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01-08-2002 | Review

Requirement of macrophages and eosinophils and their cytokines/chemokines for mammary gland development

Authors: Valérie Gouon-Evans, Elaine Y Lin, Jeffrey W Pollard

Published in: Breast Cancer Research | Issue 4/2002

Abstract

Epithelial/mesenchymal cell interactions are necessary for proper ductal morphogenesis throughout all stages of mammary gland development. Besides the well-established stromal components, such as adipocytes and fibroblasts, the mammary stroma is also infiltrated with migrating blood cells, mostly macrophages and eosinophils. The focus of this review is on the role of macrophages and their growth factor colony-stimulating factor 1 (CSF-1) in promoting branching morphogenesis during postnatal mammary gland development through to lactation. The more restricted role of eosinophils and their chemoattractant eotaxin during pubertal ductal morphogenesis is also discussed. A possible interaction between macrophages and eosinophils in ductal morphogenesis is considered, along with the roles of other chemokines. This role of macrophages in normal development also appears to be subverted by tumors of the mammary gland to promote the escape of the tumor cells from the local environment and enhance their rate of metastasis. These data emphasize the dual role of macrophages in the promotion of epithelial growth in normal and cancer states.

Robinson GW, Karpf AB, Kratochwil K: Regulation of mammary gland development by tissue interaction. J Mammary Gland Biol Neoplasia. 1999, 4: 9-19. 10.1023/A:1018748418447.PubMedCrossRef

Sakakura T, Sakagami Y, Nishizuka Y: Dual origin of mesenchymal tissues participating in mouse mammary gland embryogenesis. Dev Biol. 1982, 91: 202-207.PubMedCrossRef

Enami J, Enami S, Koga M: Growth of normal and neoplastic mouse mammary epithelial cells in primary culture: stimulation by conditioned medium from mouse mammary fibroblasts. Gann. 1983, 74: 845-853.PubMed

Levine JF, Stockdale FE: 3T3-L1 adipocytes promote the growth of mammary epithelium. Exp Cell Res. 1984, 151: 112-122.PubMedCrossRef

Carrington CA, Hosick HL: Effects of dietary fat on the growth of normal, preneoplastic and neoplastic mammary epithelial cells in vivo and in vitro. J Cell Sci. 1985, 75: 269-278.PubMed

Berdichevsky F, Alford D, D'Souza B, Taylor-Papadimitriou J: Branching morphogenesis of human mammary epithelial cells in collagen gels. J Cell Sci. 1994, 107: 3557-3568.PubMed

Gouon-Evans V, Rothenberg ME, Pollard JW: Postnatal mammary gland development requires macrophages and eosinophils. Development. 2000, 127: 2269-2282.PubMed

Silberstein GB: Tumour-stromal interactions. Role of the stroma in mammary development. Breast Cancer Res. 2001, 3: 218-223. 10.1186/bcr299.PubMedPubMedCentralCrossRef

McKnight AJ, Macfarlane AJ, Dri P, Turley L, Willis AC, Gordon S: Molecular cloning of F4/80, a murine macrophage-restricted cell surface glycoprotein with homology to the G-protein-linked transmembrane 7 hormone receptor family. J Biol Chem. 1996, 271: 486-489. 10.1074/jbc.271.50.31869.PubMedCrossRef

10.

Szewczyk G, Szukiewicz D, Zaczek R, Maslinska D: Mast cells in the mouse mammary gland-correlation with the development of lactiferous structures. Folia Biol. 2000, 48: 13-17.

11.

Outteridge PM, Lee CS: Cellular immunity in the mammary gland with particular reference to T, B lymphocytes and macrophages. Adv Exp Med Biol. 1981, 137: 513-534.PubMed

12.

Lee CS, Outteridge PM: Leucocytes of sheep colostrum, milk and involution secretion, with particular reference to ultra-structure and lymphocyte sub-populations. J Dairy Res. 1981, 48: 225-237.PubMedCrossRef

13.

Hara T, Irie K, Saito S, Ichijo M, Yamada M, Yanai N, Miyazaki S: Identification of macrophage colony-stimulating factor in human milk and mammary gland epithelial cells. Pediatr Res. 1995, 37: 437-443.PubMedCrossRef

14.

Riollet C, Rainard P, Poutrel B: Cells and cytokines in inflammatory secretions of bovine mammary gland. Adv Exp Med Biol. 2000, 480: 247-258.PubMedCrossRef

15.

Roux ME, McWilliams M, Phillips-Quagliata JM, Weisz-Carrington P, Lamm ME: Origin of IgA-secreting plasma cells in the mammary gland. J Exp Med. 1977, 146: 1311-1322.PubMedCrossRef

16.

Goldman AS, Chheda S, Garofalo R, Schmalstieg FC: Cytokines in human milk: properties and potential effects upon the mammary gland and the neonate. J Mammary Gland Biol Neoplasia. 1996, 1: 251-258.PubMedCrossRef

17.

Wagstrom EA, Yoon KJ, Zimmerman JJ: Immune components in porcine mammary secretions. Viral Immunol. 2000, 13: 383-397. 10.1089/08828240050144699.PubMedCrossRef

18.

Hanson LA: The mother-offspring dyad and the immune system. Acta Paediatr. 2000, 89: 252-258. 10.1080/080352500750028339.PubMedCrossRef

19.

van der Feltz MJ, de Groot N, Bayley JP, Lee SH, Verbeet MP, de Boer HA: Lymphocyte homing and Ig secretion in the murine mammary gland. Scand J Immunol. 2001, 54: 292-300. 10.1046/j.1365-3083.2001.00933.x.PubMedCrossRef

20.

Lee CS, McCauley I, Hartmann PE: Light and electron microscopy of cells in pig colostrum, milk and involution secretion. Acta Anat. 1983, 116: 126-135.PubMedCrossRef

21.

Colditz IG: Studies on the inflammatory response during involution of the ovine mammary gland. Q J Exp Physiol. 1988, 73: 363-368.PubMedCrossRef

22.

Tatarczuch L, Philip C, Bischof R, Lee CS: Leucocyte phenotypes in involuting and fully involuted mammary glandular tissues and secretions of sheep. J Anat. 2000, 196: 313-326. 10.1017/S0021878299006147.PubMedPubMedCentralCrossRef

23.

Sordillo LM, Shafer-Weaver K, DeRosa D: Immunobiology of the mammary gland. J Dairy Sci. 1997, 80: 1851-1865.PubMedCrossRef

24.

Paape MJ, Shafer-Weaver K, Capuco AV, Van Oostveldt K, Burvenich C: Immune surveillance of mammary tissue by phagocytic cells. Adv Exp Med Biol. 2000, 480: 259-277.PubMedCrossRef

25.

Stanley ER, Guilbert LJ, Tushinski RJ, Bartelmez SH: CSF-1 a mononuclear phagocyte lineage-specific hemopoietic growth factor. J Cell Biochem. 1983, 21: 151-159.PubMedCrossRef

26.

Tushinski RJ, Stanley ER: The regulation of macrophage protein turnover by a colony stimulating factor (CSF-1). J Cell Physiol. 1983, 116: 67-75.PubMedCrossRef

27.

Roth P, Stanley ER: The biology of CSF-1 and its receptor. Curr Top Microbiol Immunol. 1992, 181: 141-167.PubMed

28.

Tushinski RJ, Oliver IT, Guilbert LJ, Tynan PW, Warner JR, Stanley ER: Survival of mononuclear phagocytes depends on a lineage-specific growth factor that the differentiated cells selectively destroy. Cell. 1982, 28: 71-81.PubMedCrossRef

29.

Pollard JW: Role of colony-stimulating factor-1 in reproduction and development. Mol Reprod Dev. 1997, 46: 54-60. 10.1002/(SICI)1098-2795(199701)46:1<54::AID-MRD9>3.0.CO;2-Q.PubMedCrossRef

30.

Sherr CJ, Rettenmier CW, Sacca R, Roussel MF, Look AT, Stanley ER: The c-fms proto-oncogene product is related to the receptor for the mononuclear phagocyte growth factor, CSF-1. Cell. 1985, 41: 665-676.PubMedCrossRef

31.

Li W, Stanley ER: Role of dimerization and modification of the CSF-1 receptor in its activation and internalization during the CSF-1 response. EMBO J. 1991, 10: 277-288.PubMedPubMedCentral

32.

Rohrschneider LR, Bourette RP, Lioubin MN, Algate PA, Myles GM, Carlberg K: Growth and differentiation signals regulated by the M-CSF receptor. Mol Reprod Dev. 1997, 46: 96-103. 10.1002/(SICI)1098-2795(199701)46:1<96::AID-MRD15>3.0.CO;2-1.PubMedCrossRef

33.

Pixley FJ, Lee PS, Condeelis JS, Stanley ER: Protein tyrosine phosphatase phi regulates paxillin tyrosine phosphorylation and mediates colony-stimulating factor 1-induced morphological changes in macrophages. Mol Cell Biol. 2001, 21: 1795-1809. 10.1128/MCB.21.5.1795-1809.2001.PubMedPubMedCentralCrossRef

34.

Wiktor-Jedrzejczak W, Bartocci A, Ferrante AW, Ahmed-Ansari A, Sell KW, Pollard JW, Stanley ER: Total absence of colony-stimulating factor 1 in the macrophage-deficient osteopetrotic (op/op) mouse. Proc Natl Acad Sci USA. 1990, 87: 4828-4832.PubMedPubMedCentralCrossRef

35.

Yoshida H, Hayashi S, Kunisada T, Ogawa M, Nishikawa S, Okamura H, Sudo T, Shultz LD: The murine mutation osteopetrosis is in the coding region of the macrophage colony stimulating factor gene. Nature. 1990, 345: 442-444. 10.1038/345442a0.PubMedCrossRef

36.

Pollard JW, Stanley ER: Pleiotropic roles for CSF-1 in development defined by the mouse mutation osteopetrotic (op). Advances in Developmental Biochemistry. 1996, 4: 153-193.CrossRef

37.

Dai XM, Ryan GR, Hapel AJ, Dominguez MG, Russell RG, Kapp S, Sylvestre V, Stanley ER: Targeted disruption of the mouse colony-stimulating factor 1 receptor gene results in osteopetrosis, mononuclear phagocyte deficiency, increased primitive progenitor cell frequencies, and reproductive defects. Blood. 2002, 99: 111-120. 10.1182/blood.V99.1.111.PubMedCrossRef

38.

Pollard JW, Hennighausen L: Colony stimulating factor 1 is required for mammary gland development during pregnancy. Proc Natl Acad Sci USA. 1994, 91: 9312-9316.PubMedPubMedCentralCrossRef

39.

Cohen PE, Zhu L, Nishimura K, Pollard JW: Colony-stimulating factor 1 regulation of neuroendocrine pathways that control gonadal function in mice. Endocrinology. 2002, 143: 1413-1422. 10.1210/en.143.4.1413.PubMedCrossRef

40.

Nguyen AV, Pollard JW: Colony stimulating factor-1 is required to recruit macrophages into the mammary gland to facilitate mammary ductal outgrowth. Dev Biol. 2002, 247: 11-25. 10.1006/dbio.2002.0669.PubMedCrossRef

41.

Ryan GR, Dai XM, Dominguez MG, Tong W, Chuan F, Chisholm O, Russell RG, Pollard JW, Stanley ER: Rescue of the colony-stimulating factor 1 (CSF-1)-nullizygous mouse (Csf1 ^op/Csf1 ^op) phenotype with a CSF-1 transgene and identification of sites of local CSF-1 synthesis. Blood. 2001, 98: 74-84. 10.1182/blood.V98.1.74.PubMedCrossRef

42.

Kacinski BM: CSF-1 and its receptor in breast carcinomas and neoplasms of the female reproductive tract. Mol Reprod Dev. 1997, 46: 71-74. 10.1002/(SICI)1098-2795(199701)46:1<71::AID-MRD11>3.3.CO;2-M.PubMedCrossRef

43.

Sapi E, Flick MB, Rodov S, Carter D, Kacinski BM: Expression of CSF-I and CSF-I receptor by normal lactating mammary epithelial cells. J Soc Gynecol Invest. 1998, 5: 94-101. 10.1016/S1071-5576(97)00108-1.CrossRef

44.

Kacinski BM, Scata KA, Carter D, Yee LD, Sapi E, King BL, Chambers SK, Jones MA, Pirro MH, Stanley ER, Rohrschneider LR: FMS (CSF-1 receptor) and CSF-1 transcripts and protein are expressed by human breast carcinomas in vivo and in vitro. Oncogene. 1991, 6: 941-952.PubMed

45.

Welgus HG, Senior RM, Parks WC, Kahn AJ, Ley TJ, Shapiro SD, Campbell EJ: Neutral proteinase expression by human mononuclear phagocytes: a prominent role of cellular differentiation. Matrix Suppl. 1992, 1: 363-367.PubMed

46.

Blood Cell Biochemistry, Macrophages and Related Cells. Edited by: Horton MA. 1996, New York: Plenum Press, 5: 5th

47.

Polverini PJ: Role of the macrophage in angiogenesis-dependent diseases. EXS. 1997, 79: 11-28.PubMed

48.

Hogg NA, Harrison CJ, Tickle C: Lumen formation in the developing mouse mammary gland. J Embryol Exp Morphol. 1983, 73: 39-57.PubMed

49.

Humphreys RC, Krajewska M, Krnacik S, Jaeger R, Weiher H, Krajewski S, Reed JC, Rosen JM: Apoptosis in the terminal endbud of the murine mammary gland: a mechanism of ductal morphogenesis. Development. 1996, 122: 4013-4022.PubMed

50.

Sapi E, Kacinski BM: The role of CSF-1 in normal and neoplastic breast physiology. Proc Soc Exp Biol Med. 1999, 220: 1-8. 10.1046/j.1525-1373.1999.d01-1.x.PubMedCrossRef

51.

Lin EY, Gouon-Evans V, Nguyen AV, Pollard JW: The macrophage growth factor, CSF-1, in mammary gland development and tumor progression. J Mammary Gland Biol Neoplasia. 2002,

52.

O'Sullivan C, Lewis CE: Tumour-associated leucocytes: friends or foes in breast carcinoma. J Pathol. 1994, 172: 229-235.PubMedCrossRef

53.

Elgert KD, Alleva DG, Mullins DW: Tumor-induced immune dysfunction: the macrophage connection. J Leukoc Biol. 1998, 64: 275-290.PubMed

54.

Bingle L, Brown NJ, Lewis CE: The role of tumour-associated macrophages in tumour progression: implications for new anticancer therapies. J Pathol. 2002, 196: 254-265. 10.1002/path.1027.PubMedCrossRef

55.

Mantovani A, Bottazzi B, Colotta F, Sozzani S, Ruco L: The origin and function of tumor-associated macrophages. Immunol Today. 1992, 13: 265-270. 10.1016/0167-5699(92)90008-U.PubMedCrossRef

56.

Scholl SM, Pallud C, Beuvon F, Hacene K, Stanley ER, Rohrschneider L, Tang R, Pouillart P, Lidereau R: Anti-colony-stimulating factor-1 antibody staining in primary breast adenocarcinomas correlates with marked inflammatory cell infiltrates and prognosis. J Natl Cancer Inst. 1994, 86: 120-126.PubMedCrossRef

57.

Leek RD, Lewis CE, Whitehouse R, Greenall M, Clarke J, Harris AL: Association of macrophage infiltration with angiogenesis and prognosis in invasive breast carcinoma. Cancer Res. 1996, 56: 4625-4629.PubMed

58.

Leek RD, Harris AL: Tumour associated macrophages in breast cancer. J Mammary Gland Biol Neoplasia. 2002,

59.

Lin EY, Nguyen AV, Russell RG, Pollard JW: Colony-stimulating factor 1 promotes progression of mammary tumors to malignancy. J Exp Med. 2001, 193: 727-740. 10.1084/jem.193.6.727.PubMedPubMedCentralCrossRef

60.

Crowther M, Brown NJ, Bishop ET, Lewis CE: Microenvironmental influence on macrophage regulation of angiogenesis in wounds and malignant tumors. J Leukoc Biol. 2001, 70: 478-490.PubMed

61.

Garcia-Zepeda EA, Rothenberg ME, Ownbey RT, Celestin J, Leder P, Luster AD: Human eotaxin is a specific chemoattractant for eosinophil cells and provides a new mechanism to explain tissue eosinophilia. Nat Med. 1996, 2: 449-456.PubMedCrossRef

62.

Sabroe I, Hartnell A, Jopling LA, Bel S, Ponath PD, Pease JE, Collins PD, Williams TJ: Differential regulation of eosinophil chemokine signaling via CCR3 and non-CCR3 pathways. J Immunol. 1999, 162: 2946-2955.PubMed

63.

Ganzalo JA, Jia GQ, Aguirre V, Friend D, Coyle AJ, Jenkins NA, Lin GS, Katz H, Lichtman A, Copeland N, Kopf M, Gutierrez-Ramos JC: Mouse eotaxin expression parallels eosinophil accumulation during lung allergic inflammation but it is not restricted to a Th2-type response. Immunity. 1996, 4: 1-14.PubMedCrossRef

64.

Baggiolini M, Dewald B, Moser B: Human chemokines: an update. Annu Rev Immunol. 1997, 15: 675-705. 10.1146/annurev.immunol.15.1.675.PubMedCrossRef

65.

Rothenberg ME, MacLean JA, Pearlman E, Luster AD, Leder P: Targeted disruption of the chemokine eotaxin partially reduces antigen-induced tissue eosinophilia. J Exp Med. 1997, 185: 785-790. 10.1084/jem.185.4.785.PubMedPubMedCentralCrossRef

66.

Palframan RT, Collins PD, Williams TJ, Rankin SM: Eotaxin induces a rapid release of eosinophils and their progenitors from the bone marrow. Blood. 1998, 91: 2240-2248.PubMed

67.

Matthews AN, Friend DS, Zimmermann N, Sarafi MN, Luster AD, Pearlman E, Wert SE, Rothenberg ME: Eotaxin is required for the baseline level of tissue eosinophils. Proc Natl Acad Sci USA. 1998, 95: 6273-6278. 10.1073/pnas.95.11.6273.PubMedPubMedCentralCrossRef

68.

Rothenberg ME, Luster AD, Leder P: Murine eotaxin: an eosinophil chemoattractant inducible in endothelial cells and in interleukin 4-induced tumor suppression. Proc Natl Acad Sci USA. 1995, 92: 8960-8964.PubMedPubMedCentralCrossRef

69.

Mishra A, Hogan SP, Lee JJ, Foster PS, Rothenberg ME: Fundamental signals that regulate eosinophil homing to the gastrointestinal tract. Clin Invest. 1999, 103: 1719-1727.CrossRef

70.

Sanderson CJ: Interleukin-5, eosinophils, and disease. Blood. 1992, 79: 3101-3109.PubMed

71.

Gleich GJ, Adolphson CR: The eosinophilic leukocyte: structure and function. Adv Immunol. 1986, 39: 177-253.PubMedCrossRef

72.

Rothenberg ME: Eosinophilia. N Engl J Med. 1998, 338: 1592-1600. 10.1056/NEJM199805283382206.PubMedCrossRef

73.

Gouon-Evans V, Pollard JW: Eotaxin is required for eosinophil homing into the stroma of the pubertal and cycling uterus. Endocrinology. 2001, 142: 4515-4521. 10.1210/en.142.10.4515.PubMedCrossRef

74.

Uguccioni M, Mackay CR, Ochensberger B, Loetscher P, Rhis S, LaRosa GJ, Rao P, Ponath PD, Baggiolini M, Dahinden CA: High expression of the chemokine receptor CCR3 in human blood basophils. Role in activation by eotaxin, MCP-4, and other chemokines. J Clin Invest. 1997, 100: 1137-1143.PubMedPubMedCentralCrossRef

75.

Yamada H, Hirai K, Miyamasu M, Iikura M, Misaki Y, Shoji S, Takaishi T, Kasahara T, Morita Y, Ito K: Eotaxin is a potent chemotaxin for human basophils. Biochem Biophys Res Commun. 1997, 231: 365-368. 10.1006/bbrc.1997.6100.PubMedCrossRef

76.

Sallusto F, Mackay CR, Lanzavecchia A: Selective expression of the eotaxin receptor CCR3 by human T helper 2 cells. Science. 1997, 277: 2005-2007. 10.1126/science.277.5334.2005.PubMedCrossRef

77.

Samoszuk M, Ramzi E: IgE, Reed-Sternberg cells, and eosinophilia in Hodgkin's disease. Leuk Lymphoma. 1993, 9: 315-319.PubMedCrossRef

78.

Iwasaki K, Torisu M, Fujimura T: Malignant tumor and eosinophils. I. Prognostic significance in gastric cancer. Cancer. 1986, 58: 1321-1327.PubMedCrossRef

79.

Fisher ER, Paik SM, Rockette H, Jones J, Caplan R, Fisher B: Prognostic significance of eosinophils and mast cells in rectal cancer: findings from the National Surgical Adjuvant Breast and Bowel Project (protocol R-01). Hum Pathol. 1989, 20: 159-163.PubMedCrossRef

80.

Goldsmith MM, Belchis DA, Cresson DH, Merritt WD, Askin FB: The importance of the eosinophil in head and neck cancer. Otolaryngol Head Neck Surg. 1992, 106: 27-33.PubMed

81.

van Driel WJ, Hogendoorn PC, Jansen FW, Zwinderman AH, Trimbos JB, Fleuren GJ: Tumor-associated eosinophilic infiltrate of cervical cancer is indicative for a less effective immune response. Hum Pathol. 1996, 27: 904-911.PubMedCrossRef

82.

Leighton SE, Teo JG, Leung SF, Cheung AY, Lee JC, van Hasselt CA: Prevalence and prognostic significance of tumor-associated tissue eosinophilia in nasopharyngeal carcinoma. Cancer. 1996, 77: 436-440. 10.1002/(SICI)1097-0142(19960201)77:3<436::AID-CNCR3>3.0.CO;2-I.PubMedCrossRef

83.

Samoszuk M: Eosinophils and human cancer. Histol Histopathol. 1997, 12: 807-812.PubMed

84.

Samoszuk MK, Nguyen V, Gluzman I, Pham JH: Occult deposition of eosinophil peroxidase in a subset of human breast carcinomas. Am J Pathol. 1996, 148: 701-706.PubMedPubMedCentral

85.

Samoszuk M, Lin F, Rim P, Strathearn G: New marker for blood vessels in human ovarian and endometrial cancers. Clin Cancer Res. 1996, 2: 1867-1871.PubMed

86.

Bethwaite PB, Holloway LJ, Yeong ML, Thornton A: Effect of tumour associated tissue eosinophilia on survival of women with stage IB carcinoma of the uterine cervix. J Clin Pathol. 1993, 46: 1016-1020.PubMedPubMedCentralCrossRef

87.

Ownby HE, Roi LD, Isenberg RR, Brennan MJ: Peripheral lymphocyte and eosinophil counts as indicators of prognosis in primary breast cancer. Cancer. 1983, 52: 126-130.PubMedCrossRef

88.

Berger MS, Taub DD, Orlofsky A, Kleyman TR, Coupaye-Gerard B, Eisner D, Cohen SA: The chemokine C10: immunological and functional analysis of the sequence encoded by the novel second exon. Cytokine. 1996, 8: 439-447. 10.1006/cyto.1996.0060.PubMedCrossRef

89.

Orlofsky A, Berger MS, Prystowsky MB: Novel expression pattern of a new member of the MIP-1 family of cytokine-like genes. Cell Regul. 1991, 2: 403-412.PubMedPubMedCentral

90.

Wu Y, Prystowsky MB, Orlofsky A: Sustained high-level production of murine chemokine C10 during chronic inflammation. Cytokine. 1999, 11: 523-530. 10.1006/cyto.1998.0436.PubMedCrossRef

91.

Wang W, Bacon KB, Oldham ER, Schall TJ: Molecular cloning and functional characterization of human MIP-1 delta, a new C-C chemokine related to mouse CCF-18 and C10. J Clin Immunol. 1998, 18: 214-222. 10.1023/A:1020535106684.PubMedCrossRef

92.

Hara T, Bacon KB, Cho LC, Yoshimura A, Morikawa Y, Copeland NG, Gilbert DJ, Jenkins NA, Schall TJ, Miyajima A: Molecular cloning and functional characterization of a novel member of the C-C chemokine family. J Immunol. 1995, 155: 5352-5358.PubMed

93.

Pardigol A, Forssmann U, Zucht HD, Loetscher P, Schulz-Knappe P, Baggiolini M, Forssmann WG, Magert HJ: HCC-2, a human chemokine: gene structure, expression pattern, and biological activity. Proc Natl Acad Sci USA. 1998, 95: 6308-6313. 10.1073/pnas.95.11.6308.PubMedPubMedCentralCrossRef

94.

Garofalo RP, Goldman AS: Cytokines, chemokines, and colony-stimulating factors in human milk: the 1997 update. Biol Neonate. 1998, 74: 134-142. 10.1159/000014019.PubMedCrossRef

95.

Basolo F, Conaldi PG, Fiore L, Calvo S, Toniolo A: Normal breast epithelial cells produce interleukins 6 and 8 together with tumor-necrosis factor: defective IL6 expression in mammary carcinoma. Int J Cancer. 1993, 55: 926-930.PubMedCrossRef

96.

Palkowetz KH, Royer CL, Garofalo R, Rudloff HE, Schmalstieg FC, Goldman AS: Production of interleukin-6 and inter-leukin-8 by human mammary gland epithelial cells. J Reprod Immunol. 1994, 26: 57-64. 10.1016/0165-0378(93)00867-S.PubMedCrossRef

97.

Basolo F, Fiore L, Calvo S, Falcone V, Conaldi PG, Fontanini G, Caligo AM, Merlo G, Gluzman Y, Toniolo A: Defective interleukin six expression and responsiveness in human mammary cells transformed by an adeno 5/SV40 hybrid virus. Br J Cancer. 1996, 73: 1356-1361.PubMedPubMedCentralCrossRef

98.

Locksley RM, Killeen N, Lenardo MJ: The TNF and TNF receptor superfamilies: integrating mammalian biology. Cell. 2001, 104: 487-501. 10.1016/S0092-8674(01)00237-9.PubMedCrossRef

99.

Theill LE, Boyle WJ, Penninger JM: RANK-L AND RANK: T cells, bone loss, and mammalian evolution. Annu Rev Immunol. 2002, 20: 795-823. 10.1146/annurev.immunol.20.100301.064753.PubMedCrossRef

100.

Fata JE, Kong YY, Li J, Sasaki T, Irie-Sasaki J, Moorehead RA, Elliott R, Scully S, Voura EB, Lacey DL, Voura EB, Lacey DL, Boyle WJ, Khokha R, Penninger JM: The osteoclast differentiation factor osteoprotegerin-ligand is essential for mammary gland development. Cell. 2000, 103: 41-50. 10.1016/S0092-8674(00)00103-3.PubMedCrossRef

101.

Stangle NC, Kollias G, Ip MM: Disrupted mammary gland development in TNFa knockout mice [abstract]. Proc Am Assoc Cancer Res. 1999, 40: 161-

102.

Ip MM, Shoemaker SF, Darcy KM: Regulation of rat mammary epithelial cell proliferation and differentiation by tumor necrosis factor-alpha. Endocrinology. 1992, 130: 2833-2844. 10.1210/en.130.5.2833.PubMed

103.

Varela LM, Ip MM: Tumor necrosis factor-alpha: a multifunc-tional regulator of mammary gland development. Endocrinology. 1996, 137: 4915-4924. 10.1210/en.137.11.4915.PubMed

104.

Nathan CF: Secretory products of macrophages. J Clin Invest. 1987, 79: 319-326.PubMedPubMedCentralCrossRef

105.

Mickanin CS, Bhatia U, Labow M: Identification of a novel beta-chemokine, MEC, down-regulated in primary breast tumors. Int J Oncol. 2001, 18: 939-944.PubMed

106.

Krop IE, Sgroi D, Porter DA, Lunetta KL, LeVangie R, Seth P, Kaelin CM, Rhei E, Bosenberg M, Schnitt S, Schnitt S, Marks JR, Pagon Z, Belina D, Razumovic J, Polyak K: HIN-1, a putative cytokine highly expressed in normal but not cancerous mammary epithelial cells. Proc Natl Acad Sci USA. 2001, 98: 9796-9801. 10.1073/pnas.171138398.PubMedPubMedCentralCrossRef

Title: Requirement of macrophages and eosinophils and their cytokines/chemokines for mammary gland development
Authors: Valérie Gouon-Evans
Elaine Y Lin
Jeffrey W Pollard
Publication date: 01-08-2002
Publisher: BioMed Central
Published in: Breast Cancer Research / Issue 4/2002
Electronic ISSN: 1465-542X
DOI: https://doi.org/10.1186/bcr441

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