Diverse and active roles for adipocytes during mammary gland growth and function

Journal of Mammary Gland Biology and Neoplasia

Volumn 15, Issue 3, 2010, Pages 279-290

  Hovey, Russell C ^a   Aimo, Lucila ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Adipokine; Adipose; Epithelial stromal; Mammary fat pad

Indexed keywords

ADIPOCYTE; ADIPOSE TISSUE; BREAST CANCER; CANCER RISK; CELL FUNCTION; HUMAN; IN VITRO STUDY; IN VIVO STUDY; LACTATION; MAMMARY GLAND FUNCTION; NEWBORN PERIOD; POSTNATAL DEVELOPMENT; REVIEW;

ADIPOCYTES; ANIMALS; FEMALE; HUMANS; MAMMARY GLANDS, ANIMAL; MAMMARY GLANDS, HUMAN; STROMAL CELLS;

EID: 78049528087     PISSN: 10833021     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10911-010-9187-8     Document Type: Review

References (122)

1. RC Hovey JF Trott BK Vonderhaar 2002 Establishing a framework for the functional mammary gland: from endocrinology to morphology J Mammary Gland Biol Neoplasia 7 1 17 38 12160083
2. CJ Watson 2006 Involution: apoptosis and tissue remodelling that convert the mammary gland from milk factory to a quiescent organ Breast Cancer Res 8 2 203 16677411
3. C Brisken RD Rajaram 2006 Alveolar and lactogenic differentiation J Mammary Gland Biol Neoplasia 11 3-4 239 248 17111223
4. MC Neville D Medina J Monks RC Hovey 1998 The mammary fat pad J Mammary Gland Biol Neoplasia 3 2 109 116 10819521
5. RC Hovey TB McFadden RM Akers 1999 Regulation of mammary gland growth and morphogenesis by the mammary fat pad: a species comparison J Mammary Gland Biol Neoplasia 4 1 53 68 10219906
6. Hoshino K. Mammary transplantation and its histogenesis in mice. In: Yokoyama A, Mizuno H, Nagasawa H, editors. Physiology of mammary glands. Tokyo: Japan Scientific Press; 1978. p. 163-228.
7. HA Tucker 1987 Quantitative estimates of mammary growth during various physiological states: a review J Dairy Sci 70 9 1958 1966 3312321
8. S Cinti 2005 The adipose organ Prostaglandins Leukot Essent Fatty Acids 73 1 9 15 15936182
9. JB Hansen K Kristiansen 2006 Regulatory circuits controlling white versus brown adipocyte differentiation Biochem J 398 2 153 168 16898874
10. S Cinti 2009 Reversible physiological transdifferentiation in the adipose organ Proc Nutr Soc 68 4 340 349 19698198
11. B Cousin S Cinti M Morroni S Raimbault D Ricquier L Penicaud, et al. 1992 Occurrence of brown adipocytes in rat white adipose tissue: molecular and morphological characterization J Cell Sci 103 Pt 4 931 942 1362571
12. JR Hens JJ Wysolmerski 2005 Key stages of mammary gland development: molecular mechanisms involved in the formation of the embryonic mammary gland Breast Cancer Res 7 5 220 224 16168142
13. Sakakura T. Mammary embryogenesis. In: Neville MC, Daniel CW, editors. The mammary gland: development, regulation, and function. New York: Plenum Press; 1987. p. 37-66.
14. R Anbazhagan J Bartek P Monaghan BA Gusterson 1991 Growth and development of the human infant breast Am J Anat 192 4 407 417 1781450
15. R Anbazhagan BA Gusterson 1995 Ultrastructure and immunohistochemistry of the embryonic type of fat identified in the human infant breast Anat Rec 241 1 129 135 7879918
16. LG Sheffield 1988 Organization and growth of mammary epithelia in the mammary gland fat pad J Dairy Sci 71 10 2855 2874 3060494
17. Mayer G, Klein M. HIstology and cytology of the mammary gland. In: Kon SK, Cowie AT, editors. Milk: the mammary gland and its secretion. New York: Academic; 1961. p. 47-116.
18. RC Hovey DE Auldist DD Mackenzie TB McFadden 2000 Preparation of an epithelium-free mammary fat pad and subsequent mammogenesis in ewes J Anim Sci 78 8 2177 2185 10947106
19. S Ellis TB McFadden RM Akers 1998 Prepuberal ovine mammary development is unaffected by ovariectomy Domest Anim Endocrinol 15 4 217 225 9673454
20. LW Nelson WA Kelly 1974 Changes in canine mammary gland histology during the estrous cycle Toxicol Appl Pharmacol 27 1 113 122 4136584
21. Schedin P, Hovey RC. Editorial: The mammary stroma in normal development and function. J. Mammary Gland Biol. Neoplasia. 2010.
22. T Bani-Sacchi S Bianchi G Bani M Bigazzi 1987 Ultrastructural studies on white adipocyte differentiation in the mouse mammary gland following estrogen and relaxin Acta Anat (Basel) 129 1 1 9
23. M Matsumoto H Nishinakagawa M Kurohmaru Y Hayashi 1995 Effects of estrogen and progesterone on the parenchyma and blood vessels of the mammary gland in ovariectomized adult mice J Vet Med Sci 57 1 39 44 7756422
24. M Matsumoto H Nishinakagawa M Kurohmaru Y Hayashi J Otsuka 1992 Effects of estrogen and progesterone on the development of the mammary gland and the associated blood vessels in ovariectomized mice J Vet Med Sci 54 6 1117 1124 1477162
25. M Matsumoto H Nishinakagawa M Kurohmaru Y Hayashi MA Awal 1995 Ultrastructural changes in fat cells and blood capillaries of the mammary gland in starved mice J Vet Med Sci 57 4 733 736 8519907
26. V Gouon-Evans JW Pollard 2002 Unexpected deposition of brown fat in mammary gland during postnatal development Mol Endocrinol 16 11 2618 2627 12403850
27. Barbatelli G, Murano I, Madsen L, Hao Q, Jimenez M, Kristiansen K, et al. The emergence of cold-induced brown adipocytes in mouse white fat depots is determined predominantly by white to brown adipocyte transdifferentiation. Am J Physiol Endocrinol Metab. 298(6):E1244-253.
28. SR Master JL Hartman CM D'Cruz SE Moody EA Keiper SI Ha, et al. 2002 Functional microarray analysis of mammary organogenesis reveals a developmental role in adaptive thermogenesis Mol Endocrinol 16 6 1185 1203 12040007
29. Andres A-C, Djonov V. The mammary gland vasculature revisited. J. Mammary Gland Biol. Neoplasia 2010.
30. IN Soemarwoto HA Bern 1958 The effect of hormones on the vascular pattern of the mouse mammary gland Am J Anat 103 3 403 435 13649579
31. RC Hovey AS Goldhar J Baffi BK Vonderhaar 2001 Transcriptional regulation of vascular endothelial growth factor expression in epithelial and stromal cells during mouse mammary gland development Mol Endocrinol 15 5 819 831 11328861
32. S Bianchi G Bani M Bigazzi 1986 Effects of relaxin on the mouse mammary gland. III. The fat pad J Endocrinol Invest 9 2 153 160 3519745 (Pubitemid 16076339)
33. W Tang D Zeve JM Suh D Bosnakovski M Kyba RE Hammer, et al. 2008 White fat progenitor cells reside in the adipose vasculature Science 322 5901 583 586 18801968
34. E Pujol AM Proenza P Roca I Llado 2006 Changes in mammary fat pad composition and lipolytic capacity throughout pregnancy Cell Tissue Res 323 3 505 511 16328496
35. JJ Elias DR Pitelka RC Armstrong 1973 Changes in fat cell morphology during lactation in the mouse Anat Rec 177 4 533 547 4762729
36. JC Bartley JT Emerman MJ Bissell 1981 Metabolic cooperativity between epithelial cells and adipocytes of mice Am J Physiol 241 5 C204 C208 6795927
37. GK Bandyopadhyay LY Lee RC Guzman S Nandi 1995 Effect of reproductive states on lipid mobilization and linoleic acid metabolism in mammary glands Lipids 30 2 155 162 7769972
38. M Rebuffe-Scrive J Eldh LO Hafstrom P Bjorntorp 1986 Metabolism of mammary, abdominal, and femoral adipocytes in women before and after menopause Metabolism 35 9 792 797 3747836
39. JD Rink ER Simpson JJ Barnard SE Bulun 1996 Cellular characterization of adipose tissue from various body sites of women J Clin Endocrinol Metab 81 7 2443 2447 8675558
40. T Anzai K Muto S Komine 1979 Changes in fat content and some characteristics of lipolytic activity during pregnancy and lactation in mouse mammary gland Endocrinol Jpn 26 3 371 377 477624
41. RO Scow SS Chernick TR Fleck 1977 Lipoprotein lipase and uptake of triacylglycerol, cholesterol and phosphatidylcholine from chylomicrons by mammary and adipose tissue of lactating rats in vivo Biochim Biophys Acta 487 2 297 306 861238
42. TD Russell CA Palmer DJ Orlicky A Fischer MC Rudolph MC Neville, et al. 2007 Cytoplasmic lipid droplet accumulation in developing mammary epithelial cells: roles of adipophilin and lipid metabolism J Lipid Res 48 7 1463 1475 17452747
43. M Lejour 1997 Evaluation of fat in breast tissue removed by vertical mammaplasty Plast Reconstr Surg 99 2 386 393 9030144
44. DT Ramsay JC Kent RA Hartmann PE Hartmann 2005 Anatomy of the lactating human breast redefined with ultrasound imaging J Anat 206 6 525 534 15960763
45. E Vandeweyer D Hertens 2002 Quantification of glands and fat in breast tissue: an experimental determination Ann Anat 184 2 181 184 11936199
46. OT Anastassiades C Spiliades E Tsakraklides J Gogas 1983 Amount and distribution of solid and fatty tissues in the female breast and their relationship to carcinoma Pathol Res Pract 176 2-4 200 215 6856517
47. JN Lilla RV Joshi CS Craik Z Werb 2009 Active plasma kallikrein localizes to mast cells and regulates epithelial cell apoptosis, adipocyte differentiation, and stromal remodeling during mammary gland involution J Biol Chem 284 20 13792 13803 19297327
48. CM Alexander S Selvarajan J Mudgett Z Werb 2001 Stromelysin-1 regulates adipogenesis during mammary gland involution J Cell Biol 152 4 693 703 11266461
49. BA Howard BA Gusterson 2000 Human breast development J Mammary Gland Biol Neoplasia 5 2 119 137 11149569
50. SP Oliver LM Sordillo 1988 Udder health in the periparturient period J Dairy Sci 71 9 2584 2606 3053815
51. AV Capuco RM Akers JJ Smith 1997 Mammary growth in Holstein cows during the dry period: quantification of nucleic acids and histology J Dairy Sci 80 3 477 487 9098797
52. De Vries LD, Dover H, Casey T, VandeHaar MJ, Plaut K. Characterization of mammary stromal remodeling during the dry period. J Dairy Sci. 93(6):2433-43.
53. P Wang E Mariman J Renes J Keijer 2008 The secretory function of adipocytes in the physiology of white adipose tissue J Cell Physiol 216 1 3 13 18264975
54. JE Celis JM Moreira T Cabezon P Gromov E Friis F Rank, et al. 2005 Identification of extracellular and intracellular signaling components of the mammary adipose tissue and its interstitial fluid in high risk breast cancer patients: toward dissecting the molecular circuitry of epithelial-adipocyte stromal cell interactions Mol Cell Proteomics 4 4 492 522 15695426
55. JF Trott BK Vonderhaar RC Hovey 2008 Historical perspectives of prolactin and growth hormone as mammogens, lactogens and galactagogues-agog for the future! J Mammary Gland Biol Neoplasia 13 1 3 11 18204889
56. M Zinger M McFarland N Ben-Jonathan 2003 Prolactin expression and secretion by human breast glandular and adipose tissue explants J Clin Endocrinol Metab 88 2 689 696 12574200
57. ER Hugo DC Borcherding KS Gersin J Loftus N Ben-Jonathan 2008 Prolactin release by adipose explants, primary adipocytes, and LS14 adipocytes J Clin Endocrinol Metab 93 10 4006 4012 18647802
58. RC Hovey JF Trott E Ginsburg A Goldhar MM Sasaki SJ Fountain, et al. 2001 Transcriptional and spatiotemporal regulation of prolactin receptor mRNA and cooperativity with progesterone receptor function during ductal branch growth in the mammary gland Dev Dyn 222 2 192 205 11668597
59. Nakatani H, Aoki N, Okajima T, Nadano D, Flint D, Matsuda T. Establishment of a mammary stromal fibroblastic cell line for in vitro studies in mice of mammary adipocyte differentiation. Biol Reprod. 82(1):44-53.
60. S Viengchareun N Servel B Feve M Freemark M Lombes N Binart 2008 Prolactin receptor signaling is essential for perinatal brown adipocyte function: a role for insulin-like growth factor-2 PLoS ONE 3 2 e1535 18253483
61. M Freemark D Fleenor P Driscoll N Binart P Kelly 2001 Body weight and fat deposition in prolactin receptor-deficient mice Endocrinology 142 2 532 537 11159821
62. C Ling L Svensson B Oden B Weijdegard B Eden S Eden, et al. 2003 Identification of functional prolactin (PRL) receptor gene expression: PRL inhibits lipoprotein lipase activity in human white adipose tissue J Clin Endocrinol Metab 88 4 1804 1808 12679477
63. RJ Santen H Brodie ER Simpson PK Siiteri A Brodie 2009 History of aromatase: saga of an important biological mediator and therapeutic target Endocr Rev 30 4 343 375 19389994
64. JD Chow ER Simpson WC Boon 2009 Alternative 5′-untranslated first exons of the mouse Cyp19A1 (aromatase) gene J Steroid Biochem Mol Biol 115 3-5 115 125 19500729
65. Y Feuermann SJ Mabjeesh A Shamay 2009 Mammary fat can adjust prolactin effect on mammary epithelial cells via leptin and estrogen Int J Endocrinol 2009 427260 20049155
66. M Peaker E Taylor 1990 Oestrogen production by the goat mammary gland: transient aromatase activity during late pregnancy J Endocrinol 125 1 R1 R3 2338526
67. SO Mueller JA Clark PH Myers KS Korach 2002 Mammary gland development in adult mice requires epithelial and stromal estrogen receptor alpha Endocrinology 143 6 2357 2365 12021201
68. MJ Meyer AV Capuco YR Boisclair ME Van Amburgh 2006 Estrogen-dependent responses of the mammary fat pad in prepubertal dairy heifers J Endocrinol 190 3 819 827 17003282
69. MN Dieudonne MC Leneveu Y Giudicelli R Pecquery 2004 Evidence for functional estrogen receptors alpha and beta in human adipose cells: regional specificities and regulation by estrogens Am J Physiol Cell Physiol 286 3 C655 C661 14761887
70. GR Cunha P Young YK Hom PS Cooke JA Taylor DB Lubahn 1997 Elucidation of a role for stromal steroid hormone receptors in mammary gland growth and development using tissue recombinants J Mammary Gland Biol Neoplasia 2 4 393 402 10935027
71. G Cheng Z Weihua M Warner JA Gustafsson 2004 Estrogen receptors ER alpha and ER beta in proliferation in the rodent mammary gland Proc Natl Acad Sci USA 101 11 3739 3746 14762170
72. Li S, Han B, Liu G, Ouellet J, Labrie F, Pelletier G. Immunocytochemical localization of sex steroid hormone receptors in normal human mammary gland. J Histochem Cytochem. 58(6):509-15.
73. MJ Meyer RP Rhoads AV Capuco EE Connor A Hummel YR Boisclair, et al. 2007 Ontogenic and nutritional regulation of steroid receptor and IGF-I transcript abundance in the prepubertal heifer mammary gland J Endocrinol 195 1 59 66 17911397
74. AM Rowzee DA Lazzarino L Rota Z Sun TL Wood 2008 IGF ligand and receptor regulation of mammary development J Mammary Gland Biol Neoplasia 13 4 361 370 19020961
75. DL Kleinberg W Ruan 2008 IGF-I, GH, and sex steroid effects in normal mammary gland development J Mammary Gland Biol Neoplasia 13 4 353 360 19034633
76. MM Richert TL Wood 1999 The insulin-like growth factors (IGF) and IGF type I receptor during postnatal growth of the murine mammary gland: sites of messenger ribonucleic acid expression and potential functions Endocrinology 140 1 454 461 9886857
77. PD Walden W Ruan M Feldman DL Kleinberg 1998 Evidence that the mammary fat pad mediates the action of growth hormone in mammary gland development Endocrinology 139 2 659 662 9449638
78. RC Hovey HW Davey DD Mackenzie TB McFadden 1998 Ontogeny and epithelial-stromal interactions regulate IGF expression in the ovine mammary gland Mol Cell Endocrinol 136 2 139 144 9548217
79. N Rahimi R Saulnier T Nakamura M Park B Elliott 1994 Role of hepatocyte growth factor in breast cancer: a novel mitogenic factor secreted by adipocytes DNA Cell Biol 13 12 1189 1197 7811385
80. GE Kilroy SJ Foster X Wu J Ruiz S Sherwood A Heifetz, et al. 2007 Cytokine profile of human adipose-derived stem cells: expression of angiogenic, hematopoietic, and pro-inflammatory factors J Cell Physiol 212 3 702 709 17477371
81. HZ Zhang JM Bennett KT Smith N Sunil SZ Haslam 2002 Estrogen mediates mammary epithelial cell proliferation in serum-free culture indirectly via mammary stroma-derived hepatocyte growth factor Endocrinology 143 9 3427 3434 12193555
82. EJ Ehrhart P Segarini ML Tsang AG Carroll MH Barcellos-Hoff 1997 Latent transforming growth factor beta1 activation in situ: quantitative and functional evidence after low-dose gamma-irradiation FASEB J 11 12 991 1002 9337152
83. JV Soriano MS Pepper L Orci R Montesano 1998 Roles of hepatocyte growth factor/scatter factor and transforming growth factor-beta1 in mammary gland ductal morphogenesis J Mammary Gland Biol Neoplasia 3 2 133 150 10819523
84. A Maccio C Madeddu G Mantovani 2009 Adipose tissue as target organ in the treatment of hormone-dependent breast cancer: new therapeutic perspectives Obes Rev 10 6 660 670 19460113
85. Y Lin Q Li 2007 Expression and function of leptin and its receptor in mouse mammary gland Sci China C Life Sci 50 5 669 675 17879067
86. A Kamikawa O Ichii D Yamaji T Imao C Suzuki Y Okamatsu-Ogura, et al. 2009 Diet-induced obesity disrupts ductal development in the mammary glands of nonpregnant mice Dev Dyn 238 5 1092 1099 19384959
87. Thorn SR, Giesy SL, Myers MG, Jr., Boisclair YR. Mammary ductal growth is impaired in mice lacking leptin-dependent signal transducer and activator of Transcription 3 signaling. Endocrinology.
88. SR Thorn MJ Meyer ME Van Amburgh YR Boisclair 2007 Effect of estrogen on leptin and expression of leptin receptor transcripts in prepubertal dairy heifers J Dairy Sci 90 8 3742 3750 17638985
89. S Landskroner-Eiger B Qian ES Muise AR Nawrocki JP Berger EJ Fine, et al. 2009 Proangiogenic contribution of adiponectin toward mammary tumor growth in vivo Clin Cancer Res 15 10 3265 3276 19447867
90. S Perrier F Caldefie-Chezet MP Vasson 2009 IL-1 family in breast cancer: potential interplay with leptin and other adipocytokines FEBS Lett 583 2 259 265 19111549
91. JS Russell SO McGee MM Ip D Kuhlmann PA Masso-Welch 2007 Conjugated linoleic acid induces mast cell recruitment during mouse mammary gland stromal remodeling J Nutr 137 5 1200 1207 17449582
92. LN Bell L Cai BH Johnstone DO Traktuev KL March RV Considine 2008 A central role for hepatocyte growth factor in adipose tissue angiogenesis Am J Physiol Endocrinol Metab 294 2 E336 E344 18073323
93. RA Knazek SC Liu JS Bodwin BK Vonderhaar 1980 Requirement of essential fatty acids in the diet for development of the mouse mammary gland J Natl Cancer Inst 64 2 377 382 6928228
94. MJ Miyamoto-Tiaven LA Hillyard S Abraham 1981 Influence of dietary fat on the growth of mammary ducts in BALB/c mice J Natl Cancer Inst 67 1 179 188 6942189
95. CW Welsch JV DeHoog DH O'Connor LG Sheffield 1985 Influence of dietary fat levels on development and hormone responsiveness of the mouse mammary gland Cancer Res 45 12 Pt 1 6147 6154 4063968
96. K Sejrsen S Purup M Vestergaard J Foldager 2000 High body weight gain and reduced bovine mammary growth: physiological basis and implications for milk yield potential Domest Anim Endocrinol 19 2 93 104 11025189
97. MJ Meyer AV Capuco DA Ross LM Lintault ME Van Amburgh 2006 Developmental and nutritional regulation of the prepubertal bovine mammary gland: II. Epithelial cell proliferation, parenchymal accretion rate, and allometric growth J Dairy Sci 89 11 4298 4304 17033017
98. JC Beck HL Hosick 1988 Growth of mouse mammary epithelium in response to serum-free media conditioned by mammary adipose tissue Cell Biol Int Rep 12 2 85 97 3396081
99. GK Bandyopadhyay S Hwang W Imagawa S Nandi 1993 Role of polyunsaturated fatty acids as signal transducers: amplification of signals from growth factor receptors by fatty acids in mammary epithelial cells Prostaglandins Leukot Essent Fatty Acids 48 1 71 78 8424125
100. Pohlmeier WE, Hovey RC, Van Eenennaam AL. Reproductive abnormalities in mice expressing omega-3 fatty acid desaturase in their mammary glands. Transgenic Res.
101. M Peaker 1995 Endocrine signals from the mammary gland J Endocrinol 147 2 189 193 7490547
102. RA Clegg 1981 Lipoprotein lipase. Localization on plasma membrane fragments from lactating rat mammary tissue Biochim Biophys Acta 664 2 397 408 7248331
103. BK Levay-Young GK Bandyopadhyay S Nandi 1987 Linoleic acid, but not cortisol, stimulates accumulation of casein by mouse mammary epithelial cells in serum-free collagen gel culture Proc Natl Acad Sci USA 84 23 8448 8452 3317407
104. Pauloin A, Chat S, Pechoux C, Hue-Beauvais C, Droineau S, Galio L, et al. Oleate and linoleate stimulate degradation of beta-casein in prolactin-treated HC11 mouse mammary epithelial cells. Cell Tissue Res. 340(1):91-102.
105. SL Sigurdson MM Ip 1993 Casein accumulation by rat mammary epithelial cells grown within a reconstituted basement membrane is modulated by fatty acids in a hormone- and time-dependent manner Exp Cell Res 208 2 333 343 8375465
106. JF Levine FE Stockdale 1984 3T3-L1 adipocytes promote the growth of mammary epithelium Exp Cell Res 151 1 112 122 6698114
107. RC Hovey DD MacKenzie TB McFadden 1998 The proliferation of mouse mammary epithelial cells in response to specific mitogens is modulated by the mammary fat pad in vitro In Vitro Cell Dev Biol Anim 34 5 385 392 9639101
108. CA Carrington HL Hosick 1985 Effects of dietary fat on the growth of normal, preneoplastic and neoplastic mammary epithelial cells in vivo and in vitro J Cell Sci 75 269 278 4044677
109. Davidenko N, Campbell JJ, Thian ES, Watson CJ, Cameron RE. Collagen-hyaluronic acid scaffolds for adipose tissue engineering. Acta Biomater.
110. LJ Faulkin Jr KB Deome 1960 Regulation of growth and spacing of gland elements in the mammary fat pad of the C3H mouse J Natl Cancer Inst 24 953 969 13821714
111. SD Berry RD Howard PM Jobst H Jiang RM Akers 2003 Interactions between the ovary and the local IGF-I axis modulate mammary development in prepubertal heifers J Endocrinol 177 2 295 304 12740018
112. K Hoshino 1967 Transplantability of mammary gland in brown fat pads of mice Nature 213 5072 194 195 6030585
113. PB Blair RL Moretti 1967 The mammary fat pad as a privileged transplantation site Transplantation 5 3 542 544 5340357
114. FR Miller D Medina GH Heppner 1981 Preferential growth of mammary tumors in intact mammary fatpads Cancer Res 41 10 3863 3867 7284994
115. BE Elliott SP Tam D Dexter ZQ Chen 1992 Capacity of adipose tissue to promote growth and metastasis of a murine mammary carcinoma: effect of estrogen and progesterone Int J Cancer 51 3 416 424 1317363
116. CW Welsch DH O'Connor CF Aylsworth LG Sheffield 1987 Normal but not carcinomatous primary rat mammary epithelium: readily transplanted to and maintained in the athymic nude mouse J Natl Cancer Inst 78 3 557 565 3102827
117. DA Proia C Kuperwasser 2006 Reconstruction of human mammary tissues in a mouse model Nat Protoc 1 1 206 214 17406234
118. C Couldrey J Moitra C Vinson M Anver K Nagashima J Green 2002 Adipose tissue: a vital in vivo role in mammary gland development but not differentiation Dev Dyn 223 4 459 468 11921335
119. Landskroner-Eiger S, Park J, Israel D, Pollard JW, Scherer PE. Morphogenesis of the developing mammary gland: Stage-dependent impact of adipocytes. Dev Biol.
120. BW Booth CA Boulanger GH Smith 2008 Stem cells and the mammary microenvironment Breast Dis 29 57 67 19029625
121. YG Illouz A Sterodimas 2009 Autologous fat transplantation to the breast: a personal technique with 25 years of experience Aesthet Plast Surg 33 5 706 715
122. Mizuno H, Hyakusoku H. Fat grafting to the breast and adipose-derived stem cells: recent scientific consensus and controversy. Aesthet Surg J. 30(3):381-7.