Can an ancestral condition for milk oligosaccharides be determined? Evidence from the Tasmanian echidna (Tachyglossus aculeatus setosus)

Glycobiology

Volumn 24, Issue 9, 2014, Pages 826-839

  Oftedal, Olav T ^a   Nicol, Stewart C ^b   Davies, Noel W ^c   Sekii, Nobuhiro ^d   Taufik, Epi ^d,f   Fukuda, Kenji ^d   Saito, Tadao ^e   Urashima, Tadasu ^d  

^a SMITHSONIAN ENVIRONMENTAL RESEARCH CENTER   (United States)

^b School of Biological Sciences   (United States)

^c UNIVERSITY OF TASMANIA   (Australia)

^d OBIHIRO UNIVERSITY OF AGRICULTURE AND VETERINARY MEDICINE   (Japan)

^e TOHOKU UNIVERSITY   (Japan)

^f BOGOR AGRICULTURAL UNIVERSITY   (Indonesia)

Author keywords

evolution; fucosylated oligosaccharides; milk; monotreme; O acetyl sialyllactose

Indexed keywords

2' FUCOSYLLACTOSE; 3' SIALYLLACTOSE; 4 O ACETYL 3' SIALYL 3 FUCOSYLLACTOSE; 4 O ACETYL 3' SIALYLLACTOSE; 4 O ACETYL 3' SIALYLLACTOSE SULFATE; 4 O ACETYL 3' SIALYLLACTOSE SULFATE CORE; B PENTASACCHARIDE; B TETRASACCHARIDE; DI O ACETYL 3' SIALYLLACTOSE; DIFUCOSYLLACTOSE; LACTO N FUCOPENTAOSE III; LACTOSE; OLIGOSACCHARIDE; UNCLASSIFIED DRUG;

ACETYLATION; ARTICLE; CARBOHYDRATE ANALYSIS; DIGESTIVE SYSTEM; ECHIDNA; ELECTROSPRAY MASS SPECTROMETRY; FORAGING BEHAVIOR; GEL FILTRATION; HATCHLING; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; INTESTINE CELL; ION MONITORING; LACTATION; MATERNAL CARE; MICROBIAL DEGRADATION; MILK; MOLECULAR WEIGHT; NONHUMAN; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; TACHYGLOSSUS ACULEATUS SETOSUS; TANDEM MASS SPECTROMETRY; ULTRA PERFORMANCE LIQUID CHROMATOGRAPHY; ANIMAL; CHEMISTRY; GENETICS; METABOLISM; MOLECULAR EVOLUTION;

ANIMALS; ECHIDNA; EVOLUTION, MOLECULAR; MILK; OLIGOSACCHARIDES;

EID: 84905513263     PISSN: 09596658     EISSN: 14602423     Source Type: Journal    
DOI: 10.1093/glycob/cwu041     Document Type: Article

References (83)

1. Amano J, Messer M, Kobata A. 1985. Structures of the oligosaccharides isolated from milk of the platypus. Glycoconj J. 2:121-135.
2. Anraku T, Fukuda K, Saito T, Messer M, Urashima T. 2012. Chemical characterization of acidic oligosaccharides in milk of the red kangaroo (Macropus rufus). Glycoonj J. 29:147-156. doi: 10.1007/s10719-012-9372-7
3. Barra WC, Caputto R. 1965. Isolation and identification of a lactose sulphate ester from rat mammary gland. Biochim Biophys Acta. 101:367-369.
4. Bisana S, Kumar S, Rismiller P, Nicol SC, Lefèvre C, Nicholas KR, Sharp JA. 2013. Identification and functional characterization of a novel monotremespecific antibacterial protein expressed during lactation. PLoS ONE. 8(1): e53686. doi:10.1371/journal.pone.0053686
5. Bode L. 2012. Human milk oligosaccharides: Every baby needs a sugar mama. Glycobiology. 22:1147-1162. doi:10.1093/glycob/cws074
6. Bode L, Jantscher-Krenn E. 2012. Structure-function relationships of human milk oligosaccharides. Adv Nutr. 3:383S-391S; doi:10.3945/an.111.001404
7. Breton C, Šnajdrová L, Jeanneau C, Ko?a J, Imberty A. 2006. Structures and mechanisms of glycosyltransferases. Glycobiology. 16:29R-37R.
8. Brew K. 2003. Alpha;-Lactalbumin. In: Fox PF, McSweeney PLH, editors. Advanced dairy chemistry-I. Proteins. Part A, vol. 1. New York (NY): Kluver Academic. p. 387-419.
9. Bubb WA, Urashima T, Kohso K, Nakamura T, Arai I, Saito T. 1999. Occurrence of an unusual lactose sulfate in dog milk. Carbohydr Res. 318:123-128.
10. Chai W, Piskarev VE, Mulloy M, Liu Y, Evans PG, Osborn HMI, Lawson AM. 2006. Analysis of chain and blood group type and branching pattern of sialylated oligosaccharides by negative ion electrospray tandem mass spectrometry. Anal Chem. 78:1581-1592. doi: 10.1021/ac051606e.
11. Choi HU, Carubelli R. 1968. Neuramin-lactose, neuramin-lactose sulfate, and lactose sulfate from rat mammary glands. Isolation, purification, and permethylation studies. Biochemistry. 7:4423-4430.
12. Collins JG, Bradbury JH, Trifonoff E, Messer M. 1982. Structures of four new oligosaccharides from marsupial milk, determined mainly by 13C-NMR spectroscopy. Carbohydr Res. 83:327-334.
13. Costache M, Apoil PA, Cailleau A, Elmgren A, Larson G, Henry S, Blancher A, Iordachescu D, Oriol R, Mollicone R. 1997. Evolution of fucosyltransferase genes in vertebrates. J Biol Chem. 272:29721-29728.
14. DeVries T, Knegtel RMA, Holmes EH, Mache BA. 2001. Fucosyltransferases: Structure/function studies. Glycobiology. 11:119R-128R.
15. Dickson JJ, Messer M. 1978. Intestinal neuraminidase activity of suckling rats and other mammals. Relationship to the sialic acid content of milk. Biochem J. 170:407-413.
16. Domon B, Costello CE. 1988. A systematic nomenclature for carbohydrate fragmentation in FAB-MS/MS Spectra of Glycoconjugates. Glycoconj J. 5:397-409.
17. Dubois M, Gills KA, Hamilton JK, Roberts PA, Smith F. 1956. Colorimetric method for determination of sugars and related substances. Anal Chem. 28:350-356.
18. Duncan PI, Raymond F, Fuerholz A, Sprenger N. 2009. Sialic acid utilisation and synthesis in the neonatal rat revisited. PLoS ONE. 4(12):e8241. doi:10.1371/journal.pone.0008241
19. Eisert R, Oftedal OT, Barrell GK. 2013a. Milk composition in the Weddell seal (Leptonychotes weddellii): Evidence for a functional role of milk carbohydrates in pinnipeds. Physiol Biochem Zool. 86:159-175. doi: 10.1086/669036
20. Eisert R, Potter C, Oftedal OT. 2013b. Brain size in neonatal and adult Weddell seals: Costs and consequences of having a large brain. Mar Mammal Sci. 30:184-205. doi: 10.1111/mms.12033
21. Galili U. 2005. The α-gal epitope and the anti-Gal antibody in xenotransplantation and in cancer immunotherapy. Immunol Cell Biol. 83:674-686. doi:10.1111/j.1440-1711.2005.01366.x
22. Garido D, Dallas DC, Mills DA. 2013. Consumption of human milk glycoconjugates by infant-associated bifidobacteria: Mechanisms and implications. Microbiology. 159:649-664. DOI 10.1099/mic.0.064113-0
23. Goldman AS. 2002. Evolution of the mammary gland defense system and the ontogeny of the immune system. J Mammary Gland Biol Neoplasia. 7:277-289.
24. Goldman AS. 2012. Evolution of immune functions of the mammary gland and protection of the infant. Breastfeed Med. 7:132-142. doi: 10.1089/bfm. 2012.0025
25. Goto K, Fukuda K, Senda A, Saito T, Kimura K, Glander KE, Hinde K, Dittus W, Milligan LA, Power ML, et al. 2010. Chemical characterization of oligosaccharides in the milk of six species of New and Old world monkeys. Glycoconj J. 27:703-715. doi: 10.1007/s10719-010-9315-0
26. Griffiths M. 1965. Rate of growth and intake of milk in a suckling echidna. Comp Biochem Physiol. 16:383-392.
27. Griffiths M. 1978. The biology of the monotremes. New York: Academic Press.
28. Griffiths M. 1989. Tachyglossidae. In: Walton DW, Richardson BJ, editors. Fauna of Australia. Mammalia. Volume 1B. Canberra (Australia): Australian Government Publishing Service. p. 407-435.
29. Griffiths M, Green B, Leckie RMC, Messer M, Newgrain KW. 1984. Constituents of platypus and echidna milk, with particular reference to the fatty acid complement of the triglycerides. Aust J Biol Sci. 37:323-329.
30. Griffiths M, McIntosh DL, Coles REA. 1969. The mammary gland of the echidna, Tachyglossus aculeatus, with observations on the incubation of the egg and on the newly-hatched young. J Zool Lond. 158:371-386.
31. Guerardel Y, Morelle W, Plancke Y, Lemoine J, Strecker J. 1999. Structural analysis of three sulfated oligosaccharides isolated from human milk. Carbohydr Res. 320:230-238.
32. Haverkamp J, van Halbeek H, Dorland L, Vliegenthart JFG, Pfeil R, Schauer T. 1982. High-resolution 1H-NMR spectroscopy of free and glycosidically linked O-acetylated sialic acids. Eur J Biochem. 122:305-311.
33. Iwersen M, Dora H, Kohla G, Gasa S, Schauer R. 2003. Solubilisation and properties of the sialate-4-O-acetyltransferase from guinea pig liver. Biol Chem. 384:1035-1047.
34. Jenkins GA, Bradbury JH, Messer M, Trifinoff E. 1984. Determination of the structures of fucosyl-lactose and difucosyl-lactose from the milk of monotremes, using 13C-NMR spectroscopy. Carbohydr Res. 126:157-161.
35. Jourdian GW, Dean L, Roseman S. 1971. The sialic acid XI. A periodateresorcinol method for the quantitative estimation of free sialic acids and their glycosides. J Biol Chem. 256:430-435.
36. Kamerling JP, Dorland L, van Halbeek H, Vliegenthart JEG, Messer M, Schauer R. 1982. Structural studies of 4-O-acetyl-α-N-acetylneuraminyl-(2, 3)-lactose, the main oligosaccharide in echidna milk. Carbohydr Res. 100:331-340.
37. Lefèvre CM, Sharp JA, Nicholas KR. 2010. Evolution of lactation: Ancient origin and extreme adaptations of the lactation system. Annu Rev Genomics Hum Genet. 11:219-238. doi: 10.1146/annurev-genom-082509-141806
38. Luo Z-X, Yuan C-X, Meng Q-J, Ji Q. 2011. A Jurassic eutherian mammal and divergence of marsupials and placentals. Nature. 476:442-405. doi:10.1038/nature10291
39. Mariño K, Lane JA, Abrahams JL, Struwe WB, Harvey DJ, Marotta M, Hickey RM, Rudd PM. 2011. Method for milk oligosaccharide profiling by 2-aminobenzamide labeling and hydrophilic interaction chromatography. Glycobiology. 21:1317-1330. doi: 10.1093/glycob/cwr067.
40. Messer M. 1974. Identification of N-acetyl-4-O-acetylneuraminyl-lactose in echidna milk. Biochem J. 139:415-420.
41. Messer M, Gadiel PA, Ralston GB, Griffiths M. 1983. Carbohydrates of the milk of the platypus. Aust J Biol Sci. 36:129-137.
42. Messer M, Kerry K. 1973. Milk carbohydrates of the echidna and the platypus. Science. 180:201-203.
43. Messer M, Urashima T. 2002. Evolution of milk oligosaccharides and lactose. Trends Glycosci Glycotech. 14:153-176
44. Morrow GE, Andersen NA, Nicol SC. 2009. Reproductive strategies of the short-beaked echidna-a review with new data from a long-term study on the Tasmanian subspecies (Tachyglossus aculeatus setosus). Aust J Zool. 57:275-282. doi: 10.1071/ZO09037
45. Morrow GE, Nicol SC. 2013. Maternal care in the Tasmanian echidna Tachyglossus aculeatus setosus. Aust J Zool. 60:289-298. doi: 10.1071/ZO12066
46. Morrow AL, Ruiz-Palacios GM, Jiang X, Newburg DS. 2005. Human-milk glycans that inhibit pathogen binding protect breast-feeding infants against infectious diarrhea. J Nutr. 135:1304-1307.
47. Newburg DS, Ruiz-Palacios GM, Altaye M, Chaturvedi P, Meinzen-Derr J, Guerrero ML, Morrow AL. 2004. Innate protection conferred by fucosylated oligosaccharides of human milk against diarrhea in breastfed infants. Glycobiology. 14:253-263.
48. Nicol SC, Morrow GE. 2012. Sex and seasonality: Reproduction in the echidna (Tachyglossus aculeatus). In: Ruf T, Bieber C, Arnold W, Millesi E, editors. Living in a seasonal world: Thermoregulatory and metabolic adaptations. Heidelberg (Germany): Springer. p. 143-153. doi:10.1007/978-3-642-28678-0-13
49. Nicol SC, Vanpé C, Sprent J, Morrow G, Andersen NA. 2011. Spatial ecology of a ubiquitous Australian anteater, the short-beaked echidna (Tachyglossus aculeatus). J Mammal. 92:101-110. doi: 10.1644/09-MAMMA-398.1
50. Oftedal OT. 1980. Milk and mammalian evolution. In: Schmidt-Nielsen K, Bolis L, Taylor CR, editors. omparative physiology: Primitive mammals. Cambridge (England): Cambridge University Press. p. 31-42.
51. Oftedal OT. 1984. Milk composition, milk yield and energy output at peak lactation. A comparative review. Symp Zool Soc London. 51:33-85.
52. Oftedal OT. 2002a. The mammary gland and its origin during synapsid evolution. J Mammary Gland Biol Neoplasia. 7:225-252.
53. Oftedal OT. 2002b. The origin of lactation as a water source for parchmentshelled eggs. J Mammary Gland Biol Neoplasia. 7:253-266.
54. Oftedal OT. 2012. The evolution of milk secretion and its ancient origins. Animal. 6:355-368. doi: 10.1017/S1751731111001935
55. Oftedal OT. 2013. Origin and evolution of the major constituents of milk. In: Fox PF, McSweeney PLH, editors. Advanced dairy chemistry-1A. Proteins: Basic aspects. 4th ed. New York: Springer, p. 1-42. doi: 10.1007/978-1-4614- 4714-6-1
56. Oftedal OT, Dhouailly D. 2013. Evo-Devo of the mammary gland. J Mammary Gland Biol Neoplasia. 18(2):105-120. doi: 10.1007/s10911-013-9290-8.
57. Pfenninger A, Karas M, Finke B, Stahl B. 2002. Structural analysis of underivatized neutral human milk oligosaccharides in the negative ion mode by nano-electrospray MSn ( part 1: Methodology). J Am Soc Mass Spectrom. 13:1331-1340.
58. Prager EM, Wilson AC. 1988. Ancient origin of lactalbumin from lysozyme: Analysis of DNA and amino acid sequences. J Mol Evol. 27:326-335.
59. Ramakrishnan B, Qasba PK. 2001. Crystal structure of lactose synthase reveals a large conformational change in its catalytic component, the β-1,4-galactosyltransferase-I. J Mol Biol. 310:205-218.
60. Rinninger A, Richet C, Pons A, Kohla G, Schauer R, Bauer HC, Zanetta JP, Vlasak R. 2006. Localisation and distribution of O-acetylated N-acetylneuraminic acids, the endogenous substrates of the hemagglutinin-esterases of murine coronaviruses, in mouse tissue. Glycoconj J. 23:73-84.
61. Ruiz-Palacios GM, Cervantes LE, Romas P, Chavez-Munguia B, Newburg DS. 2003. Campylobacter jejuni binds intestinal H(O) antigen (Fucα1, 2Galβ1,4GlcNAc), and fucosyloligosaccharides of human milk inhibit its binding and infection. J Biol Chem. 278:14112-14120.
62. Schauer R, Shukla AK. 2008. Isolation and properties of two sialate-Oacetylesterases from horse liver with 4-and 9-O-acetyl specificities. Glycoconj J. 25:625-632. doi: 10.1007/s10719-008-9109-9
63. Schauer R, Srinivasan GV, Coddeville B, Zanetta JP, Guérardel Y. 2009. Low incidence of N-glycolylneuraminic acid in birds and reptiles and its absence in the platypus. Carbohydr Res. 344:1494-1500. doi: 0.1016/j.carres. 2009. 05.020
64. Schauer R, Srinivasan GV, Wipfler D, Kniep B, Schwartz-Albiezet R. 2011. O-Acetylated sialic acids and their role in immune defense. Adv Exp Med Biol. 705:525-548. doi: 10.1007/978-1-4419-7877-6-28
65. Shennan DB, Peaker M. 2000. Transport of milk constituents by the mammary gland. Physiol Rev. 80:925-951.
66. Smits SL, Gerwig GJ, van Vliet AL, Lissenberg A, Briza P, Kamerling JP, Vlasak R, de Groot RJ. 2005. Nidovirus sialate-O-acetylesterases: Evolution and substrate specificity of coronaviral and toroviral receptor-destroying enzymes. J Biol Chem. 280:6933-6941.
67. Stewart IM, Messer M,Walcott PJ, Gadiel PA, Griffiths M. 1983. Intestinal glycosidase activities in one adult and two suckling echidnas: Absence of a neutral lactase (β-D-galactosidase). Aust J Biol Sci. 36:139-146.
68. Sturman JA, Lin YY, Higuchi T, Fellman JH. 1985. N-Acetylneuramin lactose sulfate: A newly identified nutrient in milk. Pediatr Res. 19:216-219.
69. Taufik E, Fukuda K, Senda A, Saito T, Williams C, Tilden C, Eisert R, Oftedal OT, Urashima T. 2012. Structural characterization of neutral and acidic oligosaccharides in the milks of strepsirrhine primates: Greater galago, aye-aye, Coquerel's sifaka and mongoose lemur. Glyconj J. 29:119-134. doi: 10.1007/s10719-012-9370-9
70. Taylor SG, McKenzie IFC, Sandrin MS. 2003. Characterization of the rat α (1,3)galactosyltransferase: Evidence for two independent genes encoding glycosyltransferases that synthesize Galα(1,3)Gal by two separate glycosylation pathways. Glycobiology. 13:327-337.
71. Uemura Y, Takahashi S, Senda A, Fukuda K, Saito T, Oftedal OT, Urashima T. 2009. Chemical characterization of milk oligosaccharides of a spotted hyena (Crocuta crocuta). Comp Biochem Physiol A. 152:158-161. doi: 10.1016/j. cbpa.2008.09.013
72. Urashima T, Asakuma S, Leo F, Fukuda K, Messer M, Oftedal OT. 2012. The predominance of type 1 oligosaccharides is a feature specific to human breast milk. Adv Nutr. 3:473S-482S. doi: 0.3945/an.111.001412
73. Urashima T, Fukuda K, Messer M. 2012. Evolution of milk oligosaccharides and lactose: A hypothesis. Animal. 6:369-374. doi: 10.1017/S1751731111001248
74. Urashima T, Nagata H, Nakamura T, Arai I, Saito T, Imazu K, Hayashi T, Derocher AE, Wiig O. 2003. Differences in oligosaccharides pattern of a sample of polar bear colostrum and mid-lactation milk. Comp Biochem physiol B. 136:887-896.
75. Urashima T, Nakamura T, Ikeda A, Asakuma S, Arai I, Saito T, Oftedal OT. 2005. Characterization of oligosaccharides in milk of a mink, Mustela vison. Comp Biochem Physiol A. 142:461-471.
76. Urashima T, Nakamura T, Nakagawa D, Noda M, Arai I, Saito T, Lydersen C, Kovacs KM. 2004. Characterization of oligosaccharides in a milk of bearded seal (Erignathus barbatus). Comp Biochem Physiol B. 138:1-18.
77. Urashima T, Odaka G, Asakuma S, Uemura Y, Goto K, Senda A, Saito T, Fukuda K, Messer M, Oftedal OT. 2009. Chemical characterization of oligosaccharides in chimpanzee, bonobo, gorilla, orangutan, and siamang milk or colostrum. Glycobiology. 19:499-508. doi: 10.1093/glycob/cwp006
78. Urashima T, Sumiyoshi W, Nakamura T, Arai I, Saito T, Komatsu T, Tsubota T. 1999. Chemical characterization of milk oligosaccharides of the Japanese black bear, Ursus thibetanus japonicus. Biochim Biophys Acta. 1472: 290-306.
79. Urashima T, Yamashita T, Nakamura T, Arai I, Saito T, Derocher AE, Wiig O. 2000. Chemical characterization of milk oligosaccharides of the polar bear, Ursus maritimus. Biochim Biophys Acta. 1475:395-408.
80. Varki A, Cummings RD, Esko JD, Freeze HH, Stanley P, Bertozzi CR, Hart GW, Etzler ME. 2009. Essentials of glycobiology. 2nd ed. Cold Spring Harbor (NY): Cold Spring Harbor Laboratory Press.
81. Wang B. 2009. Sialic acid is an essential nutrient for brain development and cognition. Annu Rev Nutr. 29:177-222. doi: 10.1146/annurev.nutr.28.061807
82. Wang J, Wong ESW, Whitley JC, Li J, Stringer JM, Short KR, Renfree MB, Belov K, Cocks BG. 2011. Ancient antimicrobial peptides kill antibiotic-resistant pathogens: Australian mammals provide new options. PLoS ONE. 6(8):e24030. doi:10.1371/journal.pone.0024030
83. Wheeler SF, Harvey DJ. 2000. Negative ion mass spectrometry of sialylated carbohydrates: Discrimination of N-acetylneuraminic acid linkages by MALDI-TOF and ESI-TOF mass spectrometry. Anal Chem. 72:5027-5039.