The nipple: A simple intersection of mammary gland and integument, but focal point of organ function

Journal of Mammary Gland Biology and Neoplasia

Volumn 18, Issue 2, 2013, Pages 121-131

  Koyama, Sachiko ^a,b   Wu, Hsin Jung ^a   Easwaran, Teresa ^a   Thopady, Sunil ^c,d   Foley, John ^a,c  

^a Indiana University School of Medicine   (United States)

^b INDIANA UNIVERSITY   (United States)

^c INDIANA UNIVERSITY   (United States)

^d INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Areola; Breast cancer; Keratins; Lactation; Nipple

Indexed keywords

ANATOMICAL VARIATION; BREAST DEVELOPMENT; COW; HUMAN; INTEGUMENT; LACTATION; MAMMARY GLAND; MAMMARY GLAND FUNCTION; MARINE MAMMAL; MARSUPIAL; MONOTREMATE; MOUSE; NIPPLE; NONHUMAN; PLACENTAL MAMMALS; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; FEMALE; HUMANS; INTEGUMENTARY SYSTEM; LACTATION; MAMMARY GLANDS, ANIMAL; MAMMARY GLANDS, HUMAN; NIPPLES;

EID: 84879692685     PISSN: 10833021     EISSN: 15737039     Source Type: Journal    
DOI: 10.1007/s10911-013-9289-1     Document Type: Review

References (73)

1. Vorbach C, Capecchi MR, Penninger JM. Evolution of the mammary gland from the innate immune system? Bioessays. 2006;28:606-16.
2. McClellan HL, Miller SJ, Hartmann PE. Evolution of lactation: nutrition v. protection with special reference to five mammalian species. Nutr Res Rev. 2008;21:97-116.
3. Nowak R. Suckling, milk, and the development of preferences toward maternal cues by neonates: from early learning to filial attachment? In: Brockmann HJ, Slater PJB, Snowdon CT, editors. Advances in the Study of Behavior. San Diego: Academic Press; 2006. p. 1-58.
4. Schaal B. Mammary odor cues and pheromones" mammalian infant-directed communication about maternal state, mammae, and milk. Vitam Horm. 2010;83:83-136.
5. Logan EW, Brunet LJ, Webb WR, Cutforth T, Ngai J, Stowers L. Learned Recognition of maternal signature odors mediates the first suckling episode in mice. Curr Biol. 2012;22:1998-2007.
6. Pedersen CA. Biological aspects of social bonding and the roots of human violence. Ann NY Acad Sci. 2004;1036:106-27.
7. Moriceau S, Sullivan RM. Neurobiology of infant attachment. Dev Psychobiol. 2005;47:230-42.
8. Peaker M. The mammary gland in mammalian evolution: a brief commentary on some of the concepts. J Mammary Gland Biol Neoplasia. 2002;7(3):347-53.
9. Oftedal OT. The origin of lactation as a water source for parchment-shelled eggs. J Mammary Gland Biol Neoplasia. 2002;253-66.
10. Griffiths M, McIntosh DL, Coles REA. 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. 1969;158:371-86.
11. Findley L. The mammary glands of the tammar wallaby (Macropus eugenii) during pregnancy and lactation. J Reprod Fert. 1982;65(1):59-66.
12. Brennan AJ, Sharp JA, Digby MR, Nicholas KR. The tammar wallaby: A model system to examine endocrine and local control of lactation. IUBMB Life. 2007;59(3):146-50.
13. Martinet J, Development of the mammary gland. In: Martinet J, Houdebine, LM, Head, HH editors. Biology of lactation Paris: Institut national de la recherche agronomique 1999: 347-60.
14. Bocharev V and Cotsarelis G. Biology of Hair folicles. In: Goldsmith,L.A, Katz, SI, Gilchrest, BA, Paller, AS, Leffell DJ, Wolff K, editors Fitzpatrick's Dermatology in General Medicine Hew York: McGraw-Hill; 2012 (web edition).
15. Veltmaat JM, Mailleux AA, Theiry JP, Bellusci S. Mouse embryonic mammogenesis as a model for the molecular regulation of pattern formation. Differentiation. 2003;71:1-17.
16. Duverger, O and Morasso, MI. Epidermal patterning and induction of different hair types during mouse embryonic development
17. Shoda Y. Animals made by Humans - Evolution as Domesticated Animals. Tokyo: Tokyo Shoseki; 1987.
18. Napier JR, Napier PH. The Natural History of the Primates. Cambridge: MIT Press; 1985.
19. Slijper E. Functional morphology of the reproductive system in Cetacea. In: Norris KS, editor. Whales, Dolphins, and porpoises. Berkeley and Los Angeles: Univ Calfornia Press; 1966. p. 278-319.
20. Neville MC, Morton J. Physiology and endocrine changes underlying human lactogenesis II. J Nutr. 2001;131:3005S-8S.
21. Kuzbari R, Schlenz I. Reduction mammaplasty and sensitivity of the nipple-areola complex: sensuality versus sexuality? Ann Plast Surg. 2007;58:3-11.
22. Blass EM, Teicher MH. Suckling. Science. 1980;210:15-22.
23. Svennersten-Sjaunja K, Olsson K. Endocrinology of milk production. Domest Anim Endocrinol. 2005;29:241-58.
24. Algers B. Nursing in pigs: communicating needs and distributing resources. J Anim Sci. 1993;71:2826-31.
25. Foley J, Dann P, Hong J, Cosgrove J, Dreyer B, Rimm D, et al. Parathyroid hormone-related protein maintains mammary epithelial fate and triggers nipple skin differentiation during embryonic breast development. Development. 2001;128:513-25.
26. Giacometti L, Montagna W. The nipple and the areola of the human female breast. Anat Rec. 1962;144:191-97.
27. Montagna W. Histology and cytochemistry of human skin. XXXV: the nipple and areola. Br J Dermatol. 1970;83:2-13.
28. Helmboldt C, Jungherr EL, Plastridge WN. The Histophatology of Bovine Mastitis. Storrs Agricultural Experiment Station Paper. 1953;45:1-90. http://digitalcommons.uconn.edu/saes/45.
29. Ambrose N, Lloyd D, Maillard JC. Immune responses to Dermatophilus congolensis infections. Parasitol Today. 1999;15:295-300.
30. 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.
31. Abdalkhani A, Sellers R, Gent J, Wulitich H, Childress S, Stein B, et al. Nipple connective tissue and its development: insights from the K14-PTHrP mouse. Mech Dev. 2002;115:63-77.
32. Araco A, Araco F, Sorge R, Gravante G. Sensitivity of the nipple-areola complex and areolar pain following aesthetic breast augmentation in a retrospective series of 1200 patients: periareolar versus submammary incision. Plast Reconstr Surg. 2011;128:984-89.
33. Kobayashi T, Kronenberg HM, Foley J. Reduced expression of the PTH/PTHrP receptor during development of the mammary gland influences the function of the nipple during lactation. Dev Dyn. 2005;233:794-803.
34. Mahler B, Gocken T, Grojan M, Childress S, Spandau DF, Foley J. Keratin 2e: a marker for murine nipple epidermis. Cells Tissues Organs. 2004;176:169-77.
35. Eastwood J, Offutt C, Menon K, Keel M, Hrncirova P, Novotny MV, et al. Identification of markers for nipple epidermis: changes in expression during pregnancy and lactation. Differentiation. 2007;75:75-83.
36. Doucet S, Soussignan R, Sagot P, Schaal B. An overlooked aspect of the human breast: areolar glands in relation with breastfeeding pattern, neonatal weight gain, and the dynamics of lactation. Early Hum Dev. 2012;88:119-28.
37. Schaal B, Doucet S, Sagot P, Hertling E, Soussignan R. Human breast areolae as scent organs: morphological data and possible involvement in maternal-neonatal coadaptation. Dev Psychobiol. 2006;48:100-10.
38. Melo AI, Gonzalez-Mariscal G. Communication by olfactory signals in rabbits: its role in reproduction. Vitam Horm. 2010;83:351-71.
39. Schaal B, Coureaud G, Langlois D, Giniès C, Sémon E, Perrier G. Chemical and behavioural characterization of the rabbit mammary pheromone. Nature. 2003;424:68-72.
40. Gruet P, Maincent P, Berthelot X, Kaltsatos V. Bovine mastitis and intramammary drug delivery: review and perspectives. Adv Drug Deliv Rev. 2001;50:245-59.
41. Toker C. Clear cells of the nipple epidermis. Cancer. 1970;25:601-10.
42. Lundquist K, Kohler S, Rouse RV. Intraepidermal cytokeratin seven expression is not restricted to Paget cells but is also seen in Toker cells and Merkel cells. Am J Surg Pathol. 1999;23:212-19.
43. Nofech-Mozes S, Hanna W. Toker cells revisited. Breast J. 2009;15:394-98.
44. Seetharam S, Fentiman IS. Paget's disease of the nipple. Womens Health (Lond Engl). 2009;5:397-402.
45. Willman JH, Golitz LE, Fitzpatrick JE. Clear cells of Toker in accessory nipples. J Cutan Pathol. 2003;30:256-60.
46. Mackenzie IC, Hill MW. Connective tissue influences on patterns of epithelial architecture and keratinization in skin and oral mucosa of the adult mouse. Cell Tissue Res. 1984;235:551-59.
47. Schweizer J. Murine epidermal keratins. In: Darmon M, Blumenberg ML, editors. Molecular Biology of the Skin: the keratinocyte. Amsterdam: Academic Press; 1993. p. 33-78.
48. Dhouailly D, Prin F, Kanzler B, Viallet J. Variations of cutaneous appendages: regional specification and cross-species signals. In: Chuong C-M, editor. Molecular Basis of Epithelial Appendage Morphogenesis. Georgetown: RG Landes; 1988. p. 44-55.
49. Sengel P. Morphogenesis of Skin. Cambridge: Cambridge University Press; 1976.
50. Rinn JL, Wang JK, Allen N, Brugmann SA, Mikels AJ, Liu H, et al. A dermal HOX transcriptional program regulates site-specific epidermal fate. Genes Dev. 2008;22:303-07.
51. Cowin P, Wysolmerski J. Molecular mechanisms guiding embryonic mammary gland development. Cold Spring Harb Perspect Biol. 2010; Jun:2(6):a003251.
52. Wysolmerski JJ, Philbrick WM, Dunbar ME, Lanske B, Kronenberg H, Broadus AE. Rescue of the parathyroid hormone-related protein knockout mouse demonstrates that parathyroid hormone-related protein is essential for mammary gland development. Development. 1998;125:1285-94.
53. Hens JR, Dann P, Zhang JP, Harris S, Robinson GW, Wysolmerski J. BMP4 and PTHrP interact to stimulate ductal outgrowth during embryonic mammary development and to inhibit hair follicle induction. Development. 2007;134:1221-30.
54. Dunbar ME, Dann PR, Robinson GW, Hennighausen L, Zhang JP, Wysolmerski JJ. Parathyroid hormone-related protein signaling is necessary for sexual dimorphism during embryonic mammary development. Development. 1999;126:3485-93.
55. Toyoshima Y, Ohsako S, Nagano R, Matsumoto M, Hidaka S, Nishinakagawa H. Histological changes in mouse nipple tissue during the reproductive cycle. J Vet Med Sci. 1998;60:405-11.
56. Toyoshima Y, Ohsako S, Matsumoto M, Hidaka S, Nishinakagawa H. Histological and morphometrical studies on the rat nipple during the reproductive cycle. Exp Anim. 1998;47:29-36.
57. Kuenzi MJ, Connolly BA, Sherwood OD. Relaxin acts directly on rat mammary nipples to stimulate their growth. Endocrinology. 1995;136:2943-47.
58. Zhao L, Roche PJ, Gunnersen JM, Hammond VE, Tregear GW, Wintour EM, et al. Mice without a functional relaxin gene are unable to deliver milk to their pups. Endocrinology. 1999;140:445-53.
59. Wysolmerski J, Broadus A, Zhou J, Fuchs E, Milstone L, Philbrick W. Overexpression of parathyroid hormone-related protein in the skin of transgenic mice interferes with hair follicle development. Proc Natl Acad Sci USA. 1994;91:1133-37.
60. Wysolmerski JJ. Parathyroid hormone-related protein: an update. J Clin Endocrinol Metab. 2012;97:2947-56.
61. Cho YM, Woodard GL, Dunbar M, Gocken T, Jimènez JA, Foley J. Hair-cycle-dependent expression of parathyroid hormone-related protein and its type I receptor: evidence for regulation at the anagen to catagen transition. J Invest Dermatol. 2003;120:715-27.
62. Dunbar ME, Young P, McCaughern-Carucci J, Lanske B, Orioff JJ, et al. Stromal cells are critical targets in the regulation of mammary ductal morphogenesis by parathyroid hormone-related protein. Dev Biol. 1998;203:75-89.
63. Lee K, Deeds JD, Segre GV. Expression of parathyroid hormone-related peptide and its receptor messenger ribonucleic acids during fetal development of rats. Endocrinology. 1995;136:453-63.
64. Foley J, Longely BJ, Wysolmerski JJ, Dreyer BE, Broadus AE, Philbrick WM. PTHrP regulates epidermal differentiation in adult mice. J Invest Dermatol. 1998;111:1122-28.
65. Hiremath M, Dann P, Fischer J, Butterworth D, Boras-Granic K, Hens J, et al. Parathyroid hormone-related protein activates Wnt signaling to specify the embryonic mammary mesenchyme. Development. 2012;139:4239-49.
66. Chan GK, Miao D, Deckelbaum R, Bolivar I, Karaplis A, Goltzman D. Parathyroid hormone-related peptide interacts with bone morphogenetic protein 2 to increase osteoblastogenesis and decrease adipogenesis in pluripotent C3H10T 1/2 mesenchymal cells. Endocrinology. 2003;144:5511-20.
67. Mayer J, Foley J, De La Cruz D, Chuong C, Widelitz R. Converstion of the nipple to hair-bearing epithlia by lowering bone morphogenetic protein pathway activity at the dermal-epidermal interface. Am J Pathol. 2008;173:1339-48.
68. Jiang TX, Jung HS, Widelitz RB, Chuong CM. Self-organization of periodic patterns by dissociated feather mesenchymal cells and the regulation of size, number and spacing of primordia. Development. 1999;126:4997-5009.
69. Kandyba E, Leung Y, Chen YB, Widelitz R, Chuong CM, Kobielak K. Competitive balance of intrabulge BMP/Wnt signaling reveals a robust gene network ruling stem cell homeostasis and cyclic activation. Proc Natl Acad Sci USA. 2013;110:1351-56.
70. Plikus MV, Widelitz RB, Maxon R, Chuong CM. Analyses of regenerative wave patterns in adult hair follicle populations reveal macro-environmental regulation of stem cell activity. Int J Dev Biol. 2009;53:857-68.
71. Greco V, Chen T, Rendl M, Schober M, Pasolli HA, Dela Cruz-Pacelis J, et al. A two-step mechanism for stem cell activation during hair regeneration. Cell Stem Cell. 2009;4:155-69.
72. Griffiths M. Tachyglossidae. In: Walton DW, Richardson BJ, editors. Fauna of Australia -Vol. 1B- Mammalia. Canberra: Australian Government Publishing Service; 1989; Ch. 15:1-58.
73. Griffiths M, Elliott MA, Leckie RMC, Schoefl GI. Observations of the comparative anatomy and ultrastructure of mammary gland and on the fatty acids of the triglycerides in platypus and echidna milk fats. J Zool Lond. 1973;169:255-79.