goldblum RM, Garza C. Immunologic components in human milk during the second year of lactation. Acta Paediatr Scand 1983;72:461-462. (Pubitemid 13088031)
70. Tizard I. The protective properties of milk and colostrum in non-human species. Adv Nutr Res 2001;10:130-166.
71. Sanchez L, Aranda P, Pérez MD, et al. Concentration of lac-toferrin and transferrin throughout lactation in cow's colostrum and milk. Biol Chem Hoppe Seyler 1988;369:1005-1008.
72. Goudswaard J, Bakker-de Koff EC, van Ravenswaaij-Kraan HP. Lysozyme and its presence in bovine milk and serum. Tijdschr Diergeneeskd 1978;103:445-350.
73. Gothefors L, Marklund S. Lactoperoxidase activity in human milk and in saliva of newborn infants. Infect Immun 1975;11:1210-1215.
74. Reiter B. The lactoperoxidase system of bovine milk. In: The Lactoperoxidase System: Chemistry and Biologic Significance (Pritt RM, Tenovuo J, eds.). Marcel Dekker, New York, 1985, pp. 123-144.
75. Schroten H. Chemistry of milk mucins and their antimicrobial action. Adv Nutr Res 2001;10:231-245.
76. Olson JC, Leslie GA. IgD: A component of the secretory immune system? Ann N Y Acad Sci 1982;399:97-104. (Pubitemid 13139677)
77. Ohta Y, Flajnik M. IgD, like IgM, is a primordial immu-noglobulin class perpetuated in most jawed vertebrates. Proc Natl Acad Sci U S A 2006;103:10723-10728. (Pubitemid 44081629)
78. Chen K, Cerutti A. New insights into the enigma of im-munoglobulin D. Immunol Rev 2010;237:160-179.
79. Thatcher EF, Gershwen LJ. Colostral transfer of bovine immunoglobulin E and dynamics of serum IgE in calves. Vet Immunol Immunopathol 1989;29:325-334. (Pubitemid 19103569)
80. Kashiwakura J, Xiao W, Kitaura J, et al. Pivotal advance: IgE accelerates in vitro development of mast cells and modifies their phenotype. J Leukoc Biol 2008;84:357-367.
81. Gruber JW. A Consciousness in Conflict: The Life of St. George Jackson Mivart. Columbia University Press, New York, 1960.
82. Mivart SG. On the Genesis of Species. D. Appleton, New York, 1871.
83. Darwin C. On The Origins of Species, by Means of Natural Selection or the Preservation of Favoured Races in the Struggle for Life. J Murray, London, 1859.
84. th ed. J Murray, London, 1872.
85. Haldane JBS. The possible evolution of lactation. Zool Jahrbücher Abt Syst Okol Geol Tiere 1965;92:4-8.
86. Oftedal OT. The mammary gland and its origin during synapsid evolution. J Mammary Gland Biol Neoplasia 2002;7: 225-252. (Pubitemid 38418023)
87. Oftedal OT. The origin of lactation as a water source for parchment-shelled eggs. J Mammary Gland Biol Neoplasia 2002;7:253-266. (Pubitemid 38410713)
88. Liu J, Linwin DM, Deeming DC, et al. An egg-adult association, gender, and reproduction in pterosaurs. Science 2011;331:321-324.
89. Gwee PC, Tay BH, Brenner S, et al. Characterization of the neurohypophysial hormone gene loci in elephant shark and the Japanese lamprey: Origin of the vertebrate neuro-hypophysial hormone genes. BMC Evol Biol 2009;9:47.
90. Rossoni E, Feng J, Tirozzi B, et al. Emergent synchronous bursting of oxytocin neuronal network. PLoS Comput Biol 2008;4:e1000123.
91. Leng G, Ludwig M. Neurotransmitters and peptides: Whispered secrets and public announcements. J Physiol 2008;586:5625-5632.
92. Foitzik K, Krause K, Conrad F, et al. Human scalp hair follicles are both a target and a source of prolactin, which serves as an autocrine and/or paracrine promoter of apoptosis-driven hair follicle regression. Am J Pathol 2006; 168:748-756. (Pubitemid 43327727)
93. Keil W, von Stralendorff F, Hudson R. A behavioral bio-assay for analysis of rabbit nipple-search pheromone. Physiol Behav 1990;47:525-529. (Pubitemid 20120966)
94. Sternlicht MD. Key stages in mammary gland development: The cues that regulate ductal branching morphogenesis. Breast Cancer Res 2006;8:201.
95. Fata JE, Werb Z, Bissell MJ. Regulation of mammary gland branching morphogenesis by the extracellular matrix and its remodeling enzymes. Breast Cancer Res 2004;6:1-11. (Pubitemid 38195555)
96. Shyamala G, Chou Y-C, Louie SG, et al. Cellular expression of estrogen and progesterone receptors in mammary glands: Regulation by hormones, development and aging. J Steroid Biochem Molecular Biol 2002;80:137-148. (Pubitemid 34233736)
97. Trott JF, Vonderhaar BK, Hovey RC. Historical perspectives of prolactin and growth hormone as mammogens, lactogens and galactagogues-Agog for the future! J Mammary Gland Biol Neoplasia 2008;13:3-11.
98. Hamosh M, Dewey KG, Garza C, et al. Nutrition During Lactation. National Academy Press, Washington, DC, 1991, pp. 153-196.
99. Speakman JR. The physiological costs of reproduction in small mammals. Philos Trans R Soc Lond B Biol Sci 2008;363: 375-398. (Pubitemid 350249333)
100. Bonner WN. Lactation strategies in pinnipeds: Problems for a marine mammalian group. Symp Zool Soc Lond 1984;51: 253-272.
101. Dosako S, Taneya S, Kimura T, et al. Milk of northern fur seal: Composition, especially carbohydrate and protein. J Dairy Sci 1983;66:2076-2083.
102. Goldman AS, Chheda S, Garofalo R. Evolution of immu-nological functions of the mammary gland and the postnatal development of immunity. Pediatr Res 1998;43:155-162. (Pubitemid 28086351)
103. Goldman AS. Modulation of the gastrointestinal tract of infants by human milk. Interfaces and interactions. An evolutionary perspective. J Nutr 2000;130(2S Suppl):426S-431S. (Pubitemid 30073764)
104. Goldman AS. Evolution of the mammary gland defense system and ontogeny of the immune system. J Mammary Gland Biol Neoplasia 2002;7:277-289. (Pubitemid 38410715)
105. Porter P. Immunoglobulins in bovine mammary secretions: Quantitative changes in early lactation and absorption by the neonatal calf. Immunology 1972;23:225-238.
106. Simister NE, Story CM. Human placental Fc receptors and the transmission of antibodies from mother to fetus. J Re-prod Immunol 1997;37:1-23. (Pubitemid 28052668)
107. Goldman AS. The immune system in human milk and the developing infant. Breastfeed Med 2007;2:195-204. (Pubitemid 350274440)
108. Goldman AS, Chheda S, Keeney SE, et al. Immunology of human milk and host immunity. In: Fetal and Neonatal Physiology (Polin RL, Abman S, Fox W, eds.). Elsevier, Philadelphia, 2011, pp. 1690-1701.
109. Lemay DG, Lynn DJ, Martin WF, et al. The bovine lactation genome: Insights into the evolution of mammalian milk. Genome Biol 2009;10:R43.
110. Brew K, Vanaman TC, Hill RL. The role of a-lactalbumin and the A protein in lactose synthetase. A unique mechanism for the control of a biological reaction. Proc Natl Acad Sci U S A 1968;59:491-497.
111. Prager EM, Jollès P. Animal lysozymes C and G: An overview. In: Lysozymes: Model Enzymes in Biochemistry and Biology (Jollès P, ed.). Birkhäuser Verlag, Basel, 1996, pp. 9-31.
112. Spik G, Coddeville B, Montreuil J. Comparative study of the primary structures of sero-, lacto- and ovotransferrin glycans from different species. Biochimie 1988;70:1459-1469.
113. Giansanti F, Rossi P, Massucci MT, et al. Antiviral activity of ovotransferrin discloses an evolutionary strategy for the defensive activities of lactoferrin. Biochem Cell Biol 2002;80: 125-130. (Pubitemid 34194238)
114. Kang JF, Li XL, Zhou RY, et al. Bioinformatics analysis of lactoferrin gene for several species. Biochem Genet 2008;46: 312-322.
115. 13C-n.m.r. spectroscopy. Carbohydr Res 1984;126:157-161.
116. Teahan CG, McKenzie HA, Griffiths M. Some monotreme milk "whey" and blood proteins. Comp Biochem Physiol B 1991;99:99-118.
117. Teahan CG, McKenzie HA. Iron (III) binding proteins of echidna (Tachyglossus aculeatus) and platypus (Ornithor-hynchus anatinus). Biochem Int 1990;22:321-328.
118. Armitage SJ, Jasim SA, Marks AE, et al. The southern route "out of Africa": Evidence for an early expansion of modern humans into Arabia. Science 2011;331:453-456.
119. Blum MG, Jakobsson M. Deep divergences of human gene trees and models of human origins. Mol Biol Evol 2011; 28:889-898.
120. de Menocal PB. Anthropology. Climate and human evolution. Science 2011;331:540-542.
121. Goldblum RM, Dill CW, Albrecht TB, et al. Rapid high temperature treatment of human milk. J Pediatr 1984; 104:380-385. (Pubitemid 14160463)
122. Untalan PB, Keeney SE, Palkowetz KH, et al. Heat susceptibility of interleukin-10 and other cytokines in donor human milk. Breastfeed Med 2009;4:137-144.
123. Goldman AS, Hopkinson JM, Rassin DK. Benefits and risks of breastfeeding. Adv Pediatr 2007;54:275-304.