Kinetics of milk lipid droplet transport, growth, and secretion revealed by intravital imaging: Lipid droplet release is intermittently stimulated by oxytocin

Molecular Biology of the Cell

Volumn 28, Issue 7, 2017, Pages 935-946

  Masedunskas, Andrius ^a,b,d   Chena, Yun ^a,b,e,f   Stussman, Rebecca ^a,b,g   Weigert, Roberto ^a,b   Mather, Ian H ^a,b,c  

^a NATIONAL CANCER INSTITUTE   (United States)

^b NATIONAL INSTITUTE OF DENTAL AND CRANIOFACIAL RESEARCH   (United States)

^c UNIVERSITY OF MARYLAND   (United States)

^d UNIVERSITY OF NEW SOUTH WALES   (Australia)

^e Johns Hopkins University   (United States)

^f JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^g Department of Earth and Environmental Sciences   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FAT DROPLET; FLUORESCENT DYE; MILK FAT; OXYTOCIN; LIPID;

ANIMAL CELL; ANIMAL TISSUE; APICAL MEMBRANE; ARTICLE; BASEMENT MEMBRANE; BREAST CELL; CONTROLLED STUDY; CYTOPLASM; FEMALE; FLUORESCENCE ANALYSIS; INTRAVITAL MICROSCOPY; KINETICS; LACTATION; LIPID TRANSPORT; LIPOGENESIS; MOUSE; MYOEPITHELIUM; NONHUMAN; PRIORITY JOURNAL; TRANSGENIC MOUSE; ANIMAL; CELL MEMBRANE; EPITHELIUM CELL; LIPID METABOLISM; METABOLISM; MILK; PHYSIOLOGY; PROCEDURES; UDDER;

ANIMALS; CELL MEMBRANE; EPITHELIAL CELLS; FEMALE; INTRAVITAL MICROSCOPY; KINETICS; LACTATION; LIPID DROPLETS; LIPID METABOLISM; LIPIDS; MAMMARY GLANDS, ANIMAL; MICE; MILK; OXYTOCIN;

EID: 85016763432     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E16-11-0776     Document Type: Article

References (73)

1. Amato PA, Loizzi RF (1981). The identifcation and localization of actin and actin-like flaments in lactating guinea pig mammary gland alveolar cells. Cell Motil 1, 329-347.
2. Bargmann W, Knoop A (1959). Über die Morphologie der Milchsekretion. Licht-und Elektronenmikroskopische Studien an der Milchdrüse der Ratte. Z Zellforsch 49, 344-388.
3. Barneda D, Planas-Iglesias J, Gaspar ML, Mohammadyani4 D, Prasannan S, Dormann D, Han G-S, Jesch SA, Carman GM, Kagan V, et al. (2015). The brown adipocyte protein CIDEA promotes lipid droplet fusion via a phosphatidic acid-binding amphipathic helix. Elife 4, e07485.
4. Berga SE (1984). Electrical potentials and cell-to-cell dye movement in mouse mammary gland during lactation. Am J Physiol 247, C20-C25.
5. Caspi A, Granek R, Elbaum M (2000). Enhanced diffusion in active intracel-lular transport. Phys Rev Lett 85, 5655-5658.
6. Chen Y, Lagerholm BC, Yang B, Jacobson K (2006). Methods to measure the lateral diffusion of membrane lipids and proteins. Methods 39, 147-153.
7. Chong BM, Reigan P, Mayle-Combs KD, Orlicky DJ, McManaman JL (2011). Determinants of adipophilin function in milk lipid formation and secretion. Trends Endocrinol Metab 22, 211-217.
8. Deeney JT, Valivullah HM, Dapper CH, Dylewski D P, Keenan TW (1985). Microlipid droplets in milk secreting mammary epithelial cells: evidence that they originate from endoplasmic reticulum and are precursors of milk lipid globules. Eur J Cell Biol 38, 16-26.
9. Dutta A, Sinha DK (2015). Turnover of the actomyosin complex in zebraf-ish embryos directs geometric remodelling and the recruitment of lipid droplets. Sci Rep 5, 13915.
10. Dylewski D P, Dapper CH, Valivullah HM, Deeney JT, Keenan TW (1984). Morphological and biochemical characterization of possible intracellular precursors of milk lipid globules. Eur J Cell Biol 35, 99-111.
11. Dylewski D P, Keenan TW (1984). Centrioles in the mammary epithelium of the rat. J Cell Sci 72, 185-193.
12. Franke WW, Heid HW, Grund C, Winter S, Freudenstein C, Schmid E, Jarasch E-D, Keenan TW (1981). Antibodies to the major insoluble milk fat globule membrane-associated protein: specifc location in apical regions of lactating epithelial cells. J Cell Biol 89, 485-494.
13. Fujimoto Y, Itabe H, Kinoshita T, Homma KJ, Onoduka J, Mori M, Yamaguchi S, Makita M, Higashi Y, Yamashita A, Takano T (2007). Involvement of ACSL in local synthesis of neutral lipids in cytoplasmic lipid droplets in human hepatocyte HuH7. J Lipid Res 48, 1280-1292.
14. Gimpl G, Fahrenholz F (2001). The oxytocin receptor system: structure, function, and regulation. Physiol Rev 81, 629-683.
15. Gong J, Sun Z, Wu L, Xu W, Schieber N, Xu D, Shui G, Yang H, Parton RG, Li P (2011). Fsp27 promotes lipid droplet growth by lipid exchange and transfer at lipid droplet contact sites. J Cell Biol 195, 953-963.
16. Gorden PJ, Timms LL (2004). Lactation. In: Dukes' Physiology of Domestic Animals, ed. WO Reece, Ithaca, NY: Cornell University Press, 694-714.
17. Gouon-Evans V, Lin EY, Pollard JW (2002). Requirement of macrophages and eosinophils and their cytokines/chemokines for mammary gland development. Breast Cancer Res 4, 155-164.
18. Hadjantonakis AK, Gertsenstein M, Ikawa M, Okabe M, Nagy A (1998). Generating green fuorescent mice by germline transmission of green fuorescent ES cells. Mech Dev 76, 79-90.
19. Head JH, Beer AE (1978). The immunologic role of viable leukocytic cells in mammary exosecretions. In: Lactation, A Comprehensive Treatise, Vol. IV, ed. BL Larson, New York: Academic Press, 337-364.
20. Heid HW, Keenan TW (2005). Intracellular origin and secretion of milk fat globules. Eur J Cell Biol 84, 245-258.
21. Honvo-Houéto E, Henry C, Chat S, Layani S, Truchet S (2016). The endo-plasmic reticulum and casein-containing vesicles contribute to milk fat globule membrane. Mol Biol Cell 27, 2946-2964.
22. Huston GE, Patton S (1990). Factors related to the formation of cytoplasmic crescents on milk fat globules. J Dairy Sci 73, 2061-2066.
23. Innis SM (1991). Essential fatty acids in growth and development. Prog Lipid Res 30, 39-103.
24. Jack LJW, Mather IH (1990). Cloning and analysis of cDNA encoding bovine butyrophilin, an apical glycoprotein expressed in mammary tissue and secreted in association with the milk-fat globule membrane during lactation. J Biol Chem 265, 14481-14486.
25. Jeong J, Lisinski I, Kadegowda AKG, Shin H, Wooding FBP, Daniels BR, Schaack J, Mather IH (2013). A test of current models for the mechanism of milk-lipid droplet secretion. Traffc 14, 974-986.
26. Jeong J, Rao AU, Xu J, Ogg SL, Hathout Y, Fenselau C, Mather IH (2009). The PRY/SRY/B30.2 domain of butyrophilin 1a1 (Btn1a1) binds to xanthine oxidoreductase: implications for the function of Btn1a1 in the mammary gland and other tissues. J Biol Chem 284, 22444-22456.
27. Kassan A, Herms A, Fernández-Vidal A, Bosch M, Schieber NL, Reddy BJN, Fajardo A, Gelabert-Baldrich M, Tebar F, Enrich C, et al. (2013). Acyl-CoA synthetase 3 promotes lipid droplet biogenesis in ER micro-domains. J Cell Biol 203, 985-1001.
28. Keenan TW, Morré DJ (1970). Phospholipid class and fatty acid composition of Golgi apparatus isolated from rat liver and comparison with other cell fractions. Biochemistry 9, 19-25.
29. Keenan TW, Morré DJ, Olson DE, Yunghans WN, Patton S (1970). Bio-chemical and morphological comparison of plasma membrane and milk fat globule membrane from bovine mammary gland. J Cell Biol 44, 80-93.
30. Knight CH, Maltz E, Docherty AH (1986). Milk yield and composition in mice: effects of litter size and lactation number. Comp Biochem Physiol 84A, 127-133.
31. Knoblach B, Rachubinski RA (2015). Transport and retention mechanisms govern lipid droplet inheritance in Saccharomyces cerevisiae. Traffc 16, 298-309.
32. Larque E, Demmelmar H, Koletzko B (2002). Perinatal supply and metabo-lism of long-chain polyunsaturated fatty acids: Importance for the early development of the nervous system. Ann NY Acad Sci 967, 299-310.
33. Martin S, Parton RG (2006). Lipid droplets: a unifed view of a dynamic organelle. Nat Rev Mol Cell Biol 7, 373-378.
34. Masedunskas A, Weigert R, Mather IH (2014). Intravital imaging of the lactating mammary gland in transgenic mice expressing fuorescent proteins. In: Advances in Intravital Microscopy, ed. R Weigert, Dordrecht, Netherlands: Springer-Verlag, 187-204.
35. Mather IH, Jack LJW, Madara PJ, Johnson VG (2001). The distribution of MUC1, an apical membrane glycoprotein, in mammary epithelial cells at the resolution of the electron microscope: implications for the mechanism of milk secretion. Cell Tissue Res 304, 91-101.
36. Mather IH, Keenan TW (1983). Function of endomembranes and the cell surface in the secretion of organic milk constituents. In: Biochemistry of Lactation, ed. TB Mepham, Amsterdam: Elsevier, 231-283.
37. Mather IH, Keenan TW (1998). Origin and secretion of milk lipids. J Mammary Gland Biol Neoplasia 3, 259-273.
38. Maucort G, Kasula R, Papadopulos A, Nieminen TA, Rubinsztein-Dunlop H, Meunier FA (2014). Mapping organelle motion reveals a vesicular conveyor belt spatially replenishing secretory vesicles in stimulated chromaffn cells. PLoS One 9, e87242.
39. Mazumdar MD, Tasic B, Miyamichi K, Li L, Luo L (2007). A global double-fuorescent Cre reporter mouse. Genesis 45, 593-605.
40. McManaman JL (2012). Milk lipid secretion: recent biomolecular aspects. Biomol Concepts 3, 581-591.
41. McManaman JL, Russell TD, Schaack J, Orlicky DJ, Robenek H (2007). Molecular determinants of milk lipid secretion. J Mammary Gland Biol Neoplasia 12, 259-268.
42. Monks J, Dzieciatkowska M, Bales ES, Orlicky DJ, Wright RM, McManaman JL (2016). Xanthine oxidoreductase mediates membrane docking of milk-lipid droplets but is not essential for apocrine milk fat globule secretion. J Physiol 594, 5899-5921.
43. Moriya H, Uchida K, Okajima T, Matsuda T, Nadano D (2011). Secretion of three enzymes for fatty acid synthesis into mouse milk in association with fat globules, and rapid decrease of the secreted enzymes by treatment with rapamycin. Arch Biochem Biophys 508, 87-92.
44. Mroue R, Inman J, Mott J, Budunova I, Bissell MJ (2015). Asymmetric expression of connexins between luminal epithelial-and myoepithelial-cells is essential for contractile function of the mammary gland. Dev Biol 399, 15-26.
45. Murphy DJ (2001). The biogenesis and functions of lipid bodies in animals, plants and microorganisms. Prog Lipid Res 40, 325-438.
46. Oftedal OT (1984). Milk composition, milk yield and energy output at peak lactation: a comparative review. Symp Zool Soc Lond 51, 33-85.
47. Oftedal OT, Iverson SJ (1995). Comparative analysis of nonhuman milks. Phylogenetic variation in the gross composition of milks. In: Hand-book of Milk Composition, ed. RG Jensen, New York: Academic Press, 749-789.
48. Ogg SL, Weldon AK, Dobbie L, Smith AJH, Mather IH (2004). Expression of butyrophilin (Btn1a1) in lactating mammary gland is essential for the regulated secretion of milk-lipid droplets. Proc Natl Acad Sci USA 101, 10084-10089.
49. Peixoto de Menezes A, Pinto da Silva P (1979). Fat droplet formation in rat lactating mammary gland and mammary carcinomas viewed by freeze-fracture. Lab Invest 40, 545-553.
50. Pitelka DR, Hamamoto ST, Duafala JG, Nemanic MK (1973). Cell contacts in the mouse mammary gland I. Normal gland in postnatal development and the secretory cycle. J Cell Biol 56, 797-818.
51. Plante I, Wallis A, Shao Q, Laird DW (2010). Milk secretion and ejection are impaired in the mammary gland of mice harboring a Cx43 mutant while expression and localization of tight and adherens junction proteins remain unchanged. Biol Reprod 82, 837-847.
52. Plum A, Hallas G, Magin T, Dombrowski F, Hagendorff A, Schumacher B, Wolpert C, Kim J-S, Lamers WH, Evert M, et al. (2000). Unique and shared functions of different connexins in mice. Curr Biol 10, 1083-1091.
53. R Development Core Team (2014). R: A Language and Environment for Statistical Computing. Version 3.1.1. Available at http://www.R-project.org/(accessed 10 July 2014).
54. Reed JR, Schwertfeger KL (2010). Immune cell location and function during post-natal mammary gland development. J Mammary Gland Biol Neoplasia 15, 329-339.
55. Reverey JF, Jeon J-H, Bao H, Leippe M, Metzler R, Selhuber-Unkel C (2015). Superdiffusion dominates intracellular particle motion in the super-crowded cytoplasm of pathogenic Acanthamoeba castellanii. Sci Rep 5, 11690.
56. Rios AC, Fu NY, Jamieson PR, Pal B, Whitehead L, Nicholas KR, Lindeman GJ, Visvader JE (2016). Essential role for a novel population of binucle-ated mammary epithelial cells in lactation. Nat Commun 7, 11400.
57. Stemberger BH, Patton S (1981). Relationship of size, intracellular loca-tion, and time required for secretion of milk fat droplets. J Dairy Sci 64, 422-426.
58. Stemberger BH, Walsh RM, Patton S (1984). Morphometric evaluation of lipid droplet associations with secretory vesicles, mitochondria and other components in the lactating cell. Cell Tissue Res 236, 471-475.
59. Suzuki M, Shinohara Y, Ohsaki Y, Fujimoto T (2011). Lipid droplets: size matters. J Electron Microsc (Tokyo) 60, S101-S116.
60. Targett-Adams P, Chambers D, Gledhill S, Hope RG, Coy JF, Girod A, McLauchlan J (2003). Live cell analysis and targeting of the lipid droplet-binding adipocyte differentiation-related protein. J Biol Chem 278, 15998-16007.
61. Tauchi-Sato K, Ozeki S, Houjou T, Taguchi R, Fujimoto T (2002). The surface of lipid droplets is a phospholipid monolayer with a unique fatty acid composition. J Biol Chem 277, 44507-44512.
62. Teter BB, Sampugna J, Keeney M (1990). Milk fat depression in C57Bl/6J mice consuming partially hydrogenated fat. J Nutr 120, 818-824.
63. van Meer G (1989). Lipid traffc in animal cells. Annu Rev Cell Biol 5, 247-275.
64. Vorbach C, Scriven A, Capecchi MR (2002). The housekeeping gene xan-thine oxidoreductase is necessary for milk fat droplet enveloping and secretion: gene sharing in the lactating mammary gland. Genes Dev 16, 3223-3235.
65. Wang W, Lv N, Zhang S, Shui G, Qian H, Zhang J, Chen Y, Ye J, Xie Y, Shen Y, et al. (2012). Cidea is an essential transcriptional coactiva-tor regulating mammary gland secretion of milk lipids. Nat Med 18, 235-243.
66. Weigert R, Porat-Shliom N, Amornphimoltham P (2013). Imaging cell biology in live animals: ready for prime time. J Cell Biol 201, 969-979.
67. Welte MA (2009). Fat on the move: intracellular motion of lipid droplets. Biochem Soc Trans 37, 991-996.
68. Welte MA, Gross S P, Postner M, Block SM, Wieschaus EF (1998). Developmental regulation of vesicle transport in Drosophila embryos: forces and kinetics. Cell 92, 547-557.
69. Wilfing F, Haas JT, Walther TC, Farese RV Jr (2014). Lipid droplet biogenesis. Curr Opin Cell Biol 29, 39-45.
70. Wooding FBP (1971). The mechanism of secretion of the milk fat globule. J Cell Sci 9, 805-821.
71. Wooding FBP (1977). Comparative mammary fne structure. Symp Zool Soc Lond 41, 1-41.
72. Wooding FBP, Peaker M, Linzell JL (1970). Theories of milk secretion: evidence from the electron microscopic examination of milk. Nature 226, 762-764.
73. Wu CC, Howell KE, Neville MC, Yates JR 3rd, McManaman JL (2000). Proteomics reveal a link between the endoplasmic reticulum and lipid secretory mechanisms in mammary epithelial cells. Electrophoresis 21, 3470-3482.